Rearch Note
Antimicrobial Resistance in Escherichia coli Isolated from Retail
Milk-Fed Veal Meat from Southern Ontario,Canada
ANGELA COOK,1,2*RICHARD J.REID-SMITH,2,3REBECCA J.IRWIN,3SCOTT A.M C EWEN,2VIRGINIA YOUNG,3
KELLY BUTT,2AND CARL RIBBLE 2{
1Laboratoryyth
for Foodborne Zoonos,Public Health Agency of Canada,120-255Woodlawn Road West,Guelph,Ontario,Canada N1H 8J1;2Department
of Population Medicine,Ontario Veterinary College,University of Guelph,Guelph,Ontario,Canada N1G 1P7;and 3Laboratory for Foodborne Zoonos,
Public Health Agency of Canada,103-160Rearch Lane,Guelph,Ontario,Canada N1G 5B2
MS 10-495:Received 12November 2010/Accepted 15March 2011
ABSTRACT
This study estimated the prevalence of Escherichia coli isolates in fresh retail milk-fed veal scallopini pieces obtained from grocery stores in Ontario,Canada.In addition,the prevalence and antimicrobial resistance patterns were examined for points of public health significance.One hundred fifty-three milk-fed veal samples were collected over the cour of two sampling phas,January to May 2004and November 2004to January li isolates were recovered from 87%(95%confidence interval,80.54to 91.83%)of samples,and antimicrobial susceptibility testing was conducted on 392isolates.The prevalence of resistance to one or more antimicrobials was 70%(274of 392),while the resistance to five or more antimicrobials was 33%(128of 392).Resistance to ceftiofur (2.8%),ceftriaxone (3.6%),nalidixic acid (12%),and ciprofloxacin (3.8%)alone or in combination was obrved.Eighty-five resistance patterns were obrved;resistance to tetracycline only (7.4%)was obrved most frequently.Individual antimicrobial resistance prevalence levels were compared with grain-fed veal and retail beef data from samples collected in Ontario.In general,resistance to individual antimicrobials was obrved more frequently li isolates from milk-fed veal than in isolates from grain-fed veal and beef.Resistance to one or more antimicrobials and to five or more a
ntimicrobials li isolates was more frequent in isolates from milk-fed veal than in isolates from grain-fed veal and beef.This study provides baline data on the occurrence of resistance li isolates from milk-fed veal that can be compared with data for other commodities.li resistance patterns may rve as an indicator of antimicrobial exposure.
Although pathogenic organisms are often the primary focus of human and animal antimicrobial resistance,commensal nonpathogenic bacteria are also an important component of the complex ecology of antimicrobial resistance (12,21).Most Escherichia coli bacteria are nonpathogenic;however,their prence on retail meat provides evidence of fecal contamination,an important measure of foodborne dia risk.Commensal E.coli bacteria,which are inhabitants of the human and animal digestive tracts,may rve as indicators of antimicrobial lection pressures and,ultimately,of the potential for antimicrobial resistance transfer to pathogenic organisms of human concern (22,29).Additionally,li may contribute to the development of resistance in pathogenic bacteria by acting as a rervoir of resistance genes through their ability to readily acquire mobile genetic elements which can then transfer horizontally and exchange with pathogenic strains when they invade the intestinal tract (21).
In a recent study of retail grain-fed veal in Ontario,isolates li were recovered from 88%of the
meat samples purchad in local grocery stores;54%of the bacterial isolates were resistant to one or more antimicro-bials (7).During that study,a smaller number of milk-fed veal samples were also collected,cultured li,and analyzed for antimicrobial resistance.There are veral differences in how grain and milk-fed veal calves are managed in Ontario,including diet,market age,and housing.The management differences might lead to differences in the levels of antimicrobial resistance of isolates recovered from retail meat samples.A preliminary analysis suggested that li isolates from the milk-fed veal had a higher prevalence of antimicrobial resistance than tho obtained from grain-fed veal.This finding prompted the initiation of a cond study focusing specifically on milk-fed veal.
