Abstract
Aim: The gut microbiome plays a crucial role in colorectal cancer (CRC) tumorigenesis, but compositions of microorganisms have been inconsistent in previous studies due to the different types of specimens. We investigated the microbiomes and resistomes of CRC patients with colonic biopsy tissue and intestinal lavage fluid (IVF).Methods: Paired samples (biopsy tissue and IVF) were collected from 20 patients with CRC, and their gut microbiomes and resistomes were measured by shotgun metagenomics. Clinical and laboratory data were recorded. Bioinformatics (KneadData, Kraken2, and FMAP) and statistical analysis were done using the R (v4.0.2) software.Results: Bacterial diversity in IVF was higher than in tissue samples, and bacterial operational taxonomic units (OTUs) were 2,757 in IVF vs. 197 in tissue. β-diversity showed distinct clusters in paired samples. The predominant bacteria in IVF were phylum Proteobacteria, while the predominant bacteria of tissue were phylum Actinobacteria. Twenty-seven representative bacteria were selected to form six bacterial clusters, which showed only Firmicutes Cluster 1, and the Bacteroidetes Cluster 1 were significantly more abundant in the IVF group than those in the tissue group (p < 0.05). The Firmicutes Cluster 2, Bacteroidetes Cluster 2, Pathogen Cluster, and Prevotella Cluster were not significantly different between IVF and tissue (p > 0.05). Correlation analysis revealed that some bacteria could have effects on metabolic and inflammatory parameters of CRC patients. A total of 1,295 antibiotic resistance genes (ARGs) were detected in the gut microbiomes, which conferred multidrug resistance, as well as resistance to tetracycline, aminoglycoside, and more. Co-occurrence patterns revealed by the network showed mainly ARG-carrying bacteria to be similar between IVF and tissue, but leading bacteria located in the hub differed between IVF and tissue.Conclusion: Heterogeneity of microbiota is particularly evident when studied with IVF and tissue samples, but bacterial clusters that have close relationships with CRC carcinogenesis are not significantly different, using IVF as an alternative to tissue for gut microbiome, and resistome assessment may be a feasible method.
Highlights
Colorectal cancer (CRC) represents approximately 10% of the global cancer incidence, and is the third most diagnosed cancer (10.2% of total cases) and the second leading cause of cancer death (9.2% of total cases) worldwide (Vogelstein et al, 2013; Bray et al, 2018)
Our results suggested that the gut microbiome had higher bacterial diversity in Intestinal lavage fluid (IVF) than in tissue samples
To study the influence of bacteria or bacterial clusters on parameters reflecting patient disease characteristics, we identified the associations between bacteria genera and the following confounding factors: body mass index (BMI), metabolic parameters, including total bile acid (TBA), glucose, and lowdensity lipoprotein (LDL)/high-density lipoprotein (HDL), inflammatory parameters, including neutrophils, and tumor markers such as CA-19-9 and CEA
Summary
Colorectal cancer (CRC) represents approximately 10% of the global cancer incidence, and is the third most diagnosed cancer (10.2% of total cases) and the second leading cause of cancer death (9.2% of total cases) worldwide (Vogelstein et al, 2013; Bray et al, 2018). The gut microbiota or its metabolites is a key environmental factor influencing colon tumorigenesis, which is usually associated with altered microbial diversity, increased abundance of pathogenic microbes, or depletion of protective microbes (Wong and Yu, 2019). The intimate crosstalk between the gut microbial community and the epithelium layer of the host is a critical factor for cell proliferation and differentiation, gene expression in host epithelial cells, and regulation of inflammation (Hasegawa et al, 2007; Arthur et al, 2014). (Fn), Escherichia coli, Enterococcus faecalis, Streptococcus gallolyticus, and enterotoxigenic Bacteroides fragilis, are microorganisms that are closely associated with CRC carcinogenesis (Yoon et al, 2017). Characterization of the tumor microbiome is an essential step in unraveling the effects of bacteria on cancer hallmarks (Nejman et al, 2020)
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