#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Pattern-based approach to duodenitis and duodenopathy


Authors: Ondřej Daum 1,2;  Magdaléna Daumová 1,2;  Marián Švajdler 1,2
Authors‘ workplace: Šiklův ústav patologie LF UK a FN Plzeň 1;  Bioptická laboratoř s. r. o., Plzeň 2
Published in: Čes.-slov. Patol., 58, 2022, No. 2, p. 88-99
Category: Reviews Article

Overview

Duodenum is currently the most popular site to obtain samples of intestinal mucosa for recognition of a disorder leading to malabsorption. Although there are significant overlaps between histological findings described in various non-neoplastic diseases of the duodenum, recognition of one of the six basic morphologic patterns, namely coeliac disease-like pattern, active chronic duodenitis, acute GvHD-like pattern, enteritis with predominant eosinophilic infiltration, enteritis with predominant infiltration by macrophages, and non-inflammatory enteropathy, usually allows diagnostic separation, especially if subtle histological details, clinical setting and serological investigation are taken into account.

Keywords:

endoscopy – Biopsy – duodenum – pattern – duodenitis – duodenopathy


Sources

1. Korn ER, Foroozan P. Endoscopic biopsies of normal duodenal mucosa. Gastrointest Endosc 1974; 21(2): 51-54.

2. Kreuning J, Bosman FT, Kuiper G, Wal AM, Lindeman J. Gastric and duodenal mucosa in ‘healthy’ individuals. An endoscopic and histopathological study of 50 volunteers. J Clin Pathol 1978; 31(1): 69-77.

3. Brown I, Bettington M, Rosty C. The role of histopathology in the diagnosis and management of coeliac disease and other malabsorptive conditions. Histopathology 2021; 78(1): 88-105.

4. Hayat M, Cairns A, Dixon MF, O’Mahony S. Quantitation of intraepithelial lymphocytes in human duodenum: what is normal? J Clin Pathol 2002; 55(5): 393-394.

5. Mahadeva S, Wyatt JI, Howdle PD. Is a raised intraepithelial lymphocyte count with normal duodenal villous architecture clinically relevant? J Clin Pathol 2002; 55(6): 424-428.

6. Biagi F, Luinetti O, Campanella J, et al. Intraepithelial lymphocytes in the villous tip: do they indicate potential coeliac disease? J Clin Pathol 2004; 57(8): 835-839.

7. Veress B, Franzen L, Bodin L, Borch K. Duodenal intraepithelial lymphocyte-count revisited. Scand J Gastroenterol 2004; 39(2): 138-144.

8. Pellegrino S, Villanacci V, Sansotta N, et al. Redefining the intraepithelial lymphocytes threshold to diagnose gluten sensitivity in patients with architecturally normal duodenal histology. Aliment Pharmacol Ther 2011; 33(6): 697-706.

9. Rostami K, Marsh MN, Johnson MW, et al. ROC-king onwards: intraepithelial lymphocyte counts, distribution & role in coeliac disease mucosal interpretation. Gut 2017; 66(12): 2080-2086.

10. Goldstein NS, Underhill J. Morphologic features suggestive of gluten sensitivity in architecturally normal duodenal biopsy specimens. Am J Clin Pathol 2001; 116(1): 63-71.

11. Ensari A. Gluten-sensitive enteropathy (celiac disease): controversies in diagnosis and classification. Arch Pathol Lab Med 2010; 134(6): 826-836.

12. Owen DR, Owen DA. Celiac disease and other causes of duodenitis. Arch Pathol Lab Med 2018; 142(1): 35-43.

13. Ferguson A, Murray D. Quantitation of intraepithelial lymphocytes in human jejunum. Gut 1971; 12(12): 988-994.

14. Ferguson A. Intraepithelial lymphocytes of the small intestine. Gut 1977; 18(11): 921-937.

15. 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(1): 330-354.

16. Crowe PT, Marsh MN. Morphometric analysis of intestinal mucosa. VI--Principles in enumerating intra-epithelial lymphocytes. Virchows Arch 1994; 424(3): 301-306.

17. Jarvinen TT, Collin P, Rasmussen M, et al. Villous tip intraepithelial lymphocytes as markers of early-stage coeliac disease. Scand J Gastroenterol 2004; 39(5): 428-433.

18. Karabork BA, Yuksel S, Savas B, Ensari A. IEL counts and distribution in normal duodenum, non-GSE IELosis and GSE: Do we need a cut-off? Virchows Arch 2012; 461(Suppl. 1): S9.

19. Yantiss RK, Odze RD. Optimal approach to obtaining mucosal biopsies for assessment of inflammatory disorders of the gastrointestinal tract. Am J Gastroenterol 2009; 104(3): 774- 783.

20. Sharaf RN, Shergill AK, Odze RD, et al. Endoscopic mucosal tissue sampling. Gastrointest Endosc 2013; 78(2): 216-224.

21. Rubio-Tapia A, Hill ID, Kelly CP, Calderwood AH, Murray JA. ACG clinical guidelines: diagnosis and management of celiac disease. Am J Gastroenterol 2013; 108(5): 656-676.

22. Ludvigsson JF, Bai JC, Biagi F, et al. Diagnosis and management of adult coeliac disease: guidelines from the British Society of Gastroenterology. Gut 2014; 63(8): 1210-1228.

