Over the past few decades, the population prevalence of childhood overweight and obesity and births by cesarean delivery have increased markedly in many countries, including Australia.1,2 The World Health Organization recommends that cesarean delivery rates should not exceed 15%;3 a cesarean delivery rate more than 15% does not contribute additional reduction in maternal and neonatal mortality and morbidity. Although the trend of increased levels of obesity and rates of cesarean delivery occurred during a similar period, the association between these two is uncertain.
It has been suggested that exposure to maternal gut microbiota is crucial for the future health of the newborn (hygiene hypothesis).4 Birth by cesarean delivery has been identified as a potential risk factor for a number of childhood morbidities,5,6 including insulin-dependent diabetes mellitus5 and asthma.6 Mode of delivery often results in differential acquisition of microbiota by newborns, and it could play a pivotal role in development of these conditions later in life.4,7
At least 10 studies have examined the association between cesarean delivery and offspring obesity, with eight studies reporting a modest positive association7–14 and two reporting no association.15,16 A recent meta-analysis of these studies reported a modest association between cesarean delivery and obesity later in life when compared with vaginal delivery.17 Most of the studies failed to consider important potential confounders, including parental obesity, morbidity during pregnancy, and breastfeeding. This association has not yet been examined in Australia, despite having higher national rates of obesity and cesarean delivery.1,2 This study examined the association between the mode of delivery in the early 1980s and the risk of offspring obesity at age 21 years using a large community-based birth cohort study in Australia.
MATERIALS AND METHODS
The Mater University of Queensland Study of Pregnancy is a prospective study of 7,223 women and their offspring who received antenatal care at a major public hospital in Brisbane, Australia, between 1981 and 1983.18 At the first clinic visit, women were, on average, at 18 weeks of gestation. Of women who delivered at Mater Hospital during the baseline survey, 60% were included in the overall study. These mothers and their offspring have been followed-up prospectively and completed maternal questionnaires when their offspring were 6 months and 5, 14, and 21 years of age. In addition, at 5, 14, and 21 years, detailed physical, cognitive, and developmental examinations of the offspring were undertaken, and at 14 and 21 years the offspring completed health, social, and lifestyle questionnaires. Because of limited funding, at 21 years, we conducted physical assessments for a subsample of nearly 2,664 young adults. There were 520 mothers who delivered two newborns during 1981–1983 recruitments. However, at 21-year follow-up, of 2,625 adult offspring who provided measured heights and weights and had mode of delivery data at birth, only 185 sibling pairs had provided usable data for the main analysis. Consistent with the experiences of other cohort studies, the Mater University of Queensland Study of Pregnancy has collected a broad range of data at different follow-up times. Written informed consent from the mothers was obtained at all data collection phases and from the young adults at the 21-year follow-up. Ethics committees at the Mater Hospital and the University of Queensland approved each phase of the study. Full details of the Mater University of Queensland Study of Pregnancy design, sampling strategy, attrition, and follow-up sample characteristics are available elsewhere.18
Details of the method of delivery were recorded on the obstetric sheet as spontaneous, forceps (low, mid, rotate, and trial forceps in separate category), ventouse, breech, elective cesarean, and emergency cesarean. Initially, we combined all these groups into three categories as elective cesarean delivery and emergency cesarean delivery, and all others were vaginal delivery. If the decision for cesarean delivery was made before labor, it was coded as elective; if the decision was made during labor, it was coded as emergency. Because we found no difference in the association between cesarean elective delivery and cesarean emergency delivery regarding our outcome of interest, we collapsed the categories into two, cesarean delivery and vaginal delivery.
