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Preliminary observations of the acute effects of vestibular nerve stimulation on stride length and time in two patients with bilateral vestibular hypofunction
Abstract
Introduction: Bilateral vestibular hypofunction causes balance deficits, increases falls risk and decreases quality of life [1]. Recent work has demonstrated that vestibulo-ocular reflexes [2] and postural responses [3] can be elicited by electrical stimulation via vestibular implants.
Research question: This pilot study aimed to determine if electrical stimulation of the vestibular nerve would result in an immediate change in stride length and time.
Methods: Two female adults (71 and 51 years; P1 and P2 respectively) with bilateral vestibular hypofunction equipped with a vestibular implant [4] participated. The implants electrically stimulate the posterior ampullary branch of the vestibular nerve. Participants were tested under three conditions: after restoration of a constant baseline stimulation [4]; during baseline stimulation modulated by a gyroscope attached to the head, eliciting eye movements in the opposite direction to head movements (positive modulation); and with the gyroscope modulating the baseline stimulation eliciting eye movements in the direction of head movement (negative modulation). Experiments were conducted with the CAREN Extended system (Motekforce Link, Amsterdam, The Netherlands) using a reduced kinematic model (6 markers). The display was fixed (no optical flow) and an object was displayed for visual fixation. The participants firstly completed multiple three-minute familiarisation treadmill walking trials with no stimulation, starting at 0.3 m/s, followed by higher speeds based on ability. Three no-stimulation measurements of three minutes each at self-selected walking speeds (P1: 0.5 m/s; P2: 0.7 m/s) were then conducted. Participants then completed multiple three-minute walking bouts under baseline stimulation and stimulation modulated by positive or negative gain. The final 60 s of the last no stimulation trial and the first of each stimulation conditions were analysed. Results are expressed as mean SD.
Results: Participants showed an increase in stride length under vestibular stimulation, especially in the positive gain condition, compared to no stimulation (P1: 0.54 0.03 m, 0.56 0.03 m, 0.58 0.03 m and 0.57 0.03 m; P2: 0.8 0.04 m, 0.81 0.05 m, 0.91 0.08 m and 0.88 0.04 m for no-stimulation and baseline, positive and negative gain stimulation respectively). Stride time increased in a similar manner to stride length for both patients, with positive gain showing the greatest difference to no stimulation (P1: 1.11 0.03 s, 1.15 0.03 s, 1.18 0.04 s and 1.16 0.04 s; P2: 1.17 0.06 s, 1.17 0.06 s, 1.34 0.11 s and 1.28 0.06 s).
Discussion: These data suggest that vestibular nerve stimulation via an artificial vestibular implant can acutely alter stride length and time in these patients. Further research is needed to generalise the findings to other patients and to investigate if stability improves when using the vestibular implants.
References [1] Guinand N, et al. Ann. Otol. Rhinol. Laryngol. 2012;121(7):471–7. [2] Perez Fornos A, et al. Front Neurol. 2014;5:66. [3] Phillips C, et al. Exp. Brain Res. 2013;229(2):181–95. [4] Guinand N, et al. ORL 2015;77(4):227–40.
Supplementary resource (1)
... However, further research into the relationships between vestibulopathy, walking speed and gait variability is needed to confirm and expand on these previous findings, as these three previous studies had some potential drawbacks, namely a limited number of gait parameters being analysed (Schniepp et al., 2012), too few strides (Owings and Grabiner, 2003, Hollman et al., 2010, Konig et al., 2014, Riva et al., 2014 for a robust analysis of gait variability (Schniepp et al., 2012, the use of only preferred walking speeds or percentages of preferred walking speeds (ecologically valid, but less control over influencing factors) (Schniepp et al., 2012, small sample size , lack of a healthy control group and the presence of sham vestibular stimulation in the control condition . The study of the severe balance and gait deficits in people with BVP is both important for improving clinical care and for objective quantification of the effects of novel interventions, such as vestibular implants (Guyot et al., 2016, Lewis, 2016. Furthermore, it is fundamental to our understanding of the vestibular contributions to gait and balance control. ...
