Complex Intracranial Aneurysms: Combined Operative and
Endovascular Approaches
Lotfi Hacein-Bey, M.D., E. Sander Connolly, Jr., M.D.,
Stephan A. Mayer, M.D., William L. Young, M.D.,
John Pile-Spellman, M.D., Robert A. Solomon, M.D.
Divisions of Interventional Neuroradiology, Departments of Radiology
(LH-B, W LY, JP-S), Neurological Surgery (ESC, W LY, JP-S, RAS), Neurology (SAM),
and Anesthesiology (WLY), College of Physicians and Surgeons, Columbia University,
New York, New York

O B J E C T IV E : E n d o v a s c u la r m a n age m e n t o f c o m p le x in tra c ra n ia l a n e u ry sm s is in c re a s in g ly b e in g co n sid e re d as an
a lte rn a tiv e to sta n d a rd s u rg ic a l c lip p in g . H o w e v e r, little a tte n tio n has been p a id to the c o m p le m e n ta ry nature of
su rg e ry an d e n d o v a s c u la r th e ra p y.
M E T H O D S : B etw een Se p te m b e r 1 9 9 2 and M ay 1 9 9 7 , 12 p a tie n ts w ith c o m p le x in tra c ra n ia l a n e u ry sm s w ere treated
w ith c o m b in e d o p e ra tiv e and e n d o v a s c u la r m e th o d s. Se ve n p a tie n ts d e m o n stra te d s u h a ra c h n o id hemorrhage
(tw o o f G ra d e II, tw o o f G ra d e III, and th ree o f G ra d e IV ). Five p a tie n ts d e m o n stra te d u n ru p tu re d aneurysm s, i.e.,
th ree g ia n t a n e u ry sm s (o n e v e rte b ro b a sila r ju n c tio n a n e u ry sm , o n e m id d le c e re b ra l a rte ry b ifu rc a tio n aneurysm,
and one in te rn a l c a ro tid a rte ry -o p h th a lm ic a rte ry a n e u ry sm ), o n e la rg e in te rn a l c a ro tid a rte ry -o p h th a lm ic artery
a n e u ry sm , an d o n e m id d le ce re b ra l a rte ry se rp e n tin e a n e u ry sm . M a n a g e m e n t stra te g ie s in v o lv e d eith er surgery
fo llo w e d by e n d o v a sc u la r th e ra p y (S-E ; n = 5) o r e n d o v a s c u la r th e ra p y fo llo w e d by s u rg e ry (E -S ; n = 7). S-E
p a ra d ig m s in c lu d e d a n e u ry sm e x p lo ra tio n fo llo w e d by e n d o v a s c u la r tre a tm e n t (S -E 1 ; n = 3), p a rtia l aneurysm
c lip p in g fo llo w e d by e n d o v a sc u la r a n e u rysm p a c k in g (S -E 2 ; n = 1), and e x tra c ra n ia l-to -in tra c ra n ia l bypass
fo llo w e d by e n d o v a sc u la r p aren t vessel o c c lu s io n (S -E 3 ; n = 1). E-S p a ra d ig m s in c lu d e d su p e rse le c tiv e angiog­
ra p h y fo llo w e d by s u rg ic a l c lip p in g (E -S 1 ; n = 2 ), G u g lie lm i d e ta c h a b le c o il p a rtia l d o m e p a c k in g follow ed by
d e la ye d s u rg ic a l c lip p in g (E -S 2 ; n = 2), p ro x im a l te m p o ra ry ve ssel b a llo o n o c c lu s io n fo llo w e d by aneurysm
c lip p in g (E -S 3 ; n = 2), and p ro x im a l p e rm a n e n t vessel o c c lu s io n fo llo w e d by s u rg ic a l a n e u ry sm decom pression
fo r m ass effect tre atm en t (E -S 4 ; n = 1).
R E S U L T S : Ele ve n a n e u ry sm s ( 9 2 % ) w e re c o m p le te ly e lim in a te d . T h e re m a in in g a n e u ry sm w a s 9 0 % obliterated and
re m a in e d q u ie sce n t at the 3 4 -m o n th fo llo w -u p e x a m in a tio n , d e sp ite p re se n tin g w ith s u b a ra c h n o id hemorrhage.
N o p atie n t e x p e rie n c e d repeat b le e d in g (fo llo w -u p p e rio d , 23 ± 28 m o ). T h e re w e re no d e ath s. O n e patient
a c h ie v e d a fa ir o u tco m e (G la s g o w O u tc o m e S c a le sc o re o f III) ; a ll o th e r p a tie n ts e x p e rie n c e d e xc e lle n t outcomes
(G la s g o w O u tc o m e S c a le sc o re o f I). In a ll case s, the a n e u ry sm m a n a g e m e n t p a ra d ig m ch o se n had a positive
effect on d e fin itiv e th e ra p y.
C O N C L U S I O N : S e v e ra l fa cto rs ca n c o n trib u te to the c o m p le x ity o f in tra c ra n ia l a n e u ry sm s. M an age m en t strategies
that c o m b in e o p e ra tiv e an d e n d o v a s c u la r te ch n iq u e s in a c o m p le m e n ta ry w a y , fo r the best p o ssib le outcom es for
these p atie n ts, ca n be d e sig n e d a c c o r d in g ly . (Neurosurgery 43:1 304—131 3, 1998)
Key words: Combined approach, Complex aneurysms, Endovascular treatment, Microneurosurgery

omplex intracranial aneurysms are not uncommonly
encountered in cerebrovascular practice (1, 6-8, 11, 13,
18, 19, 32, 40, 42). Often their complexity can render
standard treatment (i.e., surgical clipping) either impossible
or exceedingly hazardous (Tabic 1). Although endovascular
C

