Cochlear synaptopathy and hidden hearing loss: a scoping review

Colla, Marina de Figueiredo; Lunardelo, Pamela Papile; Dias, Fernanda Abalen Martins

doi:10.1590/2317-1782/20232023032pt

Tabla de contenido Anterior Actual Siguiente

Tabla de contenido

Critical Review or Scoping Review • CoDAS 36 (2) • 2024 • https://doi.org/10.1590/2317-1782/20232023032en linkcopy

Cochlear synaptopathy and hidden hearing loss: a scoping review

Authorship SCIMAGO INSTITUTIONS RANKINGS

Purpose To identify the pathophysiological definitions adopted by studies investigating “cochlear synaptopathy” (CS) and “hidden hearing loss” (HHL).

Research strategies The combination of keywords “Auditory Synaptopathy” or “Neuronal Synaptopathy” or “Hidden Hearing Loss” with “etiology” or “causality” or “diagnosis” was used in the databases EMBASE, Pubmed (MEDLINE), CINAHL (EBSCO), and Web of Science.

Selection criteria Studies that investigated CS or HHL in humans using behavioral and/or electrophysiological procedures were included.

Data analysis Data analysis and extraction were performed with regard to terminology, definitions, and population.

Results 49 articles were included. Of these, 61.2% used the CS terminology, 34.7% used both terms, and 4.1% used HHL. The most-studied conditions were exposure to noise and tinnitus.

Conclusion CS terminology was used in most studies, referring to the pathophysiological process of deafferentiation between the cochlear nerve fibers and inner hair cells.

Keywords:
Hearing; Hidden Hearing Loss; Cochlear Synaptopathy; Terminology; Review

