ANTIBIOTIC RESISTANCE IN FOODBORNE PATHOGENS MAY 2013 ACSPIWhitePaperby
CarolineSmithDeWaal,J.D.,andSusanVaughnGrooters,M.P.H.
ANTIBIOTIC RESISTANCE IN FOODBORNE PATHOGENS AntibioticResistanceinFoodborneOutbreaks,2013,wasresearchedandwrittenbyCarolineSmithDeWaal
andSusanVaughnGrooters.WegratefullyacknowledgetheassistanceofMarcusGlassman,Angela
Kraszewski,CindyRoberts,andMichaelF.Jacobsoninpreparingthisreport.Wealsowouldliketo
acknowledgethoseworkinginstateandfederalpublichealthagencieswhoprovidedinformationand
inspirationforthisreport.
CenterforScienceinthePublicInterest(CSPI)isanon‐profitorganizationbasedinWashington,DC.Since
1971,CSPIhasbeenworkingtoimprovethepublic’shealth,largelythroughitsworkonnutritionandfood‐
safetyissues.CSPIissupportedprimarilybythe900,000subscriberstoitsNutritionActionHealthletter
andbyfoundationgrants.
CenterforScienceinthePublicInterest 1220LStreetN.W.,Suite300
Washington,DC20005
Tel202.332.9110
www.cspinet.org
Copyright©2013byCenterforScienceinthePublicInterest;May2013
ANTIBIOTIC RESISTANCE IN FOODBORNE PATHOGENS TableofContents
ExecutiveSummary______________________________________________________________________________________1
Introduction ______________________________________________________________________________________________2
Findings___________________________________________________________________________________________________3
Background_______________________________________________________________________________________________7
AntimicrobialDrugSalesandDistributionData____________________________________________________ 11
References ______________________________________________________________________________________________ 12
Appendix‐FoodborneOutbreakLineListing_______________________________________________________ 14
ANTIBIOTIC RESISTANCE IN FOODBORNE PATHOGENS ExecutiveSummary
APublicHealthCrisis
“[T]hereisclearevidenceofadversehumanhealthconsequences
Theillnesses,hospitalizations,
duetoresistantorganismsresultingfromnon‐humanusageof
anddeathsreportedaspartof
antimicrobials.Theseconsequencesincludeinfectionsthatwould
thiswhitepaperarethose
nothaveotherwiseoccurred,increasedfrequencyoftreatment
fromantibioticresistant
failures(insomecasesdeath)andincreasedseverityofinfections,
foodbornepathogens.Overall, asdocumentedforinstancebyfluoroquinoloneresistanthuman
Salmonellainfections.”
thoseoutbreaksrevealthat
antibioticresistantfoodborne
— WorldHealthOrganization,2003
pathogenscan,anddo,
contaminateourfoodsupply.Theresultingillnessesbecomedifficulttotreatasthe
antibioticsneededtotreatthemaremorelimited.
Thisreportdetailsantibiotic‐resistantfoodborneoutbreaksfrom1973to2011.Intotal,
55outbreakswereidentified.Fooditemsmostlikelyassociatedwithantibioticresistant
pathogensincludeddairyproducts,groundbeef,andpoultry.Thesethreefoodcategories
wereimplicatedinmorethanhalfofreportedoutbreaks(31of55).Salmonellaspp.was
themostcommoncauseofantibiotic‐resistantoutbreaksidentified(48of55).Pathogens
exhibitingmulti‐drugresistancetofiveormoreantibioticswereidentifiedinmorethan
halfoftheoutbreaks(31of55,56%).
Managingantibioticresistance,withavoluntaryapproach
InAprilof2012,theFDAissuedaplantoaddressantimicrobialresistanceinthefoodsupply,withthe
releaseofguidanceforindustry:TheJudiciousUseofMedicallyImportantAntimicrobialDrugsinFood‐
ProducingAnimals(GFI209).TheFDA’sstrategyistolimituseofantimicrobialsinfood‐producing
animalsthatarealsoimportantinhumanhealth,andultimatelytocurbthedevelopmentof
antimicrobialresistance.Usingavoluntaryapproach,theguidanceencouragesdrugcompaniesto
changethelabelingofmedicallyimportantantimicrobialsinfood‐producinganimalstopreventtheir
useinanimalsforgrowthpromotionorincreasedfeedefficiency.Thisvoluntaryapproachisflawedin
lightofFDA’spublichealthmission.Legislationsuchas“ThePreservationofAntibioticsfortheMedical
TreatmentAct”wouldprovideclearerstandardstolimittheuseofeightclassesofantibiotics,deemed
criticallyimportantforuseinhumanmedicine,thatarealsousedinanimalagriculture.ThisAct
providesamorerigorousmeasuretoaddresstheproblemofantibioticresistancebyspecifically
addressingusesofantibioticsinanimalagriculturethatarecriticaltotreatmentofhumandisease.
Page1 ANTIBIOTIC RESISTANCE IN FOODBORNE PATHOGENS Introduction
Thisreportillustratesthelinkbetweenfoods,mostlyofanimalorigin,andoutbreaksof
antibiotic‐resistantpathogensinhumans.Outbreakscausedbyantibiotic‐resistant
bacteriaarenotanemergingproblem,butanestablishedproblemthatneedsmore
routinescrutiny‐andprevention‐bypublichealthofficials.Informationonoutbreaksof
foodborneillnessduetoantibiotic‐resistantbacteriaislimited.SalmonellaandE.coliare
notroutinelytestedforantibioticresistanceand,evenwhentestsareperformed,results
arenotrequiredtobereportedtotheCentersforDiseaseControlandPrevention(CDC).
