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Published in: Annals of Hematology 7/2016

Open Access 01-06-2016 | Original Article

Prevalence of clarithromycin-resistant Helicobacter pylori strains in gastric mucosa-associated lymphoid tissue lymphoma patients

Authors: Ceren Bilgilier, Ingrid Simonitsch-Klupp, Barbara Kiesewetter, Markus Raderer, Werner Dolak, Athanasios Makristathis, Christoph Steininger

Published in: Annals of Hematology | Issue 7/2016

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Abstract

Gastric MALT lymphoma is closely associated with Helicobacter pylori infection. Bacterial eradication therapy comprising clarithromycin is the first-line treatment in gastric MALT lymphoma patients. However, antimicrobial resistance to clarithromycin has been increasing in Europe, and thus far, it has not been examined in gastric MALT lymphoma patients. Based upon histopathological investigation, 17 adult gastric MALT lymphoma patients were identified to be related with H. pylori infection between 1997 and 2014. Detection of H. pylori infection in these patients and clarithromycin susceptibility testing were performed by 23S rRNA gene real-time PCR. Twelve of the patients were confirmed with H. pylori infection by real-time PCR. Among these patients, only two were found to be infected with clarithromycin-resistant H. pylori strain. In one of them, both the clarithromycin-resistant and sensitive genotype were detected. The rate of clarithromycin resistance was 15.4 %. Clarithromycin resistance pattern in gastric MALT lymphoma patients is under the predictions since a previous study performed in Central Europe revealed a rate of 36.6 % in Austria. Considering the low antimicrobial resistance rate, clarithromycin is still an option in gastric MALT lymphoma management.
Literature
1.
go back to reference Zucca E, Bertoni F, Roggero E, Cavalli F (2000) The gastric marginal zone B-cell lymphoma of MALT type. Blood 96:410–419PubMed Zucca E, Bertoni F, Roggero E, Cavalli F (2000) The gastric marginal zone B-cell lymphoma of MALT type. Blood 96:410–419PubMed
2.
go back to reference Gisbert JP, Calvet X (2011) Review article: common misconceptions in the management of Helicobacter pylori-associated gastric MALT-lymphoma. Aliment Pharmacol Ther 34:1047–1062CrossRefPubMed Gisbert JP, Calvet X (2011) Review article: common misconceptions in the management of Helicobacter pylori-associated gastric MALT-lymphoma. Aliment Pharmacol Ther 34:1047–1062CrossRefPubMed
3.
go back to reference Nakamura S, Matsumoto T (2013) Helicobacter pylori and gastric mucosa-associated lymphoid tissue lymphoma: recent progress in pathogenesis and management. World J Gastroenterol 19:8181–8187CrossRefPubMedPubMedCentral Nakamura S, Matsumoto T (2013) Helicobacter pylori and gastric mucosa-associated lymphoid tissue lymphoma: recent progress in pathogenesis and management. World J Gastroenterol 19:8181–8187CrossRefPubMedPubMedCentral
4.
go back to reference Ruskoné-Fourmestraux A, Fischbach W, Aleman BM, Boot H, Du MQ, Megraud F, Montalban C, Raderer M, Savio A, Wotherspoon A, EGILS group (2011) EGILS consensus report. Gastric extranodal marginal zone B-cell lymphoma of MALT. Gut 60:747–758CrossRefPubMed Ruskoné-Fourmestraux A, Fischbach W, Aleman BM, Boot H, Du MQ, Megraud F, Montalban C, Raderer M, Savio A, Wotherspoon A, EGILS group (2011) EGILS consensus report. Gastric extranodal marginal zone B-cell lymphoma of MALT. Gut 60:747–758CrossRefPubMed
5.
go back to reference Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J, Vardiman JW (2008) The World Health Organization classification of tumours of haematopoietic and lymphoid tissues. WHO, Lyon Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J, Vardiman JW (2008) The World Health Organization classification of tumours of haematopoietic and lymphoid tissues. WHO, Lyon
6.
