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Plantar pressure distribution in gait is not affected by targeted reduced plantar cutaneous sensation
Clinical Biomechanics 24 (2009) 308–313
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Plantar pressure distribution in gait is not affected by targeted reduced plantar cutaneous sensation Angela Höhne a,*, Christian Stark b, Gert-Peter Brüggemann a a b
Institute of Biomechanics and Orthopaedics, German Sport University Cologne, Am Sportpark Müngersdorf 6, 50933 Köln, Germany Department of Anaesthesia, Dreifaltigkeitskrankenhaus, Cologne, Germany
a r t i c l e
i n f o
Article history: Received 28 August 2008 Accepted 6 January 2009
Keywords: Diabetes Neuropathy Foot Sensitivity Mechanoreceptors Plantar pressure Gait
a b s t r a c t Background: Plantar ulcers are a common and severe complication of the diabetic neuropathic foot. Increased plantar pressures while walking are associated to incidence of plantar ulcer formation in diabetes. There is a strong correlation between the increase in plantar pressures and the severity of peripheral neuropathy. One consequence of peripheral sensory neuropathy is insensitive skin. The influence of reduced plantar sensitivity on changes in plantar pressure distribution is not well understood. The purpose of this study was to identify possible causal dependences between reduced plantar cutaneous sensation and plantar pressure distribution during gait. Methods: Dynamic pressure distribution in gait and sensory perception threshold for pressure touch and vibration (25 Hz/200 Hz) of the plantar foot were determined pre and post sensory intervention in ten healthy subjects. Cutaneous sensation in both foot soles was experimentally reduced by means of intradermal injections of an anaesthetic solution. This procedure leaves foot and ankle proprioception as well as intrinsic foot muscles unaffected. Findings: The intervention significantly reduced plantar cutaneous sensation to the level of sensory neuropathy. Plantar pressure and force variables, contact times for the entire foot and for the plantar foot regions were not influenced significantly. Interpretation: Experimentally reducing plantar cutaneous sensation causes no changes in plantar pressure distribution while walking. Our findings suggest that in the diabetic neuropathic foot insensitive plantar skin due to peripheral sensory neuropathy may be not a decisive factor for altering plantar pressures. This is underpinning the importance of concomitant affection of different systems secondary to diabetic peripheral neuropathy. Ó 2009 Elsevier Ltd. All rights reserved.
1. Introduction Plantar ulcers are a major complication of the diabetic foot and generate significant reductions in the patient’s quality of life and a substantial economic burden for both the individual and the society. The treatment of foot ulcers and its complications is resource intensive, long term and the most common reason for diabetes-related hospital admission (Gordois et al., 2003). Approximately 15% of people with diabetes develop at least one foot ulcer during their lifetime and up to 85% of lower limb amputations are preceded by foot ulcers (Gordois et al., 2003; Boulton, 2004). To understand the mechanisms contributing to ulceration of the diabetic foot is therefore of considerable interest. Increased pressures under the foot when walking have been shown to be significantly associated to the incidence of plantar ulcer formation in patients with diabetes (Frykberg et al., 1998; Stess et al., 1997; Veves et al., 1992). It * Corresponding author. E-mail address: [email protected] (A. Höhne). 0268-0033/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.clinbiomech.2009.01.001
has been well documented that plantar pressures in diabetic patients are higher than those in healthy subjects (Boulton et al., 1983; Luger et al., 2001). Boulton et al. (1983) reported increased plantar pressures in 17% of patients with diabetes and in 51% of those with diabetes and peripheral neuropathy. Several factors have been identified as possibly being responsible for this increase. These include peripheral motor and sensory neuropathy (Caselli et al., 2002; Frykberg et al., 1998), limited joint mobility, foot deformity (Bus et al., 2005; Mueller et al., 2003; Rao et al., 2007; Robertson et al., 2002) and changes in structure and thickness of the plantar soft tissues (Abouaesha et al., 2001). To which extent the different proposed mechanisms contribute to the increase in plantar pressure in diabetes still remains unknown. Previous studies suggested that the heightening of plantar pressures significantly increases with concomitant occurrence of peripheral neuropathy and with the severity of its symptoms (Caselli et al., 2002; Frykberg et al., 1998; Pham et al., 2000). Parameters of peripheral sensory neuropathy were shown to be highly predictive of increased plantar pressure and increased risk of foot ulceration.
A. Höhne et al. / Clinical Biomechanics 24 (2009) 308–313
Vibration perception of the foot and the inability to sense a 5.07 Semmes–Weinstein Monofilament (10 g) are the most sensitive tests in clinical assessments besides the neuropathy disability score (Frykberg et al., 1998; Pham et al., 2000). One consequence of peripheral sensory neuropathy is insensitive skin, which impairs the sensory feedback of plantar pressure and pain. Plantar cutaneous afferents have been demonstrated to play an important role during human balance control (Meyer et al., 2004a,b; Perry et al., 2000). Location specific information of the foot sole is spatially coded to the central nervous system and contributes to postural responses (Kavounoudias et al., 1998). Reduced plantar cutaneous sensation could thus be considered as a relevant factor for alterations in plantar pressures whilst walking. The influence of insensitive skin on altered plantar pressures in the diabetic neuropathic foot is not understood in detail. The multifactorial character of the diabetic disease, as well as the affection of all components of the peripheral nervous system (sensory, motor and autonomic) in diabetic peripheral neuropathy, make it difficult to ascribe changes in plantar pressures to any single factor. A valuable approach for determining the contribution of plantar sensory feedback to the sensorimotor control processes maintaining posture and gait is to experimentally change plantar sensitivity in healthy subjects. Several studies tried to reduce plantar cutaneous sensation by using ischemic, hypothermic or ankle anaesthesia methods (Do et al., 1990; Nurse and Nigg, 2001; Perry et al., 2000; Thoumie and Do, 1996). But, these methods largely fail to isolate plantar cutaneous sensation from the other foot and ankle somatosensory systems and motor functions. Plantar pressure distribution during walking was investigated before and after foot sole cooling procedures in homogenous groups of young healthy subjects by using pressure platforms (Eils et al., 2002; Taylor et al., 2004) and pressure insoles (Nurse and Nigg, 2001). Ice immersion induced an obvious altered roll-over strategy of the foot as seen in a more cautious, rigid walking pattern (Eils et al., 2002; Taylor et al., 2004). Therefore it was almost obvious that the observed changes in plantar pressure and force variables (Eils et al., 2002; Nurse and Nigg, 2001; Taylor et al., 2004) should appear. Moreover, the results are to some extent contradictory, in particular for the peak plantar pressures. Exemplarily, increased peak plantar pressures at the forefoot region were reported by Nurse and Nigg (2001) and Taylor et al. (2004), whereas Eils et al. (2002) found solely decreased peak plantar pressures after ice immersion. An important drawback of hypothermic protocols is that cooling procedures do not exclusively influence plantar cutaneous receptors and therefore an affection of intrinsic foot muscles and joint receptors can not be excluded. In addition, the time window for testing the foot sole cooling intervention is limited to only one or two steps due to a quick warm-up process, as reported by Eils et al. (Eils et al., 2002; Taylor et al., 2004). The influence of insensitive skin due to peripheral sensory neuropathy on changes in plantar pressures is not well understood. Moreover, the mechanisms relating reduced plantar cutaneous feedback to changes in plantar pressure distribution and force variables during walking remain unclear. In consequence, the purpose of this study was to identify possible causal dependences between reduced plantar cutaneous sensation and plantar pressure distribution during gait. A specifically designed anaesthesia procedure targeting solely the end-organs of the plantar cutaneous mechanoreceptors was used. This way foot and ankle proprioception as well as intrinsic foot muscles were left unaffected (Meyer et al., 2004a, b). In contrast to previous hypothermic protocols, the effects were analysed after a longer period of experimentally reduced sensation. It was expected: that (a) a selective reduction of plantar cutaneous sensation would cause significant changes in plantar pressure and force variables during walking and that (b) alterations in plantar
