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  • Review Article
  • OPEN ACCESS

Prevention and Screening of Gastric Cancer by Helicobacter pylori Management: Synthesis of Existing Data

  • Xianzhu Zhou,
  • Zhaoshen Li and
  • Yiqi Du* 
 Author information  Cite
Cancer Screening and Prevention   2023;2(4):260-269

doi: 10.14218/CSP.2023.00010

Abstract

Gastric cancer (GC) is a preventable disease, and Helicobacter pylori infection is the most important controllable risk factor. Despite numerous studies confirming that eradicating H. pylori can reduce the risk of GC, there remains a significant gap between the fundamental and clinical knowledge and public health interventions. This article provides a review of the progress made in the last decade by gastroenterologists in understanding the carcinogenic effects of H. pylori. The authors also summarize the evidence demonstrating the beneficial effects of eradication of H. pylori on gastric precancerous lesions and GC, and outline current strategies for H. pylori management. Notably, a family-based approach to H. pylori management represents a novel strategy for future GC prevention and control, boasting numerous advantages and having the potential to play a crucial role in future policymaking.

Keywords

Helicobacter pylori, Gastric cancer, Prevention

Introduction

Gastric cancer (GC) is a major cause of cancer-related deaths worldwide. According to global cancer statistics,1 1,089,103 new cases of GC and 768,793 related deaths occurred in 2020, ranking fifth and third for cancer incidence and mortality, respectively. In China, GC causes a leading burden of 0.40 to 0.47 million deaths per year.2,3 Over the last few decades, several key risk factors for the development of GC have been identified, including tobacco use, high salt intake, older age, and a family history of GC. Among these factors, Helicobacter pylori infection has been identified as the most important preventable and controllable risk factor owing to the nature of this highly virulent bacterium being able to be detected and treated, as emphasized in multiple international consensus reports.4–6 In fact, China has a high prevalence of both H. pylori infection and GC. More than 40% (478,508 of 1,089,103) of GC cases worldwide were identified in China, which is alarmingly high given that China accounts for only 25% of the world’s population. The fact that the H. pylori infection rate is 44% in the general Chinese population further confirms this trend. The high concordance of H. pylori-prevalent areas having high cancer incidence provides significant potential benefits and valuable opportunities to implement national GC prevention and control initiatives.

Although there exists substantial, high-quality research elaborating the effect and affordability of different GC prevention approaches, few systematic reviews have been performed to synthesize trial results and provide definite conclusions based on dynamic epidemiological changes in China. In this article, we aim to synthesize the latest evidence on the rationale of H. pylori management, the effect of various H. pylori management, and various established H. pylori management approaches. We hope our results will help focus future research directions and inform policy-making on GC prevention in China, as well as in other countries carrying a high cancer burden in the foreseeable future.

Rationale of H. pylori eradication for GC prevention

The relationship between H. pylori and stomach-related diseases has been a focus of gastroenterologists since its discovery by Barry J Marshall and J. Robin Warren in 1983.7 The Correa cascade, a stepwise progression from atrophy to metaplasia, dysplasia, and ultimately gastric adenocarcinoma initiated by H. pylori infection, provides a useful framework for understanding the carcinogenic mechanisms involved.8 In fact, most clinical investigations into the relationship between H. pylori and GC can be divided into three main topics (Fig. 1): (1) examining the correlation between H. pylori infection and GC, (2) assessing whether eradication of H. pylori can prevent the development of GC, and (3) determining the feasibility of eradicating H. pylori on a population scale as a preventive measure against GC.

Main topics of investigations of the relationship between <italic>Helicobacter pylori infection</italic> and gastric cancer.
Fig. 1  Main topics of investigations of the relationship between Helicobacter pylori infection and gastric cancer.

Hp, Helicobacter pylori.

Does H. pylori infection lead to GC (correlation between H. pylori infection and GC)?

During the period from the 1980s to the 2000s, numerous studies have directly or indirectly indicated a causal relationship between H. pylori infection and GC. For instance, in animal model trials in 1998, Watanabe9 reported that 37% of Mongolian gerbils orally inoculated with H. pylori developed GC within 62 weeks. Epidemiological studies10 conducted in 1991 also suggested that infection with H. pylori was associated with a 3.6-fold increased risk of GC, marking an important milestone in the understanding of H. pylori. Currently, it is recognized that up to 89% of noncardia gastric cancer cases can be attributed to chronic H. pylori infection,11 while H. pylori-negative GC accounts for only 0.4–2.3% of cases.12 This valuable recognition is intricately connected with relevant studies conducted during the late 20th century.

Could H. pylori eradication counteract the progression of precancerous lesions and block the development of GC?

In the 21st century, as consensus was reached regarding the carcinogenic potential of H. pylori, academic attention of medical specialists has gradually shifted to the effectiveness of H. pylori eradication on GC prevention, both for clinical utility and public health considerations. A number of high-quality randomized controlled trials (RCTs) were initiated in China (Yantai,13 Shandong,14 Fujian,15 Taiwan16), and Korea,17 and after years of follow-up, most of the findings were published between 2010 and 2020. As research deepened, understanding of the benefits of H. pylori eradication can be broadly divided into two stages.

Firstly, H. pylori treatment can block the progression of precancerous disease along the stepwise inflammatory pathway. A randomized double-blind, placebo-controlled trial13 in China with 435 farmers infected with H. pylori, randomized to either therapy or placebo groups, demonstrated that treatment of H. pylori is protective against premalignant gastric lesions progression over a median of 10 years of follow-up. Gastric precancerous disease can also be reversed to lower-level lesions or even normal mucosa, as shown by a mass H. pylori chemoprevention program on Taiwan Matsu Island.18 In this community-based study, the prevalence of gastric atrophy in 1,762 residents declined from 59.9% in 2004 (immediately before eradication) to 13.7% in 2008 (4 years after intervention), yielding an effectiveness of 77.2% in reversing gastric atrophy. Prior to 2017, the generally accepted point-of-no-return theory stated that by H. pylori eradication, the histological severity of intestinal metaplasia (IM) or dysplasia could not be reduced, nor the progression toward GC be halted or reversed, with this view adopted by the Maastricht consensus.4 However, studies with longer follow-up periods have demonstrated significant regression in IM. Extending the follow-up period from 4 to 14 years for the previously mentioned mass eradication study in Matsu Island16 revealed a decrease in the prevalence rates of both early and advanced-stage IM from 31.7 to 21.4% and from 11.8 to 1.8%, respectively. A subsequent meta-analysis19 supported this conclusion, which has now been accepted in the guideline of latest version.20 The development of GC involves a complex and protracted evolution over several years. Although studies with longer follow-up periods are more challenging to conduct due to financial and medical limitations, they typically yield more objective and robust conclusions, providing a more comprehensive understanding of disease progression and treatment efficacy.

