CC BY-NC-ND 4.0 · Endosc Int Open 2018; 06(11): E1369-E1378
DOI: 10.1055/a-0732-5060
Original article
Owner and Copyright © Georg Thieme Verlag KG 2018

Efficacy of duodenal bulb biopsy for diagnosis of celiac disease: a systematic review and meta-analysis

Thomas R. McCarty
1   Department of Internal Medicine, Yale University School of Medicine, New Haven, Connecticut, United States
,
Corey R. O’Brien
1   Department of Internal Medicine, Yale University School of Medicine, New Haven, Connecticut, United States
,
Anas Gremida
2   Division of Gastroenterology and Hepatology, University of New Mexico, Albuquerque, New Mexico, United States
,
Christina Ling
2   Division of Gastroenterology and Hepatology, University of New Mexico, Albuquerque, New Mexico, United States
,
Tarun Rustagi
2   Division of Gastroenterology and Hepatology, University of New Mexico, Albuquerque, New Mexico, United States
› Author Affiliations
Further Information

Publication History

submitted 07 May 2018

accepted after revision 23 July 2018

Publication Date:
07 November 2018 (online)

Abstract

Background and study aims Although duodenal biopsy is considered the “gold standard” for diagnosis of celiac disease, the optimal location of biopsy within the small bowel for diagnosis remains unclear. The primary aim of this study was to perform a structured systematic review and meta-analysis to evaluate the diagnostic utility of endoscopic duodenal bulb biopsy for celiac disease.

Patients and methods Searches of PubMed, EMBASE, Web of Science, and Cochrane Library databases were performed from 2000 through December 2017. Review of titles/abstracts, full review of potentially relevant studies, and data abstraction was performed. Measured outcomes of adult and pediatric patients included location of biopsy, mean number of biopsies performed, and diagnosis of celiac disease as defined by the modified Marsh-Oberhuber classification.

Results A total of 17 studies (n = 4050) were included. Seven studies evaluated adults and 11 studies assessed pediatric populations. Mean age of adults and pediatric patients was 46.70 ± 2.69 and 6.33 ± 1.26 years, respectively. Overall, sampling from the duodenal bulb demonstrated a 5 % (95 % CI 3 – 9; P < 0.001) increase in the diagnostic yield of celiac disease. When stratified by pediatric and adult populations, duodenal bulb biopsy demonstrated a 4 % (95 % CI: 1 to 9; P < 0.001) and 8 % (95 % CI: 6 to 10; P < 0.001) increase in the diagnostic yield of celiac disease. Non-celiac histologic diagnoses including Brunner gland hyperplasia and peptic duodenitis were reported more commonly in the duodenal bulb as compared to the distal duodenum with an increase in diagnostic yield of 4 % (95 % CI 3 – 5; P < 0.001) and 1 % (95 % CI 1 – 2; P < 0.001), respectively.

Conclusions Based upon our results, biopsy and histologic examination of duodenal bulb during routine upper endoscopy increases the diagnostic yield of celiac disease.

