Journal of Crohn's and Colitis, 2017, 1430–1439

doi:10.1093/ecco-jcc/jjx102
Advance Access publication July 24, 2017
Original Article

Original Article

Prevalence of Malnutrition and Nutritional

Characteristics of Patients With Inflammatory
Bowel Disease

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María José Casanova,a Maria Chaparro,a Begoña Molina,a,*
Olga Merino,b Ricardo Batanero,b,* Carmen Dueñas-Sadornil,c
Pilar Robledo,c Ana María Garcia-Albert,d Maria Bienvenida Gómez-
Sánchez,d,* Xavier Calvet,e Maria del Roser Trallero,e,* Miguel Montoro,f
Iria Vázquez,f,* Mara Charro,g Amaya Barragán,g,* Francisco Martínez-
Cerezo,h Isabel Megias-Rangil,h,*José María Huguet,i Ezequiel Marti-
Bonmati,i,† Marta Calvo,j Mariana Campderá,j,* Margarita Muñoz-
Vicente,k Angel Merchante,k,* Ansel David Ávila,l Pilar Serrano-Aguayo,l,*
Ruth De Francisco,m Daniel Hervías,n Luis Bujanda,o Gloria Esther
Rodriguez,p Luisa Castro-Laria,q Manuel Barreiro-de Acosta,r Manuel Van
Domselaar,s Patricia Ramirez de la Piscina,t Javier Santos-Fernández,u
Alicia Algaba,v Sandra Torra,w Liliana Pozzati,x Pilar López-Serrano,y
Maria del Rosario Arribas,z Maria Luisa Rincón,aa Andrés Camilo Peláez,ab
Elena Castro,ac Antonio García-Herola,ad Cecilio Santander,a
Moisés Hernández-Alonso,c Elisa Martín-Noguerol,c
María Gómez-Lozano,d Tamara Monedero,d,* Albert Villoria,e
Ariadna Figuerola,e Andrés Castaño-García,m Jesús M. Banales,o
Laura Díaz-Hernández,p Federico Argüelles-Arias,q Javier López-Díaz,r
Isabel Pérez-Martínez,m Noelia García-Talavera,d,*
Olivia Karina Nuevo-Siguairo,m Sabino Riestra,m Javier P. Gisberta

Departments of Gastroenterology, *Endocrinology and Nutrition, and †Pharmacy from: aHospital Universitario de
La Princesa, Instituto de Investigación Sanitaria Princesa (IIS-IP) and Centro de Investigación Biomédica en Red
de Enfermedades Hepáticas y Digestivas (CIBEREHD), Madrid, Spain bHospital Universitario de Cruces, Bilbao,
Spain cHospital Universitario San Pedro Alcántara, Cáceres, Spain dHospital Universitario Reina Sofía, Murcia,
Spain eCorporació Sanitària Universitària Parc Taulí, Sabadell, Universitat Autònoma de Barcelona, and CIBEREHD,
Instituto de Salud Carlos III, Grupo de Investigación Consolidado (SGR01500), Spain fHospital San Jorge de Huesca,
Huesca, Spain gHospital Royo Villanova, Zaragoza, Spain hHospital Universitario Sant Joan de Reus, Tarragona,
Spain iHospital General Universitario de Valencia, Valencia, Spain jHospital Universitario Puerta de Hierro, Madrid,
Spain kHospital General Universitario de Castellón, Castellón, Spain lHospital Universitario Virgen del Rocío, Sevilla,
Spain mHospital Universitario Central de Asturias, Oviedo, Spain nHospital Virgen de la Altagracia, Manzanares,
Spain oHospital de Donostia, Instituto Biodonostia, Universidad del País Vasco (UPV/EHU), and CIBEREHD, Donostia,
Spain pHospital Universitario Nuestra Señora de La Candelaria, Tenerife, Spain qHospital Universitario Virgen de
La Macarena, Sevilla, Spain rHospital Clínico Universitario de Santiago de Compostela, Santiago, Spain sHospital
Universitario de Torrejón, Madrid, Spain tHospital Universitario de Álava, Vitoria, Spain uHospital Universitario Río
Hortega, Valladolid, Spain vHospital Universitario de Fuenlabrada, Madrid, Spain wParc Sanitari Sant Joan de Déu,

Copyright © 2017 European Crohn’s and Colitis Organisation (ECCO). Published by Oxford University Press. All rights reserved.
1430
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Nutrition and IBD 1431

Barcelona, Spain xHospital de Mérida, Mérida, Spain yHospital Universitario Fundación Alcorcón, Madrid, Spain
z
Hospital Universitario Infanta Sofía, Madrid, Spain aaHospital Comarcal Bidasoa, Guipúzkoa, Spain abHospital
General de Catalunya, Barcelona, Spain acHospital Lucus Augusti, Lugo, Spain adHospital Marina Baixa, Alicante;
Spain

Corresponding author: Javier P. Gisbert, MD, Gastroenterology Unit, Hospital Universitario de La Princesa, Diego de León,
62. 28006 Madrid, Spain. Tel.: 34-913093911; fax: 34-914022299; email: javier.p.gisbert@gmail.com

Abstract
Background and Aims: This study sought to determine the prevalence of malnutrition in patients
with inflammatory bowel disease, to analyse the dietary beliefs and behaviours of these patients,
to study their body composition, to evaluate their muscular strength and to identify the factors
associated with malnutrition in these patients.
Methods: This was a prospective, multicentre study. Crohn’s disease and ulcerative colitis

