CC BY-NC-ND 4.0 · Journal of Morphological Sciences 2019; 36(03): 182-189
DOI: 10.1055/s-0039-1692209
Original Article
Thieme Revinter Publicações Ltda Rio de Janeiro, Brazil

Testosterone is Key to Increase the Muscle Capillary Density of Old and Trained Rats

Walter Krause Neto
1   Department of Physical Education, Laboratory of Morphoquantitative Studies and Immunohistochemistry, Universidade São Judas Tadeu, São Paulo, SP, Brazil
,
Wellington de Assis Silva
1   Department of Physical Education, Laboratory of Morphoquantitative Studies and Immunohistochemistry, Universidade São Judas Tadeu, São Paulo, SP, Brazil
,
Amanda dos Santos da Silva
1   Department of Physical Education, Laboratory of Morphoquantitative Studies and Immunohistochemistry, Universidade São Judas Tadeu, São Paulo, SP, Brazil
,
Adriano Polican Ciena
2   Department of Physical Education, Laboratory of Morphology and Physical Activity, Universidade Estadual Paulista “Júlio de Mesquita Filho”, Rio Claro, SP, Brazil
,
Romeu Rodrigues de Souza
1   Department of Physical Education, Laboratory of Morphoquantitative Studies and Immunohistochemistry, Universidade São Judas Tadeu, São Paulo, SP, Brazil
,
Patricia Oliva Carbone
1   Department of Physical Education, Laboratory of Morphoquantitative Studies and Immunohistochemistry, Universidade São Judas Tadeu, São Paulo, SP, Brazil
,
Carlos Alberto Anaruma
2   Department of Physical Education, Laboratory of Morphology and Physical Activity, Universidade Estadual Paulista “Júlio de Mesquita Filho”, Rio Claro, SP, Brazil
,
Eliane Florencio Gama
1   Department of Physical Education, Laboratory of Morphoquantitative Studies and Immunohistochemistry, Universidade São Judas Tadeu, São Paulo, SP, Brazil
› Author Affiliations
Further Information

Publication History

11 March 2019

01 May 2019

Publication Date:
06 June 2019 (online)

Abstract

Introduction It is indicated that aging reduces muscular vascularity. Thus, strategies that aim to reverse or decrease the progression of these changes are suggested. Therefore, the present study aimed to analyze the blood capillary density of the plantaris muscle (PL) of aged rats submitted to strength training and exogenous testosterone use.

Methods A total of 30 rats were divided equally into the following groups: EA: 20 months old; OLD: 24 months old; OLD + S: testosterone; ST: strength training; and ST + S: strength training + testosterone. Strength training was performed 3 times a week for 15 weeks. Testosterone administration was performed by the intraperitoneal method 2 times a week at a dose of 10mg/kg. All of the morphological parameters were analyzed using morphoquantitative techniques.

Results A significant increase in the capillaries numerical density of the OLD + S and ST + S groups. The OLD + S and ST + S groups demonstrated a higher ratio of capillaries per myofiber than the EA, OLD and ST groups. The OLD and ST groups had a higher ratio than the EA group. The OLD + S, ST and ST + S groups presented a statistically significant increase in the cross-sectional area in the type I fibers when compared with the EA and OLD groups. However, the ST group showed a significant increase compared with the OLD group. In type II fibers, the ST and ST + S groups showed a greater cross-sectional area than the EA group. As for the mean cross-sectional area, the ST and ST + S groups presented significantly larger areas than the other groups.

Conclusion Anabolic steroid administration is crucial to increase the blood capillary density of the plantaris muscle of old rats, independently of the effects of strength training.

