Vestibular Function in Cochlear Implantation: Correlating Objectiveness and Subjectiveness

Transcription

1 The Laryngoscope VC 2015 The American Laryngological, Rhinological and Otological Society, Inc. Vestibular Function in Cochlear Implantation: Correlating Objectiveness and Subjectiveness Angel Batuecas-Caletrio, MD, PhD; Micah Klumpp, PhD; Santiago Santacruz-Ruiz, MD, PhD; Fernando Benito Gonzalez, MD; Enrique Gonzalez Sanchez, MD; Moises Arriaga, MD Objective: To evaluate vestibular function before and after cochlear implantation (CI) Study Design: A prospective descriptive study. Material and Methods: Thirty consecutive patients with profound sensorineural hearing loss undergoing CI. Objective assessment of vestibular function was performed with the caloric test and video head impulse test (vhit) in patients before and after CI. Dizziness Handicap Inventory (DHI) was used for subjective assessment before and after CI. Results: Thirty patients received CI with 21 by round window approach and nine by anteroinferior cochleostomy. Vestibular results were categorized into four groups: no changes (20 patients), changes in the caloric test and vhit (3 patients, all with DHI changes; P ), changes in vhit gain but not in caloric test (3 patients, all with DHI changes; P ), no changes in the caloric test and vhit gain but only saccades appear (4 patients, all with DHI changes; P ). Conclusions: Although CI is a safe surgery with few major complications, it is a procedure that can produce dizziness. The vhit reveals that 30% of patients demonstrate postoperative change in vestibular function. Therefore, when examining a CI patient with postoperative symptoms of dizziness, results of the vhit test and gain as well as the presence of saccades, along with an increase DHI score, are parameters to consider in their evaluation. Key Words: Cochlear implant, vestibular function, video head impulse test, dizziness. Level of Evidence: 4. Laryngoscope, 125: , 2015 From the Department of Otorhinolaryngology, Otoneurology Unit, University Hospital of Salamanca, University of Salamanca (A.B C., S.S R., F.B.G., E.G.S.), Salamanca, Spain; and the Department of Otolaryngology and Neurosurgery, Louisiana State University Health Sciences New Orleans, Division of Otology and Neurotology Hearing and Balance Center, Our Lady of the Lake Regional Medical Center (M.K., M.A.), Baton Rouge, Louisiana, U.S.A. Editor s Note: This Manuscript was accepted for publication March 9, Dr. Arriaga has received sponsorship for Louisiana State University temporal bone dissection courses from Cochlear Americas, Med-El Corporation, and Advanced Bionics Corporation. He also serves on the Med-El Corporation Surgeon s Advisory Board. Dr. Batuecas has received sponsorship from Sociedad Otorrinolaringologica de Castilla y Leon, Cantabria y La Rioja. The authors have no other funding, financial relationships, or conflicts of interest to disclose. Send correspondence to Dr. Angel Batuecas Caletrıo, Department of Otorhinolaryngology, Pso S. Vicente Salamanca, Spain. abatuc@yahoo.es DOI: /lary INTRODUCTION Cochlear implantation (CI) is a well-known surgical procedure to rehabilitate the deaf. Indications for this procedure have expanded in the last 10 years, including bilateral CI. 1 Although CI has been accepted as a safe procedure, the insertion of an electrode into the cochlea may have an adverse effect on vestibular receptors, resulting in dizziness. 2 In fact, subjective postoperative dizziness is said to affect between 2% and 47% of patients. 3,4 There are limited data describing the exact mechanisms responsible for these postoperative changes and/or symptoms, but several theories exist. The lateral wall and the fluid space are breeched during the cochleostomy. The introduction of the electrode array may damage the basilar membrane, produce perilymph leakage, and alter the pressure in the inner ear. 5 In previous research, the following vestibular assessments were utilized to determine vestibular injuries after cochlear implantation: caloric response, vestibular evoqued miogenic potentials (VEMPs), rotatory chair, and scleral search coil. 6 The video head impulse test (vhit), a new device, is an excellent test to evaluate vestibular function not only in the lateral canals but also the vertical canals. 7 Indeed, it may be more sensitive than other tests to detect insufficient vestibular function. 8 The vhit records eye movement when physicians are performing the head-thrust test. Low gain means that eyes cannot keep the gaze in a determinate point of gaze fixation. Hence, corrective saccades are necessary to redirect the gaze to the target. The term covert saccade refers to corrective saccade that occurs when head is moving, whereas overt saccade refers to catch-up saccades observed by the examiner when head is not moving. Relationships between vestibular function via objective vestibular assessments and subjective dizziness handicap (Dizziness Handicap Inventory [DHI]) have been found repeatedly at the pre- and postoperative stages. 2,9 However, the round window (RW) approach for electrode insertion has been considered to decrease the risk of loss of vestibular function and the occurrence of vertigo compared with the anterio inferior cochleostomy approach

