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ORIGINAL ARTICLE: GASTROENTEROLOGY

Maintenance of Pain in Children With Functional


Abdominal Pain
yz
Danita I. Czyzewski, yzMariella M. Self, Amy E. Williams, zjjErica M. Weidler,

Allison M. Blatz, and zjjRobert J. Shulman

ABSTRACT

Objectives: A significant proportion of children with functional abdominal What Is Known


pain develop chronic pain. Identifying clinical characteristics predicting
pain persistence is important in targeting interventions. We examined  In approximately one-third of patients, functional
whether child anxiety and/or pain-stooling relations were related to main- abdominal pain becomes chronic.
tenance of abdominal pain frequency and compared the predictive value of 3  Concurrent anxiety predicts pain intensity and dis-
methods for assessing pain-stooling relations (ie, diary, parent report, child ability, but it is unclear if anxiety relates to chronicity.
report).  Whether the presence of pain-stooling relations pre-
Methods: Seventy-six children (710 years old at baseline) who presented dicts chronicity is unknown.
for medical treatment of functional abdominal pain were followed up 18 to
24 months later. Baseline anxiety and abdominal pain-stooling relations What Is New
based on pain and stooling diaries and child- and parent questionnaires were
examined in relationship to the persistence of abdominal pain frequency.  In school-age children with functional abdominal
Results: Childrens baseline anxiety was not related to persistence of pain pain, anxiety did not predict pain chronicity.
frequency. Children who, however, displayed irritable bowel syndrome  Pain-stooling relations identified by parent question-
(IBS) symptoms at baseline maintained pain frequency at follow-up, naire and pain and stooling diaries predicted pain
whereas in children in whom there was no relationship between pain and chronicity.
stooling, pain frequency decreased. Pain and stool diaries and parent report  Child-report of pain-stooling relations, however,
of pain-stooling relations were predictive of pain persistence but child-report failed to predict pain chronicity.
questionnaires were not.

Received December 29, 2014; accepted August 14, 2015. Conclusions: The presence of IBS symptoms in school-age children with
From the Department of Pediatrics, the yMenninger Department of Psy- functional abdominal pain appears to predict persistence of abdominal pain
chiatry and Behavioral Sciences, Baylor College of Medicine, the zTexas over time, whereas anxiety does not. Prospective pain and stooling diaries
Childrens Hospital, Houston, Texas, the Indiana University School of and parent report of IBS symptoms were predictors of pain maintenance, but
Medicine & Riley Child and Adolescent Psychiatry Clinic, Indianapolis, child report of symptoms was not.
the jjChildrens Nutrition Research Center, Houston, Texas, and the
George Washington School of Medicine and Health Sciences, Key Words: abdominal pain, anxiety, children, chronic pain, irritable
Washington, DC. bowel syndrome
Address correspondence and reprint requests to Danita I. Czyzewski, PhD,
Texas Childrens Hospital, 6701 Fannin St, CC1740.01, Houston, TX
77030-2399 (e-mail: danitac@bcm.edu).
(JPGN 2016;62: 393398)
Supplemental digital content is available for this article. Direct URL
citations appear in the printed text, and links to the digital files are
provided in the HTML text of this article on the journals Web site
(www.jpgn.org).
This study was supported in part by R01 NR05337 and R01 NR013497 from
H aving been described as recurrent, functional, or medically
unexplained, abdominal pain without evidence of a patho-
logic condition is a common presenting problem in primary and
the National Institutes of Health, the Daffys Foundation, the USDA/ tertiary pediatric care. A summary of follow-up studies reveals that
ARS under Cooperative Agreement No. 6250-51000-043, and P30 5 years after first contact, approximately 30% of children with
DK56338, which funds the Texas Medical Center Digestive Disease abdominal pain who have no alarm signs will continue to complain
Center. of abdominal pain (1). This, coupled with the knowledge of the high
This work is a publication of the USDA/ARS Childrens Nutrition Research health care costs (2) and lower quality of life in children (3,4) and
Center, Department of Pediatrics, Baylor College of Medicine and Texas adults with functional gastrointestinal disorders, suggests that
Childrens Hospital. The content is solely the responsibility of the identifying children at risk for a prolonged course of pain is
authors and does not necessarily represent the official views of the a worthy challenge (5).
National Institutes of Health, does not necessarily reflect the views or For many reasons, anxiety is often conceptualized in com-
policies of the USDA, nor does mention of trade names, commercial
products, or organizations imply endorsement by the US Government.
munity and clinical settings as causative of functional abdominal
The authors report no conflicts of interest. pain. The ubiquity of this assumption may stem from the common
Copyright # 2016 by European Society for Pediatric Gastroenterology, human experience of abdominal sensations in the presence of
Hepatology, and Nutrition and North American Society for Pediatric anxiety or the idea that symptoms without identifiable organic
Gastroenterology, Hepatology, and Nutrition cause are psychologically based. Data exist linking anxiety to
DOI: 10.1097/MPG.0000000000000947 increased pain severity (5,6) and disability (59) in children with

