新たな筋横断面積指標の確立 Establishing a new index of muscle cross-sectional area

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【課程内】

博士（スポーツ科学）学位論文

新たな筋横断面積指標の確立

Establishing a new index of muscle cross-sectional area

２００９年１月

早稲田大学大学院スポーツ科学研究科

赤木亮太 Akagi, Ryota

研究指導教員：矢内利政教授

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Chapter 1 Introduction

1-1. Preface

Muscle strength is one of fundamental parameters which produce human movement, and is related to muscle cross-sectional area (CSA) (Bamman et al. 2000, de Koning et al. 1986, Ikai and Fukunaga 1968). Hence, measurement of muscle CSA is important to examine one’s ability to generate force. Magnetic resonance imaging (MRI) and computed tomography (CT) provide precise muscle size measurements, but these techniques have poor applicability to practical uses in field studies. On the other hand, muscle CSA indices determined by other techniques such as ultrasonography and/or use of a measuring tape are useful to evaluate the muscle CSA and its relation to muscle strength for a large number of subjects in field studies. The more reliable a muscle CSA index is, the more accurate the assessment of CSA and its relation with force become.

Although muscle strength is a parameter measured in contracted conditions, the muscle CSA has been measured and/or estimated at rest. In parallel-fibered muscles such as the biceps brachii and brachialis, however, it has been reported that an isometric contraction increases the thickness (Hodges et al. 2003, Shi et al. 2008). This suggests that contraction of these muscles results in an increase in their CSA and an increase in the CSA of contractile component relative to the muscle CSA index at a measurement site. Therefore, it is suggested that the muscle CSA index should not be determined at rest, but it should be done during contraction so as to properly assess the relationship between muscle CSA index and strength and/or the muscle strength per CSA index.

A use of ultrasonography and a measuring tape makes it possible to evaluate the changes in muscle architecture during contraction. Using these techniques, therefore, an index for evaluating muscle CSA during contraction can be developed. The main purposes of this thesis

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are to establish a new index for evaluating muscle CSA not only at rest but also during contraction and to examine how the index of muscle CSA measured during isometric contraction is related to muscle strength.

1-2. Terminology

(1) Muscle architecture

In this thesis, the term “muscle architecture” refers to the following elements: muscle size, pennation angle, fascicle length and moment arm of a muscle. Further details on muscle size are described below.

(2) Muscle size

The term “muscle size” is used, in general, as a generic term for muscle thickness, muscle CSA and muscle volume. It is well known that muscle size is related to muscle strength.

In particular, muscle CSA is suggested to be the most appropriate variable assessing muscle size to use when discussing muscle size-strength relationship and/or muscle strength per size (Bamman et al. 2000). Consequently, muscle CSA is adopted as the representative term of muscle size in this thesis.

(3) Muscle CSA

Two types of muscle CSA are determined; One is the anatomical CSA (ACSA) which is measured as the area perpendicular to the long axis of muscle. The other is the physiological CSA (PCSA) which is the sum of the CSA of all muscle fibers (Kawakami et al. 1994) and estimated by dividing muscle volume by muscle fiber length (Fukunaga et al. 1992). This thesis examines the biceps brachii and brachialis, which are parallel-fibered muscles (Amis et al. 1979).

It is, therefore, assumed that the ACSA of them cut all the fibers at right angles and thus

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correspond to the PCSA (Gadeberg et al. 1999, Narici et al. 1992). In this thesis, the term

“muscle CSA” represents ACSA. When previous studies are overviewed, ACSA and PCSA are described separately as needed.

(4) Muscle strength

Muscle strength has been used in a wider sense. For example, some researchers (Bamman et al. 2000, Maughan et al. 1983, Young et al. 1984, etc.) have regarded it as the magnitude of force (N) generated during a maximal voluntary contraction (MVC) and other researchers (Arokoski et al. 2002,Holzbaur et al. 2007, Miller et al. 1993) have used joint torque (Nm) as a measure of muscle strength. When prior studies are overviewed in this chapter, therefore, the term “muscle strength” is used as a generic term for the following force exerted by muscle contraction:

1) Force generated by a muscle and calculated by the product of specific tension and PCSA (Muscle force/Muscle tension).

2) Force transmitted from a muscle to a tendon and calculated by the product of muscle force (muscle tension) and cos θ (θ: pennation angle) (Tendon force/Tendon tension).

3) Force measured outside a body and calculated as the joint torque divided by a limb length of each subject or a length of lever arm of a dynamometer used for measuring joint torque.

“Muscle strength” used in this thesis represents joint force (N), which is calculated from joint torque (Nm) divided by a limb length (m) of each subject.

1-3. Review of literature

The purposes of this thesis are to establish a new index for assessing muscle CSA both at rest and during contraction and to examine the relationship between the muscle CSA index

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during isometric contraction and muscle strength. In this section, related studies are overviewed from following three viewpoints: 1) the methods of quantification of muscle size, 2) the relationship between muscle CSA and strength, and 3) the changes in muscle architecture during isometric contraction.

