Muscle strength is one of fundamental parameters in producing human movement and is related to muscle cross-sectional area (CSA) (6,12,13). In parallel-fibered muscles such as the elbow flexors, we recently found that an isometric contraction increases the CSA around the muscle belly (1,4,5) and that the index of the CSA (the product of the muscle thickness and circumference of the limb including the muscle) at a certain site during maximal voluntary contraction (MVC) is more closely related to the strength than that at rest (4,5). Thus, we consider that the measurement of muscle CSA not at rest but during MVC is important to examine an individual's ability to generate force at least in the elbow flexors. In our previous studies (4,5), however, the elbow flexor CSA was not measured but estimated at only 1 site without any consideration for individual differences in CSA distribution patterns along the upper arm length. Many studies (6,9,13,19) used the maximal CSA to accurately investigate the muscle CSA-strength relationship, and the site where CSA is maximal is expected to be highly individual. To confirm our above supposition, therefore, it is essential to more precisely determine the maximal elbow flexor CSA during MVC and to examine its relationship with elbow flexion strength. To that end, we should clarify individual variations in the CSA distribution patterns along the upper arm length and in their contraction-induced changes. Such information will be helpful for trainees to accurately assess muscle hypertrophy and also to keep track of strength capacity for a given muscle size.
Magnetic resonance imaging (MRI) provides consecutive multiple muscle CSAs with satisfactory accuracy, but the scan time is too long for many subjects to sustain MVC, and we thus fail to obtain analyzable magnetic resonance images. It is therefore unrealistic to measure muscle CSA during MVC with MRI. However, the contraction-induced elongation of a tendon, which is considered to be a factor affecting the corresponding increase in the CSA of elbow flexors (4), is remarkable in a low-intensity contraction (11,16). Additionally, muscle architecture has also been shown to change significantly with low-intensity contraction using MRI (8,18). Taken together, we expected that the contraction-induced increase in the elbow flexor CSA is small over a certain contractile level. In these cases, the determination of elbow flexor CSA during the highest possible contraction level at which MRI is applicable to determine the CSA should be useful for examining the relationship between the maximal CSA and strength during MVC for the elbow flexors. This study quantified the elbow flexor CSAs at rest and during isometric contractions at different percentages of MVC and examined their relations to the elbow flexion strength. We hypothesized that (a) the elbow flexor CSA changes greatly from rest to low-intensity contractions, (b) this contraction-induced change is small over a relatively high contractile level, and (c) the maximal muscle CSA during the highest possible contraction level is more closely related to the muscle strength than that at rest. The purpose of this study was to test these hypotheses.
Experimental Approach to the Problem
The elbow flexor CSAs were measured at sites from 1 cm proximal to 6 cm distal to the reference site (60% of the upper arm length from the acromial process of the scapula to the lateral epicondyle of the humerus) (every 1 cm; 8 sampling sites) using MRI, at rest and during 10, 20, 40, 60, and 80% of MVC of isometric elbow flexion (10%MVC, 20%MVC, 40%MVC, 60%MVC, and 80%MVC). The sampling sites were chosen so that the largest CSA was included. In accordance with previous studies (4,5), the strength of the elbow flexors was calculated by dividing the elbow flexion torque by the forearm length (the distance from the head of radius to the processus styloideus) of each subject. Using them, we determined the contraction-induced changes in the elbow flexor CSAs and examined the relationships between the maximal CSA at rest and during the isometric contractions and the MVC strength.
After having provided written informed consent, 14 young male subjects (age: 26 ± 3 years, body height: 172 ± 5 cm, body mass: 63 ± 11 kg; mean ± SDs) participated in this study. The subjects were sedentary or physically active, and none of them had any current or ongoing neuromuscular diseases and musculoskeletal injuries in the arm. The study protocol was approved by the Ethics Committee on Human Research of Waseda University.
