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Journal of Pediatric Gastroenterology and Nutrition 41:216220 August 2005 Lippincott Williams & Wilkins, Philadelphia

Are There Psychosocial Differences in Diagnostic Subgroups of Children with Recurrent Abdominal Pain?
*Paul M. Robins, Joseph J. Glutting, Stephen Shaffer, Roy Proujansky, and Devendra Mehta
*Department of Psychology, The Childrens Hospital of Philadelphia, Philadelphia, Pennsylvania; University of Delaware, Newark, Delaware; and the Division of Gastroenterology, The Alfred I. duPont Hospital for Children, Wilmington, Delaware

ABSTRACT Objectives: To examine psychosocial differences in diagnostic subgroups of children with recurrent abdominal pain (RAP). Methods: Children meeting Apleys 1975 denition of RAP were divided according to physician ratings into three subgroups, based on the Rome II diagnostic criteria of functional gastrointestinal disorders: functional dyspepsia (n = 17), irritable bowel syndrome (n = 18), and functional abdominal pain (n = 27). Groups were compared using measures of (a) child psychopathology, (b) parent psychopathology, and (c) child pain, somatization, and functional disability. Results: Multivariate results from a discriminant function analysis demonstrated that children classied according to these criteria could not be differentiated with respect to parent reported child psychopathology or child pain, somatization, and

functional disability. There were signicant univariate differences, however, between groups on parental psychopathology (F = 4.39, P = 0.02); parents of children with functional dyspepsia reported greater parental psychopathology symptoms than the other two groups. Conclusions: This study provides a preliminary comparison of pain, somatization, functional impact, and psychopathology ratings in the Rome II diagnostic subclassications of children with RAP. Further investigation utilizing larger sample sizes, pain measures specifying pain location, and parental modeling of somatic behavior is indicated to better understand potential similarities and differences between these subgroups. JPGN 41:216220, 2005. Key Words: Recurrent abdominal pain ChildrenAdolescentsClassication. 2005 Lippincott Williams & Wilkins

INTRODUCTION Recurrent abdominal pain (RAP) is a common problem affecting 10 to 15% of school-age children (1). Dayto-day functioning is affected in numerous ways, including school attendance (23), academic productivity (45), and participation in physical activities (6). Ongoing health-related difculties associated with RAP are often reported. As many as 30 to 60% of children with RAP have chronic pain (7), which sometimes persists into adolescence and adulthood (8). It is likely that there is a progression from childhood RAP to adult gastrointestinal disorders such as irritable bowel syndrome (9). Although there is a substantial literature related to the characteristics of RAP and its treatment by medical or cognitive behavioral approaches (1011), there is a signicant heterogeneity with respect to sample characteristics (1213). Such heterogeneity has made it difcult to develop a consensus on the diagnosis and treatment (14).

Received July 22, 2004; accepted May 4, 2005. Address correspondence and reprint requests to Paul M. Robins, PhD, Department of Psychology, The Childrens Hospital of Philadelphia, 3405 Civic Center Blvd., Philadelphia, PA 19104.

There are a number of reasons why heterogeneity has persisted. Recurrent abdominal pain is not a single diagnostic entity but, rather, is a descriptive term for a common pattern of symptoms with no agreed upon etiology (14). Mild symptoms are often present in healthy children, and more severe symptoms reect an extreme variation of the normal (13). Although there is no agreed upon denition of RAP, Apleys 1975 denition is most often used in research studies. Apley described RAP as pain that waxes and wanes with three or more episodes over a three-month period or longer severe enough to affect activities. There are a number of problems related to this broad denition of RAP. The denition does not clearly describe the temporal distribution of pain episodes (e.g., widely spaced versus frequent), confounds pain severity with impairment, and leaves open the issue of including or excluding cases in which the abdominal pain is thought to be based on organic disease documented visually or microscopically (14). The need to develop a classication system for differentiating subgroups of RAP is well recognized (15). To this end, a method of dening and standardizing functional gastrointestinal disorders in pediatrics was published in 1999 by the Committee on Childhood Functional Gastrointestinal Disorders, Multinational Working Teams 216

