Leptomeningeal collateralization in acute ischemic stroke: Impact on prominent cortical veins in susceptibility-weighted imaging
Introduction
The extent of the infarct core, existence of a penumbra and the site of vessel occlusion are the relevant variables which guide the therapeutic decision in the setting of acute ischemic stroke. Good collaterals which can support the blood flow to the penumbra and thus extend the therapeutic window are being increasingly recognized as a further key player in this decision process. Susceptibility-weighted imaging (SWI) is a useful imaging tool routinely applied for detection of blood byproducts, e.g. in hemorrhage and calcifications [1], [2], [3]. There is also a role for SWI in acute ischemic stroke. Three main pathological changes were described in this context. First, the susceptibility vessel sign [2], [4] that corresponds to the occluding thrombus. Second, detection of hemorrhagic transformation in the infarct [2]. Third, prominent cortical veins (PCV) in the hypoperfused regions [2], [5], [6]. A possible explanation for the signal drop marking the PCV on SWI is the increased oxygen extraction fraction (OEF) in the critically hypoperfused parenchyma. The locally increasing ratio of deoxyhemoglobin to oxyhemoglobin in capillaries and veins might be an expression of the stress that the tissue-at-risk is under [7]. The degree of the SWI signal drop in the PCV could vary according to the degree of hypoperfusion and oxygen extraction. Although a direct comparison between SWI and positron emission tomography (PET) images (the gold standard for quantifying OEF) has not yet been performed several studies have shown an association between T2* signal drop and increased OEF [8], [9], [10], [11]. Kao et al. showed a significant correlation between the extent of delayed mean transit time (MTT) in perfusion-weighted imaging (DSC) and the extent of PCV on SWI using the Alberta Stroke Program Early CT Score (ASPECTS) [5]. The authors suggest that SWI can be considered an alternative to DSC to assess the penumbra. However, PCV do not appear in every acute ischemic stroke case as shown in several studies [6], [12], making SWI a questionable alternative. In a recent prospective study of Huang et al. no association between the presence of PCV in acute ischemic stroke and prognosis, presence of later hemorrhagic transformation, edema and clinical worsening or improvement was found [6].
However, the appearance of PCV seems to be pathophysiologically complex and the clinical importance is still unclear. The aim of our study was to investigate the influence of the leptomeningeal collateralization on PCV on SWI. A good leptomeningeal collateralization has a tissue protective effect in stroke [13], [14]. We hypothesize that this protective effect is reflected in the extent and markedness of PCV. The better the leptomeningeal collateralization the lower the deoxyhemoglobin levels and the less PCV should be observed and vice versa. In addition correlations between PCV, prolonged MTT and diffusion-restricted infarction areas were investigated.
Section snippets
Patients
We retrospectively retrieved data of 144 patients treated at our Stroke Unit from January 2004 to November 2012. Inclusion criteria were an acute thromboembolic occlusion of the M1-segment of the middle cerebral artery, a preinterventional MRI including SWI, DWI and DSC, and a digital subtraction angiography (DSA). Patients were excluded if image quality was insufficient, e.g. due to severe motion artifacts and in cases of internal carotid artery occlusion. Overall, 33 subjects fulfilled the
General
33 patients with an acute ischemic stroke underwent pretreatment MRI. The basic clinical characteristics and imaging findings are shown in Table 1. The mean values of the PCV-, MTT- and DR-ASPECTS were 3.55, 1 and 5.15 respectively. Statistically significant differences were found between these ASPECTS scores: PCV-ASPECTS versus MTT ASPECTS (p = 0.000), PCV-ASPECTS versus DR ASPECTS (p = 0.03), DR ASPECTS versus MTT ASPECTS (p = 0.00).
Out of 33 patients only one showed no PCV. According to ASPECTS
Discussion
With its high sensitivity for paramagnetic substances in high resolution, like deoxygenated blood, iron or blood products SWI has emerged to an indispensable MR sequence [17], [18], [19]. For many clinical issues, e.g. intracranial hemorrhage, vascular malformation, sinus vein thrombosis or tumor, SWI has shown to be a reliable diagnostic tool [20], [21], [22], [23], [24]. The application of SWI in acute ischemic stroke is quite new but has already proven itself to be a useful technique in many
Conflict of interest
The authors declare that they have no conflict of interest.
Acknowledgements
We express our gratitude to Pietro Ballinari for statistical analysis.
References (30)
- et al.
Susceptibility weighted imaging: a new tool in magnetic resonance imaging of stroke
Clin Radiol
(2009) - et al.
ASPECTS and other neuroimaging scores in the triage and prediction of outcome in acute stroke patients
Neuroimaging Clin N Am
(2011) - et al.
Detecting subarachnoid hemorrhage: comparison of combined FLAIR/SWI versus CT
Eur J Radiol
(2013) - et al.
Susceptibility-weighted imaging for differential diagnosis of cerebral vascular pathology: a pictorial review
J Neurol Sci
(2009) - et al.
Hemodynamic monitoring of intracranial collateral flow predicts tissue and functional outcome in experimental ischemic stroke
Exp Neurol
(2012) - et al.
Susceptibility-weighted imaging: technical aspects and clinical applications, part 2
AJNR Am J Neuroradiol
(2009) - et al.
Contribution of susceptibility-weighted imaging to acute stroke assessment
Stroke
(2004) - et al.
Susceptibility sign on susceptibility-weighted imaging in acute ischemic stroke
Neurol India
(2012) - et al.
Predicting stroke evolution: comparison of susceptibility-weighted MR imaging with MR perfusion
Eur Radiol
(2012) - et al.
Clinical applications of susceptibility weighted imaging in patients with major stroke
J Neurol
(2012)
Susceptibility weighted imaging in cerebral hypoperfusion – can we predict increased oxygen extraction fraction?
Neuroradiology
Magnetic resonance cerebral metabolic rate of oxygen utilization in hyperacute stroke patients
Ann Neurol
Blood oxygen saturation assessment in vivo using T2* estimation
Magn Reson Med
Quantitative measurements of cerebral blood oxygen saturation using magnetic resonance imaging
J Cereb Blood Flow Metab
In vivo measurement of oxygenation changes after stroke using susceptibility weighted imaging filtered phase data
PLOS ONE
Cited by (47)
Related Factors of Asymmetrical Vein Sign in Acute Middle Cerebral Artery Stroke and Correlation with Clinical Outcome
2017, Journal of Stroke and Cerebrovascular DiseasesCitation Excerpt :In most cases, the presence of AMVS on SWI occurs in the patients with MCA occlusion, which reflects a poor collateralization. The OEF should be lower in case of a good collateralization due to higher oxygen supply to the tissue at risk, which proves the absence of AMVS.33 On the contrary, a poor collateralization may result in higher OEF in the ischemia tissues, which shows the presence of AMVS.
Cerebral venous collaterals: A new fort for fighting ischemic stroke?
2018, Progress in NeurobiologyCitation Excerpt :According to the follow-up imaging by Verma et al., that the extent of prominent cortical veins (PCV) which indicated venous congestion and reduced oxygen saturation, was reversely correlated with leptomeningeal arterial anastomosis. That means, less arterial collateral perfusion would affect the oxygen saturation in ipsilateral cortical veins (Verma et al., 2014). With dynamic CTA (dCTA), the delayed cortical venous filling was found excellently correlated with arterial collateral extent and perfusion rate (Bhaskar et al., 2017).
- 1
These authors contributed equally to the study.