Accepted Article
Received Date : 31-Oct-2013 Revised Date : 03-Mar-2014 Accepted Date : 02-Jun-2014 Article type
: Regular Article
Caesarean delivery is associated with childhood general obesity but not abdominal obesity in Iranian elementary school children
Amin Salehi-Abargouei1-3, Afshin Shiranian 1-3, Simin Ehsani1-3, Pamela J. Surkan4, Ahmad Esmaillzadeh1,2
1
Food Security Research Center, Isfahan University of Medical Sciences, Isfahan, Iran 2
Department of Community Nutrition, School of Nutrition and Food Science, Isfahan University of Medical Sciences, Isfahan, Iran
3
Student research committee, School of Nutrition and Food Science, Isfahan University of Medical Sciences, Isfahan, Iran
4
Department of International Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland
Running title: Caesarean delivery and obesity
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi: 10.1111/apa.12711 This article is protected by copyright. All rights reserved.
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Correspondence to: Ahmad Esmaillzadeh, PhD Department of Community Nutrition School of Nutrition and Food Science Isfahan University of Medical Sciences PO Box 81745 Isfahan, Iran Phone: +98 311 792-2791 Fax: +98 311 6682509 Email: [email protected]
Conflicts of interest: ASA, AF, SE, PJS and AE declared no personal or financial conflicts of interest.
ABSTRACT AIM: This study examined the association between caesarean delivery and general and abdominal obesity among children. Methods: In a cross-sectional study, 635 children aged from six to 12 years-of-age (476 girls and 159 boys) were randomly selected from Isfahan elementary schools. Weight, height and waist circumference were measured. General and abdominal obesity were based on World Health Organization growth charts and Iranian national cut-off points, respectively. Parents were asked about delivery type and other factors potentially related to childhood obesity
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using a self-administered questionnaire. The association between delivery type and obesity was examined using univariate and multivariate logistic regression models. Results: The overall prevalence of general and central obesity was 17.6% and 17.1%, respectively, and caesarean delivery was significantly associated with general obesity after controlling for potential confounders (OR: 2.46; 95%CI: 1.30-4.63, P=0.005). We observed a significant association between caesarean delivery and abdominal obesity in crude analyses (OR: 1.66; 1.02-2.69, P=0.04), but this disappeared after adjusting for covariates (OR: 1.96; 0.82-4.69, P=0.13). Conclusion: Our results suggest that caesarean delivery is adversely associated with general childhood obesity, but not abdominal obesity. This provides support for recommending vaginal births, unless contra-indicated. Further research in large populations is required to confirm these findings.
KEYWORDS: Caesarean delivery, obesity, abdominal obesity, anthropometry
KEY NOTES •
Worldwide increases in caesarean delivery rates have created interest in its connection with later health complications, including childhood obesity.
•
This cross-sectional study examined the association between caesarean delivery and general and abdominal obesity among 635 Iranian elementary school children aged from six to 12 years-of-age.
•
Caesarean delivery was adversely related to childhood general obesity, but not abdominal obesity and it should not be recommended, unless otherwise indicated.
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INTRODUCTION Childhood obesity has become a major health problem, as its prevalence has increased at an alarming rate in many countries worldwide (1). In 2010, the World Health Organization (WHO) reported that globally about 45 million children under five-years-of-age were obese, with 35 million of those living in developing countries (2). A nationwide study in Iran found that 12.8% and 3.4% of pre-school children were overweight and obese, respectively (3). Childhood obesity has been associated with life-threatening conditions in adulthood (1) and, as a result, studying its predictors and identifying suitable strategies to curb obesity in childhood has attracted enormous attention. The increasing prevalence of obesity suggests a strong contribution of environmental factors in its aetiology (4). Recently, caesarean delivery (CD) has been introduced as a possible determinant of childhood obesity (5-7). In an earlier study, CD was linked to atopy and allergic disease in later life (8). The rates of CD have increased recently, not only in developed countries but also in developing nations (9). While the percentage of live births by CD in developed countries is estimated to be about 21.1% (10), the rate is about 35.0% in Iran (11). Published data on the association between CD and childhood obesity are scant and inconsistent. A case-control study of Chinese children aged three to seven years-of-age reported a significant positive association between CD and obesity (12). Such findings have also been shown in a cohort study of American children, where Huh et al showed that CD increased the risk of childhood obesity (7). Similar findings have been reported in a prospective study following Brazilians in adults from 23 to 25-years-of-age (5) but a recently published paper on three Brazilian birth cohorts failed to replicate these findings and concluded that CD was not associated with childhood obesity or obesity in adulthood (13).
