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REVIEW article

Front. Neurol., 10 July 2025

Sec. Neuro-Otology

Volume 16 - 2025 | https://doi.org/10.3389/fneur.2025.1589117

The auditory outcomes in non-blast related traumatic brain injury and the role of severity, aetiology and gender: a scoping review

  • 1Hearing Sciences, Division of Mental Health and Clinical Neuroscience, School of Medicine, University of Nottingham, Nottingham, United Kingdom
  • 2National Institute of Health and Social Research (NIHR) Nottingham Biomedical Research Centre, Nottingham, United Kingdom
  • 3Division of Rehabilitation Medicine, University Hospitals of Derby and Burton NHS Foundation Trust, Derby, United Kingdom
  • 4Centre for Rehabilitation and Ageing Research, School of Medicine, University of Nottingham, Nottingham, United Kingdom
  • 5Lifespan and Population Health, School of Medicine, University of Nottingham, Nottingham, United Kingdom

Introduction: Traumatic brain injury (TBI) can cause a wide range of auditory outcomes. This review aimed to investigate common auditory outcomes associated with TBI and explore variations based on severity, aetiology, and gender.

Methods: A scoping review was conducted using an established methodological framework, which involved electronic and manual searches of databases and journals. Records published in English were included, which focused on auditory outcomes and assessments associated with non-blast related TBI in individuals 18 years and older. From 19,031 records, 61 met the inclusion criteria. Data were collated and categorized based on the study objectives.

Results: Pure-tone audiometry (56/61) was the most commonly used hearing assessment, followed by otoscopy (27/61), whilst for tinnitus and hyperacusis assessments varied from questionnaires to self-reported problems. Different types of hearing loss were reported; conductive to mixed, of these 41% noted sensorineural hearing loss (SNHL). Normal hearing (≤ 20/25 dB HL) was reported in 31% (19/61) of the studies, however, five studies found abnormal results in central auditory tests despite normal hearing. Severe TBI was reported more frequently compared to other severities (10/23). Although SNHL was noted in 4 studies related to severe TBI, various outcomes were observed ranging from normal hearing to total deafness. Motor-vehicle accidents (MVA) were the most common aetiology (36/61), followed by falls, assaults, and sports injuries. Following MVA, SNHL was observed in 12 studies and CHL was observed across 10 studies. Out of 61 articles, 53% included only male patients, and SNHL was observed more frequently in males (17/33), whilst normal hearing and other types of hearing loss were noted in both genders.

Conclusion: TBI-related auditory impairments are complex, with inconsistent assessment methods and reporting gaps complicating data synthesis. Standardized clinical practices and screening guidelines are crucial for improving auditory assessment and management in this population.

1 Introduction

Traumatic brain injury (TBI), specified as a traumatic structural injury and/or physiological deterioration of brain functions caused by an external force (1), can result in many physical, cognitive, behavioral and emotional impairments (24). TBI is estimated to affect 64–74 million people worldwide each year (5). There are different ways of classifying the severity of TBI; most commonly, the Glasgow Coma Scale (GCS) at the time of injury and duration of post-traumatic amnesia are used to classify TBI as mild, moderate or severe (6). The most common type of TBI is “mild” (GCS 13–15; post-traumatic amnesia duration <24 h; loss of consciousness <30 min) with males aged 18–65 years being at highest risk of experiencing TBI (7). There is a range of causes associated with TBI, including falls, traffic accidents, assaults, sports injuries (non-blast related) and explosions (blast-related). While there will be some similarities in the way the brain is affected by each aetiology, blast-related TBI has consistently been recognized to have some particular mechanisms- e.g., typically involves the transmission of high-pressure waves through air and/or fluid-filled spaces, which can cause widespread damage to the brain and inner ear by disrupting vascular structures, neuronal tissue, and the blood–brain barrier (8, 9). In contrast, non-blast related TBI generally results from mechanical forces such as direct impact or acceleration-deceleration forces, and may lead to more focal injuries including contusions, diffuse axonal injury and blood–brain barrier disruption (10). While both mechanisms can affect similar structures, the pattern and distribution of the resulting injuries may differ. Blast-related TBI is also more likely to be seen in a military population, which may differ from the civilian population in a range of characteristics. Given the various injury patterns and population characteristics, this review focuses specifically on non-blast related TBI, as it more accurately reflects the injuries encountered in civilian life and may offer a clearer framework for understanding auditory outcomes.

Auditory conditions (such as hearing loss, tinnitus (ringing in the ear), hyperacusis (sound sensitivity)) can be observed in patients with TBI due to impairments or damage to the central and peripheral auditory systems (11, 12). Characteristically, auditory conditions occur directly in fractures or damages in the temporal bone region. For instance, sensorineural hearing loss (SNHL) is in general associated with transverse fractures, whilst conductive hearing loss (CHL) is associated with longitudinal fractures (13). In a nationwide population-based study in Taiwan, individuals with TBI were found to have a 2.125 times higher risk of developing hearing loss (14). Moreover, in a study investigating trauma-related tinnitus, 1.7% of 1,604 patients reporting experiencing tinnitus due to head trauma (12).

Although there are studies assessing auditory functions related to TBI, there is currently no comprehensive review synthesising common auditory findings related to non-blast related TBI, in particular aetiology and severity of TBI related to auditory conditions. Addressing this gap in the knowledge will provide evidence to clarify the diagnosis and treatment methods, to help establish appropriate management strategies for auditory conditions in this patient group, and in turn reduce the negative effects of these comorbidities caused by TBI.

Specifically, the objectives here are to identify:

• What are the common auditory impairments of non-blast related TBI,

• Whether auditory outcomes vary according to severity of non-blast related TBI,

• Whether auditory outcomes vary according to aetiology of non-blast related TBI,

• Whether auditory outcomes vary by gender following non-blast related TBI.

• For this purpose, a scoping review was determined to be the most appropriate method, as it is specifically designed to explore broad and diverse research questions, map the literature, summarize the findings, and synthesize the evidence obtained from a range of study designs (15, 16).

2 Materials and methods

The methodology of this scoping review was conducted in accordance with the 6-stages framework developed by Arksey and O’Malley (15): (1) identifying the research question(s), (2) identifying relevant studies using appropriate keywords, (3) selecting relevant studies through iterative scanning of titles, abstracts, and full-texts, (4) extraction and charting the data, (5) collating, summarising and reporting of the results, (6) clinician review. The review is reported following the PRISMA-S guidelines (17) (see Supplementary Appendix Table 1).

