Hostname: page-component-848d4c4894-hfldf Total loading time: 0 Render date: 2024-05-29T08:00:16.677Z Has data issue: false hasContentIssue false
  • English
  • Français

Biometric, nutritional, biochemical, and cardiovascular outcomes in male rats submitted to an experimental model of early weaning that mimics mother abandoning

Published online by Cambridge University Press:  09 September 2020

Rogério Barbosa de Magalhães Barros ,
Thaís Alvim-Silva ,
Júlia Raquel Nunes de Souza ,
Emiliana Barbosa Marques ,
Nazareth N. Rocha ,
Fernanda C. F. Brito  and
Christianne B. V. Scaramello Open the ORCID record for Christianne B. V. Scaramello [Opens in a new window]
Rogério Barbosa de Magalhães Barros
Affiliation:
Fluminense Federal University, Niterói, Rio de Janeiro, Brazil
Thaís Alvim-Silva
Affiliation:
Fluminense Federal University, Niterói, Rio de Janeiro, Brazil
Júlia Raquel Nunes de Souza
Affiliation:
Fluminense Federal University, Niterói, Rio de Janeiro, Brazil
Emiliana Barbosa Marques
Affiliation:
Fluminense Federal University, Niterói, Rio de Janeiro, Brazil
Nazareth N. Rocha
Affiliation:
Fluminense Federal University, Niterói, Rio de Janeiro, Brazil
Fernanda C. F. Brito
Affiliation:
Fluminense Federal University, Niterói, Rio de Janeiro, Brazil
Christianne B. V. Scaramello*
Affiliation:
Fluminense Federal University, Niterói, Rio de Janeiro, Brazil
*
Address for correspondence: Christianne Bretas Vieira Scaramello, PhD, Fluminense Federal University, Rua Professor Hernani Pires de Melo, 101, Sala 204A, São Domingos, Niterói CEP 24.210-130, RJ, Brazil. Email: chrisbretas@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Literature describes breast milk as the best food for the newborn, recommending exclusive breastfeeding for up to 6 months of age. However, it is not available for more than 40% of children worldwide. Pharmacological and non-pharmacological models of 3-day early weaning were developed in rodents to investigate later outcomes related solely to this nutritional insult. Thus, the present work aimed to describe biometric, nutritional, biochemical, and cardiovascular outcomes in adult male rats submitted to 3-day early weaning achieved by maternal deprivation. This experimental model comprises not only nutritional insult but also emotional stress, simulating mother abandoning. Male offspring were physically separated from their mothers at 21st (control) or 18th (early weaning) postnatal day, receiving water/food ad libitum. Analysis performed at postnatal days 30, 90, 150, and 365 encompassed body mass and food intake monitoring and serum biochemistry determination. Further assessments included hemodynamic, echocardiographic, and cardiorespiratory evaluation. Early-weaned males presented higher body weight when compared to control as well as dyslipidemia, higher blood pressure, diastolic dysfunction, and cardiac hypertrophy in adult life. Animals early deprived of their mothers have also presented a worse performance on the maximal effort ergometer test. This work shows that 3-day early maternal deprivation favors the development of cardiovascular disease in male rats.

