Epidemiology and microbiological profile comparison between community and hospital acquired infections: A multicenter retrospective study in Lebanon

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Epidemiology and microbiological profile comparison

between community and hospital acquired infections: A

multicenter retrospective study in Lebanon

R. Matta, Souheil Hallit, R. Hallit, W. Bawab, Anne-Marie Rogues, P.

Salameh

To cite this version:

R. Matta, Souheil Hallit, R. Hallit, W. Bawab, Anne-Marie Rogues, et al.. Epidemiology and

mi-crobiological profile comparison between community and hospital acquired infections: A multicenter

retrospective study in Lebanon. Journal of Infection and Public Health, Elsevier, 2018, 11 (3),

pp.405-411. �10.1016/j.jiph.2017.09.005�. �hal-03164875�

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ContentslistsavailableatScienceDirect

Journal

of

Infection

and

Public

Health

j o u r n al ho me p ag e :h t t p : / / w w w . e l s e v i e r . c o m / l oc a t e / j i p h

Epidemiology

and

microbiological

proﬁle

comparison

between

community

and

hospital

acquired

infections:

A

multicenter

retrospective

study

in

Lebanon

Roula

Matta

a

_,

_Souheil

_Hallit

a,b,c,d,e,∗

_,

_Rabih

_Hallit

e

_,

_Wafaa

_Bawab

a

_,

_Anne-Marie

_Rogues

f

_,

Pascale

Salameh

a,f,g

a_Lebanese_University,_Faculty_of_Pharmacy,_Beirut,_Lebanon

b_Occupational_Health_Environment_Research_Team,_U1219_BPH_Bordeaux_Population_Health_Research_Center_Inserm_—_Université_de_Bordeaux,_France c_Psychiatric_Hospital_of_the_Cross,_Jal_Eddib,_Lebanon

d_Saint-Joseph_University,_Faculty_of_Pharmacy,_Beirut,_Lebanon

e_Holy_Spirit_University_of_Kaslik,_Faculty_of_Medicine_and_Medical_Sciences,_Kaslik,_Lebanon f_Unité_INSERM_657,_Bordeaux₂_University,_Bordeaux,_France

g_Lebanese_University,_Faculty_of_Medicine,_Beirut,_Lebanon

a

r

t

i

c

l

e

i

n

f

o

Articlehistory: Received5March2017

Receivedinrevisedform21August2017 Accepted9September2017 Keywords: Hospital Community Acquiredinfections Resistance

a

b

s

t

r

a

c

t

Background:Theobjectiveofthisstudyistoidentifyandcharacterizethespeciesresistanceofdifferent pathogensbetweencommunityacquiredandhospitalacquiredinfectionspointingatpatients’related independentco-morbiditiesandsocio-demographicfactors.

Methods:Itwasaretrospectivecohort,multicenterstudyfromﬁveprivatehospitalslocatedinBeirutand MountLebanon.Twohundredﬁfty-eightadultpatientswereincluded.

Results:110Gramnegativepathogensand26Grampositivepathogenswereimplicatedinhospital acquiredinfections.TheGram-negativebacteriathatshowedapositivecorrelationregardingpatient’s typeofinfectionwerePseudomonasaeruginosa(12%),Klebsiellapneumoniae(6.2%)andAcinetobacter bau-mannii(3.1%).Thesebacteriaweremorefrequentinpatientswithhospitalacquiredinfections(P=0.002, 0.013and0.017respectively).TheratioofmethicillinresistantStaphylococcusaureus,Extended Spec-trumBetaLactamaseproducingEscherichiacoliandK.pneumoniaeandmultidrugP.aeruginosashowed highsigniﬁcanceinhospitalacquiredinfections.Thelogisticregression,showedasigniﬁcantrelationship betweenresistantbacteriaandage(p<0.001,ORa=5.680,CI[2.344;13.765])andimmunosuppressed state(p=0.003,ORa=3.137,CI[1.485;6.630])andaninverserelationshipforChronicObstructive Pul-monaryDisease(COPD)(p=0.006,ORa=0.403,CI[0.212;0.765]).

Conclusion:Ourresultsconﬁrmthathospitalacquiredinfections/bacteriahavehigherratesofresistance whencomparedtocommunityacquired;theseratesincreasewithage,immunosuppressionandare inverselyproportionalwithCOPD.Therefore,physiciansshouldbeawareofpatients’comorbiditiesto properlyguideinitialtherapy.

creativecommons.org/licenses/by-nc-nd/4.0/).

