Skip to main content

Advertisement

Log in

Neisseria gonorrhoeae Antimicrobial Resistance: Past to Present to Future

  • Review Article
  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Neisseria gonorrhoeae (gonococcus) is a Gram-negative bacterium that causes gonorrhoea—a sexually transmitted disease. This gonococcus has progressively developed resistance to most of the available antimicrobials. Only a few countries around the world have been able to run extensive surveillance programmes on gonococcal infection and antimicrobial resistance, raising a global concern. Thus, this review focuses on the mechanisms of resistance to recommended antimicrobials in the past and present time. The approaches by the scientific community in the development of novel technologies such as whole-genome sequencing to predict antimicrobial resistance, track gonococcal transmission, as well as, introduce new therapeutics like Solithromycin, Zoliflodacin, and Gepotidacin were also discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. World Health Organization (2012) Department of Reproductive Health and Research. 2012. Global action plan to control the spread and impact of antimicrobial resistance in Neisseria gonorrhoeae. WHO, Geneva, p 4

    Google Scholar 

  2. World Health Organization (2012) Department of Reproductive Health and Research. Global incidence and prevalence of selected curable sexually transmitted infections—2008. WHO, Geneva, pp 1–3

    Google Scholar 

  3. Unemo M, Shafer WM (2014) Antimicrobial resistance in Neisseria gonorrhoeae in the 21st century: past, evolution, and future. Clin Microbiol Rev 27(3):587–613. https://doi.org/10.1128/CMR.00010-14

    Article  PubMed  PubMed Central  Google Scholar 

  4. Unemo M (2015) Current and future antimicrobial treatment of gonorrhea–the rapidly evolving Neisseria gonorrhoeae continues to challenge. BMC Infect Dis 15:364. https://doi.org/10.1186/s12879-015-1029-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Unemo M, Jensen JS (2017) Antimicrobial-resistant sexually transmitted infections: Gonorrhoea and Mycoplasma genitalium. Nat Rev Urol 14(3):139–152

    Article  Google Scholar 

  6. World Health Organization (2016) Guidelines for the treatment of Neisseria gonorrhoeae. WHO, Geneva, Switzerland, 2016. http://apps.who.int/iris/bitstream/10665/246114/1/9789241549691-eng.pdf

  7. Bharat A, Martin I, Demczuk W, Allen V, Haldene D, Hoang L, Mulvey MR (2016) Complete genome sequences of Neisseria gonorrhoeae with coresistance to first-line antimicrobial. Genome Announc 4(5):e00966-e1016. https://doi.org/10.1128/genomeA.00966-16

    Article  PubMed  PubMed Central  Google Scholar 

  8. Fifer H, Natarajan U, Jones L, Alexander S, Hughes G, Golparian D, Unemo M (2016) Failure of dual antimicrobial therapy in treatment of gonorrhea. N Engl J Med 374(25):2504–2506. https://doi.org/10.1056/NEJMc1512757

    Article  PubMed  Google Scholar 

  9. Dillon J-AR, Parti RP, Thakur SD (2015) Antibiotic resistance in Neisseria gonorrhoeae: will infections be untreatable in the future? Culture 35:1–8

    Google Scholar 

  10. Unemo M, Golparian D, Nicholas R, Ohnishi M, Gallay A, Sednaoui P (2012) 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 56(3):1273–1280

    Article  CAS  Google Scholar 

  11. Cristillo AD, Bristow CC, Torrone E, Dillon JA, Kirkcaldy RD, Dong H, Grad YH, Nicholas RA, Rice PA, Lawrence K, Oldach D, Shafer WM, Zhou P, Wi TE, Morris SR, Klausner JD (2019) Antimicrobial resistance in Neisseria gonorrhoeae: proceedings of the STAR sexually transmitted infection-clinical trial group programmatic meeting. Sex Transm Dis 46(3):e18–e25. https://doi.org/10.1097/OLQ.0000000000000929

    Article  PubMed  Google Scholar 

  12. Kersh EN, Pham CD, Papp JR, Myers R, Steece R, Kubin G, Weinstock H (2020) Expanding U.S. laboratory capacity for Neisseria gonorrhoeae antimicrobial susceptibility testing and whole-genome sequencing through the CDC’s antibiotic resistance laboratory network. J Clin Microb. https://doi.org/10.1128/JCM.01461-19

