The role of joint mobility in evaluating and monitoring the risk of diabetic foot ulcer

The

role

of

joint

mobility

in

evaluating

and

monitoring

the

risk

of

diabetic

foot

ulcer

Piergiorgio

Francia

*

,

Giuseppe

Seghieri

,

Massimo

Gulisano

,

Alessandra

De

Bellis

,

Sonia

Toni

,

Anna

Tedeschi

,

Roberto

Anichini

a

DepartmentofClinicalandExperimentalMedicine,UniversityofFlorence,Florence,Italy

b

TuscanyRegionalHealthAgency(ARS),Florence,Italy

c_{DiabetesUnit,USL3,St.JacopoHospital,Pistoia,Italy}

d_{DiabetesUnit,MeyerChildren’sHospital,Florence,Italy}

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received16December2014

Receivedinrevisedform

19February2015

Accepted3April2015

Availableonline15April2015

Keywords:

Diabeticfoot

Anklerangeofmotion

Limitedjointmobility

Footulcerriskscale

a

b

s

t

r

a

c

t

Aims:Evaluationofhowanklejointmobility(AJM)canbeusefulintheidentificationof

patientswithdiabetesatriskoffootulcer(FU).

Methods: Plantaranddorsalflexionoffootwereevaluatedusinganinclinometerin87

patients(54type2and33type1),and35healthysex-andage-matchedcontrolsubjects.

PatientswithdiabeteswerefollowedupfordiagnosisofFUoverthenext8yearsand

subsequently,patientsweresubdividedinto:thosewithoutahistoryofFU(18type1and

33type2),thosewhohadahistoryofFUdetectedbeforebaselineevaluation(14type2)

andthosewhohadhistoryoffirstulcerationdetectedbythe8thyearoftheevaluation

period(7type2).

Results: Aginganddiabetescausedasignificantreductioninmobilityofeachofthe

move-mentsinvestigated(p<0.001),whereasafteradjustingfortheconfoundingeffectofage,

diabetesspecificallyreducedplantarflexion(p<0.0001).AJM wassignificantlylowerin

thosewithhistoryofpreviousFUcomparedtoalltheothergroups(p<0.001).Thefirst

ulcerationwasdetectedinthesamefootpresentinglowerAJMin17ofthe22subjectswith

diabeteswithhistoryofulcer(77.27%).

Conclusions:Diabetes andagingreduce AJMalthough diabetesseemsto reduceplantar

flexiontoamorespecificextent.ReducedAJMismostlyassociatedwithaprevioushistoryof

FU.TheevaluationofAJMisavalidandreliableulcerriskscalethatindicateswhichfootisat

higherulcerrisk.

#_{2015ElsevierIrelandLtd.Allrightsreserved.}

*Correspondingauthorat:DepartmentofExperimentalandClinicalMedicine,UniversityofFlorence,LargoBrambilla,3,50134Florence,

Italy.Tel.:+390557944577;fax:+390557944586.

E-mailaddress:piergiorgiofrancia@libero.it(P.Francia).

ContentsavailableatScienceDirect

Diabetes

Research

and

Clinical

Practice

j o u r n a lh o m e p a g e :w w w . e l s e v i e r . c o m / l o c a t e / d i a b r e s

http://dx.doi.org/10.1016/j.diabres.2015.04.001

1.

Introduction

Diabeticfoot isone ofthe mostominouscomplications of

diabetes [1]. Neuropathy, vasculopathy, minor foot trauma

andfootdeformitiesareindividuallyoraltogetherthemain

etiological factors of diabetic foot ulcers. However, other

factors,suchaslimitedjointmobility(LJM)oftheankle,may

contributetothegenesisofdiabeticfootulcer[2–5].LJMisan

important riskfactor forplantar footulcer because it may

induceabnormaldistributionoffootplantarpressureinstatic

anddynamicconditions[5–9].

In particular, diabetes may exacerbate reduced joint

mobilitythattypicallyoccurs withaging[10–12]. Inclinical

practice, the effect of diabetes on joint mobility may be

difficulttopreventbecauseitcaninduceapainlessdeficitin

jointrangeofmotion(ROM)withaninsidiousonsetfollowed

by asymptomatic progressive deterioration [5,7,13]. At the

sametime,itiswellknownthatLJMcanoccurafewyears

afterdiagnosis,eveninyoungpatients[10,13–15].

