J Appl Biomed 15:139-145, 2017 | DOI: 10.1016/j.jab.2016.11.004

Antibiotic treatment of asymptomatic Ureaplasma infection improves semen parameters in infertile men

Mohammad Hossein Ahmadia, Akbar Mirsalehiana,*, Mohammad Ali Sadighi Gilanib,c,*, Abbas Bahadora, Malihe Talebid, Reza Salman Yazdib
a Department of Microbiology, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran
b Department of Andrology, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, ACECR, Tehran, Iran
c Department of Urology, Shariati Hospital, Tehran University of Medical Sciences, Tehran, Iran
d Department of Microbiology, School of Medicine, Iran University of Medical Sciences, Tehran, Iran

The role of asymptomatic infections caused by Ureaplasma species in male infertility and the efficacy of antibiotics in treatment of this failure is not yet definitely determined. A total of 165 infertile males having abnormal semen parameters (study group) as well as 165 healthy fertile men (control group) were included in this study. Semen samples were taken from all participants and after analyzing, undergone real-time PCR, microbial culture, and reactive oxygen species (ROS) as well as total antioxidant capacity (TAC) assays. Infected individuals of study group were treated with antibiotic. One month after the treatment completion, second semen samples were taken and undergone all the tests mentioned. The frequency of Ureaplasma spp. was significantly higher in the infertile men compared with the fertile ones (36.4% versus 11.5%; p < 0.001). Most of semen parameters were improved (p < 0.05) and reached their normal range, the level of TAC elevated (p < 0.001), and ROS level (p = 0.003) as well as ROS/TAC ratio (p = 0.003) reduced after antibiotic treatment. Moreover, wives of 37 infertile men (61.7%) became pregnant six months after the treatment completion. These findings indicate that Ureaplasma species are correlated with male infertility and that antibiotic therapy can improve the semen parameters and treat the male infertility.

Keywords: Ureaplasma species; Asymptomatic infections; Male infertility; Semen parameters; Antibiotic treatment

Received: September 26, 2016; Accepted: November 15, 2016; Published: May 1, 2017  Show citation

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Ahmadi MH, Mirsalehian A, Gilani MAS, Bahador A, Talebi M, Yazdi RS. Antibiotic treatment of asymptomatic Ureaplasma infection improves semen parameters in infertile men. J Appl Biomed. 2017;15(2):139-145. doi: 10.1016/j.jab.2016.11.004.
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References

