Buradasınız

Antibiyotik Dirençli Enterobacteriaceae’lerin Hayvan ve İnsan Sindirim Sistemi Arasında in vivo Plazmit Transferinden Kaynaklı Geçişi

Transmission of Antibiotic Resistant Enterobacteriaceae between Animals and Humans Gastrointestinal Tract with the Evidence of in vivo Plasmid Transfer

Journal Name:

Publication Year:

Keywords (Original Language):

Abstract (2. Language): 
Recently, the main point of discussion is being undertaken whether the resistance of bacteria and plasmids could have been transmitted to humans from animals. Using antimicrobials in livestock production was previously shown to be followed by the occurrence of the resistant bacteria in the treated animals as well as in humans (caretakers, their family members etc.). Evidences exist that the transmission of resistance might have taken place from animals to humans. Many of these evidences were not direct and were based on the similarities between the resistance profiles of bacteria (among others indicatory E. coli) isolated from animals (poultry, pigs, cattle) and from humans having contact with these animals (farm workers, animal caretakers, their family members). Direct evidences have been based on the molecular methods allowing the detection of either clonally related, resistant zoonotic bacteria in humans and animals or related to resistance of plasmids isolated from humans and animals.
Abstract (Original Language): 
Esas tartışma konusu olan nokta, bakteri ve plazmit kaynaklı bakteri direncinin hayvanlardan insanlara nasıl geçebileceğidir. Antibiyotiklerin çiftlik hayvanlarında kullanımı daha önceleri dirençli bakterilerin tedavi görmüş hayvanlarda ve insanlarda varlığını göstermiştir (hayvan bakıcıları ve çiftlik çalışanları). Direncin geçişinin hayvanlardan insanlara doğru olabileceği şeklinde kanıtlar bulunmaktadır. Bu kanıtların çoğu, direkt olmamakla birlikte hayvanlardan (çiftlik hayvanları) ve bunlarla temas halindeki insanlardan (hayvan bakıcıları ve çiftlik çalışanları) izole edilen bakteriler arasındaki direnç profillerinin benzerliklerine dayanmaktadır. Direkt kanıtlar, birbirleriyle klonal ilişkili insan ve hayvan kaynaklı dirençli zoonotik bakterilerin veya yine bunlardaki dirençle ilgili plazmitlerin moleküler metotlara dayalı olarak saptanması ile olmuştur.
32
38

REFERENCES

References: 

Abbott, J. W., Hall-Robinson, E., McDermott, P. F., 2008.
Antimicrobial resistance in Salmonella enterica
Serovar Heidelberg isolates from retail meats,
including poultry, from 2002 to 2006. Appl. Environ.
Microb. 74: 6656-6662.
Alhaj, N., Mariana, N.S., Raha, A.R., Ishak, Z., 2007.
Prevalence of antibiotic resistance among
Escherichia coli from different sources in Malaysia.
International J. Poult. Sci, 6(4): 293-297.
Allen, K. J., Poppe, C., 2002. Occurrence and
characterization of resistance to extended- spectrum
cephalosporins mediated by beta-lactamase CMY-2
in Salmonella isolated from food-producing animals
in Canada. Can J Vet Res, 66: 137-144.
Andersson, D.I., 2003. Persistence of antibiotic resistant
bacteria. Curr. Opin. Microbiol, 6(5): 452-456.
Ardiles-Villegas, K., Gonzalez-Acuna, D., Waldenstrom,
J., Olsen, B., Hernandez, J., 2011. Antibiotic
resistance patterns in fecal bacteria isolated from
Christmas shearwater (Puffinus nativitatis) and
masked booby (Sula dactylatra) at remote Easter
Island. Avian Dis. 55:486-489.
Bahl, M. I., Burmolle, M., Meisner, A., Hansen, L. H.,
Sorensen, S. J., 2009. All IncP-1 plasmid subgroups,
including the novel epsilon subgroup, are prevalent
in the influent of a Danish wastewater treatment
plant. Plasmid, 62:134-139.
Balis, E., Vatopoulos, A.C., Opoulou, M.K., Mainas, E.,
Hatzoudis, G., Kontogianni, V., Malamou-Lada, H.,
Kitsou-Kiriakopoulou, S., Kalapothaki, V., 1996.
Indications of in vitro transfer of an epidemic R
plasmid from Salmonella enteritidis to Escherichia
coli of the normal human gut flora. J. Clinic. Microb,
34(4): 977-979.
