|Year : 2022 | Volume
| Issue : 2 | Page : 59-66
Influence of sexual habits on human papillomavirus infection risk and oral cancer
Alberto Rodriguez-Archilla, Raquel Suarez-Machado
Department of Stomatology, Oral Medicine Unit, Faculty of Dentistry, University of Granada, Granada, Spain
|Date of Submission||04-Mar-2021|
|Date of Decision||03-Mar-2022|
|Date of Acceptance||18-Apr-2022|
|Date of Web Publication||12-Jul-2022|
Department of Stomatology, Oral Medicine Unit, Faculty of Dentistry, University of Granada, Colegio Maximo, s/n. Campus de Cartuja, 18071 Granada
Source of Support: None, Conflict of Interest: None
Certain sexual habits facilitate the oral spread of human papillomavirus (HPV), a virus involved in 70−90% of oropharyngeal cancers. This study aimed to investigate the influence of sexual habits, especially oral sex, on the risk of both HPV infection and oral cancer. We searched the following electronic databases for studies published between 1981 and 2018 on sexual behavior, HPV detection, and oral cancer: PubMed (MEDLINE, Cochrane Library), Web of Science (WoS), and Google Scholar. This meta-analysis included 36 studies involving 10,213 oral cancer patients (7,455 males and 2,758 females) and 52,195 subjects without oral cancer (21,172 males and 31,023 females). The data are expressed as odds ratios (ORs) with their 95% confidence intervals (CIs). The risk factors for oral cancer were first sexual contact before the age of 18 years (OR: 1.98; P < 0.01) and number of oral sex partners (> 5) (OR: 1.68; P < 0.001). There were no significant differences between oral cancer patients and controls regarding oral sex practices (P = 0.53), number of sex partners (P = 0.20), number of couples in sex work (P = 0.61), and number of marriages (P = 0.29). Oral sex increased 1.96 times the probability of HPV infection (P < 0.001). Oral cancer patients who engaged in oral sex practices had a 2.75-fold increased risk of HPV positivity (P < 0.001). Oral sex practices may be an important risk factor for HPV infection and oral cancer.
Keywords: Mouth neoplasms, oncogenic viruses, papillomavirus infections, sexual behavior
|How to cite this article:|
Rodriguez-Archilla A, Suarez-Machado R. Influence of sexual habits on human papillomavirus infection risk and oral cancer. Sci Dent J 2022;6:59-66
|How to cite this URL:|
Rodriguez-Archilla A, Suarez-Machado R. Influence of sexual habits on human papillomavirus infection risk and oral cancer. Sci Dent J [serial online] 2022 [cited 2022 Dec 8];6:59-66. Available from: https://www.scidentj.com/text.asp?2022/6/2/59/350761
| Background|| |
Head and neck cancer is the sixth most frequent cancer worldwide, with oral squamous cell carcinoma the most common histological type (90% of the cases). In the past, oral cancer most commonly affected older adults with a history of tobacco and alcohol use. However, the incidence of smoking-related oral cancers has steadily declined in the last 30 years. Now, the incidence of oropharyngeal cancers (i.e., base of the tongue, soft palate, tonsillar region, and posterior pharynx) is increasing. One recent study reported a 5-fold increase in tongue and tonsillar cancers in young adults (20−39 years), compared with a 2-fold increase in older adults (> 55 years). Today, many oral cancer patients are younger adults with no history of smoking, pointing to the involvement of other etiological factors such as human papillomavirus (HPV) infection. Sexual habits, in particular, oral sex practices, facilitate HPV spread and potential infection via contact with oral mucosa. Estimates today suggest that between 70% and 90% of new oropharyngeal cancer cases show evidence of HPV infection. The purpose of this study was to investigate the influence of sexual habits, especially oral sex, on the risk of both HPV infection and oral cancer.
| Materials and Methods|| |
A search of the following databases was conducted for studies on sexual habits, oral cancer, and HPV: PubMed (MEDLINE, Cochrane Library), Web of Science (WoS), and Google Scholar. The search strategy included a combination of Medical Subject Headings (MeSH) and free-text terms. The MeSH search terms were “sexual behavior” AND “mouth neoplasms” OR “papillomavirus infections” AND “mouth”; free-text search terms were “papillomavirus” AND “sexual behavior” OR “oral sex” AND “mouth neoplasms” OR “mouth”; the allintitle search terms were “oral sex” OR “sexual behavior” AND “oral” “cancer” OR “carcinoma.” The search identified 340 articles (PubMed, n = 122; WoS, n = 201; Google Scholar, n = 17) published between 1981 and 2018. Of these articles, 126 were duplicates. The remaining 214 articles were assessed for eligibility. Two of the authors (AR-A and RS-M) independently reviewed the titles and abstracts of these articles. Articles were included in a subsequent meta-analysis based on the consensus between the two reviewers.
