Identification of plasmid-mediated quinolone resistance genes in Helicobacter pylori isolates from gastrointestinal patients
-
Adeleh Attar
,
Parastoo Asadolahi
,
Maryam Mohammadbeigi
,
Amir Peymani
,
Amir Javadi
,
Rasoul Samimi
Abstract
Background and Objectives: The expanding antibiotic resistance of Helicobacter pylori isolates is a critical concern for global health. This research aimed to evaluate the prevalence of PMQR genes, including qnrA1-6, qnrB4, qnrB1, qnrS, qepA, and aac(6´)Ib-cr, among H. pylori strains isolated from patients at Qazvin Hospital.
Materials and Methods: In this study, 212 patients with gastrointestinal diseases who were referred to Qazvin Hospital underwent endoscopy, and gastric biopsies were collected. H. pylori isolates were confirmed by biochemical and molecular tests. PCR was performed to detect the virulence genes babA2 and sabA. Subsequently, the presence of the PMQR genes qnrA1-6, qnrB4, qnrS, qnrB1, qepA, and aac(6')Ib-cr were molecularly identified.
Results: 149 (70%) of isolates were phenotypically and molecularly confirmed as H. pylori isolates. Of the 149 isolates, 102 isolates (68.45%) with babA2 and 120 isolates (80.53%) with sabA genes were identified. frequencies of the genes qnrA1-6, qnrB4, qnrB1, and qepA were 8 (5.36%), 4 (2.68%), 12 (8.05%), and 13 (8.72%), respectively. Notably, qnrS and aac(6´)Ib-cr genes were not detected in isolates.
Conclusion: The findings of this study confirm that regular monitoring of antibiotic resistance genes is essential to prevent the further spread of PMQR resistance genes and to optimize clinical decision-making.
1. Sonnenberg A. Epidemiology of Helicobacter pylori. Aliment Pharmacol Ther 2022;55:S1-S13.
2. Aumpan N, Mahachai V, Vilaichone Rk. Management of Helicobacter pylori infection. JGH open 2023;7:3-15.
3. Sjomina O, Pavlova J, Niv Y, Leja M. Epidemiology of Helicobacter pylori infection. Helicobacter 2018;23:e12514.
4. Al-Fakhrany OM, Elekhnawy E. Helicobacter pylori in the post-antibiotics era: from virulence factors to new drug targets and therapeutic agents. Arch Microbiol 2023;205:301.
5. Кадхим АС, Ал-Карави АС. Insights into the Pathogenesis, Virulence Factors, and Diagnosis of Helicobacter pylori: A Comprehensive Review. in Library 2023;1:31-37.
6. Picoli SU, Mazzoleni LE, Fernández H, De Bona LR, Neuhauss E, Longo L, et al. Resistance to amoxicillin, clarithromycin and ciprofloxacin of Helicobacter pylori isolated from Southern Brazil patients. Rev Inst Med Trop Sao Paulo 2014;56:197-200.
7. Sousa C, Ferreira R, Azevedo NF, Oleastro M, Azeredo J, Figueiredo C, et al. Helicobacter pylori infection: from standard to alternative treatment strategies. Crit Rev Microbiol 2022;48:376-96.
8. Borka Balas R, Meliț LE, Mărginean CO. Current worldwide trends in pediatric Helicobacter pylori antimicrobial resistance. Children 2023;10:403.
9. Malfertheiner P, Mégraud F, O'Morain CA, Gisbert JP, Kuipers EJ, Axon AT, et al. Management of Helicobacter pylori infection—the Maastricht V/Florence consensus report. Gut 2017;66:6-30.
10. Sholeh M, Maleki F, Krutova M, Bavari S, Golmoradi R, Sadeghifard N, et al. The increasing antimicrobial resistance of Helicobacter pylori in Iran: a systematic review and meta‐analysis. Helicobacter 2020;25(5):e12730.
11. Khademi F, Sahebkar A. An updated systematic review and meta-analysis on the Helicobacter pylori antibiotic resistance in Iran (2010–2020). Microb Drug Resist 2020;26:1186-1194.
12. Foegeding NJ, Caston RR, McClain MS, Ohi MD, Cover TL. An overview of Helicobacter pylori VacA toxin biology. Toxins 2016;8:173.
13. Gong Y, Yuan Y. Resistance mechanisms of Helicobacter pylori and its dual target precise therapy. Crit Rev Microbiol 2018;44:371-392.
14. Ho JJ, Navarro M, Sawyer K, Elfanagely Y, Moss SF. Helicobacter pylori antibiotic resistance in the United States between 2011 and 2021: a systematic review and meta-analysis. Am J Gastroenterol 2022;117:1221-1230.
