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Can muscle size fully account for strength differences between children and adults?

2011; American Physiological Society; Volume: 110; Issue: 6 Linguagem: Inglês

10.1152/japplphysiol.01333.2010

8750-7587

Antoine Bouchant, Vincent Martin, Nicola A. Maffiuletti, Sébastien Ratel,

Children's Physical and Motor Development

ViewpointCan muscle size fully account for strength differences between children and adults?Antoine Bouchant, Vincent Martin, Nicola A. Maffiuletti, and Sébastien RatelAntoine BouchantClermont Université, Université Blaise Pascal, Laboratoire de Biologie des Activités Physiques et Sportives, Clermont-Ferrand, France; and , Vincent MartinClermont Université, Université Blaise Pascal, Laboratoire de Biologie des Activités Physiques et Sportives, Clermont-Ferrand, France; and , Nicola A. MaffiulettiNeuromuscular Research Laboratory, Schulthess Clinic, Zurich, Switzerland, and Sébastien RatelClermont Université, Université Blaise Pascal, Laboratoire de Biologie des Activités Physiques et Sportives, Clermont-Ferrand, France; and Published Online:01 Jun 2011https://doi.org/10.1152/japplphysiol.01333.2010This is the final version - click for previous versionMoreSectionsPDF (41 KB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInEmailWeChat although it is self-evident that young children produce less strength than adults during maximal voluntary contractions (MVC), it still remains unclear whether these differences persist when strength is normalized to dimensional changes throughout growth, i.e., whether there are significant differences in strength relative to muscle size between children and adults. More specifically, it remains to be elucidated whether age-related changes in absolute strength are simply due to the increase in muscle size or whether they can also be ascribed to differential qualitative factors. The implication of these factors still remains a matter of debate.The more classical approach to assess the ability to produce muscle strength in vivo is to measure the torque (i.e., the product of the applied maximal muscle-tendon force and the moment arm) during isometric MVC (8, 13). During growth, the increase in MVC torque could be related to increases in both maximal muscle force and moment arm length. In that respect, it has been reported that the differences in the moment arm between children and adults could account for ∼20% of the difference of knee extension MVC torque (23). In addition, the increase in isometric strength of the ankle dorsiflexor, plantar flexor, and finger flexor muscles during growth was found to be highly correlated with the increase in the corresponding muscle volume (11, 18, 28). In these cross-sectional studies, the ability to generate maximal strength with respect to the anatomical cross-sectional area (ACSA) of the muscles remained significantly lower in children than in adults (range: ∼50–80% of adult values for children between 7 and 12), thereby suggesting that anthropometric factors on their own could not fully account for maximal strength changes during growth and maturation. Indeed, other factors such as agonist muscle activation and antagonist muscle coactivation could explain some of these changes (21). However, in contrast to the above-cited studies (11, 18, 28), the lateral gastrocnemius component of plantar flexor torque normalized to the lateral gastrocnemius ACSA was found to be similar in children and adults (17).These conflicting results could arise from the use of different methodological approaches and strength normalization procedures. As previously mentioned (7), interpretation regarding strength changes during growth and maturation could be made differently according to the scaling denominator. In that respect, the normalization of maximal strength to ACSA could be incorrect since strength is more proportional to physiological CSA (PCSA) than ACSA (17). The results of Morse et al. (17) highlight the consequences of normalizing strength to inappropriate dimensional measures: compared with PCSA, ACSA normalization causes a relatively reduced strength in children than in adults. Indeed, in pennated muscles, the difference between ACSA and PCSA becomes larger as muscle length increases (1), as is the case during growth. On that basis, the MVC-to-ACSA ratio might be systematically overestimated in adults due to their larger muscle volume. Normalizing MVC force to PCSA directly in situ could be considered as a more accurate means of quantifying specific force as long as confounding variables such as agonist muscle activation, antagonist muscle coactivation, moment arm, and joint friction are taken into account in the calculation of force (21). In studies of animal muscles, specific force was found to be similar in young and adult animals (6). This finding was recently confirmed in humans by O'Brien et al. (21), who did not observe any difference in the specific force of the quadriceps muscle between children and adults. However, this is in contradiction with the results of Morse et al. (17), who showed greater specific force of the lateral gastrocnemius muscle in children rather than in adults. Such discrepancies could be attributed to either a muscle-specific effect or whether neural factors were taken into account, or not, in the calculation of the specific force. In both of the above studies, specific force was calculated considering the activity of the antagonist muscles (coactivation), which