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Yonis N, Mousa A, Yousef MH, Ghouneimy AM, Dabbish AM, Abdelzaher H, Hussein MA, Ezzeldin S, Adel AA, Mahmoud YH, El-Khazragy N, Abdelnaser A. Cracking the code: lncRNA-miRNA-mRNA integrated network analysis unveiling lncRNAs as promising non-invasive NAFLD biomarkers toward precision diagnosis. Comput Biol Chem 2025; 115:108325. [PMID: 39832417 DOI: 10.1016/j.compbiolchem.2024.108325] [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: 11/13/2024] [Revised: 12/15/2024] [Accepted: 12/22/2024] [Indexed: 01/22/2025]
Abstract
BACKGROUND Non-alcoholic fatty liver disease (NAFLD) involves abnormal fat accumulation in the liver, mainly as triglycerides. It ranges from steatosis to non-alcoholic steatohepatitis (NASH), which can lead to inflammation, cellular damage, liver fibrosis, cirrhosis, or hepatocellular carcinoma (HCC). Long non-coding RNAs (lncRNAs) are crucial for regulating gene expression across various conditions. LncRNAs are emerging as potential putative diagnostic markers for NAFLD-associated HCC. METHODS We used two human and two mouse datasets from the Gene Expression Omnibus to analyze the expression profiles of mRNAs and lncRNAs. We created a network linking lncRNAs, miRNAs, and mRNAs to investigate the relationships among these RNA types. Additionally, we identified NAFLD-related lncRNAs from existing literature. We then quantified the expression levels of four specific lncRNAs, including PVT1, DUBR, SNHG17, and SNHG14, in the serum of 92 Egyptian participants using qPCR. Finally, we performed a Receiver Operating Characteristic analysis to evaluate the diagnostic potential of the candidate lncRNAs. RESULTS Our data suggests that maternally expressed gene 3 (MEG3), H19, and DPPA2 Upstream Binding RNA (DUBR) were significantly upregulated, and plasmacytoma variant translocation 1 (PVT1) was markedly downregulated. PVT1 showed the highest diagnostic accuracy for both NAFLD and NASH. The combined panels of PVT1 +H19 for NAFLD and PVT1 +H19 +DUBR for NASH demonstrated high diagnostic potential. Uniquely, PVT1 can distinguish between NAFLD and NASH. PVT1 exhibited strong diagnostic potential for NAFLD and NASH, individually and in combination with other lncRNAs. CONCLUSION Our study identifies four lncRNAs as putative biomarkers with high specificity and accuracy, individually or combined, for differentiating between NAFLD and NASH. Healthy volunteers with PVT1 possess the highest diagnostic accuracy and significantly discriminate between NAFLD and NASH.
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Affiliation(s)
- Nouran Yonis
- Institute of Global Health and Human Ecology (IGHHE), School of Sciences and Engineering, The American University in Cairo, New Cairo 11835, Egypt
| | - Ahmed Mousa
- University of Science and Technology, Zewail City of Science and Technology, Giza, Egypt
| | - Mohamed H Yousef
- Biotechnology Graduate Program, School of Sciences and Engineering, The American University in Cairo, New Cairo 11835, Egypt
| | - Ahmed M Ghouneimy
- Department of Biology, School of Sciences and Engineering, The American University in Cairo, New Cairo 11835, Egypt
| | - Areeg M Dabbish
- Biotechnology Graduate Program, School of Sciences and Engineering, The American University in Cairo, New Cairo 11835, Egypt
| | - Hana Abdelzaher
- Institute of Global Health and Human Ecology (IGHHE), School of Sciences and Engineering, The American University in Cairo, New Cairo 11835, Egypt
| | - Mohamed Ali Hussein
- Institute of Global Health and Human Ecology (IGHHE), School of Sciences and Engineering, The American University in Cairo, New Cairo 11835, Egypt
| | - Shahd Ezzeldin
- Basic Research Department, Proteomics and Metabolomics Research Program, Children's Cancer Hospital 57357 (CCHE-57357), Cairo, Egypt
| | - Abdelmoneim A Adel
- Hematology and Gastroenterology Department, National Hepatology and Tropical Medicine Research Institute (NHTMRI), Egypt
| | - Yosra H Mahmoud
- Hematology and Gastroenterology Department, National Hepatology and Tropical Medicine Research Institute (NHTMRI), Egypt
| | - Nashwa El-Khazragy
- Clinical Pathology and Hematology Department, Faculty of Medicine, Ain Shams University Biomedical Research Department, Cairo 11381, Egypt
| | - Anwar Abdelnaser
- Institute of Global Health and Human Ecology (IGHHE), School of Sciences and Engineering, The American University in Cairo, New Cairo 11835, Egypt.
