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Body image dissatisfaction in patients with inflammatory bowel disease: a systematic review

Background and aims Little is known about the relationship between inflammatory bowel disease (IBD) and body image. The aim of this systematic review was to summarise the evidence on body image dissatisfaction in patients with IBD across four areas: (1) body image tools, (2) prevalence, (3) factors associated with body image dissatisfaction in IBD and (4) association between IBD and quality of life. Methods Two reviewers screened, selected, quality assessed and extracted data from studies in duplicate. EMBASE, MEDLINE, PsycINFO and Cochrane CENTRAL were searched to April 2018. Study design–specific critical appraisal tools were used to assess risk of bias. Narrative analysis was undertaken due to heterogeneity. Results Fifty-seven studies using a body image tool were included; 31 for prevalence and 16 and 8 for associated factors and association with quality of life, respectively. Studies reported mainly mean or median scores. Evidence suggested female gender, age, fatigue, disease activity and steroid use were associated with increased body image dissatisfaction, which was also associated with decreased quality of life. Conclusion This is the first systematic review on body image in patients with IBD. The evidence suggests that body image dissatisfaction can negatively impact patients, and certain factors are associated with increased body image dissatisfaction. Greater body image dissatisfaction was also associated with poorer quality of life. However, the methodological and reporting quality of studies was in some cases poor with considerable heterogeneity. Future IBD research should incorporate measurement of body image dissatisfaction using validated tools.


AbsTrACT background and aims
Little is known about the relationship between inflammatory bowel disease (IBD) and body image. The aim of this systematic review was to summarise the evidence on body image dissatisfaction in patients with IBD across four areas: (1) body image tools, (2) prevalence, (3) factors associated with body image dissatisfaction in IBD and (4) association between IBD and quality of life. Methods Two reviewers screened, selected, quality assessed and extracted data from studies in duplicate. EMBASE, MEDLINE, PsycINFO and Cochrane CENTRAL were searched to April 2018. Study design-specific critical appraisal tools were used to assess risk of bias. Narrative analysis was undertaken due to heterogeneity. results Fifty-seven studies using a body image tool were included; 31 for prevalence and 16 and 8 for associated factors and association with quality of life, respectively. Studies reported mainly mean or median scores. Evidence suggested female gender, age, fatigue, disease activity and steroid use were associated with increased body image dissatisfaction, which was also associated with decreased quality of life. Conclusion This is the first systematic review on body image in patients with IBD. The evidence suggests that body image dissatisfaction can negatively impact patients, and certain factors are associated with increased body image dissatisfaction. Greater body image dissatisfaction was also associated with poorer quality of life. However, the methodological and reporting quality of studies was in some cases poor with considerable heterogeneity. Future IBD research should incorporate measurement of body image dissatisfaction using validated tools.

IntroductIon
Inflammatory bowel disease (IBD) is associated with a range of debilitating symptoms 1 and affects around 300 000 people in the UK 2 , over 1 million in the USA and 2.5 million across Europe. 3 A potentially overlooked issue for patients with IBD is body image dissatisfaction (BID). Body image (BI) is how an individual perceives themselves physically 4 and sufferers have a distorted and negative view of themselves, feeling anxious and uncomfortable about their body. Additionally, negative BI can have a serious impact on health and well-being. 5 Social media and celebrity attention contribute to pressure to adhere to an 'ideal' body and an obsession with appearance. 6 7 Discontentment with aspects such as body weight, shape, appearance and skin may contribute towards an individual having BID. 8 Studies have shown patients with negative BI are more likely to suffer with depression, anxiety and feel suicidal and BID can impact negatively on relationships 9 and quality of life (QoL). 10 .
Various tools have been used in healthcare to measure BI including the Body Image Ideals Questionnaire, the Body Image Scale and the Cash Body Image Disturbance Questionnaire (BIDQ). 11 There are also condition-specific BI tools such as the Body Image Scale (BIS) for IBD. 12 Both condition-specific symptoms and treatments may contribute to BID in patients with IBD, particularly during periods of active disease rather than remission. Symptoms can include urgent bowel movements, bloating, excess wind, fatigue, skin problems and ulcers. Treatment with steroids can be associated with weight gain, acne and mood swings. 13 Surgeries may also impact on BI due to scarring and implementation of a stoma. 14 15 Those suffering with IBD or BID are at an increased risk of mental health issues 16 17 ; this could be worse for patients living with both conditions. Furthermore, most patients with IBD are diagnosed at adolescence, 18 when BI is important. BI is currently not routinely considered in the management of IBD.
No existing or ongoing systematic reviews on BI in IBD have been identified. However, multiple primary studies, mainly cross-sectional in nature, assess BI as an outcome in patients with IBD, with disparate results. A systematic review is therefore warranted to synthesise and clarify the evidence base.

