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BMJ Open logoLink to BMJ Open
. 2024 Nov 14;14(11):e088350. doi: 10.1136/bmjopen-2024-088350

Impact of musculoskeletal joint complaints on quality of life in patients with inflammatory bowel disease: a cross-sectional study

Maha Jamal 1,, Maren Karreman 2, Frederieke de Bruijne 1, T Martijn Kuijper 3, J M Hazes 4, Deirisa Lopes Barreto 5, Angelique E Weel 6
PMCID: PMC11575243  PMID: 39542476

Abstract

Abstract

Background

Musculoskeletal joint complaints (MSCs) are the most common extraintestinal manifestation of inflammatory bowel disease (IBD). We aimed to investigate the effect of MSC on the health-related quality of life (QoL) in patients with IBD.

Design

A survey-based cross-sectional study among adult Dutch IBD patients.

Setting

Primary care, secondary care and patient association.

Participants

In total, 635 IBD patients were included. The mean age was 46.3 (SD 14.2) years, and 35% were male.

Outcome

MSC was defined as suffering from any joint complaints. QoL was measured using the IBD questionnaire and a 36-item short form health survey questionnaire.

Methods

A univariate analysis was performed to estimate the impact of various factors, such as demographic characteristics, setting, type of IBD and fatigue, which was followed by a multiple regression analysis to adjust for the confounding factors.

Results

Of the 635 IBD patients, 332 suffered from Crohn’s disease (CD) and 303 from ulcerative colitis (UC). After adjusting for confounding factors, MSC was independently associated with reduced QoL among IBD patients (β=−10.6, 95% CI −15.2 to −6.1), both in CD (β=−8.3, 95% CI −14.6 to −2.1) and UC (β=−13.9, 95% CI −20.5 to −7.3). 11% of the IBD patients had a rheumatological diagnosis. QoL in these patients was significantly lower compared with IBD patients with non-rheumatological MSC.

Conclusions

IBD patients with MSC are associated with a lower QoL, explicitly in patients with a rheumatological diagnosis. Prospective research is necessary to evaluate the causality and suitable interventions to increase QoL in these multimorbid patients.

Keywords: Inflammatory bowel disease, Rheumatology, Patient Reported Outcome Measures, Quality of Life


STRENGTHS AND LIMITATIONS OF THIS STUDY.

  • This study evaluated the relationship between musculoskeletal joint complaints (MSCs) and quality of life (QoL) in several settings.

  • Both generic- and disease-specific questionnaires were used to evaluate the impact of MSCs on QoL and the study had a large sample size.

  • The cross-sectional design of this study limited the interpretation of a causal relation between MSCs and QoL.

Introduction

Inflammatory bowel disease (IBD) is a collective term given to multiple chronic inflammatory diseases of the digestive tract, such as Crohn’s disease (CD) and ulcerative colitis (UC). Worldwide, 6.8 million IBD cases were identified in the year 2017.1 In the Netherlands, the prevalence of IBD is estimated to be 432 per 100 000 patients.2 Musculoskeletal complaints (MSCs) are the most common extraintestinal manifestation and can, in up to 30% of IBD patients, be explained by the rheumatological diagnosis spondyloarthritis (SpA).3,5 Timely detection of SpA within IBD is important, as early treatment can reduce the burden of the disease.

In both IBD and SpA, the burden of disease is high, which is expressed by a lower quality of life (QoL).6 7 QoL is an important health outcome to monitor in patients with IBD and SpA as recommended by the International Consortium for Health Outcomes Measurement.8 9 However, it is less known whether the QoL of IBD patients is affected by SpA itself or via MSC since this disorder also negatively affects QoL.10 As approximately, 70% of all IBD patients with MSC do not develop SpA; we, therefore, aimed to investigate the impact of MSC with and without SpA on QoL in patients with IBD.