TheCenterforScienceinthePublicInterest(CSPI)inthiswhitepaperdescribesatotalof
55foodborneoutbreaksbetween1973and2011thatwerecausedbybacteriaresistantto
atleastoneantibiotic.
TheNationalAntimicrobialResistanceMonitoringSystem(NARMS)collectsdataon
patternsofresistanceinpathogens,butthosedataarenotlinkedtoactualoutbreaks.
Also,CDCdoesnottrackandpublishinformationaboutoutbreaksorsporadicillnesses
causedbyresistantbacteria,asitdoesforpathogensinitsFoodNetsystem.Thus,inthe
absenceofotherdata,CSPIhasdevelopedadatabaseofoutbreaksduetoantibiotic‐
resistantbacteriainthefoodchaintoinformhealthofficialsandthepublicandto
encouragecarefultrackingofthoseoutbreaksinthefuture.Catalogingfoodborneillness
outbreaksassociatedwithantibiotic‐resistantpathogensisacriticalstepin
understandingthelinkbetweenadministeringantibioticstofarmanimalsandhuman
illnessand,ultimately,preventingtheproblem.
Limitinguseinanimalstopreservecephalosporineffectivenessinhumans
Twopopulationsthataremostatriskoffoodborneillnessarechildrenandimmune‐compromised
individuals.Ceftriaxoneorcefotaximearethird‐generationcephalosporinsandareoftenthetreatment
ofchoiceforseverelycomplicatedpediatricsalmonellosis.Concernsaboutthepervasivenessof
plasmidsthatconferresistancetofirst‐,second‐,andthird‐generationcephalosporinsledFDAin
January2012toannouncethatitwouldbantheextra‐labeluseofcertaincephalosporinantibioticsin
majorspeciesoffood‐producinganimals.ThatbantookeffectonApril5,2012.
Page2 ANTIBIOTIC RESISTANCE IN FOODBORNE PATHOGENS Findings
Whileantibiotic‐resistantoutbreakshavebeencataloguedsincethe1970s,themajority
have(34,58%)occurredsince2000.Dairyproductsaccountedforaquarterofthe
outbreaks(14outbreaks,25%).Contaminatedgroundbeefwasalsoacommoncause(10
outbreaks,18%).Contaminatedpoultryproductscausedsevenoutbreaks,produceitems
causedfour,andseafoodaccountedfortwo.Oneoutbreakeachwaslinkedtoporkand
eggs.Multi‐ingredientfoodscausedthreeoutbreaks,andnospecificfoodvehiclewas
determinedforthirteenoftheoutbreaks,thoughcharacteristicsoftheoutbreaks
indicatedthattheywerefoodrelated(Figure1).
Figure1.OutbreaksbyFoodCategory
N=55
20
#ofOutbreaks
15
14
13
10
10
7
5
4
3
2
1
1
0
The55reportedoutbreakssickened20,601individuals,ofwhom3,166required
hospitalizationand27died.Two‐thirds(67%)ofthedeathswereduetoahugemilk‐
associatedoutbreakin1985thatkilled18andsickened16,659people.Thatoutbreakwas
alsoresponsiblefor88%(2,777)ofallreportedhospitalizations.
Page3 ANTIBIOTIC RESISTANCE IN FOODBORNE PATHOGENS ThemostcommoncauseofoutbreakswasSalmonellaspp.,identifiedin48ofthe55
outbreaks(seeFigure2).SalmonellaTyphimuriumwasthemostfrequentlyidentified
serotype,associatedwith19outbreaks(35%oftotaloutbreaks).S.Typhimurium‐
associatedoutbreakscaused17,979illnessesandincludedthelargemilk‐associated
outbreakin1985.ThesecondmostfrequentlyidentifiedserotypewasSalmonella
Newport,implicatedin15outbreakswith872linkedcases.AdditionalSalmonella
serotypeswereimplicatedinsixteenoutbreaks,andtwooutbreakswerecausedby
multipleSalmonellaserotypes.Ofthosesixteen,SalmonellaHeidelbergaccountedforfour
outbreaks,andSalmonellaHadarwasimplicatedintwooutbreaks.Byetiology,themedian
numberofoutbreaksis10.
Amongotherresistantpathogensthatcausedoutbreaks,enterotoxigenicEscherichiacoli
(ETEC)causedfiveoutbreaks,with446illnesses.CampylobacterjejuniandStaphylococcus
aureuswereeachimplicatedinoneoutbreak.
Figure2.OutbreaksbyEtiology
N=55
19
#ofOutbreaks
20
16
15
15
10
5
5
1
1
Campylobacter
S.aureus
0
S.Typhimurium*
Other
Salmonella*
S.Newport*
E.coliETEC
*MultipleSalmonella serotypesimplicatedintwooutbreaks
Drug‐resistancepatternsshowthatthemajorityofoutbreaks(39of55,70%)were
resistanttoatleastoneantibiotic,streptomycin(Figure3).Streptomycinisan
aminoglycosideclassifiedbytheWorldHealthOrganization(WHO)as“critically
important”andbytheFoodandDrugAdministration(FDA)(GuidanceforIndustry152)
as“highlyimportant”fortreatmentinhumanmedicine.(Seepage11forfurther
Page4 ANTIBIOTIC RESISTANCE IN FOODBORNE PATHOGENS discussionoftheWHOandFDAcategories.)Resistancetotetracycline,acommonlyused
antibioticinfoodanimalproduction,deemedtobehighlyimportantinhumanmedicine
bytheFDAandtheWHO,wasdetectedin47of55outbreaks(85%).Cephalosporin
antibiotic‐resistanceoccurredin28outbreaks,andresistancetocephamycin,an
antibioticsimilartocephalosporin,occurredin15outbreaks.
