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The differential diagnosis of Helicobacter pylori negative gastritis

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Abstract

Gastric biopsies are often submitted with as clinical question Helicobacter pylori (HP) infection. Regularly, the morphology suggests a HP infection but the organism is not detected in special stains. This review presents a practical approach to deal with such biopsies. The first step is to exclude a false negative result of the search for HP, by ensuring that both antral and oxyntic mucosa are present, by the use of sensitive stains, identification of marked reactive changes, such as intestinal, pseudo-pyloric, pancreatic metaplasia that may suggest a diagnosis of (HP associated or autoimmune) atrophic gastritis, and finally identification of signs of the use of proton pump inhibitors (PPI) as in such biopsies, HP may sometimes be found only within parietal cells. The differential diagnosis should include lymphocytic gastritis, other diseases affecting the stomach, such as inflammatory bowel disease (IBD), vasculitis, granulomatous disease, viral infection, such as cytomegalovirus (CMV) or more rarely Epstein-Barr virus (EBV) infection, or other bacterial infections, such as Enterococcus and Treponema pallidum. Clinical input may be required to ensure the patient is not taking medication that may cause gastritis, such as antibiotics used for HP eradication or common medications that cause a form of gastropathy. When these have been excluded, a known cause has not been found and in such a case, the term idiopathic focal/diffuse gastritis can be used.

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References

  1. Maguilnik I, Neumann WL, Sonnenberg A, Genta RM (2012) Reactive gastropathy is associated with inflammatory conditions throughout the gastrointestinal tract. Aliment Pharmacol Ther 36:736–743. https://doi.org/10.1111/apt.12031

    Article  PubMed  CAS  Google Scholar 

  2. Wolf EM, Plieschnegger W, Geppert M, Wigginghaus B, Hoss GM, Eherer A, Schneider NI, Hauer A, Rehak P, Vieth M, Langner C (2014) Changing prevalence patterns in endoscopic and histological diagnosis of gastritis? Data from a cross-sectional central European multicentre study. Dig Liver Dis 46:412–418. https://doi.org/10.1016/j.dld.2013.12.017

    Article  PubMed  Google Scholar 

  3. Kamada T, Haruma K, Ito M, Inoue K, Manabe N, Matsumoto H, Kusunoki H, Hata J, Yoshihara M, Sumii K, Akiyama T, Tanaka S, Shiotani A, Graham DY (2015) Time trends in Helicobacter pylori infection and atrophic gastritis over 40 years in Japan. Helicobacter 20:192–198. https://doi.org/10.1111/hel.12193

    Article  PubMed  PubMed Central  Google Scholar 

  4. Murakami TT, Scranton RA, Brown HE, Harris RB, Chen Z, Musuku S, Oren E (2017) Management of Helicobacter pylori in the United States: results from a national survey of gastroenterology physicians. Prev Med 100:216–222. https://doi.org/10.1016/j.ypmed.2017.04.021

    Article  PubMed  Google Scholar 

  5. Kocsmar E, Szirtes I, Kramer Z, Szijarto A, Bene L, Buzas GM, Kenessey I, Bronsert P, Csanadi A, Lutz L, Werner M, Wellner UF, Kiss A, Schaff Z, Lotz G (2017) Sensitivity of Helicobacter pylori detection by Giemsa staining is poor in comparison with immunohistochemistry and fluorescent in situ hybridization and strongly depends on inflammatory activity. Helicobacter 22. https://doi.org/10.1111/hel.12387

    Article  CAS  Google Scholar 

  6. El-Zimaity HM, Segura AM, Genta RM, Graham DY (1998) Histologic assessment of Helicobacter pylori status after therapy: comparison of Giemsa, Diff-Quik, and Genta stains. Mod Pathol 11:288–291

    PubMed  CAS  Google Scholar 

  7. El-Zimaity HMT, Gutierrez O, Kim JG, Akamatsu T, Gurer IE, Simjee AE, Graham DY (2001) Geographic differences in the distribution of intestinal metaplasia in duodenal ulcer patients. Am J Gastroenterol 96:666–672. https://doi.org/10.1111/j.1572-0241.2001.03601.x

    Article  PubMed  Google Scholar 

  8. El-Zimaity HM, Graham DY (1999) Evaluation of gastric mucosal biopsy site and number for identification of Helicobacter pylori or intestinal metaplasia: role of the Sydney System. Hum Pathol 30:72–77

    Article  CAS  PubMed  Google Scholar 

  9. El-Zimaity H, Serra S, Szentgyorgyi E, Vajpeyi R, Samani A (2013) Gastric biopsies: the gap between evidence-based medicine and daily practice in the management of gastric Helicobacter pylori infection. Can J Gastroenterol 27:e25–e30

    Article  PubMed  PubMed Central  Google Scholar 

  10. el-Zimaity HM, al-Assi MT, Genta RM, Graham DY (1995) Confirmation of successful therapy of Helicobacter pylori infection: number and site of biopsies or a rapid urease test. Am J Gastroenterol 90:1962–1964