Methods

Study design, participants and settings

We used the existing data from the AppSpA study (primary care and patient association population) and a cross-sectional study performed in a secondary care hospital to evaluate QoL in IBD patients. This enabled the integration of different care settings and avoided duplicate data-generating efforts. A survey-based cross-sectional design was performed on Dutch IBD patients aged ≥18 years from secondary care, primary care and the national IBD patient association (Crohn & Colitis Ulcerosa NL).

Patients with IBD from secondary care who were under routine control by the gastroenterologist at the Maasstad Hospital, a large trainee hospital in Rotterdam, the Netherlands, were invited to participate. Patients were selected from the electronic patient file system based on having a UC or CD. Thereafter, all IBD patients received a letter explaining the purpose of the study, informed consent and a set of questionnaires by mail. Patients were included from March 2013 to August 2013.

To explore the relation between MSC and QoL, not only in more complex secondary care IBD patients, we additionally included patients from the AppSpA study,11 which recruited IBD patients from primary care and patient association in almost the same period. This study was approved by the medical ethical committee of the Erasmus University Medical Center (MEC-2014–269). All patients signed an informant consent when they agreed to participate.

The AppSpA study was designed to gain insight into general practitioners’ (GPs’) knowledge about early recognition of SpA and to create more awareness for SpA. Between December 2014 and August 2015, 81 GPs from the Southwest of the Netherlands were recruited to participate in the AppSpA study. GPs selected all IBD patients aged 18–55 years from their databases using International Classification of Primary Care (ICPC) code D94 (ICPC code for IBD, including CD, UC and undifferentiated IBD). ICPC is the standard for coding and classification of signs and symptoms in general practice in the Netherlands.12

Patients from the patient association were invited to participate by e-mail.

Characteristics of study population

Demographic data for all settings were patient reported and included age, gender, diagnosis (CD or UC), disease duration, bowel surgery (yes/no), working status (employed, non-employed and retired), education (low, ≥12 years; intermediate, professional education; and high, bachelor’s or master’s degree), rheumatological diagnoses (reflect any kind of rheumatological condition) and medications (IBD and non-IBD).

Measures

Musculoskeletal complaints

MSCs were defined as suffering from any joint complaints. Patients recruited from secondary care were asked if they suffered from joint complaints (yes or no), while these data were extracted from the arthralgia questionnaire (online supplemental table 1) for patients recruited from the AppSpA study, which included patients from primary care and patient association. Data on rheumatology visits were available for patients in the AppSpA study. Patients were asked if they visited the rheumatologist, and if so, which diagnosis was made.

Health-related QoL questionnaires

Short form-36 (SF-36)

The SF-36 is a 36-item, patient-reported survey of patient health with high validity and reliability.13 It consists of eight domains: vitality, physical functioning, bodily pain, general health perception, physical role functioning, emotional role functioning, social role functioning and mental health. The scales are individually made into a 0–100-point scale. A higher score indicates a higher QoL. The score on all eight separate domains was compared with the scores of the reference population in the Netherlands.14 Patients from the AppSpA study (primary care and patient association) filled out the SF-36v1, whereas patients from the secondary care filled out the SF-36v2. It has been demonstrated that the norm-based scores of the SF-36v2 and SF-36v1 versions are comparable.15 To evaluate whether the difference in SF-36 domains between patients with MSC and patients without MSC is clinically relevant, values for the minimal clinically important difference from Coteur et al were used.16 These values ranged from 3.4 to 8.9 for different domains and were obtained using distribution-based estimates.

Inflammatory bowel disease questionnaire

Both the AppSpA study and secondary care study used IBDQ. The IBDQ is a widely used questionnaire for QoL assessments in patients with IBD.17 18 The IBDQ consists of 32 questions and can be divided into four domains: bowel fatigue (10 questions, score 0–70), systemic fatigue (5 questions, score 0–35), social function (5 questions, score 0–35) and emotional function (12 questions, score 0–84). The answers to the questions range from 1 (worst) to 7 (best). A total score can be calculated as the sum of all 32 items (with a total score range between 0 and 224). The higher the score, the better the QoL. For IBDQ, a clinically meaningful difference was estimated at 16 points.19

Statistical analysis

The baseline characteristics of all patients were described using simple descriptive statistics and were stratified by setting and type IBD. Patients who had missing items’ responses on the IBDQ or SF-36 questionnaire were not included in the analysis. As data on disease activity were not available, we used IBD medications as a proxy. This is a useful alternative for adult non-elderly patients.

