Multiplex real-time PCR assay with high-resolution melting analysis for characterization of antimicrobial resistance in neisseria gonorrhoeae

Journal of Clinical Microbiology

Volumn 54, Issue 8, 2016, Pages 2074-2081

  Donà, Valentina ^a   Kasraian, Sara ^a   Lupo, Agnese ^a   Guilarte, Yuvia N ^a   Hauser, Christoph ^a   Furrer, Hansjakob ^a   Unemo, Magnus ^b   Low, Nicola ^a   Endimiani, Andrea ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b ÖREBRO UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AZITHROMYCIN; CEFIXIME; CEFTRIAXONE; CIPROFLOXACIN; SPECTINOMYCIN;

ACCURACY; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL STRAIN; BACTERIUM CULTURE; BACTERIUM DETECTION; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATE; BIOASSAY; CONTROLLED STUDY; HIGH RESOLUTION MELTING ANALYSIS; LIMIT OF DETECTION; MULTIPLEX POLYMERASE CHAIN REACTION; NEISSERIA GONORRHOEAE; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SENSITIVITY AND SPECIFICITY; VALIDATION STUDY; GENETICS; GENOTYPING TECHNIQUE; HUMAN; MICROBIAL SENSITIVITY TEST; PROCEDURES; TRANSITION TEMPERATURE;

DRUG RESISTANCE, BACTERIAL; GENOTYPING TECHNIQUES; HUMANS; MICROBIAL SENSITIVITY TESTS; MULTIPLEX POLYMERASE CHAIN REACTION; NEISSERIA GONORRHOEAE; REAL-TIME POLYMERASE CHAIN REACTION; SENSITIVITY AND SPECIFICITY; TRANSITION TEMPERATURE;

EID: 84979622689     PISSN: 00951137     EISSN: 1098660X     Source Type: Journal    
DOI: 10.1128/JCM.03354-15     Document Type: Article

References (41)

