ORIGINAL ARTICLE: GASTROENTEROLOGY Constipation and Colonic Transit Times in Children With Morbid Obesity Ã Olga H. vd Baan-Slootweg, ÃOlivia Liem, ÃNoor Bekkali, yWim M.C. van Aalderen, z Tammo H. Pels Rijcken, §Carlo Di Lorenzo, and ÃMarc A. Benninga ABSTRACT conditions such as hypertension, hepatosteatosis, and diabetes Objectives: The aim of the study was to determine the frequency of mellitus type 2 (1,2). In addition to these comorbid conditions, functional constipation according to the Rome III criteria in children with functional gastrointestinal disorders have been linked to obesity morbid obesity and to evaluate by measuring colonic transit times (CTTs) (3,4). In adults, gastroesophageal reflux disease is associated with whether decreased colonic motility is present in these children. increasing body mass index (BMI), as are abdominal pain and Patients and Methods: Ninety-one children with morbid obesity ages 8 to bloating (3,4). In contrast to studies in adults reporting an increase 18 years, entering a prospective, randomized controlled study evaluating the of diarrhea in obesity, recent studies in children found an increased effect of an outpatient versus inpatient treatment program of obesity, prevalence of constipation in a group of children with obesity and, participated. All of the children ﬁlled out a standardized questionnaire vice versa, a higher prevalence of obesity in the constipated group regarding their bowel habits, and CCTs were measured using (5–7). The mechanisms underlying the relation between obesity radioopaque markers. Food diaries were also recorded to evaluate their diet. and constipation are still unknown and may involve motor and Results: A total of 19 children (21%) had functional constipation according sensory abnormalities (3). to the Rome III criteria, whereas 1 child had functional nonretentive fecal A noninvasive method to assess colonic motility is total and incontinence. Total CTT exceeded 62 hours in only 10.5% of the children segmental colonic transit time (CTT) measurement using radio- with constipation, and among them, 2 had a total CTT of >100 hours. In the opaque markers (8–10). In both adults and children, measuring nonconstipated group 8.3% had a delayed CTT. Furthermore, no difference CCT helps to differentiate among different subgroups of patients. It was found between the diet of children with or without constipation, has been suggested that slow transit constipation also affects a speciﬁcally not with respect to ﬁber and fat intake. significant subgroup of children with disorders of defecation Conclusions: Our study conﬁrms a high frequency of functional (11,12). It is unknown whether delayed colonic transit plays a role constipation in children with obesity, using the Rome III criteria. in children with obesity with constipation. However, abnormal colonic motility, as measured by CCT, was delayed The purpose of the present study was to determine the in only a minority of patients. No relation was found between constipation in frequency of functional constipation in children with morbid these children and ﬁber or fat intake. obesity and to evaluate whether delayed colonic motility is present Key Words: child, colonic transit, constipation, fecal incontinence, in these children by measuring CCTs. frequency, obesity (JPGN 2011;00: 00–00) PATIENTS AND METHODS Participants were children ages 8 to 18 years who entered a prospective randomized controlled study evaluating the effect of an C hildhood obesity has become one of the rising health con- cerns worldwide and is associated with a number of comor- bidities. Even at a young age, being overweight or obese signifi- outpatient versus inpatient treatment of obesity at a specialized obesity clinic (Heideheuvel, Hilversum, the Netherlands) between 2004 and 2007. Inclusion criteria included a BMI of 35 and above, adjusted for age and sex, or a BMI of 30 in the presence of obesity- cantly increases the chance of developing serious chronic related morbidity. BMI was calculated as weight in kilograms divided by height in square meters (kg/m2). Age adjustment was Received November 23, 2009; accepted June 17, 2010. From the ÃDepartment of Pediatric Gastroenterology and Nutrition, performed based on the curves corresponding to adult BMI cutoff Emma’s Children’s Hospital/AMC, Amsterdam, the yDepartment of points of 25 and 30 published by Cole et al (13). To obtain the curve Pediatric Pulmonology, Emma’s Children’s Hospital/AMC, Amsterdam, corresponding to an adult BMI of 35, the difference of the distance the zDepartment of Radiology, Tergooiziekenhuizen, Hilversum, the of the 25 and 30 curves was added to the 30 curve. Netherlands, and the §Department of Gastroenterology and Hepatology, Patients were excluded if they had a psychiatric disorder (eg, Nationwide Children’s Hospital, Columbus, OH. schizophrenia, severe autism, mental retardation) or other serious Address correspondence and reprint requests to Olivia Liem, MD, Emma medical conditions that would preclude participation in the pro- Children’s Hospital/Academic Medical Center, Department of Pediatric gram. Patients taking medication that potentially cause significant Gastroenterology and Nutrition, Meibergdreef 9, C2-312, 1105 AZ weight gain or medication for weight loss were also excluded as Amsterdam, The Netherlands (e-mail: email@example.com). were participants using medications for weight loss or involved in a Olga H. vd Baan-Slootweg and Olivia Liem contributed equally to this manuscript. coexisting weight management program. The authors report no conﬂicts of interest. At intake, before any intervention, a standardized question- Copyright # 2011 by European Society for Pediatric Gastroenterology, naire regarding bowel habits was filled out and a CTT study was Hepatology, and Nutrition and North American Society for Pediatric performed. A bowel diary was also used for at least 2 weeks, Gastroenterology, Hepatology, and Nutrition documenting bowel movement and fecal incontinence frequency. DOI: 10.1097/MPG.0b013e3181ef8e3c Functional constipation was defined using Rome III criteria (14). At JPGN Volume 00, Number 00, Month 2011 1Copyright 2011 by ESPGHAN and NASPGHAN. Unauthorized reproduction of this article is prohibited.