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patients from 30 Spanish centres, from the outpatient clinics, were included. A questionnaire
of 11 items was applied to obtain data from patients’ dietary behaviour and beliefs. Patients
who accepted were evaluated to assess their nutritional status using Subjective Global
Assessment and body mass index. Body composition was evaluated through bioelectrical
impedance.
Results: A total of 1271 patients were included [51% women, median age 45 years, 60% Crohn’s
disease]. Of these, 333 patients underwent the nutritional evaluation. A total of 77% of patients
declared that they avoided some foods to prevent disease relapse. Eighty-six per cent of patients
avoided some foods when they had disease activity because of fear of worsening the flare. Sixty-
seven per cent of patients modified their dietary habits after disease diagnosis. The prevalence of
malnutrition was 16% [95% confidence interval = 12–20%]. In the multivariate analysis, history of
abdominal surgery, active disease and avoidance of some foods during flares were associated
with higher risk of malnutrition.
Conclusions: The prevalence of malnutrition in inflammatory bowel disease patients was high.
We identified some predictive factors of malnutrition. Most of the patients had self-imposed food
restrictions, based on their beliefs.

Key Words: Inflammatory bowel disease; malnutrition; body composition

1. Introduction Many factors can contribute to malnutrition in these patients,

such as reduced oral intake. In IBD patients, reduced oral intake
The nutritional status of inflammatory bowel disease [IBD] patients
may play an important role in the onset of malnutrition, and can be
is frequently altered, even when the disease is in remission.1–3
due to many factors such as self imposed food restrictions, decreased
Alterations in body composition in IBD patients seem to be com-
hunger, reduced sensation of pleasure related to eating, changes in
mon, but have not been well studied.1,2 Most patients with IBD have
mood and even medical advice.8,9 Patients’ self-imposed food restric-
an altered distribution of fat-free mass and fat mass. Inadequate
tions may contribute to worsening of their nutritional status.10–12
body composition and malnutrition have been associated with
However, only a few studies have analysed the beliefs and behav-
poor outcomes, such as a higher frequency of postoperative com-
iours of patients with IBD with respect to diet.8,12–17 Moreover, the
plications, longer hospital stays, decreased quality of life and higher
contribution of these beliefs and behaviours to malnutrition has not
health costs.1,3
been well studied.
A variety of methods can be employed to measure body composi-
The aims of this study were to determine the prevalence of mal-
tion. In routine clinical practice basic anthropometry techniques are
nutrition in IBD patients, to analyse their dietary beliefs and behav-
generally used, such as body mass index [BMI]. However, BMI and
iours, to study their body composition, to evaluate their muscular
biochemical parameters of nutritional risk are not accurate enough
strength and to identify the factors associated with malnutrition in
to estimate body composition, even in patients in clinical remission
these patients.
because, in a high proportion of IBD patients, these values may be
within normal ranges while they still have an altered body composi-
tion.2,4–6 Bioelectrical impedance analysis [BIA] is a simple, fast and
2. Methods
noninvasive method to estimate body composition. It is based on the
opposition to the flow of an electric current through body tissues, 2.1. Study population
which can then be used to calculate total body water, and to estimate The present study was a multicentre, observational, prospec-
fat-fee mass [lean mass] and fat mass.7 tive study conducted at 30 Spanish centres. The study population
1432
comprised consecutive outpatients diagnosed with Crohn’s disease
[CD] or ulcerative colitis [UC] followed at IBD Units of the par-
ticipant centres between January 2015 and April 2016. Pregnant
patients, patients with pacemakers, patients with implantable auto-
matic defibrillators and patients on diuretic therapy were excluded.
2.2. Ethical aspects
The study was approved by the respective institutional ethics review
boards, and was conducted according to the Declaration of Helsinki
and Good Clinical Practice guidelines.
2.3. Data collection
The study had two parts. In the first, a questionnaire of 11 items
was applied to obtain data on the dietary behaviour and beliefs of
IBD patients. The questionnaire was developed by the IBD Unit and
the Endocrinology and Nutrition Department after a careful review
of the literature about the dietary habits of IBD patients. A pilot
questionnaire was administered to ten IBD patients and, as a result
of this pilot study, minor modifications to the questionnaire were
made. The patients who accepted to participate in this part of the
study completed the questionnaire before leaving the clinics. All the
patients who accepted to participate in the first part of the study
were invited to participate in the second part.
The second part of the study aimed to evaluate the nutritional
status of IBD patients. All the patients who accepted to participate
in this part of the study were referred to the nutrition clinics of
