ORIGINAL ARTICLE

Diabetic peripheral neuropathy in ankles and feet: musclestrength and plantar pressure

Andréa Jeanne Lourenço Nozabieli & Alessandra Rezende Martinelli &Marcela Regina de Camargo & Ana Cláudia de Souza FortalezaCláudia Regina Sgobbi de Faria & Cristina Elena Prado Teles Fregonesi

Received: 26 August 2011 /Accepted: 30 August 2013# Research Society for Study of Diabetes in India 2013

Abstract This study aims to evaluate and correlate the vascu-lar, sensory andmotor components related to the plantar surfacein individuals with diabetic peripheral neuropathy. 68 patientswere categorized into two groups: 28 in the neuropathic groupand 40 in the control group. In each patient, we assessed:circulation and peripheral perfusion of the lower limbs; somato-sensory sensitivity; ankle muscle strength; and pressure on theplantar surface in static, dynamic and gait states. We used theMann–Whitney test and analysis of variance (ANOVA andMANOVA) for comparison between groups, and performedPearson and Spearman linear correlations amongst the variables(P <0.05). The somatosensory sensitivity, peripheral circulationand ankle muscle strength were reduced in the neuropathicgroup. In full peak plantar pressures, no differences were seenbetween groups, but differences did appear when the foot

surface was divided into regions (forefoot, midfoot andhindfoot). In the static condition, the plantar surface area wasgreater in the neuropathic group. In the dynamic state, peakpressures in the neuropathic group, were higher in the forefootand lower in the hindfoot, as well as lower in the hindfootduring gait. There were positive or negative correlations be-tween the sensitivity deficit, dorsal ankle flexor strength, plantarsurface area, and peak pressure by plantar region. The sensitiv-ity deficit contributed to the increased plantar surface area.

Keywords Diabetes mellitus . Diabetic neuropathies .

Diabetic foot . Diabetic vascular diseases . Plantar ulcer

Introduction

Diabetes Mellitus (DM), a serious public health problem,leads to peripheral disorders including sensory, motor, au-tonomic and circulatory deficits [1–3].

Sensory loss leads to a gradual loss of sensitivity to pain,as well as loss of perception of plantar pressure, tempera-ture and proprioception [4]. The motor loss contributes toatrophy and weakness of the intrinsic muscles of the feet,structural alterations, deformities and to gait pattern alter-ations [5, 6]. The autonomic loss reduces sweating in thefeet, making them dry and prone to cracks and fissures [7].

Diabetic neuropathy, and the associated peripheral vas-cular diseases in the lower limbs, results in diabetic footsyndrome, characterized by the occurrence of acute orchronic injuries in the feet, high susceptibility to infection,and ulceration and destruction of deep tissues [1, 8]. Al-though diabetic foot syndrome is a primary factor in plantarulcer formation, a mechanical or physical trigger represent-ed by high pressures, precedes ulceration.

Neuropathic and vascular changes resulting from diabet-ic foot syndrome are well described [4, 6, 9–11]. However,it is still unclear how such changes interrelate and which

A. J. Lourenço Nozabieli :A. Rezende Martinelli :M. R. de Camargo :A. C. de Souza Fortaleza :C. R. Sgobbi de Faria :C. E. Prado Teles FregonesiLaboratory of Clinical Studies in Physical Therapy,Department of Physical Therapy, School of Sciencesand Technology (LECFisio), Sao Paulo State University,Rua Roberto Simonsen, 305,Presidente Prudente, SP, Brazil CEP 19060-900

A. J. Lourenço Nozabielie-mail: andrea_noza@hotmail.com

A. Rezende Martinellie-mail: lerezendemartinelli@yahoo.com.br

M. R. de Camargoe-mail: marcelarcamargo@gmail.com

A. C. de Souza Fortalezae-mail: anaclaudiafisiouel@yahoo.com.br

C. R. Sgobbi de Fariae-mail: claudiasgfaria@gmail.com

C. E. Prado Teles Fregonesi (*)Department of Physical Therapy, Rua Roberto Simonsen, 305,Presidente Prudente, SP, Brazil 19060-900e-mail: cristina@fct.unesp.br

Int J Diabetes Dev CtriesDOI 10.1007/s13410-013-0148-9

contributes more to the development of areas of pressureand ulcers. The major factor responsible for ulcers is theloss of protection sensation, with vascular diseases could beassociated with 25–30 % of such cases [12], ankle muscleweakness [13] and other factors [14].

