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Open Access 01-12-2017 | Research

Newest data on fluoroquinolone resistance mechanism of Shigella flexneri isolates in Jiangsu Province of China

Authors: Tingting Qin, Huimin Qian, Wenting Fan, Ping Ma, Lu Zhou, Chen Dong, Bing Gu, Xiang Huo

Published in: Antimicrobial Resistance & Infection Control | Issue 1/2017

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Abstract

Background

To determine the prevalence, antimicrobial susceptibility patterns and related presence of mutations in quinolone resistance-determining region (QRDR) genes and plasmid-mediated quinolone resistance (PMQR) among Shigella flexneri isolates obtained from Jiangsu Province, China.

Methods

A total of 400 Shigella flexneri clinical isolates collected during 2012–2015 were identified by biochemical and serological methods, and the antimicrobial susceptibility pattern was evaluated using the disc-diffusion method. PCR and DNA sequencing were accomplished to identify mutations in gyrA, gyrB, parC and parE, and the presence of qnrA, qnrB, qnrC, qnrD, qnrS, qepA and aac(6′)-Ib-cr genes were also detected.

Results

Of all the Shigella flexneri, 75.8% were resistant to nalidixic acid, and 37.0% were categorized as norfloxacin resistant. Overall, 75.5% of isolates possessed gyrA mutations (Ser83Leu, Asp87Gly/Asn and His211Tyr), while 84.3% had parC mutations (Ser80Ile, Ala81Pho, Gln91His and Ser129Pro). The most prevalent point mutations in gyrA and parC were Ser83Leu (75.5%, 302/400) and Ser80Ile (74.5%, 298/400), relatively. Besides, the Gln517Arg alternation in gyrB was detected in 13 S. flexneri isolates and no mutations were identified in parE. PMQR determinations of qnrB, qnrS and aac(6′)-Ib-cr were detected among 16 strains (4.0%).

