Miscarriage and future maternal cardiovascular disease: a systematic review and meta-analysis
Open accessAbstract
Context: The 2011 American Heart Association guidelines identified pregnancy complications as a risk factor for cardiovascular disease in women. However, miscarriage was not mentioned within the guidelines, and there is no consensus on the association between miscarriage and future risk of cardiovascular disease. Objective: To confirm or refute the association, a meta-analysis of published papers was conducted. Data sources: PubMed, Web of Knowledge and Scopus were systematically searched to identify appropriate articles. Reference lists were then hand searched for additional relevant titles. Study Selection: To be included, articles had to assess the association between miscarriage and subsequent cardiovascular disease in otherwise healthy women. Only women who had miscarriages were considered exposed. Pooled association measures, using random effects meta-analysis, were calculated for coronary heart disease and cerebrovascular disease. Publication bias and between-study heterogeneity were evaluated. Data Extraction: Two authors individually reviewed all studies and extracted data on patient and study characteristics along with cardiovascular outcomes. Results: 10 studies were identified, with 517 504 individuals included in the coronary heart disease meta-analysis and 134 461 individuals in the cerebrovascular disease analysis. A history of miscarriage was associated with a greater odds of developing coronary heart disease, OR (95% CI) =1.45 (1.18 to 1.78), but not with cerebrovascular disease, OR=1.11 (0.72 to 1.69). There was a strong association between recurrent miscarriage and coronary heart disease OR=1.99 (1.13 to 3.50). Evidence was found for moderate between-study heterogeneity and publication bias in the coronary heart disease analysis. Conclusions: The meta-analysis indicates that a history of miscarriage or recurrent miscarriage is associated with a greater risk of subsequent coronary heart disease.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In a review exploring individual cardiovascular diseases, miscarriage is not linked to a higher risk of stroke.
“In a review exploring individual cardiovascular diseases, miscarriage was linked to a higher risk of ischaemic heart disease but not of stroke.98”
From Association between the reproductive health of young women and cardiovascular disease in later life: umbrella review (2020) · cites this paper as [98]
In a review exploring individual cardiovascular diseases, miscarriage is linked to a higher risk of ischaemic heart disease.
“In a review exploring individual cardiovascular diseases, miscarriage was linked to a higher risk of ischaemic heart disease but not of stroke.98”
From Association between the reproductive health of young women and cardiovascular disease in later life: umbrella review (2020) · cites this paper as [98]
Incorporating the results of the Danish cohort study into the meta-analysis on risk of stroke with the existing systematic review did not alter the significance of the association between miscarriage and stroke.
“Incorporating the results in the meta-analysis on the risk of stroke with those of the existing systematic review98 did not alter the significance of the association between miscarriage and stroke.”
From Association between the reproductive health of young women and cardiovascular disease in later life: umbrella review (2020) · cites this paper as [98]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Stang, A. (2010) · European Journal of Epidemiology · doi:10.1007/s10654-010-9491-z · Cited by 17,396 · see citing works
Ahmed, A., Jorna, T., & Bhandari, S. (2016) · The Nephron journals/Nephron journals · doi:10.1159/000447068 · Cited by 11,782 · see citing works
Tsokos, G. C. (2016) · Elsevier eBooks · doi:10.1016/b978-0-323-37754-6.50094-4 · Cited by 3,990 · see citing works
Sarnak, M. J., Levey, A. S., Schoolwerth, A. C., Coresh, J., Culleton, B., Hamm, L. L., McCullough, P. A., Kasiske, B. L., Kelepouris, E., Klag, M. J., et al. (2003) · Circulation · doi:10.1161/01.cir.0000095676.90936.80 · Cited by 3,768 · see citing works