	Author (Year)	Type of study	Terminology adopted population studied	Definition
1	Schaette et al.(³) -2011	Control case	● HHL	“Deafferentiation after noise damage predominantly affects high-threshold NA fibers, while a sufficient number of low-threshold fibers remain responsive to sound.”
1	Schaette et al.(³) -2011	Control case	● Tinnitus
2	Mehraei et al.(²⁷) -2016	Cross-sectional observational	● CS and HHL - synonyms	“Loss of synapses and cochlear nerve terminals that innervate the IHCs.”
2	Mehraei et al.(²⁷) -2016	Cross-sectional observational	● Healthy
3	Bramhall et al.(¹⁹) -2017	Control case	● CS	“Partial loss of IHC synapses of auditory nerve fibers.”
3	Bramhall et al.(¹⁹) -2017	Control case	● Noise exposure	“Partial loss of IHC synapses of auditory nerve fibers.”
4	Prendergast et al.(²⁸) -2017	Cross-sectional observational	● CS and HHL - synonyms	“CS promoted by exposure to noise (often referred to as “HHL”) was demonstrated in a mouse by Kujawa and Liberman (2009).”
4	Prendergast et al.(²⁸) -2017	Cross-sectional observational	● Noise exposure
5	Grin et al.(²⁹) -2017	Control case	● CS and HHL - synonyms	“A synaptopathic lesion that affects the FMTE, which have higher response thresholds and are responsible for encoding higher-intensity sounds.”
5	Grin et al.(²⁹) -2017	Control case	● Noise exposure
6	Paul et al.(²¹) -2017	Control case	● CS and HHL - synonyms	“AN fiber damage that does not alter auditory thresholds.”
6	Paul et al.(²¹) -2017	Control case	● Tinnitus	“AN fiber damage that does not alter auditory thresholds.”
7	Wojtczak et al.(³⁰) -2017	Control case	● CS	“Diffuse and permanent loss between IHC and AN synaptic connections after exposure to high-intensity noise, without measurable permanent changes in cochlear function or auditory sensitivity.”
7	Wojtczak et al.(³⁰) -2017	Control case	● Tinnitus
8	Shim et al.(³¹) -2017	Control case	● CS and HHL - cause/symptom	“”HHL” is characterized as damage to the AS that is not sufficient to produce a threshold shift,the AS partially recovers as thresholds are restored, despite residual physical damage. Selective loss of high-threshold AN or CS fibers may occur without auditory threshold switching due to intact low-threshold fibers.”
8	Shim et al.(³¹) -2017	Control case	● Tinnitus
9	Paul et al.(²²) -2017	Cross-sectional observational	● CS	“Damage of the cochlear synapses necessary for supraliminal abilities, even when the cochlear structures necessary for threshold hearing remain unaffected.”
9	Paul et al.(²²) -2017	Cross-sectional observational	● Noise exposure
10	Grose et al.(⁴) -2017	Control case	● CS	“Suprathreshold deficits in the presence of hearing thresholds within normal limits. In which there is synaptic disruption between the IHC and primary auditory neurons.”
10	Grose et al.(⁴) -2017	Control case	● Noise exposure
11	Guest et al.(⁵), -2017	Control case	● CS	“Preferential loss of AN fibers with low spontaneous firing rate and high threshold.”
11	Guest et al.(⁵), -2017	Control case	● Tinnitus
12	Prendergast et al.(³²) -2017	Cross-sectional observational	● CS	“Loss of synapses between IHC and AN fibers.”
12	Prendergast et al.(³²) -2017	Cross-sectional observational	● Noise exposure	“Loss of synapses between IHC and AN fibers.”
13	Valderrama et al.(³³) -2018	Cross-sectional observational	● CS and HHL - synonyms	“Theory known as “HHL”, in which CS in humans is the hypothesis to explain speech intelligibility deficits in the presence of normal audiogram.”
13	Valderrama et al.(³³) -2018	Cross-sectional observational	● Noise exposure
14	Guest et al.(³⁴) -2018	Cross-sectional observational	● CS	“Loss of synapses between the IHC and the AN fibers, which can occur without cell loss or permanent threshold elevation.”
14	Guest et al.(³⁴) -2018	Cross-sectional observational	● Speech comprehension difficulty
15	Bramhall et al.(⁶) -2018	Control case	● CS	“Selective damage to the afferent auditory nerve synapses in the IHC, with auditory thresholds within normal limits.”
15	Bramhall et al.(⁶) -2018	Control case	● Noise exposure
16	Guest et al.(³⁵) -2019	Cross-sectional observational	● CS	“Loss of synapses between IHC and AN fibers.”
16	Guest et al.(³⁵) -2019	Cross-sectional observational	● Tinnitus	“Loss of synapses between IHC and AN fibers.”