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Conversely, a meta-analysis using observational data concluded that there was a significant association between CD and obesity in later life (6). The association between CD and childhood obesity is particularly relevant for Middle Eastern countries (14), where both CD and childhood obesity are highly prevalent. In addition, not much is known about the determinants of childhood obesity in these nations (15). Furthermore, earlier studies on the relation between CD and childhood obesity have not often taken into account dietary energy intake as a major determinant of obesity or economic status as a possibly important confounder (13). There is evidence that waist circumference is a better predictor of obesity and its health consequences, compared to BMI (16) and, therefore, the association between abdominal obesity and CD is relevant. Given these limited and inconsistent findings to date, we examined the association between CD and obesity in Iranian children.
SUBJECTS AND METHODS Study design and population: A cross-sectional study was conducted to assess factors associated with overweight and obesity in 971 Isfahani elementary school children aged seven to 12 years-of-age. A formula used to determine proportions in single cross-sectional surveys was used for sample size determination (17). Assuming that about 3% of Iranian children are obese (18) the minimal sample size needed was 500 participants. Participants were selected using multi-stage cluster sampling from three randomly selected geographic areas of Isfahan, Iran. We randomly selected four elementary schools from each of the geographic areas, then randomly selected one class from each grade (grades 1-5). Data collection was carried out by trained nutritionists in January 2013. Students with specific food allergies or dietary restrictions over the last year (n=50), any congenital disease (two children), or who were missing data on delivery type, anthropometric measurements or other
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confounders (284 subjects) were excluded, leaving 635 participants in the current analysis. Comparisons of excluded and included children by age, gender, BMI and waist circumference showed no significant differences. Ethical approval for the study protocol was granted by the Isfahan University of Medical Sciences Research Council.
Anthropometric measurements: Anthropometric measurements were performed on each participant by a trained nutritionist. Children were weighed wearing light clothes with digital scales that were precise to the nearest 0.1 kilogram. Height was measured in a standing position, using a plastic tape measure fixed onto a straight wall without any bumps, and recorded to the nearest centimeter. To measure height, participants were barefoot and their heads were placed in the Frankfurt position, with their shoulder blades, buttocks and heels touching the wall, to which the tape was fixed (19). Waist circumference was recorded to the nearest 0.5 centimeter using non-stretch plastic tape placed midway between iliac crest and lowest rib while participants were in standing position (19). Each anthropometric indicator was measured three times and the mean of these three measurements was used in the analysis. Overweight and obesity were defined based on the BMI for age percentiles developed by the World Health Organization (WHO) (20). Overweight was defined as BMI between the 85th and < 95th percentile and obesity was defined as a BMI ≥ the 95th percentile for age and sex. Based on Iranian national cut-off points, participants with waist circumference ≥90th percentile for age and sex were also defined as abdominally obese (21).
Assessment of delivery mode: To assess mode of delivery (caesarean/vaginal) parents were asked the following question: "What kind of delivery did the mother have to give birth to this
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child?" Participants were able to choose: "vaginal" or "caesarean". The answer to this question was used as the main independent variable in this study.
Assessment of covariates: Information on maternal age, family size, parental education (University educated/ graduate from high school or lower), obesity (obese or normal), and maternal smoking during pregnancy (exposed, non-exposed), was collected through a selfreported questionnaire taken home by the children. Parents were asked to complete the questionnaire and return it within a two-week period. Data about birth weight, birth order, length of gestation (preterm/normal/post-term), multiple birth (yes/no), breastfeeding status (exclusive/non-exclusive), and initiation of complementary feeding (before or after sixmonths-of-age), were collected from parents using a self-administered questionnaire. To assess physical activity, parents completed the Physical Activity Questionnaire for Iranian Children (PAQ-C), a validated instrument (22). Participants were placed in three categories: sedentary, moderately active and highly active, based on tertiles of the physical activity score (22). The parents’ economic status was assessed using 15 self-administered questions that inquired about the parents' occupation, family income, the head of household (father/other family members), house ownership status, car ownership, number of bedrooms and home-related facilities (including furniture, microwave, dishwasher, carpet, washing machine, laptop or personal computer) (23). Participants were categorised into poor, moderate or high economic status based on tertiles of the overall summed score. For a subgroup of 405 individuals, we applied a validated food frequency questionnaire to assess dietary intake (24). Participants’ total energy intake was calculated by summing energy intake from all food items in the food frequency questionnaire.
