Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-745bb68f8f-grxwn Total loading time: 0 Render date: 2025-01-09T13:05:59.344Z Has data issue: false hasContentIssue false

Chapter 10 - Cardiometabolic and Renal DOHaD Outcomes in Offspring of Complicated Pregnancy

from Section III - Outcomes

Published online by Cambridge University Press:  01 December 2022

By
Dino A. Giussani ,
Rebecca M. Reynolds ,
Paul Leeson ,
Karen M. Moritz ,
John F. Bertram  and
Susan E. Ozanne
Edited by
Lucilla Poston ,
Keith M. Godfrey ,
Peter D. Gluckman  and
Mark A. Hanson
Lucilla Poston
Affiliation:
King's College London
Keith M. Godfrey
Affiliation:
University of Southampton
Peter D. Gluckman
Affiliation:
University of Auckland
Mark A. Hanson
Affiliation:
University of Southampton
Get access

Summary

It is now over thirty years since epidemiological studies revealed a relationship between low birth weight and subsequent risk of developing traditionally adult-onset diseases, such as type 2 diabetes, cardiovascular and renal disease. Initial focus was directed towards the importance of fetal undernutrition. However, it is now recognized that a range of other in utero adverse exposures including chronic fetal hypoxia, maternal over-nutrition and maternal stress can also lead to increased risk of cardio-metabolic and renal diseases in later life. Animal models, including those using non-human primates, sheep and rodents have been critical in demonstrating causality of relationships and helped to define underlying mechanisms, such as epigenetic programming of gene expression and oxidative stress. As the field moves forward in the coming years, these mechanistic studies will help to identify rational intervention strategies to reduce the developmental programming of cardiometabolic and renal dysfunction in suboptimal pregnancy.

Type
Chapter
Information
Developmental Origins of Health and Disease , pp. 85 - 99
Publisher: Cambridge University Press
Print publication year: 2022

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

Barker, DJ, Osmond, C. Low birth weight and hypertension. BMJ. 1988;297(6641):134–5.Google Scholar
Brenner, BM, Garcia, DL, Anderson, S. Glomeruli and blood pressure: less of one, more the other? Am J Hypertens. 1988;1:335–47.Google Scholar
Hales, CN, Barker, DJ, Clark, PM, et al. Fetal and infant growth and impaired glucose tolerance at age 64. BMJ. 1991;303(6809):1019–22.Google Scholar
Barker, DJ, Hales, CN, Fall, CH, Osmond, C, Phipps, K, Clark, PM. Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia. 1993;36(1):62–7.Google Scholar
Lewandowski, AJ, Augustine, D, Lamata, P, et al. Preterm heart in adult life: cardiovascular magnetic resonance reveals distinct differences in left ventricular mass, geometry, and function. Circulation. 2013;127(2):197–206.Google Scholar
Leeson, CP, Whincup, PH, Cook, DG, et al. Flow-mediated dilation in 9- to 11-year-old children: the influence of intrauterine and childhood factors. Circulation. 1997;96(7):2233–8.Google Scholar
Leeson, CP, Kattenhorn, M, Morley, R, Lucas, A, Deanfield, JE. Impact of low birth weight and cardiovascular risk factors on endothelial function in early adult life. Circulation. 2001;103(9):1264–8.Google Scholar
