Training/detraining-induced gender specific functional adaptations of isolated rat heart

Radica Dragojlović Ružičić; Dragan Radovanović; Zvezdan Milanović; Anica Petković; Jovana Jeremić; Tamara Nikolić Тurnić; Isidora Milosavljević; Ivan Srejović; Vladimir Živković; Živko Krivokuća; Vladimir Jakovljević; Dušica Djordjević

doi:10.2298/VSP191127027D

Radica Dragojlović Ružičić University of Belgrade, High Medical College of Professional Studies “Milutin Milanković”, Belgrade, Serbia
Dragan Radovanović University of Niš, Faculty of Sport and Physical Education, Department of Physiology, Niš, Serbia
Zvezdan Milanović University of Priština/Kosovska Mitrovica, Faculty of Medical Sciences, Department of Physiology, Kosovska Mitrovica, Serbia
Anica Petković University of Kragujevac, Faculty of Medical Sciences, Department of Pharmacy, Kragujevac, Serbia
Jovana Jeremić University of Kragujevac, Faculty of Medical Sciences, Department of Pharmacy, Kragujevac, Serbia
Tamara Nikolić Тurnić University of Kragujevac, Faculty of Medical Sciences, Department of Pharmacy, Kragujevac, Serbia
Isidora Milosavljević University of Kragujevac, Faculty of Medical Sciences, Department of Pharmacy, Kragujevac, Serbia
Ivan Srejović University of Kragujevac, Faculty of Medical Sciences, Department of Physiology, Kragujevac, Serbia
Vladimir Živković University of Kragujevac, Faculty of Medical Sciences, Department of Physiology, Kragujevac, Serbia
Živko Krivokuća Garrison Ambulance Požega, Požega, Serbia
Vladimir Jakovljević University of Kragujevac, Faculty of Medical Sciences, Department of Physiology, Kragujevac, Serbia
Dušica Djordjević University of Kragujevac, Faculty of Medical Sciences, Department of Physiology, Kragujevac, Serbia

DOI: https://doi.org/10.2298/VSP191127027D

Keywords: adaptation, physiological, exercise, rats, heart, gender

Abstract

Background/Aim. Mechanisms responsible for the beneficial effects of aerobic exercise training on cardiovascular function are well known, but detraining effects on myocardial parameters have not been adequately elucidated. Therefore, the study aimed to determine the occurrence and speed of cardiac adaptation reversibility after the cessation of aerobic exercise and to reveal gender differences in achieved effects of training/detraining. Methods. Female and male Wistar albino rats were divided into the following groups: control, trained, and two detrained groups. Hearts were perfused according to the Langendorff technique and the following cardiodynamic parameters were determined: the maximum and minimum rate of pressure development in the left ventricle (dp/dt max and dp/dt min, respectively), systolic and diastolic left ventricular pressure (SLVP and DLVP, respectively), heart rate (HR), and coronary flow. Results. Training significantly reduced values of dp/dt max, dp/dt min, and SLVP in males and females, and coronary flow in males. Detraining caused a reversion of those changes, which was gender-specific. In females, levels of SLVP were higher after 4 weeks of detraining compred to training, and after 2 weeks of detraining. Values of SLVP were lower in both detraining periods compared to training in males. Males had higher coronary flow after 2 weeks of detraining. Simultaneously, coronary flow was reduced in the 4th week of detraining in females. Conclusion. By using a model of the isolated rat heart, the present study confirmed the existence of training-induced changes in cardiac function. Cessation of training was followed by the loss of those adaptations, faster in males than females.

References

Jakovljevic V, Djordjevic D. Physical Activity for the Prevention of Cardiovascular Diseases. Serb J Exp Clin Res 2016; 18(2): 99−109.

Kilic-Erkek O, Kilic-Toprak E, Kucukatay V, Bor-Kucukatay M. Exercise training and detraining modify hemorheological parameters of spontaneously hypertensive rats. Biorheology 2014; 51(6): 355−67.

Zachariah G, Alex AG. Exercise for prevention of cardiovascular disease: Evidence-based recommendations. J Clin Prev Cardiol 2017; 6(3): 109−14.

