Evaluation of Vestibular Symptoms and Postural Balance Control in Patients With Chronic Otitis Media PDF

Journal of Vestibular Research xx (20xx) x–xx 1 DOI:10.3233/VES-200691 IOS Press 1 Evaluation of vestibular symptoms 2 and postural balance control in patients with chronic otitis media...

Journal of Vestibular Research xx (20xx) x–xx 1 DOI:10.3233/VES-200691 IOS Press 1 Evaluation of vestibular symptoms 2 and postural balance control in patients with chronic otitis media f 3 roo 4 Rafael da Costa Monsantoa,b,∗ , Ana Luiza Papi Kasemodela , Andreza Tomaza , Thais Gomes 5 Abrahão Eliasa , Michael Mauro Paparellab,c and Norma de Oliveira Penidoa a Department rP 6 of Otolaryngology, Head & Neck Surgery, Universidade Federal de São Paulo/Escola Paulista de 7 Medicina (UNIFESP/EPM) (São Paulo, SP, Brazil) 8 b Department of Otolaryngology Head & Neck Surgery, University of Minnesota (Minnesota, MN, USA) 9 c Paparella Ear Head & Neck Institute. (Minnesota, MN, USA) tho 10 Received 28 March 2019 11 Accepted 10 January 2020 Au 12 Abstract. 13 BACKGROUND: Evidence to support potential links between chronic otitis media (COM) and vestibular impair- 14 ment/postural balance control issues is lacking. 15 OBJECTIVE: To investigate whether COM associates with vestibular symptoms, balance problems, and abnormalities in 16 vestibular function tests. 17 METHODS: We selected patients with COM and excluded patients with any identifiable underlying causes for vestibular d 18 dysfunction. Fifty-two healthy volunteers were included as controls. All subjects underwent anamnesis, physical examination, 19 posturography, and video-head impulse tests. cte 20 RESULTS: We found a high prevalence of vestibular symptoms (58.4%) among patients with COM, while only 2% of 21 the controls had vestibular symptoms. There was a positive correlation between COM activity with the presence of tinni- 22 tus and vestibular symptoms (P < 0.05). Clinical vestibular tests were abnormal in 63% of patients with COM, and those 23 positively associated with presence of vestibular symptoms. Posturography results shown worse postural balance control in 24 patients with COM as compared with controls, especially in the limit of stability (LOS) (Mean LOS, COM = 157.56 cm2 ; con- rre 25 trols = 228.98 cm2 ; p < 0.001), and in the test with eyes closed while standing on a foam mattress (sway area, COM = 10.91 cm2 ; 26 controls = 5.90 cm2 ; p < 0.001). We did not observe differences in the average vestibuloocular reflex gains in the video-head 27 impulse test between our COM and control groups. 28 CONCLUSIONS: Our results show that COM associates with a high prevalence of vestibular symptoms, worse postural 29 control, and more severe hearing loss as compared with controls. Among patients with COM, the activity of the middle-ear co 30 inflammation seemed to positively associate with more severe hearing and balance problems. 31 Keywords: Otitis media, vestibular function tests, vertigo, dizziness, postural balance Un 32 1. Introduction incidence is estimated at 4.8 new episodes per 1000 35 people every year. Patients with COM are under risk 36 33 Chronic otitis media (COM) is a disease with high of developing acute complications [30, 40, 41] and 37 34 prevalence worldwide (Monasta et al., 2012) – its also long-term sequelae [1, 2, 34, 38], which include 38 tinnitus and hearing loss. 39 ∗ Corresponding author: Rafael da Costa Monsanto, M.D., Ph.D The association between sensorineural hearing 40 student, University of Minnesota, 2001 6th St SE, Minneapolis, MN 55455. Tel.: +1 617 3194365; E-mail: rafaelmonsanto@ loss and COM has been demonstrated by several 41 hotmail.com. histopathologic and clinical studies in the past [14, 42 ISSN 0957-4271/20/$35.00 © 2020 – IOS Press and the authors. All rights reserved  2 R. da Costa Monsanto et al. / Evaluation of vestibular symptoms and postural balance control 43 38]. More recently, it has been hypothesized that demographic (sex, age, ethnicity) and other relevant 87 44 COM may associate with vestibular symptoms as information, such as presence of tinnitus, vestibu- 88 45 well [20, 47]. However, a recent systematic review lar symptoms (and its characteristics, triggers and 89 46 observed that most of the studies dedicated to evalu- worsening factors), and frequent episodes of otor- 90 47 ate the links between vestibular symptoms and COM rhea. Vestibular symptoms were classified as per the 91 48 had several potential biases, which may have compro- guideline proposed by the Bárány society. The 92 49 mised their data. Thus, the objective of this study neurologic and vestibular function were clinically 93 50 is to investigate, based on a systematic research pro- assessed by static (Romberg test) and dynamic (gait 94 f 51 tocol, whether or not COM associates with vestibular and Fukuda stepping tests) equilibrium tests, cere- 95 roo 52 symptoms, postural balance problems, and abnormal- bellar function tests (index-index, index-nose, and 96 53 ities in vestibular function tests. diadochokinesis), nystagmus (spontaneous, semi- 97 spontaneous, head impulse and head-shaking tests), 98 muscular tone and strength, examination of the cra- 99 54 2. Materials and methods nial nerves, subjective vertical visual (SVV) using the 100 rP “bucket test”, and positional tests (Dix-Hallpike and 101 55 2.1. Design and ethical considerations Head-Roll). The tonal and vocal audiometry was per- 102 formed using the AC-40 audiometer (Interacoustics 103 56 This study protocol was approved by the Institu- A/S, Middelfart, Denmark). 