  1. Abusarah, E.A., Awwad, Z.M., Charvalos, E., Shehabi, A.A., 2013. Molecular detection of potential sexually transmitted pathogens in semen and urine specimens of infertile and fertile males. Diagn. Microbiol. Infect. Dis. 77, 283-286. Go to original source... Go to PubMed...
  2. Ahmadi, M.H., Mirsalehian, A., Bahador, A., 2016. Prevalence of urogenital mycoplasmas in Iran and their effects on fertility potential: a systematic review and meta-analysis. Iran. J. Publ. Health 45, 409-422.
  3. Al-Daghistani, H.I., Abdel-Dayem, M., 2010. Clinical significance of asymptomatic urogenital Mycoplasma hominis and Ureaplasma urealyticum in relation to seminal fluid parameters among infertile Jordanian males. Middle East Fertil. Soc. J. 15, 29-34. Go to original source...
  4. Al-Daghistani, H.I., Hamad, A.W.R., Abdel-Dayem, M., Al-Swaifi, M., Abu Zaid, M., 2010. Evaluation of serum testosterone, progesterone, seminal antisperm antibody, and fructose levels among Jordanian males with a history of infertility. Biochem. Res. Int. 2010, 1-8. Go to original source... Go to PubMed...
  5. Al-Sweih, N.A., Al-Fadli, A.H., Omu, A.E., Rotimi, V.O., 2012. Prevalence of Chlamydia trachomatis, Mycoplasma hominis, Mycoplasma genitalium, and Ureaplasma urealyticum infections and seminal quality in infertile and fertile men in Kuwait. J. Androl. 33, 1323-1329. Go to original source... Go to PubMed...
  6. Ammar, A., Gad, G., Hasan, A., Lamia, A., 2014. Virulence factors in mycoplasma of human origin. Egypt. J. Med. Microbiol. 23, 29-36. Go to original source...
  7. Andrade-Rocha, F.T., 2003. Ureaplasma urealyticum and Mycoplasma hominis in men attending for routine semen analysis. Urol. Int. 71, 377-381. Go to original source... Go to PubMed...
  8. Ballow, C.H., Amsden, G.W., 1992. Azithromycin: the first azalide antibiotic. Ann. Pharmacother. 26, 1253-1261. Go to original source... Go to PubMed...
  9. Bharat, A., Cunningham, S.A., Budinger, G.S., Kreisel, D., DeWet, C.J., Gelman, A.E., Waites, K., Crabb, D., Xiao, L., Bhorade, S., 2015. Disseminated Ureaplasma infection as a cause of fatal hyperammonemia in humans. Sci. Transl. Med. 7, 1-6. Go to original source... Go to PubMed...
  10. Bornman, M., Mahomed, M., Boomker, D., Schulenburg, G., Reif, S., Crewe-Brown, H., 1990. Microbial flora in semen of infertile African men at Garankuwa hospital: Die mikrobielle Flora im Sperma von kinderlosen afrikanischen Männern aus dem Garankuwa-Hospital. Andrologia 22, 118-121. Go to original source... Go to PubMed...
  11. Cazanave, C., Manhart, L., Bébéar, C., 2012. Mycoplasma genitalium, an emerging sexually transmitted pathogen. Med. Mal. Infect. 42, 381-392. Go to original source... Go to PubMed...
  12. Citti, C., Blanchard, A., 2013. Mycoplasmas and their host: emerging and reemerging minimal pathogens. Trends Microbiol. 21, 196-203. Go to original source... Go to PubMed...
  13. Günyeli, I., Abike, F., Dünder, I., Aslan, C., Tapisiz, Ö.L., Temizkan, O., Payasli, A., Erdemog lu, E., 2011. Chlamydia, mycoplasma and ureaplasma infections in infertile couples and effects of these infections on fertility. Arch. Gynecol. Obstet. 283, 379-385. Go to original source... Go to PubMed...
  14. Gdoura, R., Kchaou, W., Chaari, C., Znazen, A., Keskes, L., Rebai, T., Hammami, A., 2007. Ureaplasma urealyticum, Ureaplasma parvum, Mycoplasma hominis and Mycoplasma genitalium infections and semen quality of infertile men. BMC Infect. Dis. 7, 1-9. Go to original source... Go to PubMed...
  15. Gdoura, R., Kchaou, W., Ammar-Keskes, L., Chakroun, N., Sellemi, A., Znazen, A., Rebai, T., Hammami, A., 2008. Assessment of Chlamydia trachomatis, Ureaplasma urealyticum, Ureaplasma parvum, Mycoplasma hominis, and Mycoplasma genitalium in semen and first void urine specimens of asymptomatic male partners of infertile couples. J. Androl. 29, 198-206. Go to original source... Go to PubMed...
  16. Gimenes, F., Souza, R.P., Bento, J.C., Teixeira, J.J., Maria-Engler, S.S., Bonini, M.G., Consolaro, M.E., 2014. Male infertility: a public health issue caused by sexually transmitted pathogens. Nat. Rev. Urol. 11, 672-687. Go to original source... Go to PubMed...
  17. Gnarpe, H., Friberg, J., 1972. Mycoplasma and human reproductive failure. Am. J. Obstet. Gynecol. 114, 727-731. Go to original source...
  18. Gupta, A., Gupta, A., Gupta, S., Mittal, A., Chandra, P., Gill, A.K., 2009. Correlation of mycoplasma with unexplained infertility. Arch. Gynecol. Obstet. 280, 981-985. Go to original source... Go to PubMed...
