Skip to main content
SpringerLink
Log in

Three-dimensional study of the capillary supply of skeletal muscle fibres using confocal microscopy

  • Published:
Journal of Muscle Research & Cell Motility Aims and scope Submit manuscript

Abstract

Three-dimensional (3D) study of capillary network of individual muscle fibres in rat extensor digitorum longus (EDL) and soleus (SOL) muscles is presented. Stereology and 3D reconstruction techniques were applied to stacks of serial optical sections recorded by a confocal microscope from thick muscle slices. The results suggest that SOL muscle fibres have a larger surface area and volume as well as a larger length of capillaries per fibre length than EDL. On the other hand, these two muscles have a similar ratio of capillary length to fibre surface area. The 3D approach to evaluation of muscle fibre capillarization brings many advantages over traditional measurements made on single muscle sections and could also be applied to the study of angiogenesis in other tissues.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aharinejad S, McDonald IC, Mackay CE and Masonsavas A (1993) New aspects of microvascular corrosion casting — a scanning, transmission electron and high resolution intravital video microscopic study. Microsc Res Tech 26: 473-488.

    Google Scholar 

  • Amann K, Breitbach M, Ritz E and Mall G (1998) Myocyte/capillary mismatch in the heart of uremic patients. J Am Soc Nephrol 9: 1018-1022.

    Google Scholar 

  • Anversa P, Capasso JM, Ricci R, Sonnenblick EH and Olivetti G (1989) Morphometric analysis of coronary capillaries during physiologic myocardial growth and induced cardiac hypertrophy: a review. Int J Microcirc Clin Exp 8: 353-363.

    Google Scholar 

  • Artacho-Perula E and Roldan-Villalobos R (1995) Estimation of capillary length density in skeletal muscle by unbiased stereological methods: I. use of vertical slices of known thickness. Anat Rec 241: 337-344.

    Google Scholar 

  • Baez S (1969) Simultaenous measurements of radii and wall thickness of microvessels in the anaesthetized rat. Circ Res 25: 315-329.

    Google Scholar 

  • Bass A, Teisinger J, Hnik P, Mackova E, Vejsada R and Erzen I (1983) Changes of lysosomal and energy-supply enzymes in hypertrophying muscles after denervation. Physiologia Bohemoslovaca 32: 506.

    Google Scholar 

  • Batra S, Konig MF and Cruz-Orive LM (1995) Unbiased estimation of capillary length from vertical slices. J Microsc 178: 152-159.

    Google Scholar 

  • Battegay EJ (1995) Angiogenesis: mechanistic insights, neovascular diseases and therapeutic prospects. J Mol Med 73: 333-346.

    Google Scholar 

  • Brodal P, Ingjer F and Hermansen L (1977) Capillary supply of skeletal muscle fibres in untrained and endurance-trained men. Am J Physiol 232: H705-H712.

    Google Scholar 

  • Brown MD, Cotter MA, Hudlická O and Vrbová G (1976) The effects of different pattern of muscle activity on capillary density, mechanical properties and structure of slow and fast rabbit muscles. Pflüg Arch 361: 241-250.

    Google Scholar 

  • Cruz-Orive LM (1993) Systematic sampling in stereology. Bull Intern Statis Inst Proceedings 49th Session, Florence 1993 55(2): 451-468.

    Google Scholar 

  • Cruz-Orive LM (1997) Stereology of single objects. J Microsc 186: 93-107.

    Google Scholar 

  • Egginton S (1987) Effect of an anabolic hormone on aerobic capacity of rat striated muscle. Pflüg Arch 410: 356-361.

    Google Scholar 

  • Egginton S (1990). Numerical and areal density estimates of fibre type composition in a skeletal muscle (rat extensor digitorum longus). J Anat 168: 73-80.

    Google Scholar 

  • Egginton S and Ross HF (1989a) Quantifying capillary distribution in four dimensions. Adv Exp Med Biol 248: 271-280.

    Google Scholar 

  • Egginton S and Ross HF (1989b) Influence of muscle phenotype on local capillary supply. Adv Exp Med Biol 248: 281-291.

    Google Scholar 

  • Egginton S, Turek Z and Hoofd L (1987) Morphometric analysis of sparse capillary networks. Adv Exp Med Biol 215: 1-12.

    Google Scholar 

  • Eken T and Gundersen K (1988) Electrical stimulation resembling normal motor-unit activity: effects on denervated fast and slow rat muscles. J Physiol 402: 651-669.

    Google Scholar 

  • Ellis CG, Mathieu-Costello O, Potter RF, MacDonald IC and Groom AC (1990) Effect of sarcomere length on total capillary length in skeletal muscle: in vivo evidence for longitudinal stretching of capillaries. Microvasc Res 40: 63-72.

