Antibiotic Resistance of Helicobacter pylori: Data from Central Asia
Aizhan Seisenbekova 1 * ,
Alyona Lavrinenko 2,
Yelena Laryushina 1,
Ayatbek Otemis 3,
Olga Volnovaya 1,
Maxim Solomadin 4,
Yekaterina Yukhnevich 5,
Antonella Chesca 6 More Detail
1 Department of Internal Diseases, Karaganda Medical University, Karaganda, Kazakhstan
2 Laboratory, Karaganda Medical University, Karaganda, Kazakhstan
3 Endoscopy department, Karaganda Regional Hospital, Karaganda, Kazakhstan
4 International Center for Vaccinology, Kazakh National Agrarian Research University (KazNARU), Almaty, Kazakhstan
5 Pharmacy department, Karaganda Regional Hospital, Karaganda, Kazakhstan
6 Faculty of Medicine, Transylvania University of Brasov, Brasov, Romania
* Corresponding Author
J CLIN MED KAZ, Volume 22, Issue 4, pp. 62-68.
https://doi.org/10.23950/jcmk/16611
OPEN ACCESS
663 Views
83 Downloads
Author Contributions: Conceptualization, S. A. and Y. Y.; collected the data, S. A., A. O., V. O.; wrote the original draft, S. A.; reviewed and edited the manuscript, Y. Y. and L. Y.; supervised, directed and managed the study, L. A. and Y. Y. All the authors have read and agreed to with the published version of the manuscript.
Data availability statement: The corresponding author can provide the data supporting the study's conclusions upon request. Due to ethical and privacy constraints, the data are not publicly accessible.
ABSTRACT
Helicobacter pylori, also known as H. pylori, is a global health concern, especially in countries with high rates of stomach cancer. Eliminating this bacterium effectively is crucial for preventing and treating related gastrointestinal conditions. Unfortunately, antibiotic resistance makes it difficult to successfully treat H. pylori infections. This review will focus on antibiotic resistance in H. pylori populations in Central Asia, as information about this issue in this region is limited.
CITATION
Seisenbekova A, Lavrinenko A, Laryushina Y, Otemis A, Volnovaya O, Solomadin M, et al. Antibiotic Resistance of Helicobacter pylori: Data from Central Asia. J CLIN MED KAZ. 2025;22(4):62-8.
https://doi.org/10.23950/jcmk/16611
REFERENCES
- Hooi JK, Lai WY, Ng WK, Suen MM. Global Prevalence of Helicobacter pylori Infection: Systematic Review and Meta-Analysis. Gastroenterology. 2017; 153: 420–429. https://DOI:10.1053/j.gastro.2017.04.022
- Sergeeva AV, Shkarin VV, Kovalishena OV. The role of Helicobacter pylori in complex human comorbidity. Russian Journal of Infection and Immunity Infektsiya i immunitet. 2022; 12: 21–32. https://doi:10.15789/2220-7619-TRO-1667
- Robinson K, Atherton JC. The Spectrum of Helicobacter-Mediated Diseases. Annu Rev Pathol. 2021; 16: 123–144. https://DOI:10.1146/annurev-pathol-032520-024949
- Malfertheiner P, Megraud F, Rokkas T, Gisbert JP, Liou JM, Schulz C, Gasbarrini A, Hunt RH, Leja M, O'Morain C, Rugge M, Suerbaum S, Tilg H, Sugano K, El-Omar EM; European Helicobacter and Microbiota Study group. Management of Helicobacter pylori infection: the Maastricht VI/Florence consensus report. Gut. 2022: gutjnl-2022-327745. https://doi:10.1136/gutjnl-2022-327745.
- Rugge M, Genta RM, Di Mario F. Gastric cancer as preventable disease. Clin Gastroenterol Hepatol. 2017; 15: 1833–1843. https://doi:10.1016/j.cgh.2017.05.023
- Warren JR, Marshall B. Unidentified curved bacilli on gastric epithelium in active chronic gastritis. Lancet. 1983; 1: 1273–1275. https://PMID:6134060
- Wu JY, Lee YC, Graham DY. The eradication of Helicobacter pylori to prevent gastric cancer: a critical appraisal. Expert Rev Gastroenterol Hepatol. 2019; 13(1): 17-24. https://doi:10.1080/17474124.2019.1542299.
