Assessment of antibiotic susceptibility in Lactobacillus isolates from chickens

Gut Pathogens

Volumn 9, Issue 1, 2017, Pages

  Dec, Marta ^a   Urban Chmiel, Renata ^a   Stȩpień Pyśniak, Dagmara ^a   Wernicki, Andrzej ^a  

^a UNIVERSITY OF LIFE SCIENCES IN LUBLIN   (Poland)

Author keywords

Antibiotic susceptibility; Lactobacillus; Poultry; Resistance genes

Indexed keywords

EID: 85029578156     PISSN: None     EISSN: 17574749     Source Type: Journal    
DOI: 10.1186/s13099-017-0203-z     Document Type: Article

References (75)

1. Lebeer S, Vanderleyden J, De Keersmaecker SC. Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Biol Rev. 2008;72:728-64.
2. Schjørring S, Krogfelt KA. Assessment of bacterial antibiotic resistance transfer in the gut. Int J Microbiol. 2011;2011:1-10.
3. Cauwerts K, Pasmans F, Devriese LA, Haesebrouck F, Decostere A. Cloacal Lactobacillus isolates from broilers often display resistance toward tetracycline antibiotics. Microb Drug Resist. 2006;12:284-8.
4. Cauwerts K, Pasmans F, Devriese LA, Martel A, Haesebrouck F, Decostere A. Cloacal Lactobacillus isolates from broilers show high prevalence of resistance towards macrolide and lincosamide antibiotics. Avian Pathol. 2006;35:160-4.
5. Saif YM. Aly M. Fadly AM, John R. Glisson JR, Larry R. McDougald LR, Nolan L K, Swayne DE, editors. Diseases of poultry. 12th edition. Iowa State, USA: Blackwell Publishing; 2008. p. 752, 771, 821, 875, 896, 934.
6. McMullin P. Medicines and Medication. In: McMullin P, Janet Bradbury J, Alexander D, editors. Pattison M. 6th edition ed. Philadelphia: Poultry Diseases. Saunders Ltd.; 2007. p. 82-93.
7. Lambert T. Antibiotics that affect the ribosome. Rev Sci Tech. 2012;31:57-64.
8. Tenover FC. Mechanisms of antimicrobial resistance in bacteria. Am J Infect Control. 2006;34:S3-10 (discussion S64-73).
9. EFSA Panel on Additives and Products or Substances used in Animal Feed (FEEDAP). Guidance on the assessment of bacterial susceptibility to antimicrobials of human and veterinary importance. EFSA J. 2012;10:2740.
10. Dec M, Puchalski A, Urban-Chmiel R, Wernicki A. 16S-ARDRA and MALDI-TOF mass spectrometry as tools for identification of Lactobacillus bacteria isolated from poultry. BMC Microbiol. 2016;16:105.
11. Dec M, Wernicki A, Puchalski A, Urban-Chmiel R. Antibiotic susceptibility of Lactobacillus strains isolated from domestic geese. Br Poult Sci. 2015;56:416-24.
12. Mayrhofer S, Van Hoek AH, Mair C, Huys G, Aarts HJ, Kneifel W, Domig KJ. Antibiotic susceptibility of members of the Lactobacillus acidophilus group using broth microdilution and molecular identification of their resistance determinants. Int J Food Microbiol. 2010;144:81-7.
13. ISO 10932/IDF 223 - Interantional Organization of Standarization/International Dairy Federation. Milk and milk products. Determination of the minimal inhibitory concentration (MIC) of antibiotics applicable to bifidobacteria and non-enterococcal lactic acid bacteria (LAB). 1st edition. ISO and IDF 2010, Geneva, Switzerland.
14. 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;49:4798-800.
15. Vakulenko SB, Donabedian SM, Voskresenskiy AM, Zervos MJ, Lerner SA, Chow JW. Multiplex PCR for detection of aminoglycoside resistance genes in enterococci. Antimicrob Agents Chemother. 2003;47:1423-6.
16. Van TT, Chin J, Chapman T, Tran LT, Coloe PJ. Safety of raw meat and shellfish in Vietnam: an analysis of Escherichia coli isolations for antibiotic resistance and virulence genes. Int J Food Microbiol. 2008;124:217-23.
17. Ramirez MS, Tolmasky ME. Aminoglycoside modifying enzymes. Drug Resist Updat. 2010;13:151-71.
18. Hummel AS, Hertel C, Holzapfel WH, Franz CM. Antibiotic resistances of starter and probiotic strains of lactic acid bacteria. Appl Environ Microbiol. 2007;73:730-9.
19. Bidya S, Suman RS. Comparative study of three β lactamase test methods in Staphylococcus aureus isolated from two nepalese hospitals. OJCD. 2014;4:47-52.