Introduction

Hospitalsareathreateningenvironmentbecauseofavariable numberofvirulentpathogensthatarebroughttoitfromthe com-munitythroughadmittedpatients;thesepatientsarethenexposed

∗ Correspondingauthorat: Street8,building560,1stﬂoor,Biakout, Mount Lebanon,Lebanon.

E-mailaddress:souheilhallit@hotmail.com(S.Hallit).

not only to the indigenous hospital flora but also to the flora ofothersickindividuals[1].Thisisaresultofimpaireddefense mechanismandthecolonizationofresistantmicroorganisms[2]. Hospitalacquiredinfectionsarequiteacommonfeatureinthe hos-pitalsthroughouttheworld.Theprevalenceofhospitalacquired infections isgenerallyhigherin developingcountriesoflimited resources[3].Thesebacteriaaregenerallyresistanttoantibiotics, owingtotheheavyuseofwidespectrumantibioticsinhospital set-tings,whichputsahighselectivepressureonbacteriaandinduces difficulttotreatinfections.Thus,hospitalacquiredinfectionshave

https://doi.org/10.1016/j.jiph.2017.09.005

1876-0341/©2017TheAuthors.PublishedbyElsevierLimitedonbehalfofKingSaudBinAbdulazizUniversityforHealthSciences.Thisisanopenaccessarticleunderthe CCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).

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406 R.Mattaetal./JournalofInfectionandPublicHealth11(2018)405–411

beenrecognizedforoveracenturyasacriticalproblemaffecting thequalityofhealthandaprincipalsourceofadversehealthcare outcomes[4].

Gram-negative bacteria are largely responsible for acquired infections. Multi-drugresistant strainsare increasingly isolated in thesesettings, including carbapenemase-producingKlebsiella pneumoniae,AcinetobacterandPseudomonasaeruginosa[5]. Acine-tobacterbaumannii hasalsobecomeoneof themostsigniﬁcant antibiotic-resistantbacteria causinghospitalacquired infections worldwide [6].One of themain methodsthrough which Gram negative bacteria develop resistance is carrying genes coding for enzymes, such as beta-lactamases, hydrolyzing and inacti-vatingbeta-lactam antibiotics [7],beta-lactams being themost widely used class of antibiotics [8]. A major source of resis-tance in Escherichia coli are plasmid-borne Extended-Spectrum ␤-Lactamases (ESBL], which are classiﬁed as enzymes capable of hydrolyzing most ␤-lactams such as penicillins, extended-spectrum cephalosporins, and monobactams; ESBLs are not inhibitedby␤-lactamaseinhibitorssuchasclavulanicacid, sul-bactam,andtazobactam[9].Basedonthis,community-onsetESBL infectionshavebecomeanimportantpublichealthissue[10].

Furthermore, Staphylococcus aureus gram-positive cocci can withstandharshenvironmentsforextendedperiodsallowing sus-ceptible individuals to become infected through contact with persistentlyortransientlycolonizedpeople[11].Thus,these bac-teria are the most common hospital acquired pathogens with increasedmorbidity[12].Penicillin-resistantstrainsappearedin hospitalizedpatientswithina shorttime aftertheintroduction oftheantibiotic;methicillin,a␤-lactamase-resistantderivativeof penicillin,subdividesthespeciesintosensitiveandresistant sub-groups.Methicillin-resistantS.aureus(MRSA)appearedin1961, oneyearaftermethicillinwasintroducedintoclinicaluse[13].

Toourknowledge,nostudyhaseveridentiﬁedcharacteristics ofbacteriacomparingcommunityandhospitalsettingsinLebanon. Thismulticenterstudywasdesignedtoidentifyandcharacterize thespeciesofdifferentpathogensbetweencommunityacquired andhospitalacquiredinfections,pointingonpatients’related inde-pendentco-morbiditiesandsocio-demographicfactors.

Materialsandmethods Studydesign

Thiswasaretrospectivecohort,multicenterstudyfromﬁve pri-vatehospitalslocatedinBeirutandMountLebanonoveroneyear. Amongthese,threewereuniversityhospitalswhereastwowere non-universityhospital.Thestudydurationwas6months. Populationanddatacollection

Theinclusioncriterionwastheinfectiondiagnosisaccordingto theCentersforDiseaseControl(CDC)criteriainanadultpatient [14].Onlytheﬁrstepisodeofinfectioninthehospitaladmission wascharacterizedforeachpatient.Overall,258adultpatientswere includedfromtheﬁvehospitalsinBeirutandMountLebanon.