The first objective of this study was to determine the prevalence of E.coli isolates on fresh milk-fed veal scallopini pieces,which are the most commonly available cut of milk-fed veal meat,obtained from veral geographic areas of Southwestern Ontario,Canada.The cond objective was to determine the prevalence and patterns of antimicrobial resistance in li isolates.The final
*Author for correspondence.Tel:519-826-2287;Fax:519-826-2244;a.
{Prent address:Department of Ecosystem &Public Health,Faculty of Veterinary Medicine,University of Calgary,TRW 2D22,3330Hospital Drive N.W.,Calgary,Alberta,Canada T2N 2Z6.1328
Journal of Food Protection,Vol.74,No.8,2011,Pages 1328–1333doi:10.4315/0362-028X.JFP-10-495
Copyright G ,International Association for Food Protection
objective was to identify resistance patterns that reprent potential public health risks,such as multidrug resistance and resistance to antimicrobials clinically important to human medicine.
MATERIALS AND METHODS
一年级英语上册Sampling design.A total of153raw milk-fed veal samples were collected over the cour of two study periods.In the first period,January and February2004,milk-fed veal samples(n~ 32)were collected from three areas of Southwestern Ontario:(i) Perth,(ii)Wellington-Dufferin-Guelph,and(iii)North Toronto. The sampling frame was a census of all retail food outlets offering veal in the study areas.A target of14raw milk-fed scallopini pieces were purchad on a weekly basis from retail food outlets in the sampling frame;however,due to the low availability of milk-fed veal,the actual number of samples
purchad was ultimately bad on product availability.Veal samples were excluded from lection if they were labeled‘‘previously frozen’’or appeared to have been frozen,asoned,breaded,ground,or tenderized prior to packaging.After purcha,samples were individually wrapped and stored in coolers at refrigeration temperature(approximately4u C) and transported within4h to the laboratory for processing.
During the cond collection period,November2004to February2005,an additional121samples were collected from five Southern Ontario census divisions:Guelph-Wellington-Dufferin, Cambridge-Kitchener-Waterloo,Hamilton,York,and Peel.Sam-pling procedures and store lists were derived from the Canadian Integrated Program for Antimicrobial Resistance Surveillance (CIPARS)(17).Approximately10samples per week were purchad;however,this was bad solely on product availability. Additionally,sample size was also dictated by time constraints and laboratory capacities.Due to limited milk-fed veal meat availabil-ity,40of the total153samples were a mixture of stew pieces, chops,and shanks rather than scallopini cuts.Exclusion criteria for samples were the same as for the first sampling period.
怎么查四级成绩Laboratory analysis.Upon receipt of samples at the laboratory,the milk-fed veal portions were aptically removed from the packaging and placed into a stomacher bag(Seward Ltd., West Susx,
UK)containing100ml of0.1%peptone water (Difco,BD,Sparks,MD)and manually massaged for3min.Fifty milliliters of the peptone rin and half of the meat sample were then transferred to a new stomacher bag containing450ml of buffered peptone water(Difco,BD)and incubated at37¡1u C for 24h.Following incubation,50ml of buffered peptone water was placed in a new stomacher bag with50ml of double-strength EC broth(Difco,BD)and incubated at37¡1u C for24h.One loopful of the incubated EC broth was then streaked onto eosin methylene blue agar(Difco,BD)and incubated for37¡1u C for24h. Presumptive colonies were then streaked on MacConkey agar (Difco,BD)and incubated at37¡1u C for24h.Purified colonies were then streaked onto Luria-Bertani agar(Difco,BD)and incubated at37¡1u C for24h.Confirmation of positive suspect isolates was performed with Kovac’s indole spot reagent(PML Microbiologicals,Mississauga,Ontario,Canada)and Simmons citrate agar(Difco,BD).Up to li isolates per positive sample were tested for antimicrobial susceptibility using broth microdilution(Sensititre System,TREK Diagnostic Systems Inc., Westlake,OH).The antimicrobials ud in the CMV7CNCD panel with their respective MIC breakpoints for E.coli were the following:amikacin(AMK),$64m g/ml;amoxicillin–clavulanic acid(AMC),$32/16m g/ml;ampicillin(AMP),$32m g/ml; cefoxitin(FOX),$32m g/ml;ceftiofur(TIO),$8m g/ml;ceftriaxone(CRO),$4m g/ml;cephalothin(CEP),$32m g/ml; chloramphenicol(CHL),$32m g/ml;ciprofloxacin(CIP),$4m g/ ml;gentamicin(GEN),$16m g/ml;kanamycin(KAN),$64m g/ ml;nalidixic
acid(NAL),$32m g/ml;streptomycin(STR), $64m g/ml;sulfamethoxazole(SMX),$512m g/ml;tetracycline (TCY),$16m g/ml;and trimethoprim-sulfamethoxazole(SXT), $4/76m g/ml.The resistance breakpoints were tho ud by the National Antimicrobial Monitoring System(NARMS)and CI-PARS and were,in part,derived from breakpoints t by the Clinical and Laboratory Standards Institute(CLSI)(6,18).
