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The role of foot morphology on foot function in diabetic subjects with or without neuropathy
Gait & Posture 37 (2013) 603–610
Contents lists available at SciVerse ScienceDirect
Gait & Posture journal homepage: www.elsevier.com/locate/gaitpost
The role of foot morphology on foot function in diabetic subjects with or without neuropathy Annamaria Guiotto a,1, Zimi Sawacha a,2, Gabriella Guarneri b,3, Giuseppe Cristoferi b,4, Angelo Avogaro b,5, Claudio Cobelli a,* a b
Department of Information Engineering, University of Padova, Via Gradenigo 6b I, 35131 Padova, Italy Department of Clinical Medicine and Metabolic Disease, University Polyclinic, Via Giustiniani 2, 35128 Padova, Italy
A R T I C L E I N F O
A B S T R A C T
Article history: Received 20 March 2012 Received in revised form 20 September 2012 Accepted 30 September 2012
The aim of this study was to investigate the role of foot morphology, related with respect to diabetes and peripheral neuropathy in altering foot kinematics and plantar pressure during gait. Healthy and diabetic subjects with or without neuropathy with different foot types were analyzed. Three dimensional multisegment foot kinematics and plantar pressures were assessed on 120 feet: 40 feet (24 cavus, 20 with valgus heel and 11 with hallux valgus) in the control group, 80 feet in the diabetic (25 cavus 13 with valgus heel and 13 with hallux valgus) and the neuropathic groups (28 cavus, 24 with valgus heel and 18 with hallux valgus). Subjects were classified according to their foot morphology allowing further comparisons among the subgroups with the same foot morphology. When comparing neuropathic subjects with cavus foot, valgus heel with controls with the same foot morphology, important differences were noticed: increased dorsiflexion and peak plantar pressure on the forefoot (P < 0.05), decreased contact surface on the hindfoot (P < 0.03). While results indicated the important role of foot morphology in altering both kinematics and plantar pressure in diabetic subjects, diabetes appeared to further contribute in altering foot biomechanics. Surprisingly, all the diabetic subjects with normal foot arch or with valgus hallux were no more likely to display significant differences in biomechanics parameters than controls. This data could be considered a valuable support for future research on diabetic foot function, and in planning preventive interventions. ß 2012 Elsevier B.V. All rights reserved.
Keywords: Diabetic foot Foot type Kinematics Plantar pressures Three dimensional
1. Introduction Diabetic and neuropathic subjects (DPN) are at increased risk for ulcer development at sites exposed to repetitive, high plantar loading [1,2]. Several studies have been conducted in the last decade to investigate diabetic foot biomechanics alterations especially in term of foot kinematics and plantar pressure (PP) during gait [1,3–8]. Previous PP studies demonstrated an important correlation between the sites displaying higher PP and the presence of callosities of DPN subjects [8,9]. Stresses were found to
* Corresponding author. Tel.: +39 049 8277661; fax: +39 049 8277699. E-mail addresses: [email protected] (A. Guiotto), [email protected] (Z. Sawacha), [email protected] (G. Guarneri), [email protected] (G. Cristoferi), [email protected] (A. Avogaro), [email protected], [email protected] (C. Cobelli). 1 Tel.: +39 049 8277805; fax: +39 049 8277699. 2 Tel.: +39 049 8277662; fax: +39 049 8277699. 3 Tel.: +39 0498213061; fax: +39 0498213062. 4 Tel.: +39 0498213061; fax: +39 0498213062. 5 Tel.: +39 0498212178; fax: +39 0498754179. 0966-6362/$ – see front matter ß 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.gaitpost.2012.09.024
be relatively higher and located closer to the skin surface where skin breakdown was most likely to occur [10]. Others demonstrated an association between higher peak PP and morphological foot alteration in DPN [8,11]. Ledoux et al. investigated diabetic subjects considering the structural differences between types of foot and demonstrated close relationships between foot morphological alterations and plantar ulcerations [12–14]. Several kinematics studies have compared DPN to control subjects (CS) [5,6]. Although these studies provided insight into the potential influence of diabetes on kinematics during gait, the majority of them considered the foot as a rigid segment and evaluated its motion with respect to the tibia. Only two recent studies [4,5] applied a three-dimensional (3D) multisegment foot kinematic model to evaluate DPN foot kinematics during gait, and observed significant alterations especially in DPN’s forefoot triplanar angles [4,5]. It has also been shown that limited joint mobility may contribute to increased foot subsegments loading by limiting foot flexibility and restraining the forward progression of body weight during the stance phase of gait [3]. However data substantiating the causes and consequences of foot morphology on limited mobility and excessive PP in DPN is limited.
