Original Article doi: 10.1111/joim.12318
Symptomatic carotid near-occlusion with full collapse might cause a very high risk of stroke E. Johansson1, K. € Ohman2 & P. Wester3 From the1Department of Pharmacology and Clinical Neuroscience and Department of Public Health and Clinical Medicine; 2Department of Radiation Sciences; and 3Department of Public Health and Clinical Medicine, Ume a University, Ume a , Sweden
€ Abstract. Johansson E, Ohman K, Wester P (Ume a University, Ume a; Ume a University, Ume a; Ume a University, Ume a; Sweden). Symptomatic carotid near-occlusion with full collapse might cause a very high risk of stroke. J Intern Med 2015; 277: 615–623. Background. The risk of early stroke recurrence amongst patients with symptomatic carotid nearocclusion with and without full collapse is unknown. Therefore, the aim of this study was to analyse the 90-day risk of recurrent ipsilateral ischaemic stroke in patients with symptomatic carotid nearocclusion both with and without full collapse. Methods. This study was a secondary analysis of the Additional Neurological SYmptoms before Surgery of the Carotid Arteries: a Prospective study (ANSYSCAP). We prospectively analysed 230 consecutive patients with symptomatic 50–99% carotid stenosis or near-occlusion. Based on the combination of several imaging modalities, 205 (89%) patients were classified as having 50–99% carotid stenosis, and 10 (4%) and 15 (7%) as having near-occlusion with and without full collapse, respectively. The
Introduction Carotid near-occlusion is a tight carotid stenosis where the lumen distal to the stenosis is reduced [1,2]. The collapse is severe in some cases of nearocclusion, resulting in a thread-like lumen distal to the stenosis, that is ‘full collapse’ [1]. However, in many cases of near-occlusion, this collapse is more moderate, that is ‘near-occlusion without full collapse’, which can easily be mistaken on angiography for 50–99% carotid stenosis [1–3]. Near-occlusion with and without full collapse are differentiated on angiography by visual assessment [1] (see Fig. 1). Several terms have been used to describe carotid near-occlusion: pseudoocclusion, incomplete
90-day risk of recurrent ipsilateral ischaemic stroke was compared between these three groups. Only events that occurred before carotid endarterectomy were analysed. Results. The 90-day risk of recurrent stroke was 18% [95% confidence interval (CI) 12–25%; n = 29] for patients with 50–99% carotid stenosis, 0% for patients with near-occlusion without full collapse and 43% (95% CI 25–89%; n = 4) for patients with near-occlusion with full collapse (P = 0.035, logrank test). The increased risk of recurrent ipsilateral ischaemic stroke for patients with symptomatic near-occlusion with full collapse remained significant after multivariable adjustment for age, sex and type of presenting event. Conclusions. Patients with symptomatic carotid nearocclusion with full collapse might have a very high risk of stroke recurrence. Carotid endarterectomy could be considered for these patients. Keywords: carotid near-occlusion, carotid stenosis, CEA, risk, stroke.
occlusion, subtotal occlusion, small distal internal carotid artery, poststenotic narrowing, string sign and slim sign [1]. The term near-occlusion with or without ‘string sign’ is more commonly used than near-occlusion with or without full collapse; however, we believe that the use of ‘string sign’ should be discouraged because it was originally defined for describing dissection, not atherosclerotic disease [4]. The difference between near-occlusion with and without full collapse was introduced in a North American Symptomatic Carotid Endarterectomy Trial (NASCET) analysis in 1997 [5] and characterized in more detail in 2005 [1]. Prognostic studies before 1997 mostly included cases with severe distal collapse, which today is classified as
ª 2014 The Association for the Publication of the Journal of Internal Medicine
615
E. Johansson et al.
Carotid near-occlusion
full collapse accounted for only a small minority of the population (6%; n = 16); the rest had nearocclusion without full collapse [1]. The findings from the NASCET and ECST, that the risk of stroke without CEA was low and the benefit of CEA was small, are only applicable to cases of near-occlusion without full collapse [1]. However, for the few cases with full collapse that were included, it was reported that the risk of recurrent stroke was low [1, 5]. The high-risk period (the first days after the presenting event) was not studied in the NASCET and ECST, but a trend towards increased benefit with CEA was seen amongst the 128 patients with near-occlusion who entered the study within 4 weeks compared to those that entered the study after 4 weeks [8]. To date, no data on the risk of early stroke recurrence for symptomatic nearocclusion have been presented.
