Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Pediatrics

Association between cesarean delivery types and obesity in preadolescence

International Journal of Obesity volume 44, pages 2023–2034 (2020)Cite this article

Subjects

Abstract

Background/objectives

The association between mode of delivery and childhood obesity remains inconclusive. Because few studies have separated C-section types (planned or unplanned C-section), our objective was to assess how these subtypes relate to preadolescent obesity.

Subjects/methods

The study consisted of 570 maternal–child pairs drawn from the WHEALS birth cohort based in Detroit, Michigan. Children were followed-up at 10 years of age where a variety of anthropometric measurements were collected. Obesity was defined based on BMI percentile (≥95th percentile), as well as through Gaussian finite mixture modeling on the anthropometric measurements. Risk ratios (RRs) and 95% confidence intervals (CIs) for obesity comparing planned and unplanned C-sections to vaginal deliveries were computed, which utilized inverse probability weights to account for loss to follow-up and multiple imputation for covariate missingness. Mediation models were fit to examine the mediation role of breastfeeding.

Results

After adjusting for marital status, maternal race, prenatal tobacco smoke exposure, maternal age, maternal BMI, any hypertensive disorders during pregnancy, gestational diabetes, prenatal antibiotic use, child sex, parity, and birthweight z-score, children born via planned C-section had 1.77 times higher risk of obesity (≥95th percentile), relative to those delivered vaginally ((95% CI) = (1.16, 2.72); p = 0.009). No association was found comparing unplanned C-section to vaginal delivery (RR (95% CI) = 0.75 (0.45, 1.23); p = 0.25). The results were similar but slightly stronger when obesity was defined by anthropometric class (RR (95% CI) = 2.78 (1.47, 5.26); p = 0.002). Breastfeeding did not mediate the association between mode of delivery and obesity.

Conclusions

These findings indicate that children delivered via planned C-section—but not unplanned C-section—have a higher risk of preadolescent obesity, suggesting that partial labor or membrane rupture (typically experienced during unplanned C-section delivery) may offer protection. Additional research is needed to understand the biological mechanisms behind this effect, including whether microbiological differences fully or partially account for the association.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Description of anthropometric classes at age 10.
Fig. 2: The mediating effect of breastfeeding in the association between planned C-section vs. vaginal delivery and 10-year anthropometric outcomes.

Similar content being viewed by others

Data availability

The datasets generated and/or analyzed during the current study are available from the corresponding author upon reasonable request.

Code availability

Code is available from the corresponding author upon reasonable request.

References

  1. Ng M, Fleming T, Robinson M, Thomson B, Graetz N, Margono C, et al. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet. 2014;384:766–81.

  2. Christoffel KK, Wang X, Binns HJ. Early origins of child obesity: bridging disciplines and phases of development—September 30-October 1, 2010. Int J Environ Res Public Health. 2012;9:1227–62.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Betrán AP, Ye J, Moller AB, Zhang J, Gülmezoglu AM, Torloni MR. The increasing trend in caesarean section rates: global, regional and national estimates: 1990–2014. PLoS ONE. 2016;11:e0148343.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. Kuhle S, Tong OS, Woolcott CG. Association between caesarean section and childhood obesity: a systematic review and meta-analysis. Obes Rev. 2015;16:295–303.

    Article  CAS  PubMed  Google Scholar 

  5. Li HT, Zhou YB, Liu JM. The impact of cesarean section on offspring overweight and obesity: a systematic review and meta-analysis. Int J Obes. 2013;37:893–9.

    Article  Google Scholar 

  6. Keag OE, Norman JE, Stock SJ. Long-term risks and benefits associated with cesarean delivery for mother, baby, and subsequent pregnancies: systematic review and meta-analysis. PLoS Med. 2018;15:e1002494.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proce Natl Acad Sci USA. 2010;107:11971–5.

