Review article - (2007)06, 292 - 304 |
Advances in Paediatric Strength Assessment: Changing Our Perspective on Strength Development |
Mark De Ste Croix |
Key words: Strength, children, muscle size, technology |
Key Points |
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Age and sex related changes |
Most of our early understanding of the age and sex associated development in strength was restricted to physical performance tests. Field tests tend to lack measurement sensitivity and therefore we are often left with a high percentage of zero scores. As strength testing is dependent upon motivation field tests may not be sensitive enough to detect the more generalised gains in strength. A good example of this is the data presented from the National Child and Youth Fitness Study ( It is also important to bear in mind that our understanding of the development of strength with age will be influenced by the nuances of the testing procedures used, such as subject positioning, degree of practice, level of motivation, lateral dominance and level of understanding about the purpose and nature of the test. When examining data relating to changes in strength due to growth and maturation it is essential to remember that the majority of data have been derived from isometric testing. Children may not produce maximal force during isometric actions, and this has been attributed to inhibitory mechanisms that preclude children from giving a maximal effort due to a feeling of discomfort caused by the rapid development of force during isometric actions. Therefore the whole motor pool may not be activated due to a reduction in the neural drive under high tension loading conditions. In his comprehensive review Blimkie, Data from isometric actions indicate that both boys and girls strength increase in a fairly linear fashion from early childhood up until the onset of puberty in boys (around 13 y) and until about the end of the pubertal period in girls (around 15 y). The marked difference between boys and girls is caused by a strength spurt in boys throughout the pubertal period, which is not evident in girls. Girls’ strength appears to increase during puberty at a similar rate to that seen during the prepubertal phase and then appears to plateau post puberty. There is some disagreement about the age at which sex differences become evident. However, although conflicting evidence is available it is generally conceded that before the male adolescent growth spurt there are considerable overlaps in strength values between boys and girls. By the age of 16/17 y very few girls out perform boys in strength tests, with boys demonstrating 54 % more strength on average than girls. Throughout childhood and puberty, particularly in males, isometric elbow flexor and knee extensor strength are highly correlated with chronological age. Although there are some data on the age related changes in the knee extensors and flexors for children the trends affecting these muscle groups are limited. In line with isometric data most cross-sectional studies of changes in dynamic strength have demonstrated a significant increase with age. For example, increases in males and females’ absolute knee extensor (314 % and 143 %) and flexor (285 % and 131 %) strength have been noted from the ages of 9-21 y (De Ste Croix et al., Some studies have suggested that age exerts an independent effect on strength development over and above maturation and stature (Maffulli et al., Some authors have suggested that sex differences in muscle strength are evident from as early as 3 years of age. As previously mentioned there is little consensus about when sex differences in muscle strength become apparent. Some studies have shown clear sex differences by 13-14 years of age. A recent longitudinal study using multilevel modelling to control for known covariates suggested that there are no sex differences in dynamic strength up until the age of 14 y. After 14 years of age boys out perform girls in muscle strength irrespective of the muscle action examined or with body size accounted for (De Ste Croix et al., Isometric data suggests that sex differences in strength are relatively greater in muscles of the upper compared to the lower body in children. Gilliam et al., For developmental physiologists understanding the complex interaction of factors during growth and maturation that may contribute to the age and sex associated change in strength development is challenging. Historically, simple anthropometric characteristics (such as stature and body mass) have been explored as possible explanatory variables for the age and sex associated changes. As technologies have become more advanced we have the possibility to explore muscle size and moment arm using magnetic resonance imaging, muscle angle of pennation and physiological cross sectional area using ultrasonography, motor unit recruitment using electromyography, and hormonal analysis using biochemistry. Our ability to concurrently examine possible explanatory variables, using sophisticated techniques, may have changed our understanding of the contributory factors of strength development during childhood and adolescence. There are few longitudinal studies that have examined these variables concurrently using appropriate scaling methods. The following sections focus on the role played by the factors associated with the development of muscle strength. |
Influence of stature and mass |