Datawere collectedthrough a standardizedsheetof patient identification. The record included patient-specific parameters suchasdemographicdata,underlyingdiseases,andriskfactors. Theinfectionvariablesrecordedpositiveculture,typeofgermsand antibiotictreatmentwithpresenceorabsenceofmulti-resistant bacteria.Hospitalacquiredinfectionswasdefinedasalocalizedor systemicconditionthatresultedfromanadversereactiondueto thepresenceofinfectiousagentswhichoccurred48hormoreafter hospitaladmissionandwasnotincubatingatthetimeof admis-sion.Communityacquiredinfectionsweredefinedasaninfection

detectedwithin48hofhospitaladmittedpatients[15].Agewas classiﬁedaccordingtothecriteriaofAcutePhysiologyandChronic HealthEvaluation(APACHE)score;forthisreason,agewas cate-gorizedintotwosubgroupslessthan44yearsandmorethan44 years.

Microbiologydata

Allparticipatingmedicalcenterswereresponsibleforisolates identiﬁcationandsusceptibilitytesting.Eachlaboratoryperformed susceptibilitytestingaccording totheirown standardized tech-niquesbasedoncurrentNationalCommitteeforClinicalLaboratory standards[16].Datacollectedwereprimarilyqualitative(resistant, intermediateorsusceptible).AllisolatesofE.coliandK.pneumoniae were tested for extended-spectrum beta-lactamase production. S.aureuswastestedformethicillinresistance.P.aeruginosawas testedforitsmultipleresistances.Streptococcuspneumoniaewere testedagainstpenicillinsusceptibility.

Comorbidity

The comorbidity of patients in the study included mainly immunosuppression,administration ofchemotherapy in the12 monthspriortohospitaladmission,radiationtherapy, administra-tionofsteroidsforatleast3monthspriortohospitaladmission, infectionwithhumanimmunodeﬁciencyvirus,chronicliver dis-ease, chronic heart failure, chronic respiratory disease,chronic renalfailure,hematologicaldisease,cancer,anddiabetesmellitus requiringinsulintherapyororalhypoglycemicagentsbeforethe infection.

Dataanalysis

Statisticalevaluationwasconductedthroughbivariateand mul-tivariableriskfactoranalyses,withtheaimofidentifyingselected bacteriaandindependentfactorsassociatedwiththepresenceofa hospitalacquiredinfectioncomparedtopatientswithacommunity acquiredinfection.Datawasenteredandanalyzed,usingStatistical PackageforSocialSciences(SPSS)version22software.Inall anal-ysis,ap-value<0.05wasconsideredsigniﬁcant.TheChi2_test_was usedforcomparingcategoricalvariablesbetweengroups;when expectedvalueswithincellswere<5,Fisherexacttestwasused.A stepwiseforwardlikelihoodratiomultivariablelogisticregressions wasperformedwiththe type ofinfection (communityhospital acquiredversushospitalacquired)asthedependentvariable,and thecharacteristicspresentingthelowestp-valuesinthebivariate analysisastheindependentones.Theﬁnalmodelwasselectedafter ensuringmodelsadequacytodatabyHosmer–Lemeshowtest. Results

Population

258patientswereincludedinthis study.Ofallpatients, 142 (55%)hadahospitalacquiredinfectionand116(45%)community acquired.Almosthalfofthepatients(50.8%)patientswerefrom communityhospitalsand(49.2%)fromuniversityhospitals. Correlationbetweenhospital-acquiredinfectionandclinical information

Bivariateanalysiswasdonetoassesstherelationshipbetween hospital acquired infection and patients’ clinical information. Tachycardiawashigherinpatientswithhospitalacquired infec-tions compared to the community (83.6% vs 64.1% p<0.001). Moreover, these patients had higher prevalence of tachypnea

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Table1

clinicaloutcomeandbacteriallocalizationincommunityandhospitalacquiredinfection.