17	Ridley et al.(³⁶) -2019	Control case	● CS and HHL - cause/symptom	“Damage AN's FBTE and FMTE, which are involved in processing moderate to loud sounds, and are more resistant to masking by background noise. A possible cause for HHL is CS.”
17	Ridley et al.(³⁶) -2019	Control case	● SNHL
18	Grose et al.(¹²) -2019	Cross-sectional observational	● CS	“Permanent damage to the synapses between the IHC and the AN fibers, insufficient to result in a permanent elevation of auditory thresholds.”
18	Grose et al.(¹²) -2019	Cross-sectional observational	● Aging
19	Bhatt & Wang(³⁷) -2019	Control case	● CS	“Irreversible damage to the synaptic connections between the IHC and AN. This noise-induced CS cannot be detected by assessing hearing thresholds because noise exposure does not always cause IHC or EHC loss.”
19	Bhatt & Wang(³⁷) -2019	Control case	● Noise exposure
20	Johannesen et al.(³⁸) -2019	Cross-sectional observational	● CS	“Animal studies have shown that the number of AN fibers decreases with increasing age in healthy cochleae. Some authors speculate that CS and/or deafferentation may be responsible for difficulties in understanding speech in the elderly.”
20	Johannesen et al.(³⁸) -2019	Cross-sectional observational	● Healthy
21	Risato-Lago et al.(³⁹) -2019	Control case	● HHL	“Condition in which AS damage does not produce threshold change or there is partial recovery as thresholds are restored to original levels despite residual physical damage.”
21	Risato-Lago et al.(³⁹) -2019	Control case	● Sickle cell anemia
22	Guest et al.(¹⁸) -2019	Control case	● CS	“Loss of synapses between cochlear IHC and AN fibers, without generalized loss of hair cells.”
22	Guest et al.(¹⁸) -2019	Control case	● Healthy
23	Prendergast et al.(⁴⁰) -2019	Cross-sectional observational	● CS	“Kujawa and Liberman(¹) described the phenomenon now known as CS (…) loss of synapses with unchanged absolute thresholds, but associated with a reduction in Wave I..”
23	Prendergast et al.(⁴⁰) -2019	Cross-sectional observational	● Noise exposure
24	Megha et al.(⁴¹) -2019	Control case	● CS and HHL - synonyms	“Temporary change in the threshold, with damage to the connections between the fibers of the AN and the IHC of the cochlea, causing CS. This type of damage to the synapse, which does not permanently raise the threshold, is called HHL.”
24	Megha et al.(⁴¹) -2019	Control case	● Noise exposure
25	Keshishzadeh et al.(⁴²) -2020	Control case	● CS	“Irreversible loss of AN synapses and degeneration of cochlear neurons, without damage to cochlear sensory hair cells.”
25	Keshishzadeh et al.(⁴²) -2020	Control case	● Speech comprehension difficulty
26	Mepani et al.(⁴³) -2020	Cross-sectional observational	● CS	“It is “hidden” because neural degeneration per se does not raise behavioral thresholds or electrophysiological thresholds until it becomes extreme.”
26	Mepani et al.(⁴³) -2020	Cross-sectional observational	● Healthy
27	Couth et al.(⁴⁴) -2020	Control case	● CS and HHL - synonyms	“Loss of synapses between IHC and spiral ganglion neurons.”
27	Couth et al.(⁴⁴) -2020	Control case	● Noise exposure	“Loss of synapses between IHC and spiral ganglion neurons.”
28	Parker et al.(¹⁰) -2020	Cross-sectional observational	● CS and HHL - cause/symptom	“Loss of the synaptic connection between the IHC and the AN fibers, impairing the ability to understand in adverse listening situations.”
28	Parker et al.(¹⁰) -2020	Cross-sectional observational	● Healthy
29	Grant et al.(⁹) -2020	Cross-sectional observational	● CS	“Damage of synapses between cochlear and IHC nerve fibers even as hair cells and thresholds recover.”
29	Grant et al.(⁹) -2020	Cross-sectional observational	● Healthy
30	Kara et al.(⁴⁵) -2020	Control case	● CS and HHL - synonyms	“Loss of IHC synapses without any evidence of increased auditory thresholds.”
30	Kara et al.(⁴⁵) -2020	Control case	● Tinnitus
31	Bramhall et al.(⁸) -2020	Control case	● CS	“Loss of synaptic connections between the IHC and their auditory afferent nerve fiber targets.”
31	Bramhall et al.(⁸) -2020	Control case	● Tinnitus and noise exposure
32	Shehorn et al.(⁴⁶) -2020	Control case	● CS	“Loss of connections between the IHC and the auditory nerve fibers, in the absence of permanent threshold change.”
32	Shehorn et al.(⁴⁶) -2020	Control case	● Speech comprehension difficulty
33	Okada et al.(⁴⁷), -2020	Cross-sectional observational	● CS	“Reduced cochlear efferent innervation and a loss of afferent synapses between the AN and sensory cells.”
