OBJECTIVE—This study was performed to 1) determine the prevalence of celiac disease in Danish children with type 1 diabetes and 2) estimate the clinical effects of a gluten-free diet (GFD) in patients with diabetes and celiac disease.

RESEARCH DESIGN AND METHODS—In a region comprising 24% of the Danish population, all patients <16 years old with type 1 diabetes were identified and 269 (89%) were included in the study. The diagnosis of celiac disease was suspected in patients with endomysium and tissue transglutaminase antibodies in serum and confirmed by intestinal biopsy. Patients with celiac disease were followed for 2 years while consuming a GFD.

RESULTS—In 28 of 33 patients with celiac antibodies, an intestinal biopsy showed villous atrophy. In 5 patients, celiac disease had been diagnosed previously, giving an overall prevalence of 12.3% (95% CI 8.6–16.9). Patients with celiac disease had a lower SD score (SDS) for height (P < 0.001) and weight (P = 0.002) than patients without celiac disease and were significantly younger at diabetes onset (P = 0.041). A GFD was obtained in 31 of 33 patients. After 2 years of follow-up, there was an increase in weight SDS (P = 0.006) and in children <14 years old an increase in height SDS (P = 0.036). An increase in hemoglobin (P = 0.002) and serum ferritin (P = 0.020) was found, whereas HbA1c remained unchanged (P = 0.311) during follow-up.

CONCLUSIONS—This population-based study showed the highest reported prevalence of celiac disease in type 1 diabetes in Europe. Patients with celiac disease showed clinical improvements with a GFD. We recommend screening for celiac disease in all children with type 1 diabetes.

It is well established that celiac disease is overrepresented in different autoimmune diseases, notably type 1 diabetes. Also celiac disease itself has features characteristic of an autoimmune disease. In numerous studies from European countries over the last 30 years, the prevalence of celiac disease in children with type 1 diabetes has been reported to be 2–8% (1). Surprisingly, no strictly population-based studies have been published, as judged from the presented material, even though two large studies from Italy (2) and Germany (3) comprise a considerable percentage of the national diabetic population.

In Denmark, the prevalence of recognized cases of celiac disease in the general population is very low compared with the prevalence in other neighboring countries (4,5). On the other hand, a high incidence of childhood type 1 diabetes has been documented (6). Therefore, it appeared to be particularly interesting to determine the prevalence of celiac disease in Danish type 1 diabetic children. In a preliminary study, we found a prevalence of celiac disease of 10% in Danish type 1 diabetic children (7). In the present study, we extended this investigation to a larger population. The study was performed in a strictly population-based design, including all type 1 diabetic children from a region representing one-fourth of the Danish population.

Despite the high prevalence of celiac disease in type 1 diabetes, the issue of routine screening of all type 1 diabetic children has been much debated (8). Many diabetic patients in whom celiac disease has been diagnosed through screening are asymptomatic or have nonspecific symptoms of celiac disease (1). The benefits of a gluten-free diet (GFD) in those patients, both in the short- and long-term, are not well established. In a few previous studies of patients with both type 1 diabetes and celiac disease, the effect of a GFD on symptoms, growth, and metabolic control has been investigated, but with inconsistent results (912). In the present study, the clinical course in diabetic children with celiac disease was evaluated during a 2-year follow-up period when they consumed a GFD.

In Denmark, the treatment of all children with type 1 diabetes is restricted to the pediatric departments within the hospital-based health system. The present study was performed in the region of southern Denmark consisting of four counties, each with one pediatric department. All children <16 years old from the pediatric departments in the four counties were included. In the county of Funen, patient identification was performed in 1997 as previously reported (7). In the remaining three counties, the children were investigated through 2002–2003.