Communityacquired Hospitalacquired Total P-value

N=142(55%) N=116(45%) N=258 Temperature>38.3◦_C ₇₄_(52.1%) ₇₂_(62.1%) ₁₄₆_(56.69%) _0.091 Tachycardia>90beats/min 91(64.1%) 97(83.6%) 188(72.9%) <0.001 Tachypnea>20breath/min 47(33.1%) 52(44.8%) 99(38.4%) 0.047 Leucocytes>12,000/mm3_/<4000/mm3 ₉₃_(65.5%) ₉₂_(79.3%) ₁₈₅_(71.7%) _0.01 CRP 53(60.2%) 37(86%) 90(34.9%) 0.003 Sepsis 105(73.9%) 115(99.1%) 220(85.3%) <0.001 Severesepsis 56(39.4%) 92(79.3%) 148(57.4%) <0.001 Deﬁnedinfection 69(48.6%) 84(72.4%) 153(59.3%) <0.001

Hospitallengthofstay>14days 44(31.2%) 79(68.1%) 123(48%) <0.001

Bacteriallocalization Communityacquired Hospitalacquired Total P-value

Sputum 25(17.6%) 26(22.4%) 51(19.8%) 0.335

Blood 35(24.6%) 39(33.6%) 74(28.7%) 0.113

Urine 64(45.1%) 60(51.7%) 124(48.1%) 0.287

Ascitesﬂuid 5(3.5%) 7(6%) 12(4.7%) 0.340

Skinandsofttissue 3(2.1%) 5(4.3%) 8(3.1%) 0.256

Catheter 4(2.8%) 14(12.1%) 18(7%) 0.004

Stools 11(7.7%) 16(13.8%) 27(10.5%) 0.114

Bronchoscopyaspiration 4(2.8%) 19(16.4%) 23(8.9%) <0.001

CSF 0 2(1.7%) 2(0.8%) 0.201

(44.8%vs 33.1% p=0.047), leukocytosisor leucopenia (79.3%vs 65.5%p=0.01),highC-reactiveprotein(86%vs50.2% p=0.003). Sepsiswasmoreprevalentinpatientswithhospitalacquired infec-tion(99.1%vs73.9%p<0.001).Themedianofhospitalstaywas14 days;wealsofoundasigniﬁcantdifferencebetweenthetwogroups wherepatientswithhospitalacquiredinfectionshadahigher hos-pitalstayabovethemedian(68.1%vs31.2%p<0.001).

Regardingthecharacteristicsofinfections,wehadaround60%of patientsmicrobiologicallydocumentedinfections;thispercentage wassigniﬁcantlyhigherinpatientswithhospitalversus commu-nityacquiredinfections(72.4%vs48.6%p<0.001).Positiveculture fromthecatheter(12.1%vs2.8%p=0.004)andfrombronchoscopy (16.4%vs2.8%p<0.001)weremorecommoninhospital-acquired comparedtocommunityinfections.

Mostcommonbacterialisolatesfromdifferentspecimentypes Most isolates were obtainedfrom the following specimens: 48.1% fromurine, 28.7%from blood,19.8% fromsputum, 10.5% fromstools, 8.9% frombronchoscopy, 7% from a catheter, 4.7% fromascitesfluid,3.1%fromaskinandsofttissuesand0.8%from cerebrospinalfluid.Withintheurinarytractinfectionandblood cultureisolates,E.coliwasthemostcommonbacteriainhospital acquiredinfection.Forsputum,A.baumannii,Enterobactercloacae, E.coli,K.pneumoniaeandP.aeruginosawerethemostcommon isolates.Clostridiumspecies fromstoolsand E.coliand Candida albicansspecies fromcatheter were mainlyisolated. Amongall typesof differentspecimencollected, bronchoscopy aspirations andcatheterweresignificantlymorecommonlycollectedamong hospitalacquiredinfections (16.4%vs2.8%)and(12.1%vs 2.8%) respectively(Table1).

Descriptivestatisticsoftheinfection

Fifty-eightpointfourpercentoftheinfectionswereduetoone Gramnegativebacteriaatleast,48%duetooneEnterobacteriaceae, 30.7%duetooneanaerobicbacteriaatleastand26.2%duetoone Grampositivebacteriaatleast.Around73%ofpatientshadmore thanoneseveritycriterionand50.8%hadsepsisdiagnosisat48h ormoreafterhospitaladmission.ThemeanICUlengthofstaywas around8days.Itisofnotethat18.2%ofthesepatientsdied.The totalmortalityathospitaldischargewas27.1%(Table2).

Table2

Descriptionoftheinfections.

