Effectiveness of Auditory Measures for Detecting Hidden Hearing Loss and/or Cochlear Synaptopathy: A Systematic Review

Christi M. Barbee; Jessica A. James; Jin Hyung Park; Emily M. Smith; Carole E. Johnson; Shari Clifton; Jeffrey L. Danhauer

doi:10.1055/s-0038-1641743

Seminars in Hearing, Table of Contents

Semin Hear 2018; 39(02): 172-209
DOI: 10.1055/s-0038-1641743

Review Article

Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Effectiveness of Auditory Measures for Detecting Hidden Hearing Loss and/or Cochlear Synaptopathy: A Systematic Review

Authors

Christi M. Barbee

¹Hearing Evaluation, Rehabilitation, and Outcomes Laboratory, Department of Communication Sciences and Disorders, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma
Jessica A. James

¹Hearing Evaluation, Rehabilitation, and Outcomes Laboratory, Department of Communication Sciences and Disorders, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma
Jin Hyung Park

¹Hearing Evaluation, Rehabilitation, and Outcomes Laboratory, Department of Communication Sciences and Disorders, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma
Emily M. Smith

¹Hearing Evaluation, Rehabilitation, and Outcomes Laboratory, Department of Communication Sciences and Disorders, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma
Carole E. Johnson

¹Hearing Evaluation, Rehabilitation, and Outcomes Laboratory, Department of Communication Sciences and Disorders, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma
Shari Clifton

¹Hearing Evaluation, Rehabilitation, and Outcomes Laboratory, Department of Communication Sciences and Disorders, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma
Jeffrey L. Danhauer

²Department of Speech and Hearing Sciences, University of California Santa Barbara, Santa Barbara, California

Abstract

Standard audiometric evaluations are not sensitive enough to identify hidden hearing loss (HHL) and/or cochlear synaptopathy (CS). Patients with either of these conditions frequently present with difficulty understanding speech in noise or other complaints such as tinnitus. The purpose of this systematic review is to identify articles in peer-reviewed journals that assessed the sensitivity of audiologic measures for detecting HHL and/or CS, and which showed potential for use in a clinical test battery for these disorders. A reference librarian submitted specific boolean terminology to MEDLINE, Embase, and Web of Science. The authors used a consensus approach with specially designed score sheets for the selection of titles, abstracts, and then articles for inclusion in the systematic review and for quality assessment. Fifteen articles were included in the systematic review. Seven articles involved humans; seven involved animals, and one study used both humans and animals. Results showed that pure-tone audiometry to 20 kHz, otoacoustic emissions, electrocochleography, auditory brainstem response (ABR), electrophysiological tests, speech recognition in noise with and without temporal distortion, interviews, and self-report measures have been used to assess HHL and/or CS. For HHL, ultra-high-frequency audiometry may help identify persons with sensory hair cell loss that does not show up on standard audiograms. Promising nonbehavioral measures for CS included ABR wave I amplitude, the summating potential-to-action potential ratio, and speech recognition in noise with and without temporal distortion. Self-report questionnaires also may help identify auditory dysfunction in persons with normal hearing.

Keywords

hidden hearing loss - cochlear synaptopathy - King–Kopetzky syndrome - assessment

