sota, with type 1 diabetes mellitus on the prevalence date January and patient cohorts from the Mayo Clinic Pediatric Diabetes …
CELIAC DISEASE IN TYPE 1 DIABETES
ORIGINAL ARTICLE
Celiac Disease in Type 1 Diabetes Mellitus in a North American Community: Prevalence, Serologic Screening, and Clinical Features
FARID H MAHMUD, MD; JOSEPH A MURRAY, MD; YOGISH C KUDVA, MBBS; ALAN R ZINSMEISTER, PHD; ROSS A DIERKHISING, MS; BRIAN D LAHR, BS; PETER J DYCK, MD; ROBERT A KYLE, MD; MOUNIF EL-YOUSSEF, MD; LAWRENCE J BURGART, MD; CAROL T VAN DYKE; DEANNA L BROGAN; AND L JOSEPH MELTON III, MD
OBJECTIVES: To estimate the prevalence of celiac disease CD in pediatric and adult type 1 diabetes mellitus in a defined population and to describe clinical features and HLA class II genotypes predictive of CD in screened patients with type 1 diabetes PATIENTS AND METHODS: All residents of Olmsted County, Minnesota, with type 1 diabetes mellitus on the prevalence date January 1, 2001, were identified with the use of an established medical records linkage system Rochester Epidemiology Project and defined clinical criteria Consenting patients underwent serologic screening with endomysial antibody and tissue transglutaminase antibody testing and intestinal biopsies to confirm the diagnosis of CD A subset of screened patients also
underwent HLA class II genotyping Quality-of-life screening Medical Outcomes Study 36Item Short-Form Health Survey was completed in a subset of patients at the time of serologic screening RESULTS: Overall, 392 Olmsted County residents with type 1 diabetes on January 1, 2001, were identified A total of 158 patients with type 1 diabetes were tested, representing 40 158/392 of the enumerated diabetic population, and 11 had biopsy-proven CD for an estimated point prevalence of 70 95 confidence interval, 35-121 Most CD-positive diabetic patients were asymptomatic and expressed an at-risk CD haplotype with at least one of but not both HLA DQ2 or DQ8 CONCLUSIONS: Celiac disease is not rare in North American patients with type 1 diabetes, and most CD-positive diabetic patients are asymptomatic irrespective of age at screening
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CD celiac disease; CI confidence interval; ELISA enzyme-linked immunosorbent assay; EMA endomysial antibody; PCR polymerase chain reaction; REP Rochester Epidemiology Project; SF-36 Medical Outcomes Study 36-Item Short-Form Health Survey; tTg tissue transglutaminase
studies in diabetic populations have estimated the
prevalence of CD to be 15 to 46 in children and 2 to 41 in adults, significantly higher than the estimated 05 to 1 overall prevalence of CD observed in the general population6-15 Both CD and type 1 diabetes are associated with the major histocompatibility complex class II antigen DQ2 encoded by the alleles DQA1501 and DQB1201, thus providing a common genetic basis for expression of both diseases16,17 Despite the advent of sensitive and specific serologic testing, routine screening for CD in diabetic populations is neither a universal nor accepted practice in North America, unlike in other jurisdictions18-22 Much of the controversy derives from previous epidemiological research that suggests that CD is a rare condition in patients with type 1 diabetes in the United States14 Subsequent work that showed a higher prevalence focused on highly selected patients who were referred to academic medical centers and was restricted to either pediatric or adult populations9,23,24 A true population-based estimate of the prevalence of CD from childhood onward in type 1 diabetes is not available from the United States This study examined the prevalence of CD in patients with type 1 diabetes in a
North American community across the entire age spectrum HLA class II genotyping and clinical features are also described
C
eliac disease CD is a chronic disorder characterized by immune-mediated damage to the mucosa of the small intestine1 These changes are triggered by ingestion of gluten and related substances found in cereal grains, such as wheat, barley, and rye Although CD was once believed to be rare in North America, recent studies2-4 have shown an increasing incidence of CD in both pediatric and adult populations However, the classic clinical features of CD, comprising diarrhea and weight loss, are observed less commonly in recently diagnosed cases4 An association between CD and type 1 diabetes mellitus has been recognized for more than 40 years5 European