- Tshibangu-Kabamba E, Yamaoka Y. Helicobacter pylori infection and antibiotic resistance — from biology to clinical implications. Nat. Rev. Gastroenterol. Hepatol. 2021; 18: 613–629. https://DOI:10.1038/s41575-021-00449-x
- Malfertheiner P, Megraud F, O'Morain CA. Management of Helicobacter pylori infection the Maastricht V/Florence Consensus Report. Gut. 2017; 66: 6–30. https://DOI:10.1136/gutjnl-2022-327745
- Vilaichone RK, Quach DT, Yamaoka Y, Sugano K, Mahachai V. Prevalence and Pattern of Antibiotic Resistant Strains of Helicobacter Pylori Infection in ASEAN. Asian Pac J Cancer Prev. 2018; 19(5): 1411–1413. https://DOI:10.22034/APJCP.2018.19.5.1411
- Miftahussurur M, Yamaoka Y. Appropriate first-line regimens to combat Helicobacter pylori antibiotic resistance: an Asian perspective. Molecules. 2015; 20(4): 6068–6092. https://doi:10.3390/molecules20046068
- Goktas S, Gezginci E. Identifying potential risk factors associated with gastrointestinal tract cancers: A case-control study in Turkey. J Clin Med Kaz. 2023. 20(5): 17–21. https://doi.org/10.23950/jcmk/13691
- Dong E, Duan L, Wu BU. Racial and Ethnic Minorities at Increased Risk for Gastric Cancer in a Regional US Population Study. Clin Gastroenterol Hepatol. 2017; 15(4): 511–517. https://doi:10.1016/j.cgh.2016.11.033.
- Han Z, Liu J, Zhang W, Kong Q, Wan M, Lin M, Lin B, Ding Y, Duan M, Li Y, Zuo X, Li Y. Cardia and non-cardia gastric cancer risk associated with Helicobacter pylori in East Asia and the West: A systematic review, meta-analysis, and estimation of population attributable fraction. Helicobacter. 2023; 28(2): e12950. https://doi:10.1111/hel.12950.
- Wang KJ, Wang RT. Meta-analysis on the epidemiology of Helicobacter pylori infection in China. Zhonghua Liu Xing Bing Xue Za Zhi. 2003; 24: 443–446. https://PMID:12848905
- Fujisawa T, Kumagai T, Akamatsu T, Kiyosawa K, Matsunaga Y. Changes in seroepidemiological pattern of Helicobacter pylori and hepatitis A virus over the last 20 years in Japan. Am. J. Gastroenterol. 1999; 94: 2094–2099. https://doi:10.1111/j.1572-0241.1999.01283.x
- Yim JY, Kim N, Choi SH, Kim YS, Cho KR, Kim SS, Seo GS, Kim HU, Baik GH, Sin CS. Seroprevalence of Helicobacter pylori in South Korea. Helicobacter. 2007; 12: 333–340. https://doi:10.1111/j.1523-5378.2007.00504.x
- Hoang TT, Bengtsson C, Phung DC, Sörberg M, Granström M. Seroprevalence of Helicobacter pylori infection in urban and rural Vietnam. Clin. Diagn. Lab. Immunol. 2005; 2: 81–85. https://doi:10.1128/CDLI.12.1.81-85.2005
- Nurgalieva ZZ, Malaty HM, Graham DY, Almuchambetova R, Machmudova A, Kapsultanova D, Osato MS, Hollinger FB, Zhangabylov A. Helicobacter pylori infection in Kazakhstan: Effect of water source and household hygiene. Am. J. Trop. Med. Hyg. 2002; 67: 201–206. https://doi:10.4269/ajtmh.2002.67.201
