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Xian L, Si Y, Luan L, Lai J, Tang J, Wang L. Epidemiological characteristics of Helicobacter pylori infection and antibiotic resistance in urban areas of Guangdong Province, China: a multi-center, cross-sectional surveillance. Eur J Clin Microbiol Infect Dis 2025:10.1007/s10096-025-05105-9. [PMID: 40080302 DOI: 10.1007/s10096-025-05105-9] [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: 12/13/2024] [Accepted: 03/07/2025] [Indexed: 03/15/2025]
Abstract
PURPOSE Helicobacter pylori (H. pylori) infection is widespread globally and can cause serious gastrointestinal complications, including gastric cancer. This study assesses the prevalence and antibiotic resistance of H. pylori in Guangdong, one of China's most developed provinces. METHODS A multi-center, cross-sectional study was conducted across six cities in Guangdong provinces, that is, Guangzhou, Shenzhen, Heyuan, Foshan, Yunfu, and Zhaoqing. Non-invasive gastric fluid samples were collected via the string test, and H. pylori infection and antibiotic resistance were detected using quantitative PCR. Risk factors for infection were analyzed. RESULTS Of 1,764 participants, 444 (25.17%) tested positive for H. pylori, with the highest infection rate in Foshan (29.81%). Antibiotic resistance testing of these 444 infected individuals revealed that, except for levofloxacin resistance in Yunfu (14.29%), clarithromycin resistance in Yunfu and resistance to other antibiotics in all cities exceeded the 15% threshold. Infection rates were significantly higher in males (OR 1.29, 95% CI 1.03-1.60, p = 0.03) and obese individuals (OR 2.04, 95% CI 1.04-3.91, p = 0.03), with obesity identified as an independent risk factor. CONCLUSION This study provides a comprehensive update on the prevalence, antibiotic resistance, and risk factors of H. pylori infection in Guangdong, offering valuable insights for public health strategies aimed at improving diagnosis and treatment.
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Affiliation(s)
- Luhua Xian
- Laboratory Medicine, Guangdong Provincial People's Hospital (Guangdong Academy of Medical Sciences, Southern Medical University, Guangzhou, Guangdong, China
| | - Yuting Si
- Laboratory Medicine, Guangdong Provincial People's Hospital (Guangdong Academy of Medical Sciences, Southern Medical University, Guangzhou, Guangdong, China
| | - Luan Luan
- Laboratory Medicine, Guangdong Provincial People's Hospital (Guangdong Academy of Medical Sciences, Southern Medical University, Guangzhou, Guangdong, China
| | - Jinxin Lai
- Laboratory Medicine, Guangdong Provincial People's Hospital (Guangdong Academy of Medical Sciences, Southern Medical University, Guangzhou, Guangdong, China
| | - Jiawei Tang
- Division of Microbiology and Immunology, School of Biomedical Sciences, The University of Western Australia, Crawley, WA, Australia
| | - Liang Wang
- Laboratory Medicine, Guangdong Provincial People's Hospital (Guangdong Academy of Medical Sciences, Southern Medical University, Guangzhou, Guangdong, China.
- Division of Microbiology and Immunology, School of Biomedical Sciences, The University of Western Australia, Crawley, WA, Australia.
- Centre for Precision Health, School of Medical and Health Sciences, Edith Cowan University, Perth, WA, Australia.
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Polyzos SA, Pyrrou N, Kountouras J. Helicobacter pylori Infection and Metabolic Dysfunction-Associated Steatotic Liver Disease. Dig Dis 2025; 43:253-256. [PMID: 39938484 DOI: 10.1159/000544122] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/07/2024] [Accepted: 02/08/2025] [Indexed: 02/14/2025]
Affiliation(s)
- Stergios A Polyzos
- First Laboratory of Pharmacology, School of Medicine, Aristotle University of Thessaloniki, Thessaloniki, Greece
| | - Nikoletta Pyrrou
- Department of Radiology, University General Hospital of Thessaloniki AHEPA, Aristotle University of Thessaloniki, Thessaloniki, Greece
| | - Jannis Kountouras
- Second Medical Clinic, School of Medicine, Aristotle University of Thessaloniki, Ippokration Hospital, Thessaloniki, Greece
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Kim JY, Kwan BS, Cho JH, Kim HI, Ko NG, Jin M, Lee OJ. Persistently Active Helicobacter pylori Infection Is Associated with the Development of Metabolic Dysfunction-Associated Steatotic Liver Disease. J Clin Med 2025; 14:1073. [PMID: 40004603 PMCID: PMC11856028 DOI: 10.3390/jcm14041073] [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: 01/18/2025] [Revised: 01/31/2025] [Accepted: 02/06/2025] [Indexed: 02/27/2025] Open
Abstract
Background/Objectives: Previous studies suggested a link between Helicobacter pylori (H. pylori) infection and steatotic liver disease, now termed metabolic dysfunction-associated steatotic liver disease (MASLD). This study aimed to identify the association of active H. pylori infection and the new concept of MASLD in a longitudinal cohort. Methods: We reviewed 1497 health examinees who had two endoscopic biopsies for H. pylori activity without hepatic steatosis at the baseline abdominal ultrasonography. Subjects were classified into four groups based on H. pylori activity. Multivariable Cox models assessed the link between active H. pylori infection status and incident MASLD. Results: Over a median follow-up of 31.1 months, 247 subjects (16.5%) developed MASLD. The groups were: H. pylori naïve (n = 57, 15.6%), de novo (n = 31, 15.3%), eradicated (n = 32, 16.1%), and persistent (n = 127, 17.4%). The H. pylori persistent group had a higher risk of MASLD compared to naïve group (hazard ratio: 1.41; 95% confidence interval: 1.01-1.96; p-value = 0.045). The association between H. pylori infection and incident MASLD was significant only with ongoing infection. Conclusions: Persistent H. pylori infection increases the risk of MASLD, indicating that active infection may contribute to MASLD development. Eradicating active H. pylori infection might help lower the incidence of MASLD.
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Affiliation(s)
- Jun Young Kim
- Department of Medicine, Gyeongsang National University Graduate School, Jinju 52727, Republic of Korea;
- Department of Internal Medicine, Samsung Changwon Hospital, Sungkyunkwan University School of Medicine, Changwon 51353, Republic of Korea
| | - Byung Soo Kwan
- Department of Internal Medicine, Samsung Changwon Hospital, Sungkyunkwan University School of Medicine, Changwon 51353, Republic of Korea
| | - Jung Hwan Cho
- Department of Internal Medicine, Samsung Changwon Hospital, Sungkyunkwan University School of Medicine, Changwon 51353, Republic of Korea
| | - Hye In Kim
- Department of Internal Medicine, Samsung Changwon Hospital, Sungkyunkwan University School of Medicine, Changwon 51353, Republic of Korea
| | - Nak Gyeong Ko
- Department of Research & Support, Samsung Changwon Hospital, Sungkyunkwan University School of Medicine, Changwon 51353, Republic of Korea
| | - Mihyeon Jin
- Department of Research & Support, Samsung Changwon Hospital, Sungkyunkwan University School of Medicine, Changwon 51353, Republic of Korea
| | - Ok Jae Lee
- Department of Internal Medicine, Gyeongsang National University College of Medicine and Gyeongsang National University Hospital, Jinju 52727, Republic of Korea
- Institute of Medical Science, Gyeongsang National University, Jinju 52727, Republic of Korea
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Liu Z, Xu H, You W, Pan K, Li W. Helicobacter pylori eradication for primary prevention of gastric cancer: progresses and challenges. JOURNAL OF THE NATIONAL CANCER CENTER 2024; 4:299-310. [PMID: 39735441 PMCID: PMC11674435 DOI: 10.1016/j.jncc.2024.06.006] [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: 04/26/2024] [Revised: 06/20/2024] [Accepted: 06/27/2024] [Indexed: 12/31/2024] Open
Abstract
Gastric cancer remains a significant global health challenge, causing a substantial number of cancer-related deaths, particularly in China. While the exact causes of gastric cancer are still being investigated, Helicobacter pylori (H. pylori) infection has been identified as the primary risk factor, which triggers chronic inflammation and a multistage progression of gastric lesions that may lead to carcinogenesis over a long latency time. Since the 1990s, numerous efforts have focused on assessing the effectiveness of H. pylori eradication in preventing new cases of gastric cancer among both the general population and patients who have undergone early-stage cancer treatment. This body of work, including several community-based interventions and meta-analyses, has shown a reduction in both the incidence of and mortality from gastric cancer following H. pylori treatment, alongside a decreased risk of metachronous gastric cancer. In this review, we seek to consolidate current knowledge on the effects of H. pylori treatment on gastric cancer prevention, its systemic consequences, cost-effectiveness, and the influence of antibiotic resistance and host characteristics on treatment outcomes. We further discuss the potential for precision primary prevention of H. pylori treatment and comment on the efficient implementation of test-and-treat policies and allocation of health resources towards minimizing the burden of gastric cancer globally.
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Affiliation(s)
- Zongchao Liu
- State Key Laboratory of Holistic Integrative Management of Gastrointestinal Cancers, Beijing Key Laboratory of Carcinogenesis and Translational Research, Department of Cancer Epidemiology, Peking University Cancer Hospital & Institute, Beijing, China
| | - Hengmin Xu
- State Key Laboratory of Holistic Integrative Management of Gastrointestinal Cancers, Beijing Key Laboratory of Carcinogenesis and Translational Research, Department of Cancer Epidemiology, Peking University Cancer Hospital & Institute, Beijing, China
| | - Weicheng You
- Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Department of Cancer Epidemiology, Peking University Cancer Hospital and Institute, Beijing, China
| | - Kaifeng Pan
- State Key Laboratory of Holistic Integrative Management of Gastrointestinal Cancers, Beijing Key Laboratory of Carcinogenesis and Translational Research, Department of Cancer Epidemiology, Peking University Cancer Hospital & Institute, Beijing, China
| | - Wenqing Li
- State Key Laboratory of Holistic Integrative Management of Gastrointestinal Cancers, Beijing Key Laboratory of Carcinogenesis and Translational Research, Department of Cancer Epidemiology, Peking University Cancer Hospital & Institute, Beijing, China
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Ibrahim T, Russel W, Getachew A, Zemene E, Cheneke W, Taye B. Association between infection with Helicobacter pylori and metabolic syndrome among diabetic patients attending Jimma medical center in Jimma city, Ethiopia: a cross-sectional study. BMC Infect Dis 2024; 24:922. [PMID: 39237908 PMCID: PMC11378407 DOI: 10.1186/s12879-024-09840-w] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/30/2024] [Accepted: 08/29/2024] [Indexed: 09/07/2024] Open
Abstract
BACKGROUND Previous studies have implicated the role of H. pylori infection in developing the metabolic syndrome. However, findings remain contradictory, and data from developing countries are scarce. METHODS We employed a cross-sectional study design to assess the relationship between H. pylori infection and metabolic syndrome among diabetic patients attending Jimma Hospital, Ethiopia. An interviewer-led questionnaire administered to study participants provided information on sociodemographic factors, and medical records were used to obtain medical history information. Metabolic parameters, including plasma glucose, triglycerides (TG), high-density lipoprotein cholesterol (HDL-c), body-mass index (BMI), waist circumference (WC), systolic blood pressure (SBP), and diastolic blood pressure (DBP) were collected. H. pylori infection status was assessed using IgG Enzyme-linked Immunosorbent Assays (ELISA). The effect of H. pylori infection on metabolic syndrome and metabolic parameters was determined using multivariate linear and logistic regressions. RESULTS We found H. pylori infection status was positively but not significantly associated with metabolic syndrome (AOR = 1.507, 95% CI: 0.570-3.981, p = 0.408). When the analysis was restricted to individual metabolic parameters, H. pylori positivity was significantly associated with lower HDL-c and higher SB, respectively. CONCLUSIONS Our result confirms that individual metabolic parameters, not an overall metabolic syndrome, are significantly associated with H. pylori infection. Future studies should examine the relationship between H. pylori and metabolic syndrome, considering gastrointestinal conditions such as GERD, GU, and DU.
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Affiliation(s)
- Temam Ibrahim
- School of Medical Laboratory Sciences, Institute of Health, Jimma University, Jimma, Ethiopia
| | - William Russel
- Department of Biology, Colgate University, Hamilton, NY, USA
| | - Aklilu Getachew
- School of Medical Laboratory Sciences, Institute of Health, Jimma University, Jimma, Ethiopia
| | - Endalew Zemene
- School of Medical Laboratory Sciences, Institute of Health, Jimma University, Jimma, Ethiopia
| | - Waqtola Cheneke
- School of Medical Laboratory Sciences, Institute of Health, Jimma University, Jimma, Ethiopia
| | - Bineyam Taye
- Department of Biology, Colgate University, Hamilton, NY, USA.
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Chen D, Wang S, Yang W, Lu H, Ren Q. Obesity, abdominal obesity, metabolic obesity phenotypes, and Helicobacter pylori infection: results from NHANES 1999-2000. BMC Infect Dis 2024; 24:676. [PMID: 38971751 PMCID: PMC11227695 DOI: 10.1186/s12879-024-09409-7] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/16/2023] [Accepted: 05/15/2024] [Indexed: 07/08/2024] Open
Abstract
BACKGROUND Recent studies on the association between Helicobacter pylori (H. pylori) infection and obesity have reported conflicting results. Therefore, the purpose of our study was to investigate the association of obesity, abdominal obesity, and metabolic obesity phenotypes with H. pylori infection. METHODS A cross-sectional study of 1568 participants aged 20 to 85 was conducted using the National Health and Nutrition Examination Survey (NHANES) cycle 1999-2000. Logistic regression models were employed to evaluate the association of general obesity as defined by body mass index (BMI), abdominal obesity as defined by waist circumference (WC) and waist-height ratio (WHtR), and metabolic obesity phenotypes with H. pylori seropositivity. Subgroup analyses stratified by age were conducted to explore age-specific differences in this association. RESULTS After grouping individuals according to their WHtR, the prevalence rate of WHtR ≥ 0.5 in H. pylori-seropositive participants was significantly higher than that in H. pylori-seronegative participants (79.75 vs. 68.39, P < 0.001). The prevalence of H. pylori seropositivity in non-abdominal obesity and abdominal obesity defined by WHtR was 24.97% and 31.80%, respectively (P < 0.001). In the subgroup analysis, the adjusted association between abdominal obesity, as defined by the WHtR, and H. pylori seropositivity was significant in subjects aged < 50 years (OR = 2.23; 95% CI, 1.24-4.01; P = 0.01) but not in subjects aged ≥ 50 years (OR = 0.84; 95% CI, 0.35-1.99; P = 0.66). Subjects older than 50 years old had an OR (95% CI) for metabolically healthy obesity of 0.04 (0.01-0.35) compared with the control group. H. pylori seropositivity was consistently not associated with obesity as defined by BMI. CONCLUSIONS Abdominal obesity, as defined by the WHtR, was associated with H. pylori infection in subjects aged ≤ 50 years.
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Affiliation(s)
- Danni Chen
- The First School of Clinical Medicine, Lanzhou University, Lanzhou, 730000, China
- Department of Gastroenterology, the First Hospital of Lanzhou University, Lanzhou, 730000, China
| | - Shiling Wang
- The First School of Clinical Medicine, Lanzhou University, Lanzhou, 730000, China
- Department of Gastroenterology, the First Hospital of Lanzhou University, Lanzhou, 730000, China
| | - Wei Yang
- The First School of Clinical Medicine, Lanzhou University, Lanzhou, 730000, China
- Department of Gastroenterology, the First Hospital of Lanzhou University, Lanzhou, 730000, China
| | - Hong Lu
- The First School of Clinical Medicine, Lanzhou University, Lanzhou, 730000, China
- Department of Gastroenterology, the First Hospital of Lanzhou University, Lanzhou, 730000, China
- Gansu Province Clinical Research Center for Digestive Diseases, Lanzhou, China
| | - Qian Ren
- The First School of Clinical Medicine, Lanzhou University, Lanzhou, 730000, China.
- Department of Gastroenterology, the First Hospital of Lanzhou University, Lanzhou, 730000, China.
- Gansu Province Clinical Research Center for Digestive Diseases, Lanzhou, China.
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Chua WK, Hong YK, Hu SW, Fan HC, Ting WH. A Significant Association between Type 1 Diabetes and Helicobacter pylori Infection: A Meta-Analysis Study. MEDICINA (KAUNAS, LITHUANIA) 2024; 60:119. [PMID: 38256380 PMCID: PMC10821400 DOI: 10.3390/medicina60010119] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 11/17/2023] [Revised: 12/11/2023] [Accepted: 12/28/2023] [Indexed: 01/24/2024]
Abstract
Background and Objectives: Type 1 diabetes mellitus (T1DM) is a chronic and serious condition that is characterized by inadequate pancreatic-β-cells' insulin production. The connection between T1DM and Helicobacter pylori infection remains uncertain. This study aimed to conduct a systematic meta-analysis to examine the association between H. pylori infection, hemoglobin A1c levels, and the development of T1DM. Materials and Methods: The initial search identified 451 articles on the association between H. pylori infection and T1DM. Among them, 12 articles had 2797 participants who met the inclusion criteria for an advanced meta-analysis. Results: A significant association was observed between H. pylori infection and T1DM (OR 1.77, 95% CI 1.47-2.12, p < 0.0001), with heterogeneity: Tau2 = 0.47; Chi2 = 57.07, df = 11 (p < 0.0001); I2 = 81%. Subgroup analysis showed that H. pylori infection was significantly associated with a longer duration of T1DM and higher hemoglobin A1c levels (p < 0.001 for both) but not with age at T1DM diagnosis (p = 0.306). Conclusions: These findings contribute to the understanding of the association between H. pylori infection and T1DM and highlight the potential role of H. pylori in influencing the duration and glycemic control of diabetes. Therefore, pediatric patients who have longstanding T1DM and poor glycemic control should be screened for H. pylori infection.