 
  • References

  • 1 Green PH, Cellier C. Celiac disease. N Engl J Med 2007; 357: 1731-1743
  • 2 Gujral N, Freeman HJ, Thomson AB. Celiac disease: prevalence, diagnosis, pathogenesis and treatment. World J Gastroenterol 2012; 18: 6036-6059
  • 3 Fasano A, Berti I, Gerarduzzi T. et al. 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: 286-292
  • 4 Biagi F, Klersy C, Balduzzi D. et al. Are we not over-estimating the prevalence of coeliac disease in the general population?. Ann Med 2010; 42: 557-561
  • 5 Murray JA, Watson T, Clearman B. et al. Effect of a gluten-free diet on gastrointestinal symptoms in celiac disease. Am J Clin Nutr 2004; 79: 669-673
  • 6 Sharaiha RZ, Lebwohl B, Reimers L. et al. Increasing incidence of enteropathy-associated T-cell lymphoma in the United States, 1973-2008. Cancer 2012; 118: 3786-3792
  • 7 Rubio-Tapia A, Hill ID, Kelly CP. et al. ACG clinical guidelines: diagnosis and management of celiac disease. Am J Gastroenterol 2013; 108: 656-676 ; quiz 77
  • 8 Cummins AG, Alexander BG, Chung A. et al. Morphometric evaluation of duodenal biopsies in celiac disease. Am J Gastroenterol 2011; 106: 145-150
  • 9 Oberhuber G, Granditsch G, Vogelsang H. The histopathology of coeliac disease: time for a standardized report scheme for pathologists. Eur J Gastroenterol Hepatol 1999; 11: 1185-1194
  • 10 Gonzalez S, Gupta A, Cheng J. et al. Prospective study of the role of duodenal bulb biopsies in the diagnosis of celiac disease. Gastrointest Endosc 2010; 72: 758-765
  • 11 Mangiavillano B, Masci E, Parma B. et al. Bulb biopsies for the diagnosis of celiac disease in pediatric patients. Gastrointest Endosc 2010; 72: 564-568
  • 12 Nenna R, Pontone S, Pontone P. et al. Duodenal bulb in celiac adults: the "whether biopsying" dilemma. J Clin Gastroenterol 2012; 46: 302-307
  • 13 Beynon R, Leeflang MM, McDonald S. et al. Search strategies to identify diagnostic accuracy studies in MEDLINE and EMBASE. Cochrane Database Syst Rev 2013; DOI: 10.1002/14651858.MR000022.pub3.
  • 14 Liberati A, Altman DG, Tetzlaff J. et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. Ann Int Med 2009; 151: W65-W94
  • 15 Howaizi M, Chahine M, Haydar F. et al. Cannabis-induced recurrent acute pancreatitis. Acta Gastroenterol Belg 2012; 75: 446-447
  • 16 Lorvellec A, Thiriet L, Andrianjafy C. et al. [Recurrent cannabis-induced acute pancreatitis]. Presse Med 2015; 44: 468-471
  • 17 Caruso R, Marafini I, Del Vecchio Blanco G. et al. Sampling of proximal and distal duodenal biopsies in the diagnosis and monitoring of celiac disease. Dig Liver Dis 2014; 46: 323-329
  • 18 Mansfield-Smith S, Savalagi V, Rao N. et al. Duodenal bulb histological analysis should be standard of care when evaluating celiac disease in children. Pediatr Dev Pathol 2014; 17: 339-343
  • 19 Levinson-Castiel R, Hartman C, Morgenstern S. et al. The role of duodenal bulb biopsy in the diagnosis of celiac disease in children. J Clin Gastroenterol 2011; 45: 26-29
  • 20 Kurien M, Evans KE, Hopper AD. et al. Duodenal bulb biopsies for diagnosing adult celiac disease: is there an optimal biopsy site?. Gastrointest Endosc 2012; 75: 1190-1196
  • 21 Tanpowpong P, Broder-Fingert S, Katz AJ. et al. Predictors of duodenal bulb biopsy performance in the evaluation of coeliac disease in children. J Clin Pathol 2012; 65: 791-794
  • 22 Sharma A, Mews C, Jevon G. et al. Duodenal bulb biopsy in children for the diagnosis of coeliac disease: experience from Perth, Australia. J Paediatr Child Health 2013; 49: 210-214
  • 23 Evans KE, Aziz I, Cross SS. et al. A prospective study of duodenal bulb biopsy in newly diagnosed and established adult celiac disease. Am J Gastroenterol 2011; 106: 1837-1842
  • 24 Bonamico M, Thanasi E, Mariani P. et al. Duodenal bulb biopsies in celiac disease: a multicenter study. J Pediatr Gastroenterol Nutr 2008; 47: 618-622
  • 25 Rashid M, MacDonald A. Importance of duodenal bulb biopsies in children for diagnosis of celiac disease in clinical practice. BMC Gastroenterol 2009; 9: 78
  • 26 Prasad KK, Thapa BR, Nain CK. et al. Assessment of the diagnostic value of duodenal bulb histology in patients with celiac disease, using multiple biopsy sites. J Clin Gastroenterol 2009; 43: 307-311
