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Table of Contents   
ORIGINAL ARTICLE  
Year : 2022  |  Volume : 28  |  Issue : 2  |  Page : 149-156
Long-term effects and benefits of Helicobacter pylori eradication on the gastric mucosa in older individuals


1 Department of Gastroenterology, Huadong Hospital Affiliated to Fudan University, Shanghai, China
2 Geriatric Medical Center, Taikang Shenyuan Rehabilitation Hospital, Shanghai, China
3 Department of General Practice, Huadong Hospital Affiliated to Fudan University, Shanghai, China
4 Department of Digestive Endoscopy, Huadong Hospital Affiliated to Fudan University, Shanghai, China
5 Department of Pathology, Huadong Hospital Affiliated to Fudan University, Shanghai, China

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Date of Submission17-Apr-2021
Date of Acceptance30-Jul-2021
Date of Web Publication25-Jan-2022
 

   Abstract 


Background: The current international consensus report indicated that all Helicobacter pylori (H. pylori)-positive patients should be treated. This study aimed to evaluate the long-term effects and benefits of H. pylori eradication on the gastric mucosa in the elderly population.
Methods: We performed a retrospective cohort study with 311 individuals aged ≥60 years, including 83 with persistent H. pylori infection (persistent group), 128 with successful H. pylori eradication (eradicated group), and 100 without H. pylori infection (control group). The results of endoscopy and mucosal histology were investigated at baseline and followed up for 5 and 10 years.
Results: In the 5 to 10-year follow-up, there was a significant difference in the atrophy score among the three groups (P < 0.001); however, no significant difference was observed in the intestinal metaplasia (IM) score (P > 0.05). There was no significant difference in the cumulative incidence of gastric neoplastic lesion (GNL) between the eradicated and persistent groups during the 5 to 10-year follow-up period (P > 0.05). The baseline IM score of patients with GNL was significantly higher than that of those without GNL in the eradicated and control groups (P < 0.05). In all patients with GNL, the mean interval time between baseline and diagnosis of GLN was more than 6 years. The severity of baseline mucosal IM (odds ratio: OR 3.092, 95% confidence interval [CI]: 1.690–5.655, P < 0.001) and H. pylori infection (OR: 2.413, 95%CI: 1.019–5.712, P = 0.045) significantly increased the risk for GNL.
Conclusions: Older patients with a life expectancy of less than 5 to 10 years, especially those with moderate to severe gastric mucosal IM, may not benefit from the eradication of H. pylori to prevent gastric cancer.

Keywords: Atrophy, elderly, Helicobacter pylori, intestinal metaplasia, life expectancy

How to cite this article:
Chen J, Zhang G, Qin J, Huang Y, Wang Y, Li Z, Ji D, Xiao L, Yin S, Bao Z. Long-term effects and benefits of Helicobacter pylori eradication on the gastric mucosa in older individuals. Saudi J Gastroenterol 2022;28:149-56

How to cite this URL:
Chen J, Zhang G, Qin J, Huang Y, Wang Y, Li Z, Ji D, Xiao L, Yin S, Bao Z. Long-term effects and benefits of Helicobacter pylori eradication on the gastric mucosa in older individuals. Saudi J Gastroenterol [serial online] 2022 [cited 2022 Jul 2];28:149-56. Available from: https://www.saudijgastro.com/text.asp?2022/28/2/149/336455

Authors Jie Chen, Gansheng Zhang and Jian Qin contributed equally to this work





   Introduction Top


With an aging population, increasing attention has been paid to the prevention and treatment of cancer. As a promoter of gastric carcinogenesis, the World Health Organization has categorized  Helicobacter pylori Scientific Name Search ori) as a class I carcinogen for gastric cancer in 1994.[1] H. pylori infection is considered a global public health problem. Older individuals aged over 60 years have the highest infection rate,[2] and the infection rate of H. pylori in the older population in Shanghai, China, is as high as 72.4%.[3]

