Abnormalities of plantar pressure distribution in early, intermediate, and late stages of diabetic neuropathy

Gait & Posture xxx (2014) xxx–xxx

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GAIPOS-4251; No. of Pages 5

Abnormalities of plantar pressure distribution in early, intermediate,and late stages of diabetic neuropathy

Isabel C.N. Sacco a,*, Adriana N. Hamamoto a, Lucas M.G. Tonicelli a, Ricky Watari a,Neli R.S. Ortega b, Cristina D. Sartor a

a University of Sao Paulo, School of Medicine, Physical Therapy, Speech and Occupational Therapy Department, Sao Paulo, SP, Brazilb University of Sao Paulo, School of Medicine, Center of Fuzzy Systems in Health, Sao Paulo, SP, Brazil

A R T I C L E I N F O

Article history:

Received 12 December 2013

Received in revised form 24 June 2014

Accepted 30 June 2014

Keywords:

Diabetic neuropathies

Diabetes mellitus

Plantar pressure

Gait

Fuzzy logic

A B S T R A C T

Inconsistent findings with regard to plantar pressure while walking in the diabetic population may be

due to the heterogeneity of the studied groups resulting from the classification/grouping criteria

adopted. The clinical diagnosis and classification of diabetes have inherent uncertainties that

compromise the definition of its onset and the differentiation of its severity stages. A fuzzy system

could improve the precision of the diagnosis and classification of diabetic neuropathy because it takes

those uncertainties into account and combines different assessment methods. Here, we investigated

how plantar pressure abnormalities evolve throughout different severity stages of diabetic polyneuro-

pathy (absent, n = 38; mild, n = 20; moderate, n = 47; severe, n = 24). Pressure distribution was analysed

over five areas while patients walked barefoot. Patients with mild neuropathy displayed an increase in

pressure–time integral at the forefoot and a lower peak pressure at the heel. The peak and pressure–time

integral under the forefoot and heel were aggravated in later stages of the disease (moderate and severe)

compared with early stages of the disease (absent and mild). In the severe group, lower pressures at the

lateral forefoot and hallux were observed, which could be related to symptoms that develop with the

aggravation of neuropathy: atrophy of the intrinsic foot muscles, reduction of distal muscle activity, and

joint stiffness. Although there were clear alterations over the forefoot and in a number of plantar areas

with higher pressures within each severity stage, they did not follow the aggravation evolution of

neuropathy classified by the fuzzy model. Based on these results, therapeutic interventions should begin

in the early stages of this disease to prevent further consequences of the disease.

� 2014 Elsevier B.V. All rights reserved.

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Gait & Posture

jo u rn al h om ep age: ww w.els evier .c o m/lo c ate /g ai tp os t

1. Introduction

Plantar pressure distribution has been widely investigated inpatients with diabetic polyneuropathy (DN) for decades because ofits relationship to tissue breakdown risk and plantar ulcerformation [1–4]. Although this relationship is well accepted byclinicians and researchers, there are still inconsistencies regardingthe number of compromised foot areas, which areas are the mostcompromised, and when the alterations in peak pressure andpressure–time integral begin during diabetes progression. Somestudies showed an increase in pressure only over the forefoot [5,6].

* Corresponding author at: Departamento de Fisioterapia, Fonoaudiologia e

Terapia Ocupacional, R. Cipotanea, 51, Cidade Universitaria, CEP: 05360-160, Sao

Paulo, SP, Brazil. Tel.: +55 11 30918426.

E-mail address: [email protected] (Isabel C.N. Sacco).

URL: http://www.usp.br/labimph

Please cite this article in press as: Sacco ICN, et al. Abnormalities of pladiabetic neuropathy. Gait Posture (2014), http://dx.doi.org/10.1016/

http://dx.doi.org/10.1016/j.gaitpost.2014.06.018

0966-6362/� 2014 Elsevier B.V. All rights reserved.

Some studies showed an increase in pressure over the entireplantar area without highlighting any one area [7–9], and other

studies did not indicate which plantar areas experienced higher

pressures [10,11]. Another factor that contributes to the inconsis-

tent findings in this area is the classification criteria for the patients

included in these previous studies. Patients without DN may or

may not have been considered neuropathic, and different degrees

of DN might have been included in the same group.Inconsistent findings with regard to plantar pressure distribu-

tion while walking in the diabetic population may be due to the

heterogeneity of the studied groups resulting from the classifica-

tion/grouping criteria adopted. Patients without neuropathy may

or may not have been considered neuropathic, and different

degrees of neuropathy may have been included in the same group.Regarding the grouping criteria, there are rarely two patients

with exactly the same symptoms due to the continuous evolution

of DN. Currently, the clinical classification of these patients is based

ntar pressure distribution in early, intermediate, and late stages ofj.gaitpost.2014.06.018


mailto:[email protected]

http://www.usp.br/labimph


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www.elsevier.com/locate/gaitpost


