General discussion

strength because of the contraction-induced increase in the CSA of contractile component relative to the muscle CSA index at the measurement site. The present results support this assumption regardless of age. Notably, this phenomenon was clearly observed in middle-aged and elderly individuals. The proportion of the noncontractile tissues within a muscle compartment for elderly individuals is greater than that for young adults (Kent-Braun et al. 2000, Klein et al. 2001, Rice et al. 1990) and the volume of the arm skin and subcutaneous tissue increases with aging (Rice et al. 1989, 1990). The MT and C include not only contractile component but also noncontractile component. In addition, C includes not only elbow flexor muscles but also other tissues such as skin and subcutaneous adipose tissue. These facts suggest that the accuracy of MTr×Cr for middle-age and elderly individuals is lower than that for young adults, and correspondingly that the difference in the accuracy of MT×C between during MVC and at rest for middle-age and elderly individuals is greater compared with young adults. In contrast to young adults, therefore, the correlation coefficient between MTm×Cm and F appears to be significantly higher than that between MTr×Cr and F in middle-aged and elderly individuals.

5-2. Effects of contraction-induced change in muscle shape on the accuracy of muscle CSA index

Age dependence of change in muscle shape induced by contraction

Muscle shape for young men was found to be greatly changed by contraction (Chapter 2).

This phenomenon is expected to be observed in other individuals. As a reason for the change in the cross-section of elbow flexor muscles induced by contraction, the elongation of a tendon during contraction has been considered. Considering that tendon stiffness decreases with aging (Kubo et al. 2003b, Onambélé et al. 2007, Reeves 2006), there is a possibility that the muscle shapes at rest and/or during contraction for middle-aged and elderly individuals are different from those for young adults. If so, this affects the differences in the accuracy of MT×C between

at rest and during MVC and/or between age groups.

Then, the cross-section of elbow flexor muscles for nine older men (57-74 yr) at the level of 60% of the upper arm length was determined by MRI in the same way as used in the Chapter 2 (Figure 2-1) and the data was compared with that of younger men (n = 11) described in the Chapter 2. During 30%MVC, there were no significant differences in all variables (CSA, thickness, height, width and H/W) between older and younger men. At rest, the CSA, thickness and width for older men were not significantly different from those for younger men. However, the height for older men, 5.2 ± 0.7 cm, was significantly higher than that for younger men, 4.6 ± 0.4 cm. In addition, H/W for older men, 0.75 ± 0.11, tended to be higher than that for younger men, 0.66 ± 0.10. The schematic diagram of the cross-sections of elbow flexor muscles at the level of 60% of the upper arm length at rest for older and younger men is shown in Figure 5-1.

Given that gravitational force acts in the posterior direction on the subjects in the supine position, these results suggest that, compared with younger men, the relaxed muscle for older men hangs more greatly in direction of gravitational force due to its more slackness. In contrast, stiffened muscle during contraction might resist gravity to maintain its shape in both older and younger men. In the Chapter 3 and Chapter 4, too, shape of elbow flexor muscles was subjected to gravitational force in the posterior direction as well as in the Chapter 2. Consequently, it is likely that the difference in the muscle shape at rest between the age groups also affects the lower accuracy of MTr×Cr in middle-aged and elderly individuals compared with that in young adults.

Muscle size dependence of change in muscle shape induced by contraction

In the preceding section, age dependence of change in muscle shape induced by contraction and its effects on the accuracy of muscle CSA index were discussed. From the results of the relationships between the product of thickness and circumference and the CSA for elbow flexor muscles in younger men (Figure 2-5) and in older men (Figure 4-2), however, it appears