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Affiliation(s)
- Wei-Kian Chua
- Division of Pediatric Endocrinology, Department of Pediatrics, Tungs’ Taichung MetroHarbor Hospital, Taichung 43503, Taiwan;
| | - Yi-Kai Hong
- Department of Dermatology, National Cheng Kung University Hospital, College of Medicine, National Cheng Kung University, Tainan 70101, Taiwan;
- International Center for Wound Repair and Regeneration (iWRR), National Cheng Kung University, Tainan 70101, Taiwan
- Department of Dermatology, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611, USA
| | - Shu-Wei Hu
- Division of Pediatric Gastroenterology, Department of Pediatrics, Tungs’ Taichung MetroHarbor Hospital, Taichung 43503, Taiwan
- Ph.D. Program in Translational Medicine, National Chung Hsing University, Taichung 40227, Taiwan
- Rong Hsing Research Center for Translational Medicine, National Chung Hsing University, Taichung 40227, Taiwan
| | - Hueng-Chuen Fan
- Rong Hsing Research Center for Translational Medicine, National Chung Hsing University, Taichung 40227, Taiwan
- Division of Pediatric Neurology, Department of Pediatrics, Tungs’ Taichung MetroHarbor Hospital, Taichung 43503, Taiwan
- Department of Rehabilitation, Jenteh Junior College of Medicine, Nursing and Management, Miaoli 35664, Taiwan
| | - Wei-Hsin Ting
- Department of Pediatric Endocrinology, MacKay Children’s Hospital, Taipei 10449, Taiwan
- Department of Medicine, MacKay Medical College, New Taipei 25245, Taiwan
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Chen X, Peng R, Peng D, Xiao J, Liu D, Li R. An update: is there a relationship between H. pylori infection and nonalcoholic fatty liver disease? why is this subject of interest? Front Cell Infect Microbiol 2023; 13:1282956. [PMID: 38145041 PMCID: PMC10739327 DOI: 10.3389/fcimb.2023.1282956] [Citation(s) in RCA: 6] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/25/2023] [Accepted: 11/21/2023] [Indexed: 12/26/2023] Open
Abstract
Helicobacter pylori (H. pylori) infection is thought to impact various extragastric diseases, including nonalcoholic fatty liver disease (NAFLD), the most common chronic liver disease. Meanwhile, the pathogenesis of NAFLD needs further research, and effective treatment for this disease remains elusive. In this mini-review, we enumerate and ponder on the evidence demonstrating an association between H. pylori infection and NAFLD. Primarily, we delve into high-quality meta-analyses and clinical randomized controlled trials focusing on the association studies between the two. We also discuss clinical studies that present opposite conclusions. In addition, we propose a mechanism through which H. pylori infection aggravates NAFLD: inflammatory cytokines and adipocytokines, insulin resistance, lipid metabolism, intestinal barrier and microbiota, H. pylori outer membrane vesicles and H. pylori-infected cell-extracellular vesicles. This mini-review aims to further explore NAFLD pathogenesis and extragastric disease mechanisms caused by H. pylori infection.
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Affiliation(s)
- Xingcen Chen
- Department of Gastroenterology, the Second Xiangya Hospital of Central South University, Changsha, Hunan, China
- Research Center of Digestive Diseases, Central South University, Changsha, Hunan, China
- Clinical Research Center, Digestive Diseases of Hunan Province, Changsha, Hunan, China
| | - Ruyi Peng
- Department of Gastroenterology, the Second Xiangya Hospital of Central South University, Changsha, Hunan, China
- Research Center of Digestive Diseases, Central South University, Changsha, Hunan, China
- Clinical Research Center, Digestive Diseases of Hunan Province, Changsha, Hunan, China
| | - Dongzi Peng
- Department of Gastroenterology, the Second Xiangya Hospital of Central South University, Changsha, Hunan, China
- Research Center of Digestive Diseases, Central South University, Changsha, Hunan, China
- Clinical Research Center, Digestive Diseases of Hunan Province, Changsha, Hunan, China
| | - Jia Xiao
- Department of Gastroenterology, the Second Xiangya Hospital of Central South University, Changsha, Hunan, China
- Research Center of Digestive Diseases, Central South University, Changsha, Hunan, China
- Clinical Research Center, Digestive Diseases of Hunan Province, Changsha, Hunan, China
| | - Deliang Liu
- Department of Gastroenterology, the Second Xiangya Hospital of Central South University, Changsha, Hunan, China
- Research Center of Digestive Diseases, Central South University, Changsha, Hunan, China
- Clinical Research Center, Digestive Diseases of Hunan Province, Changsha, Hunan, China
| | - Rong Li
- Department of Gastroenterology, the Second Xiangya Hospital of Central South University, Changsha, Hunan, China
- Research Center of Digestive Diseases, Central South University, Changsha, Hunan, China
- Clinical Research Center, Digestive Diseases of Hunan Province, Changsha, Hunan, China
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Aramouni K, Assaf RK, Azar M, Jabbour K, Shaito A, Sahebkar A, Eid AA, Rizzo M, Eid AH. Infection with Helicobacter pylori may predispose to atherosclerosis: role of inflammation and thickening of intima-media of carotid arteries. Front Pharmacol 2023; 14:1285754. [PMID: 37900161 PMCID: PMC10611526 DOI: 10.3389/fphar.2023.1285754] [Citation(s) in RCA: 12] [Impact Index Per Article: 6.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/30/2023] [Accepted: 09/25/2023] [Indexed: 10/31/2023] Open
Abstract
Atherosclerosis is a major instigator of cardiovascular disease (CVD) and a main cause of global morbidity and mortality. The high prevalence of CVD calls for urgent attention to possible preventive measures in order to curb its incidence. Traditional risk factors of atherosclerosis, like age, smoking, diabetes mellitus, dyslipidemia, hypertension and chronic inflammation, are under extensive investigation. However, these only account for around 50% of the etiology of atherosclerosis, mandating a search for different or overlooked risk factors. In this regard, chronic infections, by Helicobacter pylori for instance, are a primary candidate. H. pylori colonizes the gut and contributes to several gastrointestinal diseases, but, recently, the potential involvement of this bacterium in extra-gastric diseases including CVD has been under the spotlight. Indeed, H. pylori infection appears to stimulate foam cell formation as well as chronic immune responses that could upregulate key inflammatory mediators including cytokines, C-reactive protein, and lipoproteins. These factors are involved in the thickening of intima-media of carotid arteries (CIMT), a hallmark of atherosclerosis. Interestingly, H. pylori infection was found to increase (CIMT), which along with other evidence, could implicate H. pylori in the pathogenesis of atherosclerosis. Nevertheless, the involvement of H. pylori in CVD and atherosclerosis remains controversial as several studies report no connection between H. pylori and atherosclerosis. This review examines and critically discusses the evidence that argues for a potential role of this bacterium in atherogenesis. However, additional basic and clinical research studies are warranted to convincingly establish the association between H. pylori and atherosclerosis.
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Affiliation(s)
- Karl Aramouni
- Faculty of Medicine, American University of Beirut, Beirut, Lebanon
| | - Roland K. Assaf
- Faculty of Medicine, American University of Beirut, Beirut, Lebanon
| | - Maria Azar
- Faculty of Medicine, American University of Beirut, Beirut, Lebanon
| | - Karen Jabbour
- Faculty of Medicine, American University of Beirut, Beirut, Lebanon
| | - Abdullah Shaito
- Biomedical Research Center, Department of Biomedical Sciences at College of Health Sciences, College of Medicine, Qatar University, Doha, Qatar
| | - Amirhossein Sahebkar
- Biotechnology Research Center, Applied Biomedical Research Center, Department of Biotechnology, School of Pharmacy, Pharmaceutical Technology Institute, Mashhad University of Medical Sciences, Mashhad, Iran
| | - Assaad A. Eid
- Faculty of Medicine, American University of Beirut, Beirut, Lebanon
| | - Manfredi Rizzo
- Department of Health Promotion, Mother and Child Care, Internal Medicine and Medical Specialties, University of Palermo, Palermo, Italy
| | - Ali H. Eid
- Department of Basic Medical Sciences, College of Medicine, QU Health, Qatar University, Doha, Qatar
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10
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Liu Y, Shuai P, Chen W, Liu Y, Li D. Association between Helicobacter pylori infection and metabolic syndrome and its components. Front Endocrinol (Lausanne) 2023; 14:1188487. [PMID: 37404306 PMCID: PMC10316390 DOI: 10.3389/fendo.2023.1188487] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 03/17/2023] [Accepted: 06/02/2023] [Indexed: 07/06/2023] Open
Abstract
Background and aim The association between Helicobacter pylori (H. pylori) infection and metabolic syndrome (MetS) has been studied previously; however, the results remain controversial, which could be partly due to the different criteria used for defining MetS. We adopted five MetS criteria to provide better understanding of the association between H. pylori infection and MetS. Methods Physical examination data of 100,708 subjects were obtained from January 2014 to December 2018. MetS was defined based on five criteria including: International Diabetes Federation (IDF), The Third Report of the National Cholesterol Education Program Expert Panel, Adult Treatment Panel III (ATP III), Joint Statement of International Multi-Societies (JIS), Chinese Diabetes Society (CDS), and the Guidelines for the Prevention and Treatment of Type 2 Diabetes in China (2017 edition)(CDS DM). Multivariate logistic regression analysis was performed to elucidate the association between H. pylori infection and MetS and its components. Results The prevalence of MetS defined assessed using IDF, ATP III, JIS, CDS and CDS DM criteria was 15.8%, 19.9%, 23.7%, 8.7% and 15.4%, respectively. In males, the prevalence of MetS assessed using the five criteria in H. pylori-positive group was higher than that in negative-group; however, in females, same results were obtained using the three international criteria. In males, the prevalence of all MetS components was found to be higher in the H. pylori-positive group than those in the negative group; however, in females, only the prevalence of dyslipidemia and waist circumferences exhibited significant differences. Multivariate logistic regression analysis revealed that H. pylori infection in males was positively correlated with MetS. Additionally, H. pylori infection was found to be positively correlated with the waist circumference in the general population, and with hypertension and hyperglycemia in males. Conclusions H. pylori infection was found to be positively associated with MetS in males in China.
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Affiliation(s)
- Ying Liu
- Department of Health Management Center & Institute of Health Management, Sichuan Provincial People’s Hospital, University of Electronic Science and Technology of China, Chengdu, China
- Chinese Academy of Sciences Sichuan Translational Medicine Research Hospital, Chengdu, Sichuan, China
| | - Ping Shuai
- Department of Health Management Center & Institute of Health Management, Sichuan Provincial People’s Hospital, University of Electronic Science and Technology of China, Chengdu, China
- Chinese Academy of Sciences Sichuan Translational Medicine Research Hospital, Chengdu, Sichuan, China
| | - Wanjing Chen
- Department of Health Management Center & Institute of Health Management, Sichuan Provincial People’s Hospital, University of Electronic Science and Technology of China, Chengdu, China
- Chinese Academy of Sciences Sichuan Translational Medicine Research Hospital, Chengdu, Sichuan, China
| | - Yuping Liu
- Department of Health Management Center & Institute of Health Management, Sichuan Provincial People’s Hospital, University of Electronic Science and Technology of China, Chengdu, China
- Chinese Academy of Sciences Sichuan Translational Medicine Research Hospital, Chengdu, Sichuan, China
| | - Dongyu Li
- Department of Health Management Center & Institute of Health Management, Sichuan Provincial People’s Hospital, University of Electronic Science and Technology of China, Chengdu, China
- Chinese Academy of Sciences Sichuan Translational Medicine Research Hospital, Chengdu, Sichuan, China
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11
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Chen Y, Yang C, You N, Zhang J. Relationship between Helicobacter pylori and glycated hemoglobin: a cohort study. Front Cell Infect Microbiol 2023; 13:1196338. [PMID: 37360526 PMCID: PMC10288807 DOI: 10.3389/fcimb.2023.1196338] [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: 03/29/2023] [Accepted: 05/29/2023] [Indexed: 06/28/2023] Open
Abstract
Background Helicobacter pylori (H. pylori) has increasingly been shown to be related to extragastric diseases. Glycated hemoglobin A1c (HbA1c), an indicator of glycemic control, is closely linked to the event of diabetes. The purpose of this research was to analyze the association between H. pylori and HbA1c through a cohort study. Methods The population who underwent multiple physical checkups in the physical examination center of Taizhou Hospital was included. All of them underwent urea breath test, serological examination and physical parameter measurement. Multiple regression was used for analyzing the influencing factors of HbA1c. In addition, the result of HbA1c on H. pylori infection was studied by restricted cubic spline (RCS) analysis. The triglyceride glucose (TyG) index represents the level of insulin resistance (IR) in the population. The population was classified on the basis of primary and last H. pylori infection, therefore, the variations of HbA1c and TyG index among totally different teams were investigated. Results Multiple regression demonstrated that H. pylori was an influential factor in HbA1c. RCS analysis showed a nonlinear relationship between HbA1c and H. pylori infection. When HbA1c>5.7%, the chance of H. pylori infection was considerably enlarged. Additionally, long-term H. pylori infection increased HbA1c levels, while HbA1c levels decreased after H. pylori eradication. Similarly, long-term H. pylori infection also increased the TyG index. Conclusion Prediabetes increases the danger of H. pylori infection, long-term H. pylori infection increases HbA1c and IR levels, and wipeout of H. pylori could have a positive impact for glycemic control in the population.
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Affiliation(s)
- Yi Chen
- Departments of Gastroenterology, Taizhou Hospital of Zhejiang Province Affiliated to Wenzhou Medical University, Linhai, Zhejiang, China
| | - Chaoyu Yang
- Departments of Gastroenterology, Taizhou Hospital of Zhejiang Province Affiliated to Wenzhou Medical University, Linhai, Zhejiang, China
| | - Ningning You
- Departments of Gastroenterology, Taizhou Hospital of Zhejiang Province Affiliated to Wenzhou Medical University, Linhai, Zhejiang, China
| | - Jinshun Zhang
- Health Management Center, Taizhou Hospital of Zhejiang Province Affiliated to Wenzhou Medical University, Linhai, Zhejiang, China
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12
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Chen Y, You N, Shen C, Wu J, Zhang J. Helicobacter pylori infection increases the risk of nonalcoholic fatty liver disease in diabetic population. Front Nutr 2023; 10:1076579. [PMID: 36819677 PMCID: PMC9929141 DOI: 10.3389/fnut.2023.1076579] [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: 10/21/2022] [Accepted: 01/13/2023] [Indexed: 02/04/2023] Open
Abstract
Background The effect of Helicobacter pylori (H. pylori) on nonalcoholic fatty liver disease (NAFLD) in the population is still controversial. Diabetes and NAFLD are both metabolically related diseases, and no studies have classified the population to study the effect of H. pylori infection on NAFLD in diabetics. Methods A population of people who were examined in the Taizhou Hospital Health Examination Center from 2017 to 2022 was included, and hematological indicators, body parameters, ultrasound data, and H. pylori detection by urea nitrogen test were collected from patients. All physical examination populations were divided into diabetic and non-diabetic populations. Results After multivariate logistic regression, H. pylori infection remained an independent risk factor for NAFLD in diabetics, but it had no significant effect on NAFLD in non-diabetic population. Additionally, there was a nonlinear relationship between glycosylated hemoglobin and H. pylori infection in diabetic population. Moreover, the incidence of NAFLD in diabetics increased with persistent H. pylori infection. Conclusion In the diabetic population, H. pylori infection does increase the risk of developing NAFLD. Glycemic control and eradication of H. pylori infection may have positive implications for reducing the incidence of NAFLD in diabetic population.
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Affiliation(s)
- Yi Chen
- Department of Gastroenterology, Taizhou Hospital of Zhejiang Province Affiliated to Wenzhou Medical University, Taizhou, China
| | - Ningning You
- Department of Gastroenterology, Taizhou Hospital of Zhejiang Province Affiliated to Wenzhou Medical University, Taizhou, China
| | - Chuchen Shen
- Department of Gastroenterology, Taizhou Hospital of Zhejiang Province Affiliated to Wenzhou Medical University, Taizhou, China
| | - Juju Wu
- Department of Gastroenterology, Taizhou Hospital of Zhejiang Province Affiliated to Wenzhou Medical University, Taizhou, China
| | - Jinshun Zhang
- Health Management Center, Taizhou Hospital of Zhejiang Province Affiliated to Wenzhou Medical University, Taizhou, China,*Correspondence: Jinshun Zhang, ✉
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Valadares EC, Gestic MA, Utrini MP, Chaim FDM, Chaim EA, Cazzo E. Is Helicobacter pylori infection associated with non-alcoholic fatty liver disease in individuals undergoing bariatric surgery? Cross-sectional study. SAO PAULO MED J 2023; 141:e2022517. [PMID: 37042863 PMCID: PMC10085533 DOI: 10.1590/1516-3180.2022.0517.r1.14122022] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 08/31/2022] [Accepted: 12/14/2022] [Indexed: 04/13/2023] Open
Abstract
BACKGROUND A possible direct link between nonalcoholic fatty liver disease (NAFLD) and Helicobacter pylori (H. pylori) infection has recently emerged. OBJECTIVE This study aimed to analyze associations between the presence of histologically demonstrated NAFLD aspects with H. pylori infection in individuals with obesity undergoing bariatric surgery. DESIGN AND SETTING An observational analytical cross-sectional study was conducted based on data collected from the medical records of individuals undergoing bariatric surgery at a tertiary university hospital in 2019. METHODS NAFLD was assessed through histological examination of wedge liver biopsies collected during the proceedings. H. pylori infection was analyzed through the association of the urease test and histological examination performed in biopsies routinely collected during preoperative esophagogastroduodenoscopy. RESULTS Of the 88 participants, 85% were female, and the average age was 39.1 ± 8.4 years. H. pylori infection was present in 61.4% of the patients. The mean body mass index was 36.6 ± 3.4 kg/m2. The most prevalent histopathological aspects of NAFLD were macrovesicular steatosis (92%), hepatocellular ballooning (92%), lobular inflammation (93.2%), portal inflammation (96.6%), and fibrosis (93.2%). No histopathological aspect of NAFLD was found to be significantly associated with H. pylori infection. CONCLUSION In this study population, H. pylori infection was not significantly associated with the histopathological aspects of NAFLD in individuals with obesity undergoing bariatric surgery.
