THE EVALUATION OF GAIT IN NEUROMUSCULAR DISEASE

AANEM WORKSHOP THE EVALUATION OF GAIT IN NEUROMUSCULAR DISEASE James K. Richardson, MD AMERICAN ASSOCIATION OF NEUROMUSCULAR & ELECTRODIAGNOSTIC MEDICINE

Workshop handouts are prepared as background didactic material to complement a hands-on workshop session. This workshop handout was originally prepared in September 2008. The ideas and opinions in this publication are solely those of the author(s) and do not necessarily represent those of the AANEM. Copyright September 2008 AMERICAN ASSOCIATION OF NEUROMUSCULAR & ELECTRODIAGNOSTIC MEDICINE 2621 Superior Drive NW Rochester, MN 55901

The Evaluation of Gait in Neuromuscular Disease James K. Richardson, MD Associate Professor, Department of Physical Medicine and Rehabilitation Co-Director, Electrodiagnostic Laboratory University of Michigan Health Systems Ann Arbor, Michigan INTRODUCTION This manuscript will cover the gait effects of diseases and neuropathic conditions that are directly diagnosed in the electrodiagnostic laboratory. These will include a wide variety of focal neuropathies, diffuse peripheral neuropathy, and proximal weakness. Diseases that are not directly diagnosed in the laboratory, such as upper motor neuron processes (e.g., stroke, cervical myelopathy) or movement disorders (e.g., Parkinson s or ataxias), will not be included. For each diagnosis, alterations in the stance and swing phases of gait, natural substitutions or compensations for these alterations, potential secondary musculoskeletal pain and biomechanical treatment for the gait disorder will be described. Surgical, metabolic and immunologic therapies, which are often quite specific to the underlying diagnosis, will not be addressed. I. General considerations The importance of walking Will he be able to walk? The well-meaning families of patients with diseases or conditions that impair a wide variety of functions thinking, swallowing, speaking, and dressing always want to know if their loved one will walk. Although walking is neither necessary nor, in isolation, sufficient for independent function the question is still apt because walking isassociated with some degree of independence which, in our society, is highly valued. However, more importantly, according to Hippocrates Walking is man s best medicine. Modern research confirms Hippocrates wisdom, and suggests that exercise in the form of walking confers a significant health benefit. Men who walk regularly have reduced overall mortality 13 and women who walk three or more hours per week have a reduction in coronary events similar in magnitude to women who performed more vigorous exercise. 20 Moreover, older women who walk are less likely to demonstrate cognitive decline than more sedentary women 43 and older persons of both genders who walk are less likely to show mobility loss. 42 Relatively modest changes in lifestyle confer a benefit. It is estimated that by walking 30 or more minutes per day and reducing television time to less than 10 hrs/week women can reduce new cases of obesity and diabetes mellitus by 30 and 43%, respectively. 15 Lastly, there is evidence that weightbearing activity may be protective against foot ulcer in persons with DPN.16 Clearly it is in the patient s best interests to continue walking. Moreover, diseases that are commonly diagnosed in the electrodiagnostic laboratory often affect the ability to ambulate. Therefore, increasing the electrodiagnostician knowledge of the gait disorders that often accompany neuromuscular diagnoses is in the patient s best interest.

