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Antimicrobial resistance (AMR) and molecular characterization of Neisseria gonorrhoeae in Ghana, 2012-2015


Autoři: Naiki Attram aff001;  Bright Agbodzi aff001;  Helena Dela aff001;  Eric Behene aff001;  Edward O. Nyarko aff003;  Nicholas N. A. Kyei aff003;  John A. Larbi aff004;  Bernard W. L. Lawson aff004;  Kennedy K. Addo aff002;  Mercy J. Newman aff005;  Christopher A. Duplessis aff001;  Nehkonti Adams aff001;  Magnus Unemo aff006;  Andrew G. Letizia aff001
Působiště autorů: US Naval Medical Research Unit Number Three, Ghana Laboratory, Legon, Ghana aff001;  Noguchi Memorial Institute for Medical Research, University of Ghana, Legon, Ghana aff002;  Department of Public Health, Military Hospital, Accra, Ghana aff003;  Department of Theoretical and Applied Biology, Kwame Nkrumah University of Science and Technology, Kumasi, Ghana aff004;  Department of Medical Microbiology, School of Biomedical and Allied Health Science, College of Health Sciences, University of Ghana, Accra, Ghana aff005;  WHO Collaborating Centre for Gonorrhoea and other STIs, National Reference Laboratory for STIs, Department of Laboratory Medicine, Faculty of Medicine and Health, Örebro University, Örebro, Sweden aff006
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0223598

Souhrn

Neisseria gonorrhoeae antimicrobial resistance (AMR) surveillance is essential for tracking the emergence and spread of AMR strains in local, national and international populations. This is crucial for developing or refining treatment guidelines. N. gonorrhoeae multiantigen sequence typing (NG-MAST) is beneficial for describing the molecular epidemiology of gonococci at national and international levels. Elucidation of AMR determinants to β-lactam drugs, is a means of monitoring the development of resistance. In Ghana, little is known about the current gonococcal AMR prevalence and no characterization of gonococcal isolates has been previously performed. In this study, gonococcal isolates (n = 44) collected from five health facilities in Ghana from 2012 to 2015, were examined using AMR testing, NG-MAST and sequencing of penA. High rates of resistance were identified to tetracycline (100%), benzylpenicillin (90.9%), and ciprofloxacin (81.8%). One isolate had a high cefixime MIC (0.75 μg/ml). Twenty-eight NG-MAST sequence types (STs) were identified, seventeen of which were novel. The isolate with the high cefixime MIC contained a mosaic penA-34 allele and belonged to NG-MAST ST1407, an internationally spreading multidrug-resistant clone that has accounted for most cefixime resistance in many countries. In conclusion, AMR testing, NG-MAST, and sequencing of the AMR determinant penA, revealed high rates of resistance to tetracycline, benzylpenicillin, and ciprofloxacin; as well as a highly diverse population of N. gonorrhoeae in Ghana. It is imperative to continue with enhanced AMR surveillance and to understand the molecular epidemiology of gonococcal strains circulating in Ghana and other African countries.

Klíčová slova:

Antimicrobial resistance – Bacterial disk diffusion – Ghana – Penicillin – Sequence alignment – Tetracyclines – Etest


Zdroje

1. World Health Organisation. Global action plan to control the spread and impact of antimicrobial resistance in Neisseria gonorrhoeae. Geneva, Switzerland: Department of Reproductive Health and Research, WHO, 2012.

2. World Health Organization. Report on global sexually transmitted infection surveillance 2015. Geneva, Switzerland: 2016.

3. Tapsall JW, Ndowa F, Lewis DA, Unemo M. Meeting the public health challenge of multidrug-and extensively drug-resistant Neisseria gonorrhoeae. Exp Rev Anti-Infect Ther. 2009;7(7):821–834.

4. World Health Organisation. WHO guidelines for the treatment of Neisseria gonorrhoeae. World Health Organization., 2016. 9241549696.

5. Wi T, Lahra MM, Ndowa F, Bala M, Dillon JR, Ramon-Pardo P, et al. Antimicrobial resistance in Neisseria gonorrhoeae: Global surveillance and a call for international collaborative action. PLoS Med. 2017;14(7):1–16.

6. Newman MJ, Frimpong E, Donkor ES, Opintan JA, Asamoah-Adu A. Resistance to antimicrobial drugs in Ghana. Infect Drug Res. 2011;4:215–220.

7. Ndowa FJ, Francis JM, Machiha A, Faye-Kette H, Fonkoua MC. Gonococcal antimicrobial resistance: perspectives from the African region. Sex Trans Infect. 2013;89 (Suppl 4):iv11–iv5.

8. Ministry of Health Ghana National Drugs Programme (GNDP). Standard Treatment Guidelines (STG) and Essential Medicines List 7th ed. Ghana: Ministry of Health; 2017. p. 442–447.

9. Duplessis C, Puplampu N, Nyarko E, Carroll JNA, Dela H, Mensah A, et al. Gonorrhea surveillance in Ghana, Africa. Mil Med. 2015;180(1):17–22 doi: 10.7205/MILMED-D-13-00418 25562852

10. Martin IMC, Ison CA, Aanensen DM, Fenton KA, Spratt BG. Rapid sequence-based identification of gonococcal transmission clusters in a large metropolitan area. Jour Infect Dis. 2004;189(8):1497–1505.

