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CELIAC DISEASE: THE GREAT IMPOSTER. Jamie S. Barkin, M.D., MACP, MACG, AGAF, FASGE Professor of Medicine University of Miami, Miller School of Medicine Chief, Division of Gastroenterology Mt. Sinai Medical Center. Introduction.

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CELIAC DISEASE:

THE GREAT IMPOSTER

Jamie S. Barkin, M.D., MACP, MACG, AGAF, FASGE

Professor of Medicine

University of Miami, Miller School of Medicine

Chief, Division of Gastroenterology

Mt. Sinai Medical Center


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Introduction

  • Celiac disease is a genetically-determined autoimmune condition that can present at any age

  • It is a permanent intolerance to the gliadin fraction of proteins in wheat, barley and rye

  • Prevalence 1:100 to 1:150 persons

  • Caucasians are more at risk than other races

McGough N, Cummings JH. Proc Nutr Soc 2005;64:434-450

Marmouz F. Eur Ann Allergy & Clin Immunology 2007;39:23-25


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Prevalence of Celiac Disease

Healthy population - 1:133

1st degree relatives - 1:18 to 1:22

2nd degree relatives - 1:24 to 1:39

Fasano, et al. Arch Intern Med 2003;163:286-92


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Celiac Disease

Three peaks:

  • Infancy

  • Second to third decade of life

  • Fifth to sixth decade of life

    Delay in diagnosis – 7 years

Ciclitira PJ. Nature Clinical Practice Gastroenterology & Hepatology 2007 (4);9:483


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The Celiac Iceberg

Manifest mucosal lesion

Symptomatic Celiac disease

Silent celiac disease

Normal mucosa

Latent Celiac Disease

Genetic susceptibility – DQ2, DQ8 Positive serology

(Adapted) CDHNF - NASPGHAN


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Stages of Celiac Disease

Symptom Serology Histology

Latent - + -

Silent - + +

Diarrhea + + +


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Spectrum of Celiac Disease

Biopsy

Symptoms

Malabsorption

Villous Atrophy

1%

IEL

Atypical/Asymptomatic


Does clinical presentation correlate with degree of villous atrophy in patients with celiac disease l.jpg
Does clinical presentation correlate with degree of villous atrophy in patients with celiac disease?

  • Classical presentation– diarrhea and weight loss symptoms

  • Atypical or silent presentation – anemia, osteoporosis or dermatitis herpetiformis

    Aim: To evaluate the correlation between the clinical presentation of patients with celiac disease and the degree of villous atrophy

    Results:

  • 499 patients, more of whom had atypical or silent celiac disease than classical presentation – 56% vs. 44%

  • Clinical presentation did not correlate with the degree of villous atrophy in patients with celiac disease

www.nature.com/clinicalpractice/gasthep


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Celiac Disease World-Wide atrophy in patients with celiac disease?

  • Iran - common finding among patients labeled as irritable bowel syndrome (11%) in Iran

  • India - common cause of chronic diarrhea both in children and in adults

  • Central America/Puerto Rico/South America - under-diagnosed


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Conditions more common in celiac disease atrophy in patients with celiac disease?

(Adaptation) McGough N, Cummings JH. Proc Nutr Soc 2005;64:434-450


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Associations of CD atrophy in patients with celiac disease?

  • Hematological: IgA – deficiency, hemolytical anemia, thrombopenic purpura

  • Nephrological: IgA – nephropathy

  • Hepatic and digestive: primary biliary cirrhosis, Crohn’s disease and colorectal bleeding

  • Lupus, Sjögren’s syndrome myasthenia, rheumatoid arthritis, polyarthritis

  • Atopia, asthma, disease of farmer’s lung or poultry breeders

Marmouz F. Eur Ann Allergy & Clin Immunology 2007;39:23-25


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Pathophysiology of celiac disease atrophy in patients with celiac disease?

