Skip to main content
Top
Published in: BMC Infectious Diseases 1/2014

Open Access 01-12-2014 | Research article

Characterisation of bla TEM genes and types of β-lactamase plasmids in Neisseria gonorrhoeae – the prevalent and conserved bla TEM-135 has not recently evolved and existed in the Toronto plasmid from the origin

Authors: Ibrahim Muhammad, Daniel Golparian, Jo-Anne R Dillon, Åsa Johansson, Makoto Ohnishi, Sunil Sethi, Shao-chun Chen, Shu-ichi Nakayama, Martin Sundqvist, Manju Bala, Magnus Unemo

Published in: BMC Infectious Diseases | Issue 1/2014

Login to get access

Abstract

Background

Antimicrobial resistance (AMR) in Neisseria gonorrhoeae is a major concern worldwide. It has been recently feared that the bla TEM-1 gene is, via bla TEM-135, evolving into an extended-spectrum β-lactamase (ESBL), which could degrade all cephalosporins including ceftriaxone. The aims of the present study were to characterize the bla TEM genes, types of β-lactamase plasmids, the degradation of ampicillin by TEM-135 compared to TEM-1, and to perform molecular epidemiological typing of β-lactamase-producing N. gonorrhoeae strains internationally.

Methods

β-lactamase producing N. gonorrhoeae isolates (n = 139) cultured from 2000 to 2011 in 15 countries were examined using antibiograms, bla TEM gene sequencing, β-lactamase plasmid typing, and N. gonorrhoeae multiantigen sequence typing (NG-MAST). Furthermore, the bla TEM gene was sequenced in the first described Toronto plasmid (pJD7), one of the first Asian plasmids (pJD4) and African plasmids (pJD5) isolated in Canada. The degradation of ampicillin by TEM-135 compared to TEM-1 was examined using a MALDI-TOF MS hydrolysis assay.

Results

Six different bla TEM sequences were identified (among isolates with 125 different NG-MAST STs), i.e. bla TEM-1 (in 104 isolates), bla TEM-135 (in 30 isolates), and four novel bla TEM sequences (in 5 isolates). The bla TEM-1 allele was only found in the African and Asian plasmids, while all Rio/Toronto plasmids possessed the bla TEM-135 allele. Most interesting, the first described gonococcal Toronto plasmid (pJD7), identified in 1984, also possessed the highly conserved bla TEM-135 allele. The degradation of ampicillin by TEM-135 compared to TEM-1 was indistinguishable in the MALDI-TOF MS hydrolysis assay.

