2,321
Views
43
CrossRef citations to date
0
Altmetric
Review Article

Resistance mechanisms of Helicobacter pylori and its dual target precise therapy

&
Pages 371-392 | Received 25 Mar 2017, Accepted 08 Dec 2017, Published online: 02 Jan 2018

References

  • An B, Moon BS, Kim H, Lim HC, Lee YC, Lee G, Kim SH, Park M, Kim JB. 2013. Antibiotic resistance in Helicobacter pylori strains and its effect on H. pylori eradication rates in a single center in Korea. Ann Lab Med. 33(6):415–419.
  • Anoushiravani M, Falsafi T, Niknam V. 2009. Proton motive force-dependent efflux of tetracycline in clinical isolates of Helicobacter pylori. J Med Microbiol. 58:1309–1313.
  • Bai P, Zhou LY, Xiao XM, Luo Y, Ding Y. 2015. Susceptibility of Helicobacter pylori to antibiotics in Chinese patients. J Dig Dis. 16:464–470.
  • Binh TT, Shiota S, Nguyen LT, Ho DD, Hoang HH, Ta L, Trinh DT, Fujioka T, Yamaoka Y. 2013. The incidence of primary antibiotic resistance of Helicobacter pylori in Vietnam. J Clin Gastroenterol. 47:233–238.
  • Binh TT, Shiota S, Suzuki R, Matsuda M, Trang TT, Kwon DH, Iwatani S, Yamaoka Y. 2014. Discovery of novel mutations for clarithromycin resistance in Helicobacter pylori by using next-generation sequencing. J Antimicrob Chemother. 69:1796–1803.
  • Binh TT, Suzuki R, Trang TT, Kwon DH, Yamaoka Y. 2015. Search for novel candidate mutations for metronidazole resistance in Helicobacter pylori using next-generation sequencing. Antimicrob Agents Chemother. 59:2343–2348.
  • Boyanova L, Markovska R, Yordanov D, Gergova G, Mitov I. 2016. Clarithromycin resistance mutations in Helicobacter pylori in association with virulence factors and antibiotic susceptibility of the strains. Microb Drug Resist. 22:227–232.
  • Broutet N, Tchamgoue S, Pereira E, Lamouliatte H, Salamon R, Megraud F. 2003. Risk factors for failure of Helicobacter pylori therapy-results of an individual data analysis of 2751 patients. Aliment Pharmacol Ther. 17:99–109.
  • Burucoa C, Garnier M, Silvain C, Fauchere JL. 2008. Quadruplex real-time PCR assay using allele-specific scorpion primers for detection of mutations conferring clarithromycin resistance to Helicobacter pylori. J Clin Microbiol. 46:2320–2326.
  • Butlop TR, Mungkote NT, Chaichanawongsaroj NT. 2016. Analysis of allelic variants of rdxA associated with metronidazole resistance in Helicobacter pylori: detection of common genotypes in rdxA by multiplex allele-specific polymerase chain reaction. Genet Mol Res. 15. doi: 10.4238/gmr.15038674
  • Cai J, Huang H, Song W, Hu H, Chen J, Zhang L, Li P, Wu R, Wu C. 2015. Preparation and evaluation of lipid polymer nanoparticles for eradicating H. pylori biofilm and impairing antibacterial resistance in vitro. Int J Pharm. 495:728–737.
  • Caliskan R, Tokman HB, Erzin Y, Saribas S, Yuksel P, Bolek BK, Sevuk EO, Demirci M, Yilmazli O, Akgul O, et al. 2015. Antimicrobial resistance of Helicobacter pylori strains to five antibiotics, including levofloxacin, in Northwestern Turkey. Rev Soc Bras Med Trop. 48:278–284.
  • Calvet X, Ramirez Lazaro MJ, Lehours P, Megraud F. 2013. Diagnosis and epidemiology of Helicobacter pylori infection. Helicobacter. 18(Suppl 1):5–11.
  • Calvino-Fernandez M, Garcia-Fresnadillo D, Benito-Martinez S, McNicholl AG, Calvet X, Gisbert JP, Parra-Cid T. 2013. Helicobacter pylori inactivation and virulence gene damage using a supported sensitiser for photodynamic therapy. Eur J Med Chem. 68:284–290.
  • Cambau E, Allerheiligen V, Coulon C, Corbel C, Lascols C, Deforges L, Soussy CJ, Delchier JC, Megraud F. 2009. Evaluation of a new test, genotype HelicoDR, for molecular detection of antibiotic resistance in Helicobacter pylori. J Clin Microbiol. 47:3600–3607.
  • 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.
  • Cascorbi I, Gerloff T, Johne A, Meisel C, Hoffmeyer S, Schwab M, Schaeffeler E, Eichelbaum M, Brinkmann U, Roots I. 2001. Frequency of single nucleotide polymorphisms in the P-glycoprotein drug transporter MDR1 gene in white subjects. Clin Pharmacol Ther. 69:169–174.
  • Castano-Rodriguez N, Kaakoush NO, Goh KL, Fock KM, Mitchell HM. 2015. Autophagy in Helicobacter pylori infection and related gastric cancer. Helicobacter. 20:353–369.
  • Chakraborti S, Bhattacharya S, Chowdhury R, Chakrabarti P. 2013. The molecular basis of inactivation of metronidazole-resistant Helicobacter pylori using polyethyleneimine functionalized zinc oxide nanoparticles. PLoS One. 8:e70776.
  • Chang WL, Kao CY, Wu CT, Huang AH, Wu JJ, Yang HB, Cheng HC, Sheu BS. 2012. Gemifloxacin can partially overcome quinolone resistance of H. pylori with gyrA mutation in Taiwan. Helicobacter. 17:210–215.
  • Chao CY, Wang CH, Che YJ, Kao CY, Wu JJ, Lee GB. 2016. An integrated microfluidic system for diagnosis of the resistance of Helicobacter pylori to quinolone-based antibiotics. Biosens Bioelectron. 78:281–289.
