w w w . r b o . o r g . b r
Original
Article
Prevention
of
lower-limb
lesions
and
reduction
of
morbidity
in
diabetic
patients
夽
,
夽夽
Antônio
Homem
do
Amaral
Júnior
a,
Leonã
Aparecido
Homem
do
Amaral
a,∗,
Marcus
Gomes
Bastos
a,
Luciana
Campissi
do
Nascimento
a,
Marcio
José
Martins
Alves
a,
Marco
Antonio
Percope
de
Andrade
baUniversidadeFederaldeJuizdeFora(UFJF),JuizdeFora,MG,Brazil
bSchoolofMedicine,UniversidadeFederaldeMinasGerais(UFMG),BeloHorizonte,MG,Brazil
a
r
t
i
c
l
e
i
n
f
o
Articlehistory:
Received20June2013 Accepted23August2013 Availableonline4July2014
Keywords:
Diabetesmellitus Primaryprevention Foot
Diabeticneuropathies Peripheralvasculardiseases Infection
Ulcer Amputation
a
b
s
t
r
a
c
t
Objective:Toassesstheimpactofadiabeticfootoutpatientcliniconreducingthemorbidity
ofthisdisease,withemphasisonlower-limblesions.
Methods:Thiswasaprospectiveobservationalstudywithatargetpopulationof30cases
outofatotalof77patientsinthediabeticfootoutpatientclinic.Theinclusioncriterionwas thatdatarelatingtolaboratorytests,clinicalexaminations,neuropathicandvasculartests andtheelbow-armindexneededtobeavailablefromallthepatients,withrepetitionafter 18monthsoffollow-up,soastoanalyzetheirevolution.Thestatisticalanalysiswasdone usingtheMcNemarchi-squaretestfordependentsamples.
Results:Thepatients’meanagewas61years.Allofthemhadtype2diabetesmellitus(DM),
whichhadstarted14.5yearspreviously,onaverage,and20%hadneuropathies.After18 months,therewasnochangeinthefrequencyoflesionsindiabetestargetorgans(p=1.000) orintheneuropathyrate(p=1.000).However,thereweresignificantimprovementsin neu-ropathicsymptoms,from70%to36.7%(p=0.035),andinperipheralarterialdisease,from 73.3%to46.7%(p=0.021).Therewasalsoadecreaseinulcersfrom13.3%to10%(p=1.000).
Conclusions:Creationofspecializedoutpatientclinicsforpreventionofdiabeticfootisa
viableinvestment,whichhaslowcostcomparedwiththehighcostsgeneratedthroughthe complicationsfromthisdisease.Thisapproachnoticeablyimprovesthepatients’qualityof life,withreductionofmorbidity.
©2014SociedadeBrasileiradeOrtopediaeTraumatologia.PublishedbyElsevierEditora Ltda.Allrightsreserved.
夽
Pleasecitethisarticleas:doAmaralJúniorAH,doAmaralLAH,BastosMG,doNascimentoLC,AlvesMJM,deAndradeMAPetal. Prevenc¸ãodelesõesdemembrosinferioresereduc¸ãodamorbidadeempacientesdiabéticos.RevBrasOrtop.2014;49(5):482–7.
夽夽
WorkperformedattheMinasGeraisInstituteforNephrologyStudyandResearch(IMEPEN),whichislinkedtotheSchoolofMedicine, UniversidadeFederaldeJuizdeFora(UFJF),JuizdeFora,MG,Brazil.
∗ Correspondingauthor.
E-mail:leonanamaral@yahoo.com.br(L.A.H.doAmaral). http://dx.doi.org/10.1016/j.rboe.2014.06.001
Prevenc¸ão
de
lesões
de
membros
inferiores
e
reduc¸ão
da
morbidade
em
pacientes
diabéticos
Palavras-chave:
Diabetesmellitus
Prevenc¸ãoprimária Pé
Neuropatiasdiabéticas Doenc¸asvascularesperiféricas Infecc¸ão
Úlcera Amputac¸ão
r
e
s
u
m
o
Objetivo:Avaliaroimpactodeumambulatóriodepédiabéticonareduc¸ãodamorbidadeda
doenc¸a,comênfasenaslesõesdosmembrosinferiores.
