Prevalence and antimicrobial resistance of Ureaplasma spp. and Mycoplasma hominis isolated from semen samples of infertile men in Shanghai, China from 2011 to 2016

Original Article
  • 103 Downloads

Abstract

This study was conducted to estimate the prevalence and antimicrobial resistance rate of Ureaplasma spp. and Mycoplasma hominis that were isolated from the semen samples of infertile males in Shanghai, China from 2011 to 2016. A total of 5016 infertile males and 412 healthy male controls were examined. The cultivation, identification, and antimicrobial susceptibilities of Ureaplasma spp. and M. hominis were assessed by using a Mycoplasma IST kit that was performed in parallel to selective solid agar cultivation. The positive rate of genital Mycoplasma infections in infertile men from 2011 to 2016 was 30–55%, which initially decreased during the first four years and then increased in the last two. Two distinct high-risk age ranges of Mycoplasma infections were observed: 26–30 years (37.8%) and 31–35 years (30.7%). Semisynthetic tetracyclines and macrolide antibiotics were the most effective agents against Ureaplasma spp. Among the fluoroquinolones, sparfloxacin and levofloxacin were also effective. Antibiotic resistance of Ureaplasma spp. against tetracyclines and macrolide antibiotics in the last six years did not vary significantly. However, the rate of resistance to fluoroquinolones (except norfloxacin) and spectinomycin decreased in the last two years. The rate of genital Mycoplasma presence in infertile patients between the ages of 26 and 35 years in Shanghai was high. The prevalence of genital Mycoplasma decreased during the first four years and then increased, with a peak in 2016. Doxycycline, minocycline, josamycin, and sparfloxacin can be recommended for first-line empirical treatment of Mycoplasma infections in infertile men in Shanghai, China.

Notes

Acknowledgements

We thank LetPub (http://www.letpub.com) for its linguistic assistance during the preparation of this manuscript.

Author contributions

YHZ and HXM designed the study and drafted the manuscript. WMG and YY interpreted data and revised the manuscript critically for important intellectual content. All authors read and approved the final version of the manuscript.

Compliance with ethical standards

Ethics statements

This study was initiated after receiving approval from the Institutional Review Board of the Shanghai Provincial Crops Hospital of the Chinese People’s Armed Police Forces and carried out according to the Helsinki Declaration. Informed patient consent was obtained from all the participants. Ethics committee approval for the study protocol and written informed consent were obtained for this study.

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Data sharing statement

There will be no additional unpublished data from the study.

