CLINICAL STUDIES

Perioperative Ischemic Complications of the Brain After Carotid Endarterectomy

Matthew O. Hebb, MD, PhD
Division of Neurological Surgery, Barrow Neurological Institute, St Josephs Hospital and Medical Center, Phoenix, Arizona Current: Division of Neurosurgery, University of Western Ontario, London, Ontario, Canada

Joseph E. Heiserman, MD, PhD

Division of Neuroradiology, Barrow Neurological Institute, St Josephs Hospital and Medical Center, Phoenix, Arizona

Kirsten P. N. Forbes, MD
Division of Neuroradiology, Barrow Neurological Institute, St Josephs Hospital and Medical Center, Phoenix, Arizona Current Address: Department of Neuroradiology, Institute of Neurological Sciences, Glasgow, Scotland

Joseph M. Zabramski, MD
Division of Neurological Surgery, Barrow Neurological Institute, St Josephs Hospital and Medical Center, Phoenix, Arizona

BACKGROUND: The potential morbidity of cerebral ischemia after carotid endarterectomy (CEA) has been recognized, but its reported incidence varies widely. OBJECTIVE: To prospectively evaluate the development of cerebral ischemic complications in patients treated by CEA at a high-volume cerebrovascular center. METHODS: Fifty patients with moderate or severe carotid stenosis awaiting CEA were studied with perioperative diffusion-weighted imaging of the brain and standardized neurological evaluations. Microsurgical CEA was performed by 1 of 2 vascular neurosurgeons. Radiological studies were evaluated by faculty neuroradiologists who were blinded to the details of the clinical situation. RESULTS: Preoperative diffusion-weighted imaging studies were performed within 24 hours of surgery. A second study was obtained within 24 (92% of patients), 48 (4% of patients), or 72 (4% of patients) hours after surgery. Intraluminal shunting was used in 1 patient (2%), and patch angioplasty was used in 2 patients (4%). No patient had diffusion-weighted imaging evidence of procedure-related cerebral ischemia. Nonischemic complications consisted of postoperative confusion in an 87-year-old man with a urinary tract infection and a marginal mandibular nerve paresis in another patient. Radiological studies were normal in both patients. CONCLUSION: CEA is a relatively safe procedure that may be performed with an acceptable risk of cerebral ischemia in select patients. The low rate of ischemic complications associated with CEA sets a standard to which other carotid revascularization techniques should be held. The current results are presented with a discussion of the senior authors preferred surgical technique and a brief review of the literature.
KEY WORDS: Atherosclerosis, Emboli, Brain, Stroke, Diffusion-weighted imaging
Neurosurgery 67:286-294, 2010
DOI: 10.1227/01.NEU.0000371970.61255.39

www.neurosurgery- online.com

Robert F. Spetzler, MD
Division of Neurological Surgery, Barrow Neurological Institute, St Josephs Hospital and Medical Center, Phoenix, Arizona Reprint requests: Robert F. Spetzler, MD, Barrow Neurological Institute, St Josephs Hospital and Medical Center, 350 W Thomas Rd, Phoenix, AZ 85013. E-mail: neuropub@chw.edu Received, April 2, 2001. Accepted, September 16, 2009. Copyright 2010 by the Congress of Neurological Surgeons

arotid endarterectomy (CEA) confers a significant risk reduction for ipsilateral stroke when combined perioperative stroke and death rates are maintained below 3% for asymptomatic patients and 6% for symptomatic patients.1,2 Stroke has been used as both an outcome and a complication measure in many large CEA series as defined clinically by the persistence of central neurological deficits. Less understood is the incidence and sequelae of silent cerebral ischemia that is identified on radiologABBREVIATIONS: CCA, common carotid artery; CEA, carotid endarterectomy; DWI, diffusionweighted imaging; ECA, external carotid artery; ICA, internal carotid artery; NIHSS, National Institutes of Health Stroke Scale

ical studies and not associated with obvious neurological impairment. Previously considered innocuous, these injuries are increasingly recognized as a potential source of cognitive dysfunction and long-term morbidity.3-7 Published data regarding the incidence of cerebral ischemia after CEA are widely discordant and difficult to interpret.5,8-22 To help clarify this issue, we used diffusion-weighted imaging (DWI) to prospectively evaluate the incidence of new ischemic lesions in the brains of patients who presented with symptomatic or asymptomatic carotid stenosis that was subsequently treated by CEA at our institution. The current results are discussed in the context of pertinent surgical nuances and a brief review of the literature.