#ofOutbreaks
Figure3.DrugResistanceProfilesbyWHOcategories
(55Outbreaks)
50
45 39
40
35
30
25
20
15
10
5
0
47
36
25
19
15
15
17
14
10
2
3
1
5
4
1
CriticallyImportant
HighlyImportant
3
1
10
4
NotclassifiedonWHO'slist
Thirty‐one(56%)outbreaksinvolvedapathogenwithmulti‐drugresistancetofiveor
moreantibiotics(Figure4).Eitherreportingofantibiotic‐resistantoutbreaksis
improving,ortherecouldbeanappreciableincreaseinoutbreaksresultingfromresistant
bacteria,astwo‐thirdsofthoseoutbreaksoccurredinthelasttwodecades.Anoutbreak
associatedwitheggsin1973hadanunknownantibiotic‐resistanceprofile,asdidtwo
outbreaksfromrawmilk,onein1979,andtheotherin1980.Thus,thetotalnumberof
outbreakswithresistanceprofilesis52,not55.
Page5 ANTIBIOTIC RESISTANCE IN FOODBORNE PATHOGENS Figure4.IndividualDrugResistancesperOutbreak
N=52
#ofOutbreaks
20
15
15
10
10
6
6
5
6
5
4
0
One
Two
Three
Four
Five
Six
Seven+
#ofIneffectiveDrugs
Meatandpoultryproductswereidentifiedin18outbreaks:10ingroundbeef,7in
poultry,and1inpork.GroundbeefcontaminatedwithSalmonellaNewportcausedseven
outbreaks,andtheotherthreewereSalmonellaTyphimurium‐associated.Sixofthe
poultryoutbreakswerelinkedtoSalmonellaspp.contamination,andonewasassociated
withE.coliO27:H7.Meatandpoultryoutbreakscaused1,639casesofillness,with191
hospitalizations,andeightdeaths.
Therewere14outbreaksassociatedwithdairy:8wereassociatedwithmilkproducts,
and6wereassociatedwithcheeses.In11ofthe14outbreaks(79%),theimplicatedfood
itemwasdescribedasbeingraw/unpasteurizedmilkorcheese.Pasteurizedmilkcaused
threeoutbreaks,includingthelargeoutbreakin1985.Allofthedairy‐associated
outbreaksidentifiedSalmonellaspp.astheetiologicagent–tenassociatedwithS.
Typhimurium,threewithS.Newport(includingonealsolinkedtoS.Meleagridis),andone
withS.Dublin.Overall,dairyoutbreakswereresponsiblefor17,257illnesses,2,871
hospitalizations,and19deaths.
Page6 ANTIBIOTIC RESISTANCE IN FOODBORNE PATHOGENS Background
Thediscoveryofantibacterialagentsinthefirsthalfofthe20thcenturyradicallychanged
theoutcomeofcommonhumandiseases.Manyillnessesthatweredeadlybefore
antibioticsbecameavailablearenowreadilytreatable.Theabilityofbacteriatoevolve
mechanismstoresistattackbyantimicrobials1wasrecognizedsoonafterthewidespread
deploymentofthefirstantibiotics.
Resistanceisaninevitableconsequenceofantibioticuse;themorethatantibioticsare
used,themorebacteriawilldevelopresistance.Inrecentyears,scientistshavebegunto
understandatthemolecularlevelthesophisticatedmechanismsthatenablebacteriato
fendofforneutralizeantibiotics.Antibioticresistanceisrecognizedasagrowingproblem
thatposesamajorthreattothecontinuedeffectivenessofantibioticsusedtotreathuman
andveterinaryillnesses.Furtherexacerbatingtheproblem,pharmaceuticalcompanies
aredevelopingfewernewantibioticstoreplacethosethatarenolongereffective
(Silbergeldetal.,2008).
Numerousstudieshavedocumenteddirecttransferenceofantibiotic‐resistantbacteria
fromanimalstohumans.Researchershavefoundthatwhenantibioticswere
administeredtoanimalstotreatinfections,theprevalenceofantibiotic‐resistantE.coli
andCampylobacterbacteriaalsoincreasedinhumans(Levyet.al,1976;Smithet.al,
1999).Otherstudieshaveconfirmedthatantibiotic‐resistantCampylobacter,Salmonella
TyphimuriumDT104,andSalmonellaNewporthavemovedfromanimalstohumans
throughfoodsofanimalorigin(Smithetal.,1999;Ribotetal.,2002).Reflectingthefact
thatbacteriacandevelopresistancetonumerousantibioticsatthesametime,onegroup
ofrelatedantibiotic‐resistantSalmonellaNewportstrainsisresistanttomostavailable
antimicrobialagentsapprovedforthetreatmentofsalmonellosis,particularlyinchildren
(Guptaetal.,2003).
Thehumanhealthconsequencesofresistantpathogensincludemoreseriousinfections
andincreasedfrequencyoftreatmentfailures.Patientsmayexperienceprolonged
1Theterm“antimicrobial”isabroadtermreferringtosubstancesthatactagainstavarietyofmicroorganisms,
includingbacteria,viruses,parasites,andfungi.Theterm“antibiotic”isanarrowertermreferringtosubstancesused
totreatbacterialinfections.Classically,antibioticswereproducedbyamicroorganism,butnowbothmanufacturedand
naturally‐occurringsubstancesthatkillbacteriaarecalledantibiotics.Mostoftheconcernwithantimicrobialusein
agricultureiswithbacterialresistance,so“antibiotic”isusedinthisreport.
