Clinical Nutrition xxx (2015) 1e6

Contents lists available at ScienceDirect

Clinical Nutrition
journal homepage: http://www.elsevier.com/locate/clnu

Original article

Diet adherence and gluten exposure in coeliac disease and

self-reported non-coeliac gluten sensitivity
A. Lvik a, 1, G. Skodje a, J. Bratlie b, c, M. Brottveit d, K.E.A. Lundin c, e, f, *
a
Department of Clinical Service, Division of Cancer Medicine, Surgery and Transplantation, Oslo University Hospital Rikshospitalet, Norway
b
Research Institute of Internal Medicine, Oslo University Hospital Rikshospitalet, Norway
c
Department of Gastroenterology, Oslo University Hospital Rikshospitalet, Norway
d
Department of Gastroenterology, Oslo University Hospital Ullevl, Norway
e
Centre for Immune Regulation, University of Oslo, Norway
f
Faculty of Medicine, University of Oslo, Norway

a r t i c l e i n f o s u m m a r y

Article history: Background/objectives: Adherence to gluten-free diet in self reported non-coeliac gluten sensitive sub-
Received 11 October 2015 jects is scarcely researched. Objectives of the study were to compare dietary adherence in coeliac disease
Accepted 25 November 2015 (CD) subjects and in non-coeliac gluten sensitive (NCGS) subjects, and to estimate gluten exposure based
on weighed food records and analysis of gluten content in selected food items.
Keywords: Subjects/methods: Twenty-three subjects with biopsy veried CD on a gluten-free diet and 34 HLA-DQ2
Diet adherence
NCGS subjects on a self-instituted gluten-free diet were enrolled. The latter group was under investi-
Celiac disease
gation of CD. Dietary adherence was assessed by frequency questionnaire and structured forms supplied
Non-celiac gluten sensitivity
Gluten exposure
by weighed food records. For the analyses of food samples, the sandwich R5-ELISA, Ridascreen Gliadin
Gluten contamination competitive method was used.
Results: There was no difference in dietary adherence between CD and NCGS subjects (83% vs 68%,
p 0.21). NCGS subjects were mainly self-educated in gluten-free diet compared to CD subjects (91% and
39%, respectively, p < 0.001). In non-adherent subjects, there was no difference in gluten exposure be-
tween CD and NCGS (10 vs 138 mg/day, p 0.83). There was no difference in BMR-factor between CD and
NCGS subjects, or between adherent and non-adherent subjects.
Conclusions: Both CD and NCGS subjects were largely adherent, and adherence did not differ between
the groups. Gluten exposure varied greatly, and some CD and NCGS subjects reached gluten intake above
500 mg/day, which might have considerable health effects on the individual, especially in case of coeliac
disease.
2015 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved.

1. Introduction

Coeliac disease (CD) is one of the most common inammatory

Abbreviations: ATI, amylase-trypsin inhibitor; BMI, body mass index; BMR, basal
metabolic rate; BMR-factor, energy intake and basal metabolic rate-ratio; CD,
coeliac disease; EI, energy intake; ELISA, enzyme linked immunosorbent assay;
FODMAP, fermentable oligo-di-monosaccharides and polyols; HLA, human leuco-
cyte antigen; NCGS, non-coeliac gluten sensitivity; NCWS, non-coeliac wheat
sensitivity; NIH, National Institutes of Health; NS, non statistical; PWAWG, persons
who avoid wheat and/or gluten; SPSS, Statistical Package for the Social Sciences.
* Corresponding author. Department of Gastroenterology, Oslo University Hos-
pital Rikshospitalet, Norway. Tel.: 47 23072400.
E-mail addresses: astridmargretel@gmail.com (A. Lvik), gry.skodje@ous-hf.no
(G. Skodje), jbratlie@ous-hf.no (J. Bratlie), margit.brottveit@gmail.com
(M. Brottveit), knut.lundin@medisin.uio.no (K.E.A. Lundin).
1
Present address: Nordengvn 85 D, 0755 Oslo, Norway. Tel.: 47 99439941.
diseases of the small intestine. This chronic immune-mediated
enteropathy occurs exclusively in genetically predisposed in-
dividuals after exposure to gluten. The only current treatment of CD
is a strict, life-long gluten-free diet, which usually allows the
affected mucosa to heal [1].
Gluten has also been associated with non-coeliac gluten sensi-
tivity (NCGS), a syndrome reported to be slightly more prevalent
than CD [2]. NCGS, non-coeliac wheat sensitivity (NCWS) [3] or
persons who avoid wheat and/or gluten (PWAWG) [4] are condi-
tions in which ingestion of gluten containing food leads to clinical
signs compatible with CD, but without the typical histological and
serological signs seen in CD. Increase of intraepithelial lymphocytes

http://dx.doi.org/10.1016/j.clnu.2015.11.017
0261-5614/ 2015 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved.