vd Baan-Slootweg et al JPGN Volume 00, Number 00, Month 2011 least 2 of the following criteria had to be present for 8 weeks: 7 times per week (1–14 vs 3–21, P ¼ 0.07 for constipation and no defecation less than 3 times per week, !1 fecal incontinence constipation, respectively). Children with constipation had signifi- episodes per week, passage of large amounts of stool, presence cantly more episodes of fecal incontinence (21% vs 1%, P 0.01) of fecal impaction, painful or hard defecation, and withholding and showed more withholding behavior (67% vs 13%, P 0.01). behavior. Physical examination was performed on all of the chil- Only children with constipation showed presence of fecal impaction dren, including a rectal examination in 69 patients. (11%) and hard or painful defecation (47% and 21%, respectively). Food intake was measured using a 7-day dietary record. One child had fecal incontinence without any symptoms of con- Subjects received instructions from a dietitian on how to keep a food stipation and thus fulfilled the criteria for functional nonretentive record and were asked not to change their habitual food intakes. The fecal incontinence. In line with the latter diagnosis we found a data in the food records were used to calculate intakes of total daily normal CTT in this child. energy, fat, and fiber with a computer program based on food tables (BECEL nutrition program, version 5.05, 1995; Nederlandse Uni- lever Bedrijven BV, Rotterdam, the Netherlands). Colonic Transit Time All of the children underwent a CTT study using the method Table 1 shows the total and segmental CCTs at entry to the described by Bouchoucha et al (15) . Treatment with oral or rectal study. Both groups of children had a median total CTT of 26.4 hours. laxatives was discontinued for at least 1 week before the test. They Prolonged total CTT— exceeding 62 hours— was found in 10.5% then ingested a capsule containing 10 radioopaque markers on 6 of the children with constipation, and among them, 2 had a total consecutive mornings. An abdominal x-ray was obtained on day 7. CTT of 100 hours. In the nonconstipated group 8.3% had delayed Localization of markers was based on the identification of bony CTT. No difference was found in the RTTs between children with landmarks and gaseous outlines as described by Arhan et al (8). and without constipation. The children who received laxative Markers were counted in the right, left, and rectosigmoid regions, treatment (n ¼ 7) in the past or still had laxative treatment and mean segmental transit times were calculated according to a (n ¼ 4) tended to have a longer total CTT with a difference that previously described formula (colon transit time ¼ sum of approached statistically significance (P ¼ 0.056). Prolonged total markers Â 2.4). The normal ranges for total and segmental transit CTT was more frequent in the children who had used laxatives times were based on the upper limits (mean þ 2 SD) from a study in (36% vs 5%, P 0.01). healthy children. On the basis of those data, a CTT of 62 hours was considered delayed. The upper limits of the normal range for right colon, left colon, and rectosigmoid transit time (RSTT) were 18, 20, Diet and 34 hours, respectively. The study protocol was approved by the medical ethical A total of 68 children (75%) completed the food diary. There committee of the Academic Medical Centre in Amsterdam, the was no difference in median caloric intake between children with Netherlands. Written informed consent was obtained from the and without constipation (1452 vs 1628 kcal/day, P ¼ 0.129). Fifty- parents or guardians of the children participating and assent from five percent of the children were consuming 30% of their total all of the children 12 years and older. energy as fat, with no difference in fat intake between children with and without constipation (30% vs 32%, P ¼ 0.128). Fiber intake was Statistical Analysis below the minimum daily recommended quantity (age þ 5 g) in 74% of all of the children. Children with constipation had a median Statistical analysis of the data was conducted using the statistical software package SPSS (version 14.0; SPSS Inc, Chicago, IL). Baseline characteristics of the cohort were analyzed in a TABLE 1. Total and segmental CCTs descriptive way. Median values and ranges were used if the distri- bution of continuous variables was