11. Singh AE, Gratrix J, Read R, Lovgren M, Drews SJ, Romanowski B, et al. Neisseria gonorrhoeae multiantigen sequence typing is beneficial in further characterizing gonococcal populations in Alberta, Canada. Sex Trans Dis. 2013;40 (9):745–750.

12. Kubanova A, Kubanov A, Frigo N, Solomka V, Semina V, Vorobyev D, et al. Russian gonococcal antimicrobial susceptibility programme (RU-GASP)–resistance in Neisseria gonorrhoeae during 2009–2012 and NG-MAST genotypes in 2011 and 2012. Infect Dis. 2014;14(342).1–7

13. Unemo M, Dillon JR. Mitigating the emergence and spread of multidrug-and extensively drug-resistant gonorrhea: is there sufficient support in resource-poor settings in Africa? Sex Trans Dis. 2014;41(4):238–239.

14. Tomberg J, Unemo M, Ohnishi M, Davies C, Nicholas RA. Identification of amino acids conferring high-level resistance to expanded-spectrum cephalosporins in the penA gene from Neisseria gonorrhoeae Strain H041. Antim Agents Chemother. 2013;57(7):3029–3036.

15. Tomberg J, Unemo M, Davies C, Nicholas RA. Molecular and structural analysis of mosaic variants of penicillin binding protein 2 conferring decreased susceptibility to expanded spectrum cephalosporins in Neisseria gonorrhoeae: role of epistatic mutations. Biochem. 2010;49 (37): 8062–8070.

16. Lindberg R, Fredlund H, Nicholas R, Unemo M. Neisseria gonorrhoeae Isolates with Reduced Susceptibility to Cefixime and Ceftriaxone: Association with Genetic Polymorphisms in penA, mtrR, porB1b, and ponA. Antimicrob Agents Chemother. 2007;51(6):2117–2122. doi: 10.1128/AAC.01604-06 17420216

17. Lee S, Lee H, Jeong SH, Yong D, Chung GT, Lee SY, et al. Various penA mutations together with mtrR, porB and ponA mutations in Neisseria gonorrhoeae isolates with reduced susceptibility to cefixime or ceftriaxone. J Antimicrob Chemother. 2010;65:669–675. doi: 10.1093/jac/dkp505 20093260

18. Duplessis C, Puplampu N, Nyarko E, Carroll JNA., Dela H, Mensah A, et al. Gonorrhoea surveillance in Ghana, Africa. Sex Trans Infect. 2013;89(7):594.

19. Clinical Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing. Twenty-Sixth Edition. Wayne, PA; CLSI. 2015.

20. Centers for Disease Control and Prevention. Neisseria gonorrhoeae reference strains for antimicrobial susceptibility testing. CDC; 2005.

21. Pandori M, Pennan M, Wu A, Ren A, Whittington WLH, Liska S et al. Mosaic Penicillin-Binding Protein 2 in Neisseria gonorrhoeae isolates collected in 2008 in San Francisco, California. Antimicrob Agents Chemother. 2009;53(9):4032–4034 doi: 10.1128/AAC.00406-09 19546370

22. Allen V, Farrell DJ, Rebbapragada A, Tan J, Tijet N, Perucini S J et al. Molecular Analysis of Antimicrobial Resistance Mechanisms in Neisseria gonorrhoeae Isolates from Ontario, Canada. Antimicrob Agents Chemother. 2011;55(2):703–712. doi: 10.1128/AAC.00788-10 21098249

23. Kück P, Longo GC. FASconCAT-G: extensive functions for multiple sequence alignment preparations concerning phylogenetic studies. Front Zool. 2014;11(1):81. doi: 10.1186/s12983-014-0081-x 25426157

24. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol. 2013;30:2725–2729. doi: 10.1093/molbev/mst197 24132122

25. Demczuk W, Sidhu S, Unemo M, Whiley DM, Allen VG, Dillon JR, et al. Neisseria gonorrhoeae sequence typing for antimicrobial resistance, a novel antimicrobial resistance multilocus typing scheme for tracking global dissemination of N. gonorrhoeae strains. J Clin Microbiol. 2017;55(5):1454–1468. doi: 10.1128/JCM.00100-17 28228492

26. Olsen B, Lan PT, Golparian D, Johansson E, Khang TH, Unemo M. Antimicrobial susceptibility and genetic characteristics of Neisseria gonorrhoeae isolates from Vietnam, 2011. BMC Infect Dis. 2013;13(40):1–8.

27. Chisholm SA, Unemo M, Quaye N, Johansson E, Cole MJ, Ison CA, et al. Molecular epidemiological typing within the European Gonococcal Antimicrobial Resistance Surveillance Programme reveals predominance of a multidrug-resistant clone. Euro Surveill. 2013;18(3):1–10.

