Advertisement

Long-term sequelae of adverse pregnancy outcomes

  • Nare Torosyan
    Affiliations
    Cedars-Sinai Smidt Heart Institute, Los Angeles, CA, United States of America
    Search for articles by this author
  • Dalia Aziz
    Affiliations
    Women's Heart Center, The Christ Hospital Heart and Vascular Institute, Cincinnati, OH, United States of America
    Search for articles by this author
  • Odayme Quesada
    Correspondence
    Corresponding author at: The Carl and Edyth Lindner Center for Research and Education, The Christ Hospital Health Network, 2123 Auburn Avenue Suite 424, Cincinnati, OH 45219, United States of America.
    Affiliations
    Women's Heart Center, The Christ Hospital Heart and Vascular Institute, Cincinnati, OH, United States of America

    The Carl and Edyth Lindner Center for Research and Education, The Christ Hospital, Cincinnati, OH, United States of America
    Search for articles by this author

      Highlights

      • Adverse pregnancy outcomes represent a failed stress test for women at risk.
      • Adverse pregnancy outcomes increase women's risk of cardiovascular disease.
      • Adverse pregnancy outcomes should be accounted for in a woman's risk assessment for cardiovascular disease and stratification.

      Abstract

      A growing body of literature highlights the importance of recognizing adverse pregnancy outcomes (APOs) as cardiovascular risk factors when risk stratifying women for cardiovascular disease (CVD). We conducted a comprehensive review of the long term cardiovascular consequences associated with APOs including hypertensive disorders of pregnancy (HDP), preterm delivery, gestational diabetes (GDM), low birth weight and fetal growth restriction during pregnancy using electronic databases, PubMed and the Cochrane Library. Women with pregnancies complicated by HDP, preterm birth, and low birth weight are at higher risk of developing CVD than were women without APOs in the years following pregnancy. Among women with a history of multiple APOs, HDP and GDM are independent risk factors for atherosclerotic CVD. The pathophysiology leading to CVD is multifactorial, and includes both physiologic and environmental factors. APOs should be accounted for in a women's CVD risk assessment and stratification as recommended by prevention guidelines. Further research is needed to determine the underlying mechanisms that lead to the increased risk of CVD in women with APOs.

      Keywords

      Abbreviations:

      APO (adverse pregnancy outcomes), CVD (cardiovascular disease), GDM (gestational diabetes), HDP (hypertensive disorders of pregnancy), AHA (American Heart Association), ACC (American College of Cardiology), ESC (European Society of Cardiology)
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Maturitas
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Rich-Edwards J.W.
        • Fraser A.
        • Lawlor D.A.
        • Catov J.M.
        Pregnancy characteristics and women's future cardiovascular health: an underused opportunity to improve women's health?.
        Epidemiol. Rev. 2013; 36: 57-70https://doi.org/10.1093/epirev/mxt006
        • Parikh N.I.
        • Gonzalez J.M.
        • Anderson C.A.M.
        • Judd S.E.
        • Rexrode K.M.
        • Hlatky M.A.
        • Gunderson E.P.
        • Stuart J.J.
        • Vaidya D.
        • <collab>Council on Arteriosclerosis Thrombosis and Vascular Biologycollab
        • American Heart Association Council on Epidemiology and Prevention
        • Council on Cardiovascular and Stroke Nursing
        • the Stroke Council
        Adverse pregnancy outcomes and cardiovascular disease risk: unique opportunities for cardiovascular disease prevention in women: a scientific statement from the American Heart Association.
        Circulation. 2021; 143: e902-e916https://doi.org/10.1161/CIR.0000000000000961
        • Vogel B.
        • Acevedo M.
        • Appelman Y.
        • Bairey Merz C.N.
        • Chieffo A.
        • Figtree G.A.
        • Guerrero M.
        • Kunadian V.
        • Lam C.S.P.
        • Maas A.H.E.M.
        • Mihailidou A.S.
        • Olszanecka A.
        • Poole J.E.
        • Saldarriaga C.
        • Saw J.
        • Zühlke L.
        • Mehran R.
        The lancet women and cardiovascular disease commission: reducing the global burden by 2030.
        Lancet. 2021; 397: 2385-2438https://doi.org/10.1016/S0140-6736(21)00684-X
        • Lane-Cordova A.D.