RAP SUBGROUPS to Develop Criteria for Functional Disorders (Rome II) (16). The nal Rome II system is a symptom-based classication scheme arrived at by consensus among committee members. Five subgroups of functional abdominal pain were classied: functional dyspepsia, irritable bowel syndrome, functional abdominal pain, abdominal migraine, and aerophagia. Figure 1 presents detailed descriptions of the three most commonly occurring subgroups. To date there are no published studies examining psychosocial similarities and differences in the subgroups identied by the Rome II classication system for childhood RAP. The purpose of this study was to compare psychosocial variables in patients with three of the most common subgroups of RAP in an initial attempt to better understand these subgroup classications. Better understanding of subgroup characteristics is essential to advance treatment studies, educate health practitioners about which children require mental health services, and determine whether specic interventions should target specic RAP subgroups (14). METHOD Samples
This study was part of a larger randomized clinical trial investigating the effectiveness of medical and cognitivebehavioral treatment of children with RAP (17). The sample was drawn from patients consecutively presenting to a group of four pediatric gastroenterologists through the outpatient service of a private, non-prot childrens hospital, as well as children referred into the study from community pediatricians. A two-stage classication was used. First, each child initially met Apleys (1) criteria for nonspecic RAP, based on physician impression from the history and physical examination. Once the

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child was admitted to the study, a second classication was undertaken. The patients pediatrician or pediatric gastroenterologist or their clinical nurse practitioner completed a checklist for each child. The Rome II (16) criteria for functional dyspepsia, irritable bowel syndrome and functional abdominal pain were listed (Fig. 1). Abdominal migraine and aerophagia were not included due to the extremely low frequency of these sub classications in our clinical practice. Physicians were asked: Which of the following categories best describes your patient? Please choose only one. There was also a category labeled Other. Please briey explain. This two-stage classication resulted in four subclassications: a) abdominal pain associated with functional dyspepsia (n = 17), b) abdominal pain associated with irritable bowel syndrome (n = 18), c) functional abdominal pain without criteria for other functional gastrointestinal disorders to explain the pain (n = 27), and d) other (n = 6). Other included cases in which no stage two classication was offered, two subclassications were simultaneously endorsed, or one case later found to have an organic etiology. These six cases were not included in subsequent analyses. Tertiary care pediatric gastroenterologists referred 45% of the total sample, while primary care physicians referred 55% of the sample. Patients were largely preadolescents with mean age 11.2 6 2.35 (SD) years. The age range was six to 16 years. There were more females (57%) than males overall and in each of the subgroups (functional dyspepsia = 56% female, irritable bowel syndrome = 53% female, and functional abdominal pain = 60% female). The majority of children were Caucasian (79%). There were two African-American and 12 children whose parents did not answer or endorsed other when asked to specify their childs ethnic group or race. The mean Hollingshead parental education level was at least one year of college (mean 5.22 6 1.15) while the mean Hollingshead occupational level was manager/minor professional (mean 6.8 6 2.0). There were no signicant differences between groups with respect to age (t = 20.89, df = 84, P = 0.38), gender (x2 = 0.02, df = 1, P = 0.89),

