Patients with head and neck cancers and associatedpostirradiated carotid blowout syndrome:Endovascular therapeutic methods and outcomesFeng-Chi Chang, MD,a,b Jiing-Feng Lirng, MD,a,b Chao-Bao Luo, MD,a,b Shuu-Jiun Wang, MD,c,d

Hsiu-Mei Wu, MD,a,b Wan-Yuo Guo, MD, PhD,a,b Michael Mu Huo Teng, MD,a,b andCheng-Yen Chang, MD,a,b Taipei, Taiwan

Purpose: This study retrospectively evaluated the technical and hemostatic outcomes of reconstructive and deconstructiveendovascular management in patients with head and neck cancers associated with carotid blowout syndrome (CBS).Methods: Twenty-four patients with head and neck cancers with CBS involving the main trunk of carotid artery underwentendovascular therapy. This included reconstructive management with self-expandable stent grafts to preserve the diseasedcarotid artery in 11 patients and deconstructive management with balloons, coils, or acrylic adhesives to occlude thediseased carotid artery in 13 patients. Based on clinical severity and therapeutic priority, we classified CBS in our patientsinto two groups: acute or impending and threatened. The angiographic severity was graded from 0 to 3. Evaluation oftechnical outcome included technical success, initial and delayed complications, and patency of stent graft in thereconstructive group. The hemostatic outcome was evaluated by immediate hemostatic result, rebleeding, and durationof hemostasis. Sex, age, clinical and angiographic severities, local wound complications, and location of the pathologiclesion were examined as predictors of the technical and hemostatic outcomes of endovascular management by using Coxregression method.Results: Technical success and immediate hemostasis were achieved in all patients of both groups. Initial complicationsduring the procedures were encountered in four patients (36.4%) who underwent reconstructive management and in onepatient (7.7%) who underwent deconstructive management (P � .142). Delayed complications during the follow-up wereseen in one patient (9.1%) with reconstructive management and one patient (7.7%) with deconstructive management (P >.99). Rebleeding occurred in five patients (45.5%) in the reconstructive management group and in three patients (23.1%)in the deconstructive management group (P � .659). The mean duration of hemostasis after initial reconstructive anddeconstructive management was 4.0 � 8.1 and 8.5 � 10.1 months, respectively (P � .249). Rebleeding was noted in 7of 11 patients (63.6%) with acute CBS and in 1 of 13 patients (7.7%) with impending and threatened CBS (P � .008).Conclusion: There is no significant difference in technical and hemostatic outcomes between the reconstructive anddeconstructive endovascular management methods. Hemostatic results were influenced by clinical severity. The rebleed-

ing rate is higher in patients with advanced and acute clinical severity. ( J Vasc Surg 2008;47:936-45.)

Carotid blowout, or rupture of the carotid artery (CA),is a life-threatening complication associated with head andneck cancer and its therapy.1,2 The reported incidence ofCA rupture after radical neck dissection is 4.3%.3 Patientswith carotid blowout syndrome (CBS) can have a variety ofclinical presentations due to rupture of the CA, includingacute hemorrhage or exposure of part of the CA.4-6 Carotidblowout syndrome tends to occur in patients with head andneck cancers and those with radiation-induced necrosis,recurrent tumors, wound complications, or pharyngocuta-neous fistulas.1-4

Emergency surgical management of CBS is often tech-nically difficult to perform in previously irradiated areas andis associated with high neurologic morbidity and mortality

Department of Radiology,a and Neurological Institute,c Taipei VeteransGeneral Hospital; School of Medicine,b and Department of Neurology,d

National Yang Ming University.Competition of interest: none.Reprint requests: Feng-Chi Chang, Department of Radiology, Taipei Vet-

erans General Hospital, 201 Shih-Pai Rd, Sec 2, Taipei, Taiwan 11217ROC (e-mail: fcchang@vghtpe.gov.tw).

0741-5214/$34.00Copyright © 2008 by The Society for Vascular Surgery.

doi:10.1016/j.jvs.2007.12.030

936

rates. The reported average neurologic morbidity and mor-tality rates associated with surgical management of CBS are40% and 60%, respectively.7 Deconstructive endovasculartherapy, such as with permanent balloon occlusion of thediseased carotid artery, has improved outcomes1,6,7; how-ever, as many as 15% to 20% of patients with CBS who aretreated with permanent carotid occlusion experience im-mediate or delayed cerebral ischemia.1,8 A balloon occlu-sion test may be performed before threatened CBS istreated definitively, but this test is usually not possible inacute cases. In addition, test occlusion or even positronemission tomography studies may not help in identifyingthe small subset of patients in whom delayed hemodynamicischemia develops after the carotid artery is permanentlyoccluded.1,4,7-9 These results highlight the limitations ofdeconstructive endovascular therapy for patients with CBS.

Stent grafting has the potential to preserve the diseasedCA and achieve hemostasis. Some authors report it as prom-ising in treating CBS in patients at risk of CA occlusion8,10;however, some studies have described unfavorable long-termoutcomes.5,11-13 Therefore, the purpose of this study was tocompare the technical and hemostatic outcomes of endovas-

cular reconstruction using self-expandable stent grafts with

JOURNAL OF VASCULAR SURGERYVolume 47, Number 5 Chang et al 937

those of endovascular deconstruction using balloons, coils,or acrylic adhesive in the management of CBS in patientswith head and neck cancers. We also provide an assessmentof the clinical severity in our patients compared with theirangiographic findings to highlight the importance of earlydiagnosis and management of CBS.