Page7 ANTIBIOTIC RESISTANCE IN FOODBORNE PATHOGENS durationofillness,increasedfrequencyofbloodstreaminfections,greaterlikelihoodof
hospitalization,andincreasedmortality(Anguloetal.,2004).
Health‐care costs increase with longer hospital stays and the need for more expensive
antibioticstofightresistantpathogens.Theantibioticsusedtotreatresistantpathogens
canbemoretoxic,withmoreserioussideeffectsinthepatients.
Thereportedoutbreaksdocumenttheproblemofantibiotic‐resistantfoodborne
pathogens,butanyrisk‐managementstrategyiscomplicatedbythedivisionofauthority
amongseveralfederalagenciesandthediversestakeholders,particularlythedrug
manufacturersandcattle,hog,andpoultryindustries.Themainobstacleforresearchers
workingtoidentifysolutionstoantimicrobialresistanceisalackofdata–especiallydata
ondruguse.Morerobustdataisneededonthetypesandquantitiesofantibioticssoldfor
useinfood‐producinganimals,thespeciesinwhichtheyareused,whentheyare
administered,thepurposeoftheiruse(diseasetreatment,diseaseprevention,orgrowth
promotion),andthemethodusedtoadministerthem.Denmark,forexample,collects
dataonantibioticusefromdrugcompanies,veterinarypharmacies,feedmills,private
companies,andveterinarians.Reportingincludesspecies‐specificdrugadministration
data,theageatwhichanimalsaregivendrugs,thediseasesbeingtreated,anddosage.
SuchdatahaveallowedDanishresearcherstodeterminehowchangesintheuseof
antibioticsinanimalsaffecttheemergenceofantibiotic‐resistantbacteria(DANMAP,
2011).InformationlikethoseisnotcollectedintheUnitedSates.
Manyoftheantibioticsusedforfood‐producinganimalsarethesame,orbelongtothe
sameclasses,asthoseusedinhumanmedicine.Resistancetooneantibioticinaclass
oftenresultsinresistancetoalldrugsinthatclass,furthercompoundingtheproblem.In
addition,thegenesthatcanrenderonebacteriumresistantcanevenbesharedby
differentspeciesthroughhorizontalgenetransfer.Widespreaduseofantibioticsin
agricultureincreasesthelikelihoodthattheywillbecomeineffectiveagainsthuman
illnesses.
TheWHOhasdevelopedcriteriaforrankingantimicrobialsaccordingtotheirimportance
inhumanmedicine.TherankingsareregularlyreviewedbyWHO’sAdvisoryGroupon
IntegratedSurveillanceofAntimicrobialResistance(AGISAR).Thisrankingofdifferent
drugsfromahumanhealthperspectivewasdevisedforusebygovernmentsandother
Page8 ANTIBIOTIC RESISTANCE IN FOODBORNE PATHOGENS stakeholderswhentheydeveloprisk‐managementstrategiesconcerningtheuseof
antimicrobialsinfoodanimals.
TheWHOdividesantimicrobialsintothreecategoriesbasedontheiroverallimportance
tohumanhealth:criticallyimportant,highlyimportant,andimportant(WHO,2011).
WHOranksantimicrobialagentsascriticallyimportantwhen:
1) Theyarethesoleoroneoffewoptionsfortreatmentofhumaninfections,and
2) Theyareusedtotreatdiseasescausedbyorganismsthatmaybetransmittedvia
non‐humansourcesororganismsthatmayacquireresistancegenesfromnon‐
humansources.
Antimicrobialsthatmeetjustoneofthosecriteriaarerankedashighlyimportant,while
antimicrobialsthatmeetneithercriterionarerankedasimportant.
In2003,theFDAalsorankedantimicrobialdrugsaccordingtotheirimportanceinhuman
medicine(FDA,2003).TheFDArankingsaredividedinto“criticallyimportant”,“highly
important”and“important”.However,theFDAfocusedonantibioticsusedtotreat
foodborneillnessinhumans,ratherthanonthebroaderspectrumofhumandisease.For
example,FDAranksfourth‐generationcephalosporins,whichareanimportanttreatment
forpneumoniaandoneofthefewtherapiesforcancerpatientswithcomplicationsfrom
chemotherapy,ashighlyimportant,whileWHOranksthemascriticallyimportant(FDA
2003,WHO2011).
Antibioticsareusedinfood‐producinganimalstotreatorpreventillnesses,forexample,
duringtheweaningperiodofyounganimals.Theymayalsobeusedforlongperiodsat
lowlevelstopromotegrowth,increasefeedefficiency,orcompensateforunsanitary
growingconditionsonconcentratedanimalfeedingoperations(CAFOs).Increasedfeed
efficiencymeansanimalsrequirelessfeedperpoundofweightgain,whichtranslatesinto
lowercostsforproducers.Manyanimalproducersbelievetheuseofantibioticsfor
growthpromotionalsopreventsdisease(GAO,2011).
Intheindustrialmodelofanimalhusbandry,largenumbersofpigs,chickens,orcattleare
raisedinconfinedareas.Intheporkandchickenindustries,large‐scaleconcentrated
housingsystemsreducecostsforlabor,feed,andhousing.However,theincreasedstress
ofcrowdingandunsanitaryconditionsmakesanimalsmoresusceptibletothespreadof
Page9 ANTIBIOTIC RESISTANCE IN FOODBORNE PATHOGENS infectiousdiseases.Manyproducerscommonlyadministeranantibiotictoanentireflock
orherdviafeedorwater,butthatgivesthemlesscontroloverthedosageconsumedby
individualanimals.Thenontherapeutic2useofantibiotics,sometimesadministered
throughoutananimal’slife,isamongthepracticesofgreatestconcernforthe
developmentofantibioticresistance.