FIG. 1. Rome II Diagnostic CriteriaPhysician Completed Checklist

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by correlations with school absence and somatic symptoms. A total score was obtained by summing the ratings with higher scores representing greater functional impact. Abdominal Pain Index (API; child and parent versions). The API asks the child or parent to rate various aspects of the childs abdominal pain in the past two weeks (22). Six dimensions are included: 1) how often the pain occurs (not at all to every day), 2) how many times a day the pain usually occurs (none to constant during the day), 3) how long the pain lasts (a few minutes to all day), 4) severity of pain (11-point Likert-type scale with verbal anchors of 0 no pain to 10 the most pain possible), 5) the worst pain experienced (11-point Likert-type scale), and 6) present severity of pain (11-point Likert-type scale). Items one through three were converted to a Likerttype scale using the same number of response options per item as in the questionnaire. Higher scores represent greater reported pain. Alpha reliabilities for the API were reported to range from .80 to .93 across samples, and evidence of criterion validity was established through correlations with another pain inventory. Symptom Checklist-90-R (SCL-90-R). The SCL-90-R is a 90item self-report symptom inventory completed by the parent (23). Each item is rated on a ve-point scale of distress ranging from not at all to extremely. The Global Severity Index (GSI) of the SCL-90-R was used as a summary measure of parental psychopathology. The test authors state that the GSI is the single best indicator of psychopathology on the SCL-90-R (23). Raw scores were computed according to the manual; higher scores represent greater psychopathology.

parent education (x2 = 2.14, df = 2, P = 0.34), and parent occupation (x2 = 1.19, df = 2, P = 0.55). Therefore the three groups were deemed essentially equivalent on these background characteristics. The participants were medically healthy with the exception of pain complaints. The duration of pain complains was greater than three months by denition, and typically ranged from nine to twelve months. The most signicant impact of the pain was school absence. Over a one-year period, we found that children receiving medical care for RAP were absent an average of 14.5 days (17). Informed consent and assent documents were completed by parents and children in a manner consistent with guidelines outlined by the hospitals Institutional Review Board. Children and their mothers completed paper and pencil measures (described below) following admission to the study, either immediately following their hospital outpatient clinic visit or on receiving the questionnaires through the mail. In two cases, fathers completed the measures.

Measures
We examined psychosocial differences in diagnostic subclassications of children with abdominal pain. Since this was a pilot study without a strong theoretical model, we felt it was important to use a broad spectrum of psychosocial measures relevant to childhood recurrent pain. We therefore used measures assessing child and parent psychopathology, multidimensional child and parent reports of child abdominal pain, child and parent reports of child somatization, and the impact of pain on daily activities. Child Behavior Checklist (CBCL). The CBCL is a 118-item behavior rating scale in which parents describe the childs behavior problems during the previous six months (18). The measure is widely used clinically and its psychometric properties have been thoroughly described. The two broadband Internalizing Behavior Problems and Externalizing Behavior Problems factor scales were used in this study. Child Somatization Inventory (CSI; parent and child versions). The CSI includes symptoms derived from other somatization measures (1920). There are 36 psychophysiological symptoms, each rated on a ve-point scale ranging from not at all (0) to a whole lot (4). Parents and children rate how much the child was bothered by the symptoms over the past two weeks. Symptoms include headache, pain in the heart, hot or cold spells, nausea, and difculty swallowing. Validation studies of the CSI, using both pediatric and community samples, suggest that scores obtained are moderately stable (test-retest reliability). Studies of the CSI have demonstrated good concurrent and construct validity (1819). A total score, obtained by summing the ratings, was used with higher scores representing greater somatization. Functional Disability Inventory (FDI; child version). This instrument lists 15 activities concerning school, home, recreation, and social interaction (21). The child rates how difcult it was for him or her to perform each activity in the past few days along a ve-point severity scale, ranging from no trouble to impossible. Sample activities include walking to the bathroom, being at school all day, reading or doing homework, and running the length of a football eld. Walker and Greene (21) reported acceptable internal consistency and test-retest reliability coefcients. Validity of the instrument was investigated