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pressures similar to those seen in diabetic peripheral neuropathy would be observed. 2. Methods 2.1. Subjects Ten healthy subjects, six males and four females, (mean age 23.6, standard deviation: SD 1.9 yr; mean height 178.4, SD 8.9 cm; mean mass: 76.3, SD 12.0 kg) volunteered for the study. The study was approved by the intern ethical committee of the German Sport University Cologne. All subjects were informed in detail about the nature of the study and gave their written informed consent prior to participation. Each of the subjects underwent a physical examination and filled out a clinical routine-questionnaire to exclude any neurological disorders or musculoskeletal diseases, which could influence the experimental outcome, as well as possible allergic reactions against the anaesthetic solution. 2.2. Experimental protocol Baseline values (pre condition) for the sensory perception threshold (SPT) of the plantar foot and for the dynamic pressure distribution while walking were taken prior to the sensory intervention. Subsequently, the subjects underwent the anaesthesia procedure. The SPT of the plantar foot was evaluated again to quantify the immediate effect of the anaesthesia on plantar sensitivity (post condition 1). During the next 40–60 min the subjects performed a gait perturbation protocol (22 trials) along a walkway with unexpected changes in surface stiffness which is not discussed in the present paper. This protocol provided walking experience, allowing the subjects to get familiar to the sensory changes. Afterwards, dynamic pressure distribution while walking with reduced plantar sensitivity was measured (post condition). At the end of the experiment, the SPT of the plantar foot was quantified again, to assess the effect of the sensory intervention (post condition 2). 2.3. Sensory perception threshold evaluation The SPT of the plantar foot was determined by two validated tests for clinical assessment of peripheral sensory neuropathy: pressure touch and vibration perception (Caselli et al., 2002; Frykberg et al., 1998; Pham et al., 2000). Three plantar test regions at the right foot – centre of the second and third metatarsal head representing the forefoot, centre of the lateral midfoot and the centre of heel were choosen and tested in random order to assess the effect of the sensory intervention on plantar sensitivity. These test regions were marked to ensure that pre- and post-sensitivity tests were carried out on the same plantar regions. The SPT of pressure touch was quantified with a set of 20 Semmes–Weinstein monofilaments (SWMF) (North Coast Medical, Inc., Morgan Hill, USA). The calibrated filaments vary in diameter in correlation with a known bending force (filament size = log10 of [10 force in milligrams]). To determine the sensory threshold level of the tested region we used the 4, 2, 1 stepping algorithm (Dyck et al., 1993) and a forced-choice method (Chong and Cros, 2004). The test started at an intermediate level, filament 4.31 (pre condition) and filament 5.07 (post condition 1, 2). The subjects laid supine with eyes closed in a quiet room, then the filaments were applied perpendicularly to the skin surface at the test regions and pushed until bending. Depending on the subject’s answer, the stimulus was increased or decreased in four filament steps until a turnaround point was reached. Then the test was carried out in 2 filament steps and 1 filament steps, respectively, until three consecutive failures
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were observed. The lightest filament leading to a response, was determined to be the sensory threshold level for the tested region. To improve the accuracy of the test, five null-stimuli were applied randomly at the test algorithm. Sensory loss is clinically detected by the inability to sense filament 5.07 (115 mN) at two of three sites on plantar surface (Frykberg et al., 1998; Holewski et al., 1988). About 70% of the cutaneous mechanoreceptors at the human foot sole are the rapidly adapting FAI (Meissner corpuscles) and FAII (Pacinian corpuscles) receptors (Kennedy and Inglis, 2002). FAI receptors mainly mediate low frequencies and FAII receptors solely transmit high frequencies (Kekoni et al., 1989). Therefore, to quantify the effect of the sensory intervention on the different mechanoreceptor’s modalities, the vibration perception was evaluated using both frequency spectrums (25 Hz/200 Hz). A custom modified HVLab Tactile Vibrometer was used (Institute of Sound and Vibration Research, University Southampton, UK). The Vibrometer unit housed an electrodynamic vibrator, which was mounted on a counterbalance, so as to provide a constant upward contact force (1 N) between the application probe and the skin surface. An accelerometer was mounted on the vibrator, with the application probe connected to its upper surface. The subjects sat comfortably in a chair with an adjustable support for the right lower leg, allowing a horizontal positioning of the right foot sole. Then the application probe (perspex probe, 5 mm diameter) was placed without any surrounding contact, perpendicularly to the plantar test region with a skin indentation contact force of 1 N (±0.1 N). The subjects wore ear muffs to shield any environment or equipment noise. Test frequencies and plantar test regions were chosen in random order. The sinusoidal vibration stimulus was applied using the Békésy method of increasing and decreasing rates based on a standardised test protocol (ISO, 2001). The subject had to press a response button as long as the vibration sensation could be perceived. The amplitude of the vibration increased until the subject pressed the response button (appearance threshold). Then the amplitude decreased until the button was released (disappearance threshold). This procedure was repeated several times in order to determine the threshold level, i.e. the mean value of the mean appearance and mean disappearance thresholds at a minimum of 6 reversals. The displacement was calculated from the acceleration wave by
X¼
middle of a 10 m walkway. The pressure platform contains four calibrated capacitive sensors per cm2 with a total sensing area of 475 320 mm. Data were collected at 100 Hz sampling frequency. All subjects performed five barefoot gait trials at an individually chosen velocity at each condition. The third-step method was used, meaning that the third-step after gait initiation was hitting the platform. Using this method, five trials have shown to provide reproducible values (Bus and De Lange, 2005). Subjects performed up to four test trials to familiarize themselves with the protocol and to determine their starting position. Then, five consecutive
A ð2pf Þ2
where X is the displacement, A is the acceleration and f is the vibration frequency (Griffin, 1990). The room and plantar foot skin temperatures were controlled to exclude an affection of the SPT by changes in temperature (Laser temperature measurement device, Testo 825-T4, Testo AG, Lenzkirch, Gemany). 2.4. Dynamic pressure distribution measurement Dynamic pressure distribution was measured by an EMED-X platform (novel GmbH, Munich, Germany) mounted flush in the
Fig. 1. Mask defining the ten plantar foot regions for analysis of plantar pressure and force variables. MHE – medial heel, LHE – lateral heel, MMF – medial midfoot, LMF – lateral midfoot, MT1 – first metatarsal region, MT2 – second metatarsal region, MT 345 – metatarsal region 3, 4, 5, HAL – hallux, 2TO – second toe, 345TO – toes 3, 4, 5.
Fig. 2. Mean values and standard error of mean of the sensory perception threshold (SPT) at the plantar foot regions for pressure touch (A) and vibration (25/200 Hz) (B) before anaesthesia (pre), after anaesthesia (post 1) and after finishing the pressure distribution measurement (post 2). Statistically significant differences (P < 0.05) between: * pre and post 1, pre and post 2, à post 1 and post 2.
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A. Höhne et al. / Clinical Biomechanics 24 (2009) 308–313 Table 1 Mean values and standard deviations for contact time (% roll-over process), peak pressure (kPa) and pressure–time integral (kPas). Foot region
Contact time (% ROP) Pre
Medial heel Lateral heel Medial midfoot Lateral midfoot Metatarsal 1 Metatarsal 2 Metatarsal 3, 4, 5 Hallux Second toe Toes 3, 4, 5
49.9 49.4 30.0 58.2 77.3 81.5 83.4 65.7 54.8 63.9
Peak pressure (kPa) Post
(5.3) (5.1) (12.1) (4.5) (3.9) (2.4) (2.8) (12.9) (6.6) (8.2)
48.2 47.8 33.3 58.2 78.2 81.5 83.6 69.1 54.9 65.1
Pre (4.4) (4.2) (8.6) (6.2) (3.5) (2.8) (2.6) (9.7) (5.3) (13.7)
548.0 528.7 84.9 136.8 354.1 563.9 516.2 435.4 285.7 194.8
Pressure–time integral (kPas) Post
(126.1) (130.3) (42.3) (26.3) (135.0) (228.4) (228.0) (120.5) (86.1) (62.9)
505.0 476.1 92.2 138.2 324.1 557.5 555.2 421.6 210.0 159.0
Pre (138.5) (103.8) (32.1) (25.5) (76.7) (204.5) (284.0) (160.2) (83.2) (67.8)
Post
95.3 89.6 13.5 34.4 90.5 143.8 146.2 99.5 55.7 42.2
(26.0) (23.1) (7.9) (9.3) (20.1) (45.8) (57.0) (36.1) (21.6) (14.6)
89.1 83.0 14.6 34.1 87.5 141.1 152.5 96.9 40.5 36.3
(27.9) (21.4) (5.7) (8.5) (20.3) (47.7) (70.9) (43.1) (17.4) (18.2)
Statistically significant differences (P < 0.05) before (pre) and after (post) the sensory intervention.