Métodos: Estudo prospectivo, observacional, compopulac¸ão alvo de 30 casos do total
de77 pacientesdoambulatóriodepédiabético.Ocritériodeinclusãofoiquetodosos pacientestivessemexameslaboratoriais,exameclínico,testesneuropáticoevasculare índicetornozelo-brac¸orepetidosapós18mesesdeacompanhamento,oquepermitiu anal-isarsuaevoluc¸ão.Aanáliseestatísticafoifeitacomotestequi-quadradodeMacNemarpara amostrasdependentes.
Resultados: Amédiadeidadedospacientesfoide61anos,todosportadoresdediabetes
mellitus(DM)tipo2,iniciadaemmédiahavia14.5anos,e20%eramneuropatas.Após18
meses,nãohouvemudanc¸anafrequênciadelesãoemórgãoalvodadiabetes(p=1000) enoíndicedeneuropatia(p=1000).Obteve-se,noentanto,melhoriasignificativados sin-tomasneuropáticosde70%para36.7%(p=0.035),bemcomodadoenc¸aarterialperiféricade 73.3%para46.7%(p=0.021).Foiobservadaaindadiminuic¸ãode13.3%para10%dasúlceras (p=1000).
Conclusões: Acriac¸ão deambulatórios especializados em prevenc¸ãodopé diabético é
investimentoviável,de baixocustoquando comparadoaosaltoscustos geradospelas complicac¸õesdessadoenc¸a.Essaabordagemmelhorasensivelmenteaqualidadedevida dopaciente,comareduc¸ãodamorbidade.
©2014SociedadeBrasileiradeOrtopediaeTraumatologia.PublicadoporElsevier EditoraLtda.Todososdireitosreservados.
Introduction
Diabetes mellitus (DM) causes degenerative complications that have human and socioeconomic repercussions and havebecomeanimportantpublic healthproblem.1 Among
these complications are lesions in target organs, includ-ingretinopathy,nephropathyandacceleratedatherosclerosis, withincreasedrisksofmyocardialinfarctionorstroke,and lesionsthataffectthefeet,whicharethemostfrequenttype.2
According tothe definition ofthe International Consensus onDiabeticFoot, thiscondition isunderstood toconsistof infection,ulcerationand/ordestructionofthedeeptissues, inassociation with neurologicalabnormalities and various degreesofperipheralvascular disease inthe lower limbs.2
Theprevalenceofulcers onthe feet of the diabetic popu-lationis between4%and 10%,and 85% ofamputations of the lower extremities among these patients are preceded byulceration.2 Approximately 40–60%of all non-traumatic
amputations ofthe lower limbsare performed on diabetic patients.1,2 Threeyearsafteramputationofalower limbof
adiabetic individual,the percentagesurvivalis50%,while overafive-yearperiod,themortalityraterangesfrom39%to 68%.3
Oneveryimportantfactorrelatingtodevelopmentofulcers onthefeetisthepresenceofperipheralmotor-sensory neu-ropathy,whichhasbeen associatedwithlossofsensitivity topainandlossofperceptionofpressure,temperatureand proprioception.4–8 This leads to diminished perception of
woundsortrauma.Fouroutofeveryfiveulcersondiabetic individualsareprecipitatedbyexternaltrauma.2Furthermore,
motorneuropathygivesrisetoatrophyandweakeningofthe intrinsicmusclesofthefeetandgeneratesdeformitiessuch ascrookedtoesandabnormalgaitpatterns,whichevolveto calluses andpressure ulcers.Casesofgreater severitylead toCharcotfoot,whichisaprogressivediseasecharacterized byjointdisplacement,pathologicalfracturesanddebilitating deformities.8,9Autonomicneuropathyalsoleadstoreduction
ortotalabsenceofsudoriparoussecretionandleadstoskin desiccation,withcracksandfissures.8,10
Peripheral vascular disease (PVD) is an important risk factor for ulceration and amputation.6,11–13 It resultsfrom
atherosclerosisofperipheralarteries,leadstoobstructionof distalarteriesandarterioles,hindersbloodflowanddeprives the tissues ofadequate supplies of oxygen, nutrients and antibiotics, which impairs ulcer healing and may conse-quently lead to gangrene.14 Gangrene is four times more
commonamongindividualswithdiabetesthaninthegeneral population,anditsincidencegraduallyincreaseswithageand withthedurationofthedisease.15
Ulcers generally result from trivial, mild and repeated trauma,suchaserroneousfitanduseoffootwear,orevenfrom walkingbarefoot.8,12Approximately70–100%ofulcerspresent
signsofperipheralneuropathywithvaryingdegreesofPVD. Infectionisonlyrarelyconsideredtobethedirectcauseof anulcer.16However,infectedulcerspresentahigherriskof
subsequentamputation.2
adequate treatment.1,17,18 With thisaim inmind,an
inter-disciplinarycareprogramfordiabetics(PAID)wasstartedin January2006,bythehypertension,diabetesandobesity con-trolclinicofthemunicipalhealthdepartmentofthecitywhere thisstudywasconducted.Thisprogrampromotesspecialized multidisciplinaryfollow-upfordiabeticpatientsandaimsto educatepatientsandtoimplementpreventionandearly diag-nosisandtreatmentoflesionsintargetorgans.