RESULTS Two a priori power analyses were completed for the study. For each power analysis, data were the interval level of measurement, and analyses were completed using multiple discriminant function analyses (MDFAs). Both power analyses were directed to be sensitive to any univariate comparison such as analyses of variance (ANOVAs) of individual dependent variables following the MDFAs. Likewise, the criterion for signicance (alpha) was set at 0.05 for both power analyses. For the rst power analysis, a large effect size was anticipated (f = 0.40, as per Cohen) (24). Results indicated that with 64 participants, power was equal to 0.84, meaning there was an 84% probability of detecting large differences between groups if the differences exist in the population. For the second power analysis, a medium effect size was anticipated (f = 0.25, as per Cohen) (24). Results indicated that with 64 participants, power was equal to 0.43, meaning there was a 43% probability of detecting medium differences between groups if the differences exist in the population. Thus, the current study was sensitive to large effect sizes (group differences) but insensitive to either medium or small effect sizes. Once the three RAP subgroups were identied, utilizing the two-step classication strategy described above, it was possible to examine the extent to which they differed in terms of scores on the psychosocial variables. An objective of the study was to predict group membership from the set of psychosocial predictors. Consequently, data

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RAP SUBGROUPS were analyzed using two three-group discriminant function analyses for multivariate data, and one-way ANOVA for the univariate parental psychopathology measure. Distributional statistics for the a) child psychopathology (CBCL), b) adult psychopathology (SCL-90-R), and c) child pain (API), child somatization (CSI), and child functional disability (FDI) measures are presented for each group in Table 1. Examination of the mean t-scores on the CBCL Internalizing Problems scale suggests that all three groups demonstrated mildly elevated scale scores, at the 84th percentile, consistent with mild anxiety, depression, and withdrawal symptoms. Mean scores across groups on the Externalizing Problems scale on the other hand are at or below average. These ndings are consistent with previous studies indicating that children with RAP exhibit higher rates of internalizing problems and lower rates of externalizing problems (22). Examination of mean scores across groups on the SCL-90-R Global Symptoms Inventory indicates parental psychopathology symptoms within +1 SD of published norms for nonpsychiatric patients (23). The mean raw scores on the API-Parent and the APIChild in all three diagnostic subgroups suggest moderate levels of abdominal pain reported (possible range 250). The mean CSI-Child and CSI-Parent raw scores suggest only mild somatic symptoms other than abdominal pain (possible range 0140). Finally, examination of the mean raw scores on the child reported FDI suggests minimal functional impairment (possible range 1575) despite more pronounced pain symptoms. Discriminant function analyses reveal that child psychopathology and pain, somatization, and functional disability measures were not different among the classication subgroups (child psychopathology Wilks l = 0.992, x2 = 0.48, df [2, 59], P = 0.98; pain, somatization, and functional disability Wilks l = 0.747, x2 = 13.40, df [2, 48], P = 0.202). Because there were no signicant discriminant functions revealed, it was not possible to

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interpret functions at group centroids, or interpret classication results. There were, however, signicant differences between the three groups with respect to scores on the SCL-90R GSI (F = 4.39, P = 0.017). Parents of children classied with functional dyspepsia self-reported more overall psychopathology symptoms than parents of children classied with irritable bowel syndrome or functional abdominal pain (SCL-90-R GSI means = 0.59, 0.41, and 0.28, respectively). Despite statistically significant group differences, however, none of the group means was within the clinically signicant range, as all three group mean scores were within 6 1 SD of norms published in the SCL-9-R manual (23). DISCUSSION The purpose of the study was to examine psychosocial differences between subgroups of children with RAP utilizing the Rome II criteria. The results suggest that select psychosocial variables did not distinguish between the subgroups. The only exception was parental psychopathology. Parents of children with functional dyspepsia self-reported higher levels of psychopathology than parents of children with irritable bowel syndrome or functional abdominal pain. Parental modeling of sick behavior may be associated with inadvertent reinforcement of child illness behavior (25). Nonetheless, this single difference between groups is not particularly strong or convincing in the context of the multiple comparisons performed. Power analyses before the study showed that our sample size would be sensitive to large group differences (i.e., effect sizes) but not to medium or small differences. The lack of statistically signicant differences in the current study indicates that no large group differences were present for the variables of child internalizing or externalizing symptoms, child and parent reported abdominal pain, child and parent reported somatization, and child reported functional disability. At the same time,