MATERIALS AND METHODS

Patient population. This retrospective study was ex-empt from Institutional Review Board approval. Writtenconsent was obtained from each patient or the family beforeintervention. From 2003 to 2006, 1632 patients with headand neck cancers were treated in our institute, and 56patients sustained CBS. Two patients could not accepteither surgical or endovascular management due to profusehemorrhage with hypovolemic shock. Two patients weretreated with surgical ligation.

The study excluded 28 patients because their patho-logic lesions involved the branches of external carotid artery(ECA) that were only eligible for deconstructve manage-ment. The study included 24 patients with CBS involvingthe main trunk of the CA (Table I). We included thesepatients because the locations of their pathologic lesionscould be treated by either reconstructive or deconstructiveendovascular therapy. Eleven men with a mean age of 49.2 �7.8 years (range, 35-65 years) underwent reconstructive

Table I. Baseline characteristics of patients with reconstru

Variable Reconstructive (n

Sex, No (%)Male 11 (100)Female 0 (0)

Age, mean � SD (range) years 49.2 � 7.8 (35Clinical cancer diagnosis, No.

Nasopharyngeal 1Hypopharyngeal 5Laryngeal 2Tongue 1BuccalSinusParotid gland 1Tonsil 1

Local complications, No.Fistular formationa 5Wound complicationsb 10

CBS group, No (%)Acute 5 (45.5)Impending and threatened 6 (54.5)

Angiographic grade, No (%)0 and 1 3 (27.3)2 and 3 8 (72.7)

Location of lesion (n � 28) 13ICA, No (%) 2 (15.5)CAB, No (%) 5 (38.4)CCA, No (%) 6 (46.1)ECA, No (%) 0 (0)

CAB, Carotid artery bifurcation; CBS, carotid blowout syndrome; CCA, coaPharyngocutaneous or aerodigestive.bNecrosis, ulceration, sinus tract.

endovascular surgery in which self-expandable stent grafts

were placed to preserve the diseased CA. Thirteen patients(10 men and 3 women) with a mean age of 51.4 � 9.9 years(range, 34-67 years) underwent deconstructive endovascu-lar surgery in which the permanent CA occlusion was done.All patients had received radiation therapy or chemoradio-therapy and presented with various degrees of irradiation-induced change in their head and neck regions. Previoussurgical therapy for the malignancy had been done in 8 ofthe 11 patients in reconstructive group and 10 of the 13patients in the deconstructive group.

Clinical severity was used to classify CBS into threetypes: acute, impending, and threatened1,7:

● Acute CBS was defined as profuse hemorrhage thatwas not controlled with surgical packing, with thevessel being completely ruptured, and the patient’scondition deteriorating rapidly if immediate resuscita-tion and stabilization had not been accomplished be-fore definite treatment.

● Impending CBS was defined as short episodes of sen-tinel hemorrhage that resolved spontaneously or withsimple surgical packing; however, complete rupturewas a certainty.

● Threatened CBS was defined as exposure of the CAbecause of wound breakdown or neoplastic invasion ofthe carotid system; and although the hemorrhage had

and deconstructive endovascular management

) Deconstructive (n � 13) P

10 (76.9) .2233 (23.1)

51.4 � 9.9 (34-67) .557

3 .5961 .0611 .5761 13 .2232 .4822 1

.458

6 .97311 1

6 (46.1) .9737 (53.9)

5 (38.5) .7698 (61.5)

157 (46.7) .1153 (20) .4102 (13.3) .0963 (20) .226

n carotid artery; ECA, external carotid artery; ICA, internal carotid artery.

ctive

� 11

-65)

mmo

not yet occurred, rupture was almost inevitable if the

JOURNAL OF VASCULAR SURGERYMay 2008938 Chang et al

exposed vessel was not promptly covered with healthyvascularized tissue.

Based on therapeutic priority, we further classified CBSin our patients into two groups: (1) acute and (2) impend-ing and threatened. The patients of the former group had aclinical emergency that required emergency treatment. Thelatter group was composed of patients whose status couldbe treated more electively.

Locations of pathologic vascular lesions, such aspseudoaneurysms, were recorded as the internal carotidartery (ICA), carotid bifurcation (CBF), ECA, or commoncarotid artery (CCA). The ECA was designated the maintrunk of ECA proximal to the orifice of linguofacial trunk.

If endovascular management was anticipated, a balloontest occlusion was attempted if the patient was hemody-namically stable and not bleeding profusely. A standardizedprotocol has been described in detail in the literature.1,7

The indications for reconstructive endovascular therapywere the patients at risk of permanent carotid occlusion,such as incomplete circle of Willis on angiograms (patients3 and 4), contralateral carotid severe stenosis or totalocclusion, intolerance to a balloon occlusion test (patients8, 10, and 11), or emergency status of the patient preclud-ing an occlusion test (patients 1, 2, 5-7, and 9).7,9 Thedeconstructive method was done for patients without theabove risks of carotid occlusion (patients 1-5, 7, and 10-12)or for those refused reconstructive management (patients6, 8, 9, and 13).

