Skip to main content
Top
Published in: BMC Infectious Diseases 1/2019

Open Access 01-12-2019 | Ciprofloxacin | Research article

Chromosomal and plasmid-mediated fluoroquinolone resistance in human Salmonella enterica infection in Ghana

Authors: Godfred Acheampong, Michael Owusu, Alex Owusu-Ofori, Isaac Osei, Nimako Sarpong, Augustina Sylverken, Hung-Jui Kung, Shu-Ting Cho, Chih-Horng Kuo, Se Eun Park, Florian Marks, Yaw Adu-Sarkodie, Ellis Owusu-Dabo

Published in: BMC Infectious Diseases | Issue 1/2019

Login to get access

Abstract

Background

Salmonella infection poses significant public health threat globally, especially in resource-limited countries. Emergence and spread of antibiotic resistant strains to fluoroquinolones have led to treatment failures and increased mortality in Salmonella infection. However, there is dearth of information regarding mechanisms of resistance to fluoroquinolones in Ghana. This study therefore sought to identify chromosomal mutations and plasmid-mediated resistance as possible mechanisms of fluoroquinolone resistance from clinical isolates in Ghana.

Methods

This was a retrospective study of archived isolates biobanked at Kumasi Centre for Collaborative Research in Tropical Medicine, Ghana. Isolates were obtained from blood, stool and oropharynx samples at two hospitals, between May, 2016 and January, 2018. Salmonella identification was done using standard microbiological protocols and antibiotic susceptibility testing performed by Kirby-Bauer disc diffusion method. Isolates with intermediate susceptibility and/or resistance to nalidixic acid and/or ciprofloxacin were selected and examined for chromosomal mutations by Sanger sequencing and plasmid-mediated resistance by PCR.

Results

Of 133 biobanked isolates cultured, 68 (51.1%) and 16 (12%) were identified as Salmonella Typhi and non-typhoidal Salmonella (NTS), respectively. Sequence analysis of gyrA gene revealed the presence of 5 different nonsynonymous mutations, with the most frequent mutation (Ile203Ser) occurring in 12 out of 13 isolates tested. Gyrase B (gyrB) gene had 1 nonsynonymous mutation in 3 out of 13 isolates, substituting phenylalanine with leucine at codon 601 (Phe601Leu). No mutation was observed in parC and parE genes. Two NTS isolates were found to harbour qnrS plasmid-mediated resistant gene of molecular size 550 bp with high ciprofloxacin MIC of 0.5 μg/ml.