Beginningin2008,antibioticdrugmanufacturerswererequiredtoreportannuallytothe
FDAtheamountofdrugstheysoldordistributedforuseinfood‐producinganimals(FDA,
2010a,FDA,2011a,FDA,2013).Threeyearsofdatashowthattheaggregatequantityof
antibioticsbeingsoldforuseinfood‐producinganimalspeciesincreasedfrom28.81to
29.86millionpoundsfrom2009to2011.Combinedtotalsofdrugdistributioninhuman
medicinedatachangedlittleoverthattimeperiodfromapproximately7.31to7.25
millionpounds.ThedatareportedtoFDAisnotbrokendownbyspecies,routeof
administration,orpurposeofuse.Thus,antibioticssoldforuseinfoodanimalsconstitute
about80%ofallantibioticsdistributedintheUnitedStates.Ofthoseantibioticssoldin
2011(excludingnotindependentlyreportedor“other”antibioticsandIonophores),
approximatelythreequartersusedinanimalagricultureareidenticalorsimilartothose
usedinhumanmedicine(Table1).
2Nontherapeuticreferstousewhenanimalsaretreatedintheabsenceofbacterialdiseaseorexposuretodisease.
Page10
ANTIBIOTIC RESISTANCE IN FOODBORNE PATHOGENS Theuseofcriticallyimportantantimicrobials,suchasaminoglycosides,cephalosporins,andmacrolides,
appearstohavedecreasedfrom2009to2011basedondistributionandsalesdata(bothanimalandhuman).
Ontheotherhand,theuseinanimalsofpenicillins,aclassthatincludescriticallyimportantantibiotics,
appearstohaveincreasedfrom2009to2011.Therewasalsoasignificantincreaseinsalesanddistributionof
thehighlyimportantclassofantibiotics,tetracyclines,infood‐producinganimals.
Table 1. Antimicrobial Drugs Approved for Domestic Use in Humans and Food-Producing Animals*.
Sales and Distribution Data Reported to FDA by Drug Class.
2009 Animal Annual
Totals (LBS)
2010 Animal Annual
Totals (LBS)
2011 Animal Annual
Totals(LBS)
Aminoglycosides
748,862
442,675
473,762
Critically / highly
Cephalosporins
91,113
54,207
58,667
Critically / highly
8,246,671
8,424,167
9,090,230
Ionophores
Lincosamides
WHO Status
Not ranked
255,377
340,952
419,101
Macrolides
1,900,352
1,219,661
1,284,933
Critically
Penicillins
1,345,953
1,920,112
1,940,427
Critically / highly
Sulfas
1,141,715
1,116,020
817,959
Highly
10,167,481
12,328,521
12,439,744
Highly
4,910,501
3,345,398
3,330,241
28,808,024
2009 Human
Annual Total (LBS)
29,191,712
2010 Human
Annual Total (LBS)
29,855,066
2011 Human
Annual Total (LBS)
20,682
15,413
14,297
Critically / highly
1,101,465
1,107,957
1,095,499
Critically / highly
0
0
0
Lincosamides
153,744
152,637
157,531
Important
Macrolides
388,626
362,239
361,620
Critically
Penicillins
3,217,027
3,174,502
3,219,677
Critically / highly
Sulfas
1,039,352
1,057,081
1,061,887
Highly
289,108
284,800
250,957
Highly
1,102,567
1,074,121
1,089,921
7,312,570
7,228,750
7,251,390
Tetracyclines
Other (Not Independently Reported (NIR))**
Total
Aminoglycosides
Cephalosporins
Ionophores
Tetracyclines
Other (Not Independently Reported (NIR))**
Total
Important
WHO Status
Not ranked
* For all classes except aminoglycosides and ionophores, data includes antimicrobial drug
products which are approved and labeled for use in both food- and non-food- producing animals.
** NIR is used for antimicrobial classes with fewer than three sponsors actively marketing
products. This category includes fluoroquinolones and streptogramins.