trials were measured. Contact time, peak pressure, pressure–time integral, maximum force and force–time integral for the entire foot and ten plantar regions were calculated and analysed. The ten plantar foot regions were defined according to Cavanagh and Ulbrecht (1992) in medial heel, lateral heel, medial midfoot, lateral midfoot, metatarsal region 1, metatarsal region 2, metatarsal region 3/4/5, hallux, second toe and toe 3/4/5 (Fig. 1). The data were calculated for each trial and then averaged for each subject and condition (novel scientific software, novel GmbH, Munich, Germany). 2.5. Sensory intervention Sensation from the weight-bearing surface of both foot soles was locally reduced through multiple intradermal injections of an anaesthetic solution using a modified procedure from Meyer et al. (2004a). The anaesthetic solution (2% lidocaine HCl, 1:8 sodium bicarbonate, 1:200,000 epinephrine, 12 U/mg hyaluronidase) was intradermally applied by an anaesthesiologist using 30-gauge needles. Effective anaesthesia results were achieved by eight to twelve 0.8 ml injections for each foot. This method targets the end-organs of the cutaneous mechanoreceptors leaving joint and muscle afferents unaffected. No changes in elastic skin compliance and no affection of the proprioception of the foot were reported (Meyer et al., 2004a,b). Sensation at the skin of the forefoot, the lateral foot and heel, i.e. the weight-bearing surface with exception of the toes, was locally reduced. The toes remained untreated as the use of epinephrine in the digits is precluded. The whole procedure took about 1 h for both feet and was well tolerated by all subjects. 2.6. Statistical analysis For statistical analysis, a one-way ANOVA for repeated measurements was performed for the sensitivity tests (pre condition, post condition 1 and 2). A paired t-test for dependent samples was used to determine possible differences in the dynamic pressure distribution variables (pre and post condition). The statistical level of significance was set at P < 0.05 for all analyses, which were conducted using SPSS (Version 14.0, SPSS Inc., Chicago, Illinois, USA). 3. Results 3.1. Plantar cutaneous sensation Plantar cutaneous sensation was significantly reduced compared to the baseline values (pre condition) during the entire experimental period (post condition 1, 2) (Fig. 2). The SPT for pressure touch was significantly increased reaching the criteria values
of peripheral sensory neuropathy (filament 5.07) at all plantar test regions (Fig. 2A). Immediately after the anaesthesia (post condition 1), the filament size was increased at the forefoot from mean (SD) 4.01 (0.5) to 6.1 (0.6), P < 0.000; at the lateral foot from 3.73 (0.5) to 5.7 (0.8), P < 0.000 and at the heel from 4.21 (0.3) to 6.1 (0.7), P < 0.000. At post condition 2 (after finishing the pressure distribution measurement), the SPT for pressure touch was still significantly higher than the pre condition at all plantar test regions: forefoot mean (SD) 5.77 (0.8), P < 0.000; lateral foot 5.79 (0.8), P < 0.000 and heel 5.04 (0.9), P < 0.003. Similarly, the SPT for low (25 Hz) and high (200 Hz) frequency vibration was significantly increased at the plantar test regions (Fig. 2B). The results are presented for nine out of ten subjects, because one subject was not able to perceive the vibration stimulus after anaesthesia. The SPT at both 25 Hz and 200 Hz was increased by about 100% at the forefoot (P < 0.001), at lateral foot (P < 0.001) and at heel (P < 0.005) at both post sensory intervention conditions (post condition 1, 2), as compared to the baseline values (pre condition). Some previous studies evaluated the SPT for vibration at the plantar foot using different test protocols (Kekoni et al., 1989; Nurse and Nigg, 2001; Wells et al., 2003). Differences in the stimulus application, such as presence or absence of surround contact, diameter of the application probe, skin contact force or skin indentation, all may influence the results (Chong and Cros, 2004). Taking these methodological difficulties into account, our results for the SPT for vibration (25 Hz/200 Hz) at pre condition were within similar ranges as those of these previous studies. Likewise, the SPT for pressure touch at pre condition were in agreement with the results of studies in young healthy subjects (Eils et al., 2002; Nurse and Nigg, 2001; Taylor et al., 2004). Maximal pre-post differences in skin and room temperature were below 3 degrees. These differences were considerably lower Table 2 Mean values and standard deviations for maximum force (N) and force–time integral (relative values of total foot in %). Foot region
Maximum force (N) Pre
Medial heel Lateral heel Medial midfoot Lateral midfoot Metatarsal 1 Metatarsal 2 Metatarsal 3, 4, 5 Hallux Second toe Toes 3, 4, 5
376.5 317.5 9.8 142.1 187.4 238.5 335.6 191.9 45.5 49.9
Force–time integral (%)
Post (87.6) (61.7) (6.7) (42.9) (49.9) (60.3) (98.9) (63.0) (20.1) (20.8)
363.4 310.5 10.9 147.3 187.0 229.0 330.4 173.8 35.2 43.5
Pre (72.3) (56.9) (7.9) (41.9) (37.9) (51.0) (103.1) (64.1) (23.3) (27.8)
15.3 12.8 0.3 6.9 11.5 15.7 24.7 8.7 1.9 2.2
Post (1.6) (1.0) (0.3) (1.9) (2.7) (2.4) (3.3) (3.1) (0.9) (1.2)
14.8 12.8 0.4 7.3 12.2 15.9 24.9 8.4 1.4 2.0
(2.2) (0.8) (0.3) (1.8) (3.0) (2.5) (4.3) (2.8) (0.9) (1.5)
Statistically significant differences (P < 0.05) before (pre) and after (post) the sensory intervention.
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Table 3 Mean values and standard deviations for entire foot before (pre) and after (post) the sensory intervention. Parameter
Condition Pre
Contact time (ms) Peak pressure (kPa) Pressure–time integral (kPas) Maximum force (N) Force–time integral (Ns)
665.2 702.9 253.4 997.5 443.1
Post (44.0) (191.5) (58.7) (191.8) (85.3)
653.4 710.3 255.0 974.9 424.6
(50.3) (223.9) (75.7) (172.0) (81.7)
than those which could potentially influence the evaluation of the SPT during the measurements (ISO, 2001). 3.2. Plantar pressure distribution Data analysis was conducted for ten plantar regions (Table 1 and 2) and for the entire foot (Table 3) for contact time, peak pressure, pressure–time integral, maximum force and force–time integral. All analysed plantar pressure and force variables as well as contact times for the different regions and the entire foot were not significantly changed after the sensory intervention with exception of second toe. In this region, plantar pressure and force variables were reduced (P < 0.05) (Table 1 and 2). No increase in plantar pressures or forces was observed at any of the ten plantar foot regions or the entire foot after the sensory intervention. 4. Discussion The purpose of this study was to identify possible causal dependences between reduced plantar cutaneous sensation and plantar pressure distribution in gait. Furthermore, it was investigated whether changes occurring in plantar pressure distribution after reduced plantar cutaneous sensation resemble those seen in the diabetic neuropathic foot. The applied sensory intervention led to a significant reduction in plantar cutaneous feedback during the entire experimental period at all plantar test regions (forefoot, lateral foot and heel). The SPT for vibration (25/200 Hz) was significantly increased indicating a reduction in sensitivity of the FAI and FAII mechanoreceptors in the foot sole. Similarly, the SPT for pressure touch was clearly above the sensory threshold level of filament 5.07 (SWMF) for clinical detection of peripheral sensory neuropathy (Holewski et al., 1988; Pham et al., 2000). The anaesthesia method targeted solely the plantar cutaneous mechanoreceptor end-organs while leaving foot and ankle proprioception and intrinsic foot muscles unaffected as previously shown by Meyer et al. (2004a,b). Plantar pressures were recorded 48 min (SD 10 min) after anaesthesia and allowed therefore to observe the effects on plantar pressure distribution during walking after a longer period of reduced sensation and having had anaesthetised walking experience. The analysed variables – peak pressure, pressure–time integral, maximum force, force– time integral and contact time – did not change neither for the different foot regions nor for the entire foot. The results of our study suggest that targeted reduced plantar cutaneous sensation in healthy subjects does not cause significant changes in plantar pressure distribution whilst walking. Some methodological limitations of the study have to be acknowledged. Ethical considerations due to the invasive nature of the anaesthesia procedure restricted the sample size (n = 10). The reduction in statistical sensitivity due to small sample size was partially compensated by studying a homogeneous sample. Statistical sensitivity to detect significantly differences in plantar pressure and force variables could be therefore limited. In addition,