20. McEwen SA, Fedorka-Cray PJ. Antimicrobial use and resistance in animals. Clin Infect Dis. 2002;1(34 Suppl 3):S93-106.
21. Karapetkov N, Georgieva R, Rumyan N, Karaivanova E. Antibiotic susceptibility of different lactic acid bacteria strains. Benef Microbes. 2011;2:335-9.
22. Callens BF, Haesebrouck F, Maes D, Butaye P, Dewulf J, Boyen F. Clinical resistance and decreased susceptibility in Streptococcus suis isolates from clinically healthy fattening pigs. Microb Drug Resist. 2013;19:146-51.
23. Jones RN, Pfaller MA, Rhomberg PR, Walter DH. Tiamulin activity against fastidious and nonfastidious veterinary and human bacterial isolates: initialdevelopment of in vitro susceptibility test methods. J Clin Microbiol. 2002;40:461-5.
24. van Duijkeren E, Greko C, Pringle M, Baptiste KE, Catry B, Jukes H, Moreno MA, Pomba MC, Pyörälä S, Rantala M, Ružauskas M, Sanders P, Teale C, Threlfall EJ, Torren-Edo J, Törneke K. Pleuromutilins: use in food-producing animals in the European Union, development of resistance and impact on human and animal health. J Antimicrob Chemother. 2014;69:2022-31.
25. Si H, Zhang WJ, Chu S, Wang XM, Dai L, Hua X, Dong Z, Schwarz S, Liu S. Novel plasmid-borne multidrug resistance gene cluster including lsa(E) from a linezolid-resistant Enterococcus faecium isolate of swine origin. Antimicrob Agents Chemother. 2015;59:7113-6.
26. De Vieira Souza F, Roque R, Silva Moreira JL, Resende De Souza M, Nicoli JR, Neumann E, Cantini Nunes Á. Transfer of antibiotic resistance determinants between lactobacilli isolates from the gastrointestinal tract of chicken. Benef Microbes. 2012;3:137-44.
27. Kmet V, Piatnicová E. Antibiotic resistance in commensal intestinal microflora. Folia Microbiol. (Praha). 2010;55:332-5.
28. Chopra I, Roberts M. Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol Mol Biol Rev. 2001;65:232-60.
29. Roberts MC. Update on macrolide-lincosamide-streptogramin, ketolide, and oxazolidinone resistance genes. FEMS Microbiol Lett. 2008;282:147-59.
30. Chang YC, Tsai CY, Lin CF, Wang YC, Wang IK, Chung TC. Characterization of tetracycline resistance lactobacilli isolated from swine intestines at western area of Taiwan. Anaerobe. 2011;17:239-45.
31. Klare I, Konstabel C, Werner G, Huys G, Vankerckhoven V, Kahlmeter G, Hildebrandt B, Müller-Bertling S, Witte W, Goossens H. Antimicrobial susceptibilities of Lactobacillus, Pediococcus and Lactococcus human isolates and cultures intended for probiotic or nutritional use. J Antimicrob Chemother. 2007;59:900-12.
32. Kastner S, Perreten V, Bleuler H, Hugenschmidt G, Lacroix C, Meile L. Antibiotic susceptibility patterns and resistance genes of starter cultures and probiotic bacteria used in food. Sys Appl Microbiol. 2006;29:145-55.
33. Egervärn M, Roos S, Lindmark H. Identification and characterization of antibiotic resistance genes in Lactobacillus reuteri and Lactobacillus plantarum. J App Microbiol. 2009;107:1658-68.
34. Chin SC, Abdullah N, Siang TW, Wan HY. Plasmid profiling and curing of Lactobacillus strains isolated from the gastrointestinal tract of chicken. J Microbiol. 2005;43:251-6.
35. Delgado S, Flórez AB, Mayo B. Antibiotic susceptibility of Lactobacillus and Bifidobacterium species from the human gastrointestinal tract. Curr Microbiol. 2005;50:202-7.
36. Aarestrup FM, Agersø Y, Ahrens P, Østergaard Jørgensen JC, Madsen M, Jensen LB. Antimicrobial susceptibility and presence of resistance genes in staphylococci from poultry. Vet Microbiol. 2000;74:353-64.
37. Khan AA, Nawaz MS, Khan SA, Steele R. Detection and characterization of erythromycin-resistant methylase genes in gram-positive bacteria isolated from poultry litter. Appl Microbiol Biotechnol. 2002;59:377-81.
38. Aquilanti L, Garofalo C, Osimani A, Silvestri G, Vignaroli C, Clementi F. Isolation and molecular characterization of antibiotic-resistant lactic acid bacteria from poultry and swine meat products. J Food Prot. 2007;70:557-65.
