Cardiovascular events following pregnancy complicated by pre-eclampsia with emphasis on comparison between early- and late-onset forms: systematic review and meta-analysis

A Dall'Asta, F D'Antonio, G Saccone, D Buca, E Mastantuoni, M Liberati, M E Flacco, T Frusca, T Ghi, A Dall'Asta, F D'Antonio, G Saccone, D Buca, E Mastantuoni, M Liberati, M E Flacco, T Frusca, T Ghi

Abstract

Objective: To elucidate whether pre-eclampsia (PE) and the gestational age at onset of the disease (early- vs late-onset PE) have an impact on the risk of long-term maternal cardiovascular complications.

Methods: MEDLINE, EMBASE and Scopus databases were searched until 15 April 2020 for studies evaluating the incidence of cardiovascular events in women with a history of PE, utilizing combinations of the relevant MeSH terms, keywords and word variants for 'pre-eclampsia', 'cardiovascular disease' and 'outcome'. Inclusion criteria were cohort or case-control design, inclusion of women with a diagnosis of PE at the time of the first pregnancy, and sufficient data to compare each outcome in women with a history of PE vs women with previous normal pregnancy and/or in women with a history of early- vs late-onset PE. The primary outcome was a composite score of maternal cardiovascular morbidity and mortality, including cardiovascular death, major cardiovascular and cerebrovascular events, hypertension, need for antihypertensive therapy, Type-2 diabetes mellitus, dyslipidemia and metabolic syndrome. Secondary outcomes were the individual components of the primary outcome analyzed separately. Data were combined using a random-effects generic inverse variance approach. MOOSE guidelines and the PRISMA statement were followed.

Results: Seventy-three studies were included. Women with a history of PE, compared to those with previous normotensive pregnancy, had a higher risk of composite adverse cardiovascular outcome (odds ratio (OR), 2.05 (95% CI, 1.9-2.3)), cardiovascular death (OR, 2.18 (95% CI, 1.8-2.7)), major cardiovascular events (OR, 1.80 (95% CI, 1.6-2.0)), hypertension (OR, 3.93 (95% CI, 3.1-5.0)), need for antihypertensive medication (OR, 4.44 (95% CI, 2.4-8.2)), dyslipidemia (OR, 1.32 (95% CI, 1.3-1.4)), Type-2 diabetes (OR, 2.14 (95% CI, 1.5-3.0)), abnormal renal function (OR, 3.37 (95% CI, 2.3-5.0)) and metabolic syndrome (OR, 4.30 (95% CI, 2.6-7.1)). Importantly, the strength of the associations persisted when considering the interval (< 1, 1-10 or > 10 years) from PE to the occurrence of these outcomes. When stratifying the analysis according to gestational age at onset of PE, women with previous early-onset PE, compared to those with previous late-onset PE, were at higher risk of composite adverse cardiovascular outcome (OR, 1.75 (95% CI, 1.0-3.0)), major cardiovascular events (OR, 5.63 (95% CI, 1.5-21.4)), hypertension (OR, 1.48 (95% CI, 1.3-1.7)), dyslipidemia (OR, 1.51 (95% CI, 1.3-1.8)), abnormal renal function (OR, 1.52 (95% CI, 1.1-2.2)) and metabolic syndrome (OR, 1.66 (95% CI, 1.1-2.5).

Conclusions: Both early- and late-onset PE represent risk factors for maternal adverse cardiovascular events later in life. Early-onset PE is associated with a higher burden of cardiovascular morbidity and mortality compared to late-onset PE. © 2020 International Society of Ultrasound in Obstetrics and Gynecology.

Keywords: cardiovascular disease; dyslipidemia; hypertension; intrauterine growth restriction; obesity; preterm birth.

© 2020 International Society of Ultrasound in Obstetrics and Gynecology.