1-3-1. Methods of quantification of muscle size MRI and CT

A number of techniques are available for measuring and/or estimating muscle size (Lee et al. 2001). Of these techniques, MRI and CT are considered as a gold standard. Thus far, muscle size has been measured by them (Abe et al. 2003, Alway et al. 1996, Davies et al. 1988, Goodpaster et al. 2006, Janssen et al. 2000, Jubrias et al. 1997, Kent-Braun et al. 2000, Klein et al. 2002, Macaluso et al. 2002, Miles et al. 2005, Morse et al. 2005a, 2005b, 2007, Narici et al.

2003, Overend et al. 1992a, Rice et al. 1989, 1990, Roman et al. 1993, Sipila and Suominen 1993). The validity of these techniques has been confirmed by Mitsiopoulos et al. (1998).

However, the use of them is often limited due to the large clinical demand and considerable cost.

Hence, they have poor applicability to practical use in field studies with a large sample size. In addition, these techniques require a considerable amount of time to obtain clear images.

Moreover, CT has the problem of the radiation exposure.

Ultrasonography

Ultrasonography has the same merit as those of MRI and CT in directly visualizing muscle tissue. Since Ikai and Fukunaga (1968) directly measured the CSA of elbow flexor muscles in vivo by ultrasonography using a compound scanning technique, its method has been applied to measure muscle CSA (Kanehisa et al. 1994a, 1994b, Sipila and Suominen 1991, Young et al. 1984, 1985). On the other hand, ultrasonography using a real-time brightness mode

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(B-mode) has also been applied to measure muscle thickness (Abe et al. 1997, 2000, Campbell et al. 1995, Kubo et al. 2003a, Pinkoski et al. 2006) and produces images of high quality (Reeves et al. 2004). The precision and linearity of this image reconstruction have been described and confirmed in prior reports (Kawakami et al. 1993, Narici et al. 1996a). Some studies (Abe et al.

1997, Sipila and Suominen 1991, 1993) have reported that muscle thickness is correlated with CSA, and other studies (Fukunaga et al. 2001, Miyatani et al. 2000, 2002) have used squared value of muscle thickness as an index of muscle CSA in accordance with an idea that the cross-section of the whole skeletal muscle can be approximated by a circle and its diameter is equal to muscle thickness. Martinson and Stokes (1991) have reported that the squared value of muscle thickness is highly correlated with muscle CSA as well as the product of muscle thickness and width in the anterior tibial muscle. Moreover, muscle CSA has been directly measured using real time B-mode ultrasound images in prior studies (Esformes et al. 2002, Reeves et al. 2004). A compact type ultrasound apparatus makes it easily portable (Sanada et al.

2006). Hence, ultrasonography is applicable to practical use in field studies on a large number of subjects. However, the major drawback of this technique is the limitation to image size which may not be sufficiently large to cover the whole section of the muscle of interest.

Use of a measuring tape and/or a skinfold caliper

Use of a measuring tape and/or a skinfold caliper is also useful for the field studies with a large sample size. Many researchers have estimated muscle size by these tools (Amara et al.

2003, Bamman et al. 2000, Baumgartner et al. 1992, de Koning et al. 1986, Heymsfield et al.

1982, Jones and Pearson 1969, Katch and Hortobagyi 1990, Knapik et al. 1996, Lee et al. 2000, Overend et al. 1993, Rice et al. 1990, Tothill and Stewart 2002). Of them, the reports on the correlation coefficients between estimated and measured muscle CSA with their statistical power confirmed in accordance with the report of Cohen (1988) are summarized in Table 1-1. The

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results of these studies appear to have sufficient statistical power. However, there is a problem that the use of them overestimates muscle and bone size due to an underestimation of skin and subcutaneous tissue size (Baumgartner et al. 1992, de Koning et al. 1986, Heymsfield et al. 1982, Rice et al. 1990). Therefore, it is difficult to precisely estimate muscle size only by these tools.

As stated above, although the ultrasonography, a measuring tape and/or a skinfold caliper can be used to assess muscle CSA, single application of any one of them causes various problems. For example, the validity of the square of muscle thickness determined by ultrasonography as the muscle CSA index appears to be dependent on the architecture of the examined muscles because the squared value of muscle thickness does not reflect muscle width.

Consequently, there is still room for improvement of muscle CSA index. In prior studies (Fukunaga et al. 2001, Miyatani et al. 2004), combining muscle thickness measured by ultrasonography with morphometric values obtained by a measuring tape improved the accuracy of estimating muscle volume compared with only muscle thickness. This suggests that the combination of them is able to more precisely evaluate muscle size than using only one measure.

In addition, this combination may overcome the aforementioned concern for ultrasonography that the image size cannot cover the whole section of the muscle of interest in many cases.

Therefore, an index determined by this combination seems to be useful for evaluating muscle CSA.

