Hostname: page-component-8448b6f56d-c47g7 Total loading time: 0 Render date: 2024-04-20T04:00:01.263Z Has data issue: false hasContentIssue false
  • English
  • Français

Maternal high-fat diet consumption during pregnancy and lactation predisposes offspring to renal and metabolic injury later in life: comparative study of diets with different lipid contents

Published online by Cambridge University Press:  28 April 2022

Fernanda Busnardo de Oliveira ,
Jéssica Fortunato Silva ,
Helena Severino do Prado ,
Marcos Luiz Ferreira-Neto  and
Ana Paula Coelho Balbi Open the ORCID record for Ana Paula Coelho Balbi [Opens in a new window]
Fernanda Busnardo de Oliveira
Affiliation:
Applied Structural and Cellular Biology, Federal University of Uberlândia, Uberlândia, Brazil
Jéssica Fortunato Silva
Affiliation:
Applied Structural and Cellular Biology, Federal University of Uberlândia, Uberlândia, Brazil
Helena Severino do Prado
Affiliation:
Federal University of Uberlândia, Uberlândia, Brazil
Marcos Luiz Ferreira-Neto
Affiliation:
Department of Physiology, Federal University of Uberlândia, Uberlândia, Brazil
Ana Paula Coelho Balbi*
Affiliation:
Department of Physiology, Federal University of Uberlândia, Uberlândia, Brazil
*
Address for correspondence: Ana Paula C. Balbi, Avenida Pará, 1720, Campus Umuarama, Bloco 2A, CEP: 38400-902, Uberlândia, Minas Gerais, Brazil. Emails: paulabalb@ufu.br; paulabalb@yahoo.com.br
Get access Rights & Permissions [Opens in a new window]

Abstract

Accumulating evidence suggests that maternal overnutrition can result in a higher development risk of obesity and renal disease in the offspring’s adulthood. The present study tested different lipid levels in the maternal diet during pregnancy and lactation and its repercussions on the offspring of Wistar rats. Offspring of 1, 7, 30 and 90-d-old were divided into the following groups: Control (CNT) – offspring of dams that consumed a standard chow diet (3.5% of lipids); Experimental 1 (EXP1) – offspring of dams exposed to a high-fat diet (HFD) (28% of lipids); and Experimental 2 (EXP2) – offspring of dams exposed to a HFD (40% of lipids). Regarding maternal data, there was a decrease in the amount of diet ingested by EXP2. Daily caloric intake was higher in EXP1, while protein and carbohydrate intakes were lower in EXP2. While lipid intake was higher in the experimental groups, EXP1 consumed more lipids than EXP2, despite the body weight gain being higher in EXP2. Adult offspring from EXP1 presented higher blood glucose. Regarding morphometric analysis, in both experimental groups, there was an increase in the glomerular tuft and renal corpuscle areas, but an increase in the capsular space area only in EXP1. There was a decrease in the glomerular filtration rate (GFR) in EXP1, in contrast to an increase in GFR of EXP2, along with an increase in urinary protein excretion. In conclusion, the maternal HFDs caused significant kidney damage in offspring, but had different repercussions on the type and magnitude of recorded change.