the participant centres. All participating centres had a dietician or
an endocrinologist specialized in nutrition. In these nutrition clin-
ics, Subjective Global Assessment [SGA] was performed. SGA is a
validated nutritional assessment tool, which is implemented by a
physician, and is based on features of medical history and physi-
cal examination. SGA classifies patients as: grade A, well nourished;
grade B, moderately malnourished; and grade C, severely malnour-
ished.18 In addition, anthropometric measurements such as BMI,
triceps skinfold, twin circumference and abdominal circumference
were taken. Body composition [i.e. fat mass, fat-free mass and total
body water] was evaluated through BIA. To assess body composi-
tion, the participant centres used the Tanita MC-980-MA Body
Composition Monitor. Likewise, fat-free mass index [FFMI] was
calculated and classified in percentiles by sex and age using Schutz
et al. reference tables.19 Finally, handgrip strength was measured by
using a handgrip dynamometer [Kern-Map 80K1 model] and the
values obtained were also classified in percentiles by sex and age
according to Mateo-Lázaro et al. reference tables for the Spanish
adult population.20
Clinical, endoscopic and radiological data were collected. These
included demographic data, type of IBD, localization and extent of
the disease, duration of IBD, smoking habits, previous surgery for
IBD, IBD treatment received during the last year [including the use
of steroids], endoscopic and radiological activity [the last endoscopy
and magnetic resonance imaging performed during the last year, if
available], number of hospitalizations due to IBD flares, chronic
comorbidities which can affect the nutritional status of the patient
[e.g. coeliac disease or psychiatric diseases], and the use of nutritional
supplements and vitamins. Clinical activity data were collected at the
moment of inclusion in the study, through the Harvey–Bradshaw
index [in CD] or Partial Mayo index [in UC]. Biochemical param-
eters collected included: haemoglobin, ferric profile, leucocytes, lipid
profile, thyroid profile, albumin, C-reactive protein, vitamin B12,
folate, vitamin D and zinc. Micronutrient deficiencies were classified
using the reference values of each participant centre.
M. J. Casanova et al.
Study data were collected and managed using REDCap elec-
tronic data capture tools hosted at Asociación Española de
Gastroenterología [AEG; www.aegastro.es].21 AEG is a nonprofit
Scientific and Medical Society focused on Gastroenterology, and it
provides this service free of charge, with the sole aim of promot-
ing independent investigator-driven research. REDCap [Research
Electronic Data Capture] is a secure, web-based application designed
to support data capture for research studies, providing [1] an intui-
tive interface for validated data entry; [2] audit trails for tracking
data manipulation and export procedures; [3] automated export
procedures for seamless data downloads to common statistical pack-
ages; and [4] procedures for importing data from external sources.
2.4. Definitions
2.4.1. Malnutrition
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A patient was considered to be malnourished if he/she had one of the
following: a BMI below 18.5 kg/m2, or a FFMI lower than the 10th
percentile or an SGA grade B or C.
2.4.2. Body mass index
Weight [kg] divided by squared height [m]. BMI values were classi-
fied as follows: underweight: <18.5 kg/m2; normal: 18.5–25 kg/m2;
overweight >25–29.9 kg/m2; obesity 30 kg/m2.
2.4.3. Fat-free mass index
FFMI was calculated as fat-free mass [kg] divided by squared height
[m].19
2.4.5. Subjective Global Assessment
SGA was classified as: grade A, well nourished; grade B, moderately
malnourished; and grade C, severely malnourished.
2.4.6. Decreased handgrip strength
This was noted if the value obtained from the dynamometer below
the 10th percentile.
2.4.7. Disease activity
For luminal CD, clinical activity was defined as a Harvey–Bradshaw
index score >4 points.22 For UC, clinical activity was defined as a
partial Mayo score >2 points.23
2.5. Statistical analysis
The descriptive analysis of quantitative variables included the mean
and standard deviation or the median and interquartile range,
depending on whether the variables were normally distributed
or not. For the categorical variables, percentage and 95% confi-
dence intervals [95% CIs] were provided. Comparisons between
means were performed using the t test for independent samples or
the Wilcoxon rank-sum test according to the distribution of data.
Categorical variables were compared using the χ2 test and the Fisher
exact test. Statistical significance was set at p < 0.05.
A lineal regression model was constructed to identify predictive
factors for malnutrition. All the variables that reached statistical sig-
nificance in the univariate analysis and those that were considered
clinically relevant were included in the multivariate analysis. The
dependent variable was the risk of malnutrition. The independent
variables were: type of IBD [CD and UC], gender, age, surgery due to
IBD, extraintestinal manifestations, current smoking habit, clinical
activity [yes/no], type of IBD therapy, treatment with steroids in the
last year, avoidance of some food groups to prevent a disease flare
Nutrition and IBD 1433

