Norstrm et al.

BMC Gastroenterology 2012, 12:125

http://www.biomedcentral.com/1471-230X/12/125

RESEARCH ARTICLE

Open Access

A gluten-free diet effectively reduces symptoms

and health care consumption in a Swedish celiac
disease population
Fredrik Norstrm1*, Olof Sandstrm1,2, Lars Lindholm1 and Anneli Ivarsson1

Abstract
Background: A gluten-free diet is the only available treatment for celiac disease. Our aim was to investigate the
effect of a gluten-free diet on celiac disease related symptoms, health care consumption, and the risk of developing
associated immune-mediated diseases.
Methods: A questionnaire was sent to 1,560 randomly selected members of the Swedish Society for Coeliacs,
divided into equal-sized age- and sex strata; 1,031 (66%) responded. Self-reported symptoms, health care
consumption (measured by health care visits and hospitalization days), and missed working days were reported
both for the year prior to diagnosis (normal diet) and the year prior to receiving the questionnaire while
undergoing treatment with a gluten-free diet. Associated immune-mediated diseases (diabetes mellitus type 1,
rheumatic disease, thyroid disease, vitiligo, alopecia areata and inflammatory bowel disease) were self-reported
including the year of diagnosis.
Results: All investigated symptoms except joint pain improved after diagnosis and initiated gluten-free diet. Both
health care consumption and missed working days decreased. Associated immune-mediated diseases were
diagnosed equally often before and after celiac disease diagnosis.
Conclusions: Initiated treatment with a gluten-free diet improves the situation for celiac disease patients in terms
of reduced symptoms and health care consumption. An earlier celiac disease diagnosis is therefore of great
importance.

Background
In celiac disease (CD), gluten triggers an autoimmune
reaction in the small intestinal mucosa which results in
inflammation, villous atrophy, and malabsorption. A
gluten-free diet is the only effective treatment for CD,
and it usually results in recovery of the small intestinal
mucosa [1].
During the last 30 years the clinical spectrum of CD has
changed from mainly being comprised of young children
with overt malabsorption to often affecting adults, with
mild or atypical symptoms, and some of those diagnosed
with the disease are even asymptomatic [2]. Despite an
increased awareness of symptoms related to CD, the delay
from the first appearance of CD related symptoms to
* Correspondence: [email protected]
1
Department of Public Health and Clinical Medicine, Epidemiology and
Global Health, Ume University, Ume, Sweden
Full list of author information is available at the end of the article

diagnosis is still long [3-5]. Economic consequences of CD

for individuals and society have undergone little study. It
has been shown, however, that the cost of food for CD
patients is higher than for non-CD persons [6], and that
women with CD consume more health care than other
women [7]. CD diagnosis and treatment has also been
shown to decrease the costs for medical care in the United
States, suggesting that a diagnosis can convey economic
savings for society [8,9]. There is an association between
CD and other immune-mediated diseases, with CD being
more prevalent among diabetes mellitus type 1 and thyroid disease patients [10-12] and inflammatory bowel disease and thyroid disease being more prevalent among CD
patients [13-15]. A protective effect of a gluten-free diet
on the risk of developing these related diseases has been
proposed [16,17], but there is uncertainty in this regard
[15,18-20].

2012 Norstrm et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative
Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and
reproduction in any medium, provided the original work is properly cited.

Norstrm et al. BMC Gastroenterology 2012, 12:125

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The aim of this study was to investigate the effect of a

gluten-free diet on CD related symptoms, health care
consumption, and the risk of developing associated
immune-mediated diseases.

as well as more details about inclusion criteria, are available in a previous publication from the questionnaire
study [5]. Questionnaires were scanned and checked for
consistency.