  • Malabsorption of nutrients, especially iron, folate, calcium and vitamin D

  • Increased intestinal permeability may permit entry of other toxins which might induce autoimmune diseases

CDHNF - NASPGHAN


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Incidence of autoimmune diseases in celiac disease (CD): protective effect of the gluten-free diet

AIM:

To determine which factors modulate the risk of autoimmune disease and to evaluate the effect of gluten-free diet in 924 celiac patients

Results

  • The cumulative risk of autoimmune disease was 8.1% ±1% at age 15, and 15.7%± 1.5% at age 30

  • Factors associated with an increased risk were family history of autoimmunity and diagnosis of CD before age 36

Cosnes J, et al. Clinical Gastroenterology and Hepatology 2008;;6:753-758


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Incidence of autoimmune diseases in celiac disease (CD): protective effect of the gluten-free diet

(Cont)

Results

  • After CD diagnosis, 55/788 patients developed an autoimmune disease

  • The cumulative risk of subsequent autoimmune disease was lower in patients compliant to a gluten-free diet vs. noncompliant patients

  • The incidence of autoimmune diseases was 5.4 per 1000 patient-years during adherence to a gluten-free diet vs. 11.3 per 1000 patient-years during non-adherence to the diet

Cosnes J, et al. Clinical Gastroenterology and Hepatology 2008;;6:753-758


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Factors in celiac disease protective effect of the gluten-free diet

  • Genetic susceptibility

  • Immune system

  • Environment - Gluten in diet


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Genetics and pathogenesis of celiac disease protective effect of the gluten-free diet

  • Concordance is 75 – 90% in monozygotic twins and 10 – 20% in dizygotic twins

  • In first-degree relatives the prevalence is 10% and in second-degree relatives it is 2%

  • Patients with CD (95%) carry the human leukocyte antigen (HLA, HLA-DQ2 or HLA-DRB*4 DQ8)

McGough N, Cummings JH. Proc Nutr Soc 2005;64:434-450


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Non-dietary factors protective effect of the gluten-free diet

  • Infections

    • Viral infections

      • Sequence homology between -gliadin and adenovirus type 12 & 7, rubella and human herpes-virus 1

    • Parasitic infestations

      • sequence homology between -gliadin and plasmodium yoelli

    • Other ?

CDHNF - NASPGHAN


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Dietary Factors protective effect of the gluten-free diet

  • Wheat – (15% protein, 75% starch)

Gluten

Gliadin

Glutenin

(alcohol soluble) Prolamine

(alcohol insoluble)

  • Rye prolamines – secalines

  • Barley prolamines – hordeins

  • Oats are safe

CDHNF - NASPGHAN


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Mucosal events protective effect of the gluten-free diet

  • Epithelial cell infiltration

    • increased IEL’s – (>90% CD8, <10% CD4)

    • increased mucosal / T cells (nl <10%)

    • role of / cells in celiac disease is unknown

  • Mucosal surface alterations

    • loss of epithelial cells

    • proliferation of crypt epithelial cells

CDHNF - NASPGHAN


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Humoral response in celiac disease protective effect of the gluten-free diet

  • Humoral response

    • Enhanced antibody production

      • Anti-tissue transglutaminase

      • Anti-gliadin

      • ? Other auto-antigens (anti-actin)

    • Mechanism of antibody production unknown

CDHNF - NASPGHAN


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Expanded Definition of celiac disease protective effect of the gluten-free diet

  • Celiac disease is an autoimmune condition

  • Occurs in genetically susceptible individuals

  • DQ2 and/or DQ8 positive HLA haplotype is necessary but not sufficient

  • A unique autoimmune disorder because:

    • Both the environmental trigger (gluten) and the auto-antigen (tissue transglutaminase) are known

    • Elimination of the environmental trigger leads to a complete resolution of the disease

CDHNF - NASPGHAN


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Celiac Disease and autoimmunity protective effect of the gluten-free diet

  • Prevalence of autoimmune disorders in celiac disease related to duration of gluten exposure

    • Diagnosed before 2 years of age: 5%

    • Age 2-10 years: 17%

    • Greater than age 10 years: 24%

  • Increased incidence of autoimmune disease in patients with IDDM and ‘silent’ celiac disease and their first-degree relatives who were EMA+