  • Chen CJ, Chin JE, Ueda K, Clark DP, Pastan I, Gottesman MM, Roninson IB. 1986. Internal duplication and homology with bacterial transport proteins in the mdr1 (P-glycoprotein) gene from multidrug-resistant human cells. Cell. 47:381–389.
  • Chisholm SA, Owen RJ. 2008. Application of polymerase chain reaction-based assays for rapid identification and antibiotic resistance screening of Helicobacter pylori in gastric biopsies. Diagn Microbiol Infect Dis. 61:67–71.
  • Chung JW, Lee GH, Jeong JY, Lee SM, Jung JH, Choi KD, Song HJ, Jung HY, Kim JH. 2012. Resistance of Helicobacter pylori strains to antibiotics in Korea with a focus on fluoroquinolone resistance. J Gastroenterol Hepatol. 27:493–497.
  • Co EM, Schiller NL. 2006. Resistance mechanisms in an in vitro-selected amoxicillin-resistant strain of Helicobacter pylori. Antimicrob Agents Chemother. 50:4174–4176.
  • Cole SP, Harwood J, Lee R, She R, Guiney DG. 2004. Characterization of monospecies biofilm formation by Helicobacter pylori. J Bacteriol. 186:3124–3132.
  • Costerton JW, Cheng KJ, Geesey GG, Ladd TI, Nickel JC, Dasgupta M, Marrie TJ. 1987. Bacterial biofilms in nature and disease. Annu Rev Microbiol. 41:435–464.
  • Crispino P, Iacopini F, Pica R, Consolazio A, Bella A, Cassieri C, Nardi F, Paoluzi P. 2005. Beta-lactamase inhibition with clavulanic acid supplementing standard amoxycillin-based triple therapy does not increase Helicobacter pylori eradication rate. Dig Liver Dis. 37:826–831.
  • Dadashzadeh K, Milani M, Rahmati M, Akbarzadeh A. 2014. Real-time PCR detection of 16S rRNA novel mutations associated with Helicobacter pylori tetracycline resistance in Iran. Asian Pac J Cancer Prev. 15:8883–8886.
  • De Francesco V, Zullo A, Giorgio F, Saracino I, Zaccaro C, Hassan C, Ierardi E, Di Leo A, Fiorini G, Castelli V, et al. 2014. Change of point mutations in Helicobacter pylori rRNA associated with clarithromycin resistance in Italy. J Med Microbiol. 63:453–457.
  • Deen NS, Gong L, Naderer T, Devenish RJ, Kwok T. 2015. Analysis of the relative contribution of phagocytosis, LC3-associated phagocytosis, and canonical autophagy during Helicobacter pylori infection of macrophages. Helicobacter. 20:449–459.
  • Deen NS, Huang SJ, Gong L, Kwok T, Devenish RJ. 2013. The impact of autophagic processes on the intracellular fate of Helicobacter pylori: more tricks from an enigmatic pathogen? Autophagy. 9:639–652.
  • Deguchi R, Nakaminami H, Rimbara E, Noguchi N, Sasatsu M, Suzuki T, Matsushima M, Koike J, Igarashi M, Ozawa H, et al. 2012. Effect of pretreatment with Lactobacillus gasseri OLL2716 on first-line Helicobacter pylori eradication therapy. J Gastroenterol Hepatol. 27:888–892.
  • Demir M, Gokturk HS, Ozturk NA, Arslan H, Serin E, Yilmaz U. 2009. Clarithromycin resistance and efficacy of clarithromycin-containing triple eradication therapy for Helicobacter pylori infection in type 2 diabetes mellitus patients. South Med J. 102:1116–1120.
  • Demir M, Gokturk HS, Ozturk NA, Serin E, Yilmaz U. 2009. Efficacy of two different Helicobacter pylori eradication regimens in patients with type 2 diabetes and the effect of Helicobacter pylori eradication on dyspeptic symptoms in patients with diabetes: a randomized controlled study. Am J Med Sci. 338:459–464.
  • Di L. 2014. The role of drug metabolizing enzymes in clearance. Expert Opin Drug Metab Toxicol. 10:379–393.
  • Donlan RM, Costerton JW. 2002. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev. 15:167–193.
  • Doorakkers E, Lagergren J, Engstrand L, Brusselaers N. 2016. Eradication of Helicobacter pylori and gastric cancer: a systematic review and meta-analysis of cohort studies. J Natl Cancer Inst. 108;djw132.
  • Ducournau A, Benejat L, Sifre E, Bessede E, Lehours P, Megraud F. 2016. Helicobacter pylori resistance to antibiotics in 2014 in France detected by phenotypic and genotypic methods. Clin Microbiol Infect. 22:715–718.
  • Eghbali Z, Mojtahedi A, Moien Ansar M, Fakhrieh Asl S, Aminian K. 2016. Detection of 23SrRNA mutations strongly related to clarithromycin resistance in Helicobacter pylori strains isolated from patients in the North of Iran. Jundishapur J Microbiol. 9:e29694.
  • Fasciana T, Cala 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. 64:1408–1414.
  • Furuta T, Graham DY. 2010. Pharmacologic aspects of eradication therapy for Helicobacter pylori infection. Gastroenterol Clin North Am. 39:465–480.
  • Furuta T, Shirai N, Kodaira M, Sugimoto M, Nogaki A, Kuriyama S, Iwaizumi M, Yamade M, Terakawa I, Ohashi K, et al. 2007. Pharmacogenomics-based tailored versus standard therapeutic regimen for eradication of H. pylori. Clin Pharmacol Ther. 81:521–528.
  • Furuta T, Shirai N, Xiao F, Ohashi K, Ishizaki T. 2001. Effect of high-dose lansoprazole on intragastic pH in subjects who are homozygous extensive metabolizers of cytochrome P4502C19. Clin Pharmacol Ther. 70:484–492.
