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Benoit SL, Maier RJ. d-aspartate, an amino-acid important for human health, supports anaerobic respiration in several Campylobacter species. Res Microbiol 2024; 175:104219. [PMID: 38945250 DOI: 10.1016/j.resmic.2024.104219] [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: 05/10/2024] [Revised: 06/24/2024] [Accepted: 06/25/2024] [Indexed: 07/02/2024]
Abstract
Despite being classified as microaerophilic microorganisms, most Campylobacter species can grow anaerobically, using formate or molecular hydrogen (H2) as electron donors, and various nitrogenous and sulfurous compounds as electron acceptors. Herein, we showed that both l-asparagine (l-Asn) and l-aspartic acid (l-Asp) bolster H2-driven anaerobic growth in several Campylobacter species, whereas the d-enantiomer form of both asparagine (d-Asn) and aspartic acid (d-Asp) only increased anaerobic growth in Campylobacter concisus strain 13826 and Campylobacter ureolyticus strain NCTC10941. A gene annotated as racD encoding for a putative d/l-Asp racemase was identified in the genome of both strains. Disruption of racD in Cc13826 resulted in the inability of the mutant strain to use either d-enantiomer during anaerobic growth. Hence, our results suggest that the racD gene is required for campylobacters to use either d-Asp or d-Asn. The use of d-Asp by various human opportunistic bacterial pathogens, including C. concisus, C. ureolyticus, and also possibly select strains of Campylobacter gracilis, Campylobacter rectus and Campylobacter showae, is significant, because d-Asp is an important signal molecule for both human nervous and neuroendocrine systems. To our knowledge, this is the first report of pathogens scavenging a d-amino acid essential for human health.
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Affiliation(s)
- Stéphane L Benoit
- Department of Microbiology, University of Georgia, Athens, GA, 30602, United States; Center for Metalloenzyme Studies, University of Georgia, Athens, GA, 30602, United States.
| | - Robert J Maier
- Department of Microbiology, University of Georgia, Athens, GA, 30602, United States; Center for Metalloenzyme Studies, University of Georgia, Athens, GA, 30602, United States
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2
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Li C, Shu P, Shi T, Chen Y, Mei P, Zhang Y, Wang Y, Du X, Wang J, Zhang Y, Liu B, Sheng Z, Chan S, Dan Z. Predicting the potential deterioration of Barrett's esophagus based on gut microbiota: a Mendelian randomization analysis. Mamm Genome 2024; 35:399-413. [PMID: 38886201 DOI: 10.1007/s00335-024-10042-7] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/09/2023] [Accepted: 05/14/2024] [Indexed: 06/20/2024]
Abstract
Esophageal adenocarcinoma (EAC) is one of the most malignant tumors in the digestive system. To make thing worse, the scarcity of treatment options is disheartening. However, if detected early, there is a possibility of reversing the condition. Unfortunately, there is still a lack of relevant early screening methods. Considering that Barrett's esophagus (BE), a precursor lesion of EAC, has been confirmed as the only known precursor of EAC. Analyzing which BE cases will progress to EAC and understanding the processes and mechanisms involved is of great significance for early screening of such patients. Considering the significant alterations in the gut microbiota of patients with BE and its potential role in the progression to EAC, this study aims to analyze the relationship between BE, EAC, and GM to identify potential diagnostic biomarkers and therapeutic targets. This study utilized comprehensive statistical data on gut microbiota from a large-scale genome-wide association meta-analysis conducted by the MiBioGen consortium (n = 18,340). Subsequently, we selected a set of single nucleotide polymorphisms (SNPs) that fell below the genome-wide significance threshold (1 × 10-5) as instrumental variables. To investigate the causal relationship between gut microbiota and BE and EAC, we employed various MR analysis methods, including Inverse Variance Weighting (IVW), MR-Egger regression, weighted median (WM), and weighted mean. Additionally, we assessed the level of pleiotropy, heterogeneity, and stability of genetic variations through MR-Egger intercept test, MR-PRESSO, Cochran's Q test, and "leave-one-out" sensitivity analysis. Furthermore, we conducted reverse MR analysis to identify the causal relationships between gut microbiota and BE and EAC. The results from the Inverse Variance-Weighted (IVW) analysis indicate that Alistipes (P = 4.86 × 10-2), Lactobacillus (P = 2.11 × 10-2), Prevotella 7 (P = 4.28 × 10-2), and RuminococcaceaeUCG004 (P = 4.34 × 10-2) are risk factors for Barrett's esophagus (BE), while Flavonifractor (P = 8.81 × 10-3) and RuminococcaceaeUCG004 (P = 4.99 × 10-2) are risk factors for esophageal adenocarcinoma (EAC). On the other hand, certain gut microbiota genera appear to have a protective effect against both BE and EAC. These include Eubacterium (nodatum group) (P = 4.51 × 10-2), Holdemania (P = 1.22 × 10-2), and Lactococcus (P = 3.39 × 10-2) in the BE cohort, as well as Eubacterium (hallii group) (P = 4.07 × 10-2) and Actinomyces (P = 3.62 × 10-3) in the EAC cohort. According to the results of reverse MR analysis, no significant causal effects of BE and EAC on gut microbiota were observed. Furthermore, no significant heterogeneity or pleiotropy was detected in the instrumental variables. We have established a causal relationship between the gut microbiota and BE and EAC. This study holds profound significance for screening BE patients who may be at risk of deterioration, as it can provide them with timely medical interventions to reverse the condition.
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Affiliation(s)
- Conghan Li
- First Clinical Medical College (First Affiliated Hospital), Anhui Medical University, 81 Meishan Road, Hefei, 230032, China
| | - Panyin Shu
- State Key Laboratory of Biotherapy, West China Hospital, Sichuan University, No. 37 Guoxue Lane, Wuhou District, Chengdu, Sichuan Province, 610041, China
| | - Taiyu Shi
- First Clinical Medical College (First Affiliated Hospital), Anhui Medical University, 81 Meishan Road, Hefei, 230032, China
| | - Yuerong Chen
- First Clinical Medical College (First Affiliated Hospital), Anhui Medical University, 81 Meishan Road, Hefei, 230032, China
| | - Ping Mei
- Department of Radiology, Anqing Municipal Hospital, Anqing, Anhui Province, 246000, China
| | - Yizhong Zhang
- College of Anesthesia, Wannan Medical College, No. 22 Wenchang West Road, Yijiang District, Wuhu City, 241002, Anhui, China
| | - Yan Wang
- College of Life Sciences, Anhui Medical University, 81 Meishan Road, Hefei, 230032, China
| | - Xinyan Du
- First Clinical Medical College (First Affiliated Hospital), Anhui Medical University, 81 Meishan Road, Hefei, 230032, China
| | - Jianning Wang
- First Clinical Medical College (First Affiliated Hospital), Anhui Medical University, 81 Meishan Road, Hefei, 230032, China
| | - Yixin Zhang
- First Clinical Medical College (First Affiliated Hospital), Anhui Medical University, 81 Meishan Road, Hefei, 230032, China
| | - Bin Liu
- First Clinical Medical College (First Affiliated Hospital), Anhui Medical University, 81 Meishan Road, Hefei, 230032, China
| | - Zhijin Sheng
- Department of Physical Education, College of Humanistic Medicine, Anhui Medical University, Hefei, Anhui, China.
| | - Shixin Chan
- Department of General Surgery, The First Affiliated Hospital of Anhui Medical University, No. 218, Jixi Road, Shushan District, Hefei, 230032, China.
| | - Zhangyong Dan
- Laboratory of Molecular Biology, Department of Biochemistry, Anhui Medical University, 81 Meishan Road, Hefei, 230032, Anhui, China.
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3
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Iijima K. Etiologic factors for Barrett's esophagus: toward countermeasures in Asia. Expert Rev Gastroenterol Hepatol 2024; 18:407-420. [PMID: 39072626 DOI: 10.1080/17474124.2024.2386367] [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: 05/14/2024] [Accepted: 07/26/2024] [Indexed: 07/30/2024]
Abstract
INTRODUCTION Over the past several decades, Europe and the United States have experienced a rapid increase in esophageal adenocarcinoma. Research and countermeasures against Barrett's esophagus, its precancerous lesion, are progressing. Because esophageal adenocarcinoma has an extremely poor prognosis when diagnosed in an advanced stage, recommendations for early cancer detection have been made based on the various proven etiological factors of Barrett's esophagus and the actual cancer risk of Barrett's esophagus. In recent years, there have been indications of an increase in esophageal adenocarcinoma in Japan, and a similar trend of cancer will occur shortly in other Asian countries. Consequently, Asian countries must implement similar countermeasures against Barrett's esophagus and esophageal adenocarcinoma, referencing the knowledge gained thus far in Europe and the United States. AREAS COVERED This review summarizes the latest findings on the etiologic factors of Barrett's esophagus and discusses the differences between Westerners and Asians. The current status of Barrett's esophagus in Japan and other Asian countries is also summarized. EXPERT OPINION The etiological factors and cancer incidence of Barrett's esophagus in Asia diverge somewhat from those observed in Europe and America. Therefore, it is imperative to implement measures that are tailored to the actual circumstances of Asian people.
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Affiliation(s)
- Katsunori Iijima
- Department of Gastroenterology, Akita University Graduate School of Medicine, Akita, Japan
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4
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Wang G. Advancement of the relationship between esophageal microorganisms and esophageal diseases. GASTROENTEROLOGY & ENDOSCOPY 2024; 2:112-116. [DOI: 10.1016/j.gande.2024.07.001] [Citation(s) in RCA: 1] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 01/03/2025]
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Liu S, Wang S, Zhang N, Li P. The oral microbiome and oral and upper gastrointestinal diseases. J Oral Microbiol 2024; 16:2355823. [PMID: 38835339 PMCID: PMC11149586 DOI: 10.1080/20002297.2024.2355823] [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: 01/16/2024] [Accepted: 05/10/2024] [Indexed: 06/06/2024] Open
Abstract
Background Microbiomes are essential components of the human body, and their populations are substantial. Under normal circumstances, microbiomes coexist harmoniously with the human body, but disturbances in this equilibrium can lead to various diseases. The oral microbiome is involved in the occurrence and development of many oral and gastrointestinal diseases. This review focuses on the relationship between oral microbiomes and oral and upper gastrointestinal diseases, and therapeutic strategies aiming to provide valuable insights for clinical prevention and treatment. Methods To identify relevant studies, we conducted searches in PubMed, Google Scholar, and Web of Science using keywords such as "oral microbiome," "oral flora, " "gastrointestinal disease, " without any date restrictions. Subsequently, the retrieved publications were subject to a narrative review. Results In this review, we found that oral microbiomes are closely related to oral and gastrointestinal diseases such as periodontitis, dental caries, reflux esophagitis, gastritis, and upper gastrointestinal tumors (mainly the malignant ones). Oral samples like saliva and buccal mucosa are not only easy to collect, but also display superior sample stability compared to gastrointestinal tissues. Consequently, analysis of the oral microbiome could potentially serve as an efficient preliminary screening method for high-risk groups before undergoing endoscopic examination. Besides, treatments based on the oral microbiomes could aid early diagnosis and treatment of these diseases. Conclusions Oral microbiomes are essential to oral and gastrointestinal diseases. Therapies centered on the oral microbiomes could facilitate the early detection and management of these conditions.
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Affiliation(s)
- Sifan Liu
- Department of Gastroenterology, Beijing Friendship Hospital, Capital Medical University; State Key Laboratory for Digestive Health; National Clinical Research Center for Digestive Diseases, Beijing, China
| | - Shidong Wang
- Department of Gastroenterology, The Affiliated Hospital of Qingdao University, Qingdao, China
| | - Nan Zhang
- Department of Gastroenterology, Beijing Friendship Hospital, Capital Medical University; State Key Laboratory for Digestive Health; National Clinical Research Center for Digestive Diseases, Beijing, China
| | - Peng Li
- Department of Gastroenterology, Beijing Friendship Hospital, Capital Medical University; State Key Laboratory for Digestive Health; National Clinical Research Center for Digestive Diseases, Beijing, China
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Mager LF, Krause T, McCoy KD. Interaction of microbiota, mucosal malignancies, and immunotherapy-Mechanistic insights. Mucosal Immunol 2024; 17:402-415. [PMID: 38521413 DOI: 10.1016/j.mucimm.2024.03.007] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/29/2023] [Revised: 03/09/2024] [Accepted: 03/17/2024] [Indexed: 03/25/2024]
Abstract
The microbiome has emerged as a crucial modulator of host-immune interactions and clearly impacts tumor development and therapy efficacy. The microbiome is a double-edged sword in cancer development and therapy as both pro-tumorigenic and anti-tumorigenic bacterial taxa have been identified. The staggering number of association-based studies in various tumor types has led to an enormous amount of data that makes it difficult to identify bacteria that promote tumor development or modulate therapy efficacy from bystander bacteria. Here we aim to comprehensively summarize the current knowledge of microbiome-host immunity interactions and cancer therapy in various mucosal tissues to find commonalities and thus identify potential functionally relevant bacterial taxa. Moreover, we also review recent studies identifying specific bacteria and mechanisms through which the microbiome modulates cancer development and therapy efficacy.
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Affiliation(s)
- Lukas F Mager
- Department of Physiology and Pharmacology, Snyder Institute for Chronic Diseases, Cumming School of Medicine, University of Calgary, Calgary, Canada; Department of Internal Medicine I, Faculty of Medicine, University of Tübingen, Germany; M3 Research Center for Malignom, Metabolome and Microbiome, Faculty of Medicine University Tübingen, Germany
| | - Tim Krause
- Department of Internal Medicine I, Faculty of Medicine, University of Tübingen, Germany; M3 Research Center for Malignom, Metabolome and Microbiome, Faculty of Medicine University Tübingen, Germany
| | - Kathy D McCoy
- Department of Physiology and Pharmacology, Snyder Institute for Chronic Diseases, Cumming School of Medicine, University of Calgary, Calgary, Canada.
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Zhang R, Qin X, Liu Y. Exploration of the intestinal flora to reveal the important contribution of Radix Astragali to Huangqi Jianzhong Tang in treating chronic atrophic gastritis rats. J Pharm Biomed Anal 2024; 242:116067. [PMID: 38417324 DOI: 10.1016/j.jpba.2024.116067] [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: 11/27/2023] [Revised: 02/20/2024] [Accepted: 02/20/2024] [Indexed: 03/01/2024]
Abstract
Radix Astragali (Huangqi in Chinese, HQ) is a commonly used Chinese herbal medicine for thousands of years. In this study, A classic prescription Huangqi Jianzhong tang (HQJZ) was selected to evaluate the important effect of HQ on rats with chronic atrophic gastritis (CAG) from the perspective of intestinal flora in cecal contents samples. Traditional pharmacological indicators, including weight change, pathological examination and biochemical indicators showed that HQ exerted favorable contribution to HQJZ against CAG, where the efficiencies of HQ and HQJZ were better than HY (HQJZ prepared without HQ). An accurate strategy was adopted to screen out the differential metabolites in the metabolomis analysis of intestinal flora in cecal contents samples based on the optimal screening factors, including VIP (importance of variables in projection), FC (fold change), AUROC (area under the receiver operating characteristic curve) and -ln(p-value), which were evaluated based on their interpreting, grouping, and predicting abilities of the performed orthogonal partial least-squares-discriminate analysis (OPLS-DA) models. Ten altered differential metabolites were obtained and associated with the intestinal flora, which HQ exerted the important metabolic contributions to HQJZ. The efficacy on the diversity of intestinal flora and their correlations with the altered metabolites further showed the important role of HQ in HQJZ composition. This work provided valuable approach for looking for potential biomarkers associated with metabolomics research with more accuracy, and provided new insights into the mechanisms to explain the efficacy of HQ contributing to HQJZ formula.
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Affiliation(s)
- Ruonan Zhang
- Modern Research Center for Traditional Chinese Medicine, the Key Laboratory of Chemical Biology and Molecular Engineering of Ministry of Education, Shanxi University, No. 92, Wucheng Road, Taiyuan, Shanxi 030006, PR China; Key Laboratory of Effective Substances Research and Utilization in TCM of Shanxi Province, No. 92, Wucheng Road, Taiyuan, Shanxi 030006, PR China
| | - Xuemei Qin
- Modern Research Center for Traditional Chinese Medicine, the Key Laboratory of Chemical Biology and Molecular Engineering of Ministry of Education, Shanxi University, No. 92, Wucheng Road, Taiyuan, Shanxi 030006, PR China; Key Laboratory of Effective Substances Research and Utilization in TCM of Shanxi Province, No. 92, Wucheng Road, Taiyuan, Shanxi 030006, PR China.
| | - Yuetao Liu
- Modern Research Center for Traditional Chinese Medicine, the Key Laboratory of Chemical Biology and Molecular Engineering of Ministry of Education, Shanxi University, No. 92, Wucheng Road, Taiyuan, Shanxi 030006, PR China; Key Laboratory of Effective Substances Research and Utilization in TCM of Shanxi Province, No. 92, Wucheng Road, Taiyuan, Shanxi 030006, PR China.
