Written Case

Introduction

Intracerebral steal is a process which involves vasoconstriction within chronically under-perfused brain parenchyma that redirects blood flow. It has been identified to occur in states such as Moyamoya disease, arteriovenous malformations, and following internal carotid arterial stent placement. The pathophysiology behind this redirection of blood flow is thought to occur through the leptomeningeal arteries.  Our case report identifies how intracerebral steal in the setting of a cerebrovascular accident can present as position-dependent stroke-like symptoms.  

Case Presentation

The patient is a 55-year-old Caucasian, right-handed male with a history of current tobacco use and no encounter with a healthcare provider during the prior 20 years. One week prior to the presentation, the patient experienced one episode of right-sided facial paresthesia, disequilibrium and left upper extremity incoordination lasting 15 minutes with spontaneous resolution and no residual deficits.  At 9:15 AM on the day of presentation, he experienced an identical episode which resolved after 10 minutes.  After an additional 35 minutes without symptoms, the patient experienced two additional episodes with slurred speech and confusion in addition to prior deficits. Symptoms again resolved prior to EMS arrival by 11:00 AM.

When seen by triage in the ED at 11:32 AM, the patient had a normal neurological exam and was fully oriented. Initial vitals were HR 71, BP 158/85, RR 20, SpO2 98%, and Temp 97.2 F. Shortly after arrival, the patient experienced significant nausea with one episode of emesis. When seen by the ED physician at 11:41 AM, the patient had developed flaccid left hemiparesis, right-sided facial droop, dysarthria, and severe lateral gaze of left eye with a total NIHSS of 12. A stroke alert was then activated at 11:43 AM. Notably, the patient experienced marked resolution of symptoms when laid supine for imaging. A repeat stroke evaluation approximately 2 hours later only demonstrated mild ataxia on finger-to-nose and heel-to-shin tests in addition to vertical nystagmus on upgaze.

Diagnostic Assessment

A CTA of the head and neck with perfusion study demonstrated ischemia in the distribution of the left posterior cerebral artery, significant stenosis of the left PCA with near complete occlusion at the junction of the left P1/P2 segments, severe segmental stenosis with occlusion of the left vertebral artery and decreased flow in the left posterior inferior cerebellar artery. MRI demonstrated 6 small areas of acute diffusion restriction in the right posterior cerebral artery distribution. A transthoracic echocardiogram revealed a maintained ejection fraction with no evidence of a patent foreman ovale.  Lab evaluation was notable for elevated hemoglobin (5.7 g/dL), elevated hematocrit (50.7%), leukocytosis (14 K/CUMM), normal serum sodium (137 mmol/L), elevated serum glucose (384 mg/dL), an elevated serum osmolality (307 mOsm/kg), and a hemoglobin A1c of 11.9%.

Therapeutic Intervention

Due to the nature and extent of the patient's clinical condition, a larger center capable of thrombectomy was contacted.  The patient was started on aspirin, clopidogrel, and IV fluids with 1 L normal saline bolus followed by normal saline at 150 mL/hr. Patient was kept completely flat for 24 hours during which the patient received 3.1 L total IVF, in addition to 800 mL PO fluids, for a net balance of +2.8 L. Blood pressures ranged from 115-184/62-94 and heart rate ranged from 62 to 82 during the first 24 hours. Between 24-48 hours, the patient was allowed to sit upright with assistance for meals and to use the bedside commode. Blood pressures ranged from 118-184/59-89 and heart rate ranged from 56 to 83 with a net balance of +5.2 L at 48 hours. Between 48-72 hours, the patient was allowed to sit upright at the edge of the bed. Patient was asymptomatic by day 3 and was discharged to inpatient rehabilitation on day 5.

Follow-up and Outcomes

The patient was found to have diabetic bilateral neuropathy of the lower extremities following EMG evaluation. Low dose CT for cancer screening was notable for mild pulmonary emphysema, aortic atheromatous disease, and coronary artery calcifications. When seen approximately 2 months following discharge, the patient was largely asymptomatic except for intermittent, L-sided facial paresthesia.