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Table 1 Clinical and demographic characteristics and space-time data of control group (CS), diabetic non neuropathic group (NoDPN) and diabetic neuropathic group (DPN). The reported P values indicate the results of the comparison between the CS and NoDPN groups, the CS and the DPN groups, and the NoDPN and DPN groups (one-way Anova). A value of P < 0.05 was considered statistically significant (P*). Groups
CS # or mean
Subjects [#] Sex [# of males] BMI [kg/m2] Hypertensive disease [#] Age [years] Peripheral neuropathy [#] Autonomic neuropathy [#] Diabetic retinopathy [#] Microalbuminury [#] Vasculopathy [#] Vasculopathy (peripheric) [#] Vasculopathy (TSA) [#] Vasculopathy (coronary) [#] Type of diabetes [#] Hb A1c Years of disease Cavus foot [#] Flat foot [#] Valgus Hindfoot [#] Varus Hindfoot [#] Hallux valgus [#] Foot deformities [#] Plantar callosity [#] Gait velocity (m/s) Stride period (s) Stride length (m) Stance period (s)
20 14 24.41 0 59.35 – – – – – – – – – – – 26 0 22 0 11 12 5 0.998 1.234 1.222 0.762
NoDN SD
# or mean
– –
20 14 26.49 8 62.90 0 0 6 2 2 0 11 4 type1: 3, type2: 17 7.48 16.05
0.123 0.124 0.114 0.086
25 4 13 3 13 10 21 1.102 1.140 1.234 0.668
2.58 4.76 – – – – – – – – –
DN SD
# or mean 20 13 26.24 13 60.30 20 6 12 4 5 3 9 4 type1: 10, type 2: 10 8.12 23.00
2.22 5.63
1.36 11.14
The purpose of this study was to explore the relationship between foot deformities, 3D multisegment foot kinematics and PP during gait in diabetes and DPN. This was pursued by assessing in vivo 3D multisegment foot kinematics [5] and PP of both CS and diabetes subjects with and without neuropathy. Results of this study can be used as a support to design foot orthotic devices [15,16]. Recent literature [15,16] emphasized the importance of considering both foot biomechanics and morphology when planning various foot orthotics devices in order to efficiently reduce plantar ulcer formation and avoid amputation in diabetic subjects. 2. Methods 2.1. Subjects Subjects were recruited among the patients attending the outpatient Clinic at the Department of Metabolic Disease of the University of Padova (Italy). Inclusion criteria were: type 1 and 2 diabetic subjects with walking ability, no history of ulcers or neurological disorders (apart from neuropathy), orthopedic problems, lower limb surgery, cardiovascular disease. CS were recruited among hospital personnel and chosen to be age-, BMI- and gender-matched with the diabetic subjects. On the basis of these criteria 60 patients were examined: 20 CS, 40 diabetic patients (20 without peripheral neuropathy (NoDPN) and 20 DPN). All subjects gave written informed consent. The protocol was approved by the local Ethics Committee. Height and weight were recorded and body mass index (kg/m2) was calculated. The neurological evaluation included the assessment of symptoms, and signs compatible with peripheral nerve dysfunction. The Michigan Neuropathy Screening Instrument questionnaire was used [17]. Subjects were classified as neuropathic if they were found to be positive for three or more out of a total of 15 specified symptoms [18]. The physical examination consisted of: patellar and ankle reflexes, assessment of lower limb muscle strength, sensory testing (pin-prick), touch (10 g Semmens Weinstein monofilament) and vibration perception threshold (128 MHz tuning fork and Biothesiometer), pain sensitivity, electroneurophysiological study, and ankle-to-brachial systolic pressure ratio (Index of Winsor). Cardiovascular autonomic tests were also performed. HbA1c values from the preceding ten years were collected. Each patient had at least one ophthalmologic examination, a urinary albumin-to-creatinine ratio
0.228 0.150 0.183 0.103
SD
3.68 9.60
CS vs NoPN
CS vs PN
NoPN vs PN
P
P
P
0.5 0.009* 0.99 0.037*
0.5 0.074 1 0.694
0.37 0.776 0.94 0.303 1 0.99 0.97 0.81 0.89 0.96 0.26 0.5 type1: 0.99, type2:0.009 0.0909 0.0723
0.41 0.98 0.02* 0.96 0.69 0.31 0.99 0.05 0.005* 0.91 0.0002*
0.68 0.98 0.67 0.96 0.95 0.88 0.99 0.13 0.009* 0.96 0.001*
0.76 0.5 0.99 0.5 0.87 0.95 0.33 0.64 0.51 0.96 0.29
1.57 12.84
28 4 24 3 18 17 19 1.070 1.167 1.230 0.698
0.212 0.105 0.189 0.079
measured, a carotid artery Doppler ultrasound examination, and a 12-leads electrocardiogram in the three months period preceding the study. All subjects underwent clinical examination of the foot by a single orthopedic surgeon experienced in foot and ankle [14,19], in order to ensure reliability of the classifications and be consistent with clinical practice [18]. The type of foot (cavus, planus, normal), foot deformities (hallux valgus/normal/ rigidus, claw and hammer toes, limitation of dorsiflexion of the great toe, abducted/ adducted/overlapping toes), pre-ulceration lesions (calluses, soft corns) and hip, knee, and ankle joint mobility were assessed. Heel position and plantar foot arch during bipedal loading were also evaluated through both footprints [20] and static acquisitions [7] on the PP system. A foot was classified as: cavus if the middle third of the footprint covered less than the 2/3rd of the forefoot print’s width; as planus if the width of the middle third of the footprint exceeded 1/3rd of the full foot width [20]. The heel deviation was evaluated by comparing the Helbing line (drawn along the Achilles tendon) with the vertical one. A valgus deviation higher than 38 was considered as valgus heel. Any deviation toward the varus was considered varus heel [20]. Hallux valgus was defined as a deviation of the great toe toward the lateral side of the foot with a prominence developed over the medial side of the first metatarsal head [13].
2.2. Experimental set up Movement analysis was carried out using a 60 Hz six cameras stereophotogrammetric system (BTS S.r.l, Padova), two force plates (FP4060-10, Bertec Corporation, USA), two PP systems (410 mm 410 mm 0.5 mm, 0.64 cm2 resolution, 150 Hz, Imagortesi, Piacenza). The signals coming from all systems were synchronized in post processing as in [21]. A four-segment 3D foot kinematic model was adopted. This was previously validated in our laboratory [5,21] and it allows the 3D evaluation of ankle, hindfoot, midfoot and forefoot kinematics [21,22]. A three-segment model for the plantar sub-area definition was obtained by means of projecting the anatomical landmarks of the kinematics protocol onto the footprint [21,23]. Thus, for each patient’s foot the hindfoot, midfoot, forefoot subareas were defined as in [21]. The elaboration of PP distribution concentrated on the analysis of some meaningful parameters as in [21]: the center of pressure (COP) mediolateral (ML) and anteroposterior (AP) excursions and the curve integral [6], peak and mean pressure curves (PPC and MPC), and loaded surface curve (LSC). The motion analysis protocol was organized with a static acquisition (subject in an upright posture, with feet placed with ankles together, toes pointed 308 apart and the arms along the body [5,6,21]) and gait analysis sessions.
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Table 2 (a and b) The results of the comparison between the generic groups CS, NoDPN and DPN (GB method – a, homogeneous groups – b). Gray corresponds to those intervals in which there are statistically significant differences between the groups (P < 0.05 from t-test). Only variables with almost one P < 0.05 are reported. hf = hindfoot, mf = midfoot, ff = forefoot, invev = inversion-eversion, i-e rot = intra–extrarotation, dp = dorsiplantarflexion, PP = plantar pressures, LSC = loaded surface curve, COP EXC = center of pressure excursion, ML = medio-lateral, AP = antero-posterior.
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Fig. 1. Results for midfoot–hindfoot inversion–eversion rotation angle in generic normative bands (GB) and each comparison from 1 to 6: cavus feet (group 1), cavus feet and valgus heel (group 2), cavus feet and hallux valgus (group 3), normal feet (group 4), cavus feet and normally aligned heel (group 5), cavus feet and normal hallux (group 6).
