A systematic review and meta-analysis of prospective studies on the association between maternal cigarette smoking and preterm delivery
Open accessAbstract
We have attempted to quantify the most up-to-date estimate of the association between cigarette smoking by the mother and preterm delivery. Studies were selected for inclusion in this review if they were prospective, reported data stratified across at least two levels of maternal smoking, and defined preterm delivery on the basis of gestational age. In a meta-analysis we combined results from multiple studies that reported on preterm delivery and maternal smoking during pregnancy. Pooled odds ratios were computed for various strata of smoking intensity with the Mantel-Haenszel fixed-effects model. Twenty studies met all inclusion criteria and were included in meta-analysis. The pooled point estimate from 20 prospective studies on any maternal smoking versus no maternal smoking was 1.27 (95% confidence interval, 1.21-1.33). Subgroup analyses stratifying maternal smoking on number of cigarettes per day suggest a dose-response relationship at low to moderate levels of smoking, which was not further increased at high levels of smoking. A nonsignificant level of publication bias appears to exist in the smoking-preterm delivery literature. Cigarette smoking is a preventable risk factor that is associated with preterm delivery. Consistent results across many study populations and research designs and evidence of a dose-response relationship support its causal role in preterm delivery.
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Smoking is associated with a higher odds of sPTB and birth of SGA neonates.
“In accordance with previous studies, we indeed found that smoking is associated with a higher odds of sPTB and birth of SGA neonates [38–41].”
From Associations between periconceptional lifestyle behaviours and adverse pregnancy outcomes (2021) · cites this paper as [38]
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The complex relationship between smoking in pregnancy and very preterm delivery
Burguet, A., Kaminski, M., Abraham-Lerat, L., Schaal, J. P., Cambonie, G., Fresson, J., Grandjean, H., Truffert, P., Marpeau, L., Voyer, M., et al. (2004) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1046/j.1471-0528.2003.00037.x · Cited by 116 · see citing works
“Case–control studies linking smoking to preterm birth appear to provide higher odds ratios than cohort studies.(8) This difference might be partly due to recall bias.”
BackgroundMitochondrial toxicity of tobacco smoke and air pollution
Fetterman, J. L., Sammy, M. J., & Ballinger, S. W. (2017) · Toxicology · doi:10.1016/j.tox.2017.08.002 · Cited by 113 · see citing works
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“One case–control study of 275 women (including 34 women who delivered <34 weeks gestation) found that women who eventually delivered preterm had a wider mean utero-cervical angle during midpregnancy (assessed between 180/7 and 236/7 weeks gestation) [72].”
BackgroundReducing preterm birth by a statewide multifaceted program: an implementation study
Newnham, J. P., White, S. W., Meharry, S., Lee, H., Pedretti, M. K., Arrese, C. A., Keelan, J. A., Kemp, M. W., Dickinson, J. E., & Doherty, D. A. (2016) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2016.11.1037 · Cited by 110 · see citing works
The genomics of preterm birth: from animal models to human studies
Lamm, K. Y. B., Karjalainen, M. K., Hallman, M., Teramo, K., & Muglia, L. J. (2013) · Genome Medicine · doi:10.1186/gm438 · Cited by 107 · see citing works
Presence of an epigenetic signature of prenatal cigarette smoke exposure in childhood
Ladd‐Acosta, C., Shu, C., Lee, B. K., Gidaya, N. B., Singer, A. B., Schieve, L. A., Schendel, D., Jones, N., Daniels, J. L., Windham, G. C., et al. (2015) · Environmental Research · doi:10.1016/j.envres.2015.11.014 · Cited by 105 · see citing works
“A considerable proportion (11%) of women in the United States actively smoke during pregnancy, a major risk factor for pregnancy complications(Castles et al., 1999; Shah and Bracken, 2000) and adverse health outcomes during infancy, childhood and later life (Salmasi et al.”
