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Original article 1187
Consumption of gluten-free products: should the threshold
value for trace amounts of gluten be at 20, 100 or 200 p.p.m.?
Anna Giberta, Montserrat Espadalera, Miguel Angel Canelab, Anna Sáncheza,
Cristina Vaquéa and Magda Rafecasc
Objective The threshold of gluten contamination in
gluten-free products of both dietary and normal
consumption is under debate. The objective of this study
was to gather information on consumption of gluten-free
products intended for dietary use of people under a
gluten-free diet. This information is essential to ascertain
the exposure of coeliac patients to gluten through their diet
and deduce the maximum gluten content that these
products should contain to guarantee a safe diet.
Methods A diet diary of consumption of gluten-free
products intended for dietary use was distributed to the
coeliac societies of two typical Mediterranean countries
(Italy and Spain) and two Northern countries (Norway and
Germany). The diet diary included a self-weigh table of the
selected food items and a 10-day consumption table.
Results were reported in percentiles as distributions were
clearly right skewed.
Results The respondents included in the study accounted
for 1359 in Italy, 273 in Spain, 226 in Norway and 56 in
Germany. Gluten-free products intended for dietary use
contributed significantly to the diet of coeliac patients in
Italy, Germany and Norway and to a lesser degree in Spain.
The most consumed gluten-free product in all countries
was bread, and it was double consumed in the Northern
countries (P < 0.001). Mediterranean countries showed
consumption of a wider variety of gluten-free foods and
pasta was eaten to a large degree in Italy.
gluten-free products but in the type of products consumed.
The observed daily consumption of gluten-free products
results in the exposure to rather large amounts of gluten,
thus the limit of 200 p.p.m. should be revised. A limit of
20 p.p.m. for products naturally gluten-free and of
100 p.p.m. for products rendered gluten-free is proposed to
guarantee a safe diet and to enable coeliac patients to
make an informed choice. These limits should be revised
as new data become available. Eur J Gastroenterol Hepatol
c 2006 Lippincott Williams & Wilkins.
18:1187–1195 European Journal of Gastroenterology & Hepatology 2006, 18:1187–1195
Keywords: Codex Alimentarius, coeliac disease, consumption of
gluten-free products, gluten exposure, gluten threshold, gluten-free diet,
gluten-free labelling, gluten-free standard
a
SMAP Celı́acs de Catalunya, Coeliac Society, Departments of bApplied
Mathematics and Analysis and cNutrition and Food Science-CeRTA, University of
Barcelona, Barcelona, Spain
Correspondence and requests for reprints to Anna Gibert, C/Balmes 109,
Pral 2a 08008 Barcelona, Spain
Tel: + 34 93 412 17 89; e-mail: [email protected]
Sponsorship: This study was supported by SMAP Celı́acs de Catalunya, the
Coeliac Society of Catalonia and by Agència Catalana de Seguretat Alimentària,
the Food Safety Agency of Catalonia.
Note: Preliminary data corresponding to 500 coeliac patients from Italy were
presented at the Association of European Coeliac Societies meeting in
Edinburgh, September 2005 and at the meeting of the Working Group on
Prolamin Analysis and Toxicity in Maikammer, September 2005.
Received 27 March 2006 Accepted 19 July 2006
Conclusions The differences between Northern and
Mediterranean countries were not in the total amount of
Introduction
Coeliac disease is a chronic food hypersensitivity caused
by ingestion of gluten in genetically predisposed individuals. It is a complex multifactorial disorder developed as
a result of both genetic and environmental factors. The
description and characterization of the pathogenesis of
the disease has recently made significant progress [1–3].
T-cell response is triggered by gluten peptides with the
action of tissue transglutaminase [4]. Those peptides can
bind to human leukocyte antigen (HLA)-DQ2/DQ8 with
high affinity. The autoimmune response leads to villous
atrophy in the small bowel and subsequent nutrient
malabsorption. The consequences of untreated patients
are defined as very serious [5–7].
The classic clinical manifestations of the disease, that is,
vomiting, diarrhoea, abdominal distension and failure to
thrive, are no longer described as the only ones. Nowadays, coeliac disease has been related to extraintestinal
evidences such as dermatitis herpetiformis, osteoporosis,
anaemia, vitamin B12 deficiency, hepatitis, stomatitis and
dental defects, infertility, depression, neurological diseases and cerebellar ataxia [8–11]. The oligosymptomatic
and asymptomatic forms are being recognized as very
common presentations of the disease, although highly
under diagnosed [12].
