Abstract
Background
There is a lack of data on the effects of family-based Helicobacter pylori (H. pylori) infection control and management (FBCM) strategies in Southwest China. This study aimed to evaluate the two-year outcomes of these strategies in affected households.
Methods
Individuals who participated in a two-year H. pylori survey in Chongqing (China) were included in the study. Households where all H. pylori-infected members underwent eradication treatment were classified as group A, while those that did not follow whole family eradication therapy were designated as group B. The eradication rate, incidence of new infections, and changes in hygiene and living habits, were compared between the two groups.
Results
This study included 472 cases from 171 families, including 296 in group A and 176 in group B. The eradication rate in group A was significantly higher than that in group B (89.39% vs. 70.45%, p = 0.003). The compliance (87.88% vs. 84.09%, p = 0.519) and timely reexamination rates (46.97% vs. 31.82%, p = 0.063) were similar between the two groups. Among H. pylori-infected cases, the endoscopy uptake rate in group A was significantly higher than that in group B (30.30% vs. 13.98%, p = 0.004). Group A exhibited significant hygiene improvements after 2 years, including reduced raw water drinking (5.74% vs. 2.36%, p = 0.037), decreased shared cup usage (27.70% vs. 9.46%, p < 0.001), and increased individual dining (6.08% vs. 16.22%, p < 0.001). Group B showed decreased shared plate usage (26.14% vs. 5.11%, p < 0.001) and increased plate disinfection rates (25.00% vs. 44.89%, p < 0.001).
Conclusion
The FBCM strategy significantly improved H. pylori eradication rates and promoted healthier hygiene behaviors.
Keywords: Helicobacter pylori, Family-based infection control and management, Epidemiology
Introduction
Helicobacter pylori (H. pylori) is a major causative factor for gastric cancer (GC) and other gastroduodenal diseases. In China, approximately 78.5% of non-cardia GC cases and 62.1% of cardia GC cases were attributed to H. pylori infection [1, 2]. H. pylori eradication therapy can effectively reduce GC incidence and mortality at the population level [3, 4]. Therefore, screening and eradication of H. pylori infection have been recommended as the most practical approaches to the prevention of GC [2, 4–6].
With the improvement of hygienic conditions, economic development, and the widespread application of eradication therapies, there is a trend that the H. pylori prevalence rate has been reduced worldwide [7–9]. The crude prevalence of H. pylori in adults has decreased from 52.6% before 1990 to 43.9% after 2015 [9]. During this period, the incidence of GC declined significantly, and this trend is expected to continue through 2030 [7, 10, 11]. However, the overall burden of GC has not remarkably decreased [12]. Additionally, antibiotic resistance poses a significant challenge in managing H. pylori, particularly in China [13]. Ongoing efforts are therefore essential to eliminate the risks associated with H. pylori infection.
The H. pylori is primarily transmitted through the oral-oral and fecal-oral routes [3]. There is a possibility that viable organisms in gastric fluid may enter the mouth during episodes of reflux or vomiting, particularly when the load of H. pylori in the stomach are elevated [14–16]. Additionally, these bacteria may also be excreted through feces [17]. In cases infected with H. pylori who exhibit poor hygiene practices, such as infrequent handwashing after defecation, consuming tap water, or sharing tableware with family members, the risk of person-to-person transmission significantly increases [18–21]. Consequently, H. pylori is easily transmitted between parents and children who share meals and have close contact, as well as among siblings [22–26], exhibiting an epidemiological feature of familial clustering [27]. As a result, guidelines recommend a comprehensive household-based approach for H. pylori management, including screening, identification, treatment, health education, and follow-up for all family members [5, 28, 29]. This approach can improve the eradication rate and potentially reduce the risk of reinfection [30, 31]. A 2021 survey in Chongqing, the largest city in Southwest China, found that about 70.11% of families had at least one member infected with H. pylori, with exposure to infected family members identified as a major source of transmission [20]. However, real-world data on household H. pylori infection rates and treatment outcomes in Chongqing remain limited.
This study examined the influence of a family-based approach on H. pylori infection rates over a two-year period. Additionally, changes in hygiene practices following physician-led education were assessed. The findings could provide valuable insights into the management of H. pylori in Southwest China.
Methods
Participants’ selection
This study conducted a retrospective analysis of Chongqing households that participated in two family-based H. pylori screenings between 2021 and 2023. In the national family-based epidemiological study on H. pylori infection in 2021, 22 hospitals in Chongqing city participated as participating institutions [20]. The investigation utilized a nonprobability (convenience) sampling method from each region, while also referring to the probability sampling for sample size calculation. Based on this calculation, a sample size of 9317 was determined to produce a two-sided 95% confidence interval with a width of 0.020, assuming an infection rate of 40% (formula: n = t2pq/d2; n, t, p, q and d are sample size, t value, positive rate, negative rate and acceptable error, respectively). To address the additional bias associated with the convenience sampling method, the total sample size increased to over 10,000 households [20]. The number of samples selected from each region was determined by regional population, as well as practical considerations, such as the cost, accessibility, testing facilities and COVID-19 factors. In Chongqing city, the initial survey included 522 households (1,659 individuals) from various regions as valid samples. Recruitment was conducted through public posters and online information (detailed inclusion criteria are provided below). Participating institutions enrolled households at outpatient clinics and in community settings. All participating was voluntarily, and no specific incentives were provided. Two to four doctors from each participating institution were trained in survey methodology and guided household members on-site to complete the questionnaire and undergo the 13C-UBT. The first round of household screening occurred from September to December 2021, while the second round took place between 2023 to February 2024. All participants from the enrolled households completed the questionnaires, signed informed consent forms, and underwent the 13C-UBT to assess the current infection status. The inclusion criteria were as follows: (1) participation in the initial and present infection survey conducted at two-year intervals, (2) signing the informed consent form, and (3) completion of the questionnaire and 13C-UBT to determine H. pylori infection status.