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Statistical analysis: Children were categorised by delivery type (caesarean/vaginal). Comparisons of continuous and categorical variables across participants’ delivery status were made using students’ t-tests for independent samples and chi-square tests, respectively. Binary logistic regression was used to assess CD in relation to overweight, obesity and abdominal obesity in univariate and several multivariate adjusted models. In the first model, we controlled for age and gender. In a second model, we further adjusted for birth weight (grams), length of gestation (preterm/term), birth order, multiple birth (yes/no), breastfeeding status (exclusive/non-exclusive) and initiation of complementary feeding and physical activity. In a third model, we adjusted for maternal factors in the prenatal period, such as maternal age (in years) and smoking exposure in pregnancy (yes/no) in addition to the variables included in the second model. Other variables such as economic status, family size, parental education and obesity were further adjusted for in the fourth model. In a fifth model, we also adjusted for energy intake in a subgroup of children (405 participants), for whom we had data on dietary intake and who had reported reasonable amounts of daily energy intake (1,500-4,500 Kcal/day). The association between abdominal obesity (having waist circumference >90th percentile for age and gender) and CD was assessed using binary logistic regression, controlling for the same confounders in the previous models. All statistical analyses were performed using the Statistical Package for Social Sciences (SPSS, version 15.0 for Windows, 2006, SPSS, Inc, Chicago, IL). A p-value of < 0.05 was considered statistically significant.
RESULTS A total of 635 children aged six to 12 years-of-age (476 girls and 159 boys) were included in the analyses. The prevalence of general and central obesity was 17.6% and 17.1%, respectively. Caesarean delivery was prevalent among 64.6% of children. General This article is protected by copyright. All rights reserved.
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characteristics of the population based on delivery type (vaginal/caesarean) are presented in Table S1 online. Individuals who were born via caesarean delivery were more likely to be boys, from families with a larger household size, and have low economic status. They were less likely to be from families with high parental education and they had higher mean BMIs compared with those born vaginally. There was no significant difference between the two groups in terms of mean body weight, energy intake, prevalence of parental obesity or physical activity levels. Comparisons of prenatal characteristics between the two groups revealed that those born by CD had marginally higher birth weights than those born vaginally (Table S2). The prevalence of preterm and singleton births, exclusive breastfeeding, smoking exposure in utero, and preterm complementary feeding did not differ significantly between the two groups.
Prevalence of overweight or obesity by delivery type indicated that 20.0% of vaginally born children were overweight or obese compared with 29.8% of those born by CD (P=0.01). Furthermore, abdominal obesity was more highly prevalent among children born by CD than those born vaginally (19.2% versus 12.6% respectively, P=0.04). Multivariate-adjusted odds ratios for obesity by delivery type are provided in Table 1. In the univariate analysis, we found that caesarean delivery was significantly associated with increased chance of obesity among school children (OR: 2.20; 95% CI: 1.34-3.63, P=0.002). This association remained significant after adjustment for age and gender (OR: 2.15, 95% CI: 1.30-2.55, P=0.0003). Inclusion of birth weight, length of gestation, birth order, number of births per pregnancy, breastfeeding status, timing of initiation of complementary feeding and physical activity did not substantially influence the association (OR: 2.46, 95% CI: 1.30-4.63, P=0.005). Even after further controlling for all other potential confounders including
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economic status and total energy intake, the association remained significant (OR: 4.02, 95% CI: 1.09-14.87, P=0.04). Our analysis also revealed that CD was significantly associated with greater potential risk of child abdominal obesity (OR: 1.66, 95% CI: 1.02-2.69, P=0.04) (Table 1) and this association remained significant after adjustment for age and gender (OR: 1.75, 95% CI: 1.07-2.85, P=0.02) as well as adjustment for other potential confounders (OR: 1.92, 95% CI: 1.03-3.58, P=0.04). When maternal age and smoking exposure in utero were taken into account, the association became marginally significant (OR: 1.86, 95% CI: 0.99-3.49, P=0.05). Additional adjustment for other variables including economic status caused the association to become non-significant (OR: 1.96, 95% CI: 0.82-4.69, P =0.13) and taking total energy intake into account in the last model did not alter the significance of these findings (OR: 1.28, 95% CI: 0.40-4.07, P =0.67).
DISCUSSION The present cross-sectional study of Isfahani children showed that CD is significantly related to a greater chance of general obesity. The association became non-significant for abdominal obesity after taking potential confounders into account. To our knowledge, this is the first report examining such an association in Middle Eastern countries.
