International Journal of Pediatric Otorhinolaryngology 79 (2015) 42–46
Contents lists available at ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Usefulness of 1000-Hz probe tone in tympanometry according to age in Korean infants Mina Park a, Kyu-Hee Han a,b, Hyunseo Jung a, Mee-Hee Kim a, Hyun-Kyung Chang a, Shin Hye Kim a, Moo Kyun Park a,c, Jun Ho Lee a,c,* a
Department of Otorhinolaryngology—Head and Neck Surgery, Seoul National University College of Medicine, Seoul National University Hospital, Seoul, South Korea Department of Otorhinolaryngology, National Medical Center, Seoul, South Korea c Sensory Organ Research Institute, Seoul National University Medical Research Center, Seoul, South Korea b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 7 September 2014 Received in revised form 27 October 2014 Accepted 31 October 2014 Available online 13 November 2014
Objective: Numerous studies have shown the superiority of a 1000-Hz frequency probe tone for evaluating the middle ear status of infants. However, most of these studies examined Caucasian populations. This study validated the 1000-Hz probe tone and evaluated the age at which it should be used in Korean infants. Methods: Data from 83 infants (43 males, 40 females; mean age 9.2 6.2 (range 1–30) months, 165 ears) were analyzed. Tympanograms were classified according to Baldwin’s modification of the method of Marchant et al. and correlated with results based on combined diagnostic tests, including an endoscopic examination of the tympanic membrane, myringotomy findings, and the air and bone conduction auditory brainstem response (ABR) thresholds. Data were analyzed in five age groups, each covering a 3-month range. The traces were measured for both 226- and 1000-Hz probe tones. The sensitivity and specificity for the different age groups were also determined. Results: For the 226-Hz probe tone, the tympanograms showed normal traces for most ears with otitis media effusions in infants younger than 12 months. By contrast, the tympanograms using the 1000-Hz probe tone showed abnormal traces in most of the infants with otitis media effusions in all age groups. In infants with no otitis media effusion, the tympanograms using both 226- and 1000-Hz probe tones were interpreted as normal in most cases in all age groups. In infants younger than 12 months, the sensitivity of the 226-Hz probe tone was very low (0–6.6%), whereas that of the 1000-Hz probe tone was very high (90–100%). In infants older than 13 months, however, the sensitivities of the 226- and 1000-Hz probe tones were 76.2% and 85.7%, respectively. Regarding specificity, the difference between the two probe tones was not significant for any age group. Conclusions: This study confirmed the superiority of the 1000-Hz probe tone for evaluating the middle ear in infants. We recommend using a 1000-Hz probe tone at least up to the age of 12 months for Korean infants. ß 2014 Elsevier Ireland Ltd. All rights reserved.
Keywords: 1000-Hz probe tone Otitis media effusion Asian Korean Infant High-frequency tympanometry
Introduction Otitis media effusion (OME) is one of the most common diseases in infants. It is thought that OME occurs in more than half of all children in the first year of life [1]. Recurrent OME can result
* Corresponding author at: Department of Otorhinolaryngology—Head and Neck Surgery, Seoul National University College of Medicine, Seoul National University Hospital, 101 Daehangno, Jongno-gu, Seoul, South Korea. Tel.: +82 2 2072 2445; fax: +82 2 745 2387. E-mail address: [email protected] (J.H. Lee). http://dx.doi.org/10.1016/j.ijporl.2014.10.041 0165-5876/ß 2014 Elsevier Ireland Ltd. All rights reserved.
in mild to moderate hearing loss because it affects the mobility of the ossicles and tympanic membrane [2]. This hearing loss might affect language development and cognition [2]. In addition, OME frequently causes false-positive results in newborn hearing screening. Consequently, it is important to assess the middle ear status of infants accurately. However, the diagnosis of OME is difficult because children are restless during examination and they have small external auditory canals (EAC) [3]. Tympanometry in pediatric audiology is most commonly used to measure the middle ear pressure, which assists in the identification of OME. The conventional 226-Hz probe tone is a well-established method used in adults and children. Although the test is easy and the traces are
M. Park et al. / International Journal of Pediatric Otorhinolaryngology 79 (2015) 42–46
easy to interpret, its validity for infants has been questioned. Studies have shown that tympanometry using a 226-Hz probe tone can produce normal traces in infants younger than 4 months with confirmed OME [4–6]. It is also possible to obtain abnormal traces using a 226-Hz probe tone in normal ears [7]. Numerous studies have reported the superiority of a 1000-Hz frequency probe tone. Meyer et al. suggested that a 1000-Hz probe tone is more reliable than a 226-Hz probe tone for diagnosing OME in infants younger than 6 months [6]. Hoffmann et al. recommended using a 1000-Hz probe tone in infants up to the age of 9 months [3]. Alaerts et al. suggested that for children younger than 3 months, a 1000-Hz probe tone always be used, for children between 3 and 9 months, a two-stage evaluation be performed: first at 1000-Hz and then with a 226-Hz probe in the case of a failed result [2]. However, most of these studies examined Caucasian populations and presented normative data. It has been reported that there are differences in the parameters of middle and external ear between the Asians and Caucasians such as static admittance, tympanometric width, tympanometric peak pressure, and ear canal volume [8]. To our knowledge, there is one study reported in the English-language literature has examined when a 1000-Hz probe tone should be used in Asian infants [9]. Therefore, this study evaluated the age at which a 1000-Hz probe tone should be used in Korean infants. Materials and methods Subjects This study retrospectively analyzed data from 83 subjects (43 males, 40 females; mean age 9.2 6.2 (range 1–30) months) who visited the Department of Otorhinolaryngology Head and Neck Surgery of Seoul National University Hospital from April 2011 to May 2012 to evaluate hearing or otitis media. After excluding ears with tympanic membrane (TM) perforation, missing medical records, or concurrent sensorineural hearing loss, this study included 152 ears. This research was approved by the Institutional Review Board (IRB No. 1408-019-601) and performed according to the Declaration of Helsinki.
