Keywords IBD - Nutrition and metabolism - patient-reported outcome measures (PROMS) - Inflammatory
bowel disease - Quality of life
Schlüsselwörter CED - Ernährung und Stoffwechsel - Patient Reported Outcomes (PRO) - Chronisch entzündliche
Darmerkrankungen - Lebensqualität
Introduction
Inflammatory bowel disease (IBD), in particular the two main clinical phenotypes,
ulcerative colitis (UC) and Crohn’s disease (CD), are characterized by recurrent,
chronic inflammation of the gastrointestinal tract. IBD behavior seems to be closely
linked to nutrition with the latest research indicating that diet and nutrition are
significantly involved in the etiopathogenesis of the disease, although their specific
role throughout its clinical course remains unclear [1 ]
[2 ]. In addition, patient reports show a subjective connection between disease behavior
and nutrition [3 ]
[4 ], while IBD related quality of life seems to be connected to patients’ dietary behavior
[5 ]. Along with a perceived treatment frustration some patients hence turn to online
advice and to extreme nutritional measures [6 ]. In fact, in patients with IBD, there are many drivers for dietary change that are
also considered risk factors for disordered eating – with IBD patients exhibiting
many of the confounding traits commonly seen in patients with eating disorders, including
anxiety, depression, self-initiated diets, poor body image and/or shame (particularly
those with ostomy) [7 ]
[8 ]. It is known from the general population that quality of life (QoL) can be associated
with food and nutrition [9 ]
[10 ]. In addition, previous studies show that this is in particular true in possible
food-triggered disease such as celiac disease or food-based allergies [11 ]
[12 ]. Consequently, the latest research is now focusing on IBD food-related QoL [13 ]. However, to identify possible needs for physician-intervention validated patient
reported outcome measures (PROMs) assessing food related quality of life are needed.
The FR-QoL-29 was developed based on qualitative interviews [14 ] and is a validated PROM that queries self-imposed dietary restrictions as well as
impairments in daily life due to eating and drinking [15 ] and has successfully been used in English-speaking countries. Subsequently, it has
already been translated and validated into Turkish [16 ] and Portuguese [17 ]. Meanwhile, there is no comparable validated tool in the German-speaking area. However,
German-speaking patients and healthcare providers would truly benefit from this tool
in both research and clinical practice.
Materials and methods
Ethical considerations
This monocentric study was approved by the ethics committee of Hannover Medical School
(10847_BO_S_2023), registered at the German Clinical Trial Register (DRKS) as DRKS00032771
and the study design is in accordance with the Declaration of Helsinki (2013).
Participants and setting
Between October 2023 and August 2024, a total of 200 IBD patients as well as 10 healthy
controls were enrolled at the IBD outpatient clinic of Hannover Medical School. Prior
to study inclusion, each patient was required to provide written informed consent.
Eligibility criteria for study inclusion were a confirmed diagnosis of either UC or
CD and disease duration of at least three months. Individuals with any disorders that
preclude the assessment of the nature, scope, and potential consequences of the study
were excluded.
Data sources/measurements
All individuals who gave informed written consent were asked to complete an online
demographic survey including data on sex and gender identity, body status (weight,
height), age, marital status, employment status, and more. The survey included further
questions pertaining to IBD-specific history, therapies, surgical history, and comorbidities.
The degree of disease activity was determined in investigator-led interviews using
either the German version of the Harvey-Bradshaw Index (HBI) [18 ] for CD patients or the German version of the partial Mayo score (PMS) [19 ] for those with UC. The extent of the disease was determined using the Montreal Classification
for patients with CD and the anatomic extent for patients with UC [20 ].
FR-QoL-29-German
The FR-QoL-29 was translated into German with explicit permission granted by the copyright
holders (Prof. Kevin Whelan, King’s College London). The questionnaire was translated
via the forward-backward translation method [21 ] taking into account the special context of a cross-cultural adaptation [22 ]
[23 ], which saw two translators who are fluent in English translate the questionnaire
independent from each other. Both translations were then reviewed, and any discrepancies
were resolved jointly by the research team, consisting of gastroenterologists, IBD
experts, nutritionists, a linguist and the translators. The questionnaire was then
translated back into English by a native English speaker who was fluent in German,
not familiar with the English version, and not affiliated with the research team.