InfluentialAdverse perinatal outcomes associated with homelessness and substance use in pregnancy
Little, M., Shah, R., Vermeulen, M. J., Gorman, A., Dzendoletas, D., & Ray, J. G. (2005) · Canadian Medical Association Journal · doi:10.1503/cmaj.050406 · Cited by 104 · see citing works
Stroud, L. R., Papandonatos, G. D., Rodriguez, D., McCallum, M., Salisbury, A. L., Phipps, M. G., Lester, B., Huestis, M. A., Niaura, R., Padbury, J. F., et al. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.05.017 · Cited by 104 · see citing works
“Offspring exposed to MSDP are at increased risk for costly and adverse medical outcomes, including low birth weight, preterm delivery, andincreased length of neonatal intensive care unit stays (Shah and Bracken, 2000; Dietz et al., 2010; Adams et al., 2011).”
BackgroundPhilips, E. M., Santos, S., Trasande, L., Aurrekoetxea, J. J., Barros, H., Berg, A. V., Bergström, A., Bird, P. K., Brescianini, S., Chaoimh, C. N., et al. (2020) · PLoS Medicine · doi:10.1371/journal.pmed.1003182 · Cited by 103 · see citing works
“The risks of preterm birth were somewhat weaker than reported previously [7,9,18], potentially because no information was available about induced or spontaneous preterm birth.”
BackgroundCombined Effects of Cigarette Smoking and Alcohol Consumption on Perinatal Outcome
Odendaal, H. J., Steyn, D. W., Elliott, A. J., & Burd, L. (2008) · Gynecologic and Obstetric Investigation · doi:10.1159/000150597 · Cited by 103 · see citing works
“examined the effects of smoking on 5 common complications of pregnancy. Smoking was found to be strongly associated with an elevated risk of placenta praevia, abruptio placentae, ectopic pregnancy, and preterm prelabor rupture of membranes, and a decreased risk of preeclampsia. In a more recent meta-analysis from 20 p…”
Hobel, C. J. (2004) · Clinical Obstetrics & Gynecology · doi:10.1097/01.grf.0000142512.38733.8c · Cited by 102 · see citing works
Maccani, J. Z. J., Koestler, D., Houseman, E., Marsit, C., & Kelsey, K. (2013) · Epigenomics · doi:10.2217/epi.13.63 · Cited by 95 · see citing works
Bainbridge, S. A., Sidle, E. H., & Smith, G. N. (2004) · Medical Hypotheses · doi:10.1016/j.mehy.2004.06.019 · Cited by 99 · see citing works
Goedhart, G., Snijders, A. C., Hesselink, A. E., van Poppel, M. N. M., Bonsel, G. J., & Vrijkotte, T. G. M. (2010) · Psychosomatic Medicine · doi:10.1097/psy.0b013e3181ee4a62 · Cited by 96 · see citing works
Occupational predictors of pregnancy outcomes in Irish working women in the Lifeways cohort
Niedhammer, I., O’Mahony, D., Daly, S., Morrison, J., Kelleher, C., & the Lifeways Cross‐Generation Cohort Study Steering Group (2009) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.2009.02160.x · Cited by 94 · see citing works
Teenage pregnancies: Obstetric characteristics and outcome
Gupta, N., Kiran, U., & Bhal, K. (2007) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2007.06.013 · Cited by 94 · see citing works
Hu, J., Xia, W., Pan, X., Zheng, T., Zhang, B., Zhou, A., Buka, S. L., Bassig, B. A., Liu, W., Wu, C., et al. (2017) · The Lancet Planetary Health · doi:10.1016/s2542-5196(17)30094-3 · Cited by 92 · see citing works
Haldre, K., Rahu, M., Karro, H., & Rahu, M. (2006) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2006.05.002 · Cited by 92 · see citing works
“Smoking is associated with preterm labor [26] and reduced fetal growth [27] and was included in the logistic regression model as a confounding variable.”
