J Neurosurg 120:398–408, 2014

398 J Neurosurg / Volume 120 / February 2014

©AANS, 2014

The treatment of giant (diameter ≥ 2.5 cm) or fu-siform middle cerebral artery (MCA) aneurysms may be very challenging despite the introduction

of refined microsurgical techniques and advances in endo-vascular methods.3,8–11,14,15,17,22,26,27,33,40

Giant saccular aneurysms may have wide and par-tially calcified necks, with major branches or perforating arteries incorporated at the base, or the aneurysm walls may be atherosclerotic and the lumen partially throm-bosed, making clipping or endovascular embolization challenging and often almost impossible. Fusiform an-eurysms have no neck at all, as the entire vessel wall of the dilated arterial segment is pathological, and the lumen may be partially thrombosed, making these lesions also unamenable to conventional treatment techniques. Fusi-form aneurysms of the M1 segment of the MCA typically involve origins of lenticulostriate arteries, further compli-cating treatment strategies. Lastly, failure of previous en-dovascular treatment may present challenging problems.

Bypass surgery for complex middle cerebral artery aneurysms: impact of the exact location in the MCA tree

Clinical articleLeena KivipeLto, M.D., ph.D.,1 MiKa nieMeLä, M.D., ph.D.,1 torstein MeLing, M.D., ph.D.,2 Martin LehecKa, M.D., ph.D.,1 hanna Lehto, M.D.,1 anD Juha hernesnieMi, M.D., ph.D.1

1Department of Neurosurgery, Helsinki University Hospital, Helsinki, Finland; and 2Department of Neurosurgery, Oslo University Hospital-Rikshospitalet, Oslo, Norway

Object. The object of this study was to describe the authors’ institutional experience in the treatment of complex middle cerebral artery (MCA) aneurysms necessitating bypass and vessel sacrifice.

Methods. Cases in which patients with MCA aneurysms were treated with a combination of bypass and parent artery sacrifice were reviewed retrospectively.

Results. The authors identified 24 patients (mean age 46 years) who were treated with bypass and parent artery sacrifice. The aneurysms were located in the M1 segment in 7 patients, MCA bifurcation in 8, and more distally in 9. The mean aneurysm diameter was 30 mm (range 7–60 mm, median 26 mm). There were 8 saccular and 16 fusiform aneurysms.

Twenty-one extracranial-intracranial and 4 intracranial-intracranial bypasses were performed. Partial or total trapping (only) of the parent artery was performed in 17 cases, trapping with resection of aneurysm in 3, and aneu-rysm clipping with sacrifice of an M2 branch in 4.

The mean follow-up period was 27 months. The aneurysm obliteration rate was 100%. No recanalization of the aneurysms was detected during follow-up.

There was 1 perioperative death (4% mortality rate) and 6 cerebrovascular accidents, causing permanent mor-bidity in 5 patients. The median modified Rankin Scale score of patients with an M1 aneurysm increased from 0 pre-operatively to 2 at latest follow-up, while the score was unchanged in other patients. Most of the permanent deficits were associated with M1 aneurysms. Twenty-one patients (88%) had good outcome as defined by a Glasgow Outcome Scale score of 4 or 5.

Conclusions. Bypass in combination with parent vessel occlusion is a useful technique with acceptable frequen-cies of morbidity and mortality for complex MCA aneurysms when conventional surgical or endovascular techniques are not feasible. The location of the aneurysm should be considered when planning the type of bypass and the site of vessel occlusion. Flow alteration by partial trapping may be preferable to total trapping for the M1 aneurysms.(http://thejns.org/doi/abs/10.3171/2013.10.JNS13738)

Key WorDs      •      cerebral revascularization      •      giant aneurysm      • fusiform aneurysm      •      aneurysm treatment      •      parent vessel occlusion      • vascular disorders

Abbreviations used in this paper: ASA = acetylsalicylic acid; CTA = CT angiography; DS = digital subtraction; DSA = DS angiography; ECA = external carotid artery; EC-IC = extracranial-intracranial; ELANA = excimer laser-assisted nonocclusive anas-tomosis; GOS = Glasgow Outcome Scale; ICA = internal carotid artery; IC-IC = intracranial-intracranial; MCA = middle cerebral artery; mRS = modified Rankin Scale; OA = occipital artery; SAH = subarachnoid hemorrhage; STA = superficial temporal artery.

J Neurosurg / Volume 120 / February 2014

Bypass and vessel occlusion for complex MCA aneurysms

399

Nevertheless, because untreated giant aneurysms have a 5-year combined morbidity and mortality rate of 80%, it is widely agreed that they should not be left untreated.4,12,39,48

When conventional surgical or endovascular treat-ment is not feasible, occlusion of the aneurysm may be achieved by parent vessel sacrifice combined with distal revascularization. Several modifications of this treatment modality have been described, including extracranial-intracranial (EC-IC) or intracranial-intracranial (IC-IC) bypass or more refined revascularization methods, such as in situ bypass or various vascular reconstructions, in combination with total or partial trapping of the aneurysm by means of parent artery occlusion.21,23,24,31,34,36–38,46

So far, only small series of MCA aneurysms treated with a combination of bypass and parent vessel sacrifice have been described. We report our experience in 24 com-plex MCA aneurysm cases treated with an EC-IC or IC-IC bypass followed by partial or complete parent vessel oc-clusion. We also discuss the different treatment require-ments for aneurysms at different locations of the MCA vasculature.

MethodsThe Helsinki intracranial aneurysm database was

screened to identify all patients with an MCA aneurysm treated with a combination of bypass and parent vessel oc-clusion (Table 1). The database includes over 10,000 cases involving patients with intracranial aneurysms admitted to the Department of Neurosurgery at Helsinki Univer-sity Hospital since 1937. Medical records were reviewed for relevant clinical information. The study was approved by the Ethics Committee of Helsinki University Central Hospital.