go back to reference Zucca E, Copie-Bergman C, Ricardi U, Thieblemont C, Raderer M, Ladetto M, ESMO Guidelines Working Group (2013) Gastric marginal zone lymphoma of MALT type: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 24(Suppl 6):vi144–vi148CrossRefPubMed Zucca E, Copie-Bergman C, Ricardi U, Thieblemont C, Raderer M, Ladetto M, ESMO Guidelines Working Group (2013) Gastric marginal zone lymphoma of MALT type: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 24(Suppl 6):vi144–vi148CrossRefPubMed
7.
go back to reference Raderer M, Wöhrer S, Kiesewetter B, Dolak W, Lagler H, Wotherspoon A, Muellauer L, Chott A (2015) Antibiotic treatment as sole management of Helicobacter pylori-negative gastric MALT lymphoma: a single center experience with prolonged follow-up. Ann Hematol 94:969–973CrossRefPubMed Raderer M, Wöhrer S, Kiesewetter B, Dolak W, Lagler H, Wotherspoon A, Muellauer L, Chott A (2015) Antibiotic treatment as sole management of Helicobacter pylori-negative gastric MALT lymphoma: a single center experience with prolonged follow-up. Ann Hematol 94:969–973CrossRefPubMed
8.
go back to reference Parsonnet J, Hansen S, Rodriguez L, Gelb AB, Warnke RA, Jellum E, Orentreich N, Vogelman JH, Friedman GD (1994) Helicobacter pylori infection and gastric lypmhoma. N Engl J Med 330:1267–1271CrossRefPubMed Parsonnet J, Hansen S, Rodriguez L, Gelb AB, Warnke RA, Jellum E, Orentreich N, Vogelman JH, Friedman GD (1994) Helicobacter pylori infection and gastric lypmhoma. N Engl J Med 330:1267–1271CrossRefPubMed
9.
go back to reference Vannata B, Stathis A, Zucca E (2015) Management of the marginal zone lymphomas. In: Evens AM, Blum KA (eds) Non-Hodgkin lymphoma. Springer International Publishing, Switzerland, pp 227–249 Vannata B, Stathis A, Zucca E (2015) Management of the marginal zone lymphomas. In: Evens AM, Blum KA (eds) Non-Hodgkin lymphoma. Springer International Publishing, Switzerland, pp 227–249
10.
go back to reference Lin WC, Tsai HF, Kuo SH, Wu MS, Lin CW, Hsu PI, Cheng AL, Hsu PN (2010) Translocation of Helicobacter pylori CagA into human B lymphocytes, the origin of mucosa-associated lymphoid tissue lymphoma. Cancer Res 70:5740–5748CrossRefPubMed Lin WC, Tsai HF, Kuo SH, Wu MS, Lin CW, Hsu PI, Cheng AL, Hsu PN (2010) Translocation of Helicobacter pylori CagA into human B lymphocytes, the origin of mucosa-associated lymphoid tissue lymphoma. Cancer Res 70:5740–5748CrossRefPubMed
11.
go back to reference Peng JC, Zhong L, Ran ZH (2015) Primary lymphomas in the gastrointestinal tract. J Dig Dis 16:169–176CrossRefPubMed Peng JC, Zhong L, Ran ZH (2015) Primary lymphomas in the gastrointestinal tract. J Dig Dis 16:169–176CrossRefPubMed
12.
go back to reference Zullo A, Hassan C, Cristofari F, Perri F, Morini S (2010) Gastric low-grade mucosal-associated lymphoid tissue-lymphoma: Helicobacter pylori and beyond. World J Gastrointest Oncol 2:181–186CrossRefPubMedPubMedCentral Zullo A, Hassan C, Cristofari F, Perri F, Morini S (2010) Gastric low-grade mucosal-associated lymphoid tissue-lymphoma: Helicobacter pylori and beyond. World J Gastrointest Oncol 2:181–186CrossRefPubMedPubMedCentral
13.
go back to reference Megraud F, Coenen S, Versporten A, Kist M, Lopez-Brea M, Hirschl AM, Andersen LP, Goossens H, Glupczynski Y, Study Group participants (2013) Helicobacter pylori resistance to antibiotics in Europe and its relationship to antibiotic consumption. Gut 62:34–42CrossRefPubMed Megraud F, Coenen S, Versporten A, Kist M, Lopez-Brea M, Hirschl AM, Andersen LP, Goossens H, Glupczynski Y, Study Group participants (2013) Helicobacter pylori resistance to antibiotics in Europe and its relationship to antibiotic consumption. Gut 62:34–42CrossRefPubMed
14.
go back to reference Lehours P, Ruskone-Fourmestraux A, Lavergne A, Cantet F, Mégraud F (2003) Which test to use to detect Helicobacter pylori infection in patients with low-grade gastric mucosa-associated lymphoid tissue lymphoma? Am J Gastroenterol 98:291–295CrossRefPubMed Lehours P, Ruskone-Fourmestraux A, Lavergne A, Cantet F, Mégraud F (2003) Which test to use to detect Helicobacter pylori infection in patients with low-grade gastric mucosa-associated lymphoid tissue lymphoma? Am J Gastroenterol 98:291–295CrossRefPubMed
15.
