Exploring the Prevalence of Neisseria gonorrhoeae in Women with Genitourinary Symptoms in Tehran, Iran
-
Narjes Noori Goodarzi
,
Shaghayegh Zafar
,
Naghmeh Pourmand
,
Soheila Ajdary
,
Mir Saeed Yekaninejad
,
Mohammad Reza Pourmand
,
Farzad Badmasti
Abstract
Background: Neisseria gonorrhoeae, the second most common sexually transmitted infection (STI) worldwide, affects one million people daily. We aimed to investigate the prevalence of gonorrhea in females with genital infections in Tehran, Iran.
Methods: First, a bioinformatic study was conducted to identify a conserved and high-prevalent gene marker for detection of N. gonorrhoeae. One desirable marker was selected and a pair of specific primers was designed to amplify it. The reliability of the primer pair was evaluated in silico and in vitro. Subsequently, 172 patients with genitourinary symptoms were enrolled and an endocervical swab specimen was obtained from each patient to evaluate the presence of N. gonorrhoeae in clinical specimens using the specific primers.
Results: Restriction endonuclease subunit S (resS, WP_003687768.1) was selected as a specific detection marker. The designed primer pair targeting resS showed specific and reliable detection of N. gonorrhoeae in silico and in vitro. Out of 172 clinical samples, seven (4.06%) cases were infected by N. gonorrhoeae. Statistical analysis of clinical manifestations showed that there was a significant association between the occurrence of N. gonorrhoeae and dysuria (P= 0.043), pelvic pain (P= 0.017), and fever (P = 0.045).
Conclusion: Three promising markers were introduced for development of point-of-care testing approaches. Moreover, this study highlights a 4% prevalence of gonorrhea among women with genitourinary symptoms in Iran, which reminds the urgent need for routine surveillance and new policies in management of STIs, particularly gonorrhea.
1. Noori Goodarzi N, Ajdary S, Yekaninejad MS, et al (2023). Reverse vaccinology approaches to introduce promising immunogenic and drug targets against antibiotic-resistant Neisseria gonorrhoeae: Thinking outside the box in current prevention and treatment. Infect Genet Evol, 112:105449.
2. WHO (2024). Gonorrhoea (Neisseria gonorrhoeae infection). https://www.who.int/news-room/fact-sheets/detail/gonorrhoea-(neisseria-gonorrhoeae-infection)
3. Ratnappuli A, Bissessor M, Arumugam S, et al (2022). Culture obtained from urethral swab of asymptomatic men who screen positive for Neisseria gonorrhoeae by urine nucleic acid amplification testing. Sex Transm Infect, 98 (2):139-141.
4. Omeershffudin UNM, Kumar S (2023). Emerging threat of antimicrobial resistance in Neisseria gonorrhoeae: pathogenesis, treatment challenges, and potential for vaccine development. Arch Microbiol, 205 (10):330.
5. Smolarczyk K, Mlynarczyk-Bonikowska B, Rudnicka E, et al (2021). The Impact of Selected Bacterial Sexually Transmitted Diseases on Pregnancy and Female Fertility. Int J Mol Sci, 22 (4): 2170.
6. Campaner AB, Matuoka ML (2023). Neisseria gonorrhoeae prevalence in females in São Paulo, Brazil: surveillance of the infection over a 11-year period. Braz J Microbiol, 54 (3):1835-1840.
7. Martín-Sánchez M, Fairley CK, Ong JJ, et al (2020). Clinical presentation of asymptomatic and symptomatic women who tested positive for genital gonorrhoea at a sexual health service in Melbourne, Australia. Epidemiol Infect, 148:e240.
8. Meyer T, Buder S (2020). The Laboratory Diagnosis of Neisseria gonorrhoeae: Current Testing and Future Demands. Pathogens, 9 (2):91.
9. European Centre for Disease Prevention and Control. Gonorrhoea. In: ECDC. Annual epidemiological report for 2017. Stockholm: ECDC; 2019.,
10. Bowen VB, Braxton J, Davis DW, et al. Sexually transmitted disease surveillance 2018.
11. Akya A, Hosseini M, Olfati M, et al (2017). The frequency of Chlamydia trachomatis and Neisseria gonorrhoeae infections among women in Kermanshah, Iran. Asian Biomedicine, 7 (5):681-685.
12. Zolfaghari P, Emamie AD, Rajabpour M, et al (2022). Antimicrobial susceptibility testing and molecular characterization of Neisseria gonorrhoeae in Tehran, Iran. Int J STD AIDS, 33 (7):660-665.
