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Wideband tympanometry findings in inner ear malformations
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Wideband tympanometry findings in inner ear malformations Şule Kaya a,*, Betül Çiçek Çınar b, Merve Özbal Batuk b, Burçe Özgen c, Gonca Sennaro glu b, Gülsüm Aydan Genç b, Levent Sennaro glu d a
Ankara Yildirim Beyazit University, Faculty of Health Sciences, Audiology Department, Ankara, Turkey Hacettepe University, Faculty of Health Sciences, Audiology Department, Ankara, Turkey c Hacettepe University, Medical Faculty, Radiology Department, Ankara, Turkey d Hacettepe University, Medical Faculty, ENT Department, Ankara, Turkey b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 23 July 2019 Accepted 1 September 2019 Available online xxx
Objective: The deficits in the cochlea which is at the one end of the ear sound transfer system, may effect middle ear functions. Wideband typanometry (WBT) is frequently used to evaluate these transfer functions which play a crucial role in setting the impedance matching between the external ear and the cochlea. To this end, the aim of this study was to investigate the ear transfer functions in inner ear malformations via WBT, and to question whether these functions change depending on the types of inner ear malformation. Methods: This prospective case-control study was conducted in a university hospital. One hundered-fifty-seven ears (aged 3–37 years) under the groups of cochlear hypoplasia, incomplete partition I, incomplete partition II, cochlear aplasia and complete labyrinthine aplasia were evaluated. In the control group, 30 ears with normal hearing were enrolled and WBT was carried out. Tympanometric peak pressure, equivalent middle ear volume, static admittance, tympanogram width, resonance frequency, average wideband tympanometry and absorbance measurements were analyzed. Results: The inner ear malformation groups demonstrated statistically significant differences than the control group and from each other in terms of traditional tympanometric parameters and WBT test parameters (p < 0.05). The most remarkable difference was between the group of complete labyrinthine aplasia and the control group, most probably because of complete labyrinthine aplasia’s structural effects. However, on some parameters, incomplete partition II and the control group showed similarities. In absorbance measurements, there was significant difference between all patient groups and the control group, especially at high frequencies (p < 0.05). The largest difference was between the control group and the group of complete labyrinthine aplasia which has revealed the lowest absorbance values (p < 0.05). In averaged-wideband tympanogram analysis, all patient groups obtained a lower amplitude peak than the control group; complete labyrinthine aplasia group had the flattest peaked amplitude, while the incomplete partition II group had a near-normal curve. Conclusion: The results of the study revealed the distinctive effects of inner ear malformations in middle ear transfer functions. It is concluded that the absence of inner ear structures causes negative effects on energy absorbance and the other transfer functions of the middle ear. WBT may provide additional information on diagnosis of patients with inner ear malformations. © 2019 Elsevier B.V. All rights reserved.
Keywords: Inner ear malformations Wideband tympanometry Absorbance
1. Introduction * Corresponding author. E-mail addresses: [email protected] (Ş. Kaya).
Congenital inner ear malformations occur during embryological development [1] and they range in severity from mild
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dysplasia to complete inner ear aplasia [2–6]. Because there is a broad spectrum of anomalous patterns of inner ear, numerous classifications for inner ear malformations have been proposed [2,7–10]. In the past few decades the classification and diagnosis of ear malformations has been transformed [3,4,7,11]. Different audiological findings are observed in individuals with inner ear malformations, depending on the type and severity [7]. Inner ear malformations causing hearing loss are often detected in infancy; however, some malformations such as enlarged vestibular aquaduct (EVA), may not be diagnosed until later in life [12]. While approaching to patients with inner ear malformations, it is significant to consider their hearing characteristics. A number of disparate disorders affecting the labyrinth can produce condutive hearing loss by acting as a pathologic third window in the inner ear [13]. A study on patients with EVA who had type A tympanogram at 226 Hz shows that, those patients had significantly lower middle ear resonance frequency (RF) than the control subjects [14]. Wideband tympanometry (WBT) is a tympanometric method which uses a wideband click stimulus intead of using a single probe tone or a pure tone sweep to measure the middle ear functions [15]. Beyond the conditional tympanograms and tympanograms at multiple frequencies, WBT presents averaged wideband tympanogram (A-WBT) which is an optimised tympanogram displaying all tympanograms in a single curve. Traditional tympanometric parameters (tympanometric peak pressure TPP, equivelant ear canal volume (Veq), compansated static acoustic admittance (Ytm), tympanogram width (TW)), RF and absorbance (the proportion of energy absorbed by the middle ear) are measured via WBT [15,16]. Thus, WBT can test normal middle ear functions [17,18], evaluate different middle ear pathologies [19–23], measure middle ear development [24–26] and also analyze the middle ear functions by pressure changes in the ear canal [24,27]. To provide early diagnosis and intervention to patients with inner ear malformations, it is necessary to consider audiological bringings of the malformations [28]. Neverthless, there are few numbers of studies investigating sound transmissions characteristics in inner ear malformations. This study has two interrelated hypothesis: The first one is if different cochlear structures protrude different middle ear transfer functions. The second one is if WBT is differential to put forth this differences in inner ear malformations. To this end, different inner ear malformations were have tested via WBT to find out if WBT might have a role in diagnosis process. 2. Materials and methods This study was conducted in a university hospital which is one of the pioneers about inner ear malformations. Present study was designed and performed according to the Declaration of Helsinki. The local ethical committee approved this study (date: 04.06.2014, number: GO 14/303-18). A total of 103 (53 females and 50 males) volunteers who gave their informed consent prior to the commencement of the study, participated in the study. A total of 88 patients (157 ears) (aged 3–37), who had been previously diagnosed with inner ear malformations, and a