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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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3
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Gou GE, Li T, Liu CR, Meng T, Li YP. Potential mechanisms and therapeutic prospects of the association between Helicobacter pylori infection and metabolic dysfunction-associated steatohepatitis. World J Hepatol 2025; 17:101798. [PMID: 39871896 PMCID: PMC11736473 DOI: 10.4254/wjh.v17.i1.101798] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/27/2024] [Revised: 11/13/2024] [Accepted: 11/22/2024] [Indexed: 01/06/2025] Open
Abstract
Helicobacter pylori (H. pylori) infection is a known inducer of various gastrointestinal diseases, including gastritis, gastric ulcers, and gastric cancer. However, in recent years, research on the potential association between H. pylori infection and metabolic dysfunction-associated steatohepatitis (MASH) has been scarce. This large-scale multicenter study, covering more than 360 hospitals across 26 medical systems in the United States, systematically evaluated the association between H. pylori infection and MASH. This paper reviews the innovative aspects of this study, discusses its significance in the current research field of H. pylori and liver diseases, analyzes potential molecular mechanisms, and suggests future research directions and therapeutic prospects.
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Affiliation(s)
- Guo-E Gou
- Department of Infectious Diseases, Xi'an Jiaotong University Second Affiliated Hospital, Xi'an 710004, Shaanxi Province, China
| | - Ting Li
- Department of Infectious Diseases, Xi'an Jiaotong University Second Affiliated Hospital, Xi'an 710004, Shaanxi Province, China
| | - Chen-Rui Liu
- Department of Infectious Diseases, Xi'an Jiaotong University Second Affiliated Hospital, Xi'an 710004, Shaanxi Province, China
| | - Ting Meng
- Department of Infectious Diseases, Xi'an Jiaotong University Second Affiliated Hospital, Xi'an 710004, Shaanxi Province, China
| | - Ya-Ping Li
- Department of Infectious Diseases, Xi'an Jiaotong University Second Affiliated Hospital, Xi'an 710004, Shaanxi Province, China.
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Amal Mohammed AM, El-Hennawy AY, Hassan EH, Mohamed B, Abdelraouf A, Abdelhaleem A, El-Shahat MG, Eldein ME. Detection of H-Pylori in the Explanted Liver Tissue and the Enlarged Perihepatic Lymph Nodes of Cirrhotic Patients with Decompensated End-Stage Liver Disease Recruited for Liver Transplantation. Asian Pac J Cancer Prev 2025; 26:181-187. [PMID: 39874000 PMCID: PMC12082423 DOI: 10.31557/apjcp.2025.26.1.181] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/25/2024] [Accepted: 01/21/2024] [Indexed: 01/30/2025] Open
Abstract
BACKGROUND Helicobacter pylori bacteria colonize the gastric mucosa and contribute to the occurrence and development of gastrointestinal diseases. According to the WHO, H. pylori bacteria are considered class I carcinogen. OBJECTIVES To detect Helicobacter pylori organisms by IHC expression of anti-H. Pylori antibodies in the explanted liver tissue; and enlarged perihepatic lymph nodes of cirrhotic liver; to detect any relation between the presence of the organism and histopathological findings in the liver tissue. MATERIALS AND METHODS This retrospective cross-sectional study included forty cases of cirrhotic patients with decompensated end-stage liver, recruited for liver transplantation based on combined clinical, radiological, and histological data. Samples were immunohistochemically analyzed for anti-H-Pylori antibodies to detect Helicobacter pylori organisms in the explanted liver tissue and enlarged perihepatic lymph nodes. The presence of the organism was correlated with clinic-pathologic variables. RESULTS Eighty-five percent (34 cases) and seventy percent (28 cases) of cases were positive for anti-H-Pylori antibodies in the liver and lymph nodal tissues, respectively. More than eighty percent (14 cases) and half of the studied cases (8 cases) showed dysplasia in liver tissue expressing anti-H-Pylori-antibody in the liver tissue and the lymph nodes, respectively. All HCC cases expressed anti-H-Pylori antibody in the liver tissue and the lymph nodes. The relation between anti-H-Pylori antibody expression in lymph nodes and the presence of dysplasia or HCC in liver tissue was statistically significant (p-value = 0.037 and p-value = 0.041 respectively). CONCLUSION Our results conclude that there is a pathogenic role of extra-gastric H-Pylori colonization in lymph nodal tissue and in liver tissue, and it may be preventable by treating H. pylori, especially if treatment can be started very early.
