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Auditory Neuropathy/Dyssynchrony: A Retrospective Analysis of 15 Cases

Abstract

Introduction

Auditory neuropathy/dyssynchrony (AN/AD) comprises a spectrum of pathology affecting the auditory pathways anywhere from the inner hair cells to the brainstem. It is characterized by an absent or atypical auditory brainstem response (ABR) with preservation of the cochlear microphonics and/or otoacoustic emissions (OAEs).

Objective

Retrospective analysis of patients with AN/AD.

Methods

Fifteen patients with AN/AD were included in this study and their records were retrospectively investigated.

Results

Possible etiology of AN/AD was neonatal hyperbilirubinemia in three patients, family history of hearing loss in three patients, consanguineous marriage in two patients, head trauma in two patients, mental motor retardation in one patient, cerebrovascular disease in one patient, and there was no apparent cause in three patients.

Conclusion

Otolaryngologists should keep in mind the diagnosis of AN/AD especially in patients complaining of difficulty in hearing and speech and audiological evidence of disassociation between pure tone and speech audiometry. ABR and OAE testing is recommended in these patients for AN/AD diagnosis.

auditory neuropathy/dyssynchrony; otoacoustic emission; auditory brainstem response


Introduction

Auditory neuropathy/dyssynchrony (AN/AD) is a hearing disorder characterized by an absent or atypical auditory brainstem response (ABR), with preservation of the cochlear microphonics (CM) and/or otoacoustic emissions (OAEs).11 Madden C, Rutter M, Hilbert L, Greinwald JH Jr, Choo DI. Clinical and audiological features in auditory neuropathy. Arch Otolar yngol Head Neck Surg 2002;128(9):1026-1030 22 Lee JSM, McPherson B, Yuen KCP, Wong LLN. Screening for auditory neuropathy in a school for hearing impaired children. Int J Pediatr Otorhinolaryngol 2001;61(1):39-46 In 1996, Starr et al first described this rare entity, drawing on their observations in 10 patients.33 Starr A, Picton TW, Sininger Y, Hood LJ, Berlin CI. Auditory neuropathy. Brain 1996;119(Pt 3):741-753 The authors suggested that these patients were probably similar to those previously reported cases with a paradoxical absence of ABRs and only a slight impairment of pure tone thresholds but in whom CMs or OAEs had not been recorded.33 Starr A, Picton TW, Sininger Y, Hood LJ, Berlin CI. Auditory neuropathy. Brain 1996;119(Pt 3):741-753 44 Worthington DW, Peters JF. Quantifiable hearing and no ABR: paradox or error? Ear Hear 1980;1(5):281-285 55 Kraus N, Ozdamar O, Stein L, Reed N. Absent auditory brain stem response: peripheral hearing loss or brain stem dysfunction? Laryngoscope 1984;94(3):400-406 Also In 1998, Doyle et al reported eight patients with normal transient evoked OAEs (TEOAEs) and distortion product OAEs (DPOAEs) combined with the absence or marked abnormalities of ABRs.66 Doyle KJ, Sininger Y, Starr A. Auditory neuropathy in childhood. Laryngoscope 1998;108(9):1374-1377 Starr et al suggested that this type of hearing impairment is due to a disorder that impairs auditory nerve function and may have as one of its causes a neuropathy of the auditory nerve, occurring either in isolation or as part of a systemic neuropathic process.33 Starr A, Picton TW, Sininger Y, Hood LJ, Berlin CI. Auditory neuropathy. Brain 1996;119(Pt 3):741-753 Clinically, the diagnostic criteria of AN/AD is defined as (1) sensorineural hearing loss, usually bilateral, of any degree; (2) normal outer hair cell function as evidenced by the presence of OAEs and/or CM; (3) absent or atypical ABR; (4) understanding of speech worse than would be predicted from the behavioral or pure tone audiometry; (5) absent acoustic reflexes to the ipsilateral and contralateral tones a 110-dB hearing level.11 Madden C, Rutter M, Hilbert L, Greinwald JH Jr, Choo DI. Clinical and audiological features in auditory neuropathy. Arch Otolar yngol Head Neck Surg 2002;128(9):1026-1030 77 Rapin I, Gravel J. "Auditory neuropathy": physiologic and pathologic evidence calls for more diagnostic specificity. Int J Pediatr Otorhinolaryngol 2003;67(7):707-728 88 ShiW, Ji F, Lan L, et al. Characteristics of cochlear microphonics in infants and young children with auditory neuropathy. Acta Otolaryngol 2012;132(2):188-196 99 Roush P, Frymark T, Venediktov R,Wang B. Audiologic management of auditory neuropathy spectrum disorder in children: a systematic review of the literature. Am J Audiol 2011;20(2):159-170

