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Original Articles: Gastroenterology

Association Between Obesity/Overweight and Functional Gastrointestinal Disorders in Children

Tambucci, Renato∗,†; Quitadamo, Paolo‡,§; Ambrosi, Michela; De Angelis, Paola; Angelino, Giulia; Stagi, Stefano||; Verrotti, Albero; Staiano, Annamaria; Farello, Giovanni

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Journal of Pediatric Gastroenterology and Nutrition: April 2019 - Volume 68 - Issue 4 - p 517-520
doi: 10.1097/MPG.0000000000002208
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Abstract

What Is Known

  • Over the last decades the prevalence of obesity among children and adolescents has increased dramatically.
  • Obesity-related comorbidities include a wide variety of severe chronic diseases that may involve almost all organs and systems and may have significant long-term detrimental effects on both health and life expectancy.

What Is New

  • The presents study reports an increased prevalence of functional gastrointestinal disorders in obese children and adolescents.
  • This finding may support the emerging conceptual view of biopsychological model, in which food and nutritional substances, microbial environment, and psychosocial factors play an important role in the pathogenesis of functional gastrointestinal disorders.

Over the last 4 decades the prevalence of obesity among children has increased dramatically and, coincidentally, the well-established comorbidities have become a major health challenge, associated to a significant increase in healthcare costs (1). Obesity-related comorbidities include a wide variety of severe chronic diseases that may involve almost all organs and may have significant long-term detrimental effects on both health and life expectancy. It has been estimated that a high body mass index (BMI) accounted for about 4 million deaths and 120 million disability-adjusted life-years worldwide in year 2015 (1).

Pediatric obesity predicts adult obesity. Indeed, approximately 20% of the obese infants will become obese children, 40% of the obese children will become obese teenagers, and 80% of obese teens will inevitably become obese adults (1). In addition to the potentially life-threatening diseases, such as type 2 diabetes mellitus syndrome, cardiovascular disease, and nonalcoholic fatty liver disease, obese children are more likely to develop psychological and behavioral disorders (2). Moreover, emerging data indicate that obesity is also associated with functional gastrointestinal disorders (FGIDs) (3,4). FGIDs are common disorders in children of all ages and include a range of chronic or recurrent gastrointestinal symptoms that cannot be explained by structural or biochemical abnormalities (5). The pathogenesis of FGIDs remains elusive and is likely multifactorial. Assuming that obesity and FGIDs are mechanistically linked, studying its relationship may provide insights into the pathophysiology of FGIDs. To date, few studies have been carried out to explore the association between excess body weight and FGIDs in children and most of them suffer from drawbacks such as retrospective study design, lack of control population, or unclear diagnostic criteria.

The primary aim of the present observational, case-control study was to determine whether obese/overweight children and adolescents have a greater prevalence of FGIDs than healthy normal-weight peers. Secondary aims were to summarize the existing data on the association between obesity and FGIDs in children and to discuss the possible role of pathophysiological mechanisms that might link these 2 common conditions.

METHODS

Overweight and obese children aged 4 to 18 years were consecutively recruited from those attending the obesity outpatient clinic from January 2016 to July 2017 at the Department of Pediatrics of the San Salvatore Hospital in L’Aquila, Italy. According to the Center for Disease Control and Prevention definitions, overweight is defined as a BMI at or above the 85th percentile and lower than the 95th percentile. Obesity is defined as a BMI at or above the 95th percentile (6). Normal-weight children defined as having a BMI between the 5th and the 85th percentile were enrolled as comparison group (6). Controls were consecutively recruited from children attending immunization clinic or the emergency department for a minor injury. Systemic and infectious diseases; previous surgery; genetic, metabolic, neurodevelopmental, and immune disorders; and cardiac, hepatic, or renal diseases were considered exclusion criteria for both cases and controls.

Demographic and past medical history data were obtained at baseline. All patients underwent auxological examination by experienced pediatric endocrinologists. Height was measured in the standing position by using a Harpenden stadiometer (Holtain, London, UK). Weight was measured to 0.1 kg with an electronic stand-on scale. BMI was calculated by dividing weight (in kg) by height squared (in m). Data on BMI were converted into standard deviation scores according to the Italian reference values (7). Afterwards, children were evaluated by pediatric gastroenterologists to identify the possible presence of FGIDs, according to the Rome III criteria (5). All children were interviewed using the Italian version of the Questionnaire on Pediatric Gastrointestinal Symptoms-Rome III Version (8). Children older than 10 years were interviewed directly, whereas parents or caregivers of children younger than 10 were asked to fulfill the questionnaire on behalf of the patient.