Open access
The following four questions will be addressed: 1. What tools are used to measure BI in patients with IBD and what are their components? 2. What is the prevalence and severity of BID in patients with IBD? 3. What factors are associated with BID in patients with IBD? 4. Is there an association BID in patients with IBD and QoL?

Methods
This systematic review has been reported according to the Preferred Reporting Items of Systematic Reviews and Meta-Analysis guidelines. 19 A protocol was previously registered (PROSPERO (CRD42018060999)) and submitted for publication and is currently in process. 20 A summary of the methods is reported below. Selection, data extraction and quality assessment were carried out by two independent reviewers with disagreements resolved through discussion or third reviewer. screening and selection criteria Study eligibility was based on the following criteria:

Study design
Any primary study reporting quantitative data.

Population
Patients of any age diagnosed with IBD. At least 50% of population must have IBD unless results are reported separately for subgroups of individuals with IBD.

Tools
Any tool measuring any aspect of BI (including QoL tools that had at least one BI-related domain or question).
Studies were also eligible (for questions 2-4) where they reported any measure of prevalence/frequency and severity of BID in patients with IBD; data on associations between any factor in patients with IBD and BID; or any association between BI and QoL measures in patients with IBD, including associations between two separate domain measures of the same tool.

Exclusion criteria
Case reports, qualitative research and conference abstracts published 3 years before the date of the searches.
Reasons for exclusion were recorded.

Quality assessment
Quality assessment was based on critical appraisal checklists for both prevalence and cross-sectional analytical studies from the Joanna Briggs Institute. 21 Studies solely included for question 1 were not quality assessed as the objective of this question was to compile a list of BI tools. Important quality items included sample selection, response rate during enrolment in the study, clear inclusion criteria and measurement of outcomes in a valid and reliable way.

Analysis
A narrative synthesis was carried out separately for each question, with key findings tabulated. Substantial heterogeneity relating to populations, tools and settings was apparent in the included studies meaning that meta-analysis was not appropriate. Consistencies and discrepancies in findings between studies were noted and discussed in the context of any likely sources of heterogeneity. Quality assessment findings were used when considering the strength of evidence for the latter three questions.

results
Database searches identified 587 records and 57 12 14 22-76 studies were included, with some studies eligible for multiple questions (see figure 1 for selection process and reasons for exclusion). All 57 papers reported using BI tools, 31 14  Of the 57 studies measuring BI, 51 were cross-sectional while the others varied (case-control, 25 prospective cohort, 51 65 case series, 39 randomised controlled trial 64 and non-randomised intervention study 42 ). Study populations included adults and children in settings including outpatients, presurgery/postsurgery, summer camps and online registries, from countries across the world. Twenty studies focused on BI as one of the main outcomes, but only six of these studies were non-surgery based.
Fifteen tools were identified (table 1). Seven tools were specifically for BI and eight were QoL tools which included a BI domain or question(s). The most frequently applied tool specific to BI was the Body Image Questionnaire (BIQ) which was used in 14 studies. The BIS was used in five studies and is the only tool validated in an IBD population. IMPACT-III (or earlier IMPACT-II) is a validated QoL questionnaire aimed at adolescents and children with IBD and includes a BI domain. It was used across 18 studies. The remaining 12 tools were used in only one to three studies, respectively.
None of the tools included had a clear cut-off point for defining BID but offered an indication of increasing or decreasing likelihood of dissatisfaction. In some tools, a higher score indicated better BI (BIQ, EORTC, DUX-25). In others, a higher score indicated increased BID (IMPACT, BIS, RFIPC, IBDSI (Inflammatory bowel disease stress index), Body Image Self-Consciousness during Intimacy Scale, BIDQ and ASWAP).
Tools where items had similar themes were grouped to show general focus of BI questions and are shown in table 2.