In this retrospective study, we investigated the audiological findings, history, and clinical manifestations of patients diagnosed with AN/AD at our clinic.

Patients and Methods

Fifteen patients with AN/AD were included in this study, and their records were retrospectively investigated. All of the patients' medical and otologic histories were recorded. A complete ear, nose, and throat examination was performed. Otoscopic examinations were done by an otolaryngologist before testing to rule out any external or middle ear pathology that could affect audiometric measurements. Then pure tone audiometry (250 to 8,000 Hz), tympanometry, and acoustic reflex measurement (500 to 4,000 Hz) were done in a standard fashion (Interacoustic AC 40 and AZ 26, Denmark, Assens). DPOAEs were measured at click levels of 65 (L1) and 55 dB (L2) peak sound pressure for the F1 and F2 components (Homoth Medizinelektronik GmbH&Co, KG, Germany, Hamburg). DPOAE-grams were recorded in one-quarter-octave steps over a frequency range of F2 from 0.5 to 6 kHz. DPOAE values were plotted on a DPOAEgram, which shows the emission level as a function of the F2 frequency. ABRs were recorded using Homoth ABR equipment. Electrodes were placed on the forehead as a ground electrode and on both mastoids as active electrodes. The responses were filtered with a bandpass of 100 to 3,000 Hz. Alternate polarity clicks of 100-millisecond duration were presented monaurally with a repetition rate of 16.4/s. Each ear was tested separately, and all responses were replicated twice. Patients underwent assessment in a state of natural sleep. In this retrospective study, we did not include genetic research; we investigated only according to the history of patients.

Results

Eleven male and four female patients diagnosed with AN/AD (age range: 2 to 52 years and median age: 19.3 years) were included in this study. Possible etiology of AN/AD was neonatal hyperbilirubinemia in three patients. These patients had a history of exchange transfusion because of bilirubin levels over 20 mg/dL. Three patients had family history of hearing loss, two patients had consanguineous marriage, two patients had head trauma, one patient had mental motor retardation (psychomotor retardation), one patient had cerebrovascular disease, and there was no apparent causes in three patients.

Thirteen patients had bilateral and two patients had unilateral AN/AD.

None of the patients with AN/AD had middle or inner ear anomalies on computed tomography or magnetic resonance imaging. Table 1summarizes the patients' demographic, clinical, and audiological features (see also Fig. 1 for a left and right ear ABR and DPOAE recording of a case of AN/AD).

Fig. 1
Left and right ear auditory brain stem response and distortion product otoacoustic emission recording of a case of auditory neuropathy/dyssynchrony. Abbreviations: dBSPL, decibels sound pressure level; DP, distortion product; F1 and F2 used as formulation markers.

Table 1
Clinical and audiological features of the patients with AN/AD

Eight of 15 patients' pure tone audiometric results showed profound hearing losses; however, seven of them had mild to moderate hearing loss. Acoustic reflex tests were also absent in all of the patients.

