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J Appl Physiol 104: 469-474, 2008. First published December 20, 2007; doi:10.1152/japplphysiol.00697.2007
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Gastrocnemius muscle specific force in boys and men

Christopher I. Morse, Keith Tolfrey, Jeanette M. Thom, Vasilios Vassilopoulos, Constantinos N. Maganaris, and Marco V. Narici

Institute for Biophysical and Clinical Research into Human Movement and Health (IRM), Manchester Metropolitan University, Alsager, Cheshire, United Kingdom

Submitted 29 June 2007 ; accepted in final form 10 December 2007


   ABSTRACT
TOP
 ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 
The aim of this study was to assess whether the in vivo specific force and architectural characteristics of the lateral gastrocnemius (GL) muscle of early pubescent boys (n = 11, age = 10.9 ± 0.3 yr, Tanner stage 2) differed from those of adult men (n = 12, age = 25.3 ± 4.4 yr). Plantarflexor torque was 55% lower in the boys (77.4 ± 21.4 N·m) compared with the adults (175.6 ± 31.7 N·m, P < 0.01). Physiological cross-sectional area (PCSA), determined in vivo using ultrasonography and MRI, was 52% smaller in the boys (P < 0.01). No difference was found in pennation angle, or in the ratio of fascicle length (Lf) to muscle length between the boys and men. Moment arm length was 25% smaller in the boys (P < 0.01). Antagonist coactivation, assessed using surface EMG on the dorsiflexors, was not different between the boys and men (11.8 ± 6.7% and 13.5 ± 5.8%, respectively). Surprisingly, GL force normalized to PCSA (specific force) was significantly higher (21%) in the boys than in the men (13.1 ± 2.0 vs. 15.9 ± 2.7 N/cm2, P < 0.05). This finding could not be explained by differences in moment arm length, muscle activation, or architecture, and other factors, such as tendinous characteristics and/or changes in moment arm length with contraction, may be held responsible. These observations warrant further investigation.

pennation angle; fascicle length; muscle architecture

MUSCLE STRENGTH is largely determined by muscle size (7). Throughout adolescence both muscle strength and muscle size increase but with different rates because greater gains seen in muscle strength compared with muscle size are observed (20). It is therefore important, when comparing strength between children and adults, to scale strength to muscle size. Cross-sectional comparisons between prepubescent children and adults show knee extensor maximum voluntary contraction (MVC) torque normalized to quadriceps anatomic cross-sectional area (ACSA) to be higher in adults than in children (18, 20), a finding that has also been reported for grip strength and forearm muscle ACSA (37).

Although ACSA is an appropriate scaling factor for muscle strength in a parallel fibered muscle (2), it cannot fully account for the entire contractile mass in a pennate muscle (13). Accordingly, the correlation between ACSA and strength is often low in pennate muscles such as the knee extensors [R2 = 0.38 (31)]. In contrast to ACSA, the physiological cross-sectional area [PCSA; the ratio of muscle volume to fiber fascicle length (Lf)] includes all sarcomeres in parallel and is thus the main determinant of pennate muscle force (7).

Early studies by Goldspink (12) showed that muscle growth during development is mainly dictated by the elongation of bones. In humans, it can be expected that the same is true up to the onset of pubertal age, at which point a rapid increase in muscle mass and strength occurs due to the secretion of sex hormones (41). Hence the hypothesis may be put forward that in humans the increase in muscle mass during prepubertal development, because mainly driven by bone elongation, involves a greater addition of sarcomeres in series than in parallel, whereas with pubescence, muscle growth becomes mainly dictated by the addition of sarcomeres in parallel. However, little is known as to whether the proportionality between the increases in muscle mass (and thus volume, since muscle density is 1.05 g/cm3) and fiber length is constant during development. In addition, there is presently a paucity of data for which to compare volume and fiber length, and hence PCSA, in children.

In vivo, PCSA is not the only determinant of muscle specific force (fascicle force/PCSA) since this is also dependent on moment arm length, agonist muscle activation, and antagonist muscle coactivation (28). The importance of moment arm length on the transmission of force in children has been previously described for the jaw muscles, and although it was shown that those children with larger moment arms require less activity to produce a given force (11), moment arm measurements do not appear to have been included in the calculation of normalized strength in children (18–20, 37). Therefore, the aim of the present study was 1) to establish whether, after accounting for neural drive, muscle mass, anatomic levers, and muscle architecture, differences existed between muscle specific force of early pubescent boys and that of young adults; and 2) to provide unique in vivo data on muscle structure and function in early pubertal males.

