Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-14T06:43:03.590Z Has data issue: false hasContentIssue false

Effect of postnatal overfeeding on the male and female Wistar rat reproductive parameters

Published online by Cambridge University Press:  03 June 2019

V. M. G. Costa*
Affiliation:
Reproductive Biology Center, Federal University of Juiz de Fora, Juiz de Fora, Brazil
A. E. Andreazzi
Affiliation:
Laboratory of Physiology, Department of Physiology, Federal University of Juiz de Fora, Juiz de Fora, Brazil
M. Bolotari
Affiliation:
Reproductive Biology Center, Federal University of Juiz de Fora, Juiz de Fora, Brazil
C. G. Lade
Affiliation:
Reproductive Biology Center, Federal University of Juiz de Fora, Juiz de Fora, Brazil
M. O. Guerra
Affiliation:
Reproductive Biology Center, Federal University of Juiz de Fora, Juiz de Fora, Brazil
V. M. Peters
Affiliation:
Reproductive Biology Center, Federal University of Juiz de Fora, Juiz de Fora, Brazil
*
Address for correspondence: V. M. G. Costa, Reproductive Biology Center, Federal University of Juiz de Fora, Juiz de Fora, Brazil. Email: vini.mgcosta@gmail.com

Abstract

Overweight/obesity has become a worldwide epidemic, and factors such as a sedentary lifestyle and inadequate eating habits directly contribute to the development of this condition. Studies indicate that rapid weight gain at critical development stages, such as the lactation period, is associated with the development of obesity, cardiovascular diseases, and diabetes in the long term. In addition to metabolic changes during adulthood, overweight/obesity may influence reproductive function of the population. In this context, the present study aimed to evaluate postnatal overfeeding effects on male and female Wistar rat reproductive parameters. Postnatal overfeeding was induced by applying the litter reduction method for both sexes. Forty animals were used, divided into four groups: two with normal litters (NL♂ and NL♀) and two with small litters (SL♂ and SL♀). The males were euthanized at 90 days of age, on the same date the females were mated. Females were also euthanized after the 20-day gestation. Metabolic and reproductive variables were analyzed. Regarding males, SL animals showed increased body weight, adiposity, and decreased relative weight of the seminal vesicle, prostate, and epididymis as well as changes in the ITT and OGTT glycemic tests. Concerning females, SL animals presented increased body weight, relative perigonadal fat weight, glucose intolerance as well as modify the vaginal opening and increased weight of female pup. The litter reduction method was efficient in leading to metabolic and reproductive alterations in male and female Wistar rat.