To investigate whether the impact of MSC on QoL differs among patients with CD and UC, QoL (IBDQ) was assessed in these patient groups separately. To validate the results, the same analysis was performed using the SF-36 questionnaire as a QoL measure.

A linear regression analysis (adjusted for setting) was used to estimate the association of each variable, that is, MSC, age, gender, type of IBD, disease duration, education, working status, medications (IBD and non-IBD) and fatigue, with IBDQ scores. Variables were chosen based on the available literature.20 21 Then, statistically significant variables were added as a covariate and adjusted for in the multiple regression analyses. The results are presented as beta estimates with 95% CIs. The adjusted R² was extracted from the model. Statistical analysis was performed using Stata (V.15.2). A p value<0.05 was considered statistically significant.

Patient and public involvement

There was no direct involvement of patients and the public in the design, conduct, reporting or dissemination plans of this research.

Results

Participants

In total, 6807 patients were invited: 872 from secondary care, 535 from primary care and 5400 from patient association (figure 1). Of the 872 invited IBD patients in secondary care, 391 agreed to participate (44.8%). Of those, 32 patients (8%) were excluded for returning the questionnaires without signing the informed consent. 19 patients (5%) were excluded on the grounds of disease other than IBD (irritable bowel syndrome and unclassified colitis) or due to follow-up with their GP. Finally, 340 secondary care IBD patients were included. From the 535 primary care patients selected by the GP, 215 (40%) were willing to participate, of whom finally 194 patients (36%) were included. Via the patient association, from the 5400 patients invited, another 110 (2%) IBD patients wanted to participate, of whom finally 101 (2%) were included.

Figure 1. Flowchart of patients with IBD included from (a) secondary care, (b) primary care and (c) patient association. CD, Crohn’s disease; GP, general practitioner; IBD, inflammatory bowel disease; UC, ulcerative colitis.

Figure 1

Characteristics of study population

Table 1 lists the characteristics of all 635 included IBD patients, with a mean age of 46.3 (SD 14.2) years and n=225 (35%) being male. In 11% of the IBD patients, rheumatological diagnoses were present. Among the total 635 patients, 332 (52%) patients suffered from CD, and 303 (48%) patients suffered from UC. Patients differed significantly in characteristics between settings and types.

Table 1. Baseline characteristics.

