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Mechanisms linking exposure to preeclampsia in utero and the risk for cardiovascular disease

Part of: DOHaD ANZ Conference 2018: Genes, Environment and Evolution

Published online by Cambridge University Press:  19 February 2020

Prabha H. Andraweera Open the ORCID record for Prabha H. Andraweera [Opens in a new window] ,
Kathryn L. Gatford Open the ORCID record for Kathryn L. Gatford [Opens in a new window] ,
Alison S. Care ,
Tina Bianco-Miotto ,
Zohra S. Lassi ,
Gus A. Dekker ,
Margaret Arstall  and
Claire T. Roberts
Prabha H. Andraweera*
Affiliation:
Adelaide Medical School, The University of Adelaide, Adelaide, Australia Robinson Research Institute, The University of Adelaide, Adelaide, Australia
Kathryn L. Gatford
Affiliation:
Adelaide Medical School, The University of Adelaide, Adelaide, Australia Robinson Research Institute, The University of Adelaide, Adelaide, Australia
Alison S. Care
Affiliation:
Adelaide Medical School, The University of Adelaide, Adelaide, Australia Robinson Research Institute, The University of Adelaide, Adelaide, Australia
Tina Bianco-Miotto
Affiliation:
Robinson Research Institute, The University of Adelaide, Adelaide, Australia School of Agriculture, Food and Wine, The University of Adelaide, Adelaide, Australia
Zohra S. Lassi
Affiliation:
Adelaide Medical School, The University of Adelaide, Adelaide, Australia Robinson Research Institute, The University of Adelaide, Adelaide, Australia
Gus A. Dekker
Affiliation:
Adelaide Medical School, The University of Adelaide, Adelaide, Australia Robinson Research Institute, The University of Adelaide, Adelaide, Australia Division of Women’s Health, Lyell McEwin Hospital, Elizabeth Vale, Australia
Margaret Arstall
Affiliation:
Adelaide Medical School, The University of Adelaide, Adelaide, Australia Department of Cardiology, Lyell McEwin Hospital, Elizabeth Vale, Australia
Claire T. Roberts
Affiliation:
Adelaide Medical School, The University of Adelaide, Adelaide, Australia Robinson Research Institute, The University of Adelaide, Adelaide, Australia
*
Address for correspondence: Prabha Andraweera, Adelaide Medical School, The Robinson Research Institute, The University of Adelaide, Adelaide, Australia. Email: prabha.andraweera@adelaide.edu.au
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Abstract

Preeclampsia (PE) is now recognised as a cardiovascular risk factor for women. Emerging evidence suggests that children exposed to PE in utero may also be at increased risk of cardiovascular disease (CVD) in later life. Individuals exposed to PE in utero have higher systolic and diastolic blood pressure and higher body mass index (BMI) compared to those not exposed to PE in utero. The aim of this review is to discuss the potential mechanisms driving the relationship between PE and offspring CVD. Exposure to an adverse intrauterine environment as a consequence of the pathophysiological changes that occur during a pregnancy complicated by PE is proposed as one mechanism that programs the fetus for future CVD risk. Consistent with this hypothesis, animal models of PE where progeny have been studied demonstrate causality for programming of offspring cardiovascular health by the preeclamptic environment. Shared alleles between mother and offspring, and shared lifestyle factors between mother and offspring provide alternate pathways explaining associations between PE and offspring CVD risk. In addition, adverse lifestyle habits can also act as second hits for those programmed for increased CVD risk. PE and CVD are both multifactorial diseases and, hence, identifying the relative contribution of PE to offspring risk for CVD is a very complex task. However, considering the emerging strong association between PE and CVD, those exposed to PE in utero may benefit from targeted primary CVD preventive strategies.

