INVITED REVIEW

Psychosocial Functioning and Health-related Quality of Life in Paediatric Inflammatory Bowel Disease

Sarah C. Ross, yJulie Strachan, yRichard K. Russell, and Sarah L. Wilson

ABSTRACT
Objectives: The present systematic review examined the literature focusing on psychosocial functioning and health-related quality of life (HRQOL) in young people with inammatory bowel disease (IBD). It aimed to critique the methodological quality of the identied studies, discuss the implications of their ndings, and make recommendations for future research. Patients and Methods: Relevant articles (January 1990December 2009) were subject to strict inclusion and exclusion criteria. Identied papers were rated for methodological quality using SIGN 50 and Critical Appraisal Skills Programme guidelines before data extraction. Results: Of 2141 articles initially identied, 278 were screened in detail, leaving 12 articles for inclusion in the review: 3 having acceptable and 9 having goodquality rating scores. These 12 studies yielded a combined total of 5330 participants including 790 with IBD and 4540 controls (ages 418 years). Five main outcomesself-esteem, HRQOL, anxiety and depression, social competence, and behavioural functioningwere examined. Three of the 4 controlled studies addressing self-reported HRQOL found it to be signicantly lower in the participants with IBD. The evidence for lowered self-esteem, self-reported symptoms of depression and anxiety, impaired social competence, and behavioural problems were conicting. Methodological heterogeneity was noted in terms of areas of functioning addressed, measures used, sample size, and use of control groups. Conclusions: HRQOL is lower in patients with IBD, but conicting results and methodological aws limit conclusions on other aspects of psychosocial functioning. Future research should present data on effect sizes, avoid confounding ndings by not combining across age groups or disease severity indices, and consider investigating body image disturbance. Key Words: adolescents, children, health-related quality of life, inammatory bowel disease, psychosocial functioning

nflammatory bowel disease (IBD), comprising Crohn disease (CD) and ulcerative colitis (UC), is commonly diagnosed in childhood or adolescence. Around 15% to 25% of individuals with IBD are diagnosed in childhood (1) and the incidence of paediatric IBD is reported to be increasing in Europe and North America, although reasons for this remain unknown (2). IBD is characterised by an unpredictable illness course and includes symptoms of abdominal pain, diarrhoea, nausea, fatigue, delayed puberty, and weight loss. These symptoms, in addition to treatment (including surgery, corticosteroids, and having a stoma), can be embarrassing, socially limiting, and can lead to changes in physical appearance. This may have a negative effect on body image, self-esteem, and mood (35). The social constraints of the disease, in addition to the considerable amount of school often missed because of illness and hospital appointments, may therefore have effect on social functioning (3,4). This could result in the children having fewer opportunities to develop autonomy as they grow older.

HOW DOES IBD AFFECT PSYCHOSOCIAL FUNCTIONING/HEALTH-RELATED QUALITY OF LIFE?

The burden of living with IBD, as identified in adults (6), may be even greater in the developing child. If developmental tasks and transitions are halted, then greater psychosocial difficulties and reduced health-related quality of life (HRQOL) may be expected. Difficulties in these areas have been shown to have an adverse effect on treatment adherence (7) and may predispose children to develop more severe psychological or psychiatric conditions later in life. Additionally, recent prospective studies examining the pathogenic role of psychological stress in adults with IBD have revealed that individuals with heightened anxiety and depression are at a higher risk of further disease activity (8).

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Received March 11, 2011; accepted July 17, 2011. From the Academic Unit for Mental Health and Wellbeing, School of Medicine, University of Glasgow, and the yDepartment of Paediatric Gastroenterology, Royal Hospital for Sick Children, Glasgow, UK. Address correspondence and reprint requests to Dr S.L. Wilson, Academic Unit for Mental Health and Wellbeing, University of Glasgow, Admin. Building, Gartnavel Royal Hospital, 1055 Great Western Rd, Glasgow G12 0XH, UK (e-mail: Sarah.Wilson@glasgow.ac.uk). This work was carried out in partial fullment of the requirements for the degree of DClinPsy and was funded by NHS Education Scotland. R.K.R. has received support from a Medical Research Council PICTS grant (G0800675). The IBD team at Yorkhill, Glasgow is supported by the Catherine McEwan Foundation. The authors report no conicts of interest. Copyright # 2011 by European Society for Pediatric Gastroenterology, Hepatology, and Nutrition and North American Society for Pediatric Gastroenterology, Hepatology, and Nutrition DOI: 10.1097/MPG.0b013e31822f2c32

PSYCHOSOCIAL FUNCTIONING/HRQOL AND ITS MEASUREMENT

HRQOL, including physical, psychological, and social functioning, can be defined as one means of assessing the burden of chronic illness. Studies tend to refer to either HRQOL or psychosocial functioning and typically examine the effect of IBD on areas such as behavioural, emotional, social functioning, and self-esteem. To increase the sensitivity of the search for the present review, both terms were included or were used interchangeably. Psychosocial functioning or HRQOL is typically measured using validated structured interviews (allowing for detection of psychiatric disorders) and/or validated norm-referenced questionnaires. Most questionnaires generate standardised T scores derived from the normative sample with which the measure was developed, and provide some indication as to which children may require additional mental health input. Thus, T scores are cutoffs that

