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Human papillomavirus and Epstein-Barr virus co-infection in oral and oropharyngeal squamous cell carcinomas: A systematic review and meta-analysis

Rahman R, Shaikh MH, Gopinath D, Idris A, Johnson NW

Mol Oral Microbiol, 2023 Apr 04.
PMID: 37014754 DOI: 10.1111/omi.12412

Squamous cell carcinoma of the oral cavity (OSCC) is the most common head and neck malignancy. Importantly, we are experiencing an alarming rise in the incidence of oropharyngeal squamous cell carcinoma (OPSCC) globally. Oncogenic viruses, human papillomavirus (HPV) and Epstein-Barr virus (EBV), are known to be co-associated with OSCC and OPSCC cases. However, the reported incidence of HPV and EBV co-infection in OSCCs and OPSCCs globally is unknown. To address this, we performed a formal meta-analysis and systematic review on published studies that report the detection of both EBV and HPV in OSCCs and OPSCCs. Our analysis revealed 18 relevant studies out of a total of 1820 cases (1181 from the oral cavity and 639 from the oropharynx). Overall, HPV and EBV co-infection was found in 11.9% of OSCC and OPSCC cases combined (95% CI: 8-14.1%). Based on anatomical subsite, dual positivity estimates were 10.5% (95% CI: 6.7- 15.1%) for OSCC and 14.2% (95% CI: 9.1-21.3%) for OPSCC. The highest dual positivity rates described were in European countries: for OSCC 34.7% (95% CI: 25.9 - 44.6%) in Sweden and for OPSCC, 23.4% (95% CI: 16.9 - 31.5%) in Poland. Given these substantive prevalence rates, the value of detecting dual infection in the diagnosis and prognosis of these cancers deserves careful longitudinal studies, as do implications for cancer prevention and therapy. We further proposed molecular mechanisms that could explain how HPV and EBV could co-contribute to the aetiology of OSCCs and OPSCCs. This article is protected by copyright. All rights reserved.
Fulltext Periodontal Diseases as Putative Risk Factors for Head and Neck Cancer: Systematic Review and Meta-Analysis

Gopinath D, Kunnath Menon R, K Veettil S, George Botelho M, Johnson NW

Cancers (Basel), 2020 Jul 14;12(7).
PMID: 32674369 DOI: 10.3390/cancers12071893

Whether "periodontal disease" can be considered as an independent risk factor for head and neck cancer (HNC) remains controversial. The aim of the current meta-analysis was to quantitatively assess this relationship in order to determine whether this represents a true risk factor, with implications for cancer prevention and management. PubMed, Scopus, and Embase databases were systematically searched. Selective studies were reviewed, and meta-analysis was performed to estimate the pooled odds ratio (OR) with 95% confidence intervals (CIs) on eligible studies using a random effects model. In total, 21 eligible observational studies (4 cohorts and 17 case-controls) were identified for qualitative synthesis after a review of 1051 articles. Significant heterogeneity could be identified in measures utilized for reporting of periodontal disease. Meta-analysis performed on nine studies that employed objective measures for reporting periodontal disease demonstrated a significant association between periodontal disease and HNC [OR 3.17, 95% CI, 1.78-5.64]. A diseased periodontium represents an independent risk marker, and a putative risk factor, for HNC. Prospective studies with standardized measures of periodontal disease severity and extent, integrated with microbiological and host susceptibility facets, are needed to elucidate the mechanisms of this positive association and whether treatment of the former influences the incidence and outcomes for HNC.
Culture-independent studies on bacterial dysbiosis in oral and oropharyngeal squamous cell carcinoma: A systematic review

Gopinath D, Menon RK, Banerjee M, Su Yuxiong R, Botelho MG, Johnson NW

Crit Rev Oncol Hematol, 2019 Jul;139:31-40.
PMID: 31112880 DOI: 10.1016/j.critrevonc.2019.04.018

Imbalance within the resident bacterial community (dysbiosis), rather than the presence and activity of a single organism, has been proposed to be associated with, and to influence, the development and progression of various diseases; however, the existence and significance of dysbiosis in oral/oropharyngeal cancer is yet to be clearly established. A systematic search (conducted on 25/01/2018 and updated on 25/05/2018) was performed on three databases (Pubmed, Web of Science & Scopus) to identify studies employing culture-independent methods which investigated the bacterial community in oral/oropharyngeal cancer patients compared to control subjects. Of the 1546 texts screened, only fifteen publications met the pre-determined selection criteria. Data extracted from 731 cases and 809 controls overall, could not identify consistent enrichment of any particular taxon in oral/oropharyngeal cancers, although common taxa could be identified between studies. Six studies reported the enrichment of Fusobacteria in cancer at different taxonomic levels whereas four studies reported an increase in Parvimonas. Changes in microbial diversity remained inconclusive, with four studies showing a higher diversity in controls, three studies showing a higher diversity in tumors and three additional studies showing no difference between tumors and controls. Even though most studies identified a component of dysbiosis in oral/oropharyngeal cancer, methodological and analytical variations prevented a standardized summary, which highlights the necessity for studies of superior quality and magnitude employing standardized methodology and reporting. Indeed an holistic metagenomic approach is likely to be more meaningful, as is understanding of the overall metabolome, rather than a mere enumeration of the organisms present.
Compositional profile of mucosal bacteriome of smokers and smokeless tobacco users

Gopinath D, Wie CC, Banerjee M, Thangavelu L, Kumar R P, Nallaswamy D, et al.