The exclusion criteria were as follows: (1) inability to perform the 13C-UBT, (2) loss of contact, (3) H. pylori treatment within three months of the initial survey, and (4) absence of H. pylori infection within the family during the first survey. Researchers reviewed medical records and excluded 940 participants based on these criteria. A total of 472 participants from 171 households were ultimately included in the study (Fig. 1). As H. pylori gastritis is an infectious disease, it is recommended that all individuals with the infection, who are able to tolerate the H. pylori eradication therapy, undergo treatment for a cure. Households in which all H. pylori-infected members underwent eradication treatment were classified as group A, while other H. pylori-infected households were classified as group B. The study was approved by the Ethics Committee of the Army Specialty Medical Centre Hospital (Medical Research and Luncheon Review 2023 No. 248), and it was registered in the China Clinical Research Centre (https://www.chictr.org.cn/; Registration No. ChiCTR2300078244; Registration Date 2023-12-01).
Fig. 1.
Flowchart of retrospective cohort study process
Study design
Participants’ baseline characteristics were collected through a questionnaire, covering infection status, household economic and housing conditions (total household income, place of residence, total household area, animal ownership), family hygiene and living habits (source of drinking water, dish disinfection), general family member information (marital status, education level, occupation), personal hygiene and lifestyle habits (drinking tap water, handwashing before and after meals, frequency of dining out), and medical history (gastrointestinal symptoms over the past year, gastroscopy records from the last five years).
According to Chinese Consensus Report on Family-Based Helicobacter pylori Infection Control and Management (2021 Edition) [29], the family-based H. pylori management approach consists of three key components. Firstly, infected adults and children with digestive tract diseases within a household were advised to undergo treatment. Secondly, families were provided with medical and lifestyle guidance during the initial screening, which included both verbal and written instructions on medication side effects, as well as proper hygiene and lifestyle habits. Based on the Fifth Chinese National Consensus Report on the Management of Helicobacter pylori Infection and local antibiotic resistance data, a bismuth-containing quadruple regimen was recommended as the primary empirical therapy for H. pylori eradication [32, 33]. The standard regimen consisted of amoxicillin (1000 mg, BID) and furazolidone (100 mg, BID), to be taken 30 min after meals, along with esomeprazole (20 mg, BID) and bismuth potassium citrate (220 mg, BID), to be taken 30 min before meals, for a duration of 14 days. For patients allergic to amoxicillin, an alternative regimen of tetracycline (500 mg, TID) and furazolidone (100 mg, BID), combined with esomeprazole and bismuth potassium citrate, was recommended. The choice of treatment plan also depends on the availability of local drugs and the patient’s drug allergy. The composition of treatment regimens may vary across regions or populations, potentially introducing bias into statistical analyses. In cases where multiple household members were infected, simultaneous treatment for all affected individuals was encouraged. After 4–6 weeks of treatment [13],C-UBT tests was performed to evaluate the success of eradication. Additionally, families were instructed to implement preventive hygiene measures, such as washing hands before and after meals, using separate chopsticks and serving spoons, sterilizing cutlery, and avoiding the sharing of dental instruments and drinking cups.
In the two family-based surveys, the following data were recorded: (1) current H. pylori infection status; (2) eradication treatment history and medication adherence (defined as ingestion of > 80% of the prescribed tablets); and (3) changes in hygiene behaviors.
13C-UREA breath test
H. pylori infection status was assessed using a 13C-UBT Kit (13 C urea breath test Heliforce Kit, Beijing Richen-Force Science & Technology, Beijing, China) according to the manufacturer’s instructions. Participants were instructed to fast for at least two hours before testing. A baseline breath sample was collected before ingestion of the urea capsule, followed by a second breath sample 30 min afterward. A delta over baseline (DOB) of ≥ 4.0 was considered as a positive result for H. pylori, and a DOB < 4.0 was considered negative.
Statistical methods
Data were analyzed using Microsoft Excel 2020 (Microsoft Corp., Redmond, WA, USA) and SPSS 26.0 (IBM Corp., Armonk, NY, USA) software. Continuous variables were presented as mean ± standard deviation, and categorical variables were expressed as percentages. Continuous categorical variables were compared using the Wilcoxon rank-sum test or the Kruskal-Wallis H test. Categorical variables were compared using the Chi-square test or Fisher’s exact test where appropriate. Statistical significance was set at p < 0.05.
Results
Participants’ baseline characteristics
This study included 472 cases from 171 families infected with H. pylori, with 296 cases from group A (98 families) and 176 cases from group B (73 families). The average ages in group A and group B were 43.34 ± 18.30 and 44.52 ± 18.21 years, respectively. The H. pylori infection rates in group A and group B were 44.59% and 52.84% (p = 0.083), respectively. Table 1 summarizes the information obtained through the case report form. No significant differences were found between the two groups in any measured variables, except for a higher proportion of cases from rural areas in group B. Among all individuals included in the study, the infection rate of H. pylori was lower in children and adolescents (30.77% vs. 49.76%, p = 0.010), unmarried individuals (36.59% vs. 50.00%, p = 0.027), and those who had dined individually (23.63% vs. 50.12%, p = 0.002), while the infection rate of H. pylori was higher in individuals who frequently drank tap water (65.63% vs. 46.36%, p = 0.035) (Table 2).
Table 1.
