Preeclampsia and Fetal Congenital Heart Defects

Article ID: e150422203675 Pages: 12

  • * (Excluding Mailing and Handling)

Abstract

Endothelial dysfunction, impaired implantation and placental insufficiency have been identified as mechanisms behind the development of pre-eclampsia, resulting in angiogenic factors’ alteration. Angiogenic imbalance is also associated with congenital heart defects, and this common physiologic pathway may explain the association between them and pre-eclampsia. This review aims to understand the physiology shared by these two entities and whether women with pre-eclampsia have an increased risk of fetal congenital heart defects (or the opposite). The present research has highlighted multiple vasculogenic pathways associated with heart defects and preeclampsia, but also epigenetic and environmental factors, contributing both. It is also known that fetuses with a prenatal diagnosis of congenital heart disease have an increased risk of several comorbidities, including intrauterine growth restriction. Moreover, the impact of pre-eclampsia goes beyond pregnancy as it increases the risk for following pregnancies and for diseases later in life in both offspring and mothers. Given the morbidity and mortality associated with these conditions, it is of foremost importance to understand how they are related and its causative mechanisms. This knowledge may allow earlier diagnosis, an adequate surveillance or even the implementation of preventive strategies.

Keywords: Placenta, trophoblastic invasion, pre-eclampsia, congenital heart defects, gestational hypertension, diagnosis.

Graphical Abstract

[1]
Brodwall K, Leirgul E, Greve G, et al. Possible common aetiology behind maternal preeclampsia and congenital heart defects in the child: A cardiovascular diseases in Norway project study. Paediatr Perinat Epidemiol 2016; 30(1): 76-85.
[http://dx.doi.org/10.1111/ppe.12252] [PMID: 26479038]
[2]
Courtney JA, Cnota JF, Jones HN. The role of abnormal placentation in congenital heart disease; Cause, correlate, or consequence? Front Physiol 2018; 9: 1045.
[http://dx.doi.org/10.3389/fphys.2018.01045] [PMID: 30131711]
[3]
Thilaganathan B. Preeclampsia and fetal congenital heart defects: Spurious association or maternal confounding? Circulation 2017; 136(1): 49-51.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.117.028816] [PMID: 28674092]
[4]
Fantasia I, Andrade W, Syngelaki A, Akolekar R, Nicolaides KH. Impaired placental perfusion and major fetal cardiac defects. Ultrasound Obstet Gynecol 2019; 53(1): 68-72.
[http://dx.doi.org/10.1002/uog.20149] [PMID: 30334326]
[5]
Cedergren MI, Källén BA. Obstetric outcome of 6346 pregnancies with infants affected by congenital heart defects. Eur J Obstet Gynecol Reprod Biol 2006; 125(2): 211-6.
[http://dx.doi.org/10.1016/j.ejogrb.2005.07.006] [PMID: 16137818]
[6]
Llurba Olive E, Xiao E, Natale DR, Fisher SA. Oxygen and lack of oxygen in fetal and placental development, feto-placental coupling, and congenital heart defects. Birth Defects Res 2018; 110(20): 1517-30.
[http://dx.doi.org/10.1002/bdr2.1430] [PMID: 30576091]
[7]
Boyd HA, Basit S, Behrens I, et al. Association between fetal congenital heart defects and maternal risk of hypertensive disorders of preg-nancy in the same pregnancy and across pregnancies. Circulation 2017; 136(1): 39-48.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.116.024600] [PMID: 28424221]
[8]
Kenchegowda D, Natale B, Lemus MA, Natale DR, Fisher SA. Inactivation of maternal Hif-1α at mid-pregnancy causes placental defects and deficits in oxygen delivery to the fetal organs under hypoxic stress. Dev Biol 2017; 422(2): 171-85.
[http://dx.doi.org/10.1016/j.ydbio.2016.12.013] [PMID: 27940158]
[9]
Camm EJ, Botting KJ, Sferruzzi-Perri AN. Near to one’s heart: The intimate relationship between the placenta and fetal heart. Front Physiol 2018; 9: 629.