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8
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Strzelec B, Chmielewski PP, Kielan W. Esophageal cancer: current status and new insights from inflammatory markers - a brief review. POLISH JOURNAL OF SURGERY 2024; 96:83-87. [PMID: 38940245 DOI: 10.5604/01.3001.0054.4523] [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] [Indexed: 06/29/2024]
Abstract
Esophageal cancer (EC) poses a significant challenge to the healthcare system due to its profound impact on cancer-related morbidity and mortality worldwide. This malignancy ranks among the most arduous conditions confronting the surgeon. EC arises from a complex interplay of genetic predispositions and environmental factors. While the incidence of esophageal adenocarcinoma (EAC) is on the rise in the West, esophageal squamous cell carcinoma (ESCC) remains prevalent in the East. Chronic inflammation plays a pivotal role in the initiation and progression of EC. Accordingly, serum inflammatory markers, growth factors, and cytokines have been shown to be clinically useful. Thus, evaluating serum cytokine levels for EC prediction is a safe and feasible screening method. Given the aggressive nature and poor prognosis of the disease, innovative approaches to diagnosis, prognosis, and management of EC are indispensable. This review discusses the major risk factors and the current landscape of EC, with a specific focus on the potential contributions of new inflammatory markers to enhance disease management and improve patient outcomes.
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Affiliation(s)
- Bartłomiej Strzelec
- 2nd Department of General and Oncological Surgery, Wroclaw Medical University, Wroclaw, Poland
| | - Piotr Paweł Chmielewski
- Division of Anatomy, Department of Human Morphology and Embryology, Faculty of Medicine, Wroclaw Medical University, Wroclaw, Poland
| | - Wojciech Kielan
- 2nd Department of General Surgery and Surgical Oncology, Medical University Hospital, Wroclaw, Poland
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9
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Luk CYM, Lee SA, Naidovski N, Liu F, Tay ACY, Wang L, Riordan S, Zhang L. Investigation of Campylobacter concisus gastric epithelial pathogenicity using AGS cells. Front Microbiol 2024; 14:1289549. [PMID: 38274743 PMCID: PMC10808343 DOI: 10.3389/fmicb.2023.1289549] [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: 09/06/2023] [Accepted: 12/19/2023] [Indexed: 01/27/2024] Open
Abstract
Campylobacter concisus is an oral bacterium. Recent studies suggest that C. concisus may be involved in human gastric diseases. The mechanisms, however, by which C. concisus causes human gastric diseases have not been investigated. Here we examined the gastric epithelial pathogenicity of C. concisus using a cell culture model. Six C. concisus strains and the human gastric epithelial cell line AGS cells were used. IL-8 produced by AGS cells after incubation with C. concisus was measured using enzyme-linked immunosorbent assay (ELISA), and AGS cell apoptosis was determined by caspase 3/7 activities. The effects of C. concisus on actin arrangement in AGS cells was determined using fluorescence staining. The effects of C. concisus on global gene expression in AGS cells was determined by transcriptomic analysis and quantitative real-time PCR (qRT-PCR). The role of the upregulated CYP1A1 gene in gastric cancer survival was assessed using the Kaplan-Meier method. C. concisus induced production of IL-8 by AGS cells with strain variation. Significantly increased caspase 3/7 activities were observed in AGS cells incubated with C. concisus strains when compared to AGS cells without bacteria. C. concisus induced actin re-arrangement in AGS cells. C. concisus upregulated 30 genes in AGS cells and the upregulation of CYP1A1 gene was confirmed by qRT-PCR. The Kaplan-Meier analysis showed that upregulation of CYP1A1 gene is associated with worse survival in gastric cancer patients. Our findings suggest that C. concisus may play a role in gastric inflammation and the progression of gastric cancer. Further investigation in clinical studies is warranted.
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Affiliation(s)
- Christopher Yau Man Luk
- School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, NSW, Australia
| | - Seul A. Lee
- School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, NSW, Australia
| | - Nicholas Naidovski
- School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, NSW, Australia
| | - Fang Liu
- School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, NSW, Australia
| | - Alfred Chin Yen Tay
- Helicobacter Research Laboratory, School of Pathology and Laboratory Medicine, Marshall Centre for Infectious Diseases Research and Training, University of Western Australia, Perth, WA, Australia
| | - Liang Wang
- Laboratory Medicine, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, Guangdong, China
- The Center for Precision Health, School of Medical and Health Sciences, Edith Cowan University, Perth, WA, Australia
- Department of Medical Informatics, School of Medical Informatics and Engineering, Xuzhou Medical University, Xuzhou, Jiangsu, China
| | - Stephen Riordan
- Gastrointestinal and Liver Unit, Prince of Wales Hospital, University of New South Wales, Sydney, NSW, Australia
| | - Li Zhang
- School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, NSW, Australia
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Co EL, Hameed M, Sebastian SA, Garg T, Sudan S, Bheemisetty N, Mohan B. Narrative Review of Probiotic Use on the Recovery of Postoperative Patients with Esophageal Cancer. Curr Nutr Rep 2023; 12:635-642. [PMID: 37605086 DOI: 10.1007/s13668-023-00490-z] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 08/08/2023] [Indexed: 08/23/2023]
Abstract
PURPOSE OF REVIEW This narrative review discusses the significance of probiotic therapy in the postoperative care of patients with esophageal cancer and its role as an adjunct therapy to other treatment modalities for esophageal cancer. RECENT FINDINGS As such, there is an emerging need to address any malnutrition and gastrointestinal problems occurring in these patients which tend to have a strong negative impact on their prognosis. Probiotic effects on esophageal cancer biomarkers suggest that there is a positive correlation between these two factors. However, the beneficial effects remain controversial and warrant further investigation. Probiotics, now being widely utilized as postoperative therapy in some carcinomas of the gastrointestinal tract such as gastric cancer and colorectal cancer, have been shown in some clinical studies to positively impact the nutritional status of patients with esophageal cancer. Postoperative care among patients suffering from esophageal cancer is a very crucial aspect in the survival of these patients.
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Affiliation(s)
- Edzel Lorraine Co
- University of Santo Tomas Faculty of Medicine and Surgery, Manila, Philippines
| | - Maha Hameed
- Department of Internal Medicine, Florida State University/Sarasota Memorial Hospital, 1700 S Tamiami Trial, Sarasota, FL, 34239, USA.
| | | | - Tulika Garg
- Government Medical College and Hospital, Chandigarh, India
| | | | | | - Babu Mohan
- Department of Gastroenterology, University of Utah School of Medicine, Salt Lake City, UT, USA
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Benoit SL, Maier RJ. The Campylobacter concisus BisA protein plays a dual role: oxide-dependent anaerobic respiration and periplasmic methionine sulfoxide repair. mBio 2023; 14:e0147523. [PMID: 37607056 PMCID: PMC10653797 DOI: 10.1128/mbio.01475-23] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/09/2023] [Accepted: 06/26/2023] [Indexed: 08/24/2023] Open
Abstract
IMPORTANCE Campylobacter concisus is an excellent model organism to study respiration diversity, including anaerobic respiration of physiologically relevant N-/S-oxides compounds, such as biotin sulfoxide, dimethyl sulfoxide, methionine sulfoxide (MetO), nicotinamide N-oxide, and trimethylamine N-oxide. All C. concisus strains harbor at least two, often three, and up to five genes encoding for putative periplasmic Mo/W-bisPGD-containing N-/S-oxide reductases. The respective role (substrate specificity) of each enzyme was studied using a mutagenesis approach. One of the N/SOR enzymes, annotated as "BisA", was found to be essential for anaerobic respiration of both N- and S-oxides. Additional phenotypes associated with disruption of the bisA gene included increased sensitivity toward oxidative stress and elongated cell morphology. Furthermore, a biochemical approach confirmed that BisA can repair protein-bound MetO residues. Hence, we propose that BisA plays a role as a periplasmic methionine sulfoxide reductase. This is the first report of a Mo/W-bisPGD-enzyme supporting both N- or S-oxide respiration and protein-bound MetO repair in a pathogen.
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Affiliation(s)
- Stéphane L. Benoit
- Department of Microbiology, University of Georgia, Athens, Georgia, USA
- Center for Metalloenzyme Studies, University of Georgia, Athens, Georgia, USA
| | - Robert J. Maier
- Department of Microbiology, University of Georgia, Athens, Georgia, USA
- Center for Metalloenzyme Studies, University of Georgia, Athens, Georgia, USA
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12
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Liu H, Huang Y, Huang M, Wang M, Ming Y, Chen W, Chen Y, Tang Z, Jia B. From nitrate to NO: potential effects of nitrate-reducing bacteria on systemic health and disease. Eur J Med Res 2023; 28:425. [PMID: 37821966 PMCID: PMC10566198 DOI: 10.1186/s40001-023-01413-y] [Citation(s) in RCA: 13] [Impact Index Per Article: 6.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/19/2023] [Accepted: 09/29/2023] [Indexed: 10/13/2023] Open
Abstract
Current research has described improving multisystem disease and organ function through dietary nitrate (DN) supplementation. They have provided some evidence that these floras with nitrate (NO3-) reductase are mediators of the underlying mechanism. Symbiotic bacteria with nitrate reductase activity (NRA) are found in the human digestive tract, including the mouth, esophagus and gastrointestinal tract (GT). Nitrate in food can be converted to nitrite under the tongue or in the stomach by these symbiotic bacteria. Then, nitrite is transformed to nitric oxide (NO) by non-enzymatic synthesis. NO is currently recognized as a potent bioactive agent with biological activities, such as vasodilation, regulation of cardiomyocyte function, neurotransmission, suppression of platelet agglutination, and prevention of vascular smooth muscle cell proliferation. NO also can be produced through the conventional L-arginine-NO synthase (L-NOS) pathway, whereas endogenous NO production by L-arginine is inhibited under hypoxia-ischemia or disease conditions. In contrast, exogenous NO3-/NO2-/NO activity is enhanced and becomes a practical supplemental pathway for NO in the body, playing an essential role in various physiological activities. Moreover, many diseases (such as metabolic or geriatric diseases) are primarily associated with disorders of endogenous NO synthesis, and NO generation from the exogenous NO3-/NO2-/NO route can partially alleviate the disease progression. The imbalance of NO in the body may be one of the potential mechanisms of disease development. Therefore, the impact of these floras with nitrate reductase on host systemic health through exogenous NO3-/NO2-/NO pathway production of NO or direct regulation of floras ecological balance is essential (e.g., regulation of body homeostasis, amelioration of diseases, etc.). This review summarizes the bacteria with nitrate reductase in humans, emphasizing the relationship between the metabolic processes of this microflora and host systemic health and disease. The potential effects of nitrate reduction bacteria on human health and disease were also highlighted in disease models from different human systems, including digestive, cardiovascular, endocrine, nervous, respiratory, and urinary systems, providing innovative ideas for future disease diagnosis and treatment based on nitrate reduction bacteria.
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Affiliation(s)
- Hongyu Liu
- Department of Oral Surgery, School of Stomatology, Southern Medical University, Guangzhou, China
| | - Yisheng Huang
- Department of Oral Surgery, School of Stomatology, Southern Medical University, Guangzhou, China
| | - Mingshu Huang
- Department of Oral Surgery, School of Stomatology, Southern Medical University, Guangzhou, China
| | - Min Wang
- Department of Oral Surgery, School of Stomatology, Southern Medical University, Guangzhou, China
| | - Yue Ming
- Department of Oral Surgery, School of Stomatology, Southern Medical University, Guangzhou, China
| | - Weixing Chen
- Department of Oral Surgery, School of Stomatology, Southern Medical University, Guangzhou, China
| | - Yuanxin Chen
- Department of Oral Surgery, School of Stomatology, Southern Medical University, Guangzhou, China
| | - Zhengming Tang
- Department of Oral Surgery, School of Stomatology, Southern Medical University, Guangzhou, China
| | - Bo Jia
- Department of Oral Surgery, School of Stomatology, Southern Medical University, Guangzhou, China.
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13
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Kato I, Minkevitch J, Sun J. Oncogenic potential of Campylobacter infection in the gastrointestinal tract: narrative review. Scand J Gastroenterol 2023; 58:1453-1465. [PMID: 37366241 DOI: 10.1080/00365521.2023.2228954] [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: 03/13/2023] [Revised: 05/26/2023] [Accepted: 06/16/2023] [Indexed: 06/28/2023]
Abstract
BACKGROUND Campylobacter jejuni is the leading cause of zoonotic gastroenteritis. The other emerging group of Campylobacters spp. are part of human oral commensal, represented by C. concisus (CC), which has been recently linked to non-oral conditions. Although long-term gastrointestinal (GI) complications from these two groups of Campylobacters have been previously reviewed individually, overall impact of Campylobacter infection on GI carcinogenesis and their inflammatory precursor lesions has not been assessed collectively. AIMS To evaluate the available evidence concerning the association between Campylobacter infection/colonization and inflammatory bowel disease (IBD), reflux esophagitis/metaplasia colorectal cancer (CRC) and esophageal cancer (EC). METHODS We performed a comprehensive literature search of PubMed for relevant original publications and systematic reviews/meta-analyses of epidemiological and clinical studies. In addition, we gathered additional information concerning microbiological data, animal models and mechanistic data from in vitro studies. RESULTS Both retrospective and prospective studies on IBD showed relatively consistent increased risk associated with Campylobacter infection. Despite lack of supporting prospective studies, retrospective studies based on tissue/fecal microbiome revealed consistent enrichment of Campylobacter in CRC samples. Studies on EC precursor lesions (esophagitis and metaplasia) were generally supportive for the association with Campylobacter, while inconsistent observations on EC. Studies on both IBD and EC precursors suggested the predominant role of CC, but studies on CRC were not informative of species. CONCLUSIONS There is sufficient evidence calling for concerted effort in unveiling direct and indirect connection of this organism to colorectal and esophageal cancer in humans.
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Affiliation(s)
- Ikuko Kato
- Department of Oncology and Pathology, Wayne State University School of Medicine, Detroit, MI, USA
| | - Julia Minkevitch
- Rosalind Franklin University of Medicine and Science, Chicago, IL, USA
| | - Jun Sun
- Department of Microbiology/Immunology, University of Illinois at Chicago (UIC), Chicago, IL, USA
- UIC Cancer Center, Chicago, IL, USA
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14
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Gilroy R, Adam ME, Kumar B, Pallen MJ. An initial genomic blueprint of the healthy human oesophageal microbiome. Access Microbiol 2023; 5:acmi000558.v3. [PMID: 37424544 PMCID: PMC10323806 DOI: 10.1099/acmi.0.000558.v3] [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: 01/09/2023] [Accepted: 05/15/2023] [Indexed: 07/11/2023] Open
Abstract
Background The oesophageal microbiome is thought to contribute to the pathogenesis of oesophageal cancer. However, investigations using culture and molecular barcodes have provided only a low-resolution view of this important microbial community. We therefore explored the potential of culturomics and metagenomic binning to generate a catalogue of reference genomes from the healthy human oesophageal microbiome, alongside a comparison set from saliva. Results Twenty-two distinct colonial morphotypes from healthy oesophageal samples were genome-sequenced. These fell into twelve species clusters, eleven of which represented previously defined species. Two isolates belonged to a novel species, which we have named Rothia gullae. We performed metagenomic binning of reads generated from UK samples from this study alongside reads generated from Australian samples in a recent study. Metagenomic binning generated 136 medium or high-quality metagenome-assembled genomes (MAGs). MAGs were assigned to 56 species clusters, eight representing novel Candidatus species, which we have named Ca. Granulicatella gullae, Ca. Streptococcus gullae, Ca. Nanosynbacter quadramensis, Ca. Nanosynbacter gullae, Ca. Nanosynbacter colneyensis, Ca. Nanosynbacter norwichensis, Ca. Nanosynococcus oralis and Ca. Haemophilus gullae. Five of these novel species belong to the recently described phylum Patescibacteria . Although members of the Patescibacteria are known to inhabit the oral cavity, this is the first report of their presence in the oesophagus. Eighteen of the metagenomic species were, until recently, identified only by hard-to-remember alphanumeric placeholder designations. Here we illustrate the utility of a set of recently published arbitrary Latinate species names in providing user-friendly taxonomic labels for microbiome analyses.Our non-redundant species catalogue contained 63 species derived from cultured isolates or MAGs. Mapping revealed that these species account for around half of the sequences in the oesophageal and saliva metagenomes. Although no species was present in all oesophageal samples, 60 species occurred in at least one oesophageal metagenome from either study, with 50 identified in both cohorts. Conclusions Recovery of genomes and discovery of new species represents an important step forward in our understanding of the oesophageal microbiome. The genes and genomes that we have released into the public domain will provide a base line for future comparative, mechanistic and intervention studies.