1. Newman L, Rowley J, Vander Hoorn S, Wijesooriya NS, Unemo M, Low N, Stevens G, Gottlieb S, Kiarie J, Temmerman M. 2015. Global estimates of the prevalence and incidence of four curable sexually transmitted infections in 2012 based on systematic review and global reporting. PLoS One 10:e0143304. http://dx. doi. org/10. 1371/journal. pone. 0143304.
2. Unemo M, Shafer WM. 2011. Antibiotic resistance in Neisseria gonorrhoeae: origin, evolution, and lessons learned for the future. AnnNY Acad Sci 1230:E19-E28. http://dx. doi. org/10. 1111/j. 1749-6632. 2011. 06215. x.
3. World Health Organization. 2012. Global action plan to control the spread and impact of antimicrobial resistance in Neisseria gonorrhoeae. World Health Organization, Geneva, Switzerland.
4. Ohnishi M, Watanabe Y, Ono E, Takahashi C, Oya H, Kuroki T, Shimuta K, Okazaki N, Nakayama S, Watanabe H. 2010. Spread of a chromosomal cefixime-resistant penA gene among different Neisseria gonorrhoeae lineages. Antimicrob Agents Chemother 54:1060-1067. http: //dx. doi. org/10. 1128/AAC. 01010-09.
5. 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 56:1273-1280. http://dx. doi. org/10. 1128/AAC. 05760-11.
6. van Dam AP, van Ogtrop ML, Golparian D, Mehrtens J, de Vries HJ, Unemo M. 2014. Verified clinical failure with cefotaxime 1g for treatment of gonorrhoea in the Netherlands: a case report. Sex Transm Infect 90: 513-514. http://dx. doi. org/10. 1136/sextrans-2014-051552.
7. Unemo M, Golparian D, Potocnik M, Jeverica S. 2012. Treatment failure of pharyngeal gonorrhoea with internationally recommended first-line ceftriaxone verified in Slovenia, September 2011. Euro Surveill 17(25): pii-20200. http://www. eurosurveillance. org/ViewArticle. aspx?ArticleId-20200.
8. Unemo M, Golparian D, Stary A, Eigentler A. 2011. First Neisseria gonorrhoeae strain with resistance to cefixime causing gonorrhoea treatment failure in Austria, 2011. Euro Surveill 16(43):pii-19998. http: //www. eurosurveillance. org/ViewArticle. aspx?ArticleId-19998.
9. 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 54:3812-3816. http://dx . doi. org/10. 1128/AAC. 00309-10.
10. Ng LK, Martin I, Liu G, Bryden L. 2002. Mutation in 23S rRNA associated with macrolide resistance in Neisseria gonorrhoeae. Antimicrob Agents Chemother 46:3020-3025. http://dx. doi. org/10. 1128/AAC. 46. 9 . 3020-3025. 2002.
11. Shultz TR, Tapsall JW, White PA. 2001. Correlation of in vitro susceptibilities to newer quinolones of naturally occurring quinolone-resistant Neisseria gonorrhoeae strains with changes in GyrA and ParC. Antimicrob Agents Chemother 45:734-738. http://dx. doi. org/10. 1128/AAC. 45. 3. 734-738. 2001.
12. Sigmund CD, Ettayebi M, Morgan EA. 1984. Antibiotic resistance mutations in 16S and 23S ribosomal RNA genes of Escherichia coli. Nucleic Acids Res 12:4653-4663. http://dx. doi. org/10. 1093/nar/12. 11. 4653.
13. Ilina EN, Malakhova MV, Bodoev IN, Oparina NY, Filimonova AV, Govorun VM. 2013. Mutation in ribosomal protein S5 leads to spectinomycin resistance in Neisseria gonorrhoeae. Front Microbiol 4:186. http: //dx. doi. org/10. 3389/fmicb. 2013. 00186.
14. Endimiani A, Guilarte YN, Tinguely R, Hirzberger L, Selvini S, Lupo A, Hauser C, Furrer H. 2014. Characterization of Neisseria gonorrhoeae isolates detected in Switzerland (1998-2012): emergence of multidrugresistant clones less susceptible to cephalosporins. BMC Infect Dis 14:106. http://dx. doi. org/10. 1186/1471-2334-14-106.
15. Liew M, Pryor R, Palais R, Meadows C, Erali M, Lyon E, Wittwer C. 2004. Genotyping of single-nucleotide polymorphisms by high-resolution melting of small amplicons. Clin Chem 50:1156-1164. http://dx. doi. org /10. 1373/clinchem. 2004. 032136.
16. Whiley DM, Tapsall JW, Sloots TP. 2006. Nucleic acid amplification testing for Neisseria gonorrhoeae: an ongoing challenge. J Mol Diagn 8:3-15. http://dx. doi. org/10. 2353/jmoldx. 2006. 050045.
17. Low N, Unemo M, Skov Jensen J, Breuer J, Stephenson JM. 2014. Molecular diagnostics for gonorrhoea: implications for antimicrobial re-sistance and the threat of untreatable gonorrhoea. PLoSMed11:e1001598. http://dx. doi. org/10. 1371/journal. pmed. 1001598.
18. Gibson NJ. 2006. The use of real-time PCR methods in DNA sequence variation analysis. Clin Chim Acta 363:32-47. http://dx. doi. org/10. 1016/j . cccn. 2005. 06. 022.
19. Vossen RH, Aten E, Roos A, den Dunnen JT. 2009. High-resolution melting analysis (HRMA): more than just sequence variant screening. Hum Mutat 30:860-866. http://dx. doi. org/10. 1002/humu. 21019.
20. Seipp MT, Pattison D, Durtschi JD, Jama M, Voelkerding KV, Wittwer CT. 2008. Quadruplex genotyping of F5, F2, and MTHFR variants in a single closed tube by high-resolution amplicon melting. Clin Chem 54: 108-115.
21. Balashov S, Mordechai E, Adelson ME, Gygax SE. 2013. Multiplex bead suspension array for screening Neisseria gonorrhoeae antibiotic resistance genetic determinants in noncultured clinical samples. J Mol Diagn 15: 116-129. http://dx. doi. org/10. 1016/j. jmoldx. 2012. 08. 005.
22. Lawung R, Cherdtrakulkiat R, Charoenwatanachokchai A, Nabu S, Suksaluk W, Prachayasittikul V. 2009. One-step PCR for the identification of multiple antimicrobial resistance in Neisseria gonorrhoeae. J Microbiol Methods 77:323-325. http://dx. doi. org/10. 1016/j. mimet . 2009. 03. 009.
