sports medicine Volume 40 Issue 12 December 2010

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Sports Med 2010; 40 (12): 991-993 0112-1642/10/0012-0991/$49.95/0

ACKNOWLEDGEMENT

ª 2010 Adis Data Information BV. All rights reserved.

Dear Reader As we reach the final issue of the year for Sports Medicine, we hope that you have found the articles published throughout 2010 to be both interesting and informative. The editors and publishing staff have appreciated the high quality of content contributed to the journal this year and look forward to keeping you up to date with topical issues in the field of sports medicine and the exercise sciences in 2011. We are also pleased to advise you of a number of important developments to affect the Adis journals portfolio in 2010. This year saw Drugs in R&D being transformed from subscription based to open access, making it the first Adis journal to embrace the open-access model. Pediatric Drugs was accepted for inclusion in Current Contents/Clinical Medicine and a Thompson ISI impact factor (IF) for the journal is expected in 2013. This year, we also celebrated the 10th anniversary of the American Journal of Clinical Dermatology making significant contributions to the field of dermatology. The high quality of Adis journals was further recognized in the new ISI IFs for 2009, with ten of our titles making strong IF gains over 2008. The IF for Sports Medicine was 3.118. The most impressive gains in our other titles were made by BioDrugs (IF 3.506), up more than 55%, and Drugs in R&D (IF 1.354), which was up more than 35%. Other standout performers include Drugs (IF 4.732), up 14%, and the American Journal of Clinical Dermatology (IF 1.820), up 17%. Impressive IF gains were also registered for Clinical Pharmacokinetics (4.560), CNS Drugs (3.879), Drugs & Aging (2.209), Molecular Diagnosis & Therapy (2.167) and Clinical Drug Investigation (1.414). The American Journal of Cardiovascular Drugs, a newly tracked journal in 2009, received its first IF (1.964) and was ranked #47 in the ‘Cardiac & Cardiovascular System’ category. Last, but not least, we would like to say a big thank you to all the authors who have contributed articles to Sports Medicine in the last 12 months. Without their hard work and diligence we would not have been able to publish the journal. The quality of published articles reflects also the significant time and effort dedicated by the peer reviewers who ensure that we continue to publish content of the highest possible standard. In addition to the members of our Honorary Editorial Board, we would like to thank the following individuals who acted as referees for articles published in Sports Medicine in 2010:

Mette Aadahl, Denmark Julie Agel, USA Takayuki Akimoto, Japan Ajmol Ali, New Zealand

David G. Allen, Australia Raul Artal, USA Stephen P. Bailey, USA Romualdo R. Belardinelli, Italy

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M.F. Bobbert, the Netherlands Klaus-Michael Braumann, Germany Marybeth Brown, USA Louise M. Burke, Australia Angus Burnett, Australia Jatin Burniston, UK Robert W. Burton, USA Chris Button, New Zealand Douglas Casa, USA Nicola Casartelli, Switzerland Lisa L. Chasan-Taber, USA Mario Ciocca, USA J.F. Clapp, USA Leslie A. Consitt, USA Ben Dascombe, Australia Eamonn Delahunt, Ireland Wim Derave, Belgium Michaela C. Devries, Canada Orna Donoghue, UK Brad Donohue, USA Eric Drinkwater, Australia Barry B. Drust, UK Gregory G. Dupont, France William P. Ebben, USA Martin Fahlstrom, Sweden Oliver Faude, Germany Caroline F. Finch, Australia Kevin R. Ford, USA Christine C.M. Friedenreich, Canada Colin W. Fuller, UK David Gallahue, USA A.C. Gielen, USA Warren Gregson, UK Anthony C. Hackney, USA John W. Hafner Jr, USA Bradley Hatfield, USA Timothy Hewett, USA Angela E. Hibbs, UK Laurie A. Hiemstra, Canada Dustin S. Hittel, Canada Diana M. Hopper, Australia Con C. Hrysomallis, Australia Mike Hughes, UK Mary Ireland, USA John J. Ivy, USA David R. Jacobs, USA Asker A.E. Jeukendrup, UK Kirsten K.L. Johansen, USA Daniel A. Judelson, USA Jaak J. Jurimae, Estonia Ronald L. Kamm, USA Andreas N. Kavazis, USA Wolfgang Kemmler, Germany


Justin Keogh, New Zealand W. Ben Kibler, USA Joseph J.J. Knapik, USA Christopher A. Knight, USA Duane Knudson, USA William J. Kraemer, USA Robert R.R. Kraemer, USA Bruno M. Lapauw, Belgium Itamar Levinger, Australia D. Leyk, Germany Keith Lyons, Australia Jim Macintyre, USA Christopher L. MacLean, USA Nicola N. Maffulli, UK Terry Malone, USA Goran Markovic, Croatia Steven R. McAnulty, USA Thomas T.L. McKenzie, USA Alexandra McManus, Australia Tim T. Meyer, Germany Michael C. Meyers, USA Gregory Myer, USA Rob R. Newton, Australia John J. Orchard, Australia Francesco F. Orio, Italy Leonie Otago, Australia Craig Ranson, UK Peter Reeves, USA Matthew Robins, UK Kristin L. Sainani, USA Giorgos K. Sakkas, Greece Laura A. Schaap, the Netherlands Brian Schilling, USA Michael Schmidt, USA Kathryn Schmitz, USA Thomas L. Schwenk, USA Ian Shrier, Canada Arthur J. Siegel, USA Perikles Simon, Germany Sarianna Sipila, Finland Raymond R. So, Hong Kong Billy Sperlich, Germany Nina N.S. Stachenfeld, USA Thomas T.W. Storer, USA Kristie-Lee Taylor, Australia Toomas Timpka, Sweden Grant G.R. Tomkinson, Australia Lara B. Trifiletti, USA N. Travis Triplett, USA Jaci Van Heest, USA Damien van Tiggelen, Belgium Joseph G. Verbalis, USA Geoffrey G.M. Verrall, Australia Jeff Walkley, Australia Mathias Wernbom, Sweden

Sports Med 2010; 40 (12)

Acknowledgement

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Alun G. Williams, UK Ulrik Wisloff, Norway Jeff Zachwieja, USA

Bohdanna T. Zazulak, USA Jerzy Zoladz, Poland

We look forward to your continued support in 2011 and to bringing you first-class content from around the globe. With best wishes from the staff of Sports Medicine and all at Adis, a Wolters Kluwer business.


Sports Med 2010; 40 (12)

REVIEW ARTICLE

Sports Med 2010; 40 (12): 995-1017 0112-1642/10/0012-0995/$49.95/0


Dietary Supplements and Team-Sport Performance David Bishop Institute of Sport, Exercise and Active Living (ISEAL) and School of Sport and Exercise Science, Victoria University, Melbourne, Victoria, Australia

Contents Abstract. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 996 1. Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 997 2. Team-Sport Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 997 3. Dietary Supplements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 998 3.1 Ribose. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 998 3.1.1 Classification and Usage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 998 3.1.2 Possible Mechanisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 999 3.1.3 Effects on Team-Sport Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 999 3.1.4 Adverse Effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1000 3.2 Caffeine. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1000 3.2.1 Classification and Usage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1000 3.2.2 Possible Mechanisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1000 3.2.3 Effects on Team-Sport Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1001 3.2.4 Adverse Effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1002 3.3 Creatine. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1002 3.3.1 Classification and Usage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1002 3.3.2 Possible Mechanisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1002 3.3.3 Effects on Team-Sport Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1003 3.3.4 Adverse Effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1004 3.4 Branched-Chain Amino Acids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1004 3.4.1 Classification and Usage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1004 3.4.2 Possible Mechanisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1004 3.4.3 Effects on Team-Sport Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1004 3.4.4 Adverse Effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1005 3.5 Alkalizing Agents. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1005 3.5.1 Classification and Usage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1005 3.5.2 Possible Mechanisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1006 3.5.3 Effects on Team-Sport Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1006 3.5.4 Adverse Effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1007 3.6 b-Alanine . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1007 3.6.1 Classification and Usage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1007 3.6.2 Possible Mechanisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1008 3.6.3 Effects on Team-Sport Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1008 3.6.4 Adverse Effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1008 3.7 Bovine Colostrum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1008 3.7.1 Classification and Usage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1008 3.7.2 Possible Mechanisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1008 3.7.3 Effects on Team-Sport Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1009

Bishop

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3.7.4 Adverse Effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.8 b-Hydroxy-b-Methylbutyrate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.8.1 Classification and Usage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.8.2 Possible Mechanisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.8.3 Effects on Team-Sport Performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.8.4 Adverse Effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Risks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5. Conclusions and Recommendations for Future Research . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Abstract

1009 1009 1009 1010 1010 1010 1010 1011

A well designed diet is the foundation upon which optimal training and performance can be developed. However, as long as competitive sports have existed, athletes have attempted to improve their performance by ingesting a variety of substances. This practice has given rise to a multi-billion-dollar industry that aggressively markets its products as performance enhancing, often without objective, scientific evidence to support such claims. While a number of excellent reviews have evaluated the performance-enhancing effects of most dietary supplements, less attention has been paid to the performance-enhancing claims of dietary supplements in the context of teamsport performance. Dietary supplements that enhance some types of athletic performance may not necessarily enhance team-sport performance (and vice versa). Thus, the first aim of this review is to critically evaluate the ergogenic value of the most common dietary supplements used by team-sport athletes. The term dietary supplements will be used in this review and is defined as any product taken by the mouth, in addition to common foods, that has been proposed to have a performance-enhancing effect; this review will only discuss substances that are not currently banned by the World Anti-Doping Agency. Evidence is emerging to support the performance-enhancing claims of some, but not all, dietary supplements that have been proposed to improve team-sport-related performance. For example, there is good evidence that caffeine can improve single-sprint performance, while caffeine, creatine and sodium bicarbonate ingestion have all been demonstrated to improve multiple-sprint performance. The evidence is not so strong for the performanceenhancing benefits of b-alanine or colostrum. Current evidence does not support the ingestion of ribose, branched-chain amino acids or b-hydroxyb-methylbutyrate, especially in well trained athletes. More research on the performance-enhancing effects of the dietary supplements highlighted in this review needs to be conducted using team-sport athletes and using team-sportrelevant testing (e.g. single- and multiple-sprint performance). It should also be considered that there is no guarantee that dietary supplements that improve isolated performance (i.e. single-sprint or jump performance) will remain effective in the context of a team-sport match. Thus, more research is also required to investigate the effects of dietary supplements on simulated or actual team-sport performance. A second aim of this review was to investigate any health issues associated with the ingestion of the more commonly promoted dietary supplements. While most of the supplements described in the review appear safe when using the recommended dose, the effects of higher doses (as often taken by athletes) on indices of health remain unknown, and further research is warranted. Finally, anecdotal reports suggest


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Dietary Supplements and Team Sports

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that team-sport athletes often ingest more than one dietary supplement and very little is known about the potential adverse effects of ingesting multiple supplements. Supplements that have been demonstrated to be safe and efficacious when ingested on their own may have adverse effects when combined with other supplements. More research is required to investigate the effects of ingesting multiple supplements (both on performance and health).

1. Introduction A well designed diet that meets the energy and nutrient intake needs and incorporates the proper timing of meals, is the foundation upon which optimal training and performance can be developed. Nevertheless, there is the common belief that, in conjunction with well designed training, the appropriate ingestion of some dietary supplements can enhance team-sport performance. This belief has given rise to a multi-billion-dollar industry that aggressively markets its products to teamsport athletes as performance enhancing, often without objective, scientific evidence to support such claims. However, while a number of excellent reviews have evaluated the performance-enhancing effects of most dietary supplements,[1-4] less attention has been paid to the performance-enhancing claims of dietary supplements in the context of team-sport performance. Such an analysis is important as fatigue has been demonstrated to be highly task specific[5-7] and, therefore, dietary supplements that enhance some types of athletic performance may not enhance team-sport performance (and vice versa). For example, dietary supplements that have been demonstrated to improve continuous exercise performance may not improve intermittent exercise performance. 2. Team-Sport Performance Team sports are increasingly popular with millions of participants worldwide. However, despite the ubiquitous nature of team sports, it is difficult to define exactly what is meant by ‘teamsport performance’. This is partly because the exact physical demands will differ between sports (and also between matches), but mostly because team sports are ultimately decided by points/ ª 2010 Adis Data Information BV. All rights reserved.

goals scored rather than the speed, strength or endurance of individual players. Nonetheless, it is possible to identify some common physical qualities that are important for team-sport success. Team-sport athletes are typically required to repeatedly produce maximal or near maximal efforts (e.g. ‘all-out’ sprints of 100 g d-1)[28] or when taken during exercise.[27] To date, no studies have reported adverse effects (i.e. medical problems, diarrhoea, gastrointestinal distress, muscle cramping) to ribose supplementation.[30-32,37]

3.2 Caffeine 3.2.1 Classification and Usage

Caffeine (1,3,7-trimethylxanthine) is the most commonly consumed drug in the world and is found in coffee, tea, cola, chocolate and various ‘energy’ drinks (table I). The actions of caffeine throughout the body correlate positively with plasma caffeine levels, which are governed by absorption, metabolism and excretion.[38] Almost 100% of orally-administered caffeine is absorbed ª 2010 Adis Data Information BV. All rights reserved.

Table I. Typical caffeine content in common substances Substance

Caffeine (mg)

1 can of cola drink

40

1 cup of tea

50

1 can of Red Bull (250 mL)

80

1 cup of brewed coffee

100

1 ‘No Doz’ caffeine tablet

100

Guarana (100 mg)

100

and it begins to appear in the blood within 5 minutes of ingestion.[39] Typical experimental doses of caffeine (4–6 mg kg-1 of body mass) will produce peak plasma concentrations of 6–8 mg mL-1 (30–49 mmol L-1) within 40–60 minutes after ingestion; plasma half-life ranges from 3 to 10 hours.[40] This suggests that if caffeine is ingested during the pre-match warm up, plasma caffeine levels will be maintained for the entire match.[41,42] While it remains unclear what the effective minimal or maximal doses are, it appears that ingestion of 2–3 mg kg-1 of caffeine is sufficient to produce an ergogenic effect in most individuals.[43,44] Ingestion of doses >6 mg kg-1 do not seem to provide a further enhancement of performance.[45] It needs to be remembered, however, that caffeine uptake can vary greatly among individuals, depending on the degree of habituation,[46] and individual trialling of the appropriate dose for individual athletes is recommended. It has also been suggested that caffeine in the form of coffee may yield smaller effects than a similar dose of pure caffeine,[47] possibly due to antagonistic actions from other compounds in caffeine.

3.2.2 Possible Mechanisms

The ergogenic effects of caffeine have been attributed to a number of possible mechanisms, including the blocking of adenosine receptors,[48] central nervous system facilitation,[49] increased Na+/K+ATPase activity,[50] mobilization of intracellular calcium[51] and increased plasma catecholamine concentration.[52] It now seems likely that adenosine receptor antagonism is the primary mechanism of action and that this contributes to improved performance via increases in neurotransmitter release, motor unit firing rates and dopominergic transmission.[53] However, there is Sports Med 2010; 40 (12)


1001

3.2.3 Effects on Team-Sport Performance

While many studies have demonstrated that caffeine is ergogenic for the performance of prolonged endurance exercise,[53-55] there is limited research that has investigated the effects of caffeine on single-sprint, multiple-sprint or teamsport performance. Following caffeine ingestion, an ~7% increase in total work has been reported during a single 4-second[42] or 6-second[56] sprint on a cycle ergometer; this improvement has a tendency to be smaller when running sprints are performed (e.g. a 1.4% reduction in 30-m sprint time following caffeine ingestion[57]). This ergogenic effect appears to be maintained when sprints are repeated. For example, Schneiker et al.[42] reported a similar 7% increase in mean power when ten male team-sport athletes (peak oxygen uptake . [VO2peak] 56.5 – 8.0 mL kg-1 min-1) performed an intermittent-sprint cycle test consisting of 2 · 36-minute ‘halves’, each half comprising 18 · 4-second. sprints with 2 minutes of active recovery at 35% VO2peak between each sprint. These results were supported by another study that reported caffeine ingestion to enhance simulated, highintensity, team-sport performance in competitive male rugby players.[58] In contrast, two other studies have reported a negligible effect of caffeine ingestion when repeated running sprints (10–12 · 20- to 30-m) were separated by short rest periods (10–35 seconds).[57,59] All four of the above studies used a caffeine dose of 5–6 mg kg-1 of body mass. As a result of the improvements in initial sprint performance,[56] there is the risk that caffeine ingestion may be ergolytic as fatigue develops, possibly due to an increase in the by-products of anaerobic metabolism.[60] Indeed, in a study by Greer et al.,[61] examining the effects of a 6 mg kg-1 dose of caffeine on peak and mean power during four 30-second Wingate tests, each separated by


4 minutes, there was a non-significant trend toward enhanced performance of the first Wingate test and a significantly reduced performance by the fourth bout. However, contrary to the results of the study by Greer et al.,[61] Schneiker et al.[42] reported that although caffeine was able to significantly enhance the performance of intermittent sprints, resulting in increased plasma lactate concentrations, this did not affect the ability of participants to maintain work efforts in the latter stages of the exercise protocol. Thus, while further research is certainly warranted, these results suggest that caffeine ingestion (6 mg kg-1) is likely to improve intermittent, but not repeated, sprint performance. Furthermore, there is no apparent increase in the rate of fatigue development attributable to initial improvements in work and power achieved during intermittent-sprint tests as a consequence of caffeine ingestion. In another review article, it has also been suggested that ergogenic doses of caffeine (2–6 mg kg-1 of body mass) may negatively affect reaction time and alertness, which may, in turn, counteract the beneficial effects of caffeine on team-sport performance.[62] However, this view is inconsistent with the published research as significant increases in choice reaction time, measured before, during and after a prolonged intermittent-sprint test, have been reported following caffeine ingestion (5–6 mg kg-1) [figure 2;[63,64]]. In addition, caffeine ingestion (6 mg kg-1) has also been reported

Placebo Caffeine 340 Choice reaction time (ms)

some evidence to support each of these mechanisms and it is probable that they all contribute to the wide range of physiological responses to caffeine that make it ergogenic. A more detailed discussion on the possible mechanisms underlying the ergogenic effects of caffeine can be found elsewhere.[53,54]

320 300

*

*

280

*

260 240 220 200 Rest

Pre-1st half

Post-1st half

Post-2nd half

Fig. 2. Effects of caffeine ingestion (6 mg kg-1) on choice reaction time measured before, during and after the prolonged intermittentsprint test described by Schneiker et al.[42,63] * indicates significant difference between conditions.

Sports Med 2010; 40 (12)

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to improve the ability to pass balls accurately while being pressured to pass rapidly (i.e. simulating a rugby game).[58] 3.2.4 Adverse Effects

The common social use of caffeine suggests that low-dose caffeine intake can be considered safe. However, high-dose caffeine intake is widely thought to be associated with adverse health effects.[40] In particular, caffeine is known to increase heart rate and blood pressure.[65] Other common adverse effects of caffeine include insomnia, tremors, headaches, anxiety, dependency, withdrawal and occasional gastrointestinal distress when drinking strong coffee.[40,66] Caffeine ingestion has also been reported to eliminate the ergogenic effects of creatine (Cr) supplementation.[67] While initial concerns were raised about the possible diuretic effects of caffeine on the performance and health of team-sport athletes, these concerns appear unfounded.[63] Indeed, we have found no effect of caffeine intake on urine specific gravity following the prolonged, intermittent-sprint test described by Schneiker et al.[42] The effects of caffeine on glucose transport are unclear with one study reporting that caffeine ingestion (5 mg kg-1) impairs insulin-stimulated glucose uptake in resting and exercised human skeletal muscle,[68] while another study reported that co-ingestion of large amounts of caffeine (8 mg kg-1) with carbohydrate had an additive effect on rates of postexercise muscle glycogen accumulation compared with consumption of carbohydrate alone.[69]

3.3 Creatine 3.3.1 Classification and Usage

Cr is a naturally occurring, non-essential, guanidine compound. Cr can be obtained in the diet (from animal-based foods such as fresh fish and meat and various synthetic Cr supplements) or synthesized from the amino acids glycine, arginine and methionine (primarily in the liver, pancreas and kidneys). Cr exists in free and phosphorylated forms (i.e. PCr), and approximately 95% of the body’s Cr is stored in skeletal muscle. Total Cr concentrations in skeletal muscle (i.e. Cr + PCr) average around mmol kg dry weight (dw)-1, with a higher capacity for storage


in fast-twitch muscle fibres. Following a Cr loading phase (typically ~0.3 g kg-1 d-1 or 20 g d-1 for 4–7 days), muscle Cr levels increase on average by approximately 25% to what appears to be a maximum of about 160 mmol kg dw-1.[70,71] Thus, team-sport athletes can begin matches with greater levels of muscle Cr available for energy production. There is, however, considerable variability concerning muscle Cr increases following supplementation; some individuals are ‘nonresponders’ (little or no increase in muscle Cr), whereas others, particularly athletes with low initial muscle Cr content, are ‘high responders’ (>30% increase in muscle Cr).[70] As the body breaks down about 1–2 g of Cr per day, it is normally recommended to follow the Cr loading phase with a maintenance phase of 3–5 g d-1. Maintenance doses of 2 g d-1 have been reported to be insufficient to maintain elevated muscle Cr levels.[72] Ingesting Cr prior to team-sport training sessions may augment muscle Cr uptake, as exercise is known to promote the uptake of ingested Cr by muscle.[70] An additional strategy to potentiate Cr accumulation in muscle is to consume Cr with carbohydrates (~100 g) or carbohydrate plus protein (~50 g of each).[73] Furthermore, wash-out periods of at least 2–4 weeks (every 6–8 weeks of Cr supplementation) seem prudent based on data that indicate that the effects of Cr supplementation may diminish after 2 months.[74]


It is well established that Cr supplementation can increase both total and PCr concentrations in the muscle.[70,75,76] As single and multiple sprints produce a severe reduction in intramuscular PCr concentration (figure 3), it has been proposed that increasing muscle PCr stores may improve multiple-sprint performance via a reduced ATP degradation and a faster resynthesis of PCr between sprints.[79] In addition to increasing the contribution of PCr to ATP resynthesis, this could potentially decrease the reliance on anaerobic glycolysis during team sports and thus reduce the accumulation of H+.[80] There is also some evidence that increased muscle Cr levels may enhance oxygen uptake during high-intensity Sports Med 2010; 40 (12)


1003

Cr Placebo

b

100 90 80 70 60 50 40 30 20 10 0

*

*

Post-ex + 20 s + 60 s + 120 s + 180 s

Rest

10.0 Change in performance (%)

[PCr] (mmol • kg dw−1)

a

*

*

8.0 6.0 4.0 * 2.0 0 −2.0 24 s

54 s 84 s Total work Recovery between sprints

Fig. 3. Changes in phosphocreatine (PCr) resynthesis rate and repeated-sprint performance following short-term creatine (Cr) supplementation (20 g d-1 for 5 days); * p < 0.05.[77,78] dw = dry weight.

exercise,[81] possibly via increased shuttling of high-energy phosphates between the cytosol and the mitochondria (i.e. the creatine-phosphate shuttle). While this could potentially contribute to a smaller performance decrement during team sports, this hypothesis remains to be tested. Finally, as Cr supplementation has been reported to increase glycogen storage,[82] this could provide an additional ergogenic effect of Cr supplementation for team-sport athletes. 3.3.3 Effects on Team-Sport Performance

