OHTAC Recommendation
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1 OHTAC Recommendation Clinical Utility of Serologic Testing for Celiac Disease in Ontario Presented to the Ontario Health Technology Advisory Committee in April and October, 2010 December 2010
2 Background Celiac Disease Celiac disease is an autoimmune disease characterized by a chronic inflammatory state of the proximal small bowel mucosa, accompanied by structural and functional changes. (1) This results in impaired digestion and absorption of nutrients. (2) The immunological response is triggered by ingestion of gluten, a protein that is present in wheat, rye, and barley. (1) Treatment consists of strict lifelong adherence to a gluten-free diet. (1) Symptoms improve with a gluten-free diet (GFD) but recur when gluten-containing foods are restarted. (2) Celiac disease can have different presentations such as classic, in which patients present with gastrointestinal symptoms and the classic features of intestinal malabsorption, or atypical, in which patients present with iron deficiency anemia for instance, but little or no gastrointestinal symptoms. (3) Patients with silent disease do not present with clear gastrointestinal or atypical symptoms. (3) Individuals with some autoimmune disorders may have an increased risk of celiac disease as explained by shared HLA DQ2/DQ8 susceptibility genes, which is the case with type 1 diabetes and autoimmune thyroid disease. (2) First degree relatives of individuals with celiac disease may also have an increased risk of celiac disease. (2) Dermatitis herpetiformis is a skin manifestation of celiac disease (4) characterized by a blistering rash. (5) Patients with dermatitis herpetiformis may have concomitant small bowel mucosa abnormalities characteristic of celiac disease. (4) Published systematic literature reviews reported that the prevalence of celiac disease in the general population varied between 0.14% and 1.87% (median across studies: 0.47%, interquartile range: 0.25%, 0.71%) based on studies that used small bowel biopsy to confirm the diagnosis. (3;6) In studies with individuals with type 1 diabetes the prevalence ranged from 1 to 11%, it ranged from 2.9% to 3.3% in individuals with autoimmune thyroiditis, and 2 to 20% in first degree relatives of patients with celiac disease. (3;6) It is estimated that approximately 1.7% to 3.0% of patients with celiac disease have immunoglobulin A (IgA) deficiency. (2) Serologic Testing for Celiac Disease There are a number of serologic tests for the diagnosis of celiac disease including anti-gliadin antibody (AGA), anti-tissue transglutaminase antibody (ttg), anti-endomysial antibody (EMA), and antideamidated gliadin peptides antibody (DGP). For each serologic test, both immunoglobulin A (IgA) or IgG can be measured, however, IgA measurement is the standard antibody measured in celiac disease. (2) Celiac Disease Diagnosis According to celiac disease guidelines, the diagnosis of celiac disease is established by small bowel biopsy. (4;7;8) Serologic tests are used to initially detect and support the presence of celiac disease. (2;4;7;8) A small intestinal biopsy is indicated in individuals with a positive serologic test. (9) In some cases, endoscopy and small bowel biopsy may be necessary even with a negative serologic test depending on the clinical presentation (1;10) since this could be due to either a false negative or IgA deficiency, (9) seronegative celiac disease. (4) 2
3 OHTAC Findings The research questions of the Medical Advisory Secretariat (MAS) evaluation were: 1. What is the sensitivity and specificity of serologic tests in the diagnosis of celiac disease? 2. What is the clinical validity of serologic tests in the diagnosis of celiac disease? The clinical validity was defined as the ability of the test to change diagnosis. 3. What is the clinical utility of serologic tests in the diagnosis of celiac disease? The clinical utility was defined as the impact of the test on decision making. 4. What is the budget impact of serologic tests in the diagnosis of celiac disease? 5. What is the cost-effectiveness of serologic tests in the diagnosis of celiac disease? Findings Five systematic reviews of studies that evaluated the diagnostic accuracy of serologic tests for celiac disease were identified through the MAS literature search. Seventeen individual studies identified either through MAS systematic literature search or through manual searching of the reference list of systematic reviews were eligible for this evaluation. Studies evaluated either individual serologic tests or a combination of serologic tests. The results of the studies identified were pooled using a bivariate, binomial generalized linear mixed model. Statistical significance was defined by p-values less than 0.05, where false discovery rate adjustments were made for multiple hypothesis testing. Sensitivity The pooled analysis performed by MAS showed that IgA ttg has a sensitivity of 92.1% [95% confidence interval (CI): 88.0%, 96.3%], compared to 