investigating suspected bone infection in the diabetic foot _ the bmj
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13/06/2015 Investigatingsuspectedboneinfectioninthediabeticfoot|TheBMJ
http://www.bmj.com/content/339/bmj.b4690 1/12
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InvestigatingsuspectedboneinfectioninthediabeticfootBMJ2009339doi:http://dx.doi.org/10.1136/bmj.b4690(Published04December2009)Citethisas:BMJ2009339:b4690
ArticleRelatedcontentMetricsResponsesPeerreview
JamesTeh,consultantradiologist1,TonyBerendt,consultantphysician2,BenjaminALipsky,professorofmedicine3
Authoraffiliations
Correspondenceto:JTehjames.teh@tiscali.co.uk
Accurateandearlydiagnosisofthisconditioniskeytosuccessfulmanagement.Thisarticleguidesyouthroughthediagnosticoptions
Learningpoints
Diabeticfootosteomyelitisisinvariablyaccompaniedbyfootulceration
Plainradiographyshouldbethefirstimagingtestusedbutmaynotshowchangesforuptotwoweeks
Magneticresonanceimagingisthemostaccurateimagingmodality
Nuclearmedicinescansplayonlyamodestroleinthediagnosis
Bonebiopsyisthecriterionstandardforthediagnosisofosteomyelitisbutisnotneededineverycase
ThepatientA58yearoldmanwithlongstandingtype2diabetespresentedwithanonhealingulceronthesideoftherightgreattoe,withassociatedspreadingcellulitis.Laboratorytestsshowedawhitebloodcellcountof11.310 /l(normalrange3.29.8),aneutrophilcountof510 /l(35.8),andanerythrocytesedimentationrateof45mm/h(normal
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13/06/2015 Investigatingsuspectedboneinfectioninthediabeticfoot|TheBMJ
http://www.bmj.com/content/339/bmj.b4690 2/12
Osteomyelitisofthefootisacommonandchallengingprobleminpatientswithdiabetes.1Around25%ofpatientswithdiabeteswilldevelopafootulcer,usuallyatareasofpressure,suchastheheelormetatarsalheads.2Osteomyelitisisalmostalwayscausedbycontiguousspreadofinfectionfromoverlyingfootulcerationandcomplicatesupto20%ofulcers.3
Thetwomajordifficultiesindiagnosingdiabeticfootosteomyelitisarethatimagingtestscanbeinsensitivetoearlydiseaseandthatbonychangesrelatedtoneuroarthropathy(Charcotsfoot)canmimicinfectivechange.Accurateandearlydiagnosisofthisconditionisthekeytosuccessfulmanagement,whichmayincludeprolongedtreatmentwithantibioticsorsurgicalresection.45
Cliniciansshouldsuspectosteomyelitiswhenafootulcerisdeep,theulcerfailstohealdespiteappropriateoffloadingandperfusion,orwhenboneisvisibleorpalpablewithametalprobe.Laboratorytestshavelimitedvalueandmustbeinterpretedtogetherwiththeclinicalpicture.Anerythrocytesedimentationrateofmorethan70mm/hincreasesthelikelihoodofosteomyelitis,especiallyiftheulcerisdeep,6butthewhitecellcountisanunreliableindicator.Thediagnosisofosteomyelitisisusuallybasedonacombinationofclinicalandimagingtests,butthecriterionstandardistheisolationofpathogensordemonstrationofclassichistopathologicalchangesonbonebiopsy.
Whattestsshouldbeperformed?PlainradiographyPlainradiographsofthefoot,takeninatleasttwodifferentprojections,shouldbetheinitialimagingtest(fig1).47Typicalfindingsofearlyosteomyelitisarefocallucencyofthebone,withlossofthetrabecularpatternandcorticaldestruction.Asosteomyelitisevolves,radiographsmayshowperiostealreaction,sclerosis,andnewboneformation.
Thesensitivityofradiographsfordiagnosingosteomyelitisrangesfrom22%to75%,89mainlybecausechangesmaynotoccuruntilaround50%oftheboneisdemineralised,whichcantakemorethantwoweeks.Furthermore,coexistingneuropathicarthropathyortraumacanmimicosteomyelitis.Despitetheselimitations,radiographsplayavitalroleinthefirstlinediagnosisofosteomyelitis,becausetheirspecificityisrelativelyhighinuncomplicatedcases.Radiographyisalsousefulwhenfollowingsuspectedinfection,becauseserialchangesmayshowosteomyelitisorbonyhealing.