Please cite this article in press as: Lvik A, et al., Diet adherence and gluten exposure in coeliac disease and self-reported non-coeliac gluten
sensitivity, Clinical Nutrition (2015), http://dx.doi.org/10.1016/j.clnu.2015.11.017
2 A. Lvik et al. / Clinical Nutrition xxx (2015) 1e6

and increased IgG to gluten is frequently seen but these tests are
not diagnostic for the condition [5]. However, the underlying
mechanisms are unknown, and the reports on effect of gluten
withdrawal in subjects with self-reported NCGS are conicting
[6e8]. It has been suggested that the symptoms could be caused by
intolerance to fermentable oligo-, di-, monosaccharides, and poly-
ols (FODMAP) [7] or amylase-trypsin inhibitors (ATI) [9], which
coexist with gluten in wheat.
Adherence to a gluten-free diet is of crucial importance for
successful treatment of CD. Poor adherence could hamper sufcient
restitution of the intestinal mucosa and reduce some protection
against development of autoimmune co-morbidities, possibly
resulting in an increased need for health care [10,11]. A systematic
review indicates rates of strict dietary adherence in CD patients to
be 44e90% [12]. Adherence in NCGS is largely unknown.
The primary objectives of this study were to assess diet adher-
ence and gluten exposure in CD and NCGS subjects.
This study compares adherence in two groups depending on
gluten-free diet. Estimation of gluten exposure is based on weighed
food records and gluten analysis of food samples. This allows a
precise quantication of gluten exposure.
2. Materials and methods
2.1. Subjects
We compared two groups of subjects. The HLA-DQ2 CD pa-
tients (one HLA-DQ8) diagnosed according to NIH 2004 criteria
[13] were recruited from outpatient clinics at Oslo University
Hospital (n 11) and through Norwegian Coeliac Society by ad-
vertisements (n 13). These patients (mean age 43, range 18e65
years) are referred to as CD subjects. Most of the perceived gluten
sensitive HLA-DQ2 persons (n 35) on a self-instituted gluten-
free diet were recruited by advertisement in a daily newspaper and
investigated as described elsewhere [14]. Previously the cohort
(mean age 41, range 17e65 years) had not been properly investi-
gated for CD. During work up three of the gluten sensitive persons
were diagnosed as CD patients [14]. However, in this paper they are
included in the NCGS cohort. Both groups were investigated by
clinical and nutritional examination before inclusion. Specic di-
agnoses or diet avoidances are summarised in Table 1. Threshold
values of specic IgE to wheat was found in one of 33 examined
subjects as documented elsewhere [14]. We also know that 26% of
the NCGS subjects in Brottveit et al., which is also part of this ma-
terial, fullled the Rome II criteria retrospectively for IBS [15]. Their
symptoms at inclusion were scored by GSRS-IBS and SHC formulas.
All NCGS subjects reported symptom relief on gluten-free diet.
Morphology, immune response and symptoms after gluten chal-
lenge in the cohort are published elsewhere [14e16].
One CD and one NCGS subjects were reluctant to be interviewed.
Thus 23 CD subjects and 34 NCGS subjects were included in the study.
2.2. Dietary assessment
Subjects were interviewed about their meal situation, and their
use of gluten-free and naturally gluten-free products, by means of a
frequency questionnaire and standardised questions related to diet
understanding and diet practice, i.e.: Why did you start gluten-free
diet? and Do you get symptoms when tasting gluten containing
food?
After thorough instruction, subjects recorded their food intake
(weighed food records) for three consecutive days (one week-end-
day, two working days). They were told to maintain their usual
gluten-free diet and to record recipes and brand names of all
products consumed.
Adherence to gluten-free diet was graded into four categories:
good, fair, poor and non-adherent. Good adherence was based on
intake of always known gluten-free food ingredients when eating
at home and away from home, always checking of labels, and no
voluntary transgression. Fair adherence included possible risks like
less checking of ingredients, and no asking for ingredients in menus
when eating out. Poor adherence included additional obvious risks
like consuming food of unknown composition, tasting of gluten
containing food or having regular beer weekly or more frequently.
When eating regular meals in periods, the subjects were considered
non-adherent. In the statistical analysis good and fair adherence
were recoded into adherent, and poor and non-adherent were
recoded into non-adherent. Reported intakes of regular food used
less frequently than once a month, were not included in the cal-
culations of gluten exposure. Energy intake was calculated by
means of the Norwegian Food Composition Table (http://www.
matvaretabellen.no/).
Underreporting of food intake was assessed by calculated en-
ergy intake (EI) and calculated basal metabolic rate (BMR). The cut-
off point of BMR-factor (EI/BMR-ratio) for the relevant number of
subjects and days of records was chosen [17]. A BMR-factor less
than 1.47 was considered as underreported food intake.
2.3. Prolamin analyses and gluten calculations
Random sampling of grain, ours, seeds, bread mixes, products
labelled gluten-free or naturally gluten-free products (n 105),

Table 1
Characteristics by mean (SD) and median (Q1, Q3).

