Retrograde Angiography to Detect Dropped Thrombus in Mechanical Thrombectomy

Abstract

Objective

The risk of embolization to distal territory or to new territory in mechanical thrombectomy remains a major issue despite advancements in technological device. This condition can be caused by a large and firm dropped thrombus without passing through a guiding catheter during stent retriever or aspiration catheter withdrawal. This report introduced a novel technique referred to as retrograde angiography to detect dropped thrombus.

Methods

The retrograde angiography to detect dropped thrombus technique is a kind of retrograde angiography that consists of a contrast medium injection via a distal microcatheter and aspiration through an inflated balloon-guiding catheter. This method was used to detect dropped thrombus at the balloon-guiding catheter tip when back flow was blocked from the balloon-guiding catheter after stent retriever or aspiration catheter withdrawal. We retrospectively reviewed four consecutive patients who underwent the retrograde angiography to detect dropped thrombus technique during mechanical thrombectomy for acute ischemic stroke due to large vessel occlusion in the anterior circulation between January 2018 and January 2021.

Results

Three of four patients had dropped thrombus, which was diagnosed with the technique and retrieved completely with subsequent procedures while maintaining the balloon-guiding catheter inflated. None of the patients experienced embolization to distal territory/embolization to new territory, and a successful reperfusion was achieved in all four cases.

Conclusions

The retrograde angiography to detect dropped thrombus is a technique to detect a dropped thrombus at the balloon-guiding catheter tip and allows us to retrieve it with subsequent mechanical thrombectomy procedures while maintaining the balloon-guiding catheter inflated and it may be useful for reducing the risk of embolization to distal territory/embolization to new territory.

Introduction

Although various techniques have been recommended for achieving recanalization in mechanical thrombectomy (MT) for acute ischemic stroke due to large vessel occlusion,^1,2 embolization to distal territory (EDT) and embolization to new territory (ENT) remain a challenging and important complication. To prevent these conditions, several studies have applied some techniques that use a balloon-guiding catheter (BGC), which include aspiration-retriever technique for stroke (ARTS) and proximal balloon occlusion along with direct thrombus aspiration during stent retriever thrombectomy (PROTECT).^3–8 However, if a large and firm thrombus cannot pass through the BGC during stent retriever (SR) or aspiration catheter (AC) withdrawal, it may drop at the BGC tip and can cause EDT/ENT when antegrade flow is restarted after deflating the BGC or contrast injection is performed via the BGC. When poor back flow from the BGC is encountered after the MT techniques, removing the BGC under contact aspiration may be performed in most centers assuming the presence of such dropped thrombi: even after the BGC removal under aspiration, however, the authors experienced some cases of EDT/ENT. Thus, the authors developed a novel angiographic technique referred to as retrograde angiography to detect dropped thrombus (RAD²) to show the presence and the volume of the dropped thrombus and to consider the way to retrieve it safely with subsequent MT.

Methods

The current study was approved by the ethical committee of our institution and was performed in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the 1975 Declaration of Helsinki, as revised in 2000 (World Medical Association Declaration of Helsinki 2000).

Patients

We retrospectively assessed four patients for whom the RAD² technique was performed among 56 consecutive patients treated with MT for acute ischemic stroke due to large vessel occlusion in the anterior circulation between January 2018 and January 2021. In our hospital, MR imaging is performed to evaluate the occluded vessel, ischemic core, and penumbra region in patients with acute ischemic stroke and we decide the indication for MT.

Procedure

MT for Acute Ischemic Stroke due to Large Vessel Occlusion in the Anterior Circulation

In the MT using the ARTS or PROTECT technique for acute ischemic stroke due to large vessel occlusion in the anterior circulation,^7,8 the SR and AC withdrawal are started while sucking from the AC and inflated BGC with aspiration pump and a 20 mL syringe, respectively. If there is little back flow from the AC, suggesting that a thrombus can be captured with the AC, the SR and AC are removed with holding the state (Figure 1(A)). If there is a possibility of atherosclerotic cervical ICA occlusion, balloon angioplasty is performed. Then, manual aspiration through the BGC with a 20 mL syringe is repeatedly performed several times after withdrawing devices, such as the SR, AC, and a balloon catheter (Figure 1(B)). In general, back flow is obtained from the BGC when recanalization is achieved. If the back flow is still poor, the RAD² technique is performed with suspicion that a firm and large dropped thrombus obstructs the BGC orifice: if not, there is a possibility that thrombi occlude the lumen within the BGC, the vessel occlusion site is not recanalized completely, or collateral blood flow through anterior/posterior communicating artery is quite poor.

