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Epidemiology of healthcare-associated infections among patients from a hemodialysis unit in southeastern Brazil

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b r a z j i n f e c t d i s . 2014;18(3):327–330

The

Brazilian

Journal

of

INFECTIOUS

DISEASES

w w w . e l s e v i e r . c o m / l o c a t e / b j i d

Brief

communication

Epidemiology

of

healthcare-associated

infections

among

patients

from

a

hemodialysis

unit

in

southeastern

Brazil

Silvia

Eduara

Kennerly

de

Albuquerque

a,∗

,

Ricardo

de

Souza

Cavalcante

a,b

,

Daniela

Ponce

c

,

Carlos

Magno

Castelo

Branco

Fortaleza

a,b

aComissãodeControledeInfecc¸ãoRelacionadaàAssistênciaemSaúde,HospitaldasClínicasdaFaculdadedeMedicinadeBotucatu,

UNESP–UnivEstadualPaulista,CityofBotucatu,Brazil

bDepartamentodeDoenc¸asTropicaiseDiagnósticoporImagem,FaculdadedeMedicinadeBotucatu,UNESPUnivEstadualPaulista,

CityofBotucatu,Brazil

cDisciplinadeNefrologia,DepartamentodeClínicaMédica,FaculdadedeMedicinadeBotucatu,UNESPUnivEstadualPaulista,Cityof

Botucatu,Brazil

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received30March2013 Accepted12October2013

Availableonline22November2013

Keywords: Infectioncontrol Hemodialysis

Bloodstreaminfections Catheter-relatedinfections

a

b

s

t

r

a

c

t

Patientssubmittedtohemodialysisareatahighriskforhealthcare-associatedinfections (HAI).PresentlytherearescarcedatatoallowbenchmarkingofHAIratesindeveloping coun-tries.Also,moststudiesfocusonlyonbloodstreaminfections(BSI)orlocalaccessinfections (LAI).OurstudyaimedtoprovideawideoverviewofHAIepidemiologyinahemodialysis unitinsoutheasternBrazil.Wepresentdatafromprospectivesurveillancecarriedoutfrom March2010throughMay2012.Rateswerecompared(mid-pexacttest)andtemporally ana-lyzedinShewhartcontrolchartsforPoissondistributions.TheoverallincidenceofBSIwas 1.12per1000access-days.Theratewashigherforpatientsperformingdialysisthrough cen-tralvenouscatheters(CVC),eithertemporary(RR=13.35,95%CI=6.68–26.95)orpermanent (RR=2.10,95%CI=1.09–4.13),ascomparedtothosewitharteriovenousfistula.Controlcharts identifiedaBSIoutbreakcausedbyPseudomonasaeruginosainApril2010.LAIincidencewas 3.80per1000access-days.IncidenceratesforotherHAI(per1000patients-day)wereas follows:upperrespiratoryinfections,1.72;pneumonia,1.35;urinarytractinfections,1.25; skin/softtissuesinfections,0.93.Thedatapointouttotheusefulnessofapplyingmethods commonlyusedinhospital-basedsurveillanceforhemodialysisunits.

©2013 ElsevierEditoraLtda.Allrightsreserved.

Patients with end-stage renal disease (ESRD) undergoing hemodialysis are especially prone to acquiring healthcare-associatedinfections(HAI).1Thisisduetoboththedialysis

procedureand totheimmunecompromisingeffectsofthe underlyingdisease.2However,likeallHAI,thosehappeningin

Correspondingauthorat:ComissãodeControledeInfecc¸ãoRelacionadaàAssistênciaemSaúde,HospitaldasClínicasdaFaculdadede

MedicinadeBotucatu,DistritodeRubiãoJunior,S/N–CEP18618-970,Brazil. E-mailaddress:eduara.cciras@gmail.com(S.E.K.deAlbuquerque).

hemodialysispatientscanbepreventedwiththe implemen-tationofinfectioncontrolprotocols.3

There is a substantial amount of literature on HAI in hemodialysis units(HU) foroutpatients.4,5 Most reportson

thissubjectfocusspecificallyonbloodstreaminfections(BSI)

1413-8670/$–seefrontmatter©2013 ElsevierEditoraLtda.Allrightsreserved.

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328

braz j infect dis.2014;18(3):327–330

or localaccess infection (LAI).6,7 Also,the vast majority of

studieswereconductedindevelopedcountries.4Since

bench-markingisauseful toolformeasuringtheeffectivenessof infection controlpolicies,dataon theincidenceofHAIs in hemodialysisindevelopingcountriesareneeded.