IthasbeenreportedthatLJMincreasesinrelationtothe

diabeticperipheralneuropathylevelinpatientswithdiabetes

andisrelatedtotheincreaseinpeakplantarfootpressure,

integral pressure–time and shear forces [5–7,9,16,17]. The

significantcorrelationofLJMofthefirstmetatarso-phalangeal,

subtalarandanklejointsanddiabetesiswellknown[7,16,18].

Theoverallthickeningandstiffnessinthemaintendonsand

ligamentsofthefoot-anklecomplex,i.e.theplantarfasciaand

Achillestendons,caninfluencejointfunctionandlimitankle

ROMandfootjointmobility[19,20].Reduced jointROMcan

impairtheperformanceoflargemovementssuchasgaitin

subjects with diabetes. [8,9,21,22]. Ankle and

metatarso-phalangealLJMalterfootpropulsionandincreasetheloadat

themetatarsalheads[7,22].Theaccumulationofforefootloads

in orthostatic posture and during the whole stance phase

increasestheriskoftissuebreakdown[5–8,17,23].

SinceLJMandROMalterationscanbeevidentinsubjects

withdiabetespriortothedevelopmentofclinicalneuropathy

[7,9,24], it has been suggested for many years that the

assessmentofankleandfootjointmobilitycanhelptodefine

the risk of ulcer and to monitor a patient’s condition

[6,7,9,18,25–28].

Theaimofthisstudywastoverifyjointmobilitychanges

duringthelifetimeofpatientswithdiabetesandtouseankle

joint mobility (AJM) to monitor the risk of foot ulcer. In

addition,weinvestigatedthepresenceofadirectrelationship

betweenlimitedAJMandahigherriskoffootulcerinthesame

patient.

2.

Patients

and

methods

PatientsattendingtheSt.JacopoHospitalofPistoia,Italywere

consecutivelyrecruitedforevaluationofAJMinplantarand

dorsal flexion by means of an inclinometer.A total of 87

patientswithdiabetes,14youngand73adults,ofwhom54

type2and19type1,wereevaluatedandcomparedwith35

healthycontrolsubjects,ofwhom21wereadultsand14were

youths.Bothyounggroups(patientswithdiabetesandcontrol

subjects) ranged in age from 11 to 17 years. The detailed

clinicalcharacteristicsofthestudyparticipantsareshownin

Tables1and2.Exclusioncriteriawere:presenceofcurrent

foot ulcerat baseline,orthopedic and/orsurgical

complica-tionsor Charcotfoot.Datawerecollectedregardingtypeof

diabetes,diabetesduration,andpresenceofneuropathy.The

physicalexaminationincludedfootinspection,evaluationof

neuropathybymeansofvibrationperceptionthreshold(VPT),

10 GSemmensWeinsteinmonofilament, andevaluation of

patellar and ankle reflexes. Evaluation of vasculopathy

includeddeterminationofperipheralpulsesand

transcutane-ousoxygentension(TcpO2).HemoglobinA1cwasmeasuredat

baselineby highperformance liquidchromatographyHPLC

method. Weight, height and body mass index (BMI) were

measured. BMIwasexpressedasbody weightinkilograms

dividedbyheightinmeterssquared(kg/m2_{).Whenpatients}

had foot ulcers in thepast or duringfollow-up, theywere

gradedaccordingtotheUniversityofTexasWound

Classifi-cationSystem[29].

Patientswithdiabeteswerefollowedupfromthediagnosis

offootulcerandfor8yearsthereafter.Theadultgroupwas

Table1–Maincharacteristicsanddorsal,plantarandtotalAJM(expressedasdegrees)intype1patientswithdiabetes

comparedtoage-andsex-matchedcontrols.

Controls Type1diabetesmellituspatients p-Value*

Youths(n=14) Adults(n=21) Youths(n=14) Adults(n=19)

Age(yrs) 14.41.8 61.34.7 14.11.0 52.112.8 <0.0001

Diabetesduration(yrs) – – 6.14.6a 26.511.0b <0.0001

Gender(M/F) 6/8 10/11 7/7 10/9

HbA1c(%–mmol/mol) – – 7.20.7to566a 8.31.4to6711.b <0.02

BMI(kg/m2_{) 21.52.7a 26.63.7b 20.42.5a 28.13.5b <0.0001}

Neuropathyatbaselineno.(%) – – 0 6(31) –

Plantarflexion(8–degree) 38.54.2a 37.67.4 28.05.6b 32.79.8 <0.0005

Dorsalflexion(8) 114.410.8a 94.518.1a 91.212.3b 76.722.8b <0.0001

TotalAJM(8) 152.913.2a 131.619.2a 120.815.3b 109.427.3b <0.0001

DRight–left(8) 2.71.9 6.54.3 5.03.7 5.86.3 NS

ValuesaremeanSD.

