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Understanding physician antibiotic prescribing

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International journal of antimicrobial agents · November 2012

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InternationalJournalofAntimicrobialAgents41 (2013) 203–212

ContentslistsavailableatSciVerseScienceDirect

International

Journal

of

Antimicrobial

Agents

j o ur na l ho me p ag e :ht t p : / / w w w . e l s e v i e r . c o m / l o c a t e / i j a n t i m i c a g

Review

Understanding

physician

antibiotic

prescribing

behaviour:

a

systematic

review

of

qualitative

studies

António

Teixeira

Rodrigues

a,b,∗

_,

_Fátima

_Roque

a,c,d

_,

_Amílcar

_Falcão

b,e

_,

Adolfo

Figueiras

f,g

_,

_Maria

_Teresa

_Herdeiro

a,h,i

a_Centre_for_Cell_Biology,_University_of_Aveiro_(CBC/UA),_Aveiro,_Portugal

b_Faculty_of_Pharmacy,_University_of_Coimbra,_Pólo_das_Ciências_da_Saúde,_Coimbra,_Portugal c_Research_Unit_for_Inland_Development,_Polytechnic_Institute_of_Guarda,_Guarda,_Portugal d_University_of_Beira_Interior_(UBI),_Covilhã,_Portugal

e_Centre_for_Neuroscience_and_Cell_Biology,_University_of_Coimbra_(CNC/UC),_Coimbra,_Portugal f_Universidade_de_Santiago_de_Compostela,_Santiago_de_Compostela,_Spain

g_Consortium_for_Biomedical_Research_in_Epidemiology_&_Public_Health_(CIBER_en_{Epidemiología}_y_Salud_{Pública–CIBERESP),}_Spain h_Centre_for_Health_Technology_&_Information_Systems_Research_{(CINTESIS/FMUP),}_Portugal

i_Health_Technology_Research_Centre_{(CITS/CESPU),}_Portugal

a

r

t

i

c

l

e

i

n

f

o

Keywords: Antimicrobialresistance Antibiotic Physician Attitude Qualitative

a

b

s

t

r

a

c

t

Inappropriateprescriptionhasbeenassociatedwithmountingratesofantibioticresistanceworldwide, demandingmore detailedstudiesintophysicians’decision-makingprocess.Accordingly,this study soughttoexplorephysicians’perceptionsoffactorsinfluencingantibioticprescribing.Asystematicsearch wasperformedforqualitativestudiesfocusedonunderstandingphysicians’perceptionsofthefactors, attitudesandknowledgeinfluencingantibioticprescription.Ofthetotalof35papersselectedforreview purposes,18solelyincludedphysiciansandtheremaining17alsoincludedpatientsand/orother health-careproviders.Datacollectionwasbasedmainlyoninterviews,followedbyquestionnairesandfocus groups,andthemethodologiesmainlyusedfordataanalysisweregroundedtheoryandthematic analy-sis.Factorscitedbyphysiciansashavinganimpactonantibioticprescribingweregroupedintothosethat wereintrinsic(group1)andthosethatwereextrinsic(group2)tothehealthcareprofessional.Amongthe former,physicians’attitudes,suchascomplacencyorfear,wereratedasbeingmostinfluentialon antibi-oticprescribing,whilstpatient-relatedfactors(e.g.signsandsymptoms)orhealthcaresystem-related factors(e.g.timepressureandpolicies/guidelinesimplemented)werethemostcommonlyreported extrinsicfactors.Thesefindingsrevealedthat:(i)antibioticprescribingisacomplexprocessinfluenced byfactorsaffectingalltheactorsinvolved,includingphysicians,otherhealthcareproviders,healthcare system,patientsandthegeneralpublic;and(ii)suchfactorsaremutuallydependent.Hence,byshedding newlightontheprocess,thesefindingswillhopefullycontributetogeneratingnewandmoreeffective strategiesforimprovingantibioticprescribingandallayingglobalconcernaboutantibioticresistance.

1. Introduction

Concernsraised aboutantibioticresistancehave highlighted thisﬁeldasanimportantpublichealthproblemcallingforprompt countermeasures. According to the World Health Organization (WHO),infectionscausedbymicroorganismsoftenfailtorespond toconventional therapy, increasinghealth costs,morbidity and mortality,andthreateningareturntothepre-antibioticera[1].In

∗ Correspondingauthor.Presentaddress:CentrodeBiologiaCelular,Universidade deAveiro,CampusdeSantiago,3810-193Aveiro,Portugal.Tel.:+351234370213; fax:+351234401597.

E-mailaddress:[email protected](A.TeixeiraRodrigues).

Europe,widevariationsinresistancestatusarefounddepending onthepathogentype,antimicrobialsubstanceandgeographical region,withunimpeded growthrates beingobserved for some resistantstrains[2–4].

Currently,therearefewdoubtsabouttheassociationbetween theuseofantibioticsandthespreadofantibioticresistance,with misprescriptionof antibioticsbeing oneof themajorfavouring factors [5–7]. As key stakeholdersin the field, physicians have beenthetargetof numerousinterventionsaimedataddressing thefactorsunderlyingthemisprescriptionofantibioticsand, ulti-mately,improvingthequalityofsuchprescribing[8,9].Exploring andunderstandingthefactorsspecifictoeachsettingisthefirst andmostimportantsteptowardsdesigningeffectiveinterventions

[10].

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Insofaraspublishedreviewsseektoevaluatetheinfluenceon antibioticprescribingoftheaspectsidentified,theyhave neverthe-lessnotattemptedtoexploreandidentifythesubjectiveopinions heldbyphysiciansorthetypeofprescriber-relatedattitudesand knowledgethatcouldnotbeidentifiedbyresearchersapriori[11]. Thisisthemainobjectiveofqualitativestudiesandcouldprove extremelyusefulintermsofimprovingknowledgeinthisfield.