Tsokos, G. C. (2011) · New England Journal of Medicine · doi:10.1056/nejmra1100359 · Cited by 2,747 · see citing works
Bellamy, L., Casas, J.-P., Hingorani, A. D., & Williams, D. J. (2007) · BMJ · doi:10.1136/bmj.39335.385301.be · Cited by 2,552 · see citing works
Mosca, L., Benjamin, E. J., Berra, K., Bezanson, J. L., Dolor, R. J., Lloyd-Jones, D. M., Newby, L. K., Piña, I. L., Roger, V. L., Shaw, L. J., et al. (2011) · Circulation · doi:10.1161/cir.0b013e31820faaf8 · Cited by 2,143 · see citing works
Prevalence of Conventional Risk Factors in Patients With Coronary Heart Disease
Khot, U. N. (2003) · JAMA · doi:10.1001/jama.290.7.898 · Cited by 1,494 · see citing works
Cardiovascular sequelae of preeclampsia/eclampsia: A systematic review and meta-analyses
McDonald, S. D., Malinowski, A., Zhou, Q., Yusuf, S., & Devereaux, P. J. (2008) · American Heart Journal · doi:10.1016/j.ahj.2008.06.042 · Cited by 924 · see citing works
Effectiveness-Based Guidelines for the Prevention of Cardiovascular Disease in Women—2011 Update
Mosca, L. J., Benjamin, E. J., Berra, K. A., Bezanson, J. L., Dolor, R. J., Lloyd‐Jones, D. M., Newby, L. K., Piña, I. L., Roger, V. L., Shaw, L. J., et al. (2011) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2011.02.005 · Cited by 783 · see citing works
Smyth, A., Oliveira, G. H., Lahr, B. D., Bailey, K. R., Norby, S. M., & Garovic, V. D. (2010) · Clinical Journal of the American Society of Nephrology · doi:10.2215/cjn.00240110 · Cited by 661 · see citing works
The antiphospholipid syndrome: ten years on
Hughes, G. R. V. (1993) · The Lancet · doi:10.1016/0140-6736(93)91477-4 · Cited by 628 · see citing works
Outcome of Pregnancy in Women With Congenital Heart Disease
Drenthen, W., Pieper, P. G., Roos‐Hesselink, J. W., van Lottum, W. A., Voors, A. A., Mulder, B. J. M., van Dijk, A. P. J., Vliegen, H. W., Yap, S., Moons, P., et al. (2007) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2007.03.027 · Cited by 608 · see citing works
Wang, X., Chen, C., Wang, L., Chen, D., Guang, W., & French, J. L. (2003) · Fertility and Sterility · doi:10.1016/s0015-0282(02)04694-0 · Cited by 589 · see citing works
Increased Risk of Cardiovascular Disease in Young Women Following Gestational Diabetes Mellitus
Shah, B. R., Retnakaran, R., & Booth, G. L. (2008) · Diabetes Care · doi:10.2337/dc08-0706 · Cited by 489 · see citing works
Everett, C. (1997) · BMJ · doi:10.1136/bmj.315.7099.32 · Cited by 406 · see citing works
de Groot, P. C. M., Dekkers, O. M., Romijn, J. A., Dieben, S. W. M., & Helmerhorst, F. M. (2011) · Human Reproduction Update · doi:10.1093/humupd/dmr001 · Cited by 394 · see citing works
Carr, D. B., Utzschneider, K. M., Hull, R. L., Tong, J., Wallace, T. M., Kodama, K., Shofer, J. B., Heckbert, S. R., Boyko, E. J., Fujimoto, W. Y., et al. (2006) · Diabetes Care · doi:10.2337/dc05-2482 · Cited by 350 · see citing works
Chronic kidney disease in pregnancy
Williams, D. J., & Davison, J. M. (2008) · BMJ · doi:10.1136/bmj.39406.652986.be · Cited by 319 · see citing works
THE STUDY OF WOMEN IN GOTHENBURG 1968–1969 —A POPULATION STUDY
Bengtsson, C., Blohmé, G., Hallberg, L., Hällström, T., Isaksson, B., Korsan-Bengtsen, K., Rybo, G., Tibblin, E., Tibblin, G., & Westerberg, H. (1973) · Acta Medica Scandinavica · doi:10.1111/j.0954-6820.1973.tb10583.x · Cited by 318 · see citing works
Risk factors in miscarriage: a review
García-Enguídanos, A., Calle, M. E., Valero, J. D. L. F., Luna, S., & Rojas, V. D. (2002) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(01)00613-3 · Cited by 295 · see citing works
Germain, A. M., Romanik, M. C., Guerra, I., Solari, S., Reyes, M. S., Johnson, R. J., Price, K., Karumanchi, S. A., & Valdés, G. (2007) · Hypertension · doi:10.1161/01.hyp.0000251522.18094.d4 · Cited by 275 · see citing works
Thyroid hormone and cardiovascular disease
Gomberg‐Maitland, M., & Frishman, W. H. (1998) · American Heart Journal · doi:10.1016/s0002-8703(98)70081-x · Cited by 194 · see citing works
Atherosclerotic vascular events in a multinational inception cohort of systemic lupus erythematosus