1-3-2. Relationship between muscle CSA and strength

Importance of muscle CSA for examining muscle size-strength relationship

It is well known that muscle size is related to muscle strength. In a prior study (Bamman et al. 2000), body weight, total body lean mass, lower leg lean mass, maximum circumference of lower thigh, muscle+bone CSA estimated by a measuring tape and a skinfold caliper, muscle

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CSA (including PCSA) and muscle volume were used as indices of muscle size and their relations to plantar flexor maximum voluntary strength were examined. As a result, they suggested that muscle CSA was the most appropriate variable for assessing muscle size if one is to assess the muscle size-strength relationship and/or the muscle strength per size. Hence, the determination of muscle CSA appears to be very important to examine the muscle size-strength relationship.

Relationship between muscle CSA and strength

In 1968, by the use of ultrasonography, Ikai and Fukunaga found that muscle strength was fairly proportional to muscle CSA in vivo in young adults and that the strength per muscle CSA was nearly the same in male and female regardless of age. Afterward, many researchers examined the relationships between muscle CSA and strength in young adults by means of MRI (Bamman et al. 2000, Fukunaga et al. 1996, 2001, Kent-Braun and Ng 1999), CT (de Koning et al. 1986, Maughan et al. 1983, Maughan and Nimmo 1984, Miller et al. 1993, Nygaard et al.

1983, Overend et al. 1992b), ultrasonography (Kanehisa et al. 1994a, Young et al. 1984) and combination of a measuring tape and a skinfold caliper (Bamman et al. 2000, de Koning et al.

1986). In addition, muscle PCSA was found to be related to strength in young adults (Bamman et al. 2000, Fukunaga et al. 1996, 2001, Klein et al. 2001).

It has been investigated how the relationship between muscle CSA and strength changes with aging. Age-related declines in muscle strength (including joint torque) (Larsson et al. 1979, Lindle et al. 1997, Lynch et al. 1999, Vandervoort and McComas 1986) and/or size (Janssen et al.

2000) were found to start at about the 5th decade of life. However, its decline in muscle size was not always found to be accompanied by that in muscle strength (MacLennan et al. 1980, Metter et al. 1999). Given that the changes in muscle CSA induced by body mass reduction (Katch and Hortobagyi 1990) or resistance training (Narici et al. 1989, 1996b) differ in different sites of the

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limb, the decrease in the muscle CSA induced by that in muscle size must also differ in different sites of the limb. Consequently, the age-related decline in muscle CSA would not correspond with that in muscle strength. These phenomena suggest that there would be a weaker relationship between muscle CSA and strength in middle-aged and elderly individuals aged 50 or over compared with that in young adults. Nevertheless, it has been reported that muscle CSA is related to muscle strength in middle-aged and elderly individuals (Amara et al. 2003, Kent-Braun and Ng 1999, Sipila and Suominen 1991, Overend et al. 1992b, Young et al. 1984, 1985) as well as in young adults. Furthermore, the relationships between PCSA and strength for elbow flexor and extensor muscles in each of young and elderly men were shown by Klein et al. (2001).

Of the aforementioned studies, the correlation coefficients between muscle CSA (including PCSA) and isometric muscle strength and their statistical power are summarized in Table 1-2 (young adults) and Table 1-3 (elderly individuals), respectively. The power values for many of the studies were higher than 0.80 regardless of age. Thus, many of the correlation coefficients appear to have sufficient statistical power.

Differences in the ratio of muscle strength to CSA among prior studies

Based on the fact that muscle strength is fairly proportional to muscle CSA, the ratio of muscle strength to CSA has been evaluated as the specific tension and/or its index. Prior studies (Close 1972, Powell et al. 1984, Spector et al. 1980, Witzmann et al. 1983) have indicated that the value of specific tension is nearly equal among variety of mammalian muscles. However, the ratio of muscle strength to CSA was reportedly to vary considerably among individuals in vivo (Maughan et al. 1983, Maughan and Nimmo 1984). As explainable reasons for the large interindividual variation in the ratio of muscle strength to CSA 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.

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On the other hand, changes in this ratio with aging have been observed in many studies so far. Nevertheless, previous findings on the age-related difference in the ratio of muscle strength to CSA (including PCSA) are still in controversy. Some researchers (Bruce et al. 1989, Klein et al. 2001, Morse et al. 2005a, Toji and Kaneko 2007) have reported that the ratio for young adults is higher than that for middle-aged and elderly individuals, but others (Kent-Braun and Ng 1999, Overend et al. 1992b, Young et al. 1984) have failed to find the corresponding difference. As an explanation for the discrepancy, Klein et al. (2001) pointed out some differences in the methods used to measure muscle CSA among the prior studies. For example, muscle CSA may have been overestimated in elderly people because of the difficulty in distinguishing the muscle from the noncontractile tissue surrounding the muscle (Bruce et al.

1989, Toji and Kaneko 2007). If so, the ratio of muscle strength to CSA for elderly individuals would be underestimated and be lower than that for young adults. Furthermore, some researchers (Kent-Braun and Ng 1999, Overend et al. 1992b, Young et al. 1984) measured ACSA and others (Klein et al. 2001, Morse et al. 2005a) calculated PCSA. These methodological differences among prior studies in measuring muscle CSA could be a reason that previous findings on the age-related change in the value of muscle strength per CSA are still in controversy. In addition, they might also explain its large interindividual variation.

