Celiac Disease. Detlef Schuppan HARVARD MEDICAL SCHOOL
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1 Celiac Disease Detlef Schuppan Falk Symposium in the Intestinal Tract: Pathogenesis and Treatment, Kiev,, Ukraine, May 15-16, 16, 2009 HARVARD MEDICAL SCHOOL
2 Celiac Disease Intolerance to gluten from wheat, rye and barley Shows characteristic alterations of the small intestinal mucosa (villous atrophy, crypt hyperplasia) ) = gold standard Consequences: from asymptomatic to severe diarrhea and malabsorption May lead to health complications if untreated (auto-immune diseases, some cancers) Final diagnosis: : positive autoantibodies and characteristic duodenal histology Therapy: strict gluten free diet
3 Epidemiology and Associated Disorders
4 The Celiac Disease Iceberg Prevalence of classical celiac disease: Ireland 1:300, Sweden 1:1.000, Denmark 1: Autoantibody screening & confirmation by duodenal biopsy Prevalence of screening-detected celiac disease: Finland 1:68, Turkey 1:78, USA 1:154, Italy 1:165, India 1:200 Silent or atypical celiac disease is 5-15 times as frequent as classical celiac disease
5 Findings in 82 new diagnosed children with Cd Symptoms n iron deficiency anaemia 24 iron deficiency w/t anaemia (Ferritin ) 22 recurr.. abdominal pain 20 mood disorders 14 aphtous stomatitis 9 loss of appetite 8 recurrent diarrhoea 7 growth retardation 6 meteorism 4 obstipation 2 retarded puberty, serum albumin 2+2 Italian SIGEP-study Catassi et al, Acta Paediatr 85, S412, 1996 Prevalence 1:154
6 Diarrhea Autoimmune thyroiditis Autoimmunity Dermatitis herpetiformis Autoimmune hepatitis Type I diabetes Trisomy 21 Malignancy Malabsorption Anemia Osteoporosis Infertility/Abortions Hypertransaminasemia & Liver failure Irritable bowel syndrome Migraine Intestinal T cell lymphoma Non Hodgkin lymphoma Neuropsychiatric Schizophrenia Ataxia
7 Pathogenesis
8 albumins soluble in neutral salt solutions activation of innate immunity Gluten prolamines (gliadins) soluble in 50-70% ethanol % Glu/ Gln,, 15-30% Pro α,, β,, γ,, ω gliadins glutenins of wheat soluble in acids and bases 45% Glu/ Gln > 50 different toxic peptides in the more than 100 different gluten proteins per wheat variant predicted Vader et al, J Exp Med 2002
9 Celiac disease associated HLA-DQ2 ~ 15% of first degree relatives affected gliadin peptide HLA DQ2 heterodimer T cell response cd pts: : 95% DQ2, 5% DQ8 general population: ~30% β1*0201 α1*0501 DR3 α1*0505 DR5 encoded in cis β1*0202 DR7 encoded in trans (¼ gene dose) Sollid et al, J Exp Med 1989 Lundin et al, J Exp Med 1993
10 Transglutaminase 2 (ttg) the endomysial autoantigen Serum IgA anti-ttg ttg (EMA) is nearly 100% sensitive and specific for the presence of celiac disease Mr 85 kd, cytosolic, cellular, type II, liver-tg Released from cells during wounding, infection and stress Catalyses the irreversible cross-linking of certain matrix and intracellular proteins The glutamine-rich gliadins and glutenins are preferred substrates for ttg At acid ph, ttg deamidates certain glutamines in gliadins and glutenins (change from neutral Q to acidic E) Dieterich et al, Nat Med 1997; Dieterich et al, Gastroenterology 1998; Sulkanen et al, Gastroenterology 1998
11 α β T cell receptor Th1 (Th2)-response Q L Q P QLQPFPQPELPYPQP LPYPQP ttg F QLQPFPQPQLPYPQP LPYPQP α1 glia Johannsen et al, Int Immunol 1996 Molberg et al, Nat Med 1998 Van de Waal, J Immunol 1998 Anderson et al, Nat Med 6, 337, 2000 P 1 P Q E L Y H H H HLA - DQ2 Triggers of celiac disease 100% genetic (DQ2/DQ8) dietetic (gluten) 100% P 100% autoimmunity (ttg) P Celiac disease Q P Infections (viruses, bacteria)
12 dietary gluten peptides Intestinal lumen Mucosal permeability increase Intestinal (villous) epithelium Gluten peptides react with ttg in the subepithelial lamina propria Gluten peptides get crosslinked and deamidated and are presented to T cells by APC with HLA-DQ2 or -DQ8 Gluten peptide Deamidated gluten peptide ttg Antigen presenting cell Gluten stimulates innate immunity in epithelia, macrophages & dendritic cells CD4+ T cell this drives activation of intraepithelial lymphocytes these (Th1) T cells cause matrix destruction villous atrophy IFNγ, TNFα Gluten specific T cells are stimulated and proliferate B cell (Myo-)) Fibroblast Basement membrane Lamina propria MMP-1, 1,-3, 3,-12 these T cells stimulate B cells to produce antibodies to gluten and ttg the autoantibodies are bound in the tissue or released into the blood
13 Screening for & Diagnosis of Celiac Disease
