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Section III - Outcomes

Published online by Cambridge University Press:  01 December 2022

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
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Print publication year: 2022

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References

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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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):e128290.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, , 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):R123645.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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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):R1029R1038.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.CrossRefGoogle 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):R2634.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):R162R179.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:F865873.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:F399F406.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:F976983.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

References

Asher, MI, Rutter, CE, Bissell, K, Chiang, CY, El Sony, A, Ellwood, E et al. Global asthma network phase I study group. Worldwide trends in the burden of asthma symptoms in school-aged children: Global asthma network phase I cross-sectional study. Lancet. 2021 Oct 30;398(10311):1569–80. doi: 10.1016/S0140-6736(21)01450-1.Google Scholar
Tai, A, Tran, H, Roberts, M, Clarke, N, Wilson, J, Robertson, CF. The association between childhood asthma and adult chronic obstructive pulmonary disease. Thorax. 2014 Sep;69(9):805–10. PubMed PMID: 24646659. Epub 2014/03/22. eng.Google Scholar
Lange, P, Celli, B, Agusti, A, Boje Jensen, G, Divo, M, Faner, R, et al. Lung-function trajectories leading to chronic obstructive pulmonary disease. N Engl J Med. 2015 Jul 9;373(2):111–22. PubMed PMID: 26154786. Epub 2015/07/15. eng.Google Scholar
Postma, DS, Rabe, KF. The asthma-COPD overlap syndrome. N Engl J Med. 2015 Sep 24;373(13):1241–9. PubMed PMID: 26398072. Epub 2015/09/24. eng.Google Scholar
Chronic Obstructive Pulmonary Disease (COPD): World Health Organisation; 2015 [updated March 2015. Available from: http://www.who.int/mediacentre/factsheets/fs315/en/.Google Scholar
The Global Initiative for Asthma (GINA]. https://ginasthmaorg/gina-reports/. 2021.Google Scholar
Asher, MI, Garcia-Marcos, L, Pearce, NE, Strachan, DP. Trends in worldwide asthma prevalence. Eur Respir J. 2020 Sep 24. PubMed PMID: 32972987. Epub 2020/09/26. eng.Google Scholar
Dharmage, SC, Perret, JL, Custovic, A. Epidemiology of asthma in children and adults. Front Pediatr. 2019;7:246. PubMed PMID: 31275909. PMCID: 6591438. Epub 2019/07/06. eng.Google Scholar
Barker, DJ, Osmond, C, Law, CM. The intrauterine and early postnatal origins of cardiovascular disease and chronic bronchitis. J Epidemiol Community Health. 1989 Sep;43(3):237–40. PubMed PMID: 2607302. PMCID: 1052843. Epub 1989/09/01. eng.Google Scholar
Duijts, L, Reiss, IK, Brusselle, G, de Jongste, JC. Early origins of chronic obstructive lung diseases across the life course. Eur J Epidemiol. 2014 Dec;29(12):871–85. PubMed PMID: 25537319. Epub 2014/12/30. eng.Google Scholar
van Meel, ER, Jaddoe, VWV, Bonnelykke, K, de Jongste, JC, Duijts, L. The role of respiratory tract infections and the microbiome in the development of asthma: A narrative review. Pediatr Pulmonol. 2017 Oct;52(10):1363–70. PubMed PMID: 28869358. PMCID: 7168085. Epub 2017/09/05. eng.Google Scholar
Vehmeijer, FOL, Guxens, M, Duijts, L, El Marroun, H. Maternal psychological distress during pregnancy and childhood health outcomes: a narrative review. J Dev Orig Health Dis. 2019 Jun;10(3):274–85. PubMed PMID: 30378522. Epub 2018/11/01. eng.Google Scholar
Mensink-Bout, SM, van Meel, ER, de Jongste, JC, Annesi-Maesano, I, Aubert, AM, Bernard, JY, et al. Dietary inflammatory index and non-communicable disease risk: A narrative review. Nutrients. 2019 Aug 12;11(8):1873. PubMed PMID: 31408965. PMCID: 6722630. Epub 2019/08/15. eng.Google Scholar
den Dekker, HT, Sonnenschein-van der Voort, AMM, de Jongste, JC, Anessi-Maesano, I, Arshad, SH, Barros, H, et al. Early growth characteristics and the risk of reduced lung function and asthma: A meta-analysis of 25,000 children. J Allergy Clin Immunol. 2016 Apr;137(4):1026–35. PubMed PMID: 26548843. Epub 2015/11/10. eng.Google Scholar
Turner, S. Perinatal programming of childhood asthma: early fetal size, growth trajectory during infancy, and childhood asthma outcomes. Clin Dev Immunol. 2012;2012:962923. PubMed PMID: 22400043. PMCID: 3287283. Epub 2012/03/09. eng.Google Scholar
Mensink-Bout, SM, Santos, S, van Meel, ER, Oei, EHG, de Jongste, JC, Jaddoe, VWV, et al. General and organ fat assessed by magnetic resonance imaging and respiratory outcomes in childhood. Am J Respir Crit Care Med. 2020 Feb 1;201(3):348–55. PubMed PMID: 31597047. Epub 2019/10/10. eng.Google Scholar
Burke, H, Leonardi-Bee, J, Hashim, A, Pine-Abata, H, Chen, Y, Cook, DG, et al. Prenatal and passive smoke exposure and incidence of asthma and wheeze: systematic review and meta-analysis. Pediatrics. 2012 Apr;129(4):735–44. PubMed PMID: 22430451. Epub 2012/03/21. eng.Google Scholar
Silvestri, M, Franchi, S, Pistorio, A, Petecchia, L, Rusconi, F. Smoke exposure, wheezing, and asthma development: a systematic review and meta-analysis in unselected birth cohorts. Pediatr Pulmonol. 2015 Apr;50(4):353–62. PubMed PMID: 24648197. Epub 2014/03/22. eng.Google Scholar