Angiographic evaluation. We used a transfemoral ar-terial approach to obtain a complete neuroangiogram ofthe supra-aortic arteries and their branches. The angio-graphic findings were used to classify the severity of vascularinjury as grades 0 to 3.14 A grade of 0 meant no angio-graphic vascular disruption. Grade 1 was defined as focalirregularity or slight focal bulging of the diseased CA, suchas a focal weakening in the vascular wall. Grade 2 wasdefined as a pseudoaneurysm of the injured CA, in whichthere was a focal CA rupture confined by the integrity of thesurrounding tissue. Grade 3 was defined as active extrava-sation from the completely ruptured CA. We further clas-sified grades 0 and 1 as slight carotid injury and grades 2and 3 as advanced carotid disruption. The former grouphad a complete or weakening vascular wall. The lattergroup had an incomplete or ruptured vascular wall. Wecompared these angiographic findings with the clinicalseverities and patient outcomes.

Medication for reconstructive management. Patientswith threatened CBS were premedicated with a dual anti-platelet regimen consisting of orally administered aspirin(324 mg) and clopidogrel (300 mg) 1 day before treat-ment. Patients with acute or impending CBS were prophy-lactically given intravenous glycoprotein IIb/IIIa receptorinhibitor (Aggrastat; Merck & Co, Inc, West Point, Pa)during the interventional procedure.11 We gave an initialintravenous infusion at 0.4 �g/kg/min for 15 to 20 min-utes, followed by continuous infusion at 0.1 �g/kg/min

for 4 to 6 hours after the procedure. Approximately 50 to

70 U/Kg of heparin was also given to keep the activatedclotting time �250 seconds.

After deployment of the self-expandable stent graft, adual antiplatelet regimen with aspirin (324 mg) and clopi-dogrel (75 mg) was begun. One month later, this regimenwas changed to aspirin (100 mg) for life-long use. Becausepatient 4 sustained a brain abscesses after the stent graftdeployment, we gave 4-week prophylactic antibiotic ther-apy to patients 7 through 11.

Reconstructive management. After identifying thepathologic lesions, we exchanged the diagnostic catheterand wire to a 10F or 11F introducer sheath and a .0.35-inch, 300-cm Amplatz exchange wire (Cook, Blooming-ton, Ind) through the right femoral artery into the cervicalICA. A self-expandable Wallgraft stent graft (Boston Sci-entific Corp, Natick, Mass) was then advanced along thisexchange wire to the CA, where it was appropriately de-ployed11 (Fig 1). To avoid rebleeding from reconstitutionthrough the branches of ECA, we placed fiber coils in themain trunk of the ECA before deployment of stent grafts ifthe pathologic lesions were close to the CBF. A controlangiogram was obtained immediately and 15 minutes afterdeployment of the stent graft to confirm appropriate posi-tioning of the stent graft and patency of the CA.11 Thereconstructive endovascular management was consideredcomplete when adequate coverage of the pathologic lesionby stent graft was achieved or clinical hemostasis wasreached, or both.

Deconstructive management. A 7F Shuttle sheath(Cook, Minneapolis, Minn) was placed through the femo-ral artery to the diseased CCA. Two types of deconstructivemanagement were used in this study: cross occlusion andproximal occlusion. Cross occlusion consisted of deploy-ment of embolic materials from the pathologic lesion orfrom the CA distal to the pathologic lesion to its proximalsite (Fig 2). In such situations, we advanced two microcath-eters into the CA. One “distal microcatheter” was advancedto the CA of the pathologic lesion or distal to it, and theother “proximal microcatheter,” mounted with a detach-able balloon, was placed in the CA proximal to the lesion.

We inflated and deployed the detachable balloon fromthe proximal microcatheter first. We then deployed micro-coils (Target Therapeutics, Fremont, Calif), injected acrylicadhesive (Histoacryl, Braun, Germany), or deployed a pre-mounted balloon through the distal microcatheter to oc-clude the pathologic lesion and its adjacent CA. Proximalocclusion consisted of placing the embolic materials in theCA proximal to the pathological lesions. At least two de-tachable balloons were serially inflated and deployed toensure permanent vascular occlusion.1 Proximal occlusionwas used in cases when associated focal carotid stenosis ortortuosity impeded the balloon or microcatheter position-ing to cross the lesions. Successful deconstructive manage-ment was defined as complete obliteration of the patho-logic lesion and the related CA and the achievement ofclinical hemostasis.

Outcome evaluation. Immediate postprocedural out-

comes were evaluated by the interventional neuroradiolo-

JOURNAL OF VASCULAR SURGERYMay 2008940 Chang et al

gists or by a clinical oncologist, or both. Evaluation oftechnical outcomes included technical success, initial anddelayed complications, and patency of the stent grafts of thereconstructive group. The complications presented duringthe therapeutic procedures were defined as “initial,” andthose presented after the procedures were defined as “de-layed.” Hemostatic outcomes were evaluated by the imme-diate hemostatic results, presence of rebleeding, and dura-tion of hemostasis. Patients in the reconstructive groupunderwent follow-up contrast-enhanced computed to-mography (CT), CT angiography, ultrasonography, orconventional angiography within the first month and thenevery 2 to 4 months so that patency of the stent grafts couldbe assessed. Patients in the deconstructive group under-went regular clinical outpatient department follow-up ev-ery 6 months. If rebleeding occurred, emergency angiog-raphy and interventional management were performed.Follow-up lasted a median of 4 months (mean, 9.34 �11.42 [range, 0.1-37] months).