Each subject was instructed to lie in a supine position on the bed of an MRI system (Signa 1.5T; GE Medical Systems, Milwaukee, WI, USA), and the position of the right arm was carefully adjusted by the MRI operator to have the length of the forearm aligned with the arm of a custom-made torque meter (VINE, Japan) (1–3) and to set the long axes of the upper arm and the forearm on a plane perpendicular to the arm of the custom-made torque meter. The forearm was then securely fastened to the arm of the torque meter using a nonelastic band, with the elbow flexed at 80° (full extension = 0°) and the wrist fixed to the torque meter in a fully supinated position. The shoulder was secured to the torque meter using a custom-made attachment. An optical fiber (Shinko Electric Wire, Kagawa, Japan) was attached onto the lever arm of the torque meter to record strains around the lever arm with a fiber Bragg grating sensor monitor (FB200; Yokogawa Electric, Tokyo, Japan), combined with an amplified spontaneous emission light source (ASE-1550-25; FiberLabs, Saitama, Japan). There was a strong linear relationship between torque around the axis of rotation of the torque meter created by a spring scale and the change in wavelength of the optical fiber (R 2 = 0.99). The experimental setup was described in our previous study (1). The subjects performed isometric elbow flexion at MVC for 3 seconds to measure their joint torque. The torque data were recorded by a software (FBGMonitor; Yokogawa Electric) installed in a personal computer at a sampling frequency of 100 Hz. The measurements were repeated 2 or 3 times with at least a 2-minute interval, and the highest value was adopted to calculate the strength of the elbow flexors.
A series of cross-sectional images of the right arm were obtained by the MRI system with 2 surface coils (GE Medical Systems): 1 with a 76-mm diameter used for the forearm and another with a 127-mm diameter used for the upper arm. The MRI scans were performed with a conventional proton density-weighted fast-recovery fast-spin echo technique (repetition time: 1,300 milliseconds, echo time: 20 milliseconds, echo train length: 8, bandwidth: 31.25 kHz, number of excitations: 0.5, slice thickness: 10 mm, interspaced distance: 0 mm, field of view: 200 × 140 mm with a 256 × 160 matrix). A reference marker was attached to the subjects' skin surface at 60% of the upper arm length from the acromial process of the scapula to the lateral epicondyle of the humerus. Within the device, the subjects maintained the aforementioned posture and wore an MRI-compatible goggle (MRVision 2000 with VisuaStim Digital's Controller, Resonance Technology, Northridge, CA, USA) that displayed the strength output to provide the subjects with visual feedback about their contraction intensity. First, a series of cross-sectional images of the right arm were scanned at rest for 13 seconds. Next, the same scanning was performed while the subjects sustained isometric voluntary contraction of elbow flexion for 15 seconds. At the start of torque recording, the subjects were asked to adjust their torque output levels to the required contractile levels within 2 seconds. After the MRI operator checked visually that both levels almost coincided, the scanning was performed for 13 seconds. If the subjects failed to adjust them within 2 seconds, the measurement was resumed after a 1-minute break. The contractions (10%MVC, 20%MVC, 40%MVC, 60%MVC, and 80%MVC) were performed in order of increasing intensity with at least a 2-minute interval to minimize the effect of fatigue on the data. The values of torque data from 2 to 15 seconds after starting the recording were used to calculate the mean values of percentage of MVC strength while the subjects sustained their forces at each contraction intensity: 10.0% ± 0.3% (10%MVC), 19.9% ± 0.3% (20%MVC), 39.7% ± 0.4% (40%MVC), 59.0% ± 1.5% (60%MVC), and 77.5% ± 2.9% (80%MVC) of MVC. Thus, on average, the subjects could sustain their forces close to the required contractile level.
In all scanned images, the outlines of the elbow flexors (biceps brachii, brachialis, and brachioradialis) were digitized, and the series CSAs at sites from 1 cm proximal to 6 cm distal to the reference marker were quantified using image analysis software (Osiris 4.19, University Hospital of Geneva, Switzerland). Each measurement was performed 1 time by an experienced tester (1,4). To ensure the day-to-day repeatability of the measurements, the same procedures were performed on another day for 1 subject. The coefficient of variation (CV) of the 2 measured values (6 contraction intensities × 8 sampling sites) was 1.4 ± 0.7%, and the intraclass correlation coefficient for them was 0.989.