At study entry, all patients were interviewed by the doctor about symptoms compatible with celiac disease, and a symptom questionnaire was filled out. Height and weight were registered. Blood samples were obtained and analyzed for specific antibodies. Serum anti-gliadin antibodies (IgG and IgA AGAs) were measured by enzyme-linked immunosorbent assay (13); cutoff value was 15 arbitrary units (AU). Serum anti-tissue transglutaminase antibodies (IgA tTGAs) were measured by enzyme-linked immunosorbent assay (INOVA Diagnostics); cutoff value was 20 AU. Antibodies against endomysium (IgA EMA) in serum were measured by indirect immunofluorescence using monkey esophagus tissue (INOVA Diagnostics) as substrate. The fluorescence intensity was reported semiquantitatively (0, 1+, 2+, and 3+). In patients from the county of Funen, antibody analyses were initially performed at another laboratory (7). Frozen sera from those patients were reanalyzed by the above mentioned methods, and identical results were obtained.

In patients only positive for IgG AGA, total serum IgA was determined to exclude IgA deficiency. In patients with positive IgA AGA, EMA, and/or tTGA antibodies, an intestinal biopsy was performed. Endoscopic duodenal biopsy samples were taken and examined histologically by a gastroenterological pathologist. In patients with partial or total villous atrophy, a GFD was instituted after careful instructions by a dietitian. Subsequently, patients were seen by the doctor in the outpatient clinic every 3rd month for a minimum period of 2 years. At each visit, celiac disease–related symptoms and growth parameters were schematically registered. Blood samples were taken, and measurements of celiac antibodies and other hematological parameters (hemoglobin, mean corpuscular volume, serum ferritin, folate, cobalamin, glycosylated hemoglobin, ionized calcium, and alanine aminotransferase) were performed using routine analytical methods. After 2 years follow-up with the patient consuming a GFD, another intestinal biopsy was offered to all patients with celiac disease.

In patients with positive celiac antibodies, HLA typing was performed. HLA-DQB1* and -DQA1* typing was done by PCR amplification with sequence-specific primers. DRB1* alleles were detected by PCR amplification with sequence-specific oligonucleotides using the One Lambda Lab Type rSSO typing system for HLA typing.

All patients and their parents gave informed written consent, and the study was approved by the regional ethical committees. The study was performed in accordance with Helsinki Declaration II.

Statistics

The statistical package Intercooled STATA 7 was used for the statistical analyses. For comparisons between groups, the Mann-Whitney rank-sum test and Fisher′s exact test were used; 95% CIs for proportions were calculated by use of the binomial distribution. The follow-up data were analyzed using the Wilcoxon signed-rank test for paired observations. P values <0.05 were considered statistically significant.

A total of 303 patients with type 1 diabetes were identified in the four counties, and 269 (89%) accepted to participate. The included patients had a median age of 10.9 years (range 1.5–16.0) and a median duration of diabetes of 3.1 years (range 0.1–14.5). Five of them had a previous diagnosis of celiac disease and were consuming a GFD.

IgA AGAs were found in 11 and IgG AGAs in 28 of the patients investigated. All patients with IgA AGAs also had EMAs and tTGAs. Sixteen patients with low titers (<30 AU) of IgG AGA had neither EMA nor tTGA. In those patients IgA deficiency was excluded, and they were not further investigated. EMAs and tTGAs were found in 33 of 269 patients, and there was an absolute correlation between the presence of these antibodies. In all but one patient, an intestinal biopsy was obtained. In 28 of 32 patients, the biopsy showed partial or total crypthyperplastic villous atrophy. In four patients, the biopsy showed normal intestinal mucosa; although in one of them, increased lymphocyte infiltration in lamina propria was noted. Thus, including the 5 patients previously diagnosed with celiac disease, a total of 33 of 269 patients (17 female and 16 male) had celiac disease, corresponding to a prevalence of 12.3% (95% CI 8.6–16.9).

