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Sports Med 2010; 40 (9): 715-727 0112-1642/10/0009-0715/$49.95/0

LEADING ARTICLE

ª 2010 Adis Data Information BV. All rights reserved.

Neuromotor Control of the Lower Limb in Achilles Tendinopathy Implications for Foot Orthotic Therapy Narelle Wyndow,1 Sallie M. Cowan,2 Tim V. Wrigley1 and Kay M. Crossley 2,3 1 Centre for Health, Exercise and Sports Medicine, Melbourne Physiotherapy School, University of Melbourne, Melbourne, Victoria, Australia 2 Melbourne Physiotherapy School, University of Melbourne, Melbourne, Victoria, Australia 3 Department of Mechanical Engineering, Melbourne School of Engineering, University of Melbourne, Melbourne, Victoria, Australia

Abstract

Achilles tendinopathy (AT) is a common injury in running sports. While the exact aetiology of Achilles injury is still unclear, foot orthoses are often effectively employed in the conservative management of the condition. Foot orthoses have traditionally been provided for people with AT on the basis that they may reduce the rearfoot eversion associated with excessive foot pronation. This increased rearfoot motion is thought to produce excessive Achilles tendon loads. To date, the available literature indicates that foot orthoses have small and unsystematic effects on rearfoot kinematics. However, limitations of foot kinematic measurement currently restrict the ability to conduct truly valid investigations into kinematic responses to foot orthoses. Therefore, the roles of alternate mechanisms, for which orthoses may provide clinical success in pathology such as AT, are now being investigated. One alternative theory is that foot orthoses alter neuromotor recruitment patterns and thus lower limb loads in response to the additional sensory input provided by the device. In AT, altered neuromotor recruitment patterns of the triceps surae have been hypothesized to create differential intratendinous loads. This may lead to pathological changes within the tendon. Furthermore, it is possible that foot orthoses may aid to normalize intratendinous loads via altering neuromotor activity in the triceps surae in AT. This review examines the literature with regard to changes in neuromotor recruitment as an associated aetiological factor in AT and the role foot orthoses may play in the management of this condition.

1. Introduction Achilles tendinopathy (AT) is commonly experienced by people involved in sporting activities involving running. Abnormal load is considered

to be integral to the development of AT; however, the exact aetiology of AT is still unclear. Biomechanical ‘faults’, particularly excessive foot pronation, have been considered to contribute to the pathogenesis of AT.[1-3] However, only a few

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studies have investigated this relationship with mostly consistent results observed.[2,4,5] For example, one recent study found increased rearfoot eversion in subjects with AT when running barefoot,[2] while another study only found increased rearfoot eversion during shod running.[4] Centre of pressure (CoP) measures from the plantar surface of the foot are not more medially deviated in subjects with AT than in healthy controls.[5] Therefore, while excessive pronation may be associated with AT symptomatology, it is possible that there are alternate contributions to the mechanical pathogenesis of AT. Various investigations, from cadaver studies to in vivo cine magnetic resonance imaging (MRI), coupled with optic fibre technology, have suggested that non-homogenous stress within the Achilles tendon may be associated with tendon pathology.[6-9] An altered neuromotor activation strategy of the triceps surae has been proposed as one potential source of nonhomogenous Achilles tendon stress.[6,10] As indicated above, foot orthoses are considered an effective component in the conservative treatment of AT.[1,11-14] However, the exact mechanisms by which foot orthoses provide clinical benefit in the management of this condition are not understood. Currently, there is only one randomized controlled trial on the use of foot orthoses in AT. This study demonstrated that the use of foot orthoses for 4 weeks was sufficient to produce significant improvements in pain and eccentric calf strength in the absence of a formal strength training programme.[11] A similar improvement in pain and eccentric calf strength was found following conservative physical therapy consisting of sensorimotor and eccentric training in combination with deep frictions and ultrasound. The exact mechanism via which foot orthoses produced this response was not able to be determined from this study. However, the authors hypothesized that the orthoses may have modified sensory input to provide ‘optimization of muscular-regulated joint stability’. Recent electromyography (EMG) and MRI investigations into the response to foot orthoses in pronated but uninjured populations indicate that the devices modified the neuromotor activation patterns in a running task[15] and a seated foot adduction task.[16] While the ª 2010 Adis Data Information BV. All rights reserved.

neuromotor responses differed between the two studies, this is likely related to the specificity of neuromotor responses to both the task and the type of foot orthoses used. Developing a better understanding of whether altered neuromotor activation is associated with AT may enable the development and implementation of targeted treatment of the functional deficits associated with the pathology. Specifically, the efficacy of foot orthoses as an intervention may be increased by improving our understanding of the effect of foot orthoses on the neuromotor control of the triceps surae. Additionally, if altered neuromotor control precedes the development of AT, it may be possible to screen those at risk prior to the development of pathology. 2. Purpose and Methodology This article reviews the literature pertaining to neuromotor activity in the triceps surae in subjects with AT and uninjured runners. In addition, literature relating to the neuromotor effects of foot orthoses in the lower limb will be reviewed to provide a possible mechanism for the clinical response to foot orthoses in Achilles injuries. Searches in MEDLINE (PubMed) and Web of Knowledge databases were performed using the search terms ‘Achilles tendinosis’, ‘Achilles tendinopathy’, ‘Achilles tendonitis’, ‘shoe inserts’, ‘foot orthoses’, ‘heel lifts’, ‘running biomechanics’, ‘muscle activity’ and ‘EMG’. The reference lists of the articles obtained were also hand searched for relevant articles. 3. Achilles Tendinopathy (AT) 3.1 Incidence and Morbidity

Achilles tendon injuries are commonly experienced by individuals participating in activities involving running and/or jumping. A recent systematic review of running injuries in long-distance runners found that lower leg injuries account for 9–32.2% of all injuries sustained by runners.[17] The frequency of Achilles injury, specifically, has been reported to be between 7% and 9% of all running injuries.[1,18,19] It appears to be more common in men than women, usually presenting Sports Med 2010; 40 (9)

Neuromotor Control of the Lower Limb in Achilles Tendinopathy

in the 35–45 years of age group.[20] In a surgical cohort of 58 patients with Achilles tendon pain, 31% were classified as having low activity levels. Thus, the authors proposed that the loads associated with physical activity may not be the primary cause of the condition in this patient population.[21] While most cases of AT are managed non-operatively, there is limited evidence on which to base the conservative treatment of Achilles tendon disorders.[22,23] In a review article of AT in athletic populations, Kvist[3] commented that approximately 25% of this population required surgical intervention, and the frequency of surgery increased with patient age and duration of symptoms, as well as the presence of pathological change in the tendon. Furthermore, approximately 3–5% of patients had to abandon their sporting activities because of Achilles injuries. 3.2 Achilles Tendon Anatomy and Function

The Achilles tendon is comprised of the combined tendons of the medial and lateral heads of the gastrocnemius and the soleus muscles (triceps surae). It inserts into the posterior surface of the calcaneus. At around the level that the soleus muscle begins to contribute fibres to the Achilles tendon, the tendon spirals with the medial fibres rotating posteriorly and the posterior fibres rotating laterally.[24] The degree of rotation varies from 11 to 68.[25] Each of the triceps surae muscle bellies forms a fascicle of the tendon. A recent cadaver study found that the posterior and lateral portions of the tendon are comprised of fibres from the medial head of the gastrocnemius. The fibres from the lateral head of the gastrocnemius muscle constitute the anterior tendon layer and fibres from the soleus muscle are located in the anteromedial part of the Achilles tendon.[26] Biomechanically, the tendon transmits forces from the gastrocnemius and soleus muscles to the calcaneus during gait. Soleus is the primary plantarflexor of the ankle joint during walking (i.e. activating concentrically late in stance). In addition, it serves an eccentric postural role to control dorsiflexion and prevent excessive anterior translation of the body over the foot during static stance and during the stance phase of ª 2010 Adis Data Information BV. All rights reserved.

717

walking and running.[27] As the gastrocnemius originates on the posterior surface of the femoral condyles, it is capable of flexing the knee joint as well as plantarflexing the ankle joint. Additionally, the triceps surae has a role in the control of pronation and supination of the subtalar joint. Eversion moments at the calcaneus have been demonstrated by the tensioning of the lateral gastrocnemius in cadaver specimens, while calcaneal inversion moments are observed with all other combinations of soleus and gastrocnemius tensioning.[8] Measurement of tendon force in vivo is extremely difficult due to ethical and feasibility constraints. However, one group used a buckle-type force transducer to measure tendon force in a healthy participant.[28] They recorded force up to 9 kN during running (corresponding to 12.5 times bodyweight), 2.6 kN during walking and 7 degrees of forefoot varus. Clin J Sports Med 2006; 16 (4): 316-22 98. Vanicek N, Kingman J, Hencken C. The effects of foot orthotics on myoelectric fatigue in the vastus lateralis during a simulated skier’s squat. J Electromyogr Kinesiol 2004; 14: 693-8


727

99. Waddington G, Adams R. Football boot insoles and sensitivity to extent of ankle inversion movement. Br J Sports Med 2003; 37 (2): 170-5 100. Rose HM, Schultz SJ, Arnold BL, et al. Acute orthotic intervention does not affect muscular response times and activation patterns at the knee. J Athl Train 2002; 37 (2): 133-40 101. Murley GS, Landorf KB, Menz HB, et al. Effect of foot posture, foot orthoses and footwear on lower limb muscle activity during walking and running: a systematic review. Gait Posture 2009; 29 (2): 172-87

Correspondence: Dr Kay M. Crossley, Department of Physiotherapy, Melbourne School of Health Sciences, University of Melbourne, 200 Berkeley St, Carlton, VIC, 3010, Australia. E-mail: [email protected]

Sports Med 2010; 40 (9)

Sports Med 2010; 40 (9): 729-746 0112-1642/10/0009-0729/$49.95/0

REVIEW ARTICLE


A ‘Plane’ Explanation of Anterior Cruciate Ligament Injury Mechanisms A Systematic Review Carmen E. Quatman,1,2 Catherine C. Quatman-Yates1,3 and Timothy E. Hewett1,4,5,6 1 Cincinnati Children’s Hospital Research Foundation, Sports Medicine Biodynamics Center and Human Performance Laboratory, Cincinnati, Ohio, USA 2 University of Toledo, Engineering Center for Orthopaedic Research Excellence, College of Engineering, University of Toledo, Toledo, Ohio, USA 3 Cincinnati Children’s Hospital, Division of Occupational Therapy and Physical Therapy, Cincinnati, Ohio, USA 4 Cincinnati Children’s Hospital Research Foundation, Division of Molecular Cardiovascular Biology, Cincinnati, Ohio, USA 5 University of Cincinnati College of Medicine, Departments of Pediatrics, Orthopaedic Surgery and College of Allied Health Sciences, Department of Rehabilitation Sciences, Cincinnati, Ohio, USA 6 The Ohio State University, Sports Medicine Center, Departments of Physiology and Cell Biology, Orthopaedic Surgery, Family Medicine and Biomedical Engineering, Columbus, Ohio, USA

Contents Abstract. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Search Strategy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1 Electronic Database Literature Search . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2 Inclusionary and Exclusionary Criteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3 Independent Review and Analysis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Discussion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1 Planar Biomechanics Surrounding the Inciting Anterior Cruciate Ligament Injury Event . . . . . . . 4.2 Evidence that Supports a Sagittal Plane Mechanism Theory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3 Evidence Against a Sole Sagittal Plane Mechanism Theory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.4 Evidence that Supports a Frontal Plane Mechanism Theory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.5 Evidence Against a Sole Frontal Plane Mechanism Theory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.6 Evidence in Support of a Transverse Plane Mechanism Theory . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.7 Evidence Against of a Sole Transverse Plane Mechanism Theory . . . . . . . . . . . . . . . . . . . . . . . . . . 4.8 Multi-Planar Mechanism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.9 Kinetic Chain Involvement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Abstract

729 730 731 731 731 733 733 734 734 734 737 738 739 740 740 741 742 742

Although intrinsic and extrinsic risk factors for anterior cruciate ligament (ACL) injury have been explored extensively, the factors surrounding the inciting event and the biomechanical mechanisms underlying ACL injury remain elusive. This systematic review summarizes all the relevant data and

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clarifies the strengths and weaknesses of the literature regarding ACL injury mechanisms. The hypothesis is that most ACL injuries do not occur via solely sagittal, frontal or transverse plane mechanisms. Electronic database literature searches of PubMed MEDLINE (1966–2008), CINAHL (1982–2008) and SportDiscus (1985–2008) were used for the systematic review to identify any studies in the literature that examined ACL injury mechanisms. Methodological approaches that describe and evaluate ACL injury mechanisms included athlete interviews, arthroscopic studies, clinical imaging and physical exam tests, video analysis, cadaveric studies, laboratory tests (motion analysis, electromyography) and mathematical modelling studies. One hundred and ninety-eight studies associated with ACL injury mechanisms were identified and provided evidence regarding plane of injury, with evidence supporting sagittal, frontal and/or transverse plane mechanisms of injury. Collectively, the studies indicate that it is highly probable that ACL injuries are more likely to occur during multi-planar rather than single-planar mechanisms of injury.

