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RESEARCH

Adherence to International Antimicrobial Prophylaxis Guidelines in Cardiac Surgery: A Jordanian Study Demonstrates Need for Quality Improvement

Nairooz H. Al-Momany, MSc; Amal G. Al-Bakri, PhD; Zeid M. Makahleh, MD, MRCS; and Mayyada M.B. Wazaify, PhD

ABSTRACT BACKGROUND: Antimicrobial prophylaxis in cardiac surgery has been demonstrated to lower the incidence of surgical site infection (SSI). Inappropriate antimicrobial prophylaxis, such as inappropriate selection of the antimicrobial agent or inappropriate dosing regimen, can increase the prevalence of antibiotic resistant strains, prolong hospital stay, cause adverse reactions, and negatively affect an institution's pharmacy budget for antibiotics. In developing countries such as Jordan, where the role of clinical pharmacists is still in its primary stages, the first step in establishing an organized clinical pharmacy service is the evaluation of current practice to determine the need for improvement. OBJECTIVE: To assess the degree of adherence to international guidelines for antimicrobial prophylaxis practice in cardiac surgery performed at Queen Alia Heart Institute (QAHI) in Amman, Jordan, as part of an attempt to determine opportunities for clinical pharmacist intervention. METHODS: For a total of 236 patients who were admitted for cardiac surgery to QAHI--the only official referral hospital for cardiac patients in Jordan--between November 19, 2006, and January 22, 2007, the antimicrobial prophylaxis indication, choice, duration, dose, dosing interval, and timing appropriateness were assessed against 3 international guidelines using a pre-tested, structured clinical data collection form that was completed by 2 of the authors who work at QAHI. The study design was prospective. All patients who were scheduled for surgery were monitored daily during their inpatient stay until discharge and then were tracked in the outpatient clinic for 2 months following surgery. Data regarding antimicrobial prophylaxis indication, choice, duration, dose, dosing interval, and timing appropriateness were collected during the patient's inpatient stay; data collection was performed periodically thereafter as data became available until the end of the 2-month follow-up. The 3 guidelines agreed that (a) antimicrobial prophylaxis should be given to all patients undergoing cardiac surgeries; (b) the first- or second-generation cephalosporins (cefazolin or cefuroxime) are the antibiotics of choice, and vancomycin use is reserved for cases of allergy to beta-lactams or if presumed or known methicillin-resistant Staphylococcus aureus (MRSA) colonization is present; (c) the timing of the first dose should be within 60 minutes prior to the skin incision; and (d) the duration of antimicrobial prophylaxis should not be longer than 48 hours. RESULTS: Adherence to all antimicrobial prophylaxis guidelines was not achieved for any study patients. For the 6 evaluated criteria, (1) indication: in 100% of patients the appropriate decision was made to use antimicrobial prophylaxis in concordance with guidelines; (2) choice: only 1.7% of patients received the antibiotic of choice; (3) duration: 39.4% of patents received antimicrobial prophylaxis for a total duration of 48 hours or less in concordance with guidelines, and for 58.9% of patients, duration was longer than recommended; (4) dose: 27.9% of patients received an appropriate dose; (5) dosing interval: only 13.0% of patients received an appropriate dosing interval, and none of the doses of antimicrobial prophylaxis used at induction of anesthesia was repeated in operations that lasted longer than the half-life of the antibiotic used; and (6) timing: 99.1% of patients received antimicrobial prophylaxis dose within 60 minutes prior to skin incision as recommended by guidelines, but 97.0% of patients received an unnecessary

midnight dose of intravenous antibiotic the night before surgery. CONCLUSION: Study findings indicate that adherence to international guidelines for antimicrobial prophylaxis is far from optimal in QAHI, leading to the inappropriate administration of many antibiotics. Developing local hospital guidelines, as well as giving the clinical pharmacist a central role in the administration, monitoring, and intervention of antimicrobial prophylaxis may improve the current practice. J Manag Care Pharm. 2009;15(3):262-71 Copyright © 2009, Academy of Managed Care Pharmacy. All rights reserved.

What is already known about this subject

· Several studies worldwide have described adherence to international guidelines in antimicrobial prophylaxis in different countries.Goreckietal.(1999)foundthatin74%of211patients undergoingelectiveoremergencysurgeryinaNewYorkprivate teaching hospital, the antimicrobial prophylaxis administration wasinappropriateaccordingtoSurgicalInfectionSocietyguidelines. Problems included excessive duration (66%), switch to inappropriateantibiotics(32%),spectrum(31%),andtiming(i.e., nopre-operativedose,22%). · Inastudyoftheapplicationofguidelinesonpre-operativeantibioticprophylaxisinLeón,Nicaragua,vanDisseldorpetal.(2006) estimatedthatantibioticchoicewasdiscordantwiththehospital guidelinesin69%ofthecases,dosein20%ofthecases,andboth the timing of administration and duration in 78% of the cases. Overalladherencewasachievedin7%ofpatients.

What this study adds

· Thisstudyrepresentsthefirstattempttoassessthedegreeof adherence to antimicrobial prophylaxis practice standards in cardiacsurgeryperformedintheonlyofficialreferralhospital for cardiac patients in Jordan. This is an important step in developing strategies in Jordan and in other hospitals with similarconditions. · Complete adherence to international antimicrobial prophylaxis guidelines was not achieved for any study patients. The lowest measuredadherencerate(1.7%)wasforantibioticchoice,andthe highest (100%) was for appropriate decision making regarding useornonuseofantimicrobialprophylaxis(indication),followed bytimingofthefirstdoseatafixedtimebeforeincision(99.1%). Adherenceratesintheotherstudiedparameterswere39.4%for total duration of antimicrobial prophylaxis use, 27.9% for dose, and13.0%fordosinginterval. · The study indicates the need for interventions to improve the rationaluseofantibioticprophylaxistopreventthecomplications ofinappropriateadministrationofantimicrobials.