References

REFERENCES

    1. World Health Organization (WHO). Make every mother and child count. World Health Report 2005. WHO Press: Geneva, 2005.
    1. Barton JR, Sibai BM. Prediction and prevention of recurrent preeclampsia. Obstet Gynecol 2008; 112: 359-372.
    1. Sibai BM. Prevention of preeclampsia: a big disappointment. Am J Obstet Gynecol 1998; 179: 1275-1278.
    1. Buddeberg BS, Sharma R, O'Driscoll JM, Kaelin Agten A, Khalil A, Thilaganathan B. Cardiac maladaptation in term pregnancies with preeclampsia. Pregnancy Hypertens 2018; 13: 198-203.
    1. Mol BWJ, Roberts CT, Thangaratinam S, Magee LA, de Groot CJM, Hofmeyr GJ. Pre-eclampsia. Lancet 2016; 387: 999-1011.
    1. Steegers EA, von Dadelszen P, Duvekot JJ, Pijnenborg R. Pre-eclampsia. Lancet 2010; 376: 631-644.
    1. Foo FL, Mahendru AA, Masini G, Fraser A, Cacciatore S, MacIntyre DA, McEniery CM, Wilkinson IB, Bennett PR, Lees CC. Association Between Prepregnancy Cardiovascular Function and Subsequent Preeclampsia or Fetal Growth Restriction. Hypertension 2018; 72: 442-450.
    1. Lees CC, Marlow N, van Wassenaer-Leemhuis A, Arabin B, Bilardo CM, Brezinka C, Calvert S, Derks JB, Diemert A, Duvekot JJ, Ferrazzi E, Frusca T, Ganzevoort W, Hecher K, Martinelli P, Ostermayer E, Papageorghiou AT, Schlembach D, Schneider KT, Thilaganathan B, Todros T, Valcamonico A, Visser GH, Wolf H; TRUFFLE study group. 2 year neurodevelopmental and intermediate perinatal outcomes in infants with very preterm fetal growth restriction (TRUFFLE): a randomised trial. Lancet 2015; 385: 2162-2172.
    1. Valensise H, Vasapollo B, Gagliardi G, Novelli GP. Early and late preeclampsia: two different maternal hemodynamic states in the latent phase of the disease. Hypertension 2008; 52: 873-880.
    1. 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 2007; 335: 974.
    1. 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.
    1. Irgens HU, Reisaeter L, Irgens LM, Lie RT. Long term mortality of mothers and fathers after pre-eclampsia: population based cohort study. BMJ 2001; 323: 1213-1217.
    1. McDonald SD, Malinowski A, Zhou Q, Yusuf S, Devereaux PJ. Cardiovascular sequelae of preeclampsia/eclampsia: a systematic review and meta-analyses. Am Heart J 2008; 156: 918-930.
    1. Ahmed R, Dunford J, Mehran R, Robson S, Kunadian V. Pre-eclampsia and future cardiovascular risk among women: a review. J Am Coll Cardiol 2014; 63: 1815-1822.
    1. Bello N, Rendon ISH, Arany Z. The relationship between pre-eclampsia and peripartum cardiomyopathy: a systematic review and meta-analysis. J Am Coll Cardiol 2013; 62: 1715-1723.
    1. Grandi SM, Filion KB, Yoon S, Ayele HT, Doyle CM, Hutcheon JA, Smith GN, Gore GC, Ray JG, Nerenberg K, Platt RW. Cardiovascular Disease-Related Morbidity and Mortality in Women With a History of Pregnancy Complications. Circulation 2019; 139: 1069-1079.
    1. Weissgerber TL, Milic NM, Milin-Lazovic JS, Garovic VD. Impaired Flow-Mediated Dilation Before, During, and After Preeclampsia: A Systematic Review and Meta-Analysis. Hypertension 2016; 67: 415-423.
    1. Milic NM, Milin-Lazovic J, Weissgerber TL, Trajkovic G, White WM, Garovic VD. Preclinical atherosclerosis at the time of pre-eclamptic pregnancy and up to 10 years postpartum: systematic review and meta-analysis. Ultrasound Obstet Gynecol 2017; 49: 110-115.
    1. Wu P, Haththotuwa R, Kwok CS, Babu A, Kotronias RA, Rushton C, Zaman A, Fryer AA, Kadam U, Chew-Graham CA, Mamas MA. Preeclampsia and Future Cardiovascular Health: A Systematic Review and Meta-Analysis. Circ Cardiovasc Qual Outcomes 2017; 10: e003497.
    1. Riise HK, Sulo G, Tell GS, Igland J, Nygård O, Vollset SE, Iversen AC, Austgulen R, Daltveit AK. Incident Coronary Heart Disease After Preeclampsia: Role of Reduced Fetal Growth, Preterm Delivery, and Parity. J Am Heart Assoc 2017; 6: e004158.
