Anterior inferior cerebellar artery occlusion accompanied by hemorheology-documented increased blood viscosity: a case report

Introduction

Anterior inferior cerebellar artery (AICA) occlusion is a relatively rare type of posterior circulation stroke. Goodhart and Davison were the first to publish a pathological description of AICA, in 1936. ¹ Case series and reviews published thereafter have reported AICA territory infarction or AICA syndrome as a unique neurological condition. Posterior circulation includes areas supplied by the vertebral arteries, posterior inferior cerebellar arteries, basilar artery, AICA, pontine branches of the basilar artery, superior cerebellar artery, posterior cerebral artery, and posterior communicating arteries. The AICA supplies both the central and peripheral vestibular structures. Some pontine and pontopeduncular areas may also be affected by AICA occlusion, with consequent cranial nerve V and VII symptoms. AICA territory infarction commonly manifests as vertigo, ataxia, tinnitus, hearing loss, facial palsy, dysarthria, and Horner syndrome.^2–4

Because of the limited sensitivity of conventional noninvasive imaging approaches such as transcranial Doppler (TCD) or magnetic resonance angiography (MRA), the angiographic confirmation of AICA occlusion is occasionally challenging. An accurate determination of the etiology of occlusion of small arteries is difficult, largely because of the complexity of multiple contributory risk factors and triggers. Compared with conventional factors, the role of hemorheological parameters has attracted less attention in the medical community. We present a case of AICA occlusion that was not accurately diagnosed on TCD, MRA, or computed tomographic angiography (CTA); alterations in blood viscosity were implicated as an underlying trigger for the occlusion of small arteries, such as the AICA, based on substantial, long-term hemorheological changes observed in the patient.

Case presentation

A 50-year-old man presented to a local hospital for evaluation of dizziness, unsteady walk, tinnitus, and left peripheral facial palsy over 36 hours. He revealed a 30-year history of heavy smoking. He was diagnosed with hypertension by a primary physician 6 months prior to presentation; however, he did not receive any medication. Magnetic resonance imaging (1.5 Tesla) performed on the day of admission revealed a high-intensity signal on a diffusion-weighted imaging sequence and a low-intensity signal on an apparent diffusion coefficient sequence in the left cerebellar hemisphere and middle cerebellar peduncles (Figure 1). MRA indicated stenosis of the P1 segment of the left posterior cerebral artery. Routine blood examination showed slightly elevated erythrocyte (5.80 × 10¹²/L) and leukocyte (9.34 × 10⁹/L) counts and serum hemoglobin concentration, as well as elevated low-density lipoprotein cholesterol (LDL-c) and triglyceride levels. During hospitalization, no other abnormalities were observed, including liver function, renal function, glucose, electrolytes, myocardial enzymes, thyroid function, B-type natriuretic peptide, urine routine, stool routine, chest computed tomography, abdominal ultrasound, electrocardiogram, and echocardiography. The patient received appropriate medications, including aspirin, atorvastatin, and amlodipine, as well as rehabilitation exercises. However, the aforementioned symptoms persisted despite 5 days of treatment; he was therefore transferred to our hospital for further assessment and rehabilitation.

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Figure 1.

Magnetic resonance imaging scan (1.5 Tesla, diffusion-weighted imaging and apparent diffusion coefficient sequences) obtained on the day of admission.

Physical examination revealed left peripheral facial palsy and gait ataxia. We observed prominent right-sided gaze-evoked nystagmus, which did not subside after repetitive maneuvers. We did not observe any decline in cognition, language, swallowing function, or limb muscle strength. Electroaudiography revealed clear left-sided sensorineural hearing impairment. Repeat routine blood tests at our hospital continued to show elevated erythrocyte and leukocyte counts and serum hemoglobin concentration (Figure 2).

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Figure 2.

Leukocyte and erythrocyte counts, serum hemoglobin concentration, and hematocrit measured during hospitalization.

Conventional 12-lead electrocardiogram and subsequent bedside electrocardiogram monitoring showed no substantial arrhythmia or sign of ischemia. Carotid and vertebral arterial Doppler ultrasonography revealed mildly thickened intimal media without any atherosclerotic plaques. TCD with bubble test showed negative results. No significant arterial stenosis or occlusion was observed on CTA of the arteries above the aortic arch. A conventional coagulation profile was normal, as were D-dimer and protein C and S levels. Hemorheological evaluation performed on day 9 after onset revealed elevated whole blood viscosity (measured using light transmission or light reflection through/from red blood cell suspensions) at a low shear rate (22.55), with normal results at middle and high shear rates. Cerebrovascular digital subtraction angiography (DSA) performed on day 15 after onset confirmed left AICA occlusion (Figure 3). Dizziness, difficulty in maintaining balance, and facial palsy gradually improved in the patient following intensive rehabilitation in addition to acupuncture and traditional Chinese medicine in our department. The patient was discharged with residual tinnitus and hearing loss. Telephone follow-ups were conducted during the 6 months after his discharge; the patient stated that his remaining symptoms became milder but refused to undergo vascular reexamination because of financial reasons and traffic concerns.