The prevalence of the disease in the Western world is
very high, accounting to 1 : 100 [11,13]. It is reported as
c 2006 Lippincott Williams & Wilkins
0954-691X Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
1188 European Journal of Gastroenterology & Hepatology 2006, Vol 18 No 11
even higher in certain Western European countries [14]
and in at-risk group populations [13] such as those with
Down syndrome [15], diabetes [16] and relatives [13,16].
Coeliac disease is a common medical condition and as
such an effort is being made to identify the undiagnosed
population, defined as the iceberg theory [8,17–19], as at
present diagnosed people may be 10 times lower [9].
Although alternative therapies are being researched [20],
the only treatment available nowadays for those suffering
from coeliac disease is to adhere to a strict gluten-free
diet for life. This includes a combination of consumption
of naturally gluten-free foods, such as meat, fish, fruit,
vegetables, legumes, eggs and dairy products with glutenfree substitutes of bread, cookies, pasta and other cerealbased foods. Gluten-free products intended for dietary
use have two main roles. On the one hand, they are
essential for achieving a balanced diet and on the other,
they minimize the differences with the diet of noncoeliac
patients. These two roles should not be underestimated,
the former should provide the appropriate energy and
nutrients required for a healthy diet and the latter
improves socialization of coeliac patients, preventing
them from looking different, from feeling deprivation
and consequently from committing transgression. This is
particularly important for the newly diagnosed as they are
often undernourished, especially in cases in which a late
diagnosis has occurred. This is also crucial during
adolescence, widely documented as the most difficult
stage to manage a strict gluten-free diet. Considering the
important role of gluten-free products in the diet of
coeliac patients, the quality of these products should be
carefully assessed and reviewed.
Gluten-free products are industrially manufactured using
gluten-free cereals, mainly rice and corn. These cereals,
however, may be cross-contaminated by gluten cereals
during harvest, handling of grain cereals, transport and
milling practices. Current European legislation does not
specify the threshold for gluten contamination in glutenfree products and in addition starches that have been
rendered gluten-free by extraction may also be used to
produce gluten-free products. The inclusion of these
starches into the gluten-free diet is controversial [21–27]
as the residue of gluten may be higher than the
contamination that occurs in naturally gluten-free
products.
The current Codex Alimentarius standard for gluten-free
products [28] has been under revision since 1998. In the
draft revised standard [29], a limit of 20 p.p.m. is defined
for products consisting of or made only from naturally
gluten-free ingredients, while a limit of 200 p.p.m. is
proposed only for foodstuffs or ingredients that have been
rendered gluten-free and for foods containing a mixture
of the two ingredients. The European Food Safety
Authority (EFSA) [30], the Food and Drug Administration, Center for Food Safety and Applied Nutrition (FDA/
CFSAN) [31] and the Working Group on Prolamin
Analysis and Toxicity [32,33], however, have questioned
the scientific sound of these limits. A limit of 100 p.p.m.
has recently been proposed by Collin et al. [27] and this is
supported by the Association of European Coeliac
Societies.
The definition of the term gluten-free needs clarification
from the regulatory authorities in the very near future.
Three main issues are required to establish the safe
residue limit of gluten in gluten-free products: to have a
fully validated method of analysis to detect and quantify
low levels of gluten, to establish the threshold of
toxicological concern of gluten for coeliac patients, and
to find out the levels of exposure of coeliac patients to
gluten through the diet.
The development of a reliable and accurate method of
analysis of gluten has been one of the main objectives of
the Working Group on Prolamin Analysis and Toxicity.
One of its members, Dr Méndez from the National
Center of Biotechnology (Madrid, Spain), has developed
a sandwich enzyme-linked immunosorbent assay (ELISA)
method, based on the monoclonal antibody R5, able to
recognize the potential coeliac-toxic epitope QQPFP
[34,35]. The method has a detection limit of 3.2 p.p.m. of
gluten, thus allowing for the determination of low levels
of gluten content. The Working Group on Prolamin
Analysis and Toxicity presented the method to the Codex
Alimentarius, after performing a ring test and the
Committee decided to endorse the R5-ELISA sandwich
as the standard method for the analysis of gluten residues
in food [36].