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Adherence to International Antimicrobial Prophylaxis Guidelines in Cardiac Surgery: A Jordanian Study Demonstrates Need for Quality Improvement

lthough cardiac surgery is generally considered a clean procedure,antibioticprophylaxishasbeendemonstrated to lower the incidence of surgical site infection (SSI). SSIs of the sternal wound and underlying mediastinum occur in0.4%-4%ofcardiacsurgicalprocedures,withover50%due tothecoagulase-positiveStaphylococcus aureusorthecoagulasenegative Staphylococcus epidermidis.1 Patients who develop SSIs aftercoronaryarterybypassgraft(CABG)surgeryhaveamortalityrateof22%at1yearcomparedwith0.6%forthosewhodo notdevelopanSSI.2 Practiceguidelinesareintendedtoassistphysiciansandother healthcareprovidersinclinicaldecisionmakingbydescribing a range of generally acceptable approaches for the diagnosis, management, or prevention of specific diseases or conditions.3 Thelastdecadehasseenaproliferationofevidence-basedclinical practice guidelines.4 Antibiotic guidelines and associated interventions have been demonstrated to be effective in improving antibioticuse.5Organizationsthathavepromulgatedguidelines for antimicrobial prophylaxis in cardiac surgery include the National Surgical Infection Prevention Project (NSIPP),6 the SocietyofThoracicSurgeons(STS),1,3 andtheAmericanCollege ofCardiology/AmericanHeartAssociation(ACC/AHA).7 The main recommendations of the 3 guidelines are as follows:(a)antimicrobialprophylaxisshouldbegiventoallpatients undergoingcardiacsurgeries;(b)thefirst-orsecond-generation cephalosporins (cefazolin or cefuroxime) are the antibiotics of choice, and vancomycin use is reserved for cases of allergy to beta-lactams or if presumed or known methicillin-resistant Staphylococcus aureus(MRSA)colonizationispresent;(c)thedurationofantimicrobialprophylaxisuseshouldnotbelongerthan 48hours;and(d)thetimingofthefirstdoseshouldbewithin 60minutespriortotheskinincision(Table1).6,7Thepracticeof giving a midnight (on call) dose of intravenous (IV) antibiotic thenightpriortosurgeryaspartofantimicrobialprophylaxisis inconsistentwithguidelines;moreover,ithasbeenfranklydiscouragedbytheCentersforDiseaseControl(CDC).8 Some countries have incorporated these guidelines into a national drug policy and provided government funding for a rangeofactivitiesaimedatimprovingrationaldruguse.9Health organizationshavebecomeinterestedinsuchpoliciesbecauseof concernsaboutinappropriateantibioticprescribingandreported increase in the prevalence of antibiotic-resistant organisms.10,11 Antibiotic resistance has been described as a major threat to globalpublichealthbytheWorldHealthOrganization(WHO) because there are now few and, in some cases, no antibiotics availabletotreatcertainlifethreateninginfections.12 Despite the availability of these guidelines, recent studies assessing the current practice of prophylaxis throughout the world have shown that inappropriate antibiotic choice, excessive duration of use, and inappropriate timing of antimicrobial drugsremainsaprobleminsurgicalprophylaxis.13-20 InanItalian teachinghospital,Motolaetal.(1998)foundthatthird-generation

A

cephalosporins were the most frequently used antibiotics both in patients undergoing clean (74.1%) and clean-contaminated (73.0%) surgical procedures.15 The resulting costs were about 10-fold higher than estimated costs of antibiotic prophylaxis carried out according to international guidelines.15 In Belgium, Kurzetal.(1993)foundthatantimicrobialprophylaxiswasgiven in57%oftheproceduresforwhichprophylaxisisgenerallynot recommended,wasnotusedin14%ofproceduresforwhichitis generallyrecommendedandin14%ofcontaminatedprocedures, andwasprolongedbymorethan2dayspostoperativelyafter23% oftheproceduresandbymorethan4daysin8%.13InaCanadian survey of antimicrobial prophylaxis use among patients who underwent surgical repair of a fractured hip with insertion of prostheticmaterial,Zoutmanetal.(1999)reportedthat70%of casesdidnotreceiveadoseofantimicrobialprophylaxiswithin 2 hours pre-operatively; instead, antimicrobial prophylaxis was administered either too early or during the procedure. In 39% of cases receiving antibiotic prophylaxis, the first dose was not administereduntiltheendoftheprocedure.Antimicrobialprophylaxisconsistedofaparenteralfirst-generationcephalosporin for94%ofcases.18 Monitoringandinterventioncanbeeffectiveinincreasingthe adherencetoguidelines.Indescriptivestudieslackingacontrol group,stricterimplementationoftheexistingantimicrobialprophylaxisprotocolswasassociatedwithanincreaseintheappropriatenessofantibioticprophylaxisfromapproximately50%to 95%-100%.21,22 InJordaningeneraland,specifically,intheQueenAliaHeart Institute(QAHI),inwhichthepresentstudywasconducted,antimicrobialprophylaxisincardiacsurgeryisnotgovernedeitherby nationalorbylocalguidelines.Thisproblemistypicalofother developingcountries.23,24Studiesthatassessthecurrentclinical practiceofantimicrobialprophylaxisinJordanwerelackinguntil thepresentstudy.Previousresearchinthistopicareafocusedon thepresenceofaclearevidenceofantibioticmisuseamongthe Jordanianpopulation.25-27Inlightofthisabsenceoflocalorinstitutionalantimicrobialprophylaxisguidelines,thepresentstudy used the aforementioned 3 international guidelines--NSIPP, STS,andACC/AHA--toassesstheappropriatenessandcomplianceofantibioticprophylaxispracticesincardiacsurgerywithin QAHI.1,3,6,7 Methods Setting and Study Design PatientsenrolledinthepresentstudywereadmittedtoQAHIfor cardiologyservicesandcardiacsurgery.QAHIistheonlyofficial referral hospital for cardiac patients in Jordan, performing an averageof30cardiacsurgeriesperweek.Eligiblepatientswere enrolledinthestudybetweenNovember19,2006,andJanuary 22,2007.Generally,thestudyevaluatedpractitioneradherenceto antibioticprophylaxisguidelinesusingaclinicaldatacollection form.ThestudywasapprovedbytheCareerEthicsCommittee,

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TABLE 1

Summary of 3 International Guideline Recommendations for Antimicrobial Prophylaxis in Cardiothoracic Surgery

Antibiotic Choice Cefazolin,cefuroxime, orcefamandole Ifthepatienthasa beta-lactamallergy, vancomycinor clindamycin Dose and Route of Administration CefazolinIV:1-2gm(20-30)mgperkg standarddose.If<80kg,use1gm;if>80kg, use2gm.Endstagerenaldiseaset½=40-70 hours. CefuroximeIV:1.5gmstandarddose, 50mg/kgadjusteddose.Endstagerenaldiseaset½=15-22hours. CefamandoleIV:1gmstandarddose. Endstagerenaldiseaset½=12.3-18hours. VancomycinIVinfusion:1gmover60minute standarddose,10-15mgperkg(adult) adjusted.Endstagerenaldiseaset½=44.1406.4hours. ClindamycinIV:600-900mgstandarddose. If<10kg,useatleast37.5mg;if>10kg,use 3-6mg/kg.Endstagerenaldiseaset½=3.5-5.0 hours. CefazolinIV:1gmpre-operative prophylacticdose;forapatient>60kg, 2gmisrecommended. VancomycinIVinfusionover1hour: doseof1-1.5gmoraweight-adjusted doseof15mgperkg. AminoglycosideIV;(usuallygentamicin, 4mgperkg)inadditiontovancomycinprior tocardiacsurgery. Total Duration of AMP Use 24hoursorless Timing of First Dose at Fixed Time Before Incision; Dosing Interval Within60minutesbeforeincision. Forvancomycintheinfusionshould beginwithin120minutesbefore incision. Dosesshouldberepeatedintraoperativelyiftheoperationisstillin progress2half-livesafterthefirst dose.