        • Khan S.S.
        • Grobman W.A.
        • Greenland P.
        • Shah S.J.
        Long-term cardiovascular risks associated with adverse pregnancy outcomes: JACC review topic of the week.
        J. Am. Coll. Cardiol. 2019; 73: 2106-2116https://doi.org/10.1016/j.jacc.2018.12.092
        • Benschop L.
        • Brouwers L.
        • Zoet G.A.
        • Meun C.
        • Boersma E.
        • Budde R.P.J.
        • Fauser B.C.J.M.
        • de Groot C.M.J.
        • van der Schouw Y.T.
        • Maas A.H.E.M.
        • Velthuis B.K.
        • Linstra K.M.
        • Kavousi M.
        • Duvekot J.J.
        • Franx A.
        • Steegers E.
        • van Rijn B.B.
        • van Lennep J.E.Roeters
        • CREW Consortium
        Early onset of coronary artery calcification in women with previous preeclampsia.
        Circ. Cardiovasc. Imaging. 2020; 13e010340https://doi.org/10.1161/CIRCIMAGING.119.010340
        • Arnett D.K.
        • Blumenthal R.S.
        • Albert M.A.
        • Buroker A.B.
        • Goldberger Z.D.
        • Hahn E.J.
        • Himmelfarb C.D.
        • Khera A.
        • Lloyd-Jones D.
        • McEvoy J.W.
        • Michos E.D.
        • Miedema M.D.
        • Muñoz D.
        • Smith Jr., S.C.
        • Virani Jr., S.S.
        • Williams Sr., K.A.
        • Yeboah Sr., J.
        • Ziaeian Sr., B.
        2019 ACC/AHA guideline on the primary prevention of cardiovascular disease: a report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines.
        J. Am. Coll. Cardiol. 2019; 74: e177-e232https://doi.org/10.1016/j.jacc.2019.03.010
        • Visseren F.L.J.
        • Mach F.
        • Smulders Y.M.
        • Carballo D.
        • Benetos A.
        • Biffi A.
        • Boavida J.M.
        • Capodanno D.
        • Cosyns B.
        • Crawford C.
        • Davos C.H.
        • Desormais I.
        • Angelantonio E.Di
        • Franco O.H.
        • Halvorsen S.
        • Hobbs F.D.R.
        • Hollander M.
        • Jankowska E.A.
        • Michal M.
        • Sacco S.
        • Sattar N.
        • Tokgozoglu L.
        • Tonstad S.
        • Tsioufis K.P.
        • van Dis I.
        • van Gelder I.C.
        • Wanner C.
        • Williams B.
        • Koskinas K.C.
        • Bäck M.
        • ESC Scientific Document Group
        2021 ESC Guidelines on cardiovascular disease prevention in clinical practice: Developed by the Task Force for cardiovascular disease prevention in clinical practice with representatives of the European Society of Cardiology and 12 medical societies With the special contribution of the European Association of Preventive Cardiology (EAPC).
        Eur. Heart J. 2021; 42: 3227-3227-3337https://doi.org/10.1093/eurheartj/ehab484
        • Hutcheon J.A.
        • Lisonkova S.
        • Joseph K.S.
        Epidemiology of pre-eclampsia and the other hypertensive disorders of pregnancy.
        Best. Pract. Res. Clin. Obstet. Gynaecol. 2011; 25: 391-403https://doi.org/10.1016/j.bpobgyn.2011.01.006
        • Say L.
        • Chou D.
        • Gemmill A.
        • Tunçalp Ö.
        • Moller A.B.
        • Daniels J.
        • Gülmezoglu A.M.
        • Temmerman M.
        • Alkema L.
        Global causes of maternal death: a WHO systematic analysis.
        Lancet Glob. Health. 2014; 2: e323-e333https://doi.org/10.1016/s2214-109x(14)70227-x
        • Wu R.
        • Wang T.
        • Gu R.
        • Xing D.
        • Ye C.
        • Chen Y.
        • Liu X.
        • Chen L.
        Hypertensive disorders of pregnancy and risk of cardiovascular disease-related morbidity and mortality: a systematic review and meta-analysis.
        Cardiology. 2020; 145: 633-647https://doi.org/10.1159/000508036
        • Mogos M.F.
        • Salemi J.L.
        • Spooner K.K.