Ventura et al. Gastro 1999; Not, Diabetologia 2001



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Visible Iceberg of CD conditions

Diarrhea

Abdominal pain

Weight loss

Constipation

Bloating


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Presenting features of celiac disease conditions

  • Adults

    • Diarrhea, altered bowel habit including constipation

    • Abdominal pain, dyspepsia, bloating

    • Aphthous ulcers – mouth

    • Anemia (fe or folate and rarely vitamin B-12)

    • Weight loss

    • Dermatitis herpetiformis

    • Malabsorption, edema

    • Osteoporosis, low impact fracture

McGough N, Cummings JH. Proc Nutr Soc 2005;64:434-450


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Invisible Part of the Iceberg conditions

  • Hematological: iron deficiency anemia

  • Rheumatologic: demineralization, arthralgias fractures

  • Neurological: peripheral neuropathy (lack of), epilepsy (and cerebral calcifications) ataxia (vitamin E deficiency?), Migraine

  • Digestive: stimulating functional, mouth ulcers, unexplained increase of transaminases and rare severe hepatopathy

  • Gynecological: infertility, amenorrhea, fetal hypotrophy, miscarriages

Marmouz F. Eur Ann Allergy & Clin Immunology 2007;39:23-25


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Increased overall mortality in adult life conditions

Secondary to increased:

  • Autoimmune diseases

  • Osteoporosis

  • Liver diseases

  • Cancer

CDHNF - NASPGHAN


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COMPLICATIONS conditions




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Iron deficiency anemia resistant to oral iron Disease

  • One of the most common non-GI manifestation in adult studies

  • 5 – 8% of adults with unexplained iron deficiency anemia have celiac disease

  • In children with newly diagnosed celiac disease

    • Anemia is common

    • Little evidence that celiac disease is common in children presenting with anemia

CDHNF - NASPGHAN


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Bone Disease in Celiac Disease Disease

  • Arthritis

  • Osteoporosis

  • Osteopenia

  • Osteomalacia

  • Rickets

CDHNF - NASPGHAN


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Bones and Celiac Disease Disease

  • CD presenting with classic malabsorptive symptoms was the association with bone disease, particularly osteomalacia (Bennet et al, 1932)

  • Reduced bone mineral density, osteopenia or osteoporosis in 20 – 50% of the patients newly diagnosed with CD (Butcher, et al 1992; Corazza, et al 1995, 1996; Mc Farlane et al, 1995; Kemppainen et al, 1999; Cellier et al 2000; Meyer et al 2001)

  • The consequences of these bone changes are probably an increase in aches and pains

Cont

McGough N, Cummings JH. Proc Nutr Soc 2005;64:434-450


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Bones and Celiac Disease Disease

  • Increased fracture is reported , but the risk is small

  • Patients who presented subclinically with anemia or osteopenia or just on screening, the fracture risk is not increased compared with the controls

  • BMD does improve with a GFD but may not return to that seen in a matched population (Corraza et al. 1995; McFarlane et al 1995; Sategna-Guidetti et al. 2000; Pazianas et al. 2005)


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Risk of cancer in celiac disease Disease

(Adaptation) McGough N, Cummings JH. Proc Nutr Soc 2005;64:434-450


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“Hepatitis” and Celiac Disease Disease

  • Evidence for elevated serum transaminases (ALT, AST) in adults with untreated celiac disease

    • Up to 9% of adults with elevated ALT, AST may have silent celiac disease

    • Liver biopsies in these patients showed non-specific reactive hepatitis – may simulate NASH

    • Liver enzymes normalized on gluten-free diet

CDHNF - NASPGHAN


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Celiac disease screening amongst women of reproductive age Disease

  • A Swedish cohort study compared 2078 births by women diagnosed with celiac disease prior to or after the birth of an infant with the background child-bearing population

    Result:

  • Undiagnosed maternal celiac disease at birth was strongly linked to low or very low infant birth weight, lower placental weights and higher Cesarean section rate