Figure 1.

Schema of mechanical thrombectomy and the subsequent retrograde angiography to detect dropped thrombus (RAD²) technique. (A) Stent retriever (SR) and aspiration catheter (AC) withdrawal are started while sucking from the AC and inflated balloon guiding catheter (BGC) with aspiration pump and a 20mL syringe, respectively. Then, the SR and AC are removed with holding the state while confirming little back flow from the AC. (B) When the back flow via the BGC is still poor after SR or AC withdrawal, manual aspiration (MA) is performed to remove small dropped thrombi while the BGC is inflated. (C) If back flow is still poor via the BGC, a microcatheter (MC) is deployed proximal to the petrous segment of the internal carotid artery. Then, antegrade angiography via the MC is performed to validate whether recanalization of the occlusion site is achieved while maintaining the proximal side of the BGC open and the balloon inflated. (D) This schema is a main component of the RAD2 technique. MA through the BGC with a 20 mL syringe is subsequently started with the additional administration of a contrast medium via the MC, and a dropped thrombus can be identified at the BGC tip via the retrograde angiography.

RAD² Technique

1. A micro-guidewire and a microcatheter are deployed proximal to the petrous segment of the ICA, paying close attention to ensure that the thrombus is not pushed distally with manual aspiration from the inflated BGC.

2. Before the RAD² technique, antegrade angiography via the microcatheter is performed to validate whether recanalization is achieved. The administration of a contrast medium is started gradually with the proximal side of the BGC left open to reduce the elevation of intra-arterial pressure by contrast medium injection when recanalization on the distal side is not achieved: even if a dropped thrombus obstructs the BGC tip, a gap develops between the thrombus and the tip of the BGC by a microcatheter passing through, and through the gap, it may be possible to prevent a surge in intra-arterial pressure during the angiography. After confirming no large vessel occlusion on the distal side, the injection rate is increased to validate the degree of reperfusion (Figure 1(C)).

3. This section is the main component of RAD² technique. The second administration of a contrast medium via the microcatheter along with manual aspiration through the BGC using a 20 mL syringe is performed to identify a dropped thrombus at the BGC tip via retrograde angiography (Figure 1(D)). The manual aspiration through the BGC is performed weakly so that a thrombus does not get stuck in the BGC tip.

Procedure After the RAD² Technique

If there is a dropped thrombus at the BGC tip, additional treatments such as crushing with a guidewire, repeating MT, or carotid artery stenting upon the thrombus while maintaining the BGC inflated are considered. When the back flow is improved after the procedures for the dropped thrombus, angiography via the BGC is performed to validate the disappearance of the dropped thrombus and intracranial reperfusion after the BGC is deflated. In contrast, if there is no dropped thrombus, antegrade blood flow is restarted by deflating the BGC.

Results

The clinical characteristics of four patients who underwent the RAD² technique were shown in Table 1. All patients presented with cervical ICA occlusion. A dropped thrombus was detected with the RAD² technique in three (75%) patients. Thus, the overall frequency of a dropped thrombus was 5.4% (95% confidence interval, −0.7 to 11.4; 3 of 56 consecutive patients treated with MT) in the study period. In these cases, the thrombus was retrieved with subsequent procedures and massive fragmented thrombi were detected in the suction syringe at the end of the procedure. In case 1, manual aspiration from the BGC was performed repeatedly after the withdrawal of a microcatheter. In case 3, we crushed the dropped thrombus by pushing and pulling J-shaped guidewire and removed the fragments with manual aspiration. In case 4, a SR was deployed at the tip of the BGC and withdrawn via inflated BGC with manual aspiration. In the remaining one (25%) case that dropped thrombus was not detected, the cause of poor back flow was an occlusion at the C5 segment of the ICA due to thrombi migrating distally from the cervical ICA stenosis after percutaneous transluminal angioplasty (Figure 2). Finally, successful reperfusion (modified Thrombolysis In Cerebral Infarction (mTICI) grade 2b) was achieved in all cases and the mean puncture-to-reperfusion time was 63 (range: 38–79) minutes. Three (75%) patients achieved a good outcome (modified Rankin scale score of 0–2 at 90 days).