Qualitative methods are becoming increasingly prevalent in medicaland relatedresearch[12],andseveralqualitative stud-ieshaveinvestigatedthefactorsinvolvedinantibioticprescribing. Areviewofsuchqualitativeliteratureisfundamentaltogaining insightintothecultureofantibioticprescribing,andthisreview thereforesetouttoexploreandidentifyphysicians’perceptionsof factors,attitudesandknowledgeinﬂuencingantibioticprescribing.

2. Materialsandmethods

2.1. Searchstrategy/searchmethodsforidentiﬁcationofstudies

Forthepurposeofthissystematicbibliographicreview, MED-LINEPubMedscientiﬁcdatabasewassearchedfromJanuary1987 toDecember2011usingthefollowingbroad-basedsearchterm strategy:(attitud*ORknowle*ORpercept*)AND(physician*OR doctor*ORpractitioner*)AND(antibioticORantimicrobial*).The selectioncriteriarequiredpaperstobepublishedinEnglish, Por-tugueseorSpanish,withthoseinotherlanguagesbeingexcluded fromthereview.

2.2. Studycontentinclusion

Studiesweredeemedeligiblefor reviewiftheymetthe fol-lowing criteria:(i) they had tostate expressly that their main objectivewastoexploreand identifyphysicians’perceptions of factorsinﬂuencingantibioticprescribing;(ii)theyhadtouse qual-itativemethodologyasamethodofaffordingadditionalwaysof exploringreal-lifebehaviour,byenablingparticipantstospeakfor themselves[13];and(iii)theyhadtoincludewhateverinfectious diseasewasinvolved.Inthecaseofstudiesincludingboth quan-titativeandqualitativemethodology,onlyqualitativedatawere collected.Likewise,wherethestudypopulationincluded health-careprofessionalsotherthanphysiciansorothersubpopulations, dataweresolelyextractedfromphysicians.

Allpapersselectedwerereviewedbytwooftheauthors(ATR and FR) who decided whether or not these met the selection criteria.Inanycaseofdisagreement,thepaperin questionwas examinedbytheauthorsMTHandAFi,whotooktheﬁnaldecision.

2.3. Qualityinclusioncriteria

Toassessthequalityofthepapersselectedforinclusion,the CriticalAppraisalSkillsProgramme(CASP)qualityassessmenttool wasused[14].Thistoolcontainstwoscreeningandeightdetailed questionsthatdealverybroadlywithsomeoftheprinciplesor assumptionsthatcharacterisequalitativeresearch.

2.4. Dataextraction

Foreachstudyincludedinthereview,atablewasdrawnup(see

Table1)withthefollowingparameters:author;yearofpublication; setting;studypopulation;workplace;samplesize;methodof anal-ysis;disease/clinicalcondition;patienttype/characteristics; and datacollectionmethod.BasedontheCASP[14],Table1alsoshows theidentiﬁcationnumberofthequestionscorrectlyansweredin eachstudy.

Inaddition,theintrinsicandextrinsicfactorsreportedbyeach studyashavingornothavinganinﬂuenceonantibioticprescribing

wereextractedandrespectivelylistedintwotablesaccordingto physicians’perceptions.

Withregardtointrinsicfactorsperceivedbyphysiciansasbeing important to antibiotic prescribing, a second table was drawn up(Table2)showing‘sociodemographicfactors’,‘physicians’ atti-tudes’and ‘others’(the ‘desirefora quickfix’expressedbythe physician,anddiagnosticuncertainty).Sociodemographicfactors includedsex,medicalspecialisation,previousclinicalexperience, yearsofpractice,universityeducationandcontinuousmedical edu-cation.Sixdifferentattitudeswereidentifiedinthestudiesselected, andtheirdefinition,exceptinthecaseofconfidence,wasbasedon thefollowingpre-defineddescription[11]:

• complacency:attitudethatmotivatestheprescribingof antibi-oticstofulﬁlprofessionals’perceptionsoftheirpatients’/parents’ expectations;

• fear:attituderelatingtofearofpossiblefuturecomplicationsin thepatientand/orfearoflosingpatients;

• ignorance: lack of relationship between overprescribing and antibioticresistance,linkedtolackofknowledge;

• indifference:lackofmotivationtofeelpositivelyornegatively inclinedtotheproblemofantibioticprescribing;

• responsibility of others: attitude underlying the belief that responsibilityforgeneratingantibioticresistanceslieswithother professionals;and

• confidence:termthatseekstodescribetheself-reliancefeltby physicians whenprescribingantibiotics. Thisattitudemaybe definedasthelevelofconfidencefeltbyphysicianswhen decid-ing whetheror not to prescribe any given therapy including antibiotics, on the basis of the maxim ‘never change a win-ningpractice’.Examplesofsentencesextracteddirectlyfromthe papersinclude:(i)“Neverchangeawinningteam”wasquotedby severalresidentsandspecialists(Schoutenetal.[15]);and(ii)the negativeattitudeonthesingle-doseregimenthereforeresulted fromnoconfidenceinitseffectiveness(Liabsuetrakuletal.[16]).

Extrinsicfactorsreportedbyphysiciansashavinganinfluence onantibioticprescribingarelistedinTable3andincluded patient-related factors (age, other clinicalconditions, symptoms, signs, anxiety,economicandsocialfactors,educationallevelandexpress desire for a quick fix), healthcare system-related factors (pres-sureoftime,ownershipofpracticelocation,communicationand organisationalmodel,accreditationlevelofpracticesetting,and policies/guidelinesimplemented)andothers(influenceof pharma-ceuticalcompanies,costssavingandfinancialincentives).

Allfactorsdirectlycitedinthestudiesselectedwereexamined andextractedand,owingtothequalitativenatureofallpapers,the transcribedinterviews/consultationsusedtocollectsubjective fac-torsnotidentiﬁedbytheauthorswerealsoassessed.Paperswere analysedandthedataextractedbytworesearchers(ATRandFR) actingindependently,withtheresultsoftheirrespectiveanalyses thenbeingcompared;incasesofdoubt,athirdauthor(MTH)took theﬁnaldecision.