As for the threshold of toxicological concern, the EFSA
[30] and the FDA/CFSAN [31] reviewed available
clinical data. Although more studies are needed, currently
published data can be used to draw a conclusion to
temporarily establish a threshold for gluten.
Nonetheless, reported data on the consumption of
gluten-free products are scarce [27,37,38]. It is not
scientifically established to what extent coeliac patients
substitute bread, pasta, cookies, and other cereal-based
foods with the corresponding gluten-free products and
consequently the exposure to gluten traces cannot be
deduced.
This study was designed to collect consumption data of
gluten-free products intended for dietary use on the basis
of the responses to a 10-day diet diary of such products, in
order to ascertain the potential gluten exposure of coeliac
patients through their diet. Foods for normal consumption were not included. This information is essential to
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Consumption of gluten-free products Gibert et al. 1189
define the threshold value for gluten contamination in
gluten-free products.
Another aim of the study was to gather consumption
patterns of coeliac patients and to compare the consumption patterns of gluten-free products between two
typical Mediterranean countries (Italy and Spain) and
two Northern countries (Norway and Germany). No
studies of this kind have been performed before in
Europe.
Methods
Diet diary
A diet diary of gluten-free products intended for dietary
use for people on a gluten-free diet was designed by
health professionals (three pharmacists and one dietician) of SMAP Celı́acs de Catalunya, one expert on
Nutrition and Food Science and one statistician from the
University of Barcelona.
Owing to the diversity of the food products depending on
the country and also because coeliac food is known to be
different in size and format to the corresponding glutencontaining product, it was considered very important to
include in the questionnaire the weight of the rations or
products consumed. According to this, the first part of the
questionnaire was to self-weigh the selected gluten-free
products and to record them in a table. This was
requested just once at the beginning.
In the second part of the questionnaire, consumption of
the selected gluten-free products day by day, over a
period of 10 days, was asked to be recorded in another
table. The days did not need to be consecutive.
Very detailed instructions and examples on how to record
the weight of the rations and how to fill the daily
consumption table were given to the respondents. The
questionnaires were tested with a group of 10 study
participants from SMAP Celı́acs de Catalunya, in the
presence of the health professionals, to check that
instructions were clearly understood.
Before proceeding with the mailing, the questionnaires
were distributed to the coeliac associations of four
countries: Italy (AIC Associazione Italiana Celiachia),
Spain (SMAP Celı́acs de Catalunya, ASOCEPA Canary
Islands), Norway (NCF Norsk Cøliakiforenings) and
Germany (DZG Deutsche Zöliakie Gesellschaft e.V.).
Each country participating in the study had the
questionnaire translated to its own language and the
selected food items revised to adapt them to the food
habits of each country. The Spanish questionnaire
contained 23 items, the Italian 22, the Norwegian 18
and the German 23. Room to add other items not detailed
in the list was also included as ‘others’.
Questionnaires were mailed to 36 000 members in Italy,
5000 to two regions of Spain (Canary Islands and
Catalonia) and to 7500 in Norway. A self-addressed
stamped envelope was included so that all answers were
to be returned to SMAP Celı́acs de Catalunya. In
Germany, the questionnaire was announced on the
Society web site and returned by e-mail to SMAP Celı́acs
de Catalunya.
The questionnaire included a sentence to protect
respondents’ privacy: ‘I hereby give my consent that my
personal data are used for activities related to scientific
research or similar activities that would improve the
quality of life of coeliacs’, or similar statements.
Questionnaires were sent between May and June 2005
and received between June and October 2005.
Data collection and calculations
Each questionnaire was carefully reviewed for its validity
before being included in the study. Respondents filling
the consumption table but not recording the weight of
some rations were excluded from the sample, probably
producing a downward bias, as this typically occurred with
individuals with a wide range of consumption. Respondents with great deviations that could be attributed to
misprints or confusing the weight of the ration by the
total weight ingest for any of the items, were also
excluded.
For lasagne, only the contribution of the sheets and the
flour of the béchamel sauce was considered. For each
100 g of lasagne, 16 g of contribution of gluten-free
product was included. For each piece of crumbed meat
or fish, the weight of one heaped tablespoon of bread
crumbs (20 g) was considered. These figures were
determined experimentally, as for the rest of the food
items.