Descriptive data are presented as mean ± SDs. A two-way analysis of variance (6 contraction intensities × 8 sampling sites) with repeated measures was used to test the effect of the contraction intensities on the CSA. When the interaction between the 2 factors was significant, a simple main effect test using the Bonferroni's multiple comparison method was performed. Pearson's product-moment correlation coefficients between the maximal CSA at rest and during the isometric contractions and the MVC strength were calculated. Furthermore, a bidirectional stepwise multiple regression analysis was performed, including the maximal CSA at rest and each contraction level as the independent variables and the MVC strength as the dependent variables. Statistical significance was set at p ≤ 0.05.
The CSAs at rest and during the isometric contractions are shown in Table 1. There was a significant interaction between the contraction intensities and the sampling sites for the CSA. At sites from 1 cm proximal to 1 cm distal to the reference marker, the CSA during 80%MVC was significantly greater than that at rest. Meanwhile, the CSAs at sites 5 and 6 cm distal to the reference marker were significantly lower during 80%MVC than at rest. Compared with at rest, the CSA distribution pattern along the upper arm length varied greatly even at 10%MVC as shown in Figure 1. At each sampling site, there was no significant difference between the CSAs during 60%MVC and 80%MVC.
Figure 2 shows the elbow flexor CSA distribution patterns along the upper arm length for each subject at rest and during each isometric contraction. The site where the maximal CSA was found was highly individual at rest and each contraction level. In addition, the corresponding site during isometric contractions was more proximal than that at rest in most subjects. The MVC strength was significantly correlated with the maximal CSA in all conditions (rest: r = 0.584; 10%MVC: r = 0.606; 20%MVC: r = 0.586; 40%MVC: r = 0.606; 60%MVC: r = 0.607; 80%MVC: r = 0.641). The correlation coefficients between the maximal CSAs during 60%MVC and 80%MVC and the MVC strength were higher than that between the maximal CSA at rest and the MVC strength. As a result of the stepwise multiple regression analysis, only the maximal CSA during 80%MVC was selected as a significant contributor for estimating the MVC strength (Figure 3).
The CSA of elbow flexors was greater during 80%MVC than at rest at sites from 1 cm proximal to 1 cm distal to the reference marker, in line with previous studies (1,4,5). Meanwhile, a significantly greater CSA at rest than during 80%MVC was seen at the sites 5 and 6 cm distal to the reference marker. Given that muscle volume does not change by contraction (7), it is not surprising that the aforementioned increase in the CSA around the muscle belly with the contraction results in contraction-induced decreases in the CSA at other positions.
As shown in Figure 1, the CSA distribution pattern along the upper arm length was drastically altered even at 10%MVC compared with at rest. Moreover, the CSA during 80%MVC, which was the highest contraction intensity in this study, was not significantly different from that during 60%MVC at each sampling site (Table 1). Thus, there is a curvilinear relationship between the contraction intensity and the elbow flexor CSA, and the contraction-induced increase in the elbow flexor CSA appears to be small over 60%MVC. Therefore, the first and second hypotheses described earlier are supported, and it is expected that the elbow flexor CSA at >60%MVC differs little from that during MVC. In this study, the elbow joint was fixed at 80° both at rest and during isometric contractions, and the elbow flexor muscle-tendon complex remained constant in length. Consequently, the elongation of the tendon induced by isometric contractions affects the above CSA distribution pattern. It has been shown that, compared with at rest, the contraction-induced increase in the length of the distal tendon of the biceps brachii is 2.0, 3.3, 6.0, 7.5, and 8.5 mm during 10%MVC, 20%MVC, 40%MVC, 60%MVC and 80%MVC, respectively (16). Thus, the tendon elongation appears prominently during low-intensity contraction and comes close to its peak above a relatively high contractile level, likely contributing to the present results on the contraction-induced change in muscle CSA.