    PubMed  CAS  Google Scholar 

  11. Gabrieli D, Ciccone F, Capannolo A, Viscido A, Valerii G, Serva D, Necozione S, Coletti G, Calvisi G, Melideo D, Frieri G, Latella G (2017) Subtypes of chronic gastritis in patients with celiac disease before and after gluten-free diet. United European Gastroenterol J 5:805–810. https://doi.org/10.1177/2050640616684698

    Article  PubMed  PubMed Central  Google Scholar 

  12. Wu TT, Hamilton SR (1999) Lymphocytic gastritis: association with etiology and topology. Am J Surg Pathol 23:153–158

    Article  CAS  PubMed  Google Scholar 

  13. Rostami K, Marsh MN, Johnson MW, Mohaghegh H, Heal C, Holmes G, Ensari A, Aldulaimi D, Bancel B, Bassotti G, Bateman A, Becheanu G, Bozzola A, Carroccio A, Catassi C, Ciacci C, Ciobanu A, Danciu M, Derakhshan MH, Elli L, Ferrero S, Fiorentino M, Fiorino M, Ganji A, Ghaffarzadehgan K, Going JJ, Ishaq S, Mandolesi A, Mathews S, Maxim R, Mulder CJ, Neefjes-Borst A, Robert M, Russo I, Rostami-Nejad M, Sidoni A, Sotoudeh M, Villanacci V, Volta U, Zali MR, Srivastava A (2017) ROC-king onwards: intraepithelial lymphocyte counts, distribution & role in coeliac disease mucosal interpretation. Gut 66:2080–2086. https://doi.org/10.1136/gutjnl-2017-314297

    Article  PubMed  Google Scholar 

  14. De Giacomo C, Gianatti A, Negrini R, Perotti P, Bawa P, Maggiore G, Fiocca R (1994) Lymphocytic gastritis: a positive relationship with celiac disease. J Pediatr 124:57–62

    Article  PubMed  Google Scholar 

  15. Lebwohl B, Green PH, Genta RM (2015) The coeliac stomach: gastritis in patients with coeliac disease. Aliment Pharmacol Ther 42:180–187. https://doi.org/10.1111/apt.13249

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Kim YJ, Jang KS (2017) Development of lymphocytic gastritis with recurrent Helicobacter pylori infection. Pediatr Int 59:234–236. https://doi.org/10.1111/ped.13175

    Article  PubMed  Google Scholar 

  17. Hayat M, Arora DS, Wyatt JI, O'Mahony S, Dixon MF (1999) The pattern of involvement of the gastric mucosa in lymphocytic gastritis is predictive of the presence of duodenal pathology. J Clin Pathol 52:815–819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Madisch A, Miehlke S, Neuber F, Morgner A, Kuhlisch E, Rappel S, Lehn N, Bayerdorffer E, Seitz G, Stolte M (2006) Healing of lymphocytic gastritis after Helicobacter pylori eradication therapy—a randomized, double-blind, placebo-controlled multicentre trial. Aliment Pharmacol Ther 23:473–479. https://doi.org/10.1111/j.1365-2036.2006.02778.x

    Article  PubMed  CAS  Google Scholar 

  19. Hachem CY, El-Zimaity H (2007) A man with rheumatoid arthritis and iron-deficiency anemia. MedGenMed 9:64

    PubMed  PubMed Central  Google Scholar 

  20. Montalban-Arques A, Wurm P, Trajanoski S, Schauer S, Kienesberger S, Halwachs B, Hogenauer C, Langner C, Gorkiewicz G (2016) Propionibacterium acnes overabundance and natural killer group 2 member D system activation in corpus-dominant lymphocytic gastritis. J Pathol 240:425–436. https://doi.org/10.1002/path.4782

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Arnason T, Brown IS, Goldsmith JD, Anderson W, O'Brien BH, Wilson C, Winter H, Lauwers GY (2015) Collagenous gastritis: a morphologic and immunohistochemical study of 40 patients. Mod Pathol 28:533–544. https://doi.org/10.1038/modpathol.2014.119

    Article  PubMed  CAS  Google Scholar 

  22. Kamimura K, Kobayashi M, Sato Y, Aoyagi Y, Terai S (2015) Collagenous gastritis: review. World J Gastrointest Endosc 7:265–273. https://doi.org/10.4253/wjge.v7.i3.265

    Article  PubMed  PubMed Central  Google Scholar 

  23. Vesoulis Z, Lozanski G, Ravichandran P, Esber E (2000) Collagenous gastritis: a case report, morphologic evaluation, and review. Mod Pathol 13:591–596. https://doi.org/10.1038/modpathol.3880101

    Article  PubMed  CAS  Google Scholar 

  24. Cote JF, Hankard GF, Faure C, Mougenot JF, Holvoet L, Cezard JP, Navarro J, Peuchmaur M (1998) Collagenous gastritis revealed by severe anemia in a child. Hum Pathol 29:883–886

    Article  CAS  PubMed  Google Scholar 

  25. Lagorce-Pages C, Fabiani B, Bouvier R, Scoazec JY, Durand L, Flejou JF (2001) Collagenous gastritis: a report of six cases. Am J Surg Pathol 25:1174–1179

