Anti–Helicobacter pylori Treatment in Patients With Gastric Cancer After Radical Gastrectomy

Zhoukai Zhao; Ruopeng Zhang; Guoming Chen; Man Nie; Feiyang Zhang; Xiaojiang Chen; Jun Lin; Zewei Chen; Feizhi Lin; Chengzhi Wei; Ziqi Zheng; Shenghang Ruan; Bowen Huang; Yingbo Chen; Runcong Nie

doi:10.1001/jamanetworkopen.2024.3812

. 2024 Mar 28;7(3):e243812. doi: 10.1001/jamanetworkopen.2024.3812

Anti–Helicobacter pylori Treatment in Patients With Gastric Cancer After Radical Gastrectomy

Zhoukai Zhao ¹, Ruopeng Zhang ¹, Guoming Chen ¹, Man Nie ², Feiyang Zhang ¹, Xiaojiang Chen ¹, Jun Lin ¹, Zewei Chen ¹, Feizhi Lin ¹, Chengzhi Wei ¹, Ziqi Zheng ¹, Shenghang Ruan ¹, Bowen Huang ¹, Yingbo Chen ^1,^✉, Runcong Nie ^1,^✉

¹Department of Gastric Surgery, State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer Center, Guangzhou, China

²Department of Medical Oncology, State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Collaborative Innovation Center for Cancer Medicine, Sun Yat-sen University Cancer Center, Guangzhou, China

Accepted for Publication: January 31, 2024.

Published: March 28, 2024. doi:10.1001/jamanetworkopen.2024.3812

^✉

Corresponding Authors: Runcong Nie, MD, PhD (nierc@sysucc.org.cn), and Yingbo Chen, MD (surgeoncyb@163.com), Department of Gastric Surgery, Sun Yat-sen University Cancer Center, No. 651 Dongfeng Eastern Rd, Guangzhou 510060, Guangdong, China.

Author Contributions: Drs Y. Chen and R. Nie had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Drs Zhao, R. Zhang, G. Chen, and M. Nie contributed equally to this work.

Concept and design: Zhao, G. Chen, F. Lin, Zheng, Y. Chen, R. Nie.

Acquisition, analysis, or interpretation of data: R. Zhang, M. Nie, F. Zhang, X. Chen, J. Lin, Z. Chen, F. Lin, Wei, Zheng, Ruan, Huang.

Drafting of the manuscript: Zhao, R. Zhang, G. Chen, M. Nie, X. Chen, J. Lin, Wei, Zheng, Ruan.

Critical review of the manuscript for important intellectual content: Zhao, F. Zhang, Z. Chen, F. Lin, Huang, Y. Chen, R. Nie.

Statistical analysis: Zhao, R. Zhang, G. Chen, M. Nie, F. Zhang, X. Chen, J. Lin, Wei, Zheng, Ruan, Huang.

Obtained funding: R. Zhang, Y. Chen, R. Nie.

Administrative, technical, or material support: Zheng.

Supervision: Y. Chen, R. Nie.

Conflict of Interest Disclosures: None reported.

Funding/Support: This work was supported by grant 202201010885 from Guangzhou Science and Technology Plan Projects (Dr R. Nie), grant 81772589 from National Natural Science Foundation of China (Dr R. Nie), grants 2114050000603 (Dr Y. Chen) and SL2024A04J01162 (Dr R. Zhang) from Guangzhou Basic and Applied Basic Research Foundation, and grants Y-tongshu2021/qn-0227 and Y-Young2022–0281 from Beijing Xisike Clinical Oncology Research Foundation (Dr R. Nie).

Role of the Funder/Sponsor: The funders had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.

Data Sharing Statement: See Supplement 2.

^✉

Corresponding author.

PMCID: PMC10979314 PMID: 38546641

Key Points

Question

Is anti–Helicobacter pylori treatment associated with enhanced postgastrectomy survival prospects for patients diagnosed with gastric cancer who have a preoperative confirmation of H pylori infection?

Findings

In this cohort study of 1293 patients, the anti–H pylori treatment group had a significant survival advantage compared with the non–anti–H pylori treatment group in terms of overall survival and disease-free survival. After propensity score matching, the survival advantage for both overall and disease-free survival remained.

Meaning

The findings indicated that for patients with gastric cancer who have H pylori infections, undergoing anti–H pylori treatment may lead to improved survival outcomes.

This cohort study of patients with gastric cancer in China examines the survival benefit associated with anti–Helicobacter pylori treatment after radical gastrectomy.

Abstract

Importance

Whether anti–Helicobacter pylori treatment can provide survival benefits for patients with gastric cancer who are diagnosed with H pylori infection is an area with limited research.

Objective

To explore the potential survival benefits of anti–H pylori treatment after radical gastrectomy in patients with gastric cancer and presurgical confirmation of H pylori infection.

Design, Setting, and Participants

This retrospective cohort study was conducted using data from patients with gastric cancer treated between January 1, 2010, and December 31, 2018, and followed up for outcome ascertainment until May 19, 2021. Propensity score matching was performed in patients treated with or without anti–H pylori treatment. This study involved a single institute in a comprehensive cancer treatment and research center located in Guangzhou, Guangdong Province, China. The study included patients with gastric or esophagogastric junction adenocarcinoma who underwent curative gastrectomy with D2 lymphadenectomy and tested positive for H pylori infection. Data were analyzed from March to June 2023.

Exposure

Anti–H pylori treatment, which primarily includes triple therapy regimens consisting of amoxicillin, clarithromycin, and omeprazole for 14 days.

Main Outcomes and Measures

Clinical outcomes, including overall survival (OS) and disease-free survival (DFS), were analyzed by Kaplan-Meier method, log-rank test, and Cox proportional hazards regression model. Subgroup analysis based on crucial clinical information was also conducted.

Results

All 1293 patients (median [IQR] age, 59 [50-65] years; 860 [66.5%] male) were divided into 2 groups, with 125 patients in the anti–H pylori treatment group and 1168 patients in the non–anti–H pylori treatment group based on whether they received anti–H pylori treatment during the perioperative period and the follow-up. Survival analysis showed that the 5-year OS rates were 94.1% (95% CI, 89.3%-99.2%) in the anti–H pylori group and 73.8% (95% CI, 70.7%-77.0%) in the non–anti–H pylori group, and the hazard ratio (HR) of these 2 groups was 0.33 (95% CI, 0.18-0.60; P < .001). The survival benefit remained after propensity score matching (HR, 0.50; 95% CI, 0.26-0.99; P = .048). Multivariable analysis for OS and DFS further showed the survival benefit of anti–H pylori treatment, with HRs of 0.38 (95% CI, 0.17-0.87; P = .02) and 0.48 (95% CI, 0.28-0.83; P = .008), respectively. Among patients with TNM stage II/III disease who received adjuvant chemotherapy, anti–H pylori treatment was associated with survival benefits (OS: HR, 0.49; 95% CI, 0.24-0.99; P = .046), whereas among those who did not receive adjuvant chemotherapy, anti–H pylori treatment was not associated with survival benefits (OS: HR, 0.29; 95% CI, 0.04-2.08; P = .22).