Cr supplementation (typically ~20 g d-1 for 5–7 days) has been reported to improve[72,77,83-86] or have no effect[76,87-92] on multiple-sprint performance. Despite these conflicting results, closer inspection of these studies reveals a general trend whereby Cr supplementation does not improve performance when the recovery between sprints is ~30 seconds or less,[76,87,89-91] but is ergogenic when the recovery between sprints ranges from 50 to 120 seconds.[72,77,83,86] For example, Cr supplementation (~20 g d-1 for 5 days) has been reported to improve the performance of repeated 10-second cycle sprints interspersed with 60 seconds of recovery,[86] but not 30 seconds of recovery.[89] Moreover, within one study, Cr supplementation was reported to improve the performance of 6-second cycle sprints interspersed with recovery intervals of 54 or 84 seconds, but not 24 seconds.[77]


Thus, it appears that the recovery between sprints may determine whether or not Cr supplementation improves multiple-sprint performance. A possible explanation for the conflicting findings mentioned above is that it has been proposed that Cr supplementation may improve multiple-sprint performance via a faster resynthesis of PCr between sprints.[79] Indeed, improved multiple-sprint performance has been associated with an improved PCr replenishment rate.[77] However, as Cr supplementation has been reported to increase PCr resynthesis after 60 and 120 seconds, but not 20 seconds[78] (figure 3), this may explain why Cr supplementation does not generally improve the performance of multiple sprints interspersed with recovery periods of ~30 seconds or less. As team-sport athletes are often required to perform multiple sprints, interspersed with recovery periods ranging from 40 to 120 seconds,[93] it appears that Cr supplementation is likely to improve some aspects of team-sport performance. This is supported by the results of Cox et al.[84] who reported that Cr supplementation resulted in small improvements in some 20-m sprints and agility tasks during an exercise protocol designed to simulate match play in female soccer (association football) players; Cr supplementation had no effect on ball-kicking accuracy. Although not always explicitly reported, the improved Sports Med 2010; 40 (12)

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multiple-sprint performance appears to be due to an attenuation of fatigue as Cr supplementation has been reported to have limited effects on single-sprint performance.[87,94] It also needs to be considered that, when used in conjunction with training, Cr supplementation can potentiate gains in fat-free mass, muscle force and power output.[95-98] This augmented training response may be associated with an ability to perform more training when supplementing with Cr.[97] 3.3.4 Adverse Effects

At conventional doses, Cr supplementation in healthy adults has generally been found to be safe.[99] Throughout the years, however, some concerns have been raised, especially with respect to individuals who exceed the recommended loading and maintenance doses.[2] Cr loading is often accompanied by a rapid increase in body mass (1–2 kg in the first 2 weeks), which probably results mainly from intracellular water and/or glycogen accumulation driven by muscle Cr uptake.[62] While increases in body mass may be advantageous for contact team sports (e.g. rugby, American football), some have suggested that this may be disadvantageous for other team sports that involve considerable running.[3] The increase in muscle water content may also increase intramuscular pressure, which, in some individuals, has been reported to increase the risk of compartment syndrome.[100] While there were also initial concerns with regard to the potential adverse effects of Cr on renal function, subsequent studies have reported intact renal function after acute and prolonged dietary Cr intake.[101,102] There have been some rare reports of gastrointestinal distress,[84] which may be related to the timing of Cr ingestion or to co-ingestion with other substances.[103] 3.4 Branched-Chain Amino Acids 3.4.1 Classification and Usage

Amino acids are the building blocks of proteins. There are 20 common amino acids, of which nine are considered essential, i.e. they cannot be produced in sufficient amounts by the body and must be supplied by the diet. Branchedchain amino acids (BCAAs; leucine, isoleucine, ª 2010 Adis Data Information BV. All rights reserved.

valine) are essential amino acids that can be oxidized by skeletal muscle. Supplementation studies have typically involved doses of 5–20 g d-1.[104-107] However, some researchers have recommended doses of 7–10 g d-1 (100 mg kg body mass),[105] as such doses are less likely to increase plasma ammonia which can readily cross the blood-brain barrier and may contribute to central fatigue.


During prolonged exercise, there is increased oxidation of BCAA in the muscle and a rise in free fatty acids in the blood. As free fatty acids compete with tryptophan for binding sites on plasma albumin,[108] an increase in free fatty acids will lead to the displacement of tryptophan from its binding sites and an increase in free (unbound) tryptophan levels (figure 4). Thus, both an increase in free tryptophan and a decrease in BCAAs will act together to increase the free tryptophan : BCAA ratio. As both tryptophan and BCAAs compete for the same transporters in the brain, a decrease in this ratio will facilitate the transport of tryptophan (5-hydroxytryptamin: 5-HT) across the blood-brain barrier resulting in increased levels of brain serotonin. The ‘central fatigue hypothesis’ proposes that an increase in brain serotonin levels may limit both mental and physical performance.[109] It has therefore been hypothesized that BCAA supplementation will prevent the drop in plasma BCAA concentration, decrease the rise in free tryptophan : BCAA ratio, attenuate the increase in brain serotonin and reduce both mental[110] and physical fatigue during team sports.[107] In addition to this potential acute effect on performance, it has also been reported that BCAA supplementation before and after exercise has beneficial effects for decreasing exercise-induced muscle damage and promoting muscle-protein synthesis.[111,112] This may improve muscle recovery following hard training and matches. 3.4.3 Effects on Team-Sport Performance

While BCAA ingestion has been reported to increase the plasma BCAA concentration and to attenuate the rise in the free tryptophan : BCAA ratio,[113] most studies indicate that BCAAs do Sports Med 2010; 40 (12)


1005

Adipose tissue Selective transporter FFA A l b u m i n

FFA

FFA

Trp Fr Trp Tryptophan

BCAA

Serotonin

BCAA

Blood brain barrier Muscle Fig. 4. Proposed relationship between plasma branched-chain amino acid (BCAA) levels, plasma free fatty acid (FFA) levels, plasma tryptophan levels (Fr Trp) and increased serotonin levels in the brain.

not improve endurance performance.[110] Researchers have been unable to demonstrate any ergogenic effects of BCAA supplementation on time to fatigue during prolonged, fixed-intensity exercise[106,114-116] or incremental exercise.[117] Furthermore, in the only study to date, BCAA ingestion did not benefit time to fatigue during an intermittent shuttle test (walking, sprinting and running) designed to simulate the physiological demands of football.[107] Thus, despite a good rationale for its use, there is no evidence to suggest that the intermittent-sprint performance of team-sport athletes will be improved by BCAA ingestion. However, further research is required to investigate the effects of BCAA supplementation on other types of team-sport-related performance (e.g. repeated-sprint ability and jump performance when fatigued). As team sports require the precise execution of skills and tactics, especially late in a match when athletes are fatigued, further investigation into the effects of BCAA ingestion on the maintenance of cognitive function is also warranted. 3.4.4 Adverse Effects

BCAAs are considered relatively safe with only mild concern that high doses may cause ª 2010 Adis Data Information BV. All rights reserved.

gastrointestinal distress or interfere with the absorption of other amino acids.[4] 3.5 Alkalizing Agents 3.5.1 Classification and Usage

The bicarbonate system is present in both the intracellular and extracellular fluids and operates to resist changes in H+ concentration when a strong acid or base is added (figure 5). When a strong acid is added to the fluid, the bicarbonate ions (HCO3 -) act as weak bases to tie up the H+ released by the stronger acid, and forms carbonic acid (H2CO3). The [HCO3-] in the extracellular fluid is normally around 25 mmol L-1 at rest and this has been reported to increase by an average of 5.3 mmol L-1 after the ingestion 0.3 g kg-1 of body mass of sodium bicarbonate (NaHCO3).[118] While further

H+

+

HCO3− (Weak base)

H2CO3 (Weak acid)

H2O + CO2

Exhaled

Fig. 5. The bicarbonate buffer system.

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research is required, 0.3 g of NaHCO3 per kg of body mass appears close to an optimal dose as it is generally accepted that 0.18 g kg-1 is the threshold for induced alkalosis,[119,120] and that dosages higher than 0.3 g kg-1 are likely to cause gastrointestinal discomfort in many subjects.[121] The most effective time to ingest NaHCO3 has not been accurately determined, however, most authors agree that it should occur between 60 and 90 minutes before exercise.[122-124] In addition, it has been suggested that chronic, lower doses of NaHCO3 administration over 5 days may be more applicable to athletes as they are less likely to have gastrointestinal irritation, especially on the day of performance.[125] NaHCO3 may be administered via the ingestion of capsules, in solution or through intravenous injections. While future research is needed, the literature suggests that the optimal ingestion protocol would involve 0.2–0.3 g kg-1 of NaHCO3 taken 60–120 minutes prior to exercise. Instead of the more commonly used NaHCO3, sodium citrate has also been used as the alkalizing substance in some studies.


The cell membrane is relatively impermeable to HCO-3 ,[126] and the ingestion of NaHCO3 does not increase the resting intracellular pH or muscle buffer capacity.[123] Rather, the ingestion of alkalizing agents (e.g. NaHCO3) prior to exercise

increases the extracellular buffer capacity and enhances the efflux of H+ from the muscle into the blood, maintaining muscle pH levels closer to normal during high-intensity exercise.[126,127] This should help to reduce the potential negative effects of H+ accumulation on repeated-sprint and high-intensity running performance. While the ergogenic benefits of alkaline ingestion have been largely attributed to the enhanced extracellular buffer capacity, it has recently been demonstrated that the ingestion of alkalizing agents (either NaHCO3 or sodium citrate) can also reduce the exercise-induced increase in extracellular K+.[128,129] 3.5.3 Effects on Team-Sport Performance

While many studies have investigated the effects of alkaline ingestion on high-intensity exercise performance, there is a paucity of studies that have investigated the effects of alkaline ingestion on team-sport performance. Bishop et al.[123] reported a significant improvement in power output during sprints 3, 4 and 5 of a repeatedsprint test (5 · 6-second sprints performed every 30 seconds), following the ingestion of 0.3 g kg-1 of NaHCO3 (figure 6). In support of this finding, Lavender and Bird[130] also reported NaHCO3 ingestion to be ergogenic for the performance of ten, 10-second cycle sprints with 50 seconds of recovery between each sprint. In contrast, NaHCO3

a 80

12.5 *

12.0

* *

11.5 11.0 10.5

Muscle lactate (mmol • kg dw−1)

13.0

Peak power (W • kg−1)

NaCl NaHCO3

b

70

*

60 50 40 30 20 10 0

10.0 1

2

3 4 Sprint number

5

Pre

Post

Fig. 6. (a) Peak power output (W kg-1) for each of the five sprints of the 5 · 6-second test of repeated-sprint ability (RSA), following the ingestion of either sodium bicarbonate (NaHCO3) or a placebo (NaCl). (b) Muscle lactate values pre and post the RSA test. Values are mean – standard error of the mean (n = 10). dw = dry weight; * indicates significantly different to placebo (p < 0.05).[123]


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increase in [HCO3 -] (~5.0 mmol L-1), is likely to improve both the repeated- and intermittentsprint performance of team-sport athletes. 3.5.4 Adverse Effects

In general, alkaline supplementation is safe when taken in recommended doses. However, both NaHCO3 and sodium citrate may cause gastrointestinal side effects (abdominal pain, nausea, cramps, diarrhoea) in some subjects.[133] Excessive doses of alkalotic substances may cause severe metabolic alkalosis with complications such as heart arrhythmias, although this is not known to have occurred in athletic situations.[134] 3.6 b-Alanine 3.6.1 Classification and Usage

b-Alanine is a non-essential amino acid that is common in many foods, especially meats.[135] b-Alanine is an important precursor of carnosine (b-alanyl-L-histidine),[136] an important muscle buffer that has been estimated to account for ~10% of the total buffering capacity in the human vastus lateralis muscle[137] (figure 7). Researchers have only recently begun to investigate the effects of b-alanine and, as a result, there is little information about the optimal dose or duration of supplementation to increase muscle carnosine levels. However, 4–6 weeks of b-alanine supplementation (4.8–6.4 g d-1 divided into 6–8 equal doses throughout the day) has been reported to

Protein Phosphate Carnosine Bmin vitro (μmol • L−1 H+ • g−1 dw • pH)

ingestion produced only a small (~2%), nonsignificant improvement in the performance of ten, 6-second running sprints (on a non-motorized treadmill), separated by 30-second recovery periods.[131] While it is possible that these contrasting findings are due to differing effects of NaHCO3 ingestion on running and cycling repeated-sprint performance, the more likely explanation is the relatively small change in blood pH reported in the final study (7.38–7.43), possibly due to the greater time delay (150 min) between ingestion and exercise. Thus, while confirmatory research is required, it appears that alkaline ingestion leading to a large increase in pH (~0.1 of a pH unit) and [HCO3 -] (~5.0 mmol L-1) is likely to improve repeated-sprint performance. Furthermore, while improved K+ regulation may contribute, the greater production of muscle lactate suggests that reduced inhibition of anaerobic glycolysis also plays a role (figure 6). Alkaline ingestion may also improve intermittent-sprint performance over the duration of a match, although the results are less convincing. Price et al.[132] reported that NaHCO3 ingestion significantly increased power output during a prolonged intermittent-sprint. test (10 · 3-minute blocks of. 90 seconds at 40% VO2peak, 60 seconds at 60% VO2peak, a 14-second maximal sprint and 16 seconds of rest). The results of this study are consistent with the findings of Bishop and Claudius[12] who investigated the effects of NaHCO3 ingestion on the performance of an intermittent-sprint test involving shorter sprints (two 36-minute ‘halves’ of repeated ~2-minute blocks; all-out 4-second sprint, 100 second of active recovery at . 35% VO2peak, 20-seconds rest), also performed on a cycle ergometer. It was reported that subjects performed significantly more work and achieved a higher peak power in almost half of the secondhalf sprints. Interestingly, the plasma [HCO3 -] peaked at 30.0 mmol L-1 immediately prior to the second half of the intermittent-sprint test (approximately 90 minutes after a second ingestion of 0.2 g kg-1 of NaHCO3), and this may have contributed to why performance was improved in the second but not the first half of the test. The limited research to date, therefore, suggests that alkaline ingestion, leading to a large

1007

160 140 120 100 80 60

⎫ ⎪ Nonprotein buffer ⎬ (∼90 μmol • L H ⎪ ⎭ −1

+

• g−1 dw • pH−1)

40 20 0

Fig. 7. Components of in vitro muscle buffer capacity (Bmin vitro).[138-142] dw = dry weight.

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increase muscle carnosine by ~40–60%.[137,143-146] One study has also reported that a slightly longer supplementation period (4.0–6.4 g d-1 for 10 weeks) can produce greater increases in muscle carnosine levels (~80% ).[137]

3.7 Bovine Colostrum


In theory, a 60% increase in muscle carnosine levels[137] should equate to approximately a 6.5% increase in muscle buffer capacity. As the accumulation of H+ has been reported to affect muscle contraction,[147] and to reduce the rate of anaerobic energy production,[148-150] greater muscle buffering (via b-alanine supplementation) may translate to improvements in multiple-sprint performance. In support of this, both repeated-sprint ability[151] and prolonged, intermittent-sprint ability[152] have been correlated with muscle buffer capacity. 3.6.3 Effects on Team-Sport Performance

In the limited number of studies conducted to date, it has been reported that b-alanine supplementation results in a significant increase in total work done at 110% of the power at maximum oxygen uptake (+13%),[137] a significant increase in performance during repeated, isokinetic, leg extensions[146] and a significant increase (+2.5%)[153] or no change[154] in time to exhaustion during an incremental cycle test. It has also recently been reported that b-alanine supplementation improved mean and peak power during a 30-second, all-out isokinetic task after a 110-minute simulated cycling race.[155] However, in the only study to date, b-alanine supplementation did not improve repeated-sprint ability (2 · [5 · 5-second sprints: 45 seconds of recovery]: 2 minute recovery).[156] Further studies, using intermittentsprint protocols or simulated match play, are required to confirm the hypothesis that b-alanine supplementation may improve the multiplesprint performance of team-sport athletes. 3.6.4 Adverse Effects

Large, acute doses of b-alanine (>10 mg kg-1 body mass) have been reported to induce temporary skin reactions (mild flushing and tingling sensations) in some subjects, which dissipate in ~2 hours.[136] It is for this reason that 6–8 servings, separated by at least 2 hours, are usually ª 2010 Adis Data Information BV. All rights reserved.

recommended to achieve a dose of 4.8–6.4 g d-1. No other studies appear to have investigated or reported possible adverse effects of b-alanine supplementation on indices of health.

3.7.1 Classification and Usage

Colostrum is the initial milk secreted by mammals after parturition (bovine colostrum is secreted by cows). It is a rich source of proteins, carbohydrate, fat, vitamins, minerals and biologicallyactive components such as antimicrobial molecules, immunoglobins and growth factors (e.g. insulinlike growth factor; IGF-1).[157] To date, relatively few studies have been conducted using bovine colostrum and it is therefore difficult to recommend an optimal dose. Most of the early studies supplemented with 60 g d-1 of bovine colostrum for 8–9 weeks.[158-161] However, subsequent studies reported some positive effects on endurance performance when supplementing with 10[162] and 20 g d-1.[163] As bovine colostrum supplementation has been hypothesized to potentiate adaptations to training, there is also some limited evidence that a supplementation period of >1[164] to 4[158] weeks is required. However, as all of these studies incorporated different outcome measures, they are difficult to compare and further studies are required to establish an optimal supplementation protocol for bovine colostrum.


Colostrum is important for human development,[165] and the presence of similar active components in bovine colostrum has led to the growing use of bovine colostrum in humans.[166] Dietary colostrum has been shown to increase circulating IGF-1 concentrations in some,[164,167] but not all[158,163] studies. As IGF-1 is believed to play an important role in the development of skeletal muscle,[168] this probably contributes to the positive effects that colostrum has been reported to have on skeletal muscle protein synthesis.[167] This suggests that colostrum might improve anabolic processes during the post-training recovery and augment improvements in muscle function and athletic performance in response to a specific training stimulus. It has also been proposed Sports Med 2010; 40 (12)


3.7.3 Effects on Team-Sport Performance

To date, there is only one published study that has investigated the effects of bovine colostrum supplementation (60 g d-1 for 8 weeks), in conjunction with field-hockey training, on team-sport performance.[161] Compared with a placebo, there were no significant differences for improvements in aerobic performance (shuttle test), a trend for greater improvements in vertical jump height (2.1 – 0.7 cm vs 0.3 – 0.8 cm; p = 0.12) and a significantly greater improvement in 5 · 10 m shuttle sprint performance (-0.64 – 0.09 vs -0.33 – 0.09 seconds; p = 0.023). While the mechanisms by which colostrum exerted its ergogenic effects were not investigated, it was hypothesized that colostrum may have potentiated improvements in those systems which were trained extensively (the training programme emphasized speed and power training). Other studies, not conducted on team-sport athletes, have produced mixed results. Bovine colostrum supplementation in conjunction with endurance training has been reported to improve the recovery from intense exercise in physically-active male runners,[158] but not elite, female rowers.[160] Colostrum has also been reported to have a ‘likely benefit’ (+1.9%) on improvements in 40 km time-trial performance during high-intensity training,[162] and to augment training-induced improvements in cycle time-trial performance following a 2-hour ride.[163] Thus, while more research is needed, especially on teamsport athletes and using team-sport-relevant testing, there is some evidence that bovine colostrum supplementation may augment training-induced


improvements in sprint, jump and endurance performance. 3.7.4 Adverse Effects

No adverse effects of bovine colostrum supplementation have been reported in the literature. However, it should also be noted that there appear to be no studies that have specifically investigated potential adverse effects of prolonged bovine colostrum supplementation. 3.8 b-Hydroxy-b-Methylbutyrate 3.8.1 Classification and Usage

b-Hydroxy-b-methylbutyrate (HMB) is a naturally occurring metabolite of the essential BCAA, leucine. It is produced endogenously in small amounts (2–10% of leucine oxidation proceeds to HMB[170]) and can also be consumed through both plant (e.g. citrus fruits) and animal (e.g. catfish, breast milk) foods. As a dietary supplement, HMB is usually marketed as calcium-HMB-monohydrate. The recommended dose of HMB is 3 g d-1 for 3–8 weeks, based on the dose-dependent manner in which it has been reported to affect resistance training-induced gains in the lean body mass of untrained subjects (figure 8). It should be noted, however, that the absence of a positive effect for doses >3 g d-1 is based on one study only[171] and further research is warranted, especially with well trained subjects.

Change in lean body mass (kg)

that colostrum supplementation during training may result in greater improvements in the ability to recover from intense exercise.[158] Finally, compared with a placebo, 9 weeks of bovine colostrum supplementation, in conjunction with precompetition training, has been reported to result in a 22% greater increase in estimated,[160] but not titrated,[159] blood buffer capacity. As a higher blood buffer capacity has been associated with both improved repeated-sprint ability[123,169] and prolonged intermittent-sprint ability,[12] increases in blood buffer capacity may improve team-sport performance.

1009

1.80 1.60 1.40 1.20 1.00 0.80 0.60 0.40 0.20 0 −0.20

0

1.5

3

6

Dose (g • d −1) Fig. 8. Changes in lean body mass during 3–8 weeks of resistance training are related to the b-hydroxy-b-methylbutyrate dose.[171-173]

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3.8.4 Adverse Effects

HMB has been proposed to function as an anti-catabolic agent and to decrease exerciseinduced muscle damage.[172] This has been inferred from decreases in urine 3-methylhistidine and plasma enzymes following resistance training[172,174,175] and endurance exercise[176] in untrained subjects. However, decreases in training-induced markers of catabolism have not been observed following HMB supplementation in trained subjects.[177,178] This may be explained by the observation that adaptations to physical training cause subsequent exercise to be accompanied by less protein turnover and breakdown in trained athletes[2] thus rendering the proposed benefits of HMB less likely in trained athletes.[179] It has also been proposed that HMB may promote the synthesis of cholesterol needed to form and stabilize cell membranes.[180] By minimizing protein breakdown and the damage to cells that may occur during intense training, it is hypothesized that HMB may promote training-induced increases in both lean body mass and strength. 3.8.3 Effects on Team-Sport Performance

To date, only one study has specifically evaluated the effects of HMB supplementation on team-sport performance.[178] It was reported that HMB supplementation (3 g d-1) during winter resistance/agility training did not produce greater improvements in repeated-sprint ability (12 · 6-second sprints with 30 seconds of recovery) than a placebo. Three studies have also reported no benefits of HMB supplementation during pre-season training on the anaerobic power (10to 60-second cycle sprint) of team-sport athletes.[177,181,182] With few exceptions,[183] HMB supplementation also does not improve indices of aerobic fitness.[176,181] Due to its reported ability to promote adaptations associated with resistance training,[172,174,175,184] HMB may be of benefit to team-sport athletes who need to increase lean body mass or strength. However, as enhanced gains in lean body mass and strength have tended not to be replicated in trained athletes,[177,181,185,186] the benefits of HMB supplementation for elite, team-sport athletes remain unproven and further research is required.


There are no reports of adverse effects of the recommended 3 g d-1 dose of HMB in the limited number of short-term (1–8 weeks) studies. These include no reported changes in blood pressure, lipid profile, renal function, liver enzymes, electrolytes, haematological parameters, urinalysis, testosterone, cortisol or male fertility.[171,180,187] There are currently no data on the long-term (>8 weeks) effects of HMB supplementation, or the effects of taking more than the recommended dose.