1304

therapy is an available alternative to surgical clipping (2, 4,5,
9, 10, 14-16, 20-22, 29, 31, 33, 41), it is not without risks (2—
40In contrast, a combined approach that uses the strengths ot
the two methods in a synergistic way may enhance the
chances of success in these challenging situations. We report

Neurosurgery, Vol. 4 1 No. 6, Dec ember 1448

Combined Treatment of Complex Aneurysms

TABLE 1. Factors Contributing to a Com plex Aneurysm
Aneurysm Anatomy

Clinical Factors

Size: large or giant, too small for a clip or a coil
Shape: fusiform, serpentine
Content: filled with fresh or laminated thrombus

Neurological condition: poor grade at presentation
Timing: vasospasm at time of presentation
General: significant cardiovascular, pulmonary, renal, or
endocrine comorbidity
Age: advanced age

Neck: difficult surgical access, broad, calcified, involves
perforating arteries
Perianeurysmal environment: aneurysm embedded in brain
tissue, bone, edema, scar tissue from previous surgery
our experience with 12 such cases and propose management
paradigms.

PATIENTS A N D M E T H O D S
Between September 1992 and May 1997, 12 patients with
complex aneurysms of the posterior (n = 5) or anterior (n = 7)
circulation were treated in a combined manner by neurosur­
gical and endovascular methods. The average age was 50
years (range, 25-70 yr); five patients were male, and seven
were female. Seven patients presented with subarachnoid
hemorrhage (SAH) proven by computed tomographic scan­
ning, with two cases of Hunt and Hess Grade II, two of Grade
III, and three of Grade IV. Five other patients presented with
extraordinarily complex unruptured aneurysms, i.e., one gi­
ant distal vertebral artery aneurysm, one giant middle cere­
bral artery (MCA) aneurysm, one serpentine MCA aneurysm,
and two carotid artery-ophthalmic artery aneurysms (Table 2).
Factors contributing to and consistent with a complex an­
eurysm were identified for each patient. Three patients pre­
sented with a poor Hunt and Hess grade (Grade IV) after
SAH. Associated problems, i.e., coronary artery disease (Pabent 1), severe vasospasm (Patients 1 and 8), and unfavorable
aneurysm location (large midbasilar and low basilar locations
m Patients 1 and 2, respectively), were present for these three
patients. For the remaining nine patients, the complexity was
mainly related to the aneurysm itself, i.e., restricted surgical
access to the neck (Patients 3, 4, 5, and 9), embedding of the
aneurysm in surrounding tissues (Patients 3, 4, 5, and 9), giant
^ize (Patients 7, 9, and 11), the presence of laminated throm­
bus (Patient 9), and broad neck (Patients 4, 6, 11, and 12).
Treatment decisions for all 12 patients were made after
Multidisciplinary consultation that involved neurosurgical,
endovascular therapeutic, neurological, and anesthesiological
^ervices. The management strategy was either surgery fol°wed by endovascular therapy (S-E) (n = 5) or endovascular
therapy followed by surgery (E-S) (n = 7) (Table 3).
S"E paradigms included aneurysm exploration followed by
end°vascular treatment (S-El; n = 3), partial aneurysm clipPln8 followed by endovascular aneurysm packing (S-E2; n = 1),
j^nd extracranial-to-intracranial bypass followed by endovascuar parent vessel occlusion (S-E3; n = 1). E-S paradigms included
N e u r o s u r g e r y , Vol.

superselective angiography followed by surgical clipping (E-Sl;
n = 2), partial dome packing with Guglielmi detachable coils
(GDC) followed by delayed surgical clipping (E-S2; n = 2),
proximal temporary vessel balloon occlusion followed by an­
eurysm clipping (E-S3; n = 2), and proximal vessel occlusion
followed by surgical aneurysm decompression for mass effect
treatment (E-S4; n = 1).
Treatment was performed within 5 days after SAH for all
seven patients who presented with bleeding. Patients with
unruptured aneurysms were treated within 4 weeks of pre­
sentation. Heparin was administered intravenously to all pa­
tients during endovascular explorations (including superse­
lective angiography), embolization, or temporary arterial
occlusion during surgical exploration. Also, patients who pre­
sented with SAH received heparin treatment for a few days
after aneurysm obliteration.

