year 18, Issue 4 (July - August 2024)
Iran J Med Microbiol 2024, 18(4): 238-246 |
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Rosana Y, Utami L I, Yasmon A, Azizah F, Nilasari H, Krisanti I A. Antimicrobial Susceptibility Pattern and Molecular Characteristics of Multidrug-resistant Neisseria gonorrhoeae in Jakarta, Indonesia. Iran J Med Microbiol 2024; 18 (4) :238-246
URL: http://ijmm.ir/article-1-2368-en.html
URL: http://ijmm.ir/article-1-2368-en.html
Yeva Rosana1 
, Louisa Ivana Utami2 , Andi Yasmon3 , Fitri Azizah4 , Hanny Nilasari4 , Inge Ade Krisanti4
, Louisa Ivana Utami2 , Andi Yasmon3 , Fitri Azizah4 , Hanny Nilasari4 , Inge Ade Krisanti4
1- Department of Microbiology, Faculty of Medicine, Universitas Indonesia- Cipto Mangunkusumo Hospital, Jakarta, Indonesia , yeva.rosana@ui.ac.id
2- Master’s Programme in Biomedical Sciences, Faculty of Medicine, Universitas Indonesia, Jakarta, Indonesia & Department of Microbiology, Faculty of Medicine, Universitas Sultan Ageng Tirtayasa, Jakarta, Indonesia
3- Department of Microbiology, Faculty of Medicine, Universitas Indonesia- Cipto Mangunkusumo Hospital, Jakarta, Indonesia
4- Department of Dermato-venereology, Faculty of Medicine, Universitas Indonesia- Cipto Mangunkusumo Hospital, Jakarta, Indonesia
2- Master’s Programme in Biomedical Sciences, Faculty of Medicine, Universitas Indonesia, Jakarta, Indonesia & Department of Microbiology, Faculty of Medicine, Universitas Sultan Ageng Tirtayasa, Jakarta, Indonesia
3- Department of Microbiology, Faculty of Medicine, Universitas Indonesia- Cipto Mangunkusumo Hospital, Jakarta, Indonesia
4- Department of Dermato-venereology, Faculty of Medicine, Universitas Indonesia- Cipto Mangunkusumo Hospital, Jakarta, Indonesia
Abstract: (621 Views)
Background and Objective: There is an increasing rate of antibiotic resistance in Neisseria gonorrhoeae (N. gonorrhoeae). Several obstacles affect the culture and susceptibility testing of N. gonorrhoeae. This study was aimed to determine the antimicrobial susceptibility pattern and molecular characteristics in multidrug-resistant (MDR) N. gonorrhoeae in Jakarta, Indonesia.
Materials and Methods: Forty-one endocervical specimens were streaked onto the chocolate agar and then gently rolled onto a glass object. The suspected colonies were identified by Gram staining, oxidase testing, and biochemical identification using VITEK® 2 NH cards. The antimicrobial susceptibility testing was performed using the disk diffusion or E-test method. Molecular detection of N. gonorrhoeae was carried out using the SYBR green real-time PCR targeting the opa gene. The multiplex real-time PCR with high-resolution melting (HRM) was also conducted to analyze the gene mutations in penA and 23S rRNA. DNA sequencing was used to confirm penA and 23S rRNA mutations.
Results: SYBR green real-time PCR against the opa gene on direct specimens detected N. gonorrhoeae with higher positivity rate (49%) compared to the culture (34%). Susceptibility testing detected 11.1% N. gonorrhoeae resistant to cefixime, whereas resistance to azithromycin and ceftriaxone was 0%. The resistance of N. gonorrhoeae to levofloxacin and kanamycin was 33.3% and 88.9%, respectively. All isolates were resistant to penicillin, tetracycline and ciprofloxacin. There were no mutations in the penA genes Ala501, Gly545Ser, 23S rRNA A2059G and C2611T.
Conclusion: Cefixime resistance was found in our samples. This resistencewas not correlated with penA gene mutations. All isolates were still susceptiblle to azithromycin, which was in line with its molecular characteristics. The SYBR green real-time PCR targeting the opa gene successfully detected the DNA extracted from endocervical swabs as N. gonorrhoeae.
Keywords: Molecular characteristic, Neisseria gonorrhoeae, Susceptibility Pattern, SYBR green real-time PCR
Type of Study: Original Research Article |
Subject:
Medical Bacteriology
Received: 2024/05/29 | Accepted: 2024/08/25 | ePublished: 2024/09/29
Received: 2024/05/29 | Accepted: 2024/08/25 | ePublished: 2024/09/29
References
1. Levinson W. Review of Medical Microbiology and Immunology. 28th ed. New York, USA: McGraw-Hill Medical. 2018. pp.128-33.
2. Carroll KC, Hobden JA, Miller S, Morse SA, Mietzner TA, Detrick B, et al. Adelberg's Medical Microbiology, 27e. New York, USA: McGraw-Hill Education; 2019.