Statistical analysis. We analyzed the technical out-comes and hemostatic outcomes of our patients, includingtechnical success, initial and delayed complications, patencyof the stent grafts in the reconstructive group, immediatehemostasis, presence of rebleeding, and duration of hemo-stasis after initial intervention by using the t test, �2 test, orFisher exact test, when appropriate. Age, sex, type of CBS,local wound complication, angiographic severity, locationof the pathologic lesion, and type of endovascular manage-ment were examined as predictors for outcome analysis byusing Cox regression analysis. Clinical severity of CBS wascorrelated with angiographic severity by using the Fisherexact test. For all analyses, P � .05 was considered statisti-cally significant.

RESULTS

Baseline characteristics. Table I summarizes thebaseline characteristics of all patients. Adjustments for sex,age, clinical diagnosis, local wound complication, clinicaland angiographic severity, and location of pathologic lesion(including lesions in ICA and other than ICA) did notaffect the results.

Clinical and angiographic classification. The corre-lation between clinical and angiographic severity is shownin Fig 3. Pseudoaneurysms (grade 2) were the most com-mon angiographic findings and were present in all clinicalgroups. Active extravasation (grade 3) was only noted inpatients with acute CBS. All 11 patients with acute CBShad advanced (grade 2 and 3) carotid disruption on angio-gram (100%). Clinical severity correlated well with theangiographic severity (P � .002).

Fig 1. A, Left carotid angiogram in patient 10 of the reccarotid artery (grade 0, arrow). B, Contrast-enhanced axisinus tract (arrowheads) close to the left common carotimultiplanar reformatted images) of the left carotid artermonths later, obvious distal marginal stenosis was noted

(arrows) surrounding the stent grafts caused “floating” of left

Technical outcome. Endovascular management wassuccessfully accomplished in all 24 patients during theinitial procedures (Tables II, III, and IV). Four initialcomplications (36.4%) occurred in the 11 patients in thereconstructive group, including acute thromboembolismin three patients, and dissection and a type 3 endoleak inone patient. Only one of these four initial complicationswas symptomatic (patient 3). A delayed complication in thereconstructive group included septic thrombosis of thestent graft with multiple brain abscesses in one patients(9.1%).

Of the 13 patients in the deconstructive group, aninitial complication was an acute infarction in the territoryof MCA in one patient (7.7%). One patient (7.7%) alsopresented with brain abscess as a delayed complication afterdeconstructive management. An initial complication wasnoted in one of six patients (16.7%) in the deconstructivegroup with pathologic lesions located in the CA other thanICA and no patients with a lesion located in the ICA (P �.462). Delayed complications were found in two of sevenpatients (28.6%) with pathologic lesions located in ICA andone of six patients (16.7%) with lesions located in the CAother than ICA (P � .612).

Follow-up imaging performed �3 months demon-strated that nine patients (except for patients 1 and 2) in thereconstructive group had patent stent grafts. Varying de-grees of distal marginal stenosis were noted in five of the sixpatients (83.3%) in the reconstructive management groupafter a 3-month follow-up. One (patient 9) of these fivepatients was successfully treated with angioplasty and stent-ing 3 months after the initial intervention. Of the sixpatients who were followed up longer than 3 months, three(50%) had occluded stent grafts, and two of these (patients6 and 7) were asymptomatic. Patient 4 presented withseptic thrombosis and multiple brain abscesses. The meanduration of stent graft patency was 3.0 � 2.6 months.

Hemostatic outcome and survival analysis.Immediate hemostasis was achieved in all patients in bothgroups after the interventional procedures (Tables II, III,and IV). Seven episodes of rebleeding were noted in five ofthe 11 patients (45%) in the reconstructive group. All ofthem had acute CBS, and rebleeding resulted in death intwo of these patients. The other three patients, in whomfive episodes of rebleeding from the same diseased CAsoccurred, were successfully managed by reintervention.The duration of hemostasis after initial reconstructive man-agement was a mean of 4.0 � 8.1 months (range, 0.02-9months). Three of the 13 patients (23.1%) had rebleeding3 months after initial deconstructive management. All whohad rebleeding had undergone proximal occlusion (3 of 5

uctive group showed only slight stenosis in the commonputed tomography (CT) of the neck revealed a necrotic

ry (arrow). C, Reconstructive CT angiography (curvedonth later showed patency of the stent grafts. D, Four

wheads). Large area of soft tissue necrosis and ulceration

onstral comd artey 1 m(arro

carotid artery (long arrows).

JOURNAL OF VASCULAR SURGERYVolume 47, Number 5 Chang et al 941

patients, 60%). The mean duration of hemostasis afterinitial deconstructive management was 8.5 � 10.1 months(range, 0.5-37 months).

The mean survival of patients was 11.9 � 4.8 months inthe reconstructive group and 12.2 � 4.1 months in thedeconstructive group. No predictors for survival werefound using Cox regression analysis.

Statistical analysis. There were no significant differ-ences in initial and delayed complications, rebleeding rate,duration of hemostasis, and survival time between thereconstructive and deconstructive groups (Table IV). Pa-tients in the deconstructive group who had undergonecross occlusion had a lower rebleeding rate than those whounderwent proximal occlusion (0% vs 60%, P � .035).

The rebleeding rates of hemostatic outcome were cor-related with clinical severity (Table V). Patients with acuteCBS had a higher bleeding rate (P � .008). There were nostatistically significant differences in technical outcome andduration of hemostasis with clinical severity.