RESU LTS
C lin ic a l o u tco m e s
Eleven patients experienced excellent outcomes, defined as
no neurological deficit at the time of the most recent follow-up
examination (Glasgow Outcome Scale score of 1). One patient
(Patient 2) experienced a fair outcome (Glasgow Outcome
Scale score of 3 at a 2-yr follow-up examination), as a result of
a thromboembolic complication (the only one in this series).
After GDC packing of a large, recently ruptured, basilar apex
aneurysm, this patient continued to receive heparin therapy
to protect a large thalamo-perforating artery originating from
the aneurysm base. Heparin administration was discontinued
4 hours later for the placement of a ventricular drain. A few
hours later, the patient developed acute right third nerve
palsy and left hemiparesis, and computed tomography dem­
onstrated an upper brain stem and right thalamic infarction.
The patient eventually made a reasonable recovery, with
moderate residual hemiparesis and diplopia.

A n e u ry sm o b lite ra tio n
All aneurysms were eventually eliminated, with the excep­
tion of one large midbasilar aneurysm (Patient 4). After SAH

43,No.

December 1998

1305

1306

Hacein-Bey et al.

T A B LE 2. D em ographic and C lin ic a l Data for 12 Patients with C o m p le x Cerebral Aneurysm s
Complication

Outcome

Follow-up
Period
(mo)

Excellent
Fair

30
34

S-E1

None
Midbrain infarction
after embolization
None

Excellent

12

S-E1

None

Excellent

34

S-E2

None

Excellent

17

S-E1

None

Excellent

35

E-S1

None

Excellent

34

E-S1

None

Excellent

56

E-S4

None

Excellent

9

S-E3

None

Excellent

12

E-S3

None

Excellent

4

E-S3

None

Excellent

2

Difficulty Factor

Treatment
Paradigm

SAH/IV
SAH/IV

Poor grade after SAH
Poor grade after SAH

E-S2
E-S2

Large basilar apex

SAH/II

38

Large midbasilar

SAH/III

M

42

Small anterior
communicating

SAH/II

6

F

52

SAH/III

7

M

25

8

F

50

9

M

70

Large ICAophthalmic
Giant MCA
bifu rcation
Small anterior
communicating
Giant distal VA

Difficult surgical
access
Broad neck, embedded
in brain tissue
Embedded in brain
tissue, previous
surgery
Broad neck, embedded
in bone
Perforators near
aneurysm neck
Poor grade after SAH

10

M

47

11

F

66

12

F

42

Age
Patient Gender
(yr)

Aneurysm/)

1
2

M
F

65
33

Small mid-basilar
Large basilar apex

3

F

69

4

F

5

Large serpentine
MCA
Giant ICAophthalmic
Large ICAophthalmic

Presentation/Grade

Headaches
SAH/IV
X-XII cranial nerve
compression
Headaches, loss of
consciousness
Progressive vision
loss
Headaches

Giant aneurysm with
laminated thrombus
Fusiform shape
Broad neck, embedded
in dura
Broad neck, embedded
in dura

7 MCA, middle cerebral artery; VA, vertebral artery; SAH, subarachnoid hemorrhage; E-S, endovascular therapy followed by surgery; S-E,
surgery followed by endovascular therapy; ICA, internal carotid artery.
h Aneurysm size: small, < 1 0 mm; large, 10 to 25 mm; giant, > 25 mm.

TABLE 3. Management Paradigms for Com plex Aneurysms
E-S Paradigms

S-E Paradigms

E-S1: superselective angiography —> surgical clipping
E-S2: endovascular aneurysm dome packing —» surgica
clipping
E-S3: proximal temporary vessel balloon occlusion —» aneurysm
clipping
E-S4: endovascular proximal permanent occlusion —» surgica
aneurysm decompression

S-E1: surgical exploration —» endovascular treatment
S-E2: partial surgical clipping -^endovascular
aneurysm obliteration
S-E3: EC-IC bypass —> endovascular parent vessel
occlusion

E-S, endovascular therapy followed by surgery; S-E, surgery followed by endovascular treatment; EC-IC, extracranial-to-intracranial.

and unsuccessful GDC packing of the aneurysm dome, sur­
gical exploration revealed that the aneurysm was embedded
in the pons and therefore unclippable. During the subsequent
1 month, the patient developed progressive left-sided facial
weakness, diplopia, and hemisensory loss in the trigeminal
distribution. Repeat angiography revealed that the aneurysm
had grown, and repeat magnetic resonance imaging sug­
gested that a short circumferential, brain stem perforator had
been occluded. GDC packing of the aneurysm fundus was
then performed, with little effect on subsequent aneurysm
growth. Finally, staged bilateral vertebral artery balloon oc­
clusion was performed, with evidence of gradual aneurysm
obliteration to approximately 90% in follow-up angiograms.