- Kobayashi I, Murakami K, Kato M, Kato S, Azuma T, Takahashi S, Uemura N, Katsuyama T, Fukuda Y, Haruma K. Changing antimicrobial susceptibility epidemiology of Helicobacter pylori strains in Japan between 2002 and 2005. J. Clin. Microbiol. 2007; 45: 4006–4010. https://doi:10.1128/JCM.00740-07
- Lee JW, Kim N, Kim JM, Nam RH, Chang H, Kim JY, Shin CM, Park YS, Lee DH, Jung HC. Prevalence of primary and secondary antimicrobial resistance of Helicobacter pylori in Korea from 2003 through 2012. Helicobacter. 2013; 18: 206–214. https://doi:10.1111/hel.12031
- Gao W, Cheng H, Hu F, Li J, Wang L, Yang G, Xu L, Zheng X. The evolution of Helicobacter pylori antibiotics resistance over 10 years in Beijing, China. Helicobacter. 2010; 15: 460–466. https://doi:10.1111/j.1523-5378.2010.00788.x
- Khan A, Farooqui A, Manzoor H, Akhtar SS, Quraishy MS, Kazmi SU. Antibiotic resistance and cagA gene correlation: A looming crisis of Helicobacter pylori. World J. Gastroenterol. 2012; 18: 2245–2252. https://doi:10.3748/wjg.v18.i18.2245
- Pandya HB, Agravat HH, Patel JS, Sodagar N. Emerging antimicrobial resistance pattern of Helicobacter pylori in central Gujarat. Indian J. Med. Microbiol. 2014; 32: 408–413. https://doi:10.4103/0255-0857.142256
- Fakheri H, Bari Z, Aarabi M, Malekzadeh R. Helicobacter pylori eradication in West Asia: A review. World J. Gastroenterol. 2014; 20: 10355–10367. https://doi:10.3748/wjg.v20.i30.10355
- Ozbey G, Bahcecioglu IH, Acik MN. Resistance rates to various antimicrobial agents of Helicobacter pylori isolates in Eastern Turkey. Int. J. Mol. Clin. Microbiol. 2012. 2: 148–152.
- Bindayna KM. Antibiotic susceptibilities of Helicobacter pylori. Saudi Med. J. 2001; 22: 53–57. https://PMID:11255612
- Munita JM, Arias CA. Mechanisms of Antibiotic Resistance. Microbiol. Spectr. 2016; 4: 464–473. https://doi:10.1128/microbiolspec.vmbf-0016-2015
- Argueta EA, Ho JJ, Elfanagely Y. Clinical Implication of Drug Resistance for H. pylori Management. Antibiotics. 2022; 11: 1684. https://DOI:10.3390/antibiotics11121684
- Kim SY, Park JM, Lim CH. Types of 23S Ribosomal RNA Point Mutations and Therapeutic Outcomes for Helicobacter pylori. Gut Live. 2021; 15: 528–536. https://doi.org/10.5009/gnl20225
- Dascălu RI, Bolocan A, Păduaru DN. Multidrug resistance in Helicobacter pylori infection. Front. Microbiol. 2023, 14: 1128497. https://doi.org/10.3389/fmicb.2023.1128497
- Boyanova L, Hadzhiyski P, Kandilarov N, Markovska R, Mitov I. Multidrug resistance in Helicobacter pylori: current state and future directions. Expert Rev. Clin. Pharmacol. 2019; 12: 909–915. https://doi.org/10.1080/17512433.2019.1654858
- Malaty HM, Graham DY, Klein DG. Transmission of Helicobacter pylori Infection Studies in Families of Healthy Individuals. Scand. J. Gastroenterol. 1991; 26: 927–932. https://DOI:10.3109/00365529108996244
- Keikha M, Askari P, Ghazvini K, Karbalaei M. Levofloxacin-based therapy as an efficient alternative for eradicating Helicobacter pylori infection in Iran: a systematic review and meta-analysis. J. Glob. Antimicrob. Resist. 2021; 29: 420–429. https://doi.org/10.1016/j.jgar.2021.10.019