that the greater change in the values of the product of thickness and circumference from at rest to during 30%MVC is observed for those with the lower CSA. That is, there is a possibility that the muscle shape at rest for the subject having the lower CSA is more affected by gravity. As described above, the difference in tendon stiffness is thought to be involved in the difference in the muscle shape at rest. Scott and Loeb (1995) reported that the stiffness of tendinous tissues was positively correlated with muscle strength in the cat soleus muscle. Given that muscle CSA is related to muscle strength, therefore, tendon structure may be stiffer in subjects with greater muscle CSA. In fact, several studies (Kubo et al. 2001a, 2001b, 2002) have indicated that isometric training and/or resistance training increase the stiffness of human tendon structures as well as muscle size and strength. These reports suggest that the interindividual variation in muscle size and strength induced by resistance training and/or disuse is involved in the interindividual variation in tendon stiffness. Therefore, the difference in contraction-induced change in muscle shape might be affected by the difference in muscle size and/or strength.

To examine this possibility, the values of muscle CSA during 30%MVC for the subjects were arranged in ascending order and the subjects were allocated to a group who had a smaller CSA (7 younger men and 3 older men) and another group who had a greater CSA (4 younger men and 6 older men). The schematic diagram of the cross-sections of elbow flexor muscles at the level of 60% of the upper arm length at rest for the two groups is shown in Figure 5-2. There were significant differences in the CSA both at rest and during 30%MVC between the two groups. Correspondingly, the height and width of elbow flexor muscles measured both at rest and during 30%MVC for the group who had the smaller CSA were significantly lower than those for the group who had the greater one. The thickness at rest was also lower for the group who had the smaller CSA than for the group who had the greater one, and that during 30%MVC for the group who had the smaller CSA tended to be lower than that for the group who had the greater one. Furthermore, the vertical distance from the upper end to the humerus to the lower end of the

elbow flexor muscles during 30%MVC for the group who had the smaller CSA was significantly lower than that for the group who had the greater one. However, there was not a significant difference in the aforementioned vertical distance at rest between the two groups. In short, the variables determined during 30%MVC were lower for the group who had the smaller CSA than for the group who had the greater one depending on the difference in their CSA, but their corresponding differences were not always observed at rest. These results suggest that the values of each variable are proportional to the value of the CSA during 30%MVC since stiffened muscle during contraction might resist gravity by maintaining its shape and that the relaxed muscle for the group who had the smaller CSA hangs more greatly in direction of gravitational force due to its more slackness compared with the group who had the greater CSA. Thus, it may be that the difference in muscle size affects the differences in contraction-induced change of muscle shape and, correspondingly, in the accuracy of muscle CSA index.

As mentioned above, the change in muscle shape induced by contraction has an effect on the accuracy of muscle CSA index. In other words, it is indicated that the slackness of relaxed muscle affects the accuracy of muscle CSA index. Then, the difference in the change in muscle shape seems to be influenced by the differences in both age and muscle size. Considering that muscle size decreases with aging (Janssen et al. 2000), the relationship between the slackness of relaxed muscle and age might be influenced by muscle size. Further investigation is required to address this issue.

5-3. New explanation for the ratio of muscle strength to CSA

In the Chapter 2 and Chapter 4, the muscle CSA index determined during contraction appeared to be more highly correlated with muscle CSA than that determined at rest. Moreover,

this thesis indicated that MTm×Cm was more pertinent to evaluate F than MTr×Cr in both age groups (Figure 3-4 and Figure 4-1). Therefore, it seems that the ratio of muscle strength to CSA index should be calculated using MTm×Cm (i.e., F per MTm×Cm).

It is known that the ratio of muscle strength to CSA considerably varies among individuals in vivo (Maughan et al. 1983, Maughan and Nimmo 1984). As explainable reasons for the large interindividual variation in the ratio of human skeletal muscle, muscle fiber composition (Nygaard et al. 1983, Thorstensson et al. 1976) and neural factors (Komi and Karlsson 1979) have been considered. However, the previous findings on the muscle strength per CSA have been obtained using muscle dimensions at rest. Then, a comparison between the CVs of F per MT×C at rest and during MVC was performed in each age group. As a result, the CVs of F per MTm×Cm were 12.8% for young adults and 15.4% for middle-aged and elderly individuals, respectively. The corresponding values of F per MTr×Cr were 14.5% for young adults and 20.8% for middle-aged and elderly individuals, respectively. When a two-tailed test for difference between two CVs (Zar 1999) was performed, there was a significant difference in the CVs of F per MT×C between at rest and during MVC in middle-aged and elderly individuals (P < 0.05). These results suggest that the use of MTm×Cm is possible to conveniently and accurately assess the ratio of muscle strength to CSA index of human skeletal muscle, especially for middle-aged and elderly individuals. In other words, the application of muscle dimensions at rest can also be one of the factors producing a large interindividual variation in the value of muscle strength per CSA reported previously.

