Skip to main content
Top
Published in: BMC Infectious Diseases 1/2011

Open Access 01-12-2011 | Research article

The antimicrobial resistance patterns and associated determinants in Streptococcus suisisolated from humans in southern Vietnam, 1997-2008

Authors: Ngo T Hoa, Tran TB Chieu, Ho DT Nghia, Nguyen TH Mai, Pham H Anh, Marcel Wolbers, Stephen Baker, James I Campbell, Nguyen VV Chau, Tran T Hien, Jeremy Farrar, Constance Schultsz

Published in: BMC Infectious Diseases | Issue 1/2011

Login to get access

Abstract

Background

Streptococcus suis is an emerging zoonotic pathogen and is the leading cause of bacterial meningitis in adults in Vietnam. Systematic data on the antimicrobial susceptibility profiles of S. suis strains isolated from human cases are lacking. We studied antimicrobial resistance and associated resistance determinants in S. suis isolated from patients with meningitis in southern Vietnam.

Methods

S. suis strains isolated between 1997 and 2008 were investigated for their susceptibility to six antimicrobial agents. Strains were screened for the presence and expression of tetracycline and erythromycin resistance determinants and the association of tet(M) genes with Tn916- like transposons. The localization of tetracycline resistance gene tet(L) was determined by pulse field gel electrophoresis and Southern blotting.

Results

We observed a significant increase in resistance to tetracycline and chloramphenicol, which was concurrent with an increase in multi-drug resistance. In tetracycline resistance strains, we identified tet(M), tet(O), tet(W) and tet(L) and confirmed their expression. All tet(M) genes were associated with a Tn916-like transposon. The co-expression of tet(L) and other tetracycline resistance gene(s) encoding for ribosomal protection protein(s) was only detected in strains with a minimum inhibitory concentration (MIC) of tetracycline of ≥ 64 mg/L

