Otology & Neurotology 38:1327–1332 ß 2017, Otology & Neurotology, Inc.
The Effect of Hearing Aids and Cochlear Implants on Balance During Gait Tyler S. Weaver, Corey S. Shayman, and Timothy E. Hullar Department of Otolaryngology–Head & Neck Surgery, Oregon Health & Science University, Portland, Oregon
Hypothesis: Auditory input in people with hearing impairment will improve balance while walking. Background: Auditory input is increasingly recognized as an additional input for balance. Several studies have found auditory cues to improve static balance measured on a sway platform. The effect of audition on gait, a dynamic task also linked to fall risk, has not been fully examined. If a positive effect were shown between audition and balance, it would further indicate that improving hearing could also improve balance. Methods: Inertial sensors quantified gait parameters of 13 bilateral hearing aid users and 12 bilateral cochlear implant (CI) users with their hearing devices on and off. Outcome measures included gait velocity, stride length variability, swing time variability, and double support phase. Results: Group analysis of each of the gait outcomes showed no significant differences between the aided and unaided
conditions in both the hearing aid and CI groups. Gait velocity, an outcome most strongly linked to fall risk had 95% confidence interval differences of 2.16 to 1.52 and 1.45 to 4.17 cm/s in hearing aid and CI users, respectively (aided versus unaided condition). There was considerable variation among participants with some individuals improving in all four parameters. Conclusion: The overall findings were not statistically significant, however, a small subset of our population improved clinically across several outcomes. This demonstrates that audition may have a clinically beneficial effect on balance in some patients. Key Words: Balance—Cochlear implant— Fall—Gait—Hearing aid—Hearing loss—Presbycusis— Presbystasis—Sensory reweighting—Vestibular.
Every year, one-third of community-dwelling elderly over 65 will have a ground level fall (1,2), which can lead to injuries including intracranial bleeds and hip fractures, the latter which are associated with a 17% all-cause mortality risk within 6 months (3). A recent, growing body of evidence suggests that audition provides a fourth input for balance in addition to the traditionally recognized visual, vestibular, and proprioceptive inputs (4–8). Some studies have further indicated that hearing-impaired subjects receive a balance benefit from hearing aids (8–10). This finding is particularly important, because if sustained it would indicate that treating hearing loss would also improve balance. Almost exclusively, studies examining the effect of audition on balance have relied on static measures of balance by quantifying stability while standing still,
which have been linked to fall risk (11,12). However, gait performance is at least as important as static balance. Tripping is the underlying cause for the majority of falls (2). Decreases in dynamic balance performance, especially gait, are linked to increased risk of falling (13–15). The only study looking at the effect of audition on gait at this point is a small case series showing hearing assistive devices to be of clinical utility in improving dynamic balance tasks (16). Given the importance of dynamic balance to healthy aging, and the link between hearing loss and falling (2.39 times more likely (17)), this prospective study aimes to assess if dynamic gait parameters change when hearing aids and cochlear implant (CI) processors are worn.
Address correspondence and reprint requests to Timothy E. Hullar, M.D., Department of Otolaryngology–Head & Neck Surgery, Oregon Health and Science University, 3181 SW Sam Jackson Park Road, Mail Code PV-01, Portland, OR 97239; E-mail: [email protected] Financial Disclosures: T.E.H.: Med-El as surgical consultant, Advanced Bionics as surgical consultant. Disclosure of Funding: American Hearing Research Foundation grant, Award #1010372. The authors disclose no conflicts of interest. DOI: 10.1097/MAO.0000000000001551
This study was performed with the approval of the OHSU Institutional Review Board. Potential participants were recruited via the audiology department’s schedule and via flyers at nearby retirement communities. Inclusion criteria consisted of an age at least 18 years old, able to understand English, not be cognitively impaired according to the Short Blessed Test, able to ambulate independently without a cane or walker, able to perform a Romberg test on a solid surface with eyes closed for 30 seconds, and participants had been using their hearing aid
Otol Neurotol 38:1327–1332, 2017.
MATERIALS AND METHODS Participants
1327
Copyright © 2017 Otology & Neurotology, Inc. Unauthorized reproduction of this article is prohibited.
