Maternal smoking and the risk of still birth: systematic review and meta-analysis

Takawira C Marufu, Anand Ahankari, Tim Coleman, Sarah Lewis, Takawira C Marufu, Anand Ahankari, Tim Coleman, Sarah Lewis

Abstract

Background: Smoking in pregnancy is known to be associated with a range of adverse pregnancy outcomes, yet there is a high prevalence of smoking among pregnant women in many countries, and it remains a major public health concern. We have conducted a systematic review and meta-analysis to provide contemporary estimates of the association between maternal smoking in pregnancy and the risk of stillbirth.

Methods: We searched four databases namely MEDLINE, EMBASE, Psych Info and Web of Science for all relevant original studies published until 31(st) December 2012. We included observational studies that measured the association between maternal smoking during pregnancy and the risk of stillbirth.

Results: 1766 studies were screened for title analysis, of which 34 papers (21 cohorts, 8 case controls and 5 cross sectional studies) met the inclusion criteria. In meta-analysis smoking during pregnancy was significantly associated with a 47% increase in the odds of stillbirth (OR 1.47, 95% CI 1.37, 1.57, p < 0.0001). In subgroup analysis, smoking 1-9 cig/day and ≥10 cig/day was associated with an 9% and 52% increase in the odds of stillbirth respectively. Subsequently, studies defining stillbirth at ≥ 20 weeks demonstrated a 43% increase in odds for smoking mothers compared to mothers who do not smoke, (OR 1.43, 95% CI 1.32, 1.54, p < 0.0001), whereas studies with stillbirth defined at ≥ 24 weeks and ≥ 28 weeks showed 58% and 33% increase in the odds of stillbirth respectively.

Conclusion: Our review confirms a dose-response effect of maternal smoking in pregnancy on risk of stillbirth. To minimise the risk of stillbirth, reducing current smoking prevalence in pregnancy should continue to be a key public health high priority.

Figures

Figure 1
Figure 1
Flow diagram of included and excluded studies.
Figure 2
Figure 2
Maternal smoking in pregnancy and the risk of stillbirth.
Figure 3
Figure 3
Stillbirth risk according to the amount of daily cigarette consumption.
Figure 4
Figure 4
Maternal smoking and the risk of stillbirth according to the gestation period.