Given the risk of H. pylori infection, the current international consensus report indicated that all H. pylori-positive patients should be treated.[1],[4],[5] In areas with a high incidence of gastric cancer, especially in high-risk individuals, the “test and treat” strategy for H. pylori infection is recommended. H. pylori gastritis is an infectious disease.[1],[4] Still, there is no upper age limit for H. pylori eradication therapy. The older population, especially senior patients (aged ≥ 80 years), have a higher number of comorbidities, usage of medications, prevalence of atrophy and intestinal metaplasia (IM) (89% and 82%, respectively), or a combination of these factors.[6] In addition, because of the positive correlation between life expectancy and incidence of cancer,[7] the previous literature and international consensus reported that age alone is not sufficient to determine the appropriateness of screening and treatment. In particular, individuals who have a life expectancy of less than 5 years will not benefit from cancer screening.[8] Thus, the potential benefits of H. pylori eradication in older patients for the prevention of gastric cancer may be reduced. However, it remains unclear whether H. pylori eradication therapy should be carried out in older patients.[9] At present, there is no consensus on the treatment of H. pylori infection in older adults, and only a few studies reported the impact of eradication treatment in older individuals.[2],[10] Hence, this study aimed to evaluate the long-term effects and benefits of H. pylori eradication on the gastric mucosa in older individuals.


   Subjects and Methods Top


Study patients

From January 2007 to December 2009, as a result of a screening program for early detection of gastric cancer in the elderly aged ≥60 years, 3,671 individuals who underwent esophagogastroduodenoscopy (EGD) due to digestive diseases or routine health screening examinations were registered in Huadong Hospital Affiliated to Fudan University. Of these patients, 3,028 were investigated for their H. pylori status, and 1,636 were confirmed to have an active H. pylori infection (baseline investigation). These patients were informed about the increased risk of GC associated with H. pylori and about the need to undergo regular endoscopic histological follow-up investigations, at intervals not exceeding 3 years. The following inclusion criteria were used to enroll these individuals within the screening program: 1. age over 60 years, 2. long-term follow-up data on results of the 13C-urea breath test, EGD, and pathological examination, 3. a follow-up period of at least 10 years. Exclusion criteria included patients with 1. severe comorbidities (such as heart, lung, and other organic diseases); 2. prior dysplasia of the gastric mucosa and malignancies, or who underwent surgery, radiation, and chemical treatment; 3. cognitive behavior abnormalities who were unable to communicate and cooperate with related examinations; 4. follow-up loss. Therefore, 211 H. pylori-positive patients were enrolled in this study. All of them were divided into two groups according to H. pylori infection status, diagnosis, and treatment history: 1. persistent group (n = 83 patients), with 21 having H. pylori infection without treatment, 13 who refused treatment, 26 who experienced treatment failure, and 23 who had incomplete eradication; and 2. eradicated group (n = 128), with 91 who received initial treatment for eradication and 37 with remedial treatment for eradication, and with none of the patients experiencing reinfection. A total of 100 older subjects with no history of H. pylori infection were randomly selected as the control group in the same period [Figure 1]. General demographic and medical history data were obtained by reviewing outpatient and inpatient medical records, as well as through a telephone interview. This study was designed as a retrospective cohort study. The Ethics Committee of Huadong Hospital Affiliated with Fudan University approved this study (number: 2017K039), and all participants provided written informed consent.
Figure 1: Flow of study patients. EGD: oesophagogastroduodenoscopy; H. pylori: Helicobacter pylori

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EGD and pathological examination

According to mucosal manifestations, two pieces of mucosal tissues were obtained from the gastric antrum (from the lesser curvature of the antrum within 2 to 3 cm of the pylorus) and one piece of mucosal tissue from the gastric body (from the greater curvature of the middle of the gastric body). Samples were fixed, embedded, sectioned, and stained by modified Giemsa for mucosal histological examination and H. pylori diagnosis. The results of EGD and mucosal histology in 311 patients were investigated at baseline and followed up for 5 and 10 years. Pathological analysis was performed by an experienced pathologist who was blinded to the clinical information. Histopathological changes (inflammation, activity, atrophy, and IM), based on the visual analog scale of the updated Sydney System, were graded (none = 0, mild = 1, moderate = 2, and severe = 3).[11] The mean scores of the above two sites of each individual were recorded. Follow-up endoscopic examinations were performed to identify any gastric neoplastic lesion (GNL). A GNL was defined as a new adenocarcinoma, adenoma with dysplasia, or dysplasia without endoscopic lesions.