  19. Han, X., Wang, Y., Chen, J., 2003. A comparative study on interrelations among microelements, infection of Ureaplasma urealyticum, and male infertility. Arch. Androl. 49, 265-269. Go to original source... Go to PubMed...
  20. Huang, C., Peng, L., Zheng, Z., Jiang, Y., 2014. Value of detection of Mycoplasma, Chlamydia and anti-sperm antibodies in male infertility. Int. J. Lab. Med. 35, 1412-1414.
  21. Huang, C., Zhu, H., Xu, K., Wang, S., Fan, L., Zhu, W., 2015. Mycoplasma and ureaplasma infection and male infertility: a systematic review and metaanalysis. Andrology 3, 809-816. Go to original source... Go to PubMed...
  22. Klein, J.O., Buckland, D., Finland, M., 1969. Colonization of newborn infants by mycoplasmas. N. Engl. J. Med. 280, 1025-1030. Go to original source... Go to PubMed...
  23. Knox, C.L., Allan, J.A., Allan, J.M., Edirisinghe, W.R., Stenzel, D., Lawrence, F.A., Purdie, D.M., Timms, P., 2003. Ureaplasma parvum and Ureaplasma urealyticum are detected in semen after washing before assisted reproductive technology procedures. Fertil. Steril. 80, 921-929. Go to original source... Go to PubMed...
  24. La Vignera, S., Vicari, E., Condorelli, R., d'Agata, R., Calogero, A., 2011. Male accessory gland infection and sperm parameters (review). Int. J. Androl. 34, e330-e347. Go to original source... Go to PubMed...
  25. Lee, J.S., Kim, K.T., Lee, H.S., Yang, K.M., Seo, J.T., Choe, J.H., 2013. Concordance of Ureaplasma urealyticum and Mycoplasma hominis in infertile couples: impact on semen parameters. Urology 81, 1219-1224. Go to original source... Go to PubMed...
  26. Liu, J., Wang, Q., Ji, X., Guo, S., Dai, Y., Zhang, Z., Jia, L., Shi, Y., Tai, S., Lee, Y., 2014. Prevalence of Ureaplasma urealyticum, Mycoplasma hominis, Chlamydia trachomatis infections, and semen quality in infertile and fertile men in China. Urology 83, 795-799. Go to original source... Go to PubMed...
  27. McAuliffe, L., Ellis, R.J., Miles, K., Ayling, R.D., Nicholas, R.A., 2006. Biofilm formation by mycoplasma species and its role in environmental persistence and survival. Microbiology 152, 913-922. Go to original source... Go to PubMed...
  28. Nunez-Calonge, R., Caballero, P., Redondo, C., Baquero, F., Martinez-Ferrer, M., Meseguer, M., 1998. Ureaplasma urealyticum reduces motility and induces membrane alterations in human spermatozoa. Hum. Reprod. 13, 2756-2761. Go to original source... Go to PubMed...
  29. Ochsendorf, F., 2008. Sexually transmitted infections: impact on male fertility. Andrologia 40, 72-75. Go to original source... Go to PubMed...
  30. Pónyai, K., Mihalik, N., Ostorházi, E., Farkas, B., Párducz, L., Marschalkó, M., Kárpáti, S., Rozgonyi, F., 2013. Incidence and antibiotic susceptibility of genital mycoplasmas in sexually active individuals in Hungary. Eur. J. Clin. Microbiol. Infect. Dis. 32, 1423-1426. Go to original source... Go to PubMed...
  31. Pajovic, B., Radojevic, N., Vukovic, M., Stjepcevic, A., 2013. Semen analysis before and after antibiotic treatment of asymptomatic chlamydia-and ureaplasma-related pyospermia. Andrologia 45, 266-271. Go to original source... Go to PubMed...
  32. Pannekoek, Y., Trum, J., Bleker, O., van der Veen, F., Spanjaard, L., Dankert, J., 2000. Cytokine concentrations in seminal plasma from subfertile men are not indicative of the presence of Ureaplasma urealyticum or Mycoplasma hominis in the lower genital tract. J. Med. Microbiol. 49, 697-700. Go to original source... Go to PubMed...
  33. Peerayeh, S.N., Yazdi, R.S., Zeighami, H., 2008. Association of Ureaplasma urealyticum infection with varicocele-related infertility. J. Infect. Dev. Ctries. 2, 116-119. Go to original source... Go to PubMed...
  34. Potts, J., Sharma, R., Pasqualotto, F., Nelson, D., Hall, G., Agarwal, A., 2000. Association of ureaplasma urealyticum with abnormal reactive oxygen species levels and absence of leukocytospermia. J. Urol. 163, 1775. Go to original source... Go to PubMed...
  35. Razin, S., 2006. The genus Mycoplasma and related genera (class Mollicutes). In: Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.H., Stackebrandt, E. (Eds.), The Prokaryotes: A Handbook on the Biology of Bacteria. Springer, New York, pp. 836-904. Go to original source...
  36. Reichart, M., Kahane, I., Bartoov, B., 2000. In vivo and in vitro impairment of human and ram sperm nuclear chromatin integrity by sexually transmitted Ureaplasma urealyticum infection. Biol. Reprod. 63, 1041-1048. Go to original source... Go to PubMed...