Keywords

Preeclampsiacardiovascular diseaseoffspringprogeny
Type
Review
Information
Journal of Developmental Origins of Health and Disease , Volume 11 , Issue 3 , June 2020 , pp. 235 - 242
Copyright
© The Author(s) 2020. Published by Cambridge University Press and the International Society for Developmental Origins of Health and Disease

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References

Duley, L.The global impact of pre-eclampsia and eclampsia. Semin. Perinatol. 2009; 33, 130–137.CrossRefGoogle ScholarPubMed
Tranquilli, AL, Dekker, G, Magee, L, et al.The classification, diagnosis and management of the hypertensive disorders of pregnancy: a revised statement from the ISSHP. Pregnancy Hypertens. 2014; 4, 97–104.Google ScholarPubMed
Bellamy, L, Casas, JP, Hingorani, AD, Williams, DJ.Pre-eclampsia and risk of cardiovascular disease and cancer in later life: systematic review and meta-analysis. BMJ (Clinical Research Edition) 2007; 335, 974.CrossRefGoogle ScholarPubMed
Brown, MC, Best, KE, Pearce, MS, Waugh, J, Robson, SC, Bell, R.Cardiovascular disease risk in women with pre-eclampsia: systematic review and meta-analysis. Eur J Epidemiol. 2013; 28, 1–19.CrossRefGoogle ScholarPubMed
Heida, KY, Bots, ML, de Groot, CJ, et al.Cardiovascular risk management after reproductive and pregnancy-related disorders: a Dutch multidisciplinary evidence-based guideline. Eur J Prevent Cardiol. 2016; 23, 1863–1879.CrossRefGoogle ScholarPubMed
Tranquilli, AL, Brown, MA, Zeeman, GG, Dekker, G, Sibai, BM.The definition of severe and early-onset preeclampsia. Statements from the International Society for the Study of Hypertension in Pregnancy (ISSHP). Pregnancy Hypertens. 2013; 3, 44–47.CrossRefGoogle Scholar
Mosca, L, Benjamin, EJ, Berra, K, et al.Effectiveness-based guidelines for the prevention of cardiovascular disease in women–2011 update: a guideline from the american heart association. Circulation. 2011; 123, 1243–1262.CrossRefGoogle Scholar
Nahum Sacks, K, Friger, M, Shoham-Vardi, I, et al.Prenatal exposure to preeclampsia as an independent risk factor for long-term cardiovascular morbidity of the offspring. Pregnancy Hypertens. 2018; 13, 181–186.CrossRefGoogle ScholarPubMed
Andraweera, PH, Lassi, ZS.Cardiovascular risk factors in offspring of preeclamptic pregnancies-systematic review and meta-analysis. J Pediatr. 2019; 208, 104–113.e6.CrossRefGoogle ScholarPubMed
Anderson, CM, Lopez, F, Zimmer, A, Benoit, JN.Placental insufficiency leads to developmental hypertension and mesenteric artery dysfunction in two generations of Sprague-Dawley rat offspring. Biol Reprod. 2006; 74, 538–544.Google ScholarPubMed
Davis, EF, Newton, L, Lewandowski, AJ, et al.Pre-eclampsia and offspring cardiovascular health: mechanistic insights from experimental studies. Clin Sci. (London, England : 1979) 2012; 123, 53–72.CrossRefGoogle ScholarPubMed
Kvehaugen, AS, Dechend, R, Ramstad, HB, Troisi, R, Fugelseth, D, Staff, AC.Endothelial function and circulating biomarkers are disturbed in women and children after preeclampsia. Hypertension. 2011; 58, 63–69.CrossRefGoogle ScholarPubMed
Jayet, PY, Rimoldi, SF, Stuber, T, et al.Pulmonary and systemic vascular dysfunction in young offspring of mothers with preeclampsia. Circulation. 2010; 122, 488–494.CrossRefGoogle ScholarPubMed
Touwslager, RN, Houben, AJ, Gielen, M, et al.Endothelial vasodilatation in newborns is related to body size and maternal hypertension. J Hypertens. 2012; 30, 124–131.CrossRefGoogle ScholarPubMed