The goals of the study were to evaluate the plantar surfaceand pressures, and the vascular, sensory and motor componentsin patients with DM and to verify if alterations found inpressure and plantar surfaces were related to these components.

Methods

Sixty-eight volunteers were allocated to two groups: 28 (14men and 14women) with peripheral diabetic neuropathy (DNGgroup) and 40 non-diabetics (14 men and 26 women) in thecontrol group (CG).

To confirm the diagnosis of peripheral neuropathy, we useda Michigan Neuropathy Screening Instrument (MNSI) [15,16]. We excluded individuals with osteoarticular deformities,plantar ulcers, lower limb amputation, walking aid devices,diagnosis of any neurological disease affecting gait parameters,significant uncorrected visual deficit, age over 75 years, pres-ence of morbid obesity and inability to comprehend the tests.

The sudy was done at the Laboratory of Clinical Studiesin Physical therapy (LECFisio), in the Department of Phys-ical therapy of the School of Science and Technology(FCT), Sao Paulo State University (UNESP) – PresidentePrudente, Brazil. The study met the Criteria of Ethics inHuman Research, according to Resolution 196/96 of theNational Health Council, and was approved by the EthicsCommittee of the FCT/UNESP (Case No. 22/2009).

Evaluation of somatosensory sensitivity was performedusing Semmes-Weinstein monofilaments (Sorri Bauru®,Bauru, Brazil) producing stimuli of intensities ranging from0.05 to 300 g.We applied the monofilaments to the skin alongthe sensory dermatomes of the anterior tibial and fibularnerves in 11 predetermined areas on each foot. We coveredeach patient’s eyes during the test and instructed patients toverbally express when they felt the monofilament touchingtheir skin [1, 17]. The test was graded on a point scale frominsensitive to the 10 g monofilament or greater. We comparedeach patient’s response to the overall response [17, 18].

We used the ankle/arm brachial pressure index (ABPI) toevaluate the peripheral circulation. This test provides informa-tion on the peripheral circulation of the lower limbs by mea-suring the segmental pressures at each end with results com-pared among limbs [1, 8, 19]. Patients were supine with 5 minrest prior to each measurement. We recorded three separatevalues for the brachial artery systolic pressure (proximal pres-sure) and posterior tibial pressure (distal pressure) in right andleft limbs using a Doppler DV-2001 (MEDPEJ®, RibeiraoPreto, Brazil) and sphygmomanometer (Becton-DickinsonTM,

Bergen County, USA). ABPI was defined as the quotientbetween the systolic pressure of the greater brachial value andthe systolic pressure of the ankle. Values less than 0.90 indicat-ed peripheral obstructive arterial disease [1, 19, 20].

We assessed blood perfusion using a finger oximeter (Onyx®,Nonim Medical, Plymouth, USA). Patients remained supine for5 min. Oxygen saturation was collected in the hallux of both feetand the results were compared to the average values of the indexfingers from both hands. The oximetry of the hallux was con-sidered abnormal when the oxygen saturationwas lower than theindex finger by more than two percentage points [19, 21].

We measured ankle isometric muscle strength using aportable reversible digital dynamometer, model DD–300(Instrutherm®, Sao Paulo, Brazil), connected to an adapterdeveloped by a local laboratory (LECFisio) [22]. The adaptedtable consisted of two levels. The upper level had two holeswhere a steel cable entered and left, forming a ledge. First, themetatarsophalangeal region, and then, the distal extremity ofthe thigh, was positioned over the ledge to evaluate the dorsalankle flexor and plantar flexor muscle groups, respectively. Thecable was fixed at one end to a load cell and at the other end to acrank with locks, both attached to the lower floor of the adapter,allowing a perfect adjustment. Tomeasure the isometric musclestrength of the dorsal ankle flexor group, patients applied forceagainst the steel cable to try to remove the forefoot from thetable adapter. Likewise, when measuring the strength of theplantar flexor muscle group, patients applied force against thesteel cable, trying to remove the heel from the table. During thetest, patients received ischial support and maintained 90° flex-ion of the hip, knee and ankle.We repeatedmeasurements threetimes for each muscle group with a 30 s gap between measure-ments. Measurements were averaged [22].

