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Effects of infections with five sexually transmitted pathogens on sperm quality

  • Kim, Sung Jae (Department of Anatomy.Cell Biology, Hanyang University College of Medicine) ;
  • Paik, Doo-Jin (Department of Anatomy.Cell Biology, Hanyang University College of Medicine) ;
  • Lee, Joong Shik (Department of Urology, Cheil General Hospital and Women's Healthcare Center, Dankook University College of Medicine) ;
  • Lee, Hyo Serk (Department of Urology, Cheil General Hospital and Women's Healthcare Center, Dankook University College of Medicine) ;
  • Seo, Ju Tae (Department of Urology, Cheil General Hospital and Women's Healthcare Center, Dankook University College of Medicine) ;
  • Jeong, Mi Seon (Laboratory of Research and Development for Genomics, Cheil General Hospital and Women's Healthcare Center, Dankook University College of Medicine) ;
  • Lee, Jae-Ho (Laboratory of Molecular Oncology, Cheil General Hospital and Women's Healthcare Center, Dankook University College of Medicine) ;
  • Park, Dong Wook (Laboratory of Reproductive Medicine, Cheil General Hospital and Women's Healthcare Center, Dankook University College of Medicine) ;
  • Han, Sangchul (Laboratory of Reproductive Medicine, Cheil General Hospital and Women's Healthcare Center, Dankook University College of Medicine) ;
  • Lee, Yoo Kyung (Department of Obstetrics and Gynecology, Cheil General Hospital and Women's Healthcare Center, Dankook University College of Medicine) ;
  • Lee, Ki Heon (Department of Obstetrics and Gynecology, Cheil General Hospital and Women's Healthcare Center, Dankook University College of Medicine) ;
  • Lee, In Ho (Department of Obstetrics and Gynecology, Cheil General Hospital and Women's Healthcare Center, Dankook University College of Medicine) ;
  • So, Kyeong A (Department of Obstetrics and Gynecology, Cheil General Hospital and Women's Healthcare Center, Dankook University College of Medicine) ;
  • Kim, Seon Ah (Department of Obstetrics and Gynecology, Cheil General Hospital and Women's Healthcare Center, Dankook University College of Medicine) ;
  • Kim, Juree (Department of Radiation Oncology, Cheil General Hospital and Women's Healthcare Center, Dankook University College of Medicine) ;
  • Kim, Tae Jin (Department of Obstetrics and Gynecology, Cheil General Hospital and Women's Healthcare Center, Dankook University College of Medicine)
  • Received : 2017.08.03
  • Accepted : 2017.11.29
  • Published : 2017.12.31

Abstract

Objective: This study investigated the prevalence of infections with human papillomavirus, Chlamydia trachomatis, Ureaplasma urealyticum, Mycoplasma hominis, and Mycoplasma genitalium in the semen of Korean infertile couples and their associations with sperm quality. Methods: Semen specimens were collected from 400 men who underwent a fertility evaluation. Infection with above five pathogens was assessed in each specimen. Sperm quality was compared in the pathogen-infected group and the non-infected group. Results: The infection rates of human papillomavirus, C. trachomatis, U. urealyticum, M. hominis, and M. genitalium in the study subjects were 1.57%, 0.79%, 16.80%, 4.46%, and 1.31%, respectively. The rate of morphological normality in the U. urealyticum-infected group was significantly lower than in those not infected with U. urealyticum. In a subgroup analysis of normozoospermic samples, the semen volume and the total sperm count in the pathogen-infected group were significantly lower than in the non-infected group. Conclusion: Our results suggest that infection with U. urealyticum alone and any of the five sexually transmitted infections are likely to affect sperm morphology and semen volume, respectively.