Conclusions and Relevance

This cohort study indicates that anti–H pylori treatment may be associated with improved survival in patients with gastric cancer who have H pylori infections. The study reinforces the importance of including H pylori screening and treatment in the surgical treatment of these patients.

Introduction

Despite a recent decrease in incidence in the past few years, gastric cancer (GC) continues to be a significant global health concern. It ranks as the fifth most common cancer and stands as the fourth leading cause of cancer-related deaths worldwide, accounting for more than 1.08 million new cases and 0.76 million deaths in 2020.¹ It has been acknowledged that Helicobacter pylori infection is a major cause of chronic gastritis, peptic ulcer, and GC.² It is estimated that 4.4 billion people worldwide are infected with H pylori. Similar to the incidence of GC, the rate of H pylori infection tends to be higher in East Asian populations.³

Numerous studies have provided substantial evidence that eradicating H pylori in healthy individuals can reduce the incidence of precancerous lesions for GC, subsequently decreasing the likelihood of developing GC.^4,5,6,7,8 In addition, several studies have reported that patients with H pylori–positive GC have better survival outcomes after GC surgery compared with those with H pylori–negative GC.^9,10,11,12 Helicobacter pylori–negative status is identified as an independent prognostic factor for poor outcomes.^10,11,12 Although several high quality randomized clinical trials (RCTs) demonstrated that eradication of H pylori after endoscopic resection of early GC can significantly reduce the incidence of the development of metachronous gastric carcinoma (MGC),^13,14 the effect of H pylori eradication in patients after gastrectomy have not yet been clarified. Two previous observational studies from Korea reported conflicting results in this setting. Kim et al¹⁵ found no significant difference in overall survival (OS), GC-specific death, and cancer recurrence rates between the anti–H pylori treatment group and the placebo group in patients with GC after distal gastrectomy. However, Choi et al¹⁶ observed a statistically significant advantage in OS and GC-specific survival for the eradication group compared with the noneradication group, with H pylori positivity identified as an independent risk factor for GC-specific death. The relationship between H pylori infection and survival rates with GC is not yet fully elucidated, limited by contradictory results, small sample size, and a paucity of high-quality related research. Thus, our study seeks to provide a deeper understanding of how anti–H pylori treatment influences postoperative survival outcomes in a larger, more diverse group of patients with GC, enhancing the scope of existing research findings. We conducted a retrospective cohort study from a high-volume institution to further explore the survival benefit of anti–H pylori treatment in patients with H pylori–positive GC after radical gastrectomy.

Methods

Patients

Retrospective collection of medical data was conducted for patients who underwent curative surgical treatment for GC at Sun Yat-sen University Cancer Center (Guangzhou, China) between January 1, 2010, and December 31, 2018. Patients were included in this cohort study if they were pathologically diagnosed as having gastric adenocarcinoma or adenocarcinoma of the esophagogastric junction, underwent curative gastrectomy with D2 lymphadenectomy, and had confirmed H pylori infection. Patients were excluded if they had other malignant tumors, were pathologically diagnosed with stage IV disease, underwent R1/2 resection, had uncertain or negative H pylori status, or had previously received anti–H pylori treatment within 3 months before the diagnosis of GC. Pathological staging, including depth of tumor invasion, lymph node involvement, and resection status, was evaluated according to the eighth edition of the American Joint Committee on Cancer’s Cancer Staging Manual.¹⁷

A total of 1293 patients who met the above criteria were included in the study (Figure 1). Patients were grouped into the anti–H pylori treatment group (125 cases) and the non–anti–H pylori treatment group (1168 cases) based on whether they received anti–H pylori treatment during the perioperative period and the follow-up. The following demographic and clinicopathologic characteristics of these patients were recorded: age, sex, comorbidities (including hypertension, coronary heart disease, and diabetes), body mass index, history of smoking, histologic grade, Borrmann classification, Lauren classification, tumor depth of invasion, lymph node metastasis, TNM staging, maximum tumor diameter, type of gastrectomy, postoperative complications, preoperative carcinoembryonic antigen level, and adjuvant chemotherapy. Written informed consent to use the samples for research purposes was obtained from all the patients before surgery. This study was performed in accordance with the Declaration of Helsinki¹⁸ and was approved by the institutional review board at the Sun Yat-sen University Cancer Center. The study followed the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) reporting guideline.

Evaluation of H pylori Infection Status

All included patients in the study underwent histologic examination with the Giemsa staining method, 13C urea breath test, and/or rapid urease test to ascertain their H pylori infection status before the gastrectomy. Patients who tested negative for H pylori infection before the gastrectomy were categorized as H pylori negative and were consequently excluded from the analysis, whereas those with 1 or more positive results were confirmed to be infected with H pylori.

Anti–H pylori Treatment

According to the World Gastroenterology Organization global H pylori guidelines, the first-line treatment includes triple or quadruple therapy regimens, and the recommended treatment duration is 7 to 14 days.¹⁹ In clinical practice, variations in antibiotic selection may occur based on patients’ condition and physicians’ preferences. During data collection, 2 independent investigators carefully reviewed the recorded medications of each patient and confirmed whether the patients received an appropriate anti–H pylori treatment. According to the data collected retrospectively, the patients in our institution primarily received a triple anti–H pylori therapy consisting of amoxicillin, clarithromycin, and omeprazole for 14 days, and they were often advised by clinicians to start anti–H pylori treatment during their postoperative follow-up, particularly 4 to 6 weeks after gastrectomy, when a positive H pylori test result was observed.

Patient Follow-Up

Patients received regular follow-up care through outpatient or inpatient visits or through telephone calls every 3 to 6 months during the initial 2 years after surgery, every 6 to 12 months during the 3 to 5 years after surgery, and annually thereafter. In this study, the median (range) follow-up time was 40.4 (0.2-131.3) months. The main follow-up examinations included physical examinations (eg, palpation of left supraclavicular lymph node and digital rectal examination), tumor marker measurement, computed tomography examination, ultrasonographic examination, and endoscopy.