Detection of H. pylori infection

H. pylori infection was diagnosed when the 13C-UBT, rapid urease test, or histologic examination result was positive. When the 13C-UBT result was negative, a diagnosis of no H. pylori infection was established.[5]

Statistical analysis

Statistical analysis was performed using SPSS version 22.0. The measurement data are expressed as mean ± SD and analyzed using Student's t-test, one-way analysis of variance, or Wilcoxon's rank-sum test. Categorical data were analyzed using the Chi-square test or Fisher's exact test. The cumulative incidence of GNL was calculated using the Kaplan–Meier method, and the values among the groups were compared using the log-rank test. Risk factors of GNL were examined by multivariate analysis using the logistic regression model. P values < 0.05 were considered significant.


   Results Top


General information

A total of 311 older patients were enrolled in the study. Patients were aged 60 to 90 years, of whom 121 (38.9%) were senior patients (aged ≥80 years). At baseline and all follow-up investigations no cases of loss of visit and death occurred. There was no significant difference in the distribution of age, sex, and follow-up time among the three groups (P > 0.05) [Table 1].
Table 1: Baseline characteristics of all groups

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Age, sex, and gastric mucosa histopathological score

At baseline, mild-to-moderate gastric mucosal lesions were detected in the patients in all age groups. It was also noted that the scores of gastric mucosal atrophy and IM increased with age. The IM scores in the eradicated group and the atrophy scores in the control group were significantly increased in all age groups (χ2 = 11.999 P = 0.007; χ2 = 8.303, P = 0.04, respectively). At baseline, the scores of gastric mucosa atrophy and IM in the three groups were not correlated with sex (data not shown), and the differences were not statistically significant (P > 0.05) [Figure 2].
Figure 2: Relationship between age and the histopathological score of gastric mucosa in all groups. (a) Atrophy scores; (b) Intestinal metaplasia scores

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Follow-up time and gastric mucosa histopathological score

At baseline, the scores of gastric mucosal atrophy and IM in the persistent group were similar to those in the eradicated group (Z = −0.448, P = 0.654; Z = −0.384, P = 0.701). These scores were higher than those in the control group (Z = −2.172, P = 0.030; Z = −3.466, P = 0.001). In the 5-year follow-up, the atrophy and IM scores in the eradicated group decreased by 0.183 points (Z = −2.669, P = 0.008) and 0.013 points (Z = −0.033, P = 0.974), respectively, compared with those at baseline. Moreover, there was a more significant improvement in atrophy scores compared with IM scores in the eradicated group (Z = −6.895, P < 0.001). There was a statistically significant difference in the atrophy score among the three groups (χ2 = 16.768, P < 0.001), but no significant difference in the IM score (χ2 = 3.070, P = 0.215). In the 10-year follow-up, the atrophy score of the three groups was higher than that in the 5-year follow-up, the difference among the three groups was statistically significant (χ2 = 15.401, P < 0.001). The IM score was not significantly different among the three groups (χ2 = 5.320, P = 0.070). The atrophy and IM scores of the three groups were compared with their respective scores at baseline, and the differences were not statistically significant (P > 0.05) [Figure 3].
Figure 3: Relationship between the follow-up time and histopathological score of gastric mucosa in all groups. (a) Atrophy scores; (b) Intestinal metaplasia scores

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Cumulative incidence of GNL

At the 5-year follow-up, four patients (4.82%) in the persistent group, two (1.56%) in the eradicated group, and one (1%) in the control group developed GNL. At the 10-year follow-up, 11 patients (13.25%) in the persistent group, 10 (7.81%) in the eradicated group, and 5 (5%) in the control group developed GNL. There was no significant difference in the cumulative incidence of GNL among the three groups (χ2 = 4.190, P = 0.123) [Figure 4], [Table 2].
Figure 4:Kaplan–Meier analysis of the cumulative incidence of GNL in all groups. GNL: gastric neoplastic lesion

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Table 2: Kaplan-Meier survival analysis for the cumulative incidence of GNL in all groups

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Clinicopathological features of patients with GNL

