Xie J, Zhang ML, Guo M, Li JG, Liu Y, Chen HH, Wang F. Antibiotic resistance of Helicobacter pylori and related risk factors in Hunan Province: A multicenter study. World J Gastroenterol 2025; 31(12): 104835 [DOI: 10.3748/wjg.v31.i12.104835]
Corresponding Author of This Article
Fen Wang, MD, Professor, Department of Gastroenterology, The Third Xiangya Hospital, Central South University, No. 138 Tongzi Road, Changsha 410013, Hunan Province, China. wfen-judy@csu.edu.cn
Research Domain of This Article
Gastroenterology & Hepatology
Article-Type of This Article
Retrospective Study
Open-Access Policy of This Article
This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Jie Xie, Ming-Lin Zhang, Fen Wang, Department of Gastroenterology, The Third Xiangya Hospital, Central South University, Changsha 410013, Hunan Province, China
Jie Xie, Ming-Lin Zhang, Fen Wang, Hunan Key Laboratory of Non-resolving Inflammation and Cancer, The Third Xiangya Hospital, Central South University, Changsha 410006, Hunan Province, China
Min Guo, Department of Gastroenterology, The First People’s Hospital of Changde, Changde 415003, Hunan Province, China
Jian-Guo Li, Department of Gastroenterology, The Fourth Hospital of Changsha, Changsha 410000, Hunan Province, China
Yuan Liu, Department of Gastroenterology, Yueyang Hospital of Traditional Chinese Medicine, Yueyang 414100, Hunan Province, China
Hong-Hui Chen, Department of Gastroenterology, The Second Affiliated Hospital of South China University, Hengyang 421099, Hunan Province, China
Author contributions: Xie J, Zhang ML, Wang F, Guo M, Li JG, Liu Y, and Chen HH contributed to the methodology and resources; Xie J and Zhang ML made validation and formal analysis, wrote the original draft, and cured the data; Zhang ML and Wang F supervised the research; Wang F reviewed and edited the article; Xie J and Wang F acquired the funding; Guo M, Li JG, Liu Y, Chen HH, and Wang F conceptualized and administrated the project; Wang F is the corresponding author of the article; all authors have read and agreed to the published version of the manuscript.
Supported by the National Natural Science Foundation of China, No. 82270594; and the Independent Exploration and Innovation Project of Central South University, No. 2024ZZTS0966.
Institutional review board statement: This study was conducted in accordance with the principles of the Declaration of Helsinki, and was approved by the Ethics Committee of the Third Xiangya Hospital of Central South University (No. 23259).
Informed consent statement: The requirement to obtain informed written consent was waived, because the study was retrospective and did not involve any privacy and commercial interests.
Conflict-of-interest statement: The authors declare that they have no conflict of interest to disclose.
Data sharing statement: The data supporting the findings of this study are available from the corresponding author upon reasonable request.
Open Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Fen Wang, MD, Professor, Department of Gastroenterology, The Third Xiangya Hospital, Central South University, No. 138 Tongzi Road, Changsha 410013, Hunan Province, China. wfen-judy@csu.edu.cn
Received: January 3, 2025 Revised: February 23, 2025 Accepted: March 6, 2025 Published online: March 28, 2025 Processing time: 82 Days and 16.5 Hours
Abstract
BACKGROUND
Antibiotic resistance is a key factor influencing the treatment outcomes of Helicobacter pylori (H. pylori) infection. The antibiotic resistance spectrum of H. pylori varies in different regions. We investigated the current status of antibiotic resistance of H. pylori in Hunan Province and analyzed the factors related to such resistance to provide strategies for the accurate clinical treatment of H. pylori infection.
AIM
To understand the antibiotic resistance of H. pylori in Hunan Province and provide guidance for the clinical treatment of H. pylori infection.
METHODS
This study selected patients who underwent gastroscopy in five hospitals in Hunan Province from April 2022 to April 2023. The sensitivity of H. pylori to clarithromycin, levofloxacin, metronidazole, amoxicillin, furazolidone, and tetracycline was detected using the Agar dilution method.
