J Korean Med Sci.  2007 Feb;22(1):63-69. 10.3346/jkms.2007.22.1.63.

Helicobacter heilmannii-associated Gastritis: Clinicopathologic Findings and Comparison with Helicobacter pylori-associated Gastritis

• Joo M
• Kwak JE
• Chang SH
• Kim H
• Chi JG
• Kim KA
• Yang JH
• Lee JS
• Moon YS
• Kim KM

• KMID: 1713231
• DOI: http://doi.org/10.3346/jkms.2007.22.1.63

Abstract

The aims of this study were to evaluate the clinicopathologic features of Helicobacter heilmannii-associated gastritis and to compare H. heilmannii-associated gastritis with H. pylori-associated gastritis. We reviewed 5,985 consecutive gastric biopsy specimens. All cases of chronic gastritis with Helicobacter infection were evaluated with the Updated Sydney System, and the grades of all gastritis variables were compared between H. heilmannii-associated gastritis and H. pylori-associated gastritis groups. There were 10 cases of H. heilmannii-associated gastritis (0.17%) and 3,285 cases of H. pylori-associated gastritis (54.9%). The organisms were superficially located within the mucous layer without adhesion to epithelial cells. Interestingly, in one case many intracytoplasmic H. heilmannii organisms were observed in parietal cells with cell damage. A case of low-grade mucosa-associated lymphoid tissue (MALT) lymphoma concomitant with H. heilmannii infection was detected. Compared to H. pylori-associated gastritis, H. heilmannii-associated gastritis showed less severe neutrophilic activity (p<0.0001), mononuclear cell infiltration (p=0.0029), and endoscopic findings of chronic gastritis devoid of erosion or ulcer (p=0.0309). In conclusion, we present the detailed clinicopathologic findings of H. heilmanniiassociated gastritis compared to H. pylori-associated gastritis. H. heilmannii-associated gastritis is uncommon and milder than H. pylori-associated gastritis, however it may be noteworthy with respect to the development of MALT lymphoma.

Keyword

Helicobacter heilmannii; Helicobacter pylori; Gastritis; Lymphoma, Mucosa-Associated Lymphoid Tissue; Parietal Cells, Gastric

MeSH Terms

Stomach Neoplasms/etiology/pathology
Middle Aged
Male
Lymphoma, Mucosa-Associated Lymphoid Tissue/etiology/pathology
Humans
*Helicobacter pylori
*Helicobacter heilmannii
Helicobacter Infections/*pathology
Gastritis/*pathology
Female
Adult

Figure

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  Fig. 1 Gastrofiberscopic findings. (A) An active ulcer is noted in the body of the patient with H. pylori-associated gastritis. (B) Mild mucosal hyperemia is noted in the antrum of the patient with H. heilmannii-associated gastritis.

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  Fig. 2 H. heilmannii-associated gastritis. (A) The antral mucosa shows mild chronic gastritis with minimal neutrophilic activity (hematoxylineosin, ×100). (B) Neutrophilic infiltration and surface epithelial changes are mild in H. heilmannii-associated gastritis with high Helicobacter density, in contrast to H. pylori-associated gastritis showing dense neutrophilic infiltration into the epithelia and surface epithelial damage (C) (hematoxylin-eosin, ×400). (D) Many corkscrew-shaped spiral organisms are noted within the mucous adjacent to the gastric foveolar epithelia (hematoxylin-eosin, ×1,000). They show a cross-reaction for H. pylori immunostaining (inset). (E) Spiral organisms within a parietal cell demonstrate intact morphology and surrounding vacuole-like spaces (hematoxylin-eosin, ×1,000). (F) Parietal cells harboring organisms show degenerative change with neutrophilic infiltration (hematoxylin-eosin, ×1,000).

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  Fig. 3 H. heilmannii-associated gastric MALT lymphoma. (A) Low magnification view reveals extensive lymphocytic infiltration (hematoxylineosin, ×100) with an asterisk indicating areas of (B) and (C), and an inset representing (D) area. (B) Lymphomatous infiltrations form destructive lymphoepithelial lesions (LELs) (hematoxylin-eosin, ×400). (C) Cytokeratin immunostain highlights the remaining epithelial remnant in LELs (×400). (D) Many spiral organisms are present in the adjacent gastric pit of this case (Giemsa stain, ×1,000).

Reference

1. Marshall BJ. Helicobacter pylori. Am J Gastroenterol. 1994. 89:116–128.

2. Kuipers EJ. Helicobacter pylori and the risk and management of associated diseases: gastritis, ulcer disease, atrophic gastritis and gastric cancer. Aliment Pharmacol Ther. 1997. 11:71–88.

3. Nakamura S, Yao T, Aoyagi K, Iida M, Fujishima M, Tsuneyoshi M. Helicobacter pylori and primary gastric lymphoma. A histopathologic and immunohistochemical analysis of 237 patients. Cancer. 1997. 79:3–11.

4. Isaacson PG. Gastric MALT lymphoma: from concept to cure. Ann Oncol. 1999. 10:637–645.

5. Heilmann KL, Borchard F. Gastritis due to spiral shaped bacteria other than Helicobacter pylori: clinical, histological, and ultrastructural findings. Gut. 1991. 32:137–140.