Table 1 presents clinical characteristics of diabetic subjects with celiac disease compared with diabetic subjects without celiac disease. Patients with celiac disease had a significantly lower age at diabetes onset (P = 0.042), whereas there was no difference comparing age and sex in the two groups. The patients with celiac disease had a significantly lower height SD score (SDS) (P < 0.001) and weight SDS (P = 0.002). In the interview, they reported symptoms of celiac disease significantly more often (P < 0.001) than patients without celiac disease. Table 2 presents the prevalence of celiac disease–related symptoms in both groups. In four patients with celiac disease, the symptoms were first recognized in retrospect after a GFD was instituted. Only 5 of 33 (15%) patients with celiac disease had no clinical signs of the disease.

HLA genotyping, performed only in the patients with celiac disease, showed the HLA DQ2 genotype in 28 of 33 (85%) of the patients, HLA DQ8 in 12 of 33 (36%), and both DQ2 and DQ8 in 8 of 33 (24%). A single patient had neither the HLA DQ2 nor the DQ8 genotype. The four patients with celiac antibodies but normal biopsy findings all had the HLA DQ2 and/or DQ8 genotype.

A GFD was initiated in 31 of 33 patients with celiac disease, whereas 2 asymptomatic patients refused to start the diet. In 24 of 31 patients, the celiac antibodies disappeared, confirming the diagnosis of celiac disease according to the revised European Society for Paediatric Gastroenterology Hepatology and Nutrition (ESPGHAN) criteria (14). In seven patients with variable compliance to the GFD, the celiac antibodies declined during follow-up but never became negative (Fig. 1). In many patients, the decrease in celiac antibody titers was slow, and the antibodies became negative after 1–2 years on a strict diet. Almost all of the symptomatic patients experienced relief of symptoms while consuming the GFD (Table 2), whereas three asymptomatic patients experienced no changes. Table 3 demonstrates the development of different clinical and biochemical parameters at 6, 12, 18, and 24 months of follow-up compared with baseline. After 2 years of follow-up, there was a significant increase in weight SDS (P = 0.002), whereas the increase in height SDS (P = 0.073) did not reach significance. However, when patients who were >14 years old at the onset of the study were excluded, there was also a significant increase in height SDS (P = 0.036). There was a significant increase in hemoglobin (P = 0.001), mean corpuscular volume (P = 0.020), and serum ferritin (P = 0.012). A significant increase in serum folate was found after 6, 12, and 18 months, but the increase did not reach statistical significance at 24 months (P = 0.076). No significant change in HbA1c (A1C) was seen during the 2 years of follow-up. In 18 of 33 patients, a second intestinal biopsy was performed after they consumed a GFD for 2 years. In 14 patients, the intestinal mucosa had normalized, whereas in 4 patients, who did not follow a strict diet, the mucosa had only partially recovered.

In the present study, we investigated a total of 269 children <16 years old, representing 89% of all children with type 1 diabetes in this age-group in an area representing ∼25% of the Danish population. In this population, we found a prevalence of celiac disease of 12.3% (95% CI 8.6–16.9). The prevalence of celiac disease might be even higher. A single patient who had no biopsy sample taken still has very high celiac antibody titers. Four patients with celiac antibodies, all HLA DQ2 and/or DQ8 positive, had normal biopsy findings but may have latent celiac disease. A single patient, who was antibody negative at the primary screening, later developed symptoms of celiac disease, and the diagnosis was confirmed by celiac antibodies and intestinal biopsy. Finally, patients with celiac disease might have been missed because of false-negative serology results (15). The high prevalence of celiac disease among Danish diabetic patients is surprising in view of the low prevalence of recognized celiac disease in the general population in Denmark (4). A similar screening study in the general population might possibly reveal a prevalence of celiac disease of ∼1% as found in many other European countries (16).

In previous studies, most of which are from other European countries, the prevalence of celiac disease in type 1 diabetic children has generally been lower than that in the present study (1). Genetic and environmental factors might account for some of the regional differences. However, the higher celiac disease prevalence in the present study might also be explained by differences in study conditions: 1) this study was population-based, whereas previous studies have been based on outpatient clinics with no detailed reports of demographic data; 2) we used sensitive and specific celiac antibody tests (IgA EMAs and tTGAs) (17); 3) in contrast with many other studies, all but one of the celiac antibody-positive patients in the present study did consent to intestinal biopsy; and 4) we also included patients with previously diagnosed celiac disease. Our conclusion is that the much lower prevalences of celiac disease in type 1 diabetes found in some European countries might be underestimates of the true prevalence in the population.

