Gait Disorders -Evaluation and Management

Systems Approach to Gait Rehabilitation 325 co-ordination. This is done at a lower energy expenditure and with no deleterious effects on gait quality. C. Intensity: The Key for Improved Speed and Endurance Based on the task-specificity paradigm and on sports physiology principles, new speed-intensive training programs started to emerge and were tested in the stroke subject population. Sullivan et al. (44), in a group of chronic stroke subjects having mild to severe gait disabilities, studied the effect of a 4-week high-speed training program. Subjects were trained on a treadmill at a preset fast speed of 0.89 m/sec. The fast-speed training group was compared to a group trained at slow (0.22 m/sec) and variable (0.22–0.89 m/sec) speeds. The subjects were walking with partial BWS, which was gradually reduced as their walking capacity improved. After 4 weeks, the fast-speed training group showed the largest improvement in overground self-selected walking speed (D ¼ 0.15 m/sec), as compared to the slow (D ¼ 0.06 m/sec) and the variable (D ¼ 0.07 m/sec) training groups. The gains in speed were also retained at 3-months’ follow-up. It is worth noting that even severely disabled subjects improved and could handle the fast-training program when provided with the necessary help (BWS and manual assis- tance). In a cohort of 60 stroke subjects, Pohl et al. (43) compared the effec- tiveness of a 4-week structured speed-dependent treadmill training to that of limited progressive treadmill training and conventional gait therapy. In the speed-dependent group, subjects were required to walk at maximal speed for preset intervals. Treadmill belt speed was thereafter increased by steps of 10% upon successful completion of each walking trial. The speed-depen- dent group scored significantly higher than the other two groups in over- ground walking speed and Functional Ambulation Category scores. In fact, the speed-dependent group increased their overground fast walking speed by 1.0 m/sec (from 0.61 to 1.63 m/sec), as compared to a gain of 0.31 and 0.56 m/sec for the limited progressive and the conventional gait therapy groups, respectively. A pilot study was carried out by Dean et al. (25) to examine the efficacy of a 4-week task-related circuit-training program in a group of chronic stroke subjects (n ¼ 12). The task-circuit consisted of an exercise class with 10 workstations incorporating locomotor-related activities such as side stepping, sit-to-walk, and walking over obstacles, as well as walking races and relays. As compared to the control group, who practiced upper limb tasks, the circuit-training group demonstrated improvements in walk- ing speed, endurance, force production through the affected limb and the ability to balance on the affected limb. The effects were retained at the 2-months’ follow-up. Once again, despite the variability of functional abil- ities among the subjects, they all showed improvements. This pilot study provides evidence for the use of class exercises incorporating task-circuit

326 Lamontagne and Fung training to improve locomotor function after stroke. Such a training para- digm based on task-specificity also incorporates the principles of intensity, repetition, graded task complexity, and flexibility. It provides the patient with a motivating environment with meaningful tasks and teamwork with other patients. Training protocols that specifically target aerobic capacity were also developed and tested in chronic hemiparetic subjects (45,46,92). In contrast to the speed-intensive programs, the aerobic training programs usually involve longer durations of training, such as weekly sessions over 6 months, and require the subjects to walk or exercise within 50–60% of heart rate reserve. Such protocols, although time consuming, yielded very positive results, increasing aerobic capacity, lowering energy cost of walking and increasing workload capacity (45,46,92). Fatigue is reported by 68% of stroke subjects and is perceived as one of the worst of their symptoms that also impacts negatively on functional abilities (99). One may thus suspect that aerobic training most likely enhances functional abilities and quality of life (46), although this has not been formerly studied. How subjects with a recent stroke respond to aerobic training and how such training can be incorporated within rehabilitation programs that are under pressure to be shortened is yet to be determined. A good alternative may be to provide the subjects with outpatient services through the format of class exercises, as in Dean et al. (25). In summary, gait speed and endurance can improve markedly beyond expectations in stroke subjects, when provided with speed-specific or inten- sity-specific training. Within the present review, little if no deterioration in walking quality could be observed with fast walking. Due to proper screen- ing of the patients and monitoring of cardiac function during the intensive training protocols (43,44,46,92), no inadvertent cardiopulmonary events were induced, indicating that such training programs can be administered safely. Risks of falls must also be minimized by providing the required assis- tance and/or supervision throughout the training sessions. Faster walking speed and greater endurance may induce the most important changes in the patient’s daily life, allowing the patient, for instance, to cross the street within the required time, or to participate in community activities. V. SENSORY CUES AND BALANCE ADJUSTMENT DURING LOCOMOTION A. Balance Control During Locomotion Functional locomotion involves not only moving from one place to another but also treading on changing and uneven terrains without falling. Thus, appropriate motor strategies must be executed by the CNS, based on the sensory information gathered from the visual, vestibular, and

Systems Approach to Gait Rehabilitation 327 somatosensory systems, to counteract unexpected surface changes during locomotion. Locomotion is often challenged under unpredictable situations in daily activities. The CNS must adapt the locomotor pattern to the envir- onmental changes so that locomotion continues and equilibrium is main- tained. Such adaptation requires supraspinal control of goal-directed behavior (100,101). Uneven weight bearing is a common characteristic of stroke patients during standing with more body weight borne on the non- paretic than the paretic limb (102,103). It has been shown that the asymme- trical limb-loading pattern is associated with excessive body sway in the frontal plane and a decrease in lateral stability (103,104), leading to frequent falls towards the affected side (105). Quick and unconscious muscle acti- vations with specific spatio-temporal patterns are prerequisites of the postural responses triggered by an unexpected movement of the support sur- face. Recent results by Fung et al. (106) demonstrated that the postural responses triggered by surface perturbations in healthy subjects, as measured by the changes in center of pressure, body kinematics, and EMG activation were markedly reduced during walking, as compared to standing. In con- trast, stroke patients had difficulty maintaining balance when exposed to perturbations during standing or walking (107). B. Sensory Cues in the Control of Balance Motor learning in stroke patients can be compromised by reduced sensory feedback. Various forms of sensory feedback given to hemiplegic patients have successfully improved the performance. For example, the combined use of biofeedback and functional electrical stimulation to tibialis anterior and gastrocnemius muscles improves flexion of the knee and ankle during the swing phase of walking (108). This improvement in gait function is also shown in the increased gait velocity. Sensory feedback has also been used to improve postural control in stroke patients. Hemiplegic patients who are provided with auditory (109) or visual feedback (110) about their relative weight distribution (paretic vs. nonparetic limb) during standing demon- strate a significant improvement in weight symmetry. Karnath et al. (111) have shown that the combination of galvanic stimulation and vibration of neck muscles can improve visual verticality in stroke patients manifesting hemineglect. Somatosensory information from the fingertip, or haptic cues, is an important source of sensory feedback in the control of balance. Tactile information provided through lightly touching a rigid surface has been shown to decrease postural sway during quiet stance (112,113) and reduce the anticipatory postural adjustments from trunk and leg muscles during a unilateral shoulder flexion task (114). Even passive light touch delivered to the shoulder or leg by an object fixed to the environment can stabilize the body during standing (115). Light touch provided information on the

328 Lamontagne and Fung position and velocity of the body in relation to the external objects or surface (116,117). C. Tactile Sensory Feedback Improves Balance During Walking in Stroke Patients A recent study was conducted to examine the effects of light touch on postural responses triggered by unexpected surface perturbation in the toes-up direction walking in 11 stroke patients and 8 healthy age-matched subjects. A 5-m wide wood plank was mounted firmly beside the walkway to provide somatosensory information from the environment through the fingertip (on the nonparetic for stroke subjects and on the right side for healthy controls). The top of the rail was adjusted at the level of each indivi- dual’s hip level. A thin strip of load sensors (0.15 m  2.45 m dimension) was secured on the surface of the plank to measure the amount of force exerted by the fingertip. A force that exceeded 4 N would trigger a beep and subjects were habituated to walk while sliding the tip of their index finger along the sensor strip without triggering the sound. Figure 6A compares the instantaneous CoM velocity in the A/P direc- tion during walking between the groups of stroke and healthy subjects. In the absence of tactile cue, the speed of forward progression as measured by the CoM velocity was slightly decreased in the control subjects and mark- edly reduced in the stroke subjects when walking was perturbed by a sudden toes-up surface tilt. Generally, the stroke subjects demonstrated an average of 60% decrease in the CoM velocity when walking was perturbed in the absence of tactile cue. While tactile cue did not affect the change in the forward progression of the control subjects during perturbed walking, it significantly increased the speed of forward progression in all stroke subjects (p < 0.005), even though stroke patients still walked slower than control subjects. In the absence of tactile sensory feedback, the decrease in forward CoM velocity was associated with postural instability induced by perturba- tions during quiet stance in stroke patients, as shown by the increased RMS of CoM trajectory in the anteroposterior (AP) direction (Fig. 6B). The group of healthy subjects did not exhibit any significant relation of postural sway with decreased CoM velocity during perturbed walking (R2 ¼ 0.1), but when pooled with the group of stroke patients, a strong linear relation emerged (Fig. 6B, solid line, R2 ¼ 0.72). In the presence of tactile cue, this relation became weakened (Fig. 6B, dotted line, R2 ¼ 0.4) with decreased trunk instability in stroke patients. In addition, the deviations of the trunk and pelvis and the excursion of compensatory movements of the free arm in stroke patients during perturbed walking were significantly decreased when tactile cue was provided. The abnormal and asymmetric muscle activations used by stroke subjects in restoring equilibrium also improved significantly with light touch. The effects of light touch were more prominent in stroke

