Journal of Pediatric Gastroenterology & Nutrition:
Original Articles: Gastroenterology
Abdominal Pain–Predominant Functional Gastrointestinal Diseases in Children and Adolescents: Prevalence, Symptomatology, and Association With Emotional Stress
Devanarayana, Niranga Manjuri*; Mettananda, Sachith†; Liyanarachchi, Chathurangi†; Nanayakkara, Navoda†; Mendis, Niranjala†; Perera, Nimnadi†; Rajindrajith, Shaman†
*Department of Physiology
†Department of Paediatrics, Faculty of Medicine, University of Kelaniya, Ragama, Sri Lanka.
Address correspondence and reprint requests to Dr Niranga M Devanarayana, Department of Physiology, Faculty of Medicine, Talagolla Road, Ragama, Sri Lanka (e-mail: firstname.lastname@example.org).
Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal's Website (www.jpgn.org).
Received 11 January, 2011
Accepted 20 May, 2011
The study received financial support from the University of Kelaniya, Sri Lanka.
The authors report no conflicts of interest.
Background and Objective: Functional gastrointestinal disorders (FGD) are common among children, but little is known regarding their prevalence in developing countries. We assessed the prevalence of abdominal pain–predominant FGD, in addition to the predisposing factors and symptomatology, in Sri Lankan children.
Patients and Methods: A cross-sectional survey was conducted among a randomly selected group of 10- to 16-year-olds in 8 randomly selected schools in 4 provinces in Sri Lanka. A validated, self-administered questionnaire was completed by children independently in an examination setting. FGD were diagnosed using Rome III criteria.
Results: A total of 2180 questionnaires were distributed and 2163 (99.2%) were included in the analysis (1189 [55%] boys, mean age 13.4 years, standard deviation 1.8 years). Of them, 270 (12.5%) had at least 1 abdominal pain–predominant FGD. Irritable bowel syndrome (IBS) was seen in 107 (4.9%), functional dyspepsia in 54 (2.5%), functional abdominal pain in 96 (4.4%), and abdominal migraine (AM) in 21 (1.0%) (2 had AM and functional dyspepsia, 6 had AM and IBS). Extraintestinal symptoms were more common among affected children (P < 0.05). Abdominal pain–predominant FGD were higher in girls and those exposed to stressful events (P < 0.05). Prevalence negatively correlated with age (r = −0.05, P = 0.02).
Conclusions: Abdominal pain–predominant FGD affects 12.5% of children ages 10 to 16 years and constitutes a significant health problem in Sri Lanka. IBS is the most common FGD subtype present. Abdominal pain–predominant FGD are higher in girls and those exposed to emotional stress. Prevalence of FGD decreased with age. Extraintestinal symptoms are more frequent in affected children.
Chronic or recurrent abdominal pain (RAP) is a global health problem affecting 10% to 12% of children and adolescents (1–3). The majority of them have abdominal pain–predominant functional gastrointestinal diseases (FGD) and <25% have organic causes for their symptoms (4,5). The main abdominal pain–predominant FGD, defined in the Rome III criteria, are functional dyspepsia (FD), irritable bowel syndrome (IBS), abdominal migraine (AM), and functional abdominal pain (FAP) (6). Because the pathophysiology, clinical profile, and management strategies vary with the subtype (7,8), it is important to classify chronic/recurrent abdominal pain into different etiologic categories.
Epidemiological studies are needed to identify the true burden of these disorders in the community because a significant percentage of patients with FGD do not seek health care (9,10). So far, the majority of studies on these disorders are hospital based (4,11,12). There are only a few epidemiological studies published in the world, and data published so far have reported abdominal pain–predominant FGD in 13.8% of Asian children (13) and 0.5% of Western children (14).
Pain characteristics, associated symptoms, and bowel habits play a significant role in Rome III diagnostic criteria for abdominal pain–predominant FGD (6). It is also suggested that other somatic symptoms such as headache, limb pain, and sleeping difficulty are more common in children (15) and adults with IBS (16), but so far few studies have assessed intestinal-related and extraintestinal symptoms associated with abdominal pain–predominant FGD.
The exact etiology of FGD is not fully understood. The symptoms cannot be explained by the traditional biomedical model. The new biopsychosocial model suggests that these disorders originate from simultaneous interactions among biological, social, and psychological factors (17). Biological factors including familial predisposition (5), sociocultural factors including lower socioeconomic status (18) and psychological factors including emotional stress (19) are known to be associated with FGD. The interplay between these risk factors needs to be studied in depth to understand the possible pathological processes involving FGD, especially in children.
The present study was conducted with the objectives of identifying the prevalence of different types of abdominal pain–predominant FGD in Sri Lanka, clinical profile of the affected children, and social and psychological factors associated with these disorders.
