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Impact of maternal smoking on the infant gut microbiota and its association with child overweight: a scoping review

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Abstract

Background

Childhood obesity is a growing public health concern with evidence demonstrating that while infant exposure to maternal smoking is linked to low birth weight at birth, there is a rapid catch up in weight and increased risk of obesity in later life. This scoping review aims to synthesize up-to-date evidence on the impact of maternal smoking on the infant gut microbiota and its association with child overweight.

Methods

We conducted a PRISMA-compliant scoping review. Primary population-based cohort studies published between 1900 and April 2018 were included. Relevant publications were retrieved from seven databases: PubMed, Medline, Embase, Scopus, Biosis, Cochrane library, and Web of Science Core Collection.

Results

A total of three prospective cohort studies were included which utilized high-throughput 16S rRNA gene sequencing to assess the gut microbiota and included a total of 1277 infant/neonatal participants. Neonates exposed to environmental smoke had a higher relative abundance of Ruminococcus and Akkermansia. Infants exposed to environmental smoke during pregnancy or postnatally were found to have increased gut bacterial richness, particularly Firmicutes at 3 months of age, while 6-month-old infants born to smoking mothers had an increased abundance of Bacteroides and Staphylococcus. Elevated Firmicutes richness at 3 months of age was associated with elevated odds of child overweight and obesity at 1 and 3 years of age.

Conclusion

The limited evidence to date warrants further large scale, longitudinal studies to explore the impact of maternal smoking and environmental tobacco smoke on the infant gut microbiome and its relation to child overweight.

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References

  1. de Onis M, Blossner M, Borghi E. Global prevalence and trends of overweight and obesity among preschool children. Am J Clin Nutr. 2010;92:1257–64.

    Article  CAS  PubMed  Google Scholar 

  2. World Health Organization. Childhood overweight and obesity; 2017. http://www.who.int/dietphysicalactivity/childhood/en/. Accessed 25 May 2017.

  3. Luoto R, Kalliomaki M, Laitinen K, Delzenne NM, Cani PD, Salminen S, et al. Initial dietary and microbiological environments deviate in normal-weight compared to overweight children at 10 years of age. J Pediatr Gastroenterol Nutr. 2011;52:90–5.

    Article  PubMed  Google Scholar 

  4. McCarthy A, Hughes R, Tilling K, Davies D, Smith GD, Ben-Shlomo Y. Birth weight; postnatal, infant, and childhood growth; and obesity in young adulthood: evidence from the Barry Caerphilly Growth Study. Am J Clin Nutr. 2007;86:907–13.

    Article  CAS  PubMed  Google Scholar 

  5. Parsons TJ, Power C, Manor O. Fetal and early life growth and body mass index from birth to early adulthood in 1958 British cohort: longitudinal study. BMJ. 2001;323:1331–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. 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.

    Article  PubMed  Google Scholar 

  7. Pereira PP, Da Mata FA, Figueiredo AC, de Andrade KR, Pereira MG. Maternal active smoking during pregnancy and low birth weight in the americas: a systematic review and meta-analysis. Nicotine Tob Res. 2017;19:497–505.

    Article  PubMed  Google Scholar 

  8. Ino T, Shibuya T, Saito K, Ohtani T. Effects of maternal smoking during pregnancy on body composition in offspring. Pediatr Int. 2011;53:851–7.

    Article  PubMed  Google Scholar 

  9. Oken E, Levitan EB, Gillman MW. Maternal smoking during pregnancy and child overweight: systematic review and meta-analysis. Int J Obes (Lond). 2008;32:201–10.

    Article  CAS  Google Scholar 

  10. Rayfield S, Plugge E. Systematic review and meta-analysis of the association between maternal smoking in pregnancy and childhood overweight and obesity. J Epidemiol Community Health. 2017;71:162–73.

