Clin Nutr Res.
2018 Jan;7(1):48-55
https://doi.org/10.7762/cnr.2018.7.1.48
pISSN 2287-3732·eISSN 2287-3740 CLINICAL NUTRITION RESEARCH
Original Article Food Elimination Diet and Nutritional
Deficiency in Patients with
Inflammatory Bowel Disease
Hee-Sook Lim ,1 Soon-Kyung Kim ,2 Su-Jin Hong 3
1
Department of Food Sciences and Nutrition, Yeonsung University, Anyang 14011, Korea
2
Department of Food Sciences and Nutrition, Soonchunhyang University, Asan 31538, Korea
Digestive Disease Center and Research Institute, Department of Internal Medicine, Soonchunhyang
3
University College of Medicine, Bucheon 14584, Korea
Received: Dec 29, 2017
Revised: Jan 20, 2018
ABSTRACT
Accepted: Jan 20, 2018 Certain types of foods are common trigger for bowel symptoms such as abdominal
Correspondence to discomfort or pain in patients with inflammatory bowel disease (IBD). But indiscriminate
Soon-Kyung Kim food exclusions from their diet can lead extensive nutritional deficiencies. The aim of
Department of Food Sciences and Nutrition, this study was to investigate nutritional status, food restriction and nutrient intake status
Soonchunhyang University, in IBD patients. A total 104 patients (food exclusion group: n = 49; food non-exclusion
22 Soonchunhyang-ro, Sinchang-myeon,
group: n = 55) participated in the survey. The contents were examined by 3 categories: 1)
Asan 31538, Korea.
E-mail: soon56@sch.ac.kr anthropometric and nutritional status; 2) diet beliefs and food restriction; and 3) nutrient
intake. The malnutrition rate was significantly higher in the food exclusion group (p = 0.007)
Copyright © 2018. The Korean Society of compared to food non-exclusion group. Fifty-nine percent of patients in the food exclusion
Clinical Nutrition
group held dietary beliefs and reported modifying their intake according to their dietary
This is an Open Access article distributed
under the terms of the Creative Commons
belief. The most common restricted food was milk, dairy products (32.7%), raw fish (24.5%),
Attribution Non-Commercial License (https:// deep-spicy foods (22.4%), and ramen (18.4%). The mean daily intake of calcium (p = 0.002),
creativecommons.org/licenses/by-nc/4.0/) vitamin A (p < 0.001), and zinc (p = 0.001) were significantly lower in the food exclusion
which permits unrestricted non-commercial group. Considering malnutrition in IBD patients, nutrition education by trained dietitians
use, distribution, and reproduction in any is necessary for the patients to acquire disease-related knowledge and overall balanced
medium, provided the original work is properly
nutrition as part of strategies in treating and preventing nutrition deficiencies.
cited.
ORCID iDs Keywords: Inflammatory bowel diseases; Malnutrition; Attitude to health; Food intolerance
Hee-Sook Lim
https://orcid.org/0000-0003-0745-8906
Soon-Kyung Kim
https://orcid.org/0000-0001-9057-0792 INTRODUCTION
Su-Jin Hong
https://orcid.org/0000-0003-2012-0360 Inflammatory bowel disease (IBD) is a chronic idiopathic inflammatory disease that is
represented by ulcerative colitis and Crohn's disease. IBD is caused by a combination of
Funding
This work was supported by the
genetic and environmental factors and the patients suffer from nausea, vomiting, loss
Soonchunhyang University Research Fund. of appetite, headaches, and diarrhea during treatment [1]. Moreover, it is reported that
maintaining a good working status or daily life is difficult for the patients because of repeated
Conflict of Interest
relapse of their works. Such situation can lead anxiety, depression, or feeling of socially
The authors declare that they have no
competing interests.
isolated in patients and compromise their quality of life [2,3]. The incidence of IBD due to
dietary factors has increased specifically in patients with an increase in fat and protein intake
This paper was presented to the Korean and the lack of fruits and vegetables intake from the diet [4]. Studies have shown that when
Society of Clinical Nutrition in 2015 and was high levels of linoleic acid are consumed, a high intake of red and processed meat increases
awarded the Best Poster Award.
the risk of developing ulcerative colitis as well as relapse. The association between food
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Food Elimination Diet in IBD Patients CLINICAL NUTRITION RESEARCH
intake patterns and changes in intestinal bacteria has been emphasized in several studies [5-
7]. Ulcerative colitis and Crohn's disease are associated with a 20%–75% loss of body weight
and electrolyte imbalance [8]. Various factors are involved in causing nutritional deficiencies
in individuals with IBD, including decreased oral intakes, metabolic disorders, increased
nutritional requirements, drug interactions, and malabsorption [9]. In addition, nutritional
disorders can occur due to prolonged periods and indiscriminate manner of food restriction
for reducing discomfort from IBD symptoms.