[http://dx.doi.org/10.3389/fphys.2018.00629] [PMID: 29997513]
[10]
Llurba E, Sánchez O, Ferrer Q, et al. Maternal and foetal angiogenic imbalance in congenital heart defects. Eur Heart J 2014; 35(11): 701-7.
[http://dx.doi.org/10.1093/eurheartj/eht389] [PMID: 24159191]
[11]
Ruiz A, Ferrer Q, Sánchez O, et al. Placenta-related complications in women carrying a foetus with congenital heart disease. J Matern Fetal Neonatal Med 2016; 29(20): 3271-5.
[http://dx.doi.org/10.3109/14767058.2015.1121480] [PMID: 26744775]
[12]
Sliwa K, Mebazaa A. Possible joint pathways of early pre-eclampsia and congenital heart defects via angiogenic imbalance and potential evidence for cardio-placental syndrome. Eur Heart J 2014; 35(11): 680-2.
[http://dx.doi.org/10.1093/eurheartj/eht485] [PMID: 24302271]
[13]
Midgett M, Thornburg K, Rugonyi S. Blood flow patterns underlie developmental heart defects. Am J Physiol Heart Circ Physiol 2017; 312(3): H632-42.
[http://dx.doi.org/10.1152/ajpheart.00641.2016] [PMID: 28062416]
[14]
Linask KK. The heart-placenta axis in the first month of pregnancy: Induction and prevention of cardiovascular birth defects. J Preg 2013; p. 320413.
[PMID: 23691322]
[15]
Huppertz B, Peeters L. Vascular biology in implantation and placentation. Angiogenesis 2005; 8: 157-67.
[http://dx.doi.org/10.1007/s10456-005-9007-8] [PMID: 16211358]
[16]
Thornburg K, O’Tierney P, Louey S. The placenta is a programming agent for cardiovascular disease. Placenta 2010; 31: S54-9.
[http://dx.doi.org/10.1016/j.placenta.2010.01.002]
[17]
Alsaied T, Tseng S, King E, et al. Effect of fetal hemodynamics on growth in fetuses with single ventricle or transposition of the great arteries. Ultrasound Obstet Gynecol 2018; 52(4): 479-87.
[http://dx.doi.org/10.1002/uog.18936] [PMID: 29057564]
[18]
Wallenstein MB, Harper LM, Odibo AO, et al. Fetal congenital heart disease and intrauterine growth restriction: A retrospective cohort study. J Matern Fetal Neonatal Med 2012; 25(6): 662-5.
[http://dx.doi.org/10.3109/14767058.2011.597900] [PMID: 21823904]
[19]
Malik S, Cleves MA, Zhao W, Correa A, Hobbs CA. Association between congenital heart defects and small for gestational age. Pediatrics 2007; 119(4): e976-82.
[http://dx.doi.org/10.1542/peds.2006-2742] [PMID: 17387169]
[20]
Itsukaichi M, Kikuchi A, Yoshihara K, Serikawa T, Takakuwa K, Tanaka K. Changes in fetal circulation associated with congenital heart disease and their effects on fetal growth. Fetal Diagn Ther 2011; 30(3): 219-24.
[http://dx.doi.org/10.1159/000330202] [PMID: 21849766]
[21]
Fouzas S, Karatza AA, Davlouros PA, et al. Heterogeneity of ventricular repolarization in newborns with intrauterine growth restriction. Early Hum Dev 2014; 90(12): 857-62.
[http://dx.doi.org/10.1016/j.earlhumdev.2014.09.009] [PMID: 25463832]
[22]
Williams IA, Fifer C, Jaeggi E, Levine JC, Michelfelder EC, Szwast AL. The association of fetal cerebrovascular resistance with early neu-rodevelopment in single ventricle congenital heart disease. Am Heart J 2013; 165(4): 544-550.e1.
[http://dx.doi.org/10.1016/j.ahj.2012.11.013] [PMID: 23537971]
[23]
Vanlieferinghen S, Bernard JP, Salomon LJ, Chalouhi GE, Russell NE, Ville Y. Second trimester growth restriction and underlying fetal anomalies. Gynécol Obstét Fertil 2014; 42(9): 567-71.