13. Rajabpour M, Emamie AD, Pourmand MR, et al (2020). Chlamydia trachomatis, Neisseria gonorrhoeae, and Trichomonas vaginalis among women with genitourinary infection and pregnancy-related complications in Tehran: A cross-sectional study. Int J STD AIDS, 31 (8):773-780.
14. Ilami O, Rahimian SH, Kargar M, et al (2013). Detection of Neisseria Gonorrhoeae and Chlamydia Trachomatis in Patients with Symptomatic Urethritis Using Multiplex PCR, Gram Stain and Urine Culture. Journal of Mazandaran University of Medical Sciences, 23 (103):11-18.
15. Chaudhari NM, Gupta VK, Dutta C (2016). BPGA- an ultra-fast pan-genome analysis pipeline. Sci Rep, 6 :24373.
16. Tønjum T, van Putten J (2017). 179 - Neisseria. In: Infectious Diseases (Fourth Edition). Ed(s), Cohen J, Powderly WG, Opal SM: Elsevier, pp. 1553-1564.e1.
17. Agresti A (2012). Categorical data analysis. ed. John Wiley & Sons.
18. Bland JM, Altman DG (1995). Multiple significance tests: the Bonferroni method. BMJ, 310 (6973):170.
19. World Health Organization (WHO) Progress report of the implementation of the global strategy for prevention and control of sexually transmitted infections: 2006–2015.
20. van Gemert C, Hellard M, Bradshaw CS, et al (2018). Syndromic management of sexually transmissible infections in resource-poor settings: a systematic review with meta-analysis of the abnormal vaginal discharge flowchart for Neisseria gonorrhoea and Chlamydia trachomatis. Sex Health, 15 (1):1-12.
21. Bignell C, Unemo M (2013). 2012 European guideline on the diagnosis and treatment of gonorrhoea in adults. Int J STD AIDS, 24 (2):85-92.
22. Centers for Disease Control and Prevention (2014). Recommendations for the laboratory-based detection of Chlamydia trachomatis and Neisseria gonorrhoeae--2014. MMWR Recomm Rep, 63 (RR-02):1-19.
23. Mahony JB, Song X, Chong S, et al (2001). Evaluation of the NucliSens Basic Kit for detection of Chlamydia trachomatis and Neisseria gonorrhoeae in genital tract specimens using nucleic acid sequence-based amplification of 16S rRNA. J Clin Microbiol, 39 (4):1429-35.
24. Chaudhry U, Saluja D (2002). Detection of Neisseria gonorrhoeae by PCR using orf1 gene as target. Sex Transm Infect, 78 (1):72.
25. Trembizki E, Buckley C, Donovan B, et al (2015). Direct real-time PCR-based detection of Neisseria gonorrhoeae 23S rRNA mutations associated with azithromycin resistance. J Antimicrob Chemother, 70 (12):3244-9.
26. Geraats-Peters CWM, Brouwers M, Schneeberger PM, et al (2005). Specific andSensitive Detection of Neisseria gonorrhoeae in ClinicalSpecimens by Real-Time PCR. J Clin Microbiol, 43 (11):5653-5659.
27. Wi T, Lahra MM, Ndowa F, et al (2017). Antimicrobial resistance in Neisseria gonorrhoeae: Global surveillance and a call for international collaborative action. PLoS Med, 14 (7):e1002344.
28. Abbai NS, Moodley P, Reddy T, et al (2015). Clinical evaluation of the OneStep Gonorrhea RapiCard InstaTest for detection of Neisseria gonorrhoeae in symptomatic patients from KwaZulu-Natal, South Africa. J Clin Microbiol, 53 (4):1348-50.
29. Alary M, Gbenafa-Agossa C, Aïna G, et al (2006). Evaluation of a rapid point-of-care test for the detection of gonococcal infection among female sex workers in Benin. Sex Transm Infect, 82 Suppl 5 (Suppl 5):v29-32.
30. Samarawickrama A, Cheserem E, Graver M, et al (2014). Pilot study of use of the BioStar Optical ImmunoAssay GC point-of-care test for diagnosing gonorrhoea in men attending a genitourinary medicine clinic. J Med Microbiol, 63 (Pt 8):1111-1112.
31. Nuñez-Forero L, Moyano-Ariza L, Gaitán-Duarte H, et al (2016). Diagnostic accuracy of rapid tests for sexually transmitted infections in symptomatic women. Sex Transm Infect, 92 (1):24-8.