Barker, DJ, Osmond, C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet (London, England). 1986;1(8489):1077–81.Google Scholar
de Rooij, SR, Painter, RC, Phillips, DI, et al. Impaired insulin secretion after prenatal exposure to the Dutch famine. Diabetes Care. 2006;29(8):1897–901.Google Scholar
Roseboom, T, de Rooij, S, Painter, R. The Dutch famine and its long-term consequences for adult health. Early Hum Dev. 2006;82(8):485–91.Google Scholar
Giussani, DA, Davidge, ST. Developmental programming of cardiovascular disease by prenatal hypoxia. J Dev Orig Health Dis. 2013;4(5):328–37. ReviewGoogle Scholar
Giussani, DA. The fetal brain sparing response to hypoxia: physiological mechanisms. J Physiol. 2016;594(5):1215–30. Review.Google Scholar
Soria, R, Julian, CG, Vargas, E, Moore, LG, Giussani, DA. Graduated effects of high-altitude hypoxia and highland ancestry on birth size. Pediatr Res. 2013;74(6):633–8.Google Scholar
Sartori, C, Allemann, Y, Trueb, L, Delabays, A, Nicod, P, Scherrer, U. Augmented vasoreactivity in adult life associated with perinatal vascular insult. Lancet. 1999;353(9171):2205–7.Google Scholar
Sehgal, A, Skilton, MR. Crispi F3. Human fetal growth restriction: a cardiovascular journey through to adolescence. J Dev Orig Health Dis. 2016 Dec;7(6):626–35.Google Scholar
Lewandowski, AJ, Leeson, P. Preeclampsia, prematurity and cardiovascular health in adult life. Early Hum Dev. 2014;90(11):725–9.Google Scholar
Lewandowski, AJ, Lazdam, M, Davis, E, et al. Short-term exposure to exogenous lipids in premature infants and long-term changes in aortic and cardiac function. Arterioscler Thromb Vasc Biol. 2011;31(9):2125–35.Google Scholar
Kelly, BA, Lewandowski, AJ, Worton, SA, et al. Antenatal glucocorticoid exposure and long-term alterations in aortic function and glucose metabolism. Pediatrics. 2012;129(5):e1282–90.Google Scholar
Langley-Evans, SC, Phillips, GJ, Benediktsson, R, Gardner, DS, Edwards, CR, Jackson, AA, Seckl, JR. Protein intake in pregnancy, placental glucocorticoid metabolism and the programming of hypertension in the rat. Placenta. 1996;17(2–3):169–72.Google Scholar
Zelko, IN, Zhu, J, Roman, J. Maternal undernutrition during pregnancy alters the epigenetic landscape and the expression of endothelial function genes in male progeny. Nutr Res. 2019;61:53–63.Google Scholar
Fleming, TP, Watkins, AJ, Velazquez, MA, Mathers, JC, Prentice, AM, Stephenson, J, Barker, M, Saffery, R, Yajnik, CS, Eckert, JJ, Hanson, MA, Forrester, T, Gluckman, PD, Godfrey, KM. Origins of lifetime health around the time of conception: causes and consequences. Lancet 2018;391(10132):1842–52.Google Scholar
Beauchamp, B, Thrush, AB, Quizi, J, Antoun, G, McIntosh, N, Al-Dirbashi, OY, Patti, ME, Harper, ME. Undernutrition during pregnancy in mice leads to dysfunctional cardiac muscle respiration in adult offspring. Biosci Rep. 2015 Apr 10;35(3):e00200. doi: 10.1042/BSR20150007.Google Scholar
Jimenez-Chillarón, JC, Isganaitis, E, Charalambous, M, Gesta, S, Pentinat-Pelegrin, T, Faucette, RR, Otis, JP, Chow, A, Diaz, R, Ferguson-Smith, A, Patti, ME. Intergenerational transmission of glucose intolerance and obesity by in utero undernutrition in mice. Diabetes. 2009; 58(2):460–8Google Scholar
