Maternal smoking during pregnancy increases the risk of gut microbiome-associated childhood overweight and obesity

References

• World Health Organization. Fact sheets on obesity and overweight available from https://www.who.int/news-room/fact-sheets/detail/obesity-and-overweight#:~:text=Key%20facts,has%20nearly%20tripled%20since%201975.&text=39%20million%20children%20under%20the,overweight%20or%20obese%20in%202016.
   Google Scholar
• Ezzati M, Bentham J, Di Cesare M, Bilano V, Bixby H, Zhou B, Adams RJ, Aekplakorn W, Afsana K, Aguilar-Salinas CA. et al. Worldwide trends in body-mass index, underweight, overweight, and obesity from 1975 to 2016: a pooled analysis of 2416 population-based measurement studies in 128·9 million children, adolescents, and adults. Lancet. 2017;390(10113):2627–18. doi:10.1016/S0140-6736(17)32129-3.
   PubMed Web of Science ®Google Scholar
• World Health Organization. Taking action on childhood obesity (2018). https://apps.who.int/iris/handle/10665/274792.
   Google Scholar
• Lin X, Li H. Obesity: epidemiology, pathophysiology, and therapeutics. Front Endocrinol (Lausanne). 2021;12:706978. doi:10.3389/fendo.2021.706978.
   PubMed Web of Science ®Google Scholar
• Hruby A, Hu FB. The epidemiology of obesity: a big picture. Pharmacoeconomics. 2015;33(7):673–89. doi:10.1007/s40273-014-0243-x.
   PubMed Web of Science ®Google Scholar
• Jaakkola JM, Rovio SP, Pahkala K, Viikari J, Ronnemaa T, Jula A, Niinikoski H, Mykkänen J, Juonala M, Hutri-Kähönen N. et al. Childhood exposure to parental smoking and life-course overweight and central obesity. Ann Med. 2021;53(1):208–16. doi:10.1080/07853890.2020.1853215.
   PubMed Web of Science ®Google Scholar
• Riedel C, Schonberger K, Yang S, Koshy G, Chen YC, Gopinath B, Ziebarth S, von Kries R. 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(5):1593–1606. doi:10.1093/ije/dyu150.
   PubMed Web of Science ®Google Scholar
• von Kries R, Toschke AM, Koletzko B, Slikker W Jr. Maternal smoking during pregnancy and childhood obesity. Am J Epidemiol. 2002;156(10):954–961. doi:10.1093/aje/kwf128.
   PubMed Web of Science ®Google Scholar
• Zhao L. The gut microbiota and obesity: from correlation to causality. Nat Rev Microbiol. 2013;11(9):639–47. doi:10.1038/nrmicro3089.
   PubMed Web of Science ®Google Scholar
• Crovesy L, Masterson D, Rosado EL. Profile of the gut microbiota of adults with obesity: a systematic review. Eur J Clin Nutr. 2020;74(9):1251–62. doi:10.1038/s41430-020-0607-6.
   PubMed Web of Science ®Google Scholar
• de Cuevillas B, Milagro FI, Tur JA, Gil-Campos M, de Miguel-Etayo P, Martinez JA, de Cuevillas B, de Miguel‐Etayo P, Navas‐Carretero S. Fecal microbiota relationships with childhood obesity: a scoping comprehensive review. Obes Rev. 2022;23(Suppl 1):e13394. doi:10.1111/obr.13394.
   PubMedGoogle Scholar
• Lee P, Yacyshyn BR, Yacyshyn MB. Gut microbiota and obesity: an opportunity to alter obesity through faecal microbiota transplant (FMT). Diabetes Obes Metab. 2019;21(3):479–90. doi:10.1111/dom.13561.
   PubMed Web of Science ®Google Scholar
• Jian C, Carpen N, Helve O, de Vos WM, Korpela K, Salonen A. Early-life gut microbiota and its connection to metabolic health in children: perspective on ecological drivers and need for quantitative approach. EBioMedicine. 2021;69:103475. doi:10.1016/j.ebiom.2021.103475.