Lazdam, M, de la Horra, A, Pitcher, A, et al.Elevated blood pressure in offspring born premature to hypertensive pregnancy: is endothelial dysfunction the underlying vascular mechanism? Hypertension. 2010; 56, 159–165.CrossRefGoogle ScholarPubMed
Akcakus, M, Altunay, L, Yikilmaz, A, Yazici, C, Koklu, E.The relationship between abdominal aortic intima-media thickness and lipid profile in neonates born to mothers with preeclampsia. J Pediatr Endocrinol Metabol (JPEM). 2010; 23, 1143–1149.Google ScholarPubMed
McAloon, CJ, Boylan, LM, Hamborg, T, et al.The changing face of cardiovascular disease 2000–2012: An analysis of the world health organisation global health estimates data. Int J Cardiol. 2016; 224, 256–264.CrossRefGoogle ScholarPubMed
Barker, DJ.Fetal growth and adult disease. Br J Obstet Gynaecol. 1992; 99, 275–276.CrossRefGoogle ScholarPubMed
Barker, DJ.The effect of nutrition of the fetus and neonate on cardiovascular disease in adult life. Proc Nutr Soc. 1992; 51, 135–144.CrossRefGoogle ScholarPubMed
Barker, DJ.The developmental origins of chronic adult disease. Acta Paediatr Suppl. 2004; 93, 26–33.CrossRefGoogle ScholarPubMed
Murphy, MO, Cohn, DM, Loria, AS.Developmental origins of cardiovascular disease: impact of early life stress in humans and rodents. Neurosci Biobehav Rev. 2017; 74, 453–465.CrossRefGoogle ScholarPubMed
Andraweera, PH, Dekker, GA, Roberts, CT.The vascular endothelial growth factor family in adverse pregnancy outcomes. Human Reprod Update. 2012; 18, 436–457.CrossRefGoogle ScholarPubMed
Stojanovska, V, Scherjon, SA, Plosch, T.Preeclampsia as modulator of offspring health. Biol Reprod. 2016; 94, 53.Google ScholarPubMed
Staff, AC.The two-stage placental model of preeclampsia: an update. J Reprod Immunol. 2019; 134–135, 1–10.CrossRefGoogle ScholarPubMed
Redman, CWG, Sargent, IL.Placental stress and pre-eclampsia: a revised view. Placenta. 2009; 30, 38–42.CrossRefGoogle ScholarPubMed
Brennan, LJ, Morton, JS, Davidge, ST.Vascular dysfunction in preeclampsia. Microcirculation. 2014; 21, 4–14.CrossRefGoogle ScholarPubMed
Roberts, JM, Taylor, RN, Goldfien, A.Clinical and biochemical evidence of endothelial cell dysfunction in the pregnancy syndrome preeclampsia. Am J Hypertens. 1991; 4, 700–708.CrossRefGoogle ScholarPubMed
Myers, J, Mires, G, Macleod, M, Baker, P.In preeclampsia, the circulating factors capable of altering in vitro endothelial function precede clinical disease. Hypertension. 2005; 45, 258–263.CrossRefGoogle ScholarPubMed
Kao, CK, Morton, JS, Quon, AL, Reyes, LM, Lopez-Jaramillo, P, Davidge, ST.Mechanism of vascular dysfunction due to circulating factors in women with pre-eclampsia. Clin Sci (Lond). 2016; 130, 539–549.CrossRefGoogle ScholarPubMed
Lu, F, Bytautiene, E, Tamayo, E, et al.Gender-specific effect of overexpression of sFlt-1 in pregnant mice on fetal programming of blood pressure in the offspring later in life. Am J Obstetr Gynecol. 2007; 197, 418.e1–418.e5.CrossRefGoogle ScholarPubMed
Aouache, R, Biquard, L, Vaiman, D, Miralles, F.Oxidative stress in preeclampsia and placental diseases. Int J Mol Sci. 2018; 19, pii: E1496.CrossRefGoogle ScholarPubMed
Myatt, L, Rosenfield, RB, Eis, AL, Brockman, DE, Greer, I, Lyall, F.Nitrotyrosine residues in placenta. Evidence of peroxynitrite formation and action. Hypertension. 1996; 28, 488–493.CrossRefGoogle ScholarPubMed
