2019 New and emerging infectious diseases (Ebola, Middle Eastern respiratory syndrome coronavirus, carbapenem-resistant

2019·0.49 MB·English

AmericanJournalofInfectionControl47(2019)A29−A38
ContentslistsavailableatScienceDirect
American Journal of Infection Control
journal homepage: www.ajicjournal.org
StateoftheScienceReview
New and emerging infectious diseases (Ebola, Middle Eastern respiratory
syndrome coronavirus, carbapenem-resistant Enterobacteriaceae,
Candida auris): Focus on environmental survival and germicide
susceptibility
DavidJ.WeberMD,MPHa,b,*,EmilyE.Sickbert-BennettMS,PhDa,b,HajimeKanamoriMD,PhD,MPHc,
WilliamA.RutalaPhD,MPHb
aDepartmentofHospitalEpidemiology,UniversityofNorthCarolinaHospitals,ChapelHill,NC,USA
bDivisionofInfectiousDiseases,UniversityofNorthCarolinaSchoolofMedicine,ChapelHill,NC,USA
cInfectionControlandLaboratoryDiagnostics,TohokuUniversity,Sendai,Japan
KeyWords:
Surface
Environment
Disinfection
In the recent past, we have witnessed the emergence of many DEFINITIONS
new infectious diseases, some of which are major public health
threats. The public health threats posed by emerging diseases TheWorldHealthOrganization(WHO)states,“anemergingdis-
have been well described in 2 reports from the Institute of Medi- easeisonethathasappearedinapopulationforthefirsttime,orthat
cine, 1 in 1992 and 1 in 2001.1,2 Since the outbreak of Legionella mayhaveexistedpreviouslybutisrapidlyincreasinginincidenceor
in 19763,4 and AIDS in 19815,6 later demonstrated to be due to geographicrange.”11TheCentersforDiseaseControlandPrevention
HIVin1983,7manyemerginginfectiousdiseaseshavehadimpor- (CDC) provides the following definition of emerging infections as
tant infection control implications. This review will focus on sev- “infectiousdiseaseswhoseincidenceinhumanshasincreasedinthe
eral of the most important current infection prevention threats past2decadesorthreatenstoincreaseinthenearfuturehavebeen
including Ebola virus, Middle Eastern respiratory syndrome defined as ‘emerging.’” These diseases, which respect no national
(MERS) coronavirus (CoV), carbapenem-resistant Enterobacteria- boundaries, include: (1) new infections resulting from changes or
ceae (CRE), and Candida auris with a focus on mechanisms of evolution of existing organisms; (2) known infections spreading to
transmission,environmentalcontaminationandstability,andger- new geographic areas or populations; (3) previously unrecognized
micide susceptibility. Germicides that will be discussed include infections appearing in areas undergoing ecologic transformation,
chemical sterilantsusedtoprocesscriticalequipmentanddevices and (4) old infections reemergingas a resultof antimicrobial resis-
(eg, surgical instruments, implants), high-level disinfectants that tanceinknownagentsorbreakdownsinpublichealthmeasures.12
areusedto disinfectsemicritical equipmentanddevices(ie, med-
ical equipment or devices that come into contact with nonintact FACTORSINTHEEMERGENCEOFINFECTIOUSDISEASES
skin or mucous membranes), low-level disinfectants used for dis- ANDPREPAREDNESS
infection of surfaces or shared equipment that come into contact
with intact skin (eg, blood pressure cuffs, room surfaces), and Thefactorsleadingtotheemergenceofinfectiousdiseaseshave
antiseptics (ie, germicides used on skin or mucous membranes to beendescribed.13-17Importantly,alltheseauthorsnotedthatwewill
reducethemicrobialflora).8,9Thisreviewupdatesapreviousarti- continuetoseenewandemerginginfectiousdiseasesfortheforesee-
cle that reviewed Ebola and MERS and also reviews CRE and ablefuture.Recentarticleshaveprovidedrecommendationsforpre-
Cauris.10 parednessatthehealthcarefacility,localandnationallevels.10,18-20
KEYCONSIDERATIONSINASSESSINGANDMANAGINGTHETHREAT
OFEMERGINGINFECTIOUSDISEASESINHEALTHCAREFACILITIES
* AddresscorrespondencetoDavidJ.Weber,MD,MPH,UniversityofNorthCarolina
Assessingandmanagingthethreatofanemerginginfectiousdis-
Hospitals,2163Bioinformatics,CB#7030,ChapelHill,NC,27599-7030.
easerequiresanunderstandingofthebiologyofthepathogen,itsepi-
E-mailaddress:[email protected](D.J.Weber).
Conflictsofinterest:Nonetoreport. demiology, the clinical manifestations of infection, the methods of
https://doi.org/10.1016/j.ajic.2019.03.004
0196-6553/©2019AssociationforProfessionalsinInfectionControlandEpidemiology,Inc.PublishedbyElsevierInc.Allrightsreserved.
A30 D.J.Weberetal./AmericanJournalofInfectionControl47(2019)A29−A38
diagnosis, and therapies (if available).10 All health care facilities EVD is characterized by the sudden onset of fever, headache,
shouldhaveahighlycommunicablediseaseplanforagentsthatare myalgias,arthralgiasofthelargejoints,andbackpain.Typically,2-
transmittedbydropletoraerosols(eg,severeacuterespiratorysyn- 3 days after the initial symptoms gastrointestinal symptoms occur
drome [SARS], MERS) or are transmitted by contact (eg, Ebola, includingabdominalpain,nausea,vomiting,anddiarrhea.Amacular
Lassa).10Detailedinformationisbestfound,especiallyearlyinanepi- ormaculopapularskinrashmayappearondays5-7ofthedisease.
demic, on the web pages of local and state health department, the Hemorrhageislesscommon,occurringinonly15%-20%ofpatients.
