Carotid endarterectomy in patients with contralateral carotid occlusion: a 10-year experience
(Portuguese PDF version)

Telmo Pedro Bonamigo,1 Elton Luiz Schmidt Weber,2 Márcio Luís Lucas,3 Claudia Bianco,4 Marco Aurélio Cardozo4

1. Associate professor, Angiology and Vascular Surgery, Fundação Faculdade Federal de Ciências Médicas de Porto Alegre (FFFCMPA), Brazil. Chief of Vascular Surgery Service, Santa Casa de Misericórdia de Porto Alegre, Porto Alegre, RS, Brazil.
2. M.Sc. in Medical Sciences, FFFCMPA, Porto Alegre, RS, Brazil.
3. Resident physician, Vascular Surgery Service, Santa Casa de Misericórdia de Porto Alegre, Porto Alegre, RS, Brazil.
4. M.Sc. in Vascular Surgery.

Correspondence:
Telmo Pedro Bonamigo
Santa Casa de Misericórdia de Porto Alegre
Rua Prof. Annes Dias, 285 - 2° andar - Serviço de Cirurgia Vascular
CEP 90020-090 - Porto Alegre, RS
Brazil
Phone: +55 (51) 3214.8076
E-mail: telmobonamigo@terra.com.br


ABSTRACT

Objective To evaluate the results of carotid endarterectomy in patients with contralateral carotid occlusion, comparing them to reports available in literature.

Method: Medical protocols and records of all patients who underwent carotid endarterectomy from January 1993 to June 2003 were reviewed. Out of 663 carotid endarterectomies which were performed, 61 cases (9.2%) were selected because they involved contralateral carotid occlusion. Most patients were male (73.8%), with an average age of 68.2 years. Main risk factors for cerebrovascular disease were arterial hypertension (70.4%) and smoking habit (72.1%). Fifty-one patients (83.6%) presented with preoperative neurological symptoms, most of them related to carotid stenosis (55%). Most patients underwent standard carotid endarterectomy with intraluminal shunt (88.5%) and patch closure (96.2%).

Results:
Two patients (3.3%) had hematoma and were reoperated promptly. Postoperative rates of major stroke, myocardial infarction and death were 1.6%, 4.9% and 4.9%, respectively. Causes of perioperative deaths were myocardial infarction (two patients) and stroke (one patient).

Conclusion:
Our study concluded that carotid endarterectomy can be performed in patients with contralateral carotid occlusion with acceptable stroke and death rates (4.9%), which are much lower than the rate presented by the NASCET study (14.3%) in 1991. Review of reports published after 1990 also found morbidity and mortality rates lower than those reported by the NASCET study.

Key-words: carotid endarterectomy, cerebrovascular accident, pathologic constriction.
Palavras-chave: endarterectomia das carótidas, acidente vascular cerebral, estenose.

J Vasc Br 2004;3(3):197-205


Indications for endarterectomy in symptomatic and asymptomatic patients with carotid stenosis are well established, and results based on randomized clinical trials are well known.1-4 However, the influence of occluded contralateral carotid artery remains a controversial issue concerning surgical outcomes, and it seems to increase the risk of perioperative neurological events.5 Clinical progress of contralateral carotid occlusion (CCO) is still uncertain, and it is difficult to predict which patients will suffer a cerebral infarction and which will remain symptom-free.6 Although the Joint Study of Extracranial Arterial Occlusion,7 published in 1976, supported that medical therapy alone is the best choice for patients with carotid stenosis and CCO, many contemporary studies have been reporting that carotid endarterectomy (CEA) is a safe procedure for these patients, with results similar to those obtained for patients with patent contralateral carotid artery.8-17 Nevertheless, the North American Symptomatic Carotid Endarterectomy Trial (NASCET) presented some counter-evidence against such results; their group of patients with CCO presented a stroke rate of 14.3%, leading some authors18 to indicate carotid stenting for such patients due to increased perioperative risk.1

The aim of the present study was to review our 10-year experience with CEA in order to evaluate surgical morbidity and mortality rates of 61 patients with carotid stenosis and CCO and to compare surgical results with those found in literature.

