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Audiovestibular loss in anterior inferior cerebellar artery territory infarction: A window to early detection?
Journal of the Neurological Sciences 313 (2012) 153–159
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Journal of the Neurological Sciences journal homepage: www.elsevier.com/locate/jns
Audiovestibular loss in anterior inferior cerebellar artery territory infarction: A window to early detection? Hyung Lee ⁎ Department of Neurology, Keimyung University School of Medicine, Daegu, Republic of Korea Brain Research Institute, Keimyung University School of Medicine, Daegu, Republic of Korea
a r t i c l e
i n f o
Article history: Received 29 June 2011 Received in revised form 27 August 2011 Accepted 29 August 2011 Available online 13 October 2011 Keywords: Audiovestibular loss AICA territory infarction
a b s t r a c t Acute audiovestibular loss is a common neurotological condition that is characterized by sudden onset of severe prolonged (lasting days) vertigo and hearing loss and is diagnosed by the presence of canal paresis to caloric stimulation and sensorineural hearing loss on pure tone audiogram. Before 2000, papers on anterior inferior cerebellar artery (AICA) territory infarction focused mostly on associated brainstem and cerebellar findings, without a detailed description of neurotological findings. Since 2000, several reports have demonstrated that acute audiovestibular loss is an important sign for the diagnosis of AICA territory infarction. To date, at least eight subgroups of AICA infarction have been identified according to the pattern of neurotological presentations, among which the most common pattern of audiovestibular dysfunction is the combined loss of auditory and vestibular functions. Because audiovestibular loss may occur in isolation before ponto-cerebellar infarction involving AICA distribution, audiovestibular loss may serve as a window to prevent the progression of acute audiovestibular loss into more widespread areas of infarction in posterior circulation (mainly in the AICA territory). Clinician should keep in mind that acute audiovestibular loss may herald impending AICA territory infarction, especially when patients had basilar artery occlusive disease presumably close to the origin of the AICA on brain MRA, even if other central signs are absent and MRI does not demonstrate acute infarction. © 2011 Elsevier B.V. All rights reserved.
1. Introduction Acute audiovestibular loss is a common neurotological syndrome characterized by sudden onset of severe prolonged (lasting days) vertigo and hearing loss. The presence of canal paresis (CP) to caloric stimulation and sensorineural hearing loss (SNHL) on pure tone audiogram is considered as a mandatory sign for the diagnosis of acute audiovestiublar loss. It can occur in isolation (i.e., acute labyrinthitis or labyrinth infarction) or is associated with other neurological symptoms or signs that in the later condition are usually accompanied by ischemic stroke in the territory of the anterior inferior cerebellar artery (AICA) [1,2]. Acute ischemic stroke in the distribution of the AICA is known to be associated with vertigo, hearing loss, nystagmus, facial weakness, gait ataxia, and hypalgesia. In 1943, Adams [3] was the first to completely describe the syndrome associated with the AICA occlusion. Although neurotologic symptoms such as vertigo, tinnitus, and bilateral hearing loss were early initial symptoms in his patients, neurotological findings have received little attention. Subsequent reports [4–8] on AICA infarction before 2000 focused mostly on the brainstem and cerebellar findings or mechanism of stroke without the associated neurotologic findings. Since 2000, many studies have shown that a ⁎ Department of Neurology, Keimyung University School of Medicine, 194 Dongsan dong, Daegu 700-712, Republic of Korea. Tel.: + 82 53 250 7835; fax: + 82 53 250 7840. E-mail address: [email protected]. 0022-510X/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.jns.2011.08.039
neurotological dysfunction with vertigo and/or hearing loss is an important sign for the diagnosis of the AICA [1,9–16]. An extensive neurotological evaluation suggested that CP and SNHL are mainly caused by ischemia to the inner ear [1,9–16]. This review aims to highlight recent advances on audiovestibular loss in the AICA territory infarction and to address their clinical significance. It is especially focused on isolated audiovestibular loss as a window to early detection of AICA infarction. 2. Vascular mechanism of AICA territory infarction The mechanism for AICA occlusion was atherothrombotic in most cases [5–7]. In a series of nine patients with AICA territory infarction diagnosed by brain MRI [7], four diabetic patients had isolated unilateral AICA infarctions due to basilar artery branch occlusive disease because these patients had patent basilar artery on angiography. In these patients, plaque in the basilar artery probably extended into the AICA or microatheroma blocked the AICA orifice, resulting in isolated AICA infarction. The other five patients had infarcts extending beyond AICA territory (i.e., AICA infarct and other infarcts in the posterior circulation). These all had basilar artery occlusion including the AICA level and reconstitution of the distal basilar artery on angiography. A recent report also showed similar findings that most patients (82%, 45/55) with isolated AICA infarction showed normal basilar artery on MRA and severe basilar artery occlusive disease was more common in
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patients with posterior circulation infarcts in addition to AICA infarct [16]. Rarely emboli originating from cardiac or atheromatous plaque in the proximal artery lodge in the AICA orifice result in AICA infarction [5,17] (Fig. 1). Overall, isolated AICA infarcts are usually caused by basilar branch occlusive disease, whereas infarcts extending beyond AICA territory are mostly due to basilar artery occlusive disease [5–7,16]. 3. Audiovestibular loss as an important sign for the diagnosis of AICA territory infarction The internal auditory artery (IAA) irrigates the cochlea and vestibular labyrinth, and occlusion of the IAA causes a loss of auditory and vestibular function (i.e., audiovestibular loss), resulting in hearing loss and vertigo, so-called labyrinthine (inner ear) infarction. IAA infarction mostly occurs due to thrombotic narrowing of the AICA itself, or in the basilar artery at the orifice of the AICA [5–7]. Because the inner ear is not well visualized on routine MRI, a definite diagnosis of labyrinthine infarction with audiovestibular loss is not possible unless a pathological study is done. Hearing loss has been traditionally considered as a less common sign of AICA territory infarction. There are at least two possible explanations. First, patients may not be aware of their hearing loss during an attack of vertigo and vomiting when the unilateral hearing loss is mild or
the severity of associated vertigo is severe. Second, neurologists have not included the audiogram as a routine diagnostic tool for the evaluation of AICA infarction. However, more than 90% (11/12) of patients with AICA infarction diagnosed by brain MRI had acute SNHL, which is accompanied by acute vertigo and CP (i.e., audiovestibular loss) [1]. Several recent papers [1,9–16] emphasized that AICA infarction commonly accompanied inner ear involvement and labyrinthine infarction with audiovestibular loss is an important sign for the diagnosis of AICA infarction. When audiovestibular loss occurs, infarction of the brainstem and/ or cerebellum in the territory of the AICA is usually associated. However, AICA infarction rarely causes isolated audiovestibular loss without brainstem or cerebellar signs (i.e., isolated labyrinthine infarction), in which case an acute infarct may still be seen on brain MRI [12]. Thus, clinicians should be aware of the possibility of AICA infarction, particularly in older patients with acute audiovestibular loss and vascular risk factors, even when other brainstem or cerebellar signs are absent. 4. Isolated audiovestibular loss before AICA territory infarction: frequency and clinical implication When vertigo or hearing loss is associated with other brainstem or cerebellar signs, the diagnosis of AICA infarction is easily made.