  • Gao W, Cheng H, Hu F, Li J, Wang L, Yang G, Xu L, Zheng X. 2010. The evolution of Helicobacter pylori antibiotics resistance over 10 years in Beijing, China. Helicobacter. 15:460–466.
  • Garcia M, Raymond J, Garnier M, Cremniter J, Burucoa C. 2012. Distribution of spontaneous gyrA mutations in 97 fluoroquinolone-resistant Helicobacter pylori isolates collected in France. Antimicrob Agents Chemother. 56:550–551.
  • Gawronska-Szklarz B, Siuda A, Kurzawski M, Bielicki D, Marlicz W, Drozdzik M. 2010. Effects of CYP2C19, MDR1, and interleukin 1-B gene variants on the eradication rate of Helicobacter pylori infection by triple therapy with pantoprazole, amoxicillin, and metronidazole. Eur J Clin Pharmacol. 66:681–687.
  • Gazi S, Karameris A, Christoforou M, Agnantis N, Rokkas T, Stefanou D. 2013. Real-Time PCR detection and quantitation of Helicobacter pylori clarithromycin-resistant strains in archival material and correlation with Sydney classification. Ann Gastroenterol. 26:226–232.
  • Gehlot V, Mahant S, Mukhopadhyay AK, Das K, Alam J, Ghosh P, Das R. 2016. Low prevalence of clarithromycin-resistant Helicobacter pylori isolates with A2143G point mutation in the 23S rRNA gene in North India. J Glob Antimicrob Resist. 6:39–43.
  • Gerrits MM, Godoy AP, Kuipers EJ, Ribeiro ML, Stoof J, Mendonca S, van Vliet AH, Pedrazzoli J Jr, Kusters JG. 2006. Multiple mutations in or adjacent to the conserved penicillin-binding protein motifs of the penicillin-binding protein 1A confer amoxicillin resistance to Helicobacter pylori. Helicobacter. 11:181–187.
  • Ghotaslou R, Milani M, Akhi MT, Nahaei MR, Hasani A, Hejazi MS, Meshkini M. 2013. Diversity of Helicobacter pylori cagA and vacA genes and its relationship with clinical outcomes in Azerbaijan, Iran. Adv Pharm Bull. 3:57–62.
  • Giao MS, Azevedo NF, Wilks SA, Vieira MJ, Keevil CW. 2008. Persistence of Helicobacter pylori in heterotrophic drinking-water biofilms. Appl Environ Microbiol. 74:5898–5904.
  • Giorgio F, Ierardi E, Sorrentino C, Principi M, Barone M, Losurdo G, Iannone A, Giangaspero A, Monno R, Di Leo A. 2016. Helicobacter pylori DNA isolation in the stool: an essential pre-requisite for bacterial noninvasive molecular analysis. Scand J Gastroenterol. 51:1429–1432.
  • Glocker E, Berning M, Gerrits MM, Kusters JG, Kist M. 2005. Real-time PCR screening for 16S rRNA mutations associated with resistance to tetracycline in Helicobacter pylori. Antimicrob Agents Chemother. 49:3166–3170.
  • Glocker E, Bogdan C, Kist M. 2007. Characterization of rifampicin-resistant clinical Helicobacter pylori isolates from Germany. J Antimicrob Chemother. 59:874–879.
  • Godoy AP, Reis FC, Ferraz LF, Gerrits MM, Mendonca S, Kusters JG, Ottoboni LM, Ribeiro ML, Pedrazzoli J Jr. 2007. Differentially expressed genes in response to amoxicillin in Helicobacter pylori analyzed by RNA arbitrarily primed PCR. FEMS Immunol Med Microbiol. 50:226–230.
  • Grignon B, Tankovic J, Megraud F, Glupczynski Y, Husson MO, Conroy MC, Emond JP, Loulergue J, Raymond J, Fauchere JL. 2002. Validation of diffusion methods for macrolide susceptibility testing of Helicobacter pylori. Microb Drug Resist. 8:61–66.
  • Hanafi A, Lee WC, Loke MF, Teh X, Shaari A, Dinarvand M, Lehours P, Megraud F, Leow AH, Vadivelu J, et al. 2016. Molecular and proteomic analysis of levofloxacin and metronidazole resistant Helicobacter pylori. Front Microbiol. 7:2015.
  • Hansomburana P, Anantapanpong S, Sirinthornpunya S, Chuengyong K, Rojborwonwittaya J. 2012. Prevalence of single nucleotide mutation in clarithromycin resistant gene of Helicobacter pylori: a 32-months prospective study by using hybridization real time polymerase chain reaction. J Med Assoc Thai. 95(Suppl 3):S28–S35.
  • Heep M, Beck D, Bayerdorffer E, Lehn N. 1999. Rifampin and rifabutin resistance mechanism in Helicobacter pylori. Antimicrob Agents Chemother. 43:1497–1499.
  • Heep M, Rieger U, Beck D, Lehn N. 2000. Mutations in the beginning of the rpoB gene can induce resistance to rifamycins in both Helicobacter pylori and Mycobacterium tuberculosis. Antimicrob Agents Chemother. 44:1075–1077.
  • Hirata K, Suzuki H, Nishizawa T, Tsugawa H, Muraoka H, Saito Y, Matsuzaki J, Hibi T. 2010. Contribution of efflux pumps to clarithromycin resistance in Helicobacter pylori. J Gastroenterol Hepatol. 25 Suppl 1:S75–S79.
  • Horii T, Kimura T, Sato-Kawamura K, Nada T, Shibayama K, Ohta M.1999. Beta-lactamase inhibitors have antibacterial activities against Helicobacter pylori. J Infect Chemother: Off J Jpn Soc Chemother. 5:206–207.
  • Hu B, Zhao F, Wang S, Olszewski MA, Bian H, Wu Y, Kong M, Xu L, Miao Y, Fang Y, et al. 2016. A high-throughput multiplex genetic detection system for Helicobacter pylori identification, virulence and resistance analysis. Future Microbiol. 11:1261–1278.