We assessed full peak pressure and peak pressure by area(forefoot, midfoot and hindfoot; predefined by the software,

Fig. 1 Division of the foot by region (according to the softwareFootwork Pro, version 3.2.0.1) a Forefoot; b Midfoot; c Hindfoot

Int J Diabetes Dev Ctries

Fig. 1) and plantar surface area in static, dynamic and gaitconditions using an electronic baropodometer (FootWalkPro, AM CUBE, Paris, France). The baropodometer was2 m in length and adapted to a walking trail 8 m long,allowing patients to speed-up or slowdown in the first andlast 3 m [23]. Analyses were performed using the software,Footwork Pro, version 3.2.0.1. In the static assessment,individuals remained in the orthostatic position over theactive surface of the baropodometer with bipedal supportfor 30 s looking at an imaginary spot in front of them [24]and a free support base. This condition was recorded threetimes for each individual, with a 1 min rest interval. For thedynamic evaluation, the individual was asked to deliberate-ly step on the baropodometer, first with the right foot andthen with the left foot, three consecutive times. In the gaitevaluation, each individual walked freely across the 8 mtrail at a comfortable speed three consecutive times withoutworrying about synchronizing the step on the baropodometer.Data acquisition occurred only in the active surface region(2 intermediate meters). Each patient walked the route threetimes. We used the average of the values generated in theplatform.

All individuals went through a period of adaptation to theequipment prior to the data collection, minimizing the effectof non-familiarity with the environment. Before starting theassessment, each individual stood still on the baropodometerfor calibration.

All tests were performed by the same observer using stan-dard guidelines and verbal commands. After the evaluation ofpressures and plantar surfaces in static, dynamic and gaitstates, the region corresponding to the highest peak pressureindicated the plantar region suffering the greatest mechanicalstress. For this purpose, we divided the foot into three regions:forefoot, midfoot and hindfoot (as generated by the software).

In order to verify possible differences among groups, weperformed variance tests of normality and homogeneity. Initial-ly, we used descriptive statistics (measures of central tendencyand variability). For ordinal variables, such as somatosensorysensitivity, ABPI and blood perfusion, we used the Mann–Whitney test. We used multivariate analysis (MANOVA) toinvestigate the differences in muscle strength, maximum pres-sures and plantar surfaces. The factors usedwere group, gender,and side, with side treated as a repeated measure. All assump-tions for the use of these analyses were fulfilled and, whennecessary, univariate tests (ANOVA) were used to determinedifferences in the respective variables.

We used Spearman’s and Pearson’s tests for linear correla-tion between the vascular, sensory and motor components,pressures, and plantar surfaces, in order to verify the degree ofassociation between these variables. Finally, linear regressionanalysis was performed to identify if the vascular, sensory, andmotor variables could predict the variance of the evaluatedcomponents.

In all analyses, the significance level was kept at 0.05and the software used for statistical analyses was SPSS(Statistical Package for Social Sciences, version 17.0).

Results

Patient characteristics (Table 1) showed differences in theBMI between the two groups due to greater body weight inneuropathic patients.

Among the groups, the Mann–Whitney test showed differ-ences for somatosensory sensitivity (U =416.00, P <0.001) asevidenced by insensitivity to the 10 g monofilament in allindividuals in the neuropathy group. More patients had ABPI<0.90 for both sides in DNG (U =411.00, P <0.001) with nodifferences in blood perfusion (U =20.00, P=0.089).

For the variables referring to the ankle’s muscle isometricstrength, MANOVA showed differences among the groups(Wilks’ lambda=0.74; F(2,47)=11.08 P <0.001), genders(Wilks’ lambda=0.65, F(2,47)=16.48; P <0.001) and side(Wilks’ lambda=0.76; F(2,47)=9.76; P <0.001) and interac-tion between side and group (Wilks’ lambda=0.85; F(2,47)=5.32; P <0.001). Univariate analyses revealed that the rightside was stronger for both muscle groups: dorsal flexorsF(1,48)=13.88 (P <0.001) and plantar flexors F(1,48)=8.55(P=0.004). There was interaction between groups and sidesfor both muscle groups: dorsal flexors F(1,48)=7.25 (P=0.009) and plantar flexors F(1,48)=4.98 (P=0.029) (Table 2).