Secondly, eradication of H. pylori has been shown to reduce the incidence of GC. In recent years, several high-quality meta-analyses have assessed the benefits of H. pylori eradication in preventing GC (Table 1).21–27 These studies, with low heterogeneity, consistently demonstrate H. pylori eradication has a strong preventive effect on GC, with relative risks ranging from 0.46 to 0.66 for both primary and metachronous cancer. Ford’s conclusion,21 although limited to three trials, further indicates that H. pylori eradication not only reduces the incidence of GC, but also leads to a decrease in disease-specific mortality. This finding highlights the importance of H. pylori treatment as a preventive measure and suggests directions for future investigations. In this section, the argument regarding the “point of unstoppable” persists, as demonstrated by Chen et al.22 that eradication of H. pylori in lesions have progressed to IM does not significantly reduce the incidence of GC. However, Sugano study23 found the benefit of eradication was strongly correlated with time to eradication, and the reduction in incidence after eradication was significantly greater (p = 0.01) in groups with long-term (> 5 years) follow-up (odds ratio of 0.32) compared with those with shorter follow-up (< 5 years). Hence, confirming the potential benefit of H. pylori eradication for preventing GC in IM patients is still required. It is important to note that most of the studies included in the current meta-analyses were conducted in East Asia. Given the variability of GC heterogeneity by ethnicity in multi-ethnic societies, caution should be exercised when extrapolating above conclusions in other populations without sufficient evidence.

Table 1

High-quality meta-analysis evaluating the association between Helicobacter pylori eradication and GC development

First author, yearCountryDatabase (timespan)Sample sizeStudy inclusionEnrolled targetsGC incidence
GC mortality
EffectRRHeterogeneityEffectRRHeterogeneity
Ford AC, 201424UKMedline (1946–2013); Embase (1947–2013); Cochrane central register6,4976 RCTsHealthy asymptomatic infected Asian adults1.6% vs. 2.4%0.66I2 = 0%NA
Ford AC(a), 202021UKMEDLINE (1947 to February 2020); Embase and Embase Classic (1947 to February 2020); Cochrane central register8,3237 RCTsHealthy asymptomatic infected adults1.6% vs. 3.0%0.54I2 = 0%1.14% vs. 1.87%0.61I2 = 0%
Ford AC(b), 202021UKSame as above1,8413 RCTsIndividuals after GC resection4.5% vs. 9.3%0.49I2 = 0%NA
Chen HN, 201622ChinaMEDLINE, EMBASE, Cochrane Library (up to March 2014)7,9558 RCTsIndividuals with normal mucosa or precancerous lesions1.9% vs. 2.9%0.64 (< IM RR = 0.25); (≥ IM RR = NS)I2 = 0%
Sugano K, 201923JapanMEDLINE and Ichushi-Web (up to December 2016)31,10632 (RCTs and cohort studies)Individuals with normal mucosa, precancerous lesions, peptic ulcer, or GC undergone resection1.9% vs. 3.6%0.46I2 = 15%
Lee YC, 201625China (Taiwan)PubMed, Cochrane Library, ClinicalTrials.gov (up to May 2015)48,06424 (8 RCTs and 16 cohort studies)Individuals with normal mucosa or after GC resection1.2% vs. 1.7%0.54I2 = 0%
Doorakkers E, 201626SwedenPubMed, Web of Science, Embase, and Cochrane Library (up to November 2015)31,5449 (1 RCT and 8 cohort studies)General population0.9% vs. 1.1%0.46I2 = 32.3%
Duan F, 201927ChinaMEDLINE, PubMed, EMBASE, the Cochrane Library, China National Knowledge Infrastructure, and Wanfang (January 1997 to January 2017)40,74013 (4 RCTs and 9 cohort studies)Individuals with normal mucosa or precancerous lesions0.13% vs. 0.14%0.52I2 = 0%

GC, gastric cancer; NA, not available; NS, not significant; RCT, randomized controlled trial; RR, risk ratio.

Is it feasible to eradicate H. pylori on a population scale to prevent GC?

Clarifying the effectiveness of H. pylori eradication in preventing GC serves as a strong basis to support population-wide strategies as policy recommendations. The Taipei Consensus28 published in 2020 discussed the feasibility of population-based screening, marking the gradual emergence of population-based screening as a mainstream issue for policy makers. However, a variety of factors must be considered when initiating a universal H. pylori screening program.

Target countries or areas

Mass screening for H. pylori infection should prioritize countries or regions with a high burden of both H. pylori infection and GC, since programs in highly H. pylori-infected regions could obtain higher screening efficiency and additional health benefits by identifying more H. pylori-infected participants with equal number of tests conducted. However, the carcinogenic effect of H. pylori infection does not show uniformity across global regions but is influenced by various factors, such as ethnicity and the type of infected strain. African and certain Asian countries, such as India, exhibit a high prevalence of H. pylori infection ranging from 63.5 to 87.7%,29 surpassing the global average of 44.3%30; but their age-standardized GC incidence (4.5 per 100,000) is significantly lower than the world average of 11.10/100,000.1 Population-wide eradication is only necessary and feasible in areas where H. pylori infection is clearly carcinogenic, that is, where both H. pylori infection and GC incidence are remaining in high levels. East Asia is known for its high incidence of GC; in particular, nearly 40% of GC cases seen globally occurred in China,1 a typical country of both H. pylori and GC prevalence. A recent decision analysis synthesizing data from China’s latest epidemiological surveys and trial results concluded that implementing a universal eradication program for H. pylori would be cost effective in reducing the cancer burden in the long term.31 This program may serve as a reference for other countries or regions with similar epidemiological conditions. Recently, an effect of H. pylori eradication on the incidence of noncardia gastric adenocarcinoma was observed in a large diverse population in the USA.32 In 716,567 individuals with a history of H pylori testing and/or treatment, the adjusted subdistribution hazard ratios (HRs) and 95% confidence intervals (CIs) of GC for H pylori-positive/untreated and treated individuals were 6.07 (4.20–8.76) and 2.68 (1.86–3.86), respectively, compared with H pylori-negative individuals.

Target populations

Different demographic characteristics of the target population can result in varying levels of benefit. Health economics evaluations33,34 have consistently shown that H. pylori screening at a younger age (20–40 years) is more cost-effective owing to the higher efficacy of GC prevention. This can be attributed to the degree of mucosal damage at the time of intervention. H. pylori infection primarily occurs during childhood and adolescence and tends to persist in the absence of external intervention. Therefore, the age of the patient is considered an indicative factor of the duration of the infection and the extent and severity of the damage to the gastric mucosa. In 2016, a meta-analysis22 consisting of 7,955 subjects concluded that after H. pylori eradication therapy, the relative risk of GC decreased by 12% in 2,115 participants with IM at baseline compared to controls, and by 75% in 1,337 participants without precancerous lesions or with only atrophy, indicating early eradication of H. pylori during the early stages of mucosal damage provides the greatest benefit. In other words, the earlier the eradication of H. pylori, the greater the benefit.