References

    1. World Health Organisation (WHO) Recommendations for the prevention and management of tobacco use and second- hand smoke exposure in pregnancy. Geneva: World Health Organization; 2013.
    1. Royal College of Physicians . Passive smoking and children: a report of the Tobacco Advisory Group of the Royal College of Physicians. London: Royal College of Physicians; 2013.
    1. Royal College of Physicians . Smoking and the young. London: Royal college of Physicians; 1992.
    1. Cnattingius S, Bergstrom R, Lipworth L, Kramer MS. Pre-pregnancy weight and the risk of adverse pregnancy outcomes. N Eng J Med. 1998;338:147–52. doi: 10.1056/NEJM199801153380302.
    1. Fretts RC. Etiology and prevention of stillbirth. Am J Obstet Gynecol. 2005;193:1923–35. doi: 10.1016/j.ajog.2005.03.074.
    1. Lawn JE, Blencowe H, Pattinson R, Cousens S, Kumar R, Ibiebele I, et al. Stillbirths: Where? When? Why? How to make the data count? Lancet. 2011;377:1448–63. doi: 10.1016/S0140-6736(10)62187-3.
    1. Cnattingius S. The epidemiology of smoking during pregnancy: smoking prevalence, maternal characteristics, and pregnancy outcomes. Nicotine Tob Res. 2004;6:S125–40. doi: 10.1080/14622200410001669187.
    1. Flenady V, Koopmans L, Middleton P, Froen JF, Smith GC, Gibbons K, et al. Major risk factors for stillbirth in high-income countries: a systematic review and meta-analysis. Lancet. 2011;377:1331–40. doi: 10.1016/S0140-6736(10)62233-7.
    1. NHS Information centre. The Infant Feeding Survey 2010. Available at [Accessed January 2013].
    1. Scollo MM, Winstanley MH. Tobacco in Australia: Facts and issues. 4. Melbourne: Cancer Council Victoria; 2012.
    1. Ebert LM, Fahy K. Why do women continue to smoke in pregnancy? Women Birth. 2007;20:161–8. doi: 10.1016/j.wombi.2007.08.002.
    1. Wood SL, Chen S, Ross S, Sauve R. The risk of unexplained antepartum stillbirth in second pregnancies following caesarean section in the first pregnancy. BJOG. 2008;115:726–31. doi: 10.1111/j.1471-0528.2008.01705.x.
    1. Smith GCS, Shah I, White IR, Pell JP, Crossley JA, Dobbie R. Maternal and biochemical predictors of antepartum stillbirth among nulliparous women in relation to gestational age of fetal death. BJOG. 2007;114:705–14. doi: 10.1111/j.1471-0528.2007.01343.x.
    1. Hogberg L, Cnattingius S. The influence of maternal smoking habits on the risk of subsequent stillbirth: Is there a causal relation? BJOG. 2007;114:699–704. doi: 10.1111/j.1471-0528.2007.01340.x.
    1. United States Department of Health and Human Services (USDHHS) Women and smoking: a report of the surgeon general. Rockville MD: U.S: Department of Health and Human Services, Centre for Disease Control and Prevention, National Centre for Chronic Disease Prevention and Health Promotion, Office of Smoking and Health; 2001. Health Consequences of Tobacco use among women; pp. 177–450.
    1. Cnattingius S, Haglund B, Meirik O. Cigarette smoking as risk factor for late fetal and early neonatal death. BMJ. 1988;297:258–61. doi: 10.1136/bmj.297.6643.258.
    1. Raymond EG, Cnattingius S, Kiely JL. Effects of maternal age, parity and smoking on the risk of stillbirth. BJOG. 1994;101:301–6. doi: 10.1111/j.1471-0528.1994.tb13614.x.
    1. Schramm WF. Smoking during pregnancy: Missouri longitudinal study. Paediatr Perinat Epidemiol. 1997;11:73–83. doi: 10.1046/j.1365-3016.11.s1.10.x.
    1. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. JAMA. 2000;283:1–5. doi: 10.1001/jama.283.15.2008.
    1. Zegers-Hochschild F, Adamson GD, de Mouzon J, Ishihara O, Mansour R, Nygren K, et al. The International Committee for Monitoring Assisted Reproductive Technology (ICMART) and the World Health Organization (WHO) Revised Glossary on ART Terminology. Hum Reprod. 2009;24:2683–7. doi: 10.1093/humrep/dep343.
    1. Wells G, Shea B, O’Connell D, Peterson J, Welch V, Losos M, et al. Newcastle-Ottawa scale (NOS) for assessing the quality of non-randomised studies in meta-analysis. Available from: (accessed March 10, 2012).
    1. Higgins JPT, Green S (editors). Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 [updated March 2011]. The Cochrane Collaboration 2011. Available from .
    1. Salihu HM, Sharma PP, Getahun D, Hedaytzadeh M, Peters S, Kirby RS, et al. Prenatal tobacco use and risk of stillbirth: a case-control and bidirectional case-crossover study. Nicotine Tob Res. 2008;10:159–66. doi: 10.1080/14622200701705431.