Thus, determination of muscle CSA is important to assess its relation to muscle strength and the ratio of muscle strength to CSA. Indices of muscle CSA determined by ultrasonography and/or a measuring tape are useful for the field studies with a large sample size. Consequently, muscle CSA has often been estimated using these techniques. Nevertheless, the relationship between these indices and isometric muscle strength were examined in limited studies (Bamman et al. 2000, de Koning et al. 1986). Judging from the results reported by Bamman et al. (2000), the accuracy of existing indices of muscle CSA measured by these techniques may not be

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sufficiently high for examining their relations to muscle strength compared with muscle CSA determined by MRI and/or CT. Hence, it is essential to develop a more precise muscle CSA index and to examine its relation to muscle strength. Such an index of muscle CSA is also useful to conveniently evaluate muscle strength per size. If such a muscle CSA index is established, the index could be used to assess the ratio of muscle strength to CSA index more accurately. In doing so, more detailed information on the aforementioned discrepancies will be obtained.

1-3-3. Changes in muscle architecture during isometric contraction

Quantification of muscle architecture during isometric contraction by means of ultrasonography In many prior studies, changes in muscle architecture such as pennation angle (Fukunaga et al. 1997, Ito et al. 1998, Narici et al. 1996a, Reeves and Narici 2003), fascicle length (Fukunaga et al. 1997, Ito et al. 1998, Narici et al. 1996a, Reeves and Narici 2003) and moment arm of a muscle (Ito et al. 2000) induced by isometric contraction were measured in vivo using ultrasonography which provided a high time resolution. It is clear that their changes influence muscle strength. Thus, the measurement of muscle architecture during contraction is important to properly evaluate muscle strength.

On the other hand, some researchers (Hodges et al. 2003, Montes 2001, Shi et al. 2008) found that the thickness of parallel-fibered muscles increased during isometric contraction. This suggests that contraction of parallel-fibered muscles results in an increase in their CSA at the measurement site. Given that the highest thickness is observed during MVC (Shi et al. 2008), their CSA would also be the greatest during MVC. As stated above, contraction-induced change in muscle architecture influences muscle strength. Therefore, muscle CSA during contraction, especially during MVC, should be determined in order to examine the muscle CSA-strength relationship.

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Quantification of muscle architecture during isometric contraction by means of MRI

Recently, muscle architecture during isometric contraction was determined using MRI (Finni et al. 2003a, 2003b, 2006, 2008, Hodgson et al. 2006, Kinugasa et al. 2008, Maganaris et al. 1998, Pappas et al. 2002). The forte of MRI is that it can cover the wider section of the muscle of interest as compared with ultrasonography. Consequently, the shape and the site difference in architecture of the muscle of interest can be examined by using MRI. However, the scan time when subjects continue exertion at maximal effort is not sufficient to obtain analyzable images. Thus, the determination of muscle architecture during MVC by means of MRI may not be practical. In all of these reports except the report of Maganaris et al. (1998), therefore, muscle architecture was presumably measured under submaximal contraction.

The MRI provides precise muscle CSA. At present, however, determination of muscle CSA during MVC by means of MRI appears to be difficult. Consequently, muscle CSA during MVC should be evaluated using other techniques such as ultrasonography and/or a measuring tape which make it possible to evaluate muscle dimensional changes during contraction. In other words, an index determined by them for assessing muscle CSA not only at rest but also during MVC is needed. In prior reports (Hodges et al. 2003, Shi et al. 2008), an increase in the thickness of elbow flexor muscles induced by isometric contraction was observed. This suggests that contraction of such muscles induces an increase in their CSA, and correspondingly the increase in the CSA of contractile component relative to the muscle CSA index at a measurement site.

Given that the highest thickness is observed during MVC (Shi et al. 2008), it is likely that the muscle CSA index during MVC rather than at rest should be used, when one aims to properly examine the relationship between muscle CSA index and strength.

The quantification of changes in muscle thickness and width induced by contraction is important to establish the new index of muscle CSA since muscle cross-section involves both

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muscle thickness and width. Nevertheless, the contraction-induced change in width of parallel-fibered muscles has not been measured in vivo. Even in a submaximal contracted condition, therefore, the changes in muscle thickness and width should be measured in order to introduce the new muscle CSA index.

1-4. Approach to the problems

As described in the Review of literature, there is still room for improvement of muscle CSA index. Considering that combining muscle thickness measured by ultrasonography and morphometric values obtained by a measuring tape improves the accuracy of estimating muscle volume (Fukunaga et al. 2001, Miyatani et al. 2004), an index determined by combination of them seems to be useful for evaluating muscle CSA. Muscle cross-section involves both thickness and width. Although circumference of a limb contains other tissues besides the muscle, it should reflect muscle dimensions including both muscle thickness and width. Since the muscle CSA is a function of length to the second power, it is hypothesized that the product of muscle thickness and circumference of a limb can be an index for estimating muscle CSA. Moreover, it is expected that this index is able to evaluate muscle CSA during contraction because ultrasonography and a measuring tape make it possible to evaluate muscle dimensional changes during contraction owing to their real-time measurements. To examine whether the new index is useful for assessing muscle CSA both at rest and during MVC, the changes in muscle thickness and width induced by contraction need to be quantified. However, its change in width of parallel-fibered muscles has not been measured in vivo. Even in a submaximal contracted condition, therefore, the changes in not only muscle thickness but also its width should be determined.