The exclusion criteria were: (a) articles without full-text availability (n = 68); (b) articles with ≤ 6 stars out of a maximum of 9 stars on the Newcastle–Ottawa (NOS) methodological quality assessment scale (n = 51); and (c) studies with non-usable data (n = 59). After applying these criteria, 36 studies were included in the meta-analysis [Figure 1].
For the meta-analysis, the data were processed using the RevMan 5.4 program (The Cochrane Collaboration, Oxford, UK). For dichotomous outcomes, the Mantel–Haenszel (M–H) χ2 formula was used to calculate effect estimates. The data are expressed as odds ratios (ORs), with their 95% confidence intervals (CIs). Heterogeneity was determined according to P-values and the Higgins statistic (I2). When heterogeneity was high (I2 > 50%), a random-effects model was applied. Tables and forest plot graphs were used to present the results. A value of P < 0.05 was considered statistically significant.
| Results|| |
[Table 1] presents the descriptive characteristics and methodological quality (NOS scale) of the studies that assessed HPV status according to oral sex practices.,,,,,,,,,,,,,,,,,,,,,,, Considering sample collection, the two most commonly used methods were oral rinse (n = 15 studies, 62.5%) and oral smears (n = 7 studies, 29.2%). Of these 24 studies, 23 (95.8%) studies used the polymerase chain reaction method for HPV detection, and one (4.2%) study used in-situ hybridization.
|Table 1: Descriptive characteristics of 24 studies that analyze human papillomavirus (HPV) status according to oral sex practices|
Click here to view
[Table 2] details the descriptive characteristics and methodological quality (NOS scale) of the studies that assessed oral cancer risk according to sexual behavior. In the 13 included studies,,,,,,,,,,,,, there were 9,636 oral cancer patients (males, n = 6,922, 71.8%; females, n = 2,594, 28.2%) and 10,652 individuals without cancer (males, n = 7,277, 68.3%; females, n = 3,375, 31.7%).
|Table 2: Descriptive characteristics of 13 studies that assess oral cancer risk according to sexual behavior|
Click here to view
Twenty-two studies examined the impact of oral sex practices on HPV infection risk in oral cancer patients vs. the general population.,,,,,,,,,,,,,,,,,,,,, The results are shown in [Figure 2]. Oral sex increased 1.89 times the probability of HPV infection in the general population, with a highly significant statistical relationship (OR = 1.89; 95% CI: 1.47–2.43; P < 0.001). Four studies evaluated the effect of oral sex practices on HPV infection risk in oral cancer patients [Figure 2]B.,,, The meta-analysis of these studies revealed a 3.56-fold increase in the risk of infection, with a highly significant association between oral sex practices and HPV infection risk in oral cancer patients (OR = 3.56; 95% CI: 2.13–5.94; P < 0.001).
|Figure 2: Study data and forest plot graph for the oral sex practice in both general population (A) and oral cancer patients (B) infected by the human papillomavirus (HPV+)|
Click here to view
[Table 3] shows the main oral cancer risk factors related to sexual habits. Twelve studies examined oral sex habits in patients with oral cancer and controls without the disease.,,,,,,,,,,, Although a slightly higher percentage of controls (35.5%) than oral cancer patients (31.3%) engaged in oral sex practices, the results were not statistically significant (OR = 0.94; 95% CI: 0.76–1.15; P = 0.53).
Seven studies analyzed the possible influence of having more than five sex partners on oral cancer risk.,,,,,, Although the results revealed an association between a greater number of partners and oral cancer risks, the association was not statistically significant (OR = 1.40; 95% CI: 0.84–2.33; P = 0.20). According to three studies, engaging in oral sex with more than five partners increased the probability of oral cancer 1.68 times,,, with a highly significant statistical difference (OR = 1.68; 95% CI: 1.24–2.28; P < 0.001).