it has also to be considered that short time sensory loss of plantar cutaneous feedback differs from long-standing peripheral sensory neuropathy in patients with diabetes where long time strategies could be developed. However, as previously mentioned, most of the affected patients with diabetes develop a combination of risk factors (Abouaesha et al., 2001; Mueller et al., 2003; Rao et al., 2007; Robertson et al., 2002), which make it almost impossible to study isolated causal relations in this population. In particular the simultaneous affection of the sensory, motor and autonomic components of the peripheral nervous system (Frykberg et al., 1998; Greenman et al., 2005; Pham et al., 2000), restricts the possibility to address changes in plantar pressures to a single factor. Hence experimental interventions in healthy subjects are a valuable approach to provide usefully insights into the role of peripheral sensory neuropathy on altered plantar pressures in patients with diabetes. It is well established that plantar pressure variables as peak pressure and pressure loading over time (pressure–time integral) are increased in these patients (Boulton et al., 1983; Luger et al., 2001; Stess et al., 1997). Especially the metatarsal region is affected by an elevated ulceration risk due to increased plantar pressures (Stess et al., 1997; Veves et al., 1992). The increase of the different plantar pressure distribution variables and the risk for plantar ulceration were found to be highly correlated with concomitant occurrence and severity of peripheral neuropathy (Caselli et al., 2002; Frykberg et al., 1998; Pham et al., 2000). A more recent study using magnetic resonance imaging suggested that intrinsic foot muscle atrophy due to motor neuropathy is evident already before sensory neuropathy is detected by clinical screening techniques (Greenman et al., 2005). A possible explanation for changes in plantar pressures could be intrinsic foot muscle atrophy and the related decrease of force capacities. The consequences of intrinsic foot muscle atrophy, such as imbalances between flexor and extensor muscles resulting in toe deformity (clawing, hammer toes), as well as prominent metatarsal heads, limited joint mobility and decreased thickness of plantar soft tissue (muscle tissue), have been considered as factors contributing to an in increase in plantar pressures and ulceration risk primarily at the metatarsal region (Bus et al., 2005; Frykberg et al., 1998; Mueller et al., 2003; Robertson et al., 2002). The results of our study do not confirm the findings of hypothermic studies using cooling procedures to reduce plantar cutaneous feedback in young healthy subjects. Plantar pressure distribution while walking was investigated in ten subjects (mean age: 26.1, SD 4.1 yr) by using pressure insoles (Nurse and Nigg, 2001), in a group of 15 subjects (25.7, SD 4.1 yr) by using a pressure platform (Taylor et al., 2004) and in a group of 40 subjects (25.3, SD 3.3 yr) by using a pressure platform as well (Eils et al., 2002). Foot sole cooling led to significant changes in plantar pressure and force variables while walking (Eils et al., 2002; Nurse and Nigg, 2001; Taylor et al., 2004). Two studies observed a visibly altered, more rigid and cautious roll-over pattern of the foot after ice immersion (Eils et al., 2002; Taylor et al., 2004). Higher loads after ice immersion were reported for the forefoot and lateral midfoot. These resulted into an increase of peak pressure, pressure–time integral (Nurse and Nigg, 2001; Taylor et al., 2004), maximum force (Taylor et al., 2004), force–time integral (Eils et al., 2002; Nurse and Nigg, 2001; Taylor et al., 2004) and longer contact times (Eils et al., 2002; Taylor et al., 2004). Decreased pressure and force values were reported for the toe and heel regions (Eils et al., 2002; Nurse and Nigg, 2001; Taylor et al., 2004). One study also described a considerable reduction in walking speed after ice immersion (Taylor et al., 2004). Taking our results into account, it might be concluded that the former observed changes in plantar pressure distribution after foot sole cooling were more likely caused by an altered rollover strategy of the foot and an affection of intrinsic foot muscles and joint receptors than by plantar cutaneous sensation. The more
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rigid walking style might be a sign for an affection of joint mobility at the forefoot region. Decreased force capacities and limited joint mobility were recognized to be related to an increase in plantar pressures at the forefoot region (Rao et al., 2007; Robertson et al., 2002). The targeted reduction of plantar cutaneous sensation by locally applying intradermal anaesthesia did not change plantar pressure and force variables or contact times in a comparable group of healthy subjects. The differing results can be explained by the different methodologies. The main finding of the present study is that targeted reduced plantar cutaneous sensation in healthy subjects does not affect plantar pressure distribution while walking. Alterations of plantar pressures while walking similar to those in diabetic peripheral neuropathy could not be observed. 5. Conclusions This study demonstrated that experimentally reduced plantar cutaneous sensation without any affection of foot and ankle proprioception and intrinsic foot muscles causes no changes in plantar pressure distribution while walking. Our findings suggest that in the diabetic neuropathic foot, insensitive plantar skin due to peripheral sensory neuropathy may be not a decisive factor for alterations in plantar pressures. These results help underpinning the importance of concomitant affection of different systems secondary to diabetic peripheral neuropathy with regard to increased plantar pressures in diabetic patients. Acknowledgment We would like to thank Dr. Gaspar Morey Klapsing for his contribution to improving the manuscript. References Abouaesha, F., Van Schie, C.H., Griffths, G.D., Young, R.J., Boulton, A.J., 2001. Plantar tissue thickness is related to peak plantar pressure in the high-risk diabetic foot. Diabetes Care 24, 1270–1274. Boulton, A.J., 2004. The diabetic foot: from art to science. The 18th Camillo Golgi lecture. Diabetologia 47, 1343–1353. Boulton, A.J., Hardisty, C.A., Betts, R.P., Franks, C.I., Worth, R.C., Ward, J.D., Duckworth, T., 1983. Dynamic foot pressure and other studies as diagnostic and management aids in diabetic neuropathy. Diabetes Care 6, 26–33. Bus, S.A., De Lange, A., 2005. A comparison of the 1-step, 2-step, and 3-step protocols for obtaining barefoot plantar pressure data in the diabetic neuropathic foot. Clin. Biomech. 20, 892–899. Bus, S.A., Maas, M., De Lange, A., Michels, R.P., Levi, M., 2005. Elevated plantar pressures in neuropathic diabetic patients with claw/hammer toe deformity. J. Biomech. 38, 1918–1925. Caselli, A., Pham, H., Giurini, J.M., Armstrong, D.G., Veves, A., 2002. The forefoot-torearfoot plantar pressure ratio is increased in severe diabetic neuropathy and can predict foot ulceration. Diabetes Care 25, 1066–1071. Cavanagh, P.R., Ulbrecht, J.S., 1992. Clinical plantar pressure measurement in diabetes: rationale and methodology. Foot 4, 123–135. Chong, P.S., Cros, D.P., 2004. Technology literature review: quantitative sensory testing. Muscle Nerve 29, 734–747. Do, M.C., Bussel, B., Breniere, Y., 1990. Influence of plantar cutaneous afferents on early compensatory reactions to forward fall. Exp. Brain. Res. 79, 319–324.