[http://dx.doi.org/10.1016/j.gyobfe.2014.07.002] [PMID: 25164160]
[24]
Chen CP, Liu YP, Lin SP, et al. Ventriculomegaly, intrauterine growth restriction, and congenital heart defects as salient prenatal so-nographic findings of Miller-Dieker lissencephaly syndrome associated with monosomy 17p (17p13.2 --> pter) in a fetus. Taiwan J Obstet Gynecol 2010; 49(1): 81-6.
[http://dx.doi.org/10.1016/S1028-4559(10)60015-0] [PMID: 20466299]
[25]
Alpay F, Gül D, Lenk MK, Oğur G. Severe intrauterine growth retardation, aged facial appearance, and congenital heart disease in a new-born with Johanson-Blizzard syndrome. Pediatr Cardiol 2000; 21(4): 389-90.
[http://dx.doi.org/10.1007/s002460010089] [PMID: 10865022]
[26]
Yaegashi N, Uehara S, Ogawa H, et al. Association of intrauterine growth retardation with monosomy of the terminal segment of the short arm of the X chromosome in patients with Turner’s syndrome. Gynecol Obstet Invest 2000; 50(4): 237-41.
[http://dx.doi.org/10.1159/000010323] [PMID: 11093045]
[27]
Miremberg H, Gindes L, Schreiber L, Raucher Sternfeld A, Bar J, Kovo M. The association between severe fetal congenital heart defects and placental vascular malperfusion lesions. Prenat Diagn 2019; 39(11): 962-7.
[http://dx.doi.org/10.1002/pd.5515] [PMID: 31254468]
[28]
Balli S, Kibar AE, Ece I, Oflaz MB, Yilmaz O. Assessment of fetal cardiac function in mild preeclampsia. Pediatr Cardiol 2013; 34(7): 1674-9.
[http://dx.doi.org/10.1007/s00246-013-0702-8] [PMID: 23591803]
[29]
Burton GJ, Jauniaux E. Development of the human placenta and fetal heart: Synergic or independent? Front Physiol 2018; 9: 373.
[http://dx.doi.org/10.3389/fphys.2018.00373] [PMID: 29706899]
[30]
Tan CMJ, Lewandowski AJ. The transitional heart: From early embryonic and fetal development to neonatal life. Fetal Diagn Ther 2020; 47(5): 373-86.
[PMID: 31533099]
[31]
Bhorat I, Pillay M, Reddy T. The clinical prognostic significance of myocardial performance index (MPI) in stable placental-mediated disease. Cardiovasc J Afr 2018; 29(5): 310-6.
[PMID: 30152840]
[32]
Api O, Emeksiz MB, Api M, Ugurel V, Unal O. Modified myocardial performance index for evaluation of fetal cardiac function in pre-eclampsia. Ultrasound Obstet Gynecol 2009; 33(1): 51-7.
[http://dx.doi.org/10.1002/uog.6272] [PMID: 19086000]
[33]
Cooper KM, Barrett T, McBride CA, et al. Subclinical cardiac stiffness is associated with arterial stiffness in healthy young nulligravid women: Potential links to preeclampsia. Pregnancy Hypertens 2019; 18: 49-54.
[http://dx.doi.org/10.1016/j.preghy.2019.09.001] [PMID: 31525709]
[34]
Youssef L, Miranda J, Paules C, et al. Fetal cardiac remodeling and dysfunction is associated with both preeclampsia and fetal growth restriction. Am J Obstet Gynecol 2020; 222(1): 79.e1-9.
[http://dx.doi.org/10.1016/j.ajog.2019.07.025] [PMID: 31336074]
[35]
Hoodbhoy Z, Hasan BS, Mohammed N, Chowdhury D. Impact of pre-eclampsia on the cardiovascular health of the offspring: A cohort study protocol. BMJ Open 2018; 8(9)e024331
[http://dx.doi.org/10.1136/bmjopen-2018-024331] [PMID: 30257849]
[36]
Steinert JR, Wyatt AW, Jacob R, Mann GE. Redox modulation of Ca2+ signaling in human endothelial and smooth muscle cells in pre-eclampsia. Antioxid Redox Signal 2009; 11(5): 1149-63.