Keywords

High-fat dietrenal functionoffspringWistar rats
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 14 , Issue 1 , February 2023 , pp. 33 - 41
Check for updates
Copyright
© The Author(s), 2022. Published by Cambridge University Press in association with 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

Langle-Evans, SC. Nutrition in early life and the programming of adult disease: a review. J Hum Nutr Diet. 2015; 28(Suppl 1), 1–14.CrossRefGoogle Scholar
Parrino, C, Vinciguerra, F, La Spina, N, et al. Influence of early life and parental factors on childhood overweight and obesity. J Endocrinol Invest. 2016; 39(11), 1315–1321.CrossRefGoogle ScholarPubMed
Who (World Health Organization) Obesity and Overweight. Available https://www.who.int/news-room/fact-sheets/detail/obesity-and-overweight (2022, accessed April 2022).Google Scholar
Armitage, JA, Taylor, PD, Poston, L. Experimental models of fetal programming: consequences of exposure to an energy rich diet during development. J Physiol. 2005; 565(1), 3–8.CrossRefGoogle Scholar
Glastras, S, The, NL, Wong, MG, Saad, S. Maternal obesity and offspring risk of chronic kidney disease. Nephrology. 2018; 23, 84–87.Google Scholar
Buettner, R, Schölmerich, J, Bollheimer, LC. High-fat diets: modeling the metabolic disorders of human obesity in rodents. Obesity. 2007; 15(4), 15–808.CrossRefGoogle ScholarPubMed
Peckham, SC, Entenmann, C, Carroll, HW. The influence of a hypercaloric diet on gross body and adipose tissue composition in the rat. J Nutr. 1962; 77(2), 187–197.CrossRefGoogle Scholar
Jump, DB. Dietary polyunsaturated fatty acids and regulation of gene transcription. Curr Opin Lipidol. 2002; 13(2), 155–164.CrossRefGoogle ScholarPubMed
Ikemoto, S, Takahashi, M, Tsunoda, N, Maruyama, K, Itakura, H, Ezaki, O. High-fat diet-induced hyperglycemia and obesity in mice: differential effects of dietary oils. Metabolis. 1996; 45(12), 1539–1546.CrossRefGoogle ScholarPubMed
Hariri, M, Thibault, L. High-fat diet-induced obesity in animal models. Nutr Res Rev. 2010; 23(2), 270–299.CrossRefGoogle ScholarPubMed
Schemmel, R, Mickelsen, O, Tolgay, Z. Dietary obesity in rats: influence of diet, weight, age, and sex on body composition. Am J Physiol. 1969; 216(2), 373–379.CrossRefGoogle ScholarPubMed
Yaqoob, P, Sherrington, EJ, Jeffery, NM, et al. Comparison of the effects of a range of dietary lipids upon serum and tissue lipid composition in the rat. Int J Biochem Cell Biol. 1995; 27(3), 297–310.CrossRefGoogle ScholarPubMed
Smith, BK, West, DB, York, DA. Carbohydrate versus fat intake: differing patterns of macronutrient selection in two inbred mouse strains. Am J Physiology. 1997; 272 (1 Pt 2), R357–R362.Google ScholarPubMed
Chalkley, SM, Hettiarachchi, M, Chisholm, DJ, Kraegen, EW. Long-term high-fat feeding leads to severe insulin resistance but not diabetes in Wistar rats. Am J Physiol Endocrinol Metab. 2002; 282(6), 1231–1238.CrossRefGoogle Scholar
Kereliuk, SM, Brawerman, GM, Dolinsky, VW. Maternal macronutrient consumption and the developmental origins of metabolic disease in the offspring. Int J Mol Sci. 2017; 18(7), 18.CrossRefGoogle ScholarPubMed
Hsu, C-N, Hou, C-Y, Lee, C-T, Chan, JYH, Tain, Y-L. The interplay between maternal and post-weaning high-fat diet and gut microbiota in the developmental programming of hypertension. Nutrients. 2019; 11(9), 1982.CrossRefGoogle ScholarPubMed
Lee, KK, Edwin, AR, Lee, AJ, et al. Maternal obesity during pregnancy associates with premature mortality and major cardiovascular events in later life. Hypertension. 2015; 66(5), 938–944.CrossRefGoogle ScholarPubMed
