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A new model for fetal programming: maternal Ramadan-type fasting programs nephrogenesis

  • M. Mohany (a1), N. Ashton (a2), A. H. Harrath (a1), J. R. Nyengaard (a3), S. Y. Alomar (a1) and S. Alwasel (a1)...
Abstract

The effect of maternal Ramadan-type fasting (RTF) on the outcome of pregnancy, kidney development and nephron number in male rat offspring was investigated in current study. Pregnant rats were given food and water ad libitum during pregnancy (control) or restricted for 16 h per day (RTF). Kidney structure was examined during fetal life, at birth, and in early and late adulthood. Maternal body weight, food intake, relative food intake and plasma glucose levels were significantly lower (P<0.001) in the RTF group. Litter and pup weights also were significantly lower (P<0.05) in the RTF group at birth, with no difference in the litter size. The RTF group had a longer gestation, delayed nephrogenesis with less well-differentiated glomeruli, more connective tissue, fewer medullary rays, an increase in the nephrogenic zone/cortical zone ratio, and significant increase (P<0.001) in kidney apoptosis at birth. On the other hand, maternal fasting reduced nephron number (by ~31%) with unchanged kidney and total glomerular volumes. Mean glomerular volume was significantly higher in RTF offspring. Assessment of renal structure revealed mild glomerulosclerosis with enlarged lobulated glomeruli in the renal cortex and high interstitial fibrosis in the medulla of RTF kidneys. Taken together, gestational fasting delays nephrogenesis and reduces nephron number in the kidneys of the offspring, that could be partially owing to increased apoptosis.

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Corresponding author
Address for correspondence: S. Alwasel, Zoology Department, College of Science, King Saud University, Riyadh 11451, Kingdom of Saudi Arabia. E-mail: salwasel@ksu.edu.sa
References
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1. Alwasel, SH, Abotalib, Z, Aljarallah, JS, et al. Sex differences in birth size and intergenerational effects of intrauterine exposure to Ramadan in Saudi Arabia. Am J Hum Biol. 2011; 23, 651654.
2. Van Abeelen, AF, Veenendaal, MV, Painter, RC, et al. The fetal origins of hypertension: a systematic review and meta-analysis of the evidence from animal experiments of maternal undernutrition. J Hypertens. 2012; 30, 22552267.
3. Sánchez-Muniz, FJ, Gesteiro, E, Espárrago Rodilla, M, Rodríguez Bernal, B, Bastida, S. Maternal nutrition during pregnancy conditions the fetal pancreas development, hormonal status and diabetes mellitus and metabolic syndrome biomarkers at birth. Nutr Hosp. 2013; 28, 250274.
4. Abiri, B, Kelishadi, R, Sadeghi, H, Azizi-Soleiman, F. Effects of maternal diet during pregnancy on the risk of childhood acute lymphoblastic leukemia: a systematic review. Nutr Cancer. 2016; 68, 10651072.
5. Barker, DJ, Osmond, C, Winter, PD, Margetts, B, Simmonds, SJ. Weight in infancy and death from ischaemic heart disease. Lancet. 1989; 334, 577580.
6. Bagby, SP. Maternal nutrition, low nephron number, and hypertension in later life: pathways of nutritional programming. J Nutr. 2007; 137, 10661072.
7. Tain, YL, Hsu, CN, Chan, JY, Huang, LT. Renal transcriptome analysis of programmed hypertension induced by maternal nutritional insults. Int J Mol Sci. 2015; 16, 1782617837.
8. Koleganova, N, Piecha, G, Ritz, E. Prenatal causes of kidney disease. Blood Purif. 2009; 27, 4852.
9. Brennan, KA, Kaufman, S, Reynolds, SW, et al. Differential effects of maternal nutrient restriction through pregnancy on kidney development and later blood pressure control in the resulting offspring. Am J Physiol Regul Integr Comp Physiol. 2008; 295, R197R205.
10. Hoppe, CC, Evans, RG, Bertram, JF, Moritz, KM. Effects of dietary protein restriction on nephron number in the mouse. Am J Physiol Regul Integr Comp Physiol. 2007; 292, R1768R1774.
11. Woods, LL, Ingelfinger, JR, Nyengaard, JR, Rasch, R. Maternal protein restriction suppresses the newborn renin-angiotensin system and programs adult hypertension in rats. Pediatr Res. 2001; 49, 460467.