CDC, and the WHO. For highly communicable diseases, there are 2 Terminalcasesdevelopdisseminatedintravascularcoagulation,sep-
majorareasthatplaceahealthcarefacilityandthepersonnelatsub- ticshock,andmultiorgansystemfailure.Mortalityrangesfrom40%-
stantial risk for disease acquisitionand transmission.10 First, inade- 90%anddepends,inpart,ontheinfectingstrain.
quatescreeningprocedureswhenpatientsenterahealthcarefacility
canpotentiallyallowtransmissionfromanillpatienttohealthcare
Epidemiologyandtransmission
personnel,otherpatients,orvisitors.Second,inadequatesuppliesof
personal protective equipment (PPE) and/or training of health care
Ebola is transmitted person-to-person most commonly through
personnel (HCP) in proper donning and doffing procedures can
directcontact(ie,nonintactskinorviamucousmembranecontact)
increasetheriskofexposureforHCP. withblood,bodyfluids(eg,urine,saliva,sweat,feces,vomit,breast
Akeyfocusofthisarticleistoreviewthetransmissionroutesof
milk,andsemen)ofanillperson,orindirectlyviaobjectssuchasnee-
newandemerginginfectiousagents.Preventingdiseaseacquisition dlesandsyringesthathavebeencontaminatedwithbodyfluidsfrom
via person-to-person transmission or contact with the contami- anillperson(Table1).31Lesscommonmechanismsincludeacquisi-
natedenvironmentdependsonrapidandappropriateinstitutionof
tionfrominfectedfruitbatsornonhumanprimates.Sexualtransmis-
isolation precautions, appropriate hand hygiene, and appropriate
sionhasalsobeendescribed.Ebolaisnottransmittedviatheairorby
disinfection of medical equipment, devices, and the surface envi-
water. However, in Africa it has been acquired by handling bush
ronment. Importantly, once the nature of the emerging disease is
meat.TheincubationperiodofEbolaisgenerally8-10days(range,2-
known (ie, enveloped virus, bacteria, fungi, nonenveloped virus,
21days).Person-to-persontransmissionhasonlyoccurredfromper-
mycobacteria),itispossibletodeterminetheproperantisepticsand
sonswithsignsorsymptomsofEVD.Diagnostictestingisachieved
disinfectants,evenintheabsenceofstudiesoftheexactinfectious
with the use of real time (RT) polymerase chain reaction (PCR) on
agent.21Forexample,anenvelopedvirus(eg,Ebola,MERS-CoV)or blood.32 Viral RNA is usually detectable by PCR between 3 and
vegetative bacterium (eg, CRE) would be inactivated by any agent
10daysaftertheonsetofsymptoms.
active against nonenveloped viruses or mycobacteria. It is impor-
Patients with EVD should be provided appropriate critical care
tanttorememberthatalcoholhasreducedactivityagainstnonen- includingfluidandelectrolytereplacement;oxygentherapytomain-
veloped viruses (eg, norovirus) and no activity against spores (eg,
tainoxygenstatus;medicationstosupportbloodpressure,reducing
Clostridioidesdifficile).
vomitinganddiarrhea,andtomanagefeverandpain;oralorparen-
teral nutrition; and treating coexisting infections (eg, malaria), if
present.33-34 Although there are currently no antiviral drugs
EBOLA
approvedbytheUSFoodandDrugAdministration(FDA),anumber
oftherapiesareunderinvestigationincludingantibody-basedthera-
Historyandmicrobiology
pies (eg, convalescent blood products, monoclonal antibodies), and
drugsandsmallmolecules(eg,Ebolavirusgeneexpressioninhibitors,
ThefirstrecognizedoutbreakofEbolaoccurredinWestAfricain and Ebola virus entry and inhibitors).33-35 A number of preventive
1976.Inthe40yearssincetheinitialoutbreaksinZaireandSudan, vaccinesarecurrentlyinclinicaltrials.33-35
>20 outbreaks have occurred.22 The largest outbreak occurred in
WestAfrica(Guinea,SierraLeone,andLiberia)from2014-2016,and
resulted in 28,600 cases and 11,325 deaths.23 Importantly, in the Environmentalcontaminationandsurvival
2014-2016 outbreak >850 HCP developed confirmed or probable
Ebola virus disease (EVD).24 The percentage of exposed HCP who Ebolavirushasbeenisolatedbycellculturefrommultiplebody
developed EVD has rangedfrom 12.5%-76%.24 The mortality of HCP fluids of infected or convalescent patients including blood, saliva,
who developed Ebola has frequently exceeded 50%.24 Key concerns stool,vaginalfluid,sweat,andurinefordaysormonthsafterillness.36
forHCPincludethelowinoculatingdoserequiredfortransmission; Giventhehighvolumeofdiarrheaandvomitingandthepotentialfor
high frequency of HCP infections, especially in resource poor coun- fomitetransmission,thefrequencyofenvironmentalcontamination
tries;andhighmortality.Asof2019,anEVDoutbreakiscontinuing and survival of Ebola virus is of high concern. Several studies have
withmoderateintensityintheDemocraticRepublicoftheCongo. assessed the frequency of contamination within the health care
Overall,11peopleweretreatedforEbolaintheUnitedStatesdur-
ingthe2014-2016epidemic.23Twooutof149HCPwhocaredfora
patient with EVD in the United States developed EVD; both Table1
recovered.24 ModesoftransmissionofEbolavirus
The microbiology, epidemiology, diagnosis, clinical features, and
Common
treatmentofEbolahavebeenreviewed.22,25-30Ebolaiscausedbya (cid:1)Person-to-personviadirectcontactviabodyfluids(ie,urine,saliva,sweat,feces,
nonsegmented,single-strandednegativeRNAvirusofthefamilyFilo- vomit,breastmilk,andsemen)
viridae. There are 5 identified Ebola virus species, 4 of which are (cid:1)Person-to-personviaindirectcontactduetoenvironmentalcontamination
knowntocausediseaseinhumans:Zaire,Sudan,TaiForest(formerly (eg,needles,syringes)
Coted’Ivoire),andBundibugyo.Thefifth,Restonvirus,hascauseddis- LessCommon
(cid:1)Infectedfruitsbats
easeinnonhumanprimates,butnotinhumans.Thenaturalreservoir (cid:1)Nonhumanprimates(eg,apes,monkeys)
hostofEbolavirusremainsunknown.However,thedetectionofanti- (cid:1)SexualtransmissionviasemenfromamanwhorecoveredfromEbolavirus
bodiesagainstEbolaandEbolavirusfragmentsinfruit-andinsecti- disease(viaoral,vaginal,oranalsex)
vore bats are highly suggestive that these animals serve as a (cid:1)Ingestionofbushmeat
(cid:1)Exposureinalaboratory
reservoir.