Conclusions

The results presented here show that fluoroquinolone resistance in these clinical isolates result from mutations in chromosome, besides, despite the low prevalence of PMQR determinants in Jiangsu, it is essential to continue surveillance PMQR determinants in this area.
Literature
1.
go back to reference Liu L, Johnson HL, Cousens S, Perin J, Scott S, Lawn JE, et al. Global, regional, and national causes of child mortality: an updated systematic analysis for 2010 with time trends since 2000. Lancet. 2012;379(9832):2151–61.CrossRefPubMed Liu L, Johnson HL, Cousens S, Perin J, Scott S, Lawn JE, et al. Global, regional, and national causes of child mortality: an updated systematic analysis for 2010 with time trends since 2000. Lancet. 2012;379(9832):2151–61.CrossRefPubMed
2.
go back to reference Wang XY, Tao F, Xiao D, Lee H, Deen J, Gong J, et al. Trend and disease burden of bacillary in China (1991-2000). Bull World Health Organ. 2006;84(7):561–8.CrossRefPubMedPubMedCentral Wang XY, Tao F, Xiao D, Lee H, Deen J, Gong J, et al. Trend and disease burden of bacillary in China (1991-2000). Bull World Health Organ. 2006;84(7):561–8.CrossRefPubMedPubMedCentral
3.
go back to reference Walker CL, Rudan I, Liu L, Nair H, Theodoratou E, Bhutta ZA, et al. Global burden of childhood pneumonia and diarrhoea. Lancet. 2013;381(9875):1405–16.CrossRefPubMed Walker CL, Rudan I, Liu L, Nair H, Theodoratou E, Bhutta ZA, et al. Global burden of childhood pneumonia and diarrhoea. Lancet. 2013;381(9875):1405–16.CrossRefPubMed
5.
go back to reference Livio S, Strockbine NA, Panchalingam S, Tennant SM, Barry EM, Marohn ME, et al. Shigella isolates from the global enteric multicenter study inform vaccine development. Clin Infect Dis. 2014;59(7):933–41.CrossRefPubMedPubMedCentral Livio S, Strockbine NA, Panchalingam S, Tennant SM, Barry EM, Marohn ME, et al. Shigella isolates from the global enteric multicenter study inform vaccine development. Clin Infect Dis. 2014;59(7):933–41.CrossRefPubMedPubMedCentral
6.
go back to reference Yang H, Chen G, Zhu Y, Liu Y, Cheng J, Hu L, et al. Surveillance of antimicrobial susceptibility patterns among Shigella species isolated in China during the 7-year period of 2005-2011. Ann Lab Med. 2013;33(2):111–5.CrossRefPubMedPubMedCentral Yang H, Chen G, Zhu Y, Liu Y, Cheng J, Hu L, et al. Surveillance of antimicrobial susceptibility patterns among Shigella species isolated in China during the 7-year period of 2005-2011. Ann Lab Med. 2013;33(2):111–5.CrossRefPubMedPubMedCentral
7.
go back to reference Qin T, Bi R, Fan W, Kang H, Ma P, Gu B. Novel mutations in quinolone resistance-determining regions of gyrA, gyrB, parC and parE in Shigella flexneri clinical isolates from eastern Chinese populations between 2001 and 2011. Eur J Clin Microbiol Infect Dis. 2016;35(12):2037–45.CrossRefPubMed Qin T, Bi R, Fan W, Kang H, Ma P, Gu B. Novel mutations in quinolone resistance-determining regions of gyrA, gyrB, parC and parE in Shigella flexneri clinical isolates from eastern Chinese populations between 2001 and 2011. Eur J Clin Microbiol Infect Dis. 2016;35(12):2037–45.CrossRefPubMed
8.
go back to reference Fàbrega A, Madurga S, Giralt E, Vila J. Mechanism of action of and resistance to quinolones. Microb Biotechnol. 2009;2(1):40–61.CrossRefPubMed Fàbrega A, Madurga S, Giralt E, Vila J. Mechanism of action of and resistance to quinolones. Microb Biotechnol. 2009;2(1):40–61.CrossRefPubMed
9.
go back to reference Ruiz J. Mechanisms of resistance to quinolones: target alterations, decreased accumulation and DNA gyrase protection. J Antimicrob Chemother. 2003;51(5):1109–17.CrossRefPubMed Ruiz J. Mechanisms of resistance to quinolones: target alterations, decreased accumulation and DNA gyrase protection. J Antimicrob Chemother. 2003;51(5):1109–17.CrossRefPubMed
10.
go back to reference Clinical and Laboratory Standards Institute. Methods for dilution and antimicrobial susceptibility tests for bacteria that grow aerobically, 9th ed. Approved standard M07-A9. Clinical and Laboratory Standards Institute, 2012. Wayne, PA. Clinical and Laboratory Standards Institute. Methods for dilution and antimicrobial susceptibility tests for bacteria that grow aerobically, 9th ed. Approved standard M07-A9. Clinical and Laboratory Standards Institute, 2012. Wayne, PA.
