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Peng YH, Feng X, Zhou Z, Yang L, Shi YF. Helicobacter pylori infection in Xinjiang Uyghur Autonomous Region: Prevalence and analysis of related factors. World J Gastroenterol 2023; 29:5834-5847. [PMID: 38074913 PMCID: PMC10701308 DOI: 10.3748/wjg.v29.i43.5834] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 08/19/2023] [Revised: 10/10/2023] [Accepted: 10/29/2023] [Indexed: 11/20/2023] Open
Abstract
BACKGROUND 14C urea breath test (14C UBT) and immunohistochemical staining (IHC) are widely used for detection Helicobacter pylori (H. pylori) infection with different sensitivity, and there is a difference in H. pylori infection rate in Uyghur and Han ethnic groups. Both need large cohort studies to evaluate the differences more accurately. AIM To analyze the difference between 14C UBT and IHC for H. pylori detection in Xinjiang Uyghur Autonomous Region and the difference between Uyghur and Han populations. METHODS There were 3944 cases of H. pylori infection detected by both IHC and 14C UBT at the same time (interval < 1 wk, with sampling site including gastric antrum, selected from 5747 patients). We compared the sensitivity of 14C UBT and IHC. We also compared 555 pairs of Han/Uyghur cases (completely matched for gender and age) for their H. pylori infection rates. The overall H. pylori infection rate of all 5747 cases and the correlation with other clinicopathological data were also further analyzed. SPSS V23.0 software was used for statistical analysis. RESULTS The sensitivity was 94.9% for 14C UBT and 65.1% for IHC, which was a significant difference (n = 3944, P < 0.001). However, among those cases negative for H. pylori by 14C UBT (detection value ≤ 100), 4.8% were positive by IHC. Combining both methods, the overall H. pylori infection rate was 48.6% (n = 5747), and differences in gender, age group, ethnicity and region of residence significantly affected the H. pylori positive rates. According to age group (Han/Uyghur), the positive rates were ≤ 30 years (62.2%/100.0%), 31-40 years (45.2%/85.7%), 41-50 years (47.2%/79.2%), 51-60 years (44.6%/76.1%), 61-70 years (40.9%/68.2%), 71-80 years (41.7%/54.1%) and ≥ 81 years (42.9%/NA). The H. pylori infection rates of Han/Uyghur paired cases were 41.4% and 73.3%, which was a significant difference (P < 0.001) (555 pairs). H. pylori positivity was significantly related to moderate-severe grade 2-3 chronic/active gastritis and intestinal metaplasia (all P < 0.05). CONCLUSION The sensitivity of 14C UBT was significantly higher, but combined application can still increase the accuracy. The prevention H. pylori should be emphasized for Uygur and young people.
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Affiliation(s)
- Yu-Hua Peng
- Department of Pathology, Traditional Chinese Medical Hospital of Xinjiang Uygur Autonomous Region, The Affiliated Hospital of Traditional Chinese Medicine of Xinjiang Medical University, Urumqi 830000, Xinjiang Uygur Autonomous Region, China
| | - Xue Feng
- Department of Laboratory Medicine, Traditional Chinese Medical Hospital of Xinjiang Uygur Autonomous Region, The Affiliated Hospital of Traditional Chinese Medicine of Xinjiang Medical University, Urumqi 830000, Xinjiang Uygur Autonomous Region, China
| | - Zhong Zhou
- Department of Pathology, Traditional Chinese Medical Hospital of Xinjiang Uygur Autonomous Region, The Affiliated Hospital of Traditional Chinese Medicine of Xinjiang Medical University, Urumqi 830000, Xinjiang Uygur Autonomous Region, China
| | - Lei Yang
- Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Beijing Office for Cancer Prevention and Control, Peking University Cancer Hospital & Institute, Beijing 100142, China
| | - Yun-Fei Shi
- Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Department of Pathology, Peking University Cancer Hospital & Institute, Beijing 100142, China
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Risk assessment of metachronous gastric cancer development using OLGA and OLGIM systems after endoscopic submucosal dissection for early gastric cancer: a long-term follow-up study. Gastric Cancer 2023; 26:298-306. [PMID: 36609936 DOI: 10.1007/s10120-022-01361-2] [Citation(s) in RCA: 11] [Impact Index Per Article: 5.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 10/04/2022] [Accepted: 12/27/2022] [Indexed: 01/09/2023]
Abstract
BACKGROUND Metachronous gastric cancer (MGC) may develop in patients undergoing curative endoscopic submucosal dissection for early gastric cancer. As gastritis and intestinal metaplasia are notable precursors to gastric cancer, we assessed MGC risk using the Operative Link on Gastritis Assessment (OLGA) and Operative Link on Gastric Intestinal Metaplasia assessment (OLGIM) systems. METHODS This retrospective cohort study classified the OLGA and OLGIM stages for 916 patients who had undergone endoscopic submucosal dissection for early gastric cancer between 2005 and 2015. MGC development was followed up until 2020 and risk factors were evaluated using the Cox proportional hazards regression analysis. RESULTS During a median follow-up of 94 months, MGC developed in 120 subjects. OLGA stages II ~ IV were significantly associated with increased MGC risk (hazard ratio [HR] 1.83, 95% confidence interval [CI] 1.05-3.19; HR 2.31, 95% CI 1.22-4.38; HR 2.36, 95% CI 1.16-4.78) in multivariable analysis, even after adjusting for the well-known positive predictor of Helicobacter pylori eradication. OLGIM stages II ~ IV also showed significant association (HR 2.86, 95% CI 1.29-6.54; HR 2.94, 95% CI 1.34-6.95; HR 3.64, 95% CI 1.60-8.29). 5-year cumulative incidence increased with each stage. Helicobacter pylori-eradicated patients with OLGIM stages 0 ~ II had significantly less MGC than non-eradicated patients (4.5% vs 11.8%, p = 0.022), which was not observed with OLGIM stages III ~ IV. CONCLUSIONS High OLGA and OLGIM stages are independent risk factors for metachronous gastric cancer, with the OLGIM staging system being a better predictor. Patients with OLGIM stages 0 ~ II are a subgroup that may benefit more from Helicobacter pylori eradication.