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From the Division of Pediatric Endocrinology and Metabolism FHM, Division of Gastroenterology and Hepatology JAM, ME-L, CTVD, DLB, Division of Endocrinology, Diabetes, Metabolism, and Nutrition YCK, Department of Health Sciences Research ARZ, RAD, BDL, LJM, Department of Neurology PJD, Division of Hematology RAK, and Department of Laboratory Medicine and Pathology LJB, Mayo Clinic College of Medicine,
Rochester, Minn Dr Mahmud is now with the Childrens Hospital of Western Ontario, London Health Sciences Center, London, Ontario This work was supported by National Institutes of Health Research Grant DK57982 JAM, MO1 RR00585 General Clinical Research Centers Program, RO1 AR30582 Rochester Epidemiology Project, and NS36797 PJD Individual reprints of this article are not available Address correspondence to Joseph A Murray, MD, Division of Gastroenterology and Hepatology, Mayo Clinic College of Medicine, 200 First St SW, Rochester, MN 55905 e-mail: murrayjoseph@mayoedu 2005 Mayo Foundation for Medical Education and Research
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CELIAC DISEASE IN TYPE 1 DIABETES
PATIENTS AND METHODS STUDY SETTING Olmsted County is a medically well-defined population in southeastern Minnesota Population-based studies are feasible because Olmsted County is relatively geographically isolated, and most residents receive their medical care locally through a limited number of medical providers The major provider is the Mayo Clinic in Rochester, Minn, which has
maintained a common medical record with its affiliated hospitals Saint Marys and Rochester Methodist for more than 90 years Recorded diagnoses and surgical procedures are indexed, including diagnoses for outpatients seen during clinic consultations, emergency department visits, or nursing home care and the diagnoses recorded for hospital inpatients, at autopsy examination, or on death certificates Medical records of the other health care providers who serve the local population, notably the Olmsted Medical Group and its affiliated Olmsted Community Hospital Olmsted Medical Center, are also indexed and retrievable Thus, details of the medical care provided to local residents are available for study through this medical records linkage system Rochester Epidemiology Project [REP] as described elsewhere25 According to US census data, the population of Olmsted County was 124,277 in 2000 The population is primarily white; however, recent immigration of Southeast Asian and African populations has increased the nonwhite group to approximately 10 of the total CASE IDENTIFICATION Type 1 Diabetes Mellitus After approval of this project by the institutional review boards of the Mayo Clinic and
the Olmsted Medical Center, the resources of the REP were used to identify residents of Olmsted County with type 1 diabetes All patients with diagnostic codes Hospital Adaptation of the International Classification of Diseases and International Classification of Diseases, Ninth Revision identified for type 1 diabetes and those with diabetes-related complications were included In addition, existing databases and patient cohorts from the Mayo Clinic Pediatric Diabetes Clinic aged 0-18 years, the Rochester Diabetic Neuropathy Study,26 the adult Diabetes Electronic Management System database, and the existing REP Diabetes Study database27 were searched to ensure a complete enumeration of patients Information about residency on the prevalence date January 1, 2001 and vital status was verified using Mayo Clinic, county, and state records Medical records were abstracted for weight, height, age, and clinical features at initial diagnosis of diabetes, including initial and long-term insulin use and the presence of autoimmune thyroid disease Patients were classified as
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having type 1 diabetes with use of clinical criteria at diagnosis weight loss, polyuria, polydipsia,
the presence of ketones, or diabetic ketoacidosis, body mass index a measure of weight in kilograms divided by the square of height in meters 27 kg/m2 at the time of diagnosis, and treatment with insulin at diagnosis and for greater than 1 year subsequently, using previously published criteria28 Diabetic patients were recruited for the study in both pediatric and adult clinical settings Consenting patients underwent blood testing for serologic CD markers IgA endomysial antibody [EMA], IgA tissue transglutaminase [tTg] and HLA haplotyping A questionnaire that detailed clinical and depressive symptoms Medical Outcomes Study 36-Item Short-Form Health Survey [SF-36] also was completed at serologic screening Clinical and laboratory records were reviewed for 6 months before diagnosis to derive a mean hemoglobin A1c level Confirmation of CD Each consenting patient underwent serologic testing for EMA and tTg enzyme-linked immunosorbent assay ELISA4 All patients with positive serologic test results were offered and underwent intestinal biopsies to confirm CD At least 4 samples were taken from the distal duodenum and interpreted by a pathologist who was unaware of the serologic results The