and avoidance of some food groups during a flare. The results were Table 1. Baseline characteristics of the patients.
expressed as odds ratios [ORs] with their corresponding 95% CIs.
Variable Total

Type of disease, n [%] 1271 [100]

3. Results CD 761 [60]
3.1. Study population UC 510 [40]
Male, n [%] 617 [48.5]
A total of 1271 patients who completed the questionnaire and met
Mean age, years [range] 45 [15–86]
the inclusion criteria were included. Of these, 333 participated in the
Mean duration of IBD, years [range] 11 [1–45]
nutritional assessment. The main characteristics of the patients are Extra-intestinal manifestations, n [%] 258 [24]
summarized in Table 1. Sixty per cent of them had CD. The mean age Current smokers, n [%] 196 [18.2]
was 45 years [interquartile range 15–86]. Twenty-three per cent had History of abdominal surgery, n [%] 249 [23]
a history of abdominal surgery due to IBD, and 18% were current Treatment of IBD, n [%]
smokers. Eight per cent of the patients had been exposed to steroids None 230 [18]
in the last year. The distribution of IBD treatment was as follows: 5-ASA 320 [25]
25% 5-aminosalicylates [5-ASA], 26% immunosupressors, 11% IMMs 336[26]

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anti-tumour necrosis factor [anti-TNF] and 20% combo therapy Biologics 138 [11]
Combo therapy 247 [20]
[immunosupressors plus anti-TNF].
Systemic steroids during the last year, n [%] 105 [8.3]
Clinical activity, n [%] 238 [22]
3.2. Dietary beliefs Mild activity 165 [80.5]
Almost half of the patients [48%] declared that they believed cer- Moderate activity 34 [16.6]
tain foods increase the risk of developing IBD [question 1 of the Severe activity 6 [2.9]
questionnaire]. The role of diet as a trigger of IBD flares was con- Montreal location at CD diagnosis, n [%]
sidered to be important or very important for 68% of the patients L1 [ileal] 305 [40]
L2 [colonic] 111 [14.6]
[question 2]. The vast majority of the patients [87%] believed that it
L3 [ileocolonic] 344 [45.3]
would be useful to receive nutritional advice by qualified personnel
L4 [upper gastrointestinal tract] 1 [0.1]
[question 7]. Montreal behaviour at CD diagnosis, n [%]
When the disease was in remission, 4% of the patients noted B1 [inflammatory] 426 [56.1]
reduced appetite [question 8]. By contrast, during a flare, 69% of the B2 [stricturing] 167 [22]
patients considered that their appetite had diminished [question 9]. B3 [penetrating] 167 [22]
Perianal disease, n [%] 188 [24.7]
UC extent, n [%]
3.3. Dietary behaviours Proctitis 101 [19.8]
Seventy-six per cent of the patients avoided eating some food groups Left side colitis 196 [38.4]
in order to prevent a disease flare [question 3]. Most patients [86%] Extensive colitis 213 [41.8]
avoided eating some food groups when they had disease activity
because of a fear of worsening their symptoms [question 5]. The CD: Crohn’s disease; UC: ulcerative colitis; IMMs: immunomodulators;
foods groups avoided to prevent a flare and during a flare are sum- 5-ASA: 5-aminosalicylates.
marized in Figure 1.
After IBD diagnosis, 66% of the patients modified their dietary 95% CI: 0.97–0.99], male gender [OR 0.6, 95% CI: 0.5–0.9] and
habits [question 10], and 38% refused to dine out because of a fear UC vs CD [OR 0.7, 95% CI: 0.5–0.9] were associated with a lower
that the food could worsen the disease symptoms [question 11]. The risk of food restriction behaviour during a flare. History of surgery,
dietary beliefs and behaviours of the total patient group, and accord- extraintestinal manifestations, smoking habit, clinical activity and
ing to the type of IBD are detailed in Table 2. IBD therapy were not associated with food restriction behaviour
during a disease flare.
3.4. Factors associated with food restriction
behaviour 3.5. Nutritional assessment
A multivariate analysis was performed to evaluate the factors 3.5.1. Clinical characteristics of the patients
associated with patient self-imposed food restriction behaviour. Of the 333 patients included in this part of the study, 48% were
The factor most associated with a higher risk of food restric- male and 57% had CD [Table 3]. Regarding treatment, 26% were
tion behaviour to prevent a disease flare was treatment with treated with 5-ASA, 13% with biologics, 24% with IMMs, 30%
immunomodulators [IMMs] vs no treatment [OR 1.5, 95% CI: received combo therapy and 7% had no treatment. Eight per cent of
1.1–2.1], while UC vs CD was associated with a lower risk [OR the patients had been treated with systemic steroids in the last year.
0.6, 95% CI: 0.5–0.9], adjusted by history of abdominal surgery. Clinical disease activity was present in 26% of the patients and in
Gender, age, duration of IBD, extraintestinal manifestations, most of them [82%] it was mild.
smoking habit, clinical activity and treatment with steroids in the Regarding dietary supplements, 13% of the patients were receiv-
last year had no impact on food restriction behaviour to prevent ing vitamin B12, 8% folic acid, 12% oral iron supplements, 17%
a flare. vitamin D and 12% calcium.
By contrast, the factors associated with a higher risk of food
restriction behaviour during a disease flare were longer IBD dura- 3.5.2. Malnutrition and body composition
tion [OR 1.03, 95% CI: 1.007–1.05], and systemic steroid treatment Of the 333 patients who underwent nutritional assessment, 7%
during the last year [OR 2.9, 95% CI: 1.2–6.8]. Older age [OR 0.98, had SGA grade B or C. BMI was below 18.5 kg/m2 in 4% of these
1434 M. J. Casanova et al.

(a) (b)
Spicy foods 63%
Alcohol 48% Spicy foods 73%

Fat 40% Alcohol 62%

Carbonated Fat 57%
38% Carbonated
beverages 54%
Precooked food 26% beverages
Fiber 41%
Fiber 25%
leguminous 38%
Dairy products 23%
Processed meat 37%
Processed meat 22%
Precooked foods 37%
Sugar 21%
Dairy products 36%
Leguminous 21%
Sugar 32%
Raw vegetables 18% Raw vegetables 31%
Fruits 7% Fruits 15%
Red meat 6% Red meat 12%
Eggs 3% Eggs 6%

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Fish 3% Fish 5%
0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100% 0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100%

Figure 1. [a] Food groups avoided to prevent a flare. [b] Food groups avoided during a disease flare.

