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Video head impulse test in children with otitis media with effusion and dizziness
International Journal of Pediatric Otorhinolaryngology 129 (2020) 109783
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Video head impulse test in children with otitis media with effusion and dizziness
T
Mesut Tozara, Ela Cömerta,∗, Ziya Şencana, Gökçe Şimşeka, Nuray Bayar Muluka, Rahmi Kılıçb a b
Kırıkkale University Faculty of Medicine, Department of Otolaryngology, 1st Floor, Yenişehir, Yahşihan, Kırıkkale, Turkey Ankara Education and Research Hospital, Clinic of Otolaryngology Sakarya Mh. Ulucanlar Street No 89 Altındağ, Ankara, Turkey
A R T I C LE I N FO
A B S T R A C T
Keywords: Video head impulse test Otitis media with effusion Vestibular impairment
Objective: The objectives of the study were to evaluate the vestibular impairment in children with otitis media with effusion (OME) and dizziness by using vHIT test, and to compare their results with healthy children. Methods: The study population consisted of 30 pediatric patients with OME and dizziness and 30 healthy children, age between 4 and 15. Otoscopic and tympanometric examination and vHIT testing were performed to all subjects. vHIT test parameters were compared between pediatric patients with OME and dizziness and healthy children. Additionally, the differences of the mean vHIT gains between tympanogram types, otoscopic findings and the presence of saccades were analyzed. Results: The mean vHIT gains and gain asymmetry values of patients with OME and dizziness and healthy children were comparable. No significant difference was observed between the mean vHIT gains of patients with type B and type C2 tympanogram. Covert saccades were observed in 57% of the patients with OME and dizziness. None of the patients had over saccades and none of the healthy children had saccades. Conclusion: Our study is a preliminary study analyzing the vestibular impairment in children with OME and dizziness using vHIT test. Based on our results, it can be assumed that the children with OME and dizziness usually don't have a great vestibular impairment that can be detected with vHIT test. The covert saccades detected in this patient group are accepted as a sign of slight vestibular impairment.
1. Introduction Otitis media with effusion (OME) is the presence of effusion in the middle ear cavity without signs of ear infection [1]. Acute suppurative otitis media (ASOM) is the main cause of OME in children. Approximately 60% of the children have had one or more episodes of ASOM before the age of 4 years and the tympanometric screening of those children reveal type C2 or B pattern in 46% [2]. OME is usually diagnosed by the physician through a physical examination and a review of the child's medical history. Although most of these children do not have any complaints, their parents usually describe hearing impairment as well as clumsiness, awkwardness and frequent fallings [3]. Previous studies revealed that these complains about balance could originate from vestibular dysfunction [4–7]. Approximately 30% of the children with OME have some degree of vestibular impairment documented with vestibular tests [8,9]. Acute labyrinthitis, negative middle-ear pressure changes and the changes of the composition of the endolymph and perilymph with the ionic transfer through the round window membrane
are thought to be the reasons of the vestibular loss [10,11]. The diagnosis of vestibular dysfunction from the medical interview is difficult and clinical and neurophysiological vestibular tests are not uniformly reliable in these patients [12]. It has been demonstrated that the children with OME are more visually dependent for balance than healthy children especially for higher-frequency stimulus conditions [13]. The video-head impulse test (vHIT) is a recent technique for the functional evaluation of semicircular canals (SSC). vHIT test examines the eye movements at high frequencies of stimulation [14] and it offers an objective assessment of the function of the high frequency domain of the vestibular system [15]. Based on this information, it may be hypothesized that vHIT will be an important test for the investigation of the balance problems of children with OME. The present study aimed to evaluate the vestibular impairment in children with OME and dizziness by using vHIT test and to compare their results with healthy children.
∗
Corresponding author. E-mail addresses: [email protected] (M. Tozar), [email protected] (E. Cömert), [email protected] (Z. Şencan), [email protected] (G. Şimşek), [email protected] (N.B. Muluk), [email protected] (R. Kılıç). https://doi.org/10.1016/j.ijporl.2019.109783 Received 13 September 2019; Received in revised form 25 October 2019; Accepted 14 November 2019 Available online 18 November 2019 0165-5876/ © 2019 Elsevier B.V. All rights reserved.
International Journal of Pediatric Otorhinolaryngology 129 (2020) 109783
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2. Methods
GA = (R - L) / (R + L)
The study protocol was approved by the institutional review board of the institute and has been carried out in accordance with The Code of Ethics of the World Medical Association (Declaration of Helsinki). All subjects provided written informed consent to participate in the study.
The “R” and “L” indicate the mean gain values for impulses to the right (R) and left (L) side. The catch-up saccades were analyzed. The saccade which occurred during the head movement was considered as a covert saccade. The overt saccade was defined as the saccade occurred after the head movement crossed zero [16].
2.1. Patients
3. Statistical analysis
The study included two groups of subjects, age between 4 and 15. The patient group (Group 1) consisted of 30 patients (15 girls and 15 boys) with a mean age (SD) 8.5 (1.9) who had OME without a history of AOM in the last 3 months and admitted to the clinic with the complaint of dizziness between July 2015–July 2018. OME was defined as the presence of middle-ear effusion for more than 3 months and the diagnosis was based on the patients’ tympanometric follow-up. The criteria for qualifying subjects for Group 1 were bilateral type B or C2 tympanogram curves, typical OME symptoms in otoscopy and complaint of dizziness either from parents or from the child. Children more than 15 or less than 4 years of age, children who had an additional systemic, neurologic or vestibular disease, who were taking medication that could potentially affect saccadic performance, who had an abnormal vision and who could not cooperate on vHIT test were excluded from the study. The control group (Group 2) included 30 healthy children (15 girls and 15 boys) with a mean age (SD) 8.2 (2) who had normal otoscopic and tympanometric evaluation with no history of AOM in the last 3 months. Otoscopic and tympanometric examination and vHIT testing were performed to all subjects. Group 1 patients were also divided into subgroups according to their otoscopic and tympanometric findings.