104 tho 57 tional Review Board of our university (n.1.751.916). Subjects with COM were categorized in 3 groups: 105 58 We conducted a cross-sectional, controlled study at (1) chronic perforation of the tympanic membrane 106 59 a tertiary care referral center, from August 2016 to (CPTM) caused by otitis media, with infrequent 107 60 November 2018. suppuration; (2) chronic suppurative otitis media 108 (CSOM), defined as frequent or intractable ear 109 Au 61 2.2. Patient selection suppuration through a tympanic membrane perfo- 110 ration without cholesteatoma; and (3) COM with 111 62 From our otology outpatient clinic, we selected cholesteatoma. Patients with adhesive otitis media 112 63 consecutive patients with COM that complied with without cholesteatoma were not included in our study. 113 64 our inclusion and exclusion criteria. Patients with We also defined as “active” COM when patients 114 COM were identified by the presence of chronic had signs of active middle ear inflammation, includ- d 65 115 66 infection/inflammation of the middle ear cleft and ing presence of intense hyperemia and suppuration 116 cte 67 perforation of tympanic membrane [5, 6]. We – by definition, CPTM cases were all “inactive”. 117 68 excluded volunteers who (1) were less than 18 Patients with bilateral COM groups were categorized 118 69 years; (2) had any identifiable cause for vestibu- using the following protocol: (1) at least one ear had 119 70 lar symptoms (past use of ototoxic medication, cholesteatoma – cholesteatoma group; (2) at least one 120 71 clinical otosclerosis, definite or probable Meniere’s ear had CSOM, none had cholesteatoma – CSOM 121 rre 72 disease, definite or probable vestibular migraine, group; (3) both ears had CPTM – CPTM group. 122 73 perilymphatic fistula, untreated metabolic or cardio- With the same inclusion and exclusion criteria used 123 74 vascular diseases, diabetes or glucose intolerance, for the COM groups, we also selected volunteers with 124 75 benign paroxysmal positional vertigo, head trauma no history of ear disease using a convenience sam- 125 co 76 or traumatic head blast injury, neurologic or neurode- pling method, who were included in a control group. 126 77 generative diseases, and syphilis); (3) had a history Subjects in the control group underwent the same rou- 127 78 of otologic surgery (except ventilation tubes); (4) had tine of clinical, hearing, and vestibular testing used 128 79 cognitive deficits; (5) had genetic syndromes or oto- for the COM group. 129 Un 80 logic malformations; (6) had significant past noise 81 exposure or acoustic trauma; (7) had cancer or under- 2.4. Evaluation of vestibular function 130 82 went past chemotherapy or radiation therapy; and (8) 83 had orthopedic or visual limitations. To evaluate postural balance control and analyze 131 vestibular function, we performed static posturogra- 132 84 2.3. Clinical evaluation phy (Balance Rehabilitation Unit – BRU; Medicaa; 133 Montevideo, Uruguay) and video-head impulse 134 85 Patients with COM underwent a systematic clini- (video-HIT) (Otometrics A/S; Taastrup, Denmark) 135 86 cal, laboratory, and imaging evaluation. We collected tests. Considering that our group of subjects ranged 136  R. da Costa Monsanto et al. / Evaluation of vestibular symptoms and postural balance control 3 137 from healthy volunteers to patients with severe considered statistically significant when the value of 187 138 middle-ear abnormalities, we did not use caloric P was less than 0.05. 188 139 testing and vestibular evoked myogenic potentials 140 (VEMPs). The posturography and video-HIT tests 141 were selected because their results are not influenced 3. Results 189 142 by the presence of middle-ear disease. 143 The static posturography of the BRU allows assess- 3.1. Demography 190 144 ment of the postural control/vestibulospinal reflex f 145. A force platform measures displacement of Our final COM group comprised of 126 patients 191 roo 146 the center of pressure, while patients are exposed to with COM – demographic information is listed in 192 147 somatosensorial (eyes closed, standing on a medium Table 1. Among the 39 patients with cholesteatoma, 193 148 density foam mattress with eyes closed), vestibular, 28 (71.7%) had active signs of middle ear inflam- 194 149 and visual (saccadic, optokinetic) stimuli. The postu- mation and 11 (28.3%) did not. We did not find 195 150 ral control is analyzed under 3 parameters: (1) limit significant age differences among our study and con- 196 rP 151 of stability (LOS) = area in which the volunteers can trol groups (p = 0.34). 