Thus, nutrition goals for patients with IBD need to be coordinated so that patients can better
manage themselves with the aim of maintaining or improving a balanced nutritional status
through appropriate provision of nutrients according to their treatment conditions [10].
However, nutrition studies conducted for Korean patients with IBD are very rare. This study
was performed to assess the nutritional status of patients with IBD and to analyze whether
the diet or nutritional imbalance varies depending on food restriction. Our findings will serve
basic data to future clinical nutrition research for IBD patients.
MATERIALS AND METHODS
Study subjects
The study subjects were patients with confirmed IBD who visited the digestive division of
Soonchunhyang University Hospital in Gyeonggi-do. The first 112 patients participated but
only the final 104 results were used for the study; results from 8 patients were excluded due
to denial or missing data. The participants were fully informed of the purpose, need, and
method of this study and asked for their consent. The research design and protocol were
approved by Institutional Review Board of Soonchunhyang University (approval number:
2015-BM-002-01). Based on the study purpose, the subjects were classified into 2 groups
(food exclusion group, n = 49; food non-exclusion group, n = 55) through interviews with a
clinical dietitian.
Variable measurements and definitions
Subjects' body mass index (BMI) was calculated using height and weight. We obtained data
about the disease diagnosis period (< 1, 1–3, ≥ 3 years) and IBD classification (Crohn's disease
or ulcerative colitis). Disease activity reflected the medical record information as well as
confirmation from the physician. The patients' nutritional status was assessed by a clinical
dietitian using a subjective global assessment method and nutritional status was classified as
adequate, mild or moderate malnutrition, or severe malnutrition.
After the diagnosis, beliefs and attitude related to the patients' usual diet were investigated.
The questions were based on previous research journal and were reviewed by the researchers
[11,12]. ‘Do you think you are important to meals in the beginning and during the period
of IBD diagnosis?’, ‘Do you have a dietary modification?’, ‘Do you think that diet could play
a role in causing disease relapse?’, ‘Do you think you should avoid food to prevent disease
relapse?’, ‘In case of relapse, what diet do you believe can improve disease symptoms?’, ‘Do
you received nutrition education and management?’, ‘Do you want a nutritional education
and professional management?’ Dietary habits assessed were about drinking, smoking,
exercise, regularity of meals, eating speed, and frequency of eating out. In order to examine
the degree of restriction of food intake, a questionnaire was analyzed for a list of foods that
are usually restricted in the diet. In order to evaluate nutrient intake, 3-day food record
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Food Elimination Diet in IBD Patients CLINICAL NUTRITION RESEARCH
method was conducted and the data was analyzed using the computer-aided nutritional
analysis program (CAN-Pro 4.0; Korean Nutrition Society, Seoul, Korea).
Statistics analysis
Statistical processing and analysis for all data collected from the investigation were
performed by using the SPSS program (ver. 18.0; SPSS Inc., Chicago, IL, USA). To identify
factors differing between the groups, the independent t-test was used for continuous
variables including nutrient factors and the equal-variance, χ2 test, or Fisher's exact test for
categorical variables. For all analyses, p < 0.050 was considered statistically significant.
RESULTS
The characteristics of the 104 patients can be found in Table 1. The total number of subjects
in the food exclusion group was 49 (47.1%) and the mean age was 39.4 years. The mean
age of the food non-exclusion group was significantly lower than that of the food exclusion
group (p = 0.016). The mean BMI of all subjects was 23.6 kg/m2 and the diagnosis period
was < 1 year in 23.1%, 1–3 years in 36.5%, and ≥ 3 years in 40.4% of all subjects. The type of
IBD was Crohn's disease in 58.7% and ulcerative colitis in 41.3%. For current disease activity
27.9% of patients were categorized as active stage and there was no significant difference
between the 2 groups.
The nutritional status was adequate for 65.4% of the patients in the food exclusion group
while there was mild-moderate malnutrition in 22.4% and severe malnutrition in 12.2% of
the patients. The respective rates in the food non-exclusion group were 76.4%, 18.2%, and
5.5%. The rate of malnutrition in the food exclusion group was significantly higher than the
non-exclusion group (p = 0.007) (Figure 1).