    Article  CAS  PubMed  Google Scholar 

  26. Jin X, Koike T, Chiba T, Kondo Y, Ara N, Uno K, Asano N, Iijima K, Imatani A, Watanabe M, Shirane A, Shimosegawa T (2013) Collagenous gastritis. Dig Endosc 25:547–549. https://doi.org/10.1111/j.1443-1661.2012.01391.x

    Article  PubMed  Google Scholar 

  27. Kamimura K, Kobayashi M, Narisawa R, Watanabe H, Sato Y, Honma T, Sekine A, Aoyagi Y (2007) Collagenous gastritis: endoscopic and pathologic evaluation of the nodularity of gastric mucosa. Dig Dis Sci 52:995–1000. https://doi.org/10.1007/s10620-006-9278-y

    Article  PubMed  Google Scholar 

  28. Leung ST, Chandan VS, Murray JA, Wu TT (2009) Collagenous gastritis: histopathologic features and association with other gastrointestinal diseases. Am J Surg Pathol 33:788–798. https://doi.org/10.1097/PAS.0b013e318196a67f

    Article  PubMed  Google Scholar 

  29. Anwar MS, Aamar A, Marhaba A, Sidhu JS (2017) Collagenous gastritis in a young female with IgA deficiency. Gastroenterology Res 10:126–127. https://doi.org/10.14740/gr748w

    Article  PubMed  PubMed Central  Google Scholar 

  30. Mandaliya R, Burkart AL, DiMarino AJ, Rattan S, Cohen S (2016) Association between common variable immunodeficiency and collagenous infiltrative disorders of the gastrointestinal tract: a series of four patients. Indian J Gastroenterol 35:133–138. https://doi.org/10.1007/s12664-016-0633-4

    Article  PubMed  PubMed Central  Google Scholar 

  31. Al-Kandari A, Al-Alardati H, Sayadi H, Al-Judaibi B, Mawardi M (2014) An unusual case of collagenous gastritis in a middle- aged woman with systemic lupus erythromatosis: a case report. J Med Case Rep 8:278. https://doi.org/10.1186/1752-1947-8-278

    Article  PubMed  PubMed Central  Google Scholar 

  32. Saraswati S, Sitaraman R (2014) Aging and the human gut microbiota-from correlation to causality. Front Microbiol 5:764. https://doi.org/10.3389/fmicb.2014.00764

    Article  PubMed  Google Scholar 

  33. Billiemaz K, Robles-Medranda C, Le Gall C, Gay C, Mory O, Clemenson A, Bouvier R, Teyssier G, Lachaux A (2009) A first report of collagenous gastritis, sprue, and colitis in a 9-month-old infant: 14 years of clinical, endoscopic, and histologic follow-up. Endoscopy 41(Suppl 2):E233–E234. https://doi.org/10.1055/s-2008-1077440

    Article  PubMed  Google Scholar 

  34. Appelman MH, de Meij TG, Neefjes-Borst EA, Kneepkens CM (2016) Spontaneous gastric perforation in a case of collagenous gastritis APSP. J Case Rep 7:7

  35. Winslow JL, Trainer TD, Colletti RB (2001) Collagenous gastritis: a long-term follow-up with the development of endocrine cell hyperplasia, intestinal metaplasia, and epithelial changes indeterminate for dysplasia. Am J Clin Pathol 116:753–758. https://doi.org/10.1309/3WM2-THU3-3Q2A-DP47

    Article  PubMed  CAS  Google Scholar 

  36. Bajwa RU, Joshi A, Heikenen JB (2015) Successful treatment of collagenous gastritis in a child with a gluten-free diet. WMJ 114:271–273

    PubMed  Google Scholar 

  37. Venerito M, Varbanova M, Rohl FW, Reinhold D, Frauenschlager K, Jechorek D, Weigt J, Link A, Malfertheiner P (2016) Oxyntic gastric atrophy in Helicobacter pylori gastritis is distinct from autoimmune gastritis. J Clin Pathol 69:677–685. https://doi.org/10.1136/jclinpath-2015-203405

    Article  PubMed  CAS  Google Scholar 

  38. Antico A, Tampoia M, Villalta D, Tonutti E, Tozzoli R, Bizzaro N (2012) Clinical usefulness of the serological gastric biopsy for the diagnosis of chronic autoimmune gastritis. Clin Dev Immunol 2012:520970. https://doi.org/10.1155/2012/520970

    Article  PubMed  PubMed Central  Google Scholar 

  39. Pittman ME, Voltaggio L, Bhaijee F, Robertson SA, Montgomery EA (2015) Autoimmune metaplastic atrophic gastritis: recognizing precursor lesions for appropriate patient evaluation. Am J Surg Pathol 39:1611–1620. https://doi.org/10.1097/PAS.0000000000000481

    Article  PubMed  Google Scholar 

  40. Rudi J, Kolb C, Maiwald M, Zuna I, von Herbay A, Galle PR, Stremmel W (1997) Serum antibodies against Helicobacter pylori proteins VacA and CagA are associated with increased risk for gastric adenocarcinoma. Dig Dis Sci 42:1652–1659

  41. Ekstrom AM, Held M, Hansson LE, Engstrand L, Nyren O (2001) Helicobacter pylori in gastric cancer established by CagA immunoblot as a marker of past infection. Gastroenterology 121:784–791