Outcomes

In this study, the primary end point was OS, defined as the time from the date of surgery to the date of death from any cause. The secondary end point was disease-free survival (DFS), defined as the time from the date of surgery to disease progression, relapse, or death, whichever came first. The follow-up period for outcome ascertainment in our study extended until May 19, 2021.

Statistical Analysis

The χ² or Fisher test was used to compare differences between groups for categorical variables. Propensity score matching (PSM) was conducted to minimize the selection biases between the 2 groups in the overall cohort, with a ratio of 1:3 and a caliper value of 0.02, using the nearest matching method. The variables used for PSM included Borrmann classification, pathological T and N stages, TNM stage, tumor maximum diameter, type of gastrectomy, and adjuvant chemotherapy. This selection focused on variables that were initially imbalanced or potentially related to clinical outcomes. Kaplan-Meier analysis was used to generate the survival curves, and log-rank tests were used to compare the survival differences between groups. To explore the potential survival benefits of anti–H pylori treatment across specific patient populations, we conducted exploratory subgroup analyses based on the majority of clinical information collected, such as sex, age, and TNM staging, while taking into account the sample size. Then, in the overall cohort, the variables with statistical significance in the univariable analysis were entered into the multivariable Cox proportional hazards regression analysis for both OS and DFS. All statistical analyses were 2-sided, with P < .05 considered statistically significant. Data analysis and graphical visualization were performed using R software, version 4.2.2 (R Foundation for Statistical Computing). Data were analyzed from March to June 2023.

Results

Patient Characteristics

In this study, 1293 patients (median [IQR] age, 59 [50-65] years; 860 [66.5%] male and 433 [33.5%] female) with preoperatively confirmed H pylori infection were included. These participants had a median (IQR) body mass index of 22.0 (19.6-24.0) (calculated as weight in kilograms divided by height in meters squared), and 829 (64.1%) underwent distal gastrectomy. Postoperatively, 600 patients (46.4%) were pathologically diagnosed with TNM stage III disease and 808 (62.5%) received adjuvant chemotherapy. However, as indicated in the Table, only 125 (9.7%) had received anti–H pylori treatment. There were no statistically significant differences between the anti–H pylori treatment group and the non–anti–H pylori treatment group in terms of sex, age, body mass index, smoking history, and comorbidities. However, the anti–H pylori treatment group had a higher proportion of distal gastrectomy (102 of 125 [81.6%] vs 727 of 1168 [62.2%]; P < .001) and received less adjuvant chemotherapy (54 of 125 [43.2%] vs 754 of 1168 [64.6%]; P < .001) compared with the non–anti–H pylori treatment group. Of note, patients in the non–anti–H pylori treatment group had advanced pathological T stage, N stage, and TNM stage as well as larger tumor maximum diameter, which indicated the potential selection bias between the 2 groups.

Table. Patient Demographic, Clinical, and Pathological Characteristics Stratified by Anti–Helicobacter pylori Treatment Before and After PSM.

Variable	Anti–H pylori treatment
	Before PSM			After PSM
	Yes, No. (%) (n = 125)	No, No. (%) (n = 1168)	P value^a	Yes, No. (%) (n = 124)	No, No. (%) (n = 364)	P value^a
Sex
Male	85 (68.0)	775 (66.4)	.71	84 (67.7)	240 (65.9)	.71
Female	40 (32.0)	393 (33.6)	.71	40 (32.3)	124 (34.1)	.71
Age group, y
<60	75 (60.0)	622 (53.3)	.15	75 (60.5)	215 (59.1)	.78
≥60	50 (40.0)	546 (46.7)	.15	49 (39.5)	149 (40.9)	.78
Classification of BMI
Normal weight (18.5-24)	78 (62.4)	700 (59.9)	.59	77 (62.1)	230 (63.2)	.83
Abnormal weight (<18.5 or ≥24)	47 (37.6)	468 (40.1)	.59	47 (37.9)	134 (36.8)	.83
History of smoking
No	81 (64.8)	743 (63.6)	.79	81 (65.3)	232 (63.7)	.75
Yes	44 (35.2)	425 (36.4)	.79	43 (34.7)	132 (36.3)	.75
Hypertension
No	109 (87.2)	1005 (86.0)	.72	108 (87.1)	315 (86.5)	.87
Yes	16 (12.8)	163 (14.0)	.72	16 (12.9)	49 (13.5)	.87
Coronary heart disease
No	124 (99.2)	1155 (98.9)	>.99	123 (99.2)	359 (98.6)	>.99
Yes	1 (0.8)	13 (1.1)	>.99	1 (0.8)	5 (1.4)	>.99
Diabetes
No	119 (95.2)	1086 (93.0)	.35	118 (95.2)	342 (94.0)	.62
Yes	6 (4.8)	82 (7.0)	.35	6 (4.8)	22 (6.0)	.62
Histologic grade
G1/G2	48 (38.4)	413 (35.4)	.77	48 (38.7)	142 (39.0)	.84
G3/G4	69 (55.2)	683 (58.5)		68 (54.8)	193 (53.0)
Others	8 (6.4)	72 (6.2)		8 (6.5)	29 (8.0)
Borrmann classification
I-III	116 (92.8)	1117 (95.6)	.10	116 (93.5)	349 (95.9)	.14
IV	4 (3.2)	34 (2.9)		4 (3.2)	12 (3.3)
Unknown	5 (4.0)	17 (1.5)		4 (3.2)	3 (0.8)
Lauren classification
Diffused	50 (40.0)	445 (38.1)	.80	50 (40.3)	142 (39.0)	.56
Intestinal	31 (24.8)	328 (28.1)		30 (24.2)	110 (30.2)
Mixed	28 (22.4)	270 (23.1)		28 (22.6)	67(18.4)
Unknown	16 (12.8)	125 (10.7)		16 (12.9)	45 (12.4)
Pathological T stage
T1/2	82 (65.6)	382 (32.7)	<.001	81 (65.3)	233 (64.0)	.79
T3/4	43 (34.4)	786 (67.3)	<.001	43 (34.7)	131 (36.0)	.79
Pathological N stage
N (−)	75 (60.0)	396.(33.9)	<.001	74 (59.7)	213 (58.5)	.82
N (+)	50 (40.0)	772.0 (66.1)	<.001	50 (40.3)	151 (41.5)	.82
TNM stage
I	70 (56.0)	280 (24.0)	<.001	69 (55.6)	199 (54.7)	.85
II/III	55 (44.0)	888 (76.0)	<.001	55 (44.4)	165 (45.3)	.85
Tumor maximum diameter, cm
≤4	99 (79.2)	621 (53.2)	<.001	99 (79.8)	294 (80.8)	.82
>4	26 (20.8)	547 (46.8)	<.001	25 (20.2)	70 (19.2)	.82
Type of gastrectomy
Distal	102 (81.6)	727 (62.2)	<.001	101 (81.5)	297(81.6)	.97
Proximal	11 (8.8)	129 (11.0)		11 (8.9)	34 (9.3)
Total	12 (9.6)	312 (26.7)		12 (9.7)	33 (9.1)
CEA, ng/mL
≤5	112 (89.6)	971 (83.1)	.06	112 (90.3)	326 (89.6)	.81
>5	13 (10.4)	197 (16.9)	.06	12 (9.7)	38 (10.4)	.81
Adjuvant chemotherapy
No	71 (56.8)	414 (35.4)	<.001	70 (56.5)	202 (55.5)	.85
Yes	54 (43.2)	754 (64.6)	<.001	54 (43.5)	162 (44.5)	.85
Postoperative complication
No	116 (92.8)	1098 (94.0)	.59	115 (92.7)	344 (94.5)	.47
Yes	9 (7.2)	70 (6.0)	.59	9 (7.3)	20 (5.5)	.47