  • Huang HN, Rajanbabu V, Pan CY, Chan YL, Wu CJ, Chen JY. 2013. Use of the antimicrobial peptide Epinecidin-1 to protect against MRSA infection in mice with skin injuries. Biomaterials. 34:10319–10327.
  • Huang JQ, Hunt RH. 1999. Treatment after failure: the problem of “non-responders”. Gut 45 Suppl 1:I40–I44.
  • Hussein NR, Tunjel I, Majed HS, Yousif ST, Aswad SI, Assafi MS. 2015. Duodenal ulcer promoting gene 1 (dupA1) is associated with A2147G clarithromycin-resistance mutation but not interleukin-8 secretion from gastric mucosa in Iraqi patients. New Microb New Infect. 6:5–10.
  • Hwang IR, Kodama T, Kikuchi S, Sakai K, Peterson LE, Graham DY, Yamaoka Y. 2002. Effect of interleukin 1 polymorphisms on gastric mucosal interleukin 1beta production in Helicobacter pylori infection. Gastroenterology. 123:1793–1803.
  • Iwamoto A, Tanahashi T, Okada R, Yoshida Y, Kikuchi K, Keida Y, Murakami Y, Yang L, Yamamoto K, Nishiumi S, et al. 2014. Whole-genome sequencing of clarithromycin resistant Helicobacter pylori characterizes unidentified variants of multidrug resistant efflux pump genes. Gut Pathog. 6:27.
  • Iwanczak B, Francavailla R. 2014. Helicobacter pylori infection in pediatrics. Helicobacter. 19(Suppl 1):46–51.
  • Iwaya Y, Kobayashi M, Momose M, Hiraoka N, Sakai Y, Akamatsu T, Tanaka E, Ohtani H, Fukuda M, Nakayama J. 2013. High levels of FOXP3+ regulatory T cells in gastric MALT lymphoma predict responsiveness to Helicobacter pylori eradication. Helicobacter. 18:356–362.
  • Jeong JY, Mukhopadhyay AK, Dailidiene D, Wang Y, Velapatino B, Gilman RH, Parkinson AJ, Nair GB, Wong BC, Lam SK, et al. 2000. Sequential inactivation of rdxA (HP0954) and frxA (HP0642) nitroreductase genes causes moderate and high-level metronidazole resistance in Helicobacter pylori. J Bacteriol. 182:5082–5090.
  • Jim HS, Park JY, Permuth-Wey J, Rincon MA, Phillips KM, Small BJ, Jacobsen PB. 2012. Genetic predictors of fatigue in prostate cancer patients treated with androgen deprivation therapy: preliminary findings. Brain Behav Immun. 26:1030–1036.
  • Kafshdooz T, Akbarzadeh A, Majdi Seghinsara A, Pourhassan M, Nasrabadi HT, Milani M. 2016. Role of probiotics in managing of Helicobacter pylori infection: a review. Drug Res. 67(2):88–93.
  • Kang HY, Kim SG, Lee MK, Kim JS, Jung HC, Song IS. 2012. Effect of Helicobacter pylori eradication according to the IL-8-251 polymorphism in Koreans. J Korean Med Sci. 27(10):1202–1207.
  • Kao CY, Lee AY, Huang AH, Song PY, Yang YJ, Sheu SM, Chang WL, Sheu BS, Wu JJ. 2014. Heteroresistance of Helicobacter pylori from the same patient prior to antibiotic treatment. Infect Genet Evol. 23:196–202.
  • Kawai T, Yamagishi T, Yagi K, Kataoka M, Kawakami K, Sofuni A, Itoi T, Sakai Y, Moriyasu F, Osaka Y, et al. 2008. Tailored eradication therapy based on fecal Helicobacter pylori clarithromycin sensitivities. J Gastroenterol Hepatol. 23(Suppl 2):S171–S174.
  • Khademi F, Faghri J, Moghim S, Esfahani BN, Fazeli H, Poursina F, Adibi P, Madhi M, Safaei HG. 2014. The study of mutation in 23S rRNA resistance gene of Helicobacter pylori to clarithromycin in patients with gastrointestinal disorders in Isfahan–Iran. Adv Biomed Res. 3:98.
  • Khashei R, Dara M, Bazargani A, Bagheri Lankarani K, Taghavi A, Moeini M, Dehghani B, Sohrabi M. 2016. High rate of A2142G point mutation associated with clarithromycin resistance among Iranian Helicobacter pylori clinical isolates. APMIS. 124:787–793.
  • Kim BJ, Kim JG. 2013. Substitutions in penicillin-binding protein 1 in amoxicillin-resistant Helicobacter pylori strains isolated from Korean patients. Gut Liver. 7:655–660.
  • Kim JY, Jeon SM, Kim H, Lim N, Park MS, Kim SH. 2012. Resistance to fluoroquinolone by a combination of efflux and target site mutations in enteroaggregative Escherichia coli isolated in Korea. Osong Public Health Res Perspect. 3:239–244.
  • Kim KS, Kang JO, Eun CS, Han DS, Choi TY. 2002. Mutations in the 23S rRNA gene of Helicobacter pylori associated with clarithromycin resistance. J Korean Med Sci. 17:599–603.
  • Kuo CH, Liu CJ, Yang CC, Kuo FC, Hu HM, Shih HY, Wu MC, Chen YH, Wang HM, Ren JL, et al. 2016. A rapid and accurate method to evaluate Helicobacter pylori infection, clarithromycin resistance, and CYP2C19 genotypes simultaneously from gastric juice. Medicine (Baltimore). 95:e3458.
  • Kwak YG, Truong-Bolduc QC, Bin Kim H, Song KH, Kim ES, Hooper DC. 2013. Association of norB overexpression and fluoroquinolone resistance in clinical isolates of Staphylococcus aureus from Korea. J Antimicrob Chemother. 68:2766–2772.