All IBDsn=635 Primary caren=194 (31%) Patient associationn=101 (16%) Secondary care340 (53%) P value CDn=332 (52.3%) UCn=303 (47.7%) P value
Age (years), mean (SD) 46.3 (14.2) 42.4 (9.5) 41.9 (9.2) 49.8 (16.6) <0.001 45.1 (14.1) 47.6 (14.3) 0.028
Male gender, n (%) 225 (35.4) 56 (28.9) 19 (18.8) 150 (44.1) <0.001 225 (35.4) 410 (64.6) 0.009
Disease duration (years), n (%) 0.043 0.266
 Short (0–2) 113 (17.8) 37 (19.1) 8 (7.9) 68 (20.0) 55 (16.6) 58 (19.1)
 Intermediate (3–10) 203 (32.0) 55 (28.4) 40 (39.6) 108 (31.8) 100 (30.1) 103 (34.0)
 Long (>10) 319 (50.2) 102 (52.6) 53 (52.5) 164 (48.2) 177 (53.3) 142 (46.9)
 Bowel surgery, n (%) 158 (24.9) 53 (27.3) 35 (34.7) 70 (20.6) 0.010 134 (40.4) 24 (7.9) <0.001
 Rheumatological diagnoses, n (%)* 33/295 (11.2%) 15 (7.7%) 18 (17.8%) NA 0.008 23/151* (15.2) 10/144* (6.9) 0.025
Fibromyalgia, n (%) 12/295 (4.1) 5 (2,6) 7 (6.9) NA 0.748 10/151* (6.6) 2/144* (1.4) 0.137
Work status, n (%) <0.001 0.613
 Non-employed 154 (25.2) 41 (22.2) 34 (34) 79 (24.2) 83 (25.9) 71 (24.4)
 Employed 434 (71.0) 144 (77.8) 66 (66) 224 (68.7) 223 (69.7) 211 (72.5)
 Retired 23 (3.8) NA NA 23 (7.1) 14 (4.4) 9 (3.1)
Level of education, n (%) <0.001 0.424
 Low 187 (29.9) 46 (24.7) 6 (6) 135 (39.8) 92 (28.2) 95 (31.8)
 Intermediate 246 (39.4) 77 (41.4) 48 (48) 121 (36.7) 136 (41.7) 110 (36.8)
 High 192 (30.7) 63 (33.9) 46 (46) 83 (24.5) 98 (30.1) 94 (31.4)
Medication IBD, n (%) <0.001 <0.001
 None 126 (19.8) 58 (29.9) 16 (15.8) 52 (15.3) 68 (20.5) 58 (19.1)
 Mesalazine 214 (33.7) 65 (33.5) 34 (33.7) 115 (33.8) 52 (15.7) 162 (53.5)
 Corticosteroids 88 (13.9) 14 (7.2) 13 (12.9) 61 (17.9) 55 (16.6) 33 (10.9)
 Immunosuppressants 178 (28.0) 52 (26.8) 33 (32.7) 93 (27.4) 115 (34.6) 63 (20.8)
 Anti-TNF 104 (16.4) 29 (15.0) 25 (24.8) 50 (14.7) 72 (21.7) 32 (10.6)
 Other (non-IBD) 73 (11.5) 30 (15.5) 18 (17.8) 25 (7.3) 46 (13.9)
*

Data only available for primary care and patient association.

CDCrohn’s diseaseIBDinflammatory bowel diseaseTNFTumor Necrosis FactorUCulcerative colitis

Musculoskeletal complaints

MSC was present in 56% of the patients with IBD. The demographic characteristics of the patients with or without MSC are presented in online supplemental table 2. The percentage of patients with MSC was significantly higher in CD (62%) compared with UC (50%) (p value=0.002). Characteristics of patients with CD were comparable between patients with and without MSC, except that MSC was more prevalent among males. In UC, patients with MSC were older and less educated compared with patients with no MSC.

Quality of life

Table 2 lists QoL as measured by IBDQ. In total, 623 out of 635 patients were analysed, as 12 patients had missing outcomes on IBDQ. The mean IBDQ score, bowel symptoms, systemic symptoms and social and emotional functions were significantly lower in patients with MSC in both CD and UC.

Table 2. Mean scores of the IBDQ between CD and UC patients with and without MSCs.

CD UC
MSCsn=203 (62.9%) No MSCs n=120 (37.2%) P value MSCs n=147 (49.7%) No MSCs n=149 (50.3%) P value
Total score IBD 144.8 (32.4) 155.9 (31.0) 0.003 150.2 (6.3) 169.0 (29.9) <0.001
Bowel symptoms 46.4 (10.2) 49.6 (10.1) 0.008 48.3 (11.7) 52.6 (10.1) 0.001
Systemic symptoms 18.2 (6.1) 21.4 (6.5) <0.001 19.5 (6.2) 24.0 (5.6) <0.001
Social function 24.8 (7.1) 26.5 (6.0) 0.023 26.7 (7.7) 29.4 (5.2) <0.001
Emotional function 51.6 (12.4) 54.4 (11.2) 0.040 52.0 (13.5) 58.7 (11.4) <0.001

Variables are presented as means (SD).