1328
T. S. WEAVER ET AL.
devises for over 3 months. An hourly payment was provided to the participants. Participants were informed simply that the present study was to evaluate hearing’s potential influence on balance. When available, audiograms were extracted from the clinical record; otherwise, a screening audiogram was completed (Beltone, Glenview, IL). Unaided thresholds for all participants were worse than 30 dB in the better hearing ear. All hearing aid (HA) participants were in the normal range with instrumented hearing. All CI participants had severe to profound hearing loss bilaterally, and could hear the testing stimulus while wearing their speech processors. Participants were asked before and after testing ‘‘Do you feel that your balance is better with your hearing devices on, off, or is there no difference?’’ All participants removed their shoes, wore a gait belt, and were closely spotted.
Test Conditions Participants wore three Opal inertial sensors (APDM, Portland, OR), one at midline of the lumbar region and one at each ankle region and inertial data were analyzed via Mobility Lab (APDM, Portland, OR) and MatLab (MathWorks, Natick, MA) software. Opal sensors (3 3 cm) consist of a 6-degree of freedom accelerometer, gyroscope, and magnetometer. Inertial sensors of this type produce measurements that have been validated with sway center of pressure measures in static conditions (18,19) and dynamic gait output measures (20). They have also been related to increased fall risk (21). In a large, open, quiet (background noise 50 years old) in the CI group again showed no effect of audition. There was considerable variation among participants. For example, participant CI-110, showed improvement in all parameters, including gait velocity that met the minimal clinically important difference (MCID) at 0.10 m/s (23). Other participants showed mixed outcomes with the hearing intervention (Fig. 2). DISCUSSION Gait Comparison The data presented here do not confirm that auditory input provides a significant benefit to gait parameters, in either HA or CI patients. This is different than the
Otology & Neurotology, Vol. 38, No. 9, 2017
Copyright © 2017 Otology & Neurotology, Inc. Unauthorized reproduction of this article is prohibited.
EFFECTS OF HA AND CI ON BALANCE Gait outcomes
TABLE 2.
Hearing Aid Users Gait Parameter Gait velocity (m/s) Stride length variabliity (CoV) Swing time variability (CoV) Double support phase (%)
Mean 95% confidence Mean 95% confidence Mean 95% confidence Mean 95% confidence
interval interval interval interval
1329
Cochlear Implant Users
HA On
HA Off
p
Processors On
Processors Off
p
0.794 0.643–0.946 0.057 0.043–0.071 0.039 0.029–0.049 24.30 20.13–28.47
0.813 0.656–0.970 0.052 0.042–0.063 0.037 0.028–0.045 23.95 19.86–28.03
0.190
0.750 0.627–0.864 0.050 0.040–0.060 0.052 0.038–0.065 28.16 23.83–32.49
0.737 0.609–0.864 0.055 0.040–0.070 0.055 0.036–0.073 28.59 23.22–33.95
0.424
0.348 0.269 0.216
0.175 0.622 0.622
HA indicates hearing aids.
conclusion of the only previous study examining the effect of audition on gait, a case series showing improvements in three patients (16). There were several important differences between the present study and that report. Most notably, the three patients in the case series had vestibular deficits unlike all of the participants in this present study (normal vestibular history and a normal 30-s Romberg). Another notable difference is the sound stimulus. Shayman et al. used a ‘‘wall of sound’’ made up of multiple treadmills along the length of the walking track, as opposed to the single point source noise at the end of the track used here (16). The third major difference was the method in which data were quantified. In the previous study a GAITRite Strip (CIR Systems, Sparta, NJ) was used to measure foot position while walking but inertial sensor instrumentation of gait was used here. Inertial sensors are limited by less robust correlation with falls and require output data to be processed into meaningful gait parameters. Despite these limitations, postural sway, as measured by inertial sensors, has been validated with platform sway measures (18,19). Gait parameters derived from these sensors have also been correlated with fall risk, demonstrating a wide range of sensitivity (35–100%) and specificity (55–99%) for fall risk (21). Importance and Complexity of Gait Despite our inability to identify a definite influence of audition on gait, the potential medical significance of this effect indicates further study as the majority of falls occur during ‘‘tripping’’ rather than standing still (2). In the case of our data, given the complexities of walking, gait measures are subject to great variability. This may obscure small but important differences in individual people. Conceivable differences could be identified in larger prospective studies or by further development of other stimulus environments and/or measuring techniques. Static Balance in Individuals With Normal Hearing As a whole, studies investigating the effect of audition on static balance have supported the conclusion that audition has a small but identifiable effect particularly in people with baseline imbalance. Two papers