Objective
ToevaluatetheimpactofthePAIDdiabetic footoutpatient clinicforreducing morbidityamongdiabeticpatients, with emphasisonlower-limblesions.
Materials
and
methods
Thepresentstudywasapprovedbytheinstitution’sresearch ethics committee under protocol no. 1437.128.2008. It had supportfromtheNationalCouncilforScientificand Techno-logicalDevelopment(CNPq)throughitsinstitutionalprogram forscientificinitiationbursaries.Thiswasaprospective obser-vationalstudyoncases,withatargetpopulationformedby30 ofthe77patientsofthePAIDdiabeticfootoutpatientclinic. These patients were recruited spontaneously amongthose who,byApril2011,after18monthsoffollow-up,had under-gonecompleterepetitionoftheirinitialclinicalandlaboratory tests.
Theparticipantsinthisstudywereovertheageof18years, withoutdistinctionregardingsexorethnicity.Theywerefree torefusetoparticipateatanytime,withoutanymodification inthewayinwhichtheywereattendedbytheresearcher. Con-fidentialityandprivacywereguaranteed.Afreeandinformed consentstatementwassignedbyallparticipants.
All individuals who did not agree to participate were excluded, aswere all those who didnot participateinthe entireclinicalandlaboratoryreevaluationperformedafter18 monthsoffollow-up.
ThemultiprofessionalPAIDteamiscomposedofavascular surgeon,anendocrinologist,adermatologist,anephrologist,a psychologistandanutritionist.Allthepatientswerefollowed upand were referredtocardiologists,orthopedistsor oph-thalmologistsworkingforthemunicipalauthority,whenever necessary.
DescriptionofthefunctioningofthePAIDdiabeticfoot out-patientclinic:
1. Initial medical evaluation, with peripheral neurologi-cal clinical tests (diabetic neuropathy was classified in accordancewiththePortuguese-languageversionsofthe NeuropathicSymptomScoreandNeuropathicImpairment ScoredevisedbyMoreiraet al.19)andarterialevaluation
bymeansoftheankle-brachialindex(ABI)(systolic arte-rialpressureoftheankledivided bythe systolicarterial pressureofthe arm,bothmeasured withthepatient in thesupineposition,usingaportableDopplerdevice).2
Rep-etitionoftheneurologicalandvasculartests18 months later.
2. Laboratorytests.
3. Return visits were scheduled in accordance with the international diabetic foot consensus and the practical guidelinesformanagementandpreventionofdiabeticfoot (2007): annual returns, if neuropathy was absent; half-yearlyreturns,ifneuropathywaspresent;three-monthly returns, if neuropathy was present in association with signsofperipheralvasculardiseaseand/ordeformitiesof thefeet;orbetweeneveryoneandthreemonthsincases ofamputationorpreviousulceration.1
4. Thepatientsweresystematicallyadvisedregardingcareto betakenforavoidinglesionformation.Forthis,talkswere givenperiodically,leafletsweredistributedandguidance wasgivenduringconsultations.
5. Thewoundsweretreatedonanoutpatientbasis.Incases ofinfectedwoundsthatweregreaterthan2cmindiameter orshowedclinicalsignsofsepsis,thepatientsweresentto areferralhospital.
The data were entered into the Epi Info software (ver-sion 3.5.1). Statistical comparisons were made using the McNemarchi-squaretestfordependentsamples,whenthe variables were categorical; orusing the Student’st testfor dependent samples, whenthe variables were ofnumerical type.P-values<0.05 wereconsideredsignificant.The statis-ticalanalysiswasperformedusingtheSPSSsoftware,version 15.