- Okamoto T, Yoshiyama H, Nakazawa T. A change in PBP1 is involved in amoxicillin resistance of clinical isolates of Helicobacter pylori. J. Antimicrob. Chemother. 2002, 50: 849–856. https://doi.org/10.1093/jac/dkf140
- Qureshi NN, Gallaher B, Schiller NL. Evolution of Amoxicillin Resistance of Helicobacter pylori In Vitro: Characterization of Resistance Mechanisms. Microb. Drug Resist. 2014; 20: 509–516. https://doi.org/10.1089/mdr.2014.0019
- Gerrits MM, Berning M, Van Vliet. Effects of 16S rRNA gene mutations on tetracycline resistance in Helicobacter pylori. Antimicrob Agents Chemother. 2003; 47: 29842986. https://doi:10.1128/AAC.47.9.2984-2986.2003
- Anoushiravani M, Falsafi T, Niknam V. Proton motive force-dependent efflux of tetracycline in clinical isolates of Helicobacter pylori. J Med Microbiol. 2009; 58: 1309–1313. https://DOI:10.1099/jmm.0.010876-0
- Fock KM, Ang TL. Epidemiology of Helicobacter pylori infection and gastric cancer in Asia. J. Gastroenterol. Hepatol. 2010; 25: 479–486. https://doi:10.1111/j.1440-1746.2009.06188.x
- Lin Y, Shao Y, Yan J. Antibiotic resistance in Helicobacter pylori: From potential biomolecular mechanisms to clinical practice. J. Clin. Lab. Anal. 2023; 37: e24885, https://doi.org/10.1002/jcla.24885.
- Balapasheva AA, Mussina AZ, Smagulova GA, Ziganshina LE. Comprehensive Pharmacoepidemiological and Clinical-Economic Analysis of Antibacterial Drugs Consumed during the Pandemic at the Hospital Level in Aktobe, Kazakhstan. J Clin Med Kaz. 2024; 21: 55–58. https://doi.org/10.23950/jcmk/14495
- Igissinov N, Taszhanov R, Telmanova Z, Baibusunova A, Rustemova K, Bilyalova Z, Igissinova G, Kudaibergenova I, Kozhakhmetov S, Orazbayev S, Azhetova Z, Nurtazinova G, Sayakov U, Dzhumabayeva F, Kulayev K, Idrissov K, Kuandykov T, Mutagirov V, Shapambayev N. Trend in Gastric Cancer Mortality in Kazakhstan. Asian Pac J Cancer Prev. 2022; 23: 3779–3789. https://doi:10.31557/APJCP.2022.23.11.3779
- Han Z, Liu J, Zhang W, Kong Q, Wan M, Lin M, Lin B, Ding Y, Duan M, Li Y, Zuo X, Li Y. Cardia and non-cardia gastric cancer risk associated with Helicobacter pylori in East Asia and the West: A systematic review, meta-analysis, and estimation of population attributable fraction. Helicobacter. 2023; 28(2): e12950. https://doi:10.1111/hel.12950
- Lavrinenko A, Seisenbekova A, Turemuratova A, Shkreba A, Yukhnevich Y. Review of Methods for Detection Helicobacter pylori in Kazakhstan. JGH Open. 2025; 9(1): e70101. https://doi:10.1002/jgh3.70101.
- Zhangabylov А, Nurgalieva Z, and Almukhanbetova R. Results of Serological Studies to Detect Helicobacter pylori Infection in Residents of Alma‐Ata. International Gastroenterological Congress. 2002; 9: 66.
- Kulmagambetova G, Bekenova E, Tuyakova А, Logvinenko А, Sukshev А, Almagambetov К. The Antibiotic Resistance of Helicobacter pylori in the Population of Kazakhstan. Infection and Immune System. 2014; 4: 76.
