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Can we predict outcome of surgical reconstruction of Charcot neuroarthropathy by dynamic plantar pressure assessment?—A proof of concept study
Gait & Posture 31 (2010) 87–92
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Gait & Posture journal homepage: www.elsevier.com/locate/gaitpost
Can we predict outcome of surgical reconstruction of Charcot neuroarthropathy by dynamic plantar pressure assessment?—A proof of concept study Bijan Najafi a,*, Ryan T. Crews a, David G. Armstrong b, Lee C. Rogers c, Kamiar Aminian d, James Wrobel a a
Scholl’s Center for Lower Extremity Ambulatory Research (CLEAR), Rosalind Franklin University of Medicine and Science, North Chicago, IL, USA Southern Arizona Limb Salvage Alliance (SALSA), Department of Surgery, University of Arizona, Tucson, AZ, USA c Amputation Prevention Center at Valley Presbyterian Hospital, Los Angeles, CA, USA d Ecole Polytechnique Federale de Lausanne, Laboratory of Movement Analysis & Measurement, Lausanne, Switzerland b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 3 December 2008 Received in revised form 8 September 2009 Accepted 12 September 2009
The joint deformity that arises as a result of Charcot neuroarthropathy, leads to gait modification. Ulceration risk associated with the deformity is generally assessed by measuring plantar pressure magnitude (PPM). However, as PPM is partially dependent on gait speed and treatment interventions may impact speed, the use of PPM to validate treatment is not ideal. This study suggests a novel assessment protocol, which is speed independent and can objectively (1) characterize abnormality in dynamic plantar loading in patients with foot Charcot neuroarthropathy and (2) screen improvement in dynamic plantar loading after foot reconstruction surgery. To examine whether the plantar pressure distribution (PPD) measured using EMED platform, was normal, a customized normal distribution curve was created for each trial. Then the original PPD was fitted to the customized normal distribution curve. This technique yields a regression factor (RF), which represents the similarity of the actual pressure distribution with a normal distribution. RF values may range from negative 1 to positive 1 and as the value increases positively so does the similarity between the actual and normalized pressure distributions. We tested this novel score on the plantar pressure pattern of healthy subjects (N = 15), Charcot patients pre-operation (N = 4) and a Charcot patient post-foot reconstruction (N = 1). In healthy subjects, the RF was 0.46 0.1. When subjects increased their gait speed by 29%, PPM was increased by 8% (p < 10 5), while RF was not changed (p = 0.55), suggesting that RF value is independent of gait speed. In preoperative Charcot patients, the RF < 0, however, RF increased post-surgery (RF = 0.42), indicating a transition to normal plantar distribution after Charcot reconstruction. ß 2009 Elsevier B.V. All rights reserved.
Keywords: Charcot neuroarthropathy Diabetes Diabetic foot Outcome assessment (health care) Foot Gait Kinetics Arthropathy Neurogenic Pedography Plantar pressure Joint deformity Foot reconstruction Foot joint deformity Podiatric
1. Introduction Charcot neuroarthropathy (CN) or Charcot foot is a devastating condition occurring most commonly in those with diabetes complicated by peripheral neuropathy and frequently leads to limb loss [1,2]. The pathogenesis is not well understood, but it is generally agreed trauma (micro-repetitive or single-instance macrotrauma) in the presence of neuropathy is required to spark this syndrome [3]. Trauma precipitates an inflammatory cascade and vasodilation [4]. The vasodilation may ‘‘wash out’’ minerals
* Corresponding author at: Human Performance Lab., Shcoll’s Center for Lower Extremity Ambulatory Research (CLEAR), The Dr. William M. Scholl College of Podiatric Medicine, Rosalind Franklin University of Medicine & Science, 3333 Green Bay Road, North Chicago, IL 60064-3037, USA. Tel.: +1 847 578 8456; fax: +1 847 775 6570. E-mail address: bijan.najafi@rosalindfranklin.edu (B. Najafi). URL: http://www.CLEAR-Scholl.org 0966-6362/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.gaitpost.2009.09.003
from the bone reducing density and thereby making one more susceptible to fractures. This, coupled with glycosylation of periarticular tissue, particularly the Achilles tendon, may make the person with Charcot arthropathy of the foot prone to its characteristically impressive fracture-dislocations. Treatment of CN depends on the stage during which it is diagnosed [5]. Early diagnosis is challenging, but allows the opportunity to intervene and prevent development or worsening of such deformities. Distribution and magnitudes of plantar pressure during gait can provide insight into functional manifestations of foot and ankle disorders and may be used for early diagnosis of abnormal foot biomechanics due to CN. Additionally, these dynamic measurements often serve as objective measures for outcomes evaluation following foot surgery and can be used to track disease progression [6–10]. However, plantar pressure magnitude (PPM) alone may be inappropriate when studying the effects of foot surgery. Following corrective foot surgery, patients will many times increase their gait speed as a result of
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greater confidence and stability, and a more efficient gait pattern. Although this increase may be practically advantageous, it may also increase PPM, historically viewed as a negative outcome. For a fair evaluation of the success of surgery, a novel and speed independent variable is required that reflects improved foot biomechanics post-surgery. The objective of this investigation is to develop a novel assessment protocol which is speed independent and by which plantar pressure modification during gait could be objectively characterized. From a clinical standpoint, the purpose of this manuscript was to be a proof of concept trial for validating this novel assessment protocol to (1) screen abnormal plantar loading due to CN and (2) evaluate the success of foot reconstruction surgery to improve functional gait as well as dynamic plantar loading. To our best knowledge, this is the first study that has thoroughly and objectively addressed the impact of Charcot reconstruction upon gait.
case. All histograms were estimated using a 30-bins scheme (selected arbitrarily). Then, the original plantar pressure distribution was fitted to the customized normal distribution curve using a multiple linear regression approach. This technique yields a regression factor (RF), which represents the similarity of the actual pressure distribution with the normalized distribution. RF values may range from negative 1 to positive 1 and as the value increases positively so does the similarity between the actual and normalized pressure distributions. This process yields a simple value to represent an abnormality in dynamic plantar loading due to foot CN (see Fig. 1F). 2.3. First study: is the RF score, speed independent? To examine whether the RF score is speed independent, pressure profiles were measured for 15 healthy subjects walking at multiple speeds. 2.3.1. Subjects recruitment 15 healthy subjects (6 female, 9 male) were recruited with an average age 24.2 1.78 years, average height 173.77 14.02 cm, and average body mass 76.44 17.5 kg. The study received ethical approval in accordance with the local institutional review board. All subjects provided informed consent prior to the start of testing.