diagnosis of CD required jejunal or duodenal biopsy specimens with partial or complete villous atrophy associated with crypt hyperplasia and a lymphoplasmacytic infiltration in the lamina propria LABORATORY METHODS Anti-tTg IgA testing was undertaken with a commercially obtained ELISA kit Inova Diagnostics, San Diego, Calif and performed as described in detail previously29 In brief, stored serum samples were thawed and diluted with horseradish peroxidase diluent and tested in duplicate at room temperature along with appropriate negative and positive controls The optical density of each pair of duplicates was converted to an ELISA standard by reference to positive controls An ELISA cutoff of less than 20 was normal, 20 to 30 was equivocal, and greater than 30 was positive AntiEMA IgA was detected by an indirect immunofluorescence assay with monkey esophagus as the substrate30 The assays were performed at 3 screening dilutions of 1:5, 1:10, and 1:20 The test result was considered positive when there was a reticulated honeycomb staining of the connective tissue that surrounded the bundles of esophageal smooth muscle HLA class II typing was accomplished by the polymerase chain reaction
PCRsequence-specific primer One Lambda, Canoga Park, Calif This method is a lowresolution test to identify the alleles coded for by the DR1,2,3,4,5 and DQ1 genes of the HLA class II gene locus by PCR Because the test is based on DNA analysis, it is not subject to difficulties with lymphopenia, nonviable
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CELIAC DISEASE IN TYPE 1 DIABETES
TABLE 1 Baseline Characteristics of Olmsted County, Minnesota, Residents With Type 1 Diabetes Mellitus Screened or Not Screened for Celiac Disease Mean SD age at diagnosis y 179116 177114 181121 80 Mean SD duration of diabetes y 188143 186136 192152 90 No with autoimmune thyroiditis 33 84 20 84 13 82 90
Diabetic population Total Not screened Screened P value
No of patients 392 234 60 158 40
Sex male 51 53 48 50
lymphocytes, poor cell surface antigen expression, or poor cellular reactivity Preoptimized primers for the amplification of HLA class II genes were presented in different wells of a tray One Lambda By selecting specific primers, only products that correspond to the different HLA alleles are
amplified A qualitative indicator of specific DNA amplification is obtained by observation of ethidium bromide fluorescence of amplified DNA in control and test bands after quick gel electrophoresis of the PCR products The presence of a band determines the assignment of HLA alleles The specificity of the primers is achieved by constructing oligonucleotides in which the DNA sequence is matched at the 3 end with an allele and mismatched with all other alleles Polymerase chain reaction amplification occurs only when there is a perfect match of both primer and allele Even a single-nucleotide mismatch will block PCR amplification Apparent homozygosity was determined by the failure to identify alternate alleles at a specific locus For this analysis, we considered DQB10201 and DQB10202 as equivalent The likelihood of an alternative undetected allele was extremely low STATISTICAL ANALYSES Continuous variables were summarized as mean SD and categorical variables as frequencies and percentages The 95 confidence intervals CIs for percentages were calculated using the exact binomial distribution Participation bias was examined with use of logistic regression to assess the association among
age at diagnosis, sex, and duration of diabetes with participation agreement to testing [yes/ no] as the dependent variable The association of the presence of CD among tested diabetic patients with clinical variables, physical and mental composite scores, and HLA types was assessed using univariate logistic regression or the Fisher exact test RESULTS PREVALENCE OF CD Overall, 392 Olmsted County residents with type 1 diabetes on January 1, 2001, were identified using uniform cliniMayo Clin Proc
cal criteria A nearly equal sex distribution 191 males [49] was observed The mean SD age at the prevalence date was 367165 years, but most patients were younger than 18 years at the time of diagnosis of type 1 diabetes 235 [60] Age, sex, and duration of diabetes were not associated significantly with whether someone was screened for CD Table 1 A total of 158 diabetic patients underwent serologic testing, and 11 patients with CD were identified Four of these patients were discovered on the basis of clinical symptoms and underwent CD testing performed by their physician; the remaining 7 were identified by serologic screening The estimated crude point prevalence of CD in this diabetic