quantified sway using pressure platforms and measured outcomes in terms of center of pressure in normal hearing subjects. Kanegaonkar et al. (5) reported improvements with sound, although these were between subjects with ear defenders on versus off in the absence of salient sound and, presumably, they had very similar auditory environments. Another study used infrared position sensors to compare head sway in normal hearing subjects when a white noise sound source was on versus off. Their findings were largely positive, although the relationship between their outcome variable (head sway) and overall postural stability is not quantified (7). Static Balance in Individuals With Hearing Impairment Patients with hearing loss have also shown improvement on static measures. While Rumalla et al. (9) showed a striking finding with respect to auditory influence on static balance in hearing loss, Vitkovic et al. (10), using a force plate, demonstrated a much subtler result. Rumalla et al. (9) demonstrated a consistent group of hearing aid users were at lower fall risk when they were wearing their aids in the presence of sound. Rumalla et al. (9) exchanged range-of-motion outcome measures in favor of linking fall risk to time standing on foam. This technique may be a good way to quantify balance, as ultimately it is the risk of falling, rather than sway, which is most clinically important. In a study analyzing balance effects of cochlear implantation by Buchman et al. (24), subjects were reported to significantly improving on platform posturography with processors on compared with off, as early as 5 months postimplant. A report indicated similar findings in one case of single-sided deafness treated with a cochlear implant (25). Individuals Showing Benefit Overall, one way to interpret the static and dynamic data is that a certain subset of individuals can supplement their balance with abstract auditory input, although not all participants may benefit from sound. In this study, one CI participant (CI-110) showed robust improvements in all gait measures when wearing her speech processors. A few others showed benefit to a lesser degree (CI-108, CI-111, CI-115, HA-122), although there is no shared Otology & Neurotology, Vol. 38, No. 9, 2017
Copyright © 2017 Otology & Neurotology, Inc. Unauthorized reproduction of this article is prohibited.
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T. S. WEAVER ET AL. characteristic that could predict the performance of this group. Another study found that auditory benefit was not equally accessible among participants. Stevens et al. (8) examined a heterogeneous group, comprised of patients with normal and impaired hearing. Using a NeuroCom force platform (NeuroCom International Inc, Clackamas, OR) the study quantified a larger speed of center of pressure in the absence of sound when compared with the presence of white noise. Interestingly, in that study, the findings seem to be driven by four ‘‘top performers’’ who seem to be the most imbalanced, and the remaining subjects may not show clinically relevant improvements with sound. The gait case series by Shayman et al. (16), including patients only with documented vestibulopathies, shows one of the three subjects with a larger benefit. Given that top performers in other studies had baseline vestibulopathies, and our current study excluded vestibulopathic participants, it may be that a baseline vestibular loss is a major factor determining who will benefit. Aside from this, the current study does not give further insight as to which individuals can benefit from sound. This question should be given future consideration given the very important benefit potentially available to those at risk of fall. The presence of audition may have the ability to influence a population that relies on auditory input. Recent sensory integration studies have shown an upweighting on auditory reliance when other inputs (visual and proprioceptive) are removed (6). This is supported by general sensory reweighting principles (26). Reweighting of senses is thought be greater if it occurs earlier in development (27). Easton et al. (4) examined audition’s influence on balance in people with congenital blindness, although the study showed a similar effect of sound on balance in sighted and blind subjects.
FIG. 1. Slope graphs of gait outcomes arranged by outcome measure. Solid lines represent cochlear implant users and dotted lines represent hearing aid users. A, Gait velocity, measured in cm/s. B, Stride length variability, measured by standard deviation divided by mean, without units. C, Swing time variability, measured
Effect of Task A modified Fukuda step test has also been used to measure the effect of sound on balance (7). This test consists of the subject marching in place for 100 steps with their eyes closed. In that report, there was some improvement in angular deviation with a sound stimulus relative to a silent condition. Although the Fukuda test might be considered a test of navigation rather than strictly stability, this should not detract from its importance as a measure of balance-related disability. In fact, many vestibular-deficient patients complain strongly of a tendency to veer while walking, typically toward the affected side. Veering can severely limit daily activities and affect quality of life. Whether or not auditory supplementation to balance can be linked to a reduction in fall risk, its effect on veering while walking may still be benefit to the listener. Rumalla et al. (9) suggested sound localization as one potential mechanism. In a static task, listeners must by standard deviation divided by mean, without units. D, Double support phase, measured by percent of time in gait cycle with both feet planted.