1. Introduction The anterior cruciate ligament (ACL) is one of the most commonly injured ligaments of the knee.[1] An estimated 200 000 injuries occur annually in the US and epidemiological studies demonstrate that female athletes have a 2- to 8-fold greater ACL injury rate compared with male athletes.[2,3] ACL injuries can be devastating to an athlete, with the potential loss of a year or more of sports participation, possible loss of scholarship funding and a significantly greater risk of developing knee osteoarthritis in the long term, regardless of the treatment.[4] Prevention of ACL injury would allow many athletes to receive the health benefits of sports participation and avoid the long-term sequelae of disability associated with knee osteoarthritis. It is widely recognized that tibiofemoral knee joint motions occur in three planes (sagittal, frontal and transverse) with six degrees of freedom (three rotations, three translations) between the femoral condyles and tibial plateaus.[5] The knee joint can rotate in the sagittal plane by flexion and extension, in the frontal plane by abduction and adduction, and in the transverse plane by internal and external rotation. The knee joint can also translate in the sagittal plane anteriorly and posteriorly, in the frontal plane medially and laterally, and in the transverse plane by compression and distraction (figure 1). ª 2010 Adis Data Information BV. All rights reserved.

While the knee can move in all 12 of these potential directions, most of these motions take place in a relatively limited range with the exception of flexion and extension (tables I and II). The end range of motion (joint laxity) is highly variable in the general population and may vary by age, pubertal status, sex and race.[10-12] Excessive knee joint loading that leads to motion beyond the normal physiological range in the sagittal, frontal or transverse planes could potentially damage the internal knee joint structures. Several studies indicate that individuals with greater knee or general joint laxity have an increased risk for ACL injury.[13] The planar contributions to the mechanisms of ACL injury is a current debate in recent journal articles, which has led to many letters to the editor, commentaries and symposia at sports medicine conferences.[14-17] Many current ACL prevention programmes only target single plane landing and movement mechanics (hops/jumps in one direction) rather than complex multi-planar movements that incorporate rotational and translational directions.[18-20] Such programmes may minimize risk of injury in the targeted plane but may be ineffective at ameliorating important multi-planar contributions. Likewise, post-injury interventions that neglect to address the multi-planar contributions to ACL injury could seriously hamper ACL injury prevention efforts in athletes returning to sport after a previous ACL injury. This ongoing controversy was the primary motivation Sports Med 2010; 40 (9)

Rotations

ACL Injury Mechanisms

731

Internal/external

Lateral/medial

Flexion/extension

Posterior/anterior

Translations

Distraction/ compression

Adduction/abduction

Fig. 1. Rotation and translation motions of the knee joint.

for examining the multi-planar contributions of ACL injury supported in the literature via a thorough systematic review. This review summarizes all the relevant data and identifies the strengths and weaknesses in the literature regarding ACL injury mechanisms. The primary research goal attempts to identify and consider any biomechanical and mechanistic knee studies that evaluated the ACL in the literature to determine the most likely underlying mechanisms of ACL injuries. The hypothesis is that ACL injuries do not occur via solely sagittal, frontal or transverse plane mechanisms. 2. Search Strategy 2.1 Electronic Database Literature Search

Electronic database literature searches, including PubMed MEDLINE (1966–2008), CINAHL (1982–2008) and SportDiscus (1985–2008) with ª 2010 Adis Data Information BV. All rights reserved.

the subject term ‘anterior cruciate ligament’ were used for the review. The search was supplemented by a review of the bibliographies of retrieved articles, personal correspondence with authors of the retrieved articles and hand searching of pertinent journals to identify any additional studies addressing this topic of interest. These relatively liberal search criteria were used to identify all published relevant studies and to maximize the generalizability of this review. 2.2 Inclusionary and Exclusionary Criteria

Since the quality of a systematic review depends on the quality of studies appraised, reviewing Level I or II studies would provide the best evidence for answering our important clinical question about ACL injury mechanisms. However, it is unethical to attempt to incite ACL injury events in subjects in the laboratory and it is currently not feasible to design randomized Sports Med 2010; 40 (9)

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controlled trials that examine ACL injury mechanisms. Hence, this specific research question necessitated the inclusion of lower level evidence and a comprehensive evaluation of both basic and applied research examining probable mechanisms of ACL injury. Assimilation and integration of the results of such studies may provide important preliminary data and may identify areas of concentration for future research on ACL injury mechanisms and prevention methods. Thus, for this review, all levels of evidence for both basic and applied research were included if the studies met the required inclusionary and exclusionary criteria. Investigations were included in the review if the report identified ACL injury mechanisms, risk factors for ACL injury (prospectively or retrospectively) or knee biomechanics associated with ACL loading. However, only studies that were associated with ACL injury and provided evidence regarding a plane of injury were included in the final analysis. A study that directly observed or induced an ACL injury mechanism was defined as a direct ACL injury mechanism study. A study that evaluated the differences between in-

tact and ACL deficient conditions, described lesions or identified risk factors associated with ACL injury was defined as an indirect ACL injury mechanism study. Abstracts, unpublished data and published reports not written in English were excluded. Studies were also excluded from the analysis if the experiment was not conducted in humans or human specimens, did not examine planar loading or motion, did not contain original (i.e. review article) or empirical data, or contained only one specimen or subject (case report). In addition, studies that included subjects that had pathologies that may significantly alter knee biomechanics relative to the native (or deficient) conditions or that examined variables unrelated to ACL injury mechanisms were excluded from the analyses. For example, studies that examined reconstruction techniques, effects of bracing, effects of menstrual cycle or hormones, long-term outcomes of ACL injury, partial ACL tears or injuries resulting from vehicle accidents were excluded. Finally, studies with subject (or specimen) reported knee osteoarthritis or ACL deficiency without intact comparisons were excluded from the analyses.

Table I. Range of motion for all knee translations Translationa

Direction

Knee flexion ()

Applied force (N)

Sagittal plane

Anterior and posterior

0 20 45 90

100

Anterior Posterior

25 25

133 133

~6.9 ~5.2

Living subjects (20)

Used KT2000 to measure anterior-posterior translation and distinguishing between

7

Anterior

0 20 90 0 20 90

Manual maximum

~1.8 ~3.2 ~2.0 ~1.8 ~3.0 ~1.8

Cadaver (35); living subjects (49)

Manual maximum was not a specified force. The cadaveric and live subjects did not have a large difference in measurements

6

0 30 0 30

660–690 510–690 510–650 470–630

~4.5 ~5.0 ~4.5 ~5.0

Cadaver (2)

Small subject number and high forces that would not necessarily occur physiologically without some type of rotational component

8

Posterior

Frontal plane

Medial Lateral

a

Tibial displacement (mm) [mean] 2.0 [– 0.5] 4.8 [– 2.0] 3.9 [– 2.5] 2.9 [– 1.7]

Study type (n)

Comment

Reference

Cadaver (35)

6

Transverse plane: no data available.

mm = millimetre; n = no. of subjects; N = Newton; ~ indicates approximate; indicates degrees.


Sports Med 2010; 40 (9)


733

2.3 Independent Review and Analysis

Two independent reviewers performed firststage screening of titles and abstracts based on the study design and research question to identify all relevant articles. Any study identified by either reviewer was included in the first-stage screen. After the initial screening, a second-stage review was performed to identify which studies met the study criteria and for data extraction and analysis. If there was disagreement regarding study criteria or data extraction, a third reviewer was available to reconcile any differences of opinion. A quality appraisal of the literature was used to determine the strengths and weaknesses of the methodologies used to examine ACL injury mechanisms. Data analysis and results consisted of descriptive evaluations of each study, including the methodology, outcomes and the planar direction (if available) supported by the results for each study. 3. Results The initial literature search yielded 9861 total references; 639 articles met the minimum inclusion criteria. The articles retrieved varied by level of evidence, methodology, study population and outcomes. As expected, no randomized controlled trials were identified. Common methodological approaches used to study ACL injury mechanisms included athlete interviews or questionnaires, arthroscopic studies, clinical imaging and physical

exam testing, video analysis, in vivo laboratory tests (such as motion analysis or EMG) or mathematical modelling studies. The studies utilized either in vivo (human subjects) or in vitro (human cadaver) techniques. However, because of the unique differences between in vivo and in vitro techniques, we categorized cadaveric investigations as using a separate methodology, even though cadaveric studies often utilized similar methods such as imaging, motion analysis or arthroscopy to evaluate knee biomechanics. While 639 studies met the a priori established criteria, only 34 studies were associated with ‘direct’ ACL injury mechanisms and provided evidence regarding the planar mechanism of injury. The breakdown of studies addressing planar mechanisms of injury consisted of 16 interview/ questionnaire studies,[21-36] six video analysis studies[21,37-41] that reported a planar mechanism of injury, six modelling studies[42-47] and six cadaveric studies.[48-53] Twenty-eight of these 34 studies (82%) supported multi-planar mechanisms (table III). In addition to the studies related to direct ACL injury mechanisms, 164 studies were identified that looked at ACL injury mechanism ‘indirectly’ and provided evidence regarding possible planar injury mechanisms. A total of 80 of these 164 studies (49%) supported multi-planar mechanisms (table IV). Sixty-two of 132 (47%) diagnostic studies using imaging, arthroscopy, physical exam or instrumented laxity provided evidence to support multi-planar mechanisms (table IV). While 50 of

Table II. Range of motion for knee rotations in the frontal and transverse planes Rotation

Direction

Knee flexion ()

Applied force (Nm)

Laxity () [mean]

Study type (n)

Comment

Reference

Frontal plane

Adduction and abduction

0 10 20 45 90 135

~8

1.9 [– 1.7] 4.5 [– 1.9] 5.4 [– 2.1] 6.0 [– 2.4] 7.5 [– 2.8] 8.4 [– 3.1]

Cadaver (35)

Manual application of force to determine laxity

9

Transverse plane

Internal and external

0 10 20 45 90 135

~8

10.1 [– 4.0] 19.5 [– 4.9] 24.5 [– 4.9] 26.7 [– 5.8] 24.3 [– 4.7] 26.2 [– 7.2]

Cadaver (35)

Manual application of force to determine laxity

9

n = no. of subjects; Nm = Newton metres; ~ indicates approximate; indicates degrees.


Sports Med 2010; 40 (9)

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Table III. Planar evidence for studies directly associated with anterior cruciate ligament injury Study type

No. of studies with planar mechanism evidence

No. of studies that support multi-planar mechanisms

Other support

Cadaver

6

4

Sagittal = 1; frontal = 1

Modelling

6

3


Video

6

6

Interview/questionnaire

16

15

Sagittal = 1

Total

34

28


the 132 (38%) diagnostic studies provided evidence to support a sole sagittal plane mechanism, it is important to consider that most of these studies only evaluated anterior tibial translation and did not consider other planes in the diagnostic evaluation. Four of eight (50%) modelling studies and 13 of 23 (57%) cadaveric studies supported multiplanar mechanisms for ACL injury (table IV). Although many in vivo laboratory studies evaluated the effects of ACL deficiency on dynamic knee biomechanics, the complex neuromuscular compensation patterns that may occur as a result of injury made it difficult to interpret the planar conseqences of ACL deficiency. However, one prospective in vivo biomechanical/epidemiological laboratory study supported a multi-planar mechanism, as abnormal mechanics in all three planes during landing predicted ACL injury risk (table IV). 4. Discussion 4.1 Planar Biomechanics Surrounding the Inciting Anterior Cruciate Ligament Injury Event

The various methods used to study ACL injury mechanisms indicate that the ACL may be subject to high forces when under varying loading conditions. Based on this systematic analysis, we

accepted the hypothesis that ACL injuries do not occur via solely a sagittal, frontal or transverse plane mechanism. Table V summarizes the types, advantages and limitations of research methods used to study ACL injury mechanisms found in the studies identified through this review.[54] It is important to note that since it is well established that females have increased rates of ACL injury in similar sports compared with males, the ACL injury studies identified often focused on the determination of differences between the sexes that may increase the risk for injury in females. Sections 4.2–4.8 highlight some of the support and limitations for solely sagittal, frontal and transverse mechanisms of ACL injury compared with a multi-planar mechanistic view of ACL injury. 4.2 Evidence that Supports a Sagittal Plane Mechanism Theory

Many conventional and current theories support a sagittal plane mechanism of injury. A total of 32% of the studies identified supported a sole sagittal plane mechanism of injury. The knee has the largest range of motion in the sagittal plane compared with the frontal or transverse planes and more erect knee postures during landing are theorized to increase risk for ACL injury. Females have been reported to have less knee flexion during landing, jumping

Table IV. Planar evidence for studies indirectly associated with anterior cruciate ligament injury Study type

No. of studies with planar mechanism evidence

No. of studies that support multi-planar mechanisms

Other support Sagittal = 6; frontal = 4

Cadaver

23

13

Modelling

8

4

132

62

1

1

164

80

Diagnostic In vivo laboratory Total


Sagittal = 4 Sagittal = 50; frontal = 11; transverse = 9 Sagittal = 60; frontal = 17; transverse = 9

Sports Med 2010; 40 (9)

Examples

Advantages

Limitations

Applications in ACL research

References

In vivo

Observational: questionnaires, videos, interviews

Direct observation or description of injury mechanism

Cannot determine internal structure stresses/strains Questionnaire/interview: subjective and dependent on athletes ability to recall event Video: limited by quality of video, camera angles available and observer’s ability to describe event

Description of inciting event (contact or non-contact, type of sporting activity), gross position of knee, trunk, lower extremity during injury