PatientsTwenty-four patients (15 men and 9 women) were

treated for complex MCA aneurysms using a combina-tion of bypass and vessel sacrifice between January 1998 (when bypass surgery was initiated at our institution) and June 2012. The mean age of the patients was 46.5 years (range 12–73 years, median 48 years) (Tables 1 and 2). During the time period of our present study, 3780 patients with intracranial aneurysms were treated at our institu-tion, and 48% of these patients harbored MCA aneurysms, including 45 giant MCA aneurysms. Thus, the 24 MCA aneurysms treated with bypass represent about 1% of all the MCA aneurysms surgically treated at our institution.

In addition to these 24 cases, there were 4 cases in which a bypass was planned and attempted but was not successfully completed. The aneurysm was then directly clipped in the same surgery or later. A summary of these cases is presented in Table 3, but these cases were exclud-ed from further analysis of the bypass cases.

AneurysmsThe aneurysms were deemed “complex” on the ba-

sis of preoperative imaging or previous surgical explora-tion. The size, morphology, and location of aneurysms were assessed by digital subtraction angiography (DSA) combined with CT, 3D CT angiography (CTA), or MRI. We reviewed the size and presence of intraaneurysmal

thrombus; the morphological characteristics, side, and lo-cation of the aneurysm; symptoms at presentation; previ-ous treatment procedures; and the presence of other an-eurysms (Tables 1 and 2). Aneurysm size was measured as the largest outer diameter for saccular aneurysms and as the length of the affected arterial segment for fusiform aneurysms.

The size of the 24 aneurysms ranged from 7 to 60 mm (mean 30, median 26). Fifteen patients had a giant aneurysm. Six of the aneurysms were larger than 4 cm and were causing mass effect. In 17 cases (71%), the aneu-rysms were partially thrombosed. There were 16 fusiform and 8 saccular aneurysms, as defined by their angiograph-ic morphology. Eleven aneurysms were on the right side, 13 on the left. The aneurysms were located in the M1 seg-ment in 7 patients, at the MCA bifurcation in 8, and more distally in 9. All M1 segment and distal MCA aneurysms

TABLE 1: Baseline characteristics in 24 patients*

Description Value

sex male 15 (63) female 9 (37)age (yrs) mean 46.5 range 12–73presenting symptom SAH 2 (8) seizure 10 (42) mass effect 3 (12) TIA 4 (17)  none (incidental finding) 5 (21)aneurysm location left side 13 (54) right side 11 (46) M1 segment 7 (29) bifurcation 8 (33) distal 9 (38)aneurysm characteristics saccular 8 (33) fusiform 16 (67) partially thrombosed 17 (71)aneurysm size <20 mm 3 (12) 20–24 mm 6 (25) 25–39 mm 9 (38) ≥40 mm 6 (25)previous aneurysm treatment attempts wrapping 1 (4) surgical exploration 2 (8) diverter stenting 1 (4)

* Values represent number of patients or aneurysms (%) unless other-wise indicated. TIA = transient ischemic attack.

L. Kivipelto et al.

400 J Neurosurg / Volume 120 / February 2014

TABL

E 2:

Clin

ical

sum

mar

y of p

atie

nts u

nder

goin

g a c

ombi

natio

n of

byp

ass a

nd ve

ssel

occlu

sion

for c

ompl

ex M

CA an

eury

sms*

Case

No

.

Age

(yrs)

, Se

xM

CA

Seg

Side

Aneu

rM

orph

Aneu

rSi

ze(m

m)Int

ralum

Thro

mbPr

ev Tx

Bypa

ss Ty

peAn

eur T

x

Bypa

ssPa

tent

Posto

pAd

d’l P

rocs

Stro

keFU (m

os)

mRS

Scor

eGO

S Sc

ore

Aneu

r Ob

lit

Bypa

ss

Paten

t at

FUPr

eop

FU

121

, MM 1

rtfu

sif20

−ST

A-M

CA ×

2dis

tal o

ccl

++

120

24

++

268

, FM 1

rtfu

sif22

−wr

appin

gEC

A-M

CA bi

f,

ELAN

Apr

ox oc

cl+

+12

02

4+

NA

347

, MM 1

ltfu

sif25

−IC

A-M 1

, ELA

NApr

ox oc

cl+

−76

00

5+

NA4

36, M

M 1lt

fusif

26+

STA-

MCA

dista

l occ

l+

−13

11

5+

NA5

48, M

M 1rt

fusif

40+

STA-

M 2pr

ox oc

cl (e

ndov

asc)

++

50

24

+NA

6†52

, MM 1

ltfu

sif50

+flow div

erter

STA-

MCA

dista

l occ

l+

evac

of po

stop h

ema-

toma;

aneu

r re-

secti

on

−1.5

46

1+

+

773

, MM 1

ltfu

sif60

+ST

A-M

CAre

secti

on+

+4

13

3+

NA8

48, M

biflt

sacc

7+

surg

explo

-

ratio

nST

A-M

CAcli

pping

& M

2 sac

ri-

 fice

+−

451

14

+−

948

, Mbif

rtsa

cc20

−ST

A-M

CAcli

pping

& M

2 sac

ri-

 fice

+−

360

15

+−

1040

, Mbif

rtsa

cc23

+ST

A-M

CAcli

pping

& M

2 sac

ri-

 fice

+−

240

05

++

1150

, Mbif

ltsa

cc30

+IC

A-M 2

, ELA

NA;

ST

A-M

CAdis

tal o

ccl; d

istal

oc

cl+

−26

00

5+

−

1245

, Fbif

rtsa

cc30

+ST

A-M

CA ×

2pr

ox oc

cl+

−57

11

5+

+

1322

, Mbif

rtsa

cc34

+ST

A-M

CA ×

2tra

pping

+−

531

15

++

1445

, Mbif

rtsa

cc35

+IC

A-M 2

, ELA

NAcli

pping

& M

2 sac

ri-

 fice

+VP

shun

t for H

C−

71

05

+NA

1537

, Fbif

rtsa

cc55

+ST

A-M

CAdis

tal o

ccl (o

ne M

2

prev

’ly th

rom

-

bose

d spo

nt)