A Pre-test was conducted with five IBD patients who, after having completed the translated
questionnaires, were asked to evaluate the FR-Qol-29-German version in investigator-led
interviews. Based on this feedback the research team finalized the FR-Qol-29-German
version. The original questionnaire, as well as the German version, consists of 29
statements on food-related quality of life in the last two weeks. For each statement,
one of five possible scored answers can be chosen, ranging from Strongly agree (1) to Strongly disagree (5) . Statements 8, 9, 24 and 25 are expressed in the positive, therefore the corresponding
answers must be inverted when evaluating the questionnaire. Overall, the FR-QoL-29
score ranges from 29 to 145, with 145 indicating a good IBD food-related quality of
life [15 ].
Malnutrition Universal Screening Tool
The German version of the Malnutrition Universal Screening Tool (MUST) was used to
identify adult individuals with potential risks of malnutrition [24 ]
[25 ]. The MUST scoring is based on three areas: a) body mass index, b) unplanned weight
loss within the last 3 to 6 months, c) acute illness with an expected food abstinence
of at least five days. A maximum of 2 points can be awarded per area and a total of
0 to 6 points can be scored, with 0 points indicating a low risk and anything above
two points suggesting a high individual risk of malnutrition.
Short Health Scale
The validated German version of the Short Health Scale (SHS) [26 ] was used to assess the current IBD-related health status via four questions about
symptoms, daily activities, disease-related concerns, and general well-being over
the past seven days. Evaluation of all four domains allows for a maximum score of
400 points with higher scores indicating poorer health-related quality of life for
individuals with IBD.
Disease activity
Disease activity and remission were determined using entity-specific disease activity
index cutoffs. For binary disease activity assessment remission was defined as a Harvey-Bradshaw
Index (HBI) of <5 [18 ] or a partial mayo score (PMS) of 0–1 [19 ], respectively.
Statistical analyses
For statistical analysis SPSS Statistics software, version 28.0.1.0 (SPSS, IBM, Armonk,
NY), and GraphPad PRISM, version 10.3.0 (GraphPad Software, Boston, Massachusetts,
USA) were employed. Normal distribution was assessed via Shapiro-Wilk test. Categorical
baseline variables are expressed as total and percentage. Significance levels are
two-sided if not mentioned otherwise, and when applicable clinical relevance is reported
as effect size estimate (d).
Validity
Content validity of the translated FR-QoL-29-German items was assessed based on the
expert judgment method [27 ] as well as the investigator-led pre-test interviews. Meanwhile, to assess construct
validity, we demonstrated convergent and discriminant validity via hypothesize testing
and exploratory factor analysis (EFA). We hypothesized a negative correlation between
FR-QoL-29-German and a) health-related QoL in IBD individuals measured by SHS, and
b) malnutrition risk score measured by MUST. We further hypothesized that we would
see significant differences in FR-QoL-29-German scores for individuals in remission
compared to those with an active disease, in addition we proposed that the Fr-QoL-29-German
discriminates between IBD patients and healthy controls. For hypothesis testing we
used student’s t-test and ANOVA for comparisons of the FR-QoL-29-German score between
groups, and Pearson correlation coefficient to assess correlation between IBD health-related
quality of life with IBD food-related quality of life. Data adequacy for factor analysis
was assessed via Kaiser-Meyer-Olkin (KMO) test and Bartlett’s test of sphericity.