Full Text

References

References
1 Tremblay KL, Pinto A, Fischer ME. , et al. Self-reported hearing difficulties among adults with normal audiograms: the beaver dam offspring study. Ear Hear 2015; 36 (06) e290-e299
2 Zhao F, Stephens D. A critical review of King-Kopetzky syndrome: hearing difficulties but normal hearing. Audiol Med 2007; 5 (02) 119-124
3 Hinchcliffe R, Coles RR, King PF. Occupational noise induced vestibular malfunction?. Br J Ind Med 1992; 49 (01) 63-65
4 Saunders GH, Haggard MP. The clinical assessment of obscure auditory dysfunction--1. Auditory and psychological factors. Ear Hear 1989; 10 (03) 200-208
5 Stephens S, Rendell RJ. Auditory disability with normal hearing. Quaderni de Audiologia 1998; 4: 233-238
6 Schaette R, McAlpine D. Tinnitus with a normal audiogram: physiological evidence for hidden hearing loss and computational model. J Neurosci 2011; 31 (38) 13452-13457
7 Kujawa SG, Liberman MC. Adding insult to injury: cochlear nerve degeneration after “temporary” noise-induced hearing loss. J Neurosci 2009; 29 (45) 14077-14085
8 Mulders WH, Robertson D. Hyperactivity in the auditory midbrain after acoustic trauma: dependence on cochlear activity. Neuroscience 2009; 164 (02) 733-746
9 Finlayson PG, Kaltenbach JA. Alterations in the spontaneous discharge patterns of single units in the dorsal cochlear nucleus following intense sound exposure. Hear Res 2009; 256 (1–2): 104-117
10 Maison SF, Usubuchi H, Liberman MC. Efferent feedback minimizes cochlear neuropathy from moderate noise exposure. J Neurosci 2013; 33 (13) 5542-5552
11 Fernandez KA, Jeffers PW, Lall K, Liberman MC, Kujawa SG. Aging after noise exposure: acceleration of cochlear synaptopathy in “recovered” ears. J Neurosci 2015; 35 (19) 7509-7520
12 Kujawa SG, Liberman MC. Synaptopathy in the noise-exposed and aging cochlea: Primary neural degeneration in acquired sensorineural hearing loss. Hear Res 2015; 330 (Pt B): 191-199
13 Sergeyenko Y, Lall K, Liberman MC, Kujawa SG. Age-related cochlear synaptopathy: an early-onset contributor to auditory functional decline. J Neurosci 2013; 33 (34) 13686-13694
14 Viana LM, O'Malley JT, Burgess BJ. , et al. Cochlear neuropathy in human presbycusis: Confocal analysis of hidden hearing loss in post-mortem tissue. Hear Res 2015; 327: 78-88
15 Abdala C, Dhar S. Maturation and aging of the human cochlea: a view through the DPOAE looking glass. J Assoc Res Otolaryngol 2012; 13 (03) 403-421
16 Liberman MC, Epstein MJ, Cleveland SS, Wang H, Maison SF. Toward a differential diagnosis of hidden hearing loss in humans. PLoS One 2016; 11 (09) e0162726
17 Jensen JB, Lysaght AC, Liberman MC, Qvortrup K, Stankovic KM. Immediate and delayed cochlear neuropathy after noise exposure in pubescent mice. PLoS One 2015; 10 (05) e0125160
18 Lobarinas E, Spankovich C, Le Prell CG. Evidence of “hidden hearing loss” following noise exposures that produce robust TTS and ABR wave-I amplitude reductions. Hear Res 2017; 349: 155-163
19 Mehraei G, Hickox AE, Bharadwaj HM. , et al. Auditory brainstem response latency in noise as a marker of cochlear synaptopathy. J Neurosci 2016; 36 (13) 3755-3764
20 Möhrle D, Ni K, Varakina K. , et al. Loss of auditory sensitivity from inner hair cell synaptopathy can be centrally compensated in the young but not old brain. Neurobiol Aging 2016; 44: 173-184
21 Paquette ST, Gilels F, White PM. Noise exposure modulates cochlear inner hair cell ribbon volumes, correlating with changes in auditory measures in the FVB/nJ mouse. Sci Rep 2016; 6: 25056
22 Song Q, Shen P, Li X. , et al. Coding deficits in hidden hearing loss induced by noise: the nature and impacts. Sci Rep 2016; 6: 25200
23 Bramhall NF, Konrad-Martin D, McMillan GP, Griest SE. Auditory brainstem response altered in humans with noise exposure despite normal outer hair cell function. Ear Hear 2017; 38 (01) e1-e12
24 Guest H, Munro KJ, Prendergast G, Howe S, Plack CJ. Tinnitus with a normal audiogram: relation to noise exposure but no evidence for cochlear synaptopathy. Hear Res 2017; 344: 265-274
25 Verhulst S, Jagadeesh A, Mauermann M, Ernst F. Individual differences in auditory brainstem response wave characteristics: relations to different aspects of peripheral hearing loss. Trends Hear 2016; 20: 11