    Article  Google Scholar 

  13. Alfsnes K, Eldholm V, Olsen AO, Brynildsrud OB, Bohlin J, Steinbakk M, Caugant DA (2020) Genomic epidemiology and population structure of Neisseria gonorrhoeae in Norway, 2016–2017. Microb Genomics 6(4):e000359. https://doi.org/10.1099/mgen.0.000359

    Article  Google Scholar 

  14. Centre for Disease Prevention and Control (CDC) (2014) Sexually transmitted disease surveillance, national profile. https://www.cdc.gov/std/stats14/gonorrhea.htm. Accessed 1 June 2017

  15. Grad YH, Kirkcaldy RD, Trees D, Dordel J, Harris SR, Goldstein E, Hanage WP, Bentley S, Lipsitch M (2014) Genomic epidemiology of Neisseria gonorrhoeae with reduced susceptibility to cefixime in the USA: a retrospective observational study. Lancet Infect Dis 14(3):220–226

    Article  Google Scholar 

  16. European Centre for Disease Prevention and Control (ECDC) (2016) Gonococcal antimicrobial susceptibility surveillance in Europe 2014. Stockholm, Sweden. http://ecdc.europa.eu/en/publications/Publications/gonococcal-antimicrobialsusceptibility-surveillance-Europe-2014.pdf. Accessed 2 June 2017

  17. The European Committee on Antimicrobial Susceptibility Testing (EUCAST) (2017) Breakpoint tables for interpretation of MICs and zone diameters. Version 7.0. http://www.eucast.org/clinicalbreakpoints/. Accessed 2 June 2017

  18. Clinical and Laboratory Standards Institute (CLSI) (2017) Performance standards for antimicrobial susceptibility testing. Twenty-seventh informational supplement M100-S27. Wayne

  19. Unemo M, Ison CA, Cole M, Spiteri G, Van de Laar M, Khotenashvili L (2013) Gonorrhea and gonococcal antimicrobial resistance surveillance networks in the WHO European Region, including the independent countries of the former Soviet Union. Sex Transm Infect 89:iv42–iv46. https://doi.org/10.1136/sextrans-2012-050909

    Article  PubMed  Google Scholar 

  20. Unemo M, Lahra MM, Cole M, Galarza P, Ndowa F, Martin I, Wi T (2019) World Health Organization Global Gonococcal Antimicrobial Surveillance Program (WHO GASP): review of new data and evidence to inform international collaborative actions and research efforts. Sex Health 16(5):412–425. https://doi.org/10.1071/SH19023

    Article  PubMed  PubMed Central  Google Scholar 

  21. Lahra MM, Enriquez RP (2017) National Neisseria Network Australian Gonococcal Surveillance. Programme annual report, 2015. Commun Dis Intell Q Rep 41(1):E

    PubMed  Google Scholar 

  22. Lahra MM (2012) WHO Western Pacific and South East Asian Gonococcal Antimicrobial Surveillance Programme. Surveillance of antibiotic resistance in Neisseria gonorrhoeae in the WHO Western Pacific and South East Asian Regions, 2010. Commun Dis Intell Q Rep 36(1):95–100

    PubMed  Google Scholar 

  23. Lahra MM, Martin I, Demczuk W, Jennison AV, Lee KI, Nakayama SI et al (2018) Cooperative recognition of internationally disseminated ceftriaxone-resistant Neisseria gonorrhoeae strain. Emerg Infect Dis 24(4):735

    Article  CAS  Google Scholar 

  24. World Health Organization (2012) Baseline report on global sexually transmitted infection surveillance. http://www.who.int/reproductivehealth/publications/rtis/9789241505895/en/. Accessed 2 June 2017

  25. Ndowa FJ, Francis JM, Machiha A, Faye-Kette H, Fonkoua MC (2013) Gonococcal antimicrobial resistance: perspectives from the African region. Sex Transm Infect 89(suppl 4):iv11–iv15

    Article  Google Scholar 

  26. Maduna LD, Kock MM, van der Veer BM, Radebe O, McIntyre J, van Alphen LB, Peters RP (2020) Antimicrobial resistance of Neisseria gonorrhoeae isolates from high risk men in Johannesburg, South Africa. Antimicrobial Agents Chemother. https://doi.org/10.1128/AAC.00906-20

