Elective and nonelective cesarean section and obesity among young adult male offspring: A Swedish population–based cohort study


Autoři: Viktor H. Ahlqvist aff001;  Margareta Persson aff002;  Cecilia Magnusson aff001;  Daniel Berglind aff001
Působiště autorů: Department of Global Public Health Sciences, Karolinska Institutet, Stockholm, Sweden aff001;  Department of Nursing, Umeå University, Umeå, Sweden aff002;  Centre for Epidemiology and Community Medicine, Region Stockholm, Stockholm, Sweden aff003
Vyšlo v časopise: Elective and nonelective cesarean section and obesity among young adult male offspring: A Swedish population–based cohort study. PLoS Med 16(12): e32767. doi:10.1371/journal.pmed.1002996
Kategorie: Research Article
doi: 10.1371/journal.pmed.1002996

Souhrn

Background

Previous studies have suggested that cesarean section (CS) is associated with offspring overweight and obesity. However, few studies have been able to differentiate between elective and nonelective CS, which may differ in their maternal risk profile and biological pathway. Therefore, we aimed to examine the association between differentiated forms of delivery with CS and risk of obesity in young adulthood.

Methods and findings

Using Swedish population registers, a cohort of 97,291 males born between 1982 and 1987 were followed from birth until conscription (median 18 years of age) if they conscripted before 2006. At conscription, weight and height were measured and transformed to World Health Organization categories of body mass index (BMI). Maternal and infant data were obtained from the Medical Birth Register. Associations were evaluated using multinomial and linear regressions. Furthermore, a series of sensitivity analyses were conducted, including fixed-effects regressions to account for confounders shared between full brothers. The mothers of the conscripts were on average 28.5 (standard deviation 4.9) years old at delivery and had a prepregnancy BMI of 21.9 (standard deviation 3.0), and 41.5% of the conscripts had at least one parent with university-level education.

Out of the 97,291 conscripts we observed, 4.9% were obese (BMI ≥ 30) at conscription. The prevalence of obesity varied slightly between vaginal delivery, elective CS, and nonelective CS (4.9%, 5.5%, and 5.6%, respectively), whereas BMI seemed to be consistent across modes of delivery. We found no evidence of an association between nonelective or elective CS and young adulthood obesity (relative risk ratio 0.96, confidence interval 95% 0.83–1.10, p = 0.532 and relative risk ratio 1.02, confidence interval 95% 0.88–1.18, p = 0.826, respectively) as compared with vaginal delivery after accounting for prepregnancy maternal BMI, maternal diabetes at delivery, maternal hypertension at delivery, maternal smoking, parity, parental education, maternal age at delivery, gestational age, birth weight standardized according to gestational age, and preeclampsia. We found no evidence of an association between any form of CS and overweight (BMI ≥ 25) as compared with vaginal delivery. Sibling analysis and several sensitivity analyses did not alter our findings. The main limitations of our study were that not all conscripts had available measures of anthropometry and/or important confounders (42% retained) and that our cohort only included a male population.

Conclusions

We found no evidence of an association between elective or nonelective CS and young adulthood obesity in young male conscripts when accounting for maternal and prenatal factors. This suggests that there is no clinically relevant association between CS and the development of obesity. Further large-scale studies are warranted to examine the association between differentiated forms of CS and obesity in young adult offspring.

Trial registration

Registered as observational study at ClinicalTrials.gov Identifier: NCT03918044.

Klíčová slova:

Birth weight – Body Mass Index – Cesarean section – Labor and delivery – Obesity – Preeclampsia – Swedish people


Zdroje

1. 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

2. The National Board of Health and Welfare (Socialstyrelsen). Statistikdatabas för graviditeter, förlossningar och nyfödda. [Statistics on Pregnancies, Deliveries and Newborn Infants]. Stockholm: The National Board of Health and Welfare (Socialstyrelsen); 2019. Swedish.