CASES AND METHOD

Out of a group of 663 patients who underwent CEA at the Vascular Surgery Service of Santa Casa de Misericórdia de Porto Alegre (Brazil) from January 1993 to June 1993 (all performed by the first author), 61 (9.2%) patients were selected for this study. They presented with internal carotid artery stenosis of at least 70% and CCO evidenced by color Doppler ultrasound and confirmed by magnetic resonance or arteriography. Information concerning demography, comorbidities, surgical indications and perioperative complications was available for all patients.

The standard surgical procedure performed in all patients involved general anesthesia and systemic heparinization prior to clamping. Standard CEA was performed with intraluminal shunts inserted in most patients (88.5%), except for seven cases, in which blood reflux was exuberant or in which shunt did not remain in place or could not be inserted. Use of patch for vessel closure was performed in all female patients, but only when carotid artery had less than 4 mm in diameter for male patients.

Considering all patients who underwent CEA at our service, 9.2% had CCO. Average age of patients was 68.2 years (ranging from 43 to 86 years). Forty-five patients (73.8%) were male. Associated risk factors were smoking habit (44 patients, 72.1%), arterial hypertension (43 patients, 70.4%), ischemic heart diseases (24 patients, 39.4%) and diabetes mellitus (14 patients, 22.9%) (Table 1).

click hereTable 1 - Comorbidities of 61 patients with CCO who underwent CEA

Comorbidities n %
Smoking habit 44 72.1
Arterial hypertension 43 70.4
Ischemic heart diseases 24 39.4
Diabetes mellitus 14 22.9
CCO = contralateral carotid occlusion; CEA = carotid endarterectomy.

Twenty-one patients (34.4%) reported history of previous neurological event on the same side of the occluded carotid artery. Twenty-eight patients (45.9%) reported previous history of neurological symptoms related to stenotic carotid artery. Vertebrobasilar insufficiency was observed in 11 patients (18%); this symptom was the only clinical manifestation in two cases (3.3%). The nine remaining patients had associated symptoms in carotid artery. Ten patients (16.4%) were considered to be asymptomatic because they did not have history of any neurological event before surgery (Table 2).

click hereTable 2 - Surgical indications for 61 patients with CCO who underwent CEA

n %
Carotid symptoms
Ipsilateral (surgery) 28 45.9
TIA/amaurosis fugax 18 29.5
Stroke 10 16.4
Contralateral (surgery)

21 34.4
Vertebrobasilar symptoms
Single manifestation 2 3.3
Associated symptoms in carotid artery 9 14.8
Asymptomatic 10 16.4
CCO = contralateral carotid occlusion; CEA = carotid endarterectomy; TIA = transient ischemic attack.

Fifty-two patients (85.3%) underwent standard CEA; intraluminal shunt was used in 46 patients (88.5%). Such technique was not employed in the remaining six patients (11.5%) because of intense blood flow from internal carotid artery or because of difficulty in inserting or maintaining the shunt in place. Nine patients underwent eversion CEA due to occurrence of kinking and internal carotid stenosis. Cerebral protection was provided by placement of a shunt in eight out of these nine patients (88.8%) (Table 3).

click hereTable 3 - Intraluminal shunting according to surgical technique employed

Surgical technique n (%) Shunt (%)
Standard 52 (85.3) 46 (88.5)
Eversion 9 (14.7) 8 (88.8)
Total 61 (100) 54 (88.5)

Patch closure was performed in 50 patients (96.2%) with a segment of greater saphenous vein in 36 patients (72%), synthetic prosthesis (Dacron) in 10 patients and bovine pericardium in four patients. Primary closure was performed in two patients (3.8%) (Table 4). Five patients (8.2%) underwent simultanous CEA and myocardial revascularization.

click hereTable 4 - Use of patch after CEA in 52 patients with CCO

n %
With patch 50 96.2
Greater saphenous vein 36 72
Dacron prosthesis 10 20
Bovine pericardium 4 8
Without patch 2 3.8
CCO = contralateral carotid occlusion; CEA = carotid endarterectomy.