Lin, W, Brunekreef, B, Gehring, U. Meta-analysis of the effects of indoor nitrogen dioxide and gas cooking on asthma and wheeze in children. Int J Epidemiol. 2013 Dec;42(6):1724–37. PubMed PMID: 23962958. Epub 2013/08/22. eng.Google Scholar
Fuertes, E, Sunyer, J, Gehring, U, Porta, D, Forastiere, F, Cesaroni, G, et al. Associations between air pollution and pediatric eczema, rhinoconjunctivitis and asthma: A meta-analysis of European birth cohorts. Environ Int. 2020 Mar;136:105474. PubMed PMID: 31962272. Epub 2020/01/22. eng.Google Scholar
Hehua, Z, Qing, C, Shanyan, G, Qijun, W, Yuhong, Z. The impact of prenatal exposure to air pollution on childhood wheezing and asthma: A systematic review. Environ Res. 2017 Nov;159:519–30. PubMed PMID: 28888196. Epub 2017/09/10. eng.Google Scholar
Khreis, H, Cirach, M, Mueller, N, de Hoogh, K, Hoek, G, Nieuwenhuijsen, MJ, et al. Outdoor air pollution and the burden of childhood asthma across Europe. Eur Respir J. 2019 Oct;54(4). PubMed PMID: 31391220. Epub 2019/08/09. eng.Google Scholar
Mensink-Bout, SM, van Meel, ER, de Jongste, JC, Annesi-Maesano, I, Aubert, AM, Bernard, JY, et al. Maternal diet in pregnancy and child’s respiratory outcomes: an individual participant data meta-analysis of 18 000 children. Eur Respir J. 2021 Sep 9. PubMed PMID: 34503987. Epub 2021/09/11. eng.Google Scholar
Huang, L, Chen, Q, Zhao, Y, Wang, W, Fang, F, Bao, Y. Is elective cesarean section associated with a higher risk of asthma? A meta-analysis. J Asthma. 2015 Feb;52(1):16–25. PubMed PMID: 25162303. Epub 2014/08/28. eng.Google Scholar
Keag, OE, Norman, JE, Stock, SJ. Long-term risks and benefits associated with cesarean delivery for mother, baby, and subsequent pregnancies: Systematic review and meta-analysis. PLoS Med. 2018 Jan;15(1):e1002494. PubMed PMID: 29360829. PMCID: 5779640. Epub 2018/01/24. eng.CrossRefGoogle Scholar
Rusconi, F, Zugna, D, Annesi-Maesano, I, Baiz, N, Barros, H, Correia, S, et al. Mode of delivery and asthma at school age in 9 European Birth Cohorts. Am J Epidemiol. 2017 Mar 15;185(6):465–73. PubMed PMID: 28399567. Epub 2017/04/12. eng.Google Scholar
Barker, DJ, Godfrey, KM, Fall, C, Osmond, C, Winter, PD, Shaheen, SO. Relation of birth weight and childhood respiratory infection to adult lung function and death from chronic obstructive airways disease. BMJ. 1991 Sep 21;303(6804):671–5. PubMed PMID: 1912913. PMCID: 1670943. Epub 1991/09/21. eng.Google Scholar
Blanken, MO, Rovers, MM, Molenaar, JM, Winkler-Seinstra, PL, Meijer, A, Kimpen, JL, et al. Respiratory syncytial virus and recurrent wheeze in healthy preterm infants. N Engl J Med. 2013 May 9;368(19):1791–9. PubMed PMID: 23656644.CrossRefGoogle Scholar
Simoes, EA, Carbonell-Estrany, X, Rieger, CH, Mitchell, I, Fredrick, L, Groothuis, JR, et al. The effect of respiratory syncytial virus on subsequent recurrent wheezing in atopic and nonatopic children. J Allergy Clin Immunol. 2010 Aug;126(2):256–62. PubMed PMID: 20624638.Google Scholar
Zimmermann, P, Messina, N, Mohn, WW, Finlay, BB, Curtis, N. Association between the intestinal microbiota and allergic sensitization, eczema, and asthma: A systematic review. J Allergy Clin Immunol. 2019 Feb;143(2):467–85. PubMed PMID: 30600099. Epub 2019/01/03. eng.Google Scholar
Hu, C, van Meel, ER, Medina-Gomez, C, Kraaij, R, Barroso, M, Jong, JK, et al. A Population-based Study on Associations of Stool Microbiota with Atopic Diseases in School-age Children. J Allergy Clin Immunol. 2021 Apr 13. PubMed PMID: 33862008. Epub 2021/04/17. eng.Google Scholar
Palmer, LJ, Knuiman, MW, Divitini, ML, Burton, PR, James, AL, Bartholomew, HC, et al. Familial aggregation and heritability of adult lung function: results from the Busselton Health Study. Eur Respir J. 2001 Apr;17(4):696–702. PubMed PMID: 11401066. Epub 2001/06/13. eng.Google Scholar
El-Husseini, ZW, Gosens, R, Dekker, F, Koppelman, GH. The genetics of asthma and the promise of genomics-guided drug target discovery. Lancet Respir Med. 2020 Oct;8(10):1045–56. PubMed PMID: 32910899. Epub 2020/09/11. eng.Google Scholar
Qi, C, Xu, CJ, Koppelman, GH. The role of epigenetics in the development of childhood asthma. Expert Rev Clin Immunol. 2019 Dec;15(12):1287–302. PubMed PMID: 31674254. Epub 2019/11/02. eng.Google Scholar
Joubert, BR, den Dekker, HT, Felix, JF, Bohlin, J, Ligthart, S, Beckett, E, et al. Maternal plasma folate impacts differential DNA methylation in an epigenome-wide meta-analysis of newborns. Nat Commun. 2016;7:10577. PubMed PMID: 26861414. PMCID: 4749955. Epub 2016/02/11. eng.Google Scholar
Joubert, BR, Felix, JF, Yousefi, P, Bakulski, KM, Just, AC, Breton, C, et al. DNA Methylation in newborns and maternal smoking in pregnancy: Genome-wide Consortium meta-analysis. Am J Hum Genet. 2016 Apr 7;98(4):680–96. PubMed PMID: 27040690. PMCID: 4833289. Epub 2016/04/05. eng.Google Scholar
den Dekker, HT, Burrows, K, Felix, JF, Salas, LA, Nedeljkovic, I, Yao, J, et al. Newborn DNA-methylation, childhood lung function, and the risks of asthma and COPD across the life course. Eur Respir J. 2019 Apr;53(4):1801795. PubMed PMID: 30765504. Epub 2019/02/16. eng.Google Scholar
Guxens, M, Sonnenschein-van der Voort, AM, Tiemeier, H, Hofman, A, Sunyer, J, de Jongste, JC, et al. Parental psychological distress during pregnancy and wheezing in preschool children: the Generation R Study. J Allergy Clin Immunol. 2014 Jan;133(1):59–67 e1–12. PubMed PMID: 23777854. Epub 2013/06/20. eng.Google Scholar
Lundholm, C, Gunnerbeck, A, D’Onofrio, BM, Larsson, H, Pershagen, G, Almqvist, C. Smoking and snuff use in pregnancy and the risk of asthma and wheeze in pre-schoolchildren-A population-based register study. Clin Exp Allergy. 2020 May;50(5):597–608. PubMed PMID: 32149429. Epub 2020/03/10. eng.Google Scholar