population was 70 95 CI, 35-121, with a higher rate in females 110; 95 CI, 51-198 compared with males 26; 95 CI, 03-92, which was statistically significant P06 If clinically discovered cases of CD were excluded, a revised point prevalence for CD of 46 95 CI, 19-91 was obtained in the screened patients The prevalence of CD was similar in the 3 pediatric patients 73; 95 CI, 15-199 and 8 adults 68; 95 CI, 30-130, whether we considered their age at testing for CD or the age at diagnosis of diabetes CLINICAL FEATURES OF CD Typical clinical features of CD, including abdominal pain and diarrhea, were absent in most CD-positive patients Table 2 A single pediatric patient age, 14 years had lactose intolerance, and a single adult patient had diarrhea A single adult female patient with confirmed CD identified by screening subsequently developed dermatitis herpetiformis while continuing to ingest gluten No difference was observed in the frequency of autoimmune thyroid disease among the total diabetic population, diabetic patients not screened for CD, and patients screened for CD Table 1 A single patient with CD had autoimmune thyroid disease A subset of diabetic patients n49 completed an SF36
form, which was considered a measure of these patients quality of life Decreases in the physical P33 or mental quality-of-life scores P58 were not associated with CD in this diabetic cohort
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CELIAC DISEASE IN TYPE 1 DIABETES
TABLE 2 Individual Characteristics of Olmsted County, Minnesota, Residents With Type 1 Diabetes Mellitus and Celiac Disease Patient No/ age y/sex 1/10/F 2/14/F 3/17/M 4/29/F 5/34/F 6/45/M 7/56/F 8/31/F 9/40/F 10/65/F 11/68/F Age at diabetes diagnosis y 7 10 10 10 16 14 22 3 9 13 12 Age at CD diagnosis y 10 10 17 29 28 45 56 4 11 41 59 Gastrointestinal symptoms No Yes No No No No Yes Yes Yes Yes Yes tTg U/mL 1690 896 320 480 593 197 1397 Positive biopsy results Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes BMI kg/m2 15 25 22 28 27 28 23 15 17 20 22
EMA 1:5120 1:320 1:80 1:5120 1:640 1:20 1:640
HbA1c 7303 6206 8310 6604 8003 7804
Patients identified by serologic screening are indicated in bold-face type BMI body mass index a measure of weight in kilograms divided by the square of height in meters; CD
celiac disease; EMA endomysial antibody; HbA1c hemoglobin A1c; tTg tissue transglutaminase Biopsy positive refers to histologic features of CD observed on biopsy Mean value 6 months before diagnosis of CD Developed biopsy-confirmed dermatitis herpetiformis Cases 8 through 11 were clinically discovered with use of small bowel biopsy as the primary means of diagnosis and are included for completeness
LABORATORY AND BIOPSY RESULTS In all patients with CD found during serologic screening, positive results were confirmed by EMAs Results from 6 of these patients were positive on tTg IgA antibodies, with 1 patients results marginally below the cutoff level 20 U All 7 screened diabetic patients and the 4 patients with clinically discovered disease had at least partial villous atrophy, crypt hyperplasia, and increased intraepithelial lymphocytes that characterized CD Histologic features of simple increased intraepithelial lymphomatosis were not observed in any sample There was no association between the level of EMA or tTg IgA antibodies and the hemoglobin A1c value HLA HAPLOTYPES The HLA haplotypes for 8 73 of the CD-positive and 58 39 of the CD-negative diabetic patients were obtained
in this study All the tested CD-positive diabetic patients expressed a CD at-risk genotype; 6 patients possessed at least 1 DQ2 allele, and 2 patients expressed DQ8 homozygosity The combination of DQ2 and DQ8 was common in patients with CD-negative diabetes 30/58 In contrast, no diabetic patient who carried DQ2 and DQ8 together had CD 21/58, suggesting that the combination of DQ2 with DQ8 is associated with a lower likelihood of CD vs any other type in the diabetic population P048; Fisher exact test DISCUSSION In this community-based study, the overall prevalence of CD in patients of all ages with type 1 diabetes was 70,
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with similar rates for pediatric and adult groups Comparable North American studies have focused on selected patients seen at referral centers and observed a prevalence of CD in type 1 diabetes that ranged from 14 to 51 in pediatric patients and from 35 to 60 in adults9,14,23,24,31-33 Two European studies34,35 evaluated a combined pediatric and adult type 1 diabetic cohort and observed a biopsyproven prevalence of CD of 36 and 57, respectively However, patient recruitment in both reports was accomplished through convenience sampling at a