3. Betran AP, Torloni MR, Zhang JJ, Gulmezoglu AM; WHO Working Group on Caesarean Section. WHO Statement on Caesarean Section Rates. BJOG. 2016;123(5):667–70. doi: 10.1111/1471-0528.13526 26681211

4. Barber EL, Lundsberg LS, Belanger K, Pettker CM, Funai EF, Illuzzi JL. Indications contributing to the increasing cesarean delivery rate. Obstet Gynecol. 2011;118(1):29–38. doi: 10.1097/AOG.0b013e31821e5f65 21646928

5. Declercq E, Menacker F, Macdorman M. Maternal risk profiles and the primary cesarean rate in the United States, 1991–2002. Am J Public Health. 2006;96(5):867–72. doi: 10.2105/AJPH.2004.052381 16571712

6. Mylonas I, Friese K. Indications for and Risks of Elective Cesarean Section. Dtsch Arztebl Int. 2015;112(29–30):489–95. doi: 10.3238/arztebl.2015.0489 26249251

7. Nieminen K, Stephansson O, Ryding EL. Women's fear of childbirth and preference for cesarean section—a cross-sectional study at various stages of pregnancy in Sweden. Acta Obstet Gynecol Scand. 2009;88(7):807–13. doi: 10.1080/00016340902998436 19488882

8. Ryding EL, Wijma B, Wijma K, Rydhstrom H. Fear of childbirth during pregnancy may increase the risk of emergency cesarean section. Acta Obstet Gynecol Scand. 1998;77(5):542–7. 9654177

9. Florica M, Stephansson O, Nordstrom L. Indications associated with increased cesarean section rates in a Swedish hospital. Int J Gynaecol Obstet. 2006;92(2):181–5. doi: 10.1016/j.ijgo.2005.10.016 16364324

10. 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(1):e1002494. doi: 10.1371/journal.pmed.1002494 29360829

11. Bager P, Wohlfahrt J, Westergaard T. Caesarean delivery and risk of atopy and allergic disease: meta-analyses. Clin Exp Allergy. 2008;38(4):634–42. doi: 10.1111/j.1365-2222.2008.02939.x 18266879

12. Koplin J, Allen K, Gurrin L, Osborne N, Tang ML, Dharmage S. Is caesarean delivery associated with sensitization to food allergens and IgE-mediated food allergy: a systematic review. Pediatr Allergy Immunol. 2008;19(8):682–7. doi: 10.1111/j.1399-3038.2008.00731.x 19076564

13. 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. doi: 10.1371/journal.pone.0087896 24586295

14. 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 (Lond). 2013;37(7):893–9.

15. 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 Pediatr. 2016;170(11):e162385. doi: 10.1001/jamapediatrics.2016.2385 27599167

16. Kuhle S, Tong OS, Woolcott CG. Association between caesarean section and childhood obesity: a systematic review and meta-analysis. Obes Rev. 2015;16(4):295–303. doi: 10.1111/obr.12267 25752886

17. Hyde MJ, Mostyn A, Modi N, Kemp PR. The health implications of birth by Caesarean section. Biol Rev Camb Philos Soc. 2012;87(1):229–43. doi: 10.1111/j.1469-185X.2011.00195.x 21815988

18. 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(7):1096–9. doi: 10.1111/j.1651-2227.2009.01371.x 19638013

19. Almgren M, Schlinzig T, Gomez-Cabrero D, Gunnar A, Sundin M, Johansson S, et al. Cesarean delivery and hematopoietic stem cell epigenetics in the newborn infant: implications for future health? Am J Obstet Gynecol. 2014;211(5):502.e1–8.

20. Dahlen HG, Downe S, Kennedy HP, Foureur M. Is society being reshaped on a microbiological and epigenetic level by the way women give birth? Midwifery. 2014;30(12):1149–51. doi: 10.1016/j.midw.2014.07.007 25128348

21. Neu J, Rushing J. Cesarean versus vaginal delivery: long-term infant outcomes and the hygiene hypothesis. Clin Perinatol. 2011;38(2):321–31. doi: 10.1016/j.clp.2011.03.008 21645799

22. 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 Pediatr. 2018;172(8):777–9. doi: 10.1001/jamapediatrics.2018.0674 29889944

23. 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. Sci Rep. 2018;8(1):15113. doi: 10.1038/s41598-018-33482-z 30310162

24. 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(7):e185025. doi: 10.1001/jamanetworkopen.2018.5025 30646378

25. Masukume G, McCarthy FP, Baker PN, Kenny LC, Morton SM, 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

26. Wang Y, Beydoun MA, Liang L, Caballero B, Kumanyika SK. Will all Americans become overweight or obese? estimating the progression and cost of the US obesity epidemic. Obesity (Silver Spring). 2008;16(10):2323–30.