Among the three groups, the baseline gastric mucosal atrophy score of the patients with GNL was slightly higher than those without (P > 0.05). The baseline IM score of patients with GNL was significantly higher than those without (P < 0.05) (except for the persistent group). In contrast, the average severity of IM of patients with GNL was moderate or high. In all patients with GNL, the median interval time between baseline and diagnosis of GNL was more than 6 years; there was no significant difference among the three subgroups with GNL (F = 0.375, P = 0.691). No significant difference was observed in other clinical characteristics, including age and sex, between the patients with and without GNL in each group (P > 0.05) [Table 3].
Table 3: Comparison of clinicopathological features between individuals with and without GNL in all groups

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Factors related to GNL

A multivariate logistic regression model was used to analyze the risk factors for GNL including age, sex, follow-up time, the severity of baseline mucosal atrophy, and IM. Results showed that the severity of baseline mucosal IM (odds ratio [OR]: 3.092, 95% confidence interval [CI]: 1.690–5.655, P < 0.001) and H. pylori infection (OR: 2.413, 95% CI: 1.019–5.712 P = 0.045) significantly increased the risk for GNL, but it had no correlation with age, sex, follow-up time, and the severity of baseline mucosal atrophy (P > 0.05) [Table 4].
Table 4: Results of multivariate logistic regression analysis of risk factors for GNL

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   Discussion Top


In older individuals, H. pylori infection is mostly acquired during childhood,[12] and the proportion of people with normal gastric mucosa decreases (approximately 50%) with age.[13] Our investigation showed that over 10 years, older patients generally develop mild-to-moderate gastric mucosal lesions and higher atrophy and IM scores compared with younger patients, even in the control group; these differences were found to be regardless of sex. This trend is not only related to H. pylori infection but also shows that the extent of gastric mucosal aging and atrophy varies and is age-dependent.[13],[14] This conclusion is slightly different from the results of previous Japanese studies. Asaka showed that H. pylori infection, rather than aging itself, caused atrophic gastritis and IM.[15] However, in H. pylori-positive individuals, both atrophy and IM were aggravated by aging.[16]

The benefit of H. pylori eradication may be related to the length of the follow-up period.[17] A 12-year randomized controlled study in high-risk areas showed that H. pylori eradication had a significant effect on the repair of precancerous gastric lesions, which was cumulative and enhanced over time.[18] Our results showed that the severity of atrophy and IM gradually increased in the persistent H. pylori infection group during the disease, whereas it decreased in the eradicated group. At the 5-year follow-up, the reduction in atrophy was more evident than that of IM, showing the expected curative effect and indicating that eradication of H. pylori in older patients may have more benefit in individuals with atrophy at baseline than in those with IM within a short period (<5 years). This finding is consistent with the results of Mera.[19] However, long-term (≥5–10 years) efficacy showed no cumulative improvement effect on atrophy. On the contrary, the severity of atrophy gradually increased, especially in the control group, and the severity of atrophy and IM also showed a slow upward trend. This phenomenon indicates that with the prolonged course of the disease, even without H. pylori infection, the risk of bile reflux, and exposure to environmental factors (drugs, food, and tobacco) as well as the socioeconomic status will also significantly increase in older patients, which can lead to further chronic injury of the gastric mucosa, lamina propria glandular atrophy, and IM.[20],[21]

In this study, improvement in the IM score in the eradication group was relatively gradual during the follow-up period, which confirmed that the recovery of IM is a long-term process.[18] The eradication of H. pylori can at least prevent further development of IM; because its molecular regulatory mechanism may be different from atrophy, the change in IM after eradication of H. pylori may not be related to the latter.[22]

According to a previous study,[23] in addition to H. pylori infection (HR = 3.9), the severity of basic gastric mucosal atrophy (HR = 3.9) is also a primary contributor to the risk of gastric cancer. We have similar findings in the baseline gastric mucosal survey of patients with GNL. In the eradicated group, even if the effect of H. pylori was eliminated, the risk for GNL in patients with moderate or severe gastric mucosal IM at baseline remained significantly higher than that in patients with mild or insufficient IM at baseline. The above characteristics were also noted in the control group but not in the persistent group. Therefore, the preventive effect of H. pylori eradication on gastric cancer depends on the severity of baseline gastric mucosal lesions. When H. pylori eradication can no longer prevent the development of gastric cancer, the precancerous state (such as moderate or severe mucosal IM) may represent the point of irreversibility.[1],[24] IM is the most common precancerous lesion, but most patients with IM will not develop gastric cancer, which is closely related to the subtypes of IM rather than H. pylori infection eradication.[19] Therefore, older patients who experienced moderate and severe IM of the gastric mucosa may not benefit from the eradication of H. pylori to prevent gastric cancer.