Data analysis.All analys were performed using Stata Statistical Software,relea8.0(StatCorp,College Station,TX). Antimicrobial susceptibility results were dichotomized as resistant or susceptible;isolates with intermediate susceptibility were classified as susceptible for data analysis.Statistical differences between proportions were determined using Fisher’s exact2-way test(16).The binomial exact method was ud to calculate the 95%confidence intervals for bacterial prevalence(13).For some analysis,antimicrobials were categorized according to importance in human medicine,utilizing the classification scheme of the Veterinary Drugs Directorate,Health Canada(25).gala
RESULTS
veal samples submitted for primary isolation.Three hundred ninety-two isolates were submitted for antimicrobial susceptibility testing.Three veal samples yielded one isolate,1sample yielded two isolates,and129samples yielded three isolates each.The prevalence of resistance to one or more antimicrobials was70%(274of392),while the resistance to five or more antimicrobials was33%(128of 392)(Table1).For category I antimicrobials,of very high health importance in humans,11(2.8%)of392isolates were resistant to TIO;all of tho isolates were also resistant to CRO.Overall,CRO and AMC resistance was detected in 14(3.6%)of392and24(6.1%)of392isolates, respectively.
Resistance to NAL alone or in combination with other antimicrobials was detected in47(12%)of392isolates, while CIP resistance was found in15(3.8%)of392isolates. All CIP-resistant isolates had cross resistance to NAL.In addition,of the remaining32NAL-resistant isolates,25had reduced susceptibility to CIP(9isolates were susceptible at 0.125m g/ml,15isolates at0.25m g/ml,and1isolate at2m g/ ml)and the remaining7isolates were susceptible(0.06m g/ ml).There were85different resistance patterns obrved among li isolates(Table1).The most common unique resistance pattern was TCY alone(7.4%,29of392), followed by AMP-SMX-STR-SXT-TCY(4.6%,18of392), AMP-KAN-STR-SMX-TCY(AKSSuT)-SXT(4.1%,16of 392),KAN-SMX-STR-TCY
(3.6%,14of392),AMP-CHL-KAN-STR-SMX-TCY(ACKSSuT)-GEN-SXT(2.6%,10of 392),and STR-TCY(2.6%,10of392).The A3C(AMC-FOX-TIO-CEP)and AC(K)SSuT patterns(ACKSSuT or AKSSuT or AMP-CHL-STR-SMX-TCY)alone or in combination with resistance to other antimicrobials were en in2.8%(11of392)and16.8%(66of392)of isolates.
J.Food Prot.,Vol.74,No.8ANTIMICROBIAL RESISTANCE IN E.COLI ISOLATED FROM MILK-FED VEAL1329
Individual antimicrobial resistance prevalence levels were compared with grain-fed veal and retail beef data from samples collected in Ontario(Fig.1)(18).In general,the prevalence of resistance to individual antimicrobials was significantly higher li isolates from milk-fed veal than from grain-fed veal(for15of16antimicrobials tested) and beef(14of16).E.coli isolates from grain-fed veal had a significantly higher prevalence of resistance than isolates from beef for8of the16antimicrobials.The prevalence of resistance to one or more antimicrobials li isolates from grain-fed veal was54%compared with70%for E. coli isolates from milk-fed veal and21%li isolates from Ontario ground beef(18).Resistance to five or more antimicrobials was10%li isolates from grain-fed veal,33%li isolates from milk-fed veal,and4%li isolates from ground beef(17).
