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OY Kwon, PT, PhD, is Assistant Professor, Department of Rehabilitation Therapy, College of Health Science, Yonsei University, Wonju-si, Kangwon-do, Korea. Dr Kwon was a postdoctoral fellow at Movement Science Lab, Program in Physical Therapy, Washington University School of Medicine, St Louis, Mo, when this project was conducted
MJ Mueller, PT, PhD, is Associate Professor, Program in Physical Therapy, Washington University School of Medicine, 4444 Forest Park Blvd, Campus Box 8502, St Louis, MO 63110-2292 (USA) (muellermi{at}msnotes.wustl.edu). Address all correspondence to Dr Mueller
Key Words: Diabetic neuropathy Diabetic ulcers Forefoot pressure Walking patterns
| Introduction |
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In people with peripheral sensory neuropathy, the ability to respond to potentially injurious stimuli is diminished or lost. There is also atrophy of the intrinsic muscles of the foot because of motor neuropathy. This muscle atrophy causes instability of the metatarsophalangeal joints and anterior migration and displacement of the fat pad that is normally located directly under the metatarsal heads.9,10 Anterior displacement of the fat pad makes the forefoot more vulnerable to injury from accumulated trauma during walking.9 Brand10 has emphasized the role of decreased sensation and excessive, repetitive mechanical pressure as principal factors leading to plantar ulceration. High plantar pressures may lead to the breakdown of tissue and the formation of ulcers. These lesions often are followed by infection, gangrene, and amputation.11
Because abnormally high plantar foot pressures in people with diabetic neuropathies have been linked to the development of foot ulcers, plantar pressures have become a focus of research.12 Boulton and associates13 reported that 51% of their subjects with diabetes and neuropathic feet had abnormally high pressures underneath the metatarsal heads compared with 17% of subjects with diabetes who had no peripheral neuropathies and 7% of subjects without diabetes. They suggested that measurements of foot pressure may be useful for predicting the occurrence of ulcers and for guiding the management of care because areas susceptible to ulceration could be determined. Armstrong and associates12 also found that mean peak plantar pressures were higher for patients with ulcers (83.1±24.7 N/cm2) than for patients without ulcers (62.7±24.4 N/cm2).
Ulcers commonly occur under the first, second, or third metatarsal head and under the great toe,14 and most neuropathic ulcers result from excessive and repetitive pressure applied to the foot while walking.15 High pressures in the forefoot occur primarily during the push-off phase of walking. During the push-off phase, the heel leaves the ground and the entire body weight is borne on the forefoot and toes. The heel and midfoot bear no weight, there may be only a few square inches to carry the weight of the body, and the pressures under the metatarsal heads or toes may rise to 414 kPa (60 psi).10 These pressures, if repeated too frequently, can result in inflammation and then ulceration in people who lack sensation to pain or pressure. Therefore, the primary target for prevention and healing of neuropathic plantar ulcers is pressure relief during walking.16
To help prevent soft tissue damage during walking, decreasing high plantar pressures may be critical. Plantar pressure is defined as:
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For example, applied force distributed over a greater area during walking results in lower plantar pressure in any one area.10,17 Pressure can be reduced by decreasing force or by increasing the weight-bearing area. Skin breakdown is related to both the duration and magnitude of pressure.10 Kosiak18 studied the relationships between the magnitude of external pressure and the time it takes to produce ulceration in the skin of anesthetized dogs. The results showed that ulcers were caused by either high pressures applied for a short duration (500 mm Hg for 2 hours) or low pressures applied for a long duration (150 mm Hg for 10-12 hours).
For people with diabetic neuropathies, many strategies are used to decrease peak plantar pressures during walking. Casting, molded insoles, rocker shoes, and therapeutic footwear have been used to spread the pressures, prevent the localized pressure on the forefoot, and increase the area of the weight-bearing force. Wertsch and associates19 studied average peak plantar pressures while people walked with a total contact cast and without the cast. They measured plantar pressures in 6 male subjects, aged 25 to 40 years, during walking with and without wearing a total contact cast. They found that, when compared with the values obtained without the cast, the average pressure decrease was 32% under the fifth metatarsal, 63% under the fourth metatarsal, 69% under the first metatarsal, 65% under the great toe, and 45% under the heel when the total contact cast was worn. A limitation of their study was that walking speed was not recorded. Chantelau and Haage20 reported that protective footwear relieved forefoot plantar pressures up to 50% compared with normal shoes and was effective in preventing ulcer recurrence in people with a history of diabetic foot ulceration when worn for more than 60% of the day. Edmonds and associates8 reported that the ulcer recurrence rate was 26% in people who wore prescribed footwear, as compared with 83% in people who wore their own shoes.