    Article  Google Scholar 

  8. 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 

  9. Bäckhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe. 2015;17:690–703.

    Article  PubMed  CAS  Google Scholar 

  10. Azad MB, Konya T, Maughan H, Guttman DS, Field CJ, Chari RS, et al. Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. CMAJ. 2013;185:385–94.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Martinez KA 2nd, Devlin JC, Lacher CR, Yin Y, Cai Y, Wang J, et al. Increased weight gain by C-section: functional significance of the primordial microbiome. Sci Adv. 2017;3:eaao1874.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Cho CE, Norman M. Cesarean section and development of the immune system in the offspring. Am J Obstet Gynecol. 2013;208:249–54.

    Article  PubMed  Google Scholar 

  13. Shokry E, Marchioro L, Uhl O, Bermudez MG, Garcia-Santos JA, Segura MT, et al. Investigation of the impact of birth by cesarean section on fetal and maternal metabolism. Arch Gynecol Obstet. 2019;300:589–600.

    Article  CAS  PubMed  Google Scholar 

  14. Schlinzig T, Johansson S, Gunnar A, Ekstrom TJ, Norman M. Epigenetic modulation at birth—altered DNA-methylation in white blood cells after caesarean section. Acta Paediatr. 2009;98:1096–9.

    Article  CAS  PubMed  Google Scholar 

  15. Sutharsan R, Mannan M, Doi SA, Mamun AA. Caesarean delivery and the risk of offspring overweight and obesity over the life course: a systematic review and bias-adjusted meta-analysis. Clin Obes. 2015;5:293–301.

    Article  CAS  PubMed  Google Scholar 

  16. Stokholm J, Thorsen J, Chawes BL, Schjorring S, Krogfelt KA, Bonnelykke K, et al. Cesarean section changes neonatal gut colonization. J Allergy Clin Immunol. 2016;138:881–9.e2.

    Article  PubMed  Google Scholar 

  17. Hermansson H, Hoppu U, Isolauri E. Elective caesarean section is associated with low adiponectin levels in cord blood. Neonatology. 2014;105:172–4.

    Article  CAS  PubMed  Google Scholar 

  18. Aichbhaumik N, Zoratti EM, Strickler R, Wegienka G, Ownby DR, Havstad S, et al. Prenatal exposure to household pets influences fetal immunoglobulin E production. Clin Exp Allergy. 2008;38:1787–94.

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Wegienka G, Havstad S, Joseph CL, Zoratti E, Ownby D, Woodcroft K, et al. Racial disparities in allergic outcomes in African Americans emerge as early as age 2 years. Clin Exp Allergy. 2012;42:909–17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Havstad S, Johnson CC, Kim H, Levin AM, Zoratti EM, Joseph CL, et al. Atopic phenotypes identified with latent class analyses at age 2 years. J Allergy Clin Immunol. 2014;134:722–7.e2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Oken E, Kleinman KP, Rich-Edwards J, Gillman MW. A nearly continuous measure of birth weight for gestational age using a United States national reference. BMC Pediatr. 2003;3:6.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Hamilton CM, Strader LC, Pratt JG, Maiese D, Hendershot T, Kwok RK, et al. The PhenX Toolkit: get the most from your measures. Am J Epidemiol. 2011;174:253–60.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Kuczmarski RJ, Ogden CL, Guo SS, Grummer-Strawn LM, Flegal KM, Mei Z. et al. 2000 CDC growth charts for the United States: methods and development. Vital Health Stat. 2000;11:1–190.

    Google Scholar 

  24. CDC Division of Nutrition, Physical Activity, and Obesity [Internet]. Healthy Weight: about child & teen BMI; [updated 2020 June 29; cited 2020 Aug 10]. Available from: https://www.cdc.gov/healthyweight/assessing/bmi/childrens_bmi/about_childrens_bmi.html.

  25. Himes JH, Dietz WH. Guidelines for overweight in adolescent preventive services: recommendations from an expert committee. The Expert Committee on Clinical Guidelines for Overweight in Adolescent Preventive Services. Am J Clin Nutr. 1994;59:307–16.

