Associations of maternal quitting, reducing, and continuing smoking during pregnancy with longitudinal fetal growth: Findings from Mendelian randomization and parental negative control studies


Autoři: Judith S. Brand aff001;  Romy Gaillard aff004;  Jane West aff002;  Rosemary R. C. McEachan aff006;  John Wright aff006;  Ellis Voerman aff004;  Janine F. Felix aff004;  Kate Tilling aff002;  Deborah A. Lawlor aff002
Působiště autorů: Clinical Epidemiology and Biostatistics, School of Medical Sciences, Örebro University, Örebro, Sweden aff001;  MRC Integrative Epidemiology Unit, University of Bristol, Bristol, United Kingdom aff002;  Population Health Science, Bristol Medical School, University of Bristol, Bristol, United Kingdom aff003;  Generation R Study Group, Erasmus University Medical Center Rotterdam, Rotterdam, the Netherlands aff004;  Department of Pediatrics, Sophia Children’s Hospital, Erasmus University Medical Center Rotterdam, Rotterdam, the Netherlands aff005;  Bradford Institute for Health Research, Bradford Royal Infirmary, Bradford, United Kingdom aff006;  Department of Epidemiology, Erasmus University Medical Center Rotterdam, Rotterdam, the Netherlands aff007;  National Institute for Health Research Bristol Biomedical Research Centre, Bristol, United Kingdom aff008
Vyšlo v časopise: Associations of maternal quitting, reducing, and continuing smoking during pregnancy with longitudinal fetal growth: Findings from Mendelian randomization and parental negative control studies. PLoS Med 16(11): e1002972. doi:10.1371/journal.pmed.1002972
Kategorie: Research Article
doi: 10.1371/journal.pmed.1002972

Souhrn

Background

Maternal smoking during pregnancy is an established risk factor for low infant birth weight, but evidence on critical exposure windows and timing of fetal growth restriction is limited. Here we investigate the associations of maternal quitting, reducing, and continuing smoking during pregnancy with longitudinal fetal growth by triangulating evidence from 3 analytical approaches to strengthen causal inference.

Methods and findings

We analysed data from 8,621 European liveborn singletons in 2 population-based pregnancy cohorts (the Generation R Study, the Netherlands 2002–2006 [n = 4,682]) and the Born in Bradford study, United Kingdom 2007–2010 [n = 3,939]) with fetal ultrasound and birth anthropometric measures, parental smoking during pregnancy, and maternal genetic data. Associations with trajectories of estimated fetal weight (EFW) and individual fetal parameters (head circumference, femur length [FL], and abdominal circumference [AC]) from 12–16 to 40 weeks’ gestation were analysed using multilevel fractional polynomial models. We compared results from (1) confounder-adjusted multivariable analyses, (2) a Mendelian randomization (MR) analysis using maternal rs1051730 genotype as an instrument for smoking quantity and ease of quitting, and (3) a negative control analysis comparing maternal and mother’s partner’s smoking associations. In multivariable analyses, women who continued smoking during pregnancy had a smaller fetal size than non-smokers from early gestation (16–20 weeks) through to birth (p-value for each parameter < 0.001). Fetal size reductions in continuing smokers followed a dose-dependent pattern (compared to non-smokers, difference in mean EFW [95% CI] at 40 weeks’ gestation was −144 g [−182 to −106], −215 g [−248 to −182], and −290 g [−334 to −247] for light, moderate, and heavy smoking, respectively). Overall, fetal size reductions were most pronounced for FL. The fetal growth trajectory in women who quit smoking in early pregnancy was similar to that of non-smokers, except for a shorter FL and greater AC around 36–40 weeks’ gestation. In MR analyses, each genetically determined 1-cigarette-per-day increase was associated with a smaller EFW from 20 weeks’ gestation to birth in smokers (p = 0.01, difference in mean EFW at 40 weeks = −45 g [95% CI −81 to −10]) and a greater EFW from 32 weeks’ gestation onwards in non-smokers (p = 0.03, difference in mean EFW at 40 weeks = 26 g [95% CI 5 to 47]). There was no evidence that partner smoking was associated with fetal growth. Study limitations include measurement error due to maternal self-report of smoking and the modest sample size for MR analyses resulting in unconfounded estimates being less precise. The apparent positive association of the genetic instrument with fetal growth in non-smokers suggests that genetic pleiotropy may have masked a stronger association in smokers.