Keywords

Weaninginfant nutrition disordersadaptationphysiologicalcardiovascular diseases
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 12 , Issue 3 , June 2021 , pp. 523 - 529
Check for updates
Copyright
© The Author(s), 2020. Published by Cambridge University Press in association with the International Society for Developmental Origins of Health and Disease

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

Penkler, M, Hanson, M, Biesma, R, Müller, R. DOHaD in science and society: emergent opportunities and novel responsibilities. J DOHaD. 2018; 10(3),268–273. doi: 10.1017/S2040174418000892 Google ScholarPubMed
Victora, CG, Smith, PG, Vaughan, JP et al. Evidence for protection by breastfeeding against infant deaths from infectious diseases in Brazil. Lancet (Br Edn). 1987; 330: 319–322.CrossRefGoogle Scholar
Kramer, MS, Kakuma, R. Optimal duration of exclusive breastfeeding. Cochrane Database Syst Rev. 2012; 8(CD003517), 1–95. doi: 10.1002/14651858.CD003517.pub2 Google Scholar
WHO. Infant and Young Child Feeding. IOP Publishing WHO. 2017; http://www.who.int/mediacentre/factsheets/fs342/en/. Accessed 17 September 2019Google Scholar
UNICEF and WHO. GLOBAL BREASTFEEDING INVESTMENT CASE. IOP Publishing WHO. http://who.int/nutrition/publications/infantfeeding/global-bf-collective-investmentcase/en/. Accessed 12 December 2019Google Scholar
Kelishadi, R, Farajian, S. The protective effects of breastfeeding on chronic non-communicable diseases in adulthood: a review of evidence. Adv Biomed Res. 2014; 3, 3. doi: 10.4103/2277-9175.124629 CrossRefGoogle ScholarPubMed
Souza, LL, de Moura, EG, Lisboa, PC. Does early weaning shape future endocrine and metabolic disorders? Lessons from animal models. J Dev Orig Health Dis. 2020; 1–11. doi: 10.1017/S2040174420000410 Google ScholarPubMed
Bonomo, IT, Lisboa, PC, Passos, MC, Passos-Moura, C, Reis, AM, Moura, EG. Prolactin inhibition in lactating rats changes leptin transfer through the milk. Horm Metab Res. 2005; 37(4), 220–225. doi: 10.1055/s-2005-861381 CrossRefGoogle ScholarPubMed
Bonomo, IT, Lisboa, PC, Pereira, AR, Passos, MC, de Moura, EG. Prolactin inhibition in dams during lactation programs for overweight and leptin resistance in adult offspring. J Endocrinol. 2007; 192(2), 339–344. doi: 10.1677/joe.1.06952 CrossRefGoogle ScholarPubMed
Moura, EG, Bonomo, IT, Neto, JF, et al. Maternal prolactin inhibition during lactation programs for metabolic syndrome in adult progeny. J Physiol. 2009; 587 (20), 4919–4929. doi: 10.1113/jphysiol.2009.176289 CrossRefGoogle ScholarPubMed
Bonomo, IT, Lisboa, PC, Passos, MC, Alves, SB, Reis, AM, de Moura, EG. Prolactin inhibition at the end of lactation programs for a central hypothyroidism in adult rat. J Endocrinol. 2008; 198, 331–337. doi: 10.1677/JOE-07-0505 CrossRefGoogle ScholarPubMed
Lima, NS, Moura, EG, Passos, MC, et al. Early weaning causes undernutrition for a short period and programmes some metabolic syndrome components and leptin resistance in adult rat offspring. Br J Nutr. 2011; 105(9), 1405–1413. doi: 10.1017/S0007114510005064 CrossRefGoogle Scholar
Quinn, R. Comparing rat’s to human’s age: how old is my rat in people years? Nutrition. 2005; 21(6), 775–777. doi: 10.1016/j.nut.2005.04.002 CrossRefGoogle ScholarPubMed
