Childhood obesity has become one of the rising health concerns worldwide and is associated with a number of comorbidities. Even at a young age, being overweight or obese significantly increases the chance of developing serious chronic conditions such as hypertension, hepatosteatosis, and diabetes mellitus type 2 (1,2). In addition to these comorbid conditions, functional gastrointestinal disorders have been linked to obesity (3,4). In adults, gastroesophageal reflux disease is associated with increasing body mass index (BMI), as are abdominal pain and bloating (3,4). In contrast to studies in adults reporting an increase of diarrhea in obesity, recent studies in children found an increased prevalence of constipation in a group of children with obesity and, vice versa, a higher prevalence of obesity in the constipated group (5–7). The mechanisms underlying the relation between obesity and constipation are still unknown and may involve motor and sensory abnormalities (3).
A noninvasive method to assess colonic motility is total and segmental colonic transit time (CTT) measurement using radioopaque markers (8–10). In both adults and children, measuring CTT helps to differentiate among different subgroups of patients. It has been suggested that slow transit constipation also affects a significant subgroup of children with disorders of defecation (11,12). It is unknown whether delayed colonic transit plays a role in children with obesity with constipation.
The purpose of the present study was to determine the frequency of functional constipation in children with morbid obesity and to evaluate whether delayed colonic motility is present in these children by measuring CTTs.
PATIENTS AND METHODS
Participants were children ages 8 to 18 years who entered a prospective randomized controlled study evaluating the effect of an 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-related morbidity. BMI was calculated as weight in kilograms divided by height in square meters (kg/m2). Age adjustment was performed based on the curves corresponding to adult BMI cutoff points of 25 and 30 published by Cole et al (13). To obtain the curve corresponding to an adult BMI of 35, the difference of the distance of the 25 and 30 curves was added to the 30 curve.
Patients were excluded if they had a psychiatric disorder (eg, schizophrenia, severe autism, mental retardation) or other serious medical conditions that would preclude participation in the program. Patients taking medication that potentially cause significant weight gain or medication for weight loss were also excluded as were participants using medications for weight loss or involved in a coexisting weight management program.
At intake, before any intervention, a standardized questionnaire regarding bowel habits was filled out and a CTT study was performed. A bowel diary was also used for at least 2 weeks, documenting bowel movement and fecal incontinence frequency. Functional constipation was defined using Rome III criteria (14). At least 2 of the following criteria had to be present for 8 weeks: defecation less than 3 times per week, ≥1 fecal incontinence episodes per week, passage of large amounts of stool, presence of fecal impaction, painful or hard defecation, and withholding behavior. Physical examination was performed on all of the children, including a rectal examination in 69 patients.
Food intake was measured using a 7-day dietary record. Subjects received instructions from a dietitian on how to keep a food record and were asked not to change their habitual food intakes. The data in the food records were used to calculate intakes of total daily energy, fat, and fiber with a computer program based on food tables (BECEL nutrition program, version 5.05, 1995; Nederlandse Unilever Bedrijven BV, Rotterdam, the Netherlands).
All of the children underwent a CTT study using the method described by Bouchoucha et al (15). Treatment with oral or rectal laxatives was discontinued for at least 1 week before the test. They then ingested a capsule containing 10 radioopaque markers on 6 consecutive mornings. An abdominal x-ray was obtained on day 7. Localization of markers was based on the identification of bony landmarks and gaseous outlines as described by Arhan et al (8). Markers were counted in the right, left, and rectosigmoid regions, and mean segmental transit times were calculated according to a previously described formula (colon transit time = sum of markers × 2.4). The normal ranges for total and segmental transit times were based on the upper limits (mean + 2 SD) from a study in 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, and 34 hours, respectively.
The study protocol was approved by the medical ethical committee of the Academic Medical Centre in Amsterdam, the Netherlands. Written informed consent was obtained from the parents or guardians of the children participating and assent from all of the children 12 years and older.
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 descriptive way. Median values and ranges were used if the distribution of continuous variables was skewed. Nonparametric (Mann-Whitney U and Kruskal-Wallis) and χ2 or Fisher exact statistics were used to test for differences between groups. Spearman correlation equations were used to evaluate the correlation between features. P < 0.05 was considered significant.
A total of 91 consecutive children with morbid obesity (34% boys) completed our standardized questionnaire and underwent a CTT study. The median age at intake was 15 years (8–18 years), and all of the children had a corrected BMI >35 or 30 kg/m2 with a comorbidity. Overall, 19 children (21%) fulfilled the Rome III criteria for functional constipation. Of those children, 4 patients were already using laxatives. Seven other children did not fulfill the Rome III criteria at intake but had received laxatives in the past.