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Affiliation(s)
| | - Ahmed Y El-Hennawy
- Department of Anatomic Pathology, Faculty of Medicine, Kasralainy, Cairo University, Cairo, Egypt
| | - Ehsan H. Hassan
- Pathology Department, National Hepatology and Tropical Medicine Research Institute (NHTMRI), Cairo, Egypt
| | - Basma Mohamed
- Pathology Department, National Hepatology and Tropical Medicine Research Institute (NHTMRI), Cairo, Egypt
| | | | | | - Mariam Georgey El-Shahat
- Pathology Department, National Hepatology and Tropical Medicine Research Institute (NHTMRI), Cairo, Egypt
| | - Maha Emad Eldein
- Department of Anatomic Pathology, Faculty of Medicine, Kasralainy, Cairo University, Cairo, Egypt
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5
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Gulati A, Roytman M, Lin J, McGrath M, Klar A, Boone K, Higa K, Ma P. Association between Helicobacter pylori infection, MASLD, and liver fibrosis in patients with severe obesity: a single-center experience. Surg Endosc 2024; 38:6873-6879. [PMID: 39192041 DOI: 10.1007/s00464-024-11177-z] [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: 05/30/2024] [Accepted: 08/05/2024] [Indexed: 08/29/2024]
Abstract
BACKGROUND AND METHODS Our study sought to evaluate if an association exists between Helicobacter pylori (H. pylori), metabolic dysfunction- associated steatotic liver disease (MASLD), and liver fibrosis in patients with severe obesity (BMI > 35). Our retrospective study included 584 patients over the age of 18 years with severe obesity, who underwent preoperative liver transient elastography (VCTE), upper endoscopy, blood work, and intra-operative liver biopsy concurrent with bariatric surgery at a single institution from July 2020 to September 2021. Liver fibrosis scores including FIB-4, APRI, NAFLD fibrosis score, BARD score, AST: ALT ratio, and NAFLD activity score (NAS) were calculated from the laboratory results and liver biopsy findings. The presence or absence of H. pylori was determined based on gastric biopsies obtained during upper endoscopy. Other variables collected included age, gender, mean preoperative weight, BMI, and the presence or absence of comorbidities. Student's t-test and non-parametric testing were used for the analysis of continuous variables and Chi-square analysis was used for categorical data. RESULTS Of the 584 patients, 14.7% were H. pylori positive and 85.3% were negative. Liver fibrosis scores including FIB-4, APRI, and NAFLD fibrosis scores were significantly higher in the positive group (p < 0.05), but there was no difference in AST: ALT ratio and BARD score. A significantly higher VCTE steatosis and fibrosis scores were noted in the H. pylori-positive group (p < 0.05). Similarly, a significantly higher NAS (NAFLD activity score) on liver biopsies was noted in the positive group, with all the individual components of NAS (steatosis, lobular inflammation, and hepatocyte ballooning) being significantly higher in the positive group (p < 0.05). A significantly higher incidence of fibrosis on liver biopsies was noted in the positive group overall and across all stages of fibrosis (p < 0.05). There were no significant differences between the groups in relation to gender, mean weight, BMI, presence of comorbidities including Diabetes Mellitus, and laboratory values. CONCLUSION Our study demonstrates that H. pylori colonization or infection is associated with a higher risk of development of MASLD and progression to fibrosis. Further, population-based studies are needed to corroborate our findings.
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Affiliation(s)
| | | | - Joanne Lin
- Temple University, Philadelphia, PA, USA
| | | | - Amarita Klar
- Fresno Heart and Surgical Hospital, Fresno, CA, USA
| | - Keith Boone
- Fresno Heart and Surgical Hospital, Fresno, CA, USA
| | - Kelvin Higa
- Fresno Heart and Surgical Hospital, Fresno, CA, USA
| | - Pearl Ma
- Fresno Heart and Surgical Hospital, Fresno, CA, USA
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6
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Abdel-Razeq R, Bitar L, Bitar ER, Onwuzo C, Abu-Hammour MN, Eren B, Mohamed I, Johnson A, Boustany A, Onwuzo S, Asaad I. Prevalence and risk factors associated with metabolic dysfunction-associated steatohepatitis in patients with Helicobacter pylori infection: A population-based study. World J Hepatol 2024; 16:1349-1356. [DOI: 10.4254/wjh.v16.i10.1349] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/31/2024] [Revised: 09/03/2024] [Accepted: 09/23/2024] [Indexed: 11/22/2024] Open
Abstract
BACKGROUND Helicobacter pylori (H. pylori) is associated with the development of gastrointestinal disorders ranging from gastritis to gastric cancer. The evidence of the association between metabolic dysfunction-associated steatohepatitis (MASH) and H. pylori infection in the literature is scarce. Therefore, we aim to evaluate the risk of developing MASH in patients who have had a diagnosis of H. pylori infection independently of any confounding variables.
AIM To evaluate the risk of developing MASH in patients who have had a diagnosis of H. pylori infection.
METHODS This study used a validated multicenter research database of over 360 hospitals across 26 healthcare systems across the United States from 1999 to 2022. Multivariate regression analysis assessed the risk of developing MASH, adjusting for confounders including H. pylori infection, obesity, type 2 diabetes, hypertension, dyslipidemia, and male gender. A two-sided P value < 0.05 was considered as statistically significant, and all statistical analyses were performed using R version 4.0.2 (R Foundation for Statistical Computing, Vienna, Austria, 2008).
RESULTS A total of 79476132 individuals were screened in the database and 69232620 were selected in the final analysis after accounting for inclusion and exclusion criteria. Smokers (14.30%), patients with hyperlipidemia (70.35%), hypertension (73.86%), diabetes mellitus type 2 (56.46%), and obese patients (58.15%) were more common in patients with MASH compared to control. Using a multivariate regression analysis, the risk of MASH was increased in diabetics [odds ratio (OR): 3.55; 95%CI: 3.48-3.62], obese (OR: 5.93; 95%CI: 5.81-6.04), males (OR: 1.49; 95%CI: 1.46-1.52), individuals with hyperlipidemia (OR: 2.43; 95%CI: 2.38-2.49) and H. pylori infection (OR: 2.51; 95%CI: 2.31-2.73).
CONCLUSION This is the largest population-based study in the United States illustrating an increased prevalence and odds of developing MASH in patients with H. pylori infection after adjusting for risk factors.
