Abstract
Human papillomavirus (HPV) infections are associated with sexual behavior. Changes in the sexual habits of couples and their impact on male genital and oral HPV infections were determined during 7 years of follow-up (FU). At baseline and 7 years FU, urethral, semen/penile, and oral samples were collected from 46 men and cervical and oral samples of their spouses for HPV DNA detection. Demographic data and risk factors of spouses were recorded by questionnaire at both time points and analyzed for concordance. HPV genotyping was done with the Multimetrix® kit. At baseline, 29.5 % of the male genital and 11 % of their oral samples tested positive. Incident genital HPV infection was found in 23 % and oral infection in 10.9 % of men. Genotype-specific persistence was detected in one man (HPV53) in genital samples. Moderate to almost perfect concordance of changes in sexual habits during FU among spouses were found. Changing partners [p = 0.028; odds ratio (OR) = 15; 95 % confidence interval (CI) 1.355–166.054] and marital status (p = 0.001; 95 % CI 0.000–0.002) increased the risk of incident genital HPV infections. The overall outcome of genital HPV disease in men was linked to the frequency of sexual intercourse (p = 0.023; 95 % CI 0.019–0.026) and changes in marital status (p = 0.022; 95 % CI 0.019–0.026), while oral HPV infections were associated with the number of sexual partners (p = 0.047; 95 % CI 0.041–0.052). Taken together, asymptomatic genital HPV infections among the men were common. The risk of incident genital HPV infections increased among men reporting a change of sexual partner during FU, implicating that a stable marital relationship protects against oral and genital HPV infection.
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References
Syrjänen K, Syrjänen S (2000) Papillomavirus infections in human disease. Wiley, New York, 615 pp
Cubie HA (2013) Diseases associated with human papillomavirus infection. Virology 445(1–2):21–34. doi:10.1016/j.virol.2013.06.007
Rintala MA, Grénman SE, Pöllänen PP et al (2004) Detection of high-risk HPV DNA in semen and its association with the quality of semen. Int J STD AIDS 15:740–743
Graziottin A, Serafini A (2009) HPV infection in women: psychosexual impact of genital warts and intraepithelial lesions. J Sex Med 6:633–645. doi:10.1111/j.1743-6109.2008.01151.x
Nyitray AG, Menezes L, Lu B et al (2012) Genital human papillomavirus (HPV) concordance in heterosexual couples. J Infect Dis 206:202–211. doi:10.1093/infdis/jis327
Reiter PL, Pendergraft WF 3rd, Brewer NT (2010) Meta-analysis of human papillomavirus infection concordance. Cancer Epidemiol Biomarkers Prev 19:2916–2931. doi:10.1158/1055-9965.EPI-10-0576
Nielson CM, Harris RB, Dunne EF et al (2007) Risk factors for anogenital human papillomavirus infection in men. J Infect Dis 196:1137–1145
Bleeker MC, Berkhof J, Hogewoning CJ et al (2005) HPV type concordance in sexual couples determines the effect of condoms on regression of flat penile lesions. Br J Cancer 92:1388–1392
Mbulawa ZZ, Coetzee D, Marais DJ et al (2009) Genital human papillomavirus prevalence and human papillomavirus concordance in heterosexual couples are positively associated with human immunodeficiency virus coinfection. J Infect Dis 199:1514–1524. doi:10.1086/598220
Tobian AA, Kong X, Gravitt PE et al (2011) Male circumcision and anatomic sites of penile high-risk human papillomavirus in Rakai, Uganda. Int J Cancer 129:2970–2975. doi:10.1002/ijc.25957
Widdice LE, Breland DJ, Jonte J et al (2010) Human papillomavirus concordance in heterosexual couples. J Adolesc Health 47:151–159. doi:10.1016/j.jadohealth.2010.01.006
Rintala MA, Grénman SE, Puranen MH et al (2005) Transmission of high-risk human papillomavirus (HPV) between parents and infant: a prospective study of HPV in families in Finland. J Clin Microbiol 43:376–381
Rintala M, Grénman S, Puranen M et al (2006) Natural history of oral papillomavirus infections in spouses: a prospective Finnish HPV Family Study. J Clin Virol 35:89–94