4. Risks While most of the supplements described in this review appear safe when using the recommended dose, it needs to be remembered that athletes often work on the ‘more must be better’ principle, and there are studies indicating that people are consuming more than the recommended doses of some supplements. The effects of these higher doses on indices of health remain unknown, and further research is warranted. It needs also to be remembered that very little is known about the potential adverse effects of ingesting multiple supplements. Supplements that have been demonstrated to be safe when ingested on their own may have adverse effects when combined with other supplements. The use of supplements by adolescents needs to be carefully considered due to evidence suggesting that such use may lead to an increased risk for subsequent use of illegal, performance-enhancing substances.[26] If a team-sport athlete does decide to take a supplement, they need to ensure that they are getting what they think they are getting. Studies investigating the components of various supplements have reported more than 85% to contain less product than what was labelled.[188] Of greater concern is the possibility that some supplements may contain undeclared substances, banned by WADA, which may lead to a positive drugs test.[188,189] Baume et al.[190] reported that 19 of the 103 (18%) supplements that they tested contained substances not disclosed on the label. It is important to remember that athletes who test positive for banned substances are, in most Sports Med 2010; 40 (12)


jurisdictions, held responsible for what is found in their body, regardless of whether they knowingly ingested the banned substance.[191] For example, in 2008, a Canadian bobsled athlete was banned for 20 months based on a positive test for nandrolone, which was subsequently discovered to be an unlabelled ingredient in a supplement he was taking. 5. Conclusions and Recommendations for Future Research A well designed diet that meets the energy and nutrient intake needs, and incorporates the proper timing of meals, is the foundation upon which optimal training and performance can be developed. Nevertheless, there is the common belief by team-sport athletes and their coaches that the appropriate ingestion of some dietary supplements, in conjunction with well designed training, can enhance team-sport performance. While more research is required, evidence is emerging to support the performance-enhancing claims of some, but not all, dietary supplements that have been proposed to improve team-sport performance. For example, there is good evidence that caffeine, Cr and NaHCO3 ingestion can improve multiple-sprint performance. The evidence is not so strong for the performance-enhancing benefits of b-alanine or colostrum, although further research is warranted using more team-sport-specific performance tests. Current evidence does not support the ingestion of ribose, BCAAs or HMB, especially in well trained athletes. While many studies have evaluated the performance-enhancing effects of most dietary supplements, more research needs to be conducted using team-sport athletes and using teamsport-relevant testing. Dietary supplements that enhance some types of athletic performance may not necessarily enhance team-sport performance (and vice versa). Furthermore, there is no guarantee that the effectiveness of dietary supplements, which improve isolated performance (i.e. single-sprint or jump performance), will remain in the context of a team-sport match. Anecdotal reports suggest that team-sport athletes often ingest more than one dietary supplement. More ª 2010 Adis Data Information BV. All rights reserved.

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research is required to investigate the effects of ingesting multiple supplements (both on performance and health). Notwithstanding the real need for applied research in ‘real-life’ settings, it is important that basic research is not neglected.[192] This should include initial research to determine the optimal dose, timing and number of days/weeks to ingest the various dietary supplements proposed to enhance team-sport performance. Without such information, researchers run the risk of obtaining negative findings not because the dietary supplement is not efficacious, but because of an inappropriate supplementation protocol. In addition, despite the need to determine the effects of supplements in the ‘real world’ (e.g. regular matches, limited time devoted to physical training, coingestion of other dietary supplements), efficacy trials are first required to test whether a supplement has a substantial positive or negative effect on actual sports performance when delivered under optimum/ideal conditions. Efficacy trials (both in the laboratory and in the field) are characterized by strong control in that a standardized intervention is delivered in a uniform and tightly controlled fashion to a specific, often narrowly defined, homogenous, motivated population. This approach should include random selection of participants, random assignment to conditions and the use of placebos (ideally double blind) or cross-over designs. Subsequent research is then required to determine if the intervention effect is large enough to make a difference in an applied setting or if it interacts positively or negatively with other training/nutrition factors. Acknowledgements No sources of funding were used to assist in the preparation of this review. The author has no conflicts of interest that are directly relevant to the content of this review.

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163. Coombes JS, Conacher M, Austen SK, et al. Dose effects of oral bovine colostrum on physical work capacity in cyclists. Med Sci Sports Exerc 2002 Jul; 34 (7): 1184-8 164. Mero A, Miikkulainen H, Riski J, et al. Effects of bovine colostrum supplementation on serum IGF-I, IgG, hormone, and saliva IgA during training. J Appl Physiol 1997 Oct 1; 83 (4): 1144-51 165. Kelly D, Coutts AG. Early nutrition and the development of immune function in the neonate. Proc Nutr Soc 2000; 59: 177-85 166. Anderson O. Bioenervi floods Finland, but can it really cut recuperation times [letter]? Run Res News 1994; 10: 11 167. Burrin DG, Davis TA, Ebner S, et al. Nutrient-independent and nutrient-dependent factors stimulate protein synthesis in colostrum-fed newborn pigs. Pediatr Res 1995 May; 37 (5): 593-9 168. Liu JP, Baker J, Perkins AS, et al. Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r). Cell 1993 Oct 8; 75 (1): 59-72 169. Bishop D, Lawrence S, Spencer M. Predictors of repeatedsprint ability in elite female hockey players. J Sci Med Sport 2003; 6 (2): 199-209 170. Van Koevering M, Nissen S. Oxidation of leucine and alpha-ketoisocaproate to b-hydroxy-b-methylbutyrate in vivo. Am J Physiol 1992 Jan; 262 (1 Pt 1): E27-31 171. Gallagher PM, Carrithers JA, Godard MP, et al. b-hydroxyb-methylbutyrate ingestion, part II: effects on hematology, hepatic and renal function. Med Sci Sports Exerc 2000 Dec; 32 (12): 2116-9 172. Nissen S, Sharp R, Ray M, et al. Effect of leucine metabolite b-hydroxy-b-methylbutyrate on muscle metabolism during resistance-exercise training. J Appl Physiol 1996 Nov 1; 81 (5): 2095-104 173. Rice DE, Sharp R, Rathmacher J. Role of b-hydroxyb-methylbutyrate (HMB) during acute exercise-induced proteolysis [abstract]. Med Sci Sports Exerc 1995; 27: S220 174. Jowko E, Ostaszewski P, Jank M, et al. Creatine and b-hydroxy-b-methylbutyrate (HMB) additively increase lean body mass and muscle strength during a weighttraining program. Nutrition 2001 Jul-Aug; 17 (7-8): 558-66 175. Panton LB, Rathmacher JA, Baier S, et al. Nutritional supplementation of the leucine metabolite b-hydroxyb-methylbutyrate (HMB) during resistance training. Nutrition 2000 Sep; 16 (9): 734-9 176. Knitter AE, Panton L, Rathmacher JA, et al. Effects of b-hydroxy-b-methylbutyrate on muscle damage after a prolonged run. J Appl Physiol 2000; 89 (4): 1340-4 177. Hoffman JR, Cooper J, Wendell M, et al. Effects of b-hydroxy b-methylbutyrate on power performance and indices of muscle damage and stress during high-intensity training. J Strength Cond Res 2004 Nov; 18 (4): 747-52 178. Kreider RB, Ferreira M, Greenwood M, et al. Effects of calcium b-HMB supplementation during training on markers of catabolism, body composition, strength and sprint performance. J Exerc Physiol-online 2000; 3 (4): 48-59 179. Slater GJ, Jenkins D. b-hydroxy-b-methylbutyrate (HMB) supplementation and the promotion of muscle growth and strength. Sports Med 2000 Aug; 30 (2): 105-16

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180. Nissen S, Sharp RL, Panton L, et al. b-hydroxy-b-methylbutyrate (HMB) supplementation in humans is safe and may decrease cardiovascular risk factors. J Nutr 2000 Aug; 130 (8): 1937-45 181. O’Connor DM, Crowe MJ. Effects of b-hydroxy-b-methylbutyrate and creatine monohydrate supplementation on the aerobic and anaerobic capacity of highly trained athletes. J Sports Med Phys Fitness 2003 Mar; 43 (1): 64-8 182. O’Connor DM, Crowe MJ. Effects of six weeks of bhydroxy-b-methylbutyrate (HMB) and HMB/creatine supplementation on strength, power, and anthropometry of highly trained athletes. J Strength Cond Res 2007 May; 21 (2): 419-23 183. Vukovich MD, Dreifort GD. Effect of b-hydroxy b-methylbutyrate on the onset of blood lactate accumulation and VO2 peak in endurance-trained cyclists. J Strength Cond Res 2001 Nov; 15 (4): 491-7 184. Nissen SL, Sharp RL. Effect of dietary supplements on lean mass and strength gains with resistance exercise: a metaanalysis. J Appl Physiol 2003 Feb 1; 94 (2): 651-9 185. Ransone J, Neighbors K, Lefavi R, et al. The effect of b-hydroxy b-methylbutyrate on muscular strength and body composition in collegiate football players. J Strength Cond Res 2003 Feb; 17 (1): 34-9 186. Kreider RB, Ferreira M, Wilson M, et al. Effects of calcium b-hydroxy-b-methylbutyrate (HMB) supplementation during resistance-training on markers of catabolism, body


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Correspondence: Professor David Bishop, Institute of Sport, Exercise and Active Living (ISEAL) and School of Sport and Exercise Science, Victoria University, PO Box 14428, Melbourne, VIC 8001, Australia. E-mail: [email protected]

Sports Med 2010; 40 (12)

Sports Med 2010; 40 (12): 1019-1035 0112-1642/10/0012-1019/$49.95/0

REVIEW ARTICLE


Fundamental Movement Skills in Children and Adolescents Review of Associated Health Benefits David R. Lubans,1 Philip J. Morgan,1 Dylan P. Cliff,2 Lisa M. Barnett3 and Anthony D. Okely2 1 School of Education, University of Newcastle, Callaghan Campus, Newcastle, New South Wales, Australia 2 Interdisciplinary Educational Research Institute, University of Wollongong, Wollongong, New South Wales, Australia 3 Centre for Physical Activity and Nutrition, Deakin University, Melbourne, Victoria, Australia

Contents Abstract. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Methods. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.1 Identification of Studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2 Criteria for Inclusion/Exclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.3 Criteria for Assessment of Study Quality. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.4 Categorization of Variables and Level of Evidence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1 Overview of Studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2 Overview of Study Quality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3 Psychological Benefits . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4 Physiological Benefits . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.5 Behavioural Benefits . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Discussion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1 Overview of Findings . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2 Strengths and Limitations. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Abstract

1019 1021 1021 1021 1021 1022 1022 1022 1022 1023 1030 1030 1031 1031 1032 1032

The mastery of fundamental movement skills (FMS) has been purported as contributing to children’s physical, cognitive and social development and is thought to provide the foundation for an active lifestyle. Commonly developed in childhood and subsequently refined into context- and sport-specific skills, they include locomotor (e.g. running and hopping), manipulative or object control (e.g. catching and throwing) and stability (e.g. balancing and twisting) skills. The rationale for promoting the development of FMS in childhood relies on the existence of evidence on the current or future benefits associated with the acquisition of FMS proficiency. The objective of this systematic review was to examine the relationship between FMS competency and potential health benefits in children and adolescents. Benefits were defined in terms of psychological, physiological and behavioural outcomes that

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can impact public health. A systematic search of six electronic databases (EMBASE, OVID MEDLINE, PsycINFO, PubMed, Scopus and SportDiscus) was conducted on 22 June 2009. Included studies were crosssectional, longitudinal or experimental studies involving healthy children or adolescents (aged 3–18 years) that quantitatively analysed the relationship between FMS competency and potential benefits. The search identified 21 articles examining the relationship between FMS competency and eight potential benefits (i.e. global self-concept, perceived physical competence, cardio-respiratory fitness [CRF], muscular fitness, weight status, flexibility, physical activity and reduced sedentary behaviour). We found strong evidence for a positive association between FMS competency and physical activity in children and adolescents. There was also a positive relationship between FMS competency and CRF and an inverse association between FMS competency and weight status. Due to an inadequate number of studies, the relationship between FMS competency and the remaining benefits was classified as uncertain. More longitudinal and intervention research examining the relationship between FMS competency and potential psychological, physiological and behavioural outcomes in children and adolescents is recommended.

Fundamental movement skills (FMS) are considered to be the building blocks that lead to specialized movement sequences required for adequate participation in many organized and non-organized physical activities for children, adolescents and adults.[1,2] Commonly developed in childhood and subsequently refined into contextand sport-specific skills,[2-4] they include locomotor (e.g. running and hopping), manipulative or object control (e.g. catching and throwing) and stability (e.g. balancing and twisting) skills.[1] The mastery of FMS has been purported as contributing to children’s physical, cognitive and social development[5] and is thought to provide the foundation for an active lifestyle.[1,3] Recently, FMS competency has been proposed to interact with perceptions of motor competence and healthrelated fitness to predict physical activity and subsequent obesity from childhood to adulthood.[3] While children may naturally develop a rudimentary form of fundamental movement pattern, a mature form of FMS proficiency is more likely to be achieved with appropriate practice, encouragement, feedback and instruction.[1,2] Children who do not receive adequate motor skill instructions and practice may demonstrate developmental delays in their gross motor ability.[6] As such, ª 2010 Adis Data Information BV. All rights reserved.

early childhood physical activity guidelines, such as the National Association for Sport and Physical Education’s (NASPE) Active Start, indicate that the development of movement skills should be a key component of early childhood education programmes.[7] Likewise, FMS competency is identified in National Standards as a primary goal of quality elementary school physical education in the US[8] and represents an indicator of achievement for elementary school children in England’s national physical education curriculum.[9] Despite this focus, the prevalence of FMS mastery among children in some countries appears inadequately low.[10,11] For example, in a recent US study of 9- to 12-year-old children, only half of the students assessed demonstrated proficiency in basketball throwing and dribbling motor tasks.[11] Similarly, an Australian study[12] involving students from years 4, 6, 8 and 10 (aged 9–15 years) found that the prevalence of mastery only exceeded 40% for one skill in one group (i.e. overarm throw, year 10 boys). The rationale for promoting the development of FMS in childhood relies on the existence of evidence on the current or future benefits associated with the acquisition of FMS proficiency. Despite support for FMS promotion among motor Sports Med 2010; 40 (12)

Benefits of FMS Competency in Youth

behaviourists[3] and physical educators,[13] the potential benefits of FMS competency have not yet been methodically evaluated. The purpose of this review is to systematically examine the potential psychological, physiological and behavioural public health benefits associated with FMS competency in children and adolescents. 1. Methods 1.1 Identification of Studies

The Quality of Reporting of Meta-analyses statement (QUOROM)[14] was consulted and provided the structure for this review. A systematic search of six electronic databases (EMBASE, OVID MEDLINE, PsycINFO, PubMed, Scopus and SportDiscus) was conducted from their year of inception to 22 June 2009. Individualized search strategies for the different databases included combinations of the following keywords: ‘child’, ‘adolescent’, ‘youth’, ‘movement skill’, ‘motor skill’, ‘actual competence’, ‘object control’, ‘locomotor skill’ and ‘motor proficiency’. Only articles published or accepted for publication in refereed journals were considered for review. Conference proceedings and abstracts were not included. In the first stage of the research, titles and abstracts of identified articles were checked for relevance. In the second stage, fulltext articles were retrieved and considered for inclusion. In the final stage, the reference lists of retrieved full-text articles were searched and additional articles known to the authors were assessed for possible inclusion. Eighteen expert informants in the area were also contacted to suggest or provide relevant manuscripts. 1.2 Criteria for Inclusion/Exclusion

Two authors (DRL and DPC) independently assessed the eligibility of the studies for inclusion according to the following criteria: (i) participants were aged 3–18 years (research articles that focused on youth from special populations were not included, e.g. overweight/obese, developmental coordination disorder); (ii) process (i.e. concerned with process or technique also known as qualitative) or product (i.e. concerned with outª 2010 Adis Data Information BV. All rights reserved.

1021

come) assessment of at least two FMS (e.g. run, vertical jump, horizontal jump, hop, dodge, leap, gallop, side gallop, skip, roll, throw, stationary dribble, catch, kick, two-handed strike, static balance); (iii) summary/subtest measure of FMS competency (e.g. locomotor or object control summary score) was used in analyses; (iv) quantitative assessment of potential health benefit of FMS competency (i.e. psychological, physiological or behavioural); (v) quantitative analysis of the relationship between FMS and potential benefits in any of the above domains; (vi) cross-sectional, longitudinal or experimental/quasi-experimental study design; and (vii) published in English. As this review focused on the potential benefits of FMS, which are gross motor skills,[1] studies that used measurement batteries that included fine motor skills were excluded to preserve internal validity. 1.3 Criteria for Assessment of Study Quality

Two authors (DRL and PJM) independently assessed the quality of the studies that met the inclusion criteria. The criteria for assessing the quality of the studies were adapted from the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement[15] and the Consolidated Standards of Reporting Trials (CONSORT) statement.[16] A formal quality score for each study was completed on a 6-point scale by assigning a value of 0 (absent or inadequately described) or 1 (explicitly described and present) to each of the following questions listed: (i) Did the study describe the participant eligibility criteria? (ii) Were the participants randomly selected (or for experimental studies, was the process of randomization clearly described and adequately carried out)? (iii) Did the study report the sources and details of FMS assessment and did the instruments have acceptable reliability for the specific age group? (iv) Did the study report the sources and details of assessment of potential benefits and did all of the methods have acceptable reliability? (v) Did the study report a power calculation and was the study adequately powered to detect hypothesized relationships? (vi) Did the study report the numbers of individuals who completed each of the different measures Sports Med 2010; 40 (12)

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and did participants complete at least 80% of FMS and benefit measures? Studies that scored 0–2 were regarded as low quality studies, studies that scored 3–4 were classified as medium quality and those that scored 5–6 were classified as high quality. 1.4 Categorization of Variables and Level of Evidence

The benefits were categorized as follows: psychological (e.g. physical self-perception), physiological (e.g. fitness and healthy weight status) and behavioural (e.g. time spent in physical activity and sedentary behaviours). It should be noted that studies assessing the benefit of fitness in this review will be discussed in terms of whether they used product- or process-oriented motor skill assessments. This is because product-oriented motor skill assessments can view certain fitness constructs (such as strength and speed) as part of the motor skill assessment, unlike processorientated assessments that are concerned with the quality or technique of the skill execution. Results were coded using the methods first described by Sallis et al.[17] and more recently by Hinkley et al.[18] and Van der Horst et al.[19] The relationship between FMS competency and each potential benefit was determined by examining the percentage of studies that reported a statistically significant relationship (i.e. between FMS competency and benefit) and is explained in table I. If only 0–33% of the included studies reported a relationship between FMS competency and the benefit, the result was categorized as no association (0). If 34–59% of the studies reported statistically significant relationships between FMS competency and the benefit, the result was categorized as inconsistent

or uncertain (?). If 60–100% of studies reported a positive relationship between FMS competency and the benefit, the result was coded as a positive association (+). The methods of Sallis et al.[17] were modified to address the issue of study quality and additional coding was conducted based on studies assessed as high quality. If 60–100% of high quality studies (‡4) found a positive relationship between FMS competency and the benefit, the result was coded as having strong evidence for a positive association (++). 2. Results 2.1 Overview of Studies

A total of 1793 potentially relevant articles were identified using database searches (figure 1). Following feedback from international experts and checking the reference lists of included studies, a total of 21 articles satisfied the inclusion criteria and were included in the review (table II). The flow of studies through the review process and the reasons for exclusion are reported in figure 1. Of the included articles, 15 reported on cross-sectional studies, four on longitudinal studies and two on experimental studies. Nine studies were conducted in Australia, eight in the US, and one each in Canada, Scotland, Belgium and Germany. The number of study participants ranged from 29[23] to 4363.[40] 2.2 Overview of Study Quality

There was 96% agreement between authors on the study assessment criteria and full consensus was achieved after discussion. Results from the study quality assessment are reported in table III. Seven studies were identified as high

Table I. Rules for classifying the association between potential benefits and fundamental movement skills (FMS) competency Studies supporting association (%)

Summary code

Explanation of code

0–33

0

No association

34–59

?

Inconsistent or uncertaina

60–100

-

Negative association

60–100

+

Positive association

60–100

++

Strong evidence for a positive associationb

a

The relationship between benefit and FMS competency was considered uncertain if 60% of high quality studies (‡4 studies) reported a positive association.


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Stage 1 1793 potentially relevant articles identified using database search 70 EMBASE 388 PsycINFO 481 PubMed 389 OVID MEDLINE 34 SCOPUS 431 SportDiscus® 1741 Studies excluded based on titles and review of abstracts 766 Special population 119 Validity or reliability study 33 Review study 162 FMS not assessed 10 Adult study participants 160 Duplicate 491 Other Stage 2 52 Full-text articles reviewed 33 Studies excluded based on review of full-text article 5 Special population 2 Adult study participants 1 Validity or reliability study 10 FMS composite score not used in analyses 6 FMS composite score included fine motor skills 8 No benefits assessed 1 Other

Stage 3 19 Reference lists searched 18 International experts in FMS contacted Additional articles known to the authors assessed for relevance 21 Articles included in review Fig. 1. Flow of studies through the review process. FMS = fundamental movement skills.

quality,[24,29,30,33,34,36,40] 13 studies were rated as medium quality[11,20-23,25,26,28,32,35,37,39,41] and one study was classified as low quality.[31] Most of the studies used valid and reliable measures of FMS assessment and also reported the reliability data from their potential benefits. None of the studies reported power calculations to determine if the studies were adequately powered to detect the hypothesized relationships. 2.3 Psychological Benefits

A summary of the associations between FMS competency and potential benefits is reported in table IV. Three studies examined the relationship ª 2010 Adis Data Information BV. All rights reserved.

between perceived physical competence and FMS competency.[21,29,34] Perceived competence was associated with at least one aspect of FMS competency in all three studies. Perceived competence refers to an individual’s perception of their actual motor proficiency. In a 6-year longitudinal study, Barnett et al.[34] found that object control competency in childhood was associated with perceived physical competence in adolescence. Only one study assessed the association between FMS competency and global self-concept.[20] Martinek and colleagues[20] examined the impact of a motor skill intervention on FMS and self-concept in a sample of 344 children. Although FMS and self-concept improved over the study period, the Sports Med 2010; 40 (12)

Type of study

Analyses

Martinek et al.[20]

344 children; 6–10 y; NR; US

Experimental

ANCOVA and bivariate correlation

Rudisill et al.[21]

218 children; 9–11 y; 3, 4 and 5; US

Crosssectional

Bivariate correlation

Marshall and Bouffard[22]

200 children; NR; 1 and 4; Canada

Experimental

ANOVA and bivariate correlation

Reeves et al.[23]

29 children; 5–6 y; kindergarten; US

Crosssectional


Okely et al.[24]

2026 adolescents; 13–16 y; 8 and 10; Australia

Crosssectional

Bivariate correlations and linear regression

FMS measurea PRODUCT

Benefits assessed

Results

KTK: one-legged obstacle jumping, jumping from side to side as well as sideway movements

Global selfconcept (Self Concept Scale for Children)

FMS and self-concept improved in the intervention group over the study period. However, the relationship between self-concept and FMS was nonsignificant at baseline and post-test

Locomotor (standing long jump, 50-yard dash and shuttle run) and object control (two ball throws short and long distance)

Perceived physical competence (Motor Perceived Competence Scale)

Locomotor and object control proficiency associated with perceived competency

CRF (multi-stage fitness test)

Object control and locomotor FMS competency associated with CRF

CRF (half-mile walk/run)

CRF (half-mile walk/run) was positively associated with balance and bilateral coordination


FMS competency associated with CRF controlling for gender and grade at school

PROCESS

Test of gross motor development (run, gallop, hop, leap, horizontal jump, slide, skip, striking a stationary ball, stationary dribble, catch, kick, overhand throw and underhand roll), characterized into locomotor and object control subtests Bruininks Oseretsky Test of Motor Proficiency: (i) running speed and agility; (ii) balance; and (iii) bilateral coordination subtests FMS: A Manual for Classroom Teachers, (run, vertical jump, catch, overhand throw, kick, strike)

Continued next page

Lubans et al.