89.2% (CI: 83.3%, 95.1%; p=0.12) for IgA DGP, 85.1% (CI: 79.5%, 94.4%; p=0.07) for IgA EMA, 74.9% (CI: 63.6%, 86.2%; p=0.003) for IgA AGA. Among the IgG-based tests, the results suggest that IgG DGP has a sensitivity of 88.4% (95% CI: 82.1, 94.6), 44.7% (CI: 30.3%, 59.2%) for ttg, and 69.1% (CI: 56.0%, 82.2%) for AGA. The difference was significant when IgG DGP was compared to IgG ttg but not to IgG AGA. Combining different serologic tests yielded a slightly higher sensitivity a compared to IgA ttg (3.0%; p.0381). Different combinations of serologic celiac disease tests were used in the studies identified, the most common was a combination of IgA and IgG DGP tests ± IgA ttg. The presence of IgA deficiency may affect the sensitivity of the IgA-based serologic tests since total/severe IgA deficient subjects may not produce detectable levels of IgA antibodies. The prevalence of total or severe IgA deficiency was low in the studies identified, ranging from 0 to 1.7%, in studies in which IgA deficiency was not used as a referral indication for a celiac disease serologic test. The results of IgG-based serologic tests were positive in all patients with IgA deficiency in which celiac disease was confirmed by small bowel biopsy. Specificity A high specificity was observed across the different serologic tests, pooled estimates ranged from 90.1% to 98.7% depending on the test. a Defining a positive serology if at least one of the serologic tests used in the combination was positive. 3
4 Effects of a Gluten-Free Diet (GFD) in Patients Diagnosed with Celiac Disease Six studies identied through the systematic literature search evaluated the effects of GFD on clinical, histological, or serological improvement in patients diagnosed with celiac disease. Improvement was observed in 51% to 95% of the patients diagnosed with celiac disease. The most common symptoms presented by these patients prior to the diagnosis were gastrointestinal symptoms such as chronic diarrhea and abdominal pain, anemia, weight loss, and failure to thrive in pediatric patients. Likelihood ratios According to the likelihood ratio estimates, both IgA ttg and serologic test combinations b were considered very useful tests, generating large and often conclusive changes from pre- to post test probability (positive LR > 10 and negative LR < 0.1). Moderately useful tests included IgA EMA, IgA DGP, IgG DGP, generating moderate shifts from pre- to post-test probability (positive LR between 5 and 10 and negative LR between 0.1 and 0.2). Somewhat useful tests: IgA AGA, IgG AGA, generating small but sometimes important changes from pre- to post-test probability (positive LR between 2 and 5 and negative LR between 0.2 and 0.5) Not Useful: IgG ttg, altering pre- to post-test probability to a small and rarely important degree (positive LR between 1 and 2 and negative LR between 0.5 and 1). Clinical Validity and Clinical Utility of Serologic Celiac DiseaseTests The clinical validity of serologic tests in the diagnosis of celiac disease was considered high in subjects with symptoms consistent with the disease. This is due to the high accuracy of some of the serologic tests and the fact that serologic tests detect possible celiac disease cases and avoid unnecessary small bowel biopsy if the test result is negative, unless an endoscopy/small bowel biopsy is necessary due to clinical presentation. In addition, serologic celiac disease tests support the results of small bowel biopsy. The clinical utility of serologic tests in the diagnosis of celiac disease was also considered high in subjects with symptoms consistent with the disease given the considerations above and since diagnosis of celiac disease leads to treatment with a gluten-free diet. Economic Analysis A decision analysis was constructed to compare costs and outcomes between the tests based on the sensitivity, specificity and prevalence summary estimates from the MAS Evidence-Based Analysis. A budget impact was then calculated by multiplying the expected costs and volumes in Ontario. The outcome of the analysis was expected costs and false negatives (FN). Costs were reported in 2010 CAD$. All analyses were performed using TreeAge Pro Suite Four strategies made up the efficiency frontier; IgG ttg, IgA ttg, EMA and biopsy. All other strategies were dominated. IgG ttg was the least costly and least effective strategy ($178.95, FN avoided=0). Biopsy was the most costly and most effective strategy ($396.60, FN avoided =0.1553). The cost per FN avoided were $293, $369, $1,401 for EMA, IgA ttg and biopsy respectively. One-way sensitivity analyses did not change the ranking of strategies. b Interpreting a positive serology if at least one of the serologic tests in the combination had a positive result. 4