        • McFarlin B.L.
        • Salihu H.H.
        Hypertensive disorders of pregnancy and postpartum readmission in the United States: national surveillance of the revolving door.
        J. Hypertens. 2018; 36: 608-618https://doi.org/10.1097/hjh.0000000000001594
        • Scantlebury D.C.
        • Kattah A.G.
        • Weissgerber T.L.
        • Agarwal S.
        • Mielke M.M.
        • Weaver A.L.
        • Vaughan L.E.
        • Henkin S.
        • Zimmerman K.
        • Miller V.M.
        • White W.M.
        • Hayes S.N.
        • Garovic V.D.
        Impact of a history of hypertension in pregnancy on later diagnosis of atrial fibrillation.
        J. Am. Heart Assoc. 2018; 7e007584https://doi.org/10.1161/JAHA.117.007584
        • Grandi S.M.
        • Filion K.B.
        • Yoon S.
        • Ayele H.T.
        • Doyle C.M.
        • Hutcheon J.A.
        • Smith G.N.
        • Gore G.C.
        • Ray J.G.
        • Nerenberg K.
        • Platt R.W.
        Cardiovascular disease-related morbidity and mortality in women with a history of pregnancy complications.
        Circulation. 2019; 139: 1069-1079https://doi.org/10.1161/CIRCULATIONAHA.118.036748
        • Yang J.J.
        • Lee S.A.
        • Choi J.Y.
        • Song M.
        • Han S.
        • Yoon H.S.
        • Lee Y.
        • Oh J.
        • Lee J.K.
        • Kang D.
        Subsequent risk of metabolic syndrome in women with a history of preeclampsia: data from the health examinees study.
        J. Epidemiol. 2015; 25: 281-288https://doi.org/10.2188/jea.JE20140136
        • Søndergaard M.M.
        • Hlatky M.A.
        • Stefanick M.L.
        • Vittinghoff E.
        • Nah G.
        • Allison M.
        • Gemmill A.
        • Horn L.Van
        • Park K.
        • Salmoirago-Blotcher E.
        • Sattari M.
        • Sealy-Jefferson S.
        • Shadyab A.H.
        • Valdiviezo C.
        • Manson J.E.
        • Parik N.I.
        Association of adverse pregnancy outcomes with risk of atherosclerotic cardiovascular disease in postmenopausal women.
        JAMA Cardiol. 2020; 5: 1390-1398https://doi.org/10.1001/jamacardio.2020.4097
        • Scheres L.J.J.
        • Lijfering W.M.
        • Groenewegen N.F.M.
        • Koole S.
        • de Groot C.J.M.
        • Middeldorp S.
        • Cannegieter S.C.
        Hypertensive complications of pregnancy and risk of venous thromboembolism.
        Hypertension. 2020; 75: 781-787https://doi.org/10.1161/HYPERTENSIONAHA.119.14280
        • Wu P.
        • Haththotuwa R.
        • Kwok C.S.
        • Babu A.
        • Kotronias R.A.
        • Rushton C.
        • Zaman A.
        • Fryer A.A.
        • Kadam U.
        • Chew-Graham C.A.
        • Mamas M.A.
        Preeclampsia and future cardiovascular health.
        Circ. Cardiovasc. Qual. Outcomes. 2017; 10e003497https://doi.org/10.1161/CIRCOUTCOMES.116.003497
        • Brouwers L.
        • van der Meiden-van Roest A.
        • Savelkoul C.
        • Vogelvang T.E.
        • Lely A.T.
        • Franx A.
        • van Rijn B.B.
        Recurrence of pre-eclampsia and the risk of future hypertension and cardiovascular disease: a systematic review and meta-analysis.
        BJOG. 2018; 125: 1642-1654https://doi.org/10.1111/1471-0528.15394
        • Schliep K.
        • Zhang Y.
        • Tschanz J.
        • Majersik J.
        • Facelli J.
        • Varner M.
        Hypertensive disorders of pregnancy and risk of Alzheimer’s disease, vascular dementia, and other related dementia.
        Innovation in Aging. 2021; 5: 653https://doi.org/10.1093/geroni/igab046.2456
        • Romundstad P.R.
        • Magnussen E.B.
        • Smith G.D.
        • Vatten L.J.
        Hypertension in pregnancy and later cardiovascular risk.