References

  1. 1.
    Weng SL, Chiu CM, Lin FM, Huang WC, Liang C, Yang T, Yang TL, Liu CY, Wu WY, Chang YA, Chang TH, Huang HD (2014) Bacterial communities in semen from men of infertile couples: metagenomic sequencing reveals relationships of seminal microbiota to semen quality. PLoS One 9:e110152CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Meng Q, Ren A, Zhang L, Liu J, Li Z, Yang Y, Li R, Ma L (2015) Incidence of infertility and risk factors of impaired fecundity among newly married couples in a Chinese population. Reprod Biomed Online 30(1):92–100.  https://doi.org/10.1016/j.rbmo.2014.10.002 CrossRefPubMedGoogle Scholar
  3. 3.
    Diemer T, Huwe P, Ludwig M, Hauck EW, Weidner W (2003) Urogenital infection and sperm motility. Andrologia 35(5):283–287CrossRefPubMedGoogle Scholar
  4. 4.
    Ruggeri M, Cannas S, Cubeddu M, Molicotti P, Piras GL, Dessole S, Zanetti S (2016) Bacterial agents as a cause of infertility in humans. New Microbiol 39(3):206–209PubMedGoogle Scholar
  5. 5.
    Gimenes F, Souza RP, Bento JC, Teixeira JJ, Maria-Engler SS, Bonini MG, Consolaro ME (2014) Male infertility: a public health issue caused by sexually transmitted pathogens. Nat Rev Urol 11(12):672–687.  https://doi.org/10.1038/nrurol.2014.285 CrossRefPubMedGoogle Scholar
  6. 6.
    Zhou YH, Ma HX, Shi XX, Liu Y (2017) Ureaplasma spp. in male infertility and its relationship with semen quality and seminal plasma components. J Microbiol Immunol Infect (in press). pii: S1684-1182(17)30071-3.  https://doi.org/10.1016/j.jmii.2016.09.004
  7. 7.
    García-Castillo M, Morosini MI, Gálvez M, Baquero F, del Campo R, Meseguer MA (2008) Differences in biofilm development and antibiotic susceptibility among clinical Ureaplasma urealyticum and Ureaplasma parvum isolates. J Antimicrob Chemother 62:1027–1030.  https://doi.org/10.1093/jac/dkn337 CrossRefPubMedGoogle Scholar
  8. 8.
    Leli C, Mencacci A, Bombaci JC, D’Alò F, Farinelli S, Vitali M, Montagna P, Bietolini C, Meucci M, Perito S, Bistoni F (2012) Prevalence and antimicrobial susceptibility of Ureaplasma urealyticum and Mycoplasma hominis in a population of Italian and immigrant outpatients. Infez Med 20(2):82–87PubMedGoogle Scholar
  9. 9.
    Waites KB, Bébéar CM, Robertson JA, Talkington DF, Kenny GE (2001) Cumitech 34, laboratory diagnosis of mycoplasmal infections. Nolte FS, coordinating editor, American Society for Microbiology, Washington DC, pp 1–30Google Scholar
  10. 10.
    Viscardi RM (2010) Ureaplasma species: role in diseases of prematurity. Clin Perinatol 37(2):393–409.  https://doi.org/10.1016/j.clp.2009.12.003 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Bayraktar MR, Ozerol IH, Gucluer N, Celik O (2010) Prevalence and antibiotic susceptibility of Mycoplasma hominis and Ureaplasma urealyticum in pregnant women. Int J Infect Dis 14:e90–e95.  https://doi.org/10.1016/j.ijid.2009.03.020 CrossRefPubMedGoogle Scholar
  12. 12.
    De Francesco MA, Caracciolo S, Bonfanti C, Manca N (2013) Incidence and antibiotic susceptibility of Mycoplasma hominis and Ureaplasma urealyticum isolated in Brescia, Italy, over 7 years. J Infect Chemother 19(4):621–627.  https://doi.org/10.1007/s10156-012-0527-z CrossRefPubMedGoogle Scholar
  13. 13.
    Stellrecht KA, Woron AM, Mishrik NG, Venezia RA (2004) Comparison of multiplex PCR assay with culture for detection of genital mycoplasmas. J Clin Microbiol 42(4):1528–1533CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Kokkayil P, Dhawan B (2015) Ureaplasma: current perspectives. Indian J Med Microbiol 33(2):205–214.  https://doi.org/10.4103/0255-0857.154850 CrossRefPubMedGoogle Scholar
  15. 15.
    Citti C, Blanchard A (2013) Mycoplasmas and their host: emerging and re-emerging minimal pathogens. Trends Microbiol 21(4):196–203.  https://doi.org/10.1016/j.tim.2013.01.003 CrossRefPubMedGoogle Scholar
  16. 16.
    Salmeri M, Valenti D, La Vignera S, Bellanca S, Morello A, Toscano MA, Mastrojeni S, Calogero AE (2012) Prevalence of Ureaplasma urealyticum and Mycoplasma hominis infection in unselected infertile men. J Chemother 24(2):81–86.  https://doi.org/10.1179/1120009X12Z.00000000021 CrossRefPubMedGoogle Scholar
  17. 17.
    Abusarah EA, Awwad ZM, Charvalos E, Shehabi AA (2013) Molecular detection of potential sexually transmitted pathogens in semen and urine specimens of infertile and fertile males. Diagn Microbiol Infect Dis 77(4):283–286.  https://doi.org/10.1016/j.diagmicrobio.2013.05.018 CrossRefPubMedGoogle Scholar
  18. 18.
    Huang C, Long X, Jing S, Fan L, Xu K, Wang S, Zhu W (2016) Ureaplasma urealyticum and Mycoplasma hominis infections and semen quality in 19,098 infertile men in China. World J Urol 34(7):1039–1044.  https://doi.org/10.1007/s00345-015-1724-z CrossRefPubMedGoogle Scholar
  19. 19.
    Zhu X, Li M, Cao H, Yang X, Zhang C (2016) Epidemiology of Ureaplasma urealyticum and Mycoplasma hominis in the semen of male outpatients with reproductive disorders. Exp Ther Med 12(2):1165–1170.  https://doi.org/10.3892/etm.2016.3409 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Lee JS, Kim KT, Lee HS, Yang KM, Seo JT, Choe JH (2013) Concordance of Ureaplasma urealyticum and Mycoplasma hominis in infertile couples: impact on semen parameters. Urology 81(6):1219–1224.  https://doi.org/10.1016/j.urology.2013.02.044 CrossRefPubMedGoogle Scholar
  21. 21.
    Lu MG, Shi JL, Xu C (2005) Establishment and application of the approach to detecting two biovars of Ureaplasma urealyticum in human semen. Zhonghua Nan Ke Xue 11(3):175–178PubMedGoogle Scholar
  22. 22.
    Chen XS, Peeling RW, Yin YP, Mabey DC (2011) The epidemic of sexually transmitted infections in China: implications for control and future perspectives. BMC Med 9:111.  https://doi.org/10.1186/1741-7015-9-111 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Kechagia N, Bersimis S, Chatzipanagiotou S (2008) Incidence and antimicrobial susceptibilities of genital mycoplasmas in outpatient women with clinical vaginitis in Athens, Greece. J Antimicrob Chemother 62(1):122–125.  https://doi.org/10.1093/jac/dkn158 CrossRefPubMedGoogle Scholar
  24. 24.
    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(9):817–820.  https://doi.org/10.1136/jclinpath-2014-202248 CrossRefPubMedGoogle Scholar
  25. 25.
    Schneider SC, Tinguely R, Droz S, Hilty M, Donà V, Bodmer T, Endimiani A (2015) Antibiotic susceptibility and sequence type distribution of Ureaplasma species isolated from genital samples in Switzerland. Antimicrob Agents Chemother 59(10):6026–6031.  https://doi.org/10.1128/AAC.00895-15 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Beeton ML, Chalker VJ, Jones LC, Maxwell NC, Spiller OB (2016) Antibiotic resistance among clinical Ureaplasma isolates recovered from neonates in England and Wales between 2007 and 2013. Antimicrob Agents Chemother 60(1):52–56.  https://doi.org/10.1128/AAC.00889-15 CrossRefPubMedGoogle Scholar
  27. 27.
    Clinical and Laboratory Standards Institute (CLSI) (2011) Methods for antimicrobial susceptibility testing for human mycoplasmas; approved guideline. CLSI document M43-A. CLSI, Wayne, PAGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Clinical LaboratoryShanghai Crops Hospital of Chinese People’s Armed PoliceShanghaiChina
  2. 2.Department of Health Management Medicine, Shanghai East HospitalTongji UniversityShanghaiChina
  3. 3.Department of Clinical LaboratoryShanghai Dermatology HospitalShanghaiChina

Personalised recommendations