Discussion

AN/AD is characterized by a unique pattern of hearing loss and distorted ABR with preservation of outer hair cell function.1010 Nikolopoulos TP. Auditory dyssynchrony or auditory neuropathy: understanding the pathophysiology and exploring methods of treatment. Int J Pediatr Otorhinolaryngol 2014;78(2):171-173 1111 Sinha SK, Barman A, Singh NK, Rajeshwari G, Sharanya R. Involvement of peripheral vestibular nerve in individuals with auditory neuropathy. Eur Arch Otorhinolaryngol 2013;270(8):2207-2214 AN/AD comprises a spectrum of pathology affecting the auditory pathways anywhere from the inner hair cells to the brainstem. Thus it is difficult to define the disorder as cochlear or retrocochlear. Increased clinical suspicion supported by appropriate diagnostic tests is needed to establish an accurate diagnosis.1212 Sawada S, Mori N, Mount RJ, Harrison RV. Differential vulnerability of inner and outer hair cell systems to chronic mild hypoxia and glutamate ototoxicity: insights into the cause of auditory neuropathy. J Otolaryngol 2001;30(2):106-114 1313 Marco J, Morant A, Orts M, Pitarch MI, Garcia J. Auditory neuropathy in children. Acta Otolaryngol 2000;120(2):201-204

The clinical findings for auditory neuropathy are associated with several diagnoses including hyperbilirubinemia, neurodegenerative diseases, Charcot-Marie-Tooth syndrome, and other sensorimotor neuropathologies, mitochondrial disorders, and ischemic-hypoxic neuropathy resulting from asphyxia.1414 Cone-Wesson B, Rance G. Auditory neuropathy: a brief review. Curr Opin Otolaryngol Head Neck Surg 2000;8(5):421-425 Also, experimental animal models for auditory neuropathy have been proposed using the carboplatin ototoxicity and ischemic-hypoxic neuropathy methodologies.1212 Sawada S, Mori N, Mount RJ, Harrison RV. Differential vulnerability of inner and outer hair cell systems to chronic mild hypoxia and glutamate ototoxicity: insights into the cause of auditory neuropathy. J Otolaryngol 2001;30(2):106-114 1515 Harrison RV. An animal model of auditory neuropathy. Ear Hear 1998;19(5):355-361 1616 Salvi RJ, Wang J, Ding D, Stecker N, Arnold S. Auditory deprivation of the central auditory system resulting from selective inner hair cell loss: animalmodel of auditory neuropathy. Scand Audiol Suppl 1999;51(Suppl 51):1-12 In our series, three patients with AN/AD had neonatal hyperbilirubinemia, three patients had family history of hearing loss, two patients had consanguineous marriage, two patients had head trauma, one patient had mental motor retardation, and one patient had cerebrovascular disease. We did not find any specific etiology in three patients.

Recently two mechanisms have been proposed for explaining the abnormalities of auditory function: (1) impaired synchrony among nerve fibers and/or (2) reduced neural input.1717 Kraus N, Bradlow AR, Cheatham MA, et al. Consequences of neural asynchrony: a case of auditory neuropathy. J Assoc Res Otolaryngol 2000;1(1):33-45 1818 Starr A, McPherson D, Patterson J, et al. Absence of both auditory evoked potentials and auditory percepts dependent on timing cues. Brain 1991;114(Pt 3):1157-1180 1919 Kirkim G, Serbetçioglu MB, Ceryan K. Auditory neuropathy in children: diagnostic criteria and audiological test results. Kulak Burun Bogaz Ihtis Derg 2005;15(1-2):1-8 It is generally thought that absent or severely distorted ABR is highly likely to be related to impairment of neural synchrony in the auditory pathways. Similar to the previous reports, we could not obtain any response to the click stimulus.

