Download PDF
Int J Sports Med 2024; 45(13): 958-967
DOI: 10.1055/a-2364-1514
Physiology & Biochemistry

Mitigation of Subsequent Ovariectomy Responses through Prior Exercise Training in Rats

Renata Kelly da Palma 
1   Facultad de Ciencias de la Salud de Manresa, UVic-UCC, Vic, Spain
2   Human Movement and Rehabilitation, Post-Graduation Program, Evangelical University of Goiás-UniEVANGÉLICA, Anápolis 75083-515, GO, Brazil
,
Kátia De Angelis
3   Departament of Physiology, Unifesp EPM, Sao Paulo, Brazil
,
Guilherme Lemos Shimojo
3   Departament of Physiology, Unifesp EPM, Sao Paulo, Brazil
,
Marina Rascio Henriques Dutra
3   Departament of Physiology, Unifesp EPM, Sao Paulo, Brazil
,
Camila Paixão dos Santos
3   Departament of Physiology, Unifesp EPM, Sao Paulo, Brazil
,
Nathalia Bernardes
4   Human Moviment Laboratory, Universidade São Judas Tadeu, Sao Paulo, Brazil
,
Andressa Bolsoni-Lopes
5   Department of Nursing, Federal University of Espírito Santo University Radio 104.7 FM, Vitoria, Brazil
,
Rui Curi
6   Interdisciplinary Post-Graduate Program in Health Sciences, Cruzeiro do Sul University, Sao Paulo, Brazil
,
João Lucas Gomes
7   School of Physical Education and Sports, USP, São Paulo, Brazil
,
Edilamar Menezes Oliveira
7   School of Physical Education and Sports, USP, São Paulo, Brazil
,
Maria Claudia Irigoyen
8   Heart Institute, Heart Institute – InCor, SÃO PAULO, Brazil
,
Christiane Malfitano
9   Department of Health Sciences, Federal University of Lavras, Lavras, Brazil
› Author Affiliations
› Further Information
Also available at
    Permissions and Reprints

Abstract

It is well known that cardiometabolic dysfunction gradually increases after menopause, and the sedentary lifestyle can aggravate this condition. Therefore, we compared the effects of aerobic exercise training during the premenopausal period and after ovariectomy (OVX) on metabolic, hemodynamic, and autonomic parameters in an experimental rat model of menopause. The female rats were divided into four groups: control (C), sedentary OVX (SO), trained OVX (TO), and previously trained OVX (PTO). The PTO group was trained for 4 weeks prior to+8 weeks after OVX, and the TO group trained only after OVX on a motor treadmill. Autonomic modulation was evaluated, white adipose tissue (WAT) was removed and weighed, and lipolysis was assessed. The citrate synthase activity in the soleus muscle was analyzed. The trained groups prevented the impairment of baroreceptor reflex sensitivity in relation to SO; however, only PTO reduced the low-frequency band of the pulse interval compared to SO. PTO reduced the weight of WAT compared to the other groups; lipolysis in PTO was similar to that in C. PTO preserved muscle metabolic injury in all types of fibers analyzed. In conclusion, this study suggests that exercise training should be recommended in a premenopausal model to prevent cardiometabolic and autonomic menopause-induced deleterious effects.