23. Allen JI, Katzka D, Robert M, Leontiadis GI. American Gastroenterological Association Institute technical review on the role of upper gastrointestinal biopsy to evaluate dyspepsia in the adult patient in the absence of visible mucosal lesions. Gastroenterology 2015; 149(4): 1088-1118.

24. Robert ME, Crowe SE, Burgart L, et al. Statement on best practices in the use of pathology as a diagnostic tool for celiac disease: a guide for clinicians and pathologists. Am J Surg Pathol 2018; 42(9): e44-e58.

25. Bonamico M, Mariani P, Thanasi E, et al. Patchy villous atrophy of the duodenum in childhood celiac disease. J Pediatr Gastroenterol Nutr 2004; 38(2): 204-207.

26. Drut R, Rua EC. Histopathologic diagnosis of celiac disease in children without clinical evidence of malabsorption. Int J Surg Pathol 2007; 15(4): 354-357.

27. Bonamico M, Thanasi E, Mariani P, et al. Duodenal bulb biopsies in celiac disease: a multicenter study. J Pediatr Gastroenterol Nutr 2008; 47(5): 618-622.

28. 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(4): 758-765.

29. 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(10): 1837- 1742.

30. 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(6): 1190-1196.

31. Mooney PD, Kurien M, Evans KE, et al. Clinical and immunologic features of ultra-short celiac disease. Gastroenterology 2016; 150(5): 1125-1134.

32. Taavela J, Popp A, Korponay-Szabo IR, et al. A prospective study on the usefulness of duodenal bulb biopsies in celiac disease diagnosis in children: urging caution. Am J Gastroenterol 2016; 111(1): 124-133.

33. McCarty TR, O’Brien CR, Gremida A, Ling C, Rustagi T. Efficacy of duodenal bulb biopsy for diagnosis of celiac disease: a systematic review and meta-analysis. Endosc Int Open 2018; 6(11): e1369-e1378.

34. 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(10): 1185-1194.

35. 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(7): 838-843.

36. Ozakinci H, Kirmizi A, Savas B, et al. Classification chaos in coeliac disease: Does it really matter? Pathol Res Pract 2016; 212(12): 1174- 1178.

37. Daum O. Patologie GIT. In: Zámečník J, ed. Patologie (1 ed). Prague: LD, s.r.o. - PRAGER PUBLISHING; 2019: 461-526.

38. Švajdler Jr. M, Bohuš P, Rychlý B. Histopatologická diagnóza a diferenciálna diagnóza céliakie: prehlad pre gastroenterológov. Čes a Slov Gastroent a Hepatol 2010; 64(3): 24-30.

39. Moran CJ, Kolman OK, Russell GJ, Brown IS, Mino-Kenudson M. Neutrophilic infiltration in gluten-sensitive enteropathy is neither uncommon nor insignificant: assessment of duodenal biopsies from 267 pediatric and adult patients. Am J Surg Pathol 2012; 36(9): 1339-1345.

40. Brown IS, Smith J, Rosty C. Gastrointestinal pathology in celiac disease: a case series of 150 consecutive newly diagnosed patients. Am J Clin Pathol 2012; 138(1): 42-49.

41. Wakim-Fleming J, Pagadala MR, Lemyre MS, et al. Diagnosis of celiac disease in adults based on serology test results, without small-bowel biopsy. Clin Gastroenterol Hepatol 2013; 11(5): 511-516.

42. Tursi A, Brandimarte G, Giorgetti G, et al. Low prevalence of antigliadin and anti-endomysium antibodies in subclinical/silent celiac disease. Am J Gastroenterol 2001; 96(5): 1507- 1510.

43. Brown I, Mino-Kenudson M, Deshpande V, Lauwers GY. Intraepithelial lymphocytosis in architecturally preserved proximal small intestinal mucosa: an increasing diagnostic problem with a wide differential diagnosis. Arch Pathol Lab Med 2006; 130(7): 1020-1025.

44. Meini A, Pillan NM, Villanacci V, et al. Prevalence and diagnosis of celiac disease in IgA-deficient children. Ann Allergy Asthma Immunol 1996; 77(4): 333-336.

45. Cataldo F, Lio D, Marino V, et al. IgG(1) antiendomysium and IgG antitissue transglutaminase (anti-tTG) antibodies in coeliac patients with selective IgA deficiency. Working Groups on Celiac Disease of SIGEP and Club del Tenue. Gut 2000; 47(3): 366-369.

46. Hadithi M, von Blomberg BM, Crusius JB, et al. Accuracy of serologic tests and HLA-DQ typing for diagnosing celiac disease. Ann Intern Med 2007; 147(5): 294-302.

47. Wolters VM, Wijmenga C. Genetic background of celiac disease and its clinical implications. Am J Gastroenterol 2008; 103(1): 190- 195.

48. Rishi AR, Rubio-Tapia A, Murray JA. Refractory celiac disease. Expert Rev Gastroenterol Hepatol 2016; 10(4): 537-546.

49. Malamut G, Cellier C. Refractory celiac disease. Gastroenterol Clin North Am 2019; 48(1): 137-144.

50. Abdulkarim AS, Burgart LJ, See J, Murray JA. Etiology of nonresponsive celiac disease: results of a systematic approach. Am J Gastroenterol 2002; 97(8): 2016-2021.