Otology & Neurotology, Vol. 38, No. 9, 2017
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EFFECTS OF HA AND CI ON BALANCE
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FIG. 2. Gait outcomes arranged by participant, left to right (within participant), gait velocity, stride lengthy variability, swing time variability, double support phase. Percent change calculated by (value in aided/value in unaided) 1. Positive value denotes improvement in the aided condition relative to the unaided.
simply adjust their posture to maintain the localization information (such as loudness level in each ear) constant. This automatically keeps them in a stable position. Furthermore, in some static studies (5,9), data were collected in a sound booth further isolating and enhancing the information available from the sound source. For a dynamic task such as the one reported here, localization cues such as loudness constantly change as the listener advances toward the auditory source. Localization cues are therefore less reliable and therefore less useful for maintaining stability. Another reason that the effect of audition on balance may be more apparent in static balance studies is that measuring stability is relatively simple (quantifying center of pressure on a balance platform, e.g.) but measuring balance as a subject moves (such as measuring movement of individual body segments) is much more complicated and small changes may be missed. Additional Static Balance Studies A few studies have reported auditory input having no effect on balance in normal hearing populations. Soames and Raper (28) examined the ability of auditory input
(pure tones and conversation) to affect balance via a force platform. Although they describe a difference, especially in sound from the right side, their data are inconclusive. In two other studies, Maheu et al. (6) and Chen and Qu (29) found that the presence of sound alone did not affect stability on a force platform, the latter study reporting unpleasant sounds (i.e., vomiting, baby crying) as destabilizing. Given the growing body of evidence suggesting auditory input contributes to balance, these few neutral findings help to support the conclusion that an effect of sound maybe likely be small or helpful only in some circumstances. CONCLUSION Overall, in the HA and CI populations, gait measures linked to fall risk did not differ between aided and unaided listening conditions. Although the overall population findings were not significant, a small subset of our population clinically improved in multiple outcome measures. While a simple hearing intervention may have the possibility to meaningfully supplement balance, this study demonstrates that patient selection may be an important consideration in the degree of benefit. Otology & Neurotology, Vol. 38, No. 9, 2017
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1. Lord SR, Menz HB, Tiedemann A. A physiological profile approach to falls risk assessment and prevention. Phys Ther 2003;83:237–52. 2. Blake AJ, Morgan K, Bendall MJ, et al. Falls by elderly people at home: prevalence and associated factors. Age Ageing 1988;17: 365–72. 3. Marottoli RA, Berkman LF, Cooney LM. Decline in physical function following hip fracture. J Am Geriatr Soc 1992;40:861–6. 4. Easton RD, Greene AJ, DiZio P, Lackner JR. Auditory cues for orientation and postural control in sighted and congenitally blind people. Exp brain Res 1998;118:541–50. 5. Kanegaonkar RG, Amin K, Clarke M. The contribution of hearing to normal balance. J Laryngol Otol 2012;126:984–8. 6. Maheu M, Sharp A, Landry SP, Champoux F. Sensory reweighting after loss of auditory cues in healthy adults. Gait Posture 2017;53: 151–4. 7. Zhong X, Yost WA. Relationship between postural stability and spatial hearing. J Am Acad Audiol 2013;24:782–8. 8. Stevens MN, Barbour DL, Gronski MP, Hullar TE. Auditory contributions to maintaining balance. J Vestib Res 2017;26:433–8. 9. Rumalla K, Karim AM, Hullar TE. The effect of hearing aids on postural stability. Laryngoscope 2015;125:720–3. 10. Vitkovic J, Le C, Lee SL, Clark RA. The contribution of hearing and hearing loss to balance control. Audiol Neurotol 2016;21:195–202. 11. Swanenburg J, de Bruin ED, Uebelhart D, Mulder T. Falls prediction in elderly people: a 1-year prospective study. Gait Posture 2010;31:317–21. 12. Piirtola M, Era P. Force platform measurements as predictors of falls among older people—a review. Gerontology 2006;52:1–16. 13. Verghese J, Holtzer R, Lipton RB, Wang C. Quantitative gait markers and incident fall risk in older adults. J Gerontol A Biol Sci Med Sci 2009;64:896–901. 14. Thaler-Kall K, Peters A, Thorand B, et al. Description of spatiotemporal gait parameters in elderly people and their association with history of falls: results of the population-based cross-sectional KORA-Age study. BMC Geriatr 2015;15:32. 15. Callisaya ML, Blizzard L, McGinley JL, Srikanth VK. Risk of falls in older people during fast-walking—the TASCOG study. Gait Posture 2012;36:510–5.