Gait analysis: patients walked at a self-selected speed along a walkway; velocity, stride and step parameters were calculated. At least three gait cycles of each limb were recorded for each patient. For each trial, all angular displacements and PP curves were plotted over one stance phase of gait [21].
istic, time and space parameters were performed by means of one-way-Anova (Tukey– Kramer post hoc comparison), and paired t-test after evidence of normality (Lilliefor’s Test) or Kruskal Wallis Test (Matlab software, R2010a).
2.3. Statistical analysis
3. Results
Each subject kinematic and PP variables were represented with the mean of three representative trials. Correlation coefficient (CC) was used to aid in selecting which of each subject’s representative walking trials should be included in the computation of the mean and standard deviation (SD); thus the CC was calculated for each subject’s kinematic and PP parameters. Walking trials with a CC less than 0.75 were excluded from the statistical analysis [6]. Generic normative bands (GB) were created with the data of the CS (GB CS, mean and SD of each variable) and the data of the NoDPN and DPN groups (GB NoDPN and GB DPN) were compared with them without considering foot morphology. Furthermore, subjects were classified according to their foot morphology and each of the three groups (CS, NoDPN and DPN) was split in subgroups according to this classification:
The clinical, demographic characteristics, time and space parameters of the studied subjects were reported in Table 1, and show that all patients were in fair metabolic control. The DPN had a higher prevalence of both micro- and macrovascular complications. Results of the biomechanic analysis are shown in Table 2, Figs. 1 and 2, Appendix. In Table 2 results of the comparison among the CS, the NoDPN and the DPN without taking into account foot morphology (GB approach) have been reported and were found consistent with state of the art [1,3–8,21]. Major differences with other studies adopting different foot models can be attributed to differences in both the kinematics and PP subarea division. However several differences were observed between GB and the approach proposed herein. NoDPN with normal foot (group 4) displayed only a few differences when compared with CS with same foot morphology: increased peak and mean PP were noticed on the forefoot (P < 10 3) together with increased LSC on the midfoot (P < 0.02). As for the DPN’s kinematic data, the alterations revealed from both the GB approach and the homogeneous group one were: decreased eversion on the midfoot and increased eversion on the forefoot and midfoot for the groups with cavus foot and valgus heel or cavus foot and normal hallux. When considering the PP data analysis, excessive peak PP was found on the hindfoot of the DPN.
1. 2. 3. 4. 5. 6.
cavus feet (group 1); cavus feet and valgus heel (group 2); cavus feet and hallux valgus (group 3); normal feet (group 4); cavus feet and normally aligned heel (group 5); cavus feet and normal hallux (group 6).
Mean and SD were computed on each subgroup’s variable over the stance phase of gait and bands were created within each subgroup (mean 1 SD). Afterwards the data within each group were compared: one-way-Anova (Tukey–Kramer post hoc comparison), after evidence of normality (Lilliefor’s Test) or Kruskal Wallis Test was used (Matlab software, R2010a). These tests were performed considering the variables mean value at specific stance phase intervals: initial contact (0–3%), loading response (3–17%), midstance (17–50%), terminal stance (50–83%), and pre-swing (83–100%) [5,24]. The stance phase of gait was determined combining the force plate and kinematic data [5]. Inter-group comparisons of each demographic, clinical character-
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Fig. 2. Results for midfoot peak plantar pressure (PP) in generic normative bands (GB) and each comparison from 1 to 6: cavus feet (group 1), cavus feet and valgus heel (group 2), cavus feet and hallux valgus (group 3), normal feet (group 4), cavus feet and normally aligned heel (group 5), cavus feet and normal hallux (group 6).
In the analysis of the NoDPN with cavus foot (groups 1, 2, 3, 5 and 6), it can be noticed that some significant alterations are equally revealed by the GB approach and the homogeneous groups approach. These subjects, in the group with cavus foot and valgus heel or cavus foot and normal hallux, displayed a reduced eversion on the midfoot. The group with normal heel and normal or valgus hallux displayed an increased external rotation of the midfoot. Furthermore in the NoDPN subjects with cavus feet the forefoot was found significantly internally rotated. Regarding the PP and LSC data, NoDPN with cavus foot or cavus foot and hallux valgus registered increased peak and mean PP on both the hindfoot and midfoot while the same group with normal heel and hallux alignment displayed only an increased mean PP at the hindfoot. An opposite situation was observed on the data of DPN, where the homogeneous approach highlighted further alterations with respect to GB. These can be summarized as follows: an increased dorsiflexion on the forefoot in the group with cavus foot and valgus heel or valgus hallux, an increased peak PP on the forefoot and a decreased LSC on the hindfoot. However the increased peak PP and decreased LSC on the midfoot highlighted by the GB were not revealed with the present approach. Finally the GB approach did not register significant differences between the hindfoot rotations of either the DPN or the NoDPN and the CS ones.