15. Chen J, Li P, Huang Y, Guo Y, Ding Z, Lu H. Primary antibiotic resistance of Helicobacter pylori in different regions of China: a systematic review and meta-analysis. Pathogens 2022;11:786.
16. Hadavand F, Vahdat K, Yazdani S, Motamed N. Levofloxacin Resistance in Blood and Urine Culture Samples in Khalij Fars Hospital of Bushehr. Iran South Med J 2017;20:492-500.
17. Lotfollahi Hagghi L, Abbasi Eslamloo A, Gheibi S. Evaluation of antibiotic resistance patterns in patients admitted to intensive care units of imam khomeini teaching hospitals, Urmia. Stud Med Sci 2023;34:651-660.
18. Gisbert JP. Optimization strategies aimed to increase the efficacy of Helicobacter pylori eradication therapies with quinolones. Molecules 2020;25:5084.
19. Tariq H, Patel H, Kamal MU, Abbas N, Ameen M, Azam S, et al. Reevaluation of the efficacy of first line regimen for Helicobacter pylori. Clin Exp Gastroenterol 2020:25-33.
20. Umar Z, Tang J-W, Marshall BJ, Tay ACY, Wang L. Rapid diagnosis and precision treatment of Helicobacter pylori infection in clinical settings. Crit Rev Microbiol 2024:1-30.
21. Saniee P, HosseinI F, Kadkhodaei S, Siavoshi F, Khalili-Saman S. Helicobacter pylori multidrug resistance due to misuse of antibiotics in Iran. Arch Iran Med 2018;21:283-288.
22. Zhang Y, Wen Y, Xiao Q, Zheng W, Long G, Chen B, et al. Mutations in the antibiotic target genes related to clarithromycin, metronidazole and levofloxacin resistance in Helicobacter pylori strains from children in China. Infect Drug Resist 2020:311-322.
23. Hooper DC, Jacoby GA. Mechanisms of drug resistance: quinolone resistance. Ann N Y Acad Sci 2015;1354:12-31.
24. Vasala A, Hytönen VP, Laitinen OH. Modern tools for rapid diagnostics of antimicrobial resistance. Front Cell Infect Microbiol 2020;10:308.
25. Bujanda L, Nyssen OP, Vaira D, Saracino IM, Fiorini G, Lerang F, et al. Antibiotic resistance prevalence and trends in patients infected with Helicobacter pylori in the period 2013–2020: Results of the European Registry on H. pylori Management (Hp-EuReg). Antibiotics 2021;10:1058.
26. Cardos AI, Maghiar A, Zaha DC, Pop O, Fritea L, Miere F, et al. Evolution of diagnostic methods for Helicobacter pylori infections: from traditional tests to high technology, advanced sensitivity and discrimination tools. Diagnostics 2022;12:508.
27. Schulze RJ, Schott MB, Casey CA, Tuma PL, McNiven MA. The cell biology of the hepatocyte: A membrane trafficking machine. J Cell Biol 2019;218:2096-2112.
28. Ohlsson B. The role of smoking and alcohol behaviour in management of functional gastrointestinal disorders. Best Pract Res Clin Gastroenterol 2017;31:545-552.
29. Xu C, Soyfoo DM, Wu Y, Xu S. Virulence of Helicobacter pylori outer membrane proteins: an updated review. Eur J Clin Microbiol Infect Dis 2020;39:1821-1830.
30. Zhao Q, Song C, Wang K, Li D, Yang Y, Liu D, et al. Prevalence of Helicobacter pylori babA, oipA, sabA, and homB genes in isolates from Chinese patients with different gastroduodenal diseases. Med Microbiol Immunol 2020;209:565-577.
31. Megraud F, Bruyndonckx R, Coenen S, Wittkop L, Huang T-D, Hoebeke M, et al. Helicobacter pylori resistance to antibiotics in Europe in 2018 and its relationship to antibiotic consumption in the community. Gut 2021;70:1815-1822.
32. Wang Z, Jang HM. Comparative study on characteristics and mechanism of levofloxacin adsorption on swine manure biochar. Bioresour Technol 2022;351:127025.
33. Rezaei S, Tajbakhsh S, Naeimi B, Yousefi F. Investigation of gyrA and parC mutations and the prevalence of plasmid-mediated quinolone resistance genes in Klebsiella pneumoniae clinical isolates. BMC Microbiol 2024;24:265.
34. Talebi Bezmin Abadi A, Ghasemzadeh A, Taghvaei T, Mobarez AM. Primary resistance of Helicobacter pylori to levofloxacin and moxifloxacine in Iran. Intern Emerg Med 2012;7:447-452.