RESULTS
H. pylori strains from a total of 566 patients were isolated and identified. The resistance rates of H. pylori strains to clarithromycin, levofloxacin, metronidazole, amoxicillin, furazolidone, and tetracycline were 49.2%, 37.8%, 76.1%, 2.3%, 1.4%, and 0.7%, respectively. The resistance rates to clarithromycin, levofloxacin, and metronidazole were high in the four regions of Hunan Province, and the overall resistance rates in central Hunan Province were higher than those in other regions. The resistance rates of H. pylori strains to clarithromycin and levofloxacin were significantly different among the different age groups (P < 0.05), with the elderly group having a higher resistance rate than the young group. The resistance rate of H. pylori strains to clarithromycin was greater in patients with atrophic gastritis, and the resistance rate to levofloxacin was the lowest in patients with peptic ulcers.
CONCLUSION
The resistance rate of H. pylori to amoxicillin, clarithromycin, and metronidazole is high in Hunan Province. Age, stomach disease, and H. pylori reinfection may affect the antibiotic resistance of H. pylori.
Core Tip: Antibiotic resistance is one of the main factors that determine the treatment effect of Helicobacter pylori (H. pylori) infection. The antibiotic resistance spectrum of H. pylori varies in different regions. We investigated the current status of antibiotic resistance of H. pylori in Hunan Province, and analyzed the related factors of such resistance, so as to provide strategies for accurate clinical treatment of H. pylori infection. The resistance rate of H. pylori to amoxicillin, clarithromycin, and metronidazole is high in Hunan Province, and age, stomach disease, and H. pylori reinfection may affect the antibiotic resistance of H. pylori.
Citation: Xie J, Zhang ML, Guo M, Li JG, Liu Y, Chen HH, Wang F. Antibiotic resistance of Helicobacter pylori and related risk factors in Hunan Province: A multicenter study. World J Gastroenterol 2025; 31(12): 104835
Helicobacter pylori (H. pylori) is listed as a class I carcinogen by the International Agency for Research on Cancer[1] and plays an important role in the occurrence and development of gastric diseases such as peptic ulcers, chronic gastritis, and gastric cancer (GC)[2-4]. The increase in antibiotic resistance in H. pylori is a serious problem that significantly affects the treatment of H. pylori infection[5].
More than half of the global population is infected with H. pylori, but the prevalence of H. pylori infection varies greatly in different countries and regions[6]. Studies have shown that the prevalence of H. pylori infection in China is 28%-82%, and the overall prevalence is approximately 44.2%[7]. In addition, the antibiotic resistance patterns were geographically different and may have changed over time[8,9]. A large-scale multicenter study in China revealed that H. pylori was highly resistant to clarithromycin (CLR), levofloxacin (LVX), and metronidazole (MTZ) from 2018 to 2020, and the overall resistance rate was 47.24%, 41.40%, and 89.44%, respectively[10]. Therefore, understanding antibiotic resistance patterns in specific regions serves the basis for the development of H. pylori treatment regimens. At present, the antibiotic resistance rate of H. pylori in different parts of Hunan Province is unclear. Therefore, this study investigated the resistance of H. pylori to six commonly used antibiotics in Hunan Province and explored the relationships of H. pylori infection with age, sex, treatment history and stomach disease. We aimed to provide a reference for the precise treatment of H. pylori infection.
MATERIALS AND METHODS
Study subjects
This study investigated the susceptibility of H. pylori to six commonly used antibiotics in Hunan Province from April 2022 to April 2023 (the location distribution in Hunan Province is shown in Figure 1). The subjects were recruited from five hospitals in Hunan Province, and their baseline data (gender, age, origin, endoscopic findings, and whether they had received H. pylori eradication therapy or not) were collected. All participants underwent gastroscopy by experienced endoscopists who perform more than 1000 endoscopies per year. The endoscopist collected gastric mucosa tissue samples via biopsy of the gastric antrum and gastric body for H. pylori culture and antibiotic susceptibility testing. The detailed inclusion criteria were as follows: (1) Patients aged 18-80 years; (2) Patients who underwent gastroscopy and were diagnosed with H. pylori infection using immunohistochemical staining of the biopsy specimen; and (3) Patients for whom no antibiotics were used 4 weeks before gastroscopy and no proton pump inhibitors or H2 receptor antagonists were used 2 weeks before gastroscopy. The exclusion criteria were as follows: (1) Patients complicated with severe heart, lung, liver, or renal insufficiency; (2) Patients with severe coagulation dysfunction; (3) Patients who were pregnant or lactating; and (4) Patients with mental illness or communication disorders. This study was conducted in accordance with the principles of the Declaration of Helsinki and was approved by the Ethics Committee of the Third Xiangya Hospital of Central South University (No. 23259). The requirement for obtaining informed written consent was waived because the study was retrospective and did not involve any privacy and commercial interests. Measures were taken to anonymize biological samples, and a strict data security management system and a technical protection system for the storage, use, and sharing of biological samples and data were formulated to ensure data and personal information security.