43
a baseline was drawn from a pressure of +200 to 400 mmH2O [9]. A line was drawn vertically from the baseline to the peak of the trace either above (positive) or below (negative) the baseline. The admittance traces were classified as positive (normal middle ear function), negative (abnormal), or indeterminate (could not be classified as either positive or negative). An example is shown in Fig. 1. Excluding three ears for which the traces were classified as indeterminate, 149 ears were analyzed. The middle ear status was assessed by combining the results of three tests: (a) an endoscopic examination of the tympanic membrane (n = 99 ears); (b) myringotomy during ventilation tube insertion under general anesthesia (n = 20 ears); and (c) the air and bone conduction ABR threshold (n = 149 ears). The examination of the TM and the air and bone conduction ABR were the main elements used to judge the middle ear status and myringotomy complemented these results. Subjects’ ears that met at least two of the following criteria were considered to have OME: 1. Air-fluid level, air bubble, or amber color in TM on endoscopic examination; 2. serous or glue discharge at myringotomy during ventilation tube insertion; and 3. air bone gap (ABG) > 20 dB HL at the ABR threshold. The ABR thresholds were tested with the Navigator Pro system. A click stimulus with a 100-ms pulse duration with alternating polarity was presented through an insert ear phone transducer at a repetition rate of 11.1/s. A 10-ms (or if necessary 20 ms) poststimulus recording window was used to average at least 1024 stimulus repetitions. Responses were bandpass filtered between the negative and positive electrodes at 300–3000 Hz. Bone conduction thresholds were measured with a Radioear B71 bone conductor placed on the mastoid of the test ear. To elicit the head shadow effect, masking was introduced at stimuli above 50 dB nHL. The data were analyzed for five age groups, each covering a 3month span. The subjects were divided into groups without (OME( )) and with (OME(+)) OME. The categories of the traces were measured for both 226- and 1000-Hz probe tones. The sensitivity and specificity were determined for the different age groups.
Instruments Results A GSI TympStar Middle Ear Analyzer (ver. 2) was used for the 226- and 1000-Hz probe tones. Testing A probe that fit in the subject’s EAC was selected. The test procedures were performed by a professional audiologist in a quiet room and the tympanogram traces were obtained with 226- and 1000-Hz probe tones in random order. Traces that were difficult to interpret owing to artifact due to the restlessness of the infant or an escape of pressure were repeated. Each tympanogram was printed and interpreted by the authors, who were blind to the results of the endoscopic examination of the TM, myringotomy, and air and bone conduction auditory brainstem response (ABR) threshold. To minimize the interpreter differences, all traces were classified by two independent authors who were otology fellows with 1 and 2 years’ experience, respectively. In this study, we used Baldwin’s modification of the method of Marchant et al., who suggested a classification in which a baseline was drawn from a pressure of +300 to 400 mmH2O and the peak susceptance above the baseline was measured. Traces with no peak or a trough-shape implied middle ear dysfunction [10]. Baldwin devised a method that used admittance instead of susceptance and
Of the 149 ears, 98 (65.7%) had no OME and 51 (34.2%) had OME. The numbers of ears with or without OME according to age group are described in Table 1. Distribution of tympanogram types Fig. 2 shows the distribution of tympanogram types according to the age groups using the 226-Hz probe tone in the OME( ) and OME(+) groups. In the OME( ) group, the 226-Hz probe tone mostly produced accurate data consistent with the middle ear status in all age groups. By contrast, in the OME(+) group, the tympanograms were recorded as normal in most ears regardless of the presence of OME, except in infants older than 13 months. Fig. 3 shows the distribution of tympanogram types according to age group using the 1000-Hz probe tone for the OME(–) and OME(+) groups. For the OME( ) group, the tympanograms using the 1000-Hz probe tone were interpreted as normal in most cases in all age groups. For the OME(+) group, the tympanograms using the 1000-Hz probe tone showed abnormal traces in most cases in all age groups. That is, the 1000-Hz probe tone gave reliable results in infants of all ages examined regardless of the presence or absence of OME.
M. Park et al. / International Journal of Pediatric Otorhinolaryngology 79 (2015) 42–46
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Fig. 1. The tympanograms of a 3-month-old infant with an otitis media effusion. The tympanogram using a 226-Hz probe tone showed normal traces (A), whereas that using a 1000-Hz probe tone showed abnormal traces (B).
Table 1 The presence and absence of otitis media effusion according to age group. Age (months)
OME( )
OME(+)
0–3 4–6 7–9 10–12 13–
21 23 23 10 21
2 9 15 4 21
Total (ears) 23 32 38 14 42
Total (ears)
98
51
149
Change according to age To analyze the ages at which use of the 1000-Hz probe tone should be considered, the sensitivities and specificities according to age group were calculated and shown in Table 2. The superiority of the 1000-Hz probe tone over the 226-Hz probe tone in terms of sensitivity was significant for infants up to 12 months old, while for older infants, the difference between them decreased. Regarding the specificity, the difference between the two probe tones was not significant for all age groups. Consequently, the 1000-Hz probe tone is superior to the 226-Hz probe tone for detecting OME in infants up to 12 months old.