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ISCHEMIC COMPLICATIONS AFTER CAROTID ENDARTERECTOMY

PATIENTS AND METHODS

Participants
This protocol was approved by the institutional review board at St Josephs Hospital and Medical Center, Phoenix, Arizona. Fifty participants with the diagnosis of moderate (50%-69%) or severe (70%-99%) stenosis of the cervical internal carotid artery (ICA) who were awaiting CEA and who provided informed consent were prospectively enrolled. Patients with symptomatic stenosis of either grade were offered CEA after medical clearance. Asymptomatic patients with stenosis < 60% were managed medically; those with 60% stenosis were given the option to be treated either medically or with CEA. Exclusion criteria included lack of consent or an inability to participate in the magnetic resonance imaging (MRI) studies. Carotid stenosis was evaluated with the North American Symptomatic Carotid Endarterectomy Trial criteria as measured on computed tomographic, magnetic resonance, or catheter angiography studies.2 Forty-five patients were examined within 24 hours before and after CEA with the National Institutes of Health Stroke Scale (NIHSS) administered by a neurologist, neurosurgeon, or clinical nurse practitioner not involved in the patients routine care.23 An additional 5 patients (10%) underwent standard preoperative and postoperative neurological assessments conducted by the operating neurosurgical team. These patients had asymptomatic carotid stenosis and normal neurological evaluations before and after surgery. For the purposes of this study, these individuals were assigned an NIHSS score of 0. The current work extends preliminary findings based on 18 previously reported patients.12

Surgical Technique
CEA was performed by 1 of 2 vascular neurosurgeons (J.M.Z., R.F.S.; Figure). Patients were maintained under general anesthesia to permit application of somatosensory evoked potential monitoring of cerebral function and electroencephalographic burst suppression using barbiturate administration during ICA cross-clamping. The use of general anesthesia, compared with regional field blocks, affords better overall control of the patients hemodynamic needs and offers a less hindered environment for surgical manipulation and assertive resuscitative measures should the cerebral blood flow become compromised. A transverse cervical incision in a skin crease was preferred for enhanced cosmesis. The operating microscope was used during deep neck dissection, endarterectomy, and arteriotomy repair. A semirigid 13-French MicroVac ultramalleable suction catheter (PMI Corp, Chanhassen, Minnesota) was placed between the jugular vein and common carotid artery (CCA). Burst suppression on electroencephalography was induced with barbiturates, and 70 IU/kg intravenous heparin was administered before sequential occlusion of the ICA, CCA, external carotid artery (ECA), and superior thyroid artery with temporary aneurysm clips or an angled vascular clamp. Intraluminal shunting was used if somatosensory evoked potential monitoring showed evidence of developing ischemia after arterial occlusion. The CCA was incised and the arteriotomy was extended to the tapering point of the plaque in the ICA. Back-bleeding of the ICA confirmed collateral flow and the absence of distal occlusion. The atheromatous plaque was dissected circumferentially and excised. The arterial lumen was inspected carefully under microscopic visualization with continuous

FIGURE. Preferred technique for carotid endarterectomy (CEA). A, operating room setup. The microscope is routinely used to optimize the operative view for both the primary and assistant surgeons and the scrub nurse. B, the patient position and transverse incision within a skin crease (dashed line) are shown. C, the common carotid artery (CCA) and carotid bifurcation region are dissected. Distal internal carotid artery (ICA) exposure is facilitated with a single self-retaining

retractor and fishhooks tethered to a Leyla bar. Vessel loops may be placed around the CCA and the ICA before arterial occlusion if the need for an intraluminal shunt is anticipated. A suction microcatheter is positioned to maintain a clear surgical field. D, isolated carotid vessels before the arteriotomy (dashed line) is made. E, the atheromatous plaque is circumferentially divided at the distal CCA and dissected to a tapered end within the ICA. F, under microscopic vision, (continued)

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heparin irrigation to identify residual debris and loose intimal tags. The vessel was closed with running 6-0 Prolene sutures sewn from either end and tied in the center of the arteriotomy. On 2 occasions, patch angioplasty was performed. Before final closure, the ICA was back-bled to expel debris and air through the arteriotomy site. This was repeated for the ECA and CCA, after which the clip on the superior thyroid artery was removed to provide continuous bleeding while the arteriotomy closure was completed. The ECA clip was then released, followed by the CCA clamp, thus forcing any debris and air into the external circulation. The CCA clamp was reapplied and the ICA clip was released. The higher

pressure in the ICA system allowed flushing from the ICA to the ECA, after which the CCA clamp was finally removed. Hemostasis was ensured, and the neck wound was closed in standard fashion.24

Diffusion-Weighted Imaging
MRI was performed at 1.5 T (General Electric, Milwaukee, Wisconsin) with a single-shot echo-planar spin-echo technique. A maximum diffusion sensitivity of b = 1000 s/mm2 was applied to 3 orthogonal planes. Axial images were obtained at 20 levels, both with and without the diffusion gradient (6500/101/1 [repetition time/echo time/excitations]; section thickness, 5 mm; intersection gap, 2.5 mm; field of view, 32 cm; matrix, 128 128). Both isotropic DWI and anisotropic DWI were examined for areas of signal hyperintensity in both hemispheres, cerebellum, and brainstem. MRI studies were evaluated by faculty neuroradiologists who were unaware of the clinical details of each case.