16. Shayman CS, Earhart GM, Hullar TE. Improvements in gait with hearing aids and cochlear implants. Otol Neurotol 2017;38: 484–6. 17. Jiam NT-L, Li C, Agrawal Y. Hearing loss and falls: a systematic review and meta-analysis. Laryngoscope 2016;126:2587–96. 18. Mancini M, Salarian A, Carlson-Kuhta P, et al. ISway: a sensitive, valid and reliable measure of postural control. J Neuroeng Rehabil 2012;9:59. 19. Neville C, Ludlow C, Rieger B. Measuring postural stability with an inertial sensor: validity and sensitivity. Med Devices Evid Res 2015;8:447–55. 20. Donath L, Faude O, Lichtenstein E, Pagenstert G, Nu¨esch C, Mu¨ndermann A. Mobile inertial sensor based gait analysis: validity and reliability of spatiotemporal gait characteristics in healthy seniors. Gait Posture 2016;49:371–4. 21. Howcroft J, Kofman J, Lemaire ED, et al. Review of fall risk assessment in geriatric populations using inertial sensors. J Neuroeng Rehabil 2013;10:91. 22. Bischoff HA, Sta¨helin HB, Monsch AU, et al. Identifying a cut-off point for normal mobility: a comparison of the timed ‘‘up and go’’ test in community-dwelling and institutionalised elderly women. Age Ageing 2003;32:315–20. 23. Bohannon RW, Glenney SS. Minimal clinically important difference for change in comfortable gait speed of adults with pathology: a systematic review. J Eval Clin Pract 2014;20:295–300. 24. Buchman CA, Joy J, Hodges A, Telischi FF, Balkany TJ. Vestibular effects of cochlear implantation. Laryngoscope 2004;114: 1–22. 25. Jacob R, Stelzig Y. The Koblenz experience in treating singlesided deafness with cochlear implants. Audiol Neurotol 2011;16: 3–25. 26. Assla¨nder L, Peterka RJ. Sensory reweighting dynamics in human postural control. J Neurophysiol 2014;111:1852–64. 27. Lewald J. Exceptional ability of blind humans to hear sound motion: implications for the emergence of auditory space. Neuropsychologia 2013;51:181–6. 28. Soames RW, Raper SA. The influence of moving auditory fields on postural sway behavior in man. Eur J Appl Physiol Occup Physiol 1992;65:241–5. 29. Chen X, Qu X. Influence of affective auditory stimuli on balance control during static stance. Ergonomics 2017;60:404–9.
Otology & Neurotology, Vol. 38, No. 9, 2017
Copyright © 2017 Otology & Neurotology, Inc. Unauthorized reproduction of this article is prohibited.
The Effect of Hearing Aids and Cochlear Implants on Balance During Gait Tyler S. Weaver, Corey S. Shayman, and Timothy E. Hullar Department of Otolaryngology–Head & Neck Surgery, Oregon Health & Science University, Portland, Oregon
Hypothesis: Auditory input in people with hearing impairment will improve balance while walking. Background: Auditory input is increasingly recognized as an additional input for balance. Several studies have found auditory cues to improve static balance measured on a sway platform. The effect of audition on gait, a dynamic task also linked to fall risk, has not been fully examined. If a positive effect were shown between audition and balance, it would further indicate that improving hearing could also improve balance. Methods: Inertial sensors quantified gait parameters of 13 bilateral hearing aid users and 12 bilateral cochlear implant (CI) users with their hearing devices on and off. Outcome measures included gait velocity, stride length variability, swing time variability, and double support phase. Results: Group analysis of each of the gait outcomes showed no significant differences between the aided and unaided
conditions in both the hearing aid and CI groups. Gait velocity, an outcome most strongly linked to fall risk had 95% confidence interval differences of 2.16 to 1.52 and 1.45 to 4.17 cm/s in hearing aid and CI users, respectively (aided versus unaided condition). There was considerable variation among participants with some individuals improving in all four parameters. Conclusion: The overall findings were not statistically significant, however, a small subset of our population improved clinically across several outcomes. This demonstrates that audition may have a clinically beneficial effect on balance in some patients. Key Words: Balance—Cochlear implant— Fall—Gait—Hearing aid—Hearing loss—Presbycusis— Presbystasis—Sensory reweighting—Vestibular.