2. Methods 2.1. General hypothesis Our efforts to develop a reliable outcome measure for objectively assessing plantar loading post-reconstruction relied on two hypotheses: (1) the statistical distribution of plantar pressure during stance is independent of gait speed; and (2) any biomechanical change (or joint deformity) will affect the pattern of plantar pressure profile during gait. 2.2. Approach description Fig. 1A illustrates the temporal pattern of plantar pressure magnitude (PPM) during stance phase for three cases: a typical healthy subject, a CN patient preoperation and post-operation. The stance duration is visibly different for each pattern. This consequently may alter the temporal profile of the pressure pattern, further complicating healthy and pre/post-surgical comparisons. To overcome this shortcoming, a time-scale normalization scheme was used to moderate the effect of gait speed across different steps’ pressure profiles. For this purpose, we implemented a classical linear interpolation/decimation scheme to standardize stance duration for each step trial (see Fig. 1B). After normalizing the time-scale, we estimated the statistical distribution of the total-foot peak plantar pressure profile (see Fig. 1C). Examining the distribution pattern, we noticed that in healthy cases as well as the post-operative case, the distribution was similar to a normal– Gaussian-distribution (see Fig. 1D and E), while in pre-operative cases the distribution shape was far from a normal shape (see Fig. 1C). To attribute a numeric value to this abnormality pattern, a customized normal distribution curve was created for each trial utilizing the mean, standard deviation, and maximum probability values for the trial. These variables enable simulation of a normal distribution, which can represent the plantar distribution pattern in each
2.3.2. Measurement protocol Subjects walked – barefoot – at least 10 m at three different speeds: slow (very leisurely walk), habitual (preferred), and fast (as fast as they could safely walk). At least one practice trial occurred before each test, and each test was repeated twice. The two trials’ average was considered for the final analysis. The primary objective of these tests was to explore the relationship between gait speed and plantar pressure distribution. To control spatio-temporal parameters of gait, angular rate sensors (gyroscopes) and a Physilog1 ambulatory datalogger (Physilog1, BioAGM, CH) system were used. Elastic bands attached gyroscopes (Analog device, Inc., Norwood, Massachusetts) to each shank and each thigh. Each sensor measured the angular velocity of the segment around the medio-lateral axis (flexion–extension). Signals were digitized (16 bit) at a sampling rate of 200 Hz and stored for off-line processing on a SD memory card (512 Mb). The method for calculating the spatio-temporal parameters of gait is described in detail elsewhere [11–14]. Plantar pressure data was obtained by an Emed-X1 (Novel-Germany) platform. Subjects were allotted practice trials in order to successfully hit the platform on the 6th step during the varied gait speeds aforementioned. Floor markers were implemented in order to ensure proper gait repetition. To estimate the gait speed at the time of stepping on platform, an observer noted the number of steps taken by the subject from gait initiation until stepping on the platform. Then the gait speed corresponding to that step was estimated using Physilog data. The measured speed was compared to the average gait speed (excluding first two and last two steps) to ensure the subject did not slowdown before touching the platform. Plantar foot contact area and the vertical ground reaction force were collected at 400 Hz. To assess the plantar pressure profile, we calculated the peak pressure magnitude as a function of time using Novel1 multimasking software (version 14.3.8e).
Fig. 1. (A) Plantar pressure profile for a typical healthy subject and a typical CN patient pre- and post-operation. The duration of stance is different between three patterns, suggesting that gait speed is different between them. (B) A time-scale normalization scheme was used to moderate the effect of gait speed. The plantar pressure distribution profile in (C) Charcot case pre-operation, (D) post-operation, and (E) healthy subject. (F) RF estimated for patients pre-op (red color), post-op (blue color), and healthy (green color) subject. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of the article.)
B. Najafi et al. / Gait & Posture 31 (2010) 87–92 2.4. Second study: can the RF score screen abnormal plantar loading due to CN and its improvement post-foot reconstruction? To examine whether the RF value can be used to screen the abnormal plantar loading, we measured the plantar pressure loading during gait in four patients (men, age: 54 4 years old; body mass: 97.6 13.5 kg; height: 178.3 2.9 cm) with diabetes and Charcot foot deformities. At each visit the patients completed three barefoot walking trials with the Emed-X platform. Patients initiated gait approximately 1.5 m prior to the platform and upon stepping on the platform continued walking straight ahead approximately 2 m. The subjects were instructed to walk at a ‘‘normal’’ pace. Plantar foot contact area and the vertical ground reaction force were collected at 400 Hz. One CN patients received Charcot midfoot reconstruction surgery in the method described by Bevilacqua and Rogers [15] and his plantar pressure data was explored at 6 and 12 months after surgery to examine whether RF score can screen the improvement in dynamic plantar loading post-operation. The reconstructive procedure included a tendo-Achilles lengthening, a tarsometatarsal joint fusion and a Keller arthroplasty. The patient remained non-weightbearing in an external fixator for 10 weeks. The patient then slowly transitioned to weightbearing with a Charcot Restraint Orthotic Walker (CROW) and then extra-depth shoes with custom inserts at 5 months post-operatively. 2.5. Statistical analysis Comparisons in CN subjects for gait speed and RF values before and after surgery were made using Wilcoxon rank sum test. The same test was used to examine any difference between the average of gait speed and the subject speed at the time of stepping on platform. Comparisons for healthy subjects across the three walking speeds were made using one-way ANOVA and Scheffe’s Post Hoc test. Pearson’s correlation coefficient was calculated for peak pressures and walking speeds. For all tests an alpha level of 0.05 was considered statistically significant. All calculations were made using Matlab (MathWorks, Ver 7.4 (R2007a)).
