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. 2022 Feb 22;33(1):e2337. doi: 10.1002/rmv.2337

Transmission and clearance of human papillomavirus infection in the oral cavity and its role in oropharyngeal carcinoma – A review

Małgorzata Wierzbicka 1, Michel R M San Giorgi 2, Frederik G Dikkers 3,✉
PMCID: PMC10078185  PMID: 35194874

Abstract

The majority of sexually active individuals becomes infected with human papillomavirus (HPV) at least once in their lifetime. Pathways for HPV transmission vary across different mucosal sites per individual. They include autoinoculation within one host, direct transmission between individuals (including perinatal transmission and transmission during sexual activity), and indirect transmission through contact with hands. The authors aim to clarify the prevalence and route of transmission per anatomic site, inter‐ and intra‐individually, using a narrative review of the literature. In conclusion, transmission of HPV to the oral cavity and oropharynx is hypothesised to occur mainly through sexual contact. Transmission of particles through saliva has not been proven and daily living activities are not a documented source of HPV infection. Oropharyngeal HPV related cancer survivors and their partners do not show increased risk of infection during sexual intercourse. Transmission of HPV to the oral cavity (autoinoculation with fingers or transmission through saliva in deep kissing) is probably of limited importance.

Keywords: extragenital → extragenital, extragenital → genital, genital → extragenital, genital → genital, human papilloma virus, mucosal squamous cell carcinomas, orogenital transmission concerns

Abbreviations

DNA

deoxyribonucleic acid

HIV

human immunodeficiency virus

HPV

human papilloma virus

HPV‐OPC

human papilloma virus associated oropharyngeal carcinoma

HR‐HPV

high‐risk human papilloma virus

LR‐HPV

low‐risk human papilloma virus

MHC

major histocompatibility complex

MMP‐8

matrix metallo‐proteinase‐8

OPC

oropharyngeal carcinoma

RRP

recurrent respiratory papilloma

1. INTRODUCTION

This article will review the known pathways of transmission and clearance of oral human papilloma virus (HPV) infection. The problem of orogenital transmission concerns very sensitive personal spheres of life and is therefore often unexplored in literature. Furthermore, the literature data on the upper airway clearance mechanisms are still scarce and scattered. In this article we describe the risk of HPV transmission to the oropharynx per pathway (autoinoculation, perinatal transmission, inter‐site transmission between individuals) as well as the prevalence of simultaneous occurrence of the same type of HPV in different anatomical sites in sexual partners (concordance).

A significant proportion of mucosal squamous cell carcinomas of the head and neck, particularly of the oropharynx, are directly attributable to the HPV. 1 , 2 HPV infection is considered the most common sexually transmitted disease among both males and females. 3 The increase in the incidence of HPV‐related tumors has been postulated to be due to changing sexual practices. However, the mode of HPV transmission to the oral cavity is still poorly understood. 4 There is need of a review of potential pathways of transmission of HPV between anatomical sites and between individuals. 5

HPV infections are often asymptomatic and unrecognized. The majority of sexually active individuals becomes infected with HPV at least once in their lifetime, 6 often without being aware and not presenting any symptoms. Prevalence of HPV acquisition, persistence, and infection are correlated with sexual behaviour, viral load, anatomical site, local immunity and clearance. With age, the incidence of new infections decreases, while persistence increases. 7 This phenomenon may result from changing sexual habits and age‐related immune senescence affecting HPV clearance.

2. TRANSMISSION OF HUMAN PAPILLOMA VIRUS TO THE ORAL MUCOSA

There are multiple pathways for HPV transmission across different mucosal sites. They include autoinoculation within one host, and transmission between individuals. Interindividual transmission includes perinatal transmission, sexual transmission by various techniques of orogenital sex, deep kissing (French kissing, involving extensive or intensive contact of the inner lips, tongue, and teeth especially with prolonged or rhythmic tongue‐to‐tongue contact) and indirect transmission through contact with hands.

Contemporary HPV transmission models are based on established paradigms of multi‐site transmission and natural immunity, that differ for every mucosal site. 8 , 9 , 10 , 11 The multi‐site model represents the following transmission pathways: (1) extragenital → extragenital, (2) extragenital → genital, (3) genital → genital and (4) genital → extragenital. The extragenital site can either be the oral or anal site. Each pathway has its own probability of transmission, which is modeled per sexual partnership, duration of sexual partnerships, the specific number of different acts within a partnership or transmission probabilities per act. 9 All separate pathways will be discussed in the following paragraphs. An illustration of the most common sources of HPV infection, the infected, its pathway and relevant details are visualized in an infographic (Figure 1).

FIGURE 1.

FIGURE 1

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Infographic demonstrating the most common sources of human papilloma virus (HPV) infection, the infected, its pathway and relevant details

2.1. Autoinoculation

Autoinoculation between the genital and oral or anal sites could occur through intermediate contact with the hands or through virus shedding in the anogenital region. 12 , 13 There are some discrepancies in literature concerning oral HPV prevalence in women with cervical HPV infection. Auto‐infection among women with cervical HPV infection has been the subject of debate. 14 , 15 , 16 Women with proven cervical HPV infection, cervical dysplasia or invasive cancer have a higher prevalence of HPV in oral samples, indicating a relationship between such infections. 17 According to other authors, however, the correlation between cervical and oral colonisation by HPV is low. 18 , 19 Therefore simultaneous testing of oropharyngeal and cervical HPV infection does not seem promising as future screening strategy. 19 Patients with genital HPV infection are at risk for oral infection and, consequently, for the development of oropharyngeal carcinoma (OPC). 20 , 21 , 22