  • Kwon DH, Lee M, Kim JJ, Kim JG, El-Zaatari FA, Osato MS, Graham DY. 2001. Furazolidone- and nitrofurantoin-resistant Helicobacter pylori: prevalence and role of genes involved in metronidazole resistance. Antimicrob Agents Chemother. 45:306–308.
  • Lee HJ, Kim JI, Cheung DY, Kim TH, Jun EJ, Oh JH, Chung WC, Kim BW, Kim SS, Park SH, et al. 2013. Eradication of Helicobacter pylori according to 23S ribosomal RNA point mutations associated with clarithromycin resistance. J Infect Dis. 208:1123–1130.
  • Lee JH, Shin JH, Roe IH, Sohn SG, Lee JH, Kang GH, Lee HK, Jeong BC, Lee SH. 2005. Impact of clarithromycin resistance on eradication of Helicobacter pylori in infected adults. Antimicrob Agents Chemother. 49:1600–1603.
  • Lee JW, Kim N, Nam RH, Park JH, Choi YJ, Kim JM, Kim JS, Jung HC. 2014. GenoType HelicoDR test in the determination of antimicrobial resistance of Helicobacter pylori in Korea. Scand J Gastroenterol. 49:1058–1067.
  • Lee JW, Kim N, Nam RH, Park JH, Kim JM, Jung HC, Song IS. 2011. Mutations of Helicobacter pylori associated with fluoroquinolone resistance in Korea. Helicobacter. 16:301–310.
  • Li XZ, Plesiat P, Nikaido H. 2015. The challenge of efflux-mediated antibiotic resistance in Gram-negative bacteria. Clin Microbiol Rev. 28:337–418.
  • Li Y, Dannelly HK. 2006. Inactivation of the putative tetracycline resistance gene HP1165 in Helicobacter pylori led to loss of inducible tetracycline resistance. Arch Microbiol. 185:255–262.
  • Lim JH, Lee DH, Lee ST, Kim N, Park YS, Shin CM, Song IS. 2015. Moxifloxacin-containing triple therapy after non-bismuth quadruple therapy failure for Helicobacter pylori infection. World J Gastroenterol. 21:13124–13131.
  • 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.
  • Lopez-Brea M, Martinez MJ, Domingo D, Sanchez I, Alarcon T. 1999. Metronidazole resistance and virulence factors in Helicobacter pylori as markers for treatment failure in a paediatric population. FEMS Immunol Med Microbiol. 24(2):183–188.
  • Maeda S, Yoshida H, Ikenoue T, Ogura K, Kanai F, Kato N, Shiratori Y, Omata M. 1999. Structure of cag pathogenicity island in Japanese Helicobacter pylori isolates. Gut. 44:336–341.
  • Magalhaes AF, Carvalhaes A, Natan-Eisig J, Paraiso-Ferraz JG, Trevisan M, Zaterkaad S. 2005. CagA status and Helicobacter pylori eradication among dyspeptic patients. Gastroenterol Hepatol. 28:441–444.
  • Makobongo MO, Einck L, Peek RM Jr, Merrell DS. 2013. In vitro characterization of the anti-bacterial activity of SQ109 against Helicobacter pylori. PLoS One. 8:e68917.
  • Marais A, Bilardi C, Cantet F, Mendz GL, Megraud F. 2003. Characterization of the genes rdxA and frxA involved in metronidazole resistance in Helicobacter pylori. Res Microbiol. 154:137–144.
  • Matteo MJ, Granados G, Olmos M, Wonaga A, Catalano M. 2008. Helicobacter pylori amoxicillin heteroresistance due to point mutations in PBP-1A in isogenic isolates. J Antimicrob Chemother. 61:474–477.
  • Mazaheri Assadi M, Chamanrokh P, Whitehouse CA, Huq A. 2015. Methods for detecting the environmental coccoid form of Helicobacter pylori. Front Public Health. 3:147.
  • Megraud F, Lehours P. 2007. Helicobacter pylori detection and antimicrobial susceptibility testing. Clin Microbiol Rev. 20:280–322.
  • Mendz GL, Megraud F. 2002. Is the molecular basis of metronidazole resistance in microaerophilic organisms understood? Trends Microbiol. 10:370–375.
  • Miendje Deyi VY, Burette A, Bentatou Z, Maaroufi Y, Bontems P, Lepage P, Reynders M. 2011. Practical use of GenoType® HelicoDR, a molecular test for Helicobacter pylori detection and susceptibility testing. Diagn Microbiol Infect Dis. 70:557–560.
  • Miftahussurur M, Shrestha PK, Subsomwong P, Sharma RP, Yamaoka Y. 2016. Emerging Helicobacter pylori levofloxacin resistance and novel genetic mutation in Nepal. BMC Microbiol. 16:256.
  • Miftahussurur M, Syam AF, Nusi IA, Makmun D, Waskito LA, Zein LH, Akil F, Uwan WB, Simanjuntak D, Wibawa ID, et al. 2016. Surveillance of Helicobacter pylori antibiotic susceptibility in Indonesia: different resistance types among regions and with novel genetic mutations. PLoS one. 11:e0166199.
  • Mirzaei N, Poursina F, Moghim S, Rahimi E, Safaei HG. 2014. The mutation of the rdxA gene in metronidazole-resistant Helicobacter pylori clinical isolates. Adv Biomed Res. 3:90.
  • Monno R, Giorgio F, Carmine P, Soleo L, Cinquepalmi V, Ierardi E. 2012. Helicobacter pylori clarithromycin resistance detected by Etest and TaqMan real-time polymerase chain reaction: a comparative study. APMIS. 120:712–717.
  • Mori H, Suzuki H, Matsuzaki J, Tsugawa H, Fukuhara S, Miyoshi S, Hirata K, Seino T, Matsushita M, Nishizawa T, et al. 2016. Rifabutin-based 10-day and 14-day triple therapy as a third-line and fourth-line regimen for Helicobacter pylori eradication: a pilot study. United Eur Gastroenterol J. 4:380–387.