51. Cellier C, Patey N, Mauvieux L, et al. Abnormal intestinal intraepithelial lymphocytes in refractory sprue. Gastroenterology 1998; 114(3): 471-481.

52. Bagdi E, Diss TC, Munson P, Isaacson PG. Mucosal intra-epithelial lymphocytes in enteropathy- associated T-cell lymphoma, ulcerative jejunitis, and refractory celiac disease constitute a neoplastic population. Blood 1999; 94(1): 260-264.

53. Cellier C, Delabesse E, Helmer C, et al. Refractory sprue, coeliac disease, and enteropathy- associated T-cell lymphoma. French Coeliac Disease Study Group. Lancet 2000; 356(9225): 203-208.

54. Farstad IN, Lundin KE. Gastrointestinal intraepithelial lymphocytes and T cell lymphomas. Gut 2003; 52(2): 163-164.

55. Cellier C, Cerf-Bensussan N. Treatment of clonal refractory celiac disease or cryptic intraepithelial lymphoma: A long road from bench to bedside. Clin Gastroenterol Hepatol 2006; 4(11): 1320-1321.

56. O’Shea U, Abuzakouk M, O’Morain C, et al. Investigation of molecular markers in the diagnosis of refractory coeliac disease in a large patient cohort. J Clin Pathol 2008; 61(11): 1200-1202.

57. Celli R, Hui P, Triscott H, et al. Clinical insignificance of monoclonal T-cell populations and duodenal intraepithelial T-cell phenotypes in celiac and nonceliac patients. Am J Surg Pathol 2019; 43(2): 151-160.

58. Catassi C, Elli L, Bonaz B, et al. Diagnosis of non-celiac gluten sensitivity (NCGS): The Salerno experts’ criteria. Nutrients 2015; 7(6): 4966-4977.

59. Molina-Infante J, Carroccio A. Suspected nonceliac gluten sensitivity confirmed in few patients after gluten challenge in double- blind, placebo-controlled trials. Clin Gastroenterol Hepatol 2017; 15(3): 339-348.

60. Zanini B, Villanacci V, Marullo M, et al. Duodenal histological features in suspected non-celiac gluten sensitivity: new insights into a still undefined condition. Virchows Arch 2018; 473(2): 229-234.

61. Zanini B, Bozzola A, Villanacci V. Letter to the Editor. Virchows Arch 2019; 474(5): 639- 640.

62. Kirmizi A, Ensari A. Morphologic spectrum of gluten-related disorders: how far to go? Virchows Arch 2019; 474(5): 641-642.

63. Memeo L, Jhang J, Hibshoosh H, et al. Duodenal intraepithelial lymphocytosis with normal villous architecture: common occurrence in H. pylori gastritis. Mod Pathol 2005; 18(8): 1134-1144.

64. Nahon S, Patey-Mariaud De Serre N, Lejeune O, et al. Duodenal intraepithelial lymphocytosis during Helicobacter pylori infection is reduced by antibiotic treatment. Histopathology 2006; 48(4): 417-423.

65. Bosch DE, Liu YJ, Truong CD, et al. Duodenal intraepithelial lymphocytosis in Helicobacter pylori gastritis: comparison before and after treatment. Virchows Arch 2021; 478(4): 805- 809.

66. Aziz I, Evans KE, Hopper AD, Smillie DM, Sanders DS. A prospective study into the aetiology of lymphocytic duodenosis. Aliment Pharmacol Ther 2010; 32(11-12): 1392-1397.

67. Jenkins D, Goodall A, Gillet FR, Scott BB. Defining duodenitis: quantitative histological study of mucosal responses and their correlations. J Clin Pathol 1985; 38(10): 1119-1126.

68. Wyatt JI, Rathbone BJ, Dixon MF, Heatley RV. Campylobacter pyloridis and acid induced gastric metaplasia in the pathogenesis of duodenitis. J Clin Pathol 1987; 40(8): 841- 848.

69. van de Bovenkamp JH, Mahdavi J, Korteland- Van Male AM, et al. The MUC5AC glycoprotein is the primary receptor for Helicobacter pylori in the human stomach. Helicobacter 2003; 8(5): 521-532.

70. Suriani R, Venturini I, Actis GC, et al. Effect of Helicobacter pylori eradication on bulbitis and duodenal gastric metaplasia. Hepatogastroenterology 2004; 51(55): 176-180.

71. Frezza M, Gorji N, Melato M. The histopathology of non-steroidal anti-inflammatory drug induced gastroduodenal damage: correlation with Helicobacter pylori, ulcers, and haemorrhagic events. J Clin Pathol 2001; 54(7): 521-525.

72. Kakar S, Nehra V, Murray JA, Dayharsh GA, Burgart LJ. Significance of intraepithelial lymphocytosis in small bowel biopsy samples with normal mucosal architecture. Am J Gastroenterol 2003; 98(9): 2027-2033.

73. Lanas A, Sopena F. Nonsteroidal anti-inflammatory drugs and lower gastrointestinal complications. Gastroenterol Clin North Am 2009; 38(2): 333-352.

74. Shmidt E, Smyrk TC, Boswell CL, Enders FT, Oxentenko AS. Increasing duodenal intraepithelial lymphocytosis found at upper endoscopy: time trends and associations. Gastrointest Endosc 2014; 80(1): 105-111.