Koolhaas, JM. The laboratory rat. In The UFAW Handbook on the Care and Management of Laboratory Animals (ed. Poole, T), 2006; pp. 313–330. 7th ed. British: Blackwell Science.Google Scholar
Marques, EB, Barros, RBM, Rocha, NN, Scaramello, CBV. Aging and cardiac, biochemical, molecular and functional changes: experimental study. Int J Cardiovasc Sci. 2015; 1(1), 42–50. doi: 10.5935/2359-4802.20150007 Google Scholar
Lang, RM, Bierig, M, Devereux, RB, et al. Recommendations for chamber quantification: a report from the American Society of Echocardiography’s Guidelines and Standards Committee and the Chamber Quantification Writing Group, developed in conjunction with the European Association of Echocardiography, a branch of the European Society of Cardiology. J Am Soc Echocardiogr. 2005; 18(12), 1440–1463. doi: 10.1016/j.echo.2005.10.005 CrossRefGoogle ScholarPubMed
Sousa, JMA, Hermann, JLV, Guimarães, JB, Menezes, PPO, Carvalho, ACC. Avaliação das Pressões Sistólica, Diastólica e Pressão de Pulso como Fator de Risco para Doença Aterosclerótica Coronariana Grave em Mulheres com Angina Instável ou Infarto Agudo do Miocárdio sem Supradesnivelamento do Segmento ST. Arq Bras Cardiol. 2004; 82 (5), 426–429. doi: 10.1590/S0066-782X2004000500005 CrossRefGoogle Scholar
Fritz, M, Rinaldi, G. Influence of nitric oxide-mediated vasodilation on the blood pressure measured with the tail-cuff method in the rat. J Biomed Sci. 2007; 14(6), 757–765. doi: 10.1007/s11373-007-9191-1 CrossRefGoogle ScholarPubMed
Molnar, AM, Servais, S, Guichardant, M, et al. Mitochondrial H2O2 production is reduced with acute and chronic eccentric exercise in rat skeletal muscle. Antioxid Redox Signal. 2006; 8(3–4), 548–558. doi: 10.1089/ars.2006.8.548 CrossRefGoogle ScholarPubMed
Wonders, KY, Hydock, DS, Hayward, R. Time-course of changes in cardiac function during recovery after acute exercise. Appl Physiol Nutr Metab. 2007; 32(6), 1164–1169. doi: 10.1139/H07-127 CrossRefGoogle ScholarPubMed
Marques, EB, Motta, NAV, Kummerle, AE, et al. In vivo effect of LASSBio-785, a lipid-lowering and anti-inflammatory agent, on cardiac Ca2+-ATPases from hypercholesterolemic rats. Int J Cardiol. 2015; 201, 282–284. doi: 10.1016/j.ijcard.2015.08.091 CrossRefGoogle Scholar
Friedewald, WT, Levy, RI, Fredrickson, DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem. 1972; 18(6), 499–502.CrossRefGoogle ScholarPubMed
Castelli, WP, Garrison, RJ, Wilson, PW, Abbott, RD, Kalousdian, S, Kannel, WB. Incidence of coronary heart disease and lipoprotein cholesterol levels. The Framingham Study. JAMA. 1986; 256(20), 2835–2838. doi: 10.1001/jama.1986.03380200073024 CrossRefGoogle ScholarPubMed
Reaven, G. Metabolic syndrome: pathophysiology and implications for management of cardiovascular disease. Circulation. 2002; 106(3), 286–288. doi: 10.1161/01.CIR.0000019884.36724.D9 CrossRefGoogle ScholarPubMed
Toste, FP, de Moura, EG, Lisboa, PC, Fagundes, AT, de Oliveira, E, Passos, MC. Neonatal leptin treatment programmes leptin hypothalamic resistance and intermediary metabolic parameters in adult rats. Br J Nutr. 2006; 95(4), 830–837. doi: 10.1079/BJN20061726 CrossRefGoogle ScholarPubMed
McIntosh, J, Anisman, H, Merali, Z. Short- and long-periods of neonatal maternal separation differentially affect anxiety and feeding in adult rats: gender-dependent effects. Dev Brain Res. 1999; 113(1–2), 97–106. doi: 10.1016/S0165-3806(99)00005-X CrossRefGoogle Scholar