The study was conducted in accordance with the Helsinki Declaration, and ethical approval was obtained by the Ethics Committee of the University of L’Aquila. All the patients and/or their parents or caregivers agreed to participate and signed an informed consent.

GraphPad Prism software version 5.0 was used for the statistical analyses. Continuous variables were compared using Student t test. Chi-squared test or Fisher exact test were used, where appropriate, to analyze categorical variables. Ordinal variables were evaluated using the nonparametric Wilcoxon test. A P value <0.05 was considered statistically significant.

RESULTS

A total of 114 obese/overweight children were screened throughout the study period. Among them, 11 were excluded due to concurrent diseases (3 gastroesophageal reflux disease, 2 celiac disease, 2 autism spectrum disorder, 2 previous bowel surgery, 1 growth hormone deficiency, 1 congenital heart defect). Out of the remaining 103 children, 33 of 103 (32%) were overweight and 70 of 103 (68%) were obese. One hundred fifteen normal-weight children were enrolled as comparison group (62 from the immunization service and 53 from the emergency department). Baseline demographic and auxological characteristics of both groups are summarized in Table 1. No significant differences between them were found as far as sex and age are concerned.

TABLE 1
TABLE 1:
Demographic and auxological characteristics

As detailed in Table 2, obese/overweight children were significantly more likely to have at least one FGID as compared with normal-weight children (47.57% vs 17.39%, respectively).

TABLE 2
TABLE 2:
Prevalence of functional gastrointestinal disorders

DISCUSSION

Our data support the hypothesis that FGIDs are associated with excessive body weight in children. FGIDs include a combination of chronic or recurrent gastrointestinal age-dependent disorders not explained by known biochemical or structural abnormalities (9).

A complete understanding of the pathophysiology of FGIDs remains elusive (9,10). FGIDs are a multifactorial condition and several pathophysiological mechanisms appear to contribute to them, including altered motility, visceral hyperalgesia, brain-gut disturbances, genetic and environmental factors, and psychosocial upsets (10).

Studying the relationship between FGIDs and other conditions may help to better identify their complex biology and possibly optimize the therapeutic approaches. Although recent emerging epidemiological data in both adult and pediatric populations suggest that obesity may predispose to develop FGIDs, the relationship between obesity and FGIDs is currently a matter of debate (3,11).

Association Between Functional Gastrointestinal Disorders and Obesity: Previous Data

A pediatric review published a few years ago found that obese and overweight children had a higher prevalence of FGIDs than normal-weight children (12). Indeed, almost half of the obese/overweight children had at least 1 FGID. Despite the limited number of publications, the heterogeneity in study designs, and the differences in diagnostic criteria and recruitment settings, the authors concluded that functional abdominal pain syndrome, irritable bowel syndrome (IBS), and functional constipation (FC) were significantly related to excess body weight.

Our results indicate a higher prevalence of FC in obese/overweight children than nonobese peers (19% and 9%, respectively). The first report suggesting a significant association between FC and obesity in children was published by Fishman et al in 2004. The study lacked a control population, but the authors concluded that the prevalence of FC in their cohort of obese children was higher than the historical prevalence observed in the general pediatric population (13). Over the following years, other studies analyzed the prevalence of obesity/overweight in children with FC, reporting a significantly higher prevalence compared with the control healthy population (12,14–16).

In contrast with the above-mentioned studies, 2 large population-based studies found no association between FC (according to the Rome III criteria) and childhood overweight or obesity (17,18). Intrinsic selection bias arising from population-based sampling methods, especially when the relationship between highly prevalent conditions is explored, may explain these inconsistent results.

Finally, a recent comprehensive systematic review showed that the current available data could not confirm or refute the association between functional defecation disorders and overweight/obesity because the results are conflicting across the studies. Moreover, the authors found that only 1 study was rated to be of good quality, whereas most studies were rated to be of fair or poor quality, suggesting that the results should have been interpreted with caution (19).

The association between obesity and IBS in children has been reported by 2 pediatric studies (12,16). In 2011 Bonilla et al, however, analyzed 351 children diagnosed with abdominal pain-related FGIDs (functional abdominal pain [FAP], IBS, and functional dyspepsia [FD]) according to the Rome II criteria, reporting no baseline differences in terms of frequency and intensity of symptoms between obese and nonobese children. Nevertheless, at long-term follow-up patients with obesity were more likely to have persistence of abdominal complains, higher intensity, and higher frequency of pain than nonobese patients (20).