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Dyck, P.J., O’brien, P.C., Kosanke, J.L., Gillen, D.A., Karnes, J.L., 1993. A 4, 2, and 1 stepping algorithm for quick and accurate estimation of cutaneous sensation threshold. Neurology 43, 1508–1512. Eils, E., Nolte, S., Tewes, M., Thorwesten, L., Volker, K., Rosenbaum, D., 2002. Modified pressure distribution patterns in walking following reduction of plantar sensation. J. Biomech. 35, 1307–1313. Frykberg, R.G., Lavery, L.A., Pham, H., Harvey, C., Harkless, L., Veves, A., 1998. Role of neuropathy and high foot pressures in diabetic foot ulceration. Diabetes Care 21, 1714–1719. Gordois, A., Scuffham, P., Shearer, A., Oglesby, A., Tobian, J.A., 2003. The health care costs of diabetic peripheral neuropathy in the US. Diabetes Care 26, 1790–1795. Greenman, R.L., Khaodhiar, L., Lima, C., Dinh, T., Giurini, J.M., Veves, A., 2005. Foot small muscle atrophy is present before the detection of clinical neuropathy. Diabetes Care 28, 1425–1430. Griffin, M.J., 1990. Handbook of Human Vibration. Academic Press, London. Holewski, J.J., Stess, R.M., Graf, P.M., Grunfeld, C., 1988. Aesthesiometry: quantification of cutaneous pressure sensation in diabetic peripheral neuropathy. J. Rehabil. Res. Dev. 25, 1–10. ISO, International Organisation for Standardization, 2001. Mechanical vibration. Vibrotactile Perception Thresholds for the Assessment of Nerve Dysfunction. Part 1. ISO 13091-1. Kavounoudias, A., Roll, R., Roll, J.P., 1998. The plantar sole is a ‘dynamometric map’ for human balance control. Neuroreport 9, 3247–3252. Kekoni, J., Hamalainen, H., Rautio, J., Tukeva, T., 1989. Mechanical sensibility of the sole of the foot determined with vibratory stimuli of varying frequency. Exp. Brain. Res. 78, 419–424. Kennedy, P.M., Inglis, J.T., 2002. Distribution and behaviour of glabrous cutaneous receptors in the human foot sole. J. Physiol. 538, 995–1002. Luger, E., Nissan, M., Karpf, A., Steinberg, E., Dekel, S., 2001. Dynamic pressures on the diabetic foot. Foot Ankle Int. 22, 715–719. Meyer, P.F., Oddsson, L.I., De Luca, C.J., 2004a. The role of plantar cutaneous sensation in unperturbed stance. Exp. Brain. Res. 156, 505–512. Meyer, P.F., Oddsson, L.I., De Luca, C.J., 2004b. Reduced plantar sensitivity alters postural responses to lateral perturbations of balance. Exp. Brain. Res. 157, 526– 536. Mueller, M.J., Hastings, M., Commean, P.K., Smith, K.E., Pilgram, T.K., Robertson, D., Johnson, J., 2003. Forefoot structural predictors of plantar pressures during walking in people with diabetes and peripheral neuropathy. J. Biomech. 36, 1009–1017. Nurse, M.A., Nigg, B.M., 2001. The effect of changes in foot sensation on plantar pressure and muscle activity. Clin. Biomech. 16, 719–727. Perry, S.D., Mcilroy, W.E., Maki, B.E., 2000. The role of plantar cutaneous mechanoreceptors in the control of compensatory stepping reactions evoked by unpredictable, multi-directional perturbation. Brain Res. 877, 401–406. Pham, H., Armstrong, D.G., Harvey, C., Harkless, L.B., Giurini, J.M., Veves, A., 2000. Screening techniques to identify people at high risk for diabetic foot ulceration: a prospective multicenter trial. Diabetes Care 23, 606–611. Rao, S., Saltzman, C., Yack, H.J., 2007. Segmental foot mobility in individuals with and without diabetes and neuropathy. Clin. Biomech. 22, 464–471. Robertson, D.D., Mueller, M.J., Smith, K.E., Commean, P.K., Pilgram, T., Johnson, J.E., 2002. Structural changes in the forefoot of individuals with diabetes and a prior plantar ulcer. J. Bone Joint Surg. Am. 84-A, 1395–1404. Stess, R.M., Jensen, S.R., Mirmiran, R., 1997. The role of dynamic plantar pressures in diabetic foot ulcers. Diabetes Care 20, 855–858. Taylor, A.J., Menz, H.B., Keenan, A.M., 2004. Effects of experimentally induced plantar insensitivity on forces and pressures under the foot during normal walking. Gait Posture 20, 232–237. Thoumie, P., Do, M.C., 1996. Changes in motor activity and biomechanics during balance recovery following cutaneous and muscular deafferentation. Exp. Brain. Res. 110, 289–297. Veves, A., Murray, H.J., Young, M.J., Boulton, A.J., 1992. The risk of foot ulceration in diabetic patients with high foot pressure: a prospective study. Diabetologia 35, 660–663. Wells, C., Ward, L.M., Chua, R., Inglis, J.T., 2003. Regional variation and changes with ageing in vibrotactile sensitivity in the human footsole. J. Gerontol. A Biol. Sci. Med. Sci. 58, 680–686.
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Clinical Biomechanics journal homepage: www.elsevier.com/locate/clinbiomech
Plantar pressure distribution in gait is not affected by targeted reduced plantar cutaneous sensation Angela Höhne a,*, Christian Stark b, Gert-Peter Brüggemann a a b
Institute of Biomechanics and Orthopaedics, German Sport University Cologne, Am Sportpark Müngersdorf 6, 50933 Köln, Germany Department of Anaesthesia, Dreifaltigkeitskrankenhaus, Cologne, Germany
a r t i c l e
i n f o
Article history: Received 28 August 2008 Accepted 6 January 2009
Keywords: Diabetes Neuropathy Foot Sensitivity Mechanoreceptors Plantar pressure Gait
a b s t r a c t Background: Plantar ulcers are a common and severe complication of the diabetic neuropathic foot. Increased plantar pressures while walking are associated to incidence of plantar ulcer formation in diabetes. There is a strong correlation between the increase in plantar pressures and the severity of peripheral neuropathy. One consequence of peripheral sensory neuropathy is insensitive skin. The influence of reduced plantar sensitivity on changes in plantar pressure distribution is not well understood. The purpose of this study was to identify possible causal dependences between reduced plantar cutaneous sensation and plantar pressure distribution during gait. Methods: Dynamic pressure distribution in gait and sensory perception threshold for pressure touch and vibration (25 Hz/200 Hz) of the plantar foot were determined pre and post sensory intervention in ten healthy subjects. Cutaneous sensation in both foot soles was experimentally reduced by means of intradermal injections of an anaesthetic solution. This procedure leaves foot and ankle proprioception as well as intrinsic foot muscles unaffected. Findings: The intervention significantly reduced plantar cutaneous sensation to the level of sensory neuropathy. Plantar pressure and force variables, contact times for the entire foot and for the plantar foot regions were not influenced significantly. Interpretation: Experimentally reducing plantar cutaneous sensation causes no changes in plantar pressure distribution while walking. Our findings suggest that in the diabetic neuropathic foot insensitive plantar skin due to peripheral sensory neuropathy may be not a decisive factor for altering plantar pressures. This is underpinning the importance of concomitant affection of different systems secondary to diabetic peripheral neuropathy. Ó 2009 Elsevier Ltd. All rights reserved.
1. Introduction Plantar ulcers are a major complication of the diabetic foot and generate significant reductions in the patient’s quality of life and a substantial economic burden for both the individual and the society. The treatment of foot ulcers and its complications is resource intensive, long term and the most common reason for diabetes-related hospital admission (Gordois et al., 2003). Approximately 15% of people with diabetes develop at least one foot ulcer during their lifetime and up to 85% of lower limb amputations are preceded by foot ulcers (Gordois et al., 2003; Boulton, 2004). To understand the mechanisms contributing to ulceration of the diabetic foot is therefore of considerable interest. Increased pressures under the foot when walking have been shown to be significantly associated to the incidence of plantar ulcer formation in patients with diabetes (Frykberg et al., 1998; Stess et al., 1997; Veves et al., 1992). It * Corresponding author. E-mail address: [email protected] (A. Höhne). 0268-0033/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.clinbiomech.2009.01.001
has been well documented that plantar pressures in diabetic patients are higher than those in healthy subjects (Boulton et al., 1983; Luger et al., 2001). Boulton et al. (1983) reported increased plantar pressures in 17% of patients with diabetes and in 51% of those with diabetes and peripheral neuropathy. Several factors have been identified as possibly being responsible for this increase. These include peripheral motor and sensory neuropathy (Caselli et al., 2002; Frykberg et al., 1998), limited joint mobility, foot deformity (Bus et al., 2005; Mueller et al., 2003; Rao et al., 2007; Robertson et al., 2002) and changes in structure and thickness of the plantar soft tissues (Abouaesha et al., 2001). To which extent the different proposed mechanisms contribute to the increase in plantar pressure in diabetes still remains unknown. Previous studies suggested that the heightening of plantar pressures significantly increases with concomitant occurrence of peripheral neuropathy and with the severity of its symptoms (Caselli et al., 2002; Frykberg et al., 1998; Pham et al., 2000). Parameters of peripheral sensory neuropathy were shown to be highly predictive of increased plantar pressure and increased risk of foot ulceration.