Fujimaki, A, Watanabe, K, Mori, T, Kimura, C, Shinohara, K, Wakatsuki, A.Placental oxidative DNA damage and its repair in preeclamptic women with fetal growth restriction. Placenta. 2011; 32, 367–372.Google ScholarPubMed
Hilali, N, Kocyigit, A, Demir, M, et al.DNA damage and oxidative stress in patients with mild preeclampsia and offspring. Eur J Obstet Gynecol Reprod Biol. 2013; 170, 377–380.CrossRefGoogle ScholarPubMed
Wang, Z, Huang, Z, Lu, G, Lin, L, Ferrari, M.Hypoxia during pregnancy in rats leads to early morphological changes of atherosclerosis in adult offspring. Am J Physiol Heart Circ Physiol. 2009; 296, H1321–H1328.CrossRefGoogle ScholarPubMed
Giussani, DA, Camm, EJ, Niu, Y, et al.Developmental programming of cardiovascular dysfunction by prenatal hypoxia and oxidative stress. PloS One. 2012; 7, e31017.CrossRefGoogle ScholarPubMed
Zhang, P, Zhu, D, Chen, X, et al.Prenatal hypoxia promotes atherosclerosis via vascular inflammation in the offspring rats. Atherosclerosis. 2016; 245, 28–34.CrossRefGoogle ScholarPubMed
Santner-Nanan, B, Straubinger, K, Hsu, P, et al.Fetal–maternal alignment of regulatory T cells correlates with IL-10 and Bcl-2 upregulation in pregnancy. J Immunol. 2013; 191, 145.CrossRefGoogle ScholarPubMed
Hu, M, Eviston, D, Hsu, P, et al.Decreased maternal serum acetate and impaired fetal thymic and regulatory T cell development in preeclampsia. Nat Commun. 2019; 10, 3031.CrossRefGoogle ScholarPubMed
Nguyen Maria, U, Wallace Megan, J, Pepe, S, Menheniott, TR, Moss Timothy, J, Burgner, D.Perinatal inflammation: a common factor in the early origins of cardiovascular disease? Clin Sci. 2015; 129: 769–784.CrossRefGoogle Scholar
Alexander, BT.Placental insufficiency leads to development of hypertension in growth-restricted offspring. Hypertension. 2003; 41: 457–462.CrossRefGoogle ScholarPubMed
Alexander, BT, Hendon, AE, Ferril, G, Dwyer, TM.Renal denervation abolishes hypertension in low-birth-weight offspring from pregnant rats with reduced uterine perfusion. Hypertension. 2005; 45, 754–758.CrossRefGoogle ScholarPubMed
Ojeda, NB, Grigore, D, Yanes, LL, et al.Testosterone contributes to marked elevations in mean arterial pressure in adult male intrauterine growth restricted offspring. Am J Physiol Regul Integr Comp Physiol. 2007; 292, R758–R763.CrossRefGoogle ScholarPubMed
Heltemes, A, Gingery, A, Soldner, EL, et al.Chronic placental ischemia alters amniotic fluid milieu and results in impaired glucose tolerance, insulin resistance and hyperleptinemia in young rats. Exp Biol Med (Maywood). 2010; 235, 892–899.CrossRefGoogle ScholarPubMed
Dasinger, JH, Intapad, S, Backstrom, MA, Carter, AJ, Alexander, BT.Intrauterine growth restriction programs an accelerated age-related increase in cardiovascular risk in male offspring. Am J Physiol Renal Physiol. 2016; 311, F312–F319.CrossRefGoogle ScholarPubMed
Peyronnet, J, Roux, JC, Geloen, A, et al.Prenatal hypoxia impairs the postnatal development of neural and functional chemoafferent pathway in rat. J Physiol. 2000; 524(Pt 2), 525–537.CrossRefGoogle ScholarPubMed
Tang, J, Zhu, Z, Xia, S, et al.Chronic hypoxia in pregnancy affected vascular tone of renal interlobar arteries in the offspring. Sci Rep. 2015; 5, 9723.CrossRefGoogle ScholarPubMed
Liu, B, Liu, Y, Shi, R, et al.Chronic prenatal hypoxia down-regulated BK channel beta1 subunits in mesenteric artery smooth muscle cells of the offspring. Cell Physiol Biochem. 2018; 45, 1603–1616.CrossRefGoogle ScholarPubMed