11.
go back to reference Rahman M, Mauff G, Levy J, Couturier M, Pulverer G, Glasdorff N, et al. Detection of 4-quinolone resistance mutation in gyrA gene of Shigella dysenteriae type 1 by PCR. Antimicrob Agents Chemother. 1994;38(10):2488–91.CrossRefPubMedPubMedCentral Rahman M, Mauff G, Levy J, Couturier M, Pulverer G, Glasdorff N, et al. Detection of 4-quinolone resistance mutation in gyrA gene of Shigella dysenteriae type 1 by PCR. Antimicrob Agents Chemother. 1994;38(10):2488–91.CrossRefPubMedPubMedCentral
12.
go back to reference Chau TT, Campbell JI, Galindo CM, Van Minh HN, Diep TS, Nga TT, 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.CrossRefPubMedPubMedCentral Chau TT, Campbell JI, Galindo CM, Van Minh HN, Diep TS, Nga TT, 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.CrossRefPubMedPubMedCentral
13.
go back to reference Dutta S, Kawamura Y, Ezaki T, Nair GB, Iida K, Yoshida S. Alteration in the GyrA subunit of DNA gyrase and the ParC subunit of topoisomerase IV in quinolone-resistant Shigella dysenteriae serotype 1 clinical isolates from Kolkata. India Antimicrob Agents Chemother. 2005;49(4):1660–1.CrossRefPubMed Dutta S, Kawamura Y, Ezaki T, Nair GB, Iida K, Yoshida S. Alteration in the GyrA subunit of DNA gyrase and the ParC subunit of topoisomerase IV in quinolone-resistant Shigella dysenteriae serotype 1 clinical isolates from Kolkata. India Antimicrob Agents Chemother. 2005;49(4):1660–1.CrossRefPubMed
14.
go back to reference Robicsek A, Strahilevitz J, Sahm DF, Jacoby GA, Hooper DC. qnr prevalence in ceftazidime-resistant Enterobacteriaceae isolates from the United States. Antimicrob Agents Chemother. 2006;50(8):2872–4.CrossRefPubMedPubMedCentral Robicsek A, Strahilevitz J, Sahm DF, Jacoby GA, Hooper DC. qnr prevalence in ceftazidime-resistant Enterobacteriaceae isolates from the United States. Antimicrob Agents Chemother. 2006;50(8):2872–4.CrossRefPubMedPubMedCentral
15.
go back to reference Wang M, Guo Q, Xu X, Wang X, Ye X, Wu S, et al. New plasmid-mediated quinolone resistance gene, qnrC, found in a clinical isolate of Proteus mirabilis. Antimicrob Agents Chemother. 2009;53(5):1892–7.CrossRefPubMedPubMedCentral Wang M, Guo Q, Xu X, Wang X, Ye X, Wu S, et al. New plasmid-mediated quinolone resistance gene, qnrC, found in a clinical isolate of Proteus mirabilis. Antimicrob Agents Chemother. 2009;53(5):1892–7.CrossRefPubMedPubMedCentral
16.
go back to reference Cavaco LM, Hasman H, Xia S, Aarestrup FM. qnrD, a novel gene conferring transferable quinolone resistance in salmonella enterica serovar Kentucky and Bovismorbificans strains of human origin. Antimicrob Agents Chemother. 2009;53(2):603–8.CrossRefPubMed Cavaco LM, Hasman H, Xia S, Aarestrup FM. qnrD, a novel gene conferring transferable quinolone resistance in salmonella enterica serovar Kentucky and Bovismorbificans strains of human origin. Antimicrob Agents Chemother. 2009;53(2):603–8.CrossRefPubMed
17.
go back to reference Pu XY, Pan JC, Wang HQ, Zhang W, Huang ZC, Gu YM. Characterization of fluoroquinolone-resistant Shigella flexneri in Hangzhou area of China. J Antimicrob Chemother. 2009;63(5):917–20.CrossRefPubMed Pu XY, Pan JC, Wang HQ, Zhang W, Huang ZC, Gu YM. Characterization of fluoroquinolone-resistant Shigella flexneri in Hangzhou area of China. J Antimicrob Chemother. 2009;63(5):917–20.CrossRefPubMed
18.
go back to reference Yamane K, Wachino J, Suzuki S, Arakawa Y. Plasmid-mediated qepA gene among Escherichia coli clinical isolates from Japan. Antimicrob Agents Chemother. 2008;52(4):1564–6.CrossRefPubMedPubMedCentral Yamane K, Wachino J, Suzuki S, Arakawa Y. Plasmid-mediated qepA gene among Escherichia coli clinical isolates from Japan. Antimicrob Agents Chemother. 2008;52(4):1564–6.CrossRefPubMedPubMedCentral
19.