2.1 Identifying the research question(s)

For this purpose, research questions (listed above) were developed in consensus with the team members based on existing knowledge of the field and literature.

2.2 Identifying relevant studies

2.2.1 Eligibility criteria

Records were included if they reported studies/cases in which adults (≥18 years old) reported experiencing non-blast related TBI with associated hearing impairments, and hearing outcomes and assessment were reported (including self-reported auditory outcomes). Records were eligible if they reported symptoms or assessments pre-treatment and originated from cohort studies, case series, and case studies, as well as grey literature sources, particularly dissertations and theses. All included records were published in the English language and have full-text. Cases that did not meet our inclusion criteria were removed from the case series studies.

Records were excluded if the studies were reporting adults who may have experienced blast-related TBI, TBI in childhood, whiplash injuries, or non-TBI conditions (e.g., strokes, acoustic neuroma) or they did not clearly define TBI or provide evidence of structural injury or functional deterioration due to TBI. Records involving participants with pre-existing audiological impairments before the TBI, where the aetiology of TBI was not reported, and/or records whose primary aim was to determine the reliability and validity of tests were excluded. Review articles (including systematic reviews), book chapters, randomized control trials, qualitative research studies and any sources reporting personal/expert opinions were excluded.

2.2.2 Search strategy

The research strategy was developed by the research team and was supported by a medical information specialist (Dr Farhad Shokraneh). The search was conducted following Cochrane Handbook (18) and Cochrane’s MECIR (19) and PRESS guideline for peer-reviewing the search strategies (20). Electronic databases were searched including Embase, MEDLINE, ProQuest Dissertations & Theses A&I, PsycINFO, Science Citation Index Expanded and SPORTDiscus in May 2022. The search strategy included keywords on TBI, auditory and vestibular conditions (a separate review was conducted for vestibular outcomes). These were reviewed and revised following a primary search (see Supplementary Appendix Table 2 for search strategy). Specific search term strategies were applied in each search engine, searching article topics, titles, abstracts, and keywords. Filters were applied to retrieve articles in the English language and human participant studies only, when possible. There was no restriction in the search period. To seek further eligible documents for inclusion, manual searches of the reference lists and most common journals (determined using the interquartile rule for outliers) in which eligible records had been sourced were conducted. The final database and manual searches were conducted in September 2024.

2.3 Study selection

Records identified through electronic databases were exported with citation, title and abstract into EndNote (version X9), where duplicates were removed, before records were imported into Rayyan (21) for screening. Records were independently screened by four researchers (KB, OP, LE, KF), starting with the title and abstract, before moving onto the full text. Lead researcher (KB) screened all records. The records obtained as a result of the manual search were subjected to full-text screening. When disagreements arose regarding the inclusion or exclusion of any given record, the reviewers discussed their reasons until agreement was reached or a third reviewer was consulted to reach a majority decision.

2.4 Extraction and charting of the data

A data extraction form was developed in Microsoft Excel and piloted on five included records and was subsequently modified following team discussions. Data from each record were extracted by lead researcher (KB) and checked by KF. Data were extracted on study characteristics, study population, TBI characteristics, audiological complaints and assessments/outcomes, and limitations (Box 1).

Box 1. Data extraction fields

Authors

Year of publication

Country where study was conducted

Study Title

Aim of Study

Study Design

Study Population

Sample Size

Age

Gender

Classification method for TBI

Severity of TBI

Causes/ateiology of TBI

Status pre/post-TBI

Presence of coma

Radiological results

List of auditory complaints

List of audiological assesment tools

Audiological outcomes

Assesment time since injury

Single or repeated assessments

Study limitations

2.5 Collating, summarising and reporting results

Extracted data were collated and categorized based on the objectives of our research. Similar findings were grouped into categories such as auditory outcomes, severity of TBI, aetiology, and gender effects. Data were then summarized to identify common patterns and significant variations in auditory outcomes.

2.6 Clinician review

After the categories were identified, categorized outcomes were also examined by clinician LE.

3 Results

Figure 1 illustrates the process of record identification and selection. Electronic searches resulted in an initial set of 19.019 records. Duplicates were removed and of the remaining 12.424 records, 11.901 were excluded because the title and abstract indicated that the articles did not meet the eligibility criteria. Manual searches identified a further 12 potential articles which were subjected to full-text screening. Of the remaining 535 records, 474 records were excluded at the full-text screening. Most commonly the studies excluded did not report TBI or clearly define TBI, included participants under 18 years old and did not report TBI aetiology. Full-text records could not be located for 31 records. None of these records could be traced, regardless of support from the University of Nottingham librarian. The electronic and manual searches created a final list of 61 eligible full-text records for data collection.

Figure 1

Figure 1. The PRISMA flow diagram for the study selection process.

3.1 Study characteristics

Table 1 provides an overview of the study and participant characteristics. As shown by Table 1, the majority of records were reporting case reports/case series (51/61) (11, 2271) and were mainly conducted in the United States (n = 23), the United Kingdom (n = 5), Japan (n = 4), and Korea (n = 3). Articles were published from 1956 to 2023.

Table 1
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Table 1. Characteristics of included studies.

3.2 Participant characteristics

Across 61 records, 507 participants were included. Of these, 396 were in the patient group, whilst for four studies, 111 participants were in the control groups (either without TBI or without both TBI and auditory symptoms) (7275). Pre-TBI health status of participants was not reported consistently across studies (Table 1). Assessment time since injury varied widely across studies (Table 1). In 39 studies, follow-up/s’ assessments were performed after the initial time of injury before any treatment was offered (2227, 30, 3240, 4244, 4651, 5355, 57, 58, 6365, 6771, 76).

3.3 Overview of auditory impairments following non-blast related TBI

Many different symptoms such as hearing loss, tinnitus, and hyperacusis were reported across the studies. These symptoms were assessed using a variety of tests, including peripheral and central auditory function assessments and patient-reported outcome measurements (PROMs) which are briefly described below. A summary of these tests and PROMs are presented in Supplementary Appendix Table 3 and the results are shown in Table 2.

Table 2
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Table 2. Audiological findings of included studies.