Conclusions

bla TEM-135, encoding TEM-135, is predominantly and originally associated with the Rio/Toronto plasmid and prevalent among the β-lactamase producing gonococcal strains circulating globally. bla TEM-135 does not appear, as previously hypothesized, to have recently evolved due to some evolutionary selective pressure, for example, by the extensive use of extended-spectrum cephalosporins worldwide. On the contrary, the present study shows that bla TEM-135 existed in the Toronto plasmid from its discovery and that bla TEM-135 is highly conserved (not further evolved in the past >30 years). Nevertheless, international studies for monitoring the presence of different bla TEM alleles, the possible evolution of the bla TEM-135 allele, and the types of β-lactamase producing plasmids, remain imperative.
Appendix
Available only for authorised users
Literature
2.
go back to reference Lewis DA: The gonococcus fights back: is this time a knock out?. Sex Transm Infect. 2010, 86: 415-421.CrossRefPubMed Lewis DA: The gonococcus fights back: is this time a knock out?. Sex Transm Infect. 2010, 86: 415-421.CrossRefPubMed
3.
go back to reference 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: 821-834.CrossRefPubMed 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: 821-834.CrossRefPubMed
4.
go back to reference Unemo M, Shafer WM: Antimicrobial resistance in Neisseria gonorrhoeae in the 21st century: past, evolution and future. Clin Microbiol Rev. 2014, 27: 587-613.CrossRefPubMedPubMedCentral Unemo M, Shafer WM: Antimicrobial resistance in Neisseria gonorrhoeae in the 21st century: past, evolution and future. Clin Microbiol Rev. 2014, 27: 587-613.CrossRefPubMedPubMedCentral
5.
6.
go back to reference Deguchi T, Yasuda M, Yokoi S, Ishida K, Ito M, Ishihara S, Minamidate K, Harada Y, Tei K, Kojima K, Tamaki M, Maeda S: Treatment of uncomplicated gonococcal urethritis by double-dosing of 200 mg cefixime at a 6-h interval. J Infect Chemother. 2003, 9: 35-39.CrossRefPubMed Deguchi T, Yasuda M, Yokoi S, Ishida K, Ito M, Ishihara S, Minamidate K, Harada Y, Tei K, Kojima K, Tamaki M, Maeda S: Treatment of uncomplicated gonococcal urethritis by double-dosing of 200 mg cefixime at a 6-h interval. J Infect Chemother. 2003, 9: 35-39.CrossRefPubMed
7.
go back to reference Yokoi S, Deguchi T, Ozawa T, Yasuda M, Ito S, Kubota Y, Tamaki M, Maeda S: Threat to cefixime treatment for gonorrhea. Emerg Infect Dis. 2007, 13: 1275-1277.PubMedPubMedCentral Yokoi S, Deguchi T, Ozawa T, Yasuda M, Ito S, Kubota Y, Tamaki M, Maeda S: Threat to cefixime treatment for gonorrhea. Emerg Infect Dis. 2007, 13: 1275-1277.PubMedPubMedCentral
8.
go back to reference Ison CA, Hussey J, Sankar KN, Evans J, Alexander S: Gonorrhoea treatment failures to cefixime and azithromycin in England, 2012. Euro Surveill. 2011, 16 (14): pii=19833- Ison CA, Hussey J, Sankar KN, Evans J, Alexander S: Gonorrhoea treatment failures to cefixime and azithromycin in England, 2012. Euro Surveill. 2011, 16 (14): pii=19833-
9.
go back to reference 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: 1273-1280.CrossRefPubMedPubMedCentral 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: 1273-1280.CrossRefPubMedPubMedCentral
10.
go back to reference Unemo M, Golparian D, Stary A, Eigentler A: First Neisseria gonorrhoeae strain with resistance to cefixime causing gonorrhoea treatment failure in Austria, 2011. Euro Surveill. 2011, 16 (43): pii=19998- Unemo M, Golparian D, Stary A, Eigentler A: First Neisseria gonorrhoeae strain with resistance to cefixime causing gonorrhoea treatment failure in Austria, 2011. Euro Surveill. 2011, 16 (43): pii=19998-
11.
go back to reference 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 (47): pii=19721- 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 (47): pii=19721-
12.
go back to reference Lewis DA, Sriruttan C, Müller EE, Golparian D, Gumede L, Fick D, de Wet J, Maseko V, Coetzee J, Unemo M: 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: 1267-1270.CrossRefPubMed Lewis DA, Sriruttan C, Müller EE, Golparian D, Gumede L, Fick D, de Wet J, Maseko V, Coetzee J, Unemo M: 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: 1267-1270.CrossRefPubMed