Results
Seventy-sevenpatientsparticipatedinthefirstevaluationof thestudy,onthedaywhentheywerefirstregisteredatthe outpatientclinic.Therewere33males(42.9%)and44females (57.1%).Ofthese,30underwentcompleterepetitionofthe ini-tialsetofneurologicalandvasculartestsandlaboratorytests, after18monthsoffollow-up.
Thirteenoftheseweremale(43.3%)and17were female (56.7%), and all of them presented type 2 DM, which had started on average 14.5 years earlier. The patients’ mean age was 61 years and the standard deviation was 9.01.
At the first evaluation, four patients (13.3%) were seen tohaveundergonepreviousamputation.Amputationofthe fourth toe ofthe right footofonepatient wasseen atthe secondevaluation.
Sometypeoflesioninatargetorgan(heart,kidney,retina or microvasculature of the feet) was seen in 90% of the patients, andthe frequencyofthis didnotchangeafter18 months(p=1.000).Theratesofcardiacdiseases(40%;n=12) and renal diseases (23.3%; n=7) did not change (p=1.000), while retinopathy showed a non-significant increase from 53.3% (n=16) to 63.3% (n=19) (p=0.453). Furthermore, the patients did not present any occurrences of stroke and/or acutemyocardialinfarctionoverthisperiod.
Tables1–6presenttheresultsrelatingtothedataevaluated inthisstudy.
Table1–Perceptionofthecapacityforself-careofthefeet(n=30).
Firstevaluation Secondevaluation p
AbFr RFr(%) AbFr RFr(%)
Fullself-care 22 73.3 12 40.0 0.004
Partialself-care 7 23.3 17 56.7
Inabilitytoperformself-care 1 3.3 1 3.3
AbFr=absolutefraction;RFr=relativefraction.
Table2–Clinicalexaminationsonthefeet(n=30).
Firstevaluation Secondevaluation p
AbFr RFr(%) AbFr RFr(%)
Previousulcer 14 46.7 15 50.0 1.000
Amputation 4 13.3 5 16.7 1.000
Deformityofthefeet 6 20.0 6 20.0 1.000
Nailmycosis 19 63.3 15 50.0 0.125
Mycosisbetweentoes 14 46.7 5 16.7 0.012
Activeulcer 4 13.3 3 10.0 1.000
Cracks 3 10.0 3 10.0 1.000
Useofappropriatefootwear 14 46.7 25 83.3 0.013
Table3–Neuropathicsignscore19(n=30).
Firstevaluation Secondevaluation p
AbFr RFr(%) AbFr RFr(%) p=0.102
Normal 24 80.0 19 63.3
Mild 3 10.0 7 23.3
Moderate 3 10.0 4 13.3
Table4–Neuropathicimpairmentsymptomscore19(n=30).
Firstevaluation Secondevaluation p
AbFr RFr(%) AbFr RFr(%) p=0.035
Normal 3 10.0 8 26.7
Mild 6 20.0 11 36.7
Moderate 17 56.7 7 23.3
Severe 4 13.3 4 13.3
Table5–DiagnosisofdiabeticneuropathyaccordingtothecombinationindicatedbyMoreiraetal.19betweenthe neuropathicsymptomscoreandtheneuropathicimpairmentscore(p=1.000).
Firstevaluation Secondevaluation p
AbFr RFr(%) AbFr RFr(%) p=1.000
Neuropathicpatients 6 20.0 6 20.0
Non-neuropathicpatients 24 80.0 24 80.0
Table6–Peripheralarterialdiseasebasedontheankle-brachialindex(ABI)(n=30).
Firstevaluation Secondevaluation p
AbFr RFr(%) AbFr RFr(%)
Normal:0.91–1.30 8 26.7 13 43.3 0.129
Mildobstruction:0.70–0.90 8 26.7 6 20.0
Moderateobstruction:0.40–0.69 8 26.7 5 16.7
Poorlyreduced:>1.30 6 20.0 6 20.0
Discussion
It has been well established that 85% of the problems resultingfrom diabetic foot canbepresentedthrough spe-cialized care2,7,8,12,20,21 and that up to 50% ofamputations
and ulcerations can be presented through early diagnosis and appropriate treatment.1,17,18 Identification and
classi-fication of patients who are at risk (such as those with diabeticneuropathy,peripheralarterialdiseaseandstructural deformities),2earlyaggressivetreatmentandindividual,
fam-ilyandcommunityeducationformasolidbasisforpreventing limbamputation.22TheseactionsweretargetedinthePAID
diabeticfootoutpatientclinic.