2,21,25,27,55,56

Clinical: arthroscopic, imaging, physical exam

Identify lesions associated with injury, strain gauges on internal joint structures, analyse anatomic restraints Functional-dynamic imaging such as MRI or roentgen stereogrammetric analysis techniques offer enhanced ability to visualize internal structures during dynamic weight-bearing activities Accuracy, precision, reliability of data acquisition continues to improve

Do not directly analyse injury mechanism Post-injury pathology and associated biomechanical effects may not be reliable indicators of actual injury mechanisms Arthroscopic: not ethical for healthy subjects, may affect proprioception or cause joint impingement, expensive Imaging: possible radiation exposure, expensive Physical exam: often subjective and highly variable differences between subjects

Strain gauges placed on ACL during arthroscopy provide information about ACL strains during external loads Bone bruise locations may provide evidence for injury mechanisms Posterior tibial slope calculated from images may be associated with ACL injury Lachman’s, pivot shift, knee arthrometer data provide evidence of biomechanical effects of ACL deficiency Functional dynamic images help identify osteokinematics and ACL changes that occur during weight-bearing tasks

57,58

Laboratory: motion analysis, electromyography

Mimic specific movements that occur during injury Estimate both kinematics and net kinetics at joint during high risk movements Coupled

Do not replicate actual injury, rather estimate total joint biomechanics during high risk movements Difficult to reproduce or even approximate the strains and stresses that occur in internal joint structures

Identify sex differences in landing/cutting mechanics that may be associated with ACL injury Identify biomechanical/ neuromuscular variables

9,59-68

Continued next page

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Sports Med 2010; 40 (9)

Data collection method



Table V. Summary of research methods used to study anterior cruciate ligament (ACL) injury mechanisms (reproduced from Quatman et al.,[54] with permission from BMJ publishing group)

Data collection method

Examples

736


Table V. Contd Advantages

Limitations

Applications in ACL research

biomechanical/epidemiological studies provide predictive tools about injury risk factors (allows for both correlation and prediction of musculoskeletal injury)

(ligaments, cartilage, bones) Unethical to try to produce injury in laboratory

associated with ACL injury

References

Robotic, quasi-static, dynamic

Identify passive biomechanical characteristics of joint motions Direct injury studies possible Quantify multiple degree of freedom kinematics of joints Measure ligament and joint articulation contact forces

Age of specimens (may differ significantly from the population of interest) Difficult to reproduce dynamic joint motions and neuromuscular contributions to motion during injury conditions Expensive and injury studies often require a large number of specimens to reproduce injury mechanisms Orientation of loading, rate of loading and age of specimen may have significant effects on musculoskeletal failure loads

ACL strains and biomechanical parameters during different external loading parameters provide evidence of how ACL injuries may occur Cadaveric ACL injury may occur during anterior tibial shear, abduction, knee hyperextension and many combined loads Biomechanical consequences of ACL deficiency

48-53,69-76

In silico

Phenomenological, anatomic, rigid, finite element, quasi-static, dynamic, stochastic, inverse simulation, forward simulation

Estimate internal joint biomechanics In vivo biomechanical data can be used as input for geometric models to analyse movements Can be used to extend motion analysis data to relate ground reaction forces and kinematics to ligament, cartilage and bone forces Can be used to simulate injury mechanisms Parametric/sensitivity studies possible Relatively inexpensive if equipment is readily available Accuracy, precision, reliability of data acquisition continues to improve

Due to complexity of joints, models are simplified Certain assumptions are necessary about material properties, boundary conditions and anatomy Models must be validated (ideally by in vivo and in vitro data), which can be difficult without adequate material property characteristics available for the population of interest Not currently possible to validate high loading rate/injury simulations

ACL injury simulations for various tasks Identification of possible strategies to lower ACL injury risk Extension of coupled biomechanical/epidemiological motion analysis data to relate ground reaction forces and external loading conditions to ACL strains

44,45,77-85

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In vitro


and cutting tasks compared with males. In addition, interview and video observational studies indicate that the knee is at low (0–30) knee flexion angles during injury events.[21,25,29,37,39,41] Sagittal plane translation movements are also important to consider, since the ACL is a major stabilizing ligament of the knee that provides approximately 85% of the total restraint in the knee joint to the anterior tibial translation.[6,86] Many cadaveric, imaging and physical exam studies demonstrate that ACL-deficient knees have significantly more anterior tibial translation compared with ACL-intact conditions.[9,59] Both in vivo and in vitro studies demonstrate that the total range for anterior/posterior tibial displacement is greater at 30 than 90 of knee flexion, which indicates that the knee joint has the potential to translate further anteriorly at shallow knee flexion angles.[59,87] During sagittal plane movements at the knee joint, the quadriceps muscle contractions produce anterior shear force at the proximal end of the tibia through the patellar tendon.[48,88] Proximal tibia anterior shear is the most direct ACL loading mechanism and decreasing knee flexion angles increases the anterior shear force at the tibia.[89,90] Since video studies indicate that ACL injuries usually occur at low flexion angles, it is theorized that a powerful quadriceps force at low knee flexion angles could produce enough anterior shear force at the tibia to cause ACL rupture.[88,90-92] Correspondingly, several studies support anterior tibial shear as a mechanism for ACL injury. MRI studies after ACL injury demonstrate that tibial bone bruises are located more posteriorly than femoral condylar bone bruises and it has been speculated that this is a result of the tibia shifting anteriorly relative to the femur during the injury.[93,94] In vivo arthroscopic studies demonstrate that the ACL is a primary restraint to anterior shear loading and abnormal anterior tibial translation relative to the femur is a clinical measure used to determine ACL deficiency.[60,95] The relationships between high ACL strains, low knee flexion angles and quadriceps muscle forces have been extensively examined.[69,92,96-98] The landing phase of many sports movements are associated with large quadriceps forces at relaª 2010 Adis Data Information BV. All rights reserved.

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tively small knee flexion angles, which induce anterior force on the tibia.[98] Cadaveric investigations have demonstrated that isolated quadriceps contractions increase ACL strain and force during low knee flexion angles.[69,98] Studies by DeMorat et al. and Pandy and Shelburne indicated that aggressive quadriceps loading in slight knee flexion produce significant anterior tibial translation sufficiently large enough to injure the ACL.[48,88] Withrow et al. showed that during a high impact load, ACL strain is proportional to increased quadriceps forces.[70] In an arthroscopic study, Fleming et al. found that quadriceps contractions produced ACL strains between 0 and 30 of knee flexion.[95] At the same time, several motion analysis and EMG studies showed that females have more knee extension during landing compared with males, and that females have significant neuromuscular imbalances between quadriceps and hamstrings recruitment levels, making it more difficult to decelerate from a landing and control anterior tibial translation.[99-103] 4.3 Evidence Against a Sole Sagittal Plane Mechanism Theory

Although, theoretically, many of the studies identified support a sagittal plane mechanism, several limitations to these studies should be considered. In combination, these limitations provide a strong argument against single plane mechanisms of injury and subsequently underscore the likelihood of a more multi-planar mechanism of injury. For example, theoretically, if the mechanism was solely an anterior shear, the bone bruise patterns on MRI after ACL injury would most likely be located along the medial tibial plateau as well as the tibial plateau. Since the bone bruises are usually located laterally, lateral compression or internal/external tibial rotation of the joint also likely occurred during these injuries. Moreover, while some motion analysis studies suggest that females show greater knee extension during landing, other studies show no sex difference or even greater knee flexion in females during athletic tasks.[104-106] Video analyses of ACL injuries indicate that females may actually have a higher knee flexion angle compared with males during the Sports Med 2010; 40 (9)

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injury event.[39] Furthermore, knee flexion angle does not appear to predict ACL injury risk.[107] Cadaveric studies also indicate that hamstrings co-contraction with quadriceps contraction is effective in reducing excessive forces in the ACL, specifically between 15 and 60 of knee flexion.[92] At the same time, during landing, ACL strains are higher under multi-planar loading conditions compared with isolated anterior tibial loading situations, making it easier to damage the ACL under combined planar situations.[90] DeMorat et al. found that a quadriceps contraction appeared to affect ACL loading in more than one plane of motion, as knee internal rotation and valgus moments to the tibia occurred coincident with anterior tibial translation.[48] Mathematical models indicate that large ground reaction forces posteriorly directed with respect to the proximal tibia help protect the ACL during landing and posterior deceleration forces and reduce ACL strain during a run-to-stop simulation.[108] Moreover, hamstrings co-contraction can lead to joint compression and decreased anterior tibial translation.[109,110] Several mathematical models have demonstrated that sagittal plane mechanisms alone cannot account for ACL forces high enough to rupture the ACL.[45,111,112] Therefore, it is highly unlikely that ACL injuries result exclusively from a sagittal plane mechanism. 4.4 Evidence that Supports a Frontal Plane Mechanism Theory

The frontal plane theory mechanism has become a recent topic of debate as a contributing factor to ACL injuries. Approximately 10% of the studies identified supported a sole frontal plane mechanism and over 80% of the studies identified supported frontal plane mechanisms (specifically abduction motions) as a contributor to a multiplanar mechanism of injury. Based upon the studies identified, frontal plane motions are often associated with ACL injuries and excessive movements in the frontal plane outside normal ranges may be catastrophic to the knee joint. Ligament restraints and knee joint articulation limit the passive range of knee motion in the frontal plane, which results in a smaller range of moª 2010 Adis Data Information BV. All rights reserved.

tion in the frontal plane compared with the sagittal plane. It is difficult to accurately measure mediallateral translations of the knee since the translations that can occur in a healthy knee are limited. Cadaveric studies and in vivo studies have demonstrated that the frontal plane rotational range of motion is also relatively limited.[6] Shultz et al. demonstrated in vivo that a 10 Newton (N) metres (abduction/ adduction) load at 20 of knee flexion produced approximately 10 total knee rotation in the frontal plane (abduction ~5.5; adduction ~4.5).[7] Markolf et al. and Miyaska et al. demonstrated that cadaveric specimens subjected to adduction torque show increases in ACL tension throughout a range of knee flexion angles (0–90) with the highest between 0 and 30 of knee flexion.[71,90] Similarly, Wascher et al. and Markolf et al. demonstrated that adduction moments lead to high ACL forces particularly near full knee extension.[72,113] Arthroscopic studies indicate that the ACL strain increases under adduction moments during weight-bearing conditions.[95] While adduction motions of the knee do appear to increase the tension and strain in the ACL, few observational studies attribute this type of motion to ACL injuries.[21,39] Video analyses of ACL injuries during sports indicate a common body posture during injury in which the knee is near full extension (between 0 and 30), the tibia is externally rotated, the foot is planted and a deceleration followed by an abduction collapse of the knee joint occurs.[21,39] Olsen et al. found that dynamic abduction collapse was the most common mechanism for ACL injury in handball.[41] Similarly, Krosshaug et al. found that dynamic abduction collapse was a common ACL injury mechanism with female basketball players demonstrating a 5.3-fold higher relative risk of abduction collapse during ACL injury compared with male basketball players.[39] At the same time, motion analysis studies indicate that high knee abduction motion and torque are both common sex differences during athletic movements and predictors of future ACL injury risk.[64,65,67,68,101,104,107,114] Clinical imaging and arthroscopic studies also indicate that frontal plane mechanisms play a role in ACL injury. Bone bruises of the lateral Sports Med 2010; 40 (9)


femoral condyle or posterolateral portions of the tibial plateau are found to occur 80% of the time in MRI studies after acute ACL injury.[93,94,115,116] It is theorized that these bone bruise locations indicate that ACL injury occurs from an abduction mechanism, because bone bruising on the lateral part of the knee joint indicates that compression occurs laterally while the medial aspect of the joint opens up. In addition, arthroscopic studies indicate that abduction knee moments applied during weight-bearing conditions significantly increase relative ACL strain.[95] Several cadaveric studies have demonstrated that the ACL may have increased force during abduction loads.[72,90,113] Markolf et al. demonstrated that a quadriceps force (200 N) applied in combination with an abduction load increased the ACL force up to 100% compared with abduction loads without a quadriceps force.[90] Withrow et al. demonstrated that cadavers subjected to impulsive compression loads with the knee joint in an abduction alignment led to 30% higher ACL strains compared with knees in neutral alignment.[73] Modelling studies have also shown support for an abduction injury mechanism. McLean et al. utilized motion analysis and mathematical modelling to simulate injury and showed that external abduction loads reach values high enough to rupture the ACL during cutting manoeuvres and these abduction loads occurred more frequently in females than males.[45] Another forward dynamics model that was used to simulate ACL injuries during an abduction mechanism demonstrated that perturbations to the lower extremity during a side-step cutting manoeuvre can lead to external abduction loads that are capable of rupturing the ACL.[44] 4.5 Evidence Against a Sole Frontal Plane Mechanism Theory

Although increased lower extremity abduction loads and movements in the frontal plane may be associated with increased ACL strain and risk of injury, controversy surrounds this theory. The ACL is considered the primary restraint to anterior tibial translation during passive physical ª 2010 Adis Data Information BV. All rights reserved.

