Journal of Bodywork and Movement Therapies Official journal of the: ® Association of Neuromuscular Therapists, Ireland ® Australian Pilates Method Association ® Hands On Seminars, USA ® National Association of Myofascial Trigger Point Therapists, USA ® Pilates Foundation, UK Volume 15 Number 4 2011 EDITOR-IN-CHIEF
Leon Chaitow ND, DO
c/o School of Life Sciences, University of Westminster, 115 New Cavendish Street, London W1M 8JS, UK Preferred mailing address: P.O.Box 41, Corfu, Greece 49100 (
[email protected])
ASSOCIATE EDITORS Geoffrey M. Bove, DC, PhD Kennebunkport, ME, USA (
[email protected]) John Hannon DC San Luis Obispo, CA, USA (
[email protected]) Glenn M. Hymel EdD, LMT Department of Psychology, Loyola University, New Orleans, LA, USA (
[email protected])
Dimitrios Kostopoulos PT, MD, PhD, DSc Hands-on Physical Therapy, New York, NY, USA (
[email protected]) Craig Liebenson DC Los Angeles, CA, USA (
[email protected])
ASSOCIATE EDITORS: PREVENTION & REHABILITATION Warrick McNeill MCSP London, UK (
[email protected])
Matt Wallden MSc, Ost, Med, DO, ND London, UK (
[email protected])
International Advisory Board D. Beales MD (Cirencester, UK) C. Bron PhD MPT (Groningen, The Netherlands) I. Burman LMT (Miami, FL, USA) E. Calenda, RMT (Boulder, USA) J. Carleton PhD (New York, USA) F. P. Carpes PhD (Uruguaiana, RS, Brazil) Susan Chapelle (Squamish, Canada) Z. Comeaux DO FAAO (Lewisburg, WV, USA) P. Davies PhD (London, UK) J. P. DeLany LMT (St Petersburg, FL, USA) M. Diego PhD (Florida, USA) J. Dommerholt PT, MS, DPT, DAAPM (Bethesda, MD, USA) J. Downes DC (Marietta, GA, USA) C. Fernandez de las Peñas PT, DO, PhD (Madrid, Spain) T. M. Field PhD (Miami, FL, USA) P. Finch PhD (Toronto, ON, Canada) T. Findley MD, PhD (New Jersey, USA) D. D. FitzGerald DIP ENG, MISCP, MCSP (Dublin, Ireland) S. Fritz LMT (Lapeer, MI, USA)
G. Fryer PhD. BSc., (Osteopath), ND (Melbourne City, Australia) C. Gilbert PhD (San Francisco, USA) C. H. Goldsmith PhD (Hamilton, ON, Canada) S. Goossen BA LMT CMTPT (Jacksonville, FL, USA) S. Gracovetsky PhD (Ocracoke, NC, USA) M. Hernandez-Reif PhD (Tuscaloosa, AL, USA) P. Hodges BPhty, PhD, MedDr (Brisbane, Australia) B. Ingram-Rice OTRLMT (Sarasota, FL, USA) D. Jing-xing PhD, MD (Guangzhou, China) J. Kahn PhD (Burlington, VT, USA) R. Lardner PT (Chicago, IL, USA) P. J. M. Latey APMA (Sydney, Australia) E. Lederman DO PhD (London, UK) D. Lee BSR, FCAMT, CGIMS (Canada) D. Lewis ND (Seattle, WA, USA) W. W. Lowe LMT (Bend, OR, USA) J. McEvoy PT MSC DPT MISCP MCSP (Limerick, Ireland) L. McLaughlin DSc PT (Ontario, Canada) C. McMakin MA DC (Portland, OR, USA)
J. M. McPartland DO (Middleburg, VT, USA) C. Moyer PhD (Menomonie, WI, USA) D. R. Murphy DC (Providence, RI, USA) T. Myers LMT (Walpole, ME, USA) C. Norris MSc CBA MCSP SRP (Sale, UK) N. Osborne PhD DC (Bournemouth, UK) B. O’Neill MD (North Wales, PA, USA) J. L. Oschman PhD (Dover, NH, USA) D. Peters MB CHB DO (London, UK) M. M. Reinold PT, DPT, ATC, CSCS (Boston, MA, MD, USA) G. Rich PhD (Juneau, AK, USA) C. Rosenholtz MA, RMT (Boulder, CO, USA) R. Schleip PhD, MA, PT (Munich, Germany) J. Sharkey MSc, NMT (Dublin, Ireland) D. Thompson LMP (Seattle, WA, USA) C. Traole MCSP, SRP, MAACP (London, UK) P. W. Tunnell DC, DACRB (Ridgefield, CT, USA) E. Wilson BA MCSP SRP (York, UK) A. Vleeming PhD (Schoten, Belgium)
Officially recognised and supported by: The Alliance of Massage Therapy Education The American Massage Therapy Association Associated Bodywork and Massage Professionals The British Orthopaedic Association The Institute of Sport and Remedial massage The International Association of Structural Integrators The International College of Applied Kinesiology USA The International Society of Clinical Rehabilitation Specialists The New Zealand Manipulative Physiotherapists Association The Organisation of Chartered Physiotherapists in Private Practice The Rolf Institute The Sports Massage Association The Upledger Institute
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Journal of Bodywork & Movement Therapies (2011) 15, 395e396
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EDITORIAL
JBMTs new section with a fascial focus e Starting 2012 Previous editorials have emphasised the importance of the role of fascia in our attempts to better understand human function and dysfunction. In March 2012 the Third Fascia Research Congress, in Vancouver Canada, will once again bring together scientists and clinicians in a unique example of collaboration and enquiry across professional boundaries. http://www.fasciacongress.org/2012/. JBMT and its publisher, Elsevier, have actively supported the work of these conferences, and as a further demonstration of this, starting with the first issue of 2012, JBMT will include a section dedicated to both clinical fascial approaches, as well as pure science research, into fascia. A number of leaders in this field have agreed to contribute to this new section, and it is hoped that the special focus that this feature offers will encourage other researchers and clinicians, to do likewise. Among papers that will appear in this section in the first few issues of 2012, currently either in preparation or already In Press, are the following: Nigel Simmonds DC (in press) and colleagues, from the Anglo-European College of Chiropractic, propose that a biologically plausible mechanism that may generate a significant component of the observed effects of manual therapies of all descriptions, is the therapeutic stimulation of fascia in its various forms within the body. They have set out a what they state is a testable framework which links fascia into the therapeutic benefits provided by either high velocity, low amplitude manipulation, as well as soft tissue and mobilization approaches. This paper is In Press e available on ScienceDirect Hans Chaudhry and colleagues have developed a mathematical model to determine the relationship between stretch and the orientation of fibers in the fascia. This paper is an example of a scientific approach where the clinical implications can be translated from the findings. Since it provides a means to model manual therapy interventions in both longitudinal and transverse directions, this may allow more precise 1360-8592/$36 ª 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.jbmt.2011.07.002
specification of manual therapy techniques e such as myofascial release methods. This paper is In Press e available on ScienceDirect Geoff Bove PhD and Susan Chapelle (in press) RMT have studied the possibility of using manual techniques to both prevent and treat abdominal adhesions. The results of their work has demonstrated that, in a rat model, “visceral mobilization may have a role in the prevention and treatment of post-operative adhesions”. (This paper is In Press e available on ScienceDirect Moshe Solomonow PhD MD(Hon) and colleagues, from the University of Colorado, Denver, have compiled a review of extracted data from Solomonow’s over 25 years of (animal and human) research into what he terms Acute Repetitive Lumbar Syndrome, something the authors note to be “common in individuals engaged in long term performance of repetitive occupational/sports activities involving the spine”. Solomonow et al hypothesise that repetitive flexion strains damage collagen fibres in viscoelastic structures, together with simultaneous changes in reflexive neuromuscular function, and consequent stability problems. Inflammation and degenerative changes follow, leading to disability. Finally suggestions are offered relevant to prevention and treatment. This paper Acute repetitive lumbar syndrome; a comprehensive insight into the disorder e is currently being typeset Robert Schleip PhD of the University of Ulm, has studied the effects of isometric stretching on the stiffness of lumbodorsal fascia. Simply stated, stretching that does not produce microtrauma results in extrusion of fluid leading to reduced stiffness, which is subsequently taken up again, restoring stiffness, sometimes more so than was previously the case. The conclusions suggest that tissue hydration is a major feature in tissue stiffness, something of considerable importance in the stability of the low back. The clinical implications of these studies e relative to the lumbodorsal fascia of humans e remains to be confirmed, as the fascia in these reported studies were either murine or porcine.
396
Editorial However, as Dr Schlep points out, there is supporting evidence deriving from MRI studies of the Achilles tendon showing water extrusion during loading followed by subsequent rehydration (and stiffening). This paper: Strain hardening of fascia: Static stretching of dense fibrous connective tissues can induce a temporary stiffness increase accompanied by enhanced matrix hydration, is currently being typeset
A number of additional papers, where fascia is the main focus, are being reviewed or prepared for publication. This issue of JBMT contains another example of fascial focus, in a clinical setting. Tozzi et al. (2011) employed dynamic ultrasound evaluation to demonstrate that gentle manual methods [“low load, long duration stretch along the lines of maximal fascial restrictions”] are capable of releasing areas of impaired sliding fascial mobility, while also modifying pain. The list of papers summarised above should offer a clear sense that while fascia/connective tissue features large in all of them, their range and variety demonstrate that they
have clinical relevance in almost all manual and movement therapies e which is precisely the objective of the new fascia section.
References Bove, G., Chapelle, S. Visceral mobilization can lyse and prevent peritoneal adhesions in a rat model. doi: 10.1016/j.jbmt.2011. 02.004, in press. Simmonds N. et al. A theoretical framework for the role of fascia in manual therapy. Journal of Bodywork & Movement Therapies. 10.1016/j.jbmt.2010.08.001, in press. Chaudhry H. et al. Mathematical model of fiber orientation in anisotropic fascia layers at large displacements, in press. Tozzi, P., et al., 2011. Fascial release effects on patients with nonspecific cervical or lumbar pain. Journal of Bodywork & Movement Therapies 15 (4), 405e416.
Leon Chaitow, ND DO , Editor-in-Chief JBMT, PO Box 41, Corfu 49100, Greece E-mail address:
[email protected] Journal of Bodywork & Movement Therapies (2011) 15, 397 available at www.sciencedirect.com
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LETTER TO THE EDITOR
Correspondence re “Association of manual muscle tests and mechanical neck pain: Results from a prospective pilot study”
Dear Editor, I appreciate the fact that Cuthbert et al. (2011) have made a preliminary attempt to determine the validity of the Applied Kinesiology (AK) method of using muscle testing to determine the presence of a cervical pain disorder. Further, I am aware that this was a pilot study. However, I think the authors have erroneously concluded that their study provides evidence of the sensitivity and specificity of Applied Kinesiology manual muscle testing for determining who has cervical pain and can at best say that they have found that such research is feasible. One fundamental problem with this study is that the examiners were not blind to the status of the subjects (Straus et al., 2005). The knowledge of the clinical status of the patients means that this study design is prone to confirmation bias (Graber et al., 2005). That is that the examiner finds what the examiner believed they would find, that people with cervical pain have “weak” cervical muscles. Another fundamental problem with this study is that the healthy subjects were not tested by the same examiner who tested the subjects with cervical pain (Straus et al., 2005). Given the fact that we have no way of knowing if the forces applied by the two examiners were even of the same order of magnitude let alone reasonably similar we cannot be certain that the healthy subjects and those with cervical pain were actually tested in the same way. Finally, sensitivity and specificity are normally calculated by using a reference test (in this case the patient’s report of cervical pain or not) comparing it to the findings of the new test (in this case AK muscle testing) (Straus et al., 2005). However this was not done. Sensitivity and
DOI of original article: 10.1016/j.jbmt.2010.11.001. 1360-8592/$36 ª 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.jbmt.2011.06.005
specificity were calculated by some unknown method separately for those with cervical pain and those without. I have no idea how the sensitivity and specificities were calculated. The Journal of Bodywork & Movement Therapies subscribes to the ethical principles of the Declaration of Helsinki and states in their instructions to authors that: “The manuscript should contain a statement that the work has been approved by the appropriate ethical committees related to the institution(s) in which it was performed and that subjects gave informed consent to the work.” The authors do write “all participants were made aware of the experimental details prior to assuming their involvement in the study, and they were required to fill out a symptom questionnaire and consent form before the testing was administered.” (JBMT, 2011) I cannot find any statement that this study was approved by the appropriate ethical committee. Was this just an oversight on both the authors’ and the reviews part, or did I miss this statement?
References Cuthbert, S.C., Rosner, A.L., McDowall, D., 2011. Association of manual muscle tests and mechanical neck pain: results from a prospective pilot study. J. Bodyw. Mov. Ther. 15 (2), 192e200. Apr. Graber, M.L., Franklin, N., Gordon, R., 2005. Diagnostic error in internal medicine. Arch. Intern. Med. 11;165 (13), 1493e1499. Journal of Bodywork and Movement Therapies, 2011. Guide for Authors. Elsevier B. V. [cited June 15, 2011]; Available from: http://wwwelsevier.com/wps/find/journaldescription.cws_ home/623047/authorinstructions. Straus, S.E., Richardson, W.S., Glasziou, P., Haynes, R.B., 2005. Evidence-based medicine: How to practice and teach EBM, third ed. Elsevier Churchill Livingstone, New York.
Stephen M. Perle, DC, MS University of Bridgeport College of Chiropractic, Bridgeport, CT 06604, USA E-mail address:
[email protected] Journal of Bodywork & Movement Therapies (2011) 15, 398 available at www.sciencedirect.com
journal homepage: www.elsevier.com/jbmt
LETTER TO THE EDITOR
Response to Letter to the Editor by Perle To the Editor, We appreciate Dr. Perle’s interest in our recent publication, attempting to establish the validity of manual muscle testing in instances of cervical pain. While pointing out several cautionary notes common to clinical research, we have reason to believe that in this instance they are all misplaced in the four arguments that he has put forth: 1. Blinding: While blinding is a standard criterion of quality in traditional allopathic randomized controlled trials, its inclusion in trials involving physical medicine interventions is known to be highly problematical and in this instance could conceivably be considered to be sort of a blindman’s bluff (Rosner, in press). Furthermore, blinding has actually been known to have a detrimental effect on recruitment for clinical trials (Hemminiki et al., 2004) taking into consideration more recent data which suggest that patient choice and awareness are desirable inclusions rather than the liability that Dr. Perle suggests (Rosner, in press). Finally, blinding has no place in standard clinical practice where manual muscle testing occurs and may actually introduce an unwanted element of stress. If research is to be effectively translated into practice, our attention needs to be focused more upon translational research (Editorial, 2009) rather than the more artificial conditions imposed by blinding. 2. Different examiners: While patients with or without mechanical neck pain were tested by separate examiners, robust data exists to suggest that a substantial degree of inter-observer reliability exists in manual muscle testing (Cuthbert and Goodheart, 2007; Caruso and Leisman, 2000). 3. Sensitivity and specificity: The standard calculation for sensitivity is TP/TP þ FN, while for specificity it is TN/ FP þ TN where TP Z true positive, TN Z true negative, FP Z false positive, and TN Z true negativedprecisely the numbers that were included in our paper. The reference values used in our calculations were the actual occurrences of neck pain as reported by the patient. DOI of original article: 10.1016/j.jbmt.2011.06.005. 1360-8592/$36 ª 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.jbmt.2011.06.006
4. Ethical principals: Patient rights and safety in clinical research are well protected by the principles of the Nuremberg and Helsinki conventions. Indeed, patients were given full informed consent of the experimental details in this study and signed off to that effect. However, in situations such as this in which no experimental interventions of any kind were imposed, ethical committees and internal review boards are essentially irrelevant. This is simply because data from everyday patient appointments with their treating doctor were gathered retrospectively with no risk to, or imposition upon, the patient. In JBMT, as in most of the journals publishing research involving manual medicine, case and case-series reports are frequently published. Dr. Perle’s insistence on an “institutional review board’s” approval of all research printed in JBMT and elsewhere would have censored most of the research conducted in manual medicine for the past century. In conclusion, we believe that the criticisms raised by Dr. Perle with regard to this study can readily be addressed.
References Caruso, W., Leisman, G., 2000. A force/displacement analysis of muscle testing. Percep. Mot. Skills 91, 683e692. Cuthbert, S.C., Goodheart, G.J., 2007. On the reliability and validity of manual muscle testing: a literature review. Chiropractic & Osteopathy 15, 4. Editorial, 2009. [Translational research: two-way traffic]. J. Bodywork Move. T. Ther. 13, 295e296. Hemminiki, E., Hovi, S.L., Veerus, P., Sevon, T., Tuimala, R., Rahu, M., Hakama, M., 2004. Blinding decreased recruitment in a prevention trial of postmenopausal hormone therapy. J. Clin. Epidemiol. 57 (12), 1237e1243. Rosner, A., (in press). Evidence-based medicine: Revisiting the pyramid of priorities. J. Bodywork Movement Ther.
Anthony L. Rosner Scott Cuthbert* Donald McDowall Chiropractic Health Center, 255 West Abriendo Avenue, Pueblo, CO 81004, USA *Corresponding author. Tel.: þ1 719 544 1468. E-mail address:
[email protected] (S. Cuthbert)
Journal of Bodywork & Movement Therapies (2011) 15, 399e404
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CASE SERIES
Changes in pain and pressure pain sensitivity after manual treatment of active trigger points in patients with unilateral shoulder impingement: A case series ˜as, PT, MSc, ´sar Ferna ´ndez-de-las-Pen Amparo Hidalgo-Lozano, PT a, Ce b,c, d * ´lez-Iglesias, PT, PhD e, PhD , Lourdes Dı´az-Rodrı´guez, PhD , Javier Gonza ˜a, PhD f, Manuel Arroyo-Morales, MD, PT, PhD a Domingo Palacios-Cen a
Department of Physical Therapy, Universidad Granada, Spain Department of Physical Therapy, Occupational Therapy, Rehabilitation and Physical Medicine, Universidad Rey Juan Carlos, Alcorco´n, Madrid, Spain c Esthesiology Laboratory of Universidad Rey Juan Carlos, Alcorco´n, Spain d Department of Nursing, Health Sciences School, Universidad Granada, Spain e Centro de Fisioterapia Integral, Candas, Asturias, Spain f Department of Health Sciences II, Universidad Rey Juan Carlos, Alcorco´n, Spain b
Received 6 October 2010; received in revised form 30 November 2010; accepted 1 December 2010
KEYWORDS Shoulder impingement; Manual treatment; Trigger points; Pressure pain
Summary The aim of this case series was to investigate changes in pain and pressure pain sensitivity after manual treatment of active trigger points (TrPs) in the shoulder muscles in individuals with unilateral shoulder impingement. Twelve patients (7 men, 5 women, age: 25 9 years) diagnosed with unilateral shoulder impingement attended 4 sessions for 2 weeks (2 sessions/week). They received TrP pressure release and neuromuscular interventions over each active TrP that was found. The outcome measures were pain during arm elevation (visual analogue scale, VAS) and pressure pain thresholds (PPT) over levator scapulae, supraspinatus infraspinatus, pectoralis major, and tibialis anterior muscles. Pain was captured pre-intervention and at a 1-month follow-up, whereas PPT were assessed pre- and post-treatment, and at a 1-month follow-up. Patients experienced a significant (P < 0.001) reduction in pain after treatment (mean SD: 1.3 0.5) with a large effect size (d > 1). In addition, patients also experienced a significant increase in PPT immediate after the treatment (P < 0.05) and one month after discharge (P < 0.01), with effect sizes ranging from moderate (d Z 0.4) to large (d > 1).A significant negative association (rs Z 0.525; P Z 0.049) between the increase in
* Corresponding author. Facultad de Ciencias de la Salud, Universidad Rey Juan Carlos, Avenida de Atenas s/n, 28922 Alcorco ´n, Madrid, Spain. Tel.: þ 34 91 488 88 84; fax: þ34 91 488 89 57. E-mail address:
[email protected] (C. Ferna ´ndez-de-las-Pen ˜as). 1360-8592/$ - see front matter ª 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jbmt.2010.12.003
400
A. Hidalgo-Lozano et al. PPT over the supraspinatus muscle and the decrease in pain was found: the greater the decrease in pain, the greater the increase in PPT. This case series has shown that manual treatment of active muscle TrPs can help to reduce shoulder pain and pressure sensitivity in shoulder impingement. Current findings suggest that active TrPs in the shoulder musculature may contribute directly to shoulder complaint and sensitization in patients with shoulder impingement syndrome, although future randomized controlled trials are required. ª 2010 Elsevier Ltd. All rights reserved.
Introduction Shoulder pain is a common health problem that has a multifactorial underlying pathology with high direct costs for the society (Meislin et al., 2005). The one-year prevalence of shoulder pain ranges from 20% to 50% in the general population (Pope et al., 1997; Luime et al., 2004). Among the different causes of shoulder pain, the most prevalent diagnosis is shoulder impingement (13%) (Pribicevic et al., 2009). The aetiology of shoulder impingement is not completely understood, but there is evidence showing the role of the shoulder musculature as a potential factor (Tyler et al., 2005). Different studies have shown the presence of muscle imbalance of the shoulder musculature in this painful condition (Ludewig and Cook, 2000; Moraes et al., 2008). Due to this imbalance, Simons et al. (1999) suggested that muscle trigger points (TrP) can play a relevant role in shoulder impingement syndrome. TrPs are defined as hypersensible spots in a taut band of a skeletal muscle, painful on contraction, stretching or manual stimulation which give rise to a referred distant pain. Active TrPs are those which their local and referred pains are responsible for the patients’ symptoms. There is preliminary evidence suggesting that referred pain from active TrPs may be implicated in the clinical picture of shoulder impingement. Ingber (2000) described 3 patients with shoulder impingement syndrome who were successfully treated with TrPs injection of the subscapularis muscle. Ge et al. (2008) described the presence of active TrPs within the infraspinatus muscle in individuals with shoulder pain, without specific diagnosis. A recent study reported that the referred pain elicited by active TrPs in the supraspinatus, infraspinatus, pectoralis mayor and subscapularis muscles reproduced the pain pattern in subjects with shoulder impingement (HidalgoLozano et al., 2010). The hypothesis that active TrPs may be relevant for shoulder pain has been supported by the study of Hains et al. (2010) where myofascial therapy using ischemic compression on shoulder TrPs reduced the symptoms of patients experiencing chronic shoulder pain. Therefore, these studies suggest that referred pain from active TrPs may be relevant for shoulder pain. Hidalgo-Lozano et al also found that patients with shoulder impingement exhibit generalized pressure pain hypersensitivity as compared to controls (Hidalgo-Lozano et al., 2010). In addition, the presence of mechanical pain hypersensitivity was related to the presence of active TrPs, suggesting that active TrPs may be involved in sensitization mechanisms in individuals with impingement syndrome (Hidalgo-Lozano et al., 2010). The aim of this case series was to investigate changes in pain and pressure pain sensitivity after manual treatment of active muscle
TrPs in the shoulder musculature in patients with unilateral shoulder impingement.
Methods Patients Consecutive patients with diagnosis of strictly unilateral impingement syndrome stage I (acute inflammation and either tendonitis or bursitis) (Frieman et al., 1994) within the dominant-right hand were recruited. Patients were eligible if: 1) they had unilateral shoulder complaints with duration of at least 3 months; 2) an intensity of at least 4 on an 11-point numerical pain rating scale (NPRS) during arm elevation; 3) positive Neer test, that is, pain during passive abduction (Neer, 1983); and, 4) positive Hawkins, that is, pain when the arm is flexed at 90 and passively positioned in internal rotation (MacDonald et al., 2000). The sensitivity and specificity for the Neer test has been estimated as 79% and 53%, respectively, and for the Hawkins test 79% and 59%, respectively (Hegedus et al., 2008). Patients were excluded if they exhibited any of the following criteria: 1, bilateral shoulder symptoms; 2, younger than 18 or older than 65 years; 3, history of shoulder fractures or dislocation; 4, cervical radiculopathy; 5, previous interventions with steroid injections; 6, fibromyalgia syndrome (Wolfe et al., 1990); 7, previous history of shoulder or neck surgery; or 9, any type of physical intervention for the neck-shoulder area the previous year. The study was approved by the local Ethics Committee (UC 2009-45) conducted following the Helsinki Declaration. All participants signed an informed consent prior to their inclusion.
Outcome measures In this study, a visual analogue scale (VAS) (Jensen et al., 1999) was used to assess the intensity of pain experienced during arm elevation pre-intervention and one month after discharge. The VAS is a 10 cm line anchored with a “0” at one end representing “no pain” and “10” at the other end representing “the worst pain imaginable”. Patients placed a mark along the line corresponding to the intensity of the symptoms, which was scored to the nearest centimetre. It has been shown to be reliable and valid for assessing pain intensity (Bijur et al., 2001), and it was selected as outcome measure based on its ability to detect immediate changes in pain exhibiting a minimal clinically important difference (MCID) between 0.9 cm and 1.1 cm (Bird and Dickson, 2001; Gallagher et al., 2001).
Changes in sensitivity after treatment of active trigger points In addition, pressure pain thresholds (Vanderweeen et al., 1996) (PPT: minimal amount of pressure where a sensation of pressure first changes to pain) over the levator scapulae (2 cm superior to the superior angle of the scapula bone), supraspinatus (middle point over the fosa of the scapula), infraspinatus (middle muscle belly), pectoralis major (middle point under the clavicle bone), and tibialis anterior (halfway between the most superior attachment and its tendon in the upper one third of the muscle belly) muscles were also assessed. To investigate general hypoalgesic effects of TrP interventions, the inclusion of PPT assessment over the tibialis anterior was needed. In this study, a mechanical pressure algometer (Pain Diagnosis and Treatment Inc.ª, Great Neck, NY) was used (kg/cm2). The mean of 3 trials over each point was calculated and used for analysis. A 30-s resting period was allowed between each trial. The reliability of pressure algometry has been found to be high the same day (ICC Z 0.91 [95% CI 0.82e0.97]) (Chesterson et al., 2007) and between 4 separate days (ICC Z 0.94e0.97) (Jones et al., 2007). PPT levels were assessed pre-intervention, post-intervention and one month after discharge.
Myofascial/muscle TrP therapy None of the patients were taking any preventive drug at the time the study was performed. Participants were asked to avoid any analgesic or muscle relaxant during which the study was conducted. Patients were treated by a clinician with more than 6 years of clinical experience in the management of shoulder disorders. All participants attended the physical therapy clinic 2 days per week for 2 weeks (4 sessions). They received the following manual therapies depending on clinical findings related to the location of the TrP. Subjects were examined for the presence of active TrPs in the levator scapulae, supraspinatus, infraspinatus, subscapularis, and pectoralis major muscles by a clinician with more than 5 years of experience in the management of TrPs. TrP diagnosis was conducted according to Simons et al. (1999): 1) palpable taut band in a skeletal muscle; 2) hyperirritable tender spot in the taut band; 3) local twitch response elicited
Figure 1 (1999).
401 by the snapping palpation of the taut band; and 4) presence of referred pain in response to TrP compression (Fig. 1). These criteria, when applied by an experience assessor, have obtained a good inter-examiner reliability (kappa) ranging from 0.84 to 0.88 (Gerwin et al., 1997). Bron et al. (2007a,b) evaluated patients with shoulder pain and found that the most reliable feature of TrP was the referred pain (percentage of pair-wise agreement 70%, range 63e93%). Different manual approaches have been proposed for the management of muscle TrPs (Dommerholt and McEvoy, 2010). A recent systematic review found moderate strong evidence supporting the use of TrP pressure release for immediate pain relief of muscle TrPs (Vernon and Schneider, 2009). In the current study, patients received a TrP pressure release technique over each active TrP that was found (Fig. 2). Pressure was applied over TrPs until an increase in muscle resistance (barrier) was perceived by the clinician and maintained until the clinician perceived release of the taut band (Lewit, 1999). At this stage the pressure was increased to return to previous level of muscle tension and the process was repeated for 90 s (usually 2 to 3 repetitions). Patients also received a neuromuscular technique (longitudinal stroke) (Chaitow, 2010) over the affected muscle, particularly supraspinatus, infraspinatus, and pectoralis major muscles. The thumb of the therapist was placed over the taut band and longitudinal strokes were applied slowly with moderate pressure which was not painful for the patient. This technique has been found to be effective for reducing TrP pressure sensitivity (Iba ´n ˜ez-Garcı´a et al., 2009). TrP manual therapies were applied depending on clinical findings related to the location of the TrP on the affected arm. No pre-determined TrP location was considered.
Statistical analysis Data were analysed with the SPSS statistical package (19.0 Version). Results are expressed as mean, standard deviation (SD) or 95% confidence interval (95% CI). Due to the small sample size and the nature of the data, the use of nonparametric tests was considered robust. The non-parametric Wilcoxon signed test was used to examine differences from baseline to each time point for VAS and PPT levels. Further,
Referred pain from infraspinatus (left) and supraspinatus (right) muscle trigger points (TrPs) according to Simons et al.
402
A. Hidalgo-Lozano et al.
Changes in pressure pain sensitivity
Figure 2
TrP pressure release over infraspinatus TrPs.
changes in VAS and PPT were stratified by gender using the non-parametric U-Mann Whitney test. In addition, to further investigate if changes were clinically relevant, effect sizes were calculated using Cohen d coefficient (d ) (Cohen, 1988). Effect sizes of 0.2 are considered as small, 0.5 as moderate and 0.8 large (Cohen, 1988). Finally, the Spearman’s rho (rs) was used to investigate the associated between changes in pain intensity and changes over PPT over each point at before and one month after treatment. The statistical analysis was conducted at 95% confidence level and a P < 0.05 was considered statistically significant.
Results
The repeated Wilcoxon signed test revealed a significant effect for changes over the levator scapulae (z Z 2.040; P Z 0.041), supraspinatus (z Z 2.047; P Z 0.042), infraspinatus (z Z 2.353; P Z 0.019), pectoralis major (z Z 2.080; P Z 0.038), and tibialis anterior (z Z 2.041; P Z 0.040) muscles. Patients experienced a significant increase in PPT immediate after treatment and one month after the discharge (P < 0.05). Again, no significant differences for PPT difference scores between genders were found for the levator scapulae (t Z 0.622; P Z 0.523), supraspinatus (t Z 0.723; P Z 0.486), infraspinatus (t Z 1.672; P Z 0.125), pectoralis major (t Z 0.372; P Z 0.718), and tibialis anterior (t Z 0.972; P Z 0.502) muscles. Table 1 summarizes PPT levels at each point at pre-, post- and 1 month after discharge, whereas Table 2 shows pre-post changes for PPT data.
Relationship between changes in pain and pressure pain sensitivity A significant negative association (rs Z 0.525; P Z 0.049) between the increase in PPT over the supraspinatus muscle and the decrease in pain was found: the greater the decrease in pain, the greater the increase in pressure pain threshold.
Discussion Clinical data of the participants Twelve patients, 7 men and 5 women, aged 20e38 years (mean: 25 9 years) diagnosed with unilateral shoulder impingement participated. All patients reported pain located in the anterior and posterior parts of the shoulder and the dorso-lateral aspect of the forearm in 5 patients (42%). The mean duration of shoulder pain history was 8.7 4.8 months (95%CI 5e12.4), and the mean intensity of pain experienced during arm active elevation was 5.1 1.9 (95% CI 3.9e6.4).
Changes in pain The Wilcoxon signed test revealed a significant effect (z Z 2.511; P Z 0.011) for pain. Patients experienced a significant reduction in pain (mean SD: 1.3 0.5, 95% CI 0.9e2.3) from pre-intervention (mean SD: 5.1 1.9, 95% CI 3.9e6.4) as compared to one month after discharge (mean SD: 3.8 1.3, 95% CI 2.3e5.2). The effect size for pain was large (d > 1). No significant differences between men and women (t Z 0.781; P Z 0.453) for changes in pain were found. Table 1
The current case series has shown that manual treatment of active TrPs within the shoulder muscles reduces spontaneous pain and increases PPT levels in individuals with shoulder impingement. Current results underline the importance of inspection and inactivation of active muscle TrPs in the shoulder musculature in patients with shoulder impingement syndrome as they may contribute to the overall picture of pain; however, future randomized controlled trials are required to further confirm this assumption. In fact, two randomized controlled trials have been proposed in order to elucidate the role of inactivation of muscle TrPs in patients with shoulder impingement syndrome (Bron et al., 2007a,b; Perez-Palomares et al., 2009). The rotator cuff is formed by the supraspinatus, the infraspinatus, the teres minor and the subscapularis muscles (Keating et al., 1993). In the current case series, active myofascial TrPs in the supraspinatus, infraspinatus, and subscapularis were manually treated. A previous study found that the presence of active TrPs in the supraspinatus and infraspinatus muscles was related to a greater intensity of pain in patients with shoulder impingement, which support the role of active TrPs within the clinical pain
Pressure pain thresholds (PPT, kg/cm2) pre-intervention, post-interventon and one month after discharge. Pre-intervention
Levator scapulae muscle Supraspinatus muscle Infraspinatus muscle Pectoralis major muscle Tibialis anterior muscle
1.9 2.3 2.0 1.2 4.2
0.9 1.0 0.8 0.4 0.9
(95% (95% (95% (95% (95%
CI CI CI CI CI
Post-intervention 1.3e2.5) 1.7e3.0) 1.5e2.5) 1.0e1.4) 3.7e4.9)
2.5 2.8 2.9 1.7 4.6
0.8 0.7 1.4 0.6 1.9
Values are expressed as means standard deviation (95% confidence interval)
(95% (95% (95% (95% (95%
CI CI CI CI CI
One month after discharge 2.1e3.1) 2.4e3.3) 2.0e3.8) 1.3e2.0) 3.4e5.9)
2.8 3.0 2.9 1.8 4.9
0.9 0.8 1.0 0.4 1.9
(95% (95% (95% (95% (95%
CI CI CI CI CI
2.2e3.4) 2.5e3.5) 2.25e3.5) 1.5e2.1) 3.7e6.2)
Changes in sensitivity after treatment of active trigger points Table 2
403
Pre-post and pre-follow/up change scores and effect sizes for pressure pain thresholds (PPT, kg/cm2) Pre-post change scores
Levator scapulae muscle Supraspinatus muscle Infraspinatus muscle Pectoralis major muscle Tibialis anterior muscle
0.6 0.5 0.9 0.5 0.4
0.8 0.9 1.0 0.7 0.8
(95% (95% (95% (95% (95%
CI CI CI CI CI
0.3e1.6) 0.2e1.0) 0.4e1.4) 0.2e0.9) 0.2e1.1)
Pre-post effect size
Pre-follow/ up scores
0.75 0.45 0.90 0.64 0.50
0.9 0.7 0.9 0.6 0.7
1.0 0.9 0.7 0.3 1.0
(95% (95% (95% (95% (95%
Pre-follow/ up effect size CI CI CI CI CI
0.3e1.5) 0.2e1.3) 0.4e1.3) 0.4e0.7) 0.4e1.6)
0.90 0.78 1.10 2.00 0.70
Values are expressed as means standard deviation (95% confidence interval)
picture of these patients (Hidalgo-Lozano et al., 2010). In the current case series one month after 4 sessions of treatment, patients exhibited a decrease of 1.3 cm on pain which surpassed the MCID. Nevertheless, it should also be noted that lower bound estimation for the 95% confidence interval fall in the reported MCID of 0.9e1.1 cm (Bird and Dickson, 2001; Gallagher et al., 2001). Hence, current results should be considered with caution. These findings support the view that active TrPs in the shoulder musculature may contribute directly to shoulder pain complaint in individuals with shoulder impingement syndrome, although future randomized controlled trials are required. It has been previously reported that subjects with shoulder impingement exhibit both segmental and widespread sensitization mechanisms and that this mechanisms are related to the presence of active TrPs and pain symptoms (Hidalgo-Lozano et al., 2010). Shah et al. (2005, 2008) demonstrated that active TrPs constitutes a focus of peripheral sensitization as higher levels of algogenic substances such as bradykinin, substance P, or serotonin, are found in active TrPs as compared with non-TrPs. In addition, Li et al. (2009) recently demonstrated the existence of nociceptive and non-nociceptive hypersensitivity at muscle TrPs. Hence, it would be expected that treatment of active TrPs would reduce this sensitization. The current case series support this hypothesis as moderate to large increases in PPT levels were found one month after the intervention. Nevertheless, although effect sizes support a clinical effect over mechanical sensitivity; we recognize that MCID of PPT levels has not been previously studied. Our results support that muscle TrP treatment can decrease pressure pain hypersensitivity, which is in agreement with two previous studies that demonstrated that TrP treatment induces segmental anti-nociceptive effects (Srbely et al., 2008, 2010). In fact, Hsieh et al. (2007) showed that dry needling of active TrPs in the infraspinatus muscle decreased the pain intensity and mechanical pain sensitivity on the treated arm in patients with shoulder pain, supporting this anti-nociceptive effect. Additionally, the fact that PPT levels also improved in distant pain-free areas, e.g. tibialis anterior muscle, indicates a generalized anti-nociceptive effect of TrP therapy, which has been previously suggested (Niddam et al., 2007). Nevertheless, the association between the decrease in pain and the increases in PPT levels was weak. Finally, we should recognize some limitations to the current case series. First, a study without a comparison group does not allow for inferences to be made regarding cause and effect. Therefore, as result of a lack of control group, we cannot determine if changes in pain and pressure
sensitivity were due to the intervention. Second, we only include a small number of patients with shoulder impingement, which limit the results. Therefore, Future randomized clinical trials are now needed (Bron et al., 2007a,b; Perez-Palomares et al., 2009). Thirdly, we only examined the effects 1-month after discharge, so we do not know the long-term effects of the intervention. The fact that statistically significant changes occurred at short-term follow-up provides impetus for future research in this area.
Conclusion This case series suggests that manual treatment of active TrPs may reduce spontaneous pain and increase PPT in patients with shoulder impingement. Effect sizes were large for pain and moderate-large for changes in PPT. Current findings suggest that active TrPs in the shoulder musculature may contribute to shoulder complaint and sensitization in patients with shoulder impingement syndrome. However, due to a small sample size and the absence of a control group, these assumptions should be consider with caution.
References Bron, C., Franssen, J.L., Wensing, M., Oostendorp, A.B., 2007a. Inter-observer reliability of palpation of myofascial trigger points in shoulder muscles. J. Man. Manipulative Ther. 15, 203e215. Bijur, P., Silveer, W., Gallagher, J.E., 2001. Reliability of the visual analogue scale for measurement of acute pain. Acad. Emerg. Med. 8, 1153e1157. Bird, S.B., Dickson, E.W., 2001. Clinically significant changes in pain along the visual analogue scale. Ann. Emerg. Med. 36, 639e643. Bron, C., Wensing, M., Franssen, J.L.M., Oostendorp, R.A.B., 2007b. Treatment of myofascial trigger points in common shoulder disorders by physical therapy: a randomized controlled trial. BMC Musculoskelet. Disord. 8, 107. Chaitow, L., 2010. Modern Neuromuscular Techniques, third ed. Elsevier, London. Chesterson, L.S., Sim, J., Wright, C.C., Foster, N.E., 2007. Inter-rater reliability of algometry in measuring pressure pain thresholds in healthy humans, using multiple raters. Clin. J. Pain 23, 760e766. Cohen, J., 1988. Statistical Power Analysis for the Behavioural Sciences Hillsdale (NJ). Lawrence Erlbaum Associates. Dommerholt, J., McEvoy, J., 2010. Myofascial trigger point release approach. In: Wise, C.H. (Ed.), Orthopaedic Manual Physical Therapy: From Art to Evidence. FA Davis, Philadelphia. Frieman, B.G., Albert, T.J., Fenlin, J.M., 1994. Rotator cuff disease: a review of diagnosis, patho-physiology, and current trends in treatment. Arch. Phys. Med. Rehabil. 75, 604e609. Gallagher, E.J., Liebman, M., Bijur, P.E., 2001. Prospective validation of clinically important changes in pain severity measured on a visual analogue scale. Ann. Emerg. Med. 38, 633e638.
404 Ge, H.Y., Ferna ´ndez-de-las-Pen ˜as, C., Madeleine, P., ArendtNielsen, L., 2008. Topographical mapping and mechanical pain sensitivity of myofascial trigger points in the infraspinatus muscle. Eur. J. Pain 12, 859e865. Gerwin, R.D., Shanon, S., Hong, C.Z., Hubbard, D., Gevirtz, R., 1997. Interrater reliability in myofascial trigger point examination. Pain 69, 65e67. Hains, G., Descarreaux, M., Hains, F., 2010. Chronic shoulder pain of myofascial origin: a randomized clinical trial using ischemic compression therapy. J. Manipulative Physiol. Ther. 33, 362e369. Hegedus, E.J., Goode, A., Campbell, S., Morin, A., Tamaddoni, M., Moorman 3rd, C.T., Cook, C., 2008. Physical examination tests of the shoulder: a systematic review with meta-analysis of individual tests. Br. J. Sports Med. 42, 80e92. Hidalgo-Lozano, A., Ferna ´ndez-de-las-Pen ˜as, C., Alonso-Blanco, C., Ge, H.Y., Nielsen, A., Arroyo-Morales, M., 2010. Muscle trigger points and pressure pain hyperalgesia in the shoulder muscles in patients with unilateral shoulder impingement: a blinded, controlled study. Exp. Brain Res. 202, 915e925. Hsieh, Y.L., Kao, M.J., Kuan, T.S., Chen, S.M., Chen, J.T., Hong, C.Z., 2007. Dry needling to a key myofascial trigger point may reduce the irritability of satellite MTrPs. Am. J. Phys. Med. Reha ´bil 86, 397e403. Iba ´n ˜ez-Garcı´a, J., Alburquerque-Sendı´n, F., Rodrı´guez-Blanco, C., et al., 2009. Changes in masseter muscle trigger points following strain-counter/ strain or neuro-muscular technique. J. Bodyw Mov Ther. 13, 2e10. Ingber, R.S., 2000. Shoulder impingement in tennis/racquetball players treated with subscapularis myofascial treatments. Arch. Phys. Med. Rehabil. 81, 679e682. Jensen, M.P., Turbner, J.A., Romano, J.M., Fisher, L., 1999. Comparative reliability and validity of chronic pain intensity measures. Pain 83, 157e162. Jones, D.H., Kilgour, R.D., Comtois, A.S., 2007. Test-retest reliability of pressure pain threshold measurements of the upper limb and torso in young healthy women. J. Pain 8, 650e656. Keating, J.F., Waterworth, P., Shaw-Dunn, J., Crossan, J., 1993. The relative strength of the rotator cuff muscles: a cadaver study. J. Bone Jt. Surg. Br. 75, 137e140. Lewit, K., 1999. Manipulative Therapy in Rehabilitation of the Locomotor System, third edition. Butterworth Heinemann, Oxford. Li, L.T., Ge, H.Y., Yue, S.W., Arendt-Nielsen, L., 2009. Nociceptive and non-nociceptive hypersensitivity at latent myofascial trigger points. Clin. J. Pain 25, 132e137. Ludewig, P.M., Cook, T.M., 2000. Alterations in shoulder kinematics and associated muscle activity in people with symptoms of shoulder impingement. Phys. Ther. 80, 276e291. Luime, J.J., Koes, B.W., Hendriksen, I.J., et al., 2004. Prevalence and incidence of shoulder pain in the general population; a systematic review. Scand. J. Rheumatol. 33, 73e81. MacDonald, P.B., Clark, P., Sutherland, K., 2000. An analysis of the diagnostic accuracy of the Hawkins and Neer subacromial impingement signs. J. Shoulder Elbow Surg. 9, 299e301.
A. Hidalgo-Lozano et al. Meislin, R.J., Sperling, J.W., Stitik, T.P., 2005. Persistent shoulder pain: epidemiology, patho-physiology, and diagnosis. Am. J. Orthop. 34 (12 Suppl), 5e9. Moraes, G.F., Faria, C.D., Teixeira-Salmela, L.F., 2008. Scapular muscle recruitment patterns and isokinetic strength ratios of the shoulder rotator muscles in individuals with and without impingement syndrome. J. Shoulder Elbow Surg. 17 (1 Suppl), 48Se53S. Neer II, C.S., 1983. Impingement lesions. Clin. Orthop. Relat. Res. 173, 70e77. Niddam, D.M., Chan, R.C., Lee, S.H., Yeh, T.C., Hsieh, J.C., 2007. Central modulation of pain evoked from myofascial trigger point. Clin. J. Pain 23, 440e448. Perez-Palomares, S., Olivan-Blazquez, B., Arnal-Burro, A.M.A., et al., 2009. Contributions of myofascial pain in diagnosis and treatment of shoulder pain: a randomized controlled trial. BMC Musculoskelet. Disord. 10, 92. Pope, D.P., Croft, P.R., Pritchard, C.M., Silman, A.J., 1997. Prevalence of shoulder pain in the community: the influence of case definition. Ann. Rheum. Dis. 56, 308e312. Pribicevic, M., Pollard, H., Bonello, R., 2009. An epidemiologic survey of shoulder pain in chiropractic practice in Australia. J. Manipulative Physiol. Ther. 32, 107e117. Shah, J.P., Phillips, T.M., Danoff, J.V., Gerber, L.H., 2005. An in vitro microanalytical technique for measuring the local biochemical milieu of human skeletal muscle. J. Appl. Physiol. 99, 1977e1984. Shah, J.P., Danoff, J.V., Desai, M.J., Parikh, S., Nakamura, L.Y., Phillips, T.M., Gerber, L.H., 2008. Biochemical associated with pain and inflammations are elevated in sites near to and remote from active myofascial trigger points. Arch. Phys. Med. Rehabil. 89, 16e23. Simons, D.G., Travell, J., Simons, L.S., 1999. Travell and Simons’; Myofascial Pain and Dysfunction: The Trigger Point Manual, second ed., vol. 1. Williams & Wilkins, Baltimore. Srbely, J.Z., Dickey, J.P., Lowerison, M., Edwards, A.M., Nolet, P.S., Wong, L.L., 2008. Stimulation of myofascial trigger points with ultrasound induces segmental antinociceptive effects: a randomized controlled study. Pain 139, 260e266. Srbely, J.Z., Dickey, J.P., Lee, D., Lowerison, M., 2010. Dry needle stimulation of myofascial trigger points evokes segmental antinociceptive effects. J. Rehabil. Med. 42, 463e468. Tyler, T.F., Nahow, R., Nicholas, S., McHugh, M., 2005. Quantifying shoulder rotation weakness in patients with shoulder impingement. J. Shoulder Elbow Surg. 14, 570e574. Vanderweeen, L., Oostendorp, R.B., Vaes, P., Duquet, W., 1996. Pressure algometry in manual therapy. Man. Ther. 1, 258e265. Vernon, H., Schneider, M., 2009. Chiropractic management of myofascial trigger points and myofascial pain syndrome: a systematic review of the literature. J. Manipulative Physiol. Ther. 32, 14e24. Wolfe, F., Smythe, H.A., Yunus, M.B., et al., 1990. The American College of Rheumatology 1990 criteria for clasification of fibromyalgia: report of the multicenter criteria committee. Arthritis. Rheum. 33, 160e170.
