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Association of oral microbiota with lung cancer risk in a low-income population in the Southeastern USA

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Abstract

Purpose

Oral microbiome plays an important role in oral health and systemic diseases, including cancer. We aimed to prospectively investigate the association of oral microbiome with lung cancer risk.

Methods

We analyzed 156 incident lung cancer cases (73 European Americans and 83 African Americans) and 156 individually matched controls nested within the Southern Community Cohort Study. Oral microbiota were assessed using 16S rRNA gene sequencing in pre-diagnostic mouth rinse samples. Paired t test and the permutational multivariate analysis of variance test were used to evaluate lung cancer risk association with alpha diversity or beta diversity, respectively. Conditional logistic regression models were used to evaluate the association of individual bacterial abundance or prevalence with lung cancer risk.

Results

No significant differences were observed for alpha or beta diversity between lung cancer cases and controls. Abundance of families Lachnospiraceae_[XIV], Peptostreptococcaceae_[XI], and Erysipelotrichaceae and species Parvimonas micra was associated with decreased lung cancer risk, with odds ratios (ORs) and 95% confidence intervals (CIs) of 0.76 (0.59–0.98), 0.80 (0.66–0.97), 0.81 (0.67–0.99), and 0.83 (0.71–0.98), respectively (all p < 0.05). Prevalence of five pre-defined oral pathogens were not significantly associated with overall lung cancer risk. Prevalence of genus Bacteroidetes_[G-5] and species Alloprevotella sp._oral_taxon_912, Capnocytophaga sputigena, Lactococcus lactis, Peptoniphilaceae_[G-1] sp._oral_taxon_113, Leptotrichia sp._oral_taxon_225, and Fretibacterium fastidiosum was associated with decreased lung cancer risk, with ORs and 95% CIs of 0.55 (0.30–1.00), 0.36 (0.17–0.73), 0.53 (0.31–0.92), 0.43 (0.21–0.88), 0.43 (0.19–0.94), 0.57 (0.34–0.99), and 0.54 (0.31–0.94), respectively (all p < 0.05). Species L. sp._oral_taxon_225 was significantly associated with decreased lung cancer risk in African Americans (OR [95% CIs] 0.28 [0.12–0.66]; p = 0.00012).

Conclusion

Results from this study suggest that oral microbiota may play a role in the development of lung cancer.

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Data availability

Data and statistical codes used in the present study can be requested through the SCCS Online request System (https://ors.southerncommunitystudy.org).

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Acknowledgments

The authors wish to thank all individuals who took part in the study and all researchers, clinicians, technicians, and administrative staff who enabled this work to be carried out. We thank Dr. Mary Shannon Byers for assistance with manuscript preparation.

Funding

This study was supported by the National Institutes of Health (R01CA207466, R01CA92447, U01CA202979, and U54CA163072). Sample preparation was conducted at the Survey and Biospecimen Shared Resources, which is supported in part by the Vanderbilt-Ingram Cancer Center (P30 CA68485). The 16S rRNA gene sequencing was performed at the VANderbilt Technologies for Advanced Genomics (VANTAGE) Core, which is partly supported by NIH/NCRR grant G20 RR030956. The data analyses were conducted using the Advanced Computing Center for Research and Education (ACCRE) at Vanderbilt University, which is supported in part by the National Institutes of Health S10 Shared Instrumentation (1S10OD023680). The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Authors and Affiliations

  1. Division of Epidemiology, Department of Medicine, Vanderbilt Epidemiology Center, Vanderbilt-Ingram Cancer Center, Vanderbilt University School of Medicine, 1161 21st Avenue South, Nashville, TN, USA

    Jiajun Shi, Yaohua Yang, Jie Wu, Jirong Long, Regina Courtney, Xiao-Ou Shu, Wei Zheng, William J. Blot & Qiuyin Cai

  2. School of Dentistry, Meharry Medical College, Nashville, TN, USA

    Hua Xie

  3. Department of Biological Sciences, Tennessee State University, Nashville, TN, 37232, USA

    Xiaofei Wang

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  1. Jiajun Shi
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Contributions

WZ, WJB, and QC conceived the study. JS, YY, and JL analyzed the data and drafted the manuscript. HX, XW, JW, RC, XOS, WZ, WJB, and QC contributed resources, collected, and processed samples. All the authors edited and approved the final draft.

Corresponding author

Correspondence to Qiuyin Cai.

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The authors have declared no conflicts of interest.

Ethical approval

The Southern Community Cohort Study was reviewed and approved by the institutional review boards at Vanderbilt University and Meharry Medical College.

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Written informed consent was obtained from all individuals, and the research was performed by the principles of the Helsinki Declaration.

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All study participants provided written informed consent for the publication of any data and associated images.

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Shi, J., Yang, Y., Xie, H. et al. Association of oral microbiota with lung cancer risk in a low-income population in the Southeastern USA. Cancer Causes Control 32, 1423–1432 (2021). https://doi.org/10.1007/s10552-021-01490-6

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