Journal of the Neurological Sciences 338 (2014) 23–29
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Review article
Recent advances in acute hearing loss due to posterior circulation ischemic stroke Hyung Lee ⁎ Department of Neurology, Keimyung University School of Medicine, Daegu, South Korea Brain Research Institute, Keimyung University School of Medicine, Daegu, South Korea
a r t i c l e
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Article history: Received 16 November 2013 Received in revised form 28 December 2013 Accepted 31 December 2013 Available online 10 January 2014 Keywords: Hearing loss Vertigo Audiovestibular loss Stroke Vertebrobasilar territory Clinical implication
a b s t r a c t Acute hearing loss (AHL) has traditionally been considered to be a neglected and underestimated symptom of stroke. However, because the blood supply to the auditory system originates from the vertebrobasilar system, stroke in the distribution of the vertebrobasilar circulation can present with acute hearing loss (AHL) and/or tinnitus. Approximately one-tenth of vertebrobasilar ischemic stroke (VBIS) is accompanied by AHL. Sometimes, AHL is a warning symptom of impending VBIS (mainly in the anterior inferior cerebellar artery). In this case, the MRI is normal, and the clinician must rely on other clinical features to make the diagnosis. This review summarizes the current advances in the clinical syndromes and signs of AHL due to VBIS. © 2014 Elsevier B.V. All rights reserved.
Contents 1. 2. 3.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Vascular mechanism of AHL of a vascular cause . . . . . . . . . . . . . . . . . Lesion site of stroke in vascular AHL . . . . . . . . . . . . . . . . . . . . . . . 3.1. AHL due to inner ear infarction with normal MRI . . . . . . . . . . . . . 3.2. AHL associated with AICA territory infarction on brain MRI . . . . . . . . . 3.3. AHL associated with non-AICA territory infarction on brain MRI . . . . . . . 4. Frequency and characteristics of AHL due to VBIS . . . . . . . . . . . . . . . . . 5. Spectrum and clinical implication of audiovestibular loss associated with AICA territory 6. Clinical implication of isolated vascular AHL . . . . . . . . . . . . . . . . . . . 7. Prevalence of stroke in ISHL . . . . . . . . . . . . . . . . . . . . . . . . . . 8. Long-term outcome and factors predicting poor outcome of AHL in VBIS . . . . . . 9. How we can differentiate vascular AHL from ISHL? . . . . . . . . . . . . . . . . 10. Therapeutic implication of isolated AHL presumably of a vascular cause . . . . . . . 11. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction Hearing impairment, the most common sensory disability worldwide, has a profound effect on one's ability to function at a personal, ⁎ Department of Neurology, Keimyung University School of Medicine, 194 Dongsan dong, Daegu 700–712, South Korea. Tel.: +82 53 250 7835; fax: +82 53 250 7840. E-mail address: [email protected]. 0022-510X/$ – see front matter © 2014 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.jns.2013.12.048
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social, and occupational level. Many different conditions cause hearing impairment including inflammation, trauma, aging (presbycusis), ototoxic drugs, genetic disorders, and stroke [1]. Because the blood supply to the auditory system originates from the vertebrobasilar system, hearing loss and/or vertigo also are common with vertebrobasilar ischemic stroke (VBIS) [2,3]. Acute hearing loss (AHL) has been associated with approximately one-tenth of posterior circulation ischemic strokes [4]. Thus, it is important to differentiate
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H. Lee / Journal of the Neurological Sciences 338 (2014) 23–29
vascular AHL from idiopathic sudden hearing loss (ISHL, sudden deafness), as the therapeutic strategy and prognosis differ between these two conditions. Sometimes, AHL and/or tinnitus are warning symptoms of impending VBIS [3,5–10]. 2. Vascular mechanism of AHL of a vascular cause The internal auditory artery (IAA), a principal artery responsible for AHL, irrigates the peripheral auditory system including the inner ear. IAA is usually originated from the anterior inferior cerebellar artery (AICA), which is constantly originated from the basilar artery [2,3]. Because territorial strokes of the AICA have commonly been associated with basilar artery branch occlusive disease [11,12], AHL is usually caused by the thrombotic narrowing of the AICA, or the basilar artery at the orifice of the AICA. By this mechanism, decreased blood flow in the affected AICA might cause either a transient episode of selective ischemia to the inner ear, resulting in isolated prodromal AHL and/or vertigo, or permanent damage to the widespread areas involving the middle cerebellar peduncle, lateral pons, and anterior cerebellum, resulting in AHL and prolonged vertigo in addition to other central symptoms and signs. Hematologic diseases and vasculitis also give rise to AHL, reflecting hypercoagulation state and alteration of microcirculation in the inner ear. These conditions include leukemia, sickle cell anemia, polycythemia, macroglobulinemia, Susac syndrome, and Berger's disease [13,14]. Rarely, small emboli originating from the dissection in the vertebral artery lodge in the main cochlear artery or IAA causing cochlear infarction with AHL or labyrinthine infarction with AHL and vertigo, respectively [15,16]. 3. Lesion site of stroke in vascular AHL 3.1. AHL due to inner ear infarction with normal MRI As described above, occlusion of the IAA causes a loss of auditory and vestibular function (i.e., audiovestibular loss), resulting in AHL and vertigo, so-called labyrinthine infarction (i.e., inner ear infarction). The labyrinth requires high-energy metabolism, and the IAA is an end artery with minimal collaterals from the otic capsule; thus the labyrinth is particularly vulnerable to ischemia [17–19]. By contrast, the retrocochlear acoustic nerve has an abundant collateral blood supply derived from the arteries that supply the adjacent dura matter and petrous bone, inferior lateral pontine artery, and lateral medullary artery [20–23]. Because the inner ear is not well visualized on the routine MRI, a definitive diagnosis of labyrinthine infarction is not possible without a further pathological examination. The apical region of the cochlea is particularly vulnerable to vascular injury, and, thus, low-frequency hearing loss is common with ischemia of the inner ear [17,24]. Sometimes, patients with AICA infarction have isolated recurrent vertigo, fluctuating hearing loss, or tinnitus (similar to Meniere's disease) as initial symptoms at 1–10 days prior to permanent infarction [3]. Labyrinthine infarction should be considered in older patients with sudden onset of unilateral hearing loss and vertigo, particularly if there is a history of stroke or known vascular risk factors. Because the current methods for diagnosing labyrinthine infarction are not adequate (including MRI), clinicians should consider all of the clinical evidence when attempting to determine the etiology of the acute audiovestibular syndrome rather than emphasizing that MRI is the best way to distinguish viral from vascular etiology [25]. 3.2. AHL associated with AICA territory infarction on brain MRI The most commonly infarcted territory on brain MRI associated with AHL is in the distribution of the AICA since the IAA, a principal artery for vascular supply to the inner ear, mostly originates from the AICA [2,3,20–22]. The involvement of the lateral inferior pons and middle