In the present study, patients with celiac disease had a significantly earlier onset of diabetes compared with diabetic subjects without celiac disease (Table 1). This observation is in agreement with some (3,18,19) but not all (2022) previous studies. In a recent Italian multicenter study in which 4,322 young patients with type 1 diabetes were investigated, a threefold higher risk for celiac disease was found in children <4 years old at the onset of diabetes than in those >9 years old (2). In Denmark, an increase in the incidence of type 1 diabetes in children <5 years old has been observed during recent years (6). If the association between young age at diabetes onset and the development of celiac disease is consistent, an increase in the number of patients with both diseases might be expected.

Most patients with celiac disease diagnosed through screening are described as having subclinical celiac disease (23). In the present study, only 5 of 33 (15%) of diabetic subjects with celiac disease had the diagnosis before our screening even though the majority of the patients with celiac disease reported symptoms of celiac disease in their interview. Only 5 patients with celiac disease presented with no symptoms or biochemical signs of celiac disease. This observation supports recommendations of screening for celiac disease in type 1 diabetic patients. Despite an increased clinical awareness from the physicians, celiac disease may remain undiagnosed in many patients with type 1 diabetes if regular screening is not performed.

Although a considerable number of screening studies have been performed, only a few studies described the effects of a subsequent GFD in patients with type 1 diabetes and celiac disease. In the present study 31 of 33 patients with both diseases were followed while they consumed a GFD for at least 2 years. During follow-up, the symptomatic patients experienced increased well-being. In a few patients with variable compliance to the diet, minor symptoms remained (Table 2). The majority of patients became celiac antibody negative after 3 to 24 months after starting the GFD. At diagnosis of celiac disease, we found that patients were stunted in their growth, with both height and weight SDSs being affected, compared with diabetic patients without celiac disease (Table 1). After 2 years of consuming a GFD, patients with celiac disease had a significant increase in weight SDS. In patients <14 years old, a significant increase in height SDS was also seen, reflecting the potential for growth in younger patients. In accordance with this finding, some previous researchers have reported an impairment of growth in patients with celiac disease and type 1 diabetes compared with diabetic control subjects (3,9). In longitudinal studies of diabetic patients consuming a GFD, Amin et al. (9) found an increase in BMI SDS, Saadah et al. (10) showed an increase in weight-for-age z scores, and Sanchez-Albisua et al. (12) found an increase in height SDS in patients with good dietary compliance. On the other hand, Rami et al. (11) and Westman et al. (24) found no improvement in neither BMI SDS or height SDS on a GFD. However, most follow-up studies have been small, and interpretation of the results is difficult because of variable dietary compliance in the patients investigated.

In the present study, we evaluated hematological markers, often affected in patients with celiac disease. Iron deficiency anemia is a frequent symptom in children with celiac disease (23). In our patients, we found a significant increase in hemoglobin, mean corpuscular volume, and serum ferritin after 2 years of consuming a GFD. Acerini et al. (25) measured the same parameters longitudinally in a small group of seven diabetic patients consuming a GFD but could not demonstrate any significant changes. An important aspect in patients with type 1 diabetes and celiac disease is the metabolic control with a GFD. In the present study, A1C was almost unchanged in patients consuming a GFD. In a few studies, a decrease in A1C was seen in diabetic subjects after a GFD (9,12), whereas others could not demonstrate any improvements (10,11,25,26). However, A1C may not by itself reflect the metabolic control in diabetic subjects consuming a GFD. In the present study, two patients experienced fewer episodes of hypoglycemia after the start of the GFD. Mohn et al. (27) also described frequent episodes of hypoglycemia in diabetic children with celiac disease with a reduction in the hypoglycemic risk with a GFD. Continuous blood glucose monitoring and careful registration of insulin requirements before and after the start of the GFD would give further valuable information about the metabolic control.