Methods

The questionnaire

Study design

The questionnaire included sections covering selfreported symptoms, health care consumption, missed
working days, and self-reported diseases. For each symptom (listed in Figure 1) there were five possible answers,
which were dichotomized to major (often and always) and minor severity (never, rarely, and sometimes). Health care consumption included number of
health care visits, hospitalization days, and drug use.
Missed working days also included missed school days
and similar circumstances. For both symptoms, health
care consumption, and missed working days the respondents were asked about the situation both the year prior
to initiated treatment for CD, referred to as pre-treatment,
as well as the year prior to responding to the questionnaire, referred to as today. Regarding drug use, respondents were asked if their CD diagnosis and gluten-free
diet had resulted in them being able to stop taking any
medication.
Respondents reported whether they had the following
immune-mediated diseases: diabetes (both insulin and
non-insulin dependent; the latter is not autoimmune in
nature), rheumatic disease, thyroid disease, vitiligo, alopecia areata, or inflammatory bowel disease. Regarding these
diseases the respondents were also asked for the year of
diagnosis. As respondents were asked about insulin or
non-insulin dependent diabetes, we cannot with certainty
differentiate between diabetes mellitus type 1 and 2.

A cross-sectional questionnaire survey among Swedish

adults with CD was performed during 2009 [5]. The
questionnaire was approved by the Regional Ethical Review Board at Ume University and an English translation is available online at Biomed Central [21].
Subjects

We invited randomly selected members of the Swedish

Society for Coeliacs to respond to a postal questionnaire
administered by the Society, and when needed three
reminders were sent. The Society represents about 60%
of Swedish CD patients [5]. A questionnaire was sent to
65 males and 65 females with reported CD in five-year
age intervals from 20 years of age and above (2024,
2529, . . ., 7074, and 75 years or older), totaling 1,560
members. There were 1,031 (66%) eligible responses to
the questionnaire. Members self-report their CD diagnosis when joining the Society. As the diagnosis is not verified by the Society, we used information from the
questionnaire about how members were diagnosed
(blood sample, biopsy, and/or diet change) and if they
were recommended adherence to a gluten-free diet by a
medical professional. We excluded 91 questionnaires
where either a CD diagnosis could not be verified or age
and/or sex were not consistent with information in the
member register of the society [5]. We defined 288
responders as diagnosed due to screening of CD risk
groups. For them the primary investigation for CD was
based on a disease with a known relationship to CD or
due to heredity for CD. Among responders, 96%
reported a strict compliance with a gluten-free diet, 52%
(n = 536) were women, and the mean age was 52 years
(Table 1). More characteristics of the study population,

Statistical analysis

Results are presented using descriptive statistics. The signtest was used for comparisons between pre-treatment and
today. Time between diagnoses was calculated as time
from CD diagnosis to other disease diagnosis. When both
diagnoses occurred during the same year, time was defined

Table 1 Characteristics of celiac disease subjects

n
Participants
Males/Females
Age when responding (years)

Mean

Median

Quartile
1st

3rd

53

36

67

1,031
495/536

48/52

1,031

52

Age at diagnosis (years)

945

39

41

27

53

Duration of celiac disease diagnosis (years)a

945

10

13

19

Compliance with a gluten-free diet

Strict/Non-strict
a

1,025
979/46
st

96/4

Members were invited based on entrance to society latest 1 of April 2009. Duration of celiac disease diagnosis was calculated as years ahead of 2009 that
respondent was diagnosed.

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Figure 1 Proportion of celiac disease patients reporting major (often or always) symptoms the year prior to celiac disease
diagnosis (pre-treatment) and after initiated gluten-free diet (today). Number of respondents for each symptom ranged between 879 and
949. Differences in symptoms pre-treatment and today were tested with the sign test.

as 0 years. Differences in symptoms between members

with a recent diagnosis (20052009) and members with
earlier diagnosis were performed using Students t-test.
Comparisons of health care visits, hospitalization days,
and missed working days between the groups were performed using Wilcoxon rank-sum test. To test if a glutenfree diet might decrease the risk for associated diseases,
the proportions of diagnoses of associated diseases before
or during the same year as the CD diagnosis were compared with the proportions after CD diagnosis using Students t-test. We excluded comparisons for vitiligo and
alopecia areata due to too few complete answers. Statistical significance was defined at the 5% level. Microsoft
Access was used for data handling, while Stata 11.2 (StataCorp LP, College Station, TX) was used for statistical analysis and figures.

