Section of Child and Adolescent Psychiatry, University of Oxford, Oxford, United Kingdom
Department of Psychological Medicine, Institute of Psychiatry, London, United Kingdom
Bristol Royal Hospital for Children, Bristol, United Kingdom
Avon Longitudinal Study of Parents and Children, Department of Community-Based Medicine, University of Bristol, United Kingdom
ABSTRACT
Objective. Recurrent abdominal pain (RAP) is one of the most common complaints of childhood and is associated with several adverse outcomes in adulthood. Few large, population-based, longitudinal studies have been conducted. The purpose of this study was to investigate the prevalence and epidemiologic features of RAP through early childhood.
Design. We report findings from a large, population-based, cohort study of childhood (the Avon Longitudinal Study of Parents And Children). The prevalence and continuity of RAP from 2 to 6 years of age were explored, with associated physical and psychological symptoms among the children and their parents.
Results. In a population cohort of 13971 children, RAP was reported for 11.8% of 6-year-old children. It was less common at ages 2 years (3.8%) and 3 years (6.9%). There was a striking degree of continuity of RAP between the ages of 2 and 6 years. RAP was associated with headaches and limb pains among children and with higher rates of anxiety among both children (adjusted odds ratio: 2.12; 95% confidence interval: 1.70–2.65) and their mothers (odds ratio: 1.75; 95% confidence interval: 1.30–2.36).
Conclusions. In a large, population-based, cohort study, RAP was found to be increasingly common up to the age of 6 years. Children with RAP at a young age have a high risk of RAP later in childhood. RAP is associated with other somatic pain symptoms among children and with symptoms of anxiety among children and their mothers. These findings highlight the high prevalence and continuity of RAP through early childhood and the importance of considering psychological symptoms for these children and their families.
Key Words: recurrent abdominal pain children epidemiology anxiety parental health
Abbreviations: RAP, recurrent abdominal pain SDQ, Strengths and Difficulties Questionnaire CI, confidence interval OR, odds ratio ALSPAC, Avon Longitudinal Study of Parents and Children
Recurrent abdominal pain (RAP) is among the most common complaints of childhood. It occurs for 10% of children,1,2 with a peak occurrence in early childhood.1 It has been defined variously, but the most widely accepted definition is that coined by Apley,3 who defined RAP as being present when a child has "had at least three bouts of pain, severe enough to affect his(/her) activities, over a period of at least 3 months, with attacks continuing in the year preceding the examination". RAP is not usually associated with physical disease,3,4 although it is associated with increased presentation of other physical symptoms, such as headache.3 Children with anxiety or an anxious temperament are over-represented among children with RAP.1,5,6 Persistent abdominal pain is associated with adverse psychological and physical outcomes for the children when they reach adulthood, including psychiatric disorders7 and irritable bowel syndrome.8 However, there has been little research plotting the course of RAP through early childhood.
Parental ill health and parental anxiety may be crucial risk factors for the onset of RAP or may have a significant influence on the course of the disorder. Research has suggested that there may be differences in the ways in which parents respond to children with RAP when they are ill,9 leading to suggestions that reinforcement of symptoms may play a role, as well as modeling of illness behavior. Both of these effects may be more likely for parents who are anxious or have increased concern about their own health and the health of their child. Parents in this situation may have increased sensitivity to their children's symptomatic complaints. A number of studies have found an association with parental anxiety7,10 and parental ill health.7,11 Unfortunately, very few longitudinal studies have been conducted,7,12 and it is not clear whether these are causes or consequences of the child's RAP.
The present study set out to investigate the course of RAP through early childhood and to investigate whether it is associated with higher rates of anxiety among children and also among their parents. This was done with data from the Avon Longitudinal Study of Parents and Children (ALSPAC),13 a large, longitudinal, cohort study of children based in and around Bristol in the United Kingdom, the same geographic area studied by Apley and Naish1 in their original study. This study is more than just a modern replication of their 1958 report. We were able to describe the occurrence of RAP in a cohort of children monitored through early childhood for the first time. We also used validated measures of psychological functioning for parents and their children in a large population sample of 14000 children. Within the study of this cohort, we made the following specific predictions: (1) RAP would be associated with headaches and limb pains among children; (2) RAP would be associated with emotional symptoms (anxiety and depression) among children; and (3) RAP would be associated with anxiety among parents.