Although severe damage, such as advanced-stage IM and extensive dysplasia, is more commonly observed in older individuals, there are still significant benefits to performing H. pylori eradication in this population. A retrospective study conducted in Hong Kong, China, involving 73,237 patients who had undergone H. pylori eradication and were followed up for 7.6 years, revealed that the risk of GC was reduced by 18% among individuals over 60 years of age. Therefore, the eradication of H. pylori in elderly patients is to be encouraged.

Improving the eradication success rate

Effective control of GC relies on successful eradication of H. pylori. An RCT15 conducted in Fujian, China in 2022 showed failure of first-line H. pylori therapy did not result in a statistically significant benefit in preventing GC over a 26.5-year follow-up period (HR = 0.46, p = 0.289) compared with those who achieved successful treatment (HR = 0.46, p = 0.009). Based on the experience gained from extensive screening initiatives,17,35,36 the current success rate of eradicating H. pylori infection is limited, ranging from 70.1 to 78.2%, with considerable potential for further enhancement. Scientific and effective selection of first-line treatment regimens, along with timely adjustments based on regional variations, can significantly offset these deficiencies, and this is particularly crucial given the primary resistance rates to clarithromycin, metronidazole, and levofloxacin exceeding 15% in all regions.37 As outlined in the VI consensus report,20 the first-line algorithm for empirical H. pylori eradication in areas with low clarithromycin resistance includes bismuth quadruple therapy [proton pump inhibitor (PPI), bismuth, tetracycline, and metronidazole] and clarithromycin triple therapy (PPI, clarithromycin, and amoxicillin). In areas with high (> 15%) clarithromycin resistance, the recommended first-line treatments are bismuth quadruple therapy and nonbismuth quadruple therapy (PPI, clarithromycin, amoxicillin, and metronidazole). Triple therapy based on potassium-competitive acid blockers (also referred to as P-CAB) also demonstrated promising results in achieving high eradication rates among patients infected with clarithromycin-resistant strains.38 Meanwhile, regular monitoring of treatment efficacy in at least a subset of the population is crucial for timely adjustment of the regimen before resistance compromises therapy effects, as empirical therapy failing to achieve a cure rate of at least 90% should be abandoned.39

The failed eradication of H. pylori has become a growing concern because of the continuous increase in antibiotic resistance rates. The latest Chinese national guideline on H. pylori40 recommends treatment based on the patient’s history of antibiotic use in empirical treatment and the utilization of antibiotic sensitivity tests (ASTs) in individuals with a previous history of treatment failure. Data from China41–43 suggests that personalized therapy guided by ASTs has a higher eradication rate compared with empirical treatment regimens, resulting in an average increase of 56–126 successful eradication cases per 1,000 patients. For refractory H. pylori infection (unsuccessful eradication after two consecutive standardized eradication treatments), the use of low-resistance antibiotics such as tetracycline and furazolidone yields better eradication outcomes.40

Compliance considerations

While symptomatic patients with H. pylori infection are more likely to undergo voluntary eradication, the majority of H. pylori-infected individuals from population screening programs are asymptomatic. This presents a significant challenge to the adherence of H. pylori management. For example, the implementation of a large-scale H. pylori screening program in Taiwan revealed that 20% of participants (3,764 of 18,821) did not respond to an invitation for a 13C-urea breath test (13C-UBT), and 17.31% of H. pylori-infected patients (5,493 of 6,643) refused the eradication therapy.44 Another study demonstrated that 10% of patients prescribed H. pylori eradication regimen failed to take even 60% of their medications.45 Consequently, ensuring compliance with screening and treatment protocols needs to be emphasized. (1) Compliance with H. pylori screening: Noninvasive screening tests, such as the 13C-UBT, Helicobacter pylori stool antigen (HpSA) test, and serology testing, can help mitigate negative emotions and resistance to treatment. The 13C-UBT is the most precise noninvasive screening method, but it necessitates fasting prior to testing and a 30 m wait between two expirations. Although serology tests are the most convenient, they are not able to differentiate between current and previous infections. The HpSA test is less commonly used for screening and is not well-received by the general population. Also, H. pylori infection status can be accurately assessed by magnetic controlled capsule endoscopy.46 (2) Compliance with H. pylori therapy: The willingness to receive antibiotic therapy and the ability to adhere to the prescribed regimen are prerequisites for effective eradication. However, the incidence of short-term adverse events during treatment may discourage patients from receiving treatment, leading to lower levels of compliance.47 The European Registry on H. pylori management conducted a prospective analysis of 22,492 patients who underwent eradication therapy and found that 23% of the patients experienced at least one adverse event during medication. The most common adverse reactions observed were taste disturbance (7%), diarrhea (7%), nausea (6%), and abdominal pain (3%).48 Notably, the classic bismuth-based quadruple therapy regimen, which is widely used worldwide, was associated with a higher incidence of side effects of 37%. At the same time, long-term adverse events, such as antimicrobial resistance, constitute a potential concern for treated patients. (3) Compliance with follow-up retesting: In the context of increasing drug resistance, post-treatment retesting is becoming increasingly important. A negative test result would be considered as the official endpoint of treatment process. According to the fifth edition of the Chinese consensus on H. pylori eradication,49 retesting should be performed 4–6 weeks after medication cessation to minimize the impact of residual drugs (such as PPIs, bismuth, and antibiotics) on test results.

Active promotion of knowledge about H. pylori, including its potential gastrointestinal (GI) and extra-GI harms, as well as the benefits of eradication therapy, could be an effective approach to improving compliance among the public.50 Specific ways to conduct public education include strengthening publicity through mass media and providing health education at the community and individual level. Physicians-targeted education is also important, as study found significant proportion (more than 30%) of physicians may have incorrect knowledge or inappropriate use of eradication regimens and antibiotic combinations.48 Ensuring patients receive the appropriate treatments would be a powerful tool in overcoming public skepticism.

Existing H. pylori management strategies

In 1997, gastroenterologists from the European Helicobacter Study Group suggested performing H. pylori testing in patients over 45 years old who have dyspeptic symptoms. This recommendation was later established as a “test and treat strategy” in the Maastricht III consensus (Table 2),5,51,52,53,54 which was published in 2007. The strategy does not necessitate physicians to engage in community-based surveillance to identify infected patients. Instead, it relies on testing patients who present to the hospital with GI symptoms for H. pylori infection and is therefore categorized as a passive screening measure. Despite the recommendation for implementing the strategy in highly infected areas, it has a limited target audience and efficacy in meeting the needs for H. pylori eradication in highly infected countries, and is unable to provide a sufficiently powerful intervention for reducing population infection levels.