*** Human drug use data is based on data from the IMS Health, IMS National Sales Perspectives.
Page11
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Page13
Appendix. Antibiotic-Resistant Foodborne Outbreaks
Year Location Bacteria
Food/Source
Cases Hosp Death Resistances
1973 ME
S. Typhimurium
Eggs
32
NR
NR
unknown
1975 MD, FL,
CO
S. Newport
Ground beef
27
NR
NR
streptomycin
aminoglycosides
critically important
sulfamethoxazole
sulfonamides
highly important
1977 KY
S. Typhimurium
Raw milk
1979 CA, OR
S. Dublin
Raw milk
1980 MT
S. Typhimurium
Raw milk
1983 AZ
S. Typhimurium
Raw milk
1983 MN, SD,
NE, IA
1984 OR
1985 CA
1985 IL
S. Newport
S. Typhimurium
S. Newport
S. Typhimurium
Ground beef
Salad bar
Ground beef
Pasteurized
milk
3
39
12
18
715
298
NR
NR
Drug Family
WHO Status
tetracycline
tetracycline
highly important
ampicillin
penicillin
critically important
carbenicillin
penicillin
critically important
kanamycin
penicillin
streptomycin
tetracycline
aminoglycosides
penicillin
aminoglycosides
tetracycline
highly important
critically important
critically important
highly important
NR
NR
unknown
NR
NR
unknown
NR
1
ampicillin
penicillin
critically important
chloramphenicol
amphenicol
highly important
kanamycin
aminoglycosides
highly important
streptomycin
aminoglycosides
critically important
sulfonamide*
sulfonamides
highly important
11
45
22
tetracycline
tetracycline
highly important
ampicillin
penicillin
critically important
carbenicillin
penicillin
critically important
tetracycline
tetracycline
highly important
0
tetracycline
tetracycline
highly important
2
streptomycin
ampicillin
aminoglycosides
penicillin
critically important
critically important
chloramphenicol
amphenicol
highly important
kanamycin
aminoglycosides
highly important
streptomycin
aminoglycosides
critically important
sulfamethoxazole
sulfonamides
highly important
1
16659 2777 18
tetracycline
tetracycline
highly important
ampicillin
penicillin
critically important
kanamycin
aminoglycosides
highly important
streptomycin
aminoglycosides
critically important
sulfamethoxazole
sulfonamides
highly important
tetracycline
tetracycline
highly important
1987 GA
S. Havana
Chicken
73
36
1
tetracycline
tetracycline
highly important
1994 WI
E. coli O153:H45
(ETEC)
Unknown,
banquet food
205
NR
NR
ampicillin
penicillin
critically important
tetracycline
tetracycline
highly important
sulfisoxazole
sulfonamides
highly important
1995 AZ
1996 NE
1997 WA
S. Stanley
S. Typhimurium
DT104
S. Typhimurium
DT104
Alfalfa sprouts
Unknown,
chocolate milk
suspected
Mexican-style
soft cheese
(queso fresco)
(raw milk)
19
19
89
5
0
5
NR
0
0
streptomycin
aminoglycosides
critically important
kanamycin
aminoglycosides
highly important
tetracycline
tetracycline
highly important
trimethoprimsulfamethoxazole
ampicillin
sulfonamides
*
penicillin
critically important
chloramphenicol
amphenicol
highly important
streptomycin
aminoglycosides
critically important
sulfonamide*
sulfonamides
highly important
tetracycline
tetracycline
amoxicillin/clavulanate penicillin
highly important
critically important
ampicillin
penicillin
critically important
chloramphenicol
amphenicol
highly important
streptomycin
aminoglycosides
critically important
sulfamethoxazole
sulfonamides
highly important
tetracycline
tetracycline
highly important
Appendix. Antibiotic-Resistant Foodborne Outbreaks
Year Location Bacteria
1997 CA
1997 CA
1997 MD
1997 VT
1998 NY
1998 KS
S. Typhimurium
DT104
S. Typhimurium var
Copenhagen
DT104b
S. Heidelberg
S. Typhimurium
S. I 4,[5],12:i-
Campylobacter
jejuni
2000 TN
Staphylococcus
aureus (MRSA)
2000 PA, NJ
S. Typhimurium
Food/Source
Cases Hosp Death Resistances
Mexican-style
cheese (raw
milk)
79
Mexican-style
cheese (raw
milk)
Pork
Raw milk
Unknown,
dinner
reception
multiple foods
suspected
Unknown,
gravy, potato,
pineapple
Pork,
barbeque,
vegetable
l d
l
Pasteurized
31
706
9
86
128
13
14
NR
1
31
2
NR
NR
2
NR
0
0
2001 WI
S. Newport
E. coli
O169:H41/ST
(ETEC)
ampicillin
penicillin
critically important
chloramphenicol
amphenicol
highly important
streptomycin
aminoglycosides
critically important
sulfonamide*
sulfonamides
highly important
tetracycline
tetracycline
highly important
ampicillin
penicillin
critically important
chloramphenicol
amphenicol
highly important
streptomycin
aminoglycosides
critically important
sulfonamide*
sulfonamides
highly important
tetracycline
tetracycline
highly important
kanamycin
aminoglycosides
highly important
streptomycin
aminoglycosides
critically important
tetracycline
tetracycline
highly important
ampicillin
penicillin
critically important
chloramphenicol
amphenicol
highly important
streptomycin
aminoglycosides
critically important
sulfamethoxazole
sulfonamides
highly important
tetracycline
tetracycline
highly important
ampicillin
penicillin
critically important
streptomycin
aminoglycosides
critically important
sulfonamide*
sulfonamides
highly important
tetracycline
tetracycline
highly important
trimethoprimsulfamethoxazole
ciprofloxacin
sulfonamides
*
fluoroquinolone
critically important
tetracycline
tetracycline
highly Important
0
0
methecillin
penicillin
*
93
6
0
ampicillin
penicillin
critically important
kanamycin
aminoglycosides
highly important
streptomycin
aminoglycosides
critically important
sulfamethoxazole
sulfonamides
highly important
tetracycline
tetracycline
Italian-style soft 27