    Article  Google Scholar 

  27. World Health Organization (2017) Global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics. WHO, Geneva. Available online at: https://www.who.int/medicines/publications/WHO-PPL-Short_Summary_25Feb-ET_NM_WHO.pdf. [verified 18 May 2019]

  28. Ashford WA, Golash RG, Henning VG (1976) Penicillinase producing Neisseria gonorrhoeae. Lancet 2(7987):657–658

    Article  CAS  Google Scholar 

  29. Phillips I (1976) Beta-lactamase producing penicillin-resistant gonococcus. Lancet 2(7987):656–657

    Article  CAS  Google Scholar 

  30. Morse SA, Johnson SR, Biddle JW, Roberts MC (1986) High-level tetracycline resistance in Neisseria gonorrhoeae is result of acquisition of streptococcal tetM determinant. Antimicrob Agents Chemother 30:664–670. https://doi.org/10.1128/AAC.30.5.664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Douthwaite S, Champney WS (2001) Structures of ketolides and mac rolides determine their mode of interaction with the ribosomal target site. J Antimicrob Chemother 48(Suppl T1):1–8. https://doi.org/10.1093/jac/48.suppl_2.1

    Article  CAS  PubMed  Google Scholar 

  32. Lewis DA (2010) The gonococcus fights back: is this time a knock out? Sex Transm Infect 86(6):415–421. https://doi.org/10.1136/sti.2010.042648

    Article  PubMed  Google Scholar 

  33. Aminov RI (2010) A brief history of the antibiotic era: lessons learned and challenges for the future. Front Microbiol 1:134. https://doi.org/10.3389/fmicb.2010.00134

    Article  PubMed  PubMed Central  Google Scholar 

  34. Davenport D (2012) The war against bacteria: how were sulphonamide drugs used by Britain during World War II? Med Hum 38:55–58. https://doi.org/10.1136/medhum-2011-010024

    Article  Google Scholar 

  35. Unemo M, Shafer WM (2011) Antibiotic resistance in Neisseria gonorrhoeae: origin, evolution, and lessons learned for the future. Ann N Y Acad Sci 1230:E19–E28. https://doi.org/10.1111/j.1749-6632.2011.06215.x

    Article  PubMed  PubMed Central  Google Scholar 

  36. Dillon J-AR, Trecker MA, Thakur SD (2013) Gonococcal Antimicrobial Surveillance Program Network in Latin America and the Caribbean 1990–2011. 2013. Two decades of the gonococcal antimicrobial surveillance program in South America and the Caribbean: challenges and opportunities. Sex Transm Infect 89(Suppl 4):436–441. https://doi.org/10.1136/sextrans-2012-050905

    Article  Google Scholar 

  37. Zheng H, Wu X, Huang J, Qin X, Xue Y, Zeng W, Lan Y, Ou J, Tang S, Fang M (2015) The prevalence and epidemiology of plasmid-mediated penicillin and tetracycline resistance among Neisseria gonorrhoeae isolates in Guangzhou, China, 2002–2012. BMC Infect Dis 15:412. https://doi.org/10.1186/s12879-015-1148-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Easmon CS, Forster GE, Walker GD, Ison CA, Harris JR (1984) Spectinomycin as initial treatment for gonorrhea. Munday PEBr Med J (Clin Res Ed) 289(6451):1032–1034

    Article  CAS  Google Scholar 

  39. Moran JS (1995) Treating uncomplicated Neisseria gonorrhoeae infections: is the anatomic site of infection important? Sex Transm Dis 22:39–47

    Article  CAS  Google Scholar 

  40. Cole M, Unemo M, Hoffmann S, Chisholm SA, Ison CA, Van de Laar MJ (2011) The European gonococcal antimicrobial surveillance programme, 2009. Euro Surveill 16(42):19995