Table 2

Comparison of existing Helicobacter pylori management strategies

StrategyTest and treatScreen and treat (also called “search and screen” strategy)Family-based control and management
AimsGC prevention and dyspeptic symptom controlGC preventionGC prevention and intrafamily spread interruption
Target populationsUninvestigated dyspeptic patients with no alarm symptomsPopulations with a high incidence or high risk of GC. intermediate or high incidence of GC.Cohabitants and family members of H. pylori-infected patients
Target areasH. pylori-prevalent regions (>20%)Incidence of GC higher than 15–20 per 100,000.Both high and low prevalent regions
Type of strategyPassiveActiveEither active or passive
RecurrenceModerateModerateLow
Eradication rates>80%>80%>90%
Cancer prevention effectLow to ModerateHighModerate to high
CostLowHighModerate
Benefit-cost ratioModerate to highModerate to highHigh
ComplianceModerateModeratePotentially high (awaiting evidence)
H. pylori detection abilityModerateModerateModerate (slightly higher)
Formal inception, yearMaastricht II53 and III51 Consensus Report, 2000–2006Maastricht IV Consensus Report5 and Kyoto global consensus report,54 2006–2015Chinese Consensus Report on Family-Based H. pylori Infection,52 2022

H. pylori detection ability refers to the number of H. pylori-infected participants identified under conducting an equal number of tests. GC, gastric cancer; H. pylori, Helicobacter pylori.

The 2012 Maastricht IV Consensus5 proposed a screen and treat strategy (Table 2) to effectively address the aforementioned issues by expanding the screening audience from solely outpatients to the entire population of a given region. In contrast to the test and treat approach, which depends on patients seeking care at clinics, this strategy involves policymakers making deliberate efforts to search and detecting H. pylori carriers within the community, making it an active screening strategy. Population-based mass eradication programs for H. pylori have been implemented in various regions, including Japan,55 mainland China,35 and Taiwan,16 using both invasive testing (endoscopy) and noninvasive methods (e.g., 13C-UBT). For example, from 2004 to 2018, a large-scale H. pylori screening program was conducted in Ma Zu, resulting in a notable reduction in the H. pylori prevalence from 64.2% to 15.0% in the local population.16 Furthermore, this program led to a significant decrease in the incidence and mortality of GC by 53% and 25%, respectively, providing compelling evidence to confirm the effectiveness of “screen and treat” strategy in cancer prevention.

China is a vast country with a population of more than 1.4 billion individuals and nearly 500 million households, as per the seventh National Census.56 Achieving population-wide H. pylori eradication often requires years or decades and re-infection among the selected population would be inevitable during the lengthy process of screening implementation if the screen and treat strategy is directly applied in China. In addition, the significant regional variation of infection rates across the country combined with the uneven distribution of medical resources, further weakens the feasibility of this strategy.

In 2021, a group of Chinese scholars proposed a novel approach,52 a family-based H. pylori management strategy (Table 2), to prevent and control H. pylori infection at the community level. It supplements the first two existing strategies and focuses on countries with high rates of GC and limited per capita resources. This approach is not designed to function autonomously from the previous two strategies, but rather serves to enhance their efficacy and applicability in real-world settings. The family strategy, integrated with the test and treat approach, encompasses screening, treatment, and follow-up care for family members after identifying an H. pylori-carrier during outpatient visit, with aims to enhance family engagement, awareness, and contain the probability of bacterial transmission within the household. When used in conjunction with the screen and treat approach, the family screening strategy entails modifying the basic H. pylori screening unit from individuals to the entire family, with all family members being screened before moving on to the next household. The primary difference between family-based screening and conventional strategies lies in the order of individual screening during the procedure, despite the ultimate objective being unchanged of testing the entire population.57 The latest guideline from China provided feasible eradication treatment for completing the family screening strategy.40 Also, compared with a genetic cause, H. pylori has a larger role in GC development.58

The advantages of family-based strategy (Table 2) are: (1) Applicability in both high and low infection areas. The phenomenon of H. pylori family clustering has been demonstrated in various regions worldwide,58–61 indicating the universal suitability of the family-based strategy across regions and ethnicities. (2) Blocking intrafamily transmission. Eliminating the source of H. pylori infection in households can reduce the risk of children acquiring the bacterium and provide long-term benefits to newborns. A meta analysis62 confirmed that H. pylori family management strategies have higher success rates in eradicating H. pylori infection and lower rates of recurrence compared with traditional individual-based approaches. (3) Higher patient compliance, as family management strategies are intrinsically linked to the health of household members and cohabitants, trial participants may exhibit greater enthusiasm and higher levels of compliance for undergoing screening. This may lead to a swifter implementation of the program. (4) Higher cost-effectiveness, according to a health economics analysis, family-based strategies were more cost-effective than screen-and-treat strategies, with a cost of $9.18 per quality-of-life year gained, as opposed to $12.08 for the latter.63 (5) Better H. pylori detection, as the efficiency of screening would be enhanced by searching along the H. pylori intrafamilial transmission chain, compared with random selection. The family-based strategy has a potentially higher yield for detecting H. pylori-infected individuals, with approximately 4.02% more infections identified with equal numbers of tests conducted.64

Conclusions

GC is a preventable disease, and H. pylori infection is the most important controllable risk factor, serving as an essential step toward effective prevention and control of GC. Despite numerous studies confirming that eradicating H. pylori reduces the risk of GC, there remains a significant gap between fundamental and clinical knowledge and public health interventions. A family-based approach to H. pylori management represents a novel strategy for future GC prevention and control, boasting numerous advantages and having the potential to play a crucial role in future policy making. In addition, secondary screening measures for GC based on H. pylori represent a critical focus of attention (Table 3).65–81 Both primary and secondary preventive strategies are crucial components of effective GC management. Much like the indispensable nature of both legs in bipedal locomotion, either strategy cannot be overlooked without compromising the overall efficacy of the treatment.

