Abdominal pain is a common complaint in childhood (1–4). The term recurrent abdominal pain (RAP) has been used when the pain episodes repeat over time. In the 1970s, Apley (4) defined RAP as intermittent abdominal pain in children between the ages of 4 and 16 years that persists for >3 months and affects normal activity. Surveys suggest that 10% to 17% of children in this age group meet the criteria for RAP and that RAP accounts for at least 5% of all pediatric office visits (3,5,6). The definition of RAP was revised by Von Baeyer and Walker (7) to define better the relationship of the pain with time. A pediatric working group defined the Rome II criteria for functional bowel diseases in children (8). They subdivided abdominal pain into symptom-based groupings that included functional abdominal pain (FAP) and irritable bowel syndrome (IBS) and dispensed with the term RAP. The definition of functional abdominal pain is, however, similar to that of RAP (8). IBS can be thought of as FAP that is associated with changes in stool frequency, appearance, and/or abdominal pain relieved with stooling (8). RAP can be thought of as a symptom complex, whereas FAP and IBS are diagnoses (8).
To the best of our knowledge, there have been no longitudinal studies describing the frequency and severity with which children with RAP have pain or how often the pain interferes with activity. Similarly, we know little about the stooling pattern of children with RAP or how the pattern compares with children without abdominal pain. In addition, few data describe what proportion of children presenting with the symptoms of RAP meet the definition of FAP or IBS. Furthermore, the few data that are available were obtained only from children referred to tertiary care.
The objective of the present study was to collect longitudinal data from children with RAP in regard to pain frequency and severity, how often the pain interferes with activities, and stooling pattern (ie, what proportion of patients have FAP vs IBS). As a point of reference, we compared these data to those of control children (ie, those without a complaint of abdominal pain).
PATIENTS AND METHODS
Participants were 7 to 10 years of age and recruited from a large pediatric health care network that includes primary (pediatric) and tertiary (ie, pediatric gastroenterologist) care serving the Houston metropolitan area that accepts both public and private insurance. Participants also were recruited from 2 private pediatric gastroenterology practices, so the vast majority of gastroenterology referrals in the city were identifiable.
Children with RAP were identified using the criteria of Apley (4) as modified by von Baeyer and Walker (7) and Rasquin-Weber (8): (1) the pain occurs at least once each month, in at least 3 consecutive months, and within the last year and (2) episodes have been severe enough to cause the child to stay at home, terminate or avoid play, take medication for pain or rate the pain as moderate or severe (≥3 of 10 on a scale of pain intensity) (4,7). This definition is consistent with the term FAP proposed by the Second Pediatric Rome Working Group on Functional Gastrointestinal Diseases (8). Children were excluded if they had organic gastrointestinal illness or other significant chronic health conditions requiring daily medication (eg, diabetes) and/or specialty care follow-up (eg, congenital heart disease). Mild chronic illnesses such as asthma were not excluded. Other exclusion criteria included an abnormal physical examination, decreased growth velocity, gastrointestinal blood loss, unexplained fever, vomiting, chronic severe diarrhea, weight loss ≥5% of their body weight within a 3-month period, current use of anti-inflammatory (eg, ibuprofen) or gastrointestinal (eg, proton pump inhibitors, antacids, H2 receptor blockers, laxatives, motility agents) medications, and previous use of gastrointestinal medications that provided some symptomatic relief. (The last criterion was used to exclude children with partially treated conditions such as gastroesophageal reflux disease or constipation.)
The exact temporal relationships between pain and stool changes that constitute the definition of IBS remain to be defined. El-Matary et al. (9) have used the definition of onset of pain associated with change in stool frequency (bowel movements >3/d or <3/week). We used the definition of El-Matary et al. but also used a definition that we thought better fit the pediatric Rome II criteria for IBS: a pain episode with a change in stool character that day or the day after (8,9). Children without any chronic pain complaints (including RAP) were designated controls.