Data were processed by means of a self-designed
database. To simplify the presentation of the results,
the food items listed in the questionnaire were grouped
into the following food groups: bread, pasta, pastry,
biscuits, pizza, breakfast cereals and bread-crumb-coated
foods.
Statistics
As the distribution of intake for the various food groups
considered in this study was positively skewed, the
results reported in this study are percentiles, in order to
avoid the strong influence of the right tail of the
distribution on means and standard deviations [39]. Five
percentiles (10, 30, 50, 70 and 90th) are reported for each
of the seven food groups and for the total daily intake.
The 50th percentile (the median) is reported as the
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1190 European Journal of Gastroenterology & Hepatology 2006, Vol 18 No 11
Table 1
Summary of the population under study
Italy (n = 1359)
Men
Women
Age (years)
r2
3–10
11–30
31–50
> 50
Spain (n = 273)
Norway (n = 226)
Germany (n = 56)
n
Percentage
n
Percentage
n
Percentage
n
Percentage
328
970
29
71
102
171
37
63
64
156
29
71
13
23
36
64
12
259
439
477
173
9
19
32
35
13
11
96
58
74
34
4
35
21
27
12
0
13
26
60
125
0
6
12
27
55
2
10
14
21
7
4
18
25
37
12
Consumption data (in percentiles) of gluten-free products
of the countries studied
central measure and the extreme percentiles as a measure
of the spread.
Table 2
Differences between countries, sexes and age groups
have been tested using the nonparametric Kruskal–Wallis
test. All the calculations have been performed with R,
the public domain implementation of the S statistical
language.
Daily intake (g)
Percentile
Results
Population under study
The respondents included in the study accounted for
1359 in Italy, 273 in Spain, 226 in Norway and 56 in
Germany. These data represent 3.8% of the members of
the coeliac society in Italy, 5.0% in the two regions of
Spain (Catalonia and Canary Islands), 3.0% in Norway
and 0.3% in Germany. In all the countries studied, the
respondents were mainly female. According to age, in
Italy and Germany very similar populations entered the
study with the majority of the respondents between 11
and 50 years old. In contrast, in Spain the major group of
respondents was that aged 3–10 years and in Norway
more than half of the respondents were over 50 years. See
Table 1 for a summary of the population studied.
Consumption of gluten-free products by food groups
In Italy, Germany and Norway, gluten-free products
intended for dietary use contributed significantly to the
diet of coeliac patients. A lower consumption was
detected in Spain as compared with the other countries.
In percentages, half of the population in Italy and
Germany ate at least 16% more than in Norway and
35% more than in Spain. Table 2 is a summary, based on
percentiles, of the daily intake (grams per day). The
differences between the extreme percentiles and the
median (P90th – P50th and P50th – P10th) clearly show
that all distributions were right skewed, thus providing an
argument against the use of means and standard
deviations [39]. The differences P90th – P10th indicate
that daily consumption of gluten-free products in Italy
was more spread around the median than in the other
countries. See Fig. 1 for a graphical representation of the
distribution as adapted from Costanza et al. [39].
Italy (n = 1359)
Bread
Pasta
Pastry
Biscuits
Pizza
Breakfast cereals
Bread-crumb-coated
foods
Total daily intake
Spain (n = 273)
Bread
Pasta
Pastry
Biscuits
Pizza
Breakfast cereals
Bread-crumb-coated
foods
Total daily intake
Norway (n = 226)
Bread
Pasta
Pastry
Biscuits
Pizza
Breakfast cereals
Bread-crumb-coated
foods
Total daily intake
Germany (n = 56)
Bread
Pasta
Pastry
Biscuits
Pizza
Breakfast cereals
Bread-crumb-coated
foods
Total daily intake
10th
30th
50th
70th
90th
18.0
24.0
0.0
0.0
0.0
0.0
0.0
43.8
48.0
15.0
11.1
10.0
0.0
0.0
68.5
64.7
30.0
23.6
18.0
0.0
0.0
101.3
89.0
49.6
40.0
30.0
6.0
3.6
200.0
138.4
84.0
85.6
56.0
30.0
8.0
151.5
209.8
265.1
343.0
531.2
16.0
0.0
0.0
0.0
0.0
0.0
0.0
37.8
10.0
6.0
6.7
0.0
0.0
2.4
54.3
20.0
18.0
14.7
0.0
0.0
7.2
90.6
30.0
36.0
28.6
10.0
13.1
14.3
167.3
58.0
71.8
61.5
25.0
40.0
31.8
91.0
131.3
173.1
226.5
404.0
48.0
0.0
0.0
0.0
0.0
0.0
0.0
90.0
0.0
3.2
0.0
0.0
0.0
0.0
126.8
0.0
15.0
3.0
0.0
0.0
0.0
173.4
10.5
34.0
8.0
15.0
9.0
0.0
263.9
30.0
73.5
21.0
40.4
30.0
8.0
108.1
179.9
225.7
281.0
411.6
48.0
8.0
0.0
0.0
0.0
0.0
0.0
99.5
15.0
6.0
5.6
0.0
7.0
0.0
128.7
22.4
17.5
11.0
10.0
16.0
0.0
171.3
39.2
44.5
17.6
20.0
36.0
0.2
232.0
52.5
66.7
38.4
30.0
69.5
0.7
129.3
213.4
268.1
326.5
400.1
By food groups and based on the medians, the most
consumed gluten-free product in all countries was bread.
