Introduction
Damage to the ear is the most common organ injury after exposure to blast overpressure (BOP). A blast injury occurs due to a rapid overpressurization force to the body. The middle and inner ear are particularly sensitive to sudden pressure changes and are therefore very susceptible to blast injuries. Blast injury to the ear may be caused by the detonation of high-order explosives (e.g., dynamite, nitroglycerine) that produce a supersonic, overpressurization shock wave, or by nonexplosive sudden pressure changes in the external auditory canal (EAC), such as a slap to the side of the head. These mechanisms generally cause a rapid increase in pressure within the EAC and can lead to a variety of middle and inner ear injuries. Patients with otologic damage after BOP often present with tympanic membrane rupture. Additional signs and symptoms may include ossicular chain dislocation, conductive, mixed or sensorineural heading loss, tinnitus, and dizziness/vertigo. , While it is not uncommon for tympanic membrane perforations and conductive hearing loss to improve spontaneously, a subset of patients continues to experience transient or permanent high-frequency sensorineural hearing loss (SNHL), suggestive of additional inner ear damage. In this chapter, we examine the anatomy and physiology of the ear as it relates to blast injury.
Background: normal anatomy and physiology of the ear
Sound waves travel along the EAC to reach the tympanic membrane (TM), which separates the external ear from the pneumatized middle ear ( Fig. 4.1A ). The tympanic membrane can be divided into four quadrants and is comprised of the pars tensa and the pars flaccida. The pars tensa, which makes up the majority of the drum, consists of three distinct layers—a lateral epithelial layer, a fibrous middle layer, and an inner mucosal layer. The pars flaccida, located superiorly between the anterior and posterior malleolar ligaments, lacks the fibrous layer and is as such less resistant to pressure changes. The middle ear contains the ossicular chain, specifically the three ossicles, malleus, incus, and stapes. The malleus attaches to the tympanic membrane and medially connects with the incus via the incudomalleolar joint. The incus interacts with the stapes through the incudostapedial joint, and the stapes footplate provides direct communication with the inner ear via the oval window ( Fig. 4.1A ). The ossicular chain acts as a lever, causing relative medial displacement of the stapes footplate at the oval window. The middle ear matches the lower impedance of sound waves in the air to the higher impedance fluid in the cochlea. This amplifying function has been described as middle ear gain, and the impedance matching is essential for the efficiency of air conduction. The vibratory area of the tympanic membrane is about 20 times greater than the area of the stapes footplate. This area ratio together with the mechanical lever effect especially from the malleus and incus achieves a middle ear gain of roughly 25–35 dB. Damage to the middle ear conductive pathway impairs the efficiency of sound conduction and consecutively can lead to conductive hearing loss. ,
In the inner ear, transmitted sounds propagate as frequency-dependent travel waves through inner ear fluids along the turns of the cochlea, moving the basilar membrane and with it the organ of Corti (OC) ( Fig. 4.1B ). The cochlea is organized in tonotopic fashion, with high frequencies located at the base, and low frequencies located at the apex. Different frequencies result in a distinct peak of a traveling sound wave along the basilar membrane. Its movement creates localized shearing forces along the OC, which, through subsequent steps, initiate the process of mechanotransduction: Mechanical energy of the traveling wave is transformed into electrochemical energy at the apical surface of the inner hair cells within the OC. Stereocilia bundle movement leads to opening of ion channels, potassium influx, and subsequent depolarization of hair cells. Neurotransmitter release from ribbon synapses at the basal portion of inner hair cells stimulates bipolar afferent spiral ganglion neurons. An action potential is generated, and the signal is transmitted along the central auditory pathway in a tonotopic organization. Outer hair cells (OHCs) serve to amplify and tune the cochlear traveling wave through an additional active motile process.
Overview: types of blast explosions and blast injuries to the ear
Detonation of high-order explosives generally causes a supersonic blast wave, resulting in a large increase in pressure as the wave propagates outward from the explosion core. This is followed by the blast wind, which is a rapid decrease in pressure that pulls objects back toward the core of the explosion. This stands in contrast to low-order explosives, which produce subsonic waves without associated blast waves. The use of improvised explosive devices (IEDs) has increased with mounting frequency of terror attacks, and these devices may be a high order, low order, or a mix of both types of explosives, which makes the prediction of injury patterns challenging.
