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What determines the muscle cross-sectional area?
Journal of the Neurological Sciences, I l l (1992) 113-114 © 1992 Elsevier Science Publishers B.V. All rights reserved 0022-510X/92/$05.00
113
JNS 03823
Letters to the Editor
What determines the muscle cross-sectional area? J a n Lexell a a n d D a v i d D o w n h a m b ,i Department of Neurology, University of Umea, Umea, Sweden, and b Department of Statistics & Computational Mathematics, University of Liverpoo~ Liverpool, UK (Received 17 January, 1992) (Accepted 21 March, 1992)
It is widely accepted that the maximum force produced by a muscle is directly proportional to its crosssectional area (Knuttgen 1976; Young et al. 1981; Maughan et al., 1983; Sale et al. 1987). The relationship between the muscle area and the fibre type composition, assessed as the area and proportion of the different fibre types, is on the other hand far from clear (Hiiggmark et ai. 1978; Tesch and Karlsson 1978; Schantz et al. 1983; Maughan 1984; Ryushi et al. 1988). Recent developments of preparative techniques now enable us to study the fine structure of whole human skeletal muscle, thereby eliminating some of the technical constraints previously involved in the analysis of the muscle fibre composition. We have reanalysed data, obtained from whole muscle cross-sections (Lexell et al. 1988), on muscle area, total number, size and proportion of the different fibre types and looked closer into the relationship between these variables, to identify determinants of the size of human muscle. The vastus lateralis muscle from the right leg of 31 previously healthy men, 15-83 years of age, was extirpated less than 3 days post mortem. A slice, about I0 ram, was cut from each muscle half way between the origin and the insertion. Thin cross-sections ( 1 5 / t m ) were cut and stained for myofibrillar adenosine triphosphatase (mATPase) at pH 10.4 to visualize type I and type 2 fibres. The numbers of type I and type 2 fibres were counted within every 48th mm 2 (6 × 8) throughout the muscle cross-section, and were used to estimate the proportion of type 1 fibres, P, in the muscle cross-section. The mean cross-sectional area (mm 2) of the mus-
Correspondence to: Dr. J. Lexell, Department of Neurology, University of Ume~i, S-90185 Ume~, Sweden. Tel.: (+ 46) 90 l0 28 26; Fax: (+46) 90 14 31 07.
cle, A, was estimated by multiplying the number of systematically sampled quadrats by 48. The total number of fibres in the muscle cross-section was estimated by multiplying A by the mean number of fibres per mm 2. The mean cross-sectional areas (/~m2) of type 1 and type 2 fibres, S~ and S 2, respectively, were calculated from measurements of the area of a total of 125 fibres of each type, from five different regions throughout the muscle cross-section. The mean fibre area for the muscle cross-section was estimated by S ffi P x S~ + ( l - P ) x S 2, and the proportion of the fibre area in the muscle cross-section occupied by type 2 fibres was estimated by A 2 -- ( l - P ) × $2/S. The summary statistics and linear regression procedures of the statistical package SAS (SAS Institute Inc., U.S.A.) were used for the calculations and analyses. The muscle area, A, was regressed on the five variables T, St, $2, P and A 2. The effect of each of these variables was assessed in terms of an F-statistic and its associated significance level. The scattergrams of T, S t, S2P and A 2 with A are present in Fig. la-d. The results of the single regression analyses - the regression line, the correlation coefficient (r) and the significance level - are included in each graph. The relationship between A and T was significant at the 0.1% level (Fig. la), and the relationship between A and S 2 was significant at the 1% level (Fig. lb). There was no significant relationship between A and S I (Fig. lb), nor between A and P (Fig. lc). The relationship between A and A 2 was significant at the 0.1% level (Fig. ld). The correlation between muscle area and total number of fibres is stronger than that between muscle area and any of the other variables. This implies that the total number of fibres has the greatest influence on muscle area. The mean fibre area has been shown to be significantly correlated with the muscle area (Lexell et ai. 1988). Figure lb shows that this is accounted for
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Fig. 1. Relationship between muscle cross-sectional area and (a) total number of fibres, (b) mean area of type 1 fibres and type 2 fibres, (c) proportion of type I fibres, and (d) relative area of type 2 fibres. The regression line, the correlation coefficient (r) and the significance level are included in each graph.
exclusively by the mean type 2 fibre area. The fibre type proportion appears not to influence the muscle area. Thus, the fibre number and only the area of type 2 fibres are influencing the muscle area. When the proportion and the mean area of type 2 fibres were combined to form A 2 - the relative type 2 fibre area - and regressed against muscle area, the relationship was stronger than the two individual relationships, as reflected in the values of the correlation coefficients: 0.51, -0.27 and 0.59. This indicates that the proportion of the fibre area in the muscle crosssection occupied by type 2 fibres significantly influences the size of the muscle, so that both the size and the number of type 2 fibres are important in determining the muscle area. Thus, the cross-sectional area of the vastus lateralis muscle is mainly determined by the total number of fibres, and to a lesser extent by the size and~or the number of type 2 fibres. This complex relationship can explain some of the conflicts in the literature. References H~iggmark, T., E. Jansson and B. Svane (1978) Cross-sectional area of the thigh muscle in man measured by computet tomography. Scand. J. Clin. Lab. Invest., 38: 355-360.