Granell, R, Henderson, AJ, Evans, DM, Smith, GD, Ness, AR, Lewis, S, et al. Effects of BMI, fat mass, and lean mass on asthma in childhood: a Mendelian randomization study. PLoS Med. 2014 Jul;11(7):e1001669. PubMed PMID: 24983943. PMCID: 4077660. Epub 2014/07/02. eng.Google Scholar
Wolsk, HM, Chawes, BL, Litonjua, AA, Hollis, BW, Waage, J, Stokholm, J, et al. Prenatal vitamin D supplementation reduces risk of asthma/recurrent wheeze in early childhood: A combined analysis of two randomized controlled trials. PLoS One. 2017;12(10):e0186657. PubMed PMID: 29077711. PMCID: 5659607. Epub 2017/10/28. eng.Google Scholar
Sears, MR. Predicting asthma outcomes. J Allergy Clin Immunol. 2015 Oct;136(4):829–36; quiz 37. PubMed PMID: 26449797. Epub 2015/10/10. eng.Google Scholar

References

Vaiserman, A, Koliada, A, Lushchak, O. Developmental programming of aging trajectory. Ageing Res Rev. 2018;47:105–22.Google Scholar
Aiken, CE, Ozanne, SE. Transgenerational developmental programming. Hum Reprod Update. 2014;20(1):63–75.CrossRefGoogle Scholar
Dennison, EM, Syddall, HE, Sayer, AA, Gilbody, HJ, Cooper, C. Birth weight and weight at 1 year are independent determinants of bone mass in the seventh decade: the Hertfordshire cohort study. Pediatr Res. 2005;57(4):582–6.Google Scholar
Kemp, BR, Ferraro, KF, Morton, PM, Mustillo, SA. Early origins of adult cancer risk among men and women: influence of childhood misfortune. J Aging Health. 2018;30(1):140–63.Google Scholar
Belsky, DW, Caspi, A, Cohen, HJ, Kraus, WE, Ramrakha, S, Poulton, R, et al. Impact of early personal-history characteristics on the Pace of Aging: implications for clinical trials of therapies to slow aging and extend healthspan. Aging Cell. 2017;16(4):644–51.Google Scholar
Reynolds, RM, Allan, KM, Raja, EA, Bhattacharya, S, McNeill, G, Hannaford, PC. Maternal obesity during pregnancy and premature mortality from cardiovascular event in adult offspring: follow-up of 1 323 275 person years. The BMJ. 2013;347. f4539. doi: 10.1136/bmj.f4539.Google Scholar
Padmanabhan, V, Cardoso, RC, Puttabyatappa, M. Developmental programming, a pathway to disease. Endocrinology. 2016;157(4):1328–40.Google Scholar
Cameron, CM, Shibl, R, McClure, RJ, Ng, SK, Hills, AP. Maternal pregravid body mass index and child hospital admissions in the first 5 years of life: results from an Australian birth cohort. Int J Obes. 2014;38:1268–74. doi: 10.1038/ijo.2014.148. Epub 2014 Jul 25.Google Scholar
Haapanen, MJ, Perälä, MM, Salonen, MK, Kajantie, E, Simonen, M, Pohjolainen, P, et al. Early life stress and frailty in old age: the Helsinki birth cohort study. BMC Geriatr. 2018;18(1):179.Google Scholar
Todd, N, Valleron, A-J, Bougnères, P. Prenatal loss of father during World War One is predictive of a reduced lifespan in adulthood. Proc Natl Acad Sci U S A. 2017;114(16):4201–6.Google Scholar
Yan, X, Huang, Y, Wang, H, Du, M, Hess, BW, Ford, SP, et al. Maternal obesity induces sustained inflammation in both fetal and offspring large intestine of sheep. Inflamm Bowel Dis. 2011;17(7):1513–22.Google Scholar
Tsoulis, MW, Chang, PE, Moore, CJ, Chan, KA, Gohir, W, Petrik, JJ, et al. Maternal high-fat diet-induced loss of fetal oocytes is associated with compromised follicle growth in adult rat offspring. Biol Reprod. 2016;94(4):94.Google Scholar
Ambeskovic, M, Roseboom, TJ, Metz, GAS. Transgeneratioanl effects of early environmental insults on aging and disease incidence. Neurosci Biobehav Rev. 2020; 117: 297–316.CrossRefGoogle Scholar
Metz, GAS, Ng, JWY, Kovalchuk, I, Olson, DM. Ancestral experience as a game changer in stress vulnerability and disease outcomes. BioEssays. 2015;37(6):602–11.CrossRefGoogle Scholar
Gluckman, PD, Beedle, AS. Migrating ovaries: early life influences on later gonadal function. PLOS Medicine. 2007;4(5):e190.Google Scholar
May-Panloup, P, Boucret, L, Chao de la Barca, JM, Desquiret-Dumas, V, Ferré-L’Hotellier, V, Morinière, C, et al. Ovarian ageing: the role of mitochondria in oocytes and follicles. Hum Reprod Update. 2016;22(6):725–43.Google Scholar
Jazwiec, PA, Sloboda, DM. Nutritional adversity, sex and reproduction: 30 years of DOHaD and what have we learned? J Endocrinol. 2019;242(1):T51t68.Google Scholar
Sanchez, F, Smitz, J. Molecular control of oogenesis. Biochim Biophys Acta. 2012;1822(12):1896–912.Google Scholar
Mamsen, LS, Brochner, CB, Byskov, AG, Mollgard, K. The migration and loss of human primordial germ stem cells from the hind gut epithelium towards the gonadal ridge. Int J Dev Biol. 2012;56(10–12):771–8.Google Scholar
Haglund, K, Nezis, IP, Stenmark, H. Structure and functions of stable intercellular bridges formed by incomplete cytokinesis during development. Commun Integr Biol. 2011;4(1):1–9.Google Scholar
Pepling, ME. Follicular assembly: mechanisms of action. Reproduction. 2012;143(2):139–49.Google Scholar
Pepling, ME, Spradling, AC. Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles. Dev Biol. 2001;234(2):339–51.Google Scholar
Hirshfield, AN. Development of follicles in the mammalian ovary. Int Rev Cytol. 1991;124:43–101.Google Scholar
Li, J, Kawamura, K, Cheng, Y, Liu, S, Klein, C, Liu, S, et al. Activation of dormant ovarian follicles to generate mature eggs. Proc Natl Acad Sci USA. 2010;107(22):10280–4.Google Scholar
Bale, TL. Lifetime stress experience: transgenerational epigenetics and germ cell programming. Dialogues Clin Neurosci. 2014;16(3):297–305.Google Scholar
Heijmans, BT, Tobi, EW, Stein, AD, Putter, H, Blauw, GJ, Susser, ES, et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci U S A. 2008;105(44):17046–9.Google Scholar
Lempradl, A. Germ cell-mediated mechanisms of epigenetic inheritance. Semin Cell Dev Biol. 2020;97:116–22. doi: 10.1016/j.semcdb.2019.07.012.Google Scholar