- Mežmale L, Polaka I, Rudzite D. Prevalence and Potential Risk Factors of Helicobacter pylori Infection among Asymptomatic Individuals in Kazakhstan. Asian Pac. J. Cancer Prev. 2021; 22: 597–602. https://doi.org/10.31557/apjcp.2021.22.2.597
- Li Y, Choi H, Leung K, Jiang F, Graham DY, Leung WK. Global prevalence of Helicobacter pylori infection between 1980 and 2022: a systematic review and meta-analysis. Lancet Gastroenterol Hepatol. 2023; 8: 553–564. https://doi:10.1016/S2468-1253(23)00070-5
- Hasanuzzaman M, Bang CS, Gong EJ. Antibiotic Resistance of Helicobacter pylori: Mechanisms and Clinical Implications. J Korean Med Sci. 2024; 39(4): e44. https://doi.org/10.3346/jkms.2024.39.e44
- Giorgio F, Principi M, De Francesco V, Zullo A, Losurdo G, Di Leo A, Ierardi E. Primary clarithromycin resistance to Helicobacter pylori: Is this the main reason for triple therapy failure? World J Gastrointest Pathophysiol. 2013; 4(3): 43–46. https://doi:10.4291/wjgp.v4.i3.43.
- Kim SY, Choi DJ, Chung JW. Antibiotic treatment for Helicobacter pylori: Is the end coming? World J Gastrointest Pharmacol Ther. 2015; 6(4): 183–198. https://doi:10.4292/wjgpt.v6.i4.183.
- Moldobaeva MS, Elistratova AA, Tolombaeva NT, Sharshenalieva GK. Мodern approaches to the cancer prevention in hp-associated gastritis. Bulletin of KRSU. 2014; 5: 102–106. https://DOI:10.1111/j.1365-2036.2007.03475.x
- Dzhumabaev MN, Dzhumanova RG, Sabirov IS. The interdependence between smoking, alcohol, tooth pathology and prevalence of helicobacter pylori among ethnic groups in Kyrgyzstan. Eksp Klin Gastroenterol. 2015; 6: 16–20.
- https://www.worldlifeexpectancy.com/kyrgyzstan-stomach-cancer
- Abdiev S, Ahn KS, Khadjibaev A. Helicobacter pylori infection and cytokine gene polymorphisms in Uzbeks. Nagoya J Med Sci. 2010; 72: 167–172. https://PMID:20942272.
- Ismailova J, Yusupbekov A. Modern aspects to the problem of the prevalence of Helicobacter pylori associated stomach diseases in Uzbekistan. Journal of healthcare in developing countries. 2021; 1: 28–30. https://10.26480/jhcdc.02.2021.28.30.
- Karimov M, Sobirova G, Saatov Z. Prevalence and Molecular-Genetic Characteristics of Helicobacter pylory in Uzbekistan. Eff. Pharmacother. 2019; 15 (28): 48–51. https://doi.org/10.33978/2307-3586-2019-15-28-48-51.
- Tajikistan: Stomach Cancer. https://www.worldlifeexpectancy.com/tajikistan-stomach-cancer
- Turkmenistan: Stomach Cancer. https://www.worldlifeexpectancy.com/turkmenistan-stomach-cancer
- Aldiyarova MA. Prevalence and Features of Infection Caused by Helicobacter pylori in the Indigenous Population of the Southern Region of Kazakhstan. Epidemiology and Infectious Diseases. 2011; 1: 25–27.
- Zaidi SF. Helicobacter pylori associated Asian enigma: Does diet deserve distinction? World J Gastrointest Oncol. 2016; 8(4): 341–350. https://doi:10.4251/wjgo.v8.i4.341
- Nurgalieva ZZ, Malaty HM, Graham DY. Helicobacter pylori Infection in Kazakhstan: Effect of Water Source and Household Hygiene. American Journal of Tropical Medicine and Hygiene. 2002; 67: 201–206.
- Abylkasymova К. Comparative Analysis of the Sensitivity of Laboratory Diagnostic Methods (ELISA and PCR) for Helicobacter pylori Infection. Bulletin of KazNMU. 2012; 2: 271.