    1. Lykke JA, Langhoff-Roos J, Sibai BM, Funai EF, Triche EW, Paidas MJ. Hypertensive pregnancy disorders and subsequent cardiovascular morbidity and type 2 diabetes mellitus in the mother. Hypertension 2009; 53: 944-951.
    1. Brown MA, Magee LA, Kenny LC, Karumanchi SA, McCarthy FP, Saito S, Hall DR, Warren CE, Adoyi G, Ishaku S; International Society for the Study of Hypertension in Pregnancy (ISSHP). Hypertensive Disorders of Pregnancy: ISSHP Classification, Diagnosis, and Management Recommendations for International Practice. Hypertension 2018; 72: 24-43.
    1. Muntner P, Carey RM, Gidding S, Jones DW, Taler SJ, Wright JT Jr, Whelton PK. Potential US Population Impact of the 2017 ACC/AHA High Blood Pressure Guideline. Circulation 2018; 137: 109-118.
    1. Kerner W, Brückel J; German Diabetes Association. Definition, classification and diagnosis of diabetes mellitus. Exp Clin Endocrinol Diabetes 2014; 122: 384-386.
    1. Grundy SM, Stone NJ, Bailey AL, Beam C, Birtcher KK, Blumenthal RS, Braun LT, de Ferranti S, Faiella-Tommasino J, Forman DE, Goldberg R, Heidenreich PA, Hlatky MA, Jones DW, Lloyd-Jones D, Lopez-Pajares N, Ndumele CE, Orringer CE, Peralta CA, Saseen JJ, Smith SC Jr, Sperling L, Virani SS, Yeboah J. 2018 AHA/ACC/AACVPR/AAPA/ABC/ACPM/ADA/AGS/APhA/ASPC/NLA/PCNA Guideline on the Management of Blood Cholesterol: A Report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines. J Am Coll Cardiol 2019; 73: e285-350.
    1. Grundy SM, Cleeman JI, Daniels SR, Donato KA, Eckel RH, Franklin BA, Gordon DJ, Krauss RM, Savage PJ, Smith SC Jr, Spertus JA, Costa F; American Heart Association; National Heart, Lung, and Blood Institute. Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation 2005; 112: 2735-2752.
    1. Wells GA, Shea B, O'Connell D, Peterson J, Welch V, Losos M, Tugwell P. The Newcastle-Ottawa Scale for assessing the quality of nonrandomised studies in meta-analyses. .
    1. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, Moher D, Becker BJ, Sipe TA, Thacker SB. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 2000; 283: 2008-2012.
    1. Moher D, Shamseer L, Clarke M, Ghersi D, Liberati A, Petticrew M, Shekelle P, Stewart LA, PRISMA-P Group. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst Rev 2015; 4: 1.
    1. Callaway LK, Lawlor DA, O'Callaghan M, Williams GM, Najman JM, McIntyre HD. Diabetes mellitus in the 21 years after a pregnancy that was complicated by hypertension: findings from a prospective cohort study. Am J Obstet Gynecol 2007; 197: 492e1-7.
    1. Callaway LK, David McIntyre H, Williams GM, Najman JM, Lawlor DA, Mamun A. Diagnosis and treatment of hypertension 21 years after a hypertensive disorder of pregnancy. Aust N Z J Obstet Gynaecol 2011; 51: 437-440.
    1. Thornton C, Dahlen H, Korda A, Hennessy A. The incidence of preeclampsia and eclampsia and associated maternal mortality in Australia from population-linked datasets: 2000-2008. Am J Obstet Gynecol 2013; 208: 476e1-5.
    1. Tooher J, Thornton C, Makris A, Ogle R, Korda A, Hennessy A. All Hypertensive Disorders of Pregnancy Increase the Risk of Future Cardiovascular Disease. Hypertension 2017; 70: 798-803.
    1. Forest JC, Girouard J, Masse J, Moutquin JM, Kharfi A, Ness RB, Roberts JM, Giguere Y. Early occurrence of metabolic syndrome after hypertension in pregnancy. Obstet Gynecol 2005; 105: 1373-1380.
    1. Ray JG, Vermeulen MJ, Schull MJ, Redelmeier DA. Cardiovascular health after maternal placental syndromes (CHAMPS): population-based retrospective cohort study. Lancet 2005; 366: 1797-1803.