Systems Approach to Gait Rehabilitation 329 Figure 6 (A) Change in instantaneous velocity of the anteroposterior (AP) CoM during toes-up perturbation in walking; and (B) correlation of the RMS of CoM- AP trajectory during toes-up perturbations quiet stance with the percentage decrease in instantaneous CoM velocity during perturbed walking; in 11 stroke subjects (black) and 8 age-matched healthy controls (gray), in the presence (filled bars) or absence (open bars) of tactile cue provided through the nonparetic (stroke) or right (healthy) index fingertip. The CoM velocity is expressed as the average change from the instant of toes-up surface perturbation during double limb support to the next initial foot contact in the gait cycle, as a percentage of the baseline CoM velocity averaged over 10 unperturbed gait cycles.

330 Lamontagne and Fung subjects, possibly due to the different degree of sensory information available to the two subject groups. These results suggest that tactile sensory feedback can be used for gait rehabilitation following stroke to improve equilibrium reactions during walking. VI. CONCLUDING REMARKS A contemporary approach to gait disorders and rehabilitation is the use of systematic analyses and task-specific locomotor training paradigms. We have presented a comprehensive review of the efficacy of different modes of locomotion (treadmill vs. overground), partial weight support, and speed-intensive training on gait outcomes following stroke. Of particular interest is the potential of speed-intensive training overground with partial weight support that targets low-level functioning stroke patients in the early phase of rehabilitation, as shown by the promising results from our labora- tory. We have also investigated the control of balance during locomotion in stroke patients and explored the use of sensory feedback to improve postural adjustment during gait. Recent results have shown that light touch through the nonparetic fingertip can facilitate the recovery of upright balance when gait is perturbed in stroke patients. These new and encoura- ging findings have advanced our understanding of how motor learning concepts can be extended to gait retraining following stroke. ACKNOWLEDGMENTS We acknowledge the skilful assistance of our graduate students, especially Roain Bayat and Rumpa Boonsinsukh, in data collection and analysis. We appreciate the help of Eric Johnstone in designing and fabricating the overground constant weight support system, made possible through the funding of the JRH Foundation and the Canada Foundation for Innova- tion. We thank the physiotherapists of the JRH neurology program for their help in screening and referring patients for our experiments. A. Lamontagne is a New Investigator supported by the Canadian Institutes of Health Research. J. Fung is a William Dawson Scholar of McGill University and a research scholar of the Fonds de Recherche en Sante´ du Que´bec. The JRH Research Center is a site of the Centre de Recherche Interdisciplinaire en Re´adaptation of Montreal, Canada. REFERENCES 1. Wolfe CD, Giroud M, Kolominsky-Rabas P, Dundas R, Lemesle M, Heusch- mann P, Rudd A. Variations in stroke incidence and survival in 3 areas of Europe. European Registries of Stroke (EROS) Collaboration. Stroke 2000; 31:2074–2079.

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17 Optimizing Gait in Peripheral Neuropathy James K. Richardson Department of Physical Medicine and Rehabilitation, University of Michigan, Ann Arbor, Michigan, U.S.A. I. CHALLENGE OF WALKING AND IMPORTANCE OF SOMATOSENSORY INFORMATION Walking is deceptively difficult. Even a cursory inspection allows some insight into the challenges of upright gait. It is not by accident that humans, when compared with other species, take much longer time to achieve profi- ciency with regard to mobility. Most other mammalian species have a low center of mass, and four limbs are used as a base of support; therefore, the ability to maintain the center of mass within this broad base of support, a definition of balance, is relatively easy. In contrast, human bipedal ambu- lation requires the ability to control and propel an elevated center of mass over just two limbs, which provides a narrow and variable base of support. In order to reliably accomplish this covertly athletic feat, the central nervous system requires timely and accurate information so as to make the motor adjustments necessary to maintain balance (1). This information arrives via the somatosensory, visual, and vestibular systems. Given the difficulty of the bipedal walking task, any distortion in this afferent flow of informa- tion may lead to impairments in balance and difficulty with mobility. In this chapter we will review the epidemiology of PN, how PN-related impairment affects balance, gait and fall risk, and the evaluation of, and interventions to improve gait, balance, and reduce falls in PN. 339

340 Richardson Of the three sources of afferent information, there is a variety of evidence that the somatosensory source is of greatest importance. Among the most compelling and elegant of this evidence, Fitzpatrick and McCloskey (2) demonstrated that healthy persons could perform an equivalent standing task, which eliminated both visual and vestibular input, with solely somatosensory information. Furthermore, this task was still adequately performed after ische- mically induced cutaneous anesthesia of the feet, suggesting that the subjects required just a portion of somatosensory input to maintain balance (3). II. EPIDEMIOLOGY AND CLINICAL IDENTIFICATION OF PERIPHERAL NEUROPATHY A diffuse peripheral neuropathy (PN), which reduces distal somatosensory function and strength, is a common neurologic finding among older persons. Diabetes mellitus is the most common underlying etiology among more socioeconomically developed societies. Epidemiologic studies suggest that the prevalence of diabetes mellitus and impaired glucose tolerance are increasing and affect over 40% of U.S. citizens in the 60 to 74 years of age group (4). Further research suggests that the prevalence of PN in this age group is between 32% and 50% for persons with diabetes mellitus, 11% for persons with impaired glucose tolerance, and 7.1% for normoglyce- mic persons (5). Collectively, these data suggest that the prevalence of PN in the 60–74 years of age group is $22%. The detection of PN is an important contribution to the health care of the older person. Apart from its effect on mobility, PN contributes to or causes foot deformity and pain, skin ulceration (6), and lower extremity amputation (7) and is often associated with treatable systemic disorders (8). However, clinical history is unreliable (9) and physical examination is con- founded by the ‘‘normal’’ decrement in peripheral nerve function that occurs with aging, making the clinical recognition of PN in older persons challen- ging. Age-related changes in peripheral nerve have been detected clinically (10), anatomically (11), and electrophysiologically (12), rendering indis- tinctly the boundary between normal peripheral nerve function for age and PN. There are drawbacks to many recommended techniques for the clinical detection of PN among older patients. Some recommended examinations are lengthy and require expertise, time, and/or equipment not readily available (13,14), whereas others are simpler but have been used only in the evaluation of diabetic neuropathy among relatively young persons (15–19). Given that other causes of PN are common among older persons (20,21), the application of the techniques described in these studies to older persons, with and without diabetes, is uncertain. One-hundred subjects between the ages of 50 and 80 years were studied so as to compare clinical findings among older patients with and

Optimizing Gait in Peripheral Neuropathy 341 Table 1 Absence/Presence of PN for Discrete and Continuous Clinical Variables, Using Optimal Cut-Off Values for the Latter (22) Sensitivity Specificity PN absent PN present p valuea (%) (%) Achilles < 0.001 72.1 90.6 Absent 75 Present 3 49 68.8 Vibration toe 29 Decreased ( < 8 sec) 19 84.4b Normal ( > 8 sec) 8 Position toe 24 < 0.001 95.6 Decreased ( < 8 out 10 65 of 10) Normal ( ! 8 out of 22 3 10) 27 < 0.001 88.2 Of these 3 signs 5 0 or 1 present 60 2 or 3 present 8 < 0.0001 94.1 4 64 aChi-square test. bPositive and negative predictive values are 92.8% and 87.1%, respectively. without PN (22). Sixty-eight of the subjects had electrodiagnostic evidence of PN and 32 who did not, and approximately one-half of the subjects had diabetes mellitus. Three signs, Achilles reflex (absent, despite facilitation via gentle plantar flexion, performed using both tendon-strike and plantar- strike techniques), vibration (128 hz tuning fork perceived for < 8 sec at the great toe), and position sense (< 8 out of 10 1-cm trials at the great toe), were the best predictors of PN on both univariate and logistic regression analyses, the latter using age and body mass index (BMI) as covariates (pseudo R2 ¼ 0.744). The presence of 2 or 3 signs vs. 0 or 1 sign identified PN with reasonable sensitivity and specificity (Table 1). Values were similar among sub-groups with and without diabetes mellitus. It is anticipated that the sensitivity and specificity of these signs would decrease in the office setting, given differences in prior probabilities of finding PN. Patients with equivocal findings, or those with abnormal findings but no obvious reason for PN, should be considered for electrodiagnostic testing so as to confirm the presence of PN in the former and characterize the PN in the latter. III. STATIC BALANCE AND PN Quantified parameters of standing sway have been found to be greater (indicating worse balance) among subjects with PN, when compared with similarly aged diabetic subjects without PN and subjects with neither. These

