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RESEARCH ARTICLE

Antimicrobial resistance of Neisseria gonorrhoeae in Jakarta, Indonesia: a cross-sectional study

Wresti Indriatmi A B , Rizky Lendl Prayogo https://orcid.org/0000-0002-7516-710X A B C , Hanny Nilasari A B and Lis Surachmiati Suseno A B
+ Author Affiliations
- Author Affiliations

A Department of Dermatology and Venereology, Faculty of Medicine, Universitas Indonesia, Jalan Pangeran Diponegoro No. 71, RW 05, Kelurahan Kenari, Kecamatan Senen, Kota Jakarta Pusat, 10430, DKI Jakarta.

B Dr Cipto Mangunkusumo National General Hospital, Jakarta, Indonesia, Jalan Pangeran Diponegoro No. 71, RW 05, Kelurahan Kenari, Kecamatan Senen, Kota Jakarta Pusat, 10430, DKI Jakarta.

C Corresponding author. Email: rlendlprayogo@gmail.com

Sexual Health 17(1) 9-14 https://doi.org/10.1071/SH19140
Submitted: 15 January 2019  Accepted: 28 August 2019   Published: 16 December 2019

Abstract

Background: Neisseria gonorrhoeae has developed resistance to various antimicrobials. At least 10 countries have reported treatment failures with extended-spectrum cephalosporins. Periodic surveillance is essential to determine local treatment guidelines. This study was conducted to determine the resistance of N. gonorrhoeae to penicillin, tetracycline, levofloxacin, cefixime and ceftriaxone among the high-risk population for acquiring STIs in Jakarta and to identify factors associated with resistance. Methods: A cross-sectional study was conducted in Jakarta, Indonesia, from September to November 2018. In all, 98 high-risk males and females who fulfilled the study criteria were included. Specimens were collected from urethral or endocervical swabs, put into Amies transport medium and then transported to the Laboratory of Clinical Microbiology, Universitas Indonesia for culture and identification. Proven gonococcal isolates were examined for susceptibility to various antimicrobials using the disk diffusion method according to Clinical and Laboratory Standard Institute guidelines. Results: Of the 98 specimens, 35 were confirmed to be N. gonorrhoeae. The proportion of N. gonorrhoeae specimens resistant to penicillin, tetracycline, levofloxacin, cefixime and ceftriaxone among the high-risk population was 97.1%, 97.1%, 34.3%, 0% and 0% respectively. The possible factors associated with resistance could only be analysed for levofloxacin. Age, sexual orientation and a history of orogenital sexual activity during the past month were not associated with N. gonorrhoeae resistance to levofloxacin. Conclusion: This study detected no resistance of N. gonorrhoeae to cefixime and ceftriaxone. Further studies with larger samples are needed to obtain more representative results of N. gonorrhoeae resistance and the possible factors associated with resistance.

Additional keywords: antibiotic, gonorrhoea, susceptibility.


References

[1]  World Health Organization (WHO). Executive summary. In WHO guidelines for the treatment of Neisseria gonorrhoeae. Geneva: WHO; 2016. pp. 1–5.

[2]  World Health Organization (WHO). Annexes. In Report on global sexually transmitted infection surveillance. Geneva: WHO; 2015. pp. 37–8.

[3]  Kemenkes. Prevalensi HIV, sifilis, gonore, dan klamidia. In Surveilans terpadu biologis dan perilaku (STBP). Jakarta: Direktorat Jenderal Pengendalian Penyakit dan Penyehatan Lingkungan Kementerian Kesehatan Republik Indonesia; 2015. pp. 32–5.

[4]  Ison CA. Biology of Neisseria gonorrhoeae and the clinical picture of infection. In Gross G, Tyring SK, editors. Sexually transmitted infections and sexually transmitted diseases. Heidelberg: Springer; 2011. pp. 77–90.

[5]  World Health Organization (WHO). Gonococcal antimicrobial susceptibility. In Report on global sexually transmitted infection surveillance. Geneva: WHO; 2015. pp. 28–34.

[6]  Daili SF, Indriatmi W, Zubier F, Nilasari H. Diagnosis & pengobatan infeksi menular seksual. In Indriatmi W, Daili SF, Tarmizi SN, Prameswari HD, editors. Pedoman Nasional penanganan infeksi menular seksual. Jakarta: Direktorat Jenderal Pengendalian Penyakit dan Penyehatan Lingkungan Kementerian Kesehatan Republik Indonesia; 2016. pp. 21–54.

[7]  Kemenkes. Profil kesehatan Kecamatan Pasar Rebo tahun 2016. Jakarta: Puskesmas Kecamatan Pasar Rebo; 2016.

[8]  Kemenkes. Profil kesehatan Kecamatan Tambora tahun 2016. Jakarta: Puskesmas Kecamatan Tambora; 2016.