In all countries studied bread was chosen every day. In
Italy there was also a daily choice of pasta, and in Spain of
biscuits. In Spain and Germany, pasta was consumed
between two and three times every 10 days.
The median daily contribution in percentages of the
different groups of gluten-free products was as follows: in
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Consumption of gluten-free products Gibert et al. 1191
Owing to the size of the Italian sample, all comparisons
across countries were highly significant (P < 0.001). Even
excluding Italy, all comparisons were highly significant
(P < 0.058), except for pizza.
Fig. 1
10th percentile
50th percentile
90th percentile
600
Total intake (g/day)
500
531
404
400
300
200
265
226
152
100
0
412
173
91
Italy
Spain
108
Norway
400
268
129
Germany
Total gluten-free products consumption in percentiles by country
(grams per day).
Italy, 27% of the daily intake of gluten-free products was
bread, closely followed by pasta (24%), then pastry (11%),
biscuits (9%) and pizza (7%). In Spain, 35% of the daily
intake of gluten-free products was bread, followed by
pasta (11%), then pastry (10%), biscuits (9%) and
bread-crumb-coated foods (4%). In Norway, bread
was 61% of the daily intake of gluten-free products,
followed by a low contribution of pastry (7%) and
biscuits (1%). In Germany, 49% of the daily intake of
gluten-free products was bread, followed by pastry (10%),
pasta (9%), breakfast cereals (6%), biscuits (5%) and
pizza (3%). The contribution of the group ‘others’ was
not significant.
The Northern countries (Germany and Norway) showed
the highest intake of bread, with medians of 128.7 and
126.8 g/day, respectively. As for the Mediterranean countries, in Italy the median consumed was nearly half of this
(68.5 g/day) and in Spain slightly lower (54.3 g/day).
Italy was the country with the highest pasta intake,
followed by Germany and Spain with similar figures. In
Norway, pasta was scarcely consumed. The medians of
pizza consumption accounted for 18.0 g/day in Italy and
10.0 g/day in Germany, while in Spain and Norway this
product was barely consumed.
Pastry and biscuits contributed substantially to the
Mediterranean countries’ daily intake, particularly in
Italy, but also in Spain. These products were also
consumed in Germany, but were of less importance in
Norway. Breakfast cereals only contributed to some
extent to the diet of coeliac patients in Germany. For
the other countries, consumption of breakfast cereals was
not significant. Similarly, bread-crumb-coated foods only
contributed to the diet of coeliac patients in Spain.
Consumption of gluten-free products by age
The highest intake of gluten-free products occurred in
the age group between 11 and 30 years and the lowest in
the group aged below 2 years. This responds to the
difference in energy requirements and dietary habits
existing between these age groups. In percentages of the
medians, in Italy, Spain and Norway, the group aged
11–30 years consumed 17–22% more than the group aged
2–10 years. As compared with the group aged r 2 years,
this figure was variable depending on the country. In Italy,
the group aged 11–30 years consumed 23% more than the
group r 2 years, but in Spain this group ate 62% more
than the group r 2 years. This shows that a very
low consumption of gluten-free products in children
below 2 years occurred in Spain.