342 Richardson Table 2 Effect of PN on Measures of Balance Balance task PN subjects Control Signifi- cance, p Bipedal stance Eyes open: 550 Æ 50a 350 Æ 20a < 0.05 Force platform measured Eyes closed 1100 Æ 100a 600 Æ 50a < 0.01 < 0.01 center of pressure excursion Eye open: 35 Æ 12a 20 Æ 8a < 0.01 (sway trace in cm) (23) Eye closed: 55 Æ 18a 30 Æ 10a Center of pressure excursion 0.021 (in cm) (24) 0.12 0.58 0.001 Unipedal stance 3.8 Æ 3.5 32.2 Æ 17.7 Balancing 3 sec on command 0.068 5% lean, 0/6 5% lean, (success rate) (26) 10% lean, 0/6 3/6 Subject controlled (sec) (26) Lateral leans 10% lean, Subjects recovering successfully 1/6 for a given %foot width (48) aApproximations from graphs from Refs. 36 and 38. findings have been identified among both younger (23) and older (24) popu- lations (Table 2). In addition to alterations in standing sway, our laboratory has identified decrements in clinical and high-technology measures of one- legged balance among older PN patients when compared with age-matched controls (25,26). Although it is reasonable to suspect that PN is simply a marker for other disease processes that are the true cause of these balance impairments, such as diabetes mellitus or central nervous system pathology, this does not appear to be the case. A variety of posturographic parameters showed strong correlations with peripheral, but not central, nerve conduc- tion parameters (27) indicating that peripheral nerve dysfunction underlies the impairment in balance. Moreover, subjects with diabetic PN, but not subjects with diabetes and healthy peripheral nerves, demonstrated abnorm- alities of static and dynamic balance as compared to controls (28). IV. EFFECT OF PN ON MOBILITY There is also evidence that PN affects function. Studies have demonstrated that among older subjects, PN is associated with difficulty rising from a chair (29), decreased gait speed and stride length (30–33), and swing limb propulsion strategies based more on hip flexion than ankle plantar flexion (33). The decreased gait speed often falls well below 1.22 m/sec though necessary for safe crossing of streets (34). Subjects with PN demonstrated

Optimizing Gait in Peripheral Neuropathy 343 increased verbal reaction times to auditory stimuli during gait when compared with controls, suggesting that walking requires increased atten- tion for PN patients (35). Despite these high-technology measures of gait aberrancies among PN patients, truncal stability appears to remain normal when patients walk on a flat surface with good lighting at a self-selected speed (31), suggesting that PN patients can compensate for their neurologic impairments under ideal conditions. This finding resonates with clinical experience suggesting that patients with all but the most severe PN do well on a firm, flat, familiar surface with good lighting when not distracted and walking at a self-selected pace. To investigate neuropathic gait under more challenging conditions, we observed 12 older women PN patients and 12 similarly aged healthy older women ambulating under two conditions: (1) with normal lighting on a flat surface and (2) with low lighting (50 lux) on an irregular surface produced by placing wooden prisms under dark industrial carpeting (Fig. 1). Although both PN and control women demonstrated decreased speed and step length and increased step time and step width variabilities (as measured by standard deviations) on the irregular surface when compared with the flat, the PN subjects made significantly greater changes in their gait on the irregular surface (36). Furthermore, the magnitude of the changes in gait parameters among the PN subjects correlated well with the severity of clin- ical neuropathy as determined by the Michigan Diabetic Neuropathy Score (15). These findings suggest that gait differences between older persons with and without PN are minimal under ideal conditions but magnified by chal- lenging, as well as realistic, conditions. The findings assume greater clinical relevance when it is understood that among older persons most falls occur during ambulation, particularly on non-flat surfaces (37). V. PERIPHERAL NEUROPATHY AND FALL RISK Given abnormalities in bipedal balance, unipedal balance, and gait, it is expected that PN patients would demonstrate an increased rate of falls. Relatively young patients with diabetic PN are 15 times more likely to have an injurious fall than age-matched controls with and without diabetes who do not have PN (38). Similarly, older subjects with PN are 15 to 20 times more likely to fall and six times more likely to be injured from a fall than age-matched controls without PN (39,40). Analysis of skeletal remains from a medieval leprosy hospital, as compared to a control medieval skeletal sample, suggests that even ancient populations with PN from leprosy fell and fractured more frequently (41). As with all persons at increased risk for falls, there is concern regarding the potential for injury and loss of func- tion due to injury or fear. Perhaps, of even greater concern to the patient with diabetic PN, there is also the potential loss of a ubiquitous form of

344 Richardson Figure 1 The irregular walkway PN patients traversed under low light conditions. Note the optoelectronic markers over the midline of the trunk and the ankles. Schematic dia- gram demonstrates the manner in which step width and step length were determined. exercise, walking, which can help control the diabetic metabolic derange- ments that influence overall health and survival. VI. AFFERENT AND EFFERENT IMPAIRMENTS ASSOCIATED WITH PN Efforts have been made to quantify the afferent deficit behind the decrement in function described earlier. Cavanagh and colleagues (42) found that ankle dorsiflexion/plantar flexion proprioceptive thresholds were increased (worse) among older subjects with diabetic PN when compared with control groups of similarly aged subjects with non-neuropathic diabetes and without diabetes or PN. PN subjects’ perception thresholds were in the range of 3 to 5 degrees when compared with a threshold of 1 to 5 degrees for the subjects without PN (Table 3). It was noted that quantitative sensory testing of

Table 3 Functionally Significant Sensory and Motor Impairments Associated with PN Optimizing Gait in Peripheral Neuropathy Impairment PN subjects Control subjects Significance, p Sensory Dorsi/plantar flexion, 4.6 Æ 4.5 1.4 Æ 0.7 < 0.01 Ankle proprioceptive thresholds Inversion, 1.30 Æ 1.06 0.21 Æ 0.19 0.048 Eversion, 2.57 Æ 2.90 0.39 Æ 0.10 0.036 (degrees) (42,43) Dorsiflexion, 24.3 Æ 6.8 30.7 Æ 7.5 < 0.0001 Motor Plantar flexion, 87.8 Æ 23.2 111.0 Æ 28.7 < 0.01 Maximal isokinetic strength [open Knee extension, 150.8 Æ 38.5 178.6 Æ 52.8 < 0.0001 Knee flexion, 82.4 Æ 20.2 99.6 Æ 31.0 < 0.01 chain (Nm)] (45) Wrist extension, 8.5 Æ 2.4 9.5 Æ 3.2 Dorsiflexion, 4765 Æ 1681 6343 Æ 1524 NS Peak acceleration [open chain Plantar flexion, 5737 Æ 1977 7601 Æ 1825 < 0.001 (m/sec2)] (46) Knee extension, 4737 Æ 1820 5899 Æ 2013 < 0.001 78.2 Æ 50.8 152.7 Æ 54.6 < 0.05 Rate of torque development [closed chain inversion (Nm/sec)] (48) 0.016 Abbreviation: NS, Non-significant. 345