DISCUSSION

Carotid blowout syndrome in patients with head andneck cancers often results in catastrophic hemorrhage. Al-though deconstructive endovascular therapy has improvedpatient outcomes, it carries a risk of cerebral ischemia.1,6

Reconstructive endovascular therapy for CBS with stentgrafts has been proposed; however, recent reports haveshown unfavorable durable hemostasis and long-term out-comes.5,7 In our previous study, we treated eight CBSpatients with high risk of carotid occlusion with stent

Fig 2. A, Right carotid angiograms in patient 8 of the decon-structive group showed a ruptured internal carotid artery withactive extravasation (grade 3, arrows). B, Cross occlusion wasperformed with deployment of two balloons distal and proximal tothe pathologic lesions (arrows). A mixture of liquid adhesives wasinjected in the internal carotid artery between the 2 balloons

Fig 3. Graph shows correlation of clinical severity (groups: acute,impending, and threatened) with angiographic severity (grades 0,1, 2, and 3).

(arrowheads).

JOURNAL OF VASCULAR SURGERYMay 2008942 Chang et al

grafts.11 The results were not satisfactory on the basis oftheir poor technical outcomes (no stent graft patency after3-month follow-up) and poor hemostatic outcomes (50%rebleeding rate). We therefore ended the application ofstent grafts to treat these cancer patients with CBS inemergency or temporary practice.

Recently, however, we found distal marginal stenosiswas a common cause of stent graft occlusion and inade-quate coverage of the ongoing pathologic lesion by the

Table II. Summary of reconstructive management of 11 p

Patient

Technical outcome

Initial management:stent graft (mm)a

Complications:initial/delayed

(time)Follostent

1 8 � 50 AcuteasymptomaticICA thrombosis,occlusion/none

Not a

2 8 � 30 None/none Not a

3 8 � 50c Embolic infarct,treated withthrombolytictherapy/none

1 mo:

4 8 � 50c None/brain abscess(4 mo)

2 mo:4 mthro

5 9 � 70 None/none 0.5 m

6 7 � 30 Transientasymptomaticin-stentthrombosis/none

3 mo:6 masymthro

7 8 � 50 None/none 3 mo:3.7sten6 masymthro

8 9 � 70 None/none 0.5 m

9 8 � 50c Asymptomatic CAdissection treatedwith 7 � 40Wallstente/none

4 mo:trea7 �Walmo:

10 8 � 50, 9 � 70c None/none 4 mo:

11 8 � 50, 9 � 70c None/none 4 mo:

CA, Carotid artery; ICA, internal carotid artery; UGI, upper gastrointestinInitial technical success and immediate hemostasis were achieved in all patieaWallgraft: Boston Scientific Corporation, Natick, Mass.bTime of follow-up.cPlus fiber coils in the external carotid artery.dDistal marginal stenosis.eCarotid Wallstent: Boston Scientific Corporation.

stent graft was a cause of the rebleeding. With technical

improvement to manage these complications, we have seenbetter recent outcomes than the previous work. Therefore,we designed this study to test if endovascular reconstruc-tion by using self-expandable stent grafts has worse techni-cal and hemostatic outcomes than those of endovasculardeconstruction by using balloons, coils, or acrylic adhesiveto manage CBS in patients with head and neck cancers. Wefound the difference of the outcomes between these 2methods was insignificant. The outcomes were significantly

ts with carotid blowout syndrome

Hemostatic outcome

forncy

Time of rebleeding/reintervention

Outcome/timeb

(cause of death)

ble 0.6 mo, diseaseprogression/none

Died/0.6 mo (rebleeding)

ble 0.1 mo, inadequatecoverage of the lesion/none

Died/0.1 mo (rebleeding)

cy None Died/2 mo (diseaseprogression)

cy;tic

sis

None Alive/28 mo

ency None Died/1.5 mo (diseaseprogression,mediastinitis)

sisd;

aticsis

0.5 mo, diseaseprogression/9 � 50Wallgraft

Died/36 mo (lungmetastasis)

cy;

;

aticsis

2 mo, diseaseprogression/8 � 50Wallgraft; 3 mo/directpercutaneous punctureof ECA forembolization

Alive/27 mo

ency None Died/1 mo (lungmetastasis)

sisd

ith

e; 9ncy

0.02 mo, type 3 endoleakby the Wallstente/9 �70 Wallgraft, directpercutaneous puncturefor embolization;9 mo, recurrent type3 endoleak/10 �70-mm Wallgraft

Died/9.1 mo (transfusioncomplication, sepsis)

sisd None Died/4.5 mo (sepsis,disease progression)

sisd None Died/4 mo (UGIbleeding, transfusioncomplication)

atien

w-uppate

pplica

pplica

paten

pateno: sepmbo

o: pat

stenoo:ptommbopatenmo:osisd

o:ptommbo

o: pat

stenoted w50

lstentpate

steno

steno

al.nts.

influenced by the clinical severity of CBS of our patients.