At the 21-year follow-up, offspring height was measured without shoes using a portable stadiometer (Road Rod 214 Portable Stadiometer) to the nearest centimeter. Weight (lightly clothed) was measured with a scale accurate to 0.2 kg. Two measures of weight and height were performed and the mean of these two measures was used in all analyses. Body mass index (BMI, calculated as weight (kg)/[height (m)]2) was categorized as normal (less than 25), overweight (25–29.9), and obese (30 or more). At 21 years, waist circumference was measured horizontally using a tape approximately in line with the umbilicus, directly against but without compressing the skin. The average of two measures was taken. Waist circumference was categorized for males as follows: less than 94 cm was normal; 94 to less than 102 cm was overweight; and 102 cm or more was obese; and for females it was categorized as follows: less than 80 cm was normal; 80 to less than 88 cm was overweight, and 88 cm or more was obese.19
Maternal and neonatal characteristics were considered to be potential confounding or mediating factors on the basis of a priori knowledge20 of their association with mode of delivery and young adult BMI or waist circumference at 21 years. Available potential confounders were maternal age at birth (in years), offspring sex, race (white, Asian, Aboriginal-Islander), maternal educational attainment (did not complete secondary school, completed secondary school, completed further or higher education), maternal smoking during pregnancy, gestation, birth weight, maternal prepregnancy BMI, gestational weight gain during pregnancy, and hypertensive disorder of pregnancy, all of which may affect mode of delivery and adult BMI or waist circumference.
Maternal educational attainment and ethnicity were all obtained from questionnaires completed at the first clinic visit of the study. Gestation and birth weight (in grams) were as recorded in the obstetric record of the birth. At the first clinic visit mothers were asked, “How many cigarettes did you usually smoke per day during the past 1 week?” We categorized the responses as none, 1–19, or 20 or more cigarettes per day. Maternal prepregnancy BMI was calculated based on maternal measured height at the first clinic visit of pregnancy and self-reported prepregnancy weight, which was recorded at the study initiation from maternal questionnaires. There was a high correlation between maternal estimate of prepregnancy weight and measured weight at the first clinic visit (Pearson correlation coefficient=0.9). Maternal height was measured without shoes using a portable stadiometer to the nearest 0.1 cm, and these measurements were used to compute BMI and its categories. We calculated total gestational weight gain as the difference between maximum recorded weight during pregnancy and self-reported prepregnancy weight (determined at the first antenatal visit). Hypertensive disorder of pregnancy was defined as a diastolic blood pressure more than 90 mm Hg on at least two occasions beyond 20 weeks of gestation associated with proteinuria, excessive fluid retention (defined as generalized edema including the face and hands and excessive weight gain), or proteinuria and excessive fluid retention. Proteinuria was diagnosed if there was a score of at least 2+ of protein on dipstick testing (Albustix). Based on the data collected, we were not able to make the distinction between gestational hypertension, preeclampsia, preeclampsia superimposed on chronic hypertension, or chronic hypertension. The diagnosis of preeclampsia was made and recorded by consultant obstetricians. Breastfeeding (never, less than 4 months, or 4 months or more) information was self-reported at the 6-month follow-up.
The proportions of vaginal deliveries and cesarean deliveries by maternal and birth characteristics are presented as descriptive analyses. We used χ2 when the characteristics were categorical and we used the F test for continuous characteristics. To examine independent association of maternal and birth characteristics with mode of delivery, we used multiple logistic regression analysis. These results are presented as odds ratio (OR) with 95% confidence interval (CI). Statistical evidence for a difference in effect between males and females was assessed by computing a likelihood ratio test of the interaction with sex. Because we found no effect difference between male and female offspring, results are presented for males and females combined.
We have used multinomial logistic regression to estimate the unadjusted and adjusted ORs (95% CI) of overweight and obesity by 21 years. The multivariable model was adjusted for maternal age at delivery, educational attainment, maternal smoking during pregnancy, parental race, gestation, birth weight, gestational weight gain, hypertensive disorder in pregnancy, maternal prepregnancy BMI, and duration of breastfeeding. Similarly, we have used a multiple regression model to estimate unadjusted and adjusted mean differences of BMI and waist circumference scores at 21 years by mode of delivery. For the adjustment, we considered the same factors as we did for the multivariable logistic regression. All analyses were performed using Stata 11.0.
Of 2,625 offspring who had measured BMI and waist circumference at 21 years, 12.1% were born by cesarean delivery, a percentage similar to that the original cohort of 7,223 women (12.0%). Maternal characteristics during pregnancy by the mode of delivery are presented in Table 1. Mothers who were heavy smokers during pregnancy, had hypertensive disorder of pregnancy, delivered after 35 years of age, had premature birth, delivered a low-birth-weight newborn, and were overweight or obese before pregnancy had a greater risk of cesarean delivery (all P<.05; Table 1). Maternal education, parental racial origin, and gestational weight gain were not associated with the mode of delivery.