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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.
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A Castaneda C, Castillo M, Sanchez J, Casavilca S, Sanchez J, A Bernabe L, Suarez N, Chavez I, Ruiz E, Tello K, R Villa M, Zevallos R, Montenegro P, Dias-Neto E, Landa-Baella M, Taxa L. Detection of Helicobacter pylori in gastric cancer tissue through histopathology, immunohistochemistry and real-time reverse transcription-PCR. Future Microbiol 2020; 15:1131-1137. [PMID: 32954850 DOI: 10.2217/fmb-2019-0280] [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 is usually detected based on hematoxylin-eosin (H-E) features, but, immunohistochemistry (IHC) and real-time PCR (RT-PCR) are more precise in chronic-gastritis. We evaluated the relevance of these tests in Peruvian gastric cancer samples. Materials & methods: We performed and evaluated H-E, IHC staining and RT-PCR in 288 gastric tumors. Slides were independently evaluated by three pathologists. Results: H. pylori was detected in 167/287 through H-E, 140/288 through IHC and 175/288 through RT-PCR, and positive-status were associated (p < 0.001). H. pylori detection by H-E had a good concordance with IHC (kappa index = 0.632) but poor with RT-PCR (kappa index = 0.317). Higher median gene-copies were found in high H. pylori density through H-E or IHC (p < 0.001). Conclusion: H-E evaluation is accurate in gastric cancer, and IHC and RT-PCR can complement its results.
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Affiliation(s)
- Carlos A Castaneda
- Departamento de Oncología Médica, Instituto Nacional de Enfermedades Neoplásicas, Lima 15038, Peru.,Facultad de Ciencias de la Salud, Universidad Científica del Sur, Lima 15067, Peru
| | - Miluska Castillo
- Departamento de Investigación, Instituto Nacional de Enfermedades Neoplásicas, Lima 15038, Peru
| | - Joselyn Sanchez
- Departamento de Investigación, Instituto Nacional de Enfermedades Neoplásicas, Lima 15038, Peru
| | - Sandro Casavilca
- Departamento de Patología, Instituto Nacional de Enfermedades Neoplásicas, Lima 15038, Peru
| | - Juvenal Sanchez
- Departamento de Patología, Instituto Nacional de Enfermedades Neoplásicas, Lima 15038, Peru
| | - Luis A Bernabe
- Departamento de Investigación, Instituto Nacional de Enfermedades Neoplásicas, Lima 15038, Peru
| | - Nancy Suarez
- Departamento de Investigación, Instituto Nacional de Enfermedades Neoplásicas, Lima 15038, Peru
| | - Ivan Chavez
- Departamento de Abdomen, Instituto Nacional de Enfermedades Neoplásicas, Lima 15038, Peru
| | - Eloy Ruiz
- Departamento de Abdomen, Instituto Nacional de Enfermedades Neoplásicas, Lima 15038, Peru
| | - Katherine Tello
- Departamento de Investigación, Instituto Nacional de Enfermedades Neoplásicas, Lima 15038, Peru
| | - Maria R Villa
- Departamento de Patología, Instituto Nacional de Enfermedades Neoplásicas, Lima 15038, Peru
| | - Rocio Zevallos
- Departamento de Patología, Instituto Nacional de Enfermedades Neoplásicas, Lima 15038, Peru
| | - Paola Montenegro
- Departamento de Oncología Médica, Instituto Nacional de Enfermedades Neoplásicas, Lima 15038, Peru
| | - Emmanuel Dias-Neto
- Laboratory of Medical Genomics, CIPE, A.C. Camargo Cancer Center, São Paulo 04002-010, Brasil
| | - Maria Landa-Baella
- Departamento de Investigación, Instituto Nacional de Enfermedades Neoplásicas, Lima 15038, Peru
| | - Luis Taxa
- Departamento de Patología, Instituto Nacional de Enfermedades Neoplásicas, Lima 15038, Peru
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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.
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Affiliation(s)
- Jun-Hyung Cho
- Digestive Disease Center, Soonchunhyang University Hospital , Seoul, Korea
| | - So-Young Jin
- Department of Pathology, Soonchunhyang University Hospital , Seoul, Korea
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Huh CW, Kim BW. [Diagnosis of Helicobacter pylori Infection]. THE KOREAN JOURNAL OF GASTROENTEROLOGY = TAEHAN SOHWAGI HAKHOE CHI 2018; 72:229-236. [PMID: 30642138 DOI: 10.4166/kjg.2018.72.5.229] [Citation(s) in RCA: 16] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 09/09/2018] [Revised: 09/17/2018] [Accepted: 09/17/2018] [Indexed: 09/22/2023]
Abstract
Accurate diagnosis of Helicobacter pylori (H. pylori) infection is mandatory for the effective management of many gastroduodenal diseases. Currently, various diagnostic methods are available for detecting these infections, and the choice of method should take into account the clinical condition, accessibility, advantage, disadvantage, as well as cost-effectiveness. The diagnostic methods are divided into invasive (endoscopic-based) and non-invasive methods. Non-invasive methods included urea breath test, stool antigen test, serology, and molecular methods. Invasive methods included endoscopic imaging, rapid urease test, histology, culture, and molecular methods. In this article, we provide a review of the currently available options and recent advances of various diagnostic methods.