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Abbreviations: BMI, body mass index (calculated as weight in kilograms divided by height in meters squared); CEA, carcinoembryonic antigen; PSM, propensity score matching.

SI conversion factors: To convert CEA to micrograms per liter, multiply by 1.

^{^a}

Pearson χ² test or Fisher exact test.

Propensity Score Matching

To minimize the potential influence of selection bias, we used PSM. After PSM, a total of 124 patients in the anti–H pylori treatment group and 364 patients in the non–anti–H pylori treatment group were included, and the clinical characteristics between the 2 groups were well balanced (Table).

Survival Analysis of Patients According to Anti–H pylori Treatment

We conducted a survival analysis to compare OS of the 2 groups (Figure 2A). The OS rates were 95.9% (95% CI, 92.5%-99.5%) at 3 years and 94.1% (95% CI, 89.3%-99.2%) at 5 years in the anti–H pylori treatment group compared with 81.4% (95% CI, 79.0%-83.8%) at 3 years and 73.8% (95% CI, 70.7%-77.0%) at 5 years in the non–anti–H pylori treatment group. The OS difference between the 2 groups was significant (hazard ratio [HR], 0.33; 95% CI, 0.18-0.60; P < .001). After PSM, the difference in OS between the 2 groups remained statistically significant (HR, 0.50; 95% CI, 0.26-0.99; P = .048) (Figure 2B).

Subsequently, survival analysis on the DFS of the 2 groups was conducted. The DFS rates were 94.5% (95% CI, 90.3%-98.9%) at 3 years and 84.9% (95% CI, 75.6%-95.4%) at 5 years in the anti–H pylori treatment group compared with 70.0% (95% CI, 67.1%-73.1%) at 3 years and 59.2% (95% CI, 55.4%-63.3%) at 5 years in the non–anti–H pylori treatment group. As shown in Figure 2C, the anti–H pylori treatment group also had a significant advantage in DFS compared with the non–anti–H pylori treatment group (HR, 0.29; 95% CI, 0.17-0.50; P < .001). After PSM, the survival difference in DFS remained statistically significant (HR, 0.48; 95% CI, 0.27-0.87; P = .02) (Figure 2D).

Survival Analysis of Patients in Different Subgroups

Next, we conducted subgroup analysis of OS and DFS (eFigures 1 and 2 in Supplement 1). The relative treatment benefit of anti–H pylori was consistent across most of the subgroups, specifically with relation to age, sex, and tumor differentiation. In terms of TNM stage, we found that the differences in OS (HR, 0.86; 95% CI, 0.19-4.00; P = .85) (Figure 3A) and in DFS (HR, 0.62; 95% CI, 0.18-2.11; P = .44) (Figure 3B) between the anti–H pylori treatment group and non–anti–H pylori treatment group were not significant in patients with stage I disease. However, in patients with stage II/III disease, the differences in OS (HR, 0.43; 95% CI, 0.22-0.85; P = .01) (Figure 3C) and DFS (HR, 0.39; 95% CI, 0.21-0.71; P = .002) (Figure 3D) between the 2 groups were significant. We also explored the survival benefit of anti–H pylori treatment for patients with TNM stage II/III disease who did or did not undergo adjuvant chemotherapy. The results indicated that among patients who received adjuvant chemotherapy, anti–H pylori treatment conferred survival benefits for both OS (HR, 0.49; 95% CI, 0.24-0.99; P = .046) (Figure 4A) and DFS (HR, 0.41; 95% CI, 0.22-0.78; P = .006) (Figure 4B), whereas among those who did not receive adjuvant chemotherapy, anti–H pylori treatment did not provide survival benefits for either OS (HR, 0.29; 95% CI, 0.04-2.08; P = .22) (Figure 4C) or DFS (HR, 0.29; 95% CI, 0.04-2.07; P = .22) (Figure 4D).

Prognostic Factor Analysis With Cox Proportional Hazards Regression Model

Furthermore, univariable and multivariable analyses using the Cox proportional hazards regression model were performed. As detailed in eTable 1 in Supplement 1, age, Lauren classification, TNM stage, tumor maximum diameter, adjuvant chemotherapy, and anti–H pylori treatment were associated with the OS in the univariable analysis. In the multivariable analysis, age (≥60 years [HR, 1.47; 95% CI, 1.10-1.96; P = .009]), Lauren classification (intestinal type [HR, 0.67; 95% CI, 0.48-0.95; P = .02] and mixed type [HR, 0.62; 95% CI, 0.44-0.87; P = .007]), TNM stage II/III (HR, 8.87; 95% CI, 3.99-19.75; P < .001), tumor maximum diameter (>4 cm [HR, 2.33; 95% CI, 1.72-3.18; P < .001]), adjuvant chemotherapy (HR, 0.63; 95% CI, 0.46-0.85; P = .003), and anti–H pylori treatment (HR, 0.38; 95% CI, 0.17-0.87; P = .02) were identified as independent factors associated with OS. In eTable 2 in Supplement 1, univariable and multivariable analyses for DFS showed that TNM stage II/III (HR, 4.61; 95% CI, 2.84-7.49; P < .001), tumor maximum diameter (>4 cm [HR, 2.37; 95% CI, 1.87-3.01; P < .001]), and anti–H pylori treatment (HR, 0.48; 95% CI, 0.28-0.83; P = .008) remained associated with DFS.