I.C.N. Sacco et al. / Gait & Posture xxx (2014) xxx–xxx2

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on a clear logic—i.e., either they have DN or not—and thisdistinction is not easy to make. There are many clinicalinstruments for classifying DN and each one evaluates differentaspects of the disease, such as symptoms; pain, tactile, and thermalsensitivity; vibratory perception; and tendon reflex. In addition tothe clinical assessment, a nerve conduction study is an objectiveand reliable tool for diagnosing nerve damage, but it does notalways correlate well with symptoms and signs [12].

DN has an insidious onset, manifesting itself in different waysand at different stages of the disease. Even if clinical examinationscombine different types of assessments, there are no objectivecriteria for interpreting the association of those results. This leavesthe diagnosis to either a subjective or semi-objective decision by ahealth professional or a grading system that uses a simple sum ofthe output scores. In clinical practice, the fuzziness nature of thedecision-making process for diagnosis and treatment, which isbased on the expertise of the health professional and theinterpretation of many aspects of a patient, led us to evaluatepatient gait using a different grouping logic.

For plantar pressure studies, participant groups are usuallydivided into DN groups with or without ulceration. However,patients with DN have wide ranging clinical statuses; thus, a DNgroup will include patients who present with only a fewneuropathy symptoms combined with incipient somatosensoriallosses and patients with a complete absence of plantar sensitivityand a very advanced foot impairment with muscle atrophy [8,13–15]. Thus, a DN group is highly heterogeneous, especially whenjoint and muscle functions are not described or used to classify thefoot areas that are expected to be impaired and influence plantarpressure behaviour in severe cases.

From the beginning of plantar pressure distribution descriptionin this population [16], diverse groups have been studied. Severalstudies have observed differences in peak pressure betweengroups [5,17,18]; however, these studies differ in the way theygrouped and compared the individuals. Pataky et al. [5] andBennetts et al. [19] studied diabetic individuals who weresupposedly without DN. Conversely, Sawacha et al. [8], Guiottoet al. [13], Owings et al. [17] and Sacco et al. [14] studied onlypatients with DN but did not distinguish their severity status.Bacarin et al. [9] and Giacomozzi et al. [15] compared two subsetsof DN patients divided into groups based on their history ofprevious ulceration. The studies by Caselli et al. [18] and Phamet al. [11] were the only ones that divided the diabetic subjects intofour severity degrees in a clear manner using a classificationprocedure based on a simple sum of questionnaire output scores[11,20].

In the context presented, a linguistic fuzzy model is an optionfor classification, because it addresses issues of uncertainty in theallocation of elements in determined sets [21]. This type of modelallows us to simulate the cognitive aspect of the decision-makingprocess performed by healthcare specialists and to translatesubjective opinions into objective criteria [21], and it is capable ofobjectively measuring a subjective judgement. Fuzzy logic has

Table 1Mean (standard deviation) or median (interquartile interval) of socio-demographic and

mild neuropathy (MiN), moderate neuropathy (MoN) and severe neuropathy (SN).

D (n = 38) MiN

Sex (% male) 52 17

Age (years) 56.5 � 7.0 56

Body mass index (m/kg2) 28.7 � 4.4 29

Fast glycaemia (mg/dL) 147.2 � 59.9a 172

Diabetes duration (years) 7.2 � 6.2c,d,e 9

Gait speed (m/s) 1.86 (0.35) 1

ANOVA test, followed by Newman Keuls post hoc tests (p < 0.05).

Symbols represent statistically significant difference between groups. Legend of symbo


already been applied to other diseases, such as breast cancer [22],that have uncertain boundaries for the different stages of diseaseseverity.

Because determining DN stage can indicate plantar pressurepatterns, the identification of which is crucial for implementingearly preventive strategies, we investigated the plantar pressuredistributions of patients with DN of differing severity stages whilethey walked. DN severity was classified using a fuzzy model(artificial intelligence) developed previously [23]. We hypothe-sised that patients with later stages of DN would have a greatermagnitude of pressure related-variables over the anterior parts ofthe foot compared with patients with early and intermediatestages of DN.

