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Vol. 14, No. 1-3, 2008
Issue release date: October 2007
Section title: Paper
Free Access
J Mol Microbiol Biotechnol 2008;14:6–15
(DOI:10.1159/000106077)

Molecular Characterization of Intrinsic and Acquired Antibiotic Resistance in Lactic Acid Bacteria and Bifidobacteria

Ammor M.S.a · Flórez A.B.a · van Hoek A.H.A.M.b · de los Reyes-Gavilán C.G.a · Aarts H.J.M.b · Margolles A.a · Mayo B.a
aInstituto de Productos Lácteos de Asturias (IPLA), Consejo Superior de Investigaciones Científicas (CSIC), Carretera de Infiesto s/n, Villaviciosa, Spain; bRIKILT – Institute of Food Safety, Wageningen UR, Wageningen, The Netherlands
email Corresponding Author

Abstract

The minimum inhibitory concentrations (MICs) of 6 different antibiotics (chloramphenicol, clindamycin, erythromycin, streptomycin, tetracycline and vancomycin) were determined for 143 strains of lactic acid bacteria and bifidobacteria using the Etest. Different MICs were found for different species and strains. Based on the distribution of these MIC values, most of the strains were either susceptible or intrinsically resistant to these antibiotics. However, the MIC range of some of these antibiotics showed a bimodal distribution, which suggested that some of the tested strains possess acquired antibiotic resistance. Screening for resistance genes was performed by PCR using specific primers, or using a DNA microarray with around 300 nucleotide probes representing 7 classes of antibiotic resistance genes. The genes identified encoded resistance to tetracycline [tet(M), tet(W), tet(O) and tet(O/W)], erythromycin and clindamycin [erm(B)] and streptomycin [aph(E) and sat(3)]. Internal portions of some of these determinants were sequenced and found to be identical to genes described in other bacteria. All resistance determinants were located on the bacterial chromosome, except for tet(M), which was identified on plasmids in Lactococcus lactis. The contribution of intrinsic multidrug transporters to the antibiotic resistance was investigated by cloning and measuring the expression of Bifidobacterium breve genes in L. lactis.

© 2008 S. Karger AG, Basel


  

Key Words

  • Lactic acid bacteria
  • Bifidobacteria
  • Antibiotic resistance
  • Antibiotic resistance genes
  • Multidrug resistance