    Article  CAS  PubMed  Google Scholar 

  26. Cohen J. Statistical power analysis for the behavioral sciences, 2nd edn. Lawrence Erlbaum Associates: Mahwah, NJ, 1988.

  27. Hernán MA, Hernández-Díaz S, Robins JM. A structural approach to selection bias. Epidemiology. 2004;15:615–25.

    PubMed  Google Scholar 

  28. Robins JM, Hernan MA, Brumback B. Marginal structural models and causal inference in epidemiology. Epidemiology. 2000;11:550–60.

    Article  CAS  PubMed  Google Scholar 

  29. Scrucca L, Fop M, Murphy TB, Raftery AE. mclust 5: clustering, classification and density estimation using Gaussian finite mixture models. R J. 2016;8:289–317.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Zou G. A modified poisson regression approach to prospective studies with binary data. Am J Epidemiol. 2004;159:702–6.

    Article  PubMed  Google Scholar 

  31. Hunsberger M, O’malley J, Block T, Norris JC. Relative validation of Block Kids Food Screener for dietary assessment in children and adolescents. Matern Child Nutr. 2015;11:260–70.

    Article  PubMed  Google Scholar 

  32. Drahovzal DN BT, Campagne PD, Vallis TM, Block TJ. Comparison of the block child activity screener with an objective measure of physical activity. In: annual meeting of the International Society of Behavioral Nutrition and Physical Activity (ISBNPA). Quebec City, QC, 2003.

  33. VanderWeele TJ, Ding P. Sensitivity analysis in observational research: introducing the E-value. Ann Intern Med. 2017;167:268–74.

    Article  PubMed  Google Scholar 

  34. White IR, Royston P, Wood AM. Multiple imputation using chained equations: issues and guidance for practice. Stat Med. 2011;30:377–99.

    Article  PubMed  Google Scholar 

  35. van Buuren S. Multiple imputation of discrete and continuous data by fully conditional specification. Stat Methods Med Res. 2007;16:219–42.

    Article  PubMed  Google Scholar 

  36. Wu Y, Wang Y, Huang J, Zhang Z, Wang J, Zhou L, et al. The association between caesarean delivery and the initiation and duration of breastfeeding: a prospective cohort study in China. Eur J Clin Nutr. 2018;72:1644–54.

    Article  PubMed  Google Scholar 

  37. Rito AI, Buoncristiano M, Spinelli A, Salanave B, Kunešová M, Hejgaard T, et al. Association between characteristics at birth, breastfeeding and obesity in 22 countries: the WHO European Childhood Obesity Surveillance Initiative—COSI 2015/2017. Obes Facts. 2019;12:226–43.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Tingley D, Yamamoto T, Hirose K, Keele L, Imai K. mediation: R package for causal mediation analysis. J Stat Softw. 2014;59:1–38.

    Article  Google Scholar 

  39. Gillman MW, Barker D, Bier D, Cagampang F, Challis J, Fall C, et al. Meeting report on the 3rd international congress on developmental origins of health and disease (DOHaD). Pediatr Res. 2007;61:625–9.

    Article  PubMed  Google Scholar 

  40. Stanislawski MA, Dabelea D, Wagner BD, Iszatt N, Dahl C, Sontag MK, et al. Gut microbiota in the first 2 years of life and the association with body mass index at age 12 in a Norwegian Birth Cohort. mBio. 2018;9:e01751–18.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Bammann K, Peplies J, De Henauw S, Hunsberger M, Molnar D, Moreno LA, et al. Early life course risk factors for childhood obesity: the IDEFICS case-control study. PLoS ONE. 2014;9:e86914.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Birbilis M, Moschonis G, Mougios V, Manios Y. Obesity in adolescence is associated with perinatal risk factors, parental BMI and sociodemographic characteristics. Eur J Clin Nutr. 2013;67:115–21.

    Article  CAS  PubMed  Google Scholar 

  43. Cornier MA, Després JP, Davis N, Grossniklaus DA, Klein S, Lamarche B, et al. Assessing adiposity: a scientific statement from the American Heart Association. Circulation. 2011;124:1996–2019.