To examine whether these maternal and birth characteristics were independently associated with the cesarean delivery, we estimated adjusted OR (Table 2). The multivariable analyses were restricted to 2,382 offspring for whom we had measured height, weight, and waist circumference at 21 years, hospital recorded mode of delivery at birth, and the potential confounding and mediating factors. In the multivariable adjusted model, ORs of cesarean delivery increased 1.8 (95% CI 1.1–2.9) and 2.9 (95% CI 1.5–5.6) for mothers who were 20–34 years old and 35 years old or older, respectively, compared with the teenage mothers. Similarly, the ORs of cesarean delivery increased to 1.8 (95% CI 1.2–2.6) for mothers with a hypertensive disorder of pregnancy compared with mothers without. Mothers who delivered a low-birth-weight newborn had an OR of 2.6 (95% CI 1.4–4.7) for cesarean delivery. Mothers who were overweight (OR 1.5; 95% CI 1.0–2.1) or obese (OR 2.8; 95% CI 1.7–4.6) before pregnancy were at higher risk for cesarean delivery compared with normal-weight mothers.
Prevalence of overweight and obesity and mean scores of BMI and waist circumference at 21 years by the mode of delivery are presented in Table 3. Using BMI cutoffs, 21.5% of young adults were overweight and 12.4% were obese. Similarly, using the waist circumference cutoff, 14.2% of young adults were overweight and 13.5% were obese. Both BMI and waist circumference categories as well as scores on a continuous scale were not associated with the mode of delivery (all P>.05).
The OR of overweight and obesity at 21 years with association of delivery type was estimated using logistic regression (Table 4). The ORs (with 95% CI) are presented for 2,382 offspring for whom we had available data for all variables included in the adjusted model. In the unadjusted and adjusted models, we found that the odds of being overweight and obese at age 21 years were not significantly different for participants delivered by cesarean and those delivered vaginally. Similarly, by multivariable regression, the associations between adjusted mean difference in BMI and waist circumference scores and mode of delivery were weak and statistically insignificant (Table 5).
In additional analyses, distinguishing between elective and emergency cesarean had little influence on the associations we observed; excluding the 185 sibling pairs to reduce the correlation structure of this subsample had little effect on our results (data not shown).
In this large birth cohort study, although one-third of the offspring were overweight and obese at age 21 years, their overweight and obesity status was not associated with their mode of birth. We also found that when analyzed as continuous variables, BMI and waist circumference were not associated with mode of delivery. That is, this study does not suggest that delivery by cesarean increases the risk of overweight and obesity in young adulthood.
A greater risk of obesity has been reported in newborns delivered by cesarean compared with those who were delivered vaginally (OR 2.1 and 95% CI 1.4–3.2 at 3 years of age;8 OR 5.2 and 95% CI 1.2–22.0 among preschool children;12 and OR 1.8 in children 7–11 years of age).14 Similar but modest association has been reported in adults (OR 1.6; 95% CI 1.2–2.0),7 and the findings of our study agree with one study16 and contrast with two other studies.7,10 In Brazil, Goldani et al7 reported an increased risk of obesity attributable to cesarean delivery, whereas Barros et al16 did not find such an association after adjusting for all potential confounders in another three Brazilian birth cohorts. Because Brazil has a higher national prevalence of cesarean delivery (more than 45%)21 and obesity,22 the chances of detecting this association, if it existed, would have been higher in this population.
A limitation of our study is that for both BMI and waist circumference, we may have had less than usual statistical power to detect differences than a prospective design. A larger study of Danish children born in 1997–2002 (N=28,354) reported no association between cesarean delivery and obesity at 7 years of age.15 The authors who reported a positive association in adult populations7,10,13 did not adjust for maternal prepregnancy BMI; however, we have controlled for this factor in our multivariate analysis. Another study (N=10,219)14 that reported a positive association in children could not find a significant association in a normal-weight mother group on stratification. Maternal prepregnancy BMI is a strong predictor of obesity in offspring. It has been established that maternal factors such as obesity,23 hypertensive disorder, and premature birth24 increase the chances of delivery by cesarean.24 The prevalence of overweight and obesity among Australian pregnant women was estimated as 43%.25 An Australian study (N=75,095) reported that obese mothers (more than 30) were at twofold risk for delivering by cesarean (adjusted OR 2.2; 95% CI 2.1–2.3).26 The effect of cesarean delivery on adult obesity did not differ when stratified by planned and nonplanned cesarean delivery, which is consistent with a recent study.13
There is evidence for inverse association of cesarean delivery and breastfeeding,27 which is protective against obesity.28 Socioeconomic status is another confounder associated with cesarean delivery and obesity.16 Mode of delivery (or cesarean) appears to be a confounder, rather than a causal factor, in the development of overweight and obesity in (young) adulthood of offspring.