The Shapiro-Wilk test was used to determine the distribution of homogeneity and normality of the study values. The values that distributed homogenously and normally called parametric values were expressed as mean ± standard deviation and the values that distributed not homogenously and normally called non-parametric values were expressed as median (minimum-maximum). The mean vHIT gains and GA values were given as arithmetic mean ± standard deviation or median (minimum-maximum). The mean vHIT gains and GA values between groups for each canal were compared with the Mann-Whitney U test (for values of canals with non-parametric distribution) and Independent sample t-test (for values of canals with parametric distribution). The differences of the mean vHIT gains between tympanogram types, otoscopic findings and the presence of covert saccades were analyzed using the Mann-Whitney U test (for gain values of canals with non-parametric distribution) and Independent Samples t-test (for gain values of canals with parametric distribution). A significance level of p < 0.05 for all testing was used. All analyses were performed by SPSS for Windows, version 16.0 (SPSS Inc, an IBM Company, Chicago, Illinois).
2.2. vHIT
4. Results
The vHIT system consists of a light-weight pair of goggles integrated with a video-oculography (VOG) system (EyeSee Cam™ system Interacoustics A/S Denmark™) that consists of a high speed infrared camera (sampling rate of 250 Hz) which measures 2-D eye movements and a built-in accelerometer. The goggle is fixed to the head with a rubber band and the image of the patient's eye is reflected into the camera by a mirror. The setting and the procedure were performed in accordance with the description of Hamilton et al. [16]. The clinical head impulse test was accomplished first to explain the vHIT test procedure to the children and their parents. Before the procedure, calibration was performed to ensure accurate recording. Subjects were seated in the upright position in an adjustable height chair and focused on a visual target positioned at eye level on a plane wall 1 m away. Patients were adopted to minimize eye blinking, leave his/her head alone and focus their eye on the target during head trust maneuvers on each SSC planes. Maneuvers were performed on 6 SSC planes for each patient as described by McGarvie et al. [17]. Horizontal canal testing was applied in the horizontal plane. Vertical canal testing was performed during the head rotated 30° towards the right or left side, and the head impulse was applied in the plane of canals. Target head velocity was set to 100–200° per second with amplitude between 5 and 15° from center to lateral. The impulses were unpredictable for both directions (right versus left). The device evaluated whether the head thrust was within acceptable limits by a green check or red cross on the measurement screen. At least 15 impulses with a green check to each side were obtained. All 60 children were tested by either of two examiners who were at least 2 years experienced in clinical vestibular testing. The vHIT gain was calculated by the software for each semicircular canal as the ratio of peak slow phase eye velocity to peak head velocity at 80 ms. Gain asymmetry (GA) was calculated for vertical and horizontal canals for all subjects and defined as:
The mean ± SD or median (min-max) values of vHIT gains of Group 1 and Group 2 are presented in Table 1. No statistically significant difference was detected between groups when comparing vHIT gains of each canal (Fig. 1). When evaluated in terms of otoscopic findings, bilateral matte tympanic membrane was detected in 24 patients and bilateral retracted tympanic membrane in 6 patients in Group 1. All the children in Group 2 had a normal tympanic membrane. When comparing otoscopic findings and vHIT gains in Group 1, the differences were not significant between patients with matte and retracted tympanic membrane. Data are presented in Table 2. The tympanometry results were examined separately for each ear. Among the 60 ears in Group 1, tympanometry revealed type B tympanogram in 50 ears and type C2 tympanogram in 10 ears. All the ears of the children in Group 2 had type A tympanogram. When comparing tympanometry types and vHIT gains in Group 1, the differences were not significant. Data are presented in Table 3. Table 1 vHIT gains by groups. Mann Whitney U test, Independent Samples t-test p < 0.05 Group 1 vHIT gains
Group 2 vHIT gains
Mean ± SD/Median (min-max)
Mean ± SD/Median (min-max)
t/Z
p
0.83 1.11 0.78 0.87 0.71 0.89
0.86 1.06 0.95 0.95 0.97 0.95
−0.739 0.876* −0.649 0.300* −0.362 1.466*
0.460 0.385** 0.099 0.765** 0.717 0.148**
Canals
R ASC R LSC R PSC L ASC L LSC L PSC
(0.30–1.13) ± 0.19 (0.28–1.14) ± 0.25 (0.12–1.02) ± 0.32
(0.71–1.26) ± 0.22 (0.87–1.35) ± 0.22 (0.73–1.35) ± 0.23
vHIT, video head impulse test; R, right; L, left; ASC, anterior semicircular canal; LSC, lateral semicircular canal; PSC, posterior semicircular canal; *, t value; **, Independent Samples t-test. 2
International Journal of Pediatric Otorhinolaryngology 129 (2020) 109783
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Table 4 Comparison of vHIT gains among patients with and without saccades in Group 1. Mann Whitney U test p < 0.05 Canals
Number of saccades
Z
p
R ASC R LSC R PSC L ASC L PSC
6 4 1 1 12
−3.008 −2.168 −1.561 −1.445 −4.446
0.003 0.030 0.118 0.148 < 0.001
vHIT, video head impulse test; R, right; L, left; ASC, anterior semicircular canal; LSC, lateral semicircular canal; PSC, posterior semicircular canal.
GA was calculated for vertical and horizontal canals for both groups. The median (minimum-maximum) values of GA of Group 1 and Group 2 for horizontal canals were 0.02 (0–0.08) and 0.03 (0–0.2) respectively. No statistically significant difference was detected between groups when comparing GA values (Z = −0.299, p = 0.765). The median (minimum-maximum) values of GA of Group 1 and Group 2 for anterior canals were 0.09 (0–0.23) and 0.16 (0–0.24) respectively. No statistically significant difference was detected between groups when comparing GA values (Z = −1.835, p = 0.067). The median (minimum-maximum) values of GA of Group 1 and Group 2 for posterior canals were 0.08 (0–0.25) and 0.08 (0–0.21) respectively. No statistically significant difference was detected between groups when comparing GA values (Z = −0.282, p = 0.778).