is generally higher in children (9, 10, 12), while agonist activation was considered exclusively by O'Brien et al. (21). For the calculation of specific force, O'Brien et al. (21) estimated the maximal potential muscle force (i.e., the force produced with complete muscle activation) from linear extrapolation of the torque-activation level relation. This is consistent with the approaches adopted in animal studies where the use of electrical stimulation ensures full muscle activation (6). As many healthy humans encounter difficulties in activating muscle fully (4), it is necessary to account for any activation deficit in the calculation of the specific force. This could be particularly critical when evaluating specific force in children.No consensus has been reached regarding the neural activation capacities of children. While Belanger and McComas (3) found no difference in voluntary activation levels between pre- and postpubertal children, as estimated using the twitch interpolation technique (27), others reported lower activation scores in prepubertal children compared with their postpubertal counterparts (5) and adults (10, 21). Furthermore, it has been suggested that the effects of growth on muscle activation levels may differ as a function of sex (21), force level (10), and the muscle investigated (3, 5). Muscle length is also an essential factor to take into account when using electrical or magnetic stimulation for the assessment of voluntary activation. Indeed, tendon compliance and muscle length may have an influence on estimates of voluntary activation (16, 26). These length-dependent effects are particularly important to consider when testing young children because of their greater tendon compliance (12, 17, 22). Interestingly, Marginson and Eston (14) reported a shift of the torque-angle relationship toward longer muscle lengths in children compared with adults and attributed this finding to the lower musculotendinous stiffness of the former; however, they did not quantify activation levels in this study. O'Brien et al. (20) re-examined this relationship taking into account the activation level, but they did not report any effect of muscle length on voluntary activation level nor any difference in the torque-angle relationship between children and adults. Therefore, the influence of muscle length on voluntary activation level in children remains to be further explored. Specifically, torque and activation level should be consistently tested at a range of muscle lengths for future children-adults comparisons. Finally, maximal voluntary activation level could also be influenced by contraction type. Indeed, owing to the existence of a force-limiting mechanism (29), a lower voluntary activation level in eccentric conditions was observed in adults (2). The greater tendon compliance of children may limit the force rise during eccentric contractions, especially at high velocities, and potentially the influence of the force-limiting mechanism. Seger and Thorstensson (24, 25) investigated this possibility using surface EMG and did not find any difference between children and adults. This remains to be confirmed from direct measurements of the voluntary activation level (2). Such data are necessary to interpret the results of the studies, which normalized the power to size variables in various dynamic conditions and reported controversial differences between children and adults (15, 19).Whether the development of strength during growth is simply a matter of muscle size remains an open question. Numerous factors such as agonist and antagonist muscle activation, fascicle pennation angle and length, moment arm, and tendon stiffness should be properly measured and seriously considered in the future to ensure a fair comparison between children and adults. To date, only one study has been performed using this methodology (21), which attests of a lack of key physiological measures in this area. The authors concluded that the increased quadriceps muscle strength with maturation was not due to an increase in the specific force of the muscle but could be attributed to changes in muscle size, moment arm length, and voluntary activation level. However, although the results of this study are of potential interest, additional research is needed to ascertain whether or not the conclusions of O'Brien et al. (21) extend to other muscle groups or different mechanical conditions, such as muscle length and contraction type. Such studies will provide further insights into our scarce understanding of the effects of growth and maturation on the development of muscle strength.DISCLOSURESNo conflicts of interest, financial or otherwise, are declared by the authors.REFERENCES1. Aagaard P , Andersen JL , Dyhre-Poulsen P , Leffers AM , Wagner A , Magnusson SP , Halkjaer-Kristensen J , Simonsen EB. A mechanism for increased contractile strength of human pennate muscle in response to strength training: changes in muscle architecture. J Physiol 534: 613–623, 2001.Crossref | PubMed | ISI | Google Scholar2. Babault N , Pousson M , Ballay Y , Van Hoecke J. 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Acta Physiol Scand 140: 17–22, 1990.Crossref | PubMed | Google ScholarAUTHOR NOTESAddress for reprint requests and other correspondence: S. Ratel, Laboratory of Exercise Biology (BAPS, EA 3533), Blaise Pascal Univ., BP 104, F-63000 Clermont Ferrand (e-mail: sebastien.[email protected]fr). 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