(a)
(b)
The aim of this study was to analyse the risk of recurrent ipsilateral ischaemic stroke in the first 90 days after the presenting event in patients with symptomatic carotid near-occlusion with and without full collapse. Materials and methods Study population
Fig. 1 Computed tomography angiography of near-occlusion with full collapse (a) and near-occlusion without full collapse (b). In both examples, all four criteria for nearocclusion [2] are met. a, the distal internal carotid artery (ICA) lumen is 0.99 mm, the ICA/ICA ratio is 0.26, the ICA/external carotid artery (ECA) ratio is 0.43 and the stenosis lumen (not depicted) is 0.32 mm. b, the distal ICA lumen is 2.5 mm, the ICA/ICA ratio is 0.63, the ICA/ECA ratio is 1.09 and the stenosis lumen (not depicted) is 1.2 mm. In both panels, the thick black arrow shows the ICA distal to the stenosis, the white arrowhead shows the contralateral ICA and the thin black arrow shows the ECA. In cases of near-occlusion with full collapse, two similarly appearing parallel arteries should be identified, the distal ICA and the ascending pharyngeal artery (thick white arrow in panel a), to exclude carotid occlusion with the ascending pharyngeal artery misinterpreted as a threadlike ICA.
near-occlusion with full collapse [4, 6, 7]. In one of these early studies, urgent carotid endarterectomy (CEA) was considered mandatory [4]. However, in the pooled analysis of the NASCET and European Carotid Surgery Trial (ECST), near-occlusion with 616
ª 2014 The Association for the Publication of the Journal of Internal Medicine Journal of Internal Medicine, 2015, 277; 615–623
This study is a secondary analysis of Additional Neurological SYmptoms before Surgery of the Carotid Arteries: a Prospective study (ANSYSCAP) [9]. Briefly, we prospectively included 230 consecutive patients with symptomatic 50–99% carotid stenosis at the Ume a Stroke Center at Norrlands University Hospital (NUH), Sweden, between 1 August 2007 and 31 December 2009. Overall, 81% of the included patients were referred from 11 hospitals. Only patients who were initially considered to be eligible for CEA were included (i.e. patients healthy enough to undergo a preoperative evaluation for CEA). Therefore, as this was a selected population, the CEA rate was high (80%). All patients were treated with either antiplatelet or anticoagulant medication; in addition, 93% were treated with antihypertensive agents and 90% were treated with lipid-lowering drugs during the study period. The primary end-point was a recurrent ipsilateral ischaemic stroke or an ipsilateral retinal artery occlusion that occurred after the presenting event, but before CEA. The primary end-point did not include transient ischaemic attack (TIA) or amaurosis fugax. The observation period for the primary end-point was the first 90 days after the presenting event; for patients