Discussion In this study, the 1000-Hz probe tone was more accurate for detecting OME than the 226-Hz probe tone. This concurs with previous studies that showed the superiority of the 1000-Hz probe tone. We showed that the 1000-Hz probe tone was appropriate in Korean infants up to 12 months old. Although there is no consensus
regarding at which age the 1000-Hz probe tone should be used for in Asian infants, we found that the cut-off age for the 1000-Hz probe tone was higher than in previous studies [3,4,11,12]. Two studies reported that the 226-Hz probe tone is unreliable in infants younger than 7 months of age [4,12]. Baldwin reported that the 226-Hz probe tone is invalid in infants younger than 21 weeks and that a 1000-Hz probe tone should be used [11]. Hoffmann et al. suggested using the 1000-Hz probe tone in infants at least up to the age of 9 months [3]. The reasons for the superiority of 1000-Hz probe tone for evaluating the condition of the middle ear in infants are unclear. However, the anatomical and acoustic differences in the middle ears of infants and adults might hold the answer. Comparing the anatomy of the external and middle ears of infants and adults, adults have a larger external ear, middle ear cavity, and mastoid, a different orientation of the tympanic membrane, fusion of the tympanic ring, a decrease in the overall mass of the middle ear, tightening of the ossicular joints, closer coupling of the stapes to the annular ligament, and a bony ear canal wall. These differences affect two mechanisms. First, the ear canal impedance and reflection coefficient responses [12] and the resonance frequency for adults and infants differ. The average resonance frequency for adults is about 900 (range 650–1400) Hz [13]. Therefore, the 226Hz probe tone effectively transmits energy into the middle ear of adults. In comparison, that of infants is much lower than that of adults, and the 1000-Hz probe tone is effective [7]. Second, the adult middle ear system is stiffness-controlled, while the infant middle ear system is mass-controlled. Since the response of frequency for mass and stiffness is different, the 1000-Hz probe tone reflects the mass-controlled system, whereas the 226-Hz probe tone reflects the stiffness-controlled system.
M. Park et al. / International Journal of Pediatric Otorhinolaryngology 79 (2015) 42–46
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Fig. 2. The distribution of 226-Hz tympanogram types in ears without (A) and with (B) otitis media effusion according to Baldwin’s modification of the classification of Marchant et al.
Although it is somewhat unclear why the 1000-Hz probe tone can be used in somewhat older Korean infants compared to previous reports [2,4,11,12], ethnicity might hold the answer as most of the previous studies examined Caucasians [2,3,11]. Ethnicity is widely accepted as a variable affecting the mechanical and acoustical properties of the external and middle ears. First, adult Asians have a smaller EAC [8,14–16] than Caucasians. Ear canal volume might be a factor determining the probe tone frequency [3]. The narrower the EAC is, the better the 1000-Hz probe tone is for evaluating middle ear pathology. Hoffmann et al. suggested that 1000-Hz probe tone gives more precise results in ear canals smaller than 0.5 mL in the German population [3]. Second, Asians have smaller middle ears [8,14–16] and lower middle ear compliance than Caucasians. This concurs with findings that Asians have lower admittance [8] and lower middle ear muscle reflex thresholds than Caucasians [14]. These differences in EAC and middle ear size might result from differences in body size [8]. This is also supported by an animal model in which the size of the middle ear structures was related to body size [17,18]. Determining the best diagnostic tool for identifying middle ear effusions in neonates and infants is challenging. Visualization of the TM is an important method for evaluating otitis media, and pneumatic otoscopy, microscopy, and otoendoscopy have been used widely. These three methods have relatively high sensitivities and specificities in children: pneumatic otoscopy 84.6–93.0% sensitivity and 58–100% specificity [19–22] in infants; microscopy 88.0% sensitivity and 89.0% specificity in infants [23–26]; video
otoendoscopy 97.8% sensitivity and 100% specificity in children [27]. Recent improvements in high-quality, small-diameter, rigid endoscopes have led pediatric otologists to use otoendoscopy widely. However, some reports suggest that these three methods are not reliable in restless infants [3], with a narrow EAC and obscured cerumen [3], and less distinct landmarks [28], and there is low interobserver agreement regarding OME [29]. The presence of transient evoked otoacoustic emissions (TEOAE) indicates normal peripheral hearing [11], although TEOAE might be present despite middle ear dysfunction [30] or absent despite normal middle ear function [11]. Myringotomy is reliable [3], but cannot be applied in all cases. In addition, it might not always be accurate. We have sometimes observed that middle ear effusion can become scanty or disappear during the induction of general anesthesia, possibly due to positive pressure on the Eustachian tube orifice. Therefore, we think that ABR thresholds, including air and bone conduction thresholds, are more accurate at detecting the conductive component of the middle ear. Measuring the bone conduction ABR threshold for infants has been recommended since the late 1970s [31,32]. Due to a few technical difficulties, however, such as the narrow dynamic range, masking problems, stimulus artifact, and underestimation of low-frequency hearing loss, this has not been adopted widely [33]. Despite these difficulties, we document the conductive hearing loss component using the air and bone conduction ABR thresholds at our institute. Recognizing these advantages and disadvantages of each auditory function test, we believe that the combined use of these diagnostic tools improves the reliability of detecting the presence of OME.
Fig. 3. The distribution of 1000-Hz tympanogram types in ears without (A) and with (B) otitis media effusion according to Baldwin’s modification of the classification of Marchant et al.