Table 2. Dietary beliefs and behaviours of the patients

Question Total CD UC p-value [CD vs UC]

Q1. Do you believe that certain foods increase the risk of developing IBD? n [%]
Yes 605 [47.6] 358 [51.6] 247 [48.4] > 0.05
No 647[50.9] 393 [47] 254 [49.8]
NR 19 [1.5] 10 [1.3] 9 [1.8]
Q2. What importance do you consider that diet has as a trigger of IBD flares? n [%]
Important or very important 861 [67.7] 530 [69.6] 331 [64.9] > 0.05
Slightly important or not at all important 397 [31.2] 224 [29.5] 173 [33.9]
NR 13 [1] 7 [0.9] 6 [1.2]
Q3. Do you avoid some food groups to prevent a disease relapse? n [%]
Yes 960 [75.5] 609 [80] 351 [68.8] < 0.001
No 303 [23.8] 148 [19.4] 155 [30.4]
NR 8 [0.6] 4 [0.5] 4 [0.8]
Q5. Do you avoid some food groups for fear of worsening the disease flare? n [%]
Yes 1089 [85.7] 669 [89.7] 420 [82.4] < 0.05
No 168 [13.2] 86 [11.3] 82 [16.1]
NR 14 [1.1] 6 [0.8] 8 [1.6]
Q7. Do you believe that it would be useful to receive nutritional advice provided by qualified personnel? n [%]
Yes 1114 [87.6] 666 [87.5] 448 [87.8] > 0.05
No 144 [11.3] 89 [11.7] 55 [10.8]
NR 13 [1] 6 [0.8] 7 [1.4]
Q8. How is your appetite during disease remission? n [%]
Normal or increased 1204 [94.8] 716 [94.1] 488 [96.7] > 0.05
Decreased 50 [3.9] 36 [4.7] 14 [2.7]
NR 17 [1.3] 9 [1.2] 8 [1.6]
Q9. How is your appetite during a disease flare? n [%]
Normal or increased 377 [29.6] 162 [21.2] 215 [42.1] < 0.001
Decreased 871 [68.6] 588 [77.3] 284 [55.7]
NR 22 [1.7] 11 [1.4] 11 [2.2]
Q10. Have you modified your dietary habits since IBD diagnosis? n [%]
Yes 841 [66.2] 528 [69.4] 313 [61.4] <0.01
No 417 [32.8] 228 [30] 189 [37.1]
NR 13 [1] 5 [0.7] 8 [1.6]
Q11. Do you refuse to dine out because of fear that food could worsen your symptoms? n [%]
Yes 480 [37.8] 313 [41.1] 167 [32.7] <0.01
No 777 [61.1] 441 [58] 336 [65.9]
NR 14 [1.1] 7 [0.9] 7 [1.4]

IBD: inflammatory bowel disease; CD: Crohn’s disease; UC: ulcerative colitis; NR: non-respondents.

patients, while 11% of the patients had an FFMI below the 10th of malnutrition was 16% [95% CI = 12–20%] [Figure 2]. The
percentile, according to sex and age. Sixteen per cent of the patients prevalence of malnutrition was similar between CD [17%, 95%
met at least one of the previous criteria. Thus, the overall prevalence CI = 12–23%] and UC patients [14%, 95% CI = 7–21%] [p = 0.4].
Nutrition and IBD 1435

Table 3. Clinical characteristics of the patients who underwent nutritional assessment

Variables Total CD UC

Type of disease, n [%] 333 [100] 189 [56.8] 144 [43.2]

Male, n [%] 161 [48.3] 92 [48.7]] 69 [47.9]
Mean age, years [range] 45 [15–80] 43 [15–79] 46 [21–80]
Mean duration of IBD, years [range] 10 [1–37] 11 [1–37] 10 [1–37]
Extra-intestinal manifestations, n [%] 76 [24.1] 49 [27.1] 27 [20]
Current smokers, n [%] 54 [17.1] 39 [21.5] 15 [11.1]
History of abdominal surgery, n [%] 70 [22] 64 [35.4] 6 [4.4]
Treatment of IBD, n [%]
None 22 [6.6] 18 [9.5] 8 [5.5]
5-ASA 87 [26.1] 13 [7] 70 [48.8]
IMMs 81 [24.3] 54 [28.5] 27 [18.7]
Biologics 43 [13] 35 [18.5] 8 [5.5]
Combo therapy 100 [30] 69 [36.5] 31 [21.5]

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Systemic steroids during the last year, n [%] 26 [7.8] 16 [8.5] 10 [6.9]
Clinical activity, n [%] 87 [26.1] 49 [27.2] 38 [27.3]
Mild activity 68 [81.9] 42 [87.5] 26 [74.3]
Moderate activity 12 [14.5] 5 [10.4] 7 [20]
Severe activity 3 [3.6] 1 [2.1] 2 [5.7]
Montreal location at CD diagnosis, n [%]
L1 [ileal] 66 [35]
L2 [colonic] 32 [16.9]
L3 [ileocolonic] 91 [48.1]
Montreal behaviour at CD diagnosis, n [%]
B1 [inflammatory] 113 [59.8]
B2 [stricturing] 44 [23.3]
B3 [penetrating] 32 [16.9]
Perianal disease, n [%] 57 [30.2]
UC extent, n [%]
Proctitis 24 [16.7]
Left side colitis 59 [41]
Extensive colitis 61 [42.4]

CD: Crohn’s disease; UC: ulcerative colitis; IBD: inflammatory bowel disease; IMMs: immunomodulators; 5-ASA: 5-aminosalicylates.

100% [15% vs 7%, p < 0.05] were more frequent in malnourished patients
in comparison with well-nourished patients. Biochemical parameters
80% are detailed in Figure 3.

