THE CAPILLARY PATTERN IN HUMAN MASSETER MUSCLE DURING AGEING
Keywords:3D analysis, capillaries, confocal microscopy, human, masseter muscle
AbstractThe effect of ageing on the capillary network in skeletal muscles has produced conflicting results in both, human and animals studies. Some of the inconsistencies are due to non-comparable and biased methods that were applied on thin transversal sections, especially in muscles with complicated morphological structures, such as in human masseter muscle. We present a new immunohistochemical method for staining capillaries and muscle fibres in 100 µm thick sections as well as novel approach to 3D visualization of capillaries and muscle fibres. Applying confocal microscopy and virtual 3D stereological grids, or tracing capillaries in virtual reality, length of capillaries within a muscle volume or length of capillaries adjacent to muscle fibre per fibre length, fibre surface or fibre volume were evaluated in masseter muscle of young and old subjects by an unbiased approach. Our findings show that anatomic capillarity is well maintained in masseter muscle in old subjects; however, vascular remodelling occurs with age, which could be a response to changed muscle function and age-related muscle fibre type transformations.
Basu R, Basu A, Nair KS (2002). Muscle changes in aging. J Nutr Health Aging 6:336-41.
Brown M (1987). Change in fiber size, not number, in ageing skeletal muscle. Age Ageing 16:244-8.
Brown M, Cotter Ma, Hudlická O, Vrbová G (1976). The effects of different patterns of muscle activity on capillary density, mechanical properties and structure of slow and fast rabbit muscles. Pflugers Arch 361:241-50.
Coggan AR, Spina RJ, King DS, Rogers MA, Brown M, Nemeth PM, et al. (1992). Histochemical and enzymatic comparison of the gastrocnemius muscle of young and elderly men and women. J Gerontol 47:B71–6.
Cotter M, Hudlická O, Pette D, Staudte H, Vrbová G (1973). Changes of capillary density and enzyme pattern in fast rabbit muscles during long-term stimulation. J Physiol-London 230:34P-35P.
Croley AN, Zwetsloot KA, Westerkamp LM, Ryan NA, Pendergast AM, Hickner RC, et al. (2005). Lower capillarization, VEGF protein, and VEGF mRNA response to acute exercise in the vastus ateralis muscle of aged vs. young women. J Appl Physiol 99:1872–79.
Cvetko E, Karen P, Janáček J, Kubínová L, Plasencia AL, Eržen I (2012). Human masseter muscle fibres from the elderly express less neonatal myosin than those of young adults. Anat Rec (Hoboken) 295:1364-72.
Cui L, Ju Y, Ding L, Trejo-Morales M, Olfert IM (2008). Arteriolar and venular capillary distribution in skeletal muscles of old rats. Gerontol A Biol Sci Med Sci 63:928-35.
Čebašek V, Eržen I, Vyhnal A, Janáček J, Ribarič S, Kubínová L (2010). The estimation error of skeletal muscle capillary supply is significantly reduced by 3D method. Microvasc Res 79:40-6.
Degens H, Turek Z, Hoofd LJC, Binkhorst RA (1994). Capillary proliferation related to fibre types in hypertrophied ageing rat m. plantaris. Adv Exp Med Biol 345:669-76.
Denis C, Chatard JC, Dormois D, Linossier MT, Geyssant A, Lacour JR (1986). Effects of endurance training on capillary supply of human skeletal muscle on two age groups (20 and 60 years). J Physiol 81:379-83.
Egginton S, Hudlická O (2000). Selective long-term electrical stimulation of fast glycolytic fibres increases capillary supply but not oxidative enzyme activity in rat skeletal muscles. Exp Physiol 85:567-73.
Eržen I, Janáček J, Kubínová L (2011). Characterization of the capillary network in skeletal muscles from 3D data. Physiol Res 60:1-13.
Frontera WR, Hughes VA, Fielding RA, Fiatarone MA, Evans WJ, Roubenhoff R (2000). Aging of skeletal muscle: a 12-year longitudinal study. J Appl Physiol 88:1321-6.
Gambino DR, Malmgren LT, Gacek RR (1990). Age-related changes in the neuromuscular junctions in the human posterior cricoarytenoid muscles: a quantitative study. Laryngoscope 100: 262–8.