    Google Scholar 

  • Endre T, Mattiasson I, Berglund G and Hulthen UL (1998) Muscle fibre composition and glycogen synthase activity in hypertensionprone men. J Int Med 243: 141-147.

    Google Scholar 

  • Eržen I and Maravić V (1993) Simultaneous histochemical demonstration of capillaries and muscle fibre types. Histochemistry 99: 57-60.

    Google Scholar 

  • Folkman J (1995) Angiogenesis in cancer, vascular, rheumatoid and other disease. Nature Med 1: 27-31.

    Google Scholar 

  • Folkman J and D'Amore PA (1996) Blood vessel formation: what is its molecular basis. Cell 87: 1153-1155.

    Google Scholar 

  • Frank RM (1994) Vascular endothelial growth factor-its role in retinal vascular proliferation. N Engl J Med 331: 1519-1520.

    Google Scholar 

  • Gokhale AM (1990) Unbiased estimation of curve length in 3D using vertical slices. J Microsc 159: 133-141.

    Google Scholar 

  • Gorza L (1990) Identification of a novel type 2 fiber population in mammalian skeletal muscle by combined use of histochemical myosin ATPase and anti-myosin monoclonal antibodies. J Histochem Cytochem 38: 257-265.

    Google Scholar 

  • Gray SD and Renkin EM (1978) Microvascular supply in relation to fibre metabolic type in mixed skeletal muscles of rabbits. Microvasc Res 16: 406-425.

    Google Scholar 

  • Green H, Goreham C, Ouyang J, Ball-Burnett M and Ranney D (1999) Regulation of fibre size, oxidative potential, and capillarization in human muscle by resistance exercise. Am J Physiol 276: R591-R596.

    Google Scholar 

  • Gundersen HJG (1977) Notes on the estimation of the numerical density of arbitrary profiles: the edge effect. J Microsc 111: 219-223.

    Google Scholar 

  • Gundersen HJG and Jensen EB (1987) The efficiency of systematic sampling in stereology and its prediction. J Microsc 147: 229-263.

    Google Scholar 

  • Hansen-Smith FM, Watson L and Lu DY (1988) Griffonia simplicifoila I: fluorescent tracer for microcirculatory vessels in nonperfused thin muscles and sectioned muscle. Microvasc Res 36(3): 199-215.

    Google Scholar 

  • Hansen-Smith FM, Hudlicka O and Egginton S (1996) In vivo angiogenesis in adult rat skeletal muscle: early changes in capillary network architecture and ultrastructure. Cell Tisue Res 286: 123-136.

    Google Scholar 

  • Hernandez N, Torres SH, Finol HJ, Sosa A and Cierco M (1996) Capillary and muscle fibre type changes in DOCA-salt hypertensive rats. Anatomical Record 246: 208-216.

    Google Scholar 

  • Hoofd L, Turek Z, Kubat K, Ringnalda BEM and Kazda S (1985) Variability of intercapillary distance estimated on histological sections of rat heart. Adv Exp Biol 191: 239-297.

    Google Scholar 

  • Hudlicka O (1991) What makes blood vessels grow? J Physiol 444: 1-24.

    Google Scholar 

  • Hudlicka O, Brown M and Egginton S (1992) Angiogenesis in skeletal and cardiac muscle. Physiol Rev 72: 369-417.

    Google Scholar 

  • Ingjer F (1979) Effects of endurance training on muscle fibre ATP-ase activity, capillary supply and mitochondrial content in man. J Physiol 294: 419-432.

    Google Scholar 

  • Isner JM, Baumgartner I, Rauh G, Schainfeld R, Blair R, Manor O, Razvi S and Symes JF (1998) Treatment of thromboangiitis obliterans (Buerger's disease) by intramuscular gene transfer of vascular endothelial growth factor: preliminary clinical results. J Vascular Surg 28: 964-973.

    Google Scholar 

  • James NT (1981) A stereological analysis of capillaries in normal and hypertrophic muscle. J Morphol 168: 43-49.

    Google Scholar 

  • Jerusalem F (1994) The microcirculation of muscle. In: Engel AG and Franzini-Armstrong C (eds) Myology. (vol. 1, p. 368) McGraw-Hill, New York.

    Google Scholar 

  • Jirák D, Kubínová L, Tomori Z, Hlinka R, Jirkovská M and Krekule I (1997) Interactive visualization of a capillary bed. Physiol Res 46: 33.

