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REVIEW

Penises not required: a systematic review of the potential for human papillomavirus horizontal transmission that is non-sexual or does not include penile penetration

Zhiyue Liu A , Tasnuva Rashid A and Alan G. Nyitray A B C
+ Author Affiliations
- Author Affiliations

A Department of Epidemiology, Human Genetics and Environmental Sciences, School of Public Health, The University of Texas Health Science Center at Houston, 1200 Pressler Street, Houston, TX 77030, USA.

B Center for Infectious Diseases, The University of Texas Health Science Center at Houston, 1200 Pressler Street, Houston, TX 77030, USA.

C Corresponding author. Email: alan.g.nyitray@uth.tmc.edu

Sexual Health 13(1) 10-21 https://doi.org/10.1071/SH15089
Submitted: 1 May 2015  Accepted: 26 July 2015   Published: 5 October 2015

Abstract

The primary mode of human papillomavirus (HPV) transmission is through penetrative sex; however, there is evidence of other modes of transmission. No systematic review was found that focussed on HPV horizontal transmission that is not penocentric. A systematic review of the literature by searching Medline (Ovid), PubMed (NLM) and Embase (Ovid) was conducted to retrieve articles published from 1946 to March 2014. Studies that suggested evidence of non-sexual or non-penetrative sexual transmission of α-HPV genotypes were included. After review of 2061 titles and abstracts, 51 studies were abstracted. Fifteen studies examined HPV fomites from medical settings or public environments, and 36 examined HPV in humans. Human papillomavirus DNA was detected in the genital tract of female virgins, with prevalence estimates ranging from 0% to 51.1%. HPV transmission from hands to genitals or genitals to hands was reported for both sexes and heterosexual couples. Other studies commonly found HPV on surfaces in medical settings and public environments. Further studies on non-sexual and non-penetrative sexual transmission are needed to understand the complexity of HPV transmission. Health-care policies may need to be reassessed/established to ensure the safety of medical instruments and to reduce the risk of HPV nosocomial infection.

Additional keywords: environment, fomites, hand, nosocomial, penetrative sex, transmission, virgins.


References

[1]  IARC Working Group on the Evaluation of Carcinogenic Risks to Humans Biological agents. Volume 100 B. A review of human carcinogens: human papillomaviruses. IARC Monog Eval Carc 2012; 100 255–313.

[2]  IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Human papillomaviruses. IARC Monog Eval Carc 2007; 90 136–65.

[3]  Doorbar J, Quint W, Banks L, Bravo IG, Stoler M, Broker TR, et al The biology and life-cycle of human papillomaviruses. Vaccine 2012; 30 F55–70.
The biology and life-cycle of human papillomaviruses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhsl2ju7nE&md5=98f29afbd58630a8efd25eb158b5fad2CAS | 23199966PubMed |

[4]  Martin-Hernan F, Sanchez-Hernandez JG, Cano J, Campo J, del Romero J. Oral cancer, HPV infection and evidence of sexual transmission. Med Oral Patol Oral 2013; 18 e439–44.
Oral cancer, HPV infection and evidence of sexual transmission.Crossref | GoogleScholarGoogle Scholar |

[5]  Freitas AC, Mariz FC, Silva MA, Jesus AL. Human papillomavirus vertical transmission: review of current data. Clin Infect Dis 2013; 56 1451–6.
Human papillomavirus vertical transmission: review of current data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXntFWntL4%3D&md5=9145dda928f7663bb84a771296518a0fCAS | 23392393PubMed |

[6]  VonVille HM. Systematic review workbook for tracking search strategies & results and screening titles & abstracts. 2014. Available online at: http://libguides.sph.uth.tmc.edu/excel_SR_workbook [verified March 2014].

[7]  Beznos G, Coates V, Focchi J, Omar HA. Biomolecular study of the correlation between papillomatosis of the vulvar vestibule in adolescents and human papillomavirus. ScientificWorldJournal 2006; 6 628–36.
Biomolecular study of the correlation between papillomatosis of the vulvar vestibule in adolescents and human papillomavirus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xot1OqtL0%3D&md5=4d5f6fb3009a696246ba683104ad04a5CAS | 16832565PubMed |

[8]  Bumbuliene Z, Alisauskas J, Sepetiene A. High-risk HPV infection in sexually active and non active young women. Cent Eur J Med 2011; 6 456–62.