[http://dx.doi.org/10.1089/ars.2008.2303] [PMID: 19125611]
[37]
Tong W, Giussani DA. Preeclampsia link to gestational hypoxia. J Dev Orig Health Dis 2019; 10(3): 322-33.
[http://dx.doi.org/10.1017/S204017441900014X] [PMID: 30968806]
[38]
Yum MK, Kim K, Kim JH, Park EY. A consistent abnormality in the average local smoothness of fetal heart rate in growth-restricted fe-tuses affected by severe pre-eclampsia. Hypertens Res 2004; 27(12): 911-8.
[http://dx.doi.org/10.1291/hypres.27.911] [PMID: 15894830]
[39]
Yum MK, Kim CR, Park EY, Kim JH. Instability and frequency-domain variability of heart rates in fetuses with or without growth re-striction affected by severe preeclampsia. Physiol Meas 2004; 25(5): 1105-13.
[http://dx.doi.org/10.1088/0967-3334/25/5/002] [PMID: 15535177]
[40]
Yousif D, Bellos I, Penzlin AI, et al. Autonomic dysfunction in preeclampsia: A systematic review. Front Neurol 2019; 10: 816.
[http://dx.doi.org/10.3389/fneur.2019.00816] [PMID: 31447757]
[41]
Crispi F, Comas M, Hernández-Andrade E, et al. Does pre-eclampsia influence fetal cardiovascular function in early-onset intrauterine growth restriction? Ultrasound Obstet Gynecol 2009; 34(6): 660-5.
[http://dx.doi.org/10.1002/uog.7450] [PMID: 19827117]
[42]
Akil A, Api O, Oten Can E, et al. Does preeclampsia have any adverse effect on fetal heart? J Matern Fetal Neonatal Med 2016; 29(14): 2312-5.
[PMID: 26381715]
[43]
Andraweera PH, Gatford KL, Care AS, et al. Mechanisms linking exposure to preeclampsia in utero and the risk for cardiovascular dis-ease. J Dev Orig Health Dis 2020; 11(3): 235-42.
[http://dx.doi.org/10.1017/S2040174420000094] [PMID: 32070456]
[44]
Hammad IA, Meeks H, Fraser A, et al. Risks of cause-specific mortality in offspring of pregnancies complicated by hypertensive disease of pregnancy. Am J Obstet Gynecol 2020; 222(1): 75.e1-9.
[http://dx.doi.org/10.1016/j.ajog.2019.07.024] [PMID: 31336073]
[45]
Malik S, Cleves MA, Honein MA, et al. Maternal smoking and congenital heart defects. Pediatrics 2008; 121(4): e810-6.
[http://dx.doi.org/10.1542/peds.2007-1519] [PMID: 18381510]
[46]
Cedergren MI, Källén BA. Maternal obesity and infant heart defects. Obes Res 2003; 11(9): 1065-71.
[http://dx.doi.org/10.1038/oby.2003.146] [PMID: 12972676]
[47]
Aberg A, Westbom L, Källén B. Congenital malformations among infants whose mothers had gestational diabetes or preexisting diabetes. Early Hum Dev 2001; 61(2): 85-95.
[http://dx.doi.org/10.1016/S0378-3782(00)00125-0] [PMID: 11223271]
[48]
Smedts HP, van Uitert EM, Valkenburg O, et al. A derangement of the maternal lipid profile is associated with an elevated risk of congeni-tal heart disease in the offspring. Nutr Metab Cardiovasc 2012; pp. 477-85.
[http://dx.doi.org/10.1016/j.numecd.2010.07.016]
[49]
Giachini FR, Galaviz-Hernandez C, Damiano AE, et al. Vascular dysfunction in mother and offspring during preeclampsia: Contributions from Latin-American countries. Curr Hypertens Rep 2017; 19(10): 83.