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Affiliation(s)
- Rashid Abdel-Razeq
- Department of Internal Medicine, Cleveland Clinic Foundation, Cleveland, OH 44111, United States
| | - Lynn Bitar
- Faculty of Medicine, Saint Joseph University of Beirut, Beirut 1104 2020, Lebanon
| | - Elio R Bitar
- Faculty of Medicine, American University of Beirut, Beirut 1107 2020, Lebanon
| | - Chidera Onwuzo
- Department of Medicine & Surgery, General Hospital Lagos Island, Lagos Island 101223, Lagos, Nigeria
| | - Mohamad-Noor Abu-Hammour
- Department of Internal Medicine, Cleveland Clinic Foundation, Cleveland, OH 44111, United States
| | - Barish Eren
- Department of Internal Medicine, Cleveland Clinic Foundation, Cleveland, OH 44111, United States
| | - Islam Mohamed
- Department of Internal Medicine, Cleveland Clinic Foundation, Cleveland, OH 44111, United States
| | - Adejoke Johnson
- Department of Internal Medicine, Jacobi Medical Center/North Central Bronx Hospital, Bronx, NY 10461, United States
| | - Antoine Boustany
- Division of Gastroenterology, Department of Internal Medicine, University of Florida College of Medicine, Jacksonville, FL 32209, United States
| | - Somtochukwu Onwuzo
- Department of Gastroenterology, Allegheny General Hospital, Pittsburgh, PA 15212, United States
| | - Imad Asaad
- Department of Gastroenterology, Firelands Health, Sandusky, OH 44870, United States
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7
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Abdel-Razeq R, Bitar L, Bitar ER, Onwuzo C, Abu-Hammour MN, Eren B, Mohamed I, Johnson A, Boustany A, Onwuzo S, Asaad I. Prevalence and risk factors associated with metabolic dysfunction-associated steatohepatitis in patients with Helicobacter pylori infection: A population-based study. World J Hepatol 2024; 16:1169-1176. [PMID: 39474577 PMCID: PMC11514611 DOI: 10.4254/wjh.v16.i10.1169] [Citation(s) in RCA: 4] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/31/2024] [Revised: 09/03/2024] [Accepted: 09/23/2024] [Indexed: 10/21/2024] Open
Abstract
BACKGROUND Helicobacter pylori (H. pylori) is associated with the development of gastrointestinal disorders ranging from gastritis to gastric cancer. The evidence of the association between metabolic dysfunction-associated steatohepatitis (MASH) and H. pylori infection in the literature is scarce. Therefore, we aim to evaluate the risk of developing MASH in patients who have had a diagnosis of H. pylori infection independently of any confounding variables.
AIM To evaluate the risk of developing MASH in patients who have had a diagnosis of H. pylori infection.
METHODS This study used a validated multicenter research database of over 360 hospitals across 26 healthcare systems across the United States from 1999 to 2022. Multivariate regression analysis assessed the risk of developing MASH, adjusting for confounders including H. pylori infection, obesity, type 2 diabetes, hypertension, dyslipidemia, and male gender. A two-sided P value < 0.05 was considered as statistically significant, and all statistical analyses were performed using R version 4.0.2 (R Foundation for Statistical Computing, Vienna, Austria, 2008).
RESULTS A total of 79476132 individuals were screened in the database and 69232620 were selected in the final analysis after accounting for inclusion and exclusion criteria. Smokers (14.30%), patients with hyperlipidemia (70.35%), hypertension (73.86%), diabetes mellitus type 2 (56.46%), and obese patients (58.15%) were more common in patients with MASH compared to control. Using a multivariate regression analysis, the risk of MASH was increased in diabetics [odds ratio (OR): 3.55; 95%CI: 3.48-3.62], obese (OR: 5.93; 95%CI: 5.81-6.04), males (OR: 1.49; 95%CI: 1.46-1.52), individuals with hyperlipidemia (OR: 2.43; 95%CI: 2.38-2.49) and H. pylori infection (OR: 2.51; 95%CI: 2.31-2.73).
CONCLUSION This is the largest population-based study in the United States illustrating an increased prevalence and odds of developing MASH in patients with H. pylori infection after adjusting for risk factors.