2.2. Perinatal transmission

High prevalence (44.9%) of HPV at prenatal testing in young pregnant women was followed by frequently detected HPV in placenta samples (14%) and in newborns (11.2%). 23 Although the exact mode of transmission is not well understood, oral HPV prevalence ranged from 10% to 30% among newborns born to HPV‐positive mothers. 13 , 18 , 19 , 22 , 24 , 25 , 26 , 27 , 28

HPV infection can be acquired in utero via the placenta or umbilical cord blood, perinatally or through breast milk. 29 Vertical transmission may occur in utero through ascending infection (transplacental transmission), during vaginal delivery, at caesarean section or in periconceptual transmission from the male sexual partner. HPV can be transmitted vertically to neonates through breast feeding. 30 Transmission just after delivery can occur via body to body contacts. High carriage rates of HPV DNA detected in oral samples from newborns decrease gradually during the first 3 years of life. 24 Perinatal transmission of LR‐HPV to neonates at birth has been confirmed to be associated with recurrent respiratory papillomatosis (RRP) development. 31

LR‐HPV related diseases such as RRP can occur in neonates and children. 32 These have been transmitted in utero, as a transplacental or ascending infection or during the passage through an infected birth canal. 33 , 34 Caesarean deliveries do not completely protect neonates against HPV. 35 HPVs, including high‐risk types 16 and 18, have also been detected in tonsillar or adenoid samples from children with tonsillar or adenoid hyperplasia, chronic tonsillitis and normal mucosa. 36 Children may represent a reservoir of ‘silent’ high‐risk HPV types that may be the key to HPV persistence and related carcinogenesis in adulthood. 37 , 38

2.3. Inter‐site transmission between individuals

Inter‐site transmission between individuals occurs in modes including oral sex, anal sex, or indirect transmission through contact with hands. HPV acquisition at each anatomical site can occur independently through an infected partner, but it is difficult to distinguish which sexual behaviours are responsible for HPV transmission from the genital tract to the mouth. Deep kissing and rimming (i.e. oral‐anal contact) have also been associated with prevalent oral HPV infection. 39 Mouth‐to‐mouth transmission, through deep kissing, still remains a possible source of the viruses. 8 , 15 , 40 Non‐genital sources of virus present under fingernails could potentially provide an alternate reservoir for future infection. 41

Orogenital transmission was proven to be the best documented route for oral HPV infection. For genotype‐concordant vaginal and oral HPV infections, recent oral sexual exposure was a more important risk factor than cumulative sexual exposure. 38

In women aged 18–69 years, with available oral and vaginal HPV DNA screening data, vaginal HPV infection was present in 45.2%, oral HPV infection in 4.1%, dual infection in 3.0%, and concordant infection in 1.1%. Having a new sexual partner was positively associated with dual infection. Having more than two oral sex partners in the past year was positively associated with concordant infection. 38

Almost half of USA men have penile HPV infection. 42 , 43 , 44 High burden of penile HPV infection was associated with oral HPV infection. 45 Incidental oral HPV infection was associated with recent frequency of performing oral sex, current infection with the same HPV type in the genitals, hyponychium, 46 and recent anal sex with men. 47 , 48

For having sex with only one homosexual partner, the risk of oral HR‐HPV infection was 19.3% if the partner had a genital infection. 49 This increased to 22.2% if oral sex was performed with two or more homosexual partners. 49 The incidence of oral HPV among young heterosexual men was lower than in homosexual relationships. However, the incidence of oral HPV infection increased by a larger number of partners (17.9%), having oral sex (28.6%) and partners with oral or genital infection (11.5%). 50 , 51 Moreover, prevalence increased with frequency of oral sex among men whose partner had a genital infection with the same HPV type, supporting the evidence that oral HPV may be transmitted through either oral‐oral or oral‐genital routes. 50

Couples in which one of the partners has a documented HPV infection are particularly noteworthy regarding transmission and concordance of HPV types. 52 , 53 Husbands of women with cervical cancer had an increased standardized incidence ratio of 2.7:1 of developing tonsillar or tongue cancer, while husbands of women with cervical intraepithelial neoplasia had a ratio of 2.4:1. 52 However, the risk of HPV transmission between OPC patients and their sexual partners shows divergent results: oral HPV16 DNA was detected among patients with OPC at diagnosis, but not among their partners. 39

Many patients with cervical cancer and their partners have anxiety about HPV transmission and collinear cancer risk. 54 Diagnosis and treatment of oral squamous cell carcinomas are associated with significant declines in the frequency of vaginal and oral sex, regardless of tumor HPV status. 55 Both in HPV positive and negative OPC patients there is a decline in sexual behaviour. Risk of transmission seems not to be the only reason for this decline. It was shown that diagnosis and treatment of OPC were associated with significant declines in the frequency of vaginal and oral sex, regardless of tumor HPV status. The highly similar decline in the frequency of sexual behaviours in HPV‐positive and HPV‐negative patients argue against knowledge and concern about HPV transmission through sex as the sole underlying reason for changes in sexual behaviour. 55

Timing, lifetime number, and type of sexual partners suggest additional nuances of how and why some individuals develop HPV‐OPC. Younger age at first oral sex and oral sex intensity remained associated with significantly increased odds of HPV‐OPC. 56 Type of sexual partner (older partner when a case was younger) or partners having extramarital sex was also associated with HPV‐OPC. 56 Obviously, sexual abstinence is the most reliable method of protection against HPV, but it cannot be considered as panacea for the prevention of HPV and all other sexually transmitted infections. 57 Therefore, a careful attitude to sexual practices is the most important recommendation. A low number of lifetime sexual partners and consistent and correct use of condoms, although not offering complete protection, can decrease or reduce the exposure to HPV. 58

3. CONCORDANCE OF HUMAN PAPILLOMA VIRUS INFECTIONS BETWEEN PARTNERS AND ANATOMIC SITES

Oral HPV concordance is defined as the simultaneous occurrence of the same type of HPV in different anatomical sites or sharing the infection in sexual partners. 59 HPV transmission and genotype concordance among heterosexual partners showed HPV‐DNA concordance in 87.5% couples. 60 The prevalence of oral HPV infections with concomitant cervical HPV infection show contradictory results: high by some authors, 61 , 62 but not showed by others. 63