Clin Oral Investig, 2022 Feb;26(2):1647-1656.
PMID: 34436669 DOI: 10.1007/s00784-021-04137-7

INTRODUCTION: Smoked, and especially smokeless, tobacco are major causes of oral cancer globally. Here, we examine the oral bacteriome of smokers and of smokeless tobacco users, in comparison to healthy controls, using 16S rRNA gene sequencing.
METHODS: Oral swab samples were collected from smokers, smokeless tobacco users, and healthy controls (n = 44). Microbial DNA was extracted and the 16S rRNA gene profiled using the Illumina MiSeq platform. Sequencing reads were processed using DADA2, and taxonomical classification was performed using the phylogenetic placement method. Differentially abundant taxa were identified using DESeq2, while functional metagenomes based on KEGG orthology abundance were inferred using LIMMA.
RESULTS: A significantly higher microbial diversity was observed in smokeless tobacco users and smokers relative to controls (P 1.5; BH adj P
Fulltext Salivary bacterial shifts in oral leukoplakia resemble the dysbiotic oral cancer bacteriome

Gopinath D, Kunnath Menon R, Chun Wie C, Banerjee M, Panda S, Mandal D, et al.

J Oral Microbiol, 2020 Dec 09;13(1):1857998.
PMID: 33391629 DOI: 10.1080/20002297.2020.1857998

Objective: While some oral carcinomas appear to arise de novo, others develop within long-standing conditions of the oral cavity that have malignant potential, now known as oral potentially malignant disorders (OPMDs). The oral bacteriome associated with OPMD has been studied to a lesser extent than that associated with oral cancer. To characterize the association in detail we compared the bacteriome in whole mouth fluid (WMF) in patients with oral leukoplakia, oral cancer and healthy controls. Methods: WMF bacteriome from 20 leukoplakia patients, 31 patients with oral cancer and 23 healthy controls were profiled using the Illumina MiSeq platform. Sequencing reads were processed using DADA2, and taxonomical classification was performed using the phylogenetic placement method. Sparse Partial Least Squares Regression Discriminant Analysis model was used to identify bacterial taxa that best discriminate the studied groups. Results: We found considerable overlap between the WMF bacteriome of leukoplakia and oral cancer while a clearer separation between healthy controls and the former two disorders was observed. Specifically, the separation was attributed to 14 taxa belonging to the genera Megaspheara, unclassified enterobacteria, Prevotella, Porphyromonas, Rothia and Salmonella, Streptococcus, and Fusobacterium. The most discriminative bacterial genera between leukoplakia and oral cancer were Megasphaera, unclassified Enterobacteriae, Salmonella and Prevotella.Conclusion: Oral bacteria may play a role in the early stages of oral carcinogenesis as a dysbiotic bacteriome is associated with oral leukoplakia and this resembles that of oral cancer more than healthy controls. Our findings may have implications for developing oral cancer prevention strategies targeting early microbial drivers of oral carcinogenesis.
Fulltext Differences in the bacteriome of swab, saliva, and tissue biopsies in oral cancer

Gopinath D, Menon RK, Wie CC, Banerjee M, Panda S, Mandal D, et al.

Sci Rep, 2021 01 13;11(1):1181.
PMID: 33441939 DOI: 10.1038/s41598-020-80859-0

Microbial dysbiosis has been implicated in the pathogenesis of oral cancer. We analyzed the compositional and metabolic profile of the bacteriome in three specific niches in oral cancer patients along with controls using 16SrRNA sequencing (Illumina Miseq) and DADA2 software. We found major differences between patients and control subjects. Bacterial communities associated with the tumor surface and deep paired tumor tissue differed significantly. Tumor surfaces carried elevated abundances of taxa belonging to genera Porphyromonas, Enterobacteriae, Neisseria, Streptococcus and Fusobacteria, whereas Prevotella, Treponema, Sphingomonas, Meiothermus and Mycoplasma genera were significantly more abundant in deep tissue. The most abundant microbial metabolic pathways were those related to fatty-acid biosynthesis, carbon metabolism and amino-acid metabolism on the tumor surface: carbohydrate metabolism and organic polymer degradation were elevated in tumor tissues. The bacteriome of saliva from patients with oral cancer differed significantly from paired tumor tissue in terms of community structure, however remained similar at taxonomic and metabolic levels except for elevated abundances of Streptococcus, Lactobacillus and Bacteroides, and acetoin-biosynthesis, respectively. These shifts to a pro-inflammatory profile are consistent with other studies suggesting oncogenic properties. Importantly, selection of the principal source of microbial DNA is key to ensure reliable, reproducible and comparable results in microbiome studies.
IARC Perspective on Oral Cancer Prevention

Bouvard V, Nethan ST, Singh D, Warnakulasuriya S, Mehrotra R, Chaturvedi AK, et al.

N Engl J Med, 2022 Nov 24;387(21):1999-2005.
PMID: 36378601 DOI: 10.1056/NEJMsr2210097