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Affiliation(s)
- Rashid Abdel-Razeq
- Department of Internal Medicine, Cleveland Clinic Foundation, Cleveland, OH 44111, United States
| | - Lynn Bitar
- Faculty of Medicine, Saint Joseph University of Beirut, Beirut 1104 2020, Lebanon
| | - Elio R Bitar
- Faculty of Medicine, American University of Beirut, Beirut 1107 2020, Lebanon
| | - Chidera Onwuzo
- Department of Medicine & Surgery, General Hospital Lagos Island, Lagos Island 101223, Lagos, Nigeria
| | - Mohamad-Noor Abu-Hammour
- Department of Internal Medicine, Cleveland Clinic Foundation, Cleveland, OH 44111, United States
| | - Barish Eren
- Department of Internal Medicine, Cleveland Clinic Foundation, Cleveland, OH 44111, United States
| | - Islam Mohamed
- Department of Internal Medicine, Cleveland Clinic Foundation, Cleveland, OH 44111, United States
| | - Adejoke Johnson
- Department of Internal Medicine, Jacobi Medical Center/North Central Bronx Hospital, Bronx, NY 10461, United States
| | - Antoine Boustany
- Division of Gastroenterology, Department of Internal Medicine, University of Florida College of Medicine, Jacksonville, FL 32209, United States
| | - Somtochukwu Onwuzo
- Department of Gastroenterology, Allegheny General Hospital, Pittsburgh, PA 15212, United States
| | - Imad Asaad
- Department of Gastroenterology, Firelands Health, Sandusky, OH 44870, United States
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8
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Zhao SQ, Zheng HL, Zhong XT, Wang ZY, Su Y, Shi YY. Effects and mechanisms of Helicobacter pylori infection on the occurrence of extra-gastric tumors. World J Gastroenterol 2024; 30:4090-4103. [DOI: 10.3748/wjg.v30.i37.4090] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/09/2024] [Revised: 08/23/2024] [Accepted: 09/12/2024] [Indexed: 09/26/2024] Open
Abstract
Helicobacter pylori (H. pylori) colonizes the human stomach and many studies have discussed the mechanisms of H. pylori infection leading to gastric diseases, including gastric cancer. Additionally, increasing data have shown that the infection of H. pylori may contribute to the development of extra-gastric diseases and tumors. Inflammation, systemic immune responses, microbiome disorders, and hypergastrinemia caused by H. pylori infection are associated with many extra-gastric malignancies. This review highlights recent discoveries; discusses the relationship between H. pylori and various extra-gastric tumors, such as colorectal cancer, lung cancer, cholangiocarcinoma, and gallbladder carcinoma; and explores the mechanisms of extra-gastric carcinogenesis by H. pylori. Overall, these findings refine our understanding of the pathogenic processes of H. pylori, provide guidance for the clinical treatment and management of H. pylori-related extra-gastric tumors, and help improve prognosis.
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Affiliation(s)
- Shi-Qing Zhao
- Research Center of Clinical Epidemiology, Peking University Third Hospital, Beijing 100191, China
- Health Science Center, Peking University, Beijing 100191, China
| | - Hui-Ling Zheng
- Department of Gastroenterology, Peking University Third Hospital, Beijing 100191, China
| | - Xiao-Tian Zhong
- Research Center of Clinical Epidemiology, Peking University Third Hospital, Beijing 100191, China
- Health Science Center, Peking University, Beijing 100191, China
| | - Zi-Ye Wang
- Research Center of Clinical Epidemiology, Peking University Third Hospital, Beijing 100191, China
- Health Science Center, Peking University, Beijing 100191, China
| | - Yi Su
- Research Center of Clinical Epidemiology, Peking University Third Hospital, Beijing 100191, China
- Health Science Center, Peking University, Beijing 100191, China
| | - Yan-Yan Shi
- Research Center of Clinical Epidemiology, Peking University Third Hospital, Beijing 100191, China
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9
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Mantovani A, Lando MG, Borella N, Scoccia E, Pecoraro B, Gobbi F, Bisoffi Z, Valenti L, Tilg H, Byrne CD, Targher G. Relationship between Helicobacter pylori infection and risk of metabolic dysfunction-associated steatotic liver disease: An updated meta-analysis. Liver Int 2024; 44:1513-1525. [PMID: 38567962 DOI: 10.1111/liv.15925] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 01/23/2024] [Revised: 03/01/2024] [Accepted: 03/22/2024] [Indexed: 06/19/2024]
Abstract
BACKGROUND Recent observational studies examining the association between Helicobacter pylori infection and the risk of metabolic dysfunction-associated steatotic liver disease (MASLD) have reported conflicting results. We performed a meta-analysis to quantify the magnitude of the association between H. pylori infection and the risk of MASLD. METHODS We systematically searched three large electronic databases to identify eligible observational studies (published up to 30 November 2023) in which liver biopsy, imaging methods or blood-based biomarkers/scores were used for diagnosing MASLD. Data from selected studies were extracted, and meta-analysis was performed using common and random-effects modelling. Statistical heterogeneity among published studies, subgroup analyses, meta-regression analyses and publication bias were assessed. RESULTS A total of 28 observational studies (24 cross-sectional and 4 longitudinal studies) were identified, including 231 291 middle-aged individuals of predominantly Asian ethnicity (~95%). Meta-analysis of cross-sectional studies showed that H. pylori infection was significantly associated with a small increase in the risk of prevalent MASLD (n = 24 studies; random-effects odds ratio 1.11, 95% CI 1.05-1.18; I2 = 63%). Meta-analysis of data from longitudinal studies showed that H. pylori infection was significantly associated with an increased risk of developing incident MASLD over a mean 5-year follow-up (n = 4 studies; random-effects odds ratio 1.20, 95%CI 1.08-1.33; I2 = 44%). Sensitivity analyses did not modify these results. The funnel plot did not reveal any significant publication bias. CONCLUSIONS H. pylori infection is associated with a mildly increased risk of prevalent and incident MASLD. Further well-designed prospective and mechanistic studies are required to better decipher the complex link between H. pylori infection and the risk of MASLD.