    1. Smith GN, Pudwell J, Walker M, Wen SW. Risk estimation of metabolic syndrome at one and three years after a pregnancy complicated by preeclampsia. J Obstet Gynaecol Can 2012; 34: 836-841.
    1. Mehrabadi A, Liu S, Bartholomew S, Hutcheon JA, Magee LA, Kramer MS, Liston RM, Joseph KS, Canadian Perinatal Surveillance System Public Health Agency of Canada Hypertensive disorders of pregnancy and the recent increase in obstetric acute renal failure in Canada: population based retrospective cohort study. BMJ 2014; 349: g4731.
    1. Grandi SM, Vallee-Pouliot K, Reynier P, Eberg M, Platt RW, Arel R, Basso O, Filion KB. Hypertensive Disorders in Pregnancy and the Risk of Subsequent Cardiovascular Disease. Paediatr Perinat Epidemiol 2017; 31: 412-421.
    1. Dai L, Chen Y, Sun W, Liu S. Association Between Hypertensive Disorders During Pregnancy and the Subsequent Risk of End-Stage Renal Disease: A Population-Based Follow-Up Study. J Obstet Gynaecol Can 2018; 40: 1129-1138.
    1. Langlois AWR, Park AL, Lentz EJM, Ray JG. Preeclampsia Brings the Risk of Premature Cardiovascular Disease in Women Closer to That of Men. Can J Cardiol 2020; 36: 60-68.
    1. Lykke JA, Langhoff-Roos J, Lockwood CJ, Triche EW, Paidas MJ. Mortality of mothers from cardiovascular and non-cardiovascular causes following pregnancy complications in first delivery. Paediatr Perinat Epidemiol 2010; 24: 323-330.
    1. Behrens I, Basit S, Melbye M, Lykke JA, Wohlfahrt J, Bundgaard H, Thilaganathan B, Boyd HA. Risk of post-pregnancy hypertension in women with a history of hypertensive disorders of pregnancy: nationwide cohort study. BMJ 2017; 358: j3078.
    1. Kristensen JH, Basit S, Wohlfahrt J, Damholt MB, Boyd HA. Pre-eclampsia and risk of later kidney disease: nationwide cohort study. BMJ 2019; 365: l1516.
    1. Haukkamaa L, Salminen M, Laivuori H, Leinonen H, Hiilesmaa V, Kaaja R. Risk for subsequent coronary artery disease after preeclampsia. Am J Cardiol 2004; 93: 805-808.
    1. Mannisto T, Mendola P, Vaarasmaki M, Järvelin MR, Hartikainen AL, Pouta A, Suvanto E. Elevated blood pressure in pregnancy and subsequent chronic disease risk. Circulation 2013; 127: 681-690.
    1. Hubel CA, Snaedal S, Ness RB, Weissfeld LA, Geirsson RT, Roberts JM, Arngrimsson R. Dyslipoproteinaemia in postmenopausal women with a history of eclampsia. BJOG 2000; 107: 776-784.
    1. Funai EF, Friedlander Y, Paltiel O, Tiram E, Xue X, Deutsch L, Harlap S. Long-term mortality after preeclampsia. Epidemiology 2005; 16: 206-215.
    1. Kessous R, Shoham-Vardi I, Pariente G, Sergienko R, Sheiner E. Long-term maternal atherosclerotic morbidity in women with pre-eclampsia. Heart 2015; 101: 442-446.
    1. Blaauw J, van Pampus MG, Van Doormaal JJ, Fokkema MR, Fidler V, Smit AJ, Aarnoudse JG. Increased intima-media thickness after early-onset preeclampsia. Obstet Gynecol 2006; 107: 1345-1351.
    1. Gaugler-Senden IP, Berends AL, de Groot CJ, Steegers EA. Severe, very early onset preeclampsia: subsequent pregnancies and future parental cardiovascular health. Eur J Obstet Gynecol Reprod Biol 2008; 140: 171-177.
    1. Nijdam ME, Timmerman MR, Franx A, Bruinse HW, Numans ME, Grobbee DE, Bots ML. Cardiovascular risk factor assessment after pre-eclampsia in primary care. BMC Fam Pract 2009; 10: 77.
    1. Stekkinger E, Zandstra M, Peeters LL, Spaanderman ME. Early-onset preeclampsia and the prevalence of postpartum metabolic syndrome. Obstet Gynecol 2009; 114: 1076-1084.
    1. Aukes AM, De Groot JC, Wiegman MJ, Aarnoudse JG, Sanwikarja GS, Zeeman GG. Long-term cerebral imaging after pre-eclampsia. BJOG 2012; 119: 1117-1122.
    1. Hermes W, Franx A, van Pampus MG, Bloemenkamp KWM, Bots ML, van der Post JA, Porath M, Ponjee GAE, Tamsma JT, Mol BWJ, de Groot CJM. Cardiovascular risk factors in women who had hypertensive disorders late in pregnancy: a cohort study. Am J Obstet Gynecol 2013; 208: 474e1-8.