Bertrand, S., Weill, F. X., Cloeckaert, A., Vrints, M.,
Mairiaux, E., Praud, K., Dierick, K., Wildemauve,
C., Godard, C., Butaye, P., Imberechts, H., Grimont,
P. A., Collard, J. M., 2006. Clonal emergence of
extended-spectrum beta-lactamase (CTX-M-2)-
producing Salmonella enterica serovar Virchow
isolates with reduced susceptibilities to ciprofloxacin
among poultry and humans in Belgium and France
(2000 to 2003). J. Clin. Microb, 44: 2897-903.
Bettelheim, K., Thomas, G., 1997. Escherichia coli
Antibiotic Resistotypes.
http://ecoli.bham.ac.uk/path/antir.html
Boehme, S., Werner, G., Klare, I., Reissbrodt, R., Witte,
W., 2004. Occurrence of antibiotic resistant
enterobacteria in agricultural foodstuffs. Mol. Nutr.
Food Res. 48:522-531.
Boerlin, P., Travis, R., Gyles, C.L., Reid-Smith,R., Lim,
N.J.H., Nicholson, V., McEwen, S.A., Friendship, R.,
Archambault, M., 2005. Antimicrobial resistance and
virulence genes of Escherichia coli isolates from
swine in Ontario. Appl. Environ. Microbiol, 71(11):
6753-6761.
Bortolaia, V., Guardabassi, L., Bisgaard, M., Larsen, J.,
Bojesen, A. M., 2010. Escherichia coli producing
CTX-M-1, -2, and -9 group beta-lactamases in
organic chicken egg production. Antimicrob. Agents
Chemother. 54:3527-3528.
Briñas, L., Moreno, M. A., Zarazaga, M., Porrero, C.,
Saénz, Y., Garcia, M., Dominguez, L., Torres, C.,
2003. Detection of CMY-2, CTX-M-14, and SHV-12
β-lactamases in Escherichia coli faecal-sample
isolates from healthy chickens. Antimicrob Agents
Chemother, 47: 2056-2058.
Buchholz, U., Bernard, H., Werber, D., Bohmer, M. M.,
Remschmidt, C., Wilking, H., Delere, Y., An der, H.
M., Adlhoch, C., Dreesman, J., Ehlers, J., Ethelberg,
S., Faber, M., Frank, C., Fricke, G., Greiner, M.,
Hohle, M., Ivarsson, S. , Jark, U., Kirchner, M.,
Koch, J., Krause, G., Luber, P., Rosner, B., Stark, K.,
Kuhne, M., 2011. German outbreak of Escherichia
coli O104:H4 associated with sprouts. N. Engl. J.
Med. 365:1763-1770.
Burch, D., 2005. Problems of antibiotic resistance in pigs
in the United Kingdom.
http://www.thepigsite.com/articles/1/health-andwelfare/
1266/problems-of antibiotic-resistance-inpigs-
in-the-uk
KSÜ Doğa Bil. Derg., 17(1), 2014
KSU J. Nat. Sci., 17(1), 2014
36 Derleme
Review
Carattoli, A., Lovari, S., Franco, A., Cordaro, G., Matteo,
P. D., Battisti, A., 2005. Extended- spectrum β-
lactamases in Escherichia coli isolated from dogs and
cats in Rome, Italy, from 2001 to 2003. Antimicrob
Agents Chemother, 49: 833-835.
Chaslus-Dancla, E., Pohl, P., Meurisse, M., Marin, M.,
Lafont, J. P., 1991. High genetic homology between
plasmids of human and animal origins conferring
resistance to the aminoglycosides gentamicin and
apramycin. Antimicrob. Agents Chemother. 35:590-
593.
Chiaretto, G., Zavagnin, P., Bettini, F., Mancin, M.,
Minorello, C., Saccardin, C., Ricci, A. 2008.
Extended-spectrum β-lactamase SHV-12-producing
Salmonella from poultry. Vet Microb, 128: 406-413.
Chmelnitsky, I., Carmeli, Y., Leavitt, A., Schwaber, M. J.,
Navon-Venezia, S., 2005. CTX-M-2 and a new CTXM-
39 enzyme are the major extended-spectrum betalactamases
in multiple Escherichia coli clones
isolates in Tel Aviv, Israel. Antimicrob Agents
Chemother 49: 4745-4750.