Fig. 1. Boxplot of vHIT gains correlated with Group 1 and Group 2 (data represented as median or mean, 95% CI and interquartile ranges; no significant difference was detected between groups, Mann Whitney U test, Independent Samples t-test, p < 0.05).
5. Discussion
Table 2 Comparison of the vHIT gains according to otoscopic findings (matte and retracted) among Group 1. Mann Whitney U test, Independent Samples t-test p < 0.05 Canals
t/Z
p
R ASC R LSC R PSC L ASC L LSC L PSC
1.889* −0.727 0.267* −1.042* −0.415* −0.467
0.069** 0.467 0.792** 0.306** 0.681** 0.641
The effect of OME on the vestibular system has been investigated in many studies [6–8,10,18]. Both vestibuloocular reflex (VOR) and vestibulospinal reflex are affected by this pathology. The tests for evaluation of vestibular function during otitis media included electronystagmography (ENG), caloric tests, Vestibular Evoked Myogenic Potentials (VEMP), dynamic and static posturography, sway magnetometry, craniocorpography, and the subjective vertical visual [8]. Most of the studies analyze the effect of OME on vestibulospinal reflex, as most of these tests are relatively easy to do in children and do not stimulate the ear canal [6,18,19]. The ENG analysis is one of the most preferred and reliable test that assesses VOR for the presence of vestibular organ disturbances in the children with OME [7,20]. In ENG test, 25–60% of the patients with OME have peripheral vestibular abnormalities [9,19]. However, there are problems with the reliability of other tests evaluating VOR in this patient group. Caloric test and VEMP are negatively influenced by the presence of middle-ear effusion [8]. VEMP test with air conducted stimuli does not reveal detectable responses in most of the patients with OME, as the impairment of the sound transmission due to middle ear pathology affects air conducted VEMP results [19]. VEMP results with bone conducted stimuli vary greatly among studies [8]. The vHIT test is an objective measure for VOR that allows us to keep our visual field in focus during head movement by maintaining an opposite and equal eye movement. It examines the eye movements at high frequencies of stimulation and provides accurate canal and side specific information without stimulating vertigo. Many studies demonstrate its effectiveness in detecting SSC dysfunction in adults [15,21]. Recent studies support that the vHIT test is a sensitive and efficient vestibular test in the pediatric population as well [16,22]. It is well tolerated by children aged 3–16 years [16] and introduced as a child friendly, relatively easy-to-use, and simple tool to evaluate each of the 6 SSCs [14]. The efficacy of VOR in vHIT test is defined by either the gain of the eye movement to the corresponding head movement, called vHIT gain or by the presence of corrective catch up saccades [23]. In case of VOR impairment, the eye movement cannot be proportional to the head movement, vHIT gain decreases and a corrective eye movement appears
vHIT, video head impulse test; R, right; L, left; ASC, anterior semicircular canal; LSC, lateral semicircular canal; PSC, posterior semicircular canal; *, t value; **, Independent Samples t-test. Table 3 Comparison of the vHIT gains according to tympanogram types (type B and type C2) among Group 1. Mann Whitney U test, Independent Samples t-test p < 0.05 Canals
t/Z
p
R ASC R LSC R PSC L ASC L LSC L PSC
0.622* 2.017* −1.618 −0.610* −0.484 −0.364*
0.539** 0.053** 0.106 0.547** 0.628 0.719**
vHIT, video head impulse test; R, right; L, left; ASC, anterior semicircular canal; LSC, lateral semicircular canal; PSC, posterior semicircular canal; *, t value; **, Independent Samples t-test.
In Group 1, 24 covert saccades were determined in 17 patients (1–4 saccades per patient) in every canal except left lateral SSC plane. None of the patients had covert saccades in Group 2. None of the patients in both groups had overt saccade. vHIT gains of right anterior SSC, lateral SSC and left posterior SSC were significantly lower when saccades were present. The distribution of saccades among canals and comparison of vHIT gains among patients with and without saccades in Group 1 are presented in Table 4. 3
International Journal of Pediatric Otorhinolaryngology 129 (2020) 109783
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in the pediatric population because of its stimulation effect of the vestibular system. Based on our results, it can be assumed that the children with OME and dizziness usually don't have a great vestibular impairment that can be detected with the vHIT test. The VOR gains of these patients are compatible with healthy children and none of them have overt saccades. The covert saccades detected in this patient group are accepted as a sign of slight vestibular impairment as none of the healthy children had saccades. Although the patients have OME bilaterally, this vestibular impairment does not involve both labyrinths equally or affects the entire labyrinth. It should be also kept in mind that the vHIT test evaluates high-frequency head movements and any dizziness due to vestibular function may be a function of impact on lower frequencies of movement that cannot be detected in the vHIT test.