   PubMed Web of Science ®Google Scholar
• Tun MH, Tun HM, Mahoney JJ, Konya TB, Guttman DS, Becker AB, Mandhane PJ, Turvey SE, Subbarao P, Sears MR. et al. Postnatal exposure to household disinfectants, infant gut microbiota and subsequent risk of overweight in children. CMAJ. 2018;190(37):E1097–E1107. doi:10.1503/cmaj.170809.
   PubMed Web of Science ®Google Scholar
• Forbes JD, Azad MB, Vehling L, Tun HM, Konya TB, Guttman DS, Field CJ, Lefebvre D, Sears MR, Becker AB. 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(7):172. doi:10.1001/jamapediatrics.2018.1161.
   Web of Science ®Google Scholar
• Tun HM, Bridgman SL, Chari R, Field CJ, Guttman DS, Becker AB, Mandhane PJ, Turvey SE, Subbarao P, Sears MR. 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(4):368–77. doi:10.1001/jamapediatrics.2017.5535.
   PubMed Web of Science ®Google Scholar
• Vu K, Lou W, Tun HM, Konya TB, Morales-Lizcano N, Chari RS, Field CJ, Guttman DS, Mandal R, Wishart DS. et al. From birth to overweight and atopic disease: multiple and common pathways of the infant gut microbiome. Gastroenterology. 2021;160(1):128–44 e10. doi:10.1053/j.gastro.2020.08.053.
   PubMed Web of Science ®Google Scholar
• Tun HM, Peng Y, Chen B, Konya TB, Morales-Lizcano NP, Chari R, Field CJ, Guttman DS, Becker AB, Mandhane PJ. et al. Ethnicity associations with food sensitization are mediated by gut microbiota development in the first year of life. Gastroenterology. 2021;161(1):94–106. doi:10.1053/j.gastro.2021.03.016.
   PubMed Web of Science ®Google Scholar
• Reyna ME, Petersen C, Dai DLY, Dai R, Becker AB, Azad MB, Miliku K, Lefebvre DL, Moraes TJ, Mandhane PJ. et al. Longitudinal body mass index trajectories at preschool age: children with rapid growth have differential composition of the gut microbiota in the first year of life. Int J Obes (Lond). 2022;46(7):1351–1358. doi:10.1038/s41366-022-01117-z.
   PubMed Web of Science ®Google Scholar
• 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. 2019;15(4):341–9. doi:10.1007/s12519-019-00278-8.
   PubMed Web of Science ®Google Scholar
• Levin AM, Sitarik AR, Havstad SL, Fujimura KE, Wegienka G, Cassidy-Bushrow AE, Kim H, Zoratti EM, Lukacs NW, Boushey HA. et al. Joint effects of pregnancy, sociocultural, and environmental factors on early life gut microbiome structure and diversity. Sci Rep. 2016;6(1):31775. doi:10.1038/srep31775.
   PubMed Web of Science ®Google Scholar
• Gschwendtner S, Kang H, Thiering E, Kublik S, Fosel B, Schulz H, Krauss-Etschmann S, Heinrich J, Schöler A, Schloter M. et al. Early life determinants induce sustainable changes in the gut microbiome of six-year-old children. Sci Rep. 2019;9(1):12675. doi:10.1038/s41598-019-49160-7.
   PubMedGoogle Scholar
• Parada Venegas D, la Fuente MK D, Landskron G, Gonzalez MJ, Quera R, Dijkstra G, Harmsen HJM, Faber KN, Hermoso MA. Short chain fatty acids (SCFAs)-mediated gut epithelial and immune regulation and its relevance for inflammatory bowel diseases. Front Immunol. 2019;10:277. doi:10.3389/fimmu.2019.00277.
   PubMed Web of Science ®Google Scholar
• Canfora EE, Meex RCR, Venema K, Blaak EE. Gut microbial metabolites in obesity, NAFLD and T2DM. Nat Rev Endocrinol. 2019;15(5):261–73. doi:10.1038/s41574-019-0156-z.