Glastras, SJ, Chen, H, Teh, R, et al. Mouse models of diabetes, obesity and related kidney disease. Plos One. 2016; 11(8), 1–15.CrossRefGoogle ScholarPubMed
Glastras, SJ, Chen, H, Teh, R, et al. The renal consequences of maternal obesity in offspring are overwhelmed by postnatal high fat diet. Plos One. 2017; 12(2), 1–17.CrossRefGoogle ScholarPubMed
Hall, JE. The kidney, hypertension, and obesity. Hypertension. 2003; 41(3), 625–633.CrossRefGoogle ScholarPubMed
Paixão, AD, Alexander, BT. How the kidney is impacted by the perinatal maternal environment to develop hypertension. Biol Reprod. 2013; 89, 1–10.CrossRefGoogle ScholarPubMed
Hall, ME, Carmo, JM, Silva, AA, Juncos, LA, Wang, Z, Hall, JE. Obesity, hypertension, and chronic disease. Int J Nephrol Renovasc Dis. 2014; 7, 75–88.CrossRefGoogle Scholar
Duarte, ACGdO, Fonseca, DF, Manzoni, MSJ, et al. Hyperlipidic diet and insulin secretory capacity in rats. Rev Nutr. 2006; 19(3), 341–348.CrossRefGoogle Scholar
Correia-Santos, AM, Suzuki, A, Anjos, JS, et al. Induction of type 2 diabetes by low dose of streptozotocin and high-fat diet in wistar rats. Medicina (Ribeirão Preto). 2012; 45(4), 436–444.CrossRefGoogle Scholar
Roza, NAV, Possignolo, LF, Palanch, AC. Effect of long-term high-fat diet intake on peripheral insulin sensibility, blood pressure, and renal function in female rats. Food Nutr Res. 2016; 60(1), 60.CrossRefGoogle ScholarPubMed
Tanko, Y, Eze, ED, Daja, HS, Jimoh, A, Mohammed, KA, Musa, KY. Ameliorative effects of vitamin C and E on serum lipid profiles and liver enzymes on fructose-induced hyperglycemia in wistar rats. J Appl Pharm Sci. 2013; 3, 80–84.Google Scholar
Hillier, TA, Pedula, KL, Schimidt, MM, Mullen, JA, Charles, MA, Pettit, DJ. Childhood obesity and metabolic imprinting – the ongoing effects of maternal hyperglycemia. Diabetes Care. 2007; 30(9), 2287–2292.CrossRefGoogle ScholarPubMed
Ainge, H, Thompson, C, Ozanne, SE, Rooney, KB. A systematic review on animal models of maternal high fat feeding and offspring glycaemic control. Int J Obes. 2011; 35(3), 325–335.CrossRefGoogle ScholarPubMed
Ribaroff, GA, Wastnedge, E, Drake, AJ, Sharpe, RM, Chambers, TJG. Animal models of maternal high fat diet exposure and effects on metabolism in offspring: a meta-regression analysis. Obes Rev. 2017; 18(6), 673–686.CrossRefGoogle ScholarPubMed
Burgueño, AL, Cabrerizo, R, Gonzales Mansilla, N, Sookoian, S, Pirola, CJ. Maternal high-fat intake during pregnancy programs metabolic-syndrome-related phenotypes through liver mitochondrial DNA copy number and transcriptional activity of liver PPARGC1A. J Nutr Biochem. 2013; 24(1), 6–13.CrossRefGoogle ScholarPubMed
Khan, YI, Dekou, V, Douglas, G, et al. A high-fat diet during rat pregnancy or suckling induces cardiovascular dysfunction in adult offspring. Am J Physiol Regul Integr Comp Physiol. 2005; 288(1), 127–133.CrossRefGoogle ScholarPubMed
Hall, KD, Guo, J. Obesity energetics: body weight regulation and the effects of diet composition. Gastroenterology. 2017; 152(7), 1718–1727.CrossRefGoogle ScholarPubMed
Hall, KD, Heymsfield, SB, Kemnitz, JW, Klein, S, Schoeller, DA, Speakman, JR. Energy balance and its components: implications for body weight regulation. Am J Clin Nutr. 2012; 95(4), 989–989.CrossRefGoogle ScholarPubMed
Rolls, BJ, Bell, EA, Castellanos, VH, Chow, M, Pelkman, CL, Thorwart, ML. Energy density but not fat content of foods affected energy intake in lean and obese women. Am J Clin Nutr. 1999; 69(5), 863–871.CrossRefGoogle Scholar
Williams, L, Seki, Y, Vuguin, PM, Charron, MJ. Animal models of in utero exposure to a high fat diet: a review. Biochim Biophys Acta. 2014; 1842(3), 507–519.CrossRefGoogle ScholarPubMed