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Affiliation(s)
- Cheal Wung Huh
- Division of Gastroenterology, Department of Internal Medicine, Incheon St. Mary's Hospital, College of Medicine, The Catholic University of Korea, Seoul, Korea
| | - Byung-Wook Kim
- Division of Gastroenterology, Department of Internal Medicine, Incheon St. Mary's Hospital, College of Medicine, The Catholic University of Korea, Seoul, Korea
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Sabbagh P, Mohammadnia-Afrouzi M, Javanian M, Babazadeh A, Koppolu V, Vasigala VR, Nouri HR, Ebrahimpour S. Diagnostic methods for Helicobacter pylori infection: ideals, options, and limitations. Eur J Clin Microbiol Infect Dis 2018; 38:55-66. [PMID: 30414090 DOI: 10.1007/s10096-018-3414-4] [Citation(s) in RCA: 92] [Impact Index Per Article: 13.1] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/10/2018] [Accepted: 10/26/2018] [Indexed: 12/13/2022]
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Kim YI, Kook MC, Cho SJ, Lee JY, Kim CG, Joo J, Choi IJ. Effect of biopsy site on detection of gastric cancer high-risk groups by OLGA and OLGIM stages. Helicobacter 2017; 22. [PMID: 28940945 DOI: 10.1111/hel.12442] [Citation(s) in RCA: 16] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 02/06/2023]
Abstract
BACKGROUND/AIMS The operative link for gastritis assessment (OLGA) and operative link on gastric intestinal metaplasia assessment (OLGIM) staging systems are recommended to assess the severity of gastritis, but the optimal biopsy sites have not been clearly defined. We aimed to investigate whether the scoring of the OLGA and OLGIM stages was affected by the use of different biopsy sites. METHODS Between 2014 and 2015, to determine OLGA and OLGIM stages, seven biopsy samples were obtained from the antrum (lesser and greater curvatures [LG] of the antrum and lesser curvature of the angle) and corpus (LG and anterior and posterior walls [AP]) in 247 patients diagnosed with gastritis, gastric adenoma, or adenocarcinoma. The OLGA and OLGIM stages were scored using four different protocols: antrum + angle + corpus LG, antrum + angle + corpus AP, antrum + corpus LG, and antrum + corpus AP. High-risk group included patients who had OLGA or OLGIM stages III and IV. RESULTS For the OLGA stage, the angle + antrum + corpus LG protocol placed more patients in the high-risk group (64.4%) than the angle + antrum + corpus AP (55.5%, P < .001), antrum+corpus LG (59.5%, P = .031), and antrum + corpus AP (47.8%, P < .001) protocols. Likewise, for the OLGIM stage, the angle + antrum + corpus LG protocol placed more patients in the high-risk group (48.6%) than the angle + antrum + corpus AP (46.2%, P = .134), antrum + corpus LG (36.8%, P < .001), and antrum + corpus AP (37.2%, P < .001) protocols. CONCLUSIONS To prevent underestimation of OLGA and OLGIM stages, it is necessary to include an angle biopsy, and to obtain corpus biopsy specimens from lesser and greater curvature sites rather than from anterior and posterior wall sites.
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Affiliation(s)
- Young-Il Kim
- Center for Gastric Cancer, National Cancer Center, Goyang, Korea
| | | | - Soo-Jeong Cho
- Center for Gastric Cancer, National Cancer Center, Goyang, Korea
| | - Jong Yeul Lee
- Center for Gastric Cancer, National Cancer Center, Goyang, Korea
| | - Chan Gyoo Kim
- Center for Gastric Cancer, National Cancer Center, Goyang, Korea
| | - Jungnam Joo
- Biometric Research Branch, Research Institute and Hospital, National Cancer Center, Goyang, Korea
| | - Il Ju Choi
- Center for Gastric Cancer, National Cancer Center, Goyang, Korea
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Cho JH, Jeon SR, Kim HG, Jin SY, Park S. Factors for improving the diagnostic efficiency of the rapid urease test from the gastric corpus. Scand J Gastroenterol 2017; 52:1320-1325. [PMID: 28927301 DOI: 10.1080/00365521.2017.1378712] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.1] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 02/04/2023]
Abstract
OBJECTIVE This study aimed to evaluate the optimal biopsy site for Helicobacter pylori detection by comparing the results of rapid urease test (RUT) between the gastric corpus and the antrum. METHODS A biopsy specimen from each subject was obtained from the corpus and from the antrum. For each subject, the two specimens were separately immersed in two different RUT kits. Positive reaction times were measured at 20 minutes and 1, 3, and 24 hours. If either of the two RUT kits showed a positive reaction, H. pylori infection was confirmed. RESULTS A total of 310 H. pylori-infected subjects were eligible for study inclusion. Compared with the antrum, positive RUT reaction times in the corpus were shorter when the degree of gastric atrophy was moderate or severe (p = .001 and p < .001, respectively). A multivariate analysis revealed that the factors resulting in a faster positive RUT reaction in the corpus were age ≥50 years (odds ratio [OR] = 1.84; 95% confidence interval [CI] = 1.10-3.08; p = .021) and severe gastric atrophy (OR = 2.41; 95% CI = 1.13-5.13; p = .023). Also, severe gastric atrophy was an independent factor associated with positive RUT reaction only in the corpus (OR = 5.12; 95% CI = 1.55-16.88; p = .007). CONCLUSIONS In subjects aged ≥50 years or with severe gastric atrophy, biopsy of the corpus mucosa optimized the efficiency of H. pylori detection through a faster positive RUT reaction.