On the basis of previous studies reporting differences in normalized joint torque between adults and children, it was hypothesized that gastrocnemius lateralis specific force would differ between the boys and men.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Participants.   Eleven boys at the second stage of secondary sexual characteristic development (43) (age 10.9 ± 0.3 yr, stature 1.45 ± 0.03 m, mass 38.3 ± 8.0 kg) and 12 adult males (age 25.3 ± 4.4 yr, stature 1.76 ± 0.08 m, mass 79.1 ± 11.9 kg) volunteered to participate in this study. All participants were physically active but not participating in a structured training regime. All procedures were approved by the Manchester Metropolitan University Ethics Committee, and prior informed consent was obtained from each participant. Parental consent was provided for all of the boys.

For inclusion in the study, jointly self-assessed (by parent and child) sexual maturity status was no more than 2 (43). Therefore, the boys were a mixture of pre- and early-pubertal status. Drawings (32) of the five stages of genital and pubic hair development described by Tanner (43) were given to the parent and participant for the self-assessment. The parents were asked to assist the boys with this assessment by 1) discussing the schematic illustrations with them and 2) comparing their son's genital and pubic hair development with the schematics and accompanying written descriptions. Acceptable reliability and validity of the self-assessment method have been reported previously (32).

Familiarization.   Participants were familiarized to all proceedings on a separate session before data collection. Familiarization sessions consisted of repeated MVCs at the joint angle required for force measurements (both plantarflexion and dorsiflexion).

Strength.   Isometric plantarflexor MVC torque was recorded with the participants laying prone and the left foot secured to the foot adapter of an isokinetic dynamometer (Cybex Norm, Cybex International). Straps were used about the hips to prevent forward displacement of the body during maximal plantarflexions. Participants were positioned with the knee at full extension and the lateral malleolus aligned with the axis of rotation identified on the dynamometer. Before MVC the participants performed three submaximal isokinetic plantarflexions and dorsiflexions as a warm up. Two isometric maximal voluntary plantarflexions (MVC) were performed at an ankle joint angle of –20° (the foot in dorsiflexion); 2 min separated each MVC attempt. The foot was placed at –20° as this has been shown previously to correspond to the optimum fascicle length within the physiological range of the gastrocnemius muscle (26). To ensure MVC was achieved, visual feedback was provided using an online graphical display, and consistent verbal encouragement was provided by the investigator. Maximal isometric dorsiflexions were performed after the plantarflexion MVC to obtain maximal dorsiflexor electromyographic (EMG) data for calculation of antagonist coactivation in the tibialis anterior.

Coactivation.   EMG activity of the tibialis anterior was recorded while performing maximal isometric plantarflexions and dorsiflexions using two Ag-AgCl percutaneous unipolar electrodes 10 mm in diameter (Neuroline, Medicotest, Rugmarken, Denmark). Electrodes were set in a bipolar configuration with a 20-mm interelectrode distance at one-third of muscle length to avoid the motor point (46). Muscle boundaries were identified using ultrasonography to reduce the influence of cross talk, and the electrodes were placed along the midsagittal plane of the muscle. A reference electrode was placed on the lateral femoral condyle. Before placement of the electrodes, the skin was shaved to remove hair, and the recording sites were rubbed lightly using abrasive gel and cleansed using alcohol swabs to reduce interelectrode impedance below 5 k{Omega}. The raw EMG activity was acquired with a sampling frequency of 2,000 Hz and processed with a multichannel analog-to-digital converter (Biopac Systems, Santa Barbara, CA). The raw EMG signal was filtered with low and high band-pass filters set at 500 and 10 Hz, respectively, and amplified with a gain of 2,000. The level of coactivation of the tibialis anterior was assessed using the root mean square (RMS) of the raw EMG signal, which was integrated over 1 s about the peak MVC torque during PF; this was then expressed as the percentage EMG activity recorded from the tibialis anterior during maximal dorsiflexion (21, 23, 24). Torque produced by the dorsiflexors during plantarflexion was estimated assuming a linear relation between torque and EMG activity, which has previously been reported from the tibialis anterior muscle (29). To obtain an estimate of plantarflexion peak torque, dorsiflexion torque during plantarflexion was added to the net MVC plantarflexion torque.