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Vibration perception of the foot and the inability to sense a 5.07 Semmes–Weinstein Monofilament (10 g) are the most sensitive tests in clinical assessments besides the neuropathy disability score (Frykberg et al., 1998; Pham et al., 2000). One consequence of peripheral sensory neuropathy is insensitive skin, which impairs the sensory feedback of plantar pressure and pain. Plantar cutaneous afferents have been demonstrated to play an important role during human balance control (Meyer et al., 2004a,b; Perry et al., 2000). Location specific information of the foot sole is spatially coded to the central nervous system and contributes to postural responses (Kavounoudias et al., 1998). Reduced plantar cutaneous sensation could thus be considered as a relevant factor for alterations in plantar pressures whilst walking. The influence of insensitive skin on altered plantar pressures in the diabetic neuropathic foot is not understood in detail. The multifactorial character of the diabetic disease, as well as the affection of all components of the peripheral nervous system (sensory, motor and autonomic) in diabetic peripheral neuropathy, make it difficult to ascribe changes in plantar pressures to any single factor. A valuable approach for determining the contribution of plantar sensory feedback to the sensorimotor control processes maintaining posture and gait is to experimentally change plantar sensitivity in healthy subjects. Several studies tried to reduce plantar cutaneous sensation by using ischemic, hypothermic or ankle anaesthesia methods (Do et al., 1990; Nurse and Nigg, 2001; Perry et al., 2000; Thoumie and Do, 1996). But, these methods largely fail to isolate plantar cutaneous sensation from the other foot and ankle somatosensory systems and motor functions. Plantar pressure distribution during walking was investigated before and after foot sole cooling procedures in homogenous groups of young healthy subjects by using pressure platforms (Eils et al., 2002; Taylor et al., 2004) and pressure insoles (Nurse and Nigg, 2001). Ice immersion induced an obvious altered roll-over strategy of the foot as seen in a more cautious, rigid walking pattern (Eils et al., 2002; Taylor et al., 2004). Therefore it was almost obvious that the observed changes in plantar pressure and force variables (Eils et al., 2002; Nurse and Nigg, 2001; Taylor et al., 2004) should appear. Moreover, the results are to some extent contradictory, in particular for the peak plantar pressures. Exemplarily, increased peak plantar pressures at the forefoot region were reported by Nurse and Nigg (2001) and Taylor et al. (2004), whereas Eils et al. (2002) found solely decreased peak plantar pressures after ice immersion. An important drawback of hypothermic protocols is that cooling procedures do not exclusively influence plantar cutaneous receptors and therefore an affection of intrinsic foot muscles and joint receptors can not be excluded. In addition, the time window for testing the foot sole cooling intervention is limited to only one or two steps due to a quick warm-up process, as reported by Eils et al. (Eils et al., 2002; Taylor et al., 2004). The influence of insensitive skin due to peripheral sensory neuropathy on changes in plantar pressures is not well understood. Moreover, the mechanisms relating reduced plantar cutaneous feedback to changes in plantar pressure distribution and force variables during walking remain unclear. In consequence, the purpose of this study was to identify possible causal dependences between reduced plantar cutaneous sensation and plantar pressure distribution during gait. A specifically designed anaesthesia procedure targeting solely the end-organs of the plantar cutaneous mechanoreceptors was used. This way foot and ankle proprioception as well as intrinsic foot muscles were left unaffected (Meyer et al., 2004a, b). In contrast to previous hypothermic protocols, the effects were analysed after a longer period of experimentally reduced sensation. It was expected: that (a) a selective reduction of plantar cutaneous sensation would cause significant changes in plantar pressure and force variables during walking and that (b) alterations in plantar
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pressures similar to those seen in diabetic peripheral neuropathy would be observed. 2. Methods 2.1. Subjects Ten healthy subjects, six males and four females, (mean age 23.6, standard deviation: SD 1.9 yr; mean height 178.4, SD 8.9 cm; mean mass: 76.3, SD 12.0 kg) volunteered for the study. The study was approved by the intern ethical committee of the German Sport University Cologne. All subjects were informed in detail about the nature of the study and gave their written informed consent prior to participation. Each of the subjects underwent a physical examination and filled out a clinical routine-questionnaire to exclude any neurological disorders or musculoskeletal diseases, which could influence the experimental outcome, as well as possible allergic reactions against the anaesthetic solution. 2.2. Experimental protocol Baseline values (pre condition) for the sensory perception threshold (SPT) of the plantar foot and for the dynamic pressure distribution while walking were taken prior to the sensory intervention. Subsequently, the subjects underwent the anaesthesia procedure. The SPT of the plantar foot was evaluated again to quantify the immediate effect of the anaesthesia on plantar sensitivity (post condition 1). During the next 40–60 min the subjects performed a gait perturbation protocol (22 trials) along a walkway with unexpected changes in surface stiffness which is not discussed in the present paper. This protocol provided walking experience, allowing the subjects to get familiar to the sensory changes. Afterwards, dynamic pressure distribution while walking with reduced plantar sensitivity was measured (post condition). At the end of the experiment, the SPT of the plantar foot was quantified again, to assess the effect of the sensory intervention (post condition 2). 2.3. Sensory perception threshold evaluation The SPT of the plantar foot was determined by two validated tests for clinical assessment of peripheral sensory neuropathy: pressure touch and vibration perception (Caselli et al., 2002; Frykberg et al., 1998; Pham et al., 2000). Three plantar test regions at the right foot – centre of the second and third metatarsal head representing the forefoot, centre of the lateral midfoot and the centre of heel were choosen and tested in random order to assess the effect of the sensory intervention on plantar sensitivity. These test regions were marked to ensure that pre- and post-sensitivity tests were carried out on the same plantar regions. The SPT of pressure touch was quantified with a set of 20 Semmes–Weinstein monofilaments (SWMF) (North Coast Medical, Inc., Morgan Hill, USA). The calibrated filaments vary in diameter in correlation with a known bending force (filament size = log10 of [10 force in milligrams]). To determine the sensory threshold level of the tested region we used the 4, 2, 1 stepping algorithm (Dyck et al., 1993) and a forced-choice method (Chong and Cros, 2004). The test started at an intermediate level, filament 4.31 (pre condition) and filament 5.07 (post condition 1, 2). The subjects laid supine with eyes closed in a quiet room, then the filaments were applied perpendicularly to the skin surface at the test regions and pushed until bending. Depending on the subject’s answer, the stimulus was increased or decreased in four filament steps until a turnaround point was reached. Then the test was carried out in 2 filament steps and 1 filament steps, respectively, until three consecutive failures
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were observed. The lightest filament leading to a response, was determined to be the sensory threshold level for the tested region. To improve the accuracy of the test, five null-stimuli were applied randomly at the test algorithm. Sensory loss is clinically detected by the inability to sense filament 5.07 (115 mN) at two of three sites on plantar surface (Frykberg et al., 1998; Holewski et al., 1988). About 70% of the cutaneous mechanoreceptors at the human foot sole are the rapidly adapting FAI (Meissner corpuscles) and FAII (Pacinian corpuscles) receptors (Kennedy and Inglis, 2002). FAI receptors mainly mediate low frequencies and FAII receptors solely transmit high frequencies (Kekoni et al., 1989). Therefore, to quantify the effect of the sensory intervention on the different mechanoreceptor’s modalities, the vibration perception was evaluated using both frequency spectrums (25 Hz/200 Hz). A custom modified HVLab Tactile Vibrometer was used (Institute of Sound and Vibration Research, University Southampton, UK). The Vibrometer unit housed an electrodynamic vibrator, which was mounted on a counterbalance, so as to provide a constant upward contact force (1 N) between the application probe and the skin surface. An accelerometer was mounted on the vibrator, with the application probe connected to its upper surface. The subjects sat comfortably in a chair with an adjustable support for the right lower leg, allowing a horizontal positioning of the right foot sole. Then the application probe (perspex probe, 5 mm diameter) was placed without any surrounding contact, perpendicularly to the plantar test region with a skin indentation contact force of 1 N (±0.1 N). The subjects wore ear muffs to shield any environment or equipment noise. Test frequencies and plantar test regions were chosen in random order. The sinusoidal vibration stimulus was applied using the Békésy method of increasing and decreasing rates based on a standardised test protocol (ISO, 2001). The subject had to press a response button as long as the vibration sensation could be perceived. The amplitude of the vibration increased until the subject pressed the response button (appearance threshold). Then the amplitude decreased until the button was released (disappearance threshold). This procedure was repeated several times in order to determine the threshold level, i.e. the mean value of the mean appearance and mean disappearance thresholds at a minimum of 6 reversals. The displacement was calculated from the acceleration wave by
X¼
middle of a 10 m walkway. The pressure platform contains four calibrated capacitive sensors per cm2 with a total sensing area of 475 320 mm. Data were collected at 100 Hz sampling frequency. All subjects performed five barefoot gait trials at an individually chosen velocity at each condition. The third-step method was used, meaning that the third-step after gait initiation was hitting the platform. Using this method, five trials have shown to provide reproducible values (Bus and De Lange, 2005). Subjects performed up to four test trials to familiarize themselves with the protocol and to determine their starting position. Then, five consecutive
A ð2pf Þ2
where X is the displacement, A is the acceleration and f is the vibration frequency (Griffin, 1990). The room and plantar foot skin temperatures were controlled to exclude an affection of the SPT by changes in temperature (Laser temperature measurement device, Testo 825-T4, Testo AG, Lenzkirch, Gemany). 2.4. Dynamic pressure distribution measurement Dynamic pressure distribution was measured by an EMED-X platform (novel GmbH, Munich, Germany) mounted flush in the
Fig. 1. Mask defining the ten plantar foot regions for analysis of plantar pressure and force variables. MHE – medial heel, LHE – lateral heel, MMF – medial midfoot, LMF – lateral midfoot, MT1 – first metatarsal region, MT2 – second metatarsal region, MT 345 – metatarsal region 3, 4, 5, HAL – hallux, 2TO – second toe, 345TO – toes 3, 4, 5.
Fig. 2. Mean values and standard error of mean of the sensory perception threshold (SPT) at the plantar foot regions for pressure touch (A) and vibration (25/200 Hz) (B) before anaesthesia (pre), after anaesthesia (post 1) and after finishing the pressure distribution measurement (post 2). Statistically significant differences (P < 0.05) between: * pre and post 1, pre and post 2, à post 1 and post 2.