Open access
Similar components of tools were grouped into themes shown above. Askevold's Body Image Test (no information in paper or online), Body Image and Self-consciousness during Intimacy Scale (too specific) and the Body Image Assessment (based on figural drawing scales) were not included. ASWAP, Adapted Satisfaction with Appearance Scale; BIQ, Body Image Questionnaire; BIS, Body Image Scale; CBIDQ, Cash Body Image Disturbance Questionnaire.

What is the prevalence of BI dissatisfaction in patients with IBd?
Thirty-one studies including a total of 3634 patients reported on prevalence or severity of BID (see table 3 for study characteristics). Seventeen studies 14 14 found that 87% of patients reported some form of concern about an aspect of their BI using the Cash Body Image Disturbance Questionnaire. Muller et al 58 reported that 66.8% of patients with IBD stated they had impaired BI based on a researcher-devised questionnaire. The other 28 studies reported mean/median BI scores based on a range of tools.
In studies with populations undergoing surgery, it was found that there was no significant difference in BI scores (using the BIQ) after laparoscopic or open/ conventional surgery in patients with IBD. 33-35 63 77 Only one study found BI scores to be significantly improved after laparoscopic surgery compared with conventional surgery in CD. 36 .
BI was included as an outcome across 31 studies. All but one study compared results within the included IBD population, for example, UC versus CD, surgery versus no surgery and men versus women. Bel et al 23 found that women with IBD with disease in remission scored comparably with women in a healthy population. One longitudinal study by Saha et al 65 measured scores over 2 years and found that BI did not change despite improvements in symptoms.

What factors are associated with BId in patients with IBd?
Sixteen studies 14 23 24 30 34-36 47 54 58 60 61 63 65 67 71 totalling 2333 patients with IBD reported the association between various factors and BID (see table 4). Factors included those related to demographics as well as disease and treatment-related characteristics. Ten studies 14 63 65 female gender was found to be significantly associated with increased BID. One study 58 reported the odds of BID was over three times more in women than men (p=0.001), with strong associations reported in the other five studies. Increased disease activity was found to have a significant but moderate positive association in 7/9 studies. 14 23 34 61 65 67 71 Other factors found to be significantly associated with increased BID included steroid use, 14 60 65 71 age, 14 23 increased BMI, 14 71 smoking 14 and fatigue 23 (table 4). Saha et al 65 also found a significant association between extraintestinal manifestations and increased BID, but were the only study to assess this. Laparoscopic surgery was found to be associated with improved body image in 2/6 studies. 36 67 Ileal pouch-anal anastomosis (IPAA) seemed to result in patients being satisfied with their body image in two studies, 24 26 but they lacked a comparative surgery group. One study 50 compared IPAA and ileostomy and found better body image scores in the IPAA group. No significant associations were found between disease subtype and increased BID.

Is there an association between BId and quality of life in patients with IBd?
Eight studies 14 22-24 34 62 65 71 explored a potential association between BID and QoL across a total of 1371 patients, with seven presenting a significant association. Three studies 22 24 61 (table 4) focused on younger populations with the rest including adults only. The majority of studies included populations with both UC and CD while two 24 34 included only one subtype.
Statistically significant weak to moderately strong correlations were present in five studies 22 14 found that when using the BI scale, there was a significant difference in scores between those with good or poor QoL. Trindade et al 71 found that BI was positively correlated with psychological and physical QoL. Saha et al 65 found that a one-unit increase in the total ASWAP score (indicating poorer body image) was associated with a 0.62 decrease in QoL score (p<0.0001).
Various QoL tools (see table 1) were used across studies with some using more than one. Four of these questionnaires used (IMPACT II and III, GIQLI (Gastrointestinal Quality of Life Index) and WHOQOL-BREF (World Health Organization Quality of Life Instruments)) contain a question or domain on BI, potentially making them more likely to correlate with BI questionnaires.

