Antimicrobial resistance of Salmonella spp. isolated from food

• Autorzy: Maka L. , Popowska M.
• Języki publikacji: EN

Abstrakty

EN

This review summarizes current data on resistance among Salmonella spp. isolates of food origin from countries in different regions of the world. The mechanisms of resistance to different groups of antimicrobial compounds are also considered. Among strains resistant to quinolones and/or fluoroquinolones the most prevalent mechanism is amino acid substitutions in quinolone resistance-determining region (QRDR) of genes gyrA, parC but mechanism of growing importance is plasmid-mediated quinolone resistance (PMQR) associated with genes qnrA, qnrB, qnrC, qnrD, qnrS but frequency of their detection is different. Resistance to sulfonamides is mostly associated with genes sul1 and sul2, while resistance to trimethoprim is associated with various variants of dhfr ( dfr) genes. Taking into account Salmonella spp. strains isolated from food, resistance to β-lactams is commonly associated with β-lactamases encoding by blaTEM genes. However strains ESBL and AmpC – positive are also detected. Resistance to aminoglicosides is commonly result of enzymatic inactivation. Three types of aminoglycoside modifying enzyme are: acetyltransferases (AAC), adenyltransferases (ANT) and phosphotransferases (APH). Resistance to tetracyclines among Salmonella spp. isolated from food is most commonly associated with active efflux. Among numerous genetic determinants encoding efflux pumps tetA, tetB, tetC, tetD, tetE and tetG are reported predominatingly. One of the most common mechanisms of resistance against chloramphenicol is its inactivation by chloramphenicol acetyltrasferases (CATs), but resistance to this compound can be also mediated by chloramphenicol efflux pumps encoded by the genes cmlA and floR. It is important to monitor resistance of Salmonella isolated from food, because the globalization of trade, leading to the long-distance movement of goods, animals and food products, encourages the spread of resistant pathogens around the world.

PL

W artykule przedstawiono aktualne dane na temat mechaniznów lekooporności pałeczek Salmonella spp. pochodzących z żywności. Wśród szczepów opornych na chinolony i/lub fluorochinolony najczęściej identyfikowanym mechanizmem są substytucje aminokwasów w obrębie regionów determinujących oporność na chinolony (QRDR-quinolone resistancedetermining region) w genach gyrA i parC, jednak coraz częściej identyfikowane są geny qnr (qnrA, qnrB, qnrC, qnrD, qnrS) związane z plazmidami (PMQR - plasmid-mediated quinolone resistance). Oporność na sulfonamidy jest najczęściej związana z genami sul1 i sul2, natomiast różne warianty genów dhfr ( dfr) warunkują oporność na trimetoprim. Biorąc pod uwagę szczepy Salmonella spp. pochodzące z żywności, oporność na antybiotyki β-laktamowe związana jest zazwyczaj z produkcją β-laktamaz kodowanych przez geny blaTEM. Jednakże coraz powszechniej identyfikowane są szczepy produkujące β-laktamazy o rozszerzonym spektrum substratowym (ESBL) oraz cefalosporynazy AmpC. Oporność na aminoglikozydy najczęściej wynika z wytwarzania enzymów modyfikujących cząsteczki leku: acetylotransferaz (AAC), adenylotransferaz (ANT) oraz fosfotransferaz (APH). Oporność wobec tetracyklin wśród pałeczek Salmonella spp. izolowanych z żywności najczęściej związana jest z mechanizmem aktywnego usuwania leku za pomocą pomp (efflux) kodowanych, najczęściej przez geny tetA, tetB, tetC, tetD, tetE i tetG. Jednym a najczęściej wykrywanych mechanizmów oporności na chloramfenikol jest jego inaktywacja w wyniku działania acetylotransferazy chloramfenikolowej (CAT). Oporność na chloramfenikol może być również związana ze zjawiskiem aktywnego wypompowywania leku. Pompy efflux są kodowane przez geny floR (warunkujące oporność także na florfenikol) lub cml. Istotne znaczenie ma monitoring lekooporności wśród szczepów Salmonella spp. pochodzących z żywności, ponieważ transport środków spożywczych oraz zwierząt do i z krajów całego świata ułatwia rozprzestrzenianie się szczepów lekoopornych.

