The report of the latest achievement of molecular diagnosis and investigation of antibiotic resistance of Ureaplasma urealyticum and Neisseria gonorrhoeae isolated from cervical secretions of infertile women referring to the women's clinic of Shohadaye-Tajrish Educational-Treatment Center, Tehran

Document Type : Original Article


1 Associate Professor, Department of Microbiology, Faculty of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran.

2 Assistant Professor, Department of Medical Bacteriology, Men’s Health and Reproductive Health Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran.

3 Professor, Department of Obstetrics and Gynecology, Men’s Health and Reproductive Health Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran.

4 Associate Professor, Department of Biostatistics, Physiotherapy Research Center, School of Paramedicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran.


Introduction: Neisseria and ureaplasma are considered to be the most important bacteria causing genital infection and infertility. The present study was conducted with the aim of searching for these two pathogens in the cervical secretions of infertile women, emphasizing molecular methods and determining drug resistance genes related to azithromycin and ciprofloxacin.
Methods: In this descriptive study, endocervical samples obtained from cervical secretions of 135 infertile women and 135 healthy women referred to Shohada Tajrish Hospital from October 2018 to September 2019 were examined. Data were analyzed by SPSS statistical software (version 21). Chi-square test was used to investigate the relationship between infection and infertility in individuals. P<0.05 was considered statistically significant.
Results: The prevalence of Neisseria gonorrhoea and Ureaplasma urealyticum was significant in the case group compared to the control group (P≤0.05). According to chi-square test, a significant relationship was observed between infection and infertility (P≤0.05). The prevalence of azithromycin resistance in Ureplasma urealyticum and Neisseria gonorrhoeae was 35 cases (48.6%) and 7 cases (58.3%), respectively. Ciprofloxacin resistance was reported in 3 cases (25%) of Neisseria gonorrhoeae and 64 cases (68.8%) of Ureaplasma urealyticum. The highest prevalence of resistance genes in both bacteria was related to mtrR and gyrA.
Conclusion: Antibiotic resistance in the studied bacteria indicates the indiscriminate use of antibiotics, the spread of antibiotic resistance gene structures, and genetic transmission among populations. In order to definitively treat and prevent the occurrence of resistance in pathogen strains, it is necessary to determine the resistance pattern to follow the resistance trend.