197 152 intentionally dislocate their center of pressure (cm2 ); 153 (2) sway area = area comprising 95% of the disloca- 3.2. Clinical symptoms and audiologic 198 154 tions of the center of pressure in each specific test assessment 199 (cm2 ); and (3) sway velocity = total distance of dis- tho 155 156 location divided by the duration of the test (cm/s). The most frequent symptoms among patients with 200 157 The video-HIT is a bedside test used to evaluate COM were hearing loss and tinnitus (Table 1), and 201 158 function of the semicircular canals, providing objec- those were significantly more frequent as compared 202 159 tive measures of the gain of the vestibulo-ocular reflex with the control group (P < 0.001). We did not find 203 Au 160 (VOR) for each canal separately. The number of differences in prevalence of tinnitus among the COM 204 161 movements toward each desired semicircular canal subgroups (P = 0.102). 205 162 was set to 20. When artifacts were identified, the test The overall prevalence of vestibular symptoms in 206 163 was repeated once more. Tests were performed by one the COM groups was 58.4%; in the control group, 207 164 of the authors, who has extensive experience in video- prevalence was 2.0% (P < 0.001) (Table 1). The 208 HITs. All individual impulses collected were stored characteristics and frequency of the vestibular symp- d 165 209 166 and assessed for artifacts by a blinded researcher, toms among patients with COM are depicted in 210 cte 167 also with extensive training in video-HITs. Results Fig. 1. Among the COM subgroups, vestibular symp- 211 168 were considered abnormal when VOR gain was less toms were more frequent in patients with CSOM 212 169 than 0.8 (horizontal canals) or 0.7 (vertical canals) (77.7%) and cholesteatoma (64.1%) as compared 213 170 and corrective saccades were present. with CPTM (46.6%) (P = 0.037). Triggers for the 214 vestibular symptoms were reported by 65% of the 215 rre 171 2.5. Statistical methods patients with COM – the most frequent trigger was 216 the onset or worsening of otorrhea (75%). Other 217 172 All results obtained with the anamnesis, physical triggers were positional (21%), unspecific headache 218 173 examination, and vestibular/postural testing in both (4%) and driving (2%). In our COM groups, the pres- 219 co 174 COM and control groups were subjected to com- ence of tinnitus associated with a 2-fold increase in 220 175 parative analysis. Categoric variables were compared the risks of patients complaining of vestibular symp- 221 176 using Pearson’s x2 test and, when necessary, we per- toms (Relative Risk [RR] = 2.63; 95%CI, 1.60–4.33; 222 177 formed the post-hoc cellwise residual analysis test P < 0.001). We did not find a significant association 223 Un 178. The distribution of numerical data was assessed between the presence of vestibular symptoms and 224 179 using Shapiro-Wilk test – normally distributed data laterality (unilateral or bilateral COM), sex, or race 225 180 was analyzed using independent t-tests or ANOVA (P > 0.05). 226 181 with Tukey’s post-hoc test, and non-normal data was Results of audiometric evaluation are in Table 2. 227 182 analyzed using Mann-Whitney U, Kruskal-Wallis test Patients with COM had worse pure-tone aver- 228 183 with Dunn-Bonferroni post-hoc pairwise compar- ages (PTA) and speech discrimination scores 229 184 isons, or Spearman’s rank coefficient test. All tests in all COM groups as compared with controls 230 185 were carried using the IBM SPSS v. 23.0 Statistics (P < 0.05). Among COM groups, patients with 231 186 software (Armonk, NY; IBM Corp). Results were CSOM or cholesteatoma had significantly worse 232  4 R. da Costa Monsanto et al. / Evaluation of vestibular symptoms and postural balance control Table 1 Demography information, frequency (%) of clinical complaints reported by volunteers of the COM and control groups and otoscopy findings Demography Controls CPTM CSOM Cholesteatoma COM (total) Number of volunteers 52 (100%) 60 (47.5%) 27 (21.5%) 39 (31%) 126 (100%) Mean age (years) 39.1 43.1 44.8 41.25 42.9 Sex F, 36 (69%) F, 41 (68%) F, 17 (62.9%) F, 24 (61.5%) F, 82 (65%) Symptoms Hearing loss – 51 (85.0%) 27 (100%) 39 (100%) 117 (92.8%) f Otorrhea – 39 (65.0%) 27 (100%) 26 (66.6%) 92 (73.0%) roo Tinnitus 7 (13%) 34 (56.6%) 21 (77.7%) 28 (71.7%) 83 (65.8%) Vestibular symptoms 1 (2%) 28 (46.6%) 21 (77.7%) 25 (64.1%) 74 (58.7%) Otoscopy findings TM perforation – 60 (100%) 27 (100%) 35 (89.8%) 122 (96.8%) Inflammation/otorrhea – 0 (0.0%) 27 (100%) 26 (66.6%) 53 (42.0%) rP CPTM = Chronic perforation of the tympanic membrane; CSOM = Chronic suppurative otitis media; COM = Chronic otitis media; TM = tympanic membrane. without tinnitus (P > 0.05), and (2) patients with and 256 without vestibular symptoms (P > 0.05). 