Jiménez-Chillarón, JC, Díaz, R, Martínez, D, Pentinat, T, Ramón-Krauel, M, Ribó, S, et al. The role of nutrition on epigenetic modifications and their implications on health. Biochimie. 2012;94(11):2242–63.Google Scholar
Bajrami, E, Spiroski, M. Genomic imprinting. Open Access Maced J Med Sci. 2016;4(1):181–4.Google Scholar
Wu, H, Hauser, R, Krawetz, SA, Pilsner, JR. Environmental susceptibility of the sperm epigenome during windows of male germ cell development. Curr Environ Health Rep. 2015;2(4):356–66.Google Scholar
Cooper, C, Kuh, D, Egger, P, Wadsworth, M, Barker, D. Childhood growth and age at menarche. Br J Obstet Gynaecol. 1996;103(8):814–7.Google Scholar
de Zegher, F, Ibánez, L. Novel insights into the endocrine-metabolic and reproductive consequences of prenatal growth restraint in girls. Girls-born-small become women-born-small. Verh K Acad Geneeskd Belg. 2004;66(5–6):353–82.Google Scholar
Ibanez, L, Valls, C, Cols, M, Ferrer, A, Marcos, MV, De Zegher, F. Hypersecretion of FSH in infant boys and girls born small for gestational age. J Clin Endocrinol Metab. 2002;87(5):1986–8.Google Scholar
Ibanez, L, Potau, N, Enriquez, G, Marcos, MV, De Zegher, F. Hypergonadotrophinaemia with reduced uterine and ovarian size in women born small-for-gestational-age. Hum Reprod. 2003;18(8):1565–9.Google Scholar
de Bruin, JP, Dorland, M, Bruinse, HW, Spliet, W, Nikkels, PGJ, te Velde, ER. Fetal growth retardation as a cuase of impaired ovarian development. Early Hum Dev. 1998;51(1):39–46.Google Scholar
de Bruin, JP, Nikkels, PGJ, Bruinse, HW, van Haaften, M, Looman, CWN, te Velde, ER. Morphometry of human ovaries in normal and growth restricted fetuses. Early Hum Dev. 2001;60(3):179–92.Google Scholar
Veening, MA, van Weissenbruch, MM, Roord, JJ, Delemarre-van de Waal, HA. Pubertal development in children born small for gestational age. J Pediatr Endocrinol Metab. 2004;17(11):1487–505.Google Scholar
Ibanez, L, de Zegher, F. Puberty and prenatal growth. Mol Cell Endocrinol. 2006;254–255:22–5.Google Scholar
Sadrzadeh-Broer, S, Kuijper, EA, Van Weissenbruch, MM, Lambalk, CB. Ovarian reserve in young women with low birth weight and normal puberty: a pilot case-control study. Gynecol Endocrinol. 2011;27(9):641–4.CrossRefGoogle Scholar
Shim, YS, Park, HK, Yang, S, Hwang, IT. Age at menarche and adult height in girls born small for gestational age. Ann Pediatr Endocrinol Metab. 2013;18(2):76–80.Google Scholar
Treloar, SA, Sadrzadeh, S, Do, K-A, Martin, NG, Lambalk, CB. Birth weight and age at menopause in Australian female twin pairs: exploration of the fetal origin hypothesis. Hum Reprod. 2000;15(1):55–9.Google Scholar
Sydsjö, G, Bladh, M, Rindeborn, K, Hammar, M, Rodriguez-Martinez, H, Nedstrand, E. Being born preterm or with low weight implies a risk of infertility and premature loss of ovarian function; a national register study. Ups J Med Sci. 2020;125(3):235–9.Google Scholar
Sloboda, DM, Hart, R, Doherty, DA, Pennell, CE, Hickey, M. Age at menarche: influences of prenatal and postnatal growth. J Clin Endocrinol Metab. 2007;92(1):46–50.Google Scholar
Hvidt, JJ, Brix, N, Ernst, A, Lauridsen, LLB, Ramlau-Hansen, CH. Size at birth, infant growth, and age at pubertal development in boys and girls. Clin Epidemiol. 2019;11:873–83.Google Scholar
Escobar-Morreale, HF. Polycystic ovary syndrome: definition, aetiology, disagnosis and treatment. Nat Rev Endocrinol. 2018;14(5):270–84.Google Scholar
Bani Mohammad, M, Majdi, Seghinsara, A. Polycystic Ovary Syndrome (PCOS), diagnostic criteria, and AMH. Asian Pac J Cancer Prev. 2017;18(1):17–21.Google Scholar
Shi, M, Huang, W, Shu, L, Hou, G, Guan, Y, Song, G. Research of polycystic ovary syndrome: a bibliometric analysis from 2009 to 2019. Gynecol Endocrinol. 2021:121–5. doi: 10.1080/09513590.2020.1807501.Epub 202. Aug 19.Google Scholar
Dumesic, DA, Oberfield, SE, Stener-Victorin, E, Marshall, JC, Laven, JS, Legro, RS. Scientific statement on the diagnostic criteria, epidemiology, pathophysiology, and molecular genetics of polycystic ovary syndrome. Endocr Rev. 2015;36(5):487–525.Google Scholar
Teede, HJ, Misso, ML, Costello, MF, Dokras, A, Laven, J, Moran, L, et al. Recommendations from the international evidence-based guideline for the assessment and management of polycystic ovary syndrome. Clin Endocrinol. 2018;89(3):251–68.Google Scholar
Hickey, M, Doherty, DA, Atkinson, H, Sloboda, DM, Franks, S, Norman, RJ, et al. Clinical, ultrasound and biochemical features of polycystic ovary syndrome in adolescents: implications for diagnosis. Hum Reprod. 2011;26(6):1469–77.Google Scholar
Dapas, M, Dunaif, A. The contribution of rare genetic variants to the pathogenesis of polycystic ovary syndrome. Curr Opin Endocr Metab Res. 2020;12:26–32.Google Scholar
de Zegher, F, Reinehr, T, Malpique, R, Darendeliler, F, López-Bermejo, A, Ibáñez, L. Reduced prenatal weight gain and/or augmented postnatal weight gain precedes polycystic ovary syndrome in adolescent girls. Obesity (Silver Spring). 2017;25(9):1486–9.Google Scholar
Sadrzadeh, S, Hui, EVH, Schoonmade, LJ, Painter, RC, Lambalk, CB. Birthweight and PCOS: systematic review and meta-analysis. Hum Reprod Open. 2017;2017(2).Google Scholar
Fall, CHD, Kumaran, K. Metabolic programming in early life humans. Philos Trans R Soc Lond B Bio Sci. 2019;374(1770):20180123-.Google Scholar
Lidaka, L, Grasmane, A, Lazdane, G, Dzivite-Krisane, I, Gailite, L, Viberga, I. Can a mother’s polycystic ovary syndrome (PCOS)-related symptoms be used to predict the future clinical profile of PCOS in her adolescent daughter? A pilot study. Eur J Contracept Reprod Health Care. 2020:1–6.Google Scholar
Roseboom, TJ, Painter, RC, van Abeelen, AF, Veenendaal, MV, de Rooij, SR. Hungry in the womb: what are the consequences? Lessons from the Dutch famine. Maturitas. 2011;70(2):141–5.Google Scholar