References

  1. Ahn C, Collins-Thompson D, Duncan C, Stiles ME: Mobilization and location of the genetic determinant of chloramphenicol resistance from Lactobacillus plantarum caTC2R. Plasmid 1992;27:169–176.
  2. Anadón A, Abroix Arzo M, Bories G, et al: Opinion of the FEEDAP Panel on the updating of the criteria used in the assessment of bacteria for resistance to antibiotics of human or veterinary importance. EFSA J 2005;223:1–12.
  3. Barbosa TM, Scott KP, Flint HJ: Evidence for recent intergeneric transfer of a new tetracycline resistance gene, tet(W), isolated from Butyrivibrio fibrisolvens, and the occurrence of tet(O) in ruminal bacteria. Environ Microbiol 1999;1:53–64.
  4. Bates J, Jordens JZ, Griffiths DT: Farm animals as a putative reservoir for vancomycin-resistant enterococcal infection in man. J Antimicrob Chemother 1994;34:507–514.
  5. Blázquez J, Oliver A, Gómez-Gomez JM: Mutation and evolution of antibiotic resistance: antibiotics as promoters of antibiotic resistance? Curr Drug Targets 2002;3:345–349.
  6. Clermont D, Chesneau O, De Cespedes G, Horaud T: New tetracycline resistance determinants coding for ribosomal protection in streptococci and nucleotide sequence of tet(T) isolated from Streptococcus pyogenes A498. Antimicrob Agents Chemother 1997;41:112–116.
  7. Clinical and Laboratory Standards Institute: Methods for Antimicrobial Susceptibility Testing of Anaerobic Bacteria: Approved Standard, ed 6 (CLSI document M11-A6). Wayne, Clinical and Laboratory Standards Institute, 2004.
  8. Cui L, Ma X, Sato K, Okuma K, Tenover FC, Mamizuka EM, Gemmell CG, Kim MN, Poy MC, El-Solh N, Ferraz V, Hiramatsu K: Cell wall thickening is a common feature of vancomycin resistance in Staphylococcus aureus. J Clin Microbiol 2003;41:5–14.
  9. Danielsen M: Characterization of the tetracycline resistance plasmid pMD5057 from Lactobacillus plantarum 5057 reveals a composite structure. Plasmid 2002;48:98–103.
  10. Danielsen M, Wind A: Susceptibility of Lactobacillus spp. to antimicrobial agents. Int J Food Microbiol 2003;82:1–11.
  11. Delgado S, Flórez AB, Mayo B: Antibiotic susceptibility of Lactobacillus and Bifidobacterium species from the human gastrointestinal tract. Curr Microbiol 2005;50:202–207.
  12. De Ruyter PG, Kuipers OP, de Vos WM: Controlled gene expression systems for Lactococcus lactis with the food-grade inducer nisin. Appl Environ Microbiol 1996;62:3662–3667.
  13. Flórez AB, Delgado S, Mayo B: Antimicrobial susceptibility of lactic acid bacteria isolated from a cheese environment. Can J Microbiol 2005;51:51–58.
  14. Fons M, Hege T, Ladire M, Raibaud P, Ducluzeau R, Maguin E: Isolation and characterization of a plasmid from Lactobacillus fermentum conferring erythromycin resistance. Plasmid 1997;37:199–203.
  15. Gevers D, Masco L, Baert L, Huys G, Debevere J, Swings J: Prevalence and diversity of tetracycline resistant lactic acid bacteria and their tet genes along the process line of fermented dry sausages. Syst Appl Microbiol 2003;26:277–283.
  16. Hamilton-Miller JM, Shah S: Vancomycin susceptibility as an aid to the identification of lactobacilli. Lett Appl Microbiol 1998;26:153–115.
  17. Herzog-Velikonja B, Podlesek Z, Grabnar M: Conjugal transfer of transposon Tn916 from Enterococcus faecalis to Bacillus licheniformis. Plasmid 1994 31:201–206.
  18. Katla AK, Kruse H, Johnsen G, Herikstad H: Antimicrobial susceptibility of starter culture bacteria used in Norwegian dairy products. Int J Food Microbiol 2001;67:147–152.
  19. Kim KS, Morrison JO, Bayer AS: Deficient autholytic enzyme activity in antibiotic-tolerant lactobacilli. Infec Immun 1982;36:582–585.
  20. Klare I, Konstabel C, Muller-Bertling S, Reissbrodt R, Huys G, Vancanneyt M, Swings J, Goossens H, Witte W: Evaluation of new broth media for microdilution antibiotic susceptibility testing of lactobacilli, pediococci, lactococci, and bifidobacteria. Appl Environ Microbiol 2005;71:8982–8986.