Guideline Antimicrobial Prophylaxis forSurgery: AnAdvisory Statementfrom theNational SurgicalInfection Prevention Project(NSIPP), 2005a

TheSociety ofThoracic Surgeons (STS)Practice GuidelineSeries: Antibiotic ProphylaxisIn CardiacSurgery, 2006-2007b

Cefazolin Ifpresumedorknown MRSAcolonization, vancomycin(1-2doses) +cefazolin

48hoursorless

Forcefazolin:administration within60minutespriortotheskin incision;seconddoseof1gram shouldbeadministeredevery3-4 hours,iflongprocedure. Forvancomycin:administration slowlyover1hour,withcompletion within1houroftheskinincision. Foraminoglycosides:theinitialdose shouldbeadministeredwithin1 houroftheskinincision. Initialdosetobegiven30-60minutesbeforeskinincision. Vancomycin:30-to60-minute infusiontimedtoendbeforeskin incision.

Inpatientswith beta-lactamallergy, vancomycin(upto48 hours)+aminoglycoside (1pre-operativeand1 post-operativedose). AmericanCollege Cephalosporinclass: cefuroxime(superior ofCardiology/ efficacycomparedwith AmericanHeart theothercephalosporins), Association cefazolinorcefamandol. (ACC/AHA) GuidelineUpdate Vancomycin:reservedfor forCoronary penicillin-allergicand ArteryBypass justifiedinperiodsof c Surgery,2004 MRSAoutbreaks.

Cefuroxime:1.5gmpre-operatively, 1.5gmaftercardiopulmonarybypass, 1.5gmevery12hours. Cefamandole,cefazolin:1gmpre-operatively, 1gmatsternotomy,1gmafter cardiopulmonarybypass,1gmevery6hours. Vancomycin:1gmevery12hoursuntillines/ tubesareout.Atleast2doses.

48hoursorless

a Bratzler

bEngleman

DW, Houck PM. Am J Surg. 2005;189(4):395-404.6 et al. Ann Thoracic Surg. 2007;83(4):1569-76;1 Edwards et al. Ann Thoracic Surg. 2006;81(1):397-404.3 cEagle et al. J Am Coll Cardiol. 2004;44(5):e213-310.7 AMP = antimicrobial prophylaxis; gm = gram; IV = intravenous; kg = kilogram; mg = milligram; MRSA = methicillin-resistant Staphylococcus aureus; t½ = elimination half-life.

theequivalentofaninstitutionalreviewboardinJordan,inthe SSIbeforetheendofthefollowupperiodwerenotincludedin RoyalMedicalServices. thedataanalysis.Patientswereenrolledinthestudyifinformed consentwasobtainedfromthepatientorhis/herrepresentative. Patients Patientsscheduledforanytypeofcardiacsurgerywereeligiblefor Data Collection thestudywithafewexceptions.Patientsdiagnosedwithhuman Datawerecollectedfrompatients'verbalself-reports,files,mediimmunodeficiency virus (HIV) infection, tuberculosis, or cystic cation sheets, and prescriptions using a clinical data collection fibrosiswereexcludedfromthestudy.Toavoiddifficultiesindis- form(summarizedinTable2).Theformhadbeenpre-testedona criminatingprolongedprophylaxisfrompost-operativetherapy, smallpilotscale(n 0)andsubsequentlymodifiedtoensurethat =1 patients with suspected or established infection during surgery thedatawouldprovidevalidinformation.Theentireclinicaldata werealsoexcluded.Patientswhodiedduetoacauseotherthan collectionformisavailablefromtheauthorsuponrequest.

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FIGURE 1

Patient Selection Flow Chart

Patients scheduled for all types of cardiac surgery (n = 264)

Surgery was not performed or postponed (n = 12): · Patientswithriseinwhitebloodcellcountandsuspectedinfection(n=9) · Patientswhodidnotcometothehospital(n=3) Excluded (n = 11): Tuberculosis(n=1) Cysticfibrosis(n=2) Pneumonia(n=4) Suspectedinfection(notsurgicalsiteinfection) that required the use of antibiotics (n = 4)

Patients underwent cardiac surgery (n = 252) · · · · Total number of patients included in the study (n = 241)

Lost to follow up: Died within or after surgery due to a cause other than surgical site infection (n = 5)

Data available for analysis for (n = 236) patients

Allpartsoftheformwerecompletedby2oftheauthors(NM, a clinical pharmacist and ZM, a cardiac surgeon) who work at QAHI.Allpatientswhowerescheduledforsurgeryweremonitoreddailyduringtheirinpatientstayuntildischargeandthen trackedintheoutpatientclinicfor2monthsfollowingsurgery. Data regarding antimicrobial use in the hospital were collected duringthepatient'sinpatientstay;additionaldatacollectionwas performedperiodicallythereafterasdatabecameavailable,until theendofthe2-monthfollow-upperiod. Analysis of Prophylactic Antibiotic Use The compliance of current prophylactic antibiotic practices in cardiac surgery at QAHI with 3 published international guidelines was assessed. These guidelines were from the NSIPP (Antimicrobialprophylaxisforsurgery:anadvisorystatement),6 theSTS(Antibioticprophylaxisincardiacsurgery,partI:duration, and part II: antibiotic choice),1,3 and the ACC/AHA (2004 guidelineupdateforcoronaryarterybypassgraftsurgery).7The following6aspectsofantimicrobialprophylaxiswereassessed: (1) indication--appropriate decision making regarding use or nonuseofantimicrobialprophylaxis;(2)choice--antibioticchoice forpatientswithandwithoutallergy;(3)total durationofuse;(4) dose;(5)dosing interval--includesbothrepeatingofdosesinprocedureswithdurationslongerthanthehalf-lifeoftheantibiotic used,andintervalbetweendoses;and6)timing ofdosegivenata fixedtimebeforeincision(within60minutespriortoskinincision).Thecriteriaforevaluationofadherencearesummarizedin Table3. Ifmorethan1drugwasprescribedforasingleprocedure,all parameterswereevaluatedseparatelyforeachdrug.Finalassessmentoftheantibioticcoursewascomposedbycombiningthese