Painter, RC, Westendorp, RG, de Rooij, SR, Osmond, C, Barker, DJ, Roseboom, TJ. Increased reproductive success of women after prenatal undernutrition. Hum Reprod. 2008;23(11):2591–5.Google Scholar
Yarde, F, Broekmans, FJ, van der Pal-de Bruin, KM, Schonbeck, Y, te Velde, ER, Stein, AD, et al. Prenatal famine, birthweight, reproductive performance and age at menopause: the Dutch hunger winter families study. Hum Reprod. 2013;28(12):3328–36.Google Scholar
Lumey, LH, Stein, AD. In utero exposure to famine and subsequent fertility: the Dutch famine birth cohort study. Am J Public Health. 1997;87(12):1962–6.Google Scholar
Song, S. Assessing the impact of in utero exposure to famine on fecundity: evidence from the 1959–6. famine in China. Popul Stud (Camb). 2013;67(3):293–308.Google Scholar
Sloboda, DM, Howie, GJ, Pleasants, A, Gluckman, PD, Vickers, MH. Pre- and postnatal nutritional histories influence reproductive maturation and ovarian function in the rat. PLoS One. 2009;4(8):e6744.Google Scholar
Chan, KA, Bernal, AB, Vickers, MH, Gohir, W, Petrik, JJ, Sloboda, DM. Early life exposure to undernutrition induces ER stress, apoptosis, and reduced vascularization in ovaries of adult rat offspring. Biol Reprod. 2015;92(4):110.Google Scholar
Matsuzaki, T, Munkhzaya, M, Iwasa, T, Tungalagsuvd, A, Yano, K, Mayila, Y, et al. Prenatal undernutrition suppresses sexual behaviour in female rats. Gen Com Endocrinol. 2018;269:46–52.Google Scholar
Aiken, CE, Tarry-Adkins, JL, Ozanne, SE. Decreased ovarian reserve, dysregulation of mitochondrial biogenesis, and increased lipid peroxidation in female mouse offspring exposed to an obesogenic maternal diet. The FASEB Journal. 2013;27(10):3959–65.Google Scholar
Boynton-Jarrett, R, Rich-Edwards, J, Fredman, L, Hibert, EL, Michels, KB, Forman, MR, et al. Gestational weight gain and daughter’s age at Menarche. J Womens Health (Larchmt). 2011;20(8):1193–200.Google Scholar
Lawn, RB, Lawlor, DA, Fraser, A. Associations between maternal prepregnancy body mass index and gestational weight gain and daughter’s age at menarche: the Avon longitudinal study of parents and children. Am J Epidemiol. 2018;187(4):677–86.Google Scholar
Sloboda, DM, Hickey, M, Hart, R. Reproduction in females: the role of the early life environment. Hum Reprod Update. 2011;17(2):210–27.Google Scholar
Brix, N, Ernst, A, Lauridsen, LLB, Arah, OA, Nohr, EA, Olsen, J, et al. Maternal pre-pregnancy obesity and timing of puberty in sons and daughters: a population-based cohort study. Int J Epidemiol. 2019;48(5):1684–94.Google Scholar
Mariansdatter, SE, Ernst, A, Toft, G, Olsen, SF, Vested, A, Kristensen, SL, et al. Maternal pre-pregnancy BMI and reproductive health of daughters in young adulthood. Matern Child Health J. 2016;20(10):2150–9.Google Scholar
Kubo, A, Deardorff, J, Laurent, CA, Ferrara, A, Greenspan, LC, Quesenberry, CP, et al. Associations between maternal obesity and pregnancy hyperglycemia and timing of puberty onset in adolescent girls: a population-based study. Am J Epidemiol. 2018;187(7):1362–9.Google Scholar
Huang, Y, Hu, C, Ye, H, Luo, R, Fu, X, Li, X, et al. Imflamm-aging: a new mechanism affecting premature ovarian insufficiency. J Immunol Res. 2019;2019:8069898. doi: 10.1155/2019/8069898.Google Scholar
Franceschi, C, Garagnani, P, Parini, P, Giuliani, C, Santoro, A. Inflammaging: a new immune-metabolic viewpoint for age-related diseases. Nat Rev Endocrinol. 2018;14(10):576–90.Google Scholar
Hilakivi-Clarke, L, Clarke, R, Onojafe, I, Raygada, M, Cho, E, Lippman, M. A maternal diet high in n-6 polyunsaturated fats alters mammary gland development, puberty onset, and breast cancer risk among female rat offspring. Proc Natl Acad Sci USA. 1997;94(17):9372–7.Google Scholar
Connor, KL, Vickers, MH, Beltrand, J, Meaney, MJ, Sloboda, DM. Nature, nurture or nutrition? Impact of maternal nutrition on maternal care, offspring development and reproductive function. J Physiol. 2012;590(9):2167–80.Google Scholar
Hilakivi-Clarke, L, Stoica, A, Raygada, M, Martin, M. Consumption of a high-fat diet alters estrogen receptor content, protein kinase C activity, and mammary gland morphology in virgin and pregnant mice and female offspring. Cancer Res. 1998;58(4):654–60.Google Scholar
Yun, Y, Wei, Z, Hunter, N. Maternal obesity enhances oocyte chromosome abnormalities associated with aging. Chromosoma. 2019;128(3):413–21.Google Scholar
Jungheim, ES, Macones, GA, Odem, RR, Patterson, BW, Lanzendorf, SE, Ratts, VS, et al. Associations between free fatty acids, cumulus oocyte complex morphology and ovarian function during in vitro fertilization. Fertil Steril. 2011;95(6):1970–4.Google Scholar
Igosheva, N, Abramov, AY, Poston, L, Eckert, JJ, Fleming, TP, Duchen, MR, et al. Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes. PLOS ONE. 2010;5(4):e10074.Google Scholar
Wu, LL, Russell, DL, Wong, SL, Chen, M, Tsai, T-S, St John, JC, et al. Mitochondrial dysfunction in oocytes of obese mothers: transmission to offspring and reversal by pharmacological endoplasmic reticulum stress inhibitors. Development. 2015;142(4):681–91.Google Scholar
Boudoures, AL, Saben, J, Drury, A, Scheaffer, S, Modi, Z, Zhang, W, et al. Obesity-exposed oocytes accumulate and transmit damaged mitochondria due to an inability to activate mitophagy. Dev Biol. 2017;426(1):126–38.Google Scholar
Saben, JL, Boudoures, AL, Asghar, Z, Thompson, A, Drury, A, Zhang, W, et al. Maternal metabolic syndrome programs mitochondrial dysfunction via germline changes across three generations. Cell Reports. 2016;16(1):1–8.Google Scholar