RESULTS
Patient Demographics and Clinical Assessment The mean age of the cohort was 69 years, with a slight male predominance (60%). Most patients had severe (70%-99%) ICA stenosis that was identified incidentally (68%) or after a transient ischemic attack (30%). Most patients were neurologically intact at the time of surgery (NIHSS score = 0; 92%). There was a high incidence of risk factors for atherosclerosis within the cohort, and many patients were considered to have a higher-than-average surgical risk as a result of anatomic and physiological comorbidities. Significant cardiac or pulmonary disease was identified in 46% of individuals (Tables 1 and 2). A preoperative NIHSS score of 1 was obtained in a patient with severe right ICA stenosis who presented with a nondisabling stroke and left upperextremity paresthesia. Another patient with severe, asymptomatic left ICA stenosis had a preoperative NIHSS score of 1 that reflected a remote right hemispheric infarct associated

all loose intimal tags and debris are meticulously removed. Note the participation of the assistant surgeon. G, the arteriotomy is closed with two 6-0 Prolene sutures. Primary closure is preferred but patch angioplasty is considered when indicated. The sequential removal of the arterial clamps is carried out as described in the text. ECA, external carotid artery; EEG, electroencephalography; STA, superior thyroid artery. Used with permission from Barrow Neurological Institute.

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TABLE 1. Patient Demographicsa

NEUROSURGERY
MRA DSA MRA MRA MRA DSA DSA DSA DSA DSA MRA DSA MRA MRA MRA MRA MRA MRA MRA DSA MRA MRA MRA MRA MRA DSA MRA MRA CTA MRA MRA MRA CTA 0 0 0 3 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 No No No No No No No No No No 4 1 1 No 0 0 0 No 0 0 0 No No No No No No No No No No No No No No 0 0 0 No No 3 0 0 No No 0 0 0 No No No No No No No No No No No No No No No No No No 1 0 0 No No No 0 6 6 No No No No No No No No No No No No No No No No No No No No No 3 0 0 Yes No No No 0 0 0 No No No No 0 0 0 No No No No No No No No No No No No No No No No No No No No No No No No No 0 0 1 No No No No No 0 0 0 No No No No No No Yes Yes No Yes No No Yes Yes No No No No Yes No No Yes Yes No Yes No Yes Yes 1 0 0 No No No No No Yes 0 0 0 No No No No No Yes 3 0 0 No No No No No No Yes Yes Yes Yes No Yes Yes No Yes No Yes Yes Yes Yes Yes No Yes Yes Yes Yes Yes No Yes Yes Yes No 1 0 0 No No No No No Yes Yes 0 0 0 No Yes No No No Yes Yes 1 0 0 No No No No No No No Yes No Yes Yes No Yes No Yes Yes No No Yes No Yes No Yes Yes No Yes Yes No Yes Yes Yes No Yes No Yes Yes 1 0 0 No No No No No No Yes No 2 0 0 No No No No No Yes Yes Yes 0 0 0 No No No No No No Yes Yes No Yes No No No No No Yes No No No No No No Yes No No Yes No No Yes No No Yes No Yes No No No No No Yes 0 0 0 No No No No No No Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes No Yes Yes Yes Yes Yes No Yes Yes No Yes No Yes Yes Continues

SignifiPrior Preoper- PostoperContra- Prior Inaccescant Age, Presenting Recurrent Neck Hyper- Hyper- Diabetes Case Stenosis Imaging ative ative lateral Radiasible Medical Smoker b y/Sex Symptoms Stenosis Dissectension lipidemia Mellitus NIHSS NIHSS Occlusion tion Lesion Comortion biditiesc

73/M

Severe

63/M

Severe

69/F

Severe

68/M

Severe

61/M

Severe

71/F

Severe

72/F

Severe

51/M

Severe

64/M

Severe

10

71/M

Severe

11

73/F

Severe

12

87/M

Severe

13

84/F

Severe

14

65/M

Severe

15

56/M Moderate

16

66/M

Severe

17

75/M

Severe

18

68/F

Severe

19

70/M

Severe

20

71/M

Severe

21

50/M

Severe

22

69/M

Severe

23

78/F

Severe

24

66/M

Severe

25

58/F

Severe

26

79/F

Severe

27

58/M

Severe

28

65/M

Severe

29

79/F

Severe

30

83/M

Severe

31

83/M

Severe

32

69/F

Severe

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33

60/F

Severe

HEBB ET AL

SignifiPrior Preoper- PostoperContra- Prior Inaccescant Age, Presenting Recurrent Neck Hyper- Hyper- Diabetes Case Stenosis Imaging ative ative lateral Radiasible Medical Smoker b y/Sex Symptoms Stenosis Dissectension lipidemia Mellitus NIHSS NIHSS Occlusion tion Lesion Comortion biditiesc