3.3.1 Otoscopic assessment

In 27 (44%) studies, otoscopic assessment, a clinical procedure used to inspect the external auditory canal, tympanic membrane (eardrum), and middle ear (77), was conducted (11, 22, 23, 30, 3537, 39, 44, 46, 5153, 55, 56, 58, 59, 6163, 65, 67, 7073, 78). Some studies described otoscopic assessments as ENT, otologic, or clinical examinations (see Table 2). Eight studies presented clinical findings related to the tympanic membrane or external auditory canal without mentioning explicitly otoscopic assessment (e.g., intact eardrum) (25, 32, 38, 43, 54, 60, 64, 69) and 2 studies stated that otoscopy was performed, however the results were not reported (72, 73). In 18 (67%) out of the 27 records, the otoscopic assessment results or clinical findings indicated a normal eardrum (11, 22, 23, 25, 36, 37, 43, 44, 46, 53, 55, 56, 58, 63, 65, 70, 71, 78), whilst 16 (59%) studies noted at least one of the following symptoms: serous effusion, dried blood, blood, bloody otorrhea, cerebrospinal otorrhea, haemotympanum or haemorrhage (22, 30, 32, 35, 38, 39, 51, 52, 54, 5962, 64, 67, 69). These symptoms were detected in the right ear in most of studies (10/16) (22, 30, 35, 38, 39, 52, 5962).

3.3.2 Pure-tone (behavioral) audiometry (PTA)

PTA refers to the assessment of thresholds determined by the lowest intensity at which an individual responds to sound at least 50% of the time (79). PTA was the most commonly used audiological assessment method with 56 studies reporting it (11, 2243, 4567, 69, 7173, 75, 76, 78, 8082). In four case studies, it was not explicitly stated whether PTA was conducted, but hearing loss was reported (49, 76), audiometer screening was performed (33) or audiometric findings were presented (31).

Normal hearing was reported for 19 (34%) out of 56 studies. Of these 19 studies, ten reported that hearing was normal or normal group mean bilaterally post-TBI (11, 33, 38, 41, 47, 59, 72, 73, 75, 82), whilst 9 studies reported normal hearing in at least one ear or in one case (22, 23, 26, 29, 39, 51, 56, 65, 80). Of these, two studies (11, 82), provided an accepted range for normal hearing (≤ 25 dB HL). The remaining 17 studies (17/19) provided no explanation, but nine (9/17) did demonstrate normal hearing with audiogram results of patients or groups mean thresholds (≤ 20 dB HL or 25 dB HL) (22, 26, 29, 39, 41, 47, 65, 72, 73).

Based on PTA assessment, the most commonly reported type of hearing loss post-TBI (n = 25, 45%) was SNHL (22, 23, 2527, 36, 39, 42, 45, 46, 48, 50, 52, 53, 58, 6167, 78, 80, 81). Among these, twelve (12/25) were identified as severe or profound SNHL (22, 26, 36, 39, 46, 58, 6163, 65, 78, 81), with two case reports observing severe or profound SNHL in follow-up assessments (36, 46). Nine (9/25) were reported as mild or slight SNHL (22, 23, 42, 48, 64, 66, 67, 78, 81), with one case report observing mild SNHL in a follow-up assessment (67). In six studies (6/25), moderate SNHL was reported (27, 53, 63, 66, 67, 81), with one study noting this in a follow-up assessment (67). Following this, CHL (n = 12, 21%) was most reported (22, 24, 25, 30, 32, 35, 43, 44, 49, 54, 62, 64), whilst MHL (n = 7, 12.5%) was the least reported type of hearing loss (24, 26, 30, 39, 51, 60, 67). Three studies had no response to the stimulus in PTA assessment at all (37, 40, 55). In two other studies, no response was initially observed; however, SNHL was detected in the follow-up assessment before treatment (36, 46). In another study, MHL was observed in the initial PTA in left ear, however hearing worsened during follow-up, and no response was detected (39). In four studies, the type of hearing loss changed during follow-up assessments, and there were cases where hearing partially improved (22, 25, 30, 67). In ten studies, following PTA the degree (severity) of hearing loss or only hearing loss was reported, without reporting the type of hearing loss (in studies involving more than one case, at least one case) (22, 2830, 34, 50, 56, 69, 71, 76). Eight out of ten studies reported severe to total (profound) hearing loss post-TBI (22, 28, 30, 34, 50, 56, 69, 76). One study stated that four frequencies (0.5 to 4 kilohertz (kHz)) were used to determine the average of hearing loss (71), whilst seven studies have not described the classification method used to determine the degree of hearing loss (i.e., mild, moderate and/or severe hearing loss) (22, 28, 30, 34, 50, 71, 76).

3.3.3 Site-of-lesion tests

Site of lesions tests performed via audiometry are used to distinguish cochlear and retro-cochlear abnormalities (83). Four studies utilized 3 of the site-of-lesion tests (Békésy, Tone Decay and Alternate Binaural Loudness Balance (ABLB) test) (22, 28, 50, 66). Tone decay indicated findings in favor of retro-cochlear pathology in a patient with bilateral SNHL (66). Another study (50) that performed the Békésy test, reported a type I finding that indicated neither cochlear nor retro-cochlear pathology, even though the patient had bilateral SNHL. In one case study, the ABLB test showed no recruitment at low frequencies with severe hearing loss (28), whilst another study reported recruitment around 500 Hz in case 5 with SNHL in left ear (22).

3.3.4 Tuning fork (TF) test (weber and/or Rinne)

The TF test is used for screening and determining the type of hearing loss, confirming PTA results (84, 85). Nine studies used the Rinne and/or Weber TF tests (22, 34, 39, 40, 46, 6466, 70). In eight studies, the TF test results were consistent with the PTA results as seen in Table 2 (22, 34, 39, 40, 46, 6466), whilst the remaining study did not perform PTA (70).

3.3.5 Impedance audiometry (tympanometry and acoustic reflex thresholds)

Tympanometry objectively evaluates middle ear function (86, 87). The acoustic reflex thresholds (ART) assess auditory pathway integrity up to the superior olivary complex (SOC) via stapedius muscle reflex (88). In ten studies, both tympanometry and ART measurements were performed (11, 34, 37, 40, 43, 50, 54, 57, 67, 71), in eight only tympanometry was performed (36, 46, 55, 64, 66, 72, 73, 78) and in one study only ART measurement was conducted (39). Of the 18 studies (18/61) that performed tympanometry, normal (Type A) results were obtained from 12 (11, 34, 36, 37, 40, 46, 50, 55, 57, 71, 73, 78). The details of ART results performed ipsilaterally and/or contralaterally are presented in Table 2.