32. Vasu K, Nagaraja V (2013). Diverse functions of restriction-modification systems in addition to cellular defense. Microbiol Mol Biol Rev, 77 (1):53-72.
33. Rotman E, Seifert HS (2014). The genetics of Neisseria species. Annu Rev Genet, 48:405-31.
34. Kirkcaldy RD, Weston E, Segurado AC, Hughes G (2019). Epidemiology of gonorrhoea: a global perspective. Sex Health, 16 (5):401-411.
35. Chemaitelly H, Harfouche M, Smolak A, et al (2024). Epidemiology of gonorrhea in countries of the Middle East and North Africa: systematic review, meta analyses, and meta regressions. BMC Glob Public Health, 2 (1):56.
36. Kocaata Z, Currie B, Beck E, et al (2024). A Qualitative Concept Elicitation Study to Understand Patient-Reported Symptoms and Impacts of Neisseria gonorrhoeae Infections in the United States. Sex Transm Dis, 51 (6): 393-399.
37. Ayinde O, Tan W, Hepburn T, et al (2020). Factors associated with time to presentation for individuals with symptomatic uncomplicated genital gonorrhoea: a cross sectional cohort study of GToG trial participants. Sex Transm Dis, 96 (4):251-257.
38. Wangnapi RA, Soso S, Unger HW, et al (2015). Prevalence and risk factors for Chlamydia trachomatis, Neisseria gonorrhoeae and Trichomonas vaginalis infection in pregnant women in Papua New Guinea. Sex Transm Dis, 91 (3):194-200.
39. Beatrous SV, Grisoli SB, Riahi RR, et al (2017). Cutaneous manifestations of disseminated gonococcemia. Dermatol Online J, 23 (1): 13030/qt33b24006.
40. Humayun S, Bali A, Avula S, et al (2023). Disseminated Gonococcal Infection With Dermatitis-Arthritis Syndrome. Cureus, 15 (9):e44991.
41. Markowicz S, Anstey JR, Hites M, et al (2014). Gonococcal aneurysm of the ascending aorta: case report and review of Neisseria gonorrhoeae endovascular infections. Sex Transm Dis, 41 (2):111-3.
42. Workowski KA, Bachmann LH, Chan PA, et al (2021). Sexually transmitted infections treatment guidelines, 2021. MMWR Recomm Rep, 70 (4):1-187.
43. Demissie E, Amare A, Birhanu M, et al (2024). Neisseria gonorrhoeae antimicrobial resistance patterns and associated risk factors in women of childbearing potential in northwestern Ethiopia. BMC Womens Health, 24 (1):82.
44. Itodo OA, Viriot D, Velter A, et al (2020). Trends and determinants of condomless sex in gonorrhoea patients diagnosed in France through the sentinel surveillance network ResIST, 2005–2014. BMC Public Health, 20 (1):1620.
45. Sharma D, Muralidhar S, Lachyan AS, Khunger N (2024). Risk factors associated with increasing prevalence of gonorrhea and the antimicrobial susceptibility profiles of Neisseria gonorrhoeae among adolescents: A decade-long, hospital-based study from India. Indian J Sex Transm Dis AIDS, 45 (1): 15-18.
2. WHO (2024). Gonorrhoea (Neisseria gonorrhoeae infection). https://www.who.int/news-room/fact-sheets/detail/gonorrhoea-(neisseria-gonorrhoeae-infection)
3. Ratnappuli A, Bissessor M, Arumugam S, et al (2022). Culture obtained from urethral swab of asymptomatic men who screen positive for Neisseria gonorrhoeae by urine nucleic acid amplification testing. Sex Transm Infect, 98 (2):139-141.
4. Omeershffudin UNM, Kumar S (2023). Emerging threat of antimicrobial resistance in Neisseria gonorrhoeae: pathogenesis, treatment challenges, and potential for vaccine development. Arch Microbiol, 205 (10):330.
5. Smolarczyk K, Mlynarczyk-Bonikowska B, Rudnicka E, et al (2021). The Impact of Selected Bacterial Sexually Transmitted Diseases on Pregnancy and Female Fertility. Int J Mol Sci, 22 (4): 2170.
6. Campaner AB, Matuoka ML (2023). Neisseria gonorrhoeae prevalence in females in São Paulo, Brazil: surveillance of the infection over a 11-year period. Braz J Microbiol, 54 (3):1835-1840.
7. Martín-Sánchez M, Fairley CK, Ong JJ, et al (2020). Clinical presentation of asymptomatic and symptomatic women who tested positive for genital gonorrhoea at a sexual health service in Melbourne, Australia. Epidemiol Infect, 148:e240.