Table 3

Screening models or strategies for GC that includes indicators of Helicobacter pylori infection

ModelCountryTarget populationSample sizeIndicators included in the modelDiscrimination
Prediction models
  Ikeda F, 201665JapanGeneral Japanese population2,446PG, H. pylori0.77
  Taninaga J, 201966Healthy population1,431H. pylori serology testing and chronic atrophic gastritis, sex, age, and body mass index, white blood cell counts, neutrophil ratio, lymphocyte ratio, eosinophil ratio, monocyte ratio, basophil ratio, platelet count, hemoglobin, mean corpuscular volume, and hemoglobin A1c, gastric, or duodenal ulcers including scars, GERD, or Barrett’s esophagus and postgastrectomy0.736–0.874
  Charvat H, 201667JapanJapanese residents19,028Age, family GC history, smoking, salted food, PG, H. pylori0.768
  Murphy JD, 202268USAHealthy individuals across Japan, China, and Korea1,422Sex, age, UreA, Hp 0305, Hp 1564, PGs0.738
  Ishikura N, 202169JapanParticipants of the Hospital Epidemiology Research Program3,678Age, ABCD classification defined by H. pylori and PGs, smoking, alcohol consumption, fruit and vegetable intake, and 3 GWAS-identified SNP polymorphisms0.77–0.78
  Song M, 201870USAFinnish male smokers21,895PGI, H. pyloriNA
  Lee TY, 201571ChinaPatients with Peptic Ulcer Disease from Taiwan278,898Age, sex, ulcer site, ulcer complication, H. pylori eradication, NSAIDs duration, surveillance endoscopy0.78
Diagnostic models
  Tu, 201772ChinaPopulation from high GC mortality area9,002PGI, PGII, PGR, G-17, H. pylori IgG0.803
  Iida M, 201773JapanGeneral Japanese population2,444Age, sex, H. pylori and atrophic gastritis, Hemoglobin A1c, Current smoking0.79
  So JBY, 202174SingaporeSingapore Chinese population682miRNAs, Age, H. pylori, PG, CA199, CEA0.849–0.890
  Cai QC, 201975ChinaChinese individuals with a ‘high risk’ of GC14,929Age, H. pylori, sex, pickled food, fried food, PG, G-170.73–0.76
  Tao W, 202076ChinaChinese individuals with precancerous lesions383Age, sex, tap water drinking, H. pylori infection, GC family history, PGs
  Park CH, 201677JapanConsecutive Japanese patients562Age, sex, PGs, H. pyloriNA
  Liu MM, 201878ChinaPatients with gastric diseases62034 variables including age, BMI, sex, H. pylori infection0.62–0.74
  Ji L, 202079ChinaGeneral residents7,773Positive family history of GC in first-degree relatives, PG, H. pylori, ageNA
  Lin JT, 199580ChinaSubjects underwent endoscopy from Taiwan686Peptic ulcer, PGI, H. pylori0.84
  Kaise M, 201181JapanMedical health checkup population1,446TFFs, PGs, H. pylori0.812–0.893

BMI, body mass index; CA199, carbohydrate antigen 19-9; CEA, carcinoembryonic antigen; G-17, gastrin-17; GC, gastric cancer; GERD, gastroesophageal reflux disease; H. pylori, Helicobacter pylori; NA, not available; PG, pepsinogen; TFF, trefoil factor; urea, urease subunit a.

Abbreviations

13C-UBT: 

13C-urea breath test

AST: 

antibiotic sensitivity tests

GC: 

gastric cancer

GI: 

gastrointestinal

HpSA: 

Helicobacter pylori stool antigen

HR: 

hazard ratio

IM: 

intestinal metaplasia

P-CAB: 

potassium-competitive acid blockers

PPI: 

proton pump inhibitor

RCT: 

randomized controlled trial

Declarations

Acknowledgement

None.

Funding

This investigation was supported by the grant from the three-year action plan for the construction of Shanghai’s public health system (2023–2025), key discipline construction project (GWVI-11.1-21), and 2020 Hainan Provincial Major Science and Technology Program (No. ZDKJ202005).

Conflict of interest

Prof. Zhaoshen Li has been an editor-in-chief of Cancer Screening and Prevention since August 2021. Prof Yiqi Du has been an executive associate editor of Cancer Screening and Prevention since December 2022. Xianzhu Zhou has no other conflict of interests related to this publication.

Authors’ contributions

Contributed to study concept and design (YD and ZL), acquisition of the data (XZ and YD), assay performance and data analysis (XZ and YD), drafting of the manuscript (XZ and YD), critical revision of the manuscript (YD and ZL), supervision (YD and ZL). All authors have made a significant contribution to this study and have approved the final manuscript.