Both the presence of cervical pathology and the presence of oral HPV are related to sexual habits. 64 Long time (over 24 months) positivity of cervical high‐risk HPV can induce an increased incidence of oral HPV persistence. 62 Oral HPV16 DNA is commonly detected among patients with HPV‐OPC at diagnosis, but prevalence rate among their partners is confusing. 65 , 66 The prevalence rate of oral HPV in partners of OPC patients was rated as approximately 15% and a concordance for their HPV genotype was 49%. 65 The fact that husbands of women with cervical cancer have approximately a two‐fold increased risk of tonsillar cancer supports the concept of oral HPV transmission by performing orogenital sex. 66 HPV‐related oropharyngeal carcinoma in couples, although rare, suggests transmission of HPV16. 67

The transmission and compatibility of viral genotypes also has psycho‐social implications and requires answering very personal questions. Diagnosis and treatment of OPC sometimes are associated with significant declines in the frequency of vaginal and oral sex. 55 These restrictions of sexual activity seem to be unnecessary because of two reasons. First, persistence of the virus over a long period of time can lead to neoplastic transformation, in which viral load is modified from a balance between acquisition and clearance. Second, OPC development through HPV transmission from an OPC positive partner is very rare. 67

There is yet another aspect in favour of not having to give up sexual behaviours in a relation with a OPC positive patient: there is still discrepancy about moderate type‐specific HPV concordance between genital and oral HPV types. 61 Low overall prevalence of genotype specific concordance between anatomic sites may be explained by site variation in susceptibility to HPV infection, differential exposure characteristics, and differences in natural history at each mucosal site. 68 , 69 What's more, there are other carriers of infection. Fingers have been described as a source of transmission or autoinoculation of β‐HPVs to the oral cavity. 70 Oral HPV infection in men is significantly correlated with urinary HPV infection, with HPV16 as the most common type. 71 Also, the majority of patients present concordant oral and urinary HPV types. 71

Men and women with genital wart‐like lesions are a high‐risk population. HPV types associated with an increased risk of dysplasia were detected in 64.6% of patients with condylomata acuminata. 72 The vast majority of patients had HPV6 DNA detected at the wart site and in another site as well. 73 Oral HPV was simultaneously identified in 10.4% of subjects and high concordance was found between oral and anal HPV types. 74

Altogether, HPV transmission and HPV concordance are influenced by all configurations of couples, all clinical situations and all possible sex configurations and the lifetime number of sexual partners. Consistent use of condoms reduces the risk of HPV acquisition. 60 However, this does not apply to household members or friends with whom they do not have a direct sexual relationship. The risk of spread by droplets or by aerosols, analogous to many other viruses seems very small as synchronous (or simultaneous) infection between relatives has never been described. However, the statement that saliva or deep kissing is likely irrelevant to oral HPV transmission is opposed by multiple previously published studies. 50

4. CLEARANCE OF HUMAN PAPILLOMA VIRUS

The viral load in particular anatomical sites results from a balance between acquisition and clearance. 75 , 76 Persistence of the virus can lead to neoplastic transformation. 17 , 77 , 78 , 79 The turning point on the cross road between clearance and carcinogenesis is the interplay of the viral proteins with different elements of the antioxidant and DNA damage response systems, emphasising the processes that might be required for the viral life cycle. 80

Most of our knowledge about HPV epidemiology relates to the cervix, where HPV acquisition occurs shortly after sexual debut, most infections clear within 1–2 years, and where infections at older ages are uncommon. Most of infections are transient, but persistent HR‐HPV infection is the major cause for development of cervical cancer. 81

Acquisition of oral oncogenic HPV infection is rarer than acquisition of genital infection, although infections at both sites seem to clear at roughly the same rate. 51 , 82 Numerous groups report that clearance of oral HPV infection is similar to that of anogenital HPV infections in healthy populations. 51 , 83 , 84 , 85 Increasing oral viral load was associated with reduced clearance of infection, consistent with the cervical cancer literature. 86

In a female cohort, with positive cervical and oral samples of HPV16, natural clearance correlated with HPV antibody titers. 87 Duration of HPV persistence longer than 12 months led to an increased risk for disease progression in cervical and oral neoplasia. 88 The cut‐off point for neoplastic transformation was the persistence of HPV infection longer than 6 months 89 Similarly, newly acquired oral oncogenic HPV infections in healthy middle aged men were cleared within 1 year, with a median duration of 6.9 months 51 In a group of sexually active male university students it was cleared within approximately 4 months 46 These are higher rates of clearance than observed in a spouses study, 24 and studies which included older married men. 84 , 90 , 91 Data from the HPV Infection in Men study which followed participants >7 years revealed that 18% of HPV16 infections persisted beyond 24 months, potentially conferring higher risk of HPV‐OPC. Oral HPV16 persistence was positively associated with baseline HPV16 L1 antibody status, 6 months' persistence with age and gingivitis, while 12 months' persistence was inversely associated with lifetime number of sexual partners. 7 In a study including both genders (all positive subjects having active sexual life), prevalence of oral transient HPV infection was 6.9% and the virus was eliminated in 6 months, 20 up to maximally 2 years in a few cases. 82 A prospective cohort study assessing the dynamics of HPV infections in parents and their infants, reported HPV genotype distribution and virus persistence in oral mucosa of the mothers in 17%. One‐third of them had persistent oral HPV infections but use of oral contraceptives and a second pregnancy protected against oral HPV persistence. 92