Type
Original Article
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

WHO. Global status report on noncommunicable diseases 2014. World Health. 2014; 173.Google Scholar
Committee P, Society A. Obesity and reproduction: A committee opinion. Fertil Steril. 2015; 104(5), 11161126. doi: 10.1016/j.fertnstert.2015.08.018CrossRefGoogle Scholar
Cesaretti, MLR, Kohlmann Junior, O. Modelos experimentais de resistência à insulina e obesidade: lições aprendidas. Arq Bras Endocrinol Metabol. 2006; 50(2), 190197.CrossRefGoogle Scholar
Bei, F, Jia, J, Jia, Y, et al. Long-term effect of early postnatal overnutrition on insulin resistance and serum fatty acid profiles in male rats. Lipids Health Dis. 2015; 112. doi: 10.1186/s12944-015-0094-2Google ScholarPubMed
Plagemann, A, Harder, T, Rake, A, et al. Perinatal elevation of hypothalamic insulin, acquired malformation of hypothalamic galaninergic neurons, and syndrome X-like alterations in adulthood of neonatally overfed rats. Brain Res. 1999; 836(1-2), 146155.CrossRefGoogle ScholarPubMed
Zambrano, E, Guzmán, C, Rodríguez-González, GL, Durand-Carbajal, M, Nathanielsz, PW. Fetal programming of sexual development and reproductive function. Mol Cell Endocrinol. 2014; 382, 538549.CrossRefGoogle ScholarPubMed
Palmer, NO, Bakos, HW, Fullston, T, Lane, M. Impact of obesity on male fertility, sperm function and molecular composition. Spermatogenesis. 2012; 2(4), 253263.CrossRefGoogle ScholarPubMed
Sánchez-Garrido, MA, Ruiz-pino, F, Manfredi-lozano, M, et al. Metabolic and gonadotropic impact of sequential obesogenic insults in the female: influence of the loss of ovarian secretion. Endocrinology. 2015; 156, 29842998.CrossRefGoogle ScholarPubMed
Silva, A, Santos, M, Franca, S, et al. Acute and subchronic antihyperglycemic activities of Bowdichia virgilioides roots in non-diabetic and diabetic rats. J Intercult Ethnopharmacol. 2015; 4(1), 1.CrossRefGoogle ScholarPubMed
Hirata, AE, Alvarez-Rojas, F, Campello Carvalheira, JB, De Oliveira Carvalho, CR, Dolnikoff, MS, Abdalla Saad, MJ. Modulation of IR/PTP1B interaction and downstream signaling in insulin sensitive tissues of MSG-rats. Life Sci. 2003; 73(11), 13691381.CrossRefGoogle ScholarPubMed
Raupp, MA. Resolução normativa n° 13, de 20 desetembro de 2013. 2018; 119.Google Scholar
Lloyd, MH, Wolfensohn, SE. Practical use of distress scoring systems in the application of humane endpoints. Lloydia (Cincinnati). 1996; 4853.Google Scholar
Yamasaki, K, Sawaki, M, Noda, S, Muroi, T, Takatsuki, M. Preputial separation and glans penis changes in normal growing Crj: CD (SD) IGS rats. Reprod Toxicol. 2001; 15(5), 533536.CrossRefGoogle ScholarPubMed
WHO. Examination and processing of human semen. WHO Press. 2010; 286.Google Scholar
Seed, J, Chapin, RE, Clegg, ED, et al. Methods for assessing sperm motility, morphology, and counts in the rat, rabbit, and dog: a consensus report. Reprod Toxicol. 1996; 10(3), 237244.CrossRefGoogle ScholarPubMed
Oshio, LT, Ribeiro, CCT, Marques, RM, Guerra, MDO, da Matta, SLP, Reis, JEDP. Effect of Ginkgo biloba extract on sperm quality, serum testosterone concentration and histometric analysis of testes from adult Wistar rats. J Med Plants Res. 2015; 9(5), 122131.Google Scholar
Yakubu, MT, Adeshina, AO, Oladiji, AT, et al. Abortifacient potential of aqueous extract of Senna alata leaves in rats. J Reprod Contracept. 2010; 21(3), 163177.Google Scholar
Balasinor, N, Gill-Sharma, MK, Parte, P, D’souza, S, Kedia, N, Juneja, HS. Effect of paternal administration of an antiestrogen, tamoxifen on embryo development in rats. Mol Cell Endocrinol. 2002; 190(1-2), 159166.CrossRefGoogle ScholarPubMed