Fig. 1. Three common vascular mechanisms in AICA territory infarction. A. Infarcts on brain MRI are localized to the middle cerebellar peduncle and anterior cerebellum, which is typically known to be supplied by the AICA (A-1), and brain MRA shows no vascular compromise in the basilar artery (A-2). B. Brain MRI shows multiple infarcts in the posterior circulation (B-1), in addition to AICA territory infarction (B-2), and brain MRI shows poorly visualized basilar and distal vertebral arteries (B-3). C. The infarcted area on brain MRI is consistent with AICA territory (C-1). Initial MRA shows moderate stenosis of the lower basilar artery, presumably close to the origin of the AICA (C-2), but follow-up MRA 10 days after the onset of symptoms shows no stenosis of the basilar artery (C-3), suggesting complete recanalization. This patient had paroxysmal atrial fibrillation and emboli originating from the cardiac probably lodge in the AICA orifice, resulting in AICA infarction. AICA: anterior inferior cerebellar artery.
H. Lee / Journal of the Neurological Sciences 313 (2012) 153–159
However, partial ischemia of the AICA may give rise to isolated vertigo or hearing loss because the IAA is an end artery with minimal collaterals from other major arterial branches, and the cochlea and vestibular apparatus are supplied by different branches of the IAA [18,19]. There have been several case reports [9,13,14] indicating that acute audiovestibular loss may be an impending sign of AICA territory infarction. In one study [15], 8% (4/43) of patients with documented AICA territory infarction on brain MRI initially experienced an isolated audiovestibular loss with a normal brain MRI. Another similar study showed that in 30% (9/29) of patients with acute SNHL (mainly combined with vertigo) due to posterior circulation ischemic stroke, an isolated audiovestibular loss had been the initial presenting symptom, up to 10 days before other delayed neurological deficits [20]. In a more recent study [16], in approximately 16% (13/82) of patients with AICA territory infarction on brain MRI, acute vertigo/auditory disturbance (mostly hearing loss) in isolation had been the initial symptoms within 1 month before the infarction. Although the above three studies were somewhat different in methodology, all of these data suggested that 8–30% of patients with posterior circulation stroke (mainly AICA territory) had acute audiovestibular loss before more widespread infarction and this symptom may come to be viewed as an opportunity to prevent an impending posterior circulation stroke. Because most patients with prodromal audiovestibular disturbances had an evidence of focal or diffuse segment of reduced blood flow in the basilar artery presumably close to the origin of the AICA [1,11,16], prodromal vertigo and/or hearing loss before AICA infarction may be explained by the assumption that an atheromatous plaque within the basilar artery may have extended into the AICA ostia. By this mechanism, decreased blood flow in the affected AICA might cause transient episode of selective ischemia to the inner ear, resulting in isolated prodromal audiovestibular disturbance, because the inner ear requires high-energy metabolism and has little collateral circulation [18,19]. Although there are as yet no systematic data on what a highrisk factor suggesting impending stroke is or what interventions might be beneficial at the stage of isolated audiovestibular loss, patients with prodromal audiovestibular disturbance were more likely to have focal or diffuse stenosis of the basilar artery presumably close to the origin of the AICA than patients without audiovestibular disturbance [1,11,16]. This finding emphasized that AICA infarction should be considered, particularly in elderly patients with vascular risk factors and
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acute audiovestibular loss, even when MRI does not demonstrate acute infarction in the brain. At this stage, clinicians should consider a further investigation and proper managements to prevent progression of acute audiovestibular loss into a more widespread posterior circulation stroke, mainly in the territory of the AICA. Because current diagnostic methods (including MRI) cannot confirm labyrinthine infarction among the acute audiovestibular loss syndrome, clinicians should consider all the clinical evidences when attempting to determine the etiology of acute audiovestibular loss rather than emphasizing that MRI is the best way to distinguish viral from vascular etiology [21]. Fig. 2 illustrates the MRI findings in a patient with acute audiovestibular loss as a prodromal sign of AICA territory infarction. The diffusion-weighted MRI was normal at the time of acute isolated audiovestibular loss. The site of injury responsible for isolated audiovestibular loss was probably localized to the inner ear or vestibular nerve. 5. Which of the anatomical structures supplied by the AICA is more sensitive to ischemia? AICA territory infarction is diagnosed on brain MRI or CT by involvement of at least one of the following anatomical structures such as middle cerebellar peduncle, lateral inferior pontine area, or anterior cerebellar hemisphere [5]. Amarenco et al. showed that approximately 80% of patients with AICA infarction showed symptoms or signs indicative of lateral pontine dysfunction including facial weakness or crossed sensory loss [7]. High incidence of pontine dysfunction in AICA territory infarction may be explained by the fact that the pontine area supplied by the AICA has little collateral circulation, but the cerebellar hemisphere has a rich anastomotic network originating from other cerebellar arteries including the posterior inferior or superior cerebellar arteries [5,7,22]. Thus, involvement of the lateral inferior pons and middle cerebellar peduncle is considered as a radiological hallmark for the diagnosis of the AICA infarction. However, recent papers after 2000 have contradictive findings [1,16]. All but one (11/12, 92%) patients with AICA territory infarction had a audiovestibular loss with CP and SNHL on presentation, which is mostly resulted from injury to the inner ear, but symptoms and signs suggestive of pontine dysfunction were found in only 50% of patients [1]. In the largest series to date on the audiovestibular symptoms of AICA infarcts (82 patients), 60% had audiovestublar loss
Fig. 2. MRI findings in a patient with acute audiovestibular loss as a prodromal sign of AICA territory infarction. (A and B) Axial diffusion-weighted brain MRI 1 day after the onset of sudden right-sided hearing loss and vertigo was normal, but MRA (C) shows severe stenosis of the proximal portion of the basilar artery presumably close to the origin of the AICA and the distal right vertebral artery. One day later, the patient complained of exacerbation of vertigo and hearing loss on the right ear. On examination, there were bidirectional gaze-evoked nystagmus and dysmetria on the right limb. (D and E) Follow-up axial diffusion-weighted MRI demonstrated hyperintense foci involving the right middle cerebellar peduncle and the right anterior cerebellum. AICA: anterior inferior cerebellar artery.