As a result of the analysis of beliefs and attitudes toward diet, the rate of dietary intervention
was 77.6% in the food exclusion group and 36.4% in the food non-exclusion group, and there
was a significant difference between the 2 groups (Table 2). Total of 38 patients had a dietary
Table 1. Demographics and characteristics of the IBD patients
Characteristics Total (n = 104) Food exclusion group (n = 49) Food non-exclusion group (n = 55) p value
Age, yr 39.4 (16.1) 35.6 (13.5) 45.3 (17.9) 0.016
Sex 0.448
Male 60 (57.7) 27 (55.1) 33 (60.0)
Female 44 (42.3) 22 (44.9) 22 (40.0)
BMI, kg/m2 23.6 ± 5.8 23.0 ± 6.0 24.7 ± 3.9 0.583*
Disease duration, yr 0.127
<1 24 (23.1) 14 (28.6) 10 (18.2)
1–3 38 (36.5) 18 (36.7) 20 (36.4)
>3 42 (40.4) 17 (34.7) 25 (45.5)
Disease type 0.045
Crohn's disease 61 (58.7) 32 (65.3) 29 (52.7)
Ulcerative colitis 43 (41.3) 17 (34.7) 26 (47.3)
Disease activity 0.261
Inactive 75 (72.1) 34 (69.4) 41 (75.5)
Active 29 (27.9) 15 (30.6) 14 (25.5)
Data were reported as mean ± standard deviation or mean (standard deviation) for continuous variables and frequency (percentage) for categorical variables.
p values were calculated by χ2 test.
IBD, inflammatory bowel disease; BMI, body mass index.
*p value was calculated by independent t-test.
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Food Elimination Diet in IBD Patients CLINICAL NUTRITION RESEARCH
3 (5.5)
6 (12.2)
10 (18.2)
11 (22.4)
32 (65.4) 42 (76.4)
Food exclusion group Food non-exclusion group
Adequate Mild-moderate malnutrition Severe malnutrition
Figure 1. Comparison of nutritional status between groups. Data were reported as frequency (percentage) for
categorical variables. p value for the significant difference between 2 groups is 0.007 and was calculated by χ2 test.
modification by harmful food restriction (50.0%), harmful recipes restriction (21.0%), and
adjusting the amount of meals (15.8%). In addition, 73.5% of those in the food exclusion
group indicated that food should be avoided in order to prevent relapse of disease, as
compared to 20.0% of those in the food non-exclusion group. The percentage of people who
wanted nutrition education and management was 83.7% for the food exclusion group and
67.3% in the food non-exclusion group.
In part of the survey on eating habits and lifestyle (Table 3), there was a significant difference
only in drinking and eating out between the 2 groups. Despite the fact that there was no
difference in the ratio of men and women between the 2 groups, the food non-exclusion
group had a high rate of alcohol consumption. The rates of regular exercise and eating
regular meals was < 50%. The frequency of eating out was 1–3 times per month in the food
exclusion group and 1–2 times per week in the food non-exclusion group.
Table 2. Diet beliefs and educational demand of the IBD patients
Questionnaires Food exclusion group (n = 49) Food non-exclusion group (n = 55) p value
1) Do you think you are important to meals in the beginning and during 40 (81.6) 48 (87.3) 0.237
the period of IBD diagnosis?
2) Do you have a dietary modification? 38 (77.6) 20 (36.4) < 0.001
Adjustment of meal amount 6 (15.8) 2 (10.0) 0.148
Restriction of harmful food 19 (50.0) 7 (35.0) -
Restriction of harmful recipe 8 (21.0) 7 (35.0) -
Diet slowly 2 (5.3) 1 (5.0) -
Etc. 3 (7.9) 3 (15.0) -
3) Do you think that diet could play a role in causing disease 25 (51.0) 28 (50.9) 0.516
recurrence?
4) Do you think that you should avoid some food to prevent disease 36 (73.5) 11 (20.0) < 0.001
recurrence?
5) In case of recurrence, what diet do you believe can improve disease 31 (63.3) 30 (54.5) 0.062
symptoms?
6) Do you receive nutrition education and management? 8 (16.3) 10 (18.2) 0.728
7) Do you want a nutritional education and professional management? 41 (83.7) 37 (67.3) 0.028
Data were calculated based on answer ‘yes.’ Data were reported as frequency (percentage) for categorical variables and p values were calculated by χ2 test.