3. Results

3.1. Searchresults

Thesearch strategy identified a total of 1032studies inthe MEDLINEPubMed scientific database.Following screening, 223 paperswereretrievedandassessedaseligibleforperusalofthe fulltext, resultingin a final total of35 studies includedinthe review (Fig. 1) [15–49]. Of these, 26 exclusively used qualita-tivemethodology[15,17,19–24,27–31,33,35–39,41–46,49]and9

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A. Teixeira Rodrigues et al. / International Journal of Antimicrobial Agents 41 (2013) 203– 212 205 Table1

Methodologicalcharacteristicsofthe35studiesselected.

Author(year) Settinga _SPb _WPc _SSd _MAe _P/CCf _TPg _MDCh _CASP

Screening questions

Detailed questions

Paredesetal.(1996)[17] PE P,PA PC 40 Di Pe I 1,2 4,5,6,7,9,10

PalmerandBauchner(1997)[18] USA P,PA PC 61 Pe Q 1,2 3,4,5,7,8,9,10

Bardenetal.(1998)[19] USA P,PA PC 22 TA Pe FGD 1,2 3,4,5,8,9,10

Butleretal.(1998)[20] UK P,PA PC 21 GT RTI A,Pe I 1,2 3,4,5,6,7,8,9,10

Hastyetal.(1999)[21] USA P,PA HC 17 Emergencies Q 1,2 5,7,8,9,10

Coenenetal.(2000)[22] BE P PC,HC 24 Contentanalysis RTI A FGD 1,2 3,4,5,6,8,9,10

Walkeretal.(2000)[23] USA P,Oh HC 22 TAandcontent

analysis

UTI Institutionalised

EP

FGD 1,2 3,4,5,7,8,9,10

BjörnsdóttirandHansen(2001)[24] IS P PC 10+28C TA I+RC 1,2 3,4,5,8,9,10

Palucketal.(2001)[25] CA P PC 392 RTI Pe Q 1,2 4,5,7,8,9,10

Liabsuetrakuletal.(2002)[26] TH P HC 50 Ethnography Caesarean

section

Pregnant women

I 1,2 4,5,6,7,8,9,10

Kumaretal.(2003)[27] UK P PC 40 GT RTI I 1,2 3,4,5,6,8,9,10

Liabsuetrakuletal.(2003)[16] TH P HC 50 Ethnography Caesarean

section

Pregnant women

I 1,2 3,4,5,7,8,9

Altineretal.(2004)[28] DE P PC 42C RTI A,no

co-morbidities

RC 1,2 3,4,5,8,9,10

Moletal.(2004)[29] NL P HC 12 GT I 1,2 3,4,5,8,9,10

Sivagnanametal.(2004)[30] IN P PC,HC 285 Q 1,2 4,5,8,9,10

Weissetal.(2004)[31] UK P,PA,Oh PC,HC 181 RTI Q 1,2 4,5,6,7,8,9,10

Midthunetal.(2005)[32] USA P,Oh PC 181 UTI EP Q 1,2 3,5,8,9,10

Zaffanietal.(2005)[33] IT P,PA PC 276 RTI Pe Q 1,2 4,5,6,8,9,10

Mangione-Smithetal.(2006)[34] USA P,PA PC 522C RTI Pe RC 1,2 3,4,5,7,8,9

Tanetal.(2006)[35] CA P,Oh HC 23 GTandTA SSI Surgical

patients

I 1,2 3,4,5,6,8,9,10

Gouldetal.(2007)[36] UK P,PA PC 54 Q 1,2 4,5,8,9,10

Ongetal.(2007)[37] USA P,PA HC 54 RTI Emergencies I 1,2 4,5,6,7,8,9,10

Schoutenetal.(2007)[15] NL P,Oh HC 17 TA RTI I 1,2 3,4,5,6,8,9,10

Simpsonetal.(2007)[38] UK P PC 40 GT I 1,2 3,4,5,6,8,9,10

Woodetal.(2007)[39] UK P PC 40 GT I 1,2 3,4,5,6,7,8,9

Moroetal.(2009)[40] IT P PC,HC 633 RTI Pe Q 1,2 3,4,5,7,8,9,10

ReynoldsandMcKee(2009)[41] CN P,PA,Oh,Ot PC,HC 11 GT RTI,Di I 1,2 4,5,7,9,10

Bjorkmanetal.(2010)[42] SE P HC 20 PA I 1,2 3,4,5,7,8,9,10

Björnsdóttiretal.(2010)[43] IS P PC 8 GT I+RC 1,2 4,5,7,8,9

Kotwanietal.(2010)[44] IN P PC 36 GT FGD 1,2 3,5,9,10

Sahooetal.(2010)[45] IN P,Oh PC 8 Contentanalysis I 1,2 3,4,5,7,8,9,10

Bjorkmanetal.(2011)[46] SE P PC 20 PA Infectious

disease

I 1,2 3,4,5,7,8,9,10

Kuehleinetal.(2011)[47] DE P PC 23 TA FGD 1,2 3,4,5,6,8,9

Ongetal.(2011)[48] USA P,PA HC 260C Uncomplicated

lacerations

Emergencies I 1,2 3,4,5,6,7,8,9,10

Vazquez-Lagoetal.(2011)[49] ES P PC 33 FGD 1,2 3,4,5,6,7,8,9,10

CASP,CriticalAppraisalSkillsProgramme.

a_Setting:_PE,_Peru;_BE,_Belgium;_IS,_Iceland;_CA,_Canada;_TH,_Thailand;_DE,_Germany;_NL,_Netherlands;_IN,_India;_IT,_Italy;_CN,_China;_SE,_Sweden;_ES,_Spain. b _Study_population:_P,_physicians;_PA,_patients_and/or_their_caregivers;_Oh,_other_healthcare_providers;_Ot,_others.

c _Workplace:_PC,_primary_care;_HC,_hospital_care. d _Sample_size:_C,_{consultations.}

e_Methodology_of_analysis:_TA,_thematic_analysis;_GT,_grounded_theory;_PA,_{phenomenographic}_analysis.

f _{Pathology/clinical}_condition:_Di,_diarrhoea;_RTI,_respiratory_tract_infection;_UTI,_urinary_tract_infection;_SSI,_{surgical-site}_infection. g_Type_of_patient:_Pe,_paediatric;_A,_adult;_EP,_elderly_persons.