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Affiliation(s)
- Erick Coelho Valadares
- MD. Resident Physician, Department of Surgery, School of Medical Sciences, Universidade Estadual de Campinas (UNICAMP), Campinas, Brazil
| | - Martinho Antonio Gestic
- MD, MSc. Assistant Physician, Department of Surgery, School of Medical Sciences, Universidade Estadual de Campinas (UNICAMP), Campinas, Brazil
| | - Murillo Pimentel Utrini
- MD. Assistant Physician, Department of Surgery, School of Medical Sciences, Universidade Estadual de Campinas (UNICAMP), Campinas, Brazil
| | - Felipe David Mendonça Chaim
- MD, PhD. Assistant Physician, Department of Surgery, School of Medical Sciences, Universidade Estadual de Campinas (UNICAMP), Campinas, Brazil
| | - Elinton Adami Chaim
- MD, PhD. Full Professor, Department of Surgery, School of Medical Sciences, Universidade Estadual de Campinas (UNICAMP), Campinas, Brazil
| | - Everton Cazzo
- MD, PhD. Associate Professor, Department of Surgery, School of Medical Sciences, Universidade Estadual Campinas (UNICAMP), Campinas, Brazil
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14
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Helicobacter pylori infection eradication for nonalcoholic fatty liver disease: a randomized controlled trial. Sci Rep 2022; 12:19530. [PMID: 36376474 PMCID: PMC9663549 DOI: 10.1038/s41598-022-23746-0] [Citation(s) in RCA: 7] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/10/2022] [Accepted: 11/04/2022] [Indexed: 11/16/2022] Open
Abstract
Previous studies have suggested that Helicobacter pylori (H. pylori) infection is associated with nonalcoholic fatty liver disease (NAFLD). The purpose of the present study was to investigate the effect of H. pylori eradication treatment on NAFLD patients. Two hundred NAFLD patients who tested positive for H. pylori infection were randomized into the H. pylori eradication treatment group or the control group. Metabolic and inflammatory parameters and FibroScan were measured in all subjects at baseline and 1 year after treatment. At 1 year after treatment, the decrease in metabolic indicators, such as fasting blood glucose, glycosylated haemoglobin, homeostasis model assessment of insulin resistance (HOMA-IR), triglycerides, body mass index and controlled attenuation parameter values, were more obvious in the treatment group. Moreover, the inflammatory indicators white blood count and high-sensitivity C-reactive protein (hs-CRP) and the inflammatory factors interleukin 6 (IL-6) and tumour necrosis factor-α (TNF-α) were also significantly decreased. H. pylori eradication can further reduce the metabolic indices of NAFLD and the degree of liver steatosis. H. pylori infection may participate in the occurrence and development of NAFLD through its influence on inflammatory factors. Thus, checking for the presence of H. pylori infection in patients at risk of NAFLD may be beneficial.
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15
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Gonciarz W, Lechowicz Ł, Urbaniak M, Rechciński T, Chałubiński M, Broncel M, Kaca W, Chmiela M. Searching for serum biomarkers linking coronary heart disease and Helicobacter pylori infection using infrared spectroscopy and artificial neural networks. Sci Rep 2022; 12:18284. [PMID: 36316430 PMCID: PMC9622908 DOI: 10.1038/s41598-022-23191-z] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/16/2022] [Accepted: 10/26/2022] [Indexed: 11/07/2022] Open
Abstract
Helicobacter pylori (Hp) Gram-negative bacteria cause gastritis or gastric ulcers. They may be involved in the development of systemic diseases i.e. coronary heart disease (CHD). Both Hp infection and CHD are related to inflammation accompanied by C-reactive protein (CRP), tumor necrosis factor alfa (TNF-α) and homocysteine. Low density lipoprotein (LDL) and triglicerides are a classic risk factors of CHD. Infrared spectroscopy has been introduced for monitoring chronic infections or endogenous disorders using specific absorption bands for biocomponents typed as diagnostic markers. In this study we selected specific motives of infrared radiation (IR) spectra for the sera from CHD patients infected with Hp. In total 141 sera were used: 90 from patients with CHD, all Hp positive, and 51 from healthy donors, 32 Hp negative and 21 Hp positive. Hp status was evaluated by anti-Hp IgG antibodies and/or 13C urea breath testing. IR spectra were measured using FT-IR/FT-NIR Spectrum 400 spectrometer (PerkinElmer) chemometrically analyzed using artificial neural networks and they showed differences in absorption bands corresponding to triglicerides, CRP, homocysteine, LDL and TNF-α, and selected component groups between CHD patients infected with Hp vs healthy uninfected donors (96.15% accuracy). Triglicerides and CRP were the best biomarkers linking Hp infection with CHD.
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Affiliation(s)
- Weronika Gonciarz
- grid.10789.370000 0000 9730 2769Department of Immunology and Infectious Biology, Faculty of Biology and Environmental Protection, University of Lodz, Banacha 12/16, 90-237 Lodz, Poland ,grid.411821.f0000 0001 2292 9126Department of Synthesis and Structural Research, Faculty of Natural Sciences, Jan Kochanowski University, Świętokrzyska 11, 25-406 Kielce, Poland
| | - Łukasz Lechowicz
- grid.411821.f0000 0001 2292 9126Departament of Microbiology, Faculty of Natural Sciences, Jan Kochanowski University, Świętokrzyska 11, 25-406 Kielce, Poland
| | - Mariusz Urbaniak
- grid.411821.f0000 0001 2292 9126Department of Synthesis and Structural Research, Faculty of Natural Sciences, Jan Kochanowski University, Świętokrzyska 11, 25-406 Kielce, Poland
| | - Tomasz Rechciński
- grid.8267.b0000 0001 2165 3025Clinic and Department of Cardiology, Medical University of Lodz, 92-213 Lodz, Poland
| | - Maciej Chałubiński
- grid.8267.b0000 0001 2165 3025Department of Immunology and Allergy, Medical University of Lodz, Pomorska 251, 91-347 Lodz, Poland
| | - Marlena Broncel
- grid.8267.b0000 0001 2165 3025Laboratory of Tissue Immunopharmacology, Department of Internal Diseases and Clinical Pharmacology, Medical University of Lodz, Kniaziewicza 1/5, 91-347 Lodz, Poland
| | - Wiesław Kaca
- grid.411821.f0000 0001 2292 9126Departament of Microbiology, Faculty of Natural Sciences, Jan Kochanowski University, Świętokrzyska 11, 25-406 Kielce, Poland
| | - Magdalena Chmiela
- grid.10789.370000 0000 9730 2769Department of Immunology and Infectious Biology, Faculty of Biology and Environmental Protection, University of Lodz, Banacha 12/16, 90-237 Lodz, Poland
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16
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Wu Y, Zeng H, Zhang M, Li C, Tang Y, Li X, Yuan S, Wei Q, Wang J, Ning X, Zhang X. Sex-Specific Risk Factors Associated with Helicobacter pylori Infection Among Individuals Undergoing Health Examinations in China. Int J Gen Med 2022; 15:5861-5868. [PMID: 35791315 PMCID: PMC9250778 DOI: 10.2147/ijgm.s367142] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/19/2022] [Accepted: 05/27/2022] [Indexed: 11/23/2022] Open
Abstract
Purpose Helicobacter pylori is one of the most common causes of peptic ulcers, gastritis, and gastric cancers. This study investigated sex-specific differences in the prevalence of H. pylori infection and its associated factors among individuals undergoing hospital-based health examinations in southern China. Methods This study enrolled consecutive healthy individuals who underwent regular health examinations at a hospital physical examination center between September 2020 and September 2021. Anthropometric characteristics and biochemical profiles were measured. All individuals underwent carbon-13 urea breath tests. Univariate and multivariate analyses were used to evaluate the factors associated with H. pylori infection. Results A total of 5035 individuals (men, 59.1%; women, 40.9%) were included in the analyses. The total rate of H. pylori infection was 35.0% (men, 35.5%; women, 34.3%). In the multivariate analysis, the risk factors identified for H. pylori infections were high fasting blood glucose levels and blood pressure ≥160 mmHg in men and older age, high body mass index, and low albumin levels in women. Conclusion These findings suggest that physicians must be aware of the metabolic factors associated with H. pylori infections in the Chinese population. Early detection of these factors and timely intervention are expected to reduce H. pylori infections and provide a theoretical basis for the primary prevention of several gastrointestinal diseases.
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Affiliation(s)
- Yumei Wu
- Department of Gastroenterology, the Third People's Hospital of Shenzhen, Shenzhen, Guangdong Province, People's Republic of China
| | - Hui Zeng
- Department of Health Management, the Third People's Hospital of Shenzhen, Shenzhen, Guangdong Province, People's Republic of China
| | - Meiping Zhang
- Department of Gastroenterology, the Third People's Hospital of Shenzhen, Shenzhen, Guangdong Province, People's Republic of China
| | - Chunyan Li
- Department of Health Management, the Third People's Hospital of Shenzhen, Shenzhen, Guangdong Province, People's Republic of China
| | - Yuanlin Tang
- Department of Health Management, the Third People's Hospital of Shenzhen, Shenzhen, Guangdong Province, People's Republic of China
| | - Xiufen Li
- Department of Gastroenterology, the Third People's Hospital of Shenzhen, Shenzhen, Guangdong Province, People's Republic of China
| | - Shanyou Yuan
- Department of Orthopedics, the Third People's Hospital of Shenzhen, Shenzhen, Guangdong Province, People's Republic of China
| | - Qifeng Wei
- Department of Orthopedics, the Third People's Hospital of Shenzhen, Shenzhen, Guangdong Province, People's Republic of China
| | - Jinghua Wang
- Centre of Clinical Epidemiology, the Third People's Hospital of Shenzhen, Shenzhen, Guangdong Province, People's Republic of China
| | - Xianjia Ning
- Centre of Clinical Epidemiology, the Third People's Hospital of Shenzhen, Shenzhen, Guangdong Province, People's Republic of China
| | - Xiaoyin Zhang
- Department of Gastroenterology, the Third People's Hospital of Shenzhen, Shenzhen, Guangdong Province, People's Republic of China
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Association of Helicobacter pylori Infection with Papillary Thyroid Carcinoma: A Case-control Study. INTERNATIONAL JOURNAL OF CANCER MANAGEMENT 2022. [DOI: 10.5812/ijcm-118031] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/16/2022]
Abstract
Background: The thyroid nodules incidence has risen worldwide. Although factors such as increasing the use of imaging techniques and more rapid detection of small thyroid nodules have been implicated in the recent rise in thyroid cancer incidence, some environmental parameters such as infectious agents may be involved. Helicobacter pylori infection is an environmental risk factor, which may mimic the antigenic properties of membranes of thyrocytes. Objectives: This study aimed at evaluating the association of H. pylori infection with benign and malignant thyroid nodules in comparison with the control group. Methods: Patients with benign thyroid nodules, papillary thyroid cancer (PTC), and euthyroid healthy controls without thyroid nodules that had just been diagnosed were included in the study. All participants underwent clinical examination. Various biochemical parameters such as serum H. pylori Ab (IgG) and thyroid function tests were measured. Comparisons were made between groups. Results: Finally, 370 patients with benign thyroid nodules, 364 patients with PTC, and 360 healthy subjects without nodules participated as a control group. In the patients with PTC, the prevalence of H. pylori infection was 89.6%, while in the group of patients with benign thyroid nodules and the control group was 81.1% and 75%, respectively (P < 0.001). Helicobacter pylori antibody (Ab) titer was not significantly associated with any of the anthropometric and biochemical variables. Conclusions: Helicobacter pylori infection was significantly higher in patients with benign thyroid nodules and PTC than in the control group. Also, the rate of infection was significantly higher in the malignant nodule group than in the benign thyroid nodules group.
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18
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Kim WS, Choi Y, Kim N, Lim SH, Noh G, Kim KW, Park J, Jo H, Yoon H, Shin CM, Park YS, Lee DH. Long-term effect of the eradication of Helicobacter pylori on the hemoglobin A1c in type 2 diabetes or prediabetes patients. Korean J Intern Med 2022; 37:579-590. [PMID: 34991230 PMCID: PMC9082431 DOI: 10.3904/kjim.2021.194] [Citation(s) in RCA: 7] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/18/2021] [Accepted: 10/25/2021] [Indexed: 11/27/2022] Open
Abstract
BACKGROUND/AIMS The long-term effect of Helicobacter pylori eradication on the metabolic syndrome or diabetes are unclear. The aim of this study was to evaluate the effect of H. pylori eradication on glycemic control in type 2 diabetes mellitus (T2DM) or prediabetes mellitus (preDM). METHODS A total of 124 asymptomatic subjects with T2DM or preDM were divided into H. pylori-negative (n = 40), H. pylori-positive with non-eradicated (n = 34), and eradicated (n = 50) groups. We measured H. pylori status (culture, histology, and rapid urease test) and glycated hemoglobin A1c (A1C) levels and followed-up at the 1st year and the 5th year of follow-up. RESULTS The A1C levels significantly decreased in the eradicated group compared to the negative group and the non-eradicated groups (at the 1st year, p = 0.024; at the 5th year, p = 0.009). The A1C levels decreased in male, and/or subjects < 65 years of age in subgroup analyses (in male subjects, p = 0.047 and p = 0.020 at the 1st and the 5th year; in subjects < 65 years of age, p = 0.028 and p = 0.006 at the 1st and the 5th year; in male subjects < 65 years of age, p = 0.039 and p = 0.032 at the 1st and the 5th year). The eradication of H. pylori was related to the decrease in A1C values throughout the follow-up period, compared to the non-eradicated group (p = 0.017). CONCLUSION H. pylori eradication was related to the decreasing of A1C levels in patients with T2DM or preDM over a long-term follow-up period, especially in male and subjects < 65 years of age.
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Affiliation(s)
- Won Seok Kim
- Department of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, Korea
| | - Yonghoon Choi
- Department of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, Korea
| | - Nayoung Kim
- Department of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, Korea
- Department of Internal Medicine and Liver Research Institute, Seoul National University College of Medicine, Seoul, Korea
| | - Seon Hee Lim
- Department of Internal Medicine, Seoul National University Hospital Healthcare System Gangnam Center and Healthcare Research Institute, Seoul, Korea
| | - Gitark Noh
- Department of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, Korea
| | - Ki Wook Kim
- Department of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, Korea
| | - Jaehyung Park
- Department of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, Korea
| | - Hyeongho Jo
- Department of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, Korea
| | - Hyuk Yoon
- Department of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, Korea
| | - Cheol Min Shin
- Department of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, Korea
| | - Young Soo Park
- Department of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, Korea
| | - Dong Ho Lee
- Department of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, Korea
- Department of Internal Medicine and Liver Research Institute, Seoul National University College of Medicine, Seoul, Korea
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Kim JW, Kim TJ, Kim JE, Na JE, Lee H, Min BH, Lee JH, Rhee PL, Kim JJ. Impact of Helicobacter pylori Eradication on the Risk of Incident Nonalcoholic Fatty Liver Disease: A Cohort Study. THE KOREAN JOURNAL OF HELICOBACTER AND UPPER GASTROINTESTINAL RESEARCH 2022. [DOI: 10.7704/kjhugr.2021.0060] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 11/22/2022]
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Choi JM, Park HE, Han YM, Lee J, Lee H, Chung SJ, Lim SH, Yim JY, Chung GE. Non-alcoholic/Metabolic-Associated Fatty Liver Disease and Helicobacter pylori Additively Increase the Risk of Arterial Stiffness. Front Med (Lausanne) 2022; 9:844954. [PMID: 35280895 PMCID: PMC8914072 DOI: 10.3389/fmed.2022.844954] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/07/2022] [Accepted: 02/01/2022] [Indexed: 11/13/2022] Open
Abstract
BackgroundNon-alcoholic fatty liver disease (NAFLD) and Helicobacter pylori (Hp) infection have a close association with an increased risk of cardiovascular disease. Metabolic dysfunction-associated fatty liver disease (MAFLD) is characterized by metabolic dysfunction in NAFLD. We investigated the synergistic effects of NAFLD/MAFLD and Hp infection on the risk of arterial stiffness in an asymptomatic population.MethodsWe included individuals who underwent abdominal ultrasonography, anti-Hp IgG antibody evaluations and cardio-ankle vascular index (CAVI) during health screening tests between January 2013 and December 2017. Arterial stiffness was defined using CAVI. A logistic regression model was used to analyze the independent and synergistic effects of NAFLD/MAFLD and Hp infection on the risk of arterial stiffness.ResultsAmong 3,195 subjects (mean age 54.7 years, 68.5% male), the prevalence of increased arterial stiffness was 36.4%. In the multivariate analysis, subjects with NAFLD but without Hp infection and those with both NAFLD and Hp infection had a significantly higher risk of increased arterial stiffness [odds ratio (OR) 1.61, 95% confidence interval (CI) 1.15–2.26, and OR 2.23, 95% CI 1.63–3.06, respectively], than subjects without Hp infection and NAFLD. Regarding MAFLD, Hp infection additively increased the risk of arterial stiffness in subjects with MAFLD (OR 2.13, 95% CI 1.64–2.78).ConclusionsAn interactive effect of Hp infection on the risk of arterial stiffness in individuals with NAFLD/MAFLD was observed. Hp infection additively increases the risk of arterial stiffness in subjects with NAFLD or MAFLD.