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Psychosocial Functioning and Quality of Life in Paediatric IBD was conducted in addition to searching each database individually using subject headings. The results of the subject-heading search informed the final text-word search. The references of the most recent review (12) were examined to ensure no appropriate studies had been missed.

allow judgments to be made about the clinical significance of a young persons difficulties. Generic measures of HRQOL (eg, PedsQL) (9), which compare children with IBD to healthy peers and children with other conditions, have been used. Although these allow easy comparison across illness groups, they may not be specific enough to reflect impaired functioning in young people with IBD. Researchers in Canada and the Netherlands have collaboratively developed and validated IMPACT, a paediatric IBD-specific questionnaire measuring 6 domains: bowel symptoms, systemic symptoms, social/functional concerns, body image, emotional concerns, and test and treatment concerns (10,11). In addition to these broad HRQOL measures, questionnaires that focus on specific symptoms (eg, depression) or areas of functioning (eg, social functioning) also are popular. Mackner and Crandall (12) highlight the benefits of including a comparison group when assessing psychosocial functioning/ HRQOL. A control group (healthy age-matched peers or those with another chronic illness) can identify problems that are specific to young people with IBD. Although normative reference data are often used in place of matched control groups, these data cannot account for cohort effects, geographical location, and socioeconomic factors that may be specific to the population being studied.

Inclusion Criteria
All of the studies retrieved by the database search were examined using the following inclusion criteria. Those not meeting these criteria were excluded from the review. Published in a peer-reviewed journal Study examined data from original research Study is written in English Study uses quantitative methods Participants aged 18 years or younger Participants have a medically conrmed diagnosis of CD, UC, or IBD unclassied 7. Outcome measures include HRQOL or aspects of psychosocial functioning (eg, social/behavioural functioning, self-esteem, body image, depression, anxiety) 8. Established or standardised questionnaires are used 1. 2. 3. 4. 5. 6.

OBJECTIVES
This is a growing area of research in which various aspects of psychosocial functioning have been examined using a range of different measures. Although the most recently published review (12) summarises the literature up to 2006, it was not performed in a systematic fashion. Because several articles have been published in the intervening years, it is timely for a systematic review to be conducted to evaluate this research literature in greater depth. With increasing recognition that populations with IBD may be experiencing difficulties, intervention trials are already under way to evaluate the efficacy of psychological treatments such as cognitive-behavioural therapy (13). A thorough examination of the evidence to date is therefore clinically relevant. The present review summarises the relevant literature, focussing on psychosocial functioning and HRQOL in young people with IBD (up to age 18 years), to critique the methodological quality of this literature, discuss the implications of the findings, and make recommendations for future research and clinical practice.

Data Extraction and Quality Rating

Studies meeting inclusion criteria were quality rated by the principal researcher (S.C.R.) using an assessment developed from validated research appraisal protocols (14,15). Studies were rated on 17 items in 4 main areas: selection of participants, assessment, confounding factors, and statistical analysis. For each item, it was possible to score 2 if the item was well-covered, 1 if adequately covered, or 0 if poorly covered, giving a maximum score of 34. A quality rating percentage score of good (>75%), acceptable (>50%), or poor (<50%) was then awarded to each study. Fifty percent of included studies were randomly selected and independently rated by another researcher (K.A.R.) using the same quality rating scale. There was 100% interrater agreement for the assignment of articles to quality rating categories. Following quality rating, methodological, demographic, and clinical information were systematically extracted from each article.

PATIENTS AND METHODS Search Strategy

To identify suitable studies, the electronic databases Ovid MEDLINE, EMBASE, PsychINFO, British Nursing Index, HMIC, EBSCO (CINAHL), and Web of Science were searched between January 1990 and December 2009 using the following search terms: [affect or emotion or psychosocial or quality of life or depression or self esteem or self concept or stress or attitude or aggression or shy or social or coping or body image or anorexia or body dysmorphia or social interaction or well-being or mental health or mood or mental disorder or behaviour or anxiety or anxious or anger or fear or frustration or peer or agoraphobia or eating disorder or bulimia or mood disorder or interpersonal relations or life style or lifestyle or autonomy or self efficacy or social perception or psychology or psychiatry] AND [adolescent or pediatric or paediatric or child or children or youth or young people or young people or teen] AND [Crohn or colitis or IBD]. Because of the wide-ranging definitions of HRQOL and psychosocial functioning, these detailed search terms were chosen to increase the sensitivity of the search. A multidatabase search www.jpgn.org

RESULTS
The database search identified 2141 articles. Of these, 1863 were either duplicates or were not deemed relevant to the present review and were excluded on the basis of the title. Abstracts of the remaining 278 articles were examined using full inclusion criteria, resulting in the exclusion of a further 252 articles; this left 26 potentially appropriate articles, 14 of which were excluded after reviewing the full text (10,11,1627) (Fig. 1). The 12 remaining articles were deemed suitable to be included in the review and are discussed in detail below (4,5,2837).

