Bacteria and Esophageal Cancer

A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Medical Microbiology".

Deadline for manuscript submissions: closed (30 September 2021) | Viewed by 22606

Special Issue Editor


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Guest Editor
Division of Digestive and Liver Diseases, Columbia University Irving Medical Center, New York, NY, USA
Interests: Barrett’s esophagus; esophageal cancer; microbiome; cancer prevention

Special Issue Information

Dear Colleagues,

Bacteria are known to promote the development of multiple gastrointestinal cancers and are emerging as a key co-factor in the development of esophageal cancer. Esophageal microbiome composition is strongly influenced by proximal migration of bacteria from the mouth as well as exposures such as acid reflux. Alterations to the tissue-associated microbiome have been described in Barrett’s esophagus and esophageal adenocarcinoma as well as esophageal squamous cell cancer. However, a significant gap in knowledge remains in our understanding of the mechanisms by which bacteria promote the development of esophageal cancer, the role of bacteria in treatment response and clinical outcomes in esophageal cancer, and how exposures influence esophageal microbiome composition with regard to cancer formation.

The aim of this special issue is to summarize the role of bacteria in esophageal cancer and to present novel research that add to our knowledge in this emerging field.  Potential topics include: bacteria that promote the development of esophageal cancer; mechanisms of bacterial-induced carcinogenesis; bacteria that impact outcomes in patients with esophageal cancer; bacterial metabolites that promote the development of esophageal cancer; microbiome-targeted therapies to lower the risk or improve outcomes in esophageal cancer; the oral microbiome as a biomarker for esophageal cancer; links between oral health, microbiome composition, and esophageal cancer; factors that influence esophageal microbiome composition.

Dr. Julian Abrams
Guest Editor

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Keywords

  • Esophageal neoplasms
  • Microbiota
  • Barrett esophagus
  • Bacteria
  • Biomarkers
  • Therapeutics
  • Chemoprevention
  • Inflammation
  • Oral health

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Published Papers (6 papers)

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Research

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24 pages, 7505 KiB  
Article
High-Fructose Diet Alters Intestinal Microbial Profile and Correlates with Early Tumorigenesis in a Mouse Model of Barrett’s Esophagus
by Andrea Proaño-Vasco, Theresa Baumeister, Amira Metwaly, Sandra Reitmeier, Karin Kleigrewe, Chen Meng, Michael Gigl, Thomas Engleitner, Rupert Öllinger, Roland Rad, Katja Steiger, Akanksha Anand, Julia Strangmann, Robert Thimme, Roland M. Schmid, Timothy C. Wang and Michael Quante
Microorganisms 2021, 9(12), 2432; https://doi.org/10.3390/microorganisms9122432 - 25 Nov 2021
Cited by 8 | Viewed by 3647
Abstract
Esophageal adenocarcinoma (EAC) is mostly prevalent in industrialized countries and has been associated with obesity, commonly linked with a diet rich in fat and refined sugars containing high fructose concentrations. In meta-organisms, dietary components are digested and metabolized by the host and its [...] Read more.
Esophageal adenocarcinoma (EAC) is mostly prevalent in industrialized countries and has been associated with obesity, commonly linked with a diet rich in fat and refined sugars containing high fructose concentrations. In meta-organisms, dietary components are digested and metabolized by the host and its gut microbiota. Fructose has been shown to induce proliferation and cell growth in pancreas and colon cancer cell lines and also alter the gut microbiota. In a previous study with the L2-IL-1B mouse model, we showed that a high-fat diet (HFD) accelerated EAC progression from its precursor lesion Barrett’s esophagus (BE) through changes in the gut microbiota. Aiming to investigate whether a high-fructose diet (HFrD) also alters the gut microbiota and favors EAC carcinogenesis, we assessed the effects of HFrD on the phenotype and intestinal microbial communities of L2-IL1B mice. Results showed a moderate acceleration in histologic disease progression, a mild effect on the systemic inflammatory response, metabolic changes in the host, and a shift in the composition, metabolism, and functionality of intestinal microbial communities. We conclude that HFrD alters the overall balance of the gut microbiota and induces an acceleration in EAC progression in a less pronounced manner than HFD. Full article
(This article belongs to the Special Issue Bacteria and Esophageal Cancer)
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10 pages, 762 KiB  
Article
Minimal Associations between Short-Term Dietary Intake and Salivary Microbiome Composition
by Judith Kim, Minyi Lee, Brittany Baldwin-Hunter, Quinn S. Solfisburg, Charles J. Lightdale, Tal Korem, Chin Hur and Julian A. Abrams
Microorganisms 2021, 9(8), 1739; https://doi.org/10.3390/microorganisms9081739 - 15 Aug 2021
Cited by 3 | Viewed by 2432
Abstract
Background: Increasing evidence points to the esophageal microbiome as an important co-factor in esophageal neoplasia. Esophageal microbiome composition is strongly influenced by the oral microbiome. Salivary microbiome assessment has emerged as a potential non-invasive tool to identify patients at risk for esophageal cancer, [...] Read more.
Background: Increasing evidence points to the esophageal microbiome as an important co-factor in esophageal neoplasia. Esophageal microbiome composition is strongly influenced by the oral microbiome. Salivary microbiome assessment has emerged as a potential non-invasive tool to identify patients at risk for esophageal cancer, but key host and environmental factors that may affect the salivary microbiome have not been well-defined. This study aimed to evaluate the impact of short-term dietary intake on salivary microbiome composition. Methods: Saliva samples were collected from 69 subjects prior to upper endoscopy who completed the Automated Self-Administered 24-Hour (ASA24) Dietary Assessment. Salivary microbiome composition was determined using 16S rRNA amplicon sequencing. Results: There was no significant correlation between alpha diversity and primary measures of short-term dietary intake (total daily calories, fat, fiber, fruit/vegetables, red meat intake, and fasting time). There was no evidence of clustering on beta diversity analyses. Very few taxonomic alterations were found for short-term dietary intake; an increased relative abundance of Neisseria oralis and Lautropia sp. was associated with high fruit and vegetable intake, and an increased relative abundance of a taxon in the family Gemellaceae was associated with increased red meat intake. Conclusions: Short-term dietary intake was associated with only minimal salivary microbiome alterations and does not appear to have a major impact on the potential use of the salivary microbiome as a biomarker for esophageal neoplasia. Full article
(This article belongs to the Special Issue Bacteria and Esophageal Cancer)
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14 pages, 9663 KiB  
Article
Differences in Gut Virome Related to Barrett Esophagus and Esophageal Adenocarcinoma
by Tianli Ma, Jinlong Ru, Jinling Xue, Sarah Schulz, Mohammadali Khan Mirzaei, Klaus-Peter Janssen, Michael Quante and Li Deng
Microorganisms 2021, 9(8), 1701; https://doi.org/10.3390/microorganisms9081701 - 10 Aug 2021
Cited by 10 | Viewed by 3579
Abstract
The relationship between viruses (dominated by bacteriophages or phages) and lower gastrointestinal (GI) tract diseases has been investigated, whereas the relationship between gut bacteriophages and upper GI tract diseases, such as esophageal diseases, which mainly include Barrett’s esophagus (BE) and esophageal adenocarcinoma (EAC), [...] Read more.
The relationship between viruses (dominated by bacteriophages or phages) and lower gastrointestinal (GI) tract diseases has been investigated, whereas the relationship between gut bacteriophages and upper GI tract diseases, such as esophageal diseases, which mainly include Barrett’s esophagus (BE) and esophageal adenocarcinoma (EAC), remains poorly described. This study aimed to reveal the gut bacteriophage community and their behavior in the progression of esophageal diseases. In total, we analyzed the gut phage community of sixteen samples from patients with esophageal diseases (six BE patients and four EAC patients) as well as six healthy controls. Differences were found in the community composition of abundant and rare bacteriophages among three groups. In addition, the auxiliary metabolic genes (AMGs) related to bacterial exotoxin and virulence factors such as lipopolysaccharides (LPS) biosynthesis proteins were found to be more abundant in the genome of rare phages from BE and EAC samples compared to the controls. These results suggest that the community composition of gut phages and functional traits encoded by them were different in two stages of esophageal diseases. However, the findings from this study need to be validated with larger sample sizes in the future. Full article
(This article belongs to the Special Issue Bacteria and Esophageal Cancer)
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Review