* _{Byone-wayANOVA.}

subdivided into: patients without history of foot ulcer (18

adults with T1DM,and 33 adults withtype2 diabetes),14

patientswithtype2diabeteshadhistoryoffootulcerdetected

beforebaselineevaluationand7adultswithtype2diabetes

hadhistoryoffirstulcerationdetectedbythe8thyearofthe

evaluationperiod.Onlyonepatientwithtype1diabeteshad

thefirstulcerationduringthefollow-upperiod.Ninepatients

with prior history of ulcer had digital ulcers, three had

metatarsalandtwohadplantarheelulcers.Ofthosepatients

whodevelopedulcersatfollow-up,fivehaddigitalulcers,one

hadmetatarsalandonehadheelulcer.

2.1. Determinationofjointmobility

AJM was evaluated using an inclinometer (Fabrication

Enterprises Inc, White Plains, NY, USA) [30–32] with the

patientlyingsupine,thesubtalarjointinneutralpositionand

thefeetovertheedgeofthebed.Theknee,correspondingto

theevaluatedankle,wasextendedandputoverarigid5-cm

high support. The maximum range of dorsal and plantar

flexionwasdeterminedafterdrawingwiththedemographic

penthefifthmetatarsalboneandpositioningtheinclinometer

alongthediaphysisofthebone,withoneextremityputonthe

distal condylus. All measurements were performedby the

same observer, recording the mean of three consecutive

readings.

All participants and parentsor guardians of the young

subjectswereinformed ofthepurpose ofthestudyandits

experimentalprocedures beforeobtainingwritteninformed

consent and enrollment in the study. The protocol and

consent form were approved by the Ethics committees of

thelocalHealthAreaUnitofPistoiaHospital.Thestudywas

performedinaccordancewiththedeclarationofHelsinki.

2.2. Statisticalanalysis

DatawerereportedasmeanSDorpercentage,as

appropri-ate. ROMvalueswereexpressedindegree andreported as

meanSD.Comparisonsbetweengroupswereanalyzedby

ANOVA,usingtheBonferronicorrectionformultiple

compar-isons. Comparisons between frequencies were performed

using the Chi-square method. Multiple regression analysis

was performed using the presence of foot ulcer as the

dependentvariableand all variableswhich appeared tobe

significantlycorrelatedwithfoot ulcerationasconfounding

factorsforunivariateanalysis.Atwo-tailedpvalueof<0.05

wasregardedasstatisticallysignificant.Allcalculationswere

performedusingtheSPSSsystemforWindowsVersion16.0

(SPSSInc.,Chicago,IL,USA).

3.

Results

AsshowninTable1,inyoungandadultpatientswithtype1

diabetes, total AJM and dorsal flexion were significantly

higherthaninrespectivecontrolswhileplantarflexionwas

not significantly different between adult groups. Plantar,

dorsalandtotalAJMweresignificantlyreducedinpatients

with type 2 diabetes (Table 2). Analysis of data about

development offootulceratfollow-updemonstratedthat,

whencomparedtomatchedcontrols,thereductioninplantar

flexion and total AJM were evident in patients with no

ulceration, thosewith footulcerandthosewithhistoryof

previousulcerationatbaseline(Table3).Dorsalflexionwas

reduced in those who developed foot ulcer by the 8-year

followupandinthosewithhistoryofpreviousfootulcer,with

these latter havingthe most evident reductionin plantar

flexion(Table3).NodifferenceswerenotedastoD–right–left

difference.

Sinceageandbodyweighthad,asexpected,amajoreffect

onreductionofplantaranddorsalflexionaswellasontotal

AJM,weperformedamultivariateanalysiswithanklejoint

mobilityasdependentvariableandage,presenceofdiabetes,

sexandBMIascovariatesinbothtype1andtype2patients

with diabetesand in controls.From thisanalysis, diabetes

remained significantly associated with dorsal, plantar and

totalAJMreductioninbothtypesofdiabetes.Femalegender

was associated with a significant reduction in both dorsal

flexion and total AJM, while age was not significantly

associatedwithaplantarflexiondecreaseineithergroupof

diabeticpatients,afteradjustingforbodyweight(Table4).