Although casts, accommodative orthotic devices, and protective footwear can be used to reduce plantar pressures in people with diabetes and neuropathies, some people may require additional means of reducing forefoot pressures. For instance, people cannot wear total contact casts all of the time. In addition, even when appropriate footwear was consistently used, 26% of the subjects in one study experienced recurrence of their ulcer.8 Therefore, additional interventions to reduce forefoot pressures may be needed to help prevent the recurrence of forefoot ulcers. The purpose of this update is to review walking patterns previously described in the literature that may be useful for reducing forefoot peak plantar pressures in people with diabetic neuropathies. A basic assumption in these studies is that reducing plantar pressures will reduce the subsequent risk for skin breakdown.
| Various Walking Patterns |
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Zhu and associates17 studied the effect of a shuffling gait pattern on foot pressure distribution during walking in 10 male subjects without known musculoskeletal or neuromuscular impairments (mean age=29.6 years, SD=5.8). Peak pressure, foot-to-floor contact duration (foot contact time on the floor), and pressure-time integral (area under the pressure-time curve) under each sensor (under the posterior and anterior heels, first metatarsal head, second metatarsal head, fourth metatarsal head, fifth metatarsal head, and hallux) during walking and shuffling were analyzed and compared. A shuffling gait was defined as a gait with foot flat throughout the stance phase, with limited heel-strike or toe-off, increasing the length of the mid-stance period. The authors showed that peak plantar pressures decreased under the first and second metatarsals (up to 57.8%) and the hallux (up to 63.2%) by using a shuffling gait pattern. Foot-to-floor contact duration during shuffling gait increased 22.0% under the left fifth metatarsal and 76.9% at right posterior heel compared with normal walking. Pressure-time integrals during shuffling were decreased under the metatarsal heads and great toe (up to 26.7%).
The reduction in plantar pressures found by Zhu and associates17 may have been due to a reduced push-off, or it may have been simply a result of decreased walking speed (ie, 0.51 m/s for shuffling versus 1.29 m/s for normal walking). Several authors2123 have shown that plantar pressure distribution is dependent on walking speed. Cook and associates21 studied the effects of walking speed on vertical ground reaction forces during walking in 36 male subjects without known pathologies or impairments that might affect gait. The mean age of subjects was 25.7 years (range=19-44). Three different walking speeds were selected: normal walking speed (1.3 m/s), a speed 30% slower than normal walking speed (0.9 m/s), and a speed 30% faster than normal walking speed (1.7 m/s). The results showed that walking speed affected the vertical ground reaction forces. The vertical ground reaction forces increased as walking cadence increased. Andriacchi and associates22 studied ground reaction forces that are related to walking speed. They examined data from 17 subjects without known pathologies or impairments that might affect gait (mean age=28 years, range=22-59) and 16 subjects with knee pathologies (mean age=65 years, range=48-76). Andriacchi and associates22 also found that peak medial-lateral, fore-aft, and vertical ground reaction forces (at heel-strike and toe-off) increased with walking speed and that the vertical force during mid-stance decreased with walking speed.