4. Discussion We applied a four-segment 3D foot kinematic model together with a three-segment foot PP model in order to examine the role of foot morphology on function in DPN and NoDPN. This was performed not only taking into account the pathology but also the type of foot, heel and hallux alignment. In order to avoid inter-operator errors in classifying foot morphology, a single orthopedic surgeon with extensive experience undertook this [12–14,19,27]. This has been shown to improve its reliability with the practice [27]. Subjects with unclear morphology were not taken into consideration. Several papers tried to standardize this classification through invasive or external measurements [11,27], however these methodologies relied on operator-dependent measures, therefore there is still no universally accepted method of evaluating foot morphology. Neuropathy and diabetes subjects displayed significant differences in foot function when the data were not adjusted for type of foot, heel position, or toe deformities: these were found consistent with state of the art [1,3–8,21]. Major differences with other studies adopting different foot models can be attributed to differences in both the kinematics and PP subarea division. When type of foot, heel position, or toe deformities were taken into account, some of the results were not confirmed. In the case of the subjects with normal foot, the foot behavior is nearly the same either in CS or NoDPN, with the exception of an
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increased forefoot PP in the NoDPN group. The high incidence of cavus in diabetic feet [13] suggests that this should be considered strictly related to diabetic pathology and may originate from the thickness of the plantar fascia which is typical of these subjects, as already assessed in the literature [25]. It should be further mentioned that CS with cavus foot displayed a higher peak and mean PP on the forefoot, when compared with CS with normal foot. This is in agreement with [13,26] who demonstrated that foot structure was dominant in predicting peak pressure. In the literature this phenomenon has also been related to submetatarsal pad displacement and/or increased stiffness in NoDPN and DPN [27,28]. In contrast with the findings of Rao [4], the present approach did not highlight any differences in hindfoot kinematics of the hindfoot between CS and NoDPN or DPN. Furthermore when comparing DPN and CS with different type of foot the authors reported the presence of significant differences between midfoot rotations of DPN and CS [21]. This could be attributed to the larger representation of subjects with cavus foot and foot deformities in the DPN group. In the present paper when comparing DPN with CS with the same foot morphology this difference was not registered, thus demonstrating the major role of deformity in altering DPN foot kinematics rather that diabetes itself. However it should be considered that there is a strict relation between diabetes and foot morphology alteration especially in the presence of neuropathy [11–16]. It has been widely demonstrated that diabetic subjects are characterized by excessive ankle rigidity [6,26,29,30] however, foot morphology was not accounted for. In the present paper the angles between the hindfoot and the tibia were not found significantly different between CS and DPN or NoDPN with cavus foot. This found agreement with Bourdiol who stated that the ankle rigidity is mainly determined by the cavus foot itself and should not be attributed only to diabetes [19]. It should be mentioned that Bevans [26] demonstrated that factors limiting ankle joint dorsiflexion are anatomical, physiological or orthopedic in the non-diabetic group, in diabetic subjects glycosylation may be an important factor in altering the joint motion. When considering the PP under the forefoot of the NoDPN with cavus foot, these were found comparable to the CS with the same foot morphology. This should be taken into account as previous studies recorded a high PP, especially in this area, which was considered a high risk zone for ulceration [8–11]. In agreement with Bevans [26], it can be stated that, even without a specific pathology, foot morphology determines the biomechanical behavior and functionality of the foot. Thus the deviations of the biomechanical variables from the norm when the foot structure is altered can pre-exist the diagnosis of diabetes. However these disorders of intrinsic foot structure and function are the cause of calluses and ulcers in the presence of diabetes and in particular of neuropathy which alters the tissue response to the increased PP. Indeed in this specific case altered foot morphologies and deformities are risk factors for foot ulceration [1,11–14]. Finally the differences registered between NoDPN and DPN suggest that they adopt different motor strategies to compensate for foot deformities [5,6], similarly to CS do in the presence of altered foot morphology [26]. The present study may provide important insights into the relationship between elevated PP, kinematics during gait and foot morphology in DPN and NoDPN. It could be considered a valuable tool when there are not solutions to the pathophysiological alterations due to the diabetes and biomechanical alterations, such as foot orthotics, are considered. This finds agreement with Bus [16] who suggested that foot orthotics prescription should be successful when foot biomechanics guide therapy.
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Acknowledgements The authors thank the Imago Ortesi (Piacenza) for providing the plantar pressure systems. We also acknowledge the contribution of Giulia Dona` and Federico Foletto for their help in collecting the data in the initial stages of this research. Conflict of interest statement The authors have no conflict of interest to disclose.
Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.gaitpost .2012.09.024. References [1] Cavanagh PR, Simoneau GG, Ulbrecht JS. Ulceration, unsteadiness, and uncertainty, the biomechanical consequences of diabetes mellitus. Journal of Biomechanics 2003;26(1):23–40. [2] Ledoux W. The biomechanics of the diabetic foot. In: Harris GF, Smith PA, Marks RM, editors. Foot and ankle motion analysis (clinical treatment and technology). USA: CRC Press; 2008. p. 317–401. Chapter 20. [3] Rao S, Saltzman CL, Yack HJ. Relationships between segmental foot mobility and plantar loading in individuals with and without diabetes and neuropathy. Gait and Posture 2010;31(2):251–5. [4] Rao S, Saltzman C, Yack HJ. Segmental foot mobility in individuals with and without diabetes and neuropathy. Clinical Biomechanics 2007;22(4):464–71. [5] Sawacha Z, Cristoferi G, Guarneri G, Corazza S, Dona` G, Denti P, et al. Characterizing multisegment foot kinematics during gait in diabetic foot patients. Journal of NeuroEngineering and Rehabilitation 2009;6:37. [6] Sawacha Z, Guarneri G, Cristoferi G, Guiotto A, Avogaro A, Cobelli C. Diabetic gait and posture abnormalities: a biomechanical investigation through three dimensional gait analysis. Clinical Biomechanics 2009;24(9):722–8. [7] Giacomozzi C, Macellari V, Leardini A, Benedetti MG. Integrated pressureforce-kinematics measuring system for the characterisation of plantar foot loading during locomotion. Medical and Biological Engineering and Computing 2000;38(2):156–63. [8] Giacomozzi C, Martelli F. Peak pressure curve: an effective parameter for early detection of foot functional impairments in diabetic patients. Gait and Posture 2006;23:464–70. [9] Lavery LA, Armstrong DG, Wunderlich RP, Tredwell J, Boulton AJ. Predictive value of foot pressure assessment as part of a population based diabetes disease management program. Diabetes Care 2003;26:1069–73. [10] Mueller MJ, Zou D, Bohnert KL, Tuttle LJ, Sinacore DR. Plantar stresses on the neuropathic foot during barefoot walking. Physical Therapy 2008;88(11):1375–84. [11] Morag E, Cavanagh PR. Structural and functional predictors of regional peak pressures under the foot during walking. Journal of Biomechanics 1999;32:359–70. [12] Ledoux WR, Shofer JB, Ahroni JH, Smith DG, Sangeorzan BJ, Boyko EJ. Biomechanical differences among pes cavus, neutrally aligned, and pes planus feet in subjects with diabetes. Foot and Ankle International 2003;24:845–50. [13] Ledoux WR, Shofer JB, Smith DG, Sullivan K, Hayes SG, Assal M, et al. Relationship between foot type, foot deformity, and ulcer occurrence in the highrisk diabetic foot. Journal of Rehabilitation Research and Development 2005;42:665–72. [14] Cowley MS, Boyko EJ, Shofer JB, Ahroni JH, Ledoux WR. Foot ulcer risk and location in relation to prospective clinical assessment of foot shape and mobility among persons with diabetes. Diabetes Research and Clinical Practice 2008;82(2):226–32. [15] Erdemir A, Saucerman JJ, Lemmon D, Loppnow B, Turso B, Ulbrecht JS, et al. Local plantar pressure relief in therapeutic footwear: design guidelines from finite element models. Journal of Biomechanics 2005;38:1798–806. [16] Bus SA. Foot structure and footwear prescription in diabetes mellitus. Diabetes/Metabolism Research and Reviews 2008;24(Suppl. 1):S90–5. Review. [17] Feldman EL, Stevens MJ, Thomas PK, Browne MB, Canal N, Greene DA. A practical to-step quantitative clinical and electrophysiological assessment for the diagnosis and staging of diabetic neuropathy. Diabetes Care 1994;17(11):1281–9. [18] Consensus statement: Report and recommendations of the San Antonio conference on diabetic neuropathy. American Diabetes Association American Academy of Neurology. Diabetes Care. 1988;11(7):592–7. [19] Ledoux WR, Rohr ES, Ching RP, Sangeorzan BJ. Effect of foot shape on the threedimensional position of foot bones. Journal of Orthopaedic Research 2006;24(12):2176–86.
