Late spontaneous recanalization of symptomatic atheromatous internal carotid artery occlusion

Introduction

Definitive treatment of symptomatic chronic atheromatous internal carotid artery (ICA) occlusion remains controversial, as far as in rare cases, late spontaneous recanalization has been described. We describe therapeutic attitude according to usual care in seven patients with late recanalization (>3 months), and we review similar cases described in the literature.

Methods

We studied consecutive patients with ischemic stroke admitted to the University Hospital of Oviedo (Spain) from January 2003 to August 2012. Inclusion criteria were ischemic stroke in the ICA territory, diagnosis of ICA occlusion during hospitalization using angiographic sequences of magnetic resonance angiography (MRA) or computed tomography angiography (CTA), and atheromatous etiology. Exclusion criteria were interventional treatment at the time of admittance or during hospitalization, patients with previously known ICA occlusion, and ICA occlusion of etiology other than atheromatous. Patients with a diagnosis of ICA occlusion made using duplex echography without confirmation by other angiographic study were also excluded. After discharge, patients were followed up by carotid duplex. We defined late recanalization as more than three months from the initial diagnosis. If recanalization was suspected, a complementary angiographic study (MRA or CTA) was performed in order to avoid the possibility of mistaking a near occlusion of the ICA by echography. Because of its cost, availability, and efficacy, CTA was more frequently used than MRA. The CTA was obtained with a 64 multidetector-array technology in helicoidal with slice thickness 1.25 mm. Acquisition delay depended on the bolus test of 20 mL (15–20 s). Helical acquisition that started from the aortic arch to the circle of Willis was initiated 20 s after the start of injecting 120-mL nonionic contrast medium. Projections were reconstructed in axial, sagittal, and coronal planes. All images were analyzed by a neuroradiologist.

Results

An ICA occlusion was diagnosed in 182 patients; of these, symptomatic ICA occlusion was diagnosed in 162 patients. Eighteen (18/162) patients needed mechanical (17/18) or surgical (1/18) recanalization. Three (3/162) patients died due to an extensive hemispheric stroke (one of them after surgical treatment). Eight of 162 patients presented with dissection of the ICA, and 136/162 patients presented atheromatous ICA occlusion. Of the latter, seven patients presented a late spontaneous recanalization of the ICA (Figures 1 to 3). The cases are summarized in Table 1. OPEN IN VIEWER

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Figure 3.

Patient 5—longitudinal sections of CT angiography showed a left ICA occlusion (a) and recanalization (b) (white arrows).

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Table 1.

Patients with late spontaneous recanalization in our center.