go back to reference Schabereiter-Gurtner C, Hirschl AM, Dragosics B, Hufnagl P, Puz S, Kovách Z, Rotter M, Makristathis A (2004) Novel real-time PCR assay for detection of Helicobacter pylori infection and simultaneous clarithromycin susceptibility testing of stool and biopsy specimens. J Clin Microbiol 42:4512–4518CrossRefPubMedPubMedCentral Schabereiter-Gurtner C, Hirschl AM, Dragosics B, Hufnagl P, Puz S, Kovách Z, Rotter M, Makristathis A (2004) Novel real-time PCR assay for detection of Helicobacter pylori infection and simultaneous clarithromycin susceptibility testing of stool and biopsy specimens. J Clin Microbiol 42:4512–4518CrossRefPubMedPubMedCentral
16.
go back to reference Argent RH, Zhang Y, Atherton JC (2005) Simple method for determination of the number of Helicobacter pylori CagA variable-region EPIYA tyrosine phosphorylation motifs by PCR. J Clin Microbiol 43:791–795CrossRefPubMedPubMedCentral Argent RH, Zhang Y, Atherton JC (2005) Simple method for determination of the number of Helicobacter pylori CagA variable-region EPIYA tyrosine phosphorylation motifs by PCR. J Clin Microbiol 43:791–795CrossRefPubMedPubMedCentral
17.
go back to reference Wang HP, Zhu YL, Shao W (2013) Role of Helicobacter pylori virulence factor cytotoxin-associated gene A in gastric mucosa-associated lymphoid tissue lymphoma. World J Gastroenterol 19:8219–8226CrossRefPubMedPubMedCentral Wang HP, Zhu YL, Shao W (2013) Role of Helicobacter pylori virulence factor cytotoxin-associated gene A in gastric mucosa-associated lymphoid tissue lymphoma. World J Gastroenterol 19:8219–8226CrossRefPubMedPubMedCentral
18.
go back to reference Fischbach W, Jung T, Goebeler-Kolve M, Eck M (2000) Comparative analysis of the Helicobacter pylori status in patients with gastric MALT-type lymphoma and their respective spouses. Z Gastroenterol 38:627–630CrossRefPubMed Fischbach W, Jung T, Goebeler-Kolve M, Eck M (2000) Comparative analysis of the Helicobacter pylori status in patients with gastric MALT-type lymphoma and their respective spouses. Z Gastroenterol 38:627–630CrossRefPubMed
19.
go back to reference Eck M, Schmausser B, Haas R, Greiner A, Czub S, Müller-Hermelink HK (1997) MALT-type lymphoma of the stomach is associated with Helicobacter pylori strains expressing the CagA protein. Gastroenterology 112:1482–1486CrossRefPubMed Eck M, Schmausser B, Haas R, Greiner A, Czub S, Müller-Hermelink HK (1997) MALT-type lymphoma of the stomach is associated with Helicobacter pylori strains expressing the CagA protein. Gastroenterology 112:1482–1486CrossRefPubMed
20.
go back to reference Raderer M, Streubel B, Wöhrer S, Häfner M, Chott A (2006) Successful antibiotic treatment of Helicobacter pylori negative gastric mucosa associated lymphoid tissue lymphomas. Gut 55:616–618CrossRefPubMedPubMedCentral Raderer M, Streubel B, Wöhrer S, Häfner M, Chott A (2006) Successful antibiotic treatment of Helicobacter pylori negative gastric mucosa associated lymphoid tissue lymphomas. Gut 55:616–618CrossRefPubMedPubMedCentral
21.
go back to reference Malfertheiner P, Megraud F, O’Morain CA, Atherton J, Axon AT, Bazzoli F, Gensini GF, Gisbert JP, Graham DY, Rokkas T, El-Omar EM, Kuipers EJ, The European Helicobacter Study Group (2012) Management of Helicobacter pylori infection—the Maastricht IV/ Florence Consensus Report. Gut 61:646–664CrossRefPubMed Malfertheiner P, Megraud F, O’Morain CA, Atherton J, Axon AT, Bazzoli F, Gensini GF, Gisbert JP, Graham DY, Rokkas T, El-Omar EM, Kuipers EJ, The European Helicobacter Study Group (2012) Management of Helicobacter pylori infection—the Maastricht IV/ Florence Consensus Report. Gut 61:646–664CrossRefPubMed
22.
go back to reference Dedhia P, Tarale S, Dhongde G, Khadapkar R, Das B (2007) Evaluation of DNA extraction methods and real time PCR optimization on formalin-fixed paraffin-embedded tissues. Asian Pac J Cancer Prev 8:55–59PubMed Dedhia P, Tarale S, Dhongde G, Khadapkar R, Das B (2007) Evaluation of DNA extraction methods and real time PCR optimization on formalin-fixed paraffin-embedded tissues. Asian Pac J Cancer Prev 8:55–59PubMed
23.
