Ann Clin Microbiol.  2024 Mar;27(1):19-30. 10.5145/ACM.2024.27.1.4.

Prevalence of Helicobacter pylori infection and clarithromycin resistance rate from 2015 to 2018 using the laboratory information system of the Seegene Medical Foundation in Korea: a repeated cross-sectional study

• Jung S
• Kim MN
• Yong D
• Lee M
• Lee J
• Lee HK
• Lee MK
• Helicobacter Study Group

• KMID: 2556215
• DOI: http://doi.org/10.5145/ACM.2024.27.1.4

Abstract

Background
Numerous studies have examined the prevalence of Helicobacter pylori infection and clarithromycin (CLA) resistance rate of H. pylori. However, in South Korea, there is a lack of research analyzing specimens from local clinics and hospitals using molecular methods. This study aimed to assess the prevalence of H. pylori infection and CLA resistance across sex and age groups, as well as to explore regional variations in CLA resistance and its characteristics.
Methods
Data from a laboratory information system from 2015 to 2018 were retrospectively analyzed to determine the prevalence of H. pylori infection and CLA resistance rate. The 23S ribosomal RNA genes of H. pylori were analyzed using a dual priming oligonucleotide-based multiplex polymerase chain reaction method.
Results
The overall prevalence of H. pylori infection was 50.5%(12,000/23,773), with a significantly higher prevalence among males (53.5%) than females (47.0%). The CLA resistance rate was 28.3%, with a significantly higher rate among females (34.9%) than males (23.8%). Age group analysis revealed that the highest prevalence of H. pylori infection was among individuals in their 40s, whereas the highest CLA resistance rate was observed among those in their 60s. The CLA resistance rate exhibited an upward trend and varied among patients based on their place of residence, and A2143G mutation was the most prevalent across all regions.
Conclusion
The prevalence of H. pylori infection and CLA resistance rate in Korea remain high and vary according to sex, age, and region. To effectively eradicate H. pylori, it is crucial to periodically monitor regional CLA resistance patterns and conduct CLA susceptibility testing before prescription.

Keyword

Helicobacter pylori; clarithromycin; resistance; 23S ribosomal RNA; Korea

Reference

1. Malfertheiner P, Camargo MC, El-Omar E, Liou JM, Peek R, Schulz C, et al. Helicobacter pylori infection. Nat Rev Dis Primers 2023;9:19.

2. World Health Organization. WHO publishes list of bacteria for which new antibiotics are urgently needed. https://www.who.int/news/item/27-02-2017-who-publishes-list-of-bacteriafor-which-new-antibiotics-are-urgently-needed [Online] (last visited on 23 February 2024).

3. Hooi JKY, Lai WY, Ng WK, Suen MMY, Underwood FE, Tanyingoh D, et al. Global prevalence of Helicobacter pylori infection: systematic review and meta-analysis. Gastroenterology 2017;153:420-9.

4. Liou JM, Malfertheiner P, Lee YC, Sheu BS, Sugano K, Cheng HC, et al. Screening and eradication of Helicobacter pylori for gastric cancer prevention: the Taipei global consensus. Gut 2020;69:2093-112.

5. Lee JH, Ahn JY, Choi KD, Jung HY, Kim JM, Baik GH, et al. Nationwide antibiotic resistance mapping of Helicobacter pylori in Korea: a prospective multicenter study. Helicobacter 2019;24:e12592.

6. Lee YC, Chiang TH, Chou CK, Tu YK, Liao WC, Wu MS, et al. Association between Helicobacter pylori eradication and gastric cancer incidence: a systematic review and metaanalysis. Gastroenterology 2016;150:1113-24.e5.

7. Marques AT, Vítor JM, Santos A, Oleastro M, Vale FF. Trends in Helicobacter pylori resistance to clarithromycin: from phenotypic to genomic approaches. Microb Genom 2020;6:e000344.

8. Nishizawa T and Suzuki H. Mechanisms of Helicobacter pylori antibiotic resistance and molecular testing. Front Mol Biosci 2014;1:19.

9. Zou Y, Qian X, Liu X, Song Y, Song C, Wu S, et al. The effect of antibiotic resistance on Helicobacter pylori eradication efficacy: a systematic review and meta-analysis. Helicobacter 2020;25:e12714.

10. Malfertheiner P, Megraud 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.

11. Malfertheiner P, Megraud F, Rokkas T, Gisbert JP, Liou JM, Schulz C, et al. Management of Helicobacter pylori infection: the Maastricht VI/Florence consensus report. Gut 2022;71:172462.

12. Pohl D, Keller PM, Bordier V, Wagner K. Review of current diagnostic methods and advances in Helicobacter pylori diagnostics in the era of next generation sequencing. World J Gastroenterol 2019;25:4629-60.

13. Sholeh M, Khoshnood S, Azimi T, Mohamadi J, Kaviar VH, Hashemian M, et al. The prevalence of clarithromycin-resistant Helicobacter pylori isolates: a systematic review and meta-analysis. PeerJ 2023;11:e15121.

14. Yun JM, Kim JS, Ji JS, Kim BW, Choi H. Usefulness of dual priming oligonucleotidepolymerase chain reaction for diagnosis and treatment of Helicobacter pylori. Korean J Helicobacter Up Gastrointest Res 2016;16:147-51.

15. Lee HK, Chae HS, Kang JO, Lee MK, Sung H, Kim MN, et al. Multicenter study for the frequency of 23S rRNA point mutations associated with clarithromycin resistance in Helicobacter pylori in Korea. Korean J Clin Microbiol 2008;11:84-9.