Iftheinitialradiographsarenormalbutosteomyelitisisstillsuspected,itmaybehelpfultorepeatthetesttwotofourweekslater.Ifclassicchangesarepresentthenboneinfectionishighlylikely.Ifthechangesareequivocal,orcoexistingneuroarthropathyortraumaispresent,furtherimagingisadvised.
MagneticresonanceimagingMagneticresonanceimagingwithitslackofionisingradiation,excellentcontrastresolution,andmultiplanarcapabilityistheimagingmodalityofchoicefortheevaluationofdiabeticfootinfection.Evenifradiographssuggestosteomyelitis,magneticresonanceimagingisusefulforevaluatingtheextentofdiseaseandforguidingtreatment.
OsteomyelitismanifestsasfocaldecreasedsignalonaT1weightedsequence,withincreasedsignalonacorrespondingT2weightedfatsuppressedorshorttauinversionrecoverysequence(figs2and3).Acorticalbreachorintraosseousabscessmayalsoindicateosteomyelitis.5Noconvincingevidenceexiststhatintravenousgadoliniumincreasestheaccuracyofdiagnosisofosteomyelitis,butitdoes
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13/06/2015 Investigatingsuspectedboneinfectioninthediabeticfoot|TheBMJ
http://www.bmj.com/content/339/bmj.b4690 3/12
Fig1Plainradiographshowingsubluxationofthefirstmetatarsophalangealjoint,withlossofthenormalcorticaloutlineofthefirstmetatarsalheadandsclerosis(arrow).Minorlucencyisseen
atthebaseoftheproximalphalanxofthegreattoe.Therearemultipleoldfracturesofthemetatarsalsandarthropathyofthesecondandthirdmetatarsophalangealjointsindicatingneuroarthropathy(arrowheads).Thefindingsaresuspiciousfor,butnotdiagnosticof,active
osteomyelitis
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improvetheevaluationofsofttissuepathology,therebyhelpingtodemonstrateabscesses,synovitis,andsinustracts.1011
Magneticresonanceimaginghasanoverallsensitivityofabout90%(range80100%),withaspecificityofabout80%(40100%)forthediagnosisofdiabeticfootosteomyelitisoverallaccuracyisaround89%.12Apositivemagneticresonanceimagingresultgreatlyincreasesthelikelihoodofosteomyelitis(likelihoodratio3.8),whereasanormalresultmakesosteomyelitismuchlesslikely(0.14).12Metaanalysesshowthatmagneticresonanceimagingoutperformsplainradiographyandnuclearmedicinestudiesinthediagnosisofthiscondition.13
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13/06/2015 Investigatingsuspectedboneinfectioninthediabeticfoot|TheBMJ
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Fig2Anaxialshorttauinversionrecoveryimageshowinghighsignalinthesofttissuesadjacenttothefirstmetatarsalheadatthesiteofulceration.Highsignalisseeninthefirst
metatarsalandproximalphalanxofthegreattoe(arrowheads)thisiscompatiblewithosteomyelitisandjointsepsis
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OtherteststoconsiderIftheplainradiographisequivocalandmagneticresonanceimagingcannotbeperformed,cliniciansshouldconsiderothertests.
ComputedtomographyAdvancesincomputedtomographytechnologyincludingtheabilitytoperformreformatsinanyplanewithoutlossofresolutionenablebetterevaluationforcorticalerosions,focalareasoflucency,andsequestrathanispossiblewithradiography.However,softtissuecontrastispoorcomparedwithmagneticresonanceimaging.Inmostcircumstances,computedtomographyprovidesonlylimitedadditionalinformationoverradiographyandisnotroutinelyused.
Triplephasetechnetium99MDPbonescanThetriplephasetechnetium99mmethylenediphosphonate(MDP)bonescanhasgreatersensitivitythanradiographyindiagnosingosteomyelitisbuthaslimitedvaluebecauseofitshighfalsepositiverate.14Softtissueinfection,neuroarthropathy,degenerativechanges,andfracturesmayresultin
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13/06/2015 Investigatingsuspectedboneinfectioninthediabeticfoot|TheBMJ
http://www.bmj.com/content/339/bmj.b4690 5/12
Fig3AnaxialT1weightedimageshowingcorticaldestructionandlowsignalmarrowchange,compatiblewithosteomyelitis(arrowheads)
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increaseduptakeandmimicosteomyelitis.Itssensitivityforthedetectionofdiabeticfootosteomyelitisisabout90%(range50100%),butitisnotgenerallyrecommendedbecausespecificityisonlyaround46%(18100%).1314
WhitebloodcellandantibodyscansThesensitivityofwhitebloodcellscansandantibodyscansisabout86%(range72100%)and93%(6798%),respectively.13Thesescanshaveaslightlylowersensitivitybutsubstantiallyhigherspecificitythanthetriplephase TcMDPbonescan.Investigationscomparinglabelledwhitecellimagingalonewithlabelledwhitecellimagingplusbonescanshowthatthecombinedstudyhasonlymarginallyincreasedaccuracy.14Whitecellscanshaveamodestroleindiagnosingdiabeticfootosteomyelitisbutmaybeusefulifmagneticresonanceimagingcannotbeperformed.