Zambrano, E, Martínez-Samayoa, PM, Bautista, CJ, Deás, M, Guillén, L, Rodríguez-González, GL, Guzmán, C, Larrea, F, Nathanielsz, PW. Sex differences in transgenerational alterations of growth and metabolism in progeny (F2) of female offspring (F1) of rats fed a low protein diet during pregnancy and lactation. J Physiol. 2005;566(Pt 1):225–36.Google Scholar
Torrens, C, Poston, L, Hanson, MA. Transmission of raised blood pressure and endothelial dysfunction to the F2 generation induced by maternal protein restriction in the F0, in the absence of dietary challenge in the F1 generation. Br J Nutr. 2008;100(4):760–6.Google Scholar
Bertram, C, Khan, O, Ohri, S, Phillips, DI, Matthews, SG, Hanson, MA. Transgenerational effects of prenatal nutrient restriction on cardiovascular and hypothalamic-pituitary-adrenal function. J Physiol. 2008;586(8):2217–29.Google Scholar
Morrison, JL, Botting, KJ, Darby, JRT, David, AL, Dyson, RM, Gatford, KL, Gray, C, Herrera, EA, Hirst, JJ, Kim, B, Kind, KL, Krause, BJ, Matthews, SG, Palliser, HK, Regnault, TRH, Richardson, BS, Sasaki, A, Thompson, LP, Berry, MJ. Guinea pig models for translation of the developmental origins of health and disease hypothesis into the clinic. J Physiol. 2018;596(23):5535–69.Google Scholar
Torrens, C, Snelling, TH, Chau, R, Shanmuganathan, M, Cleal, JK, Poore, KR, Noakes, DE, Poston, L, Hanson, MA, Green, LR. Effects of pre- and periconceptional undernutrition on arterial function in adult female sheep are vascular bed dependent. Exp Physiol. 2009;94(9):1024–33.Google Scholar
Poore, KR, Hollis, LJ, Murray, RJ, Warlow, A, Brewin, A, Fulford, L, Cleal, JK, Lillycrop, KA, Burdge, GC, Hanson, MA, Green, LR. Differential pathways to adult metabolic dysfunction following poor nutrition at two critical developmental periods in sheep. PLoS One. 2014;9(3): e90994.Google Scholar
Ford, SP, Hess, BW, Schwope, MM, Nijland, MJ, Gilbert, JS, Vonnahme, KA, Means, WJ, Han, H, Nathanielsz, PW. Maternal undernutrition during early to mid-gestation in the ewe results in altered growth, adiposity, and glucose tolerance in male offspring. J Anim Sci. 2007;85(5):1285–94.Google Scholar
Kuo, AH, Li, C, Li, J, Huber, HF, Nathanielsz, PW, Clarke, GD. Cardiac remodelling in a baboon model of intrauterine growth restriction mimics accelerated ageing. J Physiol. 2017;595(4):1093–110.Google Scholar
Cambonie, G, Comte, B, Yzydorczyk, C, Ntimbane, T, Germain, N, Lê, NL, Pladys, P, Gauthier, C, Lahaie, I, Abran, D, Lavoie, JC, Nuyt, AM. Antenatal antioxidant prevents adult hypertension, vascular dysfunction, and microvascular rarefaction associated with in utero exposure to a low-protein diet. Am J Physiol Regul Integr Comp Physiol. 2007;292(3):R1236–45.Google Scholar
Tarry-Adkins, JL, Blackmore, HL, Martin-Gronert, MS, Fernandez-Twinn, DS, McConnell, JM, Hargreaves, IP, Giussani, DA, Ozanne, SE. Coenzyme Q10 prevents accelerated cardiac aging in a rat model of poor maternal nutrition and accelerated postnatal growth. Mol Metab. 2013;2(4):480–90.Google Scholar
Gray, C, Li, M, Reynolds, CM, Vickers, MH. Pre-weaning growth hormone treatment reverses hypertension and endothelial dysfunction in adult male offspring of mothers undernourished during pregnancy. PLoS One. 2013;8(1):e53505.Google Scholar