5 All testing strategies with biopsy are cheaper than biopsy alone however they also result in more FNs. The most cost-effective strategy will depend on the decision makers willingness to pay. Findings suggest that IgA ttg was the most cost-effective and feasible strategy based on its Incremental Cost-Effectiveness Ratio (ICER) and convenience to conduct the test. The potential impact of IgA ttg test in the province of Ontario would be $10.4M, $11.0M and $11.7M, respectively, in the following three years based on past volumes and trends in the province and basecase expected costs. A combination of serologic tests is the commonly used strategy in the province of Ontario and, therefore, the impact to the system would be $13.6M, $14.5M and $15.3M, respectively, in the next three years based on past volumes and trends in the province and basecase expected costs. Grading of Evidence The quality of the evidence for each of the serologic celiac tests was evaluated using the GRADE Working Group criteria. (11;12) Overall, the quality of the evidence ranged from moderate to very low depending on the serologic test. The quality was considered moderate for IgA ttg and EMA, low for IgA DGP and serologic test combinations, and very low for IgA AGA. Reasons to downgrade the quality of the evidence included the lack of clinical outcomes reporting in the studies, inconsistencies among study results, and imprecise pooled estimates for some of the serologic tests. Professional Panel and Citizen s Reference Panel on Serologic Testing for Celiac Disease As a prior recommendation from OHTAC, a Professional Panel, comprised of gastroenterologists, family physicians, laboratory personnel, nurses, and ethicists was consulted in order to advise OHTAC regarding the criteria to guide the use of serologic tests in the diagnosis of celiac disease. Similarly, the Citizens Reference Panel on Health Technology was also consulted, as part of the formal public engagement process, in order to assist OHTAC with the present recommendations. The Professional Panel provided advice concerning the clinical utility and issues regarding access to serologic tests for celiac disease. This input was considered by OHTAC in making its final recommendations. Other possible non-gastrointestinal indications and testing in asymptomatic high risk individuals were raised by the Panel, for which the Medical Advisory Secretariat will undertake an evidence-based analysis. The Citizen s Panel aided OHTAC in assessing the societal and ethical determinants of serologic testing for celiac disease. Discussion The results of the pooled analysis suggest that IgA ttg is the most accurate serologic test for celiac disease. The difference in sensitivity was not statistically significant when compared to the IgA DGP and EMA tests. However, the quality of the evidence (GRADE) for the IgA DGP was considered low due to inconsistency in results, compared to moderate with IgA ttg. The IgA EMA test (moderate quality evidence), not being automated, is more time-consuming and operator-dependent than the other tests, demanding more experience of the operator. Additionally, while IgA ttg was considered a very useful test according to the likelihood ratios, IgA DGP and EMA were considered moderately useful. The 5
6 sensitivity of IgA AGA is statistically significantly lower than other IgA-based tests. Combinations c of serologic tests have a slightly higher sensitivity compared to individual IgA-based serologic celiac disease tests however its specificity is slightly lower (not statistically significant). The results of combinations of serologic tests should be interpreted with caution since the results may not be generalizable if different combinations of serologic tests are used in clinical practice. Conclusions The clinical validity and clinical utility of serologic tests for celiac disease was considered high in subjects with symptoms consistent with the disease as they aid in the diagnosis of celiac disease and some tests present a high accuracy, and a celiac disease diagnosis leads to treatment with a gluten-free diet. The study findings suggest that IgA ttg is the most accurate and the most cost-effective test. IGA AGA has a lower accuracy compared to other IgA-based serologic celiac disease tests. Serologic test combinations appear to be more costly with little gain in accuracy. IgA deficiency seems to be uncommon in patients diagnosed with celiac disease. The generalizability of study results is contingent on performing both the serologic test and biopsy in subjects on a gluten-containing diet, since the avoidance of gluten may affect test results. c Refers to the assumption that a positive serology was defined by a positive result in at least one of the serologic tests included in the combination. 6