Gedrange T, Walter B, Tetzlaff I, Kasper M, Schubert H, Harzer W, et al. (2003). Regional alterations in fiber type distribution, capillary density, and blood flow after lower jaw sagittal advancement in pig masticatory muscles. J Dent Res 82:570-4.
Hepple RT, Vogell JE (2004). Anatomic capillarization is maintained in relative excess of fibre oxidative capacity in some skeletal muscles of late middle-aged rats. J Appl Physiol 96: 2257–64.
Ishii H, Oota I, Takuma T, Inomata K (2001). Developmental expression of vascular endothelial growth factor in the masseter muscle of rats. Arch Oral Biol 46:77-82.
Janáček J, Cvetko E, Kubínová L, Travnik L, Eržen I (2011). A novel method for evaluation of capillarity in human skeletal muscles from confocal 3D images. Microvasc Res 81:231-8.
Janáček J, Kreft M, Čebašek V, Eržen I (2012). Correcting the axial shrinkage of skeletal muscle thick sections visualized by confocal microscopy. J Microsc 246:107-2.
Kadota E, Tanji K, Nishida S, Takahashi M, Maeda M, Hiruma S, et al. (1986). Lectin (UEA -1) reaction of capillary endothelium with reference to permeability in autopsied cases of cerebral infarction. Histol Histopathol 1:219-26.
Korfage JA, Koolstra JH, Langenbach GE, van Eijden TM (2005). Fiber-type composition of the human jaw muscles--(part 1) origin and functional significance of fiber-type diversity. J Dent Res 84:774-83.
Kubínová L, Janáček J, Ribarič S, Čebašek V, Eržen I (2001). Three-dimensional study of the capillary supply of skeletal muscle fibres using confocal microscopy. J Muscle Res Cell Moti. 22:217-27.
Lyon MJ, Steer LM, Malmgren LT (2007). Stereological estimates indicate that aging does not alter the capillary length density in the human posterior cricoarytenoid muscle. J Appl Physiol 103:1815-23.
Mathieu-Costello O, Ju Y, Trejo-Morales M, Cui L (2005). Greater capillary-fibre interface per fibre mitochondrial volume in skeletal muscles of old rats. J Appl Physiol 99:281–9.
Mitchell ML, Byrnes WC, Mazzeo RS (1991). A comparison of skeletal muscle morphology with training between young and old Fischer 344 rats. Mech Ageing Dev 58:21–35.
Nelissen-Vrancken HJ, Boudier HA, Daemen MJ, Smits JF (1993). Antihypertensive therapy and adaptive mechanisms in peripheral ischemia. Hypertension 22:780-8.
Nordstrom MA, Miles TS (1990). Fatigue of single motor units in human masseter. J Appl Physiol 68:26-34.
Proctor DN, Sinning WE, Walro JM, Sieck GC, Lemon PW (1995). Oxidative capacity of human muscle fiber types: effects of age and training status. J Appl Physiol 78:2033–8.
Ryan NA, Zwetsloot KA, Westerkamp LM, Hickner RC, Pofahl WE, Gavin TP (2006). Lower skeletal muscle capillarization and VEGF expression in aged vs. young men. J Appl Physiol 100:178–85.
Sjøgaard G (1982). Capillary supply and cross-sectional area of slow and fast twitch muscle fibres in man. Histochemistry 76:547-55.
Sjøgaard G, Savard G, Juel C (1988). Muscle blood flow during isometric activity and its relation to muscle fatigue. Eur J Appl Physiol Occup Physiol 57:327-35.
Stål P, Eriksson PO, Eriksson A, Thornell LE (1990). Enzyme-histochemical and morphological characteristics of muscle fibre types in the human buccinator and orbicularis oris. Arch Oral Biol 35:449-58.
Stål P, Eriksson PO, Thornell LE (1996). Differences in capillary supply between human oro-facial, masticatory and limb muscles. J Muscle Res Cell Motil 17:183–97.
Škorjanc D, Jaschinski F, Heine G, Pette D (1998). Sequential increases in capillarization and mitochondrial enzymes in low-frequency-stimulated rabbit muscle. Am J Physiol Cell Physiol 274:C810-18.
van Steenberghe D, De Vries JH, Hollander AP (1978). Resistance of jaw-closing muscles to fatigue during repetitive maximal voluntary clenching efforts in man. Arch Oral Biol 23:697-701.