[http://dx.doi.org/10.1007/s11906-017-0781-7] [PMID: 28986756]
[50]
Stojanovska V, Scherjon SA, Plösch T. Preeclampsia as modulator of offspring health. Biol Reprod 2016; 94(3): 53.
[http://dx.doi.org/10.1095/biolreprod.115.135780] [PMID: 26792940]
[51]
Arabin B, Baschat AA. Pregnancy: An underutilized window of opportunity to improve long-term maternal and infant health-an appeal for continuous family care and interdisciplinary communication. Front Pediatr 2017; 5: 69.
[http://dx.doi.org/10.3389/fped.2017.00069] [PMID: 28451583]
[52]
Pinheiro TV, Brunetto S, Ramos JG, Bernardi JR, Goldani MZ. Hypertensive disorders during pregnancy and health outcomes in the off-spring: A systematic review. J Dev Orig Health Dis 2016; 7(4): 391-407.
[http://dx.doi.org/10.1017/S2040174416000209] [PMID: 27168118]
[53]
Herzog EM, Eggink AJ, Willemsen SP, et al. Early- and late-onset preeclampsia and the tissue-specific epigenome of the placenta and newborn. Placenta 2017; 58: 122-32.
[http://dx.doi.org/10.1016/j.placenta.2017.08.070] [PMID: 28962690]
[54]
Staff AC, Dechend R, Pijnenborg R. Learning from the placenta: Acute atherosis and vascular remodeling in preeclampsia-novel aspects for atherosclerosis and future cardiovascular health. Hypertension 2010; 56(6): 1026-34.
[http://dx.doi.org/10.1161/HYPERTENSIONAHA.110.157743] [PMID: 20956732]
[55]
Girchenko P, Lahti J, Czamara D, et al. Associations between maternal risk factors of adverse pregnancy and birth outcomes and the off-spring epigenetic clock of gestational age at birth. Clin Epigenetics 2017; 9(1): 49.
[http://dx.doi.org/10.1186/s13148-017-0349-z] [PMID: 28503212]
[56]
Anderson CM, Ralph JL, Wright ML, Linggi B, Ohm JE. DNA methylation as a biomarker for preeclampsia. Biol Res Nurs 2014; 16(4): 409-20.
[http://dx.doi.org/10.1177/1099800413508645] [PMID: 24165327]
[57]
Timpka S, Macdonald-Wallis C, Hughes AD, et al. Hypertensive disorders of pregnancy and offspring cardiac structure and function in adolescence. J Am Heart Assoc 2016; 5(11)e003906
[http://dx.doi.org/10.1161/JAHA.116.003906] [PMID: 27799232]
[58]
Phillips C, Boyd M. Assessment, management, and health implications of early-onset preeclampsia. Nurs Womens Health 2016; 20(4): 400-14.
[http://dx.doi.org/10.1016/j.nwh.2016.07.003] [PMID: 27520604]
[59]
Herrera-Garcia G, Contag S. Maternal preeclampsia and risk for cardiovascular disease in offspring. Curr Hypertens Rep 2014; 16(9): 475.
[http://dx.doi.org/10.1007/s11906-014-0475-3] [PMID: 25097112]
[60]
Rodie VA, Caslake MJ, Stewart F, et al. Fetal cord plasma lipoprotein status in uncomplicated human pregnancies and in pregnancies complicated by pre-eclampsia and intrauterine growth restriction. Atherosclerosis 2004; 176(1): 181-7.
[http://dx.doi.org/10.1016/j.atherosclerosis.2004.04.026] [PMID: 15306192]
[61]
Cheng SB, Sharma S. Preeclampsia and health risks later in life: An immunological link. Semin Immunopathol 2016; 38(6): 699-708.
[http://dx.doi.org/10.1007/s00281-016-0579-8] [PMID: 27339196]
[62]
Duffy J, Hirsch M, Kawsar A, et al. Outcome reporting across randomised controlled trials evaluating therapeutic interventions for pre-eclampsia. BJOG 2017; 124(12): 1829-39.
[http://dx.doi.org/10.1111/1471-0528.14702] [PMID: 28432737]
[63]
Tranquilli AL, Landi B, Giannubilo SR, Sibai BM. Preeclampsia: No longer solely a pregnancy disease. Pregnancy Hypertens 2012; 2(4): 350-7.