2 The Evaluation of Gait in Neuromuscular Disease AANEM Workshop Efficiency considerations in normal gait The purpose of walking is to efficiently transport the body s center of mass (CM; located anterior to the superior sacrum in most people) through space. The smaller the movement of the CM in the sagittal (vertical) and frontal (lateral) planes the more efficient the gait. A clinically normal gait is one that is smooth and rhythmic, indicating that the CM has little vertical and lateral motion and what motion does occur does so in a regular fashion. To achieve this efficient, normal gait the stance and swing limbs must accomplish specific tasks which will control the CM and minimize its motion. Stance limb adjustments that allow efficiency: If no adjustments were made and one was to walk with a stiff-legged gait then the CM would be at its zenith during single stance and at its nadir during dual stance. Therefore efficiency is improved by shortening the stance limb via mild hip and knee flexion, which are controlled by, respectively, eccentric contractions of the hip and knee extensors. In addition the CM is allowed to lower still further during stance by allowing the swing hemipelvis to gently drop; this causes a relative adduction at the hip which is controlled eccentrically by the stance hip abductors. Swing limb adjustments that allow efficiency: During swing phase the extremity must shorten so that it can swing forward freely. This is accomplished by a combination of ankle dorsiflexion, knee and hip flexion, and an eccentric contralateral hip abductor contraction which prevents excessive drop of the unsupported hemi-pelvis. Of these four mechanisms the last is the most important. 2 Dual stance adjustments that allow efficiency: During dual stance, when both feet are in contact with the ground, the lower extremities need to elongate to prevent excessive drop of the CM. In the trailing limb this is accomplished by plantar flexion at the ankle, knee extension and pelvic rotation. The last occurs as the hemi-pelvis on the side of the leading limb rotates forward causing a relative internal rotation of the trailing femur on the pelvis. In the leading limb elongation is accomplished by dorsiflexion at the ankle, extension at the knee, and pelvic rotation which causes a relative external of the leading femur on the pelvis. Control considerations in normal gait Control of the CM. Most falls occur during ambulation. 4,6,8 Controlling the CM is the key to safe ambulation. If the CM migrates too far outside of the anatomic base(s) of support then the patient will fall without executing a quick, accurate rescue step. The CM is controlled by the ground reaction force (GRF); i.e., the force the ground exerts onto the plantar aspect of the foot. The GRF is manipulated by joint torques so as to control the CM. The relationship between the CM and the GRF can be likened to that between a flock of sheep atop a small plateau with steep sides (the base of support) and a guardian sheepdog. When the sheep (CM) drift too close to the side of the plateau the sheep dog (GRF) must run rapidly so as to position herself between the sheep and peril. Similarly if the reader stands up and allows the trunk (CM/sheep) to drift anteriorly s/he will perceive contraction of the plantar flexors, which drives the sheepdog/grf anteriorly. If the ground reaction force can move anteriorly in front of the CM quickly enough then balance will be restored. If not then the reader must take a forward step which, again, moves the GRF anteriorly, or fall (Please don t!). CM control in the sagittal plane: Control of the CM in the sagittal plane is accomplished primarily by ankle plantar flexors/dorsiflexors, knee flexors/extensors and hip extensors/ flexors. Each of these three levels of control is powerful. For this reason and others (such as the availability of both upper limbs to break and arrest falls) sagittal plane stability is relatively minor clinical concern. CM control in the frontal plane: Frontal plane control is accomplished during stance by muscular manipulation at the subtalar and hip joints through, respectively, ankle inversion/eversion and thigh adduction/abduction. In contrast to the situation for sagittal plane control, there only two levels of control and these are relatively less powerful than the muscles involved in sagittal plane control. This problem is compounded by the fact that only one upper limb is available to break and arrest a lateral fall. As a result lateral falls during ambulation have been found to produce a high level of injury and are a major clinical concern. 11 The role of time: Time is critical given that humans have a little over half a second to arrest a fall after displacement of the CM has occurred. Therefore the CM is best controlled through rapid manipulation of the GRF by means of rapidly generated joint torques. The inability to produce torque rapidly is common in patients with neuromuscular disease. For example patients with even mild diabetic neuropathy have near normal ankle strength, but markedly decreased ankle rate of torque generation which correlates strongly with stability during unipedal stance. 12 (Figure 1) Similarly, rate of lower extremity torque generation differentiated between older persons who did, and did not, successfully recover from a trip. 21 General evaluation. Patients coming to the electrodiagnostic laboratory rarely have gait disorder as their primary concern. Moreover, the electrodiagnostician has many tasks to perform and so evaluation of gait cannot be in depth. However, a brief screen can be rewarding.