12. Luzardo, R, Silva, PA, Einicker-Lamas, M, et al. Metabolic programming during lactation stimulates renal Na+ transport in the adult offspring due to an early impact on local angiotensin II pathways. PLoS One. 2011; 6, e21232.
13. Schreuder, MF, Langemeijer, ME, Bökenkamp, A, Delemarre-Van de Waal, HA, Van Wijk, JA. Hypertension and microalbuminuria in children with congenital solitary kidneys. J Paediatr Child Health. 2008; 44, 363368.
14. Harrison, M, Langley-Evans, SC. Intergenerational programming of impaired nephrogenesis and hypertension in rats following maternal protein restriction during pregnancy. Br J Nutr. 2009; 101, 10201030.
15. Luzi, G, Bori, S, Iammarino, G, et al. Functional aspects of the fetal urinary apparatus in relation to growth. Arch Ital Urol Androl. 1996; 68, 912.
16. Hartman, HA, Lai, HL, Patterson, LT. Cessation of renal morphogenesis in mice. Dev Biol. 2007; 310, 379387.
17. Nascimento, FA, Ceciliano, TC, Aguila, MB, Mandarim-de-Lacerda, CA. Maternal vitamin D deficiency delays glomerular maturity in F1 and F2 offspring. PLoS One. 2012; 7, e41740.
18. Pennington, KA, Harper, JL, Sigafoos, AN, et al. Effect of food restriction and leptin supplementation on fetal programming in mice. Endocrinology. 2012; 153, 45564567.
19. Lisle, SJM, Lewis, RM, Petry, CJ, et al. Effect of maternal iron restriction during pregnancy on renal morphology in the adult rat offspring. Br J Nut. 2003; 90, 3339.
20. Barros, MA, De Brito Alves, JL, Nogueira, VO, Wanderley, AG, Costa-Silva, JH. Maternal low-protein diet induces changes in the cardiovascular autonomic modulation in male rat offspring. Nutr Metab Cardiovas Dis. 2015; 25, 123130.
21. Anson, RM, Guo, Z, de Cabo, R, et al. Intermittent fasting dissociates beneficial effects of dietary restriction on glucose metabolism and neuronal resistance to injury from calorie intake. Proc Natl Acad Sci. 2003; 100, 62166220.
22. Horne, BD, May, HT, Anderson, JL, et al. Usefulness of routine periodic fasting to lower risk of coronary artery disease in patients undergoing coronary angiography. Am J Cardiol. 2008; 102, 814819.
23. Mansi, KMS. Study the effects of Ramadan fasting on the serum glucose and lipid profile among healthy Jordanian students. Am J Appl Sci. 2007; 4, 565569.
24. Khoshdel, A, Kheiri, S, Hashemi-Dehkordi, E, et al. The effect of Ramadan fasting on LH, FSH, oestrogen, progesterone and leptin in pregnant women. J Obstet Gynaecol. 2014; 34, 634638.
25. Firouzbakht, M, Kiapour, A, Jamali, B, et al. Fasting in pregnancy: a survey of beliefs and manners of Muslim women about Ramadan fasting. Ann Trop Med Pub Heal. 2013; 6, 536.
26. Alwasel, SH, Harrath, A, Aljarallah, JS, et al. Intergenerational effects of in utero exposure to Ramadan in Tunisia. Am J Hum Biol. 2013; 25, 341343.
27. Saito, T, Sumithran, E, Glasgow, EF, Atkins, RC. The enhancement of aminonucleoside nephrosis by the co-administration of protamine. Kidney Int. 1987; 32, 691699.
28. Leelahavanichkul, A, Yan, Q, Hu, X, et al. Angiotensin II overcomes strain-dependent resistance of rapid CKD progression in a new remnant kidney mouse model. Kidney Int. 2010; 78, 11361153.
29. Schreuder, MF, Nyengaard, JR, Fodor, M, van Wijk, JA, Delemarre-van de Waal, HA. Glomerular number and function are influenced by spontaneous and induced low birth weight in rats. J Am Soc Nephrol. 2005; 16, 29132919.
30. Nyengaard, JR. Stereologic methods and their application in kidney research. J Am Soc Nephrol. 1999; 10, 11001123.
31. Paulino-Silva, KM, Costa-Silva, JH. Hypertension in rat offspring subjected to perinatal protein malnutrition is not related to the baroreflex dysfunction. Clin Exp Pharmacol Physiol. 2016; 43, 10461053.
