Flow Diversion Versus Conventional Treatment for Carotid

Cavernous Aneurysms
Mario Zanaty, MD; Nohra Chalouhi, MD; Robert M. Starke, MD; Guilherme Barros, BS;
Mark Philip Saigh, BA; Eric Winthrop Schwartz, BS; Norman Ajiboye, MD;
Stavropoula I. Tjoumakaris, MD; David Hasan, MD; Robert H. Rosenwasser, MD; Pascal Jabbour, MD

Background and Purpose—Several endovascular treatment options are available for cavernous carotid aneurysms. We
compared pipeline embolization device (PED) versus conventional endovascular treatment in terms of evolution of mass
effect, complications, recurrence, and retreatment rate.
Methods—One hundred fifty-seven patients harboring 167 cavernous carotid aneurysms were treated using PED placement,
coiling, stent-assisted coiling, and carotid vessel destruction. Procedural complications, angiographic results, and clinical
outcomes were analyzed and compared.
Results—There were no difference in age, sex, and mean aneurysm size between those treated with PED and those treated
with conventional endovascular procedures. The patients treated with PED had a significantly lower proportion of small-
size aneurysms (<10 mm) and a shorter follow-up duration. Multivariate analysis revealed treatment other than PED
(PED: odds ratio [OR], 0.03; P=0.002) and size >15 mm (OR, 4.27; P=0.003) to be predictors of no improvement in
symptoms. The rate of complete occlusion was 81.36% (48 of 59) for PED, 42.25% (39 of 71) for stent-assisted coiling,
27.27% (6 of 22) for coiling, and 73.33% (11 of 15) for carotid vessel destruction. Retreatment was needed in patients
with aneurysm size >15 mm (OR, 2.67; P=0.037) and those who were not treated with PED (PED: OR, 0.16; P=0.006).
The rate of major complications was 6.6% (11 of 167). Patients who were treated with PED or stent-assisted coiling had
3.84 lower odds to develop complications (OR, 0.26; P<0.05).
Conclusions—The use of PED should be encouraged, especially in symptomatic patients. We found PED to be
associated with less need for future treatment, higher improvement in symptoms rate, and lower rate of complications.  
(Stroke. 2014;45:2656-2661.)
Key Words: cerebral aneurysm ◼ complication intraoperative ◼ complication peroperative ◼ complication
postoperative ◼ endovascular procedure ◼ endovascular technique ◼ intracranial aneurysm

B ecause of the latest technology advances, there are several

endovascular treatment options available for cavernous
carotid aneurysms (CCA).1–5 These strategies include balloon-
Patient Cohort
Materials and Methods

After obtaining the institutional review board approval from our

assisted coiling, stent-assisted coiling (SAC), carotid vessel institution, we searched our prospectively maintained database for
destruction (CVD), and flow diversion, each varying in degrees all patients with CCA undergoing endovascular treatment between
of success. Recent studies have demonstrated the effectiveness 2005 and 2014. A total of 157 patients with 167 CCA were identi-
and safety in treating patients with large, wide-neck CCAs with fied. Medical charts, angiographic studies, MRI, and computed tomo-
graphic scans were carefully reviewed. Patient’s age and sex, as well
flow diversion techniques.6–8 There is increasing evidence that
as aneurysm size and location were recorded. Treatment was dictated
when treated with flow diversion such as the pipeline emboliza- by the dual trained attending neurosurgeons. Asymptomatic patients
tion device (PED), these aneurysms have higher rates of com- were considered for treatment if there was a significant growth of
plete occlusion, with lower rates of recurrence and retreatment the aneurysm. Any aneurysm that displayed a decreasing percentage
with less mass effect on the surrounding structures, as opposed of occlusion (>5%) on follow-up angiography was considered recur-
to traditional endovascular methods.6,9–11 In our study, we com- rent. Thromboembolic and ischemic complications were diagnosed
clinically (new deficits or change in level of consciousness) or on
pared each of these treatment modalities, PED, SAC, coiling, computed tomographic scans or MRI (new infarcts) after exclud-
and CVD, in terms of morbidity, mortality, evolution of mass ing confounders such as vasospasm, hydrocephalus, and metabolic
symptoms, aneurysm occlusion, and rate for retreatment. disorders.