METHODS
Subjects
This study is based on the ALSPAC. This was a prospective, longitudinal study of children born to women resident in Avon, England, with an expected date of delivery between April 1, 1991, and December 31, 1992, and their parents. The background and detailed methods of the study were described previously.13 Approximately 85% of eligible women took part. This resulted in 13971 live-born children who survived the first year of life; these children are still being monitored.
Measurements
Timing
Questionnaires were given to mothers and their partners at different time points during the study. The times of questionnaires used in this study are given in Table 1.
Abdominal Pain
Abdominal pain was asked about in questionnaires sent to mothers when their children were 30 months, 42 months, and 81 months (6 years 9 months) of age. Two questions were asked, as follows. Have there been times when he/she seems to have had a pain in his stomach in the past 12 months (A yes/no response was required.) How many separate times has this happened in the past 12 months (Responses were once, twice, 3 or 4 times, 5 times, or don't know.)
We decided to include all children reported as having abdominal pain 5 times in the past year in the RAP group, because this was the group reported as having the most frequent abdominal pain and matched most closely the definition of 3 episodes of abdominal pain in 3 months used by Apley and Naish.1 There were no questions about the impact of the abdominal pain on the children concerned, and any definition used in this study differs from that of Apley and Naish in this regard. However, we consider the defined groups to be broadly comparable, representing children experiencing frequent abdominal pain.
Headache, Limb Pain, and Other Symptoms
Headache was asked about at all 3 ages. Limb pain was asked about only at 81 months.
Behavioral and Emotional Problems of the Child
Mothers reported on children's behavioral and emotional problems at 42 months of age with the revised Rutter Parent Scale for preschool children14 and at 81 months with the Strengths and Difficulties Questionnaire (SDQ), a widely used and validated screening questionnaire that was developed from the Rutter questionnaires.15,16 The SDQ consists of 25 questions that are divided into 5 subscales (emotional problems, hyperactivity, conduct problems, peer problems, and prosocial score). The first 4 subscale scores can be combined to give a total difficulties score. For a more clinically meaningful comparison, we analyzed the 2 groups by looking at the highest scorers on each scale, to see whether children with RAP were more or less likely to be those most comparable to a clinically disturbed group. For both scales, the top 10% of values were included, because this represents the recommended use of the SDQ. High scores on the SDQ have been shown to be predictive of psychiatric disorders among children (specificity: 94.6%; sensitivity: 63.3%).16
Parental Anxiety
This was measured with the anxiety scale from the Crown-Crisp Experiential Index, a validated self-report questionnaire.17,18 This was included in a questionnaire given to mothers and fathers at 21 months. As in previous research, the mothers and fathers scoring in the top 15% were taken as high scorers.19,20
Parental Stomach Ulcer
Mothers were asked whether they or their partners had a stomach ulcer at 5 different time points from before birth until their children were 3 years of age. The results were combined to give all those who had ever had a stomach ulcer, up to that point in time.
Socioeconomic Status
Data on maternal social class were collected, as were data on maternal educational qualifications (from minimal to degree level).
Data Analysis
The frequencies of responses to the questions about abdominal pain at different ages were examined. Abdominal pain was then analyzed as a dichotomous (binary) variable (RAP is 5 episodes of pain in the past year). Comparisons were made between children with RAP and the remaining population sample. Where data were available, results are reported for all 3 ages. For some variables (eg, maternal and paternal anxiety and stomach ulcers), data were available only up to 21 months. There comparisons were made for the group of children 30 months of age, because this was the closest age at which RAP was inquired about. Where results refer to different time points, the ages of the children at these time points are given. Relationships between RAP and other categorical variables were examined initially with 2 tests, except those relating to the continuity of RAP, where McNemar's test was used. Results are given as odds ratios (ORs) (with 95% confidence intervals [CIs]) where possible. Logistic regression analyses were then conducted to test for possible confounding effects of the child's gender and maternal educational level and social class. All analyses were conducted with SPSS for Windows, version 11.5 (SPSS, Chicago, IL).
RESULTS
Response Rates
At 30 months of age (2 years 6 months), data on abdominal pain were available for 10205 children. This represents 73.1% of the 13961 children alive at this point. At 42 months of age (3 years 6 months), information for 9845 children (70.5%) was recorded; at 81 months of age (6 years 9 months), information on abdominal pain was returned for 8272 children (59.2%). The attrition from this study was described previously (www.alspac.bris.ac.uk) and is attributable in part to loss to follow-up monitoring (1500 children). Of particular note, mothers with high rates of anxiety were more likely to have failed to respond, making it less likely that we would be able to demonstrate a relationship between RAP and maternal anxiety.19 We did not find any evidence of selective attrition bias in the group of children with RAP between 30 and 81 months of age (RAP group: 25.4% loss; non-RAP group: 24.5%; P = .67).