23. Magooa MP, Muller EE, Gumede L, Lewis DA. 2013. Determination of Neisseria gonorrhoeae susceptibility to ciprofloxacin in clinical specimens from men using a real-time PCR assay. Int J Antimicrob Agents 42:63-67. http://dx. doi. org/10. 1016/j. ijantimicag. 2013. 02. 026.
24. Zhao L, Zhao S. 2012. TaqMan real-time quantitative PCR assay for detection of fluoroquinolone-resistant Neisseria gonorrhoeae. Curr Microbiol 65:692-695. http://dx. doi. org/10. 1007/s00284-012-0212-6.
25. Siedner MJ, Pandori M, Castro L, Barry P, Whittington WL, Liska S, Klausner JD. 2007. Real-time PCR assay for detection of quinoloneresistant Neisseria gonorrhoeae in urine samples. J Clin Microbiol 45: 1250-1254. http://dx. doi. org/10. 1128/JCM. 01909-06.
26. Li Z, Yokoi S, Kawamura Y, Maeda S, Ezaki T, Deguchi T. 2002. Rapid detection of quinolone resistance-associated gyrA mutations in Neisseria gonorrhoeae with a LightCycler. J Infect Chemother 8:145-150. http://dx . doi. org/10. 1007/s101560200025.
27. Lindback E, Rahman M, Jalal S, Wretlind B. 2002. Mutations in gyrA, gyrB, parC, and parE in quinolone-resistant strains of Neisseria gonorrhoeae. APMIS 110:651-657. http://dx. doi. org/10. 1034/j. 1600-0463. 2002 . 1100909. x.
28. Buckley C, Trembizki E, Donovan B, Chen M, Freeman K, Guy R, Kundu R, Lahra MM, Regan DG, Smith H, Whiley DM, GRAND Study Investigators. 2016. A real-time PCR assay for direct characterization of the Neisseria gonorrhoeae GyrA 91 locus associated with ciprofloxacin susceptibility. J Antimicrob Chemother 71:353-356. http://dx. doi. org/10 . 1093/jac/dkv366.
29. Unemo M, Fasth O, Fredlund H, Limnios A, Tapsall J. 2009. Phenotypic and genetic characterization of the 2008 WHO Neisseria gonorrhoeae reference strain panel intended for global quality assurance and quality control of gonococcal antimicrobial resistance surveillance for public health purposes. J Antimicrob Chemother 63:1142-1151. http://dx. doi. org/10 . 1093/jac/dkp098.
30. Clinical and Laboratory Standards Institute. 2015. Performance standards for antimicrobial susceptibility testing; twenty-fifth informational supplement. CLSI document M100-S25. CLSI, Wayne, P.A.
31. EUCAST. 2015. Breakpoint tables for interpretation of MICs and zone diameters, version 5. 0. http://www. eucast. org/.
32. Lahra MM, Ryder N, Whiley DM. 2014. A new multidrug-resistant strain of Neisseria gonorrhoeae in Australia. N Engl J Med 371:1850-1851. http: //dx. doi. org/10. 1056/NEJMc1408109.
33. Golparian D, Johansson E, Unemo M. 2012. Clinical Neisseria gonorrhoeae isolate with a N. meningitidis porA gene and no prolyliminopeptidase activity, Sweden, 2011: danger of false-negative genetic and culture diagnostic results. Euro Surveill 17(9):pii-20102. http://www . eurosurveillance. org/ViewArticle. aspx?ArticleId-20102.
34. Tabrizi SN, Chen S, Tapsall J, Garland SM. 2005. Evaluation of opabased real-time PCR for detection of Neisseria gonorrhoeae. Sex Transm Dis 32:199-202. http://dx. doi. org/10. 1097/01. olq. 0000154495. 24519. b.f.
35. Whiley DM, Buda PJ, Bayliss J, Cover L, Bates J, Sloots TP. 2004. A new confirmatory Neisseria gonorrhoeae real-time PCR assay targeting the porA pseudogene. Eur J Clin Microbiol Infect Dis 23:705-710.
36. Tanaka M, Nakayama H, Huruya K, Konomi I, Irie S, Kanayama A, Saika T, Kobayashi I. 2006. Analysis of mutations within multiple genes associated with resistance in a clinical isolate of Neisseria gonorrhoeae with reduced ceftriaxone susceptibility that shows a multidrug-resistant phenotype. Int J Antimicrob Agents 27:20-26. http://dx. doi. org/10. 1016/j . ijantimicag. 2005. 08. 021.
37. Ameyama S, Onodera S, Takahata M, Minami S, Maki N, Endo K, Goto H, Suzuki H, Oishi Y. 2002. Mosaic-like structure of penicillin-binding protein 2 gene (penA) in clinical isolates of Neisseria gonorrhoeae with reduced susceptibility to cefixime. Antimicrob Agents Chemother 46: 3744-3749. http://dx. doi. org/10. 1128/AAC. 46. 12. 3744-3749. 2002.
38. Knapp JS, Hook EW, III. 1988. Prevalence and persistence of Neisseria cinerea and other Neisseria spp. in adults. J Clin Microbiol 26:896-900.
39. Bissessor M, Tabrizi SN, Fairley CK, Danielewski J, Whitton B, Bird S, Garland S, Chen MY. 2011. Differing Neisseria gonorrhoeae bacterial loads in the pharynx and rectum in men who have sex with men: implications for gonococcal detection, transmission, and control. J Clin Microbiol 49:4304-4306. http://dx. doi. org/10. 1128/JCM. 05341-11.
40. Lindberg R, Fredlund H, Nicholas R, Unemo M. 2007. Neisseria gonorrhoeae isolates with reduced susceptibility to cefixime and ceftriaxone: association with genetic polymorphisms in penA, mtrR, porB1b, and ponA. Antimicrob Agents Chemother 51:2117-2122. http://dx. doi. org/10. 1128 /AAC. 01604-06.
41. Osaka K, Takakura T, Narukawa K, Takahata M, Endo K, Kiyota H, Onodera S. 2008. Analysis of amino acid sequences of penicillin-binding protein 2 in clinical isolates of Neisseria gonorrhoeae with reduced susceptibility to cefixime and ceftriaxone. J Infect Chemother 14:195-203. http: //dx. doi. org/10. 1007/s10156-008-0610-7.