16. Kim T, Song HJ, Shin SY, Kim JH, Na SY, Boo SJ, et al. Clarithromycin-resistant Helicobacter pylori associated with 23S rRNA point mutations in Jeju Island. Korean J Gastroenterol 2013;61:252-8.

17. Cho AR and Lee MK. A comparison analysis on the diagnosis of Helicobacter pylori infection and the detection of clarithromycin resistance according to biopsy sites. Korean J Lab Med 2010;30:381-7.

18. Jung MK, Lee JK, Heo J, Kang EJ, Lee YR. The effect of concomittent therarpy and quadruple therapy for patients who had 23S ribosomal ribonucleic acid mutated Helicobacter pylori in Daegu and Kyoungpook area. Korean J Helicobacter Up Gastrointest Res 2014;14:249-54.

19. Jeon JS, Kim JK, Kim GY. Detection of clarithromycin-resistant Helicobacter pylori by polymerase chain reaction using residual samples from rapid urease test. Indian J Med Microbiol 2017;35:406-9.

20. Chung WC, Jung SH, Oh JH, Kim TH, Cheung DY, Kim BW, et al. Dual-priming oligonucleotide-based multiplex PCR using tissue samples in rapid urease test in the detection of Helicobacter pylori infection. World J Gastroenterol 2014;20:6547-53.

21. Lee JH, Choi KD, Jung HY, Baik GH, Park JK, Kim SS, et al. Seroprevalence of Helicobacter pylori in Korea: a multicenter, nationwide study conducted in 2015 and 2016. Helicobacter 2018;23:e12463.

22. Lim SH, Kim N, Kwon JW, Kim SE, Baik GH, Lee JY, et al. Trends in the seroprevalence of Helicobacter pylori infection and its putative eradication rate over 18 years in Korea: a crosssectional nationwide multicenter study. PLoS One 2018;13:e0204762.

23. Inoue M. Changing epidemiology of Helicobacter pylori in Japan. Gastric Cancer 2017;20(Suppl 1):3-7.

24. Schröder W, Sommer H, Gladstone BP, Foschi F, Hellman J, Evengard B, et al. Gender differences in antibiotic prescribing in the community: a systematic review and meta-analysis. J Antimicrob Chemother 2016;71:1800-6.

25. Kocsmár É, Buzás GM, Szirtes I, Kocsmár I, Kramer Z, Szijártó A, et al. Primary and secondary clarithromycin resistance in Helicobacter pylori and mathematical modeling of the role of macrolides. Nat Commun 2021;12:2255.

26. De Francesco V, Margiotta M, Zullo A, Hassan C, Giorgio F, Burattini O, et al. Prevalence of primary clarithromycin resistance in Helicobacter pylori strains over a 15 year period in Italy. J Antimicrob Chemother 2007;59:783-5.

27. Chang YW, Ko WJ, Oh CH, Park YM, Oh SJ, Moon JR, et al. Clarithromycin resistance and female gender affect Helicobacter pylori eradication failure in chronic gastritis. Korean J Intern Med 2019;34:1022-9.

28. Almeida N, Romãozinho JM, Donato MM, Luxo C, Cardoso O, Cipriano MA, et al. Helicobacter pylori antimicrobial resistance rates in the central region of Portugal. Clin Microbiol Infect 2014;20:1127-33.

29. Seo JH, Koo SI, Youn HS, Jun JS, Lim JY, Park CH, et al. Comparison of the antibiotic resistance of Helicobacter pylori isolated in Jinju over a 15-year period. J Bacteriol Virol 2012;42:305-12.

30. De Francesco V, Zullo A, Ierardi E, Giorgio F, Perna F, Hassan C, et al. Phenotypic and genotypic Helicobacter pylori clarithromycin resistance and therapeutic outcome: benefits and limits. J Antimicrob Chemother 2010;65:327-32.

31. Lin Y, Shao Y, Yan J, Ye G. Antibiotic resistance in Helicobacter pylori: from potential biomolecular mechanisms to clinical practice. J Clin Lab Anal 2023;37:e24885.

32. Mégraud F. H pylori antibiotic resistance: prevalence, importance, and advances in testing. Gut 2004;53:1374-84.

33. De Francesco V, Giorgio F, Ierardi E, Zotti M, Neri M, Milano A, et al. Primary clarithromycin resistance in Helicobacter pylori: the Multicentric Italian Clarithromycin Resistance Observational (MICRO) study. J Gastrointestin Liver Dis 2011;20:235-9.

34. De Francesco V, Margiotta M, Zullo A, Hassan C, D Valle N, Burattini O, et al. Primary clarithromycin resistance in Italy assessed on Helicobacter pylori DNA sequences by TaqMan real-time polymerase chain reaction. Aliment Pharmacol Ther 2006;23:429-35.

35. Aguilar-Luis MA, Palacios-Cuervo F, Espinal-Reyes F, Calderón-Rivera A, Levy-Blitchtein S, Palomares-Reyes C, et al. Highly clarithromycin-resistant Helicobacter pylori infection in asymptomatic children from a rural community of Cajamarca-Peru. BMC Res Notes 2018;11:809.

36. Mohammadi M, Doroud D, Mohajerani N, Massarrat S. Helicobacter pylori antibiotic resistance in Iran. World J Gastroenterol 2005;11:6009-13.