Journal of Bodywork & Movement Therapies (2011) 15, 405e416
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CLINICAL RESEARCH
Fascial release effects on patients with non-specific cervical or lumbar pain Paolo Tozzi, Bsc (Hons) Ost, D.O., FT a,*, Davide Bongiorno, M.D., D.O. b, Claudio Vitturini c a
Centro di Ricerche Olistiche per la Medicina Osteopatica e Naturale, C.R.O.M.O.N., Via Pasquale Fiore 18, Rome, Italy1 Andrew Taylor Still Academy Italia, A.T.S.A.I., Bari, Naples, Milan, Italy2 c Universita` la Sapienza - Dipartimento di Psicologia, Rome, Italy b
Received 14 January 2010; received in revised form 22 November 2010; accepted 24 November 2010
KEYWORDS Connective tissue; Real-time ultrasound; Fascial imaging; Soft tissue manipulation; Pain perception; Osteopathy
Summary Background: Myofascial Release (MFR) and Fascial Unwinding (FU) are widely used manual fascial techniques (MFTs), generally incorporated in treatment protocols to release fascial restrictions and restore tissue mobility. However, the effects of MFT on pain perception, and the mobility of fascial layers, have not previously been investigated using dynamic ultrasound (US) in patients with neck pain (NP) and low back pain (LBP). Objectives: a) To show that US screening can be a useful tool to assess dysfunctional alteration of organ mobility in relation to their fascial layers, in people with non-specific NP or LBP, in the absence of any organ disease; b) To assess, by dynamic US screening, the change of sliding movements between superficial and deep fascia layers in the neck, in people with non-specific NP, before and after application of MFTs c) To assess, by dynamic US screening, the variation of right reno-diaphragmatic (RD) distance and of neck bladder (NB) mobility, in patients with nonspecific LBP, before and after application of MFTs d) To evaluate ‘if’ and ‘at what degree’ pain perception may vary in patients with NP or LBP, after MFTs are applied, over the short term. Methods: An Experimental group of 60 subjects, 30 with non-specific NP and 30 with nonspecific LBP, were assessed in the area of complaint, by Dynamic Ultrasound Topographic Anatomy Evaluation (D.US.T.A.-E.), before and after MFTs were applied in situ, in the corresponding painful region, for not more than 12 min. The results were compared with those from the respective Sham-Control group of 30 subjects. For the NP sub-groups, the pre- to post- US recorded videos of each subject were compared and assessed randomly and independently by two blinded experts in echographic screening. They were asked to rate the change observed in the cervical fascia sliding motions as ‘none’, ‘discrete’ or ‘radical’. For the LBP sub-groups,
* Corresponding author. Via Festo Avieno 150, 00136, Rome, Italy. Tel.: þ39 3486981064 (mobile); fax. þ39 06 97749900. E-mail address:
[email protected] (P. Tozzi). 1 www.cromon.it. 2 www.atsai.it. 1360-8592/$ - see front matter ª 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jbmt.2010.11.003
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P. Tozzi et al. a pre- to post- variation of the right RD distances and NB mobility were calculated on US imaging and compared. For all four sub-groups, a Short-Form McGill Pain Assessment Questionnaire (SF-MPQ) was administered on the day of recruitment as well as on the third day following treatment. Results: The Chi square test has shown a significant correlation (0.915) with a p-Value < 0.0001 between the two examiners’ results on US videos in NP sub-groups. The ANOVA test at repeated measures has shown a significant difference (p-Value < 0.0001) within Experimental and Control groups for the a) pre- to post- RD distances in LBP sub-groups, b) pre- to post- NB distances in LBP sub-groups; as well as between groups as for c) pre- to post- SF-MPQ results in NP and LBP sub-groups. Conclusions: Dynamic US evaluation can be a valid and non-invasive instrument to assess and monitor effective sliding motion of fascial layers in vivo. MFTs are effective manual techniques to release area of impaired sliding fascial mobility, and to improve pain perception over a short term duration in people with non-specific NP or LBP. ª 2010 Elsevier Ltd. All rights reserved.
Introduction Fascia and MFTs Fascia is a connective tissue organized in a three-dimensional network, that surrounds, supports, suspends, protects and connects muscular, skeletal and visceral components of the body. Studies suggest that fascia reorganizes along the lines of tension imposed or expressed in the body at both molecular (Dunn and Silver, 1983; Mosler et al., 1985) and macroscopic level (Sasaki and Odajima, 1996). Myers (2000) describes fascial meridians as tensile myofascial bands, that comprise a single continuous structure. From this perspective, the repercussion of a fascial restriction may be body-wide, and may potentially create stress on any structures enveloped by fascia (Greenman, 1989). The consequent distortion of the body’s threedimensional alignment may lead to biomechanically inefficient function (Rolf, 1977). It has been suggested that fascial strains can slowly increase, requiring progressive body adaptation at a local and global level (Levin, 1990). The pressure exerted with subsequent stress on the surrounding soft tissues may have mechanical and physiological effects. This is evident mechanically in the collagenous framework of the body, which is organized as a tensegritive structure (Levin, 1990), as well as at the cellular level (Ingber and Chen, 1999; Pischinger, 1991). The ground substance changes to a more ‘sol’-like consistency (the fluid state of living colloids, reversible into a more solid, ‘gel’-like state), while fibrous infiltration and cross links between collagen fibers may develop at the nodal points of fascial bands, together with a progressive loss of elastic properties (Chaitow, 1999). Fascial techniques aim to release such tensions, decrease pain and restore function. The proposed mechanism for fascial techniques is based on various studies that looked at the plastic, viscoelastic and piezoelectric properties of connective tissue (Fratzl, 2008). As the collagen fibers are released, they reorganize themselves in the underlying substance, whose viscosity changes so permitting tissue remodelling (Cantu and Grodin, 1992). This change in viscosity seems to involve an increase in the production of hyaluronic acid, together with the flow of as well as
improved drainage of inflammatory mediators and metabolic wastes (Schultz and Feltis, 1996); together with reduced chemical irritation of the ANS endings and nociceptive stimuli to somatic endings (Lund et al., 2002; Mense, 1983). To better understand the clinical implications of fascial restrictions in cases of acute and chronic NP or LBP, the quality of sliding motion between fascial layers in vivo appears to be of great importance (Langevin 2006). FU is a commonly used, but seldom researched, technique in osteopathic practice (Ward, 2003), aimed to release fascia restrictions and to restore tissue mobility and function. MFR is defined by Manheim (2001) as the facilitation of mechanical, neural, and psychophysiological adaptive potential as interfaced via the myofascial system. It represents a widely employed manual technique specific for fascial tissues, to reduce adhesions, restore and/or optimise fascia sliding mobility in both acute and chronic conditions (Barnes, 1996; Martin, 2009; Sucher, 1993; Walton, 2008). Some studies have shown the efficacy of MFR to decrease pain, improve posture, and quality of life (Barnes, 1990; Fernandez de las Penas et al., 2005; LeBauer et al., 2008; Lukban, 2001; Radjieski et al., 1998). However, according to Remvig (2008) “There are no published reliability studies documenting that the diagnostic method is reproducible and valid.”
US screening In many different studies and areas of practice, US is widely used to screen and diagnose for various: a) Acute (Nelson et al., 1980) and chronic conditions (De Miguel et al., 2009; Falsetti et al., 2004): infective (Gandolfo et al., 1993; Harr et al., 1982; Simons et al., 1983), genetically transmitted (Heckmatt et al., 1982), inflammatory (Karabay et al., 2007; Kenney and Hafner, 1977), degenerative (Heers and Hedtmann, 2002) and neoplastic (Nishimura et al., 1992) diseases; b) As well as to perform real-time investigation of dysfunctional syndromes, still not well-understood by other methods of screening (Cvitkovi c-Kuzmi c et al., 2002; Wong and Li, 2000).
Fascial release effects on patients with non-specific cervical or lumbar pain US is also shown to be a reliable tool: c) To assess the presence and the extent of surgery-related sequelae (Ku ¨llmer et al., 1997; Mann et al., 1989; Wiener et al., 1987), as well as the consequences of traumatic injuries (Bokhari et al., 2004; Murphy et al., 2005); d) To monitor the procedure of invasive techniques of investigation and surgical intervention (Bassi et al., 1996; Gandolfo et al., 1993; Sinha and Chan, 2004); e) To evaluate the follow up of patients under manual therapies in real-time (Hutzschenreuter et al., 1989; Park et al., 2007; Quere ´ et al., 2009; Torstensen et al., 1994), or under specific therapeutic protocols (Wang et al., 2008); f) To treat musculo-skeletal conditions when applied in a therapeutic form (Dogru et al., 2008; Downing and Weinstein, 1986; Esposito et al., 1984). However, few studies have relied on US screening to investigate alterations of the mobility of organs on their fascial layers, and even fewer have related such impaired mobility with pain on the correspondent spinal level. No research has ever assessed, by real-time US screening, any possible change in vivo of the range of sliding movements between superficial and deep fascial layers, before and after MFTs are applied in situ, on patients with non-specific NP or LBP: as has been the scope of this study. US screening of cervical organs mobility in patients with NP e Hypothesis 1 (H1) Up to now, most of research has assessed thyroid mobility, esophageal motility and larynx mobility, by US screening, in people with NP in concomitance of a disease of the organ observed: thyroid mobility and shape have been evaluated in patient complaining of NP and suffering of subacute thyroiditis (Yamashita et al., 1993) and thyroglossal duct abscesses (Rohn and Rubio, 1980); additionally, esophageal sensory and motor function has been studied by US investigation, in dysfunctional (Hirano and Pandolfino, 2007), pathological (Takebayashi et al., 1991) as well as in normal conditions (Mittal, 2005); mobility and anatomy of the healthy larynx and perilaryngeal structure have been observed by US screening (Valente et al., 1996) mainly in the paediatric field (Friedman, 1997). For the scope of this study, instead, the general mobility of cervical organs within the superficial and deep fascia complexes of the neck were investigated in relation to non-specific NP, in the absence of any cervical organ disease, before and after MFTs were applied in situ. Because the patient’s discomfort or pain should be taken in account as clinically relevant phenomena, in addition, this study has questioned whether changes in fascial mobility, following manual therapy, might influence pain perception in symptomatic patients. Thus this study’s first hypothesis: H1: i) US screening can be used to assess a dysfunctional alteration of cervical organ mobility on their fascial layers, in people with non-specific NP and without cervical organ disease; ii) The application of MFTs to the symptomatic cervical region improves the quality and quantity of such fascial layers mobility, observable by US screening; iii) The application of MFTs decreases NP perception in the short term.
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US screening of kidney and bladder mobility in people with LBP e Hypothesis 2 of this study (H2) Research has shown the relation between lumbar pain and altered renal mobility and shape in patients with frank acute (Barbagelata Lo ´pez et al., 2008) and chronic (Rivera et al., 2008) kidney pathology, as well as in cases of inherited (Bajwa et al., 2004) and acquired conditions (Watkins et al., 2009), by using US methods of screening. However, no study has established the criteria for “normal” kidney mobility. There is also no established neither if there is a correlation between renal mobility and lumbar pain in the absence of renal pathologies (although one study (Morgan and Dubbins, 1992) screened for pancreas and, partially, for renal mobility, using US, on patients with unrelated symptomatology). With regard to US assessment of bladder mobility, research studies have investigated the degree of bladder descent in primiparae (Sartori et al., 2004), nulligravid and multiparae (Meyer et al., 1996), as well as in women with stress urinary incontinence (Pregazzi et al., 2002), the latter during both Valsalva manoeuvre and maximal pelvic floor contraction. However, only a few have questioned a relationship between bladder pathology and LBP, such as in a case of bladder prolapse (Heit et al., 2002), or general urological disease (Tilscher et al., 1977). There have been no such studies reported in the absence of bladder pathology. Furthermore, no studies have investigated how back pain perception and kidney/bladder mobility varies after manual therapy is applied, in patients with no frank organic pathologies (the literature reports a preliminary study of chiropractic decompression (Browning, 1989) in six cases with pelvic dysfunction, although clinical signs were used as indicators for pre and post assessment). Therefore, this study has investigated the possible relationship between non-specific LBP and renal/bladder mobility, and their myofascial suspending and supporting structures, in patients with healthy kidneys and bladder, before and after MFTs were applied in situ. In addition, this study has questioned whether possible changes in fascial mobility, following manual therapy, may influence pain perception in symptomatic patients. Thus this study’s second hypothesis: H2: i) US screening can be used to assess dysfunctional changes in kidney and bladder mobility and their fascial layers, in people with non-specific LBP and without organ disease; ii) The application of MFTs to the symptomatic lumbo-pelvic region improves the quality and quantity of such organs mobility, measurable by US screening; iii) The application of MFTs decreases LBP perception over the short term.
Materials and methods Population During the one year period during which this study was conducted, out of the 356 subjects who came to the clinic presenting with NP or LBP, a total of 120 were recruited after examination and meeting the inclusion criteria. The inclusion criteria were an age between 18 and 60 years; a complaint of non-specific pain in the cervical or lumbar
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region, with or without associated neurological symptoms, with a duration of at least 3 weeks and of not more than 6 months; an MRI/US documented absence of inherited or acquired pathologies of the spine, or the neck, kidneys and bladder. Exclusion criteria were pregnancies, concomitant receipt of physical or manual therapy, the use of analgesics and/or anti-inflammatory drugs in the previous 72 h. Out of the 120 people included in this study, 60 were suffering from non-specific NP, while the remainder reporting non-specific LBP. The subjects were randomly selected and assigned to Experimental and Sham-Control groups. A block randomization was applied at this phase: a block size of 6 was established and a random choice of the possible balanced combination in each block was made to determine the assignment of the two sub-groups (NP and LBP) into their respective main groups (Experimental and Control). The male-female ratio as well as the age range and mean for each group are shown on Table 1.
Setting This study was conducted over a period of 13 months, from September 2008 to October 2009 at the C.R.O.M.O.N. centre in Rome, Italy.
Real-time US screening Each subject underwent a US scanning of the area of complaint, performed by a blinded, medical doctor with 15 years experience of specialised US screening. ESAOTE My LAB 25 GOLD device was used for this purpose. A Dynamic Ultrasound Topographic Anatomy Evaluation (D.US.T.A.-E.) was performed on each subject: This offered a method of US screening that included recordings of real-time US videos, with a specific focus on anatomical margins and morphologies of the organs assessed, together with their effective sliding motion on surrounding connective tissue structures in vivo.
rotation, rested on the couch, before and after MFTs or the sham treatment had been applied. A linear probe was used at 7.5e13 MHz. It was always positioned on the sagittal plane at the left antero-lateral region of the neck, between the sternocleido-mastoid muscle and the ipsilateral neurovascular bundle, as shown in Figure 1. The aim was to observe any quantitative and/or qualitative change in mobility between fascial layers of the neck region, such as pretracheal and retropharyngeal fascia, during quiet respiration, maximal inspiration-expiration, and swallowing, before and after treatment. Two medical doctors, of 19 and 21 years experience in US screening and diagnosis, were asked to compare the results independently. They were blind to the groups (Experimental and Control) from which the images were obtained. After having randomly viewed and compared the pre- and post- US videos for every NP subject, they were asked to rate any possible change in quality and quantity of the cervical fascia sliding motions as ‘none’, ‘discrete’ or ‘radical’. The values obtained by the first examiner were called Ultrasound Qualitative Scale 1 (US-QS1) results, whereas those collected from the second examiner were called Ultrasound Qualitative Scale 2 (US-QS2) results.
Lumbar and pelvic US screening A similar procedure was applied to LBP subjects: with patients supine, the probe was positioned in the lateral lumbar region, for a sagittal scan. A convex probe was used at 5 MHz and THI. The distance between the superior pole of the right kidney and the origin of the respective diaphragmatic crura (RD distance) was taken during both maximal inspiration (RdI) and maximal expiration (RdE), as shown on Figure 2, before and after treatment (see figure 2) was applied. The aim was to measure and compare
Neck US screening A D.US.T.A.-E. was performed on each subject of the NP Experimental and Sham-Control groups in supine position, with the head, in mild extension and right side-bending-
Table 1 A list of the number of subjects, male (M) and female (F), age range and age mean values for each main group (Experimental and Control) and the respective subgroups (NP and LBP) is shown. Study groups
Subjects M F Age range Age mean
Experimental group
Control group
NP
LBP
NP
LBP
30 24 6 23e48 37,3
30 18 12 21e58 39,1
30 20 10 18e56 39,6
30 22 8 28e52 39
Figure 1 Standard procedure for the neck US screening in NP subjects. The standard procedure for US screening of the neck region for NP sub-groups is shown: the patient lies supine with the head resting on the couch, in a mild extension, and right side-bending-rotation. The probe is positioned on the left antero-lateral region of the neck, between the sternocleidomastoid muscle and the ipsilateral neurovascular bundle, along the sagittal plane. A US recorded video was taken during swallowing, quiet and forced breathing, before and after treatment was applied.
Fascial release effects on patients with non-specific cervical or lumbar pain
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then drink 500 cc. of water an hour before the same session. Bladder filling influences the position and mobility of the bladder neck and the proximal urethra, which are both more mobile when the bladder is nearly empty (Dietz and Wilson, 1999).
Pain assessment
Figure 2 US RD distance measurement on LBP sub-groups. The distance between the superior pole of the right kidney and the origin of the respective diaphragmatic crura was taken during maximal inspiration and expiration in both LBP subgroups, before and after treatment was applied.
pre- to post- range of kidney’s supero-inferior sliding motion, during forced respiration. Successively, the same subjects were also assessed at their pelvic region, in supine position, using the same type of probe. In this case, the probe was always positioned above the pubic symphysis, for transverse and sagittal scanning. The distance between the neck of the bladder and the anterior vesical wall on the perpendicular line (NB distances) was taken during maximal relaxation (NbR) and contraction (NbC) of the pelvic floor muscles, as shown in Figure 3 before and after treatment was applied. All patients were asked to urinate 2 h prior the session and
Pain perception was measured using the Short-Form McGill Pain Assessment Questionnaire (SF-MPQ), a responsive scale giving both reliable and valid data (Melzack, 1987). The SF-MPQ consists in a 15-point descriptor of average pain, articulated in 11 points of sensory experience and 4 of affective experiences. An intensity scale of 0e3 representing mild, moderate or severe pain, is given for each descriptor. The sensory and affective pain rating scores (ranging from 0 to 33 and from 0 to 12 respectively) are added together to give a value for total pain experience (ranging from 0 to 45). The total score has been used as the outcome of this study. The SF-MPQ was administered to every subject on the day of recruitment, as well as three days later.
Osteopathic assessment An Osteopathic assessment was performed by an Osteopath, of 5 years experience, in the symptomatic region of the NP and LBP Experimental subjects, to locate the specific area of major fascial restriction of mobility, respectively in the neck and lumbar regions.
Treatment The Experimental group received MFTs on the painful areas, by the same Osteopath who had previously assessed them. The treatment consisted of application of MFR and FU techniques: MFR treatment MFR consists in the application of a low load, long duration stretch along the lines of maximal fascial restrictions (Barnes, 1990). The latter are palpated by the practitioner and the pressure is applied directly to the skin, into the direction of restriction just until resistance (tissue barrier) is felt. Once found, the collagenous barrier is engaged for 90e120 s, without sliding over the skin or forcing the tissue (Manheim, 2001), until the fascia complex starts to yield and a sensation of softening is achieved.
Figure 3 US NB distance measurement on LBP sub-groups. The distance between the neck of the bladder and the anterior vesical wall, on the perpendicular line, was taken during maximal relaxation and contraction of the pelvic floor muscles in both LBP sub-groups, before and after treatment was applied.
a) For the Experimental NP group: MFR was applied in two stages, for not more then 2 min each. The aim was to release the deep and superficial cervical myofascial structures, having an effect on their reciprocal sliding motion, in both the anterior and the posterior neck region. The hold used with patient supine, was with the operator’s caudal hand on the sternum and the cranial hand on the forehead, when MFR being applied to the anterior neck structures. The cranial hand was supporting the head at the subocciput when MFR was applied to the posterior neck structures (Stanborough, 2004).
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b) For the Experimental LBP group: MFR was applied in two stages, for not more then 2 min each. The aim was to firstly release the right and then left psoas major and minor as well as the iliacus muscles and related lumbar organs, by using the cross-handed hold shown in Figure 4 (Stanborough, 2004). The kidneys are embedded and suspended by the renal fascia that is anatomically related to the diaphragm and psoas fascia, that is in turn a continuation of the thoraco-lumbar fascia (Bogduk, 2005). Secondly, the pelvic floor muscles and related pelvic organs were targeted to be released by the application of MFR through a global pelvic A/P hold. With the patient supine, one operator’s hand on the sacrum, between patient legs, and one hand just above the pubic symphysis (Stanborough, 2004).
FU treatment FU consists in a functional indirect technique: the operator engages the restricted tissues by unfolding the whole pattern of dysfunctional vectors enclosed in the inherent fascial motion. A shearing, torsional or rotational component may arise in a complex three-dimensional pattern that needs to be sensed and unwound until a release is felt (Ward, 2003). a) For the Experimental NP group: MFR treatment was followed by FU of the neck, by using the same holds described above for the MFR technique. The overall FU treatment was applied for not more than 2 min. b) For the Experimental LBP group: MFR treatment was followed by FU of the lumbar and lumbo-pelvic region. With regards to the lumbar region, the hold used is shown on Figure 5. This was applied on both sides. For the pelvic release, the same global A/P hold described above for the MFR technique was used. The overall FU treatment lasted not more than 6 min.
Figure 5 FU hold for LBP Experimental group. The hold used for FU technique applied to the Experimental LBP group is shown: the patient is side lying with the lower leg flexed; the operator behind, facing the patient. The caudal hand supports the upper patient leg with flexed knee. The cranial hand contacts the lateral lumbar region. By using the patient upper leg as a lever, and the cranial hand as a fulcrum, a tissue unwinding is performed aimed to release the psoas muscle, lumbar spine and kidney mobility.
Sham treatment The Sham-Control group blindly received a sham treatment by someone who did not have any knowledge of anatomy or experience in manual therapy whatsoever. a) For the Sham-Control NP group: The sham-osteopath rested his hands on the patient’s neck, for 3 min, by using each of the two A/P holds described above for the MFR technique applied to the Experimental NP group. The sham treatment lasted 6 min in total, as was the case for the Experimental NP group (given by 4 min of MFR and 2 min of FU techniques application). b) For the Sham-Control LBP group: The sham-osteopath rested his hands on the patient’s lumbar and lumbopelvic region, for 4 min, using each of the following holds: left and right cross-hand hold, as shown in figure 4 the global A/P pelvic hold as described above for the MFR technique applied to the Experimental LBP group. The sham treatment lasted 12 min in total, as did the overall treatment for the Experimental LBP group (given by 6 min of MFR and 6 min of FU techniques application).
Ethic committee The research study was approved by the L.U.Me.N.Oli.S ethical committees, related to the institution in which it was performed. All the subjects who took part in the project gave informed consent. Figure 4 MFR hold for LBP Experimental group. The hold used for MFR technique applied to the Experimental LBP group is shown: a cross-handed hold along the psoas, with the cranial hand below the inferior costal margin and the caudal hand above the inguinal region. The aim is to release the psoas and iliacus muscles as well as related lumbar organs.
Statistical analysis All analyses were performed using the software “STATVIEW 5.0” (SAS Institute Inc.) and Microsoft EXCEL for some data graphic representations.
Fascial release effects on patients with non-specific cervical or lumbar pain a) With regards to H1 i) and ii): the results of the US-QS1 and US-QS2 were compared using the Chi square test, with a p value accepted at TrA, but no significant difference was found in muscles between the left and right sides Positive. Asymmetry in the lateral abdominal muscles was found in patients with LBP compared with those without LBP Positive. A significant increase was found in TrA muscle size during static task Positive. A significant difference was found in multifidus muscle size and symmetry between NLB and patients with CLBP Positive. A significant reduction in CSA of MF was found in CLBP group at L5 only.
Review: Application of rehabilitative ultrasound in the assessment of low back pain Table 4
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Details of trials investigating the reliability of US imaging assessment of low back muscle.
Author
Subject (number)
Measuring items (muscle)
Conclusion
Bunce et al. (2002)
NLBP (22)
Thickness (TrA)
McMeeken et al. (2004)
NLBP (9), NLBP (13)
Thickness (TrA)
Watanabe et al. (2004)
NLBP (30)
Thickness (ES)
Teyhen et al. (2005)
LBP (30)
Pressler et al. (2006)
NLBP (30)
Thickness (lateral abdominal) Thickness (MF)
Hides et al. (2007a)
NLBP (19)
Thickness (TrA, IO)
Wallwork et al. (2007)
NLBP (10)
Thickness (MF)
Norasteh et al. (2007)
ALBP (12), NLBP (27)
Thickness (TrA, IO, EO, RA)
Koppenhaver et al. (2009)
NLBP (30)
Thickness (TrA, MF)
Positive. US was found to be a reliable tool for measuring muscle thickness in different positions (both standing and walking) Positive. High ICC was reported for between days reliability (for B mode and for M-mode). The ICC for between transducer reliability was also reported to be high Positive. Sufficient intra-observer and inter-observer reproducibility was found for US imaging in measuring thickness of ES muscles Positive. A high intra-rater reliability of measuring lateral abdominal muscle thickness was achieved Positive. The high between days inter-rater reliability was reported for the right and left sides of multifidus at S1 level Positive. High reliability of a novice rater was demonstrated for some measurement conditions Positive. US was found to be a reliable tool for measuring muscle size. There was no systematic difference in muscle size measured across operators in the measurement of thicknesses at the L2e3 and at the L4e5 vertebral level Positive. US was found to be a reliable tool for measuring muscle thickness in both symptomatic and asymptomatic subjects Positive. US was found to be highly reliable for intra-rater and adequately reliable for inter-raters measurements
ALBP Z acute low back pain, NLBP Z non-low back pain, CSA Z cross-sectional area, exe. Z exercise, IO Z internal oblique, EO Z external oblique, RA Z rectus abdominis, TrA Z transverse abdominis, MF Z multifidus, EMG Z electromagnetic, SEM Z standard error of measurement, ICC Z intra correlation coefficient.
Table 5
Details of trials investigating the validity of US imaging assessment of low back muscle.
Author
Subject (number)
Measuring items (muscle)
Conclusion
Hides et al. (1995)
NLBP (10)
CSA (MF)
Hodges et al. (2003)
NLBP (13)
Architectural parameters (TrA, IO, EI, Ta, Br, Bic)
Ferreira et al. (2004)
LBP (10), NLBP (10)
Thickness (TrA, IO, EO)
McMeeken et al. (2004) Vasseljen et al. (2006)
NLBP(9), NLBP(13) NLBP (10)
Thickness (TrA) and EMG activity Activity onset (MF)
Hides et al. (2006)
NLBP (13)
Thickness (TrA, IO)
Kiesel et al. (2007a)
NLBP (7)
Thickness (MF)
Positive. Significant correlation was found between CSA measurements using US imaging and MRI Positive. US imaging was correlated with EMG findings in detecting low levels of muscles contractions but no correlation was identified in discriminating between moderate and strong contractions Positive. A relationship was found between the presence of LBP and asymmetry of muscle size using US imaging and EMG Positive. A significant correlation was found between US imaging and EMG activity Positive. M-mode US imaging at high time resolution can detect onset of muscle activity comparably accurate to intramuscular EMG Positive. US imaging was correlated with MRI findings in measuring thickness of both TrA and IO muscles Positive. Measuring MF muscle thickness using US imaging was highly correlated with EMG activity of MF in asymptornatic subjects
LBP Z low back pain, NLBP Z non-low back pain, CLBP Z chronic low back pain, CSA Z cross-sectional area, EMG Z electromyography, US Z ultrasonography, MRI Z magnetic resonance imaging, MF Z multifidus Z , TrA Z transverse abdominis, IO Z internal oblique, EO Z external oblique, T.Ant Z tibilias anterior, Br Z brachialis, Bic Z biceps brachii.
474 Some other studies were carried out on patients with LBP. In a study conducted by Norasteh et al. (2007), 12 patients with acute LBP and 27 normal subjects were selected. Within and between days reliability were tested on abdominal muscles in supine, sitting, and standing positions. They reported that there is high reliability on measuring muscle thickness not only in asymptomatic subjects but also in symptomatic subjects. These results suggest that US imaging in chronic LBP is as reliable as in healthy subjects. Together these results suggest US imaging to be a reliable measures in the assessment of lumbar and abdominal muscles, and acceptable for clinical application, in both LBP and normal populations.
Discriminating chronic LBP subjects from non-LBP Some studies focused onto the discrimination of chronic LBP from normal subjects. Results suggest that there is adequate evidence to support US as a valid instrument to detect muscle delayed activation particularly in MF and TrA in chronic LBP (Hides et al., 1994; Ainscough-Potts et al., 2006; Hides et al., 2007b). For example, Hides et al. (1994) compared CSA of MF in 26 patients with acute LBP (aged 17e46) with 51 normal subjects (aged 19e32). In all patients, CSA was measured from the 2nd to the 5th lumbar vertebrae (L2e5) and in six patients at S1 level. In all normal subjects, CSA was measured at L4 and in 10 subjects measurements were made from L2e5. They found marked asymmetry in CSA of MF in patients with the smaller muscle being on the painful side, but there was no correlation between the degree of asymmetry and severity of symptoms. In another study (Lee et al., 2006), CSA of MF was measured in 35 males to identify subjects who suffered from chronic LBP. US images were taken on both sides at the L4 and L5 levels with the subjects in prone lying, upright standing, and 25 and 45 forward stooping. In the control group, the CSA of MF increased from prone lying to upright standing and then gradually decreased from 25 to 45 forward stooping. A reverse pattern of the CSA changes was recorded in patients with chronic LBP. It was reported that MF contracts maximally at upright standing in the normal group, while maximum contraction of the muscle occurs at 25 forward stooping in the patient group. The role of MF may be altered in the stabilization of the lumbar spine of chronic LBP patients. Wallwork et al. (2009) compared both the CSA and the ability to voluntarily perform an isometric contraction of the MF muscle at four vertebral levels in 34 subjects with and without chronic LBP. Results showed a significantly smaller CSA of the MF muscle for the chronic LBP group compared with the unimpaired group at the L5 vertebral level and significantly smaller percent thickness contraction for the chronic LBP group compared with the control group at the L5 vertebral level. All studies investigating the discrimination between chronic LBP patients and non-LBP using US imaging, reported positive results with relatively high rate of identification.
L. Ghamkhar et al. et al., 2006) compared MRI with US imaging measures and five studies (Hodges et al., 2003; Ferreira et al., 2004; McMeeken et al., 2004; Vasseljen et al., 2006; Kiesel et al., 2007a) compared EMG findings with US imaging. Hides et al. (2006) compared two imaging modalities MRI and US imaging used for measurement of the MF thickness. Ten normal females aged 21e31 years were imaged on two separate days using MRI and US imaging. Bilateral measurements were made at each vertebral level from L2 to S1. For both modalities, a significant difference was demonstrated in the CSA of MF between each vertebral level measured. They indicate that if a strict protocol is adhered to, realtime US imaging can be used to document muscle size in young adults and further studies are required to validate the technique in older subjects and in different conditions. Ferreira et al. (2004) compared US imaging with EMG findings to measure trunk muscle activity on patients with LBP and normal subjects. Ten subjects with recurrent LBP and 10 matched controls were tested during isometric low load tasks with their limbs suspended. Changes in thickness from resting baseline values were obtained for TrA, internal oblique, and external oblique using US imaging. Fine wire EMG was used concurrently. Changes in automatic control of TrA were found in people with LBP and US imaging was considered a feasible non-invasive test of automatic recruitment of the abdominal muscles. Validity studies examined a number of different muscles. For example, three studies were carried out on MF (Hides et al., 1995; Vasseljen et al., 2006; Kiesel et al., 2007a), four studies on TrA (Hodges et al., 2003; Ferreira et al., 2004; McMeeken et al., 2004; Hides et al., 2006). Kiesel et al. (2007a) determined the relationship between thickness changes of the lumbar MF, as measured by US imaging and EMG findings in 7 normal subjects. They concluded that muscle thickness change as measured by US imaging was highly correlated with EMG findings of MF activity in asymptomatic subjects (r Z 79, P < 0.001). Hides et al. (2006) validated the use of real-time US imaging as a measure of the TrA muscle during a drawing-in of the abdominal wall of 13 healthy asymptomatic male elite cricket players aged 21.3 2.1 years. They were imaged using MRI and US. US imaging of muscle thickness of TrA was found to be highly correlated with measures obtained with MRI (ICC ranging from 0.78 to 0.95). In another study carried out by McMeeken et al. (2004) there was a high correlation (r Z 0.87, P < 0.001) of change in thickness of TrA between US imaging and EMG findings. Vesseljen et al. (2006) carried out a study to explore whether high-frame rate M-mode US could measure anticipatory muscle responses in the lumbar MF reliably and comparably accurate to intramuscular EMG. On 10 normal subjects, they found M-mode US imaging at high time resolution can detect onset of muscle activity comparably accurate to intramuscular EMG, but with a small systematic delay. These results indicate that US imaging appears to be a valid measure in the assessment of lumbar muscles, and acceptable for clinical application, in both LBP and normal populations, as all studies reported positive results.
Validity
Conclusion As demonstrated in Table 5, seven studies have evaluated the validity of measuring CSA of MF and abdominal muscles using US imaging. Two studies (Hides et al., 1995; Hides
The purpose of this study was to review literature published from 1990 to 2009 concerning the merits of using US imaging
Review: Application of rehabilitative ultrasound in the assessment of low back pain in the examination of back muscle function. There was a wide variation in methodology, procedures, equipment and muscles tested and variability in sample size, differences in degree and source of LBP patients, the physical fitness of individuals, etc. However, a convincing body of evidence suggests that US imaging is a reliable and valid tool for differentiating LBP patients from normal subjects and monitoring rehabilitation outcome measures. Further research regarding the classification of various subgroups of LBP patients and the identification of individuals at risk of developing LBP is needed.
Acknowledgements The authors acknowledge the University of Social Welfare and Rehabilitation Sciences and also Mazandaran University of Medical Sciences for financial support of this study. They are also grateful to Dr. Barbara Richardson at the School of Allied Health Professions, Faculty of Health, University of East Anglia for her valuable and constructive comments.
Conflict of interest None.
References Ainscough-Potts, A.M., Morrissey, M.C., Critchley, D., 2006. The response of the transverse abdominis and internal oblique muscles to different postures. Manual Therapy 11, 54e60. Akbari, A., Khorashadizadeh, S., Abdi, G., 2008. The effect of motor control exercise versus general exercise on lumbar local stabilizing muscles thickness: randomized controlled trial of patients with chronic low back pain. Journal of Back and Musculoskeletal Rehabilitation 21, 105e112. Andersson, G.B., 1999. Epidemiological features of chronic lowback pain. Lancet 354, 581e585. Bergmark, A., 1989. Stability of the lumbar spine. A study in mechanical engineering. Acta Orthopaedica Scandinavia Supplement 230, 1e54. Bunce, S.M., Moore, A.P., Hough, A.D., 2002. M-mode ultrasound: a reliable measure of transversus abdominis thickness? Clinical Biomechanics 17, 315e317. Cairns, M.C., Foster, N.E., Wright, C., 2006. Randomized controlled trial of specific spinal stabilization exercises and conventional physiotherapy for recurrent low back pain. Spine 31, E670eE681. Chhem, R.K., Kaplan, P.A., Dussault, R.G., 1994. Ultrasonography of the musculoskeletal system. Radiologic Clinics of North America 32, 275e289. Cholewicki, J., McGill, S.M., 1996. Mechanical stability of the in vivo lumbar spine: implications for injury and chronic low back pain. Clinical Biomechanics 11, 1e15. Coldron, Y., Stokes, M., Cook, K., 2003. Lumbar multifidus muscle size does not differ whether ultrasound imaging is performed in prone or side lying. Manual Therapy 8, 161e165. Cresswell, A.G., Grundstrom, H., Thorstensson, A., 1992. Observations on intra-abdominal pressure and patterns of abdominal intra-muscular activity in man. Acta Physiologica Scandinavica 144, 409e418. Cresswell, A.G., Oddsson, L., Thorstensson, A., 1994. The influence of sudden perturbations on trunk muscle activity and intraabdominal pressure while standing. Experimental Brain Research 98, 336e341.
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Critchley, D.J., Coutts, F.J., 2002. Abdominal muscle function in chronic low back pain patients: measurement with real-time ultrasound scanning. Physiotherapy 88, 322e332. Danneels, L.A., Coorevits, P.L., Cools, A.M., Vanderstraeten, G.G., Cambier, D.C., Witvrouw, E.E., 2002. Differences in electromyographic activity in the multifidus muscle and the iliocostalis lumborum between healthy subjects and patients with subacute and chronic low back pain. European Spine Journal 11, 13e19. Deyo, R.A., Mirza, S.K., Martin, B.I., 2006. Back pain prevalence and visit rates: estimates from US national surveys, 2002. Spine 31, 2724e2727. Domholdt, E., 2005. Rehabilitation Research: Principles and Applications. Elsevier Saunders, Philadelphia. Eisele, R., Schmid, R., Kinzl, L., Kramer, M., Katzmaier, P., Hartwig, E., 1998. Soft tissue texture analysis by B-modeultrasound in the evaluation of impairment in chronic low back pain. European Journal of Ultrasound 8, 167e175. Ekman, M., Jonhagen, S., Hunsche, E., Jonsson, L., 2005. Burden of illness of chronic low back pain in Sweden: a cross-sectional, retrospective study in primary care setting. Spine 30, 1777e1785. Ferreira, P.H., Ferreira, M.L., Hodges, P.W., 2004. Changes in recruitment of the abdominal muscles in people with low back pain: ultrasound measurement of muscle activity. Spine 29, 2560e2566. Ferreira, M.L., Ferreira, P.H., Latimer, J., et al., 2007. Comparison of general exercise, motor control exercise and spinal manipulative therapy for chronic low back pain: a randomized trial. Pain 131, 31e37. Goldby, L.J., Moore, A.P., Doust, J., Trew, M.E., 2006. A randomized controlled trial investigating the efficiency of musculoskeletal physiotherapy on chronic low back disorder. Spine 31, 1083e1093. Gourmelen, J., Chastang, J.F., Ozguler, A., Lanoe, J.L., Ravaud, J.F., Leclerc, A., 2007. Frequency of low back pain among men and women aged 30 to 64 years in France. Results of two national surveys. Annales de Readaptation et de Medicine Physique 50, 640e644. Harcke, H.T., Grissom, L.E., Finkelstein, M.S., 1988. Evaluation of the musculoskeletal system with sonography. American Journal of Roentgenology 150, 1253e1261. Hart, L.G., Deyo, R.A., Cherkin, D.C., 1995. Physician office visits for low back pain. Frequency, clinical evaluation, and treatment patterns from a US national survey. Spine 20, 9e11. Hides, J.A., Cooper, D.H., Stokes, M.J., 1992. Diagnostic ultrasound imaging for measurement of the lumbar lnultifidus muscle in normal young adults. Physiotherapy Theory and Practice 8, 19e26. Hides, J.A., Stokes, M.J., Saide, M., Jull, G.A., Cooper, D.H., 1994. Evidence of lumbar multifidus muscle wasting ipsilateral to symptoms in patients with acute/subacute low back pain. Spine 19, 165e172. Hides, J.A., Richardson, C.A., Jull, G.A., 1995. Magnetic resonance imaging and ultrasonography of the lumbar multifidus muscle. Comparison of two different modalities. Spine 20, 54e58. Hides, J.A., Richardson, C.A., Jull, G.A., 1996. Multifidus muscle recovery is not automatic after resolution of acute, firstepisode low back pain. Spine 21, 2763e2769. Hides, J.A., Richardson, C.A., Jull, G.A., 1998. Use of real-time ultrasound imaging for feedback in rehabilitation. Manual Therapy 3, 125e131. Hides, J.A., Wilson, S., Stanton, W., McMahon, S., Keto, H., McMahon, K., et al., 2006. An MRI investigation into the function of the transversus abdominis muscle during drawing-in of the abdominal wall. Spine 31, E175eE178. Hides, J.A., Miokovic, T., Belavy, D.L., Stanton, W.R., Richardson, C.A., 2007a. Ultrasound imaging assessment of
476 abdominal muscle function during drawing-in of the abdominal wall: an intrarater reliability study. Journal of Orthopaedic and Sports Physical Therapy 37, 480e486. Hides, J.A., Wong, I., Wilson, S.J., Belavy, D.L., Richardson, C.A., 2007b. Assessment of abdominal muscle function during a simulated unilateral weight-bearing task using ultrasound imaging. Journal of Orthopedic and Sports Physical Therapy 37, 467e471. Hides, J.A., Gilmore, C., Stanton, W., Bohlscheid, E., 2008a. Multifidus size and symmetry among chronic LBP and healthy asymptomatic subjects. Manual Therapy 13, 43e49. Hides, J.A., Stanton, W.R., McMahon, S., Sims, K., Richardson, C.A., 2008b. Effect of stabilization training on multifidus muscle cross-sectional area among young elite cricketers with low back pain. Journal of Orthopaedic and Sports Physical Therapy 38, 101e108. Hodges, P.W., Richardson, C.A., 1996. Inefficient muscular stabilization of the lumbar spine associated with low back pain. A motor control evaluation of transversus abdominis. Spine 21, 2640e2650. Hodges, P.W., Richardson, C., 1997. Contraction of the abdominal muscles associated with movement of the lower limb. Physical Therapy 77, 132e144. Hodges, P.W., Richardson, C.A., 1998. Delayed postural contraction of transversus abdominis in low back pain associated with movement of the lower limb. Journal of Spinal Disorders 11, 46e56. Hodges, P.W., Pengel, L.H.M., Herbert, R.D., Gandevia, S.C., 2003. Measurement of muscle contraction with ultrasound imaging. Muscle and Nerve 27, 682e692. Jin, K., Sorock, G.S., Courtney, T.K., 2004. Prevalence of low back pain in three occupational groups in Shanghai, People’s Republic of China. Journal of Safety Research 35, 23e28. Kaplan, P.A., Matamoros, A., Anderson, J.C., 1990. Sonography of the musculoskeletal system. American Journal of Roentgenology 155, 237e245. Kennelly, K.P., Stokes, M.J., 1993. Pattern of asymmetry of paraspinal muscle slice in scoliosis examined by ultrasound imaging. Spine 18, 913e917. Kiesel, K.B., Uhl, T.L., Underwood, F.B., Rodd, D.W., Nitz, A.J., 2007a. Measurement of lumbar multifidus muscle contraction with rehabilitative ultrasound imaging. Manual Therapy 12, 161e166. Kiesel, K.B., Underwood, F.B., Mattacola, C.G., Nitz, A.J., Malone, T.R., 2007b. A comparison of select trunk muscle thickness change between subjects with low back pain classified in the treatment-based classification system and asymptomatic controls. Journal of Orthopaedic and Sports Physical Therapy 37, 596e607. Kiesel, K.B., Uhl, T., Underwood, F.B., Nitz, A.J., 2008. Rehabilitative ultrasound measurement of select trunk muscle activation during induced pain. Manual Therapy 13, 132e138. Koppenhaver, S.L., Hebert, J.J., Fritz, J.M., Parent, E.C., Teyhen, D.S., Magel, J.S., 2009. Reliability of rehabilitative ultrasound imaging of the transversus abdominis and lumbar multifidus muscles. Archives of Physical Medicine and Rehabilitation 90, 87e94. Koumantakis, G.A., Watson, P.J., Oldham, J.A., 2005. Trunk muscle stabilization training plus general exercise versus general exercise only: randomized controlled trial of patients with recurrent low back pain. Physical Therapy 85, 209e225. Lee, S., Chan, C.K., Lam, T., Lam, C., Lau, N., Lau, R.W., et al., 2006. Relationship between low back pain and lumbar multifidus size at different postures. Spine 31, 2258e2262. Luo, X., Pietrobon, R., Sun, S.X., Liu, G.G., Hey, L., 2004. Estimates and patterns of direct health care expenditures among individuals with back pain in the United States. Spine 29, 79e86.
