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Age-related morphometric characteristics of human skeletal muscle in male subjects

Evangelia Kararizou
,
Panagiota Manta
,
Nikolaos Kalfakis
,
Demetrios Vassilopoulos

Pol J Pathol 2009; 4: 186-188
Online publish date: 2010/01/06
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Introduction
The earliest studies on ageing and muscle fibre composition suggested that type I fibre percentage increases with ageing [1, 2]. Others, particularly Grimby and Saltin, were in disagreement [3]. They examined muscle biopsies of persons aged up to 66 years and found no age-related changes in type 1 distribution. In addition, gender-related alterations of muscle function have been reported with increasing age but there are very few data on gender-related morphological changes in ageing individuals [2, 5]. The existence of these age and gender changes should be taken into account in the interpretation of muscle biopsies of aged individuals and must be investigated in detail.
The purpose of the present study is to investigate the age-related changes in muscle biopsies from the quadriceps femoris in male subjects of different ages. Our aim was to determine whether ageing was associated with quantitative changes in fibre size, fibre type composition and fibre type distribution of the two fibre types in and around the muscle fascicle.

Material and methods

A histological and histochemical study was performed on specimens from the quadriceps femoris taken during autopsy on 8 males who had died suddenly. The patients were divided into two groups. The first one contained 4 patients under the age of 50 and the second group comprised 4 men over the age of 70. The age of the subjects varied from 17 to 82 years.
No subject had a history of neuromuscular or other disease that could have a direct or indirect effect on the peripheral nervous system or the skeletal muscles. The samples were taken immediately post mortem.
Cryostat 10 µm sections were stained for routine (pH 9.4) ATPase. We performed ATPase staining using a modified protocol described by Dubowitz and Brooke [6]. It has been shown that in autopsy material a clear definition of the two fibre types is possible [7]. With the aid of an automatic image analysis system, Image-Pro Plus (Version e4,5.1-Media Cybernetic) the following measurements were performed: a) number of type 1 and 2 fibres, b) diameter of type 1 and 2 fibres, c) percentage of the number and mean diameter of the two types in the interior and the peripheral area of fascicles. Typically, at least 400 fibres were analysed for each section. The size of muscle fibres was assessed by measuring the “smallest fibre diameter” [6]. The findings for each muscle were evaluated in relation to age group.
For the statistical analysis, Student’s t-test and linear regression, as well as Spearman’s non-parametric method and analysis of variance (ANOVA) were applied.

Results

Proportion of the two fibre types in and around the muscle fascicle

The proportion of type 2 fibres decreased significantly with age (p < 0.005), but the proportion of type 1 fibres was not significantly changed (Table I). A clearly greater proportion of type 2 fibres was found in the periphery of the fascicles (p < 0.001) in the elderly group. The difference in percentage between internal and peripheral type 2 was 8.8.

Mean diameter of two fibre types in the peripheral and the internal part of the fascicle
The mean diameter of both type 1 and type 2 was smaller in the periphery of the fascicle, although the difference was not significant (Table II). The correlation of fibre size with age showed that the type 2 fibres decrease in size with age both in the peripheral and the internal part of the fascicle. This finding was more evident in the periphery of the fascicles (p < 0.05) (Table III).