27. Källén K, editor. Den ökade andelen kejsarsnittsförlossningar och dess orsaker 1973–2009. [The increasing proportion of cesarean deliveries and their causes 1973–2009]. Stockholm: Svensk Förening för Obstetrik och Gynekologi; 2010. Swedish.

28. Kolas T, Hofoss D, Daltveit AK, Nilsen ST, Henriksen T, Hager R, et al. Indications for cesarean deliveries in Norway. Am J Obstet Gynecol. 2003;188(4):864–70. doi: 10.1067/mob.2003.217 12712077

29. Mears K, McAuliffe F, Grimes H, Morrison JJ. Fetal cortisol in relation to labour, intrapartum events and mode of delivery. J Obstet Gynaecol. 2004;24(2):129–32. doi: 10.1080/01443610410001645389 14766445

30. 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(5):385–94. doi: 10.1503/cmaj.121189 23401405

31. Nordesjö L, Schéle R. Validity of an ergometer cycle test and measures of isometric muscle strength when prediction some aspects of military performance. Försvarsmedicin (Swedish journal of defence medicine). 1974;10:11–23.

32. National Board of Health Welfare. The Swedish Medical Birth Register–A summary of content and quality. Stockholm, Sweden: National Board of Health and Welfare; 2003 [cited 2019 Oct 1]. Available from: https://www.socialstyrelsen.se/publikationer/.

33. Statistics Sweden. Multi-generation register 2016—A description of contents and quality. Örebro: Statistics Sweden; 2017.

34. Värnpliktslag. [Conscription Law], 1941:967 (1941).

35. Rasmussen F, Johansson M. The relation of weight, length and ponderal index at birth to body mass index and overweight among 18-year-old males in Sweden. European Journal of Epidemiology. 1998;14(4):373–80. doi: 10.1023/a:1007411613576 9690756

36. Ahlqvist VH, Persson M, Ortega FB, Tynelius P, Magnusson C, Berglind D. Birth weight and grip strength in young Swedish males: a longitudinal matched sibling analysis and across all body mass index ranges. Sci Rep. 2019;9(1):9719. doi: 10.1038/s41598-019-46200-0 31273289

37. World Health Organization. Obesity: preventing and managing the global epidemic. Report of a WHO consultation. Geneva: World Health Organization; 2000 [cited 2019 Oct 1]. Available from: https://www.who.int/nutrition/publications/obesity/WHO_TRS_894/en/.

38. Rasmussen F, Johansson M, Hansen HO. Trends in overweight and obesity among 18-year-old males in Sweden between 1971 and 1995. Acta Paediatr. 1999;88(4):431–7. doi: 10.1080/08035259950169837 10342544

39. Yu Z, Han S, Zhu J, Sun X, Ji C, Guo X. Pre-pregnancy body mass index in relation to infant birth weight and offspring overweight/obesity: a systematic review and meta-analysis. PLoS ONE. 2013;8(4):e61627. doi: 10.1371/journal.pone.0061627 23613888

40. Chu SY, Kim SY, Schmid CH, Dietz PM, Callaghan WM, Lau J, et al. Maternal obesity and risk of cesarean delivery: a meta-analysis. Obes Rev. 2007;8(5):385–94. doi: 10.1111/j.1467-789X.2007.00397.x 17716296

41. Hillier TA, Pedula KL, Schmidt MM, Mullen JA, Charles MA, Pettitt DJ. Childhood obesity and metabolic imprinting: the ongoing effects of maternal hyperglycemia. Diabetes Care. 2007;30(9):2287–92. doi: 10.2337/dc06-2361 17519427

42. Metzger BE, Lowe LP, Dyer AR, Trimble ER, Chaovarindr U, et al.; Hapo Study Cooperative Research Group. Hyperglycemia and adverse pregnancy outcomes. N Engl J Med. 2008;358(19):1991–2002. doi: 10.1056/NEJMoa0707943 18463375