 
  • References

  • 1 Beaudart C, Locquet M, Reginster JY, Delandsheere L, Petermans J, Bruyère O. Quality of life in sarcopenia measured with the SarQoL®: impact of the use of different diagnosis definitions. Aging Clin Exp Res 2017; ;••• DOI: 10.1007/s40520-017-0866-9.
  • 2 Soares AV, Marcelino E, Maia KC, Borges Junior NG. Relação entre mobilidade funcional e dinapenia em idosos com fragilidade. Einstein (Sao Paulo) 2017; 15 (03) 278-282
  • 3 Nicholson CJ, Sweeney M, Robson SC, Taggart MJ. Estrogenic vascular effects are diminished by chronological aging. Sci Rep 2017; 7 (01) 12153 . Doi: 10.1038/s41598-017-12153-5
  • 4 Xu X, Wang B, Ren C. , et al. Recent Progress in Vascular Aging: Mechanisms and Its Role in Age-related Diseases. Aging Dis 2017; 8 (04) 486-505
  • 5 Osuka Y, Fujita S, Kitano N. , et al. Effects of Aerobic and Resistance Training Combined with Fortified Milk on Muscle Mass, Muscle Strength, and Physical Performance in Older Adults: A Randomized Controlled Trial. J Nutr Health Aging 2017; 21 (10) 1349-1357 . Doi: 10.1007/s12603-016-0864-1
  • 6 Søgaard D, Lund MT, Scheuer CM. , et al. High-intensity interval training improves insulin sensitivity in older individuals. Acta Physiol (Oxf) 2017; ;•••: [Epub ahead of print] DOI: 10.1111/apha.13009.
  • 7 Loyola WS, Camillo CA, Torres CV, Probst VS. Effects of an exercise model based on functional circuits in an older population with different levels of social participation. Geriatr Gerontol Int 2017; ;••• DOI: 10.1111/ggi.13167.
  • 8 Holloszy JO, Coyle EF. Adaptations of skeletal muscle to endurance exercise and their metabolic consequences. J Appl Physiol 1984; 56 (04) 831-838
  • 9 Prior BM, Yang HT, Terjung RL. What makes vessels grow with exercise training?. J Appl Physiol (1985) 2004; 97 (03) 1119-1128
  • 10 Rossman MJ, Kaplon RE, Hill SD. , et al. Endothelial cell senescence with aging in healthy humans: prevention by habitual exercise and relation to vascular endothelial function. Am J Physiol Heart Circ Physiol 2017; 313 (05) H890-H895 . Doi: 10.1152/ajpheart.00416.2017
  • 11 Krause Neto W, Gama FE. Strength training and anabolic steroid do not affect muscle capillarization of middle-aged rats. Rev Bras Med Esporte 2017; 23 (02) 137-141
  • 12 Hudlicka O, Brown M, Egginton S. Angiogenesis in skeletal and cardiac muscle. Physiol Rev 1992; 72 (02) 369-417
  • 13 Webb CM, Adamson DL, de Zeigler D, Collins P. Effect of acute testosterone on myocardial ischemia in men with coronary artery disease. Am J Cardiol 1999; 83 (03) 437-439 , A9
  • 14 Hayward CS, Kelly RP, Collins P. The roles of gender, the menopause and hormone replacement on cardiovascular function. Cardiovasc Res 2000; 46 (01) 28-49
  • 15 Gonçalves L, de Souza RR, Maifrino LB. , et al. Resistance exercise and testosterone treatment alters the proportion of numerical density of capillaries of the left ventricle of aging Wistar rats. Aging Male 2014; 17 (04) 243-247
  • 16 Deus APL, Bassi D, Simões RP. , et al. MMP(-2) expression in skeletal muscle after strength training. Int J Sports Med 2012; 33 (02) 137-141
  • 17 Krause Neto W, Silva WA, Ciena AP. , et al. Total training load may explain similar strength gains and muscle hypertrophy seen in aged rats submitted to resistance training and anabolic steroids. Aging Male 2017; ;•••: 1-12 . Doi: 10.1080/13685538.2017.1365832
  • 18 Harris MB, Slack KN, Prestosa DT, Hryvniak DJ. Resistance training improves femoral artery endothelial dysfunction in aged rats. Eur J Appl Physiol 2010; 108 (03) 533-540
  • 19 Tanasov VS, Krause Neto W, Gonçalves L, Maifrino LBM, De Sousa RR, Gama EF. Use of Anabolic Steroid Altered the Liver Morphology of Rats. Int J Morphol 2014; 32 (03) 756-760