Gibson, AA, Seimon, RV, Lee, CMY, et al. Do ketogenic diets really suppress appetite? A systematic review and meta-analysis. Obes Rev. 2015; 16(1), 64–76.CrossRefGoogle ScholarPubMed
Paoli, A, Bosco, G, Camporesi, EM, Mangar, D. Ketosis, ketogenic diet and food intake control: a complex relationship. Front Psychol. 2015; 6, 6.CrossRefGoogle ScholarPubMed
Dirlewanger, M, Di Vetta, V, Guenat, E, et al. Effects of short-term carbohydrate or fat overfeeding on energy expenditure and plasma leptin concentrations in healthy female subjects. Int J Obes Relat Metab Disord. 2000; 24(11), 1413–1418.CrossRefGoogle ScholarPubMed
Horton, T J, Drougas, H, Brachey, A, Reed, G W, Peters, J C, Hill, J O. Fat and carbohydrate overfeeding in humans: different effects on energy storage. Am J Clin Nutr. 1995; 62(1), 19–29.CrossRefGoogle ScholarPubMed
Aizawa-Abe, M, Ogawa, Y, Mazuzaki, H, et al. Pathophysiological role of leptin in obesity related hypertension. J Clin Invest. 2000; 105(9), 1243–1252.CrossRefGoogle ScholarPubMed
Lin, S, Thomas, TC, Storlien, LH, Huang, XF. Development of high fat diet-induced obesity and leptin resistance in C57Bl/6J mice. Int J Obes Relat Metab Disord. 2000; 24(5), 639–646.CrossRefGoogle ScholarPubMed
Fam, BC, Morris, MJ, Hansen, MJ, et al. Modulation of central leptin sensitivity and energy balance in a rat model of diet-induced obesity. Diabetes Obes Metab. 2007; 6(6), 840–852.CrossRefGoogle Scholar
Schellong, K, Melchior, K, Ziska, T, Rancourt, RC, Henrich, W, Plagemann, A. Maternal but not paternal high-fat diet (HFD) exposure at conception predisposes for ‘diabesity’ in offspring generations. Int J Environ. 2019; 17(12), 4229, 1–15.Google Scholar
Lee, MO. Determination of the surface area of the white rat with its application to the expression of metabolic results. Am J Physiol. 1929; 89(1), 24–33.CrossRefGoogle Scholar
Levin, BE, Dunn-Meynell, AA, Ricci, MR, Cummings, DE. Abnormalities of leptin and ghrelin regulation in obesityprone juvenile rats. Am J Physiol Endocrinol Metab. 2003; 285(5), 949–957.CrossRefGoogle ScholarPubMed
Levin, BE, Dunn-Meynell, AA. Reduced central leptin sensitivity in rats with diet-induced obesity. Am J Physiol Regul Integr Comp Physiol. 2002; 283(4), 941–948.CrossRefGoogle ScholarPubMed
Sapienza, C, Issa, J-P. Diet, nutrition, and cancer epigenetics. Annu Rev Nutr. 2016; 36(1), 665–681.CrossRefGoogle ScholarPubMed
Chang, S, Graham, B, Yakubu, F. Metabolic differences between obesity-prone and obesity resistant rats. Am J Physiol. 1990; 259(6), 1103–1110.Google ScholarPubMed
Hassanain, M, Levin, BE. Dysregulation of hypothalamic serotonin turnover in diet-induced obese rats. Brain Res. 2002; 929(2), 175–180.CrossRefGoogle ScholarPubMed
Jackman, MR, Kramer, RE, MacLean, PS. Trafficking of dietary fat in obesity-prone and obesity resistant rats. Am J Physiol-Endocrinol Metab. 2006; 291(5), 1083–1091.CrossRefGoogle ScholarPubMed
Srinivasan, M, Katewa, SD, Palaniyappan, A, Pandya, JD, Patel, MS. Maternal high-fat diet consumption results in fetal malprogramming predisposing to the onset of metabolic syndrome like phenotype in adulthood. Am J Physiol Endocrinol Metab. 2006; 291(4), 792–799.CrossRefGoogle Scholar
Jones, HN, Woollett, LA, Barbour, N. High-fat diet before and during pregnancy causes marked up-regulation of placental nutrient transport and fetal overgrowth in C57/BL6 mice. FASEB J. 2009; 23(1), 271–278.CrossRefGoogle ScholarPubMed
Nivoit, P, Jansen, E, Remacle, C. Established diet-induced obesity in female rats leads to offspring hyperphagia, adiposity and insulin resistance. Diabetologia. 2009; 52(6), 1133–1142.CrossRefGoogle ScholarPubMed