control group of 15 healthy subjects (30 ears) (aged 3–39), were have tested with WBT. There were a total of 6 groups consisting of five patient groups and one control group. These groups were: Group 1: Cochlear Hypoplasia (CH), Group 2: Incomplete Partition-I (IP-I), Group 3: Incomplete PartitionII (IP-II), Group 4: Cochlear Aplasia (CA), Group 5: Complete Labyrinthine Aplasia (CLA) and Group 6: Control. Inclusion criteria for the patient groups were as follows: (i) having inner ear malformations, (ii) having normal otoscopic findings and (iii) not having had external/middle ear surgery. The control group included age matched normal hearing volunteers who had a hearing threshold of better than 15 decibels (dB) between 250 Hz and 8000 Hz They had less than a 10 dB air–bone gap between 250 Hz and 4000 Hz. Patients revisiting ear-nose-throat departments were invited to the study and grouped according to clinical examination and imaging results in the archive. Patients who had outer/middle ear surgery were excluded from the study. All participants were have tested with WBT, Interacoustics Titan version 3.1 (IMP440, Denmark). The measurements of WBT were performed at octave frequencies between 226 Hz and 8000 Hz and 100 dB peSPL (adult: 100 dB peSPL 65 dB nHL) in a silent room. Traditional tympanometric parameters (TPP, Veq, Ytm, TW, RF, absorbance values and A-WBT (375–2000 Hz) were calculated and analyzed using a suitable probe tip (CIR 55-IN- SERT) placed external to the ear canal. The data were recorded in an. xls file; Microsoft Excel 2015 (Microsoft; Redmond, Washington, USA) and IBM Statistical Package for the Social Sciences (SPSS) 19.0 statistical software (SPSS Inc.; 10241440, Istanbul, Turkey) SPSS for Windows version 20.0 (IBM SPSS; Chicago, IL, USA) were used for the statistical analysis. By using descriptive statistics, frequencies were presented as the minimum, maximum and mean standard deviation. For the independent samples, the Kruskal– Wallis test and pairwise comparisons of groups were used. Patient groups were compared with not only the control group but also with each other. The significance level of p < 0.05 was used in all statistical analyses. 3. Results One hundred and three (n = 103) individuals enrolled in the study. Demographic data of the subjects in the groups were shown in Table 1. The findings of traditional tympanometric parameters were presented in Table 2. For all conditional tympanometric parameters, there were differences between the groups. The largest differences came out between CLA (5. Group) and the control group (6. Group). For Veq, the difference between CLA and the control group was statistically significant (p < 0.05). Except from CLA, RF for all groups was aroud 1200 Hz, however, CLA’s RF was approximately 2400 Hz. The results of the group’s absorbance measurements at ambient pressure and tympanometric peak pressure were in the range of 226–8000 Hz (107 frequency points in total). Those results were shown in Figs. 1 and 2 , respectively. In both graphs, absorbance values (vertical axis) varying from 0 to
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Table 1 Demographic data of the subjects. Groups
Age (Year)
Sex
MeanSD Minimum Maximum Female Male
1 group n = 23 22.3 % (39 ears)
2 group n = 18 17.5% (33 ears)
3 group n = 28 27.2% (52 ears)
4 group n = 12 11.6% (21 ears)
5 group n = 7 6.8% (12 ears)
6 group n = 15 14.6 % (30 ears)
10.96 4.91 4 22 12 11
8.56 4.24 3 19 14 4
18.25 9.11 3 37 12 16
7.33 3.57 3 13 4 8
7.00 4.32 3 14 3 4
16.06 10.73 3 39 8 7
*n = number, SD = standart deviation.
Table 2 Traditional tympanometric parameters.
TPP Veq Ytm TW RF
1 group
2 group
3 group
4 group
5 group
6 group
35.48 106.09 0.81 0.28 0.47 0.27 110 54.36 1286 725.06
34.78 100.86 0.77 0.32 0.50 0.39 122.61 64.36 1290.74 689.03
28.86 58.98 1.04 0.38 0.73 0.64 110 63 1147.58 770.27
50.71 87.47 0.75 0.22 0.42 0.24 133.20 83.49 1221.57 590.47
70.25 135.32 0.54 0.15 0.25 0.13 114.50 85.55 2380.50 2189.90
7.00 15.08 0.93 0.29 0.59 0.39 93.56 27.68 1257.96 506.11
TPP: Tympanometric Peak Pressure, daPa), Veq: Equivelant Ear Canal Volume (ml), Ytm: Compansated Static Acoustic Admittance,(ml), TW: Tympanogram Width, (daPa), RF: Resonance Frequency of Ear Canal (Hz).
1 were shown as a function of the frequency (horizontal axis) which took a value between 226 Hz and 8000 Hz. Both in the Figs. 1 and 2, there were a total of 6 curves representing the control group and 5 patient groups. Results showed that the absorbance curve representing the control patients had the highest values than all other malformation groups. For both measurements, the largest difference came out
between the control group and CLA (group 5). The absorbance difference from 226 Hz to 1000 Hz was significant (p < 0.05) between CLA and all other groups. Furthermore, a significant absorbance difference from 4237 Hz to 6535 Hz was also observed between the control group and all other patient groups (p < 0.05). On the other hand, this difference was not significant for the malformation groups (p > 0.05).
Fig. 1. Comparison of absorbance measurements at ambient pressure.
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Fig. 2. Comparison of absorbance measurements at tympanometric peak pressure.
Followingly, for the control group, the difference between absorbance at ambient pressure and absorbance at tympanometric peak pressure was not statistically significant (p > 0.05). However, they were significant for the patient groups (p < 0.05) by showing lower absorbance values at ambient pressure. In a more detailed sense, the findings of CH, IP-I, IPII, and CA groups differed from each other approximately between the 300 Hz to 2000 Hz range, on the other hand, contrary to other malformation groups, in CLA group the difference was between 1681 Hz and 4361 Hz (p < 0.05).