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exam testing, while the medial collateral ligament (MCL) is considered the primary restraint against abduction stress in the knee joint. Therefore, the abduction motion and torque at the knee joint associated with increased ACL injury risk is surprising to clinicians, since it is estimated that combined ACL/MCL injuries make up only 4–27% of all ACL injuries.[1,117] If ACL injuries occur due to movements solely in the frontal plane, higher combined ACL/MCL injury patterns would be expected. Cadaveric studies indicate that the ACL and MCL may both provide restraint to external abduction, albeit via different mechanisms. The ACL appears to prevent knee abduction by limitation of axial tibial rotation, while the MCL restrains knee abduction by limiting medial joint space opening. Thus, both the MCL and ACL are important structures for restraint of abduction loads and either one may potentially be injured during high knee abduction loading.[74] Cadaveric ACL failure loads are reported to range from approximately 640–2100 N, depending upon the age of the specimen, rate and orientation of loading.[75] Cadaveric MCL failure loads have been reported to be around 2300 N for complete MCL disruption.[118] While higher reported MCL failure loads compared with the ACL may help explain how and why the ACL may fail earlier than the MCL during external abduction loading, there are currently no reported studies to support or refute this theory. Few studies have examined ACL and MCL loading simultaneously during an abduction load. Because of the variability in laxity between specimens and different testing conditions and setups, cross referencing of studies to determine how the ACL and MCL simultaneously behave during abduction is difficult. Another limitation to the frontal plane theory is the non-descript term of ‘valgus’ used in previous studies to describe what occurs during an ACL injury. The medical definition of valgus refers to the outward angulation of the distal segment of a bone or joint. However, at the knee joint, valgus may occur from a direct abduction motion of the knee joint or from transverse-plane knee rotation motions (femoral/tibial internal Sports Med 2010; 40 (9)

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and external rotations). Thus, describing an injury mechanism as a valgus collapse does not necessarily indicate that the injury occurred solely in the frontal plane. 4.6 Evidence in Support of a Transverse Plane Mechanism Theory

Although only 5% of the studies supported a sole transverse plane mechanism, many of the studies neglected to assess the transverse rotations during experimental procedures. Thus, the transverse plane contributions to ACL injury mechanisms may be significantly underestimated. Similar to the frontal plane, transverse plane ranges of motion (rotational and translational) are not as large as sagittal plane motions and difficult to assess experimentally. Compression is the most common translation that occurs during cutting and landing activities, and could be a direct result of impact (ground reaction) forces, an indirect result from muscular stabilization or, most likely, a combination of both effects. As evidenced by the common association of bone bruises accompanying ACL injuries, compression is a likely component of the ACL injury event. The total passive range of rotation (internal and external) in the transverse plane is approximately 25, depending on the knee flexion angle.[6] Numerous studies have reported that the ACL experiences higher strains during internal tibial rotation, while only minimal increases in strains during external rotation have been noted.[71,90,113] Cadaveric studies by Meyer et al. demonstrated that high compressive or internal torsional tibial loads can cause ACL damage with limited damage to other knee ligaments.[50] Similarly, Markolf et al. demonstrated that an internal tibial torque generates significantly higher ACL forces than application of a 100 N anterior tibial force during shallow knee flexion angles.[90] In contrast, external tibial torques applied to cadaveric knees demonstrated little differences in ACL strain and tension over a wide range of flexion angles.[90] Snow skiing results in a high rate of ACL injury. A common mechanism described during snow skiing ACL injuries is internal tibial rotation or a combination of high axial loading with ª 2010 Adis Data Information BV. All rights reserved.

transverse plane rotations.[27] However, comparisons between ACL injuries that result from snow skiing and ACL injuries that occur during sports that involve cutting, jumping and landing activities are questionable. Skiers have different movement mechanics, since their feet are fixed in ski bindings and they have the added extensions of the skis, which may increase the surface area for applying external multi-planar loads to the distal end of the lower extremity. A recent imaging study by Stijak et al. found that ACL-injured patients have greater posterior lateral tibial plateau slopes compared with controls.[61] In addition, the lateral femoral condyle has greater translation on the tibia compared with the medial condyle as the flexion angle increases.[119] As the knee goes into deeper flexion, the lateral femoral condyle internally rotates relative to the tibial plateau, while the medial femoral condyle remains relatively stable.[119] Therefore, a greater posterior tibial slope may lead to greater external rotation of the femur or internal rotation of the tibia during activities and may increase an individual’s risk for ACL injury. 4.7 Evidence Against of a Sole Transverse Plane Mechanism Theory

Theoretically, the cushioning provided by the menisci and articular cartilage aids in reduction of the compressive forces and minimization of the compression that occurs during landing and cutting activities. Moreover, it is unlikely that compression without movements in other degrees of freedom could cause injury to the ACL, since ligaments are minimally stressed in compression. It is possible to rupture the ACL in vitro in distraction.[75] However, the intra-articular orientation of the ACL and its variable fibre lengths makes uniform loading of the ACL during tension difficult. Thus, the likelihood of a complete midsubstance ACL rupture is low with pure distractive loads applied along the axis of the tibia.[75] In addition, the compressive knee joint forces resulting from muscle activation during weightbearing activities would counter any distractive forces that may occur during landing and cutting activities. Sports Med 2010; 40 (9)


In addition, given the strong support for internal tibial rotations being more likely to injure the ACL than external rotations, observational studies that described an external tibial rotation during injury seem counterintuitive and contradictory.[39] Arthroscopic data indicate that during non-weight-bearing conditions, internal tibial torque significantly increases ACL strain while external tibial torques produce minimal strain in the ACL.[95] However, arthroscopic data show that weight-bearing conditions can significantly increase the ACL strain during both internal and external torques. In particular, external torques (0–10 nm) increased the ACL strain during weight-bearing conditions by 2–4% compared with non-weight-bearing conditions.[95] Since most ACL injuries occur during weightbearing conditions, it may be feasible that an external rotation torque could potentially damage the ACL. However, an alternative combined multi-planar loading mechanism may include an externally rotated foot or ski, coupled with foot hyper-pronation and tibial internal rotation and knee abduction, which would lead to high loads on the ligament. 4.8 Multi-Planar Mechanism

Many studies indicate that the knee may experience high loading conditions in any plane. In particular, high loading conditions can occur in sporting manoeuvres, such as landing, jumping and cutting, all of which require movements in multiple planes. Thus, it is unlikely that an ACL injury occurs in a single isolated plane. In support of this concept, 82% of the direct ACL injury mechanism studies identified supported a multi-planar mechanism of injury. This is in corroboration with Shimokochi and Shultz, who systematically reviewed the retrospective and observational studies available in the literature that assessed ACL injury mechanisms and found that the primary mechanism of ACL injury appears to be a result of multi-planar knee loading conditions.[120] Physical examination techniques are forensic in that they may reproduce the increased luxations that occurred during the inciting injury. The pivot shift test is one such clinical exam, which is ª 2010 Adis Data Information BV. All rights reserved.

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performed by a valgus (knee abduction) stress coupled with flexion and tibial rotation. As such, it is likely reproducing the original mechanism of injury. The pivot shift is a highly sensitive test for ACL insufficiency. Benjaminse and Gokeler reported the pivot shift exam to be the most specific clinical test for ACL rupture, demonstrating a 98% specificity (95% CI 96, 99).[121] It is also a sensitive predictor of future poor conservative outcomes following injury.[122] Cumulatively, these data demonstrate that knee abduction motion may be an important component of the ACL injury mechanism. In retrospective interview studies, individuals often reported that their knee moved in multiple planes during the injury event. Specifically, a ‘valgus’ rotation combined with either an internal or external tibial rotation at low knee flexion angles was reported by injured individuals. Similarly, video studies indicate that ACL injuries occur with minimal knee flexion and are often combined with knee ‘valgus’ or transverse knee rotation movements.[21,39,41] This is supported by the bone bruise patterns associated with ACL injuries on imaging studies, with the bone bruises located on the lateral femoral condyles and posterolateral tibial plateaus of patients with acute ACL injured knees. This bruise pattern indicates that internal tibial rotation, femoral external rotation, abduction and/or anterior tibial translation would lead to these specific bone bruise locations. While few in vivo arthroscopic studies have examined combined planar loading, Fleming et al. noted that weight bearing, which resulted in compressive forces across the joint, altered the strain results in the ACL for various loading conditions.[95] ACL strains were higher when an anterior shear force was applied to the tibia during weight-bearing conditions compared with non-weight bearing, and the weight-bearing effect was shear-load dependent. Strains in the ACL were torque dependent for internal and external rotation torques, with weight bearing leading to significantly higher strains than non-weightbearing conditions. Similarly, weight bearing led to significantly higher strains in the ACL during abduction/adduction loading compared with non-weight-bearing conditions.[95] While all of Sports Med 2010; 40 (9)

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these outcomes indicate the ACL can be subjected to high loading strains in all planes in weight bearing, combined loading of anterior shear, abduction/adduction and internal/external torques were not examined. Consequently, it is difficult to surmise the combined effects of multiplanar loading on ACL strain from the study. Cadaveric investigations show that valgus or varus moments, combined with a quadriceps contraction or anterior shear force, increases ACL strain. Markolf et al. and Berns et al. demonstrated that coupled loading of an abduction moment to an anterior tibial force (at a knee flexion greater than 10) or coupled loading of an anterior tibial force with an internal tibial torque (at knee flexion less than 20) leads to additive generation of ACL force and strain compared with an isolated anterior tibial force.[76,90] In contrast, coupled external tibial torque and anterior tibial force appears to lower the ACL tensile force after 20 of knee flexion. As such, the ACL may be less vulnerable to injury, since the MCL could be shielding the ACL from stress in this knee position.[90] Motion analysis studies have indicated that various multi-planar motions may increase risk for ACL injury in female athletes. Hewett et al. showed that subjects who subsequently went on to ACL injury after biomechanical testing had larger abduction angles at initial contact and at peak abduction in the frontal plane and significantly lower knee flexion at peak contact in the sagittal plane.[107] In addition, various sex differences in landing mechanics have been identified in multiple planes and have been speculated as possible risk factors for ACL injury. Modelling studies have provided some unique perspectives on the effects of multi-planar loading. Fung and Zhang developed 3-dimensional models of knees to examine factors that could lead to ACL impingement on the intercondylar notch of the femur.[123] Simulation of the physical interaction between the ACL and the notch during six-degrees of freedom tibiofemoral motions showed that abduction and external tibial rotation can lead to ACL impingement. McLean et al. reported that neuromuscular control perturbation produced peak stance phase knee abduction loads large enough to cause ACL injury, and ª 2010 Adis Data Information BV. All rights reserved.

landing in a more extended knee flexion angle increased this risk for injury.[44] Although the current literature is limited for the evaluation of multi-planar loading effects on knee biomechanics and, specifically, ACL stresses and strains, future modelling work may provide the opportunity to extend motion analysis data to predict stresses and strains in the internal joint structures, simulate injury scenarios, and conduct parametric studies evaluating the effects of isolated and multi-planar loading scenarios without inter-subject variability that occurs during cadaveric and in vivo investigations. 4.9 Kinetic Chain Involvement

Finally, while the ACL injury is a direct result of what occurs at the knee joint, it is important to consider the contribution of the entire kinetic chain to knee joint loading. Motion and forces at any segment of the kinetic chain (foot, ankle, hip, trunk and upper extremities) may influence knee joint mechanics. There is increasing evidence that poor or abnormal neuromuscular control of the lower limb during athletic movements, especially at the knee joint, contributes to ACL injury risk. Future work should establish the effects of proximal and distal structures on knee joint biomechanics and how they relate to ACL injury. 5. Conclusions The methodological approaches that have been utilized to investigate ACL injury mechanisms include athlete interviews, arthroscopic studies, clinical visits, video analysis, cadaveric studies, in vivo laboratory studies and mathematical modelling studies. Although none of these methodologies alone can provide strong answers to the question of what the underlying mechanisms are for ACL injuries, all of these data considered together provide important clues to ACL injury mechanisms. When the data from the published literature that relates to mechanisms of ACL injury are summarized and considered in toto, ACL injuries are more likely to occur during multiplanar rather than single-planar mechanisms of injury. Therefore, based on this systematic analysis, Sports Med 2010; 40 (9)


we accepted the hypothesis that ACL injuries likely do not occur solely via a sagittal, frontal or transverse plane mechanism. One important clinical implication for the acceptance of this hypothesis is that ACL prevention programmes that neglect multi-planar mechanisms, such as combined frontal, sagittal and transverse plane mechanisms, could seriously hamper ACL injury prevention efforts in healthy athletes and athletes returning to sport after a previous ACL injury. Future studies should focus on the examination of the precise mechanisms of combined knee joint loading scenarios to determine at-risk knee postures that may be addressed with neuromuscular training programmes targeted for ACL injury prevention. Acknowledgements The authors acknowledge funding support from the University of Toledo, College of Medicine Pre-Doctoral Fellowship, the American College of Sports Medicine Foundation, Plus One Active Research Grant on Wellness Using Internet Technology, and the National Institutes of Health Grants R01-AR049735, RO1-AR05563 and R01-AR056259. The authors thank Vijay Goel, Dean Demetropoulos, Kevin Ford, Keith Kenter and Greg Myer for their discussions about the topic covered in this review. The authors have no conflicts of interest that are directly relevant to the content of this review.

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9.

10.

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12.

13.

14. 15.

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17.