The influence of gross body size on strength development has been examined in several studies. Stature and mass are traditionally the size variables of choice because they can be quickly and easily measured. Early longitudinal studies demonstrated that isometric strength per body mass varied only slightly during childhood and through puberty in girls. In contrast, around the time of boys’ peak height velocity (PHV), i.e. age 14 y, there was an increase in strength per body mass in boys, which was still increasing by age 18 y. Body mass has been found to be highly correlated with maximal voluntary isometric strength of elbow flexors and knee extensors in males aged 9 to 18 y (Blimkie, It is well recognised that peak strength velocity occurs about a year after PHV (11.4-12.2 y in girls and 13.4-14.4y in boys). It has been suggested that the difference in attainment of PHV and subsequent peak strength gains account for the lack of a significant sex difference in strength at 14 y. Girls will be in the phase of peak strength gains at 14y whereas boys will not have experienced the strength spurt. Three recent longitudinal studies, examining isometric and isokinetic strength respectively, have used multilevel modelling to examine the factors related to strength development. Round et al., Although simple body dimensions appear to be important in the development of strength with age only 40-70 % of the variance in strength scores of 5 to 17 y-old children could be accounted for by age, sex, stature and body mass leaving a large portion of the variance unexplained. |
Maturation and hormonal influences on strength development |
Early studies indicated that maturation, determined using Tanner’s ( An important consideration regarding the development of muscle function is the effect of endocrine adaptations typical of sexual maturation such as increased levels of testosterone ([T]) and growth hormone (GH). There is both direct and indirect evidence to demonstrate the association between [T] and strength development during puberty. [T] levels accelerate from a modest 4 fold increase during the early stages of puberty to a rapid 20 fold increase in mid-late puberty in boys (around Tanner stage 3). It is not surprising that [T] levels appear to coincide with the divergence of strength between boys and girls as circulating [T] begins to rise one year before PHV, increasing steadily and reaching adult levels about 3 years after PHV. Testosterone has been shown to stimulate anabolic processes in skeletal muscle and appears to be the principal hormone responsible for the development of strength. As previously stated, Round et al. ( Ramos et al. ( |
Measuring muscle size - magnetic resonance imaging |
It has always been assumed that the size of the muscle, in particular physiological muscle cross-sectional area (pCSA) is the most important parameter in the development of force in adults. The role that muscle CSA (mCSA) plays in the production of force in the growing child has also been extensively examined, based on the relationship between force production and strength in adults. The difficulty with paediatric subjects is the influence of other explanatory variables that relate to growth and maturation and subsequently the production of force in the growing child may not simply be prescribed to the size of the muscle. When examining studies that have explored the role that the mCSA has on strength development during growth and maturation the technique used to determine muscle size must be examined. When measuring mCSA in children for research purposes the technique used should be non-invasive with no potential side effects. Many studies with children have used anthropometric techniques to estimate mCSA because they are low cost, equipment is easily accessible and often easily portable, the measurement protocols take little time and few personnel, which is important if the number of subjects is large. Every effort should be made to ensure accuracy by standardising the technique with measurements always made by the same trained observers. This is particularly important if measurements are to be taken over time, in order to safeguard the validity and usefulness of the data. At the simplest level, coaches have been known to take circumference measurements alone to estimate mCSA but circumference measurements ignore the obvious fact that limb circumference is influenced by fat and bone cross-sections as well as muscle, such that a larger circumference need not mean a larger muscle. Efforts have been made to take into account the contribution of fatness to the circumference measurement by incorporating skinfold thickness into the equation (Jones and Pearson, The techniques described by Jones and Pearson, Radiography is a technique, which can potentially provide estimates of mCSA, but due to the radiation exposure required to produce well-defined radiographs, ethical considerations mean this technique is unsuitable for use with children. In any case, conventional radiographs depict a three-dimensional object as a two dimensional image so that overlying and underlying tissues are superimposed on the image which makes determination of mCSA difficult. Computerised Tomography (CT) overcomes this problem by scanning thin slices of the body with a narrow x-ray beam, which rotates around the body, producing an image of each slice as a cross-section of the body and showing each of the tissues in a thin slice. Unlike conventional radiography, CT can distinguish well between muscle, bone and fat. Children are particularly sensitive to radiation therefore this technique is contraindicated in children. Ikai and Fukunaga, MRI is a technique that in recent years has offered exciting opportunities for the study of gross structure and metabolism of healthy and diseased muscle. With MRI ethical constraints are avoided unlike CT and radiography. MRI can accurately measure anatomical mCSA, distinct muscle groups can be differentiated and it appears to be more suitable than other imaging techniques used for the examination of mCSA. With unparalleled picture clarity it is possible to differentiate individual muscle/muscle groups and identify both intramuscular fat and blood vessels. Despite the financial limitation numerous studies have recently used MRI with paediatric populations to determine muscle volume and mCSA (Deighan et al., |
Site of mcsa measurement |