Rouwet, EV, Tintu, AN, Schellings, MW, van Bilsen, M, Lutgens, E, Hofstra, L, Slaaf, DW, Ramsay, G, Le Noble, FA. Hypoxia induces aortic hypertrophic growth, left ventricular dysfunction, and sympathetic hyperinnervation of peripheral arteries in the chick embryo. Circulation. 2002; 105(23): 2791–6.Google Scholar
Giussani, DA, Camm, EJ, Niu, Y, Richter, HG, Blanco, CE, Gottschalk, R, Blake, EZ, Horder, KA, Thakor, AS, Hansell, JA, Kane, AD, Wooding, FB, Cross, CM, Herrera, EA. Developmental programming of cardiovascular dysfunction by prenatal hypoxia and oxidative stress. PLoS One. 2012; 7(2):e31017.Google Scholar
Camm, EJ, Martin-Gronert, MS, Wright, NL, Hansell, JA, Ozanne, SE, Giussani, DA. Prenatal hypoxia independent of undernutrition promotes molecular markers of insulin resistance in adult offspring. FASEB J. 2011; 25(1):420–7.Google Scholar
Dolinsky, VW, Rueda-Clausen, CF, Morton, JS, Davidge, ST, Dyck, JRB. Continued postnatal administration of resveratrol prevents diet-induced metabolic syndrome in offspring born growth restricted. Diabetes 2011; 60:2274–84.Google Scholar
Patterson, AJ, Chen, M, Xue, Q, Xiao, D, Zhang, L. Chronic prenatal hypoxia induces epigenetic programming of PKC{epsilon} gene repression in rat hearts. Circ Res. 2010; 107(3):365–73.Google Scholar
Rook, W, Johnson, CD, Coney, AM, Marshall, JM. Prenatal hypoxia leads to increased muscle sympathetic nerve activity, sympathetic hyperinnervation, premature blunting of neuropeptide Y signaling, and hypertension in adult life. Hypertension. 2014;64(6):1321–7.Google Scholar
Brain, KL, Allison, BJ, Niu, Y, Cross, CM, Itani, N, Kane, AD, Herrera, EA, Skeffington, KL, Botting, KJ, Giussani, DA. Intervention against hypertension in the next generation programmed by developmental hypoxia. PLoS Biol. 2019 Jan 22;17(1):e2006552.Google Scholar
Garrud, TAC, Giussani, DA. Combined antioxidant and glucocorticoid therapy for safer treatment of preterm birth. Trends Endocrinol Metab. 2019;30(4):258–69. Review.Google Scholar
Jellyman, JK, Fletcher, AJW, Fowden, AL, Giussani, DA. Glucocorticoid maturation of fetal cardiovascular function. Trends Mol Med. 2020;26(2):170–84. Review.Google Scholar
Figueroa, JP, Rose, JC, Massmann, GA, Zhang, J, Acuña, G. Alterations in fetal kidney development and elevations in arterial blood pressure in young adult sheep after clinical doses of antenatal glucocorticoids. Pediatr Res. 2005 Sep;58(3):510–5.Google Scholar
Benediktsson, R, Lindsay, RS, Noble, J, Seckl, JR, Edwards, CR. Glucocorticoid exposure in utero: new model for adult hypertension. Lancet. 1993 Feb 6;341(8841):339–41. Erratum in: Lancet 1993 Feb 27;341(8844):572.Google Scholar
Celsi, G, Kistner, A, Aizman, R, Eklöf, AC, Ceccatelli, S, de Santiago, A, Jacobson, SH. Prenatal dexamethasone causes oligonephronia, sodium retention, and higher blood pressure in the offspring. Pediatr Res. 1998 Sep;44(3):317–22.Google Scholar
Dodic, M, Peers, A, Coghlan, JP, Wintour, M. Can excess glucocorticoid, predispose to cardiovascular and metabolic disease in middle age? Trends Endocrinol Metab. 1999 Apr;10(3):86–91.Google Scholar