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76. Berns GS, Hull ML, Patterson HA. Strain in the anteromedial bundle of the anterior cruciate ligament under combination loading. J Orthop Res 1992; 10 (2): 167-76 77. Gardiner JC, Weiss JA. Subject-specific finite element analysis of the human medical collateral ligament during valgus knee loading. J Orthop Res 2003; 21 (6): 1098-106 78. Moglo KE, Shirazi-Adl A. On the coupling between anterior and posterior cruciate ligaments, and knee joint response under anterior femoral drawer in flexion: a finite element study. Clin Biomech (Bristol, Avon) 2003; 18 (8): 751-9 79. Pena E, Calvo B, Martinez MA, et al. A three-dimensional finite element analysis of the combined behavior of ligaments and menisci in the healthy human knee joint. J Biomech 2006; 39 (9): 1686-701 80. Beillas P, Papaioannou G, Tashman S, et al. A new method to investigate in vivo knee behavior using a finite element model of the lower limb. J Biomech 2004; 37 (7): 1019-30 81. Blankevoort L, Huiskes R, de Lange A. Recruitment of knee joint ligaments. J Biomech Eng 1991; 113 (1): 94-103 82. Li G, Gil J, Kanamori A, et al. A validated three-dimensional computational model of a human knee joint. J Biomech Eng 1999; 121 (6): 657-62 83. Donahue TL, Hull ML, Rashid MM, et al. A finite element model of the human knee joint for the study of tibiofemoral contact. J Biomech Eng 2002; 124 (3): 273-80 84. Hirokawa S, Tsuruno R. Three-dimensional deformation and stress distribution in an analytical/computational model of the anterior cruciate ligament. J Biomech 2000; 33 (9): 1069-77 85. Gardiner JC, Weiss JA, Rosenberg TD. Strain in the human medial collateral ligament during valgus loading of the knee. Clin Orthop Relat Res 2001; (391): 266-74 86. Butler DL, Noyes FR, Grood ES. Ligamentous restraints to anterior-posterior drawer in the human knee: a biomechanical study. J Bone Joint Surg Am 1980; 62 (2): 259-70 87. Fukubayashi T, Torzilli PA, Sherman MF, et al. An in vitro biomechanical evaluation of anterior-posterior motion of the knee: tibial displacement, rotation, and torque. J Bone Joint Surg Am 1982; 64 (2): 258-64 88. Pandy MG, Shelburne KB. Dependence of cruciate-ligament loading on muscle forces and external load. J Biomech 1997; 30 (10): 1015-24 89. Sell TC, Ferris CM, Abt JP, et al. Predictors of proximal tibia anterior shear force during a vertical stop-jump. J Orthop Res 2007; 25 (12): 1589-97 90. Markolf KL, Burchfield DM, Shapiro MM, et al. Combined knee loading states that generate high anterior cruciate ligament forces. J Orthop Res 1995; 13 (6): 930-5 91. Yu B, Lin CF, Garrett WE. Lower extremity biomechanics during the landing of a stop-jump task. Clin Biomech (Bristol, Avon) 2006; 21 (3): 297-305 92. Li G, Rudy TW, Sakane M, et al. The importance of quadriceps and hamstring muscle loading on knee kinematics and in-situ forces in the ACL. J Biomech 1999; 32 (4): 395-400 93. Speer KP, Spritzer CE, Bassett 3rd FH, et al. Osseous injury associated with acute tears of the anterior cruciate ligament. Am J Sports Med 1992; 20 (4): 382-9

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94. Mink JH, Deutsch AL. Occult cartilage and bone injuries of the knee: detection, classification, and assessment with MR imaging. Radiology 1989; 170 (3 Pt 1): 823-9 95. Fleming BC, Renstrom PA, Beynnon BD, et al. The effect of weightbearing and external loading on anterior cruicate ligament strain. J Biomech 2001; 34: 163-70 96. Beynnon BD, Fleming BC, Johnson RJ, et al. Anterior cruciate ligament strain behavior during rehabilitation exercises in vivo. Am J Sports Med 1995; 23 (1): 24-34 97. Beynnon BD, Johnson RJ, Fleming BC, et al. The strain behavior of the anterior cruciate ligament during squatting and active flexion-extension: a comparison of an open and a closed kinetic chain exercise. Am J Sports Med 1997; 25 (6): 823-9 98. Durselen L, Claes L, Kiefer H. The influence of muscle forces and external loads on cruciate ligament strain. Am J Sports Med 1995; 23 (1): 129-36 99. Chappell JD, Yu B, Kirkendall DT, et al. A comparison of knee kinetics between male and female recreational athletes in stop-jump tasks. Am J Sports Med 2002; 30 (2): 261-7 100. Chappell JD, Creighton RA, Giuliani C, et al. Kinematics and electromyography of landing preparation in vertical stop-jump: risks for noncontact anterior cruciate ligament injury. Am J Sports Med 2007; 35 (2): 235-41 101. Malinzak RA, Colby SM, Kirkendall DT, et al. A comparison of knee joint motion patterns between men and women in selected athletic tasks. Clin Biomech 2001; 16 (5): 438-45 102. Hewett TE, Stroupe AL, Nance TA, et al. Plyometric training in female athletes: decreased impact forces and increased hamstring torques. Am J Sports Med 1996; 24 (6): 765-73 103. White KK, Lee SS, Cutuk A, et al. EMG power spectra of intercollegiate athletes and anterior cruciate ligament injury risk in females. Med Sci Sports Exerc 2003; 35 (3): 371-6 104. Ford KR, Myer GD, Toms HE, et al. Gender differences in the kinematics of unanticipated cutting in young athletes. Med Sci Sports 2005; 37 (1): 124-9 105. Fagenbaum R, Darling WG. Jump landing strategies in male and female college athletes and the implications of such strategies for anterior cruciate ligament injury. Am J Sports Med 2003; 31 (2): 233-40 106. Pollard CD, Davis IM, Hamill J. Influence of gender on hip and knee mechanics during a randomly cued cutting maneuver. Clin Biomech 2004; 19 (10): 1022-31 107. Hewett TE, Myer GD, Ford KR, et al. Biomechanical measures of neuromuscular control and valgus loading of the knee predict anterior cruciate ligament injury risk in female athletes: a prospective study. Am J Sports Med 2005; 33 (4): 492-501 108. Shin CS, Chaudhari AM, Andriacchi TP. The influence of deceleration forces on ACL strain during single-leg landing: a simulation study. J Biomech 2007; 40 (5): 1145-52 109. Imran A, O’Connor JJ. Theoretical estimates of cruciate ligament forces: effects of tibial surface geometry and ligament orientations. Proc Inst Mech Eng [H] 1997; 211 (6): 425-39


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Correspondence: Dr Timothy E. Hewett, PhD, Cincinnati Children’s Hospital, 3333 Burnet Avenue, MLC 10001, Cincinnati, OH 45229, USA. E-mail: [email protected]; [email protected]

Sports Med 2010; 40 (9)

Sports Med 2010; 40 (9): 747-763 0112-1642/10/0009-0747/$49.95/0

REVIEW ARTICLE


Carbohydrate Administration and Exercise Performance What Are the Potential Mechanisms Involved? Antony D. Karelis,1 JohnEric W. Smith,2 Dennis H. Passe3 and Francois Pe´ronnet4 1 2 3 4

Department of Kinesiology, Universite´ du Que´bec a` Montreál, Montreal, Quebec, Canada Gatorade Sports Science Institute, Barrington, Illinois, USA Scout Consulting, LLC, Hebron, Illinois, USA Department of Kinesiology, Universite´ de Montreál, Montreal, Quebec, Canada

Contents Abstract. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Carbohydrate (CHO) Administration and Central Fatigue during Exercise . . . . . . . . . . . . . . . . . . . . . . 1.1 Central Fatigue and Tryptophan . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2 Hypoglycaemia and Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.3 Cognition and Performance. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.4 Mouth Rinsing with CHO and Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Blood Glucose Oxidation and CHO Administration during Exercise: Effect on Performance . . . . . . . 3. Effects of CHO Administration on Muscle Glycogen Metabolism during Exercise. . . . . . . . . . . . . . . . . 4. Effects of CHO Administration on Muscle Metabolite Levels during Exercise. . . . . . . . . . . . . . . . . . . . . 5. Exercise-Induced Strain: Effect of CHO Ingestion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6. CHO Administration and Excitation-Contraction Coupling during Exercise. . . . . . . . . . . . . . . . . . . . . . 7. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Abstract

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It is well established that carbohydrate (CHO) administration increases performance during prolonged exercise in humans and animals. The mechanism(s), which could mediate the improvement in exercise performance associated with CHO administration, however, remain(s) unclear. This review focuses on possible underlying mechanisms that could explain the increase in exercise performance observed with the administration of CHO during prolonged muscle contractions in humans and animals. The beneficial effect of CHO ingestion on performance during prolonged exercise could be due to several factors including (i) an attenuation in central fatigue; (ii) a better maintenance of CHO oxidation rates; (iii) muscle glycogen sparing; (iv) changes in muscle metabolite levels; (v) reduced exercise-induced strain; and (vi) a better maintenance of excitation-contraction coupling. In general, the literature indicates that CHO ingestion during exercise does not reduce the utilization of muscle glycogen. In addition, data from a meta-analysis suggest that a dose-dependent relationship was not shown between CHO ingestion during exercise and an increase in performance. This could support the idea that providing enough CHO to maintain CHO oxidation during exercise may

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not always be associated with an increase in performance. Emerging evidence from the literature shows that increasing neural drive and attenuating central fatigue may play an important role in increasing performance during exercise with CHO supplementation. In addition, CHO administration during exercise appears to provide protection from disrupted cell homeostasis/integrity, which could translate into better muscle function and an increase in performance. Finally, it appears that during prolonged exercise when the ability of metabolism to match energy demand is exceeded, adjustments seem to be made in the activity of the Na+/K+ pump. Therefore, muscle fatigue could be acting as a protective mechanism during prolonged contractions. This could be alleviated when CHO is administered resulting in the better maintenance of the electrical properties of the muscle fibre membrane. The mechanism(s) by which CHO administration increases performance during prolonged exercise is(are) complex, likely involving multiple factors acting at numerous cellular sites. In addition, due to the large variation in types of exercise, durations, intensities, feeding schedules and CHO types it is difficult to assess if the mechanism(s) that could explain the increase in performance with CHO administration during exercise is(are) similar in different situations. Experiments concerning the identification of potential mechanism(s) by which performance is increased with CHO administration during exercise will add to our understanding of the mechanism(s) of muscle/central fatigue. This knowledge could have significant implications for improving exercise performance.

It is well established that carbohydrate (CHO) administration increases performance during prolonged exercise in humans[1-4] and animals.[5-7] For example, Coyle et al.[8] showed that the ingestion of a glucose polymer (1.8 g/min) increased exercise time from 3.02 to 4.02 hours during cycling . ). Exat 71% maximum oxygen uptake ( VO 2max . ercise time at 69% VO2max was shown by McConell et al.[9] to increase from 152 to 199 minutes with the ingestion of 285 g of CHO. Furthermore, Mitchell et al.[10] observed that the ingestion of CHO significantly increased the amount of work performed (1.98 – 0.09 vs 1.83 – 0.11 Nm · 105) in four trials of. intermittent (7 · 12 min bout) cycling at 70% VO2max. In addition to these improvements in endurance performance, the ability to perform resistance exercise has also been shown to increase when CHO is administered.[11] Lambert[12] showed that the total number of sets and repetitions tended to increase when subjects ingested 125 g of CHO while performing leg extensions at 80% of the previously determined ten repetition maximums, with 3 minutes of rest between sets. In another study by Haff et al.,[13] ª 2010 Adis Data Information BV. All rights reserved.

subjects were required to perform 16 sets of ten repetitions of leg extension/flexions at 120/s on a Cybex isokinetic dynamometer, with 3 minutes of rest between sets with and without CHO ingestion. Results show that total work performed significantly increased from 38.1 to 41.1 kJ when subjects ingested 240 g of CHO. However, two other studies reported that CHO supplementation does not improve the performance of resistance exercise.[14,15] We performed a meta-analysis of the literature that assessed the effect of CHO administration on endurance performance and capacity. For the purpose of this review, we define endurance performance as a sub-maximal exercise lasting 30 minutes or more requiring the completion of a given amount of work, task or a given distance as fast as possible or continued to exhaustion. A PubMed database search was initially conducted using the terms: carbohydrate and performance OR carbohydrate and cycling OR carbohydrate and running. Examination of reference lists from articles and review papers identified through the database further refined the search. Inclusion Sports Med 2010; 40 (9)

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Fig. 1. Performance effect of carbohydrate administration by category in the 72 compiled studies. Means of moderator variables that are not overlapped by their respective 95% confidence intervals are significantly different from each other at the 95% level. The number above each point represents the number of individual comparisons that are included into each category.

criteria requirements were that the study had to have a placebo or water control, there had to be a CHO treatment and CHO had to be consumed during exercise. As a result, a total of 72 studies[8,10,16-85] involving 1117 subjects and 112 comparisons were identified for inclusion in this analysis. Dependent measures included percentage change in the Loughborough Soccer Passing Test (LSPT) score, percentage change in the Loughborough Soccer Shooting Test (LSST) score, distance covered in time, time of performance rides, time to complete revolutions, time to complete work, time to exhaustion, power output decrement, Wingate results and work completed in time. Effect sizes (performance effect) were calculated as standardized mean differences relative to their pooled standard deviations, weighted as a function of the inverse within-group variation, and were adjusted for the correlation between pre- and post-ingestion measurements.[86] A randomized model was chosen and a correction for small-sample bias (Hedges’s g) was implemented. Effect size direction was deemed positive if performance improved from the control to the CHO condition and was deemed negative if performance decreased from the control to the CHO condition. Calculations were made using the Comprehensive Meta-Analysis V. 2.2.048 software package (Biostat, Englewood, ª 2010 Adis Data Information BV. All rights reserved.