Cloeckaert, A., Praud, K., Doublet, B., Bertini, A.,
Carattoli, A., Butaye, P., Imberechts, H., Bertrand,
S., Collard, J. M., Arlet, G., Weill, F. X., 2007.
Dissemination of an extended-spectrum-betalactamase
blaTEM-52 gene-carrying IncI1 plasmid in
various Salmonella enterica serovars isolated from
poultry and humans in Belgium and France between
2001 and 2005. Antimicrob. Agents Chemother.
51:1872-1875.
Costa, D., Poeta, P., Brinas, L., Saenz, L., Rodrigues, J.,
Torres, C., 2004. Detection of CTX-M-1 and TEM-
52 β-lactamases in Escherichia coli strains from
healthy pets in Portugal. J Antimicrob Chemother,
54: 960-961.
Costa, D., Poeta, P., Saenz, Y., Vinué, L., Rojo-Bezares,
B., Jouini, A., Zarazaga, M., Rodrigues, J., Torres,
C.,2006. Detection of Escherichia coli harbouring
extended-spectrum β- lactamases of the CTX-M,
TEM and SHV classes in faecal samples of wild
animals in Portugal. J Antimicrob Chemother, 58:
1311-1312.
Costa, D., Vinué, L., Poeta, P., Coelho, A. C., Matos, M.,
Saénz, Y., Somalo, S., Zarazaga, M., Rodrigues, J.,
Torres, C., 2009. Prevalence of extended-spectrum
beta-lactamase producing Escherichia coli isolates in
faecal samples of broilers. Vet Microb, 138: 339-
344.
Donaldson, S. C., Straley, B. A., Hegde, N. V., Sawant, A.
A., Debroy, C., Jayarao, B. M., 2006. Molecular
epidemiology of ceftiofur-resistant Escherichia coli
isolates from dairy calves. Appl Environm Microbiol,
72: 3940-3948.
Duan, R.S., Sit, T.H., Wong, S.S., Wong, R.C., Chow,
K.H., Mak, G.C., Yam, W.C., Ng, L.T., Yuen, K.Y.,
Ho, P.L., 2006. Escherichia coli producing CTX-M
beta-lactamases in food animals in Hong Kong.
Microb Drug Res, 12: 145-148.
Freter, R., Freter, R.R., Brickner, H., 1983. Experimental
and mathematical models of Escherichia coli plasmid
transfer in vitro and in vivo. Infect. Immu, 39(1): 60-
84.
Girlich, D., Poirel, L., Carattoli, A., Kempf, I., Lartigue,
M. F., Bertini, A., Normann, P., 2007. Extendedspectrum
β-lactamase CTX-M-1 in Escherichia coli
isolates from healthy poultry in France. Appl Environ
Microb, 73: 4681-4685.
Hasman, H., Mevius, D., Veldman, K., Olesen, I.,
Aarestrup, F. M., 2005. β-lactamases amoung
extended-spectrum β-lactamase (ESBL)-resistant
Salmonella from poultry, poultry products and
human patients in the Netherlands. J Antimicrob
Chemother, 56: 115 121.
Hernadez, J. R., Martinez-Martinez, L., Canton, R.,
Coque, T. M., Pascual, A., Spanish Group for
Nosocomial Infections (GEIH)., 2005. Nationwide
study of Escherichia coli and Klebsiella pneumoniae
producing extended-spectrum β-lactamases in Spain.
Antimicrob Agents Chemother, 49:2122-2125.
Heuer, H., Schmitt, H., Smalla, K., 2011. Antibiotic
resistance gene spread due to manure application on
agricultural fields. Curr. Opin. Microbiol. 14:236-
243.
Ho, P. L., Ho, A. Y. M., Chow, K. H., Wong, R. C. W.,
Duan, R. S., Ho, W. L., Mak, G. C., Tsang, K. W.,
Yam, W. C., Yuen, K. Y., 2005. Occurrence and
molecular analysis of extended-spectrum β-
lactamase-producing Proteus mirabilis in Hong
Kong, 1999-2002. J Antimicrob Chemother, 55: 840-
845.
Holmberg, S. D., Osterholm, M. T., Senger, K. A., Cohen,
M. L., 1984. Drug-resistant Salmonella from animals
fed antimicrobials. N. Engl. J. Med. 311:617-622.
