The prevalence of celiac disease in average-risk and at-risk Western European populations: A systematic review
2005; Elsevier BV; Volume: 128; Issue: 4 Linguagem: Inglês
10.1053/j.gastro.2005.02.014
ISSN1528-0012
AutoresCatherine Dubé, Alaa Rostom, Richmond Sy, Ann Cranney, Navaaz Saloojee, Chantelle Garritty, Margaret Sampson, Li Zhang, Fatemeh Yazdi, Vasil Mamaladze, Irene Pan, Joanne MacNeil, David R. Mack, Dilip Patel, David Moher,
Tópico(s)Microbial Metabolites in Food Biotechnology
ResumoUntil recently, celiac disease (CD) was felt to be a rare disease in the United States. The aim of this study was to conduct a systematic review of the prevalence of CD in general Western populations and in populations at high risk for CD. Standard systematic review methodology was used. A literature search was conducted in MEDLINE (1966 to October 2003) and EMBASE (1974 to December 2003) databases. Qualitative and quantitative prevalence estimates were produced after assessing study heterogeneity. The prevalence of CD in general Western populations is close to 1% and is somewhat higher in certain Western European populations. The prevalence of CD in populations at risk for CD is as follows: 3%–6% in type 1 diabetic patients, up to 20% in first-degree relatives, 10%–15% in symptomatic iron-deficiency anemia (IDA), 3%–6% in asymptomatic IDA, and 1%–3% in osteoporosis. The prevalence of CD in patients suspected of having CD varied depending on the reasons for suspecting CD and on whether the study was conducted in a referral center. In general, the prevalence ranged from 5% to 15%, but was up to 50% in symptomatic patients evaluated in a tertiary referral center. CD is a common medical condition. The prevalence is higher still in high-risk groups. Clinicians in a variety of specialties should have a high index of suspicion for the diagnosis of CD and in particular need to pay close attention to the identified high-risk groups. Until recently, celiac disease (CD) was felt to be a rare disease in the United States. The aim of this study was to conduct a systematic review of the prevalence of CD in general Western populations and in populations at high risk for CD. Standard systematic review methodology was used. A literature search was conducted in MEDLINE (1966 to October 2003) and EMBASE (1974 to December 2003) databases. Qualitative and quantitative prevalence estimates were produced after assessing study heterogeneity. The prevalence of CD in general Western populations is close to 1% and is somewhat higher in certain Western European populations. The prevalence of CD in populations at risk for CD is as follows: 3%–6% in type 1 diabetic patients, up to 20% in first-degree relatives, 10%–15% in symptomatic iron-deficiency anemia (IDA), 3%–6% in asymptomatic IDA, and 1%–3% in osteoporosis. The prevalence of CD in patients suspected of having CD varied depending on the reasons for suspecting CD and on whether the study was conducted in a referral center. In general, the prevalence ranged from 5% to 15%, but was up to 50% in symptomatic patients evaluated in a tertiary referral center. CD is a common medical condition. The prevalence is higher still in high-risk groups. Clinicians in a variety of specialties should have a high index of suspicion for the diagnosis of CD and in particular need to pay close attention to the identified high-risk groups. Celiac disease (CD) represents a wide spectrum of clinical features. Although classic CD (ie, fully developed gluten-induced villous atrophy and classic features of intestinal malabsorption) is described most commonly, it appears that most patients have atypical CD (fully developed gluten-induced villous atrophy found in the setting of another presentation such as iron deficiency, osteoporosis, short stature, or infertility) or silent CD (fully developed gluten-induced villous atrophy discovered in an asymptomatic patient by serologic screening or perhaps during an endoscopy performed for another reason).1Fasano A. Berti I. Gerarduzzi T. Not T. Colletti R.B. Drago S. Elitsur