|
1
|
Xiang Y, Yuan Y, Wang ZY, Zhu YM, Li WY, Ye QG, Wang YN, Sun Q, Ding XW, Longi F, Tang DH, Xu GF. Comorbidities related to metachronous recurrence for early gastric cancer in elderly patients. World J Gastrointest Endosc 2025; 17:99540. [DOI: 10.4253/wjge.v17.i3.99540] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/24/2024] [Revised: 09/15/2024] [Accepted: 12/05/2024] [Indexed: 03/14/2025] Open
Abstract
BACKGROUND A significant association between increased age and an increased risk of metachronous gastric cancer (MGC) following curative endoscopic submucosal dissection (ESD) has previously been reported.
AIM To determine risk factors for the metachronous occurrence of early gastric cancer (EGC) in elderly individuals.
METHODS This retrospective cohort study comprised 653 elderly patients (aged ≥ 65 years) who underwent curative ESD for EGC between January 2014 and June 2020 at Nanjing Drum Tower Hospital. Comprehensive analyses were conducted to compare lifestyle habits, comorbidities, and Helicobacter pylori (H. pylori) infections as potential indicators.
RESULTS During a median follow-up of 38 months, 46 patients (7.0%, 20.46/1000 person-years) developed MGC in the elderly cohort. The cumulative incidences of MGC at 2, 3, and 5 years were 3.3%, 5.3%, and 11.5%, respectively. In multivariate Cox regression analyses, the independent risk factors for MGC included metabolic dysfunction-associated steatotic liver disease (MASLD) [hazard ratio (HR) = 2.44, 95% confidence interval (CI): 1.15-5.17], persistent H. pylori infection (HR = 10.38, 95%CI: 3.36-32.07), severe mucosal atrophy (HR = 2.71, 95%CI: 1.45-5.08), and pathological differentiation of EGC (well/moderately differentiated vs poorly differentiated: HR = 10.18, 95%CI: 1.30-79.65). Based on these risk factors, a risk stratification system was developed to categorize individuals into low (0-1 point), intermediate (2-3 points), and high (4-8 points) risk categories for MGC, with cumulative incidence rates of 12.3%, 21.6%, and 45%, respectively.
CONCLUSION Among elderly individuals, MASLD, persistent H. pylori infection, severe mucosal atrophy, and well/moderately differentiated EGC were associated with an increased risk of MGC. Elderly patients are recommended to adopt healthy lifestyle practices, and undergo regular endoscopic screening and H. pylori testing after curative ESD for EGC.
Collapse
Affiliation(s)
- Ying Xiang
- Department of Gastroenterology, Nanjing Drum Tower Hospital Clinical College of Nanjing University of Chinese Medicine, Nanjing 210008, Jiangsu Province, China
| | - Ying Yuan
- Department of Gastroenterology, Affiliated Drum Tower Hospital of Nanjing University Medical School, Nanjing 210008, Jiangsu Province, China
| | - Zhen-Yu Wang
- Department of Gastroenterology, Affiliated Drum Tower Hospital of Nanjing University Medical School, Nanjing 210008, Jiangsu Province, China
| | - Yan-Mei Zhu
- Department of Gastroenterology, Nanjing Drum Tower Hospital Clinical College of Nanjing University of Chinese Medicine, Nanjing 210008, Jiangsu Province, China
| | - Wen-Ying Li
- Department of Gastroenterology, Nanjing Drum Tower Hospital Clinical College of Nanjing University of Chinese Medicine, Nanjing 210008, Jiangsu Province, China
| | - Qian-Ge Ye
- Department of Gastroenterology, Nanjing Drum Tower Hospital Clinical College of Jiangsu University, Nanjing 210008, Jiangsu Province, China
| | - Ya-Nan Wang
- Department of Gastroenterology, Hospital Clinical College of Nanjing Medical University, Nanjing 210008, Jiangsu Province, China
| | - Qi Sun
- Department of Pathology, Affiliated Drum Tower Hospital of Nanjing University Medical School, Nanjing 210008, Jiangsu Province, China
| | - Xi-Wei Ding
- Department of Gastroenterology, Affiliated Drum Tower Hospital of Nanjing University Medical School, Nanjing 210008, Jiangsu Province, China
| | - Faraz Longi
- Feinberg School of Medicine, Northwestern University, Chicago, IL 60601, United States
| | - De-Hua Tang
- Department of Gastroenterology, Affiliated Drum Tower Hospital of Nanjing University Medical School, Nanjing 210008, Jiangsu Province, China
| | - Gui-Fang Xu
- Department of Gastroenterology, Nanjing Drum Tower Hospital Clinical College of Nanjing University of Chinese Medicine, Nanjing 210008, Jiangsu Province, China
- Department of Gastroenterology, Affiliated Drum Tower Hospital of Nanjing University Medical School, Nanjing 210008, Jiangsu Province, China
- Department of Gastroenterology, Hospital Clinical College of Nanjing Medical University, Nanjing 210008, Jiangsu Province, China
| |
Collapse
|
|
2
|
Joo DC, Kim GH. Optimal Surveillance of Metachronous Gastric Lesion after Endoscopic Resection of Early Gastric Cancer. Gut Liver 2024; 18:781-788. [PMID: 39114875 PMCID: PMC11391143 DOI: 10.5009/gnl240027] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 01/15/2024] [Revised: 02/29/2024] [Accepted: 03/14/2024] [Indexed: 09/13/2024] Open
Abstract
Endoscopic resection (ER)-a minimal invasive procedure, compared to surgical gastrectomy, with the advantage of preserving the entire stomach and maintaining the patient's quality of life-is a widely used curative treatment for early gastric cancers (EGCs). Despite its advantages, such as the preservation of the whole stomach, a large area of the gastric mucosa with histologic changes such as atrophy and intestinal metaplasia remains after ER, and so does the risk of metachronous gastric cancers (MGCs). Therefore, regular surveillance endoscopy after curative ER of EGCs is important so that MGCs are detected early and so minimally invasive ER remains a treatment option. To date, the optimal interval for surveillance endoscopy after curative ER of EGCs has not been established. Therefore, this review summarizes the results of the published studies on this topic with the aim of establishing the optimal surveillance interval for early identification of MGCs. Based on my review, the median timing of MGC occurrence is within 3 years, and reports suggest biannual endoscopy during the first 3 years; however, the evidence suggests that individual patient characteristics may influence the risk of MGCs. Therefore, stratified endoscopic strategies for surveillance based on patient characteristics, such as age, family history of gastric cancer, synchronous gastric lesions, and corpus intestinal metaplasia, should be applied.