L. Ghamkhar et al. Mannion, A.F., Pulkovski, N., Gubler, D., Gorelick, M., OuRiordan, D., Loupas, T., et al., 2008. Muscle thickness changes during abdominal hollowing: an assessment of between-day measurement error in controls and patients with chronic low back pain. European Spine Journal 17, 494e501. Martinson, H., Stokes, M.J., 1991. Measurement of anterior tibial muscle size using real-time ultrasound imaging. European Journal of Applied Physiology 63, 250e254. McMeeken, J.M., Beith, I.D., Newham, D.J., Milligan, P., Critchley, D.J., 2004. The relationship between EMG and change in thickness of transversus abdominis. Clinical Biomechanics 19, 337e342. Mohseni-Bandpei, M.A., Watson, M.J., Richardson, B., 2000. Application of surface electromyography in the assessment of low back pain: a literature review. Physical Therapy Reviews 5, 93e105. Mohseni-Bandpei, M.A., Fakhri, M., Bagheri-Nesami, M., AhmadShirvani, M., Khalillan, A.R., Shayesteh-Azar, M., 2006. Occupational back pain in Iranian nurses: an epidemiological study. British Journal of Nursing 15, 914e917. Moheni-Bandpei, M.A., Bagheri-Nesami, M., Shayesteh-Azar, M., 2007. Nonspecific low back pain in 5000 Iranian school-age children. Journal of Pediatric Orthopedics 27, 126e129. Mohseni-Bandpei, M., Fakhri, M., Ahmad-Shirvani, M., Bagheri Nessami, M., Khalilian, A., Shayesteh-Azar, M., et al., 2009. Low back pain in 1100 Iranian pregnant women: prevalence and risk factors. The Spine Journal 9, 795e801. Moseley, G.L., Hodges, P.W., Gandevia, S.C., 2002. Deep and superficial fibers of the lumbar multifidus muscle are differentially active during voluntary arm movements. Spine 27, E29eE36. Norasteh, A., Ebrahimi, E., Salavati, M., Rafiei, J., Abbasnejad, E., 2007. Reliability of B-mode ultrasonography for abdominal muscles in asymptomatic and patients with acute low back pain. Journal of Bodywork and Movement Therapies 11, 17e20. O’Sullivan, P.B., Phyty, G.D., Twomey, L.T., Allison, G.T., 1997. Evaluation of specific stabilizing exercise in the treatment of chronic low back pain with radiologic diagnosis of spondylolysis or spondylolisthesis. Spine 22, 2959e2967. Panjabi, M.M., 1992. The stabilizing system of the spine. I: function, dysfunction, adaptation, and enhancement. Journal of Spinal Disorders 5, 383e389. Pressler, J.F., Heiss, D.G., Buford, J.A., Chidley, J.V., 2006. Between-day repeatability and symmetry of multifidus crosssectional area measured using ultrasound imaging. Journal of Orthopaedic and Sports Physical Therapy 36, 10e18. Raney, N.H., Teyhen, D.S., Childs, J.D., 2007. Observed changes in lateral abdominal muscle thickness after spinal manipulation: a case series using rehabilitative ultrasound imaging. Journal of Orthopaedic and Sports Physical Therapy 37, 472e479. Rankin, G., Stokes, M., Newham, D.J., 2006. Abdominal muscle size and symmetry in normal subjects. Muscle and Nerve 34, 320e326. Richardson, C.A., Jull, G.A., 1995. Muscle control-pain control. What exercises would you prescribe? Manual Therapy 1, 2e10. Sipila, S., Suominen, H., 1993. Muscle ultrasonography and computed tomography in elderly trained and untrained women. Muscle Nerve 16, 294e300. Springer, B.A., Mielcarek, B.J., Nesfield, T.K., Teyhen, D.S., 2006. Relationships among lateral abdominal muscles, gender, body mass index, and hand dominance. Journal of Orthopaedic and Sports Physical Therapy 36, 289e297. Stokes, M.J., Young, A., 1986. Measurement of quadriceps crosssectional area by ultrasonography: a description of the technique and its application in physiotherapy. Physiotherapy Theory and Practice 2, 31e36.
Review: Application of rehabilitative ultrasound in the assessment of low back pain Stokes, M., Rankin, G., Newham, D.J., 2005. Ultrasound imaging of lumbar multifidus muscle: normal reference ranges for measurements and practical guidance on the technique. Manual Therapy 10, 116e126. Stokes, M., Hides, J., Elliott, J., Kiesel, K., Hodges, P., 2007. Rehabilitative ultrasound imaging of the posterior paraspinal muscles. The Journal of Orthopaedic and Sports Physical Therapy 37, 581e595. Teyhen, D.S., Miltenberger, C.E., Deiters, H.M., Deltoro, Y.M., Pulliam, J.N., Childs, J.D., et al., 2005. The use of ultrasound imaging of the abdominal drawing-in maneuver in subjects with low back pain. Journal of Orthopaedic and Sports Physical Therapy 35, 346e355. van Holsbeeck, M., Introcaso, J.H., 1992. Musculoskeletal ultrasonography. Radiology Clinics of North America 30, 907e925. Vasseljen, O., Dahl, H.H., Mork, P.J., Torp, H.G., 2006. Muscle activity onset in the lumbar multifidus muscle recorded simultaneously by ultrasound imaging and intramuscular electromyography. Clinical Biomechanics 21, 905e913.
477
Wallwork, T.L., Hides, J.A., Stanton, W.R., 2007. Intrarater and interrater reliability of assessment of lumbar multifidus muscle thickness using rehabilitative ultrasound imaging. Journal of Orthopaedic and Sports Physical Therapy 37, 608e612. Wallwork, T.L., Stanton, W.R., Freke, M., Hides, J.A., 2009. The effect of chronic low back pain on size and contraction of the lumbar multifidus muscle. Manual Therapy 15, 496e500. Watanabe, K., Miyamoto, K., Masuda, T., Shimizu, K., 2004. Use of ultrasonography to evaluate thickness of the erector spinae muscle in maximum flexion and extension of the lumbar spine. Spine 29, 1472e1477. Wenig, C.M., Schmidt, C.O., Kohlmann, T., Schweikert, B., 2009. Costs of back pain in Germany. European Journal of Pain 13, 280e286. Wilke, H.J., Wolf, S., Claes, L.E., Arand, M., Wiesend, A., 1995. Stability increase of the lumbar spine with different muscle groups: a biomechanical in vitro study. Spine 20, 192e198.
Journal of Bodywork & Movement Therapies (2011) 15, 478e484
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MUSCLE PHYSIOLOGY STUDY
Influence of heat on fatigue and electromyographic activity of the biceps brachii muscle* Wagner Menna Pereira, MSc a, Luiz Alfredo Braun Ferreira, MSc a, Luciano Pavan Rossi, MSc a, Ivo Ilvan Kerpers, MSc a, ´ Collange Grecco St b, Alderico Rodrigues de Paula Jr, PhD c, Luanda Andre Claudia Santos Oliveira, PhD b,* a
Universidade Estadual do Centro-Oeste, Padre Salvador 875, Guarapuava, PR, 85015-430, Brazil Universidade Nove de Julho, Francisco Matarazzo 612, Sa˜o Paulo, SP, 05001-100, Brazil c Universidade do vale do Paraı´ba, Shishima Hifumi 2911, Sa˜o Jose´ dos Campos, SP, 12244-000, Brazil b
Received 10 February 2011; received in revised form 26 April 2011; accepted 30 April 2011
KEYWORDS Electromyography; Fatigue; Biceps brachii; Heat; Microwave diathermy
Summary Electromyography enables registering muscle activity during contraction and can identify muscle fatigue. In the present study, 30 volunteers between 18 and 30 years of age were submitted to an exertion 1 min of maximal voluntary isometric contraction. The electromyographic signal of the biceps brachii muscle and the strength of the flexor muscles of the elbow were determined before and after the administration of microwave diathermy in order to analyze the influence of heat over the strength of the elbow flexor muscles and fatigue of the biceps brachii. The results demonstrate that the strength of the elbow flexor muscles diminished significantly following the application of heat (p < 0.05). Heat also led to a significant reduction in the electrical activity of the muscle studied. The present study demonstrates that microwave diathermy on the biceps brachii muscle reduces the flexion strength of the elbow as well as signs of muscle fatigue in the biceps. ª 2011 Elsevier Ltd. All rights reserved.
Introduction Since 1940, electromyography has been widely used for the understanding of the functions and dysfunctions of the
muscle system during human movement. This resource has enabled research in diverse areas of interest to physiotherapists (Lariviere et al., 2004; Coelho et al., 2008; Valouchouva ´ and Lewitt, 2009). Electromyography allows
*
Study carried out at the Universidade Estadual do Centro-Oeste (UNICENTRO), Brazil. ´ gua Branca, CEP 05001-100, Sa * Corresponding author. Av. Francisco Matarazzo 612, A ˜o Paulo, SP, Brazil E-mail address:
[email protected] (C.S. Oliveira).
1360-8592/$ - see front matter ª 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.jbmt.2011.04.007
Influence of heat on fatigue and electromyographic activity of the biceps brachii muscle recording electrical signals generated by the depolarization of muscle cell membranes, thereby enabling the determination of muscle activity during contraction, although not providing information on the torque produced by the muscles (Ocarino et al., 2005). Electromyographic activity captured through surface electrodes represents the overall activity of the motor units recruited during muscle contraction (Ferreira et al., 2004). There are numerous applications of electromyography in physiotherapy, such as: the investigation of muscle strategies regarding joint stabilization; the study of stretching techniques used in sports and physiotherapy aimed at greater muscle relaxation; the evaluation of muscle activity during functional activities; the characterization of muscle activity during exercise; the analysis of motor unit firing rate; and the identification of muscle fatigue (Gonc ¸alves, 2006). Muscle fatigue is a failure to maintain a desired level of yield or work during a repetitive or sustained activity (Gonc ¸alves, 2006). According to Santos et al. (2003), muscle fatigue has a multi-factor etiology and its origin and extension depend on the specificity of the exercise, type of muscle fiber involved and degree of physical fitness. Muscle fatigue can be defined as a state reached through prolonged, intensive muscle contraction (Oksa et al., 2002). Studies involving athletes performing prolonged sub-maximal exercise demonstrate that muscle fatigue increases in nearly direct proportion to the depletion rate of muscle glycogen (Lariviere et al., 2004). Muscle fatigue during short-duration maximal exercise is associated to a lack of oxygen and an increased level of blood and muscle lactic acid as well as a parallel increase in the concentration of hydrogen in the exercised muscle (Thompson, 1985). According to De Lucca (1997), the electromyographic signal is an index for the determination of the muscle economy and fatigue is an important factor in the characterization of this pattern of movement and its efficiency. Microwave diathermy is indicated prior to kinesiotherapy techniques. The aim is to increase blood flow, remove byproducts of the inflammatory process and improve the range of motion of joints by diminishing stiffness, increasing the extensibility of collagen fibers and enhancing the elasticity of soft tissues (Thompson, 1985; Mayor, 2009). This is a therapy modality that provides heat to soft tissues in a quite satisfactory manner and is used in the prevention and treatment of musculoskeletal injuries (Mayor, 2009; Watson, 2002). However, despite its widespread use in the physiotherapy setting, there is a lack of scientific studies that evaluate the effectiveness of diathermy, the neuro-physiological characteristics of which, such as intravascular vasodilatation, are difficult to measure. A number of studies stress the use of cold and its influence over electromyography (Coelho et al., 2008; Coulange et al., 2006; Pereira, 2008). Madigan and Pidcoe (2001) investigated the influence of temperature on muscle
Table 1
479
fatigue of the flexor group of the elbow through electromyography, demonstrating that a change in the temperature of the muscle has a direct effect on the fatigue process. Pereira (2008) used ice on the tibialis anterior muscle and demonstrated that the reduction in temperature reduced the isometric strength of the muscle and altered its electrical activity. The aim of the present study was to analyze the influence of microwave diathermy over the strength of the flexor muscles of the elbow and fatigue in the biceps brachii muscle through electromyography in the frequency domain.
Materials and methods Sample Thirty healthy male and female volunteers between 18 and 30 years of age with no clinical history of osteoarticular or musculoarticular pain or injury participated in the present study. All volunteers received information on the procedures and objectives of the study and signed terms of informed consent.
Setting The study was conducted at the Biological Signal Processing Laboratory of the Physiotherapy Teaching Clinic of the Universidade Estadual do Centro-Oeste, located in Guarapuava e PR, Brazil.
Procedures The volunteers were initially submitted to a clinical evaluation (medical history and physical exam) in order to ensure the absence of any abnormality of the neuromuscular-articular system and record the anthropometric data (Table 1). The placement of the electrodes was preceded by shaving and cleaning the skin with alcohol in order to reduce bioimpedance. All volunteers underwent a warm-up period in the form of a 5-min walk in order to increase blood flow and muscle nutrition as well as to avoid injuries. The placement of the electrodes was based on the method described by Delagi and Perotto (1980). The subjects were seated, with head and shoulders in a neutral position, without arm support and an electronic goniometer was placed on the elbow such that the joint was set at precisely 90 of flexion, which is the position in which the strength of the biceps brachii is most effective (Always et al., 1992). The individuals were given a period of adaptation to the electrodes and muscle contraction in an effort to achieve greater efficiency in muscle contraction during the exercise.
Anthropometric characteristics of the sample.
Mean Standard deviation
Age (years)
Height (cm)
Weight (kg)
Body mass index
23 2
171 7
68 11
23 3
480 The volunteers were instructed to contract the biceps brachii muscle with isometric flexion of the elbow and no angular movement. Movement was impeded by a chain connected to a load cell fixed to the floor, which aided in the identification of the electrical impulse of the muscle contraction (Figure 1). Upon hearing the “start” signal, the individuals performed a contraction with maximal biceps strength for 60 s. This procedure was carried out on both arms. According to Thompson (1985), a muscle needs a 20-min rest period for the fibers to reacquire their initial structural state for the performance of further maximal voluntary activity. This period was strictly adhered to and the individuals were then submitted to additional maximal contraction of the biceps brachii on both arms, but with the prior administration of microwave diathermy (heat) for 16 min on the dominant arm. The expected circulatory effects caused by diathermy initiate 12e15 min into treatment (Goats, 1999; Low and Reed, 1994; Mitchell et al., 2008). Although previous studies report that the greatest increase in temperature provided by diathermy occurs 20 min into treatment (Draper et al., 1999; Garrett et al., 2000; Mitchell et al., 2008) and this is the most cited time in the literature (Mitchell et al., 2008; Saga et al., 2008; Nosaka et al., 2007), a time of 16 min was established in the present study, as this was the minimal time required to trigger therapeutic physiological effects. Heat was applied to the belly of the biceps brachii muscle through a circular inductive electrode positioned perpendicular to the muscle. The volunteers were instructed to report the sensation of heat, which was not to reach the point of becoming unpleasant.
Instruments An eight-channel electromyograph (EMG System Brazil Ltda) was used for the acquisition of the electromyographic signal, using active, bipolar, differential surface electrodes, connected to the Windaq signal acquisition software program. A load cell (EMG System) with a capacity to
Figure 1 System for determining electromyographic activity of the biceps brachii muscle.
W.M. Pereira et al. measure traction at an intensity of approximately 200 kgf based on transducer strength was used for the determination of traction strength of the elbow flexor muscle group. Microwaves (EFROM 2.45 G MICROWAVE) were administered for 16 min, with the intensity between 50 and 55% of the maximal intensity of the apparatus. The dosimetry suggested fixed times of 3, 8, 16 and 22 min. Two sample channels were used for the analysis of the signal e one for the load cell (kgf) and the other for muscle activation of the biceps brachii muscle. EMG Works Delsys Analysis software program was used for the acquisition of the raw values and visualization of the signal, with a graph of the signal intensity (y axis) and time (x axis), for which the 60-s data collection unit was divided into three 20-s steps. For each 20-s interval (00e20, 20e40 and 40e60), the root mean square (RMS) and median frequency (MF) values were determined and kgf was used for the quantification of the load cell. RMS values in each time interval were organized in tables separated in control limbs and those submitted to heat, along with the MF and load cell (kgf) values. The BioEstat 4.0 software program was used for the analysis of the statistical data. D’Agostino’s test was used to test the normality of the sample. As the sample demonstrated a normal distribution pattern, the Student’s t-test was used for the comparisons, with the level of significance set at 5% (p 0.05).
Results Figure 2 displays the electromyographic signal of the biceps brachii for 60 s, divided into 20-s intervals. Compared to the first evaluation, there was a reduction in peak electromyographic strength in the control limb at all time intervals (00e20; 20e40 and 40e60), but the difference was only statistically significant in the final 20 s (Figure 3). An analysis of the entire 60 s reveals that initial strength was low, reaching maximal intensity between 20 and 40 s and diminishing thereafter. For the limb treated with heat, there was a significant reduction in strength at all time intervals when compared to the evaluation before the administration of the heat. The same behavior was seen in the analysis of the entire 60 s, with an initially low intensity followed by greater peak muscle strength between 20 and 40 s and a reduction in the final 20 s (Figure 4). Figure 5 illustrates the electrical activity in the control muscle, which was similar throughout the 60 s of maximal contraction. There was a slight increase in activity between evaluations in the second (20e40) and third (40e60) intervals when compared to the initial 20 s, but this difference did not achieve statistical significance. For the heat-treated limb, there was a reduction in electromyographic activity after microwave diathermy in all time intervals when compared to the evaluation before the heat treatment, with statistically significant differences in the 00e20 and 20e40 intervals. There was also a uniform drop in muscle activity in both evaluations of the entire 60 s (Figure 6). The median frequency (MF) in the control limb increased on the second evaluation, but this difference did not achieve statistical significance. On both evaluations, there was
Influence of heat on fatigue and electromyographic activity of the biceps brachii muscle
Figure 2
481
Signal sampled for the extraction of the values in different time intervals (00e20, 20e40 and 40e60).
a drop in frequency throughout the entire 60 s of maximal contraction (Figure 7). A similar pattern was found for the heat-treated limb, with an increase in MF between the first and second evaluations and a drop in MF in both evaluations throughout the 60 s of maximal contraction (Figure 8).
Discussion Different muscle groups have been the objects of investigations into muscle fatigue using electromyography (Lariviere et al., 2004; Karlsson et al., 2003; Malachy, 2002). A large number of studies have addressed the biceps brachii muscle in particular (Langenderfer et al., 2005; Ravier et al., 2005; Sbriccoli et al., 2003; Hunter et al., 2003). Seghers and Spaepen (2004) assessed the influence of two exercise protocols on muscle fatigue of the elbow flexor muscles and postulate that muscle fatigue is identified through electromyography by an increase in the
Figure 3 Peak electromyographic strength of control limb (mean standard error); *significant difference in value (kgf) measured by the load cell transducer (p 0.05).
amplitude of the signal and drop in the median frequency (Seghers and Spaepen, 2004). In the present study, there was a drop in MF over the 60 s of data collection, but this drop was not significant. There was a significant reduction in RMS in the heat-treated limb in comparison to the control limb. Silva and Gonc ¸lves (2003) also analyzed signal amplitude and MF for the identification of muscle fatigue and found that the 60-s exertion protocol proved effective for the identification of fatigue. In the present study, an analysis of the electromyographic signal in the frequency domain revealed a reduction in the MF throughout the 60 s of maximal isometric effort. This finding demonstrates muscle fatigue, as the drop in frequency is said to be characteristic of the fatigue process. However, the MF values were higher in the heat-treated muscle when compared to the evaluation prior to the application of the heat as well as when compared to the control muscle. Madigan and Pidcoe (2001) analyzed the influence of a temperature increase on the characteristic of the
Figure 4 Peak electromyographic strength of heat-treated limb (mean standard error); *significant difference in value (kgf) measured by the load cell transducer (p 0.05).
482
Figure 5
W.M. Pereira et al.
RMS value of control limb (mean standard error).
electromyographic characteristics of the vastulateralis in six healthy men with an average age of 30 years and no history of injury to the muscle in question. The authors concluded that an increase in heat led to an increase in the median frequency of the electromyographic signal. The present investigation complements the study cited, as the same relation between the increase in heat and median frequency was found. This phenomenon may be explained by the fact that heat causes vasodilatation, which provides greater blood flow and nutrition to the muscle, allowing it to contract with greater efficiency and increasing the firing rate of the motor units needed for muscle contraction (Thompson, 1985). According to Masuda (1999), median frequency is the parameter least sensitive to noise and most sensitive to physiological and biochemical processes related to sustained contractions and is commonly used in studies on muscle fatigue. The same author also identifies this physiological muscle process based on the sudden drop in the frequency of the electromyographic signal. Gonc ¸alves and Barbosa (2005) analyzed different degrees of exertion on isometric exercises among nine male volunteers. The authors describe a reduction in median frequency and found that an increase in temperature led to a significant increase in the median frequency. In the present study, the biceps brachii muscle submitted to microwave diathermy achieved an increase in median frequency when compared to the control limb, which may be explained by the increase in muscle temperature.
Figure 6 RMS value of heat-treated limb (mean standard error); *significant difference in RMS value (p 0.05).
Figure 7
MF value of control limb (mean standard error).
Farina et al. (2005) analyzed the effect of muscle heating on electromyographic findings and report a directly proportional relationship between the increase in the velocity of muscle nerve conduction and increase in temperature. This process occurs due to electrophysiological alterations, especially an increase in the excitation threshold of the fibers and changes in membrane potential level and permeability, as heat causes an increase in nerve cell metabolism, which leads to a change in cell potential, thereby increasing the velocity of the nerve conduction (Thompson, 1985). Analyzing different muscle groups, Oliveira and Gonc ¸alves (2007) found that amplitude parameters (RMS) were more sensitive than median frequency to alterations caused by fatigue, regardless of the load employed. Regarding the intensity of the electromyographic signal, as demonstrated by the RMS, the present study found that heat caused a significant reduction in electrical activity of the biceps brachii muscle during contraction. Oksa et al. (2002) analyzed the influence of temperature on the electrical activity of the flexor muscles of the arm and found a more intensive increase in electromyographic activation
Figure 8 FM value of heat-treated limb (mean standard error); *significant difference in RMS value (p 0.05).
Influence of heat on fatigue and electromyographic activity of the biceps brachii muscle following the application of ice at a neutral or room temperature. These data demonstrate that an increase in temperature helps to reduce the intensity of the electrical signal and a reduction in temperature leads to an increase in the intensity of the electrical signal during maximal isometric contraction. However, analyzing electromyographic characteristics, Coulange et al. (2006) found no alteration in muscle performance in relation to temperature. As mentioned above, there was a significant difference in the amplitude of the electromyographic signal between the control limb and heat-treated limb, indicating that microwave diathermy led to an important reduction in the intensity of the electromyographic signal. Cardozo and Gonc ¸alves (2003) report that the RMS related to the time domain increased as a result of exercise due to the recruitment and synchronization of motor units in an effort to maintain the level of strength necessary for the exercise and compensate for fatigued motor units. The data from the present study do not corroborate this finding, as there was no significant increase in RMS following the heat treatment, but rather a reduction in the intensity of the electrical signal. During the isometric exercise until the onset of fatigue, there is a time-dependent increase in the electromyographic signal, which confers reliability to the exertion protocol used in the present study (Kumar, 2006; Masuda, 1999; Moritani and Yoshitake, 1998). This increase may occur due to the increase in the amplitude of the action potential, changes in the recruitment order of motor units after the initial seconds of contraction, an increase in motor unit recruitment or an increase in the firing rate of motor neurons. These factors are used as a compensation strategy for the loss of motor function and a sign of muscle fatigue (Sbriccoli et al., 2003; Gonc ¸alves, 2006; Carabajal et al., 2007). In the present study, only the RMS of the biceps brachii muscle was analyzed, whereas muscle strength was assessed using the force read by the load cell, which measured the strength of the elbow flexor muscles, revealing that microwave diathermy led to a significant reduction in the strength of this muscle group. Hunter et al. (2003) analyzed the activation of the elbow flexor muscles during isometric contraction at 90 and found that the load influences muscle performance, demonstrating that the biceps brachii muscle is important to the isometric flexion motion of the elbow. Analyzing muscle performance in the present study, despite the increase in the median frequency of the biceps brachii muscle and increased blood flow due to the heat treatment, there was a reduction in the flexion strength of the elbow. Analyzing the influence of 25% and 50% of maximal isometric strength, Seghers and Spaepen (2004) found that both protocols led to a reduction in strength in 10 healthy adults. These data are similar to those found in the present study, as the individuals exhibited a reduction in maximal isometric strength following the application of heat. Bandeira and Bigaton (2007) analyzed muscle fatigue in the extensor group of the wrist under conditions of normal blood flow and induced ischemia and found a reduction in strength among individuals submitted to the interruption of nutritional blood flow. Based on the findings of the present study, an interruption in blood flow is not the only reason
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for a reduction in isometric strength, as muscle temperature also proved to be an important factor. This should be interpreted with caution, as elbow flexion strength does not depend on the biceps brachii alone but a set of other muscles as well, such as the brachioradialis, round pronator and flexors of the wrist (Always et al., 1992; Gonc ¸alves et al., 2002). Thus, it cannot be affirmed that the microwave diathermy administered in the present study reached the deep muscles. It must be emphasized that the physiological effects (vascular, metabolic and tissue) obtained by the application of deep heat, are not restricted only to microwaves but to other modalities of diathermy, such as short waves. Therefore, we believe that the results obtained regarding fatigue and muscle strength may be identified with other therapeutic diathermy modalities. However, further studies are needed to investigate the reproducibility of the effects using other modalities. Moreover, the anatomy (size and depth) of the particular muscle group should be taken into consideration in the selection of the diathermy modality and parameters used. We believe that the application time should be prolonged with larger and deeper muscle groups. What we do not know is whether the effects described in this study are reproduced with a greater application time, as the peak temperature increases through diathermy occurs approximately 20 min into the application. Another aspect that must be investigated is the length of time the effects persist. Studies are needed to determine whether the effects persist after a series of exercises. Saga et al. (2008) identified a muscle protector effect after a single exercise session, but the same was not reproduced after a second session.
Conclusion Based on the findings of the present study, heat administered through microwave diathermy had an inhibitory effect on muscle fatigue, as determined for the biceps brachii muscle by the median frequency and electromyographic activity (RMS) values, the latter of which underwent a significant reduction. However, microwave diathermy on the biceps brachii led to a significant reduction in the strength of the elbow flexor muscle group, thereby suggesting that heat should not be used prior to any muscle activity that requires a strength yield. Therefore, the indication for use of this resource must take into consideration the expected results from subsequent therapeutic exercises. Although the results obtained in this study are specific to a single diathermy modality and one muscle group, we believe they can be reproduced with other modalities, such as shortwave, and in other muscle groups. Hence, the present study offers a basis for further studies to reinforce the importance of the use of diathermy as a resource for inhibiting fatigue during physical exercise.
Acknowledgements To Conselho Nacional de Desenvolvimento Cientı´fico e Tecno ´lo ´gico (CNPq).
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References Always, S.E., Grumbt, W.H., Stray-Gundersen, J., Gonyea, W.J., 1992. Effects of resistance training on elbow flexors of highly competitive bodybuilders. J. Appl. Physiol. 72, 1512e1521. Bandeira, C., Bigaton, D.R., 2007. Ana ´lise eletromiogra ´fica da fadiga no grupo muscular extensor do punho na isquemia induzida. In: Anais do XII Congresso Brasileiro de Biomeca ˆnica, vol. 4, pp. 940e944. Carabajal, D., La Torre, M., Melo, M., Arau ´jo, L.D., Candotti, C.T., 2007. Comportamento do sinal EMG na recuerac ¸a ˜o de um protocolo de fadgia muscular dos extensores lombares. In: XII Congresso Brasileiro de Biomeca ˆnica. Cardozo, A.C., Gonc ¸alves, M., 2003. Electromyographic fatigue threshold of erector spinae muscle induced by a muscular endurance test in health men. Electromyogr. Clin. Neurophysiol. 43 (6), 377e380. Coelho, M.V.C., Pereira, L.G., Pereira, R., 2008. Crioterapia no tornozelo e atividade eletromiogra ´fica do tibial anterior e fibular durante apoio unipoda ´lico no balancinho. Persp. Onl. 2 (7). Coulange, M., Hug, F., Kipson, N., Robinet, C., Desruelle, A.V., Melin, B., Jimenez, C., Galland, F., Jammes, Y., 2006. Consequences of prolonged total body immersion in cold water on muscle performance and EMG activity. Eur. J. Physiol. 452, 91e101. De Lucca, C.J., 1997. The use of surface electromyography in biomechanics. J. Appl. Biomech. 13 (2), 135e163. Delagi, E.F., Perotto, A., 1980. For the electromyographer: the limbs. Phys. Med. Rehabil. Draper, D.O., Knight, K., Fujiwara, T., Castel, J.C., 1999. Temperature change in human muscle during and after pulsed short-wave diathermy. J. Orthop. Sports Phys. Ther. 29, 13e18. Farina, D., Nielsen, A.L., Nielsen, G.T., 2005. Effectof temperature on spike-triggered average torque and electrophysiological properties of low-threshold motor units. J. Appl. Physiol. 99, 197e203. Ferreira, J.J., Carvalho, L.C., Alexandria, K.C.L., Arau ´jo, Z.T.S., 2004. Atividade Eletromiogra ´fica dos Mu ´sculos Vasto Medial e Lateral Durante Exercı´cios de Extensa ˜o do Joelho. In: Anais do IX Congresso Brasileiro de Biomeca ˆnica, vol. 1, pp. 221e226. Goats, G.C., 1999. Microwave diathermy. Br. J. Sports Med. 24, 212e218. Gonc ¸alves, M., 2006. Eletromiografia e a identificac ¸a ˜o da fadiga muscular. Rev. Bras. Educ. Fı´s. Esp., Sao Paulo 20 (5), 91e93. Gonc ¸alves, M., Barbosa, F.S.S., 2005. Comparac ¸˜ ao entre protocolos de exausta ¸˜ ao da fadiga ˜o e de 30 segundos utilizados na avaliac eletromiogra ´fica dos mu ´sculos eretores da espinha. Rev. Bras. Fisioter. 9 (1), 77e83. Gonc ¸alves, M., Cardozo, A.C., Gauglitz, A.C.F., Malagodi, B.M., 2002. Protocolo biomeca ¸a ˆnico para identificac ˜o da fadiga do mu ´sculo eretor da espinha. Rev. Mot., Rio Claro 8 (3), 29e34. Garrett, C.L., Draper, D.O., Knight, K.L., 2000. Heat distribution in the lower leg from pulsed short-wave diathermy and ultrasound treatments. J. Athl. Train. 35, 50e55. Hunter, S.K., Lepes, R., Macgillis, C.J., Enoka, R.M., 2003. Activation among the elbow flexor muscles differs when maintaining arm position during a fatiguing contraction. J. Appl. Physiol. 94, 2439e2447. Karlsson, J., Ostlund, N., Larson, B., Gerdle, B., 2003. An estimation of the influence of force decrease on the mean power spectral frequency shift of the EMG during repetitive maximum dynamic knee extensions. J. Electr. Kinesiol. 13, 461e468. Kumar, S., 2006. Localized muscle fatigue: review of three experiments. Rev. Bras. Fisioter. 10 (1), 9e28. Langenderfera, J., Lascalza, S., Mell, A., Carpenter, J.E., Kuhn, J.E., Hugues, R.E., 2005. An EMG-driven model of the upper extremity and estimation of long head biceps force. Comput. Biol. Med. 35, 25e39.
W.M. Pereira et al. Lariviere, C., Plamondon, A., Lara, J., Teller, C., Boutin, J., Dagenas, A., 2004. A study of the sensitivity and reliability of electromyographic parameters used to measure the activation and fatigue of different forearm muscles. Int. J. Ind. Ergon. 34, 101e116. Low, J., Reed, A., 1994. Eletroterapia Explicada: Princı´pios e Pra ´¸˜ ao). Editora Manole, Sa tica (3a Edic ˜o Paulo, p. 484. Madigan, M.L., Pidcoe, P.E., 2001. A muscle temperature compensation technique for EMG fatigue measures. Med. Sci. Sports Exerc. 34 (5), 780e784. Malachy, P., 2002. Electromyographic predictors of residual quadriceps muscle weakness after anterior cruciate ligament reconstruction. Am. J. Sports Med. 30, 334e339. Masuda, K., 1999. Changes in surface EMG parameters during static and dynamic fatiguing contractions. J. Electr. Kinesiol. 9, 39e46. Mayor, D., 2009. Electrotherapy: evidence-based practice. Rev. Acupunct. Med. 27, 135e136. Mitchell, S.M., Trowbridge, C.A., Fincher, L., Cramer, J.T., 2008. Effect of diathermy on muscle temperature, electromyografhy, and mechanomy. Muscle Nerv. 38, 992e1004. Moritani, T., Yoshitake, Y., 1998. The use of electromyography in applied physiology. J. Electr. Kinesiol. 8, 363e381. Nosaka, K., Muthalib, M., Lavender, A., Laursen, P.B., 2007. Attenuation of muscle damage by preconditioning with muscle hyperthermia 1-day prior to eccentric exercise. Eur. J. Appl. Physiol. 99, 183e192. Ocarino, J.M., Silva, P.L.P., Vaz, D.V., Aquino, C.F., Bricio, R.S., Fonseca, S.T., 2005. Eletromiografia: interpretac ¸a ¸o ˜o e aplicac ˜es nas cie ¸a ˆncias da reabilitac ˜o. Rev. Fisioter. Bras. 6 (4), 305e310. Oksa, J., Ducharme, M.B., Rintamaki, H., 2002. Combined effect of repetitive work and cold on muscle function and fatigue. J. Appl. Physiol. 92, 354e361. Oliveira, A.S.C., Gonc ¸alves, M., 2007. EMG amplitude and frequency parameters of muscular activity: effect of resistance training based on electromyographic fatigue threshold. J. Electr. Kinesiol. 20, 00e04. Pereira, L.G. 2008. Avaliac ¸˜ ao da atividade eletromiografica e da forc ¸a isome ¸a ´trica ma ´xima do tibial anterior apo ´s aplicac ˜o de crioterapia. Dissertac ¸˜ ao (Mestrado em Bioengenharia) e Instituto de Pesquisa e Desenvolvimento, Universidade do Vale do Paraı´ba, Sa ˜o Jose ´ dos Campos. Ravier, P.A., Buttelli, O., Jennane, R., Couratier, P., 2005. An EMG fractal indicator having different sensitivities to changes in force and muscle fatigue during voluntary static muscle contractions. J. Electr. Kinesiol. 15, 210e221. Saga, N., Kamoto, S., Naito, H., 2008. Effect of heat preconditioning by microwave hyperthermia on human skeletal muscle after eccentric exercise. J. Sports Sci. Med. 7, 176e183. Santos, M.G., Dezan, V.H., Sarraf, T.A., 2003. Bases metabo ´licas da fadiga muscular aguda. Rev. Bras. Cie ˆn. Mov., Brası´lia 11 (1), 7e12. Sbriccoli, A.P., Bazzucchi, I., Rosponi, A., Bernardi, M., De Vito, G., Felici, F., 2003. Amplitude and spectral characteristics of biceps brachii sEMG depend upon speed of isometric force generation. J. Electr. Kinesiol. 13 (2), 139e147. Seghers, J., Spaepen, A., 2004. Muscle fatigue of the elbow flexor muscles during two intermittent exercise protocols with equal mean muscle loading. Clin. Biomech. (Bristol, Avon) 19, 24e30. Silva, S.R.D., Gonc ¸lves, M., 2003. Ana ´lise da fadiga muscular pela amplitude do sinal eletromiogra ´fico. Rev. Bras. Cien. Mov. 11 (3), 15e20. Thompson, L.V., 1985. Effects of age and training on skeletal muscle physiology and performance. Phys. Ther. 74, 71e81. Valouchouva ´, P., Lewitt, K., 2009. Surface electromyography of abdominal and back muscles in patients with active scars. J. of Bod. and Mov.Ther. 13, 262e267. Watson, T., 2002. Current concepts in electrotherapy. Haemophilia 8, 413e418.
Journal of Bodywork & Movement Therapies (2011) 15, 485e495
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EXPERIMENTAL ELECTROMYOGRAPHY STUDY
The influence of kinesiophobia on trunk muscle voluntary responses with pre-programmed reactions during perturbation in patients with chronic low back pain M. Ramprasad, MSPT a,b,*, D. Shweta Shenoy, MSPT, PhD b, Jaspal Singh Sandhu, MS, DSM b, N. Sankara, M.D c a Srinivas College of Physiotherapy and Research Center (SCPTRC), Rajiv Gandhi University of Health Sciences, Mangalore, Karnataka, India b Department of Sports Medicine and Physiotherapy, Guru Nanak Dev University, Amritsar, Punjab, India c Kasturba Medical College (KMC), Mangalore, Karnataka, India
Received 20 June 2010; received in revised form 29 November 2010; accepted 1 December 2010
KEYWORDS Fear of movement; Electromyography; Forceplate; M1-M2 responses; Back pain
Summary The purpose of this study was to examine the relation between fear of movement and perturbation induced electromyographic global trunk muscle voluntary responses with preprogrammed reactions among persons with chronic low back pain (CLBP). CLBP subjects (n Z 25) were challenged to unexpected and expected perturbations on stable and unstable surfaces. ‘Tampa scale for kinesiophobia e Adjusted version-13’ was used to measure kinesiophobia. Regression analysis revealed significant negative correlation between kinesiophobia scores and voluntary responses of rectus abdominis (RA) for unexpected perturbations on stable (r Z 0.69, 95% of CI: 0.85 to 0.40, p < 0.000, r2 Z 0.41) and unstable surfaces (r Z 0.47, 95% of CI: 0.72 to 0.09, p < 0.018, r2 Z 0.29). The activity of erector spinae was not influenced by most of testing conditions in the study except task on unstable surface for expected perturbation (r Z 0.593, 95% of CI: 0.8 to 0.25, p Z 0.002, r2 Z 0.15). RA activity and kinesiophobia score of the CLBP population was significantly inversely associated during anteriorly directed unexpected perturbations. In our study, the significant association between fear of movement and the trunk muscle responses was differentially influenced by expected and unexpected postural demands. ª 2010 Elsevier Ltd. All rights reserved.
* Corresponding author. Department of Sports Medicine and Physiotherapy, Guru Nanak Dev University, Amritsar, Punjab, India. Tel.: þ91 824 2429139, þ91 9343232554; fax: þ91 824 2426766. E-mail address:
[email protected] (M. Ramprasad). 1360-8592/$ - see front matter ª 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jbmt.2010.12.002
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Introduction Low back pain is usually a self-limiting musculoskeletal problem, resolving spontaneously although some individuals progress to chronic low back pain (CLBP) and risk factors associated with this transition have been poorly studied from a biomechanical perspective. A plausible contributing factor to chronic low back pain is poor neuro-motor control of trunk muscles in response to postural exigencies of day-to-day activities. Abnormal longer spinal reflex latencies (feedbackward responses) (Reeves et al., 2009), delayed or absence of feed-forwarded CNS mediated pre-programmed reactions (Tsao and Hodges, 2007, 2008), changes in anticipatory postural adjustments (Jacobs et al., 2009) and inefficient/abnormal trunk muscle responses (Hodges and Richardson, 1996; O Sullivan et al., 1998; MacDonald et al., 2010) were consistently reported in CLBP patients during experimentally stimulated postural tasks. These dysfunctions are believed to be important postural control related biomechanical risk factors for occurrence or recurrence of back pain episodes. More studies have stressed the multidimensional causes and identified over one hundred risk factors e.g., Physical: sedentary lifestyle (Odd Ratio 1.31: 95% CI 1.08e1.58), physically strenuous activities (Odd Ratio 1.22: 95% CI 1.00e1.49) (Heneweer et al., 2009), work and work related psychosocial factors (Macfarlane et al., 2009; Nelson and Hughes, 2009) spinal mechanical load (Bakker et al., 2009) lifting heavy weights (Harkness et al., 2003), extended spinal postures (Mitchell et al., 2009), lifting and bending (Hoogendoorn et al., 2000); Psychological: distress, abnormal back pain beliefs, coping strategies, pain self-efficacy, fear of injury/movement, depression, anxiety, hyper-vigilance, stress, maladaptive cognitions and catastrophizing (Mitchell et al., 2010; Smeets et al., 2009; Feuerstein and Beattie, 1995; Schultz et al., 2002) are all risk factors for developing back pain and also transformation of a current episode of back pain into recurrent chronic back pain (Linton, 2000; Marras, 2000; Marras et al., 1995; Norman et al., 1998; Slater et al., 2009; Hides et al., 1996). This transition was extensively influenced by those psychological risk factors which possess moderate (Pincus et al., 2002) to greater risk (Casey et al., 2008; Hasenbring et al., 2001) for developing chronic back pain. Previous studies have demonstrated that psychological variables such as mental and psychosocial stress in CLBP patients resulted in: [1] Less controlled movements, increased trunk muscle coactivation and significantly increased spinal loading (Davis et al., 2002) and [2] Increased spine compression, lateral shear and differences in trunk muscle co-activation (Marras et al., 2000) during lifting maneuvers. Recently, we examined the role of pre-programmed reactions (PPRs) of global trunk muscles as they relate to the balance response, particularly their role in presetting voluntary responses for regaining postural stability after perturbation (Ramprasad et al., 2010). PPRs are continuously cortically modulated for task demands (Lewis et al.,
M. Ramprasad et al. 2004; Pruszynski et al., 2008; Shemmell et al., 2009) and appear at a latency of higher than 40 ms, but before voluntary muscles respond (w120 ms) to postural perturbation (Latash, 2008). As such, we found that PPR responses were absent ( 29, n Z 12, Low kinesiophobia group: 29 n Z 13). ManneWhitney U test revealed significant difference (Z Z 4.257, P < 0.000) between high kinesiophobia and low kinesiophobia CLBP group (Fig. 3).
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Figure 1 Scatterplots and confidence bands for regression line of mean RMS EMG scores of rectus abdominus muscle in expected (EX(b and d)), unexpected perturbations (UX(a and c)) tasks on stable (ST) and unstable surfaces (US) for kinesiophobia scores of CLBP population.
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Figure 2 Scatterplots and confidence bands for regression line of mean RMS EMG scores of erector spinae muscle in expected (EX(b and d)), unexpected perturbations (UX (a and c)) tasks on stable (ST) and unstable surfaces(US) for kinesiophobia scores of CLBP population.
Test of normality was performed to RA and ES muscles responses of low kinesiophobia group and high kinesiophobia group pertaining to predictor variables tested in this study i.e., stable, unstable surfaces, expected perturbation and unexpected perturbation (2 muscles 2 CLBP groups 2 surfaces 2 types of perturbations Z 16 conditions). ShapiroeWilk test of normality revealed normal distribution of muscle response scores in 15 tested conditions except ES activation on unstable surface, expected perturbation of low kinesiophobia CLBP group (SeW W Z 0.817, p Z 0. 0.011). Hence student t test was performed to find out the difference in trunk muscle responses of normally distributed scores of 15 tested conditions excluding ES muscle response on unstable surface, expected perturbation of low kinesiophobia CLBP group, where ManneWhitney U was performed. To convey the estimated magnitude of relationship between low and high kinesiophobia scores and muscle activity raw mean difference was analyzed. Significantly different peak voluntary responses with preprogrammed reactions were observed between both groups in unexpected perturbations on stable surface [Mean difference (Standard error difference): MD(SED) Z 8.88(1.79), p < 0.001, 95% of CI: 5.16 to 12.6], unstable surface [MD(SED) Z 8.13(2.15), p < 0.001, 95% of CI:
3.67 to 12.6] of rectus abdominus, on stable surface of erector spinae [MD(SED) Z 9.81(4.17), p < 0.028, 95% of CI: 1.17 to 18.45] and not in unstable surface (p < 0.185). ES muscle activity on unstable expected perturbation was found significant between low and high kinesiophobia CLBP group (Z Z 2.339, p Z 0.019). Similar to the regression analysis results, categorical data analysis did not revealed significant pattern of influence between kinesiophobia and ES muscle activity.
Discussion Our study revealed a clear finding that the kinesiophobia scores were inversely associated with the RMS amplitudes of voluntary responses of global abdominal trunk muscles in CLBP population during unexpected anteriorly directed perturbation on stable and unstable surfaces. However erector spinae muscle response to the varieties of perturbation was modestly and differentially influenced by kinesiophobia scores. Our study result were corroborated by the findings of [1] Geisser et al. (2004) who found high pain related fear was significantly associated with reduced lumbar flexion and smaller flexion relaxation ratio
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The box represents the inter-quartile range, which contains the 50% of values. The whiskers are lines that extend from the box to the highest and lowest values, excluding outliers. O = outliers with values. A line across the box indicates the median. N = number of test subjects; L or Low kin.Gr.= Low kinesiophobia group, H or High kin.Gr. = High kinesiophobia group, ST= stable surface, US = unstable surface, UX = unexpected perturbation, EX = expected perturbation, RA = rectus abdominus and ES = erector spinae. Figure 3 Boxplot of kinesiophobia scores and RMS VRPPR EMG values of RA and ES muscle responses of CLBP subjects on varieties of stable, unstable, unexpected and expected perturbation tasks.