   PubMed Web of Science ®Google Scholar
• Nandy D, Craig SJC, Cai J, Tian Y, Paul IM, Savage JS, Marini ME, Hohman EE, Reimherr ML, Patterson AD. et al. Metabolomic profiling of stool of two-year old children from the INSIGHT study reveals links between butyrate and child weight outcomes. Pediatr Obes. 2022;17(1):e12833. doi:10.1111/ijpo.12833.
   PubMed Web of Science ®Google Scholar
• Schwiertz A, Taras D, Schafer K, Beijer S, Bos NA, Donus C, Hardt PD. Microbiota and SCFA in lean and overweight healthy subjects. Obesity (Silver Spring). 2010;18(1):190–195. doi:10.1038/oby.2009.167.
   PubMed Web of Science ®Google Scholar
• Teixeira TF, Grzeskowiak L, Franceschini SC, Bressan J, Ferreira CL, Peluzio MC. Higher level of faecal SCFA in women correlates with metabolic syndrome risk factors. Br J Nutr. 2013;109(5):914–919. doi:10.1017/S0007114512002723.
   PubMed Web of Science ®Google Scholar
• Jian C, Silvestre MP, Middleton D, Korpela K, Jalo E, Broderick D, de Vos WM, Fogelholm M, Taylor MW, Raben A. et al. Gut microbiota predicts body fat change following a low-energy diet: a PREVIEW intervention study. Genome Med. 2022;14(1):54. doi:10.1186/s13073-022-01053-7.
   PubMed Web of Science ®Google Scholar
• Bridgman SL, Malmuthuge N, Mandal R, Field CJ, Haqq AM, Mandhane PJ, Moraes TJ, Turvey SE, Simons E, Subbarao P. et al. Childhood body mass index and associations with infant gut metabolites and secretory IgA: findings from a prospective cohort study. Int J Obes (Lond). 2022;46(9):1712–1719. doi:10.1038/s41366-022-01183-3.
   PubMed Web of Science ®Google Scholar
• Liu H, Wang J, He T, Becker S, Zhang G, Li D, Ma X. Butyrate: a double-edged sword for health? Adv Nutr. 2018;9(1):21–29. doi:10.1093/advances/nmx009.
   PubMed Web of Science ®Google Scholar
• Miletta MC, Petkovic V, Eble A, Ammann RA, Fluck CE, Mullis PE, Blachier F. Butyrate increases intracellular calcium levels and enhances growth hormone release from rat anterior pituitary cells via the G-protein-coupled receptors GPR41 and 43. PloS One. 2014;9(10):e107388. doi:10.1371/journal.pone.0107388.
   PubMed Web of Science ®Google Scholar
• Rasmussen MH. Obesity, growth hormone and weight loss. Mol Cell Endocrinol. 2010;316(2):147–53. doi:10.1016/j.mce.2009.08.017.
   PubMed Web of Science ®Google Scholar
• Reinehr T, Lindberg A, Koltowska-Haggstrom M, Ranke M. Is growth hormone treatment in children associated with weight gain?–longitudinal analysis of KIGS data. Clin Endocrinol (Oxf). 2014;81(5):721–6. doi:10.1111/cen.12464.
   PubMed Web of Science ®Google Scholar
• Backhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, Li Y, Xia Y, Xie H, Zhong H. et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe. 2015;17(5):690–703. doi:10.1016/j.chom.2015.04.004.
   PubMed Web of Science ®Google Scholar
• Subramanian S, Huq S, Yatsunenko T, Haque R, Mahfuz M, Alam MA, Benezra A, DeStefano J, Meier MF, Muegge BD. et al. Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature. 2014;510(7505):417–21. doi:10.1038/nature13421.
   PubMed Web of Science ®Google Scholar
• Fehr K, Moossavi S, Sbihi H, Boutin RCT, Bode L, Robertson B, Yonemitsu C, Field CJ, Becker AB, Mandhane PJ. et al. Breastmilk feeding practices are associated with the Co-occurrence of bacteria in mothers’ milk and the infant gut: the CHILD cohort study. Cell Host Microbe. 2020;28(2):285–297.e4. doi:10.1016/j.chom.2020.06.009.