Demographic and Methodological Information

These 12 studies had a total of 5330 participants between the ages of 4 and 18 years (mean 14.1 years). Seven hundred ninety participants had IBD, and 4540 were controls (4474 healthy, 20 headache, 20 diabetes, 26 functional gastrointestinal complaints). Ten studies (n 706) provided information on disease type (66% CD, 31% UC, and 3% IBD unclassified), and 10 studies (n 740) reported sex (54% male) (Table 1).

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Databases searched using search terms: Ovid medline EMBASE PsychInfo British nursing index HMIC EBSCO CINHAL WOK web of science between the dates 1990 Dec 2009 Articles identified n = 2141

Table 1 provides a summary of each study in its entirety for reference. In interpreting psychosocial functioning/HRQOL scores, larger or increasing scores indicate better functioning unless otherwise stated.

Self-esteem
Excluded n = 1863 Duplicates removed and articles excluded on the basis of title

Titles and abstracts screened n = 278 Excluded n = 252 Not child or adolescent sample Not original journal article Not published in peer reviewed journal Not in available in English Medical rather than psychological focus Focus on parent rather than child

Full copies of potentially appropriate articles retrieved and reviewed using full inclusion/exclusion criteria n = 26

Excluded n = 14 Secondary data from another included study n = 5 Primary outcome not HRQOL or psychosocial function n = 1 No clear outcome data n = 3 Not standardised measures n = 2 Other = 3

Publications included in systematic review. n = 12

FIGURE 1. Flowchart of the study selection process. Eleven of the studies were cross-sectional observational studies and 1 used a prospective longitudinal design (36). Four studies (33%) did not have a control group (5,28,36,37); 5 (42%) used either matched controls recruited at the time of the study (4,29,35), another illness group (32), or illness groups or healthy controls (31). Three studies (25%) used previously collected reference group data (30,33,34). Time since diagnosis varied widely between studies from 0 months (5,36), >1 to 2 months (28), 3 months (35), 6 months (30,33,34), and >1 year (4). From the information available (4 studies did not report time since diagnosis), the mean duration of disease was 2.74 years. Only 6 studies reported disease severity in categories that could be compared among studies (4,5,33,34,36,37). In these studies (n 539), 36% had mild, 45% had intermediate/moderate, and 19% had severe disease activity. A wide range of standardised assessments were administered via questionnaires and clinician-led interviews. The majority of studies included both self- and parent-report questionnaires (4 used self-report measures only). Four studies conducted standardised diagnostic interviews with either the child (31) or the child and parent (5,28,37). Quality rating revealed that 3 articles (5,28,30) scored in the acceptable range (>50%), whereas the remaining 9 papers scored in the good range (>75%). Methodological shortcomings are discussed below in relation to the results as they arise.

Self-esteem was measured using standardised, validated selfreport questionnaires in 5 studies (4,3033). Only one of these studies, using a measure of self-esteem, I think I am, developed in Sweden (38), found that young people with IBD had significantly lowered self-esteem compared with healthy controls (Fr 8.46, P < 0.04) (31). T scores were not provided, making it difficult to determine whether the reduction in self-esteem was clinically significant. Additionally, the present review used 20 outcome measures in a small sample (n 20) without adjusting significance levels for multiple comparisons. Another study using I think I am as the only outcome measure (33) found no significant difference in self-esteem between young people with IBD (n 71) and a previously assessed healthy reference group. Two studies using the Piers-Harris Childrens Self-Concept Scale (39), a more commonly used measure yielding T scores, also found no significant difference in self-esteem between young people with IBD and healthy controls (4,32). Indeed, Gold et al (32) found that young people with IBD actually had a significantly better self-concept than the normative group; however, participants in both of these studies had mild disease activity. In line with these findings, De Boer et al (30), using the Dutch version of the SelfPerception Profile for Adolescents (Harter) (40), did not find that young people with IBD had lowered self-esteem. They did demonstrate that self-esteem was a good predictor of all of the domains of HRQOL, but they were unable to make any assumptions about the direction of causality.

HRQOL
Five articles assessed HRQOL (29,30,3436). The 2 studies that administered generic multidimensional HRQOL instruments (29,30) had somewhat conflicting results. Using the Child Health Questionnaire (41,42), Cunningham et al (29) found that although parents reported their children with IBD to be more impaired than healthy controls in the overall areas of physical health (F 50.17, P < 0.001) and psychological health (F 5.789, P < 0.05), young people themselves did not report more difficulties except on the general health subscale. In contrast, using the Dutch Childrens AZL/TNO Quality of Life Questionnaire (DUCATQOL) (43), De Boer et al (30) found that adolescent boys with IBD self-reported significantly worse overall HRQOL than the reference group (P < 0.01). The age range of the reference data, however, did not match that of the participants, resulting in unsatisfactory analyses (girls with IBD could not be compared with controls in 2 of the 4 domains of the DUCATQOL) (30), and although the 25-item version of the DUCATQOL administered was reported to be internally consistent and reproducible (43), no validation studies had been published at that time. (Validity testing of the DUCATQOL has subsequently been reported (44).) Two studies using an IBD-specific HRQOL measure, the IMPACT Questionnaire (10,11), and generic HRQOL questionnaires found that HRQOL was significantly lower in young people with IBD (34,35). Loonen et al (34) analysed their data by 2 age strata in accordance with the normative data for the generic HRQOL measure (TNO-AZL Childrens Quality of Life questionnaire) (45). They found that although adolescents (1218 years, n 65) had significantly lower HRQOL than healthy peers on 4 domains (body www.jpgn.org