As a factor capable of influencing the increase in the thickness of elbow flexor muscles induced by contraction, the elongation of a tendon during contraction has been considered

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(Hodges et al. 2003). Given that a muscle connects to a bone through a tendon, muscle shape and/or its difference between at rest and during contraction may be affected by tendon characteristics. Tendon stiffness decreases with aging (Kubo et al. 2003b, Onambélé et al. 2007, Reeves 2006). Therefore, 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, the relationship between muscle CSA index during contraction and strength should be performed not only in young adults but also in middle-aged and elderly individuals. Examining the relationships will result in more detailed information on age-related effect on the ratio of muscle strength to CSA and/or the large interindividual variation in its ratio of human skeletal muscle.

1-5. Purpose

The general purposes of this thesis are 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, this thesis aims 1) to examine how the muscle cross-section changes during submaximal contraction (Chapter 2), 2) to establish the new index for assessing muscle CSA not only at rest but also during contraction (Chapter 3), and 3) to examine how the muscle CSA indices determined both at rest and during MVC are related to muscle strength (Chapter 3 and Chapter 4). The outlines of each chapter are as follows.

In Chapter 2, using MRI, muscle cross-sections were determined both at rest and during submaximal contraction in young men. The changes in muscle CSA, thickness and width were compared between both conditions.

In Chapter 3, a new muscle CSA index determined by ultrasonography and a measuring tape was

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established and its validity was investigated through a comparison with muscle CSA measured by MRI. Then, the relationships between each new index of muscle CSA determined at rest and during maximal isometric contraction and muscle strength were examined in young adults.

In Chapter 4, the relationships between each new index of muscle CSA determined at rest and during maximal isometric contraction and muscle strength were examined in middle-aged and elderly individuals.

In Chapter 5, the main findings of each chapter were firstly described. Secondly, the effects of contraction-induced change in muscle shape on the accuracy of muscle CSA index were discussed. Thirdly, new explanation for the ratio of muscle strength to CSA obtained from this thesis was argued. Lastly, several factors that might affect the interpretation of the present results were addressed.

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Table 1-1 Correlation coefficients between estimated and measured muscle cross-sectional area in prior studies. MethodsReferencesSubjectsExamined musclesCorrelation coefficientsPower upper arm0.69 (P < 0.05)> 0.90 thigh0.43 (P < 0.05)> 0.50 de Koning et al. (1986)10 men & 8 women (20-50 yr) right & left upper arm (i.e., n = 36)0.96> 0.99 31 men (20-70 yr)0.92 (P < 0.001)> 0.99 20 women (20-70 yr)0.94 (P < 0.001)> 0.99 9 men (21.0 ± 2.3 yr)0.87> 0.80 9 women (25.2 ± 5.5 yr)0.77> 0.60 9 men & 9 women (combined)0.96> 0.99 13 men (19-34 yr)0.91> 0.99 11 men (65-77 yr)0.89> 0.90 upper arm0.91> 0.90 thigh0.99> 0.90 upper arm0.83> 0.95 thigh0.74> 0.80 Tothill & Stewart (2002)8 men & 2 women (23-49 yr)thigh (5 sites; i.e., n = 50)0.94> 0.99 Knapik et al. (1996) Overend et al. (1993)

measuring tape & skinfold caliper

upper arm thigh thigh

Baumgartner et al. (1992)8 men & 17 women (68-92 yr) Rice et al. (1990)

7 men (25-38 yr) 13 men (65-90 yr)

Heymsfield et al. (1982)

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Table 1-2 Correlation coefficients between muscle CSA and isometric muscle strength in prior studiesfor young adults. CSA,cross-sectionalarea;ACSA,anatomicalCSA;PCSA,physiologicalCSA;MRI,magneticresonanceimaging; CT, computed tomography.

MethodsReferencesSubjectsExamined musclesCorrelation coefficientsPower ACSA: 0.733> 0.99 PCSA: 0.715> 0.99 dorsiflexorsACSA: 0.77> 0.50 ACSA: 0.79> 0.50 PCSA: 0.92> 0.95 ACSA: 0.89> 0.99 PCSA: 0.91> 0.99 ACSA: 0.71> 0.95 PCSA: 0.95> 0.99 Kent-Braun & Ng (1999)12 men & 12 women (25-44 yr)dorsiflexors0.77 (P < 0.001)> 0.95 elbow extensorsPCSA: 0.73> 0.80 elbow flexorsPCSA: 0.75> 0.80 de Koning et al. (1986)10 men & 8 women (20-50 yr)elbow flexors0.89 (P < 0.001)> 0.99 25 men (20-38 yr)0.59 (P < 0.01)> 0.75 25 women (20-36 yr)0.51 (P < 0.01)> 0.75 Maughan & Nimmo (1984)15 men (22-42 yr)knee extensors0.70> 0.85 Nygaard et al. (1983)4 men & 3 women (28-43 yr)elbow flexors0.75 (P < 0.05)> 0.50 Overend et al. (1992b)13 men (19-34 yr)knee extensors0.829 (P < 0.001)> 0.95 ultrasonographyYoung et al. (1984)25 women (20-29 yr)knee extensors0.53 (P < 0.01)> 0.75 Bamman et al. (2000)39 women (24-50 yr)plantar flexors0.447> 0.70 de Koning et al. (1986)10 men & 8 women (20-50 yr)elbow flexors0.90 (P < 0.001)> 0.99

knee extensors

MRI CT

Maughan et al. (1983)