Results
Symptoms

Pre-treatment, flatulence (64%) was the most commonly

reported symptom, followed by fatigue (62%), soft stool
(54%), and abdominal pain (53%). All investigated symptoms, except joint pain, improved after diagnosis and
initiated treatment with a gluten-free diet (Figure 1).
Today, flatulence and fatigue were also the most commonly reported symptoms for all participants, even
those who did not report the symptom pre-treatment
(Table 2). It was less common that participants without
a specific symptom reported pre-treatment reported the
symptom today than it was for participants who
reported the symptom pre-treatment. There were
improvements in all investigated symptoms in the
screening-detected cases except joint pain and body

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Table 2 Patients with symptoms today, also presenting

for patients asymptomatic pre-treatment
Symptom

Asymptomatica

All
b

na

nb

%b

81

8.8

432

14

3.2*

Flatulence (n = 897)

189

21

324

46

14*

Hard stool (n = 879)

95

11

708

43

6.1*

Abdominal pain (n = 918)

study population, improved after diagnosis. The only differences between recently diagnosed and those with an
earlier CD diagnosis was that weight loss and vomiting
were less common in the former pre-treatment, joint
pain was more common for recently diagnosed cases
pre-treatment, and nausea was less common for recently
diagnosed cases today.

Soft stool (n = 926)

130

14

423

24

5.7*

Health care consumption

Fatigue (n = 927)

202

22

349

42

12*

Weight loss (n = 903)

35

3.8

539

11

2.0*

Mood swings (n = 903)

56

6.2

689

13

1.9*

Depression (n = 913)

63

6.9

673

13

1.9*

Headache (n = 894)

77

8.6

742

21

2.8*

Participants reported more frequent health care visits

pre-treatment (5.4 visits during the year) than today (3.7
visits during the year) (p < 0.001), more hospitalization
days (2.3 days during the year) pre-treatment compared
to today (0.7 days during the year) (p < 0.001), and more
missed working days pre-treatment (7.2 days during the
year) than today (2.5 days during the year) (p < 0.001)
(Table 3). For screening-detected CD patients there were
also reductions in health care visits, hospitalization days
and missed working days between pre-treatment and
today. For recently diagnosed patients (20052009) there
were reductions in health care visits and missed working
days, but not in hospitalization days. We observed significantly fewer hospitalization days pre-treatment and
significantly fewer health care visits today for recently
diagnosed patients as compared to patients earlier diagnosed. Thirteen percent of participants (n = 136)
reported that they stopped taking at least one drug after
their CD diagnosis.

Joint pain (n = 897)

126

14

756

48

6.3*

Body pain (n = 897)

105

12

758

43

5.7*

Heartburn (n = 891)

51

5.7

691

16

2.3*

Nausea (n = 898)

26

2.9

762

12

1.6*

Vomiting (n = 910)

0.8

840

0.7

Skin rash (n = 898)

74

8.2

763

26

3.4*

Mouth ulcer (n = 904)

21

2.3

820

10

1.2*

Hair loss (n = 880)

20

2.3

843

1.1*

Not reporting specific symptom pre-treatment.

Reporting symptom today.
* Asymptomatic patients report fewer problems with symptom than
symptomatic patients today.

pain. Due to too few cases, comparison between pretreatment and today was not feasible for vomiting and
hair loss in the screening-detected group. For recently
diagnosed cases (20052009), all investigated symptoms
except vomiting and hair loss, which were rare in our

Self-reported immune-mediated diseases

At least one immune-mediated disease was reported by

256 (25%) of the study participants. Autoimmune thyroid disease, reported by 9.1%, was the most prevalent