Psychosocial Functioning
The 5 main outcomes (self-esteem, HRQOL, anxiety and depression, social competence, and behavioural problems/functioning) identified will be considered separately so that comparisons can be made between studies (Table 2). An average of 4 outcome assessments were used in each study, and therefore the same studies are discussed in relation to different outcomes. For this reason,

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TABLE 1. Table summarising studies included in systematic review


Age range No info; mean age 11.98 y Kiddie-SADS interview, FRI, A-SADS-L interview, FILE Parent and self-report CD or UC >12 mo; mean duration 3.5 mo Depression, anxiety, (maternal depression, life events, family relationships) HRQOL Child health questionnaire Parent and child versions Diagnosis (CD, UC, or IBDU) Outcomes assessed Assessments Self-report or parent report Signicant results Time since diagnosis

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1018 y; mean age 14.96 y IBD, no further info No info; mean duration no info

Study

Country

Participants (IBD: n) (Controls: n)

Burke et al (28)

US

IBD 36; no control group

Cunningham et al (29)

US

IBD 49; healthy controls 49

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De Boer et al (30) 1218 y; mean age 15.2 y DUCATQOL, Dutch version SPPA, Dutch version STAI, CBCL Self-report x3, parent completed CBCL CD, UC, or IBDU >6 months; mean duration 3.8 y HRQOL, self-esteem, anxiety (trait), behaviour problems

The Netherlands IBD 40; healthy children 1359 (reference data DUCATQOL)

Engstrom (31) Sweden

718 y; mean IBD 20; headache age 16.5 y control 20; diabetes control 20; healthy control 20 CBCL frisk well-being scale, Rotter sentence completion test, ITIA, CDI, RCMAS, Raven matrices, CAS

UC or CD

No info; mean Psychological adjustment, duration 4.2 y social competence, (range 1.08.2 y) well-being, emotional adjustment, psychiatric disorders, self-esteem, depression, anxiety, cognitive abilities No info; mean duration: 2 y Depression, self-concept, social adjustment CBCL, CDI, Piers-Harris Childrens Self-Concept Questionnaire developed by researchers ITIA

Parent report, self-report, and child interview

Gold et al (32) 818 y; Mean age 13.31 y UC or CD, excluded if had a colectomy

Canada

IBD 36; functional gastrointestinal complaints controls 26 1016 y; mean age 14.6 y CD, UC, or IBDU >6 mo; mean duration 2.9 y Self-esteem

Self-report and parent report

Lindfred et al (33)

Sweden

Self-report

14% met diagnostic criteria for major depression, 28% for atypical depression; 10 children had a history of anxiety. The depressed group was less severely ill than the nondepressed group (P 0.006). Parent report: IBD group signicantly impaired HRQOL compared with controls (physical health score P < 0.000, psychosocial score P < 0.05); child report: no signicant differences in HRQOL compared with controls (except in general health) Boys with IBD had signicantly worse HRQOL (P < 0.01) and more behavioural problems (P < 0.05) and internalising behaviour (P < 0.01) compared with healthy peers. Girls had more internalising behaviour (P < 0.05) only. No signicant differences in state anxiety or self-esteem compared with controls. On most variables, children with IBD had highest levels of psychiatric disturbance, that is, IBD is higher than that in healthy children for behaviour problems (P < 0.03), social competence (P < 0.04), emotional adjustment (P 0.001), psychiatric disorders (P 0.01), self-esteem (P < 0.01), and depression (P < 0.02) IBD group was less depressed and had fewer behaviour problems than controls (P 0.03). No scores were in the clinical range. Children with IBD have a higher than average self-concept. No signicant difference in self-esteem between IBD group and comparison or normative group

Loonen et al (34) 818 y; mean age 14.3 y CD, UC, or IBDU >6 mo; mean duration no info HRQOL

IBD 71; previously collected healthy reference group 1037; normative data from ITIA 2662 The Netherlands IBD 83; Dutch schoolchildren controls 1810 1117 y; mean age 14.69 y CD, UC, or IBDU >1 y; mean duration 3.53 y

TACQOL IMPACT III (NL)

Self-report

Mackner and Crandall (4)

IBD 50; healthy controls 42

YSR, CDI, RCMAS, PHSCS, coping strategies inventory, social support questionnaire Psychosocial functioning, behavioural/emotional functioning, social competence, self-esteem, coping strategies, social support HRQOL fatigue Peds-QL multidimensional fatigue scale, Peds-QL 4.0 IMPACT III, CDI-SF

Self-report

Adolescents with IBD had signicantly lowered HRQOL on 4 domains (P < 0.05). Younger children had comparable or better HRQOL than healthy peers. No signicant differences on any measures

Marcus et al (35)

