Caesarean section delivery and childhood obesity in a British longitudinal cohort study

English version

Autoři: Gwinyai Masukume ^aff001; Ali S. Khashan ^aff001; Susan M. B. Morton ^aff004; Philip N. Baker ^aff005; Louise C. Kenny ^aff006; Fergus P. McCarthy ^aff001
Působiště autorů: INFANT Research Centre, Cork, Ireland ^aff001; Department of Obstetrics and Gynaecology, University College Cork, Cork, Ireland ^aff002; School of Public Health, Western Gateway Building, University College Cork, Cork, Ireland ^aff003; Centre for Longitudinal Research–He Ara ki Mua, University of Auckland, Auckland, New Zealand ^aff004; College of Life Sciences, University of Leicester, Leicester, England, United Kingdom ^aff005; Department of Women’s and Children’s Health, Institute of Translational Medicine, Faculty of Health and Life Sciences, University of Liverpool, Liverpool, England, United Kingdom ^aff006; Department of Women and Children’s Health, School of Life Course Sciences, King’s College London, London, England, United Kingdom ^aff007
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0223856

Souhrn

Background

Several studies reported an association between Caesarean section (CS) birth and childhood obesity. However, there are several limitations in the current literature. These include an inability to distinguish between planned and emergency CS, small study sample sizes and not adjusting for pre-pregnancy body-mass-index (BMI). We examined the association between CS delivery and childhood obesity using the United Kingdom Millennium Cohort Study (MCS).

Methods

Mother-infant pairs were recruited into the MCS. Use of sampling weights ensured the sample was representative of the population. The exposure was categorised as normal vaginal delivery (VD) [reference], assisted VD, planned CS and emergency CS. Childhood obesity prevalence, at age three, five, seven, eleven and fourteen years was calculated using the International Obesity Taskforce criteria. Mixed-effects linear regression models were fitted with associations adjusted for several potential confounders like maternal age, pre-pregnancy BMI, education and infant macrosomia. Linear regression models were fitted evaluating body fat percentage (BF%), at age seven and fourteen years.

Results

Of the 18,116 infants, 3872 (21.4%) were delivered by CS; 9.2% by planned CS. Obesity prevalence was 5.4%, 5.7%, 6.5%, 7.1% and 7.6% at age three, five, seven, eleven and fourteen years respectively. The mixed-effects linear regression model showed no association between planned (adjusted mean difference = 0.00; [95% confidence interval (CI) -0.10; 0.10], p-value = 0.97) or emergency CS (adjusted mean difference = 0.08; [95% CI -0.01; 0.17], p-value = 0.09) and child BMI. At age seven years, there was no association between planned CS and BF% (adjusted mean difference = 0.13; [95% CI -0.23; 0.49]); there was no association at age fourteen years.

Conclusions

Infants born by planned CS did not have a significantly higher BMI or BF% compared to those born by normal VD. This may suggest that the association, described in the literature, could be due to the indications/reasons for CS birth or residual confounding.

Klíčová slova:

Body Mass Index – Labor and delivery – Cohort studies – Obesity – Childhood obesity – Adipose tissue – Infants

Zdroje

1. Li HT, Zhou YB, Liu JM. The impact of cesarean section on offspring overweight and obesity: a systematic review and meta-analysis. International journal of obesity (2005). 2013;37(7):893–9. Epub 2012/12/05. doi: 10.1038/ijo.2012.195 23207407.

2. Darmasseelane K, Hyde MJ, Santhakumaran S, Gale C, Modi N. Mode of delivery and offspring body mass index, overweight and obesity in adult life: a systematic review and meta-analysis. PLoS One. 2014;9(2):e87896. Epub 2014/03/04. doi: 10.1371/journal.pone.0087896 24586295; PubMed Central PMCID: PMC3935836.

3. Kuhle S, Tong OS, Woolcott CG. Association between caesarean section and childhood obesity: a systematic review and meta-analysis. Obesity reviews: an official journal of the International Association for the Study of Obesity. 2015;16(4):295–303. Epub 2015/03/11. doi: 10.1111/obr.12267 25752886.

4. 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. Clinical obesity. 2015;5(6):293–301. Epub 2015/08/20. doi: 10.1111/cob.12114 26286021.