Reliability
Internal consistency for the FR-QoL-29-German was assessed via Cronbach’s α while
the reliability of the translated questionnaire was investigated by inviting all study
subjects to complete a follow-up questionnaire, with n=113 completing the follow-up
questionnaire before data analysis cutoff. Pearson correlation coefficient and intraclass
correlation coefficient (ICC) for FR-QoL-29-German scores were used to assess test-retest
reliability. On average the follow-up questionnaire was completed 6 weeks after study
inclusion. Testing conditions for the FU-Questionnaire did not differ from the initial
run as both the baseline survey as well as the follow-up questionnaire were conducted
online. Patients with major changes in symptom characteristics (n=6) were excluded
from the follow up analysis. As an additional quality criterion, we tested for possible
ceiling and floor effect of the FR-QoL-29-German [28 ].
Sampling strategy
To eliminate distortion when comparing FR-QoL-29-German scores of IBD patients with
those of healthy controls a random sample of the IBD cohort was drawn that matched
the healthy control cohort in a ratio of 4:1.
Results
Study population
A total of 200 IBD patients were included in this study. In total, n=113 patients
completed the FU questionnaire excluding those who had major changes in symptom characteristics
since baseline (n=6). Baseline characteristics showed a skewed distribution of disease
entities (Crohn’s disease 61.8%), but a balanced distribution of sex (women: 50.8%)
and dichotomous remission status (remission: 56.2%). Overall, 45% of patients reported
having received nutritional counseling at least once in the past due to IBD. Patients
had a mean age of 40 years and a mean BMI of 25.25 kg/m2 ([Table 1 ]). For hypothesis-testing we matched a random IBD sample (n=40) to healthy controls
(n=10; women = 60%; age = 36±5).
Table 1 Baseline characteristics. Variables are expressed as total and percentage (n[%]) or
mean and standard deviation (M±SD). MUST – Malnutrition Universal Screening Tool;
BMI – Body Mass Index; UC – Ulcerative Colitis.
Baseline
(n=200)
Demographics [Mean±SD or n(%)]
Disease entity
Crohn’s disease
123 (61.8%)
Ulcerative colitis
76 (38.2%)
Female
101 (50.8%)
Disease Activity
Remission
104 (56.2%)
Mild Disease
46 (24.9%)
Moderate Disease
28 (15.1%)
Severe Disease
7 (3.8%)
Location of Crohn’s
L1
35 (28.2%)
L2
21 (16.9%)
L3
67 (54%)
L4
13 (10.5%)
Crohn’s behavior
B1
46 (37.1%)
B2
54 (43.5%)
B3
24 (19.4%)
perianal disease
33 (26.6%)
UC Montreal classification
Proctitis
5 (6.6%)
Left-sided colitis
26 (34.2%)
Pancolitis
45 (59.2%)
MUST
Low Risk
114 (57%)
Medium Risk
40 (20%)
High Risk
46 (23%)
Disease duration in years
14±10
Nutritional counselling in the past due to IBD
90 (45%)
FR-QoL-29-German score
84±22
Short Health Scale score
179±114
Gastrointestinal surgery
66 (34%)
BMI (kg/m2 )
25.25±5.48
Age (years)
40±14
Smoking status (current or former)
73 (36.7%)
Calprotectin (mg/kg)
740.47±1727.6
C-reactive protein (mg/l)
5.98±13.18
Translation and cross-cultural adaptation
The translation and subsequently cross-cultural adaptation process of the FR-QoL-29-German
consisted of several steps and was at least partially carried out blind. Despite changes
in sentence structure as well as the use of cultural appropriate synonyms of selected
words, the final translation is in effect analogues to the original. However, similar
to the FR-QoL-29-Portuguese [17 ], the labeling of the Likert scale was also discussed in the German translation and
no literal translation was chosen for Strongly agree (1) and Strongly disagree (5) , but rather the German expression Stimme voll und ganz zu (1) (English translation: Completely agree (1) ) and Stimme überhaupt nicht zu (English translation: Do not agree at all (5) ), which are frequently used in German standardized questionnaires.
