Balance Control during Stance and Gait after

Original Paper Audiology Neurotology

Audiol Neurotol 2018;23:165–172 DOI: 10.1159/000492524

Received: May 8, 2018 Accepted after revision: July 27, 2018 Published online: October 9, 2018

Balance Control during Stance and Gait after Cochlear Implant Surgery Christof Stieger a Xenia Siemens b Flurin Honegger a Kourosh Roushan a, c Daniel Bodmer a John Allum a

a Department

of ORL, University of Basel Hospital, Basel, Switzerland; b Health Sciences Teaching Centre Basel, Basel, Switzerland; c Department of ORL, Solothurn Cantonal Hospital, Olten, Switzerland

Abstract Background: After cochlear implant (CI) surgery, some patients experience vertigo, dizziness and/or deficits in vestibulo-ocular reflexes. However, little is known about the effect of CI surgery on balance control. Therefore, we examined differences in stance and gait balance control before versus after CI surgery. Methods: Balance control of 30 CI patients (mean age 59, SD 15.4 years), receiving a first unilateral CI surgery, was measured preoperatively and postoperatively 1 month after the initial implant stimulation (2 months after surgery). Trunk sway was measured during 14 stance and gait tests using an angular-velocity system mounted at lumbar vertebrae 1–3. Results: For pre- versus postoperative comparisons across all 30 patients, a nonsignificant worsening in balance control was observed. Significant changes were, however, found within subgroups. Patients younger than 60 years of age had a significant worsening of an overall balance control index (BCI) after CI surgery (p = 0.008), as did patients with a normal BCI preoperatively (p = 0.005). Gait task measures comprising the BCI followed a similar pattern, but stance control was unchanged. In contrast, patients over 60 years or with a pathological BCI preoperatively showed im-

© 2018 S. Karger AG, Basel E-Mail [email protected] www.karger.com/aud

proved tandem walking postoperatively (p = 0.0235). Conclusion: Across all CI patients, CI surgery has a minor effect on balance control 2 months postoperatively. However, for patients younger than 60 years and those with normal balance control preoperatively, balance control worsened for gait indicating the need for preoperative counseling. © 2018 S. Karger AG, Basel

Introduction

Cochlear implant (CI) surgery is a common treatment for patients with bilateral severe sensorineural hearing loss or deafness. It is a widely accepted method in Switzerland, among many countries, for these patients to regain the possibility of oral communication with an average 70% speech understanding at a typical conversation level of 65 dB SPL [Stieger et al., 2016]. CI surgery is available for a wide range of patients, including children with prelingual deafness, for those having a normal anatomy of the cochlea and an intact auditory nerve. It is also available for elderly patients with severe hearing loss or deafness which occurs with a higher prevalence in the elderly [Agrawal et al., 2009]. In recent years, elderly hearing-impaired patients have received more focus as CI candidates [Brand et al., 2014; Christof Stieger, DSc Department of ORL University of Basel Hospital CH–4031 Basel (Switzerland) E-Mail christof.stieger @ usb.ch

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Keywords Cochlear implant · Balance control · Stance · Gait

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tory [Jacobson and Newman, 1990] are related to balance deficits. The scientific evidence is however contrary to this expectation [Yip and Strupp, 2018]. For example, Dizziness Handicap Inventory values can be improved by cognitive behavorial therapy without balance scores being changed [Schmid et al., 2018]. One question that arises is whether the aforementioned weak improvement in stance balance control found by some authors postoperatively [Buchman et al., 2004; Parietti-Winkler et al., 2015; Shayman et al., 2017] is similar for gait balance control. Research to date found no change in gait balance control after CI surgery [Weaver et al., 2017]. To date, however, the effect of CI surgery on balance control during static stance and dynamic gait tests has not been evaluated as part of the same evaluation thereby permitting a comparison across stance and gait tasks. The need for such evaluations will presumably grow with the growing numbers of patients over 60 years of age being implanted as a result of a progressive hearing loss, increasing the numbers of those for whom progressive balance problems with aging can be expected [Gill et al., 2001]. In order to study the medium term (2 months postoperatively) effect of CI surgery on balance control, we examined 30 patients with bilateral severe sensorineural hearing loss before and after a first unilateral CI surgery. A verification of postoperative balance problems for stance and gait in CI patients would indicate a general need for postoperative balance-oriented physiotherapy. This therapy should not only aim to reduce the risk of falling, but should also improve a patient’s ability to leave the home and experience other acoustic learning environments. Our working hypothesis was that only subgroups of patients – elderly implant patients or those with balance problems prior to surgery – would have significant postoperative changes in balance control.