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(group 3), acute prolonged vertigo with audiovestibular loss is sometimes preceded by an episode(s) of transient vertigo/auditory disturbance, which is considered as a prodromal sign of impending AICA territory infarction. Fourth (group 4), AICA infarction rarely presented with acute prolonged vertigo and isolated auditory loss without vestibular loss (i.e., SNHL without CP). Fifth (group 5), AICA infarction rarely presented with acute prolonged vertigo and isolated superior vestibular loss without auditory loss (i.e., CP without SNHL). Sixth (group 6), AICA infarction rarely presented with acute prolonged vertigo and isolated inferior vestibular loss without auditory or superior vestibular loss (i.e., abnormal vestibular evoked myogenic potential without CP or SNHL). Seventh (group 7), AICA infarction rarely presented with acute prolonged vertigo and isolated audiovestibular loss without any other neurological symptoms/signs. Eighth (group 8), AICA infarction rarely presented with nonvestibular symptoms including tingling sensation on the face and/or extremities, gait ataxia, or cerebellar dysmetria and normal audiovestibular function. Overall, AICA territory infarction can produce a broad spectrum of neuro-otological presentations, in which the most common pattern of audiovestibular dysfunctions is the combined loss of auditory and vestibular function. Selective loss of vestibular or cochlear function is infrequently observed. The pattern of inner ear involvement in AICA territory infarction is shown in Fig. 3.
with CP and SNHL, whereas facial weakness or crossed sensory loss suggesting pontine dysfunction was found in only 28% (23/82) of patients [16]. Complete AICA infarction involving the middle cerebellar peduncle, lateral pons, and anterior inferior cerebellum was found in only 16% (13/82) of patients [16]. Thus, although pontine signs are key features differentiating AICA infarction from more common benign disorders involving the inner ear, they are less common than previously thought. As noted above, the labyrinth requires highenergy metabolism and the IAA is an end artery with minimal collaterals from the otic capsule so the labyrinth is especially vulnerable to ischemia [18,19,22]. By contrast, the retrocochlear acoustic nerve has an abundant collateral blood supply arising from the lateral medullary artery, arteries supplying adjacent dura matter and petrous bone, and the inferior lateral pontine artery [18,23,24]. Overall, recent prospectively gathered evidence suggests that the inner ear is a commonly affected site during AICA territory ischemia, as well as, the brainstem although current imaging techniques including MRI did not permit the visualization of the inner ear. 6. Vestibular dysfunction in AICA territory infarction With AICA territory infarction, the most common pattern of vestibular dysfunction is a combination of peripheral (i.e., unilateral CP), and central signs (e.g., asymmetrically impaired smooth pursuit, bidirectional gaze-evoked nystagmus, or impaired modulation of the vestibular responses using visual input) that was observed in approximately 65% (53/82) of a large series of consecutive cases [16]. These findings occur because the AICA supplies peripheral vestibular structures such as the inner ear and vestibulocochlear nerve, in addition to central vestibular structures [5,7]. Because AICA supplies both peripheral and central vestibular structures, the site(s) responsible for producing vertigo with AICA infarction is difficult to determine in an individual patient. However, most patients with AICA infarction have a unilateral decrease to CP, suggesting dysfunction of the peripheral vestibular structures at least in part. Occasionally, patients with vertigo have normal caloric responses, in which case the vertigo likely originates from ischemia to central vestibular structures.
8. Clinical implication of a broad spectrum of audiovestibular loss in AICA territory infarction When patients with risk factors for stroke developed acute onset of isolated prolonged vertigo without accompanying hearing loss or other neurological symptoms, ischemic damage to the superior vestibular labyrinth due to anterior vestibular artery (AVA) infarction is reasonably suspected because the lumen of the AVA is small and has little collateral circulation [18,19,22]. A previous report [18] also supported this assumption because approximately 50% of patients with isolated episodic vertigo of a vascular cause (i.e., vertebrobasilar insufficiency) had unilateral CP, which is commonly localized to the inner ear (i.e., superior vestibular labyrinth). However, recent finding did not support this assumption because only four (5%) patients showed isolated vestibular labyrinthine involvement at the time of AICA infarction [16]. Thus, although isolated AVA infarction may serve as a mechanism of isolated vascular vertigo, the incidence would be low. Isolated involvement of the cochlea was also an uncommon manifestation of AICA infarction, which was observed in only 3% of patients [16]. Unlike inner ear dysfunction of a viral cause, which can commonly present as an isolated vestibular (i.e., vestibular neuritis) or cochlear loss (i.e., sudden deafness), labyrinthine dysfunction of a vascular cause rarely results in isolated loss of vestibular or auditory function. Thus, when sudden onset of isolated prolonged vertigo or hearing loss occurred in patients with vascular risk factors, vascular compromise to the inner ear was less likely considered. However, when the combined audiovestibular loss occurred in patients with prolonged vertigo, the vascular cause was highly suspected.