cerebellar peduncle is a radiological hallmark for the diagnosis of the AICA infarction. Although AHL can present as a sign of AICA infarction, the incidence differs in the few series reported in the literature, from a low of 30% [11] to a high of 100% [26]. In general, neurologists have not included the audiogram as a routine diagnostic tool for the evaluation of AICA infarction. Furthermore, patients might not be aware of their hearing loss during an attack of vertigo and vomiting when the unilateral hearing loss is mild or the associated vertigo is severe [2,3,17]. These factors explain the variable incidence of AHL in previous reports of AICA stroke. When a labyrinthine infarction occurs, infarction of the brainstem and/or cerebellum in the territory of the AICA is usually associated [2,11,12,27]. Theoretically, infarction of the lateral pontomedullary region including the root entry zone of the eighth nerve and the cochlear nucleus could also cause a unilateral AHL. Because these structures receive a rich blood supply from multiple sources [20,21], isolated focal infarction in these areas would be unusual. Indeed, there are no reports of AHL due to focal infarction in the root entry zone of the eighth nerve. AICA infarction rarely causes AHL and vertigo without brainstem or cerebellar signs, in which case a small infarct may be still be seen on brain MRI [6]. Thus, clinicians should be aware of the possibility of AICA infarction, particularly in older patients with AHL and vascular risk factors, even when classic brainstem or cerebellar signs are absent. 3.3. AHL associated with non-AICA territory infarction on brain MRI As a general rule, posterior inferior cerebellar artery (PICA) territory ischemia does not produce auditory symptoms because the PICA does not typically perfuse any of the auditory pathways. However, PICA infarction can rarely be associated with AHL since the IAA sometimes originates from the PICA or directly from the basilar artery [28]. Mazzoni [20] described a PICA origin of the labyrinthine artery in 3 out of 100 temporal bone dissections. Several case reports of AHL associated with infarction in the non-AICA territory have been reported [29,30]. A recent report showed that one percent (7 of 685) of the patients with VBIS had AHL associated with non-AICA territory VBIS, in which PICA territory cerebellar infarction (5/7: 71%) was the most commonly affected territory [31]. Although the site of injury responsible for AHL in these patients cannot be confirmed without pathological examination, auditory function testing indicated a cochlear site of injury in most cases [31]. 4. Frequency and characteristics of AHL due to VBIS There were several reports on the frequency of AHL associated with VBIS. In a retrospective analysis of patients with VBIS, approximately 1.4% (7/503) of the patients had bilateral hearing loss, documented by audiometric examination [32]. Among these patients, all but one individual initially presented with bilateral hearing loss and another individual developed bilateral hearing loss as a delayed manifestation during hospitalization. In another retrospective analysis of patients with vertebrobasilar insufficiency, approximately 15% (15/70) of the patients had AHL documented by audiometric examination [33]. Hearing loss was unilateral in all cases and the cochlea was the site responsible for AHL in most case [33]. In a study focused on the patients with AHL, 1.2% (4/333) of the patients had acute VBIS involving the cerebellum or brainstem at the attack of AHL [34]. Notably, all but one had bilateral hearing loss and canal paresis (CP) to caloric stimulation found in only half of the patients. Hearing loss is commonly accompanied by delayed neurological deficits, and patients complained of occipital or nuchal pain [34]. In a prospective study of patients with VBIS documented by brain MRI, approximately 8% (29/364) of the patients presented with AHL [4]. Hearing loss was mostly unilateral (27/29), and vertigo and CP to caloric stimulation were also observed in most patients. In 31% of the patients (9/29), isolated hearing loss was the initial presenting symptom, up to 10 days before the onset of other symptoms. In
H. Lee / Journal of the Neurological Sciences 338 (2014) 23–29
nearly half of the patients (14/29), hearing loss resulted from ischemia to the inner ear, based on the cochlear auditory pattern on audiometry and the accompanying ipsilateral CP to caloric stimulation. Although these studies were somewhat different in terms of the inclusion criteria of studied group, frequency of accompanied vestibular involvement (i.e., vertigo or CP), and laterality (i.e., unilateral or bilateral) of hearing loss, these data suggest that some proportion (1.2%–21%) of patients with VBIS had AHL at initial presentation and AHL was mostly due to ischemia to the inner ear. The frequency and characteristics of AHL due to VBIS are summarized in Table 1. 5. Spectrum and clinical implication of audiovestibular loss associated with AICA territory [35] There are currently eight subgroups of AICA territory infarction according to the pattern of neuro-otological presentations [27,36]. Group 1 involves acute prolonged vertigo with audiovestibular loss, representing the most common subgroup of audiovestibular dysfunction in AICA territory infarction. Group 2 involves acute prolonged vertigo but without documented audiovestibular loss, which is also commonly presented in AICA territory infarction, where the vertigo reflects a dysfunction of the central vestibular structure. Group 3 involves acute prolonged vertigo with audiovestibular loss, a condition that is occasionally preceded by an episode(s) of transient vertigo/auditory disturbance, which is considered as a prodromal sign of impending AICA territory infarction. Group 4 involves AICA infarction, which is rarely presented with acute prolonged vertigo, and isolated auditory loss without vestibular loss (i.e., AHL without CP). Group 5 involves AICA infarction, which is rarely presented with acute prolonged vertigo, and isolated superior vestibular loss without auditory loss (i.e., CP without AHL). Group 6 involves AICA infarction, which is 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 AHL). Group 7 involves AICA infarction, which is rarely presented with acute prolonged vertigo, and isolated audiovestibular loss without any other neurological symptoms. Group 8 involves AICA infarction, which is rarely presented with nonvestibular symptoms, including tingling sensation on the face and/or extremities, gait ataxia, or cerebellar dysmetria and normal audiovestibular function. The spectrum of audiovestibular loss in AICA territory infarction is summarized in Table 2. Overall, AICA territory infarction can produce a broad spectrum of neuro-otological presentations, in
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which the most common pattern of audiovestibular dysfunctions is the combined loss of auditory and vestibular function. The selective loss of vestibular or cochlear function is infrequently observed. Vascular compromise to the inner ear typically gives rise to combined auditory and vestibular loss, while viral involvement of the inner ear commonly presents as an isolated vestibular (i.e., vestibular neuritis) or cochlear (i.e., ISHL) loss. Thus, when the sudden onset of isolated prolonged vertigo or hearing loss is occurred in patients with vascular risk factors, vascular compromise to the inner ear is less likely considered. However, when combined audiovestibular loss is occurred in patients with prolonged vertigo, the vascular cause is highly suspected. However, there are exceptions to this rule, so one must rely on other clinical features (e.g. age, vascular risk factors, auditory, and vestibular test results) to differentiate vascular from viral audiovestibular syndromes [1]. 6. Clinical implication of isolated vascular AHL When AHL or vertigo is associated with other brainstem or cerebellar signs, the diagnosis of AICA infarction is easily made. However, partial ischemia of AICA may give rise to isolated AHL or vertigo since 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 IAA [17,18]. Several reports [3,5,7,8] have indicated that AHL might indicate impending AICA territory infarction. One report [3] showed that 31% (5/16) of the patients with AICA infarction had either recurrent transient episodes or a single episode of prolonged hearing loss with or without tinnitus at 1 to 10 days before the onset of other brainstem or cerebellar symptoms. In another study [8], nine percent (4/43) of the patients with documented AICA territory infarction on brain MRI initially experienced an isolated audiovestibular symptom (i.e., AHL and vertigo) with a normal MRI. Although there are no systematic data concerning high-risk factors for impending stroke or beneficial interventions for isolated AHL, patients with prodromal AHL and vertigo 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 [2,3,27]. Thus, clinicians should consider a vascular cause in patients with AHL and vertigo, especially if the patient has vascular risk factors and vertebrobasilar compromise on brain MRA [6]. Furthermore, a normal MRI does not rule out a vascular (i.e., labyrinthine infarction) etiology
Table 1 Frequency and audiovestibular characteristics of acute hearing loss due to VBIS.