All of the recruitment and study procedures were approved by the Baylor College of Medicine Institutional Review Board, and informed consent was obtained. Children 7 to 10 years of age with abdominal pain initially were identified via billing codes for abdominal pain or IBS at primary care pediatrician and pediatric gastroenterology offices. Medical charts then were screened for inclusion and exclusion criteria. Control subjects were recruited from the same primary care pediatrician offices by reviewing billing codes for well child visits. Control subject's charts were reviewed to ensure that the children had no pain complaints of any kind in the past 3 months. Furthermore, it was required that they had no chronic or recurrent episodes of abdominal pain.
Parents were screened further by phone. For the RAP children, this screening was done to establish frequency, duration, and intensity of the child's pain complaints and to ensure that symptoms were current and of sufficient severity for enrollment. For the control children, this screening was done to ensure that they had no gastrointestinal complaints or other excluding characteristics. If the child met eligibility, then a home visit was scheduled in which the parent and child were trained to fill out the diary.
During the home visit, the research coordinators provided the child and parent with standardized training and written instructions in the use of the diaries. The research coordinators maintained weekly contact with the subject and parents to help ensure that the diaries were completed. A coupon for a video rental was provided if at least 90% of the diary was completed.
Pain and Interference Diary
Ratings were made 3 times per day (awakening, after lunch, and evening) during the 2-week period. The child rated the pain using a visual analogue scale in which he or she drew a line across a 10-cm horizontal line anchored with the phrases “no pain at all” and “worst pain you can imagine.” The pain intensity score was established by measuring the distance from the left end of the line in millimeters. The visual analogue scale has been used widely and found to be valid and reliable in measuring children's pain, including RAP pain (10–12). The visual analogue scale is easy to administer and has not been found to have the problems with unequal intervals and response biases reported for the popular faces pain scales (13,14). At each time point, the child also rated interference with activity. This measure was rated on a four-point scale (no interference, a little interference, much interference, and unable to participate in activity) (15,16).
At the home visit, the research coordinators helped the child use the diary to rate standard painful situations involving the leg (eg, basketball bounces into knee, falls and scrapes knee, breaks leg) and to make pain and interference ratings based on those events. This was done to ascertain whether the child understood the diary rating system and could fill out the diary without parents' help. However, it was acceptable and encouraged that parents remind the child to complete the diary. To avoid taking the diary to school and to make the after-lunch rating, the child was encouraged to remember that rating and mark it in the diary immediately after school.
Stooling pattern was tracked daily over the 2-week period. The child identified whether the stool was watery, mushy, formed, or hard balls or if there was no stool passed based on pictures provided in the diary. The diary has been validated previously (17). The research coordinators also instructed the child and parent in the use of this diary and provided written instructions. Parents were asked to assist the child with the stooling diary (to ensure that the record was kept and assist with comparison to the pictures on the stooling diary).
Statistical analyses were conducted with SAS version 9.0 (SAS Institute Inc, Cary, NC). We used t tests to compare results between groups. Three measures of pain were compared across groups. First, each child's mean level of severity of pain episodes across the 42 time points (3 times per day for 14 d) was computed. The second outcome was the maximum level of pain recorded during the 2-week period. Third, the number of pain episodes reported was used as an outcome. A pain episode was defined as a mark >20 mm on the visual analogue scale. t tests were computed to compare mean level of pain severity, maximum pain level, and the frequency of pain episodes between children with RAP and controls. The folded-f test was used to determine whether the 2 samples had equal variances. If the variances were unequal, then the Satterthwaite test correction was used.
Multilevel random-effect models were used to investigate the relationship between pain, stooling pattern, and group membership. This analytical method takes into account the nesting of data within a person over time. PROC MIXED in SAS was used to construct linear multilevel random-effect analyses that took into account time within children and controlled for autocorrelation or dependency between time points and pain. Multilevel models offer a number of advantages, including the ability to examine within-person factors, such as stool pattern or changes in pain and disability, and methods for handling missing data, which is common in daily diary studies. Data are expressed as mean ± SD.
One hundred eighteen participants were recruited. Of the 118 subjects, 2 did not return the diary at all and 6 others did not record any pain ratings in their diary, resulting in a final sample of 110 children. A complete description of the sample is included in Table 1. Of the 77 children in the RAP group, 40 were recruited through their primary care physician (pediatrician), and 37 were recruited through their pediatric gastroenterologist (17 through the academic gastrointestinal service, 20 through the private practice gastrointestinal service). The mean age of the children was 8.6 ± 1.1 years; 70% were girls. The age and racial distributions did not differ between groups. There were no significant differences between groups in socioeconomic status as measured by the mother's level of education.