Of note, the pathophysiology of explosive blasts is distinct from nonexplosive blast injury to the ear: nonexplosive blast injury is relatively common, with similar symptoms as explosive blast injury, but is caused by sudden sealing of the EAC with associated increased pressure in the EAC (such as a slap or punch to the ear, e.g., in sports accidents), and frequently leads to rupture of the tympanic membrane.
Blast injury can be categorized into four groups: primary, secondary, tertiary, and quaternary blast injuries. Primary blast injury (PBI) affects organs that contain gas or air, such as the lungs and the ear. This type of injury is due to extreme and fast changes in pressure caused by the blast wave. Therefore, this type of injury is unique to high-order explosives. Otologic damage is the most common outcome for survivors of blast injury, with the majority of survivors suffering from tympanic membrane perforations (TMPs). Given its unique anatomy, the tympanic membrane can be perforated at pressure changes as small as 5 psi, making it particularly sensitive to PBI. Other possible outcomes of PBI to the ear include dizziness, hearing loss, and ossicular chain injury or dislocation. , Hearing loss after BOP can be conductive, sensorineural, or mixed. Conductive hearing loss refers to mechanical damage and impaired sound transmission to the inner ear, as seen with TMP or ossicular chain dysfunction. SNHL affects structures of the inner ear and is generally irreversible.
Secondary blast injuries (SBIs) are caused by rapid movement of items in the air due to the blast wind, which may cause blunt or penetrating injuries to an individual. Resulting injuries to the ear may occur along the outer ear, including damage to the pinna and in the EAC. Similar to PBI, traumatic perforation of the tympanic membrane and ossicular chain dislocation can occur with SBI. Blast wind carrying contaminating particles in the air may lead to infections by depositing them in the ear canal and middle ear. SBI can be protected against by body armor and ear protection; it is therefore more likely to occur in civilian settings than military settings. Tertiary blast injury refers to injury sustained from displacement of the body and may lead to head trauma, which has been linked to hearing loss and/or tinnitus. Hearing loss after traumatic brain injury (TBI) without evidence of skull fractures has been documented and linked to brainstem injury and contusions involving the auditory regions in the brain. Auditory and vestibular symptoms resulting from concussions can last 6 months or longer after blast injury. Quaternary blast injury refers to other types of sustained injuries not aforementioned, from burns to posttraumatic stress disorder.
This chapter mainly focuses on research advances related to the physiology of PBI.
Blast injury to the tympanic membrane
The tympanic membrane (TM) is highly sensitive to pressure changes and is commonly ruptured during exposure to blast overpressure. Injuries caused by BOP lead to severe deformation of the TM as well as the ossicular chain, causing significant structural damage. Ear protection can lower the maximum pressure caused by the blast, but body armor and head protection cannot prevent PBI. Closer proximity to the explosion core increases chances of TMP, but this is additionally influenced by head positioning—a position perpendicular to the blast wave or a frontal blast wave has a higher likelihood of causing TMP than parallel orientation. , Four grades mark the degree of TMP related to blast injury. Grade 1 includes linear tears or pinpoint defects within the drum, grade 2 includes smaller perforations with defects up to 50% of the drum, grade 3 marks defects of >50% up to 75%, and grade 4 is reserved for total drum defects ( Fig. 4.1C ). ,
The pars tensa of the drum is most commonly affected, and central perforations outweigh perforations in marginal locations, due to higher vulnerability to disproportionate overpressurization. Spontaneous TMP recovery is possible, but positive outcomes vary widely. The size, shape, location, and often irregular margins of traumatic perforations play a significant role in the lower numbers of spontaneous recovery. , Generally, larger perforations after blast injury are less likely to heal, as are more centrally located perforations, whereas inferior perforations were the most likely to heal. ,
Multiple mathematical models, animal studies, and studies of human temporal bones have attempted to better understand the underlying changes of mechanical TM properties and damage to its microstructure after BOP. The middle layer of the TM is unique in that it is comprised of radially and circumferentially aligned collagen fibers. This layer significantly influences the elasticity or stiffness of the TM.