Collapse
Affiliation(s)
- Dong Chan Joo
- Department of Internal Medicine, Pusan National University School of Medicine and Biomedical Research Institute, Pusan National University Hospital, Busan, Korea
| | - Gwang Ha Kim
- Department of Internal Medicine, Pusan National University School of Medicine and Biomedical Research Institute, Pusan National University Hospital, Busan, Korea
| |
Collapse
|
|
3
|
Yu TH, Bai D, Liu K, Zhang WH, Chen XZ, Hu JK. Helicobacter pylori eradication following endoscopic resection might prevent metachronous gastric cancer: a systematic review and meta-analysis of studies from Japan and Korea. Front Med (Lausanne) 2024; 11:1393498. [PMID: 39286646 PMCID: PMC11402824 DOI: 10.3389/fmed.2024.1393498] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/01/2024] [Accepted: 07/25/2024] [Indexed: 09/19/2024] Open
Abstract
Objectives A systematic review and meta-analysis was performed to evaluate the preventive effectiveness of Helicobacter pylori eradication against metachronous gastric cancer (MGC) or dysplasia following endoscopic resection (ER) for early gastric cancer (EGC) or dysplasia. Methods PubMed, Cochrane Library, MEDLINE, and EMBASE were searched until 31 October 2023, and randomized controlled trials or cohort studies were peer-reviewed. The incidence of metachronous gastric lesions (MGLs) including MGC or dysplasia was compared between Helicobacter pylori persistent and negative groups, eradicated and negative groups, and eradicated and persistent groups. Results Totally, 21 eligible studies including 82,256 observations were analyzed. Compared to those never infected, Helicobacter pylori persistent group (RR = 1.58, 95% CI = 0.98-2.53) trended to have a higher risk of MGLs and significantly in partial subgroups, while the post-ER eradicated group (RR = 0.79, 95% CI = 0.43-1.45) did not increase the risk of MGLs. Moreover, successful post-ER eradication could significantly decrease the risk of MGLs (RR = 0.54, 95% CI = 0.44-0.65) compared to those persistently infected. Sensitivity analysis obtained generally consistent results, and no significant publication bias was found. Conclusion The persistent Helicobacter pylori infection trends to increase the post-ER incidence of MGC or dysplasia, but post-ER eradication can decrease the risk correspondingly. Post-ER screening and eradication of Helicobacter pylori have preventive effectiveness on MGC, and the protocol should be recommended to all the post-ER patients.Systematic review registration: The PROSPERO registration identification was CRD42024512101.
Collapse
Affiliation(s)
- Tian-Hang Yu
- Gastric Cancer Center & Gastric Cancer Laboratory, Department of General Surgery, West China Hospital, Sichuan University, Chengdu, China
| | - Dan Bai
- Department of Day Surgery, General Practice Medical Center, West China Hospital, Sichuan University, Chengdu, China
| | - Kai Liu
- Gastric Cancer Center & Gastric Cancer Laboratory, Department of General Surgery, West China Hospital, Sichuan University, Chengdu, China
| | - Wei-Han Zhang
- Gastric Cancer Center & Gastric Cancer Laboratory, Department of General Surgery, West China Hospital, Sichuan University, Chengdu, China
| | - Xin-Zu Chen
- Gastric Cancer Center & Gastric Cancer Laboratory, Department of General Surgery, West China Hospital, Sichuan University, Chengdu, China
- Ya'an Cancer Prevention and Control Center, Ya'an People's Hospital - West China Ya'an Hospital, Sichuan University, Ya'an, China
- Ya'an Key Laboratory for High Altitude Medicine, Ya'an People's Hospital - West China Ya'an Hospital, Sichuan University, Ya'an, China
| | - Jian-Kun Hu
- Gastric Cancer Center & Gastric Cancer Laboratory, Department of General Surgery, West China Hospital, Sichuan University, Chengdu, China
| |
Collapse
|
|
4
|
Niu Z, Liang D, Guan C, Zheng Y, Meng C, Sun X, Liu Z. External validation of the FAMISH predicting score for early gastric cancer with endoscopic submucosal dissection. Eur J Gastroenterol Hepatol 2024; 36:26-32. [PMID: 37642661 DOI: 10.1097/meg.0000000000002635] [Citation(s) in RCA: 2] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 08/31/2023]
Abstract
OBJECTIVE To externally validate the robustness of the FAMISH predicting score designed to estimate the risk of metachronous gastric lesions (MGLs) after endoscopic submucosal dissection (ESD) for early gastric cancer (EGC). METHODS This multicenter, retrospective study included 618 patients with EGC who underwent curative ESD at two tertiary referral teaching hospitals between January 2014 and December 2019. FAMISH score was a composite indicator of age, sex, family history, corpus intestinal metaplasia, synchronous lesions, and H. pylori infection. Discrimination, calibration, and risk stratification of these scores were assessed. Associations between MGL characteristics and FAMISH scores were also explored. RESULTS After a median follow-up period of 60 months, 83 of 618 patients (13.4%) developed MGL. The discrimination ability according to the area under the curve was 0.708 (95% CI, 0.645-0.772) for predicting the 5-year MGL. The calibration results showed good consistency between the predicted and actual MGL (Hosmer-Lemeshow, P > 0.05). In terms of risk stratification, the 5-year MGL rates were 4.1% (95% CI, 1.6%-6.5%), 10.8% (95% CI, 7.2%-14.3%), and 32.1% (95% CI, 20.9%-41.7%) in the low-, intermediate-, and high-risk groups, respectively ( P < 0.001). For patients with MGL, the curative resection rate of ESD was significantly higher in the low- and intermediate-risk groups than in the high-risk group (100% vs. 80%, P = 0.037). CONCLUSION The FAMISH predicting score was externally validated and can be generalized to an independent patient population. This adjuvant tool can assist in individual clinical decision-making.