Hausman, DB, McCloskey, HM, Martin, RJ. Maternal dietary fat type influences the growth and fatty acid composition of newborn and weanling rats. J Nutr. 1991; 121(12), 1917–1923.CrossRefGoogle ScholarPubMed
Taylor, PD, Khan, IY, Lakasing, L, et al. Uterine artery function in pregnant rats fed a diet supplemented with animal lard. Exp Physiol. 2003; 88(3), 389–398.CrossRefGoogle ScholarPubMed
Howie, GJ, Sloboda, DM, Kamal, T, Vickers, MH. Maternal nutritional history predicts obesity in adult offspring independent of postnatal diet. J Physiol. 2009; 587. 4(4), 905–915.CrossRefGoogle Scholar
Gardner, DS, Rhodes, P. Developmental origins of obesity: programming of food intake or physical activity? Adv Exp Med Biol. 2009; 646, 83–93.CrossRefGoogle ScholarPubMed
Rassmusen, KM. Effects of under- and overnutrition on lactation in laboratory rats. J Nutr. 1998; 128(2), 390–393.CrossRefGoogle Scholar
Shankar, K, Harrell, A, Liu, X, Gilchrist, JM, Ronis, MJJ, Badger, TM. Maternal obesity at conception programs obesity in the offspring. Am J Physiol Regul Integr Comp Physiol. 2008; 294(2), 528–538.CrossRefGoogle ScholarPubMed
Khan, IY, Taylor, PD, Dekou, V, et al. Gender-linked hypertension in offspring of lard-fed pregnant rats. Hypertension. 2003; 41(1), 168–175.CrossRefGoogle ScholarPubMed
Gorski, JN, Dunn-Meynell, AA, Hartman, TG, Levin, BE. Postnatal environment overrides genetic and prenatal factors influencing offspring obesity and insulin resistance. Am J Physiol Regul Integr Comp Physiol. 2006; 291(3), 768–778.CrossRefGoogle ScholarPubMed
Chaves, WF, Pinheiro, IL, Silva, LO, et al. Neonatal administration of kaempferol does not alter satiety but increases somatic growth and reduces adiposity in offspring of high-fat diet dams. Life Sci. 2020; 259(1), 118–224.CrossRefGoogle Scholar
Hokke, S, Puelles, VG, Armitage, JA, Fong, K, Bertram, JF, Cullen-McEwen, LA. Maternal fat feeding augments offspring nephron endowment in mice. PLoS One. 2016; 11(8), e0161578, 1–19.CrossRefGoogle ScholarPubMed
Boney, CM, Verma, A, Tucker, R, Vohr, BR. Metabolic syndrome in childhood: association with birth weight, maternal obesity, and gestational diabetes mellitus. Pediatrics. 2005; 115(3), 290–296.CrossRefGoogle ScholarPubMed
Oscai, LB. Dietary-induced severe obesity – a rat model. Am J Physiol. 1982; 242(3), 212–215.Google ScholarPubMed
Ainslie, DA, Proietto, J, Fam, BC, Thorburn, AW. Short-term,high-fat diets lower circulating leptin concentrations in rats. Am J Clin Nutr. 2000; 71(2), 438–442.CrossRefGoogle ScholarPubMed
Ghibaudi, L, Cook, J, Farley, C, van Heek, M, Hwa, JJ. Fat intake affects adiposity, comorbidity factors, and energy metabolism of Sprague-Dawley rats. Obes Res. 2002; 10(9), 956–963.CrossRefGoogle ScholarPubMed
Bouanane, S, Merzouk, H, Benkafalt, NB. Hepatic and very low-density lipoprotein fatty acids in obese offspring of overfed dams. Metab: Clin Exp. 2010; 59(12), 1701–1709.CrossRefGoogle ScholarPubMed
Reisin, E, Messerli, FG, Ventura, HO, Frohlich, ED. Renal hemodynamic studies in obesity hypertension. J Hypertens. 1987; 5, 397–400.CrossRefGoogle ScholarPubMed
Chagnac, A, Weinstein, T, Korzets, A. Glomerular hemodynamics in severe obesity. J Hypertens. 2000; 278(5), 817–822.Google ScholarPubMed
Whaley-Cornell, A, Sowers, JR. Obesity and kidney disease: from population to basic science and the search for new therapeutic targets. Kidney Int. 2016; 92(2), 313–333.CrossRefGoogle Scholar
Jackson, CM, Alexander, BT, Roach, L, et al. Exposure to maternal overnutrition and a high-fat diet during early postnatal development increases susceptibility to renal and metabolic injury later in life. Am J Physiol Renal Physiol. 2011; 302(6), 774–783.CrossRefGoogle Scholar