346 Richardson vibration and touch explained only about 20–45% of the variance in ankle proprioception. Our laboratory quantified ankle inversion/eversion pro- prioceptive thresholds in older subjects with PN and age-matched controls. Overall, the PN group demonstrated thresholds that were 4.6 times greater (worse) than controls subjects (Table 3) (43). Moreover, the PN subjects were found to have significantly decreased clinical toe position sense (num- ber correct of 10 1-cm trials at great toe) but normal clinical ankle position sense, suggesting that decreased clinical position sense at the toe is asso- ciated with impaired sub-clinical ankle proprioception. Motor abnormalities have been identified electrophysiologically in patients with solely sensory signs and by means of quantified strength test- ing in PN patients with normal clinical muscle testing (Table 3) (44,45). Furthermore, these motor deficits occurred not only in plantar flexion and dorsiflexion, but also in knee extension/flexion (45,46). These abnormalities correlated with clinical measures of PN severity, but not with retinopathy or nephropathy, and were not found among diabetic patients without PN. The findings contrasted markedly from the usual clinical perspective that reduced dorsiflexion strength is the first sign of strength loss at the ankle, and that the knee extensors and flexors are usually unaffected. Because of the shape of the foot and the frequency with which lateral falls lead to injury (47), ankle inversion strength is of particular importance in terms of arresting a lateral perturbation. Therefore, our laboratory quantified closed chain ankle inversion strength in six pairs of diabetic age-matched older women (one of each pair with and without PN), with clinically normal ankle strength under two different conditions (48). In the first test, the subjects were required to recover from a lateral lean, induced by the release of a horizontal lean control cable attached to a pelvic belt, and in the second test, the subjects voluntarily moved the center of reaction as quickly as possible to the lateral edge of their foot, by perform- ing an ankle inversion maneuver during a 10-sec trial. The women with PN were never able to recover from the lateral leans test, whereas some of the older women without PN were able to do so (Table 2). Somewhat surpris- ingly, the two groups did not differ in terms of closed chain ankle inversion strength (Nm). However, the rate of strength development (determined by the slope of the tangent of the force/time curve, in Nm/sec) was markedly decreased for the PN group (Table 3). Furthermore, this measure of ankle rate of strength development, but not ankle strength, strongly correlated with clinical unipedal stance time (Fig. 2). Taken together, the data suggest that strength that is rapidly available is of greater assistance in the maintenance of balance than ankle strength that is only slowly available, and that PN patients with clinically normal ankle strength have impairments in rapidly available ankle strength. Similarly, recent research among older persons without PN has demonstrated that power, a measure of speed of force

Optimizing Gait in Peripheral Neuropathy 347 Figure 2 The relationship between rate of torque development and unipedal stance time among 12 diabetic women, six with PN and six without (17). Rate of strength development at the ankle explained more of the variance in unipedal stance time than did ankle strength (17). production, is an entity distinct from strength that may have a greater influ- ence on mobility function (49). It is likely that the impairments in ankle proprioceptive thresholds and strength interact to cause impairments in balance. A useful analogy with which to visualize this interaction is to imagine the center of mass (anterior to L5) as a randomly moving but tightly bunched flock of sheep on top of a small plateau, which in turn represents the base of support. The center of ground reaction force is imagined to be a sheepdog whose job is to keep the sheep on the plateau. When the sheep wander too near the edge of the plateau, the sheepdog must position itself between the sheep and the edge and compel the sheep to move back to the middle of the plateau. Similarly, when the center of mass moves, for example, too anteriorly, the plantar flexors must quickly contract so that the ground reaction force moves ahead of the center of mass and forces it posteriorly. To be successful, the sheep- dog must be vigilant and fast. Unfortunately, for PN patients, the sheep- dog/ground reaction force is not vigilant and does not perceive the position of the sheep/center of mass until they are near the edge because of the afferent impairment discussed earlier. When the location of the sheep/center of mass is finally apparent, the sheepdog/ground reaction force moves slowly, due to the efferent impairment discussed earlier, and the sheep fall off before the sheepdog/ground reaction force can position itself between the sheep and the abyss. This interaction between afferent

348 Richardson and efferent impairments likely underlies the marked difficulty that PN patients have with one-legged stance (25,26). Furthermore, there is evidence that when ankle muscles fatigue, as likely happens more rapidly among those with PN than those without, position sense worsens still further (50). VII. WHICH PATIENTS WITH PN ARE MORE LIKELY TO FALL? Because not all patients with PN fall, it would be convenient if it were pos- sible to identify those at greatest risk. To address this question, 83 patients with PN were studied, none of whom had evidence of central neurologic or significant musculoskeletal abnormalities (51). Forty (48.8%), 28 (34.1%), and 18 (22.0%) subjects reported a history of at least one, multiple, and injurious falls, respectively, over the previous 2 years. Factors associated with single and multiple falls were similar and so, only results for multiple and injurious falls are reported. Using logistic regression controlling for age, sex, comorbidities, and use of medications associated with falls, an increased BMI and more severe PN (as determined clinically by the Michi- gan Diabetes Neuropathy Score) (15) were associated with both fall cate- gories (pseudo R2 ¼ 0.458 and 0.484, respectively, for multiple and injurious falls). Medications associated with fall risk demonstrated a trend toward association with falls among the PN subjects, but age, gender, nerve conduction study parameters, Romberg testing, and comorbidities were not consistently associated with either fall category during bivariate or multi- variate analysis. When the genders were analyzed separately, BMI appeared to be the stronger risk among women and PN severity the stronger risk among men. In addition, men with a history of falls demonstrated shorter unipedal stance times (3.7 vs. 7.8 sec, fallers vs. non-fallers; p ¼ 0.025). VIII. CLINICAL EVALUATION OF BALANCE If PN is suspected due to history or positive findings on examination, then a functional evaluation is indicated. Chair rise should be evaluated and, in one study of older women, has been related more strongly to PN than knee extensor strength (29). Romberg testing is insensitive to mild to moderate PN and so, if positive, the test indicates severe PN or the presence of more proximal disease such as myelopathy. Unipedal stance testing (three attempts on the foot of choice) is most helpful when normal. Clinical experi- ence suggests that if the older patient can achieve unipedal balance for > 10 sec, it is likely that the PN is of minimal functional significance, but if the PN patient cannot achieve !5 sec on any attempt, they should be considered at increased fall risk (51,52). It is important that the patient re-sets and equally distributes weight on both feet prior to each attempt. Unipedal stance testing may assess fall risk better in men than in women (51,52). Unipedal stance should also be used to evaluate hip abductor

Optimizing Gait in Peripheral Neuropathy 349 strength. A drop in the non-weight-bearing side of the pelvis, or an excessive lateral trunk shift toward the weight-bearing side, indicates hip abductor weakness on the stance side, a treatable finding that will lessen contralateral limb clearance during the swing phase of gait. IX. EVALUATION OF GAIT A. Foot Clearance Watching the patient ambulates several lengths of a hallway is the most important part of the evaluation. When considering the PN patient, special attention should be paid to forefoot clearance initially and at the end of the walk, because it is common for clearance to lessen over time as the anterior tibialis and/or hip abductors fatigue. If forefoot clearance is decreased unilaterally, then the strength of the dorsiflexors ipsilateral to the side of reduced clearance should be evaluated. Strength may be normal with one repetition and is therefore more effectively evaluated with 10 consecu- tive resistance maneuvers. Asymmetric strength may represent an L5 radicu- lopathy or, more likely a peroneal mononeuropathy at the fibular head, superimposed on the PN. If the latter is identified, then causes of pressure over the lateral aspect of the knee, due to activities such as leg crossing, or episodes of prolonged knee flexion should be sought and corrected. A lightweight ankle foot orthosis, custom fabricated so as to prevent skin injury and ongoing pressure over the fibular head, will be helpful and has been demonstrated to increase speed and step length and to decrease energy expenditure during gait among patients with lower motor neuron disorders (53,54). Acceptance of orthoses may improve if the patient understands that the device need only be worn during times of anticipated fatigue. If forefoot clearance is decreased bilaterally due to dorsiflexor weakness, it is likely that the patient has severe PN. Such patients will likely benefit from bilateral ankle–foot orthoses and will likely also need a cane or touch of some other surface for balance. The strength of the hip abductors contralateral to the side(s) of reduced clearance should also be evaluated. A drop in the non-weight-bearing side of the pelvis, or an excessive lateral trunk shift toward the weight-bearing side, indicates hip abductor weakness on the stance side, a treatable finding that will lessen contralateral limb clearance during the swing phase of gait. Hip abductor weakness may be due to under- lying hip arthritis, a gluteus medius tear or tendonitis, which often presents as a refractory greater trochanteric ‘‘bursitis’’ (55), L5/S1 radiculopathy, myopathy or simple deconditioning. Regardless of the etiology, if hip abductor strengthening is not successful, a cane in the contralateral upper extremity will effectively lessen demands on the affected hip abductors (56). Leg length discrepancy may also be responsible for asymmetric foot clearance, with the longer side demonstrating less clearance. A heel wedge

350 Richardson Figure 3 The cane height is adjusted to the level of the wrist and the patient places the cane forward in synchrony with the contralateral lower extremity. on the shorter side, which corrects about one-half of the discrepancy, is often helpful and may reduce energy expenditure (57). B. Step Variability The examiner should also focus on step-width variability. Patients with functionally significant PN will typically demonstrate variable foot place- ment in the frontal plane, with steps varying excessively in width. The rele- vance of this finding is underscored by biomechanical studies that indicate