CTA, computed tomography angiography; DSA, digital subtraction angiography; MRA, magnetic resonance angiography; NIHSS, National Institutes of Health Stroke Scale. Symptoms related to ipsilateral carotid stenosis: 0 = asymptomatic, 1 = retinal TIA, 2 = hemispheric and retinal TIA, 3 = hemispheric TIA, and 4 = nondisabling stroke. c Significant medical comorbidities: chronic obstructive pulmonary disease, congestive heart failure, unstable angina, multivessel coronary artery disease, and renal failure. d Intraoperative vascular shunt placed.

with right ICA stenosis that had been treated with CEA. Postoperatively, the NIHSS scores of both patients were unchanged. The NIHSS scores of 2 patients (4%) increased from 0 preoperatively to 1 postoperatively, reflecting confusion that improved with treatment of a urinary tract infection in an 87-year-old man and a marginal mandibular nerve paresis in a second patient. Two other participants had no change in their preoperative NIHSS scores of 6 and 8. The former was a 66year-old man with asymptomatic severe left ICA stenosis and a left upper-extremity paresis associated with a prior right ICA stenosis and hemispheric infarct. The latter was a 68-year-old man with severe right ICA stenosis and current transient ischemic attacks who had a remote history of left hemispheric stroke and esophageal cancer. Surgical Considerations Participants were deemed acceptable surgical candidates after undergoing preoperative evaluation by appropriate medical and anesthesia services. Patients with < 50% carotid stenosis were generally not considered for surgical treatment. The sequence of arterial clamping and release described above was used to reduce the potential for atheromatous, intimal, and air emboli to travel into the cerebral ICA circulation. An intraluminal shunt was used in 1 patient who had a tandem lesion of the M1 branch of the middle cerebral artery and an absent contralateral A1 branch of the anterior cerebral artery. Patch angioplasty was reserved for fibrosed or congenitally small carotid vessels and was used in 2 patients (Figure). Diffusion-Weighted Imaging All patients underwent DWI within 24 hours before surgery. Postoperative studies were performed within 24 hours in 92% of patients, between 24 and 48 hours in 4% of patients, and between 48 and 72 hours in 4% of patients. Preoperatively, 1 participant was found to have a DWI hyperintensity in the middle cerebral artery territory of the

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes Yes Yes Yes No No No No No 0 0 0 CTA Severe 74/F 48 No

No

No

No No No No No No No No No 1 0 0 CTA 77/M 49 Severe

No

No

No

No

No

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

No

No

No

No

No

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

No

No

Yes

No

Yes

Yes

Yes

Yes

Yes

No

No

No

No

No

No

No

No

No

No

No

No

No

No

No

No

No

No

Yes

No

No

No

No

No

No

No

No

No

No

No

No

No

Yes

No

No

No

No

No

No

No

No

No

No

No

No

No

Yes

No

No

No

No

No

No

No

No

No

No

No

No

No

No

Yes

No

No

No

No

No

No

No

No

No

No

No

No

No

No

No

No

MRA

MRA

MRA

MRA

62/M Moderate

68/M Moderate

TABLE 1. (Continued)

71/M Moderate

78/F Moderate

Severe

Severe

Severe

Severe

Severe

Severe

Severe

Severe

Severe

64/M

77/M

53/M

68/M

81/M

Severe

73/F

72/F

66/F

71/F

63/F

50

46

34

36

39

35

37

38

40

45

47

43

41

42

44

64/F

Severe

MRA

MRA

DSA

DSA

CTA

CTA

CTA

CTA

CTA

CTA

CTA

No

No

No

No

No

No

No

No

No

No

No

Yes

Yes

No

No

No

No

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TABLE 2. Clinical Summary of 50 Patients Undergoing Carotid Endarterectomya Variable Age, y Mean Median Minimum Maximum Gender, n (%) Male Female Location, n (%) Left Right Degree of stenosis, n (%) Moderate Severe Imaging modality, n (%) CT angiography MR angiography Catheter angiography Presenting symptoms, n (%)b None Retinal TIA Hemispheric TIA Retinal and hemispheric TIA Nondisabling stroke Preoperative NIHSS score, n (%) 0 1 6 8 Postoperative NIHSS score, n (%) 0 1 6 8 Anesthesia, n (%) General Local Use of vascular shunt, n (%) Yes No Patch angioplasty, n (%) Yes No 2 (4) 48 (96) Continues 1 (2) 49 (98) 50 (100) 0 (0) 44 (88) 4 (8) 1 (2) 1 (2) 46 (92) 2 (4) 1 (2) 1 (2) 32 (64) 6 (12)
a