Table 1.

Clinical characteristics of patients treated with mechanical thrombectomy (MT) with retrograde angiography to detect dropped thrombus (RAD²) technique.

	Case 1	Case 2	Case 3	Case 4
Age (years)/sex	57/M	84/M	81/M	73/M
NIHSS score upon admission	13	6	23	8
Stroke subtypes	ATBI	ATBI	CE	CE
Site of occlusion	Cervical ICA and M1d	Cervical ICA	Cervical ICA	Cervical ICA and C3
IV-tPA	No	No	Yes	Yes
Technique used prior to RAD2	PTA to ICAS, and MA	PTA to ICAS	ARTS	ADAPT and ARTS
Thrombus detection using the RAD2	Yes	No	Yes	Yes
Treatment for dropped thrombus	MA	-	CGW, MA	SR
Prolonged revascularization time due to the use of the RAD2 technique (min)	1.5	1.0	3.0	4.5
EDT, ENT	No	No	No	No
mTICI grade	2b	2b	2b	2b
Puncture-to-reperfusion time (min)	38	78	57	79
MT-related complications	No	No	No	No
Modified Rankin scale score at 90 days	0	1	4	1

ADAPT: a direct aspiration first-pass technique; ARTS: aspiration-retriever technique for stroke; ATBI: atherothrombotic brain infarction; BGC: balloon-guiding catheter; CE: cardiogenic embolism; CGW: crushing with a guidewire; EDT: embolization to distal territory; ENT: embolization to new territory; ICA: internal carotid artery; ICAS: internal carotid artery stenosis; IV-tPA: intravenous recombinant tissue plasminogen activator; M: male; MA: manual aspiration; M1d: distal portion of the M1; mTICI: modified thrombolysis in cerebral infarction; NIHSS: National Institute of Health Stroke Scale; PTA: percutaneous transluminal angioplasty; SR: stent retriever.

Figure 2.

Digital subtraction angiograms in case 2 in Table 1. (A) Right common carotid angiography via a balloon guiding catheter (BGC) reveals the right cervical internal carotid artery (ICA) occlusion. (B) Right internal carotid angiography via a microcatheter (MC) to confirm the extent of occlusion reveals patency of the intracranial ICA before mechanical thrombectomy. (C) Antegrade angiography via a MC distal to the right cervical ICA stenosis after percutaneous transluminal angioplasty reveals an occlusion of C5 segment of the ICA and subsequent retrograde angiography reveals no dropped thrombus at the BGC tip or the stenosis.

Representative Case (Case 3 in Table 1)

An 81-year-old male patient who presented with impaired consciousness and left hemiparesis of 2 h duration was diagnosed as acute ischemic stroke due to the right ICA occlusion (Figure 3(A) and (B)). Prior to performing MT after the administration of intravenous recombinant tissue plasminogen activator, a written informed consent to the treatment and publishment of the patient's information was obtained from the patient's relatives.

Figure 3.

Interventional radiologic therapy images of a representative case (case 3 in Table 1). (A) Diffusion-weighted magnetic resonance imaging on admission shows high-intensity areas in the left frontal and temporal lobes. (B) Magnetic resonance angiography shows the occlusion of the right internal carotid artery (ICA). (C) Right common carotid angiography (lateral image) via a balloon-guiding catheter (BGC) reveals the right cervical ICA occlusion before mechanical thrombectomy. (D) Antegrade angiography (lateral image) via a microcatheter deployed at the C5 segment of the right ICA reveals no intracranial large vessel occlusion after mechanical thrombectomy. (E) Filling defects (arrowhead) indicating a dropped thrombus is detected at the BGC tip in the subsequent retrograde angiography (lateral image) via the microcatheter while aspirating from the inflated BGC with a 20 mL syringe (RAD² technique). (F) Filling defects (arrowhead) indicating a dropped thrombus in Figure 2(E) is magnified. (G) Right internal carotid angiography (lateral image) shows the disappearance of the filling defects after crushing the thrombus with a J-shaped guidewire and removing the fragmented thrombi by manual aspiration through the BGC. (H) The tip of the BGC in Figure 2(G) is magnified. (I) Final right internal carotid angiography (lateral image) shows successful reperfusion (modified Thrombolysis In Cerebral Infarction grade 2b).