12 men (20-29 yr)Klein et al. (2001)

Bamman et al. (2000) measuring tape & skinfold caliper

39 women (24-50 yr)plantar flexors elbow flexors

elbow extensors 26 men (25.7 ± 2.9 yr)Fukunaga et al. (2001)

plantar flexorsFukunaga et al. (1996)8 men (33.5 ± 9.4 yr)

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Table 1-3 Correlation coefficients between muscle CSA and isometric muscle strength in prior studies for elderly individuals. CSA, cross-sectional area; PCSA, physiological CSA; MRI, magnetic resonance imaging; CT, computed tomography.

MethodsReferencesSubjectsExamined musclesCorrelation coefficientsPower Kent-Braun and Ng (1999)12 men & 12 women (65-83 yr)dorsiflexors0.81 (P < 0.001)> 0.99 elbow extensorsPCSA: 0.74> 0.80 elbow flexorsPCSA: 0.83> 0.95 knee extensors0.667 (P = 0.025)> 0.60 knee flexors0.729 (P = 0.007)> 0.80 Young et al. (1984)25 women (71-81 yr)knee extensors0.66 (P < 0.001)> 0.90 Young et al. (1985)12 men (70-79 yr)knee extensors0.77 (P < 0.03)> 0.80 Sipila and Suominen (1991)32 men (> 70 yr)knee extensors0.488 (P < 0.01)> 0.60

ultrasonography

Overend et al. (1992b)12 men (65-77 yr)

13 men (76-95 yr)Klein et al. (2001)MRI CT

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Chapter 2 Quantification of muscle cross-sections during submaximal contraction in young men

2-1. Introduction

The thickness of elbow flexor muscles increases during contraction, and is maximal during isometric MVC (Shi et al. 2008). This suggests that MVC of elbow flexor muscles increases the CSA of contractile component at the measurement site. Hence, one can assume that a muscle CSA index during MVC rather than at rest properly should reflect muscle strength well, although little attention has been paid to the relationships between muscle strength and muscle CSA indices obtained for contracting muscles.

The MRI provides muscle CSA with satisfactory accuracy, but the scan time in the order of minutes will not allow a measurement of contracting muscles, especially during MVC. It is possible however to estimate muscle CSA during MVC when one uses an index of CSA with techniques that allow real-time measurement, such as ultrasonography for muscle thickness and a measuring tape for the circumference of the limb including the muscle. Feasibility of using these techniques to compare muscle CSA between at rest and during MVC depends on their ability to capture deformation of a muscle that occurs not only in the thickness but also in the width. To clarify this, one first needs to know how muscle deforms by contraction. However, the measurement of contraction-induced changes in the cross-sectional shape of elbow flexor muscles have not been attempted in vivo, even under submaximal contraction.

This study aimed to quantify deformation of elbow flexor muscles by obtaining muscle cross-sections both at rest and during submaximal contraction with MRI. Muscle deformation was evaluated with respect to CSA, thickness and width.

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2-2. Methods

Experimental design

The contraction-induced changes in cross-sections of the belly of elbow flexor muscles were observed using MRI. The CSA, thickness (the vertical distance from the upper end of the elbow flexor muscles to that of the humerus), height (the vertical distance from the upper to the lower end of the elbow flexor muscles), width (the horizontal distance from the left to the right end of the elbow flexor muscles) and the ratio of height to width (H/W) of the elbow flexor muscles, were quantified both at rest and during 30%MVC (Figure 2-1). In addition, the circumference at a level of 60% of the upper arm length (the distance from the acromial process of the scapula to the lateral epicondyle of the humerus), distal to the acromial process, was measured. An index of muscle CSA was calculated as a product of the thickness and circumference.

Subjects

Eleven young men volunteered as subjects. Their means (±standard deviations, SDs) in age, body height and mass were 22.8 (±2.0) yr, 172.2 (±5.1) cm and 62.8 (±5.9) kg, respectively.

All measurements were performed for the subjects’ right arms in which there was no orthopedic abnormality. This study was approved by the Ethical Committee of the Faculty of Sport Sciences of Waseda University and was consistent with their requirement for human experimentation.

Each subject was informed of the purpose and procedures of this study and possible risks of the measurements beforehand. Written informed consent was obtained from each subject.