AANEM Workshop The Evaluation of Gait in Neuromuscular Disease 3 III. Neuropathic gait RTD (Nm/s) 200 150 100 50 0 RTD = 150.8-158.0 e -UPS/3.72 R 2 = 0.575 0 10 20 30 40 Unipedal Stance (s) OF PN Fit Figure 1 The relationship between ankle rate of torque generation (RTD, in Newton-meters/second) and unipedal balance time in seconds in a group of 12 older diabetic women, 6 of whom have neuropathy. Ask about falls. When a patient gives a history of falls, or near-falls, the physicians knows that the patient is having difficulty controlling the CM. Falls often occur in association with some kind of perturbation, such as a surface irregularity. Although it is tempting to dismiss the importance of such a fall, it should be understood that we all encounter such irregularities daily and the inability to navigate them is likely of clinical relevance. Watch the patient walk. It does not take great expertise to discern whether a patient has gait asymmetry, or excessive motion. The clinician should watch the pelvis and shoulders when making these determinations. Asymmetric or excess motions indicate an inefficient gait as both are associated with excessive movement of the CM. When the gait is asymmetric there is likely a lateralizing diagnosis. When there is symmetric excessive motion then a bilateral problem, such as proximal weakness, is more likely. Following these observations the usual neuromuscular examination performed prior to electrodiagnostic testing takes on greater meaning. Special attention should be paid to muscles that are involved in frontal plane control such as the ankle invertors and evertors and hip abductors. II. Gait abnormalities associated with specific electrophysiologic diagnoses. Table 1 lists deficiencies in stance and swing limb function, typical compensations, resulting musculoskeletal disorders and biomechanical treatments for specific lower extremity mononeuropathies, proximal weakness and diffuse peripheral neuropathy. A mild diffuse peripheral neuropathy, associated with diabetes or some other condition, is one of the commonest diagnoses made in the electrodiagnostic laboratory. In addition, neuropathic gait has been studied and evidence-based recommendations can be made. Neuropathy leads to balance impairment and markedly increases fall risk. Neuropathy often subtly, but always significantly, impairs balance. (Table 2) With regard to static balance such as quiet standing (which is not truly static given that the center of mass rotates about the ankle in the manner of an inverted pendulum) neuropathic subjects show increased center of pressure excursions as compared to controls, 40,35 and these excursions correlate with peripheral nerve conduction studies. 41 Neuropathy also impairs transition from bipedal to unipedal balance whether on command or subject controlled. 27 Neuropathic subjects show greater difficulty recovering from perturbations in the forms of a tilting support surface or being released following a lateral lean. 3,12 Cavanagh et al. 6 found that young adults with neuropathy were 15 times more likely to be injured while walking than a control group, and Sorock and Labiner 37 confirmed prospec- Table 2 The effect of neuropathy on measures of balance Balance Task PN subjects Control Significance Bipedal Stance Force platform Eyes open: 350 + 20* p < 0.05 measured center 550 + 50* 600 + 50* p < 0.01 of pressure excur- Eyes closed: sion ( in cm)40 1100 + 100* Center of pressure Eyes open: 20 + 8* p < 0.01 excursion (in cm)35 35 + 12* 30 + 10* p < 0.01 Unipedal Stance Eyes closed: 55 + 18* Balancing 3 seconds 0.12 0.58 P = 0.021 on command (success rate) 27 Subject controlled 3.8 + 3.5 32.2 + 17.7 P = <0.001 (sec) 27 Perturbed Unipedal Stance Success rate Eyes open: 0.47 0.75 P = 0.036 recovering from a tilting surface 3 Eyes closed: 0.02 0.21 Lateral Leans Subjects recovering 5% lean, 0/6 5% lean, 3/6 P = 0.068 successfully for 10% lean, 0/6 10% lean, 1/6 a given % foot width 12

4 The Evaluation of Gait in Neuromuscular Disease AANEM Workshop tively that neuropathy increased fall risk in a cohort of older persons living in senior housing. Similarly, in two separate studies we found that older persons with neuropathy were 23 and 17 times more likely to fall than age and gender-matched controls. 