13.
go back to reference Allen VG, Mitterni L, Seah C, Rebbapragada A, Martin IE, Lee C, Siebert H, Towns L, Melano RG, Low DE: Neisseria gonorrhoeae treatment failure and susceptibility to cefixime in Toronto, Canada. JAMA. 2013, 309: 163-170.CrossRefPubMed Allen VG, Mitterni L, Seah C, Rebbapragada A, Martin IE, Lee C, Siebert H, Towns L, Melano RG, Low DE: Neisseria gonorrhoeae treatment failure and susceptibility to cefixime in Toronto, Canada. JAMA. 2013, 309: 163-170.CrossRefPubMed
14.
go back to reference Unemo M, Golparian D, Potočnik M, Jeverica S: Treatment failure of pharyngeal gonorrhoea with internationally recommended first-line ceftriaxone verified in Slovenia, September 2011. Euro Surveill. 2012, 17: 1-4. Unemo M, Golparian D, Potočnik M, Jeverica S: Treatment failure of pharyngeal gonorrhoea with internationally recommended first-line ceftriaxone verified in Slovenia, September 2011. Euro Surveill. 2012, 17: 1-4.
15.
go back to reference Unemo M, Golparian D, Hestner A: Ceftriaxone treatment failure of pharyngeal gonorrhoea verified by international recommendations, Sweden, July 2010. Euro Surveill. 2011, 16: 1-3. Unemo M, Golparian D, Hestner A: Ceftriaxone treatment failure of pharyngeal gonorrhoea verified by international recommendations, Sweden, July 2010. Euro Surveill. 2011, 16: 1-3.
16.
go back to reference Tapsall J, Read P, Carmody C, Bourne C, Ray S, Limnios A, Sloots T, Whiley D: Two cases of failed ceftriaxone treatment in pharyngeal gonorrhoea verified by molecular microbiological methods. J Med Microbiol. 2009, 58: 683-687.CrossRefPubMed Tapsall J, Read P, Carmody C, Bourne C, Ray S, Limnios A, Sloots T, Whiley D: Two cases of failed ceftriaxone treatment in pharyngeal gonorrhoea verified by molecular microbiological methods. J Med Microbiol. 2009, 58: 683-687.CrossRefPubMed
17.
go back to reference Chen YM, Stevens K, Tideman R, Zaia A, Tomita T, Fairley CK, Lahra M, Whiley D, Hogg G: Failure of ceftriaxone 500 mg to eradicate pharyngeal gonorrhoea, Australia. J Antimicrob Chemother. 2013, 68: 1445-1447.CrossRef Chen YM, Stevens K, Tideman R, Zaia A, Tomita T, Fairley CK, Lahra M, Whiley D, Hogg G: Failure of ceftriaxone 500 mg to eradicate pharyngeal gonorrhoea, Australia. J Antimicrob Chemother. 2013, 68: 1445-1447.CrossRef
18.
go back to reference Ohnishi M, Golparian D, Shimuta K, Saika T, Hoshina S, Iwasaku K, Nakayama S, Kitawaki J, Unemo M: 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. 2011, 55: 3538-3545.CrossRefPubMedPubMedCentral Ohnishi M, Golparian D, Shimuta K, Saika T, Hoshina S, Iwasaku K, Nakayama S, Kitawaki J, Unemo M: 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. 2011, 55: 3538-3545.CrossRefPubMedPubMedCentral
19.
go back to reference Read PJ, Limnios EA, McNulty A, Whiley D, Lahra LM: One confirmed and one suspected case of pharyngeal gonorrhoea treatment failure following 500 mg ceftriaxone in Sydney, Australia. Sex Health. 2013, 10: 460-462.CrossRefPubMed Read PJ, Limnios EA, McNulty A, Whiley D, Lahra LM: One confirmed and one suspected case of pharyngeal gonorrhoea treatment failure following 500 mg ceftriaxone in Sydney, Australia. Sex Health. 2013, 10: 460-462.CrossRefPubMed
20.
go back to reference Camara J, Serra J, Ayats J, Bastida T, Carnicer-Pont D, Andreu A, Ardanuy C: Molecular characterization of two high-level ceftriaxone-resistant Neisseria gonorrhoeae isolates detected in Catalonia, Spain. J Antimicrob Chemother. 2012, 67: 1858-1860.CrossRefPubMed Camara J, Serra J, Ayats J, Bastida T, Carnicer-Pont D, Andreu A, Ardanuy C: Molecular characterization of two high-level ceftriaxone-resistant Neisseria gonorrhoeae isolates detected in Catalonia, Spain. J Antimicrob Chemother. 2012, 67: 1858-1860.CrossRefPubMed
21.
go back to reference Ashford WA, Golash RG, Hemming VG: Penicillinase-producing Neisseria gonorrhoeae. Lancet. 1976, 2: 657-658.CrossRefPubMed Ashford WA, Golash RG, Hemming VG: Penicillinase-producing Neisseria gonorrhoeae. Lancet. 1976, 2: 657-658.CrossRefPubMed