Sports Med 2010; 40 (12)

Sample; age; school grade; location

Study

1024


Table II. Summary of included studies

Study

Type of study

Okely et al.[25]

982 adolescents; 13–16 y; 8 and 10; Australia

Crosssectional

Linear regression analysis (controlling for gender, grade, SES, geographic location)

McKenzie et al.[26]


Longitudinal

Bivariate correlation and linear regression

Okely et al.[27]

4363 children and adolescents; NR; 4, 6, 8 and 10; Australia

Crosssectional

Logistic regression modelling and multiple linear regression

Graf et al.[28]

668 children; 6.7 – 0.4 y; NR; Germany

Crosssectional

ANCOVA (adjusted for age and gender) and bivariate correlation

Southall et al.[29]

142 children; 10.8 y; 5 and 6; Australia

Crosssectional

ANCOVA

Fisher et al.[30]

394 children; 4.2 – 0.5 y; NR; Scotland

Crosssectional


Analyses


Benefits assessed

Results

PA (APARQ)

FMS associated with time in organized PA but not time in non-organized PA controlling for gender and school grade

PA (PAR 7-day questionnaire) and adiposity (skinfolds: triceps and subscapular)

Inverse association between adiposity and FMS in boys but not girls Jumping related to PA at age 12 for girls FMS at ages 4–6 did not predict PA at age 12

BMI z-score and waist circumference

FMS (locomotor) inversely associated with BMI z-score in children and adolescents

BMI z-score, time spent in organized PA (parent questionnaire) and watching TV (child questionnaire)

Inverse association between BMI and FMS Positive association between FMS and PA Nonsignificant association between FMS and TV watching

Test of Gross Motor Development 2

BMI z-score, perceived physical competence (SPPC)

Overweight children had lower total FMS and locomotor FMS Overweight children had lower perceived physical competence scores No difference between overweight and normal weight children for object control skills

Movement Assessment Battery: 15 skills including jumps, balance, skips, ball exercises and throwing

PA (accelerometer)

FMS associated with total PA and MVPA

PROCESS FMS: A Manual for Classroom Teachers (run, vertical jump, catch, overhand throw, kick, strike)

Lateral jump, catch, and one foot balance

FMS: A Manual for Classroom Teachers (run, vertical jump, catch, overhand throw, kick, strike) KTK: balancing backwards, one-legged obstacle jumping, jumping from side to side as well as sideway movements

Continued next page

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Sports Med 2010; 40 (12)




Table II. Contd

Study

Type of study

Hamstra-Wright et al.[31]


Crosssectional

Linear stepwise multiple regression (controlling for gender and age) and bivariate correlation

Castelli and Valley[32]

230 children; 9.5 – 1.6 y; NR; US

Crosssectional

Barnett et al.[33]

928 children, 244 adolescents (follow-up); 16.4 y; 10 and 11; Australia

Barnett et al.[34]

928 children, 250 adolescents (PA model): 227 adolescents


Benefits assessed

Results

Test of Gross Motor Development 2 (run, gallop, hop, leap, horizontal jump, slide, striking a stationary ball, stationary dribble, catch, kick, overhand throw and underhand roll), characterized into locomotor and object control subtests

PA (sport experience questionnaire)

Participation in organized and non-organized PA was associated with locomotor competency


SCPEAP: scoring and protocols including: basketball dribble and pass, paddle bat hit and overhand ball throwing to provide a summative score for FMS competency

PA (parent and child 7-d questionnaire, pedometer), BMI z-score, flexibility, CRF (PACER), muscular endurance (curlups and push-ups) and flexibility (sit and reach)

FMS competency associated with CRF, muscular endurance, flexibility and PA No relationship between FMS and BMI z-score

Longitudinal (6-y followup)

General linear regression model controlling for gender

Get Skilled, Get Active: object control (kick, catch, overhand throw) locomotor (hop, side gallop, vertical jump)


Childhood object control proficiency associated with CRF in adolescence


Bivariate correlation and structural equation modelling to test

Get Skilled, Get Active: object control (kick, catch, overhand throw)

APARQ, CRF (multi-stage fitness test) and perceived physical

Childhood object control was associated with adolescent perceived sports competence Childhood object control

Analyses

PROCESS

Continued next page

Lubans et al.

Sports Med 2010; 40 (12)


1026


Table II. Contd

Study


Type of study

(fitness model); 16.4 y; NR; Australia

Analyses


Benefits assessed

Results

PROCESS

for mediators

locomotor (hop, side gallop, vertical jump)

competence (PSPP)

associated with adolescent PA Locomotor competency was associated with perceived competence in girls only Locomotor competency was not associated with PA in either girls or boys Locomotor competency was associated with CRF in girls only

180 children; 10.5 – 0.8 y; 4 and 5; US

Crosssectional


SCPEAP scoring and protocols including: basketball dribble and pass, overhand ball throwing and gymnastic movement and balance

PA (ACTIVITYGRAM questionnaire), physical fitness (CRF, strength, endurance, flexibility and BMI z-score)

FMS competency associated with PA and physical fitness

Hume et al.[35]

248 children; 9–12 y; NR; Australia

Crosssectional

Linear regression and bivariate correlation

FMS: A Manual for Classroom Teachers, object control (overhand throw, two handed strike, kick) and locomotor (sprint run, dodge and vertical jump)

PA (accelerometer) and BMI z-scores

MPA, VPA and MVPA associated with FMS proficiency in boys VPA associated with FMS proficiency in girls BMI z-scores not associated with FMS in boys or girls

Williams et al.[36]


Crosssectional


Children’s Activity and Movement in preschool study motor skill protocol: locomotor (run, jump, slide, gallop, leap and hop) and object control (throw, roll, kick, catch, strike and dribble)

BMI z-score and PA (accelerometry)

Object control and locomotor proficiency associated with PA in 4-y-olds, but not 3-y-olds BMI z-score not associated with object control or locomotor proficiency in 3- or 4-y-olds

Continued next page

1027

Sports Med 2010; 40 (12)

Erwin and Castelli[11]



Table II. Contd

Study


Type of study

Barnett et al.[37]

928 children, 276 adolescents (follow-up); 16.4 y; NR; Australia


General linear model controlling for grade and gender, general linear model controlling for grade and logistic regression

D’Hondt et al.[38]

117 children; 5–10 y; NR; Belgium

Crosssectional

Cliff et al.[39]

46 children; 4.3 – 0.7 y; preschool; Australia

Crosssectional

Results

Get Skilled, Get Active: object control (kick, catch, overhand throw) locomotor (hop, side gallop, vertical jump)

PA (APARQ)

Object control proficiency in childhood associated with time in MVPA and time in organized PA Object control proficiency in childhood was associated with probability of participating in VPA but not associated with probability of participating in organized PA Locomotor proficiency did not predict time in or probability of participating in any form of adolescent PA

ANOVA and bivariate correlation

Movement Assessment Battery for Children: ball skills, static and dynamic balance

BMI z-score and PA (accelerometers)

FMS competency (ball skills and balance) was higher in normal and overweight compared with obese children FMS competency (ball skills and balance) associated with PA

Bivariate correlation and linear regression

Test of Gross Motor Development 2 (run, gallop, hop, leap, horizontal jump, slide, striking a stationary ball, stationary dribble, catch, kick, overhand throw and underhand roll), characterized into locomotor and object control subtests

PA and sedentary behaviour (accelerometer)

Object control proficiency was associated with moderate PA in boys Locomotor proficiency was not significantly associated with PA in boys Locomotor proficiency and overall FMS proficiency were negatively associated with PA in girls Object control proficiency was not associated with PA in girls FMS not associated with sedentary behaviour in boys or girls

PROCESS

PRODUCT or PROCESS measure of FMS competency.

ANCOVA = analysis of covariance; APARQ = Adolescent Physical Activity Questionnaire; BMI = body mass index; CRF = cardio-respiratory fitness; FMS = fundamental movement skills; KTK = Ko¨rper Koordinations Test fu¨r Kinder; MVPA = moderate to vigorous physical activity; NR = not reported; PA = physical activity; PACER = Progressive Aerobic Cardiovascular Endurance Run; PAR = physical activity recall questionnaire; PROCESS = process assessment of FMS concerned with technique; PRODUCT = product assessment of FMS concerned with outcome; PSPP = Physical Self-Perception Profile; SCPEAP = South Carolina Physical Education Assessment; SES = socio-economic status; SPPC = SelfPerception Profile for Children; TV = television; VPA = vigorous physical activity.

Lubans et al.

Sports Med 2010; 40 (12)

a


Benefits assessed

Analyses

1028


Table II. Contd

Did the study describe the participant eligibility criteria?

Were the participants randomly selected?a

Did the study report the sources and details of FMS assessment and did the instruments have acceptable reliability for the specific age group?

Did the study report the sources and details of assessment of potential benefits and did all of the methods have acceptable reliability for the specific age group?

Did the study report a power calculation and was the study adequately powered to detect hypothesized relationships?

Did the study report the numbers of individuals who completed each of the different measures and did participants complete at least 80% of FMS and benefit measures?

Quality score total/6

Martinek et al.[20] Rudisill et al.[21] Marshall and Bouffard[22] Reeves et al.[23] Okely et al.[24] Okely et al.[25] McKenzie et al.[26] Okely et al.[27] Graf et al.[28] Southall et al.[29] Fisher et al.[30] HamstraWright et al.[31] Castelli et al.[32] Barnett et al.[33] Barnett et al.[34] Erwin and Castelli[11]

1

0

1

1

0

0

3

1

0

0

1

0

1

3

1

0

1

1

0

1

4

1

0

1

1

0

1

4

1

1

1

1

0

1

5

1

1

1

0

0

0

3

1

0

1

0

0

1

3

1

1

1

1

0

1

5

1

1

1

0

0

0

3

1

1

1

1

0

1

5

1

1

1

1

0

1

5

0

0

1

0

0

0

1

1

0

1

1

0

0

3

1

1

1

1

0

1

5

1

1

1

1

0

1

5

1

0

1

0

0

1

3

Continued next page

1029

Sports Med 2010; 40 (12)

Study



Table III. Fundamental movement skills (FMS) study quality checklist with quality scores assigned

Lubans et al.


For intervention studies the criterion was as follows: were participants randomly allocated and was the process of randomization clearly described and adequately carried out (envelope or algorithm)? a

4 0 1 1 Cliff et al.[39]

1

1

0

4 0 0 1 D’Hondt et al.[38]

1

1

1

4 0 1 1 Barnett et al.[37]

1

1

0

5 0 1 1 Williams et al.[36]

1

1

1

4 1 0 1 0 1 Hume et al.[35]

1

Did the study report a power calculation and was the study adequately powered to detect hypothesized relationships? Did the study describe the participant eligibility criteria? Study

Table III. Contd

Were the participants randomly selected?a

Did the study report the sources and details of FMS assessment and did the instruments have acceptable reliability for the specific age group?

Did the study report the sources and details of assessment of potential benefits and did all of the methods have acceptable reliability for the specific age group?

Did the study report the numbers of individuals who completed each of the different measures and did participants complete at least 80% of FMS and benefit measures?

Quality score total/6

1030

relationship between self-concept and FMS was nonsignificant at baseline and post-test.[20] 2.4 Physiological Benefits

Weight status was the most commonly assessed physiological benefit of FMS competency and was included in nine studies. Body composition was generally estimated using body mass index (BMI) z-score; however, skinfolds were used in one study.[26] Six of the nine studies found an inverse association between FMS competency and BMI z-score[11,26-29,39,41] and three studies found no association between FMS competency and weight status.[32,35,36] Four studies examined the relationship between FMS competency and CRF. All four found a positive relationship between skill ability and fitness level.[22-24,33] Three of these studies used a process-oriented motor skill assessment[22,24,33] and one used a product assessment.[23] One study found positive associations between FMS competency, muscular fitness and flexibility.[32] Another study found a positive relationship between FMS competency and a composite physical fitness score (which included CRF, strength, endurance, flexibility and BMI).[11] 2.5 Behavioural Benefits

Thirteen studies examined the relationship between FMS competency and participation in physical activity. Eight studies used self-report measures of physical activity, four studies used objective measures of physical activity (i.e. accelerometers) and one study used both self-report and pedometers. FMS competency was found to be associated with at least one component of physical activity (e.g. non-organized activity, organized activity, pedometer step counts) in 11 of the cross-sectional studies[11,25,28,30-32,34-36,39,41] and one of the longitudinal studies.[37] Longitudinally, McKenzie et al.[26] found that FMS competency at ages 4–6 years did not predict physical activity at age 12 years. Both studies that examined the association between sedentary behaviour and FMS competency in children[28,39] did not find a statistically significant relationship. Sports Med 2010; 40 (12)


1031

Table IV. Summary of studies examining the relationship between potential benefits and fundamental movement skill (FMS) competency in youth Benefits

Associated with FMS references

association (-/+)b

21, 29, 34d

+

26-29e, 41

-

Not associated with FMS

Summary codinga

references

n/N for benefit (%)c

association (-/+)b

20

1/1 (100)

?

3/3 (100)

?

5/8 (63)

-

Psychological benefits Global self-concept Perceived physical competence Physiological benefits Weight status (BMI z-score, BMI, skinfolds)

32, 35, 36

CRF

22-24, 33f

+

4/4 (100)

+

Muscular fitness

32

+

1/1 (100)

?

Flexibility

32

+

1/1 (100)

?

Physical fitnessg

11

+

1/1 (100)

?

11, 25, 28, 30-32, 35-37, 39e, 41, 34h

+

26i

11/13 (80)

++

28, 39

2/2 (100)

?

Behavioural benefits Physical activity Sedentary behaviour a

Summary code provides an overall summary of the findings for each benefit.

b

Association shows the direction of the individual and summary association. A positive or negative association was noted if at least one component of FMS competency was associated with the hypothesized benefit.

c

n = number of studies that report support for relationship, N = number of studies that examined and reported possible associations between FMS competency and potential benefit.

d

Childhood FMS competency associated with adolescent perceived competence.

e

Positive association for boys and negative association for girls.

f

Childhood FMS competency associated with CRF in adolescence.

g

Composite physical fitness score including CRF, flexibility, strength, muscular fitness and BMI.

h

Childhood FMS competency associated with physical activity in adolescence.

i

FMS competency at ages 4–6 y did not predict physical activity at age 12 y.

BMI = body mass index; CRF = cardio-respiratory fitness; + indicates positive association; ++ indicates strong evidence for a positive association; - indicates negative association; ? indicates inconsistent or uncertain.

3. Discussion 3.1 Overview of Findings

The aim of this systematic review was to identify the health benefits associated with FMS competency in children and adolescents. We found 21 articles that assessed eight potential benefits (i.e. self-concept, perceived physical competence, CRF, muscular fitness, weight status, flexibility, physical activity and sedentary behaviour). We found strong evidence from cross-sectional studies for a positive association between FMS competency and physical activity in children and adolescents. There was also a positive association between FMS competency and CRF, and an inverse association between ª 2010 Adis Data Information BV. All rights reserved.

FMS competency and weight status. Due to an inadequate number of studies, the relationship between FMS competency and global self-concept, perceived physical competence, muscular fitness, flexibility and sedentary behaviour were classified as uncertain. It has been suggested that proficiency in a range of FMS provides the foundation for an active lifestyle.[1,3] The results from this review confirm the cross-sectional relationship between FMS competency and physical activity in children and adolescents. A number of large-scale cross-sectional studies,[25,30] some of which used objective measures of physical activity,[30,36] found positive associations between FMS competency and participation in physical activity. One longitudinal study found an association Sports Med 2010; 40 (12)

Lubans et al.

1032

between childhood object control skill ability and adolescent physical activity.[34,37] The other longitudinal study in this review found no association between FMS proficiency and physical activity.[26] This study examined early childhood (ages 4–6 years), three motor skills (lateral jumping, catching a ball, and balancing on one foot) and early adolescent (12 years) physical activity participation (measured via the SevenDay Physical Activity Recall questionnaire).[26] However, the study was limited by the use of a physical activity self-report measure and the assessment of only three FMS. Furthermore, two of these skills included what the authors termed ‘a restricted range of measurement’; 0–2 for balancing and 0–6 for catching.[26] This notion that a more comprehensive skill battery might be needed to accurately test whether skill is associated with physical activity is substantiated by the positive associations found in this review; all the other studies that found positive associations between motor skill and physical activity assessed more than three motor skills. The other factor that may have precluded the longitudinal study by McKenzie et al.[26] finding no association, was that skills were measured before the children had been provided with an opportunity to participate in school physical education (PE) and in out-of-school PE and sport programmes. It has been proposed that the relationship between skill ability and physical activity may strengthen over time.[42] This theory may also be supported in this review, as the one cross-sectional study in which the relationship between physical activity and motor skill ability was most uncertain (both positive and negative associations) was in preschool children.[39] However, this study may simply be limited by a small sample size, as the other two studies in this age group found positive associations.[11,43] We also found a positive association between FMS competency and CRF, and an inverse association between FMS competency and weight status. It has also been suggested that FMS competency might influence fitness levels, as activities that involve FMS also demand high levels of muscular and cardiorespiratory fitness.[42] More skillful children may increase their time in ª 2010 Adis Data Information BV. All rights reserved.

physical activity and persist with activities that require high levels of physical fitness,[42] providing the opportunity for fitness adaptations through progressive overload. Increased time in higher intensity physical activity will contribute to higher levels of CRF and improvements in body composition.[44] 3.2 Strengths and Limitations

This is the first systematic review of studies examining the relationship between FMS competency and potential health benefits in children and adolescents. The QUOROM statement was consulted and provided the structure for this review, which included an assessment of study quality using criteria adapted from the CONSORT and STROBE statements. However, there are a number of issues that should be noted. First, we did not include studies that combined gross motor skills and fine motor skills in the same composite score. For example, Wrotniak and colleagues[45] examined the relationship between motor competency and physical activity using the Bruininks-Oseretsky Test of Motor Proficiency (BOTMP) and found a positive association. While the BOTMP is an established measure of general motor ability, the current review was limited to FMS competency and therefore the inclusion of fine motor skills was beyond the scope of this review. It should also be noted that we excluded studies that did not provide a composite FMS score. A number of studies examined the relationship between individual FMS tests and potential benefits but did not provide a summary score.[46-48] Finally, due to the relatively small number of studies and the inclusion of longitudinal studies, the results for children and adolescents have been combined. As a result, this review could not assess whether the importance of FMS competency varies between childhood and adolescence,[42] a hypothesis that requires further investigation. 4. Conclusions Our review included only two longitudinal and two experimental studies. More longitudinal Sports Med 2010; 40 (12)


studies exploring the relationship between changes in FMS competency and potential benefits over time are needed to investigate the causal nature of such relationships. It has been hypothesized that children with high motor skill proficiency will have higher levels of fitness and perceived sports competence, which in turn predict greater participation in physical activity, and vice versa.[42] This proposed reciprocal relationship could also be investigated in future studies. In the current review we did not include intervention studies that did not directly examine the relationship between FMS competency and potential benefits. For example, two previous high quality obesity prevention trials[49,50] evaluated the impact of treatment on changes in FMS competency and BMI z-score in children, but did not report the relationship between such changes. Future physical activity and obesity prevention studies should conduct mediation analyses to identify if FMS competency mediates the impact of interventions on primary outcomes (e.g. BMI z-score, fitness). Few studies have conducted mediation analyses in physical activity interventions among youth[51] and the importance of FMS competency to future physical activity and other outcomes will be reinforced through this type of analysis. The one study reviewed that did conduct a mediation analysis,[34] found that perceived sports competence acted as a mediator between skill ability and physical activity. Due to the limited number of studies it was not feasible to examine how the association between motor skill ability and potential benefits might differ according to gender. Gender differences in motor proficiency have been found, with males generally more proficient than females in object control skill performance.[35,43,52,53] In locomotor skill performance, some studies report no gender differences,[35,53,54] while others report males[55] or females[53] as more proficient. The potential impact of these differences is important to investigate. Our findings suggest that FMS development should be included in school- and communitybased interventions. Teaching children to become competent and confident performers of FMS may lead to a greater willingness to participate in physical activities that may also provide opportuª 2010 Adis Data Information BV. All rights reserved.

1033

nities to improve fitness levels and reduce the risk of unhealthy weight gain. It is important that such skills are taught during preschool and elementary school years as children are at an optimal age in terms of motor skill learning[1] and motor skill proficiency tracks through childhood.[56] In addition, improving the FMS competency of girls should be a priority as many girls lack basic skill proficiency.[10,11] Existing school physical education programmes have been criticized for not providing a learning environment to develop FMS,[57] so training and resources should be prioritized to ensure children receive quality instruction in FMS. FMS have been hypothesized as important to children and adolescents’ physical, social and psychological development,[1,2] and may be the foundation of an active lifestyle. This review has provided evidence supporting the positive association between FMS competency in children and adolescents and physical activity. Furthermore, the positive association between FMS competency and CRF and the inverse relationship between FMS proficiency and weight status suggest that developing competency in movement skills may have important health implications for young people. Acknowledgements No external funding was used for this project. The authors would like to thank Emily Hoffman and Kelly Magrann for their assistance in the retrieval of journal articles. The authors have no conflicts of interest that are directly relevant to the content of this review.

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49.

50.

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57.