Studies have shown that the spontaneous clearance rate of H. pylori is higher in older individuals than in younger adults.[1],[25] Kawaguchi demonstrated that among older patients aged over 85 years, the severity score of IM in the gastric mucosa was significantly higher in H. pylori-negative patients than in those who were positive.[20] This suggests that IM may promote clearance of H. pylori infection in older individuals. Gastric mucosa with severe atrophy and intestinal mucosa is not conducive to H. pylori colonization.[6] As a result, there is a possibility for older patients with H. pylori infection to avoid treatment for it.

The benefits of H. pylori eradication differ among patients, especially in older individuals. A 10-year follow-up study in Japan found that a lower incidence of gastric cancer after H. pylori eradication was negatively correlated with age.[26] Furthermore, a recent retrospective study from Hong Kong,[27] China, showed that H. pylori eradication in populations aged over 60 years could also be beneficial. Still, the effect of reducing the incidence of gastric cancer would not be apparent until 10 years after eradication. As a result, some studies have proposed that conventional cancer screening and treatment have no real net benefit to individuals with a limited life span.[8],[28] In 2014, gastric cancer incidence in men peaked at the age of 80 to 84 years in China, whereas in women, it peaked at the age of >85 years.[29] The average life expectancy was 76.34 years (men, 73.64 years; women, 79.43 years) at the same time.[7] In the current study, there was no significant difference in the cumulative incidence of GNL between the eradicated and persistent groups during the 5 to 10-year follow-up period. Meanwhile, the median interval time between baseline and diagnosis of GNL in all groups was more than 6 years. Therefore, we believe that the eradication of H. pylori in older individuals does not show apparent primary prevention advantages and maximum curative effect within the expected limited time (5–10 years), compared with the non-eradication of H. pylori. It is necessary to carefully evaluate the benefit–risk ratio of the eradication of H. pylori in older patients, and individualized treatment should be carried out based on comprehensive factors, such as life expectancy and comorbidity.

The results of this study confirmed that the severity of baseline gastric mucosal IM and H. pylori infection were closely related to GNL. As a primary preventive measure to reduce the risk of gastric cancer, the eradication of H. pylori cannot eliminate the risk of gastric cancer in patients with gastric mucosa IM. Therefore, it is necessary to carry out secondary preventive measures according to the basic gastric mucosal status of older individuals.[30] However, for older patients whose life expectancy is less than 5 to 10 years, especially those who have moderate or severe IM of the gastric mucosa, eradication of H. pylori is not recommended. In these cases, other corresponding treatments can be given, as appropriate, and attention should be paid to the infectivity of H. pylori.[6] Therefore, for older patients with H. pylori infection, the “endoscopy and treat” strategy may be more appropriate instead of the H. pylori ”test and treat” strategy.[10]

This study had some limitations. First, this study was a single-center retrospective cohort study without a non-elderly control group, which may be biased by selection. Second, due to the multifocal distribution of gastric precancerous lesions, there may be sampling errors, and no stratified studies have been conducted on the lesion site (antrum, corpus of the stomach), IM subtype, environmental factors (drugs, tobacco), H. pylori infection course, and treatment frequency. Third, the 10-year follow-up may not be sufficient to fully analyze the long-term results.

In conclusion, it is necessary to eradicate H. pylori in older patients to improve or delay gastric precancerous lesions and prevent gastric cancer. However, even if H. pylori is eradicated, the baseline status of the gastric mucosa in older adults affects the progression of such precancerous lesions. Older patients with a life expectancy of less than 5 to 10 years, especially those with moderate-to-severe gastric mucosal IM, may not benefit from the eradication of H. pylori infection. In future studies, a larger number of patients need to be followed up for a longer time to confirm our conclusion.