M. Park et al. / International Journal of Pediatric Otorhinolaryngology 79 (2015) 42–46
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Table 2 Comparison of the sensitivity and specificity of the 226- and 1000-Hz probe tones. Probe tone
Age group (mo)
226-Hz
Sensitivity (%) Specificity (%)
1000-Hz
Sensitivity (%) Specificity (%)
0–3
4–6
7–9
10–12
13–
0 95.2
0 100.0
6.6 100.0
0 90.0
76.2 95.2
100.0 100.0
100.0 91.3
93.3 87.0
100.0 100.0
85.7 76.2
This study had some limitations. First, it is not clear whether the difference in the EAC and middle ears of Asian and Caucasian adults [8] is replicated in infants and children. This is especially important because OME is one of the most common diseases of infants and children worldwide. Second, we did not evaluate tympanometric parameters such as the admittance, tympanometric peak pressure, tympanometric width, and EAC volume, which would improve the validity of our data. Finally, it is difficult to infer whether our results can be applied to Asian infants because we studied only Korean infants. Further study should compare the EAC and middle ear sizes of Caucasians and other Asian ethnic groups. In conclusion, we confirmed the usefulness of the 1000-Hz probe tone in infants for detecting changes in the middle ear following otitis media. We recommend including the 1000-Hz probe tone in the audiological test battery for Korean infants younger than 12 months. Conflict of interest statement The authors report no conflict of interest, financially or otherwise. Acknowledgement This work was supported by grant no 04-2013-0420130610 from the SNUH Research Fund. References [1] American Academy of Family Physicians, American Academy of OtolaryngologyHead and Neck Surgery, American Academy of Pediatrics Subcommittee on Otitis Media with Effusion, Otitis media with effusion, Pediatrics 113 (5) (2004) 1412–1429. [2] J. Alaerts, H. Luts, J. Wouters, Evaluation of middle ear function in young children: clinical guidelines for the use of 226- and 1,000-Hz tympanometry, Otol. Neurotol. 28 (2007) 727–732. [3] A. Hoffmann, D. Deuster, K. Rosslau, A. Knief, A. Am Zehnhoff-Dinnesen, C.M. Schmidt, Feasibility of 1000 Hz tympanometry in infants: tympanometric trace classification and choice of probe tone in relation to age, Int. J. Pediatr. Otorhinolaryngol. 77 (2013) 1198–1203. [4] J.L. Paradise, C.G. Smith, C.D. Bluestone, Tympanometric detection of middle ear effusion in infants and young children, Pediatrics 58 (1976) 198–210. [5] P.A. Shurin, S.I. Pelton, J.O. Klein, Otitis media in the newborn infant, Ann. Otol. Rhinol. Laryngol. 85 (1976) 216–222. [6] S.E. Meyer, C.A. Jardine, W. Deverson, Developmental changes in tympanometry: a case study, Br. J. Audiol. 31 (1997) 189–195. [7] D.H. Keefe, E. Levi, Maturation of the middle and external ears: acoustic powerbased responses and reflectance tympanometry, Ear Hear. 17 (1996) 361–373.
[8] N. Shahnaz, D. Davies, Standard and multifrequency tympanometric norms for Caucasian and Chinese young adults, Ear Hear. 27 (2006) 75–90. [9] L. Zhiqi, Y. Kun, H. Zhiwu, Tympanometry in infants with middle ear effusion having been identified using spiral computerized tomography, Am. J. Otolaryngol. 31 (2010) 96–103. [10] C.D. Marchant, P.M. McMillan, P.A. Shurin, C.E. Johnson, V.A. Turczyk, J.C. Feinstein, et al., Objective diagnosis of otitis media in early infancy by tympanometry and ipsilateral acoustic reflex thresholds, J. Pediatr. 109 (1986) 590–595. [11] M. Baldwin, Choice of probe tone and classification of trace patterns in tympanometry undertaken in early infancy, Int. J. Audiol. 45 (7) (2006) 417–427 (2006). [12] D.H. Keefe, J.C. Bulen, K.H. Arehart, E.M. Burns, Ear-canal impedance and reflection coefficient in human infants and adults, J. Acoust. Soc. Am. 94 (5) (1993) 2617–2638. [13] J. Lantz, M. Petrak, L. Prigge, Using the 1000-Hz probe tone to measure immittance in infants, Hear. J. 57 (2004) 34–42. [14] J.C. Saunders, D.E. Doan, Y.E. Cohen, The contribution of middle-ear sound conduction to auditory development, Comp. Biochem. Physiol. Comp. Physiol. 106 (1993) 7–13. [15] J. Chan, B. McPherson, Spontaneous and transient evoked otoacoustic emissions: a racial comparison, J. Audiol. Med. 10 (2001) 20–32. [16] I.K. Wan, L.L. Wong, Tympanometric norms for Chinese young adults, Ear Hear. 23 (2002) 416–421. [17] G.T. Huang, J.J. Rosowski, W.T. Peake, Relating middle-ear acoustic performance to body size in the cat family: measurements and models, J. Comp. Physiol. A 186 (5) (2000) 447–465. [18] J.J. Rosowski, Outer and middle ears, in: R.R. Fay, A.N. Popper (Eds.), Comparative Hearing: Mammals, Springer, New York, NY, 1994, pp. 172–247. [19] T. Finitzo, S. Friel-Patti, K. Chinn, O. Brown, Tympanometry and otoscopy prior to myringotomy: issues in diagnosis of otitis media, Int. J. Pediatr. Otorhinolaryngol. 24 (1992) 101–110. [20] J.G. Toner, B. Mains, Pneumatic otoscopy and tympanometry in the detection of middle ear effusion, Clin. Otolaryngol. Allied Sci. 15 (1990) 121–123. [21] R. Vaughan-Jones, R.P. Mills, The Welch Allyn Audioscope and Microtymp: their accuracy and that of pneumatic otoscopy, tympanometry and pure tone audiometry as predictors of otitis media with effusion, J. Laryngol.. Otol. 106 (1992) 600–602. [22] P.K. Harris, K.M. Hutchinson, J. Moravec, The use of tympanometry and pneumatic otoscopy for predicting middle ear disease, Am. J. Audiol. 