[2] Thomas et al. (2008) reported CLBP patients high in pain related fear specifically avoid activation of the abdominal muscles during maximal isometric trunk exertions and [3] Lamoth et al. (2004) reported fear of pain and induced pain had subtle effects on ES EMG activity during walking. The interesting observation in our study was elevated significant and non-significant ES muscle response to most perturbation tasks compared to the pattern of significant lower mean RMS RA muscle responses in all tasks and particularly to unexpected perturbation tasks (Fig. 3). Similar increase in EMG activity of ES muscle during trunk flexion was reported in previous studies (Ershad et al., 2009; Van Diee ¨n et al., 2003) emphasizing the use of greater antagonistic co-contraction for spinal stability to control the trunk flexion in CLBP population (Franklin and Granata, 2007). However ES activity was influenced minimally below 16% (Fig. 2d) and negatively during complex tasks such as unstable and expected perturbation (r Z 0.593, p Z 0.002, r2 Z 0.15). However it must acknowledged that there was a higher mean difference in ES muscle activity compared to RA muscle activity between both the CLBP groups on
stable, unexpected perturbation than unstable expected perturbation (Fig. 3). This finding reveals that ES muscle activity during postural demands was differentially influenced by and surface related factors and governed by various other factors not tested in our study. The outcome was quite similar before (Regression analysis) and after splitting up the data except one additional task was found significant in ES muscle activity i.e., unstable expected perturbation task after curving up. No clear significant relationship of patterns between ES muscle activity and kinesiophobia scores was found on the two different analyses. We found kinesiophobia scores had significant influence on abdominal muscle responses elicited during unexpected perturbation rather than expected perturbation. One explanation might be the anteriorly directed, visually cued load release used in this study for perturbation tasks. Sudden postural adjustments with reduced trunk flexion (Geisser et al., 2004) and associated abdominal muscle responses, produced during anticipated unexpected (unknown time of weight release) upper extremity loading tasks, on stable and unstable surfaces, was negatively influenced by kinesiophobia scores. However the anticipated perturbation, with prior known time of weight release, was not influenced by kinesiophobia scores. One
492 possible explanation is that attention was focused away from the pain during expected perturbation and on pain during unexpected perturbation (Butler et al., 2010). Our findings support the hypothesis proposed by Kronshage et al. (2001) and Leonhardt et al. (2009) that increased scores of fear of movement is associated with specific movement avoidance, perceived as a dangerous component of a task, rather than general task avoidance. Studies have reported similar findings i.e., decreased muscle activation for pain related fear during trunk extensioneflexion task, a weight lifting task and submaximal isometric upper extremity physical task in trunk and upper scapular muscles (Crombez et al., 1999a, 1999b; Nederhand et al., 2006). Caution is warranted while interpreting studies using the methods described above. (Marras and Davis, 2001). This is because EMG protocols with isometric EMG exertions (Sub-maximal voluntary contraction) and flexion relaxation ratio were innately associated with problems in normalization, motivational aspects and movement execution errors respectively. The striking difference in our study was pragmatic perturbation methodology to test the muscle activation and fear of movement simulating daily life’s postural demands i.e., perturbation method not influenced by the above mentioned factors. Some aspects of our methodology warrant discussion related to our results. First, the manual perturbation method adopted in our study and the need for a control group with healthy individuals. Despite the fact that weight release-perturbation method was a manual process, it was found to result in authentic fair voluntary responses from trunk muscles by diverting the participant’s attention to follow the weight release. The intra-class correlation coefficient (ICC (Two way mixed effects)) showed fair reproducibility of RA (ICC Z 0.4, 95% of CI: 0.34 to 0.78) and ES (ICC Z 0.3, 95% of CI: 0.43 to 0.77) EMG muscle responses over different perturbations. Our study results have many research and clinical implications. The main research implication of this study is that trunk muscle evaluation without controlling fear of movement or fear avoidance beliefs in CLBP may lead to abnormal findings and conflicting predictions on responses of trunk muscle during various activities. Therefore, more attention is needed to address fear related factors in methodological (inclusion, exclusion and matching criteria of participants) as well as statistical issues (e.g., covariates, predictors and confounders) while evaluating trunk muscle responses of CLBP population. In the clinical perspective of fear of movement, two important issues need to addressed while rehabilitating high and low fear sub-group of CLBP population 1] missing defense in low fear CLBP sub-group which may lead to higher muscle activation and 2] high fear of movement associated with abnormal lower muscle activation in the agonist muscle of this subgroup of CLBP group. Early rehabilitation should focus on finding the specific movement dysfunction associated with high fear and gradual training may lead to reduction in abnormal trunk muscle response in these patients. Low fear CLBP group can be trained for specific exercises focusing on postural alignment, postural control reactions or mimicking postural control strategies. These specific exercises targeting pre-programmed reactions may contribute to fine tuning of voluntary responses at the cortical level necessary
M. Ramprasad et al. for postural demands and adjustments (Pedersen et al., 2007). On the other hand, studies reported that CLBP patients were found with decreased (5e11%) prefrontal and thalamic gray-matter density and disruptions in functional connectivity of cortical regions despite performing the task equally as well as controls (Marwan et al., 2008; Apkarian et al., 2004). Hence it is important to identify, evaluate and intervene in psychological variables such as fear avoidance beliefs, depressive mood, maladaptive pain related coping strategies, mental stress, tendency to catastrophize and appraisals of control and to identify their influence on CLBP, as this may significantly change muscle response by reducing pain intensity, disability (Waddell et al., 1993; Woby et al., 2004) and further reduce the risk that transient symptoms might develop into chronic illness (Lundberg, 2003, 1999). We propose that along with cortical functional disruptions and CNS related modulation dysfunction in presetting the voluntary response, a phase of high fear of movement with lesser muscular excursions, and a phase of low fear of movement with higher peak muscle responses, may act as a cycle leading to chronic LBP. Further with the absence of cortically modulated fine tuning, sudden trunk movements to postural adjustments may result in abnormal amplitudes of global trunk muscle responses in a sub-group of CLBP patients. These abnormal muscular responses may induce abnormal translation of vertebrae causing impingement in the neutral zone and may result in spinal instability (White and Panjabi, 1990). Klenerman et al. (1995) and Vlaeyen and Linton (2000) proposed that pain related fear was a potent precursor for developing chronic low back pain from an episode of acute low back pain. In addition Klenerman et al. (1995) predicted 66% of acute sufferers went on to become CLBP, using fear-avoidance variable alone in their study. Interestingly prospective cohort studies support this notion. Carragee et al. (2005) with 5 year follow-up study, predicted development of serious LBP in patients with both structural and psychosocial risk factors by examining baseline psychosocial variables. Further a study by Feyer et al. (2000) with 4 year prospective follow-up found psychological distress to be a significant etiologic and prognostic factor for CLBP. Van Nieuwenhuyse et al. (2006) revealed relative risk of 1.8 for the high scores of pain related fear in the development of low back pain. More studies are needed on the bio-behavioral factors (Feuerstein and Beattie, 1995; Iezzi et al., 1992) particularly fear of movement and their influence on functional cortical activation and muscle related modulation dysfunction. This may reveal the relative contribution of these factors in development of CLBP. Further integrated studies focusing on temporal partitioning of EMG activation patterns i.e., short, long latency reflexes and voluntary responses during postural demands and kinesiophobia induced relative modulation on the above temporal entities may provide more insight and hopefully contribute to the prevention of CLBP from an acute episode. Cognitive-behavioral interventions should be coherently and coordinatedly given along with essential physical therapy interventions or vice versa and or personalized to the need of this population. In other words, periodic kinesiophobia evaluation and cognitive-behavioral evaluation
Kinesiophobia measurement with minimal clinically important difference score can be used to progress the graded exercise therapy interventions or with combined therapy approaches (George et al., 2004; Monticone et al., 2008). More randomized control trials in this area may provide deeper understanding of the combination of these therapies in CLBP rehabilitation.
Conclusion Our study confirms that kinesiophobia in CLBP patients differentially influences trunk muscle activation levels during sudden postural demands. The findings of this study provide preliminary data on specific muscle activation dysfunction during perturbation-induced postural demands in CLBP patients, further substantiating the evidence that fear of movement is associated with specific movements rather than whole task.
Clinical implications C
C
Early and periodic screening to identify kinesiophobia, fear of pain and the nature of fear avoidance beliefs in acute, sub-acute and chronic back pain patients can be helpful in detailed physical examination, to choose and change the course of interventions in CLBP population particularly with non-specific LBP pathologies possibly without further referral and diagnostic procedures. Physical therapy interventions optimizing high kinesiophobia induced specific movement dysfunction or low kinesiophobia associated with abnormal global trunk muscle amplitudes can be tailored with cognitivebehavioral evaluation for prescribing and progressing graded exercises for cost-effective management and an early recovery.
Acknowledgements The authors thank A Shama Rao Foundation, Mangalore and Srinivas, Wenlock, ESI and Port-Trust Hospitals, Mangalore and Narayanan, M.S.P.T., Anup Johney, M.S.P.T., for their profound assistance in carrying out the study. Thanks to Selvamani, M.P.T., Balasubramanian, M.P.T., John Varghese, M P T for assisting statistical works, manuscript preparation, revisions and anonymous reviewers for their inputs. There are no conflicts of interest for the authors and the outcome of this study. This project was supported in part with a grant from SCPTRC, Mangalore, Karnataka, India.
References Apkarian, A.V., Sosa, Y., Sreepadma, S., Robert, M., Levy, R., Norman, H., Todd, B., Parrish, D., Gitelman, R., 2004. Chronic back pain is associated with decreased prefrontal and thalamic gray matter density. The Journal of Neuroscience 24 (46), 10410e10415. Asenlof, P., Soderlund, A., 2010. A further investigation of the importance of pain cognition and behaviour in pain rehabilitation: longitudinal data suggest disability and fear of movement are most important. Clinical Rehabilitation 24 (5), 422e430.
493 Bakker, E.W., Verhagen, A.P., van Trijffel, E., Lucas, C., Koes, B.W., 2009. Spinal mechanical load as a risk factor for low back pain: a systematic review of prospective cohort studies. Spine 15 (8), E281eE293. Bonnet, M., 1983. Anticipatory changes of long-latency stretch responses during preparation for directional hand movements. Brain Research 28, 51e62. Butler, H.L., Lariviere, C., Hubley-Kozey, C.L., Sullivan, M.J., 2010. Directed attention alters the temporal activation patterns of back extensors during trunk flexion-extension in individuals with chronic low back pain. European Spine Journal 19 (9), 1508e1516. Carragee, E.J., Alamin, T.F., Miller, J.L., Carragee, J.M., 2005. Discographic, MRI and psychosocial determinants of low back pain disability and remission: a prospective study in subjects with benign persistent back pain. Spine Journal 5 (1), 24e35. Casey, Y.C., Greenberg, M.A., Nicassio, P.M., Harpin, R.E., Hubbard, D., 2008. Transition from acute to chronic pain and disability: a model including cognitive, affective, and trauma factors. Pain 2008 (134), 69e79. Clark, M.E., Haig, A.J., Colwell, M.O., 1999. Kinesiophobia and chronic pain: psychometric characteristics and factor analysis of the Tampa Scale. American Pain Society Abstracts 15, 77. Crombez, G., Eccleston, C., Baeyens, F., Van Houdenhove, B., Van den, B.A., 1999a. Attention to chronic pain is dependent upon painrelated fear. Journal of Psychosomatic Research 47, 403e410. Crombez, G., Vlaeyen, J.W., Heuts, P.H., Lysens, R., 1999b. Painrelated fear is more disabling than pain itself: evidence on the role of pain-related fear in chronic back pain disability. Pain 80, 329e339. Davis, K.G., Marras, W.S., Heaney, C.A., Waters, T.R., Gupta, P., 2002. The impact of mental processing and pacing on spine loading. Spine 27 (23), 2645e2653. Elfving, B., Andersson, T., Grooten, W.J., 2007. Low levels of physical activity in back pain patients are associated with high levels of fear-avoidance beliefs and pain catastrophizing. Physiotherapy Research International 12 (1), 14e24. Ershad, N., Kahrizi, S., Abadi, M.F., Zadeh, S.F., 2009. Evaluation of trunk muscle activity in chronic low back pain patients and healthy individuals during holding loads. Journal of Back Musculoskeletal Rehabilitation 22 (3), 165e172. Feuerstein, M., Beattie, P., 1995. Bio-behavioral factors affecting pain and disability in low back pain: mechanisms and assessment. Physical Therapy 75, 267e280. Feyer, A., Herbison, P., Williamson, A.M., de Silva, I., Mandryk, J., Hendrie, L., Hely, M.C.G., 2000. The role of physical and psychological factors in occupational low back pain: a prospective cohort study. Occupational and Environmental Medicine 57, 116e120. Franklin, T.C., Granata, K.P., 2007. Role of reflex gain and reflex delay in spinal stability-A dynamic-simulation. Journal of Biomechanics 40, 1762e1767. Fritz, J.M., George, S.V., 2002. Identifying psychosocial variables in patients with acute work-related low back pain: the importance of fear-avoidance beliefs. Physical Therapy 82 (10), 973e983. Fritz, J.M., George, S.Z., Delitto, A., 2001. The role of fearavoidance beliefs in acute low back pain: relationships with current and future disability and work status. Pain 94 (1), 7e15. Geisser, M.E., Haig, A.J., Colwell, M.O., 1999. Fear of movement/reinjury and functional activity during physical therapy evaluation among persons with chronic low back pain. American Pain Society Abstracts 18, 176. Geisser, M.E., Haig, A.J., Wallbom, A.S., Wiggert, E.A., 2004. Painrelated fear, lumbar flexion, and dynamic EMG among persons with chronic musculoskeletal low back pain. The Clinical Journal of Pain 20, 61e69. George, S.Z., Bialosky, J.E., Fritz, J.M., 2004. Physical therapist management of a patient with acute low back pain and elevated fear-avoidance beliefs. Physical Therapy 84, 538e549.
494 Granata, K.P., Slota, G.P., Bennet, B.C., 2004. Paraspinal muscle reflex dynamics. Journal of Biomechanics 37, 241e247. Grotle, M., Vøllestad, N.K., Veierød, M.B., Brox, J.I., 2004. Fearavoidance beliefs and distress in relation to disability in acute and chronic low back pain. Pain 112 (3), 343e352. Harkness, E.F., Macfarlane, G.J., Nahit, E.S., Silman, A.J., McBeth, J., 2003. Risk factors for new-onset low back pain amongst cohorts of newly employed workers. Rheumatology 42 (8), 959e968. Hasenbring, M., Hallner, D., Klasen, B., 2001. Psychological mechanisms in the transition from acute to chronic pain: overor underrated? Schmerz 15 (6), 442e447. Heneweer, H., Vanhees, L., Picavet, H.S., 2009. Physical activity and low back pain: a U-shaped relation? Pain 143, 21e25. Hides, J.A., Richardson, C.A., Jull, G.A., 1996. Multifidus muscle recovery is not automatic after resolution of acute, firstepisode low back pain. Spine 21, 2763e2769. Hodges, P.W., Bui, B.H., 1996. A comparison of computer-based methods for the determination of onset of muscle contraction using electromyography. Electroencephalography and Clinical Neurophysiology 101, 511e519. Hodges, P.W., Richardson, C.A., 1996. Inefficient muscular stabilization of the lumbar spine associated with low back pain; a motor control evaluation of transversus abdominis. Spine 21, 2640e2650. Hoogendoorn, W.E., Bongers, P.M., De Vet, H.C., Douwes, M., Koes, B.W., Miedema, M.C., Arie ¨ns, G.A., Bouter, L.M., 2000. Flexion and rotation of the trunk and lifting at work are risk factors for low back pain: results of a prospective cohort study. Spine 23, 3087e3092. Iezzi, A., Adams, H.E., Stokes, G.S., Pilon, R.N., Ault, L.C., 1992. An identification of low back pain groups using biobehavioral variables. Journal of Occupational Rehabilitation 2, 1. Jacobs, J.V., Henry, S.M., Nagle, K.J., 2009. People with chronic low back pain exhibit decreased variability in the timing of their anticipatory postural adjustments. Behavioral Neuroscience 123 (2), 455e458. Klenerman, L., Slade, P.D., Stanley, I.M., 1995. The prediction of chronicity inpatients with an acute attack of low back pain in a general practice setting. Spine 20, 478e484. Kori, S.H., Miller, R.P., Todd, D.D., 1990. Kinisophobia: a new view of chronic pain behavior. Pain Management 3, 35e43. Kronshage, U., Kroener-Herwig, B., Pfingsten, M., 2001. Kinesiophobia in chronic low back pain patients e Does the startle paradigm support the hypothesis? International Journal of Behavioral Medicine 8 (4), 304e318. Lamoth, C.J., Daffertshofer, A., Meijer, O.G., Moseley, L.G., Wuisman, P.I., Beek, P.J., 2004. Effects of experimentally induced pain and fear of pain on trunk coordination and back muscle activity during walking. Clinical Biomechanics 19 (6), 551e563. Latash, M.L., 2008. Pre-programed reactions. In: Neurophysiological Basis of Movement, second ed. Human kinetics, Leeds. Leeuw, M., Goossens, M.E., Linton, S.J., Crombez, G., Boersma, K., Vlaeyen, J.W., 2007. The fear-avoidance model of musculoskeletal pain: current state of scientific evidence. Journal of Behavioral Medicine 30 (1), 77e94. Leonhardt, C., Lehr, D., Chenot, J.F., Keller, S., Luckmann, J., Basler, H.D., Baum, E., Donner-Banzhoff, N., Pfingsten, M., Hildebrandt, J., Kochen, M.M., Becker, A., 2009. Are fearavoidance beliefs in low back pain patients a risk factor for low physical activity or vice versa? A cross-lagged panel analysis. Psycho-social Medicine 29, 6. Lewis, G.N., Polych, M.A., Byblow, W.D., 2004. Proposed cortical and sub-cortical contributions to the long-latency stretch reflex in the forearm. Experimental Brain Research 156, 72e79. Linton, S., 2000. A review of psychological risk factors in back and neck pain. Spine 25, 1148e1156.
M. Ramprasad et al. Lundberg, U., 1999. Stress responses in low-status jobs and their relationship to health risks: musculoskeletal disorders. Annals of New York Academy of Sciences 896, 162e172. Lundberg, U., 2003. Psychological stress and musculoskeletal disorders: psychobiological mechanisms. Lack of rest and recovery greater problem than workload. Lakartidningen 22 (21), 1892e1895. MacDonald, D., Moseley, G.L., Hodges, P.W., 2010. People with recurrent low back pain respond differently to trunk loading despite remission from symptoms. Spine 1 (7), 818e824. Macfarlane, G.J., Pallewatte, N., Paudyal, P., Blyth, F.M., Coggon, D., Crombez, G., Linton, S., Leino-Arjas, P., Silman, A.J., Smeets, R.J., Van der Windt, D., 2009. Evaluation of work-related psychosocial factors and regional musculoskeletal pain: results from a EULAR Task Force. Annals of the Rheumatic Diseases 68 (6), 885e891. Marras, W.S., 2000. Occupational low back disorder causation and control. Ergonomics 43, 880e902. Marras, W.S., Davis, K.G., 2001. A non-MVC EMG normalization technique for the trunk musculature: part 1. Method development. Journal of Electromyography and Kinesiology 11, 1e9. Marras, W.S., Davis, K.G., Heaney, C.A., Maronitis, A.B., Allread, W.G., 2000. The influence of psychosocial stress, gender, and personality on mechanical loading of the lumbar spine. Spine 25 (23), 3045e3054. Marras, W.S., Lavendar, S.A., Leurgans, S.E., 1995. Biomechanical risk factors for occupationally related low back disorder risk. Ergonomics 38, 377e410. Marwan, N., Baliki, P.Y., Geha, A., Apkarian, V., Dante, R.C., 2008. Beyond feeling: chronic pain hurts the brain, disrupting the default-mode network dynamics. The Journal of Neuroscience 28 (6), 1398e1403. Meyer, K., Tschopp, A., Sprott, H., Mannion, A.F., 2009. Association between catastrophizing and self-rated pain and disability in patients with chronic low back pain. Journal of Rehabilitation Medicine 41 (8), 620e625. Mitchell, T., O’Sullivan, P.B., Burnett, A., Straker, L., Smith, A., Thornton, J., Rudd, C.J., 2010. Identification of modifiable personal factors that predict new-onset low back pain: a prospective study of female nursing students. Clinical Journal of Pain 26 (4), 275e283. Mitchell, T., O’Sullivan, P.B., Smith, A., Burnett, A.F., Straker, L., Thornton, J., Rudd, C.J., 2009. Biopsychosocial factors are associated with low back pain in female nursing students: a cross-sectional study. International Journal of Nursing Studies 46, 678e688. Monticone, M., Montironi, C., Tomba, A., Righini, C., Nido, N., Giovanazzi, E., 2008. Effectiveness of a rehabilitation and occupational behavioral cognitive group intervention for chronic low back pain with low disability. Prospective study with a 6-month follow-up. Giornale Italiano di Medicina del Lavoro ed Ergonomia 30 (2), 162e168. Moseley, G.L., Zalucki, N., Birklein, F., Marinus, J., van Hilten, J.J., Luomajoki, H., 2008. Thinking about movement hurts: the effect of motor imagery on pain and swelling in people with chronic arm pain. Arthritis & Rheumatism 59 (5), 623e631. Nederhand, M.J., Hermens, H.J., Ijzerman, M.J., Groothuis, K.G., Turk, D.C., 2006. The effect of fear of movement on muscle activation in posttraumatic neck pain disability. Clinical Journal of Pain 22 (6), 519e525. Nelson, N.A., Hughes, R.E., 2009. Quantifying relationships between selected work-related risk factors and back pain: a systematic review of objective biomechanical measures and cost-related health outcomes. International Journal of Industrial Ergonomics 1 (1), 202e210. Norman, R.W., Wells, R.P., Neumann, P., Frank, J., Shannon, H., Kerr, M.A., 1998. Comparison of peak versus cumulative work exposure risk factors for the reporting of low back pain in the automotive industry. Clinical Biomechanics 13, 561e573.
Kinesiophobia measurement Noth, J., Schwarz, M., Podoll, K., Motamedi, F., 1991. Evidence that low-threshold muscle afferents evoke long-latency stretch reflexes in human hand muscles. Journal of Neurophysiology 65, 1089e1097. O’Sullivan, P.B., Twomey, L., Allison, G.T., 1998. Altered abdominal muscle recruitment in patients with chronic back pain following a specific exercise intervention. Journal of Orthopedic and Sports Physical Therapy 1998 (27), 114e124. Pedersen, M.T., Essendrop, M., Skotte, J.H., Jørgensen, K., Schibye, B., Fallentin, N., 2007. Back muscle response to sudden trunk loading can be modified by training among healthcare workers. Spine 32, 1454e1460. Picavet, H.S., Vlaeyen, J.W., Schouten, J.S., 2002. Pain catastrophizing and kinesiophobia: predictors of chronic low back pain. American Journal of Epidemiology 156 (11), 1028e1034. Pincus, T., Burton, A.K., Vogel, S., Field, A.P., 2002. A systematic review of psychological factors as predictors of chronicity/disability in prospective cohorts of low back pain. Spine 1 (5), E109eE120. Pruszynski, J.A., Kurtzer, I., Scott, S.H., 2008. Rapid motor responses are appropriately tuned to the metrics of a visuospatial task. Journal of Neurophysiology 100, 224e238. Ramprasad, M., Shweta, S.D., Jaspal, S.S., Sankara, N., Joseley, S.R.P., 2010. The magnitude of pre-programmed reaction dysfunction in back pain patients - experimental pilot electromyography study. Journal of Back and Musculoskeletal Rehabilitation 23 (2), 77e86. Reesor, K.A., Craig, K.D., 1988. Medically incongruent chronic back pain: physical limitations, suffering, and ineffective coping. Pain 32 (1), 35e45. Reeves, N.P., Cholewicki, J., Narendra, K.S., 2009. Effects of reflex delays on postural control during unstable seated balance. Journal of Biomechanics 19 (2), 164e170. Schultz, I.Z., Crook, J.M., Berkowitz, J., Meloche, G.R., Milner, R., Zuberbier, O.A., Meloche, W., 2002. Biopsychosocial multivariate predictive model of occupational low back disability. Spine 1 (23), 2720e2725. Shemmell, J., An, J.H., Perreault, E.J., 2009. The differential role of motor cortex in stretch reflex modulation induced by changes in environmental mechanics and verbal instruction. Journal of Neuroscience 21, 13255e13263. Slater, M.A., Weickgenant, A.L., Greenberg, M.A., Wahlgren, D.R., Williams, R.A., Carter, C., Patterson, T.L., Grant, I., Garfin, S.R., Webster, J.S., Atkinson, J.H., 2009. Preventing progression to chronicity in first onset, subacute low back pain: an exploratory study. Archives of Physical Medicine Rehabilitation 90 (4), 545e552. Smeets, R.J., Maher, C.G., Nicholas, M.K., Refshauge, K.M., Herbert, R.D., 2009. Do psychological characteristics predict response to exercise and advice for subacute low back pain. Arthritis Rheumatism 27 (9), 1202e1209.
495 Swinkels-Meewisse, I.E., Roelofs, J., Schouten, E.G., Verbeek, A.L., Oostendorp, R.A., Vlaeyen, J.W., 2006. Fear of movement/(re) injury predicting chronic disabling low back pain: a prospective inception cohort study. Spine 31 (6), 658e664. Thomas, J.S., France, C.R., Sha, D., Wiele, N.V., 2008. The influence of pain-related fear on peak muscle activity and force generation during maximal isometric trunk exertions. Spine 15 (11), 342e348. Tsao, H., Hodges, P.W., 2007. Immediate changes in feedforward postural adjustments following voluntary motor training. Experimental Brain Research 4, 537e546. Tsao, H., Hodges, P.W., 2008. Persistence of improvements in postural strategies following motor control training in people with recurrent low back pain. Journal of Electromyography and Kinesiology 18, 559e567. Van Diee ¨n, J.H., Cholewicki, J., Radebold, A., 2003. Trunk muscle recruitment patterns in patients with low back pain enhance the stability of the lumbar spine. Spine 15 (8), 834e841. Van Nieuwenhuyse, A., Somville, P.R., Crombez, G., Burdorf, A., Verbeke, G., Johannik, K., Van den Bergh, O., Masschelein, R., Mairiaux, P., Moens, G.F., 2006. BelCoBack Study Group. The role of physical workload and pain related fear in the development of low back pain in young workers: evidence from the BelCoBack Study; results after one year of follow up. Occupational and Environmental Medicine 63 (1), 45e52. Vlaeyen, J.W., Crombez, G., 1999. Fear of movement/(re)injury, avoidance and pain disability in chronic low back pain patients. Manual Therapy 4, 187e195. Vlaeyen, J.W., Kole-Snijders, A.M., Boeren, R.G., Van Eek, H., 1995. Fear of movement/(re)injury in chronic low back pain and its relation to behavioral performance. Pain 62, 363e372. Vlaeyen, J.W., Linton, S.J., 2000. Fear-avoidance and its consequences in chronic musculoskeletal pain: a state of the art. Pain 85, 317e332. Waddell, G., Newton, M., Henderson, I., Somerville, D., Main, C.J., 1993. A fear- avoidance beliefs questionnaire (FABQ) and the role of fear-avoidance beliefs in chronic low back pain and disability. Pain 52, 157e168. Watson, P.J., Booker, C.K., Main, C.J., 1997. Surface electromyography in the identification of chronic low back pain patients: the development of the flexion relaxation ratio. Clinical Biomechanics 3, 165e171. White, A.A., Panjabi, M.M., 1990. The problem of clinical instability in the human spine: a systematic approach, part 4: the lumbar and lumbosacral spine. In: Clinical Biomechanics of the Spine, second ed.. JB Lippincott Co, New York, pp. 342e361. Woby, S.R., Watson, P.J., Roach, N.K., Urmston, M., 2004. Adjustment to chronic low back painethe relative influence of fear-avoidance beliefs, catastrophizing, and appraisals of control. Behaviour Research and Therapy 42 (7), 761e774.
Journal of Bodywork & Movement Therapies (2011) 15, 496e501
available at www.sciencedirect.com
journal homepage: www.elsevier.com/jbmt
SENSORY-MOTOR REHABILITATION
Analysis of electromyographic activity of ankle muscles on stable and unstable surfaces with eyes open and closed* Luiz Alfredo Braun Ferreira, MSc a, Wagner Menna Pereira, MSc a, Luciano Pavan Rossi, MSc b, Ivo Ilvan Kerpers, MSc b, Alderico Rodrigues de Paula Jr, PhD a, Claudia Santos Oliveira, PhD c,* a
Universidade do Vale do Paraı´ba (UNIVAP), Brazil Universidade Estadual do Centro-Oeste (UNICENTRO), Brazil c Universidade Nove de Julho (UNINOVE), Brazil b
Received 22 September 2009; received in revised form 23 August 2010; accepted 3 September 2010
KEYWORDS Electromyography; Ankle; Proprioception
Summary Introduction: Proprioceptive exercises are performed on a daily basis in physiotherapy with the use of different unstable platforms in order to improve joint stability using the mechanical and sensory properties of ligaments, joint capsule and integrated activity of the muscles surrounding the joint. Changes in the myoelectrical characteristics of the muscles during activity can be identified using surface electromyography (EMG), which provides important information on the behavior of muscles submitted to different types of load. Objectives: The aim of the present study was to analyze the electromyographic activity of the tibialis anterior, tibialis posterior, peroneus longus, gastrocnemius lateralis and gastrocnemius medialis on stable and unstable surfaces with eyes open and closed. Methodology: Twenty-five active, healthy, male and female individuals were submitted to an anthropometric evaluation and a protocol involving warm up and the electromyographic assessment of muscle activity on different surfaces. The order of the data collection was chosen randomly by lots [on stable ground or unstable platforms (trampoline, balance platform, proprioceptive disk and proprioceptive board) with eyes open and on a trampoline, balance platform and stable ground with eyes closed]. The individuals remained balanced on these surfaces for 15 s with the knee at 30 flexion in order to provide greater instability. Results: There was a significant increase (p < 0.05) in muscle activity on the unstable surfaces, with the exception of the trampoline, which did not achieve statistically significant differences
*
Study carried out at the Universidade Estadual do Centro-Oeste UNICENTRO. ´gua Branca, Sa * Corresponding author. UNINOVE, Av. Francisco Matarazzo, 612, A ˜o Paulo 05001-100, Brazil. E-mail address:
[email protected] (C.S. Oliveira).
1360-8592/$ - see front matter ª 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jbmt.2010.09.003
Analysis of electromyographic activity of ankle muscles on stable and unstable surfaces with eyes open and closed
497
in relation to the stable ground. The tibialis anterior and peroneus longus exhibited the greatest electromyographic activity on all surfaces. The proprioceptive tests performed with eyes closed exhibited significantly greater electromyographic activity than with eyes open. Conclusion: Proprioceptive exercises on unstable surfaces generated a significant increase in electromyographic activity, especially with eyes closed, and are therefore a valuable resource in the sensory-motor rehabilitation of the ankle. ª 2010 Elsevier Ltd. All rights reserved.
Introduction A number of studies have investigated both the extrinsic and intrinsic risk factors of sprained ankles (Mchugh et al., 2006). One of the most challenging aspects for practitioner is understanding the role of mediated proprioceptive neuromuscular control following an injury and restoration through rehabilitation. Proprioception contributes toward the precise delineation of the motor programming necessary to the neuromuscular control of movement and muscle reflexes, thereby providing dynamic joint stability. Ligament trauma and proprioceptive functional deficiency lead to mechanical instability, which could ultimately lead to microtrauma and further injury (Lephart et al., 1997). Balance is defined in two forms e static and dynamic. Static and dynamic balance is maintained by the vestibular (inner ear, cochlear nerves, pathways and interrelation in the central nervous system), visual and proprioceptive systems, with the sensory receptors located in joints, muscles and tendons (Horak and Shupert, 1994; Lee and Aronson, 1974). Disorders in one or more of these systems affect balance. The vestibular system contributes toward maintaining the body in equilibrium as well as coordinating the movements of the head and body. However, vestibular signals alone are not capable of providing information to the central nervous system (Horak and Shupert, 1994). The vestibular system participates in the accurate processing of sensory information regarding postural movements, thereby fulfilling multiple functions in postural control (Buzatti et al., 2007). The visual system assists in the maintenance and orientation of an erect posture. The conscious and unconscious correction of posture is possible through visual inputs. Although the visual system is an important reference source of verticality and for the maintenance of the natural oscillation of the body within the limits of stability, it is not essential to postural control, as it is possible to maintain one’s balance with one’s eyes closed (Horak and Shupert, 1994). The proprioceptive system describes the awareness of posture, movement and changes in balance. This system is a specialized variation of the sense of touch and encompasses sensations of joint movement (kinesthesia) sense of joint position (Willems et al., 2002). When these three systems are in harmony, there is perfect spatial orientation, with eye and spinal reflexes appropriate to the automatic, unconscious maintenance of postural control. Moreover, in structures placed in disequilibrium, as in the case of the ankle, there are both static and dynamic reflexive protection mechanisms. Electromyography (either alone or in combination with other biomechanical methods) offers important information on the behavior of muscles when submitted to different types
of load as well as diverse execution angles and velocities (Silva and Gonc ¸alvez, 2003). This method also assesses myoelectric behavior under different circumstances, such as body and room temperature, neuromuscular training, etc (Weller et al., 1998; Oksa et al., 2002; Racinais et al., 2005; Shin et al., 2006). Functional training on unstable platforms is an important aspect of neuromuscular rehabilitation and conditioning and consequently furnishes improvement in coordination and the neuromuscular recruitment pattern (Stronjnik et al., 2002). During physical training, the instability of movement places joints in situations of risk. Thus, the activation of proprioceptive impulses that are integrated in various sensorymotor centers regulates adjustments in the contraction of postural muscles, thereby maintaining general postural balance (Cooke, 1980). Considering the need for determining protocols for the identification of muscle activity in proprioceptive exercises through surface electromyography, the aim of the present study was to analyze the electromyographic activity of tibialis anterior, tibialis posterior, peroneus longus, gastrocnemius lateralis and gastrocnemius medialis (anklestabilizing muscles) on stable and unstable ground with eyes open and closed.
Materials and methods This study was carried out at the Physiotherapy Clinic of the hospital of the Universidade Estadual do Centro-Oeste (city of Guarapuava, Parana ´, Brazil). Twenty young, healthy adults between 19 and 24 years of age (10 males and 10 females) from a total of 40 subjects participated in the study. Selection of the participants was based on the following inclusion criteria: age between 18 and 28 years; no distinction regarding ethnic background or gender; active individuals that did not participate in proprioceptive training or balance exercises; and a sports background. The exclusion criteria were musculoskeletal pathology, neuro-degenerative or infectious disease, chronic ankle instability, recent ankle sprain, vestibular pathology and visual impairment. All participants were informed as to the procedures of the experiment and signed terms of informed consent in compliance with the Norms for Research on Human Subjects (National Health Council Resolution n 196/96). The study received approval from the Ethics Committee of the Universidade do Vale do Paraı´ba (n H 50/CEP/2008). The tibialis anterior, tibialis posterior, peroneus longus, gastrocnemius lateralis and gastrocnemius medialis were chosen for analysis due to their being considered muscles of key activity during monopodal support (Moore and Dalley, 2001; Smith et al., 1997). The non-use of the soleus muscle in the present study is justified by the fact that it is
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a tonic postural muscle and constantly activated when standing on either one or both feet (Smith et al., 1997). Tests were performed with eyes open and closed on both stable and unstable surfaces. Tables 1e3 display the anthropometric data on the participants. Data collection on unstable (trampoline and balance platform) and stable surfaces with eyes open and closed were carried out randomly by lots regarding the order of the exercises to impede motor learning. Active bipolar electrodes were placed at a distance of 20 mm from center to center (Hermens, 1999). Trichotomy and cleaning of the areas were first performed in order to reduce bioimpedance, based on the recommendations of the Surface Electromyography for the Non-Invasive Assessment of Muscles (Hermens, 1999). The placement of the electrodes followed the anatomical reference method described by Delagi and Perotto (1980). An additional electrode was placed over the bone protuberance to serve as a neutral reference point, thereby diminishing external signals and noises. The reference electrode is necessary in order to have a common reference for the differential amplifier and should be placed, whenever possible, over an electrically neutral tissue (generally a bone protuberance) (De Luca, 1997). The ability of the amplifier to reject signals common to both inputs is called the ratio of common-mode rejection (RRMC). For the best record, filters are available that remove unwanted frequencies using high pass, low pass and band pass (Ocarino et al., 2005; Correa et al., 2003). Each individual warmed up for 5 min on a treadmill, following the guidelines of the American College of Sports Medicine e ACSM (2007), which recommends warm up prior to any physical activity or exercise. The assessment of muscle activity was performed on the dominant leg with the subject barefoot and the other leg lifted off the ground with the knee in semi-flexion. For greater muscle activation, a 30 angle of knee flexion on the support leg was standardized using a goniometer in order to avoid the lock and screw mechanism on the knee, which would lend greater stability to the ankle. Data collection time for electromyographic activity was 15 s on all types of surface, with a 1-min rest period between readings, totaling an average of 10 1 min of collection time. An eight-channel electromyograph (EMG System Brasil Ltda.) with active, bipolar, differentiated surface electrodes was used for the acquisition of the electromyographic signal. The electromyograph was connected to the Windaq signal acquisition software program, with the signal passing through a 20e500 Hz band pass filter, amplified 1000 times and converted by an A/D board with a sampling frequency of 2000 Hz for each channel and an input variation of 5 mV. The data were analyzed using the Matlab 7.0 signal processing program (MatWorks) and Origin 7.0 program
Table 1
Age (years)
Height (cm)
Weight (kg)
BMI
21 1
170 6
64 11
22 3
Mean standard deviation of anthropometric characteristics.
Characteristics of the sample of men.
Mean Standard Error
Age (years)
Height (cm)
Weight (kg)
BMI
21 1
170 6
73 8
24 2
Mean standard deviation of anthropometric characteristics.
(Massachusetts, USA). Descriptive and inferential statistics were performed using the Statistical Package for the Social Sciences 13.0 (SPSS, Illinois, USA). The Sharpiro-Wilk test was used to determine the normality of the data, with a 5% level of significance (p 0.05). As some variables did not exhibit normal distribution, the non-parametric Wilcoxon test was used for the comparison of mean values, with a 5% level of significance (p 0.05).
Results The results are presented as mean and standard error for the inferential statistics in relation to the mean amplitude values of the electromyographic signal (root mean square) of the tibialis anterior, tibialis posterior, peroneus longus, gastrocnemius lateralis and gastrocnemius medialis during the different perturbation exercises (Table 4). Figure 1 shows that the gastrocnemius medialis muscle exhibited no significant difference (p > 0.05) in values between eyes open and closed. Figure 2 displays the muscle activity on the trampoline, revealing considerable activity in the tibialis anterior and peroneus longus with eyes closed. In contrast, median activity occurred in the other muscles. All values were significant (p < 0.05) for the muscles analyzed. Figure 3 displays the electromyographic activity between eyes open and closed on the balance platform, revealing greater activity for all muscles in comparison to the other types of surface, with the greatest activity in the tibialis anterior and peroneus longus. However, the gastrocnemius medialis exhibited no significant difference (p > 0.05) in values between eyes open and closed. Thus, the tibialis anterior and peroneus longus exhibited the greatest activation in comparison to the other muscles, regardless of the type of ground. This demonstrates that both muscles are important dynamic stabilizers of the ankle joint, with the tibialis anterior acting as an invertor and dorsiflexor and the peroneus longus acting as an evertor and plantar flexor. The function of inversion and eversion should be stressed, as most unstable grounds have lateral-medial instability. This may explain why these two muscles were more active during all the perturbation exercises.
Table 3
Characteristics of the sample.
Mean Standard Error
Table 2
Characteristics of the sample of women.
Mean Standard Error
Age (years)
Height (cm)
Weight (kg)
BMI
21 1
170 6
56 7
21 2
Mean standard deviation of anthropometric characteristics.
Analysis of electromyographic activity of ankle muscles on stable and unstable surfaces with eyes open and closed Table 4
499
Significance values (p < 0.05) of all exercises performed compared to the stable ground.
BALANCE TRAMPOLINE BALANCE (EC) TRAMPOLINE (EC) STABLE (EC)
TA
PL
LG
GM
TP
0.000227 0.038432 4.8E-10 3.52E-10 2.83E-07
0.000222 0.092328 6.67E-07 2.85E-07 3.14E-07
2.23E-05 0.162251 3.42E-08 4.43E-06 5.16E-06
0.008667 0.339999 3.43E-07 0.001334 0.010681
3.37E-06 0.318043 9.3E-11 1.58E-05 4.26E-05
Underlined values were not statistically significant (p > 0.05); EC: Eyes Closed; TA: Tibialis anterior; PL:Peroneus longus; LG: Gastrocnemius lateralis; GM: Gastrocnemius medialis; TP:Tibialis posterior.
In the analysis of the total mean values on the different types of ground (Figure 4), the results reveal greater muscle activation with eyes closes in comparison to eyes open, especially on the balance platform. The data obtained using the trampoline merits attention, as similar muscle activity to that on stable ground with eyes open was demonstrated; however, when the visual system was inhibited, the electromyographic activity increased significantly (Figure 4). Figure 5 depicts the comparison of electromyographic activity between men and women, revealing no significant difference in muscle activity between genders, as the data on the gastrocnemius medialis between genders achieved a p-value of 0.0561.
Discussion No studies were found in the literature using the same characteristics and variables analyzed in the present investigation. However, there are studies assessing muscle reaction time, muscle activation on different types of ground and muscle activity following proprioceptive training on unstable ankles (Osborne et al., 2001; Cunha and Bonfim, 2007). There were no significant gender differences in the present study, which demonstrates the homogeneity of the sample. This lack of gender difference may be explained by the fact that the individuals had similar physical characteristics, such as a body mass index within the ideal range
Figure 1 Variation in electromyographic activity (root mean square) between eyes open and eyes closed on stable ground (Mean Standard Error); ) No significant difference in electromyographic activity (p > 0.05)
and a low standard deviation, as well as by the independent comparison of the electromyographic activity in a single individual on the different unstable surfaces. The greatest source of ankle mechanoreceptors is believed to be in the ligaments, which are responsible for the proprioception and maintenance of joint stability. The presence of Ruffini endings, Pacinian corpuscles and Golgi tendon organs in the ligaments of the ankle has been demonstrated histologically (Verhagen et al., 2005). Thus, exercises on unstable ground generate rapid changes in the length of the ankle ligament due to the stimulation of the joint on multiple planes of movement, thereby generating afferent stimuli and reflexive motor responses in order to produce rapid joint stability (Myers et al., 2003). According to Oliveira et al. (2006), the aim of this type of training is to induce unforeseen perturbation, thereby stimulating the stabilization reflex and the production of agonist-antagonist co-contraction. A previous electromyographic study assessed the tibialis anterior and gastrocnemius medialis in five individuals during the use of two balance platform models on different supports. The results revealed greater myoelectrical activity in the gastrocnemius medialis in comparison to the tibialis anterior during tests with the feet both closer together and further apart on both types of proprioceptive boards (Oliveira et al., 2006). In contrast, the tibialis anterior exhibited greater electromyographic activity on both stable and unstable ground in the present study and was the most solicited muscle.
Figure 2 Variation in electromyographic activity (root mean square) between eyes open and eyes closed on trampoline (Mean Standard Error); all values denote significant difference in electromyographic activity (p < 0.05)
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Figure 3 Variation in electromyographic activity (root mean square) between eyes open and eyes closed on balance platform (Mean Standard Error); ) No significant difference in electromyographic activity (p > 0.05)
Other studies stress the importance of the visual system regarding postural control in humans. Lee and Aronson (1974) carried out an experiment in order to understand the effect of the visual system on the control of the body. The authors investigated visual information by moving a suspended “room” in which the roof and lateral walls were able to move. Adults and children remained standing in this room while it was moved and the corresponding body oscillations were observed, demonstrating the considerable influence of the visual system over postural control (Lee and Aronson, 1974). Mochizuki et al. (2007) determined factors that influence the co-modulation rate of the motor unit load in the soleus muscle of both legs in a standing position with eyes open and closed and vibration on the calcaneus tendon. The results revealed that the common program for motor neurons of the two muscles exhibited no difference between standing up with eyes open or closed, but there were significant differences in relation to vibration. These results suggest that proprioception and subcortical inputs contribute toward the co-modulation of the activation rate of the pairs of muscle units in the soleus muscle of the right and left leg during static posture.
Figure 5 Variation in electromyographic activity (root mean square) between men and women on unstable ground (Mean Standard Error); No significant difference in electromyographic activity in all comparisons (p > 0.05); TA: Tibialis anterior; PL:Peroneus longus; LG: Gastrocnemius lateralis; GM: Gastrocnemius medialis; TP:Tibialis posterior
The present study investigated the effect of visual and proprioceptive information on muscle activation in the ankle regarding the maintenance of static balance in healthy young adults. The results reveal that, through sensory deprivation or perturbation, ankle muscles vary in activity, which is in agreement with previous studies. Thus, we can readily see the importance of the visual system in the proprioceptive action of the body, stressing its role in postural control and possible implications for the rehabilitation process.
Conclusion The results of the present study reveal a significant increase in muscle activity on the majority of unstable surfaces in comparison to stable ground, with a significantly greater increase when the eyes are closed, except in the gastrocnemius medialis. The techniques employed therefore proved effective in activating ankle muscles and are of fundamental importance to the sensory-motor rehabilitation of this joint. Further studies are needed for the analysis of the influence of different surfaces, different types of data collection and the removal of the visual system during other types of exercises in order contribute scientific knowledge regarding the influence of proprioceptive training over the performance of the protective musculature of the ankle.