TABLE 2

Summary of Clinical Data Collection Form

Part A Demographic data:patient'sname,identificationnumber,gender, age,weight,dateofadmission,dateofdischarge. Medical data:diagnosisandtypeofsurgery,pastmedicalhistory, drughistory,drugallergy,antibioticuseinthelast2weeks, previoushospitalizationinthelast2years. Prophylactic antibiotic(s) used:tradeandscientificname,dose, frequency,timingofdoses,routeofadministration,durationofuse, andnumberofdosesofallantibioticsused(pre-,intra-,andpostoperatively)assurgicalprophylacticantibiotics. Duration of the surgery in minutes

Part B

separatedrugevaluations.Anydivergencefromtheguidelinesin theprescriptionof1ofthedrugsledtoafinalassessmentofthe prophylacticcourseasdiscordantwiththeguidelines.Ifnoantibioticordersorprescriptionshadbeenrecorded,itwasassumed thatantibioticswerenotgiven.Ifdataonacertainparameterof the antibiotic prescription were lacking, the case was classified asmissingdataonthisparameteronly.Wedefinedanantibiotic administeredthedaybeforesurgery(e.g.,inamidnightdosethe nightbeforesurgery)asnotindicated,andfortheseevents,the parameters of antibiotic choice, duration, dose, dosing interval, andtimingwerenotevaluatedforthatnonindicateddrug;however,ifthesamepatientreceivedanantibioticonthedayofthe surgery, all parameters were evaluated for that drug because it wasindicated. All data were coded, entered, and analyzed using SPSS for Windows,version14.0(SPSSInc.,Chicago,IL).Frequencyand percentageswerecalculatedandpresented.

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TABLE 3

Criteria to Assess Adherence and Compliance With Current Antimicrobial Prophylaxis Practices Within QAHI Compared With International Guidelinesa

Concordant if ·Decisionwasmadetouseantimicrobialprophylaxis. ·Agentrecommendedbyguidelines. ·Combinationusedonlywhenindicated. ·Noswitchtoanotherantibioticintheabsenceofmicrobiologicorclinicalindication. Durationasrecommendedbyguidelines(48hoursorless). Doseasrecommendedbyguidelines.Forpediatricpatients,dosescalculatedaccordingtobody weightusingDrug Information Handbook.b Additionaldosewasgiveninsurgicalprocedurelongerthanthehalf-lifeoftheprophylactic antibioticused,anddosingintervaldidnotexceedtheguidelinebymorethan30minutes.

Parameter 1. Antibioticindication 2.Antibioticchoice

3.Totaldurationofprophylacticantimicrobialuse 4. Dose 5. Dosinginterval (a)duringsurgery

(b)ontheward Dosingintervaldidnotdeviatefromtheguidelinebymorethan60minutes. Timingofdosedidnotdeviatebymorethan15minutesfromtherecommendedtime 6.Timing Timingofdosegivenatfixedtimebeforeincision. (within30-60minutespriortoskinincision). a Guidelines used: National Surgical Infection Prevention Project;6 The Society of Thoracic Surgeons;1,3 and American College of Cardiology/American Heart Association.7 bLacy et al. Drug Information Handbook, 2006.41 QAHI = Queen Alia Heart Institute.

Results Between November 19, 2006, and January 22, 2007, 252 cardiacsurgerieswereconductedinQAHI.Aftertheapplicationof inclusion and exclusion criteria, 236 patients were enrolled in thestudy(Figure1).Patients'characteristicsandtypesofcardiac surgeriesarepresentedinTable4. Overall Assessment of All Parameters Adherence to guidelines in antimicrobial prophylaxis for all parameters was not fulfilled in any of the 236 cardiac surgeries assessed in this study. Two common deviations from the guidelines were observed: (a) the unexplained switch from an appropriateorinappropriateagent(s)toaninappropriateagent(s) inthesamepatientin230(97.5%)patients;and(b)thepracticeof givingamidnightdoseofIVantibioticthenightpriortosurgery aspartofantimicrobialprophylaxisin229(97.0%)patients. Assessment of Individual Parameters Parameterswerealsoevaluatedseparately,sothatnonadherence to1parameterdidnotprecludeassessmentoftheothers.Rates of adherence to international guidelines for indication, choice, total duration, dose, dosing interval, and timing are presented inTable5. Indication: In concordance with the guidelines, antimicrobial prophylaxis was given for all of the 236 (100%) patients who underwentcardiacsurgeries(Table5).However,amidnightdose of IV antibiotic on the night before surgery was given to 229 (97.0%) of patients (third-generation cephalosporin in 85% of patients,second-generationin10%,otherantibioticsin2%).As thisantibioticdosewasgivenwhilenotindicated,andbecause

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the midnight antibiotic might have differed from the antibiotic that was given later at induction of anesthesia, the parameters of antibiotic choice, dose, dosing interval and timing were not evaluatedforthedruggivenatmidnight;however,theseparameterswereevaluatedforanyantibioticsgiventothepatientonthe surgerydate. Antibiotic Choice: Overall, antibiotic choice was concordant with guidelines for only 4 (1.7%) patients (Table 5), almost entirely because of post-operative treatment decisions. In the operating room and during induction of anesthesia, the antibioticchoice(cefuroxime)wasconcordantwithguidelinesin226 (95.8%)patientsanddiscordantin10patients.Thereasonsfor discordancewerethefollowing: · Suspicion of beta-lactam allergy in 5 patients where cefuroximewasgiven. · Use of a vancomycin and cefuroxime combination in 3 patients who did not have either beta-lactam allergy or presumedcolonizationwithMRSA. · Missinginduction-antimicrobialprophylaxisdosein2patients towhomathird-generationcephalosporinwasgiven8hours aftertheendoftheoperation. Aftersurgery,fornearlyallpatients,therewasanunexplained switchfromanappropriateorinappropriateagent(s)toaninappropriate agent(s). Switches were made from a second-generation cephalosporin cefuroxime (or combination of cefuroxime with vancomycin) to (a) a combination of a third-generation cephalosporin with 1 of these antibiotics: vancomycin, amikacin, flucloxacillin, or imipenem in 145 (61.4%) patients; (b) a combination of vancomycin with amikacin or flucloxacillin or imipenem in 34 (14.4%) patients; (c) a third-generation

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cephalosporin alone in 32 (13.6%) patients; or (d) vancomycin alone in 19 (8.1%) patients. Cefuroxime was maintained as a singleprophylacticantibioticinonly4(1.7%)patients,andthe third-generationcephalosporinceftriaxonewasmaintainedasa singleprophylacticantibioticinonly2(0.8%)patients. Total Duration of Antimicrobial Prophylaxis Use: In 93 of 236 patients (39.4%), total duration of all agents used as antimicrobial prophylaxis was concordant with the guidelines (48 hoursorless).In139(58.9%)patients,durationwaslongerthan recommended.In4cases(1.7%),durationcouldnotbeevaluated becausemedicationchartswereincomplete. Dose: Only doses of antibiotics used in concordance with the guidelines were evaluated. The dose was concordant with the guidelines in only 63 (27.9%) of 226 evaluated doses. In all of the163(72.1%)discordantdoses,thedosewaslowerthanwhat isrecommended,eitherbecause(a)alowerdose(e.g.,750milligramsinsteadof1.5grams)wasgiventoanadultpatient;(b) no dose adjustment was made for an obese patient; or (c) the doseperkilogramcalculatedforachildwaslowerthanrecommended.