3.3.6 Basic and advanced speech audiometry

Speech audiometry examines the ability to process speech in auditory centres, starting from the outer ear and ending with the cortex, using speech signals. Of 61 included records, both basic (e.g., speech reception threshold, speech discrimination score) and advanced (e.g., speech-in-noise tests) tests were performed in 2 (3%) studies (11, 73), while basic speech audiometry test(s) were performed in 13 (21%) studies (26, 32, 37, 39, 47, 50, 53, 56, 57, 63, 66, 71, 78), including six studies using Speech Discrimination Score (SDS) (26, 32, 50, 57, 66, 71), four using Speech Reception Threshold (11, 37, 53, 73) and four using Speech Recognition Threshold (11, 32, 47, 73). The results of the tests varied depending on the patients or cases, from normal to no response at all (Table 2). A common result was not identified. Studies with follow-up assessments reported improvement in SDS results over time for one case with bilateral mild to moderate hearing loss (71), whilst another reporting worsening of SDS in one case with bilateral SNHL (50). More advanced, QuickSIN test was used in two studies (11, 73), Words-in-Noise (WIN) test was used in one of those studies (73). In both studies, although the average hearing was normal post-TBI, mild signal-to-noise-ratio (SNR) loss or an abnormal result in at least one ear was observed in the QuickSIN results. Similarly, in the WIN test, abnormal results were reported in at least one ear across 8 participants (73).

3.3.7 Otoacoustic emissions (OAEs) and suppression test

OAEs provide an objective assessment of the functionality of the outer hair cells in the cochlea (89). Only 6 (10%) studies out of the 61 records used OAEs. In 2 studies, both Distortion Product OAE (DPOAE) and Transient Evoked OAE (TEOAE) measurements were employed (37, 71), in three DPOAE was measured (47, 50, 66), and one study measured TEOAE (72). In studies where only DPOAE was performed, the DPOAE was obtained in normal hearing (47), whilst it was absent or very poor in cases of SNHL (50, 66), consistent with the hearing conditions of patients. In one case study, bilateral responses were observed in both TEOAE and DPOAE (up to 3 kHz or 4 kHz) in a patient with mild hearing loss (71), whilst another case study observed bilateral responses of TEOAE and DPOAE (only absent at 2 kHz) despite no response being obtained in either PTA or the ipsi-contralateral ART (37). In a study comparing a control group to a TBI group with/without auditory complaints (e.g., tinnitus, difficulty of hearing in noise, hyperacusis), where hearing was within normal limits in all groups, it was observed that the TEOAE amplitudes of the entire TBI group were lower than those of the control group. However, the amplitudes of the TBI group with auditory complaints were higher than those without auditory complaints (72). In one study, an OAEs suppression test referred to as medial olivocochlear suppression effect (MOSE) test, which allows for the evaluation of the efferent system (90), indicated that an absent effect of the auditory efferent system in one or both ears of the TBI patients with auditory complaints (72).

3.3.8 Electrophysiological tests

Electrophysiological tests performed with auditory potentials enable the evaluation of the auditory pathway from the auditory nerve to more central regions in the brain (91). Out of the 61 records, 16 (26%) studies used electrophysiological tests, with 15 studies using Auditory Brainstem Response (ABR/BAEP) (15/16) (34, 36, 37, 40, 41, 46, 47, 50, 53, 55, 58, 66, 68, 71, 80), one study using electrocochleography (ECOG) (38) and five using additional tests, including middle latency responses (MLR/MLAEPs) (41, 47), late latency responses (LLR) (66, 71), and mismatch negativity (MMN) and P300 (66).

Out of the 15 studies, 13 showed that ABR findings were consistent with PTA results (34, 36, 37, 41, 46, 47, 50, 53, 55, 58, 66, 71, 80). For instance, in cases of bilateral profound SNHL, either bilateral unobtainable ABRs were observed (58) or, depending on the degree of hearing loss, waves I and III were obtained, but no peak in wave V was observed (66). In cases with normal hearing normal ABR results (47), or prolonged latency in wave V were obtained (41). However, in one of these studies, ABR, PTA and ART results were not obtained consistently, whilst results of OAEs were present (37) (refer to the OAEs section). In one study, ABR results were in a normal waveform and no response was obtained in PTA, whilst ART results were present bilaterally (40). Another study by Shibata (68) reported cortical deafness due to delayed traumatic intracerebral haematoma using Magnetic Resonance Imaging (MRI), but 1 month later a normal response was observed in the ABR performed (68). Furthermore, in two case studies (50, 71), improvement in ABR results in follow-up assessments corresponded to improvement in the degree of hearing loss obtained in PTA (71), whilst deterioration in ABR results corresponded to worsening in the degree of hearing loss (50). The details of other electrophysiological test results are presented in Table 2.

3.3.9 Central auditory tests

Central auditory system assessments facilitate the evaluation of auditory processes such as the processing, interpretation, and discrimination, enabling the assessment of the central levels of the auditory pathway (92). Out of 61 records, 5 (8%) studies performed various central auditory tests (11, 33, 41, 47, 73), despite normal hearing reported in PTA, abnormal results were observed in at least one central auditory test (Table 2). The age of participants in these studies ranged from 22 to 71 years.

3.3.10 PROMs

PROMs (93) were used in 8 (13%) out of the 61 studies (11, 57, 71, 73, 74, 76, 82, 94) for assessment of hearing (11, 71, 73, 74, 82), tinnitus (57, 71, 74, 76, 82) and hyperacusis (11, 74, 82). PROMs used include Hearing Handicap Inventory for Adults (HHI-A) (11, 71, 74, 82), the speech spatial and qualities of hearing scale (73), the screening checklist for Auditory Processing in Adults (71), Tinnitus Handicap Inventory (THI) (71, 74, 82), a Likert scale for tinnitus amplitude (76), the Tinnitus Questionnaire (TQ) and numeric rating scale (NRS) for loudness, discomfort, annoyance, ignorability, and unpleasantness (57) and Hyperacusis Questionnaire (HQ) (11, 74, 82) were performed. In one study, the post-concussion symptom scale (PCSS) was used (94). In most studies (5/8), more than one PROM was used (11, 57, 71, 74, 82).

