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Surgical Neurolog

Imaging

Direct and primary carotid endarterectomy for common

carotid artery occlusion: Report of 2 cases

Tomohiro Inoue, MD, Kazuo Tsutsumi, MD4, Shinobu Adachi, MD,

Shota Tanaka, MD, Naoto Kunii, MD, Masahiro Indo, MDDepartment of Neurosurgery, Showa General Hospital, Kodaira-shi, Tokyo 187-8510, Japan

Received 18 July 2006; accepted 4 January 2007

www.surgicalneurology-online.com

Abstract Background: Cerebral ischemia associated with chronic CCA occlusion is a rare condition and

0090-3019/$ – see fro

doi:10.1016/j.surneu.2

Abbreviations: C

tomographic scan; EC

MCA, middle cerebral

magnetic resonance

posterior communicat

temporal artery; TIAs,

4 Corresponding a

E-mail address: k

raises strategic dilemma when the revascularization is needed.

Methods: Two patients with CCA occlusion presented with ischemic symptom associated with the

affected side. Both patients underwent vascular reconstruction by direct carotid endarterectomy to

achieve primary restoration of CCA to ICA flow.

Results: Successful reopening of the vessels was obtained in both patients without the evidence of

postsurgical ischemic event. Follow-up MRA was obtained at later than 6 months after surgery,

which demonstrated patent CCA-ICA in both patients.

Conclusions: Direct carotid endarterectomy of the occluded CCA can be safely performed if the

preoperative angiography suggest still patent vessels distal to carotid bifurcation and the substantial

bback flowQ is obtained from ICA during arteriotomy.

D 2008 Elsevier Inc. All rights reserved.

Keywords: Carotid endarterectomy; Common carotid artery occlusion; Ischemic cerebrovascular disease

1. Introduction

Chronic CCA occlusion is a rare condition and may be

associated with stroke, TIAs or chronic ischemia such as

vascular dementia. Several recent reports have discussed

the surgical revascularization of CCA mainly using

extracranial bypass procedure SA-ECA saphenous vein

interposition grafting with or without subsequent STA-

MCA bypass [1,3,5,6]. However, direct and primary carotid

endarterectomy for chronic CCA occlusion to reopen CCA-

ICA, CCA-ECA, or both has not been well discussed. We

report 2 patients who underwent carotid endarterectomy for

nt matter D 2008 Elsevier Inc. All rights reserved.

007.01.034

CA, common carotid artery; CT scan, computed

A, external carotid artery; ICA, internal carotid artery;

artery; MRA, magnetic resonance angiography; MRI,

imaging; PCA, posterior cerebral artery; PcomA,

ing artery; SA, subclavian artery; STA, superficial

transient ischemic attacks; VA, vertebral artery.

uthor: Tel.: +81 424 61 0052; fax: +81 424 64 7912.

.tsutsumi-md@nifty.com (K. Tsutsumi).

CCA occlusion. The details of the management are

presented and discussed.

2. Case reports

2.1. Case 1

The first subject is a 65-year-old man who presented to

another hospital with a complaint of left hemiparesis. His

medical history was significant for smoking and hyperlipid-

emia. Magnetic resonance imaging and MRA were per-

formed, which showed infarction of corona radiata and

watershed area of right cerebral hemisphere as well as right

ICA occlusion. He was referred to our department for

possible surgical revascularization. Neurologic examination

showed mental decline, left side neglect, as well as left

hemiparesis being worse in the upper extremity. Cerebral

angiography revealed right CCA occlusion with residual

stump opacified several centimeters from the origin at right

innominate artery. Collateral filling of right ECA back to the

origin of occipital artery was seen from vertebral injection

y 69 (2008) 620–626

T. Inoue et al. / Surgical Neurology 69 (2008) 620–626 621

through muscular branch, with only faint and delayed

opacification of right STA. Left carotid injection showed

moderate cross-flow toward right hemisphere and delayed

retrograde opacification of cavernous to petrous right ICA.