Finally,consideringthewholecohortofdiabeticpatients

(type 1and type2),age was theonlyvariable significantly

associated(p<0.001)withreductionofdorsal,plantarflexion

and total AJM, in a model with BMI, Hba1c and diabetes

durationasothercovariates(datanotshown).

4.

Discussion

Theetiopathogenesis ofLJM indiabeteshasnotbeen fully

explained,althoughthemaincausalfactorseemstobethe

effectofmetabolicdisordersontheincreasedstiffnessofskin,

jointcapsule,ligamentsandtendons[13,33].

Table2–Dorsal,plantarandtotalAJM(expressedasdegrees)incontrolsandintype2diabetesmellituspatients.

Controls(n=21) Type2diabetesmellituspatients(n=54) p-Value

Age(yrs) 61.34.7 63.76.6 NS

Diabetesduration(yr) – 14.29.6 –

Gender(M/F) 10/11 30/24 –

HbA1c(%–mmol/mol) – 7.71.1to619 –

BMI(kg/m2_{) 26.6}

3.7 28.74.3 <0.05

NeuropathyatbaselineNo.(%) – 25(46) –

Plantarflexion(8–degree) 37.67.4 25.710 <0.001

Dorsalflexion(8) 94.518.1 73.321.4 <0.001

TotalAJM(8) 131.619.2 99.026.0 <0.001

The main biochemical abnormality in joint tissue of

diabeticpatientsistheexcessofnon-enzymaticglycosylation

of collagen, with production of advanced glycation and

products(AGEs),whichinturnleadtoanincreaseincollagen

cross-links.Theincreaseininter-andintra-molecular

cross-linking of collagen fibers alters, in turn, the mechanical

propertiesofthesetissueswithadecrease inelasticityand

tensilestrength,causingmechanicalstiffness[13,34,35].

As amatter offact,a deficitofAJM isoftenpresent in

subjects with diabetes, even without clinically relevant

complications,whoarematchedforageandcomparedwith

healthycontrols[5,7,9].Atthesametimeitiswellknownthat

jointmobilitydecreasesasindividualsgrowolder[12].Thus,

the reduction of AJMin olderpatients, when comparedto

young healthysubjects, is the resultof at leasttwo main

factors:aginganddiabetes[12,13,36].

To verify the joint mobility changes over time in a

populationwithdiabetesandtodefinehowAJMcanbeuseful

inthemonitoringoffootulcerriskwehavestudiedacohortof

87patientswithdiabetesandmonitoredtheoccurrenceoffoot

ulcers overthe next8years.Thepopulationwithdiabetes,

both youths and adults, had significantly reduced AJM in

flexion–extension compared to healthy, age-matched

sub-jects.

Acomparisonofalladultswithdiabeteswithage-matched

healthyadultsshowsthatthepopulationwithdiabeteshasa

strong and significant AJM reduction in each movement

evaluated.

Nonetheless, the young subjects with diabetes have

significantly reduced mobility of each of the movements

investigatedwhencomparedtotheyoungcontrolgroup.This

result suggests that diabetes, even in young people, has

important negative effects on AJM, and indicates that

although the proper management of young patients with

type 1 diabetes can be difficult, it is important for the

preventionofchroniccomplicationsofthedisease.

Further-more,femalepatientswithtype1diabetesaremoreinclined

to impairment in both dorsal and total AJM than males,

probablyduetotheothergenderriskfactorssuchaswomen’s

tendencytowearhigh-heeledshoes.Themethodweusedin

thisstudyindicatesthatagingparticularlyaffectsankledorsal

Table3–Maincharacteristicsanddorsal,plantarandtotalAJM(expressedasdegrees)intype2diabeticpatients

comparedtoage-andsex-matchedcontrols.FU:follow-upperiod.

