Peripheral neuropathy (PN) is a neurological disorder that involves damage or disease of the peripheral nervous system. Diabetes is one of the most common causes of PN, whereas as many as 23% of cases are idiopathic in nature.1,2 The prevalence of PN in older adults seeking medical care in a community setting has been estimated to be as high as 8%.3 For those with type 2 diabetes mellitus, the prevalence of PN rises to 26.4%.1
Individuals with PN often experience a distal to proximal progression of motor and sensory deficits such as loss of proprioception, muscle weakness, and loss of ankle reflexes.4 The importance of proprioceptive information from the lower limbs in the regulation of postural control has been well established.5,6 Because lower-limb proprioception plays a primary role in postural control, individuals with PN often have difficulty maintaining balance, especially under conditions in which vision or vestibular input is also compromised.7,8 Because of these deficits, individuals with PN demonstrate an increased risk for falling.9–12 Richardson et al.11 reported that lower-limb neuropathy is associated with both single falls and repetitive falling, independent of age. In a group of 60 older adults with diabetes, Macgilchrist et al.10 found a significantly higher incidence of neuropathy among fallers (86%) compared with nonfallers (56%). Furthermore, PN is associated with higher risk (odds ratio, 2.5) for injurious falls in independent older adults.13
To improve balance in individuals with neuropathy, the literature suggests that providing additional or alternative sensory cues may enhance postural control. For example, even light nonsupportive touch or contact with almost any part of the body with normal sensation (e.g., fingertip contact of less than 1 N) has been shown to reduce postural sway.14–16 The literature also suggests that sensory input from more proximal trunk muscles can provide important proprioceptive information.17
One practical strategy for improving sensory input that has been investigated is the use of orthoses or ankle-foot orthoses (AFOs) to augment tactile and proprioceptive input to the foot and the lower leg.18,19 To date, work in this area specific to individuals with PN has been rather limited, although the studies conducted have provided support for this. For example, Rao and Aruin20,21 investigated the effects of a polypropylene posterior leaf spring–type AFO on force plate measures of balance in individuals with neuropathy and demonstrated significant improvements in both sensory organization (i.e., quiet standing with eyes open and eyes closed) and motor control (i.e., randomly moving platform) posturography results. In a more recent study, Rao and Aruin22 evaluated the effects of an AFO that did not provide biomechanical restraint of ankle movement but still provided auxiliary sensory cues and found improvements in several sensory organization test conditions and motor control tests in individuals with diabetic neuropathy. Although these findings are of clinical interest, relatively little is known about how AFOs may influence other more dynamic aspects of balance and gait such as rapid stepping, turning, and transitional movements in persons with PN. Work in other neurological populations have suggested that AFOs have been shown to have potentially positive effects on dynamic actions (e.g., walking in individuals with stroke), providing motivation for the current study.23 Furthermore, we are unaware of any study that has examined the effects of newer-generation carbon composite AFOs in this population, specifically nonarticulated carbon composite AFOs with an anterior shell design. The anterior shell appears to have more surface contact than do traditional leaf-spring designs, suggesting that it may be appropriate for augmenting proprioceptive feedback. Although traditional ground reaction AFOs made of thermoplastic are available and also use an anterior shell, these are heavier and not typically used for individuals with PN.
As with any assistive device, AFOs may have both positive and negative effects on function.23 For example, the sensory feedback provided may improve certain aspects of postural control, but the biomechanical constraints may impair others. Unfortunately, AFOs are frequently prescribed without full consideration of both the potentially positive and negative consequences of their use.
Therefore, the primary goal of this pilot study was to observe the immediate effects of nonarticulated anterior shell carbon composite AFOs on balance and gait in individuals with PN. This study sought to consider both force plate measures of postural control as well as a variety of clinical assessments of functional balance and gait. We hypothesized that the AFOs would improve static measures of postural control, as evident by reduced sway, especially under conditions in which other sensory systems were also compromised. However, we expected to find a decrease in performance on more dynamic measures of balance and gait.