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Affiliation(s)
- Jun-Hyung Cho
- a Digestive Disease Center , Soonchunhyang University Hospital , Seoul , Korea
| | - Seong Ran Jeon
- a Digestive Disease Center , Soonchunhyang University Hospital , Seoul , Korea
| | - Hyun Gun Kim
- a Digestive Disease Center , Soonchunhyang University Hospital , Seoul , Korea
| | - So-Young Jin
- b Department of Pathology , Soonchunhyang University Hospital , Seoul , Korea
| | - Suyeon Park
- c Department of Medical Biostatistics , Soonchunhyang University Hospital , Seoul , Korea
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Wang YK, Kuo FC, Liu CJ, Wu MC, Shih HY, Wang SSW, Wu JY, Kuo CH, Huang YK, Wu DC. Diagnosis of Helicobacter pylori infection: Current options and developments. World J Gastroenterol 2016. [PMID: 26523098 DOI: 10.3748/wjg.v21.i40.11221.] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.1] [Reference Citation Analysis] [Abstract] [Key Words] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 10/11/2022] Open
Abstract
Accurate diagnosis of Helicobacter pylori (H. pylori) infection is a crucial part in the effective management of many gastroduodenal diseases. Several invasive and non-invasive diagnostic tests are available for the detection of H. pylori and each test has its usefulness and limitations in different clinical situations. Although none can be considered as a single gold standard in clinical practice, several techniques have been developed to give the more reliable results. Invasive tests are performed via endoscopic biopsy specimens and these tests include histology, culture, rapid urease test as well as molecular methods. Developments of endoscopic equipment also contribute to the real-time diagnosis of H. pylori during endoscopy. Urea breathing test and stool antigen test are most widely used non-invasive tests, whereas serology is useful in screening and epidemiological studies. Molecular methods have been used in variable specimens other than gastric mucosa. More than detection of H. pylori infection, several tests are introduced into the evaluation of virulence factors and antibiotic sensitivity of H. pylori, as well as screening precancerous lesions and gastric cancer. The aim of this article is to review the current options and novel developments of diagnostic tests and their applications in different clinical conditions or for specific purposes.
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Affiliation(s)
- Yao-Kuang Wang
- Yao-Kuang Wang, Department of Internal Medicine, Kaohsiung Municipal Hsiao-Kang Hospital, Kaohsiung 812, Taiwan
| | - Fu-Chen Kuo
- Yao-Kuang Wang, Department of Internal Medicine, Kaohsiung Municipal Hsiao-Kang Hospital, Kaohsiung 812, Taiwan
| | - Chung-Jung Liu
- Yao-Kuang Wang, Department of Internal Medicine, Kaohsiung Municipal Hsiao-Kang Hospital, Kaohsiung 812, Taiwan
| | - Meng-Chieh Wu
- Yao-Kuang Wang, Department of Internal Medicine, Kaohsiung Municipal Hsiao-Kang Hospital, Kaohsiung 812, Taiwan
| | - Hsiang-Yao Shih
- Yao-Kuang Wang, Department of Internal Medicine, Kaohsiung Municipal Hsiao-Kang Hospital, Kaohsiung 812, Taiwan
| | - Sophie S W Wang
- Yao-Kuang Wang, Department of Internal Medicine, Kaohsiung Municipal Hsiao-Kang Hospital, Kaohsiung 812, Taiwan
| | - Jeng-Yih Wu
- Yao-Kuang Wang, Department of Internal Medicine, Kaohsiung Municipal Hsiao-Kang Hospital, Kaohsiung 812, Taiwan
| | - Chao-Hung Kuo
- Yao-Kuang Wang, Department of Internal Medicine, Kaohsiung Municipal Hsiao-Kang Hospital, Kaohsiung 812, Taiwan
| | - Yao-Kang Huang
- Yao-Kuang Wang, Department of Internal Medicine, Kaohsiung Municipal Hsiao-Kang Hospital, Kaohsiung 812, Taiwan
| | - Deng-Chyang Wu
- Yao-Kuang Wang, Department of Internal Medicine, Kaohsiung Municipal Hsiao-Kang Hospital, Kaohsiung 812, Taiwan
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Eun Bae S, Hoon Lee J, Soo Park Y, Ok Kim S, Young Choi J, Yong Ahn J, Hoon Kim D, Don Choi K, June Song H, Hyug Lee G, Choe J, Jin Jang S, Jung HY. Decrease of serum total ghrelin in extensive atrophic gastritis: comparison with pepsinogens in histological reference. Scand J Gastroenterol 2016; 51:137-44. [PMID: 26513345 DOI: 10.3109/00365521.2015.1083049] [Citation(s) in RCA: 11] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 02/04/2023]
Abstract
OBJECTIVE Ghrelin is mainly secreted by the gastric oxyntic mucosa and its production is impaired in chronic atrophic gastritis. This study aimed at evaluating how serum total ghrelin correlates with the extent of atrophy, and to compare its performance as a serologic marker with that of pepsinogen (PG). MATERIAL AND METHODS Data were collected from 154 patients with atrophic gastritis. The histological extent of atrophy was assessed by three paired biopsies from the antrum, corpus lesser curvature (CLC), and corpus greater curvature (CGC). Fasting serum concentrations of total ghrelin, pepsinogen I and II were measured. Regression analysis was performed to evaluate the factors associated with serum total ghrelin. The serologic performance was compared with that of pepsinogen using receiver-operating characteristic (ROC) curves. RESULTS The Helicobacter pylori infection rate was 85%, and extensive atrophic gastritis involving CGC was found in 24%. Serum total ghrelin was significantly decreased in patients with extensive CGC atrophy (median: 170.4 pg/mL, vs 201.1 pg/mL in patients without atrophy; p < 0.001), and its levels correlated with those of pepsinogen I and I/II ratio. The decrease of serum total ghrelin was independent of age, gender, body mass index (BMI), and H. pylori infection status. The sensitivity and specificity of serum total ghrelin in predicting extensive atrophy were 57% and 79%, respectively. The discriminatory ability was similar to that of pepsinogen I/II ratio (p = 0.612), and lower than that of pepsinogen I (p = 0.040). CONCLUSIONS Serum total ghrelin is decreased during extensive atrophy involving CGC. The serologic performance is lower than that of pepsinogen I.