IL L U S T R A T IV E C A S E S
Patient

1 w as a 65-year-old

m ale patient with hypertension

and coronary artery disease, for w hich he had recently undergone a
coronary artery b y p ass graft. H e presented with Hunt and Hess
G rad e IV. An initial an giog ram yielded norm al findings; a second
angiogram revealed a sm all m id basilar aneu rysm {Fig. 1 A). The pa­
tient w as initially treated with partial (95%) aneurysm coil packing
{Fig. IB ), to allow him to be treated in the intensive care unit during

the critical vasosp asm / rep eat h em orrh age period. Although the clin­
ical cou rse for this patient w as initially com plicated by sepsis, hydro
cephalus requiring a ventriculoperitoneal shunt, and deep venous
throm bosis requiring placem ent of a Greenfield filter, the patient
eventually m ad e a good recovery. Delayed surgical clipping of the

Neurosurgery , Vol. 41, No. 6, Hoc ember 1948

Combined Treatment of Complex Aneurysms

n o 7

V
'

â–  â– *

A
FIG U R E 1. A to C, Patient
1, a 65-year-old male patient
with hypertension and
coronary artery disease who
presented in Hunt and
Hess Grade IV condition.
%
A small basilar aneurysm
^
(A, arrowhead) was initially
treated with partial (9 5 % )
aneurysm coil packing
( B, arrowhead) to allow
management in the intensive care unit during the critical
period. Delayed aneurysm clipping was performed
uneventfully, after repeat angiography showed a patent neck
(C, arrowhead).

L

eurysm w as eventually p erform ed uneventfully, after repeat an
)graphy showed a p aten t n e c k <•
whQ suffered a G ra d e 11
Patient 5 was a 43-year-old m a p
anterior com m unicatiH from a broad-necked, upw ard v Poin ; ' hnicany difficult, in
/r• 9 a \ Qnr{?0 rv w as tecnn
j artery aneurysm (Fig. I M - =>u r & .v
placed across
rt because of n u m ero u s p erforators, w o
treated in the intene aneurysm neck. T h e p atien t w as s u c c e s s f u l y r e a p e d
^
re care unit for v asosp asm . R ep eat a W â„¢ â„¢

^ du ced the n eck

2 0 confirmed

eurysm was patent, although partia c ippi
-e presence
I * < Fof» n* u
»•
m erou s p erfora

f “

k i "

8

as possible (Fig. 2D).
Patient 9 was a 70-year-old e m p lo y e
usi
perienced a 3-m onth history o f in creasin g

^vprutive w h o had
jUent d j ZZiness,
d w eight lo ss.

it ataxia, and loss o f appetite, resu ltin g m a

eaj ed a partially

'aluation by m agnetic reso n an ce
rombosed giant an eu ry sm co m p res
ography suggested that the
;ht vertebral artery (Fig. 3B). D esp

m edulla (Fig. 3A). An-nate(j from the distal

g

an R e g r e s s i v e presigm oid
found to b e unclip-

aniectomy for exploration, the ane^
sn\
ible. Three m onths later, h y d ro cep a

peritoneal shunt was placed. The patien wa

eloped and a ventricurppxamined 3 m onths

orns^ jncluding

ter because of further p ro g ression o
Q:i.aHn a a w alker), and
urseness of voice, w o rsen in g ataxia n eces
^ ovascu j ar balloon
piration pneum onia. A t that p oin t, an
as placed across the an eu ry sm n eck in
6
ig. 3C), after successful tem p orary test occ ^
e aneurysm w as found to b e fully t
co
mpression (Fig. 3D ), the sig n s o f m edulh y

vertebral artery
^ ^eW Weeks later,
^
su rgical deession quickly

solvedV,
erienced a generalized
Patient 1 0 was driving his car w h en e exP g e n e t i c resonance
nic-clonic seizure, w ith loss o f co n scio u sn es
M C A aneurysm
'aging showed a 2 -cm , partially throm bosed ,

FIG U R E 2. A to D, Patient 5, a 43-year-old male patient
who suffered a Grade II SAH from a broad-necked, upwardly
pointing, anterior com m unicating artery aneurysm (A). Sur­
gery was technically difficult, in part because of numerous
perforators; two clips were placed across the aneurysm neck.
Repeat angiograms showed that the aneurysm remained
patent, with partial neck clipping (B, arrowhead). Superse­
lective angiography confirmed the presence of numerous
perforators (C ). Total G D C aneurysm packing was possible
(D , arrowhead).
(Fig. 4A ). A ngiography revealed a serpentine aneu rysm , with two

posterior parietal branches arising from its distal part (Fig. 4B). S u r­
gical exploration confirm ed the fusiform nature of the lesion, and a
graft w as perform ed that connected the superficial tem poral artery to
the M CA distal to the aneurysm . The follow ing day, bypass patency
w as confirm ed (Fig. 4C ) and the M C A branch afferent to the a n e u ­
rysm w as occluded for 2 0 m inutes with a platinum coil. The patient
passed the test, and the vessel w as perm anently occluded, resulting in
aneurysm exclusion (Fig. 4D ).