Financial support and sponsorship

This study was funded by the Scientific Research Projects of Shanghai Municipal Commission of Health and Family Planning (No. 201740182).

Conflicts of interest

There are no conflicts of interest.



 
   References Top

1.
Malfertheiner P, Megraud F, O'Morain CA, Gisbert JP, Kuipers EJ, Axon AT, et al. European Helicobacter and Microbiota Study Group and Consensus panel. Management of Helicobacter pylori infection-the Maastricht V/Florence consensus report. Gut 2017;66:6-30.  Back to cited text no. 1
    
2.
Pilotto A, Malfertheiner P. Review article: An approach to Helicobacter pylori infection in the elderly. Aliment Pharmacol Ther 2002;16:683-91.  Back to cited text no. 2
    
3.
Chen SY, Liu TS, Fan XM, Dong L, Fang GT, Tu CT, et al. Epidemiological study of Helicobacter pylori infection and its risk factors in Shanghai. Natl Med J China 2005;85:802-6.  Back to cited text no. 3
    
4.
Sugano K, Tack J, Kuipers EJ, Graham DY, El-Omar EM, Miura S, et al. Faculty members of Kyoto Global Consensus Conference. Kyoto global consensus report on Helicobacter pylori gastritis. Gut 2015;64:1353-67.  Back to cited text no. 4
    
5.
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:e12475. doi: 10.1111/hel. 12475.  Back to cited text no. 5
    
6.
Chen S, Ying L, Kong M, Zhang Y, Li Y. The prevalence of helicobacter pylori infection decreases with older age in atrophic gastritis. Gastroenterol Res Pract 2013;2013:494783.  Back to cited text no. 6
    
7.
Gu XY, Zheng RS, Xia CF, Zeng HM, Zhang SW, Zou XN, et al. Interactions between life expectancy and the incidence and mortality rates of cancer in China: A population-based cluster analysis. Cancer Commun (Lond) 2018;38:44-59.  Back to cited text no. 7
    
8.
Royce TJ, Hendrix LH, Stokes WA, Allen IM, Chen RC. Cancer screening rates in individuals with different life expectancies. JAMA Intern Med 2014;174:1558-65.  Back to cited text no. 8
    
9.
Liu KS, Wong IO, Leungn WK. Helicobacter pylori associated gastric intestinal metaplasia: Treatment and surveillance. World J Gastroenterol 2016;22:1311-20.  Back to cited text no. 9
    
10.
Cizginer S, Ordulu Z, Kadayifci A. Approach to Helicobacter pylori infection in geriatric population. World J Gastrointest Pharmacol Ther 2014;5:139-47.  Back to cited text no. 10
    
11.
Tytgat GN. The Sydney system: Endoscopic division. Endoscopic appearances in gastritis/duodenitis. J Gastroenterol Hepatol 1991;6:223-34.  Back to cited text no. 11
    
12.
Dore MP, Cipolli A, Ruggiu MW, Manca A, Bassotti G, Pes GM. Helicobacter pylori eradication may influence timing of endoscopic surveillance for gastric cancer in patients with gastric precancerous lesions: A retrospective study. Medicine (Baltimore) 2018;97:e9734. doi: 10.1097/MD.0000000000009734.  Back to cited text no. 12
    
13.
Wang XZ, Zheng SB; Chinese Geriatrics Society, Editorial Board of Chinese Journal of Geriatrics. Chinese expert consensus on chronic gastritis in the elderly. Chin J Geriatr 2018;37:485-91.  Back to cited text no. 13
    
14.
Sonnenberg A, Genta RM. Changes in the gastric mucosa with aging. Clin Gastroenterol Hepatol 2015;13:2276-81.  Back to cited text no. 14
    
15.
Asaka M, Kato M, Kudo M, Katagiri M, Nishikawa K, Koshiyama H. Atrophic changes of gastric mucosa are caused by Helicobacter pylori infection rather than aging: Studies in asymptomatic Japanese adults. Helicobacter 1996;1:52-6.  Back to cited text no. 15
    