Controls(n=21) Type2diabetesmellituspatients(n=54) p-Value

Nofootulceration (n=33) Footulcerationat finalFU(n=7) Historyofprevious ulceration(n=14) Age(yrs) 61.34.7 62.55.8 65.36.6 65.58.3 NS Gender(M/F) 10/11 17/16 4/3 9/5 –

Diabetesduration(yr) – 12.98.1a 22.412.5b 13.410.0 <0.04

HbA1c(%–mmol/mol) – 7.61.1to599 7.91.2to6310 7.91.3to6311 NS

BMI(kg/m2_{) 26.6}

3.7 29.34.5a 25.52.4b 28.84.1 <0.04

Neuropathyatbaselineno.(%) – 9(27)a 4(57) 12(86)b* _<0.001

Plantarflexion(8–degree) 37.67.4a 27.111.0b 26.97.3b 21.77.7b <0.0001

Dorsalflexion(8) 94.518.1a 80.821.4d 66.710.4b 58.917.5b,c <0.0001

TotalAJM(8) 131.619.2a 107.926.1b,d 93.69.3b 80.621.1b,c <0.0001

DRight/left(8) 6.64.3 5.46.0 8.85.7 7.96.4 NS

avs.b;cvs.d:p<0.001. * _{ByChi-squaremethod.}

Table4–Multivariateanalysisconsideringdorsiflexion,

plantarflexionandtotalAJM(expressedasdegrees)as

dependentvariablesandage,BMI,diabetesandsexas

independentvariablesintype1(a)ortype2(b)patients

withdiabetes.

b-Regression coefficient

p-Value p-Model

(a)

Ankledorsalflexion

Intercept 97.46 0.0001 0.0001

Age 0.48 0.0001

Diabetes(Y/N) 21.22 0.0001

BMI 0.28 NS

Sex 12.14 0.002

Ankleplantarflexion

Intrercept 33.66 0.0001 0.012 Age 0.02 NS Diabetes(Y/N) 7.14 0.0005 BMI 0.17 NS Sex 0.52 NS TotalAJM Intercept 134.89 0.0001 0.0001 Age 0.49 0.0006 Diabetes(Y/N) 27.28 0.0001 BMI 0.26 NS Sex 12.86 0.005 (b)

Ankledorsalflexion

Intercept 135.04 0.0002 0.0008

Age 0.77 0.05

Diabetes(Y/N) 19.25 0.0008

BMI 0.07 NS

Sex 3.28 NS

Ankleplantarflexion

Intercept 16.73 NS 0.0001 Age 0.16 NS Diabetes(Y/N) 13.54 0.0001 BMI 0.53 NS Sex 1.95 NS TotalAJM Intercept 152.11 0.0003 0.0001 Age 0.61 NS Diabetes(Y/N) 32.30 0.0001 BMI 0.58 NS Sex 1.12 NS

flexionincomparisonwithankleplantarflexion,whichwas

significantlyassociatedonlywithdiabetes.

Inaddition,withinthetype2diabeticgroup,plantarflexion

wassignificantlylowerinpatientswithtype2diabetesthanin

thosewithtype1.Thisresultmayfurtherreinforcethefinding

thatdiabetes,evenifithasalateronset,inducesamoresevere

deficitofplantarflexion mobilitywhichmaybeduetothe

simultaneousshorteningoftheAchillestendonand

thicken-ingoftheplantarfascia,bothofwhicharepresentindiabetes

[37]. In other words, diabetes would primarily cause the

knownalterationsintheconnectivetissue,i.e.,oftheAchilles

tendon and plantarfascia, which seem to act together in

alteringfootloadingandultimatelyinducingthetypicalfoot

postureinplantarflexion[38,39].

Otherthantoverifythepresenceofatypicalnegativetrend

inAJMinthepopulationwithdiabetes,afurtheraimofthis

studywastoevaluatethepresenceofmobilityvaluescritical

tofootulcerrisk.Ourresults,inpatientswithhistoryoffoot

ulcerdetectedbeforeorafterbaselineevaluation,showthat

AJM decreases in the population at high risk of ulcer.

Nonetheless,thegroupwhich developedfoot ulceration,in

contrastwiththosewhodidnot,hadsignificantlyreducedAJM

indorsalflexioncomparedtothenon-diabeticadultcontrol

group.ThisresultsuggeststhatAJMreductionindorsalflexion

couldbeconsideredasanadditional indicatoroffootulcer

risk. Plantar flexion mobility rather than dorsiflexion was

alreadystronglyreduced,eveninelderlydiabeticpatientswho

didnotdevelopanulceroverthenext8years,confirmingthe

strongrelationshipofthisparametertodiabetes.Thepossible

negative effect on reduced AJM possibly exerted by prior

immobilization or offloading maneuvers in patients with

previousfootulcer,canbeexcludedbythesimilarDright–left

differencesinAJMobservedinallpatients’groups,indicating

that any impairment in AJM was bilaterally uniform (see

Table3).