Zhu and associates23 studied the effect of cadence on in-shoe plantar pressures over extended periods of continuous walking in 8 male subjects without impairments. In-shoe plantar pressures were studied during 4 minutes of continuous walking at controlled cadences of 70, 80, 90, 100, 110, and 120 steps/min. For each cadence, a minimum of 200 steps were analyzed for each subject. The mean peak pressures were 551±235 kPa at 70 steps/min, 719±583 kPa at 80 steps/min, 758±580 kPa at 90 steps/min, 852±608 kPa at 100 steps/min, 875±600 kPa at 110 steps/min, and 899±519 kPa at 120 steps/min. The results showed that as walking cadence increased, mean peak pressures also increased. The mean peak pressure increased 119% at 120 steps/min compared with 70 steps/min. The authors concluded that the increase in plantar pressures with increasing cadence may be explained by Newton's Second Law: force=mass x acceleration, where the acceleration is the derivative of velocity with respect to time (dV/dt).23
In each of the studies by Zhu and associates,17,23 only young male subjects without known pathologies or impairments that might affect gait were studied. Further studies are needed to assess the effect of shuffling gait pattern on forefoot pressures in elderly people with diabetic neuropathy.
Mueller and associates24 studied the gait characteristics of patients with diabetes and peripheral neuropathies as compared with an age-matched comparison group. Twenty subjects, 10 with diabetes mellitus (2 female, 8 male) and a history of peripheral neuropathies (mean age=58 years, SD=5) and 10 (2 female, 8 male) without diabetes (mean age=57 years, SD=11), were studied. The mean duration of diabetes in the subjects with diabetes mellitus was 20.8 years (SD=6.1). The subjects with diabetes showed less ankle mobility (
=22.1°[SD=5.40°] versus
=30.6° [SD=4.1°]), peak plantar flexor ankle moment (
=1.03 N·m/kg [SD=0.34] versus
=1.36 N·m/kg [SD=0.30]), peak plantar flexor ankle power (
=1.05 W/kg [SD=0.78] versus
=1.95 W/kg [SD=0.71]), walking speed (
=1.06 m/s [SD=0.19] versus
=1.26 m/s [SD=0.19]), and stride length (
=1.20 m [SD=0.23] versus
=1.51 m [SD=0.18]) compared with the age-matched comparison group. Decreased plantar-flexor peak torque (
=49.80 N·m [SD=29.70] versus
=90.20 N·m [SD=11.10]) appeared to diminish the ability of the plantar-flexor muscles to push off and generate plantar-flexor moments or power during terminal stance (ie, at 70%-100% of normalized stance). The authors used multiple regression to support their hypothesis that limited plantar-flexion muscle torque secondary to peripheral neuropathy contributed to the change in walking pattern.24
These results suggest that the subjects with diabetes pulled their legs forward using hip flexor muscles rather than pushing their legs forward using plantar-flexor muscles, as seen in the age-matched comparison group.24 The subjects with diabetes appeared to walk more flat-footed, with minimal push-off into plantar flexion, compared with the age-matched comparison group. The authors24 suggested that emphasizing a hip pull-off pattern for patients with peripheral neuropathies may decrease the anterior-posterior sheer force, place lower pressures under the metatarsal heads, and help to prevent the occurrence of plantar ulcers. Whether the differences in kinematic and kinetic variables between the subjects with diabetes and the comparison subjects were due to walking speed or decreased plantar-flexor muscle weakness in the subjects with diabetes is not clear. The authors24 speculated that reduced plantar-flexor peak torque was the reason for the kinematic and kinetic changes because walking speed did not contribute to the multiple regression analysis when added after plantar-flexor peak torque.
Mueller and associates25 went on to test this hypothesis and determine whether instructing people to walk emphasizing a hip pull-off pattern would reduce forefoot peak plantar pressures and change the kinematics of walking. Seven male subjects with diabetes mellitus and a history of peripheral neuropathies (mean age=57.4 years, SD=15.2) and 6 subjects (1 female, 5 male) without diabetes (mean age=55.3 years, SD=14.9) were evaluated. The mean duration of diabetes in the subjects with diabetes mellitus was 22.1 years (SD=10). The subjects with diabetes and peripheral neuropathies were instructed to decrease their push-off at the ankle, pull their legs forward from their hips, and shorten their steps, but not slow their walking speed. Compared with using the normal ankle push-off pattern, using the hip pull-off pattern showed a 27% decrease in forefoot peak plantar pressures and a 24% increase in heel peak plantar pressures. This 27% reduction in forefoot peak pressures was seen in subjects wearing therapeutic footwear and controlling for speed. Kinematic changes included decreased plantar-flexion angular velocity (from 215°/s to 168°/s), hip extension range of motion (from 12.5° to 9.2°), and step length (from 1.17 m to 1.04 m) and increased dorsiflexion range of motion (from 17.2° to 19.1°) and hip flexion range of motion (from 15.3° to 18.4°), but no change in walking speed. The authors suggested that using a hip pull-off pattern may be useful for patients who wear prescriptive footwear but continue to have ulcers or for patients who are unable or unwilling to wear prescriptive footwear.