    Article  CAS  PubMed  Google Scholar 

  42. El-Zimaity HM, Ota H, Graham DY, Akamatsu T, Katsuyama T (2002) Patterns of gastric atrophy in intestinal type gastric carcinoma. Cancer 94:1428–1436

    Article  PubMed  Google Scholar 

  43. Shiotani A, Katsumata R, Gouda K, Fukushima S, Nakato R, Murao T, Ishii M, Fujita M, Matsumoto H, Sakakibara T (2018) Hypergastrinemia in long-term use of proton pump inhibitors. Digestion 97:154–162. https://doi.org/10.1159/000484688

    Article  PubMed  CAS  Google Scholar 

  44. Bektas M, Sarac N, Cetinkaya H, Toruner M, Erdemli E, Keskin O, Soykan I, Oktay EI, Korkut E, Ustun Y, Bahar K (2012) Effects of Helicobacter pylori infection and long-term proton pump inhibitor use on enterochromaffin-like cells. Ann Gastroenterol 25:123–127

    PubMed  PubMed Central  Google Scholar 

  45. Grin A, Kim YI, Mustard R, Streutker CJ, Riddell RH (2012) Duodenal gastrinoma with multiple gastric neuroendocrine tumors secondary to chronic Helicobacter pylori gastritis. Am J Surg Pathol 36:935–940. https://doi.org/10.1097/PAS.0b013e31824babc2

    Article  PubMed  Google Scholar 

  46. Davidson RJ, Atrah HI, Sewell HF (1989) Longitudinal study of circulating gastric antibodies in pernicious anaemia. J Clin Pathol 42:1092–1095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Rose MS, Chanarin I (1969) Dissociation of intrinsic factor from its antibody: application to study of pernicious anaemia gastric juice specimens. Br Med J 1:468–470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Zafad S, Madani A, Harif M, Quessar A, Benchekroun S (2007) Pernicious anemia associated with autoimmune hemolytic anemia and alopecia areata. Pediatr Blood Cancer 49:1017–1018. https://doi.org/10.1002/pbc.20896

    Article  PubMed  Google Scholar 

  49. Dahshan A, Poulick J, Tolia V (2001) Special feature: pathological case of the month. Pernicious anemia and gastric atrophy in an adolescent female with multiorgan problems. Arch Pediatr Adolesc Med 155:609–610

    Article  CAS  PubMed  Google Scholar 

  50. Guilloteau M, Bertrand Y, Lachaux A, Mialou V, Le Gall C, Girard S (2007) [Pernicious anemia: a teenager with an unusual cause of iron-deficiency anemia]. Gastroenterol Clin Biol 31:1155–1156

  51. Vorobjova T, Maaroos HI, Uibo R (2008) Immune response to Helicobacter pylori and its association with the dynamics of chronic gastritis in the antrum and corpus. APMIS 116:465–476

    Article  CAS  PubMed  Google Scholar 

  52. De Re V, Repetto O, Zanussi S, Casarotto M, Caggiari L, Canzonieri V, Cannizzaro R (2017) Protein signature characterizing Helicobacter pylori strains of patients with autoimmune atrophic gastritis, duodenal ulcer and gastric cancer. Infect Agent Cancer 12:22. https://doi.org/10.1186/s13027-017-0133-x

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. Yamaguchi E, Iwasa T, Ihara E, Tomita Y, Aso A, Oki E, Nakano K, Hirahashi M, Nakamura K (2017) Gastric neuroendocrine tumor with hypergastrinemia following type B chronic atrophic gastritis: a case report. Nihon Shokakibyo Gakkai Zasshi 114:248–255. https://doi.org/10.11405/nisshoshi.114.248

    Article  PubMed  Google Scholar 

  54. Bettington M, Brown I (2013) Autoimmune gastritis: novel clues to histological diagnosis. Pathology 45:145–149. https://doi.org/10.1097/PAT.0b013e32835cc22c

    Article  PubMed  CAS  Google Scholar 

  55. Zhang H, Jin Z, Cui R, Ding S, Huang Y, Zhou L (2017) Autoimmune metaplastic atrophic gastritis in chinese: a study of 320 patients at a large tertiary medical center. Scand J Gastroenterol 52:150–156. https://doi.org/10.1080/00365521.2016.1236397

    Article  PubMed  CAS  Google Scholar 

  56. Jhala NC, Montemor M, Jhala D, Lu L, Talley L, Haber MM, Lechago J (2003) Pancreatic acinar cell metaplasia in autoimmune gastritis. Arch Pathol Lab Med 127:854–857. https://doi.org/10.1043/1543-2165(2003)127<854:PACMIA>2.0.CO;2

    Article  PubMed  Google Scholar 

  57. Chlumska A, Boudova L, Benes Z, Zamecnik M (2005) Autoimmune gastritis. A clinicopathologic study of 25 cases. Cesk Patol 41:137–142

    PubMed  CAS  Google Scholar 

  58. Kekki M, Samloff IM, Varis K, Ihamaki T (1991) Serum pepsinogen I and serum gastrin in the screening of severe atrophic corpus gastritis. Scand J Gastroenterol Suppl 186:109–116