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Affiliation(s)
- Ji Min Choi
- Division of Gastroenterology and Hepatology, Department of Internal Medicine, Seoul National University Hospital Healthcare System Gangnam Center, Seoul, South Korea
| | - Hyo Eun Park
- Division of Cardiology, Department of Internal Medicine, Seoul National University Hospital Healthcare System Gangnam Center, Seoul, South Korea
| | - Yoo Min Han
- Division of Gastroenterology and Hepatology, Department of Internal Medicine, Seoul National University Hospital Healthcare System Gangnam Center, Seoul, South Korea
| | - Jooyoung Lee
- Division of Gastroenterology and Hepatology, Department of Internal Medicine, Seoul National University Hospital Healthcare System Gangnam Center, Seoul, South Korea
| | - Heesun Lee
- Division of Cardiology, Department of Internal Medicine, Seoul National University Hospital Healthcare System Gangnam Center, Seoul, South Korea
| | - Su Jin Chung
- Division of Gastroenterology and Hepatology, Department of Internal Medicine, Seoul National University Hospital Healthcare System Gangnam Center, Seoul, South Korea
| | - Seon Hee Lim
- Division of Gastroenterology and Hepatology, Department of Internal Medicine, Seoul National University Hospital Healthcare System Gangnam Center, Seoul, South Korea
| | - Jeong Yoon Yim
- Division of Gastroenterology and Hepatology, Department of Internal Medicine, Seoul National University Hospital Healthcare System Gangnam Center, Seoul, South Korea
| | - Goh Eun Chung
- Division of Gastroenterology and Hepatology, Department of Internal Medicine, Seoul National University Hospital Healthcare System Gangnam Center, Seoul, South Korea
- *Correspondence: Goh Eun Chung
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Jamil MZZ, Salman S, Akhtar M, Iqbal S, Bhalli A, Farooq H. Determining the Association Between Helicobacter pylori Infection and Treatment-Refractory Hypothyroidism. Cureus 2022; 14:e21316. [PMID: 35186575 PMCID: PMC8848460 DOI: 10.7759/cureus.21316] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 01/16/2022] [Indexed: 12/03/2022] Open
Abstract
Introduction Refractory hypothyroidism, despite weight-based thyroxine dosing, is a common endocrinology consultation in outpatients. Chronic Helicobacter (H.) pylori infection has been reported to be responsible for the poor absorption of thyroxine from the small gut leading to suboptimal response with contradictory evidence. This study was carried out to determine the association of chronic Helicobacter pylori infection with refractory hypothyroidism in outpatients presenting to a tertiary care hospital. Methods One hundred thirty patients with the diagnosis of hypothyroidism, visiting Jinnah Allama Iqbal Institute of Diabetes and Endocrinology (JAIDE) Jinnah Hospital Lahore, Pakistan, from January 2020 to February 2021, were included in the study after informed consent following the non-probability consecutive sampling technique. All of these patients were 15-70 years of age, non-pregnant, and receiving thyroxine treatment for at least six weeks. Patients with a history of gastric surgery, malabsorption syndrome, or poor compliance were excluded from the study. Patients’ age, sex, and body mass index (BMI) were recorded in a structured proforma. Patients were categorized into two groups, i.e. controls (biochemically euthyroid on thyroxine treatment with TSH < 4.5mU/L) and cases (refractory hypothyroidism despite 1.6 mcg/kg thyroxine treatment with TSH > 4.5 mU/L). The presence of chronic H. pylori infection was checked with serum immunoglobulin G (IgG) testing by enzyme-linked immunoassay (ELISA) from the hospital laboratory and data analysis was done by SPSS version 21.0 (IBM Corp., Armonk, NY). Results One hundred thirty patients were included in this study, with an age range from 15 to 70 years. Of these, 65/130 (50%) were euthyroid on treatment and 65/130 (50%) had treatment-refractory hypothyroidism. The mean age of patients in our study was 45.81 ± 11 years, with 118 (90.8%) female patients. The prevalence of positive H. pylori IgG antibody was 47/130 (36.2%) overall, with 23 patients (35.4%) in the control (euthyroid) group and 24 patients (36.9%) in the cases (refractory hypothyroidism) group. The difference between the two groups was not statistically significant with an odds ratio of 1.069 (CI 0.523 - 2.187) and a p-value of 0.855. Moreover, age, gender, and BMI had no effect on chronic H. pylori association with refractory hypothyroidism. Conclusion This study does not suggest any significant association between chronic H. pylori infection and treatment-refractory hypothyroidism. Other factors like poor compliance, drug-drug interactions, and malabsorption disorders should be preferably sought in case of refractory hypothyroidism.
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Liu Y, Li D, Liu Y, Shuai P. Association Between Helicobacter Pylori Infection and Non-alcoholic Fatty Liver Disease, Hepatic Adipose Deposition and Stiffness in Southwest China. Front Med (Lausanne) 2022; 8:764472. [PMID: 35004736 PMCID: PMC8739268 DOI: 10.3389/fmed.2021.764472] [Citation(s) in RCA: 10] [Impact Index Per Article: 3.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/08/2021] [Accepted: 12/02/2021] [Indexed: 12/12/2022] Open
Abstract
Background: Both nonalcoholic fatty liver disease (NAFLD) and Helicobacter pylori (H. pylori) infection have high prevalence worldwide, and the relationship between both remains controversial. We try to investigate whether H. pylori infection is associated with NAFLD and increased liver fat deposition and stiffness in this cross-sectional study. Methods: The physical examination data of 5,665 subjects were obtained from February 2018 to June 2019 in this study. Clinical and biochemical data were collected. NAFLD was diagnosed using abdominal color Doppler ultrasonography. Liver steatosis and stiffness were understood by two parameters of transient elastography (TE): fat attenuation parameter (FAP) and liver stiffness measurement (LSM). H. pylori infection was determined using the 13C urea breath tests. Results: The total prevalence of NAFLD and H. pylori infection was 30.2 and 37.0%, respectively. In men, the prevalence of NAFLD and the levels of FAP and LSM in H. pylori-positive group were significantly higher than H. pylori-negative group (all p < 0.01), but no significant difference was found in women. In men, the infection rate of H. pylori in NAFLD group and LSM ≥ 7.4 kPa group was significantly higher than control group. Multivariate logistic regression analysis revealed that H. pylori infection was not independently associated with NAFLD and FAP ≥ 240 dB/m. However, H. pylori infection was associated with LSM ≥ 7.4 kPa in men. Conclusions: Our study suggests that H. pylori infection is not significantly associated with NAFLD and elevated liver steatosis, whereas it may be the risk factor of elevated liver stiffness in men.
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Affiliation(s)
- Ying Liu
- Health Management Center, Sichuan Provincial People's Hospital, University of Electronic Science and Technology of China, Chengdu, China.,Chinese Academy of Sciences Sichuan Translational Medicine Research Hospital, Chengdu, China
| | - Dongyu Li
- Health Management Center, Sichuan Provincial People's Hospital, University of Electronic Science and Technology of China, Chengdu, China.,Chinese Academy of Sciences Sichuan Translational Medicine Research Hospital, Chengdu, China
| | - Yuping Liu
- Health Management Center, Sichuan Provincial People's Hospital, University of Electronic Science and Technology of China, Chengdu, China.,Chinese Academy of Sciences Sichuan Translational Medicine Research Hospital, Chengdu, China
| | - Ping Shuai
- Health Management Center, Sichuan Provincial People's Hospital, University of Electronic Science and Technology of China, Chengdu, China.,Chinese Academy of Sciences Sichuan Translational Medicine Research Hospital, Chengdu, China
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23
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Hegazy WAH, Rajab AAH, Abu Lila AS, Abbas HA. Anti-diabetics and antimicrobials: Harmony of mutual interplay. World J Diabetes 2021; 12:1832-1855. [PMID: 34888011 PMCID: PMC8613656 DOI: 10.4239/wjd.v12.i11.1832] [Citation(s) in RCA: 30] [Impact Index Per Article: 7.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/03/2021] [Revised: 06/26/2021] [Accepted: 10/25/2021] [Indexed: 02/06/2023] Open
Abstract
Diabetes is one of the four major non-communicable diseases, and appointed by the world health organization as the seventh leading cause of death worldwide. The scientists have turned over every rock in the corners of medical sciences in order to come up with better understanding and hence more effective treatments of diabetes. The continuous research on the subject has elucidated the role of immune disorders and inflammation as definitive factors in the trajectory of diabetes, assuring that blood glucose adjustments would result in a relief in the systemic stress leading to minimizing inflammation. On a parallel basis, microbial infections usually take advantage of immunity disorders and propagate creating a pro-inflammatory environment, all of which can be reversed by antimicrobial treatment. Standing at the crossroads between diabetes, immunity and infection, we aim in this review at projecting the interplay between immunity and diabetes, shedding the light on the overlapping playgrounds for the activity of some antimicrobial and anti-diabetic agents. Furthermore, we focused on the anti-diabetic drugs that can confer antimicrobial or anti-virulence activities.
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Affiliation(s)
- Wael A H Hegazy
- Department of Microbiology and Immunology, Zagazig University, Zagzig 44519, Egypt
| | - Azza A H Rajab
- Department of Microbiology and Immunology, Zagazig University, Zagzig 44519, Egypt
| | - Amr S Abu Lila
- Department of Pharmaceutics, Zagazig University, Faculty of Pharmacy, Zagzig 44519, Egypt
- Department of Pharmaceutics, College of Pharmacy, University of Hail, Hail 81442, Saudi Arabia
| | - Hisham A Abbas
- Department of Microbiology and Immunology, Zagazig University, Zagzig 44519, Egypt
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24
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Increased Glycated Hemoglobin but Decreased Cholesterol after a Loss of Helicobacter pylori Infection: A Community-Based Longitudinal Metabolic Parameters Follow-Up Study. J Pers Med 2021; 11:jpm11100997. [PMID: 34683138 PMCID: PMC8538159 DOI: 10.3390/jpm11100997] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/29/2021] [Revised: 09/25/2021] [Accepted: 09/28/2021] [Indexed: 11/16/2022] Open
Abstract
This study aimed to evaluate the impact of Helicobacter pylori (H. pylori) infection on metabolic parameters in a longitudinal follow-up manner. From August 2013 to August 2019, a community-based prospective study of H. pylori and metabolic syndrome (MetS) was performed in the northeastern region of Taiwan. A total of 1865 subjects were divided into four groups according to the serial results of urea breath test (UBT): new H. pylori infection (group 1, n = 41), null H. pylori infection (group 2, n = 897), loss of H. pylori infection (group 3, n = 369), and persistent H. pylori infection (group 4, n = 558). When comparing the subjects between groups 1 and 2, HBA1c was associated with a new H. pylori infection. Body mass index (BMI) was associated with a loss of H. pylori when comparing subjects between groups 3 and 4. Elevated HBA1c and high-density lipoprotein (HDL) levels but lower values of cholesterol and white blood cells (WBCs) were found during serial analyses within group 3. Conclusively, HBA1c was associated with a new H. pylori infection. BMI was associated with H. pylori loss. Increased HBA1c and HDL values but decreased values of cholesterol and WBC were associated with a loss of H. pylori infection.
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25
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Weng CY, Xu JL, Sun SP, Wang KJ, Lv B. Helicobacter pylori eradication: Exploring its impacts on the gastric mucosa. World J Gastroenterol 2021; 27:5152-5170. [PMID: 34497441 PMCID: PMC8384747 DOI: 10.3748/wjg.v27.i31.5152] [Citation(s) in RCA: 13] [Impact Index Per Article: 3.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/14/2021] [Revised: 06/14/2021] [Accepted: 07/15/2021] [Indexed: 02/06/2023] Open
Abstract
Helicobacter pylori (H. pylori) infects approximately 50% of all humans globally. Persistent H. pylori infection causes multiple gastric and extragastric diseases, indicating the importance of early diagnosis and timely treatment. H. pylori eradication produces dramatic changes in the gastric mucosa, resulting in restored function. Consequently, to better understand the importance of H. pylori eradication and clarify the subsequent recovery of gastric mucosal functions after eradication, we summarize histological, endoscopic, and gastric microbiota changes to assess the therapeutic effects on the gastric mucosa.
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Affiliation(s)
- Chun-Yan Weng
- Department of Gastroenterology, The First Clinical Medical College of Zhejiang Chinese Medical University, Hangzhou 310053, Zhejiang Province, China
| | - Jing-Li Xu
- Department of Gastrointestinal Surgery, The First Clinical Medical College of Zhejiang Chinese Medical University, Hangzhou 310053, Zhejiang Province, China
| | - Shao-Peng Sun
- Department of Gastroenterology, The First Clinical Medical College of Zhejiang Chinese Medical University, Hangzhou 310053, Zhejiang Province, China
| | - Kai-Jie Wang
- Department of Gastroenterology, The First Clinical Medical College of Zhejiang Chinese Medical University, Hangzhou 310053, Zhejiang Province, China
| | - Bin Lv
- Department of Gastroenterology, The First Clinical Medical College of Zhejiang Chinese Medical University, Hangzhou 310053, Zhejiang Province, China
- Department of Gastroenterology, The First Affiliated Hospital of Zhejiang Chinese Medical University, Hangzhou 310006, Zhejiang Province, China
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Abstract
Helicobacter pylori is the most prevalent infection worldwide, while non-alcoholic fatty liver disease emerged as the most frequent liver disease. The common occurrence can be either by chance or due to certain pathogenetic factors. Epidemiologic studies revealed that the risk of non-alcoholic liver disease is increased in patients infected with Helicobacter pylori. DNA fragments of Helicobacter pylori were rarely identified in human samples of liver carcinoma and fatty liver. Helicobacter pylori could influence the development of non-alcoholic fatty liver either by hormonal (ghrelin? gastrin? insulin?), or by effect of pro-inflammatory cytokines (interleukin 1 and 8, tumor necrosis factor ɑ, interferon ɣ) and by changes of gut microbiome as well. Probiotic supplementation could improve some clinical parameters of non-alcoholic fatty liver disease and eradication rates of Helicobacter pylori. Regimens used for eradication can be safely administered, although non-alcoholic fatty liver increases the risk of drug-induced liver damage. Controlled studies of the effect of eradication on the development and progression of non-alcoholic fatty liver are warranted.
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Affiliation(s)
- György M Buzás
- Department of Gastroenterology, Ferencváros Health Center, Budapest, Hungary -
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27
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Doulberis M, Pierre NT, Manzini G, Papaefthymiou A, Kountouras J, Klukowska-Rötzler J, Polyzos SA, Srivastava S, Exadaktylos AK, Knuchel J, Kuntzen T, Srivastava DS. Helicobacter pylori-Related Metabolic Parameters and Premalignant Gastric Mucosa Histological Lesions in Swiss Bariatric Patients. Microorganisms 2021; 9:microorganisms9071361. [PMID: 34201748 PMCID: PMC8303942 DOI: 10.3390/microorganisms9071361] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/28/2021] [Revised: 06/16/2021] [Accepted: 06/21/2021] [Indexed: 02/08/2023] Open
Abstract
Obesity, as a major risk factor of metabolic syndrome (MetS), represents a pandemic, especially in Western societies, and is considered a risk factor for malignancies. Helicobacter pylori (Hp), is a definite carcinogen with global distribution. We aimed to investigate, for the first time in Switzerland, the main gastric mucosa premalignant histological lesions of bariatric patients in correlation with MetS components and Hp Infection (Hp-I). By reviewing retrospectively 94304 patient cases, a total of 116 eligible patients having undergone bariatric surgery were identified. The mean patient age was 48.66 years. Hp(+) patients were 24% (28/116). Presence of gastric mucosa atrophy was documented in 8/28 Hp(+) patients (29%) and (2/88) Hp(-) ones (2%) (p = 0.006). Gastric mucosa intestinal metaplasia was observed in 14/28 (50%) Hp(+) patients versus 3/88 (3.4%) of Hp(-) group (p < 0.0001). Hp(+) patients exhibited statistically higher arterial hypertension (p = 0.033). The homeostatic model of assessment insulin resistance was also statistically significantly higher for the Hp(+) group (p < 0.001). In a multivariate analysis, including arterial hypertension, gastric mucosa atrophy, and intestinal metaplasia as variables, statistical significance remained only for intestinal metaplasia (p = 0.001). In conclusion, Hp-I is associated with premalignant gastric mucosa histologic lesions and MetS components, including arterial hypertension and IR. Further large-scale prospective studies are required to confirm these findings.
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Affiliation(s)
- Michael Doulberis
- Emergency Department, University Hospital Inselspital of Bern, 3010 Bern, Switzerland; (N.T.P.); (J.K.-R.); (A.K.E.); (D.S.S.)