Y. Green P.H.R. Guandalini S. Hill I.D. Pietzak M. Ventura A. Thorpe M. Kryszak D. Fornaroli F. Wasserman S.S. Murray J.A. Horvath K. Prevalence of celiac disease in at-risk and not-at-risk groups in the United States a large multicenter study.Arch Intern Med. 2003; 163: 286-292Crossref PubMed Scopus (758) Google Scholar, 2Tommasini A. Not T. Kiren V. Baldas V. Santon D. Trevisiol C. Berti I. Neri E. Gerarduzzi T. Bruno I. Lenhardt A. Zamuner E. Spano A. Crovella S. Martellossi S. Torre G. Sblattero D. Marzari R. Bradbury A. Tamburlini G. Ventura A. Mass screening for coeliac disease using antihuman transglutaminase antibody assay.Arch Dis Child. 2004; 89: 512-515Crossref PubMed Scopus (131) Google Scholar The true prevalence of CD is difficult to estimate because of this variable presentation, particularly when many patients can have little or no symptoms. In North America the prevalence has been estimated to be 1:3000, but a recent American study found it to be 1:105 among the general not-at-risk population,1Fasano A. Berti I. Gerarduzzi T. Not T. Colletti R.B. Drago S. Elitsur Y. Green P.H.R. Guandalini S. Hill I.D. Pietzak M. Ventura A. Thorpe M. Kryszak D. Fornaroli F. Wasserman S.S. Murray J.A. Horvath K. Prevalence of celiac disease in at-risk and not-at-risk groups in the United States a large multicenter study.Arch Intern Med. 2003; 163: 286-292Crossref PubMed Scopus (758) Google Scholar suggesting that the disease is underrecognized. We conducted a systematic review of the prevalence of CD in North American and Western European populations and assessed the differences in prevalence among different geographic regions/countries and at-risk populations. This article represents a portion of a multipart systematic review conducted for the Agency for Healthcare Research and Quality. A comprehensive literature search was conducted by the National Library of Medicine in collaboration with the University of Ottawa Evidence Based Practice Center. The searches were run in MEDLINE (1966 to October 2003) and EMBASE (1974 to December 2003) databases. Study selection was performed by 2 independent reviewers using 3 levels of screening. Articles passing the third-level screen fulfilled all the inclusion/exclusion criteria, allowed actual extraction of the prevalence data, and did not have fatal methodologic flaws. Articles were excluded if the studied population was non-North American or Western European, patients were identified by surveys, or if patients were solicited through celiac societies. Study data were abstracted using a predetermined electronic form by 1 reviewer, and were verified by another reviewer. Quality assessments of cross-sectional reports were assessed using a 19-item instrument adapted from Ophthalmology.3Ophthalmology Study Design Worksheet #3. Noncomparative (nonrandomized, noncontrolled) Interventional Case Series. Available from: http://www.elsevier.com/framework_products/promis_misc/620418w3.htm.Google Scholar The prevalence data were anticipated to be heterogeneous. Attempts were made to group studies by age group, study population, and serologic screening method. Statistical heterogeneity was assessed using a Pearson's χ2 test. If no heterogeneity was detected, pooled estimates of the prevalence were produced for that group of studies, otherwise a qualitative systematic review was conducted. For pooled estimates, 95% confidence intervals were calculated. The literature search yielded 2116 references. A total of 133 publications were included in the review. Of these, 14 publications were identified as duplicates on the basis that the same study population was reported on elsewhere, or as part of a larger cohort.4Catassi C. Ratsch I.M. Fabiani E. Ricci S. Bordicchia F. Pierdomenico R. Giorgi P.L. High prevalence of undiagnosed coeliac disease in 5280 Italian students screened by antigliadin antibodies.Acta Paediatr. 1995; 84: 672-676Crossref PubMed Google Scholar, 5Catassi C. Ratsch I.M. Fabiani E. Rossini M. Bordicchia F. Candela F. Coppa G.V. Giorgi P.L. Coeliac disease in the year 2000 exploring the iceberg.Lancet. 