Ludvigsson JF et al. Gastroenterology 2005;129:454-463


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Dermatitis Herpetiformis Disease

  • Erythematous macule >urticarial papule > tense

    vesicles

  • Severe pruritus

  • Symmetric distribution

  • 90% no GI symptoms

  • 75% villous atrophy

  • Gluten sensitive

Garioch JJ et al. Br J Dermatol 1994;131:822-6

Fry L. Baillieres Clin Gastroenterol 1995;9:371-93

Reunala T, et al. Br J Dermatol 1997;136:315-8


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Diagnostic principles of celiac disease Disease

  • Confirm diagnosis before treating

    • Diagnosis of celiac disease mandates a strict gluten-free diet for life

      • following the diet is not easy

      • QOL implications

  • Failure to treat has potential long-term adverse health consequences

    • Increased morbidity and mortality

CDHNF - NASPGHAN


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Role of serological tests in Celiac Disease Disease

  • Identify symptomatic individuals who need biopsy

  • Screening of asymptomatic “at risk” individuals who need a biopsy

  • Supportive evidence for the diagnosis

  • Monitoring dietary compliance

CDHNF - NASPGHAN


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Serological tests Disease

  • Antigliadin antibodies (AGA)

  • Antiendomysial antibodies (EMA)

  • Anti-tissue transglutaminase antibodies (TTG)

    • First generation (guinea pig recombinant

    • Second generation (human recombinant)

  • HLA typing

CDHNF - NASPGHAN


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Serological Test Comparison Disease

Farrell RJ, Kelly CP. Am J Gastroenterol 2001;96:3237-46


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Anti-gliadin antibodies (AGA) Disease

  • Sensitivity and specificity do not exceed 80%

  • The specificity of AGA IgA is approximately 50%

  • False positive results can be found in patients with esophagitis, gastroenteritis, inflammatory bowel diseases

Basso D, et al Lupus 2006;15:462-465


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Serology diagnosis of celiac disease Disease

  • Tissue transglutaminase is the serological test of choice for the diagnosis of CD

  • Selective IgA deficiency is found in 2-3% of individuals with CD and affects not only tTg IgA antibodies but also EMA and AGA IgA antibodies

  • Both IgA and IgG AGA antibodies are present in the sera of patients with CD, although they are not specific because gliadin crosses the normal gut mucosa, and approximately 5 -10% of the healthy population will be positive, particularly older individuals

McGough N, et al Proceedings of the Nutrition Society 2005;64;434-450


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Biopsy diagnosis of celiac disease Disease

Histological Features:

  • Increased IEL’s (>30/100 enterocytes)

  • Loss of nuclear polarity

  • Change from columnar to cuboid

  • Lamina propria cellular infiltrate

  • Crypt elongation and hyperplasia

  • Increased crypt mitotic index

  • Progressive villous flattening

CDHNF - NASPGHAN


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Role of “Routine” Small Bowel Biopsy at Endoscopy Disease

  • Current practices by pediatric GI physicians

  • Rationale:

    • Celiac disease is common and endoscopic appearance may look normal

    • Era of open access endoscopy

  • Routine biopsy in high-risk groups

    • Family members

    • Chronic liver disease

    • IBS, IDDM, IBD, Sjögren syndrome

    • Down’s syndrome

    • Patients with atypical symptoms


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Mucosal Differential Diagnosis of Immunopathology Disease

  • Celiac

  • Giardiasis

  • Milk intolerance

  • Tropical sprue

  • GVHR

Marsh, Gastroenterol 1992;102:330-354


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Two main problems when considering screening Disease

  • ~25 – 30% of individuals with positive screening serological tests may have normal biopsies. It is unclear whether these individuals have early or mild celiac disease, false positive tests or variable production of autoantibody of unclear prognostic value

  • Compliance with gluten-free diet is poor when symptoms are mild or absent and when diagnosis is made beyond childhood

Liu E, et al Clin Gastroenterol Hepatol 2003;(1):356-362


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TREATMENT Disease


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Gluten-Containing Grains to Avoid Disease