The brief training in hip pull-off pattern resulted in an unexpected 24% increase in heel peak plantar pressure, which usually occurred during the period of heel contact.25 Because the heel has a protective fat pad and is seldom the site of ulceration due to repetitive stresses,26 this increase in peak plantar pressure at the heel is not likely to cause ulceration. An additional limitation in the study by Mueller and associates25 was that the hip pull-off pattern (decrease plantar-flexor muscle activity and increase hip flexor muscle activity) was verified only by kinematic changes, without measuring electromyographic activity and kinetic variables (ie, joint moments or power). Further studies are needed to determine whether instructions to patients could be developed that will lead them to reduce the heel pressure or whether this elevated heel pressure is a danger to patients.
Another potential walking pattern that could be used to reduce forefoot plantar pressures is the "step-to" walking pattern. Brown and Mueller27 determined the effect of a step-to walking pattern on forefoot peak plantar pressures. They evaluated 10 subjects without known pathologies or impairments that might affect gait (5 female, 5 male; mean age=24.6 years, SD=4.86) and one male subject (62 years of age) with peripheral neuropathy. Subjects were told to shorten the step on their uninvolved extremity so that the step ended next to and not beyond their involved limb. Gait was supposed to be continued by the subjects stepping with the involved extremity. At the end of each stride, the subjects were momentarily in a position of quiet stance without a forceful push-off on the involved side. Walking speed during the step-through pattern (normal walking) was matched to the speed of the step-to pattern.
Brown and Mueller27 found that the peak plantar pressures of the subjects without peripheral neuropathies decreased an average of 53% on the forefoot but increased an average of 14% on the heel when subjects walked using a step-to gait compared with a step-through gait. The subject with peripheral neuropathy demonstrated an 87% decrease in peak plantar pressures at the forefoot and a 46% increase in peak plantar pressures at the heel when comparing the step-to pattern with the step-through pattern. The authors suggested that a step-to pattern should be considered when patients would benefit from a decrease in pressures on the forefoot.
Limitations of the step-to walking pattern should be considered by therapists and patients before they use this walking pattern to decrease plantar pressures. Unlike normal walking, the step-to walking pattern does not allow for symmetrical, reciprocal movements. The step-to walking pattern is not smooth, because it requires people to stop moving momentarily at the end of each stride. In addition, whether the temporary use of this walking pattern could have adverse musculoskeletal effects is not known.27 Another limitation of the step-to walking pattern is its effect on walking speed. None of the subjects were able to walk at their natural speed when adopting the step-to walking pattern.27 A step-to walking pattern was recommended for patients with unilateral extremity involvement. The usefulness of this walking pattern for the patient with bilateral involvement is unknown. Further research is needed to clarify the benefits and limitations in specific patient populations.
The walking pattern studies have some common limitations. One common limitation is the brief period of gait training. Gait training requires motor learning.28 Human walking is a complex skill in which motor, sensory, and cognitive variables continuously interact to control the large number of anatomical degrees of freedom within the body, as well as the task constraints imposed by the environment.29 Fitts30 stated that people pass through 3 stages when acquiring a new skill. In the first stage, the person gains an understanding of the requirements of the task. In the second stage, specific requirements such as speed, amplitude, and force are refined through large amounts of practice. In the last stage, a motor skill is well established and can be performed automatically or almost automatically. Therefore, some questions remain: (1) How long does it take to completely learn the new walking pattern? and (2) Can a person retain this new walking pattern? Further research is needed to identify the ongoing training people require to change their walking patterns permanently.