D.J.Weberetal./AmericanJournalofInfectionControl47(2019)A29−A38 A31
environment of a patient with EVD by culture37,39 or RT-PCR.37-42 MERS
Although the frequency of environmental contamination was vari-
able,allstudiesreportedsomeenvironmentalsampleswerepositive Historyandmicrobiology
by RT-PCR. Contamination was most often demonstrated for blood
staineditems,37,42andtoilet/latrine,39,40,42orobjectsincloseproxim- The history of MERS has been reviewed.61-63 MERS, a new viral
itytothepatient(eg,mattress,bedrails).37,42SamplesfromPPE(eg, respiratorydiseaseofhumans,wasfirstdescribedin2012andlater
gloves) have tested positive by RT-PCR for Ebola virus.37,42 Viable discoveredtobecausedbyanovelcoronavirus,MERS-CoV(lineage
viruswasnotisolatedineitherofthe2studiesthatculturedenviron- 2CbCoV).TheWHOhasreportedthatbetween2012andDecember
mentalsamples. 2018,therewere2,279laboratory-confirmedcasesofMERS,includ-
TheenvironmentalsurvivalofEbolavirushasbeenstudiedusing ing806associateddeaths(case-fatalityrate=35.3%),reportedglob-
culture-based techniques under a variety of environmental condi- ally.64 Although cases have been reported from 27 countries, the
tions (eg, temperature, humidity), in various liquids, aerosols, and majorityofcases(ie,1,901)havebeenreportedfromSaudiArabia.64
surfaces.43-49Thesestudiesmaybesummarizedasfollows.First,via- TwocasesofMERShavebeenreportedintheUnitedStates,bothof
bleEbolacansurviveinliquids(eg,liquidmedia,tissueculturemedia, whom were health care providers who acquired infection in Saudi
water,liquidblood,plasma)fordaystoweeks.Second,viableEbola Arabia.65NotransmissionhasbeenreportedintheUnitedStates.
viruscanalsosurvivedriedonavarietyofsurfaces(eg,plastic,glass, The microbiology, epidemiology, and clinical manifestations of
stainlesssteel,polypropylene,nitrile,banknotes)fordaystoweeks. MERS have been reviewed.66-72 MERS-CoV, a betacoronavirus, is a
Third,Ebolasurvivesinliquidsandonsurfacesforalongerduration single-stranded, positive-sense enveloped RNA virus that can cause
of time at lower temperatures (eg, 4°C vs 21°C). Fourth, although anacuterespiratoryillnessinhumans.MERS-CoVisazoonoticdis-
aerosol transmission has not been observed, Ebola virus has been easethatistransmittedfromanimals-to-humans.Dromedarycamels,
demonstratedtosurviveinanaerosolfor>3hours.Fifth,survivalof hosts for MERS-CoV, have been implicated in direct and indirect
Ebolaonporoussurfaces,suchascotton,issubstantiallylessthanon transmissiontohumans,althoughtheexactmodeoftransmissionis
steelandplasticsurfaces. unknown.63,67,71Batsarelikelythemainmammalianreservoir.71
Usingmacaques,viableEbolaviruswasdemonstratedtosurvive TheclinicalspectrumofMERSinfectionrangesfromasymptom-
incorpsesforatleast3daysandRNAcouldbedetectedfortissuesfor aticormildrespiratorysymptomstosevereacuterespiratorydisease
theentire10-weekstudyperiod.50EbolaviruswasdetectedbyRT- and death. Typical symptoms of MERS include fever, cough, and
PCR in a deceased patient’s house 14 days after a patient was bur- shortnessofbreath.Pneumoniaiscommonbutnotalwayspresent.
ied.41ConsistentuseofappropriatePPEwithstrictadherencetodon- Gastrointestinal symptoms (vomiting, diarrhea) frequently occur.
ninganddoffingprotocolsiscrucialtopreventingacquisitionofEVD Riskfactorsformoreseverediseaseincludeolderage,comorbidities
duringpatientcare.28,51,52AkeycomponentofreducingHCPriskis (eg, chronic lung diseases, diabetes), and immunosuppression. The
propertraininginPPEdonninganddoffingwithongoingtrainingto diagnosisisconfirmedbyapositiveRT-PCRassaytargetingatleast2
maintaincompetency. differentgenomicregions.Currently,therearenospecifictherapies
orvaccinesavailable.