22.
23.
go back to reference Bergström S, Norlander L, Norqvist A, Normark S: Contribution of a TEM-1-like beta-lactamase to penicillin resistance in Neisseria gonorrhoeae. Antimicrob Agents Chemother. 1978, 13: 618-623.CrossRefPubMedPubMedCentral Bergström S, Norlander L, Norqvist A, Normark S: Contribution of a TEM-1-like beta-lactamase to penicillin resistance in Neisseria gonorrhoeae. Antimicrob Agents Chemother. 1978, 13: 618-623.CrossRefPubMedPubMedCentral
24.
go back to reference Pagotto F, Aman AT, Ng L-K, Yeung KH, Brett M, Dillon JA: Sequence analysis of the family of penicillinase-producing plasmids of Neisseria gonorrhoeae based on DNA sequencing. Plasmid. 2000, 43: 24-34.CrossRefPubMed Pagotto F, Aman AT, Ng L-K, Yeung KH, Brett M, Dillon JA: Sequence analysis of the family of penicillinase-producing plasmids of Neisseria gonorrhoeae based on DNA sequencing. Plasmid. 2000, 43: 24-34.CrossRefPubMed
25.
go back to reference Palmer HM, Leeming JP, Turner A: A multiplex polymerase chain reaction to differentiate β-lactamase plasmids of Neisseria gonorrhoeae. J Antimicrob Chemother. 2000, 45: 777-782.CrossRefPubMed Palmer HM, Leeming JP, Turner A: A multiplex polymerase chain reaction to differentiate β-lactamase plasmids of Neisseria gonorrhoeae. J Antimicrob Chemother. 2000, 45: 777-782.CrossRefPubMed
26.
go back to reference Dillon JR, Yeung KH: β-lactamase plasmids and chromosomally mediated antibiotic resistance in pathogenic Neisseria species. Clin Microbiol Rev. 1989, 2: S125-S133.CrossRefPubMedPubMedCentral Dillon JR, Yeung KH: β-lactamase plasmids and chromosomally mediated antibiotic resistance in pathogenic Neisseria species. Clin Microbiol Rev. 1989, 2: S125-S133.CrossRefPubMedPubMedCentral
27.
go back to reference Müller EE, Fayemiwo SA, Lewis DA: Characterization of a novel β-lactamase-producing plasmid in Neisseria gonorrhoeae: sequence analysis and molecular typing of host gonococci. J Antimicrob Chemother. 2011, 66: 1514-1517.CrossRefPubMed Müller EE, Fayemiwo SA, Lewis DA: Characterization of a novel β-lactamase-producing plasmid in Neisseria gonorrhoeae: sequence analysis and molecular typing of host gonococci. J Antimicrob Chemother. 2011, 66: 1514-1517.CrossRefPubMed
28.
go back to reference Trembizki E, Buckley C, Lawrence A, Lahra M, Whiley D: On behalf of the GRAND study investigators: Characterisation of a novel Neisseria gonorrhoeae penicillinase-producing plasmid, Australia 2012. Antimicrob Agents Chemother. 2014, 58: 4984-4985.CrossRefPubMedPubMedCentral Trembizki E, Buckley C, Lawrence A, Lahra M, Whiley D: On behalf of the GRAND study investigators: Characterisation of a novel Neisseria gonorrhoeae penicillinase-producing plasmid, Australia 2012. Antimicrob Agents Chemother. 2014, 58: 4984-4985.CrossRefPubMedPubMedCentral
29.
go back to reference Ohnishi M, Ono E, Shimuta K, Watanabe H, Okamura N: Identification of TEM-135 β-lactamase in penicillinase-producing Neisseria gonorrhoeae strains in Japan. Antimicrob Agents Chemother. 2010, 54: 3021-3023.CrossRefPubMedPubMedCentral Ohnishi M, Ono E, Shimuta K, Watanabe H, Okamura N: Identification of TEM-135 β-lactamase in penicillinase-producing Neisseria gonorrhoeae strains in Japan. Antimicrob Agents Chemother. 2010, 54: 3021-3023.CrossRefPubMedPubMedCentral
30.
go back to reference Arlet G, Goussard S, Courvalin P, Philippon A: Sequences of the genes for the TEM-20, TEM-21, TEM-22, and TEM-29 extended-spectrum β-lactamases. Antimicrob Agents Chemother. 1999, 43: 969-971.PubMedPubMedCentral Arlet G, Goussard S, Courvalin P, Philippon A: Sequences of the genes for the TEM-20, TEM-21, TEM-22, and TEM-29 extended-spectrum β-lactamases. Antimicrob Agents Chemother. 1999, 43: 969-971.PubMedPubMedCentral
31.
go back to reference Michael GB, Butaye P, Cloeckaert A, Schwarz S: Genes and mutations conferring antimicrobial resistance in Salmonella: An update. Microb Infect. 2006, 8: 1898-1914.CrossRef Michael GB, Butaye P, Cloeckaert A, Schwarz S: Genes and mutations conferring antimicrobial resistance in Salmonella: An update. Microb Infect. 2006, 8: 1898-1914.CrossRef