Another three studies evaluated whether age <18 years at the time of first sexual intercourse influenced the risk of oral cancer.,, Based on these studies, the latter was associated with a 1.98-fold increase in the probability of oral cancer, with a significant statistical relationship (OR = 1.98; 95% CI: 1.26–3.12; P < 0.01).
Three studies considered the potential association of sexual contact with prostitutes (more than five partners) with oral cancer risk.,, The results revealed no statistically significant association (OR = 0.83; 95% CI: 0.41–1.70; P = 0.61). Finally, two studies assessed the role of marriage number (> 3) as a possible risk factor for oral cancer., This factor did not increase the risk, with no statistically significant association (OR = 0.78; 95% CI: 0.50–1.23; P = 0.29).
| Discussion|| |
There is limited evidence suggesting that a high number of lifetime sexual partners, engaging in oral sex, and having a female partner with a history of cervical cancer are associated with an elevated risk of both HPV infection and oral cancer, especially oropharyngeal cancer. The present meta-analysis focussed on the possible influence of sexual habits on the risk of both oral cancer and HPV infection included data from 36 studies. According to our results, oral sex practices increased the probability of HPV infection in the general population, with a highly significant statistical association between these factors (P < 0.001). Although 19 of 22 studies that reviewed the influence of oral sex practices on the risk of HPV infection found a higher risk among those who engaged in oral sex,,,,,,,,,,,,,,,,,,, three studies found a higher incidence of HPV infection among those who did not engage in oral sex.,, Similarly, oral cancer patients who engaged in oral sex practices raised their probability of HPV infection, with a highly significant statistical association (P < 0.001). All the studies that assessed risk factors for HPV highlighted a direct relationship between a higher incidence of oral sex practices and an elevated risk of oral cancer.,,,
The reported increase in the incidence of HPV-positive oropharyngeal cancers, particularly among young people who do not smoke or drink, has been attributed to changes in sexual behavior, such as oral sex habits, which may increase the likelihood of HPV transmission and oral infection. According to Shi et al., the most relevant factors that increase the risk of HPV infections are oral sex practices (multiplies six times the risk) and smoking (multiplies five times the risk). In addition, individuals who engage in oral sex with a higher number of partners have an increased likelihood of oral HPV infections.
As reported previously, oral sex and a greater number of sexual partners are the primary factors that increase the risk of oral HPV infection. Furthermore, oral infection with HPV type 16, the HPV type with the highest oncogenic risk, significantly increases the risk of oropharyngeal cancer by up to 22 times. According to the literature, the most probable mode of transmission of HPV-16 to the upper aerodigestive tract is oral-genital contact. The use of barrier methods is the most effective preventive measure to reduce the risk of both HPV infection and other sexually transmitted infections.
In this study, when we analyzed oral sex practices among oral cancer patients and controls without cancer, there was a slightly higher percentage among the controls, although the finding was not statistically significant (P = 0.53). Of the 12 studies that evaluated oral sex practices, 8 of the studies found a higher incidence of oral sex practices among the controls,,,,,,,, and the remaining 4 studies found a higher incidence among oral cancer patients.,,, Several studies found no relevant differences between oral cancer patients and controls in terms of oral sex habits.,,, Of note, one study found an inexplicable protective effect of oral sex on oral cancer risk.
When oral sex practices in the general population were analyzed according to gender, our results revealed differences between males and females with respect to oral cancer risk, with males who frequently engaged in oral sex showing a higher oral cancer risk compared to females who never engaged in oral sex. Nevertheless, other researchers did not find evidences of an association between oral sex practices and oral cancer risk among females. In the case of HPV oral infections, the results suggest that males who engage in oral sex with females may have a higher risk of HPV oral infection, but not vice versa. It is important to note that non-reporting of oral sex practices, possibly due to embarrassment, may preclude accurate assessments of the association between oral cancer risk and gender.
In the present study, although having a higher number of sex partners (> 5) did not affect the risk of oral cancer, a higher incidence or engaging in oral sex practices was significantly associated with an elevated oral cancer risk.
An increase in the number of non-oral sex partners does not seem to have a significant impact on oral cancer risk or to be associated with an increased risk of oral HPV infection, which is closely linked with oropharyngeal carcinoma. In contrast, individuals with a greater number of oral sex partners are more likely to contract oral HPV and therefore to have an elevated risk of oral cancer.