CDCrohn’s diseaseIBDinflammatory bowel diseaseIBDQinflammatory bowel disease questionnaireMSCsmusculoskeletal complaintsUCulcerative colitis

Figure 2a shows that the SF-36 was significantly lower in every domain between IBD patients with and without MSC. A minimal clinically important difference was reached for all domains except for the emotional role limitation and the mental health domain.

Figure 2. Mean scores of the SF-36 questionnaire in (a) IBD with/without MSCs and the Dutch reference population, (b) CD with/without MSC and (c) UC with/without MSC. Error bars indicate the 95% CI. *p value<0.05. **Minimal clinical important difference. BP, bodily pain; CD, Crohn’s disease; GH, general health; IBD, inflammatory bowel disease; MH, mental health; MSCs, musculoskeletal joint complaints; PF, physical function; QoL, quality of life; RE, emotional role limitation; RP, physical role limitation; SF, social function; SF-36, short form-36; VT, vitality; UC, ulcerative colitis.

Figure 2

Patients with no MSC experienced lower QoL in most domains when compared with the Dutch reference population (figure 2a). Figure 2b,c shows QoL measured with the SF-36 questionnaire for subtypes of IBD with and without MSC. Patients with CD and MSC had lower QoL in all domains (p value<0.05) except for the mental health domain (figure 2b). A minimal clinically important difference was reached for the domains of physical functioning, bodily pain and general health perception. Figure 2c shows that UC patients with MSC scored lower on all SF-36 domains (p value<0.05) compared with patients without MSC. A minimal clinically important difference was reached for all domains except emotional role functioning, despite the observed statistical difference.

Online supplemental figure 1 shows the impact of MSC on QoL in different settings. Patients with MSC irrespective of setting had significantly lower QoL compared with patients without MSC. Secondary care patients with and without MSC had significantly lower QoL compared with MSC patients from primary care or patient association.

Additional analysis was performed in IBD patients with rheumatological diagnosis. Patients with rheumatological diagnoses had a mean score of 153.2 (SD 29.6), whereas patients with MSC and no rheumatological diagnoses had a mean total IBDQ score of 164.3 (SD 27.0). The mean difference in QoL between both groups was statistically significant (p=0.037). However, clinical relevance was inconclusive.

Adjusted analysis

The univariate analysis (adjusted for setting) showed that MSC was associated with a statistically significant and clinically meaningful decrease in QoL (β=−17.9, 95% CI −22.6 to −13.1). Fatigue, corticosteroid use and other non-IBD specific medications were associated with reduced QoL, whereas age, higher education, employment, disease-type UC and mesalazine use were positively associated with QoL. Disease duration was not associated with QoL (online supplemental table 3).

After adjusting for significant factors from the univariate analysis, MSC (β=−10.5, 95% CI -15.2 to -6.1) remained statistically significant (table 3).

Table 3. Results of the multivariable analysis with the IBDQ score as the dependent factor and all variables that were significant in the univariate analyses as independent factors (adjusted for setting) for all IBD patients and patients with CD and UC.