In summary, in a population-based study of Danish children with type 1 diabetes, we found a high prevalence of celiac disease. The occurrence of celiac disease was associated with young age at diabetes onset. Patients with celiac disease were stunted in their growth, and many had unrecognized symptoms of celiac disease. Longitudinal follow-up after consumption of a GFD in this cohort of patients demonstrated symptom relief and improvements in growth parameters, but no significant changes in metabolic control. The data lend support to recommendations of regular screening for celiac disease in all children with type 1 diabetes.

Figure 1—

The development of tissue transglutaminase antibodies in children with type 1 diabetes and celiac disease, measured 0, 6, 12, 18, and 24 months after starting a GFD. ♦, patients adherent to GFD; □, patients not strictly adherent to GFD.

Figure 1—

The development of tissue transglutaminase antibodies in children with type 1 diabetes and celiac disease, measured 0, 6, 12, 18, and 24 months after starting a GFD. ♦, patients adherent to GFD; □, patients not strictly adherent to GFD.

Close modal
Table 1—

Clinical characteristics of diabetic patients with celiac disease compared with diabetic patients without celiac disease

CharacteristicsDiabetic patients with celiac diseaseDiabetic patients without celiac diseaseP value
n 33 236  
Sex (female/male) 17/16 110/126 0.710 
Age (years) 9.4 (2.0–16.0) 11.1 (1.5–15.9) 0.096 
Age at diabetes onset (years) 5.8 (0.7–12.7) 6.6 (0.6–14.9) 0.042 
Height SDS −0.65 (−3.5 to 2.1) 0.4 (−3.2 to 2.8) <0.001 
Weight SDS 0.1 (−1.4 to 1.4) 0.5 (−1.9 to 5.0) 0.002 
Prevalence of symptoms (%) 84.8 25.4 <0.001 
CharacteristicsDiabetic patients with celiac diseaseDiabetic patients without celiac diseaseP value
n 33 236  
Sex (female/male) 17/16 110/126 0.710 
Age (years) 9.4 (2.0–16.0) 11.1 (1.5–15.9) 0.096 
Age at diabetes onset (years) 5.8 (0.7–12.7) 6.6 (0.6–14.9) 0.042 
Height SDS −0.65 (−3.5 to 2.1) 0.4 (−3.2 to 2.8) <0.001 
Weight SDS 0.1 (−1.4 to 1.4) 0.5 (−1.9 to 5.0) 0.002 
Prevalence of symptoms (%) 84.8 25.4 <0.001 

* Data are median (range) unless otherwise indicated.

Table 2—

Prevalence of celiac disease–related symptoms reported by the diabetic patients before screening for celiac disease was performed and by patients with celiac disease after 2 years of consuming a GFD