The right PCA area was also filled through this moderate

cross-flow because of atretic right P1 (Fig. 1). After

thorough discussion, we decided to try carotid endrater-

ectomy, expecting that the carotid bifurcation was still

open. In the operation, CCA was exposed proximally with

ligation and resection of omohyoideus muscle. We

observed that the ICA, ECA, as well as the CCA

appeared as externally normal vessels with enough vasa

vasorum, as usually seen in carotid endarterectomy. The

proximal portion of CCA and the distal portion of ICA

and ECA were soft on palpation. With CCA and ECA

clamped, arteriotomy was made along the CCA, showing

total occlusion of CCA just around the carotid bifurcation

by atheromatous plaque and retrograde extension of

organized thrombus. Then another small arteriotomy was

Fig. 1. Upper left: preoperative CT scan of the head showing infarction of coron

preoperative right carotid angiogram (anteroposterior view) showing CCA occlusio

artery. Upper right: collateral filling of right ECAwas seen from vertebral injectio

injection (anteroposterior view) showed moderate cross-flow toward right cerebra

right ICA.

made on ICA distal to the obvious atheromatous disease,

and moderate back flow was obtained. We extracted back

flow for a while to remove a possible small thrombus in

distal ICA, and then the distal ICA was clamped.

Atheromatous plaque was dissected in the usual manner.

The extent of plaque was within usual levels for ICA and

ECA, and could be cleaned out. On the CCA side, the

plaque was dissected as proximally as possible until it was

thin enough. After removal of plaque, the inner surface of

the vessels looked smooth with some oozing of blood

showing viable media. The arteriotomy was closed via

primary closure with 6-0 prolene. Postoperatively, to

reduce the risk of hyperperfusion, rigorous attention was

paid to keep the systolic blood pressure lower than 120

mm Hg for several days. Postoperative diffusion-weighted

MRIs did not show any new hyperintense spot compared

to preoperative ones (Fig. 2). Postoperative right carotid

angiogram showed patent cervical CCA-ICA, ECA, and

robust anterograde opacification of the whole right

a radiata and watershed area of the right cerebral hemisphere. Lower left:

n with residual stump several centimeters from the origin at right innominate

n (lateral view) through vertebral muscular branch. Lower right: left carotid

l hemisphere and delayed retrograde opacification of cavernous to petrous

Fig. 2. Left: postoperative right carotid angiogram (lateral view) showing patent cervical CCA-ICA and ECA. Upper right: right carotid angiogram (lateral

view) showing robust anterograde opacification of the whole right intracranial ICA area. Lower right: postoperative diffusion-weighted MRIs did not show any

new hyperintense spot compared to preoperative ones.

T. Inoue et al. / Surgical Neurology 69 (2008) 620–626622

intracranial ICA area (Fig. 2). The patient’s neurologic

status, especially mental decline and left side neglect, was

significantly improved. At 17 months follow-up after

surgery, MRI/MRA continued to show patent right CCA-

ICA without evidence of new ischemic lesions (Fig. 3).

The patient is walking and leading an almost independent

life although hemiparesis of the left upper extremity is

still present.

2.2. Case 2

This 75-year-old man presented to another hospital

complaining of recent mental decline and forgetfulness.

His medical history was significant for smoking, diabetes

mellitus, hypertension, and angina pectoris. Carotid ultra-

sonography was performed, and results suggested severe

right carotid stenosis. He was referred to our hospital for

possible surgical intervention. Neurologic examination

showed no focal deficit, although Wechsler Memory Scale

showed significantly impaired visual memory scale com-

pared to verbal memory scale, suggestive of obtunded right

cerebral hemisphere function. Magnetic resonance images

showed multiple lacunar infarctions with slight cerebral

atrophy compatible with his age. Cerebral angiography

demonstrated right CCA occlusion with residual stump

opacified several centimeters from the origin at right

innominate artery. Collateral filling of right ECA back to

the carotid bifurcation that led to very delayed and faint

anterograde filling of cervical ICA up to cavernous portion

was seen from vertebral injection through vertebral

muscular branch. In addition, vertebral injection showed

moderate flow toward the right ICA area through PcomA

(Fig. 4). After a thorough discussion, and considering that

carotid bifurcation is still open through vertebral collateral

in this patient, we decided to proceed with direct and

primary carotid endarterectomy to reopen the CCA-ICA

anterograde flow. Details of this surgical procedure are

Fig. 3. Cervical MRA (left) and intracranial MRA (upper right) obtained at 17 months follow-up (after surgery), showing still patent right CCA-ICA flow.

T. Inoue et al. / Surgical Neurology 69 (2008) 620–626 623

almost the same as in case 1 (Fig. 5). Postoperatively,

to reduce the risk of hyperperfusion, rigorous attention

was paid to keep the systolic blood pressure lower than

Fig. 4. Left: preoperative right carotid injection (anteroposterior view) showing C

origin at right innominate artery. Upper right: vertebral injection (lateral view, e

bifurcation through vertebral muscular branch. Moderate flow toward the right

(lateral view, late arterial phase) shows delayed and faint anterograde filling of cer

ICA collateral.