Muscle volume.   Serial axial plane MRI scans were acquired along the length of the lateral head of the gastrocnemius muscle (GL) using a fixed 0.2-T MRI scanner (E-Scan, ESAOTE Biomedica, Genoa, Italy). The first scan was centered at the lower edge of the patella and was sufficient to include the origin of the GL; subsequent scans were carried out in contiguous 7-cm sections distally until the myotendinous junction of the GL had been included (Fig. 1). Axial plane scans were obtained using a T1-weighted three-dimensional isotropic profile with the following scanning parameters: time to echo, 16 ms; repetition time, 38 ms; field of view, 180 mm x 180 mm; matrix, 256 x 192. Participants were supine for 15 min before the scan to allow fluid shifts to occur (4). In total, four scans were performed along the length of the GL, consisting of seven contiguous axial slices (slice thickness = 8 mm; gap = 2 mm). To ensure that each section was reconstructed accurately, reference markers were placed along the leg to coincide with each 7-cm section. These markers were placed on the skin, along the tibia at a distance relative to the proximal end of the patella (identified using ultrasound with the subject in a supine position). The ACSA of the GL muscle was measured from each scan using digitizing software and imaging software (NIH image version 1.61/ppc, National Institutes of Health, Bethesda). ACSA (excluding visible fat and connective tissue) was then multiplied by the slice thickness (inclusive of gap) to give an estimate of muscle volume (Vol). The accuracy of this technique has been reported previously (22, 35).


Figure 1
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  		Fig. 1. Representative transverse MRI scans from an adult man (A) and a boy (B) at approximately midtibia length. The soleus (S) and the medial and lateral heads of the gastrocnemius (GM and GL, respectively) are labeled. Muscle volume of the GL was estimated by summing the cross-sectional area of scans taken along the entire length of the GL. Each cross section was separated by a scan interval of 1 cm. From these scans, in vivo physiological cross-sectional area (PCSA) was calculated as volume/fascicle length.

 
Muscle architecture.   The participants laid prone, with the foot secured at –20° dorsiflexion. Fiber fascicle length (Lf) and pennation angle ({theta}) were measured using B-Mode, real-time ultrasonography (HDI-3000, ATL, Bothell, USA), at the time point of MVC. Images were obtained along the midsagittal plane of the GL (Fig. 2), at the mid-distance between the proximal and distal tendon insertion identified by ultrasound (7.5-MHz linear-array probe). The head of the probe was held perpendicular to the dermal surface to provide an image including both superficial and deep aponeuroses, and a number of clearly visible fasciculi that could be followed between the aponeuroses. To improve acoustic coupling, water-soluble transmission gel was placed over the scan head. Ultrasound scans were recorded on VHS at 25 Hz, digitized on an Apple Macintosh G4 computer, and analyzed offline with digitizing software. Pennation angle was measured as the angle of fascicular insertion into the deep aponeurosis (44). Fascicle length Lf was defined as the length of the fascicle between the deep and superficial aponeuroses (36). PCSA (cm2) was calculated as the ratio of GL Vol (cm3) to Lf (cm). To ensure measurements of Lf and {theta} were measured at the time point of MVC, the VHS and torque recordings were synchronized. Accuracy of the ultrasound method for determining muscle architectural features has been validated previously by comparison with direct anatomic measurement on cadavers (36). One limitation of the ultrasound technique is that no information can be obtained outside of the two-dimensional orientation in which the ultrasound probe is placed. Therefore, care was taken to ensure that the orientation of the ultrasound probe coincided as much as possible with that of the muscle fascicle orientation. In fact, when the probe is aligned along the same sagittal axis of the fascicles, the entire length of the fascicles in the central portion of the image can be tracked from the deep to the superficial aponeurosis.


Figure 2
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  		Fig. 2. Sample sagittal plane sonographs, obtained during maximum voluntary contraction, for the determination of PCSA and specific force in the gastrocnemius of an adult man (A) and a boy (B).

 
Moment arm length.   MRI was used to determine moment arm length of the Achilles tendon at rest. Two sagittal plane scans were taken of the left ankle with the foot secured at –20° dorsiflexion and 20° plantarflexion. From these images an average moment arm length between the two angles of measurement was calculated according to the tendon excursion method described previously (30). Briefly, the two corresponding images were digitally overlaid from each of the scanning angles so that the talus bone from each image was aligned (OsiriX medical imaging software, OsiriX, Atlanta, GA). The center line of the tibias from each image was identified, and the angle made by the two overlaying tibia images was then recorded. On the same two images, the tibias were then aligned, and the circumferential displacement of the calcaneous was measured. The moment arm length (MA) was estimated as MA (m) = tibial angle (rad)/calcaneal displacement (m).

As the tendon excursion method provides an average MA length between the measured ankle joint angles of –20° and 20°, to obtain MA values at –20° (the joint angle at which all other measurements were made), an extrapolation of the MA was made based on the moment arm length joint angle relationship provided by Maganaris (26).

Achilles tendon force.   Tendon force was calculated by dividing the net plantarflexion torque (N·m) by the Achilles tendon moment arm length (m).