tertiary care medical center, potentially introducing reporting bias and overestimation of the actual prevalence of CD in patients with type 1 diabetes Our report, which focused on a community-based sample, indicates that CD is more common in type 1 diabetes than previously reported Although all Olmsted County residents with type 1 diabetes were enumerated, not all were screened for CD However, sex, age, and diabetes duration were not associated with being screened A similar frequency of autoimmune thyroid disease was observed between the screened and unscreened groups It is well accepted that much CD remains undiagnosed in the community2,19,36 Therefore, a strategy of case finding among high-risk populations, such as people with type 1 diabetes, may be an effective way to identify unrecognized CD Because we have enumerated all clinically found CD in the county, we are able to estimate the contribution that screening of the diabetic population would make Our previous study4 described 52 Olmsted County residents with CD, 4 of whom had type 1 diabetes By extrapolating the prevalence rate from those tested to the entire enumerated
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population of patients with type 1 diabetes, we estimate that 18 patients with CD would be identified among the entire Olmsted County diabetic cohort, in addition to the 4 patients whose conditions were diagnosed clinically Thus, a screening effort would increase the identified prevalence of CD by more than one third in the county Extrapolation of our findings to the wider diabetic population suggests that upward of 66,000 diabetic patients also may have CD, based on an estimated 942,000 patients with type 1 diabetes residing in the United States37 Thus, national screening could substantially increase the overall prevalence of diagnosed CD in this group Several screening studies in the general population have suggested a real prevalence of CD of just less than 1, most of which is clinically silent15 Therefore, there could be as many as 17 million cases of CD in the whole US population Thus, while screening patients with type 1 diabetes would add substantially to the numbers of diagnosed CD, it would have only a small overall effect on reducing
the overall numbers of undiagnosed CD in the community Although our study confirms the high prevalence of CD in type 1 diabetes, it is not clear what the consequences of CD are in these patients Only a few studies38,39 have reported that treatment of CD improves glycemic control From a clinical perspective, our patients with CD generally had no serious symptoms Among our pediatric patients, a single patient had a history of lactose intolerance, whereas another had a sibling with CD A single adult patient described diarrhea These findings further confirm the subclinical nature of CD in type 1 diabetes, making diagnosis on purely clinical grounds more difficult Despite attempts to make screening convenient and free, many diabetic patients are apprehensive about CD testing For patients and families, diabetes is a challenging condition that requires daily effort to balance meals, activity, and insulin administration to maintain adequate metabolic control In adult diabetic patients, the presence of complications is associated with worsened quality of life40,41 The effect of an additional chronic disease, such as CD, may substantially affect the quality of life in diabetic patients
Unfortunately, we are not aware of studies that address the psychosocial effect of CD screening in asymptomatic diabetic patients Because the prevalence of CD is higher in patients with type 1 diabetes, many institutions have embarked on screening programs as part of routine care From a medical perspective, numerous advantages may exist in screening asymptomatic diabetic patients, including the potential for improved diabetic control and avoidance of extraintestinal manifestations of CD, notably osteopenia and malignancy18,42 In contrast, routine screening is supported by
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minimal evidence on the long-term outcome of asymptomatic patients with CD, and our review of Mayo Clinic records uncovered no CD-positive diabetic patients with lymphoma, hypocalcemia, or symptomatic fractures, which may be reflective of their relatively younger age at diagnosis of CD mean SD age, 295194 years However, if clinicians overlook minor gastrointestinal symptoms or ascribe them to complications of long-standing diabetes, then routine testing may identify these symptomatic patients Although it is clear that DQ2 or DQ8 are essentially required for CD to occur, our HLA data suggest that