  • Murakami K, Okimoto T, Kodama M, Tanahashi J, Fujioka T, Ikeda F, Muraoka H, Takigawa M, Saika T, Hasegawa M, et al. 2009. Sitafloxacin activity against Helicobacter pylori isolates, including those with gyrA mutations. Antimicrob Agents Chemother. 53:3097–3099.
  • Narayana JL, Huang HN, Wu CJ, Chen JY. 2015. Epinecidin-1 antimicrobial activity: in vitro membrane lysis and in vivo efficacy against Helicobacter pylori infection in a mouse model. Biomaterials. 61:41–51.
  • Nebert DW, Wikvall K, Miller WL. 2013. Human cytochromes P450 in health and disease. Philos Trans R Soc Lond, B, Biol Sci. 368:20120431.
  • Ng CG, Loke MF, Goh KL, Vadivelu J, Ho B. 2017. Biofilm formation enhances Helicobacter pylori survivability in vegetables. Food Microbiol. 62:68–76.
  • Nishizawa T, Suzuki H, Matsuzaki J, Muraoka H, Tsugawa H, Hirata K, Hibi T. 2011. Helicobacter pylori resistance to rifabutin in the last 7 years. Antimicrob Agents Chemother. 55:5374–5375.
  • Ojetti V, Migneco A, Zocco MA, Nista EC, Gasbarrini G, Gasbarrini A. 2004. Beta-lactamase inhibitor enhances Helicobacter pylori eradication rate. J Intern Med. 255:125–129.
  • Ontsira Ngoyi EN, Atipo Ibara BI, Moyen R, Ahoui Apendi PC, Ibara JR, Obengui O, Ossibi Ibara RB, Nguimbi E, Niama RF, Ouamba JM, et al. 2015. Molecular detection of Helicobacter pylori and its antimicrobial resistance in Brazzaville, Congo. Helicobacter. 20:316–320.
  • Ormeci A, Emrence Z, Baran B, Gokturk S, Soyer OM, Evirgen S, Akyuz F, Karaca C, Besisik F, Kaymakoglu S, et al. 2016. Effect of cytochrome P450 2C19 polymorphisms on the Helicobacter pylori eradication rate following two-week triple therapy with pantoprazole or rabeprazole. Eur Rev Med Pharmacol Sci. 20:879–885.
  • Parreira P, Fatima Duarte M, Reis CA, Martins MC. 2016. Helicobacter pylori infection: a brief overview on alternative natural treatments to conventional therapy. Crit Rev Microbiol. 42:94–105.
  • Paulsen IT, Chen J, Nelson KE, Saier MH, Jr. 2001. Comparative genomics of microbial drug efflux systems. J Mol Microbiol Biotechnol. 3(2):145–150.
  • Phan TN, Santona A, Tran VH, Tran TN, Le VA, Cappuccinelli P, Rubino S, Paglietti B. 2015. High rate of levofloxacin resistance in a background of clarithromycin- and metronidazole-resistant Helicobacter pylori in Vietnam. Int J Antimicrob Agents. 45:244–248.
  • Prabhudesai PP, Jain S, Keshvani A, Kulkarni KP. 2011. The efficacy and safety of amoxicillin-clavulanic acid 1000/125mg twice daily extended release (XR) tablet for the treatment of bacterial community-acquired pneumonia in adults. J Indian Med Assoc. 109:124–127.
  • Quek C, Pham ST, Tran KT, Pham BT, Huynh LV, Luu NB, Le TK, Quek K, Pham VH. 2016. Antimicrobial susceptibility and clarithromycin resistance patterns of Helicobacter pylori clinical isolates in Vietnam. F1000Res. 5:671.
  • Qureshi NN, Gallaher B, Schiller NL. 2014. Evolution of amoxicillin resistance of Helicobacter pylori in vitro: characterization of resistance mechanisms. Microb Drug Resist. 20:509–516.
  • Rajper S, Khan E, Ahmad Z, Alam SM, Akbar A, Hasan R. 2012. Macrolide and fluoroquinolone resistance in Helicobacter pylori isolates: an experience at a tertiary care centre in Pakistan. JPMA J Pak Med Assoc. 62:1140–1144.
  • Ramzy I, Elgarem H, Hamza I, Ghaith D, Elbaz T, Elhosary W, Mostafa G, Elzahry MA. 2016. Genetic mutations affecting the first line eradication therapy of Helicobacter pylori-infected Egyptian patients. Rev Inst Med Trop Sao Paulo. 58:88.
  • Rasheed F, Campbell BJ, Alfizah H, Varro A, Zahra R, Yamaoka Y, Pritchard DM. 2014. Analysis of clinical isolates of Helicobacter pylori in Pakistan reveals high degrees of pathogenicity and high frequencies of antibiotic resistance. Helicobacter. 19:387–399.
  • Rimbara E, Noguchi N, Kawai T, Sasatsu M. 2008. Mutations in penicillin-binding proteins 1, 2 and 3 are responsible for amoxicillin resistance in Helicobacter pylori. J Antimicrob Chemother. 61:995–998.
  • Rimbara E, Noguchi N, Kawai T, Sasatsu M. 2012. Fluoroquinolone resistance in Helicobacter pylori: role of mutations at position 87 and 91 of GyrA on the level of resistance and identification of a resistance conferring mutation in GyrB. Helicobacter. 17:36–42.
  • Saito Y, Serizawa H, Kato Y, Nakano M, Nakamura M, Saito H, Suzuki H, Kanai T. 2015. First-line eradication for Helicobacter pylori-positive gastritis by esomeprazole-based triple therapy is influenced by CYP2C19 genotype. World J Gastroenterol. 21:13548–13554.
  • Sanches BS, Martins GM, Lima K, Cota B, Moretzsohn LD, Ribeiro LT, Breyer HP, Maguilnik I, Maia AB, Rezende-Filho J, et al. 2016. Detection of Helicobacter pylori resistance to clarithromycin and fluoroquinolones in Brazil: a national survey. World J Gastroenterol. 22:7587–7594.