CD (n 23) NCGS (n 34) p-Value Male (n 11) Female (n 46) p-Value

Age (years) 43 (41) 41 (14) 0.50 38 (15) 43 (13) 0.28a

BMI (kg/m2) 23 (3) 24 (4) 0.55 23 (3) 24 (4) 0.87a
Months on gluten-free diet 19 (12, 48) 15 (7, 28) 0.21 15 (8, 33) 16 (9, 75) 0.62a
Subjects sharing meals n (%) 18 (78) 21 (62) 0.27 7 (64) 33 (72) 0.59b
Avoiding milk n (%) 6 (26) 13 (38) 0.55 2 (18) 17 (37) 0.19b
Avoiding other foods n (%)e 5 (22) 11 (32) 0.38 4 (36) 12 (26) 0.49b
Total meals per day 5.2 (0.9) 4.9 (1.0) 0.25 4.8 (0.6) 5.1 (1.0) 0.49a
Bread meals per day 2.2 (0.8)c 1.8 (1.0)d 0.13 2.0 (0.6) 1.9 (1.0) 0.72a
Diabetes mellitus n (%) 2 (9) 0 0.16 1 (9) 1 (2) 0.35b
Thyroid disease n (%) 2 (9) 2 (6) 1.00 0 4 (9) 0.58b

Abbreviations: SD, standard deviation; CD, coeliac disease; NCGS, non-coeliac gluten sensitivity; BMI, body mass index; GF, gluten-free.
a
T-test for equality of means.
b
Chi square or Fisher exact test.
c
n 21.
d
n 32.
e
Nut, shellsh, apple, egg.