1994; 343: 200-203Abstract PubMed Scopus (592) Google Scholar, 6Grodzinsky E. Hed J. Lieden G. Sjogren F. Strom M. Presence of IgA and IgG antigliadin antibodies in healthy adults as measured by micro-ELISA Effect of various cutoff levels on specificity and sensitivity when diagnosing coeliac disease.Int Arch Allergy Immunol. 1990; 92: 119-123Crossref Google Scholar, 7Grodzinsky E. Franzen L. Hed J. Strom M. High prevalence of celiac disease in healthy adults revealed by antigliadin antibodies.Ann Allergy. 1992; 69: 66-70PubMed Google Scholar, 8Lagerqvist C. Ivarsson A. Juto P. Persson L.A. Hernell O. Screening for adult coeliac disease—which serological marker(s) to use?.J Intern Med. 2001; 250: 241-248Crossref PubMed Scopus (48) Google Scholar, 9Weile B. Grodzinsky E. Skogh T. Jordal R. Cavell B. Krasilnikoff P.A. Screening Danish blood donors for antigliadin and antiendomysium antibodies.Acta Paediatr. 1996; 412: 46Crossref Google Scholar, 10McMillan S.A. Watson R.P. McCrum E.E. Evans A.E. Factors associated with serum antibodies to reticulin, endomysium, and gliadin in an adult population.Gut. 1996; 39: 43-47Crossref PubMed Google Scholar, 11Stenhammar L. Brandt A. Wagermark J. A family study of coeliac disease.Acta Paediatr Scand. 1982; 71: 625-628Crossref PubMed Google Scholar, 12Holm K. Savilahti E. Koskimies S. Lipsanen V. Maki M. Immunohistochemical changes in the jejunum in first degree relatives of patients with coeliac disease and the coeliac disease marker DQ genes. HLA class II antigen expression, interleukin-2 receptor positive cells and dividing crypt cells.Gut. 1994; 35: 55-60Crossref PubMed Google Scholar, 13Maki M. Holm K. Lipsanen V. Hallstrom O. Viander M. Collin P. Savilahti E. Koskimies S. Serological markers and HLA genes among healthy first-degree relatives of patients with coeliac disease.Lancet. 1991; 338: 1350-1353Abstract PubMed Scopus (131) Google Scholar, 14Sjoberg K. Wassmuth R. Reichstetter S. Eriksson K.F. Ericsson U.B. Eriksson S. Gliadin antibodies in adult insulin-dependent diabetes—autoimmune and immunogenetic correlates.Autoimmunity. 2000; 32: 217-228Crossref PubMed Google Scholar, 15Carlsson A.K. Axelsson I.E. Borulf S.K. Bredberg A.C. Lindberg B.A. Sjoberg K.G. Ivarsson S.A. Prevalence of IgA-antiendomysium and IgA-antigliadin autoantibodies at diagnosis of insulin-dependent diabetes mellitus in Swedish children and adolescents.Pediatrics. 1999; 103: 1248-1252Crossref PubMed Scopus (80) Google Scholar, 16Ivarsson A. Persson L.A. Nystrom L. Ascher H. Cavell B. Danielsson L. Dannaeus A. Lindberg T. Lindquist B. Stenhammar L. Hernell O. Epidemic of coeliac disease in Swedish children.Acta Paediatr. 2000; 89: 165-171Crossref PubMed Google Scholar, 17Maki M. Holm K. Incidence and prevalence of coeliac disease in Tampere. Coeliac disease is not disappearing.Acta Paediatr Scand. 1990; 79: 980-982Crossref PubMed Google Scholar Thirty-eight studies reported on the prevalence of CD in a general population. Three of these were conducted in the United States,1Fasano A. Berti I. Gerarduzzi T. Not T. Colletti R.B. Drago S. Elitsur Y. Green P.H.R. Guandalini S. Hill I.D. Pietzak M. Ventura A. Thorpe M. Kryszak D. Fornaroli F. Wasserman S.S. Murray J.A. Horvath K. Prevalence of celiac disease in at-risk and not-at-risk groups in the United States a large multicenter study.Arch Intern Med. 2003; 163: 286-292Crossref PubMed Scopus (758) Google Scholar, 18Green P.H. Shane E. Rotterdam H. Forde K.A. Grossbard L. Significance of unsuspected celiac disease detected at endoscopy.Gastroenterol Int. 2000; 51: 60-65Google Scholar, 19Not T. Horvath K. Hill I.D. Partanen J. Hammed A. Magazzu G. Fasano A. Celiac disease risk in the USA high prevalence of antiendomysium antibodies in healthy blood donors.Scand J Gastroenterol. 1998; 33: 494-498Crossref PubMed Scopus (308) Google Scholar 16 in the Scandinavian countries,6Grodzinsky E. Hed J. Lieden G. Sjogren F. Strom M. Presence of IgA and IgG antigliadin antibodies in healthy adults as measured by micro-ELISA Effect of various cutoff levels on specificity and sensitivity when diagnosing coeliac disease.Int Arch Allergy Immunol. 