Impact of Helicobacter pylori Biofilm Formation on Clarithromycin Susceptibility and Generation of Resistance Mutations

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Yonezawa, Hideo ^a   Osaki, Takako ^a   Hanawa, Tomoko ^a   Kurata, Satoshi ^a   Ochiai, Kuniyasu ^b   Kamiya, Shigeru ^a  

^a KYORIN UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b NIHON UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CLARITHROMYCIN; RNA 23S;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BIOFILM; CELL VIABILITY; CONTROLLED STUDY; GENE EXPRESSION; GENE MUTATION; HELICOBACTER PYLORI; IN VITRO STUDY; MICROBIAL BIOMASS; MINIMUM BACTERICIDAL CONCENTRATION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PLANKTON; POINT MUTATION;

ANTI-BACTERIAL AGENTS; BIOFILMS; CLARITHROMYCIN; DRUG RESISTANCE, BACTERIAL; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; MUTATION; RNA, RIBOSOMAL, 23S;

EID: 84883624047     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0073301     Document Type: Article

References (48)

1. Parsek MR, Singh PK, (2003) Bacterial biofilms: an emerging link to disease pathogenesis. Annu Rev Microbiol 57: 677-701.
2. Costerton JW, Stewart PS, Greenberg EP, (1999) Bacterial biofilms: a common cause of persistent infections. Science 284: 1318-1322.
3. Marshall BJ, Warren JR, (1984) Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 1: 1311-1315.
4. Cellini L, Grande R, Di Campli E, Di Bartolomeo S, Di Giulio M, et al. (2008) Characterization of an Helicobacter pylori environmental strain. J Appl Microbiol 105: 761-769.
5. Cole SP, Harwood J, Lee R, She R, Guiney DG, (2004) Characterization of monospecies biofilm formation by Helicobacter pylori. J Bacteriol 186: 3124-3132.
6. Stark RM, Gerwig GJ, Pitman RS, Potts LF, Williams NA, et al. (1999) Biofilm formation by Helicobacter pylori. Lett Appl Microbiol 28: 121-126.
7. Carron MA, Tran VR, Sugawa C, Coticchia JM, (2006) Identification of Helicobacter pylori biofilms in human gastric mucosa. J Gastrointest Surg 10: 712-717.
8. Cellini L, Grande R, Di Campli E, Traini T, Giulio MD, et al. (2008) Dynamic colonization of Helicobacter pylori in human gastric mucosa. Scand J Gastroenterol 43: 178-185.
9. Coticchia JM, Sugawa C, Tran VR, Gurrola J, Kowalski E, et al. (2006) Presence and density of Helicobacter pylori biofilms in human gastric mucosa in patients with peptic ulcer disease. J Gastrointest Surg 10: 883-889.
10. Yonezawa H, Osaki T, Kurata S, Fukuda M, Kawakami H, et al. (2009) Outer membrane vesicles of Helicobacter pylori TK1402 are involved in biofilm formation. BMC Microbiol 9: 197.
11. Yonezawa H, Osaki T, Kurata S, Zaman C, Hanawa T, et al. (2010) Assessment of in vitro biofilm formation by Helicobacter pylori. J Gastroenterol Hepatol 25Suppl 1: S90-94.
12. Yonezawa H, Osaki T, Woo T, Kurata S, Zaman C, et al. (2011) Analysis of outer membrane vesicle protein involved in biofilm formation of Helicobacter pylori. Anaerobe 17: 388-390.
13. Lind T, Megraud F, Unge P, Bayerdorffer E, O'Morain C, et al. (1999) The MACH2 study: role of omeprazole in eradication of Helicobacter pylori with 1-week triple therapies. Gastroenterology 116: 248-253.