N (%)

AtleastoneGrampositivebacteria 53 26.2% AtleastoneGramnegativebacteria 118 58.4% Atleastoneenterobacteriaceae 97 48% Atleastoneanaerobicbacteria 62 30.7% Morethanoneseveritycriteria 187 72.5% Interval48hormorebetweenadmissionandsepsis 131 50.8% ICUlengthofstay(indays) 8.245 ±19.6661

ICUmortalitydischarge 47 18.2%

Totalmortalityathospitaldischarge 71 27.5% *ICU=IntensiveCareUnit.

**ICUlengthofstayisexpressedasmean±standarddeviation.

Mostcommonorganismsisolatedimplicatedinhospitalacquired infections

Atotalof221isolatesfromclinicalspecimenswerecollected; 171Gramnegative(77.4%)and50Grampositive(22.6%)isolates weredetected.Amongthem,110(64.3%)oftheGramnegativeand 26(52%)oftheGrampositivepathogenswereimplicatedin hos-pitalacquiredinfections.ThemostcommonGramnegativebacilli includedareE.coli,P.aeruginosa,K.pneumonia,E.cloacaeandA. baumanniithetotalofwhichmadeupto53.5%ofthetotalbacilli isolated.Aﬂow-chartwasdrawntoindicatethemostcommon bac-teriainvolvedinthecommunityandhospitalacquiredinfections, withtheirrespectivepercentages(Fig.1).

AlthoughE.coliwasthemostfrequentisolatedmicroorganism inbothgroups(24.6%inthecommunityvs32.8%inthehospital setting),therewerenosigniﬁcantdifferencesbetween commu-nityandhospitalacquiredinfections.TheGram-negativebacteria thatshowedapositivecorrelationregardingpatient’stypeof infec-tionwereP.aeruginosa(19%versus6.3%)(p=0.002),K.pneumonia (10.3%versus2.8%)(p=0.013)andA.baumannii(6%versus0.7%) (p=0.017);thesegermswerethusmostlyfrequentamongpatients withhospitalacquiredinfections (Table3).Moreover,themost commonGrampositivecocciwereS.aureusandcoagulase neg-ativeStaphylococcus,whichtogetherrepresented13.6%fromcocci isolated.NoneoftheGrampositivebacterialisolatesshoweda sig-niﬁcantrelationshipbetweencommunity andhospitalacquired infections(Table4).

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Table3

Gramnegativeisolatescollectedfrompatientsinhospitalandcommunityacquiredinfections.

N=142(55%) N=116(45%) N=258 Escherichiacoli 35(24.6%) 38(32.8%) 73(28.3%) 0.150 Pseudomonasaeruginosa 9(6.3%) 22(19%) 31(12%) 0.002 Klebsiellapneumoniae 4(2.8%) 12(10.3%) 16(6.2%) 0.013 Enterobactercloacae 3(2.1%) 7(6%) 10(3.9%) 0.104 Acinetobacterbaumanii 1(0.7%) 7(6%) 8(3.1%) 0.017 Proteusmirabilis 2(1.4%) 5(4.3%) 7(2.7%) 0.249 Haemophilusinﬂuenzae 3(2.1%) 3(2.6%) 6(2.3%) 0.559 Klebsiellaoxytoca 1(0.7%) 2(1.7%) 3(1.2%) 0.447 Serratiaspp 1(0.7%) 1(0.9%) 2(0.8%) 0.698 Stenotrophomonasmaltophilia 1(0.7%) 1(0.9%) 2(0.8%) 0.698 Morganellamorganii 0 2(1.7%) 2(0.8%) 0.201 Pseudomonasspp 0 2(1.7%) 2(0.8%) 0.201 Clostridiumspp 0 2(1.7%) 2(0.8%) 0.201 Burkholderiacepacia 0 1(0.9%) 1(0.4%) 0.450 Citrobacterfreundi 0 1(0.9%) 1(0.4%) 0.450 CorynebacteriumJK 0 1(0.9%) 1(0.4%) 0.450 Enterobacterspp 0 1(0.9%) 1(0.4%) 0.450

Haemophiluspara-inﬂuenzae 0 1(0.9%) 1(0.4%) 0.450

Nocardiaspp 0 1(0.9%) 1(0.4%) 0.450

Salmonellaspp 1(0.7%) 0 1(0.4%) 0.550

Fig.1.Flowchartcomparingbacteriaincommunityacquiredandhospital infec-tions.