3. Wi T, Lahra MM, Ndowa F, Bala M, Dillon JA, Ramon-Pardo P, et al. Antimicrobial resistance in Neisseria gonorrhoeae: global surveillance and a call for international collaborative action. PLoS Med. 2017;14(7):e1002344. [DOI:10.1371/journal.pmed.1002344]
4. Reimche JL, Chivukula VL, Schmerer MW, Joseph SJ, Pham CD, Schlanger K, et al. Genomic analysis of the predominant strains and antimicrobial resistance determinants within 1479 Neisseria gonorrhoeae isolates from the US Gonococcal Isolate Surveillance Project in 2018. Sex Transm Dis. 2021;48(8S):S78-87. [DOI:10.1097/OLQ.0000000000001471]
5. Singh A, Turner JM, Tomberg J, Fedarovich A, Unemo M, Nicholas RA, et al. Mutations in penicillin-binding protein 2 from cephalosporin-resistant Neisseria gonorrhoeae hinder ceftriaxone acylation by restricting protein dynamics. J Biol Chem. 2020;295(21):7529-43. [DOI:10.1074/jbc.RA120.012617]
6. Belkacem A, Jacquier H, Goubard A, Mougari F, La Ruche G, Patey O, et al. Molecular epidemiology and mechanisms of resistance of azithromycin-resistant Neisseria gonorrhoeae isolated in France during 2013-14. J Antimicrob Chemother. 2016;71(9):2471-8. [DOI:10.1093/jac/dkw182]
7. Chisholm SA, Dave J, Ison CA. High-level azithromycin resistance occurs in Neisseria gonorrhoeae as a result of a single point mutation in the 23S rRNA genes. Antimicrob Agents Chemother. 2010;54(9):3812-6. [DOI:10.1128/AAC.00309-10]
8. Rositawati A, Sawitri S, Hidayati AN. Neisseria gonorrhoeae resistance test against cefixime in gonorrhea patients in Surabaya. Dermatol Rep. 2019;11(s1):8060. [DOI:10.4081/dr.2019.8060]
9. Puspandari N, Roselinda R, Sunarno S, Kharirie K, Sariadji K, Pasaribu LR. Prevalensi dan Pola Resistensi N. gonorrhoeae Terhadap Beberapa Antibiotik pada Wanita Penjaja Seks di Jakarta Timur, Tangerang dan Palembang Tahun 2012. J Biotek Medisiana Indones. 2016;5(1):57-67.
10. Unemo M, Golparian D, Nicholas R, Ohnishi M, Gallay A, Sednaoui P. High-level cefixime-and ceftriaxone-resistant Neisseria gonorrhoeae in France: novel penA mosaic allele in a successful international clone causes treatment failure. Antimicrob Agents Chemother. 2012;56(3):1273-80. [DOI:10.1128/AAC.05760-11]
11. Tanaka M, Furuya R, Kobayashi I, Ohno A, Kanesaka I. Molecular characteristics and antimicrobial susceptibility of penicillinase-producing Neisseria gonorrhoeae isolates in Fukuoka, Japan, 1996-2018. J Glob Antimicrob Resist. 2021;26:45-51. [DOI:10.1016/j.jgar.2021.04.014]
12. Latif AS, Gwanzura L, Machiha A, Ndowa F, Tarupiwa A, Gudza-Mugabe M, et al. Antimicrobial susceptibility in Neisseria gonorrhoeae isolates from five sentinel surveillance sites in Zimbabwe, 2015-2016. Sex Transm Infect. 2018;94(1):62-6. [DOI:10.1136/sextrans-2016-053090]
13. Unemo M, Shafer WM. Antimicrobial resistance in Neisseria gonorrhoeae in the 21st century: past, evolution, and future. Clin Microbiol Rev. 2014;27(3):587-613. [DOI:10.1128/CMR.00010-14]
14. Donà V, Kasraian S, Lupo A, Guilarte YN, Hauser C, Furrer H, et al. Multiplex real-time PCR assay with high-resolution melting analysis for characterization of antimicrobial resistance in Neisseria gonorrhoeae. J Clin Microbiol. 2016;54(8):2074-81. [DOI:10.1128/JCM.03354-15]
15. Yasmon A, Febriani R, Utami LI, Fithriyah F, Rosana Y, Ibrahim F, et al. Development of a SYBR Green real-time PCR-based assay system for detection of Neisseria gonorrhoeae. J Med Sci. 2022;54(1):1-9. [DOI:10.19106/JMedSci005401202201]
16. Geraats-Peters CW, Brouwers M, Schneeberger PM, Van Der Zanden AG, Bruisten SM, Weers-Pothoff G, et al. Specific and Sensitive Detection of Neisseria Gonorrhoeae in Clinical Specimens by Real-Time PCR. J Clin Microbiol. 2005;43(11):5653-9. [DOI:10.1128/JCM.43.11.5653-5659.2005]
17. Calado J, Castro R, Lopes Â, Campos MJ, Rocha M, Pereira F. Antimicrobial resistance and molecular characteristics of Neisseria gonorrhoeae isolates from men who have sex with men. Int J Infect Dis. 2019;79:116-22. [DOI:10.1016/j.ijid.2018.10.030]
