Maternal aerobic running during mid or late gestation improves the quality of oogenesis and folliculogenesis in the ovary of neonatal rats: An experimental study


Background: Regular maternal exercise in pregnancy enhances the physiological, metabolic, and psychological health of mother and fetus.

Objective: To determine the effect of maternal aerobic running during mid or late gestation on plasma levels of estrogen and progesterone and the histological alterations in the ovary of neonatal rats.

Materials and Methods: Twenty-one female Wistar rats were randomly divided into experimental groups to exercises during the 2nd or 3rd wk of pregnancy (n = 14) and a control group (n = 7). After birth, the neonate’s blood was obtained and the estrogen and progesterone levels were evaluated. The ovaries were then removed and used for histological investigations and apoptic assessment.

Results: Higher concentrations of estrogen and progesterone were found in the neonates of the experimental groups (p = 0.001) compared to the control group. The experimental groups had a large ovarian diameter (2nd wk: p = 0.044; 3rd wk: p = 0.005) and angiogenesis (2nd wk: p = 0.003; 3rd wk: p = 0.001). In addition, significant enhancements were seen in the the experimental groups in terms of the number (2nd wk: p = 0.017; p = 0.035) and diameter (2nd wk: p = 0.046; 3rd wk: p = 0.004) of primordial follicles, as well as in the diameter of primary oocytes (2nd wk: p = 0.073; 3rd wk: p = 0.019) compared to the control group. Moreover, rats that exercised had a lower number of apoptotic primordial follicles than the control group (2nd wk: p = 0.001; 3rd wk: p = 0.001).

Conclusion: It was shown that maternal aerobic running can lead to increased plasma levels of estrogen and progesterone, also improved histological characteristics of the ovary in neonatal rats.

Key words: Apoptosis, Exercise, Neonatal, Oogenesis, Ovary, Rat.

[1] Kemper CH, Peters PW. Migration and proliferation of primordial germ cells in the rat. Teratology 1987; 36: 117– 124.

[2] Sun YCh, Sun XF, Dyce PW, Shen W, Chen H. The role of germ cell loss during primordial follicle assembly: A review of current advances. Int J Biol Sci 2017; 13: 449–457.

[3] Mottola MF, Davenport MH, Ruchat SM, Davies GA, Poitras VJ, Gray CE, et al. 2019 Canadian guideline for physical activity throughout pregnancy. Br J Sports Med 2018; 52: 1339–1346.

[4] Klein CP, Hoppe JB, Saccomori AB, Dos Santos BG, Sagini JP, Crestani MS, et al. Physical exercise during pregnancy prevents cognitive impairment induced by amyloid-β in adult offspring rats. Mol Neurobiol 2019; 56: 2022–2038.

[5] Labonte-Lemoyne E, Curnier D, Ellemberg D. Exercise during pregnancy enhances cerebral maturation in the newborn: A randomized controlled trial. J Clin Exp Neuropsychol 2017; 39: 347–354.

[6] Marcelino ThB, de Lemos Rodrigues PI, Klein CP, Dos Santos BG, Miguel PM, Netto CA, et al. Behavioral benefits of maternal swimming are counteracted by neonatal hypoxia-ischemia in the offspring. Behav Brain Res 2016; 312: 30–38.

[7] Evans ACO, Mossa F, Walsh SW, Scheetz D, Jimenez−Krassel F, Ireland JLH, et al. Effects of maternal environment during gestation on ovarian folliculogenesis and consequences for fertility in bovine offspring. Reprod Domest Anim 2012; 47 (Suppl.): 31–37.

[8] Shele G, Genkil J, Speelman D. A systematic review of the effects of exercise on hormones in women with polycystic ovary syndrome. J Funct Morphol Kinesiol 2020; 5: 35.

[9] Kaminski SL, Grazul-Bilska AT, Harris EK, Berg EP, Vonnahme KA. Impact of maternal physical activity during gestation on porcine fetal, neonatal, and adolescent ovarian development. Domest Anim Endocrinol 2014; 48: 56–61.

[10] Herring A, Donath A, Yarmolenko M, Uslar E, Conzen C, Kanakis D, et al. Exercise during pregnancy mitigates Alzheimer−like pathology in mouse offspring. FASEB J 2012; 26: 117–128.

[11] Guo Ch, Zhang G, Lin X, Zhao D, Zhang C, Mi Y. Reciprocal stimulating effects of bFGF and FSH on chicken primordial follicle activation through AKT and ERK pathway. Theriogenology 2019; 132: 27–35.

[12] Liu YX, Zhang Y, Li YY, Liu XM, Wang XX, Zhang CL, et al. Regulation of follicular development and differentiation by intra-ovarian factors and endocrine hormones. Front Biosci (Landmark Ed) 2019; 24: 983–993.