33.
go back to reference Pasquali F, Kehrenberg C, Manfreda G, Schwarz S: Physical linkage of Tn3 and part of Tn1721 in a tetracycline and ampicillin resistance plasmid from Salmonella Typhimurium. J Antimicrob Chemother. 2005, 55: 562-565.CrossRefPubMed Pasquali F, Kehrenberg C, Manfreda G, Schwarz S: Physical linkage of Tn3 and part of Tn1721 in a tetracycline and ampicillin resistance plasmid from Salmonella Typhimurium. J Antimicrob Chemother. 2005, 55: 562-565.CrossRefPubMed
34.
go back to reference Nakayama S, Tribuddharat C, Prombhul S, Shimuta K, Srifuengfung S, Unemo M, Ohnishi M: Molecular analyses of TEM genes and their corresponding penicillinase-producing Neisseria gonorrhoeae isolates in Bangkok, Thailand. Antimicrob Agents Chemother. 2012, 56: 916-920.CrossRefPubMedPubMedCentral Nakayama S, Tribuddharat C, Prombhul S, Shimuta K, Srifuengfung S, Unemo M, Ohnishi M: Molecular analyses of TEM genes and their corresponding penicillinase-producing Neisseria gonorrhoeae isolates in Bangkok, Thailand. Antimicrob Agents Chemother. 2012, 56: 916-920.CrossRefPubMedPubMedCentral
35.
go back to reference Chen SC, Yin YP, Dai XQ, Yu RX, Han Y, Sun HH, Ohnishi M, Unemo M, Chen XS: Prevalence and molecular epidemiological typing of penicillinase-producing Neisseria gonorrhoeae and their bla(TEM-135) gene variants in Nanjing, China. Sex Transm Dis. 2013, 40: 872-876.CrossRefPubMed Chen SC, Yin YP, Dai XQ, Yu RX, Han Y, Sun HH, Ohnishi M, Unemo M, Chen XS: Prevalence and molecular epidemiological typing of penicillinase-producing Neisseria gonorrhoeae and their bla(TEM-135) gene variants in Nanjing, China. Sex Transm Dis. 2013, 40: 872-876.CrossRefPubMed
36.
go back to reference Srifeungfung S, Roongpisuthipong A, Asavapiriyanont S, Lolekha R, Tribuddharat C, Lokpichart S, Sungthong P, Tongtep P: Prevalence of Chlamydia trachomatis and Neisseria gonorrhoeae in HIV-seropositive patients and gonococcal antimicrobial susceptibility: an update in Thailand. J Infect Dis. 2009, 62: 467-470. Srifeungfung S, Roongpisuthipong A, Asavapiriyanont S, Lolekha R, Tribuddharat C, Lokpichart S, Sungthong P, Tongtep P: Prevalence of Chlamydia trachomatis and Neisseria gonorrhoeae in HIV-seropositive patients and gonococcal antimicrobial susceptibility: an update in Thailand. J Infect Dis. 2009, 62: 467-470.
37.
go back to reference Orencia MC, Yoon JS, Ness JE, Stemmer WP, Stevens RC: Predicting the emergence of antibiotic resistance by directed evolution and structural analysis. Nat Struct Biol. 2001, 8: 238-242.CrossRefPubMed Orencia MC, Yoon JS, Ness JE, Stemmer WP, Stevens RC: Predicting the emergence of antibiotic resistance by directed evolution and structural analysis. Nat Struct Biol. 2001, 8: 238-242.CrossRefPubMed
38.
go back to reference Unemo M, Fasth O, Fredlund H, Limnios A, Tapsall JW: 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. 2009, 63: 1142-1151.CrossRefPubMed Unemo M, Fasth O, Fredlund H, Limnios A, Tapsall JW: 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. 2009, 63: 1142-1151.CrossRefPubMed
39.
go back to reference Yeung KH, Dillon JR, Pauzé M, Wallace E: A novel 4.9-kilobase plasmid associated with an outbreak of penicillinase-producing Neisseria gonorrhoeae. J Infect Dis. 1986, 153: 1162-1165.CrossRefPubMed Yeung KH, Dillon JR, Pauzé M, Wallace E: A novel 4.9-kilobase plasmid associated with an outbreak of penicillinase-producing Neisseria gonorrhoeae. J Infect Dis. 1986, 153: 1162-1165.CrossRefPubMed
40.
go back to reference Yeung KH, Dillon JR: In vitro transcription/translation products and molecular characterization of naturally occurring and in vitro deletion of the 7.2 kb plasmid of Neisseria gonorrhoeae. p. 209 215. The Pathogenic Neisseriae. Proceedings of the 4th international symposium, Asilomar, California, 21 25 October 1984. Edited by: Schoolnik GK. 1985, Washington, D.C: American Society for Microbiology (ASM) Yeung KH, Dillon JR: In vitro transcription/translation products and molecular characterization of naturally occurring and in vitro deletion of the 7.2 kb plasmid of Neisseria gonorrhoeae. p. 209 215. The Pathogenic Neisseriae. Proceedings of the 4th international symposium, Asilomar, California, 21 25 October 1984. Edited by: Schoolnik GK. 1985, Washington, D.C: American Society for Microbiology (ASM)