First, we examined pain frequency, pain interference with activity, and stooling pattern from the daily diary by calculating descriptive characteristics across the 14-day period. Second, we examined the possible relationships between the presence of RAP on pain and stool patterns. Third, we analyzed daily associations between pain, interference with activities and stool pattern using multilevel random-effects models to examine the same-day within-subject relationships between pain frequency, pain interference with activity and stool pattern.
Despite having been screened at the time of recruitment, control children reported episodes of abdominal pain. However, there were significantly more pain episodes in the RAP group compared with controls (Table 2; t(1, 108) = −4.2, P < 0.01). In addition, the RAP group reported a significantly greater number of pain episodes at lunch compared with controls (Table 2; χ2 = 23.1, df = 12, P < 0.05). For all groups, the location of the pain was most commonly the periumbilical area. RAP and control children often noted pain in >1 location (Table 2). There was no correlation between pain timing, severity and location.
The RAP group reported significantly higher mean levels of pain severity overall (Table 2; t(1, 108) = −3.5, P < 0.01). In addition, the RAP group reported a significantly higher maximum level of pain compared with controls (Table 2; t(1, 108) = −3.42, P < 0.01). Multilevel random-effects models indicated that on a day-to-day basis, children who were diagnosed with RAP reported significantly higher levels of pain compared with control children (Table 4; β = 4.75, t = 4.97, P < 0.001).
Pain Interference with Activity
A χ2 test was conducted to evaluate whether there were differences between groups on how much the pain interfered with activities. Table 2 shows the percentage of time that pain interfered with activities rated on a 4-point scale. The χ2 tests demonstrated that the pain interfered with activities significantly more often and at a higher level of intensity in the RAP group compared with the control group (P < 0.001).
Multilevel random-effect models indicated that there was a positive relationship between pain and interference; an increase in pain was related to increased interference with activity (Table 4; β = 0.021, t = 29.54, P < 0.001). In addition, there was a significant interaction between group and pain, indicating that the RAP group was more likely to report higher levels of interference across all levels of pain (Table 4; β = 0.038, t = 4.74, P < 0.01).
There were no differences between groups in the number of stools passed per child during the 2-week period [Table 3; t(1, 108) = −0.07, P = NS]. There was no difference between groups on the type of stools (mushy, hard balls or watery) or the number of days without a bowel movement (Table 3). When the definition of El-Matary et al. (9) was used (bowel movements >3/d or <3/week), 32 of 77 RAP children had IBS and 27 of 77 had FAP. Using our own criteria of having a pain episode with a change in stool character that day or the day after indicated that 50 of 77 children had IBS and 27 of 77 had FAP.
Multilevel random-effect models were conducted to examine the relationship between stool pattern and pain on a day-to-day basis (Table 4). These models indicated that there was a significant relationship between stool types in predicting pain, indicating that only mushy stool was significantly associated with increased pain (β = 5.5, t = 3.12, P < 0.01). Further examination of the relationship between stool type and pain revealed that there was a significant interaction between group and mushy stool in its relationship to pain (β = 3.65, t = 2.67, P < 0.01). This interaction is such that the RAP group reported significantly higher levels of pain when their stool was mushy compared with the control group.
To the best of our knowledge, our study is the first to compare longitudinally the pain symptoms and bowel habits of children with RAP and to compare these with normal children. Unlike previous studies of RAP, ours was not focused only on children referred to tertiary care. We also were able to examine the potential relationship between episodes of pain and interference with the child's activities.
Control children without a history of abdominal pain on the 3 screening steps recorded episodes of pain in their 2-week diary. However, the RAP group experienced more pain episodes that had a mean severity and maximum intensity that were greater than that of controls (Table 2).