3. Results 3.1. RF score and speed dependency There was no significant difference between the gait speed at the time of stepping on platform and average gait speed after excluding first two and last two steps (p = 0.68). This suggests that subjects did not slowdown for touching the platform. Fig. 2 summarizes the results. In healthy subjects (N = 15), the RF were 0.46 0.10; 0.45 0.07, and 0.43 0.08 respectively for habitual, slow and fast gait speeds suggesting that the pattern of plantar pressure distribution was close to normal shape (Gaussian shape) in healthy subjects irrespective of gait speed. When subjects increased their gait speed by 29% (p < 10 5, Fig. 2B) from slow to habitual, the plantar pressure magnitude (PPM) was increased by 8% (p < 10 5, Fig. 2C). Similar results were observed by comparing the data when subjects increased (25%) their gait speed from habitual to fast (7% increase in PPM, p < 10 6). This suggests that the PPM changes as a function of gait speed (p < 0.05, ANOVA—one-way test). We did not
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observe any significant correlation between gait speed and PPM in both slow and habitual gait speed trials (slow speed trials: r = 0.42, p = 0.13; habitual speed: r = 0.29, p = 0.31), suggesting that the relationship between gait speed and PPM is not linear. However, a small but significant correlation was observed between gait speed and PPM for fast speed trials (r = 0.54, p < 0.05) or by taking into account all speed trials together (r = 0.55, p < 0.05, 95%CI = [0.30,0.73]). Interestingly, no significant difference was observed in RF values for all speed trials (p = 0.55, ANOVA—one-way, see Fig. 2D) suggesting that RF is independent of gait speed. On the same note, no significant correlation was observed between gait speed and RF values for all trials (slow: r = 0.25, p = 0.39; habitual: r = 0.05, p = 0.85; fast: r = 0.01, p = 0.97) even by taking into account of all speed trials together (r = 0.09, p = 0.53, 95%CI = [ 0.39,0.21]). 3.2. RF score and dynamic plantar loading in CN patients Fig. 3 summarizes the results for pre- and post-operative case. The stance duration for pre-operation trials (one subject, three measurements), was 1.0 0.03 s versus 0.85 0.02 s for the same subject in post-operation trials (one subject, two follow-up and six measurements, see Fig. 3A). This shows a 15% improvement in gait speed following operation (p < 0.0001). Fig. 3B illustrates pattern of plantar pressure for a typical pre-operation trial and two postoperation trials for the same patient. Interestingly, only one of the post-operation trial’s PPM is reduced compared to the pre-operation trial, suggesting that PPM alone may be inappropriate when studying the effects of foot surgery. However, RF value was always negative or close to zero for pre-operation trials, and increased significantly postfoot reconstruction surgery (Fig. 4) indicating a transition to normal plantar distribution after Charcot reconstruction (see Fig. 3C). Interestingly, no significant difference was observed between RF values estimated in post-operation trials and healthy subjects (p = 0.43). Fig. 4 recaps the results of RF values in healthy subjects (for habitual and slow speed trials) as well as for all trials obtained in pre-operation patients (four subjects) as well as the post-operation case. These results demonstrate that although PPM value can be used to discriminate between CN patients from healthy subjects, it cannot discriminate between pre- and post-Charcot reconstruction surgery. While, using a simple threshold for RF values, the postoperative cases can be separated from pre-operative cases, suggesting that RF value can be used as a sensitive outcome for screening the improvement in dynamic plantar loading after treatment.
Fig. 2. RF speed dependency. (A) Experimental setup: subjects instructed to walk – barefoot – at least 10 m and three different speeds: slow, habitual, and fast. Physilog gait analyzer system was used to control spatio-temporal parameters of gait. Plantar pressure data was obtained using Emed-X platform. (B) Gait speed was increased by 29% and 62% from slow speed trials to respectively habitual and fast gait speed. (C) The increase in gait speed causes a highly significant increase in peak of plantar pressure. (D) Interestingly, there was not a significant change in RF value suggesting that RF score is independent of gait speed.
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Fig. 3. (A) The duration of stance averged cross pre-opertive cases versus post-operative trials. The stance duration was significatly reduced after surgery, indicating an improvement in patient’s gait speed. (B) Profile of plantar pressure for a typical Charcot case pre-operation (red color) and two follow-up trials post-operation (blue and green curves). The normal pressure distribution of gait usually shows two peaks, one originating from the heel and the other from the forefoot. The peaks associated with a rocker bottom foot differ significantly, primarily due to a large peak at the midfoot (red color curve). Surgical reconstruction can reduce the rocker-bottom deformity and consequently improve the dynamic plantar pressure pattern. The challenge is however characterization of this pattern to screen reliably the improvement post-surgery. (C) RF value can be used as a reliable score for screening plantar loading improvement following foot reconstruction. The symbol ‘*’ represents a statistically significant difference with p-value less than 0.05. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of the article.)