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[20] Bourdiol JR. Pied et statique. Maisonneuve; 1980. [21] Sawacha Z, Guarneri G, Cristoferi G, Guiotto A, Avogaro A, Cobelli A. Integrated kinematics-kinetics-plantar pressure data analysis: a useful tool for characterizing diabetic foot biomechanics. Gait and Posture 2012;36(1):20–6. [22] Deschamps K, Staes F, Roosen P, Nobels F, Desloovere K, Bruyninckx H, et al. Body of evidence supporting the clinical use of 3D multisegment foot models: a systematic review. Gait and Posture 2011;33(3):338–49. [23] Stebbins JA, Harrington ME, Giacomozzi C, Thompson N, Zavatsky A, Theologis TN. Assessment of sub-division of plantar pressure measurement in children. Gait and Posture 2005;22(4):372–6. [24] Perry J. Gait analysis, normal and pathological function. New York: McGrawHill; 1992. p. 435–6. [25] D’Ambrogi E, Giurato L, D’Agostino MA, Giacomozzi C, Macellari V, Caselli A, et al. Contribution of plantar fascia to the increased forefoot pressures in diabetic patients. Diabetes Care 2003;26:1525.
[26] Bevans JS, Bowker P. Foot structure and function: aetiological risk factors for callus formation in diabetic and non-diabetic subjects. The Foot 1999;9:120– 7. [27] Mueller MJ, Diamond JE, Delitto A, Sinacore DR. Insensitivity, limited joint mobility, and plantar ulcers in patients with diabetes mellitus. Physical Therapy 1989;69:453–9. [28] Chao CY, Zheng YP, Cheing GL. Epidermal thickness and biomechanical properties of plantar tissues in diabetic foot. Ultrasound in Medicine and Biology 2011;37(July (7)):1029–38. [29] Bus SA, Maas M, de Lange A, Michels RP, Levi M. Elevated plantar pressures in neuropathic diabetic patients with claw/hammer toe deformity. Journal of Biomechanics 2005;38(September (9)):1918–25. [30] Rao S, Saltzman C, Yack HJ. Ankle ROM and stiffness measured at rest and during gait in individuals with and without diabetic sensory neuropathy. Gait and Posture 2006;24(November (3)):295–301.
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Gait & Posture journal homepage: www.elsevier.com/locate/gaitpost
The role of foot morphology on foot function in diabetic subjects with or without neuropathy Annamaria Guiotto a,1, Zimi Sawacha a,2, Gabriella Guarneri b,3, Giuseppe Cristoferi b,4, Angelo Avogaro b,5, Claudio Cobelli a,* a b
Department of Information Engineering, University of Padova, Via Gradenigo 6b I, 35131 Padova, Italy Department of Clinical Medicine and Metabolic Disease, University Polyclinic, Via Giustiniani 2, 35128 Padova, Italy
A R T I C L E I N F O
A B S T R A C T
Article history: Received 20 March 2012 Received in revised form 20 September 2012 Accepted 30 September 2012
The aim of this study was to investigate the role of foot morphology, related with respect to diabetes and peripheral neuropathy in altering foot kinematics and plantar pressure during gait. Healthy and diabetic subjects with or without neuropathy with different foot types were analyzed. Three dimensional multisegment foot kinematics and plantar pressures were assessed on 120 feet: 40 feet (24 cavus, 20 with valgus heel and 11 with hallux valgus) in the control group, 80 feet in the diabetic (25 cavus 13 with valgus heel and 13 with hallux valgus) and the neuropathic groups (28 cavus, 24 with valgus heel and 18 with hallux valgus). Subjects were classified according to their foot morphology allowing further comparisons among the subgroups with the same foot morphology. When comparing neuropathic subjects with cavus foot, valgus heel with controls with the same foot morphology, important differences were noticed: increased dorsiflexion and peak plantar pressure on the forefoot (P < 0.05), decreased contact surface on the hindfoot (P < 0.03). While results indicated the important role of foot morphology in altering both kinematics and plantar pressure in diabetic subjects, diabetes appeared to further contribute in altering foot biomechanics. Surprisingly, all the diabetic subjects with normal foot arch or with valgus hallux were no more likely to display significant differences in biomechanics parameters than controls. This data could be considered a valuable support for future research on diabetic foot function, and in planning preventive interventions. ß 2012 Elsevier B.V. All rights reserved.
