394
Endovascular Hunterian Ligation
Christopher P. Kellner and Sean D. Lavine
Hunterian ligation is one of the oldest interventions for arterial
aneurysms; John Hunter first performed it with ligation of the
femoral artery to treat a popliteal aneurysm in 1785.1 More
recently, the development of endovascular techniques has made
it possible to completely occlude an artery intra-arterially, without
the need for surgical access. Because refinements in the endovas-
cular techniques used to treat cerebral aneurysms have continued
to broaden the scope of intracranial aneurysms that can be
repaired by embolization or flow diversion, hunterian ligation is
more frequently relied on as a last resort to treat only aneurysms
that are the most surgically inaccessible and cannot be stented.
Historically, hunterian ligation has entailed the permanent sacri-
fice of a parent artery to prevent access of blood to the aneurysm.
This technique has also been referred to as “deconstructive”
therapy, in contrast to “reconstructive” therapy, which refers to
the targeted occlusion of a vascular abnormality without impair-
ment of blood flow in the parent vessel. With the ongoing devel-
opment of flow diverters, hunterian ligation has become even less
common because of the newfound ability to stent over the aneu-
rysm neck while, in most cases, adjacent perforators are preserved
and the parent vessel is reconstructed. The niche remaining for
vessel sacrifice includes highly complex fusiform aneurysms, as
well as a wide range of other cerebrovascular entities, including
hemorrhagic stroke, vascular tumors, arteriovenous malforma-
tions, fistulas, and arterial dissections.
HISTORY
John Hunter’s arterial sacrifice was first applied to the cerebral
vasculature in 1804 by John Abernethy as he unsuccessfully
attempted to ligate the carotid artery in a case of posttraumatic
dissection of the carotid artery. His pioneering attempt resulted
in a stroke in the patient. The first successful carotid ligation was
performed by Sir Astley Cooper in 1808. Only a year later, Victor
Horsley successfully ligated the common carotid to treat a giant
internal carotid artery (ICA) aneurysm. Ligation of either the
common carotid artery or the ICA was a common form of treat-
ment of ruptured aneurysms until the late 1960s.1 Various
methods of occlusion (gradual or abrupt) were used. In addition,
special clamps were developed that allowed treatment while
patients were awake so that if neurological impairment occurred
with gradual occlusion, flow could be restored rapidly.1-4 In ret-
rospect, by today’s standards, carotid ligation appears to be an
inelegant treatment. Nevertheless, it was found to be effective in
preventing rebleeding over the short term (6 months) in a ran-
domized trial in which abrupt common carotid occlusion was
compared with bed rest in patients with ruptured posterior
communicating aneurysms.3 Subsequently, long-term (≈10-year)
follow-up of these patients revealed that the protection against
rebleeding was lost; long-term rebleeding rates were the same
both in patients who had undergone ligation and in those who
were assigned bed rest.5
Intracranial access would have to wait, however, until neuro-
surgical techniques dramatically improved, and it was not until
1945 that James L. Poppen became the first to document intra-
cranial ligation of the vertebral artery to treat an aneurysm. In
1962, the basilar artery was ligated proximally by Mount and
Taveras.6 Without the ability to predict which patients could
tolerate proximal arterial occlusion, however, favorable outcome
was a matter of chance. Development of the Drake tourniquet
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394
enabled the surgeon to temporarily occlude an artery the day
after surgery, when the patient had fully recovered from anesthe-
sia, and therefore observe whether sacrifice of the parent vessel
could be tolerated. In Drake’s7 original study, occlusion of the
basilar or vertebral artery in 14 patients was strikingly successful:
7 of these patients had a favorable neurologic outcome.7 Open
ligation of the carotid or vertebral arteries, however, was slowly
replaced by reconstructive techniques for most aneurysms as
intracranial microsurgery fully matured. Since the development
of endovascular balloons in the early 1990s, parent vessel occlu-
sion has become possible through transfemoral access. Further
development of endovascular coils has increased the efficacy and
expanded the indications for endovascular permanent occlusion.
INDICATIONS
Endovascular hunterian ligation today is reserved primarily for
giant and fusiform aneurysms. Certain traumatic pseudoaneu-
rysms and infectious aneurysms in which the risk associated with
endovascular intervention is high may also be good candidates.8
The most complex aneurysms cannot be treated either by con-
ventional surgical clipping or by endovascular coiling; thus the
rationale for the technique, as well as the evidence supporting its
practice, is based predominantly on observational data from case
series and individual reports.8 Although it would be ideal to
exclude the lesion from the cerebral circulation and maintain
blood flow through the parent artery, such reconstructive methods
cannot be used for all aneurysms because of their shape and loca-
tion. In 1975, Drake7 postulated that as many as two thirds of
giant intracranial aneurysms may not be amenable to clip recon-
struction because of their location or structure. This number,
however, continues to shrink because of improving endovascular
technology. When hunterian ligation is considered, the major
treatment question is whether to attempt placing a flow-diverting
stent and, if that is either too risky or technically impossible,
whether to perform an arterial bypass before permanent vessel
occlusion. The current standard of care requires preoperative
evaluation with balloon test occlusion (BTO), followed by clinical
and radiologic assessment of distal perfusion.
Although BTO may result in no symptoms, there are other
general contraindications to sacrifice of the parent vessel; the
major example is subarachnoid hemorrhage, in which even mod-
erate vasospasm can decrease blood flow to the distal vasculature
and increase the risk for delayed ischemic neurological deficits.
Whenever possible, complex ruptured aneurysms that necessitate
hunterian ligation are treated in a delayed manner or with tem-
porized treatment with a partially occlusive strategy such as dome
coiling.
The exact algorithm for assessing cerebrovascular reserve
before endovascular hunterian ligation varies among institutions.
Some surgeons advocate a universal reconstructive approach with
either bypass in all cases of vessel sacrifice or placement of
flow-diverting stents, whereas others perform selective bypass,
followed by endovascular hunterian ligation. Because of the com-
plexities and high degree of risk associated with an extracranial-
intracranial cerebral artery bypass, especially when large vein or
radial artery grafts are employed for hemispheric flow replace-
ment, patients able to tolerate vessel sacrifice should be at
least considered for hunterian ligation alone. There are currently
no comparison data regarding the long-term morbidity and
3383
 CHAPTER 394  Endovascular Hunterian Ligation 3383.e1