Please cite this article in press as: Lvik A, et al., Diet adherence and gluten exposure in coeliac disease and self-reported non-coeliac gluten
sensitivity, Clinical Nutrition (2015), http://dx.doi.org/10.1016/j.clnu.2015.11.017
 A. Lvik et al. / Clinical Nutrition xxx (2015) 1e6
was done at regular food markets and special food stores in central
parts of Oslo. Some samples of hospital made (n 5) and patient
made bread (n 2) were included in the analysis. Each food item
was transferred into plastic bags, sealed, marked and stored at a
cool or freezing temperature. Bottles of beer were opened and
poured into glass containers just before analysis.
For the rst 51 samples (49 gluten-free products and two
samples of regular white bread), the sandwich R5-ELISA
Ridascreen Gliadin competitive method (Art. No. R7011) which
quanties prolamin, was used. For the two parallels of each sample
the kit instructions were followed for each step of the sample
preparation and the analysing procedure. The peptide (prolamin)
concentration (mg/ml) corresponding to absorbance of each sample
was read from the calibration curve. To obtain the peptide con-
centration in mg/kg actually contained in each sample, the con-
centration read from the calibration curve was further multiplied
by the dilution factor 500 (mg/L mg/kg). Conversion to gliadin
(mg/g) needed the peptide concentration divided by 250. The
company's revised version of the analysis kit (Art. No. R7021) which
quanties gliadin with the same antibody was used for the
remaining samples (n 54 including 32 regular gluten containing
products). The gliadin concentration (ng/ml) read from the cali-
bration curve was multiplied by the dilution factor 500 to express
the gliadin concentration of each sample as mg/kg. In both pro-
cedures gliadin level (mg/kg) in each sample was multiplied by two
to give the gluten concentration (mg/kg). Non-detectable concen-
trations were set at less than 5 mg gluten/kg.
Both assays are considered suitable for quantitative determi-
nation of prolamins from wheat, rye and barley. The immune-active
sequence in fermented as well as hydrolysed prolamins including
beer, are recognized by both methods. However, the prolamins in
beer are incompletely extracted from barley [18]. In the calculations
of the gluten exposure the mean of the duplicate analysed gluten
values was used.
2.4. Statistical analysis
Statistical analysis was performed by of SPSS 22.0 for Windows,
SPSS Inc. The normally distributed data as age and BMI were ana-
lysed by t-test for equality of means. ManneWhitney U-test or
Pearson Chi-square was used for analysing non-parametric data as
gluten intake and grade of adherence. A statistical probability of
0.05 was considered signicant.
2.5. Ethical considerations
The clinical part of the study was approved by the Regional
Committee for Medical Research Ethics (REK Sr/st) and the Pri-
vacy Ombudsman for Research at Oslo University Hospital, and
registered at http://clinicaltrials.gov/(NCT01100099). Signed
informed consent was obtained from each participant.
3. Results
Background characteristics were comparable (Table 1), although
women were slightly more frequent among NCGS subjects than
among CD subjects (30 of 34 and 16 of 23 respectively, Chi Square,
p 0.08).
3.1. Gluten-free diet adherence, symptoms and serology
The sources to the weekly or monthly consumption of gluten
were beer, wheat our in home made wafes or pizza, bread or
spelt bread. Although the difference was non-signicant, CD sub-
jects showed a higher grade of adherence by professional
Please cite this article in press as: Lvik A, et al., Diet adherence and gluten exposure in coeliac disease and self-reported non-coeliac gluten
sensitivity, Clinical Nutrition (2015), http://dx.doi.org/10.1016/j.clnu.2015.11.017
3
assessment compared to NCGS subjects. There was a better agree-
ment between professional and patient adherence assessment
among CD patients than in NCGS subjects. Professional counselling
of gluten-free diet was most frequent in CD patients, while most of
the NCGS subjects were self-educated (Table 2).
Four subjects (2 CD and 2 NCGS subjects) excluded gluten-free
bread from their diet (Table 1) because of low taste quality of
gluten-free bread (n 2) or adherence to low carbohydrate intake
(n 2). Five subjects (2 CD and 3 NCGS subjects) reported use of
regular beer as well as gluten-free beer, and two CD subjects
consumed regular beer (pilsner type) exclusively (Table S1
Supplemental).
Four of 22 CD subjects (1 missing) experienced gastrointestinal
symptoms when tasting gluten, eight of 22 had no symptoms and
10 did not know their reaction. All the NCGS subjects reported
symptom relief as reason for gluten-free diet. Four of 34 subjects
had extra-intestinal symptoms (depression, joint pain, asthenia,
blurred vision, perspiration). Most subjects (28/34) had symptoms
when tasting gluten, 3/34 had no symptoms and another 3/34 did
not know their response. The appearance of symptoms was not
different between the groups, neither by diagnosis, nor by adher-
ence (data not shown).
Median anti-tTG2-level did not differ between adherent and
non-adherent in NCGS subjects (0.4 U/L (0.2, 0.8) vs 0.2 U/L (0.2,
0.6), p 0.06 by ManneWhitney test) or in CD patients (1.1 (0.5,
3.4) vs 0.4 (0.3, 4.6), p 0.41 by ManneWhitney).
3.2. Gluten contamination
All labelled gluten-free foods were conrmed to contain <20 mg
gluten/kg, 63% without detectable gluten (<5 mg/kg) (Table S2
Supplemental). Except for two samples of soy our and one sam-
ple of puffed oats, naturally gluten-free products and oat products
were conrmed gluten-free (<20 mg/kg) (Table S3 Supplemental).
One brand of beer formerly considered gluten-free was found to be
of very low gluten content according to the guidelines of The
Norwegian Food Safety Authority (Table S1 Supplemental). Less
frequently used gluten sources as wheat our in cookies, barley
our in cakes and bread crumbles, were not analysed and not
included in gluten contamination calculations.
3.3. Gluten level in regular bread
The gluten level varied thirteen-fold (14 000e181 400 mg/kg) in
samples from 10 different brands of regular white bread (n 11)
and more than ve-fold (30 400e165 800 mg/kg) in 8 different
brands of regular whole grain bread (n 20). Within the same
brand of bread the gluten level showed a 30e100% variation.
Several samples of bread contained gluten (181 400, 165 800 and
149 800 mg/kg) close to the amount found in regular wheat our