+−

171

14

+−

1639

, Mdis

tal

rtfu

sif10

−ST

A-M

CAre

secti

on+

−76

10

5+

NA17

55, M

dista

lrt

fusif

10−

STA-

MCA

prox

occl

+−

320

05

++

1863

, Fdis

tal

ltfu

sif20

+ST

A-M

CAtra

pping

−−

21

15

+−

1952

, Fdis

tal

ltfu

sif21

+OA

-MCA

dista

l occ

l+

−52

23

4+

−

2012

, Fdis

tal

ltfu

sif25

−ST

A-M

CApr

ox oc

cl+

−28

01

4+

+

2159

, Fdis

tal

ltfu

sif25

+ST

A-M

CAdis

tal o

ccl

+−

20

05

++

2261

, Fdis

tal

ltfu

sif35

+su

rg ex

plo-

ra

tion

STA-

MCA

trapp

ing+

−31

10

5+

+

2324

, Mdis

tal

ltfu

sif40

+IC

A-M 2

, ELA

NAdis

tal o

ccl

−an

eur r

esec

tion

+12

00

5+

NA24

67, F

dista

llt

fusif

50+

STA-

MCA

× 2

rese

ction

++

60

33

++

* Ad

d’l =

addit

ional;

aneu

r = an

eury

sm; b

if = bi

furc

ation

; end

ovas

c = en

dova

scula

r; ev

ac =

evac

uatio

n; FU

= fo

llow-

up; fu

sif =

fusif

orm;

HC

= hy

droc

epha

lus; in

tralum

= in

tralum

inal; m

orph

= m

orph

ol-og

y; NA

= no

t app

licab

le; ob

lit =

oblite

ratio

n; oc

cl =

occlu

sion;

prev

= pr

eviou

s; pr

ev’ly

= pr

eviou

sly; p

rocs

= pr

oced

ures

; pro

x = pr

oxim

al; sa

cc =

sacc

ular;

seg =

segm

ent; s

pont

= sp

onta

neou

sly; s

urg

= su

rgica

l; thr

omb =

thro

mbus

; Tx =

trea

tmen

t; VP

= ve

ntricu

loper

itone

al; +

= ye

s; −

= no

.†

This

patie

nt die

d 6 w

eeks

after

surg

ery,

but h

is by

pass

was

open

and t

he an

eury

sm w

as oc

clude

d at th

e tim

e of h

is de

ath. (

See C

linica

l Out

com

e sec

tion f

or de

tails

.)

J Neurosurg / Volume 120 / February 2014

Bypass and vessel occlusion for complex MCA aneurysms

401

were fusiform, whereas all bifurcation aneurysms were saccular.

Two patients (Cases 3 and 16) presented initially with subarachnoid hemorrhage (SAH). Ten patients had epilep-tic seizures, 3 had symptoms of mass effect, and 4 had is-chemic symptoms; 5 aneurysms were incidental findings. One patient who presented with SAH (Case 16; Hunt and Hess Grade II, Fisher Grade 3) was treated on an emer-gency basis. Another patient whose condition was dete-riorating rapidly (Case 6) due to perianeurysmal bleeding and increasing mass affect from a giant MCA aneurysm was admitted and surgically treated urgently.

Two aneurysms had been surgically explored earlier and deemed unclippable (Cases 8 and 22). In 1 case (Case 2), the fusiform M1 aneurysm continued to grow despite being wrapped with cotton 7 years earlier as did another M1 fusiform giant aneurysm after flow diverter insertion 5 months before the bypass and vessel sacrifice procedure (Case 6). Four patients had multiple aneurysms: at the anterior communicating artery (Case 2), at the origin of the posterior inferior cerebellar artery (Case 8), and in the contralateral MCA (Cases 10 and 21). (The treatment of these additional aneurysms is not included in this paper.)

Surgical StrategyBypass type, aneurysm treatment procedures, graft

patency, aneurysm obliteration, postoperative complica-tions, and clinical outcome (mRS and GOS scores) were assessed by reviewing the imaging studies, radiology re-ports, clinical examination results, and in- and outpatient records.

The preliminary planning of surgical strategy—by-pass type and whether a proximal or distal parent vessel occlusion would be performed—was done preoperatively based on the angiographic findings. No preoperative flow measurements were performed. During surgery, after ex-ploration of the aneurysm and associated vessels, the de-tails of the surgical plan were confirmed or further modi-fied, if necessary. We did not perform electrophysiological monitoring of the patients during surgery.

Decisions about bypass type depended on the caliber of the superficial temporal artery (STA) and the location of the planned vessel occlusion (the expected flow de-mand). The estimation of the STA caliber was a subjec-tive visual assessment based on the preoperative DSA and CTA studies, confirmed by the cut flow measurements in-traoperatively. In most cases we preferred an STA-MCA bypass, if possible. For some aneurysms we performed an EC-IC or IC-IC bypass with the excimer laser–assisted nonocclusive anastomosis (ELANA) method with saphe-nous vein graft. Both the conventional STA-MCA6,29,49 and the ELANA bypass technique42–44 have been comprehen-sively described previously.

In the planning of the treatment protocol, the follow-ing principles were considered.

M1 Aneurysms. The flow deficit caused by M1 oc-clusion can be well replaced with an appropriate bypass distally, but complete trapping of an M1 aneurysmal seg-ment would occlude the lenticulostriate perforator orifices leading to basal ganglion infarction and permanent neuro-TA

BLE

3: C

linic

al su

mm

ary o

f pat

ient

s tre

ated

for a

com

plex

MCA

aneu

rysm

with

out t

he ai

d of

byp

ass d

ue to

intra

oper

ative

byp

ass f

ailur

e*

Age

(yrs)

, Se

xAn

eur

Loc

Aneu

rM

orph

Aneu

rSi

ze

(mm)

Intra

lumTh

romb

Pres

Prev Tx

Bypa

ssTy

pePo

ss R

easo

ns fo

r Byp

ass F

ailur

eAn

eur T

xSt

roke

Preo

p mR

SFU

mR

SGO

SAn

eur

Oblit

FU (mos

)