Patient	Sex	Age	Symptomatology	Initial treatment	Date of occlusion	Brain CT at admission	Collateralization	Treatment	Date of recanalization	Control brain CT	Definitive treatment	Outcome
1	Male	78 y	Transient aphasia and right hand paresis	ASA 100 +  LMWH 0.4	15 June 2003	Chronic bilateral lacunar stroke	ComAA, bilateral ComPA	Clopidogrel + ASA 100 + simvastatin	17 December 2009	Bilateral lacunar infarction	Medical treatment	Clinically stable since then
2	Male	67 y	Aphasia and right hemiparesis	ASA 300 +  LMWH 0.6	17 June 2008	Chronic left anterior watershed and subacute MCA stroke	Ophthalmic artery, ComAA, left ComPA	ASA 300 + LMWH 0.8/24 +  atorvastatin 80	17 February 2009	Chronic cortical and subcortical lesions in left MCA territory	Left carotid endarterectomy after new left stroke	Clinically stable since then
3	Male	79 y	Language disturbances	ASA 300 +  LMWH 0.6	19 February 2008	Leukoaraiosis and atrophy	Ophthalmic artery, ComAA	ASA 300 +  atorvastatin 20	06 August 2010	Leukoaraiosis and atrophy	Stenting on the left side	Clinically stable since then
4	Female	66 y	Left hemiparesis	ASA 300 +  LMWH 0.6	19 May 2008	Subacute subcortical right MCA stroke	Ophthalmic artery, right ComPA	ASA 300, LMWH 0.6, atorvastatin 40	11 February 2009	Chronic subcortical right MCA stroke	Medical treatment	Clinically stable since then
5	Male	86 y	Left hemiparesis	Clopidogrel +  LMWH 0.6	22 December 2008	Leukoaraiosis and atrophy	Ophthalmic artery, bilateral ComPA, ComAA	Clopidogrel	26 January 2012	Leukoaraiosis and atrophy	Medical treatment	Clinically stable since then
6	Male	64 y	Aphasia and right arm paresis	ASA 300 +  LMWH 0.6	15 December 2009	Subacute left watershed stroke (anterior, posterior and deep)	Ophthalmic artery, left ComPA	ASA 300, atorvastatin 40	28 March 2011	Chronic left watershed stroke (anterior, posterior and deep)	Medical treatment	Clinically stable since then
7	Female	86 y	Dysarthria and left hemiparesis	ASA 300 +  LMWH 0.6	10 May 2009	Subacute right watershed stroke (posterior and deep)	Ophthalmic artery, no ComAA	Clopidogrel	03 January 2011	Right hemispheric atrophy	Medical treatment	Ovarian cystadenocarcinoma (died months later)

y

: years; ComPA: communicating posterior artery; ComAA: communicating anterior artery; ASA: acetyl salicylic acid; LMWH: low-molecular-weight heparin; CT: computed tomography; MCA: middle cerebral artery.

Discussion

Spontaneous late recanalization of atheromatous chronic ICA occlusion may be due to the natural fibrinolysis of superimposed occlusion in the setting of pre-existing severely stenotic ICA ¹ or due to the presence of the vasa vasorum providing collateral circulation. ² Apart from that, other factors take part in the recanalization: mechanism of occlusion, site of the occlusion, clot-size, composition, and age of the thromboembolic material. For all of these aspects, a late recanalization of atheromatous ICA occlusion is not a frequent event.

The best management of this unusual condition remains unclear, as little data have been reported in the literature (Table 2).^1,3–7 Whether these patients should receive the same treatment as patients with asymptomatic ICA stenosis remains unknown, as far as patients who suffered from an ipsilateral ischemic event longer than six months are currently classified as asymptomatic. ⁸

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Table 2.

Patients described in the literature with late recanalization of previous internal carotid artery (ICA) occlusion.