    Article  PubMed  Google Scholar 

  11. Riedel C, Schonberger K, Yang S, Koshy G, Chen YC, Gopinath B, et al. Parental smoking and childhood obesity: higher effect estimates for maternal smoking in pregnancy compared with paternal smoking—a meta-analysis. Int J Epidemiol. 2014;43:1593–606.

    Article  PubMed  Google Scholar 

  12. Tun HM, Bridgman SL, Chari R, Field CJ, Guttman DS, Becker AB, et al. Roles of birth mode and infant gut microbiota in intergenerational transmission of overweight and obesity from mother to offspring. JAMA Pediatr. 2018;172:368–77.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Koleva PT, Kim JS, Scott JA, Kozyrskyj AL. Microbial programming of health and disease starts during fetal life. Birth Defects Res Part C Embryo Today Rev. 2015;105:265–77.

    Article  CAS  Google Scholar 

  14. Kozyrskyj AL. Can we predict future allergies from our infant gut microbiota? Expert Rev Respir Med. 2015;9:667–70.

    Article  CAS  PubMed  Google Scholar 

  15. Savin Z, Kivity S, Yonath H, Yehuda S. Smoking and the intestinal microbiome. Arch Microbiol. 2018;200:677–84.

    Article  CAS  PubMed  Google Scholar 

  16. Boulange CL, Neves AL, Chilloux J, Nicholson JK, Dumas ME. Impact of the gut microbiota on inflammation, obesity, and metabolic disease. Genome Med. 2016;8:42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Centers for Disease Control and Prevention (US); National Center for Chronic Disease Prevention and Health Promotion (US); Office on Smoking and Health (US). How tobacco smoke causes disease: the biology and behavioral basis for smoking-attributable disease: a report of the surgeon general. publications and reports of the surgeon general. Atlanta: Centers for Disease Control and Prevention (US); 2010.

    Google Scholar 

  18. Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg. 2010;8:336–41.

    Article  PubMed  Google Scholar 

  19. Wells GA, Shea B, O’Connell D, Peterson J, Welch V, Losos M. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses; 2018. http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp. Accessed 10 May 2017.

  20. Tun HM. Exposure to tobacco smoke in prenatal and early postnatal life alters infant gut microbiota and increases risk of childhood overweight. J Dev Origins Health Dis. 2017;8.

  21. Levin AM, Sitarik AR, Havstad SL, Fujimura KE, Wegienka G, Cassidy-Bushrow AE, et al. Joint effects of pregnancy, sociocultural, and environmental factors on early life gut microbiome structure and diversity. Sci Rep. 2016;6:31775.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Gosalbes MJ, Llop S, Valles Y, Moya A, Ballester F, Francino MP. Meconium microbiota types dominated by lactic acid or enteric bacteria are differentially associated with maternal eczema and respiratory problems in infants. Clin Exp Allergy. 2013;43:198–211.

    Article  CAS  PubMed  Google Scholar 

  23. England LJ, Grauman A, Qian C, Wilkins DG, Schisterman EF, Yu KF, et al. Misclassification of maternal smoking status and its effects on an epidemiologic study of pregnancy outcomes. Nicotine Tob Res. 2007;9:1005–13.

    Article  PubMed  Google Scholar 

  24. Hall ES, Wexelblatt SL, Greenberg JM. Self-reported and laboratory evaluation of late pregnancy nicotine exposure and drugs of abuse. J Perinatol. 2016;36:814–8.

    Article  CAS  PubMed  Google Scholar 

  25. Salihu HM, Aliyu MH, Pierre-Louis BJ, Alexander GR. Levels of excess infant deaths attributable to maternal smoking during pregnancy in the United States. Matern Child Health J. 2003;7:219–27.

    Article  PubMed  Google Scholar 

  26. White RA, Bjornholt JV, Baird DD, Midtvedt T, Harris JR, Pagano M, et al. Novel developmental analyses identify longitudinal patterns of early gut microbiota that affect infant growth. PLoS Comput Biol. 2013;9:e1003042.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Kalliomaki M, Collado MC, Salminen S, Isolauri E. Early differences in fecal microbiota composition in children may predict overweight. Am J Clin Nutr. 2008;87:534–8.