Hummel, R., Tschape, H., Witte, W., 1986. Spread of
plasmid-mediated nourseothricin resistance due to
antibiotic use in animal husbandry. J. Basic
Microbiol. 26:461-466.
Jonathan, A., 2001. The development of antibiotic
resistance in Escherichia coli.
http://share3.esd105.wednet.edu/mcmillend/02SciPro
j/jonathana/JonathanA.htm
Jouini, A., Vinué, L., Slama, K. B., Saénz, Y., Klibi, N.,
Hammami, S., Boudabous, A., Torres, C., 2007.
Characterization of CTX-M and SHV extendedspectrum
β-lactamases and associated resistance
genes in Escherichia coli strains of food samples in
Tunesia. J Antimicrob Chemother 60: 1137-1141.
KSÜ Doğa Bil. Derg., 17(1), 2014
KSU J. Nat. Sci., 17(1), 2014
37 Derleme
Review
Khan, A. A., Nawaz, M. S., Summage, W. C., Khan, S.
A., Lin, J., 2005. Isolation and molecular
characterization of fluoroquinolone-resistant
Escherichia coli from poultry litter. Poult. Sci. 84:61-
66.
Kiratisin, P., Apisarnthanarak, A., Laesripa, C., Saifon, P.,
2008. Molecular characterization and epidemiology
of extended-spectrum-beta-lactamase-producing
Escherichia coli and Klebsiella pneumoniae isolates
causing health care-associated infection in Thailand,
where the CTX-M family is endemic. Antimicrob
Agents Chemother, 52: 2818-2824.
Kojima, A., Ishii, Y., Ishihara, K., Esaki, H., Asai, T.,
Oda, C., Tamura, Y., Takahashi, T., Yamaguchio, K.,
2005. Extended-spectrum-β-lactamase-producing
Escherichia coli strains isolated from farm animals
from 1999 to 2002: report from the Japanese
veterinary antimicrobial resistance monitoring
program. Antimicrob Agents Chemother, 49: 3533-
3537.
Kruger, T., Szabo, D., Keddy, K. H., Deeley, K., Marsh, J.
W., Hujer, A. M., Bonomo, R. A., Paterson, D. L.,
2004. Infections with nontyphoidal Salmonella
species producing TEM-63 or a novel TEM enzyme,
TEM-131, in South Africa. Antimicrob Agents
Chemother, 48: 4263-4270.
Leverstein-van Hall, M. A., Dierikx, C. M., Cohen, S. J.,
Voets, G. M., Van den Munckhof, M. P., Essen-
Zandbergen, A., Platteel, T., Fluit, A. C., Sande-
Bruinsma, N., Scharinga, J., Bonten, M. J., Mevius,
D. J., 2011. Dutch patients, retail chicken meat and
poultry share the same ESBL genes, plasmids and
strains. Clin. Microbiol. Infect. 17:873-880.
Levy, S. B., FitzGerald, G. B., Macone, A. B., 1976.
Spread of antibiotic-resistant plasmids from chicken
to chicken and from chicken to man. Nature 260:40-
42.
Licht, T.R., Christensen, B.B., Krogfelt, K.A., Molin, S.,
1999. Plasmid transfer in the animal intestine and
other dynamic bacterial populations: the role of
community structure and environment. Microbiol,
145: 2615-2622.
Lim, S.K., Lee, H.S., Nam, H.M., Cho, Y.S., Kim, J.M.,
Song, S.W., Park, Y.H., Jung, S.C., 2007.
Antimicrobial resistance observed in Escherichia coli
strains isolated from fecal samples of cattle and pigs
in Korea during 2003–2004. Int. J. Food Microbiol,
116(2): 283-286.
Machado, E., Coque, T. M., Canton, R., Sousa, J. C.,
Peixe, L., 2008. Antibiotic resistance integrons and
extended-spectrum β-lactamases among
Enterobacteriaceae isolates recovered from chickens
and swine in Portugal. J Antimicrob Chemother, 62:
296-302.
Madec, J. Y., Lazizzera, C., Châtre, P., Meunier, D.,
Martin, S., Lepage, G., Ménard, M. F., Lebreton, P.,
Ramboud, T., 2008. Prevalence of fecal carriage of
acquired-expanded-spectrum cephalosporin
resistance in Enterobacteriaceae strains from cattle
in France. J Clin Microb, 46:1566-1567.