Symptoms*Patients without celiac diseasePatients with celiac diseaseP valuePatients consuming a GFD
n 236 33   
Abdominal pain 23 (9.7) 16 (48.5) <0.001 0 
Loose and/or frequent stools 15 (6.4) 7 (21.2) 0.010 2 (6.5) 
Bloating 24 (10.2) 9 (27.2) 0.021 3 (9.7) 
Constipation 2 (0.8) 3 (9.0) 0.014 
Arthralgias 10 (4.2) 7 (21.2) 0.002 1 (3.2) 
Tiredness 6 (2.5) 8 (24.2) <0.001 
Frequent hypoglycemia 1 (0.4) 2 (6.0) 0.040 
Aphthous ulcers 1 (0.4) 1 (3.0) 0.230 
Tooth enamel defects 8 (3.4) 3 (9.0) 0.139 — 
Hemoglobin <6.5 mmol/l — 4 (12.1)  
Serum ferritin <15 μg/l — 9 (27.2) — 1 (3.2) 
Thyroid antibodies 13 (5.5) 3 (9.0) 0.425 — 
Dermatitis herpetiformis 1 (3.0) 0.122 — 
Autoimmune hypothyroiditis 4 (12.1) <0.001 — 
Symptoms*Patients without celiac diseasePatients with celiac diseaseP valuePatients consuming a GFD
n 236 33   
Abdominal pain 23 (9.7) 16 (48.5) <0.001 0 
Loose and/or frequent stools 15 (6.4) 7 (21.2) 0.010 2 (6.5) 
Bloating 24 (10.2) 9 (27.2) 0.021 3 (9.7) 
Constipation 2 (0.8) 3 (9.0) 0.014 
Arthralgias 10 (4.2) 7 (21.2) 0.002 1 (3.2) 
Tiredness 6 (2.5) 8 (24.2) <0.001 
Frequent hypoglycemia 1 (0.4) 2 (6.0) 0.040 
Aphthous ulcers 1 (0.4) 1 (3.0) 0.230 
Tooth enamel defects 8 (3.4) 3 (9.0) 0.139 — 
Hemoglobin <6.5 mmol/l — 4 (12.1)  
Serum ferritin <15 μg/l — 9 (27.2) — 1 (3.2) 
Thyroid antibodies 13 (5.5) 3 (9.0) 0.425 — 
Dermatitis herpetiformis 1 (3.0) 0.122 — 
Autoimmune hypothyroiditis 4 (12.1) <0.001 — 

Data are n (%).

*

A few patients with celiac disease first reported symptoms in retrospect after experiencing the relief with the GFD (three patients reported abdominal pain, a single patient reported abdominal pain, diarrhea, and tiredness, and another patient reported arthralgias).

Some patients reported abdominal pain at breach of the diet.

Table 3—

Development of different clinical parameters in patients with type 1 diabetes and celiac disease measured before and after 6, 12, 18, and 24 months of starting a GFD

nDuration of the GFD
Baseline6 months12 months18 months24 monthsP value
Weight SDS 27 −0.12 0.11 0.25* 0.30* 0.35* 0.002 
Height SDS 27 −0.46 −0.37 −0.31 −0.24 −0.26 0.073 
A1C (%) 28 8.6 9.0 8.8 8.7 8.4 0.300 
Hemoglobin (mmol/l) 25 7.6 8.4* 8.3* 8.4* 8.3* 0.001 
Mean corpuscular volume (fl) 25 81.6 83.0 83.8 83.5 84.4* 0.020 
Ferritin (μg/l) 26 26.0 31.1 39.8* 44* 37.9* 0.012 
Folate (nmol/l) 24 489 606* 637* 639* 581 0.076 
Cobalamin (pmol/l) 25 387 416 415 395 379 0.872 
Calcium (mmol/l) 23 1.24 1.26* 1.26* 1.26* 1.26* 0.044 
ALAT (units/l) 26 24.9 27.2 21.0 19.7* 20.6 0.062 
nDuration of the GFD
Baseline6 months12 months18 months24 monthsP value
Weight SDS 27 −0.12 0.11 0.25* 0.30* 0.35* 0.002 
Height SDS 27 −0.46 −0.37 −0.31 −0.24 −0.26 0.073 
A1C (%) 28 8.6 9.0 8.8 8.7 8.4 0.300 
Hemoglobin (mmol/l) 25 7.6 8.4* 8.3* 8.4* 8.3* 0.001 
Mean corpuscular volume (fl) 25 81.6 83.0 83.8 83.5 84.4* 0.020 
Ferritin (μg/l) 26 26.0 31.1 39.8* 44* 37.9* 0.012 
Folate (nmol/l) 24 489 606* 637* 639* 581 0.076 
Cobalamin (pmol/l) 25 387 416 415 395 379 0.872 
Calcium (mmol/l) 23 1.24 1.26* 1.26* 1.26* 1.26* 0.044 
ALAT (units/l) 26 24.9 27.2 21.0 19.7* 20.6 0.062 

Data are means of the group. At 24 months follow-up, the corresponding P values are also presented. Only a few follow-up data were available from patients with celiac disease diagnosed before this study. The increase in hemoglobin was not caused by the increase in hemoglobin seen in male puberty. Paired comparisons were performed by Wilcoxon signed-ranked test.