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A. Höhne et al. / Clinical Biomechanics 24 (2009) 308–313 Table 1 Mean values and standard deviations for contact time (% roll-over process), peak pressure (kPa) and pressure–time integral (kPas). Foot region
Contact time (% ROP) Pre
Medial heel Lateral heel Medial midfoot Lateral midfoot Metatarsal 1 Metatarsal 2 Metatarsal 3, 4, 5 Hallux Second toe Toes 3, 4, 5
49.9 49.4 30.0 58.2 77.3 81.5 83.4 65.7 54.8 63.9
Peak pressure (kPa) Post
(5.3) (5.1) (12.1) (4.5) (3.9) (2.4) (2.8) (12.9) (6.6) (8.2)
48.2 47.8 33.3 58.2 78.2 81.5 83.6 69.1 54.9 65.1
Pre (4.4) (4.2) (8.6) (6.2) (3.5) (2.8) (2.6) (9.7) (5.3) (13.7)
548.0 528.7 84.9 136.8 354.1 563.9 516.2 435.4 285.7 194.8
Pressure–time integral (kPas) Post
(126.1) (130.3) (42.3) (26.3) (135.0) (228.4) (228.0) (120.5) (86.1) (62.9)
505.0 476.1 92.2 138.2 324.1 557.5 555.2 421.6 210.0 159.0
Pre (138.5) (103.8) (32.1) (25.5) (76.7) (204.5) (284.0) (160.2) (83.2) (67.8)
Post
95.3 89.6 13.5 34.4 90.5 143.8 146.2 99.5 55.7 42.2
(26.0) (23.1) (7.9) (9.3) (20.1) (45.8) (57.0) (36.1) (21.6) (14.6)
89.1 83.0 14.6 34.1 87.5 141.1 152.5 96.9 40.5 36.3
(27.9) (21.4) (5.7) (8.5) (20.3) (47.7) (70.9) (43.1) (17.4) (18.2)
Statistically significant differences (P < 0.05) before (pre) and after (post) the sensory intervention.
trials were measured. Contact time, peak pressure, pressure–time integral, maximum force and force–time integral for the entire foot and ten plantar regions were calculated and analysed. The ten plantar foot regions were defined according to Cavanagh and Ulbrecht (1992) in medial heel, lateral heel, medial midfoot, lateral midfoot, metatarsal region 1, metatarsal region 2, metatarsal region 3/4/5, hallux, second toe and toe 3/4/5 (Fig. 1). The data were calculated for each trial and then averaged for each subject and condition (novel scientific software, novel GmbH, Munich, Germany). 2.5. Sensory intervention Sensation from the weight-bearing surface of both foot soles was locally reduced through multiple intradermal injections of an anaesthetic solution using a modified procedure from Meyer et al. (2004a). The anaesthetic solution (2% lidocaine HCl, 1:8 sodium bicarbonate, 1:200,000 epinephrine, 12 U/mg hyaluronidase) was intradermally applied by an anaesthesiologist using 30-gauge needles. Effective anaesthesia results were achieved by eight to twelve 0.8 ml injections for each foot. This method targets the end-organs of the cutaneous mechanoreceptors leaving joint and muscle afferents unaffected. No changes in elastic skin compliance and no affection of the proprioception of the foot were reported (Meyer et al., 2004a,b). Sensation at the skin of the forefoot, the lateral foot and heel, i.e. the weight-bearing surface with exception of the toes, was locally reduced. The toes remained untreated as the use of epinephrine in the digits is precluded. The whole procedure took about 1 h for both feet and was well tolerated by all subjects. 2.6. Statistical analysis For statistical analysis, a one-way ANOVA for repeated measurements was performed for the sensitivity tests (pre condition, post condition 1 and 2). A paired t-test for dependent samples was used to determine possible differences in the dynamic pressure distribution variables (pre and post condition). The statistical level of significance was set at P < 0.05 for all analyses, which were conducted using SPSS (Version 14.0, SPSS Inc., Chicago, Illinois, USA). 3. Results 3.1. Plantar cutaneous sensation Plantar cutaneous sensation was significantly reduced compared to the baseline values (pre condition) during the entire experimental period (post condition 1, 2) (Fig. 2). The SPT for pressure touch was significantly increased reaching the criteria values
of peripheral sensory neuropathy (filament 5.07) at all plantar test regions (Fig. 2A). Immediately after the anaesthesia (post condition 1), the filament size was increased at the forefoot from mean (SD) 4.01 (0.5) to 6.1 (0.6), P < 0.000; at the lateral foot from 3.73 (0.5) to 5.7 (0.8), P < 0.000 and at the heel from 4.21 (0.3) to 6.1 (0.7), P < 0.000. At post condition 2 (after finishing the pressure distribution measurement), the SPT for pressure touch was still significantly higher than the pre condition at all plantar test regions: forefoot mean (SD) 5.77 (0.8), P < 0.000; lateral foot 5.79 (0.8), P < 0.000 and heel 5.04 (0.9), P < 0.003. Similarly, the SPT for low (25 Hz) and high (200 Hz) frequency vibration was significantly increased at the plantar test regions (Fig. 2B). The results are presented for nine out of ten subjects, because one subject was not able to perceive the vibration stimulus after anaesthesia. The SPT at both 25 Hz and 200 Hz was increased by about 100% at the forefoot (P < 0.001), at lateral foot (P < 0.001) and at heel (P < 0.005) at both post sensory intervention conditions (post condition 1, 2), as compared to the baseline values (pre condition). Some previous studies evaluated the SPT for vibration at the plantar foot using different test protocols (Kekoni et al., 1989; Nurse and Nigg, 2001; Wells et al., 2003). Differences in the stimulus application, such as presence or absence of surround contact, diameter of the application probe, skin contact force or skin indentation, all may influence the results (Chong and Cros, 2004). Taking these methodological difficulties into account, our results for the SPT for vibration (25 Hz/200 Hz) at pre condition were within similar ranges as those of these previous studies. Likewise, the SPT for pressure touch at pre condition were in agreement with the results of studies in young healthy subjects (Eils et al., 2002; Nurse and Nigg, 2001; Taylor et al., 2004). Maximal pre-post differences in skin and room temperature were below 3 degrees. These differences were considerably lower Table 2 Mean values and standard deviations for maximum force (N) and force–time integral (relative values of total foot in %). Foot region
Maximum force (N) Pre
Medial heel Lateral heel Medial midfoot Lateral midfoot Metatarsal 1 Metatarsal 2 Metatarsal 3, 4, 5 Hallux Second toe Toes 3, 4, 5
376.5 317.5 9.8 142.1 187.4 238.5 335.6 191.9 45.5 49.9
Force–time integral (%)
Post (87.6) (61.7) (6.7) (42.9) (49.9) (60.3) (98.9) (63.0) (20.1) (20.8)
363.4 310.5 10.9 147.3 187.0 229.0 330.4 173.8 35.2 43.5
Pre (72.3) (56.9) (7.9) (41.9) (37.9) (51.0) (103.1) (64.1) (23.3) (27.8)
15.3 12.8 0.3 6.9 11.5 15.7 24.7 8.7 1.9 2.2
Post (1.6) (1.0) (0.3) (1.9) (2.7) (2.4) (3.3) (3.1) (0.9) (1.2)
14.8 12.8 0.4 7.3 12.2 15.9 24.9 8.4 1.4 2.0
(2.2) (0.8) (0.3) (1.8) (3.0) (2.5) (4.3) (2.8) (0.9) (1.5)
Statistically significant differences (P < 0.05) before (pre) and after (post) the sensory intervention.