    Article  PubMed  Google Scholar 

  44. Allison DB, Downey M, Atkinson RL, Billington CJ, Bray GA, Eckel RH, et al. Obesity as a disease: a white paper on evidence and arguments commissioned by the Council of the Obesity Society. Obesity. 2008;16:1161–77.

    Article  PubMed  Google Scholar 

  45. Cai M, Loy SL, Tan KH, Godfrey KM, Gluckman PD, Chong YS, et al. Association of elective and emergency cesarean delivery with early childhood overweight at 12 months of age. JAMA Netw Open. 2018;1:e185025.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Chojnacki MR, Holscher HD, Balbinot AR, Raine LB, Biggan JR, Walk AM, et al. Relations between mode of birth delivery and timing of developmental milestones and adiposity in preadolescence: a retrospective study. Early Hum Dev. 2019;129:52–9.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Flemming K, Woolcott CG, Allen AC, Veugelers PJ, Kuhle S. The association between caesarean section and childhood obesity revisited: a cohort study. Arch Dis Childhood. 2013;98:526–32.

    Article  Google Scholar 

  48. Mueller NT, Whyatt R, Hoepner L, Oberfield S, Dominguez-Bello MG, Widen EM, et al. Prenatal exposure to antibiotics, cesarean section and risk of childhood obesity. Int J Obes. 2015;39:665–70.

    Article  CAS  Google Scholar 

  49. Mitchell C, Chavarro JE. Mode of delivery and childhood obesity: is there a cause for concern? JAMA Netw Open. 2018;1:e185008.

    Article  PubMed  Google Scholar 

  50. Sterne JA, White IR, Carlin JB, Spratt M, Royston P, Kenward MG, et al. Multiple imputation for missing data in epidemiological and clinical research: potential and pitfalls. BMJ. 2009;338:b2393.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Cassidy-Bushrow AE, Wegienka G, Havstad S, Levin AM, Lynch SV, Ownby DR, et al. Race-specific association of caesarean-section delivery with body size at age 2 years. Ethn Dis. 2016;26:61–8.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We would like to acknowledge the continued dedicated participation of the WHEALS families in this long-standing birth cohort study.

Funding

The WHEALS study was supported by the National Institutes of Health (R01 HD082147; R01 AI050681; R01 HL-113010; P01 AI089473) and the Fund for Henry Ford Hospital. The authors take full responsibility of the content, which does not necessarily represent the official views of the funding bodies.

Author information

Authors and Affiliations

  1. Department of Public Health Sciences, Henry Ford Health System, Detroit, MI, USA

    Alexandra R. Sitarik, Suzanne L. Havstad, Christine C. Johnson, Kyra Jones, Albert M. Levin, Jennifer K. Straughen, Ganesa Wegienka, Kimberley J. Woodcroft & Andrea E. Cassidy-Bushrow

  2. Division of Gastroenterology, Department of Medicine, University of California, San Francisco, CA, USA

    Susan V. Lynch & Germaine J. M. Yong

  3. Division of Allergy & Immunology, Medical College of Georgia at Augusta University, Augusta, Georgia

    Dennis R. Ownby

  4. Department of Epidemiology, Mailman School of Public Health, Columbia University, New York, NY, USA

    Andrew G. Rundle

Authors
  1. Alexandra R. Sitarik
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Suzanne L. Havstad
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christine C. Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kyra Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Albert M. Levin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Susan V. Lynch
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Dennis R. Ownby
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Andrew G. Rundle
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jennifer K. Straughen
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Ganesa Wegienka
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Kimberley J. Woodcroft
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Germaine J. M. Yong
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Andrea E. Cassidy-Bushrow
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alexandra R. Sitarik.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sitarik, A.R., Havstad, S.L., Johnson, C.C. et al. Association between cesarean delivery types and obesity in preadolescence. Int J Obes 44, 2023–2034 (2020). https://doi.org/10.1038/s41366-020-00663-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41366-020-00663-8

This article is cited by

Search

Advanced search

Quick links