*

Significant changes from baseline.

This study received support from The Danish Research Agency and from the counties of Funen, Vejle, and Southern Jutland.

1
Collin P, Kaukinen K, Valimaki M, Salmi J: Endocrinological disorders and celiac disease.
Endocr Rev
23
:
464
–483,
2002
2
Cerutti F, Bruno G, Chiarelli F, Lorini R, Meschi F, Sacchetti C: Younger age at onset and sex predict celiac disease in children and adolescents with type 1 diabetes: an Italian multicenter study.
Diabetes Care
27
:
1294
–1298,
2004
3
Kaspers S, Kordonouri O, Schober E, Grabert M, Hauffa BP, Holl RW: Anthropometry, metabolic control, and thyroid autoimmunity in type 1 diabetes with celiac disease: a multicenter survey.
J Pediatr
145
:
790
–795,
2004
4
Bode S, Gudmand-Hoyer E: Incidence and prevalence of adult coeliac disease within a defined geographic area in Denmark.
Scand J Gastroenterol
31
:
694
–699,
1996
5
Sjoberg K, Eriksson S: Regional differences in coeliac disease prevalence in Scandinavia?
Scand J Gastroenterol
34
:
41
–45,
1999
6
Svensson J, Carstensen B, Molbak A, Christau B, Mortensen HB, Nerup J, Borch-Johnsen K: Increased risk of childhood type 1 diabetes in children born after 1985.
Diabetes Care
25
:
2197
–2201,
2002
7
Hansen D, Bennedbaek FN, Hansen LK, Hoier-Madsen M, Hegedüs L, Jacobsen BB, Husby S: High prevalence of coeliac disease in Danish children with type I diabetes mellitus.
Acta Paediatr
90
:
1238
–1243,
2001
8
Freemark M, Levitsky LL: Screening for celiac disease in children with type 1 diabetes: two views of the controversy.
Diabetes Care
26
:
1932
–1939,
2003
9
Amin R, Murphy N, Edge J, Ahmed ML, Acerini CL, Dunger DB: A longitudinal study of the effects of a gluten-free diet on glycemic control and weight gain in subjects with type 1 diabetes and celiac disease.
Diabetes Care
25
:
1117
–1122,
2002
10
Saadah OI, Zacharin M, O’Callaghan A, Oliver MR, Catto-Smith AG: Effect of gluten-free diet and adherence on growth and diabetic control in diabetics with coeliac disease.
Arch Dis Child
89
:
871
–876,
2004
11
Rami B, Sumnik Z, Schober E, Waldhor T, Battelino T, Bratanic N, Kurti K, Lebl J, Limbert C, Madacsy L, Odink RJ, Paskova M, Soltesz G: Screening detected celiac disease in children with type 1 diabetes mellitus: effect on the clinical course (a case control study).
J Pediatr Gastroenterol Nutr
41
:
317
–321,
2005
12
Sanchez-Albisua I, Wolf J, Neu A, Geiger H, Wascher I, Stern M: Coeliac disease in children with type 1 diabetes mellitus: the effect of the gluten-free diet.
Diabet Med
22
:
1079
–1082,
2005
13
Stern M, Teuscher M, Wechmann T: Serological screening for coeliac disease: methodological standards and quality control.
Acta Paediatr
Suppl
412
:
49
–51,
1996
14
Report of Working Group of European Society of Paediatric Gastroenterology and Nutrition: Revised criteria for diagnosis of coeliac disease.
Arch Dis Child
65
,
909
–911,
1990
15
Feighery C, Abuzakou M, Jackson J, Clooney A, Dunne J, Willoughby R, Whelan A: Coeliac disease serology—EMA negative disease. In
Coeliac Disease: Proceedings of the Xth International Symposium on Coeliac Disease