Prevalence of RAP
At 42 months of age, abdominal pain in the past year was reported for 39.7% of children. At 81 months of age, it was reported for 54.9% of children. The frequencies for reports of number of times are shown in Table 2. The prevalence of RAP (pain 5 times in the past year) was 3.8% (95% CI: 3.4–4.2%) at 30 months of age (2 years of age), 6.9% (95% CI: 6.4–7.4%) at 42 months of age (3 years of age), and 11.8% (95% CI: 11.1–12.5%) at 81 months of age (6 years of age).
Demographic Factors
There was a clear gender difference, with more girls experiencing RAP than boys at all ages (Table 3). RAP was also more commonly reported for children of mothers with higher educational attainment and of higher social class. A small difference in the prevalence of RAP between white and nonwhite ethnic groups was found (Table 3).
Continuity of RAP Symptoms
There was marked continuity in the presentation of RAP across the ages. A total of 35.9% (125 of 348 children) of the children with RAP at 30 months went on to have RAP at 42 months, compared with 5.7% (499 of 8687 children) of those without RAP at 30 months (OR: 9.20; 95% CI: 7.26–11.66; McNemar's test, P < .001). Of those with RAP at 42 months, 34.1% (187 of 549 children) went on to have RAP at 81 months, compared with 10.0% (716 of 7134 children) of those without RAP at 42 months (OR: 4.63; 95% CI: 3.82–5.61; McNemar's test, P < .001).
Associated Symptoms
At all 3 ages studied, children with RAP were more likely to have also experienced headaches than were those without RAP (30 months: 16.8% vs 6.3%; OR: 3.00; 95% CI: 2.26–3.99; 42 months: 27.7% vs 14.3%; OR: 2.30; 95% CI: 1.93–2.75; 81 months: 55.4% vs 37.8%; OR: 2.04; 95% CI: 1.79–2.34). A total of 25.7% of children with RAP often had limb pain, compared with 17.9% of children without RAP, at 81 months of age (OR: 1.59; 95% CI: 1.36–1.86).
Psychological Symptoms
The RAP group scored significantly higher than the non-RAP group on 3 of the subscales of the revised Rutter Scale (42 months) and the SDQ (81 months) (emotional symptoms, hyperactivity, and conduct problems) (Table 4). The strongest effect was for emotional symptoms (OR: 3.33; 95% CI: 2.84–3.91). The emotional subscale of the SDQ contains a question assessing, "often complains of headaches, stomachaches, or sickness". When this question was removed from the subscale, the relationship between RAP and high scores on the adjusted emotional subscale remained, although at a lower level (OR: 2.03; 95% CI: 1.65–2.50). When these analyses were conducted controlling for the effects of child gender, maternal social class, and maternal educational level, the strength of the associations increased.
Parental Psychological Symptoms
Mothers of children with RAP scored higher on all 3 scales of the Crown-Crisp Experiential Index (anxiety, depression, and somatic) (Table 5). These associations remained, although at a lower level, when analyses were conducted controlling for the effects of child gender, maternal social class, and maternal educational level.
No differences were seen for partner scores on the Crown-Crisp Experiential Index. These analyses were based on the relatively smaller number of fathers responding to the questionnaires (5600, depending on the question); therefore, the results should be treated with more caution.
Parental Physical Symptoms
No association was found with maternal history of stomach ulcer or paternal history of stomach ulcer and RAP at 30 months of age.
DISCUSSION
Main Findings
In this large, representative, population-based study, 978 (11.8%) of 8272 children 81 months of age were reported as having experienced RAP in the preceding year; 3.8% of children at 30 months and 6.9% at 42 months were reported as having RAP. Striking continuity of RAP symptoms for ages 2 through 6 years was demonstrated. Girls were more likely to have RAP than boys. Children with RAP were more likely to experience headaches and limb pains than were other children. They also had higher scores for a range of psychological symptoms but most notably the emotional subscale questions. They were at least twice as likely to score high for emotional symptoms at 81 months of age. Furthermore, RAP among children was associated with higher maternal scores for anxiety and depression.