CDHNF - NASPGHAN


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Ingredients that may contain gluten Disease

  • Seasonings and spice blends or mixes

  • Modified food starch

  • Malt/malt extract/flavoring

  • Modified hop extract and yeast-malt sprout extract

  • Dextrin

  • Caramel color

CDHNF - NASPGHAN


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Other items to consider Disease

  • Lipstick/gloss/balms

  • Mouthwash/toothpaste

  • Play dough

  • Stamp and envelope glues

  • Vitamin, herbal and mineral preparations

  • Prescription or OTC medications

CDHNF - NASPGHAN


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Gluten-Free Grains and Starches Disease

*for possible cross-contamination with gluten -containing grains

CDHNF - NASPGHAN


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Can oats be taken in a gluten-free diet (GFD)? A systematic review

Results

  • 10 studies involving 165 patients

  • Only 1 patient was shown to have histological damage as a result of consuming oats

    Conclusions

  • Celiac patients can, to some advantage, include oats in a GFD

  • Recommend adding oats to their GFD when they are established on a conventional GFD

Garsed K, Scott BB. Scand J Gastroenterol 2007;42:171-78


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Safe Ingredients review

  • Starch

  • Maltodextrin

    • Made from cornstarch, potato starch, or rice starch, but not from wheat

  • Vinegar and alcohol

    • Distilled vinegar and distilled spirits are gluten-free, however avoid malt vinegar and malt beverages (e.g. beer)

CDHNF - NASPGHAN


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Health beliefs of adults with celiac disease review

  • Survey of 100 people in celiac disease support group (Buffalo, NY)

    • Number of people who agreed with following statements:

      • ”If I eat less gluten I will have less intestinal damage” (51%)

      • “I’ve lived this long eating gluten, how much will the gluten-free diet really help me now?” (33%)

      • “my doctor should be the one to tell me when I need follow-up testing” (26%)

      • “Scientist/doctors still haven’t proven that gluten really hurts them” (16%)

CDHNF - NASPGHAN


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Dietary adherence: A common Problem review

  • Only 50% of Americans with chronic illness adhere to their treatment regimen including:

    • Diet

    • Exercise

    • Medication

  • Dietary compliance can be the most difficult aspect of treatment

CDHNF - NASPGHAN


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Barriers to Compliance review

  • Time pressure – time to plan, prepare food is longer

  • Planning – work required to plan meals

  • Competing priorities – family, job, etc.

  • Assessing gluten content in foods/label reading

  • Eating out – avoidance, fear, difficult to ensure food is safe

CDHNF - NASPGHAN


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Barriers to Compliance review

  • Social events – not wanting to look/be different

  • Support of family and friends – “just a little bit – it won’t hurt you”

CDHNF - NASPGHAN


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Treatment of Celiac Disease review

Gluten-free diet

  • Compliance problems due to palatability, variations in food labeling and possible cross-contamination of other foodstuffs by gluten are common

Ludvigsson JF et al. Gastroenterology 2005;129:454-463


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Factors that Improve Adherence review

  • Knowledge about the gluten-free diet

  • Understanding the risk factors and serious complications can occur to the patient

  • Ability to break down big changes into smaller steps – ability to simplify or make behavior routine

  • Ability to reinforce positive changes internally

  • Positive coping skills

  • Ability to recognize and manage mental health issues

  • External test results are motivational, especially in asymptomatic individuals

NASPGHAN



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Dietary triggers of IBS review

  • Fermentable Oligosaccharides, Disaccharides, Monosaccharide and Polyols (FODMAP)

  • FODMAPs can include fructose and lactose, polyols (such as sorbitol) and fructo-oligosaccharides (fructans)

  • Major dietary FODMAPs include fructose and fructans; fructose are fruits, honey and high fructose corn syrup, and of fructans they are wheat and onions

Shepherd SJ, et al Clinial Gastroenterology & Hepatology 2008;6:765-771


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Lactose Intolerance & Celiac Disease: Incidence review

  • Secondary lactase deficiency is estimated to be 20% - 40%

  • Increasing lactose intolerance with delayed diagnosis

  • Increased incidence in patients with GI symptoms in celiac disease

  • Decrease calcium and vitamin D intake in lactose intolerance

CDHNF - NASPGHAN


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Causes of poor response to gluten-free diet review

*common

Peter Green, M.D.


