Abstract
A 46-year-old man underwent gastrointestinal endoscopy while visiting the hospital for a general physical check-up. Coarse mucosa in the antrum with superficial erosions was found by endoscopic gastrointestinal examination, but no atrophic changes were seen in the corpus. Histopathological examination of gastric biopsy specimens revealed mucosa-associated lymphoid tissue (MALT) lymphoma. Although Helicobacter pylori was not detected in our patient, H. heilmannii was identified histologically and by polymerase chain reaction analysis, resulting in the diagnosis of H. heilmannii-associated gastric MALT lymphoma. We successfully eradicated H. heilmannii and achieved complete remission of gastric MALT lymphoma by antibiotic therapy. H. heilmannii usually causes milder gastritis than H. pylori, but it has been more closely associated with MALT lymphoma. As such, when H. pylori infection is excluded in patients with gastric MALT lymphoma, physicians should next consider the possibility of H. heilmannii. Furthermore, our research suggests that eradication therapy is effective for treatment of localized H. heilmannii-associated gastric MALT lymphoma.
Similar content being viewed by others
References
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;29:1061–4.
O’Rourke JL, Solnick JV, Neilan BA, Seidel K, Hayter R, Hansen LM, et al. Description of ‘Candidatus Helicobacter heilmannii’ based on DNA sequence analysis of 16S rRNA and urease genes. Int J Syst Evol Microbiol. 2004;54:2203–11.
Matsumoto T, Kawakubo M, Shiohara M, Kumagai T, Hidaka E, Yamauchi K, et al. Phylogeny of a novel “Helicobacter heilmannii” organism from a Japanese patient with chronic gastritis based on DNA sequence analysis of 16S rRNA and urease genes. J Microbiol. 2009;47:201–7.
Ierardi E, Monno RA, Gentile A, Francavilla R, Burattini O, Marangi S, et al. Helicobacter heilmannii gastritis: a histological and immunohistochemical trait. J Clin Pathol. 2001;54:774–7.
Okiyama Y, Matsuzawa K, Hidaka E, Sano K, Akamatsu T, Ota H. Helicobacter heilmannii infection: clinical, endoscopic and histopathological features in Japanese patients. Pathol Int. 2005;55:398–404.
Joo M, Kwak JE, Chang SH, Kim H, Chi JG, Kim KA, et al. Helicobacter heilmannii-associated gastritis: clinicopathologic findings and comparison with Helicobacter pylori-associated gastritis. J Korean Med Sci. 2007;22:63–9.
Heilmann KL, Borchard F. Gastritis due to spiral shaped bacteria other than Helicobacter pylori: clinical, histological, and ultrastructural findings. Gut. 1991;32:137–40.
Svec A, Kordas P, Pavlis Z, Novotny J. High prevalence of Helicobacter heilmannii-associated gastritis in a small, predominantly rural area: further evidence in support of a zoonosis? Scand J Gastroenterol. 2000;35:925–8.
Chen Y, Zhou D, Wang J. Biological diagnostic and therapeutic study on the infection of Helicobacter heilmannii. Zhonghua Yi Xue Za Zhi. 1998;78:490–3.
Yali Z, Yamada N, Wen M, Matsuhisa T, Miki M. Gastrospirillum hominis and Helicobacter pylori infection in Thai individuals: comparison of histopathological changes of gastric mucosa. Pathol Int. 1998;48:507–11.
Goddard AF, Logan RP, Atherton JC, Jenkins D, Spiller RC. Healing of duodenal ulcer after eradication of Helicobacter heilmannii. Lancet. 1997;349:1815–6.
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;12:534–8.
Yoshimura M, Isomoto H, Shikuwa S, Osabe M, Matsunaga K, Omagari K, et al. A case of acute gastric mucosal lesions associated with Helicobacter heilmannii infection. Helicobacter. 2002;7:322–6.
Morgner A, Bayerdorffer E, Meining A, Stolte M, Kroher G. Helicobacter heilmannii and gastric cancer. Lancet. 1995;346:511–2.
Yang H, Li X, Xu Z, Zhou D. “Helicobacter heilmannii” infection in a patient with gastric cancer. Dig Dis Sci. 1995;40:1013–4.
Morgner A, Lehn N, Andersen LP, Thiede C, Bennedsen M, Trebesius K, et al. Helicobacter heilmannii-associated primary gastric low-grade MALT lymphoma: complete remission after curing the infection. Gastroenterology. 2000;118:821–8.
Stolte M, Kroher G, Meining A, Morgner A, Bayerdorffer E, Bethke B. A comparison of Helicobacter pylori and H. heilmannii gastritis. A matched control study involving 404 patients. Scand J Gastroenterol. 1997;32:28–33.
Goteri G, Ranaldi R, Rezai B, Baccarini MG, Bearzi I. Synchronous mucosa-associated lymphoid tissue lymphoma and adenocarcinoma of the stomach. Am J Surg Pathol. 1997;21:505–9.