Demographic characteristics in group A and group B in the initial survey
| Total (n = 472) |
Group A (n = 296) |
Group B (n = 176) |
χ2 | p-value | |
|---|---|---|---|---|---|
| Result of 13 C-UBT | |||||
| Positive | 225 (47.67%) | 132 (44.59%) | 93 (52.84%) | 3.009 | 0.083 |
| Negative | 247 (52.33%) | 164 (55.41%) | 83 (47.16%) | ||
| Sex | |||||
| Men | 178 (37.71%) | 115 (38.85%) | 63 (35.80%) | 0.439 | 0.508 |
| Women | 294 (62.29%) | 181 (61.15%) | 113 (64.20%) | ||
| Marital status | |||||
| Single | 82 (17.37%) | 55 (18.58%) | 27 (15.34%) | 0.807 | 0.369 |
| Married | 390 (82.63%) | 241 (81.42%) | 149 (84.66%) | ||
| Educational level | |||||
| High school and below | 247 (52.33%) | 147 (49.66%) | 100 (56.82%) | 2.266 | 0.132 |
| College and above | 225 (47.67%) | 149 (50.34%) | 76 (43.18%) | ||
| Occupation | |||||
| Worker | 66 (13.98%) | 44 (14.86%) | 22 (12.50%) | 9.800 | 0.200 |
| Farmer | 31 (6.575) | 18 (6.08%) | 13 (7.39%) | ||
| Educator | 18 (3.81%) | 13 (4.39%) | 5 (2.84%) | ||
| Investigator | 18 (3.81%) | 16 (5.41%) | 2 (1.14%) | ||
| Medical personnel | 117 (24.79%) | 66 (22.30%) | 51 (28.98%) | ||
| Student | 57 (12.08%) | 38 (12.84%) | 19 (10.80%) | ||
| Self-employment | 43 (9.11%) | 25 (8.45%) | 18 (10.23%) | ||
| Others | 119 (25.21%) | 76 (25.68%) | 40 (22.73%) | ||
| Current gastrointestinal symptoms | |||||
| Yes | 149 (31.57%) | 97 (32.77%) | 52 (29.55%) | 0.531 | 0.466 |
| No | 323 (68.43%) | 199 (67.23%) | 124 (70.45%) | ||
| Drinking tap water | |||||
| No | 440 (93.22%) | 279 (94.26%) | 161 (91.48%) | 1.854 | 0.173 |
| Yes | 32 (6.78%) | 17 (5.74%) | 15 (8.52%) | ||
| Washing hands before meal and after defecation | |||||
| Yes | 429 (90.89%) | 267 (90.20%) | 162 (92.05%) | 0.453 | 0.501 |
| No | 43 (9.11%) | 29 (9.80%) | 14 (7.95%) | ||
| Age | |||||
| Children and adolescents (< 18 years) | 52 (11.02%) | 31 (10.47%) | 21 (11.93%) | 0.240 | 0.624 |
| Adult (≥ 18 years) | 420 (88.98%) | 265 (89.53%) | 155 (88.07%) | ||
| Rarely dining out home | |||||
| Yes | 319 (67.58%) | 194 (65.54%) | 125 (71.02%) | 1.514 | 0.219 |
| No | 153 (32.42%) | 102 (34.46%) | 51 (28.98%) | ||
| Annual household income (dollar) | |||||
| < 14,260 | 161 (34.11%) | 97 (32.77%) | 64 (36.36%) | 0.653 | 0.721 |
| 14,260–42,780 | 257 (54.45%) | 164 (55.41%) | 93 (52.84%) | ||
| > 42,780 | 54 (11.44%) | 35 (11.82%) | 19 (10.80%) | ||
| Resident location | |||||
| City | 423 (89.62%) | 273 (92.23%) | 150 (85.23%) | 5.817 | 0.016 |
| Rural | 49 (6.14%) | 23 (7.77%) | 26 (14.77%) | ||
| Household living area (m2) | |||||
| < 60 | 36 (7.63%) | 22 (7.43%) | 13 (7.39%) | 0.301 | 0.860 |
| 60–120 | 296 (62.71%) | 183 (61.82%) | 113 (64.20%) | ||
| > 120 | 141 (29.87%) | 91 (30.74%) | 50 (28.41%) | ||
| Tableware sterilization | |||||
| Yes | 116 (24.58%) | 72 (24.32%) | 44 (25.00%) | 0.024 | 0.869 |
| No | 356 (75.42%) | 224 (75.68%) | 132 (75.00%) | ||
| Individual dining | |||||
| Yes | 49 (10.38%) | 18 (6.08%) | 17 (9.66%) | 2.058 | 0.151 |
| No | 423 (89.62%) | 278 (93.92%) | 159 (90.34%) | ||
| Water cup sharing | |||||
| Yes | 128 (27.12%) | 82 (27.70%) | 46 (26.14%) | 0.137 | 0.711 |
| No | 344 (72.88%) | 214(72.30%) | 130(73.86%) | ||
Table 2.