Methods The balance control during stance and gait of 30 patients with a mean age of 59 ± 15.4 (standard deviation) years was examined on average 4 ± 0.51 months prior to and 2.1 ± 0.87 months after surgery, that is 1 month, on average, after the first postoperative initiation of electrical stimulation. For re-examination times separated by at least 3 weeks (less than the 6 months difference in this study), there is no learning effect in healthy controls [Allum and Adkin, 2003]. Each patient was receiving his or her first unilateral CI. Different types of implant systems were implanted. The Nucleus 5 (CP512) from Cochlear was implanted in 13 patients, the Freedom Nucleus 24RE(CA) system from the same company in 10 patients, the Med-El Concerto and Med-El-Synchrony were used 3

Stieger/Siemens/Honegger/Roushan/ Bodmer/Allum


Roberts et al., 2013]. It is common knowledge that in contrast to young adults, elderly patients are likely to have balance problems and suffer falls due to the effects of aging [Tinetti et al., 1988]. In CI patients, there is an additional potential risk for balance problems to be acquired following the CI surgery because of the proximity of the operation location to the vestibule and semicircular canals. If CI operations were to cause balance problems similar to those of vestibular neuritis [Allum and Honegger, 2016], such problems are likely to last a few months after CI surgery, especially if a peripheral vestibular deficit was present preoperatively. The sparse literature that exists on the subject of vestibular effects on balance control after CI surgery shows some worsening of cervical vestibular evoked myogenic potentials and caloric induced vestibular ocular responses after a CI operation in a few adult patients, but no correspondence to the greater numbers of patients with increased feelings of vertigo [Kluenter et al., 2010; Krause et al., 2009; Melvin et al., 2009]. In addition, there has been some evidence that an opening to the cochlea other than through the round window for electrode insertion may influence the prevalence of vertigo and cause cervical vestibular evoked myogenic potentials to be absent in adults [Todt et al., 2008]. For this reason, authors have suggested attention to balance problems in electrode design and surgery [Jacot et al., 2009; Todt et al., 2008]. Studies using a rotating chair, head impulse tests and caloric tests on children and adults [Buchman et al., 2004; Jacot et al., 2009] found that a majority of those with preoperative responses showed postoperative deficits. Studies examining the effect of CIs on stance tests found, in contrast, a weak improvement in postural stability during stance in some CI patients postoperatively [Buchman et al., 2004; PariettiWinkler et al., 2015; Shayman et al., 2017]. In this study we choose to focus on balance control and not vestibular ocular reflex (VOR) function as VOR tests do not provide direct insights into pathological balance control [Allum et al., 2017]. This is probably because vestibular spinal signals contributing to balance control travel along different pathways than those of VOR. Thus, it is difficult to infer balance deficits from VOR tests. For example, the structural difference in these neural pathways may underlie the different recovery times of stance and gait balance control and VOR responses following a peripheral vestibular deficit [Allum et al., 2016; Allum and Honegger, 2016]. Furthermore, we did not capture subjective feelings of dizziness with questionnaires even though it is often expected that feelings of vertigo and dizziness as captured by the Dizziness Handicap Inven-