... Determining meaningful and distinguishing gait parameters in BVP is vital for the development of interventions, as is using tasks that sufficiently replicate the day-to-day challenges of these patients, to determine candidates for intervention and to assess the effect of those interventions. Two promising interventions currently under development and investigation include noisy galvanic vestibular stimulation (nGVS) and vestibular implants (Guyot et al., 2016, Lewis, 2016, Perez Fornos et al., 2017. Discussions of these treatment options can be found elsewhere (Guyot et al., 2016, but it is important to note that both ...
... Two promising interventions currently under development and investigation include noisy galvanic vestibular stimulation (nGVS) and vestibular implants (Guyot et al., 2016, Lewis, 2016, Perez Fornos et al., 2017. Discussions of these treatment options can be found elsewhere (Guyot et al., 2016, but it is important to note that both ...
This dissertation aimed to further our understanding of how old age might affect gait stability and adaptability, with the perspective that this knowledge could improve the effectiveness and specificity of exercise-based falls reduction interventions for both healthy and clinical populations at an increased risk of falls.
Part One of this dissertation reviewed the incidence, causes and consequences of falls among older adults. Humans are living longer than ever before and the percentage of older people in our populations will continue to rise for the foreseeable future. As a result, age-related health risks and disease are becoming a larger and larger burden on our older populations and our societies as a whole. Falls and their consequences are one of the most common risks to health, mobility and quality of life among older adults and the number of injuries and hospital admissions because of falls have been increasing in recent years. In particular, mechanical perturbations such as trips und slips during walking present a significant risk for falls in older adults. Therefore, Part One concluded that examination of the stability and adaptation of gait during such mechanical perturbations may help improve the effectiveness of interventions aimed at reducing falls, by identifying specific mechanisms of gait adaptation that can be exploited.
Part Two of this dissertation examined gait variability and stability during walking tasks targeting predominantly predictive control during unperturbed and perturbed gait. Chapter 2.1 assessed the gait of young and older healthy adults, as well as adults with bilateral vestibulopathy, during multiple walking speeds, to elucidate the potential role of the vestibular system in unperturbed gait control. The findings demonstrated that walking speed significantly affects multiple gait parameters and their variability in all the participant groups, and potentially influences the vestibular contribution to locomotor control. Chapter 2.2 used a sustained resistance perturbation to explore the predictive adaptation of gait to control stability in young, middle-aged and older adults, to investigate how such control might change across the adult lifespan. Following a certain number of repeated perturbations, the older adults could achieve similar stability values to younger adults, but the rate of adaptation to a sustained perturbation was found to be slower in the older adults.
Part Three of this dissertation examined methodological aspects of reactive gait stability assessment using perturbations and how we might improve our experimental procedures to better understand how people control and adapt their gait on exposure to unexpected perturbations. Chapter 3.1 reviewed previous studies and their methodologies for examining reactive gait stability during unexpected perturbations in older adults and made suggestions regarding what methodological aspects required further investigation and regarding considerations for future research. In response to the outcomes of the literature review, Chapter 3.2 confirmed that walking speed significantly affects the stability of the body configuration during walking and presented a method to reduce interindividual differences in gait stability prior to experiencing a perturbation, allowing a theoretically more accurate examination of responses to gait perturbations and any subsequent adaptations in gait.
Part Four of this dissertation subsequently applied the improved methodology to examine how young humans adapt, retain and transfer adaptations in gait stability to controlled gait perturbations (Chapter 4.1) and whether or not the processes of adaptation and transfer are altered in older adults (Chapter 4.2). Furthermore, Chapter 4.2 investigated whether or not having young and older participants walk with equivalent gait stability using the methods presented in Chapter 3.2 would lead to different conclusions than those previously reported in the literature regarding age-related differences in gait stability. The results demonstrated that the relationship between walking speed and stability varies from person to person in both young (Chapter 4.1) and older adults (Chapter 4.2) and that older adults could demonstrate interlimb transfer of adaptations to sudden perturbations (Chapter 4.2) when younger adults did not (Chapter 4.1).