In Fig. 3, groups’ compared A-WBT results (between 375–2000 Hz frequency) is presented. Amplitude values (vertical axis) varying as a function of pressure (horizontal axis) take a value between 200 daPa and 300 daPa. The peak pressure amplitudes were compared, it was seen that all patient groups had lower amplitude than the control group. Regarding this variable; the findings of CH (group 1), IP-I (group 2), and CA (group 4) groups were quite similar. Whereas, by having the flattest curve, findings of
Fig. 3. Compared A-WBT results in control and patient groups.
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CLA (group 5) were different from all other groups. Moreover, a significant difference at certain pressure ranges in A-WBT between groups was observed. 4. Discussion The tympanic membrane, which is mechanically connected to the oval window by middle ear ossicles, is the interface between the outer ear and the middle/inner ear. When acoustically stimulated, this whole system (ear canal, middle ear, round window) vibrates together [29]. The assessment of the middle ear, which has a crucial task in sound transmission, is important in determining the pathology and malfunctioning of the whole auditory system. The role of immitance measurements in the diagnosis of inner ear dysfunctions has also begun to be discussed with the increased experience in this area [13,14]. The broadband nature of the stimulus used and the measurement without pressure make these systems superior to the immittance audiometry using a single probe tone. When the studies in the field of WBT is scanned, it is seen that those studies mainly concentrated on WBT measurements in different middle ear pathologies and they revealed differencial findings [22,23,30,31]. Although, those studies focused on WBT in different middle ear pathologies, present study examined individuals with inner ear malformations, because as the studies on electroacoustic measurements of inner ear malformations [13,14] have accelerated, debates on immitance measurements paved the ways to discuss the importance of those measurements. Inner ear malformations represent 20% of the etiology of congenital hearing loss [8,32]. There are different forms of inner ear malformations that vary in incidence depending on sexuality. Despite studies which reported that ear anomalies were more common in males than females [33], Shama has reported that inner ear anomalies are seen more often in women than in men [10]. In this study, the ratio of female and male patients were 51.1% and 48.9% respectively. TPP shows middle ear pressure indirectly. In this study, TPP values of the control group were similar to the results of the normative studies [34–36]. Unlike the control group, it was suggested that the formation of TPP at negative pressure in all anomalous groups might be caused due to malformation of the inner ear structures. Moreover, the peak pressure amplitudes of all patient groups were lower than the control group. Regarding this variable; the findings of CH (group 1), IP-I (group 2), and CA (group 4) groups were very similar, whereas those of CLA (group 5) differed from all other groups by having the flattest curve. As it is known, Stapes footplate opens into vestibule. In this regard, except for CLA, in patient groups absorbance amplitudes were similar to control group because their vestibules are normally developed and this is an important dimension separating CLA from the rest of the malformations group. Veq is a parameter that gives information about the volume of outer ear canal and the integrity of the tympanic membraine. While there are some studies which claim that age is not influential on Veq [37], there are some others which state that
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Veq increases with age, and this increase is greater in men than in women [38]. Although, labyrinthine aplasia and cochlear aphasia groups were matched in terms of age and gender, Veq was found to be significantly lower in labyrinthine aplasia patients. This result indicates that the absence of inner ear structures in labyrinthine aplasia affects ear canal volume. RF is the frequency at which mass and stiffness components are balanced. When middle ear is under the mass effect, RF shifts to low frequencies and when middle ear is under the stiffness effect, RF is shifted to high frequencies [39]. RF is also influenced by the mechanical impedance of the cochlea. Studies report that enlargement of endolymphatic suc in EVA leads a decrease in cochlear impedance, which results in lowers RF value [14]. Merchant states that despite the normal tympanic membrane and normal ventilated middle ear findings, the inner ear anomalies (including LVA and IP-III) may cause conduction pathology [13]. In this study, CLA group’s RF was nearly twofold of the control and other parient groups’ RF. This data suggests that CLA is more outstanding in terms of RF parameters among inner ear anomalies. In addition, the absence of inner ear structures in CLA may lead to a higher RF by increasing the impedance at the base of the stapes. RF, which reflects changes in middle ear transfer characteristics, can not be effectively used because there is no normative data. Further studies concering normative data will be useful in clinical practice. The absorbance configuration as a function of frequency in adults has been defined previously [18,34,40]. In many normative studies, it is shown that in all age groups, the absorbance is low at the frequencies below 1000 Hz and above 4000 Hz frequencies, and reaches the highest value somewhere between 1000 Hz and 4000 Hz [18,20,24]. The studies on maturation effects in the measurement of WBT in infants and children shows that the most significant maturational effects are seen in very early childhood as 0–6 months of age or 0–1 year of life [24,26]. Hunter et al. stated that the outer ear canal and middle ear have not completed their development at birth yet and continue to develop especially during the first 6 months and emphasized that age-specific norms should be used for infants aged 0–1 year in the measurement of WBT [31]. Moreover, Beers et al. in 2010 [41] found that WBT results of children were similar to that of adult’s. In the present study, the age range of the individuals was 3–40 years, which enabled measurements to be analyzed without influence of maturation, which was more pronounced especially in the first years of life. In addition configuration of the absorbance values of the control group are consistent with the findings of the literature [18,20,24]. Studies have shown that absorbance measurements at tympanometric peak pressure are more sensitive to middle ear pathologies than in absorbance measurements at ambient pressure [18,27,32]. In other words, WBT provides more information than measurements at ambient pressure when measured as a combined function of frequency and air pressure [17,18,24]. In the present study, for the control group, the difference between absorbance at ambient pressure and absorbance at tympanometric peak pressure was not significantly different (p > 0.05). This suggests that positive or