18. Meyer T, Buder S. The Laboratory Diagnosis of Neisseria gonorrhoeae: Current Testing and Future Demands. Pathogens. 2020;9(2):91. [DOI:10.3390/pathogens9020091]
19. Soloaga RN, Carrion N, Pagano I, Oviedo C, Diez A, Pidone JC, et al. Neisseria gonorrhoeae identification: usefulness of the Vitek 2C NH card. Rev Argent Microbiol. 2013;45(1):54-6. [DOI:10.1016/S0325-7541(13)70004-X]
20. Cole MJ, Spiteri G, Jacobsson S, Woodford N, Tripodo F, Amato-Gauci AJ, et al. Overall low extended-spectrum cephalosporin resistance but high azithromycin resistance in Neisseria gonorrhoeae in 24 European countries, 2015. BMC Infect Dis. 2017;17:1-9. [DOI:10.1186/s12879-017-2707-z]
21. Ng LK, Martin IE. The Laboratory Diagnosis of Neisseria gonorrhoeae. Can J Infect Dis Med Microbiol. 2005;16(1):15-25. [DOI:10.1155/2005/323082]
22. 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(7):821-34. [DOI:10.1586/eri.09.63]
23. 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(3):256-63. [DOI:10.1177/0956462418799017]
24. Shigemura K, Okada H, Shirakawa T, Tanaka K, Arakawa S, Kinoshita S, et al. Susceptibilities of Neisseria gonorrhoeae to fluoroquinolones and other antimicrobial agents in Hyogo and Osaka, Japan. Sex Transm Infect. 2004;80(2):105-7. [DOI:10.1136/sti.2003.006908]
25. Apalata T, Zimba TF, Sturm WA, Moodley P. Antimicrobial susceptibility profile of Neisseria gonorrhoeae isolated from patients attending a STD facility in Maputo, Mozambique. Sex Transm Dis. 2009;36(6):341-3. [DOI:10.1097/OLQ.0b013e3181982e3c]
26. Berenger BM, Demczuk W, Gratrix J, Pabbaraju K, Smyczek P, Martin I. Genetic Characterization and Enhanced Surveillance of Ceftriaxone-Resistant Neisseria gonorrhoeae Strain, Alberta, Canada, 2018. Emerg Infect Dis. 2019;25(9):1660-7. [DOI:10.3201/eid2509.190407]
27. Gernert KM, Seby S, Schmerer MW, Thomas IV JC, Pham CD, Cyr SS, et al. Antimicrobial-Resistant Neisseria gonorrhoeae Working Group. Azithromycin susceptibility of Neisseria gonorrhoeae in the USA in 2017: a genomic analysis of surveillance data. Lancet Microbe. 2020;1(4):154-64. [DOI:10.1016/S2666-5247(20)30059-8]
28. Ochiai S, Sekiguchi S, Hayashi A, Shimadzu M, Ishiko H, Matsushima-Nishiwaki R, et al. Decreased affinity of mosaic-structure recombinant penicillin-binding protein 2 for oral cephalosporins in Neisseria gonorrhoeae. J Antimicrob Chemother. 2007;60(1):54-60. [DOI:10.1093/jac/dkm166]
29. Allan-Blitz LT, Adamson PC, Klausner JD. Resistance-Guided Therapy for Neisseria gonorrhoeae. Clin Infect Dis. 2022;75(9):1655-60. [DOI:10.1093/cid/ciac371]
30. Pinto M, Matias R, Rodrigues JC, Duarte S, Vieira L, Gonçalves I, et al. Cephalosporin-Resistant Neisseria gonorrhoeae Isolated in Portugal, 2019. Sex Transm Dis. 2020;47(11):e54-6. [DOI:10.1097/OLQ.0000000000001218]
31. Golparian D, Bazzo ML, Golfetto L, Gaspar PC, Schörner MA, Schwartz Benzaken A, et al. Genomic epidemiology of Neisseria gonorrhoeae elucidating the gonococcal antimicrobial resistance and lineages/sublineages across Brazil, 2015-16. J Antimicrob Chemother. 2020;75(11):3163-72. [DOI:10.1093/jac/dkaa318]
32. Chen SC, Yin YP, Dai XQ, Unemo M, Chen XS. Antimicrobial resistance, genetic resistance determinants for ceftriaxone and molecular epidemiology of Neisseria gonorrhoeae isolates in Nanjing, China. J Antimicrob Chemother. 2014;69(11):2959-65. [DOI:10.1093/jac/dku245]
33. Hagman KE, Shafer WM. Transcriptional control of the mtr efflux system of Neisseria gonorrhoeae. J Bacteriol. 1995;177(14):4162-5. [DOI:10.1128/jb.177.14.4162-4165.1995]
34. Xiu L, Yuan Q, Li Y, Zhang C, Tang L, Peng J. Emergence of ceftriaxone-resistant Neisseria gonorrhoeae strains harbouring a novel mosaic penA gene in China. J Antimicrob Chemother. 2020;75(4):907-10. [DOI:10.1093/jac/dkz530]
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