[http://dx.doi.org/10.1016/j.preghy.2012.05.006] [PMID: 26105602]
[64]
Enkhmaa D, Wall D, Mehta PK, et al. Preeclampsia and vascular function: A window to future cardiovascular disease risk. J Womens Health (Larchmt) 2016; 25(3): 284-91.
[http://dx.doi.org/10.1089/jwh.2015.5414] [PMID: 26779584]
[65]
Simard JF, Rossides M, Arkema EV, et al. Maternal hypertensive disorders in SLE pregnancy and future cardiovascular outcomes. Arthritis Care Res (Hoboken) 2021; 73(4): 574-9.
[PMID: 32004410]
[66]
Bassily E, Bell C, Verma S, Patel N, Patel A. Significance of obstetrical history with future cardiovascular disease risk. Am J Med 2019; 132(5): 567-71.
[http://dx.doi.org/10.1016/j.amjmed.2018.11.029] [PMID: 30550756]
[67]
Paauw ND, Lely AT. Cardiovascular sequels during and after preeclampsia. Adv Exp Med Biol 2018; 1065: 455-70.
[http://dx.doi.org/10.1007/978-3-319-77932-4_28] [PMID: 30051401]
[68]
Rasmussen LG, Lykke JA, Staff AC. Angiogenic biomarkers in pregnancy: Defining maternal and fetal health. Acta Obstet Gynecol Scand 2015; 94(8): 820-32.
[http://dx.doi.org/10.1111/aogs.12629] [PMID: 25753566]
[69]
Honigberg MC, Givertz MM. Peripartum cardiomyopathy. BMJ 2019; 364: k5287.
[http://dx.doi.org/10.1136/bmj.k5287] [PMID: 30700415]
[70]
Riise HKR, Sulo G, Tell GS, et al. Hypertensive pregnancy disorders increase the risk of maternal cardiovascular disease after adjustment for cardiovascular risk factors. Int J Cardiol 2019; 282: 81-7.
[http://dx.doi.org/10.1016/j.ijcard.2019.01.097] [PMID: 30773269]
[71]
Brosens I, Benagiano M, Puttemans P, D’Elios MM, Benagiano G. The placental bed vascular pathology revisited: A risk indicator for cardiovascular disease. J Matern Fetal Neonatal Med 2019; 32(9): 1556-64.
[http://dx.doi.org/10.1080/14767058.2017.1409718] [PMID: 29172831]
[72]
Lane-Cordova AD, Khan SS, Grobman WA, Greenland P, Shah SJ. Long-term cardiovascular risks associated with ad-verse pregnancy outcomes: JACC review topic of the week. J Am Coll Cardiol 2019; 73(16): 2106-16.
[http://dx.doi.org/10.1016/j.jacc.2018.12.092] [PMID: 31023435]
[73]
Rangaswami J, Naranjo M, McCullough PA. Preeclampsia as a form of type 5 cardiorenal syndrome: An underrecognized entity in Wom-en’s cardiovascular health. Cardiorenal Med 2018; 8(2): 160-72.
[http://dx.doi.org/10.1159/000487646] [PMID: 29627841]
[74]
Berks D, Hoedjes M, Raat H, et al. Feasibility and effectiveness of a lifestyle intervention after complicated pregnancies to improve risk factors for future cardiometabolic disease. Pregnancy Hypertens 2019; 15: 98-107.
[http://dx.doi.org/10.1016/j.preghy.2018.12.004] [PMID: 30825935]
[75]
Wu P, Mamas MA, Gulati M. Pregnancy as a predictor of maternal cardiovascular disease: The era of cardio obstetrics. J Womens Health (Larchmt) 2019; 28(8): 1037-50.
[http://dx.doi.org/10.1089/jwh.2018.7480] [PMID: 31408425]
[76]
Carty DM, Delles C, Dominiczak AF. Preeclampsia and future maternal health. J Hypertens 2010; 28(7): 1349-55.