28,29 Resnick et al. 24 demonstrated that PN, rather than the presence of diabetes, is responsible for lower extremity dysfunction among older persons with diabetes mellitus. Most falls in older persons with 8 and without 4 neuropathy occur during ambulation, especially on irregular surfaces. Table 1 Diagnosis Swing changes/fall risk Swing Substitution/Compensation Stance changes/ fall risk Stance Substitution/ Compensation Deep Peroneal Foot drop makes swing a) Increased ipsilateral hip and Early stance: foot slap Stance: Hip/trunk flexion Mononeuroapthy limb too long Trips knee flexion. (steppage) Mid-stance: decreased recovery b) External rotation at hip from a posterior perturbation c) Circumduct Superficial Peroneal Minimal Not needed Mid-stance: decreased recovery Stance: Early placement of swing Mononeuropathy from a medial perturbation (low limb on the ground clinical relevance as swing limb used) Common Peroneal As above As above As above Mononeuropathy Tibial Mononeuro- Minimal Not needed Early/Mid stance: decreased recognition Stance: Plantar flexors pathy at ankle of location of GRF Late stance: decreased foot stiffness Tibial Mononeuro- Minimal Not needed As above, and decreased propulsion To control anterior perturbations: pathy at knee in mid/late stance Decreased resistance Hamstrings to stabilize anterior to anterior perturbation/trip progression of knee, Sciatic mononeuro- Foot drop As above for common Decreased recovery from perturbation To control lateral perturbation, pathy Loss of control during peroneal mononeuropathy in all directions. Decreased recognition medial trunk flexion, hip abduction terminal swing of GRF Decreased propulsion and then crossover step. Control of anterior perturbations as above Femoral mononeuro Decreased initiation of swing Gluteus medius to assist in Full knee extension during stance Gastroc/soleus to stabilize knee. -pathy swing initiation so leg too long. Decreased Trunk flexion with posterior propulsion and recovery from perturbation, then back step. posterior perturbation Obturator mono- Slight abduction or Swing: More lateral placement Minimal neuropathy circumduction of swing limb Inferior gluteal Minimal Not needed Increased trunk extension. Decreased Stance: Trunk extensors and plantar. mononeuropathy recovery from anterior perturbation flexors The latter gives extensor lurch Superior gluteal Contralateral limb too long Increased contralateral ankle dorsi- Stance hip adduction causes swing hip drop Lateral trunk shift. With lateral or medial mononeuropathy during its swing phase flexion and/or knee/hip flexion Decreased recovery from medial perturbation, ankle inversion or eversion and lateral perturbation and crossover or lateral step Radiculopathy As above, but motor and As above, but motor and sensory or /plexopathy sensory deficits usually deficits usually less complete less complete Proximal weakness Difficulty initiating and Swing: Trunk rotation to initiate, Decreased stability of knee and hip Stance: Plantar flex at ankles to stabilize (myopathic processes, maintaining swing external rotation and lateral trunk joints, with decreased recovery knees, hyperlordotic posture to stabilize defects in neuromuscular flexion away from swing limb from all perturbations. knees and A-P hip, lateral trunk sway transmission, etc.) to maintain swing to stabilize M-L hip Diffuse peripheral If severe, foot drop If foot drop, as per peroneal Diminished detection of GRF over If surface firm, flat and familiar and neuropathy (due mononeuropathy above. entire plantar aspect of foot. the lighting is good, the patient is not to diabetes and Decreased recovery from distracted and has good vision, OK. other causes) all perturbations For all other situations, upper extremity For all other situations, upper extremity touch recommended.

AANEM Workshop The Evaluation of Gait in Neuromuscular Disease 5 Neuropathy causes afferent and efferent impairments at the ankle. The ankle is the most distal joint with a significant influence on posture and, as would be expected, is the joint whose function is most impaired by the typical length dependent neuropathy. Table 3 summarizes some of the studies that have identified functionally significant sensory and motor impairments among older persons with PN. Ankle proprioceptive thresholds are increased (worse) in the frontal and sagittal planes among DPN subjects as compared to controls. 34,39 Similarly, maximal motor function is decreased in both planes at the ankle in subjects with DPN as compared to controls. 1,12 Secondary Pain Plantar fasciitis, stress fracture, gluteal myofascial pain and sacroiliac pain (depending on compensation strategy Ankle sprain/inversion injury Plantar fasciitis As above Plantar fasciitis Stress fractures Metatarsalgia Plantar fasciitis, stress fractures metatarsalgia, subtalar joint pain As above Biomechanical Treatment AFO trimmed posterior to malleoli, high-top shoes, Stretch plantar flexors Ankle orthosis with medial/lateral support especially on irregular surfaces AFO trimmed anterior to lateral malleolus or high-top shoes with medial/lateral support Foot orthosis to stiffen foot proximal to met heads Foot orthosis and rocker/roller sole to facilitate heel lift in late stance AFO, padded with good arch support, trimmed anterior to malleoli. Consider adding roller or rocker sole. Table 3 Functionally significant sensory and motor impairments associated with neuropathy. Impairment PN Subjects Control Subjects Significance Sensory Ankle proprioceptive Dorsi/plantar flexion, 4.6 + 4.5 1.4 + 0.7 p < 0.01 thresholds (degrees) 35,39 Inversion, 1.30 + 1.06 0.21 + 0.19 p = 0.048 Eversion, 2.57 + 2.90 0.39 + 0.10 p = 0.036 Motor