4. Discussion 4.1. Plantar pressure magnitude, its application in screening the dynamic plantar loading, and its shortcomings Pedobarography has been described before and after surgical procedures of the foot [16–25]. Changes in magnitude and location of peak pressures have been described [18,20,25]. These changes are dependent on the reconstructive procedure and location of the masks. The RF addresses the heterogeneity described in these reports by describing a global distribution of peak pressures compared to normal gait. Alternatively in patients with diabetes, regional forefoot amputations and panmetatarsal head resections can increase peak pressures in the foot [16,23,26]. Quite possibly
these are due to changes in gait speed or regional differences in loading patterns. The RF suggested in this study addresses both of these limitations. 4.2. Plantar pressure magnitude and its application in predicting the risk of ulceration The treatment provided to prevent and to heal ulcers is dictated by mitigating site specific physical trauma; however, the interpretation of risk associated with absolute peak pressure values is challenging. Previous research established that as PPM increases, a concurrent increase in risk of ulceration occurs [27,28]. Armstrong et al. subsequently endeavored to determine a critical level of pressure that would predict future ulceration [29]. Although their results provided additional credence to the relationship between pressure magnitude and ulceration risk, a definitive critical pressure magnitude could not be identified. One likely reason for this was inter-subject variability in soft tissue properties and skeletal structures leading to variability in the amount of trauma subjects could endure prior to ulcerating. Additionally, between trials intra-subject variability such as walking speed can make it difficult to identify peak pressure values within an individual. By disregarding absolute pressure values, the RF score appears to provide a value that can be universally interpreted across subjects and across trials. While the RF score will not identify the cause of pathological plantar loading it does appear well suited to discriminating between normal and pathological loading. In the future the tool may prove to be useful for triaging, which patients require a more detailed (and somewhat subjective) assessment of regionalized peak pressures and which patients do not. 4.3. Plantar pressure magnitude in CN patients
Fig. 4. RF values for healthy subjects (green color), pre-operative trials (blue color) and post-operative trials (red color). Although peak plantar pressure can discriminate Charcot cases from healthy subjects, it is unable to distinguish preand post-operation cases. While using the RF score, however, improvements of dynamic plantar loading behavior can be seen post-operation. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of the article.)
Diagnosing Charcot neuroarthropathy requires a heightened index of suspicion [15]. Early recognition and intervention can limit deformity. However, oftentimes patients present with an unstable deformity that is not amendable to conservative care alone. In these cases, Charcot reconstruction is necessary for limb salvage. Charcot reconstruction has been shown to be an effective method of correcting the deformity and providing a stable, plantigrade, foot [30–33]. Researchers have investigated plantar pressures in those with rocker-bottom deformities and found an increase in the pressure/
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time integral during the midstance phase of gait [34]. For example, Armstrong and Lavery reported greater peak plantar pressure in those with acute Charcot foot than persons with diabetic neuropathy and no history of Charcot neuroarthropathy [7]. Interestingly, CN peak pressures were even higher than people with neuropathic ulceration [7]. However, we are unaware of studies in the medical literature that objectively addressed the impact of Charcot reconstruction upon gait. Traditional analyses of foot kinetics were generally indicative of improvement in the subject’s gait following surgery. The newly introduced RF analysis of the peak pressure profile allowed for analysis of the pressure profile independent of the temporal profile or absolute peak pressure. While the preoperative pressure profile had an irregular statistical distribution and subsequently negative RF value, both the post-operative and healthy pressure profiles were much more Gaussian or normal in shape and yielded positive RF values. Therefore, the results of this initial case study support the use of the RF value as an objective and less biased means of evaluating plantar loading.
(approximately 4 m, 3rd step). The protocol for healthy subjects was specifically designed for validating the RF, and was done so to allow for manipulating variables such as walking speed. The protocol utilized with the Charcot patients was that which is typically utilized in clinic. If the patients had walked a greater distance it may have impacted the peak pressure values, however the validation study in the healthy subjects indicates that the RF scores would not have been impacted. Fourth, RF had a tendency to decrease – but not significantly – for the fast speed trials (average speed: 1.52 0.15 m/s). This may be due to sample frequency restriction of the Emed Platform, which may affect the resolution of estimating plantar pressure distribution, when subject is walking fast. We believe this limitation will not affect the clinical application of RF score, since it is unlikely to have such a fast gait speed in particular for preferred gait speed in pre- and/or post-operative trials. Finally, this study focused on dynamic behavior of plantar pressure during barefoot condition. Further study is required to explore whether a similar statistical distribution may be observed during shod condition in both healthy and CN subjects.
4.4. Plantar pressure distribution in CN patients
5. Conclusion
The standard pressure profile during stance phase usually shows two peaks, one originating from the heel and the other from the forefoot. The peaks associated with a rocker bottom foot due to CN, differ significantly, primarily due to a large peak at the midfoot. This alteration in peaks results in a plantar pressure profile with a statistical distribution that greatly differs from a normal curve. Clinicians also observe a qualitative anecdotal rocking back and forth of dynamic pressures in the midfoot with little preservation of forward momentum. Pressure–time integral does not appear to be an adequate construct to address this observation. Fitting the plantar pressure distribution data to a customized normal distribution yields a sensitive parameter (RF) that can be used to screen this abnormality. Therefore, RF value can be used as an objective outcome to evaluate the improvement in dynamic plantar loading post-foot CN treatment. Interestingly, RF value is also independent of gait speed and hence can overcome the shortcoming of plantar pressure magnitude that is speed dependent. This may also facilitate the protocol of pedography measurement, which in general required controlling the subject’s gait speed.
The RF appears to be independent of gait speed and offers a potentially sensitive and global interpretation of peak pressure distribution before and after foot surgery. Further larger studies are needed to observe if these relationships remain consistent. Furthermore, further testing involving both barefoot as well as in-shoe conditions may elicit a clinical outcome measure and possibly be integrated into clinical practice and telemonitoring using intelligent insoles for early recognition of Charcot neuroarthropathy.