go back to reference Chang Z, Lu S, Chen L, Jin Q, Yang J. Causative species and serotypes of shigellosis in mainland China: systematic review and meta-analysis. PLoS One. 2012;7(12):e52515.CrossRefPubMedPubMedCentral Chang Z, Lu S, Chen L, Jin Q, Yang J. Causative species and serotypes of shigellosis in mainland China: systematic review and meta-analysis. PLoS One. 2012;7(12):e52515.CrossRefPubMedPubMedCentral
20.
go back to reference Mao Y, Cui E, Bao C, Liu Z, Chen S, Zhang J, et al. Changing trends and serotype distribution of Shigella species in Beijing from 1994 to 2010. Gut Pathog. 2013;5:21.CrossRefPubMedPubMedCentral Mao Y, Cui E, Bao C, Liu Z, Chen S, Zhang J, et al. Changing trends and serotype distribution of Shigella species in Beijing from 1994 to 2010. Gut Pathog. 2013;5:21.CrossRefPubMedPubMedCentral
21.
go back to reference Ud-Din AI, Wahid SU, Latif HA, Shahnaij M, Akter M, Azmi IJ, et al. Changing trends in the prevalence of Shigella species: emergence of multi-drug resistant Shigella sonnei biotype g in Bangladesh. PLoS One. 2013;8(21):e82601.CrossRefPubMedPubMedCentral Ud-Din AI, Wahid SU, Latif HA, Shahnaij M, Akter M, Azmi IJ, et al. Changing trends in the prevalence of Shigella species: emergence of multi-drug resistant Shigella sonnei biotype g in Bangladesh. PLoS One. 2013;8(21):e82601.CrossRefPubMedPubMedCentral
22.
go back to reference von Seidlein L, Kim DR, Ali M, Lee H, Wang X, Thiem VD, et al. A multicentre study of Shigella diarrhoea in six Asian countries: disease burden, clinical manifestations, and microbiology. PLoS Med. 2006;3(9):e353.CrossRef von Seidlein L, Kim DR, Ali M, Lee H, Wang X, Thiem VD, et al. A multicentre study of Shigella diarrhoea in six Asian countries: disease burden, clinical manifestations, and microbiology. PLoS Med. 2006;3(9):e353.CrossRef
23.
go back to reference Zhang J, Jin H, Hu J, Yuan Z, Shi W, Yang X, et al. Antimicrobial resistance of Shigella spp. from humans in shanghai, China, 2004-2011. Diagn Microbiol Infect Dis. 2014;78(3):282–6.CrossRefPubMed Zhang J, Jin H, Hu J, Yuan Z, Shi W, Yang X, et al. Antimicrobial resistance of Shigella spp. from humans in shanghai, China, 2004-2011. Diagn Microbiol Infect Dis. 2014;78(3):282–6.CrossRefPubMed
25.
go back to reference Xu Y, Zhuang L, Kang H, Ma P, Xu T, Pan S, et al. Prevalence, resistance patterns, and characterization of integrons of Shigella flexneri isolated from Jiangsu Province in China, 2001-2011. Eur J Clin Microbiol Infect Dis. 2016;35(8):1347–53.CrossRefPubMed Xu Y, Zhuang L, Kang H, Ma P, Xu T, Pan S, et al. Prevalence, resistance patterns, and characterization of integrons of Shigella flexneri isolated from Jiangsu Province in China, 2001-2011. Eur J Clin Microbiol Infect Dis. 2016;35(8):1347–53.CrossRefPubMed
26.
go back to reference Nüesch-Inderbinen M, Heini N, Zurfluh K, Althaus D, Hächler H, Stephan R. Shigella antimicrobial drug resistance mechanisms, 2004-2014. Emerg Infect Dis. 2016;22(6):1083–5.CrossRefPubMedPubMedCentral Nüesch-Inderbinen M, Heini N, Zurfluh K, Althaus D, Hächler H, Stephan R. Shigella antimicrobial drug resistance mechanisms, 2004-2014. Emerg Infect Dis. 2016;22(6):1083–5.CrossRefPubMedPubMedCentral
27.
go back to reference Yang H, Duan G, Zhu J, Zhang W, Xi Y, Fan Q. Prevalence and characterisation of plasmid-mediated quinolone resistance and mutations in the gyrase and topoisomerase IV genes among Shigella isolates from Henan, China, between 2001 and 2008. Int J Antimicrob Agents. 2013;42(2):173–7.CrossRefPubMed Yang H, Duan G, Zhu J, Zhang W, Xi Y, Fan Q. Prevalence and characterisation of plasmid-mediated quinolone resistance and mutations in the gyrase and topoisomerase IV genes among Shigella isolates from Henan, China, between 2001 and 2008. Int J Antimicrob Agents. 2013;42(2):173–7.CrossRefPubMed
28.
go back to reference Zhu YL, Yang HF, Liu YY, Hu LF, Cheng J, Ye Y, et al. Detection of plasmid-mediated quinolone resistance determinants and the emergence of multidrug resistance in clinical isolates of Shigella in SiXian area. China Diagn Microbiol Infect Dis. 2013;75(3):327–9.CrossRefPubMed Zhu YL, Yang HF, Liu YY, Hu LF, Cheng J, Ye Y, et al. Detection of plasmid-mediated quinolone resistance determinants and the emergence of multidrug resistance in clinical isolates of Shigella in SiXian area. China Diagn Microbiol Infect Dis. 2013;75(3):327–9.CrossRefPubMed