    Article  CAS  PubMed  Google Scholar 

  59. Ruiz AR Jr, Borum ML (2001) Cytomegalovirus hemorrhagic gastritis. AIDS Patient Care STDs 15:1–5. https://doi.org/10.1089/108729101460047

    Article  PubMed  Google Scholar 

  60. Henson D (1972) Cytomegalovirus inclusion bodies in the gastrointestinal tract. Arch Pathol 93:477–482

    PubMed  CAS  Google Scholar 

  61. Strayer DS, Phillips GB, Barker KH, Winokur T, DeSchryver-Kecskemeti K (1981) Gastric cytomegalovirus infection in bone marrow transplant patients: an indication of generalized disease. Cancer 48:1478–1483

    Article  CAS  PubMed  Google Scholar 

  62. Eisenstat DD, Griffiths AM, Cutz E, Petric M, Drumm B (1995) Acute cytomegalovirus infection in a child with Menetrier’s disease. Gastroenterology 109:592–595

    Article  CAS  PubMed  Google Scholar 

  63. Lauwers GY, Fujita H, Nagata K, Shimizu M (2010) Pathology of non-Helicobacter pylori gastritis: extending the histopathologic horizons. J Gastroenterol 45:131–145. https://doi.org/10.1007/s00535-009-0146-3

    Article  PubMed  Google Scholar 

  64. Nohr EW, Itani DM, Andrews CN, Kelly MM (2017) Varicella-Zoster virus gastritis: case report and review of the literature. Int J Surg Pathol 25:449–452. https://doi.org/10.1177/1066896917696751

    Article  PubMed  Google Scholar 

  65. Walker C, Huber-Schumacher S, Boettler T, Thimme R, Fischer A (2016) A rare cause of upper GI bleeding in a critically ill patient. Gut 65:1438. https://doi.org/10.1136/gutjnl-2015-310564

    Article  PubMed  Google Scholar 

  66. Peixoto A, Santos-Antunes J, Silva M, Macedo G (2016) Esophageal and gastric ulceration due to synchronous herpes simplex virus, cytomegalovirus and Epstein-Barr virus infection. Acta Gastroenterol Belg 79:271–272

    PubMed  CAS  Google Scholar 

  67. Jun DW, Kim DH, Kim SH, Song MH, Lee HH, Kim SH, Jo YJ, Park YS (2007) Menetrier’s disease associated with herpes infection: response to treatment with acyclovir. Gastrointest Endosc 65:1092–1095. https://doi.org/10.1016/j.gie.2006.11.003

    Article  PubMed  Google Scholar 

  68. Chen ZM, Shah R, Zuckerman GR, Wang HL (2007) Epstein-Barr virus gastritis: an underrecognized form of severe gastritis simulating gastric lymphoma. Am J Surg Pathol 31:1446–1451. https://doi.org/10.1097/PAS.0b013e318050072f

    Article  PubMed  Google Scholar 

  69. Owens SR, Walls A, Krasinskas AM, Rund CR (2011) Epstein-Barr virus gastritis: rare or rarely sampled? A case report. Int J Surg Pathol 19:196–198. https://doi.org/10.1177/1066896908316905

    Article  PubMed  Google Scholar 

  70. Haesebrouck F, Pasmans F, Flahou B, Chiers K, Baele M, Meyns T, Decostere A, Ducatelle R (2009) Gastric helicobacters in domestic animals and nonhuman primates and their significance for human health. Clin Microbiol Rev 22:202-223, Table of Contents. doi: https://doi.org/10.1128/CMR.00041-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. De Witte C, Schulz C, Smet A, Malfertheiner P, Haesebrouck F (2016) Other helicobacters and gastric microbiota. Helicobacter 21 Suppl 1:62–68. doi: https://doi.org/10.1111/hel.12343

    Article  CAS  PubMed  Google Scholar 

  72. Okamura T, Iwaya Y, Yokosawa S, Suga T, Arakura N, Matsumoto T, Ogiwara N, Higuchi K, Ota H, Tanaka E (2013) A case of Helicobacter heilmannii-associated primary gastric mucosa-associated lymphoid tissue lymphoma achieving complete remission after eradication. Clin J Gastroenterol 6:38–45. https://doi.org/10.1007/s12328-012-0355-9

    Article  PubMed  Google Scholar 

  73. Kobayashi M, Yamamoto K, Ogiwara N, Matsumoto T, Shigeto S, Ota H (2016) Helicobacter heilmannii-like organism in parietal cells: a diagnostic pitfall. Pathol Int 66:120–122. https://doi.org/10.1111/pin.12349

    Article  PubMed  Google Scholar 

  74. Greenstein DB, Wilcox CM, Schwartz DA (1994) Gastric syphilis. Report of seven cases and review of the literature. J Clin Gastroenterol 18:4–9

    Article  CAS  PubMed  Google Scholar 

  75. Lee BS, Kim SM, Seong JK, Kim SH, Jeong HY, Lee HY, Song KS, Kang DY, Noh SM, Shin KS, Cho JS (2005) Phlegmonous gastritis after endoscopic mucosal resection. Endoscopy 37:490–493. https://doi.org/10.1055/s-2005-861254