Part Five reviewed the literature to examine the characteristics of perturbation-based balance training studies conducted with older adults that assessed prospective falls incidence and discussed several considerations for applying perturbation-based balance training in clinical settings. The results indicated that perturbation-based balance training is a feasible approach to reduce falls risk in healthy and clinical populations and the most feasible methods appear to be treadmill-based systems and therapist-applied perturbations. While more research into specific perturbation characteristics is necessary, using perturbations of multiple types, directions and magnitudes seems advisable based on the reviewed literature.
Part Six of this dissertation discussed the results of all parts of this dissertation within the broader context of exercise-based falls prevention and a number of conclusions were drawn. While improving general muscle strength is important for older adults for several other health and function-related reasons, the gait stability of older adults, and therefore falls risk, is not necessarily drastically improved with enhancements in muscle strength through resistance training. Task specific assessment and training of gait and balance is required in order to gain insight into, and positively influence, the risk of falls in older adults. Despite the strong evidence for these points, future research must continue to explore how to optimise the effectiveness of perturbation-based balance training in terms of retention and generalisability to daily life balance challenges. Other task specific skills such as gait robustness, gait or foot placement adaptability and safe landing techniques may be complimentary to perturbation-based balance training and result in an overall greater effect on falls incidence and fall-related injuries. Several challenges in improving the fall risk of people with bilateral vestibulopathy and other neurological disorders exist related to their residual function and capacity to respond to physical exercise interventions. To this end, the effects of ever-improving technical therapeutic interventions, as well as task specific exercise-based training on balance and gait in these patients should continue to be investigated.
... Two promising interventions currently under development and investigation include noisy galvanic vestibular stimulation (nGVS) and vestibular implants 16,17,[38][39][40] . Discussions of these treatment options can be found elsewhere 16,38 , but it is important to note that both show early signs of utility for improving gait in BVP 4,41 . However, it remains to be seen if improvement due to nGVS or a vestibular implant in steady state gait would likewise be seen in more dynamic locomotor task performance, where even unilateral vestibulopathy leads to significantly poorer stability performance 42 . ...
Understanding balance and gait deficits in vestibulopathy may help improve clinical care and our knowledge of the vestibular contributions to balance. Here, we examined walking speed effects on gait variability in healthy adults and in adults with bilateral vestibulopathy (BVP). Forty-four people with BVP, 12 healthy young adults and 12 healthy older adults walked at 0.4 m/s to 1.6 m/s in 0.2 m/s increments on a dual belt, instrumented treadmill. Using motion capture and kinematic data, the means and coefficients of variation for step length, time, width and double support time were calculated. The BVP group also completed a video head impulse test and examinations of ocular and cervical vestibular evoked myogenic potentials and dynamic visual acuity. Walking speed significantly affected all gait parameters. Step length variability at slower speeds and step width variability at faster speeds were the most distinguishing parameters between the healthy participants and people with BVP, and among people with BVP with different locomotor capacities. Step width variability, specifically, indicated an apparent persistent importance of vestibular function at increasing speeds. Gait variability was not associated with the clinical vestibular tests. Our results indicate that gait variability at multiple walking speeds has potential as an assessment tool for vestibular interventions.
... For the eVOR, frequency-dependent behavior was detected for a broad frequency range and was found to be similar to the natural frequency dependency of the angular vestibuloocular reflex (aVOR) [van de Berg et al., 2015;Guinand et al., 2017]. Furthermore, the VCR could be evoked and improvements of the dynamic visual acuity and gait were established [Guyot et al., 2011b;Perez Fornos et al., 2014;Pelizzone et al., 2014;van de Berg et al., 2015;Guinand et al., 2015bMcCrum et al., 2016;Nguyen et al., 2016Nguyen et al., , 2017Perez Fornos et al., 2017;van de Berg et al., 2017] ( Table 2). The variability in artificially evoked vestibular responses can be partially explained by the neural convergence as both the artificially and naturally stimulated neurons can provide information to the convergent neurons [Curthoys and Markham, 1971;Markham and Curthoys, 1972;Kushiro et al., 2000;Zhang et al., 2001Zhang et al., , 2002Goto et al., 2004;Uchino et al., 2005Uchino et al., , 2011. ...