54, F

rt M 1

fusif

60+

mass

effec

t−

ECA-

M 2em

erg o

p; th

romb

osis

at pr

ox an

ast,

de

spite

sev’l

revs

1) th

romb

ect, c

lippin

g; 2)

de-

co

mpr c

ranie

ct Da

y 2+

42

4+

19

51, M

lt bif

sacc

30+

SAH

coilin

g × 3

ICA-

M 2,

EL

ANA

occl

of dis

tal (E

LANA

) ana

st de

spite

repe

ated r

evs;

size d

iscre

p btw

n

saph

vein

graf

t & M

CA br

anch

?

thro

mbec

t, clip

ping D

ay 3

+0

33

+19

61, F

lt dist

alfu

sif60

+Sz

STA-

MCA

by

pass

at oth

er

ho

sp

ECA-

M 2,

EL

ANA

occl

of dis

tal (E

LANA

) ana

st de

spite

repe

ated r

evs;

size d

iscre

p btw

n

saph

vein

graf

t & M

CA br

anch

?

thro

mbec

t, clip

ping D

ay 6

−0

24

− 4

42, F

rt dis

tal

fusif

3−

acute

SAH

+

ICH;

HH 5,

F 4

−ST

A-M

CAem

erg o

p; br

ain ed

ema d

ue to

seve

re

SA

H, di

ff co

nditio

ns &

tech

prob

s

thro

ugho

ut op

1) tra

pping

, ICH

evac

; 2) d

e-

co

mpr c

ranie

ct, IC

H re

-

evac

Day

2

+5

43

+41

* An

ast = anasto

mosis

; cranie

ct = craniec

tomy; decomp

r = decom

pressiv

e; diff = difficult; dis

crep = disc

repancy; em

erg = em

ergency; F = Fis

her g

rade; F

U = follow-up; H

H = Hu

nt and He

ss grade; 

hosp

= ho

spita

l; ICH

= int

race

rebr

al he

matom

a; loc

= loc

ation

; pos

s = po

ssibl

e; pr

es =

pres

enta

tion;

prob

s = pr

oblem

s; re

-eva

c = re

-eva

cuati

on; r

evs =

revis

ions;

saph

= sa

phen

ous;

sev’l

= se

vera

l; Sz

= se

izure

; tech

= te

chnic

al; th

romb

ect =

thro

mbec

tomy.

L. Kivipelto et al.

402 J Neurosurg / Volume 120 / February 2014

logical deficits. By occluding the M1 segment either proxi-mally or distally to the aneurysm, a flow alteration can be induced leading to aneurysm thrombosis with a flow channel to the perforating branches remaining.

MCA Bifurcation Aneurysms. These lesions can be treated by clipping the neck together with one of the M2 branches, protected with a bypass, while preserving the anterograde flow to the other M2 trunk, or by revascular-izing both M2 branches followed by proximal (distal M1 occlusion) or distal occlusion (both M2 branches distal to aneurysm). Trapping is also an option if no perforators originate at the bifurcation.

Distal MCA Aneurysms. For distal MCA aneurysms, distal revascularization followed by either proximal or distal parent artery occlusion will result in aneurysm thrombosis. Trapping is also possible, since no significant perforating branches usually originate from these distal segments.

Drug Treatment and AnesthesiaPreoperatively, patients were treated with antiplatelet

therapy (acetylsalicylic acid [ASA] 100 mg daily), and the medication was continued after surgery. If for some rea-son ASA therapy had not been started before surgery, 300 mg ASA was administered intravenously during surgery. Systemic heparin was not routinely used, but the surgi-cal field was generously flushed with heparinized saline throughout the surgery. Bypass procedures were per-formed under general anesthesia, following the principles of neuroanesthesia described in detail by Randell et al.32

Assessment of Bypass Patency and Aneurysm OcclusionIntraoperatively, the patency of the bypass was as-

sessed using direct blood flow measurement with an ul-trasonic flow probe (Charbel Micro-Flowprobe, Transonic Systems Inc.), DSA, indocyanine green video angiogra-phy, or a combination of these methods. Following com-pletion of the bypass, partial or total trapping of the parent artery or trapping followed by resection of the aneurysm was performed. DSA was performed in all patients be-tween the 1st and 3rd postoperative day. Aneurysm oblit-eration was regarded as complete if there was no residual contrast filling of the aneurysm.

ResultsThe details of surgical procedures performed are

summarized in Tables 2 and 4.

Bypass Type and Treatment of the AneurysmTwenty-one EC-IC and 4 IC-IC bypasses were per-

formed. The STA was used as donor in 19 cases, and the occipital artery (OA), in 1 case. The external carotid ar-tery (ECA, in 1 case) or intracranial internal carotid ar-tery (ICA, in 4 cases) served as donor with a saphenous vein graft used as a conduit in the 5 ELANA bypasses.

The bypass procedure was followed by parent artery partial occlusion in 14 cases: proximal occlusion in 6 pa-tients, distal occlusion in 8 patients (in 1 case the proximal

occlusion was performed endovascularly on the 1st post-operative day, all others were intraoperative clip occlu-sions); trapping in 3 patients; trapping with aneurysm re-section in another 3 patients. Four bifurcation aneurysms were clipped together with an incorporated M2 branch.

Two aneurysms, initially treated with distal occlusion, were trapped and resected in a second surgery (see Surgi-cal Outcome).

All M1 aneurysms were fusiform. Six EC-IC bypasses (5 STA-MCA, 1 ECA-MCA ELANA) and 1 IC-IC bypass (ICA-MCA ELANA) were constructed, followed by prox-imal occlusion in 3 patients and distal occlusion in another 3. One M1 aneurysm was trapped and resected.