JOURNAL OF VASCULAR SURGERYVolume 47, Number 5 Chang et al 943

At present, no preoperative test is sufficiently accurateto justify the occlusion of a patent CA or predict whether itwill cause a neurologic deficit. Autogenous venous or arte-rial reconstruction has been proposed in the treatment ofpatients with advanced head and neck cancers with invasionto the carotid system.15 This autogenous tissue reconstruc-tion is valuable in avoiding cerebral ischemic insult whencomplete resection of the tumor and CA is needed. Com-pared with surgical autogenous tissue reconstruction, themerits of endovascular stent graft reconstruction include:

1. Less invasiveness because the endovascular reconstruc-

Table III. Summary of deconstructive management of 13

Patient

Technical outcome

Initial management:permanent carotid occlusion

(method)Complications:

initial/delayed (time

1 NBCA w/prox balloon (B) None/none

2 NBCA w/prox balloon (B) None/none3 NBCA w/prox balloon (B) None/none4 2 balloons (B) None/none

5 2 balloons (A) None/none6 Coils, NBCA w/prox

balloon (B)None/none

7 2 balloons (A) None/none

8 Distal balloon, NBCA w/prox balloon (B)

None/none

9 2 balloons (A) Embolic infarct/non10 2 balloons (A) None/brain abscess

(0.5 mo)11 NBCA w/prox balloon (B) None/none

12 2 balloons (A) None/none13 10 fiber coils w/prox

balloon (B)None/none

(A), Proximal occlusion; (B), cross occlusion; NBCA, N-Butyl-2-cyanoacryInitial technical success and immediate hemostasis were achieved in all patieaTime of follow-up.

Table IV. Analysis of technical and hemostatic outcomesof reconstructive and deconstructive endovascularmanagement

OutcomeReconstructive

(n � 11)Deconstructive

(n � 13) P

Technical outcome,No. (%)

Initial complication 4 (36.4) 1 (7.7) .142Delayed complication 1 (9.1) 1 (7.7) �.99

Hemostatic outcomeRebleeding, No. (%) 5 (45.5) 3 (23.1) .659Hemostasis duration,

mean � SD mo 4.0 � 8.1 8.5 � 10.1 .249Survival time, mean �

SD mo 11.9 � 4.8 12.2 � 4.1 .547

tion can be performed under local anesthesia and does

not need any tissue harvesting. It also needs no explo-ration in the soft tissue of the irradiated neck region.

2. No temporary interruption of CA flow because endo-vascular reconstruction does not need temporary clamp-ing of the CA for vascular replacement and thus mayreduce the risk of cerebral ischemia. This is especiallyimportant when the patients of CBS present with pro-fuse bleeding and hypovolemic status.

3. Suitable for palliative care. For selected patients withadvanced head and neck cancers with CBS, endovascu-lar stent graft reconstruction is good for achieving im-

ents with carotid blowout syndrome

Hemostatic outcome

Time of rebleedingOutcome/timea

(cause of death)

None Died/10 mo (multiple metastasis,sepsis)

None Alive/37 moNone Alive/4 moNone Died/0.5 mo (radiation myelopathy,

sepsis)None Died/2 mo (recurrent tumor, sepsis)None Died/5 mo (brain metastasis, sepsis)

3 mo (2 mo: drop offthe balloon bydébridement )

Died/3 mo (disease progression,rebleeding)

None Died/18 mo (sepsis, diseaseprogression)

3 mo Died/3 mo (rebleeding)3 mo Died/3 mo (recurrent tumor

w/rebleeding)None Died/1 mo (disease progression,

sepsis)None Alive/14 moNone Alive/10 mo

Histoacryl, Braun, Germany).

Table V. Analysis of clinical severity of carotid blowoutsyndrome and endovascular outcomes

VariableAcute

(n �11)

ImpendingThreatened(n � 13) P

Angiographic grade, No. (%)0 and 1 0 (0) 8 (61.5) .0022 and 3 11 (100) 5 (38.5)

Technical outcome, No. (%)Initial complications 4 (36.3) 1 (7.7) .142Delayed complications 1 (9.1) 1 (7.7) �.99

Hemostatic outcomeRebleeding, No. (%) 7 (63.6) 1 (7.1) .008Hemostasis duration,

mean � SD mo 3.9 � 5.5 8.6 � 11.4 .231

pati

)

e

late (nts.

mediate and temporary hemostasis.11

JOURNAL OF VASCULAR SURGERYMay 2008944 Chang et al

The clinical severity of CBS was classified into threegroups: acute, impending and threatened.1,7 This simpleclinical classification correlated well with angiographic se-verity in our study. We favor making this clinical classifica-tion as a guide for management of CBS. Typically, patientswith acute CBS were diagnosed by clinical and angio-graphic findings; however, patients with threatened or im-pending CBS can present with subtle or no angiographicabnormalities (grades 0 and 1).

One of the causes of CBS in a CA without obviousangiographic abnormalities was that the angiogram was ob-tained in the earliest stage of CBS. The vulnerable CA wasintact but had been surrounded by diseased soft tissue such asrecurrent tumor or irradiation necrosis. Correlating otherimage modalities such as CT or magnetic resonance imagingof the head and neck region can help in achieving earlydiagnosis (Fig 1). Another cause is that the subtle pathologiclesions were not shown on routine biplanar angiograms. Wesuggest obtaining multiple view angiograms or CT angio-grams to aid in the evaluation of patients with CBS withoutobvious angiographic abnormalities (Fig 1).16,17

Cerebral ischemic insult is a well-known initial compli-cation of deconstructive management of CBS.1,18 Recon-structive management, however, also carries the risk ofthromboembolism and procedurally related complicationssuch as vascular dissection.11,13 These complications maybe caused by inadequate antithrombotic medication treat-ment of the patients or product characteristics of the de-vices. The development of a new design of self-expandablestent graft with a less thrombogenic surface, higher flexi-bility, and lower profile is indicated to improve technicalsafety of reconstructive endovascular management.

