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The Potential of Colonic Tumor Tissue Fusobacterium nucleatum to Predict Staging and Its Interplay with Oral Abundance in Colon Cancer Patients

SIMPLE SUMMARY: Colon cancer (CC) is a multifactorial disease, and complex interactions among the gut microbiota, inflammation and environmental exposures are needed for colorectal carcinogenesis. Oral Fusobacterium nucleatum (Fn) and Porphyromonas gingivalis (Pg) are predominant pathogens involved...

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Autores principales: Pignatelli, Pamela, Iezzi, Lorena, Pennese, Martina, Raimondi, Paolo, Cichella, Anna, Bondi, Danilo, Grande, Rossella, Cotellese, Roberto, Di Bartolomeo, Nicola, Innocenti, Paolo, Piattelli, Adriano, Curia, Maria Cristina
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7957509/
https://www.ncbi.nlm.nih.gov/pubmed/33804585
http://dx.doi.org/10.3390/cancers13051032
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author Pignatelli, Pamela
Iezzi, Lorena
Pennese, Martina
Raimondi, Paolo
Cichella, Anna
Bondi, Danilo
Grande, Rossella
Cotellese, Roberto
Di Bartolomeo, Nicola
Innocenti, Paolo
Piattelli, Adriano
Curia, Maria Cristina
author_facet Pignatelli, Pamela
Iezzi, Lorena
Pennese, Martina
Raimondi, Paolo
Cichella, Anna
Bondi, Danilo
Grande, Rossella
Cotellese, Roberto
Di Bartolomeo, Nicola
Innocenti, Paolo
Piattelli, Adriano
Curia, Maria Cristina
author_sort Pignatelli, Pamela
collection PubMed
description SIMPLE SUMMARY: Colon cancer (CC) is a multifactorial disease, and complex interactions among the gut microbiota, inflammation and environmental exposures are needed for colorectal carcinogenesis. Oral Fusobacterium nucleatum (Fn) and Porphyromonas gingivalis (Pg) are predominant pathogens involved in periodontitis and can migrate from the oral cavity to other districts of the body, including the colon. The aim of the study was to analyze the link between oral Fn and Pg, oral health, diet, lifestyle and risk of CC. The Fn quantity was greater in the oral cavity than in CC, and its concentration influenced the Fn quantity in CC tissue. The meat consumption was related to intestinal Fn. Instead, Pg was not associated with CC. The Fn abundance in CC tissue could predict cancer staging, becoming a potential biomarker to find out the prognosis of colic cancer patients. ABSTRACT: Background. Intestinal microbiota dysbiosis may enhance the carcinogenicity of colon cancer (CC) by the proliferation and differentiation of epithelial cells. Oral Fusobacterium nucleatum (Fn) and Porphyromonas gingivalis (Pg) have the ability to invade the gut epithelium, promoting tumor progression. The aim of the study was to assess whether the abundance of these odontopathogenic bacteria was associated with colon cancer. We also investigated how lifestyle factors could influence the oral Fn and Pg abundance and CC. Methods. Thirty-six CC patients were included in the study to assess the Pg and Fn oral and colon tissue abundance by qPCR. Oral health data, food habits and lifestyles were also recorded. Results. Patients had a greater quantity of Fn in the oral cavity than matched CC and adjacent non-neoplastic mucosa (adj t) tissues (p = 0.004 and p < 0.001). Instead, Pg was not significantly detected in colonic tissues. There was an association between the Fn quantity in the oral and CC tissue and a statistically significant relation between the Fn abundance in adenocarcinoma (ADK) and staging (p = 0.016). The statistical analysis revealed a tendency towards a greater Fn quantity in CC (p = 0.073, η(2)(p) = 0.12) for high-meat consumers. Conclusion. In our study, Pg was absent in colon tissues but was correlated with the oral inflammation gingival and plaque indices. For the first time, there was evidence that the Fn oral concentration can influence colon tissue concentrations and predict CC prognosis.