Pulgar, VM, Figueroa, JP. Antenatal betamethasone administration has a dual effect on adult sheep vascular reactivity. Pediatr Res. 2006 Dec;60(6):705–10. Epub 2006 Oct 25.Google Scholar
Massmann, GA, Zhang, J, Seong, WJ, Kim, M, Figueroa, JP. Sex-dependent effects of antenatal glucocorticoids on insulin sensitivity in adult sheep: role of the adipose tissue renin angiotensin system. Am J Physiol Regul Integr Comp Physiol. 2017 Jun 1;312(6):R1029–R1038.Google Scholar
Huber, HF, Kuo, AH, Li, C, Jenkins, SL, Gerow, KG, Clarke, GD, Nathanielsz, PW. Antenatal synthetic glucocorticoid exposure at human therapeutic equivalent doses predisposes middle-age male offspring baboons to an obese phenotype that emerges with aging. Reprod Sci. 2019;26(5):591–9.Google Scholar
Nyirenda, MJ, Carter, R, Tang, JI, de Vries, A, Schlumbohm, C, Hillier, SG, Streit, F, Oellerich, M, Armstrong, VW, Fuchs, E, Seckl, JR. Prenatal programming of metabolic syndrome in the common marmoset is associated with increased expression of 11beta-hydroxysteroid dehydrogenase type 1. Diabetes. 2009;58(12):2873–9.Google Scholar
Xiong, F, Lin, T, Song, M, Ma, Q, Martinez, SR, Lv, J, MataGreenwood, E, Xiao, D, Xu, Z, Zhang, L. Antenatal hypoxia induces epigenetic repression of glucocorticoid receptor and promotes ischemic-sensitive phenotype in the developing heart. J Mol Cell Cardiol. 2016;91:160–71.Google Scholar
Wyrwoll, CS, Noble, J, Thomson, A, Tesic, D, Miller, MR, Rog-Zielinska, EA, Moran, CM, Seckl, JR, Chapman, KE, Holmes, MC. Pravastatin ameliorates placental vascular defects, fetal growth, and cardiac function in a model of glucocorticoid excess. Proc Natl Acad Sci U S A. 2016;113(22):6265–70.Google Scholar
Niu, Y, Herrera, EA, Evans, RD, Giussani, DA. Antioxidant treatment improves neonatal survival and prevents impaired cardiac function at adulthood following neonatal glucocorticoid therapy. J Physiol. 2013;591(20):5083–93.Google Scholar
Godfrey, KM, et al., Influence of maternal obesity on the long-term health of offspring. Lancet Diabetes Endocrinol. 2017;5(1):53–64.Google Scholar
Lahti-Pulkkinen, M, et al., Consequences of being overweight or obese during pregnancy on diabetes in the offspring: a record linkage study in Aberdeen, Scotland. Diabetologia. 2019;62(8):1412–19.Google Scholar
Reynolds, RM, et al., Maternal obesity during pregnancy and premature mortality from cardiovascular event in adult offspring: follow-up of 1 323 275 person years. BMJ. 2013;347:f4539.Google Scholar
Eriksson, JG, et al., Long-term consequences of maternal overweight in pregnancy on offspring later health: findings from the Helsinki Birth Cohort Study. Ann Med. 2014;46(6):434–8.Google Scholar
Smith, J, et al., Effects of maternal surgical weight loss in mothers on intergenerational transmission of obesity. J Clin Endocrinol Metab. 2009;94(11):4275–83.Google Scholar
Scholtens, DM, et al., Hyperglycemia and Adverse Pregnancy Outcome Follow-up Study (HAPO FUS): maternal glycemia and childhood glucose metabolism. Diabetes Care. 2019;42(3):381–92.Google Scholar
Kaseva, N, et al., Gestational diabetes but not prepregnancy overweight predicts for cardiometabolic markers in offspring twenty years later. J Clin Endocrinol Metab. 2019;104(7):2785–95.Google Scholar