6. Hilzenrat N, Lamoureux E, Weintrub I, Alpert E, Lichter M, Alpert L. Helicobacter heilmannii-like spiral bacteria in gastric mucosal biopsies. Prevalence and clinical significance. Arch Pathol Lab Med. 1995. 119:1149–1153.

7. Holck S, Ingeholm P, Blom J, Norgaard A, Elsborg L, Adamsen S, Andersen LP. The histopathology of human gastric mucosa inhabited by Helicobacter heilmannii-like (Gastrospirillum hominis) organisms, including the first culturable case. APMIS. 1997. 105:746–756.

8. Stolte M, Kroher G, Meining A, Morgner A, Bayerdorffer E, Bethke B. A comparison of Helicobacter pylori and Helicobacter heilmannii gastritis. A matched control study involving 404 patients. Scand J Gastroenterol. 1997. 32:28–33.

9. Ierardi E, Monno RA, Gentile A, Francavilla R, Burattini O, Marangi S, Pollice L, Francavilla A. Helicobacter heilmannii gastritis: a histological and immunohistochemical trait. J Clin Pathol. 2001. 54:774–777.

10. Jhala D, Jhala N, Lechago J, Haber M. Helicobacter heilmannii gastritis: association with acid peptic diseases and comparison with Helicobacter pylori gastritis. Mod Pathol. 1999. 12:534–538.

11. Stolte M, Wellens E, Bethke B, Ritter M, Eidt H. Helicobacter heilmannii (formerly Gastrospirillum hominis) gastritis: an infection transmitted by animals? Scand J Gastroenterol. 1994. 29:1061–1064.

12. Okiyama Y, Matsuzawa K, Hidaka E, Sano K, Akamatsu T, Ota H. Helicobcater heilmannii infection: Clinical, endoscopic and histological features in Japanese patients. Pathol Int. 2005. 55:398–404.

13. Lee YE, Kim HS, Lee SK, Lee HT, Lee YJ, Bae CY. Prevalence and risk factors of Helicobacter pylori infection in general population. J Korean Acad Fam Med. 1999. 20:186–193.

14. Dixon MF, Genta RM, Yardley JH, Correa P. Classification and grading of gastritis. The updated Sydney System. International Workshop on the Histopathology of Gastritis, Houston 1994. Am J Surg Pathol. 1996. 20:1161–1181.

15. Seo WJ, Park CS, Cho YJ, Cha KW, Lee SW, Lim ST, Sung YH, Baek AR. A case of gastric ulcer induced by Helicobacter heilmannii-like organism. Korean J Gastroenterol. 2003. 42:63–66.

16. Priestnall SL, Wiinberg B, Spohr A, Neuhaus B, Kuffer M, Wiedmann M, Simpson KW. Evaluation of "Helicobacter heilmannii" subtypes in the gastric mucosas of cats and dogs. J Clin Microbiol. 2004. 42:2144–2151.

17. Sobala GM, Crabtree JE, Dixon MF, Schorah CJ, Taylor JD, Rathbone BJ, Heatley RV, Axon AT. Acute Helicobacter pylori infection: clinical features, local and systemic immune response, gastric mucosal histology, and gastric juice ascorbic acid concentrations. Gut. 1991. 32:1415–1418.

18. Dubois A, Tarnawski A, Newell DG, Fiala N, Dabros W, Stachura J, Krivan H, Heman-Ackah LM. Gastric injury and invasion of parietal cells by spiral bacteria in rhesus monkeys. Are gastritis and hyperchlorhydria infectious diseases? Gastroenterology. 1991. 100:884–891.

19. Dye KR, Marshall BJ, Frierson HF Jr, Guerrant RL, McCallum RW. Ultrastructure of another spiral organism associated with human gastritis. Dig Dis Sci. 1989. 34:1787–1791.

20. Rollason TP, Stone J, Rhodes JM. Spiral organisms in endoscopic biopsies of the human stomach. J Clin Pathol. 1984. 37:23–26.

21. Wotherspoon AC, Ortiz-Hidalgo C, Falzon MR, Isaacson PG. Helicobacter pylori-associated gastritis and primary B-cell gastric lymphoma. Lancet. 1991. 338:1175–1176.

22. O'Rourke JL, Dixon MF, Jack A, Enno A, Lee A. Gastric B-cell mucosa-associated lymphoid tissue (MALT) lymphoma in an animal model of "Helicobacter heilmannii" infection. J Pathol. 2004. 203:896–903.

23. Morgner A, Lehn N, Andersen LP, Thiede C, Bennedsen M, Trebesius K, Neubauer B, Neubauer A, Stolte M, Bayerdorffer E. Helicobacter heilmannii-associated primary gastric low-grade MALT lymphoma: complete remission after curing the infection. Gastroenterology. 2000. 118:821–828.

24. Thomas-Marques L, Yaziji N, Bouche O, Diebold MD, Cadiot G, Thiefin G. Helicobacter heilmannii-associated low-grade gastric MALT lymphoma: a new case of complete remission after eradication. Gastroenterol Clin Biol. 2005. 29:476–477.

25. Regimbeau C, Karsenti D, Durand V, D'Alteroche L, Copie-Bergman C, Metman EH, Machet MC. Low-grade gastric MALT lymphoma and Helicobacter heilmannii (Gastrospirillum hominis). Gastroenterol Clin Biol. 1998. 22:720–723.