    Article  PubMed  CAS  Google Scholar 

  76. Kim GY, Ward J, Henessey B, Peji J, Godell C, Desta H, Arlin S, Tzagournis J, Thomas F (2005) Phlegmonous gastritis: case report and review. Gastrointest Endosc 61:168–174

    Article  PubMed  Google Scholar 

  77. Huang CT, Liao WY (2009) Emphysematous gastritis: a deadly infectious disease. Scand J Infect Dis 41:317–319. https://doi.org/10.1080/00365540902744774

    Article  PubMed  Google Scholar 

  78. Takano Y, Yamamura E, Gomi K, Tohata M, Endo T, Suzuki R, Hayashi M, Nakanishi T, Hanamura S, Asonuma K, Ino S, Kuroki Y, Maruoka N, Nagahama M, Inoue K, Takahashi H (2015) Successful conservative treatment of emphysematous gastritis. Intern Med 54:195–198. https://doi.org/10.2169/internalmedicine.54.3337

    Article  PubMed  Google Scholar 

  79. Allan K, Barriga J, Afshani M, Davila R, Tombazzi C (2005) Emphysematous gastritis. Am J Med Sci 329:205–207

    Article  PubMed  Google Scholar 

  80. Srivastava A, Lauwers GY (2007) Pathology of non-infective gastritis. Histopathology 50:15–29. https://doi.org/10.1111/j.1365-2559.2006.02553.x

    Article  PubMed  CAS  Google Scholar 

  81. Pulimood AB, Amarapurkar DN, Ghoshal U, Phillip M, Pai CG, Reddy DN, Nagi B, Ramakrishna BS (2011) Differentiation of Crohn’s disease from intestinal tuberculosis in India in 2010. World J Gastroenterol 17:433–443. https://doi.org/10.3748/wjg.v17.i4.433

    Article  PubMed  PubMed Central  Google Scholar 

  82. Washington K, Gottfried MR, Wilson ML (1991) Gastrointestinal cryptococcosis. Mod Pathol 4:707–711

    PubMed  CAS  Google Scholar 

  83. Polydorides AD (2014) Pathology and differential diagnosis of chronic, noninfectious gastritis. Semin Diagn Pathol 31:114–123. https://doi.org/10.1053/j.semdp.2014.02.008

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  85. McHugh JB, Gopal P, Greenson JK (2013) The clinical significance of focally enhanced gastritis in children. Am J Surg Pathol 37:295–299. https://doi.org/10.1097/PAS.0b013e31826b2a94

    Article  PubMed  Google Scholar 

  86. Magro F, Langner C, Driessen A, Ensari A, Geboes K, Mantzaris GJ, Villanacci V, Becheanu G, Borralho Nunes P, Cathomas G, Fries W, Jouret-Mourin A, Mescoli C, de Petris G, Rubio CA, Shepherd NA, Vieth M, Eliakim R, European Society of P, European Cs, Colitis O (2013) European consensus on the histopathology of inflammatory bowel disease. J Crohns Colitis 7:827–851. https://doi.org/10.1016/j.crohns.2013.06.001

    Article  PubMed  CAS  Google Scholar 

  87. Sharif F, McDermott M, Dillon M, Drumm B, Rowland M, Imrie C, Kelleher S, Harty S, Bourke B (2002) Focally enhanced gastritis in children with Crohn’s disease and ulcerative colitis. Am J Gastroenterol 97:1415–1420. https://doi.org/10.1111/j.1572-0241.2002.05785.x

    Article  PubMed  CAS  Google Scholar 

  88. Ectors NL, Dixon MF, Geboes KJ, Rutgeerts PJ, Desmet VJ, Vantrappen GR (1993) Granulomatous gastritis: a morphological and diagnostic approach. Histopathology 23:55–61

    Article  CAS  PubMed  Google Scholar 

  89. Shapiro JL, Goldblum JR, Petras RE (1996) A clinicopathologic study of 42 patients with granulomatous gastritis. Is there really an “idiopathic” granulomatous gastritis? Am J Surg Pathol 20:462–470

    Article  CAS  PubMed  Google Scholar 

  90. North American Society for Pediatric Gastroenterology H, Nutrition, Colitis Foundation of A, Bousvaros A, Antonioli DA, Colletti RB, Dubinsky MC, Glickman JN, Gold BD, Griffiths AM, Jevon GP, Higuchi LM, Hyams JS, Kirschner BS, Kugathasan S, Baldassano RN, Russo PA (2007) Differentiating ulcerative colitis from Crohn’s disease in children and young adults: report of a working group of the North American Society for Pediatric Gastroenterology, Hepatology, and Nutrition and the Crohn’s and Colitis Foundation of America. J Pediatr Gastroenterol Nutr 44:653–674. https://doi.org/10.1097/MPG.0b013e31805563f3

    Article  Google Scholar 

  91. Kaneki T, Koizumi T, Yamamoto H, Yamaguchi S, Hachiya T, Kubo K, Honda T, Katsuyama T, Fujimori C (2001) Gastric sarcoidosis—a single polypoid appearance in the involvement. Hepatogastroenterology 48:1209–1210