TABLE 4

Characteristics and Types of Cardiac Surgeries for Patients Enrolled in the Study

N = 236 43[25.7](0.1-73) 78.0%(184)

Characteristic Mean[SD](range)ageinyears Male%(n) PatientWeight a

Underweight(BMI18.5) 3.4% (8) Normalweight(BMI=18.5-24.9) 44.9%(106) Overweight(BMI=25-29.9) 33.9% (80) Obese(BMI30) 17.8% (42) Mean[SD](range)lengthofhospitalstaybeforesurgery 3.4[4.0](1-13) indays Mean[SD](range)totallengthofhospitalstaybeforeand 22.6[2.3](9-41) aftersurgeryindays Hospitalizationinthepast2years%(n) 15.6% (37) Diabetesmellitus%(n) 35.2% (83) Currentsmoking%(n) 25.0% (59) 33.5% (79) 3medicaldiagnosesormoreb%(n) Steroidsintakebeforeandwithinhospitalization%(n) 40.2% (95) Type of Cardiac Surgery Congenitalheartsurgery%(n) Valvereplacementsurgery%(n) Coronaryarterybypasssurgery%(n) Othersurgeriesc%(n) Meandurationofsurgery[SD](range)inhours Antibiotic Use 30.1% (71) 11.4% (27) 55.1%(130) 3.4% (8) 3.2[1.4](2.2-6.5)

Dosing Interval: Only dosing intervals of agents used in concordance with the guidelines were evaluated (n 30, Table 5). =2 Ofthese,onlythedosingintervalofantibioticsrepeatedduring Withinhospitalization%(n) 100%(236) 11.4% (27) surgeryorinthewardcouldbecalculated.Ofthe226dosesof Within2weeksbeforehospitalization%(n) antimicrobialprophylaxisusedatinductionofanesthesia,none a BMI (Body Mass Index) = weight in kilograms divided by height in squared meters 41 was repeated, even though antimicrobial prophylaxis should (Lacy et al. Drug Information Handbook, 2006). b Only chronic diseases that are present in patient's history or diagnosed in the curhavebeenrepeatedin196surgeriesbecausethedurationofthe rent admission were counted (e.g,. diabetes mellitus, hypertension, ischemic heart surgery was longer than the half-life of the antibiotic used. In diseases). the4patientsforwhomcefuroximewasmaintainedasasingle cThe other surgeries were correction of aortic coarctation, excision of left atrial prophylacticantibioticinthewardaftersurgery(incompliance myxoma, carotid endarterectomy, and repair of aortic dissection. withtheguidelines),thedosingintervalwasdiscordantwiththe guidelines(every8hoursinsteadofevery12hours).Thus,only 30(13.0%)outof230evaluatedagentdosingintervalswerecon- farfromoptimal.Oneofthemoststrikingfindingsofthisstudy cordantwiththeguidelines. was that no patient's care adhered to all guideline parameters. WhilethisresultisconsistentwiththoseofsimilarstudiesinIran Timing of Doses Given on the Surgery Date:Fordosesgiven and Nicaragua, where rates of complete adherence to practice on the day of the surgery, timing was concordant with the guidelineswere0.3%24and7%,28respectively,higherpercentages guidelines(atinductionofanesthesiawithin30minutesbefore ofadherencetoantimicrobialprophylaxisguidelineshavebeen incision)in224of226(99.1%)oftheevaluatedcardiacsurgeries. For the 2 surgeries in which antimicrobial prophylaxis timing reportedinotherstudies.Goreckietal.(1999,UnitedStates),van wasdiscordantwiththeguidelines,noantimicrobialprophylaxis Kasterenetal.(2003,theNetherlands),Lallemandetal.(2002, wasgiveninthehourspriortoorduringthesurgery;instead,a France),andVoitetal.(2005,UnitedStates)foundintheirstudthird-generationcephalosporinwasgiven8hoursaftertheend iesthatoveralladherencewasachievedin26%,28%,41.1%,and approximately50%ofsurgicalpatients,respectively.17,29-31 oftheoperation. Interestingly, although the present study reported lower adherence to all parameters than did earlier studies, the rate Discussion of adherence to timing of antimicrobial prophylaxis at a fixed Adherence in Current Practice The present study demonstrates that adherence to the interna- time before incision (99.1%) is higher than that reported in tionalguidelinesforantimicrobialprophylaxisisdisappointingly most other studies. Paradiso-Hardy et al. (2002), Lallemand

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TABLE 5

Adherence to International Guidelines in Antimicrobial Prophylaxis in Cardiac Surgery

Number (%) Meeting Criteria (Concordant With any of A,B,C) (n = 236) 236 (100.0)

International Guidelinea A=NSIPP2005 B=STS2006-2007 C=ACC/AHA2004 AnyantimicrobialprophylaxisrecommendedbyA,B,C AnyrecommendeddurationbyA,B,C AnyrecommendeddosebyA,B,C.Forpediatricdoses calculatedaccordingtobodyweightc AnyrecommendeddosingintervalbyA,B,C AnyrecommendedappropriatetimingoffirstdosebyA,B,C AnyoftheguidelinesA,B,C

a NSIPP = National

Recommendation Criteria 1. Appropriatedecisionmakingregardinguseof antimicrobialprophylaxis(indication)

2.Appropriateantibioticchoice 3.Appropriatetotaldurationofantimicrobialprophylaxisuse 4. Appropriatedose 5. Appropriatedosinginterval 6.Appropriatetimingoffirstdoseatfixedtime(within30-60 minutesbeforeincision) Appropriatecompliancewithallrecommendations Surgeons;1,3

4 (1.7) 93 (39.4) 63 (27.9)b 30 (13.0)d 224 (99.1)e 0 (0.0)

Surgical Infection Prevention STS = The Society of Thoracic Association.7 bNumber evaluated = 226. cWeight calculated according to Lacy et al. Drug Information Handbook, 2006.41 d Number evaluated = 230. eNumber evaluated = 226.