The prevalence of AN/AD in patients with hearing loss ranged from 0.5 to 15% according to studies in literature.1010 Nikolopoulos TP. Auditory dyssynchrony or auditory neuropathy: understanding the pathophysiology and exploring methods of treatment. Int J Pediatr Otorhinolaryngol 2014;78(2):171-173 1111 Sinha SK, Barman A, Singh NK, Rajeshwari G, Sharanya R. Involvement of peripheral vestibular nerve in individuals with auditory neuropathy. Eur Arch Otorhinolaryngol 2013;270(8):2207-2214 Because there are so many possible causes for AN/AD, it is difficult to estimate its exact prevalence.1414 Cone-Wesson B, Rance G. Auditory neuropathy: a brief review. Curr Opin Otolaryngol Head Neck Surg 2000;8(5):421-425 Davis and Hirsh suggested that 1 in every 200 hearing-impaired children had ABR findings inconsistent with pure tone findings.2020 Davis H, Hirsh SK. The audiometric utility of brain stem responses to low-frequency sounds. Audiology 1976;15(3):181-195 Permanent bilateral hearing loss is seen in 1.4 per 1,000 live births. Therefore the incidence of AN/AD is likely to be 1.4 per 10,000 live births. According to Rance et al, AN/AD would be present in 2.3 per 1,000 infants with risk factors for hearing loss. Thus, if OAE tests alone are used for hearing screening of infants with risk factors, 11% of infants with permanent hearing loss will be missed.1414 Cone-Wesson B, Rance G. Auditory neuropathy: a brief review. Curr Opin Otolaryngol Head Neck Surg 2000;8(5):421-425 2121 RanceG, Beer DE, Cone-Wesson B, et al. Clinical findings for a group of infants and young children with auditory neuropathy. Ear Hear 1999;20(3):238-252 These data are important for designing the newborn hearing screening protocols especially in developing countries.

Patients with AN/AD complain of hearing disability, especially in the presence of noise, and tend to have word-recognition scores that are disproportionately poorer than would be expected by audiometric thresholds. In our series, all of the patients were admitted to our department with the complaint of hearing and speech disability. Only one of them had understandable speech. Pure tone audiometric thresholds are variable in patients with AN/AD, and the degree of hearing loss can range from mild to profound sensorineural type. Eight of our patients' pure tone audiometric results showed profound hearing losses, and seven had mild to moderate hearing loss. Acoustic reflex tests were also absent in all of the patients. Because OAEs and CM are dependent on the integrity of cochlear outer hair cells and are "preneural" events, they may be present and normal in AN/AD; however, absent or grossly abnormal ABRs are seen.1414 Cone-Wesson B, Rance G. Auditory neuropathy: a brief review. Curr Opin Otolaryngol Head Neck Surg 2000;8(5):421-425 2222 Maris M, Venstermans C, Boudewyns AN. Auditory neuropathy/ dyssynchrony as a cause of failed neonatal hearing screening. Int J Pediatr Otorhinolaryngol 2011;75(7):973-975 Similar findings were observed in our cases.

The hallmark of AN/AD is an abnormal ABR reading together with a normal OAE reading. However, there is a lack of actual diagnostic procedures for AN/AD. Other tests may also be used as part of a more comprehensive evaluation of an individual's hearing and speech-perception abilities. Electrocochleography (ECoG), which objectively assesses cochlear potentials, is the indicated clinical procedure to analyze CMs. Although transtympanic ECoG yields recordings with higher amplitudes and lower test–retest variability, it has the disadvantage of being an invasive procedure. Extratympanic ECoG, therefore, is clinically more useful in this context, supporting an audiological diagnosis and increasing knowledge about cochlear function in AN/AD. ECoG is the most appropriate procedure for assessing cochlear function and helping identify CMs. CMs play an important role in the diagnosis of AN/AD. It is necessary and helpful to diagnose the sites of lesion in patients with AN/AD by analyzing the patterns of CM amplitudes. Therefore, recently ECoG has been used for diagnosing AN/AD.88 ShiW, Ji F, Lan L, et al. Characteristics of cochlear microphonics in infants and young children with auditory neuropathy. Acta Otolaryngol 2012;132(2):188-196 2323 Anastasio ART, Alvarenga KdeF, Costa Filho OA. Extratympanic electrocochleography in the diagnosis of auditory neuropathy/ auditory dyssynchrony. Braz J Otorhinolaryngol 2008;74(1): 132-136