Risal, S, Pei, Y, Lu, H, Manti, M, Fornes, R, Pui, H-P, et al. Prenatal androgen exposure and transgenerational susceptibility to polycystic ovary syndrome. Nat Med. 2019;25(12):1894–904.Google Scholar
Bailey, JL, Dalvai, M, Lessard, M, Herst, PM, Charest, PL, Navarro, P. Beyond fertilisation: how the paternal environment influences future generations. Anim Reprod Sci. 2020:106503.Google Scholar
Bodden, C, Hannan, AJ, Reichelt, AC. Diet-induced modification of the sperm epigenome programs metabolism and behavior. Trends Endocrinol Metab. 2020;31(2):131–49.Google Scholar
Champagne, FA. Interplay between paternal germline and maternal effects in shaping development: the overlooked importance of behavioural ecology. Functional Ecology. 2020;34(2):401–13.Google Scholar
Owens, JA, Mitchell, M, Palmer, NO, Fullston, T, Bakos, HW, Lane, M. Diet-induced paternal obesity in the absence of diabetes diminishes the reproductive health of two subsequent generations of mice. Hum Reprod. 2012;27(5):1391–400.Google Scholar
Binder, NK, Mitchell, M, Gardner, DK. Paternal diet-induced obesity retards early mouse embryo development, mitochondrial activity and pregnancy health. Reprod Fertl Dev. 2012;24(6):804–12.Google Scholar
Fullston, T, Shehadeh, H, Sandeman, LY, Kang, WX, Wu, LL, Robker, RL, et al. Female offspring sired by diet induced obese male mice display impaired blastocyst development with molecular alterations to their ovaries, oocytes and cumulus cells. J Assist Reprod Genet. 2015;32(5):725–35.Google Scholar
Stearns, SC. Life history evolution: successes, limitations, and prospects. Naturwissenschaften. 2000;87(11):476–86.Google Scholar
Chisholm, JS, Ellison, PT, Evans, J, Lee, PC, Lieberman, LS, Pavlik, Z, et al. Death, hope, and sex: life-history theory and the development of reproductive strategies. Curr Anthropol. 1993;34(1):1–24.Google Scholar
Evans, J, Wilson, A, Pilastro, A, Garcia-Gonzalez, F. Ejaculate-mediated paternal effects: evidence, mechanisms and evolutionary implications. Reproduction. 2019. Apr 1;157(4):R109-R126. doi: 10.1530/REP-18-0524.Google Scholar
Nathanielsz, P. W., Life Before Birth: The Challenges of Fetal Development, 2nd ed (San Antonio, TX: Life Course Health Press, LLC, 2021).Google Scholar
Puppala, S., Li, C., Glenn, J. P., Saxena, R., Gawrieh, S., Quinn, A., Palarczyk, J., Dick, E. J., Nathanielsz, P. W., & Cox, L. A., Primate fetal hepatic responses to maternal obesity: epigenetic signalling pathways and lipid accumulation. The Journal of Physiology, 596 (2018) 5823–5837. https://doi.org/10.1113/JP275422.Google Scholar
Chahal, H. S. & Drake, W. M., The endocrine system and ageing. Journal of Pathology, 211 (2007) 173–180. https://doi.org/10.1002/path.2110.Google Scholar
Rodríguez-González, G. L., Reyes-Castro, L. A., Vega, C. C., Boeck, L., Ibáñez, C., Nathanielsz, P. W., Larrea, F., & Zambrano, E., Accelerated aging of reproductive capacity in male rat offspring of protein-restricted mothers is associated with increased testicular and sperm oxidative stress. Age (Dordr), 36 (2014) 9721. https://doi.org/10.1007/s11357-014-9721-5.Google Scholar
Tarry-Adkins, J. L., Fernandez-Twinn, D. S., Chen, J. H., Hargreaves, I. P., Neergheen, V., Aiken, C. E., & Ozanne, S. E., Poor maternal nutrition and accelerated postnatal growth induces an accelerated aging phenotype and oxidative stress in skeletal muscle of male rats. DMM Disease Models and Mechanisms, 9 (2016) 1221–1229. https://doi.org/10.1242/dmm.026591.Google Scholar
Barker, D. J. P., Eriksson, J. G., Forsen, T., & Osmond, C., Fetal origins of adult disease: strength of effects and biological basis. International Journal of Epidemiology, 31 (2002) 1235–1239.Google Scholar
Barker, D. J. P., Mothers, Babies and Diseases in Later Life, 2nd ed (LP London, England: Churchill Livingstone, 1998).Google Scholar
Backhouse, E. V, Shenkin, S. D., McIntosh, A. M., Bastin, M. E., Whalley, H. C., Valdez Hernandez, M., Muñoz Maniega, S., Harris, M. A., Stolicyn, A., Campbell, A., Steele, D., Waiter, G. D., Sandu, A.-L., Waymont, J. M. J., Murray, A. D., Cox, S. R., de Rooij, S. R., Roseboom, T. J., & Wardlaw, J. M., Early life predictors of late life cerebral small vessel disease in four prospective cohort studies. Brain: A Journal of Neurology, (2021) Dec 31;144(12):3769–78. https://doi.org/10.1093/BRAIN/AWAB331.Google Scholar
Rabadán-Diehl, C. & Nathanielsz, P., From mice to men: research models of developmental programming. J Dev Orig Health Dis. 2013;4(1):3–9. https://doi.org/10.1017/S2040174412000487.Google Scholar
Zambrano, E., Reyes-Castro, L. A., & Nathanielsz, P. W., Aging, glucocorticoids and developmental programming. Age (Dordr). 2015;37(3):9774. https://doi.org/10.1007/s11357-015-9774-0.Google Scholar
Rodríguez-González, G. L., Vega, C. C., Boeck, L., Vázquez, M., Bautista, C. J., Reyes-Castro, L. A., Saldaña, O., Lovera, D., Nathanielsz, P. W., & Zambrano, E., Maternal obesity and overnutrition increase oxidative stress in male rat offspring reproductive system and decrease fertility. International Journal of Obesity (Lond), 39 (2014) 549–556. https://doi.org/10.1038/ijo.2014.209.Google Scholar
Zambrano, E., Rodríguez-González, G. L., Guzmán, C., García-Becerra, R., Boeck, L., Díaz, L., Menjivar, M., Larrea, F., & Nathanielsz, P. W., A maternal low protein diet during pregnancy and lactation in the rat impairs male reproductive development. The Journal of Physiology, 563 (2005) 275–284. https://doi.org/10.1113/jphysiol.2004.078543.Google Scholar
Rodríguez-González, G. L., Reyes-Castro, L. A., Bautista, C. J., Beltrán, A. A., Ibáñez, C. A., Vega, C. C., Lomas-Soria, C., Castro-Rodr, D. C.íguez, A. L. Elías-López, P. W. Nathanielsz, , & Zambrano, E., Maternal obesity accelerates rat offspring metabolic ageing in a sex-dependent manner. Journal of Physiology, 597 (2019) 5549–5563. https://doi.org/10.1113/JP278232.Google Scholar