In this study, first sexual contact aged younger than 18 years increased the probability of oral cancer. According to the literature, earlier initiation of sexual activity, together with oral sex practices and tobacco consumption, is associated with an elevated incidence of oral HPV infection. According to Chen et al., individuals with HPV infection who engaged in sexual activity before the age of 18 years had a 13-fold increase in oral cancer risks compared with those without HPV infection who had their first sexual contact after the age of 18 years.
In the present paper, sexual contact with a greater number of prostitutes (> 5) was not significantly associated with oral cancer risk (P = 0.61). Of the three studies that evaluated this variable, two studies found a higher incidence of engaging in sexual activity with prostitutes among oral cancer patients than controls,, whereas the other study found the opposite finding. The possible link between sexual contact with prostitutes and oral cancer is inconsistent, suggesting that other indicators of sexual habits (history of sexually transmitted diseases, total number of sexual partners, etc.) influence oral cancer risk., Based on the literature, it seems that the risk of oral cancer rises in association with an increase in the number of sexual partners, irrespective of the identity of these partners (i.e., prostitutes or not).
In this study, the number of marriages (> 3 marriages) was not statistically significantly associated with oral cancer risk (P = 0.29). Of the two studies that considered this variable, one study found a higher number of marriages among oral cancer patients, whereas the other study found a greater number among healthy controls. Thus, the potential role of marriage number in oral cancer risk is inconclusive. More studies are needed to shed light on this issue. Many factors other than marriage number seem to influence oral cancer risk. These include the number of sexual partners, type of sexual practices, history of sexually transmitted diseases, existence of wounds due to sexual activity, and HPV status of sexual partners.
The present study has some limitations. It is difficult to obtain reliable information on the sexual habits of the population, as such information is personal, and many individuals may not be totally honest about these habits. Possibly, sexual habits of the general population, including oral sex practices, have a greater influence on the risk of oral HPV infection than on the risk of oral cancer. If this is the case, sexual practices may have infective but not oncogenic potential.
The findings of this meta-analysis should be interpreted cautiously because of the high heterogeneity of some comparisons and differences between the studies in terms of data collection methods, statistical analyses, and characteristics of the study populations.
| Conclusions|| |
In this meta-analysis, oral sex practices increased the probability of HPV infection more in oral cancer patients than in the general population. Other significant oral cancer risk factors were engaging in first sexual contact before the age of 18 years and having more than five oral sex partners. No significant differences were observed between oral cancer patients and controls with respect to oral sex practices, number of sex partners, number of sexual encounters with prostitutes, and number of marriages.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al
. Cancer incidence and mortality worldwide: Sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 2015;136:E359-86.
Rodriguez-Archilla A, Stuardo-Parada A. Risk factors related to human papillomavirus infection in oral squamous cell carcinoma. Arch Med Health Sci 2019;7:33-7. [Full text]
Shiboski CH, Schmidt BL, Jordan RC. Tongue and tonsil carcinoma: Increasing trends in the U.S. population ages 20-44 years. Cancer 2005;103:1843-9.
Chaturvedi AK, Engels EA, Pfeiffer RM, Hernandez BY, Xiao W, Kim E, et al
. Human papillomavirus and rising oropharyngeal cancer incidence in the United States. J Clin Oncol 2011;29:4294-301.
Young D, Xiao CC, Murphy B, Moore M, Fakhry C, Day TA. Increase in head and neck cancer in younger patients due to human papillomavirus (HPV). Oral Oncol 2015;51: 727-30.
Wells G, Shea B, O’Connell D, Peterson J, Welch V, Losos M, et al
. The Newcastle-Ottawa Scale (NOS) for Assessing the Quality of Nonrandomised Studies in Meta-Analyses [Internet]. Ottawa, Canada: The Ottawa Hospital. Available from: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp
. [Last accessed on February 11, 2021].
Smith EM, Ritchie JM, Summersgill KF, Klussmann JP, Lee JH, Wang D, et al
. Age, sexual behavior and human papillomavirus infection in oral cavity and oropharyngeal cancers. Int J Cancer 2004;108:766-72.
D’Souza G, Agrawal Y, Halpern J, Bodison S, Gillison ML. Oral sexual behaviors associated with prevalent oral human papillomavirus infection. J Infect Dis 2009;199:1263-9.