The mean duration of stent graft patency in this studywas 3.0 � 2.6 months. This unfavorable long-term patencyis a limitation of the reconstructive method as a permanentway to manage patients with head and neck cancers andCBS. The causes of poor long-term stent graft patencywere:

1. Appropriate antithrombotic medications are usually noteffective in cases of acute or advanced clinical status, andearly management for patients in a stable condition canimprove the outcome with adequate antithromboticregimens.

2. The thrombogenic character of stent grafts needs moreadequate antithrombotic medications. Our patientswith threatened CBS were given clopidogrel and aspirinonly for 1 day before intervention. If we could diagnosethe disease at its very early stage, it potentially might dobetter if the drugs were given for at least 3 days beforethe standard carotid angioplasty and stenting.

3. The deployment of stent grafts in a contaminated fieldin patients with head and neck cancers may result inpersistent infection and ultimately cause septic throm-bosis of the CA.19 We recommend prophylactic antibi-otics before and after the intervention.

4. Distal marginal stenosis was a common cause of recur-

rent vascular narrowing or occlusion after stent graft

deployment.20 It may be caused by vascular remodelingdue to the high radial force of the self-expandable stentgrafts.21,22 The smaller diameter of the CA distal to thestent graft may suffer from stronger pressure than itsproximal side and thus cause distal marginal stenosis(Fig 1). Because it showed rapid temporal change, closefollow-up and early management are needed to improvethe outcomes in patients with stents.

These technical improvements may help stent grafting tobe a good alternative method for patients at high risk forcarotid occlusion.

Both endovascular methods were good at achievingimmediate hemostasis. Although not statistically signifi-cant, deconstructive management provided better hemo-static results than reconstructive management (Table IV).Reconstructive management with stent grafts covered onlya segment of the affected CA. The pathologic field in thepatients with head and neck cancers can show dynamicchanges as a result of complex factors such as tumor recur-rence, wound infection, or radiation necrosis. This ongoingpathologic process may progress over the initially treated area(Fig 1). We suggest assessing the extent of the pathologiclesion on CT and the field of previous irradiation before stentgraft placement is planned. A long, self-expandable stent graftcan fully cover the pathologic field, especially given thecontinuous shortening of the self-expanding stent graft as itdilates progressively.

This ongoing pathologic process with reconstitution ofcollateral vessels or recanalization of the thrombosed CAsmay also explain the rebleeding in patients in the decon-structive group who underwent proximal occlusion.23 Wesuggest performing deconstructive endovascular therapywith cross occlusion for these cancer patients with CBS toenhance durable hemostasis if they have no risk of perma-nent carotid occlusion (Fig 2). Cross occlusion is favored asa permanent deconstructive method to treat CBS becauseof its low rebleeding rate. Reconstructive endovasculartherapy with a stent graft is reserved for patients who arenot suitable for the deconstructive method.

For all patients, clinical severity is the significant factoraffecting the hemostatic outcome of endovascular manage-ment (Table V). Rebleeding occurred more commonly inpatients with acute CBS than in those in the impending andthreatened group. Poor hemostatic results in patients withacute status included patients with acute CBS who also hada more extensive and complete CA injury or soft tissueinjury, or both, than those with impending and threatenedCBS and the critical clinical status, and thus poor cooper-ation of these patients could cause technical difficulty suchas the precise positioning of the stent graft deployment, asin patient 2 in the reconstructive group; in addition, pa-tients with acute CBS have complications that may be dueto inadequate antithrombotic medication or massive trans-fusion. We suggest making an early diagnostic and treat-ment plan, such as CT or angiography with an occlusion

test, for patients with head and neck cancers if signs sug-

JOURNAL OF VASCULAR SURGERYVolume 47, Number 5 Chang et al 945

gestive of CBS are present. Early intervention for patients instable clinical condition may also improve the outcomes.

A limitation of this study was the small number ofpatients studied, many of whom had a short survival time,which hindered long-term follow-up. Diverse diseasestages and previous treatment of our patients also madestatistical analysis difficult. Comparing the two techniquesis also difficult because patients who received stent graftsare often those who cannot tolerate carotid occlusion or inwhom test occlusion is precluded by their clinical status.

A lack of experience with antithrombotic medications andprophylactic antibiotics might also have affected outcomes ofpatients in the reconstructive group. Further research withimproved prophylactic medications and associated other im-age modalities such as CT or CT angiography for early diag-nosis is invaluable to improve the outcomes.

CONCLUSION

We found no significant differences in the technical andhemostatic outcomes of reconstructive and deconstructiveendovascular management. Clinical severity is a significantfactor affecting hemostatic outcome of endovascular man-agement: patients with acute CBS were associated with ahigher rebleeding rate than those with impending andthreatened CBS. We suggest correlation of clinical findingsand other image modalities such as CT to help in earlydiagnosis of CBS if angiographic abnormalities are subtle.We also suggest early endovascular management for pa-tients with CBS. Deconstructive endovascular manage-ment with cross occlusion can be a treatment for durablehemostasis.

AUTHOR CONTRIBUTIONS

Conception and design: FCAnalysis and interpretation: CL, HW, WG, MTData collection: JL, HW, MTWriting the article: FCCritical revision of the article: FCFinal approval of the article: FC, CCStatistical analysis: SWObtained funding: Not applicableOverall responsibility: FC

REFERENCES

1. Chaloupka JC, Putman CM, Citardi MJ, Ross DA, Sasaki CT. Endo-vascular therapy for the carotid blowout syndrome in head and necksurgical patients: diagnostic and managerial considerations. AJNR Am JNeuroradiol 1996;17:843-52.