go back to reference Meine GC, Rota C, Dietz J, Sekine S, Prolla JC (2011) Relationship between cagA-Positive Helicobacter pylori infection and risk of gastric cancer: a case control study in Porto Alegre, RS, Brazil. Arq Gastroenterol 48:41–45PubMed Meine GC, Rota C, Dietz J, Sekine S, Prolla JC (2011) Relationship between cagA-Positive Helicobacter pylori infection and risk of gastric cancer: a case control study in Porto Alegre, RS, Brazil. Arq Gastroenterol 48:41–45PubMed
24.
go back to reference Uemura N, Okamoto S, Yamamoto S, Matsumura N, Yamaguchi S, Yamakido M, Taniyama K, Sasaki N, Schlemper RJ (2001) Helicobacter pylori infection and the development of gastric cancer. N Engl J Med 345:784–789CrossRefPubMed Uemura N, Okamoto S, Yamamoto S, Matsumura N, Yamaguchi S, Yamakido M, Taniyama K, Sasaki N, Schlemper RJ (2001) Helicobacter pylori infection and the development of gastric cancer. N Engl J Med 345:784–789CrossRefPubMed
25.
go back to reference Fasciana T, Calà C, Bonura C, Di Carlo E, Matranga D, Scarpulla G, Manganaro M, Camilleri S, Giammanco A (2015) Resistance to clarithromycin and genotypes in Helicobacter pylori strains, isolated in Sicily. J Med Microbiol. doi:10.1099/jmm.0.000163 PubMed Fasciana T, Calà C, Bonura C, Di Carlo E, Matranga D, Scarpulla G, Manganaro M, Camilleri S, Giammanco A (2015) Resistance to clarithromycin and genotypes in Helicobacter pylori strains, isolated in Sicily. J Med Microbiol. doi:10.​1099/​jmm.​0.​000163 PubMed
26.
go back to reference Liou JM, Chang CY, Chen MJ, Chen CC, Fang YJ, Lee JY, Wu JY, Luo JC, Liou TC, Chang WH, Tseng CH, Wu CY, Yang TH, Chang CC, Wang HP, Sheu BS, Lin JT, Bair MJ, Wu MS, Taiwan Gastrointestinal Disease and Helicobacter Consortium (2015) The primary resistance of helicobacter pylori in Taiwan after the national policy to restrict antibiotic consumption and its relation to virulence factors—a Nationwide Study. PLoS One. doi:10.1371/journal.pone.0124199 CrossRef Liou JM, Chang CY, Chen MJ, Chen CC, Fang YJ, Lee JY, Wu JY, Luo JC, Liou TC, Chang WH, Tseng CH, Wu CY, Yang TH, Chang CC, Wang HP, Sheu BS, Lin JT, Bair MJ, Wu MS, Taiwan Gastrointestinal Disease and Helicobacter Consortium (2015) The primary resistance of helicobacter pylori in Taiwan after the national policy to restrict antibiotic consumption and its relation to virulence factors—a Nationwide Study. PLoS One. doi:10.​1371/​journal.​pone.​0124199 CrossRef
27.
go back to reference Taneike I, Nami A, O’Connor A, Fitzgerald N, Murphy P, Qasim A, O’Connor H, O’Morain C (2009) Analysis of drug resistance and virulence-factor genotype of Irish Helicobacter pylori strains: is there any relationship between resistance to metranidazole and cagA status? Aliment Pharmacol Ther 30:784–790CrossRefPubMed Taneike I, Nami A, O’Connor A, Fitzgerald N, Murphy P, Qasim A, O’Connor H, O’Morain C (2009) Analysis of drug resistance and virulence-factor genotype of Irish Helicobacter pylori strains: is there any relationship between resistance to metranidazole and cagA status? Aliment Pharmacol Ther 30:784–790CrossRefPubMed
28.
go back to reference Bustamante-Rengifo JA, Matta AJ, Pazos A, Bravo LE (2013) In vitro effect of amoxicillin and clarithromycin on the 3′ region of cagA gene in Helicobacter pylori isolates. World J Gastroenterol 19:6044–6054CrossRefPubMedPubMedCentral Bustamante-Rengifo JA, Matta AJ, Pazos A, Bravo LE (2013) In vitro effect of amoxicillin and clarithromycin on the 3′ region of cagA gene in Helicobacter pylori isolates. World J Gastroenterol 19:6044–6054CrossRefPubMedPubMedCentral
Metadata
Title
Prevalence of clarithromycin-resistant Helicobacter pylori strains in gastric mucosa-associated lymphoid tissue lymphoma patients
Authors
Ceren Bilgilier
Ingrid Simonitsch-Klupp
Barbara Kiesewetter
Markus Raderer
Werner Dolak
Athanasios Makristathis
Christoph Steininger
Publication date
01-06-2016
Publisher
Springer Berlin Heidelberg
Published in
Annals of Hematology / Issue 7/2016
Print ISSN: 0939-5555
Electronic ISSN: 1432-0584
DOI
https://doi.org/10.1007/s00277-016-2672-4

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