    PubMed  CAS  Google Scholar 

  92. Collins MH (2009) Histopathology associated with eosinophilic gastrointestinal diseases. Immunol Allergy Clin N Am 29:109–117, x-xi. doi: https://doi.org/10.1016/j.iac.2008.10.005

    Article  PubMed  Google Scholar 

  93. Cianferoni A, Spergel JM (2015) Eosinophilic esophagitis and gastroenteritis. Curr Allergy Asthma Rep 15:58. https://doi.org/10.1007/s11882-015-0558-5

    Article  PubMed  CAS  Google Scholar 

  94. Rothenberg ME (2004) Eosinophilic gastrointestinal disorders (EGID). J Allergy Clin Immunol 113:11–28; quiz 29. https://doi.org/10.1016/j.jaci.2003.10.047

    Article  PubMed  CAS  Google Scholar 

  95. Johnstone JM, Morson BC (1978) Eosinophilic gastroenteritis. Histopathology 2:335–348

    Article  CAS  PubMed  Google Scholar 

  96. Goldman H, Proujansky R (1986) Allergic proctitis and gastroenteritis in children. Clinical and mucosal biopsy features in 53 cases. Am J Surg Pathol 10:75–86

    Article  CAS  PubMed  Google Scholar 

  97. Papadopoulos AA, Tzathas C, Polymeros D, Ladas SD (2005) Symptomatic eosinophilic gastritis cured with Helicobacter pylori eradication. Gut 54:1822. https://doi.org/10.1136/gut.2005.075077

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  98. Seve P, Stankovic K, Michalet V, Vial T, Scoazec JY, Broussolle C (2005) Carbimazole induced eosinophilic granulomatous vasculitis localized to the stomach. J Intern Med 258:191–195. https://doi.org/10.1111/j.1365-2796.2005.01525.x

    Article  PubMed  CAS  Google Scholar 

  99. Weisdorf DJ, Snover DC, Haake R, Miller WJ, McGlave PB, Blazar B, Ramsay NK, Kersey JH, Filipovich A (1990) Acute upper gastrointestinal graft-versus-host disease: clinical significance and response to immunosuppressive therapy. Blood 76:624–629

    PubMed  CAS  Google Scholar 

  100. Washington K, Bentley RC, Green A, Olson J, Treem WR, Krigman HR (1997) Gastric graft-versus-host disease: a blinded histologic study. Am J Surg Pathol 21:1037–1046

    Article  CAS  PubMed  Google Scholar 

  101. Snover DC, Weisdorf SA, Vercellotti GM, Rank B, Hutton S, McGlave P (1985) A histopathologic study of gastric and small intestinal graft-versus-host disease following allogeneic bone marrow transplantation. Hum Pathol 16:387–392

    Article  CAS  PubMed  Google Scholar 

  102. Shulman HM, Cardona DM, Greenson JK, Hingorani S, Horn T, Huber E, Kreft A, Longerich T, Morton T, Myerson D, Prieto VG, Rosenberg A, Treister N, Washington K, Ziemer M, Pavletic SZ, Lee SJ, Flowers ME, Schultz KR, Jagasia M, Martin PJ, Vogelsang GB, Kleiner DE (2015) NIH consensus development project on criteria for clinical trials in chronic graft-versus-host disease: II. The 2014 Pathology Working Group Report. Biol Blood Marrow Transplant 21:589–603. https://doi.org/10.1016/j.bbmt.2014.12.031

    Article  PubMed  PubMed Central  Google Scholar 

  103. El-Zimaity HM, Genta RM, Graham DY (1996) Histological features do not define NSAID-induced gastritis. Hum Pathol 27:1348–1354

    Article  CAS  PubMed  Google Scholar 

  104. Dixon MF, O'Connor HJ, Axon AT, King RF, Johnston D (1986) Reflux gastritis: distinct histopathological entity? J Clin Pathol 39:524–530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Affolter K, Samowitz W, Boynton K, Kelly ED (2017) Doxycycline-induced gastrointestinal injury. Hum Pathol 66:212–215. https://doi.org/10.1016/j.humpath.2017.02.011

    Article  PubMed  CAS  Google Scholar 

  106. Vieth M, Montgomery E (2017) Medication-associated gastrointestinal tract injury. Virchows Arch 470:245–266. https://doi.org/10.1007/s00428-017-2077-3

    Article  PubMed  CAS  Google Scholar 

  107. Leber A, Stal J (2012) Simultaneous esophageal and gastric ulceration due to doxycycline ingestion: case report and review of the literature gastroenterology. Res 5:236–238. https://doi.org/10.4021/gr498w

    Article  Google Scholar 

  108. Jy C, Brown I, Conway L, Singh M (2016) Doxycycline induced gastritis and oesophageal ulcer. Pathology:48

  109. Poley JW, Steyerberg EW, Kuipers EJ, Dees J, Hartmans R, Tilanus HW, Siersema PD (2004) Ingestion of acid and alkaline agents: outcome and prognostic value of early upper endoscopy. Gastrointest Endosc 60:372–377

    Article  PubMed  Google Scholar 

  110. Garcia Diaz E, Castro Fernandez M, Romero Gomez M, Castilla Higuero L (2001) Upper gastrointestinal tract injury caused by ingestion of caustic substances. Gastroenterol Hepatol 24:191–195