Optimizing Gait in Peripheral Neuropathy 351 medial–lateral alteration of foot placement to be the most effective and effi- cient way to control lateral motion during ambulation (58), and frontal plane balance to be primarily determined by medial–lateral foot placement relative to the center of mass (59). Of particular concern is a step so medially directed that it crosses into the path of the stance limb when it transits into swing phase. Such a step brings about the possibility of a collision, a common and destabilizing event among older persons presented with lateral perturba- tions (60), between the stance and swing limb with the next step. Therefore, correcting step-width and step-time variabilities, the latter being less clinically detectable than the former but strongly and prospec- tively associated with falls (61), in older patients with PN is of interest. We recently studied the effect of a cane (Fig. 3), touch of a vertical surface (Fig. 4), and ankle orthoses (Fig. 5) that supported the medial and lateral aspect of the distal lower leg (62) on step-width and step time variabilities in 42 PN subjects as they traversed a walkway with an irregular surface under low light conditions (as described in Fig. 1) (63). The subjects demonstrated significantly decreased step-width variability and step-width range with each of the interventions on the irregular surface, when compared with the con- trol condition without the interventions. Step-time variability also decreased with use of all three interventions; however, the decrease was significant only for the orthoses and vertical surface, whereas the decrease in step-time varia- bility with cane use was only a trend. The cane significantly slowed gait speed when compared with the control condition, whereas the orthosis and vertical surface did not change gait speed. Overall, the results suggest that with just brief (5 min) practice, each of the interventions improved med- ial–lateral stability and reduced temporal variability of PN patients during a challenging walking task but at the cost of speed for the cane and availabil- ity for the vertical surface. The orthoses had neither of these limitations but carry the concern of skin problems, particularly at the ankle for those patients with both PN and venous insufficiency. X. GENERAL RECOMMENDATION AND INTERVENTIONS A. Education Education of the patient and/or family is universally important. Patients with PN, as well as their physicians, often underestimate their degree of disability due to PN because of its insidious onset and the gradual adaptive response that restricts mobility. The patient and family must be made to understand that the PN patient has lost a special sense, as well as likely rapidly available strength, in the lower extremities and will need to compen- sate for that loss if the patient is to regain or retain previous levels of func- tion. If the use of adaptive aids to compensate for PN is described as being analogous to the use of spectacles for decreased vision or a hearing aid for

352 Richardson Figure 4 The subject touched a wall at about shoulder height as they walked on the irregular surface. Subjects used the dorsal or palmar surface of their hands, on the basis of their preference. Figure 5 The ankle orthoses in place, with foam-lined shells on the medial and lateral aspects of the lower leg.

Optimizing Gait in Peripheral Neuropathy 353 loss of hearing acuity, compliance may be better. It is also important to communicate that PN patients generally do well when undistracted, walking at a self-selected speed on a surface that is firm, flat, familiar, and well lit. Interventions are used for all other times. B. Environmental Modification Convenient and reliable surfaces for upper extremity touch or support should be arranged, particularly adjacent to stairs and any other irregular surfaces. The support need not always be obvious, such as grab bars in the bathroom, but can be solid furniture such as sofa arms. A home visit by an occupational or physical therapist is often fruitful. The patient’s intrinsic environment should be modified as well, and medications asso- ciated with falls (hypnotics, anxiolytics, anti-hypertensives, anti-depressants, anti-convulsants) should be discontinued whenever possible (51). C. Maximizing Visual Input Because somatosensory information is impaired, vision must be maximized intrinsically through proper refraction and ophthalmologic consultation and extrinsically through lighting. In particular, the path for nocturnal trips to the bathroom must be well lit. Recent work has confirmed the clinical suspicion that bifocals or trifocals (including ‘‘progressive’’ lenses) are associated with falls; therefore, reading and ‘‘walking’’ glasses are best used separately (64). D. Strengthening Our study of older PN subjects using a cane to recover from a perturbation while performing a transfer from bipedal to unipedal stance demonstrated that patients often put 25% of their body weight onto a cane during recovery (65). Therefore, upper extremity strengthening of grip, elbow extensors, and shoulder depressors will maximize efficacy of canes and walkers. Given the relative lack of healthy axons to distal muscles in the setting of PN, it is unli- kely that significant distal muscle hypertrophy can occur in subjects with PN (66). However, strengthening may still occur by means of improved centrally mediated synchronization of motor units (67). Accordingly, knee extensor strength in patients with lower motor neuron disorders has been found to increase with resistance regimen (68). In a single blind study of 20 PN patients, a 3-week program of closed chain ankle strengthening and unipe- dal balance practice led to improvements in functional reach, tandem stance, and unipedal balance, whereas a control exercise regimen did not (69). Although unstudied, strengthening of the hip abductors and abdominal oblique musculature is also recommended on the basis of the importance of these muscles to, respectively, medial–lateral hip and trunk stability.

354 Richardson E. Balance Training Little work has been done investigating the effect of balance training on PN populations. Older persons without PN who received balance training have been found to decrease standing sway on a foam surface, a condition that mimics impaired somatosensory input (70). Despite the minimal data in this area, consultation with a physical therapist is often helpful in other ways. Patients may improve their insight into their capabilities and limitations in a safe setting and receive expert assistance in designing strategies for solving unique mobility dilemmas. F. Enhancing Plantar Surface Sensation Pilot studies have demonstrated that older persons with decreased plantar sensation demonstrated a more rapid response to mediolateral perturbations when standing on a surface that indented the plantar skin surface (1-mm ball bearings) (71). In addition, recent work evaluated vibratory ‘‘noise’’ applied to the plantar aspects of the feet of older persons during standing. Under these conditions, subjects demonstrated less sway than under the control condition without the noise (72,73). These novel interventions seem promising for patients with mild PN, although their effects on gait had not been investigated at the time of this writing. G. Foot Pain Asymmetries in gait may be due to an antalgic pattern. Too often, clinicians assume that foot pain in a patient with PN is due to the PN itself. However, pain that increases with weight-bearing is rarely solely neuropathic and is usually mechanical. Foot intrinsic muscle weakness distorts the normal foot anatomy and weight-bearing forces. These changes render the PN patient susceptible to a variety of disorders, but most commonly meta-tarsal pain, plantar fasciitis, and stress fractures. These sources of pain can usually be identified clinically, despite altered sensation, by palpating the appropriate regions patiently and thoroughly. Patience is required because PN patients are often slow to recognize a pain source. Strong thumb pressure over each of the metatarsal heads and over the origin of the plantar fascia, on the med- ial aspect of the calcaneus, with the foot maximally dorsiflexed will usually uncover the source of pain. Similarly, thorough palpation of the length of each of the metatarsals from above and below with the thumb and forefinger will identify most stress fractures. Metatarsalgia and plantar fasciitis symp- toms improve with in shoe orthoses designed to support the longitudinal arch and off-load the metatarsal heads. Exercise to stretch the Achilles tendon and plantar flexors are recommended but should only be done when wearing the orthoses. When a stress fracture is suspected, the patient should undergo plain films and a bone scan if symptoms have not been

Optimizing Gait in Peripheral Neuropathy 355 prolonged and suspicion remains. The latter is particularly helpful in iden- tifying early Charcot changes. If the scan is positive, off-loading the region with a cast-boot and rocker sole or crutches is recommended, as is referral to an orthopedic specialist. XI. SUMMARY PN is a common and readily identifiable finding among older persons that distorts afferent information from the distal lower extremities and blunts rapid motor responses. These changes result in balance impairment and a marked increased risk of falls and fall-related injuries. Patients with PN and their physicians often underestimate the resultant disability because patients have minimal difficulty ambulating in the office setting and other ideal conditions. However, when challenged by an irregular surface and/ or reduced lighting, these patients show marked changes in gait and often fall. Fall risk can be minimized by a program, tailored to the patient’s specific vulnerabilities, which may include patient/family education, envir- onmental modification, maximizing visual input, strengthening, and balance training. Patients should be advised that when the walking surface is firm, flat, and familiar, the lighting good and the environment non-distracting, then patients may walk without assistance; however, when these conditions are not present, then older PN patients should use a cane, touch of a stabi- lizing surface, or use of ankle orthoses that provide medial–lateral support. ACKNOWLEDGMENT The author was supported by Public Health Services Grants 1K23 AG00989 and 2P60 AG08808. REFERENCES 1. Gandevia SG, Burke D. Does the nervous system depend on kinesthetic information to control natural limb movements?. Behav Brain Sci 1992; 15: 615–632. 2. Fitzpatrick R, McCloskey DI. Proprioceptive, visual and vestibular thresholds for the perception of sway during standing in humans. J Physiol 1994; 478(Pt 1): 173–186. 3. Fitzpatrick R, Rogers DK, McCloskey DI. Stable human standing with lower-limb muscle afferents providing the only sensory input. J Physiol 1994; 480(Pt 2):395–403. 4. Harris MI, Flegal KM, Cowie CC, Eberhardt MS, Goldstein DE, Little RR, Wiedmeyer HM, Byrd-Holt DD. Prevalence of diabetes, impaired fasting glucose and impaired glucose tolerance in U.S. adults: The Third National Health and Nutrition Examination Survey, 1988–1994. Diabetes Care 1998; 21(4):518–524.