4.5. Shortcomings/limitations of this study and future works There are several shortcomings in this study that should be addressed. First, due to recruiting limitation for Charcot foot cases, only a few subjects were involved in pre-operation cases and only one subject followed the foot reconstruction study. This was mainly because Charcot neuroarthropathy is a rather rare but exceedingly important sub population of diabetic foot complications. These patients are frequently misdiagnosed as having bone infection and therefore are frequently amputated. Identifying these patients and selecting who may benefit (and, importantly, who may not) from targeted surgical reconstruction is of prime importance. The reason studies of this type have not yet taken place are precisely because of the lack of pairing of surgically busy units and teams with expertise in motion and human performance analysis. This makes this pairing of applied researchers particularly promising. Further study is required to clinically validate the sensitivity of RF value for CN foot reconstruction outcome evaluation. Second, we had no formal sample size estimation in this pilot study. A future larger study powered using our point estimates and dispersion will further elucidate gait speed independence. Third, the Emed protocol for healthy subjects (minimum 10 m, 6th step) was different than CN subjects
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Gait & Posture journal homepage: www.elsevier.com/locate/gaitpost
Can we predict outcome of surgical reconstruction of Charcot neuroarthropathy by dynamic plantar pressure assessment?—A proof of concept study Bijan Najafi a,*, Ryan T. Crews a, David G. Armstrong b, Lee C. Rogers c, Kamiar Aminian d, James Wrobel a a
Scholl’s Center for Lower Extremity Ambulatory Research (CLEAR), Rosalind Franklin University of Medicine and Science, North Chicago, IL, USA Southern Arizona Limb Salvage Alliance (SALSA), Department of Surgery, University of Arizona, Tucson, AZ, USA c Amputation Prevention Center at Valley Presbyterian Hospital, Los Angeles, CA, USA d Ecole Polytechnique Federale de Lausanne, Laboratory of Movement Analysis & Measurement, Lausanne, Switzerland b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 3 December 2008 Received in revised form 8 September 2009 Accepted 12 September 2009
The joint deformity that arises as a result of Charcot neuroarthropathy, leads to gait modification. Ulceration risk associated with the deformity is generally assessed by measuring plantar pressure magnitude (PPM). However, as PPM is partially dependent on gait speed and treatment interventions may impact speed, the use of PPM to validate treatment is not ideal. This study suggests a novel assessment protocol, which is speed independent and can objectively (1) characterize abnormality in dynamic plantar loading in patients with foot Charcot neuroarthropathy and (2) screen improvement in dynamic plantar loading after foot reconstruction surgery. To examine whether the plantar pressure distribution (PPD) measured using EMED platform, was normal, a customized normal distribution curve was created for each trial. Then the original PPD was fitted to the customized normal distribution curve. This technique yields a regression factor (RF), which represents the similarity of the actual pressure distribution with a normal distribution. RF values may range from negative 1 to positive 1 and as the value increases positively so does the similarity between the actual and normalized pressure distributions. We tested this novel score on the plantar pressure pattern of healthy subjects (N = 15), Charcot patients pre-operation (N = 4) and a Charcot patient post-foot reconstruction (N = 1). In healthy subjects, the RF was 0.46 0.1. When subjects increased their gait speed by 29%, PPM was increased by 8% (p < 10 5), while RF was not changed (p = 0.55), suggesting that RF value is independent of gait speed. In preoperative Charcot patients, the RF < 0, however, RF increased post-surgery (RF = 0.42), indicating a transition to normal plantar distribution after Charcot reconstruction. ß 2009 Elsevier B.V. All rights reserved.
Keywords: Charcot neuroarthropathy Diabetes Diabetic foot Outcome assessment (health care) Foot Gait Kinetics Arthropathy Neurogenic Pedography Plantar pressure Joint deformity Foot reconstruction Foot joint deformity Podiatric
1. Introduction Charcot neuroarthropathy (CN) or Charcot foot is a devastating condition occurring most commonly in those with diabetes complicated by peripheral neuropathy and frequently leads to limb loss [1,2]. The pathogenesis is not well understood, but it is generally agreed trauma (micro-repetitive or single-instance macrotrauma) in the presence of neuropathy is required to spark this syndrome [3]. Trauma precipitates an inflammatory cascade and vasodilation [4]. The vasodilation may ‘‘wash out’’ minerals
* Corresponding author at: Human Performance Lab., Shcoll’s Center for Lower Extremity Ambulatory Research (CLEAR), The Dr. William M. Scholl College of Podiatric Medicine, Rosalind Franklin University of Medicine & Science, 3333 Green Bay Road, North Chicago, IL 60064-3037, USA. Tel.: +1 847 578 8456; fax: +1 847 775 6570. E-mail address: bijan.najafi@rosalindfranklin.edu (B. Najafi). URL: http://www.CLEAR-Scholl.org 0966-6362/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.gaitpost.2009.09.003
from the bone reducing density and thereby making one more susceptible to fractures. This, coupled with glycosylation of periarticular tissue, particularly the Achilles tendon, may make the person with Charcot arthropathy of the foot prone to its characteristically impressive fracture-dislocations. Treatment of CN depends on the stage during which it is diagnosed [5]. Early diagnosis is challenging, but allows the opportunity to intervene and prevent development or worsening of such deformities. Distribution and magnitudes of plantar pressure during gait can provide insight into functional manifestations of foot and ankle disorders and may be used for early diagnosis of abnormal foot biomechanics due to CN. Additionally, these dynamic measurements often serve as objective measures for outcomes evaluation following foot surgery and can be used to track disease progression [6–10]. However, plantar pressure magnitude (PPM) alone may be inappropriate when studying the effects of foot surgery. Following corrective foot surgery, patients will many times increase their gait speed as a result of
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greater confidence and stability, and a more efficient gait pattern. Although this increase may be practically advantageous, it may also increase PPM, historically viewed as a negative outcome. For a fair evaluation of the success of surgery, a novel and speed independent variable is required that reflects improved foot biomechanics post-surgery. The objective of this investigation is to develop a novel assessment protocol which is speed independent and by which plantar pressure modification during gait could be objectively characterized. From a clinical standpoint, the purpose of this manuscript was to be a proof of concept trial for validating this novel assessment protocol to (1) screen abnormal plantar loading due to CN and (2) evaluate the success of foot reconstruction surgery to improve functional gait as well as dynamic plantar loading. To our best knowledge, this is the first study that has thoroughly and objectively addressed the impact of Charcot reconstruction upon gait.
case. All histograms were estimated using a 30-bins scheme (selected arbitrarily). Then, the original plantar pressure distribution was fitted to the customized normal distribution curve using a multiple linear regression approach. This technique yields a regression factor (RF), which represents the similarity of the actual pressure distribution with the normalized distribution. RF values may range from negative 1 to positive 1 and as the value increases positively so does the similarity between the actual and normalized pressure distributions. This process yields a simple value to represent an abnormality in dynamic plantar loading due to foot CN (see Fig. 1F). 2.3. First study: is the RF score, speed independent? To examine whether the RF score is speed independent, pressure profiles were measured for 15 healthy subjects walking at multiple speeds. 2.3.1. Subjects recruitment 15 healthy subjects (6 female, 9 male) were recruited with an average age 24.2 1.78 years, average height 173.77 14.02 cm, and average body mass 76.44 17.5 kg. The study received ethical approval in accordance with the local institutional review board. All subjects provided informed consent prior to the start of testing.