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Table2

Descriptionofintrinsicfactorsidentiﬁedasinﬂuencingantibioticprescribing.

Author(year) Sociodemographicfactors Attitudesa _Others

Paredesetal.(1996)[17] Previousclinicalpractice; Yearsofpractice

Ignorance;Fear;Conﬁdence Diagnosticuncertainty PalmerandBauchner(1997)[18] Complacency;Fear

Bardenetal.(1998)[19] Indifference;Complacency;Fear; Responsibilityofothers

Desireforaquickﬁxexpressedbythe physician

Butleretal.(1998)[20] Ignorance;Indifference;Complacency;Fear; Responsibilityofothers;Conﬁdence

Diagnosticuncertainty Hastyetal.(1999)[21]

Coenenetal.(2000)[22] Complacency;Fear Diagnosticuncertainty

Walkeretal.(2000)[23] Ignorance Diagnosticuncertainty

BjörnsdóttirandHansen(2001)[24] Complacency;Conﬁdence Diagnosticuncertainty Palucketal.(2001)[25] Previousclinicalpractice;

Continuousmedicaleducation

Complacency Diagnosticuncertainty Liabsuetrakuletal.(2002)[26] Previousclinicalpractice Indifference;Complacency;Fear;Conﬁdence

Kumaretal.(2003)[27] Previousclinicalpractice; Continuousmedicaleducation

Ignorance;Complacency;Fear;Confidence Desireforaquickfixexpressedbythe physician;Diagnosticuncertainty Liabsuetrakuletal.(2003)[16] Continuousmedicaleducation Indifference;Fear;Confidence

Altineretal.(2004)[28] Complacency Desireforaquickﬁxexpressedbythe physician

Moletal.(2004)[29] Yearsofpractice Ignorance;Indifference Sivagnanametal.(2004)[30]

Weissetal.(2004)[31] Complacency

Midthunetal.(2005)[32]

Zaffanietal.(2005)[33] Complacency Desireforaquickﬁxexpressedbythe physician

Mangione-Smithetal.(2006)[34] Complacency

Tanetal.(2006)[35] Indifference;Responsibilityofothers Gouldetal.(2007)[36] Previousclinicalpractice Indifference

Ongetal.(2007)[37] Complacency;Fear

Schoutenetal.(2007)[15] Previousclinicalpractice Ignorance;Conﬁdence

Simpsonetal.(2007)[38] Universityeducation Ignorance;Indifference,Complacency;Fear

Woodetal.(2007)[39] Previousclinicalpractice Complacency;Fear Desireforaquickﬁxexpressedbythe physician;Diagnosticuncertainty

Moroetal.(2009)[40] Complacency;Fear Diagnosticuncertainty

ReynoldsandMcKee(2009)[41] Ignorance;Complacency Diagnosticuncertainty

Bjorkmanetal.(2010)[42] Ignorance;Fear Desireforaquickﬁxexpressedbythe physician;Diagnosticuncertainty Björnsdóttiretal.(2010)[43] Previousclinicalpractice Ignorance;Fear Desireforaquickﬁxexpressedbythe

physician;Diagnosticuncertainty Kotwanietal.(2010)[44] Complacency;Fear;Responsibilityofothers Diagnosticuncertainty Sahooetal.(2010)[45] Responsibilityofothers

Bjorkmanetal.(2011)[46] Complacency Desireforaquickﬁxexpressedbythe physician

Kuehleinetal.(2011)[47] Previousclinicalpractice; Universityeducation

Conﬁdence

Ongetal.(2011)[48] Complacency Diagnosticuncertainty

Vazquez-Lagoetal.(2011)[49] Ignorance;Indifference;Complacency;Fear; Responsibilityofothers

Diagnosticuncertainty

a_Attitudes_identified_and_their_definition:_Ignorance,_lack_of_relationship_between_{overprescribing}_and_antibiotic_resistance,_linked_to_lack_of_knowledge;_Fear,_attitude relatingtofearofpossiblefuturecomplicationsinthepatientand/orfearoflosingpatients;Confidence,termthatseekstodescribetheself-reliancefeltbyphysicians whenprescribingantibiotics;Complacency,attitudethatmotivatestheprescribingofantibioticstofulfilprofessionals’perceptionsoftheirpatients’/parents’expectations; Indifference,lackofmotivationtofeelpositivelyornegativelyinclinedtotheproblemofantibioticprescribing;andResponsibilityofothers,attitudeunderlyingthebelief thatresponsibilityforgeneratingantibioticresistanceslieswithotherprofessionals.

usedqualitativeandquantitativemethodology(mixedmethods)

[16,18,25,26,32,34,40,47,48].

3.2. Qualityassessment

AsshowninTable1,allthestudiesselectedfulﬁlledthe require-mentsof thescreeningquestions.However,themajorityofthe papersdidnotcoverallofthedetailedquestions.Yetsincethe mostimportantfactorsweregenerallyreported,all35paperswere includedinthisreview.

3.3. Characteristicsofselectedstudies

Thegeneralcharacteristicsoftheselectedstudiesare summa-risedinTable1.

The study setting was primary care in 20 cases

[17–20,24,25,27,28,32–34,36,38,39,43–47,49], hospital care in

10 cases [15,16,21,23,26,29,35,37,42,48] and both primary and hospitalcarein5cases[22,30,31,40,41].

The studies were drawn from ﬁve different continents, although mainly from Europe (n=18) [15,20,22,24,27–29, 31,33,36,38–40,42,43,46,47,49] and North America (n=10)

[18,19,21,23,25,32,34,35,37,48].