Nystoriak MA, Bhatnagar A. Cardiovascular Effects and Benefits of Exercise. Front Cardiovasc Med 2018; 5: 135.

Gielen S, Schuler G, Adams V. Cardiovascular effects of exercise training: molecular mechanisms. Circulation 2010; 122(12): 1221−38.

Kemi OJ, Wisløff U. Mechanisms of exercise-induced improvements in the contractile apparatus of the mammalian myocardium. Acta Physiol (Oxf) 2010; 199(4): 425-39.

Friedrich O, Wagner S, Battle AR, Schürmann S, Martinac B. Mechano-regulation of the Beating Heart at the Cellular Level—Mechanosensitive Channels in Normal and Diseased Heart. Prog Biophy Mol Biol 2012; 110(2−3): 226–38.

Oláh A, Kovács A, Lux Á, Tokodi M, Braun S, Lakatos BK, et al. Characterization of the dynamic changes in left ventricular morphology and function induced by exercise training and detraining. Int J Cardiol 2019; 277: 178−85.

Carneiro-Júnior MA, Quintão-Júnior JF, Drummond LR, Lavorato VN, Drummond FR, da Cunha DN, et al. The benefits of endurance training in cardiomyocyte function in hypertensive rats are reversed within four weeks of detraining. J Mol Cell Cardiol 2013; 57: 119−28.

Agarwal D, Dange RB, Vila J, Otamendi AJ, Francis J. Detraining differentially preserved beneficial effects of exercise on hypertension: effects on blood pressure, cardiac function, brain inflammatory cytokines and oxidative stress. PLoS One 2012; 7(12): e52569.

Mujika I, Padilla S. Cardiorespiratory and metabolic characteristics of detraining in humans. Med Sci Sports Exerc 2001; 33(3): 413−21.

Waring CD, Henning BJ, Smith AJ, Nadal-Ginard B, Torella D, Ellison GM. Cardiac adaptations from 4 weeks of intensity-controlled vigorous exercise are lost after a similar period of detraining. Physiol Rep 2015; 3(2): pii: e12302.

Bocalini DS, Carvalho EV, de Sousa AF, Levy RF, Tucci PJ. Exercise training-induced enhancement in myocardial mechanics is lost after 2 weeks of detraining in rats. Eur J Appl Physiol 2010; 109(5): 909−14.

Mujika I, Padilla S. Detraining: loss of training-induced physiological and performance adaptations. Part I: short term insufficient training stimulus. Sports Med 2000; 30(2): 79−87.

Parks RJ, Howlett SE. Sex differences in mechanisms of cardiac excitation-contraction coupling. Pflugers Arch 2013; 465(5): 747−63.

Foryst-Ludwig A, Kintscher U. Sex differences in exercise-induced cardiac hypertrophy. Pflugers Arch 2013; 465:731–737.

Bradic J, Dragojlovic Ruzicic R, Jeremic J, Petkovic A, Stojic I. Comparison of training and detraining on redox state of rats: gender specific differences. Gen Physiol Biophys 2018; 37:285-297.

Kulpa J, Chinnappareddy N, Pyle WG. Rapid changes in cardiac myofilament function following the acute activation of estrogen receptor-alpha.PLoS One 2012; 7:e41076.

Foryst-Ludwig A, Kreissl MC, Sprang C, Thalke B, Böhm C, Benz V. Sex differences in physiological cardiac hypertrophy are associated with exercise-mediated changes in energy substrate availability. Am J Physiol Heart Circ Physiol 2011; 301(1): H115−22.

Haines CD, Harvey PA, Leinwand LA. Estrogens mediate cardiac hypertrophy in a stimulus-dependent manner. Endocrinology 2012; 153(9): 4480–90.

Stojanovic Tosic JT, Jakovljevic VLJ, Zivkovic VV, Srejovic IM, Valdevit YJ, Radovanovic DS, et al. Biphasic response of cardiodynamic adaptations to swimming exercise in rats. Gen Physiol Biophys 2015; 34(3): 301−10.

Triposkiadis F, Ghiokas S, Skoularigis I, Kotsakis A, Giannakoulis I, Thanopoulos V, et al. Cardiac adaptation to intensive training in prepubertal swimmers. Eur J Clin Investig 2002; 32(1): 16−23.