Conclusions

We demonstrated that multi-drug resistance in S. suis causing disease in humans in southern Vietnam has increased over the 11-year period studied. We report the presence and expression of tet(L) in S. suis strains and our data suggest that co-expression of multiple genes encoding distinct mechanism is required for an MIC ≥ 64 mg/L to tetracycline.
Appendix
Available only for authorised users
Literature
1.
go back to reference Wertheim HF, Nghia HD, Taylor W, Schultsz C: Streptococcus suis: an emerging human pathogen. Clin Infect Dis. 2009, 48 (5): 617-625. 10.1086/596763.CrossRefPubMed Wertheim HF, Nghia HD, Taylor W, Schultsz C: Streptococcus suis: an emerging human pathogen. Clin Infect Dis. 2009, 48 (5): 617-625. 10.1086/596763.CrossRefPubMed
2.
go back to reference Yu H, Jing H, Chen Z, Zheng H, Zhu X, Wang H, Wang S, Liu L, Zu R, Luo L, et al: Human Streptococcus suis outbreak, Sichuan, China. Emerg Infect Dis. 2006, 12 (6): 914-920.CrossRefPubMedPubMedCentral Yu H, Jing H, Chen Z, Zheng H, Zhu X, Wang H, Wang S, Liu L, Zu R, Luo L, et al: Human Streptococcus suis outbreak, Sichuan, China. Emerg Infect Dis. 2006, 12 (6): 914-920.CrossRefPubMedPubMedCentral
3.
go back to reference Gottschalk M, Segura M, Xu J: Streptococcus suis infections in humans: the Chinese experience and the situation in North America. Anim Health Res Rev. 2007, 8 (1): 29-45. 10.1017/S1466252307001247.CrossRefPubMed Gottschalk M, Segura M, Xu J: Streptococcus suis infections in humans: the Chinese experience and the situation in North America. Anim Health Res Rev. 2007, 8 (1): 29-45. 10.1017/S1466252307001247.CrossRefPubMed
4.
go back to reference Mai NT, Hoa NT, Nga TV, Linh le D, Chau TT, Sinh DX, Phu NH, Chuong LV, Diep TS, Campbell J, et al: Streptococcus suis meningitis in adults in Vietnam. Clin Infect Dis. 2008, 46 (5): 659-667. 10.1086/527385.CrossRefPubMed Mai NT, Hoa NT, Nga TV, Linh le D, Chau TT, Sinh DX, Phu NH, Chuong LV, Diep TS, Campbell J, et al: Streptococcus suis meningitis in adults in Vietnam. Clin Infect Dis. 2008, 46 (5): 659-667. 10.1086/527385.CrossRefPubMed
5.
go back to reference Wertheim HF, Nguyen HN, Taylor W, Lien TT, Ngo HT, Nguyen TQ, Nguyen BN, Nguyen HH, Nguyen HM, Nguyen CT, et al: Streptococcus suis, an important cause of adult bacterial meningitis in northern Vietnam. PLoS One. 2009, 4 (6): e5973-10.1371/journal.pone.0005973.CrossRefPubMedPubMedCentral Wertheim HF, Nguyen HN, Taylor W, Lien TT, Ngo HT, Nguyen TQ, Nguyen BN, Nguyen HH, Nguyen HM, Nguyen CT, et al: Streptococcus suis, an important cause of adult bacterial meningitis in northern Vietnam. PLoS One. 2009, 4 (6): e5973-10.1371/journal.pone.0005973.CrossRefPubMedPubMedCentral
6.
go back to reference Chang B, Wada A, Ikebe T, Ohnishi M, Mita K, Endo M, Matsuo H, Asatuma Y, Kuramoto S, Sekiguchi H, et al: Characteristics of Streptococcus suis isolated from patients in Japan. Jpn J Infect Dis. 2006, 59 (6): 397-399.PubMed Chang B, Wada A, Ikebe T, Ohnishi M, Mita K, Endo M, Matsuo H, Asatuma Y, Kuramoto S, Sekiguchi H, et al: Characteristics of Streptococcus suis isolated from patients in Japan. Jpn J Infect Dis. 2006, 59 (6): 397-399.PubMed
7.
go back to reference Chu YW, Cheung TK, Chu MY, Tsang VY, Fung JT, Kam KM, Lo JY: Resistance to tetracycline, erythromycin and clindamycin in Streptococcus suis serotype 2 in Hong Kong. Int J Antimicrob Agents. 2009 Chu YW, Cheung TK, Chu MY, Tsang VY, Fung JT, Kam KM, Lo JY: Resistance to tetracycline, erythromycin and clindamycin in Streptococcus suis serotype 2 in Hong Kong. Int J Antimicrob Agents. 2009