RESULTS

Local complications were observed in two patients (3.3%), requiring surgical reintervention for hematoma drainage. One of them had a good clinical progress after reintervention; the other underwent reoperation on the first postoperative day, when blood loss from the suture line was observed. Hypoxemic encephalopathy occurred, leading to severe neurological deficit (stroke) and death on the fourth postoperative day.

Three acute myocardial infarctions (AMI) occurred (4.9%), two of them culminating in fatal outcome (one of the patients had undergone simultaneous CEA and myocardial revascularization). Combined rate of stroke and death was 4.9%, the main cause of death being cardiac events (2/3 cases) (Tables 5 and 6). There were no cases of surgical wound infection, and injuries to peripheral nerves were not evaluated in the present study.

click hereTable 5 - Perioperative complications and deaths considering 61 patients with CCO who underwent CEA

  n %
Local complications
Hematoma 2 3.3
Cardiac events
AMI 3 4.9
Neurological events
Stroke 1 1.6
Cause of death
Cardiac 2 3.3
Neurological 1 1.6
Total 3 4.9
CCO = contralateral carotid occlusion; CEA = carotid endarterectomy;AMI: acute myocardial infarctions.

click hereTable 6 - Clinical outcome of patients who underwent CEA with major complications

Patient (sex, age) Clinical record Shunt Patch Complications Outcome
Male,
55 years
SAH, previous TIA No Vein Stroke (encephalopathy) Death 4th PO day
Male,
68 years
SAH, IHD, previous stroke Yes Bovine pericardium AMI Death 4th PO day
Female,
77 years
SAH, SMO, previous TIA Yes Eversion AMI 1st PO Good progress
Female,
64 years
SAH, IHD, SMO,
simultaneous MR
Yes Vein AMI Death 1st PO day
CEA = carotid endarterectomy; SAH: systemic arterial hypertension; PO: postoperative; IHD: ischemic heart disease; SMO: smoking habit; MR: myocardial revascularization surgery; MI: myocardial infarction.

DISCUSSION

Carotid artery occlusion may remain asymptomatic for a long time. However, it can become critical if contralateral carotid artery stenosis develops.6 Progress of patient with carotid occlusion is uncertain since it is difficult to predict which patients will suffer cerebral infarction and which will remain symptom-free.6,14 Clinical manifestations of patients with internal carotid artery thrombosis range from mild neurological events to death secondary to cerebral infarction.19 Nevertheless, during a severe neurological event it is difficult to know if carotid occlusion is the cause of current symptoms.14 It is estimated that 8 to 16% of patients with transient ischemic attack (TIA) present with CCO, with a 35% risk of progressing to stroke and a 50% risk of progressing to death.7 Some studies have been evidencing that patients with internal carotid occlusion (when surgically untreated) are at higher risk for stroke. Therefore, the Joint Study of Extracranial Arterial Occlusion, published in 1976, evidenced that 35% of patients with CCO suffered a stroke during a 51-month clinical follow-up.7 Furthermore, the International Cooperative Study of Extra-intracranial Bypass20 reported a stroke rate of 29% during a 55.8-month clinical follow-up. Other reports, such as Cote et al., mentioned annual stroke rates of 5% affecting the side of occluded artery and 8% affecting the side of stenotic artery.21 Today, the use of surgical technique for treating carotid artery stenosis may lead such figures to be as low as 0.4 and 2.8%, respectively.9

Patients with CCO are at higher risk for perioperative stroke because they present with a more advanced vascular disease, and their collateral circulation may be inadequate, leading them to be more prone to postoperative cerebral hyperperfusion syndrome.

At first, three techniques were recommended to treat patients diagnosed with CCO: medical therapy alone, leading to poor results in some cases;7 extracranial bypass, which was not always effective in reducing postoperative stroke rates;22 and carotid thromboendarterectomy, which was associated with high morbidity and mortality rates, as discussed in Murphy et al.23 (who reported postoperative neurological morbidity/mortality rate of 21% in 1965). Similarly, Heyman et al.24 reported 20 cases of surgically treated CCO; five patients suffered postoperative stroke and four died. These figures corresponded to a morbidity/mortality rate of 45%. Thus, nowadays surgeons do not try to perform carotid revascularization involving high morbidity/mortality rates anymore.