Collapse
Affiliation(s)
| | | | - Chaoyong Guan
- Department of Surgery and Anesthesiology, Xingtai Third Hospital
| | - Yang Zheng
- Department of Gastroenterology, Xingtai Third Hospital
| | | | - Xiaofang Sun
- Endoscopy Room, Xingtai People's Hospital, Xingtai, China
| | | |
Collapse
|
|
5
|
Metachronous gastric neoplasm beyond 5 years after endoscopic resection for early gastric cancer. Surg Endosc 2023; 37:3901-3910. [PMID: 36732489 DOI: 10.1007/s00464-023-09889-9] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/14/2022] [Accepted: 01/04/2023] [Indexed: 02/04/2023]
Abstract
BACKGROUND AND AIMS The natural course of early gastric cancer (EGC) following endoscopic submucosal dissection (ESD) remains unclear. This study aimed to clarify the long-term clinical outcomes and risk factors of metachronous gastric neoplasm (MGN) 5 years after ESD for EGC. METHODS We performed a retrospective analysis of patients who underwent ESD for EGC from July 2005 to October 2015 in Seoul National University Hospital. Long-term clinical outcomes and risk factors of MGN after 5 years post-ESD were evaluated. RESULTS Among the 2059 patients who underwent ESD for EGC, 1102 were followed up for > 5 years. MGN developed in 132 patients 5 years after ESD. During the median follow-up period of 85 months, the cumulative incidences of MGN and metachronous gastric cancer were 11.7, 16.9, and 27.0 and 7.6, 10.8, and 18.7% after 5, 7, and 10 years, respectively. In multivariable analysis, male sex (odds ratio 1.770; P = 0.042), severe intestinal metaplasia (odds ratio 1.255; P = 0.000), tumor-positive lateral margin (odds ratio 2.711; P = 0.008), < 5 mm lateral safety margin (odds ratio 1.568; P = 0.050), and synchronous adenoma (odds ratio 2.612; P = 0.001) were positive predictive factors, and successful eradication of Helicobacter pylori (odds ratio 0.514; P = 0.024) was a negative predictive factor for MGN after 5 years post-ESD. CONCLUSION The cumulative MGN incidence was high even 5 years post-ESD for EGC. Meticulous long-term endoscopic follow-up is mandatory, especially in male patients with underlying intestinal metaplasia, tumor-positive lateral margins, lateral safety margins of < 5 mm, and synchronous adenomas.
Collapse
|
|
6
|
Chiang TH, Cheng HC, Chuang SL, Chen YR, Hsu YH, Hsu TH, Lin LJ, Lin YW, Chu CH, Wu MS, Lee YC. Mass screening and eradication of Helicobacter pylori as the policy recommendations for gastric cancer prevention. J Formos Med Assoc 2022; 121:2378-2392. [PMID: 36085264 DOI: 10.1016/j.jfma.2022.08.012] [Citation(s) in RCA: 6] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/22/2022] [Revised: 08/17/2022] [Accepted: 08/17/2022] [Indexed: 11/18/2022]
Abstract
Gastric cancer is an inflammation-related cancer triggered by Helicobacter pylori infection. Understanding of the natural disease course has prompted the hypothesis that gastric cancer can be prevented by administering a short-course antibiotic treatment to eradicate the H. pylori infection and interrupt this carcinogenic cascade. Results from randomized controlled trials and cohort studies have repeatedly confirmed this concept, which has moved attention from individual management of H. pylori infection to population-wide implementation of screening programs. Such a paradigm shift follows a three-tier architecture. First, healthcare policy-makers determine the most feasible and applicable eligibility, invitation, testing, referral, treatment, and evaluation methods for an organized screening program to maximize the population benefits and cost-effectiveness. Second, provision of knowledge and effective feedback to frontline general practitioners, including choice of diagnostic tests, selection of eradication regimens, and the indication of endoscopic examination, ensures the quality of care and increases the likelihood of desired treatment responses. Third, initiatives to raise population awareness are designed regarding the impact of H. pylori infection and risky lifestyle habits on the stomach health. These programs, with increased accessibility and geographic coverage in progress, will accelerate the decline in morbidity, mortality, and associated costs of this preventable malignancy.
Collapse
Affiliation(s)
- Tsung-Hsien Chiang
- Department of Internal Medicine, College of Medicine, National Taiwan University, Taipei, Taiwan; Department of Integrated Diagnostics and Therapeutics, National Taiwan University Hospital, Taipei, Taiwan
| | - Hsiu-Chi Cheng
- Department of Internal Medicine, Institute of Clinical Medicine, Institute of Molecular Medicine, National Cheng Kung University Hospital, College of Medicine, National Cheng Kung University, Tainan, Taiwan; Department of Internal Medicine, Tainan Hospital, Ministry of Health and Welfare, Tainan, Taiwan
| | - Shu-Lin Chuang
- Department of Medical Research, National Taiwan University Hospital, Taipei, Taiwan
| | - Yi-Ru Chen
- Department of Internal Medicine, College of Medicine, National Taiwan University, Taipei, Taiwan
| | - Yu-Hsin Hsu
- Health Promotion Administration, Ministry of Health and Welfare, Taiwan
| | - Tsui-Hsia Hsu
- Health Promotion Administration, Ministry of Health and Welfare, Taiwan
| | - Li-Ju Lin
- Health Promotion Administration, Ministry of Health and Welfare, Taiwan
| | - Yu-Wen Lin
- Public Health Bureau, Taitung County, Taiwan
| | | | - Ming-Shiang Wu
- Department of Internal Medicine, College of Medicine, National Taiwan University, Taipei, Taiwan
| | - Yi-Chia Lee
- Department of Internal Medicine, College of Medicine, National Taiwan University, Taipei, Taiwan; Department of Medical Research, National Taiwan University Hospital, Taipei, Taiwan.