Stettler, N, Stallings, VA, Troxel, AB, et al. Weight gain in the first week of life and overweight in adulthood: a cohort study of European American subjects fed infant formula. Circulation. 2005; 111(15), 18971903.CrossRefGoogle ScholarPubMed
Boullu-Ciocca, S, Dutour, A, Guillaume, V, Achard, V, Oliver, C, Grino, M. Postnatal diet-induced obesity in rats upregulates systemic and adipose tissue glucocorticoid metabolism during development and in adulthood: its relationship with the metabolic syndrome. Diabetes. 2005; 54(1), 197203.CrossRefGoogle ScholarPubMed
Collden, G, Balland, E, Parkash, J, et al. Neonatal overnutrition causes early alterations in the central response to peripheral ghrelin. Mol Metab. 2015; 4, 1524.CrossRefGoogle ScholarPubMed
Kokkoris, P, Pi-Sunyer, FX. Obesity and endocrine disease. Endocrinol Metab Clin North Am. 2003; 32(4), 895914.CrossRefGoogle ScholarPubMed
Vieira, JGH, Nakamura, OH, Ferrer, CM, Tachibana, TT, Endo, MHK, Carvalho, VM. Importância da metodologia na dosagem de testosterona sérica: comparação entre um imunoensaio direto e um método fundamentado em cromatografia líquida de alta performance e espectrometria de massa em tandem (HPLC/MS-MS). Arq Bras Endocrinol Metabol. 2008; 52(6), 10501055.CrossRefGoogle Scholar
Environment Directorate Joint Meeting of the Chemicals Committee. The working party on chemicals, pesticides and biotechnology. Env/Jm/Mono. 2001; 11, 126.Google Scholar
Cabler, S, Agarwal, A, Flint, M, Du Plessis, SS. Obesity: modern man’s fertility nemesis. Asian J Androl. 2010; 12: 480489.CrossRefGoogle ScholarPubMed
Jensen, TK, Andersson, AM, Jørgensen, N, et al. Body mass index in relation to semen quality and reproductive hormones among 1,558 Danish men. Fertil Steril. 2004; 82(4), 863870.CrossRefGoogle ScholarPubMed
Aggerholm, AS, Thulstrup, AM, Toft, G, Ramlau-Hansen, CH, Bonde, JP. Is overweight a risk factor for reduced semen quality and altered serum sex hormone profile? Fertil Steril. 2008; 90(3), 619626.CrossRefGoogle ScholarPubMed
Paasch, U, Grunewald, S, Kratzsch, J, Glander, HJ. Obesity and age affect male fertility potential. Fertil Steril. 2010; 94(7), 28982901. doi: 10.1016/j.fertnstert.2010.06.047.CrossRefGoogle ScholarPubMed
Bakos, HW, Henshaw, RC, Mitchell, M, Lane, M. Paternal body mass index is associated with decreased blastocyst development and reduced live birth rates following assisted reproductive technology. Fertil Steril. 2011; 95(5), 17001704. doi: 10.1016/j.fertnstert.2010.11.044.CrossRefGoogle ScholarPubMed
MacDonald, AA, Herbison, GP, Showell, M, Farquhar, CM. The impact of body mass index on semen parameters and reproductive hormones in human males: a systematic review with meta-analysis. Hum Reprod. 2010;16(3), 293311.Google ScholarPubMed
Sheng, H, Balonan, LC. Perinatal feedings adversely affect lipogenic activities but not glucose handling in adult rats. Pediatric Research. 2000; 48(5), 668673.Google Scholar
de Souza, Rodrigues Cunha AC, Pereira, RO, dos Santos Pereira, MJ, et al. Long-term effects of overfeeding during lactation on insulin secretion – the role of GLUT-2. J Nutr Biochem. 2009; 20(6), 435442. doi: 10.1016/j.jnutbio.2008.05.002.CrossRefGoogle Scholar
Stothard, KJ, Tennant, PWG, Bell, R, Rankin, J. Maternal overweight and obesity and the risk of congenital anomalies. Jama. 2009; 301(6), 636.CrossRefGoogle ScholarPubMed
Johansson, S, Villamor, E, Altman, M, Bonamy, A-KE, Granath, F, Cnattingius, S. Maternal overweight and obesity in early pregnancy and risk of infant mortality: a population-based cohort study in Sweden. Bmj. 2014; 349, 112.CrossRefGoogle ScholarPubMed