PATIENTS AND METHODS
An island-wide, cross-sectional survey was conducted in 4 randomly selected provinces (out of 9 provinces) of Sri Lanka. From every selected province, 2 schools each (1 urban and 1 rural) were randomly selected. From every school, 12 classes each were randomly selected from academic years 6 to 11 (2 from each academic year). All of the children present in the selected classes on the day of the survey were included in the study. School administration and parents were informed and consent to administer the questionnaire was obtained before conducting the study.
Data were collected using a pretested questionnaire that consisted of 2 parts (the questionnaire can be accessed via http://links.lww.com/MPG/A56). Part 1 included questions on sociodemographic and family factors and exposure to stressful live events. Part 2 is the Questionnaire on Paediatric Gastrointestinal Symptoms-Rome III version (self-reported form for children and adolescents, 10 years of age and older) (20), translated into the native language and validated for Sri Lankan children. The questionnaire was administered in an examination setting to ensure confidentiality and privacy. Adequate time was given to each child to complete the questionnaire and research assistants were available during this period to clarify any question.
Children with abdominal pain were categorized into abdominal pain–predominant FGD (FD, IBS, AM, and FAP) using Rome III criteria for childhood FGD (6). In this survey, we did not perform a physical examination of affected children.
Data were analyzed using χ2 and Fisher exact tests using EpiInfo (EpiInfo 6, version 6.04 , Centers for Disease Control and Prevention, Atlanta, GA, and World Health Organization, Geneva, Switzerland). P <0.05 was taken as significant. Ethical approval for the present study was granted by the ethics committee of the Sri Lanka College of Paediatricians.
A total of 2180 questionnaires were distributed and all of them were returned. Of them, 2163 (99.2%) were included in the analysis (1189 [55%] boys, mean age 13.4 years, SD 1.8 years). Seventeen incompletely filled-out questionnaires were excluded from the analysis.
Prevalence of Abdominal Pain–Predominant FGD
According to Rome III criteria, 270 had at least 1 abdominal pain–predominant FGD (Table 1). Two children with AM also had FD and 6 with AM also had IBS. Of 96 children with FAP, 42 (43.8%) fulfilled criteria for FAP syndrome (FAPS). IBS and FD were significantly more common among girls and so was the total abdominal pain–predominant FGD. Figure 1 illustrates age-related predicted probability of having an abdominal pain–predominant FGD. There was a negative correlation between prevalence of abdominal pain–predominant FGD and age (correlation coefficient −0.05, 95% confidence interval [CI] −0.008 to −0.095, P = 0.02).
Association Between Sociodemographic Characteristics and Abdominal Pain–Predominant FGD
A total of 1893 children without abdominal pain predominant FGD were identified as controls. Table 2 demonstrates the association between the socioeconomic characteristics and abdominal pain–predominant FGD. Sociodemographic characteristics were not significantly different between children with abdominal pain–predominant FGD and controls (P > 0.05).
Pain Characteristics in Children With Abdominal Pain–Predominant FGD
Table 3 demonstrates the distribution of pain characteristics of children with abdominal pain–predominant FGD. The only characteristic that significantly differed between subtypes was the presence of severe abdominal pain, which was more common among children with AM (P <0.001).
Of 270 children with abdominal pain–predominant FGD, 87 (32.2%) had disturbances in school attendance because of pain (FD 22 [40.7%], IBS 36 [33.6%], AM 7 [33.3%], and FAP 22 [22.9%])
Intestinal and Extraintestinal Symptoms in Affected Children
Intestinal-related symptoms such as bloating, loss of appetite, nausea, vomiting, flatulence, and burping and extraintestinal symptoms such as headache, limb pain, sleeping difficulty, and photophobia were more common among children with FGD compared with controls (P < 0.05) (Table 4).
Association Between Stress and Abdominal Pain–Predominant FGD
Table 5 shows association between stressful life events and abdominal pain–predominant FGD. After multiple logistic regression analysis, separation from the best friend (adjusted odds ratio [OR] 1.5, 95% CI 1.1–2.1, P = 0.017), failure in an examination (adjusted OR 1.7, 95% CI 1.0–2.6, P = 0.033), loss of parent's job (adjusted OR 2.0, 95% CI 1.0–3.8, P = 0.039), and hospitalization of the child himself or herself for another illness (adjusted OR 1.6, 95% CI 1.0–2.4, P = 0.031) were independently associated with abdominal pain–predominant FGD.
Community-based studies to assess the burden of abdominal pain–predominant FGD in children are rare. In the present epidemiological survey we demonstrated that 12.5% of native Sri Lankan children had at least 1 abdominal pain–predominant FGD. IBS was the most prevalent FGD, followed by FAP and FD. There was a negative correlation between the prevalence of abdominal pain–predominant FGD and age. Intestinal-related and extraintestinal symptoms were more common in children with all 4 types of abdominal pain–predominant FGD compared with controls. There was a significant association between exposure to stressful life events and presence of an abdominal pain–predominant FGD.