GL fascicle force.   To estimate the contribution of the GL to Achilles tendon force, the relative PCSA of the GL within the triceps surae was calculated. Previously, relative PCSA of the quadriceps muscle group has been used to determine the relative contribution of each constituent muscle to the production patella tendon force (35). Using a similar technique, it was possible to isolate the GL component of Achilles tendon force, by attributing the tendon force to the relative PCSA of the GL within the plantarflexor group. We have determined previously that the GL constitutes 11% of the triceps surae PCSA (33), and the triceps surae group was estimated to occupy 91% of the plantarflexor PCSA (45). Once the GL component of the tendon force was calculated, this was divided by the cosine of the pennation angle {theta} measured during contraction to determine the fascicle force, Ff.

Specific force.   Specific force was calculated by dividing GL fascicle force by the PCSA. To compare our data with others, the GL component of plantarflexor torque was normalized to GL ACSA (MVC/ACSA). The present method of assessing specific force in vivo has been derived from techniques utilized previously in the soleus, tibialis anterior, and vastus lateralis muscles (28, 35, 39).

Statistics.   Differences between groups were assessed using independent samples Student's t-tests. Distribution was assessed using the Shapiro-Wilk test, and homogeneity of variance was assessed using the Levene test. The level of significance was set at the 5% level. Results are presented as means ± SD.


   RESULTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Strength and antagonist coactivation.   Net plantarflexion and dorsiflexion MVC torques were significantly lower in the boys compared with the men by 56% and 46%, respectively (both P < 0.01, Table 1). Coactivation of the dorsiflexors during plantarflexion was no different between the boys and men (Table 1). Compared with the adult males, plantarflexion peak torque was 55% lower in the children (P < 0.01); correspondingly, Achilles tendon force and GL fascicle force were both smaller in the boys by 41% (P < 0.01).


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  		Table 1. In vivo joint moment and architectural characteristics of the lateral gastrocnemius muscle of boys and men

 
Muscle size and specific force.   As expected, given their smaller stature, GL Vol was 64% smaller in the boys (P < 0.05, Table 1). Lf was smaller in the boys by 24% during MVC (P < 0.05, Table 1). Although resting Lf was 20% smaller in the boys (P < 0.01), the ratio of resting Lf to muscle length was not different between the two age groups. Despite a tendency for pennation at MVC to be smaller (8%) in the boys than in the men, differences were not significant. Moment arm length was smaller in the boys by 25% (P < 0.01, Table 1). ACSA was 53% smaller in the boys compared with the men (P < 0.01), and Vol was 63% smaller (P < 0.01, Table 1). PCSA in the boys was 52% smaller than the men. MVC torque/ACSA was not significantly different between the boys and men. GL specific force was 21% higher in the boys than in the men (P < 0.05, Table 1). Due to the fact that tendon elongation was not recorded, inferences were made based on the proximal displacement of the aponeurosis (10), estimated as the difference in cos {theta} x Lf from rest to MVC. In absolute terms, fascicular shortening from rest to MVC of 2.8 cm and 3.3 cm was not significantly different between boys and men, respectively. However, when normalized to MVC force, displacement of the aponeurosis was 0.0123 ± 0.003 cm/N in the boys and 0.0081 ± 0.003 cm/N in the men (P < 0.01).


   DISCUSSION
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
ACKNOWLEDGMENTS
 REFERENCES
 
To our knowledge, this is the first study investigating muscle architecture and specific force in vivo in early pubescent boys. Moreover, the data were collected under identical experimental conditions in the boys and men, rather than using a retrospective comparison. Of particular significance was the finding that specific force in the GL was higher in boys compared with young men. This finding is unexpected when considering data from animal muscle that show either an increase in single fiber specific tension with development (40) or no difference with respect to adult muscle (6). Assuming that the same is true for human developing muscle, then any differences in specific force measured in vivo ought to be searched for elsewhere. The following sections will thus discuss the potential contribution of methodological, allometric, biomechanical, neural, architectural, and tendinous factors to the differences in specific force between juvenile and adult males observed in the present study.

Muscle size, and normalized force.   Consistent with previous studies on the knee extensors and handgrip muscles (18, 37), muscle size and absolute strength were smaller in the boys compared with the men in the present study. However, the difference in both size and strength between the boys and men varied according to the method of assessment; compared with the men, GL ACSA was 53% smaller, Vol was 64% smaller, and PCSA was 52% smaller in the boys. Similarly, plantarflexor MVC torque was 56% smaller in the boys compared with the men, whereas GL force was 42% smaller.