Keywords

References

  1. Centers for Disease Control and Prevention (CDC). STD-prevention counseling practices and human papillomavirus opinions among clinicians with adolescent patients: United States, 2004. MMWR Morb Mortal Wkly Rep 2006;55:1118-20.
  2. World Health Organization. Sexually transmitted infections (STIs): fact sheet. Geneva: World Health Organization; 2016.
  3. Schiffman M, Castle PE. Human papillomavirus: epidemiology and public health. Arch Pathol Lab Med 2003;127:930-4.
  4. Gross G, Pfister H. Role of human papillomavirus in penile cancer, penile intraepithelial squamous cell neoplasias and in genital warts. Med Microbiol Immunol 2004;193:35-44. https://doi.org/10.1007/s00430-003-0181-2
  5. Yang Y, Jia CW, Ma YM, Zhou LY, Wang SY. Correlation between HPV sperm infection and male infertility. Asian J Androl 2013;15:529-32. https://doi.org/10.1038/aja.2013.36
  6. Foresta C, Noventa M, De Toni L, Gizzo S, Garolla A. HPV-DNA sperm infection and infertility: from a systematic literature review to a possible clinical management proposal. Andrology 2015;3:163-73. https://doi.org/10.1111/andr.284
  7. Ljubin-Sternak S, Mestrovic T. Chlamydia trachomatis and genital mycoplasmas: pathogens with an impact on human reproductive health. J Pathog 2014;2014:183167.
  8. Witkin SS, Kligman I, Bongiovanni AM. Relationship between an asymptomatic male genital tract exposure to Chlamydia trachomatis and an autoimmune response to spermatozoa. Hum Reprod 1995;10:2952-5. https://doi.org/10.1093/oxfordjournals.humrep.a135827
  9. Karinen L, Pouta A, Hartikainen AL, Bloigu A, Paldanius M, Leinonen M, et al. Association between Chlamydia trachomatis antibodies and subfertility in the Northern Finland Birth Cohort 1966 (NFBC 1966), at the age of 31 years. Epidemiol Infect 2004;132:977-84. https://doi.org/10.1017/S0950268804002195
  10. Park ST, Lee SW, Kim MJ, Kang YM, Moon HM, Rhim CC. Clinical characteristics of genital Chlamydia infection in pelvic inflammatory disease. BMC Womens Health 2017;17:5. https://doi.org/10.1186/s12905-016-0356-9
  11. Hosseinzadeh S, Brewis IA, Eley A, Pacey AA. Co-incubation of human spermatozoa with Chlamydia trachomatis serovar E causes premature sperm death. Hum Reprod 2001;16:293-9. https://doi.org/10.1093/humrep/16.2.293
  12. Eley A, Hosseinzadeh S, Hakimi H, Geary I, Pacey AA. Apoptosis of ejaculated human sperm is induced by co-incubation with Chlamydia trachomatis lipopolysaccharide. Hum Reprod 2005;20:2601-7. https://doi.org/10.1093/humrep/dei082
  13. Xu C, Sun GF, Zhu YF, Wang YF. The correlation of Ureaplasma urealyticum infection with infertility. Andrologia 1997;29:219-26.
  14. Lee JS, Kim KT, Lee HS, Yang KM, Seo JT, Choe JH. Concordance of Ureaplasma urealyticum and Mycoplasma hominis in infertile couples: impact on semen parameters. Urology 2013;81:1219-24. https://doi.org/10.1016/j.urology.2013.02.044
  15. Al-Sweih NA, Al-Fadli AH, Omu AE, Rotimi VO. Prevalence of Chlamydia trachomatis, Mycoplasma hominis, Mycoplasma genitalium, and Ureaplasma urealyticum infections and seminal quality in infertile and fertile men in Kuwait. J Androl 2012;33:1323-9. https://doi.org/10.2164/jandrol.111.013821
  16. Rodriguez R, Hernandez R, Fuster F, Torres A, Prieto P, Alberto J. Genital infection and infertility. Enferm Infecc Microbiol Clin 2001;19:261-6. https://doi.org/10.1016/S0213-005X(01)72632-8
  17. Dunne EF, Nielson CM, Stone KM, Markowitz LE, Giuliano AR. Prevalence of HPV infection among men: a systematic review of the literature. J Infect Dis 2006;194:1044-57. https://doi.org/10.1086/507432
  18. Foresta C, Garolla A, Zuccarello D, Pizzol D, Moretti A, Barzon L, et al. Human papillomavirus found in sperm head of young adult males affects the progressive motility. Fertil Steril 2010;93:802-6. https://doi.org/10.1016/j.fertnstert.2008.10.050
  19. Palefsky JM. Human papillomavirus-related disease in men: not just a women's issue. J Adolesc Health 2010;46(4 Suppl):S12-9.
  20. Nielson CM, Flores R, Harris RB, Abrahamsen M, Papenfuss MR, Dunne EF, et al. Human papillomavirus prevalence and type distribution in male anogenital sites and semen. Cancer Epidemiol Biomarkers Prev 2007;16:1107-14. https://doi.org/10.1158/1055-9965.EPI-06-0997