Studypopulations includedphysicians, patientsand/or their caregivers and other healthcare providers. Eighteen studies focusedsolelyonphysicians[16,22,24–30,38–40,42–44,46,47,49]

and ten also included patients and/or their caregivers

[17–21,33,34,36,37,48].Furthermore,fourpapers studied physi-cians and other healthcare providers (nurses in two instances

[23,32],perioperativestaffinone[35]andpharmacistsinanother

[15]).Sahooetal.[45]alsoincludedphysiciansandother health-care providers, i.e. veterinarians and drug dispensers. In the case of the remaining two papers, one included physicians, nurses and patients [31] and the other included physicians,

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A.TeixeiraRodriguesetal./InternationalJournalofAntimicrobialAgents41 (2013) 203–212 207

Table3

Descriptionofextrinsicfactorsidentiﬁedasinﬂuencingantibioticprescribing.

Author(year) Patient-relatedfactors Healthcaresystem-relatedfactors Others

Paredesetal.(1996)[17] Ownershipofpracticelocation Financialincentives;

Pharmaceuticalcompanies PalmerandBauchner(1997)[18] Pressureoftime

Bardenetal.(1998)[19] Signs;Desireforaquickﬁxexpressed bythepatient/caregivers

Implementedpolicies/guidelines;Inﬂuenceof groupexposures

Pharmaceuticalcompanies Butleretal.(1998)[20] Signs;Anxiety Pressureoftime

Hastyetal.(1999)[21] Otherclinicalconditions

Coenenetal.(2000)[22] Symptoms;Signs Pressureoftime

Walkeretal.(2000)[23] Patientage;Symptoms;Signs Communicationandorganisationalmodel BjörnsdóttirandHansen(2001)[24] Otherclinicalconditions;Symptoms;

Signs;Economicandsocialfactors

Pressureoftime Costsaving Palucketal.(2001)[25] Communicationandorganisationalmodel;

Implementedpolicies/guidelines

Costsaving Liabsuetrakuletal.(2002)[26] Signs;Economicandsocialfactors Accreditationlevel Costsaving Kumaretal.(2003)[27] Symptoms;Signs;Educationallevel;

Economicandsocialfactors

Pressureoftime;Implemented policies/guidelines

Liabsuetrakuletal.(2003)[16] Communicationandorganisationalmodel; Implementedpolicies/guidelines

Costsaving Altineretal.(2004)[28] Signs;Desireforaquickﬁxexpressed

bythepatient/caregivers

Moletal.(2004)[29] Implementedpolicies/guidelines Sivagnanametal.(2004)[30] Signs Pressureoftime;Inexistenceoffacilitiesto

promotediagnostictests

Costsaving Weissetal.(2004)[31]

Midthunetal.(2005)[32] Otherclinicalconditions

Zaffanietal.(2005)[33] Patientage;Anxiety;Educationallevel

Mangione-Smithetal.(2006)[34] Communicationandorganisationalmodel Tanetal.(2006)[35] Communicationandorganisationalmodel;

Workﬂow Gouldetal.(2007)[36]

Ongetal.(2007)[37] Signs Schoutenetal.(2007)[15]

Simpsonetal.(2007)[38] Publichealthconsiderations Woodetal.(2007)[39] Patientage;Otherclinicalconditions;

Signs

Implementedpolicies/guidelines Costsaving

Moroetal.(2009)[40] Financialincentives

ReynoldsandMcKee(2009)[41] Costsaving

Bjorkmanetal.(2010)[42] Pressureoftime

Björnsdóttiretal.(2010)[43] Symptoms;Signs;Economicandsocial factors;Desireforaquickﬁxexpressed bythepatient/caregivers

Pressureoftime Costsaving

Kotwanietal.(2010)[44] Desireforaquickﬁxexpressedbythe patient/caregivers

Pressureoftime;Ownershipofpractice location;Usethesameprescriptionseveral times

Costsaving;Pharmaceutical companies

Sahooetal.(2010)[45] Pressureoftime

Bjorkmanetal.(2011)[46] Pressureoftime

Kuehleinetal.(2011)[47]

Ongetal.(2011)[48] Signs Patienthealthinsurance Costsaving Vazquez-Lagoetal.(2011)[49] Signs Implementedpolicies/guidelines

patients and other key informers as the study population

[41].

Medicalspecialtiesweredescribedin25oftheselectedarticles. Theauthorscollecteddataexclusivelyfromgeneralpractitioners (GPs)in12studies[20,24,27,28,31,36,38,39,43,46,47,49]andfrom paediatriciansin4studies[18,33,34,40].Familyphysicianswere also studiedalong with geriatricians (n=1)[32], paediatricians (n=1)[19]orGPs(n=1)[25].Surgeryphysicianswerestudiedin threepapers,namelyanaesthetistsinone[35],internistsand urol-ogistsinanother[42]andmedical,obstetrician/gynaecologyand paediatricspecialistsinthethird[30].Theremainingthreepapers includedallopathicphysicians(n=1)[45]andobstetricians(n=2)

[16,26].

Intermsofthemethodologyofanalysis,eightpapersapplied groundedtheory[20,27,29,38,39,41,43,44],fourstudiesreliedon thematic analysis [15,19,24,47] and one study used both [35]; thephenomenographicapproach[42,46],ethnography[16,26]and contentanalysis[22,45]wereusedintwopaperseach,andWalker etal.[23] performedathematicanalysisfollowed byacontent analysis.

With respect to the diseases/clinical conditions targeted, respiratory tract infections were the subject of 11 studies

[15,20,22,25,27,28,31,33,34,37,40]. Otherdiseasestargeted were urinary tract infection (n=2) [23,32], infectious diseases (n=1)

[46],surgical-siteinfections(n=1)[35],diarrhoea(n=1)[17]and uncomplicatedlacerations(n=1)[48].Onepaperaddressed respi-ratorytractinfectionanddiarrhoea[41]andtwopapersstudied antibiotic use in Caesarean section [16,26]. The remaining 15 papers(43%)failedtoidentifythediseaseorspeciﬁcclinical con-dition.