TABLE 2. (Continued) Variable Time of preoperative MRI, n (%) < 24 h 50 (100) 0 (0) 0 (0) 46 (92) 2 (4) 2 (4) 38 (76) 31 (62) 14 (28) 42 (84) 2 (4) 2 (4) 1 (2) 1 (2) 0 (0) 5 (10) 23 (46) 24 to 48 h 48 to 72 h Time of postoperative MRI, n (%) < 24 h 24 to 48 h 48 to 72 h Atherosclerosis risk factors, n (%) Hypertension Hyperlipidemia Diabetes mellitus Smoking Surgical risk factors, n (%) Recurrent stenosis Contralateral occlusion Prior neck radiation Prior neck dissection Inaccessible lesion Age > 80 y Significant medical comorbidities Value

Value

69 69 50 87 30 (60) 20 (40) 22 (44) 28 (56) 5 (10) 45 (90) 11 (22) 11 (22) 28 (56)

1 (2) 8 (16) 3 (6)

CT, computed tomography; MR, magnetic resonance; NIHSS, National Institutes of Health Stroke Scale; TIA, transient ischemic attack. b Attributable to operative side.

contralateral hemisphere. This finding was associated with hemiparesis and an NIHSS score of 6, as described above. The hemisphere ipsilateral to the side of surgery was normal. The MRI of a patient with a preoperative NIHSS score of 8 exhibited T2 shine-through phenomenon in the region of a remote infarct in the contralateral hemisphere. The hemisphere ipsilateral to the side of surgery was normal. In another participant, one third of the ipsilateral cerebral hemisphere was obscured by susceptibility artifact from an aneurysm clip, limiting interpretation. The remaining 47 preoperative DWI studies were normal. Postoperatively, no new areas of diffusion hyperintensity were identified in any participant.

DISCUSSION
The intent of this study was to further define the risk of cerebral ischemia associated with CEA. The study cohort consisted of 64% asymptomatic and 36% symptomatic patients, with 90% of individuals presenting with severe (> 70%) and 10% with moderate (> 60%) ICA stenosis. There was a 0% incidence of ischemic neurological deficits or new cerebral lesions on DWI after surgery. Nonischemic complications were limited to 2 patients (4%). Surgical technique was consistent and included, when possible,

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general anesthesia with neurophysiological monitoring, barbiturateinduced electroencephalographic burst suppression, and systemic heparinization. We have found the operating microscope invaluable for optimizing illumination and magnification during carotid dissection, especially of the distal cervical ICA, and throughout the endarterectomy and repair phases of surgery. The enhanced visualization facilitates removal of all loose debris and identification of existing or potential intimal flaps. The microscope further permits an unhindered view of the surgical field for the assistant surgeon and the operating nurse. Intraluminal shunting and patch angioplasty were used only as required. The term silent cerebral ischemia may be used erroneously in patients with seemingly normal neurological function who demonstrate measurable deficits on cognitive testing. The clinical sequelae of the ischemia are variable and may be subtle beyond detection by standard neurological evaluation or absent altogether.25 The cited risk of cerebral ischemia associated with CEA has been incon-

sistent, with reports varying from no ischemic complications to as high as one third of patients having new brain lesions on postoperative MRI (Table 3). Variability in patient factors, study methodology, and operative technique undoubtedly contributes to these discrepancies. Most technical nuances of CEA surgery are influenced by surgeon training, preference, and experience and generally do not have a significant impact on clinical outcomes. On the other hand, the practice of meticulous carotid dissection and extirpation of intimal debris and air is clearly fundamental to reducing the risk of embolic ischemic events associated with CEA. The use of an intraluminal shunt is an important issue that should be carefully considered on an individual basis. A recent topic review investigated factors involved in the development of cerebral ischemia in CEA patients who were studied with DWI in the early perioperative period.26 Selective or obligate shunting was associated with 6% versus 16% incidence of new postoperative lesions on DWI, respectively (P < .001). Another group reported an asso-

TABLE 3. Incidence of Carotid Endarterectomy-Associated Cerebral Ischemia Assessed With Magnetic Resonance Imaging in Recent Seriesa No. of Patients 40 19 78 77 48 25 51 18 33 23 26 139 72 30 50 60 30 Timing of MRI Degree of Patients With Shunt Stenosis, Symptomatic Used, % Preoper- Postoper% Stenosis, % ative ative Not specified 70 (mean) Not specified 78 (mean) 90 100 51 48 Not Not Not specified specified specified 58 37 25 25 24 h <3d 3d <3d Side Evaluated Bilateral Bilateral Bilateral Ipsilateral Bilateral Ipsilateral Ipsilateral Bilateral Ipsilateral Bilateral Bilateral Not specified Ipsilateral Bilateral Bilateral Bilateral Ipsilateral Patients With New Ischemic Lesions, % 10 16 9 34 6 4 12 0 24 9 4 9 4 3 4 12 7

References

Study Type

DWI

Jansen et al 19945

Prospective

No No No Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes

Vanninen et al 19967 Prospective Cantelmo et al 19989 Retrospective Muller et al 200017 Barth et al 20008 Feiwell et al 200110 Prospective Prospective Prospective