7. Spectrum of audiovestibular loss in AICA territory infarction (Table 1) Nearly all patients (80/82, 98%) with AICA infarction have acute prolonged (more than 24 h) vertigo and vestibular dysfunction of peripheral, central, or combined origin [16]. So far, there are eight subgroups of AICA territory infarction according to the pattern of neuro-otological presentations [16,25]. First (group 1), acute prolonged vertigo with audiovestibular loss is the most common subgroup of audiovestibular dysfunction in AICA territory infarction. Second (group 2), acute prolonged vertigo but without documented audiovestibular loss is also a common presentation in AICA territory infarction. In this condition, vertigo originates from dysfunction of the central vestibular structure. Third
Table 1 Spectrums of audiovestibular loss in AICA territory infarction.
Presented with vertigo Combined audiovestibular loss Normal audiovestibular function Prodromal audiovestibular disturbance Isolated SNHL (normal caloric and VEMPs responses) Isolated CP (normal hearing and VEMPs responses) Isolated VEMPs abnormality (normal caloric and VEMPs responses) Associated with other neurological symptoms or signs
Group 1
Group 2
Group 3
Group 4
Group 5
Group 6
Group 7
Group 8
+ + − − − − − +
+ − + − − − − +
+ + − + − − − +
+ − − − + − − +
+ − − − − + − +
+ − − − − − + +
+ + − − − − − −
− − + − − − − +
AICA: anterior inferior cerebellar artery; SNHL: sensorineural hearing loss; CP: canal paresis; VEMPs: vestibular evoked myogenic potentials.
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Fig. 3. Schematic diagram of the patterns of inner ear involvement in AICA territory infarction according to type of involved artery. A. The arterial supply to the inner ear. B. Internal auditory artery occlusion results in combined loss of cochlear and vestibular functions (i.e., SNHL, CP, and abnormal VEMP). C. Main cochlear artery occlusion causes selective loss of cochlear function (isolated SNHL). D. Anterior vestibular artery occlusion causes selective loss of superior vestibular function (isolated CP only). E. Posterior vestibular artery occlusion causes selective loss of inferior vestibular function (abnormal VEMP only). F. No involvement of the internal auditory artery results in normal cochlear and vestibular functions. Hatched region indicates area of lesion. SNHL: sensorineural hearing loss, CP: canal paresis, VEMP: vestibular evoked myogenic potentials.
9. Long-term outcome of audiovestibular loss with CP and SNHL In audiovestibular loss of a vascular cause, it was previously thought that hearing loss is usually permanent, but dizziness and
imbalance gradually improve with central compensation. However, a recent report [20] showed that most patients (17/21, 81%) with labyrinthine infarction after at least 1 year follow-up showed improved hearing loss partially or completely. A recovery rate of 81% is above
Fig. 4. MRI and progress of audiovestibular dysfunction in a patient with AICA territory infarction who had severe hearing loss initially, but showed normal hearing level on the last follow-up. A. Axial diffusion-weighted MRI demonstrates acute infarcts involving the right middle cerebellar peduncle. B. Initial pure tone audiogram reveals severe hearing loss (80 dB) with 40% speech discrimination in the right ear. Hearing levels in decibels (dB) (American National Standards Institute, 1989) are plotted against stimulus frequency on a logarithmic scale. C. Initial video-oculographic recordings of bithermal caloric tests disclose the left CP (84%). D. Follow-up testing performed 4 years after the onset of symptoms shows a complete recovery of hearing loss in the right ear. E. Follow-up caloric test performed 4 years after the onset of symptoms also shows normal caloric response on the left side. AICA, anterior inferior cerebellar artery; CP, canal paresis; Vmax, maximal velocity of slow phase of nystagmus.
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Fig. 5. MRI and progress of audiovestibular dysfunction in a patient with AICA territory infarction who had profound hearing loss at initial and last follow-up. A. Axial diffusionweighted MRI demonstrates acute infarcts involving the right middle cerebellar peduncle and right anterior cerebellar hemisphere. B. Initial pure tone audiogram reveals profound hearing loss on the right side. Hearing levels in decibels (dB) (American National Standards Institute, 1989) are plotted against stimulus frequency on a logarithmic scale. C. Initial video-oculographic recordings of bithermal caloric tests show a right CP (64%). D. Follow-up testing performed 6 years after the onset of symptoms shows persistent hearing loss with no interval change. E. Follow-up caloric test performed 6 years after the onset of symptoms shows normal caloric responses on the right side. AICA, anterior inferior cerebellar artery; CP, canal paresis; Vmax, maximal velocity of slow phase of nystagmus.
the spontaneous recovery rate (40%–69%) reported for idiopathic SNHL [26,27], but is similar to the recovery rate (61%–89%) of idiopathic SNHL after steroid treatment [28–30]. Although there are no systematic studies on factors predicting poor outcome in patients with SNHL of a vascular cause, the improvement rate of hearing loss in patients with profound hearing loss was significantly lower than that in patients with less than profound hearing loss (40% vs 94%) [20]. This is consistent with previous studies focusing on idiopathic sudden SNHL [31–33]. Similar to hearing loss of a vascular cause, CP of a vascular cause may also be normalized. A recent paper [34] showed that 67% of patients with CP associated with posterior circulation ischemic stroke after at least 1 year follow-up showed normalized caloric response. Furthermore, all patients after more than 5 years follow-up after the onset of vertigo showed normalized caloric response [34]. Overall, recent data suggests that audiovestibular loss associated with posterior circulation ischemic stroke often has a good long-term outcome. Illustrative cases of good outcome with complete recovery of audiovestibular loss and poor outcome with no recovery of SNHL of a vascular cause are shown in Figs. 4 and 5, respectively. Conflict of interest I have no conflict of interest. References [1] Lee H, Sohn SI, Jung DK, Cho YW, Lim JG, Yi SD, et al. Sudden deafness and anterior inferior cerebellar artery infarction. Stroke 2002;33:2807–12. [2] Lee H. Neuro-otological aspects of cerebellar stroke syndrome. J Clin Neurol 2009;5:65–73. [3] Adams RD. Occlusion of the anterior inferior cerebellar artery. Arch Neurol Psychiatry 1943;49:765–70.