For the plantar surface area, MANOVA revealed no differ-ence between groups for the dynamic conditions (Wilks’lambda=0.92, F(2,47)=2.68, P =0.076) and gait (Wilks’lambda=0.90; F(2,47)=0.53, P=0.207), but showed the larg-est static plantar area in the neuropathic group (Wilks’ lamb-da=0.87, F(2,47)=−4.41, P <0.001) (Table 3). Univariateanalysis revealed no difference for side (F(1,48)=0.28, P=0.228) or gender (F(1,48)=1.32, P=0.241), but showed agreater contact surface area for the neuropathy group(F(1,48)=13.52, P <0.001).

For maximum values of peak plantar pressure (kgf/cm2),MANOVA revealed no difference between groups, gender,

Table 1 Patient characteristics (Mean ± Standard Deviation)

Variables CG DNG P-values

Age (years) 65.53±6.19 62.00±4.73 0.502

BMI (kg/m2) 26.5±3.51 29.54±4.76 <0.001

Weight (kg) 69.40±12.56 79.94±13.97 0.002

Height (m) 1.63±0.10 1.65±0.10 0.425

Shoe Size (cm) 25.04±3.52 25.68±3.62 0.643

Post mealglucose (mg/dL)

115.83±14.60 184.14±80.56 <0.001

CG Control Group, DNG Neuropathic Group, N =68

Int J Diabetes Dev Ctries

or interaction between group and gender, in any condition:static (Wilks’ lambda=0.99, F(2,47)=0.33, P=0.624), dy-namic (Wilks’ lambda=0.98, F(2,47)=0.73, P=0.304) andgait (Wilks’ lambda=0.90, F(2,47)=0.53; P=0.384). How-ever, when the feet were divided into three regions (fore-foot, midfoot and hindfoot), there were no differences be-tween gender and side (Wilks’ lambda=0.81, F(2,47)=1.37, P=0.409 and Wilks’ lambda=0.84, F(2,47)=1.34,P=0.152), respectively. Between groups, the peak pressurewas higher (Wilks’ lambda=0.74, F(2,47)=2.54, P=0.04).

Because MANOVA revealed no differences betweengender and side, we performed ANOVA with only onefactor (group) to compare differences in peak plantar pres-sure, in static, dynamic and walking conditions by pedalregions, as mentioned above (Table 4).

The correlation between ABPI and blood perfusion wasmoderately positive for both lower limbs (left: r =0.56, P <0.001; right: r =0.52, P <0.001), showing that the lower theABPI, the lower the oximetry value.

The degree of somatic insensitivity showed moderate cor-relation to the plantar surface in the static condition in bothfeet (right: r =0.49, P <0.001; left: r =0.49, P <0.001), i.e., thehigher the somatosensory deficit, the higher the foot contact

with the ground. There was no correlation between somaticinsensitivity and the peak plantar pressure, but when this wascorrelated with the regions where the pressure was higher,significant correlations occurred. In the dynamic conditionand gait there were correlations for the forefoot region (r =0.39; P <0.001, r =0.27; P=0.04) and the hindfoot region (r =−0.37; P=0.002, r =−0.32; P=0.011). In other words, thegreater the deficit in the somatosensory sensitivity, the higherthe peak pressure in the forefoot in dynamic conditions andgait. And yet, the greater the deficit of somatosensory sensi-tivity, the lower the peak pressure in the hindfoot in thedynamic conditions or gait.