DISCUSSION
This study was the first in Canada to investigate the occurrence of E.coli and its antimicrobial resistance patterns in fresh retail milk-fed li was isolated primarily as an indicator of antimicrobial resistance lection pressure and as a rervoir of antimicrobial resistance genes;it is also an indicator for fecal contami-nation.The majority of milk-fed veal samples(87%)were contaminated li.li prevalences in retail grain-fed veal(88%)and ground beef samples(80%) obtained from comparable geographic areas and using similar methodologies have been documented(18).Bensink and Bothmann(3)reported that in Australia,the prevalence li on retail veal from butcher shops was11%(11of 100).Although a true difference in prevalence cannot be ruled out,differences in sampling and laboratory procedures (carcass swabbing versus enrichment broth)between the two studies probably contributed to the difference in prevalence.
In the prent study,TCY resistance alone or in combination with resistance to other antimicrobials was obrved most frequently among the milk-fed li isolates(64%,250of392),which is similar to its occurrence in other commodities(17,18).This is presumably a result of the frequent u of TCY in milk-fed veal calves.Resistance to TCY is commonly plasmid mediated,easily acquired,and reported frequently in bacteria of food animal origin(2).The prence of resistance to CIP(3.8%;15of392)and NAL(12%;47
TABLE1.Antimicrobial resistance patterns li isolates from milk-fed veal(n~392)
Antimicrobial resistance pattern a(no.of antimicrobials in pattern)No.of isolates with pattern
AMC-AMP-FOX-TIO-CRO-CEP-CHL-KAN-NAL-STR-SMX-TCY-SXT(13)3
AMC-AMP-FOX-TIO-CRO-CEP-CHL-KAN-STR-SMX-TCY-SXT(12)3
AMC-AMP-FOX-TIO-CRO-CEP-CHL-STR-SMX-TCY-SXT(12)3
AMC-AMP-FOX-CRO-CEP-CHL-KAN-STR-SMX-TCY-SXT(11)1
AMC-AMP-FOX-TIO-CRO-CEP-CHL-STR-SMX-TCY(11)1
AMC-AMP-FOX-CEP-KAN-STR-SMX-TCY-SXT(9)1
AMP-CEP-CHL-CIP-KAN-NAL-SMX-TCY-SXT(9)1
AMP-CHL-CIP-KAN-NAL-STR-SMX-TCY-SXT(9)1
CHL-CIP-GEN-KAN-NAL-STR-SMX-TCY-SXT(9)3
AMC-AMP-CEP-KAN-STR-SMX-TCY-SXT(8)3
AMC-AMP-FOX-TIO-CRO-CEP-STR-TCY(8)1
AMP-CEP-CHL-KAN-STR-SMX-TCY-SXT(8)2
AMP-CEP-GEN-NAL-STR-SMX-TCY-SXT(8)1
AMP-CEP-KAN-NAL-STR-SMX-TCY-SXT(8)1
AMP-CHL-CIP-KAN-NAL-SMX-TCY-SXT(8)3
信件结尾
AMP-CHL-GEN-KAN-STR-SMX-TCY-SXT(8)10
AMP-CHL-KAN-NAL-STR-SMX-TCY-SXT(8)4
AMP-CIP-GEN-KAN-NAL-STR-SMX-TCY(8)1
AMP-GEN-KAN-NAL-STR-SMX-TCY-SXT(8)3
AMC-AMP-CEP-KAN-STR-SMX-TCY(7)3
AMC-AMP-FOX-CEP-KAN-SMX-TCY(7)2
AMC-AMP-FOX-CRO-CEP-SMX-TCY(7)2
AMP-CEP-CHL-KAN-STR-SMX-TCY(7)1
AMP-CHL-GEN-KAN-SMX-TCY-SXT(7)2
AMP-CHL-GEN-STR-SMX-TCY-SXT(7)1
AMP-CHL-KAN-STR-SMX-TCY-SXT(7)1
AMP-CIP-NAL-STR-SMX-TCY-SXT(7)4
AMP-GEN-KAN-STR-SMX-TCY-SXT(7)2
AMP-KAN-NAL-STR-SMX-TCY-SXT(7)1
CHL-CIP-KAN-NAL-STR-SMX-TCY(7)1
CHL-KAN-NAL-STR-SMX-TCY-SXT(7)4
a Patterns of resistance to ven or more antimicrobials are shown.AMC,amoxicillin–clavulanic acid;AMP,ampicillin;FOX,cefoxitin; TIO,ceftiofur;CRO,ceftriaxone;CEP,cephalothin;CHL,chloramphenicol;KAN,kanamycin;NAL,nalidixic acid;STR,streptomycin; SMX,sulfamethoxazole;TCY,tetracycline;SXT,trimethoprim-sulfamethoxazole;CIP,ciprofloxacin;GEN,gentamicin.
