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Simultaneous detection and identification of STI pathogens by multiplex Real-Time PCR in genital tract specimens in a selected area of Apulia, a region of Southern Italy

Infection volume 45, pages 469–477 (2017)Cite this article

Abstract

Purpose

Genital tract infections are globally a major cause of morbidity in sexually active individuals. The aim of this study was to investigate the prevalence and associations of co-infections of Chlamydia trachomatis, Neisseria gonorrhoeae, Trichomonas vaginalis, Mycoplasma hominis (MH), Mycoplasma genitalium, Ureaplasma urealyticum (UU) and Ureaplasma parvum (UP) in specimens collected from female (SF) and male (SM) patients.

Methods

1575 samples from 1575 individuals from the geographical area around Bari, Apulia region in Southern Italy, were collected and analyzed by a multiplex Real-Time PCR (mRT-PCR) (AnyplexTM II STI-7, Seegene, Inc., Seoul, Korea) assay.

Results

455/1575 (28.89%) samples resulted positive for at least one of the targets named above. Statistically significant differences in prevalence of the pathogens between SF and SM were not detected except for UP (24.92% in SF vs 8.91% in SM). Prevalence of co-infections was 6.84 and 3.96% in SF and SM, respectively. Moreover, MH presence in SF, but not in SM, was associated with UU and UP.

Conclusions

Our data suggest different patterns of infections between females and male and the importance of an increased vigilance of sexually transmitted pathogens to reduce the burden on general population and the sequelae or the complications on reproductive organs.

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References

  1. Department of Reproductive Health and Research World Health Organization. Global strategy for the prevention and control of sexually transmitted infections: 2006–2015. Geneva: WHO Press; 2007.

    Google Scholar 

  2. Gewirtzman A, Bobrick L, Conner K, Tyring SK. Epidemiology of sexually transmitted infections. In: Gorss G, Tyring SK, editors. Sexually transmitted infections and sexually transmitted diseases. New York: Springer; 2011.

    Google Scholar 

  3. Johnson RE, Newhall WJ, Papp JR, Knapp JS, Black CM, Gift TL, Steece R, Markowitz LE, Devine OJ, Walsh CM, Wang S, Gunter DC, Irwin KL, DeLisle S, Berman SM. Screening tests to detect Chlamydia trachomatis and Neisseria gonorrhoeae infections. MMWR Recomm Rep. 2002;51:1–38.

    PubMed  Google Scholar 

  4. World Health Organization. Fact sheet: Emergence of multi-drug resistant Neisseria gonorrhoeae. 2012. http://apps.who.int/iris/bitstream/10665/70603/1/WHO_RHR_11.14_eng.pdf. Accessed 03 Mar 2017

  5. Larsen B, Hwang J. Mycoplasma, Ureaplasma and adverse pregnancy outcomes: a fresh look. Infect Dis Obstet Gynecol. 2010;. doi:10.1155/2010/521921.

    PubMed Central  Google Scholar 

  6. Sethi S, Singh G, Samanta P, Sharma M. Mycoplasma genitalium: an emerging sexually transmitted pathogen. Indian J Med Res. 2012;136:942–55.

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Ghazi Saeedi K, Fateminasab F, Vatani SH, Anzimi Y, Bakhshandenosrat S, Mohamadi M. Compare two methods prostatic massage and urine initial drop sample in isolates of Mycoplasma hominis and Ureaplasma urealytivum in urinary tract. J Lab Med. 2008;2:15–8.

    Google Scholar 

  8. De F, Ma Z, James G, Gordon S, Gilbert GL. Species identification and subtyping of Ureaplasma parvum and Ureaplasma urealyticum using PCR-based assays. J Clin Microbiol. 2000;38:1175–9.

    Google Scholar 

  9. Ollikainen J, Heiskanen-Kosma T, Korppi M, Katila ML, Heinonen K. Clinical relevance of Ureaplasma urealyticum colonization in preterm infants. Acta Paediatr. 1998;87:1075–8.

    CAS  Article  PubMed  Google Scholar 

  10. Berçot B, Amarsy R, Goubard A, Aparicio C, Loeung HU, Segouin C, Gueret D, Jacquier H, Meunier F, Mougari F, Cambau E. Assessment of coinfection of sexually transmitted pathogen microbes by use of the anyplex II STI-7 molecular kit. J Clin Microbiol. 2015;53:991–3. doi:10.1128/JCM.03370-14.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Kissinger P. Trichomonas vaginalis: a review of epidemiologic, clinical and treatment issues. BMC Infect Dis. 2015;15:307. doi:10.1186/s12879-015-1055-0.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Aguilera-Arreola MG, González-Cardel AM, Tenorio AM, Curiel- Quesada E, Castro-Escarpulli G. Highly specific and efficient primers for in-house multiplex PCR detection of Chlamydia trachomatis, Neisseria gonorrhoeae, Mycoplasma hominis and Ureaplasma urealyticum. BMC Res Notes. 2014;7:433. doi:10.1186/1756-0500-7-433.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Whiley DM, Tapsall JW, Sloots TP. Nucleic acid amplification testing for Neisseria gonorrhoeae: an ongoing challenge. J Mol Diagn. 2006;8:3–15. doi:10.2353/jmoldx.2006.050045.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. Camporiondo MP, Farchi F, Ciccozzi M, Denaro A, Gallone D, Maracchioni F, Favalli C, Ciotti M. Detection of HPV and co-infecting pathogens in healthy Italian women by multiplex real-time PCR. Infez Med. 2016;24:12–7.