5. 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 medicine. 2018;15(1):e1002494. Epub 2018/01/24. doi: 10.1371/journal.pmed.1002494 PubMed Central PMCID: PMC5779640. 29360829

6. Mitchell C, Chavarro JE. Mode of delivery and childhood obesity: Is there a cause for concern? JAMA Network Open. 2018;1(7):e185008. doi: 10.1001/jamanetworkopen.2018.5008 30646374

7. Bar-Meir M, Friedlander Y, Calderon-Margalit R, Hochner H. Mode of delivery and offspring adiposity in late adolescence: The modifying role of maternal pre-pregnancy body size. PLoS One. 2019;14(1):e0209581. Epub 2019/01/04. doi: 10.1371/journal.pone.0209581 30605457; PubMed Central PMCID: PMC6317793.

8. Yuan C, Gaskins AJ, Blaine AI, Zhang C, Gillman MW, Missmer SA, et al. Association Between Cesarean Birth and Risk of Obesity in Offspring in Childhood, Adolescence, and Early Adulthood. JAMA pediatrics. 2016:e162385. Epub 2016/09/07. doi: 10.1001/jamapediatrics.2016.2385 27599167.

9. Rifas-Shiman SL, Gillman MW, Hawkins SS, Oken E, Taveras EM, Kleinman KP. Association of Cesarean Delivery With Body Mass Index z Score at Age 5 Years. JAMA pediatrics. 2018. Epub 2018/06/12. doi: 10.1001/jamapediatrics.2018.0674 29889944.

10. Masukume G, O'Neill SM, Baker PN, Kenny LC, Morton SMB, Khashan AS. The Impact of Caesarean Section on the Risk of Childhood Overweight and Obesity: New Evidence from a Contemporary Cohort Study. Scientific reports. 2018;8(1):15113. Epub 2018/10/13. doi: 10.1038/s41598-018-33482-z 30310162.

11. Blustein J, Attina T, Liu M, Ryan AM, Cox LM, Blaser MJ, et al. Association of caesarean delivery with child adiposity from age 6 weeks to 15 years. International journal of obesity (2005). 2013;37(7):900–6. Epub 2013/05/15. doi: 10.1038/ijo.2013.49 23670220; PubMed Central PMCID: PMC5007946.

12. Huh SY, Rifas-Shiman SL, Zera CA, Edwards JW, Oken E, Weiss ST, et al. Delivery by caesarean section and risk of obesity in preschool age children: a prospective cohort study. Archives of disease in childhood. 2012;97(7):610–6. Epub 2012/05/25. doi: 10.1136/archdischild-2011-301141 22623615; PubMed Central PMCID: PMC3784307.

13. Hansen S, Halldorsson TI, Olsen SF, Rytter D, Bech BH, Granstrom C, et al. Birth by cesarean section in relation to adult offspring overweight and biomarkers of cardiometabolic risk. International journal of obesity (2005). 2018;42(1):15–9. Epub 2017/08/02. doi: 10.1038/ijo.2017.175 28757643.

14. Cai M, Loy S, Tan K, et al. Association of elective and emergency cesarean delivery with early childhood overweight at 12 months of age. JAMA Network Open. 2018;1(7):e185025. doi: 10.1001/jamanetworkopen.2018.5025 30646378

15. 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. Science advances. 2017;3(10):eaao1874. Epub 2017/10/14. doi: 10.1126/sciadv.aao1874 29026883; PubMed Central PMCID: PMC5636202.

16. Castillo-Ruiz A, Mosley M, Jacobs AJ, Hoffiz YC, Forger NG. Birth delivery mode alters perinatal cell death in the mouse brain. Proceedings of the National Academy of Sciences. 2018;115(46):11826. doi: 10.1073/pnas.1811962115 30322936

17. Chu DM, Ma J, Prince AL, Antony KM, Seferovic MD, Aagaard KM. Maturation of the infant microbiome community structure and function across multiple body sites and in relation to mode of delivery. Nat Med. 2017;23(3):314–26. Epub 2017/01/24. doi: 10.1038/nm.4272 28112736; PubMed Central PMCID: PMC5345907.