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Affiliation(s)
- Suh Eun Bae
- a Health Screening and Promotion Center , University of Ulsan College of Medicine, Asan Medical Center , Seoul , South Korea
| | | | | | - Seon Ok Kim
- d Department of Clinical Epidemiology and Biostatistics , University of Ulsan College of Medicine, Asan Medical Center , Seoul , South Korea
| | - Ji Young Choi
- a Health Screening and Promotion Center , University of Ulsan College of Medicine, Asan Medical Center , Seoul , South Korea
| | | | | | | | | | | | - Jaewon Choe
- a Health Screening and Promotion Center , University of Ulsan College of Medicine, Asan Medical Center , Seoul , South Korea
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Diagnostic Methods of Helicobacter pylori Infection for Epidemiological Studies: Critical Importance of Indirect Test Validation. BIOMED RESEARCH INTERNATIONAL 2016; 2016:4819423. [PMID: 26904678 PMCID: PMC4745376 DOI: 10.1155/2016/4819423] [Citation(s) in RCA: 77] [Impact Index Per Article: 8.6] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 10/02/2015] [Accepted: 12/16/2015] [Indexed: 01/06/2023]
Abstract
Among the methods developed to detect H. pylori infection, determining the gold standard remains debatable, especially for epidemiological studies. Due to the decreasing sensitivity of direct diagnostic tests (histopathology and/or immunohistochemistry [IHC], rapid urease test [RUT], and culture), several indirect tests, including antibody-based tests (serology and urine test), urea breath test (UBT), and stool antigen test (SAT) have been developed to diagnose H. pylori infection. Among the indirect tests, UBT and SAT became the best methods to determine active infection. While antibody-based tests, especially serology, are widely available and relatively sensitive, their specificity is low. Guidelines indicated that no single test can be considered as the gold standard for the diagnosis of H. pylori infection and that one should consider the method's advantages and disadvantages. Based on four epidemiological studies, culture and RUT present a sensitivity of 74.2–90.8% and 83.3–86.9% and a specificity of 97.7–98.8% and 95.1–97.2%, respectively, when using IHC as a gold standard. The sensitivity of serology is quite high, but that of the urine test was lower compared with that of the other methods. Thus, indirect test validation is important although some commercial kits propose universal cut-off values.
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Wang YK, Kuo FC, Liu CJ, Wu MC, Shih HY, Wang SSW, Wu JY, Kuo CH, Huang YK, Wu DC. Diagnosis of Helicobacter pylori infection: Current options and developments. World J Gastroenterol 2015; 21:11221-11235. [PMID: 26523098 PMCID: PMC4616200 DOI: 10.3748/wjg.v21.i40.11221] [Citation(s) in RCA: 232] [Impact Index Per Article: 23.2] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/29/2015] [Revised: 08/06/2015] [Accepted: 09/28/2015] [Indexed: 02/06/2023] Open
Abstract
Accurate diagnosis of Helicobacter pylori (H. pylori) infection is a crucial part in the effective management of many gastroduodenal diseases. Several invasive and non-invasive diagnostic tests are available for the detection of H. pylori and each test has its usefulness and limitations in different clinical situations. Although none can be considered as a single gold standard in clinical practice, several techniques have been developed to give the more reliable results. Invasive tests are performed via endoscopic biopsy specimens and these tests include histology, culture, rapid urease test as well as molecular methods. Developments of endoscopic equipment also contribute to the real-time diagnosis of H. pylori during endoscopy. Urea breathing test and stool antigen test are most widely used non-invasive tests, whereas serology is useful in screening and epidemiological studies. Molecular methods have been used in variable specimens other than gastric mucosa. More than detection of H. pylori infection, several tests are introduced into the evaluation of virulence factors and antibiotic sensitivity of H. pylori, as well as screening precancerous lesions and gastric cancer. The aim of this article is to review the current options and novel developments of diagnostic tests and their applications in different clinical conditions or for specific purposes.