Tarry-Adkins, JL, Aiken, CE, Ozanne, SE, Neonatal, infant, and childhood growth following metformin versus insulin treatment for gestational diabetes: a systematic review and meta-analysis. PLoS Med. 2019;16(8):e1002848.Google Scholar
Khan, IY, et al Gender-linked hypertension in offspring of lard-fed pregnant rats. Hypertension. 2003;41:168–75Google Scholar
Buckley, AJ, et al., Altered body composition and metabolism in the male offspring of high fat fed rats. Metabolism. 2005;54(4):500–7.Google Scholar
Taylor, PD, et al., Generation of maternal obesity models in studies of developmental programming in rodents. Methods Mol Biol. 2018;1735:167–99.Google Scholar
Samuelsson, AM, et al., Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension and insulin resistance: a novel murine model of developmental programming. Hypertension. 2008;51(2):383–92.Google Scholar
Alfaradhi, MZ, Fernandez-Twinn, DS, Martin-Gronert, MS, Musial, B, Fowden, A, Ozanne, SE. Oxidative stress and altered lipid homeostasis in the programming of offspring fatty liver by maternal obesity. Am J Physiol Regul Integr Comp Physiol. 2014;307(1):R26–34.Google Scholar
Fernandez-Twinn, DS, Blackmore, HL, Siggens, L, Giussani, DA, Cross, CM, Foo, R, Ozanne, SE. The programming of cardiac hypertrophy in the offspring by maternal obesity is associated with hyperinsulinemia, AKT, ERK, and mTOR activation. Endocrinology. 2012;153(12):5961–71.Google Scholar
Musial, B, Fernandez-Twinn, DS, Duque-Guimaraes, D, Carr, SK, Fowden, AL, Ozanne, SE, Sferruzzi-Perri, AN. Exercise alters the molecular pathways of insulin signaling and lipid handling in maternal tissues of obese pregnant mice. Physiol Rep. 2019;7(16):e14202.Google Scholar
Beeson, JH, Blackmore, HL, Carr, SK, Dearden, L, Duque-Guimarães, DE, Kusinski, LC, Pantaleão, LC, Pinnock, AG, Aiken, CE, Giussani, DA, Fernandez-Twinn, DS, Ozanne, SE. Maternal exercise intervention in obese pregnancy improves the cardiovascular health of the adult male offspring. Mol Metab. 2018;16:35–44.Google Scholar
Fernandez-Twinn, DS, Gascoin, G, Musial, B, Carr, S, Duque-Guimaraes, D, Blackmore, HL, Alfaradhi, MZ, Loche, E, Sferruzzi-Perri, AN, Fowden, AL, Ozanne, SE. Exercise rescues obese mothers’ insulin sensitivity, placental hypoxia and male offspring insulin sensitivity. Sci Rep. 2017;7:44650.Google Scholar
Ghnenis, AB, Odhiambo, JF, McCormick, RJ, Nathanielsz, PW, Ford, SP. Maternal obesity in the ewe increases cardiac ventricular expression of glucocorticoid receptors, proinflammatory cytokines and fibrosis in adult male offspring. PLoS One. 2017;12(12):e0189977.Google Scholar
Long, NM, et al., Maternal obesity and increased nutrient intake before and during gestation in the ewe results in altered growth, adiposity and glucose intolerance in adult offspring. J Anim Sci. 2010;88:2546–3553.Google Scholar
Sullivan, EL, et al., Maternal and postnatal high-fat diet consumption programs energy balance and hypothalamic melanocortin signaling in nonhuman primate offspring. Am J Physiol. 2017;313(2):R162–R179.Google Scholar
Van Assche, FA, Holemans, K, Aerts, L. Long-term consequences for offspring of diabetes during pregnancy. British Medical Bulletin. 2001;60(1):173–82.Google Scholar