  • Schmitt BH, Regner M, Mangold KA, Thomson RB Jr, Kaul KL. 2013. PCR detection of clarithromycin-susceptible and -resistant Helicobacter pylori from formalin-fixed, paraffin-embedded gastric biopsies. Mod Pathol. 26:1222–1227.
  • Seck A, Burucoa C, Dia D, Mbengue M, Onambele M, Raymond J, Breurec S. 2013. Primary antibiotic resistance and associated mechanisms in Helicobacter pylori isolates from Senegalese patients. Ann Clin Microbiol Antimicrob. 12:3.
  • Secka O, Berg DE, Antonio M, Corrah T, Tapgun M, Walton R, Thomas V, Galano JJ, Sancho J, Adegbola RA, et al. 2013. Antimicrobial susceptibility and resistance patterns among Helicobacter pylori strains from The Gambia, West Africa. Antimicrob Agents Chemother. 57:1231–1237.
  • Selgrad M, Tammer I, Langner C, Bornschein J, Meissle J, Kandulski A, Varbanova M, Wex T, Schluter D, Malfertheiner P. 2014. Different antibiotic susceptibility between antrum and corpus of the stomach, a possible reason for treatment failure of Helicobacter pylori infection. World J Gastroenterol. 20:16245–16251.
  • Shiota S, Nguyen LT, Murakami K, Kuroda A, Mizukami K, Okimoto T, Kodama M, Fujioka T, Yamaoka Y. 2012. Association of helicobacter pylori dupA with the failure of primary eradication. J Clin Gastroenterol. 46:297–301.
  • Skvarc M, Kopitar AN, Kos J, Obermajer N, Tepes B. 2014. Differences in the antigens of Helicobacter pylori strains influence on the innate immune response in the in vitro experiments. Mediators Inflamm. 2014:287531.
  • Smiley R, Bailey J, Sethuraman M, Posecion N, Showkat Ali M. 2013. Comparative proteomics analysis of sarcosine insoluble outer membrane proteins from clarithromycin resistant and sensitive strains of Helicobacter pylori. J Microbiol (Seoul, Korea). 51:612–618.
  • Stark RM, Gerwig GJ, Pitman RS, Potts LF, Williams NA, Greenman J, Weinzweig IP, Hirst TR, Millar MR. 1999. Biofilm formation by Helicobacter pylori. Lett Appl Microbiol. 28:121–126.
  • Stokkers PC, van Aken BE, Basoski N, Reitsma PH, Tytgat GN, van Deventer SJ. 1998. Five genetic markers in the interleukin 1 family in relation to inflammatory bowel disease. Gut. 43:33–39.
  • Sugano K, Tack J, Kuipers EJ, Graham DY, El-Omar EM, Miura S, Haruma K, Asaka M, Uemura N, Malfertheiner P, et al. 2015. Kyoto global consensus report on Helicobacter pylori gastritis. Gut. 64:1353–1367.
  • Sugimoto M, Furuta T, Shirai N, Ikuma M, Hishida A, Ishizaki T. 2006. Influences of proinflammatory and anti-inflammatory cytokine polymorphisms on eradication rates of clarithromycin-sensitive strains of Helicobacter pylori by triple therapy. Clin Pharmacol Ther. 80:41–50.
  • Sugimoto M, Uotani T, Sahara S, Ichikawa H, Yamade M, Sugimoto K, Furuta T. 2014. Efficacy of tailored Helicobacter pylori eradication treatment based on clarithromycin susceptibility and maintenance of acid secretion. Helicobacter. 19(4):312–318.
  • Sugimoto M, Yamaoka Y. 2009. Virulence factor genotypes of Helicobacter pylori affect cure rates of eradication therapy. Arch Immunol Ther Exp (Warsz). 57:45–56.
  • Suzuki RB, Lopes RA, da Camara Lopes GA, Hung Ho T, Speranca MA. 2013. Low Helicobacter pylori primary resistance to clarithromycin in gastric biopsy specimens from dyspeptic patients of a city in the interior of São Paulo, Brazil. BMC Gastroenterol. 13:164.
  • Suzuki S, Suzuki H, Nishizawa T, Kaneko F, Ootani S, Muraoka H, Saito Y, Kobayashi I, Hibi T. 2009. Past rifampicin dosing determines rifabutin resistance of Helicobacter pylori. Digestion. 79:1–4.
  • Tanih NF, Ndip LM, Ndip RN. 2011. Characterisation of the genes encoding resistance to metronidazole (rdxA and frxA) and clarithromycin (the 23S-rRNA genes) in South African isolates of Helicobacter pylori. Ann Trop Med Parasitol. 105:251–259.
  • Tanih NF, Ndip RN. 2013. Molecular detection of antibiotic resistance in South African isolates of Helicobacter pylori. Gastroenterol Res Pract. 2013:259457.
  • Tarlow JK, Blakemore AI, Lennard A, Solari R, Hughes HN, Steinkasserer A, Duff GW. 1993. Polymorphism in human IL-1 receptor antagonist gene intron 2 is caused by variable numbers of an 86-bp tandem repeat. Hum Genet. 91:403–404.
  • Tavira B, Gomez J, Diaz-Corte C, Suarez B, Coronel D, Arias M, Lopez-Larrea C, Iglesias S, Alonso B, Rodrigo E, et al. 2015. ABCB1 (MDR-1) pharmacogenetics of tacrolimus in renal transplanted patients: a Next Generation Sequencing approach. Clin Chem Lab Med. 53:1515–1519.
  • Teh X, Khosravi Y, Lee WC, Leow AH, Loke MF, Vadivelu J, Goh KL. 2014. Functional and molecular surveillance of Helicobacter pylori antibiotic resistance in Kuala Lumpur. PLoS One. 9:e101481.