14 (2005) 3–13. [23] D.J. Rogers, M.E. Boseley, M.T. Adams, R.L. Makowski, M.H. Hohman, Prospective comparison of handheld pneumatic otoscopy, binocular microscopy, and tympanometry in identifying middle ear effusions in children, Int. J. Pediatr. Otorhinolaryngol. 74 (2010) 1140–1143. [24] D.E. Young, W.J. Ten Cate, Z. Ahmad, R.P. Morton, The accuracy of otomicroscopy for the diagnosis of paediatric middle ear effusions, Int. J. Pediatr. Otorhinolaryngol. 73 (2009) 825–828. [25] M.J. Fields, R.S. Allison, P. Corwin, P.S. White, J. Doherty, Microtympanometry, microscopy and tympanometry in evaluating middle ear effusion prior to myringotomy, N.Z. Med. J. 106 (1993) 386–387. [26] D.H. Lee, S.W. Yeo, Clinical diagnostic accuracy of otitis media with effusion in children, and significance of myringotomy: diagnostic or therapeutic? J. Korean Med. Sci. 19 (2004) 739–743. [27] A.S. Shiao, Y.C. Guo, A comparison assessment of videotelescopy for diagnosis of pediatric otitis media with effusion, Int. J. Pediatr. Otorhinolaryngol. 69 (2005) 1497–1502. [28] L.M. Mc, C.H. Webb, Ear studies in the newborn infant: natural appearance and incidence of obscuring by vernix cleansing of vernix, and description of drum and canal after cleansing, J. Pediatr. 51 (1957) 672–677. [29] M.M. LaRossa, S. Mitchell, J.W. Cardinal, Tympanometry as a screening tool in the NICU: is it effective? Neonatal Netw. 12 (1993) 33–35. [30] C.L. Taylor, R.P. Brooks, Screening for hearing loss and middle-ear disorders in children using TEOAEs, Am. J. Audiol. 9 (2000) 50–55. [31] E.Y. Yang, A. Stuart, G.T. Mencher, L.S. Mencher, M.J. Vincer, Auditory brain stem responses to air- and bone-conducted clicks in the audiological assessment of atrisk infants, Ear Hear. 14 (1993) 175–182. [32] E.Y. Yang, A. Stuart, R. Stenstrom, W.B. Green, Test-retest variability of the auditory brainstem response to bone-conducted clicks in newborn infants, Audiology 32 (1993) 89–94. [33] P.E. Campbell, C.M. Harris, S. Hendricks, T. Sirimanna, Bone conduction auditory brainstem responses in infants, J. Laryngol. Otol. 118 (2004) 117–122.
Contents lists available at ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Usefulness of 1000-Hz probe tone in tympanometry according to age in Korean infants Mina Park a, Kyu-Hee Han a,b, Hyunseo Jung a, Mee-Hee Kim a, Hyun-Kyung Chang a, Shin Hye Kim a, Moo Kyun Park a,c, Jun Ho Lee a,c,* a
Department of Otorhinolaryngology—Head and Neck Surgery, Seoul National University College of Medicine, Seoul National University Hospital, Seoul, South Korea Department of Otorhinolaryngology, National Medical Center, Seoul, South Korea c Sensory Organ Research Institute, Seoul National University Medical Research Center, Seoul, South Korea b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 7 September 2014 Received in revised form 27 October 2014 Accepted 31 October 2014 Available online 13 November 2014
Objective: Numerous studies have shown the superiority of a 1000-Hz frequency probe tone for evaluating the middle ear status of infants. However, most of these studies examined Caucasian populations. This study validated the 1000-Hz probe tone and evaluated the age at which it should be used in Korean infants. Methods: Data from 83 infants (43 males, 40 females; mean age 9.2 6.2 (range 1–30) months, 165 ears) were analyzed. Tympanograms were classified according to Baldwin’s modification of the method of Marchant et al. and correlated with results based on combined diagnostic tests, including an endoscopic examination of the tympanic membrane, myringotomy findings, and the air and bone conduction auditory brainstem response (ABR) thresholds. Data were analyzed in five age groups, each covering a 3-month range. The traces were measured for both 226- and 1000-Hz probe tones. The sensitivity and specificity for the different age groups were also determined. Results: For the 226-Hz probe tone, the tympanograms showed normal traces for most ears with otitis media effusions in infants younger than 12 months. By contrast, the tympanograms using the 1000-Hz probe tone showed abnormal traces in most of the infants with otitis media effusions in all age groups. In infants with no otitis media effusion, the tympanograms using both 226- and 1000-Hz probe tones were interpreted as normal in most cases in all age groups. In infants younger than 12 months, the sensitivity of the 226-Hz probe tone was very low (0–6.6%), whereas that of the 1000-Hz probe tone was very high (90–100%). In infants older than 13 months, however, the sensitivities of the 226- and 1000-Hz probe tones were 76.2% and 85.7%, respectively. Regarding specificity, the difference between the two probe tones was not significant for any age group. Conclusions: This study confirmed the superiority of the 1000-Hz probe tone for evaluating the middle ear in infants. We recommend using a 1000-Hz probe tone at least up to the age of 12 months for Korean infants. ß 2014 Elsevier Ireland Ltd. All rights reserved.