Jin, Z, Zhang, W, Yang, H, et al.Maternal treatment with agonistic autoantibodies against type-1 angiotensin II receptor in late pregnancy increases apoptosis of myocardial cells and myocardial susceptibility to ischemia-reperfusion injury in offspring rats. PloS One. 2013; 8, e80709.CrossRefGoogle ScholarPubMed
Herraiz, S, Pellicer, B, Serra, V, et al.Sildenafil citrate improves perinatal outcome in fetuses from pre-eclamptic rats. BJOG. 2012; 119, 1394–1402.CrossRefGoogle ScholarPubMed
McDonnold, M, Tamayo, E, Kechichian, T, et al.The effect of prenatal pravastatin treatment on altered fetal programming of postnatal growth and metabolic function in a preeclampsia-like murine model. Am J Obstet Gynecol. 2014; 210, 542 e1–542 e7.CrossRefGoogle Scholar
Intapad, S, Tull, FL, Brown, AD, et al.Renal denervation abolishes the age-dependent increase in blood pressure in female intrauterine growth-restricted rats at 12 months of age. Hypertension. 2013; 61, 828–834.CrossRefGoogle ScholarPubMed
Intapad, S, Dasinger, JH, Fahling, JM, Backstrom, MA, Alexander, BT.Testosterone is protective against impaired glucose metabolism in male intrauterine growth-restricted offspring. PloS One. 2017; 12, e0187843.CrossRefGoogle ScholarPubMed
Bytautiene, E, Tamayo, E, Kechichian, T, et al.Prepregnancy obesity and sFlt1-induced preeclampsia in mice: developmental programming model of metabolic syndrome. Am J Obstet Gynecol. 2011; 204, 398 e1–398 e8.CrossRefGoogle ScholarPubMed
Intapad, S, Dasinger, JH, Brown, AD, Fahling, JM, Esters, J, Alexander, BT.Glucose intolerance develops prior to increased adiposity and accelerated cessation of estrous cyclicity in female growth-restricted rats. Pediatr Res. 2016; 79, 962–970.CrossRefGoogle ScholarPubMed
Butruille, L, Mayeur, S, Moitrot, E, et al.Maternal hypertension induced by NO blockade does not program adult metabolic diseases in growth-restricted rat fetuses. Metabolism. 2013; 62, 442–445.CrossRefGoogle Scholar
Payne, JA, Alexander, BT, Khalil, RA.Reduced endothelial vascular relaxation in growth-restricted offspring of pregnant rats with reduced uterine perfusion. Hypertension. 2003; 42, 768–774.CrossRefGoogle ScholarPubMed
Peyronnet, J, Dalmaz, Y, Ehrstrom, M, et al.Long-lasting adverse effects of prenatal hypoxia on developing autonomic nervous system and cardiovascular parameters in rats. Pflugers Arch. 2002, 443, 858–865.CrossRefGoogle ScholarPubMed
Wang, L, Li, M, Huang, Z, Wang, Z.The influence of hypoxia during different pregnancy stages on cardiac collagen accumulation in the adult offspring. Biomed Res Int. 2014; 2014, 419805.Google ScholarPubMed
Witlin, AG, Gangula, PR, Thompson, ML, Yallampalli, C.Growth and fertility rates in the offspring of pregnant rats treated with L-omega nitro-L-arginine methyl ester (L-NAME), a nitric oxide inhibitor. Am J Obstet Gynecol. 2002; 186, 89–93.CrossRefGoogle Scholar
Allison, BJ, Kaandorp, JJ, Kane, AD, et al.Divergence of mechanistic pathways mediating cardiovascular aging and developmental programming of cardiovascular disease. FASEB J. 2016; 30, 1968–1975.CrossRefGoogle ScholarPubMed
Tang, J, Li, N, Chen, X, et al.Prenatal hypoxia induced dysfunction in cerebral arteries of offspring rats. J Am Heart Assoc. 2017; 6, pii: e006630.CrossRefGoogle ScholarPubMed
