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J Cancer 2022; 13(4):1168-1180. doi:10.7150/jca.67068 This issue Cite

Research Paper

Influence of Oral Intaking Habit on Tongue Coating Microbiota in Patients with Esophageal Precancerous Lesions

Pan Xiao¹, Zhaolai Hua², Xiaoyu Kang¹, Bin Lu³, Meifeng Li¹, Juan Wu¹, Wei Dong¹, Junfeng Zhang^1✉, Chun Cheng^1✉

1. School of Medicine & Holistic Integrative Medicine, Nanjing University of Chinese Medicine, Nanjing 210023, Jiangsu, China
2. Yangzhong Cancer Institute, Yangzhong People's Hospital, Jiangsu Yangzhong 212200, China
3. Department of Oncology, Yangzhong People's Hospital, Yangzhong 212200, Jiangsu, China

✉ Corresponding authors: Junfeng Zhang and Chun Cheng; Department of Immunology, School of Medicine & Holistic Integrative Medicine, Nanjing University of Chinese Medicine, 138 Xianlin Avenue, Mail Box 21, Nanjing, Jiangsu 210023, P.R. China. Email: zhangjunfeng419edu.cn (J Zhang), cchengedu.cn (C Cheng). More

Abstract

Background: Esophageal cancer (EC) is a common digestive tract tumor in China, and oral intaking habit has a great influence on the development of EC. The present study explored the correlation between oral intaking habit and tongue coating (TC) microbiota in patients with esophageal precancerous lesions (EPL) to provide a reasonable interpretation of the influence of oral intaking habit on microbial alterations in the EPL.

Methods: A case-control study was designed with 123 EPL patients and 176 volunteers with mild esophagitis, and they were well matched using sex, age, and body mass index. The TC microbiota was profiled using high-throughput sequencing of the V3-V4 region of the 16S rRNA gene, and the serum levels of total bile acid (TBA) and interleukin-17α (IL-17α) were measured using enzyme-linked immunosorbent assay. Alpha diversity, community structure, and linear discriminant analysis were conducted, and Spearman correlation analysis was used to build the symbiotic network.

Results: No significant differences were observed in the diversity and richness of the TC microbiota between the cases and controls (P > 0.05). TC Peptostreptococcus and Capnocytophaga were enriched in EPL patients. Stratified analysis showed that TC microbial composition was affected by both EPL and oral intaking habit; for example, Atopobium and Actinomyces were positively related to oral intaking habit scores in both the cases and controls, while Simonsiella was negatively correlated with oral intaking habit status in cases but positively correlated with oral intaking habit status in controls. Although serum TBA and IL-17α were not associated with EPL (P > 0.05), the daily-drinking cases had a higher level of serum TBA than the nondrinking cases (P < 0.05), and Helicobacter pylori (Hp) negative controls had a higher level of serum TBA than the Hp-positive controls (P < 0.05). The symbiotic networks were comprised of 71 significant correlations in the controls and 52 significant correlations in the cases.

Conclusions: The development of EPL changed the TC microbiota and decreased the symbiotic complexity of the TC bacteria, which were also influenced by the cancer-related oral intaking habit. Bile acid may be a key factor mediating changes in TC microbiota.

Keywords: esophageal precancerous lesions, tongue coating, microbiota, oral intaking habit, bile acid

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