Ever since the 1980's, reports have been evidencing that patients with CCO may present with neurological symptoms related to any of the cerebral hemispheres, and that CEA performed on the stenotic artery is effective in providing long-term protection for both hemispheres against strokes.12,25,26

In 1974, Patterson et al.27 reported their experience with 23 patients presenting with CCO who underwent CEA on the stenotic artery; their morbidity/mortality rate was zero. Recently, NASCET reported a neurological morbidity rate of 14.3% in a group of patients presenting with CCO. Their sample was small (n = 21), and control group (under medical therapy alone) evidenced stroke rates of 56.4% at 2 years, a figure significantly higher than that of the group which underwent surgery (20.4%). Furthermore, all three cases of postoperative neurological events (two minor strokes and one major stroke) occurred in immediate postoperative period (only one related to the side of carotid occlusion). Only one of these patients required intraluminal shunting for cerebral protection, which can be regarded as a failure in providing cerebral protection for patients (Table 7). Along with such data, the study reported that stroke rates in patients with severe (70 to 90%) or mild-to-moderate (< 70%) contralateral carotid stenosis were 4 and 5.1% respectively. However, no statistical inference can be drawn from such figures comparing them to the rate of 14.3% of the CCO group, since the sample of patients with CCO was very small (21 patients).1,28

click hereTable 7 - Neurological events in patients with CCO who underwent CEA in NASCET study (21 patients)

Patient Neurological event Side Shunting
1 Stroke at 3rd PO hour Ipsilateral No
2 Stroke at 1st PO hour Ipsilateral No
3 Stroke at 1st PO hour Contralateral (occluded carotid) Yes
CCO = contralateral carotid occlusion; CEA = carotid endarterectomy.

Based on such unpromising results presented for the CCO group in NASCET study, the study by Mathur et al. is mentioned because it indicates carotid stenting for patients with CCO.18

On the other hand, there are many reports evidencing good results of CEA for patients with CCO, with morbidity/mortality rate lower than 7%, which is equivalent to results obtained for patients with patent contralateral carotid, with stroke and death rates similar to those reported by NASCET (5.5%) and by Asymptomatic Carotid Atherosclerosis Study (ACAS) (2%)5,6,8-10,12-19,29-33 (Table 8). These studies also evidenced long-term benefits, with stroke-free rates of 90% to 95% at five years9,12,26 and survival rates of 70% to 80%.9,12 Late death was mainly caused by myocardial infarctions and cancer.13,16 Therefore, indication of carotid stenting for patients with CCO based exclusively on a study with the above mentioned limitations seems not to have consistent scientific support. The occurrence of restenosis and complications inherent to carotid stenting is a reason for concern. According to Leger et al.,34 high rates of restenosis (75% of patients) at a mean follow-up of 20.2 months after carotid stenting indicate significant limitations of such procedure in terms of the results it provides.

click hereTable 8 - Results of recent reports on CEA in patients with CCO

Authors n Stroke (%) Death (%)
Mackey et al., 1990 63 4.8 0
Lesage et al., 1991 133 9.0 6.8
Mattos et al., 1992 66 3.0 1.5
Meyer et al., 1993 357 1.7 1.1
McCarthy et al., 1993 81 4.9 1.2
Deriu et al., 1994 61 1.7 0
Coyle et al., 1996 116 4.3 2.6
Samson et al., 1998 67 1.5 1.5
Pulli et al., 2002 82 2.4 0
Rockmann et al., 2002 338 3.0 0.6
Bonamigo et al., 2004 61 1.6 4.9
CCO = contralateral carotid occlusion; CEA = carotid endarterectomy.