| |
Collapse
|
|
7
|
Karbalaei M, Keikha M. Statistical proof of Helicobacter pylori eradication in preventing metachronous gastric cancer after endoscopic resection in an East Asian population. World J Gastrointest Surg 2022; 14:867-873. [PMID: 36157362 PMCID: PMC9453324 DOI: 10.4240/wjgs.v14.i8.867] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/08/2022] [Revised: 05/29/2022] [Accepted: 07/27/2022] [Indexed: 02/07/2023] Open
Abstract
We conducted a comprehensive literature review and meta-analysis study on the efficacy of Helicobacter pylori (H. pylori) eradication in preventing metachronous gastric cancer after endoscopic resection among an East Asian population. Our results showed that the eradication of this pathogen significantly reduced the risk of susceptibility to metachronous gastric cancer in these patients. However, based on the available evidence, several factors such as increasing age, severe atrophy in the corpus and antrum, and intestinal metaplasia all may increase the risk of metachronous gastric cancer in H. pylori eradicated patients.
Collapse
Affiliation(s)
- Mohsen Karbalaei
- Department of Microbiology and Virology, School of Medicine, Jiroft University of Medical Sciences, Jiroft 78617-56447, Iran
| | - Masoud Keikha
- Department of Microbiology and Virology, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad 13131-99137, Iran
| |
Collapse
|
|
8
|
Pang X, Wang Y, Li L, Miao B, Fei S. Low serum pepsinogen II levels are closely linked with a risk of metabolic syndrome among healthy individuals with asymptomatic Helicobacter pylori infection: a cross-sectional study. Biomark Med 2022; 16:811-820. [PMID: 35642469 DOI: 10.2217/bmm-2022-0139] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/21/2022] Open
Abstract
Aim: Helicobacter pylori (Hp) infection has a connection with metabolic syndrome (MetS). Pepsinogen II (PGII) is a marker for gastric epithelial function. The present research was aimed at determining the associations among serum PGII levels, Hp infection and MetS in healthy subjects. Methods: This cross-sectional study enrolled 1242 healthy people, including 545 subjects with asymptomatic Hp infection and 697 subjects without Hp infection. Based on the number of MetS components present, subjects with Hp infection were assigned to the following groups: group 1, no component (126 subjects); group 2, one or two components (260 subjects); and group 3, three or more components (159 subjects). Physical measurements and biochemical indices were recorded. Serum PGII levels were recorded using ELISA. SPSS and GraphPad Prism were used for statistical analyses. Results: Among subjects with Hp infection, serum PGII was evidently downregulated in group 3 compared with group 1 (14.95 ± 8.24 vs 17.97 ± 9.08 μg/l; p = 0.015). Serum PGII levels were correlated with an increased risk of MetS (odds ratio: 0.867; 95% CI: 0.772-0.974; p = 0.016), as indicated by the multivariate logistic regression analysis. Grouping subjects with Hp infection according to quartiles of serum PGII levels identified an evident difference in MetS prevalence among the four quartile-based groups (p = 0.047). Conclusions: Among healthy subjects with asymptomatic Hp infection, serum PGII levels were lower in those with MetS than in those without MetS. Serum PGII levels showed an independent and negative correlation with the risk of MetS in healthy subjects with Hp infection.
Collapse
Affiliation(s)
- Xunlei Pang
- Department of Gastroenterology, the Affiliated Hospital of Xuzhou Medical University, Xuzhou, Jiangsu, 221004, PR China
| | - Yanhong Wang
- Department of Gastroenterology, the Affiliated Hospital of Xuzhou Medical University, Xuzhou, Jiangsu, 221004, PR China
| | - Li Li
- Department of Gastroenterology, the Affiliated Hospital of Xuzhou Medical University, Xuzhou, Jiangsu, 221004, PR China
| | - Bei Miao
- Department of Gastroenterology, the Affiliated Hospital of Xuzhou Medical University, Xuzhou, Jiangsu, 221004, PR China
| | - Sujuan Fei
- Department of Gastroenterology, the Affiliated Hospital of Xuzhou Medical University, Xuzhou, Jiangsu, 221004, PR China
| |
Collapse
|
|
9
|
Lee SY. Serum Assay Findings after Successful Helicobacter pylori Eradication. THE KOREAN JOURNAL OF HELICOBACTER AND UPPER GASTROINTESTINAL RESEARCH 2021. [DOI: 10.7704/kjhugr.2021.0031] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 11/22/2022]
Abstract
Serum pepsinogen (PG), anti-Helicobacter pylori (H. pylori) immunoglobulin G (IgG), and gastrin-17 (G-17) are plasma biomarkers for gastritis. H. pylori serology titers and PG levels increase during active H. pylori infection; moreover, elevated PG II levels indicate a high risk for diffuse-type gastric cancer in East Asian populations. Serum PG I/II ratios and PG I levels decrease with the progression of gastric corpus atrophy; thus, a combination of serum PG I levels ≤70 ng/mL and a PG I/II ratio ≤3 (serologic atrophy) indicates a high risk of intestinal-type gastric cancer. Serum G-17 is often not used as an indicator in H. pylori-seroprevalent populations because it is usually elevated in subjects with H. pylori infections. When H. pylori is eradicated, most patients show a rapid decrease in serum PG II levels and anti-H. pylori IgG titers within a few months. Seroreversion is required for several months to years after regression of H. pylori. Moreover, seroreversion may not always be achieved in all eradicated cases. The serum PG I/II ratio starts to increase after eradication; therefore, serologic atrophy improves accordingly, unless severe atrophy is present. Thus, some eradicated patients may show normal serum assay findings but have a higher risk for developing gastric cancer than H. pylori-naive subjects. Furthermore, serum PG levels decrease after gastrectomy and increase with the intake of certain drugs (e.g., aspirin or acid suppressants) or in renal failure patients. Due to such wide variations, serum assays are inadequate for the confirmation of H. pylori eradication. It is useful when interpreted with gastroscopy and other H. pylori test findings.