Hearing impairment was observed in all studies in which HHI-A was reported (11, 71, 74, 82). In particular, although normal hearing was detected in PTA in two studies, mild to severe (82) or substantial impairment (11) was observed because of HHI-A. Similarly, for the 16 (26%) studies reporting complaints of tinnitus (11, 24, 26, 2830, 39, 47, 51, 57, 59, 61, 71, 72, 76, 78), in the 3 studies using THI a range from slight to catastrophic score was reported (71, 74, 82). In the case study where TQ and NRS were used (57), the tinnitus severity grade was reported as extreme, and the patient considered tinnitus to be a very big problem in the NRS. Furthermore, tinnitus was reported to worsen from the time of TBI to initial consultation. Three (5%) studies reported complaints of hyperacusis (11, 60, 72), out of which 2 studies found that hyperacusis was the most reported symptom among individuals with TBI using HQ. Both studies reported significant sensitivity based on HQ results (74, 82). In the case study where HQ was used, the patient found all sounds too loud and reported substantial impairment (11). Hyperacusis was also reported in the study using PCSS (94). Detailed results of other PROMs are presented in Table 2.

3.4 Effect of severity of non-blast related TBI on auditory outcomes

The majority of studies have not clearly stated the severity of TBI (38/61) (2230, 35, 36, 3845, 48, 5056, 6062, 6570, 76, 81). Of the remaining, 10 studies included severe TBI (24, 30, 33, 37, 46, 57, 58, 64, 71, 80), 6 included mild TBI (11, 47, 63, 73, 74, 78), 7 studies reported concussion (i.e., mild TBI) (29, 31, 32, 59, 75, 81, 94), 2 observed moderate/severe TBI (34, 49) and 2 included a range from mild to severe TBI patients (72, 82) (see Table 1 more details on severity, e.g., criteria of severity).

In the 2 studies with a range of mild to severe TBI (72, 82), normal hearing (≤ 20 dB HL or 25 dB HL) was observed and tinnitus and/or hyperacusis were reported. In Knoll et al. (82), tinnitus was the commonly reported symptom in both mild-TBI and moderate–severe-TBI groups. However, the mean for THI was higher in the moderate–severe-TBI group indicating more severe score than the mild TBI group (Table 2).

In 6 studies where TBI severity was classified only as mild (11, 47, 63, 73, 74, 78), abnormal results were observed in at least one central auditory test despite normal hearing in three studies (11, 47, 73), the remaining studies did not perform central hearing tests (63, 78, 82). In one study for mild TBI, a severe hearing impairment was reported using HHI-A (74). In patients exposed to mild TBI, Jang, Bae and Seo (63) observed moderate and severe SNHL, whilst Jafarzadeh et al. (78) reported mild to profound SNHL. Tinnitus was observed in four studies involving mild TBI (11, 47, 74, 78), whilst two studies reported both hyperacusis and tinnitus (11, 74). HQ results of these studies are explained in the PROMs section earlier. In the remaining three studies (11, 47, 78), tinnitus was reported; however, no formal assessment was conducted. Notably, one of these studies, the reported tinnitus resolved a several months later (47). Also, different outcomes were observed in each of the studies reporting concussion such as normal hearing, mild CHL and profound SNHL (29, 31, 32, 59, 75, 81). Hyperacusis was observed after concussion (94), and complaint of tinnitus were reported in another study (59).

SNHL was reported in 4 out of 10 studies reporting severe TBI (46, 58, 64, 80). This group also exhibited a range of outcomes from normal hearing to total deafness as well as CHL. There were tinnitus complaints in three case studies in severe TBI (30, 57, 71). In 2 studies evaluating tinnitus in this group, catastrophic score was detected in THI for mild hearing loss (71), and extreme tinnitus severity was observed in TQ in normal hearing between 0.125–2 kHz, with a steep decline toward higher frequencies on both sides (57). Hyperacusis was not indicated in any of the studies that included only severe TBI. In four of those studies, abnormal results were observed in at least one component of ABR (e.g., wave V) at the brainstem level, despite normal hearing or varying types or degrees of hearing loss (37, 46, 58, 71). Figure 2 shows the distribution of auditory outcomes across studies according to TBI severity.

Figure 2

Figure 2. Distribution of auditory outcomes based on severity of non-blast related TBI.

In summary, the severity of TBI may not consistently predict auditory outcomes and both mild and severe TBI can result in significant auditory impairments and abnormal central auditory test results.

3.5 Effect of aetiology of non-blast related TBI on auditory outcomes

In terms of aetiology, the majority of studies (36/61) reported motor vehicle accidents (MVA) at least one participant or case (Table 1) (11, 2225, 2830, 3234, 37, 38, 40, 42, 43, 49, 53, 54, 58, 60, 6264, 66, 67, 69, 7174, 76, 8082, 94).

To examine the effect of aetiologies related to TBI, they were classified into five categories: MVA, falls, sports-related injuries, assaults, and others. In six studies involving multiple participants, different aetiologies, from MVA to assault, were included (7274, 80, 82, 94). For these studies results are reported together under all aetiologies. In one of the 6 studies (73) the group mean showed normal hearing, but a small range of hearing loss was reported in at least one ear in three participants with TBI. However, the degree classification of hearing loss was not explained (Table 2) (73). For these participants, two had an aetiology of fall, whilst one was due to MVA. In another study by Knoll et al. (74), it was observed that there was no significant difference in the presence of auditory symptoms across aetiology of the TBI. For the remaining 3 studies, two studies reported normal hearing for all participants (72, 82), whilst the other study reported SNHL for only one participant, but the aetiology was not specified (80).

Out of the 30 studies reporting MVA in case series/studies, 12 studies reported SNHL in at least one case and/or ear (22, 23, 25, 42, 53, 58, 6264, 66, 67, 81), 10 studies reported CHL (22, 24, 25, 30, 32, 43, 49, 54, 62, 64), 4 studies reported MHL (24, 30, 60, 67), although two studies reported that the type of hearing loss changed in follow-up assessments (30, 67) and 6 studies reported normal hearing in at least one case and/or ear (11, 22, 23, 29, 33, 38). However, in two of these studies, despite normal hearing, abnormal results were obtained in at least one central auditory test, leading to diagnoses of auditory attentional neglect (33) or auditory processing deficits (11). Five studies reported tinnitus complaints following MVA (11, 28, 30, 71, 76), and one case reported hyperacusis linked to MVA (60).