Project;6

ACC/AHA = American College of Cardiology/American Heart

etal.(2002),vanKasterenetal.(2003),andvanDisseldorpet al.(2006)reportedintheirstudiesthattimingofthefirstdose wasconcordantwithguidelinesin72%,61.4%,50%,and22% ofcases,respectively.28-30,32 Itisnoteworthythatadherenceinallofthepreviouslymentioned studies, except ours and that of Askarian et al. (2006, Iran),wascomparedwithlocal,ratherthaninternational,guidelines.Thehigheradherenceratesinstudiesthatusedlocalguidelines (7%-50%) as opposed to studies that used international guidelines because of lack of national or local guidelines (0%0.3%),suggestthatadherencetolocalguidelinesmaybeeasierto achievethanadherencetointernationalguidelines.17,24,28-31 One potential strategy to improve antimicrobial practice in hospitals is standardization, either by adopting an international guideline or by developing a local hospital guideline. Standardizationeffortsshouldbeoverseenbyacommitteethat includes surgeons, anesthesiologists, microbiologists, pharmacists,andmembersofhospitalepidemiologyandinfectioncontroldepartments.Guidelinesshouldbebasedonhospital-specific bacterial epidemiology patterns, the best literature evidence, andsurgeonpreference.Standardizedprotocolsshouldthenbe provided to surgeons, in an effort to achieve consensus, before implementation. The present study revealed several areas for improvement at thestudyhospital.AtQAHI,theon-callsurgeon(usuallyajunior surgeon) routinely prescribes a midnight antimicrobial prophylaxisdosethenightbeforesurgeryandrecordsitonthefollow-up sheet in the patient's file. The anesthesiologist gives the intraoperative antibiotic dose and records it only on the anesthesia chart.Aftersurgery,theconsultant,orseniorsurgeon,prescribes

268 Journal of Managed Care Pharmacy

post-operative antimicrobial doses and records them on the follow-upsheetinthepatient'sfile.Theabsenceofastandardized antimicrobialpracticeguidelinecreatesalackofcommunication betweenanesthesiologists,surgeons,andevenamongthemembersofthesurgicalteam.Thislackofcommunicationproduced poormonitoring,resultingin2maindeviationsthatledto100% nonadherenceinthisstudy.Thesedeviationsfromtheguidelines areasfollows: (a)Unexplained switch to inappropriate antibiotic(s) without microbiological or clinical indication. The most common antimicrobial prophylaxisagentsusedinthisstudywereacombinationofa third-generationcephalosporinwithanotherantibiotic(vancomycin,amikacin,flucloxacillin,orimipenem);acombination of vancomycin with amikacin. flucloxacillin, or imipenem; or a third-generation cephalosporin alone. Third-generation cephalosporinsandbroadspectrumcombinationsshouldnot be used for SSI prophylaxis because they have less activity againstStaphylococcithandoescefazolin.Suchuseinducesthe emergenceofresistantorganismsandismorecostly.14,33 (b)Giving a midnight dose of IV antibiotic the night prior to surgery. Thispracticeshouldbestronglydiscouragedingroupeducation andconsensus meetings. One method ofpreventing thispracticeistoassigntheprescriptionofantimicrobialsto theanesthesiologistinchargeonly.Preventioncouldalsobe achievedbyprovidingbetterstafftrainingastothebenefits ofadherencetostandardinternationalantimicrobialprophylaxis guidelines and the risks of unnecessarily dispensing antibiotics.

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Potential solutions to avoid both of these mistakes include better organization of work and specification of tasks among individuals on the surgical team, introduction of special forms fororderingantimicrobialprophylaxis,anduseofanantibiotic prophylaxischartintheoperatingtheaters.Anothersuggestion istogiveacentralroletotheclinicalpharmacistsinantimicrobialprophylaxisadministration.Inadescriptivestudywithouta controlgroup,Pradoetal.(2002)showedthatwhenpharmacists weregivenacentralroleintheadministrationofprophylaxis,the appropriatenessoftheindicationincreasedfrom56%to100%, whilethecostsdecreasedby40%.21Moreover,inastudyofan intervention to reduce the prescribing of antibiotics for upper respiratoryinfectionsbygeneralpractitionersinAustralia,Zwar etal.(2002)foundthatgivingfeedbackonprescriptionbehavior increasedtheappropriatenessoftheprescriptions.34 Thepresentstudyalsodemonstratedthat,althoughadherence toallguidelineswasnotachievedforanystudypatients,adherencewasbetterforsomespecificguidelinesthanforothers.For example, the decision to use antimicrobial prophylaxis (indication)andthetimingofantimicrobialprophylaxisbeforeincision showedhighratesofadherence(100.0%and99.1%,respectively), indicatingthatthesurgicalteamswereawareoftheimportance ofgivingantimicrobialprophylaxiswithin30-60minutesprior toskinincisiontopreventSSIincardiacsurgeries.Theimportanceofthetimelyadministrationofpre-operativeantibioticsis well established and is broadly applicable to all procedures for which prophylactic antibiotics are administered.1 It has been suggestedthatantimicrobialselectionisamootpointiftheagent is not delivered during the optimal 30-60 minute window just beforeincisionandthatthebeneficialeffectisnegatedifthedrug isgivenafterincision.7Investigationofthereasonsforadherence totimingguidelinesrevealedthatanesthesiologistswereresponsible for giving the intra-operative antimicrobial prophylaxis doses, providing further support for the suggestion to improve adherence by specifying tasks and distributing responsibilities amongmembersofthesurgicalteam. Useofantibioticsforlongerthantherecommendedperiod, especially in the absence of any evidence of secondary infectionorSSIuntilthedayofdischargeinanattempttoprevent infection while patients were hospitalized, was observed in 58%ofourstudypatientsandhasalsobeenreportedbysome otherresearchers.24,35-36Prolongedantibioticprophylaxisis,at best,ofnobenefitand,atworst,potentiallyharmfultopatients because of drug toxicity, the risk of super-infection, and the risk of inducing more bacterial resistance, both in surgical