Conclusion

This study reports for the first time in Ghana plasmid-mediated fluoroquinolone resistant gene qnrS in Salmonella clinical isolates. Nonsynonymous mutations of gyrA and gyrB genes likely to confer Salmonella reduced susceptibility to ciprofloxacin were also reported.
Literature
1.
go back to reference Mogasale V, Maskery B, Ochiai RL, Lee JS, Mogasale VV, Ramani E, Kim YE, Park JK, Wierzba TF. Burden of typhoid fever in low-income and middle-income countries: a systematic, literature-based update with risk-factor adjustment. Lancet Glob Health. 2014;2(10):e570–80.CrossRefPubMed Mogasale V, Maskery B, Ochiai RL, Lee JS, Mogasale VV, Ramani E, Kim YE, Park JK, Wierzba TF. Burden of typhoid fever in low-income and middle-income countries: a systematic, literature-based update with risk-factor adjustment. Lancet Glob Health. 2014;2(10):e570–80.CrossRefPubMed
2.
go back to reference Tatavarthy A, Luna VA, Amuso PT. How multidrug resistance in typhoid fever affects treatment options. Ann N Y Acad Sci. 2014;1323:76–90.PubMedCrossRef Tatavarthy A, Luna VA, Amuso PT. How multidrug resistance in typhoid fever affects treatment options. Ann N Y Acad Sci. 2014;1323:76–90.PubMedCrossRef
3.
go back to reference Park SE, Pham DT, Boinett C, Wong VK, Pak GD, Panzner U, Espinoza LMC, von Kalckreuth V, Im J, Schütt-Gerowitt H. The phylogeography and incidence of multi-drug resistant typhoid fever in sub-Saharan Africa. Nat Commun. 2018;9(1):5094.PubMedPubMedCentralCrossRef Park SE, Pham DT, Boinett C, Wong VK, Pak GD, Panzner U, Espinoza LMC, von Kalckreuth V, Im J, Schütt-Gerowitt H. The phylogeography and incidence of multi-drug resistant typhoid fever in sub-Saharan Africa. Nat Commun. 2018;9(1):5094.PubMedPubMedCentralCrossRef
4.
go back to reference Wong VK, Baker S, Pickard DJ, Parkhill J, Page AJ, Feasey NA, Kingsley RA, Thomson NR, Keane JA, Weill F-X. Phylogeographical analysis of the dominant multidrug-resistant H58 clade of Salmonella Typhi identifies inter-and intracontinental transmission events. Nat Genet. 2015;47(6):632.PubMedPubMedCentralCrossRef Wong VK, Baker S, Pickard DJ, Parkhill J, Page AJ, Feasey NA, Kingsley RA, Thomson NR, Keane JA, Weill F-X. Phylogeographical analysis of the dominant multidrug-resistant H58 clade of Salmonella Typhi identifies inter-and intracontinental transmission events. Nat Genet. 2015;47(6):632.PubMedPubMedCentralCrossRef
5.
go back to reference Su L-H, Chiu C-H, Chu C, Ou JT. Antimicrobial resistance in nontyphoid Salmonella serotypes: a global challenge. Clin Infect Dis. 2004;39(4):546–51.PubMedCrossRef Su L-H, Chiu C-H, Chu C, Ou JT. Antimicrobial resistance in nontyphoid Salmonella serotypes: a global challenge. Clin Infect Dis. 2004;39(4):546–51.PubMedCrossRef
6.
go back to reference Mills-Robertson F, Addy ME, Mensah P, Crupper SS. Molecular characterization of antibiotic resistance in clinical Salmonella typhi isolated in Ghana. FEMS Microbiol Lett. 2002;215(2):249–53.PubMedCrossRef Mills-Robertson F, Addy ME, Mensah P, Crupper SS. Molecular characterization of antibiotic resistance in clinical Salmonella typhi isolated in Ghana. FEMS Microbiol Lett. 2002;215(2):249–53.PubMedCrossRef
7.
go back to reference Harish BN, Menezes GA, Sarangapani K, Parija SC. A case report and review of the literature: ciprofloxacin resistant Salmonella enterica serovar Typhi in India. J Infect Dev Ctries. 2008;2(04):324–7.PubMedCrossRef Harish BN, Menezes GA, Sarangapani K, Parija SC. A case report and review of the literature: ciprofloxacin resistant Salmonella enterica serovar Typhi in India. J Infect Dev Ctries. 2008;2(04):324–7.PubMedCrossRef