Discussion

Skeletal muscle fibre changes have been reported in ageing humans. However, the age-related patterns of changes in muscle fibres are inconclusive. Some report an increase of type 1 muscle fibres with increasing age [8-11], whereas others report insignificant changes [12, 13] or a decreased area with increased age [14]. Our findings were consistent with those of the cross-sectional studies which showed reduced number and mean area of type 2 muscle fibres during ageing [8, 10, 15-18]. The underlying mechanism of these changes is not clear. It could be a result of the reduced activity of elderly people, although selective involvement of motor neurons, particularly the larger motor neurons innervating type 2 fibres, cannot be excluded [19].
An apparent “grouping” of the muscle fibre types has been observed and these data confirm those of studies in older human skeletal muscles [20]. The mechanisms for the obvious grouping of the fibre types in the ageing human muscle still needs to be fully understood. Presently, the most evident explanation seems to be that the fibre type grouping arises from a continuous process of denervation and partial reinnervation that is claimed to accelerate with advancing age [21]. When we compared our two age groups, we found a greater proportion of type 2 but the difference tended to decrease with age, and that is in accordance with the findings of Sjöström et al. [22]. The proportion of two histochemical types of fibres varies systematically within the muscle. A greater proportion of type 2 fibres has been observed in the superficial part [8]. It has been suggested that this phenomenon could be the result of adaptation of the various parts of the muscle to different functional demands. It is known that in the flight muscles of several avian species a ring composed almost entirely of large type 2 fibres surrounds each fascicle. In non-flight muscles the distribution is random [23]. The influence of local factors in the histochemical organization of the fascicle cannot be ignored. It has been suggested that the greater amount of collagen surrounding the fascicle in comparison with the thin layer of collagen around individual fibres creates different mechanical conditions that modulate the physiological and histochemical properties of muscle fibres [24]. The role of local factors could also be supported by our findings of reduced muscle fibre diameter in the periphery of the fascicle. This could be indicative of vascular involvement, since perifascicular atrophy in dermatomyositis is considered to be a result of vasculopathy [25]. Blood flow to skeletal muscle is a potentially important factor in the reduction of muscle function associated with ageing (sarcopenia). Reduced capillary density, less maximal blood flow, and a slower hyperaemic flow response have been reported in some, but not all, studies [26]. The possibility cannot be excluded that the histochemical organization of the central and the peripheral part of the muscle fascicle is the result of a combination of the above or other factors. The matter could be further elucidated by a combined physiological, histochemical and biochemical investigation of strictly selected groups of subjects.
The gender-related morphological changes in muscle fibre composition are controversial and there is a small number of references [2, 5]. Fayet et al. in their study showed a decrease of the proportion of type 2 fibres in males without significant changes in their size [27]. Similar were the findings of Larsson et al. in their study of biopsies from the vastus lateralis muscle of male subjects from 22 to 65 years of age [19]. The differences between males and females may be partially related to gender differences in muscular activity.
In conclusion, we found that type 2 skeletal muscle fibres decreased in size and proportion with increasing age. The differences in the size and shape of the fast-twitch fibres may be a result of decreasing muscle activity, as lack of physical activity or regular exercise may result in age-related disuse atrophy. Training programmes must systematically manipulate training frequency, intensity, and duration to be effective and to improve endurance at any age. The existence of these age and gender changes should be taken into account in the interpretation of muscle biopsies of aged individuals.