Table 2
Diet adherence professionally vs self-assessed, and professional vs self-education in
gluten-free diet.
CD (n 23) NCGS (n 34) p-Valuea
% (n) % (n)
Adherent subjects:
Professionally assessed (n 42) 83 (19) 68 (23) 0.21b
Self-assessed (n 51) 87 (20) 91 (31) 0.68b
Dietary education:
Professionally instructed (n 17) 61 (14) 9 (3) <0.001
Self-educated (n 40) 39 (9) 91 (31)
Abbreviations: CD, coeliac disease; NCGS, non-coeliac gluten sensitivity.
a
Chi-Square.
b
CD vs NCGS.
4 A. Lvik et al. / Clinical Nutrition xxx (2015) 1e6
(160 600 mg/kg) (Fig. 1). Bread added gluten powder did not differ
in gluten content from bread without added gluten powder
(80 508 mg/kg (SD 41 577) vs 47 033 mg/kg (SD 24 858), p 0.07 by
Independent samples) (Fig. 1). The analysed gluten powder (Val-
idus) in this study contained 3.6 times (580 000 mg/kg) the gluten
level found in analysed wheat our. However, the gluten concen-
tration of Validus gluten powder was lower than labelled (57% vs
75e80% gluten).
3.4. Underreporting of food intake
Forty-seven of 57 subjects (20 CD and 27 NCGS subjects)
recorded their food intake. The degree of underreported (BMR-
factor < 1.47) food intake was higher (16.3%) in the CD group
compared to the NCGS group (10.2%) (Table 3), but not signicantly
different between the groups (p 0.9 by Independent samples
median test). Further, the adherent group underreported more
(14.3%) than the non-adherent group (7.5%) (p 0.9 by Indepen-
dent samples median test).
3.5. Gluten exposure in non-adherent subjects
In the non-adherent NCGS group (n 15) two subjects did not
quantify their gluten intake. One CD patient quantied the intake of
regular beer, although the dietary intake was not recorded. Gluten
exposure did not differ between diagnoses, gender or adherence,
although CD subjects consumed less gluten than NCGS subjects
(Table 4). In total, 8 of 13 non-adherent subjects consumed more
than 10 mg gluten per day, of those two CD subjects.
At inclusion, one regular beer consuming CD patient presented
mucosa damage (Marsh 3A) by intestinal biopsy. One NCGS person
with mucosa lesions (Marsh 3B) later appeared to have coeliac
disease (Table 4).
4. Discussion
Here we report that both CD and NCGS subjects are largely
adherent, but transgressions occur. NCGS subjects seem to cope
well with gluten-free diet although most of them are self-
educated. Gluten exposure varied greatly in both groups, and
both CD and NCGS subjects reached gluten intake above 500 mg/
day.
Fig. 1. Gluten (mg/kg) in regular bread with (n 25) and without (n 6) added gluten
powder, Independent samples p 0.07.
Please cite this article in press as: Lvik A, et al., Diet adherence and gluten exposure in coeliac disease and self-reported non-coeliac gluten
sensitivity, Clinical Nutrition (2015), http://dx.doi.org/10.1016/j.clnu.2015.11.017
4.1. Adherence
Adherence to gluten-free diet did not differ between CD and
NCGS subjects. Our study was performed before Lefer's Celiac
Dietary Adherence Test [19] and Biagi's validated questionnaire
[20] were published. The different categories of adherence in this
study (good, fair, poor and non-compliance) were based on a
standardized dietician evaluation of each individual. This method is
thorough but of limited access, given the low number of dieticians
skilled in treating celiac disease.
The high frequency of good adherence in CD subjects (83%) in
our study was in accordance with existing knowledge [12] and did
not differ from self-educated NCGS subjects (68%). Different
adherence between the groups would not have been surprising,
given different motivation for starting a gluten-free diet and the
well dened importance of diet adherence in coeliac disease. One
could expect poorer adherence in NCGS, given the lack of conrmed
diagnosis, self-education and possibly higher tolerance threshold
for gluten exposure than coeliac disease.
If underreporting of food intake is not taken into account, we
may suggest that self-education of gluten-free diet is sufcient in
some patients [21]. If, however, the underreporting is considered,
our results show that CD subjects report less of their actual food
intake than NCGS subjects (Table 3). We do not know if gluten
sources are the underreported food. Given that CD subjects in our
study were mostly professionally instructed in gluten-free diet
(Table 2), it could be more important to appear adherent than for
the NCGS subjects.
4.2. Gluten contamination
We still have no complete overview of the possible sources of
gluten contamination in a gluten-free diet [22]. As the number of
contaminated products (5%) was less than documented by other
reports (9.5e32%) [23,24], our study indicated a safe basic gluten-
free food selection in the sampling region. This state of affairs
probably extends to the whole country, since the most frequently
used gluten-free products (bread our, bread, pasta, etc.) are made
by national or multi-national companies.
Except for one brand of soy our and one sample of puffed
oats, the naturally gluten-free products and the labelled gluten-
free products were conrmed gluten-free. Only two of seven
regular-beer consumers exceeded 10 mg of gluten intake/day
while the regular food consumers were exposed to more than
100 mg/day.
The 13-fold variation of gluten content in white bread is
important knowledge obtained from this study. Gluten challenge
by a certain number of slices of white bread may give highly
variable gluten loads. According to the calculation method sug-
gested by others [25] and actual vegetable protein content in
regular bread (http://www.kostplanleggeren.no/) the expected
gluten level in regular white bread and regular whole grain bread
would be 6.6 g gluten/100 g and 7.0 g gluten/100 g respectively.
Both CD and NCGS subjects shared more than one bread meal per
day with persons eating regular bread. Norwegians eat more
bread compared to other Nordic countries [26] and so do CD
patients [27].
With more than two times the expected level of gluten in certain
brands of regular bread, as shown in this study, the risk of
contamination may be considerable. For the same reason, tasting of
regular bread could have more serious consequences than ex-
pected, especially for CD subjects. Voluntary transgression could be
reduced with improved palatability, increased variety and avail-
ability of the gluten-free bread, as well as better diet counselling
[28].
 A. Lvik et al. / Clinical Nutrition xxx (2015) 1e6 5