Vega, C. C., Reyes-Castro, L. A., Bautista, C. J., Larrea, F., Nathanielsz, P. W., & Zambrano, E., Exercise in obese female rats has beneficial effects on maternal and male and female offspring metabolism. International Journal of Obesity (2005), 39 (2015) 712–9. https://doi.org/10.1038/ijo.2013.150.Google Scholar
Ibáñez, C. A., Vázquez-Martínez, M., León-Contreras, J. C., Reyes-Castro, L. A., Rodríguez-González, G. L., Bautista, C. J., Nathanielsz, P. W., & Zambrano, E., Different statistical approaches to characterization of adipocyte size in offspring of obese rats: effects of maternal or offspring exercise intervention. Frontiers in Physiology, 9:1571 (2018). https://doi.org/10.3389/FPHYS.2018.01571.Google Scholar
Santos, M., Rodríguez-González, G. L., Ibáñez, C., Vega, C. C., Nathanielsz, P. W., & Zambrano, E., Adult exercise effects on oxidative stress and reproductive programming in male offspring of obese rats. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 308 (2015) R219R225. https://doi.org/10.1152/ajpregu.00398.2014.Google Scholar
Zambrano, E., Martínez-Samayoa, P. M., Rodríguez-González, G. L., & Nathanielsz, P. W., Dietary intervention prior to pregnancy reverses metabolic programming in male offspring of obese rats. The Journal of Physiology, 588 (2010) 1791–1799. https://doi.org/10.1113/jphysiol.2010.190033.Google Scholar
Rodríguez-González, G. L., Reyes-Castro, L. A., Vega, C. C., Boeck, L., Ibáñez, C., Nathanielsz, P. W., Larrea, F., & Zambrano, E., Accelerated aging of reproductive capacity in male rat offspring of protein-restricted mothers is associated with increased testicular and sperm oxidative stress. Age (Dordrecht, Netherlands), 36 (2014). Age (Dordr) 2014;36(6):9721. https://doi.org/10.1007/S11357-014-9721-5.Google Scholar
Zambrano, E., Martínez-Samayoa, P. M., Rodríguez-González, G. L., & Nathanielsz, P. W., Dietary intervention prior to pregnancy reverses metabolic programming in male offspring of obese rats. The Journal of Physiology, 588 (2010) 1791–1799. https://doi.org/10.1113/jphysiol.2010.190033.Google Scholar
Vega, C. C., Reyes-Castro, L. A., Bautista, C. J., Larrea, F., Nathanielsz, P. W., & Zambrano, E., Exercise in obese female rats has beneficial effects on maternal and male and female offspring metabolism. International Journal of Obesity, 39 (2015) 712–719. https://doi.org/10.1038/ijo.2013.150.Google Scholar
Santos, M., Rodríguez-González, G. L., Ibáñez, C., Vega, C. C., Nathanielsz, P. W., & Zambrano, E., Adult exercise effects on oxidative stress and reproductive programming in male offspring of obese rats. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 308 (2015) R219R225. https://doi.org/10.1152/ajpregu.00398.2014.Google Scholar
López-Otín, C., Blasco, M. A., Partridge, L., Serrano, M., & Kroemer, G., The hallmarks of aging. Cell, 153 (2013) 1194–1217. https://doi.org/10.1016/j.cell.2013.05.039.Google Scholar
Cheng, C. J., Gelfond, J. A. L., Strong, R., & Nelson, J. F., Genetically heterogeneous mice exhibit a female survival advantage that is age‐ and site‐specific: results from a large multi‐site study. Aging Cell, 18 (2019) e12905. https://doi.org/10.1111/acel.12905.Google Scholar
Fowden, A. L., Li, J., & Forhead, A. J., Glucocorticoids and the preparation for life after birth: are there long-term consequences of the life insurance? Proceedings of the Nutrition Society, 57 (1998) 113–122. https://doi.org/10.1079/pns19980017.Google Scholar
Malinowska, K. W., Hardy, R. N., & Nathanielsz, P. W., Plasma adrenocorticosteroid concentrations immediately after birth in the rat, rabbit and guinea-pig. Experientia, 28 (1972) 1366–1367.Google Scholar
Thomas, A. L., Krane, E. J., & Nathanielsz, P. W., Changes in the fetal thyroid axis after induction of premature parturition by low dose continuous intravascular cortisol infusion to the fetal sheep at 130 days of gestation. Endocrinology, 103 (1978) 17–23.Google Scholar
McMullen, S., Langley-Evans, S. C., Gambling, L., Lang, C., Swali, A., & McArdle, H. J., A common cause for a common phenotype: the gatekeeper hypothesis in fetal programming. Medical Hypotheses, 78 (2012) 88–94. https://doi.org/10.1016/j.mehy.2011.09.047.Google Scholar
Bowman, R. E., Maclusky, N. J., Diaz, S. E., Zrull, M. C., & Luine, V. N., Aged rats: sex differences and responses to chronic stress. Brain Research, 1126 (2006) 156–166. https://doi.org/10.1016/j.brainres.2006.07.047.Google Scholar
Ferrari, E., Cravello, L., Muzzoni, B., Casarotti, D., Paltro, M., Solerte, S. B., Fioravanti, M., Cuzzoni, G., Pontiggia, B., & Magri, F., Age-related changes of the hypothalamic-pituitary-adrenal axis: pathophysiological correlates. European Journal of Endocrinology, 144 (2001) 319–329.Google Scholar
Peeters, G. M. E. E., van Schoor, N. M., Visser, M., Knol, D. L., Eekhoff, E. M. W., de Ronde, W., & Lips, P., Relationship between cortisol and physical performance in older persons. Clinical Endocrinology (Oxf), 67 (2007) 398–406. https://doi.org/10.1111/j.1365-2265.2007.02900.x.Google Scholar
Zhao, Z.-Y. Y., Lu, F.-H. H., Xie, Y., Fu, Y.-R. R., Bogdan, A., & Touitou, Y., Cortisol secretion in the elderly. Influence of age, sex and cardiovascular disease in a Chinese population. Steroids, 68 (2003) 551–555.Google Scholar
McEwen, B. S., Protective and damaging effects of stress mediators. The New England Journal of Medicine, 338 (1998) 171–179. https://doi.org/10.1056/NEJM199801153380307.Google Scholar
Yeager, M. P., Pioli, P. A., & Guyre, P. M., Cortisol exerts bi-phasic regulation of inflammation in humans. Dose Response, 9 (2011) 332–347. https://doi.org/10.2203/dose-response.10-013.Yeager.Google Scholar