Demographic characteristics and H. pylori infection status in 472 participants in the initial survey
| Total (n = 472) |
H.pylori infection (n = 225) |
Infection rate(%) | χ2 | p-value | |
|---|---|---|---|---|---|
| Sex | |||||
| Men | 178 | 89 | 50.00% | 0.622 | 0.430 |
| Women | 294 | 136 | 46.26% | ||
| Marital status | |||||
| Single | 82 | 30 | 36.59% | 4.888 | 0.027 |
| Married | 390 | 195 | 50.00% | ||
| Educational level | |||||
| High school and below | 247 | 118 | 47.77% | 0.002 | 0.962 |
| College and above | 225 | 107 | 47.56% | ||
| Occupation | |||||
| Worker | 66 | 33 | 50.00% | 13.865 | 0.054 |
| Farmer | 31 | 14 | 45.16% | ||
| Educator | 18 | 9 | 50.00% | ||
| Investigator | 18 | 10 | 55.56% | ||
| Medical personnel | 117 | 53 | 45.30% | ||
| Student | 57 | 16 | 28.07% | ||
| Self-employment | 43 | 23 | 53.49% | ||
| Others | 119 | 67 | 56.30% | ||
| Current gastrointestinal symptoms | |||||
| Yes | 149 | 67 | 44.97% | 0.638 | 0.425 |
| No | 323 | 158 | 48.92% | ||
| Drinking tap water | |||||
| Yes | 32 | 21 | 65.63% | 4.436 | 0.035 |
| No | 440 | 204 | 46.36% | ||
| Washing hands before meal and after defecation | |||||
| Yes | 429 | 203 | 47.32% | 0.231 | 0.630 |
| No | 43 | 22 | 51.16% | ||
| Age | |||||
| Children and adolescents (< 18 years) | 52 | 16 | 30.77% | 6.691 | 0.010 |
| Adult (≥ 18 years) | 420 | 209 | 49.76% | ||
| Rarely dining out home | |||||
| Yes | 319 | 150 | 47.02% | 0.165 | 0.684 |
| No | 153 | 75 | 49.02% | ||
| Annual household income (dollar) | |||||
| < 14,260 | 161 | 87 | 50.04% | 4.801 | 0.091 |
| 14,260–42,780 | 257 | 111 | 43.19% | ||
| > 42,780 | 54 | 27 | 50.00% | ||
| Resident location | |||||
| City | 423 | 198 | 46.81% | 1.211 | 0.271 |
| Rural | 49 | 27 | 55.10% | ||
| Household living area (m2) | |||||
| < 60 | 36 | 16 | 44.44% | 3.139 | 0.208 |
| 60–120 | 296 | 150 | 50.68% | ||
| > 120 | 141 | 59 | 41.84% | ||
| Tableware sterilization | |||||
| Yes | 116 | 56 | 48.28% | 0.023 | 0.880 |
| No | 356 | 169 | 47.47% | ||
| Individual dining | |||||
| Yes | 49 | 13 | 26.53% | 9.794 | 0.002 |
| No | 423 | 212 | 50.12% | ||
| Water cup sharing | |||||
| Yes | 128 | 63 | 49.22% | 0.169 | 0.681 |
| No | 344 | 162 | 47.09% | ||
H. pylori eradication outcomes
In group A, all 132 patients received eradication treatment, and 118 (89.39%) of them were successfully eradicated. In group B, among the 93 infected patients, 44 of them received eradication treatment, of whom 31 (70.45%) were successfully eradicated. The eradication rate in group A was significantly higher than that in group B (89.39% vs. 70.45%, p = 0.003).
Medication adherence rates (116/132) (37/44) (87.88% vs. 84.09%, p = 0.519) and timely reexamination compliance rates (62/132) (14/44) (46.97% vs. 31.82%, p = 0.063) did not differ significantly between the two groups. However, the endoscopic uptake rate among infected cases was significantly higher in group A than that in group B (30.30% vs. 13.98%, p = 0.004) (Fig. 2).
Fig. 2.
The results of H. pylori eradication treatment and compliance with medical recommendations. a The success rate of eradication of infected cases in two groups. b Medication compliance of infected cases during treatment in two groups. c The proportion of infected cases who underwent gastroscopy examination in two groups. ** p < 0.01
Gastroscopy identified 9 cases of chronic atrophic gastritis, 5 cases of active gastritis, 6 cases of peptic ulcers, and 20 cases of chronic non-atrophic gastritis in group A. In group B, there were 3 cases of chronic atrophic gastritis, 3 cases of active gastritis, 1 case of peptic ulcer, and 7 cases of chronic non-atrophic gastritis.
Changes in hygiene behaviors
Compared with the baseline, the proportion of cases in group A who drank tap water (17/296 to 7/296) and shared water cups (82/296 to 28/296) significantly decreased. The use of individual plates increased from 6.08% (18/296) to 16.22% (48/296) (p < 0.05). In group B, the proportion of cases who shared water cups also declined. Additionally, the proportion of cases who disinfected their crockery increased from 25.00% (44/176) to 44.89% (79/176) (p < 0.001) (Fig. 3).
Fig. 3.
Changes in participants’ hygiene practices at the time of initial survey and 2 years later. a The changes of group A. b The changes of group B. * p < 0.05; **** p < 0.001
Incidence rate of H. pylori infection during the two-year
Among cases who tested negative for H. pylori at baseline(n = 247), 12.20% (20/164) in group A and 12.05% (10/83) in group B acquired the infection during the two years (p = 0.973). The annual incidence rates of H. pylori infection were 6.10% in group A and 6.02% in group B. From a hygiene perspective, individuals who did not wash their hands before meal and after defecation in current survey had a significantly higher rate of turning to H. pylori-positive than others (Table 3).
Table 3.