Regardingthetypeofpatientstudied,sevenstudiesconﬁned themselves to paediatric patients [17–19,25,33,34,40] and one alsoincludedadults[20];sixstudiesfocusedexclusivelyonadult

[22], elderly[23,32]and emergency[21,37,48] patients;Altiner et al.[28] selectedpatientsaged>16 years withnounderlying chroniclungdiseases,immunodeﬁcienciesorrecentepisodesof acute cough;anothertwo papers studiedthe useofantibiotics inpregnantwomen[16,26],andTanetal.[35]includedsurgical patients;theremainingpapers(49%)describednopatient-speciﬁc characteristics.

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Fig.1.Flowdiagramshowingstudyextractionandselection.

Data collection methods also varied, with most studies using semistructured and/or ‘think aloud’ interviews (n=16)

[15–17,20,26,27,29,35,37–39,41,42,45,46,48], questionnaires (n=9) [18,21,25,30–33,36,40] or focus group discussions (n=6)

[19,22,23,44,47,49]. Recorded consultation was used in two papers[28,34]andanothertwopaperscollecteddatabymeansof interviewsandrecordedconsultations[24,43].

3.4. Factorsidentiﬁedasinﬂuencingantibioticprescription

Eachstudyselectedwasassessedtoidentifyaspectssaidtobe relatedtoantibioticprescribing,i.e.factorsintrinsicandextrinsic tothehealthcareprofessional.

3.4.1. Intrinsicfactors

Intrinsicfactorscited by physicians asinfluencing antibiotic prescribingcouldbegroupedintotwobroadcategories,namely sociodemographicfactorsandphysicians’ attitudes(Table2).In general,fewstudiesdescribedsociodemographicfactorsasbeing related to misprescription of antibiotics. Medical specialisation andsexwereassessedinonepaperbutnodirectinfluencewas observed[25].Previousclinicalexperiencewasconsideredtobea factorhavinganinfluenceonantibioticprescribingbyninestudies

[15,17,25–27,36,39,43,47].Theinﬂuenceofyearsofpracticewas assessedinthreestudies,withapositivecorrelationbeingfoundin two[17,29]andnoinﬂuencefoundinthethird[25].

Two studies [38,47] reported that university education had a direct relationship with antibioticprescribing; a further two

papers,however,reportedthatthis parameterhad noinfluence onphysicians’decision-making[17,25].Continuousmedical edu-cation wasidentified as havinga direct influenceon antibiotic prescribinginthreepapers[16,25,27].

Attitudes were identiﬁed as the major factor inﬂuencing antibioticprescription.Eleven papers described thedirect rela-tionshipbetweenphysicians’ignoranceandantibioticprescription

[15,17,20,23,27,29,38,41–43,49].Adirectrelationshipwith indif-ference and antibiotic misuse was assessed in nine studies

[16,19,20,26,29,35,36,38,49].

Complacencywasthemostfrequentlymentionedattitude,with 24 papers [17–20,22,24–28,30,31,33,34,37–41,43,44,46,48,49]

expressingdivergingopinionsastoitsinfluenceand3concluding thatithadlittleornoinfluenceonantibioticprescribing[17,30,43]. Fearwasalsofrequentlydescribed:(i)ontheonehand,fear ofmore seriouscomplicationsdeveloping wasassessedas hav-ing a direct relationship withmisprescription of antibiotics by 15studies[16,17,19,20,22,26,27,37–40,42–44,49];and(ii)onthe otherhand, fear oflosing patientswas identifiedin 10 studies

[16–20,22,25,26,43,44],only1ofwhichfailedtolinkitdirectlyto antibioticmisuse[25].

Responsibilityofothers(i.e.otherphysicians,patientsorother healthcareproviders)wasdescribedinsixpapersasbeingafactor havinganinfluenceonantibioticprescribing[19,20,35,44,45,49], whilstconfidencewasidentifiedbyeightstudiesasunderlyingthe misuseofsuchdrugs[15–17,20,24,26,27,47].

Finally,physicians’expressdesireforaquickﬁxandthe prob-lemof diagnosticuncertainty werereported asbeingthe basis

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ofantibioticmisusein8studies[19,27,28,33,39,42,43,46]and15 studies[17,20,22–25,27,39–44,48,49],respectively.

3.4.2. Extrinsicfactors

Factors not directly related tophysicians but none the less reportedasinfluencingtheantibioticprescriptionprocesswere groupedintothefollowingthreecategories:patient-related fac-tors;healthcare system-relatedfactors;andtheimpactofthree otherfactors,namelytheinfluenceofpharmaceuticalcompanies, cost saving (to thepatient or healthcare system) and financial incentives(Table3).

The most frequently described patient-related factors were thoselinkedtosignsandsymptomspresentatthedateof pre-scription.Todifferentiatebetweenthesefactors,thedeﬁnitionof theMedlinePlusmedicaldictionarywasused[50],withsignsbeing assessedin14studies[19,20,22–24,26–28,30,37,39,43,48,49]and symptomsalsobeingincludedin5studies[22–24,27,43].All stud-iesidentiﬁedadirectrelationshipbetweensigns,symptomsand antibioticprescribing,withthemostcitedfactorsbeingfever(n=5)

[23,24,27,30,43],‘looksunwell’(n=7)[20,23,27,28,37,39,49],pain (n=3)[24,27,43]andphlegmcharacteristics(n=4)[20,28,37,49]. Patients’expressdesireforaquickﬁxwaslinkedtoantibiotic pre-scribinginfourpapers[19,28,43,44].

Other patient-related clinical conditions identiﬁed by four studiesas havinganinﬂuence ontheprescribingof antibiotics by physicians were as follows: allergy to antibiotics in three

[21,32,39];co-morbidity intwo [32,39]; pregnancyinone[21]; and thepatient’s speciﬁc clinical conditionin two [24,32].The remainingfactors,whichincludedage(n=3)[23,33,39],anxiety (n=2)[20,33],economicandsocialfactors(n=4)[24,26,27,43]and educationallevel(n=2)[27,33],werealsodescribedashavinga directinﬂuenceonantibioticprescribing.