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Audiovestibular loss in anterior inferior cerebellar artery territory infarction: A window to early detection? Hyung Lee ⁎ Department of Neurology, Keimyung University School of Medicine, Daegu, Republic of Korea Brain Research Institute, Keimyung University School of Medicine, Daegu, Republic of Korea
a r t i c l e
i n f o
Article history: Received 29 June 2011 Received in revised form 27 August 2011 Accepted 29 August 2011 Available online 13 October 2011 Keywords: Audiovestibular loss AICA territory infarction
a b s t r a c t Acute audiovestibular loss is a common neurotological condition that is characterized by sudden onset of severe prolonged (lasting days) vertigo and hearing loss and is diagnosed by the presence of canal paresis to caloric stimulation and sensorineural hearing loss on pure tone audiogram. Before 2000, papers on anterior inferior cerebellar artery (AICA) territory infarction focused mostly on associated brainstem and cerebellar findings, without a detailed description of neurotological findings. Since 2000, several reports have demonstrated that acute audiovestibular loss is an important sign for the diagnosis of AICA territory infarction. To date, at least eight subgroups of AICA infarction have been identified according to the pattern of neurotological presentations, among which the most common pattern of audiovestibular dysfunction is the combined loss of auditory and vestibular functions. Because audiovestibular loss may occur in isolation before ponto-cerebellar infarction involving AICA distribution, audiovestibular loss may serve as a window to prevent the progression of acute audiovestibular loss into more widespread areas of infarction in posterior circulation (mainly in the AICA territory). Clinician should keep in mind that acute audiovestibular loss may herald impending AICA territory infarction, especially when patients had basilar artery occlusive disease presumably close to the origin of the AICA on brain MRA, even if other central signs are absent and MRI does not demonstrate acute infarction. © 2011 Elsevier B.V. All rights reserved.
1. Introduction Acute audiovestibular loss is a common neurotological syndrome characterized by sudden onset of severe prolonged (lasting days) vertigo and hearing loss. The presence of canal paresis (CP) to caloric stimulation and sensorineural hearing loss (SNHL) on pure tone audiogram is considered as a mandatory sign for the diagnosis of acute audiovestiublar loss. It can occur in isolation (i.e., acute labyrinthitis or labyrinth infarction) or is associated with other neurological symptoms or signs that in the later condition are usually accompanied by ischemic stroke in the territory of the anterior inferior cerebellar artery (AICA) [1,2]. Acute ischemic stroke in the distribution of the AICA is known to be associated with vertigo, hearing loss, nystagmus, facial weakness, gait ataxia, and hypalgesia. In 1943, Adams [3] was the first to completely describe the syndrome associated with the AICA occlusion. Although neurotologic symptoms such as vertigo, tinnitus, and bilateral hearing loss were early initial symptoms in his patients, neurotological findings have received little attention. Subsequent reports [4–8] on AICA infarction before 2000 focused mostly on the brainstem and cerebellar findings or mechanism of stroke without the associated neurotologic findings. Since 2000, many studies have shown that a ⁎ Department of Neurology, Keimyung University School of Medicine, 194 Dongsan dong, Daegu 700-712, Republic of Korea. Tel.: + 82 53 250 7835; fax: + 82 53 250 7840. E-mail address: [email protected]. 0022-510X/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.jns.2011.08.039
neurotological dysfunction with vertigo and/or hearing loss is an important sign for the diagnosis of the AICA [1,9–16]. An extensive neurotological evaluation suggested that CP and SNHL are mainly caused by ischemia to the inner ear [1,9–16]. This review aims to highlight recent advances on audiovestibular loss in the AICA territory infarction and to address their clinical significance. It is especially focused on isolated audiovestibular loss as a window to early detection of AICA infarction. 2. Vascular mechanism of AICA territory infarction The mechanism for AICA occlusion was atherothrombotic in most cases [5–7]. In a series of nine patients with AICA territory infarction diagnosed by brain MRI [7], four diabetic patients had isolated unilateral AICA infarctions due to basilar artery branch occlusive disease because these patients had patent basilar artery on angiography. In these patients, plaque in the basilar artery probably extended into the AICA or microatheroma blocked the AICA orifice, resulting in isolated AICA infarction. The other five patients had infarcts extending beyond AICA territory (i.e., AICA infarct and other infarcts in the posterior circulation). These all had basilar artery occlusion including the AICA level and reconstitution of the distal basilar artery on angiography. A recent report also showed similar findings that most patients (82%, 45/55) with isolated AICA infarction showed normal basilar artery on MRA and severe basilar artery occlusive disease was more common in
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patients with posterior circulation infarcts in addition to AICA infarct [16]. Rarely emboli originating from cardiac or atheromatous plaque in the proximal artery lodge in the AICA orifice result in AICA infarction [5,17] (Fig. 1). Overall, isolated AICA infarcts are usually caused by basilar branch occlusive disease, whereas infarcts extending beyond AICA territory are mostly due to basilar artery occlusive disease [5–7,16]. 3. Audiovestibular loss as an important sign for the diagnosis of AICA territory infarction The internal auditory artery (IAA) irrigates the cochlea and vestibular labyrinth, and occlusion of the IAA causes a loss of auditory and vestibular function (i.e., audiovestibular loss), resulting in hearing loss and vertigo, so-called labyrinthine (inner ear) infarction. IAA infarction mostly occurs due to thrombotic narrowing of the AICA itself, or in the basilar artery at the orifice of the AICA [5–7]. Because the inner ear is not well visualized on routine MRI, a definite diagnosis of labyrinthine infarction with audiovestibular loss is not possible unless a pathological study is done. Hearing loss has been traditionally considered as a less common sign of AICA territory infarction. There are at least two possible explanations. First, patients may not be aware of their hearing loss during an attack of vertigo and vomiting when the unilateral hearing loss is mild or
the severity of associated vertigo is severe. Second, neurologists have not included the audiogram as a routine diagnostic tool for the evaluation of AICA infarction. However, more than 90% (11/12) of patients with AICA infarction diagnosed by brain MRI had acute SNHL, which is accompanied by acute vertigo and CP (i.e., audiovestibular loss) [1]. Several recent papers [1,9–16] emphasized that AICA infarction commonly accompanied inner ear involvement and labyrinthine infarction with audiovestibular loss is an important sign for the diagnosis of AICA infarction. When audiovestibular loss occurs, infarction of the brainstem and/ or cerebellum in the territory of the AICA is usually associated. However, AICA infarction rarely causes isolated audiovestibular loss without brainstem or cerebellar signs (i.e., isolated labyrinthine infarction), in which case an acute infarct may still be seen on brain MRI [12]. Thus, clinicians should be aware of the possibility of AICA infarction, particularly in older patients with acute audiovestibular loss and vascular risk factors, even when other brainstem or cerebellar signs are absent. 4. Isolated audiovestibular loss before AICA territory infarction: frequency and clinical implication When vertigo or hearing loss is associated with other brainstem or cerebellar signs, the diagnosis of AICA infarction is easily made.