All MCA bifurcation aneurysms were classified as saccular. Seven STA-MCA bypasses and 2 IC-IC bypass-es (ICA-MCA ELANA) were performed. Four aneurysms were clipped with sacrifice of one of the M2 branches (first revascularized with a bypass). Proximal occlusion was performed in 1 patient, distal occlusion in 2 patients, and trapping in 1 patient. One of the patients (Case 11) was operated on twice for a giant saccular bifurcation aneu-rysm: an IC-IC bypass was made followed by distal oc-clusion of the dominant M2 branch and the flow alteration

TABLE 4: Treatment characteristics and aneurysm location*

Aneurysm Location

Variable Total (%) M1 Bif Distal

bypass characteristicsall bypasses 25 (100) 7 9 9conventional 20 (80) 5 7 8ELANA 5 (20) 2 2 1EC-IC 21 (84) 6 7 8 STA-MCA 19 (76) 5 7 7 OA-MCA 1 (4) 1 ECA-MCA (ELANA) 1 (4) 1IC-IC 4 (16) 1 2 1 ICA-MCA (ELANA) 4 (16) 1 2 1bypass recipient artery M1 1 (4) 1 MCA bifurcation 1 (4) 1 M2 4 (16) 1 2 1 M3–M4 19 (76) 4 7 8

aneurysm treatment (24 aneurysms)partial trapping 14 (58) 6 3 5 proximal occlusion 6 (25) 3 1 2 distal occlusion 8 (33)* 3* 2 3*total trapping 6 (25) 1 1 4 trapping only 3 (12.5) 1 2 trapping & resection 3 (12.5) 1 2clipping, selective sacrifice of 1 M2 4 (17) 4

* Two aneurysms (1 M1 and 1 distal MCA segment aneurysm) were primarily treated with distal parent vessel occlusion (included in the numbers in this table) but later were trapped and resected in a second surgery. See text for details.

J Neurosurg / Volume 120 / February 2014

Bypass and vessel occlusion for complex MCA aneurysms

403

was expected to induce a gradual aneurysm thrombosis. However, as no signs of progressive aneurysm obliteration were detected, an STA-MCA bypass to the nondominant M2 region was performed 11 days later and the branch was occluded distal to the aneurysm.

Distal Aneurysms. All aneurysms distal to the bifur-cation were morphologically fusiform. They were treated with 8 EC-IC bypasses (7 STA-MCA, 1 OA-MCA) and 1 IC-IC bypass (ICA-MCA ELANA), followed by proximal occlusion in 2 patients, distal occlusion in 3, trapping in 2, and trapping and resection in another 2 patients.

Surgical OutcomeAt the end of surgery, the bypass was patent in all

patients (Table 2).In 2 patients with distal MCA aneurysms (Cases 18

and 23), a bypass occlusion was detected angiographically on the 1st postoperative day (early bypass patency rate 92%).

Postoperatively, 23 aneurysms (96%) were completely obliterated. A bypass for a giant fusiform M2 aneurysm (Case 23) became thrombosed on the 1st postoperative day, and brisk residual filling of the aneurysm was detect-ed. The patient underwent a second surgery, with trapping and resection of the aneurysm, 3 days later.

One patient (Case 6) underwent a second operation for evacuation of Sylvian fissure hematoma and resection of the giant aneurysm to relieve mass effect and deterio-rating clinical condition.

No perioperative aneurysm ruptures were encoun-tered.

During follow-up (mean 27 months, range 1.5–76 months, median 24 months) no sign of aneurysm recanali-zation was detected. The patency of the bypasses was not systematically assessed in long-term follow-up if no new ischemic symptoms occurred.

Clinical OutcomeOne patient died 6 weeks after surgery (the patient in

Case 6, who had a 5-cm M1 aneurysm and surrounding edema, with a preoperative mRS score of 4; Table 2), with severe brain edema and hemorrhage leading to herniation and death. His bypass was open and the aneurysm was occluded at the time of death.

Six patients (25%) had new neurological deficits, with ischemic lesions seen on postoperative CT scans. One of these patients recovered fully, but 5 (21%) had permanent symptoms (mild to moderate hemiparesis and dysphasia); 3 of the 5 patients remained independent. Vasospasm did not occur. Six postoperative hematomas (2 subdural, 4 intracerebral) were detected on routine postoperative CT scans, but only one needed evacuation. One patient with hydrocephalus needed a shunt. Two patients in whom both STA branches were used for bypass developed skin necro-sis around the surgical wound edges; one recovered with conservative treatment, one required skin grafting. Five patients had postoperative meningitis, 6 had pneumonia, and 1 had a deep venous thrombosis and pulmonary em-bolism.

The mean follow-up period was 27 months (range 1.5–76 months, median 24 months). The median mRS

score for all patients was 0 preoperatively and 1 at the latest follow-up. The preoperative median mRS scores for M1, bifurcation, and distal MCA aneurysms were 0, 1, and 0, respectively. The postoperative median mRS scores for M1, bifurcation, and distal MCA aneurysms were 2, 1, and 0, respectively. A good outcome (GOS score 5 or 4) was seen in 21 (88%) of 24 patients. Functional outcomes are summarized in Tables 2 and 5.

Illustrative CasesCase 3 (M1 Aneurysm)

A 47-year-old man presented to another hospital with an SAH 7 months before presenting to our institution. A fusiform aneurysm of the left M1 segment was found (Fig. 1 left), and the patient was subsequently referred to our hospital for consultation and treatment. The aneurysm was considered unclippable on the basis of the angiographic findings, and we estimated that a relatively high flow was needed to revascularize the entire MCA territory, with the revascularization to be followed by proximal or distal oc-clusion of the parent artery. A saphenous vein graft was harvested, and a left pterional craniotomy was performed and the sylvian fissure dissected. The large aneurysm and the M1—both distally and proximally to the fusiform an-eurysmal segment—were exposed. A platinum ring used in the ELANA technique was sutured onto the distal ICA together with a vein graft, and another ring and vein graft were sutured onto the distal M1. The laser arteriotomies were performed, and the proximal and distal sections of the vein graft were sutured in an end-to-end anastomosis. Because we had good access to the proximal end of the aneurysm, a proximal clip occlusion of the M1 adjacent to the origin of the fusiform segment was performed so that the retrograde flow from the bypass would maintain the patency of the perforating arteries originating from the aneurysmal segment. Postoperatively, the patient had tran-sient mild dysphasia, which resolved within a few days. Postoperative DSA demonstrated good blood flow in the bypass and distal MCA branches, with no filling of the aneurysm (Fig. 1 right).