    PubMed  Google Scholar 

  41. Unemo M, Daniel G, Vegard S, Anne OO, Harald M, Gaute S, Stig OH (2013) Neisseria gonorrhoeae strain with high-level resistance to spectinomycin due to a novel resistance mechanism (mutated ribosomal protein S5) verified in Norway. Antimicrob Agents Chemother 57(2):1057–1061. https://doi.org/10.1128/AAC.01775-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Boslego JW, Tramont EC, Takafuji ET, Diniega BM, Mitchell BS, Small JW, Khan WN, Stein DC (1987) Effect of spectinomycin use on the prevalence of spectinomycin-resistant and penicillinase-producing Neisseria gonorrhoeae. N Engl J Med 317:272–278. https://doi.org/10.1056/NEJM198707303170504

    Article  PubMed  Google Scholar 

  43. World Health Organization (1993) Sexually transmitted diseases treatment guidelines. Centers for Disease Control and Prevention. MMWR recommendations and reports: morbidity and mortality weekly report recommendations and reports. 42(Rr-14):1–102

  44. Anderson JE, Hobbs MM, Biswas GD, Sparling PF (2003) Opposing selective forces for expression of the gonococcal lactoferrin receptor. Mol Microbiol 48(5):1325–1337

    Article  CAS  Google Scholar 

  45. Gransden WR, Warren CA, Phillips I, Hodges M, Barlow D (1990) Decreased susceptibility of Neisseria gonorrhoeae to ciprofloxacin. Lancet 335:51

    Article  CAS  Google Scholar 

  46. Belland RJ, Morrison SG, Ison C, Huang WM (1994) Neisseria gonorrhoeae acquires mutations in analogous regions of gyrA and parC in fluoroquinolone-resistant isolates. Mol Microbiol 14:371e80

    Article  Google Scholar 

  47. Philippe RS, Lagace-Wiens PR, Sarah D, Joshua K, Alexander T, Juma S, Scott M, Eduard J-S, George Z, Nicholas M, Supriya DM (2012) Emergence of fluoroquinolone resistance in Neisseria gonorrhoeae isolates from four clinics in three regions of Kenya. Sex Transm Dis 39(5):332–334. https://doi.org/10.1097/OLQ.0b013e318248a85f

    Article  CAS  Google Scholar 

  48. Duncan S, Thiong’o AN, Macharia M, Mwarumba S, Mvera B, Smith AD, Morpeth S, Graham SM, Sanders EJ (2011) High prevalence of quinolone resistance in Neisseria gonorrhoeae in coastal Kenya. Sex Transm Infect 87(3):231

    Article  Google Scholar 

  49. Centers for Disease Control (2002) Increases in fluoroquinolone-resistant Neisseria gonorrhoeae—Hawaii and California, 2001. MMWR 51(46):1041–1044

    Google Scholar 

  50. Sethi S, Zaman K, Jain N (2017) Mycoplasma genitalium infections: current treatment options and resistance issues. Infect Drug Resist 10:283–292. https://doi.org/10.2147/IDR.S105469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Ng LK, Martin I, Liu,GG Bryden L (2002) Mutation in 23S rRNA associated with macrolide resistance in Neisseiria gonorrhoeae. Antimicrob Agents Chemother 46:3020–3025. https://doi.org/10.1128/AAC.46.9.3020-3025.2002

    Article  CAS  Google Scholar 

  52. Chisholm SA, Dave J, Ison CA (2010) High-level azithromycin resistance occurs in Neisseria gonorrhoeae as a result of a single point mutation in the 23S rRNA genes. Antimicrob Agents Chemother 54(9):3812–3816. https://doi.org/10.1128/AAC.00309-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Akasaka S, Muratani T, Yamada Y, Inatomi H, Takahashi K, Matsumoto T (2001) Emergence of cephem- and aztreonam-high-resistant Neisseria gonorrhoeae that does not produce beta-lactamase. J Infect Chemother 7(1):49–50. https://doi.org/10.1007/s101560170034

    Article  CAS  PubMed  Google Scholar 

  54. Deguchi T, Yasuda M, Yokoi S, Ishida K, Ito M, Ishihara S, Minamidate K, Harada Y, Tei K, Kojima K, Tamaki M, Maeda S (2003) Treatment of uncomplicated gonococcal urethritis by double dosing of 200 mg cefixime at a 6-h interval. J Infect Chemother 9(1):35–39