E. Johansson et al.
who underwent CEA within 90 days, the observation was terminated at the time of surgery. In the primary analysis, no difference between 50–69% and 70–99% carotid stenosis was detected (P = 0.66, log-rank test). A few cases of nearocclusion were identified before the review of all examinations performed in this analysis; in the primary analysis, these cases of near-occlusion were grouped with the cases of 70–99% carotid stenosis. The study was registered at http://www. clinicaltrials.gov (NCT 00514592) before initiation. Imaging procedures Carotid ultrasound was performed in 98% (225/ 230) of the included patients at the Department of Physiology at NUH, according to our standard clinical routine that all referred patients are re-examined with carotid ultrasound. Experienced ultrasound examiners performed the carotid ultrasound. The presence of a visible plaque in B-mode and a peak systolic velocity of either 1.50–2.45 or >2.45 m s 1 defined 50–69% or 70–99% stenosis, respectively [10]. Stenosis was regarded as nearocclusion with full collapse if all three of the following criteria were met: (i) a very pronounced plaque seen in B-mode with only a narrow flow channel on colour Doppler; (ii) a low (
Symptomatic carotid near-occlusion with full collapse might cause a very high risk of stroke E. Johansson1, K. € Ohman2 & P. Wester3 From the1Department of Pharmacology and Clinical Neuroscience and Department of Public Health and Clinical Medicine; 2Department of Radiation Sciences; and 3Department of Public Health and Clinical Medicine, Ume a University, Ume a , Sweden
€ Abstract. Johansson E, Ohman K, Wester P (Ume a University, Ume a; Ume a University, Ume a; Ume a University, Ume a; Sweden). Symptomatic carotid near-occlusion with full collapse might cause a very high risk of stroke. J Intern Med 2015; 277: 615–623. Background. The risk of early stroke recurrence amongst patients with symptomatic carotid nearocclusion with and without full collapse is unknown. Therefore, the aim of this study was to analyse the 90-day risk of recurrent ipsilateral ischaemic stroke in patients with symptomatic carotid nearocclusion both with and without full collapse. Methods. This study was a secondary analysis of the Additional Neurological SYmptoms before Surgery of the Carotid Arteries: a Prospective study (ANSYSCAP). We prospectively analysed 230 consecutive patients with symptomatic 50–99% carotid stenosis or near-occlusion. Based on the combination of several imaging modalities, 205 (89%) patients were classified as having 50–99% carotid stenosis, and 10 (4%) and 15 (7%) as having near-occlusion with and without full collapse, respectively. The
Introduction Carotid near-occlusion is a tight carotid stenosis where the lumen distal to the stenosis is reduced [1,2]. The collapse is severe in some cases of nearocclusion, resulting in a thread-like lumen distal to the stenosis, that is ‘full collapse’ [1]. However, in many cases of near-occlusion, this collapse is more moderate, that is ‘near-occlusion without full collapse’, which can easily be mistaken on angiography for 50–99% carotid stenosis [1–3]. Near-occlusion with and without full collapse are differentiated on angiography by visual assessment [1] (see Fig. 1). Several terms have been used to describe carotid near-occlusion: pseudoocclusion, incomplete
90-day risk of recurrent ipsilateral ischaemic stroke was compared between these three groups. Only events that occurred before carotid endarterectomy were analysed. Results. The 90-day risk of recurrent stroke was 18% [95% confidence interval (CI) 12–25%; n = 29] for patients with 50–99% carotid stenosis, 0% for patients with near-occlusion without full collapse and 43% (95% CI 25–89%; n = 4) for patients with near-occlusion with full collapse (P = 0.035, logrank test). The increased risk of recurrent ipsilateral ischaemic stroke for patients with symptomatic near-occlusion with full collapse remained significant after multivariable adjustment for age, sex and type of presenting event. Conclusions. Patients with symptomatic carotid nearocclusion with full collapse might have a very high risk of stroke recurrence. Carotid endarterectomy could be considered for these patients. Keywords: carotid near-occlusion, carotid stenosis, CEA, risk, stroke.
occlusion, subtotal occlusion, small distal internal carotid artery, poststenotic narrowing, string sign and slim sign [1]. The term near-occlusion with or without ‘string sign’ is more commonly used than near-occlusion with or without full collapse; however, we believe that the use of ‘string sign’ should be discouraged because it was originally defined for describing dissection, not atherosclerotic disease [4]. The difference between near-occlusion with and without full collapse was introduced in a North American Symptomatic Carotid Endarterectomy Trial (NASCET) analysis in 1997 [5] and characterized in more detail in 2005 [1]. Prognostic studies before 1997 mostly included cases with severe distal collapse, which today is classified as
ª 2014 The Association for the Publication of the Journal of Internal Medicine
615
E. Johansson et al.
Carotid near-occlusion
full collapse accounted for only a small minority of the population (6%; n = 16); the rest had nearocclusion without full collapse [1]. The findings from the NASCET and ECST, that the risk of stroke without CEA was low and the benefit of CEA was small, are only applicable to cases of near-occlusion without full collapse [1]. However, for the few cases with full collapse that were included, it was reported that the risk of recurrent stroke was low [1, 5]. The high-risk period (the first days after the presenting event) was not studied in the NASCET and ECST, but a trend towards increased benefit with CEA was seen amongst the 128 patients with near-occlusion who entered the study within 4 weeks compared to those that entered the study after 4 weeks [8]. To date, no data on the risk of early stroke recurrence for symptomatic nearocclusion have been presented.