Fig. 1. Three common vascular mechanisms in AICA territory infarction. A. Infarcts on brain MRI are localized to the middle cerebellar peduncle and anterior cerebellum, which is typically known to be supplied by the AICA (A-1), and brain MRA shows no vascular compromise in the basilar artery (A-2). B. Brain MRI shows multiple infarcts in the posterior circulation (B-1), in addition to AICA territory infarction (B-2), and brain MRI shows poorly visualized basilar and distal vertebral arteries (B-3). C. The infarcted area on brain MRI is consistent with AICA territory (C-1). Initial MRA shows moderate stenosis of the lower basilar artery, presumably close to the origin of the AICA (C-2), but follow-up MRA 10 days after the onset of symptoms shows no stenosis of the basilar artery (C-3), suggesting complete recanalization. This patient had paroxysmal atrial fibrillation and emboli originating from the cardiac probably lodge in the AICA orifice, resulting in AICA infarction. AICA: anterior inferior cerebellar artery.
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However, partial ischemia of the AICA may give rise to isolated vertigo or hearing loss because the IAA is an end artery with minimal collaterals from other major arterial branches, and the cochlea and vestibular apparatus are supplied by different branches of the IAA [18,19]. There have been several case reports [9,13,14] indicating that acute audiovestibular loss may be an impending sign of AICA territory infarction. In one study [15], 8% (4/43) of patients with documented AICA territory infarction on brain MRI initially experienced an isolated audiovestibular loss with a normal brain MRI. Another similar study showed that in 30% (9/29) of patients with acute SNHL (mainly combined with vertigo) due to posterior circulation ischemic stroke, an isolated audiovestibular loss had been the initial presenting symptom, up to 10 days before other delayed neurological deficits [20]. In a more recent study [16], in approximately 16% (13/82) of patients with AICA territory infarction on brain MRI, acute vertigo/auditory disturbance (mostly hearing loss) in isolation had been the initial symptoms within 1 month before the infarction. Although the above three studies were somewhat different in methodology, all of these data suggested that 8–30% of patients with posterior circulation stroke (mainly AICA territory) had acute audiovestibular loss before more widespread infarction and this symptom may come to be viewed as an opportunity to prevent an impending posterior circulation stroke. Because most patients with prodromal audiovestibular disturbances had an evidence of focal or diffuse segment of reduced blood flow in the basilar artery presumably close to the origin of the AICA [1,11,16], prodromal vertigo and/or hearing loss before AICA infarction may be explained by the assumption that an atheromatous plaque within the basilar artery may have extended into the AICA ostia. By this mechanism, decreased blood flow in the affected AICA might cause transient episode of selective ischemia to the inner ear, resulting in isolated prodromal audiovestibular disturbance, because the inner ear requires high-energy metabolism and has little collateral circulation [18,19]. Although there are as yet no systematic data on what a highrisk factor suggesting impending stroke is or what interventions might be beneficial at the stage of isolated audiovestibular loss, patients with prodromal audiovestibular disturbance were more likely to have focal or diffuse stenosis of the basilar artery presumably close to the origin of the AICA than patients without audiovestibular disturbance [1,11,16]. This finding emphasized that AICA infarction should be considered, particularly in elderly patients with vascular risk factors and
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acute audiovestibular loss, even when MRI does not demonstrate acute infarction in the brain. At this stage, clinicians should consider a further investigation and proper managements to prevent progression of acute audiovestibular loss into a more widespread posterior circulation stroke, mainly in the territory of the AICA. Because current diagnostic methods (including MRI) cannot confirm labyrinthine infarction among the acute audiovestibular loss syndrome, clinicians should consider all the clinical evidences when attempting to determine the etiology of acute audiovestibular loss rather than emphasizing that MRI is the best way to distinguish viral from vascular etiology [21]. Fig. 2 illustrates the MRI findings in a patient with acute audiovestibular loss as a prodromal sign of AICA territory infarction. The diffusion-weighted MRI was normal at the time of acute isolated audiovestibular loss. The site of injury responsible for isolated audiovestibular loss was probably localized to the inner ear or vestibular nerve. 5. Which of the anatomical structures supplied by the AICA is more sensitive to ischemia? AICA territory infarction is diagnosed on brain MRI or CT by involvement of at least one of the following anatomical structures such as middle cerebellar peduncle, lateral inferior pontine area, or anterior cerebellar hemisphere [5]. Amarenco et al. showed that approximately 80% of patients with AICA infarction showed symptoms or signs indicative of lateral pontine dysfunction including facial weakness or crossed sensory loss [7]. High incidence of pontine dysfunction in AICA territory infarction may be explained by the fact that the pontine area supplied by the AICA has little collateral circulation, but the cerebellar hemisphere has a rich anastomotic network originating from other cerebellar arteries including the posterior inferior or superior cerebellar arteries [5,7,22]. Thus, involvement of the lateral inferior pons and middle cerebellar peduncle is considered as a radiological hallmark for the diagnosis of the AICA infarction. However, recent papers after 2000 have contradictive findings [1,16]. All but one (11/12, 92%) patients with AICA territory infarction had a audiovestibular loss with CP and SNHL on presentation, which is mostly resulted from injury to the inner ear, but symptoms and signs suggestive of pontine dysfunction were found in only 50% of patients [1]. In the largest series to date on the audiovestibular symptoms of AICA infarcts (82 patients), 60% had audiovestublar loss
Fig. 2. MRI findings in a patient with acute audiovestibular loss as a prodromal sign of AICA territory infarction. (A and B) Axial diffusion-weighted brain MRI 1 day after the onset of sudden right-sided hearing loss and vertigo was normal, but MRA (C) shows severe stenosis of the proximal portion of the basilar artery presumably close to the origin of the AICA and the distal right vertebral artery. One day later, the patient complained of exacerbation of vertigo and hearing loss on the right ear. On examination, there were bidirectional gaze-evoked nystagmus and dysmetria on the right limb. (D and E) Follow-up axial diffusion-weighted MRI demonstrated hyperintense foci involving the right middle cerebellar peduncle and the right anterior cerebellum. AICA: anterior inferior cerebellar artery.