    Article  CAS  PubMed  Google Scholar 

  111. Iacobuzio-Donahue CA, Lee EL, Abraham SC, Yardley JH, Wu TT (2001) Colchicine toxicity: distinct morphologic findings in gastrointestinal biopsies. Am J Surg Pathol 25:1067–1073

    Article  CAS  PubMed  Google Scholar 

  112. Parfitt JR, Driman DK (2007) Pathological effects of drugs on the gastrointestinal tract: a review. Hum Pathol 38:527–536. https://doi.org/10.1016/j.humpath.2007.01.014

    Article  PubMed  CAS  Google Scholar 

  113. Hruban RH, Yardley JH, Donehower RC, Boitnott JK (1989) Taxol toxicity. Epithelial necrosis in the gastrointestinal tract associated with polymerized microtubule accumulation and mitotic arrest. Cancer 63:1944–1950

    Article  CAS  PubMed  Google Scholar 

  114. Abraham SC, Yardley JH, Wu TT (1999) Erosive injury to the upper gastrointestinal tract in patients receiving iron medication: an underrecognized entity. Am J Surg Pathol 23:1241–1247

    Article  CAS  PubMed  Google Scholar 

  115. Marginean EC, Bennick M, Cyczk J, Robert ME, Jain D (2006) Gastric siderosis: patterns and significance. Am J Surg Pathol 30:514–520

    Article  PubMed  Google Scholar 

  116. Greenson JK, Trinidad SB, Pfeil SA, Brainard JA, McBride PT, Colijn HO, Tesi RJ, Lucas JG (1993) Gastric mucosal calcinosis. Calcified aluminum phosphate deposits secondary to aluminum-containing antacids or sucralfate therapy in organ transplant patients. Am J Surg Pathol 17:45–50

    Article  CAS  PubMed  Google Scholar 

  117. Matsukuma K, Gui D, Olson KA, Tejaswi S, Clayton EF, Thai A (2016) OsmoPrep-associated gastritis: a histopathologic mimic of iron pill gastritis and mucosal calcinosis. Am J Surg Pathol 40:1550–1556. https://doi.org/10.1097/PAS.0000000000000706

    Article  PubMed  PubMed Central  Google Scholar 

  118. Goto K, Ogawa K (2016) Lanthanum deposition is frequently observed in the gastric mucosa of dialysis patients with lanthanum carbonate therapy: a clinicopathologic study of 13 cases, including 1 case of lanthanum granuloma in the colon and 2 nongranulomatous gastric cases. Int J Surg Pathol 24:89–92. https://doi.org/10.1177/1066896915613434

    Article  PubMed  CAS  Google Scholar 

  119. Makino M, Kawaguchi K, Shimojo H, Nakamura H, Nagasawa M, Kodama R (2015) Extensive lanthanum deposition in the gastric mucosa: the first histopathological report. Pathol Int 65:33–37. https://doi.org/10.1111/pin.12227

    Article  PubMed  CAS  Google Scholar 

  120. Abraham SC, Bhagavan BS, Lee LA, Rashid A, Wu TT (2001) Upper gastrointestinal tract injury in patients receiving kayexalate (sodium polystyrene sulfonate) in sorbitol: clinical, endoscopic, and histopathologic findings. Am J Surg Pathol 25:637–644

    Article  CAS  PubMed  Google Scholar 

  121. Genta RM, Sonnenberg A (2015) Helicobacter-negative gastritis: a distinct entity unrelated to Helicobacter pylori infection. Aliment Pharmacol Ther 41:218–226. https://doi.org/10.1111/apt.13007

    Article  PubMed  CAS  Google Scholar 

  122. Shiota S, Thrift AP, Green L, Shah R, Verstovsek G, Rugge M, Graham DY, El-Serag HB (2017) Clinical manifestations of Helicobacter pylori-negative gastritis. Clin Gastroenterol Hepatol 15:1037–1046.e3. https://doi.org/10.1016/j.cgh.2017.01.006

    Article  PubMed  Google Scholar 

  123. Nordenstedt H, Graham DY, Kramer JR, Rugge M, Verstovsek G, Fitzgerald S, Alsarraj A, Shaib Y, Velez ME, Abraham N, Anand B, Cole R, El-Serag HB (2013) Helicobacter pylori-negative gastritis: prevalence and risk factors. Am J Gastroenterol 108:65–71. https://doi.org/10.1038/ajg.2012.372

    Article  PubMed  CAS  Google Scholar 

  124. Broide E, Richter V, Mendlovic S, Shalem T, Eindor-Abarbanel A, Moss SF, Shirin H (2017) Lymphoid follicles in children with Helicobacter pylori-negative gastritis. Clin Exp Gastroenterol 10:195–201. https://doi.org/10.2147/CEG.S133421

    Article  PubMed  PubMed Central  Google Scholar 

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El-Zimaity, H., Choi, WT., Lauwers, G.Y. et al. The differential diagnosis of Helicobacter pylori negative gastritis. Virchows Arch 473, 533–550 (2018). https://doi.org/10.1007/s00428-018-2454-6

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