As emphasised in the previous paragraphs, contamination time is of paramount importance, which is the reverse of the cleansing potential. The longer the duration of an HPV infection, the higher the likelihood of continued persistence, and the higher the probability of detecting HPV DNA at any time point. 75

Clearance rates also vary by the virus type. LR‐HPV genotypes cleared from the oral mucosa more rapidly than HR‐HPV genotypes. 88 The most persistent is HPV16 93 : it has been identified as the most frequent type to persist at the oral cavity, 92 with longer persistence observed among men (22 months) than among women (19 months). 94

The viral load determined by the balance between acquisition and clearance is a derivative not only of sexual habits, recurrent episodes of contamination but also of an individual's immune status. Papillomaviruses have developed a variety of strategies to escape host innate and adaptive immunity. 95 , 96 Failure of immune control and detection is caused mainly by the lack of inflammatory reaction during the various stages of infection. HPV infections is confined to epithelial tissues and is highly localized. Viral proteins involved in immune escape are to enlist. E5 down‐regulate MHC class I and other key molecules in the antigen‐presentation pathways, E6 and E7 suppress host interferon pathways, activate the DNA‐damage pathways, and induce immune suppression via activation of suppressive cytokines and Tregs. 97 , 98

Higher HPV prevalence in HIV positive participants may be due to an increased persistence of HPV infection due to compromised immunity, or to a high incidence of new HPV infections as a consequence of sexual behaviour. 99 In a rehabilitation community for substance abusers' complete HPV clearance was observed in 1 year which could be related to adoption of healthier lifestyles of program participants. Nevertheless, new HPV infections were detected in these ex‐abusers even in the absence of the recognized and declared behavioural risk factors, suggesting a re‐expression from a latent infection. 99

Persistent oral HPV infection was associated with a low salivary matrix metallo‐proteinase‐8 (MMP‐8) concentration indicating eventually a failure in oral anti‐inflammatory defence. 100 Unfortunately, a reliable correlate of protective immunity or immunologic frailty to HPV currently does not exist. Previous HPV transmission models were based on a single site transmission paradigm, but it is important to assess the data of multi‐site transmission and site‐specific natural immunity. 9

However, it is unclear whether antibody response is synonymous with systemic protection against subsequent infections at other sites. Furthermore, the role of local immunity, either humoural or cell‐mediated, in protecting against subsequent infections is currently not well understood. Hence, there could be site‐specific differences in immune response and vulnerability to subsequent infections.

5. CONCLUSION

Given the lack of primary source data (i.e. no prospective studies on this topic, which require extrapolation of data from different studies to perform the analyses), it is difficult to reach to conclusions and recommendations. However, we believe that our review allows us to draw the following conclusions.

Orogenital transmission was proven to be the best documented route for oral HPV infection. Patients with cervical cancer and their partners have anxiety about HPV transmission and its consequent cancer risk. The risk of transmission depends on different clinical and life situations: having oral on anal sex, presence of a local HPV infection in one of the partners, having oral contact with a partner with OPC or having heterosexual sex with a woman with cervical carcinoma.

Transmission of HPV to the oral cavity (autoinoculation with fingers or transmission through saliva in deep kissing) is probably of limited importance.

Careful attitude to sexual practices and use of condoms in sexual behavior outside prolonged relationships is the most important recommendation for HPV cancer survivors and their partners, but there is no justification for advising discontinuation of sexual activity. Transmission of HPV particles through saliva has not been proven and daily living activities are not a documented source of HPV infection.

CONFLICT OF INTEREST

No conflict of interest declared.

AUTHOR CONTRIBUTIONS

Conceptualisation: Małgorzata Wierzbicka. Writing original draft: all authors. Writing review: all authors. Visualization: Michel R. M. San Giorgi. Editing: Frederik G. Dikkers. All authors read and approved the final manuscript.

ACKNOWLEDGEMENT

None.

Wierzbicka M, San Giorgi MRM, Dikkers FG. Transmission and clearance of human papilloma virus infection in the oral cavity and its role in oropharyngeal carcinoma – A review. Rev Med Virol. 2023;33(1):e2337. 10.1002/rmv.2337

DATA AVAILABILITY STATEMENT

Data sharing is not applicable to this article as no new data were created or analyzed in this study.