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358 Richardson 37. Berg WP, Alessio HM, Mills EM, Tong C. Circumstances and consequences of falls in independent community-dwelling older adults. Age Aging 1997; 26(4):261–268. 38. Cavanagh PR, Derr JA, Ulbrecht JS, Maser RE, Orchard TJ. Problems with gait and posture in neuropathic patients with insulin-dependent diabetes mellitus. Diabet Med 1992; 9(5):469–474. 39. Richardson JK, Ching C, Hurvitz EA. The relationship between electromyogra- phically documented peripheral neuropathy and falls. J Am Geriatr Soc 1992; 40(10):1008–1012. 40. Richardson JK, Hurvitz EA. Peripheral neuropathy: a true risk factor for falls. J Gerontol A Biol Sci Med Sci 1995; 50A(4):M211–M215. 41. Judd MA, Roberts CA. Fracture patterns at the Medieval Leper Hospital in Chichester. Am J Phys Anthropol 1998; 105(1):43–55. 42. 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. 43. Van den Bosch CG, Gilsing MG, Lee SG, Richardson JK, Ashton-Miller JA. Peripheral neuropathy effect on ankle inversion and eversion detection thresh- olds. Arch Phys Med Rehabil 1995; 76(9):850–856. 44. Wolfe GI, Baker NS, Amato AA, Jackson CE, Nations SP, Saperstein DS, Cha CH, Katz JS, Bryan WW, Barohn RJ. Chronic cryptogenic sensory polyneuropathy: clinical and laboratory characteristics. Arch Neurol 1999; 56(5):540–547. 45. 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. 46. Andersen H, Mogensen PH. Disordered mobility of large joints in association with neuropathy in patients with long-standing insulin-dependent diabetes. Diabet Med 1997; 14(3):221–227. 47. Greenspan SL, Myers ER, Maitland LA, Resnick NM, Hayes WC. Fall severity and bone mineral density as risk factors for hip fracture in ambulatory elderly. JAMA 1994; 271(2):128–133. 48. Gutierrez EM, Helber MD, Dealva D, Ashton-Miller JA, Richardson JK. Mild diabetic neuropathy affects ankle motor function. Clin Biomech 2001; 16(6): 522–528. 49. Bean JF, Leveille SG, Kiely DK, Bandinelli S, Guralnik J, Ferrucci L. A comparison of leg power and leg strength within the InCHIANTI study: which influences mobility more? J Gerontol: Bio Med Sci 2003; 58(8):728–733. 50. Forestier N, Teasdale N, Nougier V. Alteration of the position sense at the ankle induced by muscular fatigue in humans. Med Sci Sports Exerc 2002; 34(1):117–122. 51. Richardson JK. Factors associated with falls in older patients with diffuse poly- neuropathy. J Am Geriatr Soc 2002; 50(11):1767–1773. 52. Vellas BJ, Wayne SJ, Romero L, Baumgartner RN, Rubenstein LZ, Garry PJ. One-leg balance is an important predictor of injurious falls in older persons. J Am Geriatr Soc 1997; 45(6):735–738.

Optimizing Gait in Peripheral Neuropathy 359 53. Duffy CM, Graham HK, Cosgrove AP. The influence of ankle–foot orthoses on gait and energy expenditure in spina fibida. J Pediatr Orthop 2000; 20(3):356–361. 54. Bean J, Walsh A, Frontera W. Brace modification improves aerobic perfor- mance in Charcot–Marie-Tooth disease: a single-subject design. Am J Phys Med Rehabil 2001; 80(8):578–582. 55. Kingzett-Taylor A, Tirman PF, Feller J, McGann W, Prieto V, Wischer T, Cameron JA, Cvitanic O, Genant HK. Tendinosis and tears of gluteus medius and minimus muscles as a cause of hip pain: MR imaging findings. Am J Roent- genol 1999; 173(4):1123–1126. 56. Joyce BM, Kirby RL. Canes, crutches and walkers. Am Fam Physician 1991; 43(2):535–542. 57. Abdulhadi HM, Kerrigan DC, LaRaia PJ. Contralateral shoe-lift: effect on oxygen cost of walking with an immobilized knee. Arch Phys Med Rehabil 1996; 77(7):670–672. 58. Kuo AD. Stabilization of lateral motion in passive dynamic walking. Int J Robot Res 1999; 18(9):917–930. 59. MacKinnon CD, Winter DA. Control of whole body balance in the frontal plane during human walking. J Biomech 1993; 26(6):633–644. 60. Maki BE, Edmonstone MA, McIlroy WE. Age-related differences in laterally directed compensatory stepping behavior. J Gerontol: Med Sci 2000; 55A(5):M270–M277. 61. Hausdorff JM, Rios DA, Edelberg HK. Gait variability and fall risk in commu- nity-living older adults: a 1-year prospective study. Arch Phys Med Rehabil 2001; 82(8):1050–1056. 62. Active Ankle Systems Inc., 509 Barrett Ave., Louisville, KY 40204. 63. Richardson JK, Thies S, DeMott T, Ashton-Miller JA. Interventions improve gait regularity in patients with peripheral neuropathy while walking on an irre- gular surface under low light. J Am Geriatr Soc 2004; 52(4):510–515. 64. Lord SR, Dayhew J, Howland A. Multifocal glasses impair edge-contrast sen- sitivity and depth perception and increase the risk of falls in older people. J Am Geriatr Soc 2002; 50(11):1760–1766. 65. Ashton-Miller JA, Yeh MW, 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. 66. Carlson BM, Faulkner JA. Muscle regeneration in young and old rats: effects of motor nerve transection with and without marcaine treatment. J Gerontol A Biol Sci Med Sci 1998; 53(1):B52–B57. 67. Rutherford OM, Jones DA. The role of learning and coordination in strength training. Eur J Appl Occup Physiol 1986; 55(1):100–105. 68. Lindeman E, Leffers P, Spaans F, Drukker J, Reulen J, Kerckhoffs M, Koke A. Strength training in patients with myotonic dystrophy and hereditary motor and sensory neuropathy: a randomized clinical trial. Arch Phys Med Rehabil 1995; 76(7):612–620. 69. 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):205–209.

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18 Posthip Fracture and Hip Replacements Jeremy A. Idjadi and Joseph D. Zuckerman NYU—The Hospital for Joint Diseases Orthopedic Institute, New York, New York, U.S.A. Kenneth Koval Dartmouth-Hitchcock Medical Center, Orthopedic Surgery, Lebanon, New Hampshire, U.S.A. I. INTRODUCTION Disease of the hip, whether from osteoarthritis, hip fracture, or another etiology, is a significant source of morbidity and mortality. The burden on both patients and the health care system is immense. Some authors estimate that by the year 2040, over 500,000 hip fractures will occur in the United States, incurring $16 billion in health care expenses (1). Furthermore, over 250,000 total hip arthroplasties are performed in the United States each year for osteoarthritis and a variety of other diseases. In light of the obvious impact that these diseases and their treatment have on patients as well as society, attempts at decreasing morbidity by implementing safe, efficient, and effective rehabilitation programs is paramount. Loss of mobility is a factor that contributes to the prolonged recovery following hip fractures, as well as to the increased one-year mortal- ity rate (2). Additionally, pre and postoperative ambulatory ability has been shown to correlate with survival time (3). Gait, along with balance, is one of the major components of mobility (4). The effective and efficient evaluation and management of gait disorders, in patients who have undergone total hip 361

362 Idjadi et al. replacement and the operative treatment of hip fractures, is essential to improve outcomes and to lessen the burden on the patient and on society. II. GOALS As is often the case in medicine, the goal of the orthopedic surgeon, the physiatrist, and other healthcare workers, is to help return the patient to their premorbid level of function. Due to the nature of the diseases contributing to the need for hip arthroplasty, many candidates for the procedure have some element of gait dysfunction prior to surgery. Thus, the goal should be to regain the level of gait function that preceded any manifestation of the underlying disease process. There are many factors that may affect return to premorbid func- tion. Bilateral disease is one such factor that can have a dramatic effect on return of function. In these patients, optimal gait function is not achieved until both hips have been treated and have recovered. As expected, patients with unilateral disease show better gait analysis results postarthroplasty, than patients with bilateral disease after either side has been treated (5). Furthermore, though gait efficiency has been shown to improve after total hip arthroplasty, the level of recovery generally does not quite attain premor- bid gait status (6,7). It has also been shown that, as compared to healthy women, patients who underwent total hip arthroplasty show a significantly decreased hip extensor force as well as a significantly decreased gait speed (8). The goal of rehabilitation after hip fracture should be a return to prefracture ambulatory status, whether this represents independent commu- nity ambulation or household ambulation with a walker (9). As has been shown in many different studies, one of the most important predictors of ambulation progress after hip fractures, is the level of premorbid ambulation. Age, ASA rating, fracture type, and nursing home residence prior to hip fracture have also been shown to be predictors of postoperative ambulation (10–13). In one study, 41% of patients regained prefracture level of ambulation while 59% lost some degree of ambulatory ability (12). Though general condi- tioning and fitness may be promoted for at risk groups, practically speaking, it is difficult to alter these preinjury factors in the population of patients who sustain hip fractures. The importance of maximizing postoperative recovery of ambulation is emphasized by the fact that gait function has been shown to be predictive of long-term hospital care vs. discharge to home (4,14). III. PREOPERATIVE As in all of medicine, evaluation of the entire patient is of the utmost impor- tance. While the majority of patients undergoing hip replacement will have a diagnosis of unilateral osteoarthritis, it is important to consider other diag- noses which may affect the surgical plan, rehabilitation plan, and expected