The rate of new H. pylori infection during two years and the current hygiene habits for the included individuals
| H. pylori-negative in initial survey (n = 247) |
new infection cases during two years (n = 30) |
rate(%) | χ2 | p-value | |
|---|---|---|---|---|---|
| All H. pylori-infected members in family accepted eradication treatment | |||||
| Yes | 164 | 20 | 12.20% | 0.001 | 0.973 |
| No | 83 | 10 | 12.05% | ||
| Drinking tap water | |||||
| Yes | 8 | 2 | 25.00% | 1.280 | 0.258 |
| No | 239 | 28 | 11.72% | ||
| Washing hands before meal and after defecation | |||||
| Yes | 229 | 24 | 10.48% | 8.168 | 0.004 |
| No | 18 | 6 | 33.33% | ||
| Tableware sterilization | |||||
| Yes | 76 | 9 | 11.84% | 0.009 | 0.922 |
| No | 171 | 21 | 12.28% | ||
| Individual dining | |||||
| Yes | 33 | 9 | 12.12% | 0.000 | 0.996 |
| No | 214 | 26 | 12.15% | ||
| Water cup sharing | |||||
| Yes | 19 | 4 | 21.05% | 2.114 | 0.146 |
| No | 228 | 26 | 11.40% | ||
Discussion
This two-year retrospective cohort study demonstrated that H. pylori eradication was significantly more successful in cases who underwent family-based treatment (group A) compared with those who did not (group B) (89.39% vs. 70.45%, p = 0.003). Medication adherence rates were comparable between the two groups (87.88% vs. 84.09%, p > 0.05). Notably, participants in the family-based treatment group had significantly higher gastroscopy uptake rates (30.30% vs. 13.98%, p = 0.004). These findings suggest that a family-based H. pylori control and management strategy improves eradication rates, enhances compliance, increases the likelihood of undergoing gastroscopy, and promotes better hygiene practices.
This study highlights the benefits of a family-centered approach in improving H. pylori eradication rates. In developing countries, enhancing compliance with medication regimens is crucial for increasing treatment success [34]. Previous studies have primarily focused on individual-based interventions, such as telephone follow-ups, social media engagement, text messaging, and patient education, to improve disease awareness, side effect tolerance, and ultimately, adherence to treatment [34–36]. However, the impact of improving compliance at the household level remains underexplored. A recent follow-up study by Li et al. reported that family-based H. pylori management achieved a 93.5% (129/138) eradication rate, along with better drug adherence and reexamination compliance [37]. Family members of infected cases represent a high-risk group and are more likely to engage in prevention and control efforts [38]. Coordinated treatment within a household can enhance medication adherence by reducing the likelihood of missed or incorrect doses, thereby improving eradication rates. Additionally, involving family members fosters better hygiene practices, such as avoiding the sharing of utensils, water bottles, and dental items, thereby reducing intra-household H. pylori transmission [29].
Among various GC screening methods, endoscopic examination remains the most effective for early detection. Increasing endoscopic uptake rates is a key strategy for reducing the burden of GC. In China, where gastroscopy is relatively affordable and accessible, this study encouraged H. pylori-positive cases to undergo endoscopic screening. A survey conducted in Hunan Province (China) revealed that while 83.8% of adults recognized the benefits of GC screening, only 15.2% had undergone gastroscopy [38]. In this study, gastroscopy uptake rate was significantly higher in the family-based treatment group, indicating that a household-centered approach may be an effective strategy for improving screening rates.
From an economic standpoint, a family-based H. pylori infection control and management strategy is cost-effective [31, 39]. Whole-family screening and eradication can improve eradication rates, with its most significant benefit being the protection of uninfected family members. Non-infected cases in households with H. pylori-infected members face an increased risk of infection (adjusted OR: 1.98, 95% CI: 1.03–3.80) [40]. A Markov state-transition model developed by Zhang et al. assessed different H. pylori infection control strategies across 494 million households in China and found that a family-based approach significantly reduced the financial burden. Compared with a no-screening strategy, this approach saved $1,467 million, added 227 million quality-adjusted life years, and increased total life years by 59 million [39]. These findings suggest that a family-based H. pylori control strategy presents an effective balance between cost and efficiency in China.
However, the real-world implementation of family-based H. pylori control does not always achieve the ideal outcomes predicted by data models. In this study, more than one-third of households did not complete eradication treatment for all infected cases. Another family-based follow-up survey of 386 households in Shandong Province, China, which showed that only 39.3% of infected individuals received H. pylori eradication treatment during the 6-month follow-up period, indicated the fact that further studies focusing on pre-screening education are warranted to improve compliance to post-screening recommendation [41]. Apart from pediatric patients and adults with antibiotic resistance, the majority of untreated adults failed to recognize the risks of H. pylori infection and transmission. In a nationwide online survey conducted in China, only 35% of respondents correctly understood the health risks associated with H. pylori, and only 43.6% were aware of appropriate preventive measures [42]. Similarly, awareness of H. pylori infection remains suboptimal in the United States. A survey conducted by the University of Arizona revealed that only 52.3% of respondents had prior knowledge of H. pylori [43]. These findings underscore the need for greater public education on the risks and prevention of H. pylori infection.
Both national and Chinese H. pylori guidelines emphasize the importance of public health education [2, 29, 32]. A family-based control and management strategy serves as a valuable approach to promoting public awareness and improving hygiene practices. Li et al. reported that, following the implementation of a family-based strategy, 77% of respondents gained varying degrees of knowledge about H. pylori, and 39.1% (213/545) of cases with poor hygiene habits showed improvements after screening and education [37]. In the present study, the hygienic habits of individuals improved during two years. Group A exhibited a significant increase in the proportion of individual dining (from 6.08% to 16.22%), alongside significant decreases in the proportion of sharing water cups (from 67.70% to 9.46%) and drinking tap water (from 5.74% to 2.36%). Conversely, group B demonstrated a significant increase in the proportion of tableware sterilization (from 25.00% to 44.89%), accompanied by a significant decrease in the proportion of sharing water cups (from 26.14% to 5.11%). These findings suggest that family-based H. pylori management contributes to significant improvements in hygiene practices. Beyond education, ensuring adherence to family-based eradication strategies and other medical recommendations remains a challenge that warrants further investigation in clinical practice.