All IBDs CD UC
Beta-coefficient 95% CI P value Beta-coefficient 95% CI P value Beta-coefficient 95% CI P value
MSCs −10.5 -15.0 to -6.0 <0.001 −8.3 -14.6 to -2.1 0.009 −13.9 −20.5 to −7.3 <0.001
Age in years 0.28 0.09 to 0.46 0.003 0.34 0.09 to 0.60 0.008 0.20 −0.07 to 0.47 0.149
Gender (female) −4.6 -9.2 to -0.06 0.047 −6.0 −12.5 to 0.57 0.073 −3.5 −9.9 to 3.0 0.291
Type of IBD (UC) 2.3 −2.3 to 6.9 0.320
Fatigue −27.5 -33.6 to -21.4 <0.001 −29.4 -39.2 to -19.6 <0.001 −24.4 -32.2 to -16.5 <0.001
Medications
 Mesalazine 3.4 −1.4 to 8.2 0.164 1.2 −6.9 to 9.3 0.767 4.2 −1.9 to 10.3 0.178
 Corticosteroids −5.3 −11.3 to 0.75 0.086 −1.8 −9.8 to 6.1 0.648 −11.4 -20.9 to -2.1 0.017
 Other (non-IBD) −7.9 -14.3 to -1.4 <0.001 −5.0 −13.4 to 3.4 0.247 −10.8 -21.2 to -0.55 0.039
Employment
 Employed 9.6 4.5 to 14.7 <0.001 8.1 1.0 to 15.3 0.026 9.1 1.6 to 16.6 0.017
 Retired 10.6 −2.11 to 23.2 0.102 12.2 −3.8 to 28.2 0.135 1.3 −20.6 to 23.2 0.906
Education
 Intermediate 4.3 −1.4 to 9.9 0.137 9.5 1.5 to 17.5 0.020 −3.7 −12.0 to 4.6 0.385
 High 6.8 0.63 to 13.0 0.031 10.6 1.7 to 19.5 0.020 1.7 −7.1 to 10.5 0.707

CDCrohn’s diseaseIBDinflammatory bowel diseaseIBDQinflammatory bowel disease questionnaireMSCmusculoskeletal complaintUCulcerative colitis

Similar results were found for patients with CD (β=−8.3, 95% CI −14.6 to −2.1) and UC (β=−13.9, 95% CI −20.5 to −7.3). 26% of the variation in IBDQ was explained by MSC, whereas in total, 42% of the variation was explained by MSC, age, gender, fatigue, education, work status, type of IBD and medications.

Discussion

Our study shows that MSC had an independent reduced effect on QoL irrespective of type IBD patients or setting. This was demonstrated by both the SF-36 and IBD questionnaires. Both the physical and mental domains of the SF-36 were affected in patients with MSC compared with patients without MSC. 11% of the IBD patients received rheumatological diagnoses and QoL in these patients was lower compared with IBD patients with MSC.

Several studies have been performed to evaluate QoL in patients with IBD. However, most studies do not make the distinction between IBD with and without MSC nor for different settings. A study from the Netherlands reported an arthropathy prevalence of 60.1% in IBD patients22 and demonstrated that MSC has a negative impact on the QoL of IBD patients, which is comparable with our study findings. The added value of our study in comparison with the study by van der Have et al is that we investigated and controlled for a broader set of factors, such as age, level of education, work status and type of IBD that may impact the QoL or MSC of IBD patients. In addition, we analysed its impact by setting.

Palm et al reported a low prevalence (16%) of non-inflammatory joint pain, although they only analysed non-inflammatory joint pain among IBD patients who had a shorter disease duration than our study population. Their study reported reduced SF-36 and IBDQ scores.23 Within the same cohort, after a follow-up of 20 years, 40% arthralgia was reported, which was associated with poorer QoL.24 Unlike our study, SpA was not associated with poor QoL. Both studies did not include other disturbing factors that are important in the relation between MSC and QoL, such as work status and education.

Rheumatological diagnosis among IBD patients was reported by the study of van Erp et al.25 Similar to our study, rheumatological diagnosis was made in 12% of the IBD patients.

In this study, only one case of osteoarthritis was reported. Presumably, as the inclusion criteria for patients from primary care and patient association were<45 years, the average age of our study population in all settings was<50 years.

The present study has several strengths: first, our study evaluated the relationship between MSC and QoL in several settings. The added value of including patients from a primary care setting is important in evaluating the impact of MSC in IBD patients because, based on the results, this patient population also suffer from MSC associated with a reduced QoL. Therefore, extra attention should be paid to MSC by the GP. Second, we included both the SF-36 and IBDQ to evaluate QoL. Therefore, we were able to confirm the impact of MSC on QoL on both the generic- and disease-specific questionnaires. This may have an impact on its use in daily care. Third, this is the first study that investigated multimorbidity in relation to QoL in different settings. This study indicates that assessing the effect of morbidities and setting is crucial for the interpretation of outcomes on QoL.