Collapse
|
|
10
|
Noh G, Kim N, Choi Y, Lee HS, Hwang YJ, Kim HJ, Yoon H, Shin CM, Park YS, Lee DH. Long-term follow up of serum pepsinogens in patients with gastric cancer or dysplasia after Helicobacter pylori eradication. J Gastroenterol Hepatol 2020; 35:1540-1548. [PMID: 32090375 DOI: 10.1111/jgh.15017] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 11/06/2019] [Revised: 01/12/2020] [Accepted: 02/21/2020] [Indexed: 12/14/2022]
Abstract
BACKGROUND AND AIM Few studies have evaluated the change in serum pepsinogen (sPG) levels after the eradication of Helicobacter pylori. The aim of this study was to evaluate the effect of H. pylori eradication on sPG levels in patients with gastric cancer/dysplasia in comparison to a control group. METHODS We prospectively enrolled 368 patients with gastric cancer/dysplasia and 610 control subjects. H. pylori status and sPG levels were measured before and after eradication. The follow-up time points were classified as < 12, 12-23, 24-35, and ≥ 36 months. RESULTS In 179 H. pylori-eradicated patients with gastric cancer/dysplasia and 168 control group subjects, sPG I significantly decreased, and the sPG I/II ratio significantly increased after eradication compared to baseline, and this improvement in sPG values was maintained during all follow-up time points. Significant differences in sPG I and the sPG I/II ratio were observed between the gastric cancer/dysplasia group and the control group < 24 months after eradication. However, these differences in sPG values disappeared after ≥ 24 months of follow up. Moreover, significant differences in the intestinal metaplasia grade were observed between these two groups before eradication until < 24 months after eradication. However, these differences in the intestinal metaplasia grade disappeared after ≥ 24 months of follow up in the corpus. CONCLUSION The sPG values and intestinal metaplasia grade (corpus) in the gastric cancer/dysplasia group became similar to those in the control group at long-term follow up after H. pylori eradication. It might be related with the reduction of metachronous gastric neoplasm.
Collapse
Affiliation(s)
- Gitark Noh
- Departments of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, South Korea
| | - Nayoung Kim
- Departments of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, South Korea.,Department of Internal Medicine and Liver Research Institute, Seoul National University, Seoul, South Korea.,Tumor Microenvironment Global Core Research Center, Seoul National University, Seoul, South Korea
| | - Yonghoon Choi
- Departments of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, South Korea
| | - Hye Seung Lee
- Departments of Pathology, Seoul National University Bundang Hospital, Seongnam, South Korea
| | - Young Jae Hwang
- Departments of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, South Korea
| | - Hee Jin Kim
- Department of Internal Medicine, Myongji Hospital, Goyang, South Korea
| | - Hyuk Yoon
- Departments of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, South Korea
| | - Cheol Min Shin
- Departments of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, South Korea
| | - Young Soo Park
- Departments of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, South Korea
| | - Dong Ho Lee
- Departments of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, South Korea.,Department of Internal Medicine and Liver Research Institute, Seoul National University, Seoul, South Korea.,Tumor Microenvironment Global Core Research Center, Seoul National University, Seoul, South Korea
| |
Collapse
|
|
11
|
De Marco MO, Tustumi F, Brunaldi VO, Resende RH, Matsubayashi CO, Baba ER, Chaves DM, Bernardo WM, de Moura EGH. Prognostic factors for ESD of early gastric cancers: a systematic review and meta-analysis. Endosc Int Open 2020; 8:E1144-E1155. [PMID: 32904802 PMCID: PMC7458740 DOI: 10.1055/a-1201-3089] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/18/2019] [Accepted: 02/12/2020] [Indexed: 02/06/2023] Open
Abstract
Background and study aims Gastric neoplasms are one of the leading types of cancer in the world and early detection is essential to improve prognosis. Endoscopy is the gold-standard diagnostic procedure and allows adequate treatment in selected cases. Endoscopic submucosal dissection (ESD) has been reported to safely address most early gastric cancers (EGCs), with high curability rates. However, data on prognostic factors related to ESDs of EGCs are conflicting. Therefore, we aimed to systematically review the available literature and to perform a meta-analysis to identify the relevant prognostic factors in this context. Methods We performed this study according to PRISMA guidelines. Comparative studies assessing the relationship between curative resection or long-term curability rates and relevant prognostic factors were selected. Prognostic factors were demographic data, lesion features (location, morphology of the lesion, size, and depth of invasion), histological findings, Helycobacter pylori (HP) infection, presence of gastric a atrophy and body mass index (BMI). Finally, we also evaluated risk factors related to metachronous gastric neoplasm. Results The initial search retrieved 2829 records among which 46 studies were included for systematic review and meta-analysis. The total sample comprised 28366 patients and 29282 lesions. Regarding curative resection, pooled data showed no significant influence of sex [odds ratio (OR): 1.15 (0,97, 1.36) P = 0.10 I 2 = 47 %] , age [OR: 1.00 (0.61, 1.64) P = 1.00 I 2 = 58 %], posterior vs non-posterior location [OR: 1.35 (0.81, 2.27) P = 0.25 I 2 = 84 %], depressed vs von-depressed macroscopic type[OR: 1.21 (0.99, 1.49) P = 0.07 I 2 = 0 %], non-upper vs upper location [OR: 1.41 (0.93, 2.14) P = 0.10 I 2 = 77 %] and BMI [OR: 0.84 (0.57; 1.26) P = 0.41 I 2 = 0 %]. Differentiated neoplasms presented greater chance of cure compare to undifferentiated [OR: 0.10 (0.07, 0.15) P < 0.00001 I 2 = 0 %]. Ulcerated lesions had lower curative rates compared to non-ulcerated [OR: 3.92 (2.81, 5.47) P < 0.00001 I 2 = 44 %]. Lesions smaller than 20 mm had greater chance of curative resection [OR: 3.94 (3.25, 4.78) P < 0.00001 I 2 = 38 %]. Bleeding during procedure had lower curative rates compared to non-bleeding [OR: 2.13 (1.56, 2.93) P < 0.0001 I 2 = 0 %]. Concerning long-term cure, female gender [OR 1.62 (1.33, 1.97) P < 0.00001 I 2 = 0 %] and the mucosal over SM1 cancers were protective factors [OR: 0.08 (0.02, 0.39) P = 0.002 I 2 = 86 %]. Gastric atrophy [OR: 0.60 (0.45, 0.81) P = 0.0006 I 2 = 42 %] and the pepsinogen I/pepsinogen II ratio [OR 2.29 (1.47, 3.57) P = 0.0002 I 2 = 0 %] were risk factors to metachronous gastric neoplasm. Conclusions Ulcerated lesions, histology, bleeding and size > 20 mm are prognostic factors concerning curative resection. Regarding long-term cure, female gender and mucosal over SM1 cancer are predictive factors. Gastric atrophy and the pepsinogen ratio are risk factors for metachronous gastric neoplasm.