Maximal isokinetic Dorsiflexion, 24.3 + 6.8 30.7 + 7.5 p < 0.0001 strength (open chain, Plantarflexion, 87.8 + 23.2 111.0 + 28.7 p < 0.01 N-m) 1 Peak acceleration Dorsiflexion, 4765 + 1681 6343 + 1524 p < 0.001 (open chain, m/sec2) 1 Plantarflexion, 5737 + 1977 7601 + 1825 p < 0.001 Knee extension, 4737 + 1820 5899 + 2013 p < 0.05 Rate of torque Ankle inversion, 78.2 + 50.8 152.7 + 54.6 p = 0.016 development (closed chain, N-m/sec) 12 Ipsilateral knee pain (joint)? Ground reaction AFO, contralateral Ipsilateral lateral hip pain shoe lift, contralateral cane, constant (soft tissue) vigilance, PT for stairs and ramps Minimal Usually not needed. Lumbar facet and sacroiliac pain Contralateral cane placed anteriorly during stance Lumbar facet and sacroiliac with Cane contralateral hand with 10:1 lateral trunk shift or lateral hip return on cane force placed on palm pain with contralateral hip drop Plantar fasciitis, stress fractures, Environmental modification and AD knee joint pain, lateral hip pain, if upper extremities strong enough lumbar facet and sacroiliac pain. to benefit. Education. Powered Acute injuries common with falls. mobility for distance and irregular surface. Check bone density. Metatarsalgia, plantar fasciitis, Vision, patient education, upper stress fractures extremity touch (cane, wall, SO, railings, etc.) and ankle orthoses for irregular surfaces without available touch. Strengthen proximal hip and trunk muscles. The neuropathy-associated afferent and efferent impairments shrink the foot. When a human is attempting to maintain postural equilibrium during unipedal stance, for example when putting on trousers, the body s CM wavers above the anatomic base of support, the foot. As discussed earlier, the task of the ankle and foot is to activate the proper muscles so as to position the GRF between the CM and the edge of the base of support. Using the sheep/sheepdog analogy once again, when the sheep (CM) drift too close to the side of the plateau (the edge of the base of support) the sheep dog (GRF) must run rapidly so as to position herself between the sheep and peril. Therefore the area of the plateau available to the sheep for wandering is a function of the speed of the sheepdog (GRF). If the sheepdog is slow then the sheep will be lost if they wander too far from the middle of the plateau; however, if the sheepdog is quick then the sheep will be allowed to graze over the majority of the plateau without risk of being lost. Healthy persons, who have the ability to rapidly generate ankle torque and an accurate sense of the GRF location, have big feet; i.e., the center of mass may be maintained above the majority of the plantar aspect of the foot. In contrast the neuropathic patient, with diminished ankle torque generation and a coarsened sense of the GRF loca-

6 The Evaluation of Gait in Neuromuscular Disease AANEM Workshop tion, must maintain the center of mass over a small portion of the plantar aspect of the foot giving such patients small feet. The Walking on small feet leads to falls and increased gait variability. Falls. Small feet, due to neuropathic impairments, lead to a system (patient) that is not robust to perturbations. As a consequence patients with neuropathy, as discussed previously, have a markedly increased rate of falls and injury due to falls. Moreover, clinical experience and the only prospective study of falls exclusively in neuropathic patients 8 indicate that they almost invariably fall as the result of a surface irregularity. Increased gait variability. Gait variability is increasingly recognized as a quantifiable sign of dynamic disequilibrium; i.e., is a sign that the system (the patient) is not robust to perturbation. (The reader is directed to excellent works by Jeffrey M. Haursdorff, PhD and colleagues that found increased gait variability, both temporally and spatially, to be associated with mobility function, falls and a variety of diseases.) Although the precise biomechanical advantage, or necessity, of increased gait variability has not been definitively identified it seems likely that when a patient who is not robust to perturbations during single limb stance is challenged they will rapidly place the swing limb onto the ground. Rapid, urgent placement of the swing limb in response to perceived instability likely occurs in an intermittent fashion, both temporally and spatially, and in aggregate leads to measurably increased gait variability, particularly on an irregular surface. 25 Recognizing functionally significant neuropathy Unipedal balance time, neuropathy severity, body mass index and observation are the best tools for recognizing functionally significant neuropathy defined as neuropathy that leads to multiple and injurious falls. If a patient achieves greater than 10 seconds unipedal balance time on any of 3 trials then it is likely that fall risk is minimally increased, whereas the inability to achieve even 3 to 4 seconds is concerning. 