Conclusions

A consistent linear dose-dependent association of maternal smoking with fetal growth was observed from the early second trimester onwards, while no major growth deficit was found in women who quit smoking early in pregnancy except for a shorter FL during late gestation. These findings reinforce the importance of smoking cessation advice in preconception and antenatal care and show that smoking reduction can lower the risk of impaired fetal growth in women who struggle to quit.

Klíčová slova:

Alcohols – Birth weight – Body mass index – Educational attainment – Infants – Pregnancy – Smoking habits – Variant genotypes


Zdroje

1. Cnattingius S. The epidemiology of smoking during pregnancy: smoking prevalence, maternal characteristics, and pregnancy outcomes. Nicotine Tob Res. 2004;6(Suppl 2):S125–40. doi: 10.1080/14622200410001669187 15203816

2. Lange S, Probst C, Rehm J, Popova S. National, regional, and global prevalence of smoking during pregnancy in the general population: a systematic review and meta-analysis. Lancet Glob Health. 2018;6:e769–76. doi: 10.1016/S2214-109X(18)30223-7 29859815

3. Office of the Surgeon General, Office on Smoking and Health. The health consequences of smoking: a report of the Surgeon General. Atlanta: Centers for Disease Control and Prevention; 2004.

4. Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health. How tobacco smoke causes disease—the biology and behavioral basis for smoking-attributable disease: a report of the Surgeon General. Atlanta: Centers for Disease Control and Prevention; 2010.

5. Sexton M, Hebel JR. A clinical trial of change in maternal smoking and its effect on birth weight. JAMA. 1984;251:911–5. 6363731

6. Faber T, Kumar A, Mackenbach JP, Millett C, Basu S, Sheikh A, et al. Effect of tobacco control policies on perinatal and child health: a systematic review and meta-analysis. Lancet Public Health. 2017;2:e420–37. doi: 10.1016/S2468-2667(17)30144-5 28944313

7. Hawkins SS, Baum CF, Oken E, Gillman MW. Associations of tobacco control policies with birth outcomes. JAMA Pediatr. 2014;168:e142365. doi: 10.1001/jamapediatrics.2014.2365 25365250

8. Tyrrell J, Huikari V, Christie JT, Cavadino A, Bakker R, Brion MJ, et al. Genetic variation in the 15q25 nicotinic acetylcholine receptor gene cluster (CHRNA5-CHRNA3-CHRNB4) interacts with maternal self-reported smoking status during pregnancy to influence birth weight. Hum Mol Genet. 2012;21:5344–58. doi: 10.1093/hmg/dds372 22956269

9. Smith GD. Assessing intrauterine influences on offspring health outcomes: can epidemiological studies yield robust findings? Basic Clin Pharmacol Toxicol. 2008;102:245–56. doi: 10.1111/j.1742-7843.2007.00191.x 18226080

10. Kuja-Halkola R, D’Onofrio BM, Larsson H, Lichtenstein P. Maternal smoking during pregnancy and adverse outcomes in offspring: genetic and environmental sources of covariance. Behav Genet. 2014;44:456–67. doi: 10.1007/s10519-014-9668-4 25117564

11. Mook-Kanamori DO, Steegers EA, Eilers PH, Raat H, Hofman A, Jaddoe VW. Risk factors and outcomes associated with first-trimester fetal growth restriction. JAMA. 2010;303:527–34. doi: 10.1001/jama.2010.78 20145229

12. Abraham M, Alramadhan S, Iniguez C, Duijts L, Jaddoe VW, Den Dekker HT, et al. A systematic review of maternal smoking during pregnancy and fetal measurements with meta-analysis. PLoS ONE. 2017;12(2): e0170946. doi: 10.1371/journal.pone.0170946 28231292

13. Lawlor DA, Tilling K, Davey Smith G. Triangulation in aetiological epidemiology. Int J Epidemiol. 2016;45:1866–86. doi: 10.1093/ije/dyw314 28108528

14. Jaddoe VW, Mackenbach JP, Moll HA, Steegers EA, Tiemeier H, Verhulst FC, et al. The Generation R Study: design and cohort profile. Eur J Epidemiol. 2006;21:475–84. doi: 10.1007/s10654-006-9022-0 16826450

15. Wright J, Small N, Raynor P, Tuffnell D, Bhopal R, Cameron N, et al. Cohort profile: the Born in Bradford multi-ethnic family cohort study. Int J Epidemiol. 2013;42:978–91. doi: 10.1093/ije/dys112 23064411