Although the global H. pylori infection rate is declining, China continues to face substantial challenges in prevention and control due to its large infected population. In this study, 12.20% of initially H. pylori-negative cases in group A and 12.05% in group B became infected within two years. An epidemiological study in China showed that the family-based prevalence of H. pylori in Lanzhou city decreased from 76.9% (147/191) in 2021 to 67.1% (116/173) in 2023, nevertheless, 38.6% of households reported newly infected members during the follow-up period [44]. Compared to the incidence rates of less than 1% reported in developed countries such as Ireland, these figures remain high [45], highlighting the urgent need to strengthen H. pylori prevention and control measures in China. Among individuals who were H. pylori negative in the initial survey, those who did not wash hands before meal and after defecation recently exhibited a significantly higher rate of getting infected compared with who practiced hand hygiene (33.33% vs. 10.48%, p = 0.004). While individuals who shared water cup with family members (20.15% vs. 11.40%, p = 0.146) or drank tap water (25.00% vs. 11.72%, p = 0.258) also showed a marginally elevated ratio of new infections. This finding further supports the hypothesis that poor hygiene practices are associated with an increased risk of H. pylori transmission. Therefore, alongside eradication therapy, it is crucial to emphasize the significance of improving hygienic practices in households to effectively prevent new H. pylori infections.
Study limitations
This study has several limitations. Firstly, as a retrospective cohort study based on questionnaires filled by participants subjectively with a relatively small number of households included, potential selection bias might have influenced the findings. Secondly, strain culture and sequencing analyses were not performed, preventing a more detailed investigation of H. pylori transmission patterns in households. Future studies should explore this aspect to provide deeper insights into intra-household transmission patterns. Thirdly, the study lacked a control group, and the baseline characteristics of group A and group B, as well as treatment regimens the two groups received were not exactly the same. The true efficacy of family-based H. pylori control should be further evaluated through prospective randomized controlled trials.
Conclusions
This study demonstrated that a family-based H. pylori infection control and management strategy effectively improved eradication rates and enhanced hygiene awareness. However, further prospective randomized controlled studies are necessary to validate these findings and optimize family-based intervention strategies.
Acknowledgements
We thank the National Clinical Research Center for Digestive Diseases (Shanghai) for providing the standardized survey questionnaire used in this study. This study would not have been possible without the collaborative efforts in patient enrollment and specimen collection of the 22 participating hospitals in Chongqing: The Army Medical Center of People’s Liberation ArmyChongqing Hospital of Jiangsu Province HospitalChongqing University Three Gorges HospitalThe Affiliated Yongchuan Hospital of Chongqing Medical University The Affiliated Dazu’s Hospital of Chongqing Medical UniversityChonggang General HospitalThe First Affiliated Hospital of Chongqing Medical UniversityThe Fifth People’s Hospital of ChongqingChongqing University Cancer HospitalChongqing Hospital of PAPThe Ninth People’s Hospital of ChongqingPeople’s Hospital of Chongqing Nanchuan DistrictChongqing Red Cross HospitalChongqing Traditional Chinese Medicine HospitalChongqing Emergency Medical CenterChongqing General HospitalThe Xinqiao Hospital of AMUChongqing University Fuling HospitalThe Southwest Hospital of AMUPeople’s Hospital of Chongqing Banan DistrictPeople’s Liberation Army 958 HospitalThe Second Affiliated Hospital of Chongqing Medical University.
Authors’ contributions
Hengqi Liu: Investigation, Data curation, Formal analysis, Writing—original draft. Hanning Liu: Investigation, Data curation. Ling Fan, Yuntong Lan, Ping Chen, Ping He, Cheng Huang, and Sai Gu: Investigation. Haofeng Li and Qing Shi: Data curation. Chunhui Lan: Conceptualization, Funding acquisition, Writing—review & editing, Methodology. Yan Guo: Project administration, Supervision, Writing—review & editing.
Funding
This study was supported by Clinical Medical Innovation Competency Development Program of the Army Medical Center of People’s Liberation Army (Grant No. 2019CXLCB003), and Army Medical Center Artificial Intelligence + Medical Research Project (Grant No. ZXAIYB009).
Data availability
The data that support the findings of this study are not publicly available due to ethical restrictions regarding participant privacy. Data are available from the corresponding author upon reasonable request and with permission from the ethics committee.
Declarations
Ethics approval and consent to participate
Informed consent was obtained from all participants in accordance with the guidelines of the Declaration of Helsinki. The study was approved by the Ethics Committee of the Army Specialty Medical Centre Hospital (Medical Research and Luncheon Review 2023 No. 248), and it was registered in the China Clinical Research Centre (https://www.chictr.org.cn/; Registration No. ChiCTR2300078244; Registration Date 2023-12-01). All participants provided written informed consent to participate in the study.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Footnotes
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Hengqi Liu and Hanning Liu contributed equally to the study and should be regarded as co-first authors.
Contributor Information
Chunhui Lan, Email: lanchunhui@tmmu.edu.cn.
Yan Guo, Email: guoyan1112@tmmu.edu.cn.