- Division of Gastroenterology and Hepatology, Medical University Department, Kantonsspital Aarau, 5001 Aarau, Switzerland; (J.K.); (T.K.)
- Second Medical Clinic, School of Medicine, Aristotle University of Thessaloniki, Ippokration Hospital, 54642 Thessaloniki, Macedonia, Greece; (A.P.); (J.K.)
- First Laboratory of Pharmacology, Aristotle University of Thessaloniki, 54124 Thessaloniki, Macedonia, Greece;
- Correspondence:
| | - Noah Thierry Pierre
- Emergency Department, University Hospital Inselspital of Bern, 3010 Bern, Switzerland; (N.T.P.); (J.K.-R.); (A.K.E.); (D.S.S.)
- Private Practice, 4704 Niederbipp, Switzerland
| | - Giulia Manzini
- Department of General and Visceral Surgery, Kantonsspital Aarau, 5001 Aarau, Switzerland;
| | - Apostolis Papaefthymiou
- Second Medical Clinic, School of Medicine, Aristotle University of Thessaloniki, Ippokration Hospital, 54642 Thessaloniki, Macedonia, Greece; (A.P.); (J.K.)
- First Laboratory of Pharmacology, Aristotle University of Thessaloniki, 54124 Thessaloniki, Macedonia, Greece;
- Department of Gastroenterology, University Hospital of Larisa, Mezourlo, 41110 Larisa, Thessaly, Greece
| | - Jannis Kountouras
- Second Medical Clinic, School of Medicine, Aristotle University of Thessaloniki, Ippokration Hospital, 54642 Thessaloniki, Macedonia, Greece; (A.P.); (J.K.)
| | - Jolanta Klukowska-Rötzler
- Emergency Department, University Hospital Inselspital of Bern, 3010 Bern, Switzerland; (N.T.P.); (J.K.-R.); (A.K.E.); (D.S.S.)
| | - Stergios A. Polyzos
- First Laboratory of Pharmacology, Aristotle University of Thessaloniki, 54124 Thessaloniki, Macedonia, Greece;
| | | | - Aristomenis K. Exadaktylos
- Emergency Department, University Hospital Inselspital of Bern, 3010 Bern, Switzerland; (N.T.P.); (J.K.-R.); (A.K.E.); (D.S.S.)
| | - Jürg Knuchel
- Division of Gastroenterology and Hepatology, Medical University Department, Kantonsspital Aarau, 5001 Aarau, Switzerland; (J.K.); (T.K.)
| | - Thomas Kuntzen
- Division of Gastroenterology and Hepatology, Medical University Department, Kantonsspital Aarau, 5001 Aarau, Switzerland; (J.K.); (T.K.)
| | - David S. Srivastava
- Emergency Department, University Hospital Inselspital of Bern, 3010 Bern, Switzerland; (N.T.P.); (J.K.-R.); (A.K.E.); (D.S.S.)
- Department of General Internal Medicine, Kliniken Hirslanden Beau-Site, 3013 Bern, Switzerland
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Polyzos SA, Papaefthymiou A, Doulberis M, Mavridoglou G, Kountouras J. Helicobacter pylori infection and diabetes mellitus. Diabetes Metab Syndr 2021; 15:845-846. [PMID: 33873053 DOI: 10.1016/j.dsx.2021.03.034] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 03/07/2021] [Accepted: 03/30/2021] [Indexed: 01/09/2023]
Affiliation(s)
- Stergios A Polyzos
- First Laboratory of Pharmacology, School of Medicine, Aristotle University of Thessaloniki, Thessaloniki, Greece.
| | - Apostolis Papaefthymiou
- First Laboratory of Pharmacology, School of Medicine, Aristotle University of Thessaloniki, Thessaloniki, Greece; Department of Gastroenterology, University Hospital of Larissa, Thessaly, Greece
| | - Michael Doulberis
- First Laboratory of Pharmacology, School of Medicine, Aristotle University of Thessaloniki, Thessaloniki, Greece; Division of Gastroenterology and Hepatology, Medical University Department, Kanton sspital Aarau, Aarau, Switzerland
| | - George Mavridoglou
- Department of Accounting and Finance, University of Peloponnese, Kalamata, Greece
| | - Jannis Kountouras
- Second Medical Clinic, School of Medicine, Aristotle University of Thessaloniki, Ippokration Hospital, Thessaloniki, Greece
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29
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Doulberis M, Papaefthymiou A, Srivastava DS, Exadaktylos AK, Katsinelos P, Kountouras J, Polyzos SA. Update on the association between non-alcoholic fatty liver disease and Helicobacter pylori infection. Int J Clin Pract 2021; 75:e13737. [PMID: 32991019 DOI: 10.1111/ijcp.13737] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/15/2022] Open
Affiliation(s)
- Michael Doulberis
- Division of Gastroenterology and Hepatology, Medical University Department, Kantonsspital Aarau, Aarau, Switzerland
- Second Medical Clinic, School of Medicine, Aristotle University of Thessaloniki, Ippokration Hospital, Thessaloniki, Macedonia, Greece
- First Laboratory of Pharmacology, Aristotle University of Thessaloniki, Thessaloniki, Macedonia, Greece
- Emergency Department, University Hospital Inselspital, Bern, Switzerland
| | - Apostolis Papaefthymiou
- Second Medical Clinic, School of Medicine, Aristotle University of Thessaloniki, Ippokration Hospital, Thessaloniki, Macedonia, Greece
- First Laboratory of Pharmacology, Aristotle University of Thessaloniki, Thessaloniki, Macedonia, Greece
- Department of Gastroenterology, University Hospital of Larisa, Larisa, Greece
| | - David S Srivastava
- Emergency Department, University Hospital Inselspital, Bern, Switzerland
| | | | - Panagiotis Katsinelos
- Second Medical Clinic, School of Medicine, Aristotle University of Thessaloniki, Ippokration Hospital, Thessaloniki, Macedonia, Greece
| | - Jannis Kountouras
- Second Medical Clinic, School of Medicine, Aristotle University of Thessaloniki, Ippokration Hospital, Thessaloniki, Macedonia, Greece
| | - Stergios A Polyzos
- Second Medical Clinic, School of Medicine, Aristotle University of Thessaloniki, Ippokration Hospital, Thessaloniki, Macedonia, Greece
- First Laboratory of Pharmacology, Aristotle University of Thessaloniki, Thessaloniki, Macedonia, Greece
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30
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Song X, Cai C, Jin Q, Chen X, Yu C. The efficacy of Helicobacter pylori eradication in diabetics and its effect on glycemic control: A systematic review and meta-analysis. Helicobacter 2021; 26:e12781. [PMID: 33465265 DOI: 10.1111/hel.12781] [Citation(s) in RCA: 24] [Impact Index Per Article: 6.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 11/17/2020] [Revised: 12/15/2020] [Accepted: 12/15/2020] [Indexed: 01/30/2023]
Abstract
BACKGROUND AND AIMS Previous studies have revealed the association between Helicobacter pylori (H. pylori) and diabetes mellitus, but conflicts still exist. The present study tried to investigate the underlying link between these two diseases by making comprehensive analyses of the impact of diabetes on H. pylori eradication and the influence of H. pylori eradication on diabetes. METHODS We systematically searched relevant studies from PubMed, Cochrane Library, Web of Science, and Embase updated to April 23, 2020. Studies examining the association between H. pylori eradication and diabetes were included. Pooled odds ratio (OR) and weighted mean differences (WMD) were calculated for different results. RESULTS Among the 2125 retrieved studies, 36 studies were included. Patients with type 2 diabetes mellitus (T2DM) have higher risk of H. pylori eradication failure than the non-diabetic one (OR = 2.59, 95% CI 1.82-3.70). Body mass index (BMI) was identified as a major factor affecting the efficacy of H. pylori eradication in diabetics, and better glycemic control was also found in eradication succeed patients (WMD: 0.51, 95% CI 0.20-0.81). Moreover, after eradication of H. pylori, improvement of HbA1c was proved (WMD = -0.33, 95% CI -0.65 to -0.02) in T2DM. CONCLUSION A higher risk of H. pylori eradication failure in T2DM was confirmed, and it was associated with BMI and glycemic control. Moreover, we also provided evidence that H. pylori eradication could improve glycemic control in patients with T2DM, which indirectly reflect the interaction between H. pylori and the diabetes.
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Affiliation(s)
- Xin Song
- Department of Gastroenterology, The First Affiliated Hospital, College of Medicine, Zhejiang University, Hangzhou, China
| | - Changzhou Cai
- Department of Gastroenterology, The First Affiliated Hospital, College of Medicine, Zhejiang University, Hangzhou, China
| | - Qi Jin
- Department of Gastroenterology, The First Affiliated Hospital, College of Medicine, Zhejiang University, Hangzhou, China
| | - Xueyang Chen
- Department of Gastroenterology, The First Affiliated Hospital, College of Medicine, Zhejiang University, Hangzhou, China
| | - Chaohui Yu
- Department of Gastroenterology, The First Affiliated Hospital, College of Medicine, Zhejiang University, Hangzhou, China
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Assessing the Relationship between Helicobacter pylori and Chronic Kidney Disease. Healthcare (Basel) 2021; 9:healthcare9020162. [PMID: 33546229 PMCID: PMC7913305 DOI: 10.3390/healthcare9020162] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/21/2020] [Revised: 01/29/2021] [Accepted: 01/31/2021] [Indexed: 01/22/2023] Open
Abstract
The relationship between Helicobacter pylori infection and/or gastric disorders and chronic kidney disease (CKD) has not been elucidated. We investigated the relationship between Helicobacter pylori and/or atrophic gastritis (AG) and chronic kidney disease. In total, 3560 participants (1127 men and 2433 women) were eligible for this cross-sectional study. We divided participants into four study groups: with/without Helicobacter pylori infection and with/without AG. The HP (+) AG (−) group demonstrated a significant association with CKD compared with the HP (−) AG (−) group (adjusted odds ratio, 1.443; 95% confidence interval, 1.047–1.989). In contrast, the HP (+) AG (+) group showed significantly lower adjusted odds of CKD than the HP (−) AG (−) group (adjusted odds ratio, 0.608; 95% confidence interval, 0.402–0.920). H. pylori infection without AG might be associated with CKD in these participants. Conversely, the HP (+) AG (+) group had lower odds of CKD. Uncovering an association between gastric and renal conditions could lead to development of new treatment strategies.
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Martin-Nuñez GM, Cornejo-Pareja I, Clemente-Postigo M, Tinahones FJ. Gut Microbiota: The Missing Link Between Helicobacter pylori Infection and Metabolic Disorders? Front Endocrinol (Lausanne) 2021; 12:639856. [PMID: 34220702 PMCID: PMC8247771 DOI: 10.3389/fendo.2021.639856] [Citation(s) in RCA: 28] [Impact Index Per Article: 7.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/10/2020] [Accepted: 05/17/2021] [Indexed: 12/14/2022] Open
Abstract
Helicobacter pylori (H. pylori) is a gram-negative bacterium that infects approximately 4.4 billion individuals worldwide. Although the majority of infected individuals remain asymptomatic, this bacterium colonizes the gastric mucosa causing the development of various clinical conditions as peptic ulcers, chronic gastritis and gastric adenocarcinomas and mucosa-associated lymphoid tissue lymphomas, but complications are not limited to gastric ones. Extradigestive pathologies, including metabolic disturbances such as diabetes, obesity and nonalcoholic fatty liver disease, have also been associated with H. pylori infection. However, the underlying mechanisms connecting H. pylori with extragastric metabolic diseases needs to be clarified. Notably, the latest studies on the topic have confirmed that H. pylori infection modulates gut microbiota in humans. Damage in the gut bacterial community (dysbiosis) has been widely related to metabolic dysregulation by affecting adiposity, host energy balance, carbohydrate metabolism, and hormonal modulation, among others. Taking into account that Type 2 diabetic patients are more prone to be H. pylori positive, gut microbiota emerges as putative key factor responsible for this interaction. In this regard, the therapy of choice for H. pylori eradication, based on proton pump inhibitor combined with two or more antibiotics, also alters gut microbiota composition, but consequences on metabolic health of the patients has been scarcely explored. Recent studies from our group showed that, despite decreasing gut bacterial diversity, conventional H. pylori eradication therapy is related to positive changes in glucose and lipid profiles. The mechanistic insights explaining these effects should also be addressed in future research. This review will deal with the role of gut microbiota as the linking factor between H. pylori infection and metabolic diseases, and discussed the impact that gut bacterial modulation by H. pylori eradication treatment can also have in host's metabolism. For this purpose, new evidence from the latest human studies published in more recent years will be analyzed.
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Affiliation(s)
- Gracia M. Martin-Nuñez
- Unidad de Gestión Clínica de Endocrinología y Nutrición (Hospital Universitario Virgen de la Victoria), Instituto de Investigación Biomédica de Málaga (IBIMA), Universidad de Málaga, Málaga, Spain
- Centro de Investigación Biomédica en Red (CIBER) Fisiopatología de la Obesidad y Nutrición (CIBEROBN), Instituto de Salud Carlos III (ISCIII), Madrid, Spain
| | - Isabel Cornejo-Pareja
- Unidad de Gestión Clínica de Endocrinología y Nutrición (Hospital Universitario Virgen de la Victoria), Instituto de Investigación Biomédica de Málaga (IBIMA), Universidad de Málaga, Málaga, Spain
- Centro de Investigación Biomédica en Red (CIBER) Fisiopatología de la Obesidad y Nutrición (CIBEROBN), Instituto de Salud Carlos III (ISCIII), Madrid, Spain
| | - Mercedes Clemente-Postigo
- Centro de Investigación Biomédica en Red (CIBER) Fisiopatología de la Obesidad y Nutrición (CIBEROBN), Instituto de Salud Carlos III (ISCIII), Madrid, Spain
- Department of Cell Biology, Physiology and Immunology. Instituto Maimónides de Investigación Biomédica de Córdoba (IMIBIC)-Reina Sofia University Hospital, University of Cordoba, Córdoba, Spain
- *Correspondence: Francisco J. Tinahones, ; Mercedes Clemente-Postigo,
| | - Francisco J. Tinahones
- Unidad de Gestión Clínica de Endocrinología y Nutrición (Hospital Universitario Virgen de la Victoria), Instituto de Investigación Biomédica de Málaga (IBIMA), Universidad de Málaga, Málaga, Spain
- Centro de Investigación Biomédica en Red (CIBER) Fisiopatología de la Obesidad y Nutrición (CIBEROBN), Instituto de Salud Carlos III (ISCIII), Madrid, Spain
- *Correspondence: Francisco J. Tinahones, ; Mercedes Clemente-Postigo,
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Wang J, Dong F, Su H, Zhu L, Shao S, Wu J, Liu H. H. pylori is related to NAFLD but only in female: A Cross-sectional Study. Int J Med Sci 2021; 18:2303-2311. [PMID: 33967606 PMCID: PMC8100637 DOI: 10.7150/ijms.50748] [Citation(s) in RCA: 14] [Impact Index Per Article: 3.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/27/2020] [Accepted: 03/01/2021] [Indexed: 12/26/2022] Open
Abstract
Background: Recently, an increasing number of studies have focused on the extragastrointestinal effects of Helicobacter pylori (H. pylori), including metabolic syndrome, fatty liver, and rheumatic and skin diseases. Nonalcoholic fatty liver disease (NAFLD) is a common chronic disease worldwide that conveys a heavy economic burden on patients and society. The aim of this study was to investigate the relationship between H. pylori and NAFLD and to identify potential influencing factors. Methods: We conducted a cross-sectional study of individuals who had undergone regular physical examinations at the Beijing Shijitan Hospital Health Examination Center from July to October 2018. We evaluated the associations between NAFLD and NAFLD with H. pylori infection and related serum markers using multiple linear regression and logistic regression. Results: There were significant relationships between H. pylori infection status and NAFLD in females (P=0.034) but not in males (P=0.795) according to Fisher's exact test. The association persisted after further adjustment for metabolic variables, gastrin factors, and liver enzymes. Waist-to-Hip Ratio, Body Mass Index, triglycerides, High-density lipoprotein cholesterol, glucose, uric acid, alkaline phosphatase, and Alanine aminotransferase are related to NAFLD after adjusting for age or interaction between biochemical indexes. Conclusion: H. pylori infection is related to NAFLD in female patients. The relationship between H. pylori and NAFLD may be mediated by markers of lipid metabolism and glycometabolism.