    PubMed  Google Scholar 

  15. Hochberg Y, Benjamini Y. More powerful procedures for multiple significance testing. Stat Med. 1990;9:811–8.

    CAS  Article  PubMed  Google Scholar 

  16. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2016. https://www.R-project.org/.

  17. Van de Laar MJ, Morré SA. Chlamydia: a major challenge for public health. Euro Surveill. 2007;12:E1–2.

    PubMed  Google Scholar 

  18. Wilson JS, Honey E, Templeton A, Paavonen J, Mårdh PA, Stray-Pedersen B, EU Biomed Concerted Action Group. A systematic review of the prevalence of Chlamydia trachomatis among European women. Hum Reprod Update. 2002;8:38–394.

    Article  Google Scholar 

  19. Newman L, Rowley J, Vander Hoorn S, Wijesooriya NS, Unemo M, Low N, Stevens G, Gottlieb S, Kiarie J, Temmerman M. Global estimates of the prevalence and incidence of four curable sexually transmitted infections in 2012 based on systematic review and global reporting. PLoS One. 2015;10(12):e0143304. doi:10.1371/journal.pone.0143304.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Bhuiyan BU, Rahman M, Miah MR, et al. Antimicrobial susceptibilities and plasmid contents of Neisseria gonorrhoeae isolates from commercial sex workers in Dhaka, Bangladesh: emergence of high level resistance to ciprofloxacin. J Clin Microbiol. 1999;37:1130–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Nessa K, Waris SA, Sultan Z, et al. Epidemiology and etiology of sexually transmitted infection among hotel-based sex workers in Dhaka, Bangladesh. J Clin Microbiol. 2004;42:618–21.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Rahman M, Alam A, Nessa K, et al. Etiology of sexually transmitted infections among street-based female sex workers in Dhaka, Bangladesh. J Clin Microbiol. 2000;38:1244–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Grześko J, Elias M, Manowiec M, Gabryś MS. Genital mycoplasmas-morbidity and a potential influence on human fertility. Med Wieku Rozwoj. 2006;10:985–92.

    PubMed  Google Scholar 

  24. De Francesco MA, Negrini R, Pinsi G, Peroni L, Manca N. Detection of Ureaplasma biovars and polymerase chain reaction-based subtyping of Ureaplasma parvum in women with or without symptoms of genital infections. Eur J Clin Microbiol Infect Dis. 2009;28:641–6. doi:10.1007/s10096-008-0687-z.

    Article  PubMed  Google Scholar 

  25. Yamazaki T, Matsumoto M, Matsuo J, Abe K, Minami K, Yamaguchi H. Frequency of Chlamydia trachomatis in Ureaplasma-positive healthy women attending their first prenatal visit in a community hospital in Sapporo, Japan. BMC Infect Dis. 2012;12:82. doi:10.1186/1471-2334-12-82.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Ljubin-Sternak S, Meštrović T. Chlamydia trachomatis and Genital Mycoplasmas: pathogens with an impact on human reproductive health. J Pathog. 2014;2014:183167. doi:10.1155/2014/183167.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Anagrius C, Loré B, Jensen JS. Mycoplasma genitalium: prevalence, clinical significance, and transmission. Sex Transmit Infect. 2005;81:458–62. doi:10.1136/sti.2004.012062.

    CAS  Article  Google Scholar 

  28. Bujold E, Morency AM, Rallu F, et al. Bacteriology of amniotic fluid in women with suspected cervical insufficiency. J Obstet Gynaecol Can. 2008;30:882–7.

    Article  PubMed  Google Scholar 

  29. Rodrigues MM, Fernandes PA, Haddad JP, Paiva MC, Souza Mdo C, Andrade TC, et al. Frequency of Chlamydia trachomatis, Neisseria gonorrhoeae, Mycoplasma genitalium, Mycoplasma hominis and Ureaplasma species in cervical samples. J Obstet Gynaecol. 2011;31:237–41. doi:10.3109/01443615.2010.548880.