In agreement with previous studies that have reported normalized joint torque as MVC/ACSA for the triceps surae throughout adolescence (15), when MVC was normalized to ACSA, we observed no significant difference in strength between the men and boys. In contrast, specific force (Ff/PCSA) was significantly higher in the boys than in the men. The influence of the scaling denominator has been mentioned previously (8) and may explain the contrasting results between the different scaling factors used in the present investigation. First, the normalization of strength to muscle ACSA is not only incorrect, since force is strictly proportional to PCSA and not ACSA, but is also likely to be insensitive to stature differences between the boys and men since limb length may develop at a greater rate than ACSA during prepubertal growth (20). Indeed, in the present investigation, when ACSA was expressed relative to limb length, values are significantly lower in the boys than in the men. Therefore, differences in ACSA between the boys and men may not be representative of differences in muscle volume, as it only reflects a small portion of the muscle. Second, ACSA by definition represents the fiber area at right angles to the longitudinal axis of the muscle. Because of the pennation angle of the GL, a single cross section would underestimate the fiber area contributing to torque and lead to an overestimation of MVC/ACSA. Because pennation angle is greater in the men, ACSA represents a lower proportion of the fiber area in the men than in the children; this is evidenced by a low correlation between PCSA and ACSA in the men (R2 = 0.33), with higher values observed in the boys (R2 = 0.56). In relative terms, therefore, because ACSA represents less of the fiber area in the men compared with the boys, the difference in normalized strength presented as MVC/ACSA, as opposed to Ff/PCSA, would be less between the two groups when the latter is used.

Possible causes of higher specific force in boys.   Pennation angle was smaller in the boys compared with the adults during contraction, and their relative moment arm length was also smaller. The calculation of specific force (where volume and fascicle length are considered) is influenced both by the cosine of the angle of pennation and the moment arm length. However, in the present investigation, pennation angle during contraction was 21% smaller in the boys than in the men. If fascicle force and other architectural parameters are equal, this 21% smaller pennation angle affords only a 3% advantage in tendon force in the boys compared with the men (since tendon force = fascicle force·cos {theta}); therefore it cannot represent a main cause for the greater specific force in the boys.

Compared with the men, the boys in the present study demonstrated no difference in the level of antagonist coactivation of the dorsiflexors; hence this factor cannot possibly account for the observed difference in specific force. In the present investigation, agonist activation was not measured as the electrical stimulation required used in the twitch interpolation technique would have caused unnecessary discomfort to the boys. Previously, motor unit activation has been shown to be reduced in the knee extensors of children (38, 42), whereas the men who volunteered for the present study have been shown previously to have complete motor unit activation in the plantarflexors (34). In the present study, visual feedback of plantarflexion MVC torque and familiarization were given to the boys to increase the likelihood that activation was as high as possible. Most of all, had activation been reduced in the boys, the resulting specific force should have been lower and not higher in the boys. Hence the hypothesis of a lower activation must be ruled out as a possible cause for the higher specific force in the boys.

In the present study we made the assumption that the relative PCSA of the GL in the boys was the same as the men. This assumption, necessary for estimating the force of the GL acting along the tendon, seemed reasonable since both the ratio of GL Vol to total triceps surae Vol (19.6% in the adults and 18.0% in the boys) and the fascicle length to muscle length ratio (Lf/Lm) of the boys were very similar to those of the men. As PCSA is calculated as Vol/Lf, the higher specific force in the boys is unlikely to be due to an overestimation of the relative PCSA of the GL within the triceps surae. Furthermore, in addition to the triceps surae, there are five further plantarflexors. In the present investigation we have based our allocation of tendon force on previous data from adults, and it should be noted that presently there is no descriptive data available from children from which to confirm this assumption.

The allocation of tendon force based on relative PCSA is an established technique in adults (28) and relies on previous evidence that the gastrocnemius and soleus occupy similar portions of the length-tension relation [mainly on the ascending limb (14, 25, 26)]. We have assumed that the muscles of the boys and men operate over a similar region of the length tension relation as there is no published data available, but it may be the case that the muscles of the boys operate over a different portion of the length-tension relation. If, for example, the gastrocnemius muscle operates closer to the plateau region, this could contribute to the observation of a higher specific force in the present study. If it will be established in the future that the length-tension relation of children is different from that of adults, measurements of specific force should be taken at different ankle angles in the two age groups and not at the same joint angles.

Consistent with previous studies (16), when measured from rest to MVC, fascicle length decreased by 36% in men and 40% in boys regardless of the greater absolute forces generated by the men. Considering the compliant nature of tendons and the associated curvilinear shortening of the muscle fascicles with increasing force (16), it would be expected that the lower force produced by the boys would occur as a result of lesser fiber shortening. However, this was not the case, as the lower fascicle force resulted in the same relative fascicle shortening in the men and boys. It is possible that this was due to a greater tendon extensibility in the boys due to a smaller tendon CSA (17) and/or to different tendon properties. This is relevant in the present investigation because the gastrocnemius is a muscle that functions on the ascending limb of the length-tension relationship (14). Therefore the similar relative shortening in the boys compared with the men, regardless of lower contractile forces, may enable the sarcomeres to work at their optimal length and partially compensate for the smaller PCSA.