A convenience sample of individuals with PN were recruited from community support groups and through informational fliers distributed to local health care professionals. All subjects had been previously diagnosed with PN by a physician. In addition, the subjects underwent a clinical examination by the researchers before testing to confirm the clinical severity of their neuropathy and ensure that they met the following inclusion criteria: diminished or lost ankle reflexes; diminished vibration sense in the foot; a Semmes-Weinstein aesthiometry (North Coast Medical Inc, Morgan Hill, CA, USA) threshold of 3.84 or greater on the plantar surface of the foot; a minimum ankle range of motion of 5° of dorsiflexion and 10° of plantarflexion; strength of the ankles, the knees, and the hips of 2+ of 5 or greater as determined by manual muscle testing; the ability to walk with supervision for 2 minutes without an assistive device; and no history of AFO use. These inclusion criteria were set in part as an effort to establish that the deficits observed in the individuals tested were in line with the primary goal of the study, being sensory in nature rather than range of motion or strength. Subjects were excluded if they had any other neurological condition, significant pain or deformity of the lower limbs, open wounds of the feet, uncontrolled diabetes, or the presence of any medical condition that would make standing and walking for at least 2 minutes difficult or unsafe.
Sensory thresholds for inclusion were determined by applying Semmes-Weinstein monofilaments to three plantar surface sites (distal phalange of the great toe, fifth metatarsal head and heel), taking care to avoid calloused areas. The monofilaments were applied five times to each site, with a correct response recorded if the subject could identify three of five applications.24 Vibration testing was completed by placing a 128-Hz semiquantitative Rydel-Seiffer tuning fork (US Neurologicals LLC, Poulsbo, WA, USA) to the distal phalanx of each great toe.25 The vibration scale ranges from 0 to 8, with a lower score indicating a greater loss of vibration sense. This was done twice on each toe, with the values averaged.
This study was approved by the institutional review board at the University of Dayton, and all participants gave written consent after being informed of all study procedures.
Each subject was tested during a single session lasting approximately 2 hours. During this session, the subjects completed two test conditions: 1) wearing the provided carbon composite AFOs on both lower limbs and 2) without the provided AFOs (i.e., typical/usual function). The participants were counterbalanced so that half of the participants first completed the AFO condition and the other half completed the no-AFO condition to reduce possible influences of an ordering effect. The subjects were given a break of approximately 10 minutes between test conditions. For each test condition, the participants completed the same series of balance and gait assessments. All of the clinical assessments of gait and balance were completed by the same researcher.
For the AFO condition, the subjects were fit with ToeOFF® (Allard USA, Rockaway, NJ, USA) nonarticulated, rigid carbon composite AFOs, which were worn bilaterally, as shown in Figure 1. The AFOs used an anterior shell design rather than the traditional posterior leaf spring design of many AFOs. The anterior shell design appears to afford more skin surface contact area, which may maximize proprioceptive feedback. Each anterior carbon-fiber shell was lined with a thin fleece-like material for the shell-to-skin contact interface. Five different-sized pairs of these AFOs (extra small through extra large) were available to accommodate the range of participants in this study. These AFOs were worn with provided walking shoes having a moderate sole thickness (approximately 0.4 in), available in a range of sizes to accommodate individuals with foot sizes 5 to 13 (US sizes). For the no-AFO condition, the same shoes were worn for consistency. The subjects wore calf-length cotton sports socks for all testing. Generally, the AFO covered the majority of the anterior shin, reaching approximately the tibial tuberosity.
For the AFO condition, the participants donned the AFOs and were then provided a short adjustment period of approximately 5 minutes. During this time, each participant was led through a variety of movements by the researcher. These movements included ten minisquats, three sit-to-stand transitions, and two 10-m walks. It was thought that this period was enough for the participants to become familiar with what to expect as they moved and to ensure safety, while still being representative of a “new” user with regard to their performance.
Posturography measures were collected first using a three-component force platform (BP5050; Bertec Corporation, Columbus, OH, USA). Posturography assessment was conducted as an objective and sensitive measure for examining postural control under quasi-static conditions (e.g., quiet standing and limits of stability [LOS]), different from the evaluation of dynamic and functional balance and gait tested by the clinical tests. For each posturography testing condition, the participants performed the same tasks in the same order and wore the provided shoes. Quiet-standing balance measurements were made under four sensory conditions: eyes open while standing comfortably on the force plate (EO-Firm), eyes closed on the force plate (EC-Firm), eyes open while standing on a closed-cell foam pad (Airex®; Sins, Switzerland) placed on the force plate (EO-Foam), and eyes closed while standing on the foam pad (EC-Foam).26 Center-of-pressure (COP) data were collected for 20 seconds, with three trials taken for each sensory condition. The subjects stood comfortably, and foot position was marked to ensure consistent placement. The subjects then underwent an LOS test on the force plate, leaning as far forward, backward, left, and right while keeping their feet in place and using an ankle strategy. This was repeated three times.