Number of patients Percentage of acute hearing loss due to VBIS among studied population Laterality unilateral bilateral Site of lesion cochlear retrocochlear unknown (possible combined) Degree of hearing loss mild moderate severe profound Percentage of vertigo Percentage of CP Kinetics (at initial presentation) plus other symptoms isolated Outcome improved (complete or incomplete), n persistent, n NA, not available; CP, canal paresis; VBIS, vertebrobasilar ischemic stroke.
Huang et al. [32]
Yamasoba et al. [33]
Sauvaget [34]
Lee and Baloh [4]
503 1.4% (7/503)
70 21% (15/70)
333 1.2% (4/333)
364 8% (21/364)
0 7
15 0
1 3
27 2
1 1 2
14 1 0
1 1 2
14 4 2
2 0 0 5 57% (4/7) NA
6 4 0 5 100% (15/15) 50% (8/15) NA
0 3 0 3 75% (3/4) 50% (2/4)
5 12 4 9 93% (14/15) 86% (25/29)
0 4
19 10
4 1
18 5
3 4 7 0
15 0
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Table 2 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. AICA: anterior inferior cerebellar artery (From Lee, [35], with permission).
[6]. At this stage, clinicians should consider a further investigation and proper managements to prevent the progression of AHL into a more widespread posterior circulation stroke, mainly in the territory of the AICA [35]. Fig. 1 illustrates the MRI findings in a patient with AHL as a prodromal sign of AICA territory infarction. The diffusion-weighted MRI was normal at the time of isolated episode of AHL and vertigo. The site of injury responsible for isolated hearing loss and vertigo was likely the inner ear or vestibular nerve. 7. Prevalence of stroke in ISHL A recent study showed that patients with ISHL had 1.64 times [(95% confidence interval (CI), 1.31 to 2.07) higher risk for stroke than patients with appendectomy during a follow-up of 5 years and 50% of these stroke occurred within the first 2 years after ISHL [37]. The authors argued that ISHL might be an early warning sign of impending stroke and ISHL patients should undergo comprehensive hematologic and neurological examinations to identify individual potentially at risk for stroke in the near future [37]. However, this study did not show any predictive factors regarding hearing loss associated with stroke. The association between ISHL and stroke was verified in another study, in which
patients with moderate to severe hearing loss had two times (95% CI, 1.20 –3.49) higher likelihood of reporting previous stroke [38]. However, unlike the previous study [37], moderate to severe age-related hearing loss did not predict incident stroke after 5-year follow-up [38]. Unlike the previous two studies emphasizing ISHL as a potential risk factor for stroke [37,38], a most recent study showed that ISHL did not increase the risk of stroke, and the average annual incidence of stroke after ISHL was comparable with that in the general population in Taiwan [39]. The authors argued that in ISHL patients with modified risk factors for stroke, efforts should be made to prevent stroke rather than ISHL [39]. In overall, the issue on whether ISHL increases the risk of stroke still remains controversial and additional studies are needed to clarify this issue. 8. Long-term outcome and factors predicting poor outcome of AHL in VBIS Little is known on long-term outcome of AHL associated with VBIS. In a prospective study of patients with AHL due to VBIS, nearly 80% of patients (17/21) who were followed for at least 1 year (mean, 18 months) had a recovery of hearing partially or completely [4]. Although there are no systematic studies on the factors predicting poor outcome
Fig. 1. MRI findings in a patient with acute hearing loss and vertigo as prodromal signs of AICA territory infarction. (A and B) Axial diffusion-weighted brain MRI performed 1 day after the onset of hearing loss and vertigo was normal. One day later, (C and D) axial diffusion-weighted MRI scans demonstrated hyperintense foci involving the left middle cerebellar peduncle, dorsolateral pons, and anterior inferior cerebellum. AICA: anterior inferior cerebellar artery.
H. Lee / Journal of the Neurological Sciences 338 (2014) 23–29
in patients with vascular AHL, 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%) [4], which is consistent with previous studies focused on ISHL [13,41,42]. Recovery rate of cochlear loss is similar to the recovery rate (70%) of vestibular loss with CP after VBIS [40]. Both studies [4,40] suggest that audiovestibular loss with AHL and CP due to VBIS exhibits a relatively better outcome than previously thought. Illustrative cases with a good outcome with a complete recovery of hearing loss and a poor outcome with a no recovery of hearing loss of a vascular cause are shown in Figs. 2 and 3, respectively.
9. How we can differentiate vascular AHL from ISHL? At present, the differentiation of AHL due to VBIS from ISHL mostly depends on careful history and detailed examination. The history is the key cornerstone in differentiating these two conditions. For example, for a young patient who had a history of viral infection such as, URI, before onset of AHL, ISHL of a viral cause is most likely considered. By contrast, the presence of vascular risk factors may move the likely diagnosis towards a vascular cause. Neurological examination may also facilitate the differentiation of these two conditions. When AHL has occurred as a component of a larger neurological syndrome with brainstem or cerebellar signs, AHL of a vascular cause (i.e., AHL due to VBIS) is highly suggested. Compared with ISHL, AHL of a vascular cause exhibits several unique features. First, vascular AHL causes commonly accompanied the combined loss of vestibular function with acute vertigo or CP to caloric stimulation without reference to the severity of hearing loss [2,27], whereas vertigo occurred in only a small portion (15 to 30%) of patients with ISHL and was more prevalent in patients with profound hearing loss [41,43]. Second, although vertigo or CP is a well-known factor of poor outcome after ISHL [13,41,43,44], it is not considered to be an indicator
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of a poor outcome in vascular AHL because most patients with AHL due to VBIS had vertigo and CP to caloric stimulation [2,27]. Third, the most commonly infarcted territory on brain MRI associated with AHL was in the distribution of AICA. Without pathological confirmation, it is impossible to precisely determine the cause of AHL. Thus, clinician should have a careful attention to seek a clinical clue for differentiating AHL of a vascular cause from the ISHL. We need a further research to determine clinical predictors of ischemic versus viral cause and also tests to prove it. 10. Therapeutic implication of isolated AHL presumably of a vascular cause Although vascular AHL has a benign prognosis, vascular AHL may sometimes result from emboli originating from the greater vessels [15,16], and recurrent emboli may need to be treated. A large vertebrobasilar embolic infarction usually has a grave prognosis with coma and death [45–47]. Furthermore, isolated AHL of a vascular cause with or without accompanying vertigo can occasionally present as a prodromal sign of an impending pontocerebellar infarction [3,5–10]. In terms of treatment, it is reasonable to orally administer aspirin (provided a computed tomography brain scan has excluded intracranial hemorrhage), unless a vascular etiology is determined as unlikely [48]. Provided a vascular etiology is not confirmed, on current limited evidence, a tapering dose of oral steroids is indicated [48]. There is a real need for more randomized trials before other potential therapies can be recommended. 11. Conclusions Because the blood supply to the auditory system originates from the vertebrobasilar system, VBIS can present with AHL and/or vertigo. AHL
Fig. 2. MRI and progress of acute hearing loss in a patient with AICA territory infarction who initially had moderate hearing loss, but showed a normal hearing level on the last follow-up. (A) Axial diffusion-weighted MRI demonstrated acute infarct involving the AICA territory including the left middle cerebellar peduncle. (B) Initial pure tone audiogram revealed a moderate degree of hearing loss on the left side, but follow-up pure tone audiogram performed 3 years after the onset of symptoms showed a normal hearing level on the left 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 disclosed the left CP (100%), but follow-up caloric test performed 3 years after the onset of symptoms showed a normal caloric response on the left side. Vmax = maximal velocity of slow phase of nystagmus; AICA = anterior inferior cerebellar artery; CP = canal paresis; DP = directional preponderance.