Table 3
BMR-factor (energy intake/BMR ratio) by median (Q1, Q3).

CD (n 20)a NCGS (n 27)b p-Valuec Adherent (n 34) Non-adherent (n 13) p-Valuec

1.23 (0.98, 1.67) 1.32 (1.10, 1.44) 0.87 1.26 (1.04, 1.46) 1.36 (1.04, 1.62) 0.93

Abbreviations: BMR, basal metabolic rate; CD, coeliac disease; NCGS, non-coeliac gluten sensitivity.
a
Three missing food records.
b
Seven missing food records.
c
Independent samples median test.

Table 4
Gluten exposure (n 13) and mucosa status in professionally assessed non-adherent subjects on strict and non-strict diet (n 15).

Gluten exposure mg/day p-Values Mucosa status and corresponding gluten sources
Median (Q1, Q3)

Strict diet (n 9)a 6.6 (3.5, 160) 0.18b Marsh 0 (7): beer (4), on/off diet (2), spelt bread (1)
Marsh 1 (1): pizza (1)
Marsh 3A (1): beer (1)
Non-strict diet (n 6) 210.5 (11.0, 1034.0) Marsh 0 (5): beer (2), pizza (2), wafes (1)
Marsh 3B (1): bread (1)
CD (n 4) 10.0 (4.5, 607.2) 0.83c Marsh 0 (3): beer (2), pizza (1)
Marsh 3A (1): beer (1)
NCGS (n 11)d 137.7 (4.4, 543.2) Marsh 0 (9): beer (4), pizza (1), on/off diet (2), wafes (1), spelt bread (1)
Marsh 1 (1): pizza (1)
Marsh 3B (1): bread (1)

Abbreviations: CD, coeliac disease; NCGS, non-coeliac gluten sensitivity.

a
n 7 in calculations of gluten intake.
b
ManneWhitney: Strict vs non-strict diet.
c
Mann-Whitney: CD vs NCGS.
d
n 9 in calculations of gluten intake.

4.3. Gluten exposure in non-adherent subjects
A healed intestinal mucosa in most regular food or regular-beer
consumers could reect a safe level of gluten intake in the CD
group. Another explanation of a normal mucosa could be a stricter
dietary adherence the last weeks before inclusion [14]. We do not
know if the damaged intestinal mucosa (Marsh 3A) in the regular-
beer consuming CD patient was due to the gluten exposure from
beer, from additional gluten intake or from a slowly recovering
mucosa during dietary treatment (48 months).
In case of coeliac disease, tasting of gluten containing food or
food of unknown composition is not recommended. Also high
quantities of food of very low gluten content, for instance regular-
beer, could easily exceed less than 50 mg gluten/day, a threshold
often referred to by several authors discussing the safe level of
gluten intake for CD patients (10e100 mg/day) [1]. The fact that
intake of regular cereal products was not regarded as an obvious
gluten exposure by all patients could indicate lack of knowledge,
lack of diet understanding or a diet philosophy that allows some
gluten in a gluten-free diet. Using labelled gluten-free products
(20 mg/kg) exclusively in the gluten-free diet seems to guarantee
a daily gluten exposure of less than 10 mg per day and a possible
absence of health risks from contamination [29].
Excellent dietary adherence could even give an advantage of
improved cognitive performance as indicated for CD subjects in
Lichtwark et al. [30]. Others suggest that strict gluten-free diet is
especially important to CD patients with high sensitivity [31].
An increased number of subjects in each gluten-consuming
gender group could give the results more power. That would
increase the number of diet recordings from the subjects, and the
variety and number of analysed foods in the quantication of
gluten intake. The conrmation of a NCGS diagnosis should
include a blinded placebo controlled investigation as suggested
by the Salerno Expert group [32]. However, compared to the
diagnostic model suggested by Kabbani et al. [33], the investi-
gation of this NCGS cohort was taken a step further by a 3-day
open gluten challenge to conrm the diagnosis [16]. Also
special for this cohort is that all subjects had the same HLA-
genetics. Positive HLA-DQ2-gliadin tetramer test after gluten
challenge indicated coeliac disease [14]. Non-gluten related
conditions might be present in the cohort [4]. A 3-day open
gluten challenge is both short and subjective, and cannot exclude
reactions to FODMAPs or ATIs.
Unique for this study is the comparison of diet adherence in two
different populations using gluten-free diet as treatment. A quan-
tication of gluten exposure is also rarely described.
In conclusion, diet adherence does not differ between CD and
NCGS subjects. Diet adherence appears to be quite good in NCGS
subjects even though most of them are self-educated in gluten-
free diet. Daily gluten exposure is considerable in some non-
adherent subjects, and could have important effect on the indi-
vidual patient, especially in case of coeliac disease. This study
reveals a need for extended knowledge about the actual gluten
content in cereal products, which are the most dominating gluten
source in voluntary transgression. It is also important to further
explore the role of gluten-free diet in non-coeliac gluten
sensitivity.
Conict of interest
None declared.
Acknowledgement
We thank the participants for their enthusiasm and patience,
and the Norwegian Coeliac Society for providing advertisements
and funding.
Appendix A. Supplementary data
Supplementary data related to this article can be found at http://
dx.doi.org/10.1016/j.clnu.2015.11.017.