Insofarashealthcaresystem-related factorswereconcerned, pressureoftime—directlyrelatedtopatientvolume—wasassessed by12papers[18,20,22,24,25,27,30,42–46],withalackof correla-tionbetweenthisfactorandantibioticprescribingbeingfoundin onlyone[25].Infivestudies,thecommunicationandorganisational modelwasidentifiedasbeinginfluentialonantibioticprescribing

[16,23,25,34,35]. Ofthe12studiesthat addressedimplemented policies/guidelines [15,16,19,21,25,27,29,35,39,41,45,49], only 7

[16,19,25,27,29,39,49]describedthisfactorashavinganinfluence ondecision-making,thusrenderingtheresultsinconclusive.The remainingfactors,whichincludedaccreditationlevelofpractice setting(describedin onepaper)[26] andownershipofpractice location(describedby twopapers asbeingan importantfactor in antibiotic prescription [17,44]) received less mention. Other healthcare system-related factors identified were: influence of groupexposures[19];publichealthconsiderations[38];workflow

[35]; lackofdiagnostictest facilities[30]; thefactthat patients couldusethesameprescriptionmorethanonce[44];andpatients’ healthinsurance[48].

The pressure exerted by pharmaceutical companies was assessedbysixstudiesbut therewasa differenceofopinionas toits realinfluence: whereas one-halfof thestudies identified suchpressureasbeinganinfluentialfactorinantibioticprescribing

[17,19,44],theotherthreereporteditashavinglittleornoinﬂuence whatsoever[25,39,49].

Costsavingwasassessedintenpapers.Onidentifyingwhether physicians’ concernwasabout patientcosts,healthcare system expensesorboth,it wasreportedasfocusingonthehealthcare systembyﬁvepapers[16,30,39,41,44],onpatientexpensesbyone study[24]andonbothbytwostudies[26,43].Twostudiesreported costsavingasbeinganimportantfactorinthedecisiontoprescribe antibioticsbutdidnotexpresslyidentifycostsavingasthetarget

[25,48].

Lastly,twostudieshighlightedthefactthatﬁnancialincentives promotedtheoverprescriptionofantibiotics[17,40].

4. Discussion

Thiswasasystematicreviewofqualitativestudiesfocusedon examiningthesubjectiveopinionsofphysiciansaboutallthe fac-torsthatinfluencetheantibioticprescribingprocess,providinga new,specificoverviewofeachfactor involvedanditsinfluence ontheoutcomesofantibioticuse.Intheresults,attitudesemerge asbeingthemostimportantfactoraffectingantibiotic prescrip-tion,afindingthatcouldbeofgreatimportancewhenitcomes todesigninginterventionstoimproverationalantibiotic prescrib-ing.

Antibioticresistanceisbroadlyassociatedwithantibiotic mis-useand is thus related tothebehaviour ofall actorsinvolved. Physicianshaveapivotalroleandcriticalresponsibilitybecause antibiotic use is mainly associated with their counselling and prescribingpractices.Thesefindingsreflectphysicians’extended overviewofantibioticprescription,revealingittobeacomplex processinfluencedbydirect(i.e.player-related)factorsandindirect factorsthataffectthedecision-makingprocess.

Despitethewell-establisheddistinctionbetweenintrinsicand extrinsicfactors,thisreviewwouldneverthelesssuggestthatthey are interrelated. To improve rationalantibiotic prescribingand allayglobalconcern,anin-depthunderstandingofthesefactorsand theirinterrelationshipisfundamental.Inlinewiththeliterature

[51,52],wethereforeproposeatheoreticalframeworkfor system-atisingtheinterconnectionamongthefactorsidentiﬁed(Fig.2).

Asreportedelsewhere[53,54],examination oftheextracted data showed physicians’ attitudes to be dominant. Of the six attitudes identiﬁed, those most cited by physicians were complacency—mainly linked to patients’ expectations of or demandforantibiotics—andfear.Evenso,accordingtothis analy-sis,alltheattitudesarerelatedtooneormoreoftheotherfactors identiﬁed,asshowninFig.2.

Withregardtosociodemographicfactors,webelievethatthese couldinﬂuencephysicians’knowledge(previousclinicalpractice, universityeducation,continuousmedicaleducationandyearsof practice),attitudes(age,sexandmedicalspecialisation)and clin-icalpractice.Yetnotonlydoestheliteraturecontainfewstudies

[11,55] that describe how physician-related sociodemographic factorsinfluenceantibioticprescribing,buttheirresultsare incon-clusive,presumably becausethis wasnot themain goal of the studiesselected.Inthespecificcaseofuniversityeducation,bothof thestudiesthatreportthistobeafactorinfluencingantibiotic pre-scribinghighlightsupervisors’influenceduringhospitaltrainingas wellasknowledgeacquiredduringuniversityeducationas consti-tutingafundamentalstepinphysicians’clinicalpractice[38,47]. Theseresultsareinagreementwiththeliteratureandconfirmthe difficultyofchangingthebehaviourofphysicianswhoarealready trained[56].

Regarding patient-related factors, these results suggest that physiciansassumethatthesehaveaninfluenceontheirantibiotic prescribing,withsignsandsymptomsrankingamongthosewith thehighestimpact.Feverof<3daysorphlegmcharacteristicswere associatedwithantibioticprescribing,eventhoughthereisno sci-entificevidencetoshowthatantibioticsarenecessary[57].Wealso identifiedthelinkbetweenpatients’expressdesireforaquickfix andantibioticmisuseandrecognisethatthiscouldbelinkedto complacency.

Healthcare systemsare related toantibioticmisprescription, both directlyand indirectly:(i) directly via implemented poli-cies/guidelines;and(ii)indirectlyby,say,theinﬂuenceofpatient volumeandpressure,whichfostersantibioticprescribingbasedon

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Fig.2.Theoreticalframeworkoftheinﬂuenceofandinterconnectionamongfactorsthatinﬂuenceantibioticprescribing.

conﬁdenceinantibiotictherapy and/orthefearofmoreserious complicationsdevelopingoroflosingpatients.