Not < 72 h specified 24 h 24 h 12 h (mean) < 24 h < 24 h 24 h

High grade 66 Not specified > 30 > 50 > 70 Not specified > 40 > 70 Not specified 65 50 45 100 73 66

Not 3d specified (mean) 100 5 100 < 24 h < 24 h 24 h

Tomczak et al 200121 Prospective Forbes et al 2001 Wolf et al 2004

22 12

Prospective Prospective Prospective Prospective Prospective Retrospective

Flach et al 200411 Roh et al 200518 Iihara et al 200614 Inoue et al 200615 Tedesco et al 2007
20

Not Not <3d specified specified 100 <7d <7d Not Not <4d specified specified 100 <5d <5d Not Not < 48 h specified specified 4 100 97 Not 24-48 h specified < 24 h < 48 h <3d < 48 h

High grade 44 Not specified > 70 73 Not specified

Retrospective Prospective Prospective

Gossetti et al 200713 Lacroix et al 200716 Skjelland et al 2009

a

High grade 68 > 70 Not specified

19

Prospective

DWI, diffusion-weighted imaging; MRI, magnetic resonance imaging.

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ciation between intraoperative cerebral microemboli detected by continuous cranial Doppler ultrasonography and the incidence of new changes on postoperative DWI. Intraluminal shunts were used in 98% of patients, and there was a 7% incidence of new cerebral lesions after CEA. Most solid emboli occurred with establishment of shunt flow and carotid clamp release, whereas gaseous emboli were most frequently detected with initiation and cessation of shunt flow.19 In the present series, only a single patient required an intraluminal shunt, which was used without complication.

CONCLUSION
CEA may be performed with minimal risk of ischemic complications in select patients. The low incidence of ischemic morbidity associated with CEA contrasts that reported in recent angioplasty studies11,13,16,18-20 and provides a standard to which other carotid revascularization techniques should be held. Further related studies that incorporate neuropsychological and cognitive outcomes may better define the clinical impact of silent ischemia. Disclosure
The authors have no personal financial or institutional interest in any of the drugs, materials, or devices described in this article.

REFERENCES
1. Halliday A, Mansfield A, Marro J, et al. Prevention of disabling and fatal strokes by successful carotid endarterectomy in patients without recent neurological symptoms: randomised controlled trial. Lancet. 2004;363(9420):1491-1502. 2. North American Symptomatic Carotid Endarterectomy Trial Collaborators. Beneficial effect of carotid endarterectomy in symptomatic patients with highgrade carotid stenosis: North American Symptomatic Carotid Endarterectomy Trial Collaborators. N Engl J Med. 1991;325(7):445-453. 3. Gaunt ME, Smith JL, Bell PR, Martin PJ, Naylor AR. Microembolism and hemodynamic changes in the brain during carotid endarterectomy. Stroke. 1994;25(12): 2504-2505. 4. Ghogawala Z, Westerveld M, Amin-Hanjani S. Cognitive outcomes after carotid revascularization: the role of cerebral emboli and hypoperfusion. Neurosurgery. 2008;62(2):385-395. 5. Jansen C, Ramos LM, van Heesewijk JP, Moll FL, van Gijn J, Ackerstaff RG. Impact of microembolism and hemodynamic changes in the brain during carotid endarterectomy. Stroke. 1994;25(5):992-997. 6. Lal BK. Cognitive function after carotid artery revascularization. Vasc Endovascular Surg. 2007;41(1):5-13. 7. Vanninen E, Vanninen R, Aikia M, et al. Frequency of carotid endarterectomyrelated subclinical cerebral complications. Cerebrovasc Dis. 1996;6(5):272-280. 8. Barth A, Remonda L, Lovblad KO, Schroth G, Seiler RW. Silent cerebral ischemia detected by diffusion-weighted MRI after carotid endarterectomy. Stroke. 2000; 31(8):1824-1828. 9. Cantelmo NL, Babikian VL, Samaraweera RN, Gordon JK, Pochay VE, Winter MR. Cerebral microembolism and ischemic changes associated with carotid endarterectomy. J Vasc Surg. 1998;27(6):1024-1030. 10. Feiwell RJ, Besmertis L, Sarkar R, Saloner DA, Rapp JH. Detection of clinically silent infarcts after carotid endarterectomy by use of diffusion-weighted imaging. AJNR Am J Neuroradiol. 2001;22(4):646-649. 11. Flach HZ, Ouhlous M, Hendriks JM, et al. Cerebral ischemia after carotid intervention. J Endovasc Ther. 2004;11(3):251-257. 12. Forbes KP , Shill HA, Britt PM, Zabramski JM, Spetzler RF, Heiserman JE. Assessment of silent embolism from carotid endarterectomy by use of diffusion-weighted imaging: work in progress. AJNR Am J Neuroradiol. 2001;22(4):650-653. 13. Gossetti B, Gattuso R, Irace L, et al. Embolism to the brain during carotid stenting and surgery. Acta Chir Belg. 2007;107(2):151-154.