Madec, J. Y., Poirel, L., Saras, E., Gourguechon, A.,
Girlich, D., Nordmann, P., Haenni, M., 2012. Non-
ST131 Escherichia coli from cattle harbouring
human-like blaCTX-M-15-carrying plasmids. J.
Antimicrob. Chemother. 67:578-581.
Mammeri, H., Loo, M.V.D., Poirel, L., Martinez-
Martinez, L., Nordmann, L., 2005. Emergence of
plasmid-mediated quinolone resistance in
Escherichia coli in Europe. Antimicrob. Agents
Chemother. 49(1): 71–76.
Marshall, B. M., Levy, S. B., 2011. Food animals and
antimicrobials: impacts on human health. Clin.
Microbiol. Rev. 24:718-733.
Mathew, A.G., Saxton, A.M., Upchurch, W.G., Chattin,
S.E., 1999. Multiple antibiotic resistance patterns of
Escherichia coli isolates from swine farms. Appl.
Environ. Microbiol, 65(6): 2770-2772.
Mayrhofer, S., Paulsen, P., Smulders, F.J.M., Hilbert, F.,
2006. Short Communication: Antimicrobial
resistance in commensal Escherichia coli isolated
from muscle foods as related to the veterinary use of
antimicrobial agents in food-producing animals in
Austria. Microbial Drug Resistance, 12(4): 278 -283.
Miles, T. D., McLaughlin, W., Brown, P.D., 2006.
Antimicrobial resistance of Escherichia coli isolates
from broiler chickens and humans. BMC Vet. Res,
2:7.
Nirdnoy, W., 2005. The contribution of plasmids to
antibiotic resistance in Campylobacter jejuni.
Mahidol University, Faculty of graduate studies,
Bangkok, Thailand. Dissertation.
Petridis, M., Bagdasarian, M., Waldor, M. K., Walker, E.,
2005. Horizontal transfer of shiga toxin and
antibiotic resistance genes among Escherichia coli
strains in house fly (Diptera: Muscidae) gut. J. Med.
Entomol, 43(2): 288–295.
Rasko, D. A., Webster, D. R., Sahl, J. W., Bashir, A.,
Boisen, N., Scheutz, F., Paxinos, E. E., Sebra, R.,
Chin, C. S., Iliopoulos, D., Klammer, A., Peluso, P.,
Lee, L., Kislyuk, A. O., Bullard, J., Kasarskis, A.,
Wang, S., Eid, J., Rank, D., Redman, J. C., Steyert,
S. R., Frimodt-Moller, J., Struve, C., Petersen, A. M.,
Krogfelt, K. A., Nataro, J. P., Schadt, E. E., Waldor,
M. K., 2011. Origins of the E. coli strain causing an
outbreak of hemolytic-uremic syndrome in Germany.
N. Engl. J. Med. 365:709-717.
Rayamajhi, N., Kang, S. G., Lee, D. Y., Kang, M. L., Lee,
S. I., Park, K. Y., Lee, H. S., Yoo, H. S., 2008.
KSÜ Doğa Bil. Derg., 17(1), 2014
KSU J. Nat. Sci., 17(1), 2014
38 Derleme
Review
Characterization of TEM-, SHV- and AmpC-type β-
lactamases from cephalosporin- resistant
Enterobacteriaceae isolated from swine. Int J Food
Microb, 124:183-187.
Riaño, I., Moreno, M. A., Teshager, T., Saenz, Y.,
Dominguez, L., Torres, C., 2006. Detection and
characterization of extended-spectrum β-lactamases
in Salmonella enterica strains of healthy food
animals in Spain. J Antimicrob Chemother, 58: 844-
847.
Sayah, R.S., Kaneene, J.B., Johnson, Y., Miller, R.A.,
2005. Patterns of antimicrobial resistance observed in
Escherichia coli isolates obtained from domestic- and
wild-animal fecal samples, human septage, and
surface water. Appl. Environ. Microbiol, 71(3):
1394–1404.
Schjørring, S., Struve, C., Krogfelt, K.A., 2005. Plasmid
transfer from Klebsiella pneumoniae to Escherichia
coli. 15th European Congress of Clinical
Microbiology and Infectious Diseases. 2-5th April,
Copenhagen, Denmark.
http://www.blackwellpublishing.com/eccmid15/abstr
act.asp?id=37125
Schröder, C., 2004. Antimicrobial resistance in
Escherichia coli isolates in a large German
community-based hospital 1998–2003 - trends
correlated with antimicrobial use. 14th European
Congress of Clinical Microbiology and Infectious
Diseases (ESCMID), 1-4 May, Prague.
http://www.blackwellpublishing.com/eccmid14/abstr
act.asp?id=15619.