Słowa kluczowe

EN

antimicrobial resistance; Salmonella; isolation; food; food-borne pathogen; resistance; food safety

• Wydawca: -
• Czasopismo: Roczniki Państwowego Zakładu Higieny
• Rocznik: 2016
• Tom: 67
• Numer: 4
• Opis fizyczny: p.343-357,ref.

Twórcy

autor

Maka L.

• Laboratory of Food Microbiology, Department of Food Safety, National Institute of Public Health - National Institute of Hygiene, 24 Chocimska str., 00-791 Warsaw, Poland

autor

Popowska M.

• Department of Applied Microbiology, Institute of Microbiology, Faculty of Biology, University of Warsaw, Warsaw, Poland

Bibliografia

• 1. Aarestrup F.M., Hendriksen R.S., Lockett J., Gay K., Teates K., McDermott P.F., White P.G., Hasman H., Sørensen G., Bangtrakulnonth A., Pornreongwong S., Pulsrikarn C., Angulo F.J., Gerner-Smidt P.: International spread of multidrug-resistant Salmonella Schwarzengrund in food products. Emerg Infect Dis 2007;13(5):726–731.
• 2. Abbassi-Ghozzi I., Jaouani A., Hammami S., Martinez-Urtaza J., Boudabous A., Gtari, M.: Molecular analysis and antimicrobial resistance of Salmonella isolates recovered from raw meat marketed in the area of “Grand Tunis”, Tunisia. Pathol Biol 2012;60(5):e49–54.
• 3. Ahmed A.M., Nakano H., Shimamoto T.: Molecular characterization of integrons in non-typhoid Salmonella serovars isolated in Japan: description of an unusual class 2 integron. J Antimicrob Chemoth 2005;55:371-374.
• 4. Alekshun M.N., Levy S.B.: Molecular mechanisms of antibacterial multidrug resistance. Cell 2007;128:1037-1050.
• 5. Álvarez-Fernández E., Alonso-Calleja C., García-Fernández C., Capita R.: Prevalence and antimicrobial resistance of Salmonella serotypes isolated from poultry in Spain: comparison between 1993 and 2006. Int J Food Microbiol 2012;153(3):281–287.
• 6. Antunes P., Machado J., Sousa J.C., Peixe L.: Dissemination of sulfonamide resistance genes (sul1, sul2 and sul3) in Portuguese Salmonella enterica strains and relation with integrons. Antimicrob Agents Ch 2005;49(2):836-839.
• 7. Aslam M., Checkley S., Avery B., Chalmers G., Bohaychuk V., Gensler G., Reid-Smith R., Boerlin, P.: Phenotypic and genetic characterization of antimicrobial resistance in Salmonella serovars isolated from retail meats in Alberta, Canada. Food Microbiol 2012;32:110-117.
• 8. Baucheron S., Tyler S., Boyd D., Mulvey M.R., Chaslus-Dancla E., Cloeckaert, A.: AcrAB-TolC directs effluxmediated multidrug resistance in Salmonella enterica serovar Typhimurium DT104. Antimicrob Agents Ch 2004;48(10):3729-3735.
• 9. Bouchrif B., Paglietti B., Murgia M., Piana A., Cohen N., Ennaji, M.M., Rubino S., Timinouni, M.: Prevalence and antibiotic-resistance of Salmonella isolated from food in Morocco. J Infect Developing Countries 2009;3(1): 35-40.
• 10. Bradford P.A.: Extended-Spectrum β-lactamases in the 21st century: characterization, epidemiology, and detection of this important resistance threat. Clin Microbiol Rev 2001;14: 933-951.
• 11. Butaye P., Devriese L.A., Haesebrouck: Antimicrobial growth promoters used in animal feed: effects of less well known antibiotics on Gram-positive bacteria. Clin Microbiol Rev 2003;16:175–188.
• 12. Carattoli A.: Plasmid-mediated antimicrobial resistance in Salmonella enterica. Curr Issues Mol Biol 2003;5:113–122.
• 13. Cavaco L.M., Hasman H., Xia S., Aarestrup F.M.: QnrD, a novel gene conferring transferable quinolone resistance in Salmonella enterica serovar Kentucky and Bovismorbificans strains of human origin. Antimicrob Agents Ch 2009;53(2): 603-608.