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Zhou L, Zhao F, Hu B, Fang Y, Miao Y, Huang Y, Ji D, Zhang J, Xu L, Zhang Y, Bao Z, Zhao H. A Creative Helicobacter pylori Diagnosis Scheme Based on Multiple Genetic Analysis System: Qualification and Quantitation. Helicobacter 2015; 20:343-52. [PMID: 25640660 DOI: 10.1111/hel.12206] [Citation(s) in RCA: 7] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/18/2022]
Abstract
BACKGROUND Currently, several diagnostic assays for Helicobacter pylori (H. pylori) are available, but each has some limitations. Further, a high-flux quantitative assay is required to assist clinical diagnosis and monitor the effectiveness of therapy and novel vaccine candidates. METHODS Three hundred and eighty-seven adult patients [nonulcer dyspepsia (NUD) 295, peptic ulcer disease (PUD) 77, gastric cancer (GC) 15] were enrolled for gastrointestinal endoscopies. Three biopsy samples from gastric antrum were collected for the following tests: culture, rapid urease test (RUT), histopathology, conventional polymerase chain reaction (PCR), and Multiple Genetic Analysis System (MGAS). The diagnostic capability of H. pylori for all methods was evaluated through the receiver operating characteristic (ROC) curves. RESULTS Based on the gold standard, the sensitivity and specificity of MGAS were 92.9 and 92.4%, and positive predict value (PPV) and negative predict value (NPV) were 96.0 and 87.1%, respectively. All the above parameters of MGAS were higher than that of culture (except its specificity), RUT and histopathology, and nearly closed to that of conventional PCR. The area under curve (AUC) was 0.7575 (Culture), 0.8870 (RUT), 0.9000 (Histopathology), 0.9496 (Conventional PCR), and 0.9277 (MGAS). No significant statistical difference was observed for the H. pylori DNA load in different disease groups (p = .067). In contrast, a statistically significant difference in the H. pylori DNA copy number was observed based on age (p = .043) and gender (p = .021). CONCLUSIONS The data showed that MGAS performed well in detecting H. pylori infection. Furthermore, the quantitative analysis showed that the load of H. pylori was significantly different within both age and gender groups. These results suggested that MGAS could be a potential alternative method for clinical detection and monitoring of the effectiveness of H. pylori therapy.
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Affiliation(s)
- Lifang Zhou
- Department of Laboratory Medicine, Laboratory of Molecular Biology, Huadong Hospital affiliated to, Fudan University, Shanghai, China
| | - Fuju Zhao
- Department of Laboratory Medicine, Laboratory of Molecular Biology, Huadong Hospital affiliated to, Fudan University, Shanghai, China
| | - Binjie Hu
- Department of Laboratory Medicine, Laboratory of Molecular Biology, Huadong Hospital affiliated to, Fudan University, Shanghai, China
| | - Yi Fang
- Department of Laboratory Medicine, Laboratory of Molecular Biology, Huadong Hospital affiliated to, Fudan University, Shanghai, China
| | - Yingxin Miao
- Department of Laboratory Medicine, Laboratory of Molecular Biology, Huadong Hospital affiliated to, Fudan University, Shanghai, China
| | - Yiqin Huang
- Department of Gastroenterology, Gerontology Institute of Shanghai affiliated to, Huadong Hospital, Fudan University, Shanghai, China
| | - Da'nian Ji
- Department of Endoscopy, Huadong Hospital, Fudan University, Shanghai, China
| | - Jinghao Zhang
- Department of Laboratory Medicine, Laboratory of Molecular Biology, Huadong Hospital affiliated to, Fudan University, Shanghai, China
| | - Lingli Xu
- Shanghai AB Sciex Analytical Instrument Trading Co., Ltd, Shanghai, China
| | - Yanmei Zhang
- Shanghai Shine Clinical Laboratories, Inc., The Research base of MDT, DCMST, Ministry of Health, Shanghai, China
| | - Zhijun Bao
- Department of Gastroenterology, Gerontology Institute of Shanghai affiliated to, Huadong Hospital, Fudan University, Shanghai, China
| | - Hu Zhao
- Department of Laboratory Medicine, Laboratory of Molecular Biology, Huadong Hospital affiliated to, Fudan University, Shanghai, China
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Abstract
Proton pump inhibitors (PPI) are a major cause of false-negative Helicobacter pylori test results. Detecting PPI use and stopping it 2 weeks before testing is the preferred approach to improve the reliability of H pylori diagnostic tests. Immunoblot and molecular methods may be useful for the detection of H pylori infection in difficult cases. When conventional tests are negative and eradication is strongly indicated, empirical H pylori treatment should be considered. In this article, an updated critical review of the usefulness of the various invasive and noninvasive tests in the context of extensive PPI use is provided.
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Cizginer S, Ordulu Z, Kadayifci A. Approach to Helicobacter pylori infection in geriatric population. World J Gastrointest Pharmacol Ther 2014; 5:139-147. [PMID: 25133042 PMCID: PMC4133439 DOI: 10.4292/wjgpt.v5.i3.139] [Citation(s) in RCA: 16] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 01/15/2014] [Revised: 03/04/2014] [Accepted: 04/29/2014] [Indexed: 02/06/2023] Open
Abstract
The prevalence of Helicobacter pylori (H. pylori) infection and its complications increase with age. The majority of infected individuals remain asymptomatic throughout the life but 10%-20% develops peptic ulcer disease and 1% gastric malignancies. The incidence of ulcers and their complications are more common in the older population resulting in higher hospitalization and mortality rates. The increased use of medications causing gastric mucosal damage and the decreased secretion of protective prostaglandins in elderly are major factors increasing gastric mucosal sensitivity to the destructive effects of H. pylori. Due to higher prevalence of gastrointestinal (GI) malignancies, upper GI endoscopy is mostly preferred in elderly for the diagnosis of infection. Therefore, “endoscopy and treat” strategy may be more appropriate instead of “test and treat” strategy for dyspeptic patients in older age. Urea breath test and stool antigen test can be used for control of eradication, except for special cases requiring follow-up with endoscopy. The indications for treatment and suggested eradication regimens are similar with other age groups; however, the eradication failure may be a more significant problem due to high antibiotic resistance and low compliance rate in elderly. Multidrug usage and drug interactions should always be considered before starting the treatment. This paper reviews briefly the epidemiology, diagnosis, disease manifestations, and treatment options of H. pylori in the geriatric population.