257 tho 3.3. Physical examination 258 Table 1 summarizes the otoscopy findings in the 259 Au COM and control groups. Among patients with 260 COM, only 4 volunteers did not have tympanic 261 membrane perforation, all of which were from the 262 Fig. 1. Characteristics of the vestibular symptoms among patients with COM (N = 74; 58.7%). cholesteatoma group. In those patients, otoscopy 263 showed attic retraction pocket, local bony erosion, 264 and presence of the characteristic pearly-white mass d 265 233 PTA (P = 0.006 and P = 0.009) scores than patients suggestive of cholesteatoma. 266 cte 234 with CPTM. We did not find significant differ- We found abnormalities in the clinical vestibular 267 235 ences in speech recognition scores (P = 0.264) among and cerebellar function tests in 63% of patients with 268 236 the COM subgroups. Four of the volunteers from COM. Those abnormalities correlated significantly 269 237 the control group (mean age = 58.75 years) had a with the presence of vestibular symptoms (P = 0.002; 270 238 mild sensorineural hearing loss affecting the fre- 95%CI = 0.108–0.458). The test which was most 271 rre 239 quencies above 4 kHz (mean speech recognition frequently abnormal was the Fukuda stepping test 272 240 thresholds = 12.5 dB; mean speech discrimination (62%), followed by instability in the Romberg test 273 241 scores = 98%) in isolation, suggesting presbycusis. (12%), and presence of corrective saccades in the 274 242 We found no differences in the prevalence of head impulse test (1.6%). The presence of abnormal- 275 co 243 conductive as compared with mixed hearing loss ities in the clinical vestibular tests did not associate 276 244 among our COM subgroups (P > 0.05). But the pres- significantly with type of hearing loss (conductive or 277 245 ence of mixed hearing loss significantly associated mixed), laterality (unilateral or bilateral), or presence 278 246 with worse PTA and speech discrimination scores of tinnitus (P > 0.05). 279 Un 247 (P < 0.001 and P = 0.019, respectively) as compared The mean SVV results were above reference values 280 248 with conductive hearing loss. The type of hearing (±2◦ ) in all COM groups, and within normal among 281 249 loss did not correlate significantly with presence or controls (Fig. 2); the difference between SVV results 282 250 absence of tinnitus or vestibular symptoms (P > 0.30). in patients with COM and controls was statistically 283 251 Among patients who had tinnitus, PTA was also significant (P < 0.001). But we found no signifi- 284 252 significantly worse as compared with patients without cant differences in pairwise comparisons among our 285 253 tinnitus (45.5 dBNA and 38.1 dBNA, respectively; COM subgroups (P > 0.05). We did not find sig- 286 254 P = 0.024). We did not find differences in speech nificant correlations between the SVV results and 287 255 recognition scores between (1) patients with and presence/absence of tinnitus, presence of vestibular 288  R. da Costa Monsanto et al. / Evaluation of vestibular symptoms and postural balance control 5 Table 2 Results of audiometric evaluation in the study and control groups, expressed as type of hearing loss, pure-tone average (PTA) and speech discrimination score Controls CPTM CSOM Cholesteatoma COM (total) Type of hearing Normal 48 (92.3%) – – – – loss Conductive – 33 (56.9%) 8 (33.3%) 15 (42.8%) 56 (47.9%) Mixed – 25 (43.1%) 16 (66.7%) 20 (57.2%) 61 (52.1%) Sensorineural 4 (7.7%) – – – – Pure-tone average Normal 7.88 – – – – f (dB) Conductive – 32.7 43.7 45* 38.1 roo Mixed – 43.3 52.3 53.2 48.6 Sensorineural 12.5 – – – – Total 8.23 37.6* 49.6* 51.3* 43.7* Speech discrimination Normal 100% – – – – score (%) Conductive – 98.3% 99.5% 99.0% 96.7% Mixed – 94.8% 87.2%* 88.0%* 89.2.% rP Sensorineural 98.0% – – – – Total 99.8% 96.7%* 91.2%* 93.1%* 94.4% Legends: CPTM = chronic perforation of tympanic membrane; CSOM = Chronic suppurative otitis media; COM = Chronic otitis media. Light gray cells, *=significant difference (P < 0.05) as compared with controls. Dark gray cells, *=significant (P < 0.05) difference as compared with the CPTM and control groups. tho d Au cte Fig. 2. Left: boxplot graphic results obtained with the posturography test regarding the limit of stability (LOS) of the study and control groups. Right: boxplot graphic results showing results obtained with the subjective vertical visual using the “bucket test”. *=statistically significant difference (P < 0.05) as compared with the control roup. rre 289 symptoms, and abnormalities in clinical vestibular only yielded statistically significant differences as 302 290 tests (P > 0.05). compared with controls under few specific stimuli 303 co (Table 3). We observed that the sway area and sway 304 291 3.4. Vestibular function tests velocity were significantly worse in the CSOM group 305 as compared with the CPTM group in several postur- 306 292 The posturography test showed that all COM ography tests (eyes closed, eyes closed while standing 307 Un 293 groups had worse LOS results as compared with con- on a foam mattress, and optokinetic tests) (Table 4). 