Validity
Requirement for factor analysis was satisfied with the inclusion of at least 145 enrolled
patients which was further confirmed by the results of the Kaiser-Maier-Olkin test
(0.95). Furthermore, Bartlett’s test of sphericity was significant (χ2 = 4423; p <0.001)
thus indicating that the data is suitable for exploratory factor analysis (EFA). EFA
identified four factors with an eigenvalue > 1 that accounted for a total variance
of 65.63 %. However, a total of 51.41% of the variance was attributable to factor
1, therefore only factor 1 was retained ([Table 2 ]). This is in accordance with the FR-QoL-29 [15 ] as well as the FR-QoL-29-Turkish [16 ]. Hypothesis-testing for the hypotheses formulated in advance showed a negative correlation
between FR-QoL-29-german score and a) SHS score (r = −0.502; p <0.001), and b) MUST
score (r = −0.172; p = 0.008). Patients in remission scored significantly higher on
the FR-QoL-29-German than patients with an active disease (p<0.001, d = 0.6). Bonferroni
post-hoc test of one-way ANOVA revealed statistical significances of FR-QoL-29-German
scoring between all entity-specific gradations of disease activity except for remission
– mild disease (p = 0.423), and moderate disease – severe disease (p = 0.999) ([Fig. 1 ]). One-tailed student’s t-test of FR-QoL-29-German score between healthy controls
(n=10) and a matched random IBD sample (n=40) was statistically significant (p = 0.005;
d = −1.4) ([Fig. 2 ]). There was no statistically significant difference in FR-QoL-29-German score between
disease entities (p = 0.198; d = −0.2). Correlation of demographic, health and disease-specific
factors saw a positive correlation between FR-QoL-29-German score and age (r = 0.145;
p = 0.041) as well as inverse correlations for disease activity (r = −0.303; p <0.001),
MUST score (r = −0.172; p = 0.015), SHS score (r = −0.502; p <0.001), and fecal calprotectin
mg/kg (r = −0.204; p = 0.011) ([Table 3 ]). No ceiling or floor effect was apparent as out of 200 individuals with IBD only
one (0.5%) scored 29 points thus indicating a very poor food-related quality of life,
while one individual (0.5%) achieved the highest score of 145.
Table 2 Exploratory factor analysis for items of the German version of the FR-QoL-29.
FR-QoL-29-German item
Question
Factor 1
1
I have regretted eating and drinking things which have made my IBD symptoms worse
0.675
2
My enjoyment of a particular food or drink has been affected by the knowledge that
it might trigger my IBD symptoms
0.621
3
My IBD has meant that I have had to leave the table while I am eating to go to the
toilet
0.664
4
I have not been able to predict how long it will take for my body to respond to something
I have had to eat or drink due to my IBD
0.740
5
Certain foods have triggered symptoms of my IBD
0.631
6
My IBD has meant that I have been nervous that if I eat something I will need to go
to the toilet straight away
0.750
7
I have avoided having food and drink I know does not agree with my IBD
0.613
8
I have felt relaxed about what I can eat and drink despite my IBD
0.692
9
I have felt in control of what I eat and drink in relation to my IBD
0.585
10
I have struggled to eat the way that is best for my IBD because of other commitments
during the day
0.544
11
I have been frustrated about not knowing how food and drink will react with my IBD
0.777
12
I have had to concentrate on what I have been eating and drinking because of my IBD
0.833
13
I have been worried that if I eat I will get symptoms of my IBD
0.846
14
I have felt the way that I eat and drink for my IBD has affected my day to day life
0.855
15
The way I have had to eat for my IBD has restricted my lifestyle
0.827
16
I have had to concentrate on what food I buy because of my IBD
0.751
17
It has been on my mind how my IBD will be affected by what I eat and drink
0.706
18
My IBD has prevented me from getting full pleasure from the food and drink I have
had
0.805
19
I have felt that I need to know what is in the food I am eating due to my IBD
0.587
20
I have felt that I have had to be careful about when I have eaten because of my IBD
0.818
21
I have had to be more aware of what I am eating due to my IBD
0.771
22
I have missed being able to eat or drink whatever I want because of my IBD
0.872
23
I have felt that I would like to be able to eat and drink like everyone else
0.757
24
I have been happy to eat and drink around people I do not know despite my IBD
0.455
25
I have felt that I have been eating and drinking normally despite my IBD
0.615
26
I have found it hard not knowing if a certain food will trigger IBD symptoms
0.684
27
My IBD has meant I have had to make an effort to get all the nutrients my body needs
0.637
28
I have felt that I have not known how my IBD will react to food or drink
0.711
29
My IBD has meant that I have had to work hard to fit my eating habits in around my
activities during the day
0.760
Eigenvalue
14.90
% of Variance
51.41
Fig. 1 Comparison of FR-QoL-29-German score between entity-specific disease activity. Bonferroni
correction of one-way ANOVA showed statistically significances of mean FR-QoL-29-German
score between remission and severe disease (p < 0.001); remission and moderate disease
(p < 0.001); mild and moderate disease (p = 0.035); mild and severe disease (p = 0.021).