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negative pressure in the healthy middle ear does not affect the absorbance. However, absorbance values measured at ambient pressure were lower for all patient groups. In addition, the CLA group has lower absorbance measured at ambient pressure throughout a greater frequency range compared to other malformation groups. This finding suggests that testing absorbance at tympanometric peak pressure provides differential data for CLA which is the most severe inner ear malformation. Contrary to the findings of the present study, Liu et al. argue that throughout low frequencies, observing lower absorbance at the ambient pressures compared to the absorbance at tympanic peak pressure is a result of the air compression arise during the insertion of the probe in the outer ear canal [17]. However, his claim is questionable because in our study while the difference between absorbance at the ambient pressures and the absorbance at tympanic peak pressure for CLA group came out from a different the frequency range, for the other four anomalous groups they came out from the same frequency range. This suggests that, unlike Liu et al., these two measurements may provide different information [17]. In other words, it is thought that measurements on tympanometric peak pressure and ambient pressure may provide distinctive information depending on the nature of the pathology. A-WBT is a two-dimensional graph obtained by averaging the absorbance values of a range of 375–2000 Hz in a threedimensional tympanogram. In the study, peak amplitude values in A-WBT for patient groups were at a lower level than the control group (p < 0.05). In terms of this parameter, CH, IP-I, and CA groups showed similarities, whereas the CLA group was found to be flattened (p < 0.05). The decrease in the absorbance indicates that the effect of the stiffness of the middle ear is increased in the group of CLA. A significant difference in the absorbance values of A-WBT between groups at certain pressure ranges showed that the ear experienced different effects due to differences in inner ear structures. As a result, it has been found that WBT parameters may differ depending on the types of inner ear malformations. It is considered that the planning of studies, in which gender and age are taken as variables in different malformation groups, will provide valuable contributions. In addition to otologic and radiological evaluation, objective audiologic data may provide important differential information in inner ear malformations. The findings of the present study indicate that WBT can be used together with audiological examination for the diagnosis of certain hearing loss. In case of profound SNHL, the presence of low absorbance values, flattened A-WBT and high RF, may indicate the presence of CLA. It is very interesting that from a hearing perspective, CLA and CA have similar audiological configurations but they have different immitancemetric configurations as demonstrated by the findings in WBT. This is because the presence vestibule where the footplate is attached makes it possible to obtain similar values in CA with other anomalies, whereas in CLA the absence of any inner ear structure gives it very characteristic findings (the lowest value obtained in wideband absorbance). In conclusion, profound SNHL with low absorbance values, flattened A-WBT and high RF findings in WBT may suggest CLA and hence an earlier
than normal radiological intervention may be indicated to avoid time loss with hearing aids. 5. Conclusion Showing the different configurations for different types of inner ear malformations, WBT may have a distinctive role in the diagnosis of inner ear malformations. Determination of WBT parameters for other inner ear malformations that cannot be assessed in the study will also provide useful information and it is thought to be useful in clinical practice to use WBT as a part of the audiological test battery. Financial disclosures/conflicts of interest The authors declare that there is no conflict of interest. No financial support were taken for this study. Acknowledgement This study was presented as PhD thesis of Sule Kaya (2016Ankara) Supported by: Hacettepe University, Scientific Research Projects Coordination Unit, Support Project, Project Number: 014 D08 401. References [1] Paccola EC, Fernandes JC, Mondelli MF. Amplification by bone conduction in congenital malformations: patient benefits and satisfaction. Braz J Otorhinolaryngol 2013;79(3):359–65. [2] Friedrich SB, Wulke C. Classification and diagnosis of ear malformations. GMS Curr Top Otorhinolaryngol Head Neck Surg 2007;6:1–21. [3] Joshi VM, Navlekar SK, Kishore GR, Reddy KJ, Vinay Kumar EC. CT and MR imaging of the inner ear and brain in children with congenital sensorineural hearing loss. Radiographics 2012;32(3):683–98. [4] Zheng Y, Schachern PA, Cureoglu S, Mutlu C, Dijalilian H, Paparella MM. The shortened cochlea: its classification and histopathologic features. Int J Pediatr Otorhinolaryngol 2002;63(1):29–39. [5] Ozgen B, Oguz KK, Atas A, Sennaroglu L. Complete labyrinthine aplasia: clinical and radiologic findings with review of the literature. Am J Neuroradiol 2009;30(4):774–80. [6] Yang NW. Cystic cochleovestibular malformation (incomplete partition type 1). Philipp J Otolaryngol Head Neck Surg 2010;25(1):41–2. [7] Sennaroglu L, Ozkan HB, Aslan F. Impact of cochleovestibular malformations in treating children with hearing loss. Audiol Neurootol 2013;18:3–31. [8] Jackler RK, Luxford WM, House WF. Congenital malformations of the inner ear: a classification based on embryogesis. Laryngoscope 1987;97:2–14. [9] Sennaroglu L, Saatci I. A new classification for cochleovestibular malformations. Laryngoscope 2002;112(12):2230–41. [10] Shama AM. Revisit to congenital anomalies of the inner ear: the spectrum of aplastic/dysplastic labyrinthine malformations (ADLM). A new concept for classification. Egypt J Radiol Nucl Med 2012;43 (4):535–42. [11] Sennaroglu L. Histopathology of inner ear malformations: do we have enough evidence to explain pathophysiology? Cochlear Implants Int 2016;17(1):3–20. [12] Huang BY, Zdanski C, Castillo M. Pediatric sensorineural hearing loss, part 1: practical aspects for neuroradiologists. Am J Neuroradiol 2012;33(2):211–7. [13] Merchant SN, Rosowski JJ. Conductive hearing loss caused by thirdwindow lesions of the ınner ear. Otol Neurotol 2008;29(3):282–9.