Lister TA, Crowther D, Sutcliffe SB, Glatstein E, Canellos GP, Young RC, et al. Report of a committee convened to discuss the evaluation and staging of patients with Hodgkin’s disease: Cotswolds meeting. J Clin Oncol. 1989;7:1630–6.
Copie-Bergman C, Gaulard P, Lavergne-Slove A, Brousse N, Flejou JF, Dordonne K, et al. Proposal for a new histological grading system for post-treatment evaluation of gastric MALT lymphoma. Gut. 2003;52:1656.
Dent JC, McNulty CA, Uff JC, Wilkinson SP, Gear MW. Spiral organisms in the gastric antrum. Lancet. 1987;2:96.
Meining A, Kroher G, Stolte M. Animal reservoirs in the transmission of Helicobacter heilmannii. Results of a questionnaire-based study. Scand J Gastroenterol. 1998;33:795–8.
Chisholm SA, Owen RJ. Development and application of a novel screening PCR assay for direct detection of ‘Helicobacter heilmannii’-like organisms in human gastric biopsies in Southeast England. Diagn Microbiol Infect Dis. 2003;46:1–7.
Nakamura M, Murayama SY, Serizawa H, Sekiya Y, Eguchi M, Takahashi S, et al. “Candidatus Helicobacter heilmannii” from a cynomolgus monkey induces gastric mucosa-associated lymphoid tissue lymphomas in C57BL/6 mice. Infect Immun. 2007;75:1214–22.
Regimbeau C, Karsenti D, Durand V, D’Alteroche L, Copie-Bergman C, Metman EH, et al. Low-grade gastric MALT lymphoma and Helicobacter heilmannii (Gastrospirillum hominis]. Gastroenterol Clin Biol. 1998;22:720–3.
Holck S, Ingeholm P, Blom J, Norgaard A, Elsborg L, Adamsen S, et al. The histopathology of human gastric mucosa inhabited by Helicobacter heilmannii-like (Gastrospirillum hominis) organisms, including the first culturable case. APMIS. 1997;105:746–56.
Nakamura M, Matsui H, Takahashi T, Ogawa S, Tamura R, Murayama SY, et al. Suppression of lymphangiogenesis induced by Flt-4 antibody in gastric low-grade mucosa-associated lymphoid tissue lymphoma by Helicobacter heilmannii infection. J Gastroenterol Hepatol. 2010;25(Suppl 1):S1–6.
Nakamura M, Takahashi S, Matsui H, Murayama SY, Aikawa C, Sekiya Y, et al. Microcirculatory alteration in low-grade gastric mucosa-associated lymphoma by Helicobacter heilmannii infection: its relation to vascular endothelial growth factor and cyclooxygenase-2. J Gastroenterol Hepatol. 2008;23(Suppl 2):S157–60.
Suzuki A, Kobayashi M, Matsuda K, Matsumoto T, Kawakubo M, Kumazawa S, et al. Induction of high endothelial venule-like vessels expressing GlcNAc6ST-1-mediated L-selectin ligand carbohydrate and mucosal addressin cell adhesion molecule 1 (MAdCAM-1) in a mouse model of “Candidatus Helicobacter heilmannii”-induced gastritis and gastric mucosa-associated lymphoid tissue (MALT) lymphoma. Helicobacter. 2010;15:538–48.
Musshoff K. Clinical staging classification of non-Hodgkin’s lymphomas (author’s transl). Strahlentherapie. 1977;153:218–21.
Nakamura S, Matsumoto T, Ye H, Suekane H, Matsumoto H, Yao T, et al. Helicobacter pylori-negative gastric mucosa-associated lymphoid tissue lymphoma: a clinicopathologic and molecular study with reference to antibiotic treatment. Cancer. 2006;107:2770–8.
Raderer M, Streubel B, Wohrer S, Hafner M, Chott A. Successful antibiotic treatment of Helicobacter pylori negative gastric mucosa associated lymphoid tissue lymphomas. Gut. 2006;55:616–8.
Schechter NR, Portlock CS, Yahalom J. Treatment of mucosa-associated lymphoid tissue lymphoma of the stomach with radiation alone. J Clin Oncol. 1998;16:1916–21.
Datta YH, Kampalath B, Binion DG. Rituximab-induced remission of a gastric MALT lymphoma. Leukemia Lymphoma. 2004;45:1297–9.
Acknowledgments
We thank Trevor Ralph for his English editorial assistance.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Okamura, T., Iwaya, Y., Yokosawa, S. et al. A case of Helicobacter heilmannii-associated primary gastric mucosa-associated lymphoid tissue lymphoma achieving complete remission after eradication. Clin J Gastroenterol 6, 38–45 (2013). https://doi.org/10.1007/s12328-012-0355-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12328-012-0355-9