Keywords: 1000-Hz probe tone Otitis media effusion Asian Korean Infant High-frequency tympanometry
Introduction Otitis media effusion (OME) is one of the most common diseases in infants. It is thought that OME occurs in more than half of all children in the first year of life [1]. Recurrent OME can result
* Corresponding author at: Department of Otorhinolaryngology—Head and Neck Surgery, Seoul National University College of Medicine, Seoul National University Hospital, 101 Daehangno, Jongno-gu, Seoul, South Korea. Tel.: +82 2 2072 2445; fax: +82 2 745 2387. E-mail address: [email protected] (J.H. Lee). http://dx.doi.org/10.1016/j.ijporl.2014.10.041 0165-5876/ß 2014 Elsevier Ireland Ltd. All rights reserved.
in mild to moderate hearing loss because it affects the mobility of the ossicles and tympanic membrane [2]. This hearing loss might affect language development and cognition [2]. In addition, OME frequently causes false-positive results in newborn hearing screening. Consequently, it is important to assess the middle ear status of infants accurately. However, the diagnosis of OME is difficult because children are restless during examination and they have small external auditory canals (EAC) [3]. Tympanometry in pediatric audiology is most commonly used to measure the middle ear pressure, which assists in the identification of OME. The conventional 226-Hz probe tone is a well-established method used in adults and children. Although the test is easy and the traces are
M. Park et al. / International Journal of Pediatric Otorhinolaryngology 79 (2015) 42–46
easy to interpret, its validity for infants has been questioned. Studies have shown that tympanometry using a 226-Hz probe tone can produce normal traces in infants younger than 4 months with confirmed OME [4–6]. It is also possible to obtain abnormal traces using a 226-Hz probe tone in normal ears [7]. Numerous studies have reported the superiority of a 1000-Hz frequency probe tone. Meyer et al. suggested that a 1000-Hz probe tone is more reliable than a 226-Hz probe tone for diagnosing OME in infants younger than 6 months [6]. Hoffmann et al. recommended using a 1000-Hz probe tone in infants up to the age of 9 months [3]. Alaerts et al. suggested that for children younger than 3 months, a 1000-Hz probe tone always be used, for children between 3 and 9 months, a two-stage evaluation be performed: first at 1000-Hz and then with a 226-Hz probe in the case of a failed result [2]. However, most of these studies examined Caucasian populations and presented normative data. It has been reported that there are differences in the parameters of middle and external ear between the Asians and Caucasians such as static admittance, tympanometric width, tympanometric peak pressure, and ear canal volume [8]. To our knowledge, there is one study reported in the English-language literature has examined when a 1000-Hz probe tone should be used in Asian infants [9]. Therefore, this study evaluated the age at which a 1000-Hz probe tone should be used in Korean infants. Materials and methods Subjects This study retrospectively analyzed data from 83 subjects (43 males, 40 females; mean age 9.2 6.2 (range 1–30) months) who visited the Department of Otorhinolaryngology Head and Neck Surgery of Seoul National University Hospital from April 2011 to May 2012 to evaluate hearing or otitis media. After excluding ears with tympanic membrane (TM) perforation, missing medical records, or concurrent sensorineural hearing loss, this study included 152 ears. This research was approved by the Institutional Review Board (IRB No. 1408-019-601) and performed according to the Declaration of Helsinki.
43
a baseline was drawn from a pressure of +200 to 400 mmH2O [9]. A line was drawn vertically from the baseline to the peak of the trace either above (positive) or below (negative) the baseline. The admittance traces were classified as positive (normal middle ear function), negative (abnormal), or indeterminate (could not be classified as either positive or negative). An example is shown in Fig. 1. Excluding three ears for which the traces were classified as indeterminate, 149 ears were analyzed. The middle ear status was assessed by combining the results of three tests: (a) an endoscopic examination of the tympanic membrane (n = 99 ears); (b) myringotomy during ventilation tube insertion under general anesthesia (n = 20 ears); and (c) the air and bone conduction ABR threshold (n = 149 ears). The examination of the TM and the air and bone conduction ABR were the main elements used to judge the middle ear status and myringotomy complemented these results. Subjects’ ears that met at least two of the following criteria were considered to have OME: 1. Air-fluid level, air bubble, or amber color in TM on endoscopic examination; 2. serous or glue discharge at myringotomy during ventilation tube insertion; and 3. air bone gap (ABG) > 20 dB HL at the ABR threshold. The ABR thresholds were tested with the Navigator Pro system. A click stimulus with a 100-ms pulse duration with alternating polarity was presented through an insert ear phone transducer at a repetition rate of 11.1/s. A 10-ms (or if necessary 20 ms) poststimulus recording window was used to average at least 1024 stimulus repetitions. Responses were bandpass filtered between the negative and positive electrodes at 300–3000 Hz. Bone conduction thresholds were measured with a Radioear B71 bone conductor placed on the mastoid of the test ear. To elicit the head shadow effect, masking was introduced at stimuli above 50 dB nHL. The data were analyzed for five age groups, each covering a 3month span. The subjects were divided into groups without (OME( )) and with (OME(+)) OME. The categories of the traces were measured for both 226- and 1000-Hz probe tones. The sensitivity and specificity were determined for the different age groups.
