Alterations in the oral and gut microbiome of colorectal cancer patients and association with host clinical factors

Abstract

Previous studies have suggested that gut microbiota plays a critical role in colorectal cancer (CRC). Although preliminary comparisons of the oral and gut microbiota between CRC and healthy control (HC) patients have been made, the association between microbiome abundance and host clinical factors has not been fully illustrated, especially oral health conditions. Matching samples of unstimulated saliva, cancer tissues or biopsies and stools were collected from 30 CRC and 30 HC patients from Shanghai Jiao Tong University affiliated Renji Hospital for 16S rRNA sequencing analysis. The diversity in salivary and mucosal microbiome, but not stool microbiome of CRC group, was significantly different from that of HC, as demonstrated by the Principal Component Analysis. Logistic regression analysis revealed that older age and higher oral hygiene index (OHI) were independent risk factors for CRC, with odds ratios and 95% confidence intervals of 1.159 (1.045‐1.284) and 4.398 (1.328‐14.567), respectively. Salivary Firmicutes to Bacteroides ratio in CRC was significantly higher than that in the HC group (P < .001), while the mucosal ratio was slightly decreased in CRC (P < .05). Salivary Rothia and Streptococcus levels were positively correlated with OHI, while Alloprevotella, Fusobacterium, Peptostreptoccus and Prevotella genera levels were negatively associated with OHI. NetShift analysis revealed that salivary Peptococcus, Centipeda and mucosal Subdoligranulum genus might act as key drivers during the process of carcinogenesis. In conclusion, the current study provides insights into the potential influence of host clinical factors on oral and gut microbiome composition and can be a guide for future studies.

Colorectal Cancer Patients Have Four Specific Bacterial Species in Oral and Gut Microbiota in Common—A Metagenomic Comparison with Healthy Subjects

“…However, our findings showed that F. nucleatum may or may not be derived from the oral cavity, depending on the subspecies and strain, and some may or may not affect CRC progression. Furthermore, oral hygiene tended to be worse in patients with CRC compared to that in controls in previous studies [23][24][25]. Similarly, we found poor oral hygiene in our cohort of patients with CRC.…”

The Tissue-Associated Microbiota in Colorectal Cancer: A Systematic Review

“…After assessing the full text of 112 studies, 73 studies were additionally excluded as not meeting the requirements: 19 evaluated only fecal microbiota; 14 did not include controls; 13 used 16S rRNA data from previously published studies; 10 had another outcome or study design; five analyzed specific bacterial species, four did not have CRC cases; four used colonoscopy aspirates or tissue swabs; two did not characterize the microbiota; and two presented animal data only. A total of 39 studies were included in the present systematic review [ 19 , 33 , 34 , 35 , 36 , 37 , 38 , 39 , 40 , 41 , 42 , 43 , 44 , 45 , 46 , 47 , 48 , 49 , 50 , 51 , 52 , 53 , 54 , 55 , 56 , 57 , 58 , 59 , 60 , 61 , 62 , 63 , 64 , 65 , 66 , 67 , 68 , 69 , 70 ]. The PRISMA flow-chart of the study inclusion process is shown in Figure 1 .…”

“…The tissue microbiota composition of CRC was compared with that of healthy controls in six studies [ 33 , 34 , 35 , 36 , 68 , 69 ] ( Table 1 ) and with that of non-cancerous colon tissue of CRC patients in 27 studies ( Table 2 ) [ 19 , 37 , 38 , 39 , 40 , 41 , 42 , 43 , 44 , 45 , 46 , 47 , 48 , 49 , 50 , 51 , 52 , 53 , 54 , 55 , 56 , 62 , 63 , 64 , 66 , 67 , 70 ]. Six studies included both comparisons [ 57 , 58 , 59 , 60 , 61 , 65 ].…”

“…All included studies used 16S rRNA gene sequencing for microbiome analysis, with the great majority targeting variable regions V3 and V4, alone or in combination with other regions, three targeting the V1–V2 regions [ 33 , 37 , 45 ], one targeting the V5-V6 regions [ 39 ], one targeting the V6 region [ 36 ], and two not reporting the target region [ 67 , 69 ]. The most frequently used sequencing platforms were Illumina MiSeq and 454 GS FLX (Roche).…”

Bacterial and Parasitic Pathogens as Risk Factors for Cancers in the Gastrointestinal Tract: A Review of Current Epidemiological Knowledge

“…Particularly, strains harboring the pks genomic island (pks + E. coli ) produce colibactin, which is subject of research in relation to CC during the last decade ( Faïs et al, 2018 ). Microbiome studies aiming at the identification of bacterial genera and abundance of bacterial species in the gut of CRC patients revealed a significantly reduced (relative) abundance of Escherichia in feces of CRC patients compared to healthy controls ( Sheng et al, 2019 ; Tang et al, 2020 ; Wang Y. et al, 2021 ). Supplementary Table 9 summarizes the results of 14 studies assessing the link between (mainly) oncogenic/cyclomodulin-producing E. coli and CRC ( Buc et al, 2013 ; Bonnet et al, 2014 ; Kohoutova et al, 2014 ; Fukugaiti et al, 2015 ; Xie et al, 2016 ; Shimpoh et al, 2017 ; Tsuchiya et al, 2018 ; Tunsjø et al, 2019 ; Zarei et al, 2019 ; Iyadorai et al, 2020 ; Pleguezuelos-Manzano et al, 2020 ; Rezasoltani et al, 2020 ; Tang et al, 2020 ; Yoshikawa et al, 2020 ).…”