The major strength of this study was a prospective follow-up of a large cohort of mothers and offspring pairs. Potential confounders and mediators including parental prepregnancy BMI, gestation, low birth weight, and duration of breastfeeding were considered in the analyses. Like other large and long-term follow-up birth cohort studies, including a British birth cohort,31 there is considerable attrition in the Mater University of Queensland Study of Pregnancy over the course of 21-year follow-up. In general, nonparticipant mothers were more likely to be from families with low income at birth, to have mothers who smoked throughout their pregnancy, had poorer mental health, and to have mothers and fathers with lower educational attainment.18 The disproportionate loss to follow-up may have led to underestimates of the strength of associations. We have previously used multiple strategies to assess the effect of attrition on our estimates of association, and we were able to conclude that substantial variations in loss to follow-up had very little effect on the findings.18,32
In summary, we found that mode of delivery is not associated with long-term BMI, waist circumference scores, or obesity. We also found that maternal age, smoking status during pregnancy, hypertensive disorder during pregnancy, low-birth-weight newborns, and maternal overweight and obesity status before pregnancy were independently associated with mode of delivery. Findings of this study do not support the idea that cesarean delivery has increased the risk of offspring obesity.
1. World Health Organization. Obesity and overweight. Geneva (Switzerland): World Health Organization; 2011. Fact Sheet No. 311.
2. Betrán AP, Merialdi M, Lauer JA, Bing-Shun W, Thomas J, Van Look P, et al.. Rates of caesarean section: analysis of global, regional and national estimates. Paediatr Perinat Epidemiol 2007;21:98–113.
3. World Health Organization. Appropriate technology for birth. Lancet 1985;2:436–7.
4. Neu J, Rushing J. Cesarean versus vaginal delivery: long-term infant outcomes and the hygiene hypothesis. Clin Perinatol 2011;38:321–31.
5. Cardwell CR, Stene LC, Joner G, Cinek O, Svensson J, Goldacre MJ, et al.. Caesarean section is associated with an increased risk of childhood-onset type 1 diabetes mellitus: a meta-analysis of observational studies. Diabetologia 2008;51:726–35.
6. Roduit C, Scholtens S, de Jongste JC, Wijga AH, Gerritsen J, Postma DS, et al.. Asthma at 8 years of age in children born by caesarean section. Thorax 2009;64:107–13.
7. Goldani HA, Bettiol H, Barbieri MA, Silva AA, Agranonik M, Morais MB, et al.. Cesarean delivery is associated with an increased risk of obesity in adulthood in a Brazilian birth cohort study. Am J Clin Nutr 2011;93:1344–7.
8. Huh SY, Rifas-Shiman SL, Zera CA, Edwards JWR, Oken E, Weiss ST, et al.. Delivery by caesarean section and risk of obesity in preschool age children: a prospective cohort study. Arch Dis Child 2012;97:610–6.
9. Li HA. A national epidemiological survey on obesity of children under 7 years of age in nine cities of China, 2006 [in Chinese]. Zhanghua Er Ke Za Zhi 2008;46:174–8.
10. Rooney B, Mathiason M, Schauberger C. Predictors of obesity in childhood, adolescence, and adulthood in a birth cohort. Maternal Child Health J 2011;15:1166–75.
11. Steur M, Smit HA, Schipper CMA, Scholtens S, Kerkhof M, de Jongste JC, et al.. Predicting the risk of newborn children to become overweight later in childhood: the PIAMA birth cohort study. Int J Pediatr Obes 2011;6:e170–8.
12. Zhou L, He G, Zhang J, Xie R, Walker M, Wen SW. Risk factors of obesity in preschool children in an urban area in China. Eur J Pediatr 2011;170:1401–6.