Background:
In patients with bilateral vestibulopathy, the regular treatment options, such as medication, surgery, and/or vestibular rehabilitation, do not always suffice. Therefore, the focus in this field of vestibular research shifted to electrical vestibular stimulation (EVS) and the development of a system capable of artificially restoring the vestibular function. Key Message: Currently, three approaches are being investigated: vestibular co-stimulation with a cochlear implant (CI), EVS with a vestibular implant (VI), and galvanic vestibular stimulation (GVS). All three applications show promising results but due to conceptual differences and the experimental state, a consensus on which application is the most ideal for which type of patient is still missing.
Summary:
Vestibular co-stimulation with a CI is based on "spread of excitation," which is a phenomenon that occurs when the currents from the CI spread to the surrounding structures and stimulate them. It has been shown that CI activation can indeed result in stimulation of the vestibular structures. Therefore, the question was raised whether vestibular co-stimulation can be functionally used in patients with bilateral vestibulopathy. A more direct vestibular stimulation method can be accomplished by implantation and activation of a VI. The concept of the VI is based on the technology and principles of the CI. Different VI prototypes are currently being evaluated regarding feasibility and functionality. So far, all of them were capable of activating different types of vestibular reflexes. A third stimulation method is GVS, which requires the use of surface electrodes instead of an implanted electrode array. However, as the currents are sent through the skull from one mastoid to the other, GVS is rather unspecific. It should be mentioned though, that the reported spread of excitation in both CI and VI use also seems to induce a more unspecific stimulation. Although all three applications of EVS were shown to be effective, it has yet to be defined which option is more desirable based on applicability and efficiency. It is possible and even likely that there is a place for all three approaches, given the diversity of the patient population who serves to gain from such technologies.
... Two promising interventions currently under development and investigation include noisy galvanic vestibular stimulation (nGVS) and vestibular implants ( Guinand et al. 2015;Lewis 2016;Perez Fornos et al. 2017;Wuehr et al. 2017). Discussions of these treatment options can be found elsewhere ( Wuehr et al. 2017), but in the context of this study, it is important to note that both options show early signs of utility for improving the gait of people with BVP ( McCrum et al. 2016;Wuehr et al. 2016). However, it remains to be seen if improvement due to nGVS or a vestibular implant in steady state gait would likewise be seen in more dynamic locomotor task performance, where even unilateral vestibulopathy leads to significantly poorer stability performance (McCrum et al. 2014). ...
Study of balance and gait deficits associated with vestibulopathy is important for improving clinical care and is critical to our understanding of the vestibular contributions to gait and balance control. Previous studies report a speed-dependency of the vestibular contributions to gait, so we examined the walking speed effects on gait variability in healthy young and older adults and in adults with bilateral vestibulopathy (BVP). Forty-four people with BVP, 12 healthy young adults and 12 healthy older adults completed walking trials at 0.4m/s to 1.6m/s in 0.2m/s intervals on a dual belt, instrumented treadmill. Using a motion capture system and kinematic data, the means and coefficients of variation for step length, time, width and double support time were calculated. The BVP group also completed a video head impulse test and examinations of ocular and cervical vestibular evoked myogenic potentials and dynamic visual acuity. Walking speed significantly affected all assessed gait parameters. Step length variability at slower speeds and step width variability at faster speeds were the most distinguishing parameters between the healthy participants and people with BVP, and within people with BVP with different locomotor capacities. We observed for step width variability, specifically, an apparent persistent importance of vestibular function at increasing speeds. Gait variability was not associated with the clinical vestibular tests. Our results indicate that gait variability at multiple walking speeds has potential as an assessment tool for vestibular interventions.