Age-related difference in the ratio of muscle strength to CSA

The F per MTm×Cm might be useful for discussing a new insight into the age-related difference in the muscle strength per CSA. However, the slope and intercept for the regression line to predict the CSA from the product of thickness and circumference for younger were

significantly different from those for older men. Correspondingly, there were significant differences in the slopes and intercepts for the regression lines to predict the F from the MTm×Cm

between age groups. The proportion of the noncontractile tissues within a muscle compartment and the volume of the arm skin and subcutaneous tissue increases with aging (Rice et al. 1990).

The thickness measured by ultrasonography and the circumference measured by a measuring tape involve both contractile and noncontractile components, and the circumference also includes not only elbow flexor muscles but also skin and subcutaneous adipose tissue.

Consequently, it is not surprising that there were significant differences in their slopes and intercepts the regression lines to predict the F from the MTm×Cm between age groups. Thus, a comparison of the absolute values of F per MTm×Cm between them appears to be difficult.

Thus, MTm×Cm is useful to evaluate the muscle strength per CSA index and to compare its differences among individuals in each age group. However, it is impossible to elucidate the difference in the ratio of muscle strength to CSA between age groups using this index.

5-4. Factors capable of influencing the interpretation of the present results

When the relationship between MT×C and F for elbow flexor muscles was examined in this thesis, the brachioradialis, the pronator teres and the extensor carpi radialis longus muscles were not considered as the elbow flexor synergists. From the data of Murray et al. (2000), the pronator teres and the extensor carpi radialis longus muscles together generate only 14% of elbow flexion torque. Even if there is an interindividual variation in the contributions of the pronator teres and the extensor carpi radialis longus muscles to elbow flexion, therefore, the present results would not be affected by it. On the other hand, Kawakami et al. (1994) have reported that the contribution of the biceps brachii and the brachialis to elbow flexion is 3.2-6.1

times as large as that of the brachioradialis. In short, the contribution of the brachioradialis to elbow flexion is low, but its interindividual variation seems to be large. If so, the present results of the relationships between muscle CSA index and strength in both age groups might be influenced by ignoring the contribution of the brachioradialis. Then, the relationships between each of the volume of three muscles (biceps brachii, brachialis and brachioradialis) and that of two muscles (biceps brachii and brachialis) and elbow joint flexion torque were examined in 12 young men (n = 10) and women (n = 2). As a result, elbow joint flexion torque was highly correlated with either the volume of three muscles (r = 0.913, P < 0.001) or that of two muscles (r = 0.882, P < 0.001) (Figure 5-3). Furthermore, the correlation coefficients between the volume of three muscles and that of two muscles was close to 1 (r = 0.994, P < 0.001). Hence, it is most likely that the interpretation of the present results of the relationships between muscle CSA index and strength is not affected by the fact that the brachioradialis is not regarded as the elbow flexor muscles.

Activation and coactivation levels

In this thesis, activation levels of agonist muscles (i.e., elbow flexor muscles) and coactivation levels of antagonist muscles (i.e., elbow extensor muscles) during MVC were not determined. Prior studies (Klein et al. 2001, Jakobi and Rice 2002) have reported that there is no difference in the maximal voluntary activation of elbow flexor muscles between young and old men, but that its interindividual variation is higher for old men than for young men. Moreover, the coactivation level of elbow extensors during MVC of the elbow flexor muscles for old men has been shown to be higher than that for young men (Klein et al. 2001). These reports indicate that, especially in middle-aged and elderly individuals, the activation and coactivation levels during MVC probably affect the relationship between muscle CSA index and strength. However, each plot on the correlation charts shifts in the only y-axis direction and the degrees of each shift

on the correlation chart between MTr×Cr and F are equal to those between MTm×Cm and F.