Susceptibilitytogermicides Epidemiologyandtransmission
Ebolavirusisnotinactivatedbydetergents.53UsingRT-PCR,Cook MERSmaybetransmittedfromperson-to-personviadirectcon-
etal54demonstratedthatEbolavirusoutbreakvariantsdriedwithan tact likely due to droplet transmission (Table 2). This occurs most
organicsoilloadonastainlesssteelcarrierwereinertafter5minutes commonlywhenthereisclosecontactsuchasprovidingunprotected
exposuretosodiumhypochlorite(≥0.5%)andafter2.5minutesexpo- caretoaninfectedpatient.Thusfar,nosustainedcommunitytrans-
sureto70%ethanol.Smitheretal55confirmedtheactivityofsodium mission has been documented. Studies of family clusters and HCP
hypochlorite;104EbolavirusesasmeasuredbyPCRwereinactivated contacts of patients have reported low frequencies of transmission
by0.75%sodiumhypochloritewith10minutescontacttime.Inalater (ie,1%-3%).However,increasedtransmissionhasoccurredinhealth
study, Smither et al56 reported that multiple disinfectants (ie, 0.5% caresettingswithlimitedinfectioncontrolprocedures.Importantly,
hypochlorite,10%hypochlorite,5%peraceticacid,70%ethanol)were MERSmaybetransmittedfromanasymptomaticsource.73However,
effective against dried cell culture medium containing Ebola virus. superspreadershavealsobeenreported.74
However, only 5% peracetic acid consistently reduced Ebola virus TheepidemiologyandpreventionofMERSinhealthcaresettings
titersindriedbloodtoundetectablelevels.Basedonthehierarchyof hasbeenreviewed.10,75-77Infectionpreventionstrategieshavebeen
microbial susceptibility togermicidesand studiesof germicideeffi- informed by the multiple reports of outbreaks of MERS involving
cacy,theCDCstatesthatanyUSEnvironmental ProtectionAgency- healthcarefacilities,78-81andbythelargeoutbreakinSouthKorea.82
(EPA)registeredhospitaldisinfectantwithalabelclaimforanonen- Importantly,duringtheseoutbreaks>20%ofcasesmayhaveoccurred
veloped virus (eg, norovirus, rotavirus, adenovirus) can be used to inhealthcareproviders.Factorscontributingtointrahospitaltrans-
disinfectenvironmentalsurfacesinroomsofpatientswithknownor mission include: (1) the initial symptoms of MERS are nonspecific
suspectedEVD.57
In a systematic review, Kampf58 reported that 80% ethanol was
highlyeffectiveagainstall21tested,envelopedviruseswithin30sec-
Table2
onds.A>4-log reductionofanEbolastrainwasachievedin15sec-
10 ModesoftransmissionofMiddleEasternrespiratorysyndromecoronavirus
onds using the following povidone-iodine solutions: 4%, 7.5%, 10%,
and 3.2% iodine with 78% alcohol.59 Therefore, data suggests that TransmissionWellEstablished
hand antisepsis for skin contamination with Ebola virus can be (cid:1)Human-to-humantransmissionviadirectcontactduetodropletspread
(sourcemaybeasymptomatic)
obtainedwitheitherpovidone-iodineor70%-80%alcohol(although (cid:1)Animal-to-humantransmission(dromedarycamelstohumans)
properPPEshouldalwaysbeworn). TransmissionUnclear
Anultraviolet-light(UV-C)boothwasdemonstratedtoinactivate (cid:1)Human-to-humantransmissionviadirectcontactduetoairbornetransmission
>3-log bacteriophage MS2 (a nonenveloped virus) and could be (cid:1)Human-to-humantransmissionviaindirectcontact(ie,fomites,contaminated
10
usefulfordisinfectionofcontaminatedPPE.60 surfaces)
A32 D.J.Weberetal./AmericanJournalofInfectionControl47(2019)A29−A38
leadingtoafailuretoisolatethepatient;(2)inadequatecompliance organism)anditincludesbacteriathatarenotsusceptibletocarbape-
withinfectioncontrolpractices;(3)inadequatehealthcarefacilities nemsviamorethanonetypeofmechanism.”TheCDCspecifiesthat
(eg, overcrowding, close proximity of patients to cases); (4) use of carbapenem resistance mechanisms include the following: (1) the
aerosolgeneratingprocedures;and(5)prolongedviralshedding.83 production of carbapenemases (called carbapenemase-producing-
CRE),enzymesthatbreakdowncarbapenemsandrelatedantimicro-
Environmentalcontaminationandsurvival bials making them ineffective. This includes enzymes like Klebsiella
pneumoniaecarbapenemase;and(2)thecombinationofmechanisms
Extensiveenvironmentalcontaminationhasbeendocumentedby other than carbapenemase production (called non-carbapenemase-
bothcultureandRT-PCRinclinicalareashousingMERSpatients.84,85 producing-CRE),mostcommonlytheproductionofb-lactamases(eg,
Positive sites have included patient room surfaces (eg, bed sheets, AmpC) in combination with alterations in the bacteria’s cell mem-
bedrails,intravenousfluidhangers),anteroomsurfaces,medicaldevi- brane(eg,porinmutations).TheCDChasreportedthefollowingtypes
ces(eg,portablex-raymachines,thermometers),andair-ventilating of CRE in the United States: NDM, OXA48, VIM, IMP, and Klebsiella
equipment.Touchablesurfaceshavebeenfoundtobecontaminated pneumoniaecarbapenemase.93
through respiratory secretions from clinically fully recovered
patients.84 MERS-CoV has also been detected in air samples in the
Epidemiologyandtransmission
vicinityofpatients.85However,1largeoutbreakevaluationfailedto
demonstrateanytransmissionviathepotentiallycontaminatedenvi-
The biology, epidemiology, and management of CRE have been
ronmentwithoutdirectcontactwiththeindexcase.86 reviewed.94-97Recentarticleshavereviewednewerantibioticthera-