Please cite this article in press as: Lvik A, et al., Diet adherence and gluten exposure in coeliac disease and self-reported non-coeliac gluten
sensitivity, Clinical Nutrition (2015), http://dx.doi.org/10.1016/j.clnu.2015.11.017
6 A. Lvik et al. / Clinical Nutrition xxx (2015) 1e6

References determine gliadin in gluten-free food. Eur J Gastroenterol Hepatol

2005;17(10):1053e63.
[19] Lefer DA, Dennis M, Edwards George JB, Jamma S, Magge S, Cook EF, et al.
[1] Ludvigsson JF, Bai JC, Biagi F, Card TR, Ciacci C, Ciclitira PJ, et al. Diagnosis and
A simple validated gluten-free diet adherence survey for adults with celiac
management of adult coeliac disease: guidelines from the British Society of
disease. Clin Gastroenterol Hepatol Off Clin Pract J Am Gastroenterol Assoc
Gastroenterology. Gut 2014;63(8):1210e28.
2009;7(5):530e6. 6 e1e2.
[2] Volta U, Bardella MT, Calabro A, Troncone R, Corazza GR. An Italian prospec-
[20] Biagi F, Bianchi PI, Marchese A, Trotta L, Vattiato C, Balduzzi D, et al. A score
tive multicenter survey on patients suspected of having non-celiac gluten
that veries adherence to a gluten-free diet: a cross-sectional, multicentre
sensitivity. BMC Med 2014;12:85.
validation in real clinical life. Br J Nutr 2012;108(10):1884e8.
[3] Carroccio A, Rini G, Mansueto P. Non-celiac wheat sensitivity is a more
[21] Mahadev S, Simpson S, Lebwohl B, Lewis SK, Tennyson CA, Green PH. Is die-
appropriate label than non-celiac gluten sensitivity. Gastroenterology
titian use associated with celiac disease outcomes? Nutrients 2013;5(5):
2014;146(1):320e1.
1585e94.
[4] Tavakkoli A, Lewis SK, Tennyson CA, Lebwohl B, Green PH. Characteristics of
[22] Razzaq HA, Sutton KH, Motoi L. Altering the rate of glucose release from
patients who avoid wheat and/or gluten in the absence of celiac disease. Dig
starch-based foods by spray-drying with an extract from barley. J Sci Food
Dis Sci 2014;59(6):1255e61.
Agric 2013;93(11):2654e9.
[5] Volta U, Di Giorgio R, Henriksen C, Skodje GI, Lundin KE. Non-celiac gluten
[23] Thompson T, Lee AR, Grace T. Gluten contamination of grains, seeds, and
sensitivity: a work-in-progress entity in the spectrum of wheat-related dis-
ours in the United States: a pilot study. J Am Diet Assoc 2010;110(6):
orders. Best Pract Res Clin Gastroenterol 2015;29:477e91.
937e40.
[6] Biesiekierski JR, Newnham ED, Irving PM, Barrett JS, Haines M, Doecke JD,
[24] Koerner TB, Cleroux C, Poirier C, Cantin I, La Vieille S, Hayward S, et al. Gluten
et al. Gluten causes gastrointestinal symptoms in subjects without celiac
contamination of naturally gluten-free ours and starches used by Canadians
disease: a double-blind randomized placebo-controlled trial. Am J Gastro-
with celiac disease. Food Addit Contam Part A Chem Anal Control, Expo Risk
enterol 2011;106(3):508e14. quiz 15.
Assess 2013;30(12):2017e21.
[7] Biesiekierski JR, Peters SL, Newnham ED, Rosella O, Muir JG, Gibson PR. No
[25] van Overbeek FM, Uil-Dieterman IG, Mol IW, Kohler-Brands L, Heymans HS,
effects of gluten in patients with self-reported non-celiac gluten sensitivity
Mulder CJ. The daily gluten intake in relatives of patients with coeliac disease
after dietary reduction of fermentable, poorly absorbed, short-chain carbo-
compared with that of the general Dutch population. Eur J Gastroenterol
hydrates. Gastroenterology 2013;145(2):320e8. e1e3.
Hepatol 1997;9(11):1097e9.
[8] Lundin KE, Alaedini A. Non-celiac gluten sensitivity. Gastrointest Endosc Clin
[26] Kyro C, Skeie G, Dragsted LO, Christensen J, Overvad K, Hallmans G, et al.
N Am 2012;22(4):723e34.
Intake of whole grain in Scandinavia: intake, sources and compliance with