120 mm Hg for several days. Postoperative diffusion-

weighted MRIs were not performed because of contraindi-

cation (recent coronary stenting), although CT scan of the

CA occlusion with residual stump opacified several centimeters from the

arly arterial phase) showing collateral filling of right ECA back to carotid

ICA area through PcomA was also noted. Lower right: vertebral injection

vical ICA up to cavernous portion through vertebral muscular branch-ECA-

Fig. 5. Upper left: after exposure of carotid bifurcation. Distal ICA (blue tape) and ECA (red tape) were exposed beneath hypoglossal nerve. Awell-developed

vasa vasorum was also noted. Lower left: CCAwas exposed proximally after ligation and resection of omohyoideus muscle. The most proximal portion (at the

level of superior margin of clavicle) of CCA was secured with tourniquet. Upper right: atheromatous plaque was dissected as usually done in carotid

endarterectomy. Total occlusion of CCA near the carotid bifurcation by atheromatous plaque and the retrograde extension of organized thrombus was noted.

Lower right: after removal of plaque, the inner surface of the vessels looked smooth with some oozing of blood showing viable media. (For interpretation of the

references to color in this figure legend, the reader is referred to the web version of this article.)

T. Inoue et al. / Surgical Neurology 69 (2008) 620–626624

head performed at postoperative day 1 did not show any new

low-density area. Postoperative right carotid angiography

showed patent cervical CCA-ICA, ECA, and robust ante-

rograde opacification of the whole right intracranial ICA area

Fig. 6. Left: postoperative right carotid angiogram (lateral view) showing patent

showing robust anterograde opacification of the whole right intracranial ICA are

(Fig. 6). The patient was discharged without new neurologic

deficit. At 6 months follow-up after surgery, the subject is

leading an independent life without a stroke episode.

Magnetic resonance imaging/MRA continued to show patent

cervical CCA-ICA and ECA. Right: right carotid angiogram (lateral view)

a.

Fig. 7. Left and upper right: cervical MRA (left) and intracranial MRA (upper right) obtained at 6 months follow-up (after surgery) showing still patent right

CCA-ICA flow. Lower right: T2-weighted MRIs (6 months after the operation) showing no new ischemic lesion.

T. Inoue et al. / Surgical Neurology 69 (2008) 620–626 625

right CCA-ICA without the evidence of new ischemic

lesions (Fig. 7).

3. Discussion

Although the symptomatic CCA occlusion is a rare

condition, it is associated with poor prognosis due to very

restricted carotid collateral flow [2]. In the treatment of

progressive ischemia cases, the difficulty of using ipsilateral

ECA as surgical revascularization source raises a strategic

dilemma. Riles et al [7] have classified CCA occlusion into

4 types: type 1A, CCA occlusion with patent distal ICA and

ECA; type 1B, CCA occlusion with patent ECA only; type

1C, CCA occlusion with patent ICA only; type 2, complete

occlusion of the CCA-ICA-ECA. Various surgical revascu-

larizations for type 1 CCA occlusion have been reported,

mainly using extrathoracic-cervical bypass including SA to

ICA, SA (or transverse cervical artery, thyrocervical trunk)

to ECA with or without STA-MCA bypass [1,3,5,6].

However, direct carotid endarterectomy for CCA occlusion

to achieve primary restoration of CCA-ICA flow seems to

have been rarely performed and has not been well discussed.

If the conditions are well delineated, in which successful

restoration of primary CCA-ICA flow is safely achieved

with long-term patency, direct carotid endarterectomy would

be easier compared to previously mentioned complex

bypass procedures.

