By Mikhaylo Szczupak, MD, and Michael E. Hoffer, MD
Tinnitus is an auditory perception in the absence of any external sound stimulus. Many factors have been associated with tinnitus, such as brain injury, hearing loss and old age. Although the pathophysiology of this disease entity remains unknown, leading theories suggest that the following portions of the auditory pathway may be involved: injured cochlear hair cells repetitively stimulating auditory nerve fibers, spontaneous activity within individual auditory nerve fibers, hyperactivity of auditory brain stem nuclei, or reduction in suppressive activity of the central auditory cortex on peripheral auditory nerve activity (Atik, 2014). The study of tinnitus continues to be a challenge because of the subjective nature of the condition, its likely multifactorial etiology and the many varied tinnitus assessment scales (Hoffer et.al. 2003). Our goal in this review will be to examine several subtypes of post-traumatic tinnitus, in particular acoustic trauma, traumatic brain injury and barotrauma.
There is a well-known association between history of exposure to noise trauma, high-frequency hearing loss and the presence of high-pitched “whistling tinnitus” (Nicolas-Puel et al., 2006). Hearing loss severity has been demonstrated to predict degree of tinnitus discomfort in symptomatic individuals (Dias et al., 2008) Although pitch matching is not a perfect technique for measuring tinnitus symptoms, the most commonly observed frequency of tinnitus is often the same as the worst frequency for hearing (Axelsson, et al., 2002). Many believe that impulse noise is more damaging to hearing than continuous sound, pure tones are more harmful than composite sounds and high-pitched sounds are likely more harmful than low-pitched sounds (Axelsson, et al., 2002). Clearly there is an association between noise trauma and tinnitus but the exact pathogenesis remains enigmatic.
Acoustic trauma damages the hair cells of the cochlea by exerting vascular, metabolic and chemical changes on normal physiologic processes (Fausti et al., 2009). These changes have been shown to cause decreased hair cell stereocilia stiffness, auditory nerve cell swelling and ultimately cell death/degeneration of auditory nerve fibers (Fausti et al., 2009). The cochlear damage seen following acoustic trauma can be either temporary or permanent and may occur in the absence of elevated hearing thresholds (Schaette et al., 2011) Interestingly, in individuals with normal audiograms, the occurrence of tinnitus is not correlated with current occupational noise level, duration of noise exposure or even cumulative noise exposure (Rubak et al., 2008). Alterations seen following acoustic trauma may be seen centrally in addition to the peripheral changes in the cochlea mentioned above. Current theories suggest that this etiology of tinnitus is related to auditory deprivation secondary to an acoustic insult causing enhanced synchronization of neuronal activity in the auditory cortex (Ortmann el al., 2011). Ortmann et al. were the first to demonstrate these neuroplastic changes in humans, with 13 of 14 amateur rock musicians exhibiting increased gamma activity in the right auditory cortex with transient tinnitus and temporary hearing loss after noise exposure (Ortmann el al., 2011).
Certain vocations, particularly military service members, are at an increased risk of acoustic trauma and as a result, both tinnitus and hearing loss (Mrena et al., 2002). The acoustic environment of a military setting is unique for several reasons: warfighters are often required to remain in noisy environments to complete a mission without the possibility of rotating out. Aircraft/firearm operations take place in reduced areas compared to civilian operations. and individuals may sacrifice hearing protection to more easily communicate with other team members (Yankaskis, 2013). Service weapons may produce noise levels ranging from 150 to 180 dB of sound pressure level (SPL), exceeding the 140 dB SPL threshold where there is a high probability of sustaining marked damage to the auditory system (Ylikoski et al., 1995). There are few studies within the current literature reporting the prevalence of tinnitus within the entire active-duty/veteran United States (U.S.) military population. Helfer et al. demonstrated a 30.8% point estimate for tinnitus prevalence in active U.S. Army soldiers (Helfer et al., 2004). Higher rates of noise-induced tinnitus have been found for military personnel of other nations (Mrena et al., 2009).
Even more common than military service is exposure to music both professionally and recreationally. Hagberg et al. surveyed 407 Swedish music academy students and found that tinnitus was the most prevalent symptom (10.6 individuals per 1000 years of instrumental practice) (Hagberg et al., 2005). Potier et al. investigated tinnitus in disc jockeys, another population of professional musicians (Potier et al., 2009). Nearly three quarters (75.9%) of the 29 included disc jockeys complained of tinnitus, that on pitch matching corresponded with patterns seen on audiogram (Potier et al., 2009). With evolving portable music technology and ever popular electronic dance music festivals, recreational loud music exposure continues to increase. Approximately 75 to 90% of young adults have experienced transient tinnitus after loud music exposure (Quintanilla-Dieck et al., 2009. Gilles et al., 2012). These individuals reported minimal awareness of the long term impact of chronic loud music exposure with only 15% using ear plugs in a concert/nightclub setting (Quintanilla-Dieck et al., 2009). There exists an obvious potential for education of these young adults as well as professional musicians on the proper use of hearing protection to prevent tinnitus and hearing loss.