28. Jabeen K, Mal PB, Khan E, Chandio S, Jacobsson S, Unemo M. Antimicrobial resistance and Neisseria gonorrhoeae multiantigen sequence typing (NG-MAST) genotypes in N. gonorrhoeae during 2012–2014 in Karachi, Pakistan. BMC Infect Dis. 2016;16(653):1–6.

29. Harris SR, Cole MJ, Spiteri G, Sanchez-Buso L, Golparian D, Jacobsson S, et al. Euro GASP study group. Public Health Surveillance of multidrug-resistance clones of Neisseria gonorrhoeae in Europe: a genomic survey. Lancet Infect Dis. 2018;18(7):758–768. doi: 10.1016/S1473-3099(18)30225-1 29776807

30. Lewis DA, Sriruttan C, Müller EE, Golparian D, Gumede L, Fick D, et al. Phenotypic and genetic characterization of the first two cases of extended-spectrum-cephalosporin-resistant Neisseria gonorrhoeae infection in South Africa and association with cefixime treatment failure. J Antimicrob Chemother. 2013;68(6):1267–1270. doi: 10.1093/jac/dkt034 23416957

31. Unemo M, Golparian D, Syversen G, Vestrhei DF, Moi H. Two cases of verified clinical failures using internationally recommended first-line cefixime for gonorrhoea treatment, Norway, 2010. Euro Surveill. 2010;15(47):1–3.

32. Unemo M, Golparian D, Nicholas RA, 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. 2011;0066-4804(12):1273–1280.

33. Shimuta K, Unemo M, Nakayama S, Morita-Ishihara T, Dorin M, Kawahat T, et al. Antimicrobial resistance and molecular typing of Neisseria gonorrhoeae isolates in Kyoto and Osaka, Japan, 2010–2012: intensified surveillance after identification of the first strain (H041) with high level ceftriaxone resistance. Antimicrob Agents Chemother. 2013;57(11):5225–5232. doi: 10.1128/AAC.01295-13 23939890

34. Shimuta K, Watanabe Y, Nakayama S, Morita-Ishihara T, Kuroki T, Unemo M, et al. Emergence and evolution of internationally disseminated cephalosporin-resistant Neisseria gonorrhoeae clones from 1995 to 2005 in Japan. BMC Infect Dis. 2015;15:378.1–11 doi: 10.1186/s12879-015-1110-x 26381611

35. Ito M, Deguchi T, Mizutani KS, Yasuda M, Yokoi S, Ito SI, et al. Emergence and spread of Neisseria gonorrhoeae clinical isolates harboring mosaic-like structure of penicillin-binding protein 2 in Central Japan. Antimicrob Agents Chemother. 2005;49(1):137–143. doi: 10.1128/AAC.49.1.137-143.2005 15616287

36. Whiley DM, Limnios EA, Ray S, Sloots TP, Tapsall JW. Diversity of penA alterations and subtypes in Neisseria gonorrhoeae strains from Sydney, Australia, that are less susceptible to ceftriaxone. Antimicrob Agents Chemother. 2007;51(9):3111–116 doi: 10.1128/AAC.00306-07 17591846

37. Dowson CG, Jephcott AE, Gough KR, Spratt BG. Penicillin binding protein 2 genes of non-beta-lactamase producing, penicillin resistant strains of Neisseria gonorrhoeae.Mol Biol. 1989. 1(8):35–42

38. Brannigan JA, Tirodimos IA, Zhang Q-Y, Dowson CG, Spratt BG. Insertion of an extra amino-acid is the main cause of the low affinity of penicillin-binding protein 2 in penicillin resistant strains of Neisseria gonorrhoeae. Mol Biol. 1990. 4(6):913–920.

39. 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 17540669

40. Whiley DM, Goire N, Lambert SB, Ray S, Limnios EA, Niessen MD, et al. Reduced susceptibility to ceftriaxone in Neisseria gonorrhoeae is associated with mutations G542S, P551S and P551L in the gonococcal penicillin-binding protein 2. J Antimicrob Chemother. 2010;65:1615–1618. doi: 10.1093/jac/dkq187 20511367

41. Liao C-H, Lai C-C, Hsu M-S, Chu F-Y, Wu M-Y, Huang Y-T, Hsueh P-R. Antimicrobial susceptibility of Neisseria gonorrhoeae isolates determined by the agar dilution, disc difussion and Etest methods:comparison of results using GC and chocolate agar. Int J Antimicrob Agents. 2010; 35: 457–460. doi: 10.1016/j.ijantimicag.2010.01.007 20188518

42. Lagace-Wiens PRS, Duncan S, Kimani J, Thiong’o A, Shafi J, McLelland S, et al. Emergence of fluoroquinolone resistance in Neisseria gonorrhoeae Isolates from four clinics in three regions of Kenya. Sex Trans Dis. 2012;39(5):332–334.

43. Vandepitte J, Hughes P, Matovu G, Bukenya J, Grosskurth H, Lewis DA. High prevalence of ciprofloxacin-resistant gonorrhea among female sex workers in Kampala, Uganda (2008–2009). Sex Trans Dis. 2014;41:233–237.


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