  21. Klein G, Hallmann C, Casas IA, Abad J, Louwers J, Reuter G: Exclusion of vanA, vanB and vanC type glycopeptide resistance in strains of Lactobacillus reuteri and Lactobacillus rhamnosus used as probiotics by polymerase chain reaction and hybridization methods. J Appl Microbiol 2000;89:815–824.
  22. Luna VA, Cousin S Jr, Whittington WL, Roberts MC: Identification of the conjugative mef gene in clinical Acinetobacter junii and Neisseria gonorrhoeae isolates. Antimicrob Agents Chemother 2000;44:2503–2506.
  23. Margolles A, Moreno JA, van Sinderen D, de Los Reyes-Gavilán CG: Macrolide resistance mediated by a Bifidobacterium breve membrane protein. Antimicrob Agents Chemother 2005;49:4379–4381.
  24. Moubareck C, Gavini F, Vaugien L, Butel MJ, Doucet-Populaire F: Antimicrobial susceptibility of bifidobacteria. J Antimicrob Chemother 2005;55:38–44.
  25. Murray PR, Baron EJ, Jorgensen JH, Pfaller MA, Yolken RH: Manual of Clinical Microbiology. Washington, American Society for Microbiology, 2003.
  26. Nikolich MP, Hong G, Shoemaker NB, Salyers AA: Evidence for natural horizontal transfer of tetQ between bacteria that normally colonize humans and bacteria that normally colonize livestock. Appl Environ Microbiol 1994;60:3255–3260.
  27. Normark BH, Normark S: Evolution and spread of antibiotic resistance. J Intern Med 2002;252:91–106.
  28. O’Sullivan DJ, Klaenhammer TR: Rapid mini-prep isolation of high-quality plasmid DNA from Lactococcus and Lactobacillus spp. Appl Environ Microbiol 1993;59:2730–2733.
  29. Ouwehand AC, Salminen S, Isolauri E: Probiotics: an overview of beneficial effects. Antonie Van Leeuwenhoek 2002;82:279–289.
  30. Paterson DL, Bonomo RA: Extended-spectrum β-lactamases: a clinical update. Clin Microbiol Rev 2005;18:657–686.
  31. Perreten V, Schwarz F, Cresta L, Boeglin M, Dasen G, Teuber M: Antibiotic resistance spread in food. Nature 1997;389:801.
  32. Price CE, Reid SJ, Driessen AJ, Abratt VR: The Bifidobacterium longum NCIMB 702259T ctr gene codes for a novel cholate transporter. Appl Environ Microbiol 2006;72:923–926.
  33. Putman M, van Veen HW, Konings WN: Molecular properties of bacterial multidrug transporters. Microbiol Mol Biol Rev 2000;64:672–693.
  34. Roberts MC, Chung WO, Roe D, Xia M, Marquez C, Borthagaray G, Whittington EL, Holmes KK: Erythromycin-resistant Neisseria gonorrhoeae and oral commensal Neisseria spp. carry known rRNA methylase genes. Antimicrob Agents Chemother 1999;43:1367–1372.
  35. Scott KP, Melville CM, Barbosa TM, Flint HJ: Occurrence of the new tetracycline resistance gene tet(W) in bacteria from the human gut. Antimicrob Agents Chemother 2000;44:775–777.
  36. Tannock GW, Luchansky JB, Miller L, Connell H, Thode-Andersen S, Mercer AA, Klaenhammer TR: Molecular characterization of a plasmid-borne (pGT633) erythromycin resistance determinant (ermGT) from Lactobacillus reuteri 100-63. Plasmid 1994;31:60–71.
  37. Temmerman R, Pot B, Huys G, Swings J: Identification and antibiotic susceptibility of bacterial isolates from probiotic products. Int J Food Microbiol 2003;81:1–10.
  38. Teuber M, Meile L, Schwarz F: Acquired antibiotic resistance in lactic acid bacteria from food. Antonie van Leeuwenhoek 1999;76:115–137.
  39. Van Hoek AHAM, Scholtens IMJ, Cloeckaert A, Aarts HJM: Detection of antibiotic resistance genes in different Salmonella serovars by oligonucleotide microarray analysis. J Microbiol Methods 2005;62:13–23.
  40. Witte W: Selective pressure by antibiotic use in livestock. Int J Antimicrob Agents 2000;16:S19–S24.
  41. Zarazaga M, Sáenz Y, Portillo A, Tenorio C, Ruiz-Larrea F, Del Campo R, Baquero F, Torres C: In vitro activities of ketolide HMR3647, macrolides, and other antibiotics against Lactobacillus, Leuconostoc, and Pediococcus isolates. Antimicrob Agents Chemother 1999;43:3039–3041.
  42. Zhou JS, Pillidge CJ, Gopal PK, Gill HS: Antibiotic susceptibility profiles of new probiotic Lactobacillus and Bifidobacterium strains. Int J Food Microbiol 2005;98:211–217.