• 14. Chen S., Zhao S., White D.G., Schroeder C.M., Lu R., Yang H., McDermott P.F., Ayers S., Meng J.: Characterization of multiple-antimicrobial-resistant Salmonella serovars isolated from retail meats. Appl Environ Microb 2004;70(1):1-7.
• 15. Chen S., Cui S., McDermott P.F., Zhao S., White D.G., Paulsen I., Meng J.: Contribution of target gene mutations and efflux to decreased susceptibility of Salmonella enterica serovar Typhimurium to fluoroquinolones and other antimicrobials. Antimicrob Agents Ch 2007;51(2):535-542.
• 16. Dallal M.M.S., Doyle M. P., Rezadehbashi M., Dabiri H., Sanaei M., Modarresi S., Bakhtiari R, Sharify K., Taremi M., Zali M.R., Sharifi-Yazdi, M. K.: Prevalence and antimicrobial resistance profiles of Salmonella serotypes, Campylobacter and Yersinia spp. isolated from retail chicken and beef, Tehran, Iran. Food Control 2010;21(4):388392.
• 17. Daly M., Villa L., Pezzella C., Fanning S., Carattoli, A.: Comparison of multidrug resistance gene regions between two geographically unrelated Salmonella serotypes. J Antimicrob Chemoth 2005;55(4):558–561.
• 18. Datta N., Kontomichalou P.: Penicillinase synthesis controlled by infectious R Factors in Enterobacteriaceae. Nature 1965;208:239–241.
• 19. Davis M.A., Baker K.N.K., Orfe L.H., Shah D.H., Besser T.E., Call D.R.: Discovery of a gene conferring multiple-aminoglycoside resistance in Escherichia coli. Antimicrob Agents Ch 2010;54:2666–2669.
• 20. Deekshit V.K., Kumar B.K., Rai P., Srikumar S., Karunasagar I.: Detection of class 1 integrons in Salmonella Weltevreden and silent antibiotic resistance genes in some seafood-associated nontyphoidal isolates of Salmonella in south-west coast of India. J Appl Microbiol 2012;112(6):1113–1122.
• 21. Diaz-Torrez M.L., McNab R., Spratt D.A., Villedieu A., Hun, N., Wilson M., Mullany, P.: Novel tetracycline resistance determinant from the oral metagenome. Antimicrob Agents Ch 2003;47:1430–1432.
• 22. ECDC/EMEA Joint Technical Report. The bacterial challange: time to react. A call to narrow the gap between multidrug-resistant bacteria in the EU and the development of new antibacterial agents. Stockholm, September 2009.
• 23. EFSA. Analysis of the baseline survey on the prevalence of Campylobacter in broiler batches and of Campylobacter and Salmonella on broiler carcasses in the EU, 2008. Part B Campylobacter. EFSA Journal 2010;8:1-132.
• 24. EFSA and ECDC. The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-borne Outbreaks in 2011. EFSA Journal 2013;11(4): 3129
• 25. EFSA and ECDC. The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-borne Outbreaks in 2014. EFSA Journal 2015;13(12):4329.
• 26. Fabrega A., Sanchez-Cespedes J., Soto, S. and Vila, J.: Quinolone resistance in the food chain. Int J Antimicrob Ag 2008;31:307-315.
• 27. Ferguson G.C., Heinemann J.A., Kennedy M.A.: Gene transfer between Salmonella enterica serovar Typhimurium inside epithelial cells. J Bacteriol 2002;184:2235–2242.
• 28. Frye J.G., Jackson C.R.: Genetic mechanisms of antimicrobial resistance identified in Salmonella enterica, Escherichia coli, and Enteroccocus spp. isolated from U.S. food animals. Frontiers in microbiology 2013;4:135.
• 29. Galimand M., Sabtcheva S., Courvalin P., Lambert T.: World-wide disseminated armA aminoglycoside resistance methylase gene is borne by composite transposon Tn1548. Antimicrob Agents Ch 2005;49:2949– 2953.
• 30. Gebreyes W.A., Altier C.: Molecular characterization of multi-drug-resistant Salmonella enterica subsp. enterica serovar Typhimurium isolates from swine. J Clin Microbiol 2002;40:2813– 2822.
• 31. Giraud E., Cloeckaert A., Kerboeuf D., Chaslus-Dancla E.: Evidence for active efflux as the primary mechanism of resistance to ciprofloxacin in Salmonella enterica serovar Typhimurium. Antimicrob Agents Ch 2000;44:1223-1228