[9]  Doerfler D, Bernhaus A, Kottmel A, Sam C, Koelle D, Joura EA. Human papilloma virus infection prior to coitarche. Am J Obstet Gynecol 2009; 200 487.e1–5.
Human papilloma virus infection prior to coitarche.Crossref | GoogleScholarGoogle Scholar |

[10]  Fairley CK, Chen S, Tabrizi SN, Leeton K, Quinn MA, Garland SM. The absence of genital human papillomavirus DNA in virginal women. Int J STD AIDS 1992; 3 414–7.
| 1:STN:280:DyaK3s7mtVejsA%3D%3D&md5=9df1ae3bce79c567972998c2f50303c4CAS | 1337472PubMed |

[11]  Ji J, Sun HK, Smith JS, Wang H, Esser MT, Hu S, et al Seroprevalence of human papillomavirus types 6, 11, 16 and 18 in Chinese women. BMC Infect Dis 2012; 12 137–46.
Seroprevalence of human papillomavirus types 6, 11, 16 and 18 in Chinese women.Crossref | GoogleScholarGoogle Scholar | 22715915PubMed |

[12]  Marrazzo JM, Koutsky LA, Kiviat NB, Kuypers JM, Stine K. Papanicolaou test screening and prevalence of genital human papillomavirus among women who have sex with women. Am J Public Health 2001; 91 947–52.
Papanicolaou test screening and prevalence of genital human papillomavirus among women who have sex with women.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MzhvVyqsA%3D%3D&md5=e7675a12c15d237f8fca7acef2a5e8f3CAS | 11392939PubMed |

[13]  Oh JK, Ju YH, Franceschi S, Quint W, Shin HR. Acquisition of new infection and clearance of type-specific human papillomavirus infections in female students in Busan, South Korea: a follow-up study. BMC Infect Dis 2008; 8 1–6.
Acquisition of new infection and clearance of type-specific human papillomavirus infections in female students in Busan, South Korea: a follow-up study.Crossref | GoogleScholarGoogle Scholar |

[14]  Pao CC, Tsai PL, Chang YL, Hsieh TT, Jin JY. Possible non-sexual transmission of genital human papillomavirus infections in young women. Eur J Clin Microbiol 1993; 12 221–3.
Possible non-sexual transmission of genital human papillomavirus infections in young women.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3s3osFWrtA%3D%3D&md5=9d9f1451aa258cb43f5158ce24134cbaCAS |

[15]  Peters AA, Trimbos JB. The absence of human papilloma virus (HPV) related parameters in sexually non-active women. Eur J Gynaecol Oncol 1994; 15 43–5.
| 1:STN:280:DyaK2c3msFOqsQ%3D%3D&md5=9cc5d3ebc8f72cb7eecb4eac7614505eCAS | 8206070PubMed |

[16]  Rylander E, Ruusuvaara L, Almstromer MW, Evander M, Wadell G. The absence of vaginal human papillomavirus 16 DNA in women who have not experienced sexual intercourse. Obstet Gynecol 1994; 83 735–7.
| 1:STN:280:DyaK2c3hvVShsg%3D%3D&md5=359fce12c1debc519707f9a5ae1e31a2CAS | 8164934PubMed |

[17]  Shew ML, Weaver B, Tu W, Tong Y, Fortenberry JD, Brown DR. High frequency of human papillomavirus detection in the vagina before first vaginal intercourse among females enrolled in a longitudinal cohort study. J Infect Dis 2013; 207 1012–5.
High frequency of human papillomavirus detection in the vagina before first vaginal intercourse among females enrolled in a longitudinal cohort study.Crossref | GoogleScholarGoogle Scholar | 23242538PubMed |

[18]  Tay SK, Oon LL. Prevalence of cervical human papillomavirus infection in healthy women is related to sexual behaviours and educational level: a cross-sectional study. Int J STD AIDS 2014; 25 1013–21.
| 24648316PubMed |

[19]  Shimada T, Miyashita M, Miura S, Nakayama D, Miura K, Fukuda M, et al Genital human papilloma virus infection in mentally-institutionalized virgins. Gynecol Oncol 2007; 106 488–9.
Genital human papilloma virus infection in mentally-institutionalized virgins.Crossref | GoogleScholarGoogle Scholar | 17532028PubMed |