Consequently, the activation and coactivation levels during MVC would not affect the interpretation of the present results that MTm×Cm is more closely related to F than MTr×Cr in each age group.

Moment arm of a muscle

The moment arm has been reported to be increased by isometric contraction (Ito et al.

2000, Maganaris et al. 1998). Furthermore, it is not clear whether the moment arm during MVC is related to the limb length. If muscle strength is calculated from TQ divided by the moment arm during MVC in this thesis, therefore, there is a possibility that the correlations between MT×C and F in each condition and in each age group change. Further investigation is needed to clarify this point.

Measurement site of MT and C

In young men, the CSA at the site 3-4 cm distal from the level of 60% of the upper arm length was largest(Figure 2-3). Similar observation was reported for middle-aged and elderly men (Figure 5-4). When the relationships between MT×C and F were examined in each age group, MT×C was determined only at the level of 60% of the upper arm length. Hence, the limb level where MT×C was determined might be a reason for the present results that MTm×Cm is more closely related to F than MTr×Cr. The relationships between MT×C determined at the level of 70% of the upper arm length both at rest and during MVC and F were also tested in 25 young men (n = 23) and women (n = 2) to clarify this point, and, the similar observations were obtained to those reported in the Chapter 3. In short, the present results of the relationships between MT×C determined at rest and during MVC and F do not appear to be affected by the measurement site of MT and C.

5-5. Conclusion of the thesis

The general purposes of this thesis were to introduce a new index of muscle CSA and to examine the relationship between the muscle CSA index determined during isometric MVC and muscle strength. To this end, the new index of muscle CSA was established based on the quantification of muscle cross-section changes during submaximal contraction and the relationship between this index and muscle strength was examined. The main findings of this thesis are following three points. Firstly, the CSA and the thickness of belly of elbow flexor muscles increase and the width of it decreases during submaximal contraction as compared with those at rest. Secondly, MT×C can be an index for assessing muscle CSA not only at rest but also during contraction. Thirdly, MTm×Cm is more closely related to F than MTr×Cr. These findings suggest that 1) the product of thickness and circumference of elbow flexor muscles is a reliable index of muscle CSA, and that 2) the index during isometric MVC is able to more accurately examine its relation to muscle strength than that at rest.

older men younger men

anterior

posterior

gravitational force

humerus

Figure 5-1 Schematic diagram of the cross-sections of elbow flexor muscles at the level of 60% of the upper arm length at rest for younger and older men.

group who had a smaller CSA group who had a greater CSA

anterior

posterior

gravitational force

humerus

Figure 5-2 Schematic diagram of the cross-sections of elbow flexor muscles at the level of 60% of the upper arm length at rest for a group who had a smaller CSA and another group who had a greater CSA.

Elbow joint torque (Nm)

Muscle volume (cm³)

○ three muscles

● two muscles y = 0.188x + 2.68 r = 0.913 (P < 0.001) y = 0.231x + 2.50

r = 0.882 (P < 0.001)

0 30 60 90

0 100 200 300 400 500

Figure 5-3 Relationships between each of the volume of three muscles (biceps brachii, brachialis and brachioradialis) and that of two muscles (biceps brachii and brachialis) and elbow joint flexion torque in young adults (n = 12).

0 5 10 15 20 25 30

-1 0 1 2 3 4 5 6 7

Distance (cm) CSA (cm2 )

Figure 5-4 Mean values of CSA of elbow flexor muscles at rest (●) and during 30%MVC (○) for older men (n = 9). CSA, cross-sectional area; MVC, maximal voluntary contraction. The abscissa shows the distance from the level of 60% of the upper arm length in a distal direction.

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