Tissue samples of gastric mucosa biopsy from the gastric antrum and gastric body were collected during gastroscopy and stored at -80 °C. H. pylori was transported under dry ice cryopreservation conditions for further isolation, culture, identification, and antibiotic resistance determination (Hangzhou Zhiyuan Medical Inspection Institute Co., Ltd). The gastric mucosa samples were ground and inoculated on plates containing 5% defibrated sheep blood. The inoculated plates were placed in a three-gas incubator (5% oxygen, 10% carbon dioxide, and 85% nitrogen) at 37 °C, and the growth of the colonies was observed after 96 hours. If the morphology of the bacteria was consistent with that of H. pylori in the microscopic examination of the suspected colony smear and if the strain was positive in the biochemical reaction (urease, oxidase, and catalase) tests, it was determined to be H. pylori positive. If no suspected colonies were found, and the culture time was extended to the seventh day.
Antibiotic susceptibility test
The antibiotic resistance of H. pylori strains was detected using the agar dilution method. The critical points of resistance to the selected antibiotics were MTZ (8 μg/mL), CLR (1 μg/mL), amoxicillin (0.125 μg/mL), LVX (2 μg/mL), furazolidone (2 μg/mL), and tetracycline (2 μg/mL). Susceptibility test results were interpreted according to the guidelines and criteria of the European Committee of Antibiotic Susceptibility Testing (EUCAST) and Clinical and Laboratory Standards Institute (CLSI). The EUCAST recommendations are described in detail and updated regularly on the EUCAST website (http://www.eucast.org), and the CLSI recommendations are described in detail and updated regularly on the CLSI website (https://clsi.org/). Two microliters of positive bacterial suspension was absorbed and inoculated on an antibiotic plate containing 5% defibrillated sheep blood. After drying, the suspensions were placed in a three-gas incubator (5% oxygen, 10% carbon dioxide, 85% nitrogen) at 37 °C. The results were observed after culture in a microaerobic environment for 3 days, and the antibiotic sensitivity results were interpreted according to colony growth at the inoculation point. For the antibiotic susceptibility test, the ATCC43504 (NCTC11637) standard strain was selected as the control, and NCTC1637 was selected as the quality control strain with a critical antibiotic resistance value.
Statistical analysis
Data were analyzed using SPSS (version 27.0). Categorical variables are expressed as frequencies and proportions, and differences between groups were analyzed using the χ2 test or Fisher’s exact test. Two-sided P values < 0.05 were considered statistically significant.
RESULTS
Characteristics of study subjects
The gastric mucosa of 1247 patients who underwent gastroscopy at five hospitals in Hunan Province was obtained for H. pylori isolation and culture, and H. pylori strains were detected in a total of 566 patients, all of whom were eligible for inclusion in this study. The baseline information of the subjects is shown in Table 1. There were 276 males (48.8%) and 290 females (51.2%). The age range was 18 to 78 years, and the mean age was 50.0 ± 11.7 years. Among the included patients, 132 (23.3%) had previously received H. pylori treatment, 194 (34.3%) had peptic ulcers, 65 (11.5%) had chronic atrophic gastritis, and 283 (50.0%) had chronic nonatrophic gastritis. The source distribution of strains was as follows: Northern Hunan (61.8%), central Hunan (13.3%), southern Hunan (22.4%), and western Hunan (2.5%) (Table 1).