Keywords

exercise training - menopause - cardiometabolic state - autonomic dysfunctions


Publication History

Received: 13 July 2023

Accepted: 09 July 2024

Accepted Manuscript online:
10 July 2024

Article published online:
06 August 2024

© 2024. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Organization WH. A global brief on hypertension: Silent killer, global public health crisis: World Health Day 2013 (No. WHO/DCO/WHD/2013.2). World Health Organization; 2013. doi:
    CrossrefSearch in Google Scholar
  • 2 Witteman J, Grobbee DE, Kok FJ. et al. Increased risk of atherosclerosis in women after the menopause. BMJ 1989; 298: 642-644
    CrossrefPubMedSearch in Google Scholar
  • 3 Yang X-P, Reckelhoff JF. Estrogen, hormonal replacement therapy and cardiovascular disease. Curr Opin Nephrol Hypertens 2011; 20: 133
    CrossrefPubMedSearch in Google Scholar
  • 4 Dionne I, Kinaman K, Poehlman E. Sarcopenia and muscle function during menopause and hormone-replacement therapy. J Nutr Health Aging 2000; 4: 156-161
    PubMedSearch in Google Scholar
  • 5 Fonseca H, Powers S, Goncalves D. et al. Physical inactivity is a major contributor to ovariectomy-induced sarcopenia. Int J Sports Med 2012; 33: 268-278
    Thieme ConnectPubMedSearch in Google Scholar
  • 6 Dos-Santos A, do Nascimento Carvalho B, Da Costa-Santos N. et al. Effects of Exercise Intensity on Cardiometabolic Parameters of Ovariectomized Obese Mice. Int J Sports Med 2023; 44: 584-591
    Thieme ConnectPubMedSearch in Google Scholar
  • 7 Nascimento-Carvalho B, Dos-Santos A, Da Costa-Santos N. et al. Food readjustment plus exercise training improves cardiovascular autonomic control and baroreflex sensitivity in high-fat diet-fed ovariectomized mice. Physiol Rep 2023; 11: e15609
    CrossrefPubMedSearch in Google Scholar
  • 8 Dąbrowska-Galas M, Dąbrowska J, Ptaszkowski K. et al. High Physical Activity Level May Reduce Menopausal Symptoms. Medicina (Kaunas) 2019; 11: 466
    CrossrefPubMedSearch in Google Scholar
  • 9 Kilkenny C, Browne WJ, Cuthill IC. et al. Improving bioscience research reporting: The ARRIVE guidelines for reporting animal research. PLoS Biol 2010; 8: e1000412
    CrossrefPubMedSearch in Google Scholar
  • 10 Marcondes F, Bianchi F, Tanno A. Determination of the estrous cycle phases of rats: Some helpful considerations. Braz J Biol 2002; 62: 609-614
    CrossrefPubMedSearch in Google Scholar
  • 11 Irigoyen MC, Paulini J, Flores LJ. et al. Exercise training improves baroreflex sensitivity associated with oxidative stress reduction in ovariectomized rats. Hypertension 2005; 46: 998-1003
    CrossrefPubMedSearch in Google Scholar
  • 12 Brooks GA, White TP. Determination of metabolic and heart rate responses of rats to treadmill exercise. J Appl Physiol Respir Environ Exerc Physiol 1978; 45: 1009-1015
    PubMedSearch in Google Scholar
  • 13 Farah VdMA, De Angelis K, Joaquim LF. et al. Autonomic modulation of arterial pressure and heart rate variability in hypertensive diabetic rats. Clinics (Sao Paulo) 2007; 62: 477-482
    CrossrefPubMedSearch in Google Scholar
  • 14 Cerutti C, Barres C, Paultre C. Baroreflex modulation of blood pressure and heart rate variabilities in rats: Assessment by spectral analysis. Am J Physiol Heart Circ Physiol 1994; 266: H1993-H2000
    CrossrefPubMedSearch in Google Scholar
  • 15 Malliani A, Pagani M. Spectral analysis of cardiovascular variabilities in the assessment of sympathetic cardiac regulation in heart failure. Pharmacol Res 1991; 24: 43-53
    CrossrefPubMedSearch in Google Scholar
  • 16 Nordestgaard BG, Langsted A, Mora S, Kolovou G, Baum H, Bruckert E, Watts GF, Sypniewska G, Wiklund O, Borén J, Chapman MJ, Cobbaert C, Descamps OS, von Eckardstein A, Kamstrup PR, Pulkki K, Kronenberg F, Remaley AT, Rifai N, Ros E, Langlois M. European Atherosclerosis Society (EAS) and the European Federation of Clinical Chemistry and Laboratory Medicine (EFLM) joint consensus initiative. Fasting is not routinely required for determination of a lipid profile: Clinical and laboratory implications including flagging at desirable concentration cut-points – A joint consensus statement from the European Atherosclerosis Society and European Federation of Clinical Chemistry and Laboratory Medicine. Eur Heart J 2016; 37: 1944-58
    CrossrefPubMedSearch in Google Scholar
  • 17 Rodbell M, Jones AB. Metabolism of isolated fat cells III. The similar inhibitory action of phospholipase c (clostridium perfringens α toxin) and of insulin on lipolysis stimulated by lipolytic hormones and theophylline. J Biol Chem 1966; 241: 140-142
    PubMedSearch in Google Scholar
  • 18 Rodrigues LF, Pelozin BRA, da Silva Junior ND, Soci UPR, do Carmo EC, da Mota GFA, Cachofeiro V, Lahera V, Oliveira EM, Fernandes T. Angiotensin II Promotes Skeletal Muscle Angiogenesis Induced by Volume-Dependent Aerobic Exercise Training: Effects on miRNAs-27a/b and Oxidant-Antioxidant Balance. Antioxidants (Basel) 2022; 11: 651