KEY WORDS
394
hunterian ligation
arterial aneurysm
cerebral vasculature

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3384 SECTION 12  Vascular
mortality with hunterian ligation with and without adjuvant
extracranial-intracranial bypass in patients assessed with either
angiography or BTO. Because of the ever-shrinking number of
extremely complex aneurysms in which no microsurgical or
endovascular reconstructive option is feasible, these data are
unlikely to be forthcoming, and each multidisciplinary team will
be forced to make management decisions on a case-by-case basis.
Whenever vessel occlusion is being considered, a patient should
undergo cerebral reserve testing (CRT) to evaluate distal perfu-
sion during and after a test occlusion. If CRT proves that col-
lateral flow is not sufficient, bypass is necessary before permanent
occlusion to prevent ischemic stroke. Both the approach to CRT
and the form in which it is performed can vary significantly
among institutions. Most groups report a protocol that involves
a combination of tests: BTO in conjunction with clinical neuro-
logical evaluation, neurophysiologic monitoring, angiography
and assessment of cerebral hemodynamic perfusion (e.g., single-
photon emission computed tomography), and provocative mea-
sures such as a hypotensive challenge.
APPROACHES TO THE OCCLUSION
OF SPECIFIC CEREBRAL VESSELS
The Internal Carotid Arteries
Because of the surgical inaccessibility of portions of its course
and the robust circulation of the circle of Willis, the ICA is the
vessel most commonly treated with either open or endovascular
occlusion. Although ICA sacrifice is performed predominantly
for lesions of the ICA itself, it may be considered for complex
lesions of the anterior cerebral artery (ACA) or middle cerebral
artery (MCA) as well. Larson and colleagues,8a in their descrip-
tion of 58 permanent occlusion procedures performed on the
ICA over a period of 15 years, described aneurysms in multiple
locations: 40 intracavernous, 5 petrous carotid, 3 cervical carotid,
and 10 ophthalmic segment aneurysms. BTO was used in all
cases, and extracranial-intracranial bypass was performed when
deemed necessary after provocative testing. Outcomes were
reported at a mean follow-up interval of 76 months: three patients
(5%) died during treatment, six (10%) developed transient ische­
mia, two (3%) developed delayed infarction, and in one patient,
the aneurysms enlarged after endovascular occlusion, ultimately
necessitating surgical clipping.
Certain types of ICA aneurysms elude coiling by current tech-
nology and are at high risk for complications during surgery, and
although they are amenable to flow-diverting stents, permanent
occlusion may be a better solution in patients for whom antiplate-
let agents are contraindicated. In 2007, Park and coauthors9
reported 12 patients with blood blister–like aneurysms of the ICA,
of whom 7 were treated with conventional endovascular coiling
or stent-assisted coiling and 5 with BTO and endovascular trap-
ping, which consisted of permanent parent vessel occlusion both
proximally and distally to prevent arterial backwards flow. The 7
patients treated with coiling demonstrated aneurysm regrowth,
and 3 suffered rebleeding with severe morbidity. All 5 patients
treated with permanent occlusion had an excellent neurological
outcome. With appropriate neurological testing, permanent
occlusion of the ICA can be an important treatment modality that
may even be the preferred intervention in selected cases.
Researchers have evaluated a new endovascular vascular plug
(Amplatzer) for performing ICA parent vessel occlusion.10-12 The
vascular plug is a self-expanding nitinol wire mesh that can be
used independently or in conjunction with coiling, at which point
it would act as an anchor on which the coil could be deployed.
In 2013, Mihlon and colleagues12 reported successful and safe use
of the device in eight patients. They noted that advantages over
coiling alone included (1) more rapid vessel occlusion, which
would theoretically decrease the time during which there is
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partial occlusion and resultant sluggish flow and thus potentially
decrease the risk of thromboembolism, and (2) the need for fewer
coils to achieve vascular occlusion. In many cases, the vessel could
be completely occluded with one or two Amplatzer plugs; one
patient required a total of six. Further studies are needed to evalu-
ate the device’s utility, cost-effectiveness, durability, and long-
term efficacy, and it is important to understand that use of this
device in the cervical vessels is outside its current FDA-approved
indications.
The Vertebrobasilar Circulation
Ligation of the vertebrobasilar circulation for a known vertebral
artery lesion appears to have first been performed by Poppen13,14
in 1945. Vertebral artery ligation, both unilateral and bilateral, was
used by Drake7 in 1975 to treat large vertebral or basilar artery
aneurysms in 14 patients. With stricter patient selection and the
development of endovascular techniques, patient outcomes have
improved significantly enough to justify permanent occlusion of
the vertebral artery in the proximal posterior circulation.
In 1991, Aymard and associates15 reported unilateral or bilat-
eral endovascular hunterian ligation of the vertebral artery in 21
patients: 13 patients were neurologically normal at follow-up,
including 1 patient who suffered transient stroke symptoms; 6
had partial aneurysm thrombosis; 1 had no thrombosis; and 1
died. Because of this high rate of morbidity and mortality, the
authors advocated strict preoperative CRT. An important contri-
bution of this study was the authors’ observation that in most
cases, occlusion of the vertebral artery was most effective at the
level of C1 because antegrade collateral flow is possible through
the external carotid artery16; however, too much collateral flow
can prevent aneurysmal thrombosis. Halbach and coauthors17
published a series of 15 patients who underwent proximal per-
manent occlusion for vertebral artery vascular pathology and had
improved outcomes.
Collateral backwards flow from the opposite vertebral artery
and the circle of Willis makes endovascular trapping an attractive
treatment option for some vertebral artery lesions.18,19 Double
microcoil trapping after BTO of the vertebral artery proximal to
the aneurysm was performed on 11 patients suffering subarach-
noid hemorrhage from dissecting vertebral artery aneurysms. As
previously mentioned, this technique simultaneously occludes the
parent vessel proximal and distal to the vascular lesion. In their
11 patients, Kai and colleagues19 reported good neurological
outcome with only one transient adverse result. In select cases
with robust fetal circulation, surgical clipping of the basilar artery
has been described in the treatment of fusiform basilar aneu-
rysms. In a study of 15 patients, Kellner and colleagues20 demon-
strated that point occlusion of the basilar artery could be
performed without impairment of brainstem perforators and
while collateral blood flow to the posterior circulation vessels was
maintained.
Aneurysms involving the origin of the posterior inferior cer-
ebellar artery (PICA) raise important concerns that can guide
favorable management options (Fig. 394-1). Iihara and cowork-
ers18 proposed a treatment algorithm in which they suggested
that certain strategies could be used, depending on the relation-
ship between the origin of PICA and the aneurysm sac. They
proposed that if the aneurysm is separate from the origin of
PICA, internal occlusion should be the recommended treatment.
For an aneurysm involving the origin of PICA and manifested as
subarachnoid hemorrhage, the suggested treatment is proximal
occlusion and internal trapping. If the aneurysm incorporates the
origin of PICA and does not involve subarachnoid hemorrhage,
BTO should be performed, followed by occipital artery–PICA
bypass. For the authors of the case series of 18 patients, the
algorithm resulted in a favorable morbidity rate of 17% with no
instances of PICA infarction and no deaths.18
 CHAPTER 394  Endovascular Hunterian Ligation 3385