  1. Ghorbani F, Golmakani N, Shakeri MT. Relationship between the use of virtual social networks and tendency to childbearing in the students of Ferdowsi and Mashhad university of medical sciences. Iran J Obstet Gynecol Infertil 2016; 19(19):15-24.
  2. Latifnejad Roudsari R, Karami Dehkordi A, Esmaili HA, Mousavifar N, Agha Mohamadian Sherbaf H. The relationship between body image and marital adjustment in infertile women. Iran J Obstet Gynecol Infertil 2011; 14(6):9-19.
  3. Hatami H, Razavi SM, Eftekhar AH, Malesi F, Sayed Nozadi M, Parizadeh SMJ. Textbook of public health. 2nd Tehran: Arjmand; 2007.
  4. Burney RO, Schust DJ, Yai MWM. Infertility. In: Berek JS. Berek & Novak‘s gynecology .14nd London: Lippincott William &Wilkins; 2007. p. 1185-1275.
  5. Boivin J, Bunting L, Collins JA, Nygren KG. International estimates of infertility prevalence and treatment-seeking: potential need and demand for infertility medical care. Hum Reprod 2007; 22(6):1506-12.
  6. Wang Y, Liang CL, Wu JQ, Xu C, Qin SX, Gao ES. Do Ureaplasma urealyticum infections in the genital tract affect semen quality? Asian J Androl 2006; 8(5):562-8.
  7. Rosemond A, Lanotte P, Watt S, Sauget AS, Guerif F, Royère D, et al. Systematic screening tests for Chlamydia trachomatis, Mycoplasma hominis and Ureaplasma urealyticum in urogenital specimens of infertile couples. Pathologie-biologie 2005; 54(3):125-9.
  8. Knox CL, Allan JA, Allan JM, Edirisinghe WR, Stenzel D, Lawrence FA, et al. Ureaplasma parvum and Ureaplasma urealyticum are detected in semen after washing before assisted reproductive technology procedures. Fertility and sterility 2003; 80(4):921-9.
  9. Andrade-Rocha FT. Ureaplasma urealyticum and Mycoplasma hominis in men attending for routine semen analysis. Urologia internationalis 2003; 71(4):377-81.
  10. Gdoura R, Kchaou W, Chaari C, Znazen A, Keskes L, Rebai T, et al. Ureaplasma urealyticum, Ureaplasma parvum, Mycoplasma hominis and Mycoplasma genitalium infections and semen quality of infertile men. BMC infectious diseases 2007; 7(1):1-9.
  11. Murray PR, Rosenthal KS, Pfaller MA. Medical Microbiology, with Student Consult Online Access, 7: Medical Microbiology. Elsevier Health Sciences; 2013.
  12. Stellrecht KA, Woron AM, Mishrik NG, Venezia RA. Comparison of multiplex PCR assay with culture for detection of genital mycoplasmas. Journal of clinical microbiology 2004; 42(4):1528-33.
  13. Ochsendorf FR. Sexually transmitted infections: impact on male fertility. Andrologia 2008; 40(2):72-5.
  14. Karimian R, Roghanian R, Etemadifar Z. Study of accosiation between male infertility and Neisseria gonorrhoeae and Ureaplasma urealyticum infection. Iranian Journal of Medical Microbiology 2016; 10(3):11-8.
  15. Mardaneh J, Hasanzadeh P, Motamedifar M, Ahmadi K, Nikkhahi F. Diagnosis of Neisseria gonorrhoeae among pregnant women by culture method and PCR on cppB gene. ISMJ 2013; 16(5):288-95.
  16. Alimagham M, Motevasseli M, Gachkar L, Farajpour M, Niakan M. Evaluation of relation between Ureaplasma Urealyticum infection with abortion. Journal of Reproduction & Infertility 2001; 2(2):29-34.
  17. Darekordi A, Rezazadeh Zarandi E, Assar S, Rezahosseini O, Assar S. Diagnosis of bacterial infections; traditional and molecular methods: A narrative study. Journal of Rafsanjan University of Medical Sciences 2018; 17(9):865-80.
  18. 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 research notes 2014; 7(1):1-7.
  19. Shigemura K, Osawa K, Miura M, Tanaka K, Arakawa S, Shirakawa T, et al. Azithromycin resistance and its mechanism in Neisseria gonorrhoeae strains in Hyogo, Japan. Antimicrobial agents and chemotherapy 2015; 59(5):2695-9.
  20. Akya A, Aletaha M, Ghadiri K, Rezaee M. The frequency of mycoplasma hominis, mycoplasma genitalium and urea plasma urealyticum in women with cervicitis. Journal NI 2014; 1(2):31-7.
  21. Niakan M, Moradi B, Ragheb S. The prevalence of Ureaplasma urealyticumin semen of infertile men Niakan M*, Moradi B, Ragheb SH. Iranian Journal of Medical Microbiology 2009; 3(1):31-5.
  22. Leli C, Mencacci A, Bombaci JC, D'Alò F, Farinelli S, Vitali M, et al. Prevalence and antimicrobial susceptibility of Ureaplasma urealyticum and Mycoplasma hominis in a population of Italian and immigrant outpatients. Le Infezioni in Medicina 2012; 20(2):82-7.
  23. Robles-Menchero MJ, Sánchez-Aranda A, Alonso-de Mendieta M, Carballo-Mondragón E, Molina-López JF, Kably-Ambe A. Prevalence of Mycoplasma hominis and Ureaplasma urealyticum in couples with infertility during in vitro fertilization protocol. Ginecología y obstetricia de México 2021; 89(3):204-11.
  24. Song T, Liu Z, Zhang Y, Han Y, Huang J. Detection of Ureaplasma spp. serovars in genital tract of infertile males. Journal of Clinical Laboratory Analysis 2019; 33(5):e22865.