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Wideband tympanometry findings in inner ear malformations Şule Kaya a,*, Betül Çiçek Çınar b, Merve Özbal Batuk b, Burçe Özgen c, Gonca Sennaro glu b, Gülsüm Aydan Genç b, Levent Sennaro glu d a
Ankara Yildirim Beyazit University, Faculty of Health Sciences, Audiology Department, Ankara, Turkey Hacettepe University, Faculty of Health Sciences, Audiology Department, Ankara, Turkey c Hacettepe University, Medical Faculty, Radiology Department, Ankara, Turkey d Hacettepe University, Medical Faculty, ENT Department, Ankara, Turkey b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 23 July 2019 Accepted 1 September 2019 Available online xxx
Objective: The deficits in the cochlea which is at the one end of the ear sound transfer system, may effect middle ear functions. Wideband typanometry (WBT) is frequently used to evaluate these transfer functions which play a crucial role in setting the impedance matching between the external ear and the cochlea. To this end, the aim of this study was to investigate the ear transfer functions in inner ear malformations via WBT, and to question whether these functions change depending on the types of inner ear malformation. Methods: This prospective case-control study was conducted in a university hospital. One hundered-fifty-seven ears (aged 3–37 years) under the groups of cochlear hypoplasia, incomplete partition I, incomplete partition II, cochlear aplasia and complete labyrinthine aplasia were evaluated. In the control group, 30 ears with normal hearing were enrolled and WBT was carried out. Tympanometric peak pressure, equivalent middle ear volume, static admittance, tympanogram width, resonance frequency, average wideband tympanometry and absorbance measurements were analyzed. Results: The inner ear malformation groups demonstrated statistically significant differences than the control group and from each other in terms of traditional tympanometric parameters and WBT test parameters (p < 0.05). The most remarkable difference was between the group of complete labyrinthine aplasia and the control group, most probably because of complete labyrinthine aplasia’s structural effects. However, on some parameters, incomplete partition II and the control group showed similarities. In absorbance measurements, there was significant difference between all patient groups and the control group, especially at high frequencies (p < 0.05). The largest difference was between the control group and the group of complete labyrinthine aplasia which has revealed the lowest absorbance values (p < 0.05). In averaged-wideband tympanogram analysis, all patient groups obtained a lower amplitude peak than the control group; complete labyrinthine aplasia group had the flattest peaked amplitude, while the incomplete partition II group had a near-normal curve. Conclusion: The results of the study revealed the distinctive effects of inner ear malformations in middle ear transfer functions. It is concluded that the absence of inner ear structures causes negative effects on energy absorbance and the other transfer functions of the middle ear. WBT may provide additional information on diagnosis of patients with inner ear malformations. © 2019 Elsevier B.V. All rights reserved.
Keywords: Inner ear malformations Wideband tympanometry Absorbance
1. Introduction * Corresponding author. E-mail addresses: [email protected] (Ş. Kaya).
Congenital inner ear malformations occur during embryological development [1] and they range in severity from mild
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dysplasia to complete inner ear aplasia [2–6]. Because there is a broad spectrum of anomalous patterns of inner ear, numerous classifications for inner ear malformations have been proposed [2,7–10]. In the past few decades the classification and diagnosis of ear malformations has been transformed [3,4,7,11]. Different audiological findings are observed in individuals with inner ear malformations, depending on the type and severity [7]. Inner ear malformations causing hearing loss are often detected in infancy; however, some malformations such as enlarged vestibular aquaduct (EVA), may not be diagnosed until later in life [12]. While approaching to patients with inner ear malformations, it is significant to consider their hearing characteristics. A number of disparate disorders affecting the labyrinth can produce condutive hearing loss by acting as a pathologic third window in the inner ear [13]. A study on patients with EVA who had type A tympanogram at 226 Hz shows that, those patients had significantly lower middle ear resonance frequency (RF) than the control subjects [14]. Wideband tympanometry (WBT) is a tympanometric method which uses a wideband click stimulus intead of using a single probe tone or a pure tone sweep to measure the middle ear functions [15]. Beyond the conditional tympanograms and tympanograms at multiple frequencies, WBT presents averaged wideband tympanogram (A-WBT) which is an optimised tympanogram displaying all tympanograms in a single curve. Traditional tympanometric parameters (tympanometric peak pressure TPP, equivelant ear canal volume (Veq), compansated static acoustic admittance (Ytm), tympanogram width (TW)), RF and absorbance (the proportion of energy absorbed by the middle ear) are measured via WBT [15,16]. Thus, WBT can test normal middle ear functions [17,18], evaluate different middle ear pathologies [19–23], measure middle ear development [24–26] and also analyze the middle ear functions by pressure changes in the ear canal [24,27]. To provide early diagnosis and intervention to patients with inner ear malformations, it is necessary to consider audiological bringings of the malformations [28]. Neverthless, there are few numbers of studies investigating sound transmissions characteristics in inner ear malformations. This study has two interrelated hypothesis: The first one is if different cochlear structures protrude different middle ear transfer functions. The second one is if WBT is differential to put forth this differences in inner ear malformations. To this end, different inner ear malformations were have tested via WBT to find out if WBT might have a role in diagnosis process. 2. Materials and methods This study was conducted in a university hospital which is one of the pioneers about inner ear malformations. Present study was designed and performed according to the Declaration of Helsinki. The local ethical committee approved this study (date: 04.06.2014, number: GO 14/303-18). A total of 103 (53 females and 50 males) volunteers who gave their informed consent prior to the commencement of the study, participated in the study. A total of 88 patients (157 ears) (aged 3–37), who had been previously diagnosed with inner ear malformations, and a