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Fig. 3. MRI and progress of acute hearing loss in a patient with cerebellar infarction who had profound hearing loss at the initial and last follow-up. (A) Axial diffusion and T2-weighted MRIs demonstrated acute infarcts involving the PICA and AICA territories including the right entire cerebellar hemisphere and middle cerebellar peduncle. (B) Initial pure tone audiogram revealed profound hearing loss on the left side and follow-up pure tone audiogram performed 10 years after the onset of symptoms showed persistent profound hearing loss with no interval change. 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 disclosed the right CP (44%), but follow-up caloric test performed 10 years after the onset of symptoms showed a normal caloric response on the right side. Vmax = maximal velocity of slow phase of nystagmus; AICA = anterior inferior cerebellar artery; PICA = posterior inferior cerebellar artery; CP = canal paresis DP = directional preponderance.
is an important sign for the diagnosis of the AICA territory infarction and sometimes, it appears as a warning sign of impending VBIS. Clinicians should consider a vascular cause in a patient with both AHL and vertigo, especially if the patient has vascular risk factors and vertebrobasilar compromise on brain MRA. Unlike ISHL of a viral cause, AHL of a vascular cause is commonly accompanied by a vestibular involvement with acute vertigo and CP to caloric stimulation. Long-term outcome of AHL due to VBIS is often a relatively better outcome than previously suggested. References [1] Caplan LR, van Gijn Jan. Stroke syndromes. 3rd ed. New York, NY: Cambridge University Press; 2013. [2] 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. [3] Lee H, Cho YW. Auditory disturbance as a prodrome of anterior inferior cerebellar artery infarction. J Neurol Neurosurg Psychiatry 2003;74:1644–8. [4] Lee H, Baloh RW. Sudden deafness in vertebrobasilar ischemia: clinical features, vascular topographical patterns, and long-term outcome. J Neurol Sci 2005;228:99–104. [5] Lee H, Whitman GT, Lim JG, Lee SD, Park YC. Bilateral sudden deafness as a prodrome of anterior inferior cerebellar artery infarction. Arch Neurol 2001;58:1287–9. [6] Yi HA, Lee SR, Lee H, Ahn BH, Park BY, Whitman GT. Sudden deafness as a sign of stroke with normal diffusion-weighted brain MRI. Acta Otolaryngol 2005;125:1119–21. [7] Lee H, Kim HJ, Koo JW, Kim JS. Progression of acute cochleovestibulopathy into anterior inferior cerebellar artery infarction. J Neurol Sci 2009;278:119–22. [8] Kim JS, Cho KH, Lee H. Isolated labyrinthine infarction as a harbinger of anterior inferior cerebellar artery territory infarction with normal diffusion-weighted brain MRI. J Neurol Sci 2009;278:82–4. [9] Chiang CI, Chou CH, Hsueh CJ, Cheng CA, Peng GS. Acute bilateral hearing loss as a "worsening sign" in a patient with critical basilar artery stenosis. J Clin Neurosci 2013;20:177–9. [10] Ohki M, Tanaka K. An isolated vestibulocochlear symptom preceding brainstem infarction due to basilar artery occlusion. Otol Neurotol 2012;33:730–2. [11] Amarenco P, Hauw J-J. Cerebellar infarction in the territory of the anterior and inferior cerebellar artery. Brain 1990;113:139–55.
[12] Amarenco P, Rosengart A, Dewitt LD, Pessin MS, Caplan LR. Anterior inferior cerebellar artery territory infarcts. Mechanism and clinical features. Arch Neurol 1993;50:154–61. [13] Tamhankar M, Solomon D. Acute hearing loss. Curr Treat Options Neurol 2004;6:55–65. [14] Kim HA, Yi HA, Chang HW, Do YR, Lee H. Bilateral audiovestibular loss as an initial manifestation of CML. Neurol Sci 2013. http://dx.doi.org/10.1007/s10072-0131556-9. [15] Raupp SF, Jellema K, Sluzewski M, de Kort PL, Visser LH. Sudden unilateral deafness due to a right vertebral artery dissection. Neurology 2004;62:1442. [16] Choi KD, Chun JU, Han MG, Park SH, Kim JS. Embolic internal auditory artery infarction from vertebral artery Dissection. J Neurol Sci 2006;246:169–72. [17] Oas JG, Baloh RW. Vertigo and the anterior inferior cerebellar artery syndrome. Neurology 1992;42:2274–9. [18] Kim JS, Lopez I, DiPatre PL, Liu F, Ishiyama A, Baloh RW. Internal auditory artery infarction: clinical-pathologic correlation. Neurology 1999;52:40–4. [19] Kim JS, Lee H. Vertigo due to posterior circulation stroke. Semin Neurol 2013;33:179–84. [20] Mazzoni A. Internal auditory canal. Arterial relations at the porus acusticus. Ann Otol Rhinol Laryngol 1969;78:797–814. [21] Kim HN, Kim YH, Park IY, Kim GR, Chung IH. Variability of the surgical anatomy of the neurovascular complex of the cerebellopontine angle. Ann Otol Rhinol Laryngol 1990;99:288–96. [22] Kim JS, Lee H. Inner ear dysfunction due to vertebrobasilar ischemic stroke. Semin Neurol 2009;29:534–40. [23] Kim HA, Lee H. Recent advances in central acute vestibular syndrome of a vascular cause. J Neurol Sci 2012;321:17–22. [24] Lee H, Yi HA, Baloh RW. Sudden bilateral simultaneous deafness with vertigo as a sole manifestation of vertebrobasilar insufficiency. J Neurol Neurosurg Psychiatry 2003;74:539–41. [25] Kim HA, Lee SR, Lee H. Acute peripheral vestibular syndrome of a vascular cause. J Neurol Sci 2007;254:99–101. [26] Matsushita K, Naritomi H, Kazui S, Watanabe Y, Okazaki H, Kuriyama Y, et al. Infarction in the anterior inferior cerebellar artery territory: magnetic resonance imaging and auditory brain stem responses. Cerebrovasc Dis 1993;3:206–12. [27] Lee H, Kim JS, Chung EJ, Yi HA, Chung IS, Lee SR, et al. Infarction in the territory of anterior inferior cerebellar artery: spectrum of audiovestibular loss. Stroke 2009;40:3745–51.