Wit, JM, Boersma, B. Catch up growth: definition, mechanisms, and models. J Pediatr Endocrinol Metab. 2002; 15 (Suppl. 5), 1229–1241.Google ScholarPubMed
Huxley, R, Mendis, S, Zheleznyakov, E, Reddy, S, Chan, J. Body mass index, waist circumference and waist:hip ratio as predictors of cardiovascular risk – a review of the literature. Eur J Clin Nutr. 2010; 64(1), 16–22. doi: 10.1038/ejcn.2009.68 CrossRefGoogle ScholarPubMed
Franco, JG, Lisboa, PC, Lima, NS, et al. Resveratrol attenuates oxidative stress and prevents steatosis and hypertension in obese rats programmed by early weaning. J Nutr Biochem. 2013; 24(6), 960–966. doi: 10.1016/j.jnutbio.2012.06.019 CrossRefGoogle ScholarPubMed
Murad, MH, Hazem, A, Coto-Yglesias, F, et al. The association of hypertriglyceridemia with cardiovascular events and pancreatitis: systematic review and meta-analysis. BMC Endocr Disord. 2012; 12, 2. doi: 10.1186/1472-6823-12-2 CrossRefGoogle ScholarPubMed
Borén, J, Matikainen, N, Adiels, M, Taskinen, MR. Postprandial hypertriglyceridemia as a coronary risk factor. Clin Chim Acta. 2014; 431, 131–142. doi: 10.1016/j.cca.2014.01.015 CrossRefGoogle ScholarPubMed
Havel, RJ, Hamilton, RL. Hepatocytic lipoprotein receptors and intracellular lipoprotein catabolism. Hepatology. 1988; 8(6), 1689–1704. doi: 10.1002/hep.1840080637 CrossRefGoogle ScholarPubMed
Brown, MS, Goldstein, JL. Biomedicine. Lowering LDL – not only how low, but how long? Science. 2006; 311(5768), 1721–1723. doi: 10.1126/science.1125884 CrossRefGoogle ScholarPubMed
Varbo, A, Benn, M, Smith, GD, Timpson, NJ, Tybjaerg-Hansen, A, Nordestgaard, BG. Remnant cholesterol, low-density lipoprotein cholesterol, and blood pressure as mediators from obesity to ischemic heart disease. Circ Res. 2015; 116 (4), 665–673. doi: 10.1161/CIRCRESAHA.116.304846 CrossRefGoogle ScholarPubMed
Klop, B, Elte, JW, Cabezas, MC. Dyslipidemia in obesity: mechanisms and potential targets. Nutrients. 2013; 5(4), 1218–1240. doi: 10.3390/nu5041218 CrossRefGoogle ScholarPubMed
Rizzo, M, Otvos, J, Nikolic, D, Montalto, G, Toth, PP, Banach, M. Subfractions and subpopulations of HDL: an update. Curr Med Chem. 2014; 21(25), 2881–2891. doi: 10.2174/0929867321666140414103455 CrossRefGoogle ScholarPubMed
Gogonea, V. Structural insights into high density lipoprotein: old models and new facts. Front Pharmacol. 2016; 6, 318. doi: 10.3389/fphar.2015.00318 CrossRefGoogle ScholarPubMed
Dobiásová, M. Atherogenic index of plasma [log(triglycerides/HDL-cholesterol)]: theoretical and practical implications. Clin Chem. 2004; 50(7), 1113–1115. doi: 10.1373/clinchem.2004.033175 CrossRefGoogle ScholarPubMed
Sayın, S, Kutlu, R, Koçak, A. The relationship between atherogenic index of plasma and major risk factors of cardiovascular disease in obese and nonobese individuals. Eur Res J. 2019; 5(4), 678–685. doi: 10.18621/eurj.414561 Google Scholar
Fonseca-Alaniz, MH, Takada, J, Alonso-Vale, MIC, Lima, FB. O tecido adiposo como centro regulador do metabolismo. Arq Bras Endocrinol Metab. 2006; 50(2), 216–229. doi: 10.1590/S0004-27302006000200008 CrossRefGoogle Scholar
Pietrobon, CB, Bertasso, IM, Silva, BS, et al. Body adiposity and endocrine profile of female Wistar rats of distinct ages that were early weaned. Horm Metab Res. 2020; 52(1), 58–66. doi: 10.1055/a-0966-8784 Google ScholarPubMed