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Affiliation(s)
- Jingwei Wang
- Beijing Shijitan Hospital, Capital Medical University, Beijing, China
| | - Fengxiao Dong
- Beijing Shijitan Hospital, Capital Medical University, Beijing, China
| | - Hui Su
- Beijing Shijitan Hospital, Capital Medical University, Beijing, China
| | - Licun Zhu
- Beijing Shijitan Hospital, Capital Medical University, Beijing, China
| | - Sujun Shao
- Beijing Shijitan Hospital, Capital Medical University, Beijing, China
| | - Jing Wu
- Beijing Shijitan Hospital, Capital Medical University, Beijing, China
| | - Hong Liu
- Beijing Shijitan Hospital, Capital Medical University, Beijing, China
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Rahman MM, Kibria MG, Sultana N, Akhter M, Begum H, Haque MA, Haque R, Sarker SA, Ahmed F, Hasan M. Seroprevalence of Helicobacter pylori and its association with metabolic syndrome in a rural community of Bangladesh. JGH Open 2021; 5:64-72. [PMID: 33490615 PMCID: PMC7812465 DOI: 10.1002/jgh3.12448] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/26/2020] [Revised: 10/23/2020] [Accepted: 10/27/2020] [Indexed: 11/08/2022]
Abstract
BACKGROUND AND AIM As the interrelationship between Helicobacter pylori, metabolic syndrome (MetS), and non-alcoholic fatty liver disease (NAFLD) is controversial, we undertook a community-based study with the aim to find the seroprevalence of H. pylori and its relationship with MetS and NAFLD. METHODS This door-to-door survey was conducted among the adult subjects (≥18 years) of two villages (Charcharia of Dhaka district and Kharrah of Munshiganj district) of Bangladesh. Interviews using a structured questionnaire, clinical examination, anthropometric measurements, ultrasonogram of the liver, and biochemical tests were performed. RESULTS Of 1021 subjects, 781 responded (76.49%), and 767 were included in the final analysis (mean age 40.35 ± 15.56 years; female 63.5%). Anti-H. pylori antibodies were found in 418 of 767 (54.5%). There were no H. pylori serostatus association with MetS and diabetes mellitus (DM) in univariate or multivariate analysis (all P > 0.05). However, H. pylori seropositive subjects had lower systolic blood pressure (odds ratio [OR] = -2.95 [-5.58, -0.32]) and low density lipoprotein -cholesterol (OR -7.79 [-15, -0.57]) compared to seronegative subjects in the linear regression model. Seronegativity of H. pylori was associated with NALFD in univariate (P = 0.007) but not multivariate analysis (P = 0.086). There were no differences in the frequency of H. pylori seropositivity among the participants with nonobese compared to obese NAFLD (19/42 [45%] vs 43/99 [43.4%], P = 0.844). CONCLUSION In a rural community of Bangladesh, about 55% of the population were H. pylori seropositive, which was more common among the underweight than normal or obese subjects. However, there was no relationship observed between H. pylori seroprevalence and MetS, DM, or NAFLD.
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Affiliation(s)
- M. Masudur Rahman
- Department of GastroenterologySheikh Russel National Gastroliver Institute and HospitalDhakaBangladesh
| | - Md. Golam Kibria
- Department of GastroenterologySheikh Russel National Gastroliver Institute and HospitalDhakaBangladesh
| | - Nigar Sultana
- Department of GastroenterologyDelta Medical College and HospitalDhakaBangladesh
| | - Mahfuza Akhter
- Department of GastroenterologyMughda Medical College and HospitalDhakaBangladesh
| | - Hasina Begum
- Department of Radiology and ImagingSheikh Russel National Gastroliver Institute and HospitalDhakaBangladesh
| | - Md. Ahshanul Haque
- Nutrition and Clinical Service DivisionInternational Centre for Diarrhoeal Diseases Research, Bangladesh (icddr,b)DhakaBangladesh
| | - Rashidul Haque
- Infectious Disease DivisionInternational Centre for Diarrhoeal Diseases Research, Bangladesh (icddr,b)DhakaBangladesh
| | - Shafiqul Alam Sarker
- Nutrition and Clinical Service DivisionInternational Centre for Diarrhoeal Diseases Research, Bangladesh (icddr,b)DhakaBangladesh
| | - Faruque Ahmed
- Department of GastroenterologySheikh Russel National Gastroliver Institute and HospitalDhakaBangladesh
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The Effect of Probiotics Supplementation on Gut Microbiota After Helicobacter pylori Eradication: A Multicenter Randomized Controlled Trial. Infect Dis Ther 2020; 10:317-333. [PMID: 33270205 PMCID: PMC7955021 DOI: 10.1007/s40121-020-00372-9] [Citation(s) in RCA: 34] [Impact Index Per Article: 6.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/24/2020] [Accepted: 11/11/2020] [Indexed: 02/08/2023] Open
Abstract
Introduction Helicobacter pylori eradication therapy may lead to the perturbation of gut microbiota. We aim to investigate the impact of probiotics on eradication rate and gut microbiota during eradication therapy. Methods A total of 162 patients receiving bismuth quadruple therapy were enrolled and randomly assigned to groups given probiotics (n = 83) or placebo (n = 79) for 4 weeks. Fecal samples were collected before treatment and 2, 4, 6, and 8 weeks after eradication therapy. Gut microbiota was analyzed by 16S rRNA high-throughput sequencing. Results The eradication rates in the placebo and probiotics group were 82.43% and 87.01%, respectively (P > 0.05). Compared with baseline, alpha and beta diversity was significantly altered 2 weeks after eradication in both groups, which was restored at week 8. There were no significant differences in diversity between the two groups. H. pylori eradication therapy resulted in enrichment of some detrimental bacteria taxa such as Shigella, Klebsiella, and Streptococcus, while probiotics supplementation could rapidly restore these taxa levels after eradication and increase the taxa of Bacillus and Lactobacillales. Functional analysis revealed that lipopolysaccharide biosynthesis and polymyxin resistance pathways were significantly enriched after eradication, while probiotics supplementation mainly enriched the cofactors and vitamins metabolism pathways. Increased relative abundances of Roseburia and Dialister were associated with the positive eradication outcome. Conclusions Probiotics supplementation might help to construct a beneficial profile of gut microbiota after eradication therapy. Specific bacteria taxa are associated with H. pylori eradication outcome. These findings may be of value in rational use of probiotics during H. pylori eradication. Trial Registration Chinese Clinical Trial Registry, ChiCTR1900022116. Electronic supplementary material The online version of this article (10.1007/s40121-020-00372-9) contains supplementary material, which is available to authorized users.
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Alvarez CS, Florio AA, Butt J, Rivera-Andrade A, Kroker-Lobos MF, Waterboer T, Camargo MC, Freedman ND, Graubard BI, Lazo M, Guallar E, Groopman JD, Ramírez-Zea M, McGlynn KA. Associations between Helicobacter pylori with nonalcoholic fatty liver disease and other metabolic conditions in Guatemala. Helicobacter 2020; 25:e12756. [PMID: 33006810 PMCID: PMC7688101 DOI: 10.1111/hel.12756] [Citation(s) in RCA: 15] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/12/2020] [Revised: 08/07/2020] [Accepted: 08/08/2020] [Indexed: 12/12/2022]
Abstract
BACKGROUND Previous studies have suggested an association between Helicobacter pylori (H pylori) and nonalcoholic fatty liver disease (NAFLD). The aim of the current study was to examine the association in Guatemala, a region with elevated prevalences of both H pylori and NAFLD. Associations between H pylori and other metabolic conditions were also examined, as were associations between H hepaticus and H bilis and the metabolic conditions. MATERIALS & METHODS The analysis included 424 participants from a cross-sectional study in Guatemala. H pylori seropositivity was defined as positivity for ≥ 4 antigens. Seropositivities for H bilis and H hepaticus were defined as positivity for ≥ 2 antigens. NAFLD was estimated using the Fatty Liver Index and the Hepatic Steatosis Index. Other conditions examined were obesity, central obesity, hypercholesterolemia, low HDL, diabetes and metabolic syndrome (MetSyn). Prevalence odds ratios (POR) and 95% confidence intervals (CIs) were estimated. RESULTS No overall associations between H pylori,H hepaticus, or H bilis and NAFLD or related metabolic conditions were found. Seropositivity for H pylori antigens CagA and VacA and H hepaticus antigen HH0713 was each significantly associated with NAFLD, however. In addition, associations were observed between the H pylori antigens HyuA, HP1564, and UreA and specified metabolic conditions. CONCLUSIONS While no overall associations between H pylori or Helicobacter species with NAFLD or related conditions were observed, some selected Helicobacter spp. antigens were associated with NAFLD. Further research is warranted to examine whether H. species are associated with any metabolic condition.
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Affiliation(s)
- Christian S. Alvarez
- Division of Cancer Epidemiology and Genetics, National
Cancer Institute, Rockville, Maryland, U.S.A
| | - Andrea A. Florio
- Division of Cancer Epidemiology and Genetics, National
Cancer Institute, Rockville, Maryland, U.S.A
| | - Julia Butt
- Infections and Cancer Epidemiology, Infection,
Inflammation and Cancer Research Program, German Cancer Research Center (DKFZ),
Heidelberg, Germany
| | - Alvaro Rivera-Andrade
- Research Center for the Prevention of Chronic
Diseases, Institute of Nutrition of Central America and Panama (INCAP), Guatemala City,
Guatemala
| | - María F. Kroker-Lobos
- Research Center for the Prevention of Chronic
Diseases, Institute of Nutrition of Central America and Panama (INCAP), Guatemala City,
Guatemala
| | - Tim Waterboer
- Infections and Cancer Epidemiology, Infection,
Inflammation and Cancer Research Program, German Cancer Research Center (DKFZ),
Heidelberg, Germany
| | - M. Constanza Camargo
- Division of Cancer Epidemiology and Genetics, National
Cancer Institute, Rockville, Maryland, U.S.A
| | - Neal D. Freedman
- Division of Cancer Epidemiology and Genetics, National
Cancer Institute, Rockville, Maryland, U.S.A
| | - Barry I. Graubard
- Division of Cancer Epidemiology and Genetics, National
Cancer Institute, Rockville, Maryland, U.S.A
| | - Mariana Lazo
- Division of General Internal Medicine, School of Medicine,
Johns Hopkins University, Baltimore, MD, USA,Urban Health Collaborative, Dornsife School of Public
Health, Drexel University, Philadelphia, PA, USA
| | - Eliseo Guallar
- Department of Epidemiology, Bloomberg School of Public
Health, Johns Hopkins University, Baltimore, MD, U.S.A
| | - John D. Groopman
- Department of Epidemiology, Bloomberg School of Public
Health, Johns Hopkins University, Baltimore, MD, U.S.A.,Department of Environmental Health and Engineering,
Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD,
U.S.A
| | - Manuel Ramírez-Zea
- Research Center for the Prevention of Chronic
Diseases, Institute of Nutrition of Central America and Panama (INCAP), Guatemala City,
Guatemala
| | - Katherine A. McGlynn
- Division of Cancer Epidemiology and Genetics, National
Cancer Institute, Rockville, Maryland, U.S.A
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Darvishi M, Noori M, Nazer MR, Soleiman-Meigooni S, Forootan M. The Relationship between Helicobacter Pylori and Extra-Gastrointestinal Infections. IRANIAN JOURNAL OF MEDICAL MICROBIOLOGY 2020; 14:543-565. [DOI: 10.30699/ijmm.14.6.543] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 01/06/2025]
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Helicobacter pylori, Sleeve Gastrectomy, and Gastroesophageal Reflux Disease: Is There a Relation? Obes Surg 2020; 31:1839-1840. [PMID: 33111248 DOI: 10.1007/s11695-020-05066-2] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/05/2020] [Revised: 10/03/2020] [Accepted: 10/20/2020] [Indexed: 10/23/2022]
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Liou JM, Chen CC, Chang CM, Fang YJ, Bair MJ, Chen PY, Chang CY, Hsu YC, Chen MJ, Chen CC, Lee JY, Yang TH, Luo JC, Chen CY, Hsu WF, Chen YN, Wu JY, Lin JT, Lu TP, Chuang EY, El-Omar EM, Wu MS. Long-term changes of gut microbiota, antibiotic resistance, and metabolic parameters after Helicobacter pylori eradication: a multicentre, open-label, randomised trial. THE LANCET. INFECTIOUS DISEASES 2020; 19:1109-1120. [PMID: 31559966 DOI: 10.1016/s1473-3099(19)30272-5] [Citation(s) in RCA: 143] [Impact Index Per Article: 28.6] [Reference Citation Analysis] [Abstract] [Track Full Text] [Subscribe] [Scholar Register] [Received: 11/21/2018] [Revised: 05/09/2019] [Accepted: 05/14/2019] [Indexed: 02/07/2023]
Abstract
BACKGROUND In first-line treatment of Helicobacter pylori, we have previously shown that the eradication frequency was 83·7% (95% CI 80·4-86·6) for triple therapy for 14 days (T14; lansoprazole 30 mg, amoxicillin 1 g, and clarithromycin 500 mg, all given twice daily), 85·9% (82·7-88·6) for concomitant therapy for 10 days (C10; lansoprazole 30 mg, amoxicillin 1 g, clarithromycin 500 mg, and metronidazole 500 mg, all given twice daily), and 90·4% (87·6-92·6) for bismuth quadruple therapy for 10 days (BQ10; bismuth tripotassium dicitrate 300 mg four times a day, lansoprazole 30 mg twice daily, tetracycline 500 mg four times a day, and metronidazole 500 mg three times a day). In this follow-up study, we assess short-term and long-term effects of these therapies on the gut microbiota, antibiotic resistance, and metabolic parameters. METHODS This was a multicentre, open-label, randomised trial done at nine medical centres in Taiwan. Adult patients (>20 years) with documented H pylori infection were randomly assigned (1:1:1, with block sizes of six) to receive T14, C10, or BQ10. We assessed long-term outcomes (reinfection frequency, changes in the gut microbiota, antibiotic resistance, and metabolic parameters) in patients with available data, excluding all protocol violators and those with unknown post-treatment H pylori status. Faecal samples were collected before treatment and 2 weeks, 2 months, and at least 1 year after eradication therapy. Amplification of the V3 and V4 hypervariable regions of the 16S rRNA was done followed by high-throughput sequencing. Susceptibility testing for faecal Escherichia coli and Klebsiella pneumoniae was done. This trial is complete and registered with ClinicalTrials.gov, NCT01906879. FINDINGS Between July 17, 2013, and April 20, 2016, 1620 participants were randomly assigned to the three treatment groups (540 [33%] per group). 1214 (75%) attended 1-year follow-up and are included in this analysis. Compared with baseline, alpha diversity was significantly reduced 2 weeks after T14 (p=0·0002), C10 (p<0·0001), and BQ10 (p<0·0001) treatment. Beta diversity was also significantly altered 2 weeks after T14 (p=0·0010), C10 (p=0·0001), and BQ10 (p=0·0001). Alpha diversity and beta diversity were restored at week 8 (p=0·14 and p=0·918, respectively) and 1 year (p=0·14 and p=0·918) after T14, but were not fully recovered at week 8 and after 1 year in patients treated with C10 (p=0·0001 and p=0·013 at week 8; p=0·019 and p=0·064 at 1 year) and BQ10 (p<0·0001 and p=0·0002; p=0·001 and p=0·029). A transient increase at week 2 after T14 and C10 of the resistance rates of E coli to ampicillin-sulbactam (12% [15/127] to 66% [38/58] for T14, 7% [10/135] to 64% [28/44] for C10), cefazolin (13% [16/127] to 43% [25/58] for T14, 10% [13/135] to 41% [18/44] for C10), cefmetazole (8% [10/127] to 26% [15/58] for T14, 4% [5/135] to 18% [8/44] for C10), levofloxacin (8% [10/127] to 35% [20/58] for T14, 7% [10/135] to 32% [14/44] for C10), gentamicin (13% [19/146] to 47% [27/58] for T14, 15% [22/149] to 45% [20/44] for C10), and trimethoprim-sulfamethoxazole (33% [48/146] to 86% [50/58] for T14, 28% [42/148] to 86% [38/44] for C10; p<0·05 in paired samples in the above analyses) returned to basal state at week 8 and after 1 year. Although bodyweight and body-mass index slightly increased, there were significant improvements in metabolic parameters, with a decrease in insulin resistance, triglycerides, and LDL and an increase in HDL. Overall, there was no significant change in the prevalence of metabolic syndrome at week 8 and 1 year after T14, C10, and BQ10. INTERPRETATION Eradication of H pylori infection has minimal disruption of the microbiota, no effect on antibiotic resistance of E coli, and some positive effects on metabolic parameters. Collectively, these results lend support to the long-term safety of H pylori eradication therapy. FUNDING National Taiwan University Hospital and Ministry of Science and Technology of Taiwan.