Outofthe30patientswhoparticipatedinthestudy,90% presentedsometypeoflesioninatargetorgan(heart,kidney, retinaormicrovasculatureofthefeet),andthefrequencyof theselesionsremainedunchanged18monthslater(p=1.000). Thisshowsthatcaringforthewholepatientshouldformpart oftheapproach.23
After 18 months of follow-up at the PAID diabetic foot outpatient clinic, the perception regarding the full condi-tions of self-care of the feet (Table 1) varied from 73.3% atthe first evaluation to 40% at the second, and the per-ception regarding the capacity for partial self-care varied from23.3%to56.7%,whichindicatesthatasignificant num-ber of patients (p=0.004) perceived that they would need specializedfollow-upinordertoreceivetheappropriate pre-ventiveand/orcurativetreatment.Diabeticpatientswhodo notadheretotheirtreatmenthavea50-foldgreaterchanceof ulcerationofthefootanda20-foldgreaterchanceofhaving toundergoamputationthanthosewhofollowtheguidance correctly.24Onestudydemonstratedthat22outof23
ampu-tationsbelowthekneewereperformedonpatientswhohad neverreceivedanyinformationabouttherapeuticcareor pre-ventivemeasures.2
Atthe startofthe follow-up,46.7%ofthepatientswere using appropriate footwear. Eighteen months later, 83.3% were using appropriatefootwear (p=0.013) (Table 2). Inap-propriatefootwearpredisposesthefeet toextrinsictrauma and is considered to be a precipitating factor for ulcera-tion of the feet.25 Many studies have demonstrated that
when protective footwear is available, prevention of ulcer recurrenceisachievedin60–85%ofthepatients.2Theideal
footwear reduces the pressure on the feet to below the threshold for ulceration. Footwear and its insoles should be inspected frequently and exchanged when necessary. If the footwear that is habitually used cannot be adapted because oforthopedicdeformitiesor lesionsdue to exces-sivecontactarea,manufactureofspecialfootwearshouldbe indicated.5,8,11,13,21
After18 months, the rate ofmycosis between the toes hadreducedfrom46.7%to16.7%(p=0.012),nailmycosishad diminishedfrom63.3%to50%(p=0.125)andthecrackrate remainedat10%(Table2).Inonestudy,mycosisbetweenthe toeswasconsideredtoberesponsiblefor20.8%oftheulcers ofthefeet,onychomycosisfor52.5%,callusesandcracksfor 49.5%,driedandflakingskinfor63.4%and nailcleanliness and impropernail cuttingfor 73.3%.26 Basic hygiene
mea-sures such as properly washing the feet and drying them
carefully,usinghydratingcreamoroilandcuttingthenails properly and not excessively closely (tobe done by a chi-ropodist)avoidstheappearanceofthesetriggeringfactorsfor diabetic foot,and suchmeasuresare systematically imple-mentedatPAID.27
Intheinitialevaluation,13.3%ofthepatientshadahistory ofamputationand46.7%hadpreviouslyhadanulcer,which hadbeencured(Table2).Thisisahighnumberofpatientswith historiesofhighriskofamputationaccordingtotherisk clas-sificationoftheinternationaldiabeticfootconsensus.1Over
the18-monthfollow-up,thenumberofpatientswithactive ulcers decreased from four (13.3%)to three (10.0%), which demonstratesthattheobjectiveofpreventingtheappearance ofnewulcerswasachieved.Afterthese18months,itwasseen thatonlyoneamputationhadbeenperformed:thefourthtoe oftherightfootofonepatient(3.4%).Thus,thefinal evalu-ationshowedthatfivepatientshadhistoriesofamputation (16.7%).Thiswasanexcellentresult,incomparisonwiththe literature,inwhichamputationratesofaround43–85%have been reportedamongpatientsundergoingmultidisciplinary approaches.1,2,12
Inmakingthediagnosisofneuropathy,whichisan impor-tantriskfactorfordevelopmentofulcerationonthefeet,2,4–8
thecriteriaofMoreiraetal.19wereused(Tables3–5).AtPAID,