308 294 trols (Fig. 2, Tables 3 and 4) (P < 0.05). We also The test with eyes closed while standing on a foam- 309 295 observed that – in the CSOM and cholesteatoma with mattress was the most challenging and yielded higher 310 296 active middle ear infection groups – the sway areas sway area/velocity in both COM and control groups 311 297 and sway velocities were significantly increased in (Fig. 3); 3 volunteers from the CSOM group needed 312 298 the majority of posturography test as compared with support from the harness during this test. 313 299 controls (P < 0.05) (Fig. 3, Table 3). On the other Among COM groups, we found a significant neg- 314 300 hand, the posturography results in the CPTM and ative moderate correlation between the SVV results 315 301 cholesteatoma (with and without active infection) and LOS (correlation coefficient [CC], –0.350; 316  6 R. da Costa Monsanto et al. / Evaluation of vestibular symptoms and postural balance control Table 3 Values of significance (P values) obtained from the comparisons of posturography test results in volunteers with COM and controls, as the result of Kruskal-Wallis analysis of variance and Dunn-Bonferroni post-hoc’s pairwise comparisons Pairwise comparisons Parameter Kruskal- Controls- Controls- Controls- Controls-Cholesteatoma Controls-Cholesteatoma Wallis CPTM CSOM Cholesteatoma without active disease with active disease LOS >0.001* 0.001* 0.007* 0.001* 0.012* >0.001* EC SA >0.001* 1 >0.001* 0.467 0.711 0.104 SV >0.001* 1 >0.001* 0.386 0.841 0.068* f EC, foam SA >0.001* 0.486 >0.001* 0.004* 0.081 >0.001* roo SV >0.001* 0.033* >0.001* 0.065 0.818 0.007* Saccadic SA 0.022* 1 0.011* 1 0.447 0.102 SV 0.003* 0.030* 0.004* 0.403 0.872 0.039* Optokinetic SA >0.001* 0.10 0.017* 0.709 0.912 0.014* SV 0.001* 1 >0.001* 1 0.696 0.111 Visual-vestibular interaction SA 0.002* 0.068 0.002* 0.117 0.818 0.013* SV >0.001* >0.001* 0.002* 0.027* 0.207 0.004* rP LOS = Limit of stability; EC = eyes closed; EC, foam = Eyes closed, standing over foam mattress; SA = Sway area; SV = Sway Velocity; CPTM = chronic perforation of tympanic membrane; CSOM = Chronic suppurative otitis media; Infected Cholesteatoma = Volunteers who had active or chronic suppuration and cholesteatoma, excluding patients with cholesteatoma but no active infection. The cells marked in gray and marked with a * refer to significantly worse results in a specific COM group as compared with the control group (P < 0.05). tho Table 4 Values of significance (P values) obtained from the comparisons of posturography test results in volunteers with COM and controls, as the result of Dunn-Bonferroni post-hoc’s pairwise comparisons Mean results Pairwise comparisons Parameter CPTM CSOM Cholesteatoma CPTM- CPTM- CSOM- Au CSOM Cholesteatoma Cholesteatoma LOS 160.81 cm2 155.31 cm2 155.57 cm2 1 1 1 EC SA 2.51 cm2 11.58 cm2 5.66 cm2 >0.001* 0.734 0.019* SV 1.08 cm/s 1.83 cm/s 1.34 cm/s 0.002* 1 0.061 EC, foam SA 8.12 cm2 15.57 cm2 11.75 cm2 0.032* 0.499 1 SV 2.55 cm/s 2.96 cm/s 2.77 cm/s 0.625 1 0.751 d Saccadic SA 1.95 cm2 4.67 cm2 2.5 cm2 0.284 1 0.374 SV 1.09 cm/s 1.28 cm/s 1.08 cm/s 1 1 0.657 Optokinetic SA 2.12 cm2 9.57 cm2 4.43 cm2 >0.001* >0.001* 0.863 cte SV 1.07 cm/s 1.7 cm/s 1.25 cm/s 0.019* 1 0.072 Visual-vestibular interaction SA 4.43 cm2 7.95 cm2 5.45 cm2 0.845 1 0.996 SV 1.72 cm/s 1.96 cm/s 1.69 cm/s 1 1 1 LOS = Limit of stability; EC = eyes closed; EC, foam = Eyes closed, standing over foam mattress; SA = Sway area; SV = Sway Velocity; CPTM = chronic perforation of tympanic membrane; CSOM = Chronic suppurative otitis media; Cholesteatoma = presence of cholesteatoma, rre with or without active middle ear inflammation. The cells marked in gray and marked with a * refer to statistically significant difference in the results (P < 0.05). 317 95%CI, –0.150 – –0.541; P = 0.001), and a significant Comparative analysis between posturography 331 co 318 weak positive correlation between SVV and sway results and type of hearing loss showed that patients 332 319 velocity in the tests using a foam mattress (CC, 0.210; with mixed hearing loss had significantly worse 333 320 95%CI, 0.007–0.395; P = 0.049) and with the eyes sway area (eyes open, eyes closed, saccadic, optoki- 334 321 closed (CC, 0.241; 95%CI, 0.027–0.447; P = 0.023). netic and visual-vestibular integration) and sway 335 Un 322 In patients who complained of vestibular symptoms, velocity (eyes open, eyes closed, saccadic and 336 323 the sway velocity and sway area in most posturog- visual-vestibular integration) in several tests as com- 337 324 raphy tests (except the test using a foam-mattress) pared with patients with conductive hearing loss 338 325 were significantly worse as compared with patients (P < 0.05). In addition, we found a significant weak- 339 326 without vestibular symptoms (P < 0.05). We did not to-moderate negative correlation between PTA and 340 327 find significant correlations between posturography LOS in patients with COM (CC, –0.225; 95%CI, 341 328 results and laterality (unilateral or bilateral COM), –0.018 – –0.405; P = 0.027), and correlation was 342 329 abnormalities in the clinical vestibular tests, or the more powerful when including