   PubMed Web of Science ®Google Scholar
• Azad MB, Vehling L, Chan D, Klopp A, Nickel NC, McGavock JM, Becker AB, Mandhane PJ, Turvey SE, Moraes TJ. et al. Infant feeding and weight gain: separating breast milk from breastfeeding and formula from food. Pediatrics. 2018;142(4):142. doi:10.1542/peds.2018-1092.
   Web of Science ®Google Scholar
• Huang S, Mao J, Zhou L, Xiong X, Deng Y. The imbalance of gut microbiota and its correlation with plasma inflammatory cytokines in pemphigus vulgaris patients. Scand J Immunol. 2019;90(3):e12799. doi:10.1111/sji.12799.
   PubMed Web of Science ®Google Scholar
• Romani L, Del Chierico F, Chiriaco M, Foligno S, Reddel S, Salvatori G, Cifaldi C, Faraci S, Finocchi A, Rossi P. et al. Gut mucosal and fecal microbiota profiling combined to intestinal immune system in neonates affected by intestinal ischemic injuries. Front Cell Infect Microbiol. 2020;10:59. doi:10.3389/fcimb.2020.00059.
   PubMed Web of Science ®Google Scholar
• Kasabreh N. Smoking Thirties: How Tobacco & BMI Shape the Subgingival Microbiome. Dentistry. OhioLINK Electronic Theses and Dissertations Center. Ohio State University, 2019:100.
   Google Scholar
• Chen X, Sun H, Jiang F, Shen Y, Li X, Hu X, Shen X, Wei P. Alteration of the gut microbiota associated with childhood obesity by 16S rRNA gene sequencing. PeerJ. 2020;8:e8317. doi:10.7717/peerj.8317.
   PubMed Web of Science ®Google Scholar
• Gacesa R, Kurilshikov A, Vich Vila A, Sinha T, Klaassen MAY, Bolte LA, Andreu-Sánchez S, Chen L, Collij V, Hu S. et al. Environmental factors shaping the gut microbiome in a Dutch population. Nature. 2022;604(7907):732–9. doi:10.1038/s41586-022-04567-7.
   PubMed Web of Science ®Google Scholar
• Lozano CP, Wilkens LR, Shvetsov YB, Maskarinec G, Park SY, Shepherd JA, Boushey CJ, Hebert JR, Wirth MD, Ernst T. et al. Associations of the dietary inflammatory index with total adiposity and ectopic fat through the gut microbiota, LPS, and C-reactive protein in the multiethnic cohort–adiposity phenotype study. Am J Clin Nutr. 2022;115(5):1344–1356. doi:10.1093/ajcn/nqab398.
   PubMed Web of Science ®Google Scholar
• Philips EM, Santos S, Trasande L, Aurrekoetxea JJ, Barros H, von Berg A, Bergström A, Bird PK, Brescianini S, Ní Chaoimh C. et al. Changes in parental smoking during pregnancy and risks of adverse birth outcomes and childhood overweight in Europe and North America: an individual participant data meta-analysis of 229,000 singleton births. PLoS Med. 2020;17(8):e1003182. doi:10.1371/journal.pmed.1003182.
   PubMed Web of Science ®Google Scholar
• Nakamura A, Francois O, Lepeule J. Epigenetic Alterations of Maternal Tobacco Smoking during Pregnancy: A Narrative Review. Int J Environ Res Public Health. 2021;18(10):18. doi:10.3390/ijerph18105083.
   Web of Science ®Google Scholar
• de Prado-Bert P, Ruiz-Arenas C, Vives-Usano M, Andrusaityte S, Cadiou S, Carracedo Á, de Prado-Bert A, Casas M, Chatzi L, Dadvand P. et al. The early-life exposome and epigenetic age acceleration in children. Environ Int. 2021;155:106683. doi:10.1016/j.envint.2021.106683.
   PubMed Web of Science ®Google Scholar
• Stockinger B, Shah K, Wincent E. AHR in the intestinal microenvironment: safeguarding barrier function. Nat Rev Gastroenterol Hepatol. 2021;18(8):559–70. doi:10.1038/s41575-021-00430-8.