US

IBD 70; healthy controls 157

1017 y; mean age 14.1 y

CD, UC, or IBDU

>3 mo; mean duration 34 mo

Self-report and parent report

Psychosocial Functioning and Quality of Life in Paediatric IBD

Otley et al (36)

US and Canada

IBD 218; no controls

>9 y; mean age 12.7 y

CD, UC, or IBDU

0 mofollowed up to 1 y

HRQOL

IMPACT III

Self-report

IBD group had signicantly lower generic HRQOL than healthy controls (P < 0.0001). No signicant difference in depressive symptoms between IBD and controls. Signicant improvement in HRQOL scores 1 y postdiagnosis (P < 0.05)

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Age range No info (appears CD or UC to be 4.9215 y); mean age 11.6 y 0 mo Diagnosis (CD, UC, or IBDU) Outcomes assessed Assessments Self-report or parent report Signicant results Time since diagnosis 1117 y; mean age 14.7 y CD or UC No info; mean duration 2.4 y (range 09.7 y) Psychopathology of child K-SADS-P interview, AAI, Mostly parent report or 73% had DSM-III diagnoses (predominantly and parent, maternal CBCL, MCMI, Lockeinterview with parents; separation anxiety and major depression), attachment, attachmentWallace mental scale, some interview/assessment a signicant number showed internalising related disorders in FILE, IOF, COBI, of child but no self-report behaviour (P < 0.01) children (separation anxiety, Irvine sentence completion measures dysthymia/depression), test, WISC-R, TAT OCD disorder children Depression (and its relation CDI, SADS-PL if scored Self-report, clinical High rates of clinically signicant depressive with disease factors) >12 on CDI interview with child symptoms in older children and adolescents and parent with IBD. Twenty-ve percent had depressive symptoms (>12 CDI) and 16 of 19 psychiatrically interviewed had clinically signicant depressive disorder. No. studies nding young people with IBD were signicantly impaired compared with controls No. studies nding no difference compared with controls Conclusions

Ross et al

TABLE 1. (Continued )

Study

Country

Participants (IBD: n) (Controls: n)

Szajnberg et al (5)

US

IBD 15; no controls

Szigethy et al (37)

US

IBD 102; no controls

AAI Adult Attachment Interview; A-SADS-L Adult Schedule for Affective Disorders and Schizophrenia, lifetime version; CAS Childrens Assessment Schedule; CBCL Child Behaviour Checklist; CD Crohn disease; CDI-SF Child Depression InventoryShort Form; COBI Clinicians Objective Burden Index; DSM Diagnostic and Statistical Manual of Mental Disorders; DUCATQOL Dutch Childrens AZL/TNO Quality of Life; FILE Family Inventory for Life Events; FRI Family Relationship Index Scale; HRQOL Health-Related Quality of Life; IBD inammatory bowel disease; IBDU inammatory bowel disease unclassied; IOF Impact of Events Scale; IMPACT III IBD-Specic HRQOL Instrument; ITIA I think I am; K-SADS-P Kiddie Schedule for Affective Disorders and Schizophrenia; MCMI Millon Clinical Multi-Axial Inventory; OCD obsessive-compulsive disorder; Peds-QL Pediatric Quality of Life Inventory; PHSCS Piers Harris Childrens Self-Concept Scale; RCMAS Revised Childrens Manifest Anxiety Scale; SADS-PL Schedule for Affective Disorders and Schizophrenia for School-Aged ChildrenPresent and Lifetime Versions; SPPA Self-Perception Prole for Adolescents (Dutch version); STAI State-Trait Anxiety Inventory for Children (Dutch version); TACQOL TNO-AZL Child Quality of Life Questionnaire; TAT Thematic Apperception Test; UC ulcerative colitis; WISC-R Weschler Intelligence Scale Revised; YSR Youth Self-Report.

TABLE 2. Summary of included studies by outcome (including participant numbers) JPGN

Outcome

No. studies

Self-esteem HRQOL

5 4

131 (IBD: 20, healthy controls: 20) 2 using generic HRQOL measures (parent report29) (self-report, boys only30), (IBD: 89, healthy controls: 1408) 2 using IBD-specic HRQOL measures34,35 (IBD: 133, healthy controls: 1852) 0

44,30,32,33 (IBD: 197, healthy controls: 2438, other: 26) 1 (self-report29) (IBD: 49, healthy controls: 49)

Inconclusive evidence for lowered self-esteem HRQOL lowered in young people with IBD compared with healthy controls

Mood (anxiety and depression) Structured diagnostic interview

Self-report

Depression: 34,32,35 (IBD: 156, other: 26, healthy controls: 199)

Contradictory ndings between methods Young people with IBD have higher levels of depression and anxiety than do healthy controls Young people with IBD do not appear to be more depressed or anxious than do healthy controls

45,28,31,37 (IBD: 153, normative data used31; IBD: 20, healthy controls: 20, headache: 20, diabetes: 20) Depression: 131 (IBD: 20, healthy controls: 20, headache: 20, diabetes: 20) Anxiety: 0

Social competence

Anxiety: 24,31 (IBD: 70, healthy controls: 20, headache: 20, diabetes: 20) 24,32 (IBD: 86, healthy controls: 43, other: 26) 24,32 (IBD: 86, healthy controls: 43, other: 26)

Inconclusive evidence for impaired social competence Inconclusive evidence for increased incidence of behavioural difculties

Behavioural difculties

1 parent report31 (IBD: 20, healthy controls: 20, headache: 20, diabetes: 20) 231 (IBD: 20, healthy controls: 20, headache: 20, diabetes: 20) Signicant for boys only30 (IBD: 19 boys, 21 girls, healthy controls: 1359)

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HRQOL Health-related quality of life; IBD inammatory bowel disease.