16. Sanderson E, Macdonald-Wallis C, Davey Smith G. Negative control exposure studies in the presence of measurement error: implications for attempted effect estimate calibration. Int J Epidemiol. 2018;47:587–96. doi: 10.1093/ije/dyx213 29088358

17. Thorgeirsson TE, Geller F, Sulem P, Rafnar T, Wiste A, Magnusson KP, et al. A variant associated with nicotine dependence, lung cancer and peripheral arterial disease. Nature. 2008;452:638–42. doi: 10.1038/nature06846 18385739

18. Thorgeirsson TE, Gudbjartsson DF, Surakka I, Vink JM, Amin N, Geller F, et al. Sequence variants at CHRNB3-CHRNA6 and CYP2A6 affect smoking behavior. Nat Genet. 2010;42:448–53. doi: 10.1038/ng.573 20418888

19. Freathy RM, Ring SM, Shields B, Galobardes B, Knight B, Weedon MN, et al. A common genetic variant in the 15q24 nicotinic acetylcholine receptor gene cluster (CHRNA5-CHRNA3-CHRNB4) is associated with a reduced ability of women to quit smoking in pregnancy. Hum Mol Genet. 2009;18:2922–7. doi: 10.1093/hmg/ddp216 19429911

20. Jaddoe VW, Verburg BO, de Ridder MA, Hofman A, Mackenbach JP, Moll HA, et al. Maternal smoking and fetal growth characteristics in different periods of pregnancy: the generation R study. Am J Epidemiol. 2007;165:1207–15. doi: 10.1093/aje/kwm014 17329715

21. Brand JS, West J, Tuffnell D, Bird PK, Wright J, Tilling K, et al. Gestational diabetes and ultrasound-assessed fetal growth in South Asian and White European women: findings from a prospective pregnancy cohort. BMC Med. 2018;16:203. doi: 10.1186/s12916-018-1191-7 30396349

22. Royal College of Obstetricians and Gynaecologists. Routine ultrasound screening in pregnancy: protocol. London: RCOG Press; 2000.

23. Hadlock FP, Harrist RB, Sharman RS, Deter RL, Park SK. Estimation of fetal weight with the use of head, body, and femur measurements—a prospective study. Am J Obstet Gynecol. 1985;151:333–7. doi: 10.1016/0002-9378(85)90298-4 3881966

24. Munafo MR, Timofeeva MN, Morris RW, Prieto-Merino D, Sattar N, Brennan P, et al. Association between genetic variants on chromosome 15q25 locus and objective measures of tobacco exposure. J Natl Cancer Inst. 2012;104:740–8. doi: 10.1093/jnci/djs191 22534784

25. Davey Smith G, Hemani G. Mendelian randomization: genetic anchors for causal inference in epidemiological studies. Hum Mol Genet. 2014;23:R89–98. doi: 10.1093/hmg/ddu328 25064373

26. Pearce N, Lawlor DA. Causal inference-so much more than statistics. Int J Epidemiol. 2016;45:1895–903. doi: 10.1093/ije/dyw328 28204514

27. Asvold BO, Bjorngaard JH, Carslake D, Gabrielsen ME, Skorpen F, Smith GD, et al. Causal associations of tobacco smoking with cardiovascular risk factors: a Mendelian randomization analysis of the HUNT Study in Norway. Int J Epidemiol. 2014;43:1458–70. doi: 10.1093/ije/dyu113 24867305

28. Morris RW, Taylor AE, Fluharty ME, Bjorngaard JH, Asvold BO, Elvestad Gabrielsen M, et al. Heavier smoking may lead to a relative increase in waist circumference: evidence for a causal relationship from a Mendelian randomisation meta-analysis. The CARTA consortium. BMJ Open. 2015;5:e008808. doi: 10.1136/bmjopen-2015-008808 26264275

29. Shisler S, Eiden RD, Molnar DS, Schuetze P, Huestis M, Homish G. Smoking in pregnancy and fetal growth: the case for more intensive assessment. Nicotine Tob Res. 2017;19:525–31. doi: 10.1093/ntr/ntx018 28403474

30. Pickett KE, Kasza K, Biesecker G, Wright RJ, Wakschlag LS. Women who remember, women who do not: a methodological study of maternal recall of smoking in pregnancy. Nicotine Tob Res. 2009;11:1166–74. doi: 10.1093/ntr/ntp117 19640836