Its mechanical properties change based on the level of strain, and changes in TM stiffness in response to an applied force are measured by Young’s modulus. In a recent human temporal bone study, cadaveric tympanic membrane strip samples first underwent multiple blasts to create an injury pattern before the TMs were exposed to sound stimulation. Mechanical TM stiffness had decreased significantly, and the Young Modulus was found to be reduced by more than 50%. This reduction was frequency specific in that it affected mainly high-frequency sound conduction, and the residual stiffness corresponded to the degree of injury of the TM. Electron microscopy of the TM after BOP revealed corresponding damage and fractures of both radial and circumferential TM fibers.
Similar results were found in animal studies, where chinchilla tympanic membranes were exposed to BOP levels below the TM rupture threshold. Mechanical properties of the TM were analyzed with a microfringe projection system and characterized using a finite element method (FEM) model. Young’s modulus after blast was found to have decreased by more than 50%. This demonstrated that even in TMs that did not rupture after exposure to BOP, there is deformation due to the high strain rate with damage to the collagen fiber layer, softening the TM. When a similar method was used in human cadaveric temporal bones, Young’s modulus decreased by up to 20% after multiple blasts. A TM rupture dose–response risk assessment based on the FEM model predicted the probability of injury to the TM dependent on TM displacement, velocity, and acceleration. Assuming that TMP is associated with purely mechanical, structural damage after traumatic blast loading, the fast running algorithm allowed for prediction of possible moderate and severe TM ruptures.
A similar model was employed again in a follow-up study, where the influence of blast wave direction on probability of TMP was further analyzed. Blast wave exposure to the front of the face was more likely to cause rupture of the TM compared with other directions, due to comparably higher changes in maximum stress within the TM.
A novel method using laser Doppler vibrometers (LDVs) was able to successfully assess motion of the TM during BOP. TM motion in cadaveric temporal bones was recorded in response to BOP of 35 kPa, and LDVs reliably measured TM displacement and velocity to provide data on blast wave transduction through the middle ear.
Traumatic TMPs related to explosions have a much lower spontaneous healing rate compared with other traumatic TMPs, even at lower perforation grades, and improved understanding of the pathophysiology, as well as prediction of the injury pattern could significantly aid to determine when and which surgical intervention is needed. , , ,
Blast injury to the ossicular chain
PBI to the middle ear in general resulted in conductive hearing loss with impaired sound conduction into the inner ear. In patients exposed to BOP, ossicular injury requiring ossiculoplasty varied anywhere from 10% to 20%. Ossicular damage was frequently associated with TMP, and, as the nature of the blast wave tends to invert the edges of the tympanic membrane, increased risk of middle ear cholesteatoma. , The incidence of middle ear damage also positively correlated with higher levels of blast overexposure. While the TM has been fairly well studied in various model systems, less is known about the biomechanics of the ossicles during BOP. Damage in the form of dislocation of the ossicular chain or fractures has been clinically described, but the underlying pathophysiology remains elusive.
Recent biomechanical measurements, however, have been able to shed light on overall blast energy transmission through the middle ear. , , High-intensity sound from BOP changes middle ear transfer function, and with it the amount of energy that is being transmitted into the cochlea. , , Using the previously described approach with LDVs, Jiang et al. measured the displacement of the stapes footplate (SFP) during BOP in a cadaveric human temporal bone study. SFP far exceeded normal movements and ranged from 41.2 to 126.5 μm when a stimulus level of 187 dB was applied. Interestingly, placement of hearing protection devices such as ear plugs reduced movement and displacement of the SFP, indicating a preventative effect during blast exposure.