Some patients with AN/AD lost their OAE over the period of time but there was no associated change in pure tone thresholds. It has also been reported that some patients with AN/AD do not have OAEs but rather evidence of hair cell function was evident from CM. Therefore these authors suggested that presence of CM with absent ABR seems to be reliable criteria for diagnosing AN/AD.2424 Sanyelbhaa Talaat H, Khalil LH, Khafagy AH, Alkandari MM, Zein AM. Persistence of otoacoustic emissions in childrenwith auditory neuropathy spectrum disorders. Int J Pediatr Otorhinolaryngol 2013;77(5):703-706 2525 Mittal R, Ramesh AV, Panwar SS, Nilkanthan A, Nair S, Mehra PR. Auditory neuropathy spectrum disorder: its prevalence and audiological characteristics in an Indian tertiary care hospital. Int J Pediatr Otorhinolaryngol 2012;76(9):1351-1354

There has been controversy regarding whether to provide hearing devices (hearing aids, personal radiofrequency [frequency modulation] systems, or cochlear implants) to children with AN/AD and whether to offer aural-oral or visual-manual modes of habilitation.1414 Cone-Wesson B, Rance G. Auditory neuropathy: a brief review. Curr Opin Otolaryngol Head Neck Surg 2000;8(5):421-425 2626 De Leenheer EM, Dhooge IJ, Veuillet E, Lina-Granade G, Truy E. Cochlear implantation in 3 adults with auditory neuropathy/ auditory dys-synchrony. B-ENT 2008;4(3):183-191 Berlin et al suggested that conventional amplification has little beneficial effect on AN/AD patients.2727 Berlin CI,Morlet T, Hood LJ. Auditory neuropathy/dyssynchrony its diagnosis and management. Pediatr Clin N Am 2003;50:331-340 On the contrary, Cone-Wesson et al concluded that nearly 50% of children demonstrate some benefit from the use of conventional hearing aids and that a trial of amplification is warranted.1414 Cone-Wesson B, Rance G. Auditory neuropathy: a brief review. Curr Opin Otolaryngol Head Neck Surg 2000;8(5):421-425 2121 RanceG, Beer DE, Cone-Wesson B, et al. Clinical findings for a group of infants and young children with auditory neuropathy. Ear Hear 1999;20(3):238-252 Cochlear implantation may also be an option for hearing rehabilitation. Although the outcome of cochlear implantation in children with AN/AD might vary, it is favorable in most cases. Cochlear implantation seems a justified hearing rehabilitation option for children with AN/AD and limited benefits from conventional hearing aids.2828 Kontorinis G, Lloyd SK,Henderson L, et al. Cochlear implantation in children with auditory neuropathy spectrum disorders. Cochlear Implants Int 2014;15(Suppl 1):S51-S54 2929 Budenz CL, Telian SA, Arnedt C, et al. Outcomes of cochlear implantation in childrenwith isolated auditory neuropathy versus cochlear hearing loss. Otol Neurotol 2013;34(3):477-483 3030 Cardon G, Sharma A. Central auditory maturation and behavioral outcome in children with auditory neuropathy spectrum disorder who use cochlear implants. Int J Audiol 2013;52(9): 577-586 In our series, we obtained some development in hearing and speech abilities using a conventional hearing aid in one case.

The current position statement of The Joint Committee on Infant Hearing (2007) calls for (1) physiological hearing screening of all infants before they are 1 month old, (2) confirmation of the hearing loss before 3 months of age, and (3) commencement of an interdisciplinary intervention program before the infant is 6 months old. Moreover, the scope of disorders targeted for identification has been expanded to include neural hearing loss (especially AN/AD) in addition to sensorineural and permanent conductive hearing loss.3131 American Academy of Pediatrics, Joint Committee on Infant Hearing. Year 2007 position statement: principles and guidelines for early hearing detection and intervention programs. Pediatrics 2007;120(4):898-921