26 The author has observed that the presence of rapid, visible ankle and foot adjustments during attempted unipedal balance is a sign that the patient may not have functionally significant neuropathy in spite of poor balance time (and usually indicates that with practice the patient will improve), whereas the absence of these quick adjustments strongly suggests the patient does not perceive their GRF movement or lack the strength to respond to it. Step width variability can be qualitatively evaluated by watching the patient walk down a long hallway. Although patients with mild to moderate neuropathy appear stable, careful attention to step width will often reveal a wavering, inconsistent step width or frank crossover steps, signs that the neuropathy is likely to reduce dynamic equilibrium and increase fall risk. Neuropathy severity and body mass index also seem to play a role, with a Michigan Diabetes Neuropathy Score 9 > 20 (on a 46 point scale) and a body mass index > 33 appearing to increase risk for multiple and injurious falls. Interestingly these findings appear to have some gender specificity: decreased unipedal balance time and neuropathy severity predominantly influence men, and increased body mass index disproportionately influences women. 26 The clinical management of neuropathic gait Patient and family education: Because of its insidious onset, and the fact that patients often appear to walk reasonably well under ideal conditions, underestimation of the impact of neuropathy is common by patient and physician alike. The patient and family should be made to understand that the patient has lost a special sense that is likely of greater importance than vision in the maintenance of balance. 10 They should be told that the rapid generation of strength in the lower extremities, necessary to prevent a fall in the approximately 500 msec available, is lost. They should be given information regarding the considerable concentration necessary for a person with neuropathy to walk. 7 Distractions should therefore be avoided while the family member is ambulating. In general the patient and family should understand that if the walking surface is firm, flat and familiar, the lighting good and there are no distractions then the patient is probably safe. In all other circumstances the patient should employ upper extremity touch of a wall, cane or other person or use ankle orthoses (described below). Environmental modification: Reliable and convenient support surfaces for upper extremity touch (which markedly increases robustness to perturbations), should be made available in the patient s home, especially near stairs or other irregular surfaces. These need not be obvious fixtures such as grab bars but can be portions of furniture such as desk tops and sofa arms. Specific advice given by a visiting physical and/or occuational therapist can be valuable. Optimize vision: Patients with PN should not use bifocals, even those with transitional lenses, as they have been found to be an independent predictor of falls. 17 This effect, identified in an unselected group of older persons living in the community, is likely even more important to neuropathic patients who are heavily reliant upon vision. Therefore it is recommended that patients have reading and walking glasses that are used separately. Physical training: We randomized 20 older subjects with neuropathy to a 3 week balance and ankle strengthening program or a 3 week sham exercise program. 30 The subjects who performed the intervention program showed significant improvements in unipedal balance time, functional reach and tandem stance. The trial was small and single blind so firm

AANEM Workshop The Evaluation of Gait in Neuromuscular Disease 7 conclusions cannot be drawn. However, the exercises were tolerated well and so are reasonable to consider. In addition, strengthening of the hip abductor/adductor groups and trunk musculature is intuitively appealing as techniques that may minimize excessive lateral trunk shift during gait. The author has seen clinical improvement in the gait of patients with neuropathy who have followed such programs. Finally, in a secondary analysis of gait data previously obtained 33 we found that active ankle frontal plane range of motion (ankle inversion/eversion) was a significant predictor of step width variability during neuropathic gait on a smooth surface. 5 Multivariate analysis showed that this effect was independent of neuropathy severity and other variables. Therefore, although cause and effect were not confirmed by this work, the data suggest that increasing ankle eversion and inversion range of motion may allow improved frontal plane control during neuropathic gait. Finally, strengthening of the upper extremities so that 25 to 30% of body weight can be supported on a cane may be beneficial for reasons described below. External devices: We have studied a cane in two separate protocols and found that it appears to improve balance on both occasions. In the first a cane was found to markedly improve the ability of older neuropathic subjects to maintain unipedal balance for 3 seconds when challenged with an inverting or everting perturbation. 