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Psychosocial Functioning and Quality of Life in Paediatric IBD with mixed results (4,31,32,35). Although Engstrom (31) found that young people with IBD reported significantly more depressive symptoms than healthy controls (Fr 10.00, P < 0.02), the other 3 studies did not find evidence of increased symptoms of depression in comparison with healthy controls (4,35) or another illness group (32). Two of these studies (4,31) also assessed anxiety using a self-report measure: the Revised Childrens Manifest Anxiety Scale (51); they both failed to find increased symptoms of anxiety in the IBD group compared with controls.

complaints, motor functioning, autonomy, and negative emotions) (P < 0.05), younger children (811 years, n 18) had comparable or better HRQOL than controls (the small sample of younger children had mainly inactive or mild disease). Marcus et al (35) found that young people reported significantly lower HRQOL than matched healthy controls on both the IBD-specific IMPACT (P < 0.001) and on a well-established generic measure of HRQOL (PedsQL 4.0) (9) (P < 0.001). The second IMPACT was a large multisite prospective cohort study that administered the questionnaire to 218 young people with IBD; mean HRQOL scores significantly improved from baseline during the first year postdiagnosis (P < 0.05) (36).

Social Competence
Three studies examined social competence as an outcome (4,31,32). Engstrom (31) and Gold et al (32) used a parentreport questionnaire, the Child Behaviour Checklist (52), whereas Mackner and Crandall (4) administered the self-report version, the Youth Self-Report (53). Both measures have a social competence scale in which an increasing score indicates better social functioning. Although 2 studies (4,32) found social competence to be in the normal range and comparable with controls, Engstrom (31) found that mothers rated their children with IBD as significantly less socially competent than healthy children (Fr 7.86, P < 0.04). Given the small sample size and large number of measures used in the present review, however, it would be prudent to interpret these results with caution (eg, by adopting a more conservative significance level).

Mood (Anxiety and Depression)

Seven studies investigated anxiety and depression using either structured diagnostic interviews or self-report questionnaires, increasing scores on anxiety, and depression measures indicate increasing levels of distress.

Structured Diagnostic Interviews

Four studies (5,28,31,37) used standardised clinical interviews with either children or their parents. These studies found that young people with IBD had increased levels of psychiatric disturbance or symptoms of depression and anxiety meeting Diagnostic and Statistical Manual of Mental Disorders-III-R (DSM-III-R) criteria (46). Prevalence varied from 25% (37) to 73% (5). Engstrom (31) compared 20 young people with IBD to headache, diabetes, and healthy controls using the Child Assessment Schedule (47) and found that significantly more young people with IBD fulfilled criteria for psychiatric disorder (mainly depression or anxiety) than did the 3 control groups (x2 11.34, P < 0.01). The results of the other 3 studies using structured diagnostic interviews should be interpreted with caution. Burke et al (28) and Szajnberg et al (5) recruited newly or recently diagnosed young people with IBD and administered the Kiddie Schedule for Affective Disorders and Schizophrenia (48). Although this is a well-validated semistructured interview, both studies had small sample sizes of 36 (28) and 15 (5) subjects and no control groups. Burke et al (28) found that 42% of children with a mean disease duration of 3.5 months reported symptoms of depression, whereas Szajnberg et al (5) reported that 73% of their sample had psychiatric diagnoses at the time of their IBD diagnosis. Szajnberg et al also reported that all of the children with a DSM-III diagnosis had at least 1 parent with psychopathology, and Burke et al reported that the mothers of the depressed children in their study reported increased conflict and reduced cohesion in their families. Szigethy et al (37) omitted a control group, but they had a much larger sample of 102 young people with IBD. They used the Schedule for Affective Disorders and Schizophrenia for Schoolaged Children-Present and Lifetime Version (49) interview, with 19 children scoring above the clinical cutoff (>12) on a self-report questionnaire (the Childrens Depression Inventory) (50). They reported that this confirmed a clinically significant diagnosis of depression in 16 of the 19 interviewed and uncovered previously undiagnosed comorbid anxiety disorders in 11 of these individuals. No measures of parental or family functioning were used in the present review.

