Coupling between skeletal muscle fiber size and capillarization is maintained during healthy aging

Abstract

Background: As muscle capillarization is related to the oxidative capacity of the muscle and the size of muscle fibres, capillary rarefaction may contribute to sarcopenia and functional impairment in older adults. Therefore, it is important to assess how ageing affects muscle capillarization and the interrelationship between fibre capillary supply with the oxidative capacity and size of the fibres.

Methods: Muscle biopsies from healthy recreationally active young (22 years; 14 men and 5 women) and older (74 years; 22 men and 6 women) people were assessed for muscle capillarization and the distribution of capillaries with the method of capillary domains. Oxidative capacity of muscle fibres was assessed with quantitative histochemistry for succinate dehydrogenase (SDH) activity.

Results: There was no significant age-related reduction in muscle fibre oxidative capacity. Despite 18% type II fibre atrophy (P = 0.019) and 23% fewer capillaries per fibre (P < 0.002) in the old people, there was no significant difference in capillary distribution between young and old people, irrespective of sex. The capillary supply to a fibre was primarily determined by fibre size and only to a small extent by oxidative capacity, irrespective of age and sex. Based on SDH, the maximal oxygen consumption supported by a capillary did not differ significantly between young and old people.

Conclusions: The similar quantitative and qualitative distribution of capillaries within muscle from healthy recreationally active older people and young adults indicates that the age-related capillary rarefaction, which does occur, nevertheless maintains the coupling between skeletal muscle fibre size and capillarization during healthy ageing.

Keywords: Ageing; Capillary; Muscle fibre; Oxidative capacity; Succinate dehydrogenase.

Figure 1

Typical example of serial vastus lateralis muscle sections from an old man stained for (A) myosin heavy chain (MHC) type I (dark stained) and capillaries (dark dots), (B) succinate dehydrogenase (SDH) activity. Note that type I fibres (dark stained) had, as expected, a higher SDH activity compared with type II fibres (light stained). Asterisk (*) identifies same fibre in the two panels.

Figure 2

Fibre outlines and capillary domain areas. In (A), an example of a small part of a muscle section from a young man stained for myosin heavy chain type I (type I fibres appear dark and type II fibres light) and capillaries (black dots around the fibres). In (B), the type II fibre outlines are shown with the capillaries as red dots. In (C), the capillary domains are illustrated; the contours indicate the borders of the capillary domains, and the red dots correspond to the capillaries. In (D), the overlap of capillary domains and type II fibres is illustrated. It is important to note that a fibre may receive oxygen also from capillaries not in direct contact with the fibre; this situation occurs when a fibre overlaps a domain from a non‐adjacent capillary (in grey, indicated by the arrow).

Figure 3

Fibre cross‐sectional area (FCSA) in the vastus lateralis muscle of young (N = 14) and old men (N = 22) and young (N = 5) and old women (N = 6) according to fibre type (type I and II and ‘all fibres’). Note that in ‘all fibres’, type I and II and hybrid fibres are included in the analysis. Values are mean ± SD; asterisk (*) indicates significant difference between men and women at P = 0.001; number sign (#) indicates significant difference from sex‐matched young people at P = 0.019; dollar sign ($) indicates type effect at P < 0.01.

Figure 4

(A) Local capillary‐to‐fibre ratio (LCFR) and (B) capillary fibre density (CFD) in the vastus lateralis muscle of young (N = 13) and old men (N = 22), and young (N = 5) and old women (N = 6) according to the fibre type (types I and II and ‘all fibres’). Note that in ‘all fibres’, type I and II and hybrid fibres are included in the analysis. Values are mean ± SD; asterisk (*) indicates significant difference between men and women at P < 0.05; number sign (#) indicates significant difference from sex‐matched young people at P < 0.05; beta (β) indicates significant type × sex interaction reflected by a larger CFD of type II fibres in women than men.

Figure 5

Fibre oxidative capacity (A) per unit muscle volume (VO₂max _{mass specific}) and (B) per mm fibre length (VO₂max _fibre) in the vastus lateralis muscle of young men (N = 5), old men (N = 14), and old women (N = 5) according to the fibre type (types I and II and ‘all fibres’). (C) Local maximal oxygen demand supported by a capillary (MO₂max) in the vastus lateralis muscle of the same population. Note that in ‘all fibres’, type I and II and hybrid fibres are included in the analysis. Values are mean ± SD; asterisk (*) indicates significant difference between men and women at P < 0.05; number sign (#) indicates significant difference from sex‐matched young people at P < 0.05; dollar sign ($) indicates type effect at P < 0.01.

Figure 6

The relationship between the local muscle maximal oxygen demand supported by a capillary (MO₂max) and their respective domain area in the vastus lateralis muscle. A positive correlation was observed between MO₂max and domain area (R = 0.604, N = 4095 capillaries, P = 0.001). R = 0.854 ± 0.031 for regression lines from each young person (N = 6 individuals; black triangles) and R = 0.828 ± 0.018 for regression lines from each old man (N = 19 individuals; white square); mean ± SEM.

Figure 7

Fibre oxidative capacity per unit muscle volume (VO₂max _{mass specific}) in relation to fibre cross‐sectional area (FCSA) in young (N = 6 individuals; black triangles; R ² = 0.024) and old men (N = 19 individuals; white squares; R ² = 0.055) in the vastus lateralis muscle.

Figure 8

Relationships between the local capillary‐to‐fibre ratio (LCFR) with (A) the fibre cross‐sectional area (FCSA) and (B) the fibre oxidative capacity (VO₂max _fibre) in young (N = 6 individuals; black triangles) and old men (N = 19 individuals; white squares) in the vastus lateralis muscle. Relationships between the capillary fibre density (CFD) with (C) FCSA and (D) fibre oxidative capacity per muscle volume unit (VO₂max _{mass specific}) in young (N = 6 individuals; black triangles) and old men (N = 19 individuals; white squares) in the vastus lateralis muscle. Note that in (A) the FCSA and LCFR were significantly and positively correlated.