Risks of venous thromboembolism after cesarean sections: a meta-analysis

Marc Blondon, Alessandro Casini, Kara K. Hoppe

Abstract


Background: Cesarean sections (CS) are believed to be associated with greater risks of postpartum venous thromboembolism (VTE). Our objective was to systematically review the evidence on this association and on the absolute risk of VTE after CS.

Methods: Authors searched PubMed, Embase and conference proceedings from 1980 to 11/2015 for reports on the associations of delivery methods with postpartum VTE and on the incidence of VTE after CS. They excluded studies on thrombophilia or recurrent VTE and restricted to prospective studies when assessing the incidence of VTE. Pooled relative and absolute risks were estimated with random-effects models.

Results: search retrieved 28 mostly retrospective observational studies comparing risks of VTE after CS and after vaginal deliveries (VD) (n > 53 000 VTE events), and 32 prospective studies reporting risks of VTE after CS (n = 218 VTE events). Compared with VD, the relative risk of VTE after CS ranged from 1–22, with a meta-analytic odds ratio (OR) of 3.7 (95% CI 3.0–4.6). Adjustment for age and BMI had a marginal influence on the estimated pooled OR.

Associations were observed for both elective and emergency CS, with stronger estimates of associations for emergency CS. The pooled incidence was 2.6 VTE/1000 CS (95% CI 1.7–3.5), and was greater in studies with a longer and better follow-up in the postpartum (4.3/1000 CS).

Conclusion: The risk of VTE is 4-fold greater after CS than VD, appears independent of other VTE risk factors, and is greater after emergency than elective CS. On average, 3 in 1000 women will develop a VTE after CS.


Keywords


deep venous thrombosis; pulmonary embolism; pregnancy; meta analysis

References


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Wik, H.S., Jacobsen, A.F., Sandvik, L., Sandset, P.M. “Prevalence and predictors for postthrombotic syndrome 3 to 16 years after pregnancy-related venous thrombosis: a population-based, cross-sectional, case-control study.” Journal of thrombosis and haemostasis: JTH 10.5 (2012): 840–7.

Martin, J.A., Hamilton, B.E., Osterman, M.J. “Births in the United States, 2013.” NCHS Data Brief 175 (2014): 1–8.

Jacobsen, A.F., Skjeldestad, F.E., Sandset, P.M. “Ante- and postnatal risk factors of venous thrombosis: a hospital-based case-control study.” Journal of thrombosis and haemostasis: JTH 6.6 (2008): 905–12.

Stroup, D.F., Berlin, J.A., Morton, S.C., et al. “Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group.” Jama 283.15 (2000): 2008–12.

Wells, G., Shea, B., O’Connell, J., et al. “The Newcastle-Ottawa scale (NOS) for assessing the quality of nonrandomised studies in meta-analysis.” Available from: [http://www.ohri.ca/programs/clinical_epidemiology/oxford. asp], last accessed Aug 24, 2016.

Trinquart, L., Touze, E. “Pitfalls in meta-analysis of observational studies: lessons from a systematic review of the risks of stenting for intracranial atherosclerosis.” Stroke 40.10 (2009): e586–90.

James, A.H., Jamison, M.G., Brancazio, L.R., Myers, E.R. “Venous thromboembolism during pregnancy and the postpartum period: incidence, risk factors, and mortality.” American journal of obstetrics and gynecology 194.5 (2006): 1311–5.

Abbasi, N., Balayla, J., Laporta, D.P., et al. “Trends, risk factors and mortality among women with venous thromboembolism during labour and delivery: A populationbased study of 8 million births.” Archives of gynecology and obstetrics 289.2 (2014): 275–84.

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Kierkegaard, A. “Incidence and diagnosis of deep vein thrombosis associated with pregnancy.” Acta obstetricia et gynecologica Scandinavica 62.3 (1983): 239–43.

Koroukian, S.M. “Relative risk of postpartum complications in the Ohio Medicaid population: Vaginal versus cesarean delivery.” Medical Care Research and Review 61.2 (2004): 203–24.

Lindqvist, P.G., Torsson, J., Almqvist, A., Bjorgell, O. “Postpartum thromboembolism: severe events might be preventable using a new risk score model.” Vascular health and risk management 4.5 (2008): 1081–7.