Instruments Results A GSI TympStar Middle Ear Analyzer (ver. 2) was used for the 226- and 1000-Hz probe tones. Testing A probe that fit in the subject’s EAC was selected. The test procedures were performed by a professional audiologist in a quiet room and the tympanogram traces were obtained with 226- and 1000-Hz probe tones in random order. Traces that were difficult to interpret owing to artifact due to the restlessness of the infant or an escape of pressure were repeated. Each tympanogram was printed and interpreted by the authors, who were blind to the results of the endoscopic examination of the TM, myringotomy, and air and bone conduction auditory brainstem response (ABR) threshold. To minimize the interpreter differences, all traces were classified by two independent authors who were otology fellows with 1 and 2 years’ experience, respectively. In this study, we used Baldwin’s modification of the method of Marchant et al., who suggested a classification in which a baseline was drawn from a pressure of +300 to 400 mmH2O and the peak susceptance above the baseline was measured. Traces with no peak or a trough-shape implied middle ear dysfunction [10]. Baldwin devised a method that used admittance instead of susceptance and
Of the 149 ears, 98 (65.7%) had no OME and 51 (34.2%) had OME. The numbers of ears with or without OME according to age group are described in Table 1. Distribution of tympanogram types Fig. 2 shows the distribution of tympanogram types according to the age groups using the 226-Hz probe tone in the OME( ) and OME(+) groups. In the OME( ) group, the 226-Hz probe tone mostly produced accurate data consistent with the middle ear status in all age groups. By contrast, in the OME(+) group, the tympanograms were recorded as normal in most ears regardless of the presence of OME, except in infants older than 13 months. Fig. 3 shows the distribution of tympanogram types according to age group using the 1000-Hz probe tone for the OME(–) and OME(+) groups. For the OME( ) group, the tympanograms using the 1000-Hz probe tone were interpreted as normal in most cases in all age groups. For the OME(+) group, the tympanograms using the 1000-Hz probe tone showed abnormal traces in most cases in all age groups. That is, the 1000-Hz probe tone gave reliable results in infants of all ages examined regardless of the presence or absence of OME.
M. Park et al. / International Journal of Pediatric Otorhinolaryngology 79 (2015) 42–46
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Fig. 1. The tympanograms of a 3-month-old infant with an otitis media effusion. The tympanogram using a 226-Hz probe tone showed normal traces (A), whereas that using a 1000-Hz probe tone showed abnormal traces (B).
Table 1 The presence and absence of otitis media effusion according to age group. Age (months)
OME( )
OME(+)
0–3 4–6 7–9 10–12 13–
21 23 23 10 21
2 9 15 4 21
Total (ears) 23 32 38 14 42
Total (ears)
98
51
149
Change according to age To analyze the ages at which use of the 1000-Hz probe tone should be considered, the sensitivities and specificities according to age group were calculated and shown in Table 2. The superiority of the 1000-Hz probe tone over the 226-Hz probe tone in terms of sensitivity was significant for infants up to 12 months old, while for older infants, the difference between them decreased. Regarding the specificity, the difference between the two probe tones was not significant for all age groups. Consequently, the 1000-Hz probe tone is superior to the 226-Hz probe tone for detecting OME in infants up to 12 months old.
Discussion In this study, the 1000-Hz probe tone was more accurate for detecting OME than the 226-Hz probe tone. This concurs with previous studies that showed the superiority of the 1000-Hz probe tone. We showed that the 1000-Hz probe tone was appropriate in Korean infants up to 12 months old. Although there is no consensus
regarding at which age the 1000-Hz probe tone should be used for in Asian infants, we found that the cut-off age for the 1000-Hz probe tone was higher than in previous studies [3,4,11,12]. Two studies reported that the 226-Hz probe tone is unreliable in infants younger than 7 months of age [4,12]. Baldwin reported that the 226-Hz probe tone is invalid in infants younger than 21 weeks and that a 1000-Hz probe tone should be used [11]. Hoffmann et al. suggested using the 1000-Hz probe tone in infants at least up to the age of 9 months [3]. The reasons for the superiority of 1000-Hz probe tone for evaluating the condition of the middle ear in infants are unclear. However, the anatomical and acoustic differences in the middle ears of infants and adults might hold the answer. Comparing the anatomy of the external and middle ears of infants and adults, adults have a larger external ear, middle ear cavity, and mastoid, a different orientation of the tympanic membrane, fusion of the tympanic ring, a decrease in the overall mass of the middle ear, tightening of the ossicular joints, closer coupling of the stapes to the annular ligament, and a bony ear canal wall. These differences affect two mechanisms. First, the ear canal impedance and reflection coefficient responses [12] and the resonance frequency for adults and infants differ. The average resonance frequency for adults is about 900 (range 650–1400) Hz [13]. Therefore, the 226Hz probe tone effectively transmits energy into the middle ear of adults. In comparison, that of infants is much lower than that of adults, and the 1000-Hz probe tone is effective [7]. Second, the adult middle ear system is stiffness-controlled, while the infant middle ear system is mass-controlled. Since the response of frequency for mass and stiffness is different, the 1000-Hz probe tone reflects the mass-controlled system, whereas the 226-Hz probe tone reflects the stiffness-controlled system.
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Fig. 2. The distribution of 226-Hz tympanogram types in ears without (A) and with (B) otitis media effusion according to Baldwin’s modification of the classification of Marchant et al.