Theresultsofthisstudyindicate,moreover,thatthereisa

significantmobilitydifferenceindorsalandtotalankleflexion

betweenpatientswithtype2diabeteswithahistoryofulcer

and thosewithout. Ahistory ofpreviousfoot ulcerationis

associatedwithanevenhigherreductioninplantaranddorsal

mobility,comparedwiththosewhowilldevelopanulcerin

the next 8 years afterthe measurement. This suggests an

earlierimpairmentinAJMamongthosewithpasthistoryof

footulceration.Itisinterestingtonotethatprevioushistoryof

footulcerationisassociatedwiththehighestrateofperipheral

neuropathy.Thesmallnumberofpatientsinourstudydidnot

allowustodrawplausiblecorrelationsbetweenthelocationof

ulcersdevelopedatfollow-upandthetypeofreductioninAJM.

Peripheralneuropathywaspresentonlyinadultpatients,

independentlyofthetypeofdiabetes,and mostlyinthose

with previous history of foot ulcers, suggesting that it is

stronglyassociatedwithlimitedLJM.Inthetotalpopulation,

25of54patientswithtype2diabetes(46.3%)hadneuropathy

at baseline according to described criteria. This is not so

different from the expected rate [39–41]. The prevalence

increasedto57%inthegroupofpatientswhodevelopedfoot

ulcers and to86% inthose withprevious foot ulcer, from

baseline. The relatively low prevalence of neuropathy at

baselineinpatientswholaterdevelopedfootulcer,compared

tothosewhohadpreviouslyexperiencedit,canbeexplained

bythefactthatthedetrimentaleffectofAJMreductionaswell

asofmusclestrengthabnormalitiescanoccurevenbeforethe

appearanceofclinicalneuropathy[9,42,43].

In this study, aging seems to affect the difference in

mobility between the two ankles as evidenced by the

significant difference in young and elderly non-diabetic

subjects,whilediabetesdoesnotseemtohaveasimportant

aneffect.Thisdoesnotmeanthatthedifferentjointmobility

between the twoankles is aless interesting parameter. In

agreementwithMueller’s[6]retrospectiveanalysis,17outof

22ofourcases(77.27%)withahistoryofulcerationandwho

hadasubsequentfootulcer,hadthefirstepisodeinthesame

foot withlowerAJM.Forthisreason,anevaluationofjoint

mobilitydifferencebetweenthetwoanklesinasinglepatient

mayhelptoindicatewhichfootisathigherrisk.

4.1. Limitationsandstrengthsofthestudy

Ourstudyhassomelimitations:AJMwasdeterminedwitha

uniquemethodwithoutusingothermethodologicalimaging

approacheswhichareusefulforexcludingtheoccurrenceof

possibleconcomitantjointpathologies.Inaddition,ourstudy

hasthelimitationofbeingobservationalandnotdesignedina

time-course manner.Inspiteoftheselimitations,however,

ourstudyhassomeimportantstrengths:itcoversa

popula-tionofpatientswithbothtype1andtype2diabetes.Finally,

ourpatientsarewellmatchedastosexandageandwehave

followedthem upfor8years,whichisarelativelylengthy

time.

5.

Conclusion

Anklejointmobilityinflexion–extensionissignificantlylower

in adult and young patientswith diabetesthan in healthy

controls.Diabetesseemstoaffectparticularlyankleplantar

flexion whiledorsal flexionseemstobemostlyaffectedby

aging.Withinthediabeticpopulationinvestigated,anklejoint

mobility decreases as the risk of ulceration increases:

however,thegroupathighestriskseemstobethosewitha

history of previousfootulceration, indicatingthat reduced

AJMrepresentsanearlyriskfactoroffootulceration,atleastin

people withtype2diabetesmellitus. Allthis suggeststhat

ankle joint mobility is a useful indicator for monitoring

ulcerativeriskinpatientswithdiabetes,otherthanbeingable

to indicate which foot is at higher ulcerative risk. In

conclusion, measuring AJM should be performed early in

individualswithdiabetes.

Conflict

of

interest

None.

Acknowledgements

The authors thanks Mrs G. Iannone for technical and

administrative support and Mary Forrest for revising the

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