D IS C U S S IO N
Direct clipping of intracranial aneurysms is currently the
standard of care whenever possible with acceptable operative
risks (1, 2, 5-9, 11, 13, 15, 18-20, 29, 31-33, 40, 41). Endovas­
cular management (usually GDC packing) is generally re­
served for patients for whom the risk/benefit ratio for direct
surgery is considered greater than that for endovascular treat­
ment (1, 6-8, 11, 13, 18-20, 29, 31, 32, 40, 42). The estimated
risk/benefit ratio for each treatment method is highly variable
among operators (with varying experience levels and philos­
ophies). As a result, different institutions may elect to treat
similarly complex lesions in different ways, based on both
anatomic factors (aneurysm size, shape, content, and neck
configuration and perianeurysmal reaction) and clinical fac­
tors (neurological grade, timing of presentation, presence of

N e u r o s u r g e r y , Vol. 43 , No. 6, December 1998

1308

Hacein-Bey et al
»I

rM p r
f
r

*

r

-i

A

FIG U R E 3. A to D, Patient 9, a 70-year-old male patient
with a 3-month history of increasing intermittent dizziness,
gait ataxia, and loss of appetite, resulting in a 30-pound
weight loss. Magnetic resonance imaging revealed a partially
thrombosed giant aneurysm compressing the medulla
(A, arrowheads). Angiographic results suggested that the
aneurysm originated from the distal right vertebral artery
(B, arrowhead). Endovascular balloon occlusion across the
aneurysm neck in the distal vertebral artery was performed
(C, arrowhead) after successful temporary test occlusion.
A few weeks later, the aneurysm was found to be fully
thrombosed; after surgical decompression (D , arrowhead ),
the signs of m edullary compression quickly resolved.
vasospasm, general medical condition, and patient age) (Table 1).
Although several reports have attempted to delineate the supe­
riority of one method or the other in certain settings, the advan­
tages of a multidisciplinary team approach to aneurysm treat­
ment have not been well documented. Although neurosurgical
rescue for coil migration, endovascular vessel rupture, or clip­
ping of coil-treated aneurysm remnants (2, 5, 15, 41) and endo­
vascular packing of partially clipped aneurysms (Patient 5) have
been reported (10), combined management paradigms that em­
brace proactive team evaluation to optimally use the strengths of
these divergent techniques to treat difficult conditions have not
been highlighted. The advantages of such a combined philoso­
phy can be represented as management paradigms (Tabic 3).

S u p e rse le c tiv e a n g io g ra p h y b efo re su rg e ry
Aneurysm anatomy is often difficult to completely delin­
eate during routine preoperative angiography. Certain fac­
tors, including unstable patient condition, moderate experi­
ence of the angiographer, limitations in contrast medium
resulting from systemic patient disease, the presence of vaso­

FIG U R E 4. A to D, Patient 10, a 47-year-old male patient
who was driving his car when he experienced a generalized
tonic-clonic seizure, with loss of consciousness. Magnetic
resonance im aging showed a 2-cm , partially thrombosed,
M CA aneurysm (A). Angiography (postbypass study shown)
revealed a serpentine aneurysm, with two posterior parietal
branches arising from its distal part ( B ). Surgical exploration
confirm ed the fusiform nature of the lesion, and a superficial
temporal artery-distal M CA bypass graft was performed. The
follow ing day, bypass patency was confirm ed (C ), and the
M CA branch afferent to the aneurysm was occluded with a
platinum coil (D , arrowhead).

spasm or intra-aneurysmal thrombus, and the presence of nu­
merous overlying vessels, may contribute to suboptimal assess­
ment of neck and perforator anatomic features. Superselective
angiographic aneurysm exploration before surgery may prove
useful in selected cases, especially when information on the
anatomic features and number of neighboring perforators is
crucial. With experienced investigators, this should outw eigh the
potential risks of superselective aneurysm angiography (throm­
bus migration and perforation). For Patient 7, information re­
garding the exact location of the M2-MCA branches associated
with the neck of the giant MCA bifurcation aneurysm not only
was helpful in guiding eventual clip placement but also influ­
enced the decision to pursue clipping, rather than proximal
occlusion after distal bypass.
Another advantage of preoperative superselective aneu­
rysm neck exploration for broad-neck aneurysms neighboring
arterial bifurcations, such as the MCA bifurcation, lies in the
precise identification of branches involved in the aneurvsm
neck, for which a distal bypass is necessary for clipping to bt
most effective. Such information should help avoid the de\
astating effect of bypassing the noninvolved branch.