• 32. Granier S.A, Hidalgo L., San Millan A., Escudero J.A., Gutierrez B., Brisabois A., Gonzalez-Zorn B.: ArmA methyltransferase in a monophasic Salmonella enterica isolate from food. Antimicrob Agents Ch 2011;55:5262–5266.
• 33. Grave K., Torren-Edo J., Mackay D.: Comparison of the sales of veterinary antibacterial agents between 10 European countries. Antimicrob Agents Ch 2010;65:2037-2040.
• 34. Guerra B., Junker E., Helmuth R.: Incidence of the recently described sulfonamide resistance gene sul3 among German Salmonella enterica strains isolated from livestock and food, Antimicrob Agents Ch 2004;48:2712–2715.
• 35. Hammerl J.A., Beutlich J., Hertwig S., Mevius D., Threlfall E.J., Helmuth,R., Guerra, B.: pSGI15, a small ColE-like qnrB19 plasmid of a Salmonella enterica serovar Typhimurium strain carrying Salmonella genomic island 1 (SGI1). J Antimicrob Ch 2010;65:173–175.
• 36. Hansen L.H., Johannesen E., Burmolle M., Sorensen A.H., Sorensen S.J.: Plasmid-encoded multidrug efflux pump conferring resistance to olaquindox in Escherichia coli. Antimicrob Agents Ch 2004;48:3332–3337.
• 37. Hopkins K.L., Escudero J.A., Hidalgo L., Gonzalez-Zorn B.: 16S rRNA methyltransferase RmtC in Salmonella enterica serovar Virchow. Emerg Infect Dis 2010;16:712–715.
• 38. Hsu S.C., Chiu T.H., Pang J.C., Hsuan-Yuan C.H., Chang G.N., Tsen H.Y.: Characterization of antimicrobial resistance patterns and class 1 integrons among Eschericha coli and Salmonella enterica serovar Choleraesuis isolates isolated from humans and swine in Taiwan. Int J Antimicrobl Ag 2006;27:383–391.
• 39. Huovinen P., Sundstrom L., Swedberg G., Skold O.: Trimethoprim and sulfonamide resistance. Antimicrob Agents Ch 1995;39:279–289.
• 40. Islam M., Morgan J., Doyle M.P., Phatak S.C., Millner P., Jiang X.: Persistence of Salmonella enterica serovar typhimurium on lettuce and parsley and in soils on which they were grown in fields treated with contaminated manure composts or irrigation water. Foodborne Pathog Dis 2004;1:27-35.
• 41. Jacoby G.A.: AmpC β-Lactamases. Clin Microbiol Rev 2009;22:161-182.
• 42. Jacoby G., Cattoir V., Hooper D., Martinez-Martine, L., Nordmann P., Pascual A., Poirel L.,Wang M.L: Qnr gene nomenclature. Antimicrob Agents Ch 2008;52:2297-2299.
• 43. Kakatkar A.S., Pansare L.S., Gautam R.K., Shashidhar R., Karani M., Bandekar J.R.: Molecular characterization of antibiotic resistant Salmonella isolates from Indian foods. Food Res Int 2011;44:3272–3275.
• 44. Karczmarczyk M., Martins M., McCusker M., Mattar S., Amaral L., Leonard N., Aarestrup F.M., Fanning S.: Characterization of antimicrobial resistance in Salmonella enterica food and animal isolates from Colombia: identification of a qnrB19-mediated quinolone resistance marker in two novel serovars. FEMS Microbiol Lett 2010;313(1):10–19.
• 45. Leverstein-van Hall M.A., Dierikx C.M., Cohen Stuart J., Voets G.M., van den Munckhof M.P., van Essen-Zandbergen, A., Platteel, T., Fluit, A. C., van de Sande-Bruinsma, N., Scharinga, J., Bonten, M. J., Mevius, D. J.; National ESBL surveillance group.: Dutch patients, retail chicken meat and poultry share the same ESBL genes, plasmids and strains. Clin Microbiol Infect 2011;17:873-80.
• 46. Levy S.B., McMurry M., Barbosa T.M., Burdett V., Courvalin P., Hillen W., Roberts M.C., Rood J.I., Taylor D.E.: Nomenclature for new tetracycline resistance determinants. Antimicrob Agents Ch 1999;43:1523-1524.
• 47. Levy S.B.: The antibiotic paradox, 2nd ed. Cambridge, Perseus Publishing Services, 2002.
