Oral fungal profiling and risk of nasopharyngeal carcinoma: a population-based case-control studyResearch in context

Summary: Background: Dysbiosis of the oral mycobiome has been linked to some diseases, including cancers. However, the role of oral fungal communities in nasopharyngeal carcinoma (NPC) carcinogenesis has not previously been investigated. Methods: We characterized the oral salivary fungal mycobiome...

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Main Authors: Yufeng Chen, Wanxin Li, Ellen T. Chang, Justine W. Debelius, Lokeshwaran Manoharan, Yuming Zheng, Yancheng Li, Guangwu Huang, Hans-Olov Adami, Rob Knight, Yonglin Cai, Zhe Zhang, Weimin Ye
Format: Article
Language:English
Published: Elsevier 2023-10-01
Series:EBioMedicine
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Online Access:http://www.sciencedirect.com/science/article/pii/S2352396423003791
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author Yufeng Chen
Wanxin Li
Ellen T. Chang
Justine W. Debelius
Lokeshwaran Manoharan
Yuming Zheng
Yancheng Li
Guangwu Huang
Hans-Olov Adami
Rob Knight
Yonglin Cai
Zhe Zhang
Weimin Ye
author_facet Yufeng Chen
Wanxin Li
Ellen T. Chang
Justine W. Debelius
Lokeshwaran Manoharan
Yuming Zheng
Yancheng Li
Guangwu Huang
Hans-Olov Adami
Rob Knight
Yonglin Cai
Zhe Zhang
Weimin Ye
author_sort Yufeng Chen
collection DOAJ
description Summary: Background: Dysbiosis of the oral mycobiome has been linked to some diseases, including cancers. However, the role of oral fungal communities in nasopharyngeal carcinoma (NPC) carcinogenesis has not previously been investigated. Methods: We characterized the oral salivary fungal mycobiome in 476 untreated incident NPC patients and 537 population-based controls using fungal internal transcribed spacer (ITS)-2 sequencing. The relationship between oral fungal mycobiome and the risk of NPC was assessed through bioinformatic and biostatistical analyses. Findings: We found that lower fungal alpha diversity was associated with an increased odds of NPC [lower vs. higher: observed features (adjusted odds ratio [OR] = 5.81, 95% confidence interval [CI] = 3.60–9.38); Simpson diversity (1.53, 1.03–2.29); Shannon diversity (2.03, 1.35–3.04)]. We also observed a significant difference in global fungal community patterns between cases and controls based on Bray–Curtis dissimilarity (P < 0.001). Carriage of oral fungal species, specifically, Saccharomyces cerevisiae, Candida tropicalis, Lodderomyces elongisporus, Candida albicans, and Fusarium poae, was associated with significantly higher odds of NPC, with ORs ranging from 1.56 to 4.66. Individuals with both low fungal and low bacterial alpha diversity had a profoundly elevated risk of NPC. Interpretation: Our results suggest that dysbiosis in the oral mycobiome, characterized by a loss of fungal community diversity and overgrowth of several fungal organisms, is associated with a substantially increased risk of NPC. Funding: This work was funded by the US National Institutes of Health, the Swedish Research Council, the High-level Talents Research Start-up Project of Fujian Medical University, and the China Scholarship Council.
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spelling doaj.art-601bb010ccee48588ffeaae4c343b1352023-09-29T04:44:23ZengElsevierEBioMedicine2352-39642023-10-0196104813Oral fungal profiling and risk of nasopharyngeal carcinoma: a population-based case-control studyResearch in contextYufeng Chen0Wanxin Li1Ellen T. Chang2Justine W. Debelius3Lokeshwaran Manoharan4Yuming Zheng5Yancheng Li6Guangwu Huang7Hans-Olov Adami8Rob Knight9Yonglin Cai10Zhe Zhang11Weimin Ye12Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, 17177, SwedenDepartment of Epidemiology and Health Statistics &amp; Key Laboratory of Ministry of Education for Gastrointestinal Cancer, Fujian Medical University, Fuzhou, 350000, ChinaDepartment of Epidemiology and Biostatistics, University of California, San Francisco, CA, 94143, USACenter for Translational Microbiome Research, Department of Microbiology, Tumor and Cancer Biology, Karolinska Institutet, Stockholm, 17177, Sweden; Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, 21205, USANational Bioinformatics Infrastructure Sweden (NBIS), Lund University, Lund, 22100, SwedenGuangxi Health Commission Key Laboratory of Molecular Epidemiology of Nasopharyngeal Carcinoma, Wuzhou Red Cross Hospital, Wuzhou, 543002, China; Department of Preventive Medicine, Wuzhou Cancer Center, Wuzhou, 543002, ChinaGuangxi Health Commission Key Laboratory of Molecular Epidemiology of Nasopharyngeal Carcinoma, Wuzhou Red Cross Hospital, Wuzhou, 543002, China; Cangwu Institute for Nasopharyngeal Carcinoma Control and Prevention, Wuzhou, 543002, ChinaDepartment of Otolaryngology-Head &amp; Neck Surgery, First Affiliated Hospital of Guangxi Medical University, Nanning, 530021, China; Key Laboratory of