2,122
Views
0
CrossRef citations to date
0
Altmetric
Research Paper

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

ORCID Icon, ORCID Icon, , , , , , , , , , , , , , & ORCID Icon show all
Article: 2323234 | Received 14 Sep 2023, Accepted 21 Feb 2024, Published online: 04 Mar 2024

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.
  • 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.
  • World Health Organization. Taking action on childhood obesity (2018). https://apps.who.int/iris/handle/10665/274792.
  • Lin X, Li H. Obesity: epidemiology, pathophysiology, and therapeutics. Front Endocrinol (Lausanne). 2021;12:706978. doi:10.3389/fendo.2021.706978.
  • Hruby A, Hu FB. The epidemiology of obesity: a big picture. Pharmacoeconomics. 2015;33(7):673–89. doi:10.1007/s40273-014-0243-x.
  • 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.
  • 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.
  • 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.
  • Zhao L. The gut microbiota and obesity: from correlation to causality. Nat Rev Microbiol. 2013;11(9):639–47. doi:10.1038/nrmicro3089.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • Rasmussen MH. Obesity, growth hormone and weight loss. Mol Cell Endocrinol. 2010;316(2):147–53. doi:10.1016/j.mce.2009.08.017.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • Kasabreh N. Smoking Thirties: How Tobacco & BMI Shape the Subgingival Microbiome. Dentistry. OhioLINK Electronic Theses and Dissertations Center. Ohio State University, 2019:100.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • Yu Q, Li B. Mma: multiple mediation analysis. R package version 10.7-1 (2023). Available from https://CRAN.R-project.org/package=mma.
  • 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.