    1. Scholten RR, Hopman MT, Sweep FC, Van de Vlugt MJ, Van Dijk AP, Oyen VJ, Lotgering FK, Spaanderman MEA. Co-occurrence of cardiovascular and prothrombotic risk factors in women with a history of preeclampsia. Obstet Gynecol 2013; 121: 97-105.
    1. Veerbeek JH, Hermes W, Breimer AY, van Rijn BB, Koenen SV, Mol BW, Franx A, de Groot CJM, Koster MPH. Cardiovascular disease risk factors after early-onset preeclampsia, late-onset preeclampsia, and pregnancy-induced hypertension. Hypertension 2015; 65: 600-606.
    1. van Rijn BB, Bruinse HW, Veerbeek JH, Uiterweer EDP, Koenen SV, van der Bom JG, Rijkers GT, Roest M, Franx A. Postpartum Circulating Markers of Inflammation and the Systemic Acute-Phase Response After Early-Onset Preeclampsia. Hypertension 2016; 67: 404-414.
    1. Bokslag A, Teunissen PW, Franssen C, van Kesteren F, Kamp O, Ganzevoort W, Paulus WJ, de Groot CJM. Effect of early-onset preeclampsia on cardiovascular risk in the fifth decade of life. Am J Obstet Gynecol 2017; 216: 523e1-7.
    1. Vikse BE, Irgens LM, Leivestad T, Skjaerven R, Iversen BM. Preeclampsia and the risk of end-stage renal disease. N Engl J Med 2008; 359: 800-809.
    1. 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.
    1. Andersgaard AB, Acharya G, Mathiesen EB, Johnsen SH, Straume B, Oian P. Recurrence and long-term maternal health risks of hypertensive disorders of pregnancy: a population-based study. Am J Obstet Gynecol 2012; 206: 143e1-8.
    1. Skjaerven R, Wilcox AJ, Klungsoyr K, Irgens LM, Vikse BE, Vatten LJ, Terje Lie R. Cardiovascular mortality after pre-eclampsia in one child mothers: prospective, population based cohort study. BMJ 2012; 345: e7677.
    1. Egeland GM, Skurtveit S, Staff AC, Eide GE, Daltveit AK, Klungsøyr K, Trogstad L, Magnus PM, Brantsaeter AL, Haugen M. Pregnancy-Related Risk Factors Are Associated With a Significant Burden of Treated Hypertension Within 10 Years of Delivery: Findings From a Population-Based Norwegian Cohort. J Am Heart Assoc 2018; 7: e008318.
    1. Wikstrom AK, Haglund B, Olovsson M, Lindeberg SN. The risk of maternal ischaemic heart disease after gestational hypertensive disease. BJOG 2005; 112: 1486-1491.
    1. Nelander M, Cnattingius S, Akerud H, Wikstrom J, Pedersen NL, Wikstrom AK. Pregnancy hypertensive disease and risk of dementia and cardiovascular disease in women aged 65 years or older: a cohort study. BMJ Open 2016; 6: e009880.
    1. Khashan AS, Evans M, Kublickas M, McCarthy FP, Kenny LC, Stenvinkel P, Fitzgerald T, Kublickiene K. Preeclampsia and risk of end stage kidney disease: A Swedish nationwide cohort study. PLoS Med 2019; 16: e1002875.
    1. Tang CH, Wu CS, Lee TH, Hung ST, Yang CYC, Lee CH, Chu PH. Preeclampsia-eclampsia and the risk of stroke among peripartum in Taiwan. Stroke 2009; 40: 1162-1168.
    1. Lin YS, Tang CH, Yang CY, Wu LS, Hung ST, Hwa HL, Chu PH. Effect of pre-eclampsia-eclampsia on major cardiovascular events among peripartum women in Taiwan. Am J Cardiol 2011; 107: 325-330.
    1. Wu CC, Chen SH, Ho CH, Liang FW, Chu CC, Wang HY, Lu YH. End-stage renal disease after hypertensive disorders in pregnancy. Am J Obstet Gynecol 2014; 210: 147e1-8.
    1. Yeh JS, Cheng HM, Hsu PF, Sung SH, Liu WL, Fang HL, Chuang SY. Synergistic effect of gestational hypertension and postpartum incident hypertension on cardiovascular health: a nationwide population study. J Am Heart Assoc 2014; 3: e001008.
    1. Kuo YL, Chan TF, Wu CY, Ker CR, Tu HP. Preeclampsia-eclampsia and future cardiovascular risk among women in Taiwan. Taiwan J Obstet Gynecol 2018; 57: 364-369.