Neurosurgery, Vol. 43, No. (•>, December 1998

Combined Treatment of Complex Aneurysms
Temporary e n d o v a sc u la r p ro te c tio n fo r p atien ts w ith
SAH who are at h igh risk
Although the effect of poor neurological grade at presen­
tation on the outcomes for surgically treated patients is well
documented (32), it has also been demonstrated that, with
aggressive surgical clipping, favorable outcomes could be
obtained for patients with poor Hunt and Hess grades. This
was the case for 55% of patients of Grade IV condition and
25% of those of Grade V condition in a recent study (25, 26).
Also, in the same study, intraoperative complications (failure
to occlude the aneurysm, intraoperative rupture, and cerebral
contusion) were no greater among patients of poor-grade
condition undergoing early surgery than among those of
good-grade condition, at least for anterior circulation aneu­
rysms (25, 26). In addition, age alone has been reported not to
be associated with markedly increased surgical complication
rates (11). Nonetheless, in clinical practice, early surgery for
patients of poor-grade condition (Grades IV and V) with
difficult aneurysms is not advocated (41). It is also widely
thought that older patients, who are more likely than younger
patients to present with a poorer clinical status at admission,
a larger amount of subarachnoid blood, higher incidences of
hydrocephalus and intraventricular hemorrhage, more preex­
isting medical conditions, and a greater incidence of symp­
tomatic vasospasm because of diminished cerebrovascular
reserve (23), should be more strongly considered for endovas­
cular therapy whenever possible (5, 14, 29, 33, 41, 43).
Several groups have demonstrated the effectiveness of en­
dovascular GDC aneurysm treatment in protecting patients at
high risk from subsequent bleeding (5, 14, 29, 33, 43). How­
ever, procedural morbidity (9-31%) and mortality (2-9%)
rates were highly variable among groups (5, 14, 29, 33, 43).
Although troubling, these values can be compared with those
of generally accepted surgical results, namely 14% overall
morbidity and 27% mortality rates in a largely quoted series
°f 153 patients (37). Perhaps somewhat more disappointing
are the reported short-term angiographic follow-up results;
although 20-70% of aneurysms underwent initially total oblit­
eration (5, 14, 29, 33, 43), 15-30% recanalization was reported
at 12 months (5-33). Furthermore, delayed bleeding at 6
months (29), symptomatic regrowth requiring retreatment in
nearly one-third of the patients at the 3-year follow-up exam­
inations (33), and no overall improvements in outcomes and
mortality rates for patients of poor-grade status, especially
those with basilar aneurysms (29, 33), were all reported in
initial studies. Fortunately, in a large, more recent, multicenter study (43) of 403 patients, the overall morbidity rate
lvas °nly 8.9% and the mortality rate was only 6.2%. Although
these values compare favorably with reported neurosurgical
results, it is not unreasonable to expect significantly better
results in an established practice, because two important char­
acteristics of the study were a patient selection bias toward
Patients at high risk, who were considered poor surgical
Candidates, and wide variations in operator skills (during the
lrhtial learning period for some).
F°r these reasons, partial endovascular aneurysm packing,
0 °btain temporary protection without compromising future

1309

surgical management, has been advocated (2, 5, 15, 21, 22, 41,
43). This is not always possible or easy, because of the mul­
tiplicity of aneurysm configurations; future clipping can be
rendered extremely difficult, often requiring prolonged tem­
porary occlusion and aneurysm opening for coil extraction
before final clip placement (2, 41). However, such a sequential
approach was successful for Patients 1 and 2 in this series, for
whom the crucial protective effect of partial endovascular
aneurysm packing was compatible with delayed permanent
surgical clipping. The authors think that, whenever techni­
cally and logistically possible, patients with complex aneu­
rysms at high risk should be treated with temporary partial
endovascular occlusion, followed by surgical clipping. It has
also been suggested that ruptured giant or broad-necked an­
eurysms should undergo partial GDC packing followed by
further embolization or surgical clipping (43), although these
types of aneurysms may be treated with surgical clipping
during temporary balloon occlusion of the parent vessel (39)
or, in selected cases, with permanent occlusion of the parent
vessel, if tolerated (1, 6, 8, 9).

Intraop erative tem porary b alloo n o cclu sio n for clip p in g
Large aneurysms of the ophthalmic segment can be diffi­
cult to treat. Recent improvements in microsurgical tech­
niques, such as complete removal of the posterior orbit, optic
strut, and superior orbital fissure, have contributed to making
many of these aneurysms clippable. Also, suction decompres­
sion techniques have been shown to be of help. All of these
maneuvers require proximal control of the extracranial inter­
nal carotid artery (ICA), which is most commonly obtained by
surgical exposure of the cervical carotid artery. Also, certain
posterior circulation aneurysms, such as large posteroinferior
cerebellar artery or basilar apex aneurysms, greatly benefit
from proximal control of the vertebral artery. Intraoperative
endovascular techniques are well suited for proximal control
of cervical arteries and decompression (39). One factor that
might explain the lack of popularity of intraoperative endo­
vascular techniques, in addition to the need for specialized
equipment and excellent team coordination, is the require­
ment for heparin treatment. Indeed, with extensive bone ma­
nipulation, heparin treatment can potentially aggravate blood
loss. However, we and others (39) have found that rapid
technique, timely coordination among operators, and experi­
ence with the procedures allow the use of minimal amounts of
heparin. Other advantages to this approach include the ability
to extemporaneously confirm angiographically determined
optimal clip placement, postclipping documentation of aneu­
rysm obliteration, and obviation of the need for surgical ex­
posure of the carotid artery in the neck.