    Article  CAS  PubMed  Google Scholar 

  28. Stewart CJ, Auchtung TA, Ajami NJ, Velasquez K, Smith DP, De La Garza R, et al. Effects of tobacco smoke and electronic cigarette vapor exposure on the oral and gut microbiota in humans: a pilot study. PeerJ. 2018;6:e4693.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Forbes JD, Azad MB, Vehling L, Tun HM, Konya TB, Guttman DS, et al. Association of exposure to formula in the hospital and subsequent infant feeding practices with gut microbiota and risk of overweight in the first year of life. JAMA Pediatr. 2018;172:e181161.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Abbott LC, Winzer-Serhan UH. Smoking during pregnancy: lessons learned from epidemiological studies and experimental studies using animal models. Crit Rev Toxicol. 2012;42:279–303.

    Article  CAS  PubMed  Google Scholar 

  31. Wickstrom R. Effects of nicotine during pregnancy: human and experimental evidence. Curr Neuropharmacol. 2007;5:213–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Ng SP, Zelikoff JT. The effects of prenatal exposure of mice to cigarette smoke on offspring immune parameters. J Toxicol Environ Health A. 2008;71:445–53.

    Article  CAS  PubMed  Google Scholar 

  33. Gray TR, Eiden RD, Leonard KE, Connors G, Shisler S, Huestis MA. Nicotine and metabolites in meconium as evidence of maternal cigarette smoking during pregnancy and predictors of neonatal growth deficits. Nicotine Tob Res. 2010;12:658–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Wang F, Zhao H, Xiang H, Wu L, Men X, Qi C, et al. Species diversity and functional prediction of surface bacterial communities on aging flue-cured tobaccos. Curr Microbiol. 2018;75:1306–15.

    Article  CAS  PubMed  Google Scholar 

  35. Heffner LJ, Sherman CB, Speizer FE, Weiss ST. Clinical and environmental predictors of preterm labor. Obstet Gynecol. 1993;81(5 Pt 1):750–7.

    CAS  PubMed  Google Scholar 

  36. Gilbert NL, Nelson CR, Greaves L. Smoking cessation during pregnancy and relapse after childbirth in Canada. J Obstet Gynaecol Can. 2015;37:32–9.

    Article  PubMed  Google Scholar 

  37. Vurbic D, Higgins ST, McDonough SR, Skelly JM, Bernstein IM. Maternal body mass index moderates the influence of smoking cessation on breast feeding. Nicotine Tob Res. 2014;16:527–35.

    Article  PubMed  Google Scholar 

  38. Lamminpaa R, Vehvilainen-Julkunen K, Gissler M, Heinonen S. Smoking among older childbearing women—a marker of risky health behaviour a registry-based study in Finland. BMC Public Health. 2013;13:1179.

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We would like to acknowledge Linda Slater for her guidance and support in the development of search terms and search strategy.

Funding

This research was funded by Canadian Institutes of Health Research (CIHR) Microbiome Initiative (Grant no. 227312).

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Contributions

CM is the principle investigator of this review, under the supervision of ALK. In collaboration with a medical librarian, CM conducted the database search and article retrieval. CM and SJ participated in article screening and data extraction. This manuscript was drafted by CM, and critically revised by ALK and SJ. All authors have approved submission of the manuscript.

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Correspondence to Anita Kozyrskyj.

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McLean, C., Jun, S. & Kozyrskyj, A. Impact of maternal smoking on the infant gut microbiota and its association with child overweight: a scoping review. World J Pediatr 15, 341–349 (2019). https://doi.org/10.1007/s12519-019-00278-8

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  • DOI: https://doi.org/10.1007/s12519-019-00278-8

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