Common carotid angiography via a BGC (Optimo; Tokai Medical Products, Aichi, Japan) showed occlusion of the right cervical ICA (Figure 3(C)). An AC (ACE68 Penumbra System; Penumbra, California, USA) was advanced into the C5 segment of the right ICA and a 0.027-inch microcatheter (Marksman; Covidien, California, USA) was passed beyond the thrombus over a micro-guidewire (CHIKAI black 14 soft tip; Asahi Intecc, Tokyo, Japan). After super-selective angiography via the microcatheter to determine the extent of the thrombus and to validate whether the microcatheter passed beyond the thrombus (Figure 3(D)), the SR (Embotrap II; Johnson & Johnson, Tokyo, Japan) was placed via the thrombus and then both the SR and AC were withdrawn via the inflated BGC because there was little back flow from AC. However, there was still poor back flow via the BGC after manual aspiration through the BGC. Thus, a large dropped thrombus at the BGC tip was suspected, and the RAD² technique was conducted. After the microcatheter was navigated proximal to the petrous segment of the ICA with manual aspiration from the inflated BGC, recanalization of the intracranial large vessel occlusion was confirmed on antegrade angiography, and filling defects indicating dropped thrombi were detected at the BGC tip via retrograde angiography (RAD² technique) (Figure 3(E) and (F)). The thrombus was crushed with a 0.035-inch hydrophilic guidewire (Radifocus; Terumo, Tokyo, Japan) while the balloon was inflated. Then, thrombus fragments were aspirated through the BGC. Since back flow via the BGC improved, the BGC was deflated and subsequent angiography via the BGC confirmed the disappearance of the filling defect and successful reperfusion (mTICI 2b) (Figure 3(G) to (I)).

Discussion

EDT/ENT is caused by the migration of a thrombus to downstream/another territory of occluded vessels. Several reports have shown that the combined use of BGC and AC was effective in preventing EDT/ENT in MT. However, these conditions are still a major issue associated with worse clinical outcomes.^9–11

One of the causes of EDT/ENT is a dropped thrombus at the BGC tip. If a thrombus is firm or larger than the inner lumen of the BGC, it may drop without passing through the BGC during SR or AC withdrawal. Yeo et al. showed the following mechanisms of embolus formation during MT: water-hammer effects of the blood flow shearing off parts of the thrombus, crossing clots especially with a larger catheter, thrombus fragmentation by friction between the vessel wall and the thrombus while withdrawing it, a temporary loss of apposition between the SR and the thrombus while withdrawing them into a large vessel from a smaller one, thrombus crushing by struts of the thrombectomy device, and shearing off the thrombus by the sides of the guiding catheter with a small lumen into which the thrombus is pulled (Figure 4). ¹² Of thrombi sheared off by the edge of BGC, too large and firm one to be removed by the suction is focused in the present report and we defined the thrombus as “dropped thrombus.” A dropped thrombus is not affected by antegrade blood flow if the BGC is inflated, and therefore can be retrieved without distal migration. In contrast, the other types of an embolus can migrate distally by collateral blood flow via the other vessels such as anterior/posterior communicating artery even if the BGC is inflated. Furthermore, dropped thrombi likely occur in a case of the ICA occlusion with massive thrombi, and can cause the occlusion of larger vessels or more extensive cerebral ischemia when migrating distally. A dropped thrombus is not rare as in the present report, and we previously experienced a case in which distal migration of the dropped thrombus was retrospectively identified and caused poor outcome without the RAD² technique. Thus, more attention should be given to this issue.