43. Fraser A, Nelson SM, Macdonald-Wallis C, Sattar N, Lawlor DA. Hypertensive disorders of pregnancy and cardiometabolic health in adolescent offspring. Hypertension. 2013;62(3):614–20. doi: 10.1161/HYPERTENSIONAHA.113.01513 23918754

44. Ino T. Maternal smoking during pregnancy and offspring obesity: meta-analysis. Pediatr Int. 2010;52(1):94–9. doi: 10.1111/j.1442-200X.2009.02883.x 19400912

45. Lurie S, Ribenzaft S, Boaz M, Golan A, Sadan O. The effect of cigarette smoking during pregnancy on mode of delivery in uncomplicated term singleton pregnancies. J Matern Fetal Neonatal Med. 2014;27(8):812–5. doi: 10.3109/14767058.2013.842551 24020824

46. Reynolds RM, Osmond C, Phillips DI, Godfrey KM. Maternal BMI, parity, and pregnancy weight gain: influences on offspring adiposity in young adulthood. J Clin Endocrinol Metab. 2010;95(12):5365–9. doi: 10.1210/jc.2010-0697 20702520

47. Menacker F, Declercq E, Macdorman MF. Cesarean delivery: background, trends, and epidemiology. Semin Perinatol. 2006;30(5):235–41. doi: 10.1053/j.semperi.2006.07.002 17011392

48. Gillman MW, Rifas-Shiman S, Berkey CS, Field AE, Colditz GA. Maternal gestational diabetes, birth weight, and adolescent obesity. Pediatrics. 2003;111(3):e221–6. doi: 10.1542/peds.111.3.e221 12612275

49. Heffner LJ, Elkin E, Fretts RC. Impact of labor induction, gestational age, and maternal age on cesarean delivery rates. Obstet Gynecol. 2003;102(2):287–93. doi: 10.1016/s0029-7844(03)00531-3 12907101

50. Davis EF, Lazdam M, Lewandowski AJ, Worton SA, Kelly B, Kenworthy Y, et al. Cardiovascular risk factors in children and young adults born to preeclamptic pregnancies: a systematic review. Pediatrics. 2012;129(6):e1552–61. doi: 10.1542/peds.2011-3093 22614768

51. Penfield CA, Nageotte MP, Wing DA. Disparate Rates of Cesarean Delivery in Term Nulliparous Women with Hypertensive Disorders of Pregnancy. Am J Perinatol. 2019;36(10):887–1001.

52. Raju TNK, Buist AS, Blaisdell CJ, Moxey-Mims M, Saigal S. Adults born preterm: a review of general health and system-specific outcomes. Acta Paediatr. 2017;106(9):1409–37. doi: 10.1111/apa.13880 28419544

53. Myrskyla M, Fenelon A. Maternal age and offspring adult health: evidence from the health and retirement study. Demography. 2012;49(4):1231–57. doi: 10.1007/s13524-012-0132-x 22926440

54. Cleary-Goldman J, Malone FD, Vidaver J, Ball RH, Nyberg DA, Comstock CH, et al. Impact of maternal age on obstetric outcome. Obstet Gynecol. 2005;105(5 Pt 1):983–90. doi: 10.1097/01.AOG.0000158118.75532.51 15863534

55. Lissner L, Johansson SE, Qvist J, Rossner S, Wolk A. Social mapping of the obesity epidemic in Sweden. Int J Obes Relat Metab Disord. 2000;24(6):801–5. doi: 10.1038/sj.ijo.0801237 10878690

56. Witt WP, Wisk LE, Cheng ER, Mandell K, Chatterjee D, Wakeel F, et al. Determinants of cesarean delivery in the US: a lifecourse approach. Matern Child Health J. 2015;19(1):84–93. doi: 10.1007/s10995-014-1498-8 24770955

57. Frisell T, Oberg S, Kuja-Halkola R, Sjolander A. Sibling comparison designs: bias from non-shared confounders and measurement error. Epidemiology. 2012;23(5):713–20. doi: 10.1097/EDE.0b013e31825fa230 22781362