        Circulation. 2010; 122: 579-584https://doi.org/10.1161/CIRCULATIONAHA.110.943407
        • Stuart J.J.
        • Tanz L.J.
        • Rimm E.B.
        • Spiegelman D.
        • Missmer S.A.
        • Mukamal K.J.
        • Rexrode K.M.
        • Rich-Edwards J.W.
        Cardiovascular risk factors mediate the long-term maternal risk associated with hypertensive disorders of pregnancy.
        J. Am. Coll. Cardiol. 2022; 79: 1901-1913https://doi.org/10.1016/j.jacc.2022.03.335
        • Ying W.
        • Catov J.M.
        • Ouyang P.
        Hypertensive disorders of pregnancy and future maternal cardiovascular risk.
        J. Am. Heart Assoc. 2018; 7e009382https://doi.org/10.1161/JAHA.118.009382
        • Granger J.P.
        • Alexander B.T.
        • Llinas M.T.
        • Bennett W.A.
        • Khalil R.A.
        Pathophysiology of hypertension during preeclampsia linking placental ischemia with endothelial dysfunction.
        Hypertension. 2001; 38: 718-722https://doi.org/10.1161/01.HYP.38.3.718
        • Staff A.C.
        • Fjeldstad H.E.
        • Fosheim I.K.
        • Moe K.
        • Turowski G.
        • Johnsen G.M.
        • Alnaes-Katjavivi P.
        • Sugulle M.
        Failure of physiological transformation and spiral artery atherosis: their roles in preeclampsia.
        Am. J. Obstet. Gynecol. 2022; 226: S895-S906https://doi.org/10.1016/j.ajog.2020.09.026
        • Gray K.J.
        • Saxena R.
        • Karumanchi S.A.
        Genetic predisposition to preeclampsia is conferred by fetal DNA variants near FLT1, a gene involved in the regulation of angiogenesis.
        Am. J. Obstet. Gynecol. 2018; 218: 211-218https://doi.org/10.1016/j.ajog.2017.11.562
        • Purisch S.E.
        • Gyamfi-Bannerman C.
        Epidemiology of preterm birth.
        Semin. Perinatol. 2017; 41: 387-391https://doi.org/10.1053/j.semperi.2017.07.009
        • Rubens C.E.
        • Sadovsky Y.
        • Muglia L.
        • Gravett M.G.
        • Lackritz E.
        • Gravett C.
        Prevention of preterm birth: harnessing science to address the global epidemic.
        Sci. Transl. Med. 2014; 6: 262sr5https://doi.org/10.1126/scitranslmed.3009871
        • Ely D.M.
        • Driscoll A.K.
        Infant mortality in the United States, 2017: data from the period linked birth/infant death file.
        Natl. Vital. Stat. Rep. 2019; 68 (PMID: 32501205): 1-20
        • Black R.E.
        • Cousens S.
        • Johnson H.L.
        • Lawn J.E.
        • Rudan I.
        • Bassani D.G.
        • Jha P.
        • Campbell H.
        • Walker C.F.
        • Cibulskis R.
        • Eisele T.
        • Liu L.
        • Mathers C.
        • Child Health Epidemiology Reference Group of WHO and UNICEF
        Global, regional, and national causes of child mortality in 2008: a systematic analysis.
        Lancet. 2010; 375: 1969-1987https://doi.org/10.1016/S0140-6736(10)60549-1
        • Tanz L.J.
        • Stuart J.J.
        • Williams P.L.
        • Missmer S.A.
        • Rimm E.B.
        • James-Todd T.M.
        • Rich-Edwards J.W.
        Preterm delivery and maternal cardiovascular disease risk factors: the nurses' health study II.
        J. Women's Health. 2018; 28: 677-685https://doi.org/10.1089/jwh.2018.7150
        • Crump C.
        • Sundquist J.
        • Howell E.A.
        • McLaughlin M.A.
        • Stroustrup A.
        • Sundquist K.
        Pre-term delivery and risk of ischemic heart disease in women.
        J. Am. Coll. Cardiol. 2020; 76: 57-67https://doi.org/10.1016/j.jacc.2020.04.072
        • Crump C.
        • Sundquist J.
        • Sundquist K.
        Preterm delivery and long term mortality in women: national cohort and co-sibling study.