Case 13 (MCA Bifurcation Aneurysm)A 22-year-old man had a motor vehicle accident, sus-

pected to be due to an epileptic seizure. On CT, CTA, and DSA (Fig. 2 left), a giant (outer diameter 35 mm) wide-necked and partially thrombosed (23 mm diameter of the filling part) aneurysm of the right MCA bifurcation was found, with the frontal and temporal M2 branches originating from the aneurysm sac. As both branches of the STA were robust, a double STA-MCA bypass was planned. The aneurysm and the M2 branches were ex-plored via a pterional craniotomy. By following the MCA branches, suitable M3/M4 arteries distal to the aneurysm were chosen from each M2 vascular tree as recipient sites. Two STA-MCA bypasses were constructed. As the short M1 segment was accessible, the aneurysm was trapped by clipping the M1 proximally to the aneurysm and both M2 segments as they exited the aneurysm wall. Excellent flow in the bypasses was detected with Flowmeter (Charbel

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404 J Neurosurg / Volume 120 / February 2014

Micro-Flowprobe, Transonic Systems Inc.): 25 ml/min before and 50 ml/min after trapping of the aneurysm from each STA conduit. On postoperative imaging, the MCA branches filled through the bypasses, and there was no filling of the aneurysm (Fig. 2 right). The patient remained neurologically intact.

Case 20 (Distal MCA Aneurysm)A 12-year-old girl was examined because of intense

headaches, and a fusiform left temporal M3 aneurysm with a diameter of 25 mm was identified (Fig. 3 A and B). An STA-MCA bypass combined with trapping or proxi-mal/distal parent artery occlusion was planned. After preparation of the robust frontal STA branch, a relatively large pterional craniotomy was performed, and the syl-vian fissure was opened. As the aneurysm was explored, branches originating from the side of the fusiform seg-ment not detected on DSA were identified, indicating that trapping would lead to infarction. The arteries distal to the aneurysm were located so far posteriorly that the cra-niotomy had to be extended to expose these distal vessels, one of which was selected as the STA-MCA bypass re-cipient. After completion of the end-to-side anastomosis, the parent M3 arterial segment was clipped immediately proximal to the fusiform segment. The flow of the bypass was 7 ml/min before the proximal occlusion of the M3 branch and 24 ml/min after occlusion. On the 4th postop-erative day the patient developed focal epileptic symptoms and antiepileptic medication was started. On postopera-tive CTA, the arteries distal to the aneurysm were filling through a patent bypass and no filling of the aneurysm was detected (Fig. 3C).

DiscussionThis is the first study to report on the treatment strate-

gies and treatment results for a series of complex MCA aneurysms requiring bypass surgery with an emphasis on the exact location (M1, bifurcation, and distal) of the an-eurysm. Complex MCA aneurysms that cannot be treated with conventional surgical techniques are very rare, espe-cially in high-volume centers like ours where microsurgi-cal experience is at a high level. These lesions represented only 1% of all MCA aneurysms treated at our institution. Our series of 24 cases in which patients were treated with the combination of bypass and parent vessel occlusion for MCA aneurysms is to our knowledge the largest such se-ries published. Our results, with a 4% mortality rate and a 21% permanent morbidity rate, compare well with those of previously reported smaller series. Complete aneurysm

obliteration was achieved in all cases and good clinical outcome (GOS score 4 or 5) in close to 90% of the pa-tients.

In the earlier publications, including 5 or more cases of complex MCA aneurysms treated with the combina-tion of bypass and vessel occlusion, the treatment-related mortality rates vary from 0% to 11% and morbidity from 4.9% to 50%2,19,23,31,34,36–38,46 (Table 6).

Kalani et al.23 published a series of 16 giant MCA an-eurysms treated with EC-IC bypass and vessel occlusion. A 75% aneurysm obliteration rate was achieved, with 0% mortality and 31% morbidity and excellent or good clini-cal outcome in 94% of cases. Seo et al.37 reported a 100% aneurysm obliteration rate in a series of 9 complex MCA aneurysms after revascularization followed by excision, clipping, or trapping of the aneurysm; there was an 11% mortality rate and 22% morbidity rate, with 67% rate of favorable clinical outcome. Twenty-two MCA aneurysms were treated with ELANA bypass by van Doormaal et al.46 with 5% perioperative mortality, 36% morbidity, and 77% favorable outcome. The complete aneurysm oblit-eration rate was not reported clearly. Sekhar et al.36 pub-lished a series of 7 complex MCA aneurysm cases with different reconstructive solutions, including direct branch reimplantation and various arterial interposition grafts, with excellent results (100% aneurysm obliteration rate, no mortality, 14% morbidity). Similar reconstructive tech-niques and IC-IC bypasses were described in a few larger series of cases of various complex cerebral aneurysms, including treatment of 9,2 5,31 and 1634 MCA aneurysms. A variety of surgical and endovascular techniques and combinations of these modalities were applied to treat 48 complex intracranial aneurysms, among them 7 MCA an-eurysms treated with the aid of bypass.19

Treatment PrinciplesAlthough clipping or thrombectomy combined with

clip reconstruction is usually the firstline treatment for

TABLE 5: Functional outcome for patients with complex MCA aneurysm treated with bypass–vessel occlusion technique

Aneurysm LocationPreop

Median mRSMedian mRS

at FU Median GOS

all aneurysms 0 1 5M1 segment 0 2 4bifurcation 1 1 5distal segments 0 0 5

Fig. 1. Case 3. Preoperative (left) and postoperative (right) antero-posterior DS angiograms. Digital subtraction angiography demonstrat-ed a giant fusiform aneurysm in the M1 segment of the left MCA in this 47-year-old man (left). An ELANA bypass from the ICA to the distal M1 with an interpositioned saphenous vein graft, followed by proximal clip occlusion of the M1 was performed. The postoperative angiogram (right) shows brisk anterograde filling of the distal MCA branches through the patent bypass and obliteration of the aneurysm.