In2011,theBrazilianSocietyofNephrologyestimatedthat therewere45,000patientsundergoinghemodialysisinBrazil.8

Approximately91%ofpatients’therapiesweresupportedby theBrazilianPublicHealthSystem(“SistemaÚnicodeSaúde” –SUS).ThoughtherearegovernmentalrulesforcollectingHAI datainHU,nopublicreportispresentlyavailable.9Ourstudy

aimedtocontributetotheknowledgeonthisissue,presenting andanalyzingdataontheepidemiologyofHAIinaHUinthe cityofBotucatu,SãoPauloState,southeasternBrazil.

TheHUisaffiliatedtotheBotucatuMedicalSchoolteaching hospital.Itisthereferenceforhemodialysisforanarea com-prising 500,000 inhabitants. Prospective active surveillance ofHAIs has been carried out sinceMarch 2010.Our study focusesondatafromMarch2010throughMay2012. Surveil-lancemethodsincludeddailyvisitstotheunit,inspectionof cathetersaccesssitesandreal-timereviewofmedicalcharts. Wealsoperformedmonitoringofmicrobiologicalresults.The HAIdefinitionsfollowedtheCentersforDiseasesControland Prevention(CDC)guidelines.10TheincidencedensityofBSI

and LAI was expressed ininfections per 1000 access-days. Incidencewascalculatedforgroupsusingdifferentvascular accesses:temporarycatheters;permanent catheters;grafts; or arteriovenousfistulas.For all other HAIs, incidencewas expressedininfectionsper1000patient-days.

Comparisonsofgroupswereperformedusingthe mid-p exacttestinOpenEpisoftware(©EmoryUniversity,Atlanta, USA).Forestplotchartswerebuiltinafreeonlineapplicative (http://www.stattools.net/ForestPlotPgm.php).

Wealsoassessedthetemporalbehaviorofthoseinfections, usingShewhartcontrolcharts.11Briefly,webuiltchartsbased

onthePoissondistribution(alsoknownasu-charts).Monthly incidencerateswereused.Themeanrate(u)wascalculated forthewholeperiodwiththefollowingformula:

u= sumofmonthlyHAIcases

sumofmonthlyaccessdays

Thestandarderror(sigma)wasobtainedforeachmonth withtheformula:

sigma=squareroot

u

monthlyaccessdays

Finally,wedefined“upperwarninglimit”(UWL)and“upper control limit” (UCL) as two and three sigma values above themeanrate,respectively.Followingguidelinesproposedby Sellick,11wedefinedatypicaloccurrencesbasedonthefinding

ofonemonth’sincidenceabovetheUCLorvaluesaboveUWL fortwoconsecutivemonths.

Duringthestudyperiod,atotalof49,831patient-dayswere counted, which wasequal tothe sum ofaccess-days. The number of accessdays for specific groups was: temporary catheter,2460;permanentcatheter,19,110;graft,900;fistula, 27,361.

ThepooledBSI incidenceforthe study periodwas 1.12 per1000access-days(95%confidenceinterval[CI],0.86–1.45). Theincidence(per1000access-days)foraccessgroupswas

Short-term catheters

Long-term catheters

All catheters (grouped)

Grafts

0.01 0.1 1 10 100 Forest plot

RR = 13.35; 95%CI = 6.68-26.95.

RR = 2.10; 95%CI = 1.09-4.13.

RR = 3.38; 95%CI = 1.89-6.30.

RR = 2.02; 95%CI = 0.09-11.34.

Fig.1–Graphiccomparison(forestplot)oftheincidenceof bloodstreaminfectionsrelatedtoseveralvascularaccesses, usingarteriovenousfistulaasareferencecategory.Note.

RR,rateratio;CI,confidenceinterval.

asfollows:temporarycatheters,7.32(95%CI,4.47–11.34); per-manent catheters,1.15 (95%CI,0.74–1.71);grafts,1.11 (95% CI, 0.06–5.48), and fistula, 0.55 (95% CI, 0.32–0.88). TheBSI incidencewassignificantlyhigher(p<0.05)forbothcatheters groups, ascomparedtothefistulagroup(Fig. 1).Themost frequentagentsofBSI(recoveredfrombloodcultures)were: Staphylococcus aureus (36.6%), coagulase-negative staphylo-cocci (CoNS;20.0%),Klebsiellaspp. (16.7%),andPseudomonas aeruginosa(15.0%).OtherGram-negativebacilliaccountedfor 13.3% ofcases.Theresistancepatternofthose agentswas noteworthy.AmongGram-positivecocci,resistanceto methi-cillin was found in 72.7% of S. aureus and 100% of CoNS. Gram-negative bacilli were also often multidrug-resistant. Resistance tothirdgenerationcephalosporinswasfoundin threeoutoftenKlebsiellaspp.andinthetwoEscherichiacoli strainscausingBSIinthestudyperiod.Ontheotherhand,P. aeruginosaresistancetocarbapenems(11.1%)andceftazidime (22.2%)waslow.