8.
go back to reference Hendriksen RS, Mevius DJ, Schroeter A, Teale C, Jouy E, Butaye P, Franco A, Utinane A, Amado A, Moreno M, et al: Occurrence of antimicrobial resistance among bacterial pathogens and indicator bacteria in pigs in different European countries from year 2002-2004: the ARBAO-II study. Acta Vet Scand. 2008, 50: 19-10.1186/1751-0147-50-19.CrossRefPubMedPubMedCentral Hendriksen RS, Mevius DJ, Schroeter A, Teale C, Jouy E, Butaye P, Franco A, Utinane A, Amado A, Moreno M, et al: Occurrence of antimicrobial resistance among bacterial pathogens and indicator bacteria in pigs in different European countries from year 2002-2004: the ARBAO-II study. Acta Vet Scand. 2008, 50: 19-10.1186/1751-0147-50-19.CrossRefPubMedPubMedCentral
9.
go back to reference Martel A, Baele M, Devriese LA, Goossens H, Wisselink HJ, Decostere A, Haesebrouck F: Prevalence and mechanism of resistance against macrolides and lincosamides in Streptococcus suis isolates. Vet Microbiol. 2001, 83 (3): 287-297. 10.1016/S0378-1135(01)00426-6.CrossRefPubMed Martel A, Baele M, Devriese LA, Goossens H, Wisselink HJ, Decostere A, Haesebrouck F: Prevalence and mechanism of resistance against macrolides and lincosamides in Streptococcus suis isolates. Vet Microbiol. 2001, 83 (3): 287-297. 10.1016/S0378-1135(01)00426-6.CrossRefPubMed
10.
go back to reference Princivalli MS, Palmieri C, Magi G, Vignaroli C, Manzin A, Camporese A, Barocci S, Magistrali C, Facinelli B: Genetic diversity of Streptococcus suis clinical isolates from pigs and humans in Italy (2003-2007). Euro Surveill. 2009, 14 (33): Princivalli MS, Palmieri C, Magi G, Vignaroli C, Manzin A, Camporese A, Barocci S, Magistrali C, Facinelli B: Genetic diversity of Streptococcus suis clinical isolates from pigs and humans in Italy (2003-2007). Euro Surveill. 2009, 14 (33):
11.
go back to reference Ye C, Bai X, Zhang J, Jing H, Zheng H, Du H, Cui Z, Zhang S, Jin D, Xu Y, et al: Spread of Streptococcus suis sequence type 7, China. Emerg Infect Dis. 2008, 14 (5): 787-791. 10.3201/eid1405.070437.CrossRefPubMedPubMedCentral Ye C, Bai X, Zhang J, Jing H, Zheng H, Du H, Cui Z, Zhang S, Jin D, Xu Y, et al: Spread of Streptococcus suis sequence type 7, China. Emerg Infect Dis. 2008, 14 (5): 787-791. 10.3201/eid1405.070437.CrossRefPubMedPubMedCentral
12.
go back to reference Zhang C, Ning Y, Zhang Z, Song L, Qiu H, Gao H: In vitro antimicrobial susceptibility of Streptococcus suis strains isolated from clinically healthy sows in China. Vet Microbiol. 2008, 131 (3-4): 386-392. 10.1016/j.vetmic.2008.04.005.CrossRefPubMed Zhang C, Ning Y, Zhang Z, Song L, Qiu H, Gao H: In vitro antimicrobial susceptibility of Streptococcus suis strains isolated from clinically healthy sows in China. Vet Microbiol. 2008, 131 (3-4): 386-392. 10.1016/j.vetmic.2008.04.005.CrossRefPubMed
13.
go back to reference Cantin M, Harel J, Higgins R, Gottschalk M: Antimicrobial resistance patterns and plasmid profiles of Streptococcus suis isolates. J Vet Diagn Invest. 1992, 4 (2): 170-174.CrossRefPubMed Cantin M, Harel J, Higgins R, Gottschalk M: Antimicrobial resistance patterns and plasmid profiles of Streptococcus suis isolates. J Vet Diagn Invest. 1992, 4 (2): 170-174.CrossRefPubMed
14.