JPGN  Volume 62, Number 3, March 2016 393


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Czyzewski et al JPGN  Volume 62, Number 3, March 2016

functional abdominal pain. Data showing a relationship between questionnaire based on pediatric Rome II criteria for IBS (19) and
anxiety and longer-term pain is, however, scant to nonexistent (1,6). the Behavior Assessment System for Children (20), as a measure of
This may be to the result of a relative dearth of follow-up studies (1) or childrens emotional and behavioral problems. To avoid problems
may reflect a true lack of relation. Despite lack of research support, with reading comprehension, questionnaires were read to the
the proportion of pediatric gastroenterologists endorsing the concep- children by a research assistant.
tualization of psychological factors as a basis of functional abdominal Participants were instructed in completion of a 2-week pain
pain has remained steady during the past 20 years (10). Thus, a test of and stooling diary. Parents were asked to prompt children to
the connection between anxiety and long-term pain is warranted. complete diaries but allow the child to independently rate abdomi-
Growing evidence suggests pediatric functional abdominal nal pain and record stool occurrence and form (21). Children rated
pain is a precursor to adult irritable bowel syndrome (IBS) (1113). abdominal pain for 3 intervals per day (morning, afternoon, and
Historically pediatric literature has, however, focused on abdominal evening) by placing a mark on a 100-mm visual analog scale (VAS)
pain without attention to other GI symptoms (ie, pain-stool anchored by no pain at all and worst pain you can imagine.
relations, the defining characteristic of IBS). Therefore, it is not Pain intensity was established by measuring the distance from the
clear whether functional abdominal pain in general or pediatric IBS left end of the line to the mark (10 mm defined as a pain episode).
symptoms specifically predicts adult IBS. Although the 2005 Children also recorded time and form (watery, mushy, formed, or
American Academy of Pediatrics guidelines did not address pain hard) of each stool. The diary included pictorial representations of
stool-relations in their summary of findings and treatment guide- stools (analogous to the Bristol Stool Form Scale) (22) as a guide.
lines for functional abdominal pain (6), the Rome Foundation Participants were called 18 to 24 months later for follow-up. At that
on Functional Gastrointestinal Disorders has focused increased time, the initial screening interview was again administered over the
attention to the symptoms of IBS in children (14). Examining telephone to the same parent; all but 1 respondent was the mother.
pain-stooling relations within children with functional abdominal
pain may help illuminate whether early pain-stooling relations Measures
(ie, IBS symptoms) predict chronicity of pain.
The aims of the present study were to examine within a group Abdominal Pain Frequency-Parent Interview
of school-age children with functional abdominal pain whether Question
baseline anxiety symptoms and/or the presence of pain-stooling At recruitment phone screening and follow-up assessment,
relations (defining characteristic of IBS) predicted maintenance of parents who endorsed that their child had abdominal pain in the past
abdominal pain complaints 18 to 24 months later. In approaching 3 months were asked how many times per month the child
these aims, we also examined the impact of methods used to obtain experienced pain.
symptom data (eg, diary vs questionnaire; parent vs child report).
The Behavior Assessment System for Children
METHODS
The Behavior Assessment System for Children (BASC) is a
Participants well-validated measure of child emotion and behavior problems (20)
Participants 7 to 10 years of age who had been recruited from a designed and normed for 3 age ranges (25, 611, and 1218 years)
large academically affiliated health care network including both with versions for parent-report of child behaviors and self-report for
primary and tertiary care, for a descriptive study of physiological ages 8 and above. t Scores (mean 50, standard deviation 10) for
and psychological characteristics of prepubescent children with parent- and child-report anxiety scales were used. In accordance with
functional abdominal pain (15,16). Parents of children who had been clinically meaningful interpretation, children were dichotomized on
seen in primary or tertiary care within the previous year for abdominal their anxiety score with t scores of 60 and above classified as at-risk/
pain were contacted by mail. Interested participants were screened by clinically significant for anxiety.
phone to identify children who presently have pain episodes at least
monthly that interfere with activity (17), and are rated as moderate or
severe (3/10 on a scale of pain intensity), or cause children to take Pain-Stooling Relations From Child Diary
medication for pain (18). Children were excluded if phone screening
or chart review indicated they had organic GI illness (or organic GI Diaries were scored as described previously (23) to identify
illness remained in the differential as an explanation for childs pain), symptoms of IBS, specifically temporal relations between defecation
a significant chronic health condition (requiring daily medication or and abdominal pain relief, pain associated with changes in stooling
specialty care), decreased growth velocity, GI blood loss, unexplained frequency, and pain associated with changes in stool form. Changes in
fever, vomiting, chronic severe diarrhea, weight loss of 5% of their stool form and frequency were operationalized using the North
body weight within a 3-month period, present use of anti-inflamma- American Society for Pediatric Gastroenterology, Hepatology and
tory medications, or previous use of GI medication that provided Nutrition guidelines (24). Briefly, 3 or more stools per day or no stools
complete symptom relief. Additional exclusion criteria included for 2 or more stools per day were not normative in terms of frequency.
language or learning challenges preventing questionnaire or diary Stools rated as hard balls or watery were not normative in terms of
completion. Except for conditions that could be related to alarm signs form. Using the stool diary, stool occurrence or change in stool form
(such as severe diarrhea) or alternative explanations for pain, such as or frequency was identified and then compared with the pain diary to
chronic constipation, stooling patterns were not part of the initial determine whether pain occurred in conjunction with the stool
selection criteria. characteristic. Pain-stooling relations were considered present if at
least 2 of the 3 pain-stooling relations existed at any point during the
course of the 14-day diary period (23).
Procedures
The institutional review board of the Baylor College of Pain-Stooling Relations From Questionnaires
Medicine approved the study. Consent was obtained from parents
and assent from children. During a home visit, parents and The parent- and child-report questionnaires comprised yes/
children independently completed a child pain-stooling relations no questions about the relation of abdominal pain to stooling or