H. Lee / Journal of the Neurological Sciences 338 (2014) 23–29 [28] Sunderland S. The arterial relations of the internal auditory meatus. Brain 1945;68:23–7. [29] Lownie SP, Parnes LS. Isolated vestibulocochlear dysfunction of central vascular origin. Laryngoscope 1991;101:1339–42. [30] Doyle KJ, Fowler C, Starr A. Audiological findings in unilateral deafness resulting from contralateral pontine infarct. Otolaryngol Head Neck Surg 1996;114:482–6. [31] Lee H. Sudden deafness related to posterior circulation infarction in the territory of the nonanterior inferior cerebellar artery: frequency, origin, and vascular topographical pattern. Eur Neurol 2008;59:302–6. [32] Huang MH, Huang CC, Ryu SJ, Chun NS. Sudden bilateral hearing impairment in vertebrobasilar occlusive disease. Stroke 1993;24:132–7. [33] Ymasoba T, Kikuchi S, Higo R. Deafness associated with vertebrobasilar insufficiency. J Neurol Sci 2001;187:69–75. [34] Sauvaget E, Kici S, Petelle B, Kania R, Chabriat H, Herman Ph, et al. Vertebrobasilar occlusive disorders presenting as sudden SNHL. Laryngoscope 2004;114:327–32. [35] Lee H. Audiovestibular loss in anterior inferior cerebellar artery territory infarction: a window to early detection? J Neurol Sci 2012;313:153–9. [36] Ahn BH, Kim HA, Yi HA, Oh SY, Lee H. Abnormal cervical vestibular-evoked myogenic potential in anterior inferior cerebellar artery territory infarction: Frequency, pattern, and a determinant. J Neurol Sci 2011;307:114–9. [37] Lin HC, Chao PZ, Lee HC. Sudden sensorineural hearing loss increases the risk of stroke: a 5-year follow-up study. Stroke 2008;39:2744–8.
29
[38] Gopinath B, Schneider J, Rochtchina E, Leeder SR, Mitchell P. Association between age-related hearing loss and stroke in an older population. Stroke 2009;40:1496–8. [39] Chang CF, Kuo YL, Chen SP, Wang MC, Liao WH, Tu TY, et al. Relationship between idiopathic sudden sensorineural hearing loss and subsequent stroke. Laryngoscope 2013;123:1011–5. [40] Lee H, Yi HA, Chung IS, Lee SR. Long-term outcome of canal paresis of a vascular cause. J Neurol Neurosurg Psychiatry 2011;82:105–9. [41] Nakashima T, Yanagita N. Outcome of sudden deafness with and without vertigo. Laryngoscope 1993;103:1145–9. [42] Zadeh MH, Storper IS, Spitzer JB. Diagnosis and treatment of sudden-onset sensorineural hearing loss: a study of 51 patients. Otolaryngol Head Neck Surg 2003;128:92–8. [43] Byl Jr FM. Sudden hearing loss: eight years' experience and suggested prognostic table. Laryngoscope 1984;94:647–61. [44] Ceylan A, Celenk F, Kemaloglu YK, Bayazit YA, Goksu N, Ozbilen S. Impact of prognostic factors on recovery from sudden hearing loss. J Laryngol Otol 2007;121:1035–40. [45] Amarenco P, Levy C, Cohen A, Touboul PJ, Roullet E, Bousser MG. Causes and mechanisms of territorial and nonterritorial cerebellar infarcts in 115 consecutive patients. Stroke 1994;25:105–12. [46] Koh MG, Phan TG, Atkinson KL, Wijdicks EF. Neuroimaging in deteriorating patients with cerebellar infarcts and mass effect. Stroke 2001;31:2062–7. [47] Choi KD, Lee H, Kim JS. Vertigo in brainstem and cerebellar strokes. Curr Opin Neurol 2013;26:90–5. [48] Mort DJ, Bronstein AM. Sudden deafness. Curr Opin Neurol 2006;19:1–3.
Contents lists available at ScienceDirect
Journal of the Neurological Sciences journal homepage: www.elsevier.com/locate/jns
Review article
Recent advances in acute hearing loss due to posterior circulation ischemic stroke Hyung Lee ⁎ Department of Neurology, Keimyung University School of Medicine, Daegu, South Korea Brain Research Institute, Keimyung University School of Medicine, Daegu, South Korea
a r t i c l e
i n f o
Article history: Received 16 November 2013 Received in revised form 28 December 2013 Accepted 31 December 2013 Available online 10 January 2014 Keywords: Hearing loss Vertigo Audiovestibular loss Stroke Vertebrobasilar territory Clinical implication
a b s t r a c t Acute hearing loss (AHL) has traditionally been considered to be a neglected and underestimated symptom of stroke. However, because the blood supply to the auditory system originates from the vertebrobasilar system, stroke in the distribution of the vertebrobasilar circulation can present with acute hearing loss (AHL) and/or tinnitus. Approximately one-tenth of vertebrobasilar ischemic stroke (VBIS) is accompanied by AHL. Sometimes, AHL is a warning symptom of impending VBIS (mainly in the anterior inferior cerebellar artery). In this case, the MRI is normal, and the clinician must rely on other clinical features to make the diagnosis. This review summarizes the current advances in the clinical syndromes and signs of AHL due to VBIS. © 2014 Elsevier B.V. All rights reserved.