A methodological problem with many previous studies of force or torque per mCSA with growth and maturation is that the optimal site for the measurement of maximum mCSA within and between subjects has not been clearly identified. Instead, an arbitrary location on the limb has been used for mCSA determination of mid femur in the case of thigh muscles and mid humerus in the elbow flexors and extensors. Adult data suggests that for the knee extensors 2/3 upper femur height and 1/3 lower femur height for the knee flexors should be used as the site of maximal mCSA. De Ste Croix et al., |
Age and sex associated development in mcsa |
CSA of muscle fibres reach their maximal adult size by 10 y in girls and 14 y in boys. Although muscle fibres appear to reach their maximal CSA early in childhood this does not mean that muscle has reached its maximal length as muscle will continue to grow in length simultaneously with growth in limb length segments. The Harpenden Growth study examined age and sex differences in radiographically determined upper arm and calf widths of British children from infancy to age 18 y. Boys’ muscle widths appeared greater than those of girls during childhood but the difference was small. MRI studies have also found no significant sex difference in knee and elbow mCSA up until 13 / 14 y. A large cross-sectional study using MRI demonstrated a significant age effect in elbow mCSA up until 24 y (Deighan et al., According to Blimkie, There are considerable data that support the contention that differences in muscle size account for differences in muscle strength during growth. One of the earliest studies examined the relationship between isometric elbow flexion strength and mCSA determined by ultrasonography in 12 to 29 y-old (Ikai and Fukunaga, |
Age differences in strength per mcsa |
There is still some debate about whether strength per mCSA increases with age. Early studies demonstrated increasing strength per mCSA from age 7 to 13 y. Also, |
Sex differences in strength per mCSA |
Debate surrounds whether sex differences exist in strength per mCSA. Early work reported that absolute isometric strength differences between sexes disappeared when data were normalised to anthropometric muscle (plus bone) CSA in 9-12 y old. Sunnegardh et al., For example, the peak gain in muscle strength in boys occurs more often after peak stature and mCSA velocity but there is no such trend for girls. Therefore, particularly in boys there may be factors other than mCSA that affect strength expression during puberty. Also, it has been shown that the sex differences that occur in strength of boys and girls of the same stature cannot be accounted for by muscle size alone. A longitudinal study of upper arm area and elbow flexor strength have shown that boys have muscles ~5 % greater in area but which produce ~12 % more strength. Others have indicated that mCSA is a non-significant explanatory variable once stature and mass are accounted for (De Ste Croix et al., Peak muscle mass velocity has also been shown to occur at an average of 14.3 y, whereas peak strength velocity appeared at age 14.7 y. This supports the view that muscle tissue increases first in mass, then in functional strength. Consequently, this would seem to suggest a qualitative change in muscle tissue as puberty progresses and perhaps a neuromuscular maturation affecting the volitional demonstration of strength. |
Biomechanical factors - the muscle moment arm |
The mechanical advantage of the musculoskeletal system is variable across different muscle groups and is considered unfavourable because the measured force or torque is somewhat smaller than the corresponding tension developed in the muscle tendon. Another unfavourable biomechanical influence on the measured force lies in the internal muscle architecture, i.e. the greater the angle of pennation to the long axis of the muscle, the smaller proportion of force in the muscle fibres that is transmitted to the muscle tendon. The age-associated relationships between these factors have not yet been extensively investigated in children. It is probable that small differences between subjects in the location of the centre of rotation of the joint or in the length of the lower limb could contribute to the observed variability in the ratio of muscle strength to mCSA. It is difficult to account for biomechanical factors but some authors have divided strength values by the product of mCSA and stature (Nm·cm-3), i.e. the product of mCSA and possible differences in moment arm length or mechanical advantage which they assumed to be proportional to stature. There are few published data on the relationship between strength per mCSA and mechanical advantage covering different age groups, both sexes and different muscle groups but it seems sensible to correct strength for possible differences in mechanical advantage, especially if comparing children of different sizes by normalising to mCSA*limb length (LL) (Blimkie and Macauley, Numerous authors have demonstrated a moderately strong, positive correlations between stature and isometric torque per mCSA for the elbow flexors (r = 0.67) and knee extensors (r = 0.57); isokinetic knee extensors (r = 0.85) and flexors (r = 0.84); and isokinetic elbow extensors (r = 0.79) and flexors (r = 0.80) (Deighan et al., Blimkie, Early work indicated that sex differences in absolute torque remain statistically significant, although diminished, when expressed per unit mCSA*thigh length. Kanehisa et al., There has been speculation that the angle of muscle pennation plays a role in the group differences in strength per mCSA (Blimkie, |
Neuromuscular factors and strength development |