2. Methods 2.1. General hypothesis Our efforts to develop a reliable outcome measure for objectively assessing plantar loading post-reconstruction relied on two hypotheses: (1) the statistical distribution of plantar pressure during stance is independent of gait speed; and (2) any biomechanical change (or joint deformity) will affect the pattern of plantar pressure profile during gait. 2.2. Approach description Fig. 1A illustrates the temporal pattern of plantar pressure magnitude (PPM) during stance phase for three cases: a typical healthy subject, a CN patient preoperation and post-operation. The stance duration is visibly different for each pattern. This consequently may alter the temporal profile of the pressure pattern, further complicating healthy and pre/post-surgical comparisons. To overcome this shortcoming, a time-scale normalization scheme was used to moderate the effect of gait speed across different steps’ pressure profiles. For this purpose, we implemented a classical linear interpolation/decimation scheme to standardize stance duration for each step trial (see Fig. 1B). After normalizing the time-scale, we estimated the statistical distribution of the total-foot peak plantar pressure profile (see Fig. 1C). Examining the distribution pattern, we noticed that in healthy cases as well as the post-operative case, the distribution was similar to a normal– Gaussian-distribution (see Fig. 1D and E), while in pre-operative cases the distribution shape was far from a normal shape (see Fig. 1C). To attribute a numeric value to this abnormality pattern, a customized normal distribution curve was created for each trial utilizing the mean, standard deviation, and maximum probability values for the trial. These variables enable simulation of a normal distribution, which can represent the plantar distribution pattern in each
2.3.2. Measurement protocol Subjects walked – barefoot – at least 10 m at three different speeds: slow (very leisurely walk), habitual (preferred), and fast (as fast as they could safely walk). At least one practice trial occurred before each test, and each test was repeated twice. The two trials’ average was considered for the final analysis. The primary objective of these tests was to explore the relationship between gait speed and plantar pressure distribution. To control spatio-temporal parameters of gait, angular rate sensors (gyroscopes) and a Physilog1 ambulatory datalogger (Physilog1, BioAGM, CH) system were used. Elastic bands attached gyroscopes (Analog device, Inc., Norwood, Massachusetts) to each shank and each thigh. Each sensor measured the angular velocity of the segment around the medio-lateral axis (flexion–extension). Signals were digitized (16 bit) at a sampling rate of 200 Hz and stored for off-line processing on a SD memory card (512 Mb). The method for calculating the spatio-temporal parameters of gait is described in detail elsewhere [11–14]. Plantar pressure data was obtained by an Emed-X1 (Novel-Germany) platform. Subjects were allotted practice trials in order to successfully hit the platform on the 6th step during the varied gait speeds aforementioned. Floor markers were implemented in order to ensure proper gait repetition. To estimate the gait speed at the time of stepping on platform, an observer noted the number of steps taken by the subject from gait initiation until stepping on the platform. Then the gait speed corresponding to that step was estimated using Physilog data. The measured speed was compared to the average gait speed (excluding first two and last two steps) to ensure the subject did not slowdown before touching the platform. Plantar foot contact area and the vertical ground reaction force were collected at 400 Hz. To assess the plantar pressure profile, we calculated the peak pressure magnitude as a function of time using Novel1 multimasking software (version 14.3.8e).
Fig. 1. (A) Plantar pressure profile for a typical healthy subject and a typical CN patient pre- and post-operation. The duration of stance is different between three patterns, suggesting that gait speed is different between them. (B) A time-scale normalization scheme was used to moderate the effect of gait speed. The plantar pressure distribution profile in (C) Charcot case pre-operation, (D) post-operation, and (E) healthy subject. (F) RF estimated for patients pre-op (red color), post-op (blue color), and healthy (green color) subject. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of the article.)
B. Najafi et al. / Gait & Posture 31 (2010) 87–92 2.4. Second study: can the RF score screen abnormal plantar loading due to CN and its improvement post-foot reconstruction? To examine whether the RF value can be used to screen the abnormal plantar loading, we measured the plantar pressure loading during gait in four patients (men, age: 54 4 years old; body mass: 97.6 13.5 kg; height: 178.3 2.9 cm) with diabetes and Charcot foot deformities. At each visit the patients completed three barefoot walking trials with the Emed-X platform. Patients initiated gait approximately 1.5 m prior to the platform and upon stepping on the platform continued walking straight ahead approximately 2 m. The subjects were instructed to walk at a ‘‘normal’’ pace. Plantar foot contact area and the vertical ground reaction force were collected at 400 Hz. One CN patients received Charcot midfoot reconstruction surgery in the method described by Bevilacqua and Rogers [15] and his plantar pressure data was explored at 6 and 12 months after surgery to examine whether RF score can screen the improvement in dynamic plantar loading post-operation. The reconstructive procedure included a tendo-Achilles lengthening, a tarsometatarsal joint fusion and a Keller arthroplasty. The patient remained non-weightbearing in an external fixator for 10 weeks. The patient then slowly transitioned to weightbearing with a Charcot Restraint Orthotic Walker (CROW) and then extra-depth shoes with custom inserts at 5 months post-operatively. 2.5. Statistical analysis Comparisons in CN subjects for gait speed and RF values before and after surgery were made using Wilcoxon rank sum test. The same test was used to examine any difference between the average of gait speed and the subject speed at the time of stepping on platform. Comparisons for healthy subjects across the three walking speeds were made using one-way ANOVA and Scheffe’s Post Hoc test. Pearson’s correlation coefficient was calculated for peak pressures and walking speeds. For all tests an alpha level of 0.05 was considered statistically significant. All calculations were made using Matlab (MathWorks, Ver 7.4 (R2007a)).