References
- 1.Yang L, Kartsonaki C, Yao P, et al. The relative and attributable risks of cardia and non-cardia gastric cancer associated with Helicobacter pylori infection in china: a case-cohort study. Lancet Public Health. 2021;6(12):e888–96. 10.1016/S2468-2667(21)00164-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Malfertheiner P, Megraud F, Rokkas T, et al. Management of Helicobacter pylori infection: the Maastricht VI/Florence consensus report. Gut. 2022;71(9):1724–62. 10.1136/gutjnl-2022-327745. [Google Scholar]
- 3.Malfertheiner P, Camargo MC, El-Omar E, et al. Helicobacter pylori infection. Nat Rev Dis Primers. 2023;9(1):19. 10.1038/s41572-023-00431-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Moss SF, Shah SC, Tan MC, El-Serag HB. Evolving concepts in Helicobacter pylori management. Gastroenterology. 2024;166(2):267–83. 10.1053/j.gastro.2023.09.047. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Liou JM, Malfertheiner P, Lee YC, et al. Screening and eradication of Helicobacter pylori for gastric cancer prevention: the Taipei global consensus. Gut. 2020;69(12):2093–112. 10.1136/gutjnl-2020-322368. [DOI] [PubMed] [Google Scholar]
- 6.Sugano K, Tack J, Kuipers EJ, et al. Kyoto global consensus report on Helicobacter pylori gastritis. Gut. 2015;64(9):1353–67. 10.1136/gutjnl-2015-309252. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Lin Y, Zheng Y, Wang H, liang, Wu J. Global patterns and trends in gastric cancer incidence rates (1988–2012) and predictions to 2030. Gastroenterology. 2021;161(1):116–e1278. 10.1053/j.gastro.2021.03.023. [DOI] [PubMed] [Google Scholar]
- 8.Li Y, Choi H, Leung K, Jiang F, Graham DY, Leung WK. Global prevalence of Helicobacter pylori infection between 1980 and 2022: a systematic review and meta-analysis. Lancet Gastroenterol Hepatol. 2023;8(6):553–64. 10.1016/S2468-1253(23)00070-5. [DOI] [PubMed] [Google Scholar]
- 9.Chen YC, Malfertheiner P, Yu HT, et al. Global prevalence of Helicobacter pylori infection and incidence of gastric cancer between 1980 and 2022. Gastroenterology. 2024;166(4):605–19. 10.1053/j.gastro.2023.12.022. [DOI] [PubMed] [Google Scholar]
- 10.Wong MCS, Huang J, Chan PSF, et al. Global incidence and mortality of gastric Cancer, 1980–2018. JAMA Netw Open. 2021;4(7):e2118457. 10.1001/jamanetworkopen.2021.18457. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.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):209–49. 10.3322/caac.21660. [DOI] [PubMed] [Google Scholar]
- 12.Yang X, Zhang T, Zhang H, Sang S, Chen H, Zuo X. Temporal trend of gastric cancer burden along with its risk factors in China from 1990 to 2019, and projections until 2030: comparison with Japan, South Korea, and Mongolia. Biomark Res. 2021;9(1):84. 10.1186/s40364-021-00340-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Zeng S, Kong Q, Wu X, et al. Antibiotic resistance of Helicobacter pylori in Mainland China: a focus on geographic differences through systematic review and meta-analysis. Int J Antimicrob Agents. 2024;64(5):107325. 10.1016/j.ijantimicag.2024.107325. [DOI] [PubMed] [Google Scholar]
- 14.Duan M, Li Y, Liu J, et al. Transmission routes and patterns of Helicobacter pylori. Helicobacter. 2023;28(1):e12945. 10.1111/hel.12945. [DOI] [PubMed] [Google Scholar]
- 15.Young KA, Akyon Y, Rampton DS, et al. Quantitative culture of Helicobacter pylori from gastric juice: the potential for transmission. J Med Microbiol. 2000;49(4):343–7. 10.1099/0022-1317-49-4-343. [DOI] [PubMed] [Google Scholar]
- 16.Sgambato D, Visciola G, Ferrante E, et al. Prevalence of Helicobacter pylori infection in sexual partners of H. pylori-infected subjects: role of gastroesophageal reflux. United Eur Gastroenterol J. 2018;6(10):1470–6. 10.1177/2050640618800628. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Momtaz H, Souod N, Dabiri H, Sarshar M. Study of Helicobacter pylori genotype status in saliva, dental plaques, stool and gastric biopsy samples. World J Gastroenterol. 2012;18(17):2105–11. 10.3748/wjg.v18.i17.2105. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Che TH, Nguyen TC, Vu VNT, et al. Factors associated with Helicobacter pylori infection among school-aged children from a high prevalence area in Vietnam. Int J Public Health. 2023;68:1605908. 10.3389/ijph.2023.1605908. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Yuan C, Adeloye D, Luk TT, et al. The global prevalence of and factors associated with Helicobacter pylori infection in children: a systematic review and meta-analysis. Lancet Child Adolesc Health. 2022;6(3):185–94. 10.1016/S2352-4642(21)00400-4. [DOI] [PubMed] [Google Scholar]
- 20.Zhou XZ, Lyu NH, Zhu HY, 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):855–69. 10.1136/gutjnl-2022-328965. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Ding Z, Zhao S, Gong S et al. Prevalence and risk factors of Helicobacter pylori infection in asymptomatic Chinese children: a prospective, cross-sectional, population-based study. Aliment Pharmacol Ther. Published online 2015. [DOI] [PubMed]
- 22.Ito LS, Oba-Shinjo SM, Shinjo SK, Uno M, Marie SKN, Hamajima N. Community-based familial study of Helicobacter pylori infection among healthy Japanese Brazilians. Gastric Cancer. 2006;9(3):208–16. 10.1007/s10120-006-0384-5. [DOI] [PubMed] [Google Scholar]