Knuttgen, H.G. (1976) Development of muscular strength and endurance. In: H.G. Knuttgen (Ed.), Neuromuscular Mechanisms for Therapeutic and Conditioning Exercise, University Park Press, Baltimore, MD, pp. 97-118. Lexell, J,, C.C. Taylor and M. Sj6str(im (1988) What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in whole vastus lateralis from 15- to 83.year-old men. J. Neurol. Sci., 84: 275-294. Maughan, RJ. and M.A. Nimmo (1984) The influence of variations in muscle fibre composition on muscle strength and cross-sectional area in untrained males. J. Physiol., 351: 299-311. Maughan, RJ., J.S. Watson and J. Weir (1983) Strength and crosssectional area of human skeletal muscle, J. Physiol., 338: 37-49. Ryushi, T., K. Hiikkinen, H. Kauhanen and P.V. Komi (1988) Muscle fiber characteristics, muscle cross-sectional area and force production in strength athletes, physically active males and females. Scand. J. Sports Sci., 10: 7-15. Sale, D.G., J.D. MacDougall, S.E. Always and J.R. Sutton (1987) Voluntary strength and muscle characteristics in untrained men and women and male hodybuilders. J. AppI. Physiol., 62: 17861793. Schantz, P., E. Randall-Fox, W. Hutchinson, A. Tyd~n and P.-O. ,~,strand (1983) Muscle fibre type distribution, muscle cross-seetional area and maximal voluntary strength in humans. Acta Physiol. Seand., 117, 219-226. Tesch, P. and J. Karlsson (1978) Isometric strength performance and muscle fibre type distribution in man. Acta Physiol. Scand., 103: 47-51. Young, A., M. Stokes, I.C.R. Walker and D. Newham (1981) The relationship between quadriceps size and strength in normal young adults. Ann. Rheum. Dis., 40: 619.
113
JNS 03823
Letters to the Editor
What determines the muscle cross-sectional area? J a n Lexell a a n d D a v i d D o w n h a m b ,i Department of Neurology, University of Umea, Umea, Sweden, and b Department of Statistics & Computational Mathematics, University of Liverpoo~ Liverpool, UK (Received 17 January, 1992) (Accepted 21 March, 1992)
It is widely accepted that the maximum force produced by a muscle is directly proportional to its crosssectional area (Knuttgen 1976; Young et al. 1981; Maughan et al., 1983; Sale et al. 1987). The relationship between the muscle area and the fibre type composition, assessed as the area and proportion of the different fibre types, is on the other hand far from clear (Hiiggmark et ai. 1978; Tesch and Karlsson 1978; Schantz et al. 1983; Maughan 1984; Ryushi et al. 1988). Recent developments of preparative techniques now enable us to study the fine structure of whole human skeletal muscle, thereby eliminating some of the technical constraints previously involved in the analysis of the muscle fibre composition. We have reanalysed data, obtained from whole muscle cross-sections (Lexell et al. 1988), on muscle area, total number, size and proportion of the different fibre types and looked closer into the relationship between these variables, to identify determinants of the size of human muscle. The vastus lateralis muscle from the right leg of 31 previously healthy men, 15-83 years of age, was extirpated less than 3 days post mortem. A slice, about I0 ram, was cut from each muscle half way between the origin and the insertion. Thin cross-sections ( 1 5 / t m ) were cut and stained for myofibrillar adenosine triphosphatase (mATPase) at pH 10.4 to visualize type I and type 2 fibres. The numbers of type I and type 2 fibres were counted within every 48th mm 2 (6 × 8) throughout the muscle cross-section, and were used to estimate the proportion of type 1 fibres, P, in the muscle cross-section. The mean cross-sectional area (mm 2) of the mus-
Correspondence to: Dr. J. Lexell, Department of Neurology, University of Ume~i, S-90185 Ume~, Sweden. Tel.: (+ 46) 90 l0 28 26; Fax: (+46) 90 14 31 07.