32. Alzamendi, A, Zubiría, G, Moreno, G, et al. High risk of metabolic and adipose tissue dysfunctions in adult male progeny, due to prenatal and adulthood malnutrition induced by fructose rich diet. Nutrients. 2016; 8, 178.
33. Léonhardt, M, Lesage, J, Dufourny, L, et al. Perinatal maternal food restriction induces alterations in hypothalamo-pituitary-adrenal axis activity and in plasma corticosterone-binding globulin capacity of weaning rat pups. Neuroendocrinology. 2002; 75, 4554.
34. Akitake, Y, Katsuragi, S, Hosokawa, M, et al. Moderate maternal food restriction in mice impairs physical growth, behavior, and neurodevelopment of offspring. Nutr Res. 2015; 35, 7687.
35. Fleeman, TL, Cappon, GD, Chapin, RE, Hurtt, ME. The effects of feed restriction during organogenesis on embryo-fetal development in the rat. Birth Defects Res B Dev Rep Toxicol. 2005; 74, 442449.
36. Awwad, J, Usta, IM, Succar, J, et al. The effect of maternal fasting during Ramadan on preterm delivery: a prospective cohort study. BJOG. 2012; 119, 13791386.
37. Cleal, JK, Poore, KR, Newman, JP, et al. The effect of maternal undernutrition in early gestation on gestation length and fetal and postnatal growth in sheep. Pediatr Res. 2007; 62, 422427.
38. Almond, D, Mazumder, B. Health capital and the prenatal environment: the effect of maternal fasting during pregnancy (No. w14428). Natl Bur Eco Res. 2008; 14428, 179.
39. Sharp, D. The fetal matrix: evolution, development and disease. J R Soc Med. 2005; 98, 130131.
40. Almond, D, Mazumder, B. Health capital and the prenatal environment: the effect of Ramadan observance during pregnancy. Am Econ J Appl Econ. 2011; 3, 5685.
41. Woodall, SM, Johnston, BM, Breier, BH, Gluckman, PD. Chronic maternal undernutrition in the rat leads to delayed postnatal growth and elevated blood pressure of offspring. Pediatr Res. 1996; 40, 438443.
42. Osmond, C, Barker, DJ, Winter, PD, Fall, CH, Simmonds, SJ. Early growth and death from cardiovascular disease in women. Br Med J. 1993; 307, 15191524.
43. Tafti, SA, Nast, CC, Desai, M, et al. Maternal undernutrition upregulates apoptosis in offspring nephrogenesis. J Dev Orig Health Dis. 2011; 2, 226235.
44. Welham, SJ, Wade, A, Woolf, AS. Protein restriction in pregnancy is associated with increased apoptosis of mesenchymal cells at the start of rat metanephrogenesis. Kidney Int. 2002; 61, 12311242.
45. Singh, RR, Moritz, KM, Bertram, JF, Cullen-McEwen, LA. Effects of dexamethasone exposure on rat metanephric development: in vitro and in vivo studies. Am J Physiolo Renal Physiol. 2007; 293, F548F554.
46. Pham, TD, MacLennan, NK, Chiu, CT, et al. Uteroplacental insufficiency increases apoptosis and alters p53 gene methylation in the full-term IUGR rat kidney. Am J Physiol Regul Integr Comp Physiol. 2003; 285, R962R970.
47. Hokke, SN, Armitage, JA, Puelles, VG, et al. Altered ureteric branching morphogenesis and nephron endowment in offspring of diabetic and insulin-treated pregnancy. PloS One. 2013; 8, e58243.
48. Awazu, M, Hida, M. Maternal nutrient restriction inhibits ureteric bud branching but does not affect the duration of nephrogenesis in rats. Pediatr Res. 2015; 77, 633639.
49. Vaccari, B, Mesquita, FF, Gontijo, JA, Boer, PA. Fetal kidney programming by severe food restriction: effects on structure, hormonal receptor expression and urinary sodium excretion in rats. J Renin Angiotensin Aldosterone Syst. 2015; 16, 3346.
50. Benz, K, Amann, K. Maternal nutrition, low nephron number and arterial hypertension in later life. Biochim Biophys Acta. 2010; 1802, 13091317.
51. Woods, LL, Weeks, DA, Rasch, R. Programming of adult blood pressure by maternal protein restriction: role of nephrogenesis. Kidney Int. 2004; 65, 13391348.
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Journal of Developmental Origins of Health and Disease
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