[20]  Shin HR, Lee DH, Herrero R, Smith JS, Vaccarella S, Hong SH, et al Prevalence of human papillomavirus infection in women in Busan, South Korea. Int J Cancer 2003; 103 413–21.
Prevalence of human papillomavirus infection in women in Busan, South Korea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXht1yitQ%3D%3D&md5=6e4807f6761770b618fd0c75bb84ac86CAS | 12471626PubMed |

[21]  Tay SK, Ho TH, Lim-Tan SK. Is genital human papillomavirus infection always sexually transmitted? Aust N Z J Obstet Gynaecol 1990; 30 240–2.
Is genital human papillomavirus infection always sexually transmitted?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3M%2Fns1Okuw%3D%3D&md5=627b47a683fa1bdacb87fbd3db52a6bcCAS | 2256864PubMed |

[22]  Widdice LE, Brown DR, Bernstein DI, Ding L, Patel D, Shew M, et al Prevalence of human papillomavirus infection in young women receiving the first quadrivalent vaccine dose. Arch Pediatr Adolesc Med 2012; 166 774–6.
Prevalence of human papillomavirus infection in young women receiving the first quadrivalent vaccine dose.Crossref | GoogleScholarGoogle Scholar | 22869412PubMed |

[23]  Winer RL, Hughes JP, Feng Q, Xi LF, Cherne S, O’Reilly S, et al Detection of genital HPV types in fingertip samples from newly sexually active female university students. Cancer Epidem Biomar 2010; 19 1682–5.
Detection of genital HPV types in fingertip samples from newly sexually active female university students.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXosFCkurY%3D&md5=83c2a80cb20c58520b2afa715f813fceCAS |

[24]  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; 157 218–26.
Genital human papillomavirus infection: incidence and risk factors in a cohort of female university students.Crossref | GoogleScholarGoogle Scholar | 12543621PubMed |

[25]  Thilagavathi A, Shanmughapriya S, Vinodhini K, Das BC, Natarajaseenivasan K. Prevalence of human papillomavirus (HPV) among college going girls using self collected urine samples from Tiruchirappalli, Tamilnadu. Arch Gynecol Obstet 2012; 286 1483–6.
Prevalence of human papillomavirus (HPV) among college going girls using self collected urine samples from Tiruchirappalli, Tamilnadu.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38fnsVeksQ%3D%3D&md5=42c78755b2774a7274834b4143b99093CAS | 22886326PubMed |

[26]  Frega A, Cenci M, Stentella P, Cipriano L, De Ioris A, Alderisio M, et al Human papillomavirus in virgins and behaviour at risk. Cancer Lett 2003; 194 21–4.
Human papillomavirus in virgins and behaviour at risk.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtFCjs7g%3D&md5=e87a2b32f79b395565c3eb610901d62cCAS | 12706855PubMed |

[27]  Partridge JM, Hughes JP, Feng Q, Winer RL, Weaver BA, Xi LF, et al Genital human papillomavirus infection in men: incidence and risk factors in a cohort of university students. J Infect Dis 2007; 196 1128–36.
Genital human papillomavirus infection in men: incidence and risk factors in a cohort of university students.Crossref | GoogleScholarGoogle Scholar | 17955430PubMed |

[28]  Widdice LE, Breland DJ, Jonte J, Farhat S, Ma Y, Leonard AC, et al Human papillomavirus concordance in heterosexual couples. J Adolesc Health 2010; 47 151–9.
Human papillomavirus concordance in heterosexual couples.Crossref | GoogleScholarGoogle Scholar | 20638007PubMed |

[29]  Widdice L, Ma Y, Jonte J, Farhat S, Breland D, Shiboski S, et al Concordance and transmission of human papillomavirus within heterosexual couples observed over short intervals. J Infect Dis 2013; 207 1286–94.
Concordance and transmission of human papillomavirus within heterosexual couples observed over short intervals.Crossref | GoogleScholarGoogle Scholar | 23319742PubMed |

[30]  Hernandez BY, Wilkens LR, Zhu X, Thompson P, McDuffie K, Shvetsov YB, et al Transmission of human papillomavirus in heterosexual couples. Emerg Infect Dis 2008; 14 888–94.
Transmission of human papillomavirus in heterosexual couples.Crossref | GoogleScholarGoogle Scholar | 18507898PubMed |