  

Author Contacts

Mohammed Salim Ammor
Instituto de Productos Lácteos de Asturias (CSIC)
Carretera de Infiesto s/n
ES–33300 Villaviciosa (Spain)
Tel. +34 985 89 12 31, Fax +34 985 89 22 33, E-Mail ammor@ipla.csic.es

  

Article Information

Number of Print Pages : 10
Number of Figures : 1, Number of Tables : 5, Number of References : 42

  

Publication Details

Journal of Molecular Microbiology and Biotechnology

Vol. 14, No. 1-3, Year 2008 (Cover Date: October 2007)

Journal Editor: Saier Jr., M.H. (La Jolla, Calif.)
ISSN: 1464–1801 (print), 1660–2412 (Online)

For additional information: http://www.karger.com/MMB


Copyright / Drug Dosage / Disclaimer

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

Abstract

The minimum inhibitory concentrations (MICs) of 6 different antibiotics (chloramphenicol, clindamycin, erythromycin, streptomycin, tetracycline and vancomycin) were determined for 143 strains of lactic acid bacteria and bifidobacteria using the Etest. Different MICs were found for different species and strains. Based on the distribution of these MIC values, most of the strains were either susceptible or intrinsically resistant to these antibiotics. However, the MIC range of some of these antibiotics showed a bimodal distribution, which suggested that some of the tested strains possess acquired antibiotic resistance. Screening for resistance genes was performed by PCR using specific primers, or using a DNA microarray with around 300 nucleotide probes representing 7 classes of antibiotic resistance genes. The genes identified encoded resistance to tetracycline [tet(M), tet(W), tet(O) and tet(O/W)], erythromycin and clindamycin [erm(B)] and streptomycin [aph(E) and sat(3)]. Internal portions of some of these determinants were sequenced and found to be identical to genes described in other bacteria. All resistance determinants were located on the bacterial chromosome, except for tet(M), which was identified on plasmids in Lactococcus lactis. The contribution of intrinsic multidrug transporters to the antibiotic resistance was investigated by cloning and measuring the expression of Bifidobacterium breve genes in L. lactis.

© 2008 S. Karger AG, Basel


  

Author Contacts

Mohammed Salim Ammor
Instituto de Productos Lácteos de Asturias (CSIC)
Carretera de Infiesto s/n
ES–33300 Villaviciosa (Spain)
Tel. +34 985 89 12 31, Fax +34 985 89 22 33, E-Mail ammor@ipla.csic.es

  

Article Information

Number of Print Pages : 10
Number of Figures : 1, Number of Tables : 5, Number of References : 42

  

Publication Details

Journal of Molecular Microbiology and Biotechnology

Vol. 14, No. 1-3, Year 2008 (Cover Date: October 2007)

Journal Editor: Saier Jr., M.H. (La Jolla, Calif.)
ISSN: 1464–1801 (print), 1660–2412 (Online)

For additional information: http://www.karger.com/MMB


Article / Publication Details

First-Page Preview
Abstract of Paper

Published online: 10/24/2007
Issue release date: October 2007

Number of Print Pages: 10
Number of Figures: 1
Number of Tables: 5

ISSN: 1464-1801 (Print)
eISSN: 1660-2412 (Online)