2. Methods

For this study, 129 subjects were recruited from three differentsettings: (i) the database of the Physical Therapy, Speech andOccupational Therapy Department, (ii) a primary care centre (fromthe Medical School), and (iii) from a National Diabetes Association.Patients were continuously recruited, assessed and allocated intofour groups during a period of 6 months. The final groups werediabetic subjects with the absence of neuropathy (D, n = 38),mild neuropathy (MiN, n = 20), moderate neuropathy (MoN,n = 47), and severe neuropathy (SN, n = 24) (Table 1). All subjectswere informed of the research procedures and signed aninformed consent approved by the local ethics committee(Comite de Etica em Pesquisa da Faculdade de Medicina USP,protocol number 320/10).

The classification into four groups was performed using a fuzzyexpert system proposed by Watari et al. [23]. It uses threemodalities of DN assessments validated by the InternationalDiabetes Federation as inputs: symptoms (based on the MNSIquestionnaire), tactile sensitivity (10 g Semmes–Weinstein mono-filament), and vibratory perception (128 Hz tuning fork). Thisfuzzy model was built based on the knowledge of experts inevaluating DN signs and symptoms. The combination of eachassessment resulted in a DN degree that was represented by anumber between 0 and 10 and was calculated by the centre of areadefuzzification method. This value was used to sort the partici-pants into the disease classes, as follows: (i) 0–2.5: absentneuropathy; (ii) 2.6–4.5: mild neuropathy; (iii) 4.6–7.5: moderateneuropathy; and (iv) 7.6–10: severe neuropathy. Patients with ahistory of previous plantar ulceration were included in the severeneuropathy group. These classifications using this fuzzy modelwere strongly correlated with the classifications made by a groupof specialists (Pearson’s coefficient r = 0.943) and the accuracylevel of the fuzzy model was considered excellent (ROC curvearea = 0.985). More details of the model can be found in apublication by Watari et al. [23].

The eligibility criteria were as follows: presence of diabetesmellitus (types 1 or 2); under 65 years of age; ability to walk freelywithout any assistive device; absence of active ulcers at the time of

clinical data of the studied groups: diabetic subjects without neuropathy (D), with

(n = 20) MoN (n = 47) SN (n = 24)

53 67

.4 � 6.2 58.8 � 4.9 58.5 � 5.1

.5 � 4.3 29.4 � 4.9 28.2 � 3.5

.2 � 77.9b 186.2 � 91.6a,b 189.8 � 91.6

.0 � 7.7c 13.7 � 7.7d 13.0 � 7.1e

.80 (0.25) 1.91 (0.36) 1.83 (0.34)

ls: (a) p = 0.007; (b) p = 0.03; (c) p = 0.0004; (d) pp < 0.001; (e) p = 0.0005.



Fig. 1. Schematic image of an insole and the parameters used to divide the plantar

areas in heel, midfoot, lateral and medial forefoot, and hallux.

I.C.N. Sacco et al. / Gait & Posture xxx (2014) xxx–xxx 3

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assessment; absence of any type of lower limb amputation;absence of major foot deformities, such as cavus foot, flat foot, clawtoes and Charcot arthropathy; and absence of vascular disease,claudication, retinopathy, nephropathy, and any orthopaedic (e.g.,fracture) or neurological (e.g., stroke) impairment that couldinfluence gait.

The groups did not differ in terms of age, sex distribution orbody mass index (Table 1). The MoN group had higher fastingglycaemia levels compared with the D and MiN groups. The twogroups in the later stages of the disease (MoN and SN) had a longerduration of diabetes mellitus, which was expected (Table 1).

Plantar pressure-related variables (peak pressure and pres-sure–time integral) were acquired at 100 Hz for five plantar areas(heel, midfoot, lateral and medial forefoot and hallux—Fig. 1) usingthe pedar-X system (Novel1, Munich, Germany) while the patientswalked. Subjects walked along a 10 m walkway at a self-selectedcadence wearing the measurement insoles inside anti-skid socks.We ensured for each individual that the entire plantar surface wasfully covered by the insole size chosen according to patients’ feetsizes (from 6.5 to 11.5 in US shoe sizes). Before data acquisition, thesubjects were instructed to walk freely in the laboratory toreproduce their daily gait and to adapt to the laboratoryenvironment and equipment. A digital metronome was used tocheck gait cadence in order to avoid intra-individual variations

Table 2Mean and standard deviation of peak pressure (kPa), and pressure–time integral (kPa s)

(MiN), moderate neuropathy (MoN) and severe neuropathy (SN).

D (n = 38)

Peak pressure (kPa) Heel 279.5 � 63.4*

Midfoot 116.6 � 38.3

Lateral forefoot 269.3 � 64.7

Medial forefoot 287.1 � 70.2ab

Hallux 205.2 � 83.8a

Pressure–time integral (kPa s) Heel 67.9 � 15.4

Midfoot 37.9 � 13.7a

Lateral forefoot 77.2 � 18.1

Medial forefoot 79.2 � 18.6ab

Hallux 44.4 � 20.4

Statistically significant differences between groups (a, b, c, d, e).