14 IgG/IgA IgA α-gliadin IgA α-ttg (EmA) Celiac disease? Mucosal biopsy (4-5 samples) symptoms but no autoantibodies (confirmation of other diseases) IgA deficiency (in celiacs 10-fold increased: : 2% IgG anti-ttg ttg) The blood test for IgG antibodies to deamidated gliadin is useful as confirmatory & supplementary test Bai et al, J Clin Gastroenterol Hepatol 2006 Rashtak S et al, Alim Pharmacol Ther 2008 Gluten-free diet Repeat-biopsy Gluten-free diet IgA α-ttg
15 Autoantibody (anti-ttg) screening for celiac disease 1st and 2nd degree relatives of celiacs patients with cd-associated autoimmunity (DM1, dermatitis herpetiformis, ai-hepatitis hepatitis, thyroiditis...) certain unexplained neuropsychiatric disorders (cerebellar ataxia, migraine...) unexplained hypertransaminasaemia or liver failure unexplained anaemia / osteoporosis unexplained abortions / infertility representative biopsies still useful for 1 st diagnosis
16 Genetic risk factors
17 Non HLA DQ genetic risk factors for celiac diseases Genome wide association study UK, Irish & Dutch population 1643 celiacs & 3406 controls 310,000 SNPs (out of 8 Mio expected) 35% additional low impact genes via linkage analysis or candidate gene approach 3-4% most genes linked to T cell activation Van Heel DA al, Nat Gen 2007 Hunt KA et al, Nat Gen 2008 Dubois & van Heel, Clin Exp Immunol 2008
18 Refractory Sprue occurs in up to 5% of treated adults exclude inadvertent gluten ingestion by taking a meticulous dietary history exclude other (additional) disorders: similar histology bacterial overgrowth tropical sprue giardiasis/ / M. Whipple ai enteropathy (lactose intolerance) normal histology intestinal allergy pancreatic insufficiency irritable bowel syndrome microscopic colitis
19 Refractory Sprue (2) villous atrophy that is refractory to a strict gluten free diet normal cytological picture,, but abnormal IEL- phenotype (RCd( type II): CD3(+) CD103+ CD8- CD4- TCRαβ αβ- clonal TCRγ-rearrangement (RCd( type II) 1 st line treatment with Corticosteroids & Azathioprine progression to overt T cell-lymphoma lymphoma (RCd type II) Cellier et al, Gastroenterology 1998 & Lancet 2000; Carbonnel et al, Blood 1998 Bagdi et al, Blood 1999; Daum et al, Gut 2001; Meijer et al, Scand J Gastroenterol 2004 Al-Toma et al., Clin Gastroenterol Hepatol 2006
20 Survival with Refractory Coeliac Disease Type I and Type II % of deaths 50 mortality 14%: normal IEL CD3+/CD8+ (n=7): RCd type I 25 mortality 41%: abnormal IEL: CD3+/CD8- (n=34): RCd type II follow- up: months Cellier C et al, 2002
21 Nondietary therapies for celiac disease
22 The gluten free diet is an efficient and safe therapy but frequently Is not as palatable as a gluten containing diet Is a social burden Is difficult to maintain (travel, inadvertent gluten exposure) Problem of noncompliance
23
24 4. Gluten binders 5. Permeability inhibitors (AT-1001) Mucosal permeability increase dietary gluten peptides 1. Modified gluten 2. Glutenases Intestinal lumen 3. Oral neutralizing cow s antibodies to gluten Intestinal (villous) epithelium Gluten peptides react with ttg in the subepithelial lamina propria 6. ttg - inhibitors After reaction with ttg (deamidation) gluten peptides bind much better to HLA- DQ2 or -DQ8 on antigen presenting cells Gluten peptide Deamidated gluten peptide ttg (transglutaminase) Antigen presenting cell Gluten stimulates innate 9. immunity Lymphocyte in epithelia, blocking (anti-il macrophages IL-15, anti-ccr9) & dendritic cells CD4+ T cell 7. DQ2-blocking peptides this drives activation of intraepithelial lymphocytes IFNγ, TNFα Gluten specific T cells get stimulated and proliferate 8. Tolerance induction Gluten immunization B cell (Myo-)) Fibroblast Basement membrane Lamina propria these (Th1) T cells cause matrix destruction villous atrophy Proteases (MMP-1, 1,-3, 3,-12) These T cells stimulate B cells to produce antibodies to gluten and ttg The autoantibodies are bound in the tissue or released into the blood
25 COMPETIZIONE PASTA NAPOLI 1958
26 Celiac disease Cd is the most frequent intestinal (auto-) ) immune disease Most cases are not associated with diarrhea or overt malabsorption, but are silent or atypical Cd is the best defined HLA-linked disease, with gluten (and other cereal proteins) as trigger, HLA-DQ2 (DQ8) as necessary genetic predisposition and ttg as pathogenetically linked autoantigen Disease severity depends on 1. gluten dose, 2. HLA- DQ2(DQ8)-gene dose,, 3. innate immunity,, additional polygenetic and environmental factors The development of nondietary therapies is on the way
27
28 why do individual patients display such a variable response to gluten? Gene dose and (early( early) gluten exposure DQ2/DQ2 DQ2/DQ2 Villous atrophy Normal villi Microbial Microbial infection infection (early) gluten dose DQ2/DQx DQx Threshold of gluten intolerance Vader et al, PNAS 2003
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