MERS-CoV has been shown to be recoverable after 48 hours on pies for CRE.98,99 Follow-up of hospitalized CRE colonized patients
steelorplasticwashers(20°Cand40%relativehumidity).87Further, demonstrated that the mean duration of colonic carriage was >1
no decrease in stability was observed during aerosolization experi- year.100However,HCParerarely,ifever,colonized.Astudyoffecal
ments.MultiplestudiesonCoVsotherthanMERS-CoVhavedemon-
carriageamongHCPinahospitalendemicforCRErevealednoneof
strated that these viruses can remain viable for days to weeks on 177evaluatedhealthcareproviderswerecolonizedwithCRE.101
environmental surfaces.88,89 Survival is enhanced at low tempera-
ThemainreservoirleadingtohumanCREinfectionsisthehuman
tures(ie,4°Cvs20°C).89
gut.Person-to-persontransmissionviadirectandindirectcontactare
the most common mechanisms of transmission (Table 3). Multiple
Susceptibilitytogermicides
hospital outbreaks have resulted from contaminated endoscopes,
especially duodenoscopes.102-104 These outbreaks have occurred
AsMERS-CoVisanenvelopedvirus,itislikelysusceptibletoEPA-
despiteallstepsincleaningandhigh-leveldisinfectionofendoscopes
registeredhospitaldisinfectantsandFDA-approvedantiseptics.Stud-
compliant with current guidelines. Strategies to provide pathogen-
iesoninactivationofsurrogatesforSARS-CoV(mousehepatitisvirus freeendoscopeshavebeenreviewed.104Watersourcesinthehospital
and transmissible gastroenteritisvirus) demonstratedthe following
(eg,faucets,washbasins,showers,toilets),especiallysinkshavebeen
inactivationafter1-minutecontacttime:(1)fortransmissiblegastro- demonstratedtobeareservoirofCRE.105-107Strategiesandsuccess
enteritisvirus,therewasalog reductionfactorof3.2for70%etha-
10 rates of interventions to eliminate CRE from water reservoirs have
nol, 2.0 for phenolic, 2.3 for ortho-phthalaldehyde, 0.35 for 1:100 been reviewed.105,106 Companion animals have been demonstrated
hypochlorite,4.0for62%ethanol,and3.5for71%ethanol;and(2)for tooccasionallybecolonizedwithCRE.108Thisisofrelevancetohealth
mousehepatitisvirus,log reductionfactorswere3.9for70%etha-
10 care facilities considering that US health care facilities must permit
nol, 1.3 for phenolic, 1.7 for ortho-phthalaldehyde, 0.62 for 1:100 personswith“service”animalsinthefacilityandmanyhospitalsper-
hypochlorite,2.7for62%ethanol,and2.0for71%ethanol.90
mitanimal-assistedtherapy.
GuidancefromtheCDCformanagingpatientswithMERSstates,
StrategiestomanageCREcolonized/infectedpatientsandtocon-
“HCPshouldperformhandhygienebeforeandafterallpatientcon- trol outbreaks in health care facilities have been reviewed.109-111
tact,contactwithpotentiallyinfectiousmaterial,andbeforeputting BoththeWHO112andtheCDC113providedetailedguidanceonmeth-
on and upon removal of PPE, including gloves. Hand hygiene in
odstocontrolCRE.Theuseofbundlestocontrolhorizontaltransmis-
healthcare settings can be performed by washing with soap and sionofCREinhealthcarefacilitieshavebeenreviewed.114
water or using alcohol-based hand rubs. If hands are visibly soiled,
usesoapandwater,notalcohol-basedhandrubs.”91TheCDCfurther
states “Standard cleaning and disinfection procedures (eg, using Environmentalcontaminationandsurvival
cleaners and water to pre-clean surfaces prior to applying an EPA-
registereddisinfectant tofrequentlytouchedsurfacesorobjectsfor CREhasbeenisolatedfromtheenvironmentinthevicinityofhos-
appropriate contact times as indicated on the product’s label) are pitalized colonized/infected patients including pillows, infusion
appropriate for MERS-CoV in healthcare settings, including those pumps, bedside tables, and toilet areas.115-117 The frequency of
patient-care areas in which aerosol-generating procedures are per- recoveryhasvariedamongstudies,butobjectsclosertothepatient
formed.IftherearenoavailableEPA-registeredproductsthathavea aremorelikelycontaminatedwith5%-15%ofsamplesfrombedrails
labelclaimforMERS-CoV,productswithlabelclaimsagainsthuman and over bed tables yielding CRE.115,116 Fecal continence is an
coronavirusesshouldbeusedaccordingtolabelinstructions.”91
Table3
CRE
Modesoftransmissionandreservoirsofcarbapenem-resistantEnterobacteriaceae
Definitionandmicrobiology (cid:1)Patient-to-patientviadirectcontact
(cid:1)Patient-to-patientviaindirectcontact
^Transienthandcarriagebyhealthcarepersonnel
TheCDCdefinesCREforsurveillancepurposesasEnterobacteria-
^Contaminatedsharedmedicaldevices
ceae that are “resistant to imipenem, meropenem, doripenem, or ^Contaminatedendoscopes(especiallyduodenoscopes)
ertapenemORdocumentationthattheisolatepossessacarbapene- (cid:1)Healthcarefacilityreservoirtopatient
mase.”92TheCDCfurtherelaboratesthatCREis“aphenotypicdefini- ^Contaminatedsinks
^Contaminatedendoscopes(especiallyduodenoscopes)
tion (ie, based on the antibiotic susceptibility pattern of the
D.J.Weberetal./AmericanJournalofInfectionControl47(2019)A29−A38 A33
independentpredictorofbeinganonspreaderofCRE.117CREhasalso orPCRassaysspecificforCauris.Multiplevirulencefactorshavebeen
beenisolatedintheenvironmentoflong-termcarefacilities.118 described.133
Havilletal119reportedsurvivalofCREonstainlesssteeldiscsfor Themostcommonclinicalsyndromesreportedhavebeenblood-