8.
go back to reference Cuypers WL, Jacobs J, Wong V, Klemm EJ, Deborggraeve S, Van Puyvelde S. Fluoroquinolone resistance in Salmonella: insights by whole-genome sequencing. Microb Genomics. 2018;4(7):1–9. Cuypers WL, Jacobs J, Wong V, Klemm EJ, Deborggraeve S, Van Puyvelde S. Fluoroquinolone resistance in Salmonella: insights by whole-genome sequencing. Microb Genomics. 2018;4(7):1–9.
9.
go back to reference Cattoir V, Weill F-X, Poirel L, Fabre L, Soussy C-J, Nordmann P. Prevalence of qnr genes in Salmonella in France. J Antimicrob Chemother. 2007;59(4):751–4.PubMedCrossRef Cattoir V, Weill F-X, Poirel L, Fabre L, Soussy C-J, Nordmann P. Prevalence of qnr genes in Salmonella in France. J Antimicrob Chemother. 2007;59(4):751–4.PubMedCrossRef
10.
go back to reference Robicsek A, Jacoby GA, Hooper DC. The worldwide emergence of plasmid-mediated quinolone resistance. Lancet Infect Dis. 2006;6(10):629–40.PubMedCrossRef Robicsek A, Jacoby GA, Hooper DC. The worldwide emergence of plasmid-mediated quinolone resistance. Lancet Infect Dis. 2006;6(10):629–40.PubMedCrossRef
11.
go back to reference Aldred KJ, Kerns RJ, Osheroff N. Mechanism of quinolone action and resistance. Biochemistry. 2014;53(10):1565–74.PubMedCrossRef Aldred KJ, Kerns RJ, Osheroff N. Mechanism of quinolone action and resistance. Biochemistry. 2014;53(10):1565–74.PubMedCrossRef
12.
go back to reference Sjölund-Karlsson M, Howie R, Rickert R, Krueger A, Tran T-T, Zhao S, Ball T, Haro J, Pecic G, Joyce K. Plasmid-mediated quinolone resistance among non-typhiSalmonella enterica isolates, USA. Emerg Infect Dis. 2010;16(11):1789.PubMedPubMedCentralCrossRef Sjölund-Karlsson M, Howie R, Rickert R, Krueger A, Tran T-T, Zhao S, Ball T, Haro J, Pecic G, Joyce K. Plasmid-mediated quinolone resistance among non-typhiSalmonella enterica isolates, USA. Emerg Infect Dis. 2010;16(11):1789.PubMedPubMedCentralCrossRef
13.
14.
go back to reference Abgottspon H, Zurfluh K, Nüesch-Inderbinen M, Hächler H, Stephan R. Quinolone resistance mechanisms in Salmonella enterica serovars Hadar, Kentucky, Virchow, Schwarzengrund, and 4, 5, 12: i:−, isolated from humans in Switzerland, and identification of a novel qnrD variant, qnrD2, in S. Hadar. Antimicrob Agents Chemother. 2014;58(6):3560–3.PubMedPubMedCentralCrossRef Abgottspon H, Zurfluh K, Nüesch-Inderbinen M, Hächler H, Stephan R. Quinolone resistance mechanisms in Salmonella enterica serovars Hadar, Kentucky, Virchow, Schwarzengrund, and 4, 5, 12: i:−, isolated from humans in Switzerland, and identification of a novel qnrD variant, qnrD2, in S. Hadar. Antimicrob Agents Chemother. 2014;58(6):3560–3.PubMedPubMedCentralCrossRef
15.
go back to reference Al-Emran HM, Heisig A, Dekker D, Adu-Sarkodie Y, Cruz Espinoza LM, Panzner U, von Kalckreuth V, Marks F, Park SE, Sarpong N. Detection of a novel gyrB mutation associated with fluoroquinolone-nonsusceptible Salmonella enterica serovar Typhimurium isolated from a bloodstream infection in Ghana. Clin Infect Dis. 2016;62(suppl_1):S47–9.PubMedCrossRef Al-Emran HM, Heisig A, Dekker D, Adu-Sarkodie Y, Cruz Espinoza LM, Panzner U, von Kalckreuth V, Marks F, Park SE, Sarpong N. Detection of a novel gyrB mutation associated with fluoroquinolone-nonsusceptible Salmonella enterica serovar Typhimurium isolated from a bloodstream infection in Ghana. Clin Infect Dis. 2016;62(suppl_1):S47–9.PubMedCrossRef
16.