Discussion

The transient deficits were consistent with posterior circulation ischemia. Of note, the observed arterial lesions were not within the basilar artery, most commonly implicated in posterior circulation infarcts [1], instead involving the L PICA, L P1-P2 segment, and the L VA. Initial work-up did not reveal a classic infarct distribution, with CT evidence of decreased perfusion within both occipital lobes and partial involvement of the L parietal lobe in addition to MRI evidence for 6 small infarcts within the R occipital lobe. The observed imaging patterns are consistent with an etiology of a low-flow state exacerbated by asymmetric pathological anatomy. Occurrence of infarcts in the non-stenotic R PCA could be attributed to an enhanced focal steal effect by a comparatively increased ratio of surface-area-to-volume-ratios for adjoining normally-perfused and under-perfused parenchyma as determined by the surface area of the watershed zones and associated parenchyma volumes. Additionally, the R posterior communicating artery was patent and likely facilitated a steal phenomenon towards the R MCA territory. While there was an atheromatous aortic arch observed by CT, there was no occlusion observed and it is unlikely that microemboli would lead to small focal infarcts in a watershed distribution without involvement of any preceding vasculature. Nevertheless, contribution to the acute infarcts by microemboli cannot be excluded.

Intracerebral steal is a rare phenomenon which has been investigated more in recent years, with case reports detailing its occurrence in Moyamoya disease, arteriovenous malformations, and following ICA stent placement. Collateral vasculature are thought to redirect blood flow from chronically under-perfused parenchyma via differential vasoconstriction in the setting of a decreased flow-state [2, 3]. In the setting of L VA stenosis, the patient was at increased risk of a posterior circulation infarct due to decreased net basilar blood flow and increased thrombogenic potential of the basilar artery with the L PICA nearly occluded and the basilar artery exhibiting a rightward bend [4, 5]. 

Regarding contributory factors, the patient had co-morbidities associated with increased risk of intracerebral steal in addition uncontrolled type 2 diabetes mellitus, the patient was at risk for dysautonomia with impaired cerebral autoregulation and an impaired baroreflex in addition to atherosclerosis and stroke [8]. Likewise, the patient was an active smoker at presentation, increasing the stroke risk and potentiating intracerebral steal with increased pCO2, previously observed to catalyze the differential vasoconstriction in low flow states during prior studies of the phenomenon [6]. An increased hematocrit and hyperglycemia have independently been shown to decrease blood flow, which may have potentiated a low-flow state in our patient [9, 10]. 

Works Cited

1. Sparaco M, Ciolli L, Zini A. Posterior circulation ischaemic stroke-a review part I: anatomy, aetiology and clinical presentations. Neurol Sci. 2019 Oct;40(10):1995-2006. doi: 10.1007/s10072-019-03977-2. Epub 2019 Jun 20. PMID: 31222544. 

2. Kim TJ, Lee JS, Hong JM, Lim YC. Intracerebral steal phenomenon: a potential mechanism for contralateral stroke after carotid artery stenting. Neurologist. 2012 May;18(3):128-9. doi: 10.1097/NRL.0b013e318253f8b5. PMID: 22549351.

3. Mosmans PC, Jonkman EJ. The significance of the collateral vascular system of the brain in shunt and steal syndromes. Clin Neurol Neurosurg. 1980;82(3):145-56. doi: 10.1016/0303-8467(80)90032-3. PMID: 6260410.

4. Hong JM, Chung CS, Bang OY, Yong SW, Joo IS, Huh K. Vertebral artery dominance contributes to basilar artery curvature and peri-vertebrobasilar junctional infarcts. J Neurol Neurosurg Psychiatry. 2009 Oct;80(10):1087-92. doi: 10.1136/jnnp.2008.169805. Epub 2009 May 3. PMID: 19414436; PMCID: PMC2735647.

5. Sun Y, Shi YM, Xu P. The Clinical Research Progress of Vertebral Artery Dominance and Posterior Circulation Ischemic Stroke. Cerebrovasc Dis. 2022;51(5):553-556. doi: 10.1159/000521616. Epub 2022 Feb 3. PMID: 35114670.