Collapse
Affiliation(s)
- Michele Oliveira De Marco
- Gastrointestinal Endoscopy Unit, Gastroenterology Department, University of São Paulo Medical School, São Paulo, Brazil
| | - Francisco Tustumi
- Department of Gastroenterology, Digestive Surgery Division, Sao Paulo School of Medicine
| | - Vitor Ottoboni Brunaldi
- Gastrointestinal Endoscopy Unit, Gastroenterology Department, University of São Paulo Medical School, São Paulo, Brazil; Center for Gastrointestinal Endoscopy, Surgery and Anatomy Department, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, Brazil
| | - Ricardo Hannum Resende
- Gastrointestinal Endoscopy Unit, Gastroenterology Department, University of São Paulo Medical School, São Paulo, Brazil
| | - Carolina Ogawa Matsubayashi
- Gastrointestinal Endoscopy Unit, Gastroenterology Department, University of São Paulo Medical School, São Paulo, Brazil
| | - Elisa Ryoka Baba
- Gastrointestinal Endoscopy Unit, Gastroenterology Department, University of São Paulo Medical School, São Paulo, Brazil
| | - Dalton Marques Chaves
- Gastrointestinal Endoscopy Unit, Gastroenterology Department, University of São Paulo Medical School, São Paulo, Brazil
| | | | | |
Collapse
|
|
12
|
Cho JH, Jin SY. Optimized diagnosis of Helicobacter pylori and tailored eradication therapy for preventing gastric cancer: a proposal for SHAKE strategy. Expert Rev Gastroenterol Hepatol 2020; 14:553-564. [PMID: 32410515 DOI: 10.1080/17474124.2020.1770594] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/13/2022]
Abstract
INTRODUCTION To decrease gastric cancer-related mortality, the Korean National Cancer Screening Program provides biennial screening gastroscopy to all individuals aged >40 years. However, a test-and-treat strategy of Helicobacter pylori for preventing gastric cancer has not been established. AREAS COVERED In this review, we present up-to-date results of endoscopic findings of H. pylori gastritis, optimal sites for H. pylori detection, gastric cancer risk assessment using serum pepsinogen, tailored eradication based on the antimicrobial resistance against H. pylori, and post-eradication surveillance. EXPERT OPINION Here we propose approaches to H. pylori diagnosis and treatment for preventing gastric cancer, termed 'Screening for H. pylori in Korea and Eradication (SHAKE)' strategy. This strategy consists of the following: (1) optimized H. pylori diagnosis, (2) individualized management based on the H. pylori infection status, and (3) tailored eradication therapy. H. pylori gastritis can be diagnosed by endoscopic observation of the gastric mucosal pattern at the greater curvature of the corpus. Measurement of the serum pepsinogen I/II ratio is useful for assessing the risk of gastric cancer. As a first-line treatment, tailored eradication based on the results of molecular testing is effective in a country with a high rate of clarithromycin-resistant H. pylori.
Collapse
Affiliation(s)
- Jun-Hyung Cho
- Digestive Disease Center, Soonchunhyang University Hospital , Seoul, Korea
| | - So-Young Jin
- Department of Pathology, Soonchunhyang University Hospital , Seoul, Korea
| |
Collapse
|
|
13
|
Sugimoto M, Murata M, Yamaoka Y. Chemoprevention of gastric cancer development after Helicobacter pylori eradication therapy in an East Asian population: Meta-analysis. World J Gastroenterol 2020; 26:1820-1840. [PMID: 32351296 PMCID: PMC7183870 DOI: 10.3748/wjg.v26.i15.1820] [Citation(s) in RCA: 37] [Impact Index Per Article: 7.4] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/16/2019] [Revised: 03/05/2020] [Accepted: 03/31/2020] [Indexed: 02/06/2023] Open
Abstract
BACKGROUND Helicobacter pylori (H. pylori) infection is a risk factor for gastric cancer (GC), especially in East Asian populations. Most East Asian populations infected with H. pylori are at higher risk for GC than H. pylori-positive European and United States populations. H. pylori eradication therapy reduces gastric cancer risk in patients after endoscopic and operative resection for GC, as well as in non-GC patients with atrophic gastritis.
AIM To clarify the chemopreventive effects of H. pylori eradication therapy in an East Asian population with a high incidence of GC.
METHODS PubMed and the Cochrane library were searched for randomized control trials (RCTs) and cohort studies published in English up to March 2019. Subgroup analyses were conducted with regard to study designs (i.e., RCTs or cohort studies), country where the study was conducted (i.e., Japan, China, and South Korea), and observation periods (i.e., ≤ 5 years and > 5 years). The heterogeneity and publication bias were also measured.