20% ofthe patients presented neuropathies (Table 5), and this proportion did notincrease over the 18-monthperiod (p=1.000).Thisfindingisimportant,giventhatwhen periph-eral neuropathy becomes established, it is irreversible.28,29
Therefore,itisimportantforindividualswitharecent diag-nosis to have adequate control over the risk factors, and for prophylaxisto beimplemented for individuals without risk factors, such as rigorous control over blood glucose levels, guidance regarding smoking and alcohol consump-tion,andcontroloverarterialhypertension,dyslipidemiaand vasculopathy.30
With the treatment implemented at PAID, significant improvements in the symptoms of peripheral neuropathy wereobserved(p=0.035)(Table4).Therewasadeclineinthe proportion ofpatientswith moderate tosevere symptoms, from 70% to36.7% over the18-month period.There wasa non-significantdecreaseinthenumberofpatientswithsigns ofdiabeticneuropathyatnormallevels,from 80%to63.3% (p=0.102)(Table3),whichshowsthatitwaseasiertoreverse thesymptoms(whichreflectanearlierstageofneuropathy) than the signs (whichrepresent amoreadvanced stageof neuropathy).19
Distalperfusionisanotherimportantriskfactorfor ulcer-ationandamputation.2,6,11–13 Overthe18-monthperiod,our
Conclusion
Creation of diabetic foot prevention and control programs within the primary and secondary healthcaresectors is a viableinvestment,givenitslowcost,inviewoftheimportant humanandsocioeconomicrepercussionsofthedisease.This hasapositiveimpactthroughnoticeablyimprovingpatients’ quality of life and reducing the vascular and neuropathic symptomsandoccurrencesofulcerationandamputation.
Funding
Pro-RectorateforResearch,FederalUniversityofJuizdeFora (PROPESQ).
Institutional Program for Scientific Initiation Bursaries (PIBICCNPq/UFJF).
Conflicts
of
interest
Theauthorsdeclarethattherewerenoconflictsofinterest.
r
e
f
e
r
e
n
c
e
s
1. InternationalConsensusontheDiabeticFootandPractical GuidelinesontheManagementandPreventionofthe DiabeticFoot.ConsultativeSectionoftheIDF;2007. 2. Brasil.GrupodetrabalhoInternacionalsobrePéDiabético.
Consensointernacionalsobrepédiabético.Brasília: MinistériodaSaúde;2001.
3. FagliaE,FavalesF,MorabitoA.Newulceration,newmajor amputation,andsurvivalratesindiabeticsubjects
hospitalizedforfootulcerationfrom1990to1993.DiabCare. 2001;24(1):78–83.
4. ArmstrongDG,NguyenHC,LaveryLA,vanSchieCH,Boulton AJ,HarklessLB.Off-loadingthediabeticfootwound:a randomizedclinicaltrial.DiabCare.2001;24(6):1019–22. 5. BoultonAJ,ArmstrongDG,AlbertSF,FrykbergRG,HellmanR,
KirkmanMS,etal.Comprehensivefootexaminationandrisk assessment:areportofthetaskforceofthefootcareinterest groupoftheAmericanDiabetesAssociation,with
endorsementbytheAmericanAssociationofClinical Endocrinologists.DiabCare.2008;31(8):1679–85.
6. KrishnanS,NashF,BakerN,FowlerD,RaymanG.Reduction indiabeticamputationsover11yearsinadefinedU.K. population:benefitsofmultidisciplinaryteamworkand continuousprospectiveaudit.DiabCare.2008;31(1):99–101. 7. NdipA,LaveryLA,LafontaineJ,RutterMK,VardhanA,
VileikyteL,etal.Highlevelsoffootulcerationand
amputationriskinamultiracialcohortofdiabeticpatientson dialysistherapy.DiabCare.2010;33(4):878–80.
8. RathurH,BoultonAJM.Theneuropathicdiabeticfoot.Nat ClinPractEndocrinolMetab.2007;3:14–25.
9. SinacoreDR.Acutecharcotarthropathyinpatientswith diabetesmellitus:healingtimesbyfootlocation.JDiab Complications.1998;12(5):287–93.
10.GarrowAP,BoultonAJ.Vibrationperceptionthreshold–a valuableassessmentofneuraldysfunctioninpeoplewith diabetes.DiabMetabResRev.2006;22(5):411–9.
11.GameFL,JeffcoateWJ.Primarilynon-surgicalmanagementof osteomyelitisofthefootindiabetes.Diabetologia.
2008;51(6):962–7.