    1. Hannaford P, Ferry S, Hirsch S. Cardiovascular sequelae of toxaemia of pregnancy. Heart 1997; 77: 154-158.
    1. Melchiorre K, Sutherland GR, Liberati M, Thilaganathan B. Preeclampsia is associated with persistent postpartum cardiovascular impairment. Hypertension 2011; 58: 709-715.
    1. Bhattacharya S, Prescott GJ, Iversen L, Campbell DM, Smith WC, Hannaford PC. Hypertensive disorders of pregnancy and future health and mortality: A record linkage study. Pregnancy Hypertens 2012; 2: 1-7.
    1. Leon LJ, McCarthy FP, Direk K, Gonzalez-Izquierdo A, Prieto-Merino D, Casas JP, Chappell L. Preeclampsia and Cardiovascular Disease in a Large UK Pregnancy Cohort of Linked Electronic Health Records: A CALIBER Study. Circulation 2019; 140: 1050-1060.
    1. Thorogood M, Mann J, Murphy M, Vessey M. Fatal stroke and use of oral contraceptives: findings from a case-control study. Am J Epidemiol 1992; 136: 35-45.
    1. Mann JI, Doll R, Thorogood M, Vessey MP, Waters WE. Risk factors for myocardial infarction in young women. Br J Prev Soc Med 1976; 30: 94-100.
    1. Fraser A, Nelson SM, Macdonald-Wallis C, Cherry C, Butler E, Sattar N, Lawlor DA. Associations of pregnancy complications with calculated cardiovascular disease risk and cardiovascular risk factors in middle age: the Avon Longitudinal Study of Parents and Children. Circulation 2012; 125: 1367-1380.
    1. Smith GC, Pell JP, Walsh D. Pregnancy complications and maternal risk of ischaemic heart disease: a retrospective cohort study of 129,290 births. Lancet 2001; 357: 2002-2006.
    1. Wilson BJ, Watson MS, Prescott GJ, Sunderland S, Campbell DM, Hannaford P, Smith WCS. Hypertensive diseases of pregnancy and risk of hypertension and stroke in later life: results from cohort study. BMJ 2003; 326: 845.
    1. Libby G, Murphy DJ, McEwan NF, Greene SA, Forsyth JS, Chien PW, Morris AD, DARTS/MEMO Collaboration. Pre-eclampsia and the later development of type 2 diabetes in mothers and their children: an intergenerational study from the Walker cohort. Diabetologia 2007; 50: 523-530.
    1. Ayansina D, Black C, Hall SJ, Marks A, Millar C, Prescott GJ, Wilde K, Bhattacharya S. Long term effects of gestational hypertension and pre-eclampsia on kidney function: Record linkage study. Pregnancy Hypertens 2016; 6: 344-349.
    1. Rosenberg L, Miller DR, Kaufman DW, Helmrich SP, Van de Carr S, Stolley PD, Shapiro S. Myocardial infarction in women under 50 years of age. JAMA 1983; 250: 2801-2806.
    1. Kestenbaum B, Seliger SL, Easterling TR, Gillen DL, Critchlow CW, Stehman-Breen CO, Schwartz SM. Cardiovascular and thromboembolic events following hypertensive pregnancy. Am J Kidney Dis 2003; 42: 982-989.
    1. Brown DW, Dueker N, Jamieson DJ, Cole JW, Wozniak MA, Stern BJ, Giles WH, Kittner SJ. Preeclampsia and the risk of ischemic stroke among young women: results from the Stroke Prevention in Young Women Study. Stroke 2006; 37: 1055-1059.
    1. Edlow AG, Srinivas SK, Elovitz MA. Investigating the risk of hypertension shortly after pregnancies complicated by preeclampsia. Am J Obstet Gynecol 2009; 200: e60-62.
    1. Srinivas SK, Sammel MD, Bastek J, Ofori E, Andrela CM, Wolfe ML, Reilly M, Elovitz MA. Evaluating the association between all components of the metabolic syndrome and pre-eclampsia. J Matern Fetal Neonatal Med 2009; 22: 501-509.
    1. Mongraw-Chaffin ML, Cirillo PM, Cohn BA. Preeclampsia and cardiovascular disease death: prospective evidence from the child health and development studies cohort. Hypertension 2010; 56: 166-171.
    1. Hovsepian DA, Sriram N, Kamel H, Fink ME, Navi BB. Acute cerebrovascular disease occurring after hospital discharge for labor and delivery. Stroke 2014; 45: 1947-1950.