Keywords: Diabetic foot Foot type Kinematics Plantar pressures Three dimensional
1. Introduction Diabetic and neuropathic subjects (DPN) are at increased risk for ulcer development at sites exposed to repetitive, high plantar loading [1,2]. Several studies have been conducted in the last decade to investigate diabetic foot biomechanics alterations especially in term of foot kinematics and plantar pressure (PP) during gait [1,3–8]. Previous PP studies demonstrated an important correlation between the sites displaying higher PP and the presence of callosities of DPN subjects [8,9]. Stresses were found to
* Corresponding author. Tel.: +39 049 8277661; fax: +39 049 8277699. E-mail addresses: [email protected] (A. Guiotto), [email protected] (Z. Sawacha), [email protected] (G. Guarneri), [email protected] (G. Cristoferi), [email protected] (A. Avogaro), [email protected], [email protected] (C. Cobelli). 1 Tel.: +39 049 8277805; fax: +39 049 8277699. 2 Tel.: +39 049 8277662; fax: +39 049 8277699. 3 Tel.: +39 0498213061; fax: +39 0498213062. 4 Tel.: +39 0498213061; fax: +39 0498213062. 5 Tel.: +39 0498212178; fax: +39 0498754179. 0966-6362/$ – see front matter ß 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.gaitpost.2012.09.024
be relatively higher and located closer to the skin surface where skin breakdown was most likely to occur [10]. Others demonstrated an association between higher peak PP and morphological foot alteration in DPN [8,11]. Ledoux et al. investigated diabetic subjects considering the structural differences between types of foot and demonstrated close relationships between foot morphological alterations and plantar ulcerations [12–14]. Several kinematics studies have compared DPN to control subjects (CS) [5,6]. Although these studies provided insight into the potential influence of diabetes on kinematics during gait, the majority of them considered the foot as a rigid segment and evaluated its motion with respect to the tibia. Only two recent studies [4,5] applied a three-dimensional (3D) multisegment foot kinematic model to evaluate DPN foot kinematics during gait, and observed significant alterations especially in DPN’s forefoot triplanar angles [4,5]. It has also been shown that limited joint mobility may contribute to increased foot subsegments loading by limiting foot flexibility and restraining the forward progression of body weight during the stance phase of gait [3]. However data substantiating the causes and consequences of foot morphology on limited mobility and excessive PP in DPN is limited.
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Table 1 Clinical and demographic characteristics and space-time data of control group (CS), diabetic non neuropathic group (NoDPN) and diabetic neuropathic group (DPN). The reported P values indicate the results of the comparison between the CS and NoDPN groups, the CS and the DPN groups, and the NoDPN and DPN groups (one-way Anova). A value of P < 0.05 was considered statistically significant (P*). Groups
CS # or mean
Subjects [#] Sex [# of males] BMI [kg/m2] Hypertensive disease [#] Age [years] Peripheral neuropathy [#] Autonomic neuropathy [#] Diabetic retinopathy [#] Microalbuminury [#] Vasculopathy [#] Vasculopathy (peripheric) [#] Vasculopathy (TSA) [#] Vasculopathy (coronary) [#] Type of diabetes [#] Hb A1c Years of disease Cavus foot [#] Flat foot [#] Valgus Hindfoot [#] Varus Hindfoot [#] Hallux valgus [#] Foot deformities [#] Plantar callosity [#] Gait velocity (m/s) Stride period (s) Stride length (m) Stance period (s)
20 14 24.41 0 59.35 – – – – – – – – – – – 26 0 22 0 11 12 5 0.998 1.234 1.222 0.762
NoDN SD
# or mean
– –
20 14 26.49 8 62.90 0 0 6 2 2 0 11 4 type1: 3, type2: 17 7.48 16.05
0.123 0.124 0.114 0.086
25 4 13 3 13 10 21 1.102 1.140 1.234 0.668
2.58 4.76 – – – – – – – – –
DN SD
# or mean 20 13 26.24 13 60.30 20 6 12 4 5 3 9 4 type1: 10, type 2: 10 8.12 23.00
2.22 5.63
1.36 11.14
The purpose of this study was to explore the relationship between foot deformities, 3D multisegment foot kinematics and PP during gait in diabetes and DPN. This was pursued by assessing in vivo 3D multisegment foot kinematics [5] and PP of both CS and diabetes subjects with and without neuropathy. Results of this study can be used as a support to design foot orthotic devices [15,16]. Recent literature [15,16] emphasized the importance of considering both foot biomechanics and morphology when planning various foot orthotics devices in order to efficiently reduce plantar ulcer formation and avoid amputation in diabetic subjects. 2. Methods 2.1. Subjects Subjects were recruited among the patients attending the outpatient Clinic at the Department of Metabolic Disease of the University of Padova (Italy). Inclusion criteria were: type 1 and 2 diabetic subjects with walking ability, no history of ulcers or neurological disorders (apart from neuropathy), orthopedic problems, lower limb surgery, cardiovascular disease. CS were recruited among hospital personnel and chosen to be age-, BMI- and gender-matched with the diabetic subjects. On the basis of these criteria 60 patients were examined: 20 CS, 40 diabetic patients (20 without peripheral neuropathy (NoDPN) and 20 DPN). All subjects gave written informed consent. The protocol was approved by the local Ethics Committee. Height and weight were recorded and body mass index (kg/m2) was calculated. The neurological evaluation included the assessment of symptoms, and signs compatible with peripheral nerve dysfunction. The Michigan Neuropathy Screening Instrument questionnaire was used [17]. Subjects were classified as neuropathic if they were found to be positive for three or more out of a total of 15 specified symptoms [18]. The physical examination consisted of: patellar and ankle reflexes, assessment of lower limb muscle strength, sensory testing (pin-prick), touch (10 g Semmens Weinstein monofilament) and vibration perception threshold (128 MHz tuning fork and Biothesiometer), pain sensitivity, electroneurophysiological study, and ankle-to-brachial systolic pressure ratio (Index of Winsor). Cardiovascular autonomic tests were also performed. HbA1c values from the preceding ten years were collected. Each patient had at least one ophthalmologic examination, a urinary albumin-to-creatinine ratio
0.228 0.150 0.183 0.103
SD
3.68 9.60
CS vs NoPN
CS vs PN
NoPN vs PN
P
P
P
0.5 0.009* 0.99 0.037*
0.5 0.074 1 0.694
0.37 0.776 0.94 0.303 1 0.99 0.97 0.81 0.89 0.96 0.26 0.5 type1: 0.99, type2:0.009 0.0909 0.0723
0.41 0.98 0.02* 0.96 0.69 0.31 0.99 0.05 0.005* 0.91 0.0002*
0.68 0.98 0.67 0.96 0.95 0.88 0.99 0.13 0.009* 0.96 0.001*
0.76 0.5 0.99 0.5 0.87 0.95 0.33 0.64 0.51 0.96 0.29
1.57 12.84
28 4 24 3 18 17 19 1.070 1.167 1.230 0.698
0.212 0.105 0.189 0.079
measured, a carotid artery Doppler ultrasound examination, and a 12-leads electrocardiogram in the three months period preceding the study. All subjects underwent clinical examination of the foot by a single orthopedic surgeon experienced in foot and ankle [14,19], in order to ensure reliability of the classifications and be consistent with clinical practice [18]. The type of foot (cavus, planus, normal), foot deformities (hallux valgus/normal/ rigidus, claw and hammer toes, limitation of dorsiflexion of the great toe, abducted/ adducted/overlapping toes), pre-ulceration lesions (calluses, soft corns) and hip, knee, and ankle joint mobility were assessed. Heel position and plantar foot arch during bipedal loading were also evaluated through both footprints [20] and static acquisitions [7] on the PP system. A foot was classified as: cavus if the middle third of the footprint covered less than the 2/3rd of the forefoot print’s width; as planus if the width of the middle third of the footprint exceeded 1/3rd of the full foot width [20]. The heel deviation was evaluated by comparing the Helbing line (drawn along the Achilles tendon) with the vertical one. A valgus deviation higher than 38 was considered as valgus heel. Any deviation toward the varus was considered varus heel [20]. Hallux valgus was defined as a deviation of the great toe toward the lateral side of the foot with a prominence developed over the medial side of the first metatarsal head [13].