BackgroundHåkonsen, L. B., Ernst, A., & Ramlau‐Hansen, C. H. (2014) · Asian Journal of Andrology · doi:10.4103/1008-682x.122351 · Cited by 91 · see citing works
Cryptorchidism According to Maternal Gestational Smoking
Lindhard, M. S., Toft, G. V., Thulstrup, A. M., Bonde, J. P., & Olsen, J. (2007) · Epidemiology · doi:10.1097/01.ede.0000254061.90686.9f · Cited by 91 · see citing works
The Impact of Prenatal WIC Participation on Infant Mortality and Racial Disparities
Khanani, I., Elam, J., Hearn, R., Jones, C. A., & Maseru, N. (2010) · American Journal of Public Health · doi:10.2105/ajph.2009.168922 · Cited by 91 · see citing works
Biological and pathological mechanisms leading to the birth of a small vulnerable newborn
Hunter, P., Awoyemi, T., Ayede, A. I., Chico, R. M., David, A. L., Dewey, K. G., Duggan, C., Gravett, M. G., Prendergast, A. J., Ramakrishnan, U., et al. (2023) · The Lancet · doi:10.1016/s0140-6736(23)00573-1 · Cited by 91 · see citing works
Prenatal Smoking Cessation and the Risk of Delivering Preterm and Small-for-Gestational-Age Newborns
Polakowski, L. L., Akinbami, L. J., & Mendola, P. (2009) · Obstetrics & Gynecology · doi:10.1097/aog.0b013e3181ae9e9c · Cited by 86 · see citing works
Neighborhood Factors Associated with Physical Activity and Adequacy of Weight Gain During Pregnancy
Laraia, B. A., Messer, L. C., Evenson, K. R., & Kaufman, J. S. (2007) · Journal of Urban Health · doi:10.1007/s11524-007-9217-z · Cited by 82 · see citing works
Reducing tobacco smoking and smoke exposure to prevent preterm birth and its complications
Wagijo, M.-A. R., Sheikh, A., Duijts, L., & Been, J. V. (2015) · Paediatric Respiratory Reviews · doi:10.1016/j.prrv.2015.09.002 · Cited by 82 · see citing works
“To the best of our knowledge the most recent meta-analysis on the topic was published in 2000 [14].”
BackgroundTsai, H.-J., Liu, X., Mestan, K. K. L., Yu, Y., Zhang, S., Fang, Y., Pearson, C., Ortiz, K., ZUCKERMAN, B. S., Bauchner, H., et al. (2008) · Human Genetics · doi:10.1007/s00439-008-0485-9 · Cited by 81 · see citing works
“Maternal cigarette smoking is an important preventable environmental factor known to increase the risk of PTD, with odds ratios ranging from 1.1 to 2.4 (Cnattingius 2004; Pollack et al. 2000; Shah and Bracken 2000; Wang et al. 1997).”
BackgroundInfluentialPrenatal nicotine exposure increases connective tissue expression in foetal monkey pulmonary vessels
Sekhon, H. S., Proskocil, B. J., Clark, J. A., & Spindel, E. R. (2004) · European Respiratory Journal · doi:10.1183/09031936.04.00069604 · Cited by 81 · see citing works
Ambient temperature as a trigger of preterm delivery in a temperate climate
Cox, B., Vicedo-Cabrera, A. M., Gasparrini, A., Roels, H. A., Martens, E., Vangronsveld, J., Forsberg, B., & Nawrot, T. S. (2016) · Journal of Epidemiology & Community Health · doi:10.1136/jech-2015-206384 · Cited by 79 · see citing works
Risk factors for spontaneous preterm birth among Aboriginal and non‐Aboriginal women in Manitoba
Heaman, M. I., Blanchard, J., Gupton, A. L., MOFFATT, M. E. K., & Currie, R. F. (2005) · Paediatric and Perinatal Epidemiology · doi:10.1111/j.1365-3016.2005.00644.x · Cited by 77 · see citing works
Patorno, E., Hernández–Dı́az, S., Huybrechts, K. F., Desai, R. J., Cohen, J. M., Mogun, H., & Bateman, B. T. (2020) · PLoS Medicine · doi:10.1371/journal.pmed.1003322 · Cited by 75 · see citing works
Tegethoff, M., Belardi, A., Stalujanis, E., & Meinlschmidt, G. (2015) · Psychosomatic Medicine · doi:10.1097/psy.0000000000000151 · Cited by 72 · see citing works
Risk factors for preterm birth among opiate-addicted gravid women in a methadone treatment program
Almario, C. V., Seligman, N. S., Dysart, K., Berghella, V., & Baxter, J. K. (2009) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2009.05.052 · Cited by 72 · see citing works
Mongan, D., Lynch, J., Hanna, D., Shannon, C., Hamilton, S., Potter, C., Gorman, C., McCambridge, O., Morrow, R., & Mulholland, C. C. (2019) · BMC Pregnancy and Childbirth · doi:10.1186/s12884-019-2572-4 · Cited by 70 · see citing works
Prevention of preterm birth: a renewed national priority
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Janisse, J. J., Bailey, B. A., Ager, J. W., & Sokol, R. J. (2013) · Substance Abuse · doi:10.1080/08897077.2013.804483 · Cited by 70 · see citing works
“(9) Pregnancy cigarette smoking has been linked with preterm delivery,(10) and other studies have suggested fetal growth is also affected.”