go back to reference Takamatsu D, Osaki M, Sekizaki T: Chloramphenicol resistance transposable element TnSs1 of Streptococcus suis, a transposon flanked by IS6-family elements. Plasmid. 2003, 49 (2): 143-151. 10.1016/S0147-619X(02)00149-X.CrossRefPubMed Takamatsu D, Osaki M, Sekizaki T: Chloramphenicol resistance transposable element TnSs1 of Streptococcus suis, a transposon flanked by IS6-family elements. Plasmid. 2003, 49 (2): 143-151. 10.1016/S0147-619X(02)00149-X.CrossRefPubMed
15.
go back to reference Wasteson Y, Hoie S, Roberts MC: Characterization of antibiotic resistance in Streptococcus suis. Vet Microbiol. 1994, 41 (1-2): 41-49. 10.1016/0378-1135(94)90134-1.CrossRefPubMed Wasteson Y, Hoie S, Roberts MC: Characterization of antibiotic resistance in Streptococcus suis. Vet Microbiol. 1994, 41 (1-2): 41-49. 10.1016/0378-1135(94)90134-1.CrossRefPubMed
16.
go back to reference Manzin A, Palmieri C, Serra C, Saddi B, Princivalli MS, Loi G, Angioni G, Tiddia F, Varaldo PE, Facinelli B: Streptococcus suis meningitis without history of animal contact, Italy. Emerg Infect Dis. 2008, 14 (12): 1946-1948. 10.3201/eid1412.080679.CrossRefPubMedPubMedCentral Manzin A, Palmieri C, Serra C, Saddi B, Princivalli MS, Loi G, Angioni G, Tiddia F, Varaldo PE, Facinelli B: Streptococcus suis meningitis without history of animal contact, Italy. Emerg Infect Dis. 2008, 14 (12): 1946-1948. 10.3201/eid1412.080679.CrossRefPubMedPubMedCentral
17.
go back to reference Rizzotti L, La Gioia F, Dellaglio F, Torriani S: Characterization of tetracycline-resistant Streptococcus thermophilus isolates from Italian soft cheeses. Appl Environ Microbiol. 2009, 75 (12): 4224-4229. 10.1128/AEM.01380-08.CrossRefPubMedPubMedCentral Rizzotti L, La Gioia F, Dellaglio F, Torriani S: Characterization of tetracycline-resistant Streptococcus thermophilus isolates from Italian soft cheeses. Appl Environ Microbiol. 2009, 75 (12): 4224-4229. 10.1128/AEM.01380-08.CrossRefPubMedPubMedCentral
18.
go back to reference Rodriguez-Avial I, Rodriguez-Avial C, Culebras E, Picazo JJ: Distribution of tetracycline resistance genes tet(M), tet(O), tet(L) and tet(K) in blood isolates of viridans group streptococci harbouring erm(B) and mef(A) genes. Susceptibility to quinupristin/dalfopristin and linezolid. Int J Antimicrob Agents. 2003, 21 (6): 536-541. 10.1016/S0924-8579(03)00062-1.CrossRefPubMed Rodriguez-Avial I, Rodriguez-Avial C, Culebras E, Picazo JJ: Distribution of tetracycline resistance genes tet(M), tet(O), tet(L) and tet(K) in blood isolates of viridans group streptococci harbouring erm(B) and mef(A) genes. Susceptibility to quinupristin/dalfopristin and linezolid. Int J Antimicrob Agents. 2003, 21 (6): 536-541. 10.1016/S0924-8579(03)00062-1.CrossRefPubMed
19.
go back to reference Roberts MC: Update on acquired tetracycline resistance genes. FEMS Microbiol Lett. 2005, 245 (2): 195-203. 10.1016/j.femsle.2005.02.034.CrossRefPubMed Roberts MC: Update on acquired tetracycline resistance genes. FEMS Microbiol Lett. 2005, 245 (2): 195-203. 10.1016/j.femsle.2005.02.034.CrossRefPubMed
20.
go back to reference Holden MT, Hauser H, Sanders M, Ngo TH, Cherevach I, Cronin A, Goodhead I, Mungall K, Quail MA, Price C, et al: Rapid evolution of virulence and drug resistance in the emerging zoonotic pathogen Streptococcus suis. PLoS One. 2009, 4 (7): e6072-10.1371/journal.pone.0006072.CrossRefPubMedPubMedCentral Holden MT, Hauser H, Sanders M, Ngo TH, Cherevach I, Cronin A, Goodhead I, Mungall K, Quail MA, Price C, et al: Rapid evolution of virulence and drug resistance in the emerging zoonotic pathogen Streptococcus suis. PLoS One. 2009, 4 (7): e6072-10.1371/journal.pone.0006072.CrossRefPubMedPubMedCentral