go back to reference Aldred KJ, McPherson SA, Wang P, Kerns RJ, Graves DE, Turnbough CL Jr, Osheroff N. Drug interactions with Bacillus anthracis topoisomerase IV: biochemical basis for quinolone action and resistance. Biochemistry. 2011;51(1):370–81.PubMedCrossRef Aldred KJ, McPherson SA, Wang P, Kerns RJ, Graves DE, Turnbough CL Jr, Osheroff N. Drug interactions with Bacillus anthracis topoisomerase IV: biochemical basis for quinolone action and resistance. Biochemistry. 2011;51(1):370–81.PubMedCrossRef
17.
go back to reference Barnard FM, Maxwell A. Interaction between DNA gyrase and quinolones: effects of alanine mutations at GyrA subunit residues Ser83and Asp87. Antimicrob Agents Chemother. 2001;45(7):1994–2000.PubMedPubMedCentralCrossRef Barnard FM, Maxwell A. Interaction between DNA gyrase and quinolones: effects of alanine mutations at GyrA subunit residues Ser83and Asp87. Antimicrob Agents Chemother. 2001;45(7):1994–2000.PubMedPubMedCentralCrossRef
18.
go back to reference Nordmann P, Poirel L. Emergence of plasmid-mediated resistance to quinolones in Enterobacteriaceae. J Antimicrob Chemother. 2005;56(3):463–9.PubMedCrossRef Nordmann P, Poirel L. Emergence of plasmid-mediated resistance to quinolones in Enterobacteriaceae. J Antimicrob Chemother. 2005;56(3):463–9.PubMedCrossRef
20.
go back to reference Kuijpers LM, Phe T, Veng CH, Lim K, Ieng S, Kham C, Fawal N, Fabre L, Le Hello S, Vlieghe E. The clinical and microbiological characteristics of enteric fever in Cambodia, 2008-2015. PLoS Negl Trop Dis. 2017;11(9):e0005964.PubMedPubMedCentralCrossRef Kuijpers LM, Phe T, Veng CH, Lim K, Ieng S, Kham C, Fawal N, Fabre L, Le Hello S, Vlieghe E. The clinical and microbiological characteristics of enteric fever in Cambodia, 2008-2015. PLoS Negl Trop Dis. 2017;11(9):e0005964.PubMedPubMedCentralCrossRef
21.
go back to reference Thanh DP, Karkey A, Dongol S, Thi NH, Thompson CN, Rabaa MA, Arjyal A, Holt KE, Wong V, Thieu NTV. A novel ciprofloxacin-resistant subclade of H58 Salmonella Typhi is associated with fluoroquinolone treatment failure. Elife. 2016;5:e14003.CrossRef Thanh DP, Karkey A, Dongol S, Thi NH, Thompson CN, Rabaa MA, Arjyal A, Holt KE, Wong V, Thieu NTV. A novel ciprofloxacin-resistant subclade of H58 Salmonella Typhi is associated with fluoroquinolone treatment failure. Elife. 2016;5:e14003.CrossRef
22.
go back to reference Hendriksen RS, Leekitcharoenphon P, Lukjancenko O, Lukwesa-Musyani C, Tambatamba B, Mwaba J, Kalonda A, Nakazwe R, Kwenda G, Jensen JD. Genomic signature of multidrug-resistant Salmonella enterica serovar Typhi isolates related to a massive outbreak in Zambia between 2010 and 2012. J Clin Microbiol. 2015;53(1):262–72.PubMedCrossRef Hendriksen RS, Leekitcharoenphon P, Lukjancenko O, Lukwesa-Musyani C, Tambatamba B, Mwaba J, Kalonda A, Nakazwe R, Kwenda G, Jensen JD. Genomic signature of multidrug-resistant Salmonella enterica serovar Typhi isolates related to a massive outbreak in Zambia between 2010 and 2012. J Clin Microbiol. 2015;53(1):262–72.PubMedCrossRef
23.
go back to reference Consortium IT, Wong VK, Holt KE, Okoro C, Baker S, Pickard DJ, Marks F, Page AJ, Olanipekun G, Munir H. Molecular surveillance identifies multiple transmissions of typhoid in West Africa. PLoS Negl Trop Dis. 2016;10(9):e0004781.CrossRef Consortium IT, Wong VK, Holt KE, Okoro C, Baker S, Pickard DJ, Marks F, Page AJ, Olanipekun G, Munir H. Molecular surveillance identifies multiple transmissions of typhoid in West Africa. PLoS Negl Trop Dis. 2016;10(9):e0004781.CrossRef
