Abdominal pain (AP) is common in children (1–3). Thirty-eight percent of schoolage children report AP weekly, with 24% of them complaining of persistent AP for more than 8 weeks (4). A subset of children reporting AP meets symptom-based diagnostic criteria for an AP-related functional gastrointestinal disorder (FGID) (5,6). The affect of chronic AP and FGIDs in children's health is vast and probably underrecognized. Both, chronic AP and FGIDs are frequently associated with disability, psychological comorbidities, school absenteeism, and poor quality of life (4,7). Knowledge of the epidemiology of common disorders is critical to assess their affect in public health and to optimize health care planning. A review of the literature by our group revealed that current available epidemiological data on AP and FGIDs in children resulted from studies with methodological limitations. Most available data have been obtained by surveying children at the primary care setting, a strategy that is prone to selection bias or has not been conducted using up-to-date diagnostic criteria. Data from published studies corroborate these considerations. Only 2% of schoolage children reporting AP seek medical attention for their symptoms (4). Thus, a study conducted at the doctor's office may only reflect the reality of a skewed population of sicker children or parents who are able or prone to consult rather than the epidemiological reality of the community (1,3,4,8). Studies have shown that the prevalence of FGIDs varies with the diagnostic criteria been used. Adult studies comparing the prevalence of irritable bowel syndrome (IBS) using different diagnostic criteria have reported a 2- to 5-fold variation depending on the criteria applied (9,10). Studies in children have also shown significant differences in prevalence when the Rome II or Rome III criteria are applied (11). Moreover, most pediatric studies have not even used the Rome criteria employing older terminology such as recurrent abdominal pain (RAP), an old terminology that includes functional and organic conditions. These and other methodological flaws encountered in studies assessing the prevalence of AP and FGIDs in children may explain the wide variation in prevalence found among different pediatric studies (12). To date, no published studies has investigated the prevalence of chronic AP and AP-related FGIDs at the community level using up-to-date criteria and validated questionnaires in the United States. We conducted a study to assess parental reports of AP symptoms in a population of healthy community children from the Chicago metropolitan area.
Between January 2009 and March 2011, our group conducted 5 studies using identical protocols to establish the long-term risk of developing chronic AP and AP-related FGIDs in children who were previously affected by diseases involving the GI tract. Cases were children who had a previous history of cow's-milk allergy (CMA) (13), pyloric stenosis (PS) (14), Henoch-Schönlein purpura (HSP) (15), celiac disease (CD), and stem cell transplant (SC) (unpublished data), several months to years before the survey. Children in the control groups for each of these studies were unaffected siblings. In brief, 3 of the 5 studies found significant differences between cases and controls and were published as peer-reviewed articles, whereas 1 of them (negative) is being revised and a study on siblings of children with stem cell continues enrollment. In the present study, we analyzed the combined data of all the siblings that served as healthy controls in the 5 studies, a diverse sample of children of various backgrounds that was thought to provide a fair representation of the community.
The protocol followed by each of the studies included contacting families by telephone and inviting them to answer a GI symptoms telephone questionnaire and the parent report version of the Questionnaire on Pediatric Gastrointestinal Symptoms Rome III (QPGS-RIII) (5). The QPGSRIII is a validated age-appropriate instrument commonly used to facilitate the diagnosis of FGIDs in children and adolescents (11). Fair to moderate agreement in Rome criteria diagnosis of FGIDs between children's and parents’ reports of symptoms was found using the QPGS (16). Rome III criteria established a minimum time criterion of 2 months to characterize an AP case as an AP-related FGID and specific criteria for each category of AP-related FGID (IBS, functional abdominal pain [FAP], dyspepsia, and abdominal migraine). For the purpose of the present study, we considered children meeting the Rome III time criterion of AP (AP lasting >2 months) but not meeting the rest of criteria for a specific AP-related FGID as having chronic AP, whereas those meeting all of the criteria were classified as AP-related FGIDs. The presence of AP was assessed by the following question: “Has your child complained of AP in the past 2 months? (yes/no).” Parents who reported the presence of AP were asked to complete the QPGS-RIII, which includes questions addressing the frequency, intensity, location, and duration of AP symptoms. The duration of AP was assessed by the following question: “For how long has your child had AP? (≤1 month, 2 months, 3 months, 4–11 months, or ≥1 year).”