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16 pages, 765 KiB  
Review
3D Organoids: An Untapped Platform for Studying Host–Microbiome Interactions in Esophageal Cancers
by Samuel Flashner, Kelley S. Yan and Hiroshi Nakagawa
Microorganisms 2021, 9(11), 2182; https://doi.org/10.3390/microorganisms9112182 - 20 Oct 2021
Cited by 7 | Viewed by 3683
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 [...] Read more.
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. Full article
(This article belongs to the Special Issue Bacteria and Esophageal Cancer)
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19 pages, 4854 KiB  
Review
Challenges in Determining the Role of Microbiome Evolution in Barrett’s Esophagus and Progression to Esophageal Adenocarcinoma
by Caitlin Guccione, Rena Yadlapati, Shailja Shah, Rob Knight and Kit Curtius
Microorganisms 2021, 9(10), 2003; https://doi.org/10.3390/microorganisms9102003 - 22 Sep 2021
Cited by 5 | Viewed by 3991
Abstract
Esophageal adenocarcinoma (EAC) claims the lives of half of patients within the first year of diagnosis, and its incidence has rapidly increased since the 1970s despite extensive research into etiological factors. The changes in the microbiome within the distal esophagus in modern populations [...] Read more.
Esophageal adenocarcinoma (EAC) claims the lives of half of patients within the first year of diagnosis, and its incidence has rapidly increased since the 1970s despite extensive research into etiological factors. The changes in the microbiome within the distal esophagus in modern populations may help explain the growth in cases that other common EAC risk factors together cannot fully explain. The precursor to EAC is Barrett’s esophagus (BE), a metaplasia adapted to a reflux-mediated microenvironment that can be challenging to diagnose in patients who do not undergo endoscopic screening. Non-invasive procedures to detect microbial communities in saliva, oral swabs and brushings from the distal esophagus allow us to characterize taxonomic differences in bacterial population abundances within patients with BE versus controls, and may provide an alternative means of BE detection. Unique microbial communities have been identified across healthy esophagus, BE, and various stages of progression to EAC, but studies determining dynamic changes in these communities, including migration from proximal stomach and oral cavity niches, and their potential causal role in cancer formation are lacking. Helicobacter pylori is negatively associated with EAC, and the absence of this species has been implicated in the evolution of chromosomal instability, a main driver of EAC, but joint analyses of microbiome and host genomes are needed. Acknowledging technical challenges, future studies on the prediction of microbial dynamics and evolution within BE and the progression to EAC will require larger esophageal microbiome datasets, improved bioinformatics pipelines, and specialized mathematical models for analysis. Full article
(This article belongs to the Special Issue Bacteria and Esophageal Cancer)
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28 pages, 455 KiB  
Review
Microbiome and Cancers of the Esophagus: A Review
by Yukiko Yano, Arash Etemadi and Christian C. Abnet
Microorganisms 2021, 9(8), 1764; https://doi.org/10.3390/microorganisms9081764 - 18 Aug 2021
Cited by 19 | Viewed by 4232
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. [...] Read more.
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. Full article
(This article belongs to the Special Issue Bacteria and Esophageal Cancer)
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