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JPGN  Volume 62, Number 3, March 2016 Maintenance of Pain in Children With Functional Abdominal Pain

changes in stool form or frequency (eg, Is your childs stomach hi/diary symptoms diary yes) were in the average range with t scores
discomfort or pain relieved by a bowel movement?, When you of 53 or below (Table 1).
have stomach pain do you poop more often than usual?) (supple-
mental questionnaire, http://links.lww.com/MPG/A546). If the Baseline Anxiety Predicting Pain Frequency at
respondent endorsed any 2 of the 3, pain-stooling relations were
considered present.
Follow-Up
Child-Report BASC Anxiety
Analysis Based upon the clinically meaningful cutoff t score of 60,
59 children (78%) were in the normal anxiety group and 14 (22%)
To evaluate differential change over time for groups were in the elevated anxiety group (Fig. 1). The main effect of Time
dichotomized by anxiety level (assessed by child or parent report) was significant for pain frequency [F(1,71) 20.65, P < 0.001,
or presence of IBS symptoms (assessed by parent questionnaire, h2 0.23] with a decrease in monthly pain frequency from initial
child questionnaire or symptom diary), five 2  2 mixed design assessment (mean 11.53, SE 1.56) to follow-up (mean 5.16, SE
analyses of variance examined group by time interactions. Group 1.09). The Time  Child BASC Anxiety interaction was not
was the between-subjects independent variable with 2 levels significant [F(1,71) 1.41, P 0.24, h2 0.02].
(anxiety elevated/normal or pain-stooling relations present/not
present), and time was the within-subjects independent variable Parent-Report BASC Anxiety
with 2 levels (initial vs follow-up). The dependent variable for all
analyses of variance was parent report of childs abdominal pain Using parent-report BASC anxiety t scores, 57 children
frequency per month. Missing diary data or questionnaires (75%) were in the normal anxiety group and 14 (25%) were in
resulted in sample sizes for the final analyses ranging from the elevated anxiety group (Fig. 1). The main effect of Time was
55 to 73. again significant for pain frequency [F(1,69) 10.12, P < 0.01,
h2 0.13] with a decrease in pain frequency from initial assessment
RESULTS (mean 11.53, SE 1.56) to follow-up (mean 5.16, SE 1.09). The
Of the initial 118 participants, 1 child was removed from the Time  Parent BASC Anxiety interaction was again not significant
sample after being diagnosed with eosinophilic colitis; and 64% [F(1,69) 0.56, P 0.45, h2 0.01].
(76 participants) completed the follow-up. Fifty-four (71%) of the
follow-up participants were girls. Mean age at follow-up was Baseline Pain-Stooling Relations Predicting
10.8  1.8 years. Follow-up participants were 70% white, 18% Pain Frequency at Follow-up
Hispanic, 11% African American, and 1% Asian.
For the follow-up group, parent interview at baseline Diary-Scored Pain-Stooling Relations
indicated mean pain intensity for abdominal pain episodes was By diary scoring 11 (17%) children had 2 or more pain stool
6.8 (on a 10 point scale) and for 79% of the children, pain relations and 54 (83%) did not (Fig. 2). The main effect of Time was
interfered with school attendance or play. Those lost to follow-up significant for pain frequency [F(1,63) 6.06, P 0.02, h2 0.09],