Although the moment arm data in the present study are, at present, the only in vivo estimate of moment arms in men and boys, one of the limitations was that these measurements were made at rest. In a recent review by Maganaris (27), it was noted that from rest to MVC the moment arm can increase by ~25% at an ankle joint angle of –20°. Given that tendon force is calculated as joint torque/moment arm length, a greater increase in moment arm length from rest to MVC would lead to an overestimation of the forces and to an apparently higher specific force. It is, however, impossible, without a suitable model for the boys, to quantify how the change in moment arm during contraction differs between adults and children, and it is certainly something that warrants further investigation, particularly with the development of video fluoroscopy techniques that allow for the assessment of moment arms during MVC (1).

Other potential causes of the higher muscle specific force in the boys could involve differences in 1) myofibrillar protein density, 2) fiber composition, and 3) single-fiber specific tension. However, considering that myofibrils occupy more than 80% of total cell volume (9), it seems most unlikely that myofibrillar content could be higher in children since the remaining volume is occupied by vital cell components such as mitochondria, sarcoplasmic proteins, nucleus, lipids, and blood vessels. Differences in fiber composition are also an unlikely cause, since by the age of 6 yr, muscles of children have virtually the same percent fiber composition as those of adults (3). Last, specific tension of juvenile and adult animal muscle has been found to be similar (6); thus also the contribution of this factor seems doubtful.

With all the potential caveats regarding possible methodological issues associated with calculating specific force in children, it remains that specific force yielded by the GL in the present investigation is comparable to values obtained in other ankle muscles. For example, in the soleus and tibialis anterior, specific force was previously reported to be 15 N/cm2 (28), which is comparable to the 13.1 and 15.9 N/cm2 in the men and boys, respectively. As has been discussed previously (28), due to the fact that the gastrocnemius functions on the ascending limb of the length-tension relation, specific force is expected to remain lower than that reported for other muscles in vivo and in vitro (e.g., 24 N/cm2 in the rat EDL) (6). Furthermore, even when single fibers of human muscle are considered, a very large variability exists between the values reported in the literature, ranging from 6 to 20 N/cm2. As discussed by Bottinelli and Reggiani (5), physical (temperature), methodological (fiber swelling due to removal of cell membrane in skinned fibers, estimation of fiber CSA assuming a circular vs. elliptical shape, ionic strength of solution and type of salt used), and biological reasons (phosphate concentration, differences in myofibrillar protein density) may account for this discrepancy.

In conclusion, the present results suggest that specific force of early-pubertal boys is higher than that of young men. This unexpected finding was independent of differences in resting moment arm length, muscle architecture, and antagonist coactivation since these were accounted for in the calculations of specific force. Attention should, however, be drawn to the fact that the calculation of specific force in prepubertal populations requires a number of assumptions to be made based on data from adults (e.g., relative PCSA, in vivo length-tension relations, and moment arm lengths at MVC), which have yet to be confirmed experimentally. Thus the present results warrant further investigation.


   ACKNOWLEDGMENTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
REFERENCES
 
We express gratitude to Professor Roberto Bottinelli of the Institute of Human Physiology of the University of Pavia for critical advice regarding fiber specific tension.


   FOOTNOTES
 

Address for reprint requests and other correspondence: M. Narici, Institute for Biophysical Research into Human Movement and Health, Manchester Metropolitan Univ., Alsager Campus, Hassall Rd., Alsager, Cheshire ST7 2HL, UK (e-mail: m.narici{at}mmu.ac.uk)

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.