Every year, one-third of community-dwelling elderly over 65 will have a ground level fall (1,2), which can lead to injuries including intracranial bleeds and hip fractures, the latter which are associated with a 17% all-cause mortality risk within 6 months (3). A recent, growing body of evidence suggests that audition provides a fourth input for balance in addition to the traditionally recognized visual, vestibular, and proprioceptive inputs (4–8). Some studies have further indicated that hearing-impaired subjects receive a balance benefit from hearing aids (8–10). This finding is particularly important, because if sustained it would indicate that treating hearing loss would also improve balance. Almost exclusively, studies examining the effect of audition on balance have relied on static measures of balance by quantifying stability while standing still,
which have been linked to fall risk (11,12). However, gait performance is at least as important as static balance. Tripping is the underlying cause for the majority of falls (2). Decreases in dynamic balance performance, especially gait, are linked to increased risk of falling (13–15). The only study looking at the effect of audition on gait at this point is a small case series showing hearing assistive devices to be of clinical utility in improving dynamic balance tasks (16). Given the importance of dynamic balance to healthy aging, and the link between hearing loss and falling (2.39 times more likely (17)), this prospective study aimes to assess if dynamic gait parameters change when hearing aids and cochlear implant (CI) processors are worn.
Address correspondence and reprint requests to Timothy E. Hullar, M.D., Department of Otolaryngology–Head & Neck Surgery, Oregon Health and Science University, 3181 SW Sam Jackson Park Road, Mail Code PV-01, Portland, OR 97239; E-mail: [email protected] Financial Disclosures: T.E.H.: Med-El as surgical consultant, Advanced Bionics as surgical consultant. Disclosure of Funding: American Hearing Research Foundation grant, Award #1010372. The authors disclose no conflicts of interest. DOI: 10.1097/MAO.0000000000001551
This study was performed with the approval of the OHSU Institutional Review Board. Potential participants were recruited via the audiology department’s schedule and via flyers at nearby retirement communities. Inclusion criteria consisted of an age at least 18 years old, able to understand English, not be cognitively impaired according to the Short Blessed Test, able to ambulate independently without a cane or walker, able to perform a Romberg test on a solid surface with eyes closed for 30 seconds, and participants had been using their hearing aid
Otol Neurotol 38:1327–1332, 2017.
MATERIALS AND METHODS Participants
1327
Copyright © 2017 Otology & Neurotology, Inc. Unauthorized reproduction of this article is prohibited.
1328
T. S. WEAVER ET AL.
devises for over 3 months. An hourly payment was provided to the participants. Participants were informed simply that the present study was to evaluate hearing’s potential influence on balance. When available, audiograms were extracted from the clinical record; otherwise, a screening audiogram was completed (Beltone, Glenview, IL). Unaided thresholds for all participants were worse than 30 dB in the better hearing ear. All hearing aid (HA) participants were in the normal range with instrumented hearing. All CI participants had severe to profound hearing loss bilaterally, and could hear the testing stimulus while wearing their speech processors. Participants were asked before and after testing ‘‘Do you feel that your balance is better with your hearing devices on, off, or is there no difference?’’ All participants removed their shoes, wore a gait belt, and were closely spotted.
Test Conditions Participants wore three Opal inertial sensors (APDM, Portland, OR), one at midline of the lumbar region and one at each ankle region and inertial data were analyzed via Mobility Lab (APDM, Portland, OR) and MatLab (MathWorks, Natick, MA) software. Opal sensors (3 3 cm) consist of a 6-degree of freedom accelerometer, gyroscope, and magnetometer. Inertial sensors of this type produce measurements that have been validated with sway center of pressure measures in static conditions (18,19) and dynamic gait output measures (20). They have also been related to increased fall risk (21). In a large, open, quiet (background noise 50 years old) in the CI group again showed no effect of audition. There was considerable variation among participants. For example, participant CI-110, showed improvement in all parameters, including gait velocity that met the minimal clinically important difference (MCID) at 0.10 m/s (23). Other participants showed mixed outcomes with the hearing intervention (Fig. 2). DISCUSSION Gait Comparison The data presented here do not confirm that auditory input provides a significant benefit to gait parameters, in either HA or CI patients. This is different than the
Otology & Neurotology, Vol. 38, No. 9, 2017
Copyright © 2017 Otology & Neurotology, Inc. Unauthorized reproduction of this article is prohibited.
EFFECTS OF HA AND CI ON BALANCE Gait outcomes
TABLE 2.
