Published ahead of print on February 24, 2011
doi: 10.3174/ajnr.A2456

American Journal of Neuroradiology 32:E51-E52, March 2011
© 2011 American Society of Neuroradiology

R.V. Chandra^a, T.M. Leslie-Mazwi^a and D. Oh^a
aDepartment of Interventional Neuroradiology and Endovascular Neurosurgery

B. Mehta^b
bDepartment of Neurocritical Care

A.J. Yoo^c
cDepartment of Diagnostic and Interventional Neuroradiology
Massachusetts General Hospital
Harvard Medical School
Boston, Massachusetts

We commend Cuvinciuc et al¹ on their recent review of nontraumatic cortical subarachnoid hemorrhage (cSAH). While not an uncommon clinical presentation, there is an overall paucity of literature on this subject, with the largest reported series by Kumar et al² comprising only 29 patients. Cuvinciuc et al¹ suggested that cSAH may occur in the setting of high-grade atherosclerotic stenosis of the extracranial cerebral arteries, potentially by a mechanism similar to cSAH in Moyamoya disease (eg, rupture of fragile dilated pial collateral vessels). Recently 3 cases of cSAH have been described in association with bilateral cervical internal carotid artery (ICA) stenosis,³ and 2 further cases, in the setting of acute ICA occlusion during ischemic stroke.⁴We describe a rare case of unilateral extracranial ICA stenosis associated with cSAH and discuss the angiographic findings that support the postulated mechanism of fragile pial collateral vessels.

A 70-year-old man experienced a sudden onset of transient aphasia and dysarthria, along with right face and arm numbness at a systolic blood pressure of 200 mm Hg. Noncontrast CT demonstrated isolated cSAH in the left central sulcus (Fig 1), and CT angiography (CTA) revealed an 80% left ICA-origin stenosis without evidence for arterial or venous cause of the cSAH. He continued to have recurrent events in the hospital and was managed for possible transient ischemia or seizure with intravenous anticoagulation and seizure prophylaxis, respectively. MR imaging excluded acute infarction, posterior reversible leukoencephalopathy, amyloid angiopathy, or an underlying mass. There was no clinical evidence of endocarditis, with negative findings on blood cultures and a normal finding on transthoracic echocardiogram. Continuous electroencephalographic monitoring during these episodes did not reveal epileptiform correlation during briefly symptomatic episodes that remained similar to those on the initial presentation.Given the frequency of transient symptoms, carotid endarterectomy (CEA) was considered for the ipsilateral stenosis. However, it was imperative to definitively rule out any vascular lesions responsible for the cSAH, which could worsen from potential hyperperfusion syndrome following CEA. Cerebral angiography was performed and demonstrated no evidence of vasculitis, reversible cerebral vasoconstriction syndrome, mycotic aneurysm, or arteriovenous malformation.

Of note, the 80% left ICA-origin stenosis (Fig 2) resulted in a shift of the angiographic watershed between the left middlecerebral artery (MCA) and posterior cerebral artery (PCA) territories toward the central sulcus (Fig 3). Most importantly, there was minimal collateral support via the circle of Willis. A hypoplastic precommunicating right anterior cerebral artery (ACA) segment provided minimal flow across the anterior communicating artery. No left posterior communicating artery was discernible. Subsequently, the patient underwent emergent ipsilateral CEA with resolution of his symptoms.

Isolated cSAH in the present case, the 3 cases with bilateral ICA stenosis described by Kleinig et al,³ and the 2 cases ofacute ICA occlusion described by Geraldes et al,⁴ all occurred on the symptomatic side or the side with the more severe anatomic narrowing (stenosis or occlusion). All 6 patients were acutely symptomatic suggesting that cSAH may derive from an acute alteration in hemodynamics (eg, plaque rupture and further atherothrombotic narrowing or acute hypertension). We propose that this hemodynamic stress may damage already maximally dilated pial collateral vasculature and produce cSAH.