Prevalence of FGD depends on several factors. Of them, the definition used in the diagnosis is 1 of the main determinants. A previous school-based study in children ages 10 to 16 years, using Rome III criteria, has shown IBS as the most common FGD followed by FD and FAP (13). In contrast, another study using Rome II criteria has shown FD as the most common abdominal pain–predominant FGD (14). Inclusion of children of different age groups and differences in diagnostic criteria and methods of data collection could have contributed to this difference. One percent of the children in our study had AM, lower than the previous study that found AM in 3% of schoolchildren (13). Another study from the United Kingdom, using different criteria, has shown AM in 4.1% (21). These differences of prevalence may be the result of small sample size and disparity of definitions. The prevalence of FAP in our sample is comparable to that previously reported in Sri Lanka (13). FAPS is a newly described entity in the Rome III process and indicates significant loss of daily function or having somatic symptoms (6). Forty-three percent of children with FAP had FAPS. Helgeland et al (4) have shown that nearly 60% of children with FAP had FAPS. Children referred to a secondary-care hospital would be more likely to have somatic symptoms and disruption of daily activities than a community sample and this probably explains the difference between the 2 studies.
In our sample, at all of the ages, girls had a significantly higher probability of having an abdominal pain–predominant FGD. We found that FD and IBS were significantly more common among girls. Similar to our results, a previous study conducted in children with abdominal pain has shown higher prevalence in girls (22). One hospital-based study in children with dyspepsia (23) and 3 studies in children with IBS failed to show a significant sex difference (13,15,24). Our findings are compatible with findings of adult studies from Western countries, which have shown that girls have a higher tendency to develop IBS (10). Heitkemper and Jarrett (25) have previously suggested the difference in hormonal profiles between girls and boys as a contributory factor for higher prevalence of IBS in women; however, in our sample, this sex difference was significant even in young girls (10–11 years) in whom the majority have not attained menarche and do not have the full hormonal profile of women. Therefore, we believe that the sex difference in the prevalence of IBS predate the effects of reproductive hormones. The observed sex difference may result from differences in pain perception between boys and girls. Visceral hypersensitivity plays an important role in the pathogenesis of abdominal pain–predominant FGD in children (26,27). A study comparing children with FAP and IBS has found a higher rectal hypersensitivity in girls than in boys (28). Adult studies have also shown similar results (29). Therefore, it is possible that the heightened visceral sensitivity in girls predisposes them to be more likely to manifest IBS. We failed to demonstrate a significant sex difference in AM. This is similar to the findings of Abu-Arafeh and Russell (21).
The prevalence of abdominal pain–predominant FGD declined with age in both boys and girls. The reason for this phenomenon is unclear. We previously reported a similar age-related decline in the prevalence of functional defecation disorders such as constipation (30) and fecal incontinence (18).
There are conflicting data on the association between socioeconomic factors and abdominal pain–predominant FGD. Previous studies in adults have shown that an affluent childhood living condition is associated with IBS (31,32). Similarly, adult studies in Asia (China, Singapore) have shown that the prevalence of IBS is higher among people who have achieved higher educational status (33,34). In contrast, Drossman et al (35) noted that functional bowel diseases are more common in households with lower incomes. Based on these data, in the present study we hypothesized that socioeconomic factors play a significant role in the development of FGD in children. In contrast to our hypothesis, we did not find a significant association between FGD and social class. Similar to our results, other studies in children with IBS (15) and RAP (2,36) have failed to demonstrate such an association. Therefore, it is possible that social factors may play only an inconsequential role in the causation of abdominal pain–predominant FGD in children. Psychological factors such as emotional stress and biological factors such as heightened visceral sensitivity (37) and abnormal motility (38) probably play a more significant part in the pathogenesis of these disorders.
In our study, most intestinal-related symptoms (bloating, loss of appetite, nausea, vomiting, flatus, and burping) were more common in FD, IBS, FAP, and AM compared with controls. Previous studies have shown that bloating is a significant problem in children (24) and adults (39) with IBS. Furthermore, bloating correlates with patient-perceived severity of IBS (40); however, association of these features with other abdominal pain–predominant FGD such as FD, AM, and FAP has not been described in children in the past. Delayed gastric emptying and abnormal antral motility have been reported in children with all 4 types of abdominal pain–predominant FGD (41). Gastrointestinal motility dysfunctions may have contributed to abnormal gas dynamics and, therefore, to increased flatulence and burping noted in our patients. Further studies involving children with abdominal pain–predominant FGD would help to explore this possibility. In the present study, loss of appetite and nausea were less prevalent in children with FD than in the other 3 types of FGD. Comparable to our results, a previous study using Rome II criteria has demonstrated early satiety in <10% of children with FD (42); however, in the same study, nausea is seen in approximately 70% of children with FD, which is significantly higher than in our sample. The previous study was conducted in a tertiary-care gastroenterology unit, whereas our study was a school survey. Differences in patient selection and variations in genetic and environmental factors between 2 communities may have caused this deference.