References
Figure 4 Total mean electromyographic activity with eyes open and closed on different surfaces (Mean Standard Error)
American College of Sports Medicine e ACSM, 2007. Physical activity and public health: update recommendation for adults from de American College of Sports Medicine and the American Heart association. Med. Sci. Sports Exerc. 39 (8), 1423e1434.
Analysis of electromyographic activity of ankle muscles on stable and unstable surfaces with eyes open and closed Buzatti, D.R.P., et al., 2007. Reabilitac ¸a ˜o Vestibular. Revista Fisioterapia Brasil 8 (1) jan/feb. Cooke, J.D., 1980. The role of stretch reflexes during active movements. Brain Res. 181, 493e497. Correa, P.P., Santos, P.M., Veloso, A., 2003. Electromiografia: fundamentac ¸a ˜o fisiolo ´gica, me ´todos de recolha, processamento e aplicac ¸o ¸o ˜es cinesiolo ´gicas. Edic ˜es FMH, Lisboa. Cunha, P.L., Bonfim, T.R., 2007. Ativac ¸˜ ao eletromiogra ´fica em exercı´cios sobre a prancha de equilı´brio. Revista Fisioterapia Brasil 8, 192e197. De Luca, C.J., 1997. The use of surface electromyography in biomechanics. J. Appl. Biomech. 13 (2), 135e163. Delagi, E.F., Perotto, A., 1980. For the electromyographer: the limbs. Phys. Med. Rehabil.. Hermens, H.J., 1999. European Recommendations for Surface Electromyography e SENIAM 16e17. Horak, F.B., Shupert, C., 1994. The role of the vestibular system in postural control. In: Vestibular Rehabilitation. FA Davis, New York, pp. 22e46. Lee, D.N., Aronson, E., 1974. Visual proprioceptive control of standing in human infants. Percept Psychophys 15 (3), 529e532. Lephart, S.M., Pincivero, D.M., Giraido, J.L., Fu, F.H., 1997. The role of proprioception in the management and rehabilitation of athletic injuries. Am. J. Sports Med. 25, 130. Mchugh, M.P., Tyler, T.F., Tetro, D.T., Mullaney, M.J., Nicholas, S.J., 2006. Risk factors for Noncontact ankle sprains in high School Athletes: the role of Hip strength and balance ability. Am. J. Sports Med 34, 464. Mochizuki, G., Ivanova, T.D., Garland, S.J., 2007. Factors affecting the Common modulation of bilateral motor unit discharge in human soleus muscles. J. Neurophysiol. 97, 3917e3925. Moore, K., Dalley, A., 2001. Anatomia orientada para clinica, 4 ed Rio de Janeiro: Guanabara Koogan. Myers, J.B., Riemann, B., Hwang, J., et al., 2003. Effect of peripheral afferent alteration of the lateral ankle ligaments on dynamic stability. Am. J. Sports Med. 31 (4), 498e506. Ocarino, J.M., Silva, P.L.P., Vaz, D.V., Aquino, C.F., Brı´cio, R.S., Fonseca, S.T., 2005. Eletromiografia: interpretac ¸˜ ao e
501
aplicac ¸o ¸a ˜es nas cie ˆncias da reabilitac ˜o. Revista Fisioterapia Brasil 6 (4), 305e309. Oksa, J., Ducharme, M.B., Rintama ¨ki, H., 2002. Combined effect of repetitive work and cold on muscle function and fatigue. J. Appl. Physiol. 92, 354e361. Oliveira, F.B., et al., 2006. Avaliac ¸a ˜o de dois modelos de ta ´bua proprioceptiva com dois tipos de apoios por meio da eletromiografia de superfı´cie. Fisioterapia Brasil 7 (3) Maio/Junho. Osborne, M.D., Chou, L.S., Laskowski, E.R., Smith, J., Kaufman, K.R., 2001. The effect of ankle disk training on muscle reaction in subjects with a history of ankle sprain. Am. J. Sports Med. 29 (5), 627e632. Racinais, S., Blonc, S., Jonville, S., Hue, O., 2005. Time of day influences the environmental effects on muscle force and contractility. Med. Sci. Sports Exerc. 37 (2), 256e261. Shin, H.K., Cho, S.H., Lee, Y.H., Kwon, O.Y., 2006. Quantitative EMG changes during 12 week DeLorme’s axiom strength training. Yonsei Med. J. 47 (1), 93e104. Silva, S.R., Gonc ¸alvez, M., 2003. Comparac ¸a ˜o de Protocolos para Verificac ¸a ˜o da Fadiga Muscular pela Eletromiografia de Superfı´cie. Motriz, Rio Claro 3 9 (1), 51e58. Smith, L., Weiss, E., Lehmkuhl, D., 1997. Cinesiologia Clı´nica de Brunnstrom, 5a ed. Editora Manole, Sa ˜o Paulo. Stronjnik, V., Vengust, R., Pavlovic, V., 2002. The effect of proprioceptive training on neuromuscular function in patients with patellar pain. Cell Mol. Biol. Lett. 7 (1), 170e171. Verhagen, E., Van Der Beek, A., Twisk, A., Bouter, L., Bahr, R., Van Mechelen, W., 2005. An economic evaluation of a proprioceptive balance board training programme for the prevention of ankle sprains in volleyball. Br. J. Sports Med. 39, 111e115. Weller, A.S., Greenhaff, P.L., Macdonald, I.A., 1998. Physiological responses to moderate cold stress in man and the influence of prior prolonged exhaustive exercise. Exp. Physiol. 83, 679e695. Willems, T., Witvrouw, E., Verstuyft, J., et al., 2002. Proprioception and muscle strength in subjects with a history of ankle sprain and chronic instability. J. Athl Train. 37 (4), 487e493.
Journal of Bodywork & Movement Therapies (2011) 15, 502e506
available at www.sciencedirect.com
journal homepage: www.elsevier.com/jbmt
PILOT STUDY
Reliability testing of the patellofemoral joint reaction force (PFJRF) measurement in taped and untaped patellofemoral conditions during single leg squatting: A pilot study Javid Mostamand, MSc PT, PhD a,*, Dan L. Bader, DSc b, ¨ Hudson, PhD, MCSP c Zoe a
Musculoskeletal Research Centre, Isfahan University of Medical Sciences, PO Box 164, Isfahan 8174673461, Iran Department of Engineering, Queen Mary University of London, Mile End Road, London E1 4NS, UK c Centre for Sports and Exercise Medicine, Barts and the London Queen Mary’s School of Medicine and Dentistry, Mann Ward, Mile End Hospital, Bancroft Road, London E1 4DG, UK b
Received 3 October 2010; received in revised form 23 November 2010; accepted 2 December 2010
KEYWORDS Patellofemoral pain syndrome; PFJRF reliability test; Patellar taping
Summary Introduction: Measuring patellofemoral joint reaction forces (PFJRF) may provide reliable evidence for patellar taping to correct probable malalignment in subjects with anterior knee pain, or patellofemoral pain syndrome (PFPS). The aim of the present study was to examine the reliability of PFJRF measurements in different patellofemoral conditions during squatting in healthy subjects. Methods: Using a motion analysis system and one forceplate, PFJRF of eight healthy subjects was assessed during single leg squatting. Data was collected from superficial markers taped to selected landmarks. This procedure was performed on the right knees, before (BT), during (WT) and shortly after patellar taping (SAT). The PFJRF was calculated using a biomechanical model of the patellofemoral joint. Results: The results revealed that, there were no significant differences between the PFJRF mean values for three conditions of BT (2100.55 455.25), WT (2026.20 516.45) and SAT (2055.35 669.30) (p > 0.05). The CV (coefficient of variation), ICC (intra class correlation coefficient), LSD (least significant difference) and SEM (standard error of measurement) values revealed the high reliability of PFJRF measurements during single leg squatting (p < 0.05).
* Corresponding author. Tel.: þ98 311 792 2024; fax: þ98 311 6687270. E-mail addresses:
[email protected] (J. Mostamand),
[email protected] (D.L. Bader),
[email protected] (Z. Hudson). 1360-8592/$ - see front matter ª 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jbmt.2010.12.004
Reliability testing of the patellofemoral joint reaction force
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Conclusion: The high reliability of PFJRF measurements reveals that the future studies could rely on these measurements during single leg squatting. ª 2010 Elsevier Ltd. All rights reserved.
Introduction Patellofemoral pain syndrome (PFPS) is the most common diagnosis when there is knee joint pain in the young adults (Crossley et al., 2002). It is hypothesized that the biomechanics of the patellofemoral joint (PFJ), that is kinetic function, is affected in subjects with PFPS. It is also hypothesized that the values of this parameter will be different in PFPS subjects compared to subjects with asymptomatic knees. Alterations in patellofemoral joint reaction force (PFJRF) may therefore explain the cause of pain during a wide range of physical activities in subjects with PFPS. Treatment of PFPS is mostly based on physical therapy interventions (Crossley et al., 2002). Patellar taping is one of the treatment options, which is reported to reduce the pain immediately after its application in subjects with PFPS (McConnell, 1986; Bockrath et al., 1993; Powers et al., 1997; Ng and Cheng, 2002; Salsich et al., 2002). It is hypothesized that reducing pain following application of tape is related to altering PFJRF in PFPS subjects. Measuring PFJRF may therefore reveal whether the pain relief is associated with altering this parameter during functional activities. However, the reliability of PFJRF measurement during different activities and in different subject groups has not yet been reported. Accordingly, the aim of the present study is to examine the reliability of PFJRF in taped and untaped patellofemoral conditions during single leg squatting in healthy subjects. The future studies on the PFJRF values would be much more reliable in the symptomatic subjects if the results show that the reliability of PFJRF measurement is high enough during functional activities in healthy subjects.
Methods
extremities or the spinal column. They were also required to perform a single leg squat on repeated occasions.
Instrumentation Using a 2 camera (DCR-VX2000E, Sony, Japan) motion analysis system (SIMI Motion-2D&3D Motion Analysis, version 7.0, GmbH, Germany) and one forceplate (Kistler, 2812A-3, version 3.20, Switzerland), three dimensional movement and ground reaction force data of the subjects were recorded. Data were collected from superficial reflective markers taped to bony landmarks (Wallace et al., 2002). The five landmarks were the second metatarsal head, lateral malleolous, lateral aspect of the shank, lateral epicondyle of the femur and lateral aspect of the thigh, as illustrated in Figure 1.
Test procedure Before starting the main tests, all subjects were trained in how to perform single leg squats on their right legs, according to the required degrees of knee flexion, using verbal feedbacks (zero to approximately 45 degrees of knee flexion). To control any trunk forward flexion or deviation, they were asked to keep their feet in full contact with the floor during single leg squatting, while verbal feedback was used to encourage subjects to hold their trunks in a vertical position. After that, each subject was instructed to stand on their right leg on the forceplate and to keep the contralateral leg off the floor, as indicated in Figure 1. Each subject was then required to execute three shallow single leg squats, from 0 degree of the knee flexion to approximately 45 degrees of knee flexion. Subjects were subjected to three test conditions, namely, shallow single leg squatting before application of the tape (BT), with tape (WT) and a final test with no
Subjects The present study was approved by the East London and City Research Ethics Committee before recruiting subjects. Written informed consent was provided by each subject. The study was designed to examine the effects of taping on the patellofemoral joint of healthy subjects, and the reliability of outcome measurement (PFJRF) during single leg squatting. For this, eight healthy volunteers were recruited into the pilot study. These volunteers had no traumatic, inflammatory or infectious pathology in their lower extremities. Subjects with any history of surgery to their knees or dislocation or subluxation of their patellofemoral joints were also excluded from the study. Additionally, age greater than 40 years was one of the exclusion criteria to ensure subjects had no signs of secondary osteoarthritis (Crossley et al., 2002). The subjects, selected from students studying at Queen Mary University of London, had no previous history of disorders in either the lower
Figure 1 squatting
Setup used to measure kinetics during single leg
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tape (Shortly after tape Z SAT) on each testing occasion. This was conducted over three separate testing sessions. Each test session was performed with a minimum 6 h interval between them. Thus each subject executed 9 repetitions of single leg squatting at the end of the test procedure. Squatting was limited to about 3 s in duration, which was monitored by a stop watch. Patellar taping was employed to alter the alignment of the PFJ. Non-rigid, hypoallergenic tape (5 cm width, Sterofix hypoallergenic tape) was used to provide skin protection and rigid sterotape zinc-oxide tape (4 cm width, Steroplast Ltd Bredbury, England) was used for taping alteration. The taping technique involved employing a medial glide across the patella (Figure 2) according to the protocol described by McConnell (1986). As this technique is used in most subjects with PFPS to correct their lateral patellar glide (McConnell, 2002), the researcher used a similar technique in healthy subjects.
Data reduction Marker-coordinate and force data were processed by the SIMI motion analysis system. Using this system, the segmental kinematics for the foot, shank and thigh were computed. The inertial properties for the foot, shank and thigh were determined from the subject’s total body weight, segment geometry and anthropometric data (Winter, 1990). Sagittal-plane knee joint angles and net knee moments (Mk) were calculated from the inertial properties, segmental kinematics, and force platform data using inverse dynamics equations (Winter, 1990). The PFJRF was calculated using a biomechanical model of the PFJ (Salem and Powers, 2001). Based on the model, quadriceps muscle force (Fq) was calculated as the net knee moment (Mk) divided by the moment arm for the quadriceps (Lq). Fq ZMk =Lq The moment arm was estimated using the following nonlinear equation, based on the curve fitting to the data of van Eijden et al. (1987): Lq Z8:0e5 X 3 0:013X 2 þ 0:28X þ 0:046
where, X is the tibiofemoral joint angle. PFJRF was calculated as the product of the quadriceps force (Fq) and a constant (k) as follow: PFJRFZFq $k The constant k was estimated for knee joint angle (X ) using the following non-linear equation, based on the curve fitting to the data of van Eijden et al. (1986): 3:8e5 X 2 þ 1:5e3 X þ 0:462 kZ 7:0e7 X 3 þ 1:6e4 X 2 0:016X þ 1 For each test, kinetic data (Mk, PFJRF) were averaged through the 3 repetitions of single leg squatting. Data were analyzed in the eccentric phase of this activity at 30 degrees of knee flexion.
Data analysis All data were analyzed (SPSS-version 13) during the eccentric phase of squatting at 30 degrees of knee flexion. The ShapiroeWilk test was applied to all data sets (3 different sessions) of PFJRF measurements to test for normality. All data sets were found to be normally distributed and hence parametric statistics were used. Using the ANOVA test, the mean differences of PFJRF measurements during three different test sessions with 95% CI were calculated. From the mean and standard deviation of each data set, the coefficient of variation (CV) was used to describe the repeatability of the PFJRF measurements, for each subject and test. Random two-way intra class correlation coefficients for a single measure (ICC type 2, 1) were also used to examine whether the corresponding values of PFJRF during three different tape conditions (within session tests for three conditions of BT, WT and SAT) exhibited significant correlation. Additionally two statistics were calculated namely, 1. The within session least significant difference (LSD) values of PFJRF for the three different test sessions 2. The within session standard error of measurement (SEM) values of PFJRF for the three different test sessions
Results
Figure 2
Medial glide taping technique to alter the PFJ
Healthy volunteers (5 men and 3 women) with a mean age of 29.10 5.65 years were included in the study. A mean weight of 72.33 9.40 kg and a mean height of 168.20 8.25 cm were also obtained from these subjects. Summarized kinetic data of these subjects during eccentric phase of single leg squatting at 30 degrees of knee flexion are shown in Table 1. This data, relating to the right knees before, during and shortly after patellar taping, reveals few systematic trends for any of the parameters between the three tape conditions. ANOVA test revealed that, there were no significant differences between the PFJRF mean values for three conditions of BT, WT and SAT (p > 0.05).
Reliability testing of the patellofemoral joint reaction force
505
Table 1 Summarized data of three kinetic parameters measured on a group of 8 healthy subjects during the eccentric phase of single leg squatting at 30 degrees of knee flexion in 3 different conditions of before tape (BT), with tape (WT) and shortly after tape (SAT). Data represents mean SD.
BT WT SAT
Knee extensor moment (N m)
Quadriceps force (N)
PFJRF (N)
119.65 25.90 115.40 29.45 117.75 37.70
2645.20 560.25 2565.50 640.40 2615.35 705.65
2100.55 455.25 2026.20 516.45 2055.35 669.30
CV values The repeatability of the PFJRF measurements as determined from the values of CV is presented in Figure 3. It reveals that the minimum and maximum values for CV are 0.74% and 11.48%, respectively. For the majority of the cases (19 out of 24) the CV was less than 5%, indicating high repeatability of the PFJRF measurement during single leg squatting.
ICC values An analysis of the data using ICC, revealed relatively high intratester reliability for single measures of the PFJRF between three different repetitions (within session repetitions) of first (BT), second (WT) and third (SAT) test sessions. The minimum and maximum ICC values calculated for different repetitions in BT condition were 0.89 and 0.94, respectively. The values of 0.91 and 0.93 were also calculated as the minimum and maximum ICC values of WT condition. The minimum and maximum ICC values calculated for different repetitions in SAT condition were 0.90 and 0.95, respectively.
LSD values
Coefficient of variation of PFJRF (%)
Using the t value at a 5% significance level, the PFJRF LSD values of within session repetitions for the first test session (BT) were between 28.70 N and 64.95 N. The values of LSD for second test (WT) were also between 22.42 N and 57.62 N. Based on the results, the values of 20.82 Ne67.00 N were obtained from the third test (SAT) as reaction force LSD values. As there was no significant difference between each paired repetitions (p > 0.05) 15 10
BT WT SAT
5 0
S1 S2 S3 S4 S5 S6 S7 S8 Different tape conditions in healthy subjects
Figure 3 CV of the PFJRF during eccentric phase of single leg squatting (BT Z before taping, WT Z with tape and SAT Z shortly after taping) at 30 degrees of the knee flexion in eight healthy subjects (S)
these minimal differences reject the effect of random chance in obtaining similar results during within session repetitions, revealing accuracy of the results.
SEM values The SEM values of PFJRF during different test repetitions in different test conditions for 95% of probability were calculated. The SEM values of within session repetition for: first test session (BT) was between 233.0 N and 239.5 N second test session (WT) was between 263.0 N and 270.0 N third test session (SAT) was between 338.5 N and 341.0 N. These values indicated that the repeated measures (within session repetitions) fall between 2 SEM of initial measurement during these three different test conditions, demonstrating that the differences between repeated measures were not clinically relevant.
Discussion The CV values obtained from this study were low (majority of the values less than 5%) during within session tests in 3 different tape conditions, revealing high repeatability of PFJRF measurements (Figure 3). Indeed, these low scattered variabilities showed that the repeatability of PFJRF measurement is high during single leg squatting. The three tape conditions did not appear to influence the CV, revealing attachingereattaching of markers on the bony landmarks in different times, taping the patellofemoral joint or calibration of motions could not influence the results during different conditions. The ICC values of within session measurements of PFJRF during 3 conditions of BT, WT and SAT showed high reliability of the measurements. The high reliability of the PFJRF measurements during single leg squatting may reflect appropriate balance holding of the subjects during this activity. Clearly, the reliability tests using the ICC revealed that measuring the PFJRF during single leg squatting can be performed with high reliability in the future. The multiple comparison tests of PFJRF measurements in this study revealed that the measured differences of all paired mean values (within test sessions) were below the level of LSD values. This indicated that there was insufficient evidence to conclude testeretest values are different, revealing accuracy of each paired measurements. The relatively low values of within session SEM during this study, revealed that the random error of measurements were low, showing high precision of the PFJRF
506 measurements during 3 different conditions of BT, WT and SAT.
Conclusion The high reliability of PFJRF measurements using CV, ICC, LSD and SEM values reveals that future studies could rely on these measurements during single leg squatting.
Conflict of interest statement We confirm that authors have no conflict of interests regarding this paper.
Acknowledgement This article was provided as a part of the study leading to the degree of PhD, which was financially supported by Isfahan University of Medical Sciences and Ministry of Health and Medical Education of Islamic Republic of Iran.
References Bockrath, K., Wooden, C., Worrell, T., et al., 1993. Effects of patella taping on patella position and perceived pain. Medical Sciences and Sports Exercises 25, 989e992. Crossley, K., Green, S., Cowan, S., et al., 2002. Physical therapy for patellofemoral pain: a randomized, double blinded, placebo-
J. Mostamand et al. controlled trial. The American Journal of Sports Medicine 30 (6), 857e865. McConnell, J., 1986. The management of chondromalacia patellae: a long-term solution. Australian Journal of Physiotherapy 32 (4), 215e223. McConnell, J., 2002. The physical therapist’s approach to patellofemoral disorders. Clinics in Sports Medicine 21, 363e387. Ng, G.Y.F., Cheng, J.M.F., 2002. The effects of patellar taping on pain and neuromuscular performance in subjects with patellofemoral pain syndrome. Clinical Rehabilitation 16 (8), 821e827. Powers, C.M., Perry, J., Hsu, A., et al., 1997. Are patellofemoral pain and quadriceps femoris muscle torque associated with locomotor function? Physical Therapy 77 (10), 1063e1075. Salem, G.J., Powers, C.M., 2001. Patellofemoral joint kinetics during squatting in collegiate women athletes. Clinical Biomechanics 16, 424e430. Salsich, G.B., Brechter, J.H., Farwell, D., et al., 2002. The effects of patellar taping on knee kinetics, kinematics, and vastus lateralis muscle activity during stair ambulation in individuals with patellofemoral pain. The Journal of Orthopaedic and Sports Physical Therapy 32 (1), 3e10. van Eijden, T.M.G.J., Kouwenhoven, E., Verburg, J., et al., 1986. A mathematical model of the patellofemoral joint. Journal of Biomechanics 19 (3), 219e229. van Eijden, T.M.G.J., Weijs, W.A., Kouwenhoven, E., et al., 1987. Forces acting on the patella during maximal voluntary contraction of the quadriceps femoris muscle at different knee flexion/ extension angles. Acta Anatomica 129, 310e314. Wallace, D.A., Salem, G.J., Salinas, R., et al., 2002. Patellofemoral joint kinetics while squatting with and without an external load. Journal of Orthopedic Sports Physical Therapy 32 (4), 141e148. Winter, D.A., 1990. Biomechanics and Motor Control of Human Movement, second ed. A Wiley-Interscience Publication.
Journal of Bodywork & Movement Therapies (2011) 15, 507e516
available at www.sciencedirect.com
journal homepage: www.elsevier.com/jbmt
CLINICAL METHODS
A prophylactic effect of proprioceptive neuromuscular facilitation (PNF) stretching on symptoms of muscle damage induced by eccentric exercise of the wrist extensors Peanchai Khamwong, Ubon Pirunsan, Aatit Paungmali* Neuro-Musculoskeletal and Pain Research Unit, Department Physical Therapy, Faculty of Associated Medical Sciences, Chiang Mai University, Chiang Mai, Thailand 50200 Received 8 September 2009; received in revised form 23 June 2010; accepted 19 July 2010
KEYWORDS Delayed onset muscle soreness; Range of motion; Strength; Pain threshold; Stretching; Prevention
Summary Stretching with proprioceptive neuromuscular facilitation (PNF) is frequently used before exercise. The prophylactic effect of PNF on symptoms of muscle damage induced by eccentric exercise of the wrist extensors was examined in this study. Twenty-eight healthy males were randomly divided into the PNF group (n Z 14) and the control group (n Z 14). PNF was used before eccentric exercise induction in the wrist extensors. All subjects were tested to examine muscle damage characteristics including sensory-motor functions at baseline, immediately, and from 1st to 8th days after the exercise-induced muscle damage (EIMD). The results demonstrated that the PNF group showed a lesser deficit in some sensory-motor functions (p < 0.05) than the control group. The prior PNF stretching application could be useful for attenuating the signs and symptoms of muscle damage after eccentric exercise. ª 2010 Elsevier Ltd. All rights reserved.
Introduction Muscle damage occurring after unaccustomed activities or high-intensity exercise is a common physiological occurrences in daily life. Exercise-induced muscle damage (EIMD)
* Corresponding author. Tel.: þ66 53 949246; fax: þ66 53 946042. E-mail address:
[email protected] (A. Paungmali).
can cause several types of muscle pathologies such as muscle strain, cramp and soreness (Miles and Clarkson, 1994). Delayed-onset muscle soreness (DOMS) is a common neuromuscular condition that affects individuals the day after they perform vigorous or unaccustomed exercises. Eccentric muscle contraction has been reported to induce muscle damage (Miles and Clarkson, 1994; O’Connor and Hurley, 2003). The symptoms of DOMS usually decline within a week. However, when the symptoms of muscle damage happen in patients during
1360-8592/$ - see front matter ª 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jbmt.2010.07.006
508 a rehabilitation period, or in athletes, this may possibly interrupt the rehabilitation/training programs, along with sports performance, because of neuromuscular deficits. Many researchers have examined various ideas about intervention to reduce or prevent the severity of this kind of muscle damage. From a clinical perspective, preventative intervention is preferable and more important because it reduces the cost of treatment, time lost from training or rehabilitation, and the probability of persisting further injury. It also allows the continuation of exercise and competition (O’Connor and Hurley, 2003; Weerapong et al., 2004). Some useful methods to prevent musculoskeletal injuries include traditional interventions such as therapeutic exercise. In clinical practice, for example, we usually do stretching before the exercise as a preventative technique of muscle damage. It has been thought that the compliant muscle can be stretched further before it is damaged during eccentric exercise (Noonan et al., 1993; Safran et al., 1988) or that stretching could reduce muscle spasm after unaccustomed exercise (Herbert and de Noronha, 2007). Studies however have not shown the effectiveness of static stretching in the prevention of EIMD (High et al., 1989; Johansson et al., 1999). Rodenburg et al. (1994) reported that an intervention involving warm up, stretching and massage produced a significant reduction in muscle soreness. This study investigated the effects of a combination of interventions, so it could not provide an estimate of the specific effect of the stretching, in isolation from the other methods employed. However, Howatson and van Someren (2008) highlighted that other as yet uninvestigated stretching protocols, for example proprioceptive neuromuscular facilitation (PNF) may be of benefit, and therefore present a direction for further research. PNF stretching techniques are commonly used in the athletic and clinical settings to enhance both active and passive range of motions with a view to optimizing motor performance and rehabilitation. PNF stretching is one of the most effective stretching techniques which has been claimed to increase muscle flexibility (Sharman et al., 2006; Spernoga et al., 2001). There was also a report using a single set of PNF stretching which demonstrated a significant increase in flexibility (Spernoga et al., 2001). Improving tissue flexibility has also been mentioned as a means to reduce the risk of soft tissue injury and prevent muscle damage (O’Connor and Hurley, 2003; Weerapong et al., 2004). However, PNF technique has not yet been evaluated in patients with EIMD and it may prove that the use of PNF could have some potential benefit as a prophylactic effect. Much of the research on preventive damage and treatment of damaged muscles, has tended to use the group of big muscles as the model of muscle damage, for example, the biceps and the quadriceps (Nosaka et al., 2004; Sellwood et al., 2007). Other muscle groups, however, perform a range of different functions and respond to EIMD in different and diverse ways (Miles and Clarkson, 1994; Byrne et al., 2004; Jamurtas et al., 2005). The forearm muscle is an important muscle for daily activities and sports such as grasping, carrying, and sport activities which use a racquet such as tennis and squash. Limited research has been studied into the effects of PNF in the forearm extensor muscle. Therefore, the objective of this present
P. Khamwong et al. study was to understand the effect of PNF stretching on exercise-induced muscle damage in the wrist extensor muscle and determine its preventative effects.
Methods Participants Since gender and menstrual cycle influence the degree of EIMD (Dannecker et al., 2003), we conducted the study using only males. Based on a pilot study, the primarily clinical outcomes of EIMD (i.e., PPT, ROM-AE, pain-free GS and WES) were chosen to calculate the sample size. To obtain the power of 80% at the alpha level of 0.05 with the effect size of greater than 1.057, total sample size estimation would be approximately 14 subjects per group (Portney and Watkins, 2000). Demographic data of twentyeight healthy male volunteer students were presented as mean and SD (in brackets); age: 20.8 (1.3) years, height: 173.1 (4.7) cm, body weight: 61.9 (8.5) kg. They had no history of upper limb musculoskeletal disorders, neurological disorders, or any diseases that might affect the measurements prior to the study and had no experiences of arm resistance training at least 3 months before the study.
Outcome measures The non-dominant arm was used in this study to minimize possible effects of daily activities on the measures. The outcome measures consisted of pain intensity on a visual analogue scale (VAS) and modified Likert’s scale (LS), pain thresholds including thermal pain threshold [i.e., cold pain threshold (CPT)] and pressure pain threshold (PPT), range of motion in active wrist flexion (ROM-AF), active wrist extension (ROM-AE), passive wrist flexion (ROM-PF), and passive wrist extension (ROM-PE), grip strength (GS), wrist extension strength (WES) (Slater et al., 2003, 2005; Wright et al., 1994; Reese and Bandy, 2002). The order of measurements was pain intensity, CPT, PPT, ROM-AF, ROMAE, ROM-PF, and ROM-PE. Muscle strengths were measured after these measurements with a balanced randomization between GS and WES. Subjects were requested to participate in 11 experimental occasions to complete the study, and the travelling fee was reimbursed for all subjects. At the preliminary session all subjects who had agreed to take part, were familiarized with the purposes of the study and procedures. For baseline period, subjects were assessed for the dependent variables (all pain perceptions and motor functions) before the EIMD, and then evaluated for symptoms immediately and at follow up 8 days after the induction. The dependent variables were measured repeatedly at the same time of day. The CPT, PPT, ROM, and muscle strength were assessed three times to counteract variation between trials (Wright et al., 1994). To facilitate tissue recovery, 30 s interval between trials was allowed for measurements of CPT, PPT and ROM (Wright et al., 1994). For the measurement of muscle strength a 60 s rest interval was employed to avoid muscle fatigue (Slater et al., 2005). The mean value of the 3 trials was used for further analysis (Wright et al., 1994). The same
A prophylactic effect of proprioceptive neuromuscular facilitation stretching investigator conducted all measurements in a single-blinded manner. The room temperature was set at 25.0 C. All outcome measures including CPT, PPT, ROM (ROM-PF, ROMPE, ROM-AF, ROM-AE) grip and wrist extension strength, were considered to be reliable with a 24-h interval of testretest (ICC > 0.85) (Khamwong et al., 2010).
Study procedures Study design was a mixed model, 1 between (group) by 1 within (time) with a randomized-controlled experimental design. The subjects were divided into 2 groups (14 subjects per group). The control and experimental groups were arranged by chance using randomized drawing lots of 28 opaque sealed envelopes. The experimental group in this study obtained the application of PNF stretching before muscle damage induction, and the control group received muscle damage induction only. The study was approved by the institutional ethics committee and written consent was obtained from each subject.
PNF The PNF technique (hold-relax with agonist contraction) was performed for stretching. Each subject was asked to sit on an adjustable-height chair with supporting arm and then to move the hand beyond the edge of the supporting surface. The legs were set in a position of 90 hip-kneeankle, feet on the ground. The same chair and posture were applied for all subjects throughout the study. To standardize stretching method for the stretching group, the investigator passively stretched the wrist extensor muscles of the testing arm until each subject reported a mild stretch sensation and held that position for 10 s. Next, each subject was required to (isometrically contract the wrist extensor muscles to its maximum capacity) for 7 s by attempting to push his wrist back against the resistance of the investigator. After the contraction, each subject was allowed to relax for 5 s. Each subject was then asked to actively stretch the muscle, thus adding to the stretch force until a new point of mild stretch sensation was reached. The stretch was held for another 20 s (Figure 1). This sequence was repeated 10 times by each subject in the experimental group. This number of repetitions was chosen
509
as recommended by the literature and also to replicate the clinical use (Baechle and Earle, 2000; Spernoga et al., 2001).
Exercise induction The eccentric exercise protocol used the isokinetic mode of the Contrex dynamometer (CON-TREX Multijoint System, CMV AG manufacture, Switzerland). Subjects were placed in a seated position with support for the arm to be tested, to enable maximum resistance in the dynamometer’s movement from wrist extension to wrist flexion (Figure. 2). The exercise induction consisted of 5 sets of 60 maximal effort eccentric contractions of the wrist extensors at a velocity of 25 /s. A 1-min rest period between each set was allowed to counteract the effects of fatigue (Slater et al., 2005).
Pain intensity The visual analogue scale (VAS) was used to rate the intensity of pain. The VAS consisted of a 10 cm line anchored with “no pain” on the left end and “extreme pain” on the right end. Subjects were asked to rate their perceived level at pain at rest. A modified version of the Likert scale (LS) was also used to rate the level of muscle soreness as follow (Slater et al., 2003): 0 Z a complete absence of soreness; 1 Z a light soreness in the muscle felt only when touched/a vague ache; 2 Z a moderate soreness felt only when touched/a slight persistent ache; 3 Z a light muscle soreness when lifting objects or carrying objects; 4 Z a light muscle soreness, stiffness or weakness when moving the wrist without gripping an object; 5 Z a moderate muscle soreness, stiffness or weakness when moving the wrist; 6 Z a severe muscle soreness, stiffness or weakness that limits my ability to move. Thermal pain threshold (TPT) Cold pain threshold was assessed in the unit of degree Celsius ( C) using a Thermal Sensory Analyzer (Medoc Ltd., Neuro Sensory Analyzer Model TSA-II, Ramat Yishai, Israel). The measurement site was the belly of the extensor group muscles located at the prominent site over the carpi radialis brevis muscle. Subjects lay down on their backs with
Figure 1 The PNF stretching technique (hold-relax with agonist contraction) was performed by the investigator passively stretched the wrist extensor muscles until the subject reported a mild stretch sensation and held that position for 10 s. Next, the subject was asked to contract the wrist extensor muscles isometrically against the resistance of the investigator for 7 s. Then, the subject was asked to actively stretch the muscle until a new point of mild stretch sensation was reached.
510
P. Khamwong et al.
Figure 2 An eccentric exercise induction was performed using isokinetic mode of the Contrex dynamometer (CON-TREX Multijoint System, CMV AG manufacture, Zurich, Switzerland). The exercise induction consisted of 5 sets of 60 maximal effort eccentric contractions of the wrist extensors at a velocity of 25 /s.
arms by the side (0 elbow extension and 90 pronation). The thermode (5 cm2) was applied on the marked areas with Velcro strap for holding it in place. Using the standard protocol for evaluating TPT in wrist extensors, previously referred to, the initial temperature for testing cold pain threshold (CPT) was set up at 32 C. The thermode temperature was gradually decreased, by approximately 2 C/s each time to a minimum cut-off temperature of 0 C (Wright et al., 1994). Subjects held a control switch, and were instructed to press the button when they felt the sensation changing from cold to pain. Subjects received a verbal instruction approximately 1e2 s before the initiation of each test. Pressure pain threshold Pressure pain threshold (PPT) was measured in the unit of kilopascal (kPa) using a pressure algometer (Somedic Production, Algometer type II, Ho ¨rby, Sweden) with a probe of 1.0 cm2. PPT was assessed at the same muscle site as the measure of CPT. Subjects lay down on their backs with their arms by their side (0 elbow extension and 90 pronation). The probe was pressed at the reference site, and the pressure was increased at a rate of 30 kPa/s until subjects felt the sensation changing from the pressure to pain, which was indicated by the subjects pressing a button (Slater et al., 2005). Range of motion (ROM) ROM was evaluated in the unit of degree using a universal goniometer (SFTR International Standard Goniometer, Sammons Preston Healthcare, Bollingbrook, Illinois, USA) for wrist extension and flexion to determine the pain-free active and passive range of motions. Subjects sat on an arm supporting chair, and were asked to rest their arms on the support. The center of the goniometer was placed at the center of the axis of the wrist joint (triquetrum bone), and the angle parallel to the lateral midline of the ulna and the lateral midline of 5th metacarpal bone (Reese and Bandy,
2002). The pain-free active range of motion was performed by instructing the subject to move the wrist into flexion and extension directions, the subject was requested to stop the movement when first perceiving pain. For the pain-free passive range of motion, the subject was asked to relax the hand during passive movement of the wrist joint into flexion and extension directions by the investigator. The subject signaled the investigator for a position of the wrist when initial perceiving pain. Grip strength Grip strength (GS) was measured in Newtons (N) using an electronic digital hand dynamometer (Model MLT003/D, Power lab, Castle Hill, NSW, Australia). Subjects sat on a chair with their arms supported by a platform, which was set at the same length as from the elbow to the wrist joint. The upper extremity was positioned according to the recommendations of the American Hand Society of Hand Therapist (Fess, 1992) such that the shoulder was adducted and neutrally rotated, forearm in neutral position, and wrist slightly extended (20 ). GS was measured with the elbow in 90 flexion and within the comfortable grip width of each subject. The subjects were requested to grip as strongly as they could without pain (i.e., pain-free GS) and they were also instructed to perform a sustained maximal isometric contraction for 6 s (i.e., maximal GS) (Kamimura and Ikuta, 2001). Wrist extension strength Wrist extension strength (WES) was recorded via a force transducer (Model MLT003/D, Power lab, Castle Hill, NSW, Australia) in Newtons (N). A specifically designed pad hand attachment was connected to the underside of the force transducer. The transducer was mounted on a platform, which was located under the table. Each subject sat on a chair with his forearm in full pronation with 45 elbow flexion supported on an armrest of the chair, and his wrist was set in 20 extension with the 3rd knuckle placed to the
A prophylactic effect of proprioceptive neuromuscular facilitation stretching center of the force transducer. The subjects were requested to extend the wrist by pushing the dorsal surface of the hand on to the padded surface of the hand attachment as strong as they could without pain (i.e., pain-free WES) and they were also instructed to maximally extend the wrist against the dynamometer and sustained a maximal isometric contraction for 6 s (i.e., maximal WES) (Kamimura and Ikuta, 2001).
Statistical analyses Results of peak torque, total work and all outcome measures were expressed as mean and SD. Both absolute and “normalized” data were used for analysis of selected criterion measures. In case of pain intensity, VAS and LS were analyzed with absolute values. For CPT, PPT, and ROM, the “normalized” values refer to changes from preexercise values. In terms of muscle strength (GS and WES), the “normalized” values refer to percentages of pre-exercise values (i.e., normalized to pre-exercise). Outcome measurements, such as GS, WES, ROM, VAS, LS, CPT, PPT, were compared with the baseline values. The results were analyzed by the Statistical Package for the Social Sciences (SPSS) using repeated-measures ANOVA, followed by paired t-test pairwise comparisons with pre-specified contrasts to maintain experiment error rate below 5%. To test for the differences between groups at each time period, an ANOVA for independent observations was used. Statistical significance was set at 0.05 for all analyses.
Results Subject characteristics The subjects were arranged by chance into the control and the experimental groups using randomized drawing of lots. Mean differences between groups of the subjects’ characteristics (i.e., age, height, weight) were less than 3%, considering no differences in statistical and clinical aspects (Table 1). No significant differences in the baseline values between groups were observed for any of the dependent variables except for PPT (Table 1). Normalized data were used to adjust a variation among individual subjects.
Peak torque and total work during eccentric exercise All subjects were able to complete each set of the exercise induction protocol. No significant differences in mean
511
maximal torque and total work during the eccentric exercise were evident between the control and PNF groups (Table 1).
Pain intensity Pain intensity was assessed by visual analogue scale and muscle soreness using Likert’s scale. In the control group, pain intensity of VAS was significantly increased when comparing the pain level at pre-exercise to immediately post-exercise, and days 1e6, post-exercise (p < 0.044). In the PNF group, the VAS was significantly increased when comparing the pain level at pre-exercise to immediately post-exercise and days 1e4 post-exercise (p < 0.008). LS was significantly increased as the similar manner of VAS at immediately post-exercise and days 1e6 post-exercise in the control group (p < 0.026) and immediately post-exercise and days 1e5 post-exercise in the PNF group (p < 0.022). The difference in pain intensity between control and PNF were not statistically significant (Table 2).
Pain threshold Thermal pain threshold Cold pain threshold at muscle site was significantly increased when comparing the pain threshold at preexercise to days 1e3 post-exercise (p < 0.047) in the control group. CPT was not significantly different from the baseline in the PNF group. There was also a significantly lower deficit in CPT within the PNF group in comparison to the control group on days 1e5 post-exercise (p < 0.043) (Table 2). Mechanical pain threshold Pressure pain threshold at muscle site was significantly decreased from the baseline during an immediately postexercise and days 1e4 post-exercise (p < 0.048) in the PNF group; however, the PPT of the control group decreased significantly from an immediate post-exercise and did not return to the pre-exercise level by day 5 post-exercise (p < 0.011). The PNF group was significantly higher in PPT than the control group on day 8 post-exercise (p Z 0.016) (Table 2). Range of motion Range of motion was assessed in passive and active of flexion and extension. Passive range of wrist flexion was significantly decreased when comparing the range at preexercise to immediately post-exercise and days 1e8 postexercise in the control group (p < 0.013) and in the PNF
Table 1 Mean and standard deviation (in brackets) of subject’s characteristics (age, height, and weight) and work load during eccentric exercise induction. Characteristics
Control group (n Z 14)
PNF group (n Z 14)
Age (years) Height (cm) Weight (kg) Peak torque (N) Total work (J)
21.1 173.1 61.3 3.3 180.0
20.5 173.0 62.4 4.0 177.2
(1.6) (5.1) (9.6) (0.9) (56.6)
No clinically important differences between groups were evident for all data.
(0.9) (4.5) (7.6) (1.4) (60.0)
Changes in outcome measures before (pre), immediate (Imm) and 1e8 days following eccentric exercise of the PNF (n Z 14) and control (CON; n Z 14) groups. Pre
Imm
Day 1
Day 2
Day 3
Day 4
Day 5
Day 6
Day 7
Day 8
VAS (cm) CON 0 (0) PNF 0 (0)
2.5 (2.1)a 1.8 (2.0)a
4.8 (1.9)a 4.4 (2.5)a
5.0 (1.7)a 3.7 (2.4)a
3.2 (1.7)a 2.8 (2.4)a
2.0 (1.5)a 1.7 (2.0)a
0.8 (0.8)a 0.7 (1.2)
0.2 (0.4)a 0.2 (0.5)
0.0 (0.9) 0.0 (0.1)
0.0 (0.1) 0 (0)
LS (level) CON 0 (0) PNF 0 (0)
2.7 (2.1)a 1.3 (1.9)a
4.1 (1.5)a 4.9 (0.7)a
4.4 (1.6)a 4.6 (1.3)a
3.6 (1.8)a 3.6 (1.6)a
2.8 (1.8)a 2.1 (1.9)a
1.9 (1.7)a 1.6 (1.8)a
0.9 (1.4)a 0.4 (1.1)
0.1 (0.4) 0.3 (1.1)
0 (0) 0 (0)
CPT (oC) CON 0 (0) PNF 0 (0)
2.7 (4.8) 0.7 (3.8)
3.9 (6.6)a 0.7 (3.4)b
5.9 (7.8)a 0.3 (3.6)b
3.1 (5.3)a 0.7 (4.0)b
3.3 (6.1) 1.0 (3.3)b
2.6 (5.7) 1.5 (3.3)b
0.4 (4.7) 0.8 (2.8)
0.5 (5.6) 1.6 (3.2)
1.4 (6.7) 1.5 (2.5)
PPT (kPa) CON 0 (0) PNF 0 (0)
30.8 (39.2)a 50.6 (56.1)a
128.0 (95.8)a 126.5 (54.2)a
125.9 (96.5)a 123.1 (86.0)a
97.4 (84.0)a 88.3 (89.6)a
61.9 (60.7)a 43.6 (74.9)a
46.4 (55.6)a 16.5 (79.4)
15.6 (52.2) 10.8 (60.3)
8.2 (42.3) 33.1 (79.8)
2.2 (32.1) 44.6 (52.4)b
ROM-PF (degree) CON 0 (0) PNF 0 (0)
9.1 (10.5)a 8.9 (7.6)a
29.6 (12.2)a 18.4 (13.3)a,b
34.2 (14.5)a 21.7 (17.8)a
28.2 (15.6)a 19.3 (16.8)a
23.2 (14.5)a 15.7 (15.8)a
15.2 (9.5)a 9.4 (12.8)a
11.3 (9.2)a 9.1 (10.4)a
7.2 (6.3)a 5.9 (8.7)a
4.7 (6.1)a 6.0 (10.4)a
ROM-PE (degree) CON 0 (0) PNF 0 (0)
8.6 (7.7)a 3.0 (5.7)b
18.3 (9.8)a 7.2 (9.0)b
20.6 (16.4)a 4.4 (6.8)b
14.1 (13.3)a 1.4 (5.2)b
10.1 (11.8)a 1.5 (6.1)b
6.8 (9.7)a 2.4 (5.5)b
4.6 (8.1) 3.8 (6.9)b
2.6 (6.6) 2.9 (7.6)b
2.0 (7.3) 4.6 (5.6)b
ROM-AF (degree) CON 0 (0) PNF 0 (0)
9.9 (8.6)a 6.9 (4.9)a
17.1 (10.0)a 11.5 (10.3)a
21.1 (12.1)a 16.0 (13.0)a
15.9 (11.3)a 15.8 (16.9)a
13.6 (13.0)a 11.2 (13.5)a
6.1 (6.1)a 7.0 (9.5)a
2.8 (6.7) 5.6 (6.4)a
0.2 (8.1) 4.9 (6.1)a
2.1 (9.1) 4.0 (7.2)
20.5 (9.9)a 10.1 (8.8)a,b
19.5 (13.3)a 5.4 (6.3)a,b
12.6 (7.0)a 3.7 (7.5)b
8.5 (5.6)a 2.9 (8.5)b
4.3 (3.9)a 0.1 (5.4)b
4.3 (4.8)a 0.0 (5.0)b
2.5 (4.0)a 0.7 (5.2)
1.6 (3.7) 1.4 (4.3)
95.0 (15.5) 100.7 (12.0)
100.6 (16.5) 98.1 (12.5)
102.0 (14.8) 98.8 (14.6)
102.5 (17.5) 101.4 (16.8)
105.1 (16.3) 104.7 (17.8)
105.1 (14.2) 107.9 (17.4)
93.5 (18.3) 99.7 (16.7)
94.7 (18.3) 102.7 (15.7)
ROM-AE (degree) CON 0 (0) 25.8 (10.4)a PNF 0 (0) 17.2 (14.3)a GS [max] (N) CON 100 (0) PNF 100 (0)
74.4 (16.6)a 70.8 (13.8)a
90.6 (15.3)a 89.4 (11.1)a
94.9 (12.7) 95.9 (11.6)
GS [pain-free] (N) CON 100 (0) PNF 100 (0)
51.1 (19.5)a 52.2 (15.5)a
52.0 (24.5)a 66.7 (18.3)a
51.5 (24.4)a 76.5 (12.9)a,b
68.6 (27.1)a 85.3 (18.0)a
77.9 (17.5)a 89.1 (15.3)a
86.9 (16.8)a 93.3 (15.7)
88.6 (16.7)a 94.7 (14.4)
512
Table 2
P. Khamwong et al.
94.5 (23.7) 99.7 (18.7) 88.0 (21.7) 89.2 (17.5) 79.2 (19.8)a 92.1 (20.1) 75.4 (19.9)a 91.2 (18.2)a 70.8 (22.8)a 74.0 (22.4)a Data are presented as mean (SD). For GS and WES, the pre-exercise level was expressed as 100%. a Significantly different from the baseline (pre). b Significantly different from CON.