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Lopes AI, Vale FF, Oleastro M. Helicobacter pylori infection - recent developments in diagnosis. World J Gastroenterol 2014; 20:9299-9313. [PMID: 25071324 PMCID: PMC4110561 DOI: 10.3748/wjg.v20.i28.9299] [Citation(s) in RCA: 51] [Impact Index Per Article: 4.6] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 11/08/2013] [Accepted: 04/16/2014] [Indexed: 02/06/2023] Open
Abstract
Considering the recommended indications for Helicobacter pylori (H. pylori) eradication therapy and the broad spectrum of available diagnostic methods, a reliable diagnosis is mandatory both before and after eradication therapy. Only highly accurate tests should be used in clinical practice, and the sensitivity and specificity of an adequate test should exceed 90%. The choice of tests should take into account clinical circumstances, the likelihood ratio of positive and negative tests, the cost-effectiveness of the testing strategy and the availability of the tests. This review concerns some of the most recent developments in diagnostic methods of H. pylori infection, namely the contribution of novel endoscopic evaluation methodologies for the diagnosis of H. pylori infection, such as magnifying endoscopy techniques and chromoendoscopy. In addition, the diagnostic contribution of histology and the urea breath test was explored recently in specific clinical settings and patient groups. Recent studies recommend enhancing the number of biopsy fragments for the rapid urease test. Bacterial culture from the gastric biopsy is the gold standard technique, and is recommended for antibiotic susceptibility test. Serology is used for initial screening and the stool antigen test is particularly used when the urea breath test is not available, while molecular methods have gained attention mostly for detecting antibiotic resistance.
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Pathak CM, Kaur B, Bhasin DK, Mittal BR, Sharma S, Khanduja KL, Aggarwal L, Rana SS. Comparison of encapsulated versus nonencapsulated (14) C-urea breath test for the detection of Helicobacter pylori infection: a scintigraphy study. Helicobacter 2014; 19:116-23. [PMID: 24237714 DOI: 10.1111/hel.12103] [Citation(s) in RCA: 6] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/27/2022]
Abstract
BACKGROUND AND AIMS (14) C-urea breath test ((14) C-UBT) is considered as "gold standard" for detection of active gastric H. pylori infection. However, till date no comparative study using encapsulated and non-encapsulated (14) C-UBT protocols has been conducted in same subjects in identical conditions. We monitored gastric fate of capsule containing (14) C-urea with real time display and compared sensitivities of these protocols at different time points of breath collection. METHODS Non-encapsulated (14) C-UBT was performed using 74 kBq of (14) C-urea in 100 dyspeptic patients by collecting breath samples at 10, 15 and 20 minutes. Thereafter, within 2 days a gelatin capsule containing (14) C-urea along with 6.0 MBq of (99m) Tc-diethylene triamine penta-acetic acid was administered to each patient for real time display of capsule movement and its fate in gastrointestinal tract by gamma camera. Simultaneously, breath samples were collected for (14) CO2 measurement during image acquisition. RESULTS Employing non-encapsulated (14) C-UBT, 74 out of 100 dyspeptic patients were found to be H. pylori positive. Discordant (14) C-UBT results were obtained in 4/74 (5.4%) cases using these two protocols. By employing encapsulated and nonencapsulated (14) C-UBT protocols, sensitivities of (14) C-UBT were found to be 90.5 versus 98.6% at 10 and 91.8 versus 97.2% at 15 minutes respectively; while these were 94.6 versus 100, 90.7 versus 98.6 and 83.7 versus 93.2% considering any one, two or all three positive values respectively. CONCLUSIONS Incomplete/non-resolution of (14) C-urea capsule in stomach during the phase of breath collections appears to decrease sensitivity of encapsulated (14) C-UBT as compared to nonencapsulated protocol for detection of H. pylori infection.