Discussion

To the best of our knowledge, this is the largest study to investigate the survival benefit of anti–H pylori treatment in patients with H pylori–positive GC after radical gastrectomy. Our study found that postgastrectomy anti–H pylori treatment may provide substantial survival benefits in terms of both OS and DFS in a large cohort subjected to a long-term follow-up period of up to 10 years. The aforementioned conclusions remained consistent after PSM. The positive association of anti–H pylori treatment remained consistent across most subgroups, with significant OS and DFS benefits particularly pronounced in the TNM stage II/III subgroup. In contrast, the TNM stage I subgroup did not exhibit such benefits. Notably, although the patients with TNM stage II/III disease who received adjuvant chemotherapy derived benefits from anti–H pylori treatment, those who did not undergo such chemotherapy did not experience these advantages. Furthermore, Cox proportional hazards regression multivariable analysis demonstrated that anti–H pylori treatment is independently associated with both OS and DFS.

The worldwide prevalence of H pylori infection is significant. In 2015, approximately 4.4 billion individuals were infected with H pylori, constituting approximately 50% of the total population.³ Notably, H pylori infection increases the risk of GC by approximately 3 times and is the most significant risk factor for GC.²⁰ The role of H pylori infection in facilitating the development of GC is well established. However, the correlation between H pylori infection and the prognosis of patients with GC is yet to be clearly defined. Some studies have reported that patients who test negative for H pylori before undergoing curative GC surgery seem to have a worse prognosis compared with H pylori–positive patients.^2,10,11,21 Furthermore, a previous study¹² indicated that H pylori–negative GC is associated with worse OS and has intrinsic correlations with adverse pathological and clinical characteristics.

In contrast, there is evidence suggesting that H pylori infection may play a role in the progression of gastric mucosal carcinogenesis in the remnant stomach after gastrectomy for GC.²² In the Korean guidelines for H pylori, eradication of H pylori is recommended to prevent gastric mucosal dysplasia and even GC recurrence in patients who undergo distal gastrectomy.²³ Furthermore, several high-quality RCTs have demonstrated that prophylactic eradication of H pylori after endoscopic resection of early GC could prevent the development of MGC. Fukase et al¹³ reported that the odds ratio for developing MGC was 0.353 (95% CI, 0.161-0.775; P = .009) in the full intention-to-treat population, whereas the hazard ratio for developing MGC was 0.339 (95% CI, 0.157-0.729; P = .003) in the modified intention-to-treat population when comparing the eradication group with the control group. The study performed by Choi et al,¹⁴ which aimed to assess the long-term effects of H pylori eradication treatment on histologic improvement and the prevention of MGC in patients after endoscopic resection for early GC or high-grade adenoma, reported that MGC developed in 14 patients (7.2%) in the treatment group and 27 patients (13.4%) in the placebo group, with an HR of 0.50 in the treatment group (95% CI, 0.26-0.94; P = .03).

In the clinical setting, both the actual rate of anti–H pylori treatment use and the H pylori eradication rate remain low. In our study, few H pylori–positive patients (9.7%) opted for anti–H pylori treatment, and it remains an exploratory and unresolved question whether H pylori eradication is beneficial to the prognosis of patients after gastrectomy. To the best of our knowledge, only a few researchers have conducted exploratory studies in this area, and the findings are in dispute. The study conducted by Kim et al,¹⁵ which was a retrospective outcome event analysis extracted from a prospective cohort of an RCT study involving 169 patients, reported that among patients with GC after distal gastrectomy, there were no significant differences between the anti–H pylori treatment group and the placebo group in the 5-year OS, 5-year cumulative GC-specific death, and 5-year cancer recurrence rates. However, the study had certain limitations; it originated from an RCT cohort initially focused on evaluating H pylori eradication effects on mucosal atrophy and intestinal metaplasia in the remnant stomach after distal gastrectomy. Additionally, the study lacked patient stratification and was constrained by a relatively small sample size. In another study of 1031 patients with GC who underwent subtotal gastrectomy, Choi et al¹⁶ reported that the eradication group had a statistically significant advantage in terms of OS and GC-specific survival compared with the noneradication group, and this advantage persisted after PSM. However, the study included patients who tested positive for H pylori during the first postoperative gastroscopy follow-up, which occurred annually after the gastrectomy, and who underwent H pylori eradication treatment within 2 years. As a result, the interval between surgery and undergoing the test for H pylori infection in this study may be too long, and the infection status of H pylori may vary after surgery.

We designed this large-scale study to provide relevant evidence for future clinical practice for patients with GC and H pylori infection. We found that patients with H pylori infection who received anti–H pylori treatment experienced survival advantages in terms of OS and DFS compared with those who did not receive the treatment, and these advantages persisted even after PSM, similar to the previous study mentioned above.¹⁶ Furthermore, detailed stratified analyses revealed that most subgroups experienced the survival benefit of anti–H pylori treatment. In our Cox proportional hazard regression models, anti–H pylori treatment stood out as an independent prognostic factor for both OS and DFS.

Imbalances in factors related to survival between the 2 patient groups could impact the accuracy of the analysis. Therefore, it may be crucial to perform the subgroup analysis and use PSM. The previous study conducted by Choi et al¹⁶ found that H pylori eradication treatment has statistically significant survival benefits in both patients with early GC and those with advanced GC after subtotal gastrectomy. However, our subgroup analysis based on TNM stage indicated that the anti–H pylori treatment group had a significant advantage in both OS and DFS compared with the non–anti–H pylori treatment group only in patients with TNM stage II/III GC, indicating that anti–H pylori treatment may provide survival benefits only in patients with advanced-stage GC.

Another intriguing observation is that although anti–H pylori treatment offered survival benefits to the patients with TNM stage II/III who underwent adjuvant chemotherapy, no such difference was noted in those patients without adjuvant chemotherapy. This finding suggests that combining anti–H pylori treatment with adjuvant chemotherapy might offer enhanced benefits to patients. To further substantiate our conjecture, we also designed an RCT that aimed to corroborate whether anti–H pylori treatment can bring survival benefits to patients with surgically resected GC.²⁴ We hope that with the emergence of more relevant research, more effective treatment strategies will be available for patients with H pylori infection and GC.

Limitations

We acknowledge that the current study has several limitations. First, it is a retrospective analysis based on clinical data from a single institution, which may introduce selection bias. Second, the study period is relatively long, during which the details of surgical procedures and postoperative treatments received by patients may have varied. Third, the sample size is relatively small in certain subgroup analyses, which may result in limited statistical power.

