Capillary network characteristics are invaluable for diagnostics of muscle diseases. Biopsy material is limited in size and mostly not accessible for intensive research. Therefore, especially in human tissue, studies are performed on autopsy material. To approach the problem whether it is reliable to deduce hypotheses from autopsy material to explain physiological and pathological processes, we studied capillarity in pig soleus muscle 1 and 24 hr after death. Capillaries and muscle fibers were immunofluorescently marked, and images were acquired with a confocal microscope. Characteristics of the capillary network were estimated by image analysis methods using several plugins of the Ellipse program. Twenty-four hours after death, the measured characteristics of the capillary network differ by up to 50% when compared with samples excised 1 hr after death. Muscle fiber diameter, the measured capillary length, and tortuosity were reduced, and capillary network became more anisotropic. The main postmortem change that affects capillaries is evidently geometric deformation of muscle tissue. In conclusion, when comparing results from biopsy samples with those from autopsy samples, the effect of postmortem changes on the measured parameters must be carefully considered.

Biotechnical Faculty University of Ljubljana Ljubljana Slovenia

Celica Biomedical Ljubljana Slovenia

Department of Biomathematics Institute of Physiology Czech Academy of Sciences Prague Czech Republic

Faculty of Medicine University of Ljubljana Ljubljana Slovenia

Institute of Anatomy Faculty of Medicine University of Ljubljana Ljubljana Slovenia

Zobrazit více v PubMed

Ahmed SK, Egginton S, Jakeman PM, Mannion AF, Ross HF. Is human skeletal muscle capillary supply modelled according to fibre size or fibre type? Exp Physiol. 1997;82:231–4. PubMed

Al-Shammari AA, Gaffney EA, Egginton S. Modelling capillary oxygen supply capacity in mixed muscles: capillary domains revisited. J Theor Biol. 2014;356:47–61. PubMed

Olfert MI, Baum O, Hellsten Y, Egginton SE. Advances and challenges in skeletal muscle angiogenesis. Am J Physiol Heart Circ Physiol. 2016;310:H326–36. PubMed PMC

Egginton S, Gaffney E. Tissue capillary supply—it’s quality not quantity that counts! Exp Physiol. 2010;95:971–9. PubMed

Egginton S, Hudlická O. Selective long-term electrical stimulation of fast glycolytic fibres increases capillary supply but not oxidative enzyme activity in rat skeletal muscles. Exp Physiol. 2000;85:567–73. PubMed

Badr I, Brown MD, Egginton S, Hudlicka O, Milkiewicz M, Verhaeg J. Differences in local environment determine the site of physiological angiogenesis in rat skeletal muscle. Exp Physiol. 2003;88:565–8. PubMed

Bosutti A, Egginton S, Barnouin Y, Ganse B, Rittweger J, Degens H. Local capillary supply in muscle is not determined by local oxidative capacity. J Exp Biol. 2015;218:3377–80. PubMed

Barnouin Y, McPhee JS, Butler-Browne G, Bosutti A, De Vito G, Jones DA, Narici M, Behin A, Hogrel J-Y, Degens H. Coupling between skeletal muscle fiber size and capillarization is maintained during healthy aging. J Cachexia Sarcopenia Muscle. 2017;8:647–59. PubMed PMC

Hudlická O. The response of muscle to enhanced and reduced activity. Baillieres Clin Endocrinol Metab. 1990;4:417–39. PubMed

Hudlická O, Price S. The role of blood flow and/or muscle hypoxia in capillary growth in chronically stimulated fast muscles. Pflugers Arch. 1990;417:67–72. PubMed

Lexell J. Muscle capillarization: morphological and morphometrical analyses of biopsy samples. Muscle Nerve Suppl. 1997;5:S110–2. PubMed

Harris BA. The influence of endurance and resistance exercise on muscle capillarization in the elderly: a review. Acta Physiol Scand. 2005;185:89–97. PubMed

Stål P, Eriksson PO, Thornell LE. Differences in capillary supply between human oro-facial, masticatory and limb muscles. J Muscle Res Cell Motil. 1996;17:183–97. PubMed

Green H, Goreham C, Ouyang J, Ball-Burnett M, Ranney D. Regulation of fiber size, oxidative potential, and capillarization in human muscle by resistance exercise. Am J Physiol. 1999;276:R591–6. PubMed

Porter MM, Stuart S, Boij M, Lexell J. Capillary supply of the tibialis anterior muscle in young, healthy, and moderately active men and women. J Appl Physiol (1985). 2002;92:1451–7. PubMed

Charifi N, Kadi F, Feasson L, Costes F, Geyssant A, Denis C. Enhancement of microvessel tortuosity in the vastus lateralis muscle of old men in response to endurance training. J Physiol. 2004;554:559–69. PubMed PMC

Wüst RC, Gibbings SL, Degens H. Fiber capillary supply related to fiber size and oxidative capacity in human and rat skeletal muscle. Adv Exp Med Biol. 2009;645:75–80. PubMed

Egginton S, Ross HF. Quantifying capillary distribution in four dimensions. Adv Exp Med Biol. 1989;248:271–80. PubMed

Al-Shammari AA, Gaffney EA, Egginton S. Re-evaluating the use of Voronoi Tessellations in the assessment of oxygen supply from capillaries in muscle. Bull Math Biol. 2012;74:2204–31. PubMed

Fraser GM, Goldman D, Ellis CG. Microvascular flow modeling using in vivo hemodynamic measurements in reconstructed 3D capillary networks. Microcirculation. 2012;19:510–20. PubMed PMC