8. Meyer T, Buder S (2020). The Laboratory Diagnosis of Neisseria gonorrhoeae: Current Testing and Future Demands. Pathogens, 9 (2):91.
9. European Centre for Disease Prevention and Control. Gonorrhoea. In: ECDC. Annual epidemiological report for 2017. Stockholm: ECDC; 2019.,
10. Bowen VB, Braxton J, Davis DW, et al. Sexually transmitted disease surveillance 2018.
11. Akya A, Hosseini M, Olfati M, et al (2017). The frequency of Chlamydia trachomatis and Neisseria gonorrhoeae infections among women in Kermanshah, Iran. Asian Biomedicine, 7 (5):681-685.
12. Zolfaghari P, Emamie AD, Rajabpour M, et al (2022). Antimicrobial susceptibility testing and molecular characterization of Neisseria gonorrhoeae in Tehran, Iran. Int J STD AIDS, 33 (7):660-665.
13. Rajabpour M, Emamie AD, Pourmand MR, et al (2020). Chlamydia trachomatis, Neisseria gonorrhoeae, and Trichomonas vaginalis among women with genitourinary infection and pregnancy-related complications in Tehran: A cross-sectional study. Int J STD AIDS, 31 (8):773-780.
14. Ilami O, Rahimian SH, Kargar M, et al (2013). Detection of Neisseria Gonorrhoeae and Chlamydia Trachomatis in Patients with Symptomatic Urethritis Using Multiplex PCR, Gram Stain and Urine Culture. Journal of Mazandaran University of Medical Sciences, 23 (103):11-18.
15. Chaudhari NM, Gupta VK, Dutta C (2016). BPGA- an ultra-fast pan-genome analysis pipeline. Sci Rep, 6 :24373.
16. Tønjum T, van Putten J (2017). 179 - Neisseria. In: Infectious Diseases (Fourth Edition). Ed(s), Cohen J, Powderly WG, Opal SM: Elsevier, pp. 1553-1564.e1.
17. Agresti A (2012). Categorical data analysis. ed. John Wiley & Sons.
18. Bland JM, Altman DG (1995). Multiple significance tests: the Bonferroni method. BMJ, 310 (6973):170.
19. World Health Organization (WHO) Progress report of the implementation of the global strategy for prevention and control of sexually transmitted infections: 2006–2015.
20. van Gemert C, Hellard M, Bradshaw CS, et al (2018). Syndromic management of sexually transmissible infections in resource-poor settings: a systematic review with meta-analysis of the abnormal vaginal discharge flowchart for Neisseria gonorrhoea and Chlamydia trachomatis. Sex Health, 15 (1):1-12.
21. Bignell C, Unemo M (2013). 2012 European guideline on the diagnosis and treatment of gonorrhoea in adults. Int J STD AIDS, 24 (2):85-92.
22. Centers for Disease Control and Prevention (2014). Recommendations for the laboratory-based detection of Chlamydia trachomatis and Neisseria gonorrhoeae--2014. MMWR Recomm Rep, 63 (RR-02):1-19.
23. Mahony JB, Song X, Chong S, et al (2001). Evaluation of the NucliSens Basic Kit for detection of Chlamydia trachomatis and Neisseria gonorrhoeae in genital tract specimens using nucleic acid sequence-based amplification of 16S rRNA. J Clin Microbiol, 39 (4):1429-35.
24. Chaudhry U, Saluja D (2002). Detection of Neisseria gonorrhoeae by PCR using orf1 gene as target. Sex Transm Infect, 78 (1):72.
25. Trembizki E, Buckley C, Donovan B, et al (2015). Direct real-time PCR-based detection of Neisseria gonorrhoeae 23S rRNA mutations associated with azithromycin resistance. J Antimicrob Chemother, 70 (12):3244-9.
26. Geraats-Peters CWM, Brouwers M, Schneeberger PM, et al (2005). Specific andSensitive Detection of Neisseria gonorrhoeae in ClinicalSpecimens by Real-Time PCR. J Clin Microbiol, 43 (11):5653-5659.
27. Wi T, Lahra MM, Ndowa F, et al (2017). Antimicrobial resistance in Neisseria gonorrhoeae: Global surveillance and a call for international collaborative action. PLoS Med, 14 (7):e1002344.
28. Abbai NS, Moodley P, Reddy T, et al (2015). Clinical evaluation of the OneStep Gonorrhea RapiCard InstaTest for detection of Neisseria gonorrhoeae in symptomatic patients from KwaZulu-Natal, South Africa. J Clin Microbiol, 53 (4):1348-50.