60% 3.5.4. Muscular strength

Handgrip strength was decreased in 9% of the patients. There was
40% no difference between CD and UC patients [8% vs 8%, p = 0.7].
Malnourished patients had a diminished handgrip strength more fre-
quently than well-nourished patients [17% vs 8%, p < 0.05].
20% 16%
11%
7% 4% 3.5.5. Predictive factors of malnutrition
0% In the univariate analysis, history of abdominal surgery due to
SGA grade BMI < 18.5 FFMI < p10 TOTAL
B or C IBD was more frequent in patients with malnutrition that in well-
nourished patients [37% vs 19%, p < 0.01]. Moreover, clinical
Figure 2. Prevalence of malnutrition. SGA: Subjective Global Assessment; activity was more frequent in malnourished patients [52% vs 27%,
BMI: body mass index; FFMI: fat-free mass index. p < 0.001]. In addition, malnourished patients were treated more
frequently with combo therapy than well-nourished patients [44%
There were no differences between CD and UC patients in SGA vs 27%, p < 0.05]. Regarding food restriction behaviours, malnour-
grade B or C [8% vs 7%, p = 0.7], BMI < 18.5 kg/m2 [4% vs 3%, ished patients avoided some food groups to prevent a flare [82% vs
p = 0.5] and FFMI below the 10th percentile [13% vs 8%, p = 0.1]. 69%, p = 0.05], and during a flare [98% vs 83%, p < 0.01] more
According to BMI, 28% of the patients were overweight, and 18% frequently than well-nourished patients. No statistical differences
were obese. Of these, 8% had malnutrition. Nutritional characteris- were observed associated with gender, type of IBD, smoking habit,
tics of the patients are detailed in Table 4. extraintestinal manifestations, treatment with systemic steroids in
the last year, 5-ASA therapy, treatment with IMMs and biologics in
3.5.3. Biochemical parameters monotherapy.
Vitamin B12 deficiency [15% vs 4%, p < 0.01], vitamin D deficiency In the multivariate analysis [Table 5], the variables associated
or insufficiency [90% vs 78%, p < 0.05] and lower cholesterol levels with a higher risk of malnutrition were history of surgery due to IBD
1436 M. J. Casanova et al.

Table 4. Nutritional characteristics of the patients Table 5. Factors associated with risk of malnutrition in IBD patients

Variables TotalN = 333 CDN = 189 UCN = 144 Factor OR 95% CI p-value

Subjective global History of surgery due to IBD 2.1 1.02–4.2 0.04

assessment, n [%] Clinical activity 4.3 2.2–8.2 < 0.001
Grade A 308 [92.5] 174 [92] 134 [93.1] Avoidance of some food groups during a flare 10.3 1.3–78.1 0.03
Grade B 23 [6.9] 13 [6.9] 10 [6.9]
Grade C 2 [0.6] 2 [1.1] 0 [0] IBD: inflammatory bowel disease; OR: odds ratio; CI: confidence interval.
BMI, n [%]
Underweight 13 [4] 8 [4.2] 5 [3.4] investigating dietary beliefs and behaviours in IBD patients, and the
Normal 168 [50] 99 [52.4] 69 [48]
first that includes a nutritional assessment of the patients who par-
Overweight 94 [28] 45 [23.8] 49 [34]
ticipated in the study.
Obesity 58 [18] 37 [19.6] 21 [14.6]
Fat-free mass index, n [%] Almost half of the patients believed that certain foods increase
< p10 35 [10.5] 24 [12.7] 11 [7.6] the risk of IBD. This finding is similar to another study in which 48%
p10–p90 221 [66.4] 121 [64] 100 [69.4] of the patients perceived diet as an initiating factor of their disease.17

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> p90 77 [23.1] 44 [23.3] 33 [22.9] Several studies have suggested that IBD results from an unbalanced
Handgrip strength, n [%] relationship between environment, genes and the immune system.24
< p10 26 [9.1] 15 [7.9] 11 [7.6] Nutrients are an important part of the environmental factors and,
p10–p90 196 [5] 109 [57.7] 87 [60.4] in epidemiological studies, the Western dietary pattern is associated
> p90 65 [19.5] 32 [16.9] 33 [25.2] with an increased risk of developing IBD.17 Current evidence is, how-
unknown 46 [13.8] 33 [17.5] 13 [9]
ever, insufficient to draw firm conclusions about the role of dietary
components and the risk of developing IBD. Although there is a lack
CD: Crohn’s disease; UC: ulcerative colitis; BMI: body mass index; p10:
of evidence to support any recommendation of a specific diet for
tenth percentile; p90: ninetieth percentile.
IBD patients, many patients believe that some foods can induce or
100%
worsen disease symptoms. For this reason, a relevant proportion of
90% patients decide to avoid eating some food groups.8,25–32
80% 78% In our study, 68% of the patients considered that food has
an important or a very important role as a trigger of IBD flare.
60%
Moreover, 75% of the patients included in the present study avoided
some food groups in order to prevent a disease flare. Furthermore,
40% 87% of the patients avoided some food groups during a disease flare
because of fear of worsening their symptoms. The food restrictive
20% 15% 15%
behaviour was more frequent in CD patients than in UC patients.
14%
10% 12%10% 10% 10% 8% Limdi et al. studied the dietary behaviours and beliefs of 400 IBD
6% 7% 6%
4%
1% 2% 1%
0% patients.17 Of these, almost two-thirds believed that food had a role
in triggering an IBD flare, and avoided some foods to prevent a dis-
ia