24.
go back to reference CLSI. Performance standards for antimicrobial susceptibility testing. CLSI supplement M100. 28th ed. Wayne: Clinical and Laboratory Standards Institute; 2018. CLSI. Performance standards for antimicrobial susceptibility testing. CLSI supplement M100. 28th ed. Wayne: Clinical and Laboratory Standards Institute; 2018.
25.
go back to reference Mutai WC. Characterization of antibiotic resistance plasmids in Salmonella enterica serovar Typhi isolated in Nairobi, Kenya. Med Microbiol. 2016:1–139. Mutai WC. Characterization of antibiotic resistance plasmids in Salmonella enterica serovar Typhi isolated in Nairobi, Kenya. Med Microbiol. 2016:1–139.
26.
go back to reference Chau TT, Campbell JI, Galindo CM, Van Minh HN, Diep TS, Nga TT, Van Vinh CN, Tuan PQ, Page AL, Ochiai RL, et al. Antimicrobial drug resistance of Salmonella enterica serovar typhi in asia and molecular mechanism of reduced susceptibility to the fluoroquinolones. Antimicrob Agents Chemother. 2007;51(12):4315–23.PubMedPubMedCentralCrossRef Chau TT, Campbell JI, Galindo CM, Van Minh HN, Diep TS, Nga TT, Van Vinh CN, Tuan PQ, Page AL, Ochiai RL, et al. Antimicrobial drug resistance of Salmonella enterica serovar typhi in asia and molecular mechanism of reduced susceptibility to the fluoroquinolones. Antimicrob Agents Chemother. 2007;51(12):4315–23.PubMedPubMedCentralCrossRef
27.
go back to reference Eaves DJ, Randall L, Gray DT, Buckley A, Woodward MJ, White AP, Piddock LJ. Prevalence of mutations within the quinolone resistance-determining region of gyrA, gyrB, parC, and parE and association with antibiotic resistance in quinolone-resistant Salmonella enterica. Antimicrob Agents Chemother. 2004;48(10):4012–5.PubMedPubMedCentralCrossRef Eaves DJ, Randall L, Gray DT, Buckley A, Woodward MJ, White AP, Piddock LJ. Prevalence of mutations within the quinolone resistance-determining region of gyrA, gyrB, parC, and parE and association with antibiotic resistance in quinolone-resistant Salmonella enterica. Antimicrob Agents Chemother. 2004;48(10):4012–5.PubMedPubMedCentralCrossRef
28.
go back to reference Tadesse G, Tessema TS, Beyene G, Aseffa A. Molecular epidemiology of fluoroquinolone resistant Salmonella in Africa: a systematic review and meta-analysis. PLoS One. 2018;13(2):e0192575.PubMedPubMedCentralCrossRef Tadesse G, Tessema TS, Beyene G, Aseffa A. Molecular epidemiology of fluoroquinolone resistant Salmonella in Africa: a systematic review and meta-analysis. PLoS One. 2018;13(2):e0192575.PubMedPubMedCentralCrossRef
29.
go back to reference Eibach D, Al-Emran HM, Dekker DM, Krumkamp R, Adu-Sarkodie Y, Cruz Espinoza LM, Ehmen C, Boahen K, Heisig P, Im J. The emergence of reduced ciprofloxacin susceptibility in Salmonella enterica causing bloodstream infections in rural Ghana. Clin Infect Dis. 2016;62(suppl_1):S32–6.PubMedCrossRef Eibach D, Al-Emran HM, Dekker DM, Krumkamp R, Adu-Sarkodie Y, Cruz Espinoza LM, Ehmen C, Boahen K, Heisig P, Im J. The emergence of reduced ciprofloxacin susceptibility in Salmonella enterica causing bloodstream infections in rural Ghana. Clin Infect Dis. 2016;62(suppl_1):S32–6.PubMedCrossRef
30.
go back to reference Bae DH, Baek HJ, Jeong SJ, Lee YJ. Amino acid substitutions in gyrA and parC associated with quinolone resistance in nalidixic acid-resistant Salmonella isolates. Ir Vet J. 2013;66(1):23.PubMedPubMedCentralCrossRef Bae DH, Baek HJ, Jeong SJ, Lee YJ. Amino acid substitutions in gyrA and parC associated with quinolone resistance in nalidixic acid-resistant Salmonella isolates. Ir Vet J. 2013;66(1):23.PubMedPubMedCentralCrossRef