75. Marthey L, Cadiot G, Seksik P, et al. Olmesartan- associated enteropathy: results of a national survey. Aliment Pharmacol Ther 2014; 40(9): 1103-1109.

76. Choi EY, McKenna BJ. Olmesartan-associated enteropathy: a review of clinical and histologic findings. Arch Pathol Lab Med 2015; 139(10): 1242-1247.

77. Burbure N, Lebwohl B, Arguelles-Grande C, et al. Olmesartan-associated sprue-like enteropathy: a systematic review with emphasis on histopathology. Hum Pathol 2016; 50: 127- 134.

78. Kamal A, Fain C, Park A, et al. Angiotensin II receptor blockers and gastrointestinal adverse events of resembling sprue-like enteropathy: a systematic review. Gastroenterol Rep (Oxf) 2019; 7(3): 162-167.

79. Rubio-Tapia A, Herman ML, Ludvigsson JF, et al. Severe spruelike enteropathy associated with olmesartan. Mayo Clin Proc 2012; 87(8): 732-738.

80. Oble DA, Mino-Kenudson M, Goldsmith J, et al. Alpha-CTLA-4 mAb-associated panenteritis: a histologic and immunohistochemical analysis. Am J Surg Pathol 2008; 32(8): 1130- 1137.

81. Louie CY, DiMaio MA, Matsukuma KE, et al. Idelalisib-associated enterocolitis: clinicopathologic features and distinction from other enterocolitides. Am J Surg Pathol 2015; 39(12): 1653-1660.

82. Zhang ML, Neyaz A, Patil D, et al. Immune- related adverse events in the gastrointestinal tract: diagnostic utility of upper gastrointestinal biopsies. Histopathology 2020; 76(2): 233-243.

83. Gonzalez RS, Salaria SN, Bohannon CD, et al. PD-1 inhibitor gastroenterocolitis: case series and appraisal of ‘immunomodulatory gastroenterocolitis’. Histopathology 2017; 70(4): 558-567.

84. Cunningham-Rundles C, Bodian C. Common variable immunodeficiency: clinical and immunological features of 248 patients. Clin Immunol 1999; 92(1): 34-48.

85. Oksenhendler E, Gerard L, Fieschi C, et al. Infections in 252 patients with common variable immunodeficiency. Clin Infect Dis 2008; 46(10): 1547-1554.

86. Pikkarainen S, Martelius T, Ristimaki A, et al. A high prevalence of gastrointestinal manifestations in common variable immunodeficiency. Am J Gastroenterol 2019; 114(4): 648- 655.

87. Hermans PE, Diaz-Buxo JA, Stobo JD. Idiopathic late-onset immunoglobulin deficiency. Clinical observations in 50 patients. Am J Med 1976; 61(2): 221-237.

88. Washington K, Stenzel TT, Buckley RH, Gottfried MR. Gastrointestinal pathology in patients with common variable immunodeficiency and X-linked agammaglobulinemia. Am J Surg Pathol 1996; 20(10): 1240-1252.

89. Daniels JA, Lederman HM, Maitra A, Montgomery EA. Gastrointestinal tract pathology in patients with common variable immunodeficiency (CVID): a clinicopathologic study and review. Am J Surg Pathol 2007; 31(12): 1800-1812.

90. Khodadad A, Aghamohammadi A, Parvaneh N, et al. Gastrointestinal manifestations in patients with common variable immunodeficiency. Dig Dis Sci 2007; 52(11): 2977-2983.

91. Malamut G, Verkarre V, Suarez F, et al. The enteropathy associated with common variable immunodeficiency: the delineated frontiers with celiac disease. Am J Gastroenterol 2010; 105(10): 2262-2275.

92. Resnick ES, Moshier EL, Godbold JH, Cunningham- Rundles C. Morbidity and mortality in common variable immune deficiency over 4 decades. Blood 2012; 119(7): 1650- 1657.

93. Fontaine JL, Navarro J. Small intestinal biopsy in cows milk protein allergy in infancy. Arch Dis Child 1975; 50(5): 357-362.

94. Challacombe DN, Wheeler EE, Campbell PE. Morphometric studies and eosinophil cell counts in the duodenal mucosa of children with chronic nonspecific diarrhoea and cow’s milk allergy. J Pediatr Gastroenterol Nutr 1986; 5(6): 887-891.

95. Garcia-Careaga M, Jr., Kerner JA, Jr. Gastrointestinal manifestations of food allergies in pediatric patients. Nutr Clin Pract 2005; 20(5): 526-535.

96. Umetsu SE, Brown I, Langner C, Lauwers GY. Autoimmune enteropathies. Virchows Arch 2018; 472(1): 55-66.

97. Unsworth DJ, Walker-Smith JA. Autoimmunity in diarrhoeal disease. J Pediatr Gastroenterol Nutr 1985; 4(3): 375-380.

98. Akram S, Murray JA, Pardi DS, et al. Adult autoimmune enteropathy: Mayo Clinic Rochester experience. Clin Gastroenterol Hepatol 2007; 5(11): 1282-1290.

99. Singhi AD, Goyal A, Davison JM, et al. Pediatric autoimmune enteropathy: an entity frequently associated with immunodeficiency disorders. Mod Pathol 2014; 27(4): 543-553.