Although it has been suggested that the pain in RAP occurs more commonly in the morning, perhaps as part of an aversion to going to school, our data suggest that the pain is experienced evenly throughout the day from morning to evening (Table 2) (8,18). Previous studies have noted that the pain in RAP is periumbilical (4,19). Although our data support this contention, it is important to note that in more than half of the patients, the pain was located in other areas of the abdomen and/or in more than 1 location (Table 2). In addition, there was no relationship between the location or severity of pain and the time of day that pain occurred.
Abdominal pain interferes with activities more commonly in children with RAP compared with controls (Table 2). However, there was no difference between groups in the level of interference. Even 15% of control children had abdominal pain severe enough at some time that it caused interference or prevented participation in activities (Table 2). To the best of our knowledge, these findings have not been reported previously. However, they fit with the observation of Malaty et al. (20) that pain disability is an important dimension in the development of a multidimensional measure for RAP.
The results of the stool diaries from the controls point out that normal children experience day-to-day variation in stooling pattern (Table 3). Day-to-day variation in stool frequency and consistency may depend on the child's diet (21–23). For the most part, children with RAP and controls described their stools similarly (Table 3). Approximately 15% of each group had stools that were watery or mushy. Both groups had a similar number of stools passed per day, and the number of days with no stools passed also was similar between groups (Table 3). There was no relationship between the occurrence of pain and the passage of hard stool. On the contrary, there was a significant relationship between the severity of pain and mushy stools. This could not be attributed to an intercurrent illness because none of the parents reported that their children were ill during the 2-week period. Studies in adults demonstrate that individuals with IBS commonly move from 1 functional category to another (eg, IBS with diarrhea to FAP to IBS with constipation), although over time the IBS diagnosis is durable (24). Our data suggest that children may follow a similar course.
Presumably stools that were reported as watery, mushy or hard intimate that the child could meet the criteria for IBS (8). Walker et al. (25) asked parents and children 4 to 17 years of age with RAP (n = 107) who were awaiting a visit to a pediatric gastroenterologist to complete a symptom questionnaire. Based on the responses, 45% and 7.5% of the children met the pediatric Rome II criteria for IBS and FAP, respectively (25). However, in the definition of IBS that this group used in its retrospective study, there is no reference to timing other than that the pain was associated with a change in stool character (25).
El-Matary et al. (9) studied 103 children (10 ± 3.4 years of age, mean ± SD) referred to a pediatric gastroenterologist who fulfilled Apley's (9) criteria for abdominal pain. Of the children with nonorganic pain, 36% met the pediatric Rome II criteria for IBS, whereas 30% had FAP (9,25). Using the El-Matary et al. definition (bowel movements >3/d or <3/week), we found that 42% of the children in our sample had symptoms compatible with IBS, whereas 35% had FAP (9). Differences between the results of our study and those of Walker et al. (25) and El-Matary et al. (9) may be explained by differences in the ages of the children and that the categorization in our study was based on the 2-week diary instead of a single episode of recall, and their studies examined only children referred to tertiary care. Using our own definition of IBS (pain episode with a change in stool character that day or the day after) indicated that 65% of children in our sample had IBS and 35% had FAP.
Some qualifications should be kept in mind in when our results are extrapolated. We studied children between 7 and 10 years of age. Whether the results apply to younger or older children needs to be established. Although detailed instructions were given to the parents and children and constant contact was maintained throughout the study period, it is possible that not all of the data were filled in each day but recorded in ≥2-day blocks. However, despite this potential limitation, the results should be more reliable than those based solely on long-term recall.
In summary, our data show that normal children experience abdominal pain that sometimes interferes with activity and that their bowel pattern often varies. These data demonstrate the overlap in symptoms such as pain (severity, timing, location) and stool changes between children with and without RAP. The difference between RAP and control children appears to be in the degree of symptoms rather than the symptoms themselves. Indirectly these results support the importance of inquiring about the presence of other symptoms (so-called alarm symptoms [eg, weight loss, extraintestinal manifestations, fever]) in identifying children with organic disease as opposed to RAP (26,27). The relationship between the experience of pain and the presence of mushy stools is intriguing and requires further study.
The authors thank Noelle Underhill, Lauren Curtis, and Drs Margie Tripp and Mariella Lane for assistance with the home visits; Raheela Khan for technical assistance; and Dr M. Heitkemper for her helpful comments.
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