Conclusion

Although AN/AD affects only a small portion of all persons with hearing loss, the infant, child, or adult with AN/AD is often most disabled by the hearing disorder because of the lack of knowledge about its cause and, more importantly, its treatment. Continued research regarding the causes and pathologies underlying this disorder is needed.1010 Nikolopoulos TP. Auditory dyssynchrony or auditory neuropathy: understanding the pathophysiology and exploring methods of treatment. Int J Pediatr Otorhinolaryngol 2014;78(2):171-173 However, it is also necessary to develop methods to reduce false-negative screening results and to provide accurate diagnosis for the disorder.22 Lee JSM, McPherson B, Yuen KCP, Wong LLN. Screening for auditory neuropathy in a school for hearing impaired children. Int J Pediatr Otorhinolaryngol 2001;61(1):39-46 A combined OAE and ABR screening procedure may be considered to overcome the limitations of OAE-only procedures especially in high-risk infants. Also, it should be kept in mind that adult AN/D cases may be related with systemic neurological diseases.

References

  • 1
    Madden C, Rutter M, Hilbert L, Greinwald JH Jr, Choo DI. Clinical and audiological features in auditory neuropathy. Arch Otolar yngol Head Neck Surg 2002;128(9):1026-1030
  • 2
    Lee JSM, McPherson B, Yuen KCP, Wong LLN. Screening for auditory neuropathy in a school for hearing impaired children. Int J Pediatr Otorhinolaryngol 2001;61(1):39-46
  • 3
    Starr A, Picton TW, Sininger Y, Hood LJ, Berlin CI. Auditory neuropathy. Brain 1996;119(Pt 3):741-753
  • 4
    Worthington DW, Peters JF. Quantifiable hearing and no ABR: paradox or error? Ear Hear 1980;1(5):281-285
  • 5
    Kraus N, Ozdamar O, Stein L, Reed N. Absent auditory brain stem response: peripheral hearing loss or brain stem dysfunction? Laryngoscope 1984;94(3):400-406
  • 6
    Doyle KJ, Sininger Y, Starr A. Auditory neuropathy in childhood. Laryngoscope 1998;108(9):1374-1377
  • 7
    Rapin I, Gravel J. "Auditory neuropathy": physiologic and pathologic evidence calls for more diagnostic specificity. Int J Pediatr Otorhinolaryngol 2003;67(7):707-728
  • 8
    ShiW, Ji F, Lan L, et al. Characteristics of cochlear microphonics in infants and young children with auditory neuropathy. Acta Otolaryngol 2012;132(2):188-196
  • 9
    Roush P, Frymark T, Venediktov R,Wang B. Audiologic management of auditory neuropathy spectrum disorder in children: a systematic review of the literature. Am J Audiol 2011;20(2):159-170
  • 10
    Nikolopoulos TP. Auditory dyssynchrony or auditory neuropathy: understanding the pathophysiology and exploring methods of treatment. Int J Pediatr Otorhinolaryngol 2014;78(2):171-173
  • 11
    Sinha SK, Barman A, Singh NK, Rajeshwari G, Sharanya R. Involvement of peripheral vestibular nerve in individuals with auditory neuropathy. Eur Arch Otorhinolaryngol 2013;270(8):2207-2214
  • 12
    Sawada S, Mori N, Mount RJ, Harrison RV. Differential vulnerability of inner and outer hair cell systems to chronic mild hypoxia and glutamate ototoxicity: insights into the cause of auditory neuropathy. J Otolaryngol 2001;30(2):106-114
  • 13
    Marco J, Morant A, Orts M, Pitarch MI, Garcia J. Auditory neuropathy in children. Acta Otolaryngol 2000;120(2):201-204
  • 14
    Cone-Wesson B, Rance G. Auditory neuropathy: a brief review. Curr Opin Otolaryngol Head Neck Surg 2000;8(5):421-425
  • 15