cheese (raw
milk)
Quesadilla,
fajitas, nacho
chips, beans
WHO Status
3
milk
2001 CT
Drug Family
21
12
0
0
0
highly important
amoxicillin/clavulanate penicillin
critically important
ampicillin
penicillin
critically important
cefoxitin
cephamycin
highly important
ceftiofur
cephalosporin (3G) *
cephalothin
cephalosporin (1G) highly important
chloramphenicol
amphenicol
streptomycin
aminoglycosides
critically important
sulfamethoxazole
sulfonamides
highly important
highly important
tetracycline
tetracycline
highly important
tetracycline
tetracycline
highly important
Appendix. Antibiotic-Resistant Foodborne Outbreaks
Year Location Bacteria
Food/Source
Cases Hosp Death Resistances
2002 NY, MI,
PA, OH,
CT
Ground beef
47
2002 OR
2003 TN
2003 9 states
2004 NV
2004 CA
2004 IL
S. Newport
17
amoxicillin/clavulanate penicillin
critically important
ampicillin
penicillin
critically important
cefoxitin
cephamycin
highly important
ceftiofur
cephalosporin
*
cephalothin
cephalosporin (1G) highly important
chloramphenicol
amphenicol
streptomycin
aminoglycosides
critically important
sulfamethoxazole
sulfonamides
highly important
tetracycline
tetracycline
highly important
kanamycin (2/3
resistant)
ceftriaxone (2)
aminoglycosides
highly important
highly important
cephalosporin (3G) critically important
Chicken
lasagna
49
tetracycline
tetracycline
highly important
E. coli O169:H49
(ETEC)
S. Typhimurium
DT104
Catfish,
coleslaw
Ground beef
41
2
0
tetracycline
tetracycline
highly important
56
11
0
ampicillin
penicillin
critically important
chloramphenicol
amphenicol
highly important
S. Newport
S. Newport
Shrimp
Pasteurized
milk
Unknown
130
100
2
5
NR
6
0
0
NR
0
streptomycin
aminoglycosides
critically important
sulfamethoxazole
sulfonamides
highly important
streptomycin
aminoglycosides
critically important
sulfamethoxazole
sulfonamides
highly important
tetracycline
tetracycline
highly important
ampicillin
penicillin
critically important
chloramphenicol
amphenicol
highly important
nalidixic acid
quinolone
critically important
streptomycin
aminoglycosides
critically important
sulfisoxazole
sulfonamides
highly important
trimethoprimsulfamethoxazole
amoxicillin/clavulanate
ampicillin
cefoxitin
ceftiofur
sulfonamides
*
penicillin
penicillin
cephamycin
cephalosporin (3G)
critically important
critically important
highly important
*
ceftriaxone
chloramphenicol
streptomycin
sulfonamide*
tetracycline
cephalosporin
amphenicol
aminoglycosides
sulfonamides
tetracycline
highly important
highly important
critically important
highly important
highly important
amoxicillin/clavulanate penicillin
critically important
ampicillin
cefoxitin
ceftiofur
penicillin
critically important
cephamycin
highly important
cephalosporin (3G) *
ceftriaxone
chloramphenicol
kanamycin
streptomycin
sulfonamide*
tetracycline
cephalosporin
amphenicol
aminoglycosides
aminoglycosides
sulfonamides
tetracycline
highly important
highly important
highly important
critically important
highly important
highly important
sulfonamide*
tetracycline
sulfonamides
tetracycline
highly important
highly important
2004 MN
S. Agona
2004 NY
S. Istanbul
Chicken
42
14
0
tetracycline
tetracycline
highly important
2005 MN
S. Heidelberg
Chicken
4
1
0
gentamicin
streptomycin
sulfonamide*
aminoglycosides
aminoglycosides
sulfonamides
critically important
critically important
highly important
Sandwich,
turkey
24
0
0
WHO Status
E. coli O27:H7/ST
(ETEC)
E. coli O6:H16
(ETEC)
0
1
Drug Family
Appendix. Antibiotic-Resistant Foodborne Outbreaks
Year Location Bacteria
Food/Source
Cases Hosp Death Resistances
2005 TN
Unknown
19
S. Heidelberg
2005 IN, MI,
MO, OH
S. Braenderup
2005 CO
S. Typhimurium
S. Newport
2005 CO
S. Typhimurium
Tomato
Unknown
Sushi
84
100
25
2
8
1
0
0
0
0
0
Drug Family
WHO Status
gentamicin
aminoglycosides
critically important
nalidixic acid
streptomycin
tetracycline
quinolone
aminoglycosides
tetracycline
critically important
critically important
highly important
ampicillin
penicillin
critically important
gentamicin
sulfonamide*
tetracycline
aminoglycosides
sulfonamides
tetracycline
critically important
highly important
highly important
amoxicillin/clavulanate penicillin
critically important
ampicillin
cefoxitin
ceftiofur
penicillin
critically important
cephamycin
highly important
cephalosporin (3G) *
ceftriaxone
chloramphenicol
streptomycin
sulfonamide*
tetracycline
cephalosporin
amphenicol
aminoglycosides
sulfonamides
tetracycline
highly important
highly important
critically important
highly important
highly important
amoxicillin/clavulanate penicillin
critically important
ampicillin
chloramphenicol
streptomycin
sulfonamide*
trimethoprimsulfamethoxazole
tetracycline
penicillin
amphenicol
aminoglycosides
sulfonamides
sulfonamides
critically important
highly important
critically important
highly important
*
tetracycline
highly important
quinolone
critically important
2006 AR
S. I 4,[5],12:i-
Unknown
14
4
0
nalidixic acid
2006 PA
S. Typhimurium
Queso fresco, 20
unpasteurized;
raw milk
2
0
amoxicillin/clavulanate penicillin
critically important
ampicillin
cefoxitin
ceftiofur
ceftriaxone
chloramphenicol
sulfonamide*
tetracycline
critically important
highly important
*
highly important
highly important
highly important
highly important
Root vegetable 3
NR
2006 UT
S. Typhimurium
NR
2006 PA
S. Schwarzengrund Unknown
6
0
0
2006 CA
S. Newport
24
NR
NR
