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 Infectious Diseases

Mikio Namiki⁶  Atsushi Mizokami⁶  Yasuhide Kitagawa⁶  Toshiyuki Sasagawa⁷  Masayoshi Shimamura¹  Yasunori Ishii²  Kazuyoshi Nakashima⁴  Yoshitomo Kobori⁵  Akira Wakatsuki³  Shohei Kawaguchi⁶  Kazuyoshi Shigehara¹  Kazufumi Nakashima⁶ 

[1] Department of Urology, Ishikawa Prefectural Central Hospital, Kanazawa, Ishikawa, Japan;Ishii Clinic, Saitama City, Saitama, Japan;Wakatsuki Clinic, Osaka City, Osaka, Japan;Nakashima Clinic, Kanazawa, Ishikawa, Japan;Department of Urology, Dokkyo Medical School, Koshigaya Hospital, Koshigaya, Saitama, Japan;Department of Integrative Cancer Therapy and Urology, Kanazawa University Graduate School of Medical Science, 13-1, Takaramachi, Kanazawa, Ishikawa 920-8641, Japan;Department of Obstetrics & Gynecology, Kanazawa Medical School, Kahoku-gun, Ishikawa, Japan

关键词: Liquid-based cytology;    Ureaplasma;    Mycoplasma;    Oral infection;    Human papillomavirus;   

Others  :  1134883
DOI  :  10.1186/1471-2334-14-43

 received in 2013-08-12, accepted in 2014-01-23,  发布年份 2014

【 摘 要 】

Background

Oropharyngeal squamous cell carcinoma (OSCC) has shown a gradual increase in male predominance due to the increasing incidence of human papillomavirus (HPV)-associated OSCC. However, the mode of HPV transmission to the oral cavity is poorly understood, and little is known about the epidemiology of oral HPV infection in men. The prevalence rates of HPV, Neisseria gonorrhoeae, Chlamydia trachomatis, Mycoplasma spp., and Ureaplasma spp. were compared in the oropharynx (oral cavity) and urine of male Japanese patients attending a sexually transmitted disease clinic.

Methods

The study population consisted of 213 men aged 16 – 70 years old (mean: 34.4 years old). Oropharyngeal gargles and urine were collected, and sedimented cells were preserved in liquid-based cytology solution. After DNA extraction, β-globin and infectious organisms were analyzed by a PCR-based method. The HPV genotype was determined by HPV GenoArray test.

Results

β-Globin was positive in 100% and 97.7% of oral and urine samples, respectively. HPV detection rates were 18.8% and 22.1% in oral and urine samples, respectively, suggesting that the prevalence of HPV infection in the oral cavity was similar to that in the urinary tract. N. gonorrhoeae was more prevalent in oral (15.6%) than urine samples (9.1%), whereas C. trachomatis was detected more frequently in urine (15.9%) than oral samples (4.2%). The detection rates of M. genitalium, M. hominis, and Ureaplasma spp. were 5.2%, 10.3%, and 16.0% in oral samples, and 7.7%, 6.3%, and 19.2% in urine, respectively. There were no significant differences in the detection rates of Mycoplasma spp. and Ureaplasma spp. between anatomical locations. The distribution of HPV types were similar in oral and urine samples, and HPV16 was the most common type. The majority of men with HPV infection in both the oral cavity and urine had concordant oral and urinary HPV infection. The presence of urinary HPV infection was an independent risk factor of oral HPV infection, with an odds ratio of 3.39 (95% CI: 1.49 – 7.71), whereas oral gonococcal infection was inversely correlated with oral HPV infection (odds ratio: 0.096; 95% CI: 0.01 – 0.77).

Conclusions

Oral HPV infection commonly occurs in sexually active men, and is significantly correlated with urinary HPV infection.