New & Noteworthy
Walking speed significantly but differentially affects gait variability in healthy adults and in adults with bilateral vestibulopathy. Gait variability at different speeds distinguishes between participants with and without bilateral vestibulopathy, but also between more and less able walkers with bilateral vestibulopathy. Specifically, for step width variability, an apparent persistent importance of vestibular function at increasing walking speeds was observed. Gait variability was generally not correlated with clinical tests of vestibular function.
Importance People with bilateral vestibulopathy experience severe balance and mobility issues. Fear and anxiety are associated with reduced activity, which can further affect balance and fall risk. Understanding and intervening on falls in this population is essential. The aims of this narrative review are to provide an overview of the current knowledge and applied methods on fall incidence, causes, and injuries in bilateral vestibulopathy.
Observations Eleven articles reporting falls incidence in people with bilateral vestibulopathy were deemed eligible, including 3 prospective and 8 retrospective studies, with a total of 359 participants, of whom 149 (42%) fell during the assessed period. When reported, the most common perceived causes of falls were loss of balance, darkness, and uneven ground. Information on sustained injuries was limited, with bruises and scrapes being the most common, and only 4 fractures were reported. As most studies included falls as a secondary, descriptive outcome measure, fall data obtained using best practice guidelines were lacking. Only 6 studies reported their definition of a fall, of which 2 studies explicitly reported the way participants were asked about their fall status. Only 3 studies performed a prospective daily fall assessment using monthly fall diaries (a recommended practice), whereas the remaining studies retrospectively collected fall-related data through questionnaires or interviews. While most studies reported the number of people who did and did not fall, the number of total falls in individual studies was lacking.
Conclusions and Relevance The findings from this review suggest that falls in people with bilateral vestibulopathy are common but remain an understudied consequence of the disease. Larger prospective studies that follow best practice guidelines for fall data collection with the aim of obtaining and reporting fall data are required to improve current fall risk assessments and interventions in bilateral vestibulopathy.
Currently, there is no evidence of an effective treatment for patients with bilateral vestibulopathy (BV). Their main complaints are oscillopsia and imbalance. Opinions about the impact of BV on their quality of life are controversial, and their handicap is not always recognized, even among otoneurologists. The aim of this study was to objectively assess the health status of BV patients in order to evaluate the need for pursuing efforts toward the development of new treatments.
The short-form health survey (SF-36), the dizziness handicap inventory (DHI), the short falls efficacy scale-international (short FES-I), and an oscillopsia severity questionnaire were submitted to 39 BV patients. The SF-36 scores were compared to the scores of a general Dutch population. The DHI scores were correlated to the oscillopsia severity scores. The short FES-I scores were compared to scores in an elderly population. Residual otolithic function was correlated to all scores, and hearing to SF-36 scores.
Compared to the general Dutch population, the BV patients scored significantly worse on the "physical functioning", "role physical", "general health", "vitality", and "social functioning" SF-36 variables (p < 0.05). The DHI scores were strongly correlated with the oscillopsia severity scores (r = 0.75; p < 0.000001). The short FES-I scores indicated a slight to moderate increase in the patients' fear of falling. No significant score differences were found between BV patients with residual otolithic function and patients with complete BV. There was no correlation between hearing status and SF-36 scores.
The results correlate with our clinical impression that BV has a strong negative impact on physical and social functioning, leading to a quality-of-life deterioration. There is a clear need for a therapeutic solution. Efforts toward the development of a vestibular implant are justified.
- C Phillips
Phillips C, et al. Exp. Brain Res. 2013;229(2):181-95.
Corresponding author. E-mail address: chris.mccrum@maastrichtuniversity.nl (C. McCrum)
Gait & Posture xxx (2016) xxx–xxx
* Corresponding author.
E-mail address: chris.mccrum@maastrichtuniversity.nl (C. McCrum).
- N Guinand
Guinand N, et al. ORL 2015;77(4):227-40.
- A Perez Fornos
Perez Fornos A, et al. Front Neurol. 2014;5:66.