35. Mokhtari-Farsani A, Doosti A, Mohammadalipour Z. Presence of Qnr genes related to resistance to quinolones, first-, second-and third-generation in diarrhoeagenic Escherichia coli. J Patient Safety Infection Contens 2016;4:5-9.
36. Bluemel B, Goelz H, Goldmann B, Grüger J, Hamel H, Loley K, et al. Antimicrobial resistance of Helicobacter pylori in Germany, 2015 to 2018. Clin Microbiol Infect 2020;26:235-239.
37. Yan L, Liu D, Wang X-H, Wang Y, Zhang B, Wang M, et al. Bacterial plasmid-mediated quinolone resistance genes in aquatic environments in China. Sci Rep 2017;7:40610.
2. Aumpan N, Mahachai V, Vilaichone Rk. Management of Helicobacter pylori infection. JGH open 2023;7:3-15.
3. Sjomina O, Pavlova J, Niv Y, Leja M. Epidemiology of Helicobacter pylori infection. Helicobacter 2018;23:e12514.
4. Al-Fakhrany OM, Elekhnawy E. Helicobacter pylori in the post-antibiotics era: from virulence factors to new drug targets and therapeutic agents. Arch Microbiol 2023;205:301.
5. Кадхим АС, Ал-Карави АС. Insights into the Pathogenesis, Virulence Factors, and Diagnosis of Helicobacter pylori: A Comprehensive Review. in Library 2023;1:31-37.
6. Picoli SU, Mazzoleni LE, Fernández H, De Bona LR, Neuhauss E, Longo L, et al. Resistance to amoxicillin, clarithromycin and ciprofloxacin of Helicobacter pylori isolated from Southern Brazil patients. Rev Inst Med Trop Sao Paulo 2014;56:197-200.
7. Sousa C, Ferreira R, Azevedo NF, Oleastro M, Azeredo J, Figueiredo C, et al. Helicobacter pylori infection: from standard to alternative treatment strategies. Crit Rev Microbiol 2022;48:376-96.
8. Borka Balas R, Meliț LE, Mărginean CO. Current worldwide trends in pediatric Helicobacter pylori antimicrobial resistance. Children 2023;10:403.
9. Malfertheiner P, Mégraud F, O'Morain CA, Gisbert JP, Kuipers EJ, Axon AT, et al. Management of Helicobacter pylori infection—the Maastricht V/Florence consensus report. Gut 2017;66:6-30.
10. Sholeh M, Maleki F, Krutova M, Bavari S, Golmoradi R, Sadeghifard N, et al. The increasing antimicrobial resistance of Helicobacter pylori in Iran: a systematic review and meta‐analysis. Helicobacter 2020;25(5):e12730.
11. Khademi F, Sahebkar A. An updated systematic review and meta-analysis on the Helicobacter pylori antibiotic resistance in Iran (2010–2020). Microb Drug Resist 2020;26:1186-1194.
12. Foegeding NJ, Caston RR, McClain MS, Ohi MD, Cover TL. An overview of Helicobacter pylori VacA toxin biology. Toxins 2016;8:173.
13. Gong Y, Yuan Y. Resistance mechanisms of Helicobacter pylori and its dual target precise therapy. Crit Rev Microbiol 2018;44:371-392.
14. Ho JJ, Navarro M, Sawyer K, Elfanagely Y, Moss SF. Helicobacter pylori antibiotic resistance in the United States between 2011 and 2021: a systematic review and meta-analysis. Am J Gastroenterol 2022;117:1221-1230.
15. Chen J, Li P, Huang Y, Guo Y, Ding Z, Lu H. Primary antibiotic resistance of Helicobacter pylori in different regions of China: a systematic review and meta-analysis. Pathogens 2022;11:786.
16. Hadavand F, Vahdat K, Yazdani S, Motamed N. Levofloxacin Resistance in Blood and Urine Culture Samples in Khalij Fars Hospital of Bushehr. Iran South Med J 2017;20:492-500.
17. Lotfollahi Hagghi L, Abbasi Eslamloo A, Gheibi S. Evaluation of antibiotic resistance patterns in patients admitted to intensive care units of imam khomeini teaching hospitals, Urmia. Stud Med Sci 2023;34:651-660.
18. Gisbert JP. Optimization strategies aimed to increase the efficacy of Helicobacter pylori eradication therapies with quinolones. Molecules 2020;25:5084.
19. Tariq H, Patel H, Kamal MU, Abbas N, Ameen M, Azam S, et al. Reevaluation of the efficacy of first line regimen for Helicobacter pylori. Clin Exp Gastroenterol 2020:25-33.
20. Umar Z, Tang J-W, Marshall BJ, Tay ACY, Wang L. Rapid diagnosis and precision treatment of Helicobacter pylori infection in clinical settings. Crit Rev Microbiol 2024:1-30.