Previous observational studies on the association between CD and obesity have led to inconsistent results (5, 13). A large body of research indicates that CD may lead to obesity in later life (5, 7, 12, 25, 26). However, Barros et al failed to confirm such findings in an analysis of three Brazilian birth cohorts. On the other hand, a recent systematic review and meta-analysis of observational studies showed that CD may lead to higher potential risk of obesity in childhood, adolescence and even adulthood (6). Furthermore, another study using
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two Brazilian cohorts showed significant associations between CD and obesity even after taking socio-economic status into account (25). Of note is that none of the earlier studies have controlled for daily energy intake in their analyses. Furthermore, the majority of previous studies did not adjust for socio-economic status (13). Barros et al have suggested that lack of adjustment for confounders like socio-economic status in previous studies might explain why some studies found significant results (13). In the present study, we found that even after controlling for several known confounders, including energy intake, the association between CD and obesity was significant. We do not know of other studies that have controlled for almost all potential confounders in the analysis. Although a significant association between CD and abdominal obesity was found in semi-adjusted models, the relationship lost significance after further adjustment for economic status, family size, parental education and obesity in our fourth model. Such findings indicate that the association between CD and abdominal obesity is not independent of other factors.
The mechanisms through which CD might affect the risk of obesity are not fully understood. Some investigators believe that CD is associated with changes in the development or composition of the intestinal microbiota, which could in turn affect host metabolism and energy storage and, therefore, lead to the development of obesity (27). Some studies have already shown differences in child gut flora according to mode of delivery in the first year of life (28), a period that is associated with dramatic changes in number and diversity of gut microbes (29). Some researchers have found that infants delivered by caesarean section had higher stool quantities of the Firmicutes bacteria group or lower quantities of the Bacteroidetes group. The Firmicutes and Bacteroidetes bacteria constitute the majority of the microbiota in the adult human intestine (30).
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This study is the first study to investigate and report association between CD and abdominal obesity in children. Although the study was cross-sectional in nature, the delivery took place before the outcome variable and recall of delivery type is expected to be accurate for almost all mothers. However, this study, as with other retrospective surveys, may be subject to recall bias for other variables that were adjusted for in the regression models. Recall bias of confounders can affect risk estimates. About one-third of the target sample was excluded, although they had similar characteristics for age, gender, BMI and waist circumference. Boys’ schools also had lower participation rates in this study compared to girls’ schools. Given that these issues may affect our results, further studies in Middle Eastern countries with better control of sampling, and that are prospective nature, are highly recommended.
In conclusion, this cross-sectional study of Isfahani children revealed that caesarean delivery was associated with the increased likelihood of obesity in childhood. Therefore, it is important that health care providers do not perceive that CD is risk free and that they recommend vaginal delivery to mothers for whom it is not contraindicated. We failed to find a significant association between abdominal obesity and CD. As mentioned, waist circumference is suggested by some researchers to be a better predictor of obesity and its health consequences compared to BMI (16). More research, particularly prospective studies with larger sample sizes, are needed to assess if an association exists between CD and childhood central obesity. ACKNOWLEDGEMENT The authors would like to thank the parents who were interviewed during this study and the Isfahan Department of Education for its cooperation and collaboration. AUTHORS CONTRIBUTION
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ASA and AE contributed to the conception and design of the study. ASA, AE and PJS contributed to the statistical analyses, data interpretation and drafting of the manuscript. AF and SE contributed to the data collection. All authors contributed in preparing and approving the final manuscript for submission. REFERENCES 1.
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Table 1. Odds ratios and 95% confidence intervals (CIs) for the association between caesarean delivery and obesity General obesity Odds ratio (95% CI) Crude
Vaginal Caesarean
Model 11
Model 22
Model 33
2.46 (1.30-4.63)
2.45 (1.30-4.64)
0.003
0.005
0.04
1.75 (1.07-2.85)
0.02
1.92 (1.03-3.58)
0.04
1 0.006
1.86 (0.99-3.49)
0.05
1 0.04
1 4.02 (1.09-14.87)
1.66 (1.02-2.69)
1
1 2.45 (1.03-5.84)
P value
1
1
Vaginal Caesarean
0.002
1
Vaginal Caesarean
Model 55
2.15 (1.30-2.55)
Odds ratio (95% CI) 1
1
Vaginal Caesarean
Model 44
2.20 (1.34-3.63)
Vaginal Caesarean
P value
1
Vaginal Caesarean
Abdominal obesity
1.96 (0.82-4.69)
0.13
1 0.04
1.28 (0.40-4.07)
0.67
1
Adjusted for age and gender.
2
Adjusted for variables in Model 1 plus birth weight (grams), length of gestation, birth order,
multiple births (yeas/no), breastfeeding status (exclusive/non-exclusive), commencement of complementary feeding (before 6 or after 6 months of age) and physical activity. 3
Adjusted for variables in Model 2 plus maternal age and smoking exposure (yes/no).
4
Adjusted for variables in Model 3 plus economic status, family size, parental education
(high school diploma or less, university-educated) and obesity (obese or normal). 5
Adjusted for variables in Model 4 plus energy intake in a subgroup of participants who had data about dietary
intake (N=405).