39. Zonenschain D, Rebecchi A, Morelli L. Erythromycin- and tetracycline-resistant lactobacilli in Italian fermented dry sausages. J App Microbiol. 2009;107:1559-68.
40. Shazali N, Foo HL, Loh TC, Choe DW, Abdul Rahim R. Prevalence of antibiotic resistance in lactic acid bacteria isolated from the faeces of broiler chicken in Malaysia. Gut Pathog. 2014;6:1.
41. Lonkar P, Harne SD, Kalorey DR, Kurkure NV. Isolation, in vitro antibacterial activity, bacterial sensitivity and plasmid profile of lactobacilli. Asian-Aust J Anim Sci. 2005;18:1336-42.
42. Mayrhofer S, Zitz U, Birru FH, Gollan D, Gołoś AK, Kneifel W, Domig KJ. Comparison of the CLSI guideline and ISO/IDF standard for antimicrobial susceptibility testing of lactobacilli. Microb Drug Resist. 2014;20:591-603.
43. Danielsen M, Wind A. Susceptibility of Lactobacillus spp. to antimicrobial agents. Int J Food Microbiol. 2003;26:1-11.
44. Korhonen J. Antibiotic resistance of lactic acid bacteria dissertations in forestry and natural sciences. Publications of the University of Eastern Finland Dissertations in Forestry and Natural Sciences. Kuopio. 2010.
45. Kobayashi N, Alam M, Nishimoto Y, Urasawa S, Uehara N, Watanabe N. Distribution of aminoglycoside resistance genes in recent clinical isolates of Enterococcus faecalis, Enterococcus faecium and Enterococcus avium. Epidemiol Infect. 2001;126:197-204.
46. Jackson CR, Fedorka-Cray PJ, Barrett JB, Ladely SR. Genetic relatedness of high-level aminoglycoside-resistant enterococci isolated from poultry carcasses. Avian Dis. 2004;48:100-7.
47. Shao Y, Zhang W, Guo H, Pan L, Zhang H, Sun T. Comparative studies on antibiotic resistance in Lactobacillus casei and Lactobacillus plantarum. Food Control. 2015;50:250-8.
48. Rojo-Bezares B, Sáenz Y, Poeta P, Zarazaga M, Ruiz-Larrea F, Torres C. Assessment of antibiotic susceptibility within lactic acid bacteria strains isolated from wine. Int J Food Microbiol. 2006;111:234-40.
49. Tenorio C, Zarazaga M, Martinez C, Torres C. Bifunctional enzyme 6′-N-aminoglycoside cetyltransferase-2″-O aminoglycosidephosphotransferase in Lactobacillus and Pediococcus isolates of animal origin. J Clin Microbiol. 2001;39:824-5.
50. Jaimee G, Halami PM. High level aminoglycoside resistance in Enterococcus, Pediococcus and Lactobacillus species from farm animals and commercial meat products. Ann Microbiol. 2016;66:101-10.
51. Ouoba LI, Lei V, Jensen LB. Resistance of potential probiotic lactic acid bacteria and bifidobacteria of African and European origin to antimicrobials: determination and transferability of the resistance genes to other bacteria. Int J Food Microbiol. 2008;121:217-24.
52. Aarestrup FM, Jensen LB. Trends in antimicrobial susceptibility in relation to antimicrobial usage and presence of resistance genes in Staphylococcus hyicus isolated from exudative epidermitis in pigs. Vet Microbiol. 2002;89:83-94.
53. Jeric PE, Azpiroz A, Lopardo H, Centrón D. Survey of molecular determinants in Gram-positive cocci isolated from hospital settings in Argentina. J Infect Dev Ctries. 2007;1:275-83.
54. Ishihara K, Nakajima K, Kishimoto S, Atarashi F, Muramatsu Y, Hotta A, Ishii S, Takeda Y, Kikuchi M, Tamura Y. Distribution of antimicrobial-resistant lactic acid bacteria in natural cheese in Japan. Microbiol Immunol. 2013;57:684-91.
55. Marrow J, Whittington JK, Mitchell M, Hoyer LL. Maddox Prevalence and antibiotic-resistance characteristics of Enterococcus spp. Isolated from free-living and captive raptors in Central Illinois. J Wildl Dis. 2009;45:302-13.
56. Casado Muñoz Mdel C, Benomar N, Lerma LL, Gálvez A, Abriouel H. Antibiotic resistance of Lactobacillus pentosus and Leuconostoc pseudomesenteroides isolated from naturally-fermented Aloreña table olives throughout fermentation process. Int J Food Microbiol. 2014;172:110-8.
57. Andersen JL, He GX, Kakarla P, K C R, Kumar S, Lakra WS, Mukherjee MM, Ranaweera I, Shrestha U, Tran T, Varela MF. Multidrug efflux pumps from Enterobacteriaceae, Vibrio cholerae and Staphylococcus aureus bacterial food pathogens. Int J Environ Res Public Health. 2015;12:1487-547.