Hearing Aid Users Gait Parameter Gait velocity (m/s) Stride length variabliity (CoV) Swing time variability (CoV) Double support phase (%)
Mean 95% confidence Mean 95% confidence Mean 95% confidence Mean 95% confidence
interval interval interval interval
1329
Cochlear Implant Users
HA On
HA Off
p
Processors On
Processors Off
p
0.794 0.643–0.946 0.057 0.043–0.071 0.039 0.029–0.049 24.30 20.13–28.47
0.813 0.656–0.970 0.052 0.042–0.063 0.037 0.028–0.045 23.95 19.86–28.03
0.190
0.750 0.627–0.864 0.050 0.040–0.060 0.052 0.038–0.065 28.16 23.83–32.49
0.737 0.609–0.864 0.055 0.040–0.070 0.055 0.036–0.073 28.59 23.22–33.95
0.424
0.348 0.269 0.216
0.175 0.622 0.622
HA indicates hearing aids.
conclusion of the only previous study examining the effect of audition on gait, a case series showing improvements in three patients (16). There were several important differences between the present study and that report. Most notably, the three patients in the case series had vestibular deficits unlike all of the participants in this present study (normal vestibular history and a normal 30-s Romberg). Another notable difference is the sound stimulus. Shayman et al. used a ‘‘wall of sound’’ made up of multiple treadmills along the length of the walking track, as opposed to the single point source noise at the end of the track used here (16). The third major difference was the method in which data were quantified. In the previous study a GAITRite Strip (CIR Systems, Sparta, NJ) was used to measure foot position while walking but inertial sensor instrumentation of gait was used here. Inertial sensors are limited by less robust correlation with falls and require output data to be processed into meaningful gait parameters. Despite these limitations, postural sway, as measured by inertial sensors, has been validated with platform sway measures (18,19). Gait parameters derived from these sensors have also been correlated with fall risk, demonstrating a wide range of sensitivity (35–100%) and specificity (55–99%) for fall risk (21). Importance and Complexity of Gait Despite our inability to identify a definite influence of audition on gait, the potential medical significance of this effect indicates further study as the majority of falls occur during ‘‘tripping’’ rather than standing still (2). In the case of our data, given the complexities of walking, gait measures are subject to great variability. This may obscure small but important differences in individual people. Conceivable differences could be identified in larger prospective studies or by further development of other stimulus environments and/or measuring techniques. Static Balance in Individuals With Normal Hearing As a whole, studies investigating the effect of audition on static balance have supported the conclusion that audition has a small but identifiable effect particularly in people with baseline imbalance. Two papers
quantified sway using pressure platforms and measured outcomes in terms of center of pressure in normal hearing subjects. Kanegaonkar et al. (5) reported improvements with sound, although these were between subjects with ear defenders on versus off in the absence of salient sound and, presumably, they had very similar auditory environments. Another study used infrared position sensors to compare head sway in normal hearing subjects when a white noise sound source was on versus off. Their findings were largely positive, although the relationship between their outcome variable (head sway) and overall postural stability is not quantified (7). Static Balance in Individuals With Hearing Impairment Patients with hearing loss have also shown improvement on static measures. While Rumalla et al. (9) showed a striking finding with respect to auditory influence on static balance in hearing loss, Vitkovic et al. (10), using a force plate, demonstrated a much subtler result. Rumalla et al. (9) demonstrated a consistent group of hearing aid users were at lower fall risk when they were wearing their aids in the presence of sound. Rumalla et al. (9) exchanged range-of-motion outcome measures in favor of linking fall risk to time standing on foam. This technique may be a good way to quantify balance, as ultimately it is the risk of falling, rather than sway, which is most clinically important. In a study analyzing balance effects of cochlear implantation by Buchman et al. (24), subjects were reported to significantly improving on platform posturography with processors on compared with off, as early as 5 months postimplant. A report indicated similar findings in one case of single-sided deafness treated with a cochlear implant (25). Individuals Showing Benefit Overall, one way to interpret the static and dynamic data is that a certain subset of individuals can supplement their balance with abstract auditory input, although not all participants may benefit from sound. In this study, one CI participant (CI-110) showed robust improvements in all gait measures when wearing her speech processors. A few others showed benefit to a lesser degree (CI-108, CI-111, CI-115, HA-122), although there is no shared Otology & Neurotology, Vol. 38, No. 9, 2017
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T. S. WEAVER ET AL. characteristic that could predict the performance of this group. Another study found that auditory benefit was not equally accessible among participants. Stevens et al. (8) examined a heterogeneous group, comprised of patients with normal and impaired hearing. Using a NeuroCom force platform (NeuroCom International Inc, Clackamas, OR) the study quantified a larger speed of center of pressure in the absence of sound when compared with the presence of white noise. Interestingly, in that study, the findings seem to be driven by four ‘‘top performers’’ who seem to be the most imbalanced, and the remaining subjects may not show clinically relevant improvements with sound. The gait case series by Shayman et al. (16), including patients only with documented vestibulopathies, shows one of the three subjects with a larger benefit. Given that top performers in other studies had baseline vestibulopathies, and our current study excluded vestibulopathic participants, it may be that a baseline vestibular loss is a major factor determining who will benefit. Aside from this, the current study does not give further insight as to which individuals can benefit from sound. This question should be given future consideration given the very important benefit potentially available to those at risk of fall. The presence of audition may have the ability to influence a population that relies on auditory input. Recent sensory integration studies have shown an upweighting on auditory reliance when other inputs (visual and proprioceptive) are removed (6). This is supported by general sensory reweighting principles (26). Reweighting of senses is thought be greater if it occurs earlier in development (27). Easton et al. (4) examined audition’s influence on balance in people with congenital blindness, although the study showed a similar effect of sound on balance in sighted and blind subjects.