Some technical details are relevant in order to achieve successful results in surgical treatment of patients with CCO. The outcome depends on the expertise of the surgeon and on surgical demand of the service in which the patient was admitted, given that services that perform less surgical procedures annually present higher surgical morbidity/mortality rates.35 Two of the largest reported series on surgical management of patients with CCO were published by groups from New York University and Mayo Clinic. Considering two different reports covering a 34-year experience (1965-1999),8,36 making up a total number of 518 patients with CCO, the Division of Vascular Surgery at New York University (supervised by Professor A. M. Imparato) achieved stroke rates of 4.05% and mortality rates of 0.9%, with local-regional anesthesia and selective intraluminal shunting in most cases. Satisfactory results were also reported by Meyer et al.,33 from Mayo Clinic, where 357 patients with CCO underwent CEA; stroke and death rates were 1.7 and 1.1% respectively.

Along with surgical expertise, some other technical details, such as use of intraluminal shunt and intraoperative monitoring of neurological status, use of patch for vessel closure, surgical technique used and anesthetic agent chosen are crucial for achieving good outcomes and assuring patients with CCO of surgical success.

Concerning intraluminal shunt, it was used in 88.5% of cases of the present report, and different points of view are found in literature. Some authors advocate routine intraluminal shunting in patients with CCO due to occasional inadequate collateral circulation.16,19,29 However, others support that shunt insertion does not interfere with postoperative results, and thus it is also indicated for patients without CCO.6 Authors who reported use of selective shunting affirm that routine use of such a procedure may lead to complications, such as problem in shunt insertion, air embolization and difficulty in performing endarterectomy.13 Nevertheless, such complications occur only when the surgeon is not used to using the device and did not undergo adequate training to use it. Furthermore, routine use of intraluminal shunt in patients with CCO is recommended, because up to 46% of them have changes in intraoperative electroencephalogram during carotid clamping, and up to 73% have inadequate blood reflux (retrograde pressure < 50 mmHg).9

Literature review evidenced that the use of selective shunting occurred in 10.3 to 89% of cases,5,11 being much more frequent in patients with CCO in most reports5,6,9,12,13,14,38 and in similar cases in other studies.15 Analyzing the review presented in Samson et al.31 about this topic, one can realize that most authors use selective shunting. Samson et al. reported stroke and death rates of 3% considering 67 patients with CCO who underwent CEA without shunt.31 Table 9 displays a summary of postoperative results according to frequency of shunting. Stroke rate in cases in which shunting was not used (6.2%) was 2-3 times greater than in cases in which selective shunting (2.3%) or routine shunting (3%) were performed, although mortality rates were similar in all groups.

click hereTable 9 - Results of CEA in patients with CCO, according to frequency of intraluminal shunting

Frequency Reports (n) Total number of patients Stroke (%) Death (%)
Never 8 389 6.2* 1.5
Selective 14 1,231 2.3 1.5
Always 5 403 3.0 1.0

*P < 0.05 when compared to Selective shunting group. Chi-square test.

One of the most likely causes of postoperative stroke is the absence of patch for vessel closure, which can lead to restenosis and increase in neurological complication rates. In the present study, patch closure was used in 96.2% of cases; this procedure is indicated by most authors, specially when carotid artery is less than 4 mm in diameter.13-15 Although some surgeons perform routine closure without patch,19 its use was found in 36 to 98% of the cases reported in literature;12,26 in some studies, there was no difference in frequency of use of patch closure in patients with and without CCO.6,11,16 Similarly to most reports, standard CEA was performed in the present study in most cases (85.3%). Nevertheless, some authors, such as Ballotta et al., performed eversion endarterectomy in approximately 1/3 of their patients in order to reduce risk of stroke due to restenosis.