Holemans, K, et al., Streptozotocin diabetes in the pregnant rat induces cardiovascular dysfunction in adult offspring. Diabetologia. 1999;42(1):81–9.Google Scholar
Steculorum, SM, Bouret, SG. Maternal diabetes compromises the organisation of hypothalamic feeding circuits and impairs leptin sensitivity in offspring. Endocrinology. 2011;152(11):4171–9.Google Scholar
Bertram, JF, Douglas-Denton, RN, Diouf, B, Hughson, MD, Hoy, WE. Human nephron number: implications for health and disease. Ped Nephrol. 2011; 26:1529–33.Google Scholar
Hoy, WE, Hughson, MD, Singh, GR, Douglas-Denton, R, Bertram, JF. Reduced nephron number and glomerulomegaly in Australian Aborigines: a group at high risk for renal disease and hypertension. Kidney Int. 2006; 70:104–10.Google Scholar
Kanzaki, G, Puelles, VG, Cullen-McEwen, LA, Hoy, WE, Okabayashi, Y, Tsuboi, N, Shimizu, A, Denton, KM, Hughson T. Yokoo, MD, Bertram, JF. New insights on glomerular hyperfiltration: a Japanese autopsy study. (*joint first authors). J Clin Invest Insight. 2(19) pii: 94334, 2017.Google Scholar
Zhang, Z, Quinlan, J, Hoy, W, Hughson, MD, Lemire, M, Hudson, T, Hueber, P-A, Benjamin, A, Roy, A, Pascuet, E, Goodyer, M, Raju, C, Houghton, F, Bertram, JF, Goodyer, P. A common RET variant is associated with reduced newborn kidney size and function. J Am Soc Nephrol. 19:2027–34, 2008.Google Scholar
Hughson, M, Farris III, AB, Douglas-Denton, R, Hoy, WE, Bertram, JF. Glomerular number and size in autopsy kidneys: the relationship to birth weight. Kidney Int. 63:2113–22, 2003.Google Scholar
Sutherland, MR, Gubhaju, L, Moore, L, Kent, AL, Dahlstrom, JE, Horne, RS, et al. Accelerated maturation and abnormal morphology in the preterm neonatal kidney. J Am Soc Nephrol. 2011;22(7):1365–74.Google Scholar
Luyckx, VA, Bertram, JF, Brenner, BM, Fall, C, Hoy, WE, Ozanne, SE, Vikse, BE. Effect of fetal and child health on kidney development and long-term risk of hypertension and kidney disease. The Lancet. 2013; 382:273–83.Google Scholar
Luyckx, VA, Moritz, KM, Bertram, JF. Developmental programming of blood pressure and renal function through the life-course. In: Skorecki, K, Chertow, GM, Marsden, PA, Taal, MW, Yu, ASL (eds) ‘Brenner and Rector’s The Kidney’, 11 edn. 2020. Elsevier: PhiladelphiaGoogle Scholar
Keller, G, Zimmer, G, Mall, G, Ritz, E, Amann, K. Nephron number in patients with primary hypertension. NEJM. 2003 348:101–8.Google Scholar
Hughson, MD, Douglas-Denton, R, Bertram, JF, Hoy, WE. Hypertension, glomerular number, and birth weight in African Americans and white subjects in the southeastern United States. Kidney Int. 2006;69:671–8.Google Scholar
White, SL, Perkovic, V, Cass, A, et al. Is low birth weight an antecedent of CKD in later life? A systematic review of observational studies. Am J Kidney Dis. 2009;54:248–61.Google Scholar
Keijzer-Keen, MG, Schrevel, M, Finken, MJ, et al. Microalbuminuria and lower glomerular filtration rate at young adult age in subjects born very premature and after intrauterine growth retardation. J Am Soc Nephrol. 2005;16:2762–68.Google Scholar
Denic, A, Mathew, J, Lerman, LO, Lieske, JC, Larson, JJ, Alexander, MP, Poggio, E, Glassock, RJ, Rule, AD. Single-nephron glomerular filtration rate in healthy adults. NEJM. 2017;376:2349–57.Google Scholar