1330COOK ET AL.J.Food Prot.,Vol.74,No.8
学英语的美剧of 392)in E.coli is a concern.The antimicrobial surveillance systems in Canada and the United States report the abnce of CIP resistance li isolates from beef,pork,chicken,or turkey at the retail or abattoir levels (5,17,18).However,fluoroquinolone resistance was also detected in retail grain-fed li isolates in a parallel study and has also been isolated in a recent Swiss study of fecal samples from veal calves at slaughter (7,9).CIP is clinically important for the treatment of rious human invasive bacterial gastrointestinal infections in adults,such as salmonellosis and vere campylobacteriosis (24).Fluoroquinolones are approved for u in food animals in many countries;however,among food animals in Canada,they are only approved for beef cattle (14).The prence of li isolates suggests lection pressure and the spread of resistant bacteria in the population of milk-fed calves.The findings rai questions about the possible off-lab
el u of fluoroquinolones in the veal calves,which remain unanswered given the limited availability of animal antimicrobial drug u data in Canada.
asscunt
Resistance to the category I antimicrobials TIO and CRO was also detected li isolates.This is of importance to public health becau antimicrobials in this category are of high importance in human medicine.In the prent study,resistance to TIO was found in 2.8%(11of 392)of isolates.Resistance to TIO li isolates from milk-fed veal was more frequent than in grain-fed veal (0.4%)(7)and beef (0.5%)(18).In Canada,TIO is a veterinary antimicrobial and is labeled for u in calves for the treatment of respiratory dia (15).TIO and the human antimicrobial CRO are third generation cephalosporins;cross-resistance between the two is normal.Resistance to CRO was also more frequent in milk-fed than in grain-fed veal (0.6%)and retail beef (0.5%).CRO is the primary drug administered for vere salmonellosis in children (1).Resistance dismination can result from transfer
between
FIGURE 1.Comparison of individual antimicrobial resistance li isolates from retail milk-fed veal,retail grain-fed veal,and 2004CIPARS retail beef.a,Significant difference between percentage of isolates resistant in milk-fed and grain-fed veal;b,significant difference between percentage of isolates resistant in grain-fed veal and beef;c,significant difference between percentage of isolates resistant in milk-fed veal and beef.White bars,grain-fed veal (n ~1,258);black bars,milk-fed veal (n ~392);grey bars,beef (n ~190).Category I antimicrobials,very high importance in human medicine with no alternative antimicrobial for resistant infections;category II antimicrobials,high importance alternatives for resistance to category III antimicrobials;category III antimicrobials,medium importance antimicrobials ud as first-line drugs;category IV antimicrobials,low importance antimicrobials of limited u in human medicine (not shown)(25).