Martini, VC, Mandarim-de-Lacerda, CA. Offspring myocardium alteration from dams submitted to nitric oxide synthesis inhibition during pregnancy. Int J Cardiol. 2005; 100, 377–382.CrossRefGoogle ScholarPubMed
Lock, MC, Tellam, RL, Botting, KJ, et al.The role of miRNA regulation in fetal cardiomyocytes, cardiac maturation and the risk of heart disease in adults. J Physiol. 2018; 596, 5625–5640.Google ScholarPubMed
Yeung, KR, Sunderland, N, Lind, JM, et al.Increased salt sensitivity in offspring of pregnancies complicated by experimental preeclampsia. Clin Exp Pharmacol Physiol. 2018; 45, 1302–1308.CrossRefGoogle ScholarPubMed
Luyckx, VA, Bertram, JF, Brenner, BM, et al.Effect of fetal and child health on kidney development and long-term risk of hypertension and kidney disease. Lancet. 2013; 382, 273–283.CrossRefGoogle ScholarPubMed
Keller, G, Zimmer, G, Mall, G, Ritz, E, Amann, K.Nephron number in patients with primary hypertension. New Engl J Med. 2003; 348, 101–108.CrossRefGoogle ScholarPubMed
Richter, VF, Briffa, JF, Moritz, KM, Wlodek, ME, Hryciw, DH.The role of maternal nutrition, metabolic function and the placenta in developmental programming of renal dysfunction. Clin Exp Pharmacol Physiol. 2016; 43, 135–141.CrossRefGoogle ScholarPubMed
Marchand, MC, Langley-Evans, SC.Intrauterine programming of nephron number: the fetal flaw revisited. J Nephrol. 2001; 14, 327–331.Google ScholarPubMed
Moritz, KM, Cuffe, JS, Wilson, LB, et al.Review: sex specific programming: a critical role for the renal renin-angiotensin system. Placenta. 2010; 31(Suppl), S40–S46.CrossRefGoogle ScholarPubMed
Berdasco, M, Esteller, M.Clinical epigenetics: seizing opportunities for translation. Nat Rev Genet. 2019; 20, 109–127.CrossRefGoogle ScholarPubMed
Karlsson, O, Baccarelli, AA.Environmental health and long non-coding RNAs. Curr Environ Health Rep. 2016; 3, 178–187.CrossRefGoogle ScholarPubMed
Heindel, JJ. The developmental basis of disease: update on environmental exposures and animal models. Basic Clin Pharmacol Toxicol. 2019; 125(Suppl 3), 5–13.Google Scholar
Hanson, MA, Skinner, MK.Developmental origins of epigenetic transgenerational inheritance. Environ Epigenet. 2016; 2, pii: dvw002.CrossRefGoogle ScholarPubMed
Goyal, D, Limesand, SW, Goyal, R.Epigenetic responses and the developmental origins of health and disease. J Endocrinol. 2019; 242, T105–T119.CrossRefGoogle ScholarPubMed
Hanson, M.The Inheritance Of Cardiovascular Disease Risk. Acta Paediatrica (Oslo, Norway : 1992). 2019; 108, 1747–1756.CrossRefGoogle ScholarPubMed
Apicella, C, Ruano, CSM, Mehats, C, Miralles, F, Vaiman, D.The role of epigenetics in placental development and the etiology of preeclampsia. Int J Molecul Sci. 2019; 20, pii: E2837.CrossRefGoogle ScholarPubMed
Bianco-Miotto, T, Mayne, BT, Buckberry, S, Breen, J, Rodriguez Lopez, CM, Roberts, CT.Recent progress towards understanding the role of DNA methylation in human placental development. Reproduction (Cambridge, England). 2016; 152, R23–R30.CrossRefGoogle ScholarPubMed
Kazmi, N, Sharp, GC, Reese, SE, et al.Hypertensive disorders of pregnancy and DNA methylation in newborns. Hypertension. 2019; 74, 375–383.CrossRefGoogle ScholarPubMed
Julian, CG, Pedersen, BS, Salmon, CS, et al.Unique DNA methylation patterns in offspring of hypertensive pregnancy. Clin Transl Sci. 2015; 8, 740–745.CrossRefGoogle ScholarPubMed