es

ia

cy

y
ro
nc

nc

nc

nc
m

em
rid

en
te
ie

ie

ie

ie
ne

ci

ease relapse. Similar results were observed in another study.12 It is

es

in
ce
fic

fic

fic

fic
A

ffi
ol

um
ly
de

de

de

de
su
ch

ig

lb
on

tr

in

te

relevant to point out that, with the aim of preventing a flare, a sig-
w

in
B1
oa

la
y/
w
Ir

Lo

Z
Fo
nc
yp
Lo

in

ie

nificant number of patients avoided important food groups such as

H

fic
ita

de
V

fat, dairy products and vegetables. On the other hand, during a flare,
D
in
m

the number of patients who restricted the most important groups of

ita
V

Well-nourished patients Malnourished patients
Figure 3. Biochemical parameters.
[OR = 2.1, 95% CI = 1.02–4.2], clinical activity [OR = 4.3, 95%
CI = 2.2–8.2] and avoidance of some food groups during a flare
[OR = 10.3, 95% CI = 1.3–78.1]. Gender, age, type of IBD, smoking
habit, extraintestinal manifestations, treatment with steroids dur-
ing the last year, IBD therapy [IMMs, biologics in monotherapy and
combo therapy] and avoidance of some food groups to prevent a
flare had no impact on the risk of malnutrition.
4. Discussion
The results of the present study demonstrate that the vast majority
of IBD patients have self-imposed food restriction behaviour to pre-
vent a disease flare, and because of fear of worsening disease symp-
toms during a flare. Moreover, according to our findings, a restrictive
behaviour with respect to diet increases the risk of malnutrition.
To our knowledge, this is the largest published cohort of patients
foods—proteins and fat—was significantly increased. Similar results
have been reported in other studies.8,12,17
In our study, the majority of patients avoided some foods to pre-
vent a relapse, and because they thought that certain foods could
aggravate their symptoms during a flare. However, scientific evidence
to support specific dietary advice in patients with IBD is currently
lacking.33 These results are relevant because one of the mechanisms
of malnutrition in IBD patients is self-imposed food restrictions.9
Patients usually restrict some types of food based on their beliefs
on food intolerance. Many studies have analysed the relationship
between diet and IBD patient symptoms.8,17,34,35 The avoidance of
dairy products is frequent and has been reported in 16–34% of IBD
patients.8,12,17 A study from New Zealand reported that fat content of
dairy products had more influence in the symptoms of CD patients
than lactose content.36 However, another study did not find any asso-
ciation between disease relapse and the increased intake of milk and
dairy products.37
Many beliefs of the patients could be perpetuated by professional
dietary advice since there is no evidence to recommend a dairy-
free diet in IBD patients. However, a study reported that 40% of
Nutrition and IBD
physicians and nutritionists advise their IBD patients to avoid dairy
products.38 Another study found that in one-third of CD patients,
the reduction in food intake could be associated with an inadequate
restricted diet, low in fat and fibre, following medical advice.9
The vast majority of the patients considered that it would be use-
ful to receive nutritional advice from qualified personnel, in agree-
ment with other studies.8,17 However, in one study, only 50% of
the patients received professional advice from qualified personnel.8
Moreover, one-third of patients felt that their providers did not seem
to have enough time to discuss nutrition during visits.3 The role of
health professionals is important because nutritional advice has been
demonstrated to be effective in dietary management and protection
against nutritional deficiencies in patients with IBD.28,33,39,40
The prevalence of malnutrition in our IBD outpatients was
16%. This is a high value, especially taking into account that all the
patients were outpatients, and the majority of them were in remis-
sion or had mild activity. In Spain, the prevalence of malnutrition in
the general population is around 3%, with ranges from 0.5 to 14%.
However, most studies have been conducted in the elderly popula-
tion.41,42 A Spanish nationwide, cross-sectional, observational, multi-
centre study evaluated the prevalence of malnutrition in hospitalized
patients with chronic diseases. The authors found that the prevalence
of malnutrition was 37% in patients with neurological pathologies
[especially in patients with degenerative neurological diseases], 34%
in patients with cancer, 30% in patients with diabetes mellitus and
28% in patients with cardiovascular diseases.43 In IBD, there is a
wide range of prevalence of malnutrition reported in the literature,
from 12 to 85%, and this is probably due to a significant heteroge-
neity of the series regarding type of disease [CD vs UC], extent and
disease activity.44,45 In the present study there was no difference in
the prevalence of malnutrition in CD and UC patients, in agreement
with previous studies.2
The definition of malnutrition is controversial and it is con-
tinuously evolving.46,47 In the present study, a patient was classified
as having malnutrition if he/she had an SGA grade B or C, or a
BMI < 18.5 or an FFMI below the 10th percentile; therefore, nutri-
tional status was comprehensively assessed through three different
dimensions [clinical, anthropometric and body composition]. Since a
patient could have a normal BMI and still have an altered body com-
position, the definition of malnutrition is not restricted to a lower
BMI.2 We therefore decided to use three different ways to evaluate
the nutritional status and to classify a patient as malnourished if he/
she had an alteration in at least one of the evaluated dimensions.
Moreover, a comprehensive nutritional assessment seems superior to
the assessment of a single dimension status.48 Bryant et al. assessed
the nutritional status of 144 IBD patients in clinical remission, and
concluded that alterations in body composition are frequent, even
in remission, and cannot be detected by standard malnutrition
screening.2
We found that malnourished patients had a decreased hand-
grip strength compared with well-nourished patients, in agreement
with a previous study.2 Handgrip strength is considered as a reliable
marker of muscle quality, and nutritional status may influence mus-
cle quality and thus muscle strength. Many studies have shown that