Wang Y, Wisloff U, Kemi OJ. Animal models in the study of exercise-induced cardiac hypertrophy. Physiol Res 2010; 59(5): 633−44.

McMullen JR, Jennings GL. Differences between pathological and physiological cardiac hypertrophy: novel therapeutic strategies to treat heart failure. Clin Exp Pharmacol Physiol 2007; 34(4): 255– 62.

D'Souza A, Bucchi A, Johnsen AB, Logantha SJ, Monfredi O, Yanni J, et al. Exercise training reduces resting heart rate via downregulation of the funny channel HCN4. Nat Commun 2014; 5: 3775.

Ishida K, Moritani T, Itoh K. Changes in voluntary and electrically induced contractions during strength training and detraining. Eur J Appl Physiol Occup Physiol 1990; 60(4): 244−8.

Evangelista FS, Martuchi SE, Negrão CE, Brum PC. Loss of resting bradycardia with detraining is associated with intrinsic heart rate changes. Braz J Med Biol Res 2005; 38(7): 1141−6.

De Angelis K, Wichi RB, Jesus WR, Moreira ED, Morris M, Krieger EM, et al. Exercise training changes autonomic cardiovascular balance in mice. J Appl Physiol 2004; 96(6): 2174−8.

Blomqvist CG, Saltin B. Cardiovascular adaptations to physical training. Annu Rev Physiol 1983; 45: 169−89.

Yamamoto K, Miyachi M, Saitoh T, Yoshioka A, Onodera S. Effects of endurancetraining on resting and post-exercise cardiac autonomic control. Med Sci Sports Exerc 2001; 33(9): 1496−502.

Tibbits GF, Kashihara H, O’Reilly K. Na⁺–Ca²⁺ exchange in cardiac sarcolemma: modulation of C^a2+ affinity by exercise. Am J Physiol 1989; 256(3 Pt 1): C638−43.

Pierce GN, Sekhon PS, Meng HP, Maddaford TG. Effects of chronic swimming training on cardiac sarcolemmal function and composition. J Appl Physiol (1985) 1989; 66(4): 1715–21.

Pelliccia A, Maron BJ, De Luca R, Di Paolo FM, Spataro A, Culasso F. Remodeling of left ventricular hypertrophy in elite athletes after long-term deconditioning. Circulation 2002; 105(8): 944–9.

Craig BW, Martin G, Betts J, Lungren M, Lambret V, Kaiserauer S. The influence of training-detraining upon the heart, muscle and adipose tissue of female rats. Mech Agein Dev 1991; 57(1): 49–61.

Kemi OJ, Haram PM, Wisløff U, Ellingsen Ø. Aerobic fitness is associated with cardiomyocyte contractile capacity and endothelial in exercise training and detraining. Circulation 2004; 109(23): 2897–904.

Rodrigues AC, de Melo Costa J, Alves GB, Ferreira da Silva D, Picard MH, Andrade JL, et al. Left ventricular function after exercise training in young men. Am J Cardiol 2006; 97(7): 1089−92.

Konhilas JP, Maass AH, Luckey SW, Stauffer BL, Olson EN, Leinwand LA. Sex modifies exercise and cardiac adaptation in mice. Am J Physiol Heart Circ Physiol 2004; 287(6): H2768–76.

Ogawa T, Spina RJ, Martin WH, Kohrt WM, Schechtman KB, Holloszy JO, et al. Effects of aging, sex, and physical training on cardiovascular responses to exercise. Circulation 1992; 86(2): 494-503.

Mittendorfer B, Horowitz JF, Klein S. Effect of gender on lipid kinetics during endurance exercise of moderate intensity in untrained subjects. Am J Physiol Endocrinol Metab 2002; 283(1): E58−65.

Scheuer J, Malhotra A, Schaible TF, Capasso J. Effects of gonadectomy and hormonal replacement on rat hearts. Circ Res 1987; 61(1): 12−9.

Schaible TF, Penpargkul S, Scheuer J. Cardiac responses to exercise training in male and female rats. J Appl Physiol Respir Environ Exerc Physiol 1981; 50(1): 112−7.