High-Incidence-Tumor Prevention &amp; Treatment (Guangxi Medical University), Ministry of Education, Nanning, 530021, ChinaDepartment of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, 17177, Sweden; Clinical Effectiveness Group, Institute of Health and Society, University of Oslo, Oslo, NO-0316, NorwayDepartment of Pediatrics, University of California San Diego, CA, 92093, USAGuangxi Health Commission Key Laboratory of Molecular Epidemiology of Nasopharyngeal Carcinoma, Wuzhou Red Cross Hospital, Wuzhou, 543002, China; Department of Preventive Medicine, Wuzhou Cancer Center, Wuzhou, 543002, China; Corresponding author. Guangxi Health Commission Key Laboratory of Molecular Epidemiology of Nasopharyngeal Carcinoma, Wuzhou Red Cross Hospital, Wuzhou, 543002, China.Department of Otolaryngology-Head &amp; Neck Surgery, First Affiliated Hospital of Guangxi Medical University, Nanning, 530021, China; Key Laboratory of High-Incidence-Tumor Prevention &amp; Treatment (Guangxi Medical University), Ministry of Education, Nanning, 530021, China; Corresponding author. Department of Otolaryngology-Head &amp; Neck Surgery, First Affiliated Hospital of Guangxi Medical University, Nanning, 530021, China.Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, 17177, Sweden; Department of Epidemiology and Health Statistics &amp; Key Laboratory of Ministry of Education for Gastrointestinal Cancer, Fujian Medical University, Fuzhou, 350000, China; Corresponding author. Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, 171 77, Sweden.Summary: Background: Dysbiosis of the oral mycobiome has been linked to some diseases, including cancers. However, the role of oral fungal communities in nasopharyngeal carcinoma (NPC) carcinogenesis has not previously been investigated. Methods: We characterized the oral salivary fungal mycobiome in 476 untreated incident NPC patients and 537 population-based controls using fungal internal transcribed spacer (ITS)-2 sequencing. The relationship between oral fungal mycobiome and the risk of NPC was assessed through bioinformatic and biostatistical analyses. Findings: We found that lower fungal alpha diversity was associated with an increased odds of NPC [lower vs. higher: observed features (adjusted odds ratio [OR] = 5.81, 95% confidence interval [CI] = 3.60–9.38); Simpson diversity (1.53, 1.03–2.29); Shannon diversity (2.03, 1.35–3.04)]. We also observed a significant difference in global fungal community patterns between cases and controls based on Bray–Curtis dissimilarity (P < 0.001). Carriage of oral fungal species, specifically, Saccharomyces cerevisiae, Candida tropicalis, Lodderomyces elongisporus, Candida albicans, and Fusarium poae, was associated with significantly higher odds of NPC, with ORs ranging from 1.56 to 4.66. Individuals with both low fungal and low bacterial alpha diversity had a profoundly elevated risk of NPC. Interpretation: Our results suggest that dysbiosis in the oral mycobiome, characterized by a loss of fungal community diversity and overgrowth of several fungal organisms, is associated with a substantially increased risk of NPC. Funding: This work was funded by the US National Institutes of Health, the Swedish Research Council, the High-level Talents Research Start-up Project of Fujian Medical University, and the China Scholarship Council.http://www.sciencedirect.com/science/article/pii/S2352396423003791FungiITS sequencingOral mycobiomeMicrobiomeNasopharyngeal carcinomaCase–control study
spellingShingle Yufeng Chen
Wanxin Li
Ellen T. Chang
Justine W. Debelius
Lokeshwaran Manoharan
Yuming Zheng
Yancheng Li
Guangwu Huang
Hans-Olov Adami
Rob Knight
Yonglin Cai
Zhe Zhang
Weimin Ye
Oral fungal profiling and risk of nasopharyngeal carcinoma: a population-based case-control studyResearch in context
EBioMedicine
Fungi
ITS sequencing
Oral mycobiome
Microbiome
Nasopharyngeal carcinoma
Case–control study
title Oral fungal profiling and risk of nasopharyngeal carcinoma: a population-based case-control studyResearch in context
title_full Oral fungal profiling and risk of nasopharyngeal carcinoma: a population-based case-control studyResearch in context
title_fullStr Oral fungal profiling and risk of nasopharyngeal carcinoma: a population-based case-control studyResearch in context
title_full_unstemmed Oral fungal profiling and risk of nasopharyngeal carcinoma: a population-based case-control studyResearch in context
title_short Oral fungal profiling and risk of nasopharyngeal carcinoma: a population-based case-control studyResearch in context
title_sort oral fungal profiling and risk of nasopharyngeal carcinoma a population based case control studyresearch in context
topic Fungi
ITS sequencing
Oral mycobiome
Microbiome
Nasopharyngeal carcinoma
Case–control study
url http://www.sciencedirect.com/science/article/pii/S2352396423003791
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