Strengths and Limitations
We present data on a very large, unselected, population sample that is relatively free from selection bias, and we are able to present data for the same group of children from 2 to 6 years of age. The measures of psychological disturbance among parents and children were collected without reference to RAP status and so were, in effect, collected and coded blind with respect to this study's hypotheses. Structured, well-validated measures of children's and parents' psychological state were used.
There are 3 main limitations. First, the diagnostic criteria for RAP have been subject to some debate.21,22 The Rome criteria22 provided more clearly defined operational criteria for abdominal pain among children; but these have been little used in research. Our definition of RAP corresponds to the widely used criteria popularized by John Apley,1,23 except that we were unable to include a detailed assessment of the impact of symptoms, and it is possible that the group we describe here was affected slightly less severely than those in other studies. However, given that nearly one quarter (23.5%) of the children with RAP in this study had been taken to the doctor because of their abdominal pain, we think this is unlikely to be the case.
Second, the measures of symptoms among children were based on maternal report. Although this is usual for reports of symptoms among young children, it is possible that increased levels of maternal anxiety might be related to higher levels of concern and thus higher levels of reporting of children's abdominal pain. Therefore, the association found between maternal anxiety and RAP among children might be attributable in part to information bias, rather than a genuine association. Third, the findings on paternal symptoms should be treated with more caution than other findings, because of the lower response rate for this group.
Comparison With Other Studies
This is the first study to demonstrate the striking continuity that exists in the reporting of RAP across early childhood from 2 to 6 years of age. We also confirm the previous findings of a gender difference in the prevalence of RAP and a relationship with anxiety and headaches among children with RAP. The prevalence of RAP of 11.8% found in our study is very similar to the prevalence of 10% found in 2 other moderately large studies.1,2 Some other research found much higher (25%)24 or lower (4.6% of 4–7-year-old children)25 prevalence rates for RAP. Methodologic differences in sample selection seem likely to account for these differences.
This study has strengthened the findings on psychological symptoms among children by showing that, at 81 months of age, RAP is associated more strongly with emotional symptoms, such as anxiety and low mood, than with symptoms of hyperactivity or other behavioral problems. In addition, whereas previous research reported a link with "nervous breakdowns" among parents,1 our study showed a link with anxiety and depressive symptoms and somatic complaints among mothers, with well-validated measures. These findings persist when maternal educational level and social class and the gender of the child are controlled for.
The link between RAP and anxiety among children and their parents was not demonstrated consistently in previous population-based studies; therefore, this finding is particularly important. In the only other published, longitudinal, population-based study to examine a young age group, Hotopf et al7 found no relationship between chronic abdominal pain and anxiety (termed "neuroticism") among children, although there was a link with maternal "nerves" and neuroticism. The children in that study were born in 1946. A more-recent epidemiologic study of 9- to 16-year-old subjects from the United Stated26 found that stomachaches were related to emotional disorders among girls only. Other studies in selected populations attending clinical centers found higher rates of anxiety and emotional distress among children with RAP, compared with well children,5 and higher rates of anxiety among mothers of those children.10 However, the generalizability of these earlier findings to other populations is difficult to assess, because of the specialist medical setting for subject recruitment. A recent study of primary pediatric care patients also demonstrated a strong association between RAP and anxiety among children.6
CONCLUSIONS
This is the largest study of RAP among young children, and the link found between RAP and emotional (anxiety) symptoms among children themselves and among their mothers supports the idea that clinicians should be considering psychological factors for children presenting with RAP and also considering carefully the possible role of parental distress and illness in some of these families. The finding of strong continuity of RAP across early childhood highlights the importance of this complaint in the early years of a child's life.
ACKNOWLEDGMENTS
P.G.R. holds a special training fellowship in Health Services Research, funded by the Medical Research Council, United Kingdom. This study could not have been undertaken without the financial support of the Wellcome Trust, the Medical Research Council, the University of Bristol, the Department of Health, and the Department of the Environment. The ALSPAC is part of the World Health Organization-initiated European Longitudinal Study of Pregnancy and Childhood.
The ALSPAC study team includes interviewers, computer technicians, laboratory technicians, clerical workers, research scientists, volunteers, and managers, who continue to make the study possible.
We are extremely grateful to all of the mothers who took part and to the midwives for their cooperation and help with recruitment. We thank Kate Northstone and Professor Jean Golding, in particular, for their help and support with this work.
FOOTNOTES
Accepted Oct 14, 2004.
No conflict of interest declared.
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