Of the 566 H. pylori strains, only 95 (16.8%) were sensitive to all the six antibiotics. The H. pylori strains presented the highest resistance to MTZ (76.1%), followed by CLR (49.2%), LVX (37.8%), amoxicillin (2.3%), furazolidone (1.4%), and tetracycline (0.7%). Among the 434 patients with H. pylori infection treated for the first time, 349 (80.4%) were resistant to at least one of the tested antibiotics. Among the 132 patients who had previously been treated for H. pylori infection, 122 (92.4%) were resistant to at least one antibiotic. The resistance rates to the six antibiotics in the retreated patients were higher than those in the initially treated patients (Figure 2). A total of 12 patterns of resistance to H. pylori were identified. A total of 55.8% (316/566) of the isolates were resistant to two or more antibiotics, of which 30.6% were resistant to two antibiotics, 22.4% to three antibiotics, 2.1% to four antibiotics, 0.4% to five antibiotics, and 0.4% to six antibiotics. In the dual-resistance patterns, the resistance rate of the CLR + MTZ group was 18.0%, followed by that of the MTZ + LVX group (9.2%). The main triple resistance pattern was CLR + MTZ + LVX (21.7%, 123/566). Multiple patterns of resistance to four or more antibiotics were relatively rare, occurring in approximately 1% of the strains. The resistance rate to CLR + MTZ + LVX in retreated patients was significantly greater than that in initially treated patients. The rate of resistance to CLR + MTZ was almost the same between initially treated patients and retreated patients (Table 2).
Figure 2 Resistance rates of Helicobacter pylori to the six antibiotics.
Treatment-naive patients: Patients treated for Helicobacter pylori infection for the first time. Patients with therapy history: Patients who had previously been treated for Helicobacter pylori infection.
Table 2 Multiple antibiotics resistance patterns of Helicobacter pylori, n (%).
Susceptibility test results
Overall (n = 566)
Treatment-naive (n = 434)
Patients with therapy history (n = 132)
CLR + LVX
19 (3.4)
10 (2.3)
9 (6.8)
CLR + MTZ
102 (18.0)
78 (18.0)
24 (18.2)
MTZ + LVX
52 (9.2)
50 (11.5)
2 (1.5)
CLR + AMX + MTZ
3 (0.5)
3 (0.7)
0 (0.0)
CLR + FZD + MTZ
1 (0.2)
1 (0.2)
0 (0.0)
CLR + MTZ + LVX
123 (21.7)
71 (16.4)
52 (39.4)
CLR + AMX + MTZ + LVX
6 (1.1)
2 (0.5)
4 (3.0)
CLR + FZD + MTZ + LVX
3 (0.5)
0 (0.0)
3 (2.3)
CLR + MTZ + LVX + TET
2 (0.4)
1 (0.2)
1 (0.8)
FZD + MTZ + LVX + TET
1 (0.2)
1 (0.2)
0 (0.0)
CLR + AMX + FZD + MTZ + LVX
2 (0.4)
2 (0.5)
0 (0.0)
CRL + AMX + FZD + MTZ + LVX + TET
2 (0.4)
1 (0.2)
1 (0.8)
Antibiotic resistance rates of H. pylori in different regions
The strains in the four regions generally presented high antibiotic resistance to CLR, LVX, and MTZ. The resistance to these three antibiotics in central Hunan was overall high, with resistance rates of 52.0%, 48.0%, and 94.6%, respectively. No significant differences in the CLR resistance rates were noted among northern, central, and western Hunan, but the resistance rate in southern Hunan was lower. The rate of LVX resistance in central Hunan was higher than that in other areas (P < 0.05). The resistance rate to MTZ was high in all four regions, and the antibiotic resistance rates in western Hunan and central Hunan were close to 100%. The overall resistance rates to amoxicillin, furazolidone, and tetracycline were low, among which tetracycline-resistant strains were detected only in northern Hunan. No amoxicillin-resistant strains were detected in central Hunan and western Hunan, and no furazolidone-resistant strains were detected in western Hunan (Figure 3).
Figure 3 Susceptibility of Helicobacter pylori to six antibiotics in different regions of Hunan Province.
Analysis of factors associated with antibiotic resistance in H. pylori
We analyzed the associations of antibiotic resistance of H. pylori with increasing age, sex, treatment history, and incidence of gastric diseases. The resistance rates of H. pylori strains to CLR and LVX were greater in older patients (P < 0.05). The rates of resistance to CLR, LVX, and MTZ in retreated patients were higher than those in initially treated patients (P < 0.05). The resistance rate of H. pylori strains to CLR in patients with chronic atrophic gastritis was greater than that in patients with peptic ulcers and chronic nonatrophic gastritis. The resistance rate to LVX in patients with peptic ulcers was lower than that in patients with chronic atrophic gastritis and chronic nonatrophic gastritis. The sex of patients was not correlated with resistance to H. pylori to different antibiotics (P > 0.05) (Table 3).