only CSOM and 343 330 presence of tinnitus (P > 0.05). cholesteatoma groups (CC, –0.352; 95%CI, –0.103 344  R. da Costa Monsanto et al. / Evaluation of vestibular symptoms and postural balance control 7 f roo rP Fig. 3. Boxplot graphics showing comparative analysis of posturography results (sway area, cm2 ; sway velocity, cm/s) under different stimuli. Legend: Eyes closed, foam = Patient stands on a foam mattress with eyes closed; Saccadic = patient stands on a firm platform with saccadic stimuli; Optokinetic = patient stands on a firm platform while subjected to optokinetic stimuli; and Visual-vestibular = patient stands on a firm platform, while subjected to visual (optokinetic) and vestibular (head rotation) stimuli. *=statistically significant difference as tho compared with the control group. 345 – –0.568; P = 0.009). We did not find significant cor- recent systematic review has identified several poten- 373 346 relations between PTA and remaining posturography tial biases in those studies, especially concerning 374 Au 347 parameters (P > 0.05). inclusion/exclusion criteria and lack of control for 375 348 Results of the video-HIT test showed no sig- confounding variables. Therefore, to the best of 376 349 nificant differences in the VOR gain or symmetry our knowledge, ours is the largest study dedicated 377 350 between COM (total and subgroups) and control to, based on a systematic research protocol, evaluate 378 351 groups (P > 0.05). We found abnormal results in prevalence of vestibular symptoms and postural con- 379 9 of 98 (9.1%) tests in the COM groups (2, uni- trol in patients with COM, potentially providing the d 352 380 353 lateral; 7, bilateral). The abnormalities were more best available evidence in this regard. 381 cte 354 frequent in the CSOM group (CPTM, 4.5%; CSOM, We found a high prevalence of vestibular symp- 382 355 23%; cholesteatoma, 7%; P > 0.05). The canals which toms among patients with COM (58.4%), which is 383 356 yielded abnormal results were the posterior in 4 consistent with previous reports – estimated preva- 384 357 patients and the lateral in 5. The saccades observed in lence ranged from 40–60% among studies. 385 358 the lateral canals were classified as covert saccades Among our COM subgroups, the presence of vestibu- 386 rre 359 in 4 and overt in 2 – both volunteers with overt sac- lar symptoms was significantly higher in the CSOM 387 360 cades had those seen in the clinical HIT test. None of and cholesteatoma groups as compared with the 388 361 the volunteers from the control group had abnormal CPTM groups. In addition, the most frequent trig- 389 362 video-HIT results. ger to those vestibular symptoms was the onset or 390 co worsening of ear suppuration. Therefore, those find- 391 ings suggest that frequency and severity of the middle 392 363 4. Discussion ear inflammation/infection may associate with the 393 development of vestibular symptoms. Histopatho- 394 Un 364 There has been some debate in the past years logic studies provide grounds to our hypothesis: it 395 365 whether or not COM leads to vestibular problems has been demonstrated that the degree of middle 396 366 [13, 34, 35, 45]. Recently, studies in human tem- ear inflammation and tissue abnormalities associate 397 367 poral bones have demonstrated significant decrease positively with the severity of damage affecting the 398 368 in the number of vestibular hair cells, especially in sensorial epithelium of the cochlea and vestibule [24, 399 369 the saccule and utricle, in bones with COM [13, 34, 35]. 400 370 24, 35]. Clinically, the sparse studies available in Among our patients with COM, the prevalence of 401 371 this regard demonstrated a variety of abnormalities hearing problems (92.8%) was higher as compared 402 372 in several vestibular function tests; however, a with the prevalence of vestibular symptoms (58.7%). 403  8 R. da Costa Monsanto et al. / Evaluation of vestibular symptoms and postural balance control 404 In this regard, it has been observed that the auditory icantly influence their results. Although several 456 405 sequela of COM seems to precede and be more severe articles demonstrated that the SVV frequently yields 457 406 than vestibular symptoms [9, 35]. It is also possible abnormal results in diseases affecting the peripheral 458 407 that a potential chronic, slow progression of vestibu- vestibular system in isolation , the role of the 459 408 lar or balance issues secondary to COM may allow SVV in diagnosing chronic, compensated vestibu- 460 409 adequate central compensation over time – in such lar disorders has not been extensively studied yet. 461 410 case, vestibular symptoms would mostly occur in the Assuming that the SVV somewhat reflects function 462 411 events of challenging situations or acute or severe of otolithic organs, our finding showing a significant 463 f 412 episodes of middle ear inflammation [9, 26, 34]. negative correlation between the SVV and LOS may 464 roo 413 The results of audiometry tests revealed that, suggest that those balance problems may be at least 465 414 among our patients with COM, 52.1% had mixed- partially attributable to otolithic dysfunction. 