        BMJ. 2020; 370m2533https://doi.org/10.1136/bmj.m2533
        • Crump C.
        • Sundquist J.
        • Sundquist K.
        Preterm delivery and long-term risk of stroke in women: a national cohort and cosibling study.
        Circulation. 2021; 143: 2032-2044https://doi.org/10.1161/CIRCULATIONAHA.120.052268
        • Crump C.
        • Sundquist J.
        • Sundquist K.
        Preterm delivery and long-term risk of hypertension in women.
        JAMA Cardiol. 2022; 7: 65-74https://doi.org/10.1001/jamacardio.2021.4127
        • Wu P.
        • Gulati M.
        • Kwok C.S.
        • Wong C.W.
        • Narain A.
        • O'Brien S.
        • Chew-Graham C.A.
        • Verma G.
        • Kadam U.T.
        • Mamas M.A.
        Preterm delivery and future risk of maternal cardiovascular disease: a systematic review and meta-analysis.
        J. Am. Heart Assoc. 2018; 7e007809https://doi.org/10.1161/JAHA.117.007809
        • Lewandowski A.J.
        • Levy P.T.
        • Bates M.L.
        • McNamara P.J.
        • Nuyt A.M.
        • Goss K.N.
        Impact of the vulnerable preterm heart and circulation on adult cardiovascular disease risk.
        Hypertension. 2020; 76: 1028-1037https://doi.org/10.1161/HYPERTENSIONAHA.120.15574
        • Minissian M.B.
        • Kilpatrick S.
        • Eastwood J.A.
        • Robbins W.A.
        • Accortt E.E.
        • Wei J.
        • Shufelt C.L.
        • Doering L.V.
        • Merz C.N.B.
        Association of Spontaneous Preterm Delivery and Future Maternal Cardiovascular Disease.
        Circulation. 2018; 137: 865-871https://doi.org/10.1161/CIRCULATIONAHA.117.031403
        • Rodriguez B.S.Quintanilla
        • Mahdy H.
        Gestational Diabetes. [Updated 2021 Aug 25].
        (Available from:)in: StatPearls [Internet]. StatPearls Publishing, Treasure Island (FL)2022
        • Bellamy L.
        • Casas J.P.
        • Hingorani A.D.
        • Williams D.
        Type 2 diabetes mellitus after gestational diabetes: a systematic review and meta-analysis.
        Lancet. 2009; 373: 1773-1779https://doi.org/10.1016/s0140-6736(09)60731-5
        • Goueslard K.
        • Cottenet J.
        • Mariet A.S.
        • Giroud M.
        • Cottin Y.
        • Petit J.M.
        • Quantin C.
        Early cardiovascular events in women with a history of gestational diabetes mellitus.
        Cardiovasc. Diabetol. 2016; 15: 15https://doi.org/10.1186/s12933-016-0338-0
        • Kramer C.K.
        • Campbell S.
        • Retnakaran R.
        Gestational diabetes and the risk of cardiovascular disease in women: a systematic review and meta-analysis.
        Diabetologia. 2019; 62: 905-914https://doi.org/10.1007/s00125-019-4840-2
        • Tobias D.K.
        • Stuart J.J.
        • Li S.
        • Chavarro J.
        • Rimm E.B.
        • Rich-Edwards J.
        • Hu F.B.
        • Manson J.E.
        • Zhang C.
        Association of History of gestational diabetes with long-term cardiovascular disease risk in a large prospective cohort of US women.
        JAMA Intern. Med. 2017; 177: 1735-1742https://doi.org/10.1001/jamainternmed.2017.2790
        • Gunderson E.P.
        • Sun B.
        • Catov J.M.
        • Carnethon M.
        • Lewis C.E.
        • Allen N.B.
        • Sidney S.
        • Wellons M.
        • Rana J.S.
        • Hou L.
        • Carr J.J.
        Gestational diabetes history and glucose tolerance after pregnancy associated with coronary artery calcium in women during midlife: the CARDIA study.
        Circulation. 2021; 143: 974-987https://doi.org/10.1161/circulationaha.120.047320
        • Retnakaran R.
        Hyperglycemia in pregnancy and its implications for a woman's future risk of cardiovascular disease.
        Diabetes Res. Clin. Pract. 2018; 145: 193-199https://doi.org/10.1016/j.diabres.2018.04.008
        • Retnakaran R.