Table 3 Analysis of factors associated with antibiotic resistance of Helicobacter pylori, n (%).
Factor
Clarithromycin
Levofloxacin
Metronidazole
Amoxicillin
Furazolidone
Tetracycline
Age, years
18-40 (n = 115)
45 (39.1)
34 (29.6)
85 (73.9)
1 (0.9)
1 (0.9)
0 (0.0)
41-59 (n = 347)
172 (49.6)
131 (37.8)
270 (77.8)
8 (2.3)
6 (1.7)
4 (1.2)
60-80 (n = 104)
62 (59.6)
49 (47.1)
76 (73.1)
4 (3.8)
1 (1.0)
0 (0.0)
P value
0.010
< 0.001
0.500
0.339
1.000
0.473
Sex
Male (n = 276)
131 (47.5)
103 (37.3)
202 (73.2)
6 (2.2)
2 (0.7)
2 (0.7)
Female (n = 290)
148 (51.0)
111 (38.3)
229 (79.0)
7 (2.4)
6 (2.1)
2 (0.7)
P value
0.396
0.814
0.107
0.849
0.287
1.000
Treatment history
No (n = 434)
182 (41.9)
141 (32.5)
322 (74.2)
8 (1.8)
4 (0.9)
2 (0.5)
Yes (n = 132)
97 (73.5)
73 (55.3)
109 (82.6)
5 (3.8)
4 (3.0)
2 (1.5)
P value
< 0.001
< 0.001
0.048
0.194
0.090
0.233
Gastric disease
Ulcer (n = 194)
82 (42.3)
64 (33.0)
147 (75.8)
5 (2.6)
2 (1.0)
0 (0.0)
Atrophic gastritis (n = 65)
41 (63.1)
31 (47.7)
52 (80.0)
2 (1.5)
1 (1.5)
2 (3.1)
Non-atrophic gastritis (n = 283)
145 (51.2)
106 (37.5)
214 (75.6)
10 (2.1)
4 (1.4)
1 (0.4)
Others (n = 24)
12 (50.0)
14 (58.3)
19 (79.2)
1 (4.2)
1 (4.2)
1 (4.2)
P value
0.027
0.031
0.997
0.753
0.464
0.078
Regions
Northern Hunan (n = 350)
188 (53.7)
140 (40.0)
259 (74.0)
11 (3.1)
6 (1.7)
4 (1.1)
Central Hunan (n = 75)
39 (52.0)
36 (48.0)
71 (94.7)
0 (0.0)
1 (1.3)
0 (0.0)
Southern Hunan (n = 127)
45 (35.4)
34 (26.8)
87 (68.5)
2 (1.6)
1 (0.8)
0 (0.0)
Western Hunan (n = 14)
7 (50.0)
4 (28.6)
14 (100)
0 (0.0)
0 (0.0)
0 (0.0)
P value
0.005
0.011
< 0.001
0.430
0.897
0.787
DISCUSSION
H. pylori is considered a class I carcinogen, and eradicating H. pylori is recommended upon detection[11]. Studies have shown that H. pylori eradication can significantly reduce the incidence and mortality of GC and reverse intestinal metaplasia[12,13]. Increasing antibiotic resistance has become a major challenge for current H. pylori therapies[5,14,15]. Therefore, it is necessary to detect H. pylori infection and eradicate it promptly. The rate of antibiotic resistance of H. pylori varies in different countries or regions. For example, the H. pylori resistance rate in European countries in 2018 was 21.4% to CLR, 15.8% to LVX, and 38.9% to MTZ; Israel had the highest rates of resistance to CLR and MTZ (46.3% and 16.3%)[16-18]. This study investigated for the first time the resistance of H. pylori to six commonly used antibiotics in four regions of Hunan Province. The overall resistance rates of H. pylori strains to CLR, LVX, MTZ, amoxicillin, furazolidone, and tetracycline were 49.2%, 37.8%, 76.1%, 2.3%, 1.4%, and 0.7%, respectively. These rates are roughly consistent with antibiotic resistance data from a large-scale multicenter study in China, which showed that the overall antibiotic resistance rates of CLR, LVX and methonidazole were 47.24%, 41.40% and 89.44%, respectively, while the overall antibiotic resistance rates to amoxicillin, furazolidone, and tetracycline were relatively low at 3.23%, 2.05%, and 1.65%, respectively[10]. The results of this study revealed that 55.8% of the strains were resistant to at least two antibiotics. The main resistance pattern was CLR + MTZ (18.0%), followed by MTZ + LVX (9.2%), and the main triple resistance pattern was CLR + MTZ + LVX (21.7%). These findings indicate that the combination of these antibiotics should be used with caution in H. pylori eradication therapy. In this study, the antibiotic resistance rate to MTZ was the highest, with the resistance rates in both the initially treated patients and retreated patients exceeding 70%. These results indicate that treatment regimens containing MTZ should be carefully selected. In addition, the resistance rates to CLR and LVX were high, especially the resistance rate to CLR in retreated patients, which was as high as 73.5%. The consensus of foreign experts suggests that antibiotic sensitivity tests should be performed before prescribing any prescription containing