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Affiliation(s)
- Jyh-Ming Liou
- Division of Gastroenterology and Hepatology, Department of Internal Medicine, National Taiwan University Hospital, Taipei, Taiwan; Department of Internal Medicine, National Taiwan University College of Medicine, Taipei, Taiwan; Department of Internal Medicine, National Taiwan University Cancer Center, Taipei, Taiwan
| | - Chieh-Chang Chen
- Division of Gastroenterology and Hepatology, Department of Internal Medicine, National Taiwan University Hospital, Taipei, Taiwan; Department of Internal Medicine, National Taiwan University College of Medicine, Taipei, Taiwan
| | - Chih-Min Chang
- Bioinformatics and Biostatistics Core, Centers of Genomic and Precision Medicine, National Taiwan University, Taipei, Taiwan
| | - Yu-Jen Fang
- Department of Internal Medicine, National Taiwan University College of Medicine, Taipei, Taiwan; Department of Internal Medicine, National Taiwan University Hospital, Yun-Lin Branch, Yun-Lin, Taiwan
| | - Ming-Jong Bair
- Division of Gastroenterology, Department of Internal Medicine, Taitung Mackay Memorial Hospital, Taitung, Taiwan; Mackay Medical College, New Taipei City, Taiwan
| | - Po-Yueh Chen
- Division of Gastroenterology and Hepatology, Department of Internal medicine, Chia-Yi Christian Hospital, Chia-Yi, Taiwan
| | - Chi-Yang Chang
- School of Medicine, College of Medicine, Fu Jen Catholic University Hospital, New Taipei City, Taiwan; Department of Internal Medicine Fu Jen Catholic University Hospital, New Taipei City, Taiwan
| | - Yao-Chun Hsu
- School of Medicine, College of Medicine, Fu Jen Catholic University Hospital, New Taipei City, Taiwan; Department of Internal Medicine Fu Jen Catholic University Hospital, New Taipei City, Taiwan
| | - Mei-Jyh Chen
- Division of Gastroenterology and Hepatology, Department of Internal Medicine, National Taiwan University Hospital, Taipei, Taiwan; Department of Internal Medicine, National Taiwan University College of Medicine, Taipei, Taiwan
| | - Chien-Chuan Chen
- Division of Gastroenterology and Hepatology, Department of Internal Medicine, National Taiwan University Hospital, Taipei, Taiwan; Department of Internal Medicine, National Taiwan University College of Medicine, Taipei, Taiwan
| | - Ji-Yuh Lee
- Department of Internal Medicine, National Taiwan University College of Medicine, Taipei, Taiwan; Department of Internal Medicine, National Taiwan University Hospital, Yun-Lin Branch, Yun-Lin, Taiwan
| | - Tsung-Hua Yang
- Department of Internal Medicine, National Taiwan University College of Medicine, Taipei, Taiwan; Department of Internal Medicine, National Taiwan University Hospital, Yun-Lin Branch, Yun-Lin, Taiwan
| | - Jiing-Chyuan Luo
- Department of Medicine, National Yang-Ming University, School of Medicine and Taipei Veterans General Hospital, Taipei, Taiwan
| | - Chi-Yi Chen
- Division of Gastroenterology and Hepatology, Department of Internal medicine, Chia-Yi Christian Hospital, Chia-Yi, Taiwan
| | - Wen-Feng Hsu
- Division of Gastroenterology and Hepatology, Department of Internal Medicine, National Taiwan University Hospital, Taipei, Taiwan; Department of Internal Medicine, National Taiwan University College of Medicine, Taipei, Taiwan; Department of Internal Medicine, National Taiwan University Cancer Center, Taipei, Taiwan
| | - Yen-Nien Chen
- Division of Gastroenterology and Hepatology, Department of Internal Medicine, National Taiwan University Hospital, Taipei, Taiwan; Department of Internal Medicine, National Taiwan University College of Medicine, Taipei, Taiwan; Department of Internal Medicine, National Taiwan University Cancer Center, Taipei, Taiwan
| | - Jeng-Yih Wu
- Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung Medical University, Kaohsiung, Taiwan
| | - Jaw-Town Lin
- Digestive Medicine Center, China Medical University Hospital, Taichung, Taiwan
| | - Tzu-Pin Lu
- Bioinformatics and Biostatistics Core, Centers of Genomic and Precision Medicine, National Taiwan University, Taipei, Taiwan; Institute of Epidemiology and Preventive Medicine, Department of Public Health, National Taiwan University, Taipei, Taiwan
| | - Eric Y Chuang
- Bioinformatics and Biostatistics Core, Centers of Genomic and Precision Medicine, National Taiwan University, Taipei, Taiwan; Graduate Institute of Biomedical Electronics and Bioinformatics, National Taiwan University, Taipei, Taiwan
| | - Emad M El-Omar
- Microbiome Research Centre, St George & Sutherland Clinical School, University of New South Wales, Sydney, NSW, Australia
| | - Ming-Shiang Wu
- Division of Gastroenterology and Hepatology, Department of Internal Medicine, National Taiwan University Hospital, Taipei, Taiwan; Department of Internal Medicine, National Taiwan University College of Medicine, Taipei, Taiwan.
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Fang LJ, Lin XC, Huang D, Pan TT, Yan XM, Hu WG, Zhu H, Xu Z, Zhu XZ, Lu HJ, Chen GP, Huang KY. 1H NMR-based metabolomics analyses in children with Helicobacter pylori infection and the alteration of serum metabolites after treatment. Microb Pathog 2020; 147:104292. [PMID: 32505653 DOI: 10.1016/j.micpath.2020.104292] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/11/2019] [Revised: 03/28/2020] [Accepted: 05/26/2020] [Indexed: 12/22/2022]
Abstract
BACKGROUND AND AIMS Helicobacter pylori (H. pylori) infection can occur in early childhood, without eradication therapies such infection can persist throughout life and cause many different diseases. This study investigated the metabolic characteristics and explored the underlying mechanism of children with H. pylori infection, and identified potential biomarkers for evaluating the efficacy of H. pylori eradication therapies. METHODS We performed 1H NMR-based metabonomics coupled with multivariate analysis to investigate the metabolic profiling of serum samples between Children with and without H. pylori infection. In the same manner, we compared the alternations of metabolites in H. pylori-infected children before and after H. pylori eradication therapies. RESULTS 21 metabolites from serum in H. pylori-infected and H. pylori-uninfected children were identified, which were mainly involved in energy, amino acid, lipid and microbial metabolism. We found that the serum levels of trimethylamine N-oxide and alanine were significantly higher in H. pylori-infected children compared to uninfected sera, whereas lactate was significantly lower. We also found that the levels of trimethylamine N-oxide and creatine in H. pylori-infected children was significantly decreased after H. pylori eradication therapies, whereas lactate and low-density lipoprotein/very low-density lipoprotein was significantly increased. CONCLUSIONS This is the first study using 1H NMR-based metabolomics approach to explore the effects of H. pylori infection in children. Our results demonstrated that the disturbances of metabolism in energy, amino acids, lipids and microbiota could play an important role in the pathogenesis of gastrointestinal and extragastric diseases caused by H. pylori infection. Trimethylamine N-oxide and lactate might serve as potential serum biomarkers for evaluating the efficacy of H. pylori eradication therapies.
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Affiliation(s)
- Ling-Juan Fang
- Department of Pediatric Gastroenterology, The Second Affiliated Hospital and Yuying Children's Hospital of Wenzhou Medical University, Wenzhou, Zhejiang Province, China
| | - Xiao-Chun Lin
- Department of Pediatric Gastroenterology, The Second Affiliated Hospital and Yuying Children's Hospital of Wenzhou Medical University, Wenzhou, Zhejiang Province, China
| | - Dian Huang
- The Second School of Wenzhou Medical University, Wenzhou, Zhejiang Province, China
| | - Tong-Tong Pan
- Department of Pediatric Gastroenterology, The Second Affiliated Hospital and Yuying Children's Hospital of Wenzhou Medical University, Wenzhou, Zhejiang Province, China
| | - Xiu-Mei Yan
- Department of Pediatric Gastroenterology, The Second Affiliated Hospital and Yuying Children's Hospital of Wenzhou Medical University, Wenzhou, Zhejiang Province, China
| | - Wei-Guo Hu
- Department of Pediatric Gastroenterology, The Second Affiliated Hospital and Yuying Children's Hospital of Wenzhou Medical University, Wenzhou, Zhejiang Province, China
| | - Huan Zhu
- Department of Pediatric Gastroenterology, The Second Affiliated Hospital and Yuying Children's Hospital of Wenzhou Medical University, Wenzhou, Zhejiang Province, China
| | - Zhang Xu
- Department of Pediatric Gastroenterology, The Second Affiliated Hospital and Yuying Children's Hospital of Wenzhou Medical University, Wenzhou, Zhejiang Province, China
| | - Xiao-Zhou Zhu
- Department of Pediatric Gastroenterology, The Second Affiliated Hospital and Yuying Children's Hospital of Wenzhou Medical University, Wenzhou, Zhejiang Province, China
| | - Hua-Jun Lu
- Department of Pediatric Gastroenterology, The Second Affiliated Hospital and Yuying Children's Hospital of Wenzhou Medical University, Wenzhou, Zhejiang Province, China
| | - Gui-Ping Chen
- Department of Pediatric Gastroenterology, The Second Affiliated Hospital and Yuying Children's Hospital of Wenzhou Medical University, Wenzhou, Zhejiang Province, China
| | - Kai-Yu Huang
- Department of Pediatric Gastroenterology, The Second Affiliated Hospital and Yuying Children's Hospital of Wenzhou Medical University, Wenzhou, Zhejiang Province, China.
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Alberts CJ, Jeske R, de Martel C, den Hollander WJ, Michel A, Prins M, Snijder MB, Schim van der Loeff MF, Waterboer T. Helicobacter pylori seroprevalence in six different ethnic groups living in Amsterdam: The HELIUS study. Helicobacter 2020; 25:e12687. [PMID: 32147867 DOI: 10.1111/hel.12687] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 10/30/2019] [Revised: 01/20/2020] [Accepted: 02/10/2020] [Indexed: 12/30/2022]
Abstract
BACKGROUND Helicobacter pylori prevalence varies greatly worldwide. We explored the prevalence of H. pylori and CagA seropositivity among adults aged 18-44 years living in the Netherlands by ethnicity and migration status (first vs second generation). MATERIALS AND METHODS Participants from six different ethnic groups were selected from the population-based multi-ethnic HELIUS study in Amsterdam, the Netherlands. Serum samples were tested for H. pylori antigens using a validated Luminex-based multiplex serology assay. Prevalence ratios were estimated using Poisson regression analysis. RESULTS A total of 4683 participants aged 18-44 years were randomly selected based on sex, ethnicity, and age. H. pylori seroprevalence was highest in the Ghanaian group (84%), followed by Moroccan (81%), Turkish (66%), African Surinamese (51%), South-Asian Surinamese (48%), and Dutch (17%) participants. All ethnic minority groups had a significantly higher risk of being H. pylori seropositive compared to the Dutch group. This association was strongest among participants born outside the Netherlands (first generation), but was still significant and apparent among second-generation participants. Among first-generation participants, all groups, except the Moroccans, had a significantly higher proportion of individuals with a cagA + H. pylori strain compared to the Dutch participants. CONCLUSION Helicobacter pylori seroprevalence among first-generation migrants is high in the Netherlands and remains elevated among second-generation migrants (ie, those born in the Netherlands). High exposure to H. pylori, and especially to the more virulent cagA+ strain, highlights the need for tailored prevention of gastric diseases (notably peptic ulcers and cancers) among migrants.
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Affiliation(s)
- Catharina J Alberts
- International Agency for Research on Cancer, Lyon, France
- Department of Infectious Diseases, Public Health Service (GGD) of Amsterdam, Amsterdam, the Netherlands
| | - Rima Jeske
- Infection, Inflammation and Cancer Program, German Cancer Research Center (DKFZ), Heidelberg, Germany
- Faculty of Biosciences, Heidelberg University, Heidelberg, Germany
| | | | - Wouter J den Hollander
- Department of Gastroenterology and Hepatology, Leiden University Medical Center (LUMC), Leiden, the Netherlands
| | - Angelika Michel
- Infection, Inflammation and Cancer Program, German Cancer Research Center (DKFZ), Heidelberg, Germany
| | - Maria Prins
- Department of Infectious Diseases, Public Health Service (GGD) of Amsterdam, Amsterdam, the Netherlands
- Department of Internal Medicine, Amsterdam Infection & Immunity Institute (AIII), Amsterdam UMC, University of Amsterdam, Amsterdam, the Netherlands
| | - Marieke B Snijder
- Department of Public Health, Amsterdam UMC, University of Amsterdam, Amsterdam, the Netherlands
| | - Maarten F Schim van der Loeff
- Department of Infectious Diseases, Public Health Service (GGD) of Amsterdam, Amsterdam, the Netherlands
- Department of Internal Medicine, Amsterdam Infection & Immunity Institute (AIII), Amsterdam UMC, University of Amsterdam, Amsterdam, the Netherlands
| | - Tim Waterboer
- Infection, Inflammation and Cancer Program, German Cancer Research Center (DKFZ), Heidelberg, Germany
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Active Helicobacter pylori Infection is Independently Associated with Nonalcoholic Steatohepatitis in Morbidly Obese Patients. J Clin Med 2020; 9:jcm9040933. [PMID: 32235601 PMCID: PMC7230908 DOI: 10.3390/jcm9040933] [Citation(s) in RCA: 55] [Impact Index Per Article: 11.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/25/2020] [Revised: 03/24/2020] [Accepted: 03/26/2020] [Indexed: 02/07/2023] Open
Abstract
Nonalcoholic fatty liver disease (NAFLD) emerges as an important global burden and Helicobacter pylori infection (Hp-I) has been suggested as a risk factor of NAFLD, although controversy exists. This retrospective study aimed to investigate a potential impact of active Hp-I on NAFLD severity in morbidly obese patients, subjected to bariatric surgery and gastric biopsy for documentation of Hp-I. Of 64 eligible participants, 15 (23.4%) were diagnosed with active Hp-I, showing higher rates of nonalcoholic steatohepatitis (NASH) than those without Hp-I (86.7% vs. 26.5%, respectively; p < 0.001). Concerning histological lesions, steatosis grade (p = 0.027), ballooning (p < 0.001), lobular inflammation (p = 0.003), and fibrosis stage (p < 0.001) were also more severe in Hp-I positive patients. Likewise, liver function tests, insulin resistance, dyslipidemia, and arterial hypertension were significantly higher in Hp-I positive patients. Hp-I was independently positively associated with NASH (beta = 3.27; p = 0.002), severe NASH (beta = 2.37; p = 0.018), and the presence of fibrosis (beta = 3.86; p = 0.001) in a binary regression model, after adjustment for potential confounders. In conclusion, active Hp-Ι was independently associated with NASH and fibrosis, findings offering potential clinical implication.
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Papaefthymiou A, Liatsos C, Georgopoulos SD, Apostolopoulos P, Doulberis M, Kyriakos N, Giakoumis M, Papadomichelakis M, Galanopoulos M, Katsinelos P, Rokkas T, Kountouras J. Helicobacter pylori eradication regimens in an antibiotic high-resistance European area: A cost-effectiveness analysis. Helicobacter 2020; 25:e12666. [PMID: 31692137 DOI: 10.1111/hel.12666] [Citation(s) in RCA: 10] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/26/2019] [Revised: 10/04/2019] [Accepted: 10/04/2019] [Indexed: 12/13/2022]
Abstract
INTRODUCTION Helicobacter pylori infection (H pylori-I) affects more than half of the global population and consists an important burden to public health and healthcare expenditures, by contributing to many diseases' pathogenesis. AIM This study aimed to evaluate the current nonbismuth quadruple eradication regimens in a high antibiotic resistance area, such as Greece, concerning their cost-effectiveness, especially during financial crisis period. MATERIALS AND METHODS Eight hundred and nine patients who received eradication treatment against H pylori-I were included to evaluate five different regimens, using amoxicillin, clarithromycin, and metronidazole as antibiotics and one proton-pump inhibitor, based on their current eradication rates. Regimes compared 10-day concomitant use of (a) pantoprazole or (b) esomeprazole; 10-day sequential use of (c) pantoprazole or (d) esomeprazole; and 14-day hybrid using esomeprazole. Cost-effectiveness analysis ratio (CEAR) and incremental cost-effectiveness ratios were calculated taking into account all direct costs and cases who needed second-line treatment. Additionally, sensitivity analysis was performed to predict all potential combinations. RESULTS Ten-day concomitant regimen with esomeprazole was characterized by the lowest CEAR (179.17€) followed by the same regimen using pantoprazole (183.27€). Hybrid regimen, although equivalent in eradication rates, was found to have higher CEAR (187.42€), whereas sequential regimens were not cost-effective (CEAR: 204.12€ and 216.02€ respectively). DISCUSSION This is the first study evaluating the cost-effectiveness of H pylori-I treatment regimens in a high clarithromycin-resistance (≈26.5%) European area, suggesting the 10-day concomitant regimen with generics using esomeprazole 40 mg as the most appropriate one. National and regional guidelines should include cost-effectiveness in their statements, and further studies are required to clarify the necessity of a wide "test and treat" policy for H pylori-I.
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Affiliation(s)
| | - Christos Liatsos
- Department of Gastroenterology, 401 Army General Hospital of Athens, Athens, Greece
| | | | | | - Michael Doulberis
- Department of Gastroenterology and Hepatology, University of Zurich, Zurich, Switzerland.,Department of Medicine, Second Medical Clinic, Aristotle University of Thessaloniki, Ippokration Hospital, Thessaloniki, Greece
| | - Nikolaos Kyriakos
- Department of Gastroenterology, 401 Army General Hospital of Athens, Athens, Greece
| | - Marios Giakoumis
- Department of Gastroenterology, 401 Army General Hospital of Athens, Athens, Greece
| | | | - Michail Galanopoulos
- Department of Gastroenterology, 401 Army General Hospital of Athens, Athens, Greece
| | - Panagiotis Katsinelos
- Department of Medicine, Second Medical Clinic, Aristotle University of Thessaloniki, Ippokration Hospital, Thessaloniki, Greece
| | - Theodore Rokkas
- Gastroenterological Clinic, Henry Dunant Hospital, Athens, Greece
| | - Jannis Kountouras
- Department of Medicine, Second Medical Clinic, Aristotle University of Thessaloniki, Ippokration Hospital, Thessaloniki, Greece
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44
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Abo-Amer YEE, Sabal A, Ahmed R, Hasan NFE, Refaie R, Mostafa SM, Mohamed AA, Khalil M, Elagawy W, Abd-Elsalam S. Relationship Between Helicobacter pylori Infection and Nonalcoholic Fatty Liver Disease (NAFLD) in a Developing Country: A Cross-Sectional Study. Diabetes Metab Syndr Obes 2020; 13:619-625. [PMID: 32184641 PMCID: PMC7060033 DOI: 10.2147/dmso.s237866] [Citation(s) in RCA: 43] [Impact Index Per Article: 8.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 11/08/2019] [Accepted: 02/04/2020] [Indexed: 12/17/2022] Open
Abstract
BACKGROUND Non-alcoholic fatty liver disease (NAFLD) is a very common disease that affects 25-30% of the population in western countries. Many studies have observed the importance of H. pylori infection in the development of insulin resistance, non-alcoholic fatty liver disease, non-alcoholic steatohepatitis, and liver fibrosis and cirrhosis. However, the evidence from different studies was controversial. The present study aimed to investigate the relationship between H. pylori infection and NAFLD in a developing country. PATIENTS AND METHODS This cross-sectional study included all the attending outpatient clinics at four Major University hospitals and two research and clinical institutes in a developing country in the period between June and October 2019. Patients were assessed for the diagnosis of H. pylori infection as detected by H. pylori antigen in stool; they were also assessed for the diagnosis of NAFLD by ultrasound, fibroscan, and CAP. RESULTS The study was conducted on 646 patients; H. pylori infection was found to be present in 538 patients (83.3%). NAFLD (diagnosed by both U/S and Fibroscan with CAP), ALT, AST, hepatomegaly, hypertension, fasting blood sugar were significantly higher in H. pylori +ve group than H. pylori -ve group. After performing Linear regression of independent risk factors of NAFLD to prove or to refute the role of Helicobacter; H. pylori positivity, total cholesterol, degree of fatty liver by ultrasound, fasting blood sugar and diastolic blood pressure were independent risk factors for NAFLD. CONCLUSION Helicobacter pylori infection was independent risk factors for NAFLD and correlated with increased degree of steatosis.