58. Oken E, Rifas-Shiman SL, Field AE, Frazier AL, Gillman MW. Maternal gestational weight gain and offspring weight in adolescence. Obstet Gynecol. 2008;112(5):999–1006. doi: 10.1097/AOG.0b013e31818a5d50 18978098

59. Johansson K, Hutcheon JA, Stephansson O, Cnattingius S. Pregnancy weight gain by gestational age and BMI in Sweden: a population-based cohort study. Am J Clin Nutr. 2016;103(5):1278–84. doi: 10.3945/ajcn.115.110197 27009753

60. Pforr K. femlogit-Implementation of the multinomial logit model with fixed effects. Stata Journal. 2014;14(4):847–62.

61. Curran EA, Dalman C, Kearney PM, Kenny LC, Cryan JF, Dinan TG, et al. Association Between Obstetric Mode of Delivery and Autism Spectrum Disorder: A Population-Based Sibling Design Study. JAMA Psychiatry. 2015;72(9):935–42. doi: 10.1001/jamapsychiatry.2015.0846 26107922

62. Williams R. Generalized Ordered Logit/Partial Proportional Odds Models for Ordinal Dependent Variables. The Stata Journal. 2006;6(1):58–82.

63. Harrell FE. Regression Modeling Strategies. New York, NY: Springer; 2001.

64. Li H, Ye R, Pei L, Ren A, Zheng X, Liu J. Caesarean delivery, caesarean delivery on maternal request and childhood overweight: a Chinese birth cohort study of 181 380 children. Pediatr Obes. 2014;9(1):10–6. doi: 10.1111/j.2047-6310.2013.00151.x 23512941

65. Llewellyn A, Simmonds M, Owen CG, Woolacott N. Childhood obesity as a predictor of morbidity in adulthood: a systematic review and meta-analysis. Obes Rev. 2016;17(1):56–67. doi: 10.1111/obr.12316 26440472

66. Bjerregaard LG, Jensen BW, Angquist L, Osler M, Sorensen TIA, Baker JL. Change in Overweight from Childhood to Early Adulthood and Risk of Type 2 Diabetes. N Engl J Med. 2018;378(14):1302–12. doi: 10.1056/NEJMoa1713231 29617589

67. Wrzosek M, Wisniewska K, Sawicka A, Talalaj M, Nowicka G. Early Onset of Obesity and Adult Onset of Obesity as Factors Affecting Patient Characteristics Prior to Bariatric Surgery. Obes Surg. 2018;28(12):3902–9. doi: 10.1007/s11695-018-3381-y 30022421

68. 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 (Lond). 2015;39(4):665–70.

69. Schousboe K, Willemsen G, Kyvik KO, Mortensen J, Boomsma DI, Cornes BK, et al. Sex differences in heritability of BMI: a comparative study of results from twin studies in eight countries. Twin Res. 2003;6(5):409–21. doi: 10.1375/136905203770326411 14624725

70. Drake AJ, Reynolds RM. Impact of maternal obesity on offspring obesity and cardiometabolic disease risk. Reproduction. 2010;140(3):387–98. doi: 10.1530/REP-10-0077 20562299

71. Weaver JJ, Statham H, Richards M. Are there "unnecessary" cesarean sections? Perceptions of women and obstetricians about cesarean sections for nonclinical indications. Birth. 2007;34(1):32–41. doi: 10.1111/j.1523-536X.2006.00144.x 17324176

72. Ye J, Zhang J, Mikolajczyk R, Torloni MR, Gulmezoglu AM, Betran AP. Association between rates of caesarean section and maternal and neonatal mortality in the 21st century: a worldwide population-based ecological study with longitudinal data. BJOG. 2016;123(5):745–53. doi: 10.1111/1471-0528.13592 26331389

73. Vogel JP, Betran AP, Vindevoghel N, Souza JP, Torloni MR, Zhang J, et al. Use of the Robson classification to assess caesarean section trends in 21 countries: a secondary analysis of two WHO multicountry surveys. Lancet Glob Health. 2015;3(5):e260–70. doi: 10.1016/S2214-109X(15)70094-X 25866355

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