3. Results 3.1. RF score and speed dependency There was no significant difference between the gait speed at the time of stepping on platform and average gait speed after excluding first two and last two steps (p = 0.68). This suggests that subjects did not slowdown for touching the platform. Fig. 2 summarizes the results. In healthy subjects (N = 15), the RF were 0.46 0.10; 0.45 0.07, and 0.43 0.08 respectively for habitual, slow and fast gait speeds suggesting that the pattern of plantar pressure distribution was close to normal shape (Gaussian shape) in healthy subjects irrespective of gait speed. When subjects increased their gait speed by 29% (p < 10 5, Fig. 2B) from slow to habitual, the plantar pressure magnitude (PPM) was increased by 8% (p < 10 5, Fig. 2C). Similar results were observed by comparing the data when subjects increased (25%) their gait speed from habitual to fast (7% increase in PPM, p < 10 6). This suggests that the PPM changes as a function of gait speed (p < 0.05, ANOVA—one-way test). We did not
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observe any significant correlation between gait speed and PPM in both slow and habitual gait speed trials (slow speed trials: r = 0.42, p = 0.13; habitual speed: r = 0.29, p = 0.31), suggesting that the relationship between gait speed and PPM is not linear. However, a small but significant correlation was observed between gait speed and PPM for fast speed trials (r = 0.54, p < 0.05) or by taking into account all speed trials together (r = 0.55, p < 0.05, 95%CI = [0.30,0.73]). Interestingly, no significant difference was observed in RF values for all speed trials (p = 0.55, ANOVA—one-way, see Fig. 2D) suggesting that RF is independent of gait speed. On the same note, no significant correlation was observed between gait speed and RF values for all trials (slow: r = 0.25, p = 0.39; habitual: r = 0.05, p = 0.85; fast: r = 0.01, p = 0.97) even by taking into account of all speed trials together (r = 0.09, p = 0.53, 95%CI = [ 0.39,0.21]). 3.2. RF score and dynamic plantar loading in CN patients Fig. 3 summarizes the results for pre- and post-operative case. The stance duration for pre-operation trials (one subject, three measurements), was 1.0 0.03 s versus 0.85 0.02 s for the same subject in post-operation trials (one subject, two follow-up and six measurements, see Fig. 3A). This shows a 15% improvement in gait speed following operation (p < 0.0001). Fig. 3B illustrates pattern of plantar pressure for a typical pre-operation trial and two postoperation trials for the same patient. Interestingly, only one of the post-operation trial’s PPM is reduced compared to the pre-operation trial, suggesting that PPM alone may be inappropriate when studying the effects of foot surgery. However, RF value was always negative or close to zero for pre-operation trials, and increased significantly postfoot reconstruction surgery (Fig. 4) indicating a transition to normal plantar distribution after Charcot reconstruction (see Fig. 3C). Interestingly, no significant difference was observed between RF values estimated in post-operation trials and healthy subjects (p = 0.43). Fig. 4 recaps the results of RF values in healthy subjects (for habitual and slow speed trials) as well as for all trials obtained in pre-operation patients (four subjects) as well as the post-operation case. These results demonstrate that although PPM value can be used to discriminate between CN patients from healthy subjects, it cannot discriminate between pre- and post-Charcot reconstruction surgery. While, using a simple threshold for RF values, the postoperative cases can be separated from pre-operative cases, suggesting that RF value can be used as a sensitive outcome for screening the improvement in dynamic plantar loading after treatment.
Fig. 2. RF speed dependency. (A) Experimental setup: subjects instructed to walk – barefoot – at least 10 m and three different speeds: slow, habitual, and fast. Physilog gait analyzer system was used to control spatio-temporal parameters of gait. Plantar pressure data was obtained using Emed-X platform. (B) Gait speed was increased by 29% and 62% from slow speed trials to respectively habitual and fast gait speed. (C) The increase in gait speed causes a highly significant increase in peak of plantar pressure. (D) Interestingly, there was not a significant change in RF value suggesting that RF score is independent of gait speed.
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Fig. 3. (A) The duration of stance averged cross pre-opertive cases versus post-operative trials. The stance duration was significatly reduced after surgery, indicating an improvement in patient’s gait speed. (B) Profile of plantar pressure for a typical Charcot case pre-operation (red color) and two follow-up trials post-operation (blue and green curves). The normal pressure distribution of gait usually shows two peaks, one originating from the heel and the other from the forefoot. The peaks associated with a rocker bottom foot differ significantly, primarily due to a large peak at the midfoot (red color curve). Surgical reconstruction can reduce the rocker-bottom deformity and consequently improve the dynamic plantar pressure pattern. The challenge is however characterization of this pattern to screen reliably the improvement post-surgery. (C) RF value can be used as a reliable score for screening plantar loading improvement following foot reconstruction. The symbol ‘*’ represents a statistically significant difference with p-value less than 0.05. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of the article.)