466 415 type hearing loss, which, in turn, associated with The results of posturography testing revealed 467 416 worse PTA and speech discrimination scores as com- worse limit of stability in all COM groups as com- 468 417 pared with conductive hearing loss (P < 0.05). Those pared with controls (P < 0.05). In groups with active 469 rP 418 results are consistent with extensive literature show- disease (CSOM and COM with active middle ear 470 419 ing similar findings [11, 19, 35, 37, 38]. In our study, inflammation), the sway area and sway velocity 471 420 some observations seemed to suggest a correlation in the majority of the posturography tests using 472 421 between the presence of mixed-type hearing loss with different stimuli were also significantly worse as 473 tho 422 postural balance problems and presence of vestibular compared with controls. Furthermore, we observed 474 423 symptoms: (1) among patients with mixed hearing that – among patients with COM and vestibular 475 424 loss, posturography results (LOS, sway velocity and symptoms – the LOS was significantly increased as 476 425 sway area) were significantly worse as compared with compared with patients with COM who did not have 477 426 patients with conductive hearing loss (P < 0.05); and vestibular symptoms. Although those findings point 478 Au 427 (2) the presence of tinnitus, which has been asso- toward worse postural control and potential vestibular 479 428 ciated with more intense degrees of cochlear hair impairment, posturography results should be inter- 480 429 cell loss and distal afferent dendrite degeneration preted with caution, considering that it assesses 481 430 [3, 32, 48], was more frequent among patients with “balance” rather than peripheral or central vestibular 482 431 mixed hearing loss, and associated with a two-fold function. Nonetheless, it has been demonstrated 483 increase in the risk of patients suffering from vestibu- that some of its tests (particularly tests which deprive d 432 484 433 lar symptoms (P < 0.05). To our knowledge, only patient from visual and somatosensorial informa- 485 cte 434 one histopathologic study demonstrated such com- tion) may grossly correlate with vestibular (mostly 486 435 bined degeneration of the sensorial epithelium of the otolithic) function. Considering those limita- 487 436 cochlea and vestibular structures secondary to COM tions, we observed that the most challenging test for 488 437. patients with COM was the foam-mattress test with 489 438 Clinical vestibular function tests showed a high eyes closed (which deprives the patients from visual 490 rre 439 number of abnormalities in patients with COM (63%) reference and proprioception), suggesting that some 491 440 as compared with controls (2%), and those correlated of those abnormalities could have occurred due to 492 441 positively with the presence of vestibular symptoms vestibular dysfunction [15, 27]. Although specula- 493 442 (P = 0.002). The abnormalities occurred mostly in tive, the observation of worse posturography results 494 co 443 tests directly or indirectly associated with the func- among groups with more severe middle ear inflam- 495 444 tion of otolithic organs and vestibulospinal reflex mation (CSOM and cholesteatoma) may suggest that 496 445 (Fukuda, SVV, Romberg) [8, 39]. Although the role COM may play a role in the development of those 497 446 of the Fukuda and Romberg tests in the diagnosis symptoms [9, 11, 13, 24, 35, 37, 46]. 498 Un 447 of vestibular disfunction has been described in the A noteworthy fact is that – although vestibu- 499 448 past [16, 43], further studies analyzing their sensitiv- lar symptoms and worse balance control generally 500 449 ity and reliability have disputed those assumptions, associated with presence of more intense hearing 501 450 especially in chronic, compensated vestibular disor- problems – the progression of hearing problems 502 451 ders [7, 21, 22]. The SVV test, on the other hand, seemed to occur regardless of the presence of vestibu- 503 452 is a simple, validated, and reliable way to assess lar/balance issues. Those findings may associate with 504 453 otolithic function. Although it may also suf- previous observations that hearing sequela of COM 505 454 fer influences of higher vestibular structures and is more frequent and more severe than vestibular 506 455 somatosensorial input, those do not seem to signif- sequela [9, 13]. In this regard, it has also been demon- 507  R. da Costa Monsanto et al. / Evaluation of vestibular symptoms and postural balance control 9 508 strated in the past that hearing loss in isolation may cally the number of potential volunteers. The use of 560 509 lead to worse postural control as compared with con- some relevant tests for analyzing vestibular function 561 510 trols, which could have been a confounding factor in (such as caloric tests and VEMPs) was not possi- 562 511 our study [23, 44, 49]. Although our methodology ble due to the negative influence of hearing loss 563 512 and tests may not allow adequate control for such and middle-ear conduction deficits in their results. 