12.JudeEB,EleftheriadouI,TentolourisN.Peripheralarterial diseaseindiabetes–areview.DiabMed.2010;27(1):4–14. 13.LipskyBA.Newdevelopmentsindiagnosingandtreating
diabeticfootinfections.DiabMetabResRev.2008;24Suppl. 1:S66–71.
14.LevinME.Footlesionsinpatientswithdiabetesmellitus. EndocrinolMetabClinNAm.1996;25(2):447–62.
15.LevinME.Patogeniaetratamentogeraldaslesõesdopéem pacientesdiabéticos.In:BowkerJO,PfeiferMA,editors.Levin O’Neal:opédiabético.6aed.RiodeJaneiro:Di-Livros;2002.p.
221–61.
16.BrodskyJW,SchneidlerC.Diabeticfootinfections.Orthop ClinNAm.1991;22(3):473–89.
17.ApelqvistJ,BakkerK,vanHoutumWH,SchaperNC, InternationalWorkingGroupontheDiabeticFoot(IWGDF) EditorialBoard.Practicalguidelinesonthemanagementand preventionofthediabeticfoot:basedupontheInternational ConsensusontheDiabeticFoot(2007)Preparedbythe InternationalWorkingGroupontheDiabeticFoot.DiabMetab ResRev.2008;24Suppl.1:S181–7.
18.LaveryLA,HigginsKR,LanctotDR,ConstantinidesGP, ZamoranoRG,AthanasiouKA,etal.Preventingdiabeticfoot ulcerrecurrenceinhigh-riskpatients:useoftemperature monitoringasaself-assessmenttool.DiabCare.
2007;30(1):14–20.
19.MoreiraRO,CastroAP,PapelbaumM,AppolinárioJC,Ellinger VC,CoutinhoWF,etal.TranslationintoPortugueseand assessmentofthereliabilityofascaleforthediagnosisof diabeticdistalpolyneuropathy.ArqBrasEndocrinolMetabol. 2005;49(6):944–50.
20.AbbottCA,CarringtonAL,AsheH,BathS,EveryLC,GriffithsJ, etal.TheNorth-Westdiabetesfootcarestudy:incidenceof andriskfactorsfornewdiabeticfootulcerationina community-basedpatientcohort.DiabMed. 2002;19(5):377–84.
21.SinghN,ArmstrongDG,LipskyBA.Preventingfootulcersin patientswithdiabetes.JAmMedAssoc.2005;293(2):217–28. 22.VanGilsCC,WheelerLA,MellstromM,BrintonEA,MasonS,
WheelerCG.Amputationpreventionbyvascularsurgeryand podiatrycollaborationinhigh-riskdiabeticandnondiabetic patients.Theoperationdesertfootexperience.DiabCare. 1999;22(5):678–83.
23.FarberDC,FarberJS.Office-basedscreening,prevention,and managementofdiabeticfootdisorders.PrimCare.
2007;34(4):873–85.
24.ArmstrongDG,HarklessLB.Outcomesofpreventativecarein adiabeticfootspecialtyclinic.JFootAnkleSurg.
1998;37(6):460–6.
25.AbbottCA,GarrowAP,CarringtonAL,MorrisJ,VanRossER, BoultonAJ.FootulcerriskislowerinSouth-Asianand African-CaribbeancomparedwithEuropeandiabeticpatients intheU.K.:theNorth-Westdiabetesfootcarestudy.Diab Care.2005;28(8):1869–75.
26.VigoKO,TorquatoMTCG,SilvérioIAS,QueirozFA,
De-La-Torre-Ugarte-GuaniloMC,PaceAE.Caracterizac¸ãode pessoascomdiabetesemunidadesdeatenc¸ãoprimáriae secundáriaemrelac¸ãoafatoresdesencadeantesdopé diabético.ActaPaulEnferm.2006;19(3):296–303. 27.Ochoa-VigoK,PaceAE.Pédiabético:estratégiaspara
prevenc¸ão.ActaPaulEnferm.2005;18(1):100–9. 28.BoikeAM,HallJO.Apracticalguideforexaminingand
treatingthediabeticfoot.CleveClinJMed.2002;69(4):342–8. 29.LiatisS,MarinouK,TentolourisN,PagoniS,KatsilambrosN.
Usefulnessofanewindicatortestforthediagnosisof peripheralandautonomicneuropathyinpatientswith diabetesmellitus.DiabMed.2007;24(12):1375–80.