Fig. 1. Pre- to postoperative changes in the

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and 2 times, respectively. The Hires90K from Advanced Bionics was used 2 times. Scientific use of the data collected for this study was approved (approval 2014-16) by the local ethics committee responsible for the University of Basel Hospital (Ethics Committee Northwest and Central Switzerland EKNZ). Balance of the patients was assessed by measuring trunk sway during a sequence of 14 stance and gait tasks. All stance and gait tasks were performed in the same order by each patient and executed without shoes. The tasks used were chosen based on previous studies in our laboratory comparing balance for the 14 stance and gait balance tasks between different patient groups and healthy controls [Allum and Carpenter, 2005; Gill et al., 2001]. The same protocol is also used for routine clinical balance control examinations in our clinic. In detail, trunk sway during the tasks was measured with the SwayStarTM device (Balance International Innovations GmbH, Switzerland) which uses two gyroscopes to measure pitch (anterior-posterior) and roll (lateral) angular velocities of the lower trunk at a sample rate of 100 Hz. Angles were determined online by trapezoid integration of the velocity signals. The device is worn in the middle of the lower back of the patients (at the level of lumbar vertebrae L1–L3) near the body’s center of mass [Allum and Carpenter, 2005]. The SwayStarTM device has been validated by a number of clinical studies, specifically those affected by vestibular loss [Allum and Adkin, 2003; Allum and Carpenter, 2005; Allum and Honegger, 2016], and allows comparison with a normal reference data set [Gill et al., 2001]. Four 2-legged tests were performed with the feet spaced shoulder width apart. Two were performed with eyes open, on a normal surface and on a foam surface (height 10 cm, density 25 kg/m3), and 2 with eyes closed (abbreviated s2eo/s2ec/s2eof/s2ecf). Three 1-legged stance tasks were performed eyes open, 2 on a normal surface (eyes open and eyes closed) and 1, eyes open, on the foam surface (s1eo/s1ec/s1eof). For the 1-legged tasks, the patients were asked to use their better leg to stand on. The stance tasks were performed on foam to reduce the contribution of lower-leg proprioceptive inputs to balance control. Stance tasks were performed for 20 s or until the patient lost balance. The patients performed 2 tandem gait tasks, walking 8 tandem steps on a normal and foam surface (w8tan/w8tanf), and 3 walking tasks, walking 3 m while pitching the head up and down (w3mhp), while rotating the head left and right (w3mhr) and walking 3 m, eyes closed (w3mec).

The step-wise discriminant analysis used to select the above task measures entering the BCI is described in Allum and Adkin [2003]. This combination of the selected balance outcome measures has been shown previously to have a high accuracy in detecting patients with impaired balance [Allum and Adkin, 2003]. The upper 95% limit of the BCI for healthy persons of the mean age of the patients is 385 [Hegeman et al., 2007] (see also Fig. 1a). We used the 95% limit of the BCI data of at least 10 normal healthy

Balance Control during Stance and Gait after CI Surgery


Tasks were performed with eyes closed to eliminate visual inputs to balance control. For gait tasks, patients were asked to walk at their comfortable pace. Finally, patients were asked to walk up and down a set of 2 stairs and walk over 4 low (24 cm) barriers spaced 1 m apart. For gait tasks, the task duration was the time it took to complete the task or until the patient lost balance. To standardize the start of each gait task, the patients were asked to stand comfortably with feet hip width apart. Data Processing and Statistical Analysis The outcome measurements of each trial were the peak-topeak and 90% ranges for roll angle (ra), pitch angle (pa), roll angular velocity (rv), pitch velocity (pv) and the task duration (dur). The 90% range was determined using the histograms of pitch and roll angle and angular velocity having divided the peak-to-peak range into 40 bins. As there were few differences in significance for 90% and peak-to-peak ranges (see results), here we report the peak-to-peak ranges and associated statistics. We concentrated on one primary measure, a global balance control index (BCI) to compare between pre- and postoperative values. This index combines results from several different trials into one index (see details below). When this index revealed differences, we examined as secondary measures trunk sway measures comprising this index. The BCI is an additive composite score based on measures from several tests: From the test standing on 2 legs on foam with eyes closed (2 × pv), for walking 8 tandem steps (1 × ra), for walking 3 m eyes closed (1.5 × pv + 20 × dur), walking 3 m while pitching the head up and down (1.5 × pv) and stairs (12 × ra). That is BCI = 2 × s2ecfpv + tan8ra + 1.5 × w3ecpv + 20 × w3ecdur + 1.5 × w3hppv + 12 × stairsra [Hegeman et al., 2007].