Murray, R, Bryant, J, Titcombe, P, et al.DNA methylation at birth within the promoter of ANRIL predicts markers of cardiovascular risk at 9 years. Clin Epigenet. 2016; 8, 90.CrossRefGoogle ScholarPubMed
Tarrade, A, Panchenko, P, Junien, C, Gabory, A.Placental contribution to nutritional programming of health and diseases: epigenetics and sexual dimorphism. J Experiment Biol. 2015; 218, 50–58.CrossRefGoogle ScholarPubMed
Andraweera, PH, Dekker, GA, Arstall, M, Bianco-Miotto, T, Roberts, CT.Complications of Pregnancy and Future Cardiovascular Risk. Encycl Cardiovasc Res Med. 2018; 1, 643–650.CrossRefGoogle Scholar
Lie, RT, Rasmussen, S, Brunborg, H, Gjessing, HK, Lie-Nielsen, E, Irgens, LM.Fetal and maternal contributions to risk of pre-eclampsia: population based study. BMJ (Clinical Research Edition). 1998; 316, 1343–1347.CrossRefGoogle ScholarPubMed
Esplin, MS, Fausett, MB, Fraser, A, et al.Paternal and maternal components of the predisposition to preeclampsia. New Engl J Med. 2001; 344, 867–872.CrossRefGoogle ScholarPubMed
Andraweera, PH, Dekker, GA, Thompson, SD, Roberts, CT.Single-nucleotide polymorphisms in the KDR gene in pregnancies complicated by gestational hypertensive disorders and small-for-gestational-age infants. Reprod Sci. 2012; 19, 547–554.CrossRefGoogle ScholarPubMed
Andraweera, PH, Gatford, KL, Dekker, GA, et al.The INSR rs2059806 single nucleotide polymorphism, a genetic risk factor for vascular and metabolic disease, associates with pre-eclampsia. Reprod Biomed Online. 2017; 34, 392–398.CrossRefGoogle ScholarPubMed
Andraweera, PH, Dekker, GA, Thompson, SD, Dissanayake, VH, Jayasekara, RW, Roberts, CT.Hypoxia-inducible factor-1alpha gene polymorphisms in early and late onset preeclampsia in Sinhalese women. Placenta. 2014; 35, 491–495.CrossRefGoogle ScholarPubMed
Andraweera, PH, Dekker, GA, Thompson, SD, North, RA, McCowan, LM, Roberts, CT.A functional variant in ANGPT1 and the risk of pregnancies with hypertensive disorders and small-for-gestational-age infants. Mol Hum Reprod. 2012; 18, 325–332.CrossRefGoogle ScholarPubMed
Sitras, V, Fenton, C, Acharya, G.Gene expression profile in cardiovascular disease and preeclampsia: a meta-analysis of the transcriptome based on raw data from human studies deposited in Gene Expression Omnibus. Placenta. 2015; 36, 170–178.CrossRefGoogle ScholarPubMed
Johnson, MP, Fitzpatrick, E, Dyer, TD, et al.Identification of two novel quantitative trait loci for pre-eclampsia susceptibility on chromosomes 5q and 13q using a variance components-based linkage approach. Mol Hum Reprod. 2007; 13, 61–67.CrossRefGoogle ScholarPubMed
Loset, M, Johnson, MP, Melton, PE, et al.Preeclampsia and cardiovascular disease share genetic risk factors on chromosome 2q22. Pregnancy Hypertens. 2014; 4, 178–185.CrossRefGoogle ScholarPubMed
Cheong, JN, Wlodek, ME, Moritz, KM, Cuffe, JS.Programming of maternal and offspring disease: impact of growth restriction, fetal sex and transmission across generations. J Physiol. 2016; 594, 4727–4740.CrossRefGoogle Scholar
Alsnes, IV, Vatten, LJ, Fraser, A, et al.Hypertension in pregnancy and offspring cardiovascular risk in young adulthood: prospective and sibling studies in the HUNT Study (Nord-Trondelag Health Study) in Norway. Hypertension. 2017; 69, 591–598.CrossRefGoogle Scholar
Hughson, M, Farris, AB, 3rd, Douglas-Denton, R, Hoy, WE, Bertram, JF.Glomerular number and size in autopsy kidneys: the relationship to birth weight. Kidney Int. 2003; 63, 2113–2122.CrossRefGoogle ScholarPubMed