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Affiliation(s)
- Chander M Pathak
- Department of Biophysics, Post Graduate Institute of Medical Education and Research, Chandigarh, India
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Cho SJ, Choi IJ, Kook MC, Nam BH, Kim CG, Lee JY, Ryu KW, Kim YW. Staging of intestinal- and diffuse-type gastric cancers with the OLGA and OLGIM staging systems. Aliment Pharmacol Ther 2013; 38:1292-302. [PMID: 24134499 DOI: 10.1111/apt.12515] [Citation(s) in RCA: 67] [Impact Index Per Article: 5.6] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/23/2013] [Revised: 08/04/2013] [Accepted: 09/10/2013] [Indexed: 12/20/2022]
Abstract
BACKGROUND Operative link on gastritis assessment (OLGA) and Operative link on gastric intestinal metaplasia assessment (OLGIM) staging systems have been proposed for gastric cancer (GC) risk estimation. AIM To validate the OLGA and OLGIM staging systems in a region with high risk of GC. METHODS This retrospective study included 474 GC patients and age- and sex-matched health screening control persons in a cancer centre hospital. We classified gastritis patterns according to the OLGA and OLGIM systems using the histological database that a pathologist prospectively evaluated using the updated Sydney system. GC risk according to the OLGA and OLGIM stages was evaluated using logistic regression analysis. RESULTS More GC patients had OLGA stages III-IV (46.2%) than controls (26.6%, P < 0.001), particularly among patients with intestinal-type GCs (62.2%) compared with diffuse-type GCs (30.9%). OLGA stages III and IV were significantly associated with increased risk of GC [odds ratios (ORs), 2.09; P = 0.008 and 2.04; P = 0.014 respectively] in multivariate analysis. The association was more significant for intestinal-type (ORs, 4.76; P = 0.001 and 4.19; P = 0.002 respectively), but not diffuse-type GC. OLGIM stages from I to IV were significantly associated with increased risk of both intestinal-type (ORs, 3.64, 5.15, 7.89 and 13.20 respectively) and diffuse-type GC (ORs, 1.84, 2.59, 5.08 and 6.32 respectively) with a significantly increasing trend. CONCLUSION As high OLGA and OLGIM stages are independent risk factors for gastric cancer, the staging systems may be useful for risk assessment in high-risk regions, especially for intestinal-type gastric cancer.
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Affiliation(s)
- S-J Cho
- Center for Gastric Cancer, National Cancer Center, Goyang, Korea
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Cho SJ, Choi IJ, Kook MC, Yoon H, Park S, Kim CG, Lee JY, Lee JH, Ryu KW, Kim YW. Randomised clinical trial: the effects of Helicobacter pylori eradication on glandular atrophy and intestinal metaplasia after subtotal gastrectomy for gastric cancer. Aliment Pharmacol Ther 2013; 38:477-89. [PMID: 23822578 DOI: 10.1111/apt.12402] [Citation(s) in RCA: 25] [Impact Index Per Article: 2.1] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 03/02/2013] [Revised: 03/18/2013] [Accepted: 06/18/2013] [Indexed: 12/13/2022]
Abstract
BACKGROUND Helicobacter pylori eradication is recommended for early gastric cancer (GC) patients after resection. AIM To evaluate whether H. pylori eradication improves glandular atrophy and intestinal metaplasia (IM) in GC patients undergoing subtotal gastrectomy. METHODS This randomised, double-blind trial was performed in tertiary care setting. Distal GC patients with H. pylori infection were randomised to receive proton pump inhibitor-based triple therapy or placebo. The histology was evaluated using the updated Sydney system before and at 36 months after surgery. The endpoints were the comparison of atrophy and IM score changes between the allocated groups and according to final H. pylori status. RESULTS Overall, 190 patients were randomised to the treatment and placebo groups. For lesser curvature of the corpus, mean atrophy and IM scores did not differ between the treatment and placebo groups. However, the H. pylori-eradicated patients had significantly lower mean scores than the H. pylori-persistent patients regarding atrophy (0.55 ± 0.95 vs. 1.05 ± 1.10 respectively; P = 0.0046) and IM (0.66 ± 0.99 vs. 1.05 ± 1.16 respectively; P = 0.0284). The percentage change from baseline was more marked in the H. pylori-negative than in the H. pylori-positive groups (-58.6% vs. -11.0% for atrophy and -60.5% vs. -35.6% for IM respectively). For greater curvature, mean atrophy score was lower in the H. pylori-negative group than in the H. pylori-positive group (0.14 ± 0.50 vs. 0.41 ± 0.75 respectively; P = 0.0281). The percentage change was -36.4% vs. 86.3%. CONCLUSION Helicobacter pylori eradication in GC patients is beneficial, as reflected by lower scores of atrophy and IM at 36 months after subtotal gastrectomy. (ClinicalTrials.gov number, NCT01002443).
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Affiliation(s)
- S-J Cho
- Center for Gastric Cancer, National Cancer Center, Goyang, Korea
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Calvet X, Ramírez Lázaro MJ, Lehours P, Mégraud F. Diagnosis and epidemiology of Helicobacter pylori infection. Helicobacter 2013; 18 Suppl 1:5-11. [PMID: 24011238 DOI: 10.1111/hel.12071] [Citation(s) in RCA: 93] [Impact Index Per Article: 7.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/13/2022]
Abstract
A limited amount of new information was published in the field of diagnosis and epidemiology of Helicobacter pylori this last year. Besides some improvement in current tests, it is interesting to note the attempts to identify severe disease, for example gastric cancer, by breath analysis using nanomaterial-based sensors. In contrast, the predictive value for gastric cancer and atrophy of pepsinogen determinations was found inadequate. Prevalence studies of H. pylori infection have been carried out in adults and children around the world in the general population but also in specific communities. The usual risk factors were found. In addition, a Japanese study highlighted the role of grandmothers in the familial transmission of H. pylori. A study showed that the infection may not always readily establish itself in children, given the number of transient infections observed. It was also noted that after eradication, a first-year relapse is likely to be a recurrence of the previous infection, while later on it is probably a reinfection with a new strain.
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Affiliation(s)
- Xavier Calvet
- Department of Gastroenterology, Hospital de Sabadell, Barcelona, Spain; Departament de Medicina, Universitat Autonoma de Barcelona and CIBEREHD, Barcelona, Spain
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