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Table 3 Mean values and standard deviations for entire foot before (pre) and after (post) the sensory intervention. Parameter
Condition Pre
Contact time (ms) Peak pressure (kPa) Pressure–time integral (kPas) Maximum force (N) Force–time integral (Ns)
665.2 702.9 253.4 997.5 443.1
Post (44.0) (191.5) (58.7) (191.8) (85.3)
653.4 710.3 255.0 974.9 424.6
(50.3) (223.9) (75.7) (172.0) (81.7)
than those which could potentially influence the evaluation of the SPT during the measurements (ISO, 2001). 3.2. Plantar pressure distribution Data analysis was conducted for ten plantar regions (Table 1 and 2) and for the entire foot (Table 3) for contact time, peak pressure, pressure–time integral, maximum force and force–time integral. All analysed plantar pressure and force variables as well as contact times for the different regions and the entire foot were not significantly changed after the sensory intervention with exception of second toe. In this region, plantar pressure and force variables were reduced (P < 0.05) (Table 1 and 2). No increase in plantar pressures or forces was observed at any of the ten plantar foot regions or the entire foot after the sensory intervention. 4. Discussion The purpose of this study was to identify possible causal dependences between reduced plantar cutaneous sensation and plantar pressure distribution in gait. Furthermore, it was investigated whether changes occurring in plantar pressure distribution after reduced plantar cutaneous sensation resemble those seen in the diabetic neuropathic foot. The applied sensory intervention led to a significant reduction in plantar cutaneous feedback during the entire experimental period at all plantar test regions (forefoot, lateral foot and heel). The SPT for vibration (25/200 Hz) was significantly increased indicating a reduction in sensitivity of the FAI and FAII mechanoreceptors in the foot sole. Similarly, the SPT for pressure touch was clearly above the sensory threshold level of filament 5.07 (SWMF) for clinical detection of peripheral sensory neuropathy (Holewski et al., 1988; Pham et al., 2000). The anaesthesia method targeted solely the plantar cutaneous mechanoreceptor end-organs while leaving foot and ankle proprioception and intrinsic foot muscles unaffected as previously shown by Meyer et al. (2004a,b). Plantar pressures were recorded 48 min (SD 10 min) after anaesthesia and allowed therefore to observe the effects on plantar pressure distribution during walking after a longer period of reduced sensation and having had anaesthetised walking experience. The analysed variables – peak pressure, pressure–time integral, maximum force, force– time integral and contact time – did not change neither for the different foot regions nor for the entire foot. The results of our study suggest that targeted reduced plantar cutaneous sensation in healthy subjects does not cause significant changes in plantar pressure distribution whilst walking. Some methodological limitations of the study have to be acknowledged. Ethical considerations due to the invasive nature of the anaesthesia procedure restricted the sample size (n = 10). The reduction in statistical sensitivity due to small sample size was partially compensated by studying a homogeneous sample. Statistical sensitivity to detect significantly differences in plantar pressure and force variables could be therefore limited. In addition,
it has also to be considered that short time sensory loss of plantar cutaneous feedback differs from long-standing peripheral sensory neuropathy in patients with diabetes where long time strategies could be developed. However, as previously mentioned, most of the affected patients with diabetes develop a combination of risk factors (Abouaesha et al., 2001; Mueller et al., 2003; Rao et al., 2007; Robertson et al., 2002), which make it almost impossible to study isolated causal relations in this population. In particular the simultaneous affection of the sensory, motor and autonomic components of the peripheral nervous system (Frykberg et al., 1998; Greenman et al., 2005; Pham et al., 2000), restricts the possibility to address changes in plantar pressures to a single factor. Hence experimental interventions in healthy subjects are a valuable approach to provide usefully insights into the role of peripheral sensory neuropathy on altered plantar pressures in patients with diabetes. It is well established that plantar pressure variables as peak pressure and pressure loading over time (pressure–time integral) are increased in these patients (Boulton et al., 1983; Luger et al., 2001; Stess et al., 1997). Especially the metatarsal region is affected by an elevated ulceration risk due to increased plantar pressures (Stess et al., 1997; Veves et al., 1992). The increase of the different plantar pressure distribution variables and the risk for plantar ulceration were found to be highly correlated with concomitant occurrence and severity of peripheral neuropathy (Caselli et al., 2002; Frykberg et al., 1998; Pham et al., 2000). A more recent study using magnetic resonance imaging suggested that intrinsic foot muscle atrophy due to motor neuropathy is evident already before sensory neuropathy is detected by clinical screening techniques (Greenman et al., 2005). A possible explanation for changes in plantar pressures could be intrinsic foot muscle atrophy and the related decrease of force capacities. The consequences of intrinsic foot muscle atrophy, such as imbalances between flexor and extensor muscles resulting in toe deformity (clawing, hammer toes), as well as prominent metatarsal heads, limited joint mobility and decreased thickness of plantar soft tissue (muscle tissue), have been considered as factors contributing to an in increase in plantar pressures and ulceration risk primarily at the metatarsal region (Bus et al., 2005; Frykberg et al., 1998; Mueller et al., 2003; Robertson et al., 2002). The results of our study do not confirm the findings of hypothermic studies using cooling procedures to reduce plantar cutaneous feedback in young healthy subjects. Plantar pressure distribution while walking was investigated in ten subjects (mean age: 26.1, SD 4.1 yr) by using pressure insoles (Nurse and Nigg, 2001), in a group of 15 subjects (25.7, SD 4.1 yr) by using a pressure platform (Taylor et al., 2004) and in a group of 40 subjects (25.3, SD 3.3 yr) by using a pressure platform as well (Eils et al., 2002). Foot sole cooling led to significant changes in plantar pressure and force variables while walking (Eils et al., 2002; Nurse and Nigg, 2001; Taylor et al., 2004). Two studies observed a visibly altered, more rigid and cautious roll-over pattern of the foot after ice immersion (Eils et al., 2002; Taylor et al., 2004). Higher loads after ice immersion were reported for the forefoot and lateral midfoot. These resulted into an increase of peak pressure, pressure–time integral (Nurse and Nigg, 2001; Taylor et al., 2004), maximum force (Taylor et al., 2004), force–time integral (Eils et al., 2002; Nurse and Nigg, 2001; Taylor et al., 2004) and longer contact times (Eils et al., 2002; Taylor et al., 2004). Decreased pressure and force values were reported for the toe and heel regions (Eils et al., 2002; Nurse and Nigg, 2001; Taylor et al., 2004). One study also described a considerable reduction in walking speed after ice immersion (Taylor et al., 2004). Taking our results into account, it might be concluded that the former observed changes in plantar pressure distribution after foot sole cooling were more likely caused by an altered rollover strategy of the foot and an affection of intrinsic foot muscles and joint receptors than by plantar cutaneous sensation. The more
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rigid walking style might be a sign for an affection of joint mobility at the forefoot region. Decreased force capacities and limited joint mobility were recognized to be related to an increase in plantar pressures at the forefoot region (Rao et al., 2007; Robertson et al., 2002). The targeted reduction of plantar cutaneous sensation by locally applying intradermal anaesthesia did not change plantar pressure and force variables or contact times in a comparable group of healthy subjects. The differing results can be explained by the different methodologies. The main finding of the present study is that targeted reduced plantar cutaneous sensation in healthy subjects does not affect plantar pressure distribution while walking. Alterations of plantar pressures while walking similar to those in diabetic peripheral neuropathy could not be observed. 5. Conclusions This study demonstrated that experimentally reduced plantar cutaneous sensation without any affection of foot and ankle proprioception and intrinsic foot muscles causes no changes in plantar pressure distribution while walking. Our findings suggest that in the diabetic neuropathic foot, insensitive plantar skin due to peripheral sensory neuropathy may be not a decisive factor for alterations in plantar pressures. These results help underpinning the importance of concomitant affection of different systems secondary to diabetic peripheral neuropathy with regard to increased plantar pressures in diabetic patients. Acknowledgment We would like to thank Dr. Gaspar Morey Klapsing for his contribution to improving the manuscript. References Abouaesha, F., Van Schie, C.H., Griffths, G.D., Young, R.J., Boulton, A.J., 2001. Plantar tissue thickness is related to peak plantar pressure in the high-risk diabetic foot. Diabetes Care 24, 1270–1274. Boulton, A.J., 2004. The diabetic foot: from art to science. The 18th Camillo Golgi lecture. Diabetologia 47, 1343–1353. Boulton, A.J., Hardisty, C.A., Betts, R.P., Franks, C.I., Worth, R.C., Ward, J.D., Duckworth, T., 1983. Dynamic foot pressure and other studies as diagnostic and management aids in diabetic neuropathy. Diabetes Care 6, 26–33. Bus, S.A., De Lange, A., 2005. A comparison of the 1-step, 2-step, and 3-step protocols for obtaining barefoot plantar pressure data in the diabetic neuropathic foot. Clin. Biomech. 20, 892–899. Bus, S.A., Maas, M., De Lange, A., Michels, R.P., Levi, M., 2005. Elevated plantar pressures in neuropathic diabetic patients with claw/hammer toe deformity. J. Biomech. 38, 1918–1925. Caselli, A., Pham, H., Giurini, J.M., Armstrong, D.G., Veves, A., 2002. The forefoot-torearfoot plantar pressure ratio is increased in severe diabetic neuropathy and can predict foot ulceration. Diabetes Care 25, 1066–1071. Cavanagh, P.R., Ulbrecht, J.S., 1992. Clinical plantar pressure measurement in diabetes: rationale and methodology. Foot 4, 123–135. Chong, P.S., Cros, D.P., 2004. Technology literature review: quantitative sensory testing. Muscle Nerve 29, 734–747. Do, M.C., Bussel, B., Breniere, Y., 1990. Influence of plantar cutaneous afferents on early compensatory reactions to forward fall. Exp. Brain. Res. 79, 319–324.
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