to re-fixate the eye back to the target. vHIT gain is nearly 1 in healthy individuals. vHIT gains of the pediatric population tend to be between 0.7 and 1 and gains below 0.7 and presence of corrective saccades are considered to be pathologic [16,17]. The main differences of vHIT test in children consist of slower peak head velocity and the need for more trials to obtain valid impulses [22]. Additionally, children have difficulty maintaining gaze along the plane of the vertical canals [22]. In most reports, the diagnostic value of vHIT was evaluated based on the caloric test [24]. It has been documented that the VOR gain of the affected ear and GA have a significant linear relationship with unilateral weakness in the caloric test [24]. vHIT is also complementary to caloric testing especially with normal findings in caloric testing [14]. The sensitivity and specificity of vHIT in patients with unilateral vestibular loss were reported as 78% and 85% respectively [24]. However, the studies point out that the vHIT is not as sensitive as the bithermal caloric test in detecting loss of vestibular dysfunction, especially in the pediatric population [22]. To the best of our knowledge, we present the first report providing detailed information about the results of vHIT test in children with OME and dizziness. Besides, the control group in our study demonstrated the results of the vHIT test in the healthy pediatric population. The literature recently focusses on the normative findings of vHIT test in the pediatric population [16,17,25]. Previous reports reveal that VOR gains among different age groups are comparable and when compared with adults, left anterior and right posterior SSC gains are lower in children. It is also mentioned that a large amount of variability exists in the data during vertical canal testing for both healthy children and adults [26]. The vHIT gains of our healthy subjects are comparable with the literature and our study supports that vHIT gains can be variable in a great range for both vertical and horizontal SSCs in the pediatric population. Our study reveals that the vHIT gains of all SSCs do not significantly decrease in children with OME and dizziness when compared with healthy subjects. GA values of children with OME and dizziness are also compatible with healthy children for both vertical and horizontal canals. However, vestibular weakness is expected to cause a decrease in VOR gains and an increase in GA values [24]. When considering the otoscopic examination, no significant difference is found between vHIT gains of children with the matte and retracted eardrum. vHIT gains of patients with type B and type C2 tympanogram are also comparable. The main finding in the vHIT test of children with OME and dizziness is the presence of covert saccades. Covert saccades are detected in 57% of the children with OME and dizziness. This result is difficult to interpret as a sign of vestibular impairment as previous studies indicate that both overt and covert saccades can be observed in about half of the healthy subjects with no significant difference among age, suggesting that VOR is a hypometric system [26]. Additionally, it has been shown that overt saccades are the main saccades that are seen in greater vestibular impairment [24]. None of the children in our study has overt saccade. However, the absence of cover saccade in any of the healthy children lead to the evaluation of covert saccades observed in the patient group in favor of vestibular involvement. It is also open to debate why saccades are more common in the right anterior and left posterior canal directions. Pathologies assumed as the causes of vestibular impairment during OME are expected to affect the entire labyrinth. However, previous studies demonstrated that cochlear impairment also did not involve all the frequencies, sensorineural hearing loss developed only at one frequency in most of the patients with OME, especially at 2 kHz [27]. On the other hand, it is difficult to acquire head impulse in the plane of vertical canals in the pediatric population and the main reason for this result may be the higher variability of vHIT parameters in vertical canals when compared with the horizontal canal. The major drawback of our study is that an additional vestibular test could be used to support the results of vHIT. ENG with the caloric test could be complementary to vHIT test in this patient group. We don't prefer combining vHIT with the caloric test as we don't use caloric test
6. Conclusions Our study is a preliminary study analyzing the vestibular impairment in children with OME and dizziness using the vHIT test. vHIT can be the preferred test for the vestibular evaluation of the pediatric population with OME as it isn't affected by the middle ear effusion and doesn't stimulate vertigo. However, the vHIT test is a limited test to identify all forms of vestibular loss and parameters in the normal range may not be indicative of the absence of vestibular dysfunction. Funding This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. Declaration of competing interest None. Acknowledgments None. References [1] S.S. O'Connor, R. Coggins, L. Gagnon, R.M. Rosenfeld, J.J. Shin, S.A. Walsh, Plain language summary: otitis media with effusion, Otolaryngol. Head Neck Surg. 154 (2) (2016) 215–225, https://doi.org/10.1177/0194599815624409. [2] S.E. Stangerup, M. Tos, The etiologic role of acute suppurative otitis media in chronic secretory otitis, Am. J. Otol. 6 (2) (1985) 126–131. [3] F.M. Gioacchini, M. Alicandri-Ciufelli, S. Kaleci, G. Magliulo, M. Re, Prevalence and diagnosis of vestibular disorders in children: a review, Int. J. Pediatr. Otorhinolaryngol. 78 (5) (2014) 718–724, https://doi.org/10.1016/j.ijporl.2014. 02.009. [4] A.W. Blayney, B.H. Colman, Dizziness in childhood, Clin. Otolaryngol. Allied Sci. 9 (2) (1984) 77–85. [5] M.L. Casselbrant, J.M. Furman, E. Rubenstein, E.M. Mandel, Effect of otitis media on the vestibular system in children, Ann. Otol. Rhinol. Laryngol. 104 (8) (1995) 620–624, https://doi.org/10.1177/000348949510400806. [6] A. Golz, B. Angel-Yeger, S. Parush, Evaluation of balance disturbances in children with middle ear effusion, Int. J. Pediatr. Otorhinolaryngol. 43 (1) (1998) 21–26, https://doi.org/10.1016/s0165-5876(97)00150-x. [7] K. Pazdro-Zastawny, L. Pośpiech, T. Zatoński, Long-term evaluation of the effect of middle ear effusion on the vestibular system in children, Int. J. Pediatr. Otorhinolaryngol. 109 (2018) 13–16, https://doi.org/10.1016/j.ijporl.2018.03. 015. [8] R.D.C. Monsanto, A.L.P. Kasemodel, A. Tomaz, M.M. Paparella, N.O. Penido, Current evidence of peripheral vestibular symptoms secondary to otitis media, Ann. Med. 50 (5) (2018) 391–401, https://doi.org/10.1080/07853890.2018.1470665. [9] M. Koyuncu, M.M. Saka, Y. Tanyeri, T. Seşen, R. Unal, A. Tekat, F. Yilmaz, Effects of otitis media with effusion on the vestibular system in children, Otolaryngol. Head Neck Surg. 120 (1) (1999) 117–121, https://doi.org/10.1016/S0194-5998(99) 70381-5. [10] E.A. Kolkaila, A.A. Emara, T.A. Gabr, Vestibular evaluation in children with otitis media with effusion, J. Laryngol. Otol. 129 (4) (2015) 326–336, https://doi.org/10. 1017/S0022215115000535. [11] N.S. Jones, P. Radomskij, A.J. Prichard, S.E. Snashall, Imbalance and chronic secretory otitis media in children: effect of myringotomy and insertion of ventilation