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(group 3), acute prolonged vertigo with audiovestibular loss is sometimes preceded by an episode(s) of transient vertigo/auditory disturbance, which is considered as a prodromal sign of impending AICA territory infarction. Fourth (group 4), AICA infarction rarely presented with acute prolonged vertigo and isolated auditory loss without vestibular loss (i.e., SNHL without CP). Fifth (group 5), AICA infarction rarely presented with acute prolonged vertigo and isolated superior vestibular loss without auditory loss (i.e., CP without SNHL). Sixth (group 6), AICA infarction rarely presented with acute prolonged vertigo and isolated inferior vestibular loss without auditory or superior vestibular loss (i.e., abnormal vestibular evoked myogenic potential without CP or SNHL). Seventh (group 7), AICA infarction rarely presented with acute prolonged vertigo and isolated audiovestibular loss without any other neurological symptoms/signs. Eighth (group 8), AICA infarction rarely presented with nonvestibular symptoms including tingling sensation on the face and/or extremities, gait ataxia, or cerebellar dysmetria and normal audiovestibular function. Overall, AICA territory infarction can produce a broad spectrum of neuro-otological presentations, in which the most common pattern of audiovestibular dysfunctions is the combined loss of auditory and vestibular function. Selective loss of vestibular or cochlear function is infrequently observed. The pattern of inner ear involvement in AICA territory infarction is shown in Fig. 3.
with CP and SNHL, whereas facial weakness or crossed sensory loss suggesting pontine dysfunction was found in only 28% (23/82) of patients [16]. Complete AICA infarction involving the middle cerebellar peduncle, lateral pons, and anterior inferior cerebellum was found in only 16% (13/82) of patients [16]. Thus, although pontine signs are key features differentiating AICA infarction from more common benign disorders involving the inner ear, they are less common than previously thought. As noted above, the labyrinth requires highenergy metabolism and the IAA is an end artery with minimal collaterals from the otic capsule so the labyrinth is especially vulnerable to ischemia [18,19,22]. By contrast, the retrocochlear acoustic nerve has an abundant collateral blood supply arising from the lateral medullary artery, arteries supplying adjacent dura matter and petrous bone, and the inferior lateral pontine artery [18,23,24]. Overall, recent prospectively gathered evidence suggests that the inner ear is a commonly affected site during AICA territory ischemia, as well as, the brainstem although current imaging techniques including MRI did not permit the visualization of the inner ear. 6. Vestibular dysfunction in AICA territory infarction With AICA territory infarction, the most common pattern of vestibular dysfunction is a combination of peripheral (i.e., unilateral CP), and central signs (e.g., asymmetrically impaired smooth pursuit, bidirectional gaze-evoked nystagmus, or impaired modulation of the vestibular responses using visual input) that was observed in approximately 65% (53/82) of a large series of consecutive cases [16]. These findings occur because the AICA supplies peripheral vestibular structures such as the inner ear and vestibulocochlear nerve, in addition to central vestibular structures [5,7]. Because AICA supplies both peripheral and central vestibular structures, the site(s) responsible for producing vertigo with AICA infarction is difficult to determine in an individual patient. However, most patients with AICA infarction have a unilateral decrease to CP, suggesting dysfunction of the peripheral vestibular structures at least in part. Occasionally, patients with vertigo have normal caloric responses, in which case the vertigo likely originates from ischemia to central vestibular structures.
8. Clinical implication of a broad spectrum of audiovestibular loss in AICA territory infarction When patients with risk factors for stroke developed acute onset of isolated prolonged vertigo without accompanying hearing loss or other neurological symptoms, ischemic damage to the superior vestibular labyrinth due to anterior vestibular artery (AVA) infarction is reasonably suspected because the lumen of the AVA is small and has little collateral circulation [18,19,22]. A previous report [18] also supported this assumption because approximately 50% of patients with isolated episodic vertigo of a vascular cause (i.e., vertebrobasilar insufficiency) had unilateral CP, which is commonly localized to the inner ear (i.e., superior vestibular labyrinth). However, recent finding did not support this assumption because only four (5%) patients showed isolated vestibular labyrinthine involvement at the time of AICA infarction [16]. Thus, although isolated AVA infarction may serve as a mechanism of isolated vascular vertigo, the incidence would be low. Isolated involvement of the cochlea was also an uncommon manifestation of AICA infarction, which was observed in only 3% of patients [16]. Unlike inner ear dysfunction of a viral cause, which can commonly present as an isolated vestibular (i.e., vestibular neuritis) or cochlear loss (i.e., sudden deafness), labyrinthine dysfunction of a vascular cause rarely results in isolated loss of vestibular or auditory function. Thus, when sudden onset of isolated prolonged vertigo or hearing loss occurred in patients with vascular risk factors, vascular compromise to the inner ear was less likely considered. However, when the combined audiovestibular loss occurred in patients with prolonged vertigo, the vascular cause was highly suspected.