    1. Ferraz EM, Gray RH. A case-control study of stillbirths in Northeast Brazil. Int J Gynaecol Obstet. 1991;34:3–19.
    1. Walles B, Tyden T, Herbst A, Ljungblad U, Rydhstrom H. Maternal health-care program and makers for late fetal death. Acta Obstet Gynecol Scand. 1994;73:773–8. doi: 10.3109/00016349409072503.
    1. Dodds L, King WD, Fell DB, Armson BA, Allen A, Nimrod C. Stillbirth risk factors according to timing of exposure. Ann Epidemiol. 2006;16:607–13. doi: 10.1016/j.annepidem.2005.11.006.
    1. Efkarpidis S, Alexopoulos E, Kean L, Liu D, Fay T. Case-control study of factors associated with intrauterine fetal deaths. MedGenMed. 2004;6:53.
    1. Goy J, Dodds L, Rosenberg MW, King W. Health-risk behaviours: examining social disparities in the occurrence of stillbirth. Paediatr Perinat Epidemiol. 2008;22:314–20. doi: 10.1111/j.1365-3016.2008.00947.x.
    1. Ahlenius I, Thomassen P. The changing panorama of late fetal death in Sweden between 1984 and 1991. Acta Obstet Gynecol Scand. 1999;78:408–14. doi: 10.1080/j.1600-0412.1999.780512.x.
    1. Aliyu MH, Salihu HM, Wilson RE, Alio AP, Kirby RS. The risk of intrapartum stillbirth among smokers of advanced maternal age. Arch Gynecol Obstet. 2008;278:39–45. doi: 10.1007/s00404-007-0529-8.
    1. Aliyu MH, Salihu HM, Wilson RE, Kirby RS. Prenatal smoking and risk of intrapartum stillbirth. Arch Environ Occup Health. 2007;62:87–92. doi: 10.3200/AEOH.62.2.87-92.
    1. Gray R, Bonellie SR, Chalmers J, Greer I, Jarvis S, Kurinczuk JJ, et al. Contribution of smoking during pregnancy to inequalities in stillbirth and infant death in Scotland 1994-2003: retrospective population based study using hospital maternity records. BMJ. 2009;339:b3754. doi: 10.1136/bmj.b3754.
    1. Miller EC, Cao HL, Wen SW, Yang Q, Lafleche J, Walker M. The risk of adverse pregnancy outcomes is increased in preeclamptic women who smoke compared with nonpreeclamptic women who do not smoke. Am J Obstet Gynecol. 2010;203:1–8. doi: 10.1016/j.ajog.2010.05.020.
    1. Mohsin M, Bauman AE, Jalaludin B. The influence of antenatal and maternal factors on stillbirths and neonatal deaths in New South Wales. J Biosoc Sci. 2006;38:643–57. doi: 10.1017/S002193200502701X.
    1. Reddy UM, Laughon SK, Sun L, Troendle J, Willinger M, Zhang J. Prepregnancy risk factors for antepartum stillbirth in the United States. Obstet Gynecol. 2010;116:1119–26. doi: 10.1097/AOG.0b013e3181f903f8.
    1. Sutan R, Campbell D, Prescott GJ, Smith WCS. The risk factors for unexplained antepartum stillbirths in Scotland, 1994 to 2003. J Perinatol. 2010;30:311–8. doi: 10.1038/jp.2009.158.
    1. Tuthill DP, Stewart AH, Coles EC, Andrews J, Cartidge PH. Maternal cigarette smoking and pregnancy outcome. Paediatr Perinat Epidemiol. 1999;13:245–53. doi: 10.1046/j.1365-3016.1999.00187.x.
    1. Wisborg K, Kesmodel U, Henriksen TB, Olsen SF, Secher NJ. Exposure to tobacco smoke in utero and the risk of stillbirth and death in the first year of life. Am J Epidemiol. 2001;154:322–7. doi: 10.1093/aje/154.4.322.
    1. Winbo I, Serenius F, Dahlquist G, Kallen B. Maternal risk factors for cause-specific stillbirth and neonatal death. Acta Obstet Gynecol Scand. 2001;80:235–44. doi: 10.1034/j.1600-0412.2001.080003235.x.
    1. Mishra V, Retherford RD, Smith KR. Cooking smoke and tobacco smoke as risk factors for stillbirth. Int J Environ Health Res. 2005;15:397–410. doi: 10.1080/09603120500288913.
    1. Robson S, Cameron CA, Roberts CL. Birth outcomes for teenage women in New South Wales, 1998-2003. Aust N Z J Obstet Gynaecol. 2006;46:305–10. doi: 10.1111/j.1479-828X.2006.00597.x.
    1. Kleinman JC, Pierre MB, Madans JH, Jr, Land GH, Schramm WF. The effects of maternal smoking on fetal and infant mortality. Am J Epidemiol. 1988;127:274–82.
    1. Raatikainen K, Huurinainen P, Heinonen S. Smoking in early gestation or through pregnancy: a decision crucial to pregnancy outcome. Prev Med. 2007;44:59–63. doi: 10.1016/j.ypmed.2006.07.017.
    1. Huang DY, Usher RH, Kramer MS, Yang H, Morin L, Fretts RC. Determinants of unexplained antepartum fetal deaths. Obstet Gynecol. 2000;95:215–21. doi: 10.1016/S0029-7844(99)00536-0.
    1. Salihu HM, Shumpert MN, Aliyu MH, Alexander MR, Kirby RS, Alexander GR. Stillbirths and infant deaths associated with maternal smoking among mothers aged not greater than or equal to 40 years: a population study. Am J Perinatol. 2004;21:121–9. doi: 10.1055/s-2004-823776.