Received May 27, 2014; final revision received May 27, 2014; accepted June 25, 2014.
From the Department of Neurosurgery, Thomas Jefferson University and Jefferson Hospital for Neuroscience, Philadelphia, PA (M.Z., N.C., G.B.,
M.P.S., E.W.S., N.A., S.I.T., R.H.R., P.J.); Department of Neurosurgery, University of Virginia, Charlottesville (R.M.S.); and Department of Neurosurgery,
Carver College of Medicine, University of Iowa, Iowa City (D.H.).
Correspondence to Pascal Jabbour, MD, Division of Neurovascular Surgery and Endovascular Neurosurgery, Department of Neurological Surgery,
Thomas Jefferson University Hospital, Third Floor, 901 Walnut St, Philadelphia, PA 19107. E-mail [email protected]
© 2014 American Heart Association, Inc.
Stroke is available at http://stroke.ahajournals.org DOI: 10.1161/STROKEAHA.114.006247

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 Zanaty et al   PED for CCA    2657

Patient Outcome characteristics stratification according to treatments received

The primary clinical outcome was the evolution of cranial nerve is demonstrated in Table 1. There were no differences in
deficits produced by mass effect, which was classified as complete symptoms at presentation between the patients treated with
disappearance of symptoms, partial improvement in symptoms, no PED and those treated with other modalities. The follow-up
change in symptoms, and worsening of symptoms. Patients were
initially evaluated before the treatment and at every follow-up. The duration was 14.49±12.27 months.
final clinical status was assessed at the latest follow-up. The regis-
tered complications were symptomatic ischemic stroke, symptomatic Mass Effect Evolution
hemorrhagic stroke, aneurysm rupture, and vessel perforation. Of the 51 symptomatic patients treated with flow diversion,
Angiographic follow-up (digital subtraction angiography or MR
angiography) was scheduled at 6 months, 1 year, 2 years, 5 years, and 70.59% (36 of 51) became completely asymptomatic, 21.57%
>5 years after endovascular procedures. Patient clinical status was (11 of 51) improved, and 7.84% (4 of 51) remained the same
also subsequently assessed on the latest follow-up visit. Complete oc- (Table 2). Overall, the rate of improvement for patients treated
clusion was defined as >95%, near complete occlusion as >90% but with PED was 92.16% (47 of 51). For patients treated with
<95%, and incomplete occlusion if <90%. Patients without routine SAC, 50.84% (30 of 59) improved, 11.86% (5 of 59) wors-
follow-up were contacted for assessment via a structured telephone
interview, and medical records were obtained from outside hospital fa- ened, and 40.67% (42 of 59) remained the same. Of the 22
cilities. We evaluated the complication rates, the need for retreatment symptomatic patients treated with endovascular coiling, 9 (of
(because of recurrence of the aneurysm or worsening symptoms), the 18; 50.00%) improved, 2 (of 18; 11.11%) worsened, and 7 (of
aneurysm occlusion rates, and the evolution of cranial nerve deficits. 22; 38.89%) remained the same. Finally, 11 of 14 (78.57%)
patients had improvement in their symptoms; the remain-
Statistical Analysis ing 3 did not show any change in their symptoms (3 of 14;
Data are presented as mean and range for continuous variables, and as 21.43%). In multivariate analysis, the predictors of worsening
frequency for categorical variables. Patients treated with CVD, endo- mass effect were the use of other than PED or CVD (PED:
vascular coiling, SAC, and flow diversion were compared. Statistical
analyses of categorical variables was performed using the χ2 and P<0.05 and CVD P<0.05; both were perfect predictors) and
Fisher exact tests; comparison of means was performed using Student size >25 mm (odds ratio [OR], 8.96; P=0.046). Univariate
t test, and ANOVA followed by Bonferroni post hoc testing was per- predictors included in multivariate analysis were treatment
formed as appropriate. Univariate analysis was used to test covariates modality, aneurysm size, and follow-up duration after treat-
predictive of the following dependent post-treatment variables: treat- ment. Multivariate analysis revealed treatment other than
ment-related complications, aneurysm occlusion at latest follow-up,
the need for retreatment, improvement of cranial nerve deficits, and PED (PED: OR, 0.03; P=0.002) and size >15 mm (OR, 4.27;
favorable clinical outcome (modified Rankin Scale score 0–1 with- P=0.003) to be predictors of no improvement in symptoms.
out worsening signs or symptoms). Factors predictive in univariate People treated with PED had 33.33× higher odds to improve.
analysis (P<0.20) were entered into a multivariate logistic regression We identified 25 patients with incidental CCA, 2 of whom
analysis. P values <0.05 were considered statistically significant.
developed ocular symptoms after treatment with SAC.
Results
Rate of Retreatment
Patients Characteristics Twenty-seven aneurysms had >1 treatment because of recana-
Of 157 patients with CCA, the mean age was 61.4±12.7 lization, failure of occlusion, or worsening of symptoms. Of
years and 147 were women (93.6%). Mean aneurysm size 27, 3 were previously treated with PED, 8 with coils, 14 with
was 15.1±9.0 mm. CCA were treated with endovascular coil- SAC, and 2 with CVD. The need for retreatment for each
ing (22 of 167; 13.2%), CVD after balloon occlusion test intervention is given in Table 2. The only significant predic-
(15 of 167; 9.0%), SAC (71 of 167; 42.5%), and PED (59 tors on univariate and multivariate analysis were size >15 mm
of 167; 35.3%). There were no differences in mean age and (OR, 2.67; P=0.037) and treatment other than PED (PED:
proportion of giant aneurysms (>25 mm) between the differ- OR, 0.16; P=0.006). CVD was also found to decrease the
ent treatment groups. The patients treated with PED had a risk of recurrence when compared with treatment other than
significantly lower proportion of small-size aneurysms (<10 PED (OR, 0.16; P=0.001). The rate of complete occlusion
mm). The mean follow-up time of patients treated with PED was 81.36% (48 of 59) for PED, 42.25% (39 of 71) for SAC,
was significantly lower than those treated with other modali- 27.27% (6 of 22) for coiling, and 73.33% (11 of 15) for CVD
ties (Table 1). Comparison of overall patients and aneurysm (Table 2). The rate of complete and near-complete occlusion