2.2. Experimental set up Movement analysis was carried out using a 60 Hz six cameras stereophotogrammetric system (BTS S.r.l, Padova), two force plates (FP4060-10, Bertec Corporation, USA), two PP systems (410 mm 410 mm 0.5 mm, 0.64 cm2 resolution, 150 Hz, Imagortesi, Piacenza). The signals coming from all systems were synchronized in post processing as in [21]. A four-segment 3D foot kinematic model was adopted. This was previously validated in our laboratory [5,21] and it allows the 3D evaluation of ankle, hindfoot, midfoot and forefoot kinematics [21,22]. A three-segment model for the plantar sub-area definition was obtained by means of projecting the anatomical landmarks of the kinematics protocol onto the footprint [21,23]. Thus, for each patient’s foot the hindfoot, midfoot, forefoot subareas were defined as in [21]. The elaboration of PP distribution concentrated on the analysis of some meaningful parameters as in [21]: the center of pressure (COP) mediolateral (ML) and anteroposterior (AP) excursions and the curve integral [6], peak and mean pressure curves (PPC and MPC), and loaded surface curve (LSC). The motion analysis protocol was organized with a static acquisition (subject in an upright posture, with feet placed with ankles together, toes pointed 308 apart and the arms along the body [5,6,21]) and gait analysis sessions.
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Table 2 (a and b) The results of the comparison between the generic groups CS, NoDPN and DPN (GB method – a, homogeneous groups – b). Gray corresponds to those intervals in which there are statistically significant differences between the groups (P < 0.05 from t-test). Only variables with almost one P < 0.05 are reported. hf = hindfoot, mf = midfoot, ff = forefoot, invev = inversion-eversion, i-e rot = intra–extrarotation, dp = dorsiplantarflexion, PP = plantar pressures, LSC = loaded surface curve, COP EXC = center of pressure excursion, ML = medio-lateral, AP = antero-posterior.
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Fig. 1. Results for midfoot–hindfoot inversion–eversion rotation angle in generic normative bands (GB) and each comparison from 1 to 6: cavus feet (group 1), cavus feet and valgus heel (group 2), cavus feet and hallux valgus (group 3), normal feet (group 4), cavus feet and normally aligned heel (group 5), cavus feet and normal hallux (group 6).
Gait analysis: patients walked at a self-selected speed along a walkway; velocity, stride and step parameters were calculated. At least three gait cycles of each limb were recorded for each patient. For each trial, all angular displacements and PP curves were plotted over one stance phase of gait [21].
istic, time and space parameters were performed by means of one-way-Anova (Tukey– Kramer post hoc comparison), and paired t-test after evidence of normality (Lilliefor’s Test) or Kruskal Wallis Test (Matlab software, R2010a).
2.3. Statistical analysis
3. Results
Each subject kinematic and PP variables were represented with the mean of three representative trials. Correlation coefficient (CC) was used to aid in selecting which of each subject’s representative walking trials should be included in the computation of the mean and standard deviation (SD); thus the CC was calculated for each subject’s kinematic and PP parameters. Walking trials with a CC less than 0.75 were excluded from the statistical analysis [6]. Generic normative bands (GB) were created with the data of the CS (GB CS, mean and SD of each variable) and the data of the NoDPN and DPN groups (GB NoDPN and GB DPN) were compared with them without considering foot morphology. Furthermore, subjects were classified according to their foot morphology and each of the three groups (CS, NoDPN and DPN) was split in subgroups according to this classification:
The clinical, demographic characteristics, time and space parameters of the studied subjects were reported in Table 1, and show that all patients were in fair metabolic control. The DPN had a higher prevalence of both micro- and macrovascular complications. Results of the biomechanic analysis are shown in Table 2, Figs. 1 and 2, Appendix. In Table 2 results of the comparison among the CS, the NoDPN and the DPN without taking into account foot morphology (GB approach) have been reported and were found consistent with state of the art [1,3–8,21]. Major differences with other studies adopting different foot models can be attributed to differences in both the kinematics and PP subarea division. However several differences were observed between GB and the approach proposed herein. NoDPN with normal foot (group 4) displayed only a few differences when compared with CS with same foot morphology: increased peak and mean PP were noticed on the forefoot (P < 10 3) together with increased LSC on the midfoot (P < 0.02). As for the DPN’s kinematic data, the alterations revealed from both the GB approach and the homogeneous group one were: decreased eversion on the midfoot and increased eversion on the forefoot and midfoot for the groups with cavus foot and valgus heel or cavus foot and normal hallux. When considering the PP data analysis, excessive peak PP was found on the hindfoot of the DPN.
1. 2. 3. 4. 5. 6.
cavus feet (group 1); cavus feet and valgus heel (group 2); cavus feet and hallux valgus (group 3); normal feet (group 4); cavus feet and normally aligned heel (group 5); cavus feet and normal hallux (group 6).