Conclusion

This study’s findings indicate that for patients with GC and H pylori infection before surgery, undergoing anti–H pylori treatment may be associated with notable survival advantages. We suggest expanding the scope of future H pylori treatment guidelines and implementing thorough screening and treatment for H pylori in patients undergoing surgical treatment for GC.

Supplement 1.

eTable 1. Univariable and Multivariable Survival Analysis of Overall Survival in the Overall Cohort (Before PSM: n = 1293)

eTable 2. Univariable and Multivariable Survival Analysis of Disease-Free Survival in the Overall Cohort (Before PSM: n = 1293)

eFigure 1. Subgroup Analyses for Overall Survival According to Clinical Indicators Including Age, Gender, Tumor Differentiation, Etc

eFigure 2. Subgroup Analyses for Disease-Free Survival According to Clinical Indicators Including Age, Gender, Tumor Differentiation, Etc

jamanetwopen-e243812-s001.pdf^{(913.5KB, pdf)}

Supplement 2.

Data Sharing Statement

jamanetwopen-e243812-s002.pdf^{(16.5KB, pdf)}

References

1.Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71(3):209-249. doi: 10.3322/caac.21660 [DOI] [PubMed] [Google Scholar]
2.Wang F, Sun GP, Zou YF, et al. Helicobacter pylori infection predicts favorable outcome in patients with gastric cancer. Curr Oncol. 2013;20(5):e388-e395. doi: 10.3747/co.20.1417 [DOI] [PMC free article] [PubMed] [Google Scholar]
3.Hooi JKY, Lai WY, Ng WK, et al. Global prevalence of Helicobacter pylori infection: systematic review and meta-analysis. Gastroenterology. 2017;153(2):420-429. doi: 10.1053/j.gastro.2017.04.022 [DOI] [PubMed] [Google Scholar]
4.Chiang TH, Chang WJ, Chen SLS, et al. Mass eradication of Helicobacter pylori to reduce gastric cancer incidence and mortality: a long-term cohort study on Matsu Islands. Gut. 2021;70(2):243-250. doi: 10.1136/gutjnl-2020-322200 [DOI] [PMC free article] [PubMed] [Google Scholar]
5.Malfertheiner P. Helicobacter pylori treatment for gastric cancer prevention. N Engl J Med. 2018;378(12):1154-1156. doi: 10.1056/NEJMe1800147 [DOI] [PubMed] [Google Scholar]
6.Wong BCY, Lam SK, Wong WM, et al. ; China Gastric Cancer Study Group . Helicobacter pylori eradication to prevent gastric cancer in a high-risk region of China: a randomized controlled trial. JAMA. 2004;291(2):187-194. doi: 10.1001/jama.291.2.187 [DOI] [PubMed] [Google Scholar]
7.Suzuki H, Matsuzaki J. Gastric cancer: evidence boosts Helicobacter pylori eradication. Nat Rev Gastroenterol Hepatol. 2018;15(8):458-460. doi: 10.1038/s41575-018-0023-8 [DOI] [PubMed] [Google Scholar]
8.Ma JL, Zhang L, Brown LM, et al. Fifteen-year effects of Helicobacter pylori, garlic, and vitamin treatments on gastric cancer incidence and mortality. J Natl Cancer Inst. 2012;104(6):488-492. doi: 10.1093/jnci/djs003 [DOI] [PMC free article] [PubMed] [Google Scholar]
9.Postlewait LM, Squires MH III, Kooby DA, et al. Preoperative Helicobacter pylori infection is associated with increased survival after resection of gastric adenocarcinoma. Ann Surg Oncol. 2016;23(4):1225-1233. doi: 10.1245/s10434-015-4953-x [DOI] [PubMed] [Google Scholar]
10.Marrelli D, Pedrazzani C, Berardi A, et al. Negative Helicobacter pylori status is associated with poor prognosis in patients with gastric cancer. Cancer. 2009;115(10):2071-2080. doi: 10.1002/cncr.24253 [DOI] [PubMed] [Google Scholar]
11.Meimarakis G, Winter H, Assmann I, et al. Helicobacter pylori as a prognostic indicator after curative resection of gastric carcinoma: a prospective study. Lancet Oncol. 2006;7(3):211-222. doi: 10.1016/S1470-2045(06)70586-1 [DOI] [PubMed] [Google Scholar]
12.Tsai KF, Liou JM, Chen MJ, et al. ; Taiwan Gastrointestinal Disease and Helicobacter Consortium . Distinct clinicopathological features and prognosis of Helicobacter pylori negative gastric cancer. PLoS One. 2017;12(2):e0170942. doi: 10.1371/journal.pone.0170942 [DOI] [PMC free article] [PubMed] [Google Scholar]
13.Fukase K, Kato M, Kikuchi S, et al. ; Japan Gast Study Group . Effect of eradication of Helicobacter pylori on incidence of metachronous gastric carcinoma after endoscopic resection of early gastric cancer: an open-label, randomised controlled trial. Lancet. 2008;372(9636):392-397. doi: 10.1016/S0140-6736(08)61159-9 [DOI] [PubMed] [Google Scholar]
14.Choi IJ, Kook MC, Kim YI, et al. Helicobacter pylori therapy for the prevention of metachronous gastric cancer. N Engl J Med. 2018;378(12):1085-1095. doi: 10.1056/NEJMoa1708423 [DOI] [PubMed] [Google Scholar]
15.Kim YI, Cho SJ, Lee JY, et al. Effect of Helicobacter pylori eradication on long-term survival after distal gastrectomy for gastric cancer. Cancer Res Treat. 2016;48(3):1020-1029. doi: 10.4143/crt.2015.264 [DOI] [PMC free article] [PubMed] [Google Scholar]
16.Choi Y, Kim N, Yun CY, et al. Effect of Helicobacter pylori eradication after subtotal gastrectomy on the survival rate of patients with gastric cancer: follow-up for up to 15 years. Gastric Cancer. 2020;23(6):1051-1063. doi: 10.1007/s10120-020-01076-2 [DOI] [PubMed] [Google Scholar]
17.Amin MB, Greene FL, Edge SB, et al. The Eighth Edition AJCC Cancer Staging Manual: continuing to build a bridge from a population-based to a more “personalized” approach to cancer staging. CA Cancer J Clin. 2017;67(2):93-99. doi: 10.3322/caac.21388 [DOI] [PubMed] [Google Scholar]
18.World Medical Association. World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA. 2013;310(20):2191-2194. doi: 10.1001/jama.2013.281053 [DOI] [PubMed] [Google Scholar]
19.Katelaris P, Hunt R, Bazzoli F, et al. Helicobacter pylori World Gastroenterology Organization global guideline. J Clin Gastroenterol. 2023;57(2):111-126. doi: 10.1097/MCG.0000000000001719 [DOI] [PubMed] [Google Scholar]
20.Cheung KS, Leung WK. Risk of gastric cancer development after eradication of Helicobacter pylori. World J Gastrointest Oncol. 2018;10(5):115-123. doi: 10.4251/wjgo.v10.i5.115 [DOI] [PMC free article] [PubMed] [Google Scholar]
21.Kang SY, Han JH, Ahn MS, et al. Helicobacter pylori infection as an independent prognostic factor for locally advanced gastric cancer patients treated with adjuvant chemotherapy after curative resection. Int J Cancer. 2012;130(4):948-958. doi: 10.1002/ijc.26081 [DOI] [PubMed] [Google Scholar]
22.Lin YS, Chen MJ, Shih SC, Bair MJ, Fang CJ, Wang HY. Management of Helicobacter pylori infection after gastric surgery. World J Gastroenterol. 2014;20(18):5274-5282. doi: 10.3748/wjg.v20.i18.5274 [DOI] [PMC free article] [PubMed] [Google Scholar]
23.Choi IJ. Current evidence of effects of Helicobacter pylori eradication on prevention of gastric cancer. Korean J Intern Med. 2013;28(5):525-537. doi: 10.3904/kjim.2013.28.5.525 [DOI] [PMC free article] [PubMed] [Google Scholar]
24.Chinese Clinical Trial Registry. Helicobacter pylori eradication combined with adjuvant chemotherapy versus adjuvant chemotherapy in locally advanced Helicobacter pylori positive gastric cancer patients: an open-label, randomized, controlled, phase 3 trial. ChiCTR2300072891. Accessed February 9, 2024. https://www.chictr.org.cn