31. Sharp GC, Lawlor DA, Richardson SS. It’s the mother!: how assumptions about the causal primacy of maternal effects influence research on the developmental origins of health and disease. Soc Sci Med. 2018;213:20–7. doi: 10.1016/j.socscimed.2018.07.035 30055422

32. Bernstein IM, Goran MI, Amini SB, Catalano PM. Differential growth of fetal tissues during the second half of pregnancy. Am J Obstet Gynecol. 1997;176:28–32. doi: 10.1016/s0002-9378(97)80006-3 9024084

33. Iniguez C, Ballester F, Costa O, Murcia M, Souto A, Santa-Marina L, et al. Maternal smoking during pregnancy and fetal biometry: the INMA Mother and Child Cohort Study. Am J Epidemiol. 2013;178:1067–75. doi: 10.1093/aje/kwt085 24008909

34. Pringle PJ, Geary MP, Rodeck CH, Kingdom JC, Kayamba-Kay’s S, Hindmarsh PC. The influence of cigarette smoking on antenatal growth, birth size, and the insulin-like growth factor axis. J Clin Endocrinol Metab. 2005;90:2556–62. doi: 10.1210/jc.2004-1674 15713720

35. Prabhu N, Smith N, Campbell D, Craig LC, Seaton A, Helms PJ, et al. First trimester maternal tobacco smoking habits and fetal growth. Thorax. 2010;65:235–40. doi: 10.1136/thx.2009.123232 20335293

36. Esposito ER, Horn KH, Greene RM, Pisano MM. An animal model of cigarette smoke-induced in utero growth retardation. Toxicology. 2008;246:193–202. doi: 10.1016/j.tox.2008.01.014 18316152

37. Li L, Dangour AD, Power C. Early life influences on adult leg and trunk length in the 1958 British birth cohort. Am J Hum Biol. 2007;19:836–43. doi: 10.1002/ajhb.20649 17696141

38. Lindley AA, Becker S, Gray RH, Herman AA. Effect of continuing or stopping smoking during pregnancy on infant birth weight, crown-heel length, head circumference, ponderal index, and brain:body weight ratio. Am J Epidemiol. 2000;152:219–25. doi: 10.1093/aje/152.3.219 10933268

39. Hadlock FP, Deter RL, Roecker E, Harrist RB, Park SK. Relation of fetal femur length to neonatal crown-heel length. J Ultrasound Med. 1984;3:1–3.

40. Andersen MR, Simonsen U, Uldbjerg N, Aalkjaer C, Stender S. Smoking cessation early in pregnancy and birth weight, length, head circumference, and endothelial nitric oxide synthase activity in umbilical and chorionic vessels: an observational study of healthy singleton pregnancies. Circulation. 2009;119:857–64. doi: 10.1161/CIRCULATIONAHA.107.755769 19188513

41. Pisinger C, Jorgensen T. Waist circumference and weight following smoking cessation in a general population: the Inter99 study. Prev Med. 2007;44:290–5. doi: 10.1016/j.ypmed.2006.11.015 17222450

42. Aubin HJ, Farley A, Lycett D, Lahmek P, Aveyard P. Weight gain in smokers after quitting cigarettes: meta-analysis. BMJ. 2012;345:e4439. doi: 10.1136/bmj.e4439 22782848

43. Solomon L, Quinn V. Spontaneous quitting: self-initiated smoking cessation in early pregnancy. Nicotine Tob Res. 2004;6(Suppl 2):S203–16. doi: 10.1080/14622200410001669132 15203822

44. World Health Organization. WHO recommendations for the prevention and management of tobacco use and second-hand smoke exposure in pregnancy. Geneva: World Health Organization; 2013.

45. Siu AL, U.S. Preventive Services Task Force. Behavioral and pharmacotherapy interventions for tobacco smoking cessation in adults, including pregnant women: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med. 2015;163:622–34. doi: 10.7326/M15-2023 26389730

46. National Institute for Health and Care Excellence. Smoking: stopping in pregnancy and after childbirth. Public health guideline [PH26]. London: National Institute for Health and Care Excellence; 2010 [cited 2019 Oct 23]. Available from: http://www.nice.org.uk/PH26.

47. Haddad A, Davis AM. Tobacco smoking cessation in adults and pregnant women: behavioral and pharmacotherapy interventions. JAMA. 2016;315:2011–12. doi: 10.1001/jama.2016.2535 27163990

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Interní lékařství

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2019 Číslo 11

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