Table 2. Comparison of Different Types of Treatments

Table 1. Comparison of Patients’ Characteristics Between
PED and Other Modalities Complete and
Near-Complete
Other Significance Treatment Improvement in Complication Retreatment Occlusion Rate
PED Treatments (P Value) Modality Symptoms Rate Rate (>90%)
Age, mean, y 63.00 60.42 0.19 PED 92.16% (47/51) 3.39% (2/59) 5.08% (3/59) 89.83% (53/59)
Female proportion 93.22% 93.62% 0.405 SAC 50.84% (30/59) 5.63% (4/71) 19.71% (14/71) 84.51% (60/71)
Size, mean, mm 16.75 14.27 0.12 Coiling 50.00% (9/18) 13.64% (3/22) 36.36% (8/22) 54.54% (12/22)
Angiographic follow-up, mean, mo 7.31 18.24 <0.01 CVD 78.57% (11/14) 13.33% (2/15) 13.33% (2/15) 86.67% (13/15)
Symptoms at presentation 86.44% 84.26% 0.769 CVD indicates carotid vessel destruction; PED, pipeline embolization device;
PED indicates pipeline embolization device. and SAC, stent-assisted coiling.

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2658  Stroke  September 2014

combined was 89.83% (53 of 59) for PED, 84.51% (60 of 71) or fistulization is low,12,13 except for cases with giant aneu-
for SAC, 54.54% for coiling, and 86.67% (13 of 15) for CVD. rysms.14 Conventional endovascular techniques have been pre-
ferred for the treatment of symptomatic CCA. The reported
Treatment-Related Complications recurrence rate and incomplete angiographic occlusion after
The rate of major complications was 6.6% (11 of 167). Major treatment with conventional endovascular technique remains
complications are defined as symptomatic ischemic stroke, high,15,16 discouraging their use in complex aneurysms.
hemorrhagic stroke, aneurysm rupture, and vessel perforation Recently, flow diversion has been emerging as a novel treat-
that lead to neurological damage. We had 2 (of 167; 0.03%) ment, but with not enough data to establish its superiority over
post-treatment aneurysm ruptures, 1 occurred after PED place- conventional modalities. Still, many institutions are starting to
ment and 1 after SAC. Hemorrhagic stroke developed in 2 cases consider flow diversion as first-line treatment for CCA.
(of 167; 0.03%), 1 after SAC and 1 after treatment with PED.
Ischemic stroke occurred in 2 patients with SAC, 2 patients with Angiography and Clinical Outcome
CVD, and 1 patient treated with endovascular coiling, adding Traditional methods for treatment of CCA such as carotid
up to 5 cases in total (5 of 167; 2.99%). There were no proce- sacrifice with or without bypass have been effective, but sub-
dural related deaths and only 2 (of 167; 0.03%) intraoperative optimally. Carotid sacrifice achieves a 93% (95% confidence
ruptures, both of which occurred in patients treated with coils. interval [CI], 86.0–97.0) complete aneurysm occlusion and
The complication rate for each treatment modality is included in 83.0% (95% CI, 52.0–96.0) resolution of mass effect, but is
Table 2. Univariate predictors included in multivariate analysis associated with a 4.0% (95% CI, 1.0–9.0) risk of procedure-
were treatment modality, age, and aneurysm size. In multivariate related neurological deficits.1 However, because these aneu-
analysis, the only factor predictive of major complications was rysms are often very large or giant with a wide neck, standard
the use of other than PED or SAC. Patients who have been treated endovascular coiling achieved a complete aneurysm occlusion
with PED or SAC had 3.84 lower odds to develop complications rate of only 67.0% (95% CI, 55.0–77.0) in a meta-analysis
(OR, 0.26; P<0.05). This was unchanged after controlling for from 2014.1 Furthermore, the coiling group demonstrated a
duration of follow-up and patient/aneurysm characteristics. We retreatment rate of 18.0% (95% CI, 12.0–26.0) compared with
presented 2 illustrative cases (Figures 1 and 2). 6.0% (95% CI, 2.0–12.0) for CVD without bypass (P=0.01).
However, there were no differences in the improvement of
mass effect between coiling, SAC, and CVD. On the contrary,
Discussion
van Rooij17,18 found no significant difference in overall occlu-
Flow Diversion in CCA sion rates between CCA treated with coil embolization versus
CCA are associated with mass effect on adjacent cranial CVD. Therefore, the superiority of CVD over coiling in terms
nerves, whereas their risk of rupture subarachnoid hemorrhage of symptom improvement has not been established, but CVD

Figure 1. A, A 52-year-old patient presented with headache. He was found to have a right-sided carotid cavernous aneurysm measuring
20×10×22 mm, which was treated with coils. B, 12-month follow-up digital subtraction angiography (DSA) showing an incomplete occlu-
sion of the aneurysm. The patient was treated again with coil embolization. C, 12-month follow-up DSA after the second treatment show-
ing an incomplete occlusion.