Wood-Bradley, R, Barrand, S, Giot, A, Armitage, J. Understanding the role of maternal diet on kidney development, an opportunity to improve cardiovascular and renal health for future generations. Nutrients. 2015; 7(3), 1881–1905.CrossRefGoogle ScholarPubMed
Black, MJ, Briscoe, TA, Constantinou, M, Kett, MM, Bertram, JF. Is there an association between level of adult blood pressure and nephron number or renal filtration surface area? Kidney Int. 2004; 65(2), 582–588.CrossRefGoogle ScholarPubMed
Langle-Evans, SC. Critical differences between two low protein diet protocols in the programming of hypertension in the rat. Int. J. Food Sci. Nutr. 2000; 51(1), 11–17.CrossRefGoogle Scholar
Langley-Evans, SC, Welham, SJ, Jackson, AA. Fetal exposure to a maternal low protein diet impairs nephrogenesis and promotes hypertension in the rat. Life Sci. 1999; 11(11), 965–974.CrossRefGoogle Scholar
Merlet-Bénichou, C, Gilbert, T, Muffat-Joly, M, Lelièvre-Pègorier, M, Leroy, B. Intrauterine growth retardation leads to a permanent nephron deficit in the rat. Pediatr Nephrol. 1994; 2(2), 175–180.CrossRefGoogle Scholar
Jahan-Mihan, A, Rodriguez, J, Christie, C, Sadeghi, M, Zerbe, T. The role of maternal dietary proteins in development of metabolic syndrome in offspring. Nutrients. 2015; 7(11), 9185–9217.CrossRefGoogle Scholar
Fernandez-Twinn, DS, Wayman, A, Ekizoglou, S, Martin, MS, Hales, CN, Ozanne, SE. Maternal protein restriction leads to hyperinsulinemia and reduced insulin-signaling protein expression in 21-mo-old female rat offspring. Am J Physiol Regul Integr Comp Physiol. 2005; 288(2), 368–373.CrossRefGoogle ScholarPubMed
Martin-Gronert, MS, Fernandez-Twinn, DS, Bushell, M, Siddle, K, Ozanne, SE. Cell-autonomous programming of rat adipose tissue insulin signalling proteins by maternal nutrition. Diabetologia. 2016; 59(6), 1266–1275.CrossRefGoogle ScholarPubMed
Nwagwu, MO, Cook, A, Langley-Evans, SC. Evidence of progressive deterioration of renal function in rats exposed to maternal low-protein diet in utero. Br J Nutr. 2000; 83(1), 79–85.CrossRefGoogle ScholarPubMed
Tobar, A, Ori, Y, Benchetrit, S, et al. Proximal tubular hypertrophy and enlarged glomerular and proximal tubular urinary space in obese subjects with proteinuria. Plos One. 2013; 8(9), e75547, 1–9.CrossRefGoogle Scholar
Rea, DJ, Heimbach, JK, Grande, JP, et al. Glomerular volume and renal histology in obese and non-obese living kidney donors. Kidney Int. 2006; 70(9), 1636–1641.CrossRefGoogle ScholarPubMed
Goumenos, D, Kawar, B, Nahas, ME, et al. Early histological changes in the kidney of people with morbid obesity. Nephrol Dial Transplant. 2009; 24(12), 3732–3738.CrossRefGoogle ScholarPubMed
Khan, IY, Dekou, V, Douglas, G, et al. A high-fat diet during rat pregnancy or suckling induces cardiovascular dysfunction in adult offspring. Am J Physiol Regul Integr Comp Physiol. 2005; 288(1), 127–133.CrossRefGoogle ScholarPubMed
Chen, F, Cao, K, Zhang, H, Yu, H, Liu, Y, Xue, Q. Maternal high-fat diet increases vascular contractility in adult offspring in a sex-dependent manner. Hypertens Res. 2020; 44(1), 36–46.CrossRefGoogle Scholar
Loche, E, Blackmore, HL, Carpenter, AA, et al. Maternal diet-induced obesity programmes cardiac dysfunction in male mice independently of post-weaning diet. Cardiovasc Res. 2018; 114(10), 1372–1384.CrossRefGoogle ScholarPubMed
Menendez-Castro, C, Nitz, D, Cordasic, N, et al. Neonatal nephron loss during active nephrogenesis – detrimental impact with long-term renal consequences. Sci Rep. 2018; 8, 4542, 1–11.Google Scholar