2 Therefore, the aim of the present study was to assess relationships between vestibular function via objective vestibular assessments and subjective dizziness handicap via the DHI before and after CI. MATERIALS AND METHODS Subjects This study evaluated 30 patients diagnosed with a profound sensorineural hearing loss who were prospectively scheduled for surgery between May 2012 and January All were subjected to CI surgery and were reviewed in the second postoperative day. The study was performed in accordance with the ethical guidelines of the 1975 Declaration of Helsinki. Specifically, the study was approved by the institutional review board (Unidad de investigacion del Complejo Universitario de Salamanca), and informed consent was obtained from each study participant. Patients with other pathologies that could directly affect postural control, such as central nervous system diseases or orthopedic diseases, were excluded. A normal vestibular function before surgery was main inclusion criteria. Methods All 30 patients underwent transmastoid scala tympani CI performed by two surgeons (SSC, FB). Patients were implanted with Med-El devices in all cases (Sonata TI 100 standard and Sonata TI 100 FlexSoft 28, Innsbruck, Austria). If possible, electrodes were implanted via a facial recess approach through a round window insertion. Otherwise, cochleostomy was made anteroinferior to the round window niche. Each implanted electrode was reported to have reached full insertion in a single pass without any resistance or complication. Auditory nerve response telemetry was obtained in all patients. Bithermal binaural caloric irrigation, DHI, and vhit were performed in each patient within 1 month before surgery and 2 days after surgery. Exclusion criteria were vertigo episodes before surgery, less than 18 years of age, bilateral vestibular areflexia, abnormal caloric test or vhit before surgery, and abnormal otoscopy after surgery. VOR Assessment The VOR was evaluated with the head-impulse test (HIT). For this, the physician stands behind the patient and grasps the patient s head firmly with both hands. The patient is asked to keep looking at a stationary object on the wall that is at a distance of 90 cm to 100 cm. The head is quickly and unpredictably turned through 10 to 20 degrees in the horizontal plane to the left or right, which permits testing of the corresponding horizontal semicircular canal. In order to register and measure head and eye velocity during the head impulse, we used a video HIT system (vhit) (GN Otometrics, Denmark). The patient wears a pair of lightweight, tightly fitting goggles on which is mounted a small video camera and a half-silvered mirror that reflects the image of the patient s right eye into the camera. The eye is illuminated by a low-level infrared light-emitting diode. A small sensor on the goggles measures the head movement. The whole goggle system weighs about 60 g and is secured tightly to the head to minimize goggle slippage. Calibration is performed, and the procedure of vestibulo-ocular testing is initiated. The head movement speed is measured by the sensor in the goggles, and the image of the eye is captured by the high-speed camera (250 Hz) and processed to yield eye velocity. At the end of each head turn, the head-velocity stimulus and eye-velocity response are displayed simultaneously on the screen such that the clinician can see if the stimulus and response were adequate, providing a quick way to maximize the quality of the head impulse. In normal conditions (healthy patients), the physician should observe that the patient is able to maintain the eyes fixed on the stationary target during the high-speed head rotation. When unilateral vestibular weakness exists, the eyes drift in the same direction as the head, and then compensatory refixation saccades are used to reset the visual fixation on the target. In a full test, 20 impulses are delivered randomly in each direction. At the end of the full test, all of the head velocity stimuli and eye velocity responses are displayed. The parameters evaluated are the VOR mean gain (ratio of eye velocity to head velocity for every head rotation; normal 5 0.8) and the appearance of saccades (covert or overt catch-up saccades) after head impulses to right and left. Bithermal binaural water caloric irrigations were performed on all patients to assess for the presence of reduced vestibular function using the Jongkees formula. 10 videonystagmography (VNG) was performed recording eye movements by means of a video-based system (Ulmer VNG, v. 1.4, Synapsis, Marseille, France); and bithermal, binaural water caloric irrigations (cool, 30 C and warm, 44 C) were performed on all patients to assess for the presence of reduced vestibular using the Jongkees formula. For the purposes of this study, a unilateral reduced vestibular response greater than 25% was considered abnormal. Postoperative changes of 10% or more in caloric response from preoperative levels were considered abnormal. 9 Disability and Handicap Assessment Dizziness Handicap Inventory. The DHI, a validated tool of subjective dizziness handicap, consists of a 25-item 3- point questionnaire which assesses self-care skills, psychosocial behaviors, and physical activity. 