REFERENCES

  • 1. Li H, Torabi SJ, Yarbrough WG, Mehra S, Osborn HA, Judson B. Association of human papillomavirus status at head and neck carcinoma subsites with overall survival. JAMA Otolaryngol Head Neck Surg. 2018;144(6):519‐525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2. Agalliu I, Gapstur S, Chen Z, et al. Associations of oral alpha‐, beta‐, and gamma‐human papillomavirus types with risk of incident head and neck cancer. JAMA Oncol. 2016;2(5):599‐606. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3. Koutsky L. Epidemiology of genital human papillomavirus infection. Am J Med. 1997;102(5A):3‐8. [DOI] [PubMed] [Google Scholar]
  • 4. Wong MCS, Vlantis AC, Liang M, et al. Persistence and clearance of oral human papillomavirus infections: a prospective population‐based cohort study. J Med Virol. 2020. 10.1002/jmv.26130 [Epub ahead of print]. [DOI] [PubMed] [Google Scholar]
  • 5. Brondani MA, Siqueira AB, Alves CMC. Exploring lay public and dental professional knowledge around HPV transmission via oral sex and oral cancer development. BMC Publ Health. 2019;19(1):1529‐019‐7923‐6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6. Workowski KA, Berman S, Centers for Disease Control and Prevention (CDC) . Sexually transmitted diseases treatment guidelines. MMWR Recomm Rep (Morb Mortal Wkly Rep). 2010;59(RR‐12):1‐110. [PubMed] [Google Scholar]
  • 7. Bettampadi D, Sirak BA, Abrahamsen ME, et al. Factors associated with persistence and clearance of high‐risk oral HPV among participants in the HPV infection in men (HIM) study. Clin Infect Dis. 2021;73(9):e3227‐e3234. 10.1093/cid/ciaa1701 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8. Heijne JCM, van Liere GAFS, Hoebe CJPA, Bogaards JA, van Benthem BHB, Dukers‐Muijrers NHTM. What explains anorectal chlamydia infection in women? implications of a mathematical model for test and treatment strategies. Sex Transm Infect. 2017;93(4):270‐275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9. Lemieux‐Mellouki P, Drolet M, Jit M, Gingras G, Brisson M. Modelling multi‐site transmission of the human papillomavirus and its impact on vaccination effectiveness. Epidemics. 2017;21:80‐87. [DOI] [PubMed] [Google Scholar]
  • 10. Brouwer AF, Meza R, Eisenberg MC. Transmission heterogeneity and autoinoculation in a multisite infection model of HPV. Math Biosci. 2015;270(Pt A):115‐125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11. Hui B, Fairley CK, Chen M, et al. Oral and anal sex are key to sustaining gonorrhoea at endemic levels in MSM populations: a mathematical model. Sex Transm Infect. 2015;91(5):365‐369. [DOI] [PubMed] [Google Scholar]
  • 12. Rintala M, Grenman S, Puranen M, Syrjanen S. Natural history of oral papillomavirus infections in spouses: a prospective Finnish HPV family study. J Clin Virol. 2006;35(1):89‐94. [DOI] [PubMed] [Google Scholar]
  • 13. Tenti P, Zappatore R, Migliora P, Spinillo A, Belloni C, Carnevali L. Perinatal transmission of human papillomavirus from gravidas with latent infections. Obstet Gynecol. 1999;93(4):475‐479. [DOI] [PubMed] [Google Scholar]
  • 14. Gonzalez‐Losa Mdel R, Barrera ES, Herrera‐Pech V, Conde‐Ferraez L, Puerto‐Solis M, Ayora‐Talavera G. Epidemiology of oral HPV in the oral mucosa in women without signs of oral disease from yucatan, Mexico. Braz J Microbiol. 2015;46(1):301‐306. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15. Hernandez BY, Wilkens LR, Zhu X, et al. Transmission of human papillomavirus in heterosexual couples. Emerg Infect Dis. 2008;14(6):888‐894. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16. Nyitray AG, Lin HY, Fulp WJ, et al. The role of monogamy and duration of heterosexual relationships in human papillomavirus transmission. J Infect Dis. 2014;209(7):1007‐1015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17. Termine N, Giovannelli L, Matranga D, et al. Oral human papillomavirus infection in women with cervical HPV infection: new data from an Italian cohort and a metanalysis of the literature. Oral Oncol. 2011;47(4):244‐250. [DOI] [PubMed] [Google Scholar]
  • 18. Castellsague X, Drudis T, Canadas MP, et al. Human papillomavirus (HPV) infection in pregnant women and mother‐to‐child transmission of genital HPV genotypes: a prospective study in Spain. BMC Infect Dis. 2009;9:74‐2334‐9‐74. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19. Park H, Lee SW, Lee IH, et al. Rate of vertical transmission of human papillomavirus from mothers to infants: relationship between infection rate and mode of delivery. Virol J. 2012;9:80‐422X‐9‐80. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20. Cab‐Sanchez BG, Hernandez‐Solis SE, Rueda‐Gordillo F, Conde‐Ferraez L, Gomez‐Carballo JG, Gonzalez‐Losa MDR. Epidemiology of oral HPV infection in young healthy individuals. Rev Chilena Infectol. 2017;34(6):557‐562. [DOI] [PubMed] [Google Scholar]
  • 21. 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(9):1263‐1269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22. Koskimaa HM, Waterboer T, Pawlita M, Grenman S, Syrjanen K, Syrjanen S. Human papillomavirus genotypes present in the oral mucosa of newborns and their concordance with maternal cervical human papillomavirus genotypes. J Pediatr. 2012;160(5):837‐843. [DOI] [PubMed] [Google Scholar]
  • 23. Trottier H, Mayrand MH, Coutlee F, et al. Human papillomavirus (HPV) perinatal transmission and risk of HPV persistence among children: design, methods and preliminary results of the HERITAGE study. Papillomavirus Res. 2016;2:145‐152. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24. Rintala MA, Grenman SE, Puranen MH, et al. Transmission of high‐risk human papillomavirus (HPV) between parents and infant: a prospective study of HPV in families in Finland. J Clin Microbiol. 2005;43(1):376‐381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25. Bandyopadhyay S, Sen S, Majumdar L, Chatterjee R. Human papillomavirus infection among indian mothers and their infants. Asian Pac J Cancer Prev. 2003;4(3):179‐184. [PubMed] [Google Scholar]