41.
go back to reference Pagotto F, Dillon JA: Multiple origins and replication proteins influence biological properties of beta-lactamase-producing plasmids from Neisseria gonorrhoeae. J Bacteriol. 2001, 183: 5472-5481.CrossRefPubMedPubMedCentral Pagotto F, Dillon JA: Multiple origins and replication proteins influence biological properties of beta-lactamase-producing plasmids from Neisseria gonorrhoeae. J Bacteriol. 2001, 183: 5472-5481.CrossRefPubMedPubMedCentral
42.
go back to reference Sparbier K, Schubert S, Weller U, Boogen C, Kostrzewa M: Matrix-assisted laser desorption ionization-time of flight mass spectrometry-based functional assay for rapid detection of resistance against β-lactam antibiotics. J Clin Microbiol. 2012, 50: 927-937.CrossRefPubMedPubMedCentral Sparbier K, Schubert S, Weller U, Boogen C, Kostrzewa M: Matrix-assisted laser desorption ionization-time of flight mass spectrometry-based functional assay for rapid detection of resistance against β-lactam antibiotics. J Clin Microbiol. 2012, 50: 927-937.CrossRefPubMedPubMedCentral
43.
go back to reference Ambler RP, Coulson AF, Frère JM, Ghuysen JM, Joris B, Forsman M, Levesque RC, Tiraby G, Waley SG: A standard numbering scheme for the class A beta-lactamases. Biochem J. 1991, 276: 269-270.CrossRefPubMedPubMedCentral Ambler RP, Coulson AF, Frère JM, Ghuysen JM, Joris B, Forsman M, Levesque RC, Tiraby G, Waley SG: A standard numbering scheme for the class A beta-lactamases. Biochem J. 1991, 276: 269-270.CrossRefPubMedPubMedCentral
44.
go back to reference Martin IM, Ison CA, Aanensen DM, Fenton KA, Spratt BG: Rapid sequence-based identification of gonococcal transmission clusters in a large metropolitan area. J Infect Dis. 2004, 189: 1497-1505.CrossRefPubMed Martin IM, Ison CA, Aanensen DM, Fenton KA, Spratt BG: Rapid sequence-based identification of gonococcal transmission clusters in a large metropolitan area. J Infect Dis. 2004, 189: 1497-1505.CrossRefPubMed
45.
go back to reference Unemo M, Dillon JA: Review and international recommendation of methods for typing Neisseria gonorrhoeae isolates and their implications for improved knowledge of gonococcal epidemiology, treatment, and biology. Clin Microbiol Rev. 2011, 24: 447-458.CrossRefPubMedPubMedCentral Unemo M, Dillon JA: Review and international recommendation of methods for typing Neisseria gonorrhoeae isolates and their implications for improved knowledge of gonococcal epidemiology, treatment, and biology. Clin Microbiol Rev. 2011, 24: 447-458.CrossRefPubMedPubMedCentral
46.
go back to reference Unemo M, Sjöstrand A, Akhras M, Gharizadeh B, Lindbäck E, Pourmand N, Wretlind B, Fredlund H: Molecular characterization of Neisseria gonorrhoeae identifies transmission and resistance of one ciprofloxacin-resistant strain. APMIS. 2007, 115: 231-241.CrossRefPubMedPubMedCentral Unemo M, Sjöstrand A, Akhras M, Gharizadeh B, Lindbäck E, Pourmand N, Wretlind B, Fredlund H: Molecular characterization of Neisseria gonorrhoeae identifies transmission and resistance of one ciprofloxacin-resistant strain. APMIS. 2007, 115: 231-241.CrossRefPubMedPubMedCentral
Metadata
Title
Characterisation of bla TEM genes and types of β-lactamase plasmids in Neisseria gonorrhoeae – the prevalent and conserved bla TEM-135 has not recently evolved and existed in the Toronto plasmid from the origin
Authors
Ibrahim Muhammad
Daniel Golparian
Jo-Anne R Dillon
Åsa Johansson
Makoto Ohnishi
Sunil Sethi
Shao-chun Chen
Shu-ichi Nakayama
Martin Sundqvist
Manju Bala
Magnus Unemo
Publication date
01-12-2014
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2014
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/1471-2334-14-454

Other articles of this Issue 1/2014

BMC Infectious Diseases 1/2014 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.