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplement 1.

eTable 1. Univariable and Multivariable Survival Analysis of Overall Survival in the Overall Cohort (Before PSM: n = 1293)

eTable 2. Univariable and Multivariable Survival Analysis of Disease-Free Survival in the Overall Cohort (Before PSM: n = 1293)

eFigure 1. Subgroup Analyses for Overall Survival According to Clinical Indicators Including Age, Gender, Tumor Differentiation, Etc

eFigure 2. Subgroup Analyses for Disease-Free Survival According to Clinical Indicators Including Age, Gender, Tumor Differentiation, Etc

jamanetwopen-e243812-s001.pdf^{(913.5KB, pdf)}

Supplement 2.

Data Sharing Statement

jamanetwopen-e243812-s002.pdf^{(16.5KB, pdf)}

[zoi240168r1] 1.Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71(3):209-249. doi: 10.3322/caac.21660 [DOI] [PubMed] [Google Scholar]

[zoi240168r2] 2.Wang F, Sun GP, Zou YF, et al. Helicobacter pylori infection predicts favorable outcome in patients with gastric cancer. Curr Oncol. 2013;20(5):e388-e395. doi: 10.3747/co.20.1417 [DOI] [PMC free article] [PubMed] [Google Scholar]

[zoi240168r3] 3.Hooi JKY, Lai WY, Ng WK, et al. Global prevalence of Helicobacter pylori infection: systematic review and meta-analysis. Gastroenterology. 2017;153(2):420-429. doi: 10.1053/j.gastro.2017.04.022 [DOI] [PubMed] [Google Scholar]

[zoi240168r4] 4.Chiang TH, Chang WJ, Chen SLS, et al. Mass eradication of Helicobacter pylori to reduce gastric cancer incidence and mortality: a long-term cohort study on Matsu Islands. Gut. 2021;70(2):243-250. doi: 10.1136/gutjnl-2020-322200 [DOI] [PMC free article] [PubMed] [Google Scholar]

[zoi240168r5] 5.Malfertheiner P. Helicobacter pylori treatment for gastric cancer prevention. N Engl J Med. 2018;378(12):1154-1156. doi: 10.1056/NEJMe1800147 [DOI] [PubMed] [Google Scholar]

[zoi240168r6] 6.Wong BCY, Lam SK, Wong WM, et al. ; China Gastric Cancer Study Group . Helicobacter pylori eradication to prevent gastric cancer in a high-risk region of China: a randomized controlled trial. JAMA. 2004;291(2):187-194. doi: 10.1001/jama.291.2.187 [DOI] [PubMed] [Google Scholar]

[zoi240168r7] 7.Suzuki H, Matsuzaki J. Gastric cancer: evidence boosts Helicobacter pylori eradication. Nat Rev Gastroenterol Hepatol. 2018;15(8):458-460. doi: 10.1038/s41575-018-0023-8 [DOI] [PubMed] [Google Scholar]

[zoi240168r8] 8.Ma JL, Zhang L, Brown LM, et al. Fifteen-year effects of Helicobacter pylori, garlic, and vitamin treatments on gastric cancer incidence and mortality. J Natl Cancer Inst. 2012;104(6):488-492. doi: 10.1093/jnci/djs003 [DOI] [PMC free article] [PubMed] [Google Scholar]

[zoi240168r9] 9.Postlewait LM, Squires MH III, Kooby DA, et al. Preoperative Helicobacter pylori infection is associated with increased survival after resection of gastric adenocarcinoma. Ann Surg Oncol. 2016;23(4):1225-1233. doi: 10.1245/s10434-015-4953-x [DOI] [PubMed] [Google Scholar]

[zoi240168r10] 10.Marrelli D, Pedrazzani C, Berardi A, et al. Negative Helicobacter pylori status is associated with poor prognosis in patients with gastric cancer. Cancer. 2009;115(10):2071-2080. doi: 10.1002/cncr.24253 [DOI] [PubMed] [Google Scholar]

[zoi240168r11] 11.Meimarakis G, Winter H, Assmann I, et al. Helicobacter pylori as a prognostic indicator after curative resection of gastric carcinoma: a prospective study. Lancet Oncol. 2006;7(3):211-222. doi: 10.1016/S1470-2045(06)70586-1 [DOI] [PubMed] [Google Scholar]

[zoi240168r12] 12.Tsai KF, Liou JM, Chen MJ, et al. ; Taiwan Gastrointestinal Disease and Helicobacter Consortium . Distinct clinicopathological features and prognosis of Helicobacter pylori negative gastric cancer. PLoS One. 2017;12(2):e0170942. doi: 10.1371/journal.pone.0170942 [DOI] [PMC free article] [PubMed] [Google Scholar]