11 The DHI questionnaire was translated and adapted to the Spanish language following the method of cross-translation. The reliability of the scale was evaluated and the Cronbach alpha coefficient was The doctor explained the aim of the questionnaire, and the patient filled out the questionnaire. Where necessary, the technician in charge of the vestibular tests (who is well versed in the scope of the work and who has considerable experience in the vestibular laboratory) helped to clarify some items. The questionnaires were answered in a similar fashion to the original English version. In the DHI, the patient had to answer yes, sometimes, or no to each question, the responses being given a value of 4, 2, and 0, respectively. The questionnaire has 25 items; thus, the total score) ranged from 0 to 100. A change of total DHI score by > 6 points after implantation was considered significant. 13 Data Analysis. The pre- and postoperative results of the caloric response test and vhit examinations in the implanted patients were compared with DHI scores. Implant and nonimplant ears were both assessed. The caloric responses were classified as exhibiting a postoperative change (i.e., abnormal) if a difference of more than 10% was demonstrated. An absolute value of vhit gain greater than 0.8 was considered normal, less than 0.8 was considered abnormal. Also, the appearance of covert or overt saccades in the postop vhit test was considered abnormal. All patient data were compared according to DHI scores. For statistic analysis, the t test or Mann Whitney test was used (P ) (SPSS v. 21.0; IBM Corp., Armonk, NY). RESULTS A total of 30 patients undergoing unilateral CI were included in the study. The mean age was years. 2372

3 Fig. 1. Before surgery. The video head impulse test showing normal vestibular function. [Color figure can be viewed in the online issue, which is available at Of those, 18 were female and 12 were male. The surgery was performed in the right ear in 23 patients and in the left ear in 17. Round window insertion was accomplished in 21 patients and anteroinferior cochleostomy was used in 9. We categorized the patients into four groups according to the changes in the vestibular tests: group A, no changes; group B, changes in the caloric test and vhit; group C, Changes in vhit gain but not in caloric test; and group D, no changes in the caloric test and vhit gain but saccades present on vhit. Changes in the Vestibular Tests Group A. A normal caloric response and a normal vhit after surgery was found in 20 patients. This leaves 10 patients (33% of the cohort) with changes in the caloric test or in the vhit after surgeries, which are categorized in the other groups. Group B. In three patients, caloric test changes appeared after surgery, with reduced response in the operated ear (35%, 32%, 28%). In all of them, gain in the vhit became abnormal (0.75, 0.71, 0.77). In this group of patients, DHI was increased after surgery (mean DHI score 2 before surgery to 20 after surgery) (P ). All three patients in group B received cochleostomy for CI (P ). Group C. In three patients, changes in the vhit gain were observed (0.73, 0.74, 0.76), but caloric response did not change. In these patients, DHI score changed as well (mean 0 before surgery to 16 after surgery) (P ). Group D. Finally, in four patients no changes were observed in caloric responses or vhit gain, but saccades appeared (covert and overt saccades in 2 cases and overt saccades in 1 case) (Figs. 1 and 2). In these four patients, DHI changed (mean 2 before surgery to 12 after surgery) (P ) (Table I). There were no differences considering the cochlear implant device or surgeon. DISCUSSION Cochlear implantation may cause trauma by the insertion of the electrode into the inner ear, which may lead to an intraoperative loss of perilymph, foreign body reaction (i.e., labyrinthitis), postoperative perilymph fistula, and/or endolymphatic hydrops. It has been demonstrated that the electrode insertion during the CI may produce damage of the osseous spiral lamina, basilar membrane, and vestibular receptors: saccule, the utricule, and semicircular canals. There is evidence of anatomical and physiological damage. 14,15 Some cochlear implant patients have vertigo or dizziness before surgery, and there is a close relationship between hearing loss and the loss of vestibular function before surgery in patients with severe to profound hearing loss in adults and in children. 16 Previous studies in postoperative CI patients have not demonstrated a close relationship between subjective symptoms and objective vestibular assessment results, 2,9,17 including motorized head impulse rotation. Furthermore, previous reports have not shown a significant change in vhit gain before and after CI. 18 In contrast, the authors of the present study believe that examining gain alone may not represent all of the physiologic changes occurring after CI because the presence of saccadic abnormalities may exist. Moreover, previous research has demonstrated that the injury in the vestibular system in some patients is not enough to decrease objective vestibular function (i.e., caloric response or vhit gain). However, in this study there is 2373