Investigation into the ‘quality’ of children’s muscle is sparse due to the methodological issues of determining neuromuscular function. Measured voluntary strength depends highly on the degree of percentage motor unit activation (%MUA). Both the level of voluntary neural drive or motor unit recruitment and the level of activation or frequency of stimulation govern %MUA. The ideal way to measure the contractile capacity of a muscle is to record the force developed during supramaximal electrical stimulation of the nerve innervating the muscle. When an electrical stimulus is applied to a motor nerve near the muscle, the resultant muscle force is free of any inhibitory influence from above the point of stimulation. On the other hand, force or torque measured during a voluntary action is the result of neuromuscular influences from the brain and inhibitory reflex influences from the spinal cord in addition to the maximum force producing capacity of the muscle. The results of tetanic electrical stimulation may not be comparable to voluntary muscle actions, since in the former method synergistic muscles may not be excited and the procedure is very painful leading to methodological, compliance and ethical issues in children. Due to these problems with tetanic stimuli of children’s muscles, most studies that have investigated maximum force producing capacity in children have used twitch stimuli because various properties of an electrically evoked twitch reveal information about intrinsic muscle properties and %MUA. Assuming that %MUA stays constant with age, then the ratio of evoked twitch force to voluntary force should stay constant with age. Based on this assumption, Davies, The interpolated twitch technique (ITT) has been used to provide an answer to the painful tetanic stimuli method and to allow %MUA to be calculated more directly. Blimkie, In adults a sex difference has been demonstrated in the rate of force development which is an important quality for dynamic muscle actions in which there is limited time to generate force. Recent data examining isokinetic time to reach peak torque suggests that there are non-significant sex differences in the knee and elbow extensor and flexor muscles (Barber-Westin et al., Time to peak twitch torque and twitch relaxation indices can be used as measure of rate of energy turnover and fibre type composition. Backman and Henriksson, |
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There is still a clear need for further longitudinal investigation into the static and dynamic development of muscle strength through childhood and adolescence into adulthood. Our major difficulty in describing the age and sex associated development in strength is that much of the current data reveal muscle group and muscle action specific differences in the relationships described. For example, the factors responsible for the development of isokinetic eccentric elbow flexion may be different from isometric knee extension. Despite this, the age-associated development of strength is reasonably consistent, irrespective of the muscle group or action examined. There is slight disagreement about when sex differences occur. Importantly, many of the factors discussed in this chapter play a role in strength development when examined as independent variables. It would appear that for dynamic muscle actions in particular that mechanical factors may play a large role in the development of muscle torque and accurate investigation of the muscle moment arm, employing MRI techniques, would provide us with a clearer picture of the age and sex associated development. Our greatest challenge is to elucidate the factors that contribute to the age and sex associated development in strength concurrently with other known explanatory variables. |
Future directions in paediatric strength assessment |
Despite the growing number of longitudinal design research papers on the development of strength, and the use of differing methods to control for differences in body size, there are still unexplained factors that may contribute to the age and sex associated development in strength. We know relatively little about muscle fibre types in children, probably due to the invasive nature of muscle biopsies and the associated ethics that preclude the use of such techniques with paediatric subjects. There has been some tentative exploration into the use of MRI to determine fibre type (Houmard et al., There is no doubt that development in techniques to measure muscle forces (eg isokinetic dynamometers), muscle size (MRI) and newer techniques for controlling for differences in body size (allometric scaling and multilevel modelling) have contributed to our greater understanding of the age and sex associated development in strength. However, there is still much we do not know and continuing advances and access to sophisticated technologies e.g. DEXA, MRI, ultrasonography, may elucidate new thoughts in this area over the coming decade. |
Historical assessment of strength |
Early studies of strength development in paediatric subjects were primarily limited to field based tests such as number of sit ups/press ups in 1 minute or timed flexed or straight arm hang (Wilmore and Costill, |
Methodological considerations in paediatric strength testing |
Paediatric subjects provide the physiologist with added challenges relating to varying rates of growth and maturation, and subsequently most testing methods and equipment have been devised with adult testing in mind. There has been an increased awareness amongst paediatric physiologists that most commercially available equipment needs adapting for meaningful data to be obtained. Some of our early understanding of the age and sex associated changes in strength may have been clouded by use of inappropriate equipment and protocols. Choice of testing protocols with paediatric populations may be influenced by subjects, test equipment availability, cost and specificity of testing. Previous authors have suggested that the key issues relating to testing protocols should include the muscle group to be tested, joint angle, type of muscle action, velocity of muscle action and movement pattern (Blimkie, Other specific methodological issues of paediatric strength testing and reliability data have been covered in detail elsewhere (De Ste Croix et al., |