    Article  CAS  Google Scholar 

  55. Ito M, Yasuda M, Yokoi S, Satoshi I, Shin-ichi M, Takashi D (2004) Remarkable increase in central Japan in 2001–2002 of Neisseria gonorrhoeae isolates with decreased susceptibility to penicillin, tetracycline, oral cephalosporins, and fluoroquinolones. Antimicrob Agents Chemother 48:3185–3187

    Article  CAS  Google Scholar 

  56. Shimuta K, Watanabe Y, Nakayama S-I, Morita-Ishihara T, Kuroki T, Unemo M, Ohnishi M (2015) Emergence and evolution of internationally disseminated cephalosporin-resistant Neisseria gonorrhoeae clones from 1995 to 2005 in Japan. BMC Infect Dis 15:378

    Article  Google Scholar 

  57. Yokoi S, Deguchi T, Ozawa T, Yasuda M, Ito S, Kubota Y, Tamaki M, Maeda S (2007) Threat to cefixime treatment for gonorrhea. Emerg Infect Dis 13(8):1275–1277

    PubMed  PubMed Central  Google Scholar 

  58. Japanese Society of Sexually Transmitted Infection (2011) Gonococcal infection. Sexually transmitted infections, diagnosis and treatment guidelines 2011. Jpn J Sex Transm Dis 22(suppl 1):52–59

    Google Scholar 

  59. Ohnishi M, Golparian D, Shimuta K, Saika T, Hoshina S, Iwasaku K, Nakayama S, Kitawaki J, Unemo M (2011) Is Neisseria gonorrhoeae initiating a future era of untreatable gonorrhea? Detailed characterization of the first strain with high-level resistance to ceftriaxone. Antimicrob Agents Chemother 55(7):3538–3545

    Article  CAS  Google Scholar 

  60. Cámara J, Serra J, Ayats J, Bastida T, Carnicer-Pont D, Andreu A, Ardanuy C (2012) Molecular characterization of two high-level ceftriaxone-resistant Neisseria gonorrhoeae isolates detected in Catalonia, Spain. J Antimicrob Chemother 67(8):1858–1860. https://doi.org/10.1093/jac/dks162

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  62. Public Health Agency of Canada. Canadian Guidelines on Sexually Transmitted Infections. Available online: https://www.canada.ca/en/public-health/services/infectious-diseases/sexual-health-sexually-transmittedinfections/canadian-guidelines/sexually-transmitted-infections/canadian-guidelines-sexually-transmittedinfections-34.html. Accessed 22 Apr 2018

  63. Ndowa F, Lusti-Narasimhan M, Unemo M (2012) The serious threat of multidrug-resistant and untreatable gonorrhea: the pressing need for global action to control the spread of antimicrobial resistance, and mitigate the impact on sexual and reproductive health. Sex Transm Infect 88(5):317–318. https://doi.org/10.1136/sextrans-2012-050674

    Article  PubMed  Google Scholar 

  64. Public Health England (2018) UK case of Neisseria gonorrhoeae with high-level resistance to azithromycin and resistance to ceftriaxone acquired abroad; Health Protection Report; Public Health England, London, UK, volume 12

  65. Abraham AJ, Trees DL (2020) Genomic sequencing of Neisseria gonorrhoeae to respond to the urgent threat of antimicrobial-resistant gonorrhea. Pathog Dis. https://doi.org/10.1093/femspd/ftx041

    Article  Google Scholar 

  66. Singh R, Dillon JR, Demczuk W, Kusalik A (2019) Gen2Epi: an automated whole-genome sequencing pipeline for linking full genomes to antimicrobial susceptibility and molecular epidemiological data in Neisseria gonorrhoeae. BMC Genomics 20:165. https://doi.org/10.1186/s12864-019-5542-3

    Article  PubMed  PubMed Central  Google Scholar 

  67. Unemo M, Golparian D, Sánchez-Buso L, Grad Y, Jacobsson S, Ohnishi M (2016) The novel 2016 WHO Neisseria gonorrhoeae reference strains for globalquality assurance of laboratory investigations: phenotypic, genetic andreference genome characterization. J Antimicrob Chemother 71:3096–3108

