Characterization of the Oral and Esophageal Microbiota in Esophageal Precancerous Lesions and Squamous Cell Carcinoma

Overview

Journal Front Cell Infect Microbiol

Specialties Cell Biology
Infectious Diseases
Microbiology

Date 2021 Oct 4

PMID 34604107

Citations 17

Authors

Zhengqi Li

Lizhou Dou

Yueming Zhang

Shun He

Deli Zhao

Changqing Hao

Guohui Song

Wei Zhang

Yong Liu

Guiqi Wang

Affiliations

Soon will be listed here.

Abstract

Important evidence indicates that the microbiota plays a key role in esophageal squamous cell carcinoma (ESCC). Here, paired saliva and brush specimens were obtained from 276 participants undergoing upper gastrointestinal endoscopic examination before or during screening for upper gastrointestinal (UGI) cancer. The esophageal microbiota was investigated by 16S rRNA gene profiling and next-generation sequencing. We observed that as the disease progressed, the α diversity in the saliva and cell brush samples decreased. Linear discriminant analysis effect size (LEfSe) results showed that in both the saliva and cell brush specimens, , and were common biomarkers in patients with low-grade dysplasia, was a common biomarker in patients with high-grade dysplasia, and , , and were common biomarkers in patients with esophageal cancer. The top 3 genera in the saliva and cell brush specimens had areas under the curve (AUCs) of 87.16 and 89.13%, respectively, to distinguish ESCC patients from normal people. The PICRUSt2 results identified in brush samples that patients with ESCC had decreased nitrate reductase functions. Our results suggest that future studies can focus on the function of the characteristic bacteria in ESCC.

Citing Articles

From microbes to medicine: harnessing the power of the microbiome in esophageal cancer.

Liu X, Li B, Liang L, Han J, Mai S, Liu L Front Immunol. 2024; 15:1450927.

PMID: 39600698 PMC: 11588724. DOI: 10.3389/fimmu.2024.1450927.

Microbiome of esophageal endoscopic wash samples is associated with resident flora in the esophagus and incidence of cancer.

Shijimaya T, Tahara T, Yamazaki J, Kobayashi S, Matsumoto Y, Nakamura N Sci Rep. 2024; 14(1):19525.

PMID: 39174555 PMC: 11341785. DOI: 10.1038/s41598-024-67410-1.

A powerful machine learning approach to identify interactions of differentially abundant gut microbial subsets in patients with metastatic and non-metastatic pancreatic cancer.

Villani A, Fontana A, Panebianco C, Ferro C, Copetti M, Pavlovic R Gut Microbes. 2024; 16(1):2375483.

PMID: 38972056 PMC: 11229760. DOI: 10.1080/19490976.2024.2375483.

Non-invasive early detection on esophageal squamous cell carcinoma and precancerous lesions by microbial biomarkers combining epidemiological factors in China.

Li M, Shao D, Fan Z, Qin J, Xu J, Huang Q J Gastroenterol. 2024; 59(7):531-542.

PMID: 38819499 DOI: 10.1007/s00535-024-02117-8.

Salivary microbiome is associated with the response to chemoradiotherapy in initially inoperable patients with esophageal squamous cell carcinoma.

He Y, Li X, Hu A, Qian D J Oral Microbiol. 2024; 16(1):2359887.

PMID: 38813524 PMC: 11134033. DOI: 10.1080/20002297.2024.2359887.

References

Yamamura K, Izumi D, Kandimalla R, Sonohara F, Baba Y, Yoshida N . Intratumoral Levels Predict Therapeutic Response to Neoadjuvant Chemotherapy in Esophageal Squamous Cell Carcinoma. Clin Cancer Res. 2019; 25(20):6170-6179. PMC: 6801075. DOI: 10.1158/1078-0432.CCR-19-0318. View

Zhao Q, Yang T, Yan Y, Zhang Y, Li Z, Wang Y . Alterations of Oral Microbiota in Chinese Patients With Esophageal Cancer. Front Cell Infect Microbiol. 2020; 10:541144. PMC: 7609410. DOI: 10.3389/fcimb.2020.541144. View

Codipilly D, Qin Y, Dawsey S, Kisiel J, Topazian M, Ahlquist D . Screening for esophageal squamous cell carcinoma: recent advances. Gastrointest Endosc. 2018; 88(3):413-426. PMC: 7493990. DOI: 10.1016/j.gie.2018.04.2352. View

Li M, Shao D, Zhou J, Gu J, Qin J, Chen W . Signatures within esophageal microbiota with progression of esophageal squamous cell carcinoma. Chin J Cancer Res. 2021; 32(6):755-767. PMC: 7797230. DOI: 10.21147/j.issn.1000-9604.2020.06.09. View