[http://dx.doi.org/10.1097/HJH.0b013e32833a39d0] [PMID: 20467325]
[77]
Hauspurg A, Countouris ME, Catov JM. Hypertensive disorders of pregnancy and future maternal health: How can the evidence guide postpartum management? Curr Hypertens Rep 2019; 21(12): 96.
[http://dx.doi.org/10.1007/s11906-019-0999-7] [PMID: 31776692]
[78]
Kvehaugen AS, Andersen LF, Staff AC, Staff AC. Dietary intake and physical activity in women and offspring after pregnancies compli-cated by preeclampsia or diabetes mellitus. Acta Obstet Gynecol Scand 2010; 89(11): 1486-90.
[http://dx.doi.org/10.3109/00016349.2010.519378] [PMID: 20955103]
[79]
Neiger R. Long-term effects of pregnancy complications on maternal health: A review. J Clin Med 2017; 6(8)E76
[http://dx.doi.org/10.3390/jcm6080076] [PMID: 28749442]
[80]
Newman RA, Hameed AB. Matters of the heart: Cardiovascular health in women throughout their lifetimes. Obstet Gynecol Clin North Am 2019; 46(3): 515-25.
[http://dx.doi.org/10.1016/j.ogc.2019.04.009] [PMID: 31378292]
[81]
Rich-Edwards JW, Fraser A, Lawlor DA, Catov JM. Pregnancy characteristics and women’s future cardiovascular health: An underused opportunity to improve women’s health? Epidemiol Rev 2014; 36(1): 57-70.
[http://dx.doi.org/10.1093/epirev/mxt006] [PMID: 24025350]
[82]
Shah S, Gupta A. Hypertensive disorders of pregnancy. Cardiol Clin 2019; 37(3): 345-54.
[http://dx.doi.org/10.1016/j.ccl.2019.04.008] [PMID: 31279428]
[83]
Grandi SM, Filion KB, Yoon S, et al. Cardiovascular disease-related morbidity and mortality in women with a history of pregnancy com-plications. Circulation 2019; 139(8): 1069-79.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.118.036748] [PMID: 30779636]
[84]
Gladstone RA, Pudwell J, Nerenberg KA, Grover SA, Smith GN. Cardiovascular risk assessment and follow-up of women after hyperten-sive disorders of pregnancy: A prospective cohort study. J Obstet Gynaecol Can 2019; 41(8): 1157-1167.e1.
[http://dx.doi.org/10.1016/j.jogc.2018.10.024] [PMID: 30655227]
[85]
Peixoto AB, Rolo LC, Nardozza LMM, Araujo Júnior E. Epigenetics and preeclampsia: Programming of future outcomes. Methods Mol Biol 2018; 1710: 73-83.
[http://dx.doi.org/10.1007/978-1-4939-7498-6_6] [PMID: 29196995]
[86]
Mito A, Arata N, Qiu D, et al. Hypertensive disorders of pregnancy: A strong risk factor for subsequent hypertension 5 years after deliv-ery. Hypertens Res 2018; 41(2): 141-6.
[http://dx.doi.org/10.1038/hr.2017.100] [PMID: 29093561]
[87]
Kräker K, Schütte T, O’Driscoll J, et al. Speckle tracking echocardiography: New ways of translational approaches in preeclampsia to detect cardiovascular dysfunction. Int J Mol Sci 2020; 21(3): 1162.
[http://dx.doi.org/10.3390/ijms21031162] [PMID: 32050556]
[88]
Soma-Pillay P, Louw MC, Adeyemo AO, Makin J, Pattinson RC. Cardiac diastolic function after recovery from pre-eclampsia. Cardiovasc J Afr 2018; 29(1): 26-31.
[http://dx.doi.org/10.5830/CVJA-2017-031] [PMID: 28906533]
[89]
Vasapollo B, Novelli GP, Gagliardi G, Farsetti D, Valensise H. Pregnancy complications in chronic hypertensive patients are linked to pre-pregnancy maternal cardiac function and structure. Am J Obstet Gynecol 2020; 223(3): 425.e1-e13.