BackgroundThe Contribution of Birth Defects to Preterm Birth and Low Birth Weight
Dolan, S. M., Gross, S. J., Merkatz, I. R., Faber, V., SULLIVAN, L. M., Malone, F. D., Porter, T. F., Nyberg, D. A., Comstock, C. H., Hankins, G. D. V., et al. (2007) · Obstetrics and Gynecology · doi:10.1097/01.aog.0000275264.78506.63 · Cited by 69 · see citing works
Influence of smoking and snuff cessation on risk of preterm birth
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Smoking Patterns and Use of Cessation Interventions During Pregnancy
Tong, V. T., England, L. J., Dietz, P. M., & Asare, L. A. (2008) · American Journal of Preventive Medicine · doi:10.1016/j.amepre.2008.06.033 · Cited by 68 · see citing works
Women’s Knowledge, Attitudes and Behavior about Maternal Risk Factors in Pregnancy
Esposito, G., Ambrosio, R., Napolitano, F., & Giuseppe, G. D. (2015) · PLoS ONE · doi:10.1371/journal.pone.0145873 · Cited by 65 · see citing works
Poon, L. C., Savvas, M., Zamblera, D., Skyfta, E., & Nicolaides, K. H. (2012) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.2011.03203.x · Cited by 64 · see citing works
Rich-Edwards, J. W., Klungsøyr, K., Wilcox, A. J., & Skjærven, R. (2015) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2015.06.001 · Cited by 64 · see citing works
“3.(18) As is typical of registries, there were no data available on CVD risk factors, such as body mass index.”
BackgroundWomen with a recent history of early‐onset pre‐eclampsia have a worse periodontal condition
Kunnen, A., Blaauw, J., van Doormaal, J. J., van Pampus, M. G., van der Schans, C. P., Aarnoudse, J. G., Winkelhoff, A. J. V., & Abbas, F. (2006) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.2006.01036.x · Cited by 64 · see citing works
Maternal tobacco use and extremely premature birth – a population‐based cohort study
Dahlin, S., Gunnerbeck, A., Wikström, A., Cnattingius, S., & Bonamy, A. E. (2016) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/1471-0528.14213 · Cited by 64 · see citing works
Ruiz, R. J., Fullerton, J. T., Brown, C. E., & Dudley, D. J. (2002) · Biological Research For Nursing · doi:10.1177/1099800402004001007 · Cited by 63 · see citing works
Adverse effects of parental smoking during pregnancy in urban and rural areas
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“Moore and Zaccaro [43] also found different risks for different numbers of cigarettes smoked per day, but, in a systematic review and metaanalysis, this relationship was not clear [44].”