J.Food Prot.,Vol.74,No.8ANTIMICROBIAL RESISTANCE IN E.COLI ISOLATED FROM MILK-FED VEAL
1331
Compared with data for grain-fed veal,the E.coli antimicrobial resistance results in our study suggest a higher tendency for multidrug resistance in milk-fed veal.Addition-ally,although the prevalence of A3C li isolates was low(2.8%),milk-fed veal isolates were significantly more A3C resistant than isolates from grain-fed veal(0.4%)(7). Similarly,the prevalence of AC(K)SSuT resistance was higher in milk-fed veal(16.8%)than in the grain-fed veal (4.5%)E.coli isolates.The AC(K)SSuT pattern may be an indicator of the prence of the pentaresistance castte in certain Salmonella rovars;it has been documented li isolates from retail meat in Norway but is more typically associated with plasmid-mediated resistance li(23). The phenotypic A3C resistance pattern can be an indicator of plasmid-mediated extended-spectrum b-lactamas or the AmpC-like b-lactama encoded by the bla CMY-2gene.Given that identical resistance breakpoints and laboratory method-ologies were ud to test li isolates from retail milk-fed veal,grain-fed veal,and ground beef collected by CIPARS,the results can be compared.Overall,li isolates from milk-fed veal tended to carry a larger pool of individual and multidrug resistance,while the grain-fed veal and Ontario ground beef were more similar.There are veral factors that may have contributed to the higher prevalence of antimicrobial resistance in milk-fed li isolates than in grain-fed veal and beef meat isolates.Milk-fed veal calves are slaughtered at a younger age—a suboptimal immune status,potential clinical anemia,different intestinal and pharmacological physiolo
gy,and higher antimicrobial and pathogen exposure are possible contributing factors(4,10,11, 19,20,27).In Canada,a majority of the antimicrobials approved for u in cattle can also be ud in veal calves under a valid veterinarian-client-patient relationship(14,15). However,the dos and withdrawal times recommended for adult cattle may not be applicable to veal calves,since there may be considerable differences in drug metabolism between neonates(calves)and adult cattle(26).Conquently,the extrapolation of dosages and withdrawal times may result in unnecessary or prolonged antimicrobial exposure,increasing the likelihood of antimicrobial resistance development.
This study extends the scope of previous work on antimicrobial resistance and bacteria isolated from retail raw meats to an additional commodity,milk-fed veal.The findings from this study can be ud as a baline for comparison to other commodities.In addition,the resistance patterns of li isolates from retail milk-fed veal may rve as an indicator of exposure to antimicrobials and as a source of genetic material for resistance to antimicrobials of public health concern.One limitation to our analysis is that isolates subjected to antimicrobial susceptibility testing could potentially be clonal and thus bias the calculated antimicro-bial resistance prevalences.Comparison of our results with tho from other commodities generated interesting findings. Assuming an equal likelihood of being
人称代词宾格undercooked or improperly handled during food preparation,our findings suggest that retail milk-fed veal may reprent a greater risk of exposure to antimicrobial-resistant strains li than grain-fed veal.The data generated from this study can support risk asssment and help guide the development of prudent u policy to reduce food hazards;however,further rearch in this area is warranted.First,Canadian milk-fed veal should be examined for the prence of pathogenic bacteria,such as Salmonella and Campylobacter,to determine the extent of resistance among pathogens of public health significance. Second,preharvest studies should be performed in milk-fed veal to explore the significance of the potential risk factors contributing to antimicrobial resistance:antimicrobial drug u,age of animal at market time,digestive physiology,and pharmacology.In particular,it is important to determine whether the unusual CIP resistance in li isolates can be attributed to on-farm administration of this antimicrobial or whether there are other causal factors,such as age or digestive physiology.Finally,given the relatively larger investment required to perform an on-farm study compared with the investment in a retail study,the preharvest study could be ud to determine how well retail studies predict the u of on-farm antimicrobials.
ACKNOWLEDGMENTS
This study was financially supported by the Ontario Ministry of Agriculture,Food and Rural Affairs—F
ood Safety Rearch Program,the Public Health Agency of Canada,and the Ontario Veterinary College DVM Fellowship Program.We especially thank the retail field samplers,students, laboratory technicians,Maria Popa,and Andrea Desruisau for laboratory support.
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