Human Lower Limb Muscles: an Evaluation of Weight and Fiber Size

Okajimas Folia Anat. Jpn., 80(2–3): 47–56, August, 2003

Junji ITO, Hiroshi MORIYAMA, Seiichiro INOKUCHI and Noboru GOTO

Department of Anatomy, Showa University School of Medicine, Shinagawa-ku, Tokyo 142-8555, Japan

– Received for Publication, June 9, 2003 –

Key Words: Muscle ﬁber morphometry, Human lower limb, Muscle weight, Muscle ﬁber size

Summary: Morphological study of the lower limb muscles is necessary for the analysis of muscle function and its relation to the aging process. In this study, we measured the muscle weight and the muscle fiber morphometry (cross-sectional area and total number of muscle fibers at the muscular belly, and muscle fiber size) of the human lower limb in an adult Japanese cadaver (male, 58 years old). The results presented here can provide the normal control data to elucidate the aging process of the human lower limb muscles. The morphological features in the human lower limb muscles were the pronounced enlargement of the gluteus maximus in the hip, the vasti muscles in the thigh and the soleus in the leg.

The morphological features of the skeletal mus- versity School of Medicine. The cause of death did cles are in direct correlation with their function. not indicate the presence of neuro-muscular dis- Differences in weight, numbers and sizes of fibers in eases or diseases affecting the central nervous sys- each muscle depend on muscle activity. Therefore, tem. It must be added that the patient had not the analysis of such elements can be useful to ex- been reported to be bedridden prior to death. After plain muscular functions. There have been several measurement of the muscle weight, blocks of mus- reports on the greater weight of the gluteus max- cle were embedded in celloidin (Shiojirin, Showa imus, vasti and soleus muscles in comparison with Ether Co. Japan). They were then sliced into 20 mm the other muscles in the human lower limb (Ishida, thickandstainedwithhaematoxylinandeosin 1972; Ito, 1996; Ito et al., 1998). Measurement of (HE). We measured the cross-sectional areas and the muscle morphometry was conducted on several total numbers of muscle fibers at the muscular muscles in the lower limbs (Hasegawa, 1987; Ka- belly, as well as muscle fiber sizes. The total num- taoka, 1987; Oohara, 1991; Kobayashi, 1991). Data ber of muscle fibers in the muscle belly was calcu- on muscle weight and muscle fiber size in the lower lated by multiplying the cross-sectional area of the limbs from one single normal subject is indispens- transverse section through the muscular belly by able to elucidate the correlation between skeletal the number of muscle fibers per square millimeter. muscle morphology and function during the aging The muscle fiber size was calculated as the average process. However, such data have not been pub- transverse area of about 200 muscle fibers. The lished, as far as we know, although age-related shrinkage was about 8–9% in length (Shibata et al. changes have been observed on subjects aged 60 1996). years and over (Kimura et al. 2002). This study is the first to have been carried out on a 58 years-old subject. Results

The muscle weight and muscle ﬁber composition Material and Methods areshowninTables1and2.

Muscle samples were obtained from the right Muscle weight (Fig. 1): lower limb of a Japanese male cadaver (58 years The gluteus maximus showed the largest weight old) at the anatomical laboratory of Showa Uni- (573.4 g) and the plantaris the smallest (3.2 g). The

47 48 J. Ito et al.