All force platform data were collected at 1000 Hz, downsampled to 100 Hz and filtered with a fourth-order zero-lag Butterworth filter with a 5-Hz cutoff. For each quiet-standing trial, anterior-posterior COP sway range (A/P sway), medial-lateral COP sway range (M/L sway), and mean velocity were calculated. These measures indicate the amount and speed of the COP displacement, with higher values indicating larger and faster (i.e., less controlled) postural sway. Trials in which the subjects lost balance were excluded from the analysis. Loss of balance was defined as any trial in which a subject’s instability caused him/her to grab on to the support structure (the majority of cases) or be supported by the safety harness or spotter. All successful trials for each condition were averaged. For the LOS test, A/P sway and M/L sway were calculated on the basis of the difference between the maximum COP displacement reached in each direction. All successful trials were averaged.
CLINICAL BALANCE AND GAIT ASSESSMENTS
The participants then performed the Mini Balance Evaluation Systems Test (Mini-BESTest)27 of dynamic balance, which is derived from its longer counterpart, the Balance Evaluation Systems Test (BESTest).28 This clinical test requires the performance of 14 tasks that are rated on the basis of the quality of performance. The tasks include items such as sit to stand, rising on the toes, rapid compensatory stepping, pivot turns, and dynamic gait. Each task is rated on a 3-point scale (0–2), with a maximum total score of 28. A lower score indicates poorer performance. In addition to a total score, four subscores can be calculated that represent different domains of balance including 1) anticipatory postural control (items 1–3), 2) reactive postural control (items 4–6), 3) sensory orientation (items 7–9), and 4) dynamic gait (items 10–14). Test-retest reliability of the Mini-BESTest for older adults with balance disorders, including those with PN, has been shown to be excellent (intraclass correlation coefficient [ICC], 0.96).29 Research has also shown that the minimal detectable change at the 95% confidence level (MDC95) is 3.5 points and the minimally important change (MIC) is 4 points in the same population.29 The Mini-BESTest was chosen because it assesses a variety of dynamic movements that patients are likely to experience in daily life and can be easily administered in a clinical setting without specialized equipment.
Walking speed was calculated for both comfortable and fast-paced walking. This was determined by using a stop watch to measure the time required for each participant to cover the middle 10 m of a 14-m walking course.30 Two trials at each pace were recorded and averaged. During the fast-paced walking, the participants were given the instruction to “walk as fast as you possibly can while remaining safe.” Walking speed has been shown to have excellent test-retest reliability in older adults (ICC, 0.96–0.98).31 Minimally important change values ranged from 0.05 to 0.10 m/s for a mixed group of older adults including those with and without mobility deficits.31 Both normal and fast-paced walking were tested to represent a range of speeds that might be experienced in the community setting.
Finally, the Timed Up and Go (TUG) was performed, which involves recording the time required for the participant to stand from a standard arm chair, walk 3 m around a cone, and sit back down in the chair using their preferred assistive device.32 The mean time from two trials was recorded. This test has excellent test-retest reliability (ICC, 0.99) in older adults32 but has not been reported for PN. Minimally important change and MDC values for the TUG have also not been established for individuals with PN, but previous studies have reported MDC values of 3.5 and 4.1 seconds in individuals with Parkinson and Alzheimer disease, respectively.33,34
Descriptive statistics were calculated for the demographic and clinical characteristics of the participants. Data were assessed for normality using the Shapiro-Wilk test. Paired t-tests (two tailed) were used to assess differences in the force plate measures of postural control, gait speed, and the TUG between the two conditions (AFO vs. no AFO). The Wilcoxon signed rank test was used to compare differences in the nonnormally distributed and ordinal data provided by the Mini-BESTest and its subscales. Because of the exploratory nature of this study and the use of outcomes measures that were selected to assess different domains of balance and gait, a correction for multiple tests was not applied. All analyses were performed using SPSS version 18.0 (IBM, Armonk, NY, USA), with the critical α set at 0.05. When appropriate, changes in performance were also compared with known MIC values for the Mini-BESTest, gait speed, and TUG.
A total of 15 subjects were screened over the telephone for eligibility. Thirteen participated in the initial physical examination, and one subject was eliminated because his sensation was not sufficiently impaired. All eligible subjects completed the testing procedures without incident. Subject characteristics for the 12 subjects who participated in this study are given in Table 1. The mean (SD) from all six sites tested using the monofilaments was 5.59 (1.03), which indicates severe sensory impairment with loss of protective sensation (Table 1). The results of the vibratory testing indicated that seven of our subjects had no vibration sense, whereas the others had a mean (Sd) of 0.98 (1.41) (Table 1).