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Affiliation(s)
- Rachel Gilroy
- Quadram Institute Bioscience, Norwich Research Park, Norwich, UK
| | - Mina E. Adam
- Norfolk & Norwich University Hospitals NHS Foundation Trust, Norwich, UK
- School of Veterinary Medicine, University of Surrey, Guildford, Surrey, UK
| | - Bhaskar Kumar
- Norfolk & Norwich University Hospitals NHS Foundation Trust, Norwich, UK
- School of Veterinary Medicine, University of Surrey, Guildford, Surrey, UK
| | - Mark J. Pallen
- Quadram Institute Bioscience, Norwich Research Park, Norwich, UK
- School of Veterinary Medicine, University of Surrey, Guildford, Surrey, UK
- University of East Anglia, Norwich Research Park, Norwich, UK
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15
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Zaramella A, Arcidiacono D, Nucci D, Fabris F, Benna C, Pucciarelli S, Fassan M, Fantin A, De Re V, Cannizzaro R, Realdon S. Resident Esophageal Microbiota Dysbiosis Correlates with Cancer Risk in Barrett's Esophagus Patients and Is Linked to Low Adherence to WCRF/AICR Lifestyle Recommendations. Nutrients 2023; 15:2885. [PMID: 37447211 DOI: 10.3390/nu15132885] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/30/2023] [Revised: 06/19/2023] [Accepted: 06/20/2023] [Indexed: 07/15/2023] Open
Abstract
Esophageal adenocarcinoma (EAC) is the consequence of longstanding gastroesophageal reflux, which leads to inflammation and could cause Barrett's esophagus (BE), the main risk factor for EAC development. The 5 year survival rate of EAC is poor since the diagnosis occurs at the late stage of the disease. To improve patient management, a better comprehension of the mechanism undergoing the evolution through to adenocarcinoma is needed. Within this scenario, the resident microbiome investigation was studied. This study aimed to explore the esophageal microbial profile in patients affected by non-dysplastic BE, low- and high-grade dysplastic BE, and EAC to identify parameters characterizing cancer progression and to develop a score suitable for clinical practice to stratify cancer risk. The microbiota was investigated through the 16S rRNA gene sequencing of esophageal biopsies. The microbial composition was evaluated at each different taxonomic level along the disease progression. To further investigate bacteria potentially associated with cancer development, non-dysplastic and dysplastic/cancer patients were compared. The presence of the six significant microbial features with multivariate analysis was used to develop a multiparametric score (Resident Esophageal Microbial Dysbiosis Test) to predict the risk of progression toward EAC. Finally, the diagnostic ability of the test and its discrimination threshold for its ability to identify dysplastic/cancer patients were demonstrated. Since EAC has been related to obesity, the relationship between these microbial parameters and patients' diet/lifestyle habits was also investigated. Developing microbiome-based risk prediction models for esophageal adenocarcinoma onset could open new research avenues, demonstrating that the resident microbiome may be a valid cancer risk biomarker.
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Affiliation(s)
- Alice Zaramella
- Department of Surgery, Oncology and Gastroenterology (DiSCOG), University of Padua, Via Giustiniani 2, 35128 Padua, Italy
- Gastroenterology Unit, Veneto Institute of Oncology IOV-IRCCS, Via Gattamelata 64, 35128 Padua, Italy
| | - Diletta Arcidiacono
- Gastroenterology Unit, Veneto Institute of Oncology IOV-IRCCS, Via Gattamelata 64, 35128 Padua, Italy
| | - Daniele Nucci
- Dietetics and Clinical Nutrition Unit, Veneto Institute of Oncology IOV-IRCCS, Via Gattamelata 64, 35128 Padua, Italy
| | - Federico Fabris
- Department of Biomedical Sciences, University of Padua, Viale Colombo 3, 35121 Padua, Italy
| | - Clara Benna
- Department of Surgery, Oncology and Gastroenterology (DiSCOG), University of Padua, Via Giustiniani 2, 35128 Padua, Italy
| | - Salvatore Pucciarelli
- Department of Surgery, Oncology and Gastroenterology (DiSCOG), University of Padua, Via Giustiniani 2, 35128 Padua, Italy
| | - Matteo Fassan
- Department of Medicine (DIMED), University of Padua, Via Gabelli 61, 35121 Padua, Italy
- Veneto Institute of Oncology IOV-IRCCS, Via Gattamelata 64, 35128 Padua, Italy
| | - Alberto Fantin
- Gastroenterology Unit, Veneto Institute of Oncology IOV-IRCCS, Via Gattamelata 64, 35128 Padua, Italy
| | - Vallì De Re
- Immunopathology and Cancer Biomarkers, Centro di Riferimento Oncologico di Aviano (CRO), National Cancer Institute, IRCCS, 33081 Aviano, Italy
| | - Renato Cannizzaro
- Oncological Gastroenterology, Centro di Riferimento Oncologico di Aviano (CRO), National Cancer Institute, IRCCS, 33081 Aviano, Italy
- Department of Medical, Surgical and Health Sciences, University of Trieste, 34127 Trieste, Italy
| | - Stefano Realdon
- Oncological Gastroenterology, Centro di Riferimento Oncologico di Aviano (CRO), National Cancer Institute, IRCCS, 33081 Aviano, Italy
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16
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Lin Q, Guan SW, Yu HB. Immuno-oncology-microbiome axis of gastrointestinal malignancy. World J Gastrointest Oncol 2023; 15:757-775. [PMID: 37275452 PMCID: PMC10237027 DOI: 10.4251/wjgo.v15.i5.757] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/26/2022] [Revised: 03/15/2023] [Accepted: 04/14/2023] [Indexed: 05/12/2023] Open
Abstract
Research on the relationship between the microbiome and cancer has been controversial for centuries. Recent works have discovered that the intratumor microbiome is an important component of the tumor microenvironment (TME). Intratumor bacteria, the most studied intratumor microbiome, are mainly localized in tumor cells and immune cells. As the largest bacterial reservoir in human body, the gut microbiome may be one of the sources of the intratumor microbiome in gastrointestinal malignancies. An increasing number of studies have shown that the gut and intratumor microbiome play an important role in regulating the immune tone of tumors. Moreover, it has been recently proposed that the gut and intratumor microbiome can influence tumor progression by modulating host metabolism and the immune and immune tone of the TME, which is defined as the immuno-oncology-microbiome (IOM) axis. The proposal of the IOM axis provides a new target for the tumor microbiome and tumor immunity. This review aims to reveal the mechanism and progress of the gut and intratumor microbiome in gastrointestinal malignancies such as esophageal cancer, gastric cancer, liver cancer, colorectal cancer and pancreatic cancer by exploring the IOM axis. Providing new insights into the research related to gastrointestinal malignancies.
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Affiliation(s)
- Quan Lin
- Department of Surgery, Wenzhou Central Hospital, The Dingli Clinical Institute of Wenzhou Medical University, Wenzhou 325000, Zhejiang Province, China
| | - Shi-Wei Guan
- Department of Surgery, Wenzhou Central Hospital, The Dingli Clinical Institute of Wenzhou Medical University, Wenzhou 325000, Zhejiang Province, China
| | - Hai-Bo Yu
- Department of Surgery, Wenzhou Central Hospital, The Dingli Clinical Institute of Wenzhou Medical University, Wenzhou 325000, Zhejiang Province, China
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17
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Moreira C, Figueiredo C, Ferreira RM. The Role of the Microbiota in Esophageal Cancer. Cancers (Basel) 2023; 15:cancers15092576. [PMID: 37174041 PMCID: PMC10177416 DOI: 10.3390/cancers15092576] [Citation(s) in RCA: 7] [Impact Index Per Article: 3.5] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/13/2023] [Revised: 04/28/2023] [Accepted: 04/29/2023] [Indexed: 05/15/2023] Open
Abstract
Esophageal cancer is a major health problem, being the seventh most incidence cancer worldwide. Due to the often-late diagnosis and lack of efficient treatments, the overall 5-year survival is as low as 10%. Therefore, understanding the etiology and the mechanisms that drive the development of this type of cancer could improve the management of patients, increasing the chance of achieving a better clinical outcome. Recently, the microbiome has been studied as a putative etiological factor for esophageal cancer. Nevertheless, the number of studies tackling this issue is low, and the heterogeneity in the study design and data analysis has hindered consistent findings. In this work, we reviewed the current literature on the evaluation of the role of microbiota in the development of esophageal cancer. We analyzed the composition of the normal microbiota and the alterations found in precursor lesions, namely Barrett's esophagus and dysplasia, as well as in esophageal cancer. Additionally, we explored how other environmental factors can modify microbiota and contribute to the development of this neoplasia. Finally, we identify critical aspects to be improved in future studies, with the aim of refining the interpretation of the relationship between the microbiome and esophageal cancer.
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Affiliation(s)
- Clara Moreira
- Instituto de Investigação e Inovação em Saúde, Universidade do Porto (i3S), 4200-135 Porto, Portugal
- Department of Pathology, Faculty of Medicine of the University of Porto, 4200-319 Porto, Portugal
| | - Ceu Figueiredo
- Instituto de Investigação e Inovação em Saúde, Universidade do Porto (i3S), 4200-135 Porto, Portugal
- Department of Pathology, Faculty of Medicine of the University of Porto, 4200-319 Porto, Portugal
- Institute of Molecular Pathology and Immunology of the University of Porto (IPATIMUP), 4200-135 Porto, Portugal
| | - Rui Manuel Ferreira
- Instituto de Investigação e Inovação em Saúde, Universidade do Porto (i3S), 4200-135 Porto, Portugal
- Institute of Molecular Pathology and Immunology of the University of Porto (IPATIMUP), 4200-135 Porto, Portugal
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18
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Cristina Vergara Alvarez S, José Leiva Alaniz M, Victoria Mestre Furlani M, Vazquez F, Mancha Agresti P, Cristina Nally M, Paola Maturano Y. Bioprospecting of the probiotic potential of yeasts isolated from a wine environment. Fungal Genet Biol 2023; 164:103767. [PMID: 36529368 DOI: 10.1016/j.fgb.2022.103767] [Citation(s) in RCA: 11] [Impact Index Per Article: 5.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/02/2022] [Revised: 12/02/2022] [Accepted: 12/10/2022] [Indexed: 12/23/2022]
Abstract
Autochthonous yeasts of oenological origin are adapted to highly stressful and selective environments, which makes them potential candidates for probiotics. The objective of the present study was to explore the probiotic potential of 96 native yeasts of oenological origin, their biosafety, resistance to gastrointestinal tract conditions and adhesion properties. Regarding biosafety, 66 isolates shown negative hemolytic activity, negative urease activity and susceptibility to 3 or more antifungals. After the gastrointestinal resistance test, 15 isolates were selected that showed growth at different temperatures, tolerance to low pH and the presence of bile salts in in vitro tests. In general, survival after simulated conditions of the gastrointestinal tract was high and more restrictive was the duodenal. The results of the adhesion properties showed highly variable hydrophobicity and a high percentage of autoaggregation at 24 h. The maximum production of biofilm was detected in the Pichia strains. Of a total of 96 yeast strains, 15 non-Saccharomyces yeasts presented suitable properties as probiotic candidates. The native winemaking strains performed better than the reference probiotic strain, Saccharomyces cerevisiae var. boulardii CNCM I-745, which reaffirms that these strains are promising probiotic candidates and further studies are necessary to confirm their probiosis.
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Affiliation(s)
- Silvia Cristina Vergara Alvarez
- Instituto de Biotecnología, Universidad Nacional de San Juan, Av. San Martín 1109 (O), San Juan 5400, Argentina; Consejo Nacional de Investigaciones Científicas y Tecnológicas, Godoy Cruz 2290 Ciudad Autónoma de Buenos Aires C1425FQB, Argentina.
| | - María José Leiva Alaniz
- Instituto de Biotecnología, Universidad Nacional de San Juan, Av. San Martín 1109 (O), San Juan 5400, Argentina; Consejo Nacional de Investigaciones Científicas y Tecnológicas, Godoy Cruz 2290 Ciudad Autónoma de Buenos Aires C1425FQB, Argentina.
| | - María Victoria Mestre Furlani
- Instituto de Biotecnología, Universidad Nacional de San Juan, Av. San Martín 1109 (O), San Juan 5400, Argentina; Consejo Nacional de Investigaciones Científicas y Tecnológicas, Godoy Cruz 2290 Ciudad Autónoma de Buenos Aires C1425FQB, Argentina
| | - Fabio Vazquez
- Instituto de Biotecnología, Universidad Nacional de San Juan, Av. San Martín 1109 (O), San Juan 5400, Argentina
| | - Pamela Mancha Agresti
- CEFET Centro Federal de Educação Tecnológica, Av. Amazonas, 5253 Belo Horizonte, Mina Gerais 30421-169, Brasil
| | - María Cristina Nally
- Instituto de Biotecnología, Universidad Nacional de San Juan, Av. San Martín 1109 (O), San Juan 5400, Argentina; Consejo Nacional de Investigaciones Científicas y Tecnológicas, Godoy Cruz 2290 Ciudad Autónoma de Buenos Aires C1425FQB, Argentina
| | - Yolanda Paola Maturano
- Instituto de Biotecnología, Universidad Nacional de San Juan, Av. San Martín 1109 (O), San Juan 5400, Argentina; Consejo Nacional de Investigaciones Científicas y Tecnológicas, Godoy Cruz 2290 Ciudad Autónoma de Buenos Aires C1425FQB, Argentina
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19
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Liu F, Lee SA, Xue J, Riordan SM, Zhang L. Global epidemiology of campylobacteriosis and the impact of COVID-19. Front Cell Infect Microbiol 2022; 12:979055. [PMID: 36519137 PMCID: PMC9742372 DOI: 10.3389/fcimb.2022.979055] [Citation(s) in RCA: 38] [Impact Index Per Article: 12.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/27/2022] [Accepted: 10/21/2022] [Indexed: 11/29/2022] Open
Abstract
Campylobacteriosis is a gastroenteritis caused by pathogenic Campylobacter species and an important topic in public health. Here we review the global epidemiology of campylobacteriosis in the last eight years between 2014-2021, providing comprehensive and updated information on the reported incidence and outbreaks of Campylobacter infections. The government public health website of each of the 195 countries and publications from 2014 to September 2022 in public databases were searched. The reported incidence of campylobacteriosis in pre-COVID-19 years was compared to that during the COVID-19 pandemic in countries where data were available. Czech Republic had the highest reported incidence of campylobacteriosis worldwide (215 per 100,000 in 2019), followed by Australia (146.8 per 100,000 in 2016) and New Zealand (126.1 per 100,000 in 2019). Campylobacter was one of the most common human enteric pathogens in both developed and developing countries. About 90% of cases of campylobacteriosis were caused by Campylobacter jejuni, whereas less than 10% of cases were caused by Campylobacter coli. Other Campylobacter species were also isolated. The reported incidence and case numbers of campylobacteriosis in developed nations have remained steadily high prior to the COVID-19 pandemic, whilst some countries reported an increasing trend such as France and Japan. While outbreaks were more frequently reported in some countries, Campylobacter infections were mainly sporadic cases in most of the developed countries. Campylobacter infection was more common in summer in some but not all countries. Campylobacter infection was more common in males than females. The COVID-19 pandemic has reduced the reported incidence of campylobacteriosis in most countries where 2020 epidemiology data were available. In conclusion, Campylobacter infection remains a global health concern. Increased research and improved strategies are needed for prevention and reduction of Campylobacter infection.
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Affiliation(s)
- Fang Liu
- School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, NSW, Australia
| | - Seul A. Lee
- School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, NSW, Australia
| | - Jessica Xue
- Faculty of Medicine, Monash University, Melbourne, VIC, Australia
| | - Stephen M. Riordan
- Gastrointestinal and Liver Unit, Prince of Wales Hospital, University of New South Wales, Sydney, NSW, Australia
| | - Li Zhang
- School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, NSW, Australia,*Correspondence: Li Zhang,
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20
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Kashyap S, Pal S, Chandan G, Saini V, Chakrabarti S, Saini NK, Mittal A, Thakur VK, Saini AK, Saini RV. Understanding the cross-talk between human microbiota and gastrointestinal cancer for developing potential diagnostic and prognostic biomarkers. Semin Cancer Biol 2022; 86:643-651. [PMID: 33971261 DOI: 10.1016/j.semcancer.2021.04.020] [Citation(s) in RCA: 18] [Impact Index Per Article: 6.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/31/2021] [Revised: 04/19/2021] [Accepted: 04/29/2021] [Indexed: 02/07/2023]
Abstract
The interaction between gut microbes and gastrointestinal (GI) tract carcinogenesis has always attracted researchers' attention to identify therapeutic targets or potential prognostic biomarkers. Various studies have suggested that the microbiota do show inflammation and immune dysregulation, which led to carcinogenesis in GI tract. In this review, we have focused on the role of microbes present in the gut, intestine, or faeces in GI tract cancers, including esophageal cancer, gastric cancer, and colorectal cancer. Herein, we have discussed the importance of the microbes and their metabolites, which could serve as diagnostic biomarkers for cancer detection, especially in the early stage, and prognostic markers. To maximize the effect of the treatment strategies, an accurate evaluation of the prognosis is imperative for clinicians. There is a vast difference in the microbiota profiles within a population and across the populations depending upon age, diet, lifestyle, genetic makeup, use of antibiotics, and environmental factors. Therefore, the diagnostic efficiency of the microbial markers needs to be further validated. A deeper understanding of the GI cancer and the host microbiota is needed to acquire pivotal information about disease status.
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Affiliation(s)
- Sheetal Kashyap
- Department of Biotechnology, MMEC, Maharishi Markandeshwar (Deemed to be University), Mullana-Ambala, 133207, Haryana, India
| | - Soumya Pal
- Department of Biotechnology, MMEC, Maharishi Markandeshwar (Deemed to be University), Mullana-Ambala, 133207, Haryana, India
| | - Gourav Chandan
- Central Research Cell, MM Institute of Medical Sciences & Research, Maharishi Markandeshwar (Deemed to be University), Mullana, 133207, Haryana, India
| | - Vipin Saini
- Maharishi Markandeshwar University, Solan, 173229, Himachal Pradesh, India
| | - Sasanka Chakrabarti
- Central Research Cell, MM Institute of Medical Sciences & Research, Maharishi Markandeshwar (Deemed to be University), Mullana, 133207, Haryana, India
| | - Neeraj K Saini
- Department of Biotechnology, Jawaharlal Nehru University, New Delhi, 110067, India
| | - Amit Mittal
- Central Research Cell, MM Institute of Medical Sciences & Research, Maharishi Markandeshwar (Deemed to be University), Mullana, 133207, Haryana, India
| | - Vijay Kumar Thakur
- Biorefining and Advanced Materials Research Center, Scotland's Rural College (SRUC), Kings Buildings, Edinburgh, EH9 3JG, UK
| | - Adesh K Saini
- Department of Biotechnology, MMEC, Maharishi Markandeshwar (Deemed to be University), Mullana-Ambala, 133207, Haryana, India.
| | - Reena V Saini
- Department of Biotechnology, MMEC, Maharishi Markandeshwar (Deemed to be University), Mullana-Ambala, 133207, Haryana, India.