100. Masia R, Peyton S, Lauwers GY, Brown I. Gastrointestinal biopsy findings of autoimmune enteropathy: a review of 25 cases. Am J Surg Pathol 2014; 38(10): 1319-1329.

101. Biagi F, Bianchi PI, Trotta L, Corazza GR. Anti- goblet cell antibodies for the diagnosis of autoimmune enteropathy? Am J Gastroenterol 2009; 104(12): 3112.

102. Skogh T, Heuman R, Tagesson C. Anti-brush border antibodies (ABBA) in Crohn’s disease. J Clin Lab Immunol 1982; 9(3): 147-150.

103. Fiocchi C, Roche JK, Michener WM. High prevalence of antibodies to intestinal epithelial antigens in patients with inflammatory bowel disease and their relatives. Ann Intern Med 1989; 110(10): 786-794.

104. Martin-Villa JM, Camblor S, Costa R, Arnaiz- Villena A. Gut epithelial cell autoantibodies in AIDS pathogenesis. Lancet 1993; 342(8867): 380.

105. Saraswati R, Rodriguez-Justo M, Novelli M. The upper gastrointestinal tract in the immunosuppressed patient. Diagn Histopathol 2012; 18(10): 437-448.

106. Agus SG, Dolin R, Wyatt RG, Tousimis AJ, Northrup RS. Acute infectious nonbacterial gastroenteritis: intestinal histopathology. Histologic and enzymatic alterations during illness produced by the Norwalk agent in man. Ann Intern Med 1973; 79(1): 18-25.

107. Bishop RF, Davidson GP, Holmes IH, Ruck BJ. Virus particles in epithelial cells of duodenal mucosa from children with acute non-bacterial gastroenteritis. Lancet 1973; 2(7841): 1281-1283.

108. Barnes GL, Townley RR. Duodenal mucosal damage in 31 infants with gastroenteritis. Arch Dis Child 1973; 48(5): 343-349.

109. Brown IS, Bettington A, Bettington M, Rosty C. Self-limited coeliac-like enteropathy: a series of 18 cases highlighting another coeliac disease mimic. Histopathology 2016; 68(2): 254-261.

110. Bures J, Cyrany J, Kohoutova D, et al. Small intestinal bacterial overgrowth syndrome. World J Gastroenterol 2010; 16(24): 2978-2990.

111. Quigley EM, Abu-Shanab A. Small intestinal bacterial overgrowth. Infect Dis Clin North Am 2010; 24(4): 943-959.

112. Riordan SM, McIver CJ, Duncombe VM, et al. Small intestinal bacterial overgrowth and the irritable bowel syndrome. Am J Gastroenterol 2001; 96(8): 2506-2508.

113. Lappinga PJ, Abraham SC, Murray JA, et al. Small intestinal bacterial overgrowth: histopathologic features and clinical correlates in an underrecognized entity. Arch Pathol Lab Med 2010; 134(2): 264-270.

114. Hammer ST, Greenson JK. The clinical significance of duodenal lymphocytosis with normal villus architecture. Arch Pathol Lab Med 2013; 137(9): 1216-1219.

115. Tursi A, Brandimarte G, Giorgetti G. High prevalence of small intestinal bacterial overgrowth in celiac patients with persistence of gastrointestinal symptoms after gluten withdrawal. Am J Gastroenterol 2003; 98(4): 839- 843.

116. Harrison E, Hayes S, Howell L, Lal S. All that glitters is not always gold. BMJ Case Rep 2014; 2014.

117. Baker SJ, Mathan VI. Syndrome of tropical sprue in South India. Am J Clin Nutr 1968; 21(9): 984-993.

118. Klipstein FA. Tropical sprue in travelers and expatriates living abroad. Gastroenterology 1981; 80(3): 590-600.

119. Nath SK. Tropical sprue. Curr Gastroenterol Rep 2005; 7(5): 343-349.

120. Batheja MJ, Leighton J, Azueta A, Heigh R. The face of tropical sprue in 2010. Case Rep Gastroenterol 2010; 4(2): 168-172.

121. Ramakrishna BS. Tropical sprue: a riddle wrapped in a mystery inside an enigma. Indian J Med Res 2013; 137(1): 12-14.

122. Swanson VL, Thomassen RW. Pathology of the jejunal mucosa in tropical sprue. Am J Pathol 1965; 46(4): 511-551.

123. Schenk EA, Samloff IM, Klipstein FA. Morphologic characteristics of jejunal biopsy in celiac disease and tropical sprue. Am J Pathol 1965; 47(5): 765-781.

124. Brown IS, Bettington A, Bettington M, Rosty C. Tropical sprue: revisiting an underrecognized disease. Am J Surg Pathol 2014; 38(5): 666-672.

125. Maguire AA, Greenson JK, Lauwers GY, et al. Collagenous sprue: a clinicopathologic study of 12 cases. Am J Surg Pathol 2009; 33(10): 1440-1449.

126. Vakiani E, Arguelles-Grande C, Mansukhani MM, et al. Collagenous sprue is not always associated with dismal outcomes: a clinicopathological study of 19 patients. Mod Pathol 2010; 23(1): 12-26.

127. Nielsen JA, Steephen A, Lewin M. Angiotensin- II inhibitor (olmesartan)-induced collagenous sprue with resolution following discontinuation of drug. World J Gastroenterol 2013; 19(40): 6928-6930.