  • 20 Harris BA. The influence of endurance and resistance exercise on muscle capillarization in the elderly: a review. Acta Physiol Scand 2005; 185 (02) 89-97
  • 21 Hepple RT, Mathieu-Costello O. Estimating the size of the capillary-to-fiber interface in skeletal muscle: a comparison of methods. J Appl Physiol (1985) 2001; 91 (05) 2150-2156
  • 22 Andersen P. Capillary density in skeletal muscle of man. Acta Physiol Scand 1975; 95 (02) 203-205
  • 23 Degens H. Age-related changes in the microcirculation of skeletal muscle. Adv Exp Med Biol 1998; 454: 343-348
  • 24 Frontera WR, Hughes VA, Fielding RA, Fiatarone MA, Evans WJ, Roubenoff R. Aging of skeletal muscle: a 12-yr longitudinal study. J Appl Physiol (1985) 2000; 88 (04) 1321-1326
  • 25 Chilibeck PD, Paterson DH, Cunningham DA, Taylor AW, Noble EG. Muscle capillarization O2 diffusion distance, and VO2 kinetics in old and young individuals. J Appl Physiol (1985) 1997; 82 (01) 63-69
  • 26 Coggan AR, Spina RJ, Rogers MA. , et al. Histochemical and enzymatic characteristics of skeletal muscle in master athletes. J Appl Physiol (1985) 1990; 68 (05) 1896-1901
  • 27 Desaki J, Nishida N. Structural changes of microvessels in the extensor digitorum longus muscle of the aged rat. J Electron Microsc (Tokyo) 2007; 56 (04) 157-162
  • 28 Desaki J, Oki S, Ezaki T. Remodelling of capillary networks around muscle fibres in the extensor digitorum longus muscle of the normal aged rat. J Electron Microsc (Tokyo) 2002; 51 (03) 183-194
  • 29 Muller-Delp Judy, Spier SA, Ramsey MW. , et al. Effects of aging on vasoconstrictor and mechanical properties of rat skeletal muscle arterioles. Am J Physiol Heart Circ Physiol 2002; 282: H1843-H1854 First published December 6, 2001. Doi: 10.1152/ajpheart.00666.2001
  • 30 Hagerman FC, Walsh SJ, Staron RS. , et al. Effects of high-intensity resistance training on untrained older men. I. Strength, cardiovascular, and metabolic responses. J Gerontol A Biol Sci Med Sci 2000; 55 (07) B336-B346
  • 31 Dimauro J, Balnave RJ, Shorey CD. Effects of anabolic steroids and high intensity exercise on rat skeletal muscle fibres and capillarization. A morphometric study. Eur J Appl Physiol Occup Physiol 1992; 64 (03) 204-212
  • 32 Littleton-Kearney M, Hurn PD. Testosterone as a modulator of vascular behavior. Biol Res Nurs 2004; 5 (04) 276-285 . Doi: 10.1177/1099800403262927
  • 33 Cai J, Hong Y, Weng C, Tan C, Imperato-McGinley J, Zhu Y-S. Androgen stimulates endothelial cell proliferation via an androgen receptor/VEGF/cyclin A-mediated mechanism. Am J Physiol Heart Circ Physiol 2011; 300 (04) H1210-H1221 . Doi: 10.1152/ajpheart.01210.2010
  • 34 Kovacheva EL, Hikim AP, Shen R, Sinha I, Sinha-Hikim I. Testosterone supplementation reverses sarcopenia in aging through regulation of myostatin, c-Jun NH2-terminal kinase, Notch, and Akt signaling pathways. Endocrinology 2010; 151 (02) 628-638
  • 35 Griggs RC, Kingston W, Jozefowicz RF, Herr BE, Forbes G, Halliday D. Effect of testosterone on muscle mass and muscle protein synthesis. J Appl Physiol (1985) 1989; 66 (01) 498-503
  • 36 Snijders T, Verdijk LB, van Loon LJ. The impact of sarcopenia and exercise training on skeletal muscle satellite cells. Ageing Res Rev 2009; 8 (04) 328-338
  • 37 Bhasin S, Storer TW, Berman N. , et al. The effects of supraphysiologic doses of testosterone on muscle size and strength in normal men. N Engl J Med 1996; 335 (01) 1-7
  • 38 Bhasin S, Storer TW, Javanbakht M. , et al. Testosterone replacement and resistance exercise in HIV-infected men with weight loss and low testosterone levels. JAMA 2000; 283 (06) 763-770
  • 39 Willoughby DS, Taylor L. Effects of sequential bouts of resistance exercise on androgen receptor expression. Med Sci Sports Exerc 2004; 36 (09) 1499-1506