Reliability of strength testing |
In order for any strength measurement to be used as an objective and accurate measure of maximum strength it must be documented to be a reliable measurement tool. Poor reliability may lead to erroneous conclusions about the strength parameter being measured. Experimental error can be minimised effectively by standardisation of test protocols that will provide greater sensitivity to detect biological sources of variation in a child’s ability to exert maximum muscular effort. An habituation period is critical for paediatric strength testing as this essential period of learning facilitates a phase in which the specific movements, neuromuscular patterns and demands of the test become familiar to the individual. Previous studies (Deighan et al., It is difficult to compare results across studies as different statistical methods, many of which are questionable, have been used to assess reliability that is also protocol, measured parameter and dynamometer specific. However, the available literature currently supports the reliability of strength testing with children but suggests that extension movements are more reliable than flexion movements and that concentric actions are more reliable than eccentric actions. |
Eccentric testing in paediatric populations |
Eccentric actions occur in everyday life as often as concentric actions. For example, the knee extensors play a significant role in shock absorption during walking, running and jumping and the knee flexors play the role of a ‘brake’ as the knee extends during walking, kicking and running. The characteristics and control mechanisms of these two actions are very different, therefore the assessment of both types of action is essential for a complete understanding of strength development. It is possible that the limited information on eccentric strength capabilities of children may be due to the concern that eccentric testing with its potential for high muscle force production might predispose children to higher risk of muscle injury or delayed onset of muscle soreness. However, there is no reason to expect greater muscle injury with eccentric actions in children compared to adults or other forms of muscle testing, provided they are given sufficient warm-up and familiarisation (Blimkie and Macauley, |
Eccentric/concentric ratio and knee stability |
Conventionally, the hamstring/quadriceps ratio is calculated by dividing the torque of knee extensors and flexors at identical angular velocity and contraction mode. However, previous authors have suggested that to evaluate muscular balance of the knee the eccentric/concentric actions of the knee flexors (KF) and knee extensors (KE) should be examined (ECCKF/CONKE or CONKF/ECCKE ratio) and referred to as a functional ratio rather than the conventional ratios often used (ECCKF/CONKF or ECCKE/CONKE ratio) (Aagaard et al., As dictated by the force-velocity relationship, the ECC/CON ratio will increase as angular velocity increases (Colliander and Tesch, Dvir, It has been suggested that sex differences in adults in the conventional ECC/CON ratio of the knee joint are due to differences in percentage motor unit activation (%MUA) during maximal voluntary actions, with women having a lower %MUA than men during CON actions, (Griffin et al., |
Statistical analysis - the influence of adjusting for body size on strength development |
It has become common in the literature to express strength in absolute terms, with isometric data expressed in newton (N) and isokinetic data expressed in newton metre (Nm). In the study of muscle strength with growth and maturation, comparisons are made between individuals of different sizes. It is therefore important that a size-free strength variable is used for interpretive purposes. From a strength perspective the key issue to be addressed when scaling for body size differences are the body size variable with which to scale the performance variable and the method to be employed. For a detailed review of adjusting for body size on strength variables the reader is directed to a paper by Jaric, The most commonly used technique in the strength literature to partition out differences in size is the ratio standard with body mass as the most widely used denominator. However, stature and fat-free mass have also featured as covariates. Others have used allometric scaling techniques to examine the theory that muscle cross-sectional area and strength are a function of second power of height. The b exponents identified in the study of Kanehisa et al., Three longitudinal studies have used multilevel modelling to examine a number of known covariates to determine their influence on the age and sex associated changes in muscle strength (De Ste Croix et al., |
Age and sex associated changes in strength: a historical perspective |
It is clear that many factors interact to produce the expression of strength. Awareness of the anthropometric, neurologic, hormonal, age and sex -associated changes in skeletal muscle strength is important from childhood to adulthood. While there is abundant literature focussing on determinants of strength development, few studies have used common age ranges, muscle groups, testing protocols and muscle actions, making comparisons difficult. Most early strength development studies examined isometric forces generated from handgrip data. It has been suggested that strength measured as isometric or dynamic force reflects the same relative strength between individuals regardless of the type of test method (Froberg and Lammert, Isokinetic assessment has primarily been recommended for strength testing as maximal force is applied during all phases of the movement at a constant velocity (Stocker et al., |
AUTHOR BIOGRAPHY |
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