IBD, inflammatory bowel disease.
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Food Elimination Diet in IBD Patients CLINICAL NUTRITION RESEARCH
Table 3. Life habit and eating behavior of the IBD patients
Variables Food exclusion group (n = 49) Food non-exclusion group (n = 55) p value
Alcohol consumption 0.002
Yes 16 (32.7) 36 (65.5)
No 34 (69.4) 19 (34.5)
Smoking 0.670
Yes 18 (36.7) 21 (38.2)
No 31 (63.3) 34 (61.8)
Regular exercise 0.117
Yes 19 (38.8) 27 (49.1)
No 30 (61.2) 28 (50.9)
Meal regularity 0.559
Regular 24 (49.0) 25 (45.5)
Irregular 25 (51.0) 30 (54.5)
Eating speed, min 0.308
< 10 8 (16.3) 15 (27.3)
10–30 32 (65.3) 33 (60.0)
> 30 9 (18.4) 7 (12.7)
Eating out 0.010
> 3 times per wk 5 (10.2) 11 (20.0)
1–2 times per wk 16 (32.7) 26 (47.3)
1–3 times per mon 28 (57.1) 15 (27.2)
< 1 time per mon 0 (0.0) 3 (5.5)
Data were reported as frequency (percentage) for categorical variables and p values were calculated by χ2 test.
IBD, inflammatory bowel disease.
In the food exclusion group, the most frequently restricted foods were milk and dairy
products, raw fish, fatty meats, noodles, and deep-spicy foods (Table 4). Milk and dairy
products, raw fish, deep-spicy foods, deep-fried foods, and fatty meat were restricted in high
priority when the disease was activated.
As a result of nutrient intake analysis, there was no significant difference in energy, protein,
fat, carbohydrate, or fiber between 2 groups (Table 5). Calcium, zinc, and vitamin A intake in
the food exclusion group were significantly lower than those in the food non-exclusion group.
Table 4. Food items of food exclusion group (n = 49)
Food items Always avoid Avoid when disease is active
Multi-grain rice 2 (4.1) 5 (10.2)
Noodles 6 (12.2) 9 (18.4)
Bread 2 (4.1) 3 (6.1)
Popcorn, cookies 3 (6.1) 3 (6.1)
Beans 4 (8.2) 9 (18.4)
Lean meat 2 (4.1) 2 (4.1)
Fatty meat 8 (16.3) 21 (42.9)
Seafood 3 (6.1) 3 (6.1)
Raw fish 12 (24.5) 35 (71.4)
Salad and raw vegetables 1 (2.0) 1 (2.0)
Seaweeds 1 (2.0) 1 (2.0)
Nuts and seeds 5 (10.2) 6 (12.2)
Milk and dairy product 16 (32.7) 38 (77.6)
Tea or coffee 5 (10.2) 9 (18.4)
Fruits 0 (0.0) 3 (6.1)
Sugar, chocolate 5 (10.2) 7 (14.3)
Ramen 9 (18.4) 15 (30.6)
Pizza 5 (10.2) 14 (28.6)
Deep-spicy foods 11 (22.4) 26 (53.1)
Deep-fried foods 6 (12.2) 22 (44.9)
Data were reported as frequency (percentage) for categorical variables.
