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Intraepithelial Lymphocytes in the Gastrointestinal Tract: to Celiac Disease and Beyond

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6/4/2019 Disclosures Intraepithelial Lymphocytes in the Gastrointestinal Tract: • BHB Therapeutics (spouse is co‐founder) To Celiac Disease and Beyond Soo‐Jin Cho, MD, PhD Current Issues in Anatomic Pathology May 25, 2019 Outline Did you know… • Celiac disease and lymphocytosis of the small bowel • “Sprue” is an Anglicized form of the • Clinical features Dutch word “sprouw,” a term applied • Histopathology in 1669 to a chronic diarrheal disease • Differential diagnosis of unknown etiology accompanied by • Intraepithelial lymphocytes elsewhere in the GI tract aphthous ulcers that was prevalent in • Esophagus Belgium • Stomach • Colon • Other conditions with GI tract lymphocytosis • Drugs (esp. immune checkpoint inhibitors) www.TheAwkwardYeti.com 1 6/4/2019 Celiac disease and other gluten‐related disorders Celiac disease • Celiac disease (CD) • Virtually unknown condition in mid‐20th century • Non‐IgE immune‐mediated • Seroprevalence currently ~1% in European and US populations • Triggered by dietary gluten ingestion • But majority of these individuals have not been diagnosed with celiac disease • In genetically susceptible individuals • Early diagnosis is challenging in children and adults • Non‐celiac gluten sensitivity (NCGS) • Presentation of diagnosed CD has been changing, with shift toward • Patients develop intestinal and extraintestinal symptoms after gluten exposure older individuals with milder disease • Do NOT meet criteria for CD or WA • Increased awareness • Wheat allergy (WA) • Better diagnostics • Hypersensitivity reaction to wheat proteins mediated via mast cell activation and • Earlier detection through serologic testing immune mechanisms that are both IgE‐mediated and non‐IgE mediated • Environmental factors (e.g., increased wheat consumption) • Affects 0.5‐4% of the population Celiac disease: Definition and diagnosis Celiac disease: Clinical features in adults • Immune‐mediated systemic disorder • Increase in median age at diagnosis to 3rd‐4th decades • Elicited by gluten and related prolamins (plant storage proteins) • Female : Male = 3:1 • Occurs in genetically susceptible individuals • Females diagnosed at a younger age • Females present more frequently with constipation, bloating, and iron deficiency anemia • Females (and elderly) tend to have more associated autoimmune conditions • ~40% of patients at diagnosis are overweight/obese • Characterized by: • CLINICAL: Variable combination of gluten‐dependent clinical manifestations • Incidence of CD diagnosed in those >65 years has been increasing • SEROLOGIES: CD‐specific antibodies • Elderly men > women • Most common symptom = anemia • GENETICS: HLA‐DQ2 and HLA‐DQ8 haplotypes • Micronutrient deficiencies may be only presenting sign • HISTOPATHOLOGY: Enteropathy • GI symptoms less prevalent and, if present, tend to be mild 2 6/4/2019 Celiac disease: Conditions with increased Celiac disease: Clinical features prevalence of CD in childhood Adults Children • • >50% w/ GI symptoms and weight loss • “Classic” – malabsorption, diarrhea, Type I diabetes mellitus at presentation wasted buttocks • Autoimmune thyroiditis • Diarrhea most common • Vomiting and abdominal distension – esp. children <1 yr of age • • Down syndrome Bloating • Failure to thrive • Turner syndrome • Aphthous stomatitis • Iron‐resistant anemia (usually older • Alternating bowel habits children) • Williams syndrome • Constipation • Short stature (usually older children) • • GERD • Pubertal delay Selective IgA deficiency • Persistent vomiting • Personality problems • Juvenile chronic arthritis • Dermatitis herpetiformis • Chronic abdominal pain • Autoimmune liver disease • Dental enamel hyperplasia • Epilepsy with cerebellar calcification Causes of protracted diarrhea in infants Celiac disease: Serologies Normal villus architecture Villus atrophy • Transport defects • Microvillus inclusion Test Sensitivity (%) Specificity (%) • Chloride‐bicarbonate exchanger (chloride‐losing diarrhea) disease Anti‐gliadin antibody, IgA 80‐90 85‐90 • Sodium‐hydrogen exchanger (congenital sodium diarrhea) • Tufting enteropathy Anti‐gliadin antibody, IgG 75‐85 75‐98 • Ileal bile acid receptor defect • Autoimmune enteropathy • Sodium‐glucose cotransporter (glucose‐galactose • IPEX syndrome Anti‐endomysial antibody, IgA 85‐98 95‐97 malabsorption) • Celiac disease Tissue transglutaminase (tTG) antibody, IgA 90‐98 95‐97 • Micronutrient deficiency • Infectious and post‐ Deamidated anti‐gliadin peptide (DGP) antibody, IgA 80‐95 86‐93 • Acrodermatitis enteropathica (zinc deficiency) infectious enteropathy DGP antibody, IgG 80‐98 86‐97 • Enzyme deficiency • Allergic enteropathy • Enterokinase deficiency • Idiopathic • Congenital short bowel • Serologic tests need to be performed in patients when they are not on gluten restriction • Enteroendocrine cell dysgenesis/enteric • Sensitivities for all markers decrease among patients with no/mild symptoms anendocrinosis • None are entirely specific for CD and can be spuriously elevated in other immune‐mediated disorders 3 6/4/2019 Celiac disease: Genetics Celiac disease: Histopathology • HLA‐DQ2 and HLA‐DQ8 • Intraepithelial lymphocytosis (constant feature) • Present in >95% of CD patients • Variable villus atrophy with crypt hyperplasia • Present in 30‐40% of population • Lymphoplasmacytic inflammation of lamina propria • Granulocytic infiltrates (neutrophils and eosinophils); HIGH NEGATIVE PREDICTIVE VALUE: neutrophilic/eosinophilic cryptitis not prominent Lack of these permissive haplotypes essentially excludes CD • Increased crypt apoptosis • Reactive epithelial changes • Associated gastrointestinal lymphocytosis Celiac disease: Biopsies ‐ how many and where? Celiac disease: The problem with the bulb… • Most studies recommend at least 4 samples to exclude CD • Can be difficult to interpret biopsy • At least one from duodenal bulb recommended, with submission in • Brunner gland hyperplasia different containers • Villi normally broad and short overlying Brunner glands • Peptic injury common (up to 80%) • 10% of patients with CD have involvement of bulb only • Can show associated lymphocytosis and villus atrophy • “Ultra short celiac disease” • Particularly children • Heterotopias (usually gastric) • 10% of patients with CD have normal bulb and diagnostic changes more • Can have lymphoid aggregates with lymphocytosis overlying aggregates distally 4 6/4/2019 Celiac disease: Histopathologic classification Celiac disease: Our practice schemes • Counting of intraepithelial lymphocytes is performed on H&E • IHC for CD3 NOT performed Marsh‐Oberhuber Corazza‐Villanacci Ensari • Often provide a range Histologic features (1999) (2005) (2010) • Descriptive diagnosis given with differential diagnosis in comment IEL Villi (V) Crypts (C) V:C ratio • Marsh (or other) classification not performed unless specifically requested • Canned comments available for use/modification: Increased Normal Normal Normal Type 1 Grade A Type 1 Increased Normal Hyperplastic <3 Type 2 (rare) Grade A Type 1 1. Focal mild intraepithelial lymphocytosis with normal villus architecture Increased Mild atrophy Hyperplastic <3 Type 3a Grade B1 Type 2 (focally >30 IEL / 100 epithelial cells) Increased Marked atrophy Hyperplastic <1 Type 3b Grade B1 Type 2 2. Intraepithelial lymphocytosis with normal villus architecture (>30 IEL / 100 Increased Flat Hyperplastic <1 Type 3c Grade B2 Type 3 epithelial cells) Normal Flat Hyperplastic <1 Type 4 (atrophic) [Deleted] [Deleted] 3. Intraepithelial lymphocytosis with villus atrophy DDx of lymphocytosis with normal villus Case 1 architecture • Gluten‐related disorders (celiac • Immune dysregulation (e.g., • disease, non‐celiac gluten sensitivity, Hashimoto thyroiditis, rheumatoid 44‐year‐old woman with history of heavy alcohol use who presents wheat allergy) arthritis, SLE, etc.) with an 8‐month history of intermittent watery diarrhea and • Dermatitis herpetiformis • Immune deficiency (e.g., IgA unintentional weight loss of 17 pounds over the past year. • First‐degree relatives deficiency, CVID) • Partially treated celiac disease • Inflammatory bowel disease • Non‐gluten food hypersensitivity (e.g., cereals, cow’s milk, soy • Lymphocytic and collagenous colitis • Endoscopy normal products, fish, rice, chicken/egg) • Graft‐versus‐host disease • Infections (e.g., Giardia, • Pre‐infiltrative intestinal T‐cell Cryptosporidia, H. pylori, tropical lymphoma sprue) • Bacterial overgrowth • Idiopathic (including irritable bowel • Drugs (e.g., NSAIDs) syndrome) 5 6/4/2019 Duodenum Duodenum Duodenal lymphocytosis canned comment (2) Case 1: Follow‐up • Intraepithelial lymphocytosis with normal villus architecture (>30 • Stool Cx: No Salmonella, Shigella, or Campylobacter isolated; Normal IEL) enteric gram negative flora absent • The duodenal biopsy shows normal villus architecture and increase in • Stool O&P: Numerous Blastocystis hominis; no cryptosporidium or intraepithelial lymphocytes (40‐50 IELs per 100 crypt epithelial cells). The cyclospora; poorly preserved sample changes may represent symptomatic, latent or treated celiac disease. Correlation with clinical and serologic findings is necessary to confirm the • Stool Giardia Ag: Negative diagnosis of celiac disease. Increased intraepithelial lymphocytes with normal villous architecture can also be seen with dermatitis herpetiformis • TTG < 15 (2014) Repeat TTG post‐endoscopy < 10 (2019) and in first‐degree relatives of patients with celiac disease. Other reported associations include systemic autoimmune disorders, NSAIDs, Crohn disease,
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