128. Nielsen OH, Riis LB, Danese S, Bojesen RD, Soendergaard C. Proximal collagenous gastroenteritides: clinical management. A systematic review. Ann Med 2014; 46(5): 311-317.

129. Desruisseaux C, Bensoussan M, Desilets E, et al. Adding water to the mill: olmesartan- induced collagenous sprue-a case report and brief literature review. Can J Gastroenterol Hepatol 2016; 2016: 4837270.

130. Mandaliya R, Burkart AL, DiMarino AJ, Rattan S, Cohen S. Association between common variable immunodeficiency and collagenous infiltrative disorders of the gastrointestinal tract: A series of four patients. Indian J Gastroenterol 2016; 35(2): 133-138.

131. Sonnenberg A, Melton SD, Genta RM. Frequent occurrence of gastritis and duodenitis in patients with inflammatory bowel disease. Inflamm Bowel Dis 2011; 17(1): 39-44.

132. Wright CL, Riddell RH. Histology of the stomach and duodenum in Crohn’s disease. Am J Surg Pathol 1998; 22(4): 383-390.

133. Valdez R, Appelman HD, Bronner MP, Greenson JK. Diffuse duodenitis associated with ulcerative colitis. Am J Surg Pathol 2000; 24(10): 1407-1413.

134. Lin J, McKenna BJ, Appelman HD. Morphologic findings in upper gastrointestinal biopsies of patients with ulcerative colitis: a controlled study. Am J Surg Pathol 2010; 34(11): 1672-1677.

135. Kreuning J, Val AMVD, Kuiper G, Lindeman J. Chronic nonspecific duodenitis. A multiple biopsy study of the duodenal bulb in health and disease. Scand J Gastroenterol 1989; 24(Suppl. 167): 16-20.

136. Bjarnason I, Zanelli G, Smith T, et al. Nonsteroidal antiinflammatory drug-induced intestinal inflammation in humans. Gastroenterology 1987; 93(3): 480-489.

137. Bjarnason I, Zanelli G, Prouse P, et al. Blood and protein loss via small-intestinal inflammation induced by non-steroidal anti-inflammatory drugs. Lancet 1987; 2(8561): 711-714.

138. Patey-Mariaud de Serre N, Canioni D, Ganousse S, et al. Digestive histopathological presentation of IPEX syndrome. Mod Pathol 2009; 22(1): 95-102.

139. Washington K, Jagasia M. Pathology of graft-versus-host disease in the gastrointestinal tract. Hum Pathol 2009; 40(7): 909-917.

140. Parfitt JR, Jayakumar S, Driman DK. Mycophenolate mofetil-related gastrointestinal mucosal injury: variable injury patterns, including graft-versus-host disease-like changes. Am J Surg Pathol 2008; 32(9): 1367-1372.

141. Cotter MB, AbuShanab A, Merriman R, Mc- Cormick A, Sheahan K. Coeliac-like duodenal pathology in orthotopic liver transplant patients on mycophenolic acid therapy. Histopathology 2015; 66(4): 500-507.

142. Ramachandran A, Madesh M, Balasubramanian KA. Apoptosis in the intestinal epithelium: its relevance in normal and pathophysiological conditions. J Gastroenterol Hepatol 2000; 15(2): 109-120.

143. Iqbal N, Salzman D, Lazenby AJ, Wilcox CM. Diagnosis of gastrointestinal graft-versushost disease. Am J Gastroenterol 2000; 95(11): 3034-3038.

144. Lee FD. Importance of apoptosis in the histopathology of drug related lesions in the large intestine. J Clin Pathol 1993; 46(2): 118-122.

145. Iwamoto M, Koji T, Makiyama K, Kobayashi N, Nakane PK. Apoptosis of crypt epithelial cells in ulcerative colitis. J Pathol 1996; 180(2): 152-159.

146. Lempinen M, Halme L, Sarkio S, et al. CMV findings in the gastrointestinal tract in kidney transplantation patients, patients with endstage kidney disease and immunocompetent patients. Nephrol Dial Transplant 2009; 24(11): 3533-3539.

147. Kaufman SS, Magid MS, Tschernia A, Le- Leiko NS, Fishbein TM. Discrimination between acute rejection and adenoviral enteritis in intestinal transplant recipients. Transplant Proc 2002; 34(3): 943-945.

148. Nguyen T, Park JY, Scudiere JR, Montgomery E. Mycophenolic acid (cellcept and myofortic) induced injury of the upper GI tract. Am J Surg Pathol 2009; 33(9): 1355-1363.

149. Coyne JD, Campbell F. Microscopic features associated with mycophenolate mofetil in gastric and colonic biopsies. Histopathology 2012; 61(5): 993-997.

150. Epstein RJ, McDonald GB, Sale GE, Shulman HM, Thomas ED. The diagnostic accuracy of the rectal biopsy in acute graft-versushost disease: a prospective study of thirteen patients. Gastroenterology 1980; 78(4): 764- 771.

151. Lee EY, Clouse RE, Aliperti G, De- Schryver-Kecskemeti K. Small intestinal lesion resembling graft-vs-host disease. A case report in immunodeficiency and review of the literature. Arch Pathol Lab Med 1991; 115(5): 529-532.