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Affiliation(s)
- Yousry Esam-Eldin Abo-Amer
- Hepatology, Gastroenterology and Infectious Diseases Department, Mahala Hepatology Teaching Hospital, Gharbia, Egypt
| | - Aisha Sabal
- Hepatology, Tropical Medicine and Infectious Diseases Departments, National Hepatology and Tropical Medicine Research Institute, Cairo, Egypt
| | - Rehab Ahmed
- Hepatology, Tropical Medicine and Infectious Diseases Departments, National Hepatology and Tropical Medicine Research Institute, Cairo, Egypt
| | | | - Rasha Refaie
- Internal Medicine Department, Helwan University, Helwan, Egypt
| | - Sahar Mohamed Mostafa
- Hepatology, Tropical Medicine and Infectious Diseases Departments, National Hepatology and Tropical Medicine Research Institute, Cairo, Egypt
| | - Ahmed Abdelhaleem Mohamed
- Hepatology, Tropical Medicine and Infectious Diseases Departments, National Hepatology and Tropical Medicine Research Institute, Cairo, Egypt
| | - Mahmoud Khalil
- Hepatology, Tropical Medicine and Infectious Diseases Departments, National Hepatology and Tropical Medicine Research Institute, Cairo, Egypt
| | - Waleed Elagawy
- Department of Tropical Medicine, Portsaid University, Portsaid, Egypt
| | - Sherief Abd-Elsalam
- Tropical Medicine Department, Tanta University, Tanta, Egypt
- Correspondence: Sherief Abd-Elsalam Tropical Medicine Department, Tanta University, Tanta, EgyptTel +201063319696 Email
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45
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Hanafy AS, Seleem WM. Refractory Helicobacter pylori gastritis: The hidden predictors of resistance. J Glob Antimicrob Resist 2019; 19:194-200. [PMID: 31112805 DOI: 10.1016/j.jgar.2019.05.015] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/15/2019] [Revised: 05/03/2019] [Accepted: 05/09/2019] [Indexed: 02/07/2023] Open
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46
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Mohammadifard M, Saremi Z, Rastgoo M, Akbari E. Relevance between Helicobacter pylori Infection and Non-Alcoholic Fatty Liver Disease in Birjand, Iran. J Med Life 2019; 12:168-172. [PMID: 31406519 PMCID: PMC6685302 DOI: 10.25122/jml-2019-0012] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 02/06/2023] Open
Abstract
There is evidence that infection by H. pylori can have a critical proportion in the development of hepatocyte injury and both noncancerous and malignant liver conditions including non-alcoholic fatty liver disease (NAFLD). This is attributed to several mechanisms, the most important one being the toxic products of the bacterium H. pylori and oxidative injury for hepatocytes which promotes hepatic injury. The present research was aimed at determining the association between H. pylori infection and the prevalence of NAFLD in Birjand, Iran. Two groups were included in this cross-sectional study at the outpatient university clinic. One group had NAFLD (65 patients) and the other group was healthy controls without NAFLD (65 subjects). The diagnosis of NAFLD was performed using abdominal ultrasound examination and the absence of taking steatogenic medications or alcohol. Serum anti-H. pylori IgG and fecal H. pylori antigen were tested for diagnosing of H. pylori infection using ELISA method. H. pylori infection diagnosis was made if both tests were positive. None of the subjects in either group had symptoms related to the digestive system including dyspepsia, GERD (gastroesophageal reflux disease), or epigastric pain suspicious of peptic ulcer disease. There were 37 patients (28.5%) in both NAFLD (22 cases, 33.8%) and control (15 cases, 23.1%) groups whose H. pylori tests (both IgG and fecal antigen) were positive. Statistically, no significant difference was observed between the two studied groups regarding H. pylori infection frequency (p = 0.37). Asymptomatic H. pylori infection rate was not significantly different between NAFLD patients and control subjects in Birjand, Iran.
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Affiliation(s)
- Mahyar Mohammadifard
- Department of Radiology, School of Medicine, Birjand University of Medical Sciences, Birjand, Iran
| | - Zeinab Saremi
- Department of Internal Medicine, School of Medicine, Birjand University of Medical Science, Birjand, Iran
| | | | - Ehsan Akbari
- Department of Internal Medicine, School of Medicine, Birjand University of Medical Science, Birjand, Iran
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47
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Kato M, Toda A, Yamamoto‐Honda R, Arase Y, Sone H. Association between Helicobacter pylori infection, eradication and diabetes mellitus. J Diabetes Investig 2019; 10:1341-1346. [PMID: 30663265 PMCID: PMC6717903 DOI: 10.1111/jdi.13011] [Citation(s) in RCA: 21] [Impact Index Per Article: 3.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/04/2018] [Revised: 12/17/2018] [Accepted: 01/17/2019] [Indexed: 12/21/2022] Open
Abstract
AIMS/INTRODUCTION It is suspected that Helicobacter pylori is associated with extradigestive diseases including diabetes. So far, a number of studies have examined the association between H. pylori and diabetes, and the results were conflicting. The aim of the present study was to examine the association between H. pylori infection, eradication and diabetes. MATERIALS AND METHODS The present cross-sectional study was carried out using data from annual health checkups carried out at the Toranomon Hospital Health Management Center. The status of H. pylori infection, determined by serum antibodies and history of eradication, was categorized into three groups as "never," "current" and "past." The association between H. pylori infection and diabetes was examined using logistic regression. RESULTS Of 21,634 participants, 6,530 (30.2%) had a current or past history of H. pylori infection, and 1,184 (5.5%) were identified as having diabetes. Multivariate adjusted odds ratios for diabetes compared with the "never" group were 1.36 (95% confidence interval 1.10-1.67) for the "current" group and 0.92 (95% confidence interval 0.79-1.07) for the "past" group. The association between H. pylori infection and diabetes was also observed among participants without a history of eradication. CONCLUSIONS We found that current H. pylori infection was associated with an increased risk of diabetes, and the increased risk was not observed among participants after eradication. The results were concordant with the hypothesis that H. pylori infection increases the risk of diabetes. Further studies are necessary to validate the present results.
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Affiliation(s)
- Masayuki Kato
- Health Management CenterToranomon HospitalTokyoJapan
- Okinaka Memorial Institute for Medical ResearchToranomon HospitalTokyoJapan
| | - Akiko Toda
- Health Management CenterToranomon HospitalTokyoJapan
- Okinaka Memorial Institute for Medical ResearchToranomon HospitalTokyoJapan
| | - Ritsuko Yamamoto‐Honda
- Health Management CenterToranomon HospitalTokyoJapan
- Okinaka Memorial Institute for Medical ResearchToranomon HospitalTokyoJapan
| | - Yasuji Arase
- Health Management CenterToranomon HospitalTokyoJapan
- Okinaka Memorial Institute for Medical ResearchToranomon HospitalTokyoJapan
| | - Hirohito Sone
- Department of Internal Medicine (Metabolism)Faculty of MedicineNiigata UniversityNiigataJapan
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48
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Helicobacter pylori Infection: One More Contributor to Nonalcoholic Fatty Liver Disease Pathophysiology. J Clin Gastroenterol 2019; 53:624-626. [PMID: 31033804 DOI: 10.1097/mcg.0000000000001218] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/17/2022]
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49
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Wang LP, Peng XY, Lv XQ, Liu L, Li XL, He X, Lv F, Pan Y, Wang L, Liu KF, Zhang XM. High throughput circRNAs sequencing profile of follicle fluid exosomes of polycystic ovary syndrome patients. J Cell Physiol 2019; 234:15537-15547. [PMID: 30779115 DOI: 10.1002/jcp.28201] [Citation(s) in RCA: 46] [Impact Index Per Article: 7.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/29/2018] [Revised: 01/04/2019] [Accepted: 01/10/2019] [Indexed: 01/24/2023]
Abstract
Polycystic ovary syndrome (PCOS) is one of the most prevalent reproductive disorders in women worldwide. Despite rigorous research, the exact molecular mechanism that governs PCOS pathogenesis remains unclear. To investigate the potential roles of circular RNAs (circRNAs), this study sequenced ribosomal RNA-depleted total RNA from exosomes of follicle fluids obtained from PCOS patients using non-PCOS samples as controls. Bioinformatic analysis identified 167 upregulated and 245 downregulated circRNAs from a total of 16,771 detected candidates. Functional analysis suggests that pathways related to bacterial infection, associated chronic inflammation, and oxidative stress could be targeted by the differential circRNAs in PCOS patients. The obtained sequencing results were further validated by quantitative reverse-transcription polymerase chain reaction and a circRNA-microRNA interaction network was constructed. The obtained results provide a valuable addition to the published studies on the mechanism of PCOS pathogenesis by revealing a wide variety of new circRNAs, miRNA, and gene targets that merit further investigation.
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Affiliation(s)
- Li-Ping Wang
- Department of Biobank, Clinical Medical College, Yangzhou University, Yangzhou, Jiangsu, China.,Northern Jiangsu People's Hospital, Yangzhou University, Yangzhou, Jiangsu, China.,Institute of Epigenetics and Epigenomics, College of Animal Science and Technology, Yangzhou University, Yangzhou, Jiangsu, China
| | - Xiao-Yu Peng
- Northern Jiangsu People's Hospital, Yangzhou University, Yangzhou, Jiangsu, China.,Department of Obstetrics and Gynecology, Reproductive Medicine Center, Clinical Medical College, Yangzhou University, Yangzhou, Jiangsu, China
| | - Xiao-Qin Lv
- Northern Jiangsu People's Hospital, Yangzhou University, Yangzhou, Jiangsu, China.,Department of Obstetrics and Gynecology, Reproductive Medicine Center, Clinical Medical College, Yangzhou University, Yangzhou, Jiangsu, China
| | - Lin Liu
- Northern Jiangsu People's Hospital, Yangzhou University, Yangzhou, Jiangsu, China.,Department of Obstetrics and Gynecology, Reproductive Medicine Center, Clinical Medical College, Yangzhou University, Yangzhou, Jiangsu, China
| | - Xue-Li Li
- Northern Jiangsu People's Hospital, Yangzhou University, Yangzhou, Jiangsu, China.,Department of Obstetrics and Gynecology, Reproductive Medicine Center, Clinical Medical College, Yangzhou University, Yangzhou, Jiangsu, China
| | - Xiao He
- Northern Jiangsu People's Hospital, Yangzhou University, Yangzhou, Jiangsu, China.,Department of Obstetrics and Gynecology, Reproductive Medicine Center, Clinical Medical College, Yangzhou University, Yangzhou, Jiangsu, China
| | - Fang Lv
- Northern Jiangsu People's Hospital, Yangzhou University, Yangzhou, Jiangsu, China.,Department of Obstetrics and Gynecology, Reproductive Medicine Center, Clinical Medical College, Yangzhou University, Yangzhou, Jiangsu, China
| | - Yu Pan
- Northern Jiangsu People's Hospital, Yangzhou University, Yangzhou, Jiangsu, China.,Department of Obstetrics and Gynecology, Reproductive Medicine Center, Clinical Medical College, Yangzhou University, Yangzhou, Jiangsu, China
| | - Li Wang
- Johns Hopkins University School of Medicine, Baltimore, Maryland
| | - Kai-Feng Liu
- Northern Jiangsu People's Hospital, Yangzhou University, Yangzhou, Jiangsu, China.,Department of Obstetrics and Gynecology, Reproductive Medicine Center, Clinical Medical College, Yangzhou University, Yangzhou, Jiangsu, China
| | - Xiao-Mei Zhang
- Northern Jiangsu People's Hospital, Yangzhou University, Yangzhou, Jiangsu, China.,Department of Obstetrics and Gynecology, Reproductive Medicine Center, Clinical Medical College, Yangzhou University, Yangzhou, Jiangsu, China
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50
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Lim SH, Kim N, Kwon JW, Kim SE, Baik GH, Lee JY, Park KS, Shin JE, Song HJ, Myung DS, Choi SC, Kim HJ, Lim JH, Yim JY, Kim JS. Positive Association Between Helicobacter pylori Infection and Metabolic Syndrome in a Korean Population: A Multicenter Nationwide Study. Dig Dis Sci 2019; 64:2219-2230. [PMID: 30852768 DOI: 10.1007/s10620-019-05544-3] [Citation(s) in RCA: 23] [Impact Index Per Article: 3.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/03/2018] [Accepted: 02/19/2019] [Indexed: 02/08/2023]
Abstract
BACKGROUND AND AIM Helicobacter pylori (H. pylori) infection causes extra-gastrointestinal as well as gastric diseases. This analytical cross-sectional study was performed to investigate the association between H. pylori infection and metabolic syndrome in a Korean population. METHODS Anthropometric and metabolic data, as well as anti-H. pylori IgG antibodies, were measured in 21,106 subjects who participated in a health checkup between January 2016 and June 2017. The classification of metabolic syndrome followed the revised National Cholesterol Education Program criteria. RESULTS After excluding subjects with a history of H. pylori eradication therapy, or gastric symptoms, the seropositivity of H. pylori was 43.2% in 15,195 subjects. H. pylori-positive participants had significantly higher body mass index (BMI), waist circumference, total cholesterol (TC), low-density lipoprotein cholesterol (LDL-C), and lower high-density lipoprotein (HDL-C) than did seronegative participants (P < 0.05). After adjusting for confounders, high TC, low HDL-C, and high LDL-C were associated with H. pylori seropositivity. Finally, the prevalence of metabolic syndrome was higher in H. pylori-seropositive subjects than in negative ones (27.2% vs. 21.0%, P < 0.05), and H. pylori seropositivity increased the likelihood of metabolic syndrome (OR 1.19, 95% CI 1.09-1.31, P < 0.001) after adjusting for sex, age, BMI, smoking, residence, household income, and education level. However, the association between H. pylori seropositivity and metabolic syndrome disappeared in those ≥ 65 years old. CONCLUSIONS H. pylori infection plays an independent role in the pathogenesis of metabolic syndrome in Koreans under 65 years old.
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Affiliation(s)
- Seon Hee Lim
- Department of Internal Medicine and Healthcare Research Institute, Healthcare System Gangnam Center Seoul National University Hospital, Seoul, South Korea
| | - Nayoung Kim
- Department of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, Gyeonggi-do, South Korea. .,Department of Internal Medicine and Liver Research Institute, Seoul National University College of Medicine, Seoul, South Korea.
| | - Jin Won Kwon
- College of Pharmacy, Kyungpook National University, Daegu, South Korea
| | - Sung Eun Kim
- Department of Internal Medicine, Kosin University College of Medicine, Busan, South Korea
| | - Gwang Ho Baik
- Department of Internal Medicine, Chuncheon Sacred Heart Hospital, Hallym University College of Medicine, Chuncheon, Kangwon-do, South Korea
| | - Ju Yup Lee
- Department of Internal Medicine, Keimyung University College of Medicine, Daegu, South Korea
| | - Kyung Sik Park
- Department of Internal Medicine, Keimyung University College of Medicine, Daegu, South Korea
| | - Jeong Eun Shin
- Department of Internal Medicine, Dankook University College of Medicine, Cheonan, Chungcheongnam-do, South Korea
| | - Hyun Joo Song
- Department of Internal Medicine, Jeju National University School of Medicine, Jeju, South Korea
| | - Dae-Seong Myung
- Department of Internal Medicine, Chonnam National University School of Medicine, Hwasun, Chollanam-do, South Korea
| | - Suck Chei Choi
- Department of Internal Medicine, Wonkwang University College of Medicine, Iksan, Chollabuk-do, South Korea
| | - Hyun Jin Kim
- Department of Internal Medicine and Institute of Health Science, Gyeongsang National University School of Medicine, Jinju, Gyeongsangnam-do, South Korea
| | - Joo Hyun Lim
- Department of Internal Medicine and Healthcare Research Institute, Healthcare System Gangnam Center Seoul National University Hospital, Seoul, South Korea
| | - Jeong Yoon Yim
- Department of Internal Medicine and Healthcare Research Institute, Healthcare System Gangnam Center Seoul National University Hospital, Seoul, South Korea
| | - Joo Sung Kim
- Department of Internal Medicine and Healthcare Research Institute, Healthcare System Gangnam Center Seoul National University Hospital, Seoul, South Korea.,Department of Internal Medicine and Liver Research Institute, Seoul National University College of Medicine, Seoul, South Korea
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