Procedures

Measurement of MVC of isometric elbow joint flexion

Isometric elbow joint flexion torque was measured for each subject using a custom-made

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torque meter (VINE, Japan). This torque meter was made of acetal copolymer, vinyl chloride, acrylic and polyamide, all of which were nonmagnetic. A custom-made optical fiber (Shinko Electric Wire, Japan) was attached to the lever arm of the torque meter to record the strain around it with a fiber bragg grating sensor monitor (FB200, Yokogawa Electric, Japan), combined with an amplified spontaneous emission light source (ASE-1550-25, FiberLabs, Japan). The strain data were sent to a personal computer (VGN-SZ80PS, Sony, Japan) at 100 Hz for calculation of torque. Each subject was instructed to lay in a supine position and the right arm was secured to the torque meter by using a non-elastic belt, with the shoulder at 90˚ and the elbow at 80˚ (full extension = 0°), and the wrist fixed to the torque meter in a position halfway between supination and pronation (Figure 2-2). The subjects performed MVC of isometric elbow joint flexion for 3 seconds. The torque measurements were performed two times with at least a 2 min interval. If the difference between two values of torque was more than 10% of the higher one, the torque was measured one more time. In two or three torque measurements, the highest value was adopted.

Quantification of muscle cross-sections at rest and during 30%MVC

A series of cross-sectional images of the right arm were obtained using an MRI (Signa 1.5T, GE Medical Systems, USA) with a 5 inch round surface coil. Transverse scans were performed with a conventional T1-weighted Fast Spin-echo technique (a repetition time: 1300 ms, an echo time: 20 ms, a slice thickness: 10 mm, an interspaced distance: 0 mm). Imaging was carried out on a field of view of 16 × 16 cm with a 256 × 160 matrix. A marker was applied on the subjects’ skin surface at the level of 60% of the upper arm length. The level of 60% of the upper arm length was in the vicinity of the maximal CSA in the upper arm (Kanehisa et al.

1994b). Within the device, the subjects maintained the aforementioned postures and wore an MRI-compatible goggle (MRVision 2000, Resonance Technology, USA, with VisuaStim

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Digital’s Controller, Resonance Technology, USA) that displayed a screen of the computer of the torque meter system, in order to provide the subjects with a visual feedback on their contraction levels (Figure 2-2). Firstly, a series cross-sectional images of the right arm were scanned at rest.

Next, the same scanning was made while the subjects sustained 30%MVC of isometric elbow joint flexion for about 20 seconds. In each condition, the scan time was 18 seconds. In all scanned images, outlines of the elbow flexor muscles (biceps brachii, brachialis and brachioradialis) were digitized, and the series CSAs from the level of 60% of the upper arm length to that at 6 cm distal to it were measured using a personal computer (Compaq 6710b, Hewlett-Packard, USA), as well as the thickness, height, width and H/W. The circumference was determined using the personal computer only at the level of 60% of the upper arm length. Since the brachioradialis and the brachialis could not be separated precisely, the brachioradialis was traced as part of the elbow flexor muscles in this study. Each measurement was carried out one time by an experienced tester. For the image at the level of 60% of the upper arm length, the measurements of each variable were carried out twice to calculate the coefficient of variance (CV) of the two values for each variable (CSA, thickness, height, width, H/W and circumference), which was <1.4% with the intraclass correlation coefficients of >0.986.

Reproducibility of measurement variables

The measurement was repeated for 3 subjects on another day to ensure its reproducibility.

Table 2-1 summarizes the CVs and intraclass correlation coefficients of the variables. The CVs of the two measured values (CSA, thickness, height, width and H/W; 3 men × 7 measurement sites, circumference; 3 men × 1 measurement site) were <2.2 % and the intraclass correlation coefficients for them were >0.937.

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Statistical Analyses

Descriptive data are presented as means ± SDs. A two-way analysis of variance (ANOVA) (2 contraction levels × 7 measurement sites) with repeated measures was used to test the effects of the contraction level on variables other than the circumference. When the interaction between the two factors was found significant, a Student’s paired t-test was conducted in each measurement site to test the differences between at rest and during 30%MVC. A Student’s paired t-test was used to test the difference between the circumference at rest and that during 30%MVC. Pearson's product-moment correlation coefficients were calculated between the thickness and CSA as well as between the width and CSA, both at rest and during 30%MVC.

When their relationships were tested, the pooled data on the CSA, thickness and width obtained at all measurement sites (11 men × 7 measurement sites; n = 77) were used. In addition, the relationships between the product of thickness and circumference and muscle CSA as well as between the square of thickness and muscle CSA were examined by Pearson's product-moment correlation coefficients. In accordance with a prior report (Cohen and Cohen 1983), the differences in these correlation coefficients between contraction levels were tested. Statistical significance was set at P < 0.05.

2-3. Results

Figure 2-3 shows the CSA, thickness, height, width and H/W at each measurement site.

There were significant interactions between the contraction level and measurement site for each variable. From the level of 60% of the upper arm length to that at 4 cm distal to it, CSA was significantly higher during 30%MVC than at rest. At all measurement sites, the thickness, height and H/W during 30%MVC were significantly higher than those at rest. In contrast, the width during 30%MVC was significantly lower at each measurement site compared with that at rest.