Traumatic Brain Injury
Traumatic brain injury (TBI) is a broad term used to describe an entity in which there is either a blunt or blast force applied to the head transmitting force to the brain. The incidence of TBI in both the civilian and military populations continues to be a public health issue. Based on the most recent CDC statistics, 2.4 million annual emergency department visits, hospitalizations or deaths were a result of TBI (Coronado et al., 2012). Approximately 75% of these injuries can be classified as mild traumatic brain injury (mTBI) (National CIP, 2003). To warrant diagnosis of mTBI an individual must meet the following criteria: Glasgow Coma Scale (GCS) greater than or equal to 13, loss of consciousness not in excess of 1 hour and post-traumatic amnesia not exceeding 24 hours. Even with decreasing frequencies of operational military engagements, mTBI incidence is expected to remain constant as a result of military training exercises and participation of active duty members in recreational sports (Terrio, et al., 2009).
Tinnitus has been well studied in individuals suffering mTBI, particularly in the military. Since 2007, tinnitus has been the most common service-connected disability of both new (completion of service within the prior 12 months) and existing military veterans (US DOVA, 2015). Based on its prevalence in proportion to all other service-connected disabilities, the cost of tinnitus is estimated to be greater than $3 billion annually in military veterans alone (US DOVA, 2015). Balance disorders, hearing loss, tinnitus, cognitive difficulties and/or sleep disturbances can be seen in more than 95% of all individuals who sustain mTBI (Hoffer et al., 2010). One or more of these symptoms will persist in greater than 80% of individuals treated with the current standard of care (Hoffer et al., 2010).
Oleksiak et al. demonstrated that 76% of Operation Iraqi Freedom/Operation Enduring Freedom veterans diagnosed with mTBI during active duty reported tinnitus upon subsequent audiological evaluation (Oleksiak et al., 2012). In one of the largest epidemiological studies to date, Yurgil et al. prospectively assessed 1647 active-duty Marine and Navy servicemen for tinnitus and TBI (Yurgil et al., 2015). Deployment-related TBI, blast exposure and multiple TBIs each more than doubled the likelihood of post deployment tinnitus (Yurgil et al., 2015). Interestingly, the prevalence of tinnitus in the civilian population recovering from TBI has been found to be slightly lower than the military population. A pilot study of middle aged individuals recovering from blunt TBI by Jury et al. demonstrated that 53% reported symptoms of tinnitus (Jury et al., 2001). The principal theory as to why brain injury leads to auditory dysfunction is thought to be a result of diffuse axonal injury to the central auditory pathway (Nolle et al., 2004). Clearly, tinnitus following mTBI is a partially understood, prevalent condition that is worthwhile to screen for in both military and civilian populations.
The natural history of history of tinnitus secondary to mTBI follows an unexpected course. In data collected from 148 service members who sustained mTBI secondary to blast, over 90% reported “non-concerning ringing” immediately after the injury (Hoffer and Balaban, 2011). One week later only 70% reported tinnitus, and 10 days later less than 33%. Surprisingly, this value then rises to over 60% several months after the initial injury. There are likely multiple factors involved in this trend such as pre-existing tinnitus, “primed” inner ear from previous noise exposure and incompletely understood pathophysiology (Hoffer and Balaban, 2011).
Exclusive to blast mTBI, tympanic membrane rupture is a commonly observed sequelae. Of the 33 victims from the 2005 Thailand terrorist bombings with complete otologic and audiologic follow-up, 22 (66%) exhibited some degree of tympanic membrane perforation (9 bilaterally, 13 unilaterally) (Tungsinmunkong et al., 2007). The tympanic membrane is the most frequently injured anatomical structure from blast and the least resistant to increased atmospheric pressure (DePalma et al, 2005). As a result, some have suggested that if the tympanic membrane is intact, then any primary effects of the blast wave on other air-containing organs are unlikely (DePalma et al., 2005). The majority (75%) of tympanic membrane perforations heal spontaneously within several months without complication while the remainder require surgical intervention (Kronenberg et al., 1993).