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Resources review

Reputable websites

  • Celiac.com (www.celiac.com)

  • National Institutes of Health (www.niddk.nih.gov)

  • American Dietetic Association (www.eatright.org)

    Local Support Groups

  • Celiac.com (www.celiac.com)

    National Support Groups

  • The Gluten Intolerance Group – GIG (www.gluten.net)

  • Celiac Disease Foundation – CDF (www.celiac.org)

    Research and Information

  • Center for Celiac Research (www.celiaccenter.org)


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Resources review

  • Cookbooks

    • Hagman, Bette, “The Gluten-Free Gourmet Cooks Fast and Healthy”

    • Saros, Connie, “Wheat-free Gluten-free Cookbook for Kids and Busy Adults”

    • Books and Magazines

    • Case, Shelly, “Gluten-Free Diet: A comprehensive Resource Guide”

    • Gluten-Free living

    • Sully’s Living Without (www.livingwithout.com)

  • Product information

    • www.glutenfreemall.com

NSPGHAN


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Selected support groups and websites review

Liu E, et al Clin Gastroenterol Hepatol 2003;(1):356-362


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THANK YOU review


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Dietary Factors review

  • 33 amino acid peptide in gliadin contains critical epitopes – high in glutamine and proline

  • Resistant to digestion in lumen

  • Penetrates epithelial barrier

  • Modified by the enzyme tissue transglutaminase

    • Deaminates glutamine residues to glutamic acid

  • Resulting higher affinity binding to HLA DQ2 molecule on the surface of antigen-presenting cells

CDHNF - NASPGHAN


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Long-term follow-up of 61 celiac patients diagnosed in childhood: Evolution toward latency is possible on a normal diet

Introduction:

The question still remains as to whether the maintenance of a life-long gluten-free diet is necessary in all celiac children or whether in some of them a gluten-containing diet can be safely reintroduced

Aim:

To retrospectively analyze the clinical and biological status of adult celiac patients diagnosed in childhood, who remained on a normal diet after gluten challenge and were clinically silent

Matysiak-Budnik T, et al Gut 2007;56:1379-1386


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Long-term follow-up of 61 celiac patients diagnosed in childhood: Evolution toward latency is possible on a normal diet

(Cont)

Results:

  • 61 patients had resumed a normal diet and were asymptomatic

  • 48 showed different degrees of villous atrophy (silent CD); 13 had no detectable atrophy (latent CD) on duodenal biopsies

    Conclusion:

  • Long-term latency developed in about 20% of CD patients who remained symptom free after gluten reintroduction

  • Silent celiac – risk of osteoporosis necessitates gluten-free diet

Matysiak-Budnik T, et al Gut 2007;56:1379-1386


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Budesonide in the treatment of refractory celiac disease childhood: Evolution toward latency is possible on a normal diet

POP

  • 29 patients (72% female) received budesonide for a mean of 6.7 ± 8.5 months

    Results

  • 12 of 15 had complete response to Budesonide

    Conclusion

  • Response occurred in those who had refractory disease and in those with type II disease, irrespective of the presence of microscopic colitis (N = 7)

Brar P, et al. Am J Gastroenterol 2007;102:2265-2269


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Budesonide and concomitant medication use in relation to budesonide response

S – systemic steroids; A - azathioprine

Brar P, et al. Am J Gastroenterol 2007;102:2265-2269


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Response to hepatitis B vaccination in patients with celiac disease

  • Non-responsiveness to hepatitis B virus (HBV) vaccination is related to genetic features

  • Strong relationship between CD and these human leukocyte antigen (HLA) genotypes

  • Responsiveness to HBV vaccination was observed in 17 (68%) CD patients and all (100%) control subjects (P = 0.006)

Ahishali A, et al. Dig Dis Sci 2008;53:2156-2159


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