Isolatesofmulti-resistantbacteria

ThepercentageofMRSAcausinghospitalacquiredinfections is12.9%, compared to2.8%in communityinfections (p=0.001). ESBLproducingE.coliandK.pneumoniaeoccurredin30.2%and 1.7% respectively in hospital acquired infections compared to 13.4% and 0.7% in the community, respectively (p=0.001 and 0.424). P. aeruginosa showed signiﬁcance in its resistance to ﬂuoroquinolones(p<0.001),imipenem(p=0.005),overall multi-resistance(p=0.001)andBetalactams(p=0.041)(Table5).

Factorsassociatedwithhospitalacquiredinfections

Bivariate analysis was done to see if there was a rela-tionshipbetweenhospital-acquired infectionandpatient socio-demographicproﬁleandcomorbidities.Thegenderdistributionof thepatientshavinghospitalacquiredinfectionwas54.2%malesand 41.7%females(p=0.046).Patientswithhospitalacquiredinfection wereolderthanthoseofthecommunityacquiredinfectedpatients inbothagegroups(p=0.003);thesepatientshadhigher preva-lenceofpreviouscomorbiditiesnamelyhematologicmalignancy (12.1% vs 4.9% p=0.037), immunosuppression (24.1% vs 10.6% p=0.004),prioradministrationofsteroids(15.5%vs7.7%p=0.049) andchemotherapy(7.8%vs1.4%).Chronicobstructivepulmonary disease(COPD)waspredominantincommunitypatients(16.4%vs 30.3%p=0.009)(Table6).

Table7summarizestheresultsoftheforwardlikelihood logis-ticregression.Therewasasigniﬁcantrelationshipbetweenolder agegroup(ORa=5.680;CI[2.344;13.765]p<0.001)and immune-suppressedstate (ORa=3.137; CI [1.485;6.630] p=0.003) with hospitalversuscommunityacquiredinfections,whilethere was an inverse relationship for COPD (ORa=0.403 CI [0.212;0.765] p=0.006)(morecommonamongcommunityacquiredinfections).

Discussion

In this study,patientswith hospitalacquired infections had higherratesofP.aeruginosaandmulti-drugresistantP.aeruginosa,K. pneumoniaandESBLproducingK.pneumoniaandE.coli,A. bauman-niiandMRSA.Hematologicmalignancy,immunosuppression,prior administration of steroids and chemotherapy were risk factors

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Table4

Grampositiveisolatescollectedfrompatientsinhospitalandcommunityacquiredinfections.

N=142(55%) N=116(45%) N=258

Staphylococcusaureus 7(4.9%) 12(10.3%) 19(7.4%) 0.098

Staphylococcuscoagulasenegative 7(4.9%) 9(7.8%) 16(6.2%) 0.349

Enterococcusfecalis 3(2.1%) 2(1.7%) 5(1.9%) 0.595

Pneumococcusspp 4(2.8%) 0 4(1.6%) 0.090

Streptococcusagalactiae 1(0.7%) 3(2.6%) 4(1.6%) 0.239

Streptococcuspyogenes 2(1.4%) 0 2(0.8%) 0.302

Table5

Percentageofmultiresistantbacteriainhospitalandcommunityacquiredinfections.

Multiresistantbacteria Communityacquired Hospitalacquired P-value

N=142 N=116

ESBL*gramnegativepathogens 19(13.4%) 35(30.2%) 0.001

KlebsiellaESBL* ₁_(0.7%) ₂_(1.7%) _0.424

MRSA** ₄_(2.8%) ₁₅_(12.9%) _0.002

PseudomonasResistanttoImipenem 5(3.5%) 15(12.9%) 0.005

PseudomonasResistanttoAminoglycosides 3(2.1%) 8(6.9%) 0.058 PseudomonasResistanttoFluoroquinolones 3(2.1%) 17(14.7%) <0.001

PseudomonasResistanttobeta-lactamsotherthanimipenem 4(2.8%) 10(8.6%) 0.041

Multi-ResistantPseudomonas 4(2.8%) 16(13.8%) 0.001

StreptococcusResistanttoPenicillin 0 1(0.9%) 0.105

*_Extended_Spectrum_beta_lactamase. **_Methicillin_resistant_{Staphylococcus}_aureus.

thatshowedapositivecorrelationwithhospitalacquiredinfected patients.

COPD was mainlyinvolved in community infected patients. Theseresultsareinlinewiththoseofotherstudies.Infact,the Mediterranean regionhas beenidentiﬁed asan area of hyper-endemicityformulti-drugresistanthospitalpathogens[17].