[31]  Sonnex C, Strauss S, Gray JJ. Detection of human papillomavirus DNA on the fingers of patients with genital warts. Sex Transm Infect 1999; 75 317–9.
Detection of human papillomavirus DNA on the fingers of patients with genital warts.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c%2FotlOhug%3D%3D&md5=84adca942cd51e28b0c8b7c912cb852fCAS | 10616355PubMed |

[32]  Forslund O, Nordin P, Hansson BG. Mucosal human papillomavirus types in squamous cell carcinomas of the uterine cervix and subsequently on fingers. Br J Dermatol 2000; 142 1148–53.
Mucosal human papillomavirus types in squamous cell carcinomas of the uterine cervix and subsequently on fingers.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3cvgvFSjtw%3D%3D&md5=5b036a2a16323620575c598c4322b0ebCAS | 10848738PubMed |

[33]  Hunt R, Hwa C, Tzu J, Patel R, Tyring SK, Stein J. Multiple human papillomavirus-16 associated digital squamous-cell carcinomas in an immunocompetent woman with prior human papillomavirus-related genital carcinoma. Dermatol Online J 2011; 17 20
| 22031646PubMed |

[34]  Hernandez BY, Shvetsov YB, Goodman MT, Wilkens LR, Thompson PJ, Zhu X, et al Genital and extra-genital warts increase the risk of asymptomatic genital human papillomavirus infection in men. Sex Transm Infect 2011; 87 391–5.
Genital and extra-genital warts increase the risk of asymptomatic genital human papillomavirus infection in men.Crossref | GoogleScholarGoogle Scholar | 21602516PubMed |

[35]  Jin F, Prestage GP, Kippax SC, Pell CM, Donovan B, Templeton DJ, et al Risk factors for genital and anal warts in a prospective cohort of HIV-negative homosexual men: the HIM study. Sex Transm Dis 2007; 34 488–93.
| 17108849PubMed |

[36]  Handley J, Dinsmore W, Maw R, Corbett R, Burrows D, Bharucha H, et al Anogenital warts in prepubertal children; sexual abuse or not? Int J STD AIDS 1993; 4 271–9.
| 1:STN:280:DyaK2c%2Fjt1KksQ%3D%3D&md5=62f6857d492b0da1987c2d04eb54b703CAS | 8218514PubMed |

[37]  Rock B, Naghashfar Z, Barnett N, Buscema J, Woodruff JD, Shah K. Genital tract papillomavirus infection in children. Arch Dermatol 1986; 122 1129–32.
Genital tract papillomavirus infection in children.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2s%2FisVKltw%3D%3D&md5=c81251ece2d1fcb174473eb9f523a00fCAS | 3021069PubMed |

[38]  Fleming KA, Venning V, Evans M. DNA typing of genital warts and diagnosis of sexual abuse of children. Lancet 1987; 330 454
DNA typing of genital warts and diagnosis of sexual abuse of children.Crossref | GoogleScholarGoogle Scholar |

[39]  Klinglmair G, Pichler R, Zelger B, Dogan HS, Becker T, Esterbauer J, et al Prevalence of the human papillomavirus (HPV) expression of the inner prepuce in asymptomatic boys and men. World J Urol 2013; 31 1389–94.
Prevalence of the human papillomavirus (HPV) expression of the inner prepuce in asymptomatic boys and men.Crossref | GoogleScholarGoogle Scholar | 23239104PubMed |

[40]  Myhre AK, Dalen A, Berntzen K, Bratlid D. Anogenital human papillomavirus in non-abused preschool children. Acta Paediatr 2003; 92 1445–52.
Anogenital human papillomavirus in non-abused preschool children.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2c%2Fot1antQ%3D%3D&md5=41ef52e2696d5931a11e03ab4ca61d06CAS | 14971797PubMed |

[41]  McCance DJ, Campion MJ, Baram A, Singer A. Risk of transmission of human papillomavirus by vaginal specula. Lancet 1986; 328 816–7.
Risk of transmission of human papillomavirus by vaginal specula.Crossref | GoogleScholarGoogle Scholar |

[42]  Kac G, Podglajen I, Si-Mohamed A, Rodi A, Grataloup C, Meyer G. Evaluation of ultraviolet C for disinfection of endocavitary ultrasound transducers persistently contaminated despite probe covers. Infect Control Hosp Epidemiol 2010; 31 165–70.
Evaluation of ultraviolet C for disinfection of endocavitary ultrasound transducers persistently contaminated despite probe covers.Crossref | GoogleScholarGoogle Scholar | 20025531PubMed |