TABLE 1. CBCL, SCL-90-R, abdominal pain, somatization, and functional disability scores from the dyspepsia, irritable bowel, and functional abdominal pain groups
Group DYSF* M CBCL internalizing problems CBCL externalizing problems SCL-90-R GSI API-parent API-child CSI-child CSI-parent FDI 60.35 46.76 0.59 24.0 17.36 17.43 16.14 22.64 SD 15.34 12.34 0.46 8.26 11.19 12.14 10.65 6.32 M 60.72 49.17 0.41 28.82 24.27 18.82 18.55 23.73 IBS SD 10.00 9.77 0.26 13.50 8.50 12.77 10.95 6.07 M 60.18 47.93 0.28 27.5 26.81 18.88 14.77 24.50 FAP SD 9.31 12.48 0.29 8.05 9.39 12.84 8.17 7.65 Univariate P 0.012 0.184 4.39 0.927 4.31 0.07 0.61 0.32 F 0.99 0.83 0.02 0.41 0.02 0.94 0.55 0.73

DYSP, functional dyspepsia; IBS, irritable bowel syndrome; FAP, functional abdominal pain; CBCL, child behavior checklist; SCL-90-R GSI, global severity index; API, abdominal pain inventory; CSI, child somatization inventory; FDI, functional disability inventory. *n = 17; n = 18; n = 27.

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8. Walker LS, Garber J, Van Slyke DA, Greene JW. Long-term health outcomes in patients with recurrent abdominal pain. J Pediatric Psychology 1995;20:23345. 9. Walker LS. Pathways between recurrent abdominal pain and adult functional gastrointestinal disorders. J Development and Behavioral Pediatrics 1999;20:320322. 10. Sanders MR, Rebgetz M, Morrison M, et al. Cognitive-behavioral treatment of recurrent nonspecic abdominal pain in children: An analysis of generalization, maintenance, and side effects. J Consulting and Clinical Psychology 1989;57:294300. 11. Sanders MR, Shepherd RW, Cleghorn G, Woolford H. The treatment of recurrent abdominal pain in children: A controlled comparison of cognitive-behavioral family intervention and standard pediatric care. J Consulting and Clinical Psychology 1994;62: 30614. 12. Robins PM, Smith SM, Proujansky R. Children with recurrent abdominal pain: Comparison of community and tertiary care samples. Childrens Health Care 2002;31:93106. 13. Walker LS. The evolution of research on recurrent abdominal pain: History, assumptions, and a conceptual model. In McGrath PJ, Finley GA, eds. Chronic and Recurrent Pain in Children and Adolescents. Seattle: International Association for the Study of Pain; 1999. 14. von Baeyer CL, Walker LS. Children with recurrent abdominal pain: Issues in the selection and description of research participants. J Developmental & Behavioral Pediatrics 1999;20:30713. 15. Janicke DM, Finney JW. Empirically supported treatments in pediatric psychology: Recurrent abdominal pain. J Pediatric Psychology 1999;24:11527. 16. Rasquin-Weber A, Hyman PE, Cucchiara S, et al. Childhood functional gastrointestinal disorders. Gut 1999;45(suppl 2):6068. 17. Robins PM, Smith SM, Glutting JJ, Bishop CT. A randomized controlled trial of a cognitive-behavioral family intervention for pediatric recurrent abdominal pain. J Pediatric Psychology In press. 18. Achenbach TM, Edelbrock C. Manual for the Child Behavior Checklist and Revised Child Prole. Burlington: University of Vermont, Department of Psychiatry; 1983. 19. Garber J, Walker LS, Zeman J. Somatization symptoms in a community sample of children and adolescents: Further validation of the Childrens Somatization Inventory. Psychological Assessment 1991;3:58895. 20. Walker LS, Garber J. Childrens Somatization Inventory: Preliminary manual [unpublished manuscript]. Vanderbilt University Medical Center, Nashville, TN, 1991. 21. Walker LS, Greene JW. The Functional Disability Inventory: Measuring a neglected dimension of child health status. J Pediatric Psychology 1991;132:10105. 22. Walker LS, Greene JW. Children with recurrent abdominal pain and their parents: More somatic complaints, anxiety, and depression than other patient families? J Pediatric Psychology 1989;4:23143. 23. Derogatis LR. Symptom Checklist-90-R. Administration, scoring, and procedures manual. Minneapolis: Natural Computer Systems, Inc.; 1994. 24. Cohen J. Statistical Power Analysis for the Behavioral Sciences. 2nd ed. Hillsdale: Lawrence Erlbaum Associates, Inc.; 1988. 25. Walker LS, Zeman JL. Parental response to child illness behavior. J Pediatric Psychology 1992;17:4971. 26. Van Slyke DA, Guite JW, Stutts JT, Walker LS, Greene JW, Barnard JA. Psychological and biologic correlates of recurrent abdominal pain [poster session]. Poster presented at: 7th Florida Conference on Child Health Psychol; Gainesville, FL. 27. Walker LS, Garber J, Greene JW. Somatization symptoms in pediatric abdominal pain patients: Relation to chronicity of abdominal pain and parent somatization. J Abnormal Child Psychology 1991; 19:37994.