risk of bias
The 31 studies relevant for questions 2-4 were assessed using criteria from the Joanna Briggs Institute critical appraisal tools for analytical cross-sectional and prevalence designs (online supplementary table 2). Only cross-sectional data were relevant for the review. Poor Table 4 Most common factors found to be significantly associated with impaired body image in IBD as reported in each study, including associations between reduced body image and reduced QoL   30 Trindade et al, 71 Lee et al 51 and Bel et al 23 adjusted for confounders and used validated outcome measurement tools but lacked adequate response rates. Twenty studies (64.5%) used an appropriate sample frame with acquisition of patients from outpatient settings, IBD registries or healthcare records. Eighteen studies (58.1%) clearly reported inclusion criteria applied when recruiting participants. Only 12 studies (38.7%) had response rates >75%. Fifteen studies (48.4%) used a tool which had been validated using factor analysis and internal consistency analysis to measure BI. The others used non-validated tools. Twelve studies 14 35 50 51 58 64 65 72 adjusted for potential confounders such as age, gender, BMI and previous surgery often using multiple regression models. Several studies reported limited demographic data. It should also be noted that sample sizes of many of the studies were small and CIs were mostly not presented.

dIscussIon summary of findings
Overall, 15 different tools were used across 57 studies to measure BI in patients with IBD. These included QoL tools incorporating BI questions or domains, BI tools and other adapted questionnaires. None offer a defining threshold for presence or absence of BID, which is not commonly considered as a specific psychological disorder unlike body dysmorphia.
It remains unclear whether patients with IBD suffer with BID more so than the general population as most studies reported mean values with no reference to healthy population values. Three studies estimated a prevalence of a negative BI based on one question, and this varied between 21% and 81%. This wide variation likely reflects the differences in tools and study characteristics. All three studies were based on self-report questionnaires with a wide age range and registry or hospital-based population.
Certain factors including female gender, disease activity and steroid use were consistently found to be significantly associated with increased BID in patients with IBD. There was also a significant association between increasing BID and decreasing QoL reported in eight studies. These findings are consistent with a previous narrative review 78 assessing BID and sexual functioning in patients with IBD.

strengths and weaknesses of the review
This is the first systematic review assessing BID in an IBD population, and a robust methodology was employed to ensure that bias and errors were minimised. A sensitive search strategy means that it is unlikely that relevant Open access studies were missed and over 50 studies have contributed to the evidence base in an area previously unexplored by a systematic review.
The review has some limitations. Some of the extracted data are based on abstracts only where full texts could not be obtained from the authors. This will have resulted in some missing information.
Furthermore, qualitative studies were not included as this was considered beyond the scope of this review. It is likely that there are qualitative studies which could offer a deeper insight into perception of BI in patients with IBD.
strengths and weaknesses of the evidence There are some weaknesses within the included evidence. All studies had some areas of high risk of bias or had poorly reported methodological criteria, thus hampering quality assessment. Some studies had very low response rates leading to possible under-representation of certain groups. Few studies adjusted for confounders which could have resulted in overestimates of associations.
A further issue is the lack of healthy control groups. Although it appears that patients with IBD are concerned about BI, it is difficult to determine whether they are affected more than the general population. However, it has been found that children and adolescents with chronic illnesses such as asthma, cystic fibrosis and diabetes do have increased BID compared with healthy peers. 79 Non-validated tools were often used for measuring BI and the reliability and validity of findings based on these is therefore unknown. There is also still little known about potential changes in BI perception over time.