In these 2 cases, we noted 3 key issues to judge if the

primary carotid endarterectomy for CCA occlusion is

possible preoperatively and during surgical procedure. First,

we need to evaluate the patency of distal ICA. In case 2,

preoperative vertebral angiogram showed patent both distal

ECA and ICA (Riles type 1A). However, in case 1,

preoperative vertebral angiogram demonstrated only retro-

grade ECA filling as proximal as occipital artery, although

the ipsilateral retrograde cavernous to petrous ICA opaci-

fication was noted through cross-flow in delayed arterial

phase of contralateral carotid injection. Therefore, in the

preoperative evaluation, we could determine that at least still

patent ECA back to near carotid bifurcation, however, were

uncertain as for the distal ICA patency. During surgery, by

confirming substantial back flow from small arteriotomy in

distal carotid ICA, we could determine the patency of distal

ICA for certain. In the series of carotid endarterectomy for

ICA occlusion (with patent CCA and ECA), the retrograde

reflux visualization of occluded ICA back to the cavernous

T. Inoue et al. / Surgical Neurology 69 (2008) 620–626626

portion or further back to the petrous portion in preoperative

angiography has been associated with 50% and 71%

successful reopening of ICA, respectively [4]. Second, we

need to secure bsoundQ proximal CCA end. In the 2 cases,

preoperative angiography showed still opacified CCA

stump several centimeters from innominate artery, and

during operation, bsoundQ proximal CCA, which was

externally soft on palpation and with internally thin enough

intima after removal of plaque, was obtained by extending

the skin incision up to the superior margin of the clavicle

and splitting the omohyoideus muscle. If the organized

occlusion of CCA extends as far as its origin, the application

of direct carotid endarterectomy would be limited. In

addition, we need to consider the occluded side because

right CCA origin (innominate artery) is easier to access than

left CCA origin (aorta). Because the present 2 cases were

both right-side occlusion, we were able to secure the

proximal end relatively easily based on the several-

centimeter stump in preoperative angiography. In the left-

side case, a longer residual stump that extends at least above

the superior margin of clavicle would be needed to secure

the proximal end. Third, the condition of adventitia and

media across the occluded CCA before and after removal of

atheromatous plaque as well as organized thrombus need to

be evaluated during the operation to obtain a safe and long-

term patency. In both cases, enough vasa vasorum was

obvious externally after exposure of occluded CCA showing

bsoundQ adventitia and, internally, some oozing of blood

from media was noted after removal of plaque across

completely occluded portion.

In conclusion, direct carotid endarterectomy for CCA

occlusion to restore primary CCA-ICA flow is possible, and

good midterm patency as well as neurologic results can be

expected, although several special conditions need to be

evaluated preoperatively and during the procedure.

References

[1] Kobayashi T, Houkin K, Ito F, Kohama Y. Transverse cervical artery

bypass pedicle for treatment of common carotid artery occlusion: new

adjunct for revascularization of the internal carotid artery domain.

Neurosurgery 1999;45:299 -302.

[2] Levine SR, Welch KMA. Common carotid artery occlusion. Neurology

1989;39:178-86.

[3] Martin III RS, Edwards WH, Mulherin JL, Edwards Jr WH. Surgical

treatment of common carotid artery occlusion. Am J Surg

1993;165:302 -6.

[4] McCormick PW, Spetzler RF, Bailes JE, Zabramski JM, Frey JL.

Thromboendarterectomy of the symptomatic occluded internal carotid

artery. J Neurosurg 1992;76:752-8.

[5] Melgar MA, Sahni D, Weinand M. Throcervical trunk-external carotid

artery bypass for positional cerebral ischemia due to common carotid

artery occlusion. Technical note. J Neurosurg 2005;103:170 -5.

[6] Rabb CH, Moneta GL. Staged cerebral revascularization in a patient

with an occluded common carotid artery. Stroke 2005;36:e68-e70.

[7] Riles TS, Imparato AM, Posner MP, Eikelboom BC. Common

carotid occlusion. Assessment of the distal vessels. Ann Surg 1984;

199:363-6.

Commentary

This is a nice compilation of 2 cases, emphasizing what I

believe are still highly selective cases, where diagnostic

intra-arterial angiography is essential to document patent

arterial systems, and to craft revascularization procedures to

the angioarchitecture defined. This rare syndrome was

expertly managed by common carotid endarterectomy and

restoration of flow, with primary CCA repair. One would

expect, as the authors have demonstrated, long-term patency

from this operative approach. It is also of note that, with the

watershed infarct in patient 1, significant attention to

postoperative blood pressure management is essential,

because the risk of hyperperfusion and its intracranial

complications is a concern. I would also add, although the

authors did not cover this in their discussion, that a series of

Fogarty catheters can be quite useful in this scenario,

particularly if the common carotid origin is out of view and

accessibility in the operative field. Neurosurgeons would do

well to continue using intra-arterial angiography in select

cases, to tailor restoration of flow, to what the patient’s

angioarchitecture requires. The authors should be congrat-

ulated for bringing it to our attention again.

John L.D. Atkinson, MD

Department of Neurosurgery

Mayo Clinic

Rochester, Minnesota 55905, USA