4 Fig. 2. After surgery (left cochlear implantation). Only saccades appear in the video head impulse test. [Color figure can be viewed in the online issue, which is available at evidence of covert and overt saccades and an increase an increase in DHI total score immediately after CI. Therefore, the additional vhit abnormalities indentified in this study are clinically relevant because there is a relationship to subjective vestibular handicap in the DHI. 19 Covert catch-up saccades and overt catch-up saccades that occur during the head movement in the headthrust test (covert) or when the head is stopped (overt), respectively, reveal alterations of vestibular function as well as the vestibular compensation process over time. 20 In order to make a decision about which side is better to implant, the duration of deafness, degree of hearing loss, and inner ear anatomy must be considered prior to CI. Vestibular function should also be considered. To reduce the risk of postoperative dizziness, we agree with recommendations that the side with the worse vestibular function should be implanted where possible, other factors being equal. 21 A combination of vestibular function assessments are routinely carried out preoperatively in some cochlear implant centers already as an additional aid to determine the optimal side for implantation. 5 Controversies exist regarding the influence of the CI approach in preserving vestibular function as some studies do not agree with differences noted between approaches. 22 In our experience, the round window approach is safer and less traumatic than a cochleostomy for CI. Published evidence suggests that round window insertion preserves the functional integrity of the vestibular receptors (saccule/lateral semicircular canal (SCC)) to a greater extent than cochleostomy. 2,23 Other strategies such as the use of middle ear steroids during surgery decrease vestibular function changes following CI. 24 Scores obtained in DHI show a low mean handicap after surgeries. Thus, we can conclude that although CI affects vestibular function, it is mild and short-term. 5 We assume that performing vhit only in the horizontal plane could underdiagnose some deficits in vertical canals, mainly concerning posterior semicircular canal deficits. Future studies should investigate this. Although symptomatic vestibular impairment after CI appears to be short-term in most cases, with longterm disability unlikely, 6 the possibility of vestibular disturbance by CI, especially bilateral CI, should be TABLE I. Results According Groups. Group Number Changes in Vestibular Test (mean before surgery mean after surgery) Anterioinferior Cochleostomy DHI Changing Significance (mean DHI score before surgery mean DHI score after surgery) A 20 No 4 P (0 2) B 3 Caloric test (11% 31%) 1 vhit gain 3 P (2 20) ( ) C 3 vhit gain ( ) 1 P (0 16) D 4 vhit saccades 1 P (2 12) DHI 5 Dizziness Handicap Inventory; vhit 5 video head impulse test. 2374

5 explained to the patients preoperatively. 9,25 The occurrence of postop CI vestibular disturbance is especially important for the elderly and pediatric populations in which not only is vestibular function sometimes affected (15% 50% in children) but other important balance systems also are affected such as vision and proprioception. 26,27 In our opinion, vhit is an excellent procedure to test vestibular function before and after some otologic surgeries such as CI. It could offer more information about vestibular changes than other test-like calorics. DHI is a questionnaire; it is not a vestibular test. DHI should be used only to obtain information about how the patient feels. But only asking for such information can the surgeon know about a patientçs dizziness after surgery. DHI is an excellent tool to perform this analysis of subjective symptoms. Limitations This study only examined short-term vestibular function and DHI changes. The long-term clinical implications of our findings are unclear. Furthermore, whereas previous research has demonstrated that the middle ear and mastoid fluid do not influence caloric stimulation 28 ; the postoperative vestibular studies were performed in the acute postoperative time period and there is a remote possibility that our findings represent transient acute postoperative changes. Additional studies with longer follow-up and serial testing at different time intervals will be helpful. Indeed, because vhit was performed in the immediate postoperative time, we have examined patients with mild velocities in the head impulse test in all patients, trying to get homogeneus groups. High velocities in the impulse test could uncover some covert saccades 29 and should be taken into account in future studies. CONCLUSION Although CI is a safe surgery with few major complications, it is a procedure that can produce dizziness. The vhit reveals that 30% of patients demonstrate postoperative change in vestibular function. Therefore, when examining a CI patient with postoperative symptoms of dizziness, results of the vhit test, gain as well as the presence of saccades, along with an increase DHI score could be considered. In patients who will be undergoing CI, subjective and objective vestibular function assessments prior to surgery are valuable. If there is no other considerations influencing side selection, the side with the worse vestibular function should be chosen for CI, and a round window approach should be considered. Additional study is needed to determine if the short-term changes in objective and subjective vestibular function persist in longterm follow-up. BIBLIOGRAPHY 1. Krause E, Wechtenbruch, Rader T, Gurkov R. Influence of cochlear implantation on sacculus function. Otol Head neck Surg 2009;140: Todt I, Basta D, Ernst A. 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