Statistically different group from all others (p < 0.05) (*, #, &, $, %).1 Kruskal–Wallis test followed by Mann–Whitney posthoc test.


within each subject trial and to ensure that the gait speedcalculated after data acquisition was not different among theexperimental groups (p = 0.75). A mean of 20 valid steps was usedfor statistical purposes.

All pressure variables were compared among the four groupsusing Kruskal–Wallis tests followed by Mann–Whitney tests.Differences with p < 0.05 were considered statistically significant,as a normal data distribution was not achieved (Shapiro–Wilk test).

3. Results

The neuropathic groups displayed different loads at the heel when compared

with the non-neuropathic subjects, with the MiN group exhibiting lower peak

pressures and the MoN and SN groups exhibiting higher pressure–time integrals.

There seemed to be an overall increase in pressure magnitude on the other plantar

areas in the neuropathic groups. Over the midfoot and medial forefoot, the D group

had the lowest pressure–time integrals. The MiN group had the lowest peak

pressure value on the lateral forefoot. The MiN and D groups also had lower peak

pressures in the medial forefoot and hallux compared with the more affected

groups (MoN and SN). Overall, the MoN and SN groups exhibited higher pressures in

all anterior areas of the foot, with significant differences at the lateral and medial

forefoot (for both variables representing loads) and hallux (only peak pressures for

MoN). There was also a slight difference between the two groups with later stages of

neuropathy, with SN showing lower loads (peak pressure and pressure–time

integral) on the lateral forefoot and hallux than MoN, although these differences

were not statistically significant (Table 2).

4. Discussion

Overall, the results showed alterations in the plantar pressuredistributions for each severity stage, and this alteration wasparticularly clear for the medial forefoot. However, alterationswere not found to follow the aggravation evolution of diabeticpolyneuropathy. The onset of neurological involvement, whichwas present in the MiN group, shifted the higher pressure areas tothe anterior parts of the foot. MiN individuals presented a lowerpeak pressure at the heel compared with diabetics withoutneuropathy, and although this variable was lower at the lateralforefoot, the pressure–time integral was higher over all other footareas.

As neuropathy is aggravated, which occurs in patients in theintermediate stage (MoN), higher pressures (peak and integral)over the hallux and over both forefoot areas are observedcompared with patients in early stages and patients withoutneuropathy (D, MiN). This suggests a worse pressure distributionand an impaired rollover process in intermediate stage patients. Inaddition, patients in the later stages (MoN and SN) had increasedloads on the heel compared with patients in the early stages. Thesefindings could be linked to the impaired shock absorption duringthe heel strike and during the flat foot phases of the gait. This waspreviously confirmed by electromyography results, which showed

for five foot areas: diabetic subjects without neuropathy (D), with mild neuropathy

MiN (n = 20) MoN (n = 47) SN (n = 24) p1

267.7 � 62.1$ 289.8 � 68.0 297.1 � 63.1 <0.001

120.1 � 46.9 115.0 � 42.8 118.5 � 40.5 0.343

255.8 � 69.0 313.2 � 84.5 281.9 � 75.6 <0.001

282.9 � 66.0cd 330.0 � 100.8ac 321.1 � 92.9bd <0.001

207.1 � 85.2b 224.9 � 93.9ab 212.0 � 107.0 <0.001

68.6 � 13.2 79.2 � 21.1& 73.5 � 18.5* <0.001

41.3 � 16.2ab 39.6 � 15.4 39.9 � 13.7b 0.030

78.6 �24.2 91.3 � 22.6 86.3 � 23.2 <0.001

83.7 � 21.4cd 93.3 � 26.0ac 94.9 � 29.0bd <0.001

45.1 � 22.4 48.9 � 24.2 45.7 � 24.0 0.075



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a delay in tibialis anterior [24] and vastus lateralis [24,25] activityin diagnosed patients with clear signs and symptoms of diabeticneuropathy.

Patients in the later stages (SN and MoN) also presented higherpressure–time integrals and peak pressures over the entireforefoot area compared with patients in the early stages. Theseforefoot changes from the early to later stages may be related to aworsening of the eccentric control of the tibialis anterior, whichhas been previously reported in diabetic patients [24]. However, itis still unclear when during the time course of the disease thismuscle dysfunction originates. Early activation of the ankleextensor muscles, which leads to premature foot flattening, hasbeen observed in diabetic neuropathy patients [26]. Apparently,delayed tibialis anterior activity and anticipation of ankle extensormuscle activity can cause premature forefoot contact after the heelstrike increasing the pressure–time integral and peak pressureover the anterior areas of the foot.