  • 27 Bonamico M, Mariani P, Thanasi E. et al. Patchy villous atrophy of the duodenum in childhood celiac disease. J Pediatr Gastroenterol Nutr 2004; 38: 204-207
  • 28 Ravelli A, Bolognini S, Gambarotti M. et al. Variability of histologic lesions in relation to biopsy site in gluten-sensitive enteropathy. Am J Gastroenterol 2005; 100: 177-185
  • 29 Stoven SA, Choung RS, Rubio-Tapia A. et al. Analysis of biopsies from duodenal bulbs of all endoscopy patients increases detection of abnormalities but has a minimal effect on diagnosis of celiac disease. Clin Gastroenterol Hepatol 2016; 14: 1582-1588
  • 30 Mooney PD, Kurien M, Evans KE. et al. Clinical and immunologic features of ultra-short celiac disease. Gastroenterology 2016; 150: 1125-1134
  • 31 Lebwohl B, Sanders DS, Green PHR. Coeliac disease. Lancet 2018; 391: 70-81
  • 32 Malekzadeh R, Sachdev A, Fahid Ali A. Coeliac disease in developing countries: Middle East, India and North Africa. Best Pract Res Clin Gastroenterol 2005; 19: 351-358
  • 33 Rubio-Tapia A, Ludvigsson JF, Brantner TL. et al. The prevalence of celiac disease in the United States. Am J Gastroenterol 2012; 107: 1538-1544 ; quiz 7, 45
  • 34 Catassi C, Fabiani E, Ratsch IM. et al. The coeliac iceberg in Italy. A multicentre antigliadin antibodies screening for coeliac disease in school-age subjects. Acta Paediatr Suppl 1996; 412: 29-35
  • 35 Bai JC, Ciacci C. World Gastroenterology Organisation Global Guidelines: Celiac Disease February 2017. J Clin Gastroenterol 2017; 51: 755-768
  • 36 Hill ID, Fasano A, Guandalini S. et al. NASPGHAN Clinical report on the diagnosis and treatment of gluten-related disorders. J Pediatr Gastroenterol Nutr 2016; 63: 156-165
  • 37 Force USPST, Bibbins-Domingo K, Grossman DC. et al. Screening for Celiac Disease: US Preventive Services Task Force Recommendation Statement. JAMA 2017; 317: 1252-1257
  • 38 Downey L, Houten R, Murch S. et al. Recognition, assessment, and management of coeliac disease: summary of updated NICE guidance. BMJ 2015; 351: h4513
  • 39 Rubin CE, Brandborg LL, Phelps PC. et al. Studies of celiac disease. I. The apparent identical and specific nature of the duodenal and proximal jejunal lesion in celiac disease and idiopathic sprue. Gastroenterology 1960; 38: 28-49
  • 40 Fry L, Seah PP, McMinn RM. et al. Lymphocytic infiltration of epithelium in diagnosis of gluten-sensitive enteropathy. Br Med J 1972; 3: 371-374
  • 41 Marsh MN. Gluten, major histocompatibility complex, and the small intestine. A molecular and immunobiologic approach to the spectrum of gluten sensitivity ('celiac sprue'). Gastroenterology 1992; 102: 330-354
  • 42 Marsh MN, Crowe PT. Morphology of the mucosal lesion in gluten sensitivity. Baillieres Clin Gastroenterol 1995; 9: 273-293
  • 43 Ferguson A, Arranz E, O'Mahony S. Clinical and pathological spectrum of coeliac disease – active, silent, latent, potential. Gut 1993; 34: 150-151
  • 44 Troncone R, Greco L, Mayer M. et al. Latent and potential coeliac disease. Acta Paediatr Suppl 1996; 412: 10-14
  • 45 Shiner M. Small intestinal biopsy: diagnostic and research value. Proc R Soc Med 1959; 52: 10-14
  • 46 Hopper AD, Cross SS, Sanders DS. Patchy villous atrophy in adult patients with suspected gluten-sensitive enteropathy: is a multiple duodenal biopsy strategy appropriate?. Endoscopy 2008; 40: 219-224
  • 47 Vogelsang H, Hanel S, Steiner B. et al. Diagnostic duodenal bulb biopsy in celiac disease. Endoscopy 2001; 33: 336-340
  • 48 Ravelli A, Villanacci V. Tricks of the trade: How to avoid histological pitfalls in celiac disease. Pathol Res Pract 2012; 208: 197-202
  • 49 Institute AGA. AGA Institute Medical Position Statement on the Diagnosis and Management of Celiac Disease. Gastroenterology 2006; 131: 1977-1980
  • 50 Hill ID, Dirks MH, Liptak GS. 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: 1-19
  • 51 Trier JS. Diagnostic value of peroral biopsy of the proximal small intestine. N Engl J Med 1971; 285: 1470-1473
  • 52 Corazza GR, Villanacci V, Zambelli C. et al. Comparison of the interobserver reproducibility with different histologic criteria used in celiac disease. Clin Gastroenterol Hepatol 2007; 5: 838-843
  • 53 Yantiss RK, Odze RD. Optimal approach to obtaining mucosal biopsies for assessment of inflammatory disorders of the gastrointestinal tract. Am J Gastroenterol 2009; 104: 774-783