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21
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Souza RF, Spechler SJ. Mechanisms and pathophysiology of Barrett oesophagus. Nat Rev Gastroenterol Hepatol 2022; 19:605-620. [PMID: 35672395 DOI: 10.1038/s41575-022-00622-w] [Citation(s) in RCA: 18] [Impact Index Per Article: 6.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Accepted: 04/22/2022] [Indexed: 01/10/2023]
Abstract
Barrett oesophagus, in which a metaplastic columnar mucosa that can predispose individuals to cancer development lines a portion of the distal oesophagus, is the only known precursor of oesophageal adenocarcinoma, the incidence of which has increased profoundly over the past several decades. Most evidence suggests that Barrett oesophagus develops from progenitor cells at the oesophagogastric junction that proliferate and undergo epithelial-mesenchymal transition as part of a wound-healing process that replaces oesophageal squamous epithelium damaged by gastroesophageal reflux disease (GERD). GERD also seems to induce reprogramming of key transcription factors in the progenitor cells, resulting in the development of the specialized intestinal metaplasia that is characteristic of Barrett oesophagus, probably through an intermediate step of metaplasia to cardiac mucosa. Genome-wide association studies suggest that patients with GERD who develop Barrett oesophagus might have an inherited predisposition to oesophageal metaplasia and that there is a shared genetic susceptibility to Barrett oesophagus and to several of its risk factors (such as GERD, obesity and cigarette smoking). In this Review, we discuss the mechanisms, pathophysiology, genetic predisposition and cells of origin of Barrett oesophagus, and opine on the clinical implications and future research directions.
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Affiliation(s)
- Rhonda F Souza
- Division of Gastroenterology, Center for Oesophageal Diseases, Baylor University Medical Center, Dallas, TX, USA. .,Center for Oesophageal Research, Baylor Scott & White Research Institute, Dallas, TX, USA.
| | - Stuart J Spechler
- Division of Gastroenterology, Center for Oesophageal Diseases, Baylor University Medical Center, Dallas, TX, USA.,Center for Oesophageal Research, Baylor Scott & White Research Institute, Dallas, TX, USA
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22
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Lin Z, Rao W, Xiang Z, Zeng Q, Liu S, Yu K, Zhou J, Wang J, Chen W, Chen Y, Peng X, Hu Z. Characteristics and interplay of esophageal microbiota in esophageal squamous cell carcinoma. BMC Cancer 2022; 22:696. [PMID: 35739509 PMCID: PMC9229141 DOI: 10.1186/s12885-022-09771-2] [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: 03/17/2022] [Accepted: 06/13/2022] [Indexed: 12/25/2022] Open
Abstract
Background Esophageal microbiota may influence esophageal squamous cell carcinoma (ESCC) pathobiology. Therefore, we investigated the characteristics and interplay of the esophageal microbiota in ESCC. Methods We performed 16S ribosomal RNA sequencing on paired esophageal tumor and tumor-adjacent samples obtained from 120 primarily ESCC patients. Analyses were performed using quantitative insights into microbial 2 (QIIME2) and phylogenetic investigation of communities by reconstruction of unobserved states 2 (PICRUSt2). Species found to be associated with ESCC were validated using quantitative PCR. Results The microbial diversity and composition of ESCC tumor tissues significantly differed from tumor-adjacent tissues; this variation between subjects beta diversity is mainly explained by regions and sampling seasons. A total of 56 taxa were detected with differential abundance between the two groups, such as R. mucilaginosa, P. endodontalis, N. subflava, H. Pylori, A. Parahaemolyticus, and A. Rhizosphaerae. Quantitative PCR confirmed the enrichment of the species P. endodontalis and the reduction of H. Pylori in tumor-adjacent tissues. Compared with tumor tissue, a denser and more complex association network was formed in tumor-adjacent tissue. The above differential taxa, such as H. Pylori, an unclassified species in the genera Sphingomonas, Haemophilus, Phyllobacterium, and Campylobacter, also participated in both co-occurrence networks but played quite different roles. Most of the differentially abundant taxa in tumor-adjacent tissues were negatively associated with the epidermal growth factor receptor (EGFR), erb-b2 receptor tyrosine kinase 2 (ERBB2), erb-b2 receptor tyrosine kinase 4 (ERBB4), and fibroblast growth factor receptor 1 (FGFR1) signaling pathways, and positively associated with the MET proto-oncogene, receptor tyrosine kinase (MET) and phosphatase and tensin homolog (PTEN) signaling pathways in tumors. Conclusion Alterations in the microbial co-occurrence network and functional pathways in ESCC tissues may be involved in carcinogenesis and the maintenance of the local microenvironment for ESCC. Supplementary Information The online version contains supplementary material available at 10.1186/s12885-022-09771-2.
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Affiliation(s)
- Zheng Lin
- Department of Epidemiology and Health Statistics, Fujian Provincial Key Laboratory of Environment Factors and Cancer, School of Public Health, Fujian Medical University, Fuzhou, 350122, China
| | - Wenqing Rao
- Department of Epidemiology and Health Statistics, Fujian Provincial Key Laboratory of Environment Factors and Cancer, School of Public Health, Fujian Medical University, Fuzhou, 350122, China
| | - Zhisheng Xiang
- Department of Epidemiology, Fujian Medical University Cancer Hospital, Fujian Cancer Hospital, Fuzhou, 350014, China
| | - Qiaoyan Zeng
- Department of Epidemiology and Health Statistics, Fujian Provincial Key Laboratory of Environment Factors and Cancer, School of Public Health, Fujian Medical University, Fuzhou, 350122, China
| | - Shuang Liu
- Department of Epidemiology and Health Statistics, Fujian Provincial Key Laboratory of Environment Factors and Cancer, School of Public Health, Fujian Medical University, Fuzhou, 350122, China
| | - Kaili Yu
- Department of Epidemiology and Health Statistics, Fujian Provincial Key Laboratory of Environment Factors and Cancer, School of Public Health, Fujian Medical University, Fuzhou, 350122, China
| | - Jinsong Zhou
- Department of Epidemiology and Health Statistics, Fujian Provincial Key Laboratory of Environment Factors and Cancer, School of Public Health, Fujian Medical University, Fuzhou, 350122, China
| | - Jianwen Wang
- Department of Digestive Endoscopy, Anxi County Hospital, Anxi, 362400, China
| | - Weilin Chen
- Department of Radiation Oncology, Zhangzhou Affiliated Hospital of Fujian Medical University, Zhangzhou, 363000, China
| | - Yuanmei Chen
- Department of Thoracic Surgery, Fujian Medical University Cancer Hospital, Fujian Cancer Hospital, Fuzhou, 350014, China
| | - Xiane Peng
- Department of Epidemiology and Health Statistics, Fujian Provincial Key Laboratory of Environment Factors and Cancer, School of Public Health, Fujian Medical University, Fuzhou, 350122, China.,Key Laboratory of Ministry of Education for Gastrointestinal Cancer, Fujian Medical University, Fuzhou, 350122, China
| | - Zhijian Hu
- Department of Epidemiology and Health Statistics, Fujian Provincial Key Laboratory of Environment Factors and Cancer, School of Public Health, Fujian Medical University, Fuzhou, 350122, China. .,Key Laboratory of Ministry of Education for Gastrointestinal Cancer, Fujian Medical University, Fuzhou, 350122, China.
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23
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Sharma T, Gupta A, Chauhan R, Bhat AA, Nisar S, Hashem S, Akhtar S, Ahmad A, Haris M, Singh M, Uddin S. Cross-talk between the microbiome and chronic inflammation in esophageal cancer: potential driver of oncogenesis. Cancer Metastasis Rev 2022; 41:281-299. [PMID: 35511379 PMCID: PMC9363391 DOI: 10.1007/s10555-022-10026-6] [Citation(s) in RCA: 26] [Impact Index Per Article: 8.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 01/29/2022] [Accepted: 03/12/2022] [Indexed: 12/11/2022]
Abstract
Esophageal cancer (EC) is frequently considered a lethal malignancy and is often identified at a later stage. It is one of the major causes of cancer-related deaths globally. The conventional treatment methods like chemotherapy, radiotherapy, and surgery offer limited efficacy and poor clinical outcome with a less than 25% 5-year survival rate. The poor prognosis of EC persists despite the growth in the development of diagnostic and therapeutic modalities to treat EC. This underlines the need to elucidate the complex molecular mechanisms that drive esophageal oncogenesis. Apart from the role of the tumor microenvironment and its structural and cellular components in tumorigenesis, mounting evidence points towards the involvement of the esophageal microbiome, inflammation, and their cross-talk in promoting esophageal cancer. The current review summarizes recent research that delineates the underlying molecular mechanisms by which the microbiota and inflammation promote the pathophysiology of esophageal cancer, thus unraveling targets for potential therapeutic intervention.
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Affiliation(s)
- Tarang Sharma
- Department of Medical Oncology (Lab), All India Institute of Medical Sciences, New Delhi, India
| | - Ashna Gupta
- Department of Medical Oncology (Lab), All India Institute of Medical Sciences, New Delhi, India
| | - Ravi Chauhan
- Department of Medical Oncology (Lab), All India Institute of Medical Sciences, New Delhi, India
| | - Ajaz A Bhat
- Laboratory of Molecular and Metabolic Imaging, Cancer Research Department, Sidra Medicine, Doha, Qatar
| | - Sabah Nisar
- Laboratory of Molecular and Metabolic Imaging, Cancer Research Department, Sidra Medicine, Doha, Qatar
| | - Sheema Hashem
- Laboratory of Molecular and Metabolic Imaging, Cancer Research Department, Sidra Medicine, Doha, Qatar
| | - Sabah Akhtar
- Translational Research Institute, Academic Health System, Hamad Medical Corporation, Doha, Qatar
| | - Aamir Ahmad
- Translational Research Institute, Academic Health System, Hamad Medical Corporation, Doha, Qatar.,Dermatology Institute, Academic Health System, Hamad Medical Corporation, Doha, Qatar
| | - Mohammad Haris
- Laboratory of Molecular and Metabolic Imaging, Cancer Research Department, Sidra Medicine, Doha, Qatar.,Center for Advanced Metabolic Imaging in Precision Medicine, Department of Radiology, Perelman School of Medicine at the University of Pennsylvania, PA, Philadelphia, USA.,Laboratory Animal Research Center, Qatar University, Doha, Qatar
| | - Mayank Singh
- Department of Medical Oncology (Lab), All India Institute of Medical Sciences, New Delhi, India.
| | - Shahab Uddin
- Translational Research Institute, Academic Health System, Hamad Medical Corporation, Doha, Qatar. .,Dermatology Institute, Academic Health System, Hamad Medical Corporation, Doha, Qatar. .,Laboratory Animal Research Center, Qatar University, Doha, Qatar.
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24
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Hartmann P. Editorial: The Microbiome in Hepatobiliary and Intestinal Disease. Front Physiol 2022; 13:893074. [PMID: 35492588 PMCID: PMC9044070 DOI: 10.3389/fphys.2022.893074] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/09/2022] [Accepted: 03/11/2022] [Indexed: 12/12/2022] Open
Affiliation(s)
- Phillipp Hartmann
- Department of Pediatrics, University of California, San Diego, San Diego, CA, United States
- Division of Gastroenterology, Hepatology and Nutrition, Rady Children’s Hospital San Diego, San Diego, CA, United States
- *Correspondence: Phillipp Hartmann,
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25
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Dan W, Peng L, Yan B, Li Z, Pan F. Human Microbiota in Esophageal Adenocarcinoma: Pathogenesis, Diagnosis, Prognosis and Therapeutic Implications. Front Microbiol 2022; 12:791274. [PMID: 35126331 PMCID: PMC8815000 DOI: 10.3389/fmicb.2021.791274] [Citation(s) in RCA: 11] [Impact Index Per Article: 3.7] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/08/2021] [Accepted: 12/23/2021] [Indexed: 11/29/2022] Open
Abstract
Esophageal adenocarcinoma (EAC) is one of the main subtypes of esophageal cancer. The incidence rate of EAC increased progressively while the 5-year relative survival rates were poor in the past two decades. The mechanism of EAC has been studied extensively in relation to genetic factors, but less so with respect to human microbiota. Currently, researches about the relationship between EAC and the human microbiota is a newly emerging field of study. Herein, we present the current state of knowledge linking human microbiota to esophageal adenocarcinoma and its precursor lesion—gastroesophageal reflux disease and Barrett’s esophagus. There are specific human bacterial alternations in the process of esophageal carcinogenesis. And bacterial dysbiosis plays an important role in the process of esophageal carcinogenesis via inflammation, microbial metabolism and genotoxicity. Based on the human microbiota alternation in the EAC cascade, it provides potential microbiome-based clinical application. This review is focused on novel targets in prevention, diagnosis, prognosis, and therapy for esophageal adenocarcinoma.
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Affiliation(s)
- Wanyue Dan
- Department of Gastroenterology and Hepatology, The First Medical Center, Chinese PLA General Hospital, Beijing, China
- Medical School of Nankai University, Tianjin, China
| | - Lihua Peng
- Department of Gastroenterology and Hepatology, The First Medical Center, Chinese PLA General Hospital, Beijing, China
| | - Bin Yan
- Department of Gastroenterology and Hepatology, The First Medical Center, Chinese PLA General Hospital, Beijing, China
| | - Zhengpeng Li
- Department of Gastroenterology and Hepatology, The First Medical Center, Chinese PLA General Hospital, Beijing, China
| | - Fei Pan
- Department of Gastroenterology and Hepatology, The First Medical Center, Chinese PLA General Hospital, Beijing, China
- *Correspondence: Fei Pan,
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26
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Plat VD, van Rossen TM, Daams F, de Boer NK, de Meij TGJ, Budding AE, Vandenbroucke-Grauls CMJE, van der Peet DL. Esophageal microbiota composition and outcome of esophageal cancer treatment: a systematic review. Dis Esophagus 2021; 35:6425236. [PMID: 34761269 PMCID: PMC9376764 DOI: 10.1093/dote/doab076] [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] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/30/2021] [Revised: 09/24/2021] [Accepted: 10/10/2021] [Indexed: 12/11/2022]
Abstract
BACKGROUND The role of esophageal microbiota in esophageal cancer treatment is gaining renewed interest, largely driven by novel DNA-based microbiota analysis techniques. The aim of this systematic review is to provide an overview of current literature on the possible association between esophageal microbiota and outcome of esophageal cancer treatment, including tumor response to (neo)adjuvant chemo(radio)therapy, short-term surgery-related complications, and long-term oncological outcome. METHODS A systematic review of literature was performed, bibliographic databases were searched and relevant articles were selected by two independent researchers. The Newcastle-Ottawa scale was used to estimate the quality of included studies. RESULTS The search yielded 1303 articles, after selection and cross-referencing, five articles were included for qualitative synthesis and four studies were considered of good quality. Two articles addressed tumor response to neoadjuvant chemotherapy and described a correlation between high intratumoral Fusobacterium nucleatum levels and a poor response. One study assessed surgery-related complications, in which no direct association between esophageal microbiota and occurrence of complications was observed. Three studies described a correlation between shortened survival and high levels of intratumoral F. nucleatum, a low abundance of Proteobacteria and high abundances of Prevotella and Streptococcus species. CONCLUSIONS Current evidence points towards an association between esophageal microbiota and outcome of esophageal cancer treatment and justifies further research. Whether screening of the individual esophageal microbiota can be used to identify and select patients with a predisposition for adverse outcome needs to be further investigated. This could lead to the development of microbiota-based interventions to optimize esophageal microbiota composition, thereby improving outcome of patients with esophageal cancer.
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Affiliation(s)
- Victor D Plat
- Address correspondence to: Mr Victor Dirk Plat, MD, Department of Gastrointestinal Surgery, Amsterdam UMC, VU University Medical Center, De Boelelaan 1117, ZH 7F020, 1081 HV Amsterdam, The Netherlands.
| | - Tessel M van Rossen
- Department of Medical Microbiology and Infection Control, Amsterdam Institute for Infection and Immunity, Amsterdam UMC, VU University Medical Center, Amsterdam, The Netherlands
| | - Freek Daams
- Department of Gastrointestinal Surgery, Amsterdam UMC, VU University Medical Center, Amsterdam, The Netherlands
| | - Nanne K de Boer
- Department of Gastroenterology and Hepatology, Amsterdam Gastroenterology Endocrinology Metabolism (AGEM) Research Institute, Amsterdam UMC, VU University Medical Center Amsterdam, The Netherlands
| | - Tim G J de Meij
- Department of Pediatric Gastroenterology and Hepatology, Amsterdam UMC, VU University Medical Center, Amsterdam, The Netherlands
| | | | - Christina M J E Vandenbroucke-Grauls
- Department of Medical Microbiology and Infection Control, Amsterdam Institute for Infection and Immunity, Amsterdam UMC, VU University Medical Center, Amsterdam, The Netherlands
| | - Donald L van der Peet
- Department of Gastrointestinal Surgery, Amsterdam UMC, VU University Medical Center, Amsterdam, The Netherlands
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27
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Zhou J, Sun S, Luan S, Xiao X, Yang Y, Mao C, Chen L, Zeng X, Zhang Y, Yuan Y. Gut Microbiota for Esophageal Cancer: Role in Carcinogenesis and Clinical Implications. Front Oncol 2021; 11:717242. [PMID: 34733778 PMCID: PMC8558403 DOI: 10.3389/fonc.2021.717242] [Citation(s) in RCA: 16] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/30/2021] [Accepted: 09/24/2021] [Indexed: 02/05/2023] Open
Abstract
Esophageal cancer (EC) is a common malignant tumor of the upper digestive tract. The microbiota in the digestive tract epithelium comprises a large number of microorganisms that adapt to the immune defense and interact with the host to form symbiotic networks, which affect many physiological processes such as metabolism, tissue development, and immune response. Reports indicate that there are microbial compositional changes in patients with EC, which provides an important opportunity to advance clinical applications based on findings on the gut microbiota. For example, microbiota detection can be used as a biomarker for screening and prognosis, and microorganism levels can be adjusted to treat cancer and decrease the adverse effects of treatment. This review aims to provide an outline of the gut microbiota in esophageal neoplasia, including the mechanisms involved in microbiota-related carcinogenesis and the prospect of utilizing the microbiota as EC biomarkers and treatment targets. These findings have important implications for translating the use of gut microbiota in clinical applications.