    Google Scholar 

  • Jirkovská M, Kubínová L, Krekule I and Hach P (1998) Spatial arrangement of fetal placental capillaries in terminal villi: a study using confocal microscopy. Anat Embryol 197: 263-272.

    Google Scholar 

  • Kaczmarek E (1999) Visualisation and modelling of renal capillaries from confocal images. Med Biol Eng Comput 37: 273-277.

    Google Scholar 

  • Karen P, Kubínová L and Krekule I (1998) STESYS software for computer-assisted stereology. Physiol Res 47: 271-278.

    Google Scholar 

  • Kinding CA, Sexton WL, Fedde MR and Poole DC (1998) Skeletal muscle microcirculatory structure and hemodynamics in diabetes. Resp Physiol 111: 163-175.

    Google Scholar 

  • Kondering MA, van Ackern C, Steinberg F and Streffer CH (1992) Combined morphological approaches in the study of network formation in tumor angiogenesis. In: Steiner R, Weisz PB and Langer R, (eds) Angiogenesis: Key Principles Science Technology Medicine, Birkauser Verlag, Basel, 40-58.

    Google Scholar 

  • Koyama T, Gao M, Batra S, Togashi H and Saito H (1997) Myocyte hypertrophy and capillarization in spontaneously hypertensive stroke-prone rats. Adv Exp Med Biol 411: 365-368.

    Google Scholar 

  • Kriketos AD, Pan DA, Sutton JR, Hoh JFY, Baur LA, Cooney GJ, Jenkins AB and Storlien LH (1995) Relationships between muscle membrane lipids, fiber type and enzyme activities in sedentary and exercised rats. Am J Physiol 269 (Regulatory Integrative Comp Physiol 38): R1154-R1162.

    Google Scholar 

  • Krogh A (1919) The number and distribution of capillaries in muscles with calculations of the oxygen pressure head necessary for supplying the tissue. J Physiol 52: 409-415.

    Google Scholar 

  • Kubínová L and Janáček J (1998) Estimating surface area by isotropic fakir method from thick slices cut in arbitrary direction. J Microsc 191: 201-211.

    Google Scholar 

  • Large J and Tyler KR (1985) Changes in capillary distribution in rat fast muscles following nerve crush and reinnervation. J Physiol 362: 13-21.

    Google Scholar 

  • Larsen JO, Gundersen HJG and Nielsen J (1998) Global spatial sampling with isotropic virtual planes: estimators of length density and total length in thick, arbitrarily orientated sections. J Microsc 191: 238-248.

    Google Scholar 

  • Mai JV, Edgerton VR and Barnard RJ (1970) Capillarity of red, white and intermediate muscle fibres in trained and untrained guineapigs. Experientia 26: 1222-1223.

    Google Scholar 

  • Mall G, Schikora I, Mattfeldt T and Bodle R (1987) Dipyridamole-induced neoformation of capillaries in the rat heart. Quantitative stereological study on papillary muscles. Lab Invest 57: 86-93.

    Google Scholar 

  • Mathieu O, Cruz-Orive LM, Hoppeler H and Weibel ER (1983) Estimating length density and quantifying anisotropy in skeletal muscle capillaries. J Microsc 131: 131-146.

    Google Scholar 

  • Mathieu-Costello O (1987) Capillary tortuosity and degree of contraction or extension of skeletal muscles. Microvasc Res 33: 98-117.

    Google Scholar 

  • Mathieu-Costello O (1994) Morphometry of the size of the capillary-to-fiber interface in muscles. Adv Exp Med Biol 345: 661-668.

    Google Scholar 

  • Mathieu-Costello O, Potter RF, Ellis CG and Groom AC (1988) Capillary configuration and fiber shortening in muscles of the rat hindlimb: correlation between corrosion casts and stereological measurements. Microvasc Res 36: 40-55.

    Google Scholar 

  • Mattfeldt T, Möbius H-J and Mall G (1985) Orthogonal triplet probes; an efficient method for unbiased estimation of length and surface of objects with unknown orientation in space. J Microsc 139: 279-289.

    Google Scholar 

  • Mattfeldt T, Mall G, Gharchbaghi H and Moller P (1990) Estimation of surface area and length with the orientator. J Microsc 159: 301-317.

    Google Scholar 

  • McMillan PJ, Archambeau JO, Gokhale AM, Archambeau M-H and Oey M (1994) Morphometric and stereologic analysis of cerebral cortical microvessels using opical sections and thin slices. Acta Stereol 13: 33-38.

    Google Scholar 

  • Murakami H, Yayama K, Miao RQ, Wang C, Chao L and Chao J (1999) Kallikrein gene delivery inhibits vascular smooth muscle cell growth and neointima formation in the rat artery after balloon angioplasty. Hypertension 34: 164-170.