【 授权许可】

   
2014 Nakashima et al.; licensee BioMed Central Ltd.

【 参考文献 】

• [1]Zur HH: Papillomavirus infections: a major cause of human cancers. Biochem Biophys Acta 1996, 1288:F55-78.
• [2]Miralles-Guri C, Bruni L, Cubilla AL, Castellsagué X, Bosch FX, de Sanjosé S: Human papillomavirus prevalence and type distribution in penile carcinoma. J Clin Pathol 2009, 62:870-878.
• [3]Hoots BE, Palefsky JM, Pimenta JM, Smith JS: Human papillomavirus type distribution in anal cancer and anal intraepithelial lesions. Int J Cancer 2009, 124:2375-2383.
• [4]Chaturvedi AK, Engels EA, Anderson WF, Gillison ML: Incidence trends for human papillomavirus-related and -unrelated oral squamous cell carcinomas in the United States. J Clin Oncol 2008, 26:612-619.
• [5]Chaturvedi AK, Engels EA, Pfeiffer RM, Hernandez BY, Xiao W, Kim E, Jiang B, Goodman MT, Sibug-Saber M, Cozen W, et al.: Human papillomavirus and rising oropharyngeal cancer incidence in the United States. J Clin Oncol 2011, 29:4294-4301.
• [6]Ang KK, Harris J, Wheeler R, Weber R, Rosenthal DI, Nguyen-Tân PF, Westra WH, Chung CH, Jordan RC, Lu C, et al.: Human papillomavirus and survival of patients with oropharyngeal cancer. N Engl J Med 2010, 363:24-35.
• [7]Tanaka S, Sobue T: Comparison of oral and pharyngeal cancer mortality in five countries: France, Italy, Japan, UK and USA from the WHO Mortality Database (1960-2000). Jpn J Clin Oncol 2005, 35:488-491.
• [8]Gillison ML, Koch WM, Capone RB, Spafford M, Westra WH, Wu L, Zahurak ML, Daniel RW, Viglione M, Symer DE, et al.: Evidence for a causal association between human papillomavirus and a subset of head and neck cancers. J Natl Cancer Inst 2000, 92:709-720.
• [9]Smith JS, Melendy A, Melendy A, Rana RK, Pimenta JM: Age-specific prevalence of infection with human papillomavirus in females: a global review. J Adolesc Health 2008, 43(Suppl):S5-25.
• [10]Yamada R, Sasagawa T, Kirumbi LW, Kingoro A, Karanja DK, Kiptoo M, Nakitare GW, Ichimura H, Inoue M: Human papillomavirus infection and cervical abnormalities in Nairobi, Kenya, an area with a high prevalence of human immunodeficiency virus infection. J Med Virol 2008, 80:847-855.
• [11]Shigehara K, Sasagawa T, Kawaguchi S, Kobori Y, Nakashima T, Shimamura M, Taya T, Furubayashi K, Namiki M: Prevalence of human papillomavirus infection in the urinary tract of men with urethritis. Int J Urol 2010, 17:563-568.
• [12]Grisaru D, Avidor B, Niv J, Marmor S, Almog B, Leibowitz C, Graidy M, Giladi M: Pilot study of prevalence of high-risk human papillomavirus genotypes in Israeli Jewish women referred for colposcopic examination. J Clin Microbiol 2008, 46:1602-1605.
• [13]Chaudhry U, Saluja D: Detection of Neisseria gonorrhoeae by PCR using orf1 gene as target. Sex Transm Infect 2002, 78:72-78.
• [14]Mahony JB, Song X, Chong S, Faught M, Salonga T, Kapala J: Evaluation of the NucliSens Basic Kit for detection of Chlamydia trachomatis and Neisseria gonorrhoeae in genital tract specimens using nucleic acid sequence-based amplification of 16S rRNA. J Clin Microbiol 2001, 39:1429-1435.
• [15]Shigehara K, Kawaguchi S, Sasagawa T, Furubayashi K, Shimamura M, Maeda Y, Konaka H, Mizokami A, Koh E, Namiki M: Prevalence of genital Mycoplasma, Ureaplasma, Gardnerella, and human papillomavirus in Japanese men with urethritis, and risk factors for detection of urethral human papillomavirus infection. J Infect Chemother 2011, 17:487-492.