Posthip Fracture and Hip Replacements 363 outcome. Bilateral disease is one situation in which gait analysis has shown that patients reach optimal function only after bilateral total hip arthro- plasty has been performed. Patients with unilateral disease have superior postoperative gait patterns as compared to those with bilateral disease who have undergone unilateral surgery (5). The primary diagnosis may also help predict the expected outcome for specific groups. For example, it has been shown that patients with rheumatoid arthritis, who often have multiple involved joints, walk slower, are weaker preoperatively, and have less increase in strength postoperatively (15). Other concurrent pathology such as that of the ipsilateral or contralateral knee, or lumbar spine, must also be considered. Careful consideration of comorbidities is also important, as some have been found to be associated with compromised gait function. For example, Parkinsonism, age, American Society of Anesthesiology rating of operative risk, and delirium have been found to be associated with poor functional outcome, including decline in ambulation, following operative management of hip fractures (10,12,16–18). Because the occurrence of hip fractures is not predictable, little can be done preoperatively to optimize the patient’s condition before surgery. Though the operative treatment of hip fractures may be considered urgent, an attempt to medically optimize patients prior to surgery is imperative (19–23). In contrast to the need for urgent treatment of hip fractures, the condi- tions leading to total hip arthroplasty are usually much more chronic in nature. It has been demonstrated on a number of occasions, that ambulatory function prior to total hip replacement is predictive of function afterwards. More specifically, patients with greater walking disability prior to surgery were found to function at lower levels postoperatively (12,15). Thus, though some studies have shown that preoperative muscle output is not predictive of postoperative strength (15), it may be prudent to maximize gait function with attention to strength, range of motion, and endurance, prior to elective surgery. One such study compared three gait parameters (cadence, stride length, and gait velocity) as well as walk distance between exercise protocol groups and control groups, both preoperatively and postoperatively. Though there were no significant differences between the groups preoperatively, the exercise group had significantly higher postoperative scores on every parameter, at nearly every time point examined. Furthermore, a preoperative exercise program was shown to result in an approximately three month earlier return of gait function, as compared to routine preoperative and postopera- tive care (24). With regards to total hip arthroplasty, an obvious caveat is that one of the major indications is to relieve pain and restore function so that a patient may mobilize and optimize independence (24–26). It can be expected that preoperative musculoskeletal optimization may be limited by pain and decreased fitness (24). Therefore, any preoperative exercise regimen must

364 Idjadi et al. be individualized and carefully consider the patient’s discomfort and functional status. IV. INTRAOPERATIVE Intraoperatively, there are many variables that may affect outcome. In total hip arthroplasty (Figs. 1 and 2), both the procedure performed, and the implant used, have been shown to affect gait (27–30). Although the indica- tions of staged vs. simultaneous bilateral hip replacement for patients with bilateral disease is beyond the scope of this discussion, as mentioned above, it has been shown that patients do not gain optimal gait function until both hips are replaced (5). With regards to intertrochanteric hip fractures (Figs. 3 and 4), it has been suggested that the quality of fracture reduction is more predictive of better walking performance than the type of device used (31). In general, for both intertrochanteric and femoral neck fractures (Figs. 3 through 6), Figure 1 Radiograph of a hip with osteoatrthritis.

Posthip Fracture and Hip Replacements 365 Figure 2 Radiograph of an uncemented total hip replacement used to treat an osteoarthritic hip. no significant difference has been noted between internal fixation and pros- thetic replacement with regards to ambulatory ability outside of the early postoperative period (1,9,32–35). V. POSTOPERATIVE A. Early Mobilization Postoperatively, there are many ways to improve function and decrease morbidity. Early mobilization out of bed after hip surgery, whether for fracture fixation or arthroplasty, is imperative for the welfare of the patient. This reduces the risk of deep-vein thrombosis, pulmonary complications, skin breakdown, and decline in mental status (36,37). Furthermore, mobiliz- ing a patient encourages one to begin the recovery process.

366 Idjadi et al. Figure 3 Radiograph of an intertrocanteric hip fracture. B. Early Physiatry Evaluation Rehabilitation after hip surgery should be started on postoperative day 1. After an appropriate referral, the physiatrist and physical therapist should conduct a complete evaluation. This acute care evaluation should include a review of the patient’s diagnosis, the surgical procedure done, and the patient’s weight bearing status. The therapist should assess the patient’s medical status so that they may be aware of any conditions that could adversely affect the rehabilitation process. Furthermore, it is imperative that the therapist take note of the patient’s premorbid level of function, as well as their social and living situation, both of which will determine their ambu- latory needs and goals. A careful physical assessment should also be performed and documen- ted. It should include: joint range of motion, muscle strength, and flexibility. Particular attention should be directed toward the operative lower extre- mity, as well as to the upper extremities, which will be invaluable during

Posthip Fracture and Hip Replacements 367 Figure 4 Radiograph of an intertrochanteric hip fracture after internal fixation with a sliding hip screw device. transfers as well as with the use of assistive devices. Further, neurologic, balance, and functional assessments may also be made. The therapist should take note of the surgical wound or dressing and any deformities that may be present. The above evaluation, in conjunction with the orthopaedist’s or physiatrist’s physical therapy order, is then used in formulating a physical therapy treatment plan customized for each patient. Though gait training may be one of the ultimate goals, mobilization and transfer training, strength training, balance training, and maintenance of joint range of motion must be an essential part of a comprehensive rehabilitation program. The patient should be assisted out of bed to a chair on postoperative day 1. If unable to tolerate this transfer, the patient may be helped to the edge of the bed into a dangling position. The therapist should also provide instruction in bed mobility. As recovery progresses, the amount of assistance given to the patient by the therapist gradually decreases until he or she can transfer independently.

368 Idjadi et al. Figure 5 Radiograph of a femoral neck fracture. Exercise and strength training is started on the acute care service for both hip fracture and total hip replacement patients. Instruction is provided for an exercise program in three positions: supine, sitting, and standing. The exercises are administered on a daily basis. Supine exercises include quadriceps sets, heel slides, active assisted hip flexion, active assisted straight leg raising, active hip extension and abduction, and ankle pumps. Quadri- ceps strengthening is important to facilitate independent transfer ability. A significant relationship between hip abductor strength and ambulation without supervision has been found by some investigators (9). In a sitting position, exercises start with active knee extension. Self-assisted hip flexion with a towel (in patients who had internal fixation) is an effective way to increase the patient’s hip flexion strength. Standing exercises include straight leg raises while the patient holds onto parallel bars, hip abduction, hip flexion, and quarter-knee bends. Stand-

Posthip Fracture and Hip Replacements 369 Figure 6 Radiograph of a cemented hemi-arthroplasty used to treat a femoral neck fracture. ing exercises are performed concentrically with a 3 or 5 seconds isometric hold and then continued eccentrically as the lower extremity is lowered. Exercises progress from active assisted, to active, and then resistive. Repetitions are increased to enhance the patient’s endurance. Patients whose balance is impaired may require contact guarding when performing standing exercises. Activity precautions must be considered, depending on the injury or procedure performed. Patients with hip fractures treated with internal fixation generally have no restriction regarding hip range of motion. Patients who have had a prosthetic replacement using the posterior approach, whether a total hip arthroplasty or a hemiarthroplasty, are limited to 90 of hip flexion for six weeks. In addition, hip adduction and internal rotation are contraindicated. These patients are instructed to keep their legs apart and to place a pillow between their legs when lying on the uninjured side to prevent hip adduction, which could lead to prosthetic