    Google Scholar 

  • Myrhage R (1977) Microvascular supply of skeletal muscle fibres. Acta Orthopaed Scan 168(Suppl): 1-46.

    Google Scholar 

  • Nyengaard JR and Gundersen HJG (1992) The isector: a simple and direct method for generating isotropic, uniform random sections from small specimens. J Microsc 158: 19-30.

    Google Scholar 

  • Nyholm B, Qu Z, Kaal A, Pedersen SB, Gravholt CH, Andersen JL, Saltin B and Schmitz O (1997) Evidence of an increased number of type IIb muscle fibres in insulin-resistant first-degree relatives of patients with NIDDM. Diabetes 46: 1822-1828.

    Google Scholar 

  • Potter RF and Groom AC (1983) Capillary diameter and geometry in cardiac and skeletal muscle studied by means of corrosion casts. Microvasc Res 25: 68-84.

    Google Scholar 

  • Pullen AH (1977) The distribution and relative sizes of fibre types in the extensor digitorum longus and soleus muscles of the adult rat. J Anat 123: 467-486.

    Google Scholar 

  • Punkt K, Unger A, Welt K, Hilbig H and Schaffranietz (1996) Hypoxia-dependent changes of enzyme activities in different fibre types of rat soleus and extensor digitorum longus muscles. A cytophotometrical study. Acta Histochem (Jena) 98: 255-269 (R1154-R1162).

    Google Scholar 

  • Ranvier L (1874) De quelques faits relatifs à l'histologie et à la physiologie des muscles stries. Arch Physiol Norm Path 6: 1-15.

    Google Scholar 

  • Romanul FCA (1965) Capillary supply and metabolism of muscle fibres. Arch Neurol 12: 497-509.

    Google Scholar 

  • Schaper W, Gorge G, Winkler B and Schaper J (1988) The collateral circulation of the heart. Prog Cardiovasc Dis 31: 57-77.

    Google Scholar 

  • Schaper W, Sharma HS, Quinkler W, Markert T, Wünsch M and Scharper J (1990) Molecular biologic concepts of coronary anastomoses. J Am Coll Cardiol 15: 513-518.

    Google Scholar 

  • Schiaffino S, Gorza L, Sartore S, Saggin L, Ausoni S, Vianello M, Gundersen K and Lømo T (1989) Three myosin heavy chain isoforms in type 2 skeletal muscle fibres. J Musc Res Cell Motil 10: 197-205.

    Google Scholar 

  • Stål P, Eriksson PO and Thornell LE (1996) Differences in capillary supply between human oro-facial, masticatory and limb muscles. J Musc Res Cell Motil 17: 183-197.

    Google Scholar 

  • Symes JF, Losordo DW, Vale PR, Lathi KG, Esakof DD, Mayskiy M and Isner JM (1999) Gene therapy with vascular endothelial growth factor for inoperable coronary artery disease. Ann Thorac Surg 68: 830-836.

    Google Scholar 

  • Takeshita M, Ina K, Kitamura H, Shimada T and Nakamura M (1997) Ultrastructural study of capillary and myocytic changes in the masseter and heart of KK-Ay mice. J Electron Microsc 46: 413-423.

    Google Scholar 

  • Tomori Z, Matis L, Karen P, Kubínová L and Krekule I (2000) STESYS2: Extended STESYS software for MS Windows. Physiol Res 49: 695-701.

    Google Scholar 

  • Williams DA and Segal SS (1992) Microvascular architecture in rat soleus and extensor digitorum longus muscles. Microvasc Res 43: 192-204.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Physiology, Academy of Sciences of the Czech Republic, Vídeňská 1083, 14220, Prague 4, Czech Republic

    Lucie Kubínová & Jiří Janáček

  2. Institute of Pathophysiology, Medical Faculty, University of Ljubljana, Zaloška 4

    Samo Ribarič

  3. Institute of Anatomy, Medical Faculty, University of Ljubljana, Korytkova 2, SI-1000, Ljubljana, Slovenia

    Vita Čebašek & Ida Eržen

Authors
  1. Lucie Kubínová
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jiří Janáček
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Samo Ribarič
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Vita Čebašek
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ida Eržen
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kubínová, L., Janáček, J., Ribarič, S. et al. Three-dimensional study of the capillary supply of skeletal muscle fibres using confocal microscopy. J Muscle Res Cell Motil 22, 217–227 (2001). https://doi.org/10.1023/A:1012201314440

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1012201314440

Keywords

Search

Navigation