41.6 (23.8)a 71.1 (21.8)a,b 34.6 (13.5)a 57.2 (20.8)a,b WES [pain-free] (N) CON 100 (0) 38.2 (14.9)a PNF 100 (0) 44.6 (12.3)a
513
group (p < 0.049). ROM-PF did not return to the baseline values within 8 days post-exercise in both groups. The PNF group, however, demonstrated a significantly lesser deficit in ROM-PF values than in the control group on day 1 postexercise (p Z 0.028) (Table 2). Passive range of wrist extension was significantly decreased from the baseline at 1 and 2 days post-exercise (p < 0.032) in the PNF group; however, the ROM-PE of the control group decreased significantly from an immediate post-exercise and did not return to the pre-exercise level by day 5 post-exercise (p < 0.021). The PNF group significantly demonstrated a lesser deficit in ROM-PE than the control group at immediately post-exercise and on days 1e8 post-exercise (p < 0.049) (Table 2). There was no significant difference in ROM-AF between control and PNF groups. Active range of wrist extension was significantly decreased from the baseline during an immediately post-exercise and days 1e2 post-exercise (p < 0.007) in the PNF group; however, the ROM-AE of the control group decreased significantly from an immediate post-exercise and did not return to the pre-exercise level by day 7 post-exercise (p < 0.035). The PNF group significantly demonstrated a lesser deficit in ROM-AE than that of the control group on days 1e6 post-exercise (p < 0.048) (Table 2).
56.4 (27.7)a 74.6 (19.9)a
96.7 (19.7) 96.3 (18.1) 82.2 (34.9)a 87.1 (18.9)a WES [max] (N) CON 100 (0) PNF 100 (0)
63.6 (11.5)a 61.1 (14.0)a
67.3 (18.4)a 77.6 (13.3)a
86.7 (21.2)a 89.8 (21.7)
94.1 (16.0) 90.6 (18.7)
107.2 (27.0) 97.3 (20.4)
106.0 (28.1) 98.2 (20.9)
110.2 (28.4) 106.1 (24.5)
A prophylactic effect of proprioceptive neuromuscular facilitation stretching
Muscle strength Pain-free grip strength declined significantly from the baseline during an immediately post-exercise and days 1e4 post-exercise (p < 0.019) in the PNF group; however, the GS [pain-free] of the control group decreased significantly from an immediate post-exercise and did not return to the pre-exercise level by day 6 post-exercise (p < 0.023). The PNF group significantly demonstrated a lesser deficit in GS [pain-free] than the control group on day 2 post-exercise (p Z 0.002). There was no significant difference in GS [max] between control and PNF groups (Table 2). Pain-free wrist extensor strength declined significantly from the baseline during an immediately post-exercise and days 1e4 post-exercise (p < 0.001) in the PNF group; however, the WES [pain-free] of the control group decreased significantly from an immediate post-exercise and did not return to the pre-exercise level by day 6 postexercise (p < 0.002). The PNF group significantly demonstrated a lesser deficit in WES [pain-free] than that of the control group on days 1e2 and day 5 post-exercise (p < 0.037). There was no significant difference in WES [max] between control and PNF groups (Table 2).
Discussion The main findings of this study were the beneficial effects of PNF intervention on EIMD symptoms as set out in the following categories of sensory perception and muscle function.
Sensory perception The PNF group significantly demonstrated a lesser deficit in cold pain and pressure pain threshold than in the control group. We have demonstrated that using the PNF (hold-relax
514 with agonist contract) technique can help to minimize pain perception and reduce the effect of cold and pressure stimuli on CPT and PPT at the muscle site. It has been reported that a single bout of resistance exercise is capable of modifying the sensation of experimentally induced analgesia (Koltyn and Arbogast, 1998; Koltyn et al., 2001). Hoeger Bement et al. (2009) also reported that an isometric fatiguing contraction significantly alters the corticomotor pathway during application of a noxious stimulus. These insights help to explain why PNF intervention has some effect on the thermal and mechanoreceptor adaptation to these stimuli, as shown in the results from the PNF group when compared to the control group. Passive flexion range of the wrist demonstrated a lesser deficit in the PNF group. Passive extension range of the wrist in the PNF group also demonstrated fewer deficits. Muscle soreness is more painful and sensitive with stretching (Byrne et al., 2004). Passive range of motion can cause more pain especially in the opposite movement (i.e., flexion direction) of the damaged wrist extensor muscle and more compression of the muscle belly when moved in the same direction (i.e., extension direction) of the damaged muscle. The two directions of experiment lead to muscle guarding during the movement (Jones et al., 1987). This present study showed a greater reduction of ROM-PF and ROM-PE in the PNF group.
Motor function There was no significant difference in the active flexion range of the wrist between the control and the PNF groups. During the contraction of active flexion, reciprocal inhibition mechanism may take part to reduce tone of the wrist extensors when assessing the flexion range of motion (Guyton and Hall, 2006). This may be one reason why the measurement of active wrist flexion in this study has not shown any difference in ROM-AF between groups. Active extension range of the wrist in the PNF group demonstrated a lesser deficit than in the control group. Active movement (contraction) of a sore muscle can affect the excitation contraction coupling and cause pain during motion (Byrne et al., 2004). The PNF group demonstrated better passive and active wrist extension movements than in the control group. In general, EIMD can cause a reduction in the ROM due to pain or stiffness after exercise. Application of PNF has beneficial effects on active extension in this ROM measure. It seemed that pain-free muscle strength is more sensitive for detection of muscle damage than the maximal muscle strength test. The pain-free grip strength and wrist extensor strength in the PNF group have fewer deficits than the control group. Muscle strength is one of the best muscle damage indicators, which is normally reduced after exercise with slow recovery (Nosaka and Newton, 2002). The prevention of EIMD by using PNF has shown the beneficial effect on muscle strength of grip and wrist extension in this present study, as shown in a lower deficit of pain-free grip and wrist extensor strength. The result of our study was dissimilar to previous studies. High et al. (1989), Johansson et al. (1999) did not demonstrate the efficacy of stretching on muscle soreness in quadriceps and hamstrings, respectively. They applied
P. Khamwong et al. static stretching before the induction exercises in healthy student volunteers, and their results showed no effect of static stretching on EIMD. In this present study, a different stretching technique (PNF-hold-relax with agonist contraction) was performed. This technique is a combination of both static and dynamic stretching maneuvers. As a result, some advantageous effects of the PNF were evidenced on EIMD symptoms in terms of sensory perception and muscle function. The application of PNF before exercise was aimed at preparing the localized muscle to prevent EIMD symptoms. PNF technique of hold-relax with agonist contraction was used to prepare the wrist extensors with passive and active movement that can improve muscle flexibility via autogenic inhibition and reciprocal inhibition. The benefits of an active warm up may be to minimize muscle stiffness by moving the required muscle groups through their range of motion. As a result, the warm up with PNF stretching may release actin-myosin bonds and thereby reduce the passive stiffness of muscle. This may contribute to an increased rate of force development and an increase in the efficacy of muscle working during eccentric exercise (Bishop, 2003). Stretching exercises also affect the mechanical properties of the muscle-tendon unit (MTU), i.e., reduce the tension on the muscle-tendon unit that affects the visco-elastic component of tissue leading to an increase in the compliance of muscle and a reduction in muscle stiffness; consequently, less tension will be produced in the muscle during a specified stretch. The resulting improvement of muscular flexibility possibly reduces muscle and connective tissue damage after exercise (Weldon and Hill, 2003; Magnusson and Renstrom, 2006). Apart from the visco-elastic mechanism of PNF stretching, a neurophysiological mechanism may take part for the effects through neural inhibition of the muscle group being stretched via an inhibitory interneuron. As a result of reducing the activity in the alpha-motor neuron to the antagonist muscle, which then promotes greater relaxation and decreases resistance to stretch (Guyton and Hall, 2006). It is also possible that the descending pain inhibitory systems (e.g., mid brain) may be activated during PNF stimulation (Carrive, 1993). Further neurological studies, such as functional magnetic resonance imaging (fMRI), are warranted to investigate this notion. There remains a question regarding the clinical importance of the findings (i.e., CPT, PPT, ROM-PF, ROM-PE, ROMAE, GS and WES [pain-free]). As there is no information regarding this issue, we determined the clinical meaningfulness by estimating the minimally clinical important difference (MCID) using a distribution-based approach as recommended by Wells et al. (2001). The findings demonstrated that all of these observed changes were beyond the standard error of measurements (Khamwong et al., 2010), and the observed values were greater than 37% (i.e., changes in thermal pain, pressure pain, range of motion, and strength were 6.2 C, 42.4 kPa, 11.4 , 29.5 N, respectively). Therefore, we considered that these amounts of change were clinically meaningful for rehabilitation and sport performance. A limitation should be noted that the placebo condition was not included in the study. Studies in the future should consider the placebo-controlled study design for strengthening the internal validity of the study.
A prophylactic effect of proprioceptive neuromuscular facilitation stretching
Conclusion This study showed that PNF stretching prior to exercise can reduce the symptoms of muscle damage, especially pain threshold, ROM, and muscle strength. The PNF demonstrated a lesser deficit in both thermal and mechanical pain thresholds, pain-free muscle strength, passive ROM and active extension ROM than the control group. Results of this study suggests that applying PNF stretching prior to exercise help to attenuate symptoms of EIMD in the wrist extensors.
Acknowledgements The authors would like to express our gratitude to the participants and the Thai Health Promotion Foundation for funding this study.
Declaration of interest The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.
References Baechle, T.R., Earle, R.W., 2000. Essentials of Strength Training and Conditioning, second ed. Human Kinetics, Hong Kong. Bishop, D., 2003. Warm up I: potential mechanisms and the effects of passive warm up on exercise performance. Sports Med. 33 (6), 439e454. Byrne, C., Twist, C., Eston, R., 2004. Neuromuscular function after exercise-induced muscle damage: theoretical and applied implications. Sports Med. 34 (1), 49e69. Carrive, P., 1993. The periaqueductal gray and defensive behavior: functional representation and neuronal organization. Behav. Brain Res. 58 (1e2), 27e47. Dannecker, E.A., Koltyn, K.F., Riley, J.L., Robinson, M.E., 2003. Sex differences in delayed onset muscle soreness. J. Sports Med. Phys. Fitness 43 (1), 78e84. Fess, E.E., 1992. Grip strength. In: Casanova, J.S. (Ed.), Clinical Assessment Recommendations. American Society of Hand Therapists, Chicago, pp. 41e45. Guyton, A.C., Hall, J.E., 2006. Textbook of Medical Physiology, eleventh ed. Elsevier Saunders, Philadelphia, PA. Herbert, R.D., de Noronha, M., 2007. Stretching to prevent or reduce muscle soreness after exercise. Cochrane Database Syst. Rev. (4), CD004577. High, D.M., Howley, E.T., Franks, B.D., 1989. The effects of static stretching and warm-up on prevention of delayed-onset muscle soreness. Res. Q. Exerc. Sport 60 (4), 357e361. Hoeger Bement, M.K., Weyer, A., Hartley, S., Yoon, T., Hunter, S.K., 2009. Fatiguing exercise attenuates pain-induced corticomotor excitability. Neurosci. Lett. 452 (2), 209e213. Howatson, G., van Someren, K.A., 2008. The prevention and treatment of exercise-induced muscle damage. Sports Med. 38 (6), 483e503. Jamurtas, A.Z., Theocharis, V., Tofas, T., Tsiokanos, A., Yfanti, C., Paschalis, V., et al., 2005. Comparison between leg and arm eccentric exercises of the same relative intensity on indices of muscle damage. Eur. J. Appl. Physiol. 95 (2e3), 179e185. Johansson, P.H., Lindstrom, L., Sundelin, G., Lindstrom, B., 1999. The effects of preexercise stretching on muscular soreness,
515
tenderness and force loss following heavy eccentric exercise. Scand. J. Med. Sci. Sports 9 (4), 219e225. Jones, D.A., Newham, D.J., Clarkson, P.M., 1987. Skeletal muscle stiffness and pain following eccentric exercise of the elbow flexors. Pain 30 (2), 233e242. Kamimura, T., Ikuta, Y., 2001. Evaluation of grip strength with a sustained maximal isometric contraction for 6 and 10 seconds. J. Rehabil. Med. 33 (5), 225e229. Khamwong, P., Nosaka, K., Pirunsan, U., Paungmali, A., 2010. Reliability of muscle function and sensory perception measurements of the wrist extensors. Physiother. Theory Pract. 26 (4), 1e8. Koltyn, K.F., Arbogast, R.W., 1998. Perception of pain after resistance exercise. Br. J. Sports Med. 32 (1), 20e24. Koltyn, K.F., Trine, M.R., Stegner, A.J., Tobar, D.A., 2001. Effect of isometric exercise on pain perception and blood pressure in men and women. Med. Sci. Sports Exerc. 33 (2), 282e290. Magnusson, P., Renstrom, P., 2006. The European college of sports sciences position statement: the role of stretching exercises in sports. Eur. J. Sport Sc 6 (2), 87e91. Miles, M.P., Clarkson, P.M., 1994. Exercise-induced muscle pain, soreness, and cramps. J. Sports Med. Phys. Fitness 34 (3), 203e216. Noonan, T.J., Best, T.M., Seaber, A.V., Garrett Jr., W.E., 1993. Thermal effects on skeletal muscle tensile behavior. Am. J. Sports Med. 21 (4), 517e522. Nosaka, K., Newton, M., 2002. Difference in the magnitude of muscle damage between maximal and submaximal eccentric loading. J. Strength Cond. Res. 16 (2), 202e208. Nosaka, K., Sakamoto, K., Newton, M., Sacco, P., 2004. Influence of pre-exercise muscle temperature on responses to eccentric exercise. J. Athl. Train. 39 (2), 132e137. O’Connor, R., Hurley, D.A., 2003. The effectiveness of physiotherapeutic interventions in the management of delayed onset muscle soreness: a systematic review. Phys. Ther. Rev. 8 (4), 177e195. Portney, L.G., Watkins, M.P., 2000. Foundations of Clinical Research Applications to Practice, second ed. Prentice Hall Health, New Jersey. Reese, N.B., Bandy, W.D., 2002. Joint Range of Motion and Muscle Length Testing. W.B. Saunders, Philadelphia. Rodenburg, J.B., Steenbeek, D., Schiereck, P., Bar, P.R., 1994. Warm-up, stretching and massage diminish harmful effects of eccentric exercise. Int. J. Sports Med. 15 (7), 414e419. Safran, M.R., Garrett Jr., W.E., Seaber, A.V., Glisson, R.R., Ribbeck, B.M., 1988. The role of warmup in muscular injury prevention. Am. J. Sports Med. 16 (2), 123e129. Sellwood, K.L., Brukner, P., Williams, D., Nicol, A., Hinman, R., 2007. Ice-water immersion and delayed-onset muscle soreness: a randomised controlled trial. Br. J. Sports Med. 41 (6), 392e397. Sharman, M.J., Cresswell, A.G., Riek, S., 2006. Proprioceptive neuromuscular facilitation stretching: mechanisms and clinical implications. Sports Med. 36 (11), 929e939. Slater, H., Arendt-Nielsen, L., Wright, A., Graven-Nielsen, T., 2005. Sensory and motor effects of experimental muscle pain in patients with lateral epicondylalgia and controls with delayed onset muscle soreness. Pain 114 (1e2), 118e130. Slater, H., Arendt-Nielsen, L., Wright, A., Graven-Nielsen, T., 2003. Experimental deep tissue pain in wrist extensorsea model of lateral epicondylalgia. Eur. J. Pain 7 (3), 277e288. Spernoga, S.G., Uhl, T.L., Arnold, B.L., Gansneder, B.M., 2001. Duration of maintained hamstring flexibility after a one-time modified hold-relax stretching protocol. J. Athl. Train. 36 (1), 44e48. Weerapong, P., Hume, P.A., Kolt, G.S., 2004. Preventative strategies for exercise-induced muscle damage. Crit. Rev. Phys. Rehabil. 16 (2), 133e149.
516 Weldon, S.M., Hill, R.H., 2003. The efficacy of stretching for prevention of exercise-related injury: a systematic review of the literature. Man. Ther. 8 (3), 141e150. Wells, G., Anderson, J., Beaton, D., Bellamy, N., Boers, M., Bombardier, C., et al., 2001. Minimal clinically important
P. Khamwong et al. difference module: summary, recommendations, and research agenda. J. Rheumatol. 28 (2), 452e454. Wright, A., Thurnwald, P., O’Callaghan, J., Smith, J., Vicenzino, B., 1994. Hyperalgesia in tennis elbow patients. J. Musculoskelet. Pain 2 (4), 83e97.
Journal of Bodywork & Movement Therapies (2011) 15, 517e524
available at www.sciencedirect.com
journal homepage: www.elsevier.com/jbmt
EXERCISE PHYSIOLOGY RESEARCH
Influence of dynamic versus static core exercises on performance in field based fitness tests Kelly L. Parkhouse, BSc, ASCC a, Nick Ball, PhD, ASCC, CSCS b,* a b
Department of Sport and Exercise Science, University of Portsmouth, UK National Institute of Sports Studies, Faculty of Health, University of Canberra, ACT 2601, Australia
Received 5 July 2010; received in revised form 16 November 2010; accepted 30 November 2010
KEYWORDS Lumbopelvic; Stability ball; Performance
Summary Minimal evidence supports the claim that core stability training transfers into improved performance and the most effective training method to perform core exercises is still unknown. The purpose of the study was to compare the effects of a 6 week unstable static versus unstable dynamic core training program, on field based fitness tests. A static (n Z 6) and dynamic (n Z 6) training group performed two 45 min sessions per week for six weeks. Seven performance tests, consisting of three core (plank; double leg lowering; back extensions), one static (standing stork) and three dynamic (overhead medicine ball throw; vertical jump; 20 m sprint), were administered pre- and post training. Between group differences were assessed using a repeated measures MANOVA (P < 0.05). Both training groups improved in each of the core tests (P < 0.05). Neither training group demonstrated improvement in the dynamic field based tests (medicine ball throw, vertical jump height and 20 m sprint) (P > 0.05). Findings indicate that both types of training improved specific measures of core stability but did not transfer into any sport-related skill. Crown Copyright ª 2010 Published by Elsevier Ltd. All rights reserved.
Introduction Core stability training on unstable surfaces is commonplace in both healthcare and conditioning settings. Proponents of unstable training argue that such training enhances neuromuscular pathways (Beache and Earle, 2000; Hedrick, 2000), leading to greater strength (Behm et al., 2005; Gamble, 2007; * Corresponding author. Tel.: þ61 (0) 2 6201 2419; fax: þ61 (0) 2 6201 5615. E-mail address:
[email protected] (N. Ball).
Rutherford and Jones, 1986; Vera-Garcia et al., 2000), power (Jeffreys, 2002) and balance (Anderson and Behm, 2005; Goodman, 2003; Lehman et al., 2005). Generally, findings have indicated that as the degree of instability increases, the degree of core muscle activity increases proportionally (Anderson and Behm, 2005; Behm et al., 2005; Marshall and Murphy, 2005; Murphy and Wilson, 1996; Vera-Garcia et al., 2000). For this reason, resistance exercises performed on unstable surfaces have been emphasized as most effective for the development of core stability (Boyle, 2004; Chek, 1999). Kibler et al. (2006) defined core stability as ‘the ability to control the position and motion of the trunk over the pelvis,
1360-8592/$ - see front matter Crown Copyright ª 2010 Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.jbmt.2010.12.001
518 thereby allowing optimum production, transfer and control of force and motion to the terminal segment in integrated athletic kinetic chain activities’. The role of core muscles in movement is varied according to the dynamics and postural demands of a given activity (Brown, 2006; Rogers, 2006). The core region can be divided into local and global groups (based on location and attachment site) (Johnson, 2002). Local muscles consist of small, deep muscles that control intersegmental motion between adjacent vertebrae (Johnson, 2002) and act as ‘stabilizers’ (Carter et al., 2006). Global muscles are large, superficial muscles that transfer force between the thoracic cage and pelvis and play a role in creating movement (Carter et al., 2006). As the core is central to most kinetic chains in sports movements, control of core strength, balance and motion will maximize the kinetic chains of upper and lower extremity function (Kibler et al., 2006), resulting in more efficient, stronger and powerful movements (Hedrick, 2000; McCurdy et al., 2005). Hence, there is an assumption that an improved core will increase one’s ability to run, jump, throw, strike and swing. There are two primary types of core training; static and dynamic training. Static training involves the joint and muscle either working against an immovable force (maximal muscle action) or being held in a static position while opposed by resistance (sub-maximal muscle action) (Siff, 2004). Actions within a wide variety of sports require isometric strength; for example, climbing, mountain biking, Judo, wrestling, gymnastics and horseback riding (Stone et al., 2003). Dynamic strength is the ability to exert a muscle force concentrically or eccentrically repeatedly or continuously over time. Due to the body’s functional design, during dynamic movement there is more dependence on core musculature than just skeletal rigidity as in a static situation; as the purpose of movement is to resist a force that changes its plane of motion (Siff, 2004). The surface the core exercise is performed on can also be varied to attempt to stimulate increased core activation through increased proprioceptive demands compared to floor based exercises (Cosio-Lima et al., 2003). Dynamic exercises performed on unstable surfaces are unable to reproduce the force and power outputs found when performing the same exercise on a stable surface (Anderson and Behm, 2005; Carter et al., 2006; McGill, 2001; Scibek et al., 2001) thus questioning the use of performing conventional exercises on unstable surfaces to enhance the transfer of training effect for the prescribed movement. However the transfer of training effect of dynamic core exercises into dynamic movements has not been investigated. There is disagreement amongst coaches about which type of strength is preferably developed for optimal performance (Plamondon et al., 1999; Stone et al., 2003). Past research has shown a positive transfer of training effect of dynamic exercises to dynamic tasks and static exercise to static tasks for non-core musculature (O’Shea and O’Shea, 1989). Several investigators also suggest that isometric forceetime characteristics are poorly correlated with dynamic performance (Haff et al., 2005; Murphy and Wilson, 1996). This indicates a limited transfer of training of static core exercises to dynamic performance. The use of field based fitness tests is an easy and convenient assessment method to allow coaches and users to track and monitor progress following an intervention (Winter
K.L. Parkhouse, N. Ball et al., 2007). The assessment of further neuromuscular and kinetic adaptations or transfer would require the use of specific technology such as electromyography (Winter et al., 2007), linear encoders (Harris et al., 2010) and force platforms (Winter et al., 2007) which are not freely available. The purpose of the study was to compare the effects of a 6week unstable static versus unstable dynamic core stability training program on core strength and other performance variables. Based on the principle of specificity, we predict a positive transfer of training effect of dynamic core exercise to the dynamic based tasks and a positive transfer of training effect of static core exercise to the static based tasks.
Methods Experimental approach to the problem This study involved a two group, two factor design to address whether a static or dynamic core stability ball intervention improved core and field based performance tests. Factor one was test, which had two levels: pre- and post testing. Factor two was training, which also had two levels: static or dynamic group. Dependent variables included 3 measurements of core performance (a static plank and double leg lowering test and a dynamic back extension test), 3 dynamic performance tests for speed (20 m sprint), lower body power (vertical jump), upper body power (overhead medicine ball throw) and a static balance test (standing stork).
Participants A group of 12 participants (6 male: 21.2 3.3 years; 174.5 6.3 cm; 78.7 3.7 kg, 6 female: 20.6 1.7 years; 172.6 4.7 cm; 67.7 2.3 kg) volunteered for the study. Informed consent was obtained and health history questionnaires were completed. All participants competed in University level sport >8 h per week and reported no history of acute or chronic low back injury prior to this experiment. All participants had prior experience of core stability exercises but had never undertaken a prescribed core stability program. Participants were asked to refrain from any other form of core specific exercises during the training period. Before commencement, the University Ethics review board approved the study. Participants were randomly assigned to either the static or dynamic core stability training group ensuring an equal gender split in each group.
Testing procedures Participants were instructed on how to perform each test and were allowed a familiarization period. Participants recorded their assessed test no less than 3 min following the familiarization period. Sufficient rest of at least 10 min was given between each test. Participants were told to put in maximal effort throughout each test whilst maintaining the correct position of the lumbar spine, with correct technique overseen by a qualified strength and conditioning coach. The battery of seven tests were completed 1 week prior to the training interventions and repeated one week after the training interventions. All tests were randomised for each participant to minimize learning effects.
Influence of dynamic versus static core exercises on performance in field based fitness tests
Static core tests Plank Participants were required to lie face down on a mat with their forearms and toes on the floor. On command, participants were asked to raise their hips off the floor to form a straight line from the shoulders to the heels, with a neutral back. Tests commenced once the correct position was assumed and discontinued when the position changed. A demonstration was shown and teaching points emphasized. The test was timed (s) using a stopwatch. Double leg lowering Participants laid with their back on a mat and knees to chest. After contracting the core region, they slowly slid both legs out into a straight position, with feet remaining 5 cm off the floor at all times. Participants were instructed to keep a neutral back for the duration of the test. Tests were discontinued when the body position changed or when legs became less than 180 to the body. The test was timed (s) using a stopwatch.
Dynamic core test Back extensions Participants were required to lay face down with hands at the temples. The number of repetitions performed was recorded in 2 min. They were encouraged to avoid lifting the feet off the floor to avoid the gluteus maximus aiding the lower back. A back extensor endurance test was used rather than a common curl-up test because there is only very low correlation of curl-up tests with core strength and endurance (Knudson, 2001), whereas back extensor tests give a better indication of lumbo-pelvic stability and strength.
Static field based test Standing stork (balance) Participants stood with hands on hips and were instructed to lift 1 leg and place the sole of the foot on the inner thigh of the other leg. On command, participants raised the heel of the straight leg to stand on the toes. Participants were required to balance for as long as possible without the heel of the foot touching the ground, or the other foot moving away from the knee. The test was repeated on the other leg. The test was timed (s) using a stopwatch.
Dynamic field based tests Overhead medicine ball throw (upper body power) Participants were required to kneel with the back erect, facing the throwing direction with their knees just behind the start line. With a 4 kg medicine ball grasped in both hands, participants were instructed to bring the ball back over the head and in 1 motion, throw the ball forwards and upwards with maximal power. It was emphasized that the spine must not be rotated and the favored arm must not be used to throw the arm. Stockbrugger and colleagues (Stockbrugger and Haennel, 2001) have shown this test to be a valid and reliable test for assessing explosive core and upper body power.
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Vertical jump (lower body power) Vertical jump height was taken from a static position with both feet together. Participants were instructed to place both hands on their hips and upon a verbal signal selfselected their depth for the countermovement jump. Participants were required to jump vertically as high as they could. The jump height was recorded (cm) using a vertical jump meter (Takei, Japan). 20 m sprint (speed) A straight 20 m line was measured and marked with cones. Light gates (Brower, UK) were positioned at both 0 m and 20 m. Participants were asked to start with their feet behind the start cone and to perform the task maximally. On the commands ‘take your marks’ and then ‘go’ participants were asked to sprint towards and the time gates at the 20 m mark. Time (s) was recorded from the timing gates.
Training procedure Each training group was required to attend two 45 min training sessions per week with a three day gap between each session. Three days prior to the commencement of the first training session, participants completed a familiarization session to ensure they were comfortable with the procedures and to minimize any learning effects. During this they practiced the concepts of ‘drawing in’ (neutralizing the spine and working the transverse abdominis and multifidus), correct postural control, the importance of breathing (Carter et al., 2006; Gamble, 2007) and stability ball balance (Goodman, 2003). Each participant was given a ball that was in accordance to their height. The size of the ball was conducive to achieving >90 angle at both the hip and knee (Goodman, 2003). The stability balls were 55, 65 or 75 cm in diameter. At the start of each training session, participants completed a thorough 10 min warm-up which included exercises such as jogging, skipping, but kicks and side stepping, followed by static stretching and specific lumbo-pelvic mobility exercises to reduce injury risk and lower back pain. Stretching was also completed upon completion of each session. All participants in both training groups completed 6 exercises per session. Overload was provided in the forms of increased duration and frequency (sets, reps, time under tension), increasing the complexity of exercises (adding opposite limb movements), increasing the lever arm of the exercises, altering the base of support and increased loading (external weights) (Gamble, 2007) (see Tables 1 and 2). The static group used a duration of 20 s or more when using submaximal loads (such as body weight) and 8e10 s with external resistance. The dynamic group performed 16 or more repetitions when using sub-maximal loads and 8e12 repetitions with external resistance. Exercises are based on previous references for core exercise prescription and were considered safe and effective (Cissik, 2002; Goodman, 2003; Hedrick, 2000; Lehman et al., 2005; Plamondon et al., 1999; Stanton et al., 2004; Vera-Garcia et al., 2000).
Statistical analyses On the completion of data collection, statistical analyses comprised of descriptive statistics to identify means and standard deviations for each variable of interest. The initial
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K.L. Parkhouse, N. Ball
Table 1
Static core stability program. Exercise, frequency, duration and applied progression and overload for each week.
Exercise
Week 1
Week 2
Week 3
Week 4
Week 5
Week 6
a
Time e secs (sets) Instruction
Time e secs (sets) Progression Time e secs (sets) Progression Time e secs (sets) Progression
Time e secs (sets) Progression Time e secs (sets) Progression
Side planka
Shoulder bridge
Full plank
Birddoga
Diagonal cruncha
Reverse hyperextension
25 (2)
30 (2)
25 (2)
30 (2)
20 (2)
15 (2)
On elbow, Top arm by side 35 (2)
Arms to side, feet wide, knees bent 45 (2)
Knees dropped, on elbows
1 leg only
Hands on knees
Hands by side
35 (2)
40 (2)
30 (2)
25 (2)
Increase time 25 (2)
Forearms up, increase time 35 (2)
Increase time
Increase time
35 (2)
30 (2)
Increase time 25 (2)
Increase time 35 (2)
Top arm in air 25 (2)
1 leg straight
On elbows, legs straight 45 (2)
Opposite arm & leg 40 (2)
Hands on chest 35 (2)
Arms on chest 45 (2)
Both legs straight, heels on ball
Increase time
Increase time
Increase time
Increase time
40 (2)
40 (2)
30 (2)
30 (2)
30 (2)
Arms off floor, increase time 40 (2)
On hands with legs straight 45 (2)
Both arms and 1 leg 40 (2)
Hands by temples 40 (2)
Hands by temples 40 (2)
Lift 1 leg off the ball
Increase time
Increase time
Increase time
Increase time
35 (2)
Bottom arm on hand, top arm by side 35 (2) Increase time 35 (2) Top arm in air
Z each side.
data was analyzed and it determined that data was parametric. Therefore, A 2 2 (static, dynamic test time) multivariate analysis of variance (MANOVA) with repeated measures was performed to determine the effect of training
Table 2
Dynamic core stability program. Exercise, frequency, duration and applied progression and overload for each week.
Exercise
Jack knife
Russian twista
Reverse hyperextension
Lateral rolla
Hip crossovera
Reverse crunch
8 (2) Hands together, wide feet 10 (2) Increase reps 10 (2) Narrow feet 12 (2) Increase reps
25 (2) Arms by side
8 (2) Wide feet
8 (2) Arms by side
20 (2) Arms on knees
35 (2) Increase reps 35 (2) Hands on chest 45 (2) Increase reps
12 (2) Increase reps 12 (2) Narrow feet 8 (2) Increase reps
30 (2) Increase reps 25 (2) Arms on chest 35 (2) Increase reps
10 (2) Add weight plate 12 (2) Increase reps
40 (2) Arms in front
10 (2) Lift 1 leg
10 (2) Increase reps 12 (2) Increase reps 8 (2) Elbows up, hands on chest 10 (2) Increase reps
45 (2) Increase reps
12 (2) Increase reps
12 (2) Increase reps
Week 1
Reps (sets) Instruction
Week 2
Reps (sets) Progression Reps (sets) Progression Reps (sets) Progression
8 (2) Hands wide, knees on ball 12 (2) Increase reps 12 (2) Hands narrow 8 (2) Toes on ball
Week 5
Reps (sets) Progression
12 (2) Increase reps
Week 6
Reps (sets) Progression
16 (2) Increase reps
Week 3 Week 4
a
on each parameter measured. Independent variables were gender, age and training type. Mauchly’s test of sphericity revealed that my data remained normally distributed across all time points (P > 0.05). Where a main effect was observed,
Z each side.
30 (2) Hands by temples 40 (2) Increase reps
Influence of dynamic versus static core exercises on performance in field based fitness tests a least significant difference (LSD) post hoc analysis was conducted to identify the source of the difference (P < 0.05). Further analysis of the data was carried out using Pearson’s correlation coefficient which identified inter-relationships between all test variables. All statistical analysis was carried out using SPSS for windows version 14. Intra-subject reliability was based on the vertical jump scores with an intraclass correlation coefficient of 0.95 obtained.
Results Static/dynamic core and field based tests Table 3 presents the results of each core and field based test for both training groups before and after 6 weeks of training. The mean scores of the dynamic core training group were improved at the post-test in six out of the seven functional tests; however the mean scores of the static core training group only showed improvement in five out of seven tests. Both groups improved in all core based tests (Static Group e Plank: F (1 10) Z 11.755, P Z 0.000; Double leg lowering: F (1 10) Z 1.04, P Z 0.000; Back Extension: F (1 10) Z 97.5, P Z 0.006; Dynamic Group e Plank: F (1 10) Z 81.8, P Z 0.000; Double leg lowering: F (1 10) Z 40.1, P Z 0.000; Back Extension: F (1 10) Z 16.64, P Z 0.002). Post Hoc LSD found the
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dynamic training group to show greater improvements than the static group in all 3 core tests (P < 0.05). No improvements were found in any of the dynamic tests for both static and dynamic groups (P > 0.05). However, standing stork scores increased in the static group post training (F1 10 Z 1.16, P Z 0.000) (Fig. 1). For the static training group, Pearson’s Correlation coefficient found strong positive relationships between the plank/double leg lowering test (0.817), plank/vertical jump height (0.821), and standing stork/double leg lowering test (0.820). Very strong negative relationships were found for the plank/20 m sprint test (0.927), and double leg lowering/20m sprint test (0.822). The dynamic training group was found to have strong positive relationships between the plank/20 m sprint test (0.942), and moderately strong positive relationships between medicine ball throw/back extensions (0.805) and between 20 m sprint/ vertical jump height (0.794).
Discussion The purpose of the study was to compare the effects of a 6 week core stability training program with exercises performed on an unstable surface on field based performance tests. This study suggests that 6 weeks of both static and
Table 3 Static and dynamic core and field based test results after 6 weeks of training for both static and dynamic training groups (means SD). Static indicates the group that performed a static core training program; Dynamic indicates that the group performed a dynamic core training program. n Static core tests Plank (sec) Static 6 Dynamic 6 Double leg lowering (sec) Static 6 Dynamic 6 Dynamic core tests Back extension (reps) Static 6 Dynamic 6 Static field based tests Standing stork (sec) Static 6 Dynamic 6 Dynamic field based tests Vertical jump (cm) Dynamic 6 Static 6 20 m Sprint (sec) Static 6 Dynamic 6 Medicine ball throw (m) Static 6 Dynamic 6 NS Z P > 0.05. * Z P < 0.01. * Z P < 0.001.
Pre
Post
% Difference
p
59.0 4.69 51.76 4.43
64.0 4.6 63.8 5.04
8.5% 23.3%
** **
25.65 2.62 24.68 2.45
28.18 3.78 35.43 2.58
9.9% 43.6%
** **
67.00 4.34 65.60 2.16
77.80 2.64 70.10 1.94
14.9% 45.8%
* *
3.98 0.17 4.42 0.43
6.55 0.44 4.80 0.48
64.5% 8.6%
** NS
33.4 1.92 32.9 1.36
32.7 2.16 34.7 1.75
0.9% 6.1%
NS NS
5.56 0.48 5.51 0.31
5.50 0.30 5.59 0.41
1.1% 1.4%
NS NS
3.48 0.36 3.53 0.22
3.58 0.26 3.5 0.22
2.9% 0.8%
NS NS
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Figure 1 Mean pre- and post training standing stork scores for both groups (N Z 12).
dynamic type core training improves core performance (P < 0.05). However, no transfer of training effect to the dynamic tests was shown (P > 0.05). This is the first empirical study to examine the effect of static versus dynamic core stability ball training on physical performance. While core stability ball training remains a popular adjunct to training for many athletes and anecdotal evidence supports its widespread use, results of this study appear to be consistent with previous research which has found no transfer of training effect (Nesser et al., 2008; Scibek et al., 2001; Tse et al., 2005). The static training group had a significant transfer into the balance test, which accepts part of our hypothesis and is similar to previous research. Rutherford and Jones (Rutherford and Jones, 1986) found that early adaptations in short term static core training resulted in greater gains in torso balance. Supporters of instability training propose the neuromuscular system is challenged to a greater extent and increases proprioceptive demands (Rutherford and Jones, 1986). The unstable nature of the ball forces one to make postural adjustments to increase co-ordination, which require activation of the appropriate core musculature to stabilize the lumbar spine. The deep postural muscles of the trunk have a primary purpose to ensure this lumbar stabilization and to maintain the body’s centre of gravity within its base of support to minimize loss of balance (Anderson and Behm, 2005). However, although static core training has proved effective in a measure of static balance, more sports specific research may be needed to clarify this transfer. No improvements were found in the overhead medicine ball throw, 20 m sprint and vertical jump height scores post both static and dynamic training. These results provide no support for the proposal of a more enhanced and efficient transfer of energy due to an enhanced core. Therefore we reject part of our hypothesis in that dynamic exercise will demonstrate a positive transfer of training effect to dynamic tasks. This is in agreement with Scibek and colleagues (Scibek et al., 2001) who looked at the effect of Swiss ball core stability training on subsequent swim performance. Their results showed enhanced core strength in static exercises
K.L. Parkhouse, N. Ball however no improvements in swim performance. Furthermore Nesser and colleagues (Nesser et al., 2008) showed no correlation of core strength to strength and power measures in collegiate athletes. This indicates that power performance may not be affected by core strength refuting previous claims. However core training has been shown to improve 5,000 m run times (Sato and Mokha, 2009) indicating that core training modalities may have a better transfer to more endurance based events in the resistance of fatigue and maintenance of posture (Brumitt, 2004). Stanton and colleagues (Stanton et al., 2004) showed no improvement in running economy, however did not include a timed measure for the run trials performed. These studies and the current study’s findings support the notion that core training emphasizes local muscle adaptation and core strength without concomitant improvements in power based physical performance. Although the outcomes appear clear, it must be highlighted that only 12 participants were used in the study. We suggest that any future studies in this area should include a much larger sample size to ensure sound reliability of results. Furthermore, the transfer of training effect of the dynamic core exercises to the dynamic movements may have required a longer duration training program or an increased frequency of sessions. Early phase adaptations including increased stability, neuromuscular activity and proprioceptor activity have been shown after 5 weeks of training doing abdominal and one lower back exercise per day (Cosio-Lima et al., 2003), however these improvements were shown mainly in neuromuscular changes opposed to strength changes as measured by isokinetic testing. Thus the neuromuscular control and co-ordination trained by core dynamic exercises may only improve muscular recruitment in the initial phases opposed to the transferring into an external measure. Thus the benefits of the core training program here for the dynamic exercise may not be transfer into performance measures but may potentially improve kinematic and kinetic measures. Alongside program duration the nature of the exercise used may be changed for athletes with free weight exercises using moderate levels of instability may be more suitable to maintain specificity (Behm et al., 2010). The concept of specificity suggests that quick, explosive dynamic performance variables are likely to be improved by similar type training actions. To train improved speed of force application more importance is placed on performing the exercise powerfully compared to the selection of the exercise movement (Behm and Sale, 1993). Although dynamic exercises were performed by the dynamic training group, explosive power and high rates of force development were not emphasized and subsequently not transferred over. A lower repetition range with emphasis on increased speed of movement whilst maintaining lumbo-pelvic stability may have seen a better transfer into the sprint, jump and throw tests as the core would be trained in a similar manner to its use within these tests. The loading measures used in this study may not have been sufficient to improve core muscle function during dynamic exercises. Hibbs and colleagues (Hibbs et al., 2008) suggested that the cores are trained more for everyday requirements (low loads, slow movements) opposed to an athlete requirement of high load and resistive movements. The population group in this study
Influence of dynamic versus static core exercises on performance in field based fitness tests indicated a better use of their core strength in static movements compared to the high force dynamic field tests. In summary, the results of this study suggest that 6 weeks of stability ball training doesn’t improve dynamic field based performance tests based on the sample size used. The benefits of core training may reside in long term athlete development programmes whereby appropriate posture and core strength may transfer into improved co-ordination and exercise performance. Increases in training duration and speed of movement in dynamic core exercises may provide a more specific stimulus of the core for transfer into dynamic field based movements, however this warrants further investigation.
Practical applications The current study shows that both static and dynamic core stability exercises trained over a 6-week period are able to effectively increase the core strength of participants. These strength benefits do not transfer into improved dynamic performance in sprinting, throwing and jumping. The study indicates that short term training may only improve core strength by reducing fatigue in the core musculature and allowing the athlete more neuromuscular control during balance. A program that incorporates both static and dynamic exercises may provide these benefits if the dynamic exercises are then performed with increased velocity. This may improve the transfer of training effect into dynamic performance. It must be understood that the findings may only be applicable to the population under investigation and the effects on elite athletes is unknown. However due to the assumed improved core strength and physicality of elite performers it can be assumed that their scope for adaptation is smaller than the current population and thus non-significant finding for core transfer into dynamic performance can be reasonably assumed. Findings do not discourage the use of core stability ball training; instead, they suggest that specificity on the rate of force development, speed and power of each core exercise may be needed to transfer into sporting performance.
Acknowledgements Sincere thanks to all the participants who devoted their time and effort to this study.
References Anderson, K., Behm, D.G., 2005. The impact of instability resistance training on balance and stability. Sports Medicine 35, 43e53. Behm, D.G., Sale, D.G., 1993. Intended rather than actual movement velocity determines velocity-specific training response. Journal of Applied Physiology 74, 359e368. Behm, D.G., Leonard, A.M., Young, W.B., Bonsey, W.A., MacKinnon, S.N., 2005. Trunk muscle electromyographic activity with unstable and unilateral exercises. Journal of Strength and Conditioning Research 19, 193e201. Behm, D.G., Drinkwater, E.J., Willardson, J.M., Cowley, P.M., 2010. The use of instability to train the core musculature. Applied Physiology, Nutrition, and Metabolism 35, 91e108.