3 Two findings were of clear clinical significance: 1) subjects performed equally well whether the perturbation was toward or away from the cane; 2 ) Up to 25 to 30% of patient body weight was placed on the cane during this simulated emergent recovery of balance. In a separate study 43 older neuropathic subjects underwent gait analysis on an irregular surface in low light conditions with and without three interventions: a cane, ankle orthoses and touch of a vertical surface. 33 The interventions were chosen to improve frontal plane control given the injury potential of lateral falls. Step width variability and step time variability were chosen as outcomes given work supporting the former as a marker of dynamic frontal plane control, 18 and the association between the latter and falls. 14 Each of the three interventions significantly decreased step width and step time variability, as compared to the baseline condition, and did so after the subject was given just 5 minutes of practice with each intervention. It seems likely that the interventions made the subjects more robust to perturbations during single stance which, in turn, allowed for a more controlled placement of the swing limb. Accentuating plantar surface sensation: Older persons with decreased plantar sensation demonstrated more rapid responses to frontal plane perturbations when standing on small (1 mm) ball bearings. 19 In addition, a similar group of patients showed diminished standing sway when insoles provided vibratory noise to the plantar surface of the feet. 22 The effect of these interventions on the gait of patients with neuropathy under standard and challenging conditions is not yet known. REFERENCES 1. Andersen H, Poulsen PL, Mogensen CE, Jakobsen J. Isokinetic muscle strength in long-term IDDM patients in relation to diabetic complications. Diabetes 1996;45(4):440-445. 2. Anderson FC and Pandy MG. Dynamic optimization of human walking. J Biomech Eng 2001;123:381-390. 3. Ashton-Miller JA, Yeh MWL, Richardson JK, Galloway T. A cane reduces loss of balance in patients with peripheral neuropathy: results from a challenging unipedal balance test. Arch Phys Med Rehabil 1996;77(5):446-452. 4. Berg WP, Alessio HM, Mills EM, Tong C. Circumstances and consequences of falls in independent community-dwelling older adults. Age and Aging 1997;6:261-8. 5. Carter SE, Thies SB, DeMott T, Ashton-Miller JA, Richardson JK. (abs.) The relationship between frontal plane ankle range of motion and step width variability in older persons with peripheral neuropathy. American Academy of Physical Medicine and Rehabilitation. Honolulu, Hawaii, November 9 12, 2006. 6. Cavanagh PR, Derr JA, Ulbrecht JS, Maser RE, Orchard TJ. Problems with gait and posture in neuropathic patients with insulindependent diabetes mellitus. Diabetes Med 1992;9:469-474. 7. Courtemanche R, Teasdale N, Boucher P, Fleury M, Lajoi Y, Bard C. Gait problems in diabetic neourpathic patients. Arch Phys Med Rehabil 1996;77:849-55. 8. DeMott TK. Richardson JK. Thies SB. Ashton-Miller JA. Falls and gait characteristics among older persons with peripheral neuropathy. Am J Phys Med & Rehabil 2007;86(2):125-32. 9. Feldman EL, Stevens MJ, Thomas PK, Brown MB, Canal N, Greene DA. A practical two-step quantitative clinical and electrophysiological assessment for the diagnosis and staging of diabetic neuropathy. Diabetes Care 1994;17(11):1281-1289. 10. Fitzpatrick R, McCloskey DI. Proprioceptive, visual and vestibular thresholds for the perception of sway during standing in humans. J Physiol 1994;478(Pt 1):173-86. 11. Greenspan SL, Meyers ER, Maitland LA, Resnick NJ, Hayes WC. Fall severity and bone mineral density as risk factors for hip fracture in ambulatory elderly. JAMA 1994;271(2):128-33. 12. Gutierrez MS, Helber MB, Dealva D, Ashton-Miller, Richardson JK. Mild diabetic neuropathy affects ankle motor function. Clin Biomech 2001;16(6):522-528. 13. Hakim AA, Petrovitch H, Burchfiel CM, Ross GW, Rodriguez BL, White LR, Yano K, Curb JD, Abbott RD. Effects of walking on mortality among nonsmoking retired men. N Engl J Med 1998;338(2):94-99. 14. Hausdorff JM, Rios DA, Edelberg HK. Gait variability and fall risk in community-living older adults: a 1-year prospective study. Arch Phys Med Rehabil 2001;82(8):1050-56. 15. Hu FB, Li TY, Colditz GA, Willett WC, Manson JE. Television watching and other sedentary behaviors in relation to risk of obesity and type 2 diabetes mellitus in women. JAMA 2003;289(14):1785-1791. 16. LeMaster JW, Reiber GE, Smith DG, Heagerty PJ, Wallace C. Daily weight-bearing activity does not increase the risk of diabetic foot ulcers. Med Sci Sports Exerc 2003;35(7):1093-99. 17. Lord SR, Dayhew J, Howland A. Multifocal glasses impair edgecontrast sensitivity and depth perception and increase the risk of falls in older people. J Am Geriatr Soc 2002;50(11):1760-66.