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Received Date : 31-Oct-2013 Revised Date : 03-Mar-2014 Accepted Date : 02-Jun-2014 Article type
: Regular Article
Caesarean delivery is associated with childhood general obesity but not abdominal obesity in Iranian elementary school children
Amin Salehi-Abargouei1-3, Afshin Shiranian 1-3, Simin Ehsani1-3, Pamela J. Surkan4, Ahmad Esmaillzadeh1,2
1
Food Security Research Center, Isfahan University of Medical Sciences, Isfahan, Iran 2
Department of Community Nutrition, School of Nutrition and Food Science, Isfahan University of Medical Sciences, Isfahan, Iran
3
Student research committee, School of Nutrition and Food Science, Isfahan University of Medical Sciences, Isfahan, Iran
4
Department of International Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland
Running title: Caesarean delivery and obesity
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi: 10.1111/apa.12711 This article is protected by copyright. All rights reserved.
Accepted Article
Correspondence to: Ahmad Esmaillzadeh, PhD Department of Community Nutrition School of Nutrition and Food Science Isfahan University of Medical Sciences PO Box 81745 Isfahan, Iran Phone: +98 311 792-2791 Fax: +98 311 6682509 Email: [email protected]
Conflicts of interest: ASA, AF, SE, PJS and AE declared no personal or financial conflicts of interest.
ABSTRACT AIM: This study examined the association between caesarean delivery and general and abdominal obesity among children. Methods: In a cross-sectional study, 635 children aged from six to 12 years-of-age (476 girls and 159 boys) were randomly selected from Isfahan elementary schools. Weight, height and waist circumference were measured. General and abdominal obesity were based on World Health Organization growth charts and Iranian national cut-off points, respectively. Parents were asked about delivery type and other factors potentially related to childhood obesity
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using a self-administered questionnaire. The association between delivery type and obesity was examined using univariate and multivariate logistic regression models. Results: The overall prevalence of general and central obesity was 17.6% and 17.1%, respectively, and caesarean delivery was significantly associated with general obesity after controlling for potential confounders (OR: 2.46; 95%CI: 1.30-4.63, P=0.005). We observed a significant association between caesarean delivery and abdominal obesity in crude analyses (OR: 1.66; 1.02-2.69, P=0.04), but this disappeared after adjusting for covariates (OR: 1.96; 0.82-4.69, P=0.13). Conclusion: Our results suggest that caesarean delivery is adversely associated with general childhood obesity, but not abdominal obesity. This provides support for recommending vaginal births, unless contra-indicated. Further research in large populations is required to confirm these findings.
KEYWORDS: Caesarean delivery, obesity, abdominal obesity, anthropometry
KEY NOTES •
Worldwide increases in caesarean delivery rates have created interest in its connection with later health complications, including childhood obesity.
•
This cross-sectional study examined the association between caesarean delivery and general and abdominal obesity among 635 Iranian elementary school children aged from six to 12 years-of-age.
•
Caesarean delivery was adversely related to childhood general obesity, but not abdominal obesity and it should not be recommended, unless otherwise indicated.
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INTRODUCTION Childhood obesity has become a major health problem, as its prevalence has increased at an alarming rate in many countries worldwide (1). In 2010, the World Health Organization (WHO) reported that globally about 45 million children under five-years-of-age were obese, with 35 million of those living in developing countries (2). A nationwide study in Iran found that 12.8% and 3.4% of pre-school children were overweight and obese, respectively (3). Childhood obesity has been associated with life-threatening conditions in adulthood (1) and, as a result, studying its predictors and identifying suitable strategies to curb obesity in childhood has attracted enormous attention. The increasing prevalence of obesity suggests a strong contribution of environmental factors in its aetiology (4). Recently, caesarean delivery (CD) has been introduced as a possible determinant of childhood obesity (5-7). In an earlier study, CD was linked to atopy and allergic disease in later life (8). The rates of CD have increased recently, not only in developed countries but also in developing nations (9). While the percentage of live births by CD in developed countries is estimated to be about 21.1% (10), the rate is about 35.0% in Iran (11). Published data on the association between CD and childhood obesity are scant and inconsistent. A case-control study of Chinese children aged three to seven years-of-age reported a significant positive association between CD and obesity (12). Such findings have also been shown in a cohort study of American children, where Huh et al showed that CD increased the risk of childhood obesity (7). Similar findings have been reported in a prospective study following Brazilians in adults from 23 to 25-years-of-age (5) but a recently published paper on three Brazilian birth cohorts failed to replicate these findings and concluded that CD was not associated with childhood obesity or obesity in adulthood (13).