Concerning anesthesia, most authors perform CEA under general anesthesia,5,6,11-13,15,16,30,37,38 although some prefer local-regional anesthesia, achieving good results.8,17,25

Considering demographic data of patients, some aspects deserve mentioning. In international literature, the frequency of patients with CCO in relation to all patients who underwent CEA ranged from 8 to 19%;5,11 in the present study, this frequency was 9.2% (61/663). Average age of our patients was 68.2 years; in literature, average age found ranged from 63 to 71 years.17,19 Literature review evidenced incidence of diabetes mellitus of 12 to 49%;5,15 incidence of systemic arterial hypertension of 33 to 76%;15,36 incidence of smoking habit of 24 to 84%;14,15 incidence of ischemic heart disease of 25 to 65%;14,15 incidence of congestive heart failure of approximately 10%;11 and incidence of peripheral arterial disease of up to 28%.6 Table 1 displays incidences of such risk factors in our series, evidencing that they are within the ranges established in literature. Note that, in some reports, the difference of incidence of such risk factors among patients with and without CCO was not statistically significant.9,13,14,16,31

Concerning surgical indications, 28 patients in our series presented with symptoms related to the stenotic carotid (which was operated), 21 patients presented with previous symptoms related to carotid occlusion and two patients presented with vertebrobasilar symptoms, making up 51 symptomatic patients (83.6%). Literature review evidenced frequency of symptomatic patients ranging from 24 to 93.1%,17,25 and frequency of symptoms associated with occluded carotid artery of approximately 40%.14,26,36 Prevalence of vertebrobasilar symptoms ranged from 3.3 to 13%.26,36 Furthermore, incidence of TIA ranged from 11 to 58%,13,17 previous history of stroke ranged from 11 to 50%,6,13 and incidence of amaurosis fugax ranged from 8 to 16%.6,11

A review of Brazilian literature on the topic, published by Índice Bibliográfico Brasileiro de Angiologia e Cirurgia Vascular, failed to find any article specifically on CEA in patients with CCO. Samson et al.31 analyzed 27 articles, totaling 2,023 patients with CCO who underwent CEA. Global stroke and mortality rates were 3.2 and 1.9% respectively.

Reviewing data corresponding to 4,633 patients with CCO, stroke and mortality rates found were 4.2 and 2.1% respectively. Influence of the number of surgeries performed in each service over perioperative results was also evaluated. It was found that the number of patients with CCO operated ranged from 2,5 to 22 per year, with stroke and death rates of up to 6.3%14,15 and 4%14,28 respectively. In our series, frequency of surgeries performed in patients with CCO was approximately six per year, with stroke and death rates of 1.6 and 4.9% respectively.

Furthermore, morbidity/mortality rates were observed according to the number of surgeries reported in each study. In series involving less than 50 patients, stroke and death rates were 9.9 and 6.5% respectively. In series involving more than 100 patients, such rates were 3.9 and 1.7% respectively (P < 0.05). In series involving 50 to 100 patients, stroke and death rates were 4.1 and 1.6% respectively (Table 10). A statistical comparison of these series evidenced that studies with less than 50 patients presented higher perioperative stroke and mortality rates than studies with more than 50 patients, confirming the relation of the number of surgeries performed at the service to good surgical outcomes.

click hereTable 10 - Stroke and death rates after CEA according to number of surgeries performed

Patients Articles reviewed Total of patients Stroke (%) Death (%)
< 50 24 445 9.9* 6.5*
> 50 and < 100 22 1,457 4.1 1.6
> 100 14 2,445 3.9 1.7
*P < 0.05 when compared to other groups. Chi-square test.

In summary, some authors consider patients with carotid stenosis and CCO to be at high risk for postoperative stroke. As shown by literature review above, medical therapy alone is an unacceptable procedure in such cases due to high morbidity/mortality rates. Recent therapeutic alternatives, such as carotid stenting, are still lacking scientific support and confirmation of mid-term and long-term benefits. On the other hand, it has been evidenced that CEA provides long-term protection for patients with CCO against stroke onset, with rates of perioperative complications of up to 5%, as evidenced in our literature review.

In our series, stroke and death rate was 6.5% in patients with high frequency of previous neurological symptoms (86%), rate similar to that of NASCET (5.5%) for symptomatic patients without CCO. Our results confirm the position that CEA should be considered the treatment of choice for patients with CCO, as long as it is performed by a skilled and experienced surgical team, in order to provide the best mid-term and long-term results for the patient.

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