Urowitz, M. B., Gladman, D. D., Ibañez, D., Bae, S., Sanchez-Guerrero, J., Gordon, C., Clarke, A. E., Bernatsky, S., Fortin, P. R., Hanly, J. G., et al. (2010) · Arthritis Care & Research · doi:10.1002/acr.20122 · Cited by 187 · see citing works
Menstrual and Reproductive Risk Factors for Ischemic Heart Disease
Cooper, G. S., Ephross, S. A., Weinberg, C. R., Baird, D. D., Whelan, E. A., & Sandler, D. P. (1999) · Epidemiology · doi:10.1097/00001648-199905000-00011 · Cited by 162 · see citing works
Kharazmi, E., Dossus, L., Rohrmann, S., & Kaaks, R. (2010) · Heart · doi:10.1136/hrt.2010.202226 · Cited by 143 · see citing works
Tian, L., Shen, H., Lu, Q., et al. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-1123 · Cited by 140 · see citing works
Spontaneous Abortions and Major Malformations in Women with Diabetes Mellitus
Greene, M. F. (1999) · Seminars in Reproductive Medicine · doi:10.1055/s-2007-1016220 · Cited by 134 · see citing works
Lykke, J. A., Langhoff‐Roos, J., Lockwood, C. J., Triche, E. W., & Paidas, M. J. (2010) · Paediatric and Perinatal Epidemiology · doi:10.1111/j.1365-3016.2010.01120.x · Cited by 128 · see citing works
Early or Recurrent Preterm Birth and Maternal Cardiovascular Disease Risk
Catov, J. M., Wu, C. S., Olsen, J., Sutton-Tyrrell, K., Li, J., & Nohr, E. A. (2010) · Annals of Epidemiology · doi:10.1016/j.annepidem.2010.05.007 · Cited by 124 · see citing works
Jovanovic, L. G., Knopp, R. H., Kim, H. T., Cefalu, W. T., Zhu, X., Lee, Y. J., Simpson, J. L., Mills, J. L., & for the Diabetes in Early Pregnancy Study Group (2005) · Diabetes Care · doi:10.2337/diacare.28.5.1113 · Cited by 122 · see citing works
Gallagher, L. G., Davis, L. B., Ray, R. M., Psaty, B. M., Gao, D. L., Checkoway, H., & Thomas, D. B. (2011) · International Journal of Epidemiology · doi:10.1093/ije/dyr134 · Cited by 121 · see citing works
Pell, J. P. (2004) · American Journal of Epidemiology · doi:10.1093/aje/kwh064 · Cited by 108 · see citing works
Bhattacharya, S., Townend, J., Shetty, A., Campbell, D. M., & Bhattacharya, S. (2008) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.2008.01943.x · Cited by 106 · see citing works
Gholizadeh, L., & Davidson, P. M. (2007) · Health Care For Women International · doi:10.1080/07399330701723756 · Cited by 100 · see citing works
Obesity and reproduction: an educational bulletin
(2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.08.005 · Cited by 91 · see citing works
Thrombophilias and Recurrent Pregnancy Loss
Kutteh, W. H., & Triplett, D. A. (2006) · Seminars in Reproductive Medicine · doi:10.1055/s-2006-931801 · Cited by 82 · see citing works
Pregnancy outcome following recurrent spontaneous abortions
Sheiner, E., Levy, A., Katz, M. E., et al. (2004) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2004.06.015 · Cited by 76 · see citing works
Smith, G. C. S., Pell, J. P., & Walsh, D. (2003) · BMJ · doi:10.1136/bmj.326.7386.423 · Cited by 65 · see citing works
Self-citationWinkelstein, W., Stenchever, M. A., & Lilienfeld, A. M. (1958) · Journal of Chronic Diseases · doi:10.1016/0021-9681(58)90085-7 · Cited by 59 · see citing works
Endocrinology and Recurrent Early Pregnancy Loss
Smith, M., & Schust, D. J. (2011) · Seminars in Reproductive Medicine · doi:10.1055/s-0031-1293202 · Cited by 55 · see citing works
Menstrual and reproductive factors and risk of non-fatal acute myocardial infarction in Italy
Bertuccio, P., Tavani, A., Gallus, S., Negri, E., & Vecchia, C. L. (2007) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2007.01.005 · Cited by 55 · see citing works
Smith, G., Wood, A., Pell, J., & Hattie, J. (2011) · BJOG: An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.2010.02890.x · Cited by 48 · see citing works
Self-citationWinkelstein, W., & Rerate, A. C. (1964) · American Heart Journal · doi:10.1016/0002-8703(64)90094-8 · Cited by 46 · see citing works
Systematic review of cardiovascular disease in women: Assessing the risk
Worrall‐Carter, L., Ski, C. F., Scruth, E. A., Campbell, M., & Page, K. (2011) · Nursing and Health Sciences · doi:10.1111/j.1442-2018.2011.00645.x · Cited by 43 · see citing works
Endothelial Function: A Surrogate Endpoint in Cardiovascular Studies?