[13] Sloboda DM, Howie GJ, Pleasants A, Gluckman PD, Vickers MH. Pre-and postnatal nutritional histories influence reproductive maturation and ovarian function in the rat. PloS One 2009; 4: e6744.

[14] Yüksel M, Naziroğlu M, Özkaya MO. Long-term exposure to electromagnetic radiation from mobile phones and Wi- Fi devices decreases plasma prolactin, progesterone, and estrogen levels but increases uterine oxidative stress in pregnant rats and their offspring. Endocrine 2016; 52: 352–362.

[15] Loo DT. In situ detection of apoptosis by the TUNEL assay: An overview of techniques. Methods Mol Biol 2011; 683: 3–13.

[16] Mosavat M, Mohamed M, Mirsanjari MO. Effect of exercise on reproductive hormones in female athletes. International Journal of Sport and Exercise Science 2013; 5: 7–12.

[17] Zhang H, Nagaoka K, Usuda K, Nozawa K, Taya K, Yoshida M, et al. Estrogenic compounds impair primordial follicle formation by inhibiting the expression of proapoptotic Hrk in neonatal rat ovary. Biology of Reproduction 2016; 95: 78. 1–9.

[18] Wang JJ, Yu XW, Wu RY, Sun XF, Cheng ShF, Ge W, et al. Starvation during pregnancy impairs fetal oogenesis and folliculogenesis in offspring in the mouse. Cell Death Dis 2018; 9: 452.

[19] Enns DL, Tiidus PM. The influence of estrogen on skeletal muscle. Sports Medicine 2010; 40: 41–58.

[20] Moradpour R. The effects of regular aerobic exercise on primary dysmenorrhea in young girls. Journal of Physical Activity and Hormones 2019; 3: 67–82.

[21] Ketabipoor SM, Koushkie Jahromi M. Effect of aerobic exercise in water on serum estrogen and C-Reactive protein and body mass index level in obese and normal weight postmenopausal women. Women’s Health Bulletin 2015; 2: 1–6.

[22] Rahnama N, Bambaeichi E, Reilly T. Effects of training on estradiol, progesterone, luteinizing hormone and follicle stimulating hormone in female. Cell Mol Biol Lett 2004; 9 (Suppl.): 117–120.

[23] Xiong R, Ren X, Wang G, Chen G, Yang H, Yuan Q, et al. High intensity training induces alteration of the ubiquitinproteasome system gene expression profile and structural changes in the ovaries. Mol Med Rep 2012; 5: 1352–1356.

[24] Smith RL, Vernon KL, Kelley DE, Gibbons JR, Mortensen CJ. Impact of moderate exercise on ovarian blood flow and early embryonic outcomes in mares. J Anim Sci 2012; 90: 3770–3777.

[25] Bastu E, Zeybek U, Gurevin EG, Ozgor BY, Celik F, Okumus N, et al. Effects of irisin and exercise on metabolic parameters and reproductive hormone levels in high-fat diet-induced obese female mice. Reprod Sci 2018; 25: 281–291.

[26] Van Pelt DW, Guth LM, Horowitz JF. Aerobic exercise elevates markers of angiogenesis and macrophage IL- 6 gene expression in the subcutaneous adipose tissue of overweight-to-obese adults. J Appl Physiol 2017; 123: 1150–1159.

[27] Izzicupo P, D’Amico MA, Di Blasio A, Napolitano G, Nakamura FY, Di Baldassarre A, et al. Aerobic training improves angiogenic potential independently of vascular endothelial growth factor modifications in postmenopausal women. Front Endocrinol 2017; 8: 363.

[28] Qiu XH, Li ML, Li N, Sun Q, Zhou J, Ma RJ, et al. Maternal diabetes impairs the initiation of meiosis in murine female germ cells. Mol Med Rep 2017; 16: 5189–5194.

[29] Palstra AP, Crespo D, Van den Thillart GE, Planas JV. Saving energy to fuel exercise: Swimming suppresses oocyte development and downregulates ovarian transcriptomic response of rainbow trout Oncorhynchus mykiss. Am J Physiol Regul Integr Comp Physiol 2010; 299: R486–R499.

[30] Qiu S, Wu C, Lin F, Chen L, Huang Z, Jiang Z. Exercise training improved insulin sensitivity and ovarian morphology in rats with polycystic ovary syndrome. Horm Metab Res 2009; 41: 880–885.

[31] Seo H, Park ChH, Choi S, Kim W, Jeon BD, Ryu S. Effects of voluntary exercise on apoptosis and cortisol after chronic restraint stress in mice. J Exerc Nutrition Biochem 2016; 20: 16–23.