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405

saccular MCA aneurysms,33 when applied to giant par-tially thrombosed aneurysms these methods do carry in-trinsic risks of arterial occlusion with ischemic sequelae. Giant fusiform aneurysms typically have a longitudinal or serpentine flow channel inside the thrombus,25 and the fusiform pathological segment often involves the entire circumference of the vessel wall, making these lesions unclippable. Wrapping of the aneurysm with cotton or other materials has been used as an alternative treatment for “unclippable” aneurysms, but this method is not con-sidered durable.7,13 The DeBakey vascular clamp–assisted clipping of giant aneurysms with a partially calcified ath-eromatic base has been described,28 and this method can facilitate direct clipping in some rare cases. If previously performed coil embolization or stent placement has failed, clipping may be impossible with the endovascular mate-rial inside the vessel or aneurysm lumen.

In the bypass-aided method, a bypass is first con-structed to feed the vascular tree beyond the aneurysm; this is followed by a selected procedure to obliterate the

aneurysm itself. Trapping of the aneurysm will give an immediate and definitive result by completely isolating the aneurysm from the circulation. Occluding the parent artery proximal to the aneurysm will reduce the intralu-minal pressure and induce thrombosis of the aneurysm. Occlusion of the parent vessel(s) distal to the aneurysm creates high resistance in the aneurysm, leading to stagna-tion of flow and intraluminal thrombosis.

Excision or resection of the aneurysm itself is rarely needed. Even the “super giant” MCA aneurysms (diam-eter ≥ 4 cm) can usually be left in place because once the turbulent flow in the aneurysm ceases, the aneurysm stops expanding, and the thrombosed mass may even decrease in size in the long run. However, sometimes the abrupt thrombosis of a giant aneurysm, together with the increas-ing edema caused by surgical manipulation of the brain, may lead to increasing mass effect, necessitating throm-bectomy and aneurysm resection for decompression.

Traditionally, the ultimate goal of treatment of com-plex and giant aneurysms has been exclusion of the aneu-rysm from the circulation. However, a complete occlusion of the aneurysm by clip closure, trapping, or endovascu-lar coiling should not always be an aim if perforating or distal branch arteries arise from the aneurysmal segment. Partial trapping and flow alteration to reduce flow or in-duce thrombosis may be adequate to improve the natural history of the aneurysm.19 Fair results have been reported for stent-assisted coiling of wide-necked aneurysms and partial coil-embolization of aneurysms with incorporat-ed branch origins.16,47 A case of a fusiform M1 aneurysm treated successfully with a flow-diverting stent without coiling was described by Pumar et al.30

Flow RequirementsThe full flow replacement required for the entire

MCA territory is 50 ± 25 ml/min.1 A robust STA or OA may have a flow capacity of up to 100 ml/min and can supply the whole MCA region. This kind of replacement flow is needed for treatment of an M1 aneurysm. When necessary, both STA branches may be anastomosed to two different M2 trunks (one to each) to treat an M1 or a bifurcation aneurysm. If only one M2 territory or a more distal branch territory is to be replaced, the flow demand

Fig. 2. Case 13. Preoperative (left) and postoperative (right) antero-posterior DS angiograms. Digital subtraction angiography performed in this 22-year-old man revealed a partially thrombosed giant MCA bifur-cation aneurysm on the right side (left panel). Both STA branches were used to make 2 bypasses, one to each M2 main trunk distal branch, and the aneurysm was then trapped with clips. Postoperative angiography (right) demonstrated the bypass supplying the distal MCA branches but no contrast filling of the aneurysm. 

Fig. 3. Case 20. Preoperative anteroposterior (A) and lateral (B) DS angiograms and postoperative CT angiogram (C). A giant fusiform aneurysm in the distal branch of the left MCA was seen in the anteroposterior (A) and lateral (B) DS angiograms obtained in a 12-year-old girl examined for severe headaches. An STA-MCA bypass was performed, followed by proximal clip occlusion of the parent artery. Postoperative CTA (C) demonstrated a patent bypass and no filling of the aneurysm.

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is relatively low, and an ordinary STA flow will be suf-ficient. However, if the STA is not available or appears inadequate, an EC-IC or IC-IC bypass with a venous or arterial interpositioned graft, side-to-side in situ anasto-mosis, branch reimplantation, or aneurysm excision with interpositioned grafting may be performed to achieve the desired revascularization.31,36

We applied the vein graft/ELANA method quite liberally during the years 2003–2004 after adopting the technique in Helsinki. However, we gradually withdrew from using the ELANA method for MCA aneurysms, as we found the technique quite complicated and usually not absolutely necessary because “high flow” bypass is rarely required in the MCA region in terms of flow demand. As the bypass flow is often less than 50 ml/min, a saphenous vein graft used in the ELANA technique may be prone to early occlusion due to relatively low, turbulent flow in a disproportionately large venous conduit.41 This may have been one reason for bypass occlusion among our pa-tients. In our more recent cases, we have no longer used the ELANA technique in bypasses for MCA aneurysms.

There is great variability in the anatomy and func-tionality of the leptomeningeal anastomoses of the cere-bral arterial territories.5,45 Although the MCA is generally considered an “end artery,” its various natural anastomot-ic connections may explain the interindividual variability of tolerance to MCA branch occlusions. Moreover, in-creasing flow in leptomeningeal collaterals can lead to de-creasing flow in the bypass, resulting in a delayed bypass occlusion with no or only mild neurological symptoms.46 This was also observed among our patients: the natural collaterals “take over” and eventually make the bypass unnecessary. Similar collateral variability exists also in the internal capsule and basal ganglion area and probably explains why certain patients suffered permanent deficits after M1 aneurysm treatment (in this study, unintentional occlusion of lenticulostriate perforators) while only tran-sient deficits were seen in some others, even after com-plete trapping of M1 aneurysms.19,37

Aneurysm ObliterationAneurysm obliteration was achieved effectively and

durably among our patients: no recanalization of aneu-rysms was detected during a mean follow-up of 27 months. Early retreatment to occlude the aneurysm was needed in only 1 case, in which the aneurysm continued filling briskly despite the distal clip occlusion, and we ended up partially resecting and clipping the aneurysm 3 days after the first surgery.