Bihoreau, MT, Ktorza, A, Kinebanyan, MF, Picon, L. Impaired glucose homeostasis in adult rats from hyperglycemic mothers. Diabetes. 1986; 35(9), 979984.CrossRefGoogle ScholarPubMed
Caron, E, Ciofi, P, Prevot, VBS. Alteration in Neonatal Nutrition Causes Perturbations in Hypothalamic Neural Circuits Controlling Reproductive Function. J Neurosci. 2013; 27(3), 200207.Google Scholar
Biro, FM, Khoury, P, Morrison, JA, et al. Influence of obesity on timing of puberty. Int J Androl. 2006; 29, 272277.CrossRefGoogle ScholarPubMed
Solorzano, CMB, Mccartney, CR. Obesity and the pubertal transition in girls and boys. Reproduction. 2011; 140(3), 399410.CrossRefGoogle Scholar
Donnelly, JE, Blair, SN, Jakicic, JM, Manore, MM, Rankin, JW, Smith, BK. Appropriate physical activity intervention strategies for weight loss and prevention of weight regain for adults. Med Sci Sports Exerc. 2009; 41(2), 459471.CrossRefGoogle ScholarPubMed
Brewer, CJ, Balen, AH. Focus on obesity the adverse effects of obesity on conception and implantation. Reproduction. 2010; 140, 347364.Google Scholar
Regnault, N, Gillman, MW, Rifas-Shiman, SL, Eggleston, E, Oken, E. Sex-specific associations of gestational glucose tolerance with childhood body composition. Diabetes Care. 2013; 36(10), 30453053.CrossRefGoogle ScholarPubMed
Mandò, C, Calabrese, S, Mazzocco, MI, et al. Sex specific adaptations in placental biometry of overweight and obese women. Placenta. 2016; 38: 17.CrossRefGoogle ScholarPubMed
Wang, GH. The changes in the amount of daily food-intake of the albino rat during pregnancy and lactation. American Physiological Society. 1925; 736741.CrossRefGoogle Scholar
Asarian, L, Geary, N. Sex differences in the physiology of eating. AJP Regul Integr Comp Physiol. 2013; 305(11), 127. Retrieved from http://ajpregu.physiology.org/cgi/doi/10.1152/ajpregu.00446.2012.Google ScholarPubMed
Santos, F, Peters, AH, Otte, AP, Reik, W, Dean, W. Dynamic chromatin modifications characterise the first cell cycle in mouse embryos. Dev Biol. 2005; 280(1), 225236.CrossRefGoogle ScholarPubMed
Sanz, LA, Kota, SK, Feil, R. Genome-wide DNA demethylation in mammals. Genome Biol. 2010; 11(3), 14.CrossRefGoogle ScholarPubMed
Van Abeelen, AFM, De Rooij, SR, Osmond, C, Painter, RC, Veenendaal, MVE, Bossuyt, PMM, et al. The sex-specific effects of famine on the association between placental size and later hypertension. Placenta. 2011; 32(9), 694698. doi: 10.1016/j.placenta.2011.06.012.CrossRefGoogle ScholarPubMed
Kim, DW, Young, SL, Grattan, DR, Jasoni, CL. Obesity during pregnancy disrupts placental morphology, cell proliferation, and inflammation in a sex-specific manner across gestation in the mouse. Biol Reprod. 2014; 90(6), 111.CrossRefGoogle Scholar
Taylor, PD. Impaired glucose homeostasis and mitochondrial abnormalities in offspring of rats fed a fat-rich diet in pregnancy. AJP Regul Integr Comp Physiol. 2004; 288(1), 134139.CrossRefGoogle ScholarPubMed
Muralimanoharan, S, Guo, C, Myatt, L and Maloyan, A. Sexual dimorphism in miR-210 expression and mitochondrial dysfunction in the placenta with maternal obesity. Int J Obes (Lond). 2012; 39(2), 123130.Google Scholar
Saben, JL, Boudoures, AL, Asghar, Z, et al. Maternal metabolic syndrome programs mitochondrial dysfunction via germline changes across three generations. Cell Rep. 2017; 16(1), 18.CrossRefGoogle Scholar
Zhou, Z, Ribas, V, Rajbhandari, P, et al. Estrogen receptor protects pancreatic cells from apoptosis by preserving mitochondrial function and suppressing endoplasmic reticulum stress. J Biol Chem. 2018; 293(13), 47354751.CrossRefGoogle ScholarPubMed