cle, A, was estimated by multiplying the number of systematically sampled quadrats by 48. The total number of fibres in the muscle cross-section was estimated by multiplying A by the mean number of fibres per mm 2. The mean cross-sectional areas (/~m2) of type 1 and type 2 fibres, S~ and S 2, respectively, were calculated from measurements of the area of a total of 125 fibres of each type, from five different regions throughout the muscle cross-section. The mean fibre area for the muscle cross-section was estimated by S ffi P x S~ + ( l - P ) x S 2, and the proportion of the fibre area in the muscle cross-section occupied by type 2 fibres was estimated by A 2 -- ( l - P ) × $2/S. The summary statistics and linear regression procedures of the statistical package SAS (SAS Institute Inc., U.S.A.) were used for the calculations and analyses. The muscle area, A, was regressed on the five variables T, St, $2, P and A 2. The effect of each of these variables was assessed in terms of an F-statistic and its associated significance level. The scattergrams of T, S t, S2P and A 2 with A are present in Fig. la-d. The results of the single regression analyses - the regression line, the correlation coefficient (r) and the significance level - are included in each graph. The relationship between A and T was significant at the 0.1% level (Fig. la), and the relationship between A and S 2 was significant at the 1% level (Fig. lb). There was no significant relationship between A and S I (Fig. lb), nor between A and P (Fig. lc). The relationship between A and A 2 was significant at the 0.1% level (Fig. ld). The correlation between muscle area and total number of fibres is stronger than that between muscle area and any of the other variables. This implies that the total number of fibres has the greatest influence on muscle area. The mean fibre area has been shown to be significantly correlated with the muscle area (Lexell et ai. 1988). Figure lb shows that this is accounted for
114 .
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r = 0.81 P <
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Total number of fibres (x103)
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Fig. 1. Relationship between muscle cross-sectional area and (a) total number of fibres, (b) mean area of type 1 fibres and type 2 fibres, (c) proportion of type I fibres, and (d) relative area of type 2 fibres. The regression line, the correlation coefficient (r) and the significance level are included in each graph.
exclusively by the mean type 2 fibre area. The fibre type proportion appears not to influence the muscle area. Thus, the fibre number and only the area of type 2 fibres are influencing the muscle area. When the proportion and the mean area of type 2 fibres were combined to form A 2 - the relative type 2 fibre area - and regressed against muscle area, the relationship was stronger than the two individual relationships, as reflected in the values of the correlation coefficients: 0.51, -0.27 and 0.59. This indicates that the proportion of the fibre area in the muscle crosssection occupied by type 2 fibres significantly influences the size of the muscle, so that both the size and the number of type 2 fibres are important in determining the muscle area. Thus, the cross-sectional area of the vastus lateralis muscle is mainly determined by the total number of fibres, and to a lesser extent by the size and~or the number of type 2 fibres. This complex relationship can explain some of the conflicts in the literature. References H~iggmark, T., E. Jansson and B. Svane (1978) Cross-sectional area of the thigh muscle in man measured by computet tomography. Scand. J. Clin. Lab. Invest., 38: 355-360.
Knuttgen, H.G. (1976) Development of muscular strength and endurance. In: H.G. Knuttgen (Ed.), Neuromuscular Mechanisms for Therapeutic and Conditioning Exercise, University Park Press, Baltimore, MD, pp. 97-118. Lexell, J,, C.C. Taylor and M. Sj6str(im (1988) What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in whole vastus lateralis from 15- to 83.year-old men. J. Neurol. Sci., 84: 275-294. Maughan, RJ. and M.A. Nimmo (1984) The influence of variations in muscle fibre composition on muscle strength and cross-sectional area in untrained males. J. Physiol., 351: 299-311. Maughan, RJ., J.S. Watson and J. Weir (1983) Strength and crosssectional area of human skeletal muscle, J. Physiol., 338: 37-49. Ryushi, T., K. Hiikkinen, H. Kauhanen and P.V. Komi (1988) Muscle fiber characteristics, muscle cross-sectional area and force production in strength athletes, physically active males and females. Scand. J. Sports Sci., 10: 7-15. Sale, D.G., J.D. MacDougall, S.E. Always and J.R. Sutton (1987) Voluntary strength and muscle characteristics in untrained men and women and male hodybuilders. J. AppI. Physiol., 62: 17861793. Schantz, P., E. Randall-Fox, W. Hutchinson, A. Tyd~n and P.-O. ,~,strand (1983) Muscle fibre type distribution, muscle cross-seetional area and maximal voluntary strength in humans. Acta Physiol. Seand., 117, 219-226. Tesch, P. and J. Karlsson (1978) Isometric strength performance and muscle fibre type distribution in man. Acta Physiol. Scand., 103: 47-51. Young, A., M. Stokes, I.C.R. Walker and D. Newham (1981) The relationship between quadriceps size and strength in normal young adults. Ann. Rheum. Dis., 40: 619.