High recanalization rates (35%–87%) are encoun-tered after endovascular Guglielmi detachable coil em-bolization of large and giant aneurysms.18,27 Although uncommon, aneurysm regrowth and rupture have been reported after bypass and parent vessel occlusion,20,35 and we conclude that in cases in which complete trapping of the aneurysm has not been performed, lifelong follow-up of patients is indicated.

Clinical OutcomeAlthough the number of cases is low to make statis-

tical conclusions with respect to the different subgroups, we did observe that most of the significant clinical com-plications were associated with M1 segment aneurysms: 1 patient died and 4 (57%) of 7 patients had symptomatic brain infarctions with an increase in mRS score. Fortu-nately, 3 of these patients recovered to independent life despite their morbidity. Nevertheless, the median mRS score among the patients with M1 aneurysms increased from 0 preoperatively to 2 at the latest follow-up. In con-trast, there was no significant postoperative morbidity in the group of patients with bifurcation aneurysms. The 9 patients with a distal MCA aneurysm had a median mRS score of 0 both preoperatively and at follow-up. The pre-vious studies have not addressed the different subgroups of MCA aneurysms stratified by anatomical location, and therefore our observations cannot be compared with ear-lier published experience.

Three of the 4 patients who had a “super giant” aneu-

TABLE 6: Summary of publications on MCA aneurysms treated with bypass–vessel occlusion method*

Authors & YearNo. of Cases

EC-ICBypass

IC-IC Bypass

or Reconstr

Aneurysm Excision/Resection Clipping

Total Trapping

Partial Trapping

Aneur Oblit(%)

Bypass Patency

(%)Mortality

(%)Morbidity

(%)

Exc/ Good Recov

(%)FU

(yrs)

Anson et al., 1996 9 5 4 4 3 2 10 90 2.8Hoh et al., 2001 7 6 1 1 5 1 69 10 6 86Quiñones-Hinojosa & Lawton, 2005

5 5 3 100 80 0 0 100

Sekhar et al., 2005 7 7 5 2 100 100 0 14 100 5.5Van Doormaal et al., 2008

22 2 20 8 11 86 5 36 77 3.6

Sanai et al., 2009 16 7 9 98 91 0 5 90 3.4Shi et al., 2009 6 6 6 (endo-

vasc) 67 NA 0 50 83 2.6

Seo et al., 2009 9 7 2 4 3 2 100 NA 11 22 67 2.1Kalani et al., 2013 16 16 1 13 75 94 0 31 94 4.9

* Exc = excellent; reconstr = reconstruction; recov = recovery.

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rysm (diameter ≥ 4 cm) and underwent resection of the an-eurysm had an unfavorable outcome. Whether this was a consequence of manipulation of the already compromised brain or related to the nature of the pathology treated is not clear.

Three patients with M1 aneurysms suffered a periop-erative stroke due to perforating artery thrombosis despite a partial trapping. This complication could probably not have been prevented by choosing any other surgical meth-od. Whether a flow-diverting stent would have resulted in a better outcome by saving the perforators remains uncer-tain. In this study the fusiform M1 aneurysm (Case 6) in which a flow diverter had been deployed 5 months earlier continued growing, necessitating surgical treatment.

Suggestions for Treatment StrategiesWe propose slightly different treatment strategies and

principles for consideration, depending on the aneurysm’s location in the MCA vascular tree.

M1 Aneurysms. Complex M1 aneurysms are typically fusiform, and direct clipping or coil embolization is usu-ally not feasible. The aneurysmal segment often involves origins of vital lenticulostriate perforating arteries, further restricting the options for treating the aneurysm. Proximal or distal occlusion should be preferred to trapping. After performing the bypass, a flow alteration is induced by proximal or distal occlusion of the parent artery, aiming at aneurysm obliteration with preservation of flow in the perforating branches. It must be understood, however, that this kind of deliberate hemodynamic modification and thrombotic process may be unpredictable and still carries the risk of perforator occlusion.

Future development of flow diverters may provide useful treatment alternatives for M1 aneurysms, in par-ticular, with the objective of saving the perforators and reducing the shear stress on the aneurysm walls.

MCA Bifurcation Aneurysms. Complex MCA bifurca-tion aneurysms may be treated by clipping the neck to-gether with one of the incorporated M2 branches protected with a bypass, assuming that the inflow to the other M2 can be preserved. If this is not feasible, both M2 branches must be revascularized followed by proximal parent ar-tery occlusion (distal M1 occlusion) or distal occlusion (both M2 segments distal to the aneurysm). Trapping is also an option if no significant perforators arise from the base of the aneurysm.

Distal MCA Aneurysms. Complex aneurysms of M2 or more distal segments, when fusiform and large, can be treated by distal revascularization followed by occlusion of either the afferent or efferent parent vessel, resulting in aneurysm thrombosis. Trapping will give a definitive result immediately and is often feasible as perforating branches are rarely a problem.

ConclusionsSurgical treatment with bypass and occlusion method

of treating complex MCA aneurysms appears to result in durable, often definitive protection from hemorrhage and further aneurysm growth, with a mortality rate and

clinical outcome that are clearly superior to those associ-ated with the natural history of these difficult aneurysms. Partial trapping should be favored for M1 fusiform aneu-rysms, as vital perforating branches often originate in the aneurysmal segment wall.

Disclosure

The authors report no conflict of interest concerning the mate-rials or methods used in this study or the findings specified in this paper.

Author contributions to the study and manuscript preparation include the following. Conception and design: Kivipelto. Acquisition of data: Kivipelto, Meling. Analysis and interpretation of data: Kivi-pelto. Drafting the article: Kivipelto. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Kivipelto. Administrative/technical/material support: Hernesniemi. Study supervision: Kivipelto.

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Manuscript submitted April 12, 2013.Accepted August 10, 2013.Please include this information when citing this paper: published

online November 29, 2013; DOI: 10.3171/2013.10.JNS13738.Address correspondence to: Leena Kivipelto, M.D., Ph.D.,

De part ment of Neurosurgery, Helsinki University Hospital, Topeli-uksenkatu 5, 00260 Helsinki, Finland. email: leena.kivipelto@hus.fi.