References
1. Gollnick PD, Armstrong RB, Saubert CW 4th, et al. Enzyme activity and fiber composition in skeletal muscle of untrained and trained men. J Appl Physiol 1972; 33: 312-319.
2. Larsson L, Karlsson J. Isometric and dynamic endurance as a function of age and skeletal muscle characteristics. Acta Physiol Scand 1978; 104: 129-136.
3. Grimby G, Saltin B. The ageing muscle. Clin Physiol 1983; l3: 209-218.
4. Asmussen E, Heeboll-Nielsen K. Isometric muscle strength in relation to age in men and women. Ergonomics 1962; 5: 167-169.
5. Bassey EJ, Harries UJ. Normal values for handgrip strength in 920 men and women aged over 65 years of age, and longitudinal changes over 4 years in 620 survivors. Clin Sci (Lond) 1993; 84: 331-313.
6. Dubowitz V, Brooke MH. Histology and histochemical stains and reactions. In: Muscle Biopsy: A Modern Approach. Dubowitz V, Brooke MH (eds). WB Saunders, London 1973; 320-337.
7. Engel WK. Selective and non selective susceptibility of muscle fibre types. Arch Neurol 1970; 22L97-117.
8. Lexell J, Henriksson-Larsen K, Winblad B, Sjöström M. Distribution of different fibre types in human skeletal muscle: effects of ageing studied in whole muscle cross sections. Muscle Nerve 1983; 6: 588-595.
9. Lexell J, Taylor CC. Variability in muscle fibre areas in whole human quadriceps muscle: effects of increasing age. J Anat 1991; 174: 239-249.
10. Nikolic M, Malnar-Dragojevic D, Bobinac D, et al. Age-related skeletal muscle atrophy in humans: an immunohistochemical and morphometric study. Coll Antropol 2001; 25: 545-553.
11. Sjöström M, Angquist KA, Rais O. Intermittent claudication and muscle fibre fine structure: correlation between clinical and morphological data. Ultrastruct Pathol 1980; 1: 309-326.
12. Grimby G, Aniansson A, Zetterberg C, Saltin B. Is there a change in relative muscle fibre composition with age? Clin Physiol 1984; 4: 89-194.
13. Monemi M, Eriksson PO, Eriksson A, Thornell LE. Adverse changes in fibre type composition of the human masseter versus biceps brachii muscle during ageing. J Neurol Sci 1998; 154: 35-48.
14. Essen-Gustavsson B, Borges O. Histochemical and metabolic characteristics of human skeletal muscle in relation to age. Acta Physiol Scand 1986; 126: 107-114.
15. Grimby G, Danneskiold-Samsoe B, Hvid K, Saltin B. Morpho-logy and enzyme capacity in arm and leg muscle in 78-81 year old men and women. Acta Physiol Scand 1982; 115: 125-134.
16. Lexell J, Downham DY. What is the effect of ageing on type 2 muscle fibres? J Neurol Sci 1992; 107: 250-251.
17. Lee WS, Cheung WH, Qin L, Tang N. Age-associated decrease of type IIA/B human skeletal muscle fibers. Current Orthop Practise 2006; 450: 231-237.
18. Manta P, Kalfakis N, Kararizou E, et al. Size and proportion of fibre types in human muscle fascicles. Clin Neuropathol 1996; 15: 116-118.
19. Larson L, Sjodin B, Karlsson S. Histochemical and biochemical changes in human skeletal muscle with age in sedentary males aged 22-65 years. Acta Physiol Scand 1978; 103: 1-39.
20. Lexell J, Downham DY. The occurrence of fibre-type grouping in healthy human muscle: a quantitative study of cross-sections of whole vastus lateralis from men between 15 and 83 years. Acta Neuropathol 1991; 81: 377-381.
21. Lexell J. Human aging, muscle mass, and fibre type composition. J Gerontol 1995; 50: 11-16.
22. Sjöström M, Lexell J, Downham DY. Differences in fibre number and fibre type proportion within fascicles: a quantitative morphological study of whole vastus lateralis muscle from childhood to old age. Anat Rec 1992; 234: 183-189.
23. Papapetropoulos T, Rantsios A, Manta P. Type 1 and type 2 muscle fibres distribution Muscle Nerve 1983; 11: 786-787.
24. Kovanen V, Suominen H, Heikkinen E. Collagen of slow and fast twitch muscle fibres I different types of rat skeletal muscle. Eur Appl Physiol 1984; 52: 235-242.
25. Crowe WE, Bove KE, Levinston JE, Hilton PK. Clinical and pathogenetic implicayions of histopathology in childhood dermatopolymyositis. Arthritis Rheum, 1982; 25: 126-131.
26. McCully KK, Posner JDJ. The application of blood flow measurements to the study of aging muscle. Gerontol A Biol Sci Med Sci 1995; 50: 130-136.
27. Fayet G, Rouche A, Hogrel JY, et al. Age-related morphological changes of the deltoid muscle from 50 to 79 years of age. Acta Neuropathologica 2001; 101: 358-366.

Address for correspondence

dr Evangelia Kararizou

Neurologic Clinic, Aeginition Hospital, 72-74,
Vass. Sofias Ave. 11528, Athens, Greece
phone 0030210-7289282
e-mail: ekarariz@med.uoa.gr
Copyright: © 2010 Polish Association of Pathologists and the Polish Branch of the International Academy of Pathology This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0) License (http://creativecommons.org/licenses/by-nc-sa/4.0/), allowing third parties to copy and redistribute the material in any medium or format and to remix, transform, and build upon the material, provided the original work is properly cited and states its license.
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