Behavioural Problems/Functioning
Four studies examined behavioural functioning using either the Child Behaviour Checklist (3032) or Youth Self-Report (4). These measures yield a total behavioural problems score as well as internalising behaviour (withdrawn, somatic complaints, and anxious/depressed) and externalising behaviour (rule-breaking and aggressive behaviour) scores. For these domains, an increasing score indicates greater levels of behavioural problems. Engstrom (31) found that young people with IBD had significantly more total behavioural (x2 Fr 9.34, P < 0.03) and internalising behaviour (x2 Fr 9.83, P < 0.02) problems than healthy controls. De Boer et al (30), comparing young people with IBD to a healthy reference group, found significant differences on the total behavioural problems (P < 0.05) and internalising behaviour subscales (P < 0.01) for boys, whereas for girls, the only significant difference was found for internalising behaviour (P < 0.05). In contrast, Gold et al (32) and Mackner and Crandall (4) found mean scores in the normal range and no significant differences between young people with IBD and controls; a subset of 20% of participants with IBD did, however, report clinically impaired levels of behavioural/emotional functioning (4).

DISCUSSION
The reviewed studies present a somewhat mixed picture of psychosocial functioning/HRQOL in children and adolescents with IBD, although the evidence for decreased HRQOL and increased incidence of psychiatric disorders (eg, anxiety and depression, assessed using structured diagnostic interviews) seems fairly consistent across the included studies. In the 2 studies in which parental/family functioning also was assessed, all of those who showed psychiatric caseness came from families with other psychological problems. Children and young people with an emotional disorder are at least twice as likely as those without to have a parent with a mental health disorder (54). The evidence for lowered self-esteem, symptoms of depression and anxiety

Self-report Questionnaires
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Ross et al (measured by self-report measures), impaired social competence, and behavioural functioning is less clear because of conflicting results. To make sense of these findings, confounding factors that may have influenced outcomes are considered and placed in the context of other relevant research.

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people from more stable family backgrounds are more likely to have their IBD diagnosed and treated. Studies have also reported that children with CD proportionately are more likely to come from affluent backgrounds (57,58).

Age Self-report Versus Parent Report

The majority of studies assessing self-esteem using selfreport measures found that young people with IBD reported comparable self-esteem to healthy peers. In a study using a disease-specific IMPACT score, body image was found to be impaired in adolescents with IBD (34). Research on the incidence of body image disturbances in children with IBD, although studied in other chronically ill children (eg, those with diabetes), is conspicuously absent from the research literature at present. In making sense of the unimpaired levels of self-esteem, in addition to the inconsistent evidence for anxiety and depression, the discrepancy between findings of studies using self-report and parent report measures needs to be considered. Research findings indicate that young people with IBD may have difficulty reporting psychological symptoms (31) and tend to report fewer symptoms compared with their parents (22,23,29). Canning (55) found a similar discrepancy in reporting with a sample of children with other chronic illnesses (including cancer, cystic fibrosis, and diabetes) and their parents. In the healthy comparison group, however, children reported symptoms more frequently than did their parents. The underreporting or minimising of symptoms seen in some young people with IBD could be caused by denial, which may be adaptive in buffering them against experiencing the full effect of the disease; indeed, 2 studies have found that young people with IBD tend to use more avoidant coping styles than do healthy peers (27,31). Conversely, it is possible that young people with IBD are reporting symptoms accurately and it is their parents, who are themselves depressed, anxious, or overinvolved with their children, who are pathologising normal behaviour and overreporting symptoms compared with parents of nonchronically ill children. Age also may be predictive of HRQOL. Loonen et al (34) found that although adolescents with IBD had impaired HRQOL, younger children had comparable or better HRQOL than healthy peers. A longitudinal study examining HRQOL during the first year of diagnosis (36) reported that for each increasing year of age, there was an associated 5-point decrease in self-reported HRQOL. Similarly, Szigethy et al (37) noted that diagnosis later in childhood was associated with increased depressive symptoms. In the general population, depression increases in prevalence from 1% prepuberty to 3% postpuberty (54). Theoretically, it is possible that IBD has a greater detrimental effect on an adolescents ability to complete developmental tasks (eg, developing independence and autonomy) and subsequently causes greater psychological distress. In light of these findings, examining children and adolescents as 1 group may lead to these difficulties being masked. The mean ages of participants in the studies reviewed vary between 11.6 and 16.5 years, with the largest age range being 7 to 18 years. The possibility should be considered that conflicting findings may result from the developmental heterogeneity of participants within these studies. Additionally, the validity of making comparisons between adolescents with IBD, who may require longer to complete the developmental tasks associated with adolescence, and controls matched on chronological age should be questioned.

Time Since Diagnosis

Individuals with a wide range of disease durations were included in the reviewed studies, from recent onset to several years postdiagnosis. Although Burke et al (28) did not find that HRQOL scores were predicted by time since diagnosis, they were examining recent-onset cases (<12 months). A longitudinal study found improvements in HRQOL during the first 6 months following diagnosis, which persisted during the course of the first year (36). Difficulties in psychosocial functioning/HRQOL seen before 6 months postdiagnosis are perhaps more likely to be normal adjustment reactions to being acutely unwell and receiving a diagnosis of a chronic illness. Therefore, the stage at which HRQOL is assessed may determine what is actually being measured and affect the results.