6. Cipolla MJ, Liebeskind DS, Chan SL. The importance of comorbidities in ischemic stroke: Impact of hypertension on the cerebral circulation. J Cereb Blood Flow Metab. 2018 Dec;38(12):2129-2149. doi: 10.1177/0271678X18800589. Epub 2018 Sep 10. PMID: 30198826; PMCID: PMC6282213.

7. Brawley BW. The pathophysiology of intracerebral steal following carbon dioxide inhalation, an experimental study. Scand J Clin Lab Invest Suppl. 1968;102:XIII:B. doi: 10.3109/00365516809169045. PMID: 4283868.

8. Kim YS, Davis SCAT, Stok WJ, van Ittersum FJ, van Lieshout JJ. Impaired nocturnal blood pressure dipping in patients with type 2 diabetes mellitus. Hypertens Res. 2019 Jan;42(1):59-66. doi: 10.1038/s41440-018-0130-5. Epub 2018 Nov 6. PMID: 30401911.

9. Cinar Y, Demir G, Paç M, Cinar AB. Effect of hematocrit on blood pressure via hyperviscosity. Am J Hypertens. 1999 Jul;12(7):739-43. doi: 10.1016/s0895-7061(99)00011-4. PMID: 10411372.

10. Cinar Y, Senyol AM, Duman K. Blood viscosity and blood pressure: role of temperature and hyperglycemia. Am J Hypertens. 2001 May;14(5 Pt 1):433-8. doi: 10.1016/s0895-7061(00)01260-7. PMID: 11368464.

Additional References

1. Woo HG, Kim HG, Lee KM, Ha SH, Jo H, Heo SH, et al. Blood viscosity associated with stroke mechanism and early neurological deterioration in middle cerebral artery atherosclerosis. Sci Rep. 2023;13(1):9384.

2. Sparaco M, Ciolli L, Zini A. Posterior circulation ischaemic stroke-a review part I: anatomy, aetiology and clinical presentations. Neurol Sci. 2019;40(10):1995-2006.

3. Renner CJ, Kasner SE, Bath PM, Bahouth MN, Committee VAS. Stroke Outcome Related to Initial Volume Status and Diuretic Use. J Am Heart Assoc. 2022;11(24):e026903.

4. Powers WJ, Rabinstein AA, Ackerson T, Adeoye OM, Bambakidis NC, Becker K, et al. Guidelines for the Early Management of Patients With Acute Ischemic Stroke: 2019 Update to the 2018 Guidelines for the Early Management of Acute Ischemic Stroke: A Guideline for Healthcare Professionals From the American Heart Association/American Stroke Association. Stroke. 2019;50(12):e344-e418.

5. Marcinkowska-Gapinska A, Siemieniak I, Kawalkiewicz W, Stieler O, Hojan-Jezierska D, Kubisz L. Interdependence of Rheological and Biochemical Parameters of Blood in a Group of Patients with Clinically Silent Multifocal Vascular Cerebral Lesions. Biomedicines. 2023;11(7).

6. Kim YS, Davis S, Stok WJ, van Ittersum FJ, van Lieshout JJ. Impaired nocturnal blood pressure dipping in patients with type 2 diabetes mellitus. Hypertens Res. 2019;42(1):59-66.

7. Kim TJ, Lee JS, Hong JM, Lim YC. Intracerebral steal phenomenon: a potential mechanism for contralateral stroke after carotid artery stenting. Neurologist. 2012;18(3):128-9.

8. Ernst E. Haemorheological consequences of chronic cigarette smoking. J Cardiovasc Risk. 1995;2(5):435-9.

9. Coull BM, Beamer N, de Garmo P, Sexton G, Nordt F, Knox R, et al. Chronic blood hyperviscosity in subjects with acute stroke, transient ischemic attack, and risk factors for stroke. Stroke. 1991;22.

10. Chang TS, Jensen MB. Hemodilution for acute ischemic stroke. Stroke. 2015;46(1):e4-e5.

11. Bahouth MN, Gottesman RF, Szanton SL. Primary 'dehydration' and acute stroke: a systematic research review. J Neurol. 2018;265(10):2167-81.