31.
go back to reference Lunguya O, Lejon V, Phoba M-F, Bertrand S, Vanhoof R, Glupczynski Y, Verhaegen J, Muyembe-Tamfum J-J, Jacobs J. Antimicrobial resistance in invasive non-typhoid Salmonella from the Democratic Republic of the Congo: emergence of decreased fluoroquinolone susceptibility and extended-spectrum beta lactamases. PLoS Negl Trop Dis. 2013;7(3):e2103.PubMedPubMedCentralCrossRef Lunguya O, Lejon V, Phoba M-F, Bertrand S, Vanhoof R, Glupczynski Y, Verhaegen J, Muyembe-Tamfum J-J, Jacobs J. Antimicrobial resistance in invasive non-typhoid Salmonella from the Democratic Republic of the Congo: emergence of decreased fluoroquinolone susceptibility and extended-spectrum beta lactamases. PLoS Negl Trop Dis. 2013;7(3):e2103.PubMedPubMedCentralCrossRef
32.
go back to reference Ling J, Chan E, Lam A, Cheng A. Mutations in topoisomerase genes of fluoroquinolone-resistant salmonellae in Hong Kong. Antimicrob Agents Chemother. 2003;47(11):3567–73.PubMedPubMedCentralCrossRef Ling J, Chan E, Lam A, Cheng A. Mutations in topoisomerase genes of fluoroquinolone-resistant salmonellae in Hong Kong. Antimicrob Agents Chemother. 2003;47(11):3567–73.PubMedPubMedCentralCrossRef
33.
go back to reference Al-Emran HM, Eibach D, Krumkamp R, Ali M, Baker S, Biggs HM, Bjerregaard-Andersen M, Breiman RF, Clemens JD, Crump JA. A multicountry molecular analysis of Salmonella enterica serovar Typhi with reduced susceptibility to ciprofloxacin in sub-Saharan Africa. Clin Infect Dis. 2016;62(suppl_1):S42–6.PubMedPubMedCentralCrossRef Al-Emran HM, Eibach D, Krumkamp R, Ali M, Baker S, Biggs HM, Bjerregaard-Andersen M, Breiman RF, Clemens JD, Crump JA. A multicountry molecular analysis of Salmonella enterica serovar Typhi with reduced susceptibility to ciprofloxacin in sub-Saharan Africa. Clin Infect Dis. 2016;62(suppl_1):S42–6.PubMedPubMedCentralCrossRef
34.
go back to reference Zayed AA-F, Essam TM, Hashem A-GM, El-Tayeb OM. ‘Supermutators’ found amongst highly levofloxacin-resistant E. coli isolates: a rapid protocol for the detection of mutation sites. Emerg Microb Infect. 2015;4(1):1–8.CrossRef Zayed AA-F, Essam TM, Hashem A-GM, El-Tayeb OM. ‘Supermutators’ found amongst highly levofloxacin-resistant E. coli isolates: a rapid protocol for the detection of mutation sites. Emerg Microb Infect. 2015;4(1):1–8.CrossRef
35.
go back to reference Threlfall EJ. Antimicrobial drug resistance in Salmonella: problems and perspectives in food-and water-borne infections. FEMS Microbiol Rev. 2002;26(2):141–8.PubMedCrossRef Threlfall EJ. Antimicrobial drug resistance in Salmonella: problems and perspectives in food-and water-borne infections. FEMS Microbiol Rev. 2002;26(2):141–8.PubMedCrossRef
36.
go back to reference Andoh LA, Dalsgaard A, Obiri-Danso K, Newman M, Barco L, Olsen JE. Prevalence and antimicrobial resistance of Salmonella serovars isolated from poultry in Ghana. Epidemiol Infect. 2016;144(15):3288–99.PubMedCrossRef Andoh LA, Dalsgaard A, Obiri-Danso K, Newman M, Barco L, Olsen JE. Prevalence and antimicrobial resistance of Salmonella serovars isolated from poultry in Ghana. Epidemiol Infect. 2016;144(15):3288–99.PubMedCrossRef
37.