Fig. 2 Matched comparison of FR-QoL-29-German score between healthy controls and IBD patients.
Student’s t-test showed statistically significances of mean FR-QoL-29-German score
between healthy controls and a matched subsample of IBD patients (p = 0.005; d = −1.4).
HC – healthy controls; IBD – inflammatory bowel disease.
Table 3 Correlation of demographic, health and disease-specific factors with the FR-QoL-29-German
score. BMI – Body Mass Index; MUST – Malnutrition Universal Screening Tool; SHS –
Short Health Scale.
Correlation factors
Pearson correlation (r)
p
Age
0.145
0.041
Sex
0.125
0.078
BMI
0.072
0.313
Entity
0.093
0.189
Disease activity
−0.303
<0.001
MUST
−0.172
0.015
SHS
−0.502
<0.001
Calprotectin mg/kg
−0.204
0.011
Reliability
Internal consistency was high with a Cronbach’s α coefficient of 0.965, in addition
Cronbach’s α coefficient ranged from 0.962 to 0.966 if individual items were deleted.
Pearson correlation coefficient showed good test-retest reliability between the initial
FR-QoL-29-German score and the follow up FR-QoL-29-German score (r = 0.734, p <0.001)
as did the calculated intraclass correlation coefficient of 0.85 [95% CI: 0.78; 0.89].
Single item correlation between initial and follow up timepoint were significant for
all FR-QoL-29-German items (p<0.001) ([Table 4 ]).
Table 4 Results for internal consistency analysis and test-retest reliability.
FR-QoL-29-German item
Corrected-item-total score correlation
Cronbach’s Alpha if item deleted
Test-retest reliability
1
0.658
0.964
0.574*
2
0.600
0.964
0.440*
3
0.641
0.964
0.508*
4
0.723
0.963
0.440*
5
0.613
0.964
0.490*
6
0.728
0.963
0.656*
7
0.589
0.964
0.550*
8
0.643
0.964
0.530*
9
0.532
0.965
0.508*
10
0.523
0.965
0.508*
11
0.757
0.963
0.542*
12
0.818
0.963
0.580*
13
0.830
0.963
0.584*
14
0.838
0.963
0.714*
15
0.807
0.963
0.638*
16
0.730
0.963
0.577*
17
0.683
0.964
0.526*
18
0.787
0.963
0.647*
19
0.561
0.965
0.599*
20
0.799
0.963
0.640*
21
0.749
0.963
0.527*
22
0.856
0.962
0.694*
23
0.734
0.963
0.515*
24
0.406
0.966
0.443*
25
0.560
0.965
0.543*
26
0.659
0.964
0.329*
27
0.612
0.964
0.478*
28
0.686
0.964
0.424*
29
0.737
0.963
0.405*
No of Items
29
Cronbachs Alpha
0.965
Intraclass correlation coefficient [95% CI]
0.85 [95%CI: 0.78; 0.89]
Discussion
The present study introduces a novel German translation of the FR-QoL-29, which has
been developed for the systematic assessment of food-related quality of life in patients
with IBD. Psychological distress and restricted food intake are associated with poorer
health-related quality of life in IBD and other gastrointestinal diseases. However,
in IBD, less is known about the relationship between mental health, restricted food
intake, and food-related quality of life (FR-QoL), which directly measures the psychosocial
impact of eating and drinking [14 ]
[29 ]
[30 ]. Patients with IBD report that nutrition is the most important psychosocial need
affected by IBD [29 ]
[30 ]
[31 ]. Furthermore, food and diet are primary behavioral factors that can be used to help
patients control the disease and symptoms [32 ]
[33 ]
[34 ]. However, because the role of diet and specific food components in disease development
and pathogenesis remains unclear and the evidence base for nutritional therapies is
limited, nutritional counseling is often inadequate [2 ]
[35 ]
[36 ]. The FR-QoL-29 is an important patient reported outcome measure (PROM) and invaluable
in assessing food-related quality of life for IBD patients in terms of psychosocial
factors. IBD-specific nutritional strategies in order to avoid a flare-up may be restricting