18. 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. Proceedings of the National Academy of Sciences of the United States of America. 2010;107(26):11971–5. Epub 2010/06/23. doi: 10.1073/pnas.1002601107 PubMed Central PMCID: PMC2900693. 20566857

19. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444(7122):1027–31. Epub 2006/12/22. doi: 10.1038/nature05414 17183312.

20. Jumpertz R, Le DS, Turnbaugh PJ, Trinidad C, Bogardus C, Gordon JI, et al. Energy-balance studies reveal associations between gut microbes, caloric load, and nutrient absorption in humans. The American journal of clinical nutrition. 2011;94(1):58–65. Epub 2011/05/06. doi: 10.3945/ajcn.110.010132 21543530; PubMed Central PMCID: PMC3127503.

21. 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 pediatrics. 2018. Epub 2018/02/21. doi: 10.1001/jamapediatrics.2017.5535 29459942.

22. Wampach L, Heintz-Buschart A, Fritz JV, Ramiro-Garcia J, Habier J, Herold M, et al. Birth mode is associated with earliest strain-conferred gut microbiome functions and immunostimulatory potential. Nature communications. 2018;9(1):5091. Epub 2018/12/07. doi: 10.1038/s41467-018-07631-x 30504906; PubMed Central PMCID: PMC6269548.

23. Hill CJ, Lynch DB, Murphy K, Ulaszewska M, Jeffery IB, O'Shea CA, et al. Evolution of gut microbiota composition from birth to 24 weeks in the INFANTMET Cohort. Microbiome. 2017;5(1):4. Epub 2017/01/18. doi: 10.1186/s40168-016-0213-y 28095889; PubMed Central PMCID: PMC5240274.

24. Willyard C. Could baby's first bacteria take root before birth? Nature. 2018;553(7688):264–6. Epub 2018/01/19. doi: 10.1038/d41586-018-00664-8 29345664

25. Theis KR, Romero R, Winters AD, Greenberg JM, Gomez-Lopez N, Alhousseini A, et al. Does the human placenta delivered at term have a microbiota? Results of cultivation, quantitative real-time PCR, 16S rRNA gene sequencing, and metagenomics. Am J Obstet Gynecol. 2019;220(3):267.e1–.e39. Epub 2019/03/06. doi: 10.1016/j.ajog.2018.10.018 30832984.

26. Zanardo V, Solda G, Trevisanuto D. Elective cesarean section and fetal immune-endocrine response. International journal of gynaecology and obstetrics: the official organ of the International Federation of Gynaecology and Obstetrics. 2006;95(1):52–3. Epub 2006/08/22. doi: 10.1016/j.ijgo.2006.06.022 16920115.

27. Kiriakopoulos N, Grigoriadis S, Maziotis E, Philippou A, Rapani A, Giannelou P, et al. Investigating Stress Response during Vaginal Delivery and Elective Cesarean Section through Assessment of Levels of Cortisol, Interleukin 6 (IL-6), Growth Hormone (GH) and Insulin-Like Growth Factor 1 (IGF-1). J Clin Med. 2019;8(8). Epub 2019/07/31. doi: 10.3390/jcm8081112 31357604.

28. Boerma T, Ronsmans C, Melesse DY, Barros AJD, Barros FC, Juan L, et al. Global epidemiology of use of and disparities in caesarean sections. The Lancet. 2018;392(10155):1341–8. doi: 10.1016/S0140-6736(18)31928-7

29. Kumar S, Kelly AS. Review of Childhood Obesity: From Epidemiology, Etiology, and Comorbidities to Clinical Assessment and Treatment. Mayo Clinic proceedings. 2017;92(2):251–65. Epub 2017/01/10. doi: 10.1016/j.mayocp.2016.09.017 28065514.

30. Zaffarini E, Mitteroecker P. Secular changes in body height predict global rates of caesarean section. Proceedings of the Royal Society B: Biological Sciences. 2019;286(1896):20182425. doi: 10.1098/rspb.2018.2425 30963921

31. Masukume G, McCarthy FP, Baker PN, Kenny LC, Morton SMB, Murray DM, et al. Association between caesarean section delivery and obesity in childhood: a longitudinal cohort study in Ireland. BMJ Open. 2019;9(3):e025051. doi: 10.1136/bmjopen-2018-025051 30878984

32. Hehir MP, Burke N, Burke G, Turner M, Breathnach FM, McAuliffe FM, et al. Sonographic markers of increased fetal adiposity demonstrate an increased risk for Cesarean delivery. Ultrasound in obstetrics & gynecology: the official journal of the International Society of Ultrasound in Obstetrics and Gynecology. 2019. Epub 2019/03/20. doi: 10.1002/uog.20263 30887629.