4. Discussion 4.1. Plantar pressure magnitude, its application in screening the dynamic plantar loading, and its shortcomings Pedobarography has been described before and after surgical procedures of the foot [16–25]. Changes in magnitude and location of peak pressures have been described [18,20,25]. These changes are dependent on the reconstructive procedure and location of the masks. The RF addresses the heterogeneity described in these reports by describing a global distribution of peak pressures compared to normal gait. Alternatively in patients with diabetes, regional forefoot amputations and panmetatarsal head resections can increase peak pressures in the foot [16,23,26]. Quite possibly
these are due to changes in gait speed or regional differences in loading patterns. The RF suggested in this study addresses both of these limitations. 4.2. Plantar pressure magnitude and its application in predicting the risk of ulceration The treatment provided to prevent and to heal ulcers is dictated by mitigating site specific physical trauma; however, the interpretation of risk associated with absolute peak pressure values is challenging. Previous research established that as PPM increases, a concurrent increase in risk of ulceration occurs [27,28]. Armstrong et al. subsequently endeavored to determine a critical level of pressure that would predict future ulceration [29]. Although their results provided additional credence to the relationship between pressure magnitude and ulceration risk, a definitive critical pressure magnitude could not be identified. One likely reason for this was inter-subject variability in soft tissue properties and skeletal structures leading to variability in the amount of trauma subjects could endure prior to ulcerating. Additionally, between trials intra-subject variability such as walking speed can make it difficult to identify peak pressure values within an individual. By disregarding absolute pressure values, the RF score appears to provide a value that can be universally interpreted across subjects and across trials. While the RF score will not identify the cause of pathological plantar loading it does appear well suited to discriminating between normal and pathological loading. In the future the tool may prove to be useful for triaging, which patients require a more detailed (and somewhat subjective) assessment of regionalized peak pressures and which patients do not. 4.3. Plantar pressure magnitude in CN patients
Fig. 4. RF values for healthy subjects (green color), pre-operative trials (blue color) and post-operative trials (red color). Although peak plantar pressure can discriminate Charcot cases from healthy subjects, it is unable to distinguish preand post-operation cases. While using the RF score, however, improvements of dynamic plantar loading behavior can be seen post-operation. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of the article.)
Diagnosing Charcot neuroarthropathy requires a heightened index of suspicion [15]. Early recognition and intervention can limit deformity. However, oftentimes patients present with an unstable deformity that is not amendable to conservative care alone. In these cases, Charcot reconstruction is necessary for limb salvage. Charcot reconstruction has been shown to be an effective method of correcting the deformity and providing a stable, plantigrade, foot [30–33]. Researchers have investigated plantar pressures in those with rocker-bottom deformities and found an increase in the pressure/
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time integral during the midstance phase of gait [34]. For example, Armstrong and Lavery reported greater peak plantar pressure in those with acute Charcot foot than persons with diabetic neuropathy and no history of Charcot neuroarthropathy [7]. Interestingly, CN peak pressures were even higher than people with neuropathic ulceration [7]. However, we are unaware of studies in the medical literature that objectively addressed the impact of Charcot reconstruction upon gait. Traditional analyses of foot kinetics were generally indicative of improvement in the subject’s gait following surgery. The newly introduced RF analysis of the peak pressure profile allowed for analysis of the pressure profile independent of the temporal profile or absolute peak pressure. While the preoperative pressure profile had an irregular statistical distribution and subsequently negative RF value, both the post-operative and healthy pressure profiles were much more Gaussian or normal in shape and yielded positive RF values. Therefore, the results of this initial case study support the use of the RF value as an objective and less biased means of evaluating plantar loading.
(approximately 4 m, 3rd step). The protocol for healthy subjects was specifically designed for validating the RF, and was done so to allow for manipulating variables such as walking speed. The protocol utilized with the Charcot patients was that which is typically utilized in clinic. If the patients had walked a greater distance it may have impacted the peak pressure values, however the validation study in the healthy subjects indicates that the RF scores would not have been impacted. Fourth, RF had a tendency to decrease – but not significantly – for the fast speed trials (average speed: 1.52 0.15 m/s). This may be due to sample frequency restriction of the Emed Platform, which may affect the resolution of estimating plantar pressure distribution, when subject is walking fast. We believe this limitation will not affect the clinical application of RF score, since it is unlikely to have such a fast gait speed in particular for preferred gait speed in pre- and/or post-operative trials. Finally, this study focused on dynamic behavior of plantar pressure during barefoot condition. Further study is required to explore whether a similar statistical distribution may be observed during shod condition in both healthy and CN subjects.
4.4. Plantar pressure distribution in CN patients
5. Conclusion
The standard pressure profile during stance phase usually shows two peaks, one originating from the heel and the other from the forefoot. The peaks associated with a rocker bottom foot due to CN, differ significantly, primarily due to a large peak at the midfoot. This alteration in peaks results in a plantar pressure profile with a statistical distribution that greatly differs from a normal curve. Clinicians also observe a qualitative anecdotal rocking back and forth of dynamic pressures in the midfoot with little preservation of forward momentum. Pressure–time integral does not appear to be an adequate construct to address this observation. Fitting the plantar pressure distribution data to a customized normal distribution yields a sensitive parameter (RF) that can be used to screen this abnormality. Therefore, RF value can be used as an objective outcome to evaluate the improvement in dynamic plantar loading post-foot CN treatment. Interestingly, RF value is also independent of gait speed and hence can overcome the shortcoming of plantar pressure magnitude that is speed dependent. This may also facilitate the protocol of pedography measurement, which in general required controlling the subject’s gait speed.
The RF appears to be independent of gait speed and offers a potentially sensitive and global interpretation of peak pressure distribution before and after foot surgery. Further larger studies are needed to observe if these relationships remain consistent. Furthermore, further testing involving both barefoot as well as in-shoe conditions may elicit a clinical outcome measure and possibly be integrated into clinical practice and telemonitoring using intelligent insoles for early recognition of Charcot neuroarthropathy.
4.5. Shortcomings/limitations of this study and future works There are several shortcomings in this study that should be addressed. First, due to recruiting limitation for Charcot foot cases, only a few subjects were involved in pre-operation cases and only one subject followed the foot reconstruction study. This was mainly because Charcot neuroarthropathy is a rather rare but exceedingly important sub population of diabetic foot complications. These patients are frequently misdiagnosed as having bone infection and therefore are frequently amputated. Identifying these patients and selecting who may benefit (and, importantly, who may not) from targeted surgical reconstruction is of prime importance. The reason studies of this type have not yet taken place are precisely because of the lack of pairing of surgically busy units and teams with expertise in motion and human performance analysis. This makes this pairing of applied researchers particularly promising. Further study is required to clinically validate the sensitivity of RF value for CN foot reconstruction outcome evaluation. Second, we had no formal sample size estimation in this pilot study. A future larger study powered using our point estimates and dispersion will further elucidate gait speed independence. Third, the Emed protocol for healthy subjects (minimum 10 m, 6th step) was different than CN subjects
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