control group of 15 healthy subjects (30 ears) (aged 3–39), were have tested with WBT. There were a total of 6 groups consisting of five patient groups and one control group. These groups were: Group 1: Cochlear Hypoplasia (CH), Group 2: Incomplete Partition-I (IP-I), Group 3: Incomplete PartitionII (IP-II), Group 4: Cochlear Aplasia (CA), Group 5: Complete Labyrinthine Aplasia (CLA) and Group 6: Control. Inclusion criteria for the patient groups were as follows: (i) having inner ear malformations, (ii) having normal otoscopic findings and (iii) not having had external/middle ear surgery. The control group included age matched normal hearing volunteers who had a hearing threshold of better than 15 decibels (dB) between 250 Hz and 8000 Hz They had less than a 10 dB air–bone gap between 250 Hz and 4000 Hz. Patients revisiting ear-nose-throat departments were invited to the study and grouped according to clinical examination and imaging results in the archive. Patients who had outer/middle ear surgery were excluded from the study. All participants were have tested with WBT, Interacoustics Titan version 3.1 (IMP440, Denmark). The measurements of WBT were performed at octave frequencies between 226 Hz and 8000 Hz and 100 dB peSPL (adult: 100 dB peSPL 65 dB nHL) in a silent room. Traditional tympanometric parameters (TPP, Veq, Ytm, TW, RF, absorbance values and A-WBT (375–2000 Hz) were calculated and analyzed using a suitable probe tip (CIR 55-IN- SERT) placed external to the ear canal. The data were recorded in an. xls file; Microsoft Excel 2015 (Microsoft; Redmond, Washington, USA) and IBM Statistical Package for the Social Sciences (SPSS) 19.0 statistical software (SPSS Inc.; 10241440, Istanbul, Turkey) SPSS for Windows version 20.0 (IBM SPSS; Chicago, IL, USA) were used for the statistical analysis. By using descriptive statistics, frequencies were presented as the minimum, maximum and mean standard deviation. For the independent samples, the Kruskal– Wallis test and pairwise comparisons of groups were used. Patient groups were compared with not only the control group but also with each other. The significance level of p < 0.05 was used in all statistical analyses. 3. Results One hundred and three (n = 103) individuals enrolled in the study. Demographic data of the subjects in the groups were shown in Table 1. The findings of traditional tympanometric parameters were presented in Table 2. For all conditional tympanometric parameters, there were differences between the groups. The largest differences came out between CLA (5. Group) and the control group (6. Group). For Veq, the difference between CLA and the control group was statistically significant (p < 0.05). Except from CLA, RF for all groups was aroud 1200 Hz, however, CLA’s RF was approximately 2400 Hz. The results of the group’s absorbance measurements at ambient pressure and tympanometric peak pressure were in the range of 226–8000 Hz (107 frequency points in total). Those results were shown in Figs. 1 and 2 , respectively. In both graphs, absorbance values (vertical axis) varying from 0 to
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Table 1 Demographic data of the subjects. Groups
Age (Year)
Sex
MeanSD Minimum Maximum Female Male
1 group n = 23 22.3 % (39 ears)
2 group n = 18 17.5% (33 ears)
3 group n = 28 27.2% (52 ears)
4 group n = 12 11.6% (21 ears)
5 group n = 7 6.8% (12 ears)
6 group n = 15 14.6 % (30 ears)
10.96 4.91 4 22 12 11
8.56 4.24 3 19 14 4
18.25 9.11 3 37 12 16
7.33 3.57 3 13 4 8
7.00 4.32 3 14 3 4
16.06 10.73 3 39 8 7
*n = number, SD = standart deviation.
Table 2 Traditional tympanometric parameters.
TPP Veq Ytm TW RF
1 group
2 group
3 group
4 group
5 group
6 group
35.48 106.09 0.81 0.28 0.47 0.27 110 54.36 1286 725.06
34.78 100.86 0.77 0.32 0.50 0.39 122.61 64.36 1290.74 689.03
28.86 58.98 1.04 0.38 0.73 0.64 110 63 1147.58 770.27
50.71 87.47 0.75 0.22 0.42 0.24 133.20 83.49 1221.57 590.47
70.25 135.32 0.54 0.15 0.25 0.13 114.50 85.55 2380.50 2189.90
7.00 15.08 0.93 0.29 0.59 0.39 93.56 27.68 1257.96 506.11
TPP: Tympanometric Peak Pressure, daPa), Veq: Equivelant Ear Canal Volume (ml), Ytm: Compansated Static Acoustic Admittance,(ml), TW: Tympanogram Width, (daPa), RF: Resonance Frequency of Ear Canal (Hz).
1 were shown as a function of the frequency (horizontal axis) which took a value between 226 Hz and 8000 Hz. Both in the Figs. 1 and 2, there were a total of 6 curves representing the control group and 5 patient groups. Results showed that the absorbance curve representing the control patients had the highest values than all other malformation groups. For both measurements, the largest difference came out
between the control group and CLA (group 5). The absorbance difference from 226 Hz to 1000 Hz was significant (p < 0.05) between CLA and all other groups. Furthermore, a significant absorbance difference from 4237 Hz to 6535 Hz was also observed between the control group and all other patient groups (p < 0.05). On the other hand, this difference was not significant for the malformation groups (p > 0.05).
Fig. 1. Comparison of absorbance measurements at ambient pressure.
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Fig. 2. Comparison of absorbance measurements at tympanometric peak pressure.
Followingly, for the control group, the difference between absorbance at ambient pressure and absorbance at tympanometric peak pressure was not statistically significant (p > 0.05). However, they were significant for the patient groups (p < 0.05) by showing lower absorbance values at ambient pressure. In a more detailed sense, the findings of CH, IP-I, IPII, and CA groups differed from each other approximately between the 300 Hz to 2000 Hz range, on the other hand, contrary to other malformation groups, in CLA group the difference was between 1681 Hz and 4361 Hz (p < 0.05).