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Food Elimination Diet in IBD Patients CLINICAL NUTRITION RESEARCH
Table 5. Nutrient intake status of the IBD patients
Variables Total (n = 104) Food exclusion group (n = 49) Food non-exclusion group (n = 55) p value
Energy, kcal 1,883.6 ± 550.3 1,894.6 ± 583.6 1,769.3 ± 465.1 0.663
Protein, g 62.5 ± 22.4 59.9 ± 16.5 66.4 ± 21.7 0.454
Fat, g 48.4 ± 20.9 46.3 ± 14.6 50.4 ± 20.9 0.223
Carbohydrate, g 250.4 ± 63.1 249.8 ± 107.6 262.9 ± 58.9 0.415
Fiber, g 8.8 ± 5.7 8.4 ± 5.5 9.5 ± 7.9 0.547
Calcium, mg 476.3 ± 252.9 403.2 ± 255.7 568.3 ± 135.0 0.002
Phosphorous, mg 984.5 ± 425.6 918.3 ± 239.9 1,076.0 ± 409.9 0.454
Iron, mg 10.8 ± 4.6 10.0 ± 2.5 11.4 ± 5.3 0.644
Sodium, mg 4,460.7 ± 1,239.3 4,219.5 ± 1,586.3 4,521.7 ± 1,047.7 0.510
Potassium, mg 2,395.6 ± 899.4 2,373.0 ± 661.2 2,500.5 ± 931.8 0.326
Zinc, mg 7.3 ± 2.8 6.1 ± 1.5 7.7 ± 3.3 0.001
Vitamin A, mgRE 765.6 ± 548.5 644.3 ± 333.9 851.5 ± 760.6 < 0.001
Vitamin B1, mg 1.1 ± 0.7 1.0 ± 0.6 1.2 ± 0.4 0.409
Vitamin B2, mg 1.4 ± 0.6 1.4 ± 0.5 1.5 ± 0.3 0.325
Vitamin B6, mg 1.6 ± 0.7 1.5 ± 0.6 1.6 ± 0.9 0.549
Niacin, mgNE 16.0 ± 13.5 15.1 ± 6.5 16.9 ± 12.0 0.670
Vitamin C, mg 104.6 ± 35.8 99.7 ± 421 110.2 ± 29.4 0.187
Folate, µg 266.5 ± 58.2 255.4 ± 54.2 271.6 ± 82.8 0.201
Vitamin E, mg 13.6 ± 9.1 12.4 ± 5.2 13.1 ± 9.0 0.155
Data were reported as mean ± standard deviation for continuous and p value was calculated by independent t-test.
IBD, inflammatory bowel disease.
DISCUSSION
The deliberate diagnosis of ulcerative colitis and Crohn's disease is important for IBD. The
ultimate goal of IBD treatment is to improve symptoms of acute episodes and to improve the
quality of life and health of patients by treating patients well [13]. In recent years, the concept
of remission has changed, and the empirical contents such as improvement of clinical
symptom of the patient have been reflected as a new concept of ‘deep remission’ [14].
The rate of malnutrition in patients with IBD is very high and the immune system damage
caused by malnutrition has been reported to have a negative effect on treatment response. In
the case of Crohn's disease, nutritional support is needed as a primary treatment of disease,
and comparative studies with steroid treatment have proved to be effective, but ulcerative
colitis has not been recognized as an absolute necessity for primary treatment. However,
there is a common opinion that secondary treatment is needed to treat malnutrition for both
diseases [15,16]. For patients with IBD parenteral nutrition and the guideline for tube feeding
and oral intake according to intestinal function is recommended. In case of resting period,
the recurrence rate is low when a normal diet is added to a basal diet [17].
Patients with IBD have high rates of iron, calcium, vitamin B12, and vitamin D deficiencies.
One of the causes for malnutrition is a dietary adjustment to the patient's own experience
and beliefs. The degree of dietary intolerance was similar between patients with Crohn's
disease and ulcerative but studies have also identified food intolerance in artificial
sweeteners, grains, dairy products, and yeast in IBD patients [18,19]. Recent changes in the
concept of IBD treatment are not adequate to control patients' beliefs and experiences. Still,
there is a concern about an adverse effect of the diet which is based on of patients' prolonged
absolute belief. Individualized adjustments are therefore necessary to accommodate the
patient's disease and condition. In this study, the food exclusion group had a higher rate of
Crohn's disease patients and the belief that food control decreased recurrence of symptoms
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Food Elimination Diet in IBD Patients CLINICAL NUTRITION RESEARCH
compared to food non-exclusion group. However, the intake of some nutrients was poor, and
the rate of malnutrition was high in patients in the food exclusion group.
This study has a limitation. In this study the patients were not classified according to disease
or activity and the nutrient intake of study patients was assessed regardless of adequate
intake according to individual nutritional requirement. What is interesting is that the rate of
receiving nutrition education or management is very low and the rate of requests is very high.
According to an international study, about half of Crohn's disease patients who had weight
loss experienced pleasure of eating according to the management of specialists and reported
that those changes affected the recurrence of disease symptoms [20]. There are not many
domestic or foreign studies evaluating this concept between nutrition and IBD management
and this is an important area for future research. It is considered that dietary factors that
should be treated in high priority for the social life of IBD patients.
CONCLUSION
In conclusion, we emphasize that appropriate nutritional interventions are necessary to
provide information on beliefs, causes of action and clinical outcomes of patients with IBD.
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