    1. Savitz DA, Danilack VA, Elston B, Lipkind HS. Pregnancy-induced hypertension and diabetes and the risk of cardiovascular disease, stroke, and diabetes hospitalization in the year following delivery. Am J Epidemiol 2014; 180: 41-44.
    1. Cirillo PM, Cohn BA. Pregnancy complications and cardiovascular disease death: 50-year follow-up of the Child Health and Development Studies pregnancy cohort. Circulation 2015; 132: 1234-1242.
    1. Black MH, Zhou H, Sacks DA, Dublin S, Lawrence JM, Harrison TN, Reynolds N. Hypertensive disorders first identified in pregnancy increase risk for incident prehypertension and hypertension in the year after delivery. J Hypertens 2016; 34: 728-735.
    1. Cain MA, Salemi JL, Tanner JP, Kirby RS, Salihu HM, Louis JM. Pregnancy as a window to future health: maternal placental syndromes and short-term cardiovascular outcomes. Am J Obstet Gynecol 2016; 215: 484e1-14.
    1. White WM, Mielke MM, Araoz PA, Lahr BD, Bailey KR, Jayachandran M, Miller VM, Garovic VD. A history of preeclampsia is associated with a risk for coronary artery calcification 3 decades later. Am J Obstet Gynecol 2016; 214: 519e1-18.
    1. Best LG, Lunday L, Webster E, Falcon GR, Beal JR. Pre-eclampsia and risk of subsequent hypertension: in an American Indian population. Hypertens Pregnancy 2017; 36: 131-137.
    1. Kattah AG, Scantlebury DC, Agarwal S, Mielke MM, Rocca WA, Weaver AL, Vaughan LE, Miller VM, Weissgerber TL, White W, Garovic VD. Preeclampsia and ESRD: The Role of Shared Risk Factors. Am J Kidney Dis 2017; 69: 498-505.
    1. Stuart JJ, Tanz LJ, Missmer SA, Rimm EB, Spiegelman D, James-Todd TM, Rich-Edwards JM. Hypertensive Disorders of Pregnancy and Maternal Cardiovascular Disease Risk Factor Development: An Observational Cohort Study. Ann Intern Med 2018; 169: 224-232.
    1. Ackerman CM, Platner MH, Spatz ES, Illuzzi JL, Xu X, Campbell KH, Smith GN, Paidas MJ, Lipkind HS. Severe cardiovascular morbidity in women with hypertensive diseases during delivery hospitalization. Am J Obstet Gynecol 2019; 220: 582e1-11.
    1. Haas DM, Parker CB, Marsh DJ, Grobman WA, Ehrenthal DB, Greenland P, Bairey Merz CN, Pemberton VL, Silver RM, Barnes S, McNeil RB, Cleary K, Reddy UM, Chung JH, Parry S, Theilen LH, Blumenthal EA, Levine LD, Mercer BM, Simhan H, Polito LA, Wapner RJ, Catov J, Chen I, Saade GR, NHLBI nuMoM2b Heart Health Study. Association of Adverse Pregnancy Outcomes With Hypertension 2 to 7 Years Postpartum. J Am Heart Assoc 2019; 8: e013092.
    1. Haukkamaa L, Moilanen L, Kattainen A, Luoto R, Kahonen M, Leinonen M, Jula A, Kesäniemi YA, Kaaja R. Pre-eclampsia is a risk factor of carotid artery atherosclerosis. Cerebrovasc Dis. 2009; 27: 599-607.
    1. Buurma AJ, Turner RJ, Driessen JH, Mooyaart AL, Schoones JW, Bruijn JA, Bloemenkamp KWM, Dekkers OM, Baelde HJ. Genetic variants in pre-eclampsia: a meta-analysis. Hum Reprod Update. 2013;19(3):289-303. doi:10.1093/humupd/dms060
    1. Kazmi N, Sharp GC, Reese SE, Vehmeijer FO, Lahti J, Page CM, Zhang W, Rifas-Shiman SL, Rezwan FI, Simpkin AJ, Burrows K, Richardson TG, Santos Ferreira DL, Fraser A, Harmon QE, Zhao S, Jaddoe VWV, Czamara D, Binder EB, Magnus MC, Håberg SE, Nystad W, Nohr EA, Starling AP, Kechris KJ, Yang IV, DeMeo DL, Litonjua AA, Baccarelli A, Oken E, Holloway JW, Karmaus W, Arshad SH, Dabelea D, Sørensen TIA, Laivuori H, Raikkonen K, Felix JF, London SJ, Hivert MF, Gaunt TR, Lawlor DA, Relton CL. Hypertensive Disorders of Pregnancy and DNA Methylation in Newborns. Hypertension 2019; 74: 375-383.
    1. Lazdam M, de la Horra A, Diesch J, Kenworthy Y, Davis E, Lewandowski AJ, Szmigielski C, Shore A, Mackillop L, Kharbanda R, Alp N, Redman C, Kelly B, Leeson P. Unique blood pressure characteristics in mother and offspring after early onset preeclampsia. Hypertension 2012; 60: 1338-1345.
