investigating suspected bone infection in the diabetic foot _ the bmj

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

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JamesTeh,consultantradiologist1,TonyBerendt,consultantphysician2,BenjaminALipsky,professorofmedicine3

Authoraffiliations

Correspondenceto:[email protected]

Accurateandearlydiagnosisofthisconditioniskeytosuccessfulmanagement.Thisarticleguidesyouthroughthediagnosticoptions

Learningpoints

Diabeticfootosteomyelitisisinvariablyaccompaniedbyfootulceration

Plainradiographyshouldbethefirstimagingtestusedbutmaynotshowchangesforuptotwoweeks

Magneticresonanceimagingisthemostaccurateimagingmodality

Nuclearmedicinescansplayonlyamodestroleinthediagnosis

Bonebiopsyisthecriterionstandardforthediagnosisofosteomyelitisbutisnotneededineverycase

ThepatientA58yearoldmanwithlongstandingtype2diabetespresentedwithanonhealingulceronthesideoftherightgreattoe,withassociatedspreadingcellulitis.Laboratorytestsshowedawhitebloodcellcountof11.310 /l(normalrange3.29.8),aneutrophilcountof510 /l(35.8),andanerythrocytesedimentationrateof45mm/h(normal



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



Fig1Plainradiographshowingsubluxationofthefirstmetatarsophalangealjoint,withlossofthenormalcorticaloutlineofthefirstmetatarsalheadandsclerosis(arrow).Minorlucencyisseen

atthebaseoftheproximalphalanxofthegreattoe.Therearemultipleoldfracturesofthemetatarsalsandarthropathyofthesecondandthirdmetatarsophalangealjointsindicatingneuroarthropathy(arrowheads).Thefindingsaresuspiciousfor,butnotdiagnosticof,active

osteomyelitis

DownloadfigureOpeninnewtab

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improvetheevaluationofsofttissuepathology,therebyhelpingtodemonstrateabscesses,synovitis,andsinustracts.1011

Magneticresonanceimaginghasanoverallsensitivityofabout90%(range80100%),withaspecificityofabout80%(40100%)forthediagnosisofdiabeticfootosteomyelitisoverallaccuracyisaround89%.12Apositivemagneticresonanceimagingresultgreatlyincreasesthelikelihoodofosteomyelitis(likelihoodratio3.8),whereasanormalresultmakesosteomyelitismuchlesslikely(0.14).12Metaanalysesshowthatmagneticresonanceimagingoutperformsplainradiographyandnuclearmedicinestudiesinthediagnosisofthiscondition.13



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



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


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.



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.



Provenanceandpeerreview:Commissionedexternallypeerreviewed.

Patientconsentobtained.

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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

10.MorrisonWB,SchweitzerME,BatteWG,RadackDP,RusselKM.Osteomyelitisofthefoot:relativeimportanceofprimaryandsecondaryMRimagingsigns.Radiology1998207:62532. Medline WebofScience

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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17.BerendtAR,PetersEJ,BakkerK,EmbilJM,EnerothM,HinchliffeRJ,etal.Diabeticfootosteomyelitis:aprogressreportondiagnosisandasystematicreviewoftreatment.DiabetesMetabResRev200824(suppl1):S14561. CrossRef Medline WebofScience

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investigating suspected bone infection in the diabetic foot _ the bmj

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