Author	Sex	Age	Symptomatology	Diagnostic method	Arterial pathology	Treatment	Time of recanalization	Diagnostic method	Symptoms at recanalization	Definitive treatment	Pathological study
Shah et al. 1	Male	74 y	Right hemiparesis	Carotid duplex confirmed by CTA	Left ICA occlusion	Medical treatment	8 months	Carotid duplex	Syncope	Left carotid endarterectomy	Atherosclerotic plaque
Som and  Schanzer 3	Female	58 y	Right hemiparesis, aphasia	Carotid duplex confirmed by MRA	Left ICA occlusion, 40–60% stenosis right ICA	ASA, Clopidogrel, statins	4 months	Carotid duplex and MRA	Asymptomatic	Left carotid endarterectomy	No
Matic et al. 4	Male	64 y	Left hemiparesis	CTA	Right ICA occlusion, severe stenosis left ICA	Left carotid endarterectomy, ASA, statins	2 years	Carotid duplex and CTA	Asymptomatic	Right carotid endarterectomy	Fibrous plaque (no intraplaque hemorrhage)
Klonaris et al. 5	Male	73 y	Right arm paresis and right  facial paresis	Carotid duplex confirmed by angiography	Left ICA occlusion	Clopidogrel	1 year	Carotid duplex and angiography	Asymptomatic	Left carotid endarterectomy	Hard plaque (no intraplaque hemorrhage)
Buslovich and  Schanzer 6	Male	85 y	Right-hand side weakness  and numbness	Digital subtraction angiogram	Left ICA occlusion	Medical treatment	1 year and 2 months	MRA	Ipsilateral TIAs	Left carotid endarterectomy	Atherosclerotic plaque
	Male	67 y	Left hemispheric transient attacks	MRA	Left ICA occlusion	Coumadin	2 years and 9 months	Carotid duplex and MRA	Asymptomatic	Medical treatment	No
	Male	75 y	Multiple cardiovascular risk factors	Carotid duplex	Left ICA occlusion	Medical treatment	5 years	Carotid duplex and MRA	Asymptomatic	Carotid endarterectomy	Calcified atherosclerotic plaque
Camporese  et al. 7	Female	66 y	Ipsilateral TIA	Carotid duplex and angiography	Left ICA occlusion	ASA	1 year and 5 months	Carotid duplex and angiography	Contralateral TIA	Warfarin	No
	Male	67 y	Amaurosis fugax	Carotid duplex	Left ICA occlusion	Clopidogrel	11 months	Carotid duplex and angiography	Asymptomatic	Clopidogrel	No
	Female	70 y	Ipsilateral TIA	Carotid duplex and angiography	Right ICA occlusion	ASA	6 months	Carotid duplex and angiography	Asymptomatic	ASA	No
	Female	55 y	Ipsilateral TIA	Carotid duplex and angiography	Right ICA occlusion	ASA	7 years and 4 months	Carotid duplex	Asymptomatic	ASA	No
	Male	65 y	Ipsilateral stroke	Carotid duplex and angiography	Right ICA occlusion	ASA	7 years and 10 months	Carotid duplex and angiography	Asymptomatic	ASA	No

In patients with asymptomatic ICA stenosis, medical treatment alone seems to be the best treatment for stroke prevention.^9,10 However, recent studies which focused on the asymptomatic ICA stenosis support the idea that the combination of several factors may identify patients who will benefit from other therapeutic approaches apart from medical treatment. A complex atherosclerotic carotid plaque,^11–13 positive cerebral CT findings such as silent infarcts,^11–14 the degree of the carotid stenosis,^11–13,15 disturbances in cerebral vasoreactivity, ¹³ or history of contralateral transient ischemic attacks ¹⁵ may identify those patients who will need interventional treatment.^11–13 Moreover, patients with previous symptomatic carotid artery pathology would have a relatively unstable carotid plaque composition, with higher prevalence of intraplaque hemorrhage, compared with patients who have never experienced ipsilateral events. ⁸ It would suggest that patients with past events might have different long-term ipsilateral stroke risks. ⁸ For this reason, and due to the possibility of recanalization, patients with symptomatic atheromatous chronic ICA occlusion should deserve further attention.

After reviewing previously published clinical cases, medical treatment seems to be as effective as interventional treatment in these patients. Although these studies were performed in the chronic phase when thrombus could have disappeared, pathological studies described in the literature show atheromatous fibrous plaques or calcified carotid plaques without any sign of unstable carotid pathology.^1,4–6 In addition to patients with asymptomatic carotid pathology, ischemic cerebrovascular events have been described in these patients with late recanalization: an ipsilateral ischemic event, such as the case described by Buslovich and Hines ⁶ or our second patient, or contralateral ischemic stroke, such as the case described by Camporese et al. ⁷ or our first patient, supports that in some cases, the prognosis would not be as benign as expected. Revascularization techniques should be considered in these cases to improve not only the ipsilateral hemispheric circulation but also the collateral circulation to the contralateral hemisphere.

The authors attempt to highlight the unusual condition of recanalization after a symptomatic atheromatous chronic ICA occlusion. If these patients can be treated similar to patients with asymptomatic carotid pathology, then this needs to be clarified. More studies are needed to establish the most appropriate therapeutical approach in order to avoid arbitrary treatment in these patients. OPEN IN VIEWER