Yang W, Chen C, Jia M, Xing X, Gao L, Tsai H . Tumor-Associated Microbiota in Esophageal Squamous Cell Carcinoma. Front Cell Dev Biol. 2021; 9:641270. PMC: 7930383. DOI: 10.3389/fcell.2021.641270. View

Ju F, Zhang T . 16S rRNA gene high-throughput sequencing data mining of microbial diversity and interactions. Appl Microbiol Biotechnol. 2015; 99(10):4119-29. DOI: 10.1007/s00253-015-6536-y. View

Fillon S, Harris J, Wagner B, Kelly C, Stevens M, Moore W . Novel device to sample the esophageal microbiome--the esophageal string test. PLoS One. 2012; 7(9):e42938. PMC: 3434161. DOI: 10.1371/journal.pone.0042938. View

Dong L, Yin J, Zhao J, Ma S, Wang H, Wang M . Microbial Similarity and Preference for Specific Sites in Healthy Oral Cavity and Esophagus. Front Microbiol. 2018; 9:1603. PMC: 6056649. DOI: 10.3389/fmicb.2018.01603. View

Nagtegaal I, Odze R, Klimstra D, Paradis V, Rugge M, Schirmacher P . The 2019 WHO classification of tumours of the digestive system. Histopathology. 2019; 76(2):182-188. PMC: 7003895. DOI: 10.1111/his.13975. View

10.

Liu A, Vogtmann E, Shao D, Abnet C, Dou H, Qin Y . A Comparison of Biopsy and Mucosal Swab Specimens for Examining the Microbiota of Upper Gastrointestinal Carcinoma. Cancer Epidemiol Biomarkers Prev. 2019; 28(12):2030-2037. PMC: 7294753. DOI: 10.1158/1055-9965.EPI-18-1210. View

11.

Liu Y, Lin Z, Lin Y, Chen Y, Peng X, He F . Streptococcus and Prevotella are associated with the prognosis of oesophageal squamous cell carcinoma. J Med Microbiol. 2018; 67(8):1058-1068. DOI: 10.1099/jmm.0.000754. View

12.

Di Pilato V, Freschi G, Ringressi M, Pallecchi L, Rossolini G, Bechi P . The esophageal microbiota in health and disease. Ann N Y Acad Sci. 2016; 1381(1):21-33. DOI: 10.1111/nyas.13127. View

13.

Peters B, Wu J, Pei Z, Yang L, Purdue M, Freedman N . Oral Microbiome Composition Reflects Prospective Risk for Esophageal Cancers. Cancer Res. 2017; 77(23):6777-6787. PMC: 5726431. DOI: 10.1158/0008-5472.CAN-17-1296. View

14.

Liu F, Liu M, Liu Y, Guo C, Zhou Y, Li F . Oral microbiome and risk of malignant esophageal lesions in a high-risk area of China: A nested case-control study. Chin J Cancer Res. 2021; 32(6):742-754. PMC: 7797237. DOI: 10.21147/j.issn.1000-9604.2020.06.07. View

15.

Okereke I, Hamilton C, Wenholz A, Jala V, Giang T, Reynolds S . Associations of the microbiome and esophageal disease. J Thorac Dis. 2019; 11(Suppl 12):S1588-S1593. PMC: 6702393. DOI: 10.21037/jtd.2019.05.82. View

16.

Douglas G, Maffei V, Zaneveld J, Yurgel S, Brown J, Taylor C . PICRUSt2 for prediction of metagenome functions. Nat Biotechnol. 2020; 38(6):685-688. PMC: 7365738. DOI: 10.1038/s41587-020-0548-6. View

17.

Abnet C, Arnold M, Wei W . Epidemiology of Esophageal Squamous Cell Carcinoma. Gastroenterology. 2017; 154(2):360-373. PMC: 5836473. DOI: 10.1053/j.gastro.2017.08.023. View

18.

Chen R, Liu Y, Song G, Li B, Zhao D, Hua Z . Effectiveness of one-time endoscopic screening programme in prevention of upper gastrointestinal cancer in China: a multicentre population-based cohort study. Gut. 2020; 70(2):251-260. PMC: 7815635. DOI: 10.1136/gutjnl-2019-320200. View

19.

Zhang L, Wang S . Bacterial community diversity on in-shell walnut surfaces from six representative provinces in China. Sci Rep. 2017; 7(1):10054. PMC: 5577159. DOI: 10.1038/s41598-017-10138-y. View

20.

Wang Q, Rao Y, Guo X, Liu N, Liu S, Wen P . Oral Microbiome in Patients with Oesophageal Squamous Cell Carcinoma. Sci Rep. 2019; 9(1):19055. PMC: 6910992. DOI: 10.1038/s41598-019-55667-w. View