muscular strength is related to the prognosis of chronic diseases.49
Therefore, the evaluation of muscular strength should probably be a
routine part of nutritional assessment.49,50
According to our results, clinical activity was associated with
malnutrition. Clinical activity has been associated with malnutri-
tion in several studies.44,51,52 Nevertheless, malnutrition may occur
in patients with mild activity and even in remission.1,9 A previous
1437
study evaluated nutritional status shortly after IBD diagnosis and
concluded that it was already affected negatively at the time of
diagnosis.48
Our results also found that history of abdominal surgery was
associated with malnutrition. Abdominal surgery due to IBD may
cause malnutrition through different mechanisms such as malab-
sorption or reduced oral intake. A nationwide study performed in
IBD patients found that having undergone resective bowel surgery
was associated with malnutrition or body weight loss.53,54
Finally, food restrictive behaviour during a flare was associated
with a higher risk of malnutrition in our study. Dietary beliefs are
one of the most important reasons why patients restrict some types
of food, as has been demonstrated in the present study. Moreover,
the majority of patients reported to have decreased appetite during
a disease flare, which, together with the food-restrictive behaviour,
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could lead to malnutrition. Furthermore, according to our results,
the majority of patients changed their dietary habits after the diag-
nosis of IBD.
These results highlight the importance of educating patients to
prevent malnutrition. This is important because malnutrition has
been associated with poorer outcomes in IBD patients.3 In fact, the
proportion of patients with malnutrition has been considered one
of the ten key quality outcome measurements for IBD.55 Therefore,
nutritional assessment should be included in routine clinical practice.
Interestingly, we found that almost half of the patients were over-
weight or obese and, of these, 8% had malnutrition. This is a rel-
evant finding, since obesity in IBD patients has been associated with
elevated inflammatory markers and a more severe clinical course in
CD patients.2 Moreover, 5% of the obese IBD patients met criteria
for sarcopenic obesity [BMI > 30 kg/m2 and a low FFMI], which is
associated with metabolic disorders and is an important cause of
disability, morbidity and mortality.56 These findings confirm that all
IBD patients should be included in the nutritional assessment. The
reasons for the lack of nutritional assessment are unclear but may be
due to underestimation of patient risk, limited visit time and a lack
of familiarity with the criteria involved in the diagnosis of malnutri-
tion.3 A multidisciplinary team of qualified personnel in nutrition
comprising gastroenterologists, nurses, dieticians and nutritionists is
necessary for providing dietary advice and support for IBD patients.
Screening for malnutrition should be performed in all IBD
patients at least once, and more frequently in those patients with
active disease or with factors associated with a higher risk of mal-
nutrition. A complete evaluation of nutritional status should include
the assessment of these three dimensions: clinical [SGA], anthropo-
metric [BMI] and body composition [BIA]. Additionally, all patients
should receive individualized dietary advice.
The present study has several limitations. First, we did not meas-
ure body composition using dual-energy X-ray absorptiometry,
which is the gold standard to evaluate body composition. However,
we used BIA, which is a simple, fast and noninvasive method to
evaluate body composition. Moreover, since BIA is accessible and is
available in all nutrition clinics, its use reflects routine clinical prac-
tice. Second, it would have been interesting to follow-up the patients
after the nutritional assessment in order to evaluate impact on their
nutritional status. Third, endoscopic activity was not evaluated at
the moment of inclusion in the study; nevertheless, we performed
a clinical assessment using the clinical validated scales for CD and
UC. Finally, there could be a bias if the majority of patients who
accepted to participate in the nutritional assessment were those who
had disease activity; however, we included consecutive patients and
the majority of them were in clinical remission or had mild activity.
1438
One of the strengths of the present study is that—to the best of
our knowledge—it is the largest cohort of patients in whom dietary
behaviours and beliefs have been evaluated. Moreover, this prospec-
tive study includes a nutritional assessment of an important number
of patients who completed the questionnaire. In addition, this is the
first study that has evaluated behaviours and beliefs of IBD patients
and their nutritional status, and which included a comprehensive
assessment of the three dimensions of nutritional status: clinical,
anthropometric and body composition.
In conclusion, the results of this large prospective multicentre
study showed that self-imposed food restrictions in IBD patients
are very frequent and favour malnutrition. Moreover, we found that
almost 20% of outpatients met malnutrition criteria. Based on these
findings, screening for malnutrition in IBD patients should be imple-
mented in routine clinical practice, as well as individualized dietary
advice, to limit the baseless beliefs of the patients and their corre-
sponding nutritional restrictive behaviours.
Funding
None.
Conflict of Interest
JPG and MC have served as speakers, consultants, and advisory members for
and have received research funding from MSD and Abbvie; XC has received
grants for research, fees for advisory boards, and lectures from Abbott and
MSD; MBdeA has served as a consultant and an advisory board member for
MSD and Abbott. All other authors: none.
Author Contributions
MJC, MC and JPG conceived and designed the study. All authors participated
in the collection of patient data. MJC, MC and JPG analysed and interpreted
the results and wrote the manuscript. All authors critically reviewed the manu-
script, and have read and approved the final version of the manuscript.
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