In Fig. 3, groups’ compared A-WBT results (between 375–2000 Hz frequency) is presented. Amplitude values (vertical axis) varying as a function of pressure (horizontal axis) take a value between 200 daPa and 300 daPa. The peak pressure amplitudes were compared, it was seen that all patient groups had lower amplitude than the control group. Regarding this variable; the findings of CH (group 1), IP-I (group 2), and CA (group 4) groups were quite similar. Whereas, by having the flattest curve, findings of
Fig. 3. Compared A-WBT results in control and patient groups.
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CLA (group 5) were different from all other groups. Moreover, a significant difference at certain pressure ranges in A-WBT between groups was observed. 4. Discussion The tympanic membrane, which is mechanically connected to the oval window by middle ear ossicles, is the interface between the outer ear and the middle/inner ear. When acoustically stimulated, this whole system (ear canal, middle ear, round window) vibrates together [29]. The assessment of the middle ear, which has a crucial task in sound transmission, is important in determining the pathology and malfunctioning of the whole auditory system. The role of immitance measurements in the diagnosis of inner ear dysfunctions has also begun to be discussed with the increased experience in this area [13,14]. The broadband nature of the stimulus used and the measurement without pressure make these systems superior to the immittance audiometry using a single probe tone. When the studies in the field of WBT is scanned, it is seen that those studies mainly concentrated on WBT measurements in different middle ear pathologies and they revealed differencial findings [22,23,30,31]. Although, those studies focused on WBT in different middle ear pathologies, present study examined individuals with inner ear malformations, because as the studies on electroacoustic measurements of inner ear malformations [13,14] have accelerated, debates on immitance measurements paved the ways to discuss the importance of those measurements. Inner ear malformations represent 20% of the etiology of congenital hearing loss [8,32]. There are different forms of inner ear malformations that vary in incidence depending on sexuality. Despite studies which reported that ear anomalies were more common in males than females [33], Shama has reported that inner ear anomalies are seen more often in women than in men [10]. In this study, the ratio of female and male patients were 51.1% and 48.9% respectively. TPP shows middle ear pressure indirectly. In this study, TPP values of the control group were similar to the results of the normative studies [34–36]. Unlike the control group, it was suggested that the formation of TPP at negative pressure in all anomalous groups might be caused due to malformation of the inner ear structures. Moreover, the peak pressure amplitudes of all patient groups were lower than the control group. Regarding this variable; the findings of CH (group 1), IP-I (group 2), and CA (group 4) groups were very similar, whereas those of CLA (group 5) differed from all other groups by having the flattest curve. As it is known, Stapes footplate opens into vestibule. In this regard, except for CLA, in patient groups absorbance amplitudes were similar to control group because their vestibules are normally developed and this is an important dimension separating CLA from the rest of the malformations group. Veq is a parameter that gives information about the volume of outer ear canal and the integrity of the tympanic membraine. While there are some studies which claim that age is not influential on Veq [37], there are some others which state that
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Veq increases with age, and this increase is greater in men than in women [38]. Although, labyrinthine aplasia and cochlear aphasia groups were matched in terms of age and gender, Veq was found to be significantly lower in labyrinthine aplasia patients. This result indicates that the absence of inner ear structures in labyrinthine aplasia affects ear canal volume. RF is the frequency at which mass and stiffness components are balanced. When middle ear is under the mass effect, RF shifts to low frequencies and when middle ear is under the stiffness effect, RF is shifted to high frequencies [39]. RF is also influenced by the mechanical impedance of the cochlea. Studies report that enlargement of endolymphatic suc in EVA leads a decrease in cochlear impedance, which results in lowers RF value [14]. Merchant states that despite the normal tympanic membrane and normal ventilated middle ear findings, the inner ear anomalies (including LVA and IP-III) may cause conduction pathology [13]. In this study, CLA group’s RF was nearly twofold of the control and other parient groups’ RF. This data suggests that CLA is more outstanding in terms of RF parameters among inner ear anomalies. In addition, the absence of inner ear structures in CLA may lead to a higher RF by increasing the impedance at the base of the stapes. RF, which reflects changes in middle ear transfer characteristics, can not be effectively used because there is no normative data. Further studies concering normative data will be useful in clinical practice. The absorbance configuration as a function of frequency in adults has been defined previously [18,34,40]. In many normative studies, it is shown that in all age groups, the absorbance is low at the frequencies below 1000 Hz and above 4000 Hz frequencies, and reaches the highest value somewhere between 1000 Hz and 4000 Hz [18,20,24]. The studies on maturation effects in the measurement of WBT in infants and children shows that the most significant maturational effects are seen in very early childhood as 0–6 months of age or 0–1 year of life [24,26]. Hunter et al. stated that the outer ear canal and middle ear have not completed their development at birth yet and continue to develop especially during the first 6 months and emphasized that age-specific norms should be used for infants aged 0–1 year in the measurement of WBT [31]. Moreover, Beers et al. in 2010 [41] found that WBT results of children were similar to that of adult’s. In the present study, the age range of the individuals was 3–40 years, which enabled measurements to be analyzed without influence of maturation, which was more pronounced especially in the first years of life. In addition configuration of the absorbance values of the control group are consistent with the findings of the literature [18,20,24]. Studies have shown that absorbance measurements at tympanometric peak pressure are more sensitive to middle ear pathologies than in absorbance measurements at ambient pressure [18,27,32]. In other words, WBT provides more information than measurements at ambient pressure when measured as a combined function of frequency and air pressure [17,18,24]. In the present study, for the control group, the difference between absorbance at ambient pressure and absorbance at tympanometric peak pressure was not significantly different (p > 0.05). This suggests that positive or