Another common limitation of studies examining modified gait is that walking was measured while people walked for a short distance (6-32 m).17,25,27 Zhu and associates17 reported that all subjects without known pathologies or impairments that might affect gait became fatigued more quickly during the shuffling gait. Further study is needed to assess the effects of fatigue with long-term use of shuffling, hip pull-off, and step-to walking patterns in people with diabetic neuropathies.
An additional limitation of the research design of studies involving gait modification is that these studies did not clarify whether the people with diabetic neuropathies can change their gait pattern easily and permanently without sensory feedback from the legs. With intact sensation, the nervous system presumably can adjust to proprioceptive feedback by changing the length of the gait cycle and varying the position of the foot. On the contrary, people with insensitive feet lack the sensory feedback (pain and proprioception) that signals the need to shift their gait pattern, rest, or remove a shoe to allow the traumatized foot to recover. Sensory feedback is important and essential for motor learning.31 Courtemanche and associates32 demonstrated that a deficit of sensory feedback in people with diabetic neuropathies yields a slower and more conservative gait pattern and an increase in attention demands when walking. Further study is needed to clarify that people with diabetic peripheral neuropathies can learn and retain new walking patterns without sensory feedback from the lower extremity.
| Sensory Substitution |
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The gait trainer in the study by Walker and associates33 was composed of 3 parts. The first part was a set of 6 remote sensors that fit into an insole inside the person's shoe. The second component was a data analyzer, a small box that was attached onto a belt at the person's waist. Microchips within this device collected data from the remote sensors and made decisions according to predetermined criteria to decide whether the person should be notified that a step should be terminated. The third component, an auditory cue, was a means of alerting the person that a step should be modified.
Walker and associates33 studied the ability of individuals with and without diabetes and peripheral neuropathies to learn to use this lower-extremity sensory substitution device. Thirty patients with diabetes mellitus and peripheral neuropathies (17 female, 13 male; average age=37.9 years, range=20-64) and 20 individuals without diabetes (10 female, 10 male; average age=38.5 years, range=20-57) were evaluated. The participants were asked to walk on a treadmill at 3 speeds (1, 2, and 2.5 mph) with auditory sensory feedback to cue ground contact time greater than 80% of the duration of the baseline measurement. Each session consisted of a 10-minute walk on a motorized treadmill. The sensory substitution gait trainer was programmed so that it would generate a beeping sound via an earphone when the participant's surface contact time reached 80% of the baseline measurement. The participant was instructed to unload the instrumented foot by a shortened step or unilateral limping as soon as the tone was heard via the earphone. The goal was to rarely or never hear the beeping tone. A beep indicated an error.
The results showed that the errors per minute were decreased when errors were compared during the first and last minutes of each session in subjects with and without diabetes. This finding suggests that people with diabetic neuropathies are able to learn to use the gait trainer to modify their gait during steady ambulation and that the skill acquired in using the device can be retained. However, subjects with diabetes and peripheral neuropathies showed higher error rates for the 1-mph speed rate than subjects without diabetes and peripheral neuropathies (5.17±11.80 versus 1.47±2.20 errors per minute). These results suggest that subjects with diabetes and peripheral neuropathies learned to use the device less quickly than did the control group.
Although Walker and associates33 demonstrated that people with diabetic neuropathies can learn to use a lower-extremity sensory substitution device to change gait, they used surface contact time rather than plantar pressure data to provide auditory feedback. Training aids, such as forefoot plantar sensors that could provide auditory feedback when a certain pressure threshold is reached, may be more beneficial to reduce forefoot peak plantar pressures and to learn walking patterns than a device based on contact time.
Abu-Faraj and associates34 developed a Holter-type, microprocessor-based, portable, in-shoe plantar pressure data acquisition system. This Holter-type device enables long-term and continuous recording (up to 8 hours) of pressure data. The authors demonstrated that the foot pressure sensor was able to tolerate repetitive gait cycles with high sensitivity. Richter and associates35 developed an electronic system in a shoe that monitors temperature, pressure, and humidity, storing the data in a battery-powered device for later uploading to a host computer for data analysis. High temperature and moisture are believed to contribute to skin breakdown.36 The pressure sensors are located at the heel and under 3 metatarsal heads. Temperature sensors are located under 3 metatarsal heads, and 2 sensors are under the heel with the humidity sensor. The authors demonstrated that pressure and temperature sensor data were highly correlated (r>.93) with pressure data obtained with an F-scan and a standard mercury thermometer. Both research groups34,35 indicated that future iterations of the devices could be used to provide sensory feedback to people.