  • 26. Rombaldi RL, Serafini EP, Mandelli J, Zimmermann E, Losquiavo KP. Transplacental transmission of human papillomavirus. Virol J. 2008;5:106‐422X‐5‐106. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27. Lee SM, Park JS, Norwitz ER, et al. Risk of vertical transmission of human papillomavirus throughout pregnancy: a prospective study. PLoS One. 2013;8(6):e66368. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28. Hahn HS, Kee MK, Kim HJ, et al. Distribution of maternal and infant human papillomavirus: risk factors associated with vertical transmission. Eur J Obstet Gynecol Reprod Biol. 2013;169(2):202‐206. [DOI] [PubMed] [Google Scholar]
  • 29. Roman A, Fife K. Human papillomavirus DNA associated with foreskins of normal newborns. J Infect Dis. 1986;153(5):855‐861. [DOI] [PubMed] [Google Scholar]
  • 30. Louvanto K, Rautava J, Willberg J, et al. Genotype‐specific incidence and clearance of human papillomavirus in oral mucosa of women: a six‐year follow‐up study. PLoS One. 2013;8(1):e53413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31. Louvanto K, Roger M, Faucher MC, Syrjanen K, Grenman S, Syrjanen S. HLA‐G and vertical mother‐to‐child transmission of human papillomavirus infection. Hum Immunol. 2018;79(6):471‐476. [DOI] [PubMed] [Google Scholar]
  • 32. Silverberg MJ, Thorsen P, Lindeberg H, Grant LA, Shah KV. Condyloma in pregnancy is strongly predictive of juvenile‐onset recurrent respiratory papillomatosis. Obstet Gynecol. 2003;101(4):645‐652. [DOI] [PubMed] [Google Scholar]
  • 33. Tseng CJ, Liang CC, Soong YK, Pao CC. Perinatal transmission of human papillomavirus in infants: relationship between infection rate and mode of delivery. Obstet Gynecol. 1998;91(1):92‐96. [DOI] [PubMed] [Google Scholar]
  • 34. Medeiros LR, Ethur AB, Hilgert JB, et al. Vertical transmission of the human papillomavirus: a systematic quantitative review. Cad Saúde Pública. 2005;21(4):1006‐1015. [DOI] [PubMed] [Google Scholar]
  • 35. Gomez LM, Ma Y, Ho C, McGrath CM, Nelson DB, Parry S. Placental infection with human papillomavirus is associated with spontaneous preterm delivery. Hum Reprod. 2008;23(3):709‐715. [DOI] [PubMed] [Google Scholar]
  • 36. Chen R, Sehr P, Waterboer T, et al. Presence of DNA of human papillomavirus 16 but no other types in tumor‐free tonsillar tissue. J Clin Microbiol. 2005;43(3):1408‐1410. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37. Mammas IN, Sourvinos G, Spandidos DA. The paediatric story of human papillomavirus (review). Oncol Lett. 2014;8(2):502‐506. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38. King EM, Gilson R, Beddows S, et al. Human papillomavirus DNA in men who have sex with men: type‐specific prevalence, risk factors and implications for vaccination strategies. Br J Cancer. 2015;112(9):1585‐1593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 39. D'Souza G, Gross ND, Pai SI, et al. Oral human papillomavirus (HPV) infection in HPV‐positive patients with oropharyngeal cancer and their partners. J Clin Oncol. 2014;32(23):2408‐2415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 40. Vogt SL, Gravitt PE, Martinson NA, Hoffmann J, D'Souza G. Concordant oral‐genital HPV infection in South Africa couples: evidence for transmission. Front Oncol. 2013;3:303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41. Fu TC, Hughes JP, Feng Q, et al. Epidemiology of human papillomavirus detected in the oral cavity and fingernails of mid‐adult women. Sex Transm Dis. 2015;42(12):677‐685. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42. Han JJ, Beltran TH, Song JW, Klaric J, Choi YS. Prevalence of genital human papillomavirus infection and human papillomavirus vaccination rates among US adult men: national health and nutrition examination survey (NHANES) 2013‐2014. JAMA Oncol. 2017;3(6):810‐816. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43. Gargano JW, Unger ER, Liu G, et al. Prevalence of genital human papillomavirus in males, United States, 2013‐2014. J Infect Dis. 2017;215(7):1070‐1079. [DOI] [PubMed] [Google Scholar]
  • 44. Gravitt PE. Human papillomavirus: the equal opportunity pathogen. J Infect Dis. 2017;215(7):1014‐1016. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 45. Winer RL, Lee SK, Hughes JP, Adam DE, Kiviat NB, Koutsky LA. Genital human papillomavirus infection: incidence and risk factors in a cohort of female university students. Am J Epidemiol. 2003;157(3):218‐226. [DOI] [PubMed] [Google Scholar]
  • 46. Edelstein ZR, Schwartz SM, Hawes S, et al. Rates and determinants of oral human papillomavirus infection in young men. Sex Transm Dis. 2012;39(11):860‐867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 47. Coutlee F, Trottier AM, Ghattas G, et al. Risk factors for oral human papillomavirus in adults infected and not infected with human immunodeficiency virus. Sex Transm Dis. 1997;24(1):23‐31. [DOI] [PubMed] [Google Scholar]
  • 48. Gillison ML, Broutian T, Pickard RK, et al. Prevalence of oral HPV infection in the United States, 2009‐2010. JAMA. 2012;307(7):693‐703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 49. Sonawane K, Suk R, Chiao EY, 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(10):714‐724. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 50. Dahlstrom KR, Burchell AN, Ramanakumar AV, et al. Sexual transmission of oral human papillomavirus infection among men. Cancer Epidemiol Biomarkers Prev. 2014;23(12):2959‐2964. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 51. Kreimer AR, Pierce Campbell CM, Lin HY, et al. Incidence and clearance of oral human papillomavirus infection in men: the HIM cohort study. Lancet. 2013;382(9895):877‐887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 52. Hemminki K, Dong C, Frisch M. Tonsillar and other upper aerodigestive tract cancers among cervical cancer patients and their husbands. Eur J Cancer Prev. 2000;9(6):433‐437. [DOI] [PubMed] [Google Scholar]