Table 2 provides the mean values for each parameter without AFOs and with AFOs for each testing condition. For all conditions other than EC-Foam, the mean values of all sway parameters were higher in the no-AFO condition as compared with the AFO condition, with larger sway ranges and faster speed of sway indicative of poorer postural control. The only statistically significant differences between the no-AFO and the AFO condition occurred in the EC-Firm condition. In this condition, while wearing AFOs, the subjects swayed significantly less in the A/P and M/L as compared with not wearing the AFOs (p = 0.012 and p =0.048, respectively). In the EC-Foam condition, all measures were higher when the AFOs were worn as compared with when they were not, indicating poorer performance; however, this could be an artifact of the high prevalence of the subjects who lost balance in this condition. Eight of the 12 subjects lost balance on at least one EC-Foam trial, with 2 subjects losing balance on all three no-AFO trials and another 2 losing balance on all three AFO trials.
LIMITS OF STABILITY POSTUROGRAPHY
While wearing the AFOs, the subjects leaned significantly less in the A/P direction than when they were not wearing the AFOs (p = 0.000). The LOS in the medial-lateral direction were also reduced in the AFO condition, but this difference was not statistically significant (p = 0.159).
CLINICAL BALANCE AND GAIT ASSESSMENTS
Table 3 displays the results of the clinical balance and gait measures. No significant differences (p > 0.05) were identified between the AFO versus the no-AFO condition for any of the measures. However, four subjects demonstrated changes in their total Mini-BESTest scores that equaled or exceeded the MIC value of 4 points when wearing the AFOs. Subjects 2 and 6 demonstrated an 8- and 4-point improvement, respectively, whereas subjects 3 and 9 showed a 6- and 5-point decrease in performance, respectively. For comfortable gait speed when wearing the AFOs, subject 9 showed a decrease in gait speed of 0.13 m/s whereas subject 10 had a 0.13-m/s increase, which are similar to known MIC gait speed values.
While wearing AFOs, the subjects swayed less and more slowly in the A/P and M/L directions during the EO-Firm, EC-Firm, and EO-Foam conditions. Although these findings indicate an improvement in postural control, they were statistically significant only in the EC-Firm condition for the measures of A/P and M/L sway range. Because individuals with PN tend to have more difficulty maintaining balance when visual input is also compromised, the significant improvements for this condition were somewhat expected.7,8 The additional somatosensory cues to the lower leg and biomechanical support provided by the braces are likely the reason that sway was reduced. Future work is needed to determine whether these improvements would translate to improved function or a decrease in fall risk.
In contrast to the improved postural control for the posturography conditions above, the EC-Foam condition resulted in an increase in sway while wearing the AFOs, although this difference was not statistically significant. These results should be interpreted with caution because of the number of trials that and the number of subjects who had to be removed from analysis because of losses of balance. Because only successful trials were analyzed, this reduced the sample size from 12 to 8 for this condition. However, from a purely observational and clinical perspective, the fact that more individuals experienced a loss of balance when using the AFOs on the foam indicates that clinicians may want to carefully evaluate patient responses on softer surfaces such as thick carpeting and grass, especially when vision is compromised. It is possible that the additional ankle strategies and movements that are required to adapt to unstable and uneven surfaces were limited by the biomechanical constraints imposed by the braces. It could also be that individuals with PN under these most challenging conditions have postural deficits that are most pronounced in this condition, and the AFOs do not provide enough tactile help to make notable changes. Future work is needed to explore this further.
The quiet-standing results of this study suggest that the use of AFOs has an immediate positive impact on static postural control except on unstable surfaces when vision is compromised. These findings are in general agreement with the work of Rao and Aruin,21,22 who also found significant but even greater and more consistent improvements in individuals with diabetic neuropathy while wearing AFOs. This may be due to differences in the testing methodology and reporting because Rao and Aruin used the EquiTest® (NeuroCom International Inc, Clackamas, OR, USA), which uses a single-axis (sagittal plane) rotating platform rather than foam for the unstable surface conditions. In addition, in their 2011 study,22 subjects used an articulated AFO that reduced the biomechanical restrictions at the ankle and would likely influence performance, especially during the unstable and dynamic surface conditions.
LIMITS OF STABILITY POSTUROGRAPHY
The results from the LOS testing suggest that the AFOs significantly restrict the ability to lean, which is generally undesirable. While wearing the AFOs, the subjects were able to lean, on average, approximately 2 cm less in the A/P direction, a notable and significant difference. This could have implications for functional tasks, such as making it more difficult to reach forward to a high cabinet. In an attempt to offset the biomechanical restrictions imposed by traditional AFOs, Rao and Aruin22 evaluated an articulated AFO with a semirigid element that did not restrict sagittal ankle motion and found improvements in dynamic postural responses associated with unexpected forward and backward translations of a force plate. They speculated that these improvements were primarily due to the auxiliary sensory cues provided around the shank and calf area. On the basis of this finding, the trade-offs between providing biomechanical support versus restrictions to normal movement should be considered when prescribing AFOs.