References

  1. Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, 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 View Article PubMed/NCBI
  2. Yan X, Lei L, Li H, Cao M, Yang F, He S, et al. Stomach cancer burden in China: Epidemiology and prevention. Chin J Cancer Res 2023;35(2):81-91 View Article PubMed/NCBI
  3. Zheng R, Zhang S, Zeng H, Wang S, Sun K, Chen R, et al. Cancer incidence and mortality in China, 2016. Journal of the National Cancer Center 2022;2:1-9 View Article
  4. Malfertheiner P, Megraud F, O’Morain CA, Gisbert JP, Kuipers EJ, Axon AT, et al. Management of Helicobacter pylori infection-the Maastricht V/Florence Consensus Report. Gut 2017;66(1):6-30 View Article PubMed/NCBI
  5. Malfertheiner P, Megraud F, O’Morain CA, Atherton J, Axon AT, Bazzoli F, et al. Management of Helicobacter pylori infection—the Maastricht IV/ Florence Consensus Report. Gut 2012;61(5):646-664 View Article PubMed/NCBI
  6. Du Y, Zhu H, Liu J, Li J, Chang X, Zhou L, et al. Consensus on eradication of Helicobacter pylori and prevention and control of gastric cancer in China (2019, Shanghai). J Gastroenterol Hepatol 2020;35(4):624-629 View Article PubMed/NCBI
  7. Marshall BJ, Warren JR. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 1984;1(8390):1311-1315 View Article PubMed/NCBI
  8. Correa P. Human gastric carcinogenesis: a multistep and multifactorial process—First American Cancer Society Award Lecture on Cancer Epidemiology and Prevention. Cancer Res 1992;52(24):6735-6740 PubMed/NCBI
  9. Watanabe T, Tada M, Nagai H, Sasaki S, Nakao M. Helicobacter pylori infection induces gastric cancer in mongolian gerbils. Gastroenterology 1998;115(3):642-648 View Article PubMed/NCBI
  10. Parsonnet J, Friedman GD, Vandersteen DP, Chang Y, Vogelman JH, Orentreich N, et al. Helicobacter pylori infection and the risk of gastric carcinoma. N Engl J Med 1991;325(16):1127-1131 View Article PubMed/NCBI
  11. Plummer M, Franceschi S, Vignat J, Forman D, de Martel C. Global burden of gastric cancer attributable to Helicobacter pylori. Int J Cancer 2015;136(2):487-490 View Article PubMed/NCBI
  12. Yamamoto Y, Fujisaki J, Omae M, Hirasawa T, Igarashi M. Helicobacter pylori-negative gastric cancer: characteristics and endoscopic findings. Dig Endosc 2015;27(5):551-561 View Article PubMed/NCBI
  13. Leung WK, Lin SR, Ching JY, To KF, Ng EK, Chan FK, et al. Factors predicting progression of gastric intestinal metaplasia: results of a randomised trial on Helicobacter pylori eradication. Gut 2004;53(9):1244-1249 View Article PubMed/NCBI
  14. Li WQ, Zhang JY, Ma JL, Li ZX, Zhang L, Zhang Y, et al. Effects of Helicobacter pylori treatment and vitamin and garlic supplementation on gastric cancer incidence and mortality: follow-up of a randomized intervention trial. BMJ 2019;366:l5016 View Article PubMed/NCBI
  15. Yan L, Chen Y, Chen F, Tao T, Hu Z, Wang J, et al. Effect of Helicobacter pylori Eradication on Gastric Cancer Prevention: Updated Report From a Randomized Controlled Trial With 26.5 Years of Follow-up. Gastroenterology 2022;163(1):154-162.e3 View Article PubMed/NCBI
  16. Chiang TH, Chang WJ, Chen SL, Yen AM, Fann JC, Chiu SY, 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 View Article PubMed/NCBI
  17. Choi IJ, Kim CG, Lee JY, Kim YI, Kook MC, Park B, et al. Family History of Gastric Cancer and Helicobacter pylori Treatment. N Engl J Med 2020;382(5):427-436 View Article PubMed/NCBI
  18. Lee YC, Chen TH, Chiu HM, Shun CT, Chiang H, Liu TY, et al. The benefit of mass eradication of Helicobacter pylori infection: a community-based study of gastric cancer prevention. Gut 2013;62(5):676-682 View Article PubMed/NCBI
  19. Hwang YJ, Kim N, Lee HS, Lee JB, Choi YJ, Yoon H, et al. Reversibility of atrophic gastritis and intestinal metaplasia after Helicobacter pylori eradication - a prospective study for up to 10 years. Aliment Pharmacol Ther 2018;47(3):380-390 View Article PubMed/NCBI
  20. Malfertheiner P, Megraud F, Rokkas T, Gisbert JP, Liou JM, Schulz C, et al. Management of Helicobacter pylori infection: the Maastricht VI/Florence consensus report. Gut 2022;71:1724-1762 View Article PubMed/NCBI
  21. Ford AC, Yuan Y, Moayyedi P. Helicobacter pylori eradication therapy to prevent gastric cancer: systematic review and meta-analysis. Gut 2020;69(12):2113-2121 View Article PubMed/NCBI
  22. Chen HN, Wang Z, Li X, Zhou ZG. Helicobacter pylori eradication cannot reduce the risk of gastric cancer in patients with intestinal metaplasia and dysplasia: evidence from a meta-analysis. Gastric Cancer 2016;19(1):166-175 View Article PubMed/NCBI
  23. Sugano K. Effect of Helicobacter pylori eradication on the incidence of gastric cancer: a systematic review and meta-analysis. Gastric Cancer 2019;22(3):435-445 View Article PubMed/NCBI
  24. Ford AC, Forman D, Hunt RH, Yuan Y, Moayyedi P. Helicobacter pylori eradication therapy to prevent gastric cancer in healthy asymptomatic infected individuals: systematic review and meta-analysis of randomised controlled trials. BMJ 2014;348:g3174 View Article PubMed/NCBI
  25. Lee YC, Chiang TH, Chou CK, Tu YK, Liao WC, Wu MS, et al. Association Between Helicobacter pylori Eradication and Gastric Cancer Incidence: A Systematic Review and Meta-analysis. Gastroenterology 2016;150(5):1113-1124.e5 View Article PubMed/NCBI
  26. Doorakkers E, Lagergren J, Engstrand L, Brusselaers N. Eradication of Helicobacter pylori and Gastric Cancer: A Systematic Review and Meta-analysis of Cohort Studies. J Natl Cancer Inst 2016;108(9):djw132 View Article PubMed/NCBI
  27. Duan F, Song C, Zhang J, Wang P, Ye H, Dai L, et al. Evaluation of the Epidemiologic Efficacy of Eradicating Helicobacter pylori on Development of Gastric Cancer. Epidemiol Rev 2019;41(1):97-108 View Article PubMed/NCBI
  28. Liou JM, Malfertheiner P, Lee YC, Sheu BS, Sugano K, Cheng HC, et al. Screening and eradication of Helicobacter pylori for gastric cancer prevention: the Taipei global consensus. Gut 2020;69(12):2093-2112 View Article PubMed/NCBI
  29. Hooi JKY, Lai WY, Ng WK, Suen MMY, Underwood FE, Tanyingoh D, et al. Global Prevalence of Helicobacter pylori Infection: Systematic Review and Meta-Analysis. Gastroenterology 2017;153(2):420-429 View Article PubMed/NCBI
  30. Zamani M, Ebrahimtabar F, Zamani V, Miller WH, Alizadeh-Navaei R, Shokri-Shirvani J, et al. Systematic review with meta-analysis: the worldwide prevalence of Helicobacter pylori infection. Aliment Pharmacol Ther 2018;47(7):868-876 View Article PubMed/NCBI