Lima, NS, Moura, EG, Franco, JG, et al. Developmental plasticity of endocrine disorders in obesity model primed by early weaning in dams. Horm Metab Res. 2013; 45(1), 22–30. doi: 10.1055/s-0032-1323703 Google ScholarPubMed
Nagueh, SF, Appleton, CP, Gillebert, TC, et al. Recommendations for the evaluation of left ventricular diastolic function by echocardiography. Eur J Echocardiogr 2009; 10(2), 165–193. doi: 10.1016/j.echo.2008.11.023 CrossRefGoogle ScholarPubMed
Hoss, AJ, Petterson, CHP, Scherer, L. Miocardiopatia hipertrófica. Papel da ecocardiografia doppler no diagnóstico e na orientação terapêutica. Arq Bras Cardiol 1998; 70(4), 301–306. doi: 10.1590/S0066-782X1998000400012 CrossRefGoogle Scholar
Boon, JA. Manual of Veterinary Echocardiography, 1998; pp. 478. Williams and Wilkins, Baltimore.Google Scholar
Rodrigues, B, Figueroa, DM, Mostarda, CT, Heeren, MV, Irigoyen, MC, De Angelis, K. Maximal exercise test is a useful method for physical capacity and oxygen consumption determination in streptozotocin-diabetic rats. Cardiovasc Diabetol. 2007; 6 (38). doi: 10.1186/1475-2840-6-38 CrossRefGoogle ScholarPubMed
Cohen-Solal, A, Beauvais, F, Tabet, JY. Physiology of the abnormal response of heart failure patients to exercise. Curr Cardiol Rep. 2004; 6(3), 176–181. doi: 10.1007/s11886-004-0020-0 CrossRefGoogle ScholarPubMed
Otto, MEB, Pereira, MM, Beck, ALS, Milani, M. Correlação da função diastólica com a capacidade máxima de exercício ao teste ergométrico. Arq. Bras. Cardiol. 2011; 96(2), 107–113. doi: 10.1590/S0066-782X2011005000004 CrossRefGoogle Scholar
Little, WC, Kitzman, DW, Cheng, CP. Diastolic dysfunction as a cause of exercise intolerance. Heart Fail Rev. 2000; 5(4), 301–306. doi: 10.1023/a:1026503028065 CrossRefGoogle ScholarPubMed
Tractenberg, SG, Levandowski, M, de Azeredo, LA et al. An overview of maternal separation effects on behavioural outcomes in mice: evidence from a four-stage methodological systematic review. Neurosci Biobehav Rev. 2016; 68, 489–503. doi: 10.1016/j.neubiorev.2016.06.021 CrossRefGoogle ScholarPubMed
Kikusui, T, Ichikawa, S, Mori, Y. Maternal deprivation by early weaning increases corticosterone and decreases hippocampal BDNF and neurogenesis in mice. Psychoneuroendocrinology 2009; 34(5), 762–772.CrossRefGoogle ScholarPubMed
Huang, BS, White, RA, Ahmad, M, Leenen, F. Role of brain corticosterone and aldosterone in central angiotensin II-induced hypertension. Hypertension. 2013; 62, 564–571. http://dx.doi.org/10.1161/HYPERTENSIONAHA.113.01557 CrossRefGoogle ScholarPubMed
Dickstein, K, Cohen-Solal, A, Filippatos, G, et al. ESC Committee for Practice Guidelines (CPG). ESC guidelines for the diagnosis and treatment of acute and chronic heart failure 2008: the Task Force for the diagnosis and treatment of acute and chronic heart failure 2008 of the European Society of Cardiology. Developed in collaboration with the Heart Failure Association of the ESC (HFA) and endorsed by the European Society of Intensive Care Medicine (ESICM). Eur J Heart Fail. 2008; 10(10), 933–989. doi: 10.1016/j.ejheart.2008.08.005 CrossRefGoogle Scholar
Montera, MW, Almeida, RA, Tinoco, EM et al. Sociedade Brasileira de Cardiologia. II Diretriz Brasileira de Insuficiência Cardíaca Aguda. Arq Bras Cardiol. 2009; 93(3 Suppl. 3), 1–65. doi: 10.1590/S0066-782X2009001900001 Google Scholar