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Lindqvist, P., Dahlback, B., Marsal, K. “Thrombotic risk during pregnancy: a population study.” Obstetrics and gynecology 94.4 (1999):595–9.

Liu, S., Rouleau, J., Joseph, K.S., et al. “Epidemiology of pregnancy-associated venous thromboembolism: a population-based study in Canada.” Journal of obstetrics and gynaecology Canada: JOGC 31.7 (2009): 611–20.

Ghaji, N., Boulet, S.L., Tepper, N., Hooper, W.C. “Trends in venous thromboembolism among pregnancy-related hospitalizations, United States, 1994-2009.” American Journal of Obstetrics and Gynecology 209.5 (2013): e431–438.

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GOST Style Citations


1. Pomp, E.R., Lenselink, A.M., Rosendaal, F.R., Doggen, C.J.M. “Pregnancy, the postpartum period and prothrombotic defects: Risk of venous thrombosis in the MEGA study.” Journal of Thrombosis and Haemostasis 6.4 (2008): 632–7.

2. Wik, H.S., Jacobsen, A.F., Sandvik, L., Sandset, P.M. “Prevalence and predictors for postthrombotic syndrome 3 to 16 years after pregnancy-related venous thrombosis: a population-based, cross-sectional, case-control study.” Journal of thrombosis and haemostasis: JTH 10.5 (2012): 840–7.

3. Martin, J.A., Hamilton, B.E., Osterman, M.J. “Births in the United States, 2013.” NCHS Data Brief 175 (2014): 1–8.

4. Jacobsen, A.F., Skjeldestad, F.E., Sandset, P.M. “Ante- and postnatal risk factors of venous thrombosis: a hospital-based case-control study.” Journal of thrombosis and haemostasis: JTH 6.6 (2008): 905–12.

5. Stroup, D.F., Berlin, J.A., Morton, S.C., et al. “Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group.” Jama 283.15 (2000): 2008–12.

6. Wells, G., Shea, B., O’Connell, J., et al. “The Newcastle-Ottawa scale (NOS) for assessing the quality of nonrandomised studies in meta-analysis.” Available from: [http://www.ohri.ca/programs/clinical_epidemiology/oxford. asp], last accessed Aug 24, 2016.

7. Trinquart, L., Touze, E. “Pitfalls in meta-analysis of observational studies: lessons from a systematic review of the risks of stenting for intracranial atherosclerosis.” Stroke 40.10 (2009): e586–90.

8. James, A.H., Jamison, M.G., Brancazio, L.R., Myers, E.R. “Venous thromboembolism during pregnancy and the postpartum period: incidence, risk factors, and mortality.” American journal of obstetrics and gynecology 194.5 (2006): 1311–5.

9. Abbasi, N., Balayla, J., Laporta, D.P., et al. “Trends, risk factors and mortality among women with venous thromboembolism during labour and delivery: A populationbased study of 8 million births.” Archives of gynecology and obstetrics 289.2 (2014): 275–84.

10. Macklon, N.S., Greer, I.A. “Venous thromboembolic disease in obstetrics and gynaecology: the Scottish experience.” Scottish medical journal 41.3 (1996): 83–6.

11. Treffers, P.E., Huidekoper, B.L., Weenink, G.H., et al. “Epidemiological observations of thrombo-embolic disease during pregnancy and in the puerperium, in 56,022 women.” International journal of gynaecology and obstetrics: the official organ of the International Federation of Gynaecology and Obstetrics 21.4 (1983): 327–31.

12. Galanaud, J.P., Cochery-Nouvellon, E., Alonso, S., et al. “Paternal endothelial protein C receptor 219Gly variant as a mild and limited risk factor for deep vein thrombosis during pregnancy.” Journal of thrombosis and haemostasis: JTH 8.4 (2010): 707–13.

13. Hiltunen, L., Rautanen, A., Rasi, V., et al. “An unfavorable combination of Factor V Leiden with age, weight, and blood group causes high risk of pregnancyassociated venous thrombosis: a population-based nested casecontrol study.” Thrombosis research 119.4 (2007): 423–32.