Theseresultsarealsosimilartowhatwasfoundinboth Euro-pean[18]andnon-Europeancountries[19];asanexample,MRSA prevalencevariedfromlessthan1%inNorthernEuropeto high-estthan40%inSouthernandWesternEurope[18].Withregardto resistantpathogens,(ESBL)-producingE.coliwasmostfrequently recoveredinhospital acquiredpatientsfollowed bycommunity acquiredinfections[20].Moreover,hospitalacquiredP.aeruginosa weresigniﬁcantlymoreresistantthancommunityacquiredspecies toallantimicrobialdrugsevaluated.Theseresultsareconsistent withtheconceptthat isolatesacquiredinthehospitalare usu-allymoreresistantthanthose acquiredin thecommunity [21], andthemajorityofinfectionscausedbyresistantpathogenswere describedashospitalacquired[22].Thisisinaccordancewithour resultswherecommunity-acquiredorganismsweremore suscep-tibletoantimicrobialdrugstestedthanhospitalacquiredisolates, butstillwefoundaround13%ofESBLresistanceamongE.coliinthe community.Infact,recentdatasuggestthatinfectionscausedby resistantmicroorganismsareanemergingproblemincommunity patients[20].

OurresultsshowedthatStreptococcusinfectionswerenot fre-quentinthecommunitysetting,inopposite topreviousstudies [23,24]thatshowedthat this germwasthemostcommon eti-ological pathogen isolated. This might be due to the fact that currently,S. pyogenesis considered a rarecause of community acquiredpneumonia,beingaclinicalentityseenonlysporadically afteraninﬂuenzainfection[25].Furthermore,theproportionof CAPattributedtoS.pneumoniaeshowedgreatvariationbetween countries,withaverageratesof24%inJapan,14%inSouthKorea andTaiwan,12%inThePhilippines,8–9%inThailand,Chinaand Indiaand4–5%inMalaysiaandSingapore[26].Alackofrigorous microbiologicalstandards,forexample,specimencollection fol-lowingantibioticuse,delaysinspecimentransport,orcultureof specimenswithinadequatemicroscopicscreeningforwhiteblood

cells,mightbeexpectedtoreducetheisolation ofmore fastidi-ousbacteriasuchasS.pneumoniae[27].Wealsohypothesizethat mostoftheantibioticchoicesareprescribedempiricallytopatients becauseofthetimerequiredtoidentifycommunity-acquired res-piratory tractinfections mainlyin peoplewithcriticalﬁnancial conditions,andthetimerequiredtoﬁndtheorganism[28].

Asforassociatedfactors,wefoundsigniﬁcantclinical parame-tersintermofunderlyingdiseasesthatwoulddistinguishhospital fromcommunityacquiredinfections.Similartoourresults,Haley andSchabergidentiﬁedage,sex,underlyingdiseaseand immuno-suppressive therapy as intrinsic factors increasing the risk of infections [29].In anotherstudy,theprincipalfactorsthat con-tributed to the risk of acquiring a hospital acquired infection include immunosuppression[30],extensivesurgicalprocedures [31],ageandgender[32],anduseofprolongedantibiotictherapy [33];however,inourstudy,nodifferenceingenderwasreported. Neoplasticdiseases,suchashematologicmalignanciesandsolid tumors, immune-compromised state [34] were also commonly associated conditionin patientswithhospital acquiredinfected patients.OurresultswerealsosimilartoKangetal.[35].Chronic obstructivepulmonarydiseasehadarelationshipwithcommunity acquiredinfectionsduetoitsexacerbationsthatusuallyrequire hospitalization[36].Thus,inordertoreducefailureofinitial antibi-otic therapyinpatientsfromthecommunity,itis importantto takethesefactorsintoaccountandperformadequateantibiotic empiricalcontrol.

Limitations

Ourstudyhaslimitations.Itwasanobservational,retrospective studyconductedonasmallsamplegroupwithashortduration. Prospectivestudiesinvolvingalargenumberofpatientsfrom dif-ferentinstitutionsandgeographicareasarewarrantedtoconfirm ourfindingsandevaluatetheneedtodevelopspecificguidelinesfor thisnewgroupofpatients.Samplingbiasisdetectedbyconvenient samplingfromselectedhospitalswhereuniversityhospitalsare overrepresented[37];inaddition,theseasonoftheyearmayhave asignificantinfluenceonratesofdiseasesandmultidrugresistant bacteria[38];thishastobetakenintoaccountinfuturestudies.