152. Pascal RR, Gramlich TL, Parker KM, Gansler TS. Geographic variations in eosinophil concentration in normal colonic mucosa. Mod Pathol 1997; 10(4): 363-365.

153. DeBrosse CW, Case JW, Putnam PE, Collins MH, Rothenberg ME. Quantity and distribution of eosinophils in the gastrointestinal tract of children. Pediatr Dev Pathol 2006; 9(3): 210-218.

154. Polydorides AD, Banner BF, Hannaway PJ, Yantiss RK. Evaluation of site-specific and seasonal variation in colonic mucosal eosinophils. Hum Pathol 2008; 39(6): 832-836.

155. Matsushita T, Maruyama R, Ishikawa N, et al. The number and distribution of eosinophils in the adult human gastrointestinal tract: a study and comparison of racial and environmental factors. Am J Surg Pathol 2015; 39(4): 521-527.

156. Talley NJ, Walker MM, Aro P, et al. Non-ulcer dyspepsia and duodenal eosinophilia: an adult endoscopic population-based case-control study. Clin Gastroenterol Hepatol 2007; 5(10): 1175-1183.

157. Lowichik A, Weinberg AG. A quantitative evaluation of mucosal eosinophils in the pediatric gastrointestinal tract. Mod Pathol 1996; 9(2): 110-114.

158. Rothenberg ME. Eosinophilic gastrointestinal disorders (EGID). J Allergy Clin Immunol 2004; 113(1): 11-28.

159. Lee CM, Changchien CS, Chen PC, et al. Eosinophilic gastroenteritis: 10 years experience. Am J Gastroenterol 1993; 88(1): 70-74.

160. Chen MJ, Chu CH, Lin SC, Shih SC, Wang TE. Eosinophilic gastroenteritis: clinical experience with 15 patients. World J Gastroenterol 2003; 9(12): 2813-2816.

161. Hallgren R, Colombel JF, Dahl R, et al. Neutrophil and eosinophil involvement of the small bowel in patients with celiac disease and Crohn’s disease: studies on the secretion rate and immunohistochemical localization of granulocyte granule constituents. Am J Med 1989; 86(1): 56-64.

162. Lanham JG, Elkon KB, Pusey CD, Hughes GR. Systemic vasculitis with asthma and eosinophilia: a clinical approach to the Churg- Strauss syndrome. Medicine (Baltimore) 1984; 63(2): 65-81.

163. Barbie DA, Mangi AA, Lauwers GY. Eosinophilic gastroenteritis associated with systemic lupus erythematosus. J Clin Gastroenterol 2004; 38(10): 883-886.

164. Valent P, Klion AD, Horny HP, et al. Contemporary consensus proposal on criteria and classification of eosinophilic disorders and related syndromes. J Allergy Clin Immunol 2012; 130(3): 607-612.

165. Hahn HP, Hornick JL. Immunoreactivity for CD25 in gastrointestinal mucosal mast cells is specific for systemic mastocytosis. Am J Surg Pathol 2007; 31(11): 1669-1676.

166. Kirsch R, Geboes K, Shepherd NA, et al. Systemic mastocytosis involving the gastrointestinal tract: clinicopathologic and molecular study of five cases. Mod Pathol 2008; 21(12): 1508-1516.

167. Sokol H, Georgin-Lavialle S, Grandpeix- Guyodo C, et al. Gastrointestinal involvement and manifestations in systemic mastocytosis. Inflamm Bowel Dis 2010; 16(7): 1247-1253.

168. Doyle LA, Sepehr GJ, Hamilton MJ, et al. A clinicopathologic study of 24 cases of systemic mastocytosis involving the gastrointestinal tract and assessment of mucosal mast cell density in irritable bowel syndrome and asymptomatic patients. Am J Surg Pathol 2014; 38(6): 832-843.

169. Saeed SA, Integlia MJ, Pleskow RG, et al. Tacrolimus- associated eosinophilic gastroenterocolitis in pediatric liver transplant recipients: role of potential food allergies in pathogenesis. Pediatr Transplant 2006; 10(6): 730-735.

170. Barak N, Hart J, Sitrin MD. Enalapril-induced eosinophilic gastroenteritis. J Clin Gastroenterol 2001; 33(2): 157-158.

171. Martin DM, Goldman JA, Gilliam J, Nasrallah SM. Gold-induced eosinophilic enterocolitis: response to oral cromolyn sodium. Gastroenterology 1981; 80(6): 1567-1570.

172. Hurrell JM, Genta RM, Melton SD. Histopathologic diagnosis of eosinophilic conditions in the gastrointestinal tract. Adv Anat Pathol 2011; 18(5): 335-348.

173. Rivasi F, Pampiglione S, Boldorini R, Cardinale L. Histopathology of gastric and duodenal Strongyloides stercoralis locations in fifteen immunocompromised subjects. Arch Pathol Lab Med 2006; 130(12): 1792-1798.

174. Couture C, Measures L, Gagnon J, Desbiens C. Human intestinal anisakiosis due to consumption of raw salmon. Am J Surg Pathol 2003; 27(8): 1167-1172.

175. Oddo D, Mendez GP, Retamal Y, Oddo A. Intestinal isosporiasis in patients with acquired immunodeficiency syndrome (AIDS). Pathologic diagnosis in small intestinal mucosal biopsies. Ann Diagn Pathol 2018; 33): 17-22.