it is important to note that the study was insensitive to medium or small differences (i.e., effect sizes) that might be present between groups. Therefore, the current investigation must be considered preliminary until other studies are completed with larger samples of children with RAP. The reliability and validity of the Rome II classication system has not yet been empirically assessed, and it is not yet in general clinical use. These preliminary results suggest that there may be important psychosocial similarities in subgroups of children with abdominal pain classied by the Rome II criteria. It is also possible that while there may be reliable differences between groups based on biomedical assessment, biomedical factors are not strongly related to pain, somatization, or functional disability reports (26). Assessing the pain beliefs and coping mechanisms characteristic of subgroups might be more revealing. Thus, while use of the Rome II criteria may enhance the reliability of RAP subgroup classication along biomedical parameters, it is not yet clear whether such sub classication is justied along psychosocial parameters. Further research paths are claried by the present study. Initial evaluation of the interrater reliability of the sub classications is necessary. In addition, while the pain measure used in this study did not specify pain location, Rome II criteria delineate pain location as one distinguishing factor among subgroups. It, thus, appears important to assess pain location in future subgroup research. In addition, the role of parental psychopathology and modeling of somatic behavior is a potentially fruitful area for further investigation (25,27). To this end, it is important to assess parents responses to childrens pain complaints to better understand modeling effects.
Acknowledgments: This study was supported in part by a grant through the Nemours Research Programs awarded to the rst author.

REFERENCES
1. Apley J. The child with abdominal pain. Oxford: Blackwell; 1975. 2. Heath CP. School phobia: Etiology, evaluation, and treatment. Paper presented at: Annual Meeting of the National Association of School Psychologists; April 1985; Las Vegas, NV. 3. Wasserman AL, Whitington PF, Rivara FP. Psychogenic basis for abdominal pain in children and adolescents. J American Academy of Child and Adolescent Psychiatry 1988;27:17984. 4. Kolbe LL, Collins J, Cortese P. Building the capacity of schools to improve the health of the nation. Am Psychol 1997;52:256265. 5. Kusche CA, Cook ET, Greenberg M. Neuropsychologic and cognitive functioning in children with anxiety, externalizing, and comorbid psychopathology. J Clinical Child Psychology 1993;22: 17293. 6. Walker LS, Greene JS. Development and validation of a measure of functional disability for children and adolescents. Paper presented at: Florida Conference on Child Health Psychol; April 1988; Gainesville, FL. 7. Apley J, Hale B. Children with recurrent abdominal pain: How do they grow up? British Medical Journal 1973;3:79.

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