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Figure 3.

Digital subtraction angiography scan showing the right anterior inferior cerebellar artery (AICA; arrow) and absence of the left AICA.

All treatments were administered after acquiring written consent from the patient. The reporting of this study conforms to the CARE guidelines. ⁵ Ethics approval is not required at our institution for the submission of case reports and we have received permission from the science and education department for publication. Written informed consent was obtained from the patient to publish the details of this case and for the use of his data for scientific purposes.

Discussion

In clinical practice, the accurate diagnosis of AICA territory infarction etiology is usually challenging. Branch atheromatous disease is the leading cause of AICA occlusion. Atherosclerosis and/or stenosis of the posterior circulation has been observed in most previously reported cases.^1,2,6 Furthermore, a previous study describing the angiographic characteristics of 31 patients with cerebellar infarcts reported large-artery disease and in situ branch artery disease in 28 patients; however, the other 3 patients did not have angiographically documented disease and showed small infarcts in the posterior inferior cerebellar artery, AICA, or superior cerebellar artery territories. ⁷ Kumral et al. observed large-artery atherosclerotic disease in the vertebrobasilar system of 16 of 23 patients with MRA-documented AICA territory infarction, whereas 5 patients (22%) showed normal results on arterial investigation. ⁸

Although AICA territory infarction can be established based on clinical manifestations and magnetic resonance imaging characteristics, direct angiographic features are often difficult to confirm. In the present case, MRA and CTA failed to identify AICA occlusion; MRA suggested posterior cerebral artery stenosis but this was found to be image deformation on subsequent DSA. The poor sensitivity of MRA and CTA as imaging modalities highlights the usefulness of DSA for the detection of AICA occlusion, and particularly for its accurate diagnosis in clinical research.

Blood in circulation can be described as a non-Newtonian fluid. Although several studies have observed an association between hemorheological abnormalities and stroke, this association is frequently neglected by the medical community.^9,10 Accumulating evidence suggests that increased blood viscosity is associated with major risk factors of stroke such as hypertension, diabetes, obesity, dyslipidemia, tobacco use, and aging. ¹⁰ Moreover, research has confirmed an association between hyperviscosity and increased thrombotic risk.^11,12 The Edinburgh Artery Study reported significantly elevated blood viscosity in patients with new-onset stroke, and found that blood hyperviscosity augments stroke incidence independent of risk factors including smoking habits, diastolic blood pressure, and LDL-c levels. ¹³ Notably, two Asian studies have reported that blood viscosity at admission is higher in patients with stroke secondary to small-artery occlusion than in those with stroke associated with cardioembolism and large-artery atherosclerosis.^14,15

Hematocrit, the mechanical properties of erythrocytes, and plasma viscosity are the primary determinants of whole blood viscosity;^16,17 of these, hematocrit plays a key role. ¹⁸ Many previous studies have reported that hematocrit elevation increases stroke risk after adjusting for several variables.^13,19,20 Furthermore, abnormally high hemoglobin concentrations are correlated with stroke incidence and severity,^21–24 and plasma viscosity is an important rheological variable independently associated with stroke recurrence. ²⁵

Clinical manifestations, as well as magnetic resonance imaging and angiographic findings, confirmed AICA occlusion in our patient. Notably, DSA revealed no atherosclerotic arteries except the occluded AICA, and carotid and vertebral artery Doppler ultrasonography revealed no evidence of significant atherosclerosis. The patient was hypertensive and a tobacco user; however, his serum total cholesterol level was within the reference range, with only mildly elevated triglyceride and LDL-c levels. His serum hemoglobin concentration and red and white blood cell counts remained elevated over repeated testing on many separate occasions. The patient showed no sign of dehydration; his red and white blood cell counts and serum hemoglobin concentration remained elevated after adequate fluid replenishment. Blood viscosity at a low shear rate was also elevated, even on day 11 after onset.

The Trial of ORG 10172 in Acute Stroke Treatment classification categorizes small-vessel occlusion as a subtype of acute stroke; however, small-vessel occlusion is more a phenotypic than an etiologic subtype. ²⁶ Stroke is associated with a multifactorial etiology in a relatively large proportion of patients. Although conventional risk factors are associated with a high risk of stroke, confirmation of the “trigger” is often challenging. We concluded that hemorheological changes were a key contributor to accelerated thrombosis in our patient.

Conclusions

Acute AICA occlusion is a relatively rare subtype of posterior circulation stroke; however, clinicians should remain mindful of this entity, with clinical manifestations including dizziness, ataxia, central nystagmus, tinnitus, hearing loss, and peripheral facial palsy. Notably, TCD, MRA, and CTA may fail to identify arterial occlusion. Cerebral infarction with AICA occlusion caused by hemorheological abnormalities has been rarely reported. Moreover, the importance of hemorheological changes as a factor of stroke is frequently neglected. We have therefore reported this case hoping to emphasize its relevance, especially in small-artery occlusion.