Fraser GM, Milkovich S, Goldman D, Ellis CG. Mapping 3-D functional capillary geometry in rat skeletal muscle in vivo. Am J Physiol Heart Circ Physiol. 2012;302:H654–64. PubMed PMC

Fraser GM, Sharpe MD, Goldman D, Ellis CG. Impact of incremental perfusion loss on oxygen transport in a capillary network mathematical model. Microcirculation. 2015;22:348–59. PubMed

Kubínová L, Janáček J, Ribarič S, Čebašek V, Eržen I. Three-dimensional study of the capillary supply of skeletal muscle fibres using confocal microscopy. J Muscle Res Cell Motil. 2001;22:217–27. PubMed

Čebašek V, Eržen I, Vyhnal, Janáček J, Ribarič S, Kubínová L. The estimation error of skeletal muscle capillary supply is significantly reduced by 3D method. Microvasc Res. 2010;79:40–6. PubMed

Janáček J, Cvetko E, Kubínová L, Travnik L, Eržen I. A novel method for evaluation of capillarity in human skeletal muscles from confocal 3D images. Microvasc Res. 2011;81:231–8. PubMed

Mathieu O, Cruz-Orive LM, Hoppeler H, Weibel ER. Estimating length density and quantifying anisotropy in skeletal muscle capillaries. J Microsc. 1983;131:131–46. PubMed

Egginton S, Johnston IA. An estimate of capillary anisotropy and determination of surface and volume densities of capillaries in skeletal muscles of the conger eel (Conger conger L.). Q J Exp Physiol. 1983;68:603–17. PubMed

Mathieu-Costello O. Capillary configuration in contracted muscles: comparative aspects. In: Gonzalez NC, Fedde MR. editors. Advances in Experimental Medicine and Biology: Vol. 227. Oxygen transfer from atmosphere to tissues. New York: Plenum Press; 1988. p. 229–36. PubMed

Mathieu-Costello O. Capillary tortuosity and degree of contraction or extension of skeletal muscles. Microvas Res. 1987;33:98–117. doi:10.1016/0026-2862(87)90010-0. PubMed DOI

Janáček J, Kreft M, Čebašek V, Eržen I. Correcting the axial shrinkage of skeletal muscle thick sections visualized by confocal microscopy. J Microsc. 2012;246:107–12. PubMed

Henssge C, Madea B, Gallenkemper E. Death time estimation in case work. II. Integration of different methods. Forensic Sci Int. 1988;39:77–87. PubMed

Collan Y, Salmenpera M. Electron microscopy of postmortem autolysis of rat muscle tissue. Acta Neuropathol. 1976;35:219–33. PubMed

MacNaughtan AF. A histological study of post mortem changes in the skeletal muscle of the fowl (Gallus domesticus). J Anat. 1978;125:461–76. PubMed PMC

Damjanovska M, Cvetko E, Hadzic A, Seliskar A, Plavec T, Mis K, Vuckovic Hasanbegovic I, Stopar Pintaric T. Neurotoxicity of perineural vs intraneural-extrafascicular injection of liposomal bupivacaine in the porcine model of sciatic nerve block. Anaesthesia. 2015;70:1418–26. PubMed PMC

Laitinen L. Griffonia simplicifolia lectins bind specifically to endothelial cells and some epithelial cells in mouse tissues. Histochem J. 1987;19:225–34. PubMed

Janáček J, Čebašek V, Kubínová L, Ribarič S, Eržen I. 3D visualization and measurement of capillaries supplying metabolically different fiber types in the rat extensor digitorum longus muscle during denervation and reinnervation. J Histochem Cytochem. 2009;57:437–47. PubMed PMC

Sanoudou D, Kang PB, Haslett JN, Han M, Kunkel LM, Beggs AH. Transcriptional profile of postmortem skeletal muscle. Physiol Genomics. 2004;16:222–8. PubMed

Mikami H, Terazawa K, Takatori T, Tokudome S, Tsukamoto T, Haga K. Estimation of time of death by quantification of melatonin in corpses. Int J Legal Med. 1994;107:42–51. PubMed

Bendall JR. The shortening of rabbit muscles during rigor mortis; its relation to the breakdown of adenosine triphosphate and creatine phosphate and to muscular contraction. J Physiol. 1951;114:71–88. PubMed PMC

Hooper AC, Hegarty PV. The percentage of passively contracted fibres in rigor skeletal muscles from different species. Comp Biochem Physiol A Comp Physiol. 1973;45:411–6. PubMed

Bendall JR. Post-mortem changes in muscle. In: Bourne GH, editor. The structure and function of muscle. New York: Academic Press; 1960. vol. 3 p. 217–24.

Voyle CA. Some observations on the histology of cold-shortened muscle. J Food Technol. 1969;4:275–81.

Beecher GR, Cassens RG, Hoekstra WG, Briskey EJ. Red and white fiber content and associated post-mortem properties of seven porcine muscles. J Food Sci. 1965;30:969–76.

Kobayashi M, Takemori S, Yamaguchi M. Differential rigor development in red and white muscle revealed by simultaneous measurement of tension and stiffness. Forensic Sci Int. 2004;140:79–84. PubMed

Mathieu-Costello O. Capillary tortuosity and degree of contraction or extension of skeletal muscles. Microvasc Res. 1987;33:98–117. PubMed

Mathieu-Costello O, Hoppeler H, Weibel ER. Capillary tortuosity in skeletal muscles of mammals depends on muscle contraction. J Appl Physiol (1985). 1989;66:1436–42. PubMed

Skeletal muscle myosin heavy chain expression and 3D capillary network changes in streptozotocin-induced diabetic female mice

3D analysis of capillary network in skeletal muscle of obese insulin-resistant mice