>10 days. However, Weber et al120 reported that 3 species of CRE stream infections (candidemia), wound infections, and ear infec-
(Klebsiella, Enterobacter, and Escherichia coli) survived poorly (>85% tions.129Otherclinicalsyndromesreportedhaveincludedinfections
die-offin24hours).Likelythisdifferencewasowingtothefactthat of the respiratory tract, central nervous system, urogenital system,
Havill et al119 used a high inoculum (ie, 5-7-log ) whereas Weber intra-abdominal, skin and soft tissues, and bone.127 Patients with C
10
used a low inoculum (ie, »2-log ), which is similar to the actual auris infection have almost always presented with underlying ill-
10
amountofCREfoundonsurfacesinthevicinityofpatientscolonized/ nessesorcomorbiditiessuchasdiabetes,chronicoracuterenalfail-
infectedwithCRE. ure, pulmonary disease, immunosuppressive conditions, tumor or
malignancies,liverdisease,orsolidorgantransplants.137Riskfactors
Susceptibilitytogermicides forinfectionhaveusuallyincludedcareinanintensivecareunit,the
presenceofindwellingcentralvenouscatheters,arteriallines,Foley
Withrarepossibleexceptions,antibiotic-resistantbacteriainclud- catheters, invasive surgical procedures, mechanical ventilation, and
ingmultidrug-resistantorganismsdonothavereducedsusceptibility priororcontinuedexposuretobroad-spectrumantibioticsandanti-
toEPA-registeredgermicides.121Evenwhenreducedsusceptibilityto fungalagents.132,133,136Mortalityrates>30%havebeenreportedfor
a germicide(eg, quaternaryammonium compounds by methicillin- patientswithinvasiveinfections.127,132,133
resistantStaphylococcusaureus[MRSA])hasbeendemonstrated,the Atthepresenttime,therearenoclinicalbreakpointsforCauris.
pathogenhasnotdemonstratedresistancetotheuseconcentration Highminimuminhibitoryconcentrationshavebeenreportedtoflu-
ofthegermicide.121Kanamorietal122assessedtheefficacyof21ger- conazoleandothertriazoleantifungalssuchasvoriconazole,itraco-
micidesagainstmultiple CREEnterobacteriaceaestrainsat1-minute nazole, and isavaconazole.127,132 Variability in susceptibility of
contact time and in the presence of 5% fetal calf serum. Four high- isolateshasalsobeenreportedtoamphotericin.127
level disinfectants achieved >4-log kill for all tested strains, but
10
0.55% ortho-phthalaldehyde achieved a 2.4-4.8-log kill depending
ontheCREstraintested.Eightdisinfectantsallach1i0eveda >4-log Epidemiologyandtransmission
10
kill. Among the 9 antiseptics tested (70% ethanol, 10% povidone-
Caurishasbeenassociatedwithmultiplenosocomialoutbreaks,
iodine, 2% and 4% chlorhexidine gluconate, 70% isopropyl alcohol,
and 1% chloroxylenol) achieved ≥2.9-log kill against all test CRE especiallyintheintensivecaresetting.139-144AnevaluationofCauris
10 in New York City health care facilities demonstrated epidemiologic
strains. Based on this study, EPA-registered disinfectants and FDA-
links betweencasesin multiple hospitalsand long-termcare facili-
approved antiseptics can be used with assurance for equipment/
ties.138 Importantly, colonization with C auris has been detected at
instrument high-level disinfection, surface disinfection, and hand
multiplebodysitesincludingnares,groin,axilla,andrectum.127Pro-
antisepsis. A UV-C device for room disinfection has been shown to
inactivate>5-log CREreductionindirectlineofsightand>4-log longed colonization has been reported with C auris detected >3
10 10 months after initial isolation and despite multiple negative screens
CRE reduction in indirect line of sight when used at the recom-
andantifungaltherapy.136,138
mended cycle time (ie, 5-10 minutes).123 The effectiveness of UV-C
forroomdisinfectionwasconfirmedinanotherstudy.124 MultiplemechanismsfortransmissionofCaurisarelikelybased
onoutbreakinvestigations(Table4).Riskfactorsforcolonizationor
CAURIS infectionhavebeenreportedtoincludecontactwithpatientsknown
toharborCauris.138,145SharinganenvironmentwithaCaurispatient
or sequential bed occupancy that was previously occupied by a
Historyandmicrobiology
patientwithCaurishasalsobeendescribedasarisk.145Importantly,
CaurisisanovelCandidaspeciesthatwasfirstreportedfollowing patients occupying a room that previously housed a patient with
C auris have acquired C auris even though the room had been
itsisolationfromtheearcanalofapatientinJapanin2009.125Since
decontaminatedpriortooccupancy.145Anoutbreakevaluationfound
then,Caurishasbeenreportedfrommultiplecountriesthroughout
thatuseofreusableprobesfortemperaturemonitoringwasassoci-
theworld.126-128TheCDCreportedthatasofJanuary22,2019,551
atedwithasignificantlyincreasedriskofCauriscolonizationwithan
casesofCaurishadbeenreportedfrom12states,withsomestates
(ie,NewYork,Illinois,NewJersey)reporting>100cases.129Caurisis odds ratio of 6.80.142 Transmission of C auris via transplantation of
lungfromapatientwithrespiratorytractcolonizationorinfectionto
anemergingpathogenthatpresentsaseriousglobalhealththreatfor
thelungtransplantrecipienthasbeenreported.146
the following reasons: (1) it causes serious infections with a high
mortality;(2)itisoftendifficulttoidentifywithstandardlaboratory Caurishasoccasionallybeenisolatedfromhealthcareproviders.