E n d o v a sc u la r a rte ria l o c c lu s io n fo r
a n e u rysm d e co m p re ssio n
Aneurysms can present with mass effects that are alleviated
by decompression, either by aneurysm sac packing or by
parent vessel occlusion (16). In the anterior circulation, the
currently preferred treatment for cavernous ICA aneurysms
and certain complex posterior ICA aneurysms involves ICA

N e u r o s u r g e r y , Vol. 43, No. 6, December / 998

1310

Hacein-Bey et al

occlusion. The effectiveness of hunterian ligation is greatest
when the aneurysm neck is occluded, and it decreases grad­
ually as the occlusion is more remote from the neck. Endo­
vascular balloon occlusion provides the ability to occlude the
vessel close to the aneurysm, which also reduces the likeli­
hood of "stump emboli" (9). For vertebrobasilar aneurysms
originating just distal to the posteroinferior cerebellar artery
and midbasilar aneurysms originating just distal to critical
midbrain perforators, as demonstrated by superselective an­
giography, proximal ligation or trapping via direct clipping is
the recommended treatment, because balloons may occlude
the origins of critical vessels. More proximal balloon occlu­
sion, which is slightly less effective but safer, was performed
for Patient 4, with a basilar bifurcation aneurysm that could
not be treated by clipping or coil placement. Vertebral artery
balloon occlusion across the neck of a giant distal vertebral
aneurysm allowed thrombosis of the lesion before successful
surgical debulking for mass effect treatment for Patient 9.

E x p lo ra to ry su rg e ry b e fo re e n d o v a sc u la r tre atm e n t
In some circumstances, only exploratory craniotomy con­
firms, for a surgeon, that a complex aneurysm is unclippable.
Also, total aneurysm neck clipping is not always possible, for
a variety of reasons (presence of perforators, lack of adequate
exposure, lack of an adequate clip, calcification in the neck
region of the aneurysm, and partial intracavemous location).
However, exploratory or incomplete surgery should not be
viewed as a failure, because it may provide important infor­
mation to the interventional neuroradiologist. Observations
regarding the thinnest part of an aneurysm wall or, even
better, muslin wrapping of the thin aneurysm wall contrib­
utes to the safety of subsequent endovascular treatment, by
helping avoid dome perforation by a catheter or coils.

boembolism, with resultant ischemic stroke, were not uncom­
mon. Furthermore, antegrade flow was not always completely
obliterated, especially in the case of carotid artery bifurcation
or basilar apex lesions, which often continued to fill via fetal
posterior communicating arteries.
Balloon test occlusion has allowed functional evaluation in
conscious patients, thereby greatly improving patient selec­
tion. This test has become even more effective with the advent
of additional pharmacological challenges. When test occlu­
sion is tolerated, subsequent occlusion with complete hepa­
rinization decreases thromboembolic complications; as a re­
sult, this approach has become the treatment of choice for
certain aneurysms, such as giant proximal intradural carotid
artery aneurysms. For patients who do not tolerate test occlu­
sion, a preliminary extracranial-to-intracranial bypass (either
superficial temporal artery-MCA or external carotid arteryMCA, with reversed saphenous vein) is performed. These
bypasses can, in some cases, result in such profound flow
alteration that aneurysm thrombosis is promoted before final
parent vessel occlusion, as was the case for Patient 10 in our
series.

O b s ta c le s
There are several potential obstacles to the development of
a completely integrated approach to aneurysm management,
such as differences in perceived roles among various specialty
teams, geographic separation of operating rooms and endo­
vascular suites within health facilities, and the current lack of
guidelines for the training of interventionalists. In addition,
the lack of unbiased outcome data for either management
strategy may contribute to creating distrust among participants
in the two groups. However, increased communication between
groups is the best approach to transcend these barriers.

P a rtia l s u rg ic a l c lip p in g fo llo w e d by e n d o v a sc u la r
a n e u rysm o b lite ra tio n
Completion of aneurysm obliteration by endovascular
means after partial clipping has been reported (10). Partial
clipping also reduces the size of the neck, making compaction
of the coil mass less technically challenging and safer. Other
advantages to this approach involve the information provided
by the surgeon regarding the perianeurysmal environment,
such as the presence of perforators, and the possibility of
further protecting the aneurysm by wrapping it with muslin.

E n d o v a sc u la r a rte ria l o c c lu s io n after b yp ass
Hunterian or proximal ligation of parent arteries has long
been used for the treatment of both anterior and posterior
circulation aneurysms (1, 6-9, 11, 13, 18-20, 29, 31, 32, 40, 42).
Traditionally, ICA ligation was performed extracranially by
surgical ligation, and posterior fossa aneurysms were treated
either by direct vertebral artery sacrifice distal to the postero­
inferior cerebellar artery or by basilar occlusion between the
superior cerebellar artery and the posterior cerebral artery
segments. Because of the lack of preoperative functional test­
ing and postoperative heparinization, flow failure and throm­

C O N C L U S IO N S
Not infrequently, the therapeutic difficulties presented by
complex cerebral aneurysms are not appreciated prospectively, for a variety of reasons, including the severity of the
disease and the need to provide protection from s u b s e q u e n t
hemorrhaging. Treating physicians, whether neurosurgeons or
interventional neuroradiologists, may find themselves pressed
to exceed the limits of their techniques. However, the availability
of other options and their judicious integration in patient care
may have a positive effect on outcomes. Temporary endovascu­
lar protection of aneurysms before clipping, endovascular d e l i n ­
eation of perforator anatomic features before surgery, comple­
tion of aneurysm packing after partial clipping, intraoperative
temporary balloon occlusion of the parent vessel to assist s u r g i ­
cal clipping, and bypass surgery before endovascular occlusion
are all possible using combined surgical/endovascular manage­
ment strategies. When used rationally, this approach emphasizes
the complementary nature of these techniques and offers the
—
best chance for reducing treatment morbidity and improving
long-term outcomes in the most difficult cases.