This idea is supported by our angiographic findings, in which the subarachnoid hemorrhage colocalized to the watershed region between the MCA and PCA territories. In the setting of severe ICA stenosis or occlusion, it is the MCA-PCA watershed rather than the MCA-ACA watershed that may be particularly prone to this phenomenon, because the ipsilateral ACA and MCA have reduced perfusion pressure and are less able to respond to acute hemodynamic failure, particularly in the absence of sufficient blood flow via the anterior or posterior communicating arteries as in this case. On the other hand, the normally perfused PCA territory is able to mount a compensatory increase in perfusion pressure, which may rupture fragile pial collateral vessels in the watershed. Consistent with this idea, 4 of the 6 described cases occurred in a perirolandic location, at the watershed between the MCA and PCA territories.

The rarity of cSAH in the setting of unilateral extracranial ICA stenosis may reflect the collateral pathways across the circle of Willis that are usually present. As in our case, the absence of adequate collaterals may provide a clue to this mechanism of cSAH. Contrary to Cuvinciuc et al,¹ who advocated only brain vascular imaging, CTA evaluation of cSAH must include the cervical vasculature, lest a high-risk yet treatable lesion is missed.

References

1. Cuvinciuc V, Viguier A, Calviere L, et al. Isolated acute nontraumatic cortical subarachnoid hemorrhage. AJNR Am J Neuroradiol 2010;31:1355–62[Abstract/Free Full Text]
2. Kumar S, Goddeau RP, Jr, Selim MH, et al. Atraumatic convexal subarachnoid hemorrhage: clinical presentation, imaging patterns, and etiologies. Neurology 2010;74:893–99[Abstract/Free Full Text]
3. Kleinig TJ, Kimber TE, Thompson PD. Convexity subarachnoid haemorrhage associated with bilateral internal carotid artery stenoses. J Neurol 2009;256:669–71[CrossRef][Medline]
4. Geraldes R, Santos C, Canhao P. Atraumatic localized convexity subarachnoid hemorrhage associated with acute carotid artery occlusion. Eur J Neurol 2011;2:e28–e29

Reply

Published ahead of print on February 24, 2011
doi: 10.3174/ajnr.A2559

American Journal of Neuroradiology 32:E53, March 2011
© 2011 American Society of Neuroradiology

V. Cuvinciuc^a and F. Bonneville^a
aDepartment of Neuroradiology

A. Viguier^b
bDepartment of Vascular Neurology
Rangueil University Hospital
Toulouse, France

We thank Chandra et al for their contribution in detailing the angiographic findings of extracranial internal carotid stenosis associated with cortical subarachnoid hemorrhage (cSAH). Our postulated mechanism of rupture of fragile dilated collateral pial vessels is supported by their findings of severe extracranial internal carotid artery stenosis, angiographic visualization of dilated pial anastomoses, the borderline topography of cSAH (in the same area as the dilated pial anastomoses), and the absence of other potential causes.

Autoregulatory vasodilation is a compensatory mechanism for decreases in cerebral perfusion pressure in patients with unilateral chronic steno-occlusive disease. It would be interesting to have, in this setting, a functional examination for evaluation of cerebral vascular reserve. Different techniques exist (eg, positron-emission tomography, single-photon emission CT, and,more widely available, CT perfusion with acetazolamide challenge).^1,2 We suppose that fragile dilated collaterals would be associated with a depletion of the cerebral vascular reserve, with very limited reactivity after acetazolamide challenge compared with the contralateral side.

In our clinical routine, we prefer performing a brain CT angiography for patients with cSAH, and if negative, it is completed with cervical contrast-enhanced MR imaging or CT angiography to evaluate the presence of this rare association of a cSAH and an extracranial carotid artery stenosis. Angiography should remain reserved for selected cases only.

References

1. Kim E, Sohn CH, Na DG, et al. Perfusion computed tomography evaluation of cerebral hemodynamic impairment in patients with unilateral chronic steno-occlusive disease: a comparison with the acetazolamide challenge 99mTc-hexamethylpropyleneamine oxime single-photon emission computed tomography. J Comput Assist Tomogr 2009;33:546–51[CrossRef][Medline]
2. Chen A, Shyr MH, Chen TY, et al. Dynamic CT perfusion imaging with acetazolamide challenge for evaluation of patients with unilateral cerebrovascular steno-occlusive disease. AJNR Am J Neuroradiol 2006;27:1876–81[Abstract/Free Full Text]