Frick, M., & Weidinger, F. (2007) · Current Pharmaceutical Design · doi:10.2174/138161207780831211 · Cited by 42 · see citing works
Miscarriage and risk of cardiovascular disease
Kharazmi, E., Fallah, M., & Luoto, R. M. (2009) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.3109/00016340903380758 · Cited by 39 · see citing works
Hypertensive Disorders in Pregnancy and Preterm Delivery and Subsequent Stroke in Asian Women
Wang, I., Chang, S., Liao, C., Liang, C., Chang, C., Lin, H., Liu, J.-H., Liu, Y., Chuang, F., Hsu, C. Y., et al. (2011) · Stroke · doi:10.1161/strokeaha.110.594523 · Cited by 39 · see citing works
El-Bastawissi, A. Y., Sorensen, T. K., Akafomo, C. K., et al. (2003) · Maternal and Child Health Journal · doi:10.1023/a:1022593601948 · Cited by 32 · see citing works
Germaín, A., Valdés, G., Romanik, M. C., & Reyes, M. S. (2004) · Hypertension · doi:10.1161/01.hyp.0000129825.52269.9e · Cited by 31 · see citing works
Wade, N. S., & Major, A. S. (2011) · Thrombosis and Haemostasis · doi:10.1160/th11-05-0330 · Cited by 28 · see citing works
Recurrent pregnancy loss and thrombophilia.
Micco, P. D., D’Uva, M., Strina, I., et al. (2007) · PubMed · Cited by 26 · see citing works
Evaluation of the relationship between insulin resistance and recurrent pregnancy loss.
Çelik, N., Evsen, M. S., Sak, M. E., Soydinç, H. E., & Gül, T. (2011) · PubMed · Cited by 23 · see citing works
Recurrent pregnancy loss and thrombophilia
Motha, M. B. C., & Palihawadana, T. S. (2014) · Ceylon Medical Journal · doi:10.4038/cmj.v59i1.6730 · Cited by 22 · see citing works
Bhattacharya, S., Townend, J., Shetty, A., et al. (2009) · Obstetric Anesthesia Digest · doi:10.1097/01.aoa.0000362077.75516.1e · Cited by 13 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- [26]Winkelstein WJ Stenchever M Lilenfeld AM Occurrence of pregnancy, abortion, and artificial menopause among women with coronary artery disease: a preliminary study. J Chronic Dis 1958; 7: 273– 86 13539140
- [27]Winkelstein WJ Rekate A Age trend of mortality from coronary artery disease in women and observations on the reproductive patterns of those affected. Am Heart J 1964; 67: 481– 8 14138810
Cited by
Sorted by citations
Sex differences in cardiovascular risk factors and disease prevention
Appelman, Y., van Rijn, B. B., ten Haaf, M. E., Boersma, E., & Peters, S. A. E. (2015) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2015.01.027 · Cited by 588 · see citing works
Okoth, K., Chandan, J. S., Marshall, T., Thangaratinam, S., Thomas, G. N., Nirantharakumar, K., & Adderley, N. J. (2020) · BMJ · doi:10.1136/bmj.m3502 · Cited by 416 · see citing works
Reproductive factors in relation to heart failure in women: A systematic review
Bolijn, R., Onland-Moret, N. C., Asselbergs, F. W., & van der Schouw, Y. T. (2017) · Maturitas · doi:10.1016/j.maturitas.2017.09.004 · Cited by 17 · see citing works
LeBlanc, E. S., Brooks, N., Davies, M., & Chatterjee, R. (2024) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgae655 · Cited by 11 · see citing works
- Authors
- Oliver-Williams, C. T., Heydon, E. E., Smith, G. C. S., & Wood, A. M.
- Affiliations
- Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK
- University of Cambridge (GB)
- Venue
- Heart
- Publisher
- BMJ
- Published
- 2013-03-28
- Volume
- 99
- Issue
- 22
- Pages
- 1636-1644
- ISSN
- 1355-6037 (ISSN-L)
- 1468-201X
- PMC
- PMC3812894
- OpenAlex
- W2101718326
- Cited by
- 151
- References
- 55
- Citations by year
- 2026: 10 · 2025: 8 · 2024: 23 · 2023: 14 · 2022: 15 · 2021: 11 · 2020: 9 · 2019: 24 · 2018: 12 · 2017: 8 · 2016: 4 · 2015: 8 · 2014: 4 · 2013: 1
- FWCI
- 0.49
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc
- Locations
- Heart (publishedVersion, cc-by-nc)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Funders
- National Institute for Health and Care Research (NF-SI-0512-10165)
- British Heart Foundation (RG/08/014/24067)
- Medical Research Council (MR/L003120/1)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
- Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiovascular Issues in Pregnancy
- Keywords
- miscarriage, recurrent pregnancy loss, maternal cardiovascular disease, coronary artery disease, cerebrovascular disease, pregnancy complications, cardiovascular risk factors, postpartum women
- MeSH terms
- Abortion, Spontaneous, Coronary Disease, Female, Humans, Risk
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