There are several specific causes of pulsatile and nonpulsatile tinnitus that occur following TBI. A vascular origin is assumed for pulsatile tinnitus until proven otherwise, several of which are considered life threatening (Kruezer et al., 2014). The three most common causes of post-traumatic pulsatile tinnitus are carotid dissection, arteriovenous fistulas and carotid cavernous fistulas (Chae et al., 2001. Liang et al., 2007. Redekop, 2008). Post-traumatic nonpulsatile tinnitus can occur due to injury at several points along the auditory pathway, such as the cochlea, the auditory nerve or the brain (Kruezer et al., 2014). The most frequent etiologies of nonpulsatile tinnitus are temporal/petrous bone fractures, labyrinthine concussion, ossicular chain disruption and perilymphatic fistula (Fitzgerald, 1995. Chen et al., 2001. Ulug and Ulubil, 2006. Yetiser et al., 2008). The latter two typically surgical intervention and can also be seen following barotrauma.
Air travel and underwater diving are two common situations when barotrauma to the ear may occur. These injuries are a result of rapid pressure changes from either ascending or descending with inadequate pressure equalization. Damage ensues from a pressure gradient between the middle ear cavity and the external atmosphere across the tympanic membrane (Mirza and Richardson, 2005). For ascent during both air travel and underwater diving, the ambient atmospheric pressure decreases while the gas in the middle ear cavity expands. Subsequently, the eustachian tube opens and vents off positive air pressure beginning at a pressure differential of 15 mmHg (Mizra and Richardson, 2005). Problems rarely occur with passive venting if the eustachian tubes are patent and functioning properly. In contrast, descent during both air travel and underwater diving is an active process. Air does not typically enter the middle ear cavity passively and some form of muscular activity (swallowing, yawning, chewing, etc.) is required. At a pressure differential of 90 mmHg, the soft nasopharyngeal end of the eustachian tube closes at a force greater than that which can be developed by the muscles that open the tube.41 Attempts to equalize pressure once this has occurred are ineffective. The significant density disparity between water and air explains why barotrauma occurs more frequently from underwater diving compared to air travel (Becker and Parell, 2001).
Damage may occur as a result of mucosal edema or blood within the middle ear cavity causing symptoms of tinnitus and/or hearing loss (Becker and Pareell, 2001). More severe injuries include tympanic membrane rupture and ossicular chain disruption (Mizra and Richardson, 2005). Less frequently, injury to the inner ear structures may occur, commonly presenting with the additional symptom of dizziness. Three hypothesized mechanisms of injury are hemorrhage, labyrinthine membrane tear and perilymph fistula via the oval or round windows (Mizra and Richardson, 2005). Damage to the round window occurs more frequently because the oval window membrane is thicker and protected by the both the stapes footplate and surrounding ligaments (Mizra and Richardson, 2005). Treatment of barotrauma injuries is generally conservative aside from ossicular chain disruption, perilymphatic fistula and refractory tympanic membrane perforation, which all require surgery (Duplessis and Hoffer, 2006).
Tinnitus is a common sequelae following brain injury. Severe traumatic events can cause multiple sub-types of post-traumatic tinnitus. For example, following a major blast injury, a soldier may sustain traumatic brain injury as well as acoustic trauma and barotrauma. Additionally, tinnitus is rarely the only complaint after trauma and individuals may present with multiple symptoms which all require evaluation (Kreuzer et al., 2014). A comprehensive diagnostic assessment (complete history and physical, audiological testing, imaging) is crucial to identify the injury and guide treatment which will be covered in subsequent articles within this edition. Ultimately, education and prevention will take a leading role in averting post-traumatic tinnitus as these protective technologies continue to develop.
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ABOUT THE AUTHORS
Captain Michael E. Hoffer, MD, received his undergraduate degree from Stanford University and graduated from Medical School at the University of California, San Diego. After his Otolaryngology Residency at the University of Pennsylvania, he completed a neurotology fellowship with Dr. Herb Silverstein in Sarasota, Florida after which he was commissioned as an active duty officer in the United States Navy. Captain Hoffer is board certified in Otolaryngology and Neurotology and serves as specialty leader for Navy Otolaryngology. Dr. Hoffer serves on multiple national level boards including the council of the Triologic Society, the council of the National Institute of Deafness and Communication Disorders, and the NASA Neurologic IPT. He is a member of many national and international societies and considered an expert in inner ear drug delivery and audio-vestibular disorders after blunt and blast head trauma. Captain Hoffer has been deployed twice to Iraq serving with the U.S. Marines and is Fleet Marine Corps Officer Qualified.
Mikhaylo Szczupak, MD, is post-doctoral research fellow in the Department of Otolaryngology at the University of Miami.
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