Pain characteristics of FD, IBS, FAP, and AM in our sample behaved as per definition. All of the children with FD had pain in the upper abdomen, 7% had daily symptoms, and only 22% had severe pain. In contrast to this, a hospital-based study by Hyams et al (23) reported daily symptoms in the majority (69%). Furthermore, in our sample, only 4.7% of children with IBS had daily symptoms and most of them had pain duration of <1 hour. Compared with these findings, a hospital-based study in the United States in children ages 5 to 17 years noted that 60% of them have daily symptoms, with 34% having pain duration of >1 hour (43). It is possible that children in our community-based sample have less severe pain and lower pain duration compared with both of these hospital-based studies. Severity of the pain is one of the main determinants of health care seeking. Therefore, children with a higher frequency of pain would seek health care more frequently and are more likely to be included in hospital-based studies. The majority of children with AM in our study had pain in the lower abdomen or around the umbilicus. Abu-Arafeh and Russell (21) noted that 78% of children with AM in their sample had periumbilical pain.
In our study, extraintestinal symptoms such as headache, difficulty in sleeping, limb pain, photophobia, and feeling light-headed were noted to occur more frequently in children with all 4 types of abdominal pain–predominant FGD. Similar to our findings, Dong et al (15) have reported headaches and difficulty in sleeping more commonly in children with IBS. Another community-based study has found that adults with dyspepsia have significantly higher somatic symptom scores than controls (9). Extraintestinal somatic symptoms are an integrated part of FGD and contribute significantly to the severity of diseases and quality of life (40). Therefore, it is important to seek these symptoms in the clinical evaluation of children because they may contribute to significant distress and poor quality of life.
Psychological stress plays a key role in initiating and precipitating FGD in susceptible individuals. Human and animal studies have shown that both psychological and physical stresses alter gastric motility and visceral sensitivity (44). In our study, school-related stressful life events such as separation from their best friend and failure at an examination, family-related events such as loss of a parent's job, and other stressors such as hospitalization of the child himself or herself for another illness were significantly associated with abdominal pain–predominant FGD. According to previous studies, RAP and defecation disorders such as constipation and fecal incontinence are more common among those exposed to stressful life events (18,19,30). Failure at an examination is a significant stress in the competitive school environment in Sri Lanka. Loss of job by a parent would undoubtedly put children under stress because of financial restrains. Alteration of the function of the brain-gut axis under these circumstances may have predisposed children to develop abdominal pain–predominant FGD. Furthermore, positive family history of functional gastrointestinal disorders and psychiatric disorders are recognized risk factors for developing FGD (45,46). Information regarding such disorders in first-degree relatives would have been useful to determine the familial tendency. Unfortunately, during validation of the questionnaire and a previous study (13), we understood that the majority of children are unaware of diseases and symptoms that are present in their family members, especially in parents. Therefore, we did not assess family history of FGD and psychiatric disorders in the present study.
The present study has several strengths. We have included more than 2000 children from 4 randomly selected provinces (out of 9) of the country to obtain a representative sample. Furthermore, we used standard Rome III criteria to diagnose FGD in children. In this questionnaire-based school survey, however, we did not perform a physical examination to exclude organic causes for abdominal pain. In a previous study we identified organic diseases in 10.9% of children with RAP. The organic diseases observed in the previous study include urinary tract infection, gastroesophageal reflux, urinary calculi, antral gastritis, and intestinal amoebiasis (5). Parasitic infestations such as giardiasis and amoebiasis have been considered to be possible mimickers of FGD; however, in that study, prevalence of these diseases was 1.8% (5). Similarly, several previous studies conducted in Sri Lanka have demonstrated a low prevalence of parasitic infections (47,48). Therefore, it is unlikely that parasitic infestations have directly contributed to abdominal symptoms in these children.
In conclusion, abdominal pain–predominant FGD are common among Sri Lankan children ages 10 to 16 years. IBS is the most common abdominal pain–predominant FGD diagnosed, followed by FAP and FD. Abdominal pain–predominant FGDs are significantly higher in girls compared with boys. There is a negative correlation between the age and prevalence of abdominal pain–predominant FGD. Intestinal-related and extraintestinal symptoms are more frequent in affected children, compared with controls. Exposure to stressful life events is significantly associated with abdominal pain–predominant FGD.
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