[9]  Nilasari H. Prevalensi infeksi menular seksual dan aspek sosial pada WPS dalam rehabilitasi di Panti Sosial Karya Wanita Mulya Jaya Departemen Sosial Pasar Rebo Jakarta. MDVI 2014; 41 147–51.

[10]  Daili SF, Indriatmi W, Zubier F, Nilasari H. Pemeriksaan klinis pasien infeksi menular seksual. In Indriatmi W, Daili SF, Tarmizi SN, Prameswari HD, editors. Pedoman Nasional penanganan infeksi menular seksual. Jakarta: Direktorat Jenderal Pengendalian Penyakit dan Penyehatan Lingkungan Kementerian Kesehatan RI; 2016. pp. 11–20.

[11]  Knapp JS. Neisseria gonorrhoeae confirmatory identification and antimicrobial susceptibility testing. In Knapp JS, editor. Manual for the laboratory identification and antimicrobial susceptibility testing of bacterial pathogens of public health importance in the developing world. Atlanta: World Health Organization; 2003. pp. 63–102.

[12]  Patel JB, Weinstein MP, Eliopoulos GM, Jenkins SG, Lewis II JS, Limbago B, et al. Neisseria gonorrhoeae. In M100 performance standards for antimicrobial susceptibility testing. 27th edn. Pennsylvania: Clinical and Laboratory Standards Institute; 2017. pp. 72–7.

[13]  Beauduy CE, Winston LG. Sulfonamides, trimethoprime, & quinolones. In Katzung BG, editor. Basic & clinical pharmacology. 14th edn. San Francisco: McGraw-Hill; 2018. pp. 834–41.

[14]  Aditama TY, Subuh M, Wandra T, Daili SF, Indriatmi W, Zubier F, et al. Diagnosis dan pengobatan infeksi menular seksual. In Daili SF, Indriatmi W, Wandra T, Hastuti EB, Sukmaputri IO, editors. Pedoman Nasional penanganan infeksi menular seksual. Jakarta: Direktorat Jenderal Pengendalian Penyakit dan Penyehatan Lingkungan Kementerian Kesehatan RI; 2011. pp. 23–56.

[15]  World Health Organization (WHO). Gonococcal infections. In Guidelines for the management of sexually transmitted infections. Geneva: WHO; 2001. pp. 32–4.

[16]  Unemo M, del Rio C, Shafer WM. Antimicrobial resistance expressed by Neisseria gonorrhoeae: a major global public health problem in the 21st century. Microbiol Spectr 2016; 4 1–32.
Antimicrobial resistance expressed by Neisseria gonorrhoeae: a major global public health problem in the 21st century.Crossref | GoogleScholarGoogle Scholar |

[17]  Araneta CMP, Juayang AC, Lim JPT, Quilop EMG, Casaysay NJG, Tamesis GML, et al Antibiotic susceptibility monitoring of Neisseria gonorrhoeae in Bacolod City, Philippines. Trop Med Infect Dis 2017; 2 45
Antibiotic susceptibility monitoring of Neisseria gonorrhoeae in Bacolod City, Philippines.Crossref | GoogleScholarGoogle Scholar |

[18]  Li W, Zhu B-Y, Qin S-Q, Yang M-C, Liang M, He S, et al Surveillanve of antimicrobial susceptibilities of Neisseria gonorrhoeae from 2013 to 2015 in Guangxi Province, China. Jpn J Infect Dis 2018; 71 148–51.
Surveillanve of antimicrobial susceptibilities of Neisseria gonorrhoeae from 2013 to 2015 in Guangxi Province, China.Crossref | GoogleScholarGoogle Scholar | 29279442PubMed |

[19]  Phouangsouvanh S, Mayxay M, Keoluangkhot V, Vongsouvath M, Davong V, Dance DAB. Antibiotic susceptibility of Neisseria gonorrhoeae in Vientiane, Lao PDR. J Glob Antimicrob Resist 2017; 13 91–3.
| 29229280PubMed |

[20]  Sharma M, Rizvi M, Gupta R, Azam M, Khan HM, Parvez A, et al Alarming resistance of Neisseria gonorrhoeae in a tertiary care hospital of North India. Indian J Med Microbiol 2018; 36 285–8.
Alarming resistance of Neisseria gonorrhoeae in a tertiary care hospital of North India.Crossref | GoogleScholarGoogle Scholar | 30084426PubMed |

[21]  Tribuddharat C, Pongpech P, Charoenwatachokchai A, Lokpichart S, Srifuenfung S, Sonprasert S. Gonococcal antimicrobial susceptibility and the prevalence of blaTEM-1 and blaTEM-135 genes in Neisseria gonorrhoeae isolates from Thailand. Jpn J Infect Dis 2017; 70 213–15.
Gonococcal antimicrobial susceptibility and the prevalence of blaTEM-1 and blaTEM-135 genes in Neisseria gonorrhoeae isolates from Thailand.Crossref | GoogleScholarGoogle Scholar | 27580580PubMed |