Brown B, Blas MM, Cabral A, Carcamo C, Gravitt PE, Halsey N. Oral sex practices, oral human papillomavirus and correlations between oral and cervical human papillomavirus prevalence among female sex workers in Lima, Peru. Int J STD AIDS 2011;22:655-8.
Sánchez-Vargas LO, Díaz-Hernández C, Martinez-Martinez A. Detection of human papilloma virus (HPV) in oral mucosa of women with cervical lesions and their relation to oral sex practices. Infect Agent Cancer 2010;5:25.
Dahlstrom KR, Li G, Tortolero-Luna G, Wei Q, Sturgis EM. Differences in history of sexual behavior between patients with oropharyngeal squamous cell carcinoma and patients with squamous cell carcinoma at other head and neck sites. Head Neck 2011;33:847-55.
Gillison ML, Broutian T, Pickard RK, Tong ZY, Xiao W, Kahle L, et al
. Prevalence of oral HPV infection in the United States, 2009-2010. JAMA 2012;307:693-703.
Bui TC, Markham CM, Ross MW, Mullen PD. Examining the association between oral health and oral HPV infection. Cancer Prev Res (Phila) 2013;6:917-24.
Lang Kuhs KA, Gonzalez P, Struijk L, Castro F, Hildesheim A, van Doorn LJ, et al
; Costa Rica Vaccine Trial Group. Prevalence of and risk factors for oral human papillomavirus among young women in Costa Rica. J Infect Dis 2013;208:1643-52.
Antonsson A, Cornford M, Perry S, Davis M, Dunne MP, Whiteman DC. Prevalence and risk factors for oral HPV infection in young Australians. PLoS One 2014;9:e91761.
Cook RL, Thompson EL, Kelso NE, Friary J, Hosford J, Barkley P, et al
. Sexual behaviors and other risk factors for oral human papillomavirus infections in young women. Sex Transm Dis 2014;41:486-92.
Dahlstrom KR, Burchell AN, Ramanakumar AV, Rodrigues A, Tellier PP, Hanley J, et al
. Sexual transmission of oral human papillomavirus infection among men. Cancer Epidemiol Biomarkers Prev 2014;23:2959-64.
Davidson CL, Richter KL, Van der Linde M, Coetsee J, Boy SC. Prevalence of oral and oropharyngeal human papillomavirus in a sample of South African men: A pilot study. S Afr Med J 2014;104:358-61.
Hang D, Liu F, Liu M, He Z, Sun M, Liu Y, et al
. Oral human papillomavirus infection and its risk factors among 5,410 healthy adults in China, 2009-2011. Cancer Epidemiol Biomarkers Prev 2014;23:2101-10.
Machado AP, Gatto de Almeida F, Bonin CM, Martins Prata TT, Sobrinho Ávilla L, Junqueira Padovani CT, et al
. Presence of highly oncogenic human papillomavirus in the oral mucosa of asymptomatic men. Braz J Infect Dis 2014;18:266-70.
Meyer MF, Huebbers CU, Siefer OG, Vent J, Engbert I, Eslick GD, et al
. Prevalence and risk factors for oral human papillomavirus infection in 129 women screened for cervical HPV infection. Oral Oncol 2014;50:27-31.
Vidotti LR, Vidal FC, Monteiro SC, Nunes JD, Salgado JV, Brito LM, et al
. Association between oral DNA-HPV and genital DNA-HPV. J Oral Pathol Med 2014;43:289-92.
Chen F, Yan L, Liu F, Huang J, Liu F, Wu J, et al
. Oral human papillomavirus infection, sexual behaviors and risk of oral squamous cell carcinoma in southeast of China: A case–control study. J Clin Virol 2016;85:7-12.
Kedarisetty S, Orosco RK, Hecht AS, Chang DC, Weissbrod PA, Coffey CS. Concordant oral and vaginal human papillomavirus infection in the United States. JAMA Otolaryngol Head Neck Surg 2016;142:457-65.
Rosen BJ, Walter L, Gilman RH, Cabrerra L, Gravitt PE, Marks MA. Prevalence and correlates of oral human papillomavirus infection among healthy males and females in Lima, Peru. Sex Transm Infect 2016;92:149-54.
Cab-Sánchez BG, Hernández-Solís SE, Rueda-Gordillo F, Conde-Ferráez L, Gómez-Carballo JG, González-Losa MR. Epidemiology of oral HPV infection in young healthy individuals. Rev Chil Infectol 2017;34:557-62.