    Article  CAS  Google Scholar 

  68. Harris RS, Cole MJ, Spiteri G, Sánchez-Busó L, Golparian D, Jacobsson S, Goater R, Abudahab K, Yeats CA, Bercot B, Borrego MJ, Crowley B, Stefanelli P, Tripodo F, Abad R, Aanensen DM, Unemo M (2018) Public health surveillance of multidrug-resistant clones of Neisseria gonorrhoeae in Europe: a genomic survey. Lancet Infect Dis 18:758–768. https://doi.org/10.1016/S1473-3099(18)30225-1

    Article  PubMed  PubMed Central  Google Scholar 

  69. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477

    Article  CAS  Google Scholar 

  70. Kwong JC, Chow EPF, Stevens K, Stinear TP, Seemann T, Fairley CK, Chen MY, Howden BP (2018) Whole-genome sequencing reveals transmission of gonococcal antibiotic resistance among men who have sex with men: an observational study. Sex Transm Infect 94:151–157. https://doi.org/10.1136/sextrans-2017-053287

    Article  PubMed  Google Scholar 

  71. Mortimera TD, Grada YH (2020) Applications of genomics to slow the spread of MDR Neisseria gonorrhoeae. Ann N Y Acad Sci 1435(1):93–109. https://doi.org/10.1111/nyas.13871

    Article  Google Scholar 

  72. Abrams AJ, Trees DL, Nicholas RA (2015) Complete genome sequences of three Neisseria gonorrhoeae laboratory reference strains, determined using PacBio singlemolecule real-time technology. Genome Announc 3(5):e01052-e1115. https://doi.org/10.1128/genomeA.01052-15

    Article  PubMed  PubMed Central  Google Scholar 

  73. Ozer EA, Prister LL, Yin S, Ward BH, Ivanov S, Seifert HS (2019) PacBio amplicon sequencing method to measure pilin antigenic variation frequencies of Neisseria gonorrhoeae. mSphere 4:e00562-19. https://doi.org/10.1128/mSphere.00562-19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Page AJ, De Silva N, Hunt M, Quail MA, Parkhill J, Harris SR (2016) Robust high-throughput prokaryote de novo assembly and improvement pipeline for Illumina data. Microb Genomics 2(8):e000083

    Article  Google Scholar 

  75. Jain M, Tyson JR, Loose M, Ip CL, Eccles DA, O’GradyJ, Malla S, Leggett RM, Wallerman O, Jansen HJ, Zalunin V (2017) MinION Analysis and Reference Consortium: phase 2 data release and analysis of R9.0 chemistry. F1000Research 6:760

    Article  Google Scholar 

  76. Goodwin S, Gurtowski J, Ethe-Sayers S, Deshpande P, Schatz MC, McCombie WR (2015) Oxford nanopore sequencing, hybrid error correction, and de novo assembly of a eukaryotic genome. Genome Res 25(11):1750–1756

    Article  CAS  Google Scholar 

  77. Baxter J (2019) Evaluation of Oxford nanopore’s MinION: use, functionality, and genome assembly, 1–23

  78. Zhang C, Wang F, Zhu C, Xiu L, Li Y, Li L, Liu B, Li Y, Zeng Y, Guo B, Peng J (2020) Determining antimicrobial resistance profiles and identifying novel mutations of Neisseria gonorrhoeae genomes obtained by multiplexed MinION sequencing. Sci China Life Sci 63(7):1063–1070

    Article  CAS  Google Scholar 

  79. Golparian D, Donà V, Sánchez-Busó L, Foerster S, Harris S, Endimiani A, Low N, Unemo M (2018) Antimicrobial resistance prediction and phylogenetic analysis of Neisseria gonorrhoeae isolates using the Oxford Nanopore MinION sequencer. Sci Rep 8(1):1–12

    Article  CAS  Google Scholar 

  80. Beatriz Suay-García ID, María Teresa TP (2018) Future prospect for Neisseria gonorrhoeae treatment. Antibiotics (Basel) 7(2):49. https://doi.org/10.3390/antibiotics7020049