Although it is somewhat unclear why the 1000-Hz probe tone can be used in somewhat older Korean infants compared to previous reports [2,4,11,12], ethnicity might hold the answer as most of the previous studies examined Caucasians [2,3,11]. Ethnicity is widely accepted as a variable affecting the mechanical and acoustical properties of the external and middle ears. First, adult Asians have a smaller EAC [8,14–16] than Caucasians. Ear canal volume might be a factor determining the probe tone frequency [3]. The narrower the EAC is, the better the 1000-Hz probe tone is for evaluating middle ear pathology. Hoffmann et al. suggested that 1000-Hz probe tone gives more precise results in ear canals smaller than 0.5 mL in the German population [3]. Second, Asians have smaller middle ears [8,14–16] and lower middle ear compliance than Caucasians. This concurs with findings that Asians have lower admittance [8] and lower middle ear muscle reflex thresholds than Caucasians [14]. These differences in EAC and middle ear size might result from differences in body size [8]. This is also supported by an animal model in which the size of the middle ear structures was related to body size [17,18]. Determining the best diagnostic tool for identifying middle ear effusions in neonates and infants is challenging. Visualization of the TM is an important method for evaluating otitis media, and pneumatic otoscopy, microscopy, and otoendoscopy have been used widely. These three methods have relatively high sensitivities and specificities in children: pneumatic otoscopy 84.6–93.0% sensitivity and 58–100% specificity [19–22] in infants; microscopy 88.0% sensitivity and 89.0% specificity in infants [23–26]; video
otoendoscopy 97.8% sensitivity and 100% specificity in children [27]. Recent improvements in high-quality, small-diameter, rigid endoscopes have led pediatric otologists to use otoendoscopy widely. However, some reports suggest that these three methods are not reliable in restless infants [3], with a narrow EAC and obscured cerumen [3], and less distinct landmarks [28], and there is low interobserver agreement regarding OME [29]. The presence of transient evoked otoacoustic emissions (TEOAE) indicates normal peripheral hearing [11], although TEOAE might be present despite middle ear dysfunction [30] or absent despite normal middle ear function [11]. Myringotomy is reliable [3], but cannot be applied in all cases. In addition, it might not always be accurate. We have sometimes observed that middle ear effusion can become scanty or disappear during the induction of general anesthesia, possibly due to positive pressure on the Eustachian tube orifice. Therefore, we think that ABR thresholds, including air and bone conduction thresholds, are more accurate at detecting the conductive component of the middle ear. Measuring the bone conduction ABR threshold for infants has been recommended since the late 1970s [31,32]. Due to a few technical difficulties, however, such as the narrow dynamic range, masking problems, stimulus artifact, and underestimation of low-frequency hearing loss, this has not been adopted widely [33]. Despite these difficulties, we document the conductive hearing loss component using the air and bone conduction ABR thresholds at our institute. Recognizing these advantages and disadvantages of each auditory function test, we believe that the combined use of these diagnostic tools improves the reliability of detecting the presence of OME.
Fig. 3. The distribution of 1000-Hz tympanogram types in ears without (A) and with (B) otitis media effusion according to Baldwin’s modification of the classification of Marchant et al.
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Table 2 Comparison of the sensitivity and specificity of the 226- and 1000-Hz probe tones. Probe tone
Age group (mo)
226-Hz
Sensitivity (%) Specificity (%)
1000-Hz
Sensitivity (%) Specificity (%)
0–3
4–6
7–9
10–12
13–
0 95.2
0 100.0
6.6 100.0
0 90.0
76.2 95.2
100.0 100.0
100.0 91.3
93.3 87.0
100.0 100.0
85.7 76.2
This study had some limitations. First, it is not clear whether the difference in the EAC and middle ears of Asian and Caucasian adults [8] is replicated in infants and children. This is especially important because OME is one of the most common diseases of infants and children worldwide. Second, we did not evaluate tympanometric parameters such as the admittance, tympanometric peak pressure, tympanometric width, and EAC volume, which would improve the validity of our data. Finally, it is difficult to infer whether our results can be applied to Asian infants because we studied only Korean infants. Further study should compare the EAC and middle ear sizes of Caucasians and other Asian ethnic groups. In conclusion, we confirmed the usefulness of the 1000-Hz probe tone in infants for detecting changes in the middle ear following otitis media. We recommend including the 1000-Hz probe tone in the audiological test battery for Korean infants younger than 12 months. Conflict of interest statement The authors report no conflict of interest, financially or otherwise. Acknowledgement This work was supported by grant no 04-2013-0420130610 from the SNUH Research Fund. References [1] American Academy of Family Physicians, American Academy of OtolaryngologyHead and Neck Surgery, American Academy of Pediatrics Subcommittee on Otitis Media with Effusion, Otitis media with effusion, Pediatrics 113 (5) (2004) 1412–1429. [2] J. Alaerts, H. Luts, J. Wouters, Evaluation of middle ear function in young children: clinical guidelines for the use of 226- and 1,000-Hz tympanometry, Otol. Neurotol. 28 (2007) 727–732. [3] A. Hoffmann, D. Deuster, K. Rosslau, A. Knief, A. Am Zehnhoff-Dinnesen, C.M. Schmidt, Feasibility of 1000 Hz tympanometry in infants: tympanometric trace classification and choice of probe tone in relation to age, Int. J. Pediatr. Otorhinolaryngol. 77 (2013) 1198–1203. [4] J.L. Paradise, C.G. Smith, C.D. Bluestone, Tympanometric detection of middle ear effusion in infants and young children, Pediatrics 58 (1976) 198–210. [5] P.A. Shurin, S.I. Pelton, J.O. Klein, Otitis media in the newborn infant, Ann. Otol. Rhinol. Laryngol. 85 (1976) 216–222. [6] S.E. Meyer, C.A. Jardine, W. Deverson, Developmental changes in tympanometry: a case study, Br. J. Audiol. 31 (1997) 189–195. [7] D.H. Keefe, E. Levi, Maturation of the middle and external ears: acoustic powerbased responses and reflectance tympanometry, Ear Hear. 17 (1996) 361–373.
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