Disease Severity
Disease severity also may contribute to the variation in results. Increased disease severity was found to correlate with increased depression (37), lowered self-esteem (33), and decreased HRQOL (29,35,36). It seems intuitive that young people experiencing more severe symptoms would report lower HRQOL than those in remission. Most of the studies reviewed had large proportions of participants categorised with either mild or moderate disease severity. Therefore, information about the difficulties experienced by individuals with more severe symptoms may be missing. The underrepresentation of this group also may make correlations between severity and psychosocial functioning more difficult to appreciate; however, a number of studies found no association between disease severity and psychopathology (4,17,18,28). There is, however, some evidence that psychosocial factors are more predictive of emotional and behavioural functioning than disease factors (24,28). Low socioeconomic status has been found to correlate with increased depression (32) and decreased selfesteem (33), whereas parental separation correlated with reduced self-esteem (33). This is consistent with research in the general population, where these factors are considered to increase risk for psychological difficulties (56). Interestingly, children with IBD have a consistently higher proportion of cohabiting or married parents than those in healthy control groups (31). Parents perhaps stay together to care for their sick child, or alternatively, young

Strengths and Weaknesses of the Evidence

The reviewed studies have a number of methodological limitations, which make interpreting this body of evidence challenging. The frequent lack of comparison groups and reliance on normative data make it difficult to determine whether differences are the result of cohort effects or an effect of the disease. Although there may not be large numbers of young people with IBD experiencing clinically significant symptoms, there may be subsets that are impaired and would benefit from extra support from their gastroenterology team. Standardised, validated measures that provide T scores would allow the clinical significance of study results to be determined. The small sample sizes, which are common and often unavoidable in paediatric research, make it more difficult to determine the validity of significant results. None of the included studies based sample size on a power calculation and only 1 www.jpgn.org

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Psychosocial Functioning and Quality of Life in Paediatric IBD needs to be considered given the increased awareness of body image and appearance that is typical of teenage development. Developing a clearer understanding of the effect of IBD on HRQOL and psychosocial functioning would be beneficial for clinical staff working with this illness group because it would allow early interventions to be targeted to those most at risk. This may prevent the development of more serious mental health problems such as depression, which has been linked to difficulties with medication adherence (61), and anxiety, which may exacerbate future disease activity (8). In addition to the individual benefits associated with improved emotional and physical health, there could be financial benefits and associated savings for the health system in terms of reduced hospital admissions; also, there is a likelihood of reducing school absences, which in turn will have positive effects on the childs or teenagers social, emotional, and academic development. Acknowledgment: The authors thank Dr Kimberly Ross, who co-rated the papers included in the review.

calculated effect sizes for their results (30). The majority of studies included participants from a wide age range with varying disease severity and disease durations. The present review indicates that these factors may have an influence on HRQOL and as such should be considered carefully in the study design and analysis. Inclusion and exclusion criteria were often not reported in sufficient detail. All of the studies except for one used a cross-sectional design, which means causality cannot be determined. More recently published studies, however, appear to be addressing some of the limitations outlined above. Otley and colleagues (36) ongoing longitudinal study will provide valuable information about HRQOL over time. Since the validation of an IBD-specific HRQOL measure (the IMPACT score), a growing number of studies have reported robust results that allow easy comparison. HRQOL is frequently used as an outcome in clinical studies of patients with IBD. There also has been an increase in the use of objective, standardised disease severityrating questionnaires (eg, the Paediatric Crohn Disease Activity Index (59), the Pediatric Ulcerative Colitis Activity Index (60)), allowing for more accurate disease severity recording and better comparison between studies.

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Strengths and Limitations of the Review

The present review used an extensive search strategy to identify all of the relevant studies to the review question. The strict inclusion and exclusion criteria ensured that only articles with a high level of methodological quality were included. The findings correspond with those reported in the most recent review (12), but consider these in more depth and discuss confounding factors such as time since diagnosis and self- versus parent reporting. Despite these strengths, there are several limitations that should be considered when interpreting the conclusions of the present review. Because of time constraints, it was neither possible to conduct hand searches of major journals in the field nor co-rate all of the included studies. For the same reason, unpublished studies and articles not available in English were not included in the review. This may have resulted in a publication bias in the included studies.

CONCLUSIONS AND FUTURE DIRECTIONS

Owing to the conflicting findings, methodological variation, and limitations of the research in this field, only tentative conclusions can be drawn. Young people with IBD appear to be at a higher risk of reduced HRQOL and of developing psychiatric conditions such as anxiety or depression compared with their healthy peers. There may be a higher incidence of low self-esteem, symptoms of depression and anxiety, impaired social competence, and internalising behaviour problems, but the evidence to date is mixed. More research, therefore, is required. The additional research must take into account the discrepancy in child and parent reporting by using multiple informants; address the issue of disease severity by either ensuring groups are more homogenous or using statistical techniques to adjust for variation; and address the issue of age by examining children and adolescents separately. To avoid pathologising normal adjustment reactions and labelling young people with psychiatric diagnoses, only those who have had sufficient time to adjust to their IBD diagnosis should be recruited. Ensuring that studies have larger sample sizes informed by a power calculation where appropriate, using standardised well-validated measures, and reporting results more consistently would increase the quality of this area of research. Research into body image would be timely because this appears to be an underresearched area and www.jpgn.org

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Ross et al
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