- 23.Kivi M, Tindberg Y, Sörberg M, et al. Concordance of Helicobacter pylori strains within families. J Clin Microbiol. 2003;41(12):5604–8. 10.1128/JCM.41.12.5604-5608.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Herrera PM, Mendez M, Velapatiõ B, et al. DNA-level diversity and relatedness of Helicobacter pylori strains in shantytown families in Peru and transmission in a developing-country setting. J Clin Microbiol. 2008;46(12):3912–8. 10.1128/JCM.01453-08. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Didelot X, Nell S, Yang I, Woltemate S, Van Der Merwe S, Suerbaum S. Genomic evolution and transmission of Helicobacter pylori in two South African families. Proc Natl Acad Sci U S A. 2013;110(34):13880–5. 10.1073/pnas.1304681110. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Nahar S, Kibria KMK, Hossain ME, et al. Evidence of intra-familial transmission of Helicobacter pylori by PCR-based RAPD fingerprinting in Bangladesh. Eur J Clin Microbiol Infect Dis. 2009;28(7):767–73. 10.1007/s10096-008-0699-8. [DOI] [PubMed] [Google Scholar]
- 27.Dominici P, Bellentani S, Biase ARD, et al. Familial clustering of Helicobacter pylori infection: population based study. BMJ. 1999;319:537-40. 10.1136/bmj.319.7209.537. [DOI] [PMC free article] [PubMed]
- 28.Ding SZ. Global whole family based-Helicobacter pylori eradication strategy to prevent its related diseases and gastric cancer. World J Gastroenterol. 2020;26(10):995–1004. 10.3748/wjg.v26.i10.995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Ding SZ, Du YQ, Lu H, et al. Chinese consensus report on family-based Helicobacter pylori infection control and management (2021 edition). Gut. 2022;71(2):238–53. 10.1136/gutjnl-2021-325630. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30.Zhao JB, Yuan L, Yu XC, 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. 10.1111/hel.12793. [DOI] [PubMed] [Google Scholar]
- 31.Ma J, Yu M, Shao QQ, 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. 10.1111/hel.12911. [DOI] [PubMed] [Google Scholar]
- 32.Liu WZ, Xie Y, Lu H, et al. Fifth Chinese national consensus report on the management of Helicobacter pylori infection. Helicobacter. 2018;23(2):e12475. 10.1111/hel.12475. [DOI] [PubMed] [Google Scholar]
- 33.Han R, Lu H, Jiang MW, et al. Multicenter study of antibiotic resistance profile of H. pylori and distribution of CYP2C19 gene polymorphism in rural population of Chongqing, China. Gastroenterol Res Pract. 2016;2016:8547686. 10.1155/2016/8547686. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Zeng R, Li X, Wang F, Xie J, Song C, Xie Y. Reinforced medication adherence improves Helicobacter pylori eradication rate in developing countries: a systematic review and meta-analysis of randomized controlled trials. Helicobacter. 2023;28(4):e12989. 10.1111/hel.12989. [DOI] [PubMed] [Google Scholar]
- 35.Zhou B, Yan X, Wan L, Zhang Q, Li B, Ai Y. Effect of enhanced patient instructions on Helicobacter pylori eradication: a systematic review and meta-analysis of randomized controlled trials. Helicobacter. 2022;27(2):e12869. 10.1111/hel.12869. [DOI] [PubMed] [Google Scholar]
- 36.Zha J, Li YY, Qu JY, Yang XX, Han ZX, Zuo X. Effects of enhanced education for patients with the Helicobacter pylori infection: a systematic review and meta-analysis. Helicobacter. 2022;27(2):e12880. 10.1111/hel.12880. [DOI] [PubMed] [Google Scholar]
- 37.Li XT, Xu L, Zhang C, et al. Improved patient adherence to family-based Helicobacter pylori infection control and management strategy in central China and its influencing factors. Helicobacter. 2024;29(4):e13114. 10.1111/hel.13114. [DOI] [PubMed] [Google Scholar]
- 38.Liu Q, Zeng X, Wang W, et al. Awareness of risk factors and warning symptoms and attitude towards gastric cancer screening among the general public in China: a cross-sectional study. BMJ Open. 2019;9(7):e029638. 10.1136/bmjopen-2019-029638. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 39.Zhang C, Qi YB, Hu RB. Family‐based Helicobacter pylori infection control and management strategy and screen‐and‐treat strategy are highly cost‐effective in preventing multiple upper gastrointestinal diseases in Chinese population at national level. Helicobacter. 2024;29(3):e13063. 10.1111/hel.13063. [DOI] [PubMed] [Google Scholar]
- 40.Lei WY, Lee JY, Chuang SL, 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;(12):gutjnl–2023. 10.1136/gutjnl-2023-329871. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41.Kong Q, Li Y, Li R, et al. Low compliance to post-screening recommendations in a family‐based Helicobacter pylori screening and treatment program: A prospective cohort study. Helicobacter. 2022;27(5). 10.1111/hel.12912. [DOI] [PubMed]
- 42.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. 10.1111/hel.12705. [DOI] [PubMed] [Google Scholar]
- 43.Bailey KS, Brown HE, Lekic V, Pradeep K, Merchant JL, Harris RB. Helicobacter pylori treatment knowledge, access and barriers: a cross-sectional study. Helicobacter. 2023;28(2):e12954. 10.1111/hel.12954. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 44.Zhou JK, Zheng Y, Wang YP, Ji R. Prevalence and associated risk factors of Helicobacter pylori infection in community households in Lanzhou City. World J Gastroenterol. 2024;30(47):5018–31. 10.3748/wjg.v30.i47.5018. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 45.Rowland M, Clyne M, Daly L, et al. Long-term follow-up of the incidence of Helicobacter pylori. Clin Microbiol Infect. 2018;24(9):980–4. 10.1016/j.cmi.2017.10.020. [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The data that support the findings of this study are not publicly available due to ethical restrictions regarding participant privacy. Data are available from the corresponding author upon reasonable request and with permission from the ethics committee.