        • Qi Y.
        • Connelly P.W.
        • Sermer M.
        • Zinman B.
        • Hanley A.J.
        Glucose intolerance in pregnancy and postpartum risk of metabolic syndrome in young women.
        J. Clin. Endocrinol. Metab. 2010; 95: 670-677https://doi.org/10.1210/jc.2009-1990
        • Retnakaran R.
        The insulin-like growth factor axis: a newplayer in gestational diabetes?.
        Diabetes. 2016; 65: 3246-3248https://doi.org/10.2337/dbi16-0048
        • Filardi T.
        • Catanzaro G.
        • Grieco G.E.
        • Splendiani E.
        • Trocchianesi S.
        • Santangelo C.
        • Brunelli R.
        • Guarino E.
        • Sebastiani G.
        • Dotta F.
        • Morano S.
        • Ferretti E.
        Identification and validation of miR-222-3p and miR-409-3p as plasma biomarkers in gestational diabetes mellitus sharing validated target genes involved in metabolic homeostasis.
        Int. J. Mol. Sci. 2022; 23: 4276https://doi.org/10.3390/ijms23084276
        • Gęca T.
        • Kwaśniewska A.
        The influence of gestational diabetes mellitus upon the selected parameters of the maternal and fetal system of insulin-like growth factors (IGF-1, IGF-2, IGFBP1-3)-a review and a clinical study.
        J. Clin. Med. 2020; 9: 3256https://doi.org/10.3390/jcm9103256
        • Davey Smith G.
        • Hyppönen E.
        • Power C.
        • Lawlor D.A.
        Offspring birth weight and parental mortality: prospective observational study and meta-analysis.
        Am. J. Epidemiol. 2007; 166: 160-169https://doi.org/10.1093/aje/kwm054
        • Horikoshi M.
        • Beaumont R.N.
        • Day F.R.
        • Warrington N.M.
        • Kooijman M.N.
        • Fernandez-Tajes J.
        • Feenstra B.
        • van Zuydam N.R.
        • Gaulton K.J.
        • Grarup N.
        • Bradfield J.P.
        • Strachan D.P.
        • Li-Gao R.
        • Ahluwalia T.S.
        • Kreiner E.
        • Rueedi R.
        • Lyytikäinen L.P.
        • Cousminer D.L.
        • Wu Y.
        • Thiering E.
        • Wang C.A.
        • Have C.T.
        • Hottenga J.J.
        • Vilor-Tejedor N.
        • Joshi P.K.
        • Boh E.T.H.
        • Ntalla I.
        • Pitkänen N.
        • Mahajan A.
        • van Leeuwen E.M.
        • Joro R.
        • Lagou V.
        • Nodzenski M.
        • Diver L.A.
        • Zondervan K.T.
        • Bustamante M.
        • Marques-Vidal P.
        • Mercader J.M.
        • Bennett A.J.
        • Rahmioglu N.
        • Nyholt D.R.
        • Ma R.C.W.
        • Tam C.H.T.
        • Tam W.H.
        • Group C.H.A.R.G.E.Consortium Hematology Working
        • Ganesh S.K.
        • van Rooij F.J.
        • Jones S.E.
        • Loh P.R.
        • Ruth K.S.
        • Tuke M.A.
        • Tyrrell J.
        • Wood A.R.
        • Yaghootkar H.
        • Scholtens D.M.
        • Paternoster L.
        • Prokopenko I.
        • Kovacs P.
        • Atalay M.
        • Willems S.M.
        • Panoutsopoulou K.
        • Wang X.
        • Carstensen L.
        • Geller F.
        • Schraut K.E.
        • Murcia M.
        • van Beijsterveldt C.E.
        • Willemsen G.
        • Appel E.V.R.
        • Fonvig C.E.
        • Trier C.
        • Tiesler C.M.
        • Standl M.
        • Kutalik Z.
        • Bonas-Guarch S.
        • Hougaard D.M.
        • Sánchez F.
        • Torrents D.
        • Waage J.
        • Hollegaard M.V.
        • de Haan H.G.
        • Rosendaal F.R.
        • Medina-Gomez C.
        • Ring S.M.
        • Hemani G.
        • McMahon G.
        • Robertson N.R.
        • Groves C.J.
        • Langenberg C.
        • Luan J.
        • Scott R.A.