Blast injury to the inner ear
Blast-induced SNHL with associated tinnitus and vertigo has been well documented as a direct consequence of blast overpressure in military and civilian settings, but the underlying pathophysiology is distinct from the purely mechanical damage seen in the middle ear. , In cases of inner ear hearing loss, the symptoms can be temporary, and hearing loss presents as temporary threshold shift (TTS) which resolves over time; or, depending on the injury pattern, symptoms and threshold shift may be permanent (PTS). , , SNHL is considered irreversible and associated with permanent macroscopic or microscopic damage to auditory structures within the inner ear. ,
Recovery of hearing after initial threshold shift is not uncommon after blast injury. , In patients with SNHL, high-frequency SNHL appeared to be the most common pattern. , , Next to TTS or PTS, tinnitus was one of the most common audiological complaints after blast injury and presented immediately after the injury in the majority of cases, rather than over time. , , , Tinnitus and hyperacusis also remained as symptoms despite recovery of hearing thresholds, with lasting increased sensitivity to noise and hearing difficulties in noisy environments. This was attributed to possible “hidden hearing loss.” Hidden hearing loss has recently been described as a new form of SNHL, a cochlear synaptopathy associated with isolated ribbon synapse loss and without visible threshold shift ( Fig. 4.1D ).
In analogy to studies on conductive hearing loss and BOP, computational, cadaveric, and animal studies have been serving as models to investigate SNHL related to traumatic inner ear damage after blast injury.
Previous data indicated that SNHL after high intensity sounds or a blast wave may be a result of enhanced energy transmission through the middle ear via the TM and ossicular chain.
This was supported by modeling of a blast wave moving from the external ear to the cochlea, which demonstrated increased displacement of the tympanic membrane and the ossicular chain, and which translated into exaggerated movement and displacement of the stapes footplate during BOP, subsequently leading to significantly increased cochlear pressures and basilar membrane at a level conducive to irreversible structural damage to the inner ear.
An additional study confirmed that SNHL and PTS in mice after BOP were directly related to the blast wave and not associated with concurrent TMP. Lower-pressure blast waves produced elevated auditory brainstem evoked responses (ABRs) and distortion product otoacoustic emission (DPOAE) thresholds on day 0. DPOAEs function as a measure of cochlear hair cell function. ABR thresholds at frequencies lower than 30 kHz recovered completely, while those above 30 kHz did not. DPOAE-elevated thresholds did not recover. Higher pressure blast correlated with larger threshold elevation in ABR and reduced threshold recovery. Cochleas lacked outer hair cells in the blast-exposed, high-frequency regions in up to 40%, and spiral ganglion neurons were increasingly reduced with higher-pressure blast waves. Despite this, the overall morphology of the cochlea was not changed.
When using a blast stimulator on mice for either single or triple blast wave exposure to the inner ear, animals experienced the previously described TMP, as well as ABR threshold elevations of 50–65 dB 1 day after exposure. Single blast animals partially recovered low-frequency thresholds after 1 month, but triple blast exposed mice never showed measurable recovery. DPOAE thresholds were undetectable across all frequencies in both groups up to 1 week after the blast, but partially recovered in the majority of single-blast mice after 6 months. This clearly indicates a dose dependency between SNHL, cochlear damage, and severity of BOP. This was supported by histological analysis, which found significant loss of OHC in basal and middle turns in triple blasted mice. IHC and spiral ganglion numbers were unchanged between control, single, and triple blasted mice, but presynaptic portions of ribbon synapses were reduced in middle and apical cochlear regions of triple-blasted mice and in the middle cochlear region of single-blasted mice, suggesting additional beginning synaptopathy.
To better identify histologic and molecular changes associated with BOP, another study utilized an advanced blast simulator to create inner ear damage in a rat model. Associated TMP was observed after blast exposure, which healed completely by 4 weeks. Presence of inner ear hemorrhage at day 1 and 7 correlated with absent DPOAEs. DPOAEs slightly recovered by 1 month, but remained elevated compared with baseline ( Fig. 4.2 ). ABR thresholds were elevated across all frequencies, in addition to significant reduction and increased latency of ABR wave 1 amplitude, a measure of the distal portion of the spiral ganglion nerves (SGN). Thresholds partially improved, but only in the lower frequencies. RNA sequencing (RNASeq) of inner ear tissue demonstrated differentially expressed genes in the cochlea 1 day (acute) and 1 month (chronic) after blast exposure, underlining additional subcellular changes related to altered transcriptional regulation and activation of immune response within the inner ear. During the acute phase, 1 day after blast exposure, gene upregulation was found in pathways related to cation channel activity, nervous system development, and neurotransmitter release, among others. One month after blast injury, positively regulated pathways involved cell–cell junction, protein binding, and antigen processing and presentation.