  21. Gimenes F, Souza RP, Bento JC, Teixeira JJ, Maria-Engler SS, Bonini MG, et al. Male infertility: a public health issue caused by sexually transmitted pathogens. Nat Rev Urol 2014;11:672-87. https://doi.org/10.1038/nrurol.2014.285
  22. Brookings C, Goldmeier D, Sadeghi-Nejad H. Sexually transmitted infections and sexual function in relation to male fertility. Korean J Urol 2013;54:149-56. https://doi.org/10.4111/kju.2013.54.3.149
  23. Huang C, Zhu HL, Xu KR, Wang SY, Fan LQ, Zhu WB. Mycoplasma and Ureaplasma infection and male infertility: a systematic review and meta-analysis. Andrology 2015;3:809-16. https://doi.org/10.1111/andr.12078
  24. Liu J, Wang Q, Ji X, Guo S, Dai Y, Zhang Z, et al. Prevalence of Ureaplasma urealyticum, Mycoplasma hominis, Chlamydia trachomatis infections, and semen quality in infertile and fertile men in China. Urology 2014;83:795-9. https://doi.org/10.1016/j.urology.2013.11.009
  25. Seo HH, Kim YJ, Jeong MS, Hong SR, Lee IH, So KA, et al. Combined SYBR green real-time polymerase chain reaction and microarray method for the simultaneous determination of human papillomavirus loads and genotypes. Obstet Gynecol Sci 2016;59:489-97. https://doi.org/10.5468/ogs.2016.59.6.489
  26. Park HR, Kim YH, Lee HJ, Oh JS, Kim HJ. Usefulness of the MYCOFAST test (MYCOFAST(R) Evolution 2) for the diagnosis of nongonococcal genitourinary infections. Korean J Urol 2006;47:1117-23. https://doi.org/10.4111/kju.2006.47.10.1117
  27. Shin HR, Franceschi S, Vaccarella S, Roh JW, Ju YH, Oh JK, et al. Prevalence and determinants of genital infection with papillomavirus, in female and male university students in Busan, South Korea. J Infect Dis 2004;190:468-76. https://doi.org/10.1086/421279
  28. Castellsague X. Natural history and epidemiology of HPV infection and cervical cancer. Gynecol Oncol 2008;110(3 Suppl 2):S4-7. https://doi.org/10.1016/j.ygyno.2008.07.045
  29. Huang C, Long X, Jing S, Fan L, Xu K, Wang S, et al. Ureaplasma urealyticum and Mycoplasma hominis infections and semen quality in 19,098 infertile men in China. World J Urol 2016;34:1039-44. https://doi.org/10.1007/s00345-015-1724-z
  30. Brossfield JE, Chan PJ, Patton WC, King A. Tenacity of exogenous human papillomavirus DNA in sperm washing. J Assist Reprod Genet 1999;16:325-8. https://doi.org/10.1023/A:1020458100382
  31. Connelly DA, Chan PJ, Patton WC, King A. Human sperm deoxyribonucleic acid fragmentation by specific types of papillomavirus. Am J Obstet Gynecol 2001;184:1068-70. https://doi.org/10.1067/mob.2001.115226
  32. Rintala MA, Grenman SE, Pollanen PP, Suominen JJ, Syrjanen SM. Detection of high-risk HPV DNA in semen and its association with the quality of semen. Int J STD AIDS 2004;15:740-3. https://doi.org/10.1258/0956462042395122
  33. Motrich RD, Cuffini C, Oberti JP, Maccioni M, Rivero VE. Chlamydia trachomatis occurrence and its impact on sperm quality in chronic prostatitis patients. J Infect 2006;53:175-83. https://doi.org/10.1016/j.jinf.2005.11.007
  34. Puerta Suarez J, Sanchez LR, Salazar FC, Saka HA, Molina R, Tissera A, et al. Chlamydia trachomatis neither exerts deleterious effects on spermatozoa nor impairs male fertility. Sci Rep 2017;7:1126. https://doi.org/10.1038/s41598-017-01262-w
  35. Gerovassili A, Marcandona O, Asimakopoulos B, Karavasilis V, Panopoulou M, Ikonomidis A. Relationship between Chlamydia-Ureaplasma-Mycoplasma genital detection with semen concentration and motility among Greek men. Int J Fertil Steril 2017;11:130-3.
  36. Styler M, Shapiro SS. Mollicutes (mycoplasma) in infertility. Fertil Steril 1985;44:1-12. https://doi.org/10.1016/S0015-0282(16)48668-1
  37. Bliatka D, Lymperi S, Mastorakos G, Goulis DG. Effect of endocrine disruptors on male reproduction in humans: why the evidence is still lacking? Andrology 2017;5:404-7. https://doi.org/10.1111/andr.12339
  38. Comhaire FH, de Kretser D, Farley TM, Rowe PJ. Towards more objectivity in diagnosis and management of male infertility. Int J Androl 1987;7:1-53.
  39. World Health Organization. WHO manual for the standardized investigation and diagnosis of the infertile couple. Geneva: World Health Organization; 2000.

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