NJ, USA). Results are presented with 95% confidence intervals (CI). The effects of various moderator variables on the change in performance with CHO administration are presented in figure 1. Means of moderator variables that are not overlapped by their respective 95% CI are significantly different from each other at the 95% level. The scale proposed by Cohen[87] (small [0.2], medium [0.5] or large [0.8]) may be used as a starting point for interpreting the results. We confirmed that a significant performance effect was observed in the total data set when CHO are ingested during exercise. Interestingly, the mean performance effect in studies with a more than 2-hour exercise duration was significantly greater than in studies with a less than 2-hour exercise duration. No other significant differences in performance effect were observed between moderator variables. Most of the performance effects in figure 1 approach the medium level in Cohen’s nomenclature, which corresponds to effect sizes ‘‘visible to the naked eye.’’[87] Moreover, based on the examination of studies with exercise time ranging between about 30 and 60 minutes, it seems that the beneficial effect of CHO administration on performance may occur when exercise lasts for at least 40–50 minutes.[18,22,63,88,89] In the study of Bonen Sports Med 2010; 40 (9)

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et al.,[88] which was the shortest exercise period we found in the literature, ingestion of glucose (1.5 g/kg) immediately before or during exercise did not . increase cycling time to exhaustion at 80% VO2max (26.6 and 26.1 minutes, respectively, vs 29.9 minutes with the placebo). Similarly, Mitchell et al.[89] did not observe any change in the time required to run 10 km with ingestion of water (41.9 minutes), 0.9 g/min of glucose (41.7 minutes) or a glucose-sucrose mixture (41.8 minutes), and 1.2 g/min of a high-fructose corn syrup (41.7 minutes). In contrast, Anantaraman et al.[18] showed that during a 60-minute exercise period to exhaustion, when compared with the placebo (138 W), the power output sustained between minutes 40 and 60 was significantly higher with ingestion of glucose immediately before exercise (30 g) and with ingestion of glucose both before and during exercise (120 g) [~164 W in both situations]. In the study by Neufer et al.,[63] subjects . performed 45 minutes of exercise at 77% VO2max on a cycle ergometer, followed by a 15-minute exercise period in which they were requested to produce the maximal amount of work. When compared with the placebo (159 kJ), performance significantly increased with ingestion of 45 g of CHO 5 minutes before exercise (175 kJ). Finally, Ball et al.[22] showed that the performance on a Wingate anaerobic test following cycling at 80% . VO2max for 50 minutes with ingestion of CHO (0.9 g/min) was significantly higher than with ingestion of a placebo (i.e. mean power output = 700 vs 655 W). The increase in performance with CHO ingestion during exercise has been extensively reviewed and will not be further summarized or discussed in this review.[1-4] The mechanism(s), which could mediate improvements in exercise performance associated with CHO administration however, remain(s) unclear. This review of the literature focuses on possible underlying mechanisms that could explain the increase in performance observed with the administration of CHO during prolonged exercise or muscle contractions in humans and animals. The beneficial effect of CHO ingestion on performance during prolonged exercise could be due to several factors including (i) an attenuation in central fatigue; ª 2010 Adis Data Information BV. All rights reserved.

(ii) a better maintenance in CHO oxidation rates; (iii) muscle glycogen sparing; (iv) changes in muscle metabolite levels; (v) reduced exercise-induced strain; and (vi) a better maintenance of excitationcontraction coupling (table I). There is evidence to suggest that these six factors may be associated with fatigue.[90-92] In addition, these six factors may be related and involved in proper muscle function in order to produce muscle force and perform prolonged exercise.[90-92] Therefore, positive changes in one or several of these factors could lead to an increase in performance during prolonged exercise. It should be noted that other possible factors may also be involved that have yet to be identified or more fully described. For example, on a whole body level, the better muscle functioning during exercise with CHO administration may be associated with a better gross efficiency, which could translate into an increase in performance.[93] 1. Carbohydrate (CHO) Administration and Central Fatigue during Exercise 1.1 Central Fatigue and Tryptophan

Newsholme et al.[94] proposed the hypothesis that higher serotonin levels could potentially influence the development of central fatigue by affecting arousal and mood linked to altered Table I. Potential mechanisms that could explain the increase in performance with carbohydrate (CHO) administration during exercise Potential mechanisms

Effect of CHO administration during exercise

Glucose oxidation rates

›

Blood glucose levels

›

Utilization of muscle glycogen

fl2

Na+/K+ pump activity

›

Ca2+ cycling

2

Central fatigue

fl

Cognitive function

›

Heat shock proteins

fl

Immune system

fl

5-Adenosine monophosphateactivated protein kinase

fl2

Oxidative stress

fl2

2 indicates no change; fl indicates decreases; › indicates increases.

Sports Med 2010; 40 (9)

Carbohydrate Administration and Performance

perceptions of effort and muscle fatigue. In support of this hypothesis, it has been shown that serotonin levels in the brain are increased during prolonged exercise in rats.[95] Since tryptophan is the precursor for the synthesis of serotonin, increased plasma levels of free tryptophan could increase cerebral tryptophan uptake and enhance serotonin production in the brain.[96] During prolonged exercise low levels of plasma insulin are observed, which favours the release of free fatty acids (FFA) from adipose tissue. This results in an increased plasma level of both FFA and free tryptophan, as FFA binds to albumin and displaces some of the albumin-bound tryptophan.[97] Glucose ingestion stimulates the secretion of insulin and blunts the exercise-induced rise in both plasma FFA and free tryptophan.[96] Therefore, this could counteract the development of central fatigue by attenuating the rise in brain serotonin. This hypothesis was tested in the study of Davis et al.[98] Their research showed that in the control situation, plasma free tryptophan increased by ~7-fold, when subjects performed . prolonged exercise for 200 minutes at 68% VO2max. This was associated with an increase in plasma FFA levels and reduced blood glucose levels from 5 to 4 mmol/L. When subjects ingested ~1 g/min of CHO, the blood glucose level was maintained at 5.5 mmol/L, and plasma free tryptophan as well as FFA was significantly attenuated and fatigue was delayed by ~1 hour. 1.2 Hypoglycaemia and Performance

Circulating glucose and lactate seem to be the two main energy sources for the central nervous system during exercise and a continuous supply may be essential for optimal function in activating skeletal muscle.[99,100] Accordingly, the findings of Koslowski et al.[101] support the idea that CHO availability for the brain may be important in maintaining an adequate neural drive to the muscles. Their study demonstrated that the infusion of glucose directly into the carotid artery (increasing central blood glucose level from 4 to 10 mmol/L and maintaining peripheral blood glucose level at 4.5 mmol/L) delayed fatigue in dogs exercising until exhaustion on a treadmill ª 2010 Adis Data Information BV. All rights reserved.

751

with a slope of 12% and a speed ranging from 1.2 to 1.8 m/sec. Nybo[102] showed that the average force production during a sustained maximal muscle contraction .was decreased after 3 hours of exercise at 60% VO2max in endurance-trained subjects, in which blood glucose levels significantly decreased from 4.5 to 3 mmol/L after exercise. The reduced force development in this study was associated with a diminished activation drive from the CNS. This central fatigue was reversed when euglycaemia (4.5 mmol/L) was maintained with the ingestion of 200 g of CHO. In addition, it was easier for the subjects to retain power output at the end of prolonged exercise when hypoglycaemia was prevented. However, Felig et al.[38] showed that hypoglycaemia may not affect performance during prolonged exercise, and that a better maintenance of glucose levels appears not to consistently improve performance. They demonstrated a progressive decline in blood glucose levels and hypoglycaemia (blood glucose LMI › No influence of drug on [BDNF]s, but › in [COR]s, HR and memory

. VO2peak, [BDNF]p, [insulin]p, [COR]p, [IGF-1]p, [b-amyloids 40-42]p, cognitive tests

. VO2peak, [BDNF]s, [IGF-1]s

[BDNF]s, questionnaire on lifestyle

. VO2max (estimated), HR, [BDNF]s, HPA index

Results [BDNF]p in F with MCI > [BDNF]p in M with MCI (p = 0.09) Wk 24 at rest: fl in [BDNF]p in F and › in [BDNF]p in M vs controlsa; [BDNF]p ~ [cortisol]p in aerobic training group Wk 0 at rest: [BDNF]s in MS < [BDNF]s in controls Wk 0 after LMI: [BDNF]s fl in MS and controls Wk 4 at rest: [BDNF]s › in MS; [BDNF]s fi in controls Wk 4 after LMI: [BDNF]s fl in MS and controls Wk 8 at rest: [BDNF]s fi in MS and controls Wk 8 after LMI: [BDNF]s fl in MS and controls BDNF was measured 30 min, 2 h and 3 h postLMI [BDNF]s highly trained < [BDNF]s moderately trained [BDNF]s ~ watching television at younger age [BDNF]s in high cardio-respiratory fit subjects < [BDNF]s in low cardio-respiratory fit subjects

Continued next page

769

Sports Med 2010; 40 (9)

Study (year)

BDNF and Exercise in Humans


Table I. Data extraction from 24 included studies

770


Table I. Contd Study design

Sample size; sex; age (mean – SD)

Intervention; Groups

Outcome measures

Results

Goekint et al.[57] (2010)

CT

23 healthy subjects; 78.3% M; 20.8 – 0.6 y

Acute strength exercise, 10-wk strength training; Strength training and control group

[BDNF]s, [IGF-1]s, [IGFBP-3]s, cognitive assessment

Acute strength exercise, after sixth session: [BDNF]s fi , [IGF1]s fi , [IGFBP3]s fi After thirtieth session: [BDNF]s fi , [IGF1]s fi , [IGFBP3]s fi Strength training, wk 10 at rest: [BDNF]s fi , [IGF1]s fi , [IGFBP3]s fi in strength training group and controls; short-term memory › in both groups (no differences between strength training group and controls); wk 10 after strength exercise: [BDNF]s fi , [IGF1]s fi , [IGFBP3]s fi in strength training group and controls

Gold et al.[47] (2003)

CT

45 subjects (25 MS patients, 20 healthy controls); 33.3% M; 39.9 – 1.9 y

Acute aerobic exercise: LMI, pre-exercise: GXT; Persons with MS and healthy control group

Gustafsson et al.[58] (2009)

CT

36 subjects (18 patients with MDD, 18 healthy controls); 50% M; 34.0 y

Acute aerobic exercise: LMI and HI; Patients with moderate MDD and healthy control group

Laske et al.[59] (2010)

CT

55 subjects (35 patients with remitted MDD, 20 healthy controls); 0% M; 60.0 – 6.9 y

Acute aerobic exercise: HI; Patients with remitted MDD and healthy control group

. VO2max, HR, [BDNF]s, [NGF]p, lactate

HR, RPEb, [BDNF]p, [COR], MADRSscore

. VO2peak, ECG, RPEb, lactate, [BDNF]s, HAMD-scale, MMSE and DemTect score, HPA index

At rest: [NGF]p in MS > [NGF]p in controls; [BDNF]s in MS = [BDNF]s in controls LMI: [BDNF]s › in MS and controls (no differences between MS and controls)

At rest: [BDNF]p in MDD = [BDNF]p in controls LMI: [BDNF]p › in M MDD; [BDNF]p fi in M controls, F MDD and F controls HI: [BDNF]p › in M MDD at 0 min and 60 min post-HI exercise; [BDNF]p › in F MDD and M controls at 0 min post-HI; [BDNF]p fi in F controls at 0 min post-HI; [BDNF]p fi in F MDD and F and M controls at 60 min post-HI; [BDNF]p fi in M and F MDD and controls at 30 min post-HI No correlation between: [BDNF]p and cortisol; [BDNF]p and MADRS scores

At rest: [BDNF]s in MDD < [BDNF]s in healthy controls; BMI in MDD > BMI in healthy controls; physical fitness in MDD < physical fitness in healthy controls; [BDNF]s ~ HAMD-score in MDD HI: [BDNF]s › in MDD, [BDNF]s fi in healthy controls at 0 min post-HI; [BDNF]s fl in MDD, [BDNF]s fl 30 min post-HI Continued next page

Knaepen et al.