  • Thung I, Aramin H, Vavinskaya V, Gupta S, Park JY, Crowe SE, Valasek MA. 2016. Review article: the global emergence of Helicobacter pylori antibiotic resistance. Aliment Pharmacol Ther. 43:514–533.
  • Toledo H, Lopez SR. 2010. Tetracycline resistance in Chilean clinical isolates of Helicobacter pylori. J Antimicrob Chemother. 65:470–473.
  • Treiber G, Wittig J, Ammon S, Walker S, van Doorn LJ, Klotz U. 2002. Clinical outcome and influencing factors of a new short-term quadruple therapy for Helicobacter pylori eradication: a randomized controlled trial (MACLOR study). Arch Intern Med. 162:153–160.
  • Trespalacios AA, Otero W, Caminos JE, Mercado MM, Avila J, Rosero LE, Arevalo A, Poutou-Pinales RA, Graham DY. 2013. Phenotypic and genotypic analysis of clarithromycin-resistant Helicobacter pylori from Bogota D.C., Colombia. J Microbiol. 51:448–452.
  • Trespalacios AA, Rimbara E, Otero W, Reddy R, Graham DY. 2015. Improved allele-specific PCR assays for detection of clarithromycin and fluoroquinolone resistant of Helicobacter pylori in gastric biopsies: identification of N87I mutation in GyrA. Diagn Microbiol Infect Dis. 81:251–255.
  • Trespalacios-Rangel AA, Otero W, Arevalo-Galvis A, Poutou-Pinales RA, Rimbara E, Graham DY. 2016. Surveillance of levofloxacin resistance in Helicobacter pylori isolates in Bogotá-Colombia (2009–2014). PLoS One. 11:e0160007.
  • Tseng YS, Wu DC, Chang CY, Kuo CH, Yang YC, Jan CM, Su YC, Kuo FC, Chang LL. 2009. Amoxicillin resistance with beta-lactamase production in Helicobacter pylori. Eur J Clin Invest. 39:807–812.
  • Tu IF, Liao JH, Yang FL, Lin NT, Chan HL, Wu SH. 2014. Lon protease affects the RdxA nitroreductase activity and metronidazole susceptibility in Helicobacter pylori. Helicobacter. 19:356–366.
  • 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.
  • van Doorn LJ, Schneeberger PM, Nouhan N, Plaisier AP, Quint WG, de Boer WA. 2000. Importance of Helicobacter pylori cagA and vacA status for the efficacy of antibiotic treatment. Gut. 46:321–326.
  • Vangsted AJ, Klausen TW, Abildgaard N, Andersen NF, Gimsing P, Gregersen H, Nexo BA, Vogel U. 2011. Single nucleotide polymorphisms in the promoter region of the IL1B gene influence outcome in multiple myeloma patients treated with high-dose chemotherapy independently of relapse treatment with thalidomide and bortezomib. Ann Hematol. 90:1173–1181.
  • Wang YH, Lv ZF, Zhong Y, Liu DS, Chen SP, Xie Y. 2017. The internalization of Helicobacter pylori plays a role in the failure of H. pylori eradication. Helicobacter. 22. doi: 10.1111/hel.12324
  • Wu JY, Wang SS, Lee YC, Yamaoka Y, Graham DY, Jan CM, Wang WM, Wu DC. 2014. Detection of genotypic clarithromycin-resistant Helicobacter pylori by string tests. World J Gastroenterol. 20:3343–3349.
  • Wueppenhorst N, Stueger HP, Kist M, Glocker E. 2009. Identification and molecular characterization of triple- and quadruple-resistant Helicobacter pylori clinical isolates in Germany. J Antimicrob Chemother. 63:648–653.
  • Yamade M, Sugimoto M, Uotani T, Nishino M, Kodaira C, Furuta T. 2011. Resistance of Helicobacter pylori to quinolones and clarithromycin assessed by genetic testing in Japan. J Gastroenterol Hepatol. 26:1457–1461.
  • Yonezawa H, Osaki T, Hanawa T, Kurata S, Ochiai K, Kamiya S. 2013. Impact of Helicobacter pylori biofilm formation on clarithromycin susceptibility and generation of resistance mutations. PLoS One. 8:e73301.
  • Zambon CF, Fasolo M, Basso D, D'Odorico A, Stranges A, Navaglia F, Fogar P, Greco E, Schiavon S, Padoan A, et al. 2007. Clarithromycin resistance, tumor necrosis factor alpha gene polymorphism and mucosal inflammation affect H. pylori eradication success. J Gastrointest Surg. 11:1506–1514.
  • Zerbetto De Palma G, Mendiondo N, Wonaga A, Viola L, Ibarra D, Campitelli E, Salim N, Corti R, Goldman C, Catalano M. 2016. Occurrence of mutations in the antimicrobial target genes related to levofloxacin, clarithromycin, and amoxicillin resistance in Helicobacter pylori isolates from Buenos Aires City. Microbial Drug Resist. 23:351–358.
  • Zhang L, Mei Q, Li QS, Hu YM, Xu JM. 2010. The effect of cytochrome P2C19 and interleukin-1 polymorphisms on H. pylori eradication rate of 1-week triple therapy with omeprazole or rabeprazole, amoxycillin and clarithromycin in Chinese people. J Clin Pharm Ther. 35:713–722.
  • Zhang YX, Zhou LY, Song ZQ, Zhang JZ, He LH, Ding Y. 2015. Primary antibiotic resistance of Helicobacter pylori strains isolated from patients with dyspeptic symptoms in Beijing: a prospective serial study. World J Gastroenterol. 21:2786–2792.
  • Zhao LJ, Huang YQ, Chen BP, Mo XQ, Huang ZS, Huang XF, Wei LD, Wei HY, Chen YH, Tang HY, et al. 2014. Helicobacter pylori isolates from ethnic minority patients in Guangxi: resistance rates, mechanisms, and genotype. World J Gastroenterol. 20:4761–4770.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.