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Correspondence: Dr David Lubans, University of Newcastle, School of Education, Callaghan Campus, University Drive, NSW 2308, Australia. E-mail: [email protected]

Sports Med 2010; 40 (12)

Sports Med 2010; 40 (12): 1037-1053 0112-1642/10/0012-1037/$49.95/0

REVIEW ARTICLE


Testosterone Physiology in Resistance Exercise and Training The Up-Stream Regulatory Elements Jakob L. Vingren,1,2 William J. Kraemer,2,3 Nicholas A. Ratamess,4 Jeffrey M. Anderson,2 Jeff S. Volek2 and Carl M. Maresh2,3 1 Applied Physiology Laboratories, Department of Kinesiology, Health Promotion and Recreation, University of North Texas, Denton, Texas, USA 2 Human Performance Laboratory, Department of Kinesiology, University of Connecticut, Storrs, Connecticut, USA 3 Department of Physiology and Neurobiology, University of Connecticut, Storrs, Connecticut, USA 4 Department of Health and Exercise Science, The College of New Jersey, Ewing, New Jersey, USA

Contents Abstract. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Testosterone Production and Release . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.1 Testosterone Production . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2 Hypothalamic-Pituitary-Gonadal Axis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.3 Stimulation and Inhibition of the Hypothalamic-Pituitary-Gonadal Axis . . . . . . . . . . . . . . . . . . . . 2. The Biological Effects of Testosterone . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1 Transport of Testosterone in the Circulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2 Actions on the Muscle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.1 Effect on Androgen Receptor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.2 Importance for Normal Muscle Development and Maintenance . . . . . . . . . . . . . . . . . . . 3. Testosterone Response to Resistance Exercise and Training. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1 Men . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1.1 Intensity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1.2 Number of Sets . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1.3 Volume . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1.4 Choice of Exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1.5 Order of Exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1.6 Rest Period Duration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2 Women. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3 Effect of Age . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4 Effect on Androgen Receptor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Abstract

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Testosterone is one of the most potent naturally secreted androgenicanabolic hormones, and its biological effects include promotion of muscle growth. In muscle, testosterone stimulates protein synthesis (anabolic effect) and inhibits protein degradation (anti-catabolic effect); combined, these effects account for the promotion of muscle hypertrophy by testosterone. These

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physiological signals from testosterone are modulated through the interaction of testosterone with the intracellular androgen receptor (AR). Testosterone is important for the desired adaptations to resistance exercise and training; in fact, testosterone is considered the major promoter of muscle growth and subsequent increase in muscle strength in response to resistance training in men. The acute endocrine response to a bout of heavy resistance exercise generally includes increased secretion of various catabolic (breakdown-related) and anabolic (growth-related) hormones including testosterone. The response of testosterone and AR to resistance exercise is largely determined by upper regulatory elements including the acute exercise programme variable domains, sex and age. In general, testosterone concentration is elevated directly following heavy resistance exercise in men. Findings on the testosterone response in women are equivocal with both increases and no changes observed in response to a bout of heavy resistance exercise. Age also significantly affects circulating testosterone concentrations. Until puberty, children do not experience an acute increase in testosterone from a bout of resistance exercise; after puberty some acute increases in testosterone from resistance exercise can be found in boys but not in girls. Aging beyond 35–40 years is associated with a 1–3% decline per year in circulating testosterone concentration in men; this decline eventually results in the condition known as andropause. Similarly, aging results in a reduced acute testosterone response to resistance exercise in men. In women, circulating testosterone concentration also gradually declines until menopause, after which a drastic reduction is found. In summary, testosterone is an important modulator of muscle mass in both men and women and acute increases in testosterone can be induced by resistance exercise. In general, the variables within the acute programme variable domains must be selected such that the resistance exercise session contains high volume and metabolic demand in order to induce an acute testosterone response.

This review examines androgen endocrine physiology (i.e. testosterone and the androgen receptor [AR]) and its relationship to resistance exercise and training. Knowledge of the general testosterone physiology is important because it is the foundation for understanding the physiological implications of changes in testosterone and AR concentrations. The first section provides an overview of testosterone production and the signals for testosterone production and release. The next section examines the biological effects of testosterone including transport, signalling and physiological functions with special attention given to the importance of testosterone for normal muscle development and maintenance. Finally, the acute and chronic testosterone and AR responses to resistance exercise and training is discussed with the focus on upper regulatory elements: ª 2010 Adis Data Information BV. All rights reserved.

acute exercise programme variable domains, sex and age. 1. Testosterone Production and Release 1.1 Testosterone Production

Testosterone (17b-hydroxy-4-androstene-3-one) is a 0.288 kD C19 steroid hormone produced from cholesterol via a series of conversions catalysed by specific enzymes; this process takes approximately 20–30 minutes from initiation to final product.[1] Several of the intermediates in this process are hormones with their own physiological actions and include progesterone, dihydroepiandrosterone (DHEA) and androstenedione; the former is involved in the female reproductive cycle[2] and the latter two have weak androgenic-anabolic effects.[3] Sports Med 2010; 40 (12)

Testosterone and Resistance Exercise

The primary production site of testosterone is the Leydig cells. These cells are only found in the testes, which largely explain the approximately 10-fold higher circulating testosterone concentrations in men compared with women. Testosterone is also produced in smaller quantities in the ovaries and the zona reticularis of the adrenal cortex.[4] This testosterone formation is mainly spillover from the production of other hormones such as cortisol and aldosterone (in the adrenal glands) that share some precursors with testosterone, and estradiol (in the ovaries) for which testosterone itself is a precursor.[5] These shared precursors help explain how the adrenal gland and the ovaries can produce testosterone despite the absence of Leydig cells in these tissues. This spillover, along with peripheral conversion of androgens, is the primary source of testosterone in females and adolescent boys. The absence of functioning cells dedicated to testosterone production and release prevents large acute increases in circulating testosterone in females and adolescent boys in response to exercise. Although peripheral production (e.g. in muscle tissue) of testosterone occurs,[6] this production does not appear to be affected by resistance exercise in humans.[7] 1.2 Hypothalamic-Pituitary-Gonadal Axis

The signal for gonadal testosterone production and release originates in the hypothalamus. The hypothalamus is innervated by the CNS and thus provides a direct link between the nervous and the endocrine systems.[8] Specialized neurons in the hypothalamus produce and secrete gonadotrophin releasing hormone (GnRH).[8] GnRH travels directly to the anterior pituitary gland via the hypothalamic-hypophyseal portal vein. This allows for a quick delivery of the hormonal signal from the hypothalamus to the pituitary target cells. In the anterior pituitary, GnRH stimulates the production and release of luteinizing hormone (LH) and follicle-stimulating hormone (FSH) from the gonadotrophs.[8] LH and FSH then enter the circulation and are transported to the gonads. In the gonads, LH stimulates testosterone production in the Leydig cells of men and the theca cells of women. LH binds to a G-protein-coupled memª 2010 Adis Data Information BV. All rights reserved.

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brane receptor; the signal induced by LH activates cyclic adenosine monophosphate-dependent protein kinases (protein kinase A),[9,10] which stimulates the rate-limiting step in testosterone synthesis.[9] Testosterone is a steroid hormone and thus cannot be stored in the cells that produce it; instead, testosterone is released from the cells following production. In women, testosterone is further processed to estradiol in the granulosa cells adjacent to the theca cells. FSH does not appear to have direct effects on testosterone production in men but is important in stimulation of steroid binding protein production in the liver. In women, FSH stimulates the production of pregnenolone in the granulosa cells and steroid binding protein production in the liver. The signal cascade from FSH is similar to that induced by LH in the theca and Leydig cells; the produced pregnenolone can leave the granulosa cells for the theca cells where it can be further processed to testosterone. Finally, FSH stimulates the synthesis of p450 aromatase, which is responsible for the conversion of testosterone to estradiol in the granulosa cell. This system of signalling events from the hypothalamus to the gonads leading to testosterone (and estradiol) production and secretion is termed the ‘hypothalamic-pituitarygonadal axis’. 1.3 Stimulation and Inhibition of the Hypothalamic-Pituitary-Gonadal Axis

The initiation of the hypothalamic-pituitarygonadal axis, which ultimately leads to increased testosterone release, is caused either by direct nervous stimulation of the hypothalamus by the CNS or by reduced feedback inhibition on the hypothalamus by testosterone. Testosterone induces negative feedback on (i) the hypothalamus to reduce GnRH release; and (ii) the gonadotrophs in the anterior pituitary to reduce the release of LH and FSH in response to GnRH. The use of GnRH analogues have shown that in the absence of a GnRH signal the gonadotrophs in the anterior pituitary do not independently release LH despite very low circulating testosterone concentrations.[11,12] Since the GnRH analogue prevented an exercise-induced increase in Sports Med 2010; 40 (12)

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circulating LH and testosterone, it appears that the signal for increased testosterone release with resistance exercise is controlled at the level of the hypothalamus. 2. The Biological Effects of Testosterone Testosterone is one of the most potent naturally secreted androgenic-anabolic hormones,[13] and its biological effects include promotion of secondary male-sex characteristics, such as beard and body hair growth, nitrogen retention and muscle growth.[14] In muscle, testosterone stimulates protein synthesis (anabolic effect)[15] and inhibits protein degradation (anti-catabolic effect);[16] combined, these effects account for the promotion of muscle hypertrophy by testosterone. The physiological effects of testosterone are induced by its binding to the intracellular AR, which then translocates to the nucleus where the AR-testosterone complex induces transcription of specific genes.[17] Recently, membrane receptors for testosterone have been proposed to explain the rapid effects of testosterone on the cell.[18] In addition to the anabolic effects, testosterone has anti-catabolic effects that are believed to include an inhibition of cortisol signalling by blocking the glucocorticoid receptor.[19,20] The administration of testosterone to patients receiving long-term glucocorticoid therapy attenuates or even reverses some of the adverse effects from glucocorticoid treatment such as reductions in bone mineral density and muscle mass.[21] Similarly, excess glucocorticoids can interfere with testosterone signalling[22] and suppress testosterone production in the Leydig cells.[23] It is mainly the anabolic effects of testosterone that are of interest to those engaged in resistance exercise; however, the anti-catabolic effects might also be a very important aspect because they help protect muscle protein and aid in recovery. These anabolic effects are also primarily what have led athletes from many different sports to abuse various pharmacological forms of testosterone. Although generally not considered among the primary anabolic hormones in women, testosterone has a potent effect on female muscle tissue. ª 2010 Adis Data Information BV. All rights reserved.

2.1 Transport of Testosterone in the Circulation

Testosterone is hydrophobic and consequently does not readily dissolve in the blood; instead, almost all testosterone in the circulation is bound to binding proteins that are hydrophilic.[24] The primary binding protein for testosterone is sex hormone-binding globulin (SHBG), which binds approximately 44–60% of total serum testosterone.[25,26] The remaining testosterone is either loosely bound to albumin and other binding proteins or free (i.e. not bound to any binding proteins); however, only about 0.2–2% of total testosterone is in the free form.[26,27] Free testosterone is the most biologically active fraction of testosterone; thus, the biological activity of testosterone is regulated by its interaction with the different binding proteins.[28] The physiological effects of the binding proteins vary. SHBG reduces the movement of testosterone from the blood into other biocompartments; whereas, albumin does not appear to interfere with this movement.[29,30] Furthermore, in contrast to free testosterone, binding proteins cannot move across the cell membrane; as a result, association with the binding protein reduces the likelihood for testosterone interaction with the intra-cellular nuclear AR. Binding to SHBG effectively prevents the biological actions of testosterone; whereas, binding to albumin appears to still allow for a large bioavailability of testosterone.[31] In addition to facilitating the transport of the hydrophobic testosterone in the watery environment of the blood, binding proteins reduce the clearance of testosterone from the blood.[29] Testosterone cannot be stored in the cells that produce it, which is in contrast to most peptide hormones, so the association with binding proteins can act as storage in the circulation. The bound testosterone can then be released to become free testosterone in order to enter the cell. 2.2 Actions on the Muscle

As mentioned in section 2, testosterone is a potent anabolic hormone that stimulates muscle protein synthesis[13,15] and intramuscular amino acid uptake,[32] resulting in improved net protein balance.[33] Sports Med 2010; 40 (12)


2.2.1 Effect on Androgen Receptor

Testosterone increases the AR in muscle cells and associated myonuclei and satellite cells.[33-36] The precise mechanism for this upregulation is not fully understood, but it is known that androgens increase the half-life of AR in cell culture suggesting a potential mechanism.[37,38] Several in vivo studies have shown that AR content is upregulated acutely by administration of pharmacological variants of testosterone in rats[35,36] and humans.[39] AR content continues to increase for several days after which the increased concentration of AR is maintained. It appears that after long-term continuous high circulating concentrations of testosterone from exogenous use, e.g. several months, the AR content returns to baseline in men,[33] whereas, cycling on and off exogenous testosterone, as many athletes who use anabolic steroids do, leads to a sustained long-term AR content increase in men.[34] 2.2.2 Importance for Normal Muscle Development and Maintenance

Testosterone is important for the development and maintenance of muscle mass in males. In boys, puberty is associated with increased circulating testosterone concentrations and accrual of muscle mass.[40] In contrast, sarcopenia (loss of muscle mass) has been associated with the decline in testosterone concentrations found with aging in men.[41-43] In older men, the effects of sarcopenia on muscle mass and function can be reversed by testosterone administration that returns circulating testosterone concentrations to within or near the normal physiological range.[33] Hypogonadism resulting from surgery (orchiectomy) or pharmacological testosterone deprivation therapy (the latter is commonly used with prostate cancer) also leads to reductions in muscle mass and function in adult males.[44-46] The importance of normal circulating concentrations of testosterone on muscle mass in women is less clear as a reduction in testosterone generally does not occur independently of reductions in other hormones such as estrogens (e.g. with menopause).[47] Despite these limitations, testosterone appears to be important for the maintenance of muscle mass in women. In women with muscle mass reductions resulting from hypopituitarism, testosterone adª 2010 Adis Data Information BV. All rights reserved.

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ministration that returns free testosterone to a normal concentration increased fat-free mass and muscle cross-sectional area.[48] Similarly, combined testosterone and estrogen administration to oophorectomized women resulted in increased lean mass; whereas, estrogen administration alone had no effect on lean mass.[49] In addition to these controlled clinical trials, there is substantial, yet anecdotal, evidence that exogenous supraphysiological doses of testosterone, as those used by some women body builders, have a very potent effect on muscle mass accretion in women. In a series of experiments, Mauras and colleagues[15,50,51] examined the effects of testosterone on muscle protein synthesis and accretion in young men and prepubertal boys. Combined, these studies show that testosterone is vital for the development and maintenance of muscle mass via testosterone’s stimulation of whole body protein synthesis and inhibition of proteolysis resulting in a net anabolic effect. In healthy prepubertal boys, acute testosterone administration increased protein synthesis, as measured by nonoxidative leucine disappearance as well as protein proteolysis, with an overall improvement in leucine and presumably protein balance.[50] In growth hormone (GH)-deficient prepubetal boys, testosterone reduced protein oxidation, as measured by leucine oxidation, but did not alter measures of protein synthesis; however, when 22-kD GH and testosterone were administered together, marked increases in protein synthesis were observed.[51] The authors concluded that a minimum concentration of GH was needed for the actions of testosterone; consequently, they suggested that GH had a permissive or synergistic effect on testosterone’s promotion of protein synthesis. In accordance with the findings on testosterone administration, 10 weeks of administration of a GnRH analogue to young men (resulting in very low circulating testosterone concentrations) caused marked decreases in the rates of whole-body protein turnover and protein synthesis.[15] These reductions were manifested in decreased fat-free mass and muscle strength supporting the crucial role of testosterone in the maintenance of muscle mass and function in men. Testosterone also has a stimulating effect on the production of other anabolic hormones. In Sports Med 2010; 40 (12)

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healthy, short-stature, prepubertal boys (Tanner stage 1), testosterone administration led to increases in circulating immunoreactive GH concentrations.[50] In GH-deficient prepubetal boys, testosterone administration increased circulating insulin-like growth factor (IGF)-I, although testosterone and 22-kD GH administered together caused an even greater increase in IGF-I.[51] Based on these findings, testosterone and 22-kD GH appear to have a synergistic effect on IGF-I release, although the effect of 22-kD GH alone was not examined. In mildly hypogonadal older men, testosterone treatment increased muscle IGF-I protein expression,[33] and in young men pharmacological testosterone deprivation reduced IGF-I messenger RNA (mRNA) expression (the nuclearderived signal for IGF-I protein production at the ribosome) in muscle despite no changes in circulating immunoreactive GH and IGF-I concentrations.[15] Furthermore, cell cultures incubated with testosterone upregulate IGF-I mRNA expression in a dose-dependent manner.[52] Combined, these findings suggest that testosterone is required for muscle IGF-I production, and that this is a direct effect of testosterone independent of circulating immunoreactive growth hormone and IGF-I concentrations. However, a synergistic effect of testosterone and 22-kD GH on muscle IGF-I appears to exist. The recent identification of androgen response elements in the IGF-I upstream promoter region[52] provides further support for the importance of testosterone in muscle IGF-I production. Since IGF-I is also a potent anabolic hormone that directly increases anabolic gene transcription via the AKT/mammalian target of rapamycin (mTOR) pathway,[53] this influence of testosterone on muscle IGF-I production provides an additional mechanism by which testosterone can increase muscle protein synthesis and accretion. 3. Testosterone Response to Resistance Exercise and Training The acute endocrine response to a bout of resistance exercise includes increased secretion of various catabolic (breakdown-related) and anabolic (growth-related) hormones. One of the primary anabolic hormones released in response to ª 2010 Adis Data Information BV. All rights reserved.

resistance exercise is testosterone; in fact, testosterone is believed to be the major promoter of muscle growth and subsequent increase in muscle strength in response to resistance training in men. In general, total testosterone and free testosterone are elevated directly following heavy resistance exercise in men, whereas, findings on the testosterone response to a bout of heavy resistance exercise in women are equivocal with both increases[54,55] and no changes observed.[56-58] The endocrine response for the days following resistance exercise is unclear. Ha¨kkinen and Pakarinen[59] found a decrease of both total testosterone and free testosterone in men for the first 2 days following heavy squats (10 sets of 10 repetitions at 70% of 1-repetition maximum [1RM] or 20 sets of 1 repetition with 100% of 1RM), whereas, Koziris and colleagues[60] found no difference in total testosterone for the same timepoints following whole-body circuit resistance exercise using universal gym machines (3 circuits of upper- and lower-body exercises with a 5RM load). This difference in findings could be due to the different exercise protocols used in the two studies and would suggest that the testosterone response for the days following resistance exercise is also specific to the resistance exercise protocol used. The protocol used by Ha¨kkinen and Pakarinen,[59] especially the 10 sets of 10 repetitions, involved substantially more volume than the protocol used by Koziris et al.[60] Accordingly, the extent to which testosterone is acutely affected by resistance exercise largely depends on the selection among the acute programme variable domains for the exercise session. Several of the acute programme variable domains interact with each other, so to investigate the effect of one variable domain on the testosterone response to resistance exercise other variable domains must often be manipulated. To reduce redundancy, studies in which this occurs will mainly be examined once and not repeated in sections for the other variable domains. 3.1 Men

In general, circulating total testosterone and free testosterone increase immediately after a bout of heavy resistance exercise in men and return to, or below, baseline within 30 minutes;[12,27,56,61-67] Sports Med 2010; 40 (12)


however, the appearance and magnitude of these testosterone increases are greatly influenced by the selection among the ‘acute programme variable domains’ (intensity, number of sets, choice of exercise, order of exercise and rest period duration) for the exercise session. 3.1.1 Intensity

Intensity refers to the load or resistance used for a given exercise. There appears to be a relative intensity and volume threshold (total work performed; see section 3.1.3 below) that must be reached in order to induce a testosterone response. Comparing protocols with the same volume but different loads (4 sets of 6 repetitions at 52.5% of 1RM vs 3 sets of 6 repetitions at 40% of 1RM during concentric actions and 100% of 1RM during eccentric actions) for the bench press and squat exercises, Yarrow et al.[68] found that neither protocol produced an increase in testosterone. The intensity used in that study, with the exception of the eccentric action, was very low and this likely explains the lack of a testosterone response. Kraemer et al.[61] examined the effect of altering the intensity while keeping total work constant and found that when intensity was reduced, the testosterone response was attenuated. When the number of repetitions is kept constant, higher intensity and thus higher volume induces a greater testosterone response. Raastad et al.[69] showed that 3 sets of 6 repetitions for three lower-body exercises at 100% of 6RM but not at 70–76% of 6RM induced a significant increase in testosterone. Similarly, 5 sets of 10 repetitions with 10RM has been found to induce a significant testosterone increase; whereas, 5 sets of 10 repetitions with either 70% or 40% of 10RM did not affect testosterone concentrations.[56] The findings on the effect of high relative intensity alone on the testosterone response are equivocal with both increases[70] and no changes found post-exercise.[59,64] Ten sets of 1RM in resistance trained men resulted in a significant acute increase in circulating testosterone;[70] however, 20 sets of 1RM in elite strength athletes did not induce an increase in testosterone.[59] Although speculative, the difference in findings could be attributed to the difference in rest periods (2 and 3 minutes, for the 10- and 20-set protocols, reª 2010 Adis Data Information BV. All rights reserved.

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spectively) or the training level of the participants. In accordance with the findings by Ha¨kkinen and Pakarinen[59] high relative intensity and lowmoderate total work protocols (2, 4 or 6 sets of 5 repetitions with 80–88% of 1RM) did not induce a testosterone response.[64] In general, it appears that high relative intensity alone is not sufficient to induce a testosterone response if the total volume of the protocol is low; however, a relative intensity minimum threshold must be met, even with a high volume, to induce a testosterone response. 3.1.2 Number of Sets

This variable refers to the number of sets performed for each exercise in a resistance exercise session. When total volume is held constant, the number of sets does not appear to influence the acute testosterone response to resistance exercise.[61,71] Goto et al.[71] examined the effect of adding a 30-second rest period in the middle of each 10-repetition set. This added rest period essentially produced double the number of sets with half the repetitions but similar volume. Despite a lower metabolic demand (i.e. attenuated lactate response) the addition of the rest did not result in differences in the testosterone response. When changing the load while keeping volume constant, (and thus changing the number of sets) Kraemer et al.[61] found that no alterations in the resistance exercise-induced testosterone concentrations occurred. Similarly, 16 weeks of resistance training with all sets to either failure or not to failure, but the same volume and intensity (thus adding sets), did not alter resting testosterone; however, an increase in resting testosterone was found after 11 weeks.[72] It is difficult to ascertain the reason for this transient difference on the resting testosterone concentration, but it does suggest that subtle differences in adaptations can occur when sets are manipulated while keeping load and volume constant. It is possible that the high stress from performing each set to failure, which prevented a training-induced reduction in resting cortisol, led to a state of overreaching or mild overtraining and thus prevented a transient anabolic adaptation manifested in elevated testosterone concentrations. This possibility is supported by the finding that IGF-I concentrations were reduced with the Sports Med 2010; 40 (12)

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sets to failure condition, although performance did not appear to be affected in this group. 3.1.3 Volume

Volume refers to the total work performed and is often used in the context of resistance exercise to mean (set · number of repetitions · intensity). Using this definition, volume is a function of several different acute programme variable domains and is therefore not considered an independent acute programme variable domain. However, manipulating volume by changing several of its constituents can significantly affect the hormonal response; this potent effect of volume warrants its inclusion in this review. There appears to be a threshold of volume or metabolic demand that must be reached before increases in testosterone are observed. Ratamess et al.[66] showed that 6 sets, but not 1 set, of 10 repetition squats significantly increased total testosterone post-exercise. The metabolic demand of the 1-set protocol was relatively low, manifested by an only modest increase in lactate; whereas the 6 sets produced a large increase in lactate, suggesting a high metabolic demand. The requirement for a high metabolic demand and not just high intensity for an increase in testosterone post-exercise was shown by Ha¨kkinen and Pakarinen.[59] Twenty sets of 1RM resulted in no change in testosterone, whereas 10 sets of 10RM resulted in a large increase in free and total testosterone. The lactate response was modest (~4 mmol/L) with the high-intensity protocol but substantially larger (~15 mmol/L) with the high volume protocol supporting the hypothesis that a large metabolic demand is needed to induce a testosterone response. Furthermore, an examination of various combinations of sets and repetitions found that, in general, a higher volume created a greater testosterone response.[64] In that study,[64] the threshold for a testosterone response appeared to be based more on metabolic demand than on volume per se; however, the study did not attempt to establish this threshold. 3.1.4 Choice of Exercise

Choice of exercise refers to the specific exercise chosen (e.g. power clean), the equipment used ª 2010 Adis Data Information BV. All rights reserved.