Table 3 Health care consumption pre-treatment and today

Disease

Pre-treatment
n

pa

Today

Mean

Median

SD

Mean

Median

SD

All
Health care visits

814

5.4

7.8

3.7

8.0

<0.001

Hospitalization

836

2.3

8.5

0.7

4.0

<0.001

Missed working days

754

7.2

16

2.5

9.6

<0.001

Health care visits

144

4.8

9.0

4.1

9.9

0.001

Hospitalization

151

3.0

11

1.0

5.4

0.036

Missed working daysb

136

9.0

21

1.8

7.4

<0.001

Health care visits

202

5.0

7.1

4.3

8.8

<0.001

Hospitalization

200

0.62

2.7

0.36

1.8

0.860

188

7.5

17

3.4

13

<0.001

Screening-detected casesc

Recent diagnosisd

Missed working days

a

Using the sign test.

b
Also including missed school days and similar circumstances.
c
Primary investigation started based on a disease with known relation to CD or due to heredity for CD.
d
CD diagnosis between 2005 and 2009.

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immune-mediated disease (Table 4). There was a predominance of females for rheumatic disease and autoimmune thyroid disease but not for other self-reported
associated diseases. There was no difference in the frequency of being diagnosed prior to or after CD diagnosis
for any of the associated diseases (Figure 2).

Discussion
CD patients suffer from more symptoms and consume
more health care before diagnosis and initiated glutenfree diet than they do afterwards. However, we did not
observe a difference in the risk of developing other
immune-mediated diseases after initiated treatment with
a gluten-free diet.
This study is one of the largest of its kind and it has a
high response rate. Its unique contribution is that it
compares the situation before and after initiation of a
gluten-free diet, including symptoms and health care
consumption, which adds valuable information about individual and societal costs of untreated CD.
Our retrospective approach involves the risk of recall
bias. We observed a similar pattern for symptom relief,
health care visits, and missed working days when
restricting our analysis to screened and recently diagnosed (20052009) CD patients. There was not a significant reduction in hospitalization days for the

recently diagnosed (20052009) CD patients. This

could indicate an improved situation due to earlier
diagnosis, which we have reported earlier in the same
population [5], or it might be due to problems remembering hospitalization days if diagnosed earlier than
2005. In an attempt to assess if the risk of developing
associated immune-mediated diseases is affected by a
gluten-free diet, we assumed that if fewer were diagnosed with the related disease after the CD diagnosis
this would indicate a protective effect. The patient is
likely to remember which disease was diagnosed first,
but if there is a delay in diagnosis for one of the diseases the association could still be incorrect. A causal
relation cannot be determined with certainty by a
cross-sectional questionnaire study. An examination of
hospital files would have been a valuable addition in
this respect, but that was not within the scope of this
study.
Retrospectively reported symptoms prior to a CD
diagnosis have been studied previously [4], as have
symptoms at the time of CD diagnosis [22-25]. Most
studies have reported symptoms at the time of diagnosis that were obtained from medical records, making
comparisons with our results difficult. Our main interest was to detect experienced changes in symptoms
after initiated treatment with a gluten-free diet.

Table 4 Proportion of immune-mediated diseases and time development in relation to celiac disease (CD) diagnosis
All
Diabetes, insulin
Diabetes, non-insulin
Rheumatic disease
Thyroid disease
Vitiligo
Alopecia areata

Males

Females

pa

Before

Jointlyb

After

nc

pd

0.19

53%

6%

41%

32

0.29

0.04

20%

13%

67%

15

0.20

<0.01

42%

8%

50%

48

1.00

<0.01

47%

15%

38%

68

0.05e

0.24

72%

11%

17%

18

<0.01

0.52

62%

8%

31%

13

0.16

0.09

31%

27%

42%

26

0.43

<0.01

n/af

n/a

n/a

n/a

n/a

39

24

15

3.8

4.8

2.8

24

17

2.3

3.4

1.3

80

19

61

7.8

3.8

11

94

19

75

9.1

3.8

14

39

16

23

3.8

3.2

4.3

19

11

1.8

2.2

1.5

Inflammatory bowel disease

44

17

27

4.3

3.4

5.0

Any immune-mediated diseasee

256

170

86

25

32

17

Comparing males with females using Students t-test.

b
CD associated immune-mediated disease reported for same year as CD diagnosis.
c
Specified year for both CD and other diagnosis.
d
Comparing proportion with auto-immune disease diagnosed before or jointly with CD with proportion after CD diagnosis.
e
Non-significant.
f
Not including non-insulin dependent diabetes.
g
Comparisons not applicable for Any disease.