    Harrison RV. An animal model of auditory neuropathy. Ear Hear 1998;19(5):355-361
  • 16
    Salvi RJ, Wang J, Ding D, Stecker N, Arnold S. Auditory deprivation of the central auditory system resulting from selective inner hair cell loss: animalmodel of auditory neuropathy. Scand Audiol Suppl 1999;51(Suppl 51):1-12
  • 17
    Kraus N, Bradlow AR, Cheatham MA, et al. Consequences of neural asynchrony: a case of auditory neuropathy. J Assoc Res Otolaryngol 2000;1(1):33-45
  • 18
    Starr A, McPherson D, Patterson J, et al. Absence of both auditory evoked potentials and auditory percepts dependent on timing cues. Brain 1991;114(Pt 3):1157-1180
  • 19
    Kirkim G, Serbetçioglu MB, Ceryan K. Auditory neuropathy in children: diagnostic criteria and audiological test results. Kulak Burun Bogaz Ihtis Derg 2005;15(1-2):1-8
  • 20
    Davis H, Hirsh SK. The audiometric utility of brain stem responses to low-frequency sounds. Audiology 1976;15(3):181-195
  • 21
    RanceG, Beer DE, Cone-Wesson B, et al. Clinical findings for a group of infants and young children with auditory neuropathy. Ear Hear 1999;20(3):238-252
  • 22
    Maris M, Venstermans C, Boudewyns AN. Auditory neuropathy/ dyssynchrony as a cause of failed neonatal hearing screening. Int J Pediatr Otorhinolaryngol 2011;75(7):973-975
  • 23
    Anastasio ART, Alvarenga KdeF, Costa Filho OA. Extratympanic electrocochleography in the diagnosis of auditory neuropathy/ auditory dyssynchrony. Braz J Otorhinolaryngol 2008;74(1): 132-136
  • 24
    Sanyelbhaa Talaat H, Khalil LH, Khafagy AH, Alkandari MM, Zein AM. Persistence of otoacoustic emissions in childrenwith auditory neuropathy spectrum disorders. Int J Pediatr Otorhinolaryngol 2013;77(5):703-706
  • 25
    Mittal R, Ramesh AV, Panwar SS, Nilkanthan A, Nair S, Mehra PR. Auditory neuropathy spectrum disorder: its prevalence and audiological characteristics in an Indian tertiary care hospital. Int J Pediatr Otorhinolaryngol 2012;76(9):1351-1354
  • 26
    De Leenheer EM, Dhooge IJ, Veuillet E, Lina-Granade G, Truy E. Cochlear implantation in 3 adults with auditory neuropathy/ auditory dys-synchrony. B-ENT 2008;4(3):183-191
  • 27
    Berlin CI,Morlet T, Hood LJ. Auditory neuropathy/dyssynchrony its diagnosis and management. Pediatr Clin N Am 2003;50:331-340
  • 28
    Kontorinis G, Lloyd SK,Henderson L, et al. Cochlear implantation in children with auditory neuropathy spectrum disorders. Cochlear Implants Int 2014;15(Suppl 1):S51-S54
  • 29
    Budenz CL, Telian SA, Arnedt C, et al. Outcomes of cochlear implantation in childrenwith isolated auditory neuropathy versus cochlear hearing loss. Otol Neurotol 2013;34(3):477-483
  • 30
    Cardon G, Sharma A. Central auditory maturation and behavioral outcome in children with auditory neuropathy spectrum disorder who use cochlear implants. Int J Audiol 2013;52(9): 577-586
  • 31
    American Academy of Pediatrics, Joint Committee on Infant Hearing. Year 2007 position statement: principles and guidelines for early hearing detection and intervention programs. Pediatrics 2007;120(4):898-921

Publication Dates

  • Publication in this collection
    Apr-Jun 2015

History

  • Received
    04 June 2014
  • Accepted
    25 Aug 2014
Fundação Otorrinolaringologia R. Teodoro Sampaio, 483, 05405-000 São Paulo/SP Brasil, Tel.: (55 11) 3068-9855, Fax: (55 11) 3079-6769 - São Paulo - SP - Brazil
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