16.
Sakaki N, Kozawa H, Egawa N, Tu Y, Sanaka M. Ten-year prospective follow-up study on the relationship between Helicobacter pylori infection and progression of atrophic gastritis, particularly assessed by endoscopic findings. Aliment Pharmacol Ther 2002;16:198-203.  Back to cited text no. 16
    
17.
Kong YJ, Yi HG, Dai JC, Wei MX. Histological changes of gastric mucosa after Helicobacter pylori eradication: A systematic review and meta-analysis. World J Gastroenterol 2014;20:5903-11.  Back to cited text no. 17
    
18.
Mera R, Fontham ETH, Bravo LE, Bravo JC, Piazuelo MB, Camargo MC, et al. Long term follow up of patients treated for Helicobacter pylori infection. Gut 2005;54:1536–40.  Back to cited text no. 18
    
19.
Mera RM, Bravo LE, Camargo MC, Bravo JC, Delgado AG, Romero-Gallo J, et al. Dynamics of Helicobacter pylori infection as a determinant of progression of gastric precancerous lesions: 16-year follow-up of an eradication trial. Gut 2018;67:1239-46.  Back to cited text no. 19
    
20.
Kawaguchi H, Haruma K, Komoto K, Yoshihara M, Sumii K, Kajiyama G. Helicobacter pylori infection is the major risk factor for atrophic gastritis. Am J Gastroenterol 1996;91:959-62.  Back to cited text no. 20
    
21.
Kwon YH, Heo J, Lee HS, Cho CM, Jeon SW. Failure of Helicobacter pylori eradication and age are independent risk factors for recurrent neoplasia after endoscopic resection of early gastric cancer in 283 patients. Aliment Pharmacol Ther 2014;39:609-18.  Back to cited text no. 21
    
22.
Niikura R, Hayakawa Y, Hirata Y, Ogura K, Fujishiro M, Yamada A, et al. The reduction in gastric atrophy after helicobacter pylori eradication is reduced by treatment with inhibitors of gastric acid secretion. Int J Mol Sci 2019;20:1-11.  Back to cited text no. 22
    
23.
Kaji K, Hashiba A, Uotani C, Yamaguchi Y, Ueno T, Ohno K, et al. Grading of atrophic gastritis is useful for risk stratification in endoscopic screening for gastric cancer. Am J Gastroenterol 2019;114:71-9.  Back to cited text no. 23
    
24.
Du YQ, Zhu HY, Liu J, Li JN, Chang X, Zhou LY, et al. Consensus on eradication of Helicobacter pylori and prevention and control of gastric cancer in China (2019, Shanghai). J Gastroenterol Hepatol 2019;35:624-9.  Back to cited text no. 24
    
25.
Tytgat GN. Long-term consequences of Helicobacter pylori eradication. Scand J Gastroenterol 1994;205(Suppl):38-44.  Back to cited text no. 25
    
26.
Asaka M, Kato M, Graham DY. Strategy for eliminating gastric cancer in Japan. Helicobacter 2010;15:486-90.  Back to cited text no. 26
    
27.
Leung WK, Wong IO, Cheung KS, Yeung KF, Chan EW, Wong AY, et al. Effects of Helicobacter pylori Treatment on incidence of gastric cancer in older individuals. Gastroenterology 2018;155:67-75.  Back to cited text no. 27
    
28.
Woolf SH, Harris R. The harms of screening: New attention to an old concern. JAMA 2012;307:565-6.  Back to cited text no. 28
    
29.
Yang L, Zheng R, Wang N, Yuan Y, Liu S, Li H, et al. Incidence and mortality of stomach cancer in China, 2014. Chin J Cancer Res 2018;30:291-8.  Back to cited text no. 29
    
30.
Bornschein J, Bird-Lieberman EL, Malfertheiner P. The rationale and efficacy of primary and secondary prevention in adenocarcinomas of the upper gastrointestional tract. Dig Dis 2019;37:381-93.  Back to cited text no. 30
    

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Correspondence Address:
Dr. Shuming Yin
No. 221 West Yan'an Road, Shanghai - 200040
China
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/sjg.sjg_206_21

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