• [16]Stellrecht KA, Woron AM, Mishrik NG, Venezia RA: Comparison of multiplex PCR assay with culture for detection of genital mycoplasmas. J Clin Microbiol 2004, 42:1528-1533.
• [17]D'Souza G, Kreimer AR, Viscidi R, Pawlita M, Fakhry C, Koch WM, Westra WH, Gillison ML: Case-control study of human papillomavirus and oropharyngeal cancer. N Engl J Med 2007, 356:1944-1956.
• [18]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, 199:1263-1269.
• [19]Kreimer AR, Villa A, Nyitray AG, Abrahamsen M, Papenfuss M, Smith D, Hildesheim A, Villa LL, Lazcano-Ponce E, Giuliano AR: The epidemiology of oral HPV infection among a multinational sample of healthy men. Cancer Epidemiol Biomarkers Prev 2011, 20:172-182.
• [20]Kreimer AR, Bhatia RK, Messeguer AL, González P, Herrero R, Giuliano AR: Oral human papillomavirus in healthy individuals: a systematic review of the literature. Sex Transm Dis 2010, 37:386-391.
• [21]Marais DJ, Passmore JA, Denny L, Sampson C, Allan BR, Williamson AL: Cervical and oral human papillomavirus types in HIV-1 positive and negative women with cervical disease in South Africa. J Med Virol 2008, 80:953-959.
• [22]Smith EM, Ritchie JM, Yankowitz J, Wang D, Turek LP, Haugen TH: HPV prevalence and concordance in the cervix and oral cavity of pregnant women. Infect Dis Obstet Gynecol 2004, 12:45-56.
• [23]Fakhry C, D’souza G, Sugar E, Weber K, Goshu E, Minkoff H, Wright R, Seaberg E, Gillison M: Relationship between prevalent oral and cervical human papillomavirus infections in human immunodeficiency virus-positive and –negative women. J Clin Microviol 2006, 44:4479-4485.
• [24]Edelstein ZR, Schwartz SM, Hawes S, Hughes JP, Feng Q, Stern ME, O'Reilly S, Lee SK, Fu Xi L, Koutsky LA: Rates and determinants of oral human papillomavirus infection in young men. Sex Transm Dis 2012, 39:860-867.
• [25]Kawaguchi S, Shigehara K, Sasagawa T, Shimamura M, Nakashima T, Sugimoto K, Nakashima K, Furubayashi K, Namiki M: Liquid-based urine cytology as a tool for detection of human papillomavirus, Mycoplasma spp., and Ureaplasma spp. in men. J Clin Microbiol 2012, 50:401-406.
• [26]Sasagawa T, Basha W, Yamazaki H, Inoue M: High-risk and multiple human papillomavirus infections associated with cervical abnormalities in Japanese women. Cancer Epidemiol Biomarkers Prev 2001, 10:45-52.
• [27]Takahashi S, Takeyama K, Miyamoto S, Ichihara K, Maeda T, Kunishima Y, Matsukawa M, Tsukamoto T: Detection of Mycoplasma genitalium, Mycoplasma hominis, Ureaplasma urealyticum, and Ureaplasma parvum DNAs in urine from asymptomatic healthy young Japanese men. J Infect Chemother 2006, 12:269-271.
• [28]Sackel SG, Alpert S, Fiumara NJ, Donner A, Laughlin CA, McCormack WM: Orogenital contact and the isolation of Neisseria gonorrhoeae, Mycoplasma hominis, and Ureaplasma urealyticum from the pharynx. Sex Transm Dis 1979, 6:64-68.
• [29]Peters RP, Nijsten N, Mutsaers J, Jansen CL, Morré SA, van Leeuwen AP: Screening of oropharynx and anorectum increases prevalence of Chlamydia trachomatis and Neisseria gonorrhoeae infection in female STD clinic visitors. Sex Transm Dis 2011, 38:783-787.
• [30]Giuliano AR, Nielson CM, Flores R, Dunne EF, Abrahamsen M, Papenfuss MR, Markowitz LE, Smith D, Harris RB: The optimal anatomic sites for sampling heterosexual men for human papillomavirus (HPV) detection: the HPV detection in men study. J Infect Dis 2007, 196:1146-1152.