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negative pressure in the healthy middle ear does not affect the absorbance. However, absorbance values measured at ambient pressure were lower for all patient groups. In addition, the CLA group has lower absorbance measured at ambient pressure throughout a greater frequency range compared to other malformation groups. This finding suggests that testing absorbance at tympanometric peak pressure provides differential data for CLA which is the most severe inner ear malformation. Contrary to the findings of the present study, Liu et al. argue that throughout low frequencies, observing lower absorbance at the ambient pressures compared to the absorbance at tympanic peak pressure is a result of the air compression arise during the insertion of the probe in the outer ear canal [17]. However, his claim is questionable because in our study while the difference between absorbance at the ambient pressures and the absorbance at tympanic peak pressure for CLA group came out from a different the frequency range, for the other four anomalous groups they came out from the same frequency range. This suggests that, unlike Liu et al., these two measurements may provide different information [17]. In other words, it is thought that measurements on tympanometric peak pressure and ambient pressure may provide distinctive information depending on the nature of the pathology. A-WBT is a two-dimensional graph obtained by averaging the absorbance values of a range of 375–2000 Hz in a threedimensional tympanogram. In the study, peak amplitude values in A-WBT for patient groups were at a lower level than the control group (p < 0.05). In terms of this parameter, CH, IP-I, and CA groups showed similarities, whereas the CLA group was found to be flattened (p < 0.05). The decrease in the absorbance indicates that the effect of the stiffness of the middle ear is increased in the group of CLA. A significant difference in the absorbance values of A-WBT between groups at certain pressure ranges showed that the ear experienced different effects due to differences in inner ear structures. As a result, it has been found that WBT parameters may differ depending on the types of inner ear malformations. It is considered that the planning of studies, in which gender and age are taken as variables in different malformation groups, will provide valuable contributions. In addition to otologic and radiological evaluation, objective audiologic data may provide important differential information in inner ear malformations. The findings of the present study indicate that WBT can be used together with audiological examination for the diagnosis of certain hearing loss. In case of profound SNHL, the presence of low absorbance values, flattened A-WBT and high RF, may indicate the presence of CLA. It is very interesting that from a hearing perspective, CLA and CA have similar audiological configurations but they have different immitancemetric configurations as demonstrated by the findings in WBT. This is because the presence vestibule where the footplate is attached makes it possible to obtain similar values in CA with other anomalies, whereas in CLA the absence of any inner ear structure gives it very characteristic findings (the lowest value obtained in wideband absorbance). In conclusion, profound SNHL with low absorbance values, flattened A-WBT and high RF findings in WBT may suggest CLA and hence an earlier
than normal radiological intervention may be indicated to avoid time loss with hearing aids. 5. Conclusion Showing the different configurations for different types of inner ear malformations, WBT may have a distinctive role in the diagnosis of inner ear malformations. Determination of WBT parameters for other inner ear malformations that cannot be assessed in the study will also provide useful information and it is thought to be useful in clinical practice to use WBT as a part of the audiological test battery. Financial disclosures/conflicts of interest The authors declare that there is no conflict of interest. No financial support were taken for this study. Acknowledgement This study was presented as PhD thesis of Sule Kaya (2016Ankara) Supported by: Hacettepe University, Scientific Research Projects Coordination Unit, Support Project, Project Number: 014 D08 401. References [1] Paccola EC, Fernandes JC, Mondelli MF. Amplification by bone conduction in congenital malformations: patient benefits and satisfaction. Braz J Otorhinolaryngol 2013;79(3):359–65. [2] Friedrich SB, Wulke C. Classification and diagnosis of ear malformations. GMS Curr Top Otorhinolaryngol Head Neck Surg 2007;6:1–21. [3] Joshi VM, Navlekar SK, Kishore GR, Reddy KJ, Vinay Kumar EC. CT and MR imaging of the inner ear and brain in children with congenital sensorineural hearing loss. Radiographics 2012;32(3):683–98. [4] Zheng Y, Schachern PA, Cureoglu S, Mutlu C, Dijalilian H, Paparella MM. The shortened cochlea: its classification and histopathologic features. Int J Pediatr Otorhinolaryngol 2002;63(1):29–39. [5] Ozgen B, Oguz KK, Atas A, Sennaroglu L. Complete labyrinthine aplasia: clinical and radiologic findings with review of the literature. Am J Neuroradiol 2009;30(4):774–80. [6] Yang NW. Cystic cochleovestibular malformation (incomplete partition type 1). Philipp J Otolaryngol Head Neck Surg 2010;25(1):41–2. [7] Sennaroglu L, Ozkan HB, Aslan F. Impact of cochleovestibular malformations in treating children with hearing loss. Audiol Neurootol 2013;18:3–31. [8] Jackler RK, Luxford WM, House WF. Congenital malformations of the inner ear: a classification based on embryogesis. Laryngoscope 1987;97:2–14. [9] Sennaroglu L, Saatci I. A new classification for cochleovestibular malformations. Laryngoscope 2002;112(12):2230–41. [10] Shama AM. Revisit to congenital anomalies of the inner ear: the spectrum of aplastic/dysplastic labyrinthine malformations (ADLM). A new concept for classification. Egypt J Radiol Nucl Med 2012;43 (4):535–42. [11] Sennaroglu L. Histopathology of inner ear malformations: do we have enough evidence to explain pathophysiology? Cochlear Implants Int 2016;17(1):3–20. [12] Huang BY, Zdanski C, Castillo M. Pediatric sensorineural hearing loss, part 1: practical aspects for neuroradiologists. Am J Neuroradiol 2012;33(2):211–7. [13] Merchant SN, Rosowski JJ. Conductive hearing loss caused by thirdwindow lesions of the ınner ear. Otol Neurotol 2008;29(3):282–9.
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Please cite this article in press as: Kaya Ş, et al. Wideband tympanometry findings in inner ear malformations. Auris Nasus Larynx (2019), https://doi.org/10.1016/j.anl.2019.09.001