58. Swick MC, Morgan-Linnell SK, Carlson KM, Zechiedrich L. Expression of multidrug efflux pump genes acrAB-tolC, mdfA, and norE in Escherichia coli clinical isolates as a function of fluoroquinolone and multidrug resistance. Antimicrob Agents Chemother. 2011;55:921-4.
59. Schwarz FV, Perreten V, Teuber M. Sequence of the 50-kb conjugative multiresistance plasmid pRE25 from Enterococcus faecalis RE25. Plasmid. 2001;46:170-87.
60. Gevers D, Huys G, Swings J. In vitro conjugal transfer of tetracycline resistance from Lactobacillus isolates to other Gram-positive bacteria. FEMS Microbiol Lett. 2003;225:125-30.
61. Ammor MS, Gueimonde M, Danielsen M, Zagorec M, Van Hoek AH, De Los Reyes-Gavilán CG, Mayo B, Margolles A. Two different tetracycline resistance mechanisms, plasmid-carried tet(L) and chromosomally located transposon-associated tet(M), coexist in Lactobacillus sakei Rits 9. Appl Environ Microbiol. 2008;2008(74):394-401.
62. Feld L, Bielak E, Hammer K, Wilcks A. Characterization of a small erythromycin resistance plasmid pLFE1 from the food-isolate Lactobacillus plantarum M345. Plasmid. 2009;61:159-70.
63. Behnood A, Farajnia S, Moaddab SR, Ahdi-Khosroshahi S, Katayounzadeh A. Prevalence of aac(6')-Ie-aph(2″)-Ia resistance gene and its linkage to Tn5281 in Enterococcus faecalis and Enterococcus faecium isolates from Tabriz hospitals. Iran J Microbiol. 2013;5:203-8.
64. Ng LK, Martin I, Alfa M, Mulvey M. Multiplex PCR for the detection of tetracycline resistant genes. Mol Cell Probes. 2001;15:209-15.
65. Masco L, Van Hoorde K, De Brandt E, Swings J, Huys G. Antimicrobial susceptibility of Bifidobacterium strains from humans, animals and probiotic products. J Antimicrob Chemother. 2006;58:85-94.
66. Toomey N, Bolton D, Fanning S. Characterisation and transferability of antibiotic resistance genes from lactic acid bacteria isolated from Irish pork and beef abattoirs. Res Microbiol. 2010;161:127-35.
67. Werner G, Hildebrandt B, Witte W. The newly described msrC gene is not equally distributed among all isolates of Enterococcus faecium. Antimicrob Agents Chemother. 2001;45:3672-3.
68. Kehrenberg C, Schwarz S. Distribution of florfenicol resistance genes fexA and cfr among chloramphenicol-resistant Staphylococcus isolates. Antimicrob Agents Chemother. 2006;50:1156-63.
69. Li XS, Dong WC, Wang XM, Hu GZ, Wang YB, Cai BY, Wu CM, Wang Y, Du XD. Presence and genetic environment of pleuromutilin-lincosamide-streptogramin A resistance gene lsa(E) in enterococci of human and swine origin. J Antimicrob Chemother. 2014;69:1424-6.
70. Li J, Li B, Wendlandt S, Schwarz S, Wang Y, Wu C, Ma Z, Shen J. Identification of a novel vga(E) gene variant that confers resistance to pleuromutilins, lincosamides and streptogramin A antibiotics in staphylococci of porcine origin. J Antimicrob Chemother. 2014;69:919-23.
71. Haroche J, Morvan A, Davi M, Allignet J, Bimet F, El Solh N. Clonal diversity among streptogramin A-resistant Staphylococcus aureus isolates collected in Frenchhospitals. J Clin Microbiol. 2003;41:586-91.
72. Garofalo C, Vignaroli C, Zandri G, Aquilanti L, Bordoni D, Osimani A, Clementi F, Biavasco F. Direct detection of antibiotic resistance genes in specimens of chicken and pork meat. Int J Food Microbiol. 2007;113:75-83.
73. Lee JH. Methicillin (Oxacillin)-resistant Staphylococcus aureus strains isolated from major food animals and their potential transmission to humans. Appl Environ Microbiol. 2003;69:6489-94.
74. Obeng AS, Rickard H, Ndi O, Sexton M, Barton M. Comparison of antimicrobial resistance patterns in enterococci from intensive and free range chickens in Australia. Avian Pathol. 2013;42:45-54.
75. Patel D, Kosmidis C, Seo SM, Kaatz GW. Ethidium bromide MIC screening for enhanced efflux pump gene expression or efflux activity in Staphylococcus aureus. Antimicrob Agents Chemother. 2010;54:5070-3.