Tenk, J., Mátrai, P., Hegyi, P., Rostás, I., Garami, A., Szabó, I., Solymár, M., Pétervári, E., Czimmer, J., Márta, K., Mikó, A., Füredi, N., Párniczky, A., Zsiborás, C., & Balaskó, M., In obesity, HPA axis activity does not increase with BMI, but declines with aging: a meta-analysis of clinical studies. PLoS One, 11 (2016) e0166842. https://doi.org/10.1371/journal.pone.0166842.Google Scholar
Yang, S., Gerow, K. G., Huber, H. F., Considine, M. M., Li, C., Mattern, V., Comuzzie, A. G., Ford, S. P., & Nathanielsz, P. W., A decline in female baboon hypothalamo-pituitary-adrenal axis activity anticipates aging. Aging, 9 (2017) 1375–1385. https://doi.org/10.18632/aging.101235.Google Scholar
Willis, E. L., Eberle, R., Wolf, R. F., White, G. L., & McFarlane, D., The effects of age and cytomegalovirus on markers of inflammation and lymphocyte populations in captive baboons. PLoS ONE, 9 (2014). https://doi.org/10.1371/journal.pone.0107167.Google Scholar
Jang, Y. C., Liu, Y., Hayworth, C. R., Bhattacharya, A., Lustgarten, M. S., Muller, F. L., Chaudhuri, A., Qi, W., Li, Y., Huang, J.-Y., Verdin, E., Richardson, A., Van Remmen, H., The, S., & Barshop, A., Dietary restriction attenuates age-associated muscle atrophy by lowering oxidative stress in mice even in complete absence of CuZnSOD. Aging Cell, 11 (2012) 770–782. https://doi.org/10.1111/j.1474-9726.2012.00843.x.Google Scholar
Pacher, P., Obrosova, I., Mabley, J., & Szabo, C., Role of nitrosative stress and peroxynitrite in the pathogenesis of diabetic complications. Emerging new therapeutical strategies. Current Medicinal Chemistry, 12 (2012) 267–275. https://doi.org/10.2174/0929867053363207.Google Scholar
Morimoto, S., Sosa, T. C., Calzada, L., Reyes-Castro, L. A., Díaz-Díaz, E., Morales, A., Nathanielsz, P. W., & Zambrano, E., Developmental programming of aging of isolated pancreatic islet glucose-stimulated insulin secretion in female offspring of mothers fed low-protein diets in pregnancy and/or lactation. Journal of Developmental Origins of Health and Disease, 3 (2012) 483–8. https://doi.org/10.1017/S2040174412000463.Google Scholar
Morimoto, S., Calzada, L., Sosa, T. C., Reyes-Castro, L. A., Rodriguez-Gonz, G. L.ález, A. Morales, P. W. Nathanielsz, , & Zambrano, E., Emergence of ageing-related changes in insulin secretion by pancreatic islets of male rat offspring of mothers fed a low-protein diet. The British Journal of Nutrition, 107(11) (2012) 1562–5. https://doi.org/10.1017/S0007114511004855.Google Scholar
Rodríguez-González, G. L., Vega, C. C., Boeck, L., Vázquez, M., Bautista, C. J., Reyes-Castro, L. A., Saldaña, O., Lovera, D., Nathanielsz, P. W., & Zambrano, E., Maternal obesity and overnutrition increase oxidative stress in male rat offspring reproductive system and decrease fertility. International Journal of Obesity, 39 (2015) 549–556. https://doi.org/10.1038/ijo.2014.209.Google Scholar
Beeson, J. H., Blackmore, H. L., Carr, S. K., Dearden, L., Duque-Guimar, D. E.ães, L. C. Kusinski, L. C. Pantaleão, A. G. Pinnock, C. E. Aiken, D. A. Giussani, D. S. Fernandez-Twinn, , & Ozanne, S. E., Maternal exercise intervention in obese pregnancy improves the cardiovascular health of the adult male offspring. Molecular Metabolism, 16 (2018) 35–44. https://doi.org/10.1016/j.molmet.2018.06.009.Google Scholar
Santos, M., Rodríguez-González, G. L., Ibáñez, C., Vega, C. C., Nathanielsz, P. W., & Zambrano, E., Adult exercise effects on oxidative stress and reproductive programming in male offspring of obese rats. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 308 (2015) 219–225. https://doi.org/10.1152/ajpregu.00398.2014.-Exercise.Google Scholar
Horvath, S., Haghani, A., Zoller, J. A., Lu, A. T., Ernst, J., Pellegrini, M., Jasinska, A. J., Mattison, J. A., Salmon, A. B., Raj, K., Horvath, M., Paul, K. C., Ritz, B. R., Robeck, T. R., Spriggs, M., Ehmke, E. E., Jenkins, S., Li, C., & Nathanielsz, P. W., Pan-primate DNA methylation clocks. bioRxiv, (2021). https://doi.org/10.1101/2020.11.29.402891.Google Scholar
Bronikowski, A. M., Alberts, S. C., Altmann, J., Packer, C., Dee Carey, K., & Tatar, M., The aging baboon: comparative demography in a non-human primate. Proceedings of the National Academy of Sciences of the United States of America, 99 (2002) 9591–9595. https://doi.org/10.1073/pnas.142675599.Google Scholar
Allison, B. J., Kaandorp, J. J., Kane, A. D., Camm, E. J., Lusby, C., Cross, C. M., Nevin‐Dolan, R., Thakor, A. S., Derks, J. B., Tarry‐Adkins, J. L., Ozanne, S. E., & Giussani, D. A., Divergence of mechanistic pathways mediating cardiovascular aging and developmental programming of cardiovascular disease. The FASEB Journal, 30 (2016) 1968–1975. https://doi.org/10.1096/fj.201500057.Google Scholar
Reyes-Castro, L. A., Padilla-Gómez, E., Parga-Martínez, N. J., Castro-Rodr, D. C.íguez, G. L. Quirarte, S. Díaz-Cintra, P. W. Nathanielsz, , & Zambrano, E., Hippocampal mechanisms in impaired spatial learning and memory in male offspring of rats fed a low-protein isocaloric diet in pregnancy and/or lactation. Hippocampus, 28 (2018) 18–30. https://doi.org/10.1002/hipo.22798.Google Scholar
Rodriguez, J. S. S., Rodríguez-González, G. L. L., Reyes-Castro, L. A. A., Ibáñez, C., Ramírez, A., Chavira, R., Larrea, F., Nathanielsz, P. W. W., & Zambrano, E., Maternal obesity in the rat programs male offspring exploratory, learning and motivation behavior: prevention by dietary intervention pre-gestation or in gestation. International Journal of Developmental Neuroscience: The Official Journal of the International Society for Developmental Neuroscience, 30 (2012) 75–81. https://doi.org/10.1016/j.ijdevneu.2011.12.012.Google Scholar

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