2. Stuart J. Wong, Mitchell Machtay, Yi Li. Locally recurrent, previouslyirradiated head and neck cancer: concurrent re-irradiation and chemo-therapy, or chemotherapy alone? J Clin Oncol 2006;24:2653-8.

3. Maran AGD, Amin M, Wilson JA. Radical neck dissection: a 19-yearexperience. J Laryngol Otol 1989;103:395-400.

4. Macdonald S, Gan J, Mckay AJ, Edward RD. Endovascular treatment ofacute carotid blowout syndrome. J Vasc Interv Radiol 2000;11:1184-8.

5. Warren FM, Cohen JI, Nesbit GM, Barnwell SL, Wax MK, AndersenPE. Management of carotid “blowout” with endovascular stent grafts.

Laryngoscope 2002;112:428-33.

6. Chaloupka JC, Roth TC, Putman CM, Mitra S, Ross DA, Lowlicht RA,et al. Recurrent carotid blowout syndrome: Diagnosis and therapeuticchallenges in a newly recongnized subgroup of patients. AJNR Am JNeuroradiol 1999;20:1069-77.

7. Citardi MJ, Chaloupak JC, Son YH, Ariyan S, Sasaki CT. Managementof carotid artery rupture by monitored endovascular therapeutic occlu-sion (1988-1994). Laryngoscope 1995;105:1086-92.

8. Lesley WS, Chaloupka JC, Weigele JB, Mangla S, Dogar MA. Prelimi-nary experience with endovascular reconstruction for the managementof carotid blowout syndrome. AJNR Am J Neuroradiol 2003;24:975-81.

9. Chazono H, Okamoto Y, Matsuzaki Z, Horiguchi S, Matsuoka T,Horikoshi T, et al. Carotid artery resection: preoperative temporaryocclusion is not always an accurate predictor of collateral blood flow.Acta Otolaryngol 2005;125:196-200.

10. Desuter G, Hammer F, Gardiner Q, Grégoire V, Machiels JP, HamoirM, et al. Carotid stenting for impending carotid blowout: suitablesupportive care for head and neck cancer patients? Palliative Medicine2005;19:427-9.

11. Chang FC, Lirng JF, Luo CB, Guo WY, Teng MM, Tai SK, et al.Carotid blowout syndrome in patients with head-and-neck cancers:reconstructive management by self-expandable stent-grafts. AJNR Am JNueroradiol 2007;28:181-8.

12. Simental A, Hohnson JT, Horowitz M. Delayed complications ofendovascular stenting for carotid blowout. Am J Otolaryngol 2003;24:417-9.

13. Smith TP, Alexander MJ, Enterline DS. Delayed stenosis followingplacement of polyethylene terephthalate endograft in the cervical ca-rotid artery. J Neurosurg 2003;98:421-5.

14. Castañer E, Andreu M, Gallardo X, Mata HM, Cabezuelo MA, et al. CTin nontraumatic acute thoracic aortic disease: Typical and atypicalfeatures and complcations. Radiographics 2003;23 Spec No:S93-110.

15. Wright JG, Nicholson R, Schuller DE, Smead WL. Resection of theinternal carotid artery and replacement with greater saphenous vein: asafe procedure for en bloc cancer resections with carotid involvement.J Vasc Surg 1996;23:775-82.

16. Silvennoinen HM, Ikonen S, Soinne L, Railo M, Valanne L. CTangiographic analysis of carotid artery stenosis: comparison of manualassessment, semiautomatic vessel analysis, and digital subtraction an-giography. AJNR AM J Neuroradiol 2007;28:97-103.

17. Bell RB, Osborn T, Dierks EJ, Potter BE, Long WB. Management ofpenetrating neck injury: a new paradigm for civilian trauma. J OralMaxillofac Surg 2007;65:591-705.

18. Luo CB, Chang FC, Teng MMH, Chen CCC, Lirng JF, Chang CY.Endovascular treatment of the carotid artery rupture with massivehemorrhage. J Chin Med Assoc 2003;66:140-7.

19. Chang FC, Lirng JF, Tai SK, Luo CB, Teng MMH, Chang CY. Brainabscess formation: a delayed complication of carotid blowout syndrometreated by self-expandable stent-graft. AJNR Am J Neuroradiol 2006;27:1543-5.

20. Gercken U, Lansky AJ, Bullesfeld L, Desai K, Badereldin M, Mueller R,et al. Results of the Jostent coronary stent graft implantation in variousclinical settings: procedural and follow-up results. Cathet CardiovascIntervent 2002;56:353-60.

21. Tanaka N, Martin J-B, Tokunaga K, Abe T, Uchivama Y, Hayabuchi N,et al. Conformity of carotid stents with vascular anatomy: evaluation incarotid models. AJNR Am J Neuroradiol 2004;25:604-7.

22. Berkefeld J, Turowski B, Dietz A, Lanfermann H, Sitzer M, Schmitz-Rixen T, et al. Recanalization results after carotid stent placement.AJNR Am J Neuroradiol 2002;23:113-20.

23. Numagami Y, Ezura M, Takahashi A, Yoshimoto T. Antegrade recan-alization of completely embolized internal carotid artery after treatmentof a giant intracavernous aneurysm: a case report. Surg Neurol 1999;52:611-6.

Submitted Sep 14, 2007; accepted Dec 11, 2007.