523
Beache, T.R., Earle, R.W., 2000. Essentials of Strength Training and Conditioning. Human Kinetics, Champaign, IL. Boyle, M., 2004. Functional Training for Sports. Human Kinetics, Champaign, IL. Brown, T.D., 2006. Getting to the core of the matter. Strength and Conditioning Journal 28, 50e53. Brumitt, J., 2004. The missing component to core training: endurance. NSCA Performance Training Journal 3, 233e239. Carter, J.M., Beam, W.C., McMahan, S.G., Barr, M.L., Brown, L.E., 2006. The effects of stability ball training on spinal stability in sedentary individuals. Journal of Strength and Conditioning Research 20, 429e435. Chek, P., 1999. Swiss ball exercises for swimming, soccer & basketball. Sports Coach 21, 12e13. Cissik, J.M., 2002. Programming abdominal training, part 1. Strength and Conditioning Journal 24 (1), 9e15. Cosio-Lima, L.M., Reynolds, K.L., Winter, C., Paolone, V., Jones, M.T., 2003. Effects of physioball and conventional floor exercises on early phase adaptations in back and abdominal core stability and balance in women. Journal of Strength and Conditioning Research 17, 721e725. Gamble, P., 2007. An integrated approach to training core stability. Strength and Conditioning Journal 29, 58e68. Goodman, P.J., 2003. The core of the workout should be on the ball. NSCA Performance Training Journal 2, 34e38. Haff, G.G., Carlock, J.M., Hartman, M.J., Kilgore, J.L., Kawamori, N., Jackson, J.R., Morris, R.T., Sands, W.T., Stone, M.H., 2005. Forcetime curve characteristics of dynamic and isometric muscle actions of elite women olympic weightlifters. Journal of Strength and Conditioning Research 19, 741e748. Harris, N.K., Cronin, J., Taylor, K., Jidovtseff, B., Sheppard, J., 2010. Understanding position transducer technology for strength and conditioning practioners. Journal of Strength and Conditioning Research 32 (4), 66e79. Hedrick, A., 2000. Training the trunk for improved athletic performance. Strength and Conditioning Journal 22, 50e61. Hibbs, A.E., Thompson, K.G., French, D., Wrigley, A., Spears, I., 2008. Optimizing performance by improving core stability and core strength. Sports Medicine 38, 995e1008. Jeffreys, I., 2002. Developing a progressive core stability program. Strength and Conditioning Journal 24, 65e66. Johnson, P., 2002. Training the trunk in the athlete. Strength and Conditioning Journal 24, 52e59. Kibler, W.B., Press, J., Sciascia, A., 2006. The role of core stability in athletic function. Sports Medicine 36, 189e198. Knudson, D., 2001. The validity of recent curl-up tests in young adults. Journal of Strength and Conditioning Research 15, 81e85. Lehman, G.L., Gordon, T., Langley, J., Pemrose, P., Tregaskis, S., 2005. Replacing a Swiss ball for an exercise bench causes variable changes in trunk muscle activity during upper limb strength exercises. Dynamic Medicine 4. doi:10.1186/1476-5918-4-6. Marshall, P.W., Murphy, B.A., 2005. Core stability exercises on and off a Swiss ball. Archives of Physical Medicine and Rehabilitation 86, 242e249. doi:10.1016/japmr.2004.05.004. McCurdy, K.W., Langford, G.A., Doscher, M.W., Wiley, L.P., Mallard, K.G., 2005. The effects of short-term unilateral and bilateral lower-body resistance training on measures of strength and power. Journal of Strength and Conditioning Research 19, 9e15. McGill, S.M., 2001. Low back stability: from formal description to issues for performance and rehabilitation. Exercise and Sport Science Reviews 29, 26e31. Murphy, A.J., Wilson, G.J., 1996. Poor correlations between isometric tests and dynamic performance: relationship to muscle activation. European Journal of Applied Physiology and Occupational Physiology 73, 353e357. doi:10.1007/BF.0242.5498. Nesser, T.W., Huxel, K.C., Tincher, J.L., Okada, T., 2008. The relationship between core stability and performance in division
524 I football players. Journal of Strength and Conditioning Research 22, 1750e1754. O’Shea, K.L., O’Shea, J.P., 1989. Functional isometric weight training: its effect on dynamic and static strength. Journal of Applied Sport Science Research 3, 30e33. Plamondon, A., Marceau, C., Stainton, S., Desjardins, P., 1999. Toward a better prescription of the prone back extension exercise to strengthen the back muscles. Scandinavian Journal of Medicine and Science in Sports 9, 226e232. Rogers, R.G., 2006. Research-based rehabilitation for the lower back. Strength and Conditioning Journal 28, 30e35. Rutherford, O.M., Jones, D.A., 1986. The role of learning and coordination in strength training. European Journal of Applied Physiology 55, 100e105. Sato, K., Mokha, M., 2009. Does core strength training influence running kinetics, lower extremity stability and 5000-M performance in runners? Journal of Strength and Conditioning Research 23, 133e140. Scibek, J.S., Guskiewicz, K.M., Prentice, W.E., Mays, S., Davis, J.M., 2001. The effect of core stabilization training on functional performance in swimming. Master’s Thesis, University of North Carolina, Chapel Hill. Siff, M.C., 2004. Supertraining. Supertraining Institute, Denver.
K.L. Parkhouse, N. Ball Stanton, R., Reaburn, P.R., Humpries, B., 2004. The effect of short-term Swiss ball training on core stability and running economy. Journal of Strength and Conditioning Research 18, 522e528. Stockbrugger, B.A., Haennel, R.G., 2001. Validity and reliability of a medicine ball explosive power test. Journal of Strength and Conditioning Research 15, 431e438. Stone, M.H., Sanborn, K., O’Bryant, H.S., Hartman, M., Stone, M.E., Proulx, C., Ward, B., Hruby, J., 2003. Maximum strength-power-performance relationships in collegiate throwers. Journal of Strength and Conditioning Research 17, 739e745. Tse, M.A., McManus, A.M., Masters, R.S., 2005. Development and validation of a core endurance intervention program: implications for performance in college-age rowers. Journal of Strength and Conditioning Research 19, 547e552. Vera-Garcia, F.J., Grenier, S.G., McGill, S.M., 2000. Abdominal muscle response during curl-ups on both stable and labile surfaces. Physical Therapy 80, 564e569. Winter, E.M., Jones, A.M., Davison, R., Bromley, P.D., Mercer, T., 2007. Sport and Exercise Physiology Testing Guidelines: Exercise and Clinical Testing. Routledge, USA.
Journal of Bodywork & Movement Therapies (2011) 15, 525e527
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PREVENTION & REHABILITATION: EDITORIAL
Stimulus and response
Primal Lifestyle, Unit 5 Glebelands, Vincent Lane, Dorking, Surrey RH4 3HW, UK The very origins of life on Earth were based on a stimuluseresponse; a photoreceptive pigment responding to the stimulus of the sunlight. From this the most basic of hormonal systems evolved, and from around 3.5 billion years ago, an electrochemical dance was the key controlling influence on the behavior of organisms. It wasn’t for, nigh-on, a further 3 billion years (around 490 million years ago) that organisms had evolved to the extent that a nervous system had formed along the axis of the organism’s body to allow for a higher-speed stimuluseresponse system (Raff, 1996). It is of little surprise, then, that at this current juncture of evolution, the ability of the human organism to respond to the stimuli applied to it is both deeply complex and intricately wired so as to have plethoric interwoven and back-up systems. However, this doesn’t stop such systems from sometimes crashing, nor does it necessarily inform our methods of rehabilitating crashes. It is this author’s belief that understanding the way the system is wired should provide deep insights into how to effectively re-wire it, when such crashes do occur. In this Rehabilitation & Prevention section there are two very similar, yet very disparate papers featured. The first is a paper, which is more of a classic manual therapy-style review paper looking at the evidence behind reported successes of various interventions: Movement therapy induced neural reorganization and motor recovery in stroke: A review (Arya et al., 2011). The second paper is a brief case study of a patient with chronic migraine who is treated using the Vojta and DNS approaches which have evolved from the same centre in Prague that gifted the world of manual therapy with Vladimir Janda and Karel Lewit, among others: A case study utilizing Vojta/Dynamic Neuromuscular Stabilization
E-mail address:
[email protected].
therapy to control symptoms of a chronic migraine sufferer (Juehring and Barbara, 2011). To better understand what these papers offer, a brief description of three useful clinical models is presented below.
Modeling & human health According to Holland (2000) “A well conceived model can yield organized complexities that repay decades and centuries of study. If the [model] is faithful, we can make predictions into the indefinite future” In this editorial, there are 3 models shared with the reader to help to contextualize the research papers. The first is Panjabi’s famous model of joint stability. The second is a schema for motor learning described by Lederman. The last is the author’s own evolutionary model designed to provide a hierarchical understanding of ascending and descending influences on human health.
Motor control In 1992, Panjabi proposed the model of joint stability in which he described the 3 key components for optimal motor control about the joint. These comprised the passive, the active and the neural components of the joint. Disruption to any of these components would compromise the overall function of the joint (Figure 1). How this may be applied to the papers featured in this section is that, far from just activating the muscles in nonspecific electrochemical ways, the effective retraining of muscle activation must surely depend on dynamic interplay of information coming in to the nervous system from higher centers and from the passive (connective) and active (muscular) tissues.
1360-8592/$ - see front matter ª 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.jbmt.2011.07.001
PREVENTION & REHABILITATION e EDITOR: MATT WALLDEN
Matt Wallden, MSc Ost Med, BSc (Hons) Ost Med, DO, ND
PREVENTION & REHABILITATION e EDITOR: MATT WALLDEN
526
Figure 1 Panjabi et al.’s (1989) model of joint stability predicts that for optimal joint function each of the 3 components must be fully functional. If the nervous system is aberrant (inhibited, facilitated or dyssynergic), motor recruitment cannot be optimal and will result in stress on the passive system. The passive system is the primary component of feedback for the neural system (including joint proprioception, mechanoreception and even spindle cell feedback from tendons), so any dysfunction at the passive level (inflammation, neovascularisation, creep or contracture) will disrupt optimal afferent information processing. The efferent drive to the active system, controlled by the neural subsystem, will only be as effective as the afferent drive coming into the neural system.
Manual treatment of muscles may have useful physiological effects that enhance their ability to respond to subsequent or accompanying rehabilitation protocols, however, when applied in isolation, repatterning of motor habits is improbable, so the likelihood of long-term benefits are questionable. Indeed this is what is found in the Arya et al’s. (2011) paper and what is implied by the Juehring and Barbara’s (2011) paper.
Motor learning In 1997, Lederman described a motor learning model in which he explained that in order for there to be habitual changes in a patient’s motor behavior, active engagement of the patient is required; over and above simple passive approaches (such as massage, stretching, mobilization or manipulation) (Figure 2). How this model relates to the papers included in this section is that the Arya et al’s. (2011) paper demonstrates that passive modalities are now rarely used and/or require more research to demonstrate efficacy; while the active approaches, which engage central processes are enjoying greater clinical success, as the model predicts. The Juehring and Barbara’ (2011) case study demonstrates that, while the more passive Vojta’ approach may facilitate deeply embedded neural programs, the DNS approach adds a further active component to the therapeutic intervention; which is, likely, key to the favorable outcome, as predicted by Lederman’s model.
Dimensional mastery Lastly, in 2008, Wallden proposed a model of dimensional mastery (Wallden, 2008, 2010) in which it is suggested that
M. Wallden
Figure 2 Lederman’s schema of motor learning predicts that passive modalities applied to the patient, will only have a temporary effect based on their influence being modulated primarily subcortically (at the segmental/peripheral reflexive level). In contrast, skilled active modalities applied by the patient must, by their nature, be centrally processed and therefore influence motor habits, creating more permanent changes in motor behaviour.
the evolution of morphophysiology provides insight into the foundations of human function and therefore the processes through which human function can be restored. How this model relates to the papers in this section is that it implicates breathing and eating as fundamental underpinning to health, the former of which is an integral part of the Vojta/DNS approach. It also suggests that dimensional mastery (mastery of each of the dimensions of space) follows a specific sequence, which just so happens to be the sequence of mastery seen in the evolution of species and in infant motor development; something also described in the Vojta/DNS approach (Juehring and Barbara, 2011), but found to be missing in the Stroke rehabilitation approaches described (Arya et al., 2011). It is also apparent that when isolationbased approaches are utilized their success is limited, such as the bodyweight supported treadmill training, described by Arya et al. (2011). From a dimensional mastery point of view, this would figuratively be learning to run before you can walk, or more literally, learning to walk before you can crawl, creep, twist, turn or breathe functionally. Finally, as you follow the natural progression of the dimensional mastery model (Figure 3) where the 3 dimensions of space become mastered, the next progression is to consider both the 4th and the 5th dimensions. The 4th is the dimension of time and mind, while the 5th is the dimension outside of spaceetime where, traditionally, spirituality, non-locality, and the timeless dwells. In the context of the two papers presented, the Stroke paper demonstrates that the use of mind from a practitioner perspective to deduce complex, often expensive, approaches to rehabilitation may sometimes yield poor results; if mastery of the foundation spatial dimensions is not first mastered. Both papers demonstrate that repetition is required to learn new e or to re-learn old e skills (as described by Lederman, 1997) and that repetition can, of course, only occur across the 4th dimension of time.
Editorial
527 The stroke paper also highlights that, from a patient’s perspective, if the mind (4th dimensional) focus is specific enough, it may be of benefit to the patients recovery, in the form of mental imagery. However, both papers highlight the requirement for the patient’s engagement, their interaction, their embracing of their rehabilitation program; and it is this prerequisite e their belief in the process, that is perhaps most key.
Conclusion
References Holland, J., 2000. Emergence. OUP, Oxford. Lederman, E., 1997. Fundamentals of Manual Therapy. Churchill Livingstone, Edinburgh, pp. 105. Panjabi, M., Abumi, K., Duanceau, J., Oxland, T., 1989. Spinal stability and intersegmental muscle forces. A biomechanical model. Spine 14 (2), 194e200. Raff, R., 1996. The Shape of Life e Genes, Development, and the Evolution of Animal Forms. University of Chicago Press, Chicago. Wallden, M., 2008. In: Chaitow, L. (Ed.), Rehabilitation & Movement Re-education Approaches in Naturopathic Physical Medicine. Wallden, M., Nov 2010. Phylontogenic factors in motor control: an organismal model of systems integration in motor control. In: 7th Interdisciplinary World Congress on Low Back and Pelvic Pain. Los Angeles; pp. 542e544.
PREVENTION & REHABILITATION e EDITOR: MATT WALLDEN
Figure 3 Wallden’s model of dimensional mastery recognizes how development of increasing neurological complexity across time correlates with the greater computational power required to master the 4 dimensions of spaceetime reality. The model predicts that if a foundational level of mastery is impaired or forgotten, mastery of each successive dimension will be incomplete or unstable. Clinically, it predicts nutritional and respiratory function underpins movement function, and that movement function will most effectively be built through mastery of peristaltic (radial) contraction, followed by frontal (lateral), followed by sagittal (front-back), and concluded by transverse plane (rotational) motions. The neurological complexity required to master such movement patterns is a system that has the neural capacity to create mind (and to conceptualize time). The transcendence of mind and time, moving outside of the space-time continuum, is considered the 5th dimension; often referred to as the spiritual realm.
The message is, if the foundations are in place, the program is intelligently designed to invoke the correct stimuli across time, and the patient has no doubt in their mind, and therefore truly believes in the process, then the response is likely to be most optimal.
Journal of Bodywork & Movement Therapies (2011) 15, 528e537
available at www.sciencedirect.com
journal homepage: www.elsevier.com/jbmt
REHABILITATION
Movement therapy induced neural reorganization and motor recovery in stroke: A review
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Kamal Narayan Arya, MOT, PhD Scholar (Neurology), Sr. Occupational Therapist a,b,*, Shanta Pandian, MOT (Neurology), Superintendent OT (OPD) b, Rajesh Verma, DM (Neurology), DNB (Neurology), Professor a, R.K. Garg, DM (Neurology), Professor & HOD a a
Department of Neurology, CSM Medical University (KGMU), Lucknow, UP 226003, India Pt. Deendayal Upadhyaya Institute for the Physically Handicapped, University of Delhi, Ministry of Social Justice & Empowerment, Govt. of India, New Delhi 110002, India
b
Received 7 October 2010; received in revised form 22 January 2011; accepted 29 January 2011
KEYWORDS Stroke; Neurorehabilitation; Cortical reorganization; Neuroplasticity
Summary This paper is a review conducted to provide an overview of accumulated evidence on contemporary rehabilitation methods for stroke survivors. Loss of functional movement is a common consequence of stroke for which a wide range of interventions has been developed. Traditional therapeutic approaches have shown limited results for motor deficits as well as lack evidence for their effectiveness. Stroke rehabilitation is now based on the evidence of neuroplasticity, which is responsible for recovery following stroke. The neuroplastic changes in the structure and function of relevant brain areas are induced primarily by specific rehabilitation methods. The therapeutic method which induces neuroplastic changes, leads to greater motor and functional recovery than traditional methods. Further, the recovery is permanent in nature. During the last decade various novel stroke rehabilitative methods for motor recovery have been developed. This review focuses on the methods that have evidence of associated cortical level reorganization, namely task-specific training, constraint-induced movement therapy, robotic training, mental imaging, and virtual training. All of these methods utilize principles of motor learning. The findings from this review demonstrated convincing evidence both at the neural and functional level in response to such therapies. The main aim of the review was to determine the evidence for these methods and their application into clinical practice. ª 2011 Elsevier Ltd. All rights reserved.
* Corresponding author. Department of Neurology, CSM Medical University (KGMU), Lucknow, UP 226003, India. E-mail address:
[email protected] (K.N. Arya). 1360-8592/$ - see front matter ª 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.jbmt.2011.01.023
Introduction Stroke is the second leading cause of death and one of the leading causes of adult disability in the world today (Gresham et al., 1997). Traditionally, stroke rehabilitation comprised a number of neurophysiological approaches developed by Bobath, Rood, Kabat, Brunstrom and Carr & Shepherd (Paci, 2003; Chan et al., 2006). It also includes compensation of lost movement through the use of the unaffected arm or leg (Dobkin, 2004). Some of the neurophysiological approaches, such as Bobath, are based on theories of motor control and motor learning. Due to frequent changes and development of these theories such approaches need to be redefined. For example, traditionally Bobath approach was based on reflexive and hierarchical theory of motor control while now it is based on the theory of distributed control of the central nervous system (Shumway-Cook and Woollacott, 2006). Though stroke is a leading cause of disability, there is no accepted rehabilitation method (Jette et al., 2005). Most of the traditional approaches used for enhancing recovery in post stroke patients, do not have strong evidence (Paci, 2003; Hafsteinsdo ´ttir et al., 2005). Therapists use eclectic approaches to intervention rather than one specific intervention technique (Schaechter, 2004). During the past two decades, compelling evidence in neuroscience has resulted in knowledge that the brain can change or reorganize itself in response to sensory input, experience and learning (Chan et al., 2006). This ability of the brain and other parts of the central nervous system to reorganize itself is referred to as Neuroplasticity (Rossini et al., 2003) and exclusively of cortex as Cortical plasticity (Jain, 2002). Neuroplasticity occurs in both a healthy and injured brain (Hubbard et al., 2009). For example, the structural brain changes have been reported among the healthy cab drivers due to a purposive activity, such as the frequent use of a street and traffic pattern (Gauthier et al., 2008). Neuroimaging findings in animals (Markus et al., 2005) and humans (Richards et al., 2008b) support the basis of reorganization in many parts of the brain both in response to recovery and goaldirected motor therapy (Turkstra et al., 2003; Dobkin, 2004; Nudo, 2007). Richards et al. (2008b) conducted a meta-analysis of 13 studies to examine changes associated with neural plasticity in post stroke patients following movement based therapy. The changes were examined either by transcranial magnetic stimulation, functional magnetic resonance imaging (fMRI), or positron emission tomography (PET). Results indicated that neural changes in the sensorimotor cortex of the lesioned hemisphere accompany the motor gains in the paretic upper extremity. The traditional neurorehabilitation approaches for post stroke patients focus on motor and functional recovery (Chan et al., 2006). Motor recovery refers to an ability of an individual to carry out movements under voluntary control in the same manner as before the stroke (Levin et al., 2009), while functional recovery refers to improvement in the ability of the individual to perform activities such as selfcare and mobility independently (Davis, 2006). Post stroke, recovery also occurs at brain level (neurological recovery), which is generally associated with the structural and
529 functional reorganization of brain. Both motor and functional recoveries are influenced by neurological recovery. However, functional recovery may also occur independently of neurological recovery (Teasell et al., 2005). Research in neuroplasticity has led to the development of new movement therapy methods inducing neural as well as motor recovery. Many movement therapy protocols such as taskspecific training, constraint-induced movement therapy (CIMT), and mental imagery have preliminary but convincing evidence for their impact on such reorganization and associated motor and functional recovery (Wolf et al., 2006; Page et al., 2007, 2009; Gauthier et al., 2008; Richards et al., 2008a, b). Thus, neural reorganization after stroke is thought to be an important mechanism to facilitate motor recovery (Jones et al., 2009). Furthermore, most of these protocols utilize the principles of motor learning (Krakauer, 2006). Motor learning refers to the permanent changes in behavior because of practice or experience (Schmidt, 2005). The protocols target deficits in the neuromuscular system and use practice or an experience for a specific goal or task to produce skilled motor action (Jette et al., 2005). For example, doing repetitive practice for reaching a glass of water to improve the elbow extension. Learning such motor skills cause structural and functional changes in the motor cortex and cerebellum. Further, the changes are indicative of motor recovery, which is permanent in nature (Kleim and Jones, 2008). Such changes are not found with simple exercises, for example, performing elbow flexioneextension without any goal (Nudo et al., 2001; Maldonado et al., 2008). Hence, the concept of neuroplasticity is important in stroke rehabilitation. The validity of therapy induced neuroplasticity has also been strongly supported by activation of specific brain areas in many fMRI studies. These studies have shown the diversity and complexity of reorganization patterns (Richards et al., 2008b). The process of reorganization is dynamic and also depends upon various factors such as the time period elapsed between stroke and therapy, and the intensity and type of therapy given (Nudo et al., 2001; Nudo, 2003). The aim of the review was to identify the evidence for neuroplasticity as well as associated motor and functional recovery in response to various movement based therapeutic methods and to determine the application of these methods in stroke rehabilitation.
Search strategy Though the review was not systematic, the following search strategy was used to review current evidence from the literature: Search engines: Pubmed, the Cochrane Library of systematic reviews Keywords used Stroke and Rehabilitation Motor learning Motor control Motor recovery
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K.N. Arya et al. Neuroplasticity Cortical organization
Inclusion criteria Types of participant: stroke survivors in the acute phase, the rehabilitation phase and the chronic phase. Type of event: ischemic and hemorrhagic stroke Types of outcome measure: outcomes of interventions focused on neurological recovery (brain reorganization),/motor recovery (motor performance)/functional recovery (activities of daily living). Research design: meta-analysis, systematic reviews, reviews and randomized controlled trials which incorporated methods to investigate the neural reorganization. Time of publication: articles published in English between January 2000 and December 2009.
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Motor learning Most of the evolving movement therapies which induce cortical reorganization are based on the principles of motor learning. Motor learning leads to sprouting of dendrites, formation of new synapses, alteration in existing synapses and production of neurochemicals (Mulder and Hochstenbach, 2001). These changes are greater if the practice method is meaningful, repetitive and intensive in nature (Daly and Ruff, 2007). Further, such practice method leads to long-term retention and generalization of the learned motor behavior. For example, if an individual tries to reach for a glass filled with water to attempt to drink (meaningful), 50 times (repetitive), thrice daily for four weeks (intensive). Motor improvement then achieved such as an increased range of elbow extension would be permanent in nature and could be applied in other task performances (Kleim and Jones, 2008; Hubbard et al., 2009). Thus, stroke rehabilitation methods should consist of intensive and repetitive practice of meaningful tasks. Recovery achieved by motor learning may be divided into true or compensatory motor recovery. True motor recovery happens when undamaged or alternative pathways transport commands to the same muscles that were used before the injury (Krakauer, 2006). A proposed mechanism for this is through redundancy of motor cortical areas with unmasking of pre-existing corticocortical connections (Teasell et al., 2005). Compensation is the use of alternative muscles to accomplish the task goal (Krakauer, 2006). Motor learning is required for both the types of recovery (Krakauer, 2006). However, the goal of all the emerging movement based therapeutic methods for post stroke rehabilitation is true motor recovery. Most of these methods are based on motor learning and have meaningful, repetitive and intensive practice as a key element for training (Krakauer, 2006; Kleim and Jones, 2008; Richards et al., 2008a).
Task-specific training Task-specific training is a term that has evolved from the movement science and motor skill learning literature (Schmidt, 2005). Other terms interchangeably used are ‘repetitive task practice’, ‘repetitive functional task practice’, and ‘task-oriented therapy’ (French et al., 2007;
Hubbard et al., 2009). Task-specific training emphasizes the practice and repetition of skilled motor performance to improve individual’s functional abilities (Bayona et al., 2005). Task-specific training may restore function by using spared parts of the brain, which are generally adjacent to the lesion and/or recruiting supplementary parts of the brain (Nudo et al., 2000). There is increasing evidence of neural plastic changes associated with such training (Jang et al., 2003; Luft et al., 2004; Richards et al., 2008a, b). Task-specific training, in comparison to traditional stroke rehabilitation, induces long-lasting motor learning and associated cortical reorganization specific to the corresponding areas being used (Bayona et al., 2005; Dobkin, 2005; Schmidt, 2005; Gauthier et al., 2008; Harvey, 2009). In response to task-specific training, Jang et al. (2003) found cortical activation changes with the upper extremity functional recovery. fMRI changes showed decrease activation in the unaffected and an increase in the affected primary sensorimotor cortex. Similarly, Luft et al. (2004), observed increased activation in the contralesional cerebrum and ipsilesional cerebellum (p Z 0.009), in response to repetitive bilateral arm training as compared to control therapy. Furthermore, repetitive task-specific training has been found to achieve better functional gains when compared to non-repetitive training (Langhammer and Stanghelle, 2000; Salbach et al., 2004; Michaelsen et al., 2006; Page et al., 2007). It has also been found to be effective in gait retraining, sit-to-stand retraining and motor training of the upper limb (Hubbard et al., 2009). Langhammer and Stanghelle (2000), in an RCT of 61 stroke patients, compared the motor relearning programme (MRP), consisting of physiotherapy with task-oriented strategies, and the Bobath techniques, which involve physiotherapy with facilitation/inhibition strategies. Although statistically insignificant, patients who were treated with the taskoriented strategies were more likely to improve on tests of motor function but not on more general functional outcome testing. A double-blind randomized control trial was also conducted to determine whether task-specific training with trunk-restraint (TR) produces greater improvements in arm impairment and function than training without TR in 30 patients with chronic hemiparesis (Michaelsen et al., 2006). TR group exhibited greater improvements in impairment and function as compared to control (p < 0.05). There was increased active elbow joint range in TR group while increased compensatory movement in the control group. Salbach et al. (2004) evaluated the efficacy of a task-orientated intervention in enhancing competence in walking in 91 chronic stroke patients. Significant between-group effects of 0.21 m/s (95% CI: 0.12, 0.30) and of 0.11 m/s (95% CI: 0.03, 0.19) in maximum and comfortable walking speed, respectively, were observed. People with a mild, moderate or severe walking deficit at baseline improved an average of 36, 55 and 18 m, respectively; in 6-min walk test performance following the experimental intervention. In a systematic review, French et al. (2007) summarized the evidence of task-specific training in post stroke patients. Overall, it was found that some form of task-specific training resulted in improvement in global motor function, and in both arm and lower limb function, although the evidence for upper limb interventions was less clear because of insufficient good-quality evidence.
In addition to task specificity, environment for the training is important in motor learning and associated cortical reorganization (Do ¨bro ¨ssy and Dunnet, 2001). Environmental factors play an important role in inducing the optimum response from the individual during task-specific training (Davis, 2006). The therapeutic environment which provides a greater opportunity for activity and interaction is termed as an enriched environment (Do ¨bro ¨ssy and Dunnett, 2001). The enriched environment provides individuals with clear understanding of what is being expected of them during task-specific practice and improves their performance (Davis, 2006). For instance, animals exposed to complex housing environments post injury typically have improved the functional outcomes compared to animals in standard housing (Will et al., 2004). Similarly, an individual would stand for a longer period of time if he is brushing his teeth in front of a washbasin as compared to someone who simply stands in the middle of a therapy room. Thus, stroke rehabilitation programs should include repetitive task-specific movement training in an enriched environment in order to promote cortical reorganization, motor and functional recovery.
Constraint-induced movement therapy (CIMT) CIMT has received greatest attention among all the emerging movement based therapeutic methods in the last decade. It has shown significant improvement of the paretic upper limb function in chronic stroke patients (Schaechter, 2004). It is one of the most studied motor rehabilitation protocols for post stroke patients. CIMT combines various interventional principles aimed at enhancing the use of the paretic upper extremity after stroke. CIMT was developed originally to ameliorate the phenomenon of “learned non-use” in which individuals with stroke form the habit of not using their paretic upper extremity despite the ability to use it in some functional activities. It mainly consists of constraining the less affected arm by wearing a sling or mitt during waking hours and practicing tasks with the more affected one (Taub et al., 2006). In addition to repetitive practice of a task, it also includes successive approximation. The successive approximation is a process of either increasing the successful numbers of repetitions or reducing the time to complete the task successfully with one effort (Wolf, 2007). fMRI studies on the adult stroke patients have demonstrated functional changes at the physiological level of brain, including changes in cortical excitability, metabolic rate, and blood flow after CIMT (Schaechter et al., 2002). Although important, these alterations in the brain physiology fluctuate rapidly over time and give findings, which may not be reliable. Structural neuroplasticity (i.e., increases or decreases in the amount of gray matter) has also been studied. Post CIMT profuse increases in the gray matter has been found in the sensory and motor cortical areas, both contralateral and ipsilateral to the affected arm. The structural changes were accompanied by large improvements in spontaneous realworld arm function (Gauthier et al., 2008). Hence, CIMT has evidence for the physiological and structural brain changes as well as improvement in the affected upper limb function in post stroke patients. Various trials have been conducted to examine the effectiveness of CIMT in improving motor and functional
531 recovery in post stroke patients (Hakkennes and Keating, 2005; Taub et al., 2006; Wolf et al., 2006; Lin et al., 2009). Taub et al. (2006), in their trial with 41 subjects, found large to very large improvements in the functional use of the more affected arm in the daily lives of the subjects (p < 0.0001). The changes persisted over two years. Wolf et al. (2006) conducted similar but a larger multi-site randomized clinical trial, the extremity constraint-induced therapy evaluation (EXCITE). Two hundred and twenty-two patients who had a stroke within the previous 3e9 months were recruited. CIMT produced statistically significant and clinically relevant improvements in arm motor function that persisted for at least one year. However, control group either received usual care or no treatment. The control treatment was also not matched for dose with the experimental one. These could be important confounders for the findings. Although early therapy is an important factor to induce neuroplasticity (Kleim and Jones, 2008) and CIMT is feasible in acute stage (Dromerick et al., 2000), most of the studies were conducted on chronic stroke patients. Only one CIMT trial for acute stroke patients has been found (Dromerick et al., 2009). They conducted very early constraint-induced movement during stroke rehabilitation (VECTORS), a phase II trial of CIMT with 52 acute stroke patients (within 28 days of admission). The VECTORS study did not support the hypothesis that CIMT therapy was superior to traditional therapy in acute stage of stroke. This could be due to minimal or no learned non-use during the acute phase. However, CIMT was found to be effective in a trial of small sample (n Z 14) of sub-acute stroke (mean Z 4.4-month post stroke) (Page et al., 2002). Stroke affects various health domains such as participation in the community which represents a societal perspective of functioning, for example, work and employment (Davis, 2006). Though there is evidence of CIMT intervention at various levels, participation of the client at the community level has not been studied yet. Further, almost all studies have reported its efficacy for subjects having 20 wrist extension and 10 finger extension (Hakkennes and Keating, 2005; Wolf et al., 2006; Lin et al., 2009). However, in stroke, many people (75%) do not reach this level of the hand recovery and, therefore, may not benefit from CIMT (Sawner and LaVigne, 1992; Wolf, 2007). Lin et al. (2009) studied the effect of CIMT with a little different inclusion criteria and objective. In the study, the inclusion criteria were placing the hand behind the back, moving the arm forward to a horizontal position, or performing pronation and supination with the elbow flexed at 90 (Brunnstrom stage IV), instead of specific degree of wrist and finger extension. However, again these criteria did not cover the larger proportion (>50%) of severely disabled stroke population (Sawner and LaVigne, 1992). Unlike other studies, Lin et al. used comprehensive outcome measures of motor ability, perceived functional use of the affected limb, basic and extended performance of activities of daily living, and quality of life. As compared to control group, the CIMT group exhibited significantly better performance in motor function (p < 0.06), level of functional independence (p < 0.001), extended activities during daily life (p < 0.04), and health-related quality of life after treatment (p < 0.009). In a systematic review of 14 RCTs, Hakkennes and Keating (2005) concluded that CIMT may improve upper
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532 limb function following stroke for some patients when compared to alternative or no treatment. Well-designed and adequately powered trials are further required to evaluate the efficacy of different CIMT protocols on the different types of stroke patients and to assess the impact on quality of life, cost and patient/care giver satisfaction. Given the available evidence, CIMT may be considered as one of the important movement therapies for the chronic stroke patients.
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Mental imagery/practice Mental imagery is a cognitive process of creating any experience (auditory, visual, tactile, and kinesthetic) in the mind without its actual presence (Dickstein and Deutsch, 2007). Specifically, motor imagery is an act of producing an internal representation of a movement without generating any motor output (Jackson et al., 2001; Braun et al., 2006). It is the imagination of movement/s of a body part/s, for example, imagination of the elbow flexion. Mental practice is the voluntary rehearsal of an imaginary scene, for example, imagination of eating an ice-cream using the impaired upper extremity. However, the term mental practice and motor imagery practice are used interchangeably (Dickstein et al., 2004). The concept has been taken from sport psychology, where this method is used to maintain the performance level of athletes during recovery from injury. The rationale behind this technique is the activation of same brain areas and pathways even in the absence of real movement performance. Brain mapping techniques have shown the activation of the motor cortex and other associated areas during imagery as well as during the execution of the movement (de Vries and Mulder, 2007). This capability of the cerebral cortex and related network can be exploited for stroke patients. Mental imagery can be used during the phase of recovery when volitional movements are either impossible or being performed synergistically. Studies have reported fMRI evidence of cortical reorganization induced by mental imagery. Mental practice led to increased activation of the cerebellar, premotor, primary motor cortex and striatal sensorimotor network. The changes correlated with motor and functional recovery (Lacourse et al., 2004; Page et al., 2009). It has also been suggested that mental imagery/practice alone is not enough to induce recovery. Whenever possible, it should be complemented by another evidence based motor rehabilitation approaches such as CIMT and repetitive task practice (Butler and Page, 2006; Sharma et al., 2006; Zimmermann-Schlatter et al., 2008; Page et al., 2009). In an RCT of 32 chronic stroke patients (mean Z 3.6 years) with moderate motor deficits, experimental group received 30-min mental practice (MP) sessions and physical practice while the control group received the relaxation and physical practice. Subjects receiving MP showed significant reductions in affected arm impairment and significant increases in daily arm function (both at the p < 0.0001) (Page et al., 2007). Both short term and long-term functional benefits of mental imagery on relearning and performance of daily arm function in post stroke patients have been reported in two randomized controlled trials (Liu et al., 2004; Page et al., 2007).
K.N. Arya et al. Although mental imagery was found to be effective in improving gait in post stroke clients, no randomized controlled trial has been conducted (Dickstein et al., 2004). Hence, whilst there is adequate functional, as well as neuro-imaging evidence for use of mental imaging for upper extremity rehabilitation of post stroke patients; this does not exist for the lower limb. Further, the generation of motor images is a complex cognitive skill. The skill level varies from person to person. The ability to generate strong motor images is considered to be an important determinant of the effectiveness of mental imagery. An individual may use alternative cognitive strategies that, if not screened for, could confound investigations and produce conflicting results. Few questionnaires have been developed to assess the imagery ability and accuracy (Sharma et al., 2006). Despite this, the available evidence suggests the value of mental imagery for post stroke patients. Moreover, the method is found to be highly cost effective and safe for the rehabilitation of post stroke clients. (Gaggioli et al., 2004; Page et al., 2007).
Body weight support treadmill training Ambulation is one of the most affected activities in post stroke survivors (Wevers et al., 2009). Stroke rehabilitation usually focuses on gait and gait related activities to improve mobility, although most individuals continue to have some residual disability in ambulation (Laufer et al., 2001). Initially developed for people with spinal cord injuries (Hicks and Ginis, 2008), body weight support treadmill training (BWSTT) is now also becoming a promising approach for gait rehabilitation in stroke. In this approach, body weight support, provided by a harness, reduces the biomechanical and equilibrium constraints for walking and a treadmill facilitates normal walking pattern (Laufer et al., 2001). Consequently, the individual can practice repetitive training without abnormal deviations of trunk and lower extremity. Furthermore, the training may activate spinal centers, referred to as Central pattern generators (CPGs) (Drew et al., 2008). CPGs are networks of nerve cells producing specific, rhythmic movements such as walking, without conscious effort and without the aid of peripheral afferent feedback (MacKay-Lyons, 2002). Walking is based on a “pacemaker” activity of the CPGs. CPGs generate stepping patterns consist of synergistic joint movement (Nielsen, 2003; Drew et al., 2008). For example, alternate movement of lower limbs during walking; consists of hip flexion and knee extension of one limb while hip extension and knee extension of the other limb. However, the evidence of pattern generation in humans is limited and indirect, based either on animal studies or studies of a single human subject with spinal cord injury (MacKay-Lyons, 2002). In post stroke patients, there is often hemiparesis, with abnormal control of one lower limb producing an asymmetrical gait pattern. In a hemiparetic patient, BWSTT creates a partial unloading of the lower extremities. Reduced load on the paretic lower extremity results in a straighter trunk and knee alignment during the weight bearing phase (Laufer et al., 2001; Lindquist et al., 2007; Lam et al., 2009). Further, due to movement of treadmill, there is a decrease in double-limb support time (stance
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97 sub-acute (within 6 weeks of stroke onset) post stroke subjects. After treatment (BWSTT and over ground training), all patients were able to walk. Both groups (experimental group; n Z 52 and control group; n Z 45) showed improvement in all of the outcome measures (Motricity Index, trunk control test, Barthel index, functional ambulation categories, 10-m and 6-min walk tests, and walking handicap scale) at the end of the treatment and at the follow-up. However, no difference was seen between the groups after the treatment and at the follow-up. Thus, more research is needed to validate the present evidence for effectiveness of BWSTT in chronic and subacute stroke patients (Laufer et al., 2001; Moseley et al., 2005; Franceschini et al., 2009). Studies are also warranted in subjects with the acute stroke (McCain and Smith, 2007). However, with the available evidence, BWSTT may be considered as a standard gait training protocol for the chronic stroke survivors with the gait dysfunction along with the usual movement therapy methods.
Robotic-assisted training Robotic-assisted stroke rehabilitation has been developed during the last two decades (Prange et al., 2006). Robots can provide intensive, reproducible, and task-specific movement therapy. They are also able to address a wide range of treatment needs via active, assistive, or resisted exercise (Fasoli et al., 2004). Robotic training involves two interacting processes: the patient trying to move and the robot assisting or resisting the movements during repetitive practice. It can: provide movement therapy for long time periods, in a consistent & precise manner, with reduced fatigue be programmed to perform in different modes of assistance for the client such as passive (full assistance), active assistive (partial assistance) and active (no assistance) with a single click measure & record a range of behaviors in parallel with the therapeutic applications (Takahashi et al., 2008). be coupled with a virtual environment technology (discussed later) to increase motivation of the client (Mirelman et al., 2009). Further, robotic devices have programmable forceproducing ability, which can replicate some features of a therapist’s manual assistance, allowing patients to semiautonomously practice movement (Kahn et al., 2006). However, some of its features such as mechanical manipulation cannot be replicated by the therapists due to their limited speed, sensation, strength, and repeatability of the neuromuscular system (Lum et al., 2002; Kahn et al., 2006). There are various commercial types of Robotic system. Most of the available types are mainly for the upper limb training such as the Assisted rehabilitation and measurement (ARM) guide, Mirror image movement enabler (MIME), MIT Manus, Hand wrist assistive rehabilitation device (HWARD) while few like Lokomat, Robotic-assisted gait training (RAGT) device are also available for the gait training (Kahn et al., 2006; Prange et al., 2006; Richards et al., 2008a; Takahashi et al., 2008; Marchal-Crespo and Reinkensmeyer, 2009).
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phase), increase in single-limb support time (swing phase) and increase in walking speed (Laufer et al., 2001; Enzinger et al., 2009). This provides an environment for specific and repetitive training for walking (Lindquist et al., 2007). This type of specific and repetitive learning is hypothesized to induce neuroplasticity and associated motor recovery (Schmidt, 2005). Though gait control has more of a subcortical contribution through CPGs (MacKay-Lyons, 2002), BWSTT training is associated with bilateral cortical activation changes in chronic stroke. It was found to increase brain activity in the bilateral primary sensorimotor cortices, the cingulate motor areas, and the caudate nuclei bilaterally and in the thalamus of the affected hemisphere (Enzinger et al., 2009). This may be due to the requirement of motor control in response to environmental demand, position sense and balance during walking, which are being controlled by brain (Nielsen, 2003). Animal studies have also shown that motor cortex modifies the synergies produced by CPGs during complex demand of locomotion (Drew et al., 2008). BWSTT can be used to manage post stroke gait dysfunction by normal gait programming generated by this novel approach. (Laufer et al., 2001; Gorman, 2007; Lam et al., 2009). Randomized trials of BWSTT have shown improvements in gait parameters such as stride length and singlelimb support in the chronic stroke patients (Laufer et al., 2001; Werner et al., 2002). These studies suggested that the treadmill training may be more effective than the conventional gait training for improving gait parameters such as functional ambulation, stride length, percentage of the paretic single stance period, and muscular activity. Enzinger et al. (2009) investigated walking ability after 4 weeks of BWSTT in 18 chronic patients (mean age, 59.9 13.5 years) with mild to moderate paresis and functional ambulation category range, 3e5. Walking endurance improved after the training (2-min timed walking distance: from 105.1 38.1 m to 121.5 39.0; p < 0.0001). BWSTT has also been shown to be effective in conjunction with functional electrical stimulation, a method of augmenting insufficient muscle force by predetermined frequencies and amplitudes of electrical currents (Bogey and Hornby, 2007; Lindquist et al., 2007). Although independent studies have shown significant motor and functional improvement, in a Cochrane review it was found that there was not enough evidence to determine the effects of the treadmill training (Moseley et al., 2005). In their multicentre randomized controlled trial, Nilsson et al. (2001) studied the effect of BWSTT and walking training on the ground at an early stage of rehabilitation in 73 post stroke patients. However, there was no statistically significant difference found between the groups at discharge or at the 10-month follow-up with regard to the functional independence measure, walking velocity, functional ambulation category, Fugl-Meyer assessment, and Berg’s balance scale. Similarly, Suputtitada et al. (2004) also did not find any statistically significant difference between the BWSTT and control group, after a 4-week training period with regard to floor walking velocities and functional balance. It was an observer blinded, randomized controlled trial with 48 chronic stroke patients. Franceschini et al. (2009) also conducted a single-blind, randomized, controlled trial with a 6-month follow-up with
533
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534 Cortical reorganization and associated motor recovery of chronic stroke patients can be enhanced by a robot-aided therapy (Prange et al., 2006; Takahashi et al., 2008). fMRI changes indicate the potential benefit of robotic training in inducing cortical plasticity in the chronic stroke patients (Mintzopoulos et al., 2008). In response to the HWARD robotic-assisted training, fMRI changes showed the significant increase in the sensorimotor cortex activation across the period of therapy (p < 0.05) (Takahashi et al., 2008). Takahashi et al. (2008) also determined the effect of the HWARD on motor function. Post treatment, significant gains were found in the action research arm test and arm motor Fugl-Meyer score (p < 0.0005 & 0.0001, respectively). Robotic-assisted therapy is useful in facilitating motor control (muscle activation patterns, selectivity, and speed of movement) and has long-term effects of several months to several years (Prange et al., 2006). However, no consistent effect on the improvement in functional abilities has been reported (Prange et al., 2006). Though in its infancy, preliminary evidence of the robotic-assisted training shows no adverse effect (Prange et al., 2006). However, it is not clear whether this therapy improves outcome to a greater extent than the conventional therapy (Richards et al., 2008a). Further, considering the high cost value of the robotic devices, its use in a typical clinical practice is limited (Marchal-Crespo and Reinkensmeyer, 2009). More studies are needed to examine the substantial benefits from this hi-technology based therapy program.
Virtual training Virtual reality (VR) is another new promising computer assisted technology to promote motor recovery in the stroke patients (You et al., 2005). It is an interactive intervention approach, which involves real-time simulation of an environment, scenario or activity that allows user interaction. Multiple sensory channels are also used to provide threedimensional and sensorial feedbacks (Crosbie et al., 2007). Using VR, intensity of practice and sensory feedback (visual, auditory and sometimes touch) can be systematically manipulated to provide the most appropriate, individualized real-life motor training (Merians et al., 2002). For example, a virtual environment of outdoor game in which auditory feedback in the form of clapping is provided on every correct motor performance. VR training programs are designed to be either task specific or meaningful to the participant, which are important in maximizing motor learning (Henderson et al., 2007). There are various types of Virtual reality devices/systems available in neurorehabilitation practice (Adamovich et al., 2009). In general, there are two types of VR, immersive and non-immersive. Fully immersive VR can use large screen projection where the environment is projected on a concave surface to create the sense of immersion. In a non-immersive VR, users interact to different degrees with the environment displayed on a computer screen, with or without interface devices such as a computer mouse (Henderson et al., 2007). IREX VR system is an immersive type of VR, enables a patient to move freely in the real world while allowing manipulation of the virtual objects and navigation in the 3-dimension virtual world. For example, snowboard
K.N. Arya et al. games with virtual environments to facilitate the lower limb range of motion, balance, mobility, stepping, and ambulation skills (You et al., 2005). Nintendo Wii introduced a new style of non-immersive VR by using a wireless controller that interacts with the player through a motion detection system. The controllers use embedded acceleration sensors that can respond to changes in direction, speed, and acceleration to enable participant’s wrist, arm, and hand movements to interact with the games (http://www.nintendo.com/wii). VR has been found to induce cortical reorganization and improve associated motor function in the chronic hemiparesis (Piron et al., 2003; You et al., 2005; Jang et al., 2005; Adamovich et al., 2009; Kim et al., 2009). In an RCT, fMRI changes were found to be evident in the corresponding sensorimotor cortex of the chronic stroke patients after locomotor VR training by IREX VR system (You et al., 2005). Also, post VR training, the altered activations in the bilateral primary sensorimotor cortices (SM1s) and contralesional premotor cortex disappeared and significant activation of the ipsilesional SM1 was found (p < 0.05) (Jang et al., 2005). Piron et al. (2003) conducted an RCT with 24 sub-acute stroke patients to study the effect of non-immersive VR system on arm recovery. Though the difference between the groups was not statistically significant, the VR group showed 20.2% and 12.4% improvements in the Fugl-Meyer assessment and functional independence measure scale mean scores respectively. The control group showed significant but smaller score improvements: 11.3% and 9.1%, respectively. However, the evidence on the effectiveness of using VR for upper extremity recovery is limited. Very few goodquality RCTs for the upper extremity have been conducted (Jang et al., 2005; Henderson et al., 2007; Kim et al., 2009). Kim et al. (2009) examined the effect of GAITRite VR system on balance and gait function in patients with 24 chronic stroke patients. The experimental group improved on the Berg balance scale scores, gait velocity, cadence, step time, step length, and stride length (p < 0.05), compared with the controls. Furthermore, VR training has been combined with the robotic therapy and has demonstrated improvement in motor function, balance and ambulation (Mirelman et al., 2009). The combination of the robotic and virtual Reality devices allows manipulation of the duration, intensity, and feedback of training programs. These characteristics of training were reported to be closely related to recovery, reorganization, and cortical plasticity after stroke (Mirelman et al., 2009). VR is a novel and costly approach; further trials are needed to justify its effectiveness. Technological research is required to develop VR programs, specifically for the functional tasks or activities of relevance to the patients. Such programs are assumed to induce better cortical reorganization.