  37. Rybar, R., Prinosilova, P., Kopecka, V., Hlavicova, J., Veznik, Z., Zajicova, A., Rubes, J., 2012. The effect of bacterial contamination of semen on sperm chromatin integrity and standard semen parameters in men from infertile couples. Andrologia 44, 410-418. Go to original source... Go to PubMed...
  38. Salmeri, M., Valenti, D., Vignera, S.L., Bellanca, S., Morello, A., Toscano, M.A., Mastrojeni, S., Calogero, A.E., 2012. Prevalence of Ureaplasma urealyticum and Mycoplasma hominis infection in unselected infertile men. J. Chemother. 24, 81-86. Go to original source... Go to PubMed...
  39. Sanocka-Maciejewska, D., Ciupin  ska, M., Kurpisz, M., 2005. Bacterial infection and semen quality. J. Reprod. Immunol. 67, 51-56. Go to original source... Go to PubMed...
  40. Shalika, S., Dugan, K., Smith, R.D., Padilla, S.L., 1996. The effect of positive semen bacterial and Ureaplasma cultures on in-vitro fertilization success. Hum. Reprod. 11, 2789-2792. Go to original source... Go to PubMed...
  41. Sharma, R.K., Pasqualotto, F.F., Nelson, D.R., Thomas, A.J., Agarwal, A., 1999. The reactive oxygen species-total antioxidant capacity score is a new measure of oxidative stress to predict male infertility. Hum. Reprod. 14, 2801-2807. Go to original source... Go to PubMed...
  42. Smith, R., Vantman, D., Ponce, J., Escobar, J., Lissi, E., 1996. Andrology: total antioxidant capacity of human seminal plasma. Hum. Reprod. 11, 1655-1660. Go to original source... Go to PubMed...
  43. Song, T., Ye, A., Xie, X., Huang, J., Ruan, Z., Kong, Y., Song, J., Wang, Y., Chen, J., Zhang, J., 2014. Epidemiological investigation and antimicrobial susceptibility analysis of ureaplasma species and Mycoplasma hominis in outpatients with genital manifestations. J. Clin. Pathol. 67, 817-820. Go to original source... Go to PubMed...
  44. Taylor-Robinson, D., Bebear, C., 1997. Antibiotic susceptibilities of mycoplasmas and treatment of mycoplasmal infections. J. Antimicrob. Chemother. 40, 622-630. Go to original source... Go to PubMed...
  45. Taylor-Robinson, D., Lamont, R., 2011. Mycoplasmas in pregnancy. BJOG Int. J. Obstet. Gynaecol. 118, 164-174. Go to original source... Go to PubMed...
  46. Tully, J., Razin, S., 1983. Methods in Mycoplasmology V2: Diagnostic Mycoplasmology, first ed. Academic Press Inc., New York.
  47. Viscardi, R.M., 2010. Ureaplasma species: role in diseases of prematurity. Clin. Perinatol. 37, 393-409. Go to original source... Go to PubMed...
  48. Waites, K.B., Katz, B., Schelonka, R.L., 2005. Mycoplasmas and ureaplasmas as neonatal pathogens. Clin. Microbiol. Rev. 18, 757-789. Go to original source... Go to PubMed...
  49. Waites, K.B., Schelonka, R.L., Xiao, L., Grigsby, P.L., Novy, M.J., 2009. Congenital and opportunistic infections: Ureaplasma species and Mycoplasma hominis. Semin. Fetal Neonatal Med. 14, 190-199. Go to original source... Go to PubMed...
  50. Wang, Y., Liang, C.L., Wu, J.Q., Xu, C., Qin, S.X., Gao, E.S., 2006a. Do Ureaplasma urealyticum infections in the genital tract affect semen quality? Asian J. Androl. 8, 562-568. Go to original source... Go to PubMed...
  51. Wang, Y., Sun, G., Pan, J., Li, T., 2006b. Correlation of Ureaplasma urealyticum and Chlamydia trachomatis infections with male sterility: a meta-analysis of randomized control trials. Zhonghua Nan Ke Xue 12, 615-618. Go to PubMed...
  52. World Health Organization, 1999. WHO Laboratory Manual for the Examination of Human Semen and Sperm-Cervical Mucus Interaction, 4th edn. Cambridge University Press, Cambridge.
  53. World Health Organization, 2010. WHO Laboratory Manual for the Examination and Processing of Human Semen. WHO Press, Switzerland.
  54. Xu, C., Sun, G., Zhu, Y., Wang, Y., 1997. The correlation of Ureaplasma urealyticum infection with infertility. Andrologia 29, 219-226. Go to original source... Go to PubMed...
  55. Zeighami, H., Peerayeh, S., Yazdi, R., Sorouri, R., 2009. Prevalence of Ureaplasma urealyticum and Ureaplasma parvum in semen of infertile and healthy men. Int. J. STD AIDS 20, 387-390. Go to original source... Go to PubMed...
  56. Zhang, Z., Zhang, H., Dong, Y., Han, R., Dai, R., Liu, R., 2011. Ureaplasma urealyticum in male infertility in Jilin Province, North-east China, and its relationship with sperm morphology. J. Int. Med. Res. 39, 33-40. Go to original source... Go to PubMed...
  57. Zhang, Q., Xiao, Y., Zhuang, W., Cheng, B., Zheng, L., Cai, Y., Zhou, H., Wang, Q., 2014. Effects of biovar I and biovar II of Ureaplasma urealyticum on sperm parameters, lipid peroxidation, and deoxyribonucleic acid damage in male infertility. Urology 84, 87-92. Go to original source... Go to PubMed...