1990; 92: 119-123Crossref Google Scholar, 7Grodzinsky E. Franzen L. Hed J. Strom M. High prevalence of celiac disease in healthy adults revealed by antigliadin antibodies.Ann Allergy. 1992; 69: 66-70PubMed Google Scholar, 8Lagerqvist C. Ivarsson A. Juto P. Persson L.A. Hernell O. Screening for adult coeliac disease—which serological marker(s) to use?.J Intern Med. 2001; 250: 241-248Crossref PubMed Scopus (48) Google Scholar, 9Weile B. Grodzinsky E. 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High prevalence of undiagnosed coeliac disease in adults a Swedish population-based study.J Intern Med. 1999; 245: 63-68Crossref PubMed Scopus (130) Google Scholar, 25Kolho K.L. Farkkila M.A. Savilahti E. Undiagnosed coeliac disease is common in Finnish adults.Scand J Gastroenterol. 1998; 33: 1280-1283Crossref PubMed Scopus (106) Google Scholar, 26Maki M. Mustalahti K. Kokkonen J. Kulmala P. Haapalahti M. Karttunen T. Ilonen J. Laurila K. Dahlbom I. Hansson T. Hopfl P. Knip M. Prevalence of celiac disease among children in Finland.N Engl J Med. 2003; 348: 2517-2524Crossref PubMed Scopus (548) Google Scholar, 27Sjoberg K. Alm R. Ivarsson S.A. Lindstrom C. Eriksson S. Prevalence and clinical significance of gliadin antibodies in healthy children and adults.Scand J Gastroenterol. 1994; 29: 248-254Crossref PubMed Google Scholar, 28Sjoberg K. Eriksson S. Regional differences in coeliac disease prevalence in Scandinavia?.Scand J Gastroenterol. 1999; 34: 41-45PubMed Google Scholar, 29Weile I. Grodzinsky E. Skogh T. Jordal R. Cavell B. Krasilnikoff P.A. High prevalence rates of adult silent coeliac disease, as seen in Sweden, must be expected in Denmark.APMIS. 2001; 109: 745-750Crossref PubMed Google Scholar, 30Borch K. Grodzinsky E. Petersson F. Jonsson K.-A. Mardh S. Valdimarsson T. Prevalence of coeliac disease and relations to Helicobacter pylori infection and duodenitis in a Swedish adult population sample a histomorphological and serological survey.Inflammopharmacology. 2000; 8: 341-350Crossref Scopus (3) Google Scholar, 31Csizmadia C.G.D.S. Mearin M.L. Von Blomberg B.M.E. Brand R. Verloove-Vanhorick S.P. An iceberg of childhood coeliac disease in the Netherlands.Lancet. 1999; 353: 813-814Abstract Full Text Full Text PDF PubMed Google Scholar 9 in Italy,2Tommasini A. Not T. Kiren V. Baldas V. Santon D. Trevisiol C. Berti I. Neri E. 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The smaller size of the 'coeliac iceberg' in adults.Scand J Gastroenterol. 1997; 32: 917-919Crossref PubMed Google Scholar the Netherlands,44Rostami K. Mulder C.J. Werre J.M. van Beukelen F.R. Kerchhaert J. Crusius J.B. Pena A.S. Willekens F.L. Meijer J.W. High prevalence of celiac disease in apparently healthy blood donors suggests a high prevalence of undiagnosed celiac disease in the Dutch population.Scand J Gastroenterol. 1999; 34: 276-279Crossref PubMed Google Scholar Switzerland,45Rutz R. Ritzler E. Fierz W. Herzog D. Prevalence of asymptomatic celiac disease in adolescents of eastern Switzerland.Swiss Med Wkly. 2002; 132: 43-47PubMed Google Scholar and Germany46Jaeger C. Hatziagelaki E. Petzoldt R. Bretzel R.G. Comparative analysis of organ-specific autoantibodies and celiac disease—associated antibodies in type 1 diabetic patients, their first-degree relatives, and healthy control subjects.Diabetes Care. 2001; 24: 27-32Crossref PubMed Google Scholar). Several pairs of duplicate publications were identified including 2 triplets,4Catassi C. Ratsch I.M. Fabiani E. Ricci S. Bordicchia F. Pierdomenico R. Giorgi P.L. High prevalence of undiagnosed coeliac disease in 5280 Italian students screened by antigliadin antibodies.Acta Paediatr. 1995; 84: 672-676Crossref PubMed Google Scholar, 5Catassi C. Ratsch I.M. Fabiani E. Rossini M. Bordicchia F. Candela F. Coppa G.V. Giorgi P.L. Coeliac disease in the year 2000 exploring the iceberg.Lancet. 