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Affiliation(s)
- Alessandro Mantovani
- Section of Endocrinology, Diabetes and Metabolism, Department of Medicine, University and Azienda Ospedaliera Universitaria Integrata of Verona, Verona, Italy
| | - Maria Giovanna Lando
- Section of Endocrinology, Diabetes and Metabolism, Department of Medicine, University and Azienda Ospedaliera Universitaria Integrata of Verona, Verona, Italy
| | - Nicolò Borella
- Section of Endocrinology, Diabetes and Metabolism, Department of Medicine, University and Azienda Ospedaliera Universitaria Integrata of Verona, Verona, Italy
| | - Enrico Scoccia
- Section of Endocrinology, Diabetes and Metabolism, Department of Medicine, University and Azienda Ospedaliera Universitaria Integrata of Verona, Verona, Italy
| | - Barbara Pecoraro
- Section of Endocrinology, Diabetes and Metabolism, Department of Medicine, University and Azienda Ospedaliera Universitaria Integrata of Verona, Verona, Italy
| | - Federico Gobbi
- Department of Infectious Tropical Diseases and Microbiology, IRCCS Sacro Cuore - Don Calabria Hospital, Negrar di Valpolicella, Italy
- Department of Clinical and Experimental Sciences, University of Brescia, Brescia, Italy
| | - Zeno Bisoffi
- Department of Infectious Tropical Diseases and Microbiology, IRCCS Sacro Cuore - Don Calabria Hospital, Negrar di Valpolicella, Italy
| | - Luca Valenti
- Precision Medicine-Biological Resource Center, Transfusion Medicine, Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico Milano, Milan, Italy
- Department of Pathophysiology and Transplantation, University of Milan, Milan, Italy
| | - Herbert Tilg
- Department of Internal Medicine I, Gastroenterology, Hepatology, Endocrinology and Metabolism, Medical University Innsbruck, Innsbruck, Austria
| | - Christopher D Byrne
- National Institute for Health and Care Research, Southampton Biomedical Research Centre, University Hospital Southampton and University of Southampton, Southampton, UK
| | - Giovanni Targher
- Department of Medicine, University of Verona, Verona, Italy
- Metabolic Diseases Research Unit, IRCCS Sacro Cuore - Don Calabria Hospital, Negrar di Valpolicella, Italy
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10
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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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11
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Mohammadi M, Attar A, Mohammadbeigi M, Peymani A, Bolori S, Fardsanei F. The possible role of Helicobacter pylori in liver diseases. Arch Microbiol 2023; 205:281. [PMID: 37430019 DOI: 10.1007/s00203-023-03602-z] [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: 02/27/2023] [Revised: 05/15/2023] [Accepted: 05/29/2023] [Indexed: 07/12/2023]
Abstract
According to previous studies, Helicobacter pylori infection is associated with liver disease. In order to better understand the risk of acquiring various liver diseases, we reviewed current knowledge on the impact of H. pylori on the onset, intensification, and progression of various liver diseases caused by the infection of H. pylori. It has been estimated that between 50 and 90% of people worldwide have been infected with H. pylori. The bacterium is mostly responsible for inflamed gastric mucosa, ulcers, and cancers associated with the gastric mucosa. Through the active antioxidant system in H. pylori, the bacteria can neutralize free radicals by synthesizing VacA, a toxin that causes cell damage and apoptosis. Furthermore, there is a possibility that CagA genes may play a role in cancer development. People who have been infected with H. pylori are likely to develop lesions in the skin, the circulation system, and the pancreas. Moreover, transferring blood from the stomach may allow H. pylori to colonize the liver. The bacterium worsened liver function during autoimmune inflammation, toxic injury, chronic HCV infection, chronic HBV infection, and liver cirrhosis. Increasing portal pressure, hyperammonemia, and esophageal varices may be associated with H pylori infection. As a result, it is crucial to diagnose and treat this infection in patients with H. pylori.
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Affiliation(s)
- Mahnaz Mohammadi
- Medical Microbiology Research Center, Qazvin University of Medical Sciences, Qazvin, Iran
| | - Adeleh Attar
- Medical Microbiology Research Center, Qazvin University of Medical Sciences, Qazvin, Iran
| | - Maryam Mohammadbeigi
- Medical Microbiology Research Center, Qazvin University of Medical Sciences, Qazvin, Iran
| | - Amir Peymani
- Medical Microbiology Research Center, Qazvin University of Medical Sciences, Qazvin, Iran
| | - Shahin Bolori
- Medical Microbiology Research Center, Qazvin University of Medical Sciences, Qazvin, Iran
| | - Fatemeh Fardsanei
- Medical Microbiology Research Center, Qazvin University of Medical Sciences, Qazvin, Iran.