CLR[19], and the consensus of Chinese experts suggests LVX as a second-line experimental antibiotic[20]. Therefore, the use of MTZ, CLR, and LVX should be considered after antibiotic sensitivity tests have been performed. Fortunately, in this study, we observed that the antibiotic resistance rates to amoxicillin, furazolidone, and tetracycline were low in both initially treated and retreated patients, and no amoxicillin-resistant strains were found in the western and central Hunan regions of Hunan Province, which was also consistent with the results reported in a single-center study in south-central China. That study showed resistance rates of 38.5%, 61.5%, 27.9%, and 13.5% to CLR, MTZ, LVX, and amoxicillin, respectively, while no strain was resistant to tetracycline or furazolidone[21]. Currently, bismuth-containing quadruple therapy is used in H. pylori eradication therapy. In addition, high-dose proton pump inhibitors-amoxicillin dual therapy has the same efficacy and compliance with fewer side effects than bismuth-containing quadruple therapy[22] and has been used in clinical treatment.
There is currently some controversy regarding the relationships among sex, age, stomach disease, and antibiotic resistance. A German study revealed that female sex and previous antibacterial treatment were risk factors for CLR resistance, and advanced age was associated with LVX resistance[23]. In contrast, in a study in Bhutan, no statistically significant relationship was noted between antibiotic resistance and age, sex, or endoscopy results[24]. In this study, we found that there were statistically significant differences in the resistance rates of H. pylori strains to CLR and LVX in patients in different age groups (P < 0.05). The resistance rate to CLR in the elderly group was greater than that in the young group, and the resistance rate to LVX increased with increasing age. A Chinese study which examined H. pylori antibiotic resistance in 13 provinces and cities in China from 2010 to 2016 reported similar findings, with younger patients (< 40 years) showing lower resistance rates to CLR and LVX[25]. This may be due to the increase in the number of times that people use antibiotics as they age, and the rate of resistance increases accordingly. In addition, we found that the strain isolated from patients with atrophic gastritis had a high resistance rate to CLR, which was consistent with a previous study[26]. This phenomenon may be related to bacterium-specific virulence factors. For example, cytotoxin-associated gene A is an important effector protein of H. pylori that has previously been shown to not only activate cell senescence and cause gastric mucosa atrophy but also promote the further formation of biofilms in H. pylori strains, thereby causing resistance to multiple antibiotics[27-30].
This was a retrospective cross-sectional study that included a subset of hospital patients, so there was some selection bias. In addition, the sample size in western Hunan is small, which may not accurately reflect the actual level of antibiotic resistance. Thus, in future studies, we will expand the sample size and increase the inclusion of community samples to provide a more comprehensive picture of resistance patterns and associated risk factors. Moreover, we only obtained complete endoscopic data of the subjects, lacking baseline information such as patient symptoms, family history, and analysis of antibiotic resistance status, which may require further study.
CONCLUSION
In conclusion, the resistance rates of H. pylori to amoxicillin, CLR, and MTZ are high in Hunan Province. Age and stomach disease are associated with the resistance rate of H. pylori to antibiotics. Antibiotic resistance in H. pylori is related to many factors, and other potential factors deserve further study. In addition, differences in antibiotic resistance are noted in different regions, and more high-quality studies with large samples and multiple centers are needed.