7 Decision Determinants OHTAC has developed a decision-making framework that consists of seven guiding principles for decision making and a decision-making tool, called the Decision Determinants (DD) tool. The evaluation of the four explicit main criteria (overall clinical benefit, value for money, feasibility of adoption into health system, and consistency with expected societal & ethical values) are reported in using 1 of 4 symbols. For more information on the Decision-Making Framework and the meaning of the symbols below, please refer to the Decision Determinants Guidance Document or visit: Overall clinical benefit Serologic testing for celiac disease in subjects with suspicion of celiac disease*, unexplained iron deficiency anemia unresponsive to iron supplementation, and dermatitis herpetiformis Consistency with expected societal and ethical values Value for money Feasibility of adoption into the health system * Adults: chronic diarrhea especially in the presence of weight loss, abdominal pain, and/or unexplained iron-deficiency anemia unresponsive to iron supplementation. Pediatrics: Chronic diarrhea especially in the presence of failure to thrive or weight loss; severe constipation especially with poor weight gain. 7
8 OHTAC Recommendations The following recommendations are being made in regards to gastrointestinal indications, unexplained anemia unresponsive to iron supplementation, and dermatitis herpetiformis. OHTAC will make recommendations regarding IgA ttg testing for possible non-gastrointestinal indications and for asymptomatic high risk individuals once the evidence-based analysis for these indications is provided for its consideration. 1. Based on moderate quality evidence for IgA ttg, OHTAC supports the use of this serologic test in the diagnosis of celiac disease in subjects with suspicion of celiac disease (see * below), 2. Patients with a negative IgA ttg serologic test with strong suspicion of celiac disease (see * below) with or without IgA deficiency should be referred to a gastroenterologist for consideration of a small bowel biopsy. 3. Individuals with type 1 diabetes mellitus, autoimmune thyroid disease, and first degree relatives of individuals with celiac disease are reported to be at a higher risk of developing celiac disease and there should be a heightened awareness in testing for celiac disease if they meet the criteria listed at * below. 4. In people with a positive serologic test for celiac disease it is recommended that a confirmatory small bowel biopsy be performed. 5. Repeat serologic testing for patients diagnosed with celiac disease is reasonable for those patients who remain symptomatic despite strict adherence to a gluten-free diet. In this case, serologic testing for celiac disease should not be repeated more that once a year for each patient. * In Adults: chronic diarrhea especially in the presence of weight loss, abdominal pain, and/or unexplained iron-deficiency anemia unresponsive to iron supplementation. In Pediatrics: Chronic diarrhea especially in the presence of failure to thrive or weight loss; severe constipation especially with poor weight gain. In Adults and Pediatrics: Unexplained iron deficiency anemia unresponsive to iron supplementation, or subjects with dermatitis herpetiformis. IgA ttg refers to the immunoglobulin A (IgA) anti-tissue transglutaminase antibody serologic test. 8
9 References (1) Green PH, Cellier C. Celiac disease. N Engl J Med 2007; 357(17): (2) Rostom A, Murray JA, Kagnoff MF. American Gastroenterological Association (AGA) Institute technical review on the diagnosis and management of celiac disease. Gastroenterology 2006; 131(6): (3) Rostom, A., Dube, C., Cranney, A., Saloojee, N., Sy, R., and Garritty, C. Celiac disease [Internet]. Rockville, MD: Agency for Healthcare Research and Quality [cited: 2010 Mar 3]. 183 p. Available from: (4) Hill ID, Dirks MH, Liptak GS, Colletti RB, Fasano A, Guandalini S et al. Guideline for the diagnosis and treatment of celiac disease in children: recommendations of the North American Society for Pediatric Gastroenterology, Hepatology and Nutrition. J Pediatr Gastroenterol Nutr 2005; 40(1):1-19. (5) Dickey W. Joint BAPEN and British Society of Gastroenterology Symposium on 'Coeliac disease: basics and controversies'. Coeliac disease in the twenty-first century. Proc Nutr Soc 2009; 68(3): (6) National Institute for Health and Clinical Excellence. Coeliac disease: recognition and assessment of coeliac disease [Internet]. London: National Institute for Health and Clinical Excellence [cited: 2010 Mar 4]. 86 p. Clinical Practice Guideline 86. Available from: (7) AGA Institute. AGA Institute Medical Position Statement on the Diagnosis and Management of Celiac Disease. Gastroenterology 2006; 131(6): (8) Revised criteria for diagnosis of coeliac disease. Report of Working Group of European Society of Paediatric Gastroenterology and Nutrition. Arch Dis Child 1990; 65(8): (9) NIH Consensus Development Conference on Celiac Disease. NIH Consensus & State-of-the- Science Statements 2004; 21(1):1-23. (10) Anderson RP. Coeliac disease: current approach and future prospects. Intern Med J 2008; 38(10): (11) Atkins D, Best D, Briss PA, Eccles M, Falck-Ytter Y, Flottorp S et al. Grading quality of evidence and strength of recommendations. BMJ 2004; 19;328(7454):1490. (12) Schunemann HJ, Oxman AD, Brozek J, Glasziou P, Jaeschke R, Vist GE et al. Grading quality of evidence and strength of recommendations for diagnostic tests and strategies. BMJ 2008; 336(7653):
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