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 Zanaty et al   PED for CCA    2659

Figure 2. A and B, A 68-year-old man with a large right-sided cavernous aneurysm measuring 20×15mm. The patient was treated with
pipeline embolization device (PED) placement. C and D, 6-month follow-up digital subtraction angiography after PED placement shows
100% occlusion of the aneurysm and resolution of the cranial nerve deficit.

is still preferred given the higher occlusion rate demonstrated upwards of 90% of patients.4 Starke et al2 treated 3 CCA with
by meta-analysis and systemic reviews of nonrandomized PED after incomplete occlusion with coiling, with a 100%
controlled trials. success rate. Our study supports these findings, because PED
The experience with flow diversion has somewhat been dif- was associated with a significantly lower retreatment rates and
ferent. Lanzino et al5 have conducted a retrospective matched- a significantly higher rate of improvement in symptoms when
pair comparison of paraclinoid aneurysms treated with PED compared with conventional treatments.
versus conventional endovascular techniques. The aneurysm Flow diverters seem to be more effective than the conven-
and patient characteristics were not different between the 2 tional techniques because they completely seal the aneurysm
groups. The second most common type of paraclinoid aneu- neck, diverting flow away from the aneurysm and leading to
rysm was the CCA (18 in total). The authors report a signifi- its thrombosis and shrinkage19–22 while simultaneously provid-
cantly higher rate of complete occlusion in patients treated ing a support for the diseased vessel allowing its reconstruc-
with PED (76.2%) versus the control group (21.4%) on tion.23,24 The re-establishment of the homeostasis seems to be
follow-up.5 However, the small sample of CCA in the study responsible for the favorable angiographic occlusion and evo-
imposes a major limitation. Puffer et al3 reported a complete lution of symptoms. The resolution of mass effect might be
occlusion rate of 71% (25 of 35) for CCA treated by PED because of the decreased pulsation in the aneurysm along with
embolization. Improvement of symptoms was noted in 90% a decrease in its size when successfully excluded out of the
patients (26 of 29). Of the remaining patients with incomplete aneurysm, as demonstrated by Szikora et al.25
occlusion, 50% (4 of 8) were found to have progressed to
complete occlusion at final follow-up.3 Hence, we included Complication Rates
and accounted for follow-up duration in the multivariate The safety and efficacy of PED placement have to be com-
analysis in our study. The Canadian trial reported complete pared with that of conventional endovascular therapy. Major
occlusion rates of 70% to 100% and symptom improvement in concerns after flow diversion are delayed aneurysm rupture,

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2660  Stroke  September 2014