[http://dx.doi.org/10.1016/j.ajog.2020.02.043] [PMID: 32142824]
[90]
Stergiotou I, Crispi F, Valenzuela-Alcaraz B, Bijnens B, Gratacos E. Patterns of maternal vascular remodeling and responsiveness in early- versus late-onset preeclampsia. Am J Obstet Gynecol 2013; 209(6): 558.e1-558.e14.
[http://dx.doi.org/10.1016/j.ajog.2013.07.030] [PMID: 23911383]
[91]
White WM, Mielke MM, Araoz PA, et al. A history of preeclampsia is associated with a risk for coronary artery calcification 3 decades later. Am J Obstet Gynecol 2016; 214(4): 519.e1-8.
[http://dx.doi.org/10.1016/j.ajog.2016.02.003] [PMID: 26874301]
[92]
Auger N, Potter BJ, He S, Healy-Profitós J, Schnitzer ME, Paradis G. Maternal cardiovascular disease 3 decades after preterm birth: Longi-tudinal cohort study of pregnancy vascular disorders. Hypertension 2020; 75(3): 788-95.
[http://dx.doi.org/10.1161/HYPERTENSIONAHA.119.14221] [PMID: 32008431]
[93]
Brouwers L, van der Meiden-van Roest AJ, Savelkoul C, et al. Recurrence of pre-eclampsia and the risk of future hypertension and cardi-ovascular disease: A systematic review and meta-analysis. BJOG 2018; 125(13): 1642-54.
[http://dx.doi.org/10.1111/1471-0528.15394] [PMID: 29978553]
[94]
Adams T, Yeh C, Bennett-Kunzier N, Kinzler WL. Long-term maternal morbidity and mortality associated with ischemic placental disease. Semin Perinatol 2014; 38(3): 146-50.
[http://dx.doi.org/10.1053/j.semperi.2014.03.003] [PMID: 24836826]
[95]
Kessous R, Shoham-Vardi I, Parientel G, Sheiner E. Assotiation between pregnancy complications and long term maternal cardiovascular morbidity. Harefuah 2016; 155(5): 286-290, 322.
[PMID: 27526556]
[96]
Facca TA, Kirsztajn GM, Sass N. Preeclampsia (marker of chronic kidney disease): From genesis to future risks. J Bras Nefrol 2012; 34(1): 87-93.
[http://dx.doi.org/10.1590/S0101-28002012000100015] [PMID: 22441189]
[97]
Mirabito Colafella KM. Endothelin type B (ETB) receptors: Friend or foe in the pathogenesis of pre-eclampsia and future cardiovascular disease (CVD) risk? Clin Sci (Lond) 2018; 132(1): 33-6.
[http://dx.doi.org/10.1042/CS20171366] [PMID: 29295950]
[98]
Shahul S, Tung A, Minhaj M, et al. Racial disparities in comorbidities, complications, and maternal and fetal outcomes in women with preeclampsia/eclampsia. Hypertens Pregnancy 2015; 34(4): 506-15.
[http://dx.doi.org/10.3109/10641955.2015.1090581] [PMID: 26636247]
[99]
Soh MC, Dib F, Nelson-Piercy C, Westgren M, McCowan L, Pasupathy D. Maternal-placental syndrome and future risk of accelerated cardiovascular events in Parous Swedish women with systemic lupus erythematosus - a population-based retrospective cohort study with time-to-event analysis. Rheumatology (Oxford) 2016; 55(7): 1235-42.
[http://dx.doi.org/10.1093/rheumatology/kew043] [PMID: 27016663]
[100]
Hanson M. The inheritance of cardiovascular disease risk. Acta Paediatr 2019; 108(10): 1747-56.
[http://dx.doi.org/10.1111/apa.14813] [PMID: 30964948]
[101]
Leslie K, Whitley GS, Herse F, et al. Increased apoptosis, altered oxygen signaling, and antioxidant defenses in first-trimester pregnancies with high-resistance uterine artery blood flow. Am J Pathol 2015; 185(10): 2731-41.
[http://dx.doi.org/10.1016/j.ajpath.2015.06.020] [PMID: 26362067]