For additional information: http://www.karger.com/MMB


Copyright / Drug Dosage

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

References

  1. Ahn C, Collins-Thompson D, Duncan C, Stiles ME: Mobilization and location of the genetic determinant of chloramphenicol resistance from Lactobacillus plantarum caTC2R. Plasmid 1992;27:169–176.
  2. Anadón A, Abroix Arzo M, Bories G, et al: Opinion of the FEEDAP Panel on the updating of the criteria used in the assessment of bacteria for resistance to antibiotics of human or veterinary importance. EFSA J 2005;223:1–12.
  3. Barbosa TM, Scott KP, Flint HJ: Evidence for recent intergeneric transfer of a new tetracycline resistance gene, tet(W), isolated from Butyrivibrio fibrisolvens, and the occurrence of tet(O) in ruminal bacteria. Environ Microbiol 1999;1:53–64.
  4. Bates J, Jordens JZ, Griffiths DT: Farm animals as a putative reservoir for vancomycin-resistant enterococcal infection in man. J Antimicrob Chemother 1994;34:507–514.
  5. Blázquez J, Oliver A, Gómez-Gomez JM: Mutation and evolution of antibiotic resistance: antibiotics as promoters of antibiotic resistance? Curr Drug Targets 2002;3:345–349.
  6. Clermont D, Chesneau O, De Cespedes G, Horaud T: New tetracycline resistance determinants coding for ribosomal protection in streptococci and nucleotide sequence of tet(T) isolated from Streptococcus pyogenes A498. Antimicrob Agents Chemother 1997;41:112–116.
  7. Clinical and Laboratory Standards Institute: Methods for Antimicrobial Susceptibility Testing of Anaerobic Bacteria: Approved Standard, ed 6 (CLSI document M11-A6). Wayne, Clinical and Laboratory Standards Institute, 2004.
  8. Cui L, Ma X, Sato K, Okuma K, Tenover FC, Mamizuka EM, Gemmell CG, Kim MN, Poy MC, El-Solh N, Ferraz V, Hiramatsu K: Cell wall thickening is a common feature of vancomycin resistance in Staphylococcus aureus. J Clin Microbiol 2003;41:5–14.
  9. Danielsen M: Characterization of the tetracycline resistance plasmid pMD5057 from Lactobacillus plantarum 5057 reveals a composite structure. Plasmid 2002;48:98–103.
  10. Danielsen M, Wind A: Susceptibility of Lactobacillus spp. to antimicrobial agents. Int J Food Microbiol 2003;82:1–11.
  11. Delgado S, Flórez AB, Mayo B: Antibiotic susceptibility of Lactobacillus and Bifidobacterium species from the human gastrointestinal tract. Curr Microbiol 2005;50:202–207.
  12. De Ruyter PG, Kuipers OP, de Vos WM: Controlled gene expression systems for Lactococcus lactis with the food-grade inducer nisin. Appl Environ Microbiol 1996;62:3662–3667.
  13. Flórez AB, Delgado S, Mayo B: Antimicrobial susceptibility of lactic acid bacteria isolated from a cheese environment. Can J Microbiol 2005;51:51–58.
  14. Fons M, Hege T, Ladire M, Raibaud P, Ducluzeau R, Maguin E: Isolation and characterization of a plasmid from Lactobacillus fermentum conferring erythromycin resistance. Plasmid 1997;37:199–203.
  15. Gevers D, Masco L, Baert L, Huys G, Debevere J, Swings J: Prevalence and diversity of tetracycline resistant lactic acid bacteria and their tet genes along the process line of fermented dry sausages. Syst Appl Microbiol 2003;26:277–283.
  16. Hamilton-Miller JM, Shah S: Vancomycin susceptibility as an aid to the identification of lactobacilli. Lett Appl Microbiol 1998;26:153–115.
  17. Herzog-Velikonja B, Podlesek Z, Grabnar M: Conjugal transfer of transposon Tn916 from Enterococcus faecalis to Bacillus licheniformis. Plasmid 1994 31:201–206.
  18. Katla AK, Kruse H, Johnsen G, Herikstad H: Antimicrobial susceptibility of starter culture bacteria used in Norwegian dairy products. Int J Food Microbiol 2001;67:147–152.
  19. Kim KS, Morrison JO, Bayer AS: Deficient autholytic enzyme activity in antibiotic-tolerant lactobacilli. Infec Immun 1982;36:582–585.
  20. Klare I, Konstabel C, Muller-Bertling S, Reissbrodt R, Huys G, Vancanneyt M, Swings J, Goossens H, Witte W: Evaluation of new broth media for microdilution antibiotic susceptibility testing of lactobacilli, pediococci, lactococci, and bifidobacteria. Appl Environ Microbiol 2005;71:8982–8986.