21. Saniee P, HosseinI F, Kadkhodaei S, Siavoshi F, Khalili-Saman S. Helicobacter pylori multidrug resistance due to misuse of antibiotics in Iran. Arch Iran Med 2018;21:283-288.
22. Zhang Y, Wen Y, Xiao Q, Zheng W, Long G, Chen B, et al. Mutations in the antibiotic target genes related to clarithromycin, metronidazole and levofloxacin resistance in Helicobacter pylori strains from children in China. Infect Drug Resist 2020:311-322.
23. Hooper DC, Jacoby GA. Mechanisms of drug resistance: quinolone resistance. Ann N Y Acad Sci 2015;1354:12-31.
24. Vasala A, Hytönen VP, Laitinen OH. Modern tools for rapid diagnostics of antimicrobial resistance. Front Cell Infect Microbiol 2020;10:308.
25. Bujanda L, Nyssen OP, Vaira D, Saracino IM, Fiorini G, Lerang F, et al. Antibiotic resistance prevalence and trends in patients infected with Helicobacter pylori in the period 2013–2020: Results of the European Registry on H. pylori Management (Hp-EuReg). Antibiotics 2021;10:1058.
26. Cardos AI, Maghiar A, Zaha DC, Pop O, Fritea L, Miere F, et al. Evolution of diagnostic methods for Helicobacter pylori infections: from traditional tests to high technology, advanced sensitivity and discrimination tools. Diagnostics 2022;12:508.
27. Schulze RJ, Schott MB, Casey CA, Tuma PL, McNiven MA. The cell biology of the hepatocyte: A membrane trafficking machine. J Cell Biol 2019;218:2096-2112.
28. Ohlsson B. The role of smoking and alcohol behaviour in management of functional gastrointestinal disorders. Best Pract Res Clin Gastroenterol 2017;31:545-552.
29. Xu C, Soyfoo DM, Wu Y, Xu S. Virulence of Helicobacter pylori outer membrane proteins: an updated review. Eur J Clin Microbiol Infect Dis 2020;39:1821-1830.
30. Zhao Q, Song C, Wang K, Li D, Yang Y, Liu D, et al. Prevalence of Helicobacter pylori babA, oipA, sabA, and homB genes in isolates from Chinese patients with different gastroduodenal diseases. Med Microbiol Immunol 2020;209:565-577.
31. Megraud F, Bruyndonckx R, Coenen S, Wittkop L, Huang T-D, Hoebeke M, et al. Helicobacter pylori resistance to antibiotics in Europe in 2018 and its relationship to antibiotic consumption in the community. Gut 2021;70:1815-1822.
32. Wang Z, Jang HM. Comparative study on characteristics and mechanism of levofloxacin adsorption on swine manure biochar. Bioresour Technol 2022;351:127025.
33. Rezaei S, Tajbakhsh S, Naeimi B, Yousefi F. Investigation of gyrA and parC mutations and the prevalence of plasmid-mediated quinolone resistance genes in Klebsiella pneumoniae clinical isolates. BMC Microbiol 2024;24:265.
34. Talebi Bezmin Abadi A, Ghasemzadeh A, Taghvaei T, Mobarez AM. Primary resistance of Helicobacter pylori to levofloxacin and moxifloxacine in Iran. Intern Emerg Med 2012;7:447-452.
35. Mokhtari-Farsani A, Doosti A, Mohammadalipour Z. Presence of Qnr genes related to resistance to quinolones, first-, second-and third-generation in diarrhoeagenic Escherichia coli. J Patient Safety Infection Contens 2016;4:5-9.
36. Bluemel B, Goelz H, Goldmann B, Grüger J, Hamel H, Loley K, et al. Antimicrobial resistance of Helicobacter pylori in Germany, 2015 to 2018. Clin Microbiol Infect 2020;26:235-239.
37. Yan L, Liu D, Wang X-H, Wang Y, Zhang B, Wang M, et al. Bacterial plasmid-mediated quinolone resistance genes in aquatic environments in China. Sci Rep 2017;7:40610.
| Files | ||
| Issue | Vol 18 No 2 (2026) | |
| Section | Original Article(s) | |
| Keywords | ||
| Helicobacter pylori Quinolones Drug resistance Plasmid Gastrointestinal diseases | ||
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How to Cite
1.
Attar A, Asadolahi P, Mohammadbeigi M, Peymani A, Javadi A, Samimi R. Identification of plasmid-mediated quinolone resistance genes in Helicobacter pylori isolates from gastrointestinal patients. Iran J Microbiol. 2026;18(2):226-234.