CLINICAL BALANCE AND GAIT ASSESSMENTS
No significant differences or trends were identified between the AFO conditions for the clinical balance and gait assessments. We had originally hypothesized that there would be a decrease in performance for the AFO condition on the more dynamic tests such as the Mini-BESTest, the TUG, and gait speed. This prediction was based on the assumption that, although the AFOs may provide additional sensory feedback, they would also restrict ankle motion necessary during dynamic gait and balance tasks. It was also assumed that, because the subjects were given limited opportunity to adapt to the AFOs, they would have difficulty with new movement strategies that may be needed to use AFOs effectively.
Although no significant differences or obvious trends were identified between the conditions, there was variability in performance for individual subjects that could be considered clinically important. For example, several subjects demonstrated positive and negative changes in the balance and gait assessments that exceeded known MIC values. For the Mini-BESTest (MIC, 4), two subjects demonstrated 8- and 4-point improvements in their total scores in the AFO condition as compared with the no-AFO condition, with most of those improvements coming from the dynamic gait subscore (5 and 2 points, respectively). Conversely, two subjects demonstrated 6- and 5-point decreases in total scores in the AFO condition as compared with the no-AFO condition, with one subject showing the greatest change in the reactive postural control subscore (−3 points); and the other, in the dynamic gait subscore (−2 points). The effects on gait speed were also mixed, with one subject experiencing an increase (+0.13 m/s) in the AFO condition as compared with the no-AFO condition and another subject experiencing a decrease (−0.13 m/s) in comfortable gait speed that exceeded MIC values (0.10 m/s). These findings indicate that the effects of the AFOs were more variable for the most dynamic components of the Mini-BESTest as well as gait speed and should be considered when evaluating the effects of AFOs on individual patients. A review of the subjects who had positive or negative responses to the AFOs did not reveal any obvious characteristics that might explain or predict this response. Because of the small sample size of the study, further statistical exploration of possible covariates was not possible.
In interpreting the findings of the clinical tests requiring dynamic movements and balance as compared with the LOS posturography testing, it is important to note key differences in the testing methodology that may explain the differences observed in the results. The LOS testing requires the individual being tested to isolate and use only an ankle strategy in his/her movements. In contrast, the Mini-BESTest allows subjects to be much freer in their movements, and subjects may use other compensatory actions. Therefore, it is not necessarily surprising that the LOS posturography results indicated that AFOs significantly affected ability to lean, whereas similar trends were not observed in the clinical tests, likely because compensatory actions were being taken to counteract the increased rigidity and restriction at the ankle.
CLINICAL AND RESEARCH IMPLICATIONS
Despite the limitations of this small pilot study, there are several clinical implications worth noting. First, when wearing the AFOs, two subjects demonstrated an immediate decrease in dynamic balance that could lead to at least a temporary increase in fall risk. Given this fact, individuals with PN who are prescribed AFOs may benefit from some type of standardized dynamic balance testing (e.g., Mini-BESTest) that allows the clinician to assess the immediate impact of the AFOs and to evaluate adaptations over time. In addition, by assessing performance on the subcomponents of dynamic balance tests such as the Mini-BESTest, clinicians can make more specific and informed recommendations about activities that should be approached with caution when acclimating to AFO use.
This pilot study may also have implications for future research. For example, larger trials of this nature may allow for identification of specific patient characteristics that may predict favorable or unfavorable responses to AFOs. Future studies that assess changes in balance and gait performance at regular intervals during a period of adaptation to AFOs could be beneficial in determining the importance and contribution of motor learning in the process.
In this pilot study, we found that individuals with PN wearing carbon composite AFOs for the first time had immediate improvements in static postural control but had more variable responses during dynamic balance and gait activities. Clinicians should consider performing standardized assessments that include a variety of dynamic balance and gait activities when prescribing AFOs to individuals with PN to determine both immediate and long-term responses.
The authors thank Mark Horowitz, CPO, LPO, clinical director of the Hanger Clinic (Dayton, OH, USA), for his expertise and consultation and Allard USA Inc (Rockaway, NJ, USA) for providing the ToeOFF® ankle-foot orthoses used in this study. The authors thank Lindzi Hoersten and Victoria Wawzyniak for assistance with data analysis.
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