14. Iihara K, Murao K, Sakai N, Yamada N, Nagata I, Miyamoto S. Outcome of carotid endarterectomy and stent insertion based on grading of carotid endarterectomy risk: a 7-year prospective study. J Neurosurg. 2006;105(4):546-554. 15. Inoue T, Tsutsumi K, Maeda K, et al. Incidence of ischemic lesions by diffusionweighted imaging after carotid endarterectomy with routine shunt usage. Neurol Med Chir (Tokyo). 2006;46(11):529-533. 16. Lacroix V, Hammer F, Astarci P, et al. Ischemic cerebral lesions after carotid surgery and carotid stenting. Eur J Vasc Endovasc Surg. 2007;33(4):430-435. 17. Muller M, Reiche W, Langenscheidt P, Hassfeld J, Hagen T. Ischemia after carotid endarterectomy: comparison between transcranial Doppler sonography and diffusion-weighted MR imaging. AJNR Am J Neuroradiol. 2000;21(1):47-54. 18. Roh HG, Byun HS, Ryoo JW, et al. Prospective analysis of cerebral infarction after carotid endarterectomy and carotid artery stent placement by using diffusionweighted imaging. AJNR Am J Neuroradiol. 2005;26(2):376-384. 19. Skjelland M, Krohg-Sorensen K, Tennoe B, Bakke SJ, Brucher R, Russell D. Cerebral microemboli and brain injury during carotid artery endarterectomy and stenting. Stroke. 2009;40:230-234. 20. Tedesco MM, Coogan SM, Dalman RL, et al. Risk factors for developing postprocedural microemboli following carotid interventions. J Endovasc Ther. 2007; 14(4):561-567. 21. Tomczak R, Wunderlich A, Liewald F, Stuber G, Gorich J. Diffusion-weighted MRI: detection of cerebral ischemia before and after carotid thromboendarterectomy. J Comput Assist Tomogr. 2001;25(2):247-250. 22. Wolf O, Heider P, Heinz M, et al. Microembolic signals detected by transcranial Doppler sonography during carotid endarterectomy and correlation with serial diffusion-weighted imaging. Stroke. 2004;35(11):e373-e375. 23. Goldstein LB, Bertels C, Davis JN. Interrater reliability of the NIH stroke scale. Arch Neurol. 1989;46(6):660-662. 24. Theodore N, Baskin JJ, Spetzler RF, Vishteh AG, Apostolides PJ. Microsurgical carotid endarterectomy. Oper Tech Neurosurg. 1998;1(4):178-184. 25. Heyer EJ, DeLaPaz R, Halazun HJ, et al. Neuropsychological dysfunction in the absence of structural evidence for cerebral ischemia after uncomplicated carotid endarterectomy. Neurosurgery. 2006;58(3):474-480. 26. Schnaudigel S, Groschel K, Pilgram SM, Kastrup A. New brain lesions after carotid stenting versus carotid endarterectomy: a systematic review of the literature. Stroke. 2008;39(6):1911-1919.

COMMENTS
n this article, the authors report on 50 patients who underwent carotid endarterectomy by 2 experienced surgeons with extremely low complications. In this group of 50, the patients suffered no immediate mortality, and 2 patients had minimal morbidity. Most important, they showed no new diffusion-weighted imaging change in the first 72 postoperative hours compared with preoperative diffusion-weighted imaging. This finding suggests that with appropriate patient selection and technique, extraordinarily low embolic events are possible. This is relatively important because the literature is confusing regarding the numbers and techniques that may cause emboli. This question may be studied by several techniques, including examination of the brain preoperatively and postoperatively for new imaging deficits, such as the authors do here. In addition, Doppler recording of emboli may be used during the actual procedure, as well as preoperatively and postoperatively. Such events have been published elsewhere. Finally, clinical testing of both motor and cognitive function was done to determine whether new events occur with surgery. Many studies have taken place, and none are completely definitive. This particular contribution does suggest that in a very experienced surgeons hands with meticulous technique, immediate perioperative diffusionweighted imaging lesions, which are usually considered to be embolic, can be avoided. The article sets a high bar for other techniques for comparison, but it must be clarified that not just technique but also patient selection and perioperative care must be included if one is to expect excellent results. The majority of these patients are in an asymptomatic group. By their nature, asymptomatic plaques are less friable and less likely to