Across studies reporting falls (21/61) in case series/studies, SNHL was observed in 10 studies (22, 26, 36, 45, 46, 48, 50, 65, 78, 81), followed by normal hearing in 4 studies (23, 47, 51, 65), MHL across 3 studies (26, 39, 51), and CHL in one study (32) at least one ear and/or one case. In 6 studies, either hearing loss without the type was reported or a diagnosis (e.g., unilateral ossicular chain disruption) was noted (29, 31, 55, 57, 68, 70). Five studies report tinnitus complaints following falls (26, 29, 47, 51, 57), and one study reported hyperacusis (11).

Out of 7 studies reporting different types of assaults in case series/studies, normal hearing (39, 56), and all types of hearing loss [SNHL (26, 39, 61)], [CHL (30, 44)], and [MHL (24)] in at least one ear and/or one case, and tinnitus in (24, 26, 39, 61) were observed. In the 4 studies reporting sports-related TBI (35, 41, 59, 75), normal hearing or normal hearing with a brainstem auditory-processing disorder were observed across three studies (41, 59, 75), CHL was observed in one case study (35) and tinnitus was reported in one study (59). Three studies were categorised under ‘other’ aetiologies: striking the back of the head (39), industrial injury (52), and an object falling from a bookcase (27). In two of these studies, SNHL was detected (27, 52), whilst Lyos et al. (39) initially observed MHL, one week later, one ear had normal hearing, and no response was obtained in PTA in the other. Figure 3 illustrates the distribution of auditory outcomes according to the aetiology of non-blast related TBI.

Figure 3

Figure 3. Distribution of auditory outcomes based on aetiology of non-blast related TBI.

Similar to TBI severity, various auditory outcomes ranging from normal hearing to different types of hearing loss were observed across aetiologies of TBI. Additionally, tinnitus and hyperacusis were reported across different aetiologies.

3.6 Effect of gender on auditory outcomes following non-blast related TBI

In terms of gender, out of 33 studies that included only male patients (n of male = 43) (22, 24, 26, 28, 31, 33, 35, 36, 39, 41, 42, 4446, 4850, 52, 5562, 6468, 71, 76), SNHL was reported in 17 studies in a total of 21 male (22, 26, 36, 39, 42, 45, 46, 48, 50, 52, 58, 61, 62, 6467). Normal hearing in 8 studies, comprising 9 male cases (22, 26, 33, 39, 41, 56, 59, 65), CHL across 7 studies in 8 males (22, 24, 35, 44, 49, 62, 64), and MHL in 5 studies at least one ear and/or one case in six males (24, 26, 39, 60, 67). Tinnitus complaints were reported in 9 of these studies, in a total of 11 male (24, 26, 28, 39, 57, 59, 61, 71, 76), whilst only one case study noted hyperacusis before the assessment (60). The results for other male patients are detailed in Table 2.

In 15 studies involving only female participants (n of females = 16) (11, 25, 27, 34, 37, 38, 40, 43, 47, 51, 53, 54, 63, 69, 70), normal hearing was reported across 4 studies and in 4 females (11, 38, 47, 51), SNHL in 4 case studies (25, 27, 53, 63), CHL in 3 studies and in 4 females (25, 43, 54), and MHL in one case study (51). There were also female cases where no response was obtained in PTA (37, 40), or total hearing loss was observed (69). Additionally, tinnitus complaints before assessment were noted in three studies and females (11, 47, 51), with one study reporting hyperacusis in addition to tinnitus (11). The distribution of auditory outcomes from studies that included only male or only female participants was shown in Figure 4.

Figure 4

Figure 4. Distribution of auditory outcomes by gender following non-blast related TBI.

When cases with the same aetiology and severity (e.g., MVA-related severe or mild TBI) were compared within each gender, auditory outcomes still varied from normal hearing with abnormal central auditory tests (11, 33) to moderate-to-severe hearing loss, including SNHL (58, 63, 64) in both males and females.

Of the 12 studies that included both genders (23, 29, 30, 32, 72, 74, 75, 78, 8082, 94), 4 studies included more males than females (72, 75, 78, 80), and 3 studies included more females than males (74, 82, 94). Seven studies involved multiple participants (72, 74, 75, 78, 80, 82, 94), of which four studies reported normal hearing or a mean of normal hearing (72, 75, 80, 82), except for one participant with SNHL (gender not specified) (80). Another study with 20 males and one female reported SNHL in 47.6% of participants (78). In the five case studies involving both genders (23, 29, 30, 32, 81), hearing conditions ranged from normal hearing (3 females) to CHL (1 female, 3 males) and SNHL (1 female, 4 males). No MHL was reported in female cases, whilst the MHL reported in one male (Case 3) later turned into CHL (30).

Six studies reported participants experiencing tinnitus and hyperacusis. In two case studies, participants reporting tinnitus were male (29, 30). In another cross-sectional study, the number of males with auditory complaints including tinnitus and/or hyperacusis was higher than females, however no formal statistical analysis was undertaken (72). In one study, no significant differences were found between genders in THI and HQ mean scores (74), whereas another study reported that females had greater symptom severity levels than males in the PCSS in relation to hyperacusis (94). Finally, Jafarzadeh et al. (78) did not report the gender of the participants reporting tinnitus.

Overall, the studies showed a range of auditory outcomes based on gender. SNHL was frequently reported in studies with male participants (17/33, 52%), whilst normal hearing and other types of hearing loss were noted in both genders. Tinnitus and hyperacusis were observed in both males and females.

4 Discussion

This scoping review compiled the common auditory impairments of non-blast related TBI, along with exploring the impact of severity, aetiology of TBI, and gender on auditory outcomes. The predominance of case studies compared to other research designs makes it difficult to generalize the results due to individual differences.