29. Alary M, Gbenafa-Agossa C, Aïna G, et al (2006). Evaluation of a rapid point-of-care test for the detection of gonococcal infection among female sex workers in Benin. Sex Transm Infect, 82 Suppl 5 (Suppl 5):v29-32.
30. Samarawickrama A, Cheserem E, Graver M, et al (2014). Pilot study of use of the BioStar Optical ImmunoAssay GC point-of-care test for diagnosing gonorrhoea in men attending a genitourinary medicine clinic. J Med Microbiol, 63 (Pt 8):1111-1112.
31. Nuñez-Forero L, Moyano-Ariza L, Gaitán-Duarte H, et al (2016). Diagnostic accuracy of rapid tests for sexually transmitted infections in symptomatic women. Sex Transm Infect, 92 (1):24-8.
32. Vasu K, Nagaraja V (2013). Diverse functions of restriction-modification systems in addition to cellular defense. Microbiol Mol Biol Rev, 77 (1):53-72.
33. Rotman E, Seifert HS (2014). The genetics of Neisseria species. Annu Rev Genet, 48:405-31.
34. Kirkcaldy RD, Weston E, Segurado AC, Hughes G (2019). Epidemiology of gonorrhoea: a global perspective. Sex Health, 16 (5):401-411.
35. Chemaitelly H, Harfouche M, Smolak A, et al (2024). Epidemiology of gonorrhea in countries of the Middle East and North Africa: systematic review, meta analyses, and meta regressions. BMC Glob Public Health, 2 (1):56.
36. Kocaata Z, Currie B, Beck E, et al (2024). A Qualitative Concept Elicitation Study to Understand Patient-Reported Symptoms and Impacts of Neisseria gonorrhoeae Infections in the United States. Sex Transm Dis, 51 (6): 393-399.
37. Ayinde O, Tan W, Hepburn T, et al (2020). Factors associated with time to presentation for individuals with symptomatic uncomplicated genital gonorrhoea: a cross sectional cohort study of GToG trial participants. Sex Transm Dis, 96 (4):251-257.
38. Wangnapi RA, Soso S, Unger HW, et al (2015). Prevalence and risk factors for Chlamydia trachomatis, Neisseria gonorrhoeae and Trichomonas vaginalis infection in pregnant women in Papua New Guinea. Sex Transm Dis, 91 (3):194-200.
39. Beatrous SV, Grisoli SB, Riahi RR, et al (2017). Cutaneous manifestations of disseminated gonococcemia. Dermatol Online J, 23 (1): 13030/qt33b24006.
40. Humayun S, Bali A, Avula S, et al (2023). Disseminated Gonococcal Infection With Dermatitis-Arthritis Syndrome. Cureus, 15 (9):e44991.
41. Markowicz S, Anstey JR, Hites M, et al (2014). Gonococcal aneurysm of the ascending aorta: case report and review of Neisseria gonorrhoeae endovascular infections. Sex Transm Dis, 41 (2):111-3.
42. Workowski KA, Bachmann LH, Chan PA, et al (2021). Sexually transmitted infections treatment guidelines, 2021. MMWR Recomm Rep, 70 (4):1-187.
43. Demissie E, Amare A, Birhanu M, et al (2024). Neisseria gonorrhoeae antimicrobial resistance patterns and associated risk factors in women of childbearing potential in northwestern Ethiopia. BMC Womens Health, 24 (1):82.
44. Itodo OA, Viriot D, Velter A, et al (2020). Trends and determinants of condomless sex in gonorrhoea patients diagnosed in France through the sentinel surveillance network ResIST, 2005–2014. BMC Public Health, 20 (1):1620.
45. Sharma D, Muralidhar S, Lachyan AS, Khunger N (2024). Risk factors associated with increasing prevalence of gonorrhea and the antimicrobial susceptibility profiles of Neisseria gonorrhoeae among adolescents: A decade-long, hospital-based study from India. Indian J Sex Transm Dis AIDS, 45 (1): 15-18.
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| Neisseria gonorrhoeae Prevalence Gonorrhea | ||
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How to Cite
1.
Noori Goodarzi N, Zafar S, Pourmand N, Ajdary S, Yekaninejad MS, Pourmand M, Badmasti F. Exploring the Prevalence of Neisseria gonorrhoeae in Women with Genitourinary Symptoms in Tehran, Iran. Iran J Public Health. 2025;54(4):850-859.