Fluorine18fluorodeoxyglucosepositronemissiontomographyFluorine18fluorodeoxyglucose,amarkerforincreasedintracellularglucosemetabolismaccumulatesatsitesofinfectionandinflammation.15Combinedwithcomputedtomography,thetechniqueallowspreciseanatomicallocalisationofincreasedisotopeuptake,therebyimprovingthedifferentiationbetweenosteomyelitisandsofttissueinfection.16Fewstudieshavebeenperformed,however,andfurtherinvestigationisneededbeforethistestcanberecommended.17
Ultrasound
99m
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13/06/2015 Investigatingsuspectedboneinfectioninthediabeticfoot|TheBMJ
http://www.bmj.com/content/339/bmj.b4690 6/12Fig4Afluoroscopicimageshowingpercutaneousbiopsyofthefirstmetatarsalheadusinga14
UltrasoundUltrasoundhaslimitedvalueinevaluatingdiabeticfootosteomyelitis.Nevertheless,itisusefulforevaluatingthesofttissuesandguidingaspirationorsofttissuebiopsy.
BonebiopsyforcultureandhistologyBonebiopsyisrecommendedifthediagnosisofboneinfectionremainsindoubtafterimaging,ifempiricaltreatmentwithantibioticsfails,ifamultidrugresistantorganismissuspected,orifametallicimplantisplannedforthesuspectbone.Deepneedlepuncturesandswabculturesareunreliableincomparisonandarenotrecommended.
Treatmentismorelikelytobesuccessfulifthechoiceofantibioticisbasedontheresultsofboneculture.Samplescanbeobtainedpercutaneouslyunderimagingguidanceorbyopensurgery.Antibioticsshouldbestoppedforatleast48hoursbeforebiopsytoincreasetheyieldofcultures.Scrupulousaseptictechniqueisneededtoavoidcontamination.Werecommendusingatleasta14gaugebonebiopsyneedle.Atleasttwobonesamplesshouldbeobtained,andtheseshouldbesentformicrobiologyandhistology.Althoughsafetoperform,bonebiopsyisnotwidelyused.
OutcomeBecausetheulcerfailedtohealoversevenweeksdespiteappropriatecare,includingbroadspectrumantibiotics,thepatientunderwentfluoroscopicguidedpercutaneousbiopsyofthefirstmetatarsalhead(fig4).AcultureofthebonesamplegrewStaphylococcusaureus,whichwasfoundtobesensitivetoflucloxacillin.Thehistopathologysamplewascrushedandconsiderednondiagnostic.Afterasixweekcourseoforalflucloxacillintheulcereventuallyhealed.Figure5showsasuggestedimagingalgorithmforsuspectedfootosteomyelitisindiabetes.
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13/06/2015 Investigatingsuspectedboneinfectioninthediabeticfoot|TheBMJ
http://www.bmj.com/content/339/bmj.b4690 7/12
Fig4Afluoroscopicimageshowingpercutaneousbiopsyofthefirstmetatarsalheadusinga14gaugebonebiopsyneedle
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Fig5Suggestedimagingalgorithmforsuspectedfootosteomyelitisindiabetes
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NotesCitethisas:BMJ2009339:b4690
Footnotes
Thisseriesprovidesanupdateonthebestuseofdifferentimagingmethodsforcommonorimportantclinicalpresentations.TheseriesadvisersareFergusGleeson,consultantradiologist,ChurchillHospital,Oxford,andKaminiPatel,consultantradiologist,HomertonUniversityHospital,London.
Contributors:JTselectedthepatient,searchedtheliterature,wrotethepaper,andchosetheimages.TBandBALhelpededitandpreparethefinaldraft.
Competinginterests:Nonedeclared.