14. Jacobsen, A.F., Skjeldestad, F.E., Sandset, P.M. “Incidence and risk patterns of venous thromboembolism in pregnancy and puerperium – a register-based case-control study.” American journal of obstetrics and gynecology 198.2 (2008): e231–237.

15. Landon, M.B., Hauth, J.C., Leveno, K.J., et al. “Maternal and perinatal outcomes associated with a trial of labor after prior cesarean delivery.” N Engl J Med 351.25 (2004): 2581–9.

16. Virkus, R.A., Lokkegaard, E., Lidegaard, O., et al. “Risk factors for venous thromboembolism in 1.3 million pregnancies: a nationwide prospective cohort.” PloS one 9.5 (2014): e96495.

17. Abdul Sultan, A., Grainge, M.J., West, J., et al. “Impact of risk factors on the timing of first postpartum venous thromboembolism: a population-based cohort study from England.” Blood 124.18 (2014): 2872–80.

18. Blondon, M., Harrington, L.B., Righini, M., et al. “Racial and ethnic differences in the risk of postpartum venous thromboembolism: a population-based, case-control study.” Journal of thrombosis and haemostasis: JTH 12.12 (2014): 2002–9.

19. Colmorn, L.B., Ladelund, S., Rasmussen, S., Secher, N.J. “Risk of a venous thromboembolic episode due to caesarean section and BMI: A study in northern Denmark covering 2000–2010.” Journal of Obstetrics and Gynaecology 34.4 (2014): 313–6.

20. Sultan, A.A., Tata, L.J., West, J., et al. “Risk factors for first venous thromboembolism around pregnancy: a population-based cohort study from the United Kingdom.” Blood 121.19 (2013): 3953–61.

21. Danilenko-Dixon, D.R., Heit, J.A., Silverstein, M.D., et al. “Risk factors for deep vein thrombosis and pulmonary embolism during pregnancy or post partum: A populationbased, casecontrol study.” American Journal of Obstetrics and Gynecology 184.2 (2001): 104–10.

22. Kierkegaard, A. “Incidence and diagnosis of deep vein thrombosis associated with pregnancy.” Acta obstetricia et gynecologica Scandinavica 62.3 (1983): 239–43.

23. Koroukian, S.M. “Relative risk of postpartum complications in the Ohio Medicaid population: Vaginal versus cesarean delivery.” Medical Care Research and Review 61.2 (2004): 203–24.

24. Lindqvist, P.G., Torsson, J., Almqvist, A., Bjorgell, O. “Postpartum thromboembolism: severe events might be preventable using a new risk score model.” Vascular health and risk management 4.5 (2008): 1081–7.

25. Kobayashi, T., Nakabayashi, M., Ishikawa, M., et al. “Pulmonary thromboembolism in obstetrics and gynecology increased by 6.5-fold over the past decade in Japan.” Circulation journal : official journal of the Japanese Circulation Society 72.5 (2008): 753–6.

26. Burrows, L.J., Meyn, L.A., Weber, A.M. “Maternal morbidity associated with vaginal versus cesarean delivery.” Obstetrics and gynecology 103 (5 Pt 1) (2004): 907–12.

27. Chan, L.Y., Tam, W.H., Lau, T.K. “Venous thromboembolism in pregnant Chinese women.” Obstetrics and gynecology 98.3 (2001): 471–5.

28. Gherman, R.B., Goodwin, T.M., Leung, B., et al. “Incidence, clinical characteristics, and timing of objectively diagnosed venous thromboembolism during pregnancy.” Obstetrics and gynecology 94 (5 Pt 1) (1999): 730–4.

29. Simpson, E.L., Lawrenson, R.A., Nightingale, A.L., et al. “Venous thromboembolism in pregnancy and the puerperium: Incidence and additional risk factors from a London perinatal database.” British Journal of Obstetrics and Gynaecology 108.1 (2001): 56–60.

30. Won, H.S., Kim do, Y., Yang, M.S., et al. “Pregnancy-induced hypertension, but not gestational diabetes mellitus, is a risk factor for venous thromboembolism in pregnancy.” Korean Circ J 41.1 (2011): 23–7.