176. Croese J, Wood MJ, Melrose W, Speare R. Allergy controls the population density of Necator americanus in the small intestine. Gastroenterology 2006; 131(2): 402-409.

177. Hesdorffer CS, Ziady F. Eosinophilic gastro- enteritis - a complication of schistosomiasis and peripheral eosinophilia? A case report and review of the pathogenesis. S Afr Med J 1982; 61(16): 591-593.

178. Black-Schaffer B. The tinctoral demonstration of a glycoprotein in Whipple’s disease. Proc Soc Exp Biol Med 1949; 72(1): 225-227.

179. Chears WC, Jr., Ashworth CT. Electron microscopic study of the intestinal mucosa in Whipple’s disease. Demonstration of encapsulated bacilliform bodies in the lesion. Gastroenterology 1961; 41: 129-138.

180. Relman DA, Schmidt TM, MacDermott RP, Falkow S. Identification of the uncultured bacillus of Whipple’s disease. N Engl J Med 1992; 327(5): 293-301.

181. Wilson KH, Blitchington R, Frothingham R, Wilson JA. Phylogeny of the Whipple’s-disease- associated bacterium. Lancet 1991; 338(8765): 474-475.

182. Baisden BL, Lepidi H, Raoult D, et al. Diagnosis of Whipple disease by immunohistochemical analysis: a sensitive and specific method for the detection of Tropheryma whipplei (the Whipple bacillus) in paraffin- embedded tissue. Am J Clin Pathol 2002; 118(5): 742-748.

183. Newman B, Pope RH. A case of intestinal lipodystrophy, Whipple’s disease, simulating Boeck’s sarcoid. Gastroenterology 1948; 11(1): 120-126.

184. Rodarte JR, Garrison CO, Holley KE, Fontana RS. Whipple’s disease simulating sarcoidosis. A case with unique clinical and histologic features. Arch Intern Med 1972; 129(3): 479-482.

185. Trier JS, Phelps PC, Eidelman S, Rubin CE. Whipple’s disease: light and electron microscope correlation of jejunal mucosal histology with antibiotic treatment and clinical status. Gastroenterology 1965; 48(6): 684-707.

186. Ramaiah C, Boynton RF. Whipple’s disease. Gastroenterol Clin North Am 1998; 27(3): 683- 695.

187. Haggerty CM, Britton MC, Dorman JM, Marzoni FA, Jr. Gastrointestinal histoplasmosis in suspected acquired immunodeficiency syndrome. West J Med 1985; 143(2): 244-246.

188. Alvarez-Nebreda ML, Alvarez-Fernandez E, Rada S, et al. Unusual duodenal presentation of leishmaniasis. J Clin Pathol 2005; 58(12): 1321-1322.

189. Kinchen K, Kinchen TH, Inglesby T, Jr. Pneumocystis carinii infection of the small intestine. J Natl Med Assoc 1998; 90(10): 625-627.

190. Sagaert X, Tousseyn T, De Hertogh G, Geboes K. Macrophage-related diseases of the gut: a pathologist’s perspective. Virchows Arch 2012; 460(6): 555-567.

191. Canani RB, Terrin G. Recent progress in congenital diarrheal disorders. Curr Gastroenterol Rep 2011; 13(3): 257-264.

192. Martin BA, Kerner JA, Hazard FK, Longacre TA. Evaluation of intestinal biopsies for pediatric enteropathy: a proposed immunohistochemical panel approach. Am J Surg Pathol 2014; 38(10): 1387-1395.

193. Groisman GM, Amar M, Livne E. CD10: a valuable tool for the light microscopic diagnosis of microvillous inclusion disease (familial microvillous atrophy). Am J Surg Pathol 2002; 26(7): 902-907.

194. Ruemmele FM, Schmitz J, Goulet O. Microvillous inclusion disease (microvillous atrophy). Orphanet J Rare Dis 2006; 1: 22.

195. Bell SW, Kerner JA, Jr., Sibley RK. Microvillous inclusion disease. The importance of electron microscopy for diagnosis. Am J Surg Pathol 1991; 15(12): 1157-1164.

196. van der Velde KJ, Dhekne HS, Swertz MA, et al. An overview and online registry of microvillus inclusion disease patients and their MYO5B mutations. Hum Mutat 2013; 34(12): 1597-1605.

197. Goulet O, Salomon J, Ruemmele F, de Serres NP, Brousse N. Intestinal epithelial dysplasia (tufting enteropathy). Orphanet J Rare Dis 2007; 2: 20.

198. Schnell U, Kuipers J, Mueller JL, et al. Absence of cell-surface EpCAM in congenital tufting enteropathy. Hum Mol Genet 2013; 22(13): 2566-2571.

199. Sivagnanam M, Mueller JL, Lee H, et al. Identification of EpCAM as the gene for congenital tufting enteropathy. Gastroenterology 2008; 135(2): 429-437.

200. Cortina G, Smart CN, Farmer DG, et al. Enteroendocrine cell dysgenesis and malabsorption, a histopathologic and immunohistochemical characterization. Hum Pathol 2007; 38(4): 570-580.

Labels
Anatomical pathology Forensic medical examiner Toxicology
Login
Forgotten password

Enter the email address that you registered with. We will send you instructions on how to set a new password.

Login

Don‘t have an account?  Create new account

#ADS_BOTTOM_SCRIPTS#