Inclusion criteria were healthy children 4 to 18 years of age and the presence of a sibling who was previously diagnosed as having CD, CMA, PS, HSP, or SC. Exclusion criteria were a history of CD, CMA, PS, HSP, or SC; nonverbal children; non–English speaking. As additional inclusion criteria, and only in the case of the CD study, controls were required to have either normal TTG IgA and IgA determination or a normal EGD. Demographic data obtained included sex, age, and race/ethnicity. The values are reported as mean ± standard deviation (SD). Fisher exact test statistics were calculated to determine associations between demographic factors and AP/AP-related FGIDs. Descriptive statistics were calculated using Statistical Package for the Social Sciences version 11.5 for Windows (SPSS Inc, Chicago, IL). All of the studies were approved by the institutional review board of Children's Memorial Hospital.
Two hundred forty-six of 984 families (25%) accepted to participate and were included in the studies: CMA (53), HSP (38), PS (91), CD (31), and SC (33) (Fig. 1). Five hundred sixty-two families could not be reached because of incorrect telephone numbers or change of address, did not meet the criteria (56), refused to participate (23), or had an incorrect diagnosis (97). Cumulative demographic characteristics of the control population of the four studies are shown in Table 1. The mean age of the children was 9.8 ± 4.44 years (112 girls, 46%). Eighty-six percent of the participants were white, 3.2% were black, 6.5% were Asian, and 3.8% could not be identified. Thirty-two percent were Hispanic (white and nonwhite). Two hundred twenty-six children had no complaints of AP (91.9%). Parents reported the presence of AP in 20 (8.1%) children (age range 4–18 years, 11 girls). All of the children who reported AP had at least 2 months of symptoms (2 patients had pain for 2 months, 6 patients reported pain for 3 months, 4 patients reported pain for 4 to 11 months, and 8 patients reported having pain for ≥1 year). AP data (frequency, location, intensity, and disability) are shown in Table 2. Most children (50%) reported AP above the navel. Eleven children (55%) had pain 1 to 3 times per month, whereas the rest of the children reported a higher frequency of AP. AP was severe enough to impair daily activities in 8 (40%) children. Six children (2.4%) met the QPGS-RIII diagnostic criteria for AP-related FGIDs: 3 for FAP and 3 for IBS. The rest of the patients who reported AP were not classifiable by Rome III criteria as having AP-related FGIDs due to unmet criteria for pain frequency (1–3 times per month vs at least 4 times per month). We found no significant sex (P = 0.11), race (P = 0.75), or ethnicity (P = 0.60) effect in the prevalence of AP or AP-related FGIDs.
The present study is the first to assess the prevalence of FGIDs in a sample of community children using parental report and validated Rome III criteria questionnaires in the United States. Descriptive epidemiologic studies are important because they offer key data about the rate of a disease in a population or its subgroups. The sample of our study included children of a wide age range, race, and ethnicity. Similarly to the epidemiology of American children (17), white non-Hispanic and Hispanic/Latino children were the 2 predominant groups in our sample. We found a prevalence of AP-related FGIDs of 2.4% and AP of 8.1%. The prevalence of AP-related FGIDs found in our study is consistent with most of the data obtained in previous studies using different diagnostic criteria. Studies on RAP showed a prevalence ranging from 0.3% to 19% (12,18,19). A school-based study using a loose definition of the Rome II criteria found “IBS-like symptoms” in 8% of middle school students (1). The prevalence of AP found in our study is lower than figures reported in other studies using children's report of symptoms (1,2,20). A school-based study surveyed children from 2 schools in Chicago weekly for the presence of GI symptoms throughout the school year. Twenty-four percent of schoolchildren reported persistent AP lasting >8 weeks. Fifteen percent of schoolchildren in the study answered that they reported their AP episodes to teachers, friends, or family members other than their parents. The study did not survey whether children always report each episode of AP. Our study interviewed parents to investigate their child's symptoms. The lower prevalence of AP in our study may be inherent to parental report of child's data.