• 48. Little C.L., Richardson J.F., Owen R.J., de Pinna E., Threlfall E.J.: Campylobacter and Salmonella in raw red meats in the United Kingdom: prevalence, characterization and antimicrobial resistance pattern, 2003-2005. Food Microbiol 2008;25(3):538–543.
• 49. Martinez-Martinez L., Pascual A., Jacoby G.A.: Quinolone resistance from a trensferable plasmid. Lancet 1998;351:797-799.
• 50. Mayrhofer S., Paulsen P., Smulders F.J.M., Hilbert F.: Antimicrobial resistance profile of five major foodborne pathogens isolated from beef, pork and poultry. Int J Food Microbiol 2004;97:23–29.
• 51. Mąka Ł., Maćkiw E., Ścieżyńska H., Pawłowska K., Popowska M.: Antimicrobial susceptibility of Salmonella strains isolated from retail meat products in Poland between 2008 and 2012. Food Control 2014;36:199–204.
• 52. Mąka Ł., Maćkiw E., Ścieżyńska H., Popowska M.: Occurrence and antimicrobial resistance of Salmonella spp. isolated in Poland from food other than meat. Ann Agr Env Med 2015;22(3): 403-408.
• 53. Mąka Ł., Ścieżyńska H., Grochowska A., Pawłowska K., Windyga B., Karłowski K.: Antimicrobial susceptibility of Salmonella strains isolated from food in Poland. Bromat Chem Toksykol 2010;42(3):260-265 (in Polish).
• 54. Medeiros M.A.N., Oliveira D.C.N., Rodrigues D.P., Freitas D.R.C.: Prevalence and antimicrobial resistance of Salmonella in chicken carcasses at retail in 15 Brazilian cities. Rev Panam Salud Publica 2011;30(6):555–560.
• 55. Mellon M., Benbrook C., Benbrook K.L.: Hogging it: estimates of antimicrobial abuse in livestock. Cambridge, MA, Union of Concerned Scientists, 2001. http://www.ucsusa.org/assets/documents/food_and_ agriculture/hog_front.pdf (Accessed 11 July 2016)
• 56. Mezali L., Hamdi T.M.: Prevalence and antimicrobial resistance of Salmonella isolated from meat and meat products in Algiers (Algeria). Foodborne Pathog Dis 2012;9:522–529.
• 57. Michalova E., Novotna P., Schlegelova J.: Tetracyclines in veterinary medicine and bacterial resistance to them. Vet Med–Czech 2004;49:79-100.
• 58. Miko A., Pries K., Schroeter A., Helmuth R.: Molecular mechanisms of resistance in multidrug-resistant serovars of Salmonella enterica isolated from foods in Germany. J Antimicrob Chemoth 2005;56:1025–1033.
• 59. Mølbak K.: Spread of resistant bacteria and resistance genes from animals to humans-the public health consequences. J Vet Med B Infect Dis Vet Public Health 2004;51:364-369.
• 60. Mürmann L., dos Santos M.C., Cardoso M.: Prevalence, genetic characterization and antimicrobial resistance of Salmonella isolated from fresh pork sausages in Porto Alegre, Brazil. Food Control 2009;20:191–195.
• 61. Nordmann P., Poirel L. Emergence of plasmid-mediated resistance to quinolones in Enterobacteriaceae. J Antimicrob Chemoth 2005;56:463-469.
• 62. The OzFoodNet Working Group. Monitoring the incidence and causes of diseases potentially transmitted by food in Australia: Annual report of the OzFoodNet network, 2010. Communicable Diseases Intelligence 2012;36:E213.
• 63. Philippon A., Arlet G., Jacoby G.A.: Plasmid-determined AmpC-type β-lactamases, Antimicrob Angents Ch 2002;46:1-11.
• 64. Popowska M., Krawczyk-Balska A.: Broad-host-range IncP-1 plasmids and their resistance potential. Frontiers in Microbiology 2013;4:Article number 44.
• 65. Robicsek A., Jacoby G.A, Hooper D.C.: The worldwide emergence of plasmid-mediated quinolone resistance. The Lancet Infect Dis 2006a;6(10):629–640.
• 66. Robicsek A., Strahilevitz J., Jacoby G.A., Macielag M., Abbanat D., Park C.H., Bush K., Hooper D.C.: Fluoroquinolone-modyfying enzyme: a new adaptation of a common aminoglycoside acetyltransferase. Nat Med 2006b;12:83-88.