Data on the association between FAP and childhood obesity are even less consistent. In a large school-based study Malaty et al (21) found that obese children were more likely to suffer from recurrent abdominal pain compared to nonobese children (33.3% vs 22.5%, respectively). Nevertheless, later on the same above-mentioned studies by Teitelbaum et al, Phatak and Pashankar et al, and Bonilla et al (12,16,20) failed to find any significant association between obesity and FAP in children. Our data on FAP confirm these results, but the low number of patients detected does not allow for definitive conclusions.

Although we found that FD was the most prevalent disorder in our cohort of patients with obesity, data from scientific literature on the relationship between FD and obesity in children are too limited to draw any conclusions (15). A recent study by Jung et al (22) showed that visceral adiposity was associated with an increased risk of FD, suggesting that visceral adiposity may play an important role as a metabolically active organ in the pathogenesis of FD.

Possible Pathophysiological Link Between Functional Gastrointestinal Disorders and Obesity

Several explanations have been offered to understand how obesity could cause FGIDs. A caloric intake greater than physiologic needs and notably excessive consumption of high glycemic index foods and sugar-containing beverages associated with low-fiber and high-fat diet are considered causal factors for obesity development (23). Recently, increasing attention has been paid to the effects of food on the onset of FGIDs. Consistent evidence supports the notion that diet containing fermentable oligo-, di-, and monosaccharides and polyols may trigger gastrointestinal symptoms in patients with IBS. Conversely, a diet poor in fermentable oligo-, di-, and monosaccharides and polyols offers considerable symptom relief in the majority of patients (24). Dietary habits and lifestyle behaviors predisposing to excessive weight gain have also been linked to FC development in children (25,26). Furthermore, an increased consumption of fatty meal may result in delayed gastric emptying while excessive food intake during a relatively short time may potentially overcome the functional accommodation and emptying of the stomach, leading to the development of dyspeptic symptoms in individuals with obesity (27).

In addition to dietary habits, obesity and FGIDs share a further potential pathophysiological factor that is under increased consideration: the gut microbiota. During the past years, many studies have focused on the role of gut microbiome in the genesis of FGIDs, and the emerging concept of the microbiome-gut-brain axis has been proposed (28–30). Changes in the gut microbiota composition have been implied in the onset and maintenance of FGIDs, but they have been also suggested as an important factor influencing energy metabolism and development of obesity (31–33).

Finally, psychosocial disorders are considered to play an important role in the pathophysiology of both obesity and FGIDs. Several investigators have clearly shown that psychiatric disorders, such as anxiety, depression, and trauma disorders, are highly prevalent in patients with FGIDs (34–36). Moreover, recent evidence suggests that obesity and psychological problems are not separate conditions but share common biological mechanisms (37–39). Therefore, novel insights into the role of psychosocial factors in children with obesity may help to improve individualized approach for FGIDs.

In summary, our data suggest that FGIDs and obesity are associated conditions in children. Compared to previous articles, we acknowledge that the present study has some undeniable strengths. We tried to keep possible biases to a minimum by prospectively enrolling our patients. Moreover, a control group of age- and sex-matched healthy children was enrolled and the diagnosis of FGIDs was made according to the standardized Rome III criteria by using validated questionnaires for children.

We are also aware that our study has some drawbacks, mainly bound to the study design. Results arise from a single “snapshot” of a population sample, in which exposure (obesity) and outcome (FGIDs) have been determined simultaneously. Therefore, it is not possible to determine whether the reported association implies a causality relationship or it is the mere consequence of the high prevalence of both conditions. Moreover, children were enrolled in a tertiary care setting, and thus being perhaps poorly representative of the entire population. Finally, our study lacked a psychological assessment and did not provide information on symptom severity. Understanding if FGIDs are even more severe (and more frequent) in children with obesity could represent a further field to be explored in the future.

Our study may establish a solid basis for further researches about obesity and FGIDs in children. In the emerging conceptual view of the biopsychological model, food and nutritional substances, gut microbial environment, and psychosocial factors play an important role in the pathogenesis of FGIDs. The high prevalence of FGIDs in children with obesity may support this model. Further studies are needed for a more exact and detailed definition of this model, and for the establishment of causal relationships.

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Keywords:

biopsychosocial model; functional constipation; functional dyspepsia; irritable bowel syndrome

Copyright © 2019 by European Society for Pediatric Gastroenterology, Hepatology, and Nutrition and North American Society for Pediatric Gastroenterology, Hepatology, and Nutrition