7. Spectrum of audiovestibular loss in AICA territory infarction (Table 1) Nearly all patients (80/82, 98%) with AICA infarction have acute prolonged (more than 24 h) vertigo and vestibular dysfunction of peripheral, central, or combined origin [16]. So far, there are eight subgroups of AICA territory infarction according to the pattern of neuro-otological presentations [16,25]. First (group 1), acute prolonged vertigo with audiovestibular loss is the most common subgroup of audiovestibular dysfunction in AICA territory infarction. Second (group 2), acute prolonged vertigo but without documented audiovestibular loss is also a common presentation in AICA territory infarction. In this condition, vertigo originates from dysfunction of the central vestibular structure. Third
Table 1 Spectrums of audiovestibular loss in AICA territory infarction.
Presented with vertigo Combined audiovestibular loss Normal audiovestibular function Prodromal audiovestibular disturbance Isolated SNHL (normal caloric and VEMPs responses) Isolated CP (normal hearing and VEMPs responses) Isolated VEMPs abnormality (normal caloric and VEMPs responses) Associated with other neurological symptoms or signs
Group 1
Group 2
Group 3
Group 4
Group 5
Group 6
Group 7
Group 8
+ + − − − − − +
+ − + − − − − +
+ + − + − − − +
+ − − − + − − +
+ − − − − + − +
+ − − − − − + +
+ + − − − − − −
− − + − − − − +
AICA: anterior inferior cerebellar artery; SNHL: sensorineural hearing loss; CP: canal paresis; VEMPs: vestibular evoked myogenic potentials.
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Fig. 3. Schematic diagram of the patterns of inner ear involvement in AICA territory infarction according to type of involved artery. A. The arterial supply to the inner ear. B. Internal auditory artery occlusion results in combined loss of cochlear and vestibular functions (i.e., SNHL, CP, and abnormal VEMP). C. Main cochlear artery occlusion causes selective loss of cochlear function (isolated SNHL). D. Anterior vestibular artery occlusion causes selective loss of superior vestibular function (isolated CP only). E. Posterior vestibular artery occlusion causes selective loss of inferior vestibular function (abnormal VEMP only). F. No involvement of the internal auditory artery results in normal cochlear and vestibular functions. Hatched region indicates area of lesion. SNHL: sensorineural hearing loss, CP: canal paresis, VEMP: vestibular evoked myogenic potentials.
9. Long-term outcome of audiovestibular loss with CP and SNHL In audiovestibular loss of a vascular cause, it was previously thought that hearing loss is usually permanent, but dizziness and
imbalance gradually improve with central compensation. However, a recent report [20] showed that most patients (17/21, 81%) with labyrinthine infarction after at least 1 year follow-up showed improved hearing loss partially or completely. A recovery rate of 81% is above
Fig. 4. MRI and progress of audiovestibular dysfunction in a patient with AICA territory infarction who had severe hearing loss initially, but showed normal hearing level on the last follow-up. A. Axial diffusion-weighted MRI demonstrates acute infarcts involving the right middle cerebellar peduncle. B. Initial pure tone audiogram reveals severe hearing loss (80 dB) with 40% speech discrimination in the right ear. Hearing levels in decibels (dB) (American National Standards Institute, 1989) are plotted against stimulus frequency on a logarithmic scale. C. Initial video-oculographic recordings of bithermal caloric tests disclose the left CP (84%). D. Follow-up testing performed 4 years after the onset of symptoms shows a complete recovery of hearing loss in the right ear. E. Follow-up caloric test performed 4 years after the onset of symptoms also shows normal caloric response on the left side. AICA, anterior inferior cerebellar artery; CP, canal paresis; Vmax, maximal velocity of slow phase of nystagmus.
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Fig. 5. MRI and progress of audiovestibular dysfunction in a patient with AICA territory infarction who had profound hearing loss at initial and last follow-up. A. Axial diffusionweighted MRI demonstrates acute infarcts involving the right middle cerebellar peduncle and right anterior cerebellar hemisphere. B. Initial pure tone audiogram reveals profound hearing loss on the right side. Hearing levels in decibels (dB) (American National Standards Institute, 1989) are plotted against stimulus frequency on a logarithmic scale. C. Initial video-oculographic recordings of bithermal caloric tests show a right CP (64%). D. Follow-up testing performed 6 years after the onset of symptoms shows persistent hearing loss with no interval change. E. Follow-up caloric test performed 6 years after the onset of symptoms shows normal caloric responses on the right side. AICA, anterior inferior cerebellar artery; CP, canal paresis; Vmax, maximal velocity of slow phase of nystagmus.
the spontaneous recovery rate (40%–69%) reported for idiopathic SNHL [26,27], but is similar to the recovery rate (61%–89%) of idiopathic SNHL after steroid treatment [28–30]. Although there are no systematic studies on factors predicting poor outcome in patients with SNHL of a vascular cause, the improvement rate of hearing loss in patients with profound hearing loss was significantly lower than that in patients with less than profound hearing loss (40% vs 94%) [20]. This is consistent with previous studies focusing on idiopathic sudden SNHL [31–33]. Similar to hearing loss of a vascular cause, CP of a vascular cause may also be normalized. A recent paper [34] showed that 67% of patients with CP associated with posterior circulation ischemic stroke after at least 1 year follow-up showed normalized caloric response. Furthermore, all patients after more than 5 years follow-up after the onset of vertigo showed normalized caloric response [34]. Overall, recent data suggests that audiovestibular loss associated with posterior circulation ischemic stroke often has a good long-term outcome. Illustrative cases of good outcome with complete recovery of audiovestibular loss and poor outcome with no recovery of SNHL of a vascular cause are shown in Figs. 4 and 5, respectively. Conflict of interest I have no conflict of interest. References [1] Lee H, Sohn SI, Jung DK, Cho YW, Lim JG, Yi SD, et al. Sudden deafness and anterior inferior cerebellar artery infarction. Stroke 2002;33:2807–12. [2] Lee H. Neuro-otological aspects of cerebellar stroke syndrome. J Clin Neurol 2009;5:65–73. [3] Adams RD. Occlusion of the anterior inferior cerebellar artery. Arch Neurol Psychiatry 1943;49:765–70.
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