   REFERENCES
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 

  1. Baltzopoulos V. A videofluoroscopy method for optical distortion correction and measurement of knee-joint kinematics. Clin Biomech 10: 85–92, 1995.[CrossRef][Medline]
  2. Bamman MM, Newcomer BR, Larson-Meyer DE, Weinsier RL, Hunter GR. Evaluation of the strength-size relationship in vivo using various muscle size indices. Med Sci Sports Exerc 32: 1307–1313, 2000.
  3. Bell RD, MacDougall JD, Billeter R, Howald H. Muscle fiber types and morphometric analysis of skeletal muscle in six-year-old children. Med Sci Sports Exerc 12: 28–31, 1980.
  4. Berg HE, Tedner B, Tesch PA. Changes in lower limb muscle cross-sectional area and tissue fluid volume after transition from standing to supine. Acta Physiol Scand 148: 379–385, 1993.[Web of Science][Medline]
  5. Bottinelli R, Reggiani C. Human skeletal muscle fibres: molecular and functional diversity. Prog Biophys Mol Biol 73: 195–262, 2000.[CrossRef][Web of Science][Medline]
  6. Brooks SV, Faulkner JA. Contractile properties of skeletal muscles from young, adult and aged mice. J Physiol 404: 71–82, 1988.[Abstract/Free Full Text]
  7. Close RI. The relations between sarcomere length and characteristics of twitch contractions of frog sartorius muscle. J Physiol 220: 742–762, 1972.
  8. De Ste-Croix M, Deigham MA, Armstrong N. Assessment and interpretation of isokinetic muscle strength during growth and maturation. Sports Med 33: 727–743, 2003.[CrossRef][Web of Science][Medline]
  9. Eisenberg BR, Salmons S. The reorganization of subcellular structure in muscle undergoing fast-to-slow type transformation. A stereological study. Cell Tissue Res 220: 449–471, 1981.[CrossRef][Web of Science][Medline]
  10. Fukashiro S, Itoh M, Ichinose Y, Kawakami Y, Fukunaga T. Ultrasonography gives directly but noninvasively elastic characteristic of human tendon in vivo. Eur J Appl Physiol Occupat Physiol 71: 555–557, 1995.[CrossRef]
  11. Garcia-Morales P, Buschang PH, Throckmorton GS, English JD. Maximum bite force, muscle efficiency and mechanical advantage in children with vertical growth patterns. Eur J Orthod 25: 265–272, 2003.[Abstract/Free Full Text]
  12. Goldspink G. Increase in length of skeletal muscle during normal growth. Nature 204: 1095–1096, 1964.[CrossRef][Medline]
  13. Haxton HA. Absolute muscle force in the ankle flexors of man. J Physiol 103: 267–273, 1944.[Free Full Text]
  14. Herzog W, Read LJ, ter Keurs H. Experimental determination of force-length relations of intact human gastrocnemius muscles. Clin Biomech 6: 230–238, 1991.[CrossRef]
  15. Ikai M, Fukunaga T. Calculation of muscle strength per unit cross-sectional area of human muscle by means of ultrasonic measurement. Int Z Angew Physiol Einschl Arbeitsphysiol 26: 26–32, 1968.[CrossRef]
  16. Ito M, Kawakami Y, Ichinose Y, Fukashiro S, Fukunaga T. Nonisometric behavior of fascicles during isometric contractions of a human muscle. J Appl Physiol 85: 1230–1235, 1998.[Abstract/Free Full Text]
  17. Jozsa L, Kannus P. Postnatal development and differentiation of tendons. In: Human Tendons: Anatomy, Physiology, and Pathology. Champaign, IL: Human Kinetics, 1997, p. 116–118.
  18. Kanehisa H, Ikegawa S, Tsunoda N, Fukunaga T. Strength and cross-sectional area of knee extensor muscles in children. Eur J Appl Physiol Occupat Physiol 68: 402–405, 1994.[CrossRef]
  19. Kanehisa H, Ikegawa S, Tsunoda N, Fukunaga T. Strength and cross-sectional areas of reciprocal muscle groups in the upper arm and thigh during adolescence. Int J Sports Med 16: 54–60, 1995.[Web of Science][Medline]
  20. Kanehisa H, Yata H, Ikegawa S, Fukunaga T. A cross-sectional study of the size and strength of the lower leg muscles during growth. Eur J Appl Physiol Occupat Physiol 72: 150–156, 1995.[CrossRef]
  21. Klein CS, Rice CL, Marsh GD. Normalized force, activation, and coactivation in the arm muscles of young and old men. J Appl Physiol 91: 1341–1349, 2001.[Abstract/Free Full Text]
  22. Kubo K, Kanehisa H, Azuma K, Ishizu M, Kuno SY, Okada M, Fukunaga T. Muscle architectural characteristics in women aged 20–79 years. Med Sci Sports Exerc 35: 39–44, 2003.
  23. Macaluso A, De Vito G, Felici F, Nimmo MA. Electromyogram changes during sustained contraction after resistance training in women in their 3rd and 8th decades. Eur J Appl Physiol 82: 418–424, 2000.[CrossRef][Web of Science][Medline]