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12
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Krishnan A, Woreta TA, Sims OT, Hamilton JP, Potter JJ, Alqahtani SA. Impact of nonalcoholic fatty liver disease on clinical outcomes in patients with COVID-19 among persons living with HIV: A multicenter research network study. J Infect Public Health 2023; 16:673-679. [PMID: 36931143 PMCID: PMC9922673 DOI: 10.1016/j.jiph.2023.02.008] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/22/2022] [Revised: 01/22/2023] [Accepted: 02/08/2023] [Indexed: 02/16/2023] Open
Abstract
BACKGROUND People living with human immunodeficiency virus (PLWH) are at an increased risk of nonalcoholic fatty liver disease (NAFLD) but how these patients react to COVID-19 infection is unclear. We examined the clinical characteristics and outcomes of patients with and without nonalcoholic fatty liver disease (NAFLD) among people living with human immunodeficiency virus (PLWH) diagnosed with COVID-19. METHODS A multicenter, retrospective cohort study was conducted using TriNetX. Participants diagnosed with COVID-19 between January 20, 2020, and October 31, 2021, in PLWH were identified and divided into cohorts based on preexisting NAFLD. The primary outcome was all-cause mortality, and secondary outcomes were hospitalization, severe disease, critical care, need for mechanical ventilation, and acute kidney injury(AKI). Propensity score matching (PSM) mitigated the imbalance among group covariates. Risk ratios (RR) with 95 % confidence intervals (CI) were calculated. RESULTS Of the 5012 PLWH identified with confirmed COVID-19 during the study period, 563 had a diagnosis of NAFLD. After PSM, both groups were well-matched with 561 patients. The primary outcome did not differ between the cohorts at 30-days, even after a fully adjusted analysis, and the risk of all-cause mortality did not differ at 60 and 90 days. NAFLD had a significantly higher risk for hospitalization rates (RR 1.32; 95 % CI, 1.06-1.63) and AKI (RR 2.55; 95 % CI 1.42-4.57) than the non-NAFLD group at 30 days. No other differences were detected in other secondary outcome measures. CONCLUSIONS Preexisting NAFLD is associated with an increased risk for hospitalization and AKI among PLWH infected with COVID-19. The potential role of NAFLD in developing severe COVID-19 among PLWH remains to be elucidated in future studies. Still, this study indicates the need for careful monitoring of this at-risk population.
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Affiliation(s)
- Arunkumar Krishnan
- Division of Gastroenterology and Hepatology, Johns Hopkins University School of Medicine, Baltimore, MD 21287, USA; Section of Gastroenterology and Hepatology, West Virginia University School of Medicine, Morgantown, WV 26506, USA.
| | - Tinsay A Woreta
- Division of Gastroenterology and Hepatology, Johns Hopkins University School of Medicine, Baltimore, MD 21287, USA
| | - Omar T Sims
- Department of Gastroenterology, Hepatology and Nutrition, Cleveland Clinic Foundation, Cleveland, OH, USA; Department of Quantitative Health Sciences, Cleveland Clinic Foundation, Cleveland, OH, USA
| | - James P Hamilton
- Division of Gastroenterology and Hepatology, Johns Hopkins University School of Medicine, Baltimore, MD 21287, USA
| | - James J Potter
- Division of Gastroenterology and Hepatology, Johns Hopkins University School of Medicine, Baltimore, MD 21287, USA
| | - Saleh A Alqahtani
- Division of Gastroenterology and Hepatology, Johns Hopkins University School of Medicine, Baltimore, MD 21287, USA; Liver Transplant Center, King Faisal Specialist Hospital & Research Center, Riyadh 12713, Saudi Arabia.
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13
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Yang H, Mou Y, Hu B. Discussion on the common controversies of Helicobacter pylori infection. Helicobacter 2023; 28:e12938. [PMID: 36436202 DOI: 10.1111/hel.12938] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 08/14/2022] [Revised: 11/02/2022] [Accepted: 11/03/2022] [Indexed: 11/28/2022]
Abstract
BACKGROUND Helicobacter pylori ( H. pylori ) can persistently colonize on the gastric mucosa after infection and cause gastritis, atrophy, metaplasia, and even gastric cancer (GC). METHODS Therefore, the detection and eradication of H. pylori are the prerequisite. RESULTS Clinically, there are some controversial issues, such as why H. pylori infection is persistent, why it translocases along with the lesser curvature of the stomach, why there is oxyntic antralization, what the immunological characteristic of gastric chronic inflammation caused by H. pylori is, whether H. pylori infection is associated with extra-gastric diseases, whether chronic atrophic gastritis (CAG) is reversible, and what the potential problems are after H. pylori eradication. What are the possible answers? CONCLUSION In the review, we will discuss these issues from the attachment to eradication in detail.