Multiple foods
penicillin
cephamycin
cephalosporin (3G)
cephalosporin
amphenicol
sulfonamides
tetracycline
amoxicillin/clavulanate penicillin
critically important
ampicillin
chloramphenicol
streptomycin
sulfonamide*
tetracycline
penicillin
amphenicol
aminoglycosides
sulfonamides
tetracycline
critically important
highly important
critically important
highly important
highly important
amoxicillin/clavulanate
ampicillin
cefoxitin
ceftiofur
penicillin
penicillin
cephamycin
cephalosporin (3G)
critically important
critically important
highly important
*
ceftriaxone
cephalosporin
highly important
amoxicillin/clavulanate
ampicillin
cefoxitin
ceftiofur
ceftriaxone
chloramphenicol
streptomycin
sulfonamide*
tetracycline
penicillin
penicillin
cephamycin
cephalosporin (3G)
cephalosporin
amphenicol
aminoglycosides
sulfonamides
tetracycline
critically important
critically important
highly important
*
highly important
highly important
critically important
highly important
highly important
Appendix. Antibiotic-Resistant Foodborne Outbreaks
Year Location Bacteria
Food/Source
Cases Hosp Death Resistances
2006 IL
Unknown
9
2006 IL
S. Newport
S. Newport
S. Meleagridis
Mexican-style 96
cheese (cotija),
(raw milk)
3
36
0
0
2006 TN
S. Hadar
Unknown
9
1
0
2007 CA, AZ,
ID, NV
S. Newport
Ground beef
43
15
0
2007 MN
2009 7 states
S. Newport
S. Typhimurium
DT104
2009 14 states S. Newport
Unknown
Ground beef
Ground beef
11
14
68
0
6
4
0
0
0
Drug Family
WHO Status
amoxicillin/clavulanate penicillin
critically important
ampicillin
cefoxitin
ceftiofur
ceftriaxone
chloramphenicol
streptomycin
sulfonamide*
tetracycline
critically important
highly important
*
highly important
highly important
critically important
highly important
highly important
penicillin
cephamycin
cephalosporin (3G)
cephalosporin
amphenicol
aminoglycosides
sulfonamides
tetracycline
amoxicillin/clavulanate penicillin
critically important
ampicillin
penicillin
critically important
cefoxitin
cephamycin
highly important
ceftiofur
chloramphenicol
cephalosporin (3G) *
amphenicol
highly important
streptomycin
aminoglycosides
critically important
sulfamethoxazole
sulfonamides
highly important
tetracycline
tetracycline
highly important
streptomycin
aminoglycosides
critically important
tetracycline
tetracycline
highly important
amoxicillin/clavulanate penicillin
ampicillin
penicillin
critically important
critically important
cefoxitin
cephamycin
highly important
ceftiofur
cephalosporin (3G) *
ceftriaxone
cephalosporin
critically important
chloramphenicol
amphenicol
highly important
streptomycin
aminoglycosides
critically important
sulfonamide*
sulfonamides
highly important
tetracycline
tetracycline
highly important
amoxicillin/clavulanate penicillin
critically important
ampicillin
penicillin
critically important
cefoxitin
cephamycin
highly important
ceftiofur
cephalosporin (3G) *
chloramphenicol
amphenicol
streptomycin
aminoglycosides
critically important
sulfamethoxazole
sulfonamides
highly important
tetracycline
tetracycline
highly important
streptomycin
aminoglycosides
critically important
highly important
ampicillin
penicillin
critically important
chloramphenicol
amphenicol
highly important
streptomycin
aminoglycosides
critically important
sulfamethoxazole
sulfonamides
highly important
tetracycline
tetracycline
highly important
amoxicillin/clavulanate penicillin
critically important
ampicillin
penicillin
critically important
cefoxitin
cephamycin
highly important
ceftiofur
cephalosporin (3G) *
cephalothin
cephalosporin (1G) highly important
chloramphenicol
amphenicol
streptomycin
aminoglycosides
critically important
sulfamethoxazole
sulfonamides
highly important
tetracycline
tetracycline
highly important
highly important
Appendix. Antibiotic-Resistant Foodborne Outbreaks
Year Location Bacteria
Food/Source
Cases Hosp Death Resistances
2009 AZ
Ground beef
2
S. Newport
2011 10 states S. Hadar
2011 34 states S. Heidelberg
2011 7 states
S. Typhimurium
Ground turkey
(Jennie-O
ground turkey
burgers)
Ground turkey
(Cargill)
Ground beef
NR
NR
critically important
ampicillin
penicillin
critically important
cefoxitin
cephamycin
highly important
ceftiofur
cephalosporin (3G) *
cephalothin
cephalosporin (1G) highly important
chloramphenicol
amphenicol
streptomycin
aminoglycosides
critically important
sulfamethoxazole
sulfonamides
highly important
tetracycline
tetracycline
highly important
3
0
ampicillin
penicillin penicillin
amoxicillin/clavulanate cephalosporin
cephalothin
tetracycline
tetracycline
136
37
1
ampicillin
streptomycin
20
8
0
NR = Not Reported
20601 3166
27
WHO Status
amoxicillin/clavulanate penicillin
12
Source: Center for Science in the Public Interest
Totals
Drug Family
penicillin
aminoglycosides
highly important
critically important
critically important
highly important
highly important
critically important
critically important
tetracycline
tetracycline
highly important
gentamicin
aminoglycosides
critically important
amoxicillin/clavulanate
ampicillin
ceftriaxone
cefoxitin
kanamycin
streptomycin
sulfisoxazole
tetracycline
penicillin
penicillin
cephalosporin
cephamycin
aminoglycosides
aminoglycosides
sulfonamides
tetracycline
critically important
critically important
critically important
highly important
highly important
critically important
highly important
highly important
* Not on WHO's list of antimicrobials used in human medicine