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Affiliation(s)
- Jianfeng Zhou
- Department of Thoracic Surgery, West China Hospital, Sichuan University, Chengdu, China
| | - Shangwei Sun
- Department of Thoracic Surgery, West China Hospital, Sichuan University, Chengdu, China
| | - Siyuan Luan
- Department of Thoracic Surgery, West China Hospital, Sichuan University, Chengdu, China
| | - Xin Xiao
- Department of Thoracic Surgery, West China Hospital, Sichuan University, Chengdu, China
| | - Yushang Yang
- Department of Thoracic Surgery, West China Hospital, Sichuan University, Chengdu, China
| | - Chengyi Mao
- Department of Thoracic Surgery, West China Hospital, Sichuan University, Chengdu, China
| | - Longqi Chen
- Department of Thoracic Surgery, West China Hospital, Sichuan University, Chengdu, China
| | - Xiaoxi Zeng
- West China Biomedical Big Data Center, West China Hospital, Sichuan University, Chengdu, China
| | - Yonggang Zhang
- Department of Periodical Press, National Clinical Research Center for Geriatrics, West China Hospital, Sichuan University, Chengdu, China.,Nursing Key Laboratory of Sichuan Province, West China Hospital, Sichuan University, Chengdu, China
| | - Yong Yuan
- Department of Thoracic Surgery, West China Hospital, Sichuan University, Chengdu, China
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28
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Flashner S, Yan KS, Nakagawa H. 3D Organoids: An Untapped Platform for Studying Host-Microbiome Interactions in Esophageal Cancers. Microorganisms 2021; 9:2182. [PMID: 34835308 PMCID: PMC8622040 DOI: 10.3390/microorganisms9112182] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/24/2021] [Revised: 10/15/2021] [Accepted: 10/17/2021] [Indexed: 12/12/2022] Open
Abstract
The microbiome is an emerging key co-factor in the development of esophageal cancer, the sixth leading cause of cancer death worldwide. However, there is a paucity of data delineating how the microbiome contributes to the pathobiology of the two histological subtypes of esophageal cancer: esophageal squamous cell carcinoma and esophageal adenocarcinoma. This critical knowledge gap is partially due to inadequate modeling of host-microbiome interactions in the etiology of esophageal cancers. Recent advances have enabled progress in this field. Three dimensional (3D) organoids faithfully recapitulate the structure and function of the normal, preneoplastic, and neoplastic epithelia of the esophagus ex vivo and serve as a platform translatable for applications in precision medicine. Elsewhere in the gastrointestinal (GI) tract, the co-culture of 3D organoids with the bacterial microbiome has fostered insight into the pathogenic role of the microbiome in other GI cancers. Herein, we will summarize our current understanding of the relationship between the microbiome and esophageal cancer, discuss 3D organoid models of esophageal homeostasis, review analogous models of host-microbiome interactions in other GI cancers, and advocate for the application of these models to esophageal cancers. Together, we present a promising, novel approach with the potential to ameliorate the burden of esophageal cancer-related morbidity and mortality via improved prevention and therapeutic interventions.
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Affiliation(s)
- Samuel Flashner
- Herbert Irving Comprehensive Cancer Center, Columbia University Irving Medical Center, New York, NY 10032, USA; (S.F.); (K.S.Y.)
| | - Kelley S. Yan
- Herbert Irving Comprehensive Cancer Center, Columbia University Irving Medical Center, New York, NY 10032, USA; (S.F.); (K.S.Y.)
- Division of Digestive and Liver Diseases, Department of Medicine, Columbia University Irving Medical Center, New York, NY 10032, USA
- Department of Genetics and Development, Columbia University Irving Medical Center, New York, NY 10032, USA
| | - Hiroshi Nakagawa
- Herbert Irving Comprehensive Cancer Center, Columbia University Irving Medical Center, New York, NY 10032, USA; (S.F.); (K.S.Y.)
- Division of Digestive and Liver Diseases, Department of Medicine, Columbia University Irving Medical Center, New York, NY 10032, USA
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29
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Lee SA, Liu F, Yun DY, Riordan SM, Tay ACY, Liu L, Lee CS, Zhang L. Campylobacter concisus upregulates PD-L1 mRNA expression in IFN-γ sensitized intestinal epithelial cells and induces cell death in esophageal epithelial cells. J Oral Microbiol 2021; 13:1978732. [PMID: 34552702 PMCID: PMC8451702 DOI: 10.1080/20002297.2021.1978732] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/08/2021] [Revised: 08/20/2021] [Accepted: 09/06/2021] [Indexed: 12/23/2022] Open
Abstract
Introduction: Campylobacter concisus is an oral bacterium that is associated with inflammatory bowel disease (IBD) and Barrett's esophagus (BE). Programmed cell death ligand-1 (PD-L1) is an immune checkpoint protein that is used by tumor cells for immune evasion and has increased expression in patients with IBD and BE. We examined whether C. concisus upregulates PD-L1 expression in intestinal and esophageal epithelial cells. Methods: Human intestinal epithelial HT-29 cells and esophageal epithelial FLO-1 cells with and without interferon (IFN)-γ sensitization were incubated with C. concisus strains. The level of PD-L1 mRNA was quantified using quantitative real-time PCR. Cytokines were measured using Enzyme-Linked Immunosorbent Assay (ELISA). Apoptosis of HT-29 and FLO-1 cells were measured using caspase 3/7 assay. Results: We found that intestinal epithelial cells with IFN-γ sensitization incubated with C. concisus significantly upregulated PD-L1 expression and significantly increased the production of interleukin (IL)-8. Whereas, PD-L1 expression was significantly inhibited in IFN-γ sensitized FLO-1 cells incubated with C. concisus strains. Furthermore, FLO-1 cells with and without IFN-γ sensitization incubated with C. concisus strains both had significantly higher levels of cell death. Conclusion: C. concisushas the potential to cause damage to both intestinal and esophageal epithelial cells, however, with different pathogenic effects.
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Affiliation(s)
- Seul A Lee
- School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, Australia
| | - Fang Liu
- School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, Australia
| | - Doo Young Yun
- School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, Australia
| | - Stephen M Riordan
- Gastrointestinal and Liver Unit,Prince of Wales Hospital, University of New South Wales, Sydney, Australia
| | - Alfred Chin Yen Tay
- Helicobacter Research Laboratory, Marshall Centre for Infectious Diseases Research and Training, School of Pathology and Laboratory Medicine, University of Western Australia, Perth, Australia
| | - Lu Liu
- School of Medical Sciences, University of New South Wales, Sydney, Australia
| | - Cheok Soon Lee
- School of Medicine, Western Sydney University, Sydney, Australia
- South Western Sydney Clinical School, University of New South Wales, Sydney, Australia
- Central Clinical School, University of Sydney, Sydney, Australia
- Department of Anatomical Pathology, Liverpool Hospital, Sydney, Australia
| | - Li Zhang
- School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, Australia
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30
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Meza-Torres J, Auria E, Dupuy B, Tremblay YDN. Wolf in Sheep's Clothing: Clostridioides difficile Biofilm as a Reservoir for Recurrent Infections. Microorganisms 2021; 9:1922. [PMID: 34576818 PMCID: PMC8470499 DOI: 10.3390/microorganisms9091922] [Citation(s) in RCA: 19] [Impact Index Per Article: 4.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/10/2021] [Revised: 09/06/2021] [Accepted: 09/07/2021] [Indexed: 12/21/2022] Open
Abstract
The microbiota inhabiting the intestinal tract provide several critical functions to its host. Microorganisms found at the mucosal layer form organized three-dimensional structures which are considered to be biofilms. Their development and functions are influenced by host factors, host-microbe interactions, and microbe-microbe interactions. These structures can dictate the health of their host by strengthening the natural defenses of the gut epithelium or cause disease by exacerbating underlying conditions. Biofilm communities can also block the establishment of pathogens and prevent infectious diseases. Although these biofilms are important for colonization resistance, new data provide evidence that gut biofilms can act as a reservoir for pathogens such as Clostridioides difficile. In this review, we will look at the biofilms of the intestinal tract, their contribution to health and disease, and the factors influencing their formation. We will then focus on the factors contributing to biofilm formation in C. difficile, how these biofilms are formed, and their properties. In the last section, we will look at how the gut microbiota and the gut biofilm influence C. difficile biofilm formation, persistence, and transmission.
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Affiliation(s)
- Jazmin Meza-Torres
- Laboratoire Pathogenèse des Bactéries Anaérobies, Institut Pasteur, UMR-CNRS 2001, Université de Paris, 25 rue du Docteur Roux, 75724 Paris, France; (J.M.-T.); (E.A.)
| | - Emile Auria
- Laboratoire Pathogenèse des Bactéries Anaérobies, Institut Pasteur, UMR-CNRS 2001, Université de Paris, 25 rue du Docteur Roux, 75724 Paris, France; (J.M.-T.); (E.A.)
| | - Bruno Dupuy
- Laboratoire Pathogenèse des Bactéries Anaérobies, Institut Pasteur, UMR-CNRS 2001, Université de Paris, 25 rue du Docteur Roux, 75724 Paris, France; (J.M.-T.); (E.A.)
| | - Yannick D. N. Tremblay
- Laboratoire Pathogenèse des Bactéries Anaérobies, Institut Pasteur, UMR-CNRS 2001, Université de Paris, 25 rue du Docteur Roux, 75724 Paris, France; (J.M.-T.); (E.A.)
- Health Sciences Building, Department of Biochemistry, Microbiology and Immunology, University of Saskatchewan, 107 Wiggins Rd, Saskatoon, SK S7N 5E5, Canada
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31
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The oesophageal microbiome and cancer: hope or hype? Trends Microbiol 2021; 30:322-329. [PMID: 34493428 DOI: 10.1016/j.tim.2021.08.007] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/13/2021] [Revised: 08/12/2021] [Accepted: 08/16/2021] [Indexed: 02/08/2023]
Abstract
The human oesophagus is home to a complex microbial community, the oesophageal microbiome. Despite decades of work, we still have only a poor, low-resolution view of this community, which makes it hard to distinguish hope from hype when it comes to assessing links between the oesophageal microbiome and cancer. Here we review the potential importance of this microbiome and discuss new approaches, including culturomics, metagenomics, and recovery of whole-genome sequences, that bring renewed hope for an in-depth characterisation of this community that could deliver translational impact.
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32
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Zhang Z, Curran G, Altinok Dindar D, Wu Y, Wu H, Sharpton T, Zhao L, Lieberman D, Otaki F. Insights Into the Oral Microbiome and Barrett's Esophagus Early Detection: A Narrative Review. Clin Transl Gastroenterol 2021; 12:e00390. [PMID: 34446641 PMCID: PMC8397287 DOI: 10.14309/ctg.0000000000000390] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 01/12/2021] [Accepted: 07/09/2021] [Indexed: 11/29/2022] Open
Abstract
Barrett's esophagus (BE) prevalence has increased steadily over the past several decades and continues to be the only known precursor of esophageal adenocarcinoma. The exact cause of BE is still unknown. Most evidence has linked BE to gastroesophageal reflux disease, which injures squamous esophageal mucosa and can result in the development of columnar epithelium with intestinal metaplasia. However, this relationship is inconsistent-not all patients with severe gastroesophageal reflux disease develop BE. There is increasing evidence that the host microbiome spanning the oral and esophageal environments differs in patients with and without BE. Several studies have documented the oral and esophageal microbiome's composition for BE with inconsistent findings. The scarcity and inconsistency of the literature and the dynamic phenomena of microbiota all warrant further studies to validate the findings and dissect the effects of oral microbiota, which are considered a viable proxy to represent esophageal microbiota by many researchers. This review aims to summarize the variability of the oral and esophageal microbiome in BE by using the example of Streptococcus to discuss the limitations of the current studies and suggest future directions. Further characterization of the sensitivity and specificity of the oral microbiome as a potential risk prediction or prevention marker of BE is critical, which will help develop noninvasive early detection methods for BE, esophageal adenocarcinoma, and other esophageal diseases.
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Affiliation(s)
- Zhenzhen Zhang
- Division of Oncological Sciences, Knight Cancer Institute, Oregon Health & Science University, Portland, Oregon, USA
| | - Grace Curran
- Cancer Early Detection Advanced Research (CEDAR), Knight Cancer Institute, Oregon Health & Science University, Portland, Oregon, USA
| | - Duygu Altinok Dindar
- Cancer Early Detection Advanced Research (CEDAR), Knight Cancer Institute, Oregon Health & Science University, Portland, Oregon, USA
| | - Ying Wu
- Department of Integrative Biomedical and Diagnostic Sciences, School of Dentistry, Oregon Health & Science University, Portland, Oregon, USA
| | - Hui Wu
- Department of Integrative Biomedical and Diagnostic Sciences, School of Dentistry, Oregon Health & Science University, Portland, Oregon, USA
| | - Thomas Sharpton
- Department of Microbiology, Oregon State University, Corvallis, Oregon, USA
- Department of Statistics, Oregon State University, Corvallis, Oregon, USA
| | - Lianmei Zhao
- Research Center, the Fourth Hospital of Hebei Medical University, Shijiazhuang, Hebei Province, China;
| | - David Lieberman
- Division of Gastroenterology & Hepatology, Department of Internal Medicine, Oregon Health Sciences University, Portland, Oregon, USA
| | - Fouad Otaki
- Division of Gastroenterology & Hepatology, Department of Internal Medicine, Oregon Health Sciences University, Portland, Oregon, USA
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33
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Yano Y, Etemadi A, Abnet CC. Microbiome and Cancers of the Esophagus: A Review. Microorganisms 2021; 9:1764. [PMID: 34442842 PMCID: PMC8398938 DOI: 10.3390/microorganisms9081764] [Citation(s) in RCA: 13] [Impact Index Per Article: 3.3] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/12/2021] [Revised: 08/11/2021] [Accepted: 08/14/2021] [Indexed: 01/04/2023] Open
Abstract
Esophageal cancer (EC) is an aggressive malignant disease ranking amongst the leading causes of cancer deaths in the world. The two main histologic subtypes, esophageal squamous cell carcinoma (ESCC) and esophageal adenocarcinoma (EAC), have distinct geographic and temporal patterns and risk factor profiles. Despite decades of research, the factors underlying these geo-temporal patterns are still not fully understood. The human microbiome has recently been implicated in various health conditions and disease, and it is possible that the microbiome may play an important role in the etiology of EC. Although studies of the microbiome and EC are still in their early stages, we review our current understanding of the potential links between ESCC, EAC, and bacterial communities in the oral cavity and esophagus. We also provide a summary of the epidemiology of EC and highlight some key challenges and future directions.
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Affiliation(s)
- Yukiko Yano
- Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892, USA; (A.E.); (C.C.A.)
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34
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Shifera AS, Pockrandt C, Rincon N, Ge Y, Lu J, Varabyou A, Jedlicka AE, Sun K, Scott AL, Eberhart C, Thorne JE, Salzberg SL. Identification of microbial agents in tissue specimens of ocular and periocular sarcoidosis using a metagenomics approach. F1000Res 2021; 10:820. [PMID: 36212901 PMCID: PMC9515606 DOI: 10.12688/f1000research.55090.1] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Accepted: 08/09/2021] [Indexed: 11/20/2022] Open
Abstract
Background: Metagenomic sequencing has the potential to identify a wide range of pathogens in human tissue samples. Sarcoidosis is a complex disorder whose etiology remains unknown and for which a variety of infectious causes have been hypothesized. We sought to conduct metagenomic sequencing on cases of ocular and periocular sarcoidosis, none of them with previously identified infectious causes. Methods: Archival tissue specimens of 16 subjects with biopsies of ocular and periocular tissues that were positive for non-caseating granulomas were used as cases. Four archival tissue specimens that did not demonstrate non-caseating granulomas were also included as controls. Genomic DNA was extracted from tissue sections. DNA libraries were generated from the extracted genomic DNA and the libraries underwent next-generation sequencing. Results: We generated between 4.8 and 20.7 million reads for each of the 16 cases plus four control samples. For eight of the cases, we identified microbial pathogens that were present well above the background, with one potential pathogen identified for seven of the cases and two possible pathogens for one of the cases. Five of the eight cases were associated with bacteria ( Campylobacter concisus, Neisseria elongata, Streptococcus salivarius, Pseudopropionibacterium propionicum, and Paracoccus yeei), two cases with fungi ( Exophiala oligosperma, Lomentospora prolificans and Aspergillus versicolor) and one case with a virus (Mupapillomavirus 1). Interestingly, four of the five bacterial species are also part of the human oral microbiome. Conclusions: Using a metagenomic sequencing we identified possible infectious causes in half of the ocular and periocular sarcoidosis cases analyzed. Our findings support the proposition that sarcoidosis could be an etiologically heterogenous disease. Because these are previously banked samples, direct follow-up in the respective patients is impossible, but these results suggest that sequencing may be a valuable tool in better understanding the etiopathogenesis of sarcoidosis and in diagnosing and treating this disease.