the combination of DQ2 with DQ8 may be relatively protective against development of CD, as suggested in a large population cohort in Finland43 It has been suggested that carriage of both alleles together may reduce the binding or presentation of the gluten peptides to the gluten-reactive T cells in the gut16 HLA information from a larger cohort of type 1 diabetes patients may allow a more precise estimation or prediction of celiac risk in these patients and shed light on the common genetic factors that predispose patients to both diseases The relative proportions of these HLA types may partly explain the variation in the prevalence numbers for CD in different diabetic populations This study had several strengths, including the ability to enumerate all diabetic patients both adults and children in a defined geographic population Furthermore, serologic results were confirmed by biopsy and HLA haplotyping analysis, which has not been performed in a population-based sample The shortcomings of this study may include a small sample size, which would affect wider relevance to other populations Nevertheless, this study identified CD-positive cases in an at-risk population by using rigorous
uniform diagnostic criteria for both type 1 diabetes and CD CONCLUSIONS The prevalence of biopsy-proven CD in a combined pediatric and adult population with diabetes was 70 in a defined North American community This relatively high prevalence rate was associated with minimal or no symptoms or clinical consequences and appeared to affect those with either DQ2 or DQ8 but not both haplotypes This finding indicates that CD in type 1 diabetic populations is not rare and that clinicians caring for those with type 1 diabetes or investigating gastrointestinal symptoms should strongly suspect CD Ultimately, studies of the outcome of testing for CD in this population are needed before widespread screening of patients with type 1 diabetes can be advocated
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REFERENCES 1 Farrell RJ, Kelly CP Celiac sprue N Engl J Med 2002;346:180-188 2 Fasano A, Berti I, Gerarduzzi T, et al Prevalence of celiac disease in atrisk and not-at-risk groups in the United States: a large multicenter study Arch Intern Med 2003;163:286-292 3
Green PHR, Stavropoulos SN, Panagi SG, et al Characteristics of adult celiac disease in the USA: results of a national survey Am J Gastroenterol 2001;96:126-131 4 Murray JA, Van Dyke C, Plevak MF, Dierkhising RA, Zinsmeister AR, Melton LJ III Trends in the identification and clinical features of celiac disease in a North American community, 1950-2001 Clin Gastroenterol Hepatol 2003;1:19-27 5 Payne WW Coeliac disease and diabetes mellitus in the same patient Great Ormond St J 1954-1955;8:118-122 6 Savilahti E, Simell O, Koskimies S, Rilva A, Akerblom HK Celiac disease in insulin-dependent diabetes mellitus J Pediatr 1986;1085, pt 1: 690-693 7 Koletzko S, Burgin-Wolff A, Koletzko B, et al Prevalence of coeliac disease in diabetic children and adolescents: a multicentre study Eur J Pediatr 1988;148:113-117 8 Maki M, Hallstrom O, Huupponen T, Vesikari T, Visakorpi JK Increased prevalence of coeliac disease in diabetes Arch Dis Child 1984;59: 739-742 9 Aktay AN, Lee PC, Kumar V, Parton E, Wyatt DT, Werlin SL The prevalence and clinical characteristics of celiac disease in juvenile diabetes in Wisconsin J Pediatr Gastroenterol Nutr 2001;33:462-465 10 Sigurs N, Johansson C, Elfstrand PO,
Viander M, Lanner A Prevalence of coeliac disease in diabetic children and adolescents in Sweden Acta Paediatr 1993;82:748-751 11 Collin P, Salmi J, Hallstrom O, et al High frequency of coeliac disease in adult patients with type-I diabetes Scand J Gastroenterol 1989;24:81-84 12 Page SR, Lloyd CA, Hill PG, Peacock I, Holmes GK The prevalence of coeliac disease in adult diabetes mellitus QJM 1994;87:631-637 13 Sategna-Guidetti C, Grosso S, Pulitano R, Benaduce E, Dani F, Carta Q Celiac disease and insulin-dependent diabetes mellitus: screening in an adult population Dig Dis Sci 1994;39:1633-1637 14 Rossi TM, Albini CH, Kumar V Incidence of celiac disease identified by the presence of serum endomysial antibodies in children with chronic diarrhea, short stature, or insulin-dependent diabetes mellitus J Pediatr 1993;123:262264 15 Hoffenberg EJ, MacKenzie T, Barriga KJ, et al A prospective study of the incidence of childhood celiac disease J Pediatr 2003;143:308-314 16 Sollid LM Coeliac disease: dissecting a complex inflammatory disorder Nat Rev Immunol 2002;2:647-655 17 Saukkonen T, Ilonen J, Akerblom HK, Savilahti E Prevalence of coeliac disease in siblings of patients with type I