Table 1. Weight of muscles in the human lower limb nus (1,403,084), the gluteus medius (1,302,085) and the vastus medialis (1,006,500). The plantaris Muscles Weight (g) (81,013) was the smallest in number. M. iliopsoas 159.3 M. gluteus maximus 573.4 M. gluteus medius 251.7 Muscle fiber size (Fig. 4): 2 M. gluteus minimus 85.1 The soleus (2,669.9 mm ) was the largest (Fig. M. tensor fasciae latae 50.9 5A), followed by the adductor magnus (2,219.8 mm2). M. piriformis 20.4 The gracilis (487.0 mm2) was the smallest (Fig. 5C). M. obturatorius internus 31.7 The gluteus maximus (992.9 mm2) was moderate Mm. gemellis 8.7 2 M. quadratus femoris 34.5 (Fig. 5B) and the iliopsoas (508.9 mm )wasrather ------small. The quadricep muscles were relatively large. M. sartorius 96.8 The biceps femoris long head (1,620.6 mm2)andthe M. rectus femoris 114.8 semimenbranosus (1,255.7 mm2) were larger com- M. vastus lateralis 320.5 pared to the other hamstring muscles. M. vastus intermedius 182.7 M. vastus medialis 230.3 M. pectineus 30.9 M. adductor longus 86.6 M. adductor brevis 71.2 Discussion M. adductor magnus 452.6 M. gracilis 53.0 Age-related decrease of the number of muscle M. obturatorius externus 35.1 fibers and their size in the tibialis anterior has been M. biceps femoris caput longum 115.8 observed in subjects aged 60 years and over (Ki- M. biceps femoris caput breve 57.1 M. semitendinosus 97.5 mura et al. 2002). In this study, we measured muscle M. semimembranosus 114.7 weight and muscle fiber size in a 58-year-old sub------ject. Therefore, the present results can provide M. tibialis anterior 71.7 normal control data on the muscle fiber size to elu- M. extensor digitorum longus 34.2 cidate the aging process and functional recovery of M. extensor hallucis longus 15.7 M. peroneus longus 36.8 human lower limb muscles. M. peroneus brevis 17.2 The principle characteristic of human locomo- M. gastrocnemius 139.3 tion is erect bipedalism and the muscle activity M. soleus 210.5 patterns during bipedal walking have been repre- M. plantaris 3.2 sented in electromyographic studies (Basmajian, M. popliteus 16.1 M. tibialis posterior 72.4 1985; Stern, 1988). Muscles with larger mass and M. flexor digitorum longus 14.5 fiber size play the most important role in joint M. flexor hallucis longus 35.3 movements. In the gluteal muscles, the gluteus medius and minimus are used during most of the stance phase; the gluteus maximus is used very little during that largest muscle in each segment was the gluteus phase (or, indeed, during the whole walking pro- maximus in the hip muscles, the adductor magnus cess). These activities are reflected in the smaller (452.6 g) in the thigh muscles and the soleus muscle fiber size of the gluteus maximus, compared (210.5 g) in the leg muscles. to that of the gluteus medius and minimus. The iliopsoas acts to produce the flexion of the Cross-sectional area at the muscular belly (Fig. 2): hip joint needed to bring the swinging limb for- The gluteus maximus (4,842.0 mm2)wasthe ward. This action does not seem to need a powerful largest, followed in decreasing order by the ad- force, because, as mentioned above, the iliopsoas ductor magnus (2,687.9 mm2), the vastus medialis muscle fibers are relatively small in size. This had (1,650.0 mm2), the gluteus medius (1,489.8 mm2), also been reported earlier (Hasegawa, 1987). the vastus lateralis (1,246.0 mm2) and the soleus The vasti muscles act during the early part of the (1,195.8 mm2). The plantaris (59.7 mm2)wasthe stance phase to prevent knee flexion. At this phase, smallest. the hip joint enacts the extension movement but the rectus femoris does not contribute to it. Those two Total number of muscle fibers at the muscular belly actions are mirrored in the fiber size of the muscles: (Fig. 3): large for vasti muscles, which are one-joint muscles, The gluteus maximus (4,110,858) had the most, and smaller for the rectus femoris, which is a two- followed in decreasing order by the adductor mag- joint muscle (Kobayashi, 1991). Human Lower Limb Muscles 49

Table 2. Morphometry of human lower limb muscle ﬁbers

Muscles Cross sectional Number Total Size (mm2) area (mm2) per mm2 number mean G SD

M. iliopsoas 831.8 1553 1180732 508.9 227.72 M. gluteus maximus 4842.0 849 4110858 992.9 314.22 M. gluteus medius 1489.8 874 1302085 1029.1 425.19 M. gluteus minimus 976.3 540 527202 1427.7 508.01 M. tensor fasciae latae 334.6 739 247269 1039.0 213.72 M. piriformis 321.3 636 204347 1043.2 433.99 M. obturatorius internus 514.4 1263 649687 637.1 232.09 Mm. gemellis 99.2 770 76384 867.1 380.85 M. quadratus femoris 606.6 324 196538 2127.0 598.32 ------M. sartorius 183.0 1483 271389 568.5 234.35 M. rectus femoris 493.1 697 343691 1125.1 353.04 M. vastus lateralis 1246.0 640 797440 1280.5 465.77 M. vastus intermedius 928.4 450 417780 1322.5 456.66 M. vastus medialis 1650.0 610 1006500 1856.1 575.19 M. pectineus 246.4 1535 378224 543.7 139.19 M.adductorlongus 455.1 1335 607559 615.1 229.90 M. adductor brevis 547.3 1240 678652 698.6 223.48 M. adductor magnus 2687.9 522 1403084 2219.8 1223.48 M. gracilis 212.2 1763 374109 487.0 137.61 M. obturatorius externus 336.2 1236 415543 573.2 168.79 M. biceps femoris caput longu 574.4 447 256757 1620.6 707.74 M. biceps femoris caput breve 302.7 1099 332667 772.2 283.97 M. semitendinosus 452.9 1428 646741 613.4 194.76 M. semimembranosus 567.4 603 342142 1255.7 482.76 ------M. tibialis anterior 366.6 954 349736 860.0 225.52 M. extensor digitorum longus 150.8 1192 179754 682.2 177.04 M. extensor hallucis longus 105.4 904 95282 890.4 239.06 M. peroneus longus 235.6 904 212982 844.6 307.06 M. peroneus brevis 95.8 921 88232 758.9 254.63 M. gastrocnemius 937.3 877 822012 971.1 457.23 M. soleus 1195.8 288 344390 2669.9 769.36 M. plantaris 59.7 1357 81013 614.3 221.95 M. popliteus 202.8 1025 207870 714.3 201.69 M. tibialis posterior 291.8 478 139480 1478.7 395.57 M. ﬂexor digitorum longus 122.7 940 115338 868.2 231.90 M. ﬂexor hallucis longus 229.9 726 166907 1148.9 355.38