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Affiliation(s)
| | - Christopher Pockrandt
- Center for Computational Biology, Johns Hopkins University, Baltimore, MD, USA
- Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD, USA
| | - Natalia Rincon
- Center for Computational Biology, Johns Hopkins University, Baltimore, MD, USA
- Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD, USA
| | - Yuchen Ge
- Center for Computational Biology, Johns Hopkins University, Baltimore, MD, USA
- Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD, USA
| | - Jennifer Lu
- Center for Computational Biology, Johns Hopkins University, Baltimore, MD, USA
- Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD, USA
| | - Ales Varabyou
- Center for Computational Biology, Johns Hopkins University, Baltimore, MD, USA
- Department of Computer Science, Johns Hopkins University, Baltimore, MD, USA
| | - Anne E. Jedlicka
- Genomic Analysis and Sequencing Core Facility, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA
| | - Karen Sun
- Wilmer Eye Institute, Johns Hopkins University, Baltimore, MD, USA
| | - Alan L. Scott
- Department of Microbiology & Immunology, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA
| | - Charles Eberhart
- Wilmer Eye Institute, Johns Hopkins University, Baltimore, MD, USA
| | - Jennifer E. Thorne
- Wilmer Eye Institute, Johns Hopkins University, Baltimore, MD, USA
- Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA
| | - Steven L. Salzberg
- Center for Computational Biology, Johns Hopkins University, Baltimore, MD, USA
- Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD, USA
- Department of Computer Science, Johns Hopkins University, Baltimore, MD, USA
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Poosari A, Nutravong T, Sa-Ngiamwibool P, Namwat W, Chatrchaiwiwatana S, Ungareewittaya P. Association between infection with Campylobacter species, poor oral health and environmental risk factors on esophageal cancer: a hospital-based case-control study in Thailand. Eur J Med Res 2021; 26:82. [PMID: 34332608 PMCID: PMC8325836 DOI: 10.1186/s40001-021-00561-3] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/20/2021] [Accepted: 07/23/2021] [Indexed: 02/07/2023] Open
Abstract
Background Previous studies have shown the association between Campylobacter species infection and that environmental factors, poor oral hygiene in particular, are linked to an increased risk of esophageal cancer (EC). However, no study has reported on these factors in Thailand. Thus, this study’s objective was to evaluate the impact of the relationship between Campylobacter infection and environmental factors on EC incidence in the population of Thailand. Methods Data from a case–control study were collected from 105 newly diagnosed EC cases and 105 controls recruited from 2007 to 2017. Infection with Campylobacter spp. was detected in the formalin-fixed paraffin-embedded (FFPE) tissue of EC taken from gastroesophageal biopsy specimens obtained from the participants, and evaluated using TaqMan® real-time PCR. Multivariable logistic regression was performed to calculate the odds ratios (ORs) and perform data analysis. Results Smoking, alcohol use, a family history of cancer, history of gastroesophageal reflux disease, poor oral hygiene and Campylobacter spp. infection were shown to be significant risk factors for EC (p < 0.05). The combination of poor oral hygiene and infection with Campylobacter spp. constituted significant risk for EC (p < 0.001). In addition, the risk of EC in subjects co-infected with C. rectus and C. concisus that practiced poor oral hygiene was even higher and was significant (ORadj = 4.7; 95% CI 2.41–9.98; p = 0.003). Conclusions In Thailand, the major risk factors for EC are smoking status, alcohol drinking, family history of cancer, GERD, poor oral hygiene and Campylobacter spp. infection. This study found Campylobacter spp. prevalence to be associated with EC and appears to be enhanced by poor oral hygiene, suggesting that a combination of poor oral hygiene and Campylobacter species infection may together act as an important etiological risk factor for EC. Supplementary Information The online version contains supplementary material available at 10.1186/s40001-021-00561-3.
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Affiliation(s)
- Arisara Poosari
- Department of Microbiology, Faculty of Medicine, Khon Kaen University, Khon Kaen, 40002, Thailand
| | - Thitima Nutravong
- Department of Microbiology, Faculty of Medicine, Khon Kaen University, Khon Kaen, 40002, Thailand.
| | - Prakasit Sa-Ngiamwibool
- Department of Pathology, Faculty of Medicine, Khon Kaen Universtity, Khon Kaen, 40002, Thailand
| | - Wises Namwat
- Department of Microbiology, Faculty of Medicine, Khon Kaen University, Khon Kaen, 40002, Thailand
| | | | - Piti Ungareewittaya
- Department of Pathology, Faculty of Medicine, Khon Kaen Universtity, Khon Kaen, 40002, Thailand
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The Role of Microbiota in the Pathogenesis of Esophageal Adenocarcinoma. BIOLOGY 2021; 10:biology10080697. [PMID: 34439930 PMCID: PMC8389269 DOI: 10.3390/biology10080697] [Citation(s) in RCA: 15] [Impact Index Per Article: 3.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 06/14/2021] [Revised: 07/05/2021] [Accepted: 07/12/2021] [Indexed: 12/20/2022]
Abstract
Simple Summary Esophageal adenocarcinoma has a poor 5-year survival rate and is among the highest mortality cancers. Changes in the esophageal microbiome have been associated with cancer pathogenesis; however, the molecular mechanism remains obscure. This review article critically analyzes the molecular mechanisms through which microbiota may mediate the development and progression of esophageal adenocarcinoma and its precursors-gastroesophageal reflux disease and Barrett’s esophagus. It summarizes changes in esophageal microbiome composition in normal and pathologic states and subsequently discusses the role of altered microbiota in disease progression. The potential role of esophageal microbiota in protecting against the development of esophageal adenocarcinoma is also discussed. By doing so, this article highlights specific directions for future research developing microbiome-mediated therapeutics for esophageal adenocarcinoma. Abstract Esophageal adenocarcinoma (EAC) is associated with poor overall five-year survival. The incidence of esophageal cancer is on the rise, especially in Western societies, and the pathophysiologic mechanisms by which EAC develops are of extreme interest. Several studies have proposed that the esophageal microbiome may play an important role in the pathophysiology of EAC, as well as its precursors—gastroesophageal reflux disease (GERD) and Barrett’s esophagus (BE). Gastrointestinal microbiomes altered by inflammatory states have been shown to mediate tumorigenesis directly and are now being considered as novel targets for both cancer treatment and prevention. Elucidating molecular mechanisms through which the esophageal microbiome potentiates the development of GERD, BE, and EAC will provide a foundation on which new therapeutic targets can be developed. This review summarizes current findings that elucidate the molecular mechanisms by which microbiota promote the pathogenesis of GERD, BE, and EAC, revealing potential directions for additional research on the microbiome-mediated pathophysiology of EAC.
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Impact of Environmental and Pharmacologic Changes on the Upper Gastrointestinal Microbiome. Biomedicines 2021; 9:biomedicines9060617. [PMID: 34072493 PMCID: PMC8229529 DOI: 10.3390/biomedicines9060617] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/22/2021] [Revised: 05/23/2021] [Accepted: 05/26/2021] [Indexed: 02/08/2023] Open
Abstract
Diseases of the upper gastrointestinal tract have become more prevalent over time. Mechanisms of disease formation are still only partially understood. Recent literature has shown that the surrounding microbiome affects the propensity for disease formation in various parts of the upper gastrointestinal tract. A review was performed of any literature to our best knowledge concerning the effects of pharmacologic agents, environmental changes, and surgical intervention on the microbiome of the upper gastrointestinal tract. Searches of the literature were performed using specific keywords related to drugs, surgical procedures, and environmental factors. Many prescription and nonprescription drugs that are commonly used have varying effects on the upper gastrointestinal tract. Proton pump inhibitors may affect the relative prevalence of some organisms in the lower esophagus and have less effect in the proximal esophagus. Changes in the esophageal microbiome correlate with some esophageal diseases. Drugs that induce weight loss have also been shown to affect the microbiomes of the esophagus and stomach. Common surgical procedures are associated with shifts in the microbial community in the gastrointestinal tract. Environmental factors have been shown to affect the microbiome in the upper gastrointestinal tract, as geographic differences correlate with alterations in the microbiome of the gastrointestinal tract. Understanding the association of environmental and pharmacologic changes on the microbiome of the upper gastrointestinal tract will facilitate treatment plans to reduce morbidity from disease.
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Tustumi F, de Sousa JHB, Dornelas NM, Rosa GM, Steinman M, Bianchi ET. The Mechanisms for the Association of Cancer and Esophageal Dysmotility Disorders. Med Sci (Basel) 2021; 9:32. [PMID: 34064058 PMCID: PMC8163009 DOI: 10.3390/medsci9020032] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/13/2021] [Revised: 05/12/2021] [Accepted: 05/21/2021] [Indexed: 02/06/2023] Open
Abstract
BACKGROUND Achalasia and other esophageal dysmotility disorders mimicking achalasia can be associated with cancer. This study aimed to review the main mechanisms for which cancer may develop in esophageal dysmotility disorder patients. METHODS A narrative review was performed. RESULTS The mechanism for developing squamous cell carcinoma and adenocarcinoma are discussed. Besides, achalasia-like syndromes related to familial KIT-gene mutation and pseudoachalasia are discussed. CONCLUSIONS Knowing the main mechanism for which achalasia can be related to cancer is essential for clinicians to conduct the proper investigation, surveillance, and treatment.
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Affiliation(s)
- Francisco Tustumi
- Hospital Israelita Albert Einstein, Sao Paulo 05652-900, Brazil; (J.H.B.d.S.); (N.M.D.); (G.M.R.); (M.S.); (E.T.B.)
- Department of Gastroenterology, Faculdade de Medicina, Universidade de Sao Paulo, Sao Paulo 05403-000, Brazil
| | | | - Nicolas Medeiros Dornelas
- Hospital Israelita Albert Einstein, Sao Paulo 05652-900, Brazil; (J.H.B.d.S.); (N.M.D.); (G.M.R.); (M.S.); (E.T.B.)
| | - Guilherme Maganha Rosa
- Hospital Israelita Albert Einstein, Sao Paulo 05652-900, Brazil; (J.H.B.d.S.); (N.M.D.); (G.M.R.); (M.S.); (E.T.B.)
| | - Milton Steinman
- Hospital Israelita Albert Einstein, Sao Paulo 05652-900, Brazil; (J.H.B.d.S.); (N.M.D.); (G.M.R.); (M.S.); (E.T.B.)
| | - Edno Tales Bianchi
- Hospital Israelita Albert Einstein, Sao Paulo 05652-900, Brazil; (J.H.B.d.S.); (N.M.D.); (G.M.R.); (M.S.); (E.T.B.)
- Department of Gastroenterology, Faculdade de Medicina, Universidade de Sao Paulo, Sao Paulo 05403-000, Brazil
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D'Souza SM, Houston K, Keenan L, Yoo BS, Parekh PJ, Johnson DA. Role of microbial dysbiosis in the pathogenesis of esophageal mucosal disease: A paradigm shift from acid to bacteria? World J Gastroenterol 2021; 27:2054-2072. [PMID: 34025064 PMCID: PMC8117736 DOI: 10.3748/wjg.v27.i18.2054] [Citation(s) in RCA: 18] [Impact Index Per Article: 4.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/02/2021] [Revised: 03/06/2021] [Accepted: 04/14/2021] [Indexed: 02/06/2023] Open
Abstract
Genomic sequencing, bioinformatics, and initial speciation (e.g., relative abundance) of the commensal microbiome have revolutionized the way we think about the "human" body in health and disease. The interactions between the gut bacteria and the immune system of the host play a key role in the pathogenesis of gastrointestinal diseases, including those impacting the esophagus. Although relatively stable, there are a number of factors that may disrupt the delicate balance between the luminal esophageal microbiome (EM) and the host. These changes are thought to be a product of age, diet, antibiotic and other medication use, oral hygiene, smoking, and/or expression of antibiotic products (bacteriocins) by other flora. These effects may lead to persistent dysbiosis which in turn increases the risk of local inflammation, systemic inflammation, and ultimately disease progression. Research has suggested that the etiology of gastroesophageal reflux disease-related esophagitis includes a cytokine-mediated inflammatory component and is, therefore, not merely the result of esophageal mucosal exposure to corrosives (i.e., acid). Emerging evidence also suggests that the EM plays a major role in the pathogenesis of disease by inciting an immunogenic response which ultimately propagates the inflammatory cascade. Here, we discuss the potential role for manipulating the EM as a therapeutic option for treating the root cause of various esophageal disease rather than just providing symptomatic relief (i.e., acid suppression).
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Affiliation(s)
- Steve M D'Souza
- Department of Internal Medicine, Division of Gastroenterology, Eastern Virginia Medical School, Norfolk, VA 23502, United States
| | - Kevin Houston
- Department of Internal Medicine, Division of Gastroenterology, Eastern Virginia Medical School, Norfolk, VA 23502, United States
| | - Lauren Keenan
- Department of Internal Medicine, Division of Gastroenterology, Eastern Virginia Medical School, Norfolk, VA 23502, United States
| | - Byung Soo Yoo
- Department of Internal Medicine, Division of Gastroenterology, Eastern Virginia Medical School, Norfolk, VA 23502, United States
| | - Parth J Parekh
- Department of Internal Medicine, Division of Gastroenterology, Eastern Virginia Medical School, Norfolk, VA 23502, United States
| | - David A Johnson
- Department of Internal Medicine, Division of Gastroenterology, Eastern Virginia Medical School, Norfolk, VA 23502, United States
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Engevik MA, Danhof HA, Ruan W, Engevik AC, Chang-Graham AL, Engevik KA, Shi Z, Zhao Y, Brand CK, Krystofiak ES, Venable S, Liu X, Hirschi KD, Hyser JM, Spinler JK, Britton RA, Versalovic J. Fusobacterium nucleatum Secretes Outer Membrane Vesicles and Promotes Intestinal Inflammation. mBio 2021; 12:e02706-20. [PMID: 33653893 PMCID: PMC8092269 DOI: 10.1128/mbio.02706-20] [Citation(s) in RCA: 142] [Impact Index Per Article: 35.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/22/2020] [Accepted: 01/22/2021] [Indexed: 12/17/2022] Open
Abstract
Multiple studies have implicated microbes in the development of inflammation, but the mechanisms remain unknown. Bacteria in the genus Fusobacterium have been identified in the intestinal mucosa of patients with digestive diseases; thus, we hypothesized that Fusobacterium nucleatum promotes intestinal inflammation. The addition of >50 kDa F. nucleatum conditioned media, which contain outer membrane vesicles (OMVs), to colonic epithelial cells stimulated secretion of the proinflammatory cytokines interleukin-8 (IL-8) and tumor necrosis factor (TNF). In addition, purified F. nucleatum OMVs, but not compounds <50 kDa, stimulated IL-8 and TNF production; which was decreased by pharmacological inhibition of Toll-like receptor 4 (TLR4). These effects were linked to downstream effectors p-ERK, p-CREB, and NF-κB. F. nucleatum >50-kDa compounds also stimulated TNF secretion, p-ERK, p-CREB, and NF-κB activation in human colonoid monolayers. In mice harboring a human microbiota, pretreatment with antibiotics and a single oral gavage of F. nucleatum resulted in inflammation. Compared to mice receiving vehicle control, mice treated with F. nucleatum showed disruption of the colonic architecture, with increased immune cell infiltration and depleted mucus layers. Analysis of mucosal gene expression revealed increased levels of proinflammatory cytokines (KC, TNF, IL-6, IFN-γ, and MCP-1) at day 3 and day 5 in F. nucleatum-treated mice compared to controls. These proinflammatory effects were absent in mice who received F. nucleatum without pretreatment with antibiotics, suggesting that an intact microbiome is protective against F. nucleatum-mediated immune responses. These data provide evidence that F. nucleatum promotes proinflammatory signaling cascades in the context of a depleted intestinal microbiome.IMPORTANCE Several studies have identified an increased abundance of Fusobacterium in the intestinal tracts of patients with colon cancer, liver cirrhosis, primary sclerosing cholangitis, gastroesophageal reflux disease, HIV infection, and alcoholism. However, the direct mechanism(s) of action of Fusobacterium on pathophysiological within the gastrointestinal tract is unclear. These studies have identified that F. nucleatum subsp. polymorphum releases outer membrane vesicles which activate TLR4 and NF-κB to stimulate proinflammatory signals in vitro Using mice harboring a human microbiome, we demonstrate that F. nucleatum can promote inflammation, an effect which required antibiotic-mediated alterations in the gut microbiome. Collectively, these results suggest a mechanism by which F. nucleatum may contribute to intestinal inflammation.