33	Okada et al.(⁴⁷), -2020	Cross-sectional observational	● CHL
34	Washnik et al.(⁴⁸) -2020	Control case	● CS and HHL - synonyms	“Irreversible damage to the synaptic connections between the cochlear IHC and the NA fibers. This type of peripheral hearing loss can lead to impaired speech perception and has been called “HHL”.
34	Washnik et al.(⁴⁸) -2020	Control case	● Noise exposure
35	Carcagno & Plack(⁴⁹) -2020	Cross-sectional observational	● CS	“Permanent loss of synapses between IHC and AN fibers.”
35	Carcagno & Plack(⁴⁹) -2020	Cross-sectional observational	● Aging	“Permanent loss of synapses between IHC and AN fibers.”
36	Marmel et al.(⁵⁰) -2020	Control case	● CS and HHL - synonyms	“Subclinical auditory pathology that could explain some hearing difficulties observed despite (almost) normal audiometric thresholds.”
36	Marmel et al.(⁵⁰) -2020	Control case	● Tinnitus
37	Carcagno & Plack(⁵¹) -2021	Cross-sectional observational	● CS	“Permanent loss of synapses between IHC and AN fibers.”
37	Carcagno & Plack(⁵¹) -2021	Cross-sectional observational	● Aging	“Permanent loss of synapses between IHC and AN fibers.”
38	Shim et al.(⁵²) -2021	Control case	● CS	“The selective loss of high-threshold fibers and/or high-threshold synaptopathy.”
38	Shim et al.(⁵²) -2021	Control case	● Unilateral tinnitus
39	Bal et al.(¹¹) -2021	Control case	● CS and HHL - synonyms	“Damage to cochlear nerve fibers, especially in the FBTE, with disruption of synaptic communication between the sensory IHC and cochlear nerve fiber subsets.”
39	Bal et al.(¹¹) -2021	Control case	● Noise exposure
40	Suresh et al.(²⁰) -2021	Control case	● CS and HHL - cause/symptom	“Reduction in the number of synaptic strands between the IHC and the AN fibers without affecting the audiometric thresholds.”
40	Suresh et al.(²⁰) -2021	Control case	● Noise exposure
41	Nam et al.(⁵³) -2021	Control case	● CS and HHL - synonyms	“When synapses are damaged, nerve fibers subsequently degenerate.”
41	Nam et al.(⁵³) -2021	Control case	● Noise exposure
42	Megha et al.(¹³) -2021	Control case	● SC and HHL - synonyms	“Loss of synapses and cochlear nerve endings that innervate the IHC.”
42	Megha et al.(¹³) -2021	Control case	● Noise exposure and aging
43	Wang et al.(⁷) -2021	Cross-sectional observational	● CS	“Permanent dysfunction at the junctions between the IHC and the AN fibers caused by low-grade trauma to the inner ear, typically associated with noise exposure, insufficient for permanent elevation of thresholds.”
43	Wang et al.(⁷) -2021	Cross-sectional observational	● Noise exposure
44	Vasilkov et al.(⁵⁴) -2021	Control case	● CS	“Degeneration of the synaptic terminals of spiral ganglion cells, which precedes IHC damage in the aging process.”
44	Vasilkov et al.(⁵⁴) -2021	Control case	● Aging
45	Bramhall et al.(²³) -2021	Control case	● CS	“Loss of connection between the IHI and their afferent AN fiber targets.”
45	Bramhall et al.(²³) -2021	Control case	● Noise exposure
46	Chen et al.(⁵⁵) -2021	Cross-sectional observational	● CS	“Affects the connection between the IHCs, with dysfunction in the FBTE, reducing the ability to perceive speech in a noisy environment.”
46	Chen et al.(⁵⁵) -2021	Cross-sectional observational	● Aging
47	Edvall et al.(⁵⁶) -2022	Control case	● CS	“Loss of synaptic connection between the IHC and the afferent fibers of the AN.”
47	Edvall et al.(⁵⁶) -2022	Control case	● Tinnitus
48	Turner et al.(⁵⁷) -2022	Control case	● CS	“Synaptic change between the IHC and the auditory nerve fibers.”
48	Turner et al.(⁵⁷) -2022	Control case	● Tinnitus
49	Bramhall et al.(²⁴) -2022	Control case	● CS	“Loss of synapses between the IHC and afferent auditory nerve fibers.”
49	Bramhall et al.(²⁴) -2022	Control case	● Noise exposure

location_on

Sociedade Brasileira de Fonoaudiologia Al. Jaú, 684, 7º andar, 01420-002 São Paulo - SP Brasil, Tel./Fax 55 11 - 3873-4211 - São Paulo - SP - Brazil
E-mail: revista@codas.org.br

rss_feed Acompañe los números de esta revista en su lector de RSS

[1] Caption: CS = Cochlear synaptopathy; HHL = Hidden Hearing Loss; AN = Auditory Nerve; IHC = Inner Hair Cell; FMTE = Medium Rate Spontaneous Fibers; FBTE = Low Rate Spontaneous Fibers; AS = Auditory System; EHC = External Hair Cell; . SNHL = Sensorineural Hearing Loss; CHL = Conductive Hearing Loss