    Article  CAS  Google Scholar 

  81. Alirol E, Wi TE, Bala M, Bazzo ML, Chen XS, Deal C, Dillon J-AR, Kularatne R, Heim J, Hooft van Huijsduijnen R, Hook EW, Lahra MM, Lewis DA, Ndowa F, Shafer WM, Tayler L, Workowski K, Unemo M, Balasegaram M (2017) Multidrug-resistant gonorrhea: a research and development roadmap to discover new medicines. PLoS Med 14(7):e1002366. https://doi.org/10.1371/journal.pmed.1002366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Golparian D, Fernandes P, Ohnishi M, Jensen JS, Unemo M (2012) In vitro activity of the new fluoroketolide solithromycin (CEM-101) against a large collection of clinical Neisseria gonorrhoeae isolates and international reference strains, including those with high-level antimicrobial resistance: potential treatment option for gonorrhea? Antimicrob Agents Chemother 56(5):2739–2742. https://doi.org/10.1128/AAC.00036-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Hook EW 3rd, Golden M, Jamieson BD, Dixon PB, Harbison HS, Lowens S, Fernandes PA (2015) Phase 2 trial of oral solithromycin 1200 mg or 1000 mg as single-dose oral therapy for uncomplicated gonorrhea. Clin Infect Dis 61(7):1043–1048. https://doi.org/10.1093/cid/civ478

    Article  PubMed  Google Scholar 

  84. Oldach D (2017) Results of the SOLITAIRE-U Phase 3 trial: solithromycin vs. ceftriaxone + azithromycin for treatment of uncomplicated urogenital gonorrhea. Chapel Hill: Cempra, Inc. Available online at: https://starstictg.s-3.net/sites/default/files/page_files/12.%20Results%20of%20the%20SOLITAIRE-U%20Phase%203%20Trial_Solithromycin_Oldach_4.13.2017.pptx. [verified 18 May 2019]

  85. O’Donnell J, Lawrence K, Vishwanathan K, Hosagrahara V, Mueller JP (2018) Single-dose pharmacokinetics, excretion, and metabolism of zoliflodacin, a novel spiropyrimidinetrione antibiotic, in healthy volunteers. Antimicrob Agents Chemother 63(1):e01808-e1818

    Article  Google Scholar 

  86. Basarab GS, Kern GH, McNulty J, Mueller JP, Lawrence K, Vishwanathan K, Alm RA, Barvian K, Doig P, Galullo V, Gardner H, Gowravaram M, Huband M, Kimzey A, Morningstar M, Kutschke A, Lahiri SD, Perros M, Singh R, Schuck VJ, Tommasi R, Walkup G, Newman JV (2015) Responding to the challenge of untreatable gonorrhea: ETX0914, a first-in-class agent with a distinct mechanism-of-action against bacterial Type II topoisomerases. Sci Rep 5:11827. https://doi.org/10.1038/srep11827

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Farrell DJ, Sader HS, Rhomberg PR, Scangarella-Oman NE, Flamm RK (2017) In vitro activity of gepotidacin (GSK2140944) against Neisseria gonorrhoeae. Antimicrob Agents Chemother 61(3):e02047-e2116. https://doi.org/10.1128/AAC.02047-16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Taylor SN, Morris DH, Avery AK, Workowski KA, Batteiger BE, Tiffany CA, Perry CR, Raychaudhuri A, Scangarella-Oman NE, Hossain M, Dumont EF (2018) Gepotidacin for the treatment of uncomplicated urogenital gonorrhea: a phase 2, randomized, dose-ranging single-oral dose evaluation. Clin Infect Dis 67(4):504–512. https://doi.org/10.1093/cid/ciy145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Górski A, Międzybrodzki R, Jończyk-Matysiak E, Borysowski J, Letkiewicz S, Weber-Dąbrowska B (2019) The fall and rise of phage therapy in modern medicine. Expert Opin Biol Ther 19:1115–1117

    Article  Google Scholar 

  90. Kim BO, Kim ES, Yoo YJ, Bae HW, Chung IY, Cho YH (2019) Phage-derived antibacterials: harnessing the simplicity, plasticity, and diversity of phages. Viruses 11(3):268

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Georgina L. Aitolo.

Ethics declarations

Conflict of interest

None declared.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Aitolo, G.L., Adeyemi, O.S., Afolabi, B.L. et al. Neisseria gonorrhoeae Antimicrobial Resistance: Past to Present to Future. Curr Microbiol 78, 867–878 (2021). https://doi.org/10.1007/s00284-021-02353-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-021-02353-8

Navigation