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Table6

Bivariateanalysisofthepredictivefactorsofhospitalacquiredinfection.

Patients’riskfactors Community acquired142(55%) Hospitalacquired 116(45%) P-value Age <44years 30(21.9%) 107(78.1%) 0.001 >44years 8(7%) 107(93%) Gender Male 65(45.8%) 77(54.2%) 0.046 Female 67(58.3%) 48(41.7%) Obesity No 79(57.7%) 58(42.3%) 0.562 Yes 27(52.9%) 24(41.7%) Hematologicmalignancies No 135(95.1%) 7(4.9%) 0.037 Yes 102(87.9%) 14(12.1%) AIDS No 142(100%) 0 0.450 Yes 115(99.1%) 1(0.9%) Cirrhosis No 139(97.9%) 3(2.1%) 0.473 Yes 111(95.7%) 8(4.3%)

Chronicheartfailure

No 98(69%) 44(31%) 0.365 Yes 86(74.1%) 30(25.9%) Metastaticcancer No 127(89%) 15(10.6%) 0.774 Yes 105(90.5%) 11(9.5%) COPD No 99(69.7%) 43(30.3%) 0.009 Yes 97(83.6%) 19(16.4%) Alcoholism No 139(97.9%) 3(2.1%) 0.183 Yes 110(94.8%) 6(5.2%) Diabetesmellitus No 92(64.8%) 50(35.2%) 0.392 Yes 81(69.8%) 35(30.2%)

Chronicrenalfailure

No 116(81.7%) 26(18.3%) 0.757

Yes 93(80.2%) 23(19.8%)

Osteo-muscularproblem

No 126(88.7%) 16(11.3%) 0.482

Yes 106(91.4%) 10(8.6%) Bonemarrowtransplantation

No 141(99.3%) 1(0.7%) 0.482

Yes 114(98.3%) 2(1.7%)

Immunocompromisedstate

No 127(89.4%) 15(10.6%) 0.004

Yes 88(75.9%) 28(24.1%)

Prioradministrationofprednisone

No 131(92.3%) 11(7.7%) 0.049 Yes 98(8.5%) 18(15.5%) Chemotherapy No 140(98.6%) 2(1.4%) 0.002 Yes 107(92.2%) 9(7.8%) Severemalnutrition No 138(97.2%) 4(2.8%) 0.735 Yes 111(95.7%) 5(4.3%)

Solidorgantransplantation

No 132(93%) 10(7%) 0.746

Yes 109(94%) 7(6%)

Table7

Logisticregressionofpredictorsofhospitalversuscommunityacquiredinfections. Independentvariable ORa 95%CI P-value

Olderageclass 5.680 [2.344;13.765] <0.001 Immuno-compromisedstate 3.137 [1.485;6.630] 0.003

COPD 0.403 [0.212;0.765] 0.006

Overallpercentage:62.7%;Omnibustestsigniﬁcant;HosmerLemeshowP=0.709(Not signiﬁcant).

Variablesinitiallyentered:Ageclass,COPD,immuno-compromisedstate,Hematologic malignancyandradiationorchemotherapy.

Conclusion

Ourresultsconfirmthathospitalacquiredinfectionshavehigher ratesofresistantbacteriawhencomparedtocommunityacquired infections.Microbiologistshavetoplayanimportantroleinthe preventionof hospitalacquiredinfections becausetheyarethe first to detect the patients’ bacteriological flora and their pat-ternof resistance. Physicians shouldalso beaware of patients’ comorbiditiestoproperlyguidetheinitialtherapy,particularlyage, immunosuppression,andCOPD;sinceresistanceisattributedto localepidemiologyanduncontrolleduseofantimicrobialagents, furtherresearchinvolvingalargenumberofpatientsfromdifferent hospitalsareneededinordertoconfirmourfindingsandhighlight theneedforantimicrobialstewardship.

Ethicalapproval

TheLebanese University ethicalcommittee waivedapproval ofthestudysinceitisanobservationalnon-invasivestudythat respects participants’ autonomyand anonymity; thestudy fol-lowedprinciplesoftheDeclarationofHelsinkiforsuchtypesof studies. Conﬂictsofinterest Nonedeclared. Fundingsources Nofundingsources. References

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