Mean and SD were computed on each subgroup’s variable over the stance phase of gait and bands were created within each subgroup (mean 1 SD). Afterwards the data within each group were compared: one-way-Anova (Tukey–Kramer post hoc comparison), after evidence of normality (Lilliefor’s Test) or Kruskal Wallis Test was used (Matlab software, R2010a). These tests were performed considering the variables mean value at specific stance phase intervals: initial contact (0–3%), loading response (3–17%), midstance (17–50%), terminal stance (50–83%), and pre-swing (83–100%) [5,24]. The stance phase of gait was determined combining the force plate and kinematic data [5]. Inter-group comparisons of each demographic, clinical character-
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Fig. 2. Results for midfoot peak plantar pressure (PP) in generic normative bands (GB) and each comparison from 1 to 6: cavus feet (group 1), cavus feet and valgus heel (group 2), cavus feet and hallux valgus (group 3), normal feet (group 4), cavus feet and normally aligned heel (group 5), cavus feet and normal hallux (group 6).
In the analysis of the NoDPN with cavus foot (groups 1, 2, 3, 5 and 6), it can be noticed that some significant alterations are equally revealed by the GB approach and the homogeneous groups approach. These subjects, in the group with cavus foot and valgus heel or cavus foot and normal hallux, displayed a reduced eversion on the midfoot. The group with normal heel and normal or valgus hallux displayed an increased external rotation of the midfoot. Furthermore in the NoDPN subjects with cavus feet the forefoot was found significantly internally rotated. Regarding the PP and LSC data, NoDPN with cavus foot or cavus foot and hallux valgus registered increased peak and mean PP on both the hindfoot and midfoot while the same group with normal heel and hallux alignment displayed only an increased mean PP at the hindfoot. An opposite situation was observed on the data of DPN, where the homogeneous approach highlighted further alterations with respect to GB. These can be summarized as follows: an increased dorsiflexion on the forefoot in the group with cavus foot and valgus heel or valgus hallux, an increased peak PP on the forefoot and a decreased LSC on the hindfoot. However the increased peak PP and decreased LSC on the midfoot highlighted by the GB were not revealed with the present approach. Finally the GB approach did not register significant differences between the hindfoot rotations of either the DPN or the NoDPN and the CS ones.
4. Discussion We applied a four-segment 3D foot kinematic model together with a three-segment foot PP model in order to examine the role of foot morphology on function in DPN and NoDPN. This was performed not only taking into account the pathology but also the type of foot, heel and hallux alignment. In order to avoid inter-operator errors in classifying foot morphology, a single orthopedic surgeon with extensive experience undertook this [12–14,19,27]. This has been shown to improve its reliability with the practice [27]. Subjects with unclear morphology were not taken into consideration. Several papers tried to standardize this classification through invasive or external measurements [11,27], however these methodologies relied on operator-dependent measures, therefore there is still no universally accepted method of evaluating foot morphology. Neuropathy and diabetes subjects displayed significant differences in foot function when the data were not adjusted for type of foot, heel position, or toe deformities: these were found consistent with state of the art [1,3–8,21]. Major differences with other studies adopting different foot models can be attributed to differences in both the kinematics and PP subarea division. When type of foot, heel position, or toe deformities were taken into account, some of the results were not confirmed. In the case of the subjects with normal foot, the foot behavior is nearly the same either in CS or NoDPN, with the exception of an
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increased forefoot PP in the NoDPN group. The high incidence of cavus in diabetic feet [13] suggests that this should be considered strictly related to diabetic pathology and may originate from the thickness of the plantar fascia which is typical of these subjects, as already assessed in the literature [25]. It should be further mentioned that CS with cavus foot displayed a higher peak and mean PP on the forefoot, when compared with CS with normal foot. This is in agreement with [13,26] who demonstrated that foot structure was dominant in predicting peak pressure. In the literature this phenomenon has also been related to submetatarsal pad displacement and/or increased stiffness in NoDPN and DPN [27,28]. In contrast with the findings of Rao [4], the present approach did not highlight any differences in hindfoot kinematics of the hindfoot between CS and NoDPN or DPN. Furthermore when comparing DPN and CS with different type of foot the authors reported the presence of significant differences between midfoot rotations of DPN and CS [21]. This could be attributed to the larger representation of subjects with cavus foot and foot deformities in the DPN group. In the present paper when comparing DPN with CS with the same foot morphology this difference was not registered, thus demonstrating the major role of deformity in altering DPN foot kinematics rather that diabetes itself. However it should be considered that there is a strict relation between diabetes and foot morphology alteration especially in the presence of neuropathy [11–16]. It has been widely demonstrated that diabetic subjects are characterized by excessive ankle rigidity [6,26,29,30] however, foot morphology was not accounted for. In the present paper the angles between the hindfoot and the tibia were not found significantly different between CS and DPN or NoDPN with cavus foot. This found agreement with Bourdiol who stated that the ankle rigidity is mainly determined by the cavus foot itself and should not be attributed only to diabetes [19]. It should be mentioned that Bevans [26] demonstrated that factors limiting ankle joint dorsiflexion are anatomical, physiological or orthopedic in the non-diabetic group, in diabetic subjects glycosylation may be an important factor in altering the joint motion. When considering the PP under the forefoot of the NoDPN with cavus foot, these were found comparable to the CS with the same foot morphology. This should be taken into account as previous studies recorded a high PP, especially in this area, which was considered a high risk zone for ulceration [8–11]. In agreement with Bevans [26], it can be stated that, even without a specific pathology, foot morphology determines the biomechanical behavior and functionality of the foot. Thus the deviations of the biomechanical variables from the norm when the foot structure is altered can pre-exist the diagnosis of diabetes. However these disorders of intrinsic foot structure and function are the cause of calluses and ulcers in the presence of diabetes and in particular of neuropathy which alters the tissue response to the increased PP. Indeed in this specific case altered foot morphologies and deformities are risk factors for foot ulceration [1,11–14]. Finally the differences registered between NoDPN and DPN suggest that they adopt different motor strategies to compensate for foot deformities [5,6], similarly to CS do in the presence of altered foot morphology [26]. The present study may provide important insights into the relationship between elevated PP, kinematics during gait and foot morphology in DPN and NoDPN. It could be considered a valuable tool when there are not solutions to the pathophysiological alterations due to the diabetes and biomechanical alterations, such as foot orthotics, are considered. This finds agreement with Bus [16] who suggested that foot orthotics prescription should be successful when foot biomechanics guide therapy.
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Acknowledgements The authors thank the Imago Ortesi (Piacenza) for providing the plantar pressure systems. We also acknowledge the contribution of Giulia Dona` and Federico Foletto for their help in collecting the data in the initial stages of this research. Conflict of interest statement The authors have no conflict of interest to disclose.
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