[43]  Casalegno JS, Le Bail Carval K, Eibach D, Valdeyron ML, Lamblin G, Jacquemoud H, et al High risk HPV contamination of endocavity vaginal ultrasound probes: an underestimated route of nosocomial infection? PLoS One 2012; 7 1–4.
High risk HPV contamination of endocavity vaginal ultrasound probes: an underestimated route of nosocomial infection?Crossref | GoogleScholarGoogle Scholar |

[44]  Ma STC, Yeung AC, Chan PKS, Graham CA. Transvaginal ultrasound probe contamination by the human papillomavirus in the emergency department. Emerg Med J 2013; 30 472–5.
Transvaginal ultrasound probe contamination by the human papillomavirus in the emergency department.Crossref | GoogleScholarGoogle Scholar |

[45]  Ferenczy A, Bergeron C, Richart RM. Human papillomavirus DNA in fomites on objects used for the management of patients with genital human papillomavirus infections. Obstet Gynecol 1989; 74 950–4.
| 1:STN:280:DyaK3c%2Fmslelug%3D%3D&md5=ca60cf27b65d2521abb701ae695fd3b0CAS | 2555753PubMed |

[46]  Ilmarinen T, Auvinen E, Hiltunen-Back E, Ranki A, Aaltonen L, Pitkaranta A. Transmission of human papillomavirus DNA from patient to surgical masks, gloves and oral mucosa of medical personnel during treatment of laryngeal papillomas and genital warts. Eur Arch Otorhinolaryngol 2012; 269 2367–71.
Transmission of human papillomavirus DNA from patient to surgical masks, gloves and oral mucosa of medical personnel during treatment of laryngeal papillomas and genital warts.Crossref | GoogleScholarGoogle Scholar | 22588197PubMed |

[47]  Kashima HK, Kessis T, Mounts P, Shah K. Polymerase chain reaction identification of human papillomavirus DNA in CO2 laser plume from recurrent respiratory papillomatosis. Otolaryng Head Neck 1991; 104 191–5.
| 1:STN:280:DyaK3M7nvFOgtQ%3D%3D&md5=8541eb6f841973da555780e4ca142c21CAS |

[48]  Hallmo P, Naess O. Laryngeal papillomatosis with human papillomavirus DNA contracted by a laser surgeon. Eur Arch Otorhinolaryngol 1991; 248 425–7.
Laryngeal papillomatosis with human papillomavirus DNA contracted by a laser surgeon.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK38%2Fot1KltA%3D%3D&md5=ec43aa780b20692b1708a5030b2b626aCAS | 1660719PubMed |

[49]  Garden JM, O’Banion MK, Shelnitz LS, Pinski KS, Bakus AD, Reichmann ME, et al Papillomavirus in the vapor of carbon dioxide laser-treated verrucae. JAMA 1988; 259 1199–202.
Papillomavirus in the vapor of carbon dioxide laser-treated verrucae.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1c7hvFCjug%3D%3D&md5=0d1d0f83de88237e6c177808706303c8CAS | 2828703PubMed |

[50]  Bergbrant I, Samuelsson L, Olofsson S, Jonassen F,, Ricksten A. Polymerase chain reaction for monitoring human papillomavirus contamination of medical personnel during treatment of genital warts with CO2 laser and electrocoagulation. Acta Derm Venereol 1994; 74 393–5.
| 1:STN:280:DyaK2M7hslCgtg%3D%3D&md5=ed704feed2459830ed68fe61ab51f385CAS | 7817682PubMed |

[51]  Andre P, Orth G, Evenou P, Guillaume JC, Avril MF. Risk of papillomavirus infection in carbon dioxide laser treatment of genital lesions. J Am Acad Dermatol 1990; 22 131–2.
Risk of papillomavirus infection in carbon dioxide laser treatment of genital lesions.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3c7jtFalsQ%3D%3D&md5=7459a774437341714f204abc0a99ac88CAS | 2153715PubMed |

[52]  Lobraico RV, Schifano MJ, Brader KR. Acquired HPV lesions compared in laser and nonlaser users. J Gynecol Surg 1989; 5 77–85.
Acquired HPV lesions compared in laser and nonlaser users.Crossref | GoogleScholarGoogle Scholar |