distal hemorrhage, and major ipsilateral stroke.26 In patients symptomatic CCA. Finally, complete occlusion seems to be
with intracranial aneurysms, the procedure-related morbidity higher with pipeline placement; this along with vessel recon-
and mortality are 5% and 4%, respectively; the rate of intra- struction and aneurysm shrinkage confers PED a potential
parenchymal hemorrhage is 3% and that of stroke is 6%, as advantage over other modalities when treating giant CCA in
reported by Brinjikji et al27 in their meta-analysis. Puffer et al3 hope of avoiding subarachnoid hemorrhage.
treated 44 CCA using PED. They encountered in 36% (16 of
44) of procedures minor technical complications (minor vaso- Limitations
spasm, incomplete opening, vessel perforation). No patient The limitations of the present study include retrospective
who experienced intraprocedural or delayed complications design and possible selection bias. Patients in our cohort
had any clinical sequelae. Although Briganti et al28 reported were treated at a tertiary referral hospital by dual trained
a 4% mortality rate (3 of 76) for treatment of CCA with flow neurosurgeons leading to a potential ascertainment bias,
diverters, the mortality rate in a multitude of studies,2–5 includ- limiting the external validity of the results. The lack of an
ing ours, is 0%. The Canadian study4 reported a 0% overall untreated control group limits assessment of intervention
morbimortality in 70 CCA. In a meta-analysis of 316 patients strategies. Nevertheless, our study is the only one compar-
with CCA performed in 2002, procedure-related neurologi- ing results of flow diversion, including mass effect evolution,
cal deficits occurred in 5% of patients treated with CVD and head to head with other conventional endovascular studies in
0% of patients treated with coils alone.29 More recently, in a patients harboring CCA. It is also the cohort with the largest
series of 113 patients treated either by coiling or SAC, the rate sample of CCA.
of neurological complications was 3.5%.30 Recently, Turfe
et al1 performed a meta-analysis to determine the complica- Conclusions
tions associated with endovascular coiling and CVD for CCA. In the absence of randomized controlled trials, hard evidence
The perioperative morbidity rate for endovascular coiling was guidelines are lacking. Randomized controlled trials have to
3.0%, significantly lower than that of CVD (7.0%). There was overcome many obstacles, including an adequate sample size
no difference in the mortality rate between the 2 groups, which for analysis, given the low prevalence of CCA in the popula-
was 0% for the coiling cohort and 4% for the CVD. Therefore, tion. With the present findings in literature and with the results
it is safe to assume, based on the literature, that coiling is safer found in this study, the use of flow diversion should be encour-
than CVD in the treatment of CCA. On the contrary, the litera- aged, especially in symptomatic patients. We found PED to be
ture does not allow such conclusion on PED versus coiling in associated with higher obliteration rate, less need for future
terms of morbidity and mortality, because direct comparison treatment, higher improvement rates in mass symptoms, and
has not been made. Our study, however, compared PED head lower complications when compared with traditional endovas-