AAEM 8 Course The Medical-Legal Evaluation Issues of Gait in in Electrodiagnostic Neuromuscular Medicine Disease AANEM Workshop 8 18. MacKinnon CD, Winter DA. Control of whole body balance in the frontal plane during human walking. J Biomech 1993;26(6):633-44. 19. Maki BE, McIlroy WE. Postural control in the older adult. Clin Geriatr Med, Studenski S, Ed. 199;12(4):635-58. 20. Manson JE, Hu FB, Rich-Edwards JW, Colditz GA, Stampfer MJ, Willett WC, Speizer FE, Hennekens CH. A prospective study of walking as compared with vigorous exercise in the prevention of coronary heart disease in women. N Engl J Med 1999;341(9):650-658. 21. Pijnappels M. Bobbert MF. van Dieen JH. Push-off reactions in recovery after tripping discriminate young subjects, older non-fallers and older fallers. Gait & Posture 2004;21(4):388-94. 22. Priplata AA, Niemi JB, Harry JD, Lipsitz LA, Collins JJ. Vibrating insoles and balance control in elderly people. Lancet 2003;362(9390):2003-04. 23. Reeves NP, Narenda KS, Cholewicki J. Spine stability: the six blind men and the elephant. Clin Biomech 2007;22:266-74. 24. Resnick HE, Vinik AI, Schwartz AV, Leveille SG, Brancati FL, Balfour J, Guralnik JM. Independent effects of peripheral nerve dysfunction on lower-extremity physical function in old age. Diabetes Care 2000;23:1642-7. 25. Richardson JK, Thies SB, Ashton-Miller JA. An exploration of step time variability on smooth and irregular surfaces in older persons with neuropathy. Clinical Biomechanics 2008;23(3):349-56. 26. Richardson JK. Factors associated with falls in older patients with diffuse polyneuropathy. J Amer Geriatr Soc 2002(11);50:1767-73. 27. Richardson JK, Ashton-Miller JA, Lee SG, Jacobs K. Moderate peripheral neuropathy impairs weight transfer and unipedal balance in the elderly. Arch Phys Med Rehabil 1996;77:1152-1156. 28. Richardson JK, Ching C, Hurvitz EA. The relationship between electromyographically documented peripheral neuropathy and falls. J Am Geriatr Soc 1992;40:1008-1012. 29. Richardson JK, Hurvitz EA. Peripheral neuropathy: a true risk factor for falls. J Gerontol: Med Sci 1995;50A(4):M211-215. 30. Richardson JK, Sandman D, Vela S: A focused exercise regimen improves clinical measures of balance in patients with peripheral neuropathy. Arch Phys Med Rehabil 2001;82(2):205-9. 31. Richardson JK, Thies SB, DeMott TK, Ashton-Miller JA. A comparison of gait characteristics between older women with and without peripheral neuropathy in standard and challenging environments. J Amer Geriatr Soc 2004;52:1532-37. 32. Richardson JK, Thies SB, DeMott TK, Ashton-Miller JA. Gait analysis in a challenging environment differentiates between fallers and non-fallers among older patients with peripheral neuropathy. Arch Phys Med Rehabil 2005;86(8):1539-44. 33. Richardson JK, Thies S, DeMott T, Ashton-Miller JA. Interventions improve gait regularity in patients with peripheral neuropathy while walking on an irregular surface under low light. J Am Geriatr Soc 2004;52(4):510-15. 34. Simoneau GG, Derr JA, Ulbrecht JS, Becker MB, Cavanagh PR. Diabetic sensory neuropathy effect on ankle joint movement perception. Arch Phys Med Rehabil 1996;77(5):453-460. 35. Simoneau GG, Ulbrecht JS, Derr JA, Becker MB, Cavanagh PR. Postural instability in patients with diabetic sensory neuropathy. Diabetes Care 1994;17(12):1411-1421. 36. Son J. Unipedal balance: biomechanical analyses of the effects of age and disease. PhD Dissertation, University of Michigan, Department of Mechanical Engineering, 2006. 37. Sorock GS and Labiner DM. Peripheral neuromuscular dysfunction and falls in an elderly cohort. Am J Epidemiol 1992:136:584-91. 38. Thies SB, Richardson JK, Demott T, Ashton-Miller JA: Influence of an irregular surface and low light on the step variability of patients with peripheral neuropathy during level gait. Gait & Posture 2005;40-45. 39. van den Bosch C, Gilsing MG, Lee SG, Richardson JK, Ashton- Miller JA. Peripheral neuropathy effect on ankle inversion and eversion detection thresholds. Arch Phys Med Rehabil 1995;76:850-856. 40. Uccioli L, Giacomini PG, Monticone G, Magrini A, Durola L, Bruno E, Parisi L, Di Girolamo S, Menzinger G. Body sway in diabetic neuropathy. Diabetes Care 1995;18(3):339-344. 41. Uccioli L, Gicomini PG, Pasqualetti P, DiGirolamo S, Ferrigno P, Monticone G, Bruno E, Boccasena P, Magrini A, Parisi L, Menzinger G, Rossini PM. Contribution of central neuropathy to postural instability in IDDM patients with peripheral neuropathy. Diabetes Care 1997;20:929-934. 42. Visser M, Simonsick EM, Colbert LH, Brach J, Rubin SM, Kritchevsky SB, et al. Type and intensity of activity and risk of mobility limitation: the mediating role of muscle parameters. J Am Geriatr Soc 2005;53:762-70. 43. Yaffe K, Barnes D, Nevitt M, Lui LY, Covinsky K. A prospective study of physical activity and cognitive decline in elderly women: women who walk. Arch of Internal Med 2001;161(14):1703-1708.

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