However, in the most advanced stage of the disease (SN), we didnot observe an additional increase in the loading variables in themedial forefoot or hallux from the MoN stage, rather, we observeda decrease or stabilisation of the magnitude of those variables. Thisdecrease/stabilisation of plantar loading could have occurred forseveral reasons: a shorter centre of pressure (COP) excursion in theantero-posterior and latero-lateral direction [7,15]; atrophy of thesmall intrinsic foot muscles [27], which impairs the toe and halluxfunctions, thereby, altering the rollover process [28]; and as aconsequence of a more cautious walking strategy, even though wecontrolled for gait speed. This unexpected result deserves furtherinvestigation because it could represent a functional disability,such as gait instability.

A shorter COP excursion may partially explain our halluxfindings in SN patients, which were the most severe patientsstudied and were similar to the group studied by Giacomozzi et al.[15]—a diabetic neuropathic population with previous ulceration.This finding suggests that the role of the hallux in gait is reduced inpatients in later stages of the disease because in the beginning ofthe stance phase, the anterior parts of the foot terminate theircontact with the floor at the metatarsal heads before reaching thehallux.

Several studies have reported altered peak pressures andpressure–time integrals in diabetic subjects, although none haveinvestigated these differences between patients with the absenceof neuropathy and patients in a severe stage using a fuzzyprogression. The classification paradigm of the present studyincluded common parameters regularly used in clinical practice asinput variables for an artificial intelligence model that addressesissues of uncertainty in determining boundaries between theseverity stages of diabetic polyneuropathy. Therefore, this fuzzymodel could be a useful and feasible tool in healthcare systems tofacilitate the classification of patients, as it includes a variety ofcommonly used clinical variables in a linguistic scale and doesnot require specialised personnel or sophisticated or invasiveassessments, such as electroneuromyography. Although elec-troneuromyography is considered the gold standard for theclinical diagnosis of neuropathy, it is not capable of classifyingits severity. Nerve conduction studies do not always correlatewell with symptoms and signs; thus, they are only recom-mended for patients with symptomatic, confusing, unusual orsevere neuropathy [12].

One of the advantages of the fuzzy model is that it gives a widerview of patient status and, most importantly, it takes into accountpatients with early impairments. The aim of the fuzzy model is notto identify patients at risk of ulcer formation but to identify earlyclinical alterations related to DN to aid in early interventionsbefore any risk of foot ulceration develops. There are other healthissues related to DN status in addition to ulceration that also


impact patient quality of life, such as an increase in incidence offalls, gait instability and a loss of function [29].

The lack of a control group without diabetes mellitus is alimitation of this study; however, the identification of differencesbetween the early and late stages of neuropathy was importantconsidering the current state of knowledge in the diabetes field.Other studies have also lacked a comparison between a diabeticand non-diabetic population [18], but it would be useful to makethis comparison in the future.

Our findings showed that as neuropathy progresses, thenumber of foot areas with altered pressure distributions alsoincreases, particularly over the anterior areas of the foot (medialand lateral forefoot and hallux). Unexpectedly, the severe groupdid not show a further increase in plantar loading from themoderate severity group. We also showed the importance ofclassifying diabetic patients into different neuropathy severitystages, considering the uncertainty of the current classificationsystem used in clinical practice. Our fuzzy model is an easy andsimple option for classifying neuropathy severity, although furthervalidation of this model is still necessary.

5. Conclusion

There are clear alterations in the plantar pressure over theforefoot and in a number of plantar areas with higher pressures ateach severity stage of DN, but these alterations do not follow theaggravation evolution of diabetic polyneuropathy classified by thefuzzy model. The later the neuropathy stages, the worse the plantarpressure distribution was during walking. There were remarkableincreases in pressures over the entire forefoot and a change inthe role of the hallux in foot rollover. Even in the early stages ofthe disease, it is possible to identify a load shifting to the moreanterior parts of the plantar surface. Detecting altered pressuredistribution patterns in the early stages of neuropathymight lead to a better definition of preventive interventionsto avoid further gait impairment as a consequence of diabeticneuropathy.

Acknowledgements

The authors are grateful to CNPq (National Council for Scientificand Technological Development) for the Watari scholarship(Master 556374/2010-0) and to the Sao Paulo State ResearchFoundation (FAPESP) for the Sartor scholarship (2011/19304-4).

Conflict of interest

None declared.

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Abnormalities of plantar pressure distribution in early, intermediate, and late stages of diabetic neuropathy