Lower figures of AP by parental report than child's report may be explained by underreporting of AP by the child to the parents. Children who are asked to report their symptoms may report symptoms that the parents ignore. Lack of parental awareness of their child's symptoms may constitute one of the factors explaining the low ratio of consultation in children reporting AP found in other studies (4,8). This is an important aspect that may affect health care because families may not seek medical attention unless symptoms are severe enough to affect the child's quality of life. Alternatively, a lower frequency of AP by parental report may result from parental limitation of recall or selective attention bias with parents paying more attention to the abdominal complaints of a “sicker child,” the one with a history of a “serious” disease or a GI disease that required medical attention rather than the “healthy sibling.” However, the opposite argument can also be made, because mothers who had a sick child with a condition involving the GI tract would be more vigilant about any GI symptoms in the siblings. Moreover, the inclusion of a “negative” study (celiac study) strengthens our results. A negative study makes the possibility of our data being solely explained by selective attention bias less likely as similar findings should have been obtained in all of the studies in particular in children with CD, a chronic condition that requires lifelong dietary modification. Because most studies use parental report of symptoms as a surrogate for child's complaints, the possibility of obtaining lower reports of symptoms by parental report than child's report should be considered in future studies.
Most children who reported chronic AP in our study failed to meet Rome III criteria for an AP-related FGID. Our findings are consistent with previous observations using the Rome II criteria showing that almost half of the children complaining of AP did not meet criteria for an AP-related FGID (21,22). FAP was the most common diagnosis in our sample. Studies that have investigated the relative frequency of the different AP-related FGIDs defined by the Rome II criteria have found a wide range of results (16,21,22). A clinic-based study found that FAP was the most common AP-associated FGID (23), whereas a community-based study using the same Rome II criteria found that IBS-type symptoms (1) were the most common complains.
Similar to the findings of community-based studies, we did not find an association among sex, race, or ethnicity and the prevalence of AP or AP-related FGIDs (1). Previous studies have found that female predominance of symptoms is present in adolescents as opposed to younger children, and the mean age of our sample was 9.9 years.
Our study is not devoid of limitations. A limited sample size, using parental questionnaires as a method of assessment, and the use of a nonrandomly selected population constitute some of the study's drawbacks. Parental involvement in the report of the child's symptoms is difficult to overcome in young children. In children older than 10 years of age, it can be argued that parental report of symptoms measures the parental perspective of the problem because older children may not share with the parents all of their complaints; however, the parent and child agreement has been shown to be fair to moderate in previous studies (16). The selection of a sample of siblings of children who had a disease that required medical attention may not fairly represent the epidemiological reality of all of the community children; however, there is no indication in the literature that siblings of children with cow's-milk protein allergy, PS, HSP, or SC who did not have the disease have a higher risk of AP or FGIDs. Siblings of children diagnosed with CD are at higher risk of developing CD (24), but the absence of CD in the siblings of the index cases was guaranteed by maternal report, review of history, and presence of a negative serological or endoscopic study on at least one occasion in all of the children. There is evidence that some FGIDs, including IBS, aggregate strongly in families (25); however, most of the patients who met criteria for AP-related FGIDs did not have siblings who met criteria. Finally, the selection of the QPGS-RIII as a diagnostic tool requires parents to accurately recall 2 months of symptoms. A design based on long-term recall of symptoms may lead to inaccurate estimates.
In summary, AP is common in community children. FAP and IBS were the most common FGIDs among healthy community children. Future prospective studies should confirm our findings and investigate the factors influencing parental report of symptoms including parental awareness of children's symptoms and what drives the decision of medical consultation in children with AP.