did not significantly differ from follow-up participants for with a decrease in pain frequency from initial assessment (mean
baseline age, sex, ethnicity, baseline pain intensity or interference 8.96, SE 1.80) to follow-up (mean 5.39, SE 1.09). This effect was
with activity. Follow-up completers reported significantly more qualified by a significant Time  Diary-based pain-stooling
frequent pain episodes per month at baseline than noncom- relations interaction [F(1,63) 5.90, P 0.02, h2 0.09]. Children
pleters (10.3  10.4 vs 5.4  5.3, respectively, t (1, 111) 2.688, who did not have evidence of 2 pain-stooling relations (ie, no IBS
P 0.001). symptoms) at baseline had a significant decrease in pain frequency
Mean anxiety scores (as measured by child report and parent (P < 0.001, d 0.78) from initial evaluation (mean 11.05, SE 1.48)
report) between IBS/no IBS groups (as measured by diary, parent to follow-up (mean 3.95, SE 0.90). Children with pain-stooling
questionnaire, children questionnaire) were compared. No signifi- relations did not have a significant change in (ie, maintained) pain
cant differences were found in any of the 6 comparisons. Further- frequency (P 0.99, d 0.01) from initial evaluation (mean 6.86,
more, the means for each of 12 subgroups (eg, parent rated anxiety SE 3.29) to follow-up (mean 6.82, SE 1.98).

TABLE 1. Initial BASC Anxiety Scores for IBS and non-IBS groups designated by 3 methods

Initial BASC ANX t score Initial BASC ANX t score

n DIARY IBS n DIARY not IBS P value of t test

Child BASC 9 44.0 54 50.1 0.101


Parent BASC 11 53.0 50 51.2 0.616

PARENT Q IBS PARENT Q not IBS

Child BASC 13 48.2 41 50.3 0.204


Parent BASC 14 51.6 41 52.7 0.673

CHILD Q IBS CHILD Q not IBS

Child BASC 23 47.6 34 51.1 0.506


Parent BASC 19 50.9 34 52.2 0.726

BASC Behavior Assessment System for Children; IBS irritable bowel syndrome.

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Czyzewski et al JPGN  Volume 62, Number 3, March 2016

A Child-report anxiety A Diary


30 16
Pain frequency (per month)

Pain frequency (per month)


14
25
12
20 10
8 Not IBS
15 Low anxiety
6 IBS
High anxiety
10 4
2
5
0
Baseline Follow-Up
0
Baseline Follow-Up

B Parent-report anxiety B Child questionnaire


16

Pain frequency (per month)


18
Pain frequency (per month)

16 14
14 12
12 10
8 Not IBS
10
Low anxiety
8 6 IBS
High anxiety
6 4

4 2

2 0
Baseline Follow-Up
0
Baseline Follow-Up

FIGURE 1. Pain frequency at baseline and follow-up based on child C Parent questionnaire
and parent report of child anxiety at baseline.
Pain frequency (per month)

16
14
12
Child-Report Questionnaire of Pain-Stooling 10
Relations 8 Not IBS
6 IBS
By child-report questionnaire, 23 children had 2 or 4
more pain-stool relations and 34 children did not (Fig. 2). The
2
main effect of Time was significant for pain frequency
0
[F(1,55) 21.30, P < 0.001, h2 0.28] with a decrease in pain
Baseline Follow-Up
frequency from initial testing (mean 10.60, SE 1.55) to follow-up
(mean 4.73, SE 0.95). The Time  Child Questionnaire of Pain- FIGURE 2. Pain frequency at baseline and follow-up based on irritable
stooling relations interaction was not significant [F(1,55) 1.68, bowel syndrome (IBS) symptoms at baseline determined by prospec-
P 0.20, h2 0.03]. tive diary, child questionnaire, and parent questionnaire.