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13/06/2015 Investigatingsuspectedboneinfectioninthediabeticfoot|TheBMJ
http://www.bmj.com/content/339/bmj.b4690 8/12
Provenanceandpeerreview:Commissionedexternallypeerreviewed.
Patientconsentobtained.
References1.LipskyBA.Osteomyelitisofthefootindiabeticpatients.ClinInfectDis199725:131826.
Abstract/FREEFullText
2.LaveryLA,ArmstrongDG,WunderlichRP,TredwellJ,BoultonAJ.Diabeticfootsyndrome:evaluatingtheprevalenceandincidenceoffootpathologyinMexicanAmericansandnonHispanicwhitesfromadiabetesdiseasemanagementcohort.DiabetesCare200326:14358. Abstract/FREEFullText
3.LaveryLA,PetersEJ,ArmstrongDG,WendelCS,MurdochDP,LipskyBA.Riskfactorsfordevelopingosteomyelitisinpatientswithdiabeticfootwounds.DiabetesResClinPract200983:34752. CrossRef MedlineWebofScience
4.BerendtAR,PetersEJ,BakkerK,EmbilJM,EnerothM,HinchliffeRJ,etal.Specificguidelinesfortreatmentofdiabeticfootosteomyelitis.DiabetesMetabResRev200824(suppl1):S1901. CrossRef MedlineWebofScience
5.MorrisonWB,SchweitzerME,WapnerKL,HechtPJ,GannonFH,BehmWR.Osteomyelitisinfeetofdiabetics:clinicalaccuracy,surgicalutility,andcosteffectivenessofMRimaging.Radiology1995196:55764.CrossRef Medline WebofScience
6.FleischerAE,DidykAA,WoodsJB,BurnsSE,WrobelJS,ArmstrongDG.Combinedclinicalandlaboratorytestingimprovesdiagnosticaccuracyforosteomyelitisinthediabeticfoot.JFootAnkleSurg200948:3946.CrossRef Medline WebofScience
7.LipskyBA,BerendtAR,DeeryHG,EmbilJM,JosephWS,KarchmerAW,etal.Diagnosisandtreatmentofdiabeticfootinfections.ClinInfectDis200439:885910. FREEFullText
8.EckmanMH,GreenfieldS,MackeyWC,WongJB,KaplanS,SullivanL,etal.Footinfectionsindiabeticpatients.Decisionandcosteffectivenessanalyses.JAMA1995273:71220. CrossRef Medline WebofScience
9.DinhMT,AbadCL,SafdarN.Diagnosticaccuracyofthephysicalexaminationandimagingtestsforosteomyelitisunderlyingdiabeticfootulcers:metaanalysis.ClinInfectDis200847:51927.Abstract/FREEFullText
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11.TanPL,TehJ.MRIofthediabeticfoot:differentiationofinfectionfromneuropathicchange.BrJRadiol200780:93948. Abstract/FREEFullText
12.ButaliaS,PaldaVA,SargeantRJ,DetskyAS,MouradO.Doesthispatientwithdiabeteshaveosteomyelitisofthelowerextremity?JAMA2008299:80613. CrossRef Medline WebofScience
13.KapoorA,PageS,LavalleyM,GaleDR,FelsonDT.Magneticresonanceimagingfordiagnosingfootosteomyelitis:ametaanalysis.ArchInternMed2007167:12532. CrossRef Medline WebofScience
14.CapriottiG,ChianelliM,SignoreA.Nuclearmedicineimagingofdiabeticfootinfection:resultsofmetaanalysis.NuclMedCommun200627:75764. CrossRef Medline WebofScience
15.BasuS,ChryssikosT,MoghadamKiaS,ZhuangH,TorigianDA,AlaviA.Positronemissiontomographyasadiagnostictoolininfection:presentroleandfuturepossibilities.SeminNuclMed200939:3651. CrossRefMedline WebofScience
16.KeidarZ,MilitianuD,MelamedE,BarShalomR,IsraelO.Thediabeticfoot:initialexperiencewith18F
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13/06/2015 Investigatingsuspectedboneinfectioninthediabeticfoot|TheBMJ
http://www.bmj.com/content/339/bmj.b4690 9/12
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16.KeidarZ,MilitianuD,MelamedE,BarShalomR,IsraelO.Thediabeticfoot:initialexperiencewith18FFDGPET/CT.JNuclMed200546:4449. Abstract/FREEFullText
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TehJames,BerendtTony,LipskyBenjaminA.InvestigatingsuspectedboneinfectioninthediabeticfootBMJ2009339:b4690
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