[9] Schuppan D, Zevallos V. Wheat amylase trypsin inhibitors as nutritional ac-
new national recommendations. Scand J Public Health 2012;40(1):76e84.
tivators of innate immunity. Dig Dis 2015;33(2):260e3.
[27] Lovik A, Gjoen AU, Morkrid L, Guttormsen V, Ueland TL, Lundin KE. Oats in a
[10] Bai JC, Fried M, Corazza GR, Schuppan D, Farthing M, Catassi C, et al. World
strict gluten-free diet is associated with decreased gluten intake and
gastroenterology organisation global guidelines on celiac disease. J Clin Gas-
increased serum bilirubin. Eur J Clin Nutr Metab (4)2009:e315e20. http://
troenterol 2013;47(2):121e6.
dx.doi.org/10.1016/j.eclnm.2009.09.002.
[11] Lundin KE, Wijmenga C. Coeliac disease and autoimmune disease-genetic
[28] do Nascimento AB, Fiates GM, dos Anjos A, Teixeira E. Gluten-free is not
overlap and screening. Nat Rev Gastroenterol Hepatol 2015;12(9):507e15.
enough e perception and suggestions of celiac consumers. Int J Food Sci Nutr
[12] Hall NJ, Rubin G, Charnock A. Systematic review: adherence to a gluten-free
2014;65(4):394e8.
diet in adult patients with coeliac disease. Aliment Pharmacol Ther
[29] La Vieille S, Dubois S, Hayward S, Koerner TB. Estimated levels of gluten
2009;30(4):315e30.
incidentally present in a Canadian gluten-free diet. Nutrients 2014;6(2):
[13] James SP. National institutes of health consensus development conference
881e96.
statement on celiac disease, June 28e30, 2004. Gastroenterology
[30] Lichtwark IT, Newnham ED, Robinson SR, Shepherd SJ, Hosking P, Gibson PR,
2005;128(4):S1e9.
et al. Cognitive impairment in coeliac disease improves on a gluten-free diet
[14] Brottveit M, Raki M, Bergseng E, Fallang LE, Simonsen B, Lovik A, et al.
and correlates with histological and serological indices of disease severity.
Assessing possible celiac disease by an HLA-DQ2-gliadin tetramer test. Am J
Aliment Pharmacol Ther 2014;40(2):160e70.
Gastroenterol 2011;106(7):1318e24.
[31] Hollon JR, Cureton PA, Martin ML, Puppa EL, Fasano A. Trace gluten contam-
[15] Brottveit M, Vandvik PO, Wojniusz S, Lovik A, Lundin KE, Boye B. Absence of
ination may play a role in mucosal and clinical recovery in a subgroup of diet-
somatization in non-coeliac gluten sensitivity. Scand J Gastroenterol
adherent non-responsive celiac disease patients. BMC Gastroenterol 2013;13:
2012;47(7):770e7.
40.
[16] Brottveit M, Beitnes AC, Tollefsen S, Bratlie JE, Jahnsen FL, Johansen FE, et al.
[32] Catassi C, Elli L, Bonaz B, Bouma G, Carroccio A, Castillejo G, et al. How the
Mucosal cytokine response after short-term gluten challenge in celiac disease
diagnosis of non-celiac gluten sensitivity (NCGS) should be conrmed: the
and non-celiac gluten sensitivity. Am J Gastroenterol 2013;108(5):842e50.
Salerno experts' criteria. Nutrients 2015;7:4966e77.
[17] Black AE. Critical evaluation of energy intake using the Goldberg cut-off for
[33] Kabbani TA, Vanga RR, Lefer DA, Villafuerte-Galvez J, Pallav K, Hansen J, et al.
energy intake: basal metabolic rate. A practical guide to its calculation, use
Celiac disease or non-celiac gluten sensitivity? An approach to clinical dif-
and limitations. Int J Obes Relat Metab Disord 2000;24(9):1119e30.
ferential diagnosis. Am J Gastroenterol 2014;109(5):741e6. quiz 7.
[18] Mendez E, Vela C, Immer U, Janssen FW. Report of a collaborative trial to
investigate the performance of the R5 enzyme linked immunoassay to

Please cite this article in press as: Lvik A, et al., Diet adherence and gluten exposure in coeliac disease and self-reported non-coeliac gluten
sensitivity, Clinical Nutrition (2015), http://dx.doi.org/10.1016/j.clnu.2015.11.017