        • Zhao J.H.
        • Mentch F.D.
        • MacKenzie S.M.
        • Reynolds R.M.
        • Lowe Jr., W.L.
        • Tönjes Jr., A.
        • Stumvoll Jr., M.
        • Lindi Jr., V.
        • Lakka Jr., T.A.
        • van Duijn Jr., C.M.
        • Kiess Jr., W.
        • Körner Jr., A.
        • Sørensen Jr., T.I.
        • Niinikoski Jr., H.
        • Pahkala Jr., K.
        • Raitakari Jr., O.T.
        • Zeggini Jr., E.
        • Teo Jr., G.V.Dedoussis Y.Y.
        • Saw Jr., S.M.
        • Melbye Jr., M.
        • Campbell Jr., H.
        • Wilson Jr., J.F.
        • Vrijheid Jr., M.
        • de Geus Jr., E.J.
        • Boomsma Jr., D.I.
        • Kadarmideen Jr., H.N.
        • Holm Jr., J.C.
        • Hansen Jr., T.
        • Sebert Jr., S.
        • Hattersley Jr., A.T.
        • Beilin Jr., L.J.
        • Newnham Jr., J.P.
        • Pennell Jr., C.E.
        • Heinrich Jr., J.
        • Adair Jr., L.S.
        • Borja Jr., J.B.
        • Mohlke Jr., K.L.
        • Eriksson Jr., J.G.
        • Kähönen Jr., M.
        • Viikari Jr., J.S.
        • Lehtimäki Jr., T.
        • Vollenweider Jr., P.
        • Bønnelykke Jr., K.
        • Bisgaard Jr., H.
        • Mook-Kanamori Jr., D.O.
        • Hofman Jr., A.
        • Rivadeneira Jr., F.
        • Uitterlinden Jr., A.G.
        • Pisinger Jr., C.
        • Pedersen Jr., O.
        • Power Jr., C.
        • Hyppönen Jr., E.
        • Wareham Jr., N.J.
        • Hakonarson Jr., H.
        • Davies Jr., E.
        • Walker Jr., B.R.
        • Jaddoe Jr., V.W.
        • Jarvelin Jr., M.R.
        • Grant Jr., S.F.
        • Vaag Jr., A.A.
        • Lawlor Jr., D.A.
        • Frayling Jr., T.M.
        • Smith Jr., G.Davey
        • Morris Jr., A.P.
        • Ong Jr., K.K.
        • Felix Jr., J.F.
        • Timpson Jr., N.J.
        • Perry Jr., J.R.
        • Evans Jr., D.M.
        • McCarthy Jr., M.I.
        • Freathy Jr., R.M.
        • Widén E.E.
        • Early Growth Genetics (EGG) Consortium
        Genome-wide associations for birth weight and corr.elations with adult disease.
        Nature. 2016; 538: 248-252https://doi.org/10.1038/nature19806
        • Melamed N.
        • Baschat A.
        • Yinon Y.
        • Athanasiadis A.
        • Mecacci F.
        • Figueras F.
        • Berghella V.
        • Nazareth A.
        • Tahlak M.
        • McIntyre H.D.
        • Da Silva Costa F.
        • Kihara A.B.
        • Hadar E.
        • McAuliffe F.
        • Hanson M.
        • Ma R.C.
        • Gooden R.
        • Sheiner E.
        • Kapur A.
        • Divakar H.
        • Ayres-de-Campos D.
        • Hiersch L.
        • Poon L.C.
        • Kingdom J.
        • Romero R.
        • Hod M.
        FIGO (international Federation of Gynecology and obstetrics) initiative on fetal growth: best practice advice for screening, diagnosis, and management of fetal growth restriction.
        Int. J. Gynaecol. Obstet. 2021; 152: 3-57https://doi.org/10.1002/ijgo.13522
        • Yinon Y.
        • Kingdom J.C.
        • Odutayo A.
        • Moineddin R.
        • Drewlo S.
        • Lai V.
        • Cherney D.Z.
        • Hladunewich M.A.
        Vascular dysfunction in women with a history of preeclampsia and intrauterine growth restriction: insights into future vascular risk.
        Circulation. 2010; 122: 1846-1853https://doi.org/10.1161/circulationaha.110.948455
        • Melchiorre K.
        • Sutherland G.R.
        • Liberati M.