1994; 343: 200-203Abstract PubMed Scopus (592) Google Scholar, 6Grodzinsky E. Hed J. Lieden G. Sjogren F. Strom M. Presence of IgA and IgG antigliadin antibodies in healthy adults as measured by micro-ELISA Effect of various cutoff levels on specificity and sensitivity when diagnosing coeliac disease.Int Arch Allergy Immunol. 1990; 92: 119-123Crossref Google Scholar, 7Grodzinsky E. Franzen L. Hed J. Strom M. High prevalence of celiac disease in healthy adults revealed by antigliadin antibodies.Ann Allergy. 1992; 69: 66-70PubMed Google Scholar, 8Lagerqvist C. Ivarsson A. Juto P. Persson L.A. Hernell O. Screening for adult coeliac disease—which serological marker(s) to use?.J Intern Med. 2001; 250: 241-248Crossref PubMed Scopus (48) Google Scholar, 9Weile B. Grodzinsky E. Skogh T. Jordal R. Cavell B. Krasilnikoff P.A. Screening Danish blood donors for antigliadin and antiendomysium antibodies.Acta Paediatr. 1996; 412: 46Crossref Google Scholar, 10McMillan S.A. Watson R.P. McCrum E.E. Evans A.E. Factors associated with serum antibodies to reticulin, endomysium, and gliadin in an adult population.Gut. 1996; 39: 43-47Crossref PubMed Google Scholar, 22Grodzinsky E. Screening for coeliac disease in apparently healthy blood donors.Acta Paediatr. 1996; 412: 36-38Crossref Google Scholar, 24Ivarsson A. Persson L.A. Juto P. Peltonen M. Suhr O. Hernell O. High prevalence of undiagnosed coeliac disease in adults a Swedish population-based study.J Intern Med. 1999; 245: 63-68Crossref PubMed Scopus (130) Google Scholar, 29Weile I. Grodzinsky E. Skogh T. Jordal R. Cavell B. Krasilnikoff P.A. High prevalence rates of adult silent coeliac disease, as seen in Sweden, must be expected in Denmark.APMIS. 2001; 109: 745-750Crossref PubMed Google Scholar, 32Catassi C. Fabiani E. Ratsch I.M. Coppa G.V. Giorgi P.L. Pierdomenico R. Alessandrini S. Iwanejko G. Domenici R. Mei E. Miano A. Marani M. Bottaro G. Spina M. Dotti M. Montanelli A. Barbato M. Viola F. Lazzari R. Vallini M. Guariso G. Plebani M. Cataldo F. Traverso G. Ventura A. The coeliac iceberg in Italy. A multicentre antigliadin antibodies screening for coeliac disease in school-age subjects.Acta Paediatr. 1996; 412: 29-35Crossref Google Scholar, 47Holmes G.K. Non-malignant complications of coeliac disease.Acta Paediatr Suppl. 1996; 412: 68-75Crossref PubMed Google Scholar which brought the total number of included unique articles down to 30. The articles with the most complete data were used for the report.1Fasano A. Berti I. Gerarduzzi T. Not T. Colletti R.B. Drago S. Elitsur Y. Green P.H.R. Guandalini S. Hill I.D. Pietzak M. Ventura A. Thorpe M. Kryszak D. Fornaroli F. Wasserman S.S. Murray J.A. Horvath K. Prevalence of celiac disease in at-risk and not-at-risk groups in the United States a large multicenter study.Arch Intern Med. 2003; 163: 286-292Crossref PubMed Scopus (758) Google Scholar, 2Tommasini A. Not T. Kiren V. Baldas V. Santon D. Trevisiol C. Berti I. Neri E. Gerarduzzi T. Bruno I. Lenhardt A. Zamuner E. Spano A. Crovella S. Martellossi S. Torre G. Sblattero D. Marzari R. Bradbury A. Tamburlini G. Ventura A. Mass screening for coeliac disease using antihuman transglutaminase antibody assay.Arch Dis Child. 2004; 89: 512-515Crossref PubMed Scopus (131) Google Scholar, 18Green P.H. Shane E. Rotterdam H. Forde K.A. Grossbard L. Significance of unsuspected celiac disease detected at endoscopy.Gastroenterol Int. 2000; 51: 60-65Google Scholar, 19Not T. Horvath K. Hill I.D. Partanen J. Hammed A. Magazzu G. Fasano A. Celiac disease risk in the USA high prevalence of antiendomysium antibodies in healthy blood donors.Scand J Gastroenterol. 1998; 33: 494-498Crossref PubMed Scopus (308) Google Scholar, 20Carlsson A.K. Axelsson I.E. Borulf S.K. Bredberg A.C. Ivarsson S.A. Serological screening for celiac disease in healthy 2.5-year-old children in Sweden.Pediatrics. 2001; 107: 42-45Crossref PubMed Scopus (115) Google Scholar, 21Collin P. Rasmussen M. Kyronpalo S. Laippala P. Kaukinen K. The hunt for coeliac disease in primary care.QJM. 2002; 95: 75-77Crossref PubMed Google Scholar, 22Grodzinsky E. 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