At rest, the site where the maximal CSA was found varied with each individual (Figure 2A), presumably because of individual differences in the upper arm length and the length of the elbow flexors. There was also a large individual variation in the corresponding site during isometric contractions, and the site showing the maximal CSA during each contraction was more proximal than that at rest in most subjects (Figure 2B–F). These results suggest that measuring muscle CSAs at multiple sites is important to accurately examine the muscle CSA-strength relationship. In addition, the individual differences in muscle CSA at each site during isometric contractions were generally larger than those at rest as shown in Figure 3. In the previous study cited above (16), the elongation of the distal tendon of the biceps brachii was shown to be highly individual during isometric contractions (the CVs for 14 young men were approximately 34–47% during 10–80%MVC). This may be a reason for the large differences in muscle CSA at each site under the contracted condition because the elongation of the distal tendon of the biceps brachii is a factor in the contraction-induced change in the CSA distribution pattern along the upper arm length as described above. Previously, we estimated the muscle CSA both at rest and during MVC at only 1 site and mentioned the importance of measuring the muscle CSA during MVC for investigating the muscle CSA-strength relationship (4,5). Considering the present findings, however, the muscle CSA during the highest possible contraction level to which MRI is applicable (i.e., 80%MVC in this study) needs to be quantified at multiple sites to more accurately assess the muscle CSA-strength relationship.
Although the MVC strength was significantly correlated with the maximal CSAs in all conditions, the correlation coefficients between the maximal CSAs at 60%MVC (and higher levels as well) and the MVC strength were higher than that between the maximal CSA at rest and the MVC strength. Additionally, only the maximal CSA during 80%MVC was selected as a significant contributor for estimating the MVC strength. This supports the previous finding that a muscle CSA index determined by ultrasonography and a measuring tape during MVC is more closely related to muscle strength than that at rest (4,5). Strictly speaking, physiological CSA should be used to precisely evaluate the muscle CSA-strength relationship and/or the muscle strength per CSA (14,17). In parallel-fibered muscles whose fibers are oriented in parallel to the muscle line of action, however, it is considered that the CSA cuts all the fibers at right angles and thus corresponds to the physiological CSA (10,15). Thus, the maximal CSA of a parallel-fibered muscle can be a useful parameter to accurately assess the muscle CSA-strength relationship, like its physiological CSA. In terms of the maximal CSA, this study suggests that the CSA during MVC rather than at rest should be adopted to more precisely evaluate the muscle CSA-strength relationship and one's ability to generate force in the elbow flexors.
This study showed that the elbow flexor CSA and its distribution pattern along the upper arm length changed greatly even at 10%MVC and that the contraction-induced change in the elbow flexor CSA reached almost saturated at and above 60%MVC. To our knowledge, this is the first study to demonstrate the detailed changes in muscle CSA induced by several contraction intensities and to discuss the contribution of tendon elongation to the aforementioned changes in muscle CSA. Given that muscle CSA is a major determinant of muscle strength (6,12,13), the data related to contraction-induced muscle CSA are useful to develop a more realistic musculotendinous model. In addition, this study found that the elbow flexion strength was significantly correlated with the maximal elbow flexor CSAs at rest and each contraction level, but only the maximal CSA during 80%MVC was selected as a significant contributor for estimating the strength. These results suggest that the muscle CSA during the highest possible contraction level to which MRI is applicable needs to be quantified at multiple sites. In doing so, one can evaluate the muscle CSA-strength relationship more accurately.
This study was partly supported by JSPS KAKENHI Grant Number 22800089 (Grant-in-Aid for Research Activity Start-up) and 24700689 (Grant-in-Aid for Young Scientists (B)).
1. Akagi R, Iwanuma S, Fukuoka M, Kanehisa H, Fukunaga T, Kawakami Y. Methodological issues related to thickness-based muscle size evaluation. J Physiol Anthropol 30: 169–174, 2011.
2. Akagi R, Iwanuma S, Hashizume S, Kanehisa H, Yanai T, Kawakami Y. In vivo measurements of moment arm lengths of three elbow flexors at rest and during isometric contractions. J Appl Biomech 28: 63–69, 2012.