In Italy and Spain, consumption of bread increased with
age (P < 0.001). In Norway no difference of bread
consumption occurred with age and in Germany consumption of bread was also quite homogeneous across the
different age groups, except for children r 2 years. On
the contrary, biscuits were mainly eaten by children in all
countries studied.
Consumption of gluten-free products by sex
In all countries, males ate more than females (13–28%).
The sex effect was significant in Italy for biscuits
(P < 0.001), pastry (P < 0.001), pasta (P < 0.001) and
pizza (P = 0.014). In Spain it was significant for biscuits
(P = 0.043) and pasta (P = 0.003), and in Norway it was
only significant for bread (P < 0.001).
As for their consumption patterns, however, males and
females of the same country tended to consume the same
types of foods, except that in Norway the median of pasta
consumption was null for males and in Germany pizza was
exclusively eaten by males.
Discussion
Studies on the diet followed by coeliac patients have
been focused on topics such as the inclusion of wheat
starch [27,40] or oats [40–42] in the gluten-free diet, in
the adequacy of nutrients intake [43–45], in the level of
dietary compliance [46–51] or in the impact on the
quality of life [52]. Only three studies containing data on
the quantity and/or type of gluten-free products eaten by
coeliac patients have been identified in the literature
[27,37,38]. One study [53] contained data on the amount
of gluten consumed by first-degree relatives of coeliac
patients in the Netherlands.
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1192 European Journal of Gastroenterology & Hepatology 2006, Vol 18 No 11
In the framework of such studies, the 10-day recording
period of this survey, chosen to minimize day-to-day
variations, and the complete list of gluten-free products
intended for dietary use to facilitate the record of each
food item, provided an adequate tool to assess consumption patterns of such products. The number of respondents made this survey representative of the coeliac
population of Italy, Norway and the two regions of Spain,
although it may be only informative for Germany owing to
the smaller size of the population studied. The survey
was only limited by a slight downward bias caused by the
incomplete questionnaires that could not be included.
follow-up to achieve a nutritionally adequate diet, as has
been strongly recommended [45,58,59].
The age of the respondents was indicative of the
situation of the water line of the coeliac iceberg in each
of the countries studied. In Italy, Norway and Germany,
the diagnosis and awareness of the disease has made
significant progress in the recent decades [54]. The high
participation of adults in those countries reflects on the
one hand the paediatric population diagnosed some years
ago and on the other, the progress of adult detection of
the disease. On the contrary, in Spain, the disease has
recently shown a high incidence owing to awareness of
paediatricians [55,56], but diagnosis in adults is only
incipient. This may explain the high number of
respondents below 10 years of age and the low number
of adults. It is also worth mentioning that the higher
number of female respondents in all countries reflects
the higher incidence of coeliac disease in the female sex.
Greco et al. [37] studied the consumption of Italian
adolescents in a gluten-free diet and found an average of
about 11.32 kg/month (377.3 g/day) of gluten-free products. This figure was similar to the mean found in our
study for the group aged between 11 and 30 years in Italy
(345.0 g/day).
Contribution of gluten-free products in coeliac patients’
diet
Despite the different kind of recommended daily intakes,
cereals provide the greatest amount of calories per person
in all European countries [57] and are described as the
main source of carbohydrates and also provide protein and
vitamins. According to FAO food balance sheets of 2002,
per capita supply of cereals in Europe (15 countries) was
mainly due to gluten cereals (wheat, barley, rye, oats),
accounting for 90% of the total. Only 10% of the per
capita supply was due to rice, maize, millet or sorghum.
To follow such consumption pattern, coeliac patients
must substitute their gluten cereals intake with the
corresponding amount of gluten-free cereals.
The coeliac population included in this study showed an
important contribution to the diet of gluten-free
products, thus implying that coeliac patients base their
diet not only on naturally gluten-free products but also on
important amounts of gluten-free bread, pasta, pastry,
biscuits or pizza. As it has been reported that coeliac
patients’ diets are often unbalanced [38,43,45] and have
higher percentage of calories from fat and proteins and
less from carbohydrates [43,45], however, the reported
intake of these products could even be higher in the
following years if coeliac patients get dietary advice and
Thompson et al. [38], in a study of gluten-free diets of
American coeliac patients, found a mean daily intake of
grain food servings of 4.6 for women and 6.6 for men,
which is lower than the recommended [60]. The
authors also reported that coeliac patients’ diets have so
far been focused on the allowed/not allowed food rather
than on ensuring a nutritionally adequate diet, and
recommended a daily intake of 6–11 servings of glutenfree products.