31. Lindqvist, P., Dahlback, B., Marsal, K. “Thrombotic risk during pregnancy: a population study.” Obstetrics and gynecology 94.4 (1999):595–9.

32. Liu, S., Rouleau, J., Joseph, K.S., et al. “Epidemiology of pregnancy-associated venous thromboembolism: a population-based study in Canada.” Journal of obstetrics and gynaecology Canada: JOGC 31.7 (2009): 611–20.

33. Ghaji, N., Boulet, S.L., Tepper, N., Hooper, W.C. “Trends in venous thromboembolism among pregnancy-related hospitalizations, United States, 1994-2009.” American Journal of Obstetrics and Gynecology 209.5 (2013): e431–438.

34. Kane, E.V., Calderwood, C., Dobbie, R., et al. “A populationbased study of venous thrombosis in pregnancy in Scotland 1980–2005.” European Journal of Obstetrics Gynecology and Reproductive Biology 169.2 (2013): 223–9.

35. Morris, J.M., Algert, C.S., Roberts, C.L. “Incidence and risk factors for pulmonary embolism in the postpartum period.” Journal of thrombosis and haemostasis: JTH 8.5 (2010): 998–1003.

36. Pallasmaa, N., Ekblad, U., Gissler, M. “Severe maternal morbidity and the mode of delivery.” Acta Obstetricia et Gynecologica Scandinavica 87.6 (2008): 662–8.

37. Chauleur, C., Quenet, S., Varlet, M.N., et al. “Feasibility of an easy-to-use risk score in the prevention of venous thromboembolism and placental vascular complications in pregnant women: a prospective cohort of 2736 women.” Thrombosis research 122.4 (2008): 478–84.

38. Silver, R.M., Landon, M.B., Rouse, D.J., et al. “Maternal morbidity associated with multiple repeat cesarean deliveries.” Obstetrics and gynecology 107.6 (2006): 1226–32.

39. Burrows, R.F., Gan, E.T., Gallus, A.S., et al. “A randomised doubleblind placebo controlled trial of low molecular weight heparin as prophylaxis in preventing venous thrombolic events after caesarean section: a pilot study.” BJOG: an international journal of obstetrics and gynaecology 108.8 (2001): 835–9.

40. Cavazza, S., Rainaldi, M.P., Adduci, A., Palareti, G. “Thromboprophylaxis following cesarean delivery: one site prospective pilot study to evaluate the application of a risk score model.” Thrombosis research 129.1 (2012): 28–31.

41. Gates, S., Brocklehurst, P., Ayers, S., Bowler, U. “Thromboprophylaxis and pregnancy: two randomized controlled pilot trials that used low-molecular-weight heparin.” American journal of obstetrics and gynecology 191.4 (2004): 1296–303.

42. Gizzo, S., Noventa, M., Anis, O., et al. “Pharmacological anti-thrombotic prophylaxis after elective caesarean delivery in thrombophilia unscreened women: Should maternal age have a role in decision making?” Journal of Perinatal Medicine 42.3 (2014): 339–47.

43. Kalro, B.N., Davidson, R.A., Owen, P. “Low incidence of asymptomatic deep venous thrombosis following caesarean section: a colour Doppler study.” Health bulletin 57.6 (1999): 418–21.

44. Larsson, C., Saltvedt, S., Wiklund, I., Andolf, E. “Planned vaginal delivery versus planned caesarean section: short-term medical outcome analyzed according to intended mode of delivery.” Journal of obstetrics and gynaecology Canada: JOGC 33.8 (2011): 796–802.

45. Lindqvist, P.G., Svensson, P.J., Marsal, K., et al. “Activated protein C resistance (FV:Q506) and pregnancy.” Thrombosis and Haemostasis 81.4 (1999): 532–7.

46. Salomon, O., Seligsohn, U., Steinberg, D.M., et al. “The common prothrombotic factors in nulliparous women do not compromise blood flow in the feto-maternal circulation and are not associated with preeclampsia or intrauterine growth restriction.” American journal of obstetrics and gynecology 191.6 (2004): 2002–9.

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DOI: http://dx.doi.org/10.18370/2309-4117.2016.31.73-79

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