The strength of the dorsal flexors correlated with thepressures in the static condition in the forefoot (r =0.25;P=0.05) and hind foot (r =−0.31; P=0.05) and, duringgait, in the forefoot (r =0.29; P=0.03). Thus, the weaker

Table 2 Mean ± Standard De-viation of ankle isometricstrength (kgf) of the right andleft dorsal flexor and plantarflexor groups for both gendersin each group

CG Control Group, DNG Neu-ropathy Group, N =68

Muscle group Factors P-values

Dorsal flexors (right side) Gender Male Female

9.09±3.06 6.23±2.22 <0.001

Group DNG CG

6.30±3.46 8.18±2.46 <0.001

Dorsal flexors (left side) Gender Male Female

7.83±2.45 5.69±1.92 <0.001

Group DNG CG

6.05±2.95 6.94±2.21 <0.001

Plantar flexors (right side) Gender Male Female

22.18±7.49 14.91±6.32 <0.001

Group DNG CG

14.95±6.65 20.05±7.69 <0.001

Plantar flexors (left side) Gender Male Female

24.62±9.83 16.20±7.75 <0.001

Group DNG CG

15.23±8.34 22.45±9.20 <0.001

Table 3 Mean ± Standard Deviation values for plantar surface area(cm2) in static, dynamic and gait in each group

Condition CG DNG P-values

Static 56.63±12.41 70.60±13.04 <0.001

Dynamic 105.04±19.36 105.19±17.02 0.154

Gait 94.34±19.69 95.24±18.11 0.668

CG Control Group, DNG Neuropathy Group, N =68

Table 4 Mean ± Standard Deviation for peak plantar pressures (kgf/cm2) in static, dynamic and walking conditions by pedal region(forefoot, midfoot and hindfoot) in each group

Conditions Regions CG DNG P-values

Static Forefoot 0.18±0.25 0.11±0.22 0.222

Midfoot 0.02±0.11 0.00±0.00 0.407

Hindfoot 0.28±0.23 0.34±0.20 0.175

Dynamic Forefoot 0.92±0.78 1.32±0.39 0.016

Midfoot 0.03±0.18 0.03±0.18 0.910

Hindfoot 0.47±0.67 0.06±0.21 0.002

Gait Forefoot 1.12±0.74 1.38±0.50 0.121

Midfoot 0.03±0.22 0.07±0.35 0.651

Hindfoot 0.36±0.72 0.07±0.26 0.040

CG Control Group, DNG Neuropathy Group, N =68

Int J Diabetes Dev Ctries

the dorsal flexors, the lower the peak pressure in the fore-foot in static conditions or gait, and the higher peak pres-sure in the hindfoot in the static condition.

Linear regression analysis revealed that the only variablethat significantly contributed to the variance of the plantarsurface area occurred in the static condition was insensitivityto the 10 gmonofilament (r =0.68, F(1,38)=17.31,P <0.001).In this case, greater insensitivity predicted a greater plantarsurface area in the static condition. No variable was able topredict the full peak pressure, even when divided by regions.

Discussion

The vascular, sensory and motor functions were decreased inpeople with neuropathy somatosensory sensitivity. Only bloodperfusion values were similar in both groups. The plantarsurface area was similar for both groups in the dynamic condi-tion or gait, but was higher in patients with neuropathy in thestatic condition. The maximum peak pressures were similar forboth groups in the three conditions. The maximum peak pres-sure by plantar region showed that the neuropathy group had ahigher pressure in the forefoot in the dynamic condition andless pressure in the hindfoot in the dynamic condition and gait.

Correlation analysis showed that ABPI is directly associ-ated with blood perfusion. Additionally, the sensitivity deficitis directly associated with the plantar surface area, increasedpressure in the forefoot and decreased pressure in the hindfoot,in the dynamic condition or gait. The strength deficit of thedorsal flexor muscle group was associated with decreasedpeak pressure in the forefoot in the static condition or gait,and increased peak pressure in the hindfoot in the staticcondition. Regression analysis showed that the sensitivitydeficit can predict the plantar surface area.

The evaluation of peripheral circulation in the lowerlimbs using ABPI showed that 25 % of the individualsfrom the DNG already had mild vascular obstructivechange [1] with an average index of 0.81 (higher than thenon-diabetic population). These values are similar to thoseof Elhadd et al. [25], Hirsch et al. [26] and Marso and Hiatt[27] who found a prevalence of vascular obstructive changeof 20–30 % in diabetic individuals with ABPI<0.90. Usingperipheral oximetry, changes were observed in 7.1 % ofindividuals in the DNG, with no differences compared tothe control group. The correlation results showed a positiveassociation between ABPI and perfusion. Thus, eventhough the latter did not differ among the groups, we sawa dependency among these variables. Macro and micro-vascular changes may occur in different time periods be-cause diseases of large and small vessels do not alwaysprogress at the same speed [28].