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International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Video head impulse test in children with otitis media with effusion and dizziness
T
Mesut Tozara, Ela Cömerta,∗, Ziya Şencana, Gökçe Şimşeka, Nuray Bayar Muluka, Rahmi Kılıçb a b
Kırıkkale University Faculty of Medicine, Department of Otolaryngology, 1st Floor, Yenişehir, Yahşihan, Kırıkkale, Turkey Ankara Education and Research Hospital, Clinic of Otolaryngology Sakarya Mh. Ulucanlar Street No 89 Altındağ, Ankara, Turkey
A R T I C LE I N FO
A B S T R A C T
Keywords: Video head impulse test Otitis media with effusion Vestibular impairment
Objective: The objectives of the study were to evaluate the vestibular impairment in children with otitis media with effusion (OME) and dizziness by using vHIT test, and to compare their results with healthy children. Methods: The study population consisted of 30 pediatric patients with OME and dizziness and 30 healthy children, age between 4 and 15. Otoscopic and tympanometric examination and vHIT testing were performed to all subjects. vHIT test parameters were compared between pediatric patients with OME and dizziness and healthy children. Additionally, the differences of the mean vHIT gains between tympanogram types, otoscopic findings and the presence of saccades were analyzed. Results: The mean vHIT gains and gain asymmetry values of patients with OME and dizziness and healthy children were comparable. No significant difference was observed between the mean vHIT gains of patients with type B and type C2 tympanogram. Covert saccades were observed in 57% of the patients with OME and dizziness. None of the patients had over saccades and none of the healthy children had saccades. Conclusion: Our study is a preliminary study analyzing the vestibular impairment in children with OME and dizziness using vHIT test. Based on our results, it can be assumed that the children with OME and dizziness usually don't have a great vestibular impairment that can be detected with vHIT test. The covert saccades detected in this patient group are accepted as a sign of slight vestibular impairment.
1. Introduction Otitis media with effusion (OME) is the presence of effusion in the middle ear cavity without signs of ear infection [1]. Acute suppurative otitis media (ASOM) is the main cause of OME in children. Approximately 60% of the children have had one or more episodes of ASOM before the age of 4 years and the tympanometric screening of those children reveal type C2 or B pattern in 46% [2]. OME is usually diagnosed by the physician through a physical examination and a review of the child's medical history. Although most of these children do not have any complaints, their parents usually describe hearing impairment as well as clumsiness, awkwardness and frequent fallings [3]. Previous studies revealed that these complains about balance could originate from vestibular dysfunction [4–7]. Approximately 30% of the children with OME have some degree of vestibular impairment documented with vestibular tests [8,9]. Acute labyrinthitis, negative middle-ear pressure changes and the changes of the composition of the endolymph and perilymph with the ionic transfer through the round window membrane
are thought to be the reasons of the vestibular loss [10,11]. The diagnosis of vestibular dysfunction from the medical interview is difficult and clinical and neurophysiological vestibular tests are not uniformly reliable in these patients [12]. It has been demonstrated that the children with OME are more visually dependent for balance than healthy children especially for higher-frequency stimulus conditions [13]. The video-head impulse test (vHIT) is a recent technique for the functional evaluation of semicircular canals (SSC). vHIT test examines the eye movements at high frequencies of stimulation [14] and it offers an objective assessment of the function of the high frequency domain of the vestibular system [15]. Based on this information, it may be hypothesized that vHIT will be an important test for the investigation of the balance problems of children with OME. The present study aimed to evaluate the vestibular impairment in children with OME and dizziness by using vHIT test and to compare their results with healthy children.
∗
Corresponding author. E-mail addresses: [email protected] (M. Tozar), [email protected] (E. Cömert), [email protected] (Z. Şencan), [email protected] (G. Şimşek), [email protected] (N.B. Muluk), [email protected] (R. Kılıç). https://doi.org/10.1016/j.ijporl.2019.109783 Received 13 September 2019; Received in revised form 25 October 2019; Accepted 14 November 2019 Available online 18 November 2019 0165-5876/ © 2019 Elsevier B.V. All rights reserved.
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2. Methods
GA = (R - L) / (R + L)
The study protocol was approved by the institutional review board of the institute and has been carried out in accordance with The Code of Ethics of the World Medical Association (Declaration of Helsinki). All subjects provided written informed consent to participate in the study.
The “R” and “L” indicate the mean gain values for impulses to the right (R) and left (L) side. The catch-up saccades were analyzed. The saccade which occurred during the head movement was considered as a covert saccade. The overt saccade was defined as the saccade occurred after the head movement crossed zero [16].
2.1. Patients
3. Statistical analysis
The study included two groups of subjects, age between 4 and 15. The patient group (Group 1) consisted of 30 patients (15 girls and 15 boys) with a mean age (SD) 8.5 (1.9) who had OME without a history of AOM in the last 3 months and admitted to the clinic with the complaint of dizziness between July 2015–July 2018. OME was defined as the presence of middle-ear effusion for more than 3 months and the diagnosis was based on the patients’ tympanometric follow-up. The criteria for qualifying subjects for Group 1 were bilateral type B or C2 tympanogram curves, typical OME symptoms in otoscopy and complaint of dizziness either from parents or from the child. Children more than 15 or less than 4 years of age, children who had an additional systemic, neurologic or vestibular disease, who were taking medication that could potentially affect saccadic performance, who had an abnormal vision and who could not cooperate on vHIT test were excluded from the study. The control group (Group 2) included 30 healthy children (15 girls and 15 boys) with a mean age (SD) 8.2 (2) who had normal otoscopic and tympanometric evaluation with no history of AOM in the last 3 months. Otoscopic and tympanometric examination and vHIT testing were performed to all subjects. Group 1 patients were also divided into subgroups according to their otoscopic and tympanometric findings.