Sports Med 2010; 40 (9)

Study (year)

Study design



Outcome measures

Results

Levinger et al.[60] (2008)

RCT

49 healthy untrained subjects; 51.0% M; 50.9 – 6.2 y

10-wk strength training; HiMF and LoMF group

[BDNF]p, [TG]p, [HDL]p, [glucose]p, [insulin]p, [HbA1c]p, anthropometry, muscle strength, MetS, blood pressure

Wk 0 at rest: [BDNF]p in HiMF > [BDNF]p in LoMF Wk 10 at rest: [BDNF]p fi , muscle strength ›, lean body mass › [BDNF]p ~ risk factors for MetS ([TG]p, [glucose]p, [HbA1c]p, insulin resistance)

Nofuji et al.[61] (2008)

ROS

26 healthy subjects; all M; 22.1 – 1.1 y

No intervention; Sedentary and trained group

[BDNF]s, [BDNF]p, HbA1c, FBG, TC, HDL-C, TG, BMI, body fat (%), WHR, psychological assessment, physical activity

[BDNF]s in sedentary > [BDNF]s in trained subjects [BDNF]p in sedentary = [BDNF]p in trained subjects [BDNF]s negative ~ TEE, MEE and WC No differences in age, anthropometric and psychological parameters between sedentary and trained subjects

Rasmussen et al.[62] (2009)

T

8 healthy subjects; all M; 22–40 y

Acute aerobic exercise: HI, pre-exercise: GXT; No groups

HR, [BDNF]p, lactate, glucose, SaO2, SjvO2, PaCO2

At rest: [BDNF]p arterial < [BDNF]p a-v diff < [BDNF]p vena jug; ƒBDNF = 72 – 32% HI: [BDNF]p arterial › , [BDNF]p vena jug › , [BDNF]p a-v diff › ; [BDNF]p arterial < [BDNF]p a-v diff < [BDNF]p vena jug; ƒBDNF = 84 – 8%

Rojas Vega et al.[63,64] (2006, 2007)

T

8 healthy athletes; all M; 24.6 – 1.3 y

Acute aerobic exercise: LMI and HI, pre-exercise: GXT; No groups

Rojas Vega et al.[65] (2008)

T

11 SCI athletes; all M; 40.6 – 6.3 y

Acute aerobic exercise: LMI and HI, pre-exercise: GXT; No groups

Schiffer et al.[66] (2009)

RCT

27 healthy subjects; NS; 22.2 – 1.8 y

12-wk strength training, 12-wk aerobic training, pre-/posttraining: GXT; Aerobic, strength training and control group

. VO2max, HR, [BDNF]s, [COR]s, lactate, RPEb

. VO2max, HR, [BDNF]s, [IGF-1]s, [PRL]s, [COR]s, lactate

. VO2max, HR, [BDNF]p, [IGF-1]p, lactate

LMI: [BDNF]s fi , [COR]s fi , lactate fi HI: [BDNF]s › , lactate › ; [COR]s › during recovery (10 min and 15 min post-HI)

At restc: [BDNF]s › ; [IGF-1]s, [PRL]s, [COR]s normal LMI: [BDNF]s › , [IGF-1]s › , [PRL]s fi , [COR]s fi HI: [BDNF]s fi , [IGF-1]s › ; [PRL]s › , [COR]s › Wk 12 at rest, strength training: [BDNF]p fi , strength › , [IGF-1]p fl ; aerobic training: [BDNF]p fi , aerobic performance › , [IGF-1]p fl – controls: [BDNF]p fi , [IGF-1]p fl Continued next page

771

Sports Med 2010; 40 (9)

Study (year)



Table I. Contd

772


Table I. Contd Study design



Outcome measures

Schulz et al.[67] (2004)

RCT

28 MS patients; 32.1% M; 39.5 – 10 y

8-wk aerobic training, pre-/post-training: GXT and LMI; Persons with MS and MS control (no intervention) group

Seifert et al.[68] (2010)

RCT

12 obese subjects; all M; 30.0 – 6.5 y

12-wk aerobic training, pretraining: GXT, pre-/posttraining: LMI and HI; Aerobic training and control group

Stro¨hle et al.[69] (2010)

RCT (crossover)

24 subjects (12 patients with panic disorder, 12 healthy controls); 25% M; 31.4 – 2.4 y

Acute aerobic exercise: LMI; LMI, quiet rest and healthy control group

VASarousal/anxiety, [BDNF]s

At rest: [BDNF]s fl in subjects with panic disorder LMI: [BDNF]s › in subjects with panic disorder, [BDNF]s in healthy controls; [BDNF]s ~ VASarousal/anxiety

Tang et al.[70] (2008)

T

16 healthy subjects; 50% M; 19–30 y

Acute aerobic exercise: LMI; No groups

HR, [BDNF]s

At rest: large inter-individual differences in [BDNF]s; LMI: [BDNF]s ›

Winter et al.[71] (2007)

RCT (crossover)


Acute aerobic exercise: LMI and HI, pre-exercise: GXT; LMI, HI and control group

HR, [BDNF]s, [DA]p, [NE]p, [E]p, lactate, RPEb, cognitive assessment, mood rating

LMI: [BDNF]s › , [DA]p › , [NE]p › , [E]p › HI: [BDNF]s › , [DA]p › , [NE]p › , [E]p › [BDNF]s: HI › > controls ›

. VO2max, HR, [BDNF]s, [NGF]s, [IL-6]p, [sIL-6R]p, [ACTH]p, [COR]p, [NE]p, [E]p, [lactate]s, assessment of coordinative function, psychological assessment

. VO2max, HR, [BDNF]p arterial and [BDNF]p vena jug, MCA Vmean, CBF

Results Wk 0 after LMI: [BDNF]s › d Wk 8 after LMI (vs rest at wk 8): lactate fl , [BDNF]s › d Wk 8 at rest and after LMI vs wk 0: [BDNF]s fi , [NGF]s fi , [IL-6]p fi , [sIL-6R]p fi , [ACTH]p fi , [COR]p fi , [NE]p fi , [E]p fi ; diseasespecific quality of life › < - > wk 8 at rest and after LMI: [BDNF]s › in MS, but difference with MS control group and assessment at wk 0 was not significant Wk 0 after HI: [BDNF]p arterial › , [BDNF]p vena jug fi ; [BDNF]p vena jug in trained > [BDNF]p vena jug in control; [BDNF]p a-v diff in trained [BDNF]p a-v diff in control Wk 12 at rest: [BDNF]p arterial fi , [BDNF]p vena jug › , [BDNF]p a-v diff › ; [BDNF]p vena jug in trained > [BDNF]p vena jug in control; [BDNF]p a-v diff in trained [BDNF]p a-v diff in control Wk 12 after HI: [BDNF]p arterial fi compared with pre-training after HI; [BDNF]p arterial › compared with post-training at rest; [BDNF]p vena jug fi compared with pre-training after HI and to post-training at rest; [BDNF]p vena jug in trained > [BDNF]p vena jug in control; [BDNF]p a-v diff in trained [BDNF]p a-v diff in control

Continued next page

Knaepen et al.

Sports Med 2010; 40 (9)

Study (year)

Study (year)

Study design



Outcome measures

Results [DA]p: HI › = LMI › = controls › [NE]p: HI › > LMI › > controls › [E]p: HI › > controls › Cognitive assessment: 20% better after HI compared with LMI and controls

Yarrow et al.[72] (2010)

RT


Acute strength exercise: 5-wk strength training; TRAD and ECC+ group

Zoladz et al.[75] (2008)

T


5-wk aerobic training, pre-/post-training: GXT; No groups

[BDNF]s, [testosterone]s, [growth hormone]s, [lactate]s[73,74]

. VO2max, HR, [BDNF]p, [insulin]p, [glucose]p, [lactate]p

Acute strength exercise (wk 0): [BDNF]s fi in TRAD and ECC+ Strength training, wk 5 at rest: [BDNF]s fi in TRAD and ECC+; wk 5 after strength exercise: [BDNF]s › in TRAD and ECC+ › [BDNF]s from rest to post-strength exercise is 98% greater in post-strength training compared with baseline › [BDNF]s is load dependent



Table I. Contd

Wk 0 after GXT: [BDNF]p fi Wk 5 at rest: [BDNF]p › Wk 5 after GXT: [BDNF]p › Wk 5: [BDNF]p › after GXT > [BDNF]p › at rest

a

This is a sex-specific effect of aerobic training versus stretching on [BDNF]p (i.e. group X sex ANOVA, F1,23 = 4.68; p = 0.04).[50]

b

See Borg[76] for the RPE = rating of perceived exertion.

c Rojas Vega et al.[65] did not include a control group of healthy subjects in their study. Consequently, the finding that baseline [BDNF]s is increased compared with able-bodied subjects cannot be verified. d

Schulz et al.[67] found no statistically significant differences at wks 0 and 8 of aerobic training at rest or after LMI between the MS group and the MS control group. The differences that are mentioned in this table are not significant.

773

Sports Med 2010; 40 (9)

ACTH = adrenocorticotropic hormone; BDNF = brain-derived neurotrophic factor; [BDNF]p arterial = [BDNF] measured in arterial plasma; [BDNF]p vena jug = [BDNF] measured in jugular venous plasma; [BDNF]p a-v diff = difference between arterial and jugular venous plasma BDNF concentration; BMI = body mass index; CBF = cerebral blood flow; COR = cortisol; CT = non-randomized controlled trial; DA = dopamine; DemTect = cognitive screening for diagnosis of mild cognitive impairment and dementia ; E = epinephrine; ECC+ = eccentric-enhanced resistance exercise/training; ECG = electrocardiogram; F = female; FBG = fasting blood glucose; ƒBDNF = cerebral fractional release of BDNF; G-CSF = granulocyte colony stimulating factor; GXT = graded exercise test; HAMD-scale = Hamilton rating scale for depression; HbA1c = glycated hemoglobin A1c; HDL = high density lipoprotein; HI = high-intensity exercise; HiMF = high metabolic risk group; HPA-index = Baecke habitual physical activity index; HR = heart rate; IGF-1 = insulin-like growth factor-1; IGFBP-3 = insulin-like growth factor binding protein 3; IL = interleukin; LMI = low to moderate intensity exercise; LoMF = low metabolic risk group; M = male; MADRSscore = Montgomery-Asberg depression rating scale; MCA Vmean = mean flow velocity of middle cerebral artery; MCI = mild cognitive impairment; MDD = major depressive disorder; MEE = movement-related energy expenditure; MetS = metabolic risk factor; MMSE = mini-mental status examination; MRI = magnetic resonance imaging; MS = multiple sclerosis; NE = norepinephrine; NGF = neuronal growth factor; NS = not specified; PaCO2 = arterial carbon dioxide tension; PRL = prolactin; RCT = randomized controlled trial; ROS = retrospective observational study; RPE = rating of perceived exertion; RT = randomized non-controlled trial; SaO2 = arterial haemoglobin oxygen saturation; SCI = spinal cord injured; TG = triglycerides; SjvO2 = jugular venous haemoglobin oxygen saturation; T = non-randomized non-controlled trial; TC = cholesterol; TEE = total daily energy expenditure; . TH = threshold; TRAD = traditional resistance exercise/training; VASarousal/anxiety = visual analogue scale for arousal and anxiety; Vth = ventilator threshold; VO2max = maximal oxygen . uptake; VO2peak = peak oxygen uptake; WC = walking count; WHR = waist-to-hip ratio; []s indicates serum concentration; []p indicates plasma concentration; ~ indicates correlation; › indicates significant increase; fl indicates significant decrease; fi indicates no significant difference.

Knaepen et al.

774

2.2 Study Populations

The sample size of trials that were included in this review varied from 8[62-64] to 55[59] subjects with a mean sample size of 24 subjects. For the four retrospective observational studies, sample sizes were larger, ranging from 26[61] and over 44[53] and 75[55] to 85[52] subjects. Proof of evidence would become more solid if all studies included an a priori power analysis to determine the appropriate sample size. Study populations were drawn from several sources; for example, general population,[47,54,57,60,66] students,[66] athletes,[56,63,64] spinal cord injured (SCI) athletes,[65] persons with major depression,[58,59] cognitive impairment[50] or MS.[47,51,67] Thirteen studies examined both males and females,[47,50-55,57-58,60,67,69-70] while nine studies examined only males[56,61-65,68,71-72,75] and one study only females.[59] The mean age of participants in all the included studies ranged from 20.8 – 0.6 years[57] to 70.0 – 8.3 years.[50] Three studies examined a population of the elderly (i.e. mean age ‡55.0 years)[50,55,59] and no study that included children or adolescents (i.e. mean age £18.0 years). Lommatzsch et al.[77] showed that basal concentrations of BDNF significantly changes with increasing age. Katoh-Semba et al.[78] stated that children and adolescents could be prone to changes in neurotrophines due to maturation and growth. Therefore, it might be interesting to study possible differences in effects of acute exercise and training on peripheral concentration of BDNF between young and old healthy subjects or in young and old persons with a chronic disease or disability. In most of the included studies, it is not always clear whether it concerns untrained, moderately trained or well trained subjects. Studies should report on the level of. fitness, expressed in maximal oxygen uptake (VO2max) or maximal power output, of their study population. It is likely that the effects of acute exercise and training on peri-

pheral BDNF depend on the physical fitness of the subjects, as BDNF could be involved in processes of energy metabolism.[37,40,79] 2.3 Exercise Protocols

Twenty out of 24 studies applied an exercise intervention. In general, four different interventions can be distinguished as follows: an acute aerobic or strength exercise; and an aerobic or strength training programme. 2.3.1 Acute Exercise Protocols

Predominantly, the effect of an acute aerobic exercise on peripheral BDNF has been investigated in human subjects. However, there is a large variation in the protocols used to apply to an acute aerobic exercise intervention (tables II and III). Graded exercise tests (GXTs) should be distinguished from acute aerobic exercise protocols of long or short duration. Sixteen of 20 interventional studies carried out a GXT until exhaustion a few days prior to the intervention or as an intervention on its own. In these studies, GXTs are mainly performed to determine the intensity of an acute aerobic exercise or training protocol. In three studies, a GXT was used as an isolated intervention to study its effect on circulating concentrations of BDNF.[54,59,75] In these cases, a GXT is evaluated as a short acute exercise of high intensity (table III). In two studies a GXT was part of a prolonged acute exercise protocol of high intensity1.[55,62,63] Protocols of all GXTs can be found in table II. Fifteen of 20 studies applied an acute aerobic exercise intervention (table III). Seven of those studies (table III) investigated the effect of both low to moderate and high-intensity aerobic exercises,[54,56,58,63-65,68,71] five studies focused only on exercises of low to moderate intensity[47,51,67,69,70] and three on the effects of an isolated high-intensity exercise[59,62,75] on concentration of BDNF. The protocols of the acute exercise interventions differ in each study, which makes it difficult to

1 It should be noted that in the studies of Rojas Vega et al.[63,64] and Gustafsson et al.,[58] an acute exercise of low to moderate intensity preceded the GXT. This could influence the effect of a GXT on peripheral BDNF levels. The preceding exercise of low to moderate intensity, together with the GXT, has also been evaluated as a prolonged acute exercise protocol of high intensity and will be discussed in section 2.6.1.