Contents 1. 2. 3.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Vascular mechanism of AHL of a vascular cause . . . . . . . . . . . . . . . . . Lesion site of stroke in vascular AHL . . . . . . . . . . . . . . . . . . . . . . . 3.1. AHL due to inner ear infarction with normal MRI . . . . . . . . . . . . . 3.2. AHL associated with AICA territory infarction on brain MRI . . . . . . . . . 3.3. AHL associated with non-AICA territory infarction on brain MRI . . . . . . . 4. Frequency and characteristics of AHL due to VBIS . . . . . . . . . . . . . . . . . 5. Spectrum and clinical implication of audiovestibular loss associated with AICA territory 6. Clinical implication of isolated vascular AHL . . . . . . . . . . . . . . . . . . . 7. Prevalence of stroke in ISHL . . . . . . . . . . . . . . . . . . . . . . . . . . 8. Long-term outcome and factors predicting poor outcome of AHL in VBIS . . . . . . 9. How we can differentiate vascular AHL from ISHL? . . . . . . . . . . . . . . . . 10. Therapeutic implication of isolated AHL presumably of a vascular cause . . . . . . . 11. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction Hearing impairment, the most common sensory disability worldwide, has a profound effect on one's ability to function at a personal, ⁎ Department of Neurology, Keimyung University School of Medicine, 194 Dongsan dong, Daegu 700–712, South Korea. Tel.: +82 53 250 7835; fax: +82 53 250 7840. E-mail address: [email protected]. 0022-510X/$ – see front matter © 2014 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.jns.2013.12.048
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social, and occupational level. Many different conditions cause hearing impairment including inflammation, trauma, aging (presbycusis), ototoxic drugs, genetic disorders, and stroke [1]. Because the blood supply to the auditory system originates from the vertebrobasilar system, hearing loss and/or vertigo also are common with vertebrobasilar ischemic stroke (VBIS) [2,3]. Acute hearing loss (AHL) has been associated with approximately one-tenth of posterior circulation ischemic strokes [4]. Thus, it is important to differentiate
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H. Lee / Journal of the Neurological Sciences 338 (2014) 23–29
vascular AHL from idiopathic sudden hearing loss (ISHL, sudden deafness), as the therapeutic strategy and prognosis differ between these two conditions. Sometimes, AHL and/or tinnitus are warning symptoms of impending VBIS [3,5–10]. 2. Vascular mechanism of AHL of a vascular cause The internal auditory artery (IAA), a principal artery responsible for AHL, irrigates the peripheral auditory system including the inner ear. IAA is usually originated from the anterior inferior cerebellar artery (AICA), which is constantly originated from the basilar artery [2,3]. Because territorial strokes of the AICA have commonly been associated with basilar artery branch occlusive disease [11,12], AHL is usually caused by the thrombotic narrowing of the AICA, or the basilar artery at the orifice of the AICA. By this mechanism, decreased blood flow in the affected AICA might cause either a transient episode of selective ischemia to the inner ear, resulting in isolated prodromal AHL and/or vertigo, or permanent damage to the widespread areas involving the middle cerebellar peduncle, lateral pons, and anterior cerebellum, resulting in AHL and prolonged vertigo in addition to other central symptoms and signs. Hematologic diseases and vasculitis also give rise to AHL, reflecting hypercoagulation state and alteration of microcirculation in the inner ear. These conditions include leukemia, sickle cell anemia, polycythemia, macroglobulinemia, Susac syndrome, and Berger's disease [13,14]. Rarely, small emboli originating from the dissection in the vertebral artery lodge in the main cochlear artery or IAA causing cochlear infarction with AHL or labyrinthine infarction with AHL and vertigo, respectively [15,16]. 3. Lesion site of stroke in vascular AHL 3.1. AHL due to inner ear infarction with normal MRI As described above, occlusion of the IAA causes a loss of auditory and vestibular function (i.e., audiovestibular loss), resulting in AHL and vertigo, so-called labyrinthine infarction (i.e., inner ear infarction). The labyrinth requires high-energy metabolism, and the IAA is an end artery with minimal collaterals from the otic capsule; thus the labyrinth is particularly vulnerable to ischemia [17–19]. By contrast, the retrocochlear acoustic nerve has an abundant collateral blood supply derived from the arteries that supply the adjacent dura matter and petrous bone, inferior lateral pontine artery, and lateral medullary artery [20–23]. Because the inner ear is not well visualized on the routine MRI, a definitive diagnosis of labyrinthine infarction is not possible without a further pathological examination. The apical region of the cochlea is particularly vulnerable to vascular injury, and, thus, low-frequency hearing loss is common with ischemia of the inner ear [17,24]. Sometimes, patients with AICA infarction have isolated recurrent vertigo, fluctuating hearing loss, or tinnitus (similar to Meniere's disease) as initial symptoms at 1–10 days prior to permanent infarction [3]. Labyrinthine infarction should be considered in older patients with sudden onset of unilateral hearing loss and vertigo, particularly if there is a history of stroke or known vascular risk factors. Because the current methods for diagnosing labyrinthine infarction are not adequate (including MRI), clinicians should consider all of the clinical evidence when attempting to determine the etiology of the acute audiovestibular syndrome rather than emphasizing that MRI is the best way to distinguish viral from vascular etiology [25]. 3.2. AHL associated with AICA territory infarction on brain MRI The most commonly infarcted territory on brain MRI associated with AHL is in the distribution of the AICA since the IAA, a principal artery for vascular supply to the inner ear, mostly originates from the AICA [2,3,20–22]. The involvement of the lateral inferior pons and middle
cerebellar peduncle is a radiological hallmark for the diagnosis of the AICA infarction. Although AHL can present as a sign of AICA infarction, the incidence differs in the few series reported in the literature, from a low of 30% [11] to a high of 100% [26]. In general, neurologists have not included the audiogram as a routine diagnostic tool for the evaluation of AICA infarction. Furthermore, patients might not be aware of their hearing loss during an attack of vertigo and vomiting when the unilateral hearing loss is mild or the associated vertigo is severe [2,3,17]. These factors explain the variable incidence of AHL in previous reports of AICA stroke. When a labyrinthine infarction occurs, infarction of the brainstem and/or cerebellum in the territory of the AICA is usually associated [2,11,12,27]. Theoretically, infarction of the lateral pontomedullary region including the root entry zone of the eighth nerve and the cochlear nucleus could also cause a unilateral AHL. Because these structures receive a rich blood supply from multiple sources [20,21], isolated focal infarction in these areas would be unusual. Indeed, there are no reports of AHL due to focal infarction in the root entry zone of the eighth nerve. AICA infarction rarely causes AHL and vertigo without brainstem or cerebellar signs, in which case a small infarct may be still be seen on brain MRI [6]. Thus, clinicians should be aware of the possibility of AICA infarction, particularly in older patients with AHL and vascular risk factors, even when classic brainstem or cerebellar signs are absent. 3.3. AHL associated with non-AICA territory infarction on brain MRI As a general rule, posterior inferior cerebellar artery (PICA) territory ischemia does not produce auditory symptoms because the PICA does not typically perfuse any of the auditory pathways. However, PICA infarction can rarely be associated with AHL since the IAA sometimes originates from the PICA or directly from the basilar artery [28]. Mazzoni [20] described a PICA origin of the labyrinthine artery in 3 out of 100 temporal bone dissections. Several case reports of AHL associated with infarction in the non-AICA territory have been reported [29,30]. A recent report showed that one percent (7 of 685) of the patients with VBIS had AHL associated with non-AICA territory VBIS, in which PICA territory cerebellar infarction (5/7: 71%) was the most commonly affected territory [31]. Although the site of injury responsible for AHL in these patients cannot be confirmed without pathological examination, auditory function testing indicated a cochlear site of injury in most cases [31]. 