  31. Wang Z, Han W, Xue F, Zhao Y, Wu P, Chen Y, et al. Nationwide gastric cancer prevention in China, 2021-2035: a decision analysis on effect, affordability and cost-effectiveness optimisation. Gut 2022;71(12):2391-2400 View Article PubMed/NCBI
  32. Li D, Jiang SF, Lei NY, Shah SC, Corley DA. Effect of Helicobacter pylori Eradication Therapy on the Incidence of Noncardia Gastric Adenocarcinoma in a Large Diverse Population in the United States. Gastroenterology 2023;165(2):391-401.e2 View Article PubMed/NCBI
  33. Lee YC, Lin JT, Wu HM, Liu TY, Yen MF, Chiu HM, et al. Cost-effectiveness analysis between primary and secondary preventive strategies for gastric cancer. Cancer Epidemiol Biomarkers Prev 2007;16(5):875-885 View Article PubMed/NCBI
  34. Cheng HC, Wang JD, Chen WY, Chen CW, Chang SC, Sheu BS. Helicobacter pylori test-and-treat program can be cost-effective to prevent gastric cancer in Taiwanese adults: referred to the nationwide reimbursement database. Helicobacter 2015;20(2):114-124 View Article PubMed/NCBI
  35. Pan KF, Zhang L, Gerhard M, Ma JL, Liu WD, Ulm K, et al. A large randomised controlled intervention trial to prevent gastric cancer by eradication of Helicobacter pylori in Linqu County, China: baseline results and factors affecting the eradication. Gut 2016;65(1):9-18 View Article PubMed/NCBI
  36. Wong BC, Zhang L, Ma JL, Pan KF, Li JY, Shen L, et al. Effects of selective COX-2 inhibitor and Helicobacter pylori eradication on precancerous gastric lesions. Gut 2012;61(6):812-818 View Article PubMed/NCBI
  37. Savoldi A, Carrara E, Graham DY, Conti M, Tacconelli E. Prevalence of Antibiotic Resistance in Helicobacter pylori: A Systematic Review and Meta-analysis in World Health Organization Regions. Gastroenterology 2018;155(5):1372-1382.e17 View Article PubMed/NCBI
  38. Jung YS, Kim EH, Park CH. Systematic review with meta-analysis: the efficacy of vonoprazan-based triple therapy on Helicobacter pylori eradication. Aliment Pharmacol Ther 2017;46(2):106-114 View Article PubMed/NCBI
  39. Graham DY, Liou JM. Primer for Development of Guidelines for Helicobacter pylori Therapy Using Antimicrobial Stewardship. Clin Gastroenterol Hepatol 2022;20(5):973-983.e1 View Article PubMed/NCBI
  40. Zhou L, Lu H, Song Z, Lyu B, Chen Y, Wang J, et al. 2022 Chinese national clinical practice guideline on Helicobacter pylori eradication treatment. Chin Med J (Engl) 2022;135(24):2899-2910 View Article PubMed/NCBI
  41. Pan J, Shi Z, Lin D, Yang N, Meng F, Lin L, et al. Is tailored therapy based on antibiotic susceptibility effective? a multicenter, open-label, randomized trial. Front Med 2020;14(1):43-50 View Article PubMed/NCBI
  42. Ji CR, Liu J, Li YY, Qiao C, Qu JY, Hu JN, et al. Susceptibility-guided quadruple therapy is not superior to medication history-guided therapy for the rescue treatment of Helicobacter pylori infection: A randomized controlled trial. J Dig Dis 2020;21(10):549-557 View Article PubMed/NCBI
  43. Dong F, Ji D, Huang R, Zhang F, Huang Y, Xiang P, et al. Multiple Genetic Analysis System-Based Antibiotic Susceptibility Testing in Helicobacter pylori and High Eradication Rate With Phenotypic Resistance-Guided Quadruple Therapy. Medicine (Baltimore) 2015;94(47):e2056 View Article PubMed/NCBI
  44. Lei WY, Lee JY, Chuang SL, Bair MJ, Chen CL, Wu JY, et al. Eradicating Helicobacter pylori via (13)C-urea breath screening to prevent gastric cancer in indigenous communities: a population-based study and development of a family index-case method. Gut 2023 View Article PubMed/NCBI
  45. Graham DY, Lew GM, Malaty HM, Evans DG, Evans DJ, Klein PD, et al. Factors influencing the eradication of Helicobacter pylori with triple therapy. Gastroenterology 1992;102(2):493-496 View Article PubMed/NCBI
  46. Xi S, Jing L, Lili W, Tingting L, Jun L, Ming W, et al. Magnetic controlled capsule endoscope (MCCE)’s diagnostic performance for H. pylori infection status based on the Kyoto classification of gastritis. BMC Gastroenterol 2022;22(1):502 View Article PubMed/NCBI
  47. O’Connor JP, Taneike I, O’Morain C. Improving compliance with helicobacter pylori eradication therapy: when and how?. Therap Adv Gastroenterol 2009;2(5):273-279 View Article PubMed/NCBI
  48. Nyssen OP, Perez-Aisa A, Tepes B, Castro-Fernandez M, Kupcinskas J, Jonaitis L, et al. Adverse Event Profile During the Treatment of Helicobacter pylori: A Real-World Experience of 22,000 Patients From the European Registry on H. pylori Management (Hp-EuReg). Am J Gastroenterol 2021;116(6):1220-1229 View Article PubMed/NCBI
  49. Liu WZ, Xie Y, Lu H, Cheng H, Zeng ZR, Zhou LY, et al. Fifth Chinese National Consensus Report on the management of Helicobacter pylori infection. Helicobacter 2018;23(2):e12475 View Article PubMed/NCBI
  50. Wu Y, Su T, Zhou X, Lu N, Li Z, Du Y. Awareness and attitudes regarding Helicobacter pylori infection in Chinese physicians and public population: A national cross-sectional survey. Helicobacter 2020;25(4):e12705 View Article PubMed/NCBI
  51. Malfertheiner P, Megraud F, O’Morain C, Bazzoli F, El-Omar E, Graham D, et al. Current concepts in the management of Helicobacter pylori infection: the Maastricht III Consensus Report. Gut 2007;56(6):772-781 View Article PubMed/NCBI
  52. Ding SZ, Du YQ, Lu H, Wang WH, Cheng H, Chen SY, et al. Chinese Consensus Report on Family-Based Helicobacter pylori Infection Control and Management (2021 Edition). Gut 2022;71(2):238-253 View Article PubMed/NCBI
  53. Malfertheiner P, Mégraud F, O’Morain C, Hungin AP, Jones R, Axon A, et al. Current concepts in the management of Helicobacter pylori infection—the Maastricht 2-2000 Consensus Report. Aliment Pharmacol Ther 2002;16(2):167-180 View Article PubMed/NCBI
  54. Liu XM, Ma XY, Liu F, Liu ZL, Tang XY, Ji MZ, et al. Gastric Cancer Screening Methods: A Comparative Study of the Chinese New Gastric Cancer Screening Score and Kyoto Classification of Gastritis. Gastroenterol Res Pract 2022;2022:7639968 View Article PubMed/NCBI
  55. Tsuda M, Asaka M, Kato M, Matsushima R, Fujimori K, Akino K, et al. Effect on Helicobacter pylori eradication therapy against gastric cancer in Japan. Helicobacter 2017;22(5):e12415 View Article PubMed/NCBI
  56. National Bureau of Statistics of China. China (NBoSo). China Statistical Yearbook 2021. Beijing: China Statistical Press; 2022