    1. Wright D, Wright A, Nicolaides KH. The competing risk approach for prediction of preeclampsia. Am J Obstet Gynecol 2020; 223: 12-23.e7.
    1. Wright D, Tan MY, O'Gorman N, Poon LC, Syngelaki A, Wright A, Nicolaides KH. Predictive performance of the competing risk model in screening for preeclampsia. Am J Obstet Gynecol 2019; 220: 199.e1-13.
    1. Chen CW, Jaffe IZ, Karumanchi SA. Pre-eclampsia and cardiovascular disease. Cardiovasc Res 2014; 101: 579-586.
    1. Rodie VA, Freeman DJ, Sattar N, Greer IA. Pre-eclampsia and cardiovascular disease: metabolic syndrome of pregnancy? Atherosclerosis 2004; 175: 189-202.
    1. van Rijn BB, Nijdam ME, Bruinse HW, Roest M, Uiterwaal CS, Grobbee DE, Bots ML, Franx A. Cardiovascular disease risk factors in women with a history of early-onset preeclampsia. Obstet Gynecol 2013; 121: 1040-1048.
    1. Walsh SW. Obesity: a risk factor for preeclampsia. Trends Endocrinol Metab 2007; 18: 365-370.
    1. Ford CA, Nonnemaker JM, Wirth KE. The influence of adolescent body mass index, physical activity, and tobacco use on blood pressure and cholesterol in young adulthood. J Adolesc Health 2008; 43: 576-583.
    1. Shroff R, Kerchner A, Maifeld M, Van Beek EJ, Jagasia D, Dokras A. Young obese women with polycystic ovary syndrome have evidence of early coronary atherosclerosis. J Clin Endocrinol Metab 2007; 92: 4609-4614.
    1. O'Brien TE, Ray JG, Chan WS. Maternal body mass index and the risk of preeclampsia: a systematic overview. Epidemiology 2003; 14: 368-374.
    1. Lloyd-Jones D, Adams RJ, Brown TM, Carnethon M, Dai S, De Simone G, Ferguson TB, Ford E, Furie K, Gillespie C, Go A, Greenlund K, Haase N, Hailpern S, Ho PM, Howard V, Kissela B, Kittner S, Lackland D, Lisabeth L, Marelli A, McDermott MM, Meigs J, Mozaffarian D, Mussolino M, Nichol G, Roger V, Rosamond W, Sacco R, Sorlie P, Stafford R, Thom T, Wasserthiel-Smoller S, Wong ND, Wylie-Rosett J. Heart disease and stroke statistics; 2010 update. A report from the American Heart Association. Circulation 2010; 121: e46-215.
    1. Wu P, Kwok CS, Haththotuwa R, Kotronias RA, Babu A, Fryer AA, Myint PK, Chew-Graham CA, Mamas MA. Pre-eclampsia is associated with a twofold increase in diabetes: a systematic review and meta-analysis. Diabetologia 2016; 59: 2518-2526.
    1. Visser S, Hermes W, Ket JC, Otten RHJ, van Pampus MG, Bloemenkamp KWM, Franx A, Mol BW, de Groot CJM. Systematic review and metaanalysis on nonclassic cardiovascular biomarkers after hypertensive pregnancy disorders. Am J Obstet Gynecol 2014; 211: 373.e1-9.
    1. Ferrazzi E, Zullino S, Stampalija T, Vener C, Cavoretto P, Gervasi MT, Vergani P, Mecacci F, Marozio L, Oggè G, Algeri P, Ruffatti A, Milani S, Todros T. Bedside diagnosis of two major clinical phenotypes of hypertensive disorders of pregnancy. Ultrasound Obstet Gynecol 2016; 48: 224-231.
    1. Ferrazzi E, Stampalija T, Monasta L, Di Martino D, Vonck S, Gyselaers W. Maternal hemodynamics: a method to classify hypertensive disorders of pregnancy. Am J Obstet Gynecol 2018; 218: 124.e1-11.
    1. Tay J, Foo L, Masini G, Bennett PR, McEniery CM, Wilkinson IB, Lees CC. Early and late preeclampsia are characterized by high cardiac output, but in the presence of fetal growth restriction, cardiac output is low: insights from a prospective study. Am J Obstet Gynecol 2018; 218: 517.e1-12.
    1. Brouwers L, van der Meiden-van Roest AJ, Savelkoul C, Vogelvang TE, Lely AT, Franx A, van Rijn BB. Recurrence of pre-eclampsia and the risk of future hypertension and cardiovascular disease: a systematic review and meta-analysis. BJOG 2018; 125: 1642-1654.

Source: PubMed

Patrocinadores e Colaboradores

Condições médicas

Intervenções de drogas

3
Se inscrever