ACKNOWLEDGEMENTS
We would like to thank all the participants in this study. We are particularly grateful to Dr. Chen B, Dr. Li XM, Dr. Deng AJ, Ms. Shen YC, Ms. Yang XE, and Dr. Yao SY for their assistance in collecting information.
Footnotes
Provenance and peer review: Unsolicited article; Externally peer reviewed.
Peer-review model: Single blind
Specialty type: Gastroenterology and hepatology
Country of origin: China
Peer-review report’s classification
Scientific Quality: Grade B, Grade C, Grade C, Grade D
Novelty: Grade B, Grade B, Grade C, Grade C
Creativity or Innovation: Grade B, Grade B, Grade C, Grade D
Scientific Significance: Grade B, Grade C, Grade C, Grade C
P-Reviewer: Babar A; Rao RSP; Xie Y S-Editor: Fan M L-Editor: Wang TQ P-Editor: Zheng XM
Malfertheiner P, Megraud F, O'Morain CA, Gisbert JP, Kuipers EJ, Axon AT, Bazzoli F, Gasbarrini A, Atherton J, Graham DY, Hunt R, Moayyedi P, Rokkas T, Rugge M, Selgrad M, Suerbaum S, Sugano K, El-Omar EM; European Helicobacter and Microbiota Study Group and Consensus panel. Management of Helicobacter pylori infection-the Maastricht V/Florence Consensus Report.Gut. 2017;66:6-30.
[PubMed] [DOI] [Full Text][Cited in This Article: ][Cited by in Crossref: 1710][Cited by in RCA: 1934][Article Influence: 241.8][Reference Citation Analysis (1)]
Hu S, Zhou Y, Deng Y, Bo Y, Chen X, Yang W, Shi R, Zhao W, Hou Z, Hu J, Liu J, Zhang X, Yong H, Wang P, Li F, Qi H, Wang X, Jin L, Cui T, Yong H, Li X, Yang B, Yu Y, Ma B, Fu L, Wang X, Ma Z, Tang N, You Y, Guo J, Yu X, Yao L, Gao R, Li Y, Xin R, Liu J, Cao Z, Li H, Ma L, Ma S, Cao Y, Tang Y, Liu J, Hao Q, Li X, Li X, Mu R, Niu M, Su X, Gao H. Characteristics of phenotypic antibiotic resistance of Helicobacter pylori and its correlation with genotypic antibiotic resistance: A retrospective study in Ningxia.Helicobacter. 2023;28:e12960.
[PubMed] [DOI] [Full Text][Cited in This Article: ][Cited by in RCA: 2][Reference Citation Analysis (0)]
Zhang Y, Feng X, Bian L, Zhang Y, Li Q, Xu Y, She Q, Yan C, Lu G, Wu J, Xiao W, Ding Y, Deng B. Antibiotic Resistance of Helicobacter pylori and Related Risk Factors in Yangzhou, China: A Cross-Sectional Study.J Clin Med. 2023;12.
[PubMed] [DOI] [Full Text][Cited in This Article: ][Cited by in RCA: 5][Reference Citation Analysis (0)]
Zhong Z, Zhang Z, Wang J, Hu Y, Mi Y, He B, Zhang Y, Zhang X, Xia X, Huang H, Lai Y, Lin M, Su C, Zhang Z, Wu Z, Lu L, Zhang B, Huang S, Zhong C, Zeng X, Peng Y, Chen G, Zhang H, Zhou G, Liu S, Yang C, Yan L, Chen A, Zhang G, Xu P, Wang S, Zheng P, Xu S, Gao H. A retrospective study of the antibiotic-resistant phenotypes and genotypes of Helicobacter pylori strains in China.Am J Cancer Res. 2021;11:5027-5037.
[PubMed] [DOI][Cited in This Article: ]
Liou JM, Malfertheiner P, Lee YC, Sheu BS, Sugano K, Cheng HC, Yeoh KG, Hsu PI, Goh KL, Mahachai V, Gotoda T, Chang WL, Chen MJ, Chiang TH, Chen CC, Wu CY, Leow AH, Wu JY, Wu DC, Hong TC, Lu H, Yamaoka Y, Megraud F, Chan FKL, Sung JJ, Lin JT, Graham DY, Wu MS, El-Omar EM; Asian Pacific Alliance on Helicobacter and Microbiota (APAHAM). Screening and eradication of Helicobacter pylori for gastric cancer prevention: the Taipei global consensus.Gut. 2020;69:2093-2112.