13. Svensson E, Hyde MJ, Modi N, Ehrenstein V. Caesarean section and body mass index among Danish adult men. Obesity (Silver Spring) 2013;21:429–33.
14. Blustein J, Attina T, Liu M, Ryan A, Cox L, Blaser M, et al.. Association of caesarean delivery with child adiposity from age 6 weeks to 15 years. Int J Obes (Lond) 2013;37:900–6.
15. Ajslev T, Andersen C, Gamborg M, Sørensen T, Jess T. Childhood overweight after establishment of the gut microbiota: the role of delivery mode, pre-pregnancy weight and early administration of antibiotics. Int J Obes (Lond) 2011;35:522–9.
16. 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. Am J Clin Nutr 2012;95:465–70.
17. Li H, Zhou Y, Liu J. The impact of cesarean section on offspring overweight and obesity: a systematic review and meta-analysis. Int J Obes (Lond) 2012;37:893–9.
18. Najman J, Bor W, O'Callaghan M, Williams G, Aird R, Shuttlewood G. Cohort profile: the Mater-University of Queensland study of pregnancy (MUSP). Int J Epidemiol 2005;34:992–7.
19. Obesity: preventing and managing the global epidemic. Report of a WHO consultation. World Health Organ Tech Rep Ser 2000;894:i–xii; 1–253.
20. Hernan MA, Hernandez-Diaz S, Werler MM, Mitchell AA. Causal knowledge as a prerequisite for confounding evaluation: an application to birth defects epidemiology. Am J Epidemiol 2002;155:176–84.
21. Gibbons L, Belizan JM, Lauer JA, Betran AP, Merialdi M, Althabe F. Inequities in the use of cesarean section deliveries in the world. Am J Obstetrics Gynecol 2012;206:331.e1–19.
22. Gigante DP, EC Moura, Sardinha LM. Prevalence of overweight and obesity and associated factors, Brazil, 2006. Rev de Saúde Pública 2009;43:83–9.
23. Poobalan A, Aucott L, Gurung T, Smith WCS, Bhattacharya S. Obesity as an independent risk factor for elective and emergency caesarean delivery in nulliparous women–systematic review and meta-analysis of cohort studies. Obes Rev 2009;10:28–35.
24. Bettegowda VR, Dias T, Davidoff MJ, Damus K, Callaghan WM, Petrini JR. The Relationship between cesarean delivery and gestational age among US Singleton births. Clin Perinatol 2008;35:309–23.
25. Athukorala C, Rumbold A, Willson K, Crowther C. The risk of adverse pregnancy outcomes in women who are overweight or obese. BMC Pregnancy Childbirth 2010;10:56.
26. McIntyre HD, Gibbons KS, Flenady VJ, Callaway LK. Overweight and obesity in Australian mothers: epidemic or endemic. Med J Aust 2012;196:184–8.
27. Zanardo V, Svegliado G, Cavallin F, Giustardi A, Cosmi E, Litta P, et al.. Elective cesarean delivery: does it have a negative effect on breastfeeding? Birth 2010;37:275–9.
28. Horta B, Bah L R, Martines J, Victora C. Evidence of the long-term effects of breastfeeding: systematic reviews and meta-analysis. Geneva (Switzerland): World Health Organization Publication; 2007.
29. Grölund M-M, Lehtonen O-P, Eerola E, Kero P. Fecal microflora in healthy infants born by different methods of delivery: permanent changes in intestinal flora after cesarean delivery. J Pediatr Gastroenterol Nutr 1999;28:19–25.
30. Penders J, Thijs C, Vink C, Stelma FF, Snijders B, Kummeling I, et al.. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 2006;118:511–21.
31. Power C, Elliott J. Cohort profile: 1958 British birth cohort (National Child Development Study). Int J Epidemiol 2006;35:34–41.
© 2013 by The American College of Obstetricians and Gynecologists. Published by Wolters Kluwer Health, Inc. All rights reserved.
32. Horwood LJ, Fergusson DM, Hayatbakhsh MR, Najman JM, Coffey C, Patton GC, et al.. Cannabis use and educational achievement: findings from three Australasian cohort studies. Drug Alcohol Depend 2010;110:247–53.