to head with coiling and SAC and demonstrated that PED cular treatments.
placement is associated with lower complication rates com-
pared with coiling and CVD. Disclosures
Dr Jabbour is a consultant at Covidien. Dr Tjoumakaris is a consul-
Risk–Benefit Analysis tant at Covidien and Stryker. The other authors report no conflicts.
A risk–benefit analysis should be assessed before deciding
on whether or not to treat patients with CCA, and what type References
of treatment is most adequate. The analysis should factor in 1. Turfe ZA, Brinjikji W, Murad MH, Lanzino G, Cloft HJ, Kallmes DF.
Endovascular coiling versus parent artery occlusion for treatment of cav-
the patient’s age, interventionalist experience, aneurysm size, ernous carotid aneurysms: a meta-analysis [published online ahead of
morbimortality rate, occlusion rate, and presence or absence print March 21, 2014]. J Neurointerv Surg. http://jnis.bmj.com/content/
of symptoms. CVD is an effective treatment with high occlu- early/2014/03/21/neurintsurg-2014–011102.long?eaf. Accessed April
sion rates, but limited by the risk of complications, risk of 20, 2014.
2. Starke RM, Chalouhi N, Ali MS, Tjoumakaris SI, Jabbour PM, Fernando
aneurysm formation along the collateral pathways, and pres- Gonzalez L, et al. Endovascular treatment of carotid cavernous aneu-
ence of contralateral mirror aneurysms.5,31–34 These limita- rysms: complications, outcomes and comparison of interventional strate-
tions make flow diversion, a reconstructive technique, more gies. J Clin Neurosci. 2014;21:40–46.
3. Puffer RC, Piano M, Lanzino G, Valvassori L, Kallmes DF, Quilici L, et
appealing. Even more, CCA have a sidewall morphology al. Treatment of cavernous sinus aneurysms with flow diversion: results
and lack perforating side branches, which make them well in 44 patients. AJNR Am J Neuroradiol. 2014;35:948–951.
suited for PED placement.3,5 However, many authors still 4. O’Kelly CJ, Spears J, Chow M, Wong J, Boulton M, Weill A, et
prefer CVD in elderly patients with excessive tortuous ves- al. Canadian experience with the pipeline embolization device for
repair of unruptured intracranial aneurysms. AJNR Am J Neuroradiol.
sels or where traversing the aneurysm is thought to be chal- 2013;34:381–387.
lenging.3 The results of our study strongly suggest the use 5. Lanzino G, Crobeddu E, Cloft HJ, Hanel R, Kallmes DF. Efficacy and
of flow diversion, which might help avoid the higher rate safety of flow diversion for paraclinoid aneurysms: a matched-pair
analysis compared with standard endovascular approaches. AJNR Am J
of complications that we are currently having with conven- Neuroradiol. 2012;33:2158–2161.
tional treatments and to dodge the need for retreatment in the 6. Chalouhi N, Tjoumakaris S, Starke RM, Gonzalez LF, Randazzo C,
future. Additionally, the findings in this study demonstrate Hasan D, et al. Comparison of flow diversion and coiling in large unrup-
tured intracranial saccular aneurysms. Stroke. 2013;44:2150–2154.
that patients treated with PED had the highest likelihood
7. Zanaty M, Chalouhi N, Tjoumakaris SI, Rosenwasser RH, Gonzalez
of improvement in symptoms and mass effect. We encour- LF, Jabbour P. Flow-diversion panacea or poison? Front Neurol.
age the use of flow diversion in patients who present with 2014;5:21.