methodsandcanbemisidentifiedinlaboratoriesunlessspecialized Biswaletal144reportedthatCauriswasdetectedonthehandsof4
technologyisused;(3)itisoftenmultidrugresistant(intrinsicorrap-
idly inducible antifungal resistance); (4) it is becoming more wide- Table4
spread geographically; (5) increasing prevalence; (6) biofilm ModesoftransmissionofCandidaauris
formation;(7)persistenceintheenvironment;and(8)ithascaused
Common
multipleoutbreaksinhealthcarefacilities.128,130,131 (cid:1)Patient-to-patientviadirectcontact
The microbiology, clinical syndromes, diagnosis, and treatment of (cid:1)Patient-to-patientviaindirectcontactduetoenvironmentalcontamination
Caurishavebeenreviewed.127,132-136Geneticanalyseshaveshownthat (ie,sharingsamehospitalroom,admissiontoahospitalroompreviously
CaurisismostcloselyrelatedtoClusitaniaeandChaemulonii,although occupiedbyapatientwithCauris)
ithasastrikingdivergencefromsomeotherCandidaspecies.127Cauris LessCommon
(cid:1)Patient-to-patientviaindirectcontact:sharedequipmentduetoinadequate
isoftenmisidentifiedinconventionaldiagnosticlaboratoriesusingbio-
disinfection(eg,thermometer)
chemicaltyping.127Caurismostcommonlyhasbeenmisidentifiedas (cid:1)Patient-to-patientviadirectcontact:donor-derivedtransmission
Chaemulonii,butalsoasCfamata,Csake,Rhodotorulaglutinis,Rmucila- (eg,lungtransplantation)
ginosa, and Saccharomyces boulardii.127,137,138 Currently, accurate (cid:1)Person-to-personviaindirectcontactduetotransientlycolonizedhealth
identificationofCauriscanbeaccomplishedbytheuseofMALDI-TOF careprovider’shands
A34 D.J.Weberetal./AmericanJournalofInfectionControl47(2019)A29−A38
health care providers(2.8%), although this waslikely due to inade- inactivationforEcoli.Importantly,theseinvitroexperimentswere
quate hand hygiene rather than long-term colonization. Schelenz doneunderchallengingconditions(ie,5%fetalcalfserumand1-min-
et al,139 while conducting an outbreak investigation in the United uteexposuretime).Itislikelythatallhigh-leveldisinfectantsthatare
Kingdom,screened(nose,axilla,groin,andthroat)>250healthcare currently approved by the FDA when used appropriately (ie, after
providers for colonization and found only a single person (nurse) appropriatecleaningandthemanufacturer’srecommendedconcen-
transientlycolonizedwithCauris. trationandduration)areeffectiveagainstC.auris.
Theactivityoflow-leveldisinfectantshasbeenevaluatedbyseveral
Environmentalcontaminationandsurvival investigations.152,153 Direct comparison between the studies is
impededbytheuseofdifferenttestconditionsincludingtestmethod,
Widespreadcontaminationofthesurfaceenvironmenthasbeen durationofexposure,andpresenceorabsenceofproteinssuchasfetal
reported by multiple investigators.138 Importantly, contaminated calfserum.Theactivityoflow-leveldisinfectantshasbeenmostcom-
siteshaveincludedsitesinthepatient’sroomsuchassurfaces,toilets, prehensivelyinvestigatedusingthedisc-basedquantitativecarriertest
ventilator/respiratory equipment, and sites outside of the patient’s and is summarized in Table 5.152,153 Importantly, both investigators
room such as computer workstations, thermometers, glucometers, added 5% fetal calf serum to assess germicidal efficacy under more
housekeeping carts, dialysis equipment, ultrasound equipment, and stringentconditions(ie,presenceofproteins).Importantly,quaternary
vital sign machines.138 The environmental survival of C auris has ammoniumdisinfectantsaloneweresignificantlylesseffectiveagainst
beenstudied.144,147,148Inlaboratorytests,CaurisandotherCandida C auris than other products.152,153 Some investigators reported that
spp weredemonstrated to persistfor 7 dayson moistordry (steel concentrations of sodium hypochlorite ≥1,000 ppm were effective in
disks) surfaces.147 Survival on dry linen for up to 7 days has been killing >4-log10 C auris in 3-5 minutes,150,151 whereas others153
demonstrated.148Cauriscellshavebeendemonstratedtoremainvia- reported sodium hypochlorite »1,200 ppm at an exposure time of
bleonplasticsurfacesforatleast4weeks,or2weeksaftertheywere 1minuteresultedinonlya1.6-log10reductioninCauris.Itisunclear