[22]  Tshokey T, Tshering T, Pradha AR, Adhikari D, Sharma R, Gurung K, et al Antibiotic resistance in Neisseria gonorrhoea and treatment outcomes of gonococcal urethritis suspected patients in two large hospitals in Bhutan, 2015 PLoS One 2018; 13 e0201721
Antibiotic resistance in Neisseria gonorrhoea and treatment outcomes of gonococcal urethritis suspected patients in two large hospitals in Bhutan, 2015Crossref | GoogleScholarGoogle Scholar | 30067836PubMed |

[23]  Wu X, Qin X, Huang J, Wang F, Li M, Wu Z, et al Determining the in vitro susceptibility of Neisseria gonorrhoeae isolates from 8 cities in Guangdong Province through an improved microdilution method. Diagn Microbiol Infect Dis 2018; 92 325–31.
Determining the in vitro susceptibility of Neisseria gonorrhoeae isolates from 8 cities in Guangdong Province through an improved microdilution method.Crossref | GoogleScholarGoogle Scholar | 30292397PubMed |

[24]  Affolabi D, Goma E, Sogbo F, Ahotin G, Orekan J, Massou F, et al Antimicrobial susceptibility profile of Neisseria gonorrhoeae isolated in Cotonou, Benin (2015–2017). Sex Transm Infect 2018; 94 20
Antimicrobial susceptibility profile of Neisseria gonorrhoeae isolated in Cotonou, Benin (2015–2017).Crossref | GoogleScholarGoogle Scholar | 29021407PubMed |

[25]  Ali S, Sewunet T, Sahlemariam Z, Kibru G. Neisseria gonorrhoeae among suspects of sexually transmitted infection in Gambella Hospital, Ethiopia: risk factors and drug resistance. BMC Res Notes 2016; 9 439
Neisseria gonorrhoeae among suspects of sexually transmitted infection in Gambella Hospital, Ethiopia: risk factors and drug resistance.Crossref | GoogleScholarGoogle Scholar | 27619365PubMed |

[26]  Mabonga E, Parkes-Ratanshi R, Riedel S, Nabweyambo S, Mbabazi O, Taylor C, et al Complete ciprofloxacin resistance in gonococcal isolates in an urban Ugandan clinic: findings from a cross-sectional study. Int J STD AIDS 2019; 30 256–63.
| 30392463PubMed |

[27]  Yéo A, Kouamé-Blavo B, Kouamé C, Ouattara A, Yao A, Gbedé BD, et al Establishment of a Gonococcal Antimicrobial Surveillance Programme, in accordance with World Health Organization standards, in Côte d’Ivoire, Western Africa, 2014–2017. Sex Transm Dis 2019; 46 179–84.
Establishment of a Gonococcal Antimicrobial Surveillance Programme, in accordance with World Health Organization standards, in Côte d’Ivoire, Western Africa, 2014–2017.Crossref | GoogleScholarGoogle Scholar | 30461598PubMed |

[28]  Yeshanew AG, Geremew RA. Neisseria gonorrhoae and their antimicrobial susceptibility patterns among symptomatic patients from Gondar town, north West Ethiopia. Antimicrob Resist Infect Control 2018; 7 85
Neisseria gonorrhoae and their antimicrobial susceptibility patterns among symptomatic patients from Gondar town, north West Ethiopia.Crossref | GoogleScholarGoogle Scholar | 30026943PubMed |

[29]  Bazzo ML, Golfetto L, Gaspar PC, Pires AF, Ramos MC, Franchini M, et al First nationwide antimicrobial susceptibility surveillance for Neisseria gonorrhoeae in Brazil, 2015–16. J Antimicrob Chemother 2018; 73 1854–61.
First nationwide antimicrobial susceptibility surveillance for Neisseria gonorrhoeae in Brazil, 2015–16.Crossref | GoogleScholarGoogle Scholar | 29635367PubMed |

[30]  Lee RS, Seemann T, Heffernan H, Kwong JC, da Silva AG, Carter GP, et al Genomic epidemiology and antimicrobial resistance of Neisseria gonorrhoeae in New Zealand. J Antimicrob Chemother 2018; 73 353–64.
Genomic epidemiology and antimicrobial resistance of Neisseria gonorrhoeae in New Zealand.Crossref | GoogleScholarGoogle Scholar | 29182725PubMed |

[31]  McAuliffe G, Smith M, Brokenshire M, Forster R, Reid M, Roberts S. Keeping track of antimicrobial resistance for Neisseria gonorrhoeae in Auckland, New Zealand: past, present and future considerations. N Z Med J 2018; 131 71–7.
| 29927918PubMed |

[32]  Daili SF, Indriatmi W, Zubier F, Nilasari H. Pertimbangan praktis pengobatan infeksi menular seksual. In Indriatmi W, Daili SF, Tarmizi SN, Prameswari HD, editors. Pedoman Nasional penanganan infeksi menular seksual. Jakarta: Direktorat Jenderal Pengendalian Penyakit dan Penyehatan Lingkungan Kementerian Kesehatan Republik Indonesia; 2016. pp. 55–9.