Finally, we had a large sample size where the degree of missing data was minor, resulting in a patient exclusion rate of less than 2%. Moreover, we selected IBD patients from various GP databases, resulting in an adequate representation of the general IBD population from various regions of the Netherlands, which may have increased the accuracy of our data.

This study also has some limitations. First, we performed a cross-sectional study, which limited the interpretation of a causal relation between MSC and QoL. However, since other studies show the same associations, our findings underline the need for MSC management of IBD patients in both primary and secondary care. Second, we could not verify whether primary care and patient association were seen by secondary care specialist; therefore, the impact of MSC on QoL might have been an underestimation. Third, information on IBD disease activity was not available. Therefore, we could not investigate whether disease activity is a confounding variable in the relationship between MSC and QoL. However, as in the previous studies, medications were used as a proxy for disease activity26 27 for which we controlled for in the analyses. We believe that, in adult non-elderly patients, as in our study population, the use of medication as a proxy for disease activity is a useful alternative. However, in elderly patients, this could be misleading due to polypharmacy and multimorbidities.27 Fourth, the data on comorbidities other than rheumatological diagnosis were not collected explicitly. However, this was controlled for in the analysis by adjusting for non-IBD medication use. Finally, although we did not perform sample size calculation, our sample size was large and representative of the population, which makes our findings valuable.

Conclusions

MSC has a significant independent negative impact on the QoL of patients irrespective of the type of IBD or setting. This was most obvious in patients having both IBD and a rheumatological disease. This might have clinical consequences for the gastroenterologists, GPs and rheumatologists. We, therefore, recommend routinely administering a questionnaire investigating MSC, such as the one used by van Erp et al25 prior or during hospital or GP visit, as this is currently often not performed in clinical practice. In addition, we suggest to incorporate referral strategies in international guidelines for gastroenterologists and GPs for patients at risk for inflammatory rheumatic diseases.

supplementary material

online supplemental file 1
bmjopen-14-11-s001.pdf (619.2KB, pdf)
DOI: 10.1136/bmjopen-2024-088350

Acknowledgements

We would like to thank all general practitioners, the national patient association (Crohn & Colitis Ulcerosa NL) and all patients for participating in this study. Additionally, we thank Alex van Geel for his contribution in data entry and cleaning.

Footnotes

Funding: The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.

Prepublication history and additional supplemental material for this paper are available online. To view these files, please visit the journal online (https://doi.org/10.1136/bmjopen-2024-088350).

Provenance and peer review: Not commissioned; externally peer reviewed.

Patient consent for publication: Not applicable.

Ethics approval: This study involves human participants and was approved by the medical ethical committee of the Maasstad Ziekenhuis in Rotterdam and Erasmus University Medical Center (MEC-2014-269). Participants gave informed consent to participate in the study before taking part.

Patient and public involvement: Patients and/or the public were not involved in the design, conduct, reporting or dissemination plans of this research.

Contributor Information

Maha Jamal, Email: AbdelkadirM@maasstadziekenhuis.nl.

Maren Karreman, Email: m.hof-karreman@erasmusmc.nl.

Frederieke de Bruijne, Email: BruijneF@maasstadziekenhuis.nl.

T. Martijn Kuijper, Email: kuijpert@maasstadziekenhuis.nl.

J M Hazes, Email: j.hazes@erasmusmc.nl.

Deirisa Lopes Barreto, Email: LopesBarretoD@maasstadziekenhuis.nl.

Angelique E Weel, Email: weela@maasstadziekenhuis.nl.

Data availability statement

Data are available upon reasonable request. All data relevant to the study are included in the article or uploaded as supplementary information.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

online supplemental file 1
bmjopen-14-11-s001.pdf (619.2KB, pdf)
DOI: 10.1136/bmjopen-2024-088350

Data Availability Statement

Data are available upon reasonable request. All data relevant to the study are included in the article or uploaded as supplementary information.


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