skewed. Nonparametric (Mann- Children with Children without Whitney U and Kruskal-Wallis) and x2 or Fisher exact statistics constipation constipation were used to test for differences between groups. Spearman cor- Transit time, h (n ¼ 19) (n ¼ 72) relation equations were used to evaluate the correlation between features. P 0.05 was considered significant. Total colon Median 26.4 26.4 RESULTS 25th–75th percentiles 14.4–52.8 12.0–40.2 A total of 91 consecutive children with morbid obesity (34% Delayed 62 h, % 10.5 8.3 boys) completed our standardized questionnaire and underwent a Ascending colon CTT study. The median age at intake was 15 years (8–18 years), Median 4.8 2.4 and all of the children had a corrected BMI 35 or 30 kg/m2 with a 25th–75th percentiles 0–12.0 2.4–9.6 comorbidity. Overall, 19 children (21%) fulfilled the Rome III Delayed 18 h, % 5.3 5.6 criteria for functional constipation. Of those children, 4 patients Descending colon were already using laxatives. Seven other children did not fulfill the Median 2.4 2.4 Rome III criteria at intake but had received laxatives in the past. 25th–75th percentiles 0–7.2 0–9.0 Delayed 20 h, % 15.8 9.7 Constipated Children vs Nonconstipated Rectosigmoid Children Median 16.8 14.4 25th–75th percentiles 4.8–38 4.8–25.8 Children with constipation were younger (14.0 vs 15.5, Delayed 34 h, % 26.3 17.7 P ¼ 0.02) than children without constipation. No difference was found in sex between children with or without constipation. The Mann-Whitney U test was used. P 0.05 was deemed signiﬁcant. median weekly frequency of bowel movements at presentation was CCT ¼ colonic transit time. 2 www.jpgn.orgCopyright 2011 by ESPGHAN and NASPGHAN. Unauthorized reproduction of this article is prohibited.
JPGN Volume 00, Number 00, Month 2011 Constipation and CTTs in Children With Morbid Obesity fiber intake of 66% (range 20–147) of the recommended amount, fat-containing meals were shown to induce more simultaneous and and children without constipation consumed 77% (range 25–166). retrograde contractions that may delay stool transit. No CCT studies This difference was not statistically significant (P ¼ 0.42). Overall, have been done to look at this phenomenon. 63% of children with constipation had fiber intake lower than In conclusion, our study confirms that there is a higher recommended compared with 53% of the children without consti- frequency of childhood constipation in children with obesity using pation (P ¼ 0.88). No correlation could be found between total the Rome III criteria. We showed that the increased frequency was transit time and fiber or fat intake (r ¼ À0.02, P ¼ 0.89 and not due to decreased colonic motility because only a minority of the r ¼ À0.08, P ¼ 0.65, respectively). children with obesity had a prolonged CCT. The difference in frequency could also not be explained by differences in the diet, especially in fiber or fat intake. Therefore, other studies are needed DISCUSSION to elucidate the relation between constipation and obesity in The present prospective study reports a frequency of 21% of children because other factors such as hormones and exercise constipation in children with morbid obesity according to the Rome may also play a role. III criteria. This is significantly higher than the prevalence of 8.9% found in children worldwide (16). The increased frequency could not be explained by delayed colonic transit, which was present in Acknowledgment: The authors thank Christine Tamminga for only 8.8% of all of the children and 10.5% of the children with assistance in the acquisition and processing of the data. constipation. In earlier studies in children with constipation, CTT was REFERENCES delayed in approximately 50% of children (17,18). In such studies, a 1. Freedman DS, Dietz WH, Srinivasan SR, et al. The relation of over- low defecation frequency, a high number of fecal incontinence weight to cardiovascular risk factors among children and adolescents: episodes, in combination with palpable stools in the rectum corre- the Bogalusa Heart Study. Pediatrics 1999;103:1175–82. lated well with prolonged total CTT and especially RSTT (19). The 2. Sagi R, Reif S, Neuman G, et al. Nonalcoholic fatty liver disease in normal CTT findings found in the majority of patients with obesity overweight children and adolescents. 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