    CAS  Article  PubMed  Google Scholar 

  30. Waites KB, Katz B, Schelonka RL. Mycoplasmas and ureaplasmas as neonatal pathogens. Clin Microbiol Rev. 2005;18:757–89. doi:10.1128/CMR.18.4.757-789.2005.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Kacerovský M, Boudyš L. Preterm premature rupture of membranes and Ureaplasma urealyticum. Ceska Gynekol. 2008;73:154–9.

    PubMed  Google Scholar 

  32. World Health Organization. Global programme of AIDS. Geneva: World Health Organization; 2001.

    Google Scholar 

  33. Zhu C, Liu J, Ling Y, Dong C, Wu T, Yu X, Hou Y, Dong L, Cheng X. Prevalence and antimicrobial susceptibility of Ureaplasma urealyticum and Mycoplasma hominis in Chinese women with genital infectious diseases. Indian J Dermatol Venereol Leprol. 2012;78:406–7. doi:10.4103/0378-6323.95480.

    PubMed  Google Scholar 

  34. Capoccia R, Greub G, Baud D. Ureaplasma urealyticum, Mycoplasma hominis and adverse pregnancy outcomes. Curr Opin Infect Dis. 2013;26:231–40. doi:10.1097/QCO.0b013e328360db58.

    Article  PubMed  Google Scholar 

  35. Kwak DW, Hwang HS, Kwon JY, Park YW, Kim YH. Co-infection with vaginal Ureaplasma urealyticum and Mycoplasma hominis increases adverse pregnancy outcomes in patients with preterm labor or preterm premature rupture of membranes. J Matern Fetal Neonatal Med. 2014;27:333–7. doi:10.3109/14767058.2013.818124.

    Article  PubMed  Google Scholar 

  36. Huang C, Liu Z, Lin N, Tu Y, Li J, Zhang D. Susceptibility of mixed infection of Ureaplasma urealyticum and Mycoplasma hominis to seven antimicrobial agents and comparison with that of Ureaplasma urealyticum infection. J Huazhong Univ Sci Technolog Med Sci. 2003;23:203–5.

    CAS  Article  PubMed  Google Scholar 

  37. Kataoka S, Yamada T, Chou K, Nishida R, Morikawa M, Minami M, Yamada H, Sakuragi N, Minakami H. Association between preterm birth and vaginal colonization by mycoplasmas in early pregnancy. J Clin Microbiol. 2006;44:51–5. doi:10.1128/JCM.44.1.51-55.2006.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Yamazaki T, Matsuo J, Nakamura S, Oguri S, Yamaguchi H. Effect of Ureaplasma parvum co-incubation on Chlamydia trachomatis maturation in human epithelial HeLa cells treated with interferon-γ. J Infect Chemother. 2014;20:460–4. doi:10.1016/j.jiac.2014.04.003.

    CAS  Article  PubMed  Google Scholar 

  39. Fernández G, Martró E, González V, Saludes V, Bascuñana E, Marcó C, Rivaya B, López E, Coll P, Matas L, Ausina V. Usefulness of a novel multiplex real-time PCR assay for the diagnosis of sexually-transmitted infections. Enferm Infecc Microbiol Clin. 2016;34:471–6. doi:10.1016/j.eimc.2015.10.014.

    Article  PubMed  Google Scholar 

  40. Choe HS, Lee DS, Lee SJ, Hong SH, Park DC, Lee MK, Kim TH, Cho YH. Performance of Anyplex™ II multiplex real-time PCR for the diagnosis of seven sexually transmitted infections: comparison with currently available methods. Int J Infect Dis. 2013;17:e1134–40. doi:10.1016/j.ijid.2013.

    CAS  Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Section of Microbiology, Interdisciplinary Department of Medicine (DIM), University of Bari “ Aldo Moro”, Piazza G. Cesare, 4-I-70124, Bari, Italy

    Raffaele Del Prete, Mirella Lestingi, Grazia Addati, Umberto Filippo Angelotti & Giuseppe Miragliotta

  2. UOC Microbiologia e Virologia, Azienda Ospedaliera-Universitaria Policlinico di Bari, Bari, Italy

    Raffaele Del Prete, Luigi Ronga & Giuseppe Miragliotta

  3. Department of Experimental Medicine and Surgery, University of Rome Tor Vergata, Rome, Italy

    Domenico Di Carlo

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  1. Raffaele Del Prete
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  2. Luigi Ronga
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Correspondence to Raffaele Del Prete.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. For this type of study, formal consent is not required.

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Del Prete, R., Ronga, L., Lestingi, M. et al. Simultaneous detection and identification of STI pathogens by multiplex Real-Time PCR in genital tract specimens in a selected area of Apulia, a region of Southern Italy. Infection 45, 469–477 (2017). https://doi.org/10.1007/s15010-017-1002-7

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  • DOI: https://doi.org/10.1007/s15010-017-1002-7

Keywords

  • Genital tract
  • Sexually transmitted infections
  • Co-infections
  • Multiplex Real-Time PCR