564 513 variable, some findings from our and other studies In addition, although the selected vestibular func- 565 514 suggest that hearing loss may not be the only fac- tion tests (video-HIT and posturography) are not 566 515 tor playing a role in the development of postural influenced by those factors, they have other inherent 567 f 516 balance problems: (1) among patients with COM, limitations in evaluating vestibular function: postur- 568 roo 517 the presence of sensorineural hearing loss which ography testing results do not directly correlate with 569 518 was more frequent in significantly associated with vestibular function , and video-HIT test seems 570 519 worse LOS as compared with patients with pure con- to have limitations to assess VOR abnormalities in 571 520 ductive hearing loss; and (2) histopathologic studies chronic, compensated vestibular disorders. It is 572 521 have demonstrated a significant positive correlation possible that – in the future – other vestibular function 573 rP 522 between the severity of loss of cochlear hair cells tests (such as rotational chair testing, videooculogra- 574 523 with loss of vestibular hair cells of temporal bones phy, dynamic posturography test, and dynamic SVV 575 524 with COM, suggesting that the inner ear damage sec- during centrifugation in the rotatory chair) may be 576 525 ondary to COM may affect the neuroepithelium of used to further assess vestibular function among 577 tho 526 both the cochlea and vestibule [13, 24, 35]. Thus, patients with COM. 578 527 is possible that the presence of inner ear damage 528 secondary to COM may also contribute with the 529 development of postural instability in patients with 5. Conclusion 579 530 COM. Au 531 We found no significant differences in the results Our study demonstrates that COM associates with 580 532 of the video-HIT between COM and control groups. a high prevalence of vestibular symptoms, abnormal- 581 533 We hypothesized 3 possible explanations for those ities in clinical vestibular function tests, and worse 582 534 findings: (1) the sensitivity of video-HIT may not postural control in the static posturography as com- 583 535 allow accurate detection of chronic, compensated pared with controls. Patients in COM groups with 584 abnormalities affecting the semicircular canals, ; signs of active middle ear inflammation (CSOM and d 536 585 537 (2) because VHIT measures the VOR at high fre- cholesteatoma with active middle ear inflammation) 586 cte 538 quency, it is possible that abnormalities affecting the seemed to be more symptomatic and have worse 587 539 semicircular canal function in the lower, and more postural control than patients in the group with less 588 540 physiologic, frequencies could have been missed frequent suppuration (CPTM). 589 541 ; and (3) semicircular canals may be less affected 542 by the inflammatory damages caused by COM than rre 543 the otolithic organs. The latter hypothesis is fur- Funding sources 590 544 ther supported by Chang et al. , who demonstrated 545 that, in COM, vestibular deficits are more signifi- Three authors (RCM, ALPK, TGAE) received 591 546 cant in the otolithic organs, while semicircular canal a scholarship from the the “Coordenação de 592 co 547 dysfunction occurs only in later stages. Aperfeiçoamento de Pessoal de Nı́vel Superior - 593 548 Our findings bear important clinical implications. Brasil (CAPES)” (Finance Code 001). 594 549 The clinical vestibular tests and posturography find- 550 ings suggest that patients with COM (especially Un 551 elderly) may be at an increased risk of disequilib- Conflicts of interest 595 552 rium and falls, which is a major cause of morbidity 553 and mortality [35, 50]. Considering that COM is one None to declare. 596 554 of the leading causes of hearing impairment [25, 33], 555 postural balance problems may constitute an addi- 556 tional burden to patients with COM. Acknowledgments 597 557 Our study has some limitations. First, the strict- 558 ness of our exclusion criteria (which is one of the We thank Flavia Salvaterra Cusin for the great 598 559 main strengths of our study) has reduced drasti- technical support; Grace Sinae Park for critically 599  10 R. da Costa Monsanto et al. / Evaluation of vestibular symptoms and postural balance control 600 reviewing the manuscript; and the “Coordenação de S.S. da Costa, L.P.S. Rosito and C. Dornelles, Sen- 659 601 Aperfeiçoamento de Pessoal de Nı́vel Superior - sorineural hearing loss in patients with chronic otitis 660 media, Eur Arch Otorhinolaryngol 266(2) (2009), 221–224. 661 602 Brasil (CAPES)” (Finance Code 001) for partially https://doi.org/10.1007/s00405-008-0739-0 662 603 financing this study. C. Fujimoto, T. Murofushi, Y. Chihara, M. Ushio, K. 663 Sugasawa, T. Yamaguchi, T. Yamasoba and S. 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