patientsandthroughoutthehospital.37-39 Dosesanddosingintervalswerediscordantin72%and88% of patients, respectively. That is, no dose adjustment was done whenitwasneededanddoseswerenotrepeatedintra-operatively inlong-durationprocedures.Thesefindingsareconsistentwith the work of Gupta et al. (2003), who found that prophylactic antibioticadministrationinprocedureslastingmorethan4hours wasrepeatedinonly9patients(3%)in300casesatthecorrect timefortheentiredurationofthesurgeryincompletecompliance withthepublishedguidelines.40 Limitations First, the exact timing of the intra-operative antimicrobial prophylaxisdosewasassessedbasedontheanesthesiologists'notes ontheanesthesiachart,anditwasrecordedalwaysatinduction. However, we cannot guarantee the accuracy of recorded notes. Inthefuture,onecouldconsideramethodtorecordthetimeof doseadministrationmoreprecisely.Second,althoughanecdotal informationsuggeststhatmosthospitalsinJordansharesimilar standards, our results may not be entirely applicable to other countries.However,ourresultscanbegeneralizedtohospitalsin otherdevelopingcountries,wherenotmuchattentionispaidto internationalpracticeguidelines.Additionally,previousresearch has documented widespread nonadherence to antimicrobial practice guidelines in many countries, including the United StatesandCanada.17,18,31 Conclusion Wefoundthatadherencetointernationalantimicrobialprophylaxis guidelines for cardiac surgery is far from optimal in the QAHI, which led to the inappropriate administration of many antibiotics.Thispatternunnecessarilyincreasesexpendituresand likelyplaysamajorroleinthegrowingprevalenceofantibioticresistant microbial strains. Strategies such as the development of local hospital guidelines may improve current antimicrobial prophylaxispracticeinQAHIspecificallyandinotherhospitals ingeneral.Thereisaneedtoincreaseadherencetoclinicalguidelinesforantimicrobialprophylaxisincardiacsurgerypatientsin QAHI,andotherresearchhasshownqualityimprovementusing clinicalpharmacistsinacentralroleintheadministration,monitoring,andinterventionofantimicrobialprophylaxis.Additional effortshouldalsobedirectedtowardsincreasingtheawareness ofpractitionersaboutthedangersofinappropriateuseofantimicrobialsbefore,during,andaftersurgeries.

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Adherence to International Antimicrobial Prophylaxis Guidelines in Cardiac Surgery: A Jordanian Study Demonstrates Need for Quality Improvement

Authors

NAIROOZ H. AL-MOMANY, MSc, is Clinical Pharmacist in charge of the inpatient pharmacy, King Hussein Medical Center, Amman, Jordan; AMAL G. AL-BAKRI, PhD, is Associate Professor of Pharmaceutical Microbiology, Faculty of Pharmacy, The University of Jordan, Amman, Jordan; ZEID M. MAKAHLEH, MD, MRCS, is Specialist Cardiac Surgeon, Queen Alia Heart Institute, Amman, Jordan; and MAYYADA M.B. WAZAIFY, PhD, is Assistant Professor of Pharmacy Practice, Faculty of Pharmacy, The University of Jordan, Amman, Jordan. AUTHOR CORRESPONDENCE: Mayyada M.B. Wazaify, PhD, Faculty of Pharmacy, University of Jordan, Amman, Amman 11942, Jordan. Tel.: 009626-5355000, ext. 23354; E-mail: [email protected]

8.MangramAJ,HoranTC,PearsonML,SilverLC,JarvisWR.Guidelinefor preventionofsurgicalsiteinfection,1999.CentersforDiseaseControland Prevention(CDC)HospitalInfectionControlPracticesAdvisoryCommittee. Am J Infect Control.1999;27(2):97-132. 9.CommonwealthofAustralia,TheDepartmentofCommunications, InformationTechnologyandtheArts. The National Strategy for Quality Use of Medicines.Canberra,Australia:CommonwealthofAustralia;2002,pp.1-36. 10.YangY-H,FuS-G,PengH,etal.AbuseofantibioticsinChinaandits potentialinterferenceindeterminingtheetiologyofpediatricbacterialdiseases.Pediatr Infect Dis J.1993;12(12):986-88. 11.LiH,LiX,ZengX.Astudyonantibioticabusein750childrenwith acuterespiratoryinfectioninTongxianCountyofBeijing.Zhonghua Yu Fang Yi Xue Za Zhi [Chinese Journal of Preventive Medicine]. 1995;29(6):331-34. 12.WorldHealthOrganization(WHO).Antimicrobialresistance:thefacts. Essential Drugs Monitor.2000;28and29:8-9.Availableat:http://mednet2. who.int/edmonitor/edition/EDM2829en.pdf.AccessedFebruary24,2009. 13.KurzX,MertensR,RonveauxO.Antimicrobialprophylaxisinsurgeryin Belgianhospitals:roomforimprovement.Eur J Surg.1996;162(1):15-21. 14.SilverA,EichornA,KralJ,etal.Timelinessanduseofantibioticprophylaxisinselectedinpatientsurgicalprocedures.TheAntibioticProphylaxis StudyGroup.Am J Surg.1996;171(6):548-52. 15.MotolaG,RussoF,MangrellaM,VaccaC,MazzeoF,RossiF.Antibiotic prophylaxisforsurgicalprocedures:asurveyfromanItalianuniversityhospital. J Chemother.1998;10(5):375-80. 16.SasseA,MertensR,SionJP,etal.SurgicalprophylaxisinBelgian hospitals:estimateofcostsandpotentialsavings.J Antimicrob Chemother. 1998;41(2):267-72. 17.GoreckiP,ScheinM,RucinskiJC,WiseL.Antibioticadministrationin patientsundergoingcommonsurgicalproceduresinacommunityteaching hospital:thechaoscontinues.World J Surg.1999;23(5):429-32. 18.ZoutmanD,ChauL,WattersonJ,MackenzieT,DjurfeldtM.ACanadian surveyofprophylacticantibioticuseamonghip-fracturepatients.Infect Control Hosp Epidemiol.1999;20(11):752-55. 19.BurkeJP.Maximizingappropriateantibioticprophylaxisforsurgicalpatients:anupdatefromLDSHospital,SaltLakeCity.Clin Infect Dis. 2001;33(Suppl2):S78-S83. 20.TalonD,MoureyF,TouratierS,etal.Evaluationofcurrentpracticesin surgicalantimicrobialprophylaxisbeforeandafterimplementationoflocal guidelines.J Hosp Infect.2001;49(3):193­98. 21.PradoMA,LimaMP,GomesIR,Bergsten-MendesG.Theimplementationofasurgicalantibioticprophylaxisprogram:thepivotalcontributionof thehospitalpharmacy.Am J Infect Control.2002;30(1):49-56. 22.AleranyC,CampanyD,MonterdeJ,SemeraroC.Impactoflocalguidelinesandanintegrateddispensingsystemonantibioticprophylaxisquality inasurgicalcentre.J Hosp Infect.2005;60(2):111-17. 23.al-HarbiM.Antimicrobialprophylacticpracticeinsurgicalpatients.East Afr Med J.1998;75(12):703-07. 24.AskarianM,MoravvejiAR,MirkhaniH,NamaziS,WeedH.Adherence toAmericanSocietyofHealth-SystemPharmacistssurgicalantibioticprophylaxisguidelinesinIran.Infect Control Hosp Epidemiol.2006;27(8):876-78. 25.OtoomS,BatiehaA,HadidiH,HasanM,Al-SaudiK.Evaluationofdrug useinJordanusingWHOprescribingindicators.East Mediterr Health J. 2002;8(4-5):537-43. 26.Al-BakriAG,BustanjiY,YousefAM.CommunityconsumptionofantibacterialdrugswithintheJordanianpopulation:sources,patternsand appropriateness.Int J Antimicrob Agents.2005;26(5):389-95. 27.OtoomSA,SequeiraRP.Healthcareproviders'perceptionsoftheproblemsandcausesofirrationaluseofdrugsintwoMiddleEastcountries.Int J Clin Pract.2006;60(5):565-70.