  21. Klein G, Hallmann C, Casas IA, Abad J, Louwers J, Reuter G: Exclusion of vanA, vanB and vanC type glycopeptide resistance in strains of Lactobacillus reuteri and Lactobacillus rhamnosus used as probiotics by polymerase chain reaction and hybridization methods. J Appl Microbiol 2000;89:815–824.
  22. Luna VA, Cousin S Jr, Whittington WL, Roberts MC: Identification of the conjugative mef gene in clinical Acinetobacter junii and Neisseria gonorrhoeae isolates. Antimicrob Agents Chemother 2000;44:2503–2506.
  23. Margolles A, Moreno JA, van Sinderen D, de Los Reyes-Gavilán CG: Macrolide resistance mediated by a Bifidobacterium breve membrane protein. Antimicrob Agents Chemother 2005;49:4379–4381.
  24. Moubareck C, Gavini F, Vaugien L, Butel MJ, Doucet-Populaire F: Antimicrobial susceptibility of bifidobacteria. J Antimicrob Chemother 2005;55:38–44.
  25. Murray PR, Baron EJ, Jorgensen JH, Pfaller MA, Yolken RH: Manual of Clinical Microbiology. Washington, American Society for Microbiology, 2003.
  26. Nikolich MP, Hong G, Shoemaker NB, Salyers AA: Evidence for natural horizontal transfer of tetQ between bacteria that normally colonize humans and bacteria that normally colonize livestock. Appl Environ Microbiol 1994;60:3255–3260.
  27. Normark BH, Normark S: Evolution and spread of antibiotic resistance. J Intern Med 2002;252:91–106.
  28. O’Sullivan DJ, Klaenhammer TR: Rapid mini-prep isolation of high-quality plasmid DNA from Lactococcus and Lactobacillus spp. Appl Environ Microbiol 1993;59:2730–2733.
  29. Ouwehand AC, Salminen S, Isolauri E: Probiotics: an overview of beneficial effects. Antonie Van Leeuwenhoek 2002;82:279–289.
  30. Paterson DL, Bonomo RA: Extended-spectrum β-lactamases: a clinical update. Clin Microbiol Rev 2005;18:657–686.
  31. Perreten V, Schwarz F, Cresta L, Boeglin M, Dasen G, Teuber M: Antibiotic resistance spread in food. Nature 1997;389:801.
  32. Price CE, Reid SJ, Driessen AJ, Abratt VR: The Bifidobacterium longum NCIMB 702259T ctr gene codes for a novel cholate transporter. Appl Environ Microbiol 2006;72:923–926.
  33. Putman M, van Veen HW, Konings WN: Molecular properties of bacterial multidrug transporters. Microbiol Mol Biol Rev 2000;64:672–693.
  34. Roberts MC, Chung WO, Roe D, Xia M, Marquez C, Borthagaray G, Whittington EL, Holmes KK: Erythromycin-resistant Neisseria gonorrhoeae and oral commensal Neisseria spp. carry known rRNA methylase genes. Antimicrob Agents Chemother 1999;43:1367–1372.
  35. Scott KP, Melville CM, Barbosa TM, Flint HJ: Occurrence of the new tetracycline resistance gene tet(W) in bacteria from the human gut. Antimicrob Agents Chemother 2000;44:775–777.
  36. Tannock GW, Luchansky JB, Miller L, Connell H, Thode-Andersen S, Mercer AA, Klaenhammer TR: Molecular characterization of a plasmid-borne (pGT633) erythromycin resistance determinant (ermGT) from Lactobacillus reuteri 100-63. Plasmid 1994;31:60–71.
  37. Temmerman R, Pot B, Huys G, Swings J: Identification and antibiotic susceptibility of bacterial isolates from probiotic products. Int J Food Microbiol 2003;81:1–10.
  38. Teuber M, Meile L, Schwarz F: Acquired antibiotic resistance in lactic acid bacteria from food. Antonie van Leeuwenhoek 1999;76:115–137.
  39. Van Hoek AHAM, Scholtens IMJ, Cloeckaert A, Aarts HJM: Detection of antibiotic resistance genes in different Salmonella serovars by oligonucleotide microarray analysis. J Microbiol Methods 2005;62:13–23.
  40. Witte W: Selective pressure by antibiotic use in livestock. Int J Antimicrob Agents 2000;16:S19–S24.
  41. Zarazaga M, Sáenz Y, Portillo A, Tenorio C, Ruiz-Larrea F, Del Campo R, Baquero F, Torres C: In vitro activities of ketolide HMR3647, macrolides, and other antibiotics against Lactobacillus, Leuconostoc, and Pediococcus isolates. Antimicrob Agents Chemother 1999;43:3039–3041.
  42. Zhou JS, Pillidge CJ, Gopal PK, Gill HS: Antibiotic susceptibility profiles of new probiotic Lactobacillus and Bifidobacterium strains. Int J Food Microbiol 2005;98:211–217.