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Abstract
Oral cancers are attributed to a number of causal agents including tobacco, alcohol, human papillomavirus (HPV), and areca (betel) nut. Although betel nut chewing has been established as an independent cause of oral cancer, the mechanisms of carcinogenesis are poorly understood. An investigation was undertaken to evaluate the influence of betel nut chewing on the oral microbiome and oral premalignant lesions. Study participants were recruited from a dental clinic in Guam. Structured interviews and oral examinations were performed. Oral swabbing and saliva samples were evaluated by 454 pyrosequencing of the V3- V5 region of the 16S rRNA bacterial gene and genotyped for HPV. One hundred twenty-two adults were enrolled including 64 current betel nut chewers, 37 former chewers, and 21 with no history of betel nut use. Oral premalignant lesions, including leukoplakia and submucous fibrosis, were observed in 10 chewers. Within-sample bacterial diversity was significantly lower in long-term (≥10 years) chewers vs. never chewers and in current chewers with oral lesions vs. individuals without lesions. Between-sample bacterial diversity based on Unifrac distances significantly differed by chewing status and oral lesion status. Current chewers had significantly elevated levels of Streptococcus infantis and higher and lower levels of distinct taxa of the Actinomyces and Streptococcus genera. Long-term chewers had reduced levels of Parascardovia and Streptococcus. Chewers with oral lesions had significantly elevated levels of Oribacterium, Actinomyces, and Streptococcus, including Streptococcus anginosus. In multivariate analyses, controlling for smoking, oral HPV, S.anginosus, and S. infantis levels, current betel nut chewing remained the only predictor of oral premalignant lesions. Our study provides evidence that betel nut chewing alters the oral bacterial microbiome including that of chewers who develop oral premalignant lesions. Nonetheless, whether microbial changes are involved in betel nut-induced oral carcinogenesis is only speculative. Further research is needed to discern the clinical significance of an altered oral microbiome and the mechanisms of oral cancer development in betel nut chewers.
Highlights
Oral cancers, comprising tumors of the oral cavity and oropharynx, are among the most common malignancies worldwide.[1]
In multivariate models which included oral Human papillomavirus (HPV) and levels of S. anginosus and S. infantis as covariates, current betel nut chewing remained the only predictor of oral premalignant lesions
Our study provides evidence that betel nut chewing alters the oral bacterial microbiome
Summary
Oral cancers, comprising tumors of the oral cavity and oropharynx, are among the most common malignancies worldwide.[1]. [2] Chewing of betel nut, which comes from the Areca catechu palm tree, is practiced by 10%20% of the world’s population with the highest prevalence of use in South and Southeastern Asia and the Pacific.[2, 5] Worldwide, the highest incidence of oral cavity tumors is found in Melanesia, including Papua New Guinea and the Solomon Islands, where betel nut chewing is widely used.[1, 2, 6] In Guam, a U.S territory in the western Pacific where betel nut chewing is prevalent [7], oral cancer mortality rates among the native Chamorro population are six times higher than that of the U.S.[8] Areca (betel) nut chewing is a leading cause of oral cancer in parts of Asia and the Pacific. [2] Chewing of betel nut, which comes from the Areca catechu palm tree, is practiced by 10%20% of the world’s population with the highest prevalence of use in South and Southeastern Asia and the Pacific.[2, 5] Worldwide, the highest incidence of oral cavity tumors is found in Melanesia, including Papua New Guinea and the Solomon Islands, where betel nut chewing is widely used.[1, 2, 6] In Guam, a U.S territory in the western Pacific where betel nut chewing is prevalent [7], oral cancer mortality rates among the native Chamorro population are six times higher than that of the U.S.[8]
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