21.
go back to reference Nghia HD, Hoa NT, Linh le D, Campbell J, Diep TS, Chau NV, Mai NT, Hien TT, Spratt B, Farrar J, et al: Human case of Streptococcus suis serotype 16 infection. Emerg Infect Dis. 2008, 14 (1): 155-157. 10.3201/eid1401.070534.CrossRefPubMedPubMedCentral Nghia HD, Hoa NT, Linh le D, Campbell J, Diep TS, Chau NV, Mai NT, Hien TT, Spratt B, Farrar J, et al: Human case of Streptococcus suis serotype 16 infection. Emerg Infect Dis. 2008, 14 (1): 155-157. 10.3201/eid1401.070534.CrossRefPubMedPubMedCentral
22.
go back to reference Montanari MP, Mingoia M, Giovanetti E, Varaldo PE: Differentiation of resistance phenotypes among erythromycin-resistant Pneumococci. J Clin Microbiol. 2001, 39 (4): 1311-1315. 10.1128/JCM.39.4.1311-1315.2001.CrossRefPubMedPubMedCentral Montanari MP, Mingoia M, Giovanetti E, Varaldo PE: Differentiation of resistance phenotypes among erythromycin-resistant Pneumococci. J Clin Microbiol. 2001, 39 (4): 1311-1315. 10.1128/JCM.39.4.1311-1315.2001.CrossRefPubMedPubMedCentral
23.
go back to reference Malhotra-Kumar S, Lammens C, Piessens J, Goossens H: Multiplex PCR for simultaneous detection of macrolide and tetracycline resistance determinants in streptococci. Antimicrob Agents Chemother. 2005, 49 (11): 4798-4800. 10.1128/AAC.49.11.4798-4800.2005.CrossRefPubMedPubMedCentral Malhotra-Kumar S, Lammens C, Piessens J, Goossens H: Multiplex PCR for simultaneous detection of macrolide and tetracycline resistance determinants in streptococci. Antimicrob Agents Chemother. 2005, 49 (11): 4798-4800. 10.1128/AAC.49.11.4798-4800.2005.CrossRefPubMedPubMedCentral
24.
go back to reference Agerso Y, Pedersen AG, Aarestrup FM: Identification of Tn5397-like and Tn916-like transposons and diversity of the tetracycline resistance gene tet(M) in enterococci from humans, pigs and poultry. J Antimicrob Chemother. 2006, 57 (5): 832-839. 10.1093/jac/dkl069.CrossRefPubMed Agerso Y, Pedersen AG, Aarestrup FM: Identification of Tn5397-like and Tn916-like transposons and diversity of the tetracycline resistance gene tet(M) in enterococci from humans, pigs and poultry. J Antimicrob Chemother. 2006, 57 (5): 832-839. 10.1093/jac/dkl069.CrossRefPubMed
25.
go back to reference Berthelot-Herault F, Marois C, Gottschalk M, Kobisch M: Genetic diversity of Streptococcus suis strains isolated from pigs and humans as revealed by pulsed-field gel electrophoresis. J Clin Microbiol. 2002, 40 (2): 615-619. 10.1128/JCM.40.2.615-6192002.CrossRefPubMedPubMedCentral Berthelot-Herault F, Marois C, Gottschalk M, Kobisch M: Genetic diversity of Streptococcus suis strains isolated from pigs and humans as revealed by pulsed-field gel electrophoresis. J Clin Microbiol. 2002, 40 (2): 615-619. 10.1128/JCM.40.2.615-6192002.CrossRefPubMedPubMedCentral
26.
go back to reference Chopra I, Roberts M: Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol Mol Biol Rev. 2001, 65 (2): 232-260. 10.1128/MMBR.65.2.232-260.2001. second page, table of contents.CrossRefPubMedPubMedCentral Chopra I, Roberts M: Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol Mol Biol Rev. 2001, 65 (2): 232-260. 10.1128/MMBR.65.2.232-260.2001. second page, table of contents.CrossRefPubMedPubMedCentral