BackgroundBird, A. L., Grant, C. C., Bandara, D. K., Mohal, J., Carr, P. A., WISE, M. R., Inskip, H. M., Miyahara, M., & Morton, S. (2016) · Australian and New Zealand Journal of Obstetrics and Gynaecology · doi:10.1111/ajo.12557 · Cited by 60 · see citing works
“0 (or weight loss) 223 (4) 1–5 kg 672 (12) 6–10 kg 2079 (38) 11–15 kg 1588 (29) 16–20 kg 597 (11) >20 kg 348 (6) Maternal smoking (n = 6161) No smoking (before or during) 4904 (80) Stopped smoking for pregnancy 610 (10) Continued smoking during pregnancy 647 (10) Alcohol use before pregnancy (n = 6805) No alcohol 1982…”
Heaman, M. I., & Chalmers, K. I. (2005) · Birth · doi:10.1111/j.0730-7659.2005.00387.x · Cited by 59 · see citing works
Second Births to Teenage Mothers: Risk Factors For Low Birth Weight and Preterm Birth
Partington, S. N., Steber, D. L., Blair, K. A., & Cisler, R. A. (2009) · Perspectives on Sexual and Reproductive Health · doi:10.1363/4110109 · Cited by 57 · see citing works
“Smoking during pregnancy has been consistently associated with decreased birth weight and preterm birth in both teenage and older mothers.(38,39) One study estimated that among infants born to teenagers, maternal smoking during pregnancy accounted for 39% of the risk of low birth weight and 12% of the risk of preterm…”
BackgroundSelected Vaginal Bacteria and Risk of Preterm Birth: An Ecological Perspective
Wen, A., Srinivasan, U., Goldberg, D. E., Owen, J., Marrs, C. F., Misra, D. P., Wing, D. A., Ponnaluri-Wears, S., Miles-Jay, A., Bucholz, B., et al. (2013) · The Journal of Infectious Diseases · doi:10.1093/infdis/jit632 · Cited by 58 · see citing works
“These factors include black race [3], smoking [15], douching [16–19], extremes of BMI [3, 20], and shortened cervical length during pregnancy [3, 21].”
BackgroundIon, R., Wills, A. K., & Bernal, A. L. (2015) · Reproductive Sciences · doi:10.1177/1933719115612135 · Cited by 57 · see citing works
“27).(2) The prospective way in which exposure information was collected reduces the risk of reporting bias.”
BackgroundPrenatal substance exposure and offspring development: Does DNA methylation play a role?
Knopik, V. S., Marceau, K., Bidwell, L. C., & Rolan, E. (2018) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2018.01.009 · Cited by 45 · see citing works
“, non-genetically informed studies) suggest that SDP is associated with multiple adverse birth related outcomes, such as preterm delivery (Castles et al., 1999; Kaddar et al., 2009; Shah and Bracken, 2000), increased risk for spontaneous abortion (Castles et al.”
Background
- Authors
- Shah, N. R., & Bracken, M. B.
- Affiliations
- Yale University (US)
- ORCID
- Shah, Nirav R.
- Venue
- American Journal of Obstetrics and Gynecology
- Publisher
- Elsevier BV
- Published
- 2000-02
- Volume
- 182
- Issue
- 2
- Pages
- 465-472
- ISSN
- 0002-9378 (ISSN-L)
- PMC
- PMC2706697
- OpenAlex
- W2014933068
- Cited by
- 394
- References
- 48
- Citations by year
- 2026: 9 · 2025: 10 · 2024: 10 · 2023: 13 · 2022: 23 · 2021: 18 · 2020: 22 · 2019: 23 · 2018: 15 · 2017: 26 · 2016: 23 · 2015: 24 · 2014: 17 · 2013: 23 · 2012: 16
- FWCI
- 2.15
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- American Journal of Obstetrics and Gynecology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Heart, Lung, and Blood Institute (F32HL074478)
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
- Health Sciences › Medicine › Epidemiology › Preterm Birth and Chorioamnionitis
- Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
- Keywords
- maternal cigarette smoking, preterm birth, smoking during pregnancy, dose-response relationship, smoking intensity, preterm birth risk factors, publication bias
- MeSH terms
- Dose-Response Relationship, Drug, Female, Gestational Age, Humans, Obstetric Labor, Premature, Pregnancy, Prospective Studies, Retrospective Studies, Smoking, Odds Ratio, Case-Control Studies, MEDLINE
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