  25. Najar Peerayeh S, Samimi R. Detection of ureaplasma urealyticum in clinical samples from infertile women by polymerase chain reaction. Iranian J Pharmacol Therapeut 2007; 6(1):23-6.
  26. Maleki S, Motamedi H, Moosavian SM, Shahbaziyan N. Frequency of Mycoplasma hominis and Ureaplasma urealyticum in females with urogenital infections and habitual abortion history in Ahvaz, Iran; using multiplex PCR. Jundishapur J Microbiol 2013; 6(6).
  27. Ghorbanalinezhad E, Amirmozafari N, Akhavan Sepahi A, Khavari-nejad R. Survey on the genital Mycoplasmosis by multiplex PCR. Int J Mol Clin Microbiol 2014; 4(2):451-6.
  28. Pourabbas B, Rezaei Z, Mardaneh J, Shahian M, Alborzi A. Prevalence of Chlamydia trachomatis and Neisseria gonorrhoeae infections among pregnant women and eye colonization of their neonates at birth time, Shiraz, Southern Iran. BMC Infect Dis 2018; 18(1):1-4.
  29. Esteghamati A, Mazouri A, Sayyahfar S, Khanaliha K, Haghighi F, Faramarzi M, et al. Transmission Rates of Chlamydia trachomatis and Neisseria gonorrhoeae Infections from Pregnant Women to Newborns, Tehran, Iran. Jundishapur Journal of Microbiology 2020; 13(3):e92549.
  30. Ahmadi A, Mousavi A, Salimizand H, Hedayati MA, Ramazanzadeh R, Farhadifar F, et al. Prevalence of Neisseria gonorrhoeae in Western Iran. Japanese Journal of Infectious Diseases 2022; 75(1):1-4.
  31. Ghanbarzade N, Moghanni M, Goljahani N, Karamian M, Zare_Bidaki M. Frequency of Neisseria gonorrhoeae and Trichomonas vaginalis in women with vaginal discharge referring to the gynecology clinic of Vali-e-Asr Hospital in Birjand in 2018. Journal of Basic Research in Medical Sciences 2019; 6(2):51-7.
  32. Xu WH, Chen JJ, Sun Q, Wang LP, Jia YF, Xuan BB, et al. Chlamydia trachomatis, Ureaplasma urealyticum and Neisseria gonorrhoeae among C hinese women with urinary tract infections in S hanghai: A community‐based cross‐sectional study. Journal of Obstetrics and Gynaecology Research 2018; 44(3):495-502.
  33. Erfanian MR, Esmaili H, Ejtehadi MM. Study on Neisseria gonorrhoeae antibiogram and its resistance to Quinolones and third generation Cephalosporins in men with gonococcal urethritis. Zahedan J Res Med Sci 2005; 7(3).
  34. World Health Organization. Global antimicrobial resistance surveillance system (GLASS) report: early implementation; 2020.
  35. Khademi F, Sahebkar A. Antibiotic resistance of Neisseria species in Iran: A systematic review and meta-analysis. Asian Pacific Journal of Tropical Medicine 2019; 12(1):8.
  36. Afrasiabi S, Moniri R, Samimi M, Mousavi SG. The frequency of Neisseria gonorrhoeae endocervical infection among female carrier and changing trends of antimicrobial susceptibility patterns in Kashan, Iran. Iranian journal of microbiology 2014; 6(3):194-7.
  37. Kalantar E, Taati N, Ghasemian A. Detection of alarming increase in antibiotic resistant neisseria gonorrhoeae isolates in Karaj, Iran. MOJ Immunol 2018; 6(2):44-7.
  38. Bokaeian M, Iqbal-Qureshi M, Dabiri S. Antibiotic resistance of Neisseria gonorrhoeae isolated from gonorrhoeae patients. Zahedan Journal of Research in Medical Sciences 2010; 12(2):e94309.
  39. World Health Organization (WHO). WHO publishes list of bacteria for which new antibiotics are urgently needed. Geneva, Switzerland: WHO; 2017.
  40. Lee H, Unemo M, Kim HJ, Seo Y, Lee K, Chong Y. Emergence of decreased susceptibility and resistance to extended-spectrum cephalosporins in Neisseria gonorrhoeae in Korea. Journal of Antimicrobial Chemotherapy 2015; 70(9):2536-42.
  41. de Vega IF, Baliu-Piqué C, Mestres JB, Gómez AV, Vallés X, Gibert MA. Risk factors for antimicrobial-resistant Neisseria gonorrhoeae and characteristics of patients infected with gonorrhea. . Enferm Infec Microbiol Clin 2018; 36(3):165-8.
  42. Bayraktar MR, Ozerol IH, Gucluer N, Celik O. Prevalence and antibiotic susceptibility of Mycoplasma hominis and Ureaplasma urealyticum in pregnant women. International Journal of Infectious Diseases 2010; 14(2):e90-5.
  43. Azizmohammadi S, Azizmohammadi S. Antimicrobial susceptibility patterns of Ureaplasma urealyticum and Mycoplasma hominis isolated from pregnant women. Iranian Red Crescent Medical Journal 2015; 17(12).
  44. Mardaneh J, Mohammadzadeh A, Alavi MS, Zendehdel M, Bahri N, Mehraban M, et al. Occurrence of Ureaplasma urealyticumin in Women in the Northeast of Iran: Characterization of Resistance Trends. International Journal of Women's Health and Reproduction Sciences 2021; 9(4):274-9.
  45. Zhao L, Zhao S. TaqMan real-time quantitative PCR assay for detection of fluoroquinolone-resistant Neisseria gonorrhoeae. Current microbiology 2012; 65(6):692-5.
  46. Allen VG, Farrell DJ, Rebbapragada A, Tan J, Tijet N, Perusini SJ, et al. Molecular analysis of antimicrobial resistance mechanisms in Neisseria gonorrhoeae isolates from Ontario, Canada. Antimicrobial agents and chemotherapy 2011; 55(2):703-12.