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Conversely, a meta-analysis using observational data concluded that there was a significant association between CD and obesity in later life (6). The association between CD and childhood obesity is particularly relevant for Middle Eastern countries (14), where both CD and childhood obesity are highly prevalent. In addition, not much is known about the determinants of childhood obesity in these nations (15). Furthermore, earlier studies on the relation between CD and childhood obesity have not often taken into account dietary energy intake as a major determinant of obesity or economic status as a possibly important confounder (13). There is evidence that waist circumference is a better predictor of obesity and its health consequences, compared to BMI (16) and, therefore, the association between abdominal obesity and CD is relevant. Given these limited and inconsistent findings to date, we examined the association between CD and obesity in Iranian children.
SUBJECTS AND METHODS Study design and population: A cross-sectional study was conducted to assess factors associated with overweight and obesity in 971 Isfahani elementary school children aged seven to 12 years-of-age. A formula used to determine proportions in single cross-sectional surveys was used for sample size determination (17). Assuming that about 3% of Iranian children are obese (18) the minimal sample size needed was 500 participants. Participants were selected using multi-stage cluster sampling from three randomly selected geographic areas of Isfahan, Iran. We randomly selected four elementary schools from each of the geographic areas, then randomly selected one class from each grade (grades 1-5). Data collection was carried out by trained nutritionists in January 2013. Students with specific food allergies or dietary restrictions over the last year (n=50), any congenital disease (two children), or who were missing data on delivery type, anthropometric measurements or other
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confounders (284 subjects) were excluded, leaving 635 participants in the current analysis. Comparisons of excluded and included children by age, gender, BMI and waist circumference showed no significant differences. Ethical approval for the study protocol was granted by the Isfahan University of Medical Sciences Research Council.
Anthropometric measurements: Anthropometric measurements were performed on each participant by a trained nutritionist. Children were weighed wearing light clothes with digital scales that were precise to the nearest 0.1 kilogram. Height was measured in a standing position, using a plastic tape measure fixed onto a straight wall without any bumps, and recorded to the nearest centimeter. To measure height, participants were barefoot and their heads were placed in the Frankfurt position, with their shoulder blades, buttocks and heels touching the wall, to which the tape was fixed (19). Waist circumference was recorded to the nearest 0.5 centimeter using non-stretch plastic tape placed midway between iliac crest and lowest rib while participants were in standing position (19). Each anthropometric indicator was measured three times and the mean of these three measurements was used in the analysis. Overweight and obesity were defined based on the BMI for age percentiles developed by the World Health Organization (WHO) (20). Overweight was defined as BMI between the 85th and < 95th percentile and obesity was defined as a BMI ≥ the 95th percentile for age and sex. Based on Iranian national cut-off points, participants with waist circumference ≥90th percentile for age and sex were also defined as abdominally obese (21).
Assessment of delivery mode: To assess mode of delivery (caesarean/vaginal) parents were asked the following question: "What kind of delivery did the mother have to give birth to this
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child?" Participants were able to choose: "vaginal" or "caesarean". The answer to this question was used as the main independent variable in this study.
Assessment of covariates: Information on maternal age, family size, parental education (University educated/ graduate from high school or lower), obesity (obese or normal), and maternal smoking during pregnancy (exposed, non-exposed), was collected through a selfreported questionnaire taken home by the children. Parents were asked to complete the questionnaire and return it within a two-week period. Data about birth weight, birth order, length of gestation (preterm/normal/post-term), multiple birth (yes/no), breastfeeding status (exclusive/non-exclusive), and initiation of complementary feeding (before or after sixmonths-of-age), were collected from parents using a self-administered questionnaire. To assess physical activity, parents completed the Physical Activity Questionnaire for Iranian Children (PAQ-C), a validated instrument (22). Participants were placed in three categories: sedentary, moderately active and highly active, based on tertiles of the physical activity score (22). The parents’ economic status was assessed using 15 self-administered questions that inquired about the parents' occupation, family income, the head of household (father/other family members), house ownership status, car ownership, number of bedrooms and home-related facilities (including furniture, microwave, dishwasher, carpet, washing machine, laptop or personal computer) (23). Participants were categorised into poor, moderate or high economic status based on tertiles of the overall summed score. For a subgroup of 405 individuals, we applied a validated food frequency questionnaire to assess dietary intake (24). Participants’ total energy intake was calculated by summing energy intake from all food items in the food frequency questionnaire.