The Shapiro-Wilk test was used to determine the distribution of homogeneity and normality of the study values. The values that distributed homogenously and normally called parametric values were expressed as mean ± standard deviation and the values that distributed not homogenously and normally called non-parametric values were expressed as median (minimum-maximum). The mean vHIT gains and GA values were given as arithmetic mean ± standard deviation or median (minimum-maximum). The mean vHIT gains and GA values between groups for each canal were compared with the Mann-Whitney U test (for values of canals with non-parametric distribution) and Independent sample t-test (for values of canals with parametric distribution). The differences of the mean vHIT gains between tympanogram types, otoscopic findings and the presence of covert saccades were analyzed using the Mann-Whitney U test (for gain values of canals with non-parametric distribution) and Independent Samples t-test (for gain values of canals with parametric distribution). A significance level of p < 0.05 for all testing was used. All analyses were performed by SPSS for Windows, version 16.0 (SPSS Inc, an IBM Company, Chicago, Illinois).
2.2. vHIT
4. Results
The vHIT system consists of a light-weight pair of goggles integrated with a video-oculography (VOG) system (EyeSee Cam™ system Interacoustics A/S Denmark™) that consists of a high speed infrared camera (sampling rate of 250 Hz) which measures 2-D eye movements and a built-in accelerometer. The goggle is fixed to the head with a rubber band and the image of the patient's eye is reflected into the camera by a mirror. The setting and the procedure were performed in accordance with the description of Hamilton et al. [16]. The clinical head impulse test was accomplished first to explain the vHIT test procedure to the children and their parents. Before the procedure, calibration was performed to ensure accurate recording. Subjects were seated in the upright position in an adjustable height chair and focused on a visual target positioned at eye level on a plane wall 1 m away. Patients were adopted to minimize eye blinking, leave his/her head alone and focus their eye on the target during head trust maneuvers on each SSC planes. Maneuvers were performed on 6 SSC planes for each patient as described by McGarvie et al. [17]. Horizontal canal testing was applied in the horizontal plane. Vertical canal testing was performed during the head rotated 30° towards the right or left side, and the head impulse was applied in the plane of canals. Target head velocity was set to 100–200° per second with amplitude between 5 and 15° from center to lateral. The impulses were unpredictable for both directions (right versus left). The device evaluated whether the head thrust was within acceptable limits by a green check or red cross on the measurement screen. At least 15 impulses with a green check to each side were obtained. All 60 children were tested by either of two examiners who were at least 2 years experienced in clinical vestibular testing. The vHIT gain was calculated by the software for each semicircular canal as the ratio of peak slow phase eye velocity to peak head velocity at 80 ms. Gain asymmetry (GA) was calculated for vertical and horizontal canals for all subjects and defined as:
The mean ± SD or median (min-max) values of vHIT gains of Group 1 and Group 2 are presented in Table 1. No statistically significant difference was detected between groups when comparing vHIT gains of each canal (Fig. 1). When evaluated in terms of otoscopic findings, bilateral matte tympanic membrane was detected in 24 patients and bilateral retracted tympanic membrane in 6 patients in Group 1. All the children in Group 2 had a normal tympanic membrane. When comparing otoscopic findings and vHIT gains in Group 1, the differences were not significant between patients with matte and retracted tympanic membrane. Data are presented in Table 2. The tympanometry results were examined separately for each ear. Among the 60 ears in Group 1, tympanometry revealed type B tympanogram in 50 ears and type C2 tympanogram in 10 ears. All the ears of the children in Group 2 had type A tympanogram. When comparing tympanometry types and vHIT gains in Group 1, the differences were not significant. Data are presented in Table 3. Table 1 vHIT gains by groups. Mann Whitney U test, Independent Samples t-test p < 0.05 Group 1 vHIT gains
Group 2 vHIT gains
Mean ± SD/Median (min-max)
Mean ± SD/Median (min-max)
t/Z
p
0.83 1.11 0.78 0.87 0.71 0.89
0.86 1.06 0.95 0.95 0.97 0.95
−0.739 0.876* −0.649 0.300* −0.362 1.466*
0.460 0.385** 0.099 0.765** 0.717 0.148**
Canals
R ASC R LSC R PSC L ASC L LSC L PSC
(0.30–1.13) ± 0.19 (0.28–1.14) ± 0.25 (0.12–1.02) ± 0.32
(0.71–1.26) ± 0.22 (0.87–1.35) ± 0.22 (0.73–1.35) ± 0.23
vHIT, video head impulse test; R, right; L, left; ASC, anterior semicircular canal; LSC, lateral semicircular canal; PSC, posterior semicircular canal; *, t value; **, Independent Samples t-test. 2
International Journal of Pediatric Otorhinolaryngology 129 (2020) 109783
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Table 4 Comparison of vHIT gains among patients with and without saccades in Group 1. Mann Whitney U test p < 0.05 Canals
Number of saccades
Z
p
R ASC R LSC R PSC L ASC L PSC
6 4 1 1 12
−3.008 −2.168 −1.561 −1.445 −4.446
0.003 0.030 0.118 0.148 < 0.001
vHIT, video head impulse test; R, right; L, left; ASC, anterior semicircular canal; LSC, lateral semicircular canal; PSC, posterior semicircular canal.
GA was calculated for vertical and horizontal canals for both groups. The median (minimum-maximum) values of GA of Group 1 and Group 2 for horizontal canals were 0.02 (0–0.08) and 0.03 (0–0.2) respectively. No statistically significant difference was detected between groups when comparing GA values (Z = −0.299, p = 0.765). The median (minimum-maximum) values of GA of Group 1 and Group 2 for anterior canals were 0.09 (0–0.23) and 0.16 (0–0.24) respectively. No statistically significant difference was detected between groups when comparing GA values (Z = −1.835, p = 0.067). The median (minimum-maximum) values of GA of Group 1 and Group 2 for posterior canals were 0.08 (0–0.25) and 0.08 (0–0.21) respectively. No statistically significant difference was detected between groups when comparing GA values (Z = −0.282, p = 0.778).