Constipated Children vs Nonconstipated Children
Children with constipation were younger (14.0 vs 15.5, P = 0.02) than children without constipation. No difference was found in sex between children with or without constipation. The median weekly frequency of bowel movements at presentation was 7 times per week (1–14 vs 3–21, P = 0.07 for constipation and no constipation, respectively). Children with constipation had significantly more episodes of fecal incontinence (21% vs 1%, P < 0.01) and showed more withholding behavior (67% vs 13%, P < 0.01). Only children with constipation showed presence of fecal impaction (11%) and hard or painful defecation (47% and 21%, respectively). One child had fecal incontinence without any symptoms of constipation and thus fulfilled the criteria for functional nonretentive fecal incontinence. In line with the latter diagnosis we found a normal CTT in this child.
Colonic Transit Time
Table 1 shows the total and segmental CTTs at entry to the study. Both groups of children had a median total CTT of 26.4 hours. Prolonged total CTT— exceeding 62 hours— was found in 10.5% of the children with constipation, and among them, 2 had a total CTT of >100 hours. In the nonconstipated group 8.3% had delayed CTT. No difference was found in the RTTs between children with and without constipation. The children who received laxative treatment (n = 7) in the past or still had laxative treatment (n = 4) tended to have a longer total CTT with a difference that approached statistically significance (P = 0.056). Prolonged total CTT was more frequent in the children who had used laxatives (36% vs 5%, P < 0.01).
A total of 68 children (75%) completed the food diary. There was no difference in median caloric intake between children with and without constipation (1452 vs 1628 kcal/day, P = 0.129). Fifty-five percent of the children were consuming >30% of their total energy as fat, with no difference in fat intake between children with and without constipation (30% vs 32%, P = 0.128). Fiber intake was below the minimum daily recommended quantity (age + 5 g) in 74% of all of the children. Children with constipation had a median fiber intake of 66% (range 20–147) of the recommended amount, and children without constipation consumed 77% (range 25–166). This difference was not statistically significant (P = 0.42). Overall, 63% of children with constipation had fiber intake lower than recommended compared with 53% of the children without constipation (P = 0.88). No correlation could be found between total transit time and fiber or fat intake (r = −0.02, P = 0.89 and r = −0.08, P = 0.65, respectively).
The present prospective study reports a frequency of 21% of constipation in children with morbid obesity according to the Rome 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 only 8.8% of all of the children and 10.5% of the children with constipation.
In earlier studies in children with constipation, CTT was delayed in approximately 50% of children (17,18). In such studies, a low defecation frequency, a high number of fecal incontinence episodes, in combination with palpable stools in the rectum correlated well with prolonged total CTT and especially RSTT (19). The normal CTT findings found in the majority of patients with obesity concur with the mild symptoms of constipation found in the present study.
Infrequent painful defecation and fecal incontinence are the major clinical features present in 49% and 84% of children with constipation, respectively (18,20). In our study, however, only 1 child in the constipated group defecated fewer than 3 times per week. Fecal incontinence as result of severe fecal impaction was present in only 20% of the children with constipation. A Brazilian population-based study looking at the prevalence of constipation found scybalous stools in 66% of children with constipation and painful defecation in 38%, with only 31.2% of them having fecal incontinence (24). We hypothesize that the lower prevalence of fecal incontinence in our study and the Brazilian study could be explained by the different severity of symptoms. Thus, a lower prevalence of fecal incontinence can be expected when compared with a cohort study describing constipated children with constipation as the major complaint. This may explain why only a few children in our study who had functional constipation according to the Rome III criteria were using laxatives and those who had or were using laxatives tended to have a longer CTT; or maybe children with obesity may not seek medical attention for their defecation problems due to embarrassment.
Diet as a reason why children with obesity are more constipated comes to mind when trying to find other hypotheses. Dietary fiber intake in particular was of interest because it has been described that whole grains consumption is inversely related to BMI in adults (22). The role of dietary fiber in childhood obesity, however, is not known, and conflicting reports exist about the role of fiber in childhood constipation (21,23–25). Data on the effect of fibers on CTT are also inconsistent (26,27). These contradictions have been described in studies in adults as well (9,10,28). Our study showed that the majority of children did not consume the minimum recommended dietary fiber, but McClung et al (29) found that even in health-conscious families, approximately half of the healthy children do not receive the recommended daily grams of fiber. The children with constipation in our study tended to have a lower fiber intake, but this was not statistically significant.
No difference in fat intake, another important element of a diet that can influence motility, was also found. Previously it was shown that meals containing fat delay gastric emptying and small bowel transit (30). Using colonic manometry predominantly fat-containing meals were shown to induce more simultaneous and retrograde contractions that may delay stool transit. No CTT studies have been done to look at this phenomenon.
In conclusion, our study confirms that there is a higher frequency of childhood constipation in children with obesity using the Rome III criteria. We showed that the increased frequency was not due to decreased colonic motility because only a minority of the children with obesity had a prolonged CTT. 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 to elucidate the relation between constipation and obesity in children because other factors such as hormones and exercise may also play a role.
The authors thank Christine Tamminga for assistance in the acquisition and processing of the data.
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