        • Thilaganathan B.
        Maternal cardiovascular impairment in pregnancies complicated by severe fetal growth restriction.
        Hypertension. 2012; 60: 437-443https://doi.org/10.1161/HYPERTENSIONAHA.112.194159
        • Beck Jensen R.B.
        • Chellakooty M.
        • Vielwerth S.
        • Vaag A.
        • Larsen T.
        • Greisen G.
        • Skakkebaek N.E.
        • Scheike T.
        • Juul A.
        Intrauterine growth retardation and consequences for endocrine and cardiovascular diseases in adult life: does insulin-like growth factor-I play a role?.
        Horm. Res. 2003; 60: 136-148https://doi.org/10.1159/000074515
        • Johnston L.B.
        • Clark A.J.
        • Savage M.O.
        Genetic factors contributing to birth weight.
        Arch. Dis. Child. Fetal. Neonatal. Ed. 2002; 86: F2-F3https://doi.org/10.1136/fn.86.1.f2-a
        • Li C.Y.
        • Chen H.F.
        • Sung F.C.
        • Chen C.C.
        • Lu T.H.
        • Yang C.H.
        • Ko M.C.
        Offspring birth weight and parental cardiovascular mortality.
        Int. J. Epidemiol. 2010; 39: 1082-1090https://doi.org/10.1093/ije/dyq045
        • Nguyen B.
        • Jin K.
        • Ding D.
        Breastfeeding and maternal cardiovascular risk factors and outcomes: a systematic review.
        PLoS One. 2017; 12: e0187923https://doi.org/10.1371/journal.pone.0187923
        • Gunderson E.P.
        • Lewis C.E.
        • Lin Y.
        • Sorel M.
        • Gross M.
        • Sidney S.
        • Jacobs Jr., D.R.
        • Shikany J.M.
        • Quesenberry Jr., C.P.
        Lactation duration and progression to diabetes in women across the childbearing years: the 30-year CARDIA study.
        JAMA Intern. Med. 2018; 178: 328-337https://doi.org/10.1001/jamainternmed.2017.7978
        • Ajmera V.H.
        • Terrault N.A.
        • VanWagner L.B.
        • Sarkar M.
        • Lewis C.E.
        • Carr J.J.
        • Gunderson E.P.
        Longer lactation duration is associated with decreased prevalence of non-alcoholic fatty liver disease in women.
        J. Hepatol. 2019; 70: 126-132https://doi.org/10.1016/j.jhep.2018.09.013
        • Jacobson L.T.
        • EM E.M.Hade
        • Collins T.C.
        • Margolis K.L.
        • Waring M.E.
        • Horn L.V.Van
        • Silver B.
        • Sattari M.
        • Bird C.E.
        • Kimminau K.
        • Wambach K.
        • Stefanick M.L.
        Breastfeeding History and Risk of Stroke Among Parous Postmenopausal Women in the Women's Health Initiative.
        J. Am. Heart. Assoc. 2018; 7e008739https://doi.org/10.1161/JAHA.118.008739
        • Nguyen B.
        • Gale J.
        • Nassar N.
        • Bauman A.
        • Joshy G.
        • Ding D.
        Breastfeeding and cardiovascular disease hospitalization and mortality in parous women: evidence from a large australian cohort study.
        J. Am. Heart Assoc. 2019; 8e011056https://doi.org/10.1161/JAHA.118.011056
        • Hypertension in pregnancy
        Report of the American College of Obstetricians and Gynecologists’ Task Force on Hypertension in Pregnancy.
        Obstet. Gynecol. 2013; 122: 1122-1131https://doi.org/10.1097/01.AOG.0000437382.03963.88
        • Ying W.
        • Catov J.M.
        • Ouyang P.
        Hypertensive disorders of pregnancy and future maternal cardiovascular risk.
        J. Am. Heart Assoc. 2018; 7e009382https://doi.org/10.1161/JAHA.118.009382
        • Roberge S.
        • Nicolaides K.
        • Demers S.
        • Hyett J.
        • Chaillet N.
        • Bujold E.
        The role of aspirin dose on the prevention of preeclampsia and fetal growth restriction: systematic review and meta-analysis.
        Am. J. Obstet. Gynecol. 2017; 216: 110-120.e6https://doi.org/10.1016/j.ajog.2016.09.076