The hamstring muscles act, along with the glu- functional muscle for plantarflexion at the ankle. teus maximus, to prevent the forward momentum As for the tibialis anterior, it functions as a dor- of the trunk at the hip joint. The biceps femoris siflexor during the swing phase. The load during the (long head) and semimembranosus were largest of dorsiflexion phase is only the weight of the foot. the hamstrings (Oohara, 1991). This is consistent Powerful force is therefore not required, and the with their important contribution to the act of muscle fiber size in the tibialis anterior is moderate. walking. However, it is considered that, in spite of its mod- The triceps surae activate the plantarflexion of erate fiber size, degeneration of the tibialis anterior the ankle during the latter half of the stance phase, causes stumbling during walking. and need powerful force to exert antigravity against This morphometric data contributes to the de- body weight. Among these, the soleus showed the velopment for further research in the field of kine- largest muscle fiber size, as befits its role as the main siology and myology. 50 J. Ito et al.

Fig. 1. Weight of human lower limb muscles (g). Human Lower Limb Muscles 51

Fig. 2. Cross-sectional area at the muscular belly of the human lower limb muscles (mm2). 52 J. Ito et al.

Fig. 3. Total number of muscle ﬁbers at the muscular belly of the human lower limb (1,000). Human Lower Limb Muscles 53

Fig. 4. Muscle ﬁber size of the human lower limb (mm2). 54 J. Ito et al.

Fig. 5. Transverse sections of the soleus (A), gluteus maximus (B) and gracilis (C). HE stain, bar ¼ 50 mm. Human Lower Limb Muscles 55

References 6) Oohara K. Myofibrous organization in human hamstring muscles. J Showa Med Assoc 1991; 51:151–158. (in Japa- 1) Ishida H. On the muscular composition of lower extrem- nese with English summary) ities of apes based on the relative weight. J Anthrop Soc 7) Kobayashi K. Myofibrous organization in human quad- Nippon 1972; 80:125–145. (in Japanese with English sum- riceps femoris muscles. J Showa Med Assoc 1991; 51:186– mary) 196. (in Japanese with English summary) 2) Ito J. Morphological analysis of the human lower extremity 8) Kimura T, Hamai K and Shiraishi Y. Age-related func- based on the relative muscle weight. Okajimas Folia Anat tional and morphological changes in the anterior tibial Jpn 1996; 73:247–252. muscle of men: Muscular atrophy and decrease in the 3) Ito J, Shiraishi N, Umino M, Kimura T and Akita H. Mor- number of muscle fibers. Anthropological Science 2002; phological evaluation of the baboon hind limb muscles 110:403–413. based on relative weight. Okajimas Folia Anat Jpn 2000; 9) Shibata M, Suzuki M and Goto N. A new embedding ma- 77:161–166. terial for morphometry: Shiojirin E-10. Acta Anat Nippon 4) Hasegawa M. On the myofibrous organization of human 1996; 71:656–661. (in Japanese with English summary) iliopsoas muscle (psoas major muscle and iliacus muscle). 10) Basmajian JV. Human locomotion. In: Basmajian JV, ed, J Showa Med Assoc 1987; 47:833–842. (in Japanese with Muscles Alive. Baltimore, Williams & Wilkins, 1985; 367– English summary) 388. 5) Kataoka J. Comparative studies on muscle structure of 11) Stern JT Jr. Use of lower limb muscles in walking. In: Stern the m. triceps surae and m. plantaris in man and monkey. JT Jr. ed, Essentials of Gross Anatomy. Philadelphia, F.A. J Showa Med Assoc 1987; 47:851–861. (in Japanese with DAVIS, 1988; 704–711. English summary)