ThepooledLAIincidencewas3.80(95%CI,3.30–4.39)per 1000access-days.Theincidencewassignificantlyhigherfor patientswithpermanentcatheters(9.58;95%CI,8.26–11.04) when compared to those with temporary catheters (2.03, 95%CI,0.66–4.74).LAIincidenceforfistulaswas0.07(95%CI, 0.01–0.24)per1000access-days.TherewasnoLAIingraftsin thestudyperiod.

Incidence rates for other HAI (per 1000 patients-day) were as follows:upper respiratoryinfections, 1.72 (95%CI, 1.35–2.16);pneumonia,1.35(95%CI,0.73–1.97);urinarytract infections (UTI), 1.25 (95% CI, 0.94–1.93); skin/soft tissues infections,0.93(95%CI,0.67–1.26);othersites,0.12 (95%CI, 0.04–0.27).Gram-negativepredominatedamongagentsofUTI: Klebsiellaspp.(33.9%),E.coli(27.5%),Enterobacter(14.5%)andP. aeruginosa(14.5%).TwothirdsofKlebsiellaandE.coliisolates producedextended-spectrumbeta-lactamases.

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brazj infect dis.2014;18(3):327–330

329

0 1

Rate Mean

UWL UCL

Rate Mean

UWL UCL 2

3 4 5 6

0 1 2 3 4 5 6 7 8 9 10

Mar-10 Apr-10 Ma

y-10

J

un-10 Jul-10 Aug-10 Sep-10 Oct-10 No

v-10

Dec-10 Jan-11 Feb-11 Mar-11 Apr-11 Ma

y-11

J

un-11 Jul-11 Aug-11 Sep-11 Oct-11 No

v-11

Dec-11 Jan-12 Feb-12 Mar-12 Apr-12 Ma

y-12

Mar-10 Apr-10 May-10 Jun-10 Jul-10 Aug-10 Sep-10 Oct-10 No

v-10

Dec-10 Jan-11 Feb-11 Mar-11 Apr-11 May-11 Jun-11 Jul-11 Aug-11 Sep-11 Oct-11 No

v-11

Dec-11 Jan-12 Feb-12 Mar-12 Apr-12 May-12

A

B

Fig.2–Shewhartcontrolchartsformonthlyincidenceratesofbloodstreaminfections(A)andlocalaccessinfections(B).

Note.UWL,upperwarninglimit;UCL,uppercontrollimit.

whichoninvestigationprovedtoberelatedtocontamination ofwatersupply.WealsodetectedariseintheincidenceofLAI intheendofthestudyperiod,concurrentlywiththehiringof newnursingpersonnel.

Therearesimilaritiesbetweeninfectionsoccurringin hos-pitalwardsandthoseaffectingoutpatientsonhemodialysis. Thisisparticularlytrueforcatheterrelatedinfections.Infact, both BSIand LAI are similar to their nosocomial counter-parts interms ofetiology,pathogenesis, and prevention.12

It is somewhat surprising that epidemiological tools from nosocomial infection surveillance are rarely applied in HU.

Benchmarkingisoneofthosevaluablestoolsforinfection control.13Thecomparisonofparticularunitswithaggregate

datafrommulticentersurveillanceprovidesabasisfor self-assessmentandforestablishingpoliciesandgoals.Themost complete data for benchmarking of hemodialysis-related infections were reported bythe CDC’sNational Healthcare SafetyNetwork(NHSN).13NHSNdatawasexpressedin

infec-tionsper100patient-months.Whenweconvertedourdata tothatunit,BSIincidencevalueswereasfollows:3.5 (perma-nentcatheter),21.9(temporary catheter),3.3(graft)and 1.7 (fistula).TheNHSNdataforthesegroupsare4.2,27.1,0.9and 0.5,respectively.Eventhoughtheincidenceofcatheter-related BSIinourinstitutionwasslightlylowerthanthatreportedby NSHN,itwasthreetimeshigherforpatientsusinggraftsand fistula.Ontheotherhand,ourdataonLAIrelatedtoNSHN incidenceinthefollowingproportions:temporarycatheters, 28.8(ourHU)/5.1(NHSN);permanentcatheters,6.9/1.7;graft, 0/0.4;fistula,0.2/0.2.Unfortunately,nostandardsfor bench-markingareavailableforHUinBrazil.

Control charts are other important tools for HAI surveillance.11 The follow-up of monthly rates allows

infection control practitioners to assess tendencies and to identifyatypicalsituations(suchasoutbreaks).Controlcharts wereparticularlyhelpfulforinfectioncontroldiagnosisand policyplanninginourHUinthestudyperiod.Thefindingof atypicalincidencesforBSIand LAI supportedarevisionof

thewatersupplyandastrategyforcontinuouseducationfor nursesandnursingtechnicians.