Collin et al. [27] reported that the median daily use
of flours by coeliac patients in Finland was 80 g (range
10–300 g) for adults and 60 g (range 20–140 g) for
children. In this study, results of daily intake were
calculated on the finished product and not on the amount
of flour consumed.
Differences between Northern and Mediterranean
consumption patterns
This survey showed that the difference between Northern (Germany and Norway) and Mediterranean (Italy and
Spain) countries’ coeliac patients’ diet was not in the
total amount of gluten-free products consumed. Italy,
Germany and Norway showed similar medians,
although in Italy some individuals ate very high amounts
as shown by the high value of the 90th percentile. On
the contrary, in Spain a lower consumption of gluten-free
products as compared with the other countries was
detected. This may be related to the fact that gluten-free
products are not funded in Spain. It is reasonable that
coeliac patients may deliberately divert their diet to
consumption of nondietary naturally gluten-free
products that are less expensive and more accessible,
although this would most likely lead to nutritional
deficiencies.
The differences between Northern and Mediterranean
countries were in the contribution of the different types
of gluten-free products in the diet. The most significant
difference was the consumption of bread (P < 0.001).
The Northern countries consume double the amount of
bread than the Mediterranean. Consumption of bread
(in grams per person per day) by the general population
has been reported [61] to be 158 in Italy, 141 in Spain and
197 in Norway, thus confirming the tendency of Northern
countries to a higher consumption.
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Consumption of gluten-free products Gibert et al. 1193
reported that maximum gluten intake should lie between
10 and 100 mg/day.
The other main difference between Northern and
Mediterranean countries was in pasta consumption,
traditionally part of the Mediterranean diet. The survey
showed that this product was highly consumed in Italy,
and was also greatly consumed by coeliac patients of
Spain and Germany. In contrast, in Norway consumption
of pasta was nearly null.
Clinical data are nonconclusive, but meanwhile the FDA/
CFSAN [31] has stated that the safety assessment-based
approach is a viable approach to establish a threshold for
gluten using currently available ‘no observed adverse
effect level’ (NOAEL) or ‘lowest observed adverse effect
level’ (LOAEL) data for coeliac disease. The threshold
for gluten contamination in gluten-free products following the safety assessment-based approach can be deduced
from the tolerable daily intake (TDI = NOAEL/uncertainty factor), which must then be compared with the
level of intake in the upper part of the distribution [65].
In conclusion, coeliac patients of the Mediterranean
countries but also of Germany ate the same types of food:
bread, pasta, biscuits, pastries and pizza to some extent,
so that a wide variety of products contribute to their diet.
On the contrary, in Norway, the intake of cereals by the
coeliac population was made almost exclusively by means
of high amounts of bread.
In this study, the level of intake of gluten-free products
intended for dietary use has been assessed. Table 3 shows
a summary of the exposure to gluten calculated from the
different percentiles used by regulatory agencies [65]
(90th percentile in United States, 95th percentile in the
European Union, 97.5th in the United Kingdom) and the
different thresholds of gluten contamination under
debate (20, 100 and 200 p.p.m.). It can be observed that
with the limit of 20 p.p.m. and in the different
percentiles, values of gluten daily exposure due to
consumption of gluten-free products range from 8.0 to
20.1 mg. For the limit of 200 p.p.m., the values range from
80.0 to 201.0 mg/day. At midway, with the limit of
100 p.p.m., the values range from 40.0 to 100.4 mg/day.
One should bear in mind that these levels of gluten
exposure do not take into account other sources of gluten
in the diet of coeliac patients such as those carried by
consumption of normal processed food, for which
manufacturers often use the 200 p.p.m. limit as the
reference for labelling it as gluten-free, regardless of the
vegetal (wheat/nonwheat) origin of their ingredients.
Gluten exposure assessment
The threshold for gluten that triggers an adverse reaction
has not yet been ascertained. The studies to establish
this threshold are difficult and expensive, because in the
absence of animal models, the studies need to be
performed in humans and assessed by means of biopsy.
Available clinical data have been reviewed by Collin et al.