    1. Moga M, Preda GH. Smoking and pregnancy. J Environ Prot Ecol. 2008;9:566–73.
    1. Bukowski R, Carpenter M, Conway D, Coustan D, Dudley DJ, Goldenberg RL, et al. Association between stillbirth and risk factors known at pregnancy confirmation. JAMA. 2011;306:2469–79. doi: 10.1001/jama.2011.1798.
    1. Kunzel W, Misselwitz B. Unexpected fetal death during pregnancy – a problem of unrecognised fetal disorders during antenatal care? Eur J Obstet Gynecol Reprod Biol. 2003;110:S86–92. doi: 10.1016/S0301-2115(03)00177-5.
    1. Xu B, Jarvelin MR, Rantakallio P. Maternal smoking in pregnancy and sex differences in perinatal death between boys and girls. Soc Biol. 1998;45:273–7.
    1. Kallen K. The impact of maternal smoking during pregnancy on delivery outcome. Eur J Public Health. 2001;11:329–33. doi: 10.1093/eurpub/11.3.329.
    1. Verkerk PH, Buitendijk SE, Verloove-Vanhorick SP. Differential misclassification of alcohol and cigarette consumption by pregnancy outcome. Int J Epidemiol. 1994;23:1218–25. doi: 10.1093/ije/23.6.1218.
    1. Maleckiene L, Nadisauskiene R, Bergstrom S. Scio-economic demographic and obstetric risk factors for late death of unknown etiology in Luthuania: a case—referent study. Acta Obstet Gynecol Scand. 2001;80:321–5.
    1. Beyerleinl A, Von Kriesl R, Hummel M, Lack N, Schiessl B, Giani G. Improvement in pregnancy-related outcomes in the offspring of diabetic mothers in Bavaria, Germany, during 1987–2007. Diabet Med. 2010;27:1379–84. doi: 10.1111/j.1464-5491.2010.03109.x.
    1. Froen JF, Arnestad M, Vege A, Irgens, Rognum T, Saugstad O. Comparative epidemiology of sudden infant death syndrome and sudden intrauterine unexplained death. Arch Dis Child. 2002;87:118–21. doi: 10.1136/fn.87.2.F118.
    1. Little RE, Weinberg CR. Risk-factors for antepartum and intrapartum still-birth. Am J Epidemiol. 1993;137:1177–89.
    1. McCowan LM, George-Haddad M, Stacey T, Thompson JM. Fetal growth restriction and other risk factors for stillbirth in a New Zealand setting. Aust N Z J Obstet Gynaecol. 2007;47:450–6. doi: 10.1111/j.1479-828X.2007.00778.x.
    1. Aliyu MH, Salihu HM, Alio AP, Wilson RE, Charkrabarty S, Clayton HB. Prenatal smoking among adolescents and risk of fetal demise before and during labor. J Pediatr Adolesc Gynecol. 2010;23:129–35. doi: 10.1016/j.jpag.2009.10.008.
    1. Bai J, Wong FW, Gyneshwar R, Stewart HC. Profile of maternal smokers and their pregnancy outcomes in south western Sydney. J Obstet Gynaecol Res. 2000;26:127–32. doi: 10.1111/j.1447-0756.2000.tb01295.x.
    1. Flenady V. Causes and risk factors of stillbirth in Australia. Perinatal Society of Austarlia and New Zealand Congress 2008. Gold Coast. Paediatr Child Health. 2008:2-10.
    1. Marrow RJ, Ritchie JW, Bull SB. Maternal cigarette smoking: the effects on umbilical and uterine blood flow velocity. Am J Obstet Gynecol. 1988;159:1069–71. doi: 10.1016/0002-9378(88)90415-2.
    1. Lambers DS, Clark KE. The maternal and fetal physiologic effects of nicotine. Semin Perinatol. 1996;20:115–26. doi: 10.1016/S0146-0005(96)80079-6.
    1. Ylikorkala O, Viinikka L, Lehtovirta P. Effect of nicotine on fetal prostacyclin and thromboxane in humans. Obstet Gynecol. 1985;66:102–5.
    1. Bruner JP, Forouzan I. Smoking and Bucally administered nicotine. Acute effect on uterine and umbilical artery Doppler flow velocity wave forms. J Reprod Med. 1991;36:435–40.
    1. Salihu HM, Aliyu HM, Kirby RS. In utero nicotine exposure and fetal growth inhibition among twins. Am J Perinatol. 2005;22:421–7. doi: 10.1055/s-2005-915219.
    1. Hammoud AO, Bujold E, Sorokin Y, Schild C, Krapp M, Baumann P. Smoking in pregnancy revisited: findings from a large population-based study. Am J Obstet Gynecol. 2005;192:1856–63. doi: 10.1016/j.ajog.2004.12.057.
    1. Hajek P, Stead LF, West R, Jarvis M, Hartmann-Boyce J, Lancaster T. Relapse prevention interventions for smoking cessation. Cochrane Database Syst Rev 2013, Issue 8. Art. No.: CD003999. doi:10.1002/14651858.CD003999.pub4.
    1. Coleman T, Chamberlain C, Davey MA, Cooper SE, Leonardi-Bee J. Pharmacological interventions for promoting smoking cessation during pregnancy. Cochrane Database Syst Rev 2012, Issue 9. Art. No.: CD010078. doi:10.1002/14651858.CD010078

Source: PubMed

Sponzoři a spolupracovníci

Zdravotní podmínky

Drogové intervence

3
Předplatit