go back to reference Dekker D, Eibach D, Boahen KG, Akenten CW, Pfeifer Y, Zautner AE, Mertens E, Krumkamp R, Jaeger A, Flieger A. Fluoroquinolone-resistant Salmonella enterica, Campylobacter spp., and Arcobacter butzleri from local and imported poultry meat in Kumasi, Ghana. Foodborne Pathog Dis. 2019;16(5):352–8.PubMedPubMedCentralCrossRef Dekker D, Eibach D, Boahen KG, Akenten CW, Pfeifer Y, Zautner AE, Mertens E, Krumkamp R, Jaeger A, Flieger A. Fluoroquinolone-resistant Salmonella enterica, Campylobacter spp., and Arcobacter butzleri from local and imported poultry meat in Kumasi, Ghana. Foodborne Pathog Dis. 2019;16(5):352–8.PubMedPubMedCentralCrossRef
38.
go back to reference Gunell M, Webber MA, Kotilainen P, Lilly AJ, Caddick JM, Jalava J, Huovinen P, Siitonen A, Hakanen AJ, Piddock LJ. Mechanisms of resistance in nontyphoidal Salmonella enterica strains exhibiting a nonclassical quinolone resistance phenotype. Antimicrob Agents Chemother. 2009;53(9):3832–6.PubMedPubMedCentralCrossRef Gunell M, Webber MA, Kotilainen P, Lilly AJ, Caddick JM, Jalava J, Huovinen P, Siitonen A, Hakanen AJ, Piddock LJ. Mechanisms of resistance in nontyphoidal Salmonella enterica strains exhibiting a nonclassical quinolone resistance phenotype. Antimicrob Agents Chemother. 2009;53(9):3832–6.PubMedPubMedCentralCrossRef
39.
go back to reference Murray A, Mather H, Coia J, Brown D. Plasmid-mediated quinolone resistance in nalidixic-acid-susceptible strains of Salmonella enterica isolated in Scotland. J Antimicrob Chemother. 2008;62(5):1153–5.PubMedCrossRef Murray A, Mather H, Coia J, Brown D. Plasmid-mediated quinolone resistance in nalidixic-acid-susceptible strains of Salmonella enterica isolated in Scotland. J Antimicrob Chemother. 2008;62(5):1153–5.PubMedCrossRef
40.
go back to reference Govender N, Smith AM, Karstaedt AS, Keddy KH. Plasmid-mediated quinolone resistance in Salmonella from South Africa. J Med Microbiol. 2009;58(10):1393–4.PubMedCrossRef Govender N, Smith AM, Karstaedt AS, Keddy KH. Plasmid-mediated quinolone resistance in Salmonella from South Africa. J Med Microbiol. 2009;58(10):1393–4.PubMedCrossRef
41.
go back to reference Veldman K, Cavaco LM, Mevius D, Battisti A, Franco A, Botteldoorn N, Bruneau M, Perrin-Guyomard A, Cerny T, De Frutos EC. International collaborative study on the occurrence of plasmid-mediated quinolone resistance in Salmonella enterica and Escherichia coli isolated from animals, humans, food and the environment in 13 European countries. J Antimicrob Chemother. 2011;66(6):1278–86.PubMedCrossRef Veldman K, Cavaco LM, Mevius D, Battisti A, Franco A, Botteldoorn N, Bruneau M, Perrin-Guyomard A, Cerny T, De Frutos EC. International collaborative study on the occurrence of plasmid-mediated quinolone resistance in Salmonella enterica and Escherichia coli isolated from animals, humans, food and the environment in 13 European countries. J Antimicrob Chemother. 2011;66(6):1278–86.PubMedCrossRef
42.
go back to reference García-Fernández A, Fortini D, Veldman K, Mevius D, Carattoli A. Characterization of plasmids harbouring qnrS1, qnrB2 and qnrB19 genes in Salmonella. J Antimicrob Chemother. 2008;63(2):274–81.PubMedCrossRef García-Fernández A, Fortini D, Veldman K, Mevius D, Carattoli A. Characterization of plasmids harbouring qnrS1, qnrB2 and qnrB19 genes in Salmonella. J Antimicrob Chemother. 2008;63(2):274–81.PubMedCrossRef
43.
go back to reference Dionisi AM, Graziani C, Lucarelli C, Filetici E, Villa L, Owczarek S, Caprioli A, Luzzi I. Molecular characterization of multidrug-resistant strains of Salmonella enterica serotype Typhimurium and monophasic variant (S. 4,[5], 12: i:–) isolated from human infections in Italy. Foodborne Pathog Dis. 2009;6(6):711–7.PubMedCrossRef Dionisi AM, Graziani C, Lucarelli C, Filetici E, Villa L, Owczarek S, Caprioli A, Luzzi I. Molecular characterization of multidrug-resistant strains of Salmonella enterica serotype Typhimurium and monophasic variant (S. 4,[5], 12: i:–) isolated from human infections in Italy. Foodborne Pathog Dis. 2009;6(6):711–7.PubMedCrossRef