  • 53. Uken RB, Brummer O, von Schubert‐Bayer C, Brodegger T, Teudt IU. Oral HPV prevalence in women positive for cervical HPV infection and their sexual partners: a German screening study. Eur Arch Oto‐Rhino‐Laryngol. 2016;273(7):1933‐1942. [DOI] [PubMed] [Google Scholar]
  • 54. 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(5):457‐465. [DOI] [PubMed] [Google Scholar]
  • 55. Taberna M, Inglehart RC, Pickard RK, et al. Significant changes in sexual behavior after a diagnosis of human papillomavirus‐positive and human papillomavirus‐negative oral cancer. Cancer. 2017;123(7):1156‐1165. [DOI] [PubMed] [Google Scholar]
  • 56. Drake VE, Fakhry C, Windon MJ, et al. Timing, number, and type of sexual partners associated with risk of oropharyngeal cancer. Cancer. 2021;127(7):1029‐1038. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 57. Workowski KA, Bolan GA, Centers for Disease Control and Prevention . Sexually transmitted diseases treatment guidelines. MMWR Recomm Rep (Morb Mortal Wkly Rep). 2015;64(RR‐03):1‐137. [PMC free article] [PubMed] [Google Scholar]
  • 58. Markowitz LE, Dunne EF, Saraiya M, et al. Human papillomavirus vaccination: recommendations of the advisory committee on immunization practices (ACIP). MMWR Recomm Rep (Morb Mortal Wkly Rep). 2014;63(RR‐05):1‐30. [PubMed] [Google Scholar]
  • 59. Kero K, Rautava J. HPV infections in heterosexual couples: mechanisms and covariates of virus transmission. Acta Cytol. 2019;63(2):143‐147. [DOI] [PubMed] [Google Scholar]
  • 60. Beder Ribeiro CM, Ferrer I, Santos de Farias AB, et al. Oral and genital HPV genotypic concordance between sexual partners. Clin Oral Investig. 2014;18(1):261‐268. [DOI] [PubMed] [Google Scholar]
  • 61. Steinau M, Hariri S, Gillison ML, et al. Prevalence of cervical and oral human papillomavirus infections among US women. J Infect Dis. 2014;209(11):1739‐1743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 62. Tezal M, Wactawski‐Wende J, Grossi SG, Dmochowski J, Genco RJ. Periodontal disease and the incidence of tooth loss in postmenopausal women. J Periodontol. 2005;76(7):1123‐1128. [DOI] [PubMed] [Google Scholar]
  • 63. Eggersmann TK, Sharaf K, Baumeister P, et al. Prevalence of oral HPV infection in cervical HPV positive women and their sexual partners. Arch Gynecol Obstet. 2019;299(6):1659‐1665. [DOI] [PubMed] [Google Scholar]
  • 64. Sanchez‐Siles M, Remezal‐Solano M, Lopez‐Lopez AM, Camacho‐Alonso F. Prevalence of human papillomavirus in the saliva of sexually active women with cervical intraepithelial neoplasias. Med Oral Patol Oral Cir Bucal. 2020;25(2):e195‐e204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 65. Tsao AS, Papadimitrakopoulou V, Lin H, et al. Concordance of oral HPV prevalence between patients with oropharyngeal cancer and their partners. Infect Agent Cancer. 2016;11:21‐01600669. eCollection 2016. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 66. D'Souza G, Cullen K, Bowie J, Thorpe R, Fakhry C. Differences in oral sexual behaviors by gender, age, and race explain observed differences in prevalence of oral human papillomavirus infection. PLoS One. 2014;9(1):e86023. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 67. Sathasivam HP, Bhatia R, Bradley P, et al. Concurrent HPV‐related oropharyngeal carcinoma in four couples. Oral Oncol. 2018;86:33‐37. [DOI] [PubMed] [Google Scholar]
  • 68. Woelber L, Breuer J, Meyer T, et al. Oral human papillomavirus in women with high‐grade cervical intraepithelial neoplasia. J Low Genit Tract Dis. 2017;21(3):177‐183. [DOI] [PubMed] [Google Scholar]
  • 69. Veldhuijzen NJ, Snijders PJ, Reiss P, Meijer CJ, van de Wijgert JH. Factors affecting transmission of mucosal human papillomavirus. Lancet Infect Dis. 2010;10(12):862‐874. [DOI] [PubMed] [Google Scholar]
  • 70. Winer RL, Gheit T, Feng Q, et al. Prevalence and correlates of beta‐ and gamma‐human papillomavirus detection in oral samples from mid‐adult women. J Infect Dis. 2019;219(7):1067‐1075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 71. Nakashima K, Shigehara K, Kawaguchi S, et al. Prevalence of human papillomavirus infection in the oropharynx and urine among sexually active men: a comparative study of infection by papillomavirus and other organisms, including neisseria gonorrhoeae, chlamydia trachomatis, mycoplasma spp., and ureaplasma spp. BMC Infect Dis. 2014;14:43‐2334‐14‐43. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 72. Brown DR, Schroeder JM, Bryan JT, Stoler MH, Fife KH. Detection of multiple human papillomavirus types in condylomata acuminata lesions from otherwise healthy and immunosuppressed patients. J Clin Microbiol. 1999;37(10):3316‐3322. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 73. Greer CE, Wheeler CM, Ladner MB, et al. Human papillomavirus (HPV) type distribution and serological response to HPV type 6 virus‐like particles in patients with genital warts. J Clin Microbiol. 1995;33(8):2058‐2063. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 74. Kofoed K, Sand C, Forslund O, Madsen K. Prevalence of human papillomavirus in anal and oral sites among patients with genital warts. Acta Derm Venereol. 2014;94(2):207‐211. [DOI] [PubMed] [Google Scholar]
  • 75. Beachler DC, Sugar EA, Margolick JB, et al. Risk factors for acquisition and clearance of oral human papillomavirus infection among HIV‐infected and HIV‐uninfected adults. Am J Epidemiol. 2015;181(1):40‐53. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 76. Beachler DC, Waterboer T, Pierce Campbell C, et al. HPV16 E6 seropositivity among cancer‐free men with oral, anal or genital HPV16 infection. Papillomavirus Res. 2016;2:141‐144. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 77. Gillison ML, Castellsague X, Chaturvedi A, et al. Eurogin roadmap: comparative epidemiology of HPV infection and associated cancers of the head and neck and cervix. Int J Cancer. 2014;134(3):497‐507. [DOI] [PubMed] [Google Scholar]