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Statistical analysis: Children were categorised by delivery type (caesarean/vaginal). Comparisons of continuous and categorical variables across participants’ delivery status were made using students’ t-tests for independent samples and chi-square tests, respectively. Binary logistic regression was used to assess CD in relation to overweight, obesity and abdominal obesity in univariate and several multivariate adjusted models. In the first model, we controlled for age and gender. In a second model, we further adjusted for birth weight (grams), length of gestation (preterm/term), birth order, multiple birth (yes/no), breastfeeding status (exclusive/non-exclusive) and initiation of complementary feeding and physical activity. In a third model, we adjusted for maternal factors in the prenatal period, such as maternal age (in years) and smoking exposure in pregnancy (yes/no) in addition to the variables included in the second model. Other variables such as economic status, family size, parental education and obesity were further adjusted for in the fourth model. In a fifth model, we also adjusted for energy intake in a subgroup of children (405 participants), for whom we had data on dietary intake and who had reported reasonable amounts of daily energy intake (1,500-4,500 Kcal/day). The association between abdominal obesity (having waist circumference >90th percentile for age and gender) and CD was assessed using binary logistic regression, controlling for the same confounders in the previous models. All statistical analyses were performed using the Statistical Package for Social Sciences (SPSS, version 15.0 for Windows, 2006, SPSS, Inc, Chicago, IL). A p-value of < 0.05 was considered statistically significant.
RESULTS A total of 635 children aged six to 12 years-of-age (476 girls and 159 boys) were included in the analyses. The prevalence of general and central obesity was 17.6% and 17.1%, respectively. Caesarean delivery was prevalent among 64.6% of children. General This article is protected by copyright. All rights reserved.
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characteristics of the population based on delivery type (vaginal/caesarean) are presented in Table S1 online. Individuals who were born via caesarean delivery were more likely to be boys, from families with a larger household size, and have low economic status. They were less likely to be from families with high parental education and they had higher mean BMIs compared with those born vaginally. There was no significant difference between the two groups in terms of mean body weight, energy intake, prevalence of parental obesity or physical activity levels. Comparisons of prenatal characteristics between the two groups revealed that those born by CD had marginally higher birth weights than those born vaginally (Table S2). The prevalence of preterm and singleton births, exclusive breastfeeding, smoking exposure in utero, and preterm complementary feeding did not differ significantly between the two groups.
Prevalence of overweight or obesity by delivery type indicated that 20.0% of vaginally born children were overweight or obese compared with 29.8% of those born by CD (P=0.01). Furthermore, abdominal obesity was more highly prevalent among children born by CD than those born vaginally (19.2% versus 12.6% respectively, P=0.04). Multivariate-adjusted odds ratios for obesity by delivery type are provided in Table 1. In the univariate analysis, we found that caesarean delivery was significantly associated with increased chance of obesity among school children (OR: 2.20; 95% CI: 1.34-3.63, P=0.002). This association remained significant after adjustment for age and gender (OR: 2.15, 95% CI: 1.30-2.55, P=0.0003). Inclusion of birth weight, length of gestation, birth order, number of births per pregnancy, breastfeeding status, timing of initiation of complementary feeding and physical activity did not substantially influence the association (OR: 2.46, 95% CI: 1.30-4.63, P=0.005). Even after further controlling for all other potential confounders including
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economic status and total energy intake, the association remained significant (OR: 4.02, 95% CI: 1.09-14.87, P=0.04). Our analysis also revealed that CD was significantly associated with greater potential risk of child abdominal obesity (OR: 1.66, 95% CI: 1.02-2.69, P=0.04) (Table 1) and this association remained significant after adjustment for age and gender (OR: 1.75, 95% CI: 1.07-2.85, P=0.02) as well as adjustment for other potential confounders (OR: 1.92, 95% CI: 1.03-3.58, P=0.04). When maternal age and smoking exposure in utero were taken into account, the association became marginally significant (OR: 1.86, 95% CI: 0.99-3.49, P=0.05). Additional adjustment for other variables including economic status caused the association to become non-significant (OR: 1.96, 95% CI: 0.82-4.69, P =0.13) and taking total energy intake into account in the last model did not alter the significance of these findings (OR: 1.28, 95% CI: 0.40-4.07, P =0.67).
DISCUSSION The present cross-sectional study of Isfahani children showed that CD is significantly related to a greater chance of general obesity. The association became non-significant for abdominal obesity after taking potential confounders into account. To our knowledge, this is the first report examining such an association in Middle Eastern countries.