29.
go back to reference Yang C, Li P, Zhang X, Ma Q, Cui X, Li H, et al. Molecular characterization and analysis of high-level multidrug-resistance of Shigella flexneri serotype 4s strains from China. Sci Rep. 2016;6:29124.CrossRefPubMedPubMedCentral Yang C, Li P, Zhang X, Ma Q, Cui X, Li H, et al. Molecular characterization and analysis of high-level multidrug-resistance of Shigella flexneri serotype 4s strains from China. Sci Rep. 2016;6:29124.CrossRefPubMedPubMedCentral
30.
go back to reference Bhattacharya D, Bhattacharya H, Thamizhmani R, Sayi DS, Reesu R, Anwesh M, et al. Shigellosis in bay of Bengal Islands, India: clinical and seasonal patterns, surveillance of antibiotic susceptibility patterns, and molecular characterization of multidrug-resistant Shigella strains isolated during a 6-year period from 2006 to 2011. Eur J Clin Microbiol Infect Dis. 2014;33(2):157–70.CrossRefPubMed Bhattacharya D, Bhattacharya H, Thamizhmani R, Sayi DS, Reesu R, Anwesh M, et al. Shigellosis in bay of Bengal Islands, India: clinical and seasonal patterns, surveillance of antibiotic susceptibility patterns, and molecular characterization of multidrug-resistant Shigella strains isolated during a 6-year period from 2006 to 2011. Eur J Clin Microbiol Infect Dis. 2014;33(2):157–70.CrossRefPubMed
31.
go back to reference Liu Y, Hu L, Pan Y, Cheng J, Zhu Y, Ye Y, et al. Prevalence of plasmid-mediated quinolone resistance determinants in association with beta-lactamases, 16S rRNA methylase genes and integrons amongst clinical isolates of Shigella flexneri. J Med Microbiol. 2012;61(Pt 8):1174–6.CrossRefPubMed Liu Y, Hu L, Pan Y, Cheng J, Zhu Y, Ye Y, et al. Prevalence of plasmid-mediated quinolone resistance determinants in association with beta-lactamases, 16S rRNA methylase genes and integrons amongst clinical isolates of Shigella flexneri. J Med Microbiol. 2012;61(Pt 8):1174–6.CrossRefPubMed
32.
go back to reference Pu XY, Pan JC, Zhang W, Zheng W, Wang HQ, Gu YM. Quinolone resistance-determining region mutations and the plasmid-mediated quinolone resistance gene qnrS played important roles in decreased susceptibility to fluoroquinolones among Shigella isolates in southeast China between 1998 and 2013. Int J Antimicrob Agents. 2015;45(4):438–9.CrossRefPubMed Pu XY, Pan JC, Zhang W, Zheng W, Wang HQ, Gu YM. Quinolone resistance-determining region mutations and the plasmid-mediated quinolone resistance gene qnrS played important roles in decreased susceptibility to fluoroquinolones among Shigella isolates in southeast China between 1998 and 2013. Int J Antimicrob Agents. 2015;45(4):438–9.CrossRefPubMed
33.
go back to reference Xiong Z, Li J, Li T, Shen J, Hu F, Wang M. Prevalence of plasmid-mediated quinolone-resistance determinants in Shigella flexneri isolates from Anhui Province, China. J Antibiot (Tokyo). 2010;63(4):187–9.CrossRef Xiong Z, Li J, Li T, Shen J, Hu F, Wang M. Prevalence of plasmid-mediated quinolone-resistance determinants in Shigella flexneri isolates from Anhui Province, China. J Antibiot (Tokyo). 2010;63(4):187–9.CrossRef
34.
go back to reference Thompson CN, Thieu NT, Vinh PV, Duc AN, Wolbers M, Vinh H, et al. Clinical implications of reduced susceptibility to fluoroquinolones in paediatric Shigella sonnei and Shigella flexneri infections. J Antimicrob Chemother. 2016;71(3):807–15.CrossRefPubMed Thompson CN, Thieu NT, Vinh PV, Duc AN, Wolbers M, Vinh H, et al. Clinical implications of reduced susceptibility to fluoroquinolones in paediatric Shigella sonnei and Shigella flexneri infections. J Antimicrob Chemother. 2016;71(3):807–15.CrossRefPubMed
Metadata
Title
Newest data on fluoroquinolone resistance mechanism of Shigella flexneri isolates in Jiangsu Province of China
Authors
Tingting Qin
Huimin Qian
Wenting Fan
Ping Ma
Lu Zhou
Chen Dong
Bing Gu
Xiang Huo
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Antimicrobial Resistance & Infection Control / Issue 1/2017
Electronic ISSN: 2047-2994
DOI
https://doi.org/10.1186/s13756-017-0249-1

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