27.
go back to reference Roberts MC: Tetracycline resistance determinants: mechanisms of action, regulation of expression, genetic mobility, and distribution. FEMS Microbiol Rev. 1996, 19 (1): 1-24. 10.1111/j.1574-6976.1996.tb00251.x.CrossRefPubMed Roberts MC: Tetracycline resistance determinants: mechanisms of action, regulation of expression, genetic mobility, and distribution. FEMS Microbiol Rev. 1996, 19 (1): 1-24. 10.1111/j.1574-6976.1996.tb00251.x.CrossRefPubMed
28.
go back to reference Melville CM, Scott KP, Mercer DK, Flint HJ: Novel tetracycline resistance gene, tet(32), in the Clostridium-related human colonic anaerobe K10 and its transmission in vitro to the rumen anaerobe Butyrivibrio fibrisolvens. Antimicrob Agents Chemother. 2001, 45 (11): 3246-3249. 10.1128/AAC.45.11.3246-3249.2001.CrossRefPubMedPubMedCentral Melville CM, Scott KP, Mercer DK, Flint HJ: Novel tetracycline resistance gene, tet(32), in the Clostridium-related human colonic anaerobe K10 and its transmission in vitro to the rumen anaerobe Butyrivibrio fibrisolvens. Antimicrob Agents Chemother. 2001, 45 (11): 3246-3249. 10.1128/AAC.45.11.3246-3249.2001.CrossRefPubMedPubMedCentral
29.
go back to reference Smith HE, Veenbergen V, van der Velde J, Damman M, Wisselink HJ, Smits MA: The cps genes of Streptococcus suis serotypes 1, 2, and 9: development of rapid serotype-specific PCR assays. J Clin Microbiol. 1999, 37 (10): 3146-3152.PubMedPubMedCentral Smith HE, Veenbergen V, van der Velde J, Damman M, Wisselink HJ, Smits MA: The cps genes of Streptococcus suis serotypes 1, 2, and 9: development of rapid serotype-specific PCR assays. J Clin Microbiol. 1999, 37 (10): 3146-3152.PubMedPubMedCentral
30.
go back to reference Wisselink HJ, Joosten JJ, Smith HE: Multiplex PCR assays for simultaneous detection of six major serotypes and two virulence-associated phenotypes of Streptococcus suis in tonsillar specimens from pigs. J Clin Microbiol. 2002, 40 (8): 2922-2929. 10.1128/JCM.40.8.2922-2929.2002.CrossRefPubMedPubMedCentral Wisselink HJ, Joosten JJ, Smith HE: Multiplex PCR assays for simultaneous detection of six major serotypes and two virulence-associated phenotypes of Streptococcus suis in tonsillar specimens from pigs. J Clin Microbiol. 2002, 40 (8): 2922-2929. 10.1128/JCM.40.8.2922-2929.2002.CrossRefPubMedPubMedCentral
31.
go back to reference Ng LK, Martin I, Alfa M, Mulvey M: Multiplex PCR for the detection of tetracycline resistant genes. Mol Cell Probes. 2001, 15 (4): 209-215. 10.1006/mcpr.2001.0363.CrossRefPubMed Ng LK, Martin I, Alfa M, Mulvey M: Multiplex PCR for the detection of tetracycline resistant genes. Mol Cell Probes. 2001, 15 (4): 209-215. 10.1006/mcpr.2001.0363.CrossRefPubMed
Metadata
Title
The antimicrobial resistance patterns and associated determinants in Streptococcus suisisolated from humans in southern Vietnam, 1997-2008
Authors
Ngo T Hoa
Tran TB Chieu
Ho DT Nghia
Nguyen TH Mai
Pham H Anh
Marcel Wolbers
Stephen Baker
James I Campbell
Nguyen VV Chau
Tran T Hien
Jeremy Farrar
Constance Schultsz
Publication date
01-12-2011
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2011
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/1471-2334-11-6

Other articles of this Issue 1/2011

BMC Infectious Diseases 1/2011 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.