33. Connelly R, Platt L. Cohort profile: UK Millennium Cohort Study (MCS). International journal of epidemiology. 2014;43(6):1719–25. Epub 2014/02/20. doi: 10.1093/ije/dyu001 24550246.

34. Cole TJ, Bellizzi MC, Flegal KM, Dietz WH. Establishing a standard definition for child overweight and obesity worldwide: international survey. Bmj. 2000;320(7244):1240–3. Epub 2000/05/08. doi: 10.1136/bmj.320.7244.1240 10797032; PubMed Central PMCID: PMC27365.

35. Cole TJ, Flegal KM, Nicholls D, Jackson AA. Body mass index cut offs to define thinness in children and adolescents: international survey. Bmj. 2007;335(7612):194. Epub 2007/06/27. doi: 10.1136/bmj.39238.399444.55 17591624; PubMed Central PMCID: PMC1934447.

36. Cole TJ, Lobstein T. Extended international (IOTF) body mass index cut-offs for thinness, overweight and obesity. Pediatric obesity. 2012;7(4):284–94. Epub 2012/06/21. doi: 10.1111/j.2047-6310.2012.00064.x 22715120.

37. Kêkê LM, Samouda H, Jacobs J, di Pompeo C, Lemdani M, Hubert H, et al. Body mass index and childhood obesity classification systems: A comparison of the French, International Obesity Task Force (IOTF) and World Health Organization (WHO) references. Revue d'Épidémiologie et de Santé Publique. 2015;63(3):173–82. doi: 10.1016/j.respe.2014.11.003 26002984

38. Leroy J. zscore06: Stata command for the calculation of anthropometric z-scores using the 2006 WHO child growth standards. 2011.

39. 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. Epub 2009/07/01. doi: 10.1136/bmj.b2393 19564179; PubMed Central PMCID: PMC2714692.

40. Dong Y, Peng CY. Principled missing data methods for researchers. SpringerPlus. 2013;2(1):222. Epub 2013/07/16. doi: 10.1186/2193-1801-2-222 23853744; PubMed Central PMCID: PMC3701793.

41. Weng SF, Redsell SA, Nathan D, Swift JA, Yang M, Glazebrook C. Estimating overweight risk in childhood from predictors during infancy. Pediatrics. 2013;132(2):e414–21. Epub 2013/07/17. doi: 10.1542/peds.2012-3858 23858427.

42. Hawkins SS, Baum CF, Rifas-Shiman SL, Oken E, Taveras EM. Examining Associations between Perinatal and Postnatal Risk Factors for Childhood Obesity Using Sibling Comparisons. Childhood obesity (Print). 2019. Epub 2019/03/19. doi: 10.1089/chi.2018.0335 30883194.

43. Betran AP, Ye J, Moller AB, Zhang J, Gulmezoglu AM, Torloni MR. The Increasing Trend in Caesarean Section Rates: Global, Regional and National Estimates: 1990–2014. PLoS One. 2016;11(2):e0148343. doi: 10.1371/journal.pone.0148343 26849801; PubMed Central PMCID: PMC4743929.

44. Vinding RK, Sejersen TS, Chawes BL, Bonnelykke K, Buhl T, Bisgaard H, et al. Cesarean Delivery and Body Mass Index at 6 Months and Into Childhood. Pediatrics. 2017;139(6). Epub 2017/08/18. doi: 10.1542/peds.2016-4066 28814549.

45. Afshin A, Forouzanfar MH, Reitsma MB, Sur P, Estep K, Lee A, et al. Health Effects of Overweight and Obesity in 195 Countries over 25 Years. The New England journal of medicine. 2017;377(1):13–27. Epub 2017/06/13. doi: 10.1056/NEJMoa1614362 28604169; PubMed Central PMCID: PMC5479627.