44.
go back to reference Frye JG, Jackson CR. Genetic mechanisms of antimicrobial resistance identified in Salmonella enterica, Escherichia coli, and Enteroccocus spp. isolated from US food animals. Front Microbiol. 2013;4:135.PubMedPubMedCentralCrossRef Frye JG, Jackson CR. Genetic mechanisms of antimicrobial resistance identified in Salmonella enterica, Escherichia coli, and Enteroccocus spp. isolated from US food animals. Front Microbiol. 2013;4:135.PubMedPubMedCentralCrossRef
45.
go back to reference Cavaco L, Korsgaard H, Sørensen G, Aarestrup FM. Plasmid-mediated quinolone resistance due to qnrB5 and qnrS1 genes in Salmonella enterica serovars Newport, Hadar and Saintpaul isolated from Turkey meat in Denmark. J Antimicrob Chemother. 2008;62(3):632–4.PubMedCrossRef Cavaco L, Korsgaard H, Sørensen G, Aarestrup FM. Plasmid-mediated quinolone resistance due to qnrB5 and qnrS1 genes in Salmonella enterica serovars Newport, Hadar and Saintpaul isolated from Turkey meat in Denmark. J Antimicrob Chemother. 2008;62(3):632–4.PubMedCrossRef
46.
go back to reference Colomer-Lluch M, Jofre J, Muniesa M. Quinolone resistance genes (qnrA and qnrS) in bacteriophage particles from wastewater samples and the effect of inducing agents on packaged antibiotic resistance genes. J Antimicrob Chemother. 2014;69(5):1265–74.PubMedCrossRef Colomer-Lluch M, Jofre J, Muniesa M. Quinolone resistance genes (qnrA and qnrS) in bacteriophage particles from wastewater samples and the effect of inducing agents on packaged antibiotic resistance genes. J Antimicrob Chemother. 2014;69(5):1265–74.PubMedCrossRef
47.
go back to reference Hopkins KL, Wootton L, Day MR, Threlfall EJ. Plasmid-mediated quinolone resistance determinant qnrS1 found in Salmonella enterica strains isolated in the UK. J Antimicrob Chemother. 2007;59(6):1071–5.PubMedCrossRef Hopkins KL, Wootton L, Day MR, Threlfall EJ. Plasmid-mediated quinolone resistance determinant qnrS1 found in Salmonella enterica strains isolated in the UK. J Antimicrob Chemother. 2007;59(6):1071–5.PubMedCrossRef
48.
go back to reference Jacoby GA. Plasmid-mediated quinolone resistance. In: Antimicrobial Drug Resistance. Berlin: Springer; 2017. p. 265–8.CrossRef Jacoby GA. Plasmid-mediated quinolone resistance. In: Antimicrobial Drug Resistance. Berlin: Springer; 2017. p. 265–8.CrossRef
49.
go back to reference Martínez-Martínez L, Pascual A, Jacoby GA. Quinolone resistance from a transferable plasmid. Lancet. 1998;351(9105):797–9.PubMedCrossRef Martínez-Martínez L, Pascual A, Jacoby GA. Quinolone resistance from a transferable plasmid. Lancet. 1998;351(9105):797–9.PubMedCrossRef
Metadata
Title
Chromosomal and plasmid-mediated fluoroquinolone resistance in human Salmonella enterica infection in Ghana
Authors
Godfred Acheampong
Michael Owusu
Alex Owusu-Ofori
Isaac Osei
Nimako Sarpong
Augustina Sylverken
Hung-Jui Kung
Shu-Ting Cho
Chih-Horng Kuo
Se Eun Park
Florian Marks
Yaw Adu-Sarkodie
Ellis Owusu-Dabo
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2019
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-019-4522-1

Other articles of this Issue 1/2019

BMC Infectious Diseases 1/2019 Go to the issue
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.