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balance control index (BCI) across the complete test population. a Comparison of the mean population pre- and postoperative values (column height) with a vertical bar on the columns indicating the standard error of the mean. The mean and mean + 1 standard deviation of BCI values for normal subjects of the same age are indicated by the horizontal dashed and dotted lines, respectively. b The individual post- to preoperative differences in BCI values. The BCI is a combination of trunk sway and task duration measures from both stance and gait tasks as defined in the Methods section.

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Fig. 2. Changes in BCI values for those with (a) and without (b) a pathological BCI val-

ue preoperatively. Each insert compares the pre- and postoperative values. c The individual differences for these 2 subpopulations. The differences indicated in b and c for those without a pathological BCI preoperatively are significant for the Wilcoxon signed-rank test. For details, refer to the legend for Figure 1.

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persons of the same age as the patient to determine whether the patient had pathological balance control preoperatively. To compare the difference between pre- and postoperative values nonparametric paired analyses (Wilcoxon signed-rank tests) were used after determining, with Shapiro-Wilks tests, that differences were not normally distributed (Fig. 1–5). The significance level was set at p < 0.05. We did not apply a Bonferroni correction for the comparison of the secondary measures comprising the BCI.

Results

The overall pre- to postoperative trend in BCI values indicated a worsening of balance control as measured by the BCI (Fig. 1). Across the complete patient group, this trend was not significant. By splitting up the patients into various subgroups, specifically those with and without a pathological BCI preoperatively and those with an age at implantation less or greater than 60 years, a significant worsening of balance was observed in 2 subgroups (Fig. 2–4). That is for those with a normal balance preoperatively (Fig. 2b) and those less than 60 years of age (Fig. 3a), a significant worsening of balance was observed, p = 0.008 and 0.005, respectively (compare Fig. 2a and b and compare Fig. 3a and b). It should be noted that there was no tendency (8 of 15) for the younger (less than 60) 168


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group to be those with normal balance control preoperatively. However, more of the elderly group (greater than 60 years) were classified into the pathological balance control group (11 of 15 preoperatively). Our analysis indicated that 5 of 15 (33%) patients who had normal balance preoperatively had pathological balance control postoperatively (Fig. 4). Furthermore, 7 of the 12 (58%) patients who were less than 60 years of age had pathological balance postoperatively. Four of these were already pathological preoperatively, leaving 3 of 12 (25%) who became pathological postoperatively (Fig. 4). Our statistical analysis indicated that the significant changes in BCI values described above were caused by changes in gait task measures. We observed no significant changes in balance control during stance tests for the 2 subgroups, in particular, not for the most difficult stance task standing eyes closed on foam. The significant contributions to changes we observed in BCI values for patients with normal preoperative BCI values were primarily caused by changes during the stairs test as illustrated in Figure 5b and c. The roll angle amplitude for the stairs task increased significantly for patients with normal balance preoperatively (p = 0.012; Fig. 5b). Concerning the BCI differences for those greater and less than 60 years at implantation we noted that pitch velocity measured while Stieger/Siemens/Honegger/Roushan/ Bodmer/Allum


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tients with pathological BCI values postoperatively in the different patient groups: those less or more than 60 years of age at implantation and those with normal and pathological BCI values preoperatively.

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