Neurosurgery , Vol. 43 , No. 6, December 1998

•

Combined Treatment of Complex Aneurysms
Received, January 23, 1998.
Accepted, July 31, 1998.

17. Heros RC: T h rom boem b olic com plications after com bined inter­

Reprint requests: Lotfi H acein-Bey, M.D., D iagnostic and Interven­
tional Neuroradiology Section, D ep artm ent of Radiology, University
of Vermont College of M edicine, 1 1 1 C olchester A venue, Burlington,
VT 05401.

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CO M M EN TS
Hacein-Bey et al. describe their experience with 12 patients
with complex intracranial aneurysms who were treated with
combined operative and endovascular methods. Although
these approaches have been reported in simple case reports
from other institutions, the authors have systematically sum­
marized the options from both the endovascular and surgical
perspectives. In Table 3, the authors discuss the management
paradigms for complex aneurysms and, in the category of
endovascular followed by surgical treatment, they indicate
that supraselective angiography might lead to surgical clip­
ping because of a large neck or perforator involvement, which
would preclude endovascular therapy. Our experience with
computed tomographic angiography has demonstrated that
supraselective angiography is often not necessary to delineate
these features, but computed tomographic angiography is
extremely useful in assessing not only neck size but also the
presence of critical perforators in areas that could only be
treated surgically and that would be at high risk from endo­
vascular occlusion. In addition, endovascular dome packing
followed by surgical clipping has not actually been shown to
reduce repeat bleeding, although the authors observed no
repeat hemorrhaging in this small group of patients. We also
have provided aneurysm protection by incomplete endovas­
cular obliteration, but our approach has been to treat the
entire lesion with coils, if at all possible. If a delayed recur­
rence occurs, then certainly these patients can be treated with
definitive surgical therapy; proximal temporary balloon oc­
clusion and suction decompression have been found to be
extremely useful in the treatment of giant paraclinoid aneu­
rysms and aneurysms of the posterior circulation. These tech­

niques provide excellent decompression of the sac and are
easily performed intraoperatively from a transfemoral route.
It has not been our experience that the heparin infusion asso­
ciated with this technique leads to increased blood loss.
There is no question that partial surgical clipping of large
complex aneurysms may lead to successful endovascular
obliteration, by transforming large-necked aneurysms into
small-necked aneurysms, allowing safe coil placement within
the aneurysms without fear of parent vessel occlusion, and
providing better long-lasting obliteration rates by controlling
the inflow zone. Obviously, this finding must be investigated
in a larger study. Most importantly, the authors, from a very
experienced neurovascular center, emphasize that a multidis­
ciplinary approach is essential for the best patient care and we
should put aside differences in perceived roles among various
specialty teams. It is hoped that, in the future, the approach to
such complex aneurysms will be multidisciplinary.

Robert H . Rosenwasser
Philadelphia, Pennsylvania
The authors report the management outcomes for 12 pa­
tients with complex intracranial aneurysmal disease. This re­
port emphasizes the necessity for a collaborative and multi­
disciplinary approach to these difficult problems. The authors
draw our attention to several specific aspects of the diagnos­
tic, therapeutic, and postoperative periods for which the com­
bination of intravascular and extravascular approaches is sen­
sible. Clinicians can evaluate each case in terms of the assets
and liabilities of each specific therapeutic alternative and can
develop well-considered strategies onlv by working as a co­
hesive team. As the authors have illustrated, unexpected
events during the course of treatment mandate a flexible
approach, with reconsideration of alternatives to the origi­
nally planned strategy.
It is becoming clearer that certain lesions are best treated by
microsurgery and other lesions are best treated by endovas­
cular techniques. However, there is an increasing percentage
of lesions for which the best treatment is not obvious. It is
these lesions that the authors have discussed in the context of
a true multidisciplinary approach. It is important to remem­
ber that the advent of microsurgery was originally thought to
have solved the problem of simple and complex intracranial
aneurysms. The development of endovascular techniques was
similarly thought, several years ago, to provide the definitive
solution. Time has clarified this issue and has confirmed that
we do not now have the means to manage the most complex
forms of this condition. The dysplastic vasculature leading to
complex large and giant aneurysms defies straightforward
treatment. Regardless of the strategies applied, it is critical
that long-term follow-up monitoring (for many years) be used
for these patients. Despite comments to the contrary, recur­
rence remains a lifetime risk, regardless of treatment strategy,
for patients with complex aneurysms.

Neurosurgery, Vol. 43, No. 6, December 1C)C)8

H. H unt B atjer
C h ic a g o , Illinois