• 67. Rodríguez I., Barownick W., Helmuth R., Mendoza M.C., Rodicio M.R., Schroeter A., Guerra B.: Extendedspectrum β-lactamases and AmpC β-lactamases in ceftiofur-resistant Salmonella enterica isolates from food and livestock obtained in Germany during 2003-07. J Antimicrob Chemoth 2009;64:301–309.
• 68. Rychlik I., Gregorova D., Hradecka H.: Distribution and function of plasmids in Salmonella enterica. Vet Microbiol 2006;112:1–10.
• 69. Scallan E., Hoekstra R.M., Angulo F.J., Tauxe R.V., Widdowson M.-A., Roy S.L., Jones J.L., Griffin P.M.: Foodborne illness acquired in the United States – major pathogens. Emerg Infect Dis 2011;17:7-15.
• 70. Singh S., Yadav A.S., Singh S.M., Bharti P.: Prevalence of Salmonella in chicken eggs collected from poultry farms and marketing channels and their antimicrobial resistance. Food Res Int 2010;43:2027–2030.
• 71. Sköld O.: Sulfonamide resistance: mechanisms and trends. Drug Resist Update 2000;3:155-160.
• 72. Sørensen A.H., Hansen L.H., Johannesen E., Sørensen S.J.: Conjugative plasmid conferring resistance to olaquindox. Antimicrob Agents Ch 2003;47:798–799.
• 73. Stevens A., Kaboré Y., Perrier-Gros-Claude J.-D., Millemann Y., Brisabois A., Catteau M., Cavin J.-F., Dufour B.: Prevalence and antibiotic-resistance of Salmonella isolated from beef sampled from the slaughterhouse and from retailers in Dakar (Senegal). Int J Food Microbiol 2006;110:178–186.
• 74. Storteboom H., Arabi M., Davis J.G., Crimi B., Pruden A.: Tracking antibiotic resistance genes in the South Platte River basin using molecular signatures of urban, agricultural, and pristine sources. Environ Sci Technol 2010;44:7397-7404.
• 75. Szych J., Wołkowicz T., La Ragione R., Madajczak G.: Impact of antibiotics on the intestinal microbiota and of shiga-toxin-producing Escherichia coli and Salmonella infections treatment. Curr Pharm Des, 2014;20(28):4535-4548.
• 76. Ścieżyńska H., Maćkiw E., Mąka Ł., Pawłowska K.: Nowe zagrożenia mikrobiologizne w żywności. [The new microbiological hazards in food]. Rocz Panstw Zakl Hig 2012; 63(4):397-402 (in Polish).
• 77. Thai T.H., Hirai T., Lan N.T., Shimada A., Ngoc P.T., Yamaguchi R.: Antimicrobial resistance of Salmonella serovars isolated from beef at retail markets in the North Vietnam. Journal Vet Med Sci 2012a;74:1163-1169.
• 78. Thai T.H., Hirai T., Lan N.T., Yamaguchi R.: Antibiotic resistance profiles of Salmonella serovars isolated from retail pork and chicken meat in North Vietnam. Int J Food Microbiol 2012b;156:147–151.
• 79. Thong K.L., Modarressi S.: Antimicrobial resistant genes associated with Salmonella from retail meats and street foods. Food Res Int 2011;44:2641–2646.
• 80. Van T.T.H., Moutafis G., Tran L.T., Coloe P. J.: Antibiotic resistance in food-borne bacterial contaminants in Vietnam. Appl Environ Microb 2007;73:7906–11.
• 81. Van T.T.H., Nguyen H.N.K., Smooker P.M., Coloe P.J.: The antibiotic resistance characteristics of non-typhoidal Salmonella enterica isolated from food-producing animals, retail meat and humans in South East Asia. Int J Food Microbiol 2012;154:98–106.
• 82. Veldman K., Cavaco L.M., Mevius D., Battisti A., Franco A., Botteldoorn N., Bruneau M., Perrin-Guyomard A., Cerny T, De Frutos Escobar C., Guerra B., Schroeter A., Gutierrez,M., Hopkins K., Myllyniemi A.-L., Sunde M., Wasy, D., Aarestrup F.M.: International collaborative study on the occurrence of plasmidmediated quinolone resistance in Salmonella enterica and Escherichia coli isolated from animals, humans, food and the environment in 13 European countries. J Antimicrob Chemoth 2011;66:1278–1286.