or excluding certain foods. However, disease-related restrictive eating can be isolating,
burdensome on everyday life, and exacerbate a decrease in mental health. Indeed, variations
in eating behavior is not uncommon in IBD patients as fear of symptoms from eating
is one major issue and studies have further shown that IBD patients are at high risk
for disordered eating [37 ]
[38 ]. Our study has revealed a concerning percentage of individuals with a medium (20%)
and high risk (23%) of malnutrition, which could exacerbate disease development [39 ]. The need for measures such as the FR-QoL-29 is therefore evident, however so far
there has been no validated German translation. Using the forward-backward translation
method [21 ] we subsequently assessed validity and reliability of the German translation of the
FR-QoL-29 in an ongoing single-center cohort-study. Internal consistency of the FR-QoL-29-German
was excellent with a Cronbach’s α coefficient of 0.965 and thus similar to the FR-QoL-29
(Cronbach’s α coefficient 0.959) [15 ], the FR-QoL-29-Turkish (Cronbach’s α coefficient 0.96) [16 ], and FR-QoL-29-Portuguese (Cronbach’s α coefficient 0.966) [17 ]. No items were excluded since Cronbach’s α coefficient was never higher than 0.966
after individual item deletion. By comparing the IBD sum score with the HC sum score,
good discriminant validity was demonstrated. In addition, it was shown that the total
score differs significantly between entity-specific gradations of disease activity,
this is in accordance with the original publication. Consequently, when considered
collectively, the FR-QoL-29 has been demonstrated to be consistent with health-related
quality of life and disease activity surrogates in IBD.
We acknowledge that this study has certain limitations, including its monocentric
design within a tertiary referral center, which may have introduced a degree of selection
bias. Another potential limitation is the outpatient setting. It would be beneficial
for future research to include hospitalized IBD patients with severe disease activity,
in order to gain further insight into the deterioration in food-related quality of
life in this distinct setting. In the present study, only seven patients with severe
disease activity were included. However, as the majority of IBD patients are treated
within an outpatient setting, this study represents a “real world cohort”. The present
study has additional notable strengths. Firstly, the sample size of IBD patients was
large and diverse. Secondly, the inclusion of healthy controls allowed for a more
comprehensive comparison of the instrument’s performance.
In conclusion, the results of this study demonstrate that the FR-QoL-29-German is
a valid and reliable tool for the assessment of food-related quality of life in German-speaking
IBD patients. As there is an increasing body of evidence indicating a close relation
between IBD and nutrition, a specific measure of the psychosocial aspects of eating
and drinking in IBD enables physicians and other health-workers to assess the disease
impact on patients’ food-related quality of life in a standardized way. This provides
further insight into the significant impact of IBD on the daily lives of individuals.
Further research is required to elucidate the explicit role and connection between
patients’ food-related quality of life and the course of their IBD disease e. g. in
terms of therapy-response or disease complications. We hereby present a tool for the
systematic measurement of this aspect in German-speaking IBD patients.