  24. Macaluso A, Nimmo MA, Foster JE, Cockburn M, McMillan NC, De Vito G. Contractile muscle volume and agonist-antagonist coactivation account for differences in torque between young and older women. Muscle Nerve 25: 858–863, 2002.[CrossRef][Web of Science][Medline]
  25. Maganaris CN. Force-length characteristics of in vivo human skeletal muscle. Acta Physiol Scand 172: 279–285, 2001.[CrossRef][Web of Science][Medline]
  26. Maganaris CN. Force-length characteristics of the in vivo human gastrocnemius muscle. Clin Anat 16: 215–223, 2003.[CrossRef][Web of Science][Medline]
  27. Maganaris CN. Imaging-based estimates of moment arm length in intact human muscle tendons. Eur J Appl Physiol 91: 130–139, 2004.[CrossRef][Web of Science][Medline]
  28. Maganaris CN, Baltzopoulos V, Ball D, Sargeant AJ. In vivo specific tension of human skeletal muscle. J Appl Physiol 90: 865–872, 2001.[Abstract/Free Full Text]
  29. Maganaris CN, Baltzopoulos V, Sargeant AJ. Differences in human antagonistic ankle dorsiflexor coactivation between legs; can they explain the moment deficit in the weaker plantarflexor leg? Exp Physiol 83: 843–855, 1998.[Abstract]
  30. Maganaris CN, Baltzopoulos V, Sargeant AJ. In vivo measurement-based estimations of the human Achilles tendon moment arm. Eur J Appl Physiol 83: 363–369, 2000.[CrossRef][Web of Science][Medline]
  31. Maughan RJ, Watson JS, Weir J. Strength and cross-sectional area of human skeletal muscle. J Physiol 338: 37–49, 1983.[Abstract/Free Full Text]
  32. Morris NM, Udry JR. Validation of a self-administered instrument to assess stage of adolescent development. J Youth Adolescence 9: 271–280, 1980.[CrossRef][Web of Science]
  33. Morse CI, Thom JM, Birch KM, Narici MV. Changes in triceps surae muscle architecture with sarcopenia. Acta Physiol Scand 183: 291–298, 2005.[CrossRef][Web of Science][Medline]
  34. Morse CI, Thom JM, Davis MG, Fox KR, Birch KM, Narici MV. Reduced plantarflexor specific torque in the elderly is associated with a lower activation capacity. Eur J Appl Physiol 92: 219–226, 2004.[CrossRef][Web of Science][Medline]
  35. Narici M, Landoni L, Minetti A. Assessment of human knee extensor muscles stress from in vivo physiological cross-sectional area and strength measurements. Eur J Appl Physiol Occupat Physiol 65: 438–444, 1992.[CrossRef]
  36. Narici MV, Binzoni T, Hiltbrand E, Fasel J, Terrier F, Cerretelli P. In vivo human gastrocnemius architecture with changing joint angle at rest and during graded isometric contraction. J Physiol 496: 287–297, 1996.[Abstract/Free Full Text]
  37. Neu CM, Rauch F, Rittweger J, Manz F, Schoenau E. Influence of puberty on muscle development at the forearm. Am J Physiol Endocrinol Metab 283: E103–E107, 2002.[Abstract/Free Full Text]
  38. Ramsay JA, Blimkie CJ, Smith K, Garner S, MacDougall JD, Sale DG. Strength training effects in prepubescent boys. Med Sci Sports Exerc 22: 605–614, 1990.
  39. Reeves N, Narici M, Maganaris CN. Effect of resistance training on skeletal muscle-specific force in elderly humans. J Appl Physiol 96: 885–892, 2004.[Abstract/Free Full Text]
  40. Reiser PJ, Westfall MV, Schiaffino S, Solaro RJ. Tension production and thin-filament protein isoforms in developing rat myocardium. Am J Physiol Heart Circ Physiol 267: H1589–H1596, 1994.[Abstract/Free Full Text]
  41. Round JM, Jones DA, Honour JW, Nevill AM. Hormonal factors in the development of differences in strength between boys and girls during adolescence: a longitudinal study. Ann Hum Biol 26: 49–62, 1999.[CrossRef][Medline]
  42. Streckis V, Skurvydas A, Ratkevicius A. Children are more susceptible to central fatigue than adults. Muscle Nerve 36: 357–363, 2007.[CrossRef][Medline]
  43. Tanner JM. Growth at Adolescence.: Blackwell, 1962.
  44. Vernon A, Alexander R. The Dimensions of Knee and Ankle Muscles and the forces they exert. J Hum Mov Stud 1: 115–123, 1979.
  45. Wickiewicz TL, Roy RR, Powell PL, Edgerton VR. Muscle architecture of the human lower limb. Clin Orthopaed Related Res: 275–283, 1983.
  46. Zipp P. Recommendations for the standardization of lead positions in surface electromyography. Eur J Appl Physiol Occupat Physiol 50: 41–54, 1982.[CrossRef]




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