1. Hyams JS, Burke G, Davis PM, et al. Abdominal pain and irritable bowel syndrome in adolescents: a community-based study. J Pediatr
2. Ramchandani PG, Hotopf M, Sandhu B, et al. The epidemiology of recurrent abdominal pain from 2 to 6 years of age: results of a large population-based study. Pediatrics
3. Saps M, Sztainberg M, Di Lorenzo C. A prospective community-based study of gastroenterological symptoms in school-age children. J Pediatr Gastroenterol Nutr
4. Saps M, Seshadri R, Sztainberg M, et al. A prospective school-based study of abdominal pain and other common somatic complaints in children. J Pediatr
5. Rasquin A, Di Lorenzo C, Forbes D, et al. Childhood functional gastrointestinal disorders: child/adolescent. Gastroenterology
6. Drossman DA. Introduction. The Rome Foundation and Rome III. Neurogastroenterol Motil
7. Youssef NN, Atienza K, Langseder AL, et al. Chronic abdominal pain and depressive symptoms: analysis of the national longitudinal study of adolescent health. Clin Gastroenterol Hepatol
8. Starfield B, Hoekelman RA, McCormick M, et al. Who provides health care to children and adolescents in the United States? Pediatrics
9. Saito YA, Locke GR, Talley NJ, et al. A comparison of the Rome and Manning criteria for case identification in epidemiological investigations of irritable bowel syndrome. Am J Gastroenterol
10. Saito YA, Talley NJ, L. JM, et al. The effect of new diagnostic criteria for irritable bowel syndrome on community prevalence estimates. Neurogastroenterol Motil
11. Baber KF, Anderson J, Puzanovova M, et al. Rome II versus Rome III classification of functional gastrointestinal disorders in pediatric chronic abdominal pain. J Pediatr Gastroenterol Nutr
12. Chitkara DK, Rawat DJ, Talley NJ. The epidemiology of childhood recurrent abdominal pain in western countries: a systematic review. Am J Gastroenterol
13. Saps M, Lu P, Bonilla S. Cow's-milk allergy is a risk factor for the development of FGIDs in children. J Pediatr Gastroenterol Nutr
14. Bonilla S, Saps M. Early life events: infants with pyloric stenosis have a higher risk of developing chronic abdominal pain in childhood. J Pediatr
15. Saps M, Dhroove G, Chogle A. Henoch-Schönlein purpura leads to functional gastrointestinal disorders. Dig Dis Sci
16. Schurman JV, Friesen CA, Danda CE, et al. Diagnosing functional abdominal pain with the Rome II criteria: parent, child, and clinician agreement. J Pediatr Gastroenterol Nutr
18. Apley J, Naish N. Recurrent abdominal pains: a field survey of 1,000 school children. Arch Dis Child
19. Bode G, Brenner H, Adler G, et al. Recurrent abdominal pain in children: evidence from a population-based study that social and familial factors play a major role but not Helicobacter pylor
i infection. J Psychosom Res
20. Perquin CW, Hunfeld JA, Hazebroek-Kampschreur AA, et al. The natural course of chronic benign pain in childhood and adolescence: a two-year population-based follow-up study. Eur J Pain
21. Walker LS, Lipani TA, Greene JW, et al. Recurrent abdominal pain: symptom subtypes based on the Rome II criteria for pediatric functional gastrointestinal disorders. J Pediatr Gastroenterol Nutr
22. Caplan A, Walker L, Rasquin A. Validation of the pediatric Rome II criteria for functional gastrointestinal disorders using the questionnaire on pediatric gastrointestinal symptoms. J Pediatr Gastroenterol Nutr
23. Teitelbaum JE, Sinha P, Micale M, et al. Obesity is related to multiple functional abdominal diseases. J Pediatr
24. Bardella MT, Elli L, Velio P, et al. Silent celiac disease is frequent in the siblings of newly diagnosed celiac patients. Digestion
25. Saito YA, Petersen GM, Larson JJ, et al. Familial aggregation of irritable bowel syndrome: a family case-control study. Am J Gastroenterol