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New Perspectives on Traumatic Auditory Injury

Lubner, Rory J. BS; Kozin, Elliott D. MD

doi: 10.1097/01.HJ.0000582428.19700.50
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Mr. Lubner, left, is a research fellow at Massachusetts Eye and Ear Infirmary. Dr. Kozin is the Neskey-Coghlan Neurotology Fellow at the Massachusetts Eye and Ear. His laboratory focuses on traumatic brain injury and its effects on audiovestibular dysfunction.

Traumatic brain injury (TBI) is a major public health concern, contributing to over 2.8 million deaths, hospitalizations, and emergency department visits annually in the United States.1 While blast-related injuries are a common cause of TBI in military personnel, other types of injuries, such as falls, motor vehicle accidents, assaults, and sports-related head impact, are the most common events that lead to TBI in the civilian population.2 TBI classifications range from mild to severe based on the duration of loss of consciousness, mental status change, posttraumatic amnesia, and imaging findings.3 Mild TBI (mTBI), commonly referred to as a concussion, comprise up to 90 percent of all treated brain injuries.4,5 Patients with mTBI present with a variety of physical and/or sensory abnormalities, including cognitive, sensory, perceptual, psychological, and language deficits, as well as audiovestibular symptoms.6

While balance disorders such as dizziness and vertigo are well-recognized sequalae of head injury,7,8 auditory symptoms have largely been understudied from both clinical and mechanistic perspectives. Emerging studies have examined the auditory symptoms following TBI.9 A recent systematic review including 13 studies and 773 patients with TBI found that up to 58 percent of patients experienced hearing loss.10 Additionally, a recent prospective cohort study of patients with mTBI reported that hearing loss and tinnitus were each experienced in over 60 percent of the study participants.9

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DEPRESSION AND ANXIETY IN HYPERACUSIS

Hyperacusis, often synonymous with noise sensitivity (NS), is increasingly being recognized as a symptom following head injury, including TBI.9,11-13 NS is an auditory disorder of loudness perception in which individuals perceive normal intensities of everyday sounds as uncomfortably loud.14 NS has been shown to be more prevalent among those with TBI compared with age-matched controls.15 A recent study conducted in New Zealand by Shepard and colleagues aimed to investigate the clinical correlates of NS and possible contributing factors in 151 adults who had experienced mTBI within two weeks of the study period.11 Each subject was surveyed using patient-reported outcome measures (PROMs), including Post-Concussion Symptoms Questionnaire (RPQ), Hospital Anxiety and Depression Scale (HADS), and computerized neurocognitive battery testing (CNS-VS). Relationships between NS and other variables were analyzed using stepwise regression.11

JOURNAL CLUB HIGHLIGHT

Shepherd D, Landon J, Kalloor M, Theadom A. Clinical correlates of noise sensitivity in patients with acute TBI. Brain Inj 2019:1-9.

Shepard, et al., found that over half (59%) of all mTBI patients reported some degree of NS.11 They also found a moderate positive association between NS and depression (r=.375, p <.001) and anxiety (r=.399, p<.001) within the mTBI population.11 Previous research has demonstrated that patients with depression suffer from early auditory processing deficits,16 and it is therefore difficult to discern whether auditory symptoms precede depression, or vice versa. Further research is necessary to characterize the interplay between NS and depression within the context of head injury.

In addition to anxiety being independently associated with NS severity, anxiety was also found to be the single strongest clinical marker for NS following mTBI and stepwise multilinear regression modeling, predicting the largest amount of variability (~20%) in NS scores.11 While the mechanism underlying the association between anxiety and NS among people with head injuries is not well understood, the authors hypothesized that NS may be a form of hypervigilance from fear of the head injury reoccurring. Clinical recognition of the close relationship between anxiety and NS may help provide counseling for patients with NS following mTBI.