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embolize. A study of predominantly symptomatic patients may have different results. One third of the patients in this study were symptomatic, and that small group of patients also enjoyed good results. Further studies would benefit from long-term follow-up Doppler detection of emboli and cognitive evaluation because silent infarcts may manifest by decline in executive cognitive function. Robert J. Dempsey Madison, Wisconsin

his excellent prospective study demonstrates that perioperative ischemic events as detected by magnetic resonance imaging are exceedingly uncommon after carotid endarterectomy in patients with asymptomatic carotid stenosis. This study therefore reconfirms the surgical literature that has documented repetitively that in competent surgical hands, carotid endarterectomy is a very low-risk procedure for asymptomatic disease and remains the gold standard compared with carotid angioplasty. It is important to recall that the risk of stroke for asymptomatic hemodynamically significant stenosis (> 70% stenosis) is approximately 3% per year. Therefore, to achieve a result superior to the natural history of the disease, the operation needs to be done expertly. In this reviewers experience, the majority of ischemic events occur during the initial dissection of the carotid artery from dislodging of fragile plaque. Therefore, as noted by the authors, it is worth reemphasizing that meticulous dissection and avoidance of carotid manipulation are important. In my practice, dissection is not allowed underneath the carotid bifurcation for 2 reasons: to prevent embolus and to decrease the risk of injury to the superior laryngeal nerve, which can be the source of swallowing difficulties. Lastly, what remains to be studied is the incidence of magnetic resonance imagingdetected ischemic events in patients with symptomatic high-grade stenoses compared with stenting. Fredric B. Meyer Rochester, Minnesota

arotid endarterectomy is at this point one of the most thoroughly studied and best understood operations that we perform. In asymptomatic patients, the perioperative mortality is 1% and the stroke rate is 1.7%1; in symptomatic patients, the perioperative mortality is 0.6% and the stroke rate is 5.2%.2 It has been reported, however, that carotid endarterectomy can result in subtle, cognitive deficits that often go unnoticed.3 To address this issue, the group from the Barrow Neurological Institute reports here the results of isotropic and anisotropic diffusionweighted imaging in 50 mostly asymptomatic carotid endarterectomy patients. Of these 50 patients, 64% were asymptomatic, 30% presented with transient ischemic attacks, and 6% presented with a stroke. In this group, 90% of patients had 70% to 99% stenosis and 10% had 60% to 69% stenosis by computed tomographic angiography, magnetic resonance imaging, or angiographic criteria. The age range was 50 to 87 years (mean age, 69 years). To assess the issue of silent ischemic injury, all patients under-

went preoperative and postoperative diffusion-weighted imaging studies. Only 1 patient had a preoperative diffusion-weighted imaging abnormality, which correlated with a known stroke. The authors found no evidence of ischemia by diffusion-weighted imaging in any of the patients, which argues for the safety of this procedure when performed meticulously in well-selected patients. The authors describe in detail several steps in their technique that should be noted. To minimize the need for shunting, they used routine electroencephalographic and somatosensory evoked potential monitoring and barbiturate-induced burst suppression before clamping. They place a shunt if the somatosensory evoked potentials deteriorate. We fully agree with the authors that the insertion of a shunt should be minimized because it is undoubtedly associated with an increased stroke rate. In our reported series of 194 patients, most of which were symptomatic (40% transient ischemic attacks + 23% cerebrovascular accidents = 63% total symptomatic), selective shunting based on electroencephalographic/somatosensory evoked potential monitoring was associated with a stroke rate of 1% compared with a stroke rate of 4% in patients who underwent routine shunting.4 The induction of barbiturate burst suppression before carotid clamping is an interesting maneuver that eliminates the indication for shunt placement if the electroencephalography (but not the somatosensory evoked potentials) deteriorates, given that the electroencephalography is obviously nullified by burst suppression. The authors do not mention their intraoperative blood pressure parameters, but we routinely raise the mean arterial pressure by 10% before clamping. The authors rarely use patch angioplasty and reserve it for either fibrosed or congenitally small vessels. Suturing a patch increases the clamp time because the suture line is at least twice as long as that of an arterial repair without grafting. Another important detail is their description of the flushing maneuvers before fully opening the carotid system, which we also routinely use. In the final stages of closing the arteriotomy, the authors first back-bleed the internal carotid artery, then flush the common carotid artery into the external carotid artery, and finally flush the internal carotid artery into the external carotid artery. Finally, the use of magnification in this operation with either high-powered loupes or a microscope is of tremendous importance. Rafael J. Tamargo Baltimore, Maryland

1. Halliday A, Mansfield A, Marro J, et al. Prevention of disabling and fatal strokes by successful carotid endarterectomy in patients without recent neurological symptoms: randomised controlled trial. Lancet. 2004;363(9420):1491-1502. 2. NASCET Collaborators. Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis: North American Symptomatic Carotid Endarterectomy Trial Collaborators. N Engl J Med. 1991;325(7):445-453. 3. Lal BK. Cognitive function after carotid artery revascularization. Vasc Endovascular Surg. 2007;41(1):5-13. 4. Woodworth GF, McGirt MJ, Than KD, Huang J, Perler BA, Tamargo RJ. Selective versus routine intraoperative shunting during carotid endarterectomy: a multivariate outcome analysis. Neurosurgery. 2007;61(6):1170-1176.

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