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spelling pubmed-79575092021-03-16 The Potential of Colonic Tumor Tissue Fusobacterium nucleatum to Predict Staging and Its Interplay with Oral Abundance in Colon Cancer Patients Pignatelli, Pamela Iezzi, Lorena Pennese, Martina Raimondi, Paolo Cichella, Anna Bondi, Danilo Grande, Rossella Cotellese, Roberto Di Bartolomeo, Nicola Innocenti, Paolo Piattelli, Adriano Curia, Maria Cristina Cancers (Basel) Article SIMPLE SUMMARY: Colon cancer (CC) is a multifactorial disease, and complex interactions among the gut microbiota, inflammation and environmental exposures are needed for colorectal carcinogenesis. Oral Fusobacterium nucleatum (Fn) and Porphyromonas gingivalis (Pg) are predominant pathogens involved in periodontitis and can migrate from the oral cavity to other districts of the body, including the colon. The aim of the study was to analyze the link between oral Fn and Pg, oral health, diet, lifestyle and risk of CC. The Fn quantity was greater in the oral cavity than in CC, and its concentration influenced the Fn quantity in CC tissue. The meat consumption was related to intestinal Fn. Instead, Pg was not associated with CC. The Fn abundance in CC tissue could predict cancer staging, becoming a potential biomarker to find out the prognosis of colic cancer patients. ABSTRACT: Background. Intestinal microbiota dysbiosis may enhance the carcinogenicity of colon cancer (CC) by the proliferation and differentiation of epithelial cells. Oral Fusobacterium nucleatum (Fn) and Porphyromonas gingivalis (Pg) have the ability to invade the gut epithelium, promoting tumor progression. The aim of the study was to assess whether the abundance of these odontopathogenic bacteria was associated with colon cancer. We also investigated how lifestyle factors could influence the oral Fn and Pg abundance and CC. Methods. Thirty-six CC patients were included in the study to assess the Pg and Fn oral and colon tissue abundance by qPCR. Oral health data, food habits and lifestyles were also recorded. Results. Patients had a greater quantity of Fn in the oral cavity than matched CC and adjacent non-neoplastic mucosa (adj t) tissues (p = 0.004 and p < 0.001). Instead, Pg was not significantly detected in colonic tissues. There was an association between the Fn quantity in the oral and CC tissue and a statistically significant relation between the Fn abundance in adenocarcinoma (ADK) and staging (p = 0.016). The statistical analysis revealed a tendency towards a greater Fn quantity in CC (p = 0.073, η(2)(p) = 0.12) for high-meat consumers. Conclusion. In our study, Pg was absent in colon tissues but was correlated with the oral inflammation gingival and plaque indices. For the first time, there was evidence that the Fn oral concentration can influence colon tissue concentrations and predict CC prognosis. MDPI 2021-03-01 /pmc/articles/PMC7957509/ /pubmed/33804585 http://dx.doi.org/10.3390/cancers13051032 Text en © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Pignatelli, Pamela
Iezzi, Lorena
Pennese, Martina
Raimondi, Paolo
Cichella, Anna
Bondi, Danilo
Grande, Rossella
Cotellese, Roberto
Di Bartolomeo, Nicola
Innocenti, Paolo
Piattelli, Adriano
Curia, Maria Cristina
The Potential of Colonic Tumor Tissue Fusobacterium nucleatum to Predict Staging and Its Interplay with Oral Abundance in Colon Cancer Patients
title The Potential of Colonic Tumor Tissue Fusobacterium nucleatum to Predict Staging and Its Interplay with Oral Abundance in Colon Cancer Patients
title_full The Potential of Colonic Tumor Tissue Fusobacterium nucleatum to Predict Staging and Its Interplay with Oral Abundance in Colon Cancer Patients
title_fullStr The Potential of Colonic Tumor Tissue Fusobacterium nucleatum to Predict Staging and Its Interplay with Oral Abundance in Colon Cancer Patients
title_full_unstemmed The Potential of Colonic Tumor Tissue Fusobacterium nucleatum to Predict Staging and Its Interplay with Oral Abundance in Colon Cancer Patients
title_short The Potential of Colonic Tumor Tissue Fusobacterium nucleatum to Predict Staging and Its Interplay with Oral Abundance in Colon Cancer Patients
title_sort potential of colonic tumor tissue fusobacterium nucleatum to predict staging and its interplay with oral abundance in colon cancer patients
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7957509/
https://www.ncbi.nlm.nih.gov/pubmed/33804585
http://dx.doi.org/10.3390/cancers13051032
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