Lupato V, Holzinger D, Höfler D, Menegaldo A, Giorgi Rossi P, Del Mistro A, et al
. Prevalence and determinants of oral human papillomavirus infection in 500 young adults from Italy. PLoS One 2017;12:e0170091.
Shi N, Lu Q, Zhang J, Li L, Zhang J, Zhang F, et al
. Analysis of risk factors for persistent infection of asymptomatic women with high-risk human papilloma virus. Hum Vaccin Immunother 2017;13:1-7.
Sonawane K, Suk R, Chiao EY, Chhatwal J, Qiu P, Wilkin T, et al
. Oral human papillomavirus infection: Differences in prevalence between sexes and concordance with genital human papillomavirus infection, NHANES 2011 to 2014. Ann Intern Med 2017;167:714-24.
Taberna M, Inglehart RC, Pickard RK, Fakhry C, Agrawal A, Katz ML, et al
. Significant changes in sexual behavior after a diagnosis of human papillomavirus-positive and human papillomavirus-negative oral cancer. Cancer 2017;123:1156-65.
Maden C, Beckmann AM, Thomas DB, McKnight B, Sherman KJ, Ashley RL, et al
. Human papillomaviruses, herpes simplex viruses, and the risk of oral cancer in men. Am J Epidemiol 1992;135:1093-102.
Schwartz SM, Daling JR, Doody DR, Wipf GC, Carter JJ, Madeleine MM, et al
. Oral cancer risk in relation to sexual history and evidence of human papillomavirus infection. J Natl Cancer Inst 1998;90:1626-36.
Talamini R, Vaccarella S, Barbone F, Tavani A, La Vecchia C, Herrero R, et al
. Oral hygiene, dentition, sexual habits and risk of oral cancer. Br J Cancer 2000;83:1238-42.
Garrote LF, Herrero R, Reyes RM, Vaccarella S, Anta JL, Ferbeye L, et al
. Risk factors for cancer of the oral cavity and oro-pharynx in Cuba. Br J Cancer 2001;85:46-54.
Herrero R, Castellsagué X, Pawlita M, Lissowska J, Kee F, Balaram P, et al
; IARC Multicenter Oral Cancer Study Group. Human papillomavirus and oral cancer: The international agency for research on cancer multicenter study. J Natl Cancer Inst 2003;95:1772-83.
Lissowska J, Pilarska A, Pilarski P, Samolczyk-Wanyura D, Piekarczyk J, Bardin-Mikolłajczak A, et al
. Smoking, alcohol, diet, dentition and sexual practices in the epidemiology of oral cancer in Poland. Eur J Cancer Prev 2003;12: 25-33.
Rajkumar T, Sridhar H, Balaram P, Vaccarella S, Gajalakshmi V, Nandakumar A, et al
. Oral cancer in Southern India: The influence of body size, diet, infections and sexual practices. Eur J Cancer Prev 2003;12:135-43.
Rosenquist K, Wennerberg J, Schildt EB, Bladström A, Göran Hansson B, Andersson G. Oral status, oral infections and some lifestyle factors as risk factors for oral and oropharyngeal squamous cell carcinoma. A population-based case–control study in Southern Sweden. Acta Otolaryngol 2005;125:1327-36.
D’Souza G, Kreimer AR, Viscidi R, Pawlita M, Fakhry C, Koch WM, et al
. Case–control study of human papillomavirus and oropharyngeal cancer. N Engl J Med 2007;356:1944-56.
Heck JE, Berthiller J, Vaccarella S, Winn DM, Smith EM, Shan’gina O, et al
. Sexual behaviours and the risk of head and neck cancers: A pooled analysis in the International Head and Neck Cancer Epidemiology (INHANCE) consortium. Int J Epidemiol 2010;39:166-81.
Loyha K, Vatanasapt P, Promthet S, Parkin DM. Risk factors for oral cancer in Northeast Thailand. Asian Pac J Cancer Prev 2012;13:5087-90.
Laprise C, Madathil SA, Allison P, Abraham P, Raghavendran A, Shahul HP, et al
. No role for human papillomavirus infection in oral cancers in a region in Southern India. Int J Cancer 2016;138:912-7.
[Figure 1], [Figure 2]
[Table 1], [Table 2], [Table 3]