RESULTS For non-GC patients with atrophic gastritis and patients after resection for GC, 4 and 4 RCTs and 12 and 18 cohort studies were included, respectively. In RCTs, the median incidence of GC for the untreated control groups and the treatment groups was 272.7 (180.4–322.4) and 162.3 (72.5–588.2) per 100000 person-years in non-GC cases with atrophic gastritis and 1790.7 (406.5–2941.2) and 1126.2 (678.7–1223.1) per 100000 person-years in cases of after resection for GC. Compared with non-treated H. pylori-positive controls, the eradication groups had a significantly reduced risk of GC, with a relative risk of 0.67 [95% confidence interval (CI): 0.47–0.96] for non-GC patients with atrophic gastritis and 0.51 (0.36–0.73) for patients after resection for GC in the RCTs, and 0.39 (0.30–0.51) for patients with gastritis and 0.54 (0.44–0.67) for patients after resection in cohort studies.
CONCLUSION In the East Asian population with a high risk of GC, H. pylori eradication effectively reduced the risk of GC, irrespective of past history of previous cancer.
Collapse
Affiliation(s)
- Mitsushige Sugimoto
- Department of Gastroenterological Endoscopy, Tokyo Medical University Hospital, Sinjuku, Tokyo 1600023, Japan
| | - Masaki Murata
- Department of Gastroenterology, National Hospital Organization Kyoto Medical Center, Kyoto 6128555, Japan
| | - Yoshio Yamaoka
- Department of Gastroenterology, Department of Environmental and Preventive Medicine, Oita University Faculty of Medicine, Yufu, Oita 8795593, Japan
| |
Collapse
|
|
14
|
Lee MW, Kim GH. Metachronous Gastric Cancer: Another Hurdle for Successful Endoscopic Treatment for Early Gastric Cancer? Gut Liver 2020; 14:145-147. [PMID: 32172548 PMCID: PMC7096229 DOI: 10.5009/gnl20018] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/11/2022] Open
Affiliation(s)
- Moon Won Lee
- Department of Internal Medicine, Pusan National University School of Medicine and Biomedical Research Institute, Pusan National University Hospital, Busan, Korea
| | - Gwang Ha Kim
- Department of Internal Medicine, Pusan National University School of Medicine and Biomedical Research Institute, Pusan National University Hospital, Busan, Korea
| |
Collapse
|
|
15
|
Fan F, Wang Z, Li B, Zhang H. Effects of eradicating Helicobacter pylori on metachronous gastric cancer prevention: A systematic review and meta-analysis. J Eval Clin Pract 2020; 26:308-315. [PMID: 31141285 DOI: 10.1111/jep.13179] [Citation(s) in RCA: 14] [Impact Index Per Article: 2.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 03/31/2019] [Revised: 04/22/2019] [Accepted: 04/24/2019] [Indexed: 12/24/2022]
Abstract
BACKGROUND Helicobacter pylori (H pylori) infection is closely associated with the incidence of gastric cancer. However, whether H pylori eradication prevents metachronous gastric cancer remains uncertain. The aim of our study is to assess how eradicating H pylori influences metachronous gastric cancer onset following treatment of early stage gastric cancer via endoscopic resective surgery. PATIENTS AND METHODS We performed a systematic review and meta-analysis by searching PubMed, Embase, Web of Science, and the Cochrane Library. Cohort studies and randomized controlled trials that compared individuals receiving H pylori eradication with individuals receiving placebo/nontreatment and evaluated the subsequent onset of metachronous gastric cancer as the main outcome were eligible for our study. Two authors reviewed articles and extracted data independently. Integrated results for all data were presented as risk ratio. RESULTS Thirteen studies containing 3863 patients were consistent with study inclusion criteria. Of the 2480 individuals in whom H pylori was successfully eradicated, 163 (6.57%) developed metachronous gastric cancer, as compared with 176 (12.73%) out of 1383 persistently infected individuals. The pooled risk ratio of metachronous gastric cancer for these studies was 0.46 (95% CI, 0.37-0.57, P < .001), providing support for the therapeutic elimination of H pylori. Subgroup analyses yielded similar results. CONCLUSION Eradicating H pylori via therapeutic treatment can effectively reduce rates of metachronous gastric cancer, and as such, it should be implemented in H pylori-infected individuals recently treated for early stage gastric cancers via endoscopic resection.
Collapse
Affiliation(s)
- Fangfang Fan
- Center for Sleep and Circadian Neurobiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania
| | - Zhe Wang
- School of Basic Medical Sciences, Xi'an Jiaotong University, Xi'an, Shaanxi, China
| | - Bing Li
- Department of Laboratory Medicine, ShenZhen AladdinMed LLC, Shenzhen, China
| | - Hongtao Zhang
- Department of Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, Pennsylvania
| |
Collapse
|
|
16
|
Cho JH, Jeon SR, Jin SY, Park S. Analysis of factors associated with recovery of the serum pepsinogen ratio after Helicobacter pylori eradication: a long-term follow-up study in Korea. Scand J Gastroenterol 2019; 54:1306-1314. [PMID: 31702966 DOI: 10.1080/00365521.2019.1686058] [Citation(s) in RCA: 8] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 02/06/2023]
Abstract
Objective: Serum levels of pepsinogen (PG) are related to Helicobacter pylori-induced inflammation of the gastric mucosa. This study aimed to examine the influence of H. pylori eradication on serum PG, analyze its associated factors, and evaluate the long-term outcomes.Methods: H. pylori-positive patients who underwent gastroscopy and serum PG measurement were enrolled in a single academic hospital. After H. pylori eradication, the measurement of serum PG level was performed. Recovery of serum PG I/II ratio was defined as a PG I/II ratio after eradication of >3.0 in patients with a PG I/II ratio ≤ 3.0 before eradication. Follow-up involved serum PG measurement and gastroscopy with a rapid urease test annually.Results: In all, 327 patients were eligible for study inclusion. Compared to those before H. pylori eradication, serum PG I (74.9 vs. 44.3 ng/mL, p < .001) and PG II (25.4 vs. 9.1 ng/mL, p < .001) levels significantly decreased after successful eradication. In addition, there was a significant increase in serum PG I/II ratio after eradication (3.07 vs. 4.98, p < .001). In multivariate analyses, the following were independently associated with failed recovery of serum PG I/II ratio despite successful eradication: age ≥ 60 years (odds ratio [OR] = 0.231, 95% confidence interval [CI] = 0.084-0.629, p = .004) and severe gastric atrophy (OR = 0.156, 95% CI = 0.055-0.440, p < .001).Conclusions: Recovery of serum PG I/II ratio after H. pylori eradication may be achieved in H. pylori-infected patients aged <60 years without severe gastric atrophy.