Downloaded from http://stroke.ahajournals.org/ at Rutgers University Libraries on April 4, 2015

 Zanaty et al   PED for CCA    2661

8. Leung GK, Tsang AC, Lui WM. Pipeline embolization device for intracra- 21. Kim YH, Xu X, Lee JS. The effect of stent porosity and strut shape on
nial aneurysm: a systematic review. Clin Neuroradiol. 2012;22:295–303. saccular aneurysm and its numerical analysis with lattice Boltzmann
9. Chitale R, Gonzalez LF, Randazzo C, Dumont AS, Tjoumakaris S, method. Ann Biomed Eng. 2010;38:2274–2292.
Rosenwasser R, et al. Single center experience with pipeline stent: fea- 22. Sadasivan C, Cesar L, Seong J, Wakhloo AK, Lieber BB. Treatment of
sibility, technique, and complications. Neurosurgery. 2012;71:679–691, rabbit elastase-induced aneurysm models by flow diverters: development
discussion 691. of quantifiable indexes of device performance using digital subtraction
10. Shapiro M, Babb J, Becske T, Nelson PK. Safety and efficacy of adjunctive angiography. IEEE Trans Med Imaging. 2009;28:1117–1125.
balloon remodeling during endovascular treatment of intracranial aneu- 23. Kallmes DF, Ding YH, Dai D, Kadirvel R, Lewis DA, Cloft HJ. A new
rysms: a literature review. AJNR Am J Neuroradiol. 2008;29:1777–1781. endoluminal, flow-disrupting device for treatment of saccular aneu-
11. Bodily KD, Cloft HJ, Lanzino G, Fiorella DJ, White PM, Kallmes DF. rysms. Stroke. 2007;38:2346–2352.
Stent-assisted coiling in acutely ruptured intracranial aneurysms: a 24. Kallmes DF, Ding YH, Dai D, Kadirvel R, Lewis DA, Cloft HJ. A sec-
qualitative, systematic review of the literature. AJNR Am J Neuroradiol. ond-generation, endoluminal, flow-disrupting device for treatment of
2011;32:1232–1236. saccular aneurysms. AJNR Am J Neuroradiol. 2009;30:1153–1158.
12. Kupersmith MJ, Hurst R, Berenstein A, Choi IS, Jafar J, Ransohoff J. 25. Szikora I, Marosfoi M, Salomváry B, Berentei Z, Gubucz I. Resolution
The benign course of cavernous carotid artery aneurysms. J Neurosurg. of mass effect and compression symptoms following endoluminal
1992;77:690–693. flow diversion for the treatment of intracranial aneurysms. AJNR Am J
13. Kupersmith MJ, Stiebel-Kalish H, Huna-Baron R, Setton A, Niimi Y, Neuroradiol. 2013;34:935–939.
Langer D, et al. Cavernous carotid aneurysms rarely cause subarachnoid 26. Nelson PK, Lylyk P, Szikora I, Wetzel SG, Wanke I, Fiorella D. The
hemorrhage or major neurologic morbidity. J Stroke Cerebrovasc Dis. pipeline embolization device for the intracranial treatment of aneurysms
2002;11:9–14. trial. AJNR Am J Neuroradiol. 2011;32:34–40.
14. Wiebers DO, Whisnant JP, Huston J III, Meissner I, Brown RD Jr, 27. Brinjikji W, Murad MH, Lanzino G, Cloft HJ, Kallmes DF. Endovascular
Piepgras DG, et al; International Study of Unruptured Intracranial treatment of intracranial aneurysms with flow diverters: a meta-analysis.
Aneurysms Investigators. Unruptured intracranial aneurysms: natural Stroke. 2013;44:442–447.