• 83. Villa L., Mammina C., Miriagou V., Tzouvelekis L.S., Tassios P.T., Nastasi A., Carattoli A. Multidrug and broad-spectrum cephalosporin resistance among Salmonella enterica serotype Enteritidis clinical isolates in southern Italy. J Clin Microbiol 2002;40:2662-2665.
• 84. Villegas M.V, Lolans K., Correa A., Suarez C.J., Lopez J.A., Vallejo M., Quinn J.P., Colombian Nosocomial Resistance Study Group: First detection of the plasmidmediated class A carbapenemase KPC-2 in clinical isolates of Klebsiella pneumoniae from South America. Antimicrob Agents Ch 2006;50:2880–2882.
• 85. Voetsch A.C., Van Gilder T J, Angulo F J., Farley M.M., Shallow S., Marcus R., Cieslak P.R., Deneen V.C., Tauxe R.V.: FoodNet estimate of the burden of illness caused by nontyphoidal Salmonella infections in the United States. Clin Infect Dis 2004;38(Suppl. 3):S127-S134.
• 86. Wachtel M.R., Whitehand L.C., Mandrell R.E.: Prevalence of Escherichia coli associated with a cabbage crop inadvertently irrigated with partially treated sewage wastewater. J Food Prot 2002;65:471-475.
• 87. Wasyl D., Hoszowski, A.: First isolation of ESBLproducing Salmonella and emergence of multiresistant Salmonella Kentucky in turkey in Poland. Food Res Int 2012;45:958–961.
• 88. Wiesner M., Zaidi M.B., Calva E., Fernández-Mora M., Calva J.J., Silva C.: Association of virulence plasmid and antibiotic resistance determinants with chromosomal multilocus genotypes in Mexican Salmonella enterica serovar Typhimurium strains. BMC Microbiol 2009;9:131.
• 89. Winokur P.L., Brueggemann A., DeSalvo D.L., Hoffmann L., Apley M.D., Uhlenhopp E.K., Pfaller M.A., Doern G.V.: Animal and human multidrug-resistant, cephalosporin-resistant Salmonella isolates expressing a plasmid-mediated CMY-2 AmpC β-Lactamase. Antimicrob Agents Ch 2000;44:2777-2783.
• 90. Wong M.H.Y., Chen S.: First detection of oqxAB in Salmonella spp. isolated from food. Antimicrob Agents Ch 2013;57:658–60.
• 91. World Health Organization (WHO), The Regional Office for Europe: Tackling antibiotic resistance from a food safety perspective in Europe. 2011.
• 92. Yan H., Li L., Alam M.J., Shinoda S., Miyoshi S.-I., Shi L. Prevalence and antimicrobial resistance of Salmonella in retail foods in northern China. Int J Food Microbiol 2010;143:230-234.
• 93. Yang B., Qu D., Zhang X., Shen J., Cui S., Shi Y., Xi M., Sheng M., Zhi S., Meng J.: Prevalence and characterization of Salmonella serovars in retail meats of marketplace in Shaanxi, China. Int J Food Microbiol 2010;141:63-72.
• 94. Yang B., Xi M., Cui S., Zhang X., Shen J., Sheng M., Qu D., Wang X., Meng J.: Mutations in gyrase and topoisomerase genes associated with fluoroquinolone resistance in Salmonella serovars from retail meats. Food Res Int 2012;45:935–939.
• 95. Yamane K., Wachino J., Suzuki S., Kimura K., Shibata N., Kato H., Shibayama K., Konda T., Arakawa Y.: New plasmid-mediated fluoroquinolone efflux pump, QepA, found in an Escherichia coli clinical isolate. Antimicrob Agents Ch 2007;51:3354–3360.
• 96. Yildirim Y., Gonulalan Z., Pamuk S., Ertas N.: Incidence and antibiotic resistance of Salmonella spp. on raw chicken carcasses. Food Res Int 2011;44:725–728.
• 97. Zewdu E., Cornelius P.: Antimicrobial resistance pattern of Salmonella serotypes isolated from food items and personnel in Addis Ababa, Ethiopia. Trop Anim Health Pro 2009;41:241–249.
• 98. Zhao S., White D.G., Friedman S.L., Glenn A., Blickenstaff K., Ayers S.L., Abbott J.W., Hall-Robinson E., McDermott P.F.: Antimicrobial resistance in Salmonella enterica serovar Heidelberg isolates from retail meats, including poultry, from 2002 to 2006. Appl Environ Microb 2008;74:6656-6662.