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Affiliation(s)
- Melinda A Engevik
- Department of Pathology and Immunology, Baylor College of Medicine, Houston, Texas, USA
- Department of Pathology, Texas Children's Hospital, Houston, Texas, USA
| | - Heather A Danhof
- Department of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, Texas, USA
| | - Wenly Ruan
- Department of Pediatrics, Baylor College of Medicine, Houston, Texas, USA
| | - Amy C Engevik
- Department of Surgical Sciences, Vanderbilt University Medical Center, Nashville Tennessee, USA
| | - Alexandra L Chang-Graham
- Department of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, Texas, USA
| | - Kristen A Engevik
- Department of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, Texas, USA
| | - Zhongcheng Shi
- Department of Pathology and Immunology, Baylor College of Medicine, Houston, Texas, USA
- Department of Pathology, Texas Children's Hospital, Houston, Texas, USA
| | - Yanling Zhao
- Department of Pediatrics, Texas Children's Cancer Center, Texas Children's Hospital, Houston, Texas, USA
| | - Colleen K Brand
- Department of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, Texas, USA
| | - Evan S Krystofiak
- Department of Cell and Developmental Biology, Vanderbilt University, Nashville, Tennessee, USA
| | - Susan Venable
- Department of Pathology and Immunology, Baylor College of Medicine, Houston, Texas, USA
- Department of Pathology, Texas Children's Hospital, Houston, Texas, USA
| | - Xinli Liu
- Department of Pharmacological and Pharmaceutical Sciences, University of Houston, Houston, Texas, USA
| | - Kendal D Hirschi
- Department of Pediatrics and Human and Molecular Genetics, Children's Nutrition Research Center, Baylor College of Medicine, Houston, Texas, USA
| | - Joseph M Hyser
- Department of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, Texas, USA
| | - Jennifer K Spinler
- Department of Pathology and Immunology, Baylor College of Medicine, Houston, Texas, USA
- Department of Pathology, Texas Children's Hospital, Houston, Texas, USA
| | - Robert A Britton
- Department of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, Texas, USA
| | - James Versalovic
- Department of Pathology and Immunology, Baylor College of Medicine, Houston, Texas, USA
- Department of Pathology, Texas Children's Hospital, Houston, Texas, USA
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Mennini M, Tambucci R, Riccardi C, Rea F, De Angelis P, Fiocchi A, Assa'ad A. Eosinophilic Esophagitis and Microbiota: State of the Art. Front Immunol 2021; 12:595762. [PMID: 33679739 PMCID: PMC7933523 DOI: 10.3389/fimmu.2021.595762] [Citation(s) in RCA: 15] [Impact Index Per Article: 3.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/17/2020] [Accepted: 01/04/2021] [Indexed: 12/12/2022] Open
Abstract
Eosinophilic esophagitis (EoE) is a chronic, food-triggered, immune-mediated disease of the oesophagus, clinically characterized by symptoms referred to oesophagal dysfunction, and histologically defined by an eosinophil productive inflammation of the oesophagal mucosa, among other cell types. The involvement of an adaptive Th2-type response to food antigens in EoE was known since 2000; several cytokines and chemokines promote food-specific responses, during which local production of IgE, but also IgG4 derived from plasma cells in lamina propria of oesophagal mucosa might play an important role. Evidence pointing towards a possible role for the innate immunity in EoE has arisen recently. Together, this evidence gives rise to a potential role that the innate immune system in general, and also the microbial pattern recognition receptors (PRRs) might play in EoE pathogenesis. Among PRRs, Toll-like receptors (TLRs) are type-I transmembrane receptors expressed both on epithelial and lamina propria cells with the capacity to distinguish between pathogen and commensal microbes. As TLRs in the different intestinal epithelia represent the primary mechanism of epithelial recognition of bacteria, this evidence underlines that oesophagal TLR-dependent signaling pathways in EoE support the potential implication of microbiota and the innate immune system in the pathogenesis of this disease. The oesophagal mucosa hosts a resident microbiota, although in a smaller population as compared with other districts of the gastrointestinal tract. Few studies have focused on the composition of the microbiota of the normal oesophagus alone. Still, additional information has come from studies investigating the oesophagal microbiota in disease and including healthy patients as controls. Our review aims to describe all the evidence on the oesophagal and intestinal microbiota in patients with EoE to identify the specific features of dysbiosis in this condition.
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Affiliation(s)
- Maurizio Mennini
- Division of Allergy, Bambino Gesù Children's Hospital-Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS), Rome, Italy
| | - Renato Tambucci
- Digestive Endoscopy and Surgery Unit, Bambino Gesù Children's Hospital-IRCCS, Rome, Italy
| | - Carla Riccardi
- Division of Allergy, Bambino Gesù Children's Hospital-Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS), Rome, Italy
| | - Francesca Rea
- Digestive Endoscopy and Surgery Unit, Bambino Gesù Children's Hospital-IRCCS, Rome, Italy
| | - Paola De Angelis
- Digestive Endoscopy and Surgery Unit, Bambino Gesù Children's Hospital-IRCCS, Rome, Italy
| | - Alessandro Fiocchi
- Division of Allergy, Bambino Gesù Children's Hospital-Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS), Rome, Italy
| | - Amal Assa'ad
- Division of Allergy and Immunology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, United States
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Choudhry H. The Microbiome and Its Implications in Cancer Immunotherapy. Molecules 2021; 26:E206. [PMID: 33401586 PMCID: PMC7795182 DOI: 10.3390/molecules26010206] [Citation(s) in RCA: 14] [Impact Index Per Article: 3.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/29/2020] [Revised: 12/22/2020] [Accepted: 12/30/2020] [Indexed: 02/06/2023] Open
Abstract
Cancer is responsible for ~18 million deaths globally each year, representing a major cause of death. Several types of therapy strategies such as radiotherapy, chemotherapy and more recently immunotherapy, have been implemented in treating various types of cancer. Microbes have recently been found to be both directly and indirectly involved in cancer progression and regulation, and studies have provided novel and clear insights into the microbiome-mediated emergence of cancers. Scientists around the globe are striving hard to identify and characterize these microbes and the underlying mechanisms by which they promote or suppress various kinds of cancer. Microbes may influence immunotherapy by blocking various cell cycle checkpoints and the production of certain metabolites. Hence, there is an urgent need to better understand the role of these microbes in the promotion and suppression of cancer. The identification of microbes may help in the development of future diagnostic tools to cure cancers possibly associated with the microbiome. This review mainly focuses on various microbes and their association with different types of cancer, responses to immunotherapeutic modulation, physiological responses, and prebiotic and postbiotic effects.
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Affiliation(s)
- Hani Choudhry
- Department of Biochemistry, Faculty of Sciences, Cancer and Mutagenesis Unit, King Fahd Medical Research Center, King Abdulaziz University, Jeddah 21589, Saudi Arabia
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Liu F, Liu M, Liu Y, Guo C, Zhou Y, Li F, Xu R, Liu Z, Deng Q, Li X, Zhang C, Pan Y, Ning T, Dong X, Hu Z, Bao H, Cai H, Silva IDS, He Z, Ke Y. Oral microbiome and risk of malignant esophageal lesions in a high-risk area of China: A nested case-control study. Chin J Cancer Res 2020; 32:742-754. [PMID: 33446997 PMCID: PMC7797237 DOI: 10.21147/j.issn.1000-9604.2020.06.07] [Citation(s) in RCA: 14] [Impact Index Per Article: 2.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/07/2023] Open
Abstract
Objective We aimed to prospectively evaluate the association of oral microbiome with malignant esophageal lesions and its predictive potential as a biomarker of risk. Methods We conducted a case-control study nested within a population-based cohort with up to 8 visits of oral swab collection for each subject over an 11-year period in a high-risk area for esophageal cancer in China. The oral microbiome was evaluated with 16S ribosomal RNA (rRNA) gene sequencing in 428 pre-diagnostic oral specimens from 84 cases with esophageal lesions of severe squamous dysplasia and above (SDA) and 168 matched healthy controls. DESeq analysis was performed to identify taxa of differential abundance. Differential oral species together with subject characteristics were evaluated for their potential in predicting SDA risk by constructing conditional logistic regression models. Results A total of 125 taxa including 37 named species showed significantly different abundance between SDA cases and controls (all P<0.05 & false discovery rate-adjusted Q<0.10). A multivariate logistic model including 11 SDA lesion-related species and family history of esophageal cancer provided an area under the receiver operating characteristic curve (AUC) of 0.89 (95% CI, 0.84−0.93). Cross-validation and sensitivity analysis, excluding cases diagnosed within 1 year of collection of the baseline specimen and their matched controls, or restriction to screen-endoscopic-detected or clinically diagnosed case-control triads, or using only bacterial data measured at the baseline, yielded AUCs>0.84. Conclusions The oral microbiome may play an etiological and predictive role in esophageal cancer, and it holds promise as a non-invasive early warning biomarker for risk stratification for esophageal cancer screening programs.
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Affiliation(s)
- Fangfang Liu
- Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Laboratory of Genetics, Peking University Cancer Hospital & Institute, Beijing 100142, China
| | - Mengfei Liu
- Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Laboratory of Genetics, Peking University Cancer Hospital & Institute, Beijing 100142, China
| | - Ying Liu
- Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Laboratory of Genetics, Peking University Cancer Hospital & Institute, Beijing 100142, China
| | - Chuanhai Guo
- Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Laboratory of Genetics, Peking University Cancer Hospital & Institute, Beijing 100142, China
| | | | - Fenglei Li
- Hua County People's Hospital, Anyang 456400, China
| | - Ruiping Xu
- Anyang Cancer Hospital, Anyang 455000, China
| | - Zhen Liu
- Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Laboratory of Genetics, Peking University Cancer Hospital & Institute, Beijing 100142, China
| | - Qiuju Deng
- Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Laboratory of Genetics, Peking University Cancer Hospital & Institute, Beijing 100142, China
| | - Xiang Li
- Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Laboratory of Genetics, Peking University Cancer Hospital & Institute, Beijing 100142, China
| | - Chaoting Zhang
- Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Laboratory of Genetics, Peking University Cancer Hospital & Institute, Beijing 100142, China
| | - Yaqi Pan
- Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Laboratory of Genetics, Peking University Cancer Hospital & Institute, Beijing 100142, China
| | - Tao Ning
- Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Laboratory of Genetics, Peking University Cancer Hospital & Institute, Beijing 100142, China
| | - Xiao Dong
- Novogene Co., Ltd, Beijing 100080, China
| | - Zhe Hu
- Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Laboratory of Genetics, Peking University Cancer Hospital & Institute, Beijing 100142, China
| | - Huanyu Bao
- Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Laboratory of Genetics, Peking University Cancer Hospital & Institute, Beijing 100142, China
| | - Hong Cai
- Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Laboratory of Genetics, Peking University Cancer Hospital & Institute, Beijing 100142, China
| | - Isabel Dos Santos Silva
- Department of Non-communicable Disease Epidemiology, London School of Hygiene & Tropical Medicine, London WC1E 7HT, UK
| | - Zhonghu He
- Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Laboratory of Genetics, Peking University Cancer Hospital & Institute, Beijing 100142, China
| | - Yang Ke
- Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Laboratory of Genetics, Peking University Cancer Hospital & Institute, Beijing 100142, China
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Relationship of the Esophageal Microbiome and Tissue Gene Expression and Links to the Oral Microbiome: A Randomized Clinical Trial. Clin Transl Gastroenterol 2020; 11:e00235. [PMID: 33512805 PMCID: PMC7721221 DOI: 10.14309/ctg.0000000000000235] [Citation(s) in RCA: 13] [Impact Index Per Article: 2.6] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/24/2022] Open
Abstract
INTRODUCTION Although the microbiome is altered in various esophageal diseases, there is no direct evidence for a link between the oral or esophageal microbiome and underlying esophageal tissue. Here, we aimed to address these gaps through use of an antimicrobial mouth rinse to modify the esophageal microbiome and tissue gene expression. METHODS In this randomized controlled trial, patients scheduled to undergo endoscopy for clinical indications used chlorhexidine mouth rinse or no treatment for 2 weeks before endoscopy. Oral swabs and saliva were collected at baseline and at follow-up, and the esophagus was sampled on the day of endoscopy. The microbiome was analyzed by 16S rRNA gene sequencing, and esophageal tissue gene expression was ascertained by RNA-Seq. RESULTS Twenty subjects were enrolled and included in the analyses. Within individuals, the oral and esophageal microbiome composition was significantly correlated. Chlorhexidine treatment associated with significant alterations to the relative abundance of several esophageal bacterial taxa, and to expression of genes in the esophagus including reductions in periostin, claudin-18, chemokines CXCL1 and CXCL13, and several members of the tumor necrosis factor receptor superfamily. A taxon in genus Haemophilus in the esophagus also associated with significant changes in tissue gene expression. DISCUSSION The oral and esophageal microbiomes are closely related within individuals, and esophageal microbiome alterations correlate with tissue gene expression changes. The esophageal microbiome may act as an important cofactor that influences pathogenesis and outcomes of diseases such as eosinophilic esophagitis, gastroesophageal reflux, and Barrett's esophagus.
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45
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Ren X, Hao S, Yang C, Yuan L, Zhou X, Zhao H, Yao J. Alterations of intestinal microbiota in liver cirrhosis with muscle wasting. Nutrition 2020; 83:111081. [PMID: 33348106 DOI: 10.1016/j.nut.2020.111081] [Citation(s) in RCA: 14] [Impact Index Per Article: 2.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/14/2020] [Revised: 11/09/2020] [Accepted: 11/09/2020] [Indexed: 02/08/2023]
Abstract
OBJECTIVES The intestinal microbiota plays an important role in the nutritional status and energy metabolism of the host. Liver cirrhosis is accompanied by muscle wasting or sarcopenia. The aim of this study was to to explore the changes in intestinal microbiota in patients with liver cirrhosis and muscle wasting by using metagenomics. METHODS This was a cross-sectional study of patients with (n = 30) and without (n = 30) muscle wasting and age- and sex-matched healthy controls (n = 30) to evaluate changes in intestinal microbiota by metagenomic gene sequencing. Muscle wasting was determined by the third lumbar vertebrae skeletal muscle index (L3 SMI). RESULTS The Shannon index, which represents species diversity, of patients in the muscle-wasting group (2.11 ± 0.88) was lower than in the non-muscle-wasting group (2.64 ± 0.68; P = 0.039), which was significantly lower than in the healthy control group (2.70 ± 0.53; P = 0.023). There were 17 microbial species with significant differences in relative abundance between the two groups (linear discriminant analysis score >2; P < 0.05). The relative abundance of Escherichia coli, Peptostreptococcus stomatis, and Bacteroides uniformis showed the most significant association with L3 SMI. CONCLUSIONS There were compositional alterations in intestinal microbiota in patients with liver cirrhosis and muscle wasting. L3 SMI is closely related to E. coli, P. stomatis, and B. uniformis in liver cirrhosis. Further interventional studies are needed to confirm whether improving intestinal microbiota can improve the nutritional status of patients with liver cirrhosis.
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Affiliation(s)
- Xiaojing Ren
- Department of Gastroenterology and General Surgery, Shanxi Bethune Hospital, Shanxi Medical University, Taiyuan, China; Shanxi Bethune Hospital, Taiyuan, China
| | - Shasha Hao
- Department of Gastroenterology and General Surgery, Shanxi Bethune Hospital, Shanxi Medical University, Taiyuan, China; Shanxi Bethune Hospital, Taiyuan, China
| | - Chuanli Yang
- Department of Gastroenterology and General Surgery, Shanxi Bethune Hospital, Shanxi Medical University, Taiyuan, China; Shanxi Bethune Hospital, Taiyuan, China
| | - Lili Yuan
- Department of Gastroenterology and General Surgery, Shanxi Bethune Hospital, Shanxi Medical University, Taiyuan, China; Shanxi Bethune Hospital, Taiyuan, China
| | - Xiaoshuang Zhou
- Department of Nephrology, Shanxi Provincial People's Hospital, Shanxi Medical University, Taiyuan, China
| | - Haoliang Zhao
- Department of Gastroenterology and General Surgery, Shanxi Bethune Hospital, Shanxi Medical University, Taiyuan, China; Shanxi Bethune Hospital, Taiyuan, China
| | - Jia Yao
- Department of Gastroenterology and General Surgery, Shanxi Bethune Hospital, Shanxi Medical University, Taiyuan, China; Shanxi Bethune Hospital, Taiyuan, China.
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46
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Liu F, Chen S, Luu LDW, Lee SA, Tay ACY, Wu R, Riordan SM, Lan R, Liu L, Zhang L. Analysis of complete Campylobacter concisus genomes identifies genomospecies features, secretion systems and novel plasmids and their association with severe ulcerative colitis. Microb Genom 2020; 6:mgen000457. [PMID: 33111662 PMCID: PMC7725323 DOI: 10.1099/mgen.0.000457] [Citation(s) in RCA: 12] [Impact Index Per Article: 2.4] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/12/2020] [Accepted: 10/01/2020] [Indexed: 12/12/2022] Open
Abstract
Campylobacter concisus is an emerging enteric pathogen that is associated with several gastrointestinal diseases, such as inflammatory bowel disease (IBD), which includes Crohn's disease (CD) and ulcerative colitis (UC). Currently, only three complete C. concisus genomes are available and more complete C. concisus genomes are needed in order to better understand the genomic features and pathogenicity of this emerging pathogen. DNA extracted from 22 C. concisus strains were subjected to Oxford Nanopore genome sequencing. Complete genome assembly was performed using Nanopore genome data in combination with previously reported short-read Illumina data. Genome features of complete C. concisus genomes were analysed using bioinformatic tools. The enteric disease associations of C. concisus plasmids were examined using 239 C. concisus strains and confirmed using PCRs. Proteomic analysis was used to examine T6SS secreted proteins. We successfully obtained 13 complete C. concisus genomes in this study. Analysis of 16 complete C. concisus genomes (3 from public databases) identified multiple novel plasmids. pSma1 plasmid was found to be associated with severe UC. Sec-SRP, Tat and T6SS were found to be the main secretion systems in C. concisus and proteomic data showed a functional T6SS despite the lack of ClpV. T4SS was found in 25% of complete C. concisus genomes. This study also found that GS2 strains had larger genomes and higher GC content than GS1 strains and more often had plasmids. In conclusion, this study provides fundamental genomic data for understanding C. concisus plasmids, genomospecies features, evolution, secretion systems and pathogenicity.