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Figure 2 Difference in years between the diagnosis of celiac disease and the diagnosis of associated immune-mediated disease.
Difference positive if celiac disease diagnosis first and 0 if both diagnoses during same year.

Previously, similar comparisons were done for a more

limited number of symptoms by Murray and colleagues in the United States, showing a similar positive
pattern for investigated symptoms after initiated treatment for CD [26]. Also Ukkola with colleagues showed
an improvement in symptoms after initiated treatment
with a gluten-free diet for Finnish CD patients [27].
Little is known about the added costs of CD for individuals and society. Although many participants had
their CD for a long time, and therefore were considerably older today, their health consumption was significantly lower today than prior to the CD diagnosis,
indicating a decreased need for health care after
initiated treatment with a gluten-free diet.
There is a well-known association between CD and
other immune-mediated diseases [1]. A protective effect
of a gluten-free diet was proposed more than a decade
ago [16,28], but later studies have shown conflicting
results [15,18]. In our study 25% of the individuals
reported associated immune-mediated diseases. The prevalences of autoimmune thyroid disease and diabetes
mellitus type 1 were similar to figures previously

reported in a Swedish CD population study based on patient chart reviews [25]. Our results could not verify or
reject a risk reduction effect of a gluten-free diet on the
development of any of the associated immune-mediated
diseases that were studied. Further studies are needed to
investigate this relationship.
In a previous publication based on the same study
population and questionnaire, we reported that there is
a long delay until CD diagnosis and that CD patients experience a poor health-related quality of life that is significantly improved after initiation of a gluten-free diet
[5]. Considering this and the results of the present study,
there is a strong implication that greater effort must be
made to diagnose CD earlier to decrease the burden of
both poorer health-related quality of life and CD-related
symptoms. This would also result in economic savings
for society in terms of a reduction in health care consumption and missed working days.
Recent studies have indicated that the extent of symptoms that patients detected through a population-based
CD screening might have may be similar to that of nonCD persons [29,30]. The screening-detected cases in our

Norstrm et al. BMC Gastroenterology 2012, 12:125

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study were mainly from risk groups. They reported the

same positive effect of symptom relief after diagnosis
and initiated treatment with a gluten-free diet as the CD
patients who had their primary investigation due to
symptoms.

Page 7 of 8

10.
11.

Conclusion
In conclusion, CD patients profit from being diagnosed
and treated with a gluten-free diet, since this reduces
both symptoms and health care consumption. An earlier
celiac disease diagnosis is therefore of great importance.
The possible protective role of a gluten-free diet regarding the development of other immune-mediated diseases
remains to be demonstrated.

12.

Competing interests
The authors declare that they have no competing interests.

15.

Authors contributions
Study design by FN, AI, and LL. FN coordinated data acquisition. FN
performed the analyses and the interpretation in collaboration with AI, LL,
and OS. FN drafted the paper and all co-authors contributed actively. All
authors read and approved the final manuscript.

16.

Acknowledgements
We thank all who responded to the questionnaire, as well as the Swedish
Society for Coeliacs for their assistance in improving the questionnaire and
their crucial administrative help. The study was funded by the Swedish
Research Council, the Swedish Research Council for Environment,
Agricultural Sciences and Spatial Planning, and the Swedish Council for
Working Life and Social Research. The study was undertaken at the Ume
Centre for Global Health Research at Ume University.

13.

14.

17.

18.

19.

20.
Author details
1
Department of Public Health and Clinical Medicine, Epidemiology and
Global Health, Ume University, Ume, Sweden. 2Department of Clinical
Sciences, Pediatrics, Ume University, Ume, Sweden.

21.

Received: 16 December 2011 Accepted: 30 August 2012

Published: 17 September 2012

22.

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Cite this article as: Norstrm et al.: A gluten-free diet effectively reduces
symptoms and health care consumption in a Swedish celiac disease
population. BMC Gastroenterology 2012 12:125.

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