  57. Marshall B. Epidemiology of Helicobacter in Chinese families: a foundation for cost-effective eradication strategies?. Gut 2023 View Article PubMed/NCBI
  58. Usui Y, Taniyama Y, Endo M, Koyanagi YN, Kasugai Y, Oze I, et al. Helicobacter pylori, Homologous-Recombination Genes, and Gastric Cancer. N Engl J Med 2023;388(13):1181-1190 View Article PubMed/NCBI
  59. Zhou XZ, Lyu NH, Zhu HY, Cai QC, Kong XY, Xie P, et al. Large-scale, national, family-based epidemiological study on Helicobacter pylori infection in China: the time to change practice for related disease prevention. Gut 2023;72(5):855-869 View Article PubMed/NCBI
  60. Drumm B, Perez-Perez GI, Blaser MJ, Sherman PM. Intrafamilial clustering of Helicobacter pylori infection. N Engl J Med 1990;322(6):359-363 View Article PubMed/NCBI
  61. Dominici P, Bellentani S, Di Biase AR, Saccoccio G, Le Rose A, Masutti F, et al. Familial clustering of Helicobacter pylori infection: population based study. BMJ 1999;319(7209):537-540 View Article PubMed/NCBI
  62. Zhao JB, Yuan L, Yu XC, Shao QQ, Ma J, Yu M, et al. Whole family-based Helicobacter pylori eradication is a superior strategy to single-infected patient treatment approach: A systematic review and meta-analysis. Helicobacter 2021;26(3):e12793 View Article PubMed/NCBI
  63. Ma J, Yu M, Shao QQ, Yu XC, Zhang C, Zhao JB, et al. Both family-based Helicobacter pylori infection control and management strategy and screen-and-treat strategy are cost-effective for gastric cancer prevention. Helicobacter 2022;27(4):e12911 View Article PubMed/NCBI
  64. Zhang J, Deng Y, Liu C, Wang H, Ren H, Chen S, et al. ‘Family-based’ strategy for Helicobacter pylori infection screening: an efficient alternative to ‘test and treat’ strategy. Gut 2023 View Article PubMed/NCBI
  65. Ikeda F, Shikata K, Hata J, Fukuhara M, Hirakawa Y, Ohara T, et al. Combination of Helicobacter pylori Antibody and Serum Pepsinogen as a Good Predictive Tool of Gastric Cancer Incidence: 20-Year Prospective Data From the Hisayama Study. J Epidemiol 2016;26(12):629-636 View Article PubMed/NCBI
  66. Taninaga J, Nishiyama Y, Fujibayashi K, Gunji T, Sasabe N, Iijima K, et al. Prediction of future gastric cancer risk using a machine learning algorithm and comprehensive medical check-up data: A case-control study. Sci Rep 2019;9(1):12384 View Article PubMed/NCBI
  67. Charvat H, Sasazuki S, Inoue M, Iwasaki M, Sawada N, Shimazu T, et al. Prediction of the 10-year probability of gastric cancer occurrence in the Japanese population: the JPHC study cohort II. Int J Cancer 2016;138(2):320-331 View Article PubMed/NCBI
  68. Murphy JD, Olshan AF, Lin FC, Troester MA, Nichols HB, Butt J, et al. A Predictive Model of Noncardia Gastric Adenocarcinoma Risk Using Antibody Response to Helicobacter pylori Proteins and Pepsinogen. Cancer Epidemiol Biomarkers Prev 2022;31(4):811-820 View Article PubMed/NCBI
  69. Ishikura N, Ito H, Oze I, Koyanagi YN, Kasugai Y, Taniyama Y, et al. Risk Prediction for Gastric Cancer Using GWAS-Identifie Polymorphisms, Helicobacter pylori Infection and Lifestyle-Related Risk Factors in a Japanese Population. Cancers (Basel) 2021;13(21):5525 View Article PubMed/NCBI
  70. Song M, Camargo MC, Weinstein SJ, Murphy G, Freedman ND, Koshiol J, et al. Serum pepsinogen 1 and anti-Helicobacter pylori IgG antibodies as predictors of gastric cancer risk in Finnish males. Aliment Pharmacol Ther 2018;47(4):494-503 View Article PubMed/NCBI
  71. Lee TY, Wang CB, Chen TT, Kuo KN, Wu MS, Lin JT, et al. A tool to predict risk for gastric cancer in patients with peptic ulcer disease on the basis of a nationwide cohort. Clin Gastroenterol Hepatol 2015;13(2):287-293.e1 View Article PubMed/NCBI
  72. Tu H, Sun L, Dong X, Gong Y, Xu Q, Jing J, et al. A Serological Biopsy Using Five Stomach-Specific Circulating Biomarkers for Gastric Cancer Risk Assessment: A Multi-Phase Study. Am J Gastroenterol 2017;112(5):704-715 View Article PubMed/NCBI
  73. Iida M, Ikeda F, Hata J, Hirakawa Y, Ohara T, Mukai N, et al. Development and validation of a risk assessment tool for gastric cancer in a general Japanese population. Gastric Cancer 2018;21(3):383-390 View Article PubMed/NCBI
  74. So JBY, Kapoor R, Zhu F, Koh C, Zhou L, Zou R, et al. Development and validation of a serum microRNA biomarker panel for detecting gastric cancer in a high-risk population. Gut 2021;70(5):829-837 View Article PubMed/NCBI
  75. Cai Q, Zhu C, Yuan Y, Feng Q, Feng Y, Hao Y, et al. Development and validation of a prediction rule for estimating gastric cancer risk in the Chinese high-risk population: a nationwide multicentre study. Gut 2019;68(9):1576-1587 View Article PubMed/NCBI
  76. Tao W, Wang HX, Guo YF, Yang L, Li P. Establish a Scoring Model for High-Risk Population of Gastric Cancer and Study on the Pattern of Opportunistic Screening. Gastroenterol Res Pract 2020;2020:5609623 View Article PubMed/NCBI
  77. Park CH, Kim EH, Jung DH, Chung H, Park JC, Shin SK, et al. The new modified ABCD method for gastric neoplasm screening. Gastric Cancer 2016;19(1):128-135 View Article PubMed/NCBI
  78. Liu MM, Wen L, Liu YJ, Cai Q, Li LT, Cai YM. Application of data mining methods to improve screening for the risk of early gastric cancer. BMC Med Inform Decis Mak 2018;18(Suppl 5):121 View Article PubMed/NCBI
  79. Ji L, Liu Z, Zhou B, Cai Y, An F, Wang L, et al. Community-Based Pilot Study of a Screening Program for Gastric Cancer in a Chinese Population. Cancer Prev Res (Phila) 2020;13(1):73-82 View Article PubMed/NCBI
  80. Lin JT, Lee WC, Wu MS, Wang JT, Wang TH, Chen CJ. Diagnosis of gastric adenocarcinoma using a scoring system: combined assay of serological markers of Helicobacter pylori infection, pepsinogen I and gastrin. J Gastroenterol 1995;30(2):156-161 View Article PubMed/NCBI
  81. Kaise M, Miwa J, Tashiro J, Ohmoto Y, Morimoto S, Kato M, et al. The combination of serum trefoil factor 3 and pepsinogen testing is a valid non-endoscopic biomarker for predicting the presence of gastric cancer: a new marker for gastric cancer risk. J Gastroenterol 2011;46(6):736-745 View Article PubMed/NCBI
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  • Cancer Screening and Prevention
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  • eISSN 2835-3315

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Prevention and Screening of Gastric Cancer by Helicobacter pylori Management: Synthesis of Existing Data

Xianzhu Zhou, Zhaoshen Li, Yiqi Du
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