26 Mehraei G, Gallardo AP, Shinn-Cunningham BG, Dau T. Auditory brainstem response latency in forward masking, a marker of sensory deficits in listeners with normal hearing thresholds. Hear Res 2017; 346: 34-44
27 Stuermer KJ, Beutner D, Foerst A, Hahn M, Lang-Roth R, Walger M. Electrocochleography in children with auditory synaptopathy/neuropathy: diagnostic findings and characteristic parameters. Int J Pediatr Otorhinolaryngol 2015; 79 (02) 139-145
28 Prendergast G, Guest H, Munro KJ. , et al. Effects of noise exposure on young adults with normal audiograms I: electrophysiology. Hear Res 2017; 344: 68-81
29 Plack CJ, Léger A, Prendergast G, Kluk K, Guest H, Munro KJ. Toward a diagnostic test for hidden hearing loss. Trends Hear 2016; 20: 7
30 Dobie RA, Clark WW. Exchange rates for intermittent and fluctuating occupational noise: a systematic review of studies of human permanent threshold shift. Ear Hear 2014; 35 (01) 86-96
31 Mehrparvar AH, Mirmohammadi SJ, Davari MH. , et al. Conventional audiometry, extended high-frequency audiometry, and DPOAE for early diagnosis of NIHL. Iran Red Crescent Med J 2014; 16 (01) e9628
32 Konrad-Martin DG, Gordon JS, Reavis KM, Wilmington DJ, Helt WJ, Fausti SA. Audiological monitoring of patients receiving ototoxic drugs. Perspec Hear Hear Dis Diagn 2005; 9 (01) 17-22
33 Henry JA, Jastreboff MM, Jastreboff PJ, Schechter MA, Fausti SA. Assessment of patients for treatment with tinnitus retraining therapy. J Am Acad Audiol 2002; 13 (10) 523-544
34 Kemp DT, Ryan S, Bray P. A guide to the effective use of otoacoustic emissions. Ear Hear 1990; 11 (02) 93-105
35 Desai A, Reed D, Cheyne A, Richards S, Prasher D. Absence of otoacoustic emissions in subjects with normal audiometric thresholds implies exposure to noise. Noise Health 1999; 1 (02) 58-65
36 Prasher D, Sułkowski W. The role of otoacoustic emissions in screening and evaluation of noise damage. Int J Occup Med Environ Health 1999; 12 (02) 183-192
37 Attias J, Horovitz G, El-Hatib N, Nageris B. Detection and clinical diagnosis of noise-induced hearing loss by otoacoustic emissions. Noise Health 2001; 3 (12) 19-31
38 Uchida Y, Ando F, Shimokata H, Sugiura S, Ueda H, Nakashima T. The effects of aging on distortion-product otoacoustic emissions in adults with normal hearing. Ear Hear 2008; 29 (02) 176-184
39 Poling GL, Siegel JH, Lee J, Lee J, Dhar S. Characteristics of the 2f(1)-f(2) distortion product otoacoustic emission in a normal hearing population. J Acoust Soc Am 2014; 135 (01) 287-299
40 Hood LJ. A review of objective methods of evaluating auditory neural pathways. Laryngoscope 1999; 109 (11) 1745-1748
41 Krause CM, Boman PA, Sillanmäki L, Varho T, Holopainen IE. Brain oscillatory EEG event-related desynchronization (ERD) and -sychronization (ERS) responses during an auditory memory task are altered in children with epilepsy. Seizure 2008; 17 (01) 1-10
42 Purcell DW, John SM, Schneider BA, Picton TW. Human temporal auditory acuity as assessed by envelope following responses. J Acoust Soc Am 2004; 116 (06) 3581-3593
43 Venail F, Artaud JP, Blanchet C, Uziel A, Mondain M. Refining the audiological assessment in children using narrow-band CE-Chirp-evoked auditory steady state responses. Int J Audiol 2015; 54 (02) 106-113
44 Cone-Wesson B, Dowell RC, Tomlin D, Rance G, Ming WJ. The auditory steady-state response: comparisons with the auditory brainstem response. J Am Acad Audiol 2002; 13 (04) 173-187 , quiz 225–226
45 Newman CW, Weinstein BE, Jacobson GP, Hug GA. The Hearing Handicap Inventory for Adults: psychometric adequacy and audiometric correlates. Ear Hear 1990; 11 (06) 430-433
46 Newman CW, Jacobson GP, Spitzer JB. Development of the Tinnitus Handicap Inventory. Arch Otolaryngol Head Neck Surg 1996; 122 (02) 143-148
47 Poulsen T. Equivalent threshold sound pressure levels (ETSPL) for Interacoustics DD 45 supra-aural audiometric earphones. Int J Audiol 2010; 49 (11) 850-855
48 Zhou X, Jen PHS, Seburn KL, Frankel WN, Zheng QY. Auditory brainstem responses in 10 inbred strains of mice. Brain Res 2006; 1091 (01) 16-26
49 Bauch CD, Olsen WO. Comparison of ABR amplitudes with TIPtrode and mastoid electrodes. Ear Hear 1990; 11 (06) 463-467