[PubMed] [DOI] [Full Text][Cited in This Article: ][Cited by in Crossref: 135][Cited by in RCA: 275][Article Influence: 55.0][Reference Citation Analysis (0)]
Piazuelo MB, Bravo LE, Mera RM, Camargo MC, Bravo JC, Delgado AG, Washington MK, Rosero A, Garcia LS, Realpe JL, Cifuentes SP, Morgan DR, Peek RM Jr, Correa P, Wilson KT. The Colombian Chemoprevention Trial: 20-Year Follow-Up of a Cohort of Patients With Gastric Precancerous Lesions.Gastroenterology. 2021;160:1106-1117.e3.
[PubMed] [DOI] [Full Text][Cited in This Article: ][Cited by in Crossref: 33][Cited by in RCA: 57][Article Influence: 14.3][Reference Citation Analysis (0)]
Hong TC, El-Omar EM, Kuo YT, Wu JY, Chen MJ, Chen CC, Fang YJ, Leow AHR, Lu H, Lin JT, Tu YK, Yamaoka Y, Wu MS, Liou JM; Asian Pacific Alliance on Helicobacter and Microbiota. Primary antibiotic resistance of Helicobacter pylori in the Asia-Pacific region between 1990 and 2022: an updated systematic review and meta-analysis.Lancet Gastroenterol Hepatol. 2024;9:56-67.
[PubMed] [DOI] [Full Text][Cited in This Article: ][Cited by in RCA: 31][Reference Citation Analysis (0)]
Megraud F, Bruyndonckx R, Coenen S, Wittkop L, Huang TD, Hoebeke M, Bénéjat L, Lehours P, Goossens H, Glupczynski Y; European Helicobacter pylori Antimicrobial Susceptibility Testing Working Group. Helicobacter pylori resistance to antibiotics in Europe in 2018 and its relationship to antibiotic consumption in the community.Gut. 2021;70:1815-1822.
[PubMed] [DOI] [Full Text][Cited in This Article: ][Cited by in Crossref: 67][Cited by in RCA: 163][Article Influence: 40.8][Reference Citation Analysis (0)]
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.
[PubMed] [DOI] [Full Text][Cited in This Article: ][Cited by in Crossref: 501][Cited by in RCA: 555][Article Influence: 185.0][Reference Citation Analysis (0)]
Liu WZ, Xie Y, Lu H, Cheng H, Zeng ZR, Zhou LY, Chen Y, Wang JB, Du YQ, Lu NH; Chinese Society of Gastroenterology, Chinese Study Group on Helicobacter pylori and Peptic Ulcer. Fifth Chinese National Consensus Report on the management of Helicobacter pylori infection.Helicobacter. 2018;23:e12475.
[PubMed] [DOI] [Full Text][Cited in This Article: ][Cited by in Crossref: 187][Cited by in RCA: 319][Article Influence: 45.6][Reference Citation Analysis (0)]
Liu DS, Wang YH, Zeng ZR, Zhang ZY, Lu H, Xu JM, Du YQ, Li Y, Wang JB, Xu SP, Chen Y, Lan CH, Cheng H, Jiang MD, Zhang LX, Huo LJ, Chen SY, Zhang GX, Wu KC, Zhu X, Chen YX, Zhu Y, Shu X, Xie Y, Lu NH. Primary antibiotic resistance of Helicobacter pylori in Chinese patients: a multiregion prospective 7-year study.Clin Microbiol Infect. 2018;24:780.e5-780.e8.
[PubMed] [DOI] [Full Text][Cited in This Article: ][Cited by in Crossref: 40][Cited by in RCA: 62][Article Influence: 7.8][Reference Citation Analysis (0)]
Shao Y, Lin Y, Fang Z, Yan J, Zheng T, Ye G. Analysis of Helicobacter pylori resistance in patients with different gastric diseases.Sci Rep. 2024;14:4912.
[PubMed] [DOI] [Full Text][Cited in This Article: ][Reference Citation Analysis (0)]