4. Frequency and characteristics of AHL due to VBIS There were several reports on the frequency of AHL associated with VBIS. In a retrospective analysis of patients with VBIS, approximately 1.4% (7/503) of the patients had bilateral hearing loss, documented by audiometric examination [32]. Among these patients, all but one individual initially presented with bilateral hearing loss and another individual developed bilateral hearing loss as a delayed manifestation during hospitalization. In another retrospective analysis of patients with vertebrobasilar insufficiency, approximately 15% (15/70) of the patients had AHL documented by audiometric examination [33]. Hearing loss was unilateral in all cases and the cochlea was the site responsible for AHL in most case [33]. In a study focused on the patients with AHL, 1.2% (4/333) of the patients had acute VBIS involving the cerebellum or brainstem at the attack of AHL [34]. Notably, all but one had bilateral hearing loss and canal paresis (CP) to caloric stimulation found in only half of the patients. Hearing loss is commonly accompanied by delayed neurological deficits, and patients complained of occipital or nuchal pain [34]. In a prospective study of patients with VBIS documented by brain MRI, approximately 8% (29/364) of the patients presented with AHL [4]. Hearing loss was mostly unilateral (27/29), and vertigo and CP to caloric stimulation were also observed in most patients. In 31% of the patients (9/29), isolated hearing loss was the initial presenting symptom, up to 10 days before the onset of other symptoms. In
H. Lee / Journal of the Neurological Sciences 338 (2014) 23–29
nearly half of the patients (14/29), hearing loss resulted from ischemia to the inner ear, based on the cochlear auditory pattern on audiometry and the accompanying ipsilateral CP to caloric stimulation. Although these studies were somewhat different in terms of the inclusion criteria of studied group, frequency of accompanied vestibular involvement (i.e., vertigo or CP), and laterality (i.e., unilateral or bilateral) of hearing loss, these data suggest that some proportion (1.2%–21%) of patients with VBIS had AHL at initial presentation and AHL was mostly due to ischemia to the inner ear. The frequency and characteristics of AHL due to VBIS are summarized in Table 1. 5. Spectrum and clinical implication of audiovestibular loss associated with AICA territory [35] There are currently eight subgroups of AICA territory infarction according to the pattern of neuro-otological presentations [27,36]. Group 1 involves acute prolonged vertigo with audiovestibular loss, representing the most common subgroup of audiovestibular dysfunction in AICA territory infarction. Group 2 involves acute prolonged vertigo but without documented audiovestibular loss, which is also commonly presented in AICA territory infarction, where the vertigo reflects a dysfunction of the central vestibular structure. Group 3 involves acute prolonged vertigo with audiovestibular loss, a condition that is occasionally preceded by an episode(s) of transient vertigo/auditory disturbance, which is considered as a prodromal sign of impending AICA territory infarction. Group 4 involves AICA infarction, which is rarely presented with acute prolonged vertigo, and isolated auditory loss without vestibular loss (i.e., AHL without CP). Group 5 involves AICA infarction, which is rarely presented with acute prolonged vertigo, and isolated superior vestibular loss without auditory loss (i.e., CP without AHL). Group 6 involves AICA infarction, which is 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 AHL). Group 7 involves AICA infarction, which is rarely presented with acute prolonged vertigo, and isolated audiovestibular loss without any other neurological symptoms. Group 8 involves AICA infarction, which is rarely presented with nonvestibular symptoms, including tingling sensation on the face and/or extremities, gait ataxia, or cerebellar dysmetria and normal audiovestibular function. The spectrum of audiovestibular loss in AICA territory infarction is summarized in Table 2. Overall, AICA territory infarction can produce a broad spectrum of neuro-otological presentations, in
25
which the most common pattern of audiovestibular dysfunctions is the combined loss of auditory and vestibular function. The selective loss of vestibular or cochlear function is infrequently observed. Vascular compromise to the inner ear typically gives rise to combined auditory and vestibular loss, while viral involvement of the inner ear commonly presents as an isolated vestibular (i.e., vestibular neuritis) or cochlear (i.e., ISHL) loss. Thus, when the sudden onset of isolated prolonged vertigo or hearing loss is occurred in patients with vascular risk factors, vascular compromise to the inner ear is less likely considered. However, when combined audiovestibular loss is occurred in patients with prolonged vertigo, the vascular cause is highly suspected. However, there are exceptions to this rule, so one must rely on other clinical features (e.g. age, vascular risk factors, auditory, and vestibular test results) to differentiate vascular from viral audiovestibular syndromes [1]. 6. Clinical implication of isolated vascular AHL When AHL or vertigo is associated with other brainstem or cerebellar signs, the diagnosis of AICA infarction is easily made. However, partial ischemia of AICA may give rise to isolated AHL or vertigo since 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 IAA [17,18]. Several reports [3,5,7,8] have indicated that AHL might indicate impending AICA territory infarction. One report [3] showed that 31% (5/16) of the patients with AICA infarction had either recurrent transient episodes or a single episode of prolonged hearing loss with or without tinnitus at 1 to 10 days before the onset of other brainstem or cerebellar symptoms. In another study [8], nine percent (4/43) of the patients with documented AICA territory infarction on brain MRI initially experienced an isolated audiovestibular symptom (i.e., AHL and vertigo) with a normal MRI. Although there are no systematic data concerning high-risk factors for impending stroke or beneficial interventions for isolated AHL, patients with prodromal AHL and vertigo 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 [2,3,27]. Thus, clinicians should consider a vascular cause in patients with AHL and vertigo, especially if the patient has vascular risk factors and vertebrobasilar compromise on brain MRA [6]. Furthermore, a normal MRI does not rule out a vascular (i.e., labyrinthine infarction) etiology
Table 1 Frequency and audiovestibular characteristics of acute hearing loss due to VBIS.
Number of patients Percentage of acute hearing loss due to VBIS among studied population Laterality unilateral bilateral Site of lesion cochlear retrocochlear unknown (possible combined) Degree of hearing loss mild moderate severe profound Percentage of vertigo Percentage of CP Kinetics (at initial presentation) plus other symptoms isolated Outcome improved (complete or incomplete), n persistent, n NA, not available; CP, canal paresis; VBIS, vertebrobasilar ischemic stroke.
Huang et al. [32]
Yamasoba et al. [33]
Sauvaget [34]
Lee and Baloh [4]
503 1.4% (7/503)
70 21% (15/70)
333 1.2% (4/333)
364 8% (21/364)
0 7
15 0
1 3
27 2
1 1 2
14 1 0
1 1 2
14 4 2
2 0 0 5 57% (4/7) NA
6 4 0 5 100% (15/15) 50% (8/15) NA
0 3 0 3 75% (3/4) 50% (2/4)
5 12 4 9 93% (14/15) 86% (25/29)
0 4
19 10
4 1
18 5
3 4 7 0
15 0
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H. Lee / Journal of the Neurological Sciences 338 (2014) 23–29
Table 2 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. AICA: anterior inferior cerebellar artery (From Lee, [35], with permission).