Although there are few reports on infection sites other than BSIand LAI, theyare byno means negligible.Recent studies have indicated hemodialysis units as sources of healthcare-associatedpneumonia.14,15Kawasakietal.found

that hemodialysis-associated pneumonia (HDAP) differed from casesarisinginthecommunityinbothetiology(with predominanceofStaphylococcusaureus)andseverity(withhigh case-fatalityratio).16TherateofHDAPinourstudy(1.35per

1000patients-day)wassimilartothatreportedfornosocomial pneumoniaamongadultpatientsnotsubmittedto mechani-calventilationinaBrazilianhospital(whichwas1.02per1000 patients-day).17Thissuggeststhattheunderlyingdiseaseand

exposuretohealthcaredonotdifferbetweendialysis units andnoncriticalhospitalwards.Eventhoughfurtherstudies focusingthisissuearenecessary,theextensionofsurveillance forHDAP and other infection sites (not relatedto vascular devices)maybeusefulfortimelydetectionandappropriate managementofindividualcasesoroutbreaks.

In conclusion, our study found that BSI and LAI and endemicinourHU, withatypicalpeaks relatedtoworking processes. Also,it allowed ustoidentifyhigh incidenceof infectionsinothersites,especiallyHDAP.Aboveall,ourdata underscore the usefulnessofapplying methodscommonly used inhospital-based surveillance toassess the safety of healthcareforpatientsundergoinghemodialysis.

Conflicts

of

interest

Theauthorsdeclarenoconflictsofinterest.

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surveillanceandauditinginarenalcareenvironment.JRen Care.2011;37:167–73.

2. ChoncholM.Neutrophildysfunctionandinfectionriskin end-stagerenaldisease.SeminDial.2006;19:291–6.

3. Pugh-ClarkeK,DonlonS,McCannM.Preventionofinfection inpatientswithchronickidneydiseasepart1:applicationof infectioncontrolprinciplestotherenalcareenvironment.J RenCare.2010;36:191–8.

4. TokarsJI,MillerER,SteinG.Newnationalsurveillancesystem forhemodialysis-associatedinfections:initialresults.AmJ InfectControl.2002;30:288–95.

5. BagdasarianN,HeungM,MalaniPN.Infectiouscomplications ofdialysisaccessdevices.InfectDisClinNorthAm.

2012;26:127–41.

6. Kybartien ˙eS,Skarupskien ˙eI,Ziginskien ˙eE,KuzminskisV. Vascularaccessforhemodialysis:creation,functioning,and complications(dataoftheHospitalofKaunasUniversityof Medicine).Medicina(Kaunas).2010;46:550–5.

7. SucupiraC,AbramczykML,deAbreuCarvalhaesJT,de Moraes-PintoMI.Surveillancesystemof

hemodialysis-associatedinfectionsinapediatricunit.Infect ControlHospEpidemiol.2012;33:521–3.

8. SessoRC,LopesAA,ThoméFS,LugonJR,WatanabeY,Santos DR.ChronicdialysisinBrazil—ReportoftheBrazilianDialysis Census,2011.JBrasNefrol.2012;34:272–7.

9. Agência.NacionaldeVigilânciaSanitária(ANVISA), Resoluc¸ãodaDiretoriaColegiada(RDC),154;2004.

10.CentersforDiseasesControlandPrevention.National HealthcareSafetyNetwork.Atlanta:DialysisEvent SurveillanceManual;2013.http://www.cdc.gov/nhsn/PDFs/ pscManual/Dialysis-Manual.pdf

11.SellickJrJA.Theuseofstatisticalprocesscontrolchartsin hospitalepidemiology.InfectControlHospEpidemiol. 1993;14:649–56.

12.DormanA,DaintonM.Reducinghaemodialysisaccess infectionrates.BrJNurs.2011;20:621–7.

13.KlevensRM,EdwardsJR,AndrusML,etal.Dialysis SurveillanceReport:NationalHealthcareSafetyNetwork (NHSN)-datasummaryfor2006.SeminDial.2008;21:24–8.

14.AminA,KollefMH.Healthcare-associatedpneumonia.Hosp Pract(Minneap).2010;38:63–74.

15.CarratalàJ,Garcia-VidalC.Whatishealthcare-associated pneumoniaandhowisitmanaged?CurrOpinInfectDis. 2008;21:168–73.

16.KawasakiS,AokiN,KikuchiH,etal.Clinicaland microbiologicalevaluationofhemodialysis-associated pneumonia(HDAP):shouldHDAPbeincludedin healthcare-associatedpneumonia?JInfectChemother. 2011;17:640–5.

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