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Dysbiotic microbiome variation in colorectal cancer patients is linked to lifestyles and metabolic diseases

BACKGROUND: Differences in the composition and diversity of the gut microbial communities among individuals are influenced by environmental factors. However, there is limited research on factors affecting microbiome variation in colorectal cancer patients, who display lower inter-individual variatio...

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Autores principales: Hoang, Tung, Kim, Minjung, Park, Ji Won, Jeong, Seung-Yong, Lee, Jeeyoo, Shin, Aesun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9883847/
https://www.ncbi.nlm.nih.gov/pubmed/36709262
http://dx.doi.org/10.1186/s12866-023-02771-7
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author Hoang, Tung
Kim, Minjung
Park, Ji Won
Jeong, Seung-Yong
Lee, Jeeyoo
Shin, Aesun
author_facet Hoang, Tung
Kim, Minjung
Park, Ji Won
Jeong, Seung-Yong
Lee, Jeeyoo
Shin, Aesun
author_sort Hoang, Tung
collection PubMed
description BACKGROUND: Differences in the composition and diversity of the gut microbial communities among individuals are influenced by environmental factors. However, there is limited research on factors affecting microbiome variation in colorectal cancer patients, who display lower inter-individual variations than that of healthy individuals. In this study, we examined the association between modifiable factors and the microbiome variation in colorectal cancer patients. METHODS: A total of 331 colorectal cancer patients who underwent resection surgery at the Department of Surgery, Seoul National University Hospital between October 2017 and August 2019 were included. Fecal samples from colorectal cancer patients were collected prior to the surgery. Variations in the gut microbiome among patients with different lifestyles and metabolic diseases were examined through the network analysis of inter-connected microbial abundance, the assessment of the Anna Karenina principle effect for microbial stochasticity, and the identification of the enriched bacteria using linear discrimination analysis effect size. Associations of dietary diversity with microbiome variation were investigated using the Procrustes analysis. RESULTS: We found stronger network connectivity of microbial communities in non-smokers, non-drinkers, obese individuals, hypertensive subjects, and individuals without diabetes than in their counterparts. The Anna Karenina principle effect was found for history of smoking, alcohol consumption, and diabetes (with significantly greater intra-sample similarity index), whereas obesity and hypertension showed the anti-Anna Karenina principle effect (with significantly lower intra-sample similarity index). We found certain bacterial taxa to be significantly enriched in patients of different categories of lifestyles and metabolic diseases using linear discrimination analysis. Diversity of food and nutrient intake did not shape the microbial diversity between individuals (p(Procrustes)>0.05). CONCLUSIONS: Our findings suggested an immune dysregulation and a reduced ability of the host and its microbiome in regulating the community composition. History of smoking, alcohol consumption, and diabetes were shown to affect partial individuals in shifting new microbial communities, whereas obesity and history of hypertension appeared to affect majority of individuals and shifted to drastic reductions in microbial compositions. Understanding the contribution of modifiable factors to microbial stochasticity may provide insights into how the microbiome regulates effects of these factors on the health outcomes of colorectal cancer patients. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-023-02771-7.
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spelling pubmed-98838472023-01-29 Dysbiotic microbiome variation in colorectal cancer patients is linked to lifestyles and metabolic diseases Hoang, Tung Kim, Minjung Park, Ji Won Jeong, Seung-Yong Lee, Jeeyoo Shin, Aesun BMC Microbiol Research BACKGROUND: Differences in the composition and diversity of the gut microbial communities among individuals are influenced by environmental factors. However, there is limited research on factors affecting microbiome variation in colorectal cancer patients, who display lower inter-individual variations than that of healthy individuals. In this study, we examined the association between modifiable factors and the microbiome variation in colorectal cancer patients. METHODS: A total of 331 colorectal cancer patients who underwent resection surgery at the Department of Surgery, Seoul National University Hospital between October 2017 and August 2019 were included. Fecal samples from colorectal cancer patients were collected prior to the surgery. Variations in the gut microbiome among patients with different lifestyles and metabolic diseases were examined through the network analysis of inter-connected microbial abundance, the assessment of the Anna Karenina principle effect for microbial stochasticity, and the identification of the enriched bacteria using linear discrimination analysis effect size. Associations of dietary diversity with microbiome variation were investigated using the Procrustes analysis. RESULTS: We found stronger network connectivity of microbial communities in non-smokers, non-drinkers, obese individuals, hypertensive subjects, and individuals without diabetes than in their counterparts. The Anna Karenina principle effect was found for history of smoking, alcohol consumption, and diabetes (with significantly greater intra-sample similarity index), whereas obesity and hypertension showed the anti-Anna Karenina principle effect (with significantly lower intra-sample similarity index). We found certain bacterial taxa to be significantly enriched in patients of different categories of lifestyles and metabolic diseases using linear discrimination analysis. Diversity of food and nutrient intake did not shape the microbial diversity between individuals (p(Procrustes)>0.05). CONCLUSIONS: Our findings suggested an immune dysregulation and a reduced ability of the host and its microbiome in regulating the community composition. History of smoking, alcohol consumption, and diabetes were shown to affect partial individuals in shifting new microbial communities, whereas obesity and history of hypertension appeared to affect majority of individuals and shifted to drastic reductions in microbial compositions. Understanding the contribution of modifiable factors to microbial stochasticity may provide insights into how the microbiome regulates effects of these factors on the health outcomes of colorectal cancer patients. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-023-02771-7. BioMed Central 2023-01-28 /pmc/articles/PMC9883847/ /pubmed/36709262 http://dx.doi.org/10.1186/s12866-023-02771-7 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Hoang, Tung
Kim, Minjung
Park, Ji Won
Jeong, Seung-Yong
Lee, Jeeyoo
Shin, Aesun
Dysbiotic microbiome variation in colorectal cancer patients is linked to lifestyles and metabolic diseases
title Dysbiotic microbiome variation in colorectal cancer patients is linked to lifestyles and metabolic diseases
title_full Dysbiotic microbiome variation in colorectal cancer patients is linked to lifestyles and metabolic diseases
title_fullStr Dysbiotic microbiome variation in colorectal cancer patients is linked to lifestyles and metabolic diseases
title_full_unstemmed Dysbiotic microbiome variation in colorectal cancer patients is linked to lifestyles and metabolic diseases
title_short Dysbiotic microbiome variation in colorectal cancer patients is linked to lifestyles and metabolic diseases
title_sort dysbiotic microbiome variation in colorectal cancer patients is linked to lifestyles and metabolic diseases
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9883847/
https://www.ncbi.nlm.nih.gov/pubmed/36709262
http://dx.doi.org/10.1186/s12866-023-02771-7
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