[27], by the EFSA [30] and also by FDA/CFSAN [31]. Invivo challenge studies have covered different exposures
to gliadin (from 1.2 mg to 1 g/day) or gluten (from 100 to
500 mg/kg/day), for different lengths of time (from hours,
days, months or years) and by means of different
methodologies.
A recent case study has shown that the ingestion of 1 mg
of gluten per day over a period of 2 years prevented
histological recovery [62]. Collin et al. [27] reported that
according to histology changes, a daily intake of 30 mg of
gluten was safe. The most recent challenge study has
been performed by Catassi et al. [63]. The study has
promising and reliable results as it is a prospective,
multicentre, placebo-controlled, double-blind, randomized gluten challenge trial performed on 36 coeliac
patients exposed to gluten for 3 months. Preliminary
results of this study showed that 10 mg/day were
well tolerated but there was a trend to histological
changes when patients were challenged with 50 mg.
Hischenhuber et al. [64], in a review article, have recently
Gluten-free standard
As mentioned before, the draft revised standard for
gluten-free products is under discussion. It seems that
there is a general agreement on the fact that the limit of
20 p.p.m. is protective enough for coeliac patients. The
limit of 200 p.p.m. for products rendered gluten-free,
however, is not accepted in the same way.
Table 3 Daily gluten exposure deduced from the different percentiles of consumption of gluten-free products and the different thresholds
of gluten contamination
Italy (n = 1359)
Spain (n = 273)
Norway (n = 226)
Germany (n = 56)
Percentiles of daily intake (g)
90th
531.2
95th
639.4
97.5th
1003.7
90th
404.0
10.6
53.1
106.2
13.9
69.6
139.3
20.1
100.4
201.0
8.1
40.4
80.8
Gluten
threshold
(p.p.m.)
20
100
200
95th
97.5th
90th
95th
512.2
717.2
411.6
512.1
Daily amount of gluten exposure (mg)
97.5th
638.3
90th
400.1
95th
467.3
97.5th
505.7
10.2
51.2
102.4
12.8
63.8
127.7
8.0
40.0
80.0
9.3
46.7
93.5
10.1
50.6
101.1
14.3
71.7
143.4
8.2
41.2
82.3
10.0
50.2
100.4
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
1194 European Journal of Gastroenterology & Hepatology 2006, Vol 18 No 11
It is well known that Northern countries are less
concerned about the 200 p.p.m. limit, while the Mediterranean countries prefer the 20 p.p.m. limit. In Italy,
there is a National Regulation [66] that does not allow
the use of wheat starch in the manufacture of gluten-free
products and consequently establishes a unique limit of
20 p.p.m. These differences might be related to consumption patterns, as on the one hand, cereals highly
contribute to the Mediterranean diet and consequently
the exposure to gluten traces may be higher. On the
other, the existence of a 200 p.p.m. limit allows using
wheat starch to produce bread of good quality and texture
and makes it highly appreciated in the Northern
countries in which bread seems to be the main glutenfree product of the coeliac diet. It should be mentioned
that because of the evolving food technology of recent
years, bread of great characteristics can also be produced
using no wheat-based ingredients.
With the data collected in this study, consumption of
gluten-free products in both Northern and Mediterranean countries results in the exposure to rather large
amounts of gluten. Until the tolerable daily intake for
gluten and subsequent risk assessment to establish the
safe threshold of gluten for coeliac patients are completed and following the precautionary principle of
European food law, it is suggested to define as glutenfree any product with a content of less than 20 p.p.m.
This standard is achievable for naturally gluten-free
products and gluten can be detected and quantified with
available analytical methods. This limit of 20 p.p.m.
should also be the upper limit for labelling foods
for normal consumption according to the recent
European Union Directive on Allergen Declaration [67].
This would allow coeliac patients to follow a strict glutenfree diet exclusively based on naturally gluten-free
products coming from both gluten-free products intended for dietary use and processed foods for normal
consumption.
teeing a safe diet for coeliac patients. These limits,
however, should be revised as new data become available.
Acknowledgements
Coeliac societies from Italy, Norway, Canary Islands and
Germany have been of great help with translations and
promoting participation. Special mention should be given
to the Italian Society for its high contribution to the
study. We also thank the Youth and volunteers of SMAP
Celı́acs de Catalunya for their contribution to data
collection.
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