nolongerculturable.148 whetherthelongerexposuretimesandlackofproteinloadledtothe
high reduction rates reported by Abdolrasouli et al150 and Moore
Susceptibilitytogermicides et al.151 However,all investigatorshavereported that a 1:10 dilution
of 5.25% sodium hypochlorite is effective in killing >4-log C auris
10
Severalreviewshaveincludedadiscussionofthesusceptibilityof evenwithshortexposuretimes(ie,1minute)andinthepresenceof
Cauristogermicides.149ThesusceptibilityofCauristogermicides(ie, protein.152,153 Based on current studies, the CDC states “Quaternary
antisepticsanddisinfectants)hasbeenstudiedbyseveralinvestiga- ammoniumcompounds(QACs)thatareroutinelyusedfordisinfection
tors.139,144,150-153 Rutala et al153 assessed the germicidal activity of may not be effective against C auris....Until further information is
high-leveldisinfectantsand/orchemicalsterilantsandreportedthat availableforCauris,CDCrecommendsuseofanEnvironmentalProtec-
allagents(ie,0.20%peraceticacid,2.4%glutaraldehyde,0.65%hydro- tion Agency (EPA)-registered hospital-grade disinfectant effective
genperoxideplus0.14%peroxyaceticacid,2%acceleratedhydrogen against Clostridium difficile spores (List K)”.154 CDC further states that
peroxide)achieveda≥4.1-log reductionofCauriswiththeexcep- whentheuseofproductsonListKisnotfeasible,publishedresearch
10
tion of 0.55% ortho- phthalaldehyde that achieved only a 2.3-log has found that the following products led to a substantial reduction
10
Table5
SusceptibilityofCandidaauristolow-leveldisinfectantsusedforsurfacedisinfection*
HighlyEffective(≥3.8-log10 ModeratelyEffective(2.0-3.8-log10 LessEffective(<2.0-log10Reduction)
Reduction)[ET,minutes] Reduction)[ET,minutes] [ET,minutes]
(cid:1)70%isopropylalcohol[1] (cid:1)>5%aceticacid(pH2.0) (cid:1)1:50dilution,5.25%sodium
(cid:1)1:10dilution,5.25%sodium (whitedistilledvinegar)[3] hypochlorite
hypochlorite(»6,100-6,700ppm)[1] (»1,245ppm)[1]
(cid:1)1:128dilution,9.09%o-phenylphenol, (cid:1)1:256dilution,21.7%QACk[1]
7.66%p-tertiaryamylphenol[1] (cid:1)QAC{[1]
(cid:1)1.4%hydrogenperoxide[1] (cid:1)QAC#[1]
(cid:1)58%ethanol,0.1%QACy[1]
(cid:1)55%isopropylalcohol,0.5%QACz[1]
(cid:1)28.7%isopropylalcohol,27.3%ethyl
alcohol,0.61%QACx[1]
(cid:1)0.65%sodiumhypochlorite[1]
(cid:1)0.39%sodiumhypochlorite[1]
(cid:1)0.825%sodiumhypochlorite[1]
(cid:1)Peraceticacid1200ppm,hydrogen
peroxide<1%,aceticacid[3]
(cid:1)1.4%hydrogenperoxide[1]
(cid:1)0.5%hydrogenperoxide[10]
(cid:1)29.4%ethylalcohol[0.5]
NOTE.SusceptibilityofCandidaauristolow-leveldisinfectantsusedforsurfacedisinfection.152,153
ET,exposuretime;ppm,partspermillion;QAC,quaternaryammoniumcompound.
*Disc-basedquantitativecarriertest,1minuteexposuretimeunlessotherwisenoted,5%fetalcalfserum.
yQAC:alkyl(C1450%,C1240%,C1610%)dimethylbenzylammoniumsaccharinate0.1%.
zQAC:n-alkyl(C1268%,C1432%)dimethylethylbenzylammoniumchlorides0.25%;n-alkyl(C1460%,C1630%,C125%,C185%)dimethylbenzylammoniumchlorides0.25%.
xQAC:didecyldimethylammoniumchloride0.61%.
kQAC:octyldecyldimethylammoniumchloride6.51%;dioctyldimethylammoniumchloride2.604%;didecyldimethylammoniumchloride3.906%;alkyl(50%C14,40%C12,10%
C16)dimethylbenzylammoniumchloride8.68%.
{Alkyldimethylbenzylammoniumchlorides.
#Didecyldimethylammoniumchloride,n-alkyldimethylbenzylammoniumchloride.
D.J.Weberetal./AmericanJournalofInfectionControl47(2019)A29−A38 A35
Table6 antisepticsmightreducetheburdenofCaurisontheskin,andthere-
SusceptibilityofCandidaauristoantisepticsinselectedstudies* fore provide a potentially valuable tool for infection prevention,
remainsunclear.TheCDCstatesthatwhencaringforpatientswithC
Disinfectant Log10Reduction(minutes) Reference auris “healthcare personnel should follow standard hand hygiene
Alcohol practices,whichincludealcohol-basedhandsanitizeruseor,ifhands
70%alcohol 6.0(NS) Biswaletal,2017144y
70%ethanol 4.0(1)z Rutalaetal,2019153 are visibly soiled, washing with soap and water. Wearing gloves is
70%isopropanol 3.8(1)z Rutalaetal,2019153 notasubstituteforhandhygiene.”154
CHG
0.5% 6.0(NS) Biswaletal,2017144
2.0% 1.6(1)z Rutalaetal,2019153 References
4.0% 1.9(1)z Rutalaetal,2019153
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