[53]  Hughes PSH, Hughes AP. Absence of human papillomavirus DNA in the plume of erbium: YAG laser-treated warts. J Am Acad Dermatol 1998; 38 426–8.
Absence of human papillomavirus DNA in the plume of erbium: YAG laser-treated warts.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c7nvVyntA%3D%3D&md5=df56531a970cc5c15abd35ba3b8ded27CAS |

[54]  Strauss S, Sastry P, Sonnex C, Edwards S, Gray J. Contamination of environmental surfaces by genital human papillomaviruses. Sex Transm Infect 2002; 78 135–8.
Contamination of environmental surfaces by genital human papillomaviruses.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38zjvVejsg%3D%3D&md5=7e13067d2fb93151279d6f398631dccfCAS | 12081177PubMed |

[55]  Strauss S, Stephen H, Sonnex C, Gray J. Contamination of environmental surfaces by genital human papillomaviruses (HPV): a follow up study. Sex Transm Infect 2003; 79 426–7.
Contamination of environmental surfaces by genital human papillomaviruses (HPV): a follow up study.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3srgslKgug%3D%3D&md5=5e50e2e958bb1f4751519334e34bc8cbCAS | 14573848PubMed |

[56]  Smelov V, Eklund C, Arroyo Muhr LS, Hultin E, Dillner J. Are human papillomavirus DNA prevalences providing high-flying estimates of infection? An international survey of HPV detection on environmental surfaces. Sex Transm Infect 2013; 89 627
Are human papillomavirus DNA prevalences providing high-flying estimates of infection? An international survey of HPV detection on environmental surfaces.Crossref | GoogleScholarGoogle Scholar | 24191269PubMed |

[57]  Anderson TA, Schick V, Herbenick D, Dodge B, Fortenberry JD. A study of human papillomavirus on vaginally inserted sex toys, before and after cleaning, among women who have sex with women and men. Sex Transm Infect 2014; 90 529–31.
A study of human papillomavirus on vaginally inserted sex toys, before and after cleaning, among women who have sex with women and men.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2cnktFOrsw%3D%3D&md5=f1854dfead1fee12192183aef1fea6ffCAS | 24739872PubMed |

[58]  Winer RL, Hughes JP, Feng Q, Xi LF, Cherne S, O’Reilly S, Kiviat NB, Koutsky LA. Early natural history of incident, type-specific human papillomavirus infections in newly sexually active young women. Cancer Epidemiol Biomarkers Prev 2011; 20 699–707.
Early natural history of incident, type-specific human papillomavirus infections in newly sexually active young women.Crossref | GoogleScholarGoogle Scholar | 21173170PubMed |

[59]  Coutlee F, Hankins C, Lapointe N. Comparison between vaginal tampon and cervicovaginal lavage specimen collection for detection of human papillomavirus DNA by the polymerase chain reaction. The Canadian Women’s HIV Study Group. J Med Virol 1997; 51 42–7.
Comparison between vaginal tampon and cervicovaginal lavage specimen collection for detection of human papillomavirus DNA by the polymerase chain reaction. The Canadian Women’s HIV Study Group.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s7ktVCltQ%3D%3D&md5=41c09df8377ff3ecda490fba607b7a3fCAS | 8986948PubMed |

[60]  Roden RB, Lowy DR, Schiller JT. Papillomavirus is resistant to desiccation. J Infect Dis 1997; 176 1076–9.
Papillomavirus is resistant to desiccation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2svnt1entA%3D%3D&md5=5af14bd48a05ae1659969331c6581d95CAS | 9333171PubMed |

[61]  Ding DC, Chang YC, Liu HW, Chu TY. Long-term persistence of human papillomavirus in environments. Gynecol Oncol 2011; 121 148–51.
Long-term persistence of human papillomavirus in environments.Crossref | GoogleScholarGoogle Scholar | 21208649PubMed |

[62]  Nyitray AG, Lin HY, Fulp WJ, Chang M, Menezes L, Lu B, et al The role of monogamy and duration of heterosexual relationships in human papillomavirus transmission. J Infect Dis 2014; 209 1007–15.
The role of monogamy and duration of heterosexual relationships in human papillomavirus transmission.Crossref | GoogleScholarGoogle Scholar | 24253288PubMed |