Fig. 1. Boxplot of vHIT gains correlated with Group 1 and Group 2 (data represented as median or mean, 95% CI and interquartile ranges; no significant difference was detected between groups, Mann Whitney U test, Independent Samples t-test, p < 0.05).
5. Discussion
Table 2 Comparison of the vHIT gains according to otoscopic findings (matte and retracted) among Group 1. Mann Whitney U test, Independent Samples t-test p < 0.05 Canals
t/Z
p
R ASC R LSC R PSC L ASC L LSC L PSC
1.889* −0.727 0.267* −1.042* −0.415* −0.467
0.069** 0.467 0.792** 0.306** 0.681** 0.641
The effect of OME on the vestibular system has been investigated in many studies [6–8,10,18]. Both vestibuloocular reflex (VOR) and vestibulospinal reflex are affected by this pathology. The tests for evaluation of vestibular function during otitis media included electronystagmography (ENG), caloric tests, Vestibular Evoked Myogenic Potentials (VEMP), dynamic and static posturography, sway magnetometry, craniocorpography, and the subjective vertical visual [8]. Most of the studies analyze the effect of OME on vestibulospinal reflex, as most of these tests are relatively easy to do in children and do not stimulate the ear canal [6,18,19]. The ENG analysis is one of the most preferred and reliable test that assesses VOR for the presence of vestibular organ disturbances in the children with OME [7,20]. In ENG test, 25–60% of the patients with OME have peripheral vestibular abnormalities [9,19]. However, there are problems with the reliability of other tests evaluating VOR in this patient group. Caloric test and VEMP are negatively influenced by the presence of middle-ear effusion [8]. VEMP test with air conducted stimuli does not reveal detectable responses in most of the patients with OME, as the impairment of the sound transmission due to middle ear pathology affects air conducted VEMP results [19]. VEMP results with bone conducted stimuli vary greatly among studies [8]. The vHIT test is an objective measure for VOR that allows us to keep our visual field in focus during head movement by maintaining an opposite and equal eye movement. It examines the eye movements at high frequencies of stimulation and provides accurate canal and side specific information without stimulating vertigo. Many studies demonstrate its effectiveness in detecting SSC dysfunction in adults [15,21]. Recent studies support that the vHIT test is a sensitive and efficient vestibular test in the pediatric population as well [16,22]. It is well tolerated by children aged 3–16 years [16] and introduced as a child friendly, relatively easy-to-use, and simple tool to evaluate each of the 6 SSCs [14]. The efficacy of VOR in vHIT test is defined by either the gain of the eye movement to the corresponding head movement, called vHIT gain or by the presence of corrective catch up saccades [23]. In case of VOR impairment, the eye movement cannot be proportional to the head movement, vHIT gain decreases and a corrective eye movement appears
vHIT, video head impulse test; R, right; L, left; ASC, anterior semicircular canal; LSC, lateral semicircular canal; PSC, posterior semicircular canal; *, t value; **, Independent Samples t-test. Table 3 Comparison of the vHIT gains according to tympanogram types (type B and type C2) among Group 1. Mann Whitney U test, Independent Samples t-test p < 0.05 Canals
t/Z
p
R ASC R LSC R PSC L ASC L LSC L PSC
0.622* 2.017* −1.618 −0.610* −0.484 −0.364*
0.539** 0.053** 0.106 0.547** 0.628 0.719**
vHIT, video head impulse test; R, right; L, left; ASC, anterior semicircular canal; LSC, lateral semicircular canal; PSC, posterior semicircular canal; *, t value; **, Independent Samples t-test.
In Group 1, 24 covert saccades were determined in 17 patients (1–4 saccades per patient) in every canal except left lateral SSC plane. None of the patients had covert saccades in Group 2. None of the patients in both groups had overt saccade. vHIT gains of right anterior SSC, lateral SSC and left posterior SSC were significantly lower when saccades were present. The distribution of saccades among canals and comparison of vHIT gains among patients with and without saccades in Group 1 are presented in Table 4. 3
International Journal of Pediatric Otorhinolaryngology 129 (2020) 109783
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in the pediatric population because of its stimulation effect of the vestibular system. Based on our results, it can be assumed that the children with OME and dizziness usually don't have a great vestibular impairment that can be detected with the vHIT test. The VOR gains of these patients are compatible with healthy children and none of them have overt saccades. The covert saccades detected in this patient group are accepted as a sign of slight vestibular impairment as none of the healthy children had saccades. Although the patients have OME bilaterally, this vestibular impairment does not involve both labyrinths equally or affects the entire labyrinth. It should be also kept in mind that the vHIT test evaluates high-frequency head movements and any dizziness due to vestibular function may be a function of impact on lower frequencies of movement that cannot be detected in the vHIT test.