  • 78. Koshiol J, Lindsay L, Pimenta JM, Poole C, Jenkins D, Smith JS. Persistent human papillomavirus infection and cervical neoplasia: a systematic review and meta‐analysis. Am J Epidemiol. 2008;168(2):123‐137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 79. Pierce Campbell CM, Kreimer AR, Lin HY, et al. Long‐term persistence of oral human papillomavirus type 16: the HPV infection in men (HIM) study. Cancer Prev Res. 2015;8(3):190‐196. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 80. Cruz‐Gregorio A, Manzo‐Merino J, Lizano M. Cellular redox, cancer and human papillomavirus. Virus Res. 2018;246:35‐45. [DOI] [PubMed] [Google Scholar]
  • 81. Strander B, Ryd W, Wallin KL, et al. Does HPV‐status 6‐12 months after treatment of high grade dysplasia in the uterine cervix predict long term recurrence? Eur J Cancer. 2007;43(12):1849‐1855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 82. Beachler DC, Lang Kuhs KA, Struijk L, et al. The natural history of oral human papillomavirus in young costa rican women. Sex Transm Dis. 2017;44(7):442‐449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 83. D'Souza G, Fakhry C, Sugar EA, et al. Six‐month natural history of oral versus cervical human papillomavirus infection. Int J Cancer. 2007;121(1):143‐150. [DOI] [PubMed] [Google Scholar]
  • 84. Zhang C, Liu F, Pan Y, et al. Incidence and clearance of oral human papillomavirus infection: a population‐based cohort study in rural China. Oncotarget. 2017;8(35):59831‐59844. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 85. Hang D, Liu F, Liu M, 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(10):2101‐2110. [DOI] [PubMed] [Google Scholar]
  • 86. D'Souza G, Clemens G, Strickler HD, et al. Long‐term persistence of oral HPV over 7 years of follow‐up. JNCI Cancer Spectr. 2020;4(5):pkaa047. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 87. Paaso AE, Louvanto K, Syrjanen KJ, et al. Lack of type‐specific concordance between human papillomavirus (HPV) serology and HPV DNA detection in the uterine cervix and oral mucosa. J Gen Virol. 2011;92(Pt 9):2034‐2046. [DOI] [PubMed] [Google Scholar]
  • 88. Syrjanen K, Shabalova I, Naud P, et al. Persistent high‐risk human papillomavirus infections and other end‐point markers of progressive cervical disease among women prospectively followed up in the new independent states of the former soviet union and the Latin american screening study cohorts. Int J Gynecol Cancer. 2009;19(5):934‐942. [DOI] [PubMed] [Google Scholar]
  • 89. Syrjanen K, Shabalova I, Naud P, et al. Risk estimates for persistent high‐risk human papillomavirus infections as surrogate endpoints of progressive cervical disease critically depend on reference category: analysis of the combined prospective cohort of the new independent states of the former soviet union and Latin american screening studies. Int J STD AIDS. 2011;22(6):315‐323. [DOI] [PubMed] [Google Scholar]
  • 90. Giuliano AR, Lee JH, Fulp W, et al. Incidence and clearance of genital human papillomavirus infection in men (HIM): a cohort study. Lancet. 2011;377(9769):932‐940. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 91. Rodier C, Lapointe A, Coutlee F, et al. Juvenile respiratory papillomatosis: risk factors for severity. J Med Virol. 2013;85(8):1447‐1458. [DOI] [PubMed] [Google Scholar]
  • 92. Rautava J, Willberg J, Louvanto K, et al. Prevalence, genotype distribution and persistence of human papillomavirus in oral mucosa of women: a six‐year follow‐up study. PLoS One. 2012;7(8):e42171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 93. Ahn SM, Chan JY, Zhang Z, et al. Saliva and plasma quantitative polymerase chain reaction‐based detection and surveillance of human papillomavirus‐related head and neck cancer. JAMA Otolaryngol Head Neck Surg. 2014;140(9):846‐854. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 94. Kero K, Rautava J, Syrjanen K, Willberg J, Grenman S, Syrjanen S. Smoking increases oral HPV persistence among men: 7‐year follow‐up study. Eur J Clin Microbiol Infect Dis. 2014;33(1):123‐133. [DOI] [PubMed] [Google Scholar]
  • 95. Doorbar J. Host control of human papillomavirus infection and disease. Best Pract Res Clin Obstet Gynaecol. 2018;47:27‐41. [DOI] [PubMed] [Google Scholar]
  • 96. Stanley MA, Sterling JC. Host responses to infection with human papillomavirus. Curr Probl Dermatol. 2014;45:58‐74. [DOI] [PubMed] [Google Scholar]
  • 97. McKinney CC, Hussmann KL, McBride AA. The role of the DNA damage response throughout the papillomavirus life cycle. Viruses. 2015;7(5):2450‐2469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 98. van Esch EM, van Poelgeest MI, Trimbos JB, Fleuren GJ, Jordanova ES, van der Burg SH. Intraepithelial macrophage infiltration is related to a high number of regulatory T cells and promotes a progressive course of HPV‐induced vulvar neoplasia. Int J Cancer. 2015;136(4):E85‐E94. [DOI] [PubMed] [Google Scholar]
  • 99. Pugliese DB, Bruzzesi G, Montaldo C, et al. Oral prevalence and clearance of oncogenic human papilloma virus in a rehabilitation community for substance abusers in Italy: a case of behavioral correction? J Oral Pathol Med. 2015;44(9):728‐733. [DOI] [PubMed] [Google Scholar]
  • 100. Haukioja A, Tervahartiala T, Sorsa T, Syrjanen S. Persistent oral human papillomavirus (HPV) infection is associated with low salivary levels of matrix metalloproteinase 8 (MMP‐8). J Clin Virol. 2017;97:4‐9. [DOI] [PubMed] [Google Scholar]

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