The relationships between each of the thickness and width and the CSA are shown in

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Figure 2-4. In the both conditions, there were significant correlations between the thickness and CSA (rest: r = 0.714, P < 0.001; 30%MVC: r = 0.739, P < 0.001) and between the width and CSA (rest: r = 0.668, P < 0.001; 30%MVC: r = 0.627, P < 0.001).

The circumference at rest (28.1 ± 2.5 cm) was significantly smaller than that during 30%MVC (29.4 ± 2.6 cm). The relationships between each of the square of thickness and the product of thickness and circumference and the CSA are shown in Figure 2-5. In the rest condition, the CSA was significantly correlated with the product of thickness and circumference (r = 0.613, P < 0.05) but was not significantly correlated with the square of thickness (r = 0.517, P > 0.05). There was a significant difference between these correlation coefficients (P < 0.05).

During 30%MVC, there were significant correlations between the product of thickness and circumference and CSA (r = 0.843, P < 0.01) and between the square of thickness and CSA (r = 0.770, P < 0.01). The difference between these correlation coefficients was not significant.

2-4. Discussion

The values of CSA of the elbow flexor muscles during 30%MVC were significantly higher than those at rest in all levels from the 60% to 4 cm distal of the upper arm length (Figure 2-3). When the joint is fixed at a given angle, the muscle-tendon complex is constant in length.

However, the tendon is stretched during isometric contraction (Kubo et al. 1999) and consequently the muscle length is shortened. In the case of a parallel-fibered muscle, the shortening of muscle length results in an increase of muscle CSA because muscle volume does not change by contraction (Baskin and Paolini 1967). Thus, the greater CSA during contraction as compared with that at rest seems to be affected by the elongation of the tendon during contraction. Another possibility is the effect of gravity on muscle shape. A relaxed muscle is deformed by gravity due to its slackness. During contraction, stiffened muscle might resist gravity to maintain its shape, which could also influence different the CSA at rest and during

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30%MVC.

The thickness and height of the elbow flexor muscles during 30%MVC were significantly increased from at rest (Figure 2-3). This result supports the findings of prior studies that muscle thickness during contraction was higher than that at rest (Hodges et al. 2003, Shi et al. 2008). In contrast, the width of the elbow flexor muscles was significantly decreased during 30%MVC (Figure 2-3). In other words, muscle shape was changed longer in the vertical direction by contraction (Figure 2-3). Moreover, although the thickness was significantly higher during 30%MVC than at rest at all measurement sites, there was no difference in the values of CSA between the two conditions at the site 5 cm and 6 cm distal to the level of 60% of the upper arm length (Figure 2-3). This result indicates that the contraction-induced increase in muscle thickness does not always result in an increase in muscle CSA.

In each condition, the product of thickness and circumference was significantly correlated with the CSA (Figure 2-5). On the other hand, the square of thickness was not significantly correlated with the CSA at rest (Figure 2-5), and its correlation coefficient was significantly lower than that between the product of thickness and circumference and CSA. In a prior study (Martinson and Stokes 1991), the square of muscle thickness was highly correlated with muscle CSA as was the product of muscle thickness and width in the anterior tibial muscle.

However, as shown in Figure 2-4, muscle CSA is dependent on both muscle thickness and width, and correspondingly, the contraction-induced increase in muscle CSA cannot be explained thoroughly by that of thickness. Therefore, the product of thickness and circumference, the latter of which involves both muscle thickness and width, appears to be a more reasonable index for evaluating muscle CSA compared with the square of thickness.

In this study, muscle cross-sections during 30%MVC were measured. Since a muscle CSA index during MVC will be examined in the following chapter, changes in muscle cross-sections induced by higher levels of contraction should also be studied. In the report of Shi

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et al. (2008), a linear relationship between the contraction level and muscle thickness was observed. On the other hand, a previous study (Akagi 2005) showed that there was a nonlinear relationship between the contraction level and muscle thickness and muscle thickness during 50-60%MVC was not significantly different from that during MVC. As stated in the earlier part, the elongation of a tendon appears to affect the contraction-induced increase in muscle CSA.

Given that there is a nonlinear relationship between contraction level and tendon elongation, the relationship between contraction level and muscle thickness could also be nonlinear. To test this possibility, the muscle cross-sections during 50%MVC were taken in 4 out of 11 subjects. The result indicated that the variables during 30%MVC were comparable to those during 50%MVC (Figure 2-6). Therefore, changes in muscle cross-sections during from 30%MVC to MVC are expected to be smaller than those from at rest to during 30%MVC.

2-5. Summary

This study showed that the thickness of the elbow flexor muscles was increased and the width was decreased during submaximal contraction, indicating that the increase in muscle thickness was not always accompanied by that in its CSA. It is likely that the product of thickness and circumference is more appropriate to assess muscle CSA compared with the square of thickness.

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Width

Thi ckne ss He ig ht

Width

Thi cknes s Hei g ht

CSA

Figure 2-1 MRI images of cross-sections of elbow flexor muscles at rest (left) and during 30%MVC (right). MRI, magnetic resonance imaging; MVC, maximal voluntary contraction;

CSA, cross-sectional area.

新たな筋横断面積指標の確立 Establishing a new index of muscle cross-sectional area