Loss of strength in the distal muscles of the limbs is also acommon finding in diabetic neuropathy. Muscle weakness and

atrophy are related to the type and time of diagnosis [29–31].The results of our study are consistent with earlier studies.

Plantar contact surface area increased in the neuropathicgroup. This finding agrees with Andersen et al. [31], whoobserved a 50 % decrease in the volume of the intrinsicmuscles of the foot in diabetic neuropathy, suggesting at-rophy of these muscles and collapse of the plantar vault,increasing contact area with the ground. This finding wasalso reported by Sacco et al. [6], that individuals withdiabetes have a lower plantar longitudinal arch. Our regres-sion analysis results correlate with previous findings, sincethe only variable able to predict the plantar surface area wasthe sensitivity deficit, which contributed to the increasedsurface area in contact with the ground. However, in ourpatients, the DNG had a higher BMI, that can also lead toflattening of the longitudinal arch [32, 33].

We observed that maximum peak pressures in eachregion of the foot differed from controls only in the dy-namic condition. For this reason, in the static condition, dueto weakness or atrophy of intrinsic muscles, the plantarflattening of the feet worsened and could have increasedthe surface contact, thus, “relieving” the local concentrationof pressure. However, in the dynamic condition, the forcesinvolved are larger and even with greater duration of con-tact of the feet with the ground [34], there is no time toincrease the surface contact, except in the presence of analready fixed deformity of the foot, and for these reasons,the pressure peaks appear more clearly.

We found that, no vascular variable was associated with theparameters related to the appearance of ulcers (surface areaand peak plantar pressure). However, the lack of sensitivityand weakness of dorsal ankle flexors showed few significantcorrelations and were consistent with previous results. Thesensitivity deficit was associated with greater surface contactwith the ground and higher pressures in the forefoot in thedynamic condition. Weakness of the dorsal ankle flexors wasassociated with less pressure in the forefoot in the staticposture and gait and with higher pressures in the hindfoot inthe static condition. Therefore, due to lack of sensitivity andstrength under dynamic conditions, the pressure peaks dimin-ish in the hindfoot and focus in the forefoot, and the oppositeoccurs under static conditions.

The distribution of plantar pressure can be affected by sev-eral factors, notably deformities and changes in the anatomicalstructures of the feet [35]. Such changes may be the result ofthickening of the Achilles tendon and plantar fascia, whichtogether with neuropathy, eventually generate the ‘WindlassMechanism’ , pulling the metatarsal heads during gait and in-creasing the likelihood of pressure peaks in the forefoot [36].

When studying gait [37], found that the pressure in-creased in the forefoot region only in diabetics with severeneuropathy vs. moderate diabetic neuropathy and no neu-ropathy, possibly indicating that the maldistribution of plantar

Int J Diabetes Dev Ctries

pressure increases according to the degree of neuropathy. How-ever, patients with type 2 diabetes, without neuropathy or anyperipheral vascular disease and also had an anterior displace-ment of the weight in the diabetic group during gait [38]. Thismay be because diabetic foot syndrome develops gradually, andmay begin even before the clinical diagnosis. In some people,these symptoms may be more pronounced.

The results of our study indicate the need for early inter-vention in diabetics with a specific focus on training tostrengthen muscles of the distal lower limb. Future researchshould be encouraged to include patients with a history ofulceration and with varying degrees of neuropathy to betterunderstand the evolution of the disease.

In conclusion, individuals with diabetic peripheral neuropa-thy associated with circulatory deficits, but with no change inblood perfusion and no history of foot complications (ulcers,amputations and deformities), had plantar pressure values with-in the normal range. However, there was uneven distributionwithin the various regions of the feet, suggesting changes in gaitpattern and strategy. Many of the sensory, vascular, and mus-culoskeletal changes found among this population were asso-ciated with factors that predispose to the development of plantarulcers. However, only somatosensory deficit contributed sig-nificantly to increase the contact area with the ground (one ofthe factors that can facilitate the process of ulceration).

Conflicts of interest None

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