DISCLOSURE AND ACKNOWLEDGEMENTS This study was funded by the Deanship of Academic Research at The UniversityofJordan. Allauthorscontributedequallytoconceptanddesign,datacollectionand interpretation,andwritingandrevisionofthemanuscript. Theauthorswouldliketothankallthephysiciansandnursesworkingat QueenAliaHeartInstitute(QAHI)whohelpedusinpatientrecruitmentand datacollection.

REFERENCES 1.EngelmanR,ShahianD,SheminR,etal.;WorkforceonEvidenceBasedMedicine,SocietyofThoracicSurgeons.TheSocietyofThoracic Surgeonspracticeguidelineseries:antibioticprophylaxisincardiac surgery,partII:antibioticchoice.Ann Thorac Surg.2007;83(4):156976.Availableat:http://www.sts.org/documents/pdf/guidelines/ AntibioticProphylaxisCardiacSurgeryPart_IIAntibiotic_Choice.pdf. AccessedFebruary24,2009. 2.HollenbeakCS,MurphyDM,KoenigS,WoodwardRS,DunaganWC, FraserVJ.Theclinicalandeconomicimpactofdeepchestsurgicalinfections followingcoronaryarterybypassgraftsurgery.Chest.2000;118(2):397-402. 3.EdwardsFH,EngelmanRM,HouckP,ShahianDM,BridgesCR;The SocietyofThoracicSurgeons.TheSocietyofThoracicSurgeonspractice guidelineseries:antibioticprophylaxisincardiacsurgery,partI:duration. Ann Thorac Surg.2006;81(1):397-404.Availableat:http://www.sts.org/documents/pdf/guidelines/AntibioticProphylaxisinCardiacSurgeryPartIDuration. pdf.AccessedDecember20,2008. 4.SilagyCA,WellerDP,LapsleyH,MiddletonP,Shelby-JamesT,FazekasB. Theeffectivenessoflocaladaptationofnationallyproducedclinicalpractice guidelines.Fam Pract.2002;19(3):223-30. 5.HarveyK,DartnellJ,HemmingM.Improvingantibioticuse:25yearsof antibioticguidelinesandrelatedinitiatives.Commun Dis Intell.2003;(Suppl 27):S9­S12. 6.BratzlerDW,HouckPM;SurgicalInfectionPreventionGuidelineWriters Workgroup.Antimicrobialprophylaxisforsurgery:anadvisorystatementfromtheNationalSurgicalInfectionPreventionProject.Am J Surg. 2005;189(4):395-404. 7.EagleKA,GuytonRA,DavidoffR,etal.ACC/AHA2004guidelineupdate forcoronaryarterybypassgraftsurgery:areportoftheAmericanCollegeof Cardiology/AmericanHeartAssociationTaskForceonPracticeGuidelines (CommitteetoUpdatethe1999GuidelinesforCoronaryArteryBypass GraftSurgery).J Am Coll Cardiol.2004;44(5):e213-310.

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28vanDisseldorpJ,SlingenbergEJ,MatuteA,DelgadoE,HakE, HoepelmanIM.ApplicationofguidelinesonpreoperativeantibioticprophylaxisinLeon,Nicaragua.Neth J Med.2006;64(11):411-16. 29.LallemandS,ThouverezM,BaillyP,BertrandX,TalonD.Nonobservanceofguidelinesforsurgicalantimicrobialprophylaxisandsurgicalsiteinfections.Pharm World Sci.2002;24(3):95-99. 30.vanKasterenME,KullbergBJ,deBoerAS,Mintjes-deGrootJ,Gyssens IC.Adherencetolocalhospitalguidelinesforsurgicalantimicrobialprophylaxis:amulticentreauditinDutchhospitals.J Antimicrob Chemother. 2003;51(6):1389-96. 31.VoitSB,ToddJK,NelsonB,NyquistAC.Electronicsurveillance systemformonitoringsurgicalantimicrobialprophylaxis.Pediatrics. 2005;116(6):1317-22. 32.Paradiso-HardyFL,CornishP,PharandC,FremesSE.Anationalsurvey ofantimicrobialprophylaxisinadultcardiacsurgeryacrossCanada.Can J Infect Dis.2002;13(1):21-27. 33.MartinC,PourriatJL.Qualityofperioperativeantibioticadministration byFrenchanaesthetists.J Hosp Infect.1998;40(1):47-53. 34.ZwarN,HendersonJ,BrittH,McGeechanK,YeoG.Influencingantibioticprescribingbyprescriberfeedbackandmanagementguidelines:a 5-yearfollow-up.Fam Pract.2002;19(1):12-17.

35.ThomasM,GovilS,MosesBV,JosephA.Monitoringofantibioticusein aprimaryandtertiarycarehospital.J Clin Epidemiol.1996;49(2):251-54. 36.HuS,LiuX,PengY.AssessmentofantibioticprescriptioninhospitalisedpatientsataChineseuniversityhospital.J Infect.2003;46(3):161-63. 37.HeineckI,FerreiraMB,SchenkelEP.Prescribingpracticeforantibiotic prophylaxisfor3commonlyperformedsurgeriesinateachinghospitalin Brazil.Am J Infect Control.1999;27(3):296-300. 38.MartelliA,MattioliF.Aretrospectivestudyshowingthemisuseofprophylacticantibioticsinpatientsundergoingappendectomyandcholecystectomy.Curr Ther Res Clin Exp.2000;61:534-39. 39.HarbarthS,SamoreMH,LichtenbergD,CarmeliY.Prolongedantibiotic prophylaxisaftercardiovascularsurgeryanditseffectonsurgicalsiteinfectionsandantimicrobialresistance.Circulation.2000;101(25):2916-21. 40.GuptaN,Kaul-GuptaR,CarstensMM,FrangaD,MartindaleRG. Analyzingprophylacticantibioticadministrationinprocedureslasting morethanfourhours:arepublishedguidelinesbeingfollowed?Am Surg. 2003;69(8):669-73(discussion673-74). 41.LacyCF,ArmstrongLL,GoldmanMP,LanceLL.Drug Information Handbook 2006-2007.15thed.Washington,D.C.:TheAmerican PharmaceuticalAssociation;2006.

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