14. Malfertheiner P, Megraud F, O'Morain C, Bell D, Bianchi Porro G, et al. (1997) Current European concepts in the management of Helicobacter pylori infection-the Maastricht Consensus Report. The European Helicobacter Pylori Study Group (EHPSG). Eur J Gastroenterol Hepatol 9: 1-2.
15. Asaka M, Kato M, Takahashi S, Fukuda Y, Sugiyama T, et al. (2010) Guidelines for the management of Helicobacter pylori infection in Japan: 2009 revised edition. Helicobacter 15: 1-20.
16. Graham DY, de Boer WA, Tytgat GN, (1996) Choosing the best anti-Helicobacter pylori therapy: effect of antimicrobial resistance. Am J Gastroenterol 91: 1072-1076.
17. Adamek RJ, Suerbaum S, Pfaffenbach B, Opferkuch W, (1998) Primary and acquired Helicobacter pylori resistance to clarithromycin, metronidazole, and amoxicillin-influence on treatment outcome. Am J Gastroenterol 93: 386-389.
18. Megraud F, Doermann HP, (1998) Clinical relevance of resistant strains of Helicobacter pylori: a review of current data. Gut 43Suppl 1: S61-65.
19. Malfertheiner P, Megraud F, O'Morain CA, Atherton J, Axon AT, et al. (2012) Management of Helicobacter pylori infection-the Maastricht IV/Florence Consensus Report. Gut 61: 646-664.
20. Horiki N, Omata F, Uemura M, Suzuki S, Ishii N, et al. (2009) Annual change of primary resistance to clarithromycin among Helicobacter pylori isolates from 1996 through 2008 in Japan. Helicobacter 14: 86-90.
21. Kobayashi I, Murakami K, Kato M, Kato S, Azuma T, et al. (2007) Changing antimicrobial susceptibility epidemiology of Helicobacter pylori strains in Japan between 2002 and 2005. J Clin Microbiol 45: 4006-4010.
22. Garcia-Arata MI, Baquero F, de Rafael L, Martin de Argila C, Gisbert JP, et al. (1999) Mutations in 23S rRNA in Helicobacter pylori conferring resistance to erythromycin do not always confer resistance to clarithromycin. Antimicrob Agents Chemother 43: 374-376.
23. Versalovic J, Osato MS, Spakovsky K, Dore MP, Reddy R, et al. (1997) Point mutations in the 23S rRNA gene of Helicobacter pylori associated with different levels of clarithromycin resistance. J Antimicrob Chemother 40: 283-286.
24. Nakagawa S, Osaki T, Fujioka Y, Yamaguchi H, Kamiya S, (2005) Long-term infection of Mongolian gerbils with Helicobacter pylori: microbiological, histopathological, and serological analyses. Clin Diagn Lab Immunol 12: 347-353.
25. Rinttila T, Kassinen A, Malinen E, Krogius L, Palva A, (2004) Development of an extensive set of 16S rDNA-targeted primers for quantification of pathogenic and indigenous bacteria in faecal samples by real-time PCR. J Appl Microbiol 97: 1166-1177.
26. Liu ZQ, Zheng PY, Yang PC, (2008) Efflux pump gene hefA of Helicobacter pylori plays an important role in multidrug resistance. World J Gastroenterol 14: 5217-5222.
27. Noguchi N, Rimbara E, Kato A, Tanaka A, Tokunaga K, et al. (2007) Detection of mixed clarithromycin-resistant and-susceptible Helicobacter pylori using nested PCR and direct sequencing of DNA extracted from faeces. J Med Microbiol 56: 1174-1180.
28. Di Bonaventura G, Spedicato I, D'Antonio D, Robuffo I, Piccolomini R, (2004) Biofilm formation by Stenotrophomonas maltophilia: modulation by quinolones, trimethoprim-sulfamethoxazole, and ceftazidime. Antimicrob Agents Chemother 48: 151-160.
29. Bode G, Mauch F, Malfertheiner P, (1993) The coccoid forms of Helicobacter pylori. Criteria for their viability. Epidemiol Infect 111: 483-490.