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(e.g. machine or free weight), and how the exercises are performed (e.g. type of muscle action, velocity of movement). One of the major determinants for the occurrence of a testosterone increase with resistance exercise is the muscle mass used. Involvement of a small muscle mass, even when exercised vigorously, does not elevate testosterone above resting concentrations.[73] Exercise selection, therefore, significantly influences the testosterone response to a resistance exercise session. Bilateral knee extension alone[74] or the combination of unilateral knee extension and leg press[75] performed with a 5–10RM load does not induce a testosterone response. Similarly, unilateral biceps curls alone do not induce a testosterone response, but the addition of bilateral knee extensions and leg press to the biceps curl protocol results in a significant testosterone response.[76] When resistance exercise induces an increase in testosterone, the magnitude of that increase is also affected by muscle mass involvement; a jump squat protocol increases testosterone concentration more than a bench press protocol performed by the same participants (15% vs 7% for the jump squat and bench press, respectively).[77] Similarly, exercises such as the squat[27,66,78] and Olympic lifts,[79] that involve a large muscle mass, produce larger elevations in testosterone compared with smaller muscle mass exercises.[76,80,81] Larger muscle mass involvement allows for greater total volume, which helps to explain the importance of muscle mass involvement in inducing a testosterone response to resistance exercise. As described in section 3.1.3, the total volume of work has important implications for the appearance and magnitude of the testosterone response to resistance exercise. The effect of exercise modality (free-weight or machine exercises) on the testosterone response does not appear to have been investigated directly, but both modalities can produce substantial increases in testosterone when a high load and volume is used. Only a few studies have investigated the effect of modes of muscle contraction on the acute testosterone response to resistance exercise.[80,82,83] When the same relative intensity is used, there does not appear to be a difference in the testosterone response between concentric and eccentric Sports Med 2010; 40 (12)


exercises.[80] Durand et al.[82] found that concentric and eccentric exercise protocols using the same absolute intensity produced an increase in testosterone with no difference between modes of contraction. Despite the lack of a significant difference between modes of contraction, the concentric condition produced almost twice as large an increase in testosterone compared with the eccentric condition, suggesting that mode of contraction can affect the testosterone response to resistance exercise.[82] When the same relative load is used, free testosterone increases similarly following concentric and eccentric muscle action resistance exercise.[83] It seems likely that the potential difference in the testosterone response between modes of contraction using the same absolute load, as presented by Durand and colleagues,[82] might be because the maximal force capability is higher for eccentric muscle actions than for concentric muscle actions[84] and as a consequence, the relative intensity was lower during the eccentric exercises. In recent years, whole-body vibration (WBV) has resurfaced as an alternative mode of resistance training. The hormonal response to WBV has been examined by a few studies with both no effects[85-87] and elevations found for testosterone.[88] Ten sets of 1-minute isometric half squats during WBV did not affect salivary testosterone concentrations;[85] similarly, neither 25 minutes of standing WBV[87] nor 6 sets of 8 repetitions of unloaded squat (30-second per set) during WBV affected circulating testosterone concentrations.[86] Adding WBV to a protocol consisting of 6 sets of 8RM squats did not affect the postexercise increase in testosterone compared with the squat protocol alone; furthermore, this response was not altered by 9 weeks of training using WBV and squats.[86] In contrast to these findings, Bosco and colleagues[88] found that 10 sets of 1-minute isometric squats during WBV significantly increased circulating testosterone, although the increase was only modest (1.6 nmol/L, equal to ~7%). It appears that WBV has no or only a limited effect on testosterone. More research is needed to firmly establish the effects of WBV on the acute testosterone response to exercise. ª 2010 Adis Data Information BV. All rights reserved.

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3.1.5 Order of Exercise

The order of exercise refers to the sequence of exercises within an exercise session; this order affects the power output and the number of repetitions that can be completed for each exercise.[89] The order of exercise can also affect the timing of the hormonal response to resistance exercise. Large muscle mass exercises are needed to acutely increase circulating testosterone concentrations and as a result when large muscle mass exercises are performed in the beginning of an exercise session, the muscle used during subsequent exercises will be perfused with an elevated testosterone concentration. The importance of elevated anabolic hormones including testosterone was shown by the finding that when the biceps is trained after 4 sets of leg press, it hypertrophied significantly more compared with training of the biceps alone.[76] It remains to be determined if altering the order of exercises while keeping the load and repetitions constant, affects the post-exercise testosterone response. 3.1.6 Rest Period Duration

The duration of rest periods refers to the time (minutes or seconds) between each set and each exercise. Rest period duration can substantially affect the metabolic demand of a bout of resistance exercise as evident by the lactate response[61] and the average oxygen consumption[90] for the session. It is well established that increased metabolic demands augment the response of certain other hormones, such as immunoreactive GH,[61] yet this effect has not been shown for testosterone. Only a single study appears to have isolated the effect of rest period duration on the testosterone response to resistance exercise. That study observed that only in the context of moderate loads (10RM) with high volume (~60 000 J) did short rest (1 minute) result in a significantly larger testosterone response compared with longer rest (3 minutes).[61] Ahtiainen and colleagues[91] reported no effect of rest period duration (2 vs 5 minutes) on the testosterone response to resistance exercise; however, the protocols used for each rest period duration condition differed slightly in the load and sets used making direct comparisons difficult. It appears that with different combinations Sports Med 2010; 40 (12)

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of load and volume, rest period can affect the acute resistance exercise-induced testosterone response. Synergistic integration among resistance, rest and volume therefore likely exists, but the magnitude of each required for the different testosterone response patterns remains to be determined. 3.2 Women

The biological mechanisms for a potential exercise-induced increase in testosterone might be different in women compared with men. Women do not have Leydig cells and Kvorning et al.[12] have shown that the Leydig cells are likely involved in the acute resistance exercise-induced increase in testosterone in men. An increase in free or total testosterone for women has been found in some studies[54,55,62,92] but not all studies.[56,58,93] One might speculate that such equivocal findings are due to differences in the selections within each acute programme variable domain; however, this has not been substantiated. Only a few studies have directly examined the effect of specific acute programme variable domains on the testosterone response to resistance exercise in women; however, these studies have found no acute elevation in testosterone post-exercise. Linnamo et al.[56] demonstrated no changes in total testosterone following 5 sets of 10 repetitions each of sit-ups, bench press and leg press using three different loading conditions: maximal (10RM), submaximal (70% of 10RM) and explosive (40% of 10RM). In men, the same maximal load condition led to a significant increase in total testosterone.[56] Similarly, Kraemer et al.[58] showed that with heavy resistance exercise altering rest period duration or load while keeping total volume constant did not result in post-exercise testosterone concentrations above baseline in women. Although no acute changes following exercise were found, the simultaneous manipulation within several of the acute programme variable domains has been shown to affect resting total testosterone following long-term resistance training in women.[93] A low-volume, single-set circuit programme produced only a modest increase in resting testosterone after 12 weeks, but resting testosterone ª 2010 Adis Data Information BV. All rights reserved.

Vingren et al.

returned to baseline at 24 weeks of training. In contrast, a periodized high-volume, multiple-set programme produced a large increase in resting testosterone at 12 weeks and an even larger increase at 24 weeks of training. Thus, the training programme design significantly affected the magnitude and sustainability of the increase in resting testosterone concentration. It has been reported that in men a GnRH analogue (goserelin), which suppresses circulating LH and thus Leydig cell function resulting in castrate concentrations of testosterone, prevents an acute resistance exercise-induced increase in total and free testosterone.[12] Thus, it appears that the Leydig cells are responsible for acute increases in testosterone following resistance exercise, and this would explain the lack of consistent findings for the testosterone response to resistance exercise in women. The acute increase in testosterone, especially free testosterone, following resistance exercise reported in some studies could originate as a byproduct of cortisol production. Adrenocorticotropic hormone, which stimulates production and release of cortisol, also causes release of testosterone from the adrenal cortex.[94] Adrenocorticotropic hormone concentrations increase in response to heavy resistance exercise,[95] which could lead to a greater adrenal production and release of testosterone. Considering that free testosterone is a very small part of total testosterone (0.5–2%), a small increase in free testosterone might not be detectable in total testosterone concentration analysed using standard enzymatic procedures. None of the studies that showed an increase in testosterone included measurements of the adrenocorticotropic hormone response to resistance exercise, and only one study included measurements of cortisol; Copeland et al.[55] found that both testosterone and cortisol were elevated compared with control following resistance exercise. Alternatively, the resistance exercise-induced increases in testosterone could simply be due to a reduction in plasma volume, which could cause an increase in circulating testosterone concentration without a change in the amount of testosterone in the circulation. It is also possible that statistical limitations due to the relatively low number of subjects in some of these Sports Med 2010; 40 (12)


studies might negate findings of significant increases due to the potential variance involved in women’s response patterns. 3.3 Effect of Age

Age significantly affects circulating testosterone concentration. Children have low concentrations of testosterone until puberty when testosterone increases markedly in boys and to a minor extent in girls.[96] Aging beyond 35–40 years is associated with a 1–3% decline per year in circulating testosterone concentration (1.6% in total and 2–3% in bioavailable testosterone) in men.[97] This reduction can eventually lead to very low resting concentrations of circulating testosterone, a condition that has been termed andropause.[98] In women, circulating testosterone concentrations also gradually decline until menopause after which a 60% reduction is found within 2–5 years.[47] The testosterone response to resistance exercise is also greatly affected by age. Boys do not experience an acute increase in testosterone in response to resistance exercise; even after the onset of puberty when resting testosterone is increased in boys, they appear to experience no or only a minor resistance exercise-induced increase in testosterone.[63,99] Following the same resistance exercise session, testosterone increased in college-aged men but not in high school-aged young men.[100] Similarly, Pullinen et al.[63,99] showed that in contrast to resistance-trained men, there was no or only a minor increase in testosterone following resistance exercise in 14- and 15-year-old boys, respectively, who had been engaged in resistance training for at least 1 year. This lack of exerciseinduced increase in testosterone in boys existed even though there was no difference in resting testosterone concentrations between the men and boys.[63,99] Although speculative, the reason for this limited testosterone response to resistance exercise in teenage boys might be due to an inability of the testis to quickly increase testosterone release or a lack of sufficient metabolic stimulus (volume) from the exercise session based on the relatively low maximal strength in this population. This notion is supported by the finding that junior weightlifters (14–18 years of age) with ª 2010 Adis Data Information BV. All rights reserved.

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more than 2 years of weight-lifting experience produce a greater acute testosterone response than those with less than 2 years of experience.[79] In older (‡59 years)[27,62,78,101] and middle-aged (38–53 years)[62,81,101] men a bout of resistance exercise can elicit a significant elevation in circulating total and free testosterone, but the magnitude of this elevation is generally smaller compared with that in younger (20–30 years) men.[27,78,81,101] This attenuated exercise-induced increase is especially apparent for free testosterone. The discrepancy between findings for free testosterone and total testosterone could be due to the increased concentrations of SHBG and reduced concentrations of albumin found with aging.[102,103] The findings for training effects on the acute testosterone response to resistance exercise in older men are equivocal with both no effects and augmented responses found. A 10-week periodized strength-power training programme led to increased pre-exercise free testosterone and post-exercise total testosterone concentrations in ~60-year-old men with no changes found for ~30-year-old men undergoing the same training programme.[78] In contrast, Ha¨kkinen and colleagues[62] found no changes in the acute preor post-resistance exercise testosterone response following 6 months of strength training in older (~70 years old) and middle-aged (~40 years old) men. Both studies,[62,78] however, found that there were no changes in testosterone concentrations of older men at rest (i.e. not immediately preexercise) after the resistance training period. It is difficult to speculate on the cause of the discrepancy in the findings for the acute testosterone response to resistance exercise, but it is possible that an anticipatory response was present following training in the study by Kraemer et al.[78] In middle-aged (~40-year-old) and older (~60to 70-year-old) women who are untrained, total and free testosterone do not change acutely in response to a high (5 sets of 10RM in the leg press)[62,104] or moderate (1 set of 13 exercises at 80% of 1RM)[105] volume resistance exercise session. Long-term strength training does not appear to change resting total and free testosterone[62,104-107] or post-exercise total testosterone concentrations in response to high[62,104] or Sports Med 2010; 40 (12)

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moderate volume.[105] One study, however, found that in recreationally trained 19- to 69-year-old women, total testosterone increased acutely following a high-volume (3 sets of 8 exercise at 10RM and 1 minute rest between sets) resistance exercise session and that this increase was not affected by age.[55] Findings on the effect of training on the acute free testosterone response to resistance exercise in aging women are equivocal. In both middle-aged and older women, an acute increase in free testosterone following resistance exercise (5 sets of 10RM in the leg press) after 6 months of resistance training has been observed.[62] A different study by the same authors[104] using similar older female populations and the almost identical acute resistance exercise protocol, (2 minutes instead of 3 minutes of rest between sets) found that 21 weeks of strength training did not change the acute free testosterone concentrations following a bout of resistance exercise. Based on these findings, it appears that the testosterone response to resistance exercise and training in aging women is similar to that for younger women. In both younger and older women, resistance exercise can induce an acute increase in circulating testosterone; however, the selection among the acute programme variable domains required for this increase to occur has not yet been fully determined. 3.4 Effect on Androgen Receptor

Only a limited number of studies have examined the acute AR response to a bout of resistance exercise in men;[12,65-67,74,92,108] only one study appears to have been conducted in women.[92] From the studies in men combined with the findings from animal research,[109,110] it appears that the AR concentration is initially reduced acutely following a bout of resistance exercise, but that AR is upregulated during the later stages (several hours after exercise) of recovery from resistance exercise. The timeline for this AR down- and upregulation has not been fully elucidated. Ratamess et al.[66] and Vingren et al.[92] found that in young resistance-trained men 6 sets of 10 repetitions in the squat exercise with 2 minutes of rest between sets resulted in a sigª 2010 Adis Data Information BV. All rights reserved.

Vingren et al.

nificant decline in AR 1-hour post-exercise. Similarly, Lee et al.,[35] using a male rat model, found that overload ablation caused a decrease in AR 24-hours post-overload introduction. In contrast to these findings, Kraemer and colleagues,[67] using a similar population to Ratamess et al.[66] and Vingren et al.[92] but a slightly different resistance exercise protocol (4 sets of 10 repetitions of squat, bench press and shoulder press and row with 2 minutes of rest between sets), found that AR increased 1-hour post-exercise when subjects ingested either water or a carbohydrate-protein drink immediately after exercise. The increase in AR was much greater with the carbohydrateprotein drink compared with the water ingestion condition suggesting a potent effect of nutrition on the AR response to resistance exercise.[67] The differences in AR expression between the studies in the fasted conditions (water) were observed despite similar testosterone responses and involvement of the muscle sampled for AR. This indicates that other variables such as time from onset of exercise or testosterone exposure might affect the AR response. Finally, Spiering et al.[74] recently found that in untrained men, AR was upregulated 3 hours post-resistance exercise only when the exercise bout produced an increase in circulating testosterone. Although not considered resistance exercise, it is also worth noting that strenuous swimming has been shown to upregulate AR acutely (within hours) following exercise.[111] Combined, these studies suggest that after an initial reduction in AR following exercise, an acute upregulation of AR in the hours following a bout of resistance exercise in men occur, although the timeline for the events in this response is uncertain. The only finding for women suggest that the AR response is similar among men and women except that the initial reduction in AR is present 10-minutes post-exercise and AR returns to baseline by 70-minutes post-exercise.[92] Findings for AR during the later stages of recovery from resistance exercise are more consistent. Forty eight hours following a bout of resistance training AR mRNA is upregulated.[65,108] However, Willoughby and Taylor[65] did not find an increase in AR protein content until 48 hours after two consecutive resistance exercise sessions Sports Med 2010; 40 (12)


separated by 48 hours. In animal models, electrical stimulation[110,112] and overload ablation[109] result in an acute upregulation of AR during the later stages of recovery (several days after the initial overload stimulus). Collectively, these studies suggest that the acute AR response to resistance exercise includes a stabilization phase followed by an acute initial downregulation after which an upregulation of AR to above baseline concentrations occur. Despite the few studies on the acute AR response to resistance exercise, it appears that factors such as exercise volume and nutrient intake affect this response. Ratamess et al.[66] showed that a single set of 10 repetitions in the squat exercise did not alter AR 1-hour post-exercise. This was mirrored by limited changes in circulating lactate and hormonal concentrations suggesting that a minimum of volume is needed to induce AR changes in response to resistance exercise. Post-exercise ingestion of a drink containing protein and carbohydrate led to an increase in AR 1-hour post-exercise with or without L-carnitine supplementation.[67] Interestingly, it has also been demonstrated that when a protein and/or carbohydrate drink is ingested before or after resistance exercise, the increase in testosterone is attenuated during exercise, and the reduction in testosterone during recovery is augmented compared with a placebo condition.[67,113,114] The authors of these studies suggested that increased testosterone uptake by the AR might account for this attenuated testosterone response. 4. Conclusions As a hormone, circulating testosterone signalling resides within a multivariate system of anabolic signals for many different target tissues through the body, and the exact role of testosterone in the temporal timeframes of a resistance training programme are hard to pinpoint. Yet, dismissal of its anabolic role in the human body due to a lack of a simple correlation or comparison of punctual circulating testosterone concentrations with variables that have accumulated over time with training (e.g. muscle size, strength) is over-simplistic at best and understates the importance of this hormone to the physiology of ª 2010 Adis Data Information BV. All rights reserved.

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adaptational mechanisms in the human body to exercise stressors. The interaction of testosterone with a host of receptors on different tissues and the resulting signalling processes are vital to human health and performance. The increase in testosterone found in men is important for the resistance exercise-induced adaptations. The importance of testosterone for adaptations to resistance exercise in women has not been substantially examined, but it appears that testosterone plays only a minor role. Acknowledgements No sources of funding were used to assist in the preparation of this review. The authors have no potential conflicts of interest that are directly relevant to the content of this review.

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78. Kraemer WJ, Hakkinen K, Newton RU, et al. Effects of heavy-resistance training on hormonal response patterns in younger vs older men. J Appl Physiol 1999 Sep; 87 (3): 982-92 79. Kraemer WJ, Fry AC, Warren BJ, et al. Acute hormonal responses in elite junior weightlifters. Int J Sports Med 1992 Feb; 13 (2): 103-9 80. Reeves GV, Kraemer RR, Hollander DB, et al. Comparison of hormone responses following light resistance exercise with partial vascular occlusion and moderately difficult resistance exercise without occlusion. J Appl Physiol 2006 Dec; 101 (6): 1616-22 81. Hakkinen K, Pakarinen A, Newton RU, et al. Acute hormone responses to heavy resistance lower and upper extremity exercise in young versus old men. Eur J Appl Physiol Occup Physiol 1998 Mar; 77 (4): 312-9 82. Durand RJ, Castracane VD, Hollander DB, et al. Hormonal responses from concentric and eccentric muscle contractions. Med Sci Sports Exerc 2003 Jun; 35 (6): 937-43 83. Kraemer RR, Hollander DB, Reeves GV, et al. Similar hormonal responses to concentric and eccentric muscle actions using relative loading. Eur J Appl Physiol 2006 Mar; 96 (5): 551-7 84. Krylow AM, Sandercock TG. Dynamic force responses of muscle involving eccentric contraction. J Biomech 1997 Jan; 30 (1): 27-33 85. Erskine J, Smillie I, Leiper J, et al. Neuromuscular and hormonal responses to a single session of whole body vibration exercise in healthy young men. Clin Physiol Funct Imaging 2007 Jul; 27 (4): 242-8 86. Kvorning T, Bagger M, Caserotti P, et al. Effects of vibration and resistance training on neuromuscular and hormonal measures. Eur J Applied Physiol 2006 Mar; 96 (5): 615-25 87. Di Loreto C, Ranchelli A, Lucidi P, et al. Effects of wholebody vibration exercise on the endocrine system of healthy men. J Endocrinol Invest 2004 Apr; 27 (4): 323-7 88. Bosco C, Iacovelli M, Tsarpela O, et al. Hormonal responses to whole-body vibration in men. Eur J Appl Physiol 2000 Apr; 81 (6): 449-54 89. Spreuwenberg LP, Kraemer WJ, Spiering BA, et al. Influence of exercise order in a resistance-training exercise session. J Strength Cond Res 2006 Feb; 20 (1): 141-4 90. Ratamess NA, Falvo MJ, Mangine GT, et al. The effect of rest interval length on metabolic responses to the bench press exercise. Eur J Appl Physiol 2007 May; 100 (1): 1-17 91. Ahtiainen JP, Pakarinen A, Alen M, et al. Short vs long rest period between the sets in hypertrophic resistance training: influence on muscle strength, size, and hormonal adaptations in trained men. J Strength Cond Res 2005 Aug; 19 (3): 572-82 92. Vingren JL, Kraemer WJ, Hatfield DL, et al. Effect of resistance exercise on muscle steroid receptor protein content in strength-trained men and women. Steroids 2009 Nov-Dec; 74 (13-14): 1033-9 93. Marx JO, Ratamess NA, Nindl BC, et al. Low-volume circuit versus high-volume periodized resistance training in women. Med Sci Sports Exerc 2001 Apr; 33 (4): 635-43


Vingren et al.