In terms of assessment, PTA was the most commonly used assessment method, followed by otoscopic assessment; in contrast, other audiological assessments (e.g., OAEs, central auditory tests and electrophysiological measures) were applied in less than 30% of studies. Inconsistencies in the assessment methods employed indicate a lack of both methodological and clinical standardization in studies conducted in this field. Furthermore, audiological training emphasises the need for performing tests based on a holistic approach and the principle of cross-checking (95), whilst the differences among records can suggest that this approach is not strictly adhered to in practice. However, the presence of abnormal results in central auditory tests (11, 33, 41, 47, 73) or the observation of auditory symptoms such as tinnitus, hyperacusis and difficulty understanding speech-in-noise (11, 72, 73, 82) even in individuals with normal hearing post-TBI, underscores the importance of auditory assessments ranging from PROMs to central auditory tests in this patient group. For instance, in a case study, Cevette et al. (37) observed bilateral results in TEOAE and DPOAE, which indicated normal outer hair cell function, even though results in ipsi-contralateral ARTs and abnormal ABR findings at 90 dB normalized hearing-level (nHL) and as such highlighted the importance of applying OAE tests when investigating potential involvement of different auditory pathway regions due to non-blast TBI. In addition, although the included studies comprehensively assessed the auditory pathway through various tests, as shown in Supplementary Appendix Table 4, some assessments, such as extended-high frequency audiometry (EHFs) and uncomfortable loudness levels (ULLs), were not performed in any of the studies. These assessments may be important for this patient group, or if they are not applied, the reasons for their non-application should be justified. These findings further support the argument for standardising post-TBI audiological assessments, particularly in light of the variability in test application despite the presence of significant auditory symptoms.

Consistent with previous literature (14, 96), the most common type of hearing loss following non-blast related TBI was SNHL (n = 25). Nevertheless, drawing any definitive conclusions can be difficult due to the observation of both normal hearing and other types of hearing loss. Across all studies that performed PTA, the lack of reporting of the type of hearing loss, the accepted classification method for degree of hearing loss, and/or frequencies used to calculate the pure-tone averages also hinder reaching general conclusions about hearing loss associated with non-blast related TBI. Significantly, cases where the type and degree of hearing loss, and/or auditory symptoms change over time (22, 25, 30, 36, 39, 46, 50, 71) show the importance of refraining from making a definitive diagnosis at the initial assessment following non-blast related TBI and emphasize the necessity for regular follow-up assessments in this patient group. Future research is needed with large sample sizes to determine the ideal/recommended time points for audiological assessment post-injury.

Although patients complained of tinnitus and/or hyperacusis, neither PROMs nor any specific methods were used to assess these symptoms across all studies (24, 26, 2830, 39, 51, 57, 5961, 72, 78). This finding may suggest that there were no recommended guidelines for earlier studies or that existing guidelines are not universally/commonly adopted at present, indicating a lack of standardization in assessment (97100). The THI and HQ are among the most commonly used PROMs in the UK (101, 102), and our results of studies using PROMs aligned with this (11, 71, 74, 82). In our review, studies reported a range of tinnitus severity related to TBI, from slight to catastrophic. This could indicate the diverse impacts of TBI on each patient. The fact that hyperacusis is the most commonly reported symptom among TBI patients in studies using the HQ (74, 82) highlights the importance of not overlooking hyperacusis in these patients. Therefore, it is essential to have standardized practices for the assessment of tinnitus and/or hyperacusis in this patient population.

Furthermore, this review highlights the limited use of PROMs across auditory complaints, despite patient-reported symptoms. The limited reports of PROMs may reflect a global lack of awareness or willingness to use PROMS in clinical and/or research contexts and the inclination to prioritise traditional audiological assessments, such as PTA. Another potential reason for limited use is the lack of language-specific validated PROMs for non-English-speaking countries. Whilst traditional audiological assessments do provide essential assessment information, PROMs provide a better understanding of the individual effects of the symptoms which inform both the diagnostic process and intervention plans in a holistic manner (103). Moreover, PROMs are important to evaluate the impact and effectiveness of management strategies on patients’ well-being, functional status and psychosocial needs (104).

In terms of severity, the presence of similar auditory symptoms and types of hearing loss across different severities of TBI suggests that auditory outcomes may arise independently of TBI severity. However, the absence of a study specifically evaluating moderate TBI, inconsistent reporting of TBI severity across studies, and the existing literature indicating a correlation between TBI severity and hearing loss (105, 106) prevent a definitive conclusion on this matter. Furthermore, the lack of consistent reporting of severity criteria among studies that specified TBI severity, and the use of different criteria (e.g., GCS, DSM-5) in the few studies that did report them, make it difficult to draw robust and generalisable conclusions about the impact of TBI severity on auditory outcomes. Although the widely used GCS classification system was introduced in 1974 (6), the earliest study among those included that reported TBI severity was published in 1984 (30), and this study did not specify the criteria used. The earliest study in our records that reported both severity and the criteria for determining it dates back to 2005 (72). This highlights how historical changes in definitions and classifications may affect data comparability. Therefore, future studies should consistently report both the TBI severity and the criteria used for its determination.

Similarly, the observation of normal hearing, all types of hearing loss, and tinnitus in MVAs, falls, and assaults, suggests that aetiology may not have a specific effect on auditory outcomes. Therefore, no definitive framework can be drawn for symptoms related to aetiology. Notably, studies related to sports injuries did not report SNHL and MHL, however, this finding is not sufficient for generalization. Further studies are needed to evaluate the impact of TBI aetiology on auditory outcomes.

The predominance of males who experienced TBI can likely be attributed to the higher incidence of TBI among males, as observed in epidemiological studies (107, 108). Auditory symptoms such as tinnitus and hyperacusis were observed in both genders. SNHL was observed more frequently in male patients, whilst there were no notable differences observed for female patients in the type of hearing loss. Even when similarities in severity and aetiology were controlled, there was still range in auditory outcomes for both genders. However, it should be noted that the imbalance in gender distribution may affect the overall validity of this finding. In the similarity comparison conducted to minimize bias arising from gender imbalance, the presence of different auditory outcomes across both genders impeded clear gender-based interpretations.

The main focus of this review was not to investigate age-related effects of TBI; however, the age range of participants in the studies (from young to older adults) raises important conditions. For instance, in several cases, despite normal hearing, abnormal central auditory test results were observed even in younger adults, which can be considered an important finding for more clearly tracking the direct effects of TBI. However, in studies that include middle-aged and older adults, the potential contribution of age-related central auditory processing decline or hearing loss should not be overlooked (109). Moreover, particular age groups are at higher or lower risk of TBI (110). It is also recognized that neural plasticity varies across the lifespan, which may influence the brain’s response to injury (111). These findings highlight the necessity of considering age-related comparisons when interpreting auditory outcomes in future studies of the TBI population, as age can act as a compound factor affecting both peripheral and central auditory functions.