Parent-Report Questionnaire of Pain-Stooling DISCUSSION


Relations In this cohort of children who presented for medical care for
functional abdominal pain, we examined 2 factors, child anxiety
By parent-report questionnaire, 14 children had 2 or more level and presence/absence of pain-stooling relations, to determine
pain-stool relations and 42 children did not (Fig. 2). The main effect whether either accounted for the persistence of pain 18 to 24 months
of Time was significant for pain frequency [F(1,54) 10.43, later. Although anxiety is commonly considered related to abdomi-
P 0.002, h2 0.6], again with a decrease in pain frequency from nal pain in children, our results are consistent with research failing
initial assessment (mean 10.60, SE 1.77) to follow-up (mean 5.96, to show a relation between anxiety and abdominal pain chronicity
SE 1.05). The Time  Parent Questionnaire of Pain-stooling (6,7). In contrast, children with pain-stooling relations (ie, IBS
relations interaction approached significance [F(1,54) 3.84, symptoms), as opposed to those without IBS symptoms, were more
P 0.055, h2 0.07]. Because the interaction approached signifi- likely to have persistence of abdominal pain at follow-up.
cance and had a medium effect size, exploratory analyses were Previous research suggests concurrent anxiety is related to
conducted. Children whose parents did not report that they had increased pain severity and disability (59) in children with func-
2 pain-stooling relations (ie, not IBS) had a significant decrease in tional abdominal pain and that the presence of functional abdominal
pain frequency (P < 0.001, d 0.80) from initial assessment (mean pain at an early age predicts vulnerability to later anxiety disorders
11.33, SE 1.77) to follow-up (mean 3.89, SE 1.05), whereas those (25). Only 1 identified study, however, found anxiety to be a
with parent reported pain-stooling relations maintained similar pain significant predictor of longer-term pain in children. In a 5-year
frequency (P 0.47, d 0.18) from initial assessment (mean 9.86, follow-up of children and adolescents with functional abdominal
SE 3.07) to follow-up (mean 8.04, SE 1.82). pain, Mulvaney et al (26) reported that higher anxiety at baseline

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JPGN  Volume 62, Number 3, March 2016 Maintenance of Pain in Children With Functional Abdominal Pain

was associated with greater pain symptoms at the time of second likely to participate in the follow-up, potentially reducing the
contact. In contrast to the young children in our study, participants generalizability of these results. Also, the sample size did not allow
in the Mulvaney et al study were 6 to 18 years old with a mean age at examining both anxiety and IBS symptoms in the same analyses to
baseline of 12 years. Further research is needed to better understand explore the potential interactions of these variables. Pain diaries
these discrepant results, but it may be that for older children and rather than parent recall to assess the frequency of childrens pain
adolescents, anxiety is related to longer-term pain, whereas for may improve the validity of the outcome variable, although in this
younger children this factor may be less salient. study parent recall and diary of pain-stooling relations yielded
In contrast to anxiety, our data suggest that GI symptoms similar results.
related to IBS (ie, pain-stooling relations) are associated with In summary, our study suggests that in preadolescent chil-
maintenance of pain (Fig. 2). A recent Dutch study reported a dren with functional abdominal pain, the presence of IBS symptoms
12-month follow-up of children 4 to 17 years of age presenting to (pain-stooling relations) predicts persistence of pain, whereas
primary care for abdominal pain (27). The authors reported that the absence of such symptoms increases the likelihood that pain will
prevalence of abdominal pain in children with IBS symptoms did remit with time. Anxiety does not appear to play a significant role in
not decrease for 12 months, whereas the prevalence decreased predicting pain persistence. If this finding is replicated, families of
significantly in children without IBS symptoms at baseline (27). the children with IBS symptoms may be more vigorously targeted
Their cohort contained children and adolescents with both organic for intervention to learn how to successfully manage chronic
and functional disorders, and the use of an unspecified stooling symptoms, minimizing disability, and preventing unnecessary
questionnaire made it somewhat unclear how the diagnosis of IBS health care seeking and its attendant problems.
was made (27,28). Although their study cohort differed somewhat
from ours, their findings support our present observation that the
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