Conclusion For many years, the human brain was characterized as hard wired, which led to the development of therapeutic methods for compensation only. Recent evidence, both in neuroscience and neurorehabilitation, has shown that the human brain is neuroplastic. This feature of the brain contributes to recovery following stroke and can be exploited through
specific treatment methods based on movements. Such therapeutic methods for improving motor and functional recovery should be applied in neurorehabilitation practice, but these innovative approaches should only be applied with consideration of the evidence, cost effectiveness and participation of the client. Irrespective of sophistication in technology, treatment methods driving recovery at motor as well as neural level should be selected. Research must be continued in the direction of movement therapy induced cortical reorganization and related motor recovery for rehabilitation of post stroke patients.
References Adamovich, S.V., Fluet, G.G., Tunic, E., Merians, A.S., 2009. Sensorimotor training in virtual reality: a review. NeuroRehabilitation 25 (1), 29e44. Bayona, N.A., Bitensky, J., Salter, K., Teasell, R., 2005. The role of task-specific training in rehabilitation therapies. Top Stroke Rehabil. 12 (3), 58e65. Bogey, R., Hornby, G.T., 2007. Gait training strategies utilized in poststroke rehabilitation: are we really making a difference? Top Stroke Rehabil. 14 (6), 1e8. Braun, S.M., Beurskens, A.J., Borm, P.J., Schack, T., Wade, D.T., 2006. The effects of mental practice in stroke rehabilitation: a systematic review. Arch. Phys. Med. Rehabil. 87 (6), 842e852. Butler, A.J., Page, S.J., 2006. Mental practice with motor imagery: evidence for motor recovery and cortical reorganization after stroke. Arch. Phys. Med. Rehabil. 87 (12 Suppl. 2), S2eS11. Chan, D.Y., Chan, C.C., Au, D.K., 2006. Motor relearning programme for stroke patients: a randomized controlled trial. Clin. Rehabil. 20 (3), 191e200. Crosbie, J.H., Lennon, S., Basford, J.R., McDonough, S.M., 2007. Virtual reality in stroke rehabilitation: still more virtual than real. Disabil. Rehabil. 29 (14), 1139e1152. Daly, J.J., Ruff, R.L., 2007. Construction of efficacious gait and upper limb functional interventions based on brain plasticity evidence and model-based measures for stroke patients. Scientific World J. 20 (7), 2031e2045. Davis, J.Z., 2006. Task selection and enriched environments: a functional upper extremity training program for stroke survivors. Top Stroke Rehabil. 13 (3), 1e11. de Vries, S., Mulder, T., 2007. Motor imagery and stroke rehabilitation: a critical discussion. J. Rehabil. Med. 39 (1), 5e13. Dickstein, R., Deutsch, J.E., 2007. Motor imagery in physical therapist practice. Phys. Ther. 87 (7), 942e953. Dickstein, R., Dunsky, A., Marcovitz, E., 2004. Motor imagery for gait rehabilitation in post-stroke hemiparesis. Phys. Ther. 84 (12), 1167e1177. Dobkin, B.H., 2004. Strategies for stroke rehabilitation. Lancet Neurol. 3 (9), 528e536. Dobkin, B.H., 2005. Clinical practice. Rehabilitation after stroke. N. Engl. J. Med. 352 (16), 1677e1684. Do ¨bro ¨ssy, M.D., Dunnett, S.B., 2001. The influence of environment and experience on neural graft. Neuroscience 2, 871e879. Drew, T., Kalaska, J., Krouchev, N., 2008. Muscle synergies during locomotion in the cat: a model for motor cortex control. J. Physiol. 586 (5), 1239e1245. Dromerick, A.W., Edwards, D.F., Hahn, M., 2000. Does the application of constraint-induced movement therapy during acute rehabilitation reduce arm impairment after ischemic stroke? Stroke 31 (12), 2984e2988. Dromerick, A.W., Lang, C.E., Birkenmeier, R.L., et al., 2009. Very Early Constraint-Induced Movement during Stroke Rehabilitation (VECTORS): a single-center RCT. Neurology 73 (3), 195e201.
535 Enzinger, C., Dawes, H., Johansen-Berg, H., et al., 2009. Brain activity changes associated with treadmill training after stroke. Stroke 40 (7), 2460e2467. Fasoli, S.E., Krebs, H.I., Hogan, N., 2004. Robotic technology and stroke rehabilitation: translating research into practice. Top. Stroke Rehabil. 11 (4), 11e19. Franceschini, M., Carda, S., Agosti, M., et al., 2009. Walking after stroke: what does treadmill training with body weight support add to overground gait training in patients early after stroke?: a single-blind, randomized, controlled trial. Stroke 40 (9), 3079e3085. French, B., Thomas, L.H., Leathley, M.J., et al., 2007. Repetitive task training for improving functional ability after stroke. Cochrane Database Syst. Rev. 4, CD006073. Gaggioli, A., Morganti, F., Walker, R., et al., 2004. Training with computer-supported motor imagery in post-stroke rehabilitation. Cyberpsychol Behav. 7 (3), 327e332. Gauthier, L.V., Taub, E., Perkins, C., Ortmann, M., Mark, V.W., Uswatte, G., 2008. Remodeling the brain: plastic structural brain changes produced by different motor therapies after stroke. Stroke 39 (5), 1520e1525. Gorman, S.L., 2007. Contemporary issues and theories of motor control, motor learning, neuroplasticity: assessment of movement & posture. In: Umphered, D.A. (Ed.), Neurological Rehabilitation, fifth ed. Mosby Elsevier, USA, pp. 56e70. Gresham, G.E., Alexander, D., Bishop, D.S., et al., 1997. American Heart Association Prevention Conference. IV. Prevention and Rehabilitation of Stroke. Rehabilitation. Stroke 28 (7), 1522e1526. Hafsteinsdo ´ttir, T.B., Algra, A., Kappelle, L.J., Grypdonck, M.H., Dutch NDT Study Group, 2005. Neurodevelopmental treatment after stroke: a comparative study. J. Neurol. Neurosurg. Psychiatr 76 (6), 788e792. Hakkennes, S., Keating, J.L., 2005. Constraint-induced movement therapy following stroke: a systematic review of randomised controlled trials. Aust. J. Physiother. 51 (4), 221e231. Harvey, R.L., 2009. Improving poststroke recovery: neuroplasticity and task oriented training. Curr. Treat. Options Cardiovasc. Med. 11 (3), 251e259. Henderson, A., Korner-Bitensky, N., Levin, M., 2007. Virtual reality in stroke rehabilitation: a systematic review of its effectiveness for upper limb motor recovery. Top Stroke Rehabil. 14 (2), 52e61. Hicks, A.L., Ginis, K.A., 2008. Treadmill training after spinal cord injury: it’s not just about the walking. J. Rehabil. Res. Dev. 45 (2), 241e248. http://www.nintendo.com/wii. accessed 10.12.09. Hubbard, I.J., Parsons, M.W., Neilson, C., Carey, L.M., 2009. Taskspecific training: evidence for and translation to clinical practice. Occup. Ther. Int. 16 (3e4), 175e189. Jackson, P.L., Lafleur, M.F., Malouin, F., Richards, C., Doyon, J., 2001. Potential role of mental practice using motor imagery in neurologic rehabilitation. Arch. Phys. Med. Rehabil. 82 (8), 1133e1141. Jain, N., 2002. Adult brain plasticity e what is revealed is exciting, what is hidden is critical. J. Biosci. 27 (5), 439e442. Jang, S.H., Kim, Y.H., Cho, S.H., Lee, J.H., Park, J.W., Kwon, Y.H., 2003. Cortical reorganization induced by task-oriented training in chronic hemiplegic stroke patients. Neuroreport 14 (1), 137e141. Jang, S.H., You, S.H., Hallett, M., et al., 2005. Cortical reorganization and associated functional motor recovery after virtual reality in patients with chronic stroke: an experimenter-blind preliminary study. Arch. Phys. Med. Rehabil. 86 (11), 2218e2223. Jette, D.U., Latham, N.K., Smout, R.J., Gassaway, J., Slavin, M.D., Horn, S.D., 2005. Physical therapy interventions for patients with stroke in inpatient rehabilitation facilities. Phys. Ther. 85 (3), 238e248. Jones, T.A., Allred, R.P., Adkins, D.L., Hsu, J.E., O’Bryant, A., Maldonado, M.A., 2009. Remodeling the brain with behavioral experience after stroke. Stroke 40 (3 Suppl.), S136eS138.
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536 Kahn, L.E., Lum, P.S., Rymer, W.Z., Reinkensmeyer, D.J., 2006. Robot-assisted movement training for the stroke-impaired arm: does it matter what the robot does? J. Rehabil. Res. Dev. 43 (5), 619e630. Kim, J.H., Jang, S.H., Kim, C.S., Jung, J.H., You, J.H., 2009. Use of virtual reality to enhance balance and ambulation in chronic stroke: a double-blind, randomized controlled study. Am. J. Phys. Med. Rehabil. 88 (9), 693e701. Kleim, J.A., Jones, T.A., 2008. Principles of experience-dependent neural plasticity: implications for rehabilitation after brain damage. J. Speech Lang. Hear Res. 51 (1), S225eS239. Krakauer, J.W., 2006. Motor learning: its relevance to stroke recovery and neurorehabilitation. Curr. Opin. Neurol. 19 (1), 84e90. Lacourse, M.G., Turner, J.A., Randolph-Orr, E., Schandler, S.L., Cohen, M.J., 2004. Cerebral and cerebellar sensorimotor plasticity following motor imagery-based mental practice of a sequential movement. J. Rehabil. Res. Dev. 41 (4), 505e524. Lam, T., Luttmann, K., Houldin, A., Chan, C., 2009. Treadmillbased locomotor training with leg weights to enhance functional ambulation in people with chronic stroke: a pilot study. J. Neurol. Phys. Ther. 33 (3), 129e135. Langhammer, B., Stanghelle, J.K., 2000. Bobath or motor relearning programme? A comparison of two different approaches of physiotherapy in stroke rehabilitation: a randomized controlled study. Clin. Rehabil. 14 (4), 361e369. Laufer, Y., Dickstein, R., Chefez, Y., Marcovitz, E., 2001. The effect of treadmill training on the ambulation of stroke survivors in the early stages of rehabilitation: a randomized study. J. Rehabil. Res. Dev. 38 (1), 69e78. Levin, M.F., Kleim, J.A., Wolf, S.L., 2009. What do motor "recovery" and "compensation" mean in patients following stroke? Neurorehabil. Neural Repair 23 (4), 313e319. Lin, K.C., Wu, C.Y., Liu, J.S., Chen, Y.T., Hsu, C.J., 2009. Constraint-induced therapy versus dose-matched control intervention to improve motor ability, basic/extended daily functions, and quality of life in stroke. Neurorehabil. Neural Repair 23 (2), 160e165. Lindquist, A.R., Prado, C.L., Barros, R.M., Mattioli, R., da Costa, P.H., Salvini, T.F., 2007. Gait training combining partial body-weight support, a treadmill, and functional electrical stimulation: effects on poststroke gait. Phys. Ther. 87 (9), 1144e1154. Liu, K.P., Chan, C.C., Lee, T.M., Hui-Chan, C.W., 2004. Mental imagery for promoting relearning for people after stroke: a randomized controlled trial. Arch. Phys. Med. Rehabil. 85 (9), 1403e1408. Luft, A.R., McCombe-Waller, S., Whitall, J., et al., 2004. Repetitive bilateral arm training and motor cortex activation in chronic stroke: a randomized controlled trial. JAMA 292 (15), 1853e1861. Lum, P., Reinkensmeyer, D., Mahoney, R., Rymer, W.Z., Burgar, C., 2002. Robotic devices for movement therapy after stroke: current status and challenges to clinical acceptance. Top. Stroke Rehabil. 8 (4), 40e53. MacKay-Lyons, M., 2002. Central pattern generation of locomotion: a review of the evidence. Phys. Ther. 82 (1), 69e83. Maldonado, M.A., Allred, R.P., Felthauser, E.L., Jones, T.A., 2008. Motor skill training, but not voluntary exercise, improves skilled reaching after unilateral ischemic lesions of the sensorimotor cortex in rats. Neurorehabil. Neural Repair 22 (3), 250e261. Marchal-Crespo, L., Reinkensmeyer, D.J., 2009. Review of control strategies for robotic movement training after neurologic injury. J. Neuroeng Rehabil. 16 (6), 20. Markus, T.M., Tsai, S.Y., Bollnow, M.R., et al., 2005. Recovery and brain reorganization after stroke in adult and aged rats. Ann. Neurol. 58 (6), 950e953. McCain, K.J., Smith, P.S., 2007. Locomotor treadmill training with body-weight support prior to over-ground gait: promoting
K.N. Arya et al. symmetrical gait in a subject with acute stroke. Top. Stroke Rehabil. 14 (5), 18e27. Merians, A.S., Jack, D., Boian, R., et al., 2002. Virtual realityaugmented rehabilitation for patients following stroke. Phys. Ther. 82 (9), 898e915. Michaelsen, S.M., Dannenbaum, R., Levin, M.F., 2006. Task-specific training with trunk restraint on arm recovery in stroke: randomized control trial. Stroke 37 (1), 186e192. Mintzopoulos, D., Khanicheh, A., Konstas, A.A., et al., 2008. Functional MRI of rehabilitation in chronic Stroke patients using novel MR-Compatible hand Robots. Open Neuroimag J. 27 (2), 94e101. Mirelman, A., Bonato, P., Deutsch, J.E., 2009. Effects of training with a robot-virtual reality system compared with a robot alone on the gait of individuals after stroke. Stroke 40 (1), 169e174. Moseley, A.M., Stark, A., Cameron, I.D., Pollock, A., 2005. Treadmill training and body weight support for walking after stroke. Cochrane Database Syst. Rev. 19 (4), CD002840. Mulder, T., Hochstenbach, J., 2001. Adaptability and flexibility of the human motor system: implications for neurological rehabilitation. Neural Plast. 8 (1e2), 131e140. Nielsen, J.B., 2003. How we walk: central control of muscle activity during human walking. Neuroscientist 9 (3), 195e204. Nilsson, L., Carlsson, J., Danielsson, A., Fugl-Meyer, A., Hellstro ¨m, K., Kristensen, L., Sjo ¨lund, B., Sunnerhagen, K.S., Grimby, G, 2001. Walking training of patients with hemiparesis at an early stage after stroke: a comparison of walking training on atreadmill with body weight support and walking training on the ground. Clin. Rehabil 15 (5), 515e527. Nudo, R.J., 2003. Adaptive plasticity in motor cortex: implications for rehabilitation after brain injury. J. Rehabil. Med. 41 (Suppl.), 7e10. Nudo, R.J., 2007. Post infarct cortical plasticity and behavioral recovery. Stroke 38 (2 Suppl.), 840e845. Nudo, R.J., Friel, K.M., Delia, S.W., 2000. Role of sensory deficits in motor impairments after injury to primary motor cortex. Neuropharmacology 39 (5), 733e742. Nudo, R.J., Plautz, E.J., Frost, S.B., 2001. Role of adaptive plasticity in recovery of function after damage to motor cortex. Muscle Nerve 24 (8), 1000e1019. Paci, M., 2003. Physiotherapy based on the Bobath concept for adults with post-stroke hemiplegia: a review of effectiveness studies. J. Rehabil. Med. 35 (1), 2e7. Page, S.J., Sisto, S., Johnston, M.V., Levine, P., 2002. Modified constraint-induced therapy after subacute stroke: a preliminary study. Neurorehabil. Neural Repair 16 (3), 290e295. Page, S.J., Levine, P., Leonard, A., 2007. Mental practice in chronic stroke: results of a randomized, placebo-controlled trial. Stroke 38 (4), 1293e1297. Page, S.J., Szaflarski, J.P., Eliassen, J.C., Pan, H., Cramer, S.C., 2009. Cortical plasticity following motor skill learning during mental practice in stroke. Neurorehabil. Neural Repair 23 (4), 382e388. Piron, L., Tonin, P., Atzori, A.M., et al., 2003. The augmentedfeedback rehabilitation technique facilitates the arm motor recovery in patients after a recent stroke. Stud. Health Technol. Inform. 94, 265e267. Prange, G.B., Jannink, M.J., Groothuis-Oudshoorn, C.G., Hermens, H.J., Ijzerman, M.J., 2006. Systematic review of the effect of robot-aided therapy on recovery of the hemiparetic arm after stroke. J. Rehabil. Res. Dev. 43 (2), 171e184. Richards, L., Hanson, C., Wellborn, M., Sethi, A., 2008a. Driving motor recovery after stroke. Top. Stroke Rehabil. 15 (5), 397e411. Richards, L.G., Stewart, K.C., Woodbury, M.L., Senesac, C., Cauraugh, J.H., 2008b. Movement-dependent stroke recovery: a systematic review and meta-analysis of TMS and fMRI evidence. Neuropsychologia 46 (1), 3e11.
Rossini, P.M., Calautti, C., Pauri, F., Baron, J.C., 2003. Post-stroke plastic reorganisation in the adult brain. Lancet Neurol. 2 (8), 493e502. Salbach, N.M., Mayo, N.E., Wood-Dauphinee, S., Hanley, J.A., Richards, C.L., Co ˆte ´, R., 2004. A task-orientated intervention enhances walking distance and speed in the first year post stroke: a randomized controlled trial. Clin. Rehabil. 18 (5), 509e519. Sawner, K.A., LaVigne, J.M., 1992. Brunnstrom’s Movement Therapy in Hemiplegia: a Neurophysiological Approach, second ed. JB Lippincott, Philadelphia. Schaechter, J.D., 2004. Motor rehabilitation and brain plasticity after hemiparetic stroke. Prog. Neurobiol. 73 (1), 61e72. Schaechter, J.D., Kraft, E., Hilliard, T.S., et al., 2002. Motor recovery and cortical reorganization after constraint-induced movement therapy in stroke patients: a preliminary study. Neurorehabil. Neural Repair 16 (4), 326e338. Schmidt, R.A., 2005. Motor Control and Learning: a Behavioral Emphasis, fourth ed. Human Kinetics, Champaign, IL, USA. 1e22. Sharma, N., Pomeroy, V.M., Baron, J.C., 2006. Motor imagery: a backdoor to the motor system after stroke? Stroke 37 (7), 1941e1952. Shumway-Cook, A., Woollacott, M., 2006. Motor Control e Translating Research into Clinical Practice, third ed. Lippincott Williams & Wilkins. 3e20. Suputtitada, A., Yooktanan, P., Rarerng-Ying, T., 2004. Effect of partial body weight support treadmill training in chronic stroke patients. J. Med. Assoc. Thai 87 (Suppl. 2), S107eS111. Takahashi, C.D., Der-Yeghiaian, L., Le, V., Motiwala, R.R., Cramer, S.C., 2008. Robot-based hand motor therapy after stroke. Brain 131 (Pt 2), 425e437. Taub, E., Uswatte, G., King, D.K., Morris, D., Crago, J.E., Chatterjee, A., 2006. A placebo-controlled trial of constraint-
537 induced movement therapy for upper extremity after stroke. Stroke 37 (4), 1045e1049. Teasell, R., Bayona, N.A., Bitensky, J., 2005. Plasticity and reorganization of the brain post stroke. Top. Stroke Rehabil. 12 (3), 11e26. Turkstra, L.S., Holland, A.L., Bays, G.A., 2003. The neuroscience of recovery and rehabilitation: what have we learned from animal research? Arch. Phys. Med. Rehabil. 84 (4), 604e612. Werner, C., Bardeleben, A., Mauritz, K.H., Kirker, S., Hesse, S., 2002. Treadmill training with partial body weight support and physiotherapy in stroke patients: a preliminary comparison. Eur. J. Neurol. 9 (6), 639e644. Wevers, L., van de Port, I., Vermue, M., Mead, G., Kwakkel, G., 2009. Effects of task-oriented circuit class training on walking competency after stroke: a systematic review. Stroke 40 (7), 2450e2459. Will, B., Galani, R., Kelche, C., Rosenzweig, M.R., 2004. Recovery from brain injury in animals: relative efficacy of environmental enrichment, physical exercise or formal training. Prog. Neurobiol. 72 (3), 167e182. Wolf, S.L., 2007. Revisiting constraint-induced movement therapy: are we too smitten with the mitten? Is all nonuse "learned"? and other quandaries. Phys. Ther. 87 (9), 1212e1223. Wolf, S.L., Winstein, C.J., Miller, J.P., et al., 2006 November 1. Effect of constraint-induced movement therapy on upper extremity function 3 to 9 months after stroke: the EXCITE randomized clinical trial. JAMA 296 (17), 2095e2104. You, S.H., Jang, S.H., Kim, Y.H., et al., 2005. Virtual realityinduced cortical reorganization and associated locomotor recovery in chronic stroke: an experimenter-blind randomized study. Stroke 36 (6), 1166e1171. Zimmermann-Schlatter, A., Schuster, C., Puhan, M.A., Siekierka, E., Steurer, J., 2008. Efficacy of motor imagery in post-stroke rehabilitation: a systematic review. J. Neuroeng Rehabil. 14 (5), 8.
PREVENTION & REHABILITATION - REHABILITATION
Neurorehabilitation Neuroplasticity
Journal of Bodywork & Movement Therapies (2011) 15, 538e541
available at www.sciencedirect.com
journal homepage: www.elsevier.com/jbmt
CLINICAL METHODS
A case study utilizing Vojta/Dynamic Neuromuscular Stabilization therapy to control symptoms of a chronic migraine sufferer PREVENTION & REHABILITATION e CLINICAL METHODS
David D. Juehring, DC, DACRB*, Michelle R. Barber, BA, MSW, DC Palmer Chiropractic Rehabilitation and Sports Injury Department, Palmer College of Chiropractic, 1000 Brady Street, Davenport, IA 52803, United States Received 10 November 2010; received in revised form 21 December 2010; accepted 14 January 2011
KEYWORDS Migraine; Chronic; Treatment; Vojta; Dynamic Neuromuscular Stabilization
Summary Introduction: Migraine is a complex disorder of the brain characterized by severe headache, photophobia, phonophobia, and nausea. This case report demonstrated the reduction of a 49-year-old female’s chronic migraine symptoms after 12 weeks of Vojta/Dynamic Neuromuscular Stabilization (DNS) therapy. Methods: Vojta/DNS treatment occurred either in the office or at home over a 12-week period. Symptoms were tracked via a patient diary, a VAS pain scale, and a Headache Disability Index (HDI). Results: The patient’s migraine symptoms were typically of 3 days duration, a frequency of 8e10 times per month, and an intensity of 10/10 on a VAS pain scale. After a 12-week trial of Vojta/DNS care, subjective improvements were noted, with a reduction in frequency to 1e2 times per month, duration of 12 h at most, and decreased intensity to a 2/10 on a VAS pain scale. HDI scores dropped from 48% to 34%. Discussion: This therapy reduced the patient migraine sysmptoms in frequency, duration and intensity. This therapy is not well-known in North America despite its use for over 40 years in Europe. Conclusion: This case demonstrated that Vojta/DNS treatment over a 12-week period helped manage the patient’s migraines and could be a possible treatment option for future research. ª 2011 Elsevier Ltd. All rights reserved.
* Corresponding author. Tel.: þ1 563 884 5455; fax: þ1 563 884 5865. E-mail address:
[email protected] (D.D. Juehring). 1360-8592/$ - see front matter ª 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.jbmt.2011.01.019
Introduction Migraine is a complex disorder of the brain which is typically characterized by spontaneous attacks of unilateral, throbbing headaches which are often aggravated by movements (Messlinger, 2009), along with non-headache symptoms including photophobia, phonophobia, and nausea (Sprenger and Goadsby, 2009). These characteristic symptoms are found in all types of migraine, the most common types being migraine without aura, fo0llowed by migraine with aura (Messlinger, 2009). It has been found that nearly half the world’s population has an active headache disorder and according to the American Migraine Prevalence and Prevention study of 2004 (Lipton et al., 2007), migraine in particular has a prevalence of 12% in the general population, 18% in women, and 6% in men (Robbins and Lipton, 2010). Migraine is reported to be among the top 20 causes of disability worldwide, as more than half of those affected have such severe symptoms that they cannot function normally in their routine daily activities, including work, school, and social activities (Brandes, 2009). 48.2% of migraineurs reported some level of impairment, 22.1% were severely disabled, and more than half reported the need for bed rest (Lipton et al., 2007). In addition, during the periods between attacks, worry, stress, and expectation of future attacks may also lead to functional impairment, a phenomenon known as the interictal burden (Brandes, 2009). It is commonly noted that migraine attacks may be precipitated by a number of factors, which are often termed “migraine triggers.” Approximately 76% of migraine sufferers report identifiable triggers (Sauro and Becker, 2009). Reported triggers are widely varied, including hormonal changes in women e migraine headache is related to the menstrual cycle in about 60% of female patients (Lambert and Zagami, 2009) e certain foods, missing meals, weather changes, alcohol, and sleep disturbances. Fatigue is the most commonly reported trigger, with stress the second most common (Sauro and Becker, 2009). Additional triggers can include flickering lights, loud noises, strong smells, drugs which deplete the brain of the neurotransmitter serotonin, environmental changes e especially in temperature and barometric pressure e and for many patients no external trigger is apparent at all (Lambert and Zagami, 2009). The variety of triggers and the individual nature of triggers have led to the hypothesis that only some kind of neural event can explain triggering. There is much evidence in the literature at this time to support the notion that migraine is more than a headache disorder, but instead is a pathophysiologically complex disorder that arises from a neurovascular disturbance in the brain itself, and involves modulatory mechanisms in the brainstem, subcortical, and cortical levels to process pain. These processing mechanisms may be abnormal in migraine, which uses otherwise normal neural pathways for pain transmission (Purdy, 2010). As depression travels slowly across the cerebral cortex (cortical spreading depression), trigeminal nerve terminals surrounding the meningeal arteries are stimulated, eliciting a trigeminovascular reflex that explains subsequent vascular changes and headache (Martins, 2009). Migraine sufferers typically try a multitude of interventions in an effort to reduce the frequency and severity of
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their attacks as well as to improve function and reduce disability (Brandes, 2009). There are numerous pharmacological interventions, including beta-blockers, antidepressants, anticonvulsants, calcium channel blockers and serotonin antagonists, but side effects and contraindications because of co-morbidities can complicate treatment (Sprenger and Goadsby, 2009). Over half of the diagnosed migraineurs in the US use OTC analgesics, which are effective in up to 60% of cases (Whyte et al., 2010). Many migraine patients try manual therapies; primary choices are physical therapy, massage, and spinal manipulative therapy (Biondi, 2005). Recent reviews have shown physical therapy is most effective in combination with other therapies such as biofeedback, relaxation training, and exercise (Biondi, 2005). Massage therapy was shown to be beneficial in reducing frequency of migraine attacks, as well as improving perceived stress and coping efficacy (Lawler and Cameron, 2006). There is also some evidence indicating that spinal manipulation has effectiveness similar to a firstline prophylactic prescription medication (amitriptyline) for the prophylactic treatment of migraine (Bronfort et al., 2010). In addition, migraine patients also frequently use complementary and alternative medicine (CAM), with relaxation therapies and chiropractic care being the most common CAM therapies employed (Astin and Ernst, 2002). Additional alternative treatments include: vitamins and minerals such as riboflavin, niacin, and magnesium; supplements such as feverfew, butterbur, and coenzymeQ10; mind-body therapies such as biofeedback, cognitive behavioral therapy, guided imagery, “headache school,” self-hypnosis, meditation, and relaxation training; physical treatments such as acupuncture, massage therapy, physical therapy, and spinal manipulation; and lifestyle modifications such as food and alcohol elimination, aerobic exercise, and sleep hygiene (DynaMed, 1995). Vojta/Dynamic Neuromuscular Stabilization (DNS) is a therapy used predominantly in Europe to manage neurological and musculoskeletal conditions (Laufens et al., 1999; Niethard, 1987; Bo ¨hme and Futschik, 1995; Bauer et al., 1992; Vojta and Peters, 2007). Vojta therapy was developed from 1955 to 1969 by a Czech pediatric neurologist Vaclav Vojta (Bauer et al., 1992; Vojta and Peters, 2007). His treatment approach in the broadest of terms involved utilizing digital pressure on specific points of the body to provide afferent stimulation to evoke genetically predetermined CNS motor programs to address various neurological-based conditions (Vojta and Peters, 2007). Since the mid-nineties, these treatment principles and approaches have since been modified by Pavel Kola ´r, a physiotherapist from the Czech Republic. His modified approach was eventually named Dynamic Neuromuscular Stabilization (Bokarius and Bokarius, 2008). The purpose of this case report is to demonstrate how the Vojta/DNS treatment approach greatly reduced diagnosed migraine symptoms over a 12-week period for a 49-year-old female who had consistently experienced intense frequent symptoms over her last 40 years.
Methods The initial treatments consisted of Vojta/DNS therapy for 10e15 min in a supine position with the patient’s palms
PREVENTION & REHABILITATION e CLINICAL METHODS
A case study utilizing Vojta/Dynamic Neuromuscular Stabilization therapy
PREVENTION & REHABILITATION e CLINICAL METHODS
540 placed down on the treatment table. The patient was positioned supine due the ease of maintaining cervical spine neutral posture. On general patient visual observation of the cervical spine on both standing and supine the patient had a slight left lateral shearing and rotation along with anterior head carriage. It was theorized that this postural aberration may have been the possible cause for the patient’s chronic symptoms. To neutralize this postural issue in the cervical spine, mild long-axis digital pressure was applied at the occiput to help hold the cervical spine in the neutral position while minimizing upper cervical hyperextension. This positioning maximized cervical spinal joint centration, ultimately relaxing overactive cervical muscles and establishing a neutral cervical spine posture. Along with this positioning, firm digital pressure was applied between ribs seven and eight at the mid-clavicular line directed towards the fourth thoracic vertebral body to provide proprioceptive afferent input as part of the treatment approach. Clinical judgment determined daily treatment times based upon a reduction of cervical tension to enhance neutral cervical posture; treatment times were longer in the initial stages of care as compared to the end stages of daily treatment times. Care was taken to apply firm pressure without causing a painful stimulus to the patient and that digital pressure did not cause any lateral bending, rotation, or shear in the thoracic spine to maintain a neutral spine. The above treatment procedure was performed on one side of the body for half the treatment time, then switched to the contralateral side based upon the patient’s cervical asymmetries (Kola ´r, 2007). During the course of treatment, the patient’s initial Vojta/DNS treatments started at 2e3 days of treatments each week for the first three weeks, then tapered to one treatment every 2e3 weeks until the last month of care when the patient was only seen once. At three weeks of care it was apparent that positive outcomes were obvious by patient report, at which time the patient’s spouse was trained to provide basic care at home on non-office days to help progress the continual drop in the patient’s frequency, duration and intensity of symptoms. For home care, it was recommended that the care be performed daily at the same duration and position used in the office. It was also recommended to perform the care on a firm surface such as the floor similar to the hardness of the office treatment tables. The patient’s symptoms pertaining to these parameters were monitored per patient visit and via a daily diary kept by the patient. A Headache Disability Index and VAS pain scale was utilized on the initial visit and only again at week 12 comparison without intermediate assessments.
Results Prior to treatment, the patient reported symptoms of intense headaches, light sensitivity, vision disturbances, vomiting, and fatigue which occurred 8e10 times per month and lasted consistently for three days. After a 12week clinical trial, subjective improvements were noted, with a reduction of symptom frequency of one to two times a month, lasting at most 12 h in duration and with an eightpoint reduction on a ten-point VAS pain scale. Headache Disability Index scores dropped from 48% to 34%. At one
D.D. Juehring, M.R. Barber time during therapy, the patient was without migraines for a three-week period, which she recalled had never happened before.
Discussion Vojta/Dynamic Neuromuscular Stabilization therapy has been utilized in the management of neurological and musculoskeletal conditions (Laufens et al., 1999; Niethard, 1987; Bo ¨hme and Futschik, 1995; Bauer et al., 1992; Vojta and Peters, 2007) throughout Europe, though it is not well known as a care option in North America. Vojta therapy has been applied roughly from the 1950s to present and was initially developed by the pediatric neurologist Vaclav Vojta (Bauer et al., 1992; Vojta and Peters, 2007). Through his clinical observation of the development of healthy infants, he noted a natural progression that they underwent for functional movements. He believed this was not a learned behavior but a genetically predetermined program that was expressed by the CNS as it developed (Vojta and Peters, 2007). Vojta’s clinical approach to less-than-ideal development movement patterns was to manually stimulate specific zones of the body to evoke genetically predetermined efferent motor expressions of the CNS to regain ideal movement patterns. This program was defined as “reflex locomotion” (Vojta and Peters, 2007). This approach was eventually applied to adults for numerous neuromusculoskeletal conditions. The principles and treatment methods were later expanded upon by Pavel Kola ´r, Director of the Rehabilitation Department at University Hospital Motol, in Prague, Czech Republic. Dr. Kola ´r added active components and loaded positioning to these methods to address dysfunctions and coined the name Dynamic Neuromuscular Stabilization (DNS) (Bokarius and Bokarius, 2008). In this case, the patient had been diagnosed with migraines by two neurologists and three MRIs spanning a twenty-year period. She tried many treatment approaches with nominal results. She had tried upper cervical specific chiropractic care for an approximately three-month period of time with an occasional mild reduction of symptoms which would quickly return within a week. Also she had tried soft tissue release for two visits to address the hyperflexion of the upper cervical spine which greatly intensified the frequency, intensity and length of her migraine symptoms. The therapy she most utilized was OTC pain and headache medicines with only mild temporary results. She reported having “debilitating” migraines once to twice a year that would be relieved by Imitrex (triptan) injections. Unfortunately, there exists little published Vojta/DNS literature on the concepts and treatment approaches, with even less articles written in English. The Vojta/DNS approach was considered in this case due to its proposed speculative ability to address global neurological disturbances at a subcortical level, based upon the concepts and treatment possibilities presented in printed materials (Laufens et al., 1999; Niethard, 1987; Bo ¨hme and Futschik, 1995; Bauer et al., 1992; Vojta and Peters, 2007; Kola ´r, 2007). With the theories of migraine as a pathophysiologically complex disorder that arises from a neurovascular disturbance in the brain itself, and involves modulatory mechanisms in the brainstem, subcortical and cortical
levels to process pain (Purdy, 2010), the authors postulated that it would appear worthy of a clinical trial for this patient’s particular condition utilizing Vojta/DNS therapy. Vojta/DNS care was also considered as a possible method of treatment due to her responses to other previous neuromuscular care. Although negative with the soft tissue treatment and only slightly positive with the upper cervical adjustive care the authors speculated that a treatment in the cervical spine given the postural asymmetries could be minimized or eliminated from the neuromuscular impacts suggested in published articles (Bokarius and Bokarius, 2008; Laufens et al., 1999; Kola ´r, 2007). The supine position was utilized to help facilitate global neutral positioning of the cervical spine to address left lateral shear and rotation along with anterior head carriage to reduce cervical postural asymmetries in hopes to impact symptoms. The stimulation point and body posture utilized is considered the most effective at facilitating sagittal stability (Vojta and Peters, 2007). Other beneficial reasons for the choice of this treatment position were its comfort for the patient and the relative ease of educating the patient’s husband to perform the appropriate positioning and treatment at home for an effective therapeutic response by a lay person.
Conclusion This case demonstrated that Vojta/DNS treatment over the course of 12 weeks helped manage the patient’s migraines. This treatment approach demonstrated an effect on this patient’s condition by reducing the patient’s reported frequency, duration and intensity of symptoms along with reduced VAS pain scale and Headache Disability Index scores. Migraine is a disorder of the brain characterized by a complex sensory dysfunction, and as such, interventional neuromodular approaches with neural targets are most promising (Sprenger and Goadsby, 2009). Looking at migraine from a neurobiological approach, it would seem that any approaches which involve change or perturbation of the abnormal processes could reduce migraine symptoms (Purdy, 2010). The positive outcomes achieved in this case using the Vojta/DNS approach to addressing neurological disturbances have promising potential. Further research is needed to evaluate this clinical approach and its success in treating other patients with migraine disorders.
Conflict of interest The authors declare that they have no conflict of interest.
References Astin, J.A., Ernst, E., 2002. The effectiveness of spinal manipulation for the treatment of headache disorders: a systematic review of randomized clinical trials. Cephalalgia 22 (8), 617e623.
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Bauer, H., Appaji, g, Mundt, D., 1992. Vojta Neurophysiologic Therapy. Indian Journal of Pediatrics 59, 37e51. Biondi, D., 2005. Physical treatments for headache: A structured review. Headache (45), 738e746. Bo ¨hme, B., Futschik, M., 1995. Verbesserte Lungenfunktion nach Vojta-Brustzonen-Reiz bei bronchopulmonaler Dysplasie. Monatsschrift fu ¨r Kinderheilkunde 143, 1231e1234 (in German). Brandes, J.L., 2009. Migraine and functional impairment. CNS Drugs 23 (12), 1039e1045. Bronfort, G., Haas, M., Evans, R., Leininger, B., Triano, J., 2010. Effectiveness of manual therapies: the UK evidence report. Chiropractic and Osteopathy 18:3. Bokarius, A.V., Bokarius, V., 2008. Long-term efficacy of dynamic neuromuscular stabilization in treatment of chronic musculoskeletal pain. In: Abstract of the 12th World Congress on Pain, Glasgow, Scotland. DynaMed [Internet], 1995. EBSCO Publishing, Ipswich (MA) [cited 2010 Nov 2]. Available from: http://www.ebscohost.com/ dynamed/. Kola ´r, P., 2007. Facilitation of agonist-antagonist activation by reflex stimulation methods. In: Liebenson, C. (Ed.), Rehabilitation of the Spine, second ed. Lippincott/Williams & Wilkins, Philadelphia. Lambert, G.A., Zagami, A.S., 2009. The mode of action of migraine triggers: a hypothesis. Headache 49 (2), 253e275. Laufens, G., Poltz, W., Prinz, E., Reimann, G., Schmiegelt, F., 1999. Verbesserung der Lokomotion durch kombinierte Laufband-/Vojta-Physiotherapie bei ausgewa ¨hlten MS-Patienten. Physikalische Medizin. Rehabilitationsmedizin, Kurortmedizin 9, 187e189 (in German). Lawler, S.P., Cameron, L.D., 2006. A randomized, controlled trial of massage therapy as a treatment for migraine. Annals of Behavioral Medicine 32 (1), 50e59. Lipton, R.B., Bigal, M.E., Diamond, M., Freitag, F., Reed, M.L., Stewart, W.F.AMPP Advisory Group, 2007. Migraine prevalence, disease burden, and the need for preventive therapy. Neurology 68 (5), 343e349. Martins, I.P., 2009. Migraine. Acta Me ´dica Portuguesa 22 (5), 589e598 (in Portugese). Messlinger, K., 2009. Migraine: where and how does the pain originate? Experimental Brain Research 196 (1), 179e193. Niethard, F.U., 1987. Vorla ¨ufige Behandlung angeborener Hu ¨ftluxation durch physikalische Therapie auf Basis der Neurophysiologie. Zeitschrift fu ¨die und Unfallchirurgie 125, ¨r Orthopa 28e34 (in German). Purdy, R.A., 2010. Migraine is curable! Neurologic Sciences 31 (Suppl. 1), S141eS143. Robbins, M.S., Lipton, R.B., 2010. The epidemiology of primary headache disorders. Seminars in Neurology 30 (2), 107e119. Sauro, K.M., Becker, W.J., 2009. The stress and migraine interaction. Headache 49 (9), 1378e1386. Sprenger, T., Goadsby, P.J., Nov 16 2009. Migraine pathogenesis and state of pharmacological treatment options. BMC Medicine 7, 71. Vojta, V., Peters, A., 2007. Das Vojta-Prinzip Muskelspiele in Reflexfortbewegung und Motorischer Ontogenese, third ed. Springer Medizin Verlag, Heidelberg. Whyte, C., Tepper, S.J., Evans, R.W., 2010. Expert opinion: rescue me: rescue medication for migraine. Headache 50 (2), 307e313.
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Journal of Bodywork & Movement Therapies (2011) 15, 542e544
available at www.sciencedirect.com
PREVENTION & REHABILITATION e SELF MANAGEMENT: PATIENT SECTION
journal homepage: www.elsevier.com/jbmt
PREVENTION & REHABILITATION e SELF MANAGEMENT: PATIENT SECTION
Functional training with the kettlebell Craig Liebenson, DC* L.A. Sports & Spine, 10474 Santa Monica Blvd, #304, Los Angeles 90025, USA There are various types of traditional strengthening exercises such as Nautilus, free weights, pulleys, etc. Most follow a certain rule of isolating individual muscles and making them bigger and stronger. Kettlebells have been used in Russia for a long time, but are new in most other parts of the world. What is unique about kettle bells is that due to their shape they provide an unstable force which the body has to learn to handle. It is not merely a matter of building strength, but learning how to control e or stabilize e the weight. In this way kettlebell (KB) exercises are ideal for functional training that mirrors the challenges one faces in day to day activities (McGill, 2011). Many people with persistent pain have trouble carrying objects. Carrying a briefcase, grocery bag, or baby requires both strength and stability. Strength is needed to lift the object, while stability is necessary to maintain balance or equilibrium during the task. Unfortunately, in training stability is usually ignored even though it is the more decisive of the two components in determining your injury risk. The KB exercises shown here are excellent for training both strength and stability during carrying activities. Key points are highlighted for each exercise to ensure that stability is not sacrificed while trying to build as much strength as possible. Each of the exercises shown here focus on hip and trunk stability in what is called the frontal plane. Whereas popular exercises like sit-ups, chest press, or bicep curls train forward or backward bending motions, these carrying exercises work stability in a side to side direction. This is of great importance since instability in the frontal plane leads to excessive side to side motion which has been shown to cause injury to the knee or low back (see Fig. 1).
* Tel.: þ1 31047 02909; fax: þ1 31047 03286. E-mail address:
[email protected]. URL: http://craigliebenson.com. 1360-8592/$ - see front matter ª 2011 Published by Elsevier Ltd. doi:10.1016/j.jbmt.2011.07.003
Suitcase Carry Start with this exercise Hold a KB in your hand like it is a suitcase (see Figure 2) Take about 20 steps at a normal or somewhat brisk pace Then, switch hands Start with a light weight such as 5 kg
Figure 1
Carrying a grocery bag (a) unstable (b) stable.
Figure 2
Suitcase Carry.
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Figure 3
Waiter Carry.
Key Point: Avoid excessive side to side swaying of the body Waiter Carry Grip the KB in your hand like it is a barbell (see Figure 3) Take about 20 steps at a normal or somewhat brisk pace Then, switch hands Start with a light weight such as 5 kg Key Point: Avoid excessive shrugging of your shoulder on the side of the weight Overhead Carry Grip the KB in your hand while reaching your arm overhead as far as possible (see Figure 4) Take about 20 steps at a normal or somewhat brisk pace Then, switch hands Start with a light weight such as 5 kg Key Point: Avoid leaning to the side when walking with the KB Bottoms Up Carry Hold the KB by the handle firmly and turn it upside down so that it’s bottom is facing up (see Figure 5a) Keep your elbow in at your side and slightly “brace” (i.e. tighten) your core to stabilize your body Take about 20 steps at a normal or somewhat brisk pace Then, switch hands Start with a light weight such as 5 kg
Figure 4
Overhead Carry.
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Functional training with the kettlebell
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C. Liebenson
Figure 5
Bottoms Up Carry (a) correct arm position (b) incorrect.
Key Point: Avoid holding the KB away from your body (see Figure 5b) The Farmer’s Walk Hold a KB in each hand with arms extended down at your side (see Figure 6)
Take about 20 steps at a normal or somewhat brisk pace Start with a light weight such as 5 kg Key Point: Avoid excessive swaying side to side while walking
Reference McGill, S., 2011. Ultimate Back Fitness and Performance, fourth edition. Back Fit Pro.
Figure 6
Farmer’s Walk.