Sports Med 2010; 40 (9)

Study (year)

GXT

Exercise

GXT protocol

GXT until exhaustion (mean maximal exercise values at baseline)

BDNF measured pre- and post-GXT

Acute aerobic exercise protocols Castellano and White[51] (2008)

Yes

Cycling

NS + 5–20 W every 2 min

Yes (NS: symptom-limited maximum or 85% of estimated HRmax)

No

Ferris et al.[54] (2007)

Yes

Cycling

NS

WRmax (293.47 – 17.65 W); . VO2max (2805.80 – 164.31 mL/min); HRmax (175.67 – 3.19 bpm), % pred HRmax (90.31 – 1.75 %); RER (1.27 – 0.02); lactate (10.67 – 0.66 mmol/L)

Yes ›

No


Yes

Cycling

80 W + 40 W every 3 min

Yes (NS)

Gold et al.[47] (2003)

Yes

Cycling


Yes (NS)

No


Yes

Cycling

50 W (30 W F) + 5 W every 20 s (30 s F)

Yes (NS)

Yes › a,b

Laske et al.[59] (2010)

Yes

Treadmill

3 km/h at 0% inclination + simultaneous › in speed and inclination every 3 minc

. VO2max (1.9 – 0.3 mol/L/min); Wmax/kg (1.3 – 0.4 W/kg)

Yes › d

Rasmussen et al.[62] (2009)

Yes

Rowing

NS

Yes (NS)

No

Rojas Vega et al.[63,64] (2006, 2007)

Yes

Cycling

NS + 40 W every 5 min

Yes › a


Yes

Handcycling


Time test (7.3 – 1.1 min); Wpeak (431.3 – 57.9 W); relative Wpeak (5.9 – . 0.7 W/kg); VO2max (56.6 – 8.6 mL/kg/min); HRmax (189.3 – 10.3 bpm) . Wmax (158.2 – 28.9 W); HRmax (183 – 11.8 bpm); VO2max (34.5 – 9.2 mL/kg/min); RPEmax (19.5 – 1.2)



Table II. Protocols for graded exercise tests (GXTs) until volitional fatigue prior to or following an acute exercise or training protocol

No


No

NS

NS

NS

NS

Tang et al.[70] (2008)

No

NS

NS

NS

NS


Yes

Running (field)

8 km/h + 2 km/h every 3 min

Yes (NS)

No

Acute strength exercise protocols Goekint et al.[57] (2010)

No

NS

NS

NS

NS


No

NS

NS

NS

NS

Baker et al.[50] (2010)

Pre/post

Treadmill walking

2 km/h + NSe

. VO2peak (22.95 – 4.35 mol/L/kg)

No

Castellano and White[51] (2008)

Pre

Cycling

NS + 5–20 W every 2 min

Yes (NS: symptom-limited maximum or 85% of estimated maximum heart rate)

No

Yes (NS: RER >1.1; HR >190; lactate > 8) . Wmax (168.8 – 40.5 W); VO2max (31.0 – 7.45 mL/kg/min) . VO2max (3.45 – 0.3 L/min); RER >1.14 . VO2max (3472 – 94 ml/min [or 45.29 – 0.93 mL/kg/min]); Wmax (255 – 7 W)

No

Aerobic training protocols

Pre/post

Running

7 km/h + 1.5 km/h; NS


Pre/post

Cycling



Pre

Cycling



Pre/post

Cycling


No No Yes fi

Continued next page

775

Sports Med 2010; 40 (9)

Schiffer et al.[66] (2009)

Knaepen et al.


% pred HRmax = percentage of predicted maximal heart rate; BDNF = brain-derived neurotrophic factor; bpm = beats per minute; F = female; HI = exercise of high-intensity; HR = heart . rate; HRmax = maximal heart rate; M = male; NS = not specified; RER = respiratory exchange ratio; RPEmax = maximal rating of perceived exertion[82]; VO2max = maximal oxygen uptake; . VO2peak = peak oxygen uptake; Wmax = maximal power output; WRmax = maximal work rate; › indicates significant increase; fi indicates no significant difference.

d Significant increase in [BDNF]s in MDD patients following a GXT but not in healthy control subjects (Laske et al.[59]).

e Baker et al.[50] used the modified Balke test[81] for their aerobic training protocol.

Significant increase in [BDNF]p in M and F MDD patients and healthy M control subjects following a GXT but not in healthy F control subjects (Gustaffson et al.[58]). b

c Laske et al.[59] used the same protocol as Porszasz et al.[80] for the acute aerobic exercise protocol.

NS NS NS NS No

In the studies of Gustaffson et al.[58] and Rojas Vega et al.,[63,64] the GXT was preceded by an acute aerobic exercise of moderate intensity, so the increase in BDNF may not be exclusively contributed to the effect of a GXT on its own. Protocols of both studies will be considered as a prolonged acute aerobic exercise protocol of high-intensity exercise and will be described in table III.


a

No Yes (NS: RER >1.1; HR >190; lactate >8) 7 km/h + 1.5 km/h every NS Pre/post Schiffer et al.[66] (2009)

Running

NS

NS

NS

NS

NS

NS

NS No

No Levinger et al.[60] (2008)

Strength training protocols

NS

Exercise GXT Study (year)

Table II. Contd


BDNF measured pre- and post-GXT GXT protocol

GXT until exhaustion (mean maximal exercise values at baseline)

776

compare between studies. Nevertheless, all studies could be categorized according to their exercise intensity (i.e. based on exercise load and duration) [table III]. In four studies the acute exercise intervention was part of the test protocol before and after an aerobic training programme. The effect of an aerobic training programme on the BDNF response from rest to the end of a standardized acute exercise of low, moderate or high intensity was studied.[51,67,68,75] Recently, the relation between an acute strength exercise session and concentration of BDNF was researched in two studies.[57,72] Goekint et al.[57] and Yarrow et al.[72] used an acute strength exercise session to analyse the change in BDNF from rest to immediately post-exercise and this was repeated at the end of a strength training programme. Table III shows that the moments of blood acquisition for analysis of BDNF are similar in most of the 16 studies on acute exercise: (i) at baseline; (ii) immediately following a low-, moderate- or high-intensity strength or aerobic exercise; and (iii) 15-60 minutes following the acute exercise. In two cases blood was not collected immediately following the acute exercise[51,70] and only Castellano and White[51] collected blood more than 60 minutes following the acute exercise. 2.3.2 Exercise Training Protocols

Six studies implemented an aerobic training programme ranging from 5 to 24 weeks, two to seven sessions a week of different loads, mode and duration.[50,51,66-68,75] Except for Baker et al.[50] and Schiffer et al.,[66] all studies on aerobic training investigated the effects of training on basal concentration of BDNF and on BDNF concentration following an acute exercise. Details on the aerobic training programme can be found in table IV. A strength training programme was conducted in four studies during 5, 10 or 12 weeks, respectively, three sessions a week of different intensity and repetitions.[57,60,66,72,83] Goekint et al.[57] and Yarrow et al.[72] studied the effects of strength training on basal concentration of BDNF and on BDNF concentration following an acute strength exercise session. A complete body workout with strength training devices was Sports Med 2010; 40 (9)


777

Table III. Protocols for acute aerobic and strength exercise interventions in 17 studies (i.e. acute exercise protocols, not graded exercise tests [GXTs]) Study (year)

Setting

Exercise

Protocol

Moment of BDNF collection before, during and after the acute exercise

Acute aerobic exercise protocols LMI Castellano and White[51] (2008)

Laboratory

Cycling

. 30 min at 60% VO2peak

T0 // T30, T120, T180 post-LMI

Gold et al.[47] (2003)

Laboratory

Cycling

. 30 min at 60% VO2max

T0 // T0, T30 post-LMI


Laboratory

Cycling




Laboratory

Walking


T0 // T0 post-LMI

Tang et al.[70] (2008)

Laboratory

Stepping

15 min


Ferris et al.[54] (2007)

Laboratory

Cycling

LMI: 30 min at Vth - 20% HI: 30 min at Vth + 10% GXT (see table II)

T0 // T0 post-LMI and -HI


Climatic chamber

Cycling

LMI: 60 min at 55% Wmax HI: LMI + TT equal to 30 min at 75% Wmax

T0, T60 // T0, T15 post-HI


Laboratory

Cycling

LMI in F: (30 W + 5 W every 30 s) + 6 min at Wconstant HI in F: LMI + GXT until exhaustion LMI in M/HI in M: idem as in F but with different intensity: 50 W + 5 W every 20 s

T0 // T0 post-LMI; T0, T30, T60 post-HI

Rojas Vega et al.[63,64] (2006, 2007)

Laboratory

Cycling

LMI: 10 min at 2 W/kg + 2 min at 2 W/kg HI: LMI + GXT with 25 W every 30 s until exhaustion + 15 min active recovery

T0, T10 // T0, T3, T6, T10, T15 postHI


Laboratory

Handcycling

T0, T10 // T0 post-HI


Laboratory

Cycling

LMI: 10 min warm up at 54% HRmax HI: LMI + TT over 42 km at 89% HRmax . LMI: 15 min at 70% VO2max . . HI: 60%VO2max with 10% VO2max every 4 min (6 min . rest between workloads until 100% VO2max)


Laboratory

Running

LMI and HI

LMI: 40 min at fixed individual HR and lactate 10 mmol/L

T0, T5, T10, T15 // and at the end of each workload during incremental cycling T0 // T0 post-HI // T0 post-learning task

HI Laske et al.[59] (2010) Rasmussen et al.[62] (2009)

See table II (GXT) Laboratory

Rowing


240 at 10–15% below LT

T0, T120 // T0, T60 post-HI

See table II (GXT)

Acute strength exercise protocols Goekint et al.[57] (2010)

Fitness centre

6 strength exercises

Warm up: 20 repetitions at 30% 1RM Exercise: 3 · 10 repetitions at 80% 1RM

T0 // T0 post-strength training session both in UC and TC Continued next page


Sports Med 2010; 40 (9)

Knaepen et al.

778

Table III. Contd Study (year)

Setting

Exercise

Protocol

Moment of BDNF collection before, during and after the acute exercise


Laboratory (NS)

2 strength exercises per group

TRAD group: 4 · 6 repetitions at 52.5% 1RM concentrically and eccentrically ECC+ group: 3 · 6 repetitions at 40% 1RM concentrically and 100% 1RM eccentrically

T0 // T1, T30 and T60 post-strength exercise

1RM = one repetition maximum; BDNF = brain-derived neurotrophic factor; ECC+ = eccentric-enhanced resistance exercise/training; F = female; HI = exercise of high-intensity; HR = heart rate; HRmax = maximal HR; LMI = exercise of low to moderate intensity; LT = lactate threshold; M = male; NS = not specified; T = moment of BDNF collection e.g. T120 = at 120 minutes following the start of the acute exercise or T60 post HI = 60 minutes following the end of the high-intensity exercise; TC = trained condition (at 30th strength training session); TT = time trial; TRAD = traditional resistance exercise/training; UC = untrained condition (at sixth strength training session); Vth = ventilatory threshold; . . VO2max = maximal oxygen uptake; VO2peak = peak oxygen uptake; Wconstant = constant power output; Wmax = maximal power output; [] indicates concentration; // separates moments of BDNF collection in time e.g. T0 // T0 post HI = T0 is at the start of the high intensity exercise, T0 post HI is the first BDNF collection immediately at the end of the high intensity exercise; so ‘//’ separates moments of BDNF collection during and following an acute exercise.

accomplished in three out of four strength training studies.[57,60,66] Only Yarrow et al.[72] used just two strength exercises for the workout. In all studies circulating BDNF was analysed pre-/posttraining and in two cases also halfway through the training programme.[50,51] Overall, training protocols differed in all studies (table IV). 2.4 Blood Sampling and Biochemical Analysis

For the analysis of free circulating peripheral BDNF, blood serum (16 studies) is preferred to that of blood plasma (eight studies). This could be due to the fact that blood serum has been the conventional standard for most biochemical analysis although, generally, the choice between blood serum and plasma is determined by the requirements of the individual laboratory. In some studies, preference is given to blood serum because the addition of anticoagulants (e.g. heparin or EDTA) in blood plasma can activate blood platelets and change the concentration of the constituents to be measured.[84,85] Concentrations of serum BDNF are approximately 200fold higher relative to those of plasma BDNF, indicating that low concentrations of BDNF are circulating free in the blood and higher amounts of BDNF are stored in platelets or in immune cells.[86,87] Moreover, platelets circulate for up to 11 days in peripheral blood, whereas BDNF protein circulates in plasma for

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