Louvanto K, Rintala MA, Syrjänen KJ et al (2010) Genotype-specific persistence of genital human papillomavirus (HPV) infections in women followed for 6 years in the Finnish Family HPV Study. J Infect Dis 202:436–444. doi:10.1086/653826
Miller SA, Dykes DD, Polesky HF (1988) A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16:1215
Snijders PJ, van den Brule AJ, Schrijnemakers HF et al (1990) The use of general primers in the polymerase chain reaction permits the detection of a broad spectrum of human papillomavirus genotypes. J Gen Virol 71:173–181
Cogliano V, Baan R, Straif K et al (2005) Carcinogenicity of human papillomaviruses. Lancet Oncol 6:204
Schmitt M, Bravo IG, Snijders PJ et al (2006) Bead-based multiplex genotyping of human papillomaviruses. J Clin Microbiol 44:504–512
Giuliano AR, Nielson CM, Flores R et al (2007) The optimal anatomic sites for sampling heterosexual men for human papillomavirus (HPV) detection: the HPV detection in men study. J Infect Dis 196:1146–1152
D’Hauwers K, Depuydt C, Bogers JP et al (2007) Urine versus brushed samples in human papillomavirus screening: study in both genders. Asian J Androl 9:705–710
Louvanto K, Rintala MA, Syrjänen KJ et al (2011) Incident cervical infections with high- and low-risk human papillomavirus (HPV) infections among mothers in the prospective Finnish Family HPV Study. BMC Infect Dis 22:179. doi:10.1186/1471-2334-11-179
Giuliano AR, Lee JH, Fulp W et al (2011) Incidence and clearance of genital human papillomavirus infection in men (HIM): a cohort study. Lancet 377:932–940. doi:10.1016/S0140-6736(10)62342-2
Giuliano AR, Anic G, Nyitray AG (2010) Epidemiology and pathology of HPV disease in males. Gynecol Oncol 117:S15–S19. doi:10.1016/j.ygyno.2010.01.026
Kero K, Rautava J, Syrjänen K et al (2011) Human papillomavirus genotypes in male genitalia and their concordance among pregnant spouses participating in the Finnish Family HPV study. J Sex Med 8:2522–2531. doi:10.1111/j.1743-6109.2011.02378.x
Abalos AT, Harris RB, Nyitray AG et al (2012) Human papillomavirus type distribution among heterosexual couples. J Low Genit Tract Dis 16:10–15. doi:10.1097/LGT.0b013e31822a8404
Parada R, Morales R, Giuliano AR et al. (2010) Prevalence, concordance and determinants of human papillomavirus infection among heterosexual partners in a rural region in central Mexico. BMC Infect Dis 10:223. doi:10.1186/1471-2334-10-223
D’Souza G, Fakhry C, Sugar EA et al (2007) Six-month natural history of oral versus cervical human papillomavirus infection. Int J Cancer 121:143–150
Bell MC, Schmidt-Grimminger D, Jacobsen C et al (2011) Risk factors for HPV infection among American Indian and White women in the Northern Plains. Gynecol Oncol 121:532–536. doi:10.1016/j.ygyno.2011.02.032
Kreimer AR, Villa A, Nyitray AG et al (2011) The epidemiology of oral HPV infection among a multinational sample of healthy men. Cancer Epidemiol Biomarkers Prev 20:172–182. doi:10.1158/1055-9965.EPI-10-0682
Kero K, Rautava J, Syrjänen K et al (2014) Smoking increases oral HPV persistence among men: 7-year follow-up study. Eur J Clin Microbiol Infect Dis 33:123–133
Acknowledgments
The authors would like to thank Dr. Marjut Rintala, Dr. Virpi Rantanen, and midwife Elisa Hovimäki for participating in the enrolment of the women in the Finnish Family HPV (FFHPV) study and their clinical follow-up. The skillful technical assistance of Mrs. Tatjana Pescova, Mariia Henttinen, and Keitlin Adel is gratefully acknowledged. The FFHPV study has been supported by the Academy of Finland, Finnish Cancer Foundation, Government Special Foundation (EVO) to Turku University Hospital, the Finnish Society against Sexually Transmitted Infection, and Orion Corporation
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Kero, K.M., Rautava, J., Syrjänen, K. et al. Stable marital relationship protects men from oral and genital HPV infections. Eur J Clin Microbiol Infect Dis 33, 1211–1221 (2014). https://doi.org/10.1007/s10096-014-2061-7
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DOI: https://doi.org/10.1007/s10096-014-2061-7