    CrossrefPubMedSearch in Google Scholar
  • 19 Brooke MH, Kaiser KK. Muscle fiber types: How many and what kind?. Arch Neurol 1970; 23: 369-379
    CrossrefPubMedSearch in Google Scholar
  • 20 Lowry OH, Rosebrough NJ, Farr AL. et al. Protein measurement with the Folin phenol reagent. J Biol Chem 1951; 193: 265-275
    CrossrefPubMedSearch in Google Scholar
  • 21 Srere P. Citrate synthase. Methods Enzymol 1967; 13: 3-22
    CrossrefPubMedSearch in Google Scholar
  • 22 Reznick AZ, Packer L. Oxidative damage to proteins: Spectrophotometric method for carbonyl assay. Methods Enzymol 1994; 357-363
    CrossrefPubMedSearch in Google Scholar
  • 23 Evelson P, Travacio M, Repetto M. et al. Evaluation of total reactive antioxidant potential (TRAP) of tissue homogenates and their cytosols. Arch Biochem Biophys 2001; 388: 261-266
    CrossrefPubMedSearch in Google Scholar
  • 24 Aebi H. Catalase in vitro. Methods Enzymol 1984; 105: 121-126
    CrossrefPubMedSearch in Google Scholar
  • 25 Flohe L, Gunzler WA. Assays of glutathione peroxidase. Methods Enzymol 1984; 105: 114-121
    CrossrefPubMedSearch in Google Scholar
  • 26 Del Maestro R, McDonald W. Oxidative enzymes in tissue homogenates. Boca Raton, FL: CRC Press; 1985
    Search in Google Scholar
  • 27 Sherk VD, Jackman MR, Higgins JA. et al. Impact of Exercise and Activity on Weight Regain and Musculoskeletal Health Post-Ovariectomy. Med Sci Sports Exerc 2019; 51: 2465-2473
    CrossrefPubMedSearch in Google Scholar
  • 28 Ferreira JA, Foley AM, Brown M. Sex hormones differentially influence voluntary running activity, food intake and body weight in aging female and male rats. Eur J Appl Physiol 2012; 112: 3007-3018
    CrossrefPubMedSearch in Google Scholar
  • 29 Shimomura K, Shimizu H, Tsuchiya T. et al. Is leptin a key factor which develops obesity by ovariectomy?. Endocr J 2002; 49: 417-423
    CrossrefPubMedSearch in Google Scholar
  • 30 Landsberg L, Aronne LJ, Beilin LJ. et al. Obesity-related hypertension: Pathogenesis, cardiovascular risk, and treatment: A position paper of the Obesity Society and the American Society of Hypertension. J Clin Hypertens (Greenwich) 2013; 15: 14-33
    CrossrefPubMedSearch in Google Scholar
  • 31 Machi JF, da Silva Dias D, Freitas SC. et al. Impact of aging on cardiac function in a female rat model of menopause: Role of autonomic control, inflammation, and oxidative stress. Clin Interv Aging 2016; 11: 341
    CrossrefPubMedSearch in Google Scholar
  • 32 Maturana MA, Irigoyen MC, Spritzer PM. Menopause, estrogens, and endothelial dysfunction: Current concepts. Clinics (Sao Paulo) 2007; 62: 77-86
    CrossrefPubMedSearch in Google Scholar
  • 33 Wassmann S, Bäumer AT, Strehlow K. et al. Endothelial dysfunction and oxidative stress during estrogen deficiency in spontaneously hypertensive rats. Circulation 2001; 103: 435-441
    CrossrefPubMedSearch in Google Scholar
  • 34 Yung LM, Wong WT, Tian XY. et al. Inhibition of renin-angiotensin system reverses endothelial dysfunction and oxidative stress in estrogen deficient rats. PloS one 2011; 6: e17437
    CrossrefPubMedSearch in Google Scholar
  • 35 Braga VA, Couto GK, Lazzarin MC. et al. Aerobic exercise training prevents the onset of endothelial dysfunction via increased nitric oxide bioavailability and reduced reactive oxygen species in an experimental model of menopause. PloS one 2015; 10: e0125388
    CrossrefPubMedSearch in Google Scholar
  • 36 da Palma RK, Moraes-Silva IC, da Silva Dias D. et al. Resistance or aerobic training decreases blood pressure and improves cardiovascular autonomic control and oxidative stress in hypertensive menopausal rats. J Appl Physiol (1985) 2016; 121: 1032-1038
    CrossrefPubMedSearch in Google Scholar
  • 37 Conti FF, Brito Jde O, Bernardes N. et al. Positive effect of combined exercise training in a model of metabolic syndrome and menopause: Autonomic, inflammatory, and oxidative stress evaluations. Am J Physiol Regul Integr Comp Physiol 2015; 309: R1532-1539
    CrossrefPubMedSearch in Google Scholar
  • 38 Chen JQ, Delannoy M, Cooke C. et al. Mitochondrial localization of ERα and ERβ in human MCF7 cells. Am J Physiol Endocrinol Metab 2004; 286: E1011-E1022
    CrossrefPubMedSearch in Google Scholar
  • 39 Kadi F, Karlsson C, Larsson B. et al. The effects of physical activity and estrogen treatment on rat fast and slow skeletal muscles following ovariectomy. J Muscle Res Cell Motil 2002; 23: 335
    CrossrefPubMedSearch in Google Scholar
  • 40 Muka T, Vargas KG, Jaspers L. et al. Estrogen receptor β actions in the female cardiovascular system: A systematic review of animal and human studies. Maturitas 2016; 86: 28-43
    CrossrefPubMedSearch in Google Scholar