Shiraki, Y., Shibata, N., Doi, Y., Arakawa, Y., 2004.
Escherichia coli producing CTX-M-2 betalactamase
in cattle, Japan. Emerg Infect Dis, 10: 69-
75.
Smet, A., Martel, A., Persoons, D., Dewulf, J.,
Heyndrickx, M., Catry, B., Herman, L.,
Haesebrouck, F., Butaye, P., 2008. Diversity of
extended-spectrum β-lactamases and class C β-
lactamases among cloacal Escherichia coli in
Belgian broiler farms. Antimicrob Agents
Chemother, 52: 1238-1243.
Sunde, M., Sorum, H., 2001. Self-transmissible multidrug
resistance plasmids in Escherichia coli of the
normal intestinal flora of healthy swine. Microb.
Drug Resist, 7(2): 191-196.
Tian, G.B., Wang, H.N., Zou, L.K., Tang, J.N., Zhao,
Y.W., Ye, M.Y., Tang, J.Y., Zhang, Y., Zhang, A.Y.,
Yang, X., Xu, C.W., Fu, Y.J., 2009. Detection of
CTX-M-15, CTX-M-22 and SHV-2 extendedspectrum
β-lactamases (ESBLs) in Escherichia coli
fecal sample isolates from pig farms in China.
Microb Drug Res, 3: 297-304.
Umolu, P.I., Ohenhen, E.R., Okwu, I.G., Ogiehor, I.S.,
2006. Multiple Antibiotic resistant index and plasmid
of Escherichia coli in beef in Ekpoma. Am. J. Sci,
2(3): 1-4.
VSPA (World Society for the Protection of Animals),
2006. Resistant bacteria in people and farm animals
around the world.
http://wspafarmwelfare.org/hhantibiotics.html
Winokur, P. L., Bruegegemann, A., DeSalvo, D. L.,
Hoffmann, L., Apley, M. D., Uhlenhopp, E. K.,
Pfaller, M. A., Doern, G. V., 2000. Animal and
human multidrug-resistant Salmonella isolates
expressing a plasmid-mediated CMY-2 AmpC β-
lactamase. Antimicrob Agents Chemother, 44: 2777-
2783.
Wu, S., Chouliara, E., Hasman, H., Dalsgaard, A., Vieira,
A., Jensen, L. B., 2008. Detection of a single isolate
of CTX-M-1-producing Escherichia coli from
healthy pigs in Denmark. J. Antimicrob. Chemother.
61:747-749.
Wu, S., Dalsgaard, A., Vieira, A. R., Emborg, H. D.,
Jensen, L. B., 2009. Prevalence of tetracycline
resistance and genotypic analysis of populations of
Escherichia coli from animals, carcasses and cuts
processed at a pig slaughterhouse. Int. J. Food
Microbiol. 135:254-259.
Yan, S.S., Gilbert, J.M., 2004. Antimicrobial drug
delivery in food animals and microbial food safety
concerns: An overview of in vitro and in vivo factors
potentially affecting the animal gut micro flora. Adv.
Drug. Deliv. Rev, 56(10): 1497-1521.
Zhao, S., Blickenstaff, K., Bodeis-Jones, S., Gaines, S. A.,
Tong, E., McDermott, P. F., 2012. A Comparison of
the Prevalence and Antimicrobial Resistance of
Escherichia coli from Different Retail Meats in the
United States: 2002-2008. Appl. Environ. Microbiol.
78(6), 1701-1707.
http://dx.doi.org/10.1128/AEM.07522-11
Zhao, S., White, D. G., Friedman, S. L., Glenn, A.,
Blickenstaff, K., Ayers, S. L., Abbott J.W, Hall-
Robinson E, McDermott P.F. 2008. Antimicrobial
resistance in Salmonella enterica serovar Heidelberg
isolates from retail meats, including poultry, from
2002 to 2006. Appl Environ. Microbiol. 74 (21):6656-
62. doi: 10.1128/AEM.01249-08. Epub 2008 Aug 29.

Thank you for copying data from http://www.arastirmax.com