. Cerf-Bensussan N, Brousse N, Caillat-Zucman S, Cellier C, Schmitz J, Eds. Surrey, U.K., John Libbey Eurotext,
2003
, p.
183
–185
16
Dube C, Rostom A, Sy R, Cranney A, Saloojee N, Garritty C, Sampson M, Zhang L, Yazdi F, Mamaladze V, Pan I, Macneil J, Mack D, Patel D, Moher D: The prevalence of celiac disease in average-risk and at-risk Western European populations: a systematic review.
Gastroenterology
128
:
S57
–S67,
2005
17
Basso D, Gallo N, Guariso G, Pittoni M, Piva MG, Plebani M: Role of anti-transglutaminase (anti-tTG), anti-gliadin, and anti-endomysium serum antibodies in diagnosing celiac disease: a comparison of four different commercial kits for anti-tTG determination.
J Clin Lab Anal
15
:
112
–115,
2001
18
Barera G, Bianchi C, Calisti L, Cerutti F, Dammacco F, Frezza E, Illeni MT, Mistura L, Pocecco M, Prisco F, et al.: Screening of diabetic children for coeliac disease with antigliadin antibodies and HLA typing.
Arch Dis Child
66
:
491
–494,
1991
19
Carlsson AK, Axelsson IE, Borulf SK, Bredberg AC, Lindberg BA, Sjoberg KG, Ivarsson SA: Prevalence of IgA-antiendomysium and IgA-antigliadin autoantibodies at diagnosis of insulin-dependent diabetes mellitus in Swedish children and adolescents.
Pediatrics
103
:
1248
–1252,
1999
20
Vitoria JC, Castano L, Rica I, Bilbao JR, Arrieta A, Garcia M: Association of insulin-dependent diabetes mellitus and celiac disease: a study based on serologic markers.
J Pediatr Gastroenterol Nutr
27
:
47
–52,
1998
21
Sumnik Z, Kolouskova S, Cinek O, Kotalova R, Vavrinec J, Snajderova M: HLA-DQA1*05-DQB1*0201 positivity predisposes to coeliac disease in Czech diabetic children.
Acta Paediatr
89
:
1426
–1430,
2000
22
Barera G, Bonfanti R, Viscardi M, Bazzigaluppi E, Calori G, Meschi F, Bianchi C, Chiumello G: Occurrence of celiac disease after onset of type 1 diabetes: a 6-year prospective longitudinal study.
Pediatrics
109
:
833
–838,
2002
23
Fasano A: Clinical presentation of celiac disease in the pediatric population.
Gastroenterology
128
:
S68
–S73,
2005
24
Westman E, Ambler GR, Royle M, Peat J, Chan A: Children with coeliac disease and insulin dependent diabetes mellitus—growth, diabetes control and dietary intake.
J Pediatr Endocrinol Metab
12
:
433
–442,
1999
25
Acerini CL, Ahmed ML, Ross KM, Sullivan PB, Bird G, Dunger DB: Coeliac disease in children and adolescents with IDDM: clinical characteristics and response to gluten-free diet.
Diabet Med
15
:
38
–44,
1998
26
Kaukinen K, Salmi J, Lahtela J, Siljamaki-Ojansuu U, Koivisto AM, Oksa H, Collin P: No effect of gluten-free diet on the metabolic control of type 1 diabetes in patients with diabetes and celiac disease: retrospective and controlled prospective survey.
Diabetes Care
22
:
1747
–1748,
1999
27
Mohn A, Cerruto M, Lafusco D, Prisco F, Tumini S, Stoppoloni O, Chiarelli F: Celiac disease in children and adolescents with type I diabetes: importance of hypoglycemia.
J Pediatr Gastroenterol Nutr
32
:
37
–40,
2001

A table elsewhere in this issue shows conventional and Système International (SI) units and conversion factors for many substances.

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