94. Nakamura Y, Hornsby PJ, Casson P, et al. Type 5 17betahydroxysteroid dehydrogenase (AKR1C3) contributes to testosterone production in the adrenal reticularis. J Clin Endocrinol Metab 2009 Jun; 94 (6): 2192-8 95. Kraemer WJ, French DN, Spiering BA, et al. Cortitrol supplementation reduces serum cortisol responses to physical stress. Metab Clin Exper 2005 May; 54 (5): 657-68 96. Korth-Schutz S, Levine LS, New MI. Serum androgens in normal prepubertal and pubertal children and in children with precocious adrenarche. J Clin Endocrinol Metab 1976; 42 (1): 117-24 97. Feldman HA, Longcope C, Derby CA, et al. Age trends in the level of serum testosterone and other hormones in middle-aged men: longitudinal results from the Massachusetts male aging study. J Clin Endocrinol Metab 2002 Feb; 87 (2): 589-98 98. Vermeulen A, Deslypere JP, De Meirleir K. A new look to the andropause: altered function of the gonadotrophs. J Steroid Biochem 1989 Jan; 32 (1B): 163-5 99. Pullinen T, Mero A, MacDonald E, et al. Plasma catecholamine and serum testosterone responses to four units of resistance exercise in young and adult male athletes. Eur J Appl Physiol Occup Physiol 1998 Apr; 77 (5): 413-20 100. Fahey TD, Rolph R, Moungmee P, et al. Serum testosterone, body composition, and strength of young adults. Med Sci Sports 1976 Spring; 8 (1): 31-4 101. Baker JR, Bemben MG, Anderson MA, et al. Effects of age on testosterone responses to resistance exercise and musculoskeletal variables in men. J Strength Cond Res 2006 Nov; 20 (4): 874-81 102. Hayashi T, Yamada T. Association of bioavailable estradiol levels and testosterone levels with serum albumin levels in elderly men. Aging Male 2008 Jun; 11 (2): 63-70 103. Rodriguez A, Muller DC, Metter EJ, et al. Aging, androgens, and the metabolic syndrome in a longitudinal study of aging. J Clin Endocrinol Metab 2007 Sep; 92 (9): 3568-72 104. Hakkinen K, Pakarinen A, Kraemer WJ, et al. Selective muscle hypertrophy, changes in EMG and force, and serum hormones during strength training in older women. J Appl Physiol 2001 Aug; 91 (2): 569-80 105. Borst SE, Vincent KR, Lowenthal DT, et al. Effects of resistance training on insulin-like growth factor and its binding proteins in men and women aged 60 to 85. J Am Geriatr Soc 2002 May; 50 (5): 884-8 106. Petrella JK, Kim JS, Cross JM, et al. Efficacy of myonuclear addition may explain differential myofiber growth among resistance-trained young and older men and women. Am J Physiol 2006 Nov; 291 (5): E937-46 107. Daly RM, Dunstan DW, Owen N, et al. Does highintensity resistance training maintain bone mass during moderate weight loss in older overweight adults with type 2 diabetes? Osteoporos Int 2005 Dec; 16 (12): 1703-12 108. Bamman MM, Shipp JR, Jiang J, et al. Mechanical load increases muscle IGF-I and androgen receptor mRNA concentrations in humans. Am J Physiol 2001 Mar 1; 280 (3): E383-90 109. Lee WJ, Thompson RW, McClung JM, et al. Regulation of androgen receptor expression at the onset of functional overload in rat plantaris muscle. Am J Physiol Regulatory Integrative Comp Physiol 2003 Nov 1; 285 (5): R1076-85

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110. Inoue K, Yamasaki S, Fushiki T, et al. Rapid increase in the number of androgen receptors following electrical stimulation of the rat muscle. Eur J Appl Physiol Occup Physiol 1993 Jan 1; 66 (2): 134-40 111. Tchaikovsky VS, Astratenkova JV, Basharina OB. The effect of exercises on the content and reception of the steroid hormones in rat skeletal muscles. J Steroid Biochem 1986 Jan; 24 (1): 251-3 112. Inoue K, Yamasaki S, Fushiki T, et al. Androgen receptor antagonist suppresses exercise-induced hypertrophy of skeletal muscle. Eur J Appl Physiol Occup Physiol 1994 Jan 1; 69 (1): 88-91 113. Kraemer WJ, Volek JS, Bush JA, et al. Hormonal responses to consecutive days of heavy-resistance exercise


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with or without nutritional supplementation. J Appl Physiol 1998 Oct; 85 (4): 1544-55 114. Chandler RM, Byrne HK, Patterson JG, et al. Dietary supplements affect the anabolic hormones after weighttraining exercise. J Appl Physiol 1994 Feb; 76 (2): 839-45

Correspondence: Dr William J. Kraemer, Human Performance Laboratory, Department of Kinesiology, 2095 Hillside Road, Unit-1110, University of Connecticut, Storrs, CT 06269-1110, USA. E-mail: [email protected]

Sports Med 2010; 40 (12)

Sports Med 2010; 40 (12): 1055-1074 0112-1642/10/0012-1055/$49.95/0

REVIEW ARTICLE


Current Best Evidence Recommendations on Measurement and Interpretation of Physical Function in Patients with Chronic Kidney Disease Pelagia Koufaki1 and Evangelia Kouidi2 1 School of Life Sciences, Heriot-Watt University, Edinburgh, Scotland 2 Laboratory of Sports Medicine, Aristotle University of Thessaloniki, Thessaloniki, Greece

Contents Abstract. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Literature Search Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Domains of Physical Function Assessment Spectrum. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1 Choosing a Physical Function Outcome Measure. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Clinical Utility of Physical Function Outcomes in Patients with Chronic Kidney Disease . . . . . . . . . . . 4. Physical Function Assessment – Tools, Methods and Protocols . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1 Assessment of Exercise Tolerance/Capacity (Physiological Impairment) . . . . . . . . . . . . . . . . . . . 4.1.1 Proposed Cardiorespiratory Fitness Assessment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1.2 Proposed Muscular Fitness Assessment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2 Assessment of Functional Limitations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2.1 Proposed Walking Tests . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2.2 Proposed Functional Muscular Fitness Tests . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3 Assessment of Functional Disability (Self-Reported Physical Functioning). . . . . . . . . . . . . . . . . . . 5. Special Considerations for Physical Function Assessment. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6. Discussion and Future Considerations for Research. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Abstract

1055 1057 1057 1058 1059 1060 1060 1060 1063 1065 1066 1066 1068 1068 1069 1071

Chronic kidney disease (CKD) is becoming a serious health problem throughout the world and is one of the most potent known risk factors for cardiovascular disease. Deterioration of physical function is accelerated in patients with CKD to levels that significantly impact on clinically and patient-important outcomes such as morbidity, employment, quality of life and, ultimately, survival. However, meaningful interpretation of the existing physical function-related literature in adult patients with CKD is hindered, possibly due to inconsistent choice of methodology, assessment tools and reporting of data. The current comprehensive review of the literature aims to provide the theoretical rationale and framework for physical function assessment and to identify the prevailing approaches to (i) the characterization (classification and terminology), (ii) interpretation, and (iii) reporting of physical function assessment in people with CKD. Comprehensive assessment of

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physical function can provide important information about the presence of ‘physiological impairment’ at a body systems level (exercise tolerance under well controlled, laboratory-based procedures), ‘functional limitations’ (physical performance during tasks imitating usual daily, personal or occupational tasks) and ‘functional disability’ (via self-reported physical functioning in the context of a socio-cultural environment). The selection of physical function assessment tools should be guided by the primary purpose of the assessment (e.g. research or routine clinical monitoring), by the overall scientific ‘soundness’ of the chosen tool (e.g. validity, utility, reproducibility, responsiveness characteristics) and by operational factors (e.g. patient collaboration, cost, personnel expertise). Recommendations for tests, methods and protocols are therefore presented, for the assessment of cardiorespiratory and muscular fitness, physical performance and self-reported physical functioning. These recommendations are based on synthesis of available information as derived from controlled exercise training interventions in adult patients with CKD. Special considerations for physical function assessment and suggestions for future research are also addressed. Such an information synthesis might promote greater standardization of the physical function assessment of patients with CKD in routine clinical care or research settings. This would potentially lead to generation of adequate scientific decision-making criteria to help researchers and healthcare providers in selecting the most appropriate measures according to the physical function areas assessed, and to accurately and meaningfully characterize and compare patients’ responses to therapeutic interventions.

The prevalence of chronic kidney disease (CKD) is increasing worldwide primarily as a consequence of the alarmingly rapid rise in diabetes mellitus and hypertension.[1] Renal disease is a complex chronic condition that has a significant impact not only on the mortality rates of patients, but also on morbidity and hospitalization rates, physical function and independent living, employment and quality of life.[2] Adequate physical function is a key component of independent living and good quality of life. Higher levels of physical function and habitual physical activity (PA) have been shown to be related to clinically important outcomes, such as enhanced longevity, less morbidity and hospitalization rates, and enhanced quality of life, in patients receiving dialysis-based renal replacement therapy.[3-9] Deterioration of physical function has been reported to start early in the disease process and may result in severe disability, especially in the older cohort of patients in the more advanced stages of the disease.[10,11] Patients commonly re-


port reduced levels of physical functioning and severe debilitating symptoms such as muscle and joint pain, muscle weakness and fatiguability, breathlessness, tiredness, lack of energy, etc.[2] It is important that physical functioning of patients across the discrete stages of renal function is comprehensively and accurately characterized based on scientifically sound outcome measures, and that changes in physical functioning levels can also be meaningfully interpreted. Only then will we be able to demonstrate and evaluate the effectiveness of rehabilitation or other medical interventions on physical function changes and associated outcomes. Currently, there is no standardized way to assess or describe physical function and its components in patients with CKD. A literature search reveals a plethora of physical functioning evaluation outcomes and techniques that hinder informative synthesis and meaningful interpretation of existing evidence on physical functioning levels and their responses to various interventions. The

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Physical Function Assessment in Patients with CKD

challenge faced, therefore, is to identify a set of physical function outcomes that are relevant to patients and service providers, which can be used in the existing renal healthcare environments. The purpose of this article is to review existing physical function literature upon which to base recommendations on standardizing physical function terminology and classification, interpretation and reporting of data. Hopefully, this review will contribute towards a more unifying approach in physical function assessment and evaluation of patients with CKD that can be applied in most healthcare settings. 1. Literature Search Methods A literature search of the databases Web of Science, MEDLINE and CINAHL was conducted using search terms such as ‘exercise’, ‘exercise training’, ‘rehabilitation’, ‘physical function’, ‘functional capacity’, ‘exercise tolerance’, . . ‘VO2peak/VO2max’, ‘physical performance’, ‘fitness’, ‘muscle strength’, ‘cardiorespiratory fitness’, ‘exercise testing’, ‘six-minute walk test’, ‘sit to stand’, ‘quality of life’, ‘health-related function and dialysis’, ‘renal failure’, ‘renal disease’, ‘chronic kidney disease’, ‘transplantation’ and ‘kidney failure’. The reference lists of studies and review articles were also hand searched. English languageonly restrictions were applied. All controlled exercise interventions (published as full papers) in adult patients with CKD that reported physical function outcomes were included. No restrictions to search periods were applied. 2. Domains of Physical Function Assessment Spectrum Physical function assessment purpose, methodology and measurement tools may differ across different groups of people (e.g. athletes, patients, children, etc.). For patients with CKD, assessment of health-related physical functioning levels is the outcome of interest. Health-related physical function can be defined as a component of healthrelated fitness (cardiorespiratory/muscular fitness, body composition and flexibility) that is concerned with characterizing an individual’s ability ª 2010 Adis Data Information BV. All rights reserved.

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to perform and participate in life activities necessary for normal physical, emotional, mental and social function.[12] A number of factors may influence overall health-related function, ranging from severe physiological and structural deviations from expected normal, to environmental and personal variations. Conventionally, the assessment and characterization of physical function in various clinical populations is accomplished within a measurement spectrum that groups measures according to whether they determine (i) physiological impairment at the level of one or more organs or systems; (ii) functional limitations at the level of the person as a whole; and (iii) disability/selfreported physical functioning at the level of a person as a whole within its associated social and cultural environment.[2,12,13] For standardization purposes and to improve communication among users, we propose that the same classification of physical function and discriminatory terminology is also used in reports involving patients with CKD as follows: Physiological impairment (as determined via exercise tolerance/capacity tests) is usually determined by means of well established ‘objective’, mainly laboratory environment-based techniques. This refers to the level of functioning for one or more body organs or systems, under well defined and countable maximal or submaximal amounts of physical stress. The characterization of exercise tolerance often requires specially trained personnel, expensive equipment and specific analytical skills/knowledge to interpret the data that may limit its practical utility, especially in routine clinical assessment. Functional limitations (as determined via physical performance tests) are usually determined by means of ‘objective’ and expedient physical performance tests. This refers to the measured ability of an individual to execute physical tasks that mostly imitate activities encountered in daily living such as body position transfers, in a standardized environment, which resembles the usual living environment. The amount of physical stress imposed on individuals is mostly regulated by the individual’s willingness/ability to perform the required physical task. The implementation Sports Med 2010; 40 (12)

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of physical performance tests is relatively simple, quick and cost effective, does not require any specially trained personnel and interpretation of data is ‘common sense’ and immediate. Therefore, they are the ideal option for objective assessment of physical function in routine healthcare/ clinical settings. However, familiarization and adherence to the recommended administration protocols for all physical function tests should be ensured in order to achieve a standardized approach for good quality control. Functional disability (self-reported physical functioning) is usually determined by means of self- and/or proxy reports and, thus, ‘subjective’, questionnaires. This domain of the physical function assessment spectrum reflects one’s perception of the ability to perform a physical task within a given socio-cultural environment. These methodologies can capture important patient-focused information relating to their own feelings, fears, dependencies and other behavioural and psychological factors in relation to physical function and PA that cannot be obtained in any other way. However, self-report methods are also subject to a number of external influences such as mood, cognition, education, etc. Characterization of self-reported physical functioning is easy, cost effective, time efficient and risk free. Habitual PA levels: A common parameter that underpins and, to a certain extent, determines adequate health-related physical function, is the amount (frequency and intensity) of habitual PA, which essentially captures the idea of ‘active living’. PA is defined as any body movement that results in energy expenditure above that of the resting metabolic requirements. Habitual levels of PA can be quantified objectively by devices such as accelerometers, or subjectively by self-reported questionnaires such as the 7-day PA recall questionnaire, or the PA scale for the elderly.[14] 2.1 Choosing a Physical Function Outcome Measure

With the aforementioned recommended categorization of physical function domains in mind, ª 2010 Adis Data Information BV. All rights reserved.

Koufaki & Kouidi

it becomes apparent that comprehensive characterization of physical function in patients with CKD is a multi-dimensional task. Often, professionals face dilemmas about which domain to assess for research or for routine purposes, or which assessment tool to use. Currently, there is no consensus on a single best approach or it may even be inappropriate to recommend a single best tool to characterize physical function in CKD. Research reports have highlighted that even the ‘gold standard’ measurement of integrated .physiological assessment (peak oxygen uptake [VO2peak]), when used in isolation, may underestimate (estimates ~35% deficit compared to age, sex and PA matched healthy individuals) the true extent of functional limitations, especially in tasks that are associated with daily independent living (up to 60–102% deficits in sit-tostand [STS], stair climb and descent tests).[12,15,16] Assessment of physical function using tools that cover the measurement spectrum, therefore, could provide a more accurate picture of the physical functioning pathway in CKD patients. In routine clinical practice, however, assessing patients using a battery of assessment tools is not always feasible. As a rule of thumb, in cases where all three physical function assessment domains are not possible, the primary purpose of the assessment should be the main determinant for which domain of physical function should be assessed. For example, if physical function assessment is part of a research investigation, with the aim to understand and explain underlying mechanisms responsible for changes in physical function, then objective, robust, physiological exercise tolerance tests should be the first option to explore. On the other hand, routine assessment of physical function as part of monitoring patients’ clinical status can be provided by simpler and quicker, objective physical performance tests and/or by self-reported physical function questionnaires. The final choice of course will also be determined by practicalities such as access to equipment and human resources and patient baseline health status collaboration/ consent etc. (see table I for commonly reported advantages and disadvantages). The choice of which assessment tool to use for each domain of physical function depends on the Sports Med 2010; 40 (12)


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Table I. Some factors commonly reported in the literature as determinants of physical function assessment choice in patients (pts) with chronic kidney disease Advantages

Disadvantages

Objective (pts’ ‘measured’ ability of what and how much they can physically do)

Easier to quantify on a continuous scale Less susceptible to ‘floor’ or ‘ceiling’ effects Less susceptible to external factor variations (e.g. cognitive function, language, education, environment) Better for cross-cultural and geographical comparisons

Additional time demands on staff and pts Physical effort Carry certain amount of risks May require additional staff training Vary in complexity and costs

Subjective (pts’ ‘perceived’ ability of what and how much they can physically do)

Minimum effort, interference and time Risk free Capture how pts feel and perform in their usual environment

Cannot provide explanatory physiological mechanisms for changes Subject to floor/ceiling effects Shown to overestimate physical function

overall scientific ‘soundness’ of the chosen tool. Briefly, the scientific criteria necessary in order to deem a test as a suitable screening tool are (i) validity (does it measure what it claims to measure?); (ii) utility (its usefulness in clinical practice with prognostic and discriminatory qualities); (iii) reproducibility (is it consistent in producing similar results with repeat measurements?); and (iv) responsiveness (is it sensitive enough to track changes over time?). See Lohr et al.[17] for a more detailed generic review on the above criteria. 3. Clinical Utility of Physical Function Outcomes in Patients with Chronic Kidney Disease For the implementation of physical function assessment in practice, it is essential that renal care professionals/research investigators can accurately characterize physical function, but also interpret change in physical function measurements over time. To achieve this, valid and clinically meaningful cut-off points or ranges of ‘normal’ physical function values corresponding to different stages of CKD are required. This type of information would be important in order to determine the amount of change that is associated with worsening or improving prognosis and, also, what actually constitutes a meaningful change response to an intervention.[18] The following section focuses on the current available data on ª 2010 Adis Data Information BV. All rights reserved.

the predictive and discriminatory value of physical function-related outcomes in CKD patients. In reference to habitual PA levels and sedentary behaviour as assessed by various self-reported questionnaires, a number of studies have reported significant morbidity and mortality benefits for patients who reported higher levels of habitual PA than their sedentary counterparts.[3,19] In the study by Stack et al.,[8] having at least 2–5 physically active days a week (but not all days) and reporting little or no limitations in moderate to vigorous intensity activities was associated with a 30% reduction in all-cause mortality risk in dialysis patients. In contrast, the study by Chen et al.[20] did not observe a beneficial effect on survival over an 11-year observation period in predialysis patients who reported higher levels of habitual PA compared with those who reported lower levels of habitual PA. However, what constituted a ‘higher’ versus a ‘lower’ dose of PA in the latter study was not clearly defined. Taken together, these reports are well in line with the current recommendations for PA in the healthy adult population for good physical functioning and health-related benefits.[21] This level of PA participation is probably more likely to impact on aspects of health-related physical fitness such as cardiorespiratory and muscular fitness. Prospective mortality/morbidity studies focusing on objective or self-reported measurements reflecting these health-related fitness components in dialysis patients reveal a statistically Sports Med 2010; 40 (12)

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significant survival benefit for those patients with better health-related fitness. In particular, Sietsema et al.[7] followed a group of dialysis patients who had.cardiorespiratory fitness categorized by. means of VO2peak for 3.5 years. Patients with VO2peak >17.5 mL/kg/min had a significantly better survival rate than patients with the same index that was less than this cut-off point. Muscle mass and muscle function-related measures have also been implicated in predicting disease progress and survival in patients receiving dialysis therapy.[9,22,23] Reduced levels of muscular fitness, reflected in muscle strength/power, endurance and flexibility indices, have also been associated with the early detection of adverse clinical outcomes such as severe muscle loss and malnutrition.[24,25] Loss of muscle strength and power is the immediate manifestation of altered neuromuscular recruitment patterns, muscle quantity and/or quality, and this may be reflected in simple measurements of strength such as hand grip (HG) strength. Isometric HG strength, measured by means of hand-held dynamometers, has been identified as a significant prognostic indicator of survival in male patients[9] and is the strongest independent marker of malnutrition.[25] It has been reported that patients (with kidney failure at a stage that required initiation of dialysis therapy or who had received transplantation) who had a value for HG strength greater than the group median value, had a significantly better survival prognosis over a 3-year period.[9] Unfortunately, the cut-off median value for HG strength from the above study was not clearly reported. In addition, the ability to rise from a chair even once, may have a discriminatory capacity to identify patients with severe functional limitations who may be in immediate need of intervention. Brodin and colleagues[26] recently reported significant associations between a decline in glomerular filtration rate and the presence of diabetes, and in the ability to perform one STS. Mercer et al.[27] have also reported significant associations between nutritional status that was assessed using a subjective global questionnaire and STS tests, and with a STS-60 test in particular, explaining 52% of the shared variance. These observations suggest that STS performance may ª 2010 Adis Data Information BV. All rights reserved.

Koufaki & Kouidi

accurately reflect changes in muscle mass and function and other aforementioned factors, especially in the context of diabetes and diminishing renal function. Self-reported, physical function status, evaluated using the physical component score (PCS) from the Short Form (SF)-36 questionnaire, has also been shown to carry a significant hospitalization and survival prognostic value for patients receiving dialysis therapy. The studies by Mapes et al.[4] and Lowrie et al.[5] suggested that a 1-point increase in the PCS translated into a 2% reduction in mortality rate and that a total PCS of 1.15 RPE report of 20 . VO2peak plateaus BP >220/110 mmHg Cannot maintain protocol instructions

Comments:

+

NRCP; 7

Petersen et al.,

2010

NRCT; 24

-1

Serious cardiac arrhythmias Evidence of cardiac ishaemia No increases in BP with increasing workload Symptoms such as dizziness, angina, Lack of responsiveness to oral and/or visual signs Pts request Equipment failure

Comfortable walking speed Grade: 1–2 METs increase

RCT; 95

NRCT; 51 Treadmill

Painter et al.,[58] 2002

2007 van den Ham et al.,

NRCT; 10 Poortmans et al.,[56] 1997


Cycle ergometer

RCT; 48


Transplants

NRCT; 20

Beasley et al.,[53] 1986

[57]

RCT; 33

NRCT; 18

Ouzouni et al.,[52] 2009


max. = maximum; METs = metabolic equivalents; mph = miles per hour; NRCT = non-randomized controlled trial; pt(s) = patient(s); RCT = randomized controlled trial;. RER = . respiratory exchange ratio; RPE = ratings of perceived exertion; rpm = revolutions per minute; VO2peak = peak oxygen uptake; + indicates use of gas exchange to determine VO2peak; . - indicates lack of use of gas exchange for VO2peak determination.

-

10–25 W min-1 increase Pedalling rate: 60–70 rpm

+

+

10 W min-1 increase

+

+

+ Increments of 0.5 METs/min at a comfortable speed

+

+

RCT; 48

RCT; 34

Konstantinidou et al.,[50] 2002

Kouidi et al.,[51] 2004

Study design; no. of pts (allocated) Study, year

Table II. Contd

Testing protocol

Gas exchange

Termination criteria


1063

and aim to maintain this speed throughout the test. For most patients this speed is around 2.5–3.5 mph or 4–5.5 km/h starting from 0% grade increments and increasing to 1–3% every minute depending on individual characteristics. For example, 3% grade increments may be more appropriate for younger individuals without additional co-morbidities, whereas a 1% increment may be more suitable for older, more co-morbid individuals. Test-retest reproducibility information on cardiorespiratory fitness-related outcomes in patients with CKD is scarce in the literature. One study[59] has reported standard errors of measurement (SEM) and corresponding coefficients of variation (CV%) for a number of different symptom-limited and VT-anchored indices, obtained during incremental . cycle ergometry. Indicatively, the CV% for VO2peak. and at VT was 4.7% and 6.6%, respectively. VO2peak is the most widely reported physical function index in controlled exercise intervention studies (table II). This index seems to be the more consistent in its response to exercise interventions of various modalities and intensities (noted average increases in the range of 11–42%, which exceed reported CV%) in comparison to responses obtained from the control groups. Therefore, overall, this index seems to be responsive and sensitive to exercise-based interventions. 4.1.2 Proposed Muscular Fitness Assessment

Muscular fitness is broadly defined as maximum strength and muscle endurance. Strength can be defined as the maximum force that a muscle group can generate against resistance. Force development can result into movement (dynamic strength) or not (isometric strength). An important element of strength quality is also muscle power, which reflects the muscle’s ability to perform work in relation to time (force and velocity of movement). Muscle endurance enables a muscle group to tolerate fatigue during repeated and sustained muscular contractions against specified resistance. As it is evident from table III, physiological muscular fitness has been assessed using a wide range of techniques and protocols for nearly all the main muscle groups involving a range of joint angles and/or limb movement speeds. No adverse Sports Med 2010; 40 (12)

Study, year

Method

Study design; no. of pts (randomized)

Evaluation outcome

Termination criteria

Castaneda et al.,[32] 2001

1RM

RCT; 26

Knee extensor absolute dynamic strength

Pts request

Heiwe et al.,[30] 2001

1RM

RCT; 25

Knee extensor absolute dynamic strength

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Table III. Physiological muscular fitness assessment methodology in published controlled exercise interventions in adults with chronic kidney disease

Pre-dialysis

Max. repetitions at 60% of 1RM frequency: 60 movements/min Heiwe et al.,[60] 2005

1RM

Relative dynamic endurance RCT; 12

Max. repetitions at 60% of 1RM frequency: 60 movements/min Clyne et al.,[28] 1991

Knee extensor absolute dynamic strength Relative dynamic endurance

Max. repetitions at 60% of 1RM frequency: 60 movements/min Time to exhaustion with 3 kg around the ankles for males and 2 kg for females

NRCT; 10

Isokinetic dynamometry

RCT; 68

Knee extensor relative dynamic endurance Knee extensor/hip flexor isometric endurance

Dialysis Johansen et al.,[61] 2006

3RM

Knee extensor strength Knee extensor/hip abductor/flexor dynamic strength

Cheema et al.,[62] 2007

Isometric dynamometry

RCT; 44

Knee extensor/hip abductors/triceps strength

Segura-Ortı´ et al.,[44] 2009

Isometric dynamometry

RCT; 25

Knee extensor/hip abductors/triceps strength

Petersen et al.,[40] 2010

Isometric and isokinetic dynamometry

NRCP; 7

Knee extensor strength and muscular fatigue

Leg-power instrument

NRCT; 24

Storer et al.,[39] 2005

5RM

Inability to continue due to adverse symptom development Cannot maintain protocol instructions Comments: Familiarization sessions may be required; Whole body and muscle group specific warm-up sessions are required

Knee and hip extensor strength/power Hamstring and quadriceps dynamic strength

5RM

RCT; 38

Hamstring and quadriceps dynamic strength

Headley et al.,[64] 2002

HG test

NRCP; 10

Non-dominant hand isometric forearm muscle strength

Yurtkuran et al.,[65] 2007

HG test

RCT; 37

Non-dominant hand isometric forearm muscle strength

Rus et al.,[66] 2005

HG test (mean score of two trials)

NRCT; 26

Both hand isometric forearm muscle strength

Hsieh et al.,[67] 2006

HG test (mean score of three trials)

NRCT; 54

Transplants van den Ham et al.,[57] 2007


NRCT; 95

Knee extensor strength



RCT; 51

Knee extensor strength

HG = hand grip; max. = maximum; NRCP = non-randomized control period; NRCT = non-randomized controlled trial; pts = patients; RCT = randomized controlled trial; RM = repetitions maximum.