Figure 4.

Schema of the mechanisms of embolus formation during mechanical thrombectomy with a stent retriever (SR). (A) Water-hammer effects of the blood flow shearing off parts of the thrombus. (B) Crossing clots especially with a larger microcatheter (MC). (C) Crushing clots by struts of the SR. (D) Thrombus fragmentation by friction between the vessel wall and the thrombus while withdrawing it. (E) A temporary loss of apposition between the SR and the thrombus while withdrawing them into a large vessel from a smaller one. (F) Shearing off the thrombus by the sides of the balloon-guiding catheter (BGC) with a smaller lumen into which the thrombus is pulled.

Few studies have focused on treatment for dropped thrombi. One of the main reasons is that it may not be detected as dropped thrombus via general procedures. In cases that a BGC is not used, a dropped thrombus immediately migrates to the distal vessels via antegrade blood flow. Even in cases using a BGC, if poor back flow is not paid attention to, it may migrate distally when antegrade blood flow is restarted after deflating the BGC or when a contrast medium is administered via the BGC to validate whether recanalization is achieved. Otherwise, a BGC is often withdrawn completely under contact aspiration when back flow via the BGC is still poor after the BGC deflation, assuming that a dropped thrombus occludes the orifice or thrombi occlude the lumen of the BGC, although there are no reports on its safety. The method of BGC removal under aspiration may be performed in most centers and quite safe in a case of thrombus occlusion within the BGC lumen. However, if no or not enough recanalization was found on subsequent angiography, the BGC has to be redeployed for another MT and the time for the redeployment is wasted. In cases with massive dropped thrombi, in addition, there may be a risk of distal migration of dropped thrombus fragments separated by the friction with the vessel wall and/or antegrade blood flow while withdrawing the deflated BGC together with the dropped thrombi even under constant aspiration from the BGC. If dropped thrombus is not completely removed by the single BGC removal procedure, there is a risk of distal embolization by antegrade blood flow and at the same time, the time to deploy the BGC again for subsequent MT is wasted. Thus, we devised the RAD² technique to solve the problem and decided to introduce it.

The advantage of the RAD² technique is to let us know not only the extent of recanalization but also the presence and the volume of a dropped thrombus, allowing us to consider what to do next. For instance, if successful reperfusion and no dropped thrombus are shown, we should remove the BGC because it may indicate poor collateral flow through anterior/posterior communicating artery or intraluminal obstruction of the BGC. When there are massive thrombi found at the BGC tip, we can consider the way to remove them while avoiding distal embolization as much as possible. The RAD² technique itself has a low risk of distal embolization: both the deployment of a microcatheter and the angiography to detect dropped thrombi are performed under manual aspiration from the inflated BGC which blocks antegrade blood flow. Immediately following the RAD² technique, the dropped thrombi also can be retrieved with antegrade blood flow blocked by the inflated BGC to avoid distal embolization, by the procedures such as crushing with guidewire followed by the aspiration: if insufficient recanalization is found, another MT can be performed immediately as well. In short, the RAD² technique can show the cause of poor back flow from the BGC and enables countermeasures according to the cause while keeping the BGC inflated, possibly leading to a lower risk of EDT/ENT and serving to save total time until successful recanalization.

Intra-arterial pressure can increase with the administration of a contrast medium, inducing arterial injury. ¹³ Particularly when a large vessel remains occluded in MT, angiography via an inflated BGC can cause arterial injury directly associated with fatal complications or can push a thrombus distally, leading to difficulty in removing it in the subsequent MT procedures. ¹⁴ However, the RAD² technique may be able to avoid the elevated intra-arterial pressure since the administration of a contrast medium is performed via a microcatheter with the proximal side of a BGC open, and this is considered another advantage of this method. Further large-scale studies are needed to demonstrate the usefulness of the RAD² technique.

Conclusion

The authors developed a novel technique referred to as the RAD² for detecting a dropped thrombus at the BGC tip after SR or AC withdrawal. The technique allows us to retrieve a dropped thrombus with subsequent MT procedures while maintaining the BGC inflated and it may be useful for reducing the risk of EDT/ENT.