   PubMed Web of Science ®Google Scholar
• Korecka A, Dona A, Lahiri S, Tett AJ, Al-Asmakh M, Braniste V, D’Arienzo R, Abbaspour A, Reichardt N, Fujii-Kuriyama Y. et al. Bidirectional communication between the aryl hydrocarbon receptor (AhR) and the microbiome tunes host metabolism. Npj Biofilms Microbiomes. 2016;2(1):16014. doi:10.1038/npjbiofilms.2016.14.
   PubMedGoogle Scholar
• Group WHOMGRS. WHO child growth standards based on length/height, weight and age. Acta Paediatr Suppl. 2006;450:76–85. doi:10.1111/j.1651-2227.2006.tb02378.x.
   PubMedGoogle Scholar
• Azad MB, Konya T, Maughan H, Guttman DS, Field CJ, Chari RS, Sears MR, Becker AB, Scott JA, Kozyrskyj AL. et al. Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. CMAJ. 2013;185(5):385–94. doi:10.1503/cmaj.121189.
   PubMed Web of Science ®Google Scholar
• Bolyen E, Rideout JR, Dillon MR, Bokulich N, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F. et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37(8):852–7. doi:10.1038/s41587-019-0209-9.
   PubMed Web of Science ®Google Scholar
• Douglas GM, Maffei VJ, Zaneveld JR, Yurgel SN, Brown JR, Taylor CM, Huttenhower C, Langille MGI. PICRUSt2 for prediction of metagenome functions. Nat Biotechnol. 2020;38(6):685–688. doi:10.1038/s41587-020-0548-6.
   PubMed Web of Science ®Google Scholar
• Caspi R, Billington R, Ferrer L, Foerster H, Fulcher CA, Keseler IM, Kothari A, Krummenacker M, Latendresse M, Mueller LA. et al. The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res. 2016;44(D1):D471–80. doi:10.1093/nar/gkv1164.
   PubMed Web of Science ®Google Scholar
• Drall KM, Tun HM, Morales-Lizcano NP, Konya TB, Guttman DS, Field CJ, Mandal R, Wishart DS, Becker AB, Azad MB. et al. Clostridioides difficile colonization is differentially associated with gut microbiome profiles by infant feeding modality at 3–4 months of age. Front Immunol. 2019;10:2866. doi:10.3389/fimmu.2019.02866.
   PubMed Web of Science ®Google Scholar
• Parks J, McLean KE, McCandless L, de Souza RJ, Brook JR, Scott J, Turvey SE, Mandhane PJ, Becker AB, Azad MB. et al. Assessing secondhand and thirdhand tobacco smoke exposure in Canadian infants using questionnaires, biomarkers, and machine learning. J Expo Sci Environ Epidemiol. 2022;32(1):112–23. doi:10.1038/s41370-021-00350-4.
   PubMed Web of Science ®Google Scholar
• Alli BY. InteractionR: an R package for full reporting of effect modification and interaction. Softw Impacts. 2021;10:100147. doi:10.1016/j.simpa.2021.100147.
   Google Scholar
• Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12(6):12. doi:10.1186/gb-2011-12-6-r60.
   Web of Science ®Google Scholar
• Tingley D, Yamamoto T, Hirose K, Keele L, Imai K. Mediation: R package for causal mediation analysis. J Stat Softw. 2014;59(5):1–38. doi:10.18637/jss.v059.i05.
   PubMed Web of Science ®Google Scholar
• Fong C, Ratkovic M, Imai K. CBPS: covariate balancing propensity score. R package version 0.23 (2022). Available from https://CRAN.R-project.org/package=CBPS.
   Google Scholar
• Yu Q, Li B. Mma: multiple mediation analysis. R package version 10.7-1 (2023). Available from https://CRAN.R-project.org/package=mma.
   Google Scholar
• Brandao Gois MF, Sinha T, Spreckels JE, Vich Vila A, Bolte LA, Weersma RK, Wijmenga C, Fu J, Zhernakova A, Kurilshikov A. et al. Role of the gut microbiome in mediating lactose intolerance symptoms. Gut. 2022;71(1):215–7. doi:10.1136/gutjnl-2020-323911.
   PubMed Web of Science ®Google Scholar