[6]. At this stage, clinicians should consider a further investigation and proper managements to prevent the progression of AHL into a more widespread posterior circulation stroke, mainly in the territory of the AICA [35]. Fig. 1 illustrates the MRI findings in a patient with AHL as a prodromal sign of AICA territory infarction. The diffusion-weighted MRI was normal at the time of isolated episode of AHL and vertigo. The site of injury responsible for isolated hearing loss and vertigo was likely the inner ear or vestibular nerve. 7. Prevalence of stroke in ISHL A recent study showed that patients with ISHL had 1.64 times [(95% confidence interval (CI), 1.31 to 2.07) higher risk for stroke than patients with appendectomy during a follow-up of 5 years and 50% of these stroke occurred within the first 2 years after ISHL [37]. The authors argued that ISHL might be an early warning sign of impending stroke and ISHL patients should undergo comprehensive hematologic and neurological examinations to identify individual potentially at risk for stroke in the near future [37]. However, this study did not show any predictive factors regarding hearing loss associated with stroke. The association between ISHL and stroke was verified in another study, in which
patients with moderate to severe hearing loss had two times (95% CI, 1.20 –3.49) higher likelihood of reporting previous stroke [38]. However, unlike the previous study [37], moderate to severe age-related hearing loss did not predict incident stroke after 5-year follow-up [38]. Unlike the previous two studies emphasizing ISHL as a potential risk factor for stroke [37,38], a most recent study showed that ISHL did not increase the risk of stroke, and the average annual incidence of stroke after ISHL was comparable with that in the general population in Taiwan [39]. The authors argued that in ISHL patients with modified risk factors for stroke, efforts should be made to prevent stroke rather than ISHL [39]. In overall, the issue on whether ISHL increases the risk of stroke still remains controversial and additional studies are needed to clarify this issue. 8. Long-term outcome and factors predicting poor outcome of AHL in VBIS Little is known on long-term outcome of AHL associated with VBIS. In a prospective study of patients with AHL due to VBIS, nearly 80% of patients (17/21) who were followed for at least 1 year (mean, 18 months) had a recovery of hearing partially or completely [4]. Although there are no systematic studies on the factors predicting poor outcome
Fig. 1. MRI findings in a patient with acute hearing loss and vertigo as prodromal signs of AICA territory infarction. (A and B) Axial diffusion-weighted brain MRI performed 1 day after the onset of hearing loss and vertigo was normal. One day later, (C and D) axial diffusion-weighted MRI scans demonstrated hyperintense foci involving the left middle cerebellar peduncle, dorsolateral pons, and anterior inferior cerebellum. AICA: anterior inferior cerebellar artery.
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in patients with vascular AHL, 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%) [4], which is consistent with previous studies focused on ISHL [13,41,42]. Recovery rate of cochlear loss is similar to the recovery rate (70%) of vestibular loss with CP after VBIS [40]. Both studies [4,40] suggest that audiovestibular loss with AHL and CP due to VBIS exhibits a relatively better outcome than previously thought. Illustrative cases with a good outcome with a complete recovery of hearing loss and a poor outcome with a no recovery of hearing loss of a vascular cause are shown in Figs. 2 and 3, respectively.
9. How we can differentiate vascular AHL from ISHL? At present, the differentiation of AHL due to VBIS from ISHL mostly depends on careful history and detailed examination. The history is the key cornerstone in differentiating these two conditions. For example, for a young patient who had a history of viral infection such as, URI, before onset of AHL, ISHL of a viral cause is most likely considered. By contrast, the presence of vascular risk factors may move the likely diagnosis towards a vascular cause. Neurological examination may also facilitate the differentiation of these two conditions. When AHL has occurred as a component of a larger neurological syndrome with brainstem or cerebellar signs, AHL of a vascular cause (i.e., AHL due to VBIS) is highly suggested. Compared with ISHL, AHL of a vascular cause exhibits several unique features. First, vascular AHL causes commonly accompanied the combined loss of vestibular function with acute vertigo or CP to caloric stimulation without reference to the severity of hearing loss [2,27], whereas vertigo occurred in only a small portion (15 to 30%) of patients with ISHL and was more prevalent in patients with profound hearing loss [41,43]. Second, although vertigo or CP is a well-known factor of poor outcome after ISHL [13,41,43,44], it is not considered to be an indicator
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of a poor outcome in vascular AHL because most patients with AHL due to VBIS had vertigo and CP to caloric stimulation [2,27]. Third, the most commonly infarcted territory on brain MRI associated with AHL was in the distribution of AICA. Without pathological confirmation, it is impossible to precisely determine the cause of AHL. Thus, clinician should have a careful attention to seek a clinical clue for differentiating AHL of a vascular cause from the ISHL. We need a further research to determine clinical predictors of ischemic versus viral cause and also tests to prove it. 10. Therapeutic implication of isolated AHL presumably of a vascular cause Although vascular AHL has a benign prognosis, vascular AHL may sometimes result from emboli originating from the greater vessels [15,16], and recurrent emboli may need to be treated. A large vertebrobasilar embolic infarction usually has a grave prognosis with coma and death [45–47]. Furthermore, isolated AHL of a vascular cause with or without accompanying vertigo can occasionally present as a prodromal sign of an impending pontocerebellar infarction [3,5–10]. In terms of treatment, it is reasonable to orally administer aspirin (provided a computed tomography brain scan has excluded intracranial hemorrhage), unless a vascular etiology is determined as unlikely [48]. Provided a vascular etiology is not confirmed, on current limited evidence, a tapering dose of oral steroids is indicated [48]. There is a real need for more randomized trials before other potential therapies can be recommended. 11. Conclusions Because the blood supply to the auditory system originates from the vertebrobasilar system, VBIS can present with AHL and/or vertigo. AHL
Fig. 2. MRI and progress of acute hearing loss in a patient with AICA territory infarction who initially had moderate hearing loss, but showed a normal hearing level on the last follow-up. (A) Axial diffusion-weighted MRI demonstrated acute infarct involving the AICA territory including the left middle cerebellar peduncle. (B) Initial pure tone audiogram revealed a moderate degree of hearing loss on the left side, but follow-up pure tone audiogram performed 3 years after the onset of symptoms showed a normal hearing level on the left 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 disclosed the left CP (100%), but follow-up caloric test performed 3 years after the onset of symptoms showed a normal caloric response on the left side. Vmax = maximal velocity of slow phase of nystagmus; AICA = anterior inferior cerebellar artery; CP = canal paresis; DP = directional preponderance.
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Fig. 3. MRI and progress of acute hearing loss in a patient with cerebellar infarction who had profound hearing loss at the initial and last follow-up. (A) Axial diffusion and T2-weighted MRIs demonstrated acute infarcts involving the PICA and AICA territories including the right entire cerebellar hemisphere and middle cerebellar peduncle. (B) Initial pure tone audiogram revealed profound hearing loss on the left side and follow-up pure tone audiogram performed 10 years after the onset of symptoms showed persistent profound hearing loss with no interval change. 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 disclosed the right CP (44%), but follow-up caloric test performed 10 years after the onset of symptoms showed a normal caloric response on the right side. Vmax = maximal velocity of slow phase of nystagmus; AICA = anterior inferior cerebellar artery; PICA = posterior inferior cerebellar artery; CP = canal paresis DP = directional preponderance.
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