to re-fixate the eye back to the target. vHIT gain is nearly 1 in healthy individuals. vHIT gains of the pediatric population tend to be between 0.7 and 1 and gains below 0.7 and presence of corrective saccades are considered to be pathologic [16,17]. The main differences of vHIT test in children consist of slower peak head velocity and the need for more trials to obtain valid impulses [22]. Additionally, children have difficulty maintaining gaze along the plane of the vertical canals [22]. In most reports, the diagnostic value of vHIT was evaluated based on the caloric test [24]. It has been documented that the VOR gain of the affected ear and GA have a significant linear relationship with unilateral weakness in the caloric test [24]. vHIT is also complementary to caloric testing especially with normal findings in caloric testing [14]. The sensitivity and specificity of vHIT in patients with unilateral vestibular loss were reported as 78% and 85% respectively [24]. However, the studies point out that the vHIT is not as sensitive as the bithermal caloric test in detecting loss of vestibular dysfunction, especially in the pediatric population [22]. To the best of our knowledge, we present the first report providing detailed information about the results of vHIT test in children with OME and dizziness. Besides, the control group in our study demonstrated the results of the vHIT test in the healthy pediatric population. The literature recently focusses on the normative findings of vHIT test in the pediatric population [16,17,25]. Previous reports reveal that VOR gains among different age groups are comparable and when compared with adults, left anterior and right posterior SSC gains are lower in children. It is also mentioned that a large amount of variability exists in the data during vertical canal testing for both healthy children and adults [26]. The vHIT gains of our healthy subjects are comparable with the literature and our study supports that vHIT gains can be variable in a great range for both vertical and horizontal SSCs in the pediatric population. Our study reveals that the vHIT gains of all SSCs do not significantly decrease in children with OME and dizziness when compared with healthy subjects. GA values of children with OME and dizziness are also compatible with healthy children for both vertical and horizontal canals. However, vestibular weakness is expected to cause a decrease in VOR gains and an increase in GA values [24]. When considering the otoscopic examination, no significant difference is found between vHIT gains of children with the matte and retracted eardrum. vHIT gains of patients with type B and type C2 tympanogram are also comparable. The main finding in the vHIT test of children with OME and dizziness is the presence of covert saccades. Covert saccades are detected in 57% of the children with OME and dizziness. This result is difficult to interpret as a sign of vestibular impairment as previous studies indicate that both overt and covert saccades can be observed in about half of the healthy subjects with no significant difference among age, suggesting that VOR is a hypometric system [26]. Additionally, it has been shown that overt saccades are the main saccades that are seen in greater vestibular impairment [24]. None of the children in our study has overt saccade. However, the absence of cover saccade in any of the healthy children lead to the evaluation of covert saccades observed in the patient group in favor of vestibular involvement. It is also open to debate why saccades are more common in the right anterior and left posterior canal directions. Pathologies assumed as the causes of vestibular impairment during OME are expected to affect the entire labyrinth. However, previous studies demonstrated that cochlear impairment also did not involve all the frequencies, sensorineural hearing loss developed only at one frequency in most of the patients with OME, especially at 2 kHz [27]. On the other hand, it is difficult to acquire head impulse in the plane of vertical canals in the pediatric population and the main reason for this result may be the higher variability of vHIT parameters in vertical canals when compared with the horizontal canal. The major drawback of our study is that an additional vestibular test could be used to support the results of vHIT. ENG with the caloric test could be complementary to vHIT test in this patient group. We don't prefer combining vHIT with the caloric test as we don't use caloric test
6. Conclusions Our study is a preliminary study analyzing the vestibular impairment in children with OME and dizziness using the vHIT test. vHIT can be the preferred test for the vestibular evaluation of the pediatric population with OME as it isn't affected by the middle ear effusion and doesn't stimulate vertigo. However, the vHIT test is a limited test to identify all forms of vestibular loss and parameters in the normal range may not be indicative of the absence of vestibular dysfunction. Funding This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. Declaration of competing interest None. Acknowledgments None. References [1] S.S. O'Connor, R. Coggins, L. Gagnon, R.M. Rosenfeld, J.J. Shin, S.A. Walsh, Plain language summary: otitis media with effusion, Otolaryngol. Head Neck Surg. 154 (2) (2016) 215–225, https://doi.org/10.1177/0194599815624409. [2] S.E. Stangerup, M. Tos, The etiologic role of acute suppurative otitis media in chronic secretory otitis, Am. J. Otol. 6 (2) (1985) 126–131. [3] F.M. Gioacchini, M. Alicandri-Ciufelli, S. Kaleci, G. Magliulo, M. Re, Prevalence and diagnosis of vestibular disorders in children: a review, Int. J. Pediatr. Otorhinolaryngol. 78 (5) (2014) 718–724, https://doi.org/10.1016/j.ijporl.2014. 02.009. [4] A.W. Blayney, B.H. Colman, Dizziness in childhood, Clin. Otolaryngol. Allied Sci. 9 (2) (1984) 77–85. [5] M.L. Casselbrant, J.M. Furman, E. Rubenstein, E.M. Mandel, Effect of otitis media on the vestibular system in children, Ann. Otol. Rhinol. Laryngol. 104 (8) (1995) 620–624, https://doi.org/10.1177/000348949510400806. [6] A. Golz, B. Angel-Yeger, S. Parush, Evaluation of balance disturbances in children with middle ear effusion, Int. J. Pediatr. Otorhinolaryngol. 43 (1) (1998) 21–26, https://doi.org/10.1016/s0165-5876(97)00150-x. [7] K. Pazdro-Zastawny, L. Pośpiech, T. Zatoński, Long-term evaluation of the effect of middle ear effusion on the vestibular system in children, Int. J. Pediatr. Otorhinolaryngol. 109 (2018) 13–16, https://doi.org/10.1016/j.ijporl.2018.03. 015. [8] R.D.C. Monsanto, A.L.P. Kasemodel, A. Tomaz, M.M. Paparella, N.O. Penido, Current evidence of peripheral vestibular symptoms secondary to otitis media, Ann. Med. 50 (5) (2018) 391–401, https://doi.org/10.1080/07853890.2018.1470665. [9] M. Koyuncu, M.M. Saka, Y. Tanyeri, T. Seşen, R. Unal, A. Tekat, F. Yilmaz, Effects of otitis media with effusion on the vestibular system in children, Otolaryngol. Head Neck Surg. 120 (1) (1999) 117–121, https://doi.org/10.1016/S0194-5998(99) 70381-5. [10] E.A. Kolkaila, A.A. Emara, T.A. Gabr, Vestibular evaluation in children with otitis media with effusion, J. Laryngol. Otol. 129 (4) (2015) 326–336, https://doi.org/10. 1017/S0022215115000535. [11] N.S. Jones, P. Radomskij, A.J. Prichard, S.E. Snashall, Imbalance and chronic secretory otitis media in children: effect of myringotomy and insertion of ventilation
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