370 Idjadi et al. dislocation. Conversely, external rotation and extension are contraindicated if the procedure was performed using an anterior approach. C. Weight Bearing as Appropriate Gait training is initiated on the first or second postoperative day. The major- ity of patients who have been surgically treated with either internal fixation or prosthetic replacement, should be allowed to bear weight as tolerated. Although in the past, partial weight bearing was frequently utilized, we now understand that a weight bearing as tolerated protocol is appropriate. It has been shown that even partial weight bearing involves the generation of considerable force across the hip by the lower extremity musculature. The forces exerted across the hip when a patient uses his upper extremities to transfer onto a bedpan approach four times body weight (38). Studies have also demonstrated that unrestricted weight bearing does not increase complication rates following internal fixation or prosthetic replacement after femoral neck or intertrochanteric fracture (39–44). It has also been suggested that early full weight bearing helps rehabilitation and discharge of patients (45–47). Furthermore, with gait analysis, it has been shown that patients that are allowed to bear weight as tolerated after femoral neck or intertrochanteric fractures, will self limit the loading of the injured limb. Specifically, patients who underwent internal fixation of an unstable inter- trochanteric fracture or a displaced femoral neck fracture, initially placed significantly less weight on the injured extremity than patients who sustained a femoral neck fracture which was treated with prosthetic replacement (48). Over time, the patients progressed their weight bearing to full status. With regards to total hip arthroplasty, weight-bearing status is again dependent on many variables. In general, cemented or hybrid total hip arthroplasty patients are allowed weight bearing as tolerated in the early postoperative period (49). In uncemented total hip arthroplasty, the weight-bearing recommendations are a bit more complex. In light of the fact that early weight bearing may lead to movement at the bone–prosthesis interface and thereby inhibit bone ingrowth (50), limiting the weight bearing in these patients has been suggested. However, there is no general agreement on this. Many surgeons will allow full weight bearing following noncemen- ted arthroplasty. However, later weight bearing has been shown to have detrimental effects on gait, hip extension, and strength (51–53). Although by 24 weeks after surgery, no significant functional consequences persist (54). The goal of weight bearing as tolerated (WBAT) ambulation, follow- ing internal fixation or arthroplasty, might be modified if fixation stability is compromised or if an intraoperative fracture occurred, requiring additional fixation. Although older patients are allowed to weight bear as tolerated, regardless of fracture pattern or implant selection, weight bearing may be limited in younger patients who sustain a displaced femoral neck or unstable

Posthip Fracture and Hip Replacements 371 intertrochanteric fracture. Limited weight bearing is much better performed and tolerated in younger patients than older patients, although there is no data as yet to confirm a beneficial effect in outcome. Younger patients are restricted to foot-flat weight bearing until there is radiographic evidence of healing—unless the fracture was stabilized with an interlocked nail and bone-to-bone contact was achieved at surgery. If there is no contraindication to unrestricted weight bearing, patient’s goals are set to ambulate weight bearing as tolerated 15 ft with moderate assistance on postoperative day 1, progressing to 20 ft with minimal assis- tance on day 2 and 40 ft on day 3. On postoperative day 3 or 4, the patient is instructed in stair climbing with maximal supervision. Subsequent patient goals include progression of ambulation to crutches as tolerated and progression of stair climbing with decreased supervision. These goals are to be taken as general guidelines. Every patient’s rehabilitation program must be tailored to the individual’s physical, psychological, and social situation. D. Adaptive Equipment Adaptive equipment and assistive devices are routinely prescribed for patients to aid in gait performance. These devices are used to increase stabi- lity and lower the weight bearing forces across the operative extremity. Stan- dard walkers provide the greatest base of support, however, they tend to be more cumbersome and may be difficult to advance. Though rolling walkers may be moved forward more easily, they should only be prescribed for individuals with sufficient coordination to stop the motion when needed. Axillary and forearm crutches are less cumbersome than walkers and can be used to provide either unilateral or bilateral support. Canes, four- pronged or straight, offer the least degree of stability. However, they are the least cumbersome and therefore the easiest to manipulate. The cane is held in the hand opposite the impaired side. Ambulatory status, as it pertains to the use of assistive devices and functional domain (community vs. household), has been studied in patients with hip fractures. In general, it has been found that the majority of patients lose at least one level of ambulatory function after sustaining a hip fracture. For example, if a patient was a community ambulatory without an assistive device preinjury, they may require a walking aid postoperatively. Likewise, if a patient was a community ambulator with an assistive device preinjury, they may become a household ambulator postoperatively (12). Similarly, other studies have found that increased dependence (>50%), in lower extre- mity physical activities of daily living such as walking 10 ft, walking one block, and climbing five stairs, persists at two year follow up. Perhaps the most striking finding was a new dependency (>89%) in climbing five stairs at one year, for patients who required no prefracture assistance (55).

372 Idjadi et al. Assistive devices benefit patients with regards to stability and safety. However, it has been shown that their use may be detrimental to gait and muscular training in some patients following total hip arthroplasty. In one study, though patients with crutches walked more symmetrically and with a longer stride length, they reduced the activity of pelvi-trochanteric muscles and abductor muscles on the operative side, thus adversely affecting rehabilitation of these groups (56). Others have also found that the prolonged use of crutches may inhibit function (54). E. Disposition Postoperatively, a social worker should meet with the patient and family to assess the patient’s needs and resources following hospital discharge. The goal of treatment is to return the patient to his or her premorbid level of independence. Depending on the patient’s ambulatory ability, social support network, and financial resources, discharge disposition may be to a variety of settings. Inpatient rehabilitation is a setting where patients may receive intense daily physical and occupational therapy for at least three hours per day. Subacute rehabilitation units provide at least one hour of daily therapy. Skilled nursing facilities offer various degrees of rehabilitation, ranging from little or no therapy to daily sessions. These facilities may function to fine-tune skills learned in an acute rehabilitation program before discharge home. Day hospitals allow individuals with good social support systems to receive a full day of therapeutic activity in a hospital setting while being able to return home at night. Outpatient facilities may offer less comprehensive interdisciplinary therapeutic programs than may be provided on an inpatient basis, yet are ideal for individuals requiring limited rehabi- litative intervention. Finally, physical and occupational therapy can be provided in the home environment where individuals have the opportunity to make functional gains in familiar surroundings until they are sufficiently mobile and independent to progress to an outpatient program. The effect of inpatient rehabilitation on patient outcome and gait function following hip fracture has been examined. In one such study, patients who received two hours of inpatient physical therapy seven days a week for gait training, stair climbing, transfers, joint range of motion, and upper and lower extremity strengthening, were compared to those discharged to an outside rehabilitation facility. No differences were found in the patients’ ambulatory ability at 6- and 12-months follow up (48). Other authors believe that aggressive and intense physical therapy is responsible for the high percentage of independent ambulation that permeated all types of hip fractures as well as surgical treatments (9). Furthermore, other studies have suggested that patients who attended more physical therapy visits had a greater likelihood of returning to prefracture ambulatory status (32).

Posthip Fracture and Hip Replacements 373 Though intuition may suggest that more intense physical therapy would accelerate rehabilitation and subsequent hospital discharge, studies have not confirmed this. In one study, 88 patients with operatively treated hip fractures were randomized to 3.6 hr per week of physical therapy vs. 1.9 hr per week. When using the criteria of: (1) walking 50 m without resting in two minutes, with assistive device if necessary and (2) climbing one flight of stairs, with assistive device if necessary, as well as other nongait functional measures, no difference was noted between the groups with regard to duration of physical rehabilitation. In this case, the findings were thought to be due to the considerable dropout rate in the intervention group. These findings suggested that a focus on out-patient rehabilitation may be in order (57). The results for hip fracture have been mixed with regards to patients that are discharged home and receive standard physical therapy vs. specia- lized home rehabilitation programs. Some have shown increased walking velocity and mobility (58), while others have shown no significant difference in gait performance (59). One study of patients undergoing total hip arthro- plasty showed that a home based perioperative exercise intervention program both before and up to 24 weeks postoperatively yielded patients with greater stride length and gait velocity at three weeks post surgery and greater gait velocity and walking distance at 12 and 24 weeks. Subjects in the intervention program also benefited from a 3 month earlier return of gait function as compared to controls (24). With regard to disposition and postoperative rehabilitation, it is clear that there are a significant number of variables, most of which have not been studied in randomized controlled clinical trials. Thus, the individual, as well as their financial resources and social support systems, should be considered when determining the appropriate disposition and rehabilitation in any given case. VI. SUMMARY Though gait evaluation and treatment for patients who have undergone total hip replacement and the operative treatment of hip fracture is a complex matter, it can be approached in a straightforward manner so that safe, efficient, and effective rehabilitation can be implemented. The goal is to return all patients to their premorbid level of function. Weight-bearing status and precautions should be determined on an individual basis. With the approach discussed above, realistic outcomes may be expected, gait function may be improved, and associated morbidity may be lessened. REFERENCES 1. Cummings SR, Rubin SM, Black D. The future of hip fractures in the United States. Numbers, costs, and potential effects of postmenopausal estrogen. Clin Orthop 1990; 252:163–166.

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