[33]  Yasuda M, Hatazaki K, Ito S, Kitanohara M, Yoh M, Kojima M, et al Antimicrobial susceptibility of Neisseria gonorrhoeae in Japan from 2000 to 2015. Sex Transm Dis 2017; 44 149–53.
| 28178112PubMed |

[34]  Hananta IPY, van Dam AP, Bruisten SM, van der Loeff MFS, Soebono H, de Vries HJ. Gonorrhea in Indonesia: high prevalence of asymptomatic urogenital gonorrhea but no circulating extended spectrum cephalosporins-resistant Neisseria gonorrhoeae strains in Jakarta, Yogyakarta, and Denpasar, Indonesia. Sex Transm Dis 2016; 43 608–16.
Gonorrhea in Indonesia: high prevalence of asymptomatic urogenital gonorrhea but no circulating extended spectrum cephalosporins-resistant Neisseria gonorrhoeae strains in Jakarta, Yogyakarta, and Denpasar, Indonesia.Crossref | GoogleScholarGoogle Scholar |

[35]  Centers for Disease Control and Prevention. Sexually transmitted disease surveillance 2015: Gonococcal Isolate Surveillance Project (GISP) supplement and profiles. Atlanta: Department of Health and Human Services; 2017.

[36]  Cole MJ, Spiteri G, Town K, Unemo M, Hoffman S, Chisholm SA, et al Risk factors for antimicrobial-resistant Neisseria gonorrhoeae in Europe. Sex Transm Dis 2014; 41 723–9.
Risk factors for antimicrobial-resistant Neisseria gonorrhoeae in Europe.Crossref | GoogleScholarGoogle Scholar | 25581808PubMed |

[37]  Goldstein E, Kirkcaldy RD, Reshef D, Berman S, Weinstock H, Sabeti P, et al Factors related to increasing prevalence of resistance to ciprofloxacin and other antimicrobial drugs in Neisseria gonorrhoeae, United States. Emerg Infect Dis 2012; 18 1290–7.
Factors related to increasing prevalence of resistance to ciprofloxacin and other antimicrobial drugs in Neisseria gonorrhoeae, United States.Crossref | GoogleScholarGoogle Scholar | 22840274PubMed |

[38]  World Health Organization (WHO). Dissemination, updating, and implementation of the guidelines. In WHO guidelines for the treatment of Neisseria gonorrhoeae. Geneva: WHO; 2016. pp. 15–16.

[39]  Deguchi T, Yasuda M, Yokoi S. Treatment of uncomplicated gonococcal urethritis by double-dosing of 200 mg cefixime at a 6-h interval. J Infect Chemother 2003; 9 35–9.
Treatment of uncomplicated gonococcal urethritis by double-dosing of 200 mg cefixime at a 6-h interval.Crossref | GoogleScholarGoogle Scholar | 12673405PubMed |

[40]  Yokoi S, Deguchi T, Ozawa T, Yasuda M, Ito S, Kubota Y, et al Threat to cefixime treatment for gonorrhea. Emerg Infect Dis 2007; 13 1275–7.
| 17953118PubMed |

[41]  Tapsall JW, Ndowa F, Lewis DA, Unemo M. Meeting the public health challenge of multidrug- and extensively drug-resistant Neisseria gonorrhoeae. Expert Rev Anti Infect Ther 2009; 7 821–34.
Meeting the public health challenge of multidrug- and extensively drug-resistant Neisseria gonorrhoeae.Crossref | GoogleScholarGoogle Scholar | 19735224PubMed |

[42]  Unemo M, Golparian D, Syversen G, Vestrheim DF, Moi H. Two cases of verified clinical failures using internationally recommended first-line cefixime for gonorrhoea treatment, Norway, 2010. Euro Surveill 2010; 15 19721
Two cases of verified clinical failures using internationally recommended first-line cefixime for gonorrhoea treatment, Norway, 2010.Crossref | GoogleScholarGoogle Scholar | 21144442PubMed |

[43]  Barry PM, Klausner JD. The use of cephalosporins for gonorrhea: the impending problem of resistance. Expert Opin Pharmacother 2009; 10 555–77.
The use of cephalosporins for gonorrhea: the impending problem of resistance.Crossref | GoogleScholarGoogle Scholar | 19284360PubMed |