Despite the older studies dating back to 1956 in this field, the complex nature of TBI and the lack of a guideline and/or standardization in auditory assessment within this patient group make it challenging to establish a comprehensive framework for auditory outcomes. Current findings indicate a wide variation in auditory outcomes based on TBI severity, aetiology and gender. This underscores the need for standardization in assessment and reporting, particularly within the TBI patient group, beginning from general audiological assessments. For this purpose, a guideline should be developed for assessing auditory outcomes in non-blast related TBI patients, and the effect of TBI variables on outcomes should be investigated through larger, systematic research designs in future studies.

4.1 Strengths and limitations

This scoping review provided a comprehensive evaluation of the research objectives through an extensive literature review and analysis. The investigation of the potential effects of TBI severity, aetiology and gender variables on auditory outcomes allowed for an in-depth analysis and insights into the impact of these factors on auditory conditions. However, although the assessment time of the auditory outcomes related to TBI was reported throughout the records, potential differences in auditory outcomes due to assessment time were not examined within this review. Future studies should consider exploring the impact of assessment time on auditory outcomes. In addition, an imbalance in the sample representation of gender, such as a predominance of male participants, limited the generalizability of the findings related to the effects of this variable on auditory outcomes. By conducting a detailed review of studies containing terms such as head injury, fracture, and thalamic lesion, we ensured that only those meeting the diagnostic criteria of TBI (described in inclusion criteria) were included. This allowed us to directly report the auditory consequences of non-blast related TBI. However, it should be recognized that this review only included studies published in English and as such the findings may not be as generalizable to other non-English speaking countries, although studies were included from a range of countries.

5 Conclusion

The compiled findings highlight the diversity of auditory outcomes associated with non-blast related TBI. However, the lack of standardization in audiological assessment methods and reporting, not conducting further assessments (e.g., central auditory tests) in cases of normal hearing, and/or not frequently assessing other audiological symptoms such as tinnitus and hyperacusis hinder a definitive conclusion about the auditory outcomes of TBI patients. Furthermore, these can complicate the diagnosis and treatment process, leading to worsening auditory conditions in TBI patients. All these audiological deficiencies also negatively affect the determination of the effect of variables such as TBI severity, aetiology and gender on auditory outcomes. Therefore, it is crucial to determine standard audiological practices for assessing, reporting, and managing auditory conditions in TBI patients. Following the establishment of these standards, there is a need for specifically designed large-sample size studies with more balanced sample characteristics (e.g., gender or aetiology) to determine the effects of variables on auditory outcomes of non-blast related TBI patients.

Author contributions

KB: Methodology, Project administration, Writing – original draft, Writing – review & editing, Conceptualization, Data curation, Formal analysis, Investigation, Software. LE: Supervision, Writing – review & editing, Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Project administration, Validation. OP: Writing – review & editing, Data curation, Formal analysis. KF: Supervision, Writing – review & editing, Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Project administration.

Funding

The author(s) declare that financial support was received for the research and/or publication of this article. KB was funded by the Ministry of National Education of the Republic of Türkiye to undertake this work as part of her PhD (N/A for the award/grant number). KF was funded by National Institute for Health Research (NIHR Post-Doctoral Fellowship, PDF-2018-11-ST2-003) at the time of completing this work.

Acknowledgments

The authors wish to express gratitude to Dr. Farhad Shokraneh, a medical information specialist who contributed to the development of the research strategy. We would like to express our gratitude to Professor David Baguley, who sadly passed away during this study. His knowledge and expertise helped develop the fundamental ideas for this research, for which we are very thankful.

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Generative AI statement

The author declares that no Gen AI was used in the creation of this manuscript.

Publisher’s note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Author disclaimer

The views expressed in this publication are those of the author(s) and not necessarily those of the NIHR, the NHS or the Department of Health and Social Care.

Supplementary material

The Supplementary material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fneur.2025.1589117/full#supplementary-material

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Abbreviations

ABLB - Alternate Binaural Loudness Balance

ABR - Auditory Brainstem Response

ART - Acoustic Reflex Thresholds

CHL - Conductive Hearing Loss

DPOAE - Distortion Product OAE

ECOG - Electrocochleography

EHFs - Extended-high Frequency

ENT - Ear, Nose and Throat

HHI-A - Hearing Handicap Inventory for Adults

HQ - Hyperacusis Questionnaire

GCS - Glasgow Coma Scale

kHz - Kilohertz

LLR - Late Latency Responses

MHL - Mixed Hearing Loss

MLR - Middle Latency Responses

MMN - Mismatch Negativity

MOSE - Medial Olivocochlear Suppression Effect

MRI - Magnetic Resonance Imaging

MVA - Motor Vehicle Accident

nHL - Normalized hearing-level

NRS - Numeric Rating Scale

OAEs - Otoacoustic Emissions

PCSS - Post-Concussion Symptom Scale

PROMs - Patient-Reported Outcome Measurements

PTA - Pure tone Audiometry

SDS - Speech Discrimination Score

SNHL - Sensorineural Hearing Loss

SNR - Signal-to-Noise-Ratio

SOC - Superior Olivary Complex

TBI - Traumatic Brain Injury

TEOAE - Transient Evoked OAE

TF - Tuning Fork

THI - Tinnitus Handicap Inventory

TQ - Tinnitus Questionnaire

ULLs - Uncomfortable Loudness Levels

WIN - Words-in-Noise

Keywords: traumatic brain injury, auditory, hearing loss, tinnitus, hyperacusis, TBI severity, aetiology, gender

Citation: Bölükbaş K, Edwards L, Phillips OR and Fackrell K (2025) The auditory outcomes in non-blast related traumatic brain injury and the role of severity, aetiology and gender: a scoping review. Front. Neurol. 16:1589117. doi: 10.3389/fneur.2025.1589117

Received: 06 March 2025; Accepted: 21 May 2025;
Published: 10 July 2025.

Edited by:

Ruosha Lai, Central South University, China

Reviewed by:

Yuanping Zhu, Hainan General Hospital, China
Ningning Shao, Geneva Foundation, United States

Copyright © 2025 Bölükbaş, Edwards, Phillips and Fackrell. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Kübra Bölükbaş, a3VicmEuYm9sdWtiYXNAbm90dGluZ2hhbS5hYy51aw==

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