(a)
(b)
The aim of this study was to analyse the risk of recurrent ipsilateral ischaemic stroke in the first 90 days after the presenting event in patients with symptomatic carotid near-occlusion with and without full collapse. Materials and methods Study population
Fig. 1 Computed tomography angiography of near-occlusion with full collapse (a) and near-occlusion without full collapse (b). In both examples, all four criteria for nearocclusion [2] are met. a, the distal internal carotid artery (ICA) lumen is 0.99 mm, the ICA/ICA ratio is 0.26, the ICA/external carotid artery (ECA) ratio is 0.43 and the stenosis lumen (not depicted) is 0.32 mm. b, the distal ICA lumen is 2.5 mm, the ICA/ICA ratio is 0.63, the ICA/ECA ratio is 1.09 and the stenosis lumen (not depicted) is 1.2 mm. In both panels, the thick black arrow shows the ICA distal to the stenosis, the white arrowhead shows the contralateral ICA and the thin black arrow shows the ECA. In cases of near-occlusion with full collapse, two similarly appearing parallel arteries should be identified, the distal ICA and the ascending pharyngeal artery (thick white arrow in panel a), to exclude carotid occlusion with the ascending pharyngeal artery misinterpreted as a threadlike ICA.
near-occlusion with full collapse [4, 6, 7]. In one of these early studies, urgent carotid endarterectomy (CEA) was considered mandatory [4]. However, in the pooled analysis of the NASCET and European Carotid Surgery Trial (ECST), near-occlusion with 616
ª 2014 The Association for the Publication of the Journal of Internal Medicine Journal of Internal Medicine, 2015, 277; 615–623
This study is a secondary analysis of Additional Neurological SYmptoms before Surgery of the Carotid Arteries: a Prospective study (ANSYSCAP) [9]. Briefly, we prospectively included 230 consecutive patients with symptomatic 50–99% carotid stenosis at the Ume a Stroke Center at Norrlands University Hospital (NUH), Sweden, between 1 August 2007 and 31 December 2009. Overall, 81% of the included patients were referred from 11 hospitals. Only patients who were initially considered to be eligible for CEA were included (i.e. patients healthy enough to undergo a preoperative evaluation for CEA). Therefore, as this was a selected population, the CEA rate was high (80%). All patients were treated with either antiplatelet or anticoagulant medication; in addition, 93% were treated with antihypertensive agents and 90% were treated with lipid-lowering drugs during the study period. The primary end-point was a recurrent ipsilateral ischaemic stroke or an ipsilateral retinal artery occlusion that occurred after the presenting event, but before CEA. The primary end-point did not include transient ischaemic attack (TIA) or amaurosis fugax. The observation period for the primary end-point was the first 90 days after the presenting event; for patients
E. Johansson et al.
who underwent CEA within 90 days, the observation was terminated at the time of surgery. In the primary analysis, no difference between 50–69% and 70–99% carotid stenosis was detected (P = 0.66, log-rank test). A few cases of nearocclusion were identified before the review of all examinations performed in this analysis; in the primary analysis, these cases of near-occlusion were grouped with the cases of 70–99% carotid stenosis. The study was registered at http://www. clinicaltrials.gov (NCT 00514592) before initiation. Imaging procedures Carotid ultrasound was performed in 98% (225/ 230) of the included patients at the Department of Physiology at NUH, according to our standard clinical routine that all referred patients are re-examined with carotid ultrasound. Experienced ultrasound examiners performed the carotid ultrasound. The presence of a visible plaque in B-mode and a peak systolic velocity of either 1.50–2.45 or >2.45 m s 1 defined 50–69% or 70–99% stenosis, respectively [10]. Stenosis was regarded as nearocclusion with full collapse if all three of the following criteria were met: (i) a very pronounced plaque seen in B-mode with only a narrow flow channel on colour Doppler; (ii) a low (