| Using a Cane to Reduce Forefoot Pressures |
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Wertsch and associates38 studied the effect of using a cane in the ipsilateral hand versus contralateral hand when trying to unload pressures on a foot in 9 subjects without known pathologies or impairments that might affect gait. A portable in-shoe pressure system was used to measure plantar pressures at 7 sites under each foot. Subjects decreased loading on the plantar surface of the foot an average of 17% using a cane in the ipsilateral hand and 21.5% using a cane in the contralateral hand compared with walking without a cane. Use of a cane in the contralateral hand resulted in the greatest unloading on the lateral side of the foot (35%), whereas a cane in either hand minimally unloaded the medial side of foot (14%). In addition, pressure increased (21%) on the great toe (9 subjects) and first metatarsal (8 subjects) of the uninvolved foot. The authors suggested that use of a cane in the contralateral hand to unload a neurotrophic ulcer is more likely to be successful for a fifth metatarsal ulcer than for a first metatarsal ulcer and that cane use to unload one foot may put the other foot at risk for ulceration.
The use of crutches enables a person to unload one extremity completely, but using crutches is more difficult and requires more balance than a using cane. For an older or more debilitated population, using crutches may not always be a reasonable option.27 Blount39 suggested that a cane should not be used if the force applied to the cane is more than 20% to 25% of a person's body weight, because the cane is too unstable. Jebsen40 suggested that if more than 20% to 25% of a person's body weight is to be unloaded on the ambulation aid, an aluminum forearm crutch that can support 40% to 50% of body weight will be more effective than a simple cane. The study by Wertsch and associates38 was conducted on subjects without known pathologies or impairments that might affect gait. Further studies are needed to clarify whether using a cane can decrease forefoot plantar pressures in people with diabetic neuropathies.
| Summary |
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One method for reducing forefoot peak plantar pressures is to spread weight-bearing forces over the entire plantar aspect the foot while walking. Physical therapists have used various strategies to reduce peak plantar pressures on the insensitive foot. Although casts, accommodative orthotic devices, and therapeutic footwear have been used to reduce plantar pressures, alteration of the walking pattern also may be useful to decrease forefoot peak plantar pressures in some individuals with diabetic neuropathies.
We reviewed and discussed 3 walking patterns that can be used to reduce the forefoot peak plantar pressures. A shuffling gait pattern can decrease the peak plantar pressures under the first and second metatarsals (up to 57.8%) and the hallux (up to 63.2%). A hip pull-off pattern can decrease the peak plantar pressures at the forefoot (up to 27%), and a step-to walking pattern can decrease the peak plantar pressures at the forefoot (up to 53%). These walking patterns may be useful to help prevent or heal forefoot ulcers in people with diabetic neuropathies who are most at risk for skin breakdown. Therefore, alteration of the walking pattern should be considered for reducing forefoot peak plantar pressures in people with diabetic neuropathies who wear prescriptive footwear and who continue to have ulcers or in people who are unable or unwilling to wear prescriptive footwear and who have newly healed plantar ulcers.
Further studies are needed to determine whether people with diabetic peripheral neuropathies can retain new walking patterns and to determine the long-term effects of altering walking patterns. Further studies also are needed to clarify whether the altered walking patterns cause other adverse musculoskeletal and biomechanical effects on the spine, hip, knee, or ankle joints. In the future, portable, microprocessor-based insole pressure measurement systems may be prescribed by clinicians as a lower-extremity sensory substitution device to cue walking pattern alteration and to assess the effectiveness of altering the walking patterns in people with diabetic neuropathies. Research is needed to determine whether altered walking patterns or sensory substitution can help prevent skin breakdown and subsequent amputation in people with diabetes and peripheral neuropathies.
| Footnotes |
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This work was supported by Grant RO1 36576-01 to Dr Mueller from the National Center for Medical Rehabilitation Research, National Institutes of Health.
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