Sasaki, T, Tsuboi, N, Okabayashi, Y, Haruhara, K, Kanzaki, G, Koike, K., Kobayashi, A., Yamamoto, I, Takahashi, S, Ninomiya, T., Shimizu, A, Rule, AD, Bertram, JF, Yokoo, T. Estimation of nephron number in living humans by combining unenhanced computed tomography with biopsy-based stereology. Sci. Reports (in press Sept 10 2019); 9(1):14400.Google Scholar
Baldelomar, EJ, Charlton, JR, deRonde, KA, Bennett, KM. In vivo measurements of kidney glomerular number and size in healthy and Os/+ mice using MRI. Am J Physiol Renal Physiol. 2019;317:F865–873.Google Scholar
Baldelomar, EJ, Charlton, JR, Beeman, SC, Bennett, KM. Measuring rat kidney glomerular number and size in vivo with MRI. Am J Physiol Renal Physiol. 2018;314:F399–F406.Google Scholar
Moritz, KM, Wintour-Coghlan, EM, Black, MJ, Bertram, JF, Caruana, G. Factors influencing mammalian kidney development: implications for health in adult life. Adv Anat Embryol Cell Biol. 2008;196:1–78.Google Scholar
Hokke, SN, 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.Google Scholar
Walton, S, Moritz, KM, Bertram, JF, Singh, RR. Lengths of nephron tubule segments and collecting ducts in the CD-1 mouse kidney: an ontogeny study. Am J Physiol Renal Physiol. 2016;311:F976–983.Google Scholar
Gonçalves, GD, Walton, SL, Gazzard, SE, van der Wolde, J, Mathias, PCF, Moritz, KM, Cullen-McEwen, LA, Bertram, JF. Maternal hypoxia developmentally programs low podocyte endowment in male, but not female offspring. Anat Rec. 2020;303:2668–78.Google Scholar
Gray, SP, Denton, KM, Cullen-McEwen, L, Bertram, JF, Moritz, KM. Prenatal exposure to alcohol reduces nephron number and raises blood pressure in progeny. J Am Soc Nephrol 2010;21(11):1891–902.Google Scholar
Stelloh, C, Allen, KP, Mattson, DL, Lerch-Gaggl, A, Reddy, S, El-Meanawy, A. Prematurity in mice leads to reduction in nephron number, hypertension, and proteinuria. Transl Res. 2012 Feb;159(2):80–9.Google Scholar
Woods, LL, Weeks, DA, Rasch, R. Programming of adult blood pressure by maternal protein restriction: role of nephrogenesis. Kidney Int. 2004 Apr;65(4):1339–48.Google Scholar
Zhang, J, Massmann, GA, Rose, JC, Figueroa, JP. Differential effects of clinical doses of antenatal betamethasone on nephron endowment and glomerular filtration rate in adult sheep. Reprod Sci 2010;17(2):186–95.Google Scholar
Walton, SL, Bielefeldt-Ohmann, H, Singh, RR, Li, J, Paravicini, TM, Little, MH, Moritz, KM. Prenatal hypoxia leads to hypertension, renal renin-angiotensin system activation and exacerbates salt-induced pathology in a sex-specific manner. Sci Rep. 2017 Aug 15;7(1):8241.Google Scholar
Moritz, KM, Mazzuca, MQ, Siebel, AL, Mibus, A, Arena, D, Tare, M, Owens, JA, Wlodek, ME. Uteroplacental insufficiency causes a nephron deficit, modest renal insufficiency but no hypertension with ageing in female rats. J Physiol. 2009;587(Pt 11):2635–46.Google Scholar
Hokke, SN, Arias, N, Armitage, JA, Puelles, V, Geraci, S, Gretz, N, Bertram, JF, Cullen-McEwen, LA. Maternal glucose intolerance reduces offspring nephron endowment and increases glomerular volume in adult offspring. Diab/Metab Res Rev. 2016;32:816–26.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×