There were other extrinsic factors identified in the studies selectedbuttheirpoordescriptionpreventsusfromdrawingany generalconclusions. Nevertheless, we believe that in order for antibioticprescriptionpatternsinanygivensettingtobe prop-erlyunderstood,certainspecificfactorsmustbetakenintoaccount whenimplementinganyintervention.Therearecertainfactorsthat tendtobeassociatedwithagivencontext,beitacountryorhealth system,etc.Inthisreview,therefore,manysuchfactorswerefound andnotallcouldbeanalysed:thesewerefactorsspecifictoagroup ofphysicians(workflow)[35]ortypeofpatient(groupexposures)

[19],healthcaresystem(accreditationlevel,inexistenceof diagnos-ticfacilities,ownershipofpracticelocation)[17,26,30,44]orpublic healthpolicy(publichealthconsiderations)[38].

Althoughthisanalysisoftheroleofthepharmaceuticalindustry yieldedcontroversialresults,somestudieshavealreadydescribed thedirectrelationshipbetweenthisfactorandantibiotic prescrib-ing[58–60].

Accordingtothisanalysis,communicationskillsanddiagnostic uncertainty rank among theprincipal indirect factors influenc-ing antibioticprescription and may provide an attractivebasis forimprovingprescribingpractices.Althoughphysiciansreported communication skills as a problemin only five of the studies selected[16,23,25,34,35],weneverthelessbelievethat,onthebasis ofcomplacency,thisfactorisanattituderelatedtopatient expecta-tions,inlinewithpublishedpaperswhichshowthatimprovement in physician–patientcommunication can reduce patient expec-tationsof antibiotictreatment[61,62].Inthecase ofdiagnostic uncertainty,thecurrent findingssuggestthat this mayhavean indirectimpactbyinfluencingphysicians’attitudes,suchasfearor confidence.Theliteraturealsodescribestherelationshipbetween diagnosticuncertainty andantibioticmisuse,stressingtheneed forrapiddiagnostictests,implementationofpolicies/guidelinesor useofdelayedprescribingaswaysofcounteractingthisproblem

[23,27,63–65].

Someauthorshavealreadystudiedtheimplementationof spe-ciﬁc interventions [66–68]along withhealthcare professionals’ opinionsaboutdifferentstrategies forovercomingtheobstacles that could affect the success of such interventions [63,69–71]. Indeed, considering the heterogeneity of the factors identiﬁed

ashavingan influenceonantibioticprescribingbythis review, we believe that, when it comes to designing effective strate-gies,factorsspecifictoeachclinicalpracticemustbetakeninto account.ThisisinlinewithTonkin-Crineetal.[8]whosuggest that,inordertoaddressfactorsinfluencingantibioticprescribing decisions,interventionsshouldreflectGPs’ownpractices,reduce diagnosticuncertainty,educatehealthprofessionalsabout antibi-oticprescribing,facilitatepatient-centredcareandbebeneficialfor GPstoimplementinpractice.

Thisreviewhassomelimitations:itonlyincludedpublished papersandthesewereveryheterogeneous,renderingitsusceptible tobias[72].Themainimportanceofsuchheterogeneityliesinthe differentsettings(thestudiesweremainlyfromEuropeandNorth America),workplaces(differentrealitiespresentdifferentfactors), datacollectionmethods,andmethodsofanalysisused.Itisalso importanttounderstandthatqualitativeresearchconcernsbias andgeneralisationandismorevalidbutlessreliablethan quan-titativeresearch[73].Ingeneral,thesmallnumberofphysicians whoparticipatedinthequalitativestudiesreviewedamountsto anotherlimitationonthegeneralisationoftheconclusions.

Weacknowledgethattheconclusionscouldberelatedtoour speciﬁcinterpretationsoftherespectivepapers’results,andthat otherconclusionsmightbeequallyvalid.Itisalsoimportantto pointoutthat,althoughtheattitudesareshownasseparateand distinct,weareawarethatincertainsituationssomemaywellbe linked(e.g.fearoflosingpatientsandcomplacency).

5. Implicationsforpracticeandresearch

Qualitativemethodologyisbecomingroutineinmedical stud-ies, assuming the main role of exploring complex topics and definingnewapproachestothefieldtargeted[74,75].Withregard toantibioticprescribing,thismethodologyhasshownitselftobe veryusefulforunderstandingthesubjectiveperceptionsofallthe playersinvolved, essentiallyphysiciansand policy-makers.This paperpresentsafundamental understandingofthefactorsthat physiciansseeasinfluencingantibioticprescribingand engender-ingthemisuse ofantibiotics. Thisstudycomplements previous quantitativeresearch[11]andenhancesexistingknowledgeofthe relationshipbetweenthefactorsidentifiedandphysicians’ percep-tionsandfeelings.

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Wefeelthatanysubsequentinterventionsaimedatimproving rationalantibioticprescribingwoulddowelltoconsidertheresults reportedinthisreview.Thedetailedknowledgeaboutphysicians containedherecouldprovevitalwhenitcomestotackling world-wideconcerneffectively.

6. Conclusions

Inconclusion, we believethatthesefindings willpromote a betterunderstandingofphysicians’perceptionsofthefactorsthat influencetheantibioticprescribingprocess,clarifyhowsuch fac-tors influence thedecision-making process, and highlight their importanceinthedesignofstrategiesaimedattacklingthis con-cerneffectively.

Funding:ThisworkwassupportedbytheFundac¸ãoparaa Ciên-ciaeaTecnologia(FCT)[grantPTDC/SAU-ESA/105530/2008]from thePortugueseMinistryof Science&Education,and theFondo deInvestigaciónSanitaria(FIS)[grantsPI081239andPI09/90609] fromtheSpanishMinistryofHealth.

Competinginterests:Nonedeclared. Ethicalapproval:Notrequired.

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