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AUDIOVESTIBULAR SYMPTOMS IN SPORTS-RELATED TBI

In one of the largest published cohort studies for sports-related TBI to date, Chorney and colleagues utilized data collected by the National College Athletic Association Injury Surveillance System (NCAA-ISS) to determine the rates of audiovestibular symptoms following sports-related concussions among college athletes.17 After including 1,647 recorded concussions within a five-year period, the authors found that dizziness, imbalance, and NS at the time of the injury were associated with prolonged concussion duration. Interestingly, imbalance and NS were also correlated with an increased return to participation time. The authors concluded that audiovestibular symptoms including NS may serve as reliable clinical prognostic indicators following head impact that results in mTBI.17

JOURNAL CLUB HIGHLIGHT

Chorney SR, Suryadevara AC, Nicholas BD. Audiovestibular symptoms as predictors of prolonged sports-related concussion among NCAA athletes. Laryngoscope 2017; 127:2850-2853.

Further characterization of NS in sports-related mTBI patients was performed in 58 college-level athletes with normal hearing, in which 28 had a history of one or more concussions.18 The authors found that concussed athletes scored higher on the HQ and had a greater sensitivity to sound on psychoacoustic tasks compared with non-concussed athletes. Interestingly, when concussed athletes were separated by reporting sound sensitivity symptoms, concussed athletes had lower loudness discomfort levels and increased HQ and depression scores on the Beck Depression Inventory (BDI),18 consistent with the reported association between NS and depression in Shepard, et al.11 Symptoms such as noise sensitivity have been described by athletes as the worst part of a concussion, and thus increased social isolation and return to play time perpetuate the athletes’ audiovestibular and depressive symptoms.18 The authors from both studies highlighted the growing role of cognitive behavior therapy as part of NS treatment.

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TBI-RELATED NOISE SENSITIVITY, AUDITORY DYSFUNCTION

Auditory symptoms, including noise sensitivity, are often overlooked during TBI rehabilitation, likely due to the subjective nature of symptom reporting and a lack of understanding of the pathophysiological underpinnings behind impact-related auditory dysfunction. Potential etiologies can be divided into peripheral and central causes. In terms of peripheral causes, the diagnosis of labyrinthine concussion has been used to describe auditory symptoms following head injury without temporal bone fracture.19,20 Recently published human otopathologic studies have demonstrated distinct histologic changes in patients following head injury, including loss of hair and spiral ganglion cells.21 Head injury studies on animal models conducted throughout the 20th century have described a range of potential causes, including inner ear hemorrhage, traveling pressure wave, obstruction of the endolymphatic sac, and stretching of the cochlear nerve.22-25 Research by Kujawa and Liberman over the past decade points to cochlear synaptopathy (also known as hidden hearing loss) as a potential etiology for auditory dysfunction after noise trauma, resulting in difficulty hearing in noise, hyperacusis, and tinnitus.26,27 Although the concept of cochlear synaptopathy has been largely studied in the context of noise-induced hearing loss, our increasing awareness of this phenomenon may help inform future research on TBI-related auditory dysfunction.

With regard to the central causes of auditory dysfunction, a landmark paper by Kraus, et al., found that children who sustained a concussion have a signature neural profile based upon measured speech-evoked frequency-following responses (FFRs).28 The authors argued that FFR can be used to correctly identify 90 percent of pediatric concussion cases and clear 95 percent of all control cases without concussion. In contrast to Assi's study that suggested the use of NS as a predictor for concussion duration, Kraus argued that FFRs may serve as an additional biomarker in the accurate diagnosis and prompt treatment of mTBI and its clinical symptoms.28

Auditory symptoms, including NS, are increasingly being recognized as a sequala of mTBI. In particular, NS has been linked as a prognostic factor for concussion symptom duration following sports-related mTBI. While no standard treatment protocol exists for NS following a head injury, interventions that address the major clinical correlates of NS such as anxiety may help alleviate the associated auditory symptoms. Future histopathological and clinical investigations that utilize animal models of TBI may be useful when further delineating the mechanisms behind auditory symptoms and elucidating novel therapeutic strategies to effectively reduce symptoms.

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REFERENCES

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