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Affiliation(s)
- Fang Liu
- School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, Australia
| | - Siying Chen
- School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, Australia
| | - Laurence Don Wai Luu
- School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, Australia
| | - Seul A. Lee
- School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, Australia
| | - Alfred Chin Yen Tay
- Helicobacter Research Laboratory, Marshall Centre for Infectious Diseases Research and Training, School of Pathology and Laboratory Medicine, University of Western Australia, Perth, Australia
| | - Ruochen Wu
- School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, Australia
| | - Stephen M. Riordan
- Gastrointestinal and Liver Unit, Prince of Wales Hospital, University of New South Wales, Sydney, Australia
| | - Ruiting Lan
- School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, Australia
| | - Lu Liu
- School of Medical Sciences, University of New South Wales, Sydney, NSW, Australia
| | - Li Zhang
- School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, Australia
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47
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Gyawali CP, Sonu I, Becker L, Sarosiek J. The esophageal mucosal barrier in health and disease: mucosal pathophysiology and protective mechanisms. Ann N Y Acad Sci 2020; 1482:49-60. [PMID: 33128243 DOI: 10.1111/nyas.14521] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/15/2020] [Revised: 10/09/2020] [Accepted: 10/10/2020] [Indexed: 12/13/2022]
Abstract
Diseases of the esophagus, such as gastroesophageal reflux (GER), can result in changes to mucosal integrity, neurological function, and the microbiome. Although poorly understood, both age and GER can lead to changes to the enteric nervous system. In addition, the esophagus has a distinct microbiome that can be altered in GER. Mucosal integrity is also at risk due to persistent damage from acid. Diagnostic tools, such as ambulatory pH/impedance testing and esophageal mucosal impedance, can assess short-term and longitudinal GER burden, which can also assess the risk for mucosal compromise. The quality of the mucosal barrier is determined by its intercellular spaces, tight junctions, and tight junction proteins, which are represented by claudins, occludins, and adhesion molecules. Fortunately, there are protective factors for mucosal integrity that are secreted by the esophageal submucosal mucous glands and within saliva that are augmented by mastication. These protective factors have potential as therapeutic targets for GER. In this article, we aim to review diagnostic tools used to predict mucosal integrity, aging, and microbiome changes to the esophagus and esophageal mucosal defense mechanisms.
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Affiliation(s)
- C Prakash Gyawali
- Division of Gastroenterology and Hepatology, Washington University School of Medicine, St. Louis, Missouri
| | - Irene Sonu
- Division of Gastroenterology and Hepatology, Stanford University School of Medicine, Stanford, California
| | - Laren Becker
- Division of Gastroenterology and Hepatology, Stanford University School of Medicine, Stanford, California
| | - Jerzy Sarosiek
- Division of Gastroenterology and Hepatology, Molecular Medicine Research Laboratory, Texas Tech University Health Sciences Center, Paul L. Foster School of Medicine, El Paso, Texas
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48
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Lopetuso LR, Severgnini M, Pecere S, Ponziani FR, Boskoski I, Larghi A, Quaranta G, Masucci L, Ianiro G, Camboni T, Gasbarrini A, Costamagna G, Consolandi C, Cammarota G. Esophageal microbiome signature in patients with Barrett's esophagus and esophageal adenocarcinoma. PLoS One 2020; 15:e0231789. [PMID: 32369505 PMCID: PMC7199943 DOI: 10.1371/journal.pone.0231789] [Citation(s) in RCA: 64] [Impact Index Per Article: 12.8] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/16/2019] [Accepted: 03/31/2020] [Indexed: 12/16/2022] Open
Abstract
Preliminary studies suggested a possible correlation of microbiota with Barrett's esophagus (BE) and esophageal adenocarcinoma (EAC), where the need for tools to ameliorate its poor prognosis is mandatory. We explored the potential signature of esophageal microbiota and its predicted functional profile along the continuous spectrum from BE to EAC. We analyzed through 16S-based amplicon sequencing the mucosal microbiota and the microbiota-related functional predictions in 10 BE and 6 EAC patients compared with 10 controls, exploring also potential differences between the metaplastic mucosa (BEM) and the adjacent normal areas of BE patients (BEU). BEM and EAC showed a higher level of α and β-diversity. BEM evidenced a decrease of Streptococcus and an increase of Prevotella, Actinobacillus, Veillonella, and Leptotrichia. EAC displayed a striking reduction of Streptococcus, with an increase of Prevotella, Veillonella and Leptotrichia. LefSe analysis identified Leptotrichia as the main taxa distinguishing EAC. BEM showed a decreased α-diversity compared with BEU and a reduction of Bacteroidetes, Prevotella and Fusobacterium. Functional predictions identified peculiar profiles for each group with a high potential for replication and repair in BEM; an upregulated energy, replication and signaling metabolisms, with the fatty-acids biosynthesis and nitrogen and D-alanine pathways down-regulated in EAC. Our pilot study identifies a unique microbial structure and function profile for BE and EAC, as well as for metaplastic and near-normal areas. It proposes a new concept for BE, which could be intended not only as the histological, but, also, as the microbial closest precursor of EAC. This requires further larger follow-up studies, but opens intriguing horizons towards innovative diagnostic and therapeutic options for EAC.
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Affiliation(s)
- Loris Riccardo Lopetuso
- Dipartimento di Scienze Mediche e Chirurgiche, UOC Medicina Interna e Gastroenterologia, Fondazione Policlinico Universitario A. Gemelli IRCCS, Roma, Italia.,Department of Medicine and Ageing Sciences,"G. d'Annunzio" University of Chieti-Pescara, Chieti, Italia.,Center for Advanced Studies and Technology (CAST), "G. d'Annunzio" University of Chieti-Pescara, Chieti, Italia
| | - Marco Severgnini
- Institute of Biomedical Technologies, Italian National Research Council, Segrate (Milano), Italia
| | - Silvia Pecere
- Digestive Endoscopy Unit, Fondazione Policlinico Universitario A. Gemelli IRCSS, Roma, Italia.,Centre for Endoscopic Research Therapeutic and Training CERTT, Università Cattolica del Sacro Cuore, Roma, Italia
| | - Francesca Romana Ponziani
- Dipartimento di Scienze Mediche e Chirurgiche, UOC Medicina Interna e Gastroenterologia, Fondazione Policlinico Universitario A. Gemelli IRCCS, Roma, Italia.,Istituto di Patologia Speciale Medica, Università Cattolica del Sacro Cuore, Roma, Italia
| | - Ivo Boskoski
- Digestive Endoscopy Unit, Fondazione Policlinico Universitario A. Gemelli IRCSS, Roma, Italia.,Centre for Endoscopic Research Therapeutic and Training CERTT, Università Cattolica del Sacro Cuore, Roma, Italia
| | - Alberto Larghi
- Digestive Endoscopy Unit, Fondazione Policlinico Universitario A. Gemelli IRCSS, Roma, Italia.,Centre for Endoscopic Research Therapeutic and Training CERTT, Università Cattolica del Sacro Cuore, Roma, Italia
| | - Gianluca Quaranta
- Dipartimento di Microbiologia, Fondazione Policlinico Universitario A. Gemelli IRCCS, Roma, Italia
| | - Luca Masucci
- Dipartimento di Microbiologia, Fondazione Policlinico Universitario A. Gemelli IRCCS, Roma, Italia
| | - Gianluca Ianiro
- Dipartimento di Scienze Mediche e Chirurgiche, UOC Medicina Interna e Gastroenterologia, Fondazione Policlinico Universitario A. Gemelli IRCCS, Roma, Italia.,Istituto di Patologia Speciale Medica, Università Cattolica del Sacro Cuore, Roma, Italia
| | - Tania Camboni
- Institute of Biomedical Technologies, Italian National Research Council, Segrate (Milano), Italia
| | - Antonio Gasbarrini
- Dipartimento di Scienze Mediche e Chirurgiche, UOC Medicina Interna e Gastroenterologia, Fondazione Policlinico Universitario A. Gemelli IRCCS, Roma, Italia.,Istituto di Patologia Speciale Medica, Università Cattolica del Sacro Cuore, Roma, Italia
| | - Guido Costamagna
- Digestive Endoscopy Unit, Fondazione Policlinico Universitario A. Gemelli IRCSS, Roma, Italia.,Centre for Endoscopic Research Therapeutic and Training CERTT, Università Cattolica del Sacro Cuore, Roma, Italia
| | - Clarissa Consolandi
- Centre for Endoscopic Research Therapeutic and Training CERTT, Università Cattolica del Sacro Cuore, Roma, Italia
| | - Giovanni Cammarota
- Dipartimento di Scienze Mediche e Chirurgiche, UOC Medicina Interna e Gastroenterologia, Fondazione Policlinico Universitario A. Gemelli IRCCS, Roma, Italia.,Istituto di Patologia Speciale Medica, Università Cattolica del Sacro Cuore, Roma, Italia
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49
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Park CH, Lee SK. Exploring Esophageal Microbiomes in Esophageal Diseases: A Systematic Review. J Neurogastroenterol Motil 2020; 26:171-179. [PMID: 32235026 PMCID: PMC7176507 DOI: 10.5056/jnm19240] [Citation(s) in RCA: 39] [Impact Index Per Article: 7.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/28/2019] [Revised: 02/11/2020] [Accepted: 02/27/2020] [Indexed: 12/12/2022] Open
Abstract
Studies that investigated esophageal microbiomes are limited when compared to those on intestinal microbiomes. Nevertheless, several studies have investigated the relationship between esophageal microbiomes and various esophageal diseases, owing to the advancement of next-generation sequencing techniques. Streptococcus is the most common bacterial taxon in a normal esophagus. Additionally, Haemophilus, Neisseria, Prevotella, and Veillonella are also found. However, gram-negative bacteria, including Prevotella, are more abundant in a diseased esophagus, such as in gastroesophageal reflux disease and Barrett’ esophagus. This systematic review aims to summarize current evidences on esophageal microbiomes in various esophageal diseases.
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Affiliation(s)
- Chan Hyuk Park
- Department of Internal Medicine, Hanyang University Guri Hospital, Hanyang University College of Medicine, Guri, Gyeonggi-do, Korea
| | - Sang Kil Lee
- Division of Gastroenterology, Department of Internal Medicine, Severance Hospital, Yonsei University College of Medicine, Seoul, Korea
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50
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Jung HK, Hong SJ, Lee OY, Pandolfino J, Park H, Miwa H, Ghoshal UC, Mahadeva S, Oshima T, Chen M, Chua ASB, Cho YK, Lee TH, Min YW, Park CH, Kwon JG, Park MI, Jung K, Park JK, Jung KW, Lim HC, Jung DH, Kim DH, Lim CH, Moon HS, Park JH, Choi SC, Suzuki H, Patcharatrakul T, Wu JCY, Lee KJ, Tanaka S, Siah KTH, Park KS, Kim SE. 2019 Seoul Consensus on Esophageal Achalasia Guidelines. J Neurogastroenterol Motil 2020; 26:180-203. [PMID: 32235027 PMCID: PMC7176504 DOI: 10.5056/jnm20014] [Citation(s) in RCA: 53] [Impact Index Per Article: 10.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 01/29/2020] [Accepted: 03/08/2020] [Indexed: 12/13/2022] Open
Abstract
Esophageal achalasia is a primary motility disorder characterized by insufficient lower esophageal sphincter relaxation and loss of esophageal peristalsis. Achalasia is a chronic disease that causes progressive irreversible loss of esophageal motor function. The recent development of high-resolution manometry has facilitated the diagnosis of achalasia, and determining the achalasia subtypes based on high-resolution manometry can be important when deciding on treatment methods. Peroral endoscopic myotomy is less invasive than surgery with comparable efficacy. The present guidelines (the "2019 Seoul Consensus on Esophageal Achalasia Guidelines") were developed based on evidence-based medicine; the Asian Neurogastroenterology and Motility Association and Korean Society of Neurogastroenterology and Motility served as the operating and development committees, respectively. The development of the guidelines began in June 2018, and a draft consensus based on the Delphi process was achieved in April 2019. The guidelines consist of 18 recommendations: 2 pertaining to the definition and epidemiology of achalasia, 6 pertaining to diagnoses, and 10 pertaining to treatments. The endoscopic treatment section is based on the latest evidence from meta-analyses. Clinicians (including gastroenterologists, upper gastrointestinal tract surgeons, general physicians, nurses, and other hospital workers) and patients could use these guidelines to make an informed decision on the management of achalasia.
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Affiliation(s)
- Hye-Kyung Jung
- Department of Internal Medicine, Ewha Womans University College of Medicine, Seoul, Korea
| | - Su Jin Hong
- Digestive Disease Center and Research Institute, Department of Internal Medicine, Soonchunhyang University College of Medicine, Bucheon, Korea
| | - Oh Young Lee
- Department of Internal Medicine, Hanyang University Hospital, Hanyang University College of Medicine, Seoul, Korea
| | - John Pandolfino
- Department of Medicine, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA
| | - Hyojin Park
- Division of Gastroenterology, Gangnam Severance Hospital, Yonsei University College of Medicine, Seoul, Korea
| | - Hiroto Miwa
- Division of Gastroenterology, Department of Internal Medicine, Hyogo College of Medicine, Mukogawa-cho, Nishinomiya, Hyogo, Japan
| | - Uday C Ghoshal
- Department of Gastroenterology, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, India
| | - Sanjiv Mahadeva
- Division of Gastroenterology, Department of Medicine, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia
| | - Tadayuki Oshima
- Division of Gastroenterology, Department of Internal Medicine, Hyogo College of Medicine, Mukogawa-cho, Nishinomiya, Hyogo, Japan
| | - Minhu Chen
- Department of Gastroenterology and Hepatology, The First Affiliated Hospital of Sun Yat-sen University, Guangzhou, China
| | | | - Yu Kyung Cho
- Division of Gastroenterology and Hepatology, Department of Internal Medicine, Seoul St. Mary's Hospital, The Catholic University of Korea, Seoul, Korea
| | - Tae Hee Lee
- Department of Internal Medicine, College of Medicine, Soonchunhyang University Hospital, Seoul, Korea
| | - Yang Won Min
- Department of Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea
| | - Chan Hyuk Park
- Department of Internal Medicine, Hanyang University Guri Hospital, Hanyang University College of Medicine, Guri, Korea
| | - Joong Goo Kwon
- Department of Internal Medicine, Daegu Catholic University School of Medicine, Daegu, Korea
| | - Moo In Park
- Department of Internal Medicine, Kosin University College of Medicine, Busan, Korea
| | - Kyoungwon Jung
- Department of Internal Medicine, Kosin University College of Medicine, Busan, Korea
| | - Jong Kyu Park
- Department of Internal Medicine, Gangneung Asan Hospital, University of Ulsan College of Medicine, Gangneung, Gangwon-do, Korea
| | - Kee Wook Jung
- Department of Gastroenterology, Asan Medical Center, University of Ulsan College of Medicine, University of Ulsan College of Medicine, Seoul, Korea
| | - Hyun Chul Lim
- Department of Internal Medicine, Yongin Severance Hospital, Yonsei University College of Medicine, Yongin, Korea
| | - Da Hyun Jung
- Division of Gastroenterology, Department of Internal Medicine, Severance Hospital, Yonsei University College of Medicine, Seoul, Korea
| | - Do Hoon Kim
- Department of Gastroenterology, Asan Medical Center, University of Ulsan College of Medicine, University of Ulsan College of Medicine, Seoul, Korea
| | - Chul-Hyun Lim
- Department of Internal Medicine, Eunpyeong St. Mary's Hospital, College of Medicine, The Catholic University of Korea, Seoul, Korea
| | - Hee Seok Moon
- Department of Internal Medicine, Chungnam National University School of Medicine, Daejeon, Korea
| | - Jung Ho Park
- Division of Gastroenterology, Department of Internal Medicine, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul, Korea
| | - Suck Chei Choi
- Department of Internal Medicine and Digestive Disease Research Institute, Wonkwang University School of Medicine, Iksan, Korea
| | - Hidekazu Suzuki
- Department of Gastroenterology and Hepatology, Tokai University School of Medicine, Isehara, Kanagawa, Japan
| | - Tanisa Patcharatrakul
- Department of Medicine, King Chulalongkorn Memorial Hospital, Thai Red Cross Society, Bangkok, Thailand
| | - Justin C Y Wu
- Department of Medicine and Therapeutics, Prince of Wales Hospital, Hong Kong, China
| | - Kwang Jae Lee
- Department of Gastroenterology, Ajou University School of Medicine, Suwon, Gyeonggi-do, Korea
| | - Shinwa Tanaka
- Department of Gastroenterology, Kobe University Hospital, Hyogo, Japan
| | - Kewin T H Siah
- Division of Gastroenterology and Hepatology, National University Health System, Singapore City, Singapore
| | - Kyung Sik Park
- Department of Internal Medicine, Keimyung University School of Medicine, Daegu, Korea
| | - Sung Eun Kim
- Department of Internal Medicine, Kosin University College of Medicine, Busan, Korea
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