diabetes is related to the prevalence of DQB102 allele Diabetologia 2001;44:1051-1053 18 Freemark M, Levitsky LL Screening for celiac disease in children with type 1 diabetes: two views of the controversy Diabetes Care 2003;26:19321939 19 Fasano A Where have all the American celiacs gone? Acta Paediatr Suppl 1996;412:20-24 20 Cerutti F, Bruno G, Chiarelli F, Lorini R, Meschi F, Sacchetti C, Diabetes Study Group of the Italian Society of Pediatric Endocrinology and Diabetology Younger age at onset and sex predict celiac disease in children and adolescents with type 1 diabetes: an Italian multicenter study Diabetes Care 2004;27:1294-1298 21 Consensus Development Panel National Institutes of Health Consensus Development Conference Statement on Celiac Disease, June 28-30, 2004 Available at: http://consensusnihgov/2004/2004CeliacDisease118htmlhtm Accessibility verified September 8, 2005 22 Hill ID, Dirks MH, Liptak GS, et al Guideline for the diagnosis and treatment of celiac disease in children: recommendations of the North Ameri-
can Society for Pediatric Gastroenterology, Hepatology and Nutrition J Pediatr Gastroenterol Nutr 2005;40:1-19 23 Rensch MJ, Merenich JA, Lieberman M, Long
BD, Davis DR, McNally PR Gluten-sensitive enteropathy in patients with insulin-dependent diabetes mellitus Ann Intern Med 1996;124:564-567 24 Talal AH, Murray JA, Goeken JA, Sivitz WI Celiac disease in an adult population with insulin-dependent diabetes mellitus: use of endomysial antibody testing Am J Gastroenterol 1997;92:1280-1284 25 Melton LJ III History of the Rochester Epidemiology Project Mayo Clin Proc 1996;71:266-274 26 Dyck PJ, Kratz KM, Lehman KA, et al The Rochester Diabetic Neuropathy Study: design, criteria for types of neuropathy, selection bias, and reproducibility of neuropathic tests Neurology 1991;41:799-807 27 Leibson CL, OBrien PC, Atkinson E, Palumbo PJ, Melton LJ III Relative contributions of incidence and survival to increasing prevalence of adult-onset diabetes mellitus: a population-based study Am J Epidemiol 1997; 146:12-22 28 Melton LJ III, Palumbo PJ, Chu CP Incidence of diabetes mellitus by clinical type Diabetes Care 1983;6:75-86 29 Locke GR III, Murray JA, Zinsmeister AR, Melton LJ III, Talley NJ Celiac disease serology in irritable bowel syndrome and dyspepsia: a population-based case-control study Mayo Clin Proc 2004;79:476-482 30 Chorzelski TP,
Sulej J, Tchorzewska H, Jablonska S, Beutner EH, Kumar V IgA class endomysium antibodies in dermatitis herpetiformis and coeliac disease Ann N Y Acad Sci 1983;420:325-334 31 Fraser-Reynolds KA, Butzner JD, Stephure DK, Trussell RA, Scott RB Use of immunoglobulin A-antiendomysial antibody to screen for celiac disease in North American children with type 1 diabetes Diabetes Care 1998;21: 1985-1989 32 Barera G, Bonfanti R, Viscardi M, et al Occurrence of celiac disease after onset of type 1 diabetes: a 6-year prospective longitudinal study Pediatrics 2002;109:833-838 33 Hansen D, Bennedbaek FN, Hansen LK, et al High prevalence of coeliac disease in Danish children with type I diabetes mellitus Acta Paediatr 2001;90:1238-1243 34 Seissler J, Schott M, Boms S, et al Autoantibodies to human tissue transgutaminase identify silent coeliac disease in type I diabetes [letter] Diabetologia 1999;42:1440-1441 35 Not T, Tommasini A, Tonini G, et al Undiagnosed coeliac disease and risk of autoimmune disorders in subjects with type I diabetes mellitus Diabetologia 2001;44:151-155 36 Catassi C, Fabiani E, Ratsch IM, et al The coeliac iceberg in Italy: a multicentre antigliadin antibodies screening
for coeliac disease in school-age subjects Acta Paediatr Suppl 1996;412:29-35 37 Amos AF, McCarty DJ, Zimmet P The rising global burden of diabetes and its complications: estimates and projections to the year 2010 Diabet Med 1997;14suppl 5:S1-S85 38 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 2002;25:1117-1122 39 Saadah OI, Zacharin M, OCallaghan 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 2004;89:871-876 40 Rubin RR, Peyrot M Quality of life and diabetes Diabetes Metab Res Rev 1999;15:205-218 41 Jacobson AM, de Groot M, Samson JA The evaluation of two measures of quality of life in patients with type I and type II diabetes Diabetes Care 1994;17:267-274 42 Holmes GK Non-malignant complications of coeliac disease Acta Paediatr Suppl 1996;412:68-75 43 Maki M, Mustalahti K, Kokkonen J, et al Prevalence of celiac disease among children in Finland N Engl J Med 2003;348:2517-2524
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