[zoi240168r13] 13.Fukase K, Kato M, Kikuchi S, et al. ; Japan Gast Study Group . Effect of eradication of Helicobacter pylori on incidence of metachronous gastric carcinoma after endoscopic resection of early gastric cancer: an open-label, randomised controlled trial. Lancet. 2008;372(9636):392-397. doi: 10.1016/S0140-6736(08)61159-9 [DOI] [PubMed] [Google Scholar]

[zoi240168r14] 14.Choi IJ, Kook MC, Kim YI, et al. Helicobacter pylori therapy for the prevention of metachronous gastric cancer. N Engl J Med. 2018;378(12):1085-1095. doi: 10.1056/NEJMoa1708423 [DOI] [PubMed] [Google Scholar]

[zoi240168r15] 15.Kim YI, Cho SJ, Lee JY, et al. Effect of Helicobacter pylori eradication on long-term survival after distal gastrectomy for gastric cancer. Cancer Res Treat. 2016;48(3):1020-1029. doi: 10.4143/crt.2015.264 [DOI] [PMC free article] [PubMed] [Google Scholar]

[zoi240168r16] 16.Choi Y, Kim N, Yun CY, et al. Effect of Helicobacter pylori eradication after subtotal gastrectomy on the survival rate of patients with gastric cancer: follow-up for up to 15 years. Gastric Cancer. 2020;23(6):1051-1063. doi: 10.1007/s10120-020-01076-2 [DOI] [PubMed] [Google Scholar]

[zoi240168r17] 17.Amin MB, Greene FL, Edge SB, et al. The Eighth Edition AJCC Cancer Staging Manual: continuing to build a bridge from a population-based to a more “personalized” approach to cancer staging. CA Cancer J Clin. 2017;67(2):93-99. doi: 10.3322/caac.21388 [DOI] [PubMed] [Google Scholar]

[zoi240168r18] 18.World Medical Association. World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA. 2013;310(20):2191-2194. doi: 10.1001/jama.2013.281053 [DOI] [PubMed] [Google Scholar]

[zoi240168r19] 19.Katelaris P, Hunt R, Bazzoli F, et al. Helicobacter pylori World Gastroenterology Organization global guideline. J Clin Gastroenterol. 2023;57(2):111-126. doi: 10.1097/MCG.0000000000001719 [DOI] [PubMed] [Google Scholar]

[zoi240168r20] 20.Cheung KS, Leung WK. Risk of gastric cancer development after eradication of Helicobacter pylori. World J Gastrointest Oncol. 2018;10(5):115-123. doi: 10.4251/wjgo.v10.i5.115 [DOI] [PMC free article] [PubMed] [Google Scholar]

[zoi240168r21] 21.Kang SY, Han JH, Ahn MS, et al. Helicobacter pylori infection as an independent prognostic factor for locally advanced gastric cancer patients treated with adjuvant chemotherapy after curative resection. Int J Cancer. 2012;130(4):948-958. doi: 10.1002/ijc.26081 [DOI] [PubMed] [Google Scholar]

[zoi240168r22] 22.Lin YS, Chen MJ, Shih SC, Bair MJ, Fang CJ, Wang HY. Management of Helicobacter pylori infection after gastric surgery. World J Gastroenterol. 2014;20(18):5274-5282. doi: 10.3748/wjg.v20.i18.5274 [DOI] [PMC free article] [PubMed] [Google Scholar]

[zoi240168r23] 23.Choi IJ. Current evidence of effects of Helicobacter pylori eradication on prevention of gastric cancer. Korean J Intern Med. 2013;28(5):525-537. doi: 10.3904/kjim.2013.28.5.525 [DOI] [PMC free article] [PubMed] [Google Scholar]

[zoi240168r24] 24.Chinese Clinical Trial Registry. Helicobacter pylori eradication combined with adjuvant chemotherapy versus adjuvant chemotherapy in locally advanced Helicobacter pylori positive gastric cancer patients: an open-label, randomized, controlled, phase 3 trial. ChiCTR2300072891. Accessed February 9, 2024. https://www.chictr.org.cn

PERMALINK

Anti–Helicobacter pylori Treatment in Patients With Gastric Cancer After Radical Gastrectomy

Zhoukai Zhao, MD

Ruopeng Zhang, MD, PhD

Guoming Chen, MD, PhD

Man Nie, MD, PhD

Feiyang Zhang, MD

Xiaojiang Chen, MD, PhD

Jun Lin, MD

Zewei Chen, MD

Feizhi Lin, MD

Chengzhi Wei, MD

Ziqi Zheng, MD, PhD

Shenghang Ruan, MD

Bowen Huang, MD, PhD

Yingbo Chen, MD

Runcong Nie, MD, PhD

Key Points

Question

Findings

Meaning

Abstract

Importance

Objective

Design, Setting, and Participants

Exposure

Main Outcomes and Measures

Results

Conclusions and Relevance

Introduction

Methods

Patients

Figure 1. Flowchart of Patient Inclusion and Exclusion.

Evaluation of H pylori Infection Status

Anti–H pylori Treatment

Patient Follow-Up

Outcomes

Statistical Analysis

Results

Patient Characteristics

Table. Patient Demographic, Clinical, and Pathological Characteristics Stratified by Anti–Helicobacter pylori Treatment Before and After PSM.

Propensity Score Matching

Survival Analysis of Patients According to Anti–H pylori Treatment

Figure 2. Kaplan-Meier Analysis for Overall Survival and Disease-Free Survival of the Patients With Gastric Cancer in the Anti–Helicobacter pylori Treatment Group Compared With Those in the Non–Anti–H pylori Treatment Group Before and After Propensity Score Matching (PSM).

Survival Analysis of Patients in Different Subgroups

Figure 3. Kaplan-Meier Analysis for Overall Survival and Disease-Free Survival of Patients With Gastric Cancer in the Anti–Helicobacter pylori Treatment Group Compared With Those in the Non–Anti–H pylori Treatment Group in TNM Stage I and Stage II/III Subgroups.

Figure 4. Kaplan-Meier Analysis for Overall Survival and Disease-Free Survival of the Patients With TNM Stage II/III Gastric Cancer Comparing Anti–Helicobacter pylori With Non–Anti–H pylori Treatment Groups in the Subgroups Receiving and Not Receiving Adjuvant Chemotherapy .

Prognostic Factor Analysis With Cox Proportional Hazards Regression Model

Discussion

Limitations

Conclusion

References

Associated Data

Supplementary Materials

ACTIONS

PERMALINK

RESOURCES

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