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Affiliation(s)
- Hang Yang
- Department of Gastroenterology, West China Hospital, Sichuan University, Chengdu, China
| | - Yi Mou
- Department of Gastroenterology, West China Hospital, Sichuan University, Chengdu, China
| | - Bing Hu
- Department of Gastroenterology, West China Hospital, Sichuan University, Chengdu, China
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14
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Xu G, Ma S, Dong L, Mendez-Sanchez N, Li H, Qi X. Relationship of Helicobacter pylori Infection with Nonalcoholic Fatty Liver Disease: A Meta-Analysis. Can J Gastroenterol Hepatol 2023; 2023:5521239. [PMID: 36742347 PMCID: PMC9891807 DOI: 10.1155/2023/5521239] [Citation(s) in RCA: 2] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 11/08/2022] [Revised: 12/17/2022] [Accepted: 12/24/2022] [Indexed: 01/27/2023] Open
Abstract
BACKGROUND AND AIMS Helicobacter pylori (H. pylori) and nonalcoholic fatty liver disease (NAFLD) have become increasingly recognized, both of which affect human health globally. The association of H. pylori infection with NAFLD remains unclear. METHODS PubMed, EMBASE, and Cochrane Library databases were searched. Only a random-effects model was used. Odds ratios (ORs) and risk ratios (RRs) with 95% confidence intervals (CIs) were calculated for the combined estimates of raw data. Adjusted ORs (aORs) and hazard ratios (aHRs) with 95% CIs were calculated for the combined estimates of data adjusted for confounders. RESULTS Thirty-four studies with 218573 participants were included. Based on unadjusted data from 26 cross-sectional studies and 3 case-control studies, H. pylori infection was significantly associated with the presence of NAFLD (OR = 1.26, 95% CI = 1.17-1.36, P < 0.001). Based on adjusted data from 15 cross-sectional studies and 1 case-control study, H. pylori infection was significantly associated with the presence of NAFLD (aOR = 1.25, 95% CI = 1.08-1.44, P < 0.001). Compared with control subjects without NAFLD, patients with moderate (OR = 1.67, 95% CI = 1.17-2.39, P = 0.005) and severe (OR = 1.71, 95% CI = 1.30-2.24, P < 0.001) NAFLD, but not those with mild NAFLD (OR = 1.14, 95% CI = 0.9-1.45, P = 0.286), had significantly higher proportions of H. pylori infection. The association of H. pylori infection with the occurrence of NAFLD was statistically significant based on adjusted data from 3 cohort studies (aHR = 1.18, 95% CI = 1.05-1.34, P = 0.007), but not based on unadjusted data from 3 cohort studies (RR = 1.41, 95% CI = 0.80-2.48, P = 0.237). CONCLUSION H. pylori infection is associated with NAFLD, especially moderate and severe NAFLD. The impact of H. pylori eradication on the prevention of NAFLD should be further explored.
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Affiliation(s)
- Guangqin Xu
- Department of Gastroenterology, General Hospital of Northern Theater Command, Shenyang 110840, China
- Postgraduate College, Dalian Medical University, Dalian 116044, China
| | - Shaoze Ma
- Department of Gastroenterology, General Hospital of Northern Theater Command, Shenyang 110840, China
- Postgraduate College, Dalian Medical University, Dalian 116044, China
| | - Liyan Dong
- Department of Gastroenterology, General Hospital of Northern Theater Command, Shenyang 110840, China
- Postgraduate College, China Medical University, Shenyang 110122, China
| | - Nahum Mendez-Sanchez
- Liver Research Unit, Medica Sur Clinic & Foundation, Faculty of Medicine, National Autonomous University of Mexico, Mexico City, Mexico
| | - Hongyu Li
- Department of Gastroenterology, General Hospital of Northern Theater Command, Shenyang 110840, China
- Postgraduate College, Dalian Medical University, Dalian 116044, China
- Postgraduate College, China Medical University, Shenyang 110122, China
| | - Xingshun Qi
- Department of Gastroenterology, General Hospital of Northern Theater Command, Shenyang 110840, China
- Postgraduate College, Dalian Medical University, Dalian 116044, China
- Postgraduate College, China Medical University, Shenyang 110122, China
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15
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Zhang H, Shen H, Zhou L, Xie L, Kong D, Wang H. Mucosal-Associated Invariant T Cells in the Digestive System: Defender or Destroyer? Cell Mol Gastroenterol Hepatol 2023; 15:809-819. [PMID: 36584816 PMCID: PMC9971522 DOI: 10.1016/j.jcmgh.2022.12.014] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/09/2022] [Revised: 12/22/2022] [Accepted: 12/22/2022] [Indexed: 01/01/2023]
Abstract
Mucosal-associated invariant T (MAIT) cells are a subset of innate T lymphocytes that express the semi-invariant T cell receptor and recognize riboflavin metabolites via the major histocompatibility complex class I-related protein. Given the abundance of MAIT cells in the human body, their role in human diseases has been increasingly studied in recent years. MAIT cells may serve as targets for clinical therapy. Specifically, this review discusses how MAIT cells are altered in gastric, esophageal, intestinal, and hepatobiliary diseases and describes their protective or pathogenic roles. A greater understanding of MAIT cells will provide a more favorable therapeutic approach for digestive diseases in the clinical field.
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Affiliation(s)
- Hejiao Zhang
- Department of Gastroenterology, the First Affiliated Hospital of Anhui Medical University, Hefei, China
| | - Haiyuan Shen
- Department of Oncology, the First Affiliated Hospital of Anhui Medical University, Hefei, China; Inflammation and Immune Mediated Diseases Laboratory of Anhui Province, Anhui Medical University, Hefei, China
| | - Liangliang Zhou
- Department of Oncology, the First Affiliated Hospital of Anhui Medical University, Hefei, China; Inflammation and Immune Mediated Diseases Laboratory of Anhui Province, Anhui Medical University, Hefei, China
| | - Linxi Xie
- School of Basic Medical Science, Anhui Medical University, Hefei, China
| | - Derun Kong
- Department of Gastroenterology, the First Affiliated Hospital of Anhui Medical University, Hefei, China.
| | - Hua Wang
- Department of Oncology, the First Affiliated Hospital of Anhui Medical University, Hefei, China; Inflammation and Immune Mediated Diseases Laboratory of Anhui Province, Anhui Medical University, Hefei, China.
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