30. van Amsterdam K, Bart A, van der Ende A, (2005) A Helicobacter pylori TolC efflux pump confers resistance to metronidazole. Antimicrob Agents Chemother 49: 1477-1482.
31. Hirata K, Suzuki H, Nishizawa T, Tsugawa H, Muraoka H, et al. (2010) Contribution of efflux pumps to clarithromycin resistance in Helicobacter pylori. J Gastroenterol Hepatol 25Suppl 1: S75-79.
32. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM, (1995) Microbial biofilms. Annu Rev Microbiol 49: 711-745.
33. Mah TF, O'Toole GA, (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9: 34-39.
34. Adams JL, McLean RJ, (1999) Impact of rpoS deletion on Escherichia coli biofilms. Appl Environ Microbiol 65: 4285-4287.
35. Anderl JN, Franklin MJ, Stewart PS, (2000) Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob Agents Chemother 44: 1818-1824.
36. Desai M, Buhler T, Weller PH, Brown MR, (1998) Increasing resistance of planktonic and biofilm cultures of Burkholderia cepacia to ciprofloxacin and ceftazidime during exponential growth. J Antimicrob Chemother 42: 153-160.
37. Dunne WM Jr, Mason EO Jr, Kaplan SL, (1993) Diffusion of rifampin and vancomycin through a Staphylococcus epidermidis biofilm. Antimicrob Agents Chemother 37: 2522-2526.
38. Grande R, Di Giulio M, Bessa LJ, Di Campli E, Baffoni M, et al. (2011) Extracellular DNA in Helicobacter pylori biofilm: a backstairs rumour. J Appl Microbiol 110: 490-498.
39. Yang FL, Hassanbhai AM, Chen HY, Huang ZY, Lin TL, et al. (2011) Proteomannans in biofilm of Helicobacter pylori ATCC 43504. Helicobacter 16: 89-98.
40. Taylor DE, Ge Z, Purych D, Lo T, Hiratsuka K, (1997) Cloning and sequence analysis of two copies of a 23S rRNA gene from Helicobacter pylori and association of clarithromycin resistance with 23S rRNA mutations. Antimicrob Agents Chemother 41: 2621-2628.
41. Tomb JF, White O, Kerlavage AR, Clayton RA, Sutton GG, et al. (1997) The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388: 539-547.
42. Alm RA, Ling LS, Moir DT, King BL, Brown ED, et al. (1999) Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397: 176-180.
43. Fujimura S, Kato S, Iinuma K, Watanabe A, (2004) In vitro exposure to macrolide antibiotics in Helicobacter pylori strains isolated from children. J Infect Chemother 10: 128-130.
44. Wang G, Wilson TJ, Jiang Q, Taylor DE, (2001) Spontaneous mutations that confer antibiotic resistance in Helicobacter pylori. Antimicrob Agents Chemother 45: 727-733.
45. Nakamura M, Spiller RC, Barrett DA, Wibawa JI, Kumagai N, et al. (2003) Gastric juice, gastric tissue and blood antibiotic concentrations following omeprazole, amoxicillin and clarithromycin triple therapy. Helicobacter 8: 294-299.
46. Macia MD, Perez JL, Molin S, Oliver A, (2011) Dynamics of mutator and antibiotic-resistant populations in a pharmacokinetic/pharmacodynamic model of Pseudomonas aeruginosa biofilm treatment. Antimicrob Agents Chemother 55: 5230-5237.
47. Mulet X, Macia MD, Mena A, Juan C, Perez JL, et al. (2009) Azithromycin in Pseudomonas aeruginosa biofilms: bactericidal activity and selection of nfxB mutants. Antimicrob Agents Chemother 53: 1552-1560.
48. Cammarota G, Sanguinetti M, Gallo A, Posteraro B, (2012) Review article: biofilm formation by Helicobacter pylori as a target for eradication of resistant infection. Aliment Pharmacol Ther 36: 222-230.