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DePaul et al.,[63] 2002


complications have been reported following correct and properly supervised testing procedures. Isokinetic measurement of strength requires expensive equipment and specially trained operators that may not be easily accessible or obtainable. Isometric strength assessment may also require expensive equipment, although there have been five studies that have used a hand dynamometer to evaluate isometric maximal HG strength.[64-68] Investigators need to bear in mind that isometric force production is only relevant to the specific musclejoint angle and muscle group assessed and therefore it may not accurately reflect daily operational muscle strength. Conversely, hand-held dynamometers are relatively inexpensive, execution of the test is quicker than any other muscle strength or endurance test and is probably less uncomfortable for the patients. Nonetheless, as an assessment tool, it has been reported to carry some prognostic and discriminatory value and therefore may be clinically useful. Probably the most relevant components of muscular fitness for patients with CKD are measurements of dynamic muscle strength and power and muscle endurance as these qualities are strongly implicated in activities of daily living, are good indicators of functional muscle mass and strongly correlate with other measures of physical function.[23,69] Published information regarding the reliability of muscle fitness indicators in patients with CKD is extremely limited. Test re-test reproducibility, expressed as CV% for peak force and rate of force development indices during maximal voluntary isometric force production of the knee extensor (45 knee flexion angle [0 = full knee extension]), was reported to be 6.6% and 20.3%, respectively.[70] Due to a wide range of protocols used and different reported outcomes relating to various muscle groups assessed across various exercise training intervention studies, it is impossible to even attempt summarizing and commenting on responsiveness of these indices. Recommended Muscle Strength and Endurance Protocols

Dynamic strength of all major muscle groups can be assessed using the 1, 3 or 5 repitition maxiª 2010 Adis Data Information BV. All rights reserved.

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mum (RM) protocols. Participants should start with a light warm-up of five to ten repetitions with resistance that approximately corresponds to 40–60% of perceived maximum. Following 1–2 minutes of rest, some weight is added (approximately corresponding to 60–80% of perceived maximum) and participants should be asked to perform three to five repetitions. If 3–5RM is the aim, then small amounts of weight should be added after resting breaks of 1–2 minutes, until participants cannot execute more than three to five repetitions; a note of the maximal weight lifted (in kilograms) is made. If 1RM is the aim, small amounts of weight are added until patients cannot perform more than 1 repetition with the correct technique.[30,32,39,60,61,63,71] For assessing muscular endurance, a percentage of pre-defined RM is chosen (60% of 1RM and 80% of 5RM have been reported in the literature)[30,39,60,69] and the maximum number of repetitions, with emphasis on the correct technique, that patients can sustain at this level without stopping, is taken as an indication of muscle endurance. For assessing HG strength the patient should be tested in the sitting position, holding the dynamometer so that the forearm is at a right angle with the upper arm with the elbow close to the body. The dynamometer should be adjusted to fit an individual’s palm size. The patient should be instructed to squeeze the dynamometer with maximum effort and maintain the effort for 3–5 seconds. The best of two trials for the dominant or both hands should be recorded and reported in kg m s-2 (N).[64-67,71] Although, there is no evidence that exercise activities using the fistula arm may be harmful, in many countries patients are instructed to protect the arm with arterio-venous fistula by avoiding any exercise or activity. Therefore, the muscle strength of the fistula arm may be impaired. However, HG strength can be assessed on the fistula arm as long as the fistula is well healed.

4.2 Assessment of Functional Limitations

The use of objective, performance-based measures of physical function over more complicated Sports Med 2010; 40 (12)

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physiological testing or self-reports has received preferential support by many investigators in many different chronic conditions and settings.[13,72,73] In the CKD population, Mercer et al.[74] has drawn attention to research findings suggesting that simple and inexpensive measures of physical performance that reflect large muscle group mass and function may enhance the utility of established clinical tools such as nutritional status classification questionnaires. Moreover, deterioration of functional walking performance with progression of CKD has been reported[11] and physical performance tests have been used as broad indices of cardiorespiratory and muscular fitness.[74,75] Despite the great potential of simple physical performance tests for research and routine clinical use, their prognostic utility for medium and longer term outcomes has not yet been established in patients with CKD. Therefore, further research in this area is required to develop clinically meaningful criteria relevant to CKD patients for evaluation and risk stratification purposes. There have been a number of different physical performance outcomes reported in the renal exercise literature (table IV). Based on an extensive review of the data reported in controlled exercise intervention studies, we propose the following tests to be considered for future use. 4.2.1 Proposed Walking Tests North Staffordshire Royal Infirmary Walk

The proposed North Staffordshire Royal Infirmary (NSRI) walk uses a combination of tasks to assess gait speed as well as dynamic strength and balance (for instructions and testing protocol refer to Mercer et al.[74]). Gait, climb and descent speed should also be reported in metres/second (m s-1) to allow comparison across studies. This test . has been shown to significantly correlate with VO2peak in patients with CKD (r = -0.83) with a prediction error of 11%. Therefore, it seems to be a very useful overall assessment of physical performance and ability to complete ambulatory tasks often required in daily living. Reproducibility analysis has shown that an overall CV% for the North Staffordshire Royal Infirmary walk was 8.2% and, separately, for the stair climb was 11.1% and for the stair descent 11.4%.[35]


Six-Minute Walk Test

Reproducibility and validity information on the 6-minute walk test (6MWT) in patients with CKD does not currently exist but it has been used as a research outcome in renal patients (for a description and instructions on how to perform this assessment please refer to the American Thoracic Society statement.[81]). Patients receiving dialysis therapy have, on average, a maximal walking distance of 458 m (1.27 m s-1)[62-64,82] and pre-dialysis patients about 620 m in 6 minutes (1.72 m s-1).[30,76] Test-retest change in distance covered has been reported to range from 0% to 17% in other clinical populations.[81] If the 6MWT is used in follow-up evaluations, a change in walking distance beyond the range of 37–71 m has been identified as clinically meaningful in other chronic conditions.[81] Gait speed of 15 seconds, has also been identified as an important predictor of recurrent falls in the elderly population.[84,85] The clinical utility and predictive/discriminatory value of this physical performance index needs to be researched and confirmed further in the CKD population. 4.3 Assessment of Functional Disability (Self-Reported Physical Functioning)

A wide range of self- or proxy reports of physical functioning have been reported in the literature, such as the Karnofsky performance status scale, Sickness Impact Profile, Human Activity Profile, SF-36 questionnaire, walking impairment questionnaire, the 7-day PA Recall Interview questionnaire and more (for full reference lists and more details on each questionnaire please refer to Kouidi[86]). Johansen et al.[87] validated a number of different self-reported, physical function and PA recall questionnaires against objectively determined PA levels via accelerometry counts and physical performance tests, in a sample of patients receiving dialysis therapy. All the questionnaires that were used, significantly correlated with the objective measurements of PA levels and physical performance, indicating that self-report information may be used to estimate physical function and habitual PA levels. However, in order to minimize any possible influence of cognitive function, language, education, environment, etc. on selfreported data, the interview approach may also be used. The following questionnaires have been used in patients with CKD and repeatedly reported in the literature. There is still a lot of research needed to determine clinical utility and to establish scientific evaluation criteria of these selfreported methodologies for assessing physical function. The most comprehensively researched ª 2010 Adis Data Information BV. All rights reserved.

Koufaki & Kouidi

questionnaire, the physical function sub-component of which has been identified as a significant prognostic indicator of future outcomes in CKD, is the SF-36 questionnaire. Proposed questionnaires for determining selfreported physical functioning are as follows: the Human Activity Profile (HAP) [for an extensive review including use in renal patients refer to Davidson[88]]; the Medical Outcomes Study SF36 item questionnaire;[89] the Duke Activity Status Index (DASI).[90] Proposed questionnaires for estimating habitual levels of PA are as follows: the Stanford 7-day recall questionnaire (7PARQ);[91] the Physical Activity Scale for the Elderly (PASE).[92] 5. Special Considerations for Physical Function Assessment To our knowledge and based on our group’s collective experience on measuring and evaluating physical function-related indices in patients with CKD, no major adverse effects and complications, as a result of physical function assessment, have been encountered or reported in the literature. The following summarizes safety precautions as adapted from literature reports and our own practices from various European countries. These can be used as a guide to minimize safety risks and enhance standardization of physical function assessment procedures: 1. A complete list of medication regimen and doses should be obtained and reviewed before each test to ensure informed decisions are made in case of adverse medication-exercise interaction effects. For reviewing interactive effects between different medications and exercise refer to the American College of Sports Medicine’s guidelines for exercise testing and prescription.[71] Lists and doses of medications at the time of assessment, should be stated in published reports. 2. For patients receiving haemodialysis therapy, it is recommended that all physical function assessments are performed on non-dialysis days and, preferably, not immediately after a weekend, Sports Med 2010; 40 (12)


as this will normally be the longest interval without dialysis and may influence the outcome. It is advisable that all assessments are completed very close together within the same 5-day week. 3. Food and fluid consumption, and PA participation advice prior to testing should be standardized and special emphasis and advice should be given to patients with diabetes, especially, if a sustained period of exercise testing is anticipated. Table V summarizes indications of increased safety concerns during physical function testing. 4. Patients on peritoneal dialysis may find it easier to perform tests with their abdominal cavity empty of the dialyzing fluid, as this may increase pressure on the diaphragm and result in more symptoms of breathlessness and chest discomfort. However, the results may not be reflective of patients’ abilities in real life conditions, since most patients routinely have fluid in their abdominal cavity at all times, except during the

Table V. Indications for increased safety concerns for any type of physical function testing in patients with chronic kidney disease Strong indications (to avoid physical exertion)

Relative indications (to avoid physical exertion)

Hyper/hypokalaemia (>6 or 180/100 or 20 mmHg with symptoms Resting blood glucose of 10 mmol l-1

Uncontrolled diabetes mellitus Recent cerebrovascular event Acute infections Patient’s refusal In the presence of strong indications the risk of undergoing exertional physical function assessment may be high. Reevaluate when management of condition has stabilized

Patients that present with relative indications to avoid physical exertion may be assessed only after the risk/benefit ratio has been evaluated and close monitoring of vital signs is in place

The presence of qualified clinical staff is also required, especially during assessments that result in mild to severe levels of physical exertion


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exchange procedures. Moreover, testing procedures may become more complicated if drainage of fluid before and re-infusion afterward are added. 5. The arm with the arterio-venous fistula should not be used for BP monitoring, as there is a possibility that this will give erroneous readings, and may also possibly damage the fistula if attempts to obtain accurate readings are persistent. 6. It is evident from the literature that the application of many muscle performance assessment protocols is feasible and safe to execute in patients with CKD. However, extra caution still needs to be applied as these people may be more prone to muscle and tendon ruptures in response to sudden changes in forces or unusually high levels of resistance. To ensure that more representative (closer to the ‘true’ value) and consistent testing results are obtained, familiarization with the testing protocols is required. In addition, extensive whole-body- and muscle-group-specific warm-up exercise and stretches are mandated before the execution of any strength assessment protocols to minimize the risk of injuries and for enhanced performance. Moreover, emphasis should be given to proper and continuous breathing during test execution avoiding valsalva manoeuvres. 6. Discussion and Future Considerations for Research This review attempts to provide the theoretical rationale and framework for physical function assessment in patients with CKD, with the aim to move towards a more standardized and unifying approach in characterizing and evaluating functional impairment, limitations and functional disability level. In the process of reviewing and evaluating the existing physical function literature, a number of research gaps and ‘missing’ information were realized that currently, significantly limit a comprehensive synthesis of the existing evidence in order to reach a consensus on physical function guidelines. The following issues have been identified and future research efforts should aim to address these. There is limited information on the utility and clinical importance of many physical-function Sports Med 2010; 40 (12)

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outcomes in patients with CKD, especially for those tests that can be expediently and routinely administered in the clinical setting. More research is needed to establish guidance relating to what constitutes (i) an important amount of change in physical function for health-related benefits; and (ii) the amount of change that is associated with renal disease progression and overall risk progression, or is needed to modify prognosis for a specific longer term outcome. This information would be deemed essential for monitoring physical health over time, but could also be very useful in meaningfully evaluating responses to therapeutic interventions such as exercise rehabilitation. Currently, reporting of physical functionrelated outcomes is inconsistent and varies across published studies. Pooling information from different studies is therefore extremely difficult or even inappropriate. This may be partly due to the first point raised; as researchers are not fully informed/aware of which physical function assessment tools may be more informative or clinically useful. This is further complicated by the lack of recommended standardized procedures and protocols for a number of physical function assessment tools used in renal practice. The observed magnitude of physiological impairment or functional limitation may be dependent on the measurement protocol and . testing procedures employed. For example, VO2peak values measured during treadmill or cycle ergometers using ramp or step . increments may vary. VO2peak may also vary depending on the criteria that researchers employ to terminate the test and also as a result of the timing of testing in relation to dialysis treatment. Therefore, it is crucial that all investigators/renal care professionals should aim to use standardized methodological procedures for determining and evaluating physical function. For these reasons, we believe that the standardization of physical function assessment protocols and reporting of data should be an urgent priority for the renal care community. In addition, there is an extremely limited amount of information on validity, responsiveness and reliability characteristics of reported outcomes in CKD patients, and future research should focus on developing these minimum scientific evaluative criteria. ª 2010 Adis Data Information BV. All rights reserved.

Koufaki & Kouidi

Meaningful evaluation and interpretation of physical function is dependent on the (i) selection and use of valid, reliable and responsive assessment tools; (ii) appropriately trained personnel; (iii) strict application of standardized testing conditions and protocols; and (iv) existence and application of objective decision-making criteria for the characterization of physical function levels and interpretation of change over time. The most widely recommended evaluative approaches[18,93] that have also been applied to the renal population[94] include the establishment of the following: Minimum important difference: This approach is often indicated by the SEM as developed for a specific assessment tool and derived from reproducibility studies. This criterion represents the expected amount of error (technical and biological) that is associated with a measurement tool and is the least amount of change that should be expected to be seen in follow-up measurements. An amount of change that is equal or smaller than the SEM should not be considered a change at all. Therefore, the SEM represents the smallest amount of ‘meaningful’ change that can be observed; however, it does not necessarily represent a ‘clinically meaningful’ change. The latter term has been used to describe the amount of change in a measure that is linked with important patient and clinical status, relevant endpoint outcomes such as hospitalization or quality of life.[93] ‘Normality’ of physical function levels: Assessing the ‘normality’ of physical function levels has also been recommended in the literature as an acceptable way of (a) characterizing the pattern and degree of physical (dys)function; (b) evaluating the effectiveness of interventions in reducing the amount of deviation from expected normal physical functioning; and (c) evaluating physical function changes over time. The adoption of a modified version of the International Classification of Functioning, Disability and Health system[12] could help researchers standardize reporting of physical function level classification in patients with CKD. We propose that classification of functioning should be based on direct comparison (if possible) to a healthy reference group without any Sports Med 2010; 40 (12)


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Table VI. Summary of recommended objective physical function assessment tools for patients (pts) with chronic kidney disease Physical function domain

Evaluation outcomes

How to report

Comments

Report highest 30 s mean . VO2peak value; . VO2peak in mL kg-1 min-1 . VO2 at VT (mL kg-1 min-1) HR at VT (beats/min-1) Peak power in W Total exercise time in min Report speed in m min-1 and grade in % (for treadmill protocols)

Most pts terminate test because of muscle fatigue and/or lack of confidence; familiarization sessions should be provided; perform in standardized environmental conditions Physiological indices obtained at submaximal levels of exercise may more accurately reflect exercise tolerance and (motivation-free) ability to sustain physical tasks Most commonly reported indices in the literature Ease of comparability with a wide range of other chronic conditions

1, 3, 5RM Max. no. of repetitions performed at 60% of RM Max. kg achieved

Report max. kg lifted Report number of repetitions and absolute kg lifted Report in kg min s-2

Familiarization sessions should be provided Whole-body- and muscle-groupspecific warm-up sessions are required Ease of comparability with a wide range of other chronic conditions

Distance covered and gait speed Gait speed and dynamic strength/balance Time it takes to complete five or ten complete STS cycles No. of completed STS cycles in 1 min

Total distance covered in m Gait speed in m s-1 Report total time and split times for constituent elements in s Also, report total elevation height and/or number of stair steps Report in s

Familiarization sessions may be required Ease of comparability with a wide range of other chronic conditions Perform in standardized environmental conditions

Physiological impairment Exercise capacity /cardiorespiratory fitness . VO2peak . VO2@ LT/VT Exercise time achieved . Time to VO2peak Time to LT/VT Peak power output Power output at LT/VT Peak HR and BP HR and BP at LT/VT

Muscular Fitness Absolute dynamic muscle strength Dynamic muscle endurance Isometric HG strength

Functional limitations 6MWT NSRI walk STS-5 or STS-10 STS-60

6MWT = 6-minute walk test; HG = hand grip; HR = heart. rate; LT = lactate threshold; max. = maximum; NSRI = North Staffordshire Royal . Infirmary; RM = repetition maximum; STS = sit-to-stand; VO2 = oxygen uptake; VO2peak = peak oxygen uptake; VT = ventilatory threshold.

chronic conditions that are expected to have an obvious influence on health-related physical function. The reference group should be age, sex and PA matched (if we wish to accurately decompose the effects of CKD as distinct from disuse atrophy) to the patient group under investigation. This classification system can be applied to all components of physical function measurement. Patient functioning classification should also include the report ª 2010 Adis Data Information BV. All rights reserved.

of the CKD stage the patient belongs to at the time of testing. 7. Conclusions It is evident from the existing renal exercise literature that development of physical function assessment guidelines for patients with CKD is not possible due to significant gaps in the research literature. Given the limitations, a best evidence Sports Med 2010; 40 (12)

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synthesis attempt identified a number of physical function assessment tools that carry merit for future use and further research in patients with CKD. At this stage, it also seems to be of crucial importance to try and standardize assessment procedures and protocols for use in interventions that aim to influence physical function (see table VI). Acknowledgements This review is submitted on behalf of the European Association of Rehabilitation in Chronic Kidney Disease (www.renalrehab.com). Administration council nucleus members who have commended the scope and content of the current review and contributed by providing expert opinion and revisions include, in alphabetical order: Dr N. Clyne, Dr A. Daul, Professor A. Deligiannis, Dr I. Fuhrmann, Dr R. Krause, Professor T.H. Mercer and Dr P. Naish. No funding was used to assist in the preparation of this review. The authors have no conflicts of interest that are directly relevant to the content of this review.

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Correspondence: Dr Pelagia Koufaki, School of Life Sciences, John Muir Building, Sport and Exercise Science Discipline, Heriot-Watt University, Edinburgh. EH144AS, Scotland. E-mail: [email protected] and [email protected]

Sports Med 2010; 40 (12)

sports medicine Volume 40 Issue 12 December 2010

sports medicine Volume 40 Issue 10 October 2010

sports medicine Volume 40 Issue 8 August 2010

sports medicine Volume 39 Issue 12 December 2009

sports medicine Volume 38 Issue 12 December 2008

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sports medicine Volume 40 Issue 7 July 2010

sports medicine Volume 40 Issue 9 September 2010

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sports medicine Volume 40 Issue 5 May 2010

Canadian Journal of Philosophy, Volume 40, Number 4, December 2010

Behavioral and Brain Sciences, Volume 33, Issue 6, December 2010

sports medicine Volume 41 Issue 9 September 2011

sports medicine Volume 41 Issue 4 April 2011

sports medicine Volume 39 Issue 8 August 2009

sports medicine Volume 41 Issue 7 July 2011

sports medicine Volume 41 Issue 10 October 2011

sports medicine Volume 39 Issue 5 May 2009

sports medicine Volume 41 Issue 5 May 2011

sports medicine Volume 39 Issue 10 October 2009

sports medicine Volume 39 Issue 7 July 2009

sports medicine Volume 38 Issue 10 October 2008

sports medicine Volume 41 Issue 3 March 2011

sports medicine Volume 39 Issue 4 April 2009

sports medicine Volume 39 Issue 9 September 2009

sports medicine Volume 39 Issue 1 January 2008

sports medicine Volume 41 Issue 1 January 2011

sports medicine Volume 40 Issue 12 December 2010

sports medicine Volume 40 Issue 10 October 2010

sports medicine Volume 40 Issue 8 August 2010

sports medicine Volume 39 Issue 12 December 2009

sports medicine Volume 38 Issue 12 December 2008

sports medicine Volume 40 Issue 11 November 2010

sports medicine Volume 40 Issue 7 July 2010

sports medicine Volume 40 Issue 9 September 2010

sports medicine Volume 40 Issue 4 April 2010

sports medicine Volume 40 Issue 1 January 2010

sports medicine Volume 40 Issue 2 February 2010

sports medicine Volume 40 Issue 3 March 2010

sports medicine Volume 40 Issue 6 June 2010

sports medicine Volume 40 Issue 5 May 2010

Canadian Journal of Philosophy, Volume 40, Number 4, December 2010

Behavioral and Brain Sciences, Volume 33, Issue 6, December 2010

sports medicine Volume 41 Issue 9 September 2011

sports medicine Volume 41 Issue 4 April 2011

sports medicine Volume 39 Issue 8 August 2009

sports medicine Volume 41 Issue 7 July 2011

sports medicine Volume 41 Issue 10 October 2011

sports medicine Volume 39 Issue 5 May 2009

sports medicine Volume 41 Issue 5 May 2011

sports medicine Volume 39 Issue 10 October 2009

sports medicine Volume 39 Issue 7 July 2009

sports medicine Volume 38 Issue 10 October 2008

sports medicine Volume 41 Issue 3 March 2011

sports medicine Volume 39 Issue 4 April 2009

sports medicine Volume 39 Issue 9 September 2009

sports medicine Volume 39 Issue 1 January 2008

sports medicine Volume 41 Issue 1 January 2011

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