history, clinical outcome, and risks of surgical and endovascular treat- 28. Briganti F, Napoli M, Tortora F, Solari D, Bergui M, Boccardi E, et al.
ment. Lancet. 2003;362:103–110. Italian multicenter experience with flow-diverter devices for intracranial
15. Crobeddu E, Lanzino G, Kallmes DF, Cloft HJ. Review of 2 decades of unruptured aneurysm treatment with periprocedural complications–a ret-
aneurysm-recurrence literature, part 1: reducing recurrence after endo- rospective data analysis. Neuroradiology. 2012;54:1145–1152.
vascular coiling. AJNR Am J Neuroradiol. 2013;34:266–270. 29. van der Schaaf IC, Brilstra EH, Buskens E, Rinkel GJ. Endovascular
16. Crobeddu E, Lanzino G, Kallmes DF, Cloft HJ. Review of 2 decades of treatment of aneurysms in the cavernous sinus: a systematic review
aneurysm-recurrence literature, part 2: Managing recurrence after endo- on balloon occlusion of the parent vessel and embolization with coils.
vascular coiling. AJNR Am J Neuroradiol. 2013;34:481–485. Stroke. 2002;33:313–318.
17. van Rooij WJ. Endovascular treatment of cavernous sinus aneurysms. 30. Choulakian A, Drazin D, Alexander MJ. Endosaccular treatment of 113
AJNR Am J Neuroradiol. 2012;33:323–326. cavernous carotid artery aneurysms. J Neurointerv Surg. 2010;2:359–362.
18. van Rooij WJ, Sluzewski M. Unruptured large and giant carotid artery 31. Brisman JL, Song JK, Newell DW. Cerebral aneurysms. N Engl J Med.
aneurysms presenting with cranial nerve palsy: comparison of clinical 2006;355:928–939.
recovery after selective aneurysm coiling and therapeutic carotid artery 32. Tomsick T. Long-term clinical follow-up of therapeutic internal carotid
occlusion. AJNR Am J Neuroradiol. 2008;29:997–1002. artery occlusion. AJNR Am J Neuroradiol. 2007;28:1626.
19. Aenis M, Stancampiano AP, Wakhloo AK, Lieber BB. Modeling of 33. Klemme WM. Hemorrhage from a previously undemonstrated intra-
flow in a straight stented and nonstented side wall aneurysm model. J cranial aneurysm as a late complication of carotid artery ligation. Case
Biomech Eng. 1997;119:206–212. report. J Neurosurg. 1977;46:654–658.
20. Kim M, Taulbee DB, Tremmel M, Meng H. Comparison of two stents 34. Niiro M, Shimozuru T, Nakamura K, Kadota K, Kuratsu J. Long-term fol-
in modifying cerebral aneurysm hemodynamics. Ann Biomed Eng. low-up study of patients with cavernous sinus aneurysm treated by proxi-
2008;36:726–741. mal occlusion. Neurol Med Chir (Tokyo). 2000;40:88–96, discussion 96.

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 Flow Diversion Versus Conventional Treatment for Carotid Cavernous Aneurysms
Mario Zanaty, Nohra Chalouhi, Robert M. Starke, Guilherme Barros, Mark Philip Saigh, Eric
Winthrop Schwartz, Norman Ajiboye, Stavropoula I. Tjoumakaris, David Hasan, Robert H.
Rosenwasser and Pascal Jabbour

Stroke. 2014;45:2656-2661; originally published online July 22, 2014;

doi: 10.1161/STROKEAHA.114.006247
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