Collapse
Affiliation(s)
- Jun-Hyung Cho
- Digestive Disease Center, Soonchunhyang University Hospital, Seoul, Korea
| | - Seong Ran Jeon
- Digestive Disease Center, Soonchunhyang University Hospital, Seoul, Korea
| | - So-Young Jin
- Department of Pathology, Soonchunhyang University Hospital, Seoul, Korea
| | - Suyeon Park
- Department of Medical Biostatistics, Soonchunhyang University Hospital, Seoul, Korea
| |
Collapse
|
|
17
|
Xiao S, Li S, Zhou L, Jiang W, Liu J. Helicobacter pylori status and risks of metachronous recurrence after endoscopic resection of early gastric cancer: a systematic review and meta-analysis. J Gastroenterol 2019; 54:226-237. [PMID: 30251121 DOI: 10.1007/s00535-018-1513-8] [Citation(s) in RCA: 31] [Impact Index Per Article: 5.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/27/2018] [Accepted: 09/13/2018] [Indexed: 02/07/2023]
Abstract
The impact of different Helicobacter pylori (H. pylori) status (H. pylori negative, H. pylori eradication and H. pylori persistence) on the development of metachronous gastric lesions after endoscopic resection of early gastric cancer is not well defined. Thus, a systematic review and meta-analysis was performed to investigate this relationship. Two authors independently searched the electronic databases (Pubmed, Embase, the Cochrane Library and Web of Science) through March 2018, without language restriction. Pooled risk ratio for metachronous gastric lesions with regard to H. pylori status was calculated using fixed- or random-effects models, and heterogeneity and publication bias were also measured. 20 eligible studies were finally identified in systematic review, and 17 out of 20 studies were further included in meta-analysis. H. pylori eradication was associated with overall 50% lower odds of metachronous events (RR = 0.50; 95 % CI 0.41-0.61). Pooled risk ratios for metachronous gastric neoplasm were 0.85 (95 % CI 0.43-1.68) between H. pylori-eradicated and -negative patients, and 0.63 (95 % CI 0.35-1.12) between H. pylori-negative and -persistent patients, respectively. In conclusion, based on the best available evidence, eradication of H. pylori can provide protection against secondary gastric neoplasm, and this quantitative benefit seemed greater than among asymptomatic individuals. Metachronous risk seems comparable between H. pylori-eradicated and -negative population, or between H. pylori-negative and -persistent patients.
Collapse
Affiliation(s)
- Shiyu Xiao
- Department of Gastroenterology, Peking University Third Hospital, 49 North Garden Road, Haidian District, Beijing, 100191, China
| | - Sizhu Li
- Department of Gastroenterology, Peking University Third Hospital, 49 North Garden Road, Haidian District, Beijing, 100191, China
| | - Liya Zhou
- Department of Gastroenterology, Peking University Third Hospital, 49 North Garden Road, Haidian District, Beijing, 100191, China.
| | - Wenjun Jiang
- Department of Gastroenterology, Peking University Third Hospital, 49 North Garden Road, Haidian District, Beijing, 100191, China
| | - Jinzhe Liu
- Department of Gastroenterology, Peking University Third Hospital, 49 North Garden Road, Haidian District, Beijing, 100191, China
| |
Collapse
|
|
18
|
Abstract
Serum pepsinogen can reflect the functional status of the gastric mucosa. The pathological changes of the gastric mucosa include chronic gastritis, gastric ulcer, atrophic gastritis, and gastric cancer, and the relationship between serum pepsinogen and gastric cancer/atrophic gastritis is the most prominent. Since the detection of serum pepsinogen is simple, inexpensive, time-saving, highly sensitive, and highly specific, it has attracted great attention from scholars and is regarded as "serological biopsy". In this paper, we discuss the value of serum pepsinogen in the diagnosis of gastric diseases.
Collapse
Affiliation(s)
- Jian Gan
- Department of Gastroenterology, Heji Hospital Affiliated to Changzhi Medical College, Changzhi 046000, Shanxi Province, China
| | - Rong-Gui Cheng
- Department of Gastroenterology, Heji Hospital Affiliated to Changzhi Medical College, Changzhi 046000, Shanxi Province, China
| | - Shao-Feng Wang
- Department of Gastroenterology, Changzhi People's Hospital, Changzhi 046000, Shanxi Province, China
| |
Collapse
|
|
19
|
Kwon Y, Jeon S. Editorial: risk stratification for endoscopic surveillance of metachronous gastric cancer after endoscopic resection-Authors' reply. Aliment Pharmacol Ther 2017; 46:1015-1016. [PMID: 29052851 DOI: 10.1111/apt.14363] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/08/2022]
Affiliation(s)
- Y Kwon
- Department of Internal Medicine, Kyungpook National University School of Medicine, Daegu, Korea
| | - S Jeon
- Department of Internal Medicine, Kyungpook National University School of Medicine, Daegu, Korea
| |
Collapse
|
|
20
|
Fock KM, Ang TL. Editorial: risk stratification for endoscopic surveillance of metachronous gastric cancer after endoscopic resection. Aliment Pharmacol Ther 2017; 46:1014-1015. [PMID: 29052852 DOI: 10.1111/apt.14322] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.1] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/15/2022]
Affiliation(s)
- K M Fock
- Department of Gastroenterology and Hepatology, Changi General Hospital, Singapore
| | - T L Ang
- Department of Gastroenterology and Hepatology, Changi General Hospital, Singapore
| |
Collapse
|