3. Akagi R, Iwanuma S, Hashizume S, Kanehisa H, Yanai T, Kawakami Y. Association between contraction-induced increases in elbow flexor muscle thickness and distal biceps brachii
tendon moment arm depends on the muscle thickness measurement site. J Appl Biomech 30: 134–139, 2014.
4. Akagi R, Kanehisa H, Kawakami Y, Fukunaga T. Establishing a new index of muscle cross-sectional area and its relationship with isometric muscle strength. J Strength Cond Res 22: 82–87, 2008.
5. Akagi R, Takai Y, Kato E, Fukuda M, Wakahara T, Ohta M, Kanehisa H, Kawakami Y, Fukunaga T. Relationships between muscle strength and indices of muscle cross-sectional area determined during maximal voluntary contraction in middle-aged and elderly individuals. J Strength Cond Res 23: 1258–1262, 2009.
6. 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.
7. Baskin RJ, Paolini PJ. Volume change and pressure development in muscle during contraction. Am J Physiol 213: 1025–1030, 1967.
8. Finni T, Havu M, Sinha S, Usenius JP, Cheng S. Mechanical behavior of the quadriceps femoris muscle tendon unit during low-load contractions. J Appl Physiol 104: 1320–1328, 2008.
9. Fukunaga T, Miyatani M, Tachi M, Kouzaki M, Kawakami Y, Kanehisa H. Muscle volume is a major determinant of joint torque in humans. Acta Physiol Scand 172: 249–255, 2001.
10. Gadeberg P, Andersen H, Jakobsen J. Volume of ankle dorsiflexors and plantar flexors determined with stereological techniques. J Appl Physiol (1985) 86: 1670–1675, 1999.
11. Ito M, Kawakami Y, Ichinose Y, Fukashiro S, Fukunaga T. Nonisometric behavior of fascicles during isometric contractions of a human muscle. J Appl Physiol (1985) 85: 1230–1235, 1998.
12. Kent-Braun JA, Ng AV. Specific strength and voluntary muscle activation in young and elderly women and men. J Appl Physiol (1985) 87: 22–29, 1999.
13. Klein CS, Rice CL, Marsh GD. Normalized force, activation, and coactivation in the arm muscles of young and old men. J Appl Physiol (1985) 91: 1341–1349, 2001.
14. Morse CI, Tolfrey K, Thom JM, Vassilopoulos V, Maganaris CN, Narici MV. Gastrocnemius muscle specific force in boys and men. J Appl Physiol (1985) 104: 469–474, 2008.
15. Narici MV, Landoni L, Minetti AE. Assessment of human knee extensor muscles stress from in vivo physiological cross-sectional area and strength measurements. Eur J Appl Physiol Occup Physiol 65: 438–444, 1992.
16. Ohta M, Masuo Y, Kanehisa H, Kawakami Y, Fukunaga T. Study on the application of the bio-electrical impedance method for the estimation of tendon elongation. Int J Sport Health Sci 3: 296–303, 2005.
17. O'Brien TD, Reeves ND, Baltzopoulos V, Jones DA, Maganaris CN. In vivo measurements of muscle specific tension in adults and children. Exp Physiol 95: 202–210, 2010.
18. Pappas GP, Asakawa DS, Delp SL, Zajac FE, Drace JE. Nonuniform shortening in the biceps brachii
during elbow flexion. J Appl Physiol (1985) 92: 2381–2389, 2002.
19. Wokke BH, van den Bergen JC, Versluis MJ, Niks EH, Milles J, Webb AG, van Zwet EW, Aartsma-Rus A, Verschuuren JJ, Kan HE. Quantitative MRI and strength measurements in the assessment of muscle quality in Duchenne muscular dystrophy. Neuromuscul Disord 24: 409–416, 2014.
Keywords:Copyright © 2015 by the National Strength & Conditioning Association.
biceps brachii; brachialis; brachioradialis; isometric contraction; magnetic resonance imaging