46. Gray LA, Hernandez Alava M, Kelly MP, Campbell MJ. Family lifestyle dynamics and childhood obesity: evidence from the millennium cohort study. BMC public health. 2018;18(1):500. doi: 10.1186/s12889-018-5398-5 29807535

47. Barros AJ, Santos LP, Wehrmeister F, Motta JV, Matijasevich A, Santos IS, et al. Caesarean section and adiposity at 6, 18 and 30 years of age: results from three Pelotas (Brazil) birth cohorts. BMC public health. 2017;17(1):256. doi: 10.1186/s12889-017-4165-3 28292278; PubMed Central PMCID: PMC5351260.

48. Azcorra H, Rodriguez L, Banik SD, Bogin B, Varela-Silva MI, Dickinson F. Caesarean birth and adiposity parameters in 6- to 8-year-old urban Maya children from two cities of Yucatan, Mexico. American journal of human biology: the official journal of the Human Biology Council. 2019:e23217. Epub 2019/02/02. doi: 10.1002/ajhb.23217 30706581.

49. Barros FC, Matijasevich A, Hallal PC, Horta BL, Barros AJ, Menezes AB, et al. Cesarean section and risk of obesity in childhood, adolescence, and early adulthood: evidence from 3 Brazilian birth cohorts. The American journal of clinical nutrition. 2012;95(2):465–70. Epub 2012/01/13. doi: 10.3945/ajcn.111.026401 22237058; PubMed Central PMCID: PMC3260073.

50. Rooney BL, Mathiason MA, Schauberger CW. Predictors of obesity in childhood, adolescence, and adulthood in a birth cohort. Maternal and child health journal. 2011;15(8):1166–75. Epub 2010/10/12. doi: 10.1007/s10995-010-0689-1 20927643.

51. Alotaibi MF. Physiology of puberty in boys and girls and pathological disorders affecting its onset. J Adolesc. 2019;71:63–71. Epub 2019/01/15. doi: 10.1016/j.adolescence.2018.12.007 30639665.

52. Doblhammer G, Vaupel JW. Lifespan depends on month of birth. Proc Natl Acad Sci U S A. 2001;98(5):2934–9. doi: 10.1073/pnas.041431898 11226344; PubMed Central PMCID: PMC30243.

53. Robson MS. Classification of caesarean sections. Fetal and Maternal Medicine Review. 2001;12(1):23–39. Epub 01/17. doi: 10.1017/S0965539501000122

54. Quigley MA, Hockley C, Davidson LL. Agreement between hospital records and maternal recall of mode of delivery: evidence from 12 391 deliveries in the UK Millennium Cohort Study. BJOG: an international journal of obstetrics and gynaecology. 2007;114(2):195–200. Epub 2006/12/15. doi: 10.1111/j.1471-0528.2006.01203.x 17166217.

55. Isganaitis E, Suehiro H, Cardona C. Who's your daddy?: paternal inheritance of metabolic disease risk. Current opinion in endocrinology, diabetes, and obesity. 2017;24(1):47–55. Epub 2016/12/03. doi: 10.1097/med.0000000000000307 27906710.

56. Bogaerts A, De Baetselier E, Ameye L, Dilles T, Van Rompaey B, Devlieger R. Postpartum weight trajectories in overweight and lean women. Midwifery. 49:134–41. doi: 10.1016/j.midw.2016.08.010 27638342

57. Heslehurst N, Vieira R, Akhter Z, Bailey H, Slack E, Ngongalah L, et al. The association between maternal body mass index and child obesity: A systematic review and meta-analysis. PLoS medicine. 2019;16(6):e1002817. Epub 2019/06/12. doi: 10.1371/journal.pmed.1002817 31185012; PubMed Central PMCID: PMC6559702.

58. Delisle Nystrom C, Henriksson P, Alexandrou C, Lof M. The Tanita SC-240 to Assess Body Composition in Pre-School Children: An Evaluation against the Three Component Model. Nutrients. 2016;8(6). Epub 2016/06/21. doi: 10.3390/nu8060371 27322313; PubMed Central PMCID: PMC4924212.

59. Huberman Samuel M, Meiri G, Dinstein I, Flusser H, Michaelovski A, Bashiri A, et al. Exposure to General Anesthesia May Contribute to the Association between Cesarean Delivery and Autism Spectrum Disorder. Journal of Autism and Developmental Disorders. 2019. doi: 10.1007/s10803-019-04034-9 31053992