Thrombus imaging in acute stroke: correlation of thrombus length on susceptibility-weighted imaging with endovascular reperfusion success

In our series of patients with MCA occlusions, 95.5 % of the thrombi were clearly definable on SWI. This detection rate is in line with those recently reported for SWI and T2* gradient-echo imaging in anterior circulation stroke [7, 11]. We propose a new technique for defining thrombus location that is applicable to different imaging modalities (Fig. 1). Using this technique we found a strong correlation between the location of the proximal thrombus end as seen on SWI and that on TOF-MRA, GE-MRA and DSA. These findings support previous reports which showed that SWI and T2* gradient-echo imaging can reliably depict thrombus location when compared to TOF-MRA [11] and DSA [7]. Moreover, we demonstrated that thrombus length as measured on SWI did not appear to have an impact on success of endovascular reperfusion therapy of MCA occlusions.

The latter finding is of particular interest. Various studies have shown that the success of vessel recanalization with intravenous thrombolysis seems to depend on clot burden. Clot burden was defined either on thin-slice non-enhanced CT, CT-angiography, or recently on T2* gradient-echo images measuring either absolute thrombus length [2] or applying a scoring system based on thrombus location [12, 13]. MCA thrombi measuring more than 8 mm in length were found to have nearly no potential for recanalization with intravenous thrombolysis [2]. Lower clot burden scores, indicating a higher thrombus burden, showed significant associations with worse clinical outcome [12, 13].

The effect of thrombus burden on reperfusion success and clinical outcome after endovascular treatment remains less clear. A study by Puetz et al. analysing clinical outcome in relation to the clot burden score on CT-angiography found no differential effect on outcome between patients treated by intravenous thrombolysis, endovascular means or a combination of both [12]. Barreto et al. used the modified TIMI criteria to assess thrombus burden in patients undergoing endovascular therapy alone or in combination with bridging thrombolysis [14]. In his study, a significant association between high clot burden and worse clinical outcome at 3 months was observed. Although the percentage of patients with successful reperfusion (TICI 2b–3) was higher in the group with lower clot burden compared to those with larger clots, this difference was not significant [14]. In the present study, thrombus length as measured on SWI did not significantly affect reperfusion success (P = 0.153). Our findings suggest that when using multimodal endovascular revascularization techniques, thrombus length does not affect the chances of successful reperfusion. It has to be noted that the comparability between the aforementioned studies is limited because of the variable methods used to assess clot burden or size.

Detection rates of vessel occlusions were similar between SWI (95.5 %), TOF-MRA (98.9 %) and GE-MRA (97.5 %). In two of the four patients with no definable SVS, the interpretability of SWI was limited because of severe motion artefacts and in one patient with a proximal M1 occlusion, the MCA was partially obscured by susceptibility artefacts in the proximity of the skull base. In the fourth patient the thrombus could not be detected on SWI for unknown reasons, even in direct comparison with TOF-MRA, GE-MRA and DSA which clearly depicted a vessel occlusion.

Interestingly, small but systematic differences were found between the distances of the proximal thrombus end to the midline measured on SWI and those obtained on TOF-MRA (mean bias 1.6 mm; percentage error 6.4 %) using Bland–Altman statistics (Fig. 3). On TOF-MRA slow flow, such as seen proximal to an occlusion, can lead to inadequate depiction of vessel segments that are still patent, potentially resulting in overestimation of the occlusion [15, 16]. This phenomenon might explain the shorter distance measured from midline to proximal thrombus end on TOF-MRA compared with the other angiographic methods.

Although TOF-MRA and GE-MRA remain indispensable in stroke imaging, SWI adds important complementary information. SWI not only shows the proximal end of the occluding thrombus, but also its length. For these reasons SWI has become a valuable part of our stroke imaging protocol. For optimal planning of the endovascular procedure, we deem it necessary to know the thrombus extension as well as each individual patient’s angioarchitecture from the aortic arch up to the distal branches of the large intracranial arteries. In daily practice thrombus imaging with SWI guides us in the selection of the treatment approach in patients with MCA occlusions. In patients with relatively short thrombi measuring less than 8 mm in length we preferentially use intravenous thrombolysis and continue with endovascular therapy only in case the symptoms do not improve [2]. In patients with longer thrombi limited to the sphenoidal segment of the MCA (M1 segment), stent retriever thrombectomy is the treatment of choice. In the absence of contraindications, bridging thrombolysis is usually initiated before endovascular treatment. When using stent retrievers it is important to deploy the distal tip of the device in the vessel segment distal to the thrombus so as not to shear off parts of the clot during stent retraction. Again, SWI is helpful for planning this procedure as it can identify the distal thrombus end as well as the curvature of the occluded vessel segment. This information is especially important in patients with thrombi extending from the M1 segment to the insular segment (M2) or even affecting opercular branches (M3). In order to deploy a stent retriever, the microcatheter has first to be navigated without the aid of a roadmap, through the curved vasculature at the transition of the sphenoidal to the opercular segment, or even through the vessels in the limen insulae. Furthermore, diameter, length and type of the stent retriever can be selected prior to the intervention on the basis of information from the SWI. Additional techniques, such as the use of distal access aspiration catheters [17], can be prearranged and applied in complex thrombus and vessel anatomy. Figure 4 shows different types of thrombi as seen on SWI warranting different treatment approaches.

Our study has some limitations. One could argue that it is unknown to what extent the distal end of the susceptibility vessel sign is caused by the thrombus itself, and to what extent by stagnating, deoxyhaemoglobin-rich blood distal to the occlusion, resulting in overestimation of the real thrombus length. A recent study addressed this uncertainty by showing an excellent correlation between the thrombus length as measured on T2* gradient-echo imaging and that on DSA [7]. To avoid the limited sensitivity of SWI in proximity to the skull base, i.e. intracranial segment of the internal carotid artery and posterior circulation arteries, we decided to assess only MCA occlusions to correlate the sensitivity of SWI with various angiographic techniques. The sensitivity of gradient-echo imaging in detecting thrombi appears to be lower for the posterior circulation [7]. Only few patients presented with isolated occlusions of the M2 segment and none had an occlusion of the M3/4 segments. The generalizability of the results regarding the thrombus location defined by vessel segment is therefore limited because of the rather small patient number. Furthermore, all patients included in our study underwent endovascular treatment. Such patients usually present with more proximal and larger thrombi compared to those treated by intravenous thrombolysis alone. Thrombus length has been shown to influence detectability of thrombi on T2* gradient-echo imaging [7]. An additional bias may have been introduced by obtaining SWI at two different field strengths (1.5 T and 3 T). A study analysing the effect of field strength on the diameter of cerebral microbleeds as measured on SWI showed an increase in size with higher field strength [18]. Likewise, the length of the SVS on SWI may slightly vary with field strength. Finally, SWI tends to overestimate the real proportions of material with different magnetic susceptibility than the surrounding tissue (e.g. microbleeds, thrombi) [19, 20], probably resulting in a slight overestimation of maximal thrombus length.