Findings in context
This review is consistent with findings from the narrative review by Jedel et al 78 which found that BI could potentially be a problem in patients with IBD. While surgery has been found to be an important contributing factor in BID in other research, 80 it is unclear how it impacts on patients with IBD. An association between BID and poorer QoL has been highlighted in both.
Females and adolescents are more likely to be concerned with BI and to suffer with BID compared with men and older people. [81][82][83][84][85][86] While we found inconsistent results surrounding age, IBD is often diagnosed in adolescence when BID could be more of a concern.
In oncology, BI is more widely researched. One study suggested patients with gynaecological cancer suffered with BID which predicted emotional well-being. 87 Another study with patients with advanced cancer suggested BID was associated with depression, anxiety and fatigue. 88 Qualitative research in pregnancy 89 and systematic lupus 90 suggests BI can affect medication compliance and that patients would like more support around dealing with BI issues. This could also be true for patients with IBD.
Finally, a previous systematic review found that children with chronic conditions were more likely to be dissatisfied with their body than healthy peers. 79 Although patients with IBD were not included, patients with similar chronic diseases like diabetes, cancer, asthma and scoliosis were suggesting patients with IBD could be similarly affected.

Implications
This evidence identified in this review suggests an association between BID and poorer QoL as well as finding factors influencing BI in patients with IBD. There were, however, limitations to the evidence in terms of methodological quality and/or reporting. Also, results were difficult to compare across studies. More promisingly, BI is becoming an increasingly assessed outcome, highlighting the need for continued research in this area.
Current research suggests that age, gender, medication and disease activity in IBD may impact on BI. These could be taken into account by clinicians and patients by altering therapy or targeting comorbidities which could have a beneficial effect on BID. Interventions to improve BI could be incorporated into treatment strategies, which may in turn help to improve QoL. A recent systematic review 91 found that stress management, mindfulness and talking therapies may offer small to moderate improvements in BI; however, there is a lack of evidence from good randomised controlled trials.

Future research
Future research should focus on developing a consensus around which validated tool or tools are best suited to measuring BID in an IBD population. While we describe validity of tools such as the Body Image Scale, we have not independently verified this; therefore, we could not recommend a particular tool. Defining thresholds may allow estimation of the prevalence of BID in this population. Establishing reference values in a healthy population would allow for more meaningful interpretation of BID scores across different chronic diseases. Enrolling patients from diagnosis and following them over time would be useful to measure how BI changes with duration, activity of disease and treatment. While more severe IBD symptoms or invasive treatment options may exacerbate BID, BID itself and any associated anxiety or depressive symptoms may in turn exacerbate IBD symptoms, 92 93 and future research should also address this association. If BID is recognised and treated early, it may contribute to preventing worsening disease course. It may also be useful to encourage the use of BI as a patient-reported outcome in future IBD studies. This would increase data on BID and lead to a greater understanding of the condition.

conclusIon
In conclusion, the evidence suggests a detrimental effect of IBD on BI, but uncertainty remains due a lack of comparison data from healthy populations.

Open access
Associations of BID with disease-related factors such as steroid treatment, fatigue, disease activity and surgery are apparent and findings suggest a correlation between impaired BI and poorer QoL. These results should be cautiously interpreted due to risk of bias and/or poor reporting of methodological criteria among included studies, and the wide variation between populations, BI tools and scoring systems. Future studies should make use of validated measurement tools and include BI as a main outcome where appropriate.
Contributors SEB identified the topic, undertook scoping, defined the question, developed the protocol and wrote the draft of the manuscript. IMH contributed to the methods development and carried out second reviewer tasks as well as helping to draft, comment on and approve the final version of this paper. DM provided substantial methodological input to aid protocol development and assisted with drafting and reading, commenting on approving the final version. JD provided methodological input and read, commented on and edited the draft and approved the final version.
Funding During this research, IMH was funded by a National Institute for Health Research (NIHR) Research Methods-Systematic Review Fellowship and SEB was a locally funded trainee in systematic reviews at the University of Birmingham with agreement from the NIHR.
Disclaimer This article presents independent research funded by the NIHR. The views expressed are those of the authors and not necessarily those of the NHS, the NIHR or the Department of Health.
Competing interests None declared.

Patient consent for publication Not required.
Provenance and peer review Not commissioned; externally peer reviewed.
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