FIG. 1. Slope graphs of gait outcomes arranged by outcome measure. Solid lines represent cochlear implant users and dotted lines represent hearing aid users. A, Gait velocity, measured in cm/s. B, Stride length variability, measured by standard deviation divided by mean, without units. C, Swing time variability, measured
Effect of Task A modified Fukuda step test has also been used to measure the effect of sound on balance (7). This test consists of the subject marching in place for 100 steps with their eyes closed. In that report, there was some improvement in angular deviation with a sound stimulus relative to a silent condition. Although the Fukuda test might be considered a test of navigation rather than strictly stability, this should not detract from its importance as a measure of balance-related disability. In fact, many vestibular-deficient patients complain strongly of a tendency to veer while walking, typically toward the affected side. Veering can severely limit daily activities and affect quality of life. Whether or not auditory supplementation to balance can be linked to a reduction in fall risk, its effect on veering while walking may still be benefit to the listener. Rumalla et al. (9) suggested sound localization as one potential mechanism. In a static task, listeners must by standard deviation divided by mean, without units. D, Double support phase, measured by percent of time in gait cycle with both feet planted.
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FIG. 2. Gait outcomes arranged by participant, left to right (within participant), gait velocity, stride lengthy variability, swing time variability, double support phase. Percent change calculated by (value in aided/value in unaided) 1. Positive value denotes improvement in the aided condition relative to the unaided.
simply adjust their posture to maintain the localization information (such as loudness level in each ear) constant. This automatically keeps them in a stable position. Furthermore, in some static studies (5,9), data were collected in a sound booth further isolating and enhancing the information available from the sound source. For a dynamic task such as the one reported here, localization cues such as loudness constantly change as the listener advances toward the auditory source. Localization cues are therefore less reliable and therefore less useful for maintaining stability. Another reason that the effect of audition on balance may be more apparent in static balance studies is that measuring stability is relatively simple (quantifying center of pressure on a balance platform, e.g.) but measuring balance as a subject moves (such as measuring movement of individual body segments) is much more complicated and small changes may be missed. Additional Static Balance Studies A few studies have reported auditory input having no effect on balance in normal hearing populations. Soames and Raper (28) examined the ability of auditory input
(pure tones and conversation) to affect balance via a force platform. Although they describe a difference, especially in sound from the right side, their data are inconclusive. In two other studies, Maheu et al. (6) and Chen and Qu (29) found that the presence of sound alone did not affect stability on a force platform, the latter study reporting unpleasant sounds (i.e., vomiting, baby crying) as destabilizing. Given the growing body of evidence suggesting auditory input contributes to balance, these few neutral findings help to support the conclusion that an effect of sound maybe likely be small or helpful only in some circumstances. CONCLUSION Overall, in the HA and CI populations, gait measures linked to fall risk did not differ between aided and unaided listening conditions. Although the overall population findings were not significant, a small subset of our population clinically improved in multiple outcome measures. While a simple hearing intervention may have the possibility to meaningfully supplement balance, this study demonstrates that patient selection may be an important consideration in the degree of benefit. Otology & Neurotology, Vol. 38, No. 9, 2017
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T. S. WEAVER ET AL. REFERENCES
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