Previous observational studies on the association between CD and obesity have led to inconsistent results (5, 13). A large body of research indicates that CD may lead to obesity in later life (5, 7, 12, 25, 26). However, Barros et al failed to confirm such findings in an analysis of three Brazilian birth cohorts. On the other hand, a recent systematic review and meta-analysis of observational studies showed that CD may lead to higher potential risk of obesity in childhood, adolescence and even adulthood (6). Furthermore, another study using
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two Brazilian cohorts showed significant associations between CD and obesity even after taking socio-economic status into account (25). Of note is that none of the earlier studies have controlled for daily energy intake in their analyses. Furthermore, the majority of previous studies did not adjust for socio-economic status (13). Barros et al have suggested that lack of adjustment for confounders like socio-economic status in previous studies might explain why some studies found significant results (13). In the present study, we found that even after controlling for several known confounders, including energy intake, the association between CD and obesity was significant. We do not know of other studies that have controlled for almost all potential confounders in the analysis. Although a significant association between CD and abdominal obesity was found in semi-adjusted models, the relationship lost significance after further adjustment for economic status, family size, parental education and obesity in our fourth model. Such findings indicate that the association between CD and abdominal obesity is not independent of other factors.
The mechanisms through which CD might affect the risk of obesity are not fully understood. Some investigators believe that CD is associated with changes in the development or composition of the intestinal microbiota, which could in turn affect host metabolism and energy storage and, therefore, lead to the development of obesity (27). Some studies have already shown differences in child gut flora according to mode of delivery in the first year of life (28), a period that is associated with dramatic changes in number and diversity of gut microbes (29). Some researchers have found that infants delivered by caesarean section had higher stool quantities of the Firmicutes bacteria group or lower quantities of the Bacteroidetes group. The Firmicutes and Bacteroidetes bacteria constitute the majority of the microbiota in the adult human intestine (30).
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This study is the first study to investigate and report association between CD and abdominal obesity in children. Although the study was cross-sectional in nature, the delivery took place before the outcome variable and recall of delivery type is expected to be accurate for almost all mothers. However, this study, as with other retrospective surveys, may be subject to recall bias for other variables that were adjusted for in the regression models. Recall bias of confounders can affect risk estimates. About one-third of the target sample was excluded, although they had similar characteristics for age, gender, BMI and waist circumference. Boys’ schools also had lower participation rates in this study compared to girls’ schools. Given that these issues may affect our results, further studies in Middle Eastern countries with better control of sampling, and that are prospective nature, are highly recommended.
In conclusion, this cross-sectional study of Isfahani children revealed that caesarean delivery was associated with the increased likelihood of obesity in childhood. Therefore, it is important that health care providers do not perceive that CD is risk free and that they recommend vaginal delivery to mothers for whom it is not contraindicated. We failed to find a significant association between abdominal obesity and CD. As mentioned, waist circumference is suggested by some researchers to be a better predictor of obesity and its health consequences compared to BMI (16). More research, particularly prospective studies with larger sample sizes, are needed to assess if an association exists between CD and childhood central obesity. ACKNOWLEDGEMENT The authors would like to thank the parents who were interviewed during this study and the Isfahan Department of Education for its cooperation and collaboration. AUTHORS CONTRIBUTION
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ASA and AE contributed to the conception and design of the study. ASA, AE and PJS contributed to the statistical analyses, data interpretation and drafting of the manuscript. AF and SE contributed to the data collection. All authors contributed in preparing and approving the final manuscript for submission. REFERENCES 1.
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Table 1. Odds ratios and 95% confidence intervals (CIs) for the association between caesarean delivery and obesity General obesity Odds ratio (95% CI) Crude
Vaginal Caesarean
Model 11
Model 22
Model 33
2.46 (1.30-4.63)
2.45 (1.30-4.64)
0.003
0.005
0.04
1.75 (1.07-2.85)
0.02
1.92 (1.03-3.58)
0.04
1 0.006
1.86 (0.99-3.49)
0.05
1 0.04
1 4.02 (1.09-14.87)
1.66 (1.02-2.69)
1
1 2.45 (1.03-5.84)
P value
1
1
Vaginal Caesarean
0.002
1
Vaginal Caesarean
Model 55
2.15 (1.30-2.55)
Odds ratio (95% CI) 1
1
Vaginal Caesarean
Model 44
2.20 (1.34-3.63)
Vaginal Caesarean
P value
1
Vaginal Caesarean
Abdominal obesity
1.96 (0.82-4.69)
0.13
1 0.04
1.28 (0.40-4.07)
0.67
1
Adjusted for age and gender.
2
Adjusted for variables in Model 1 plus birth weight (grams), length of gestation, birth order,
multiple births (yeas/no), breastfeeding status (exclusive/non-exclusive), commencement of complementary feeding (before 6 or after 6 months of age) and physical activity. 3
Adjusted for variables in Model 2 plus maternal age and smoking exposure (yes/no).
4
Adjusted for variables in Model 3 plus economic status, family size, parental education
(high school diploma or less, university-educated) and obesity (obese or normal). 5
Adjusted for variables in Model 4 plus energy intake in a subgroup of participants who had data about dietary
intake (N=405).
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