394

A B C

D E F
Figure 394-1. Subarachnoid hemorrhage and dissecting aneurysm.While sitting at her kitchen table, a
59-year-old woman had an acute onset of the worst headache of her life, accompanied by severe neck pain.
Subarachnoid hemorrhage (arrow) was visible on the initial computed tomographic (CT) scan (A). A left
vertebral dissecting aneurysm (arrows) proximal to the posterior inferior cerebellar artery (PICA) was seen on
CT angiography and conventional angiography (B to D). Endovascular left vertebral sacrifice with preservation
of PICA was performed (E, arrow) without retrograde filling of the aneurysm from the contralateral vertebral
artery (F, arrow).

In 1991, Hodes and coworkers22 described five successful

The Distal Circulation
The ACA, MCA, and posterior cerebral artery are distal to the
collateral circulation of the circle of Willis; however, because of
collateral flow through leptomeningeal vessels, permanent occlu-
sion in the distal circulation is possible. In their anterior circula-
tion case series published in 1994, Drake and coworkers21
described 29 cases of surgical hunterian ligation and bypass as a
treatment strategy for distal aneurysms involving the ACA and
MCA. In 4 of the 29 patients, the bypass failed, but none of these
patients suffered postoperative morbidity because of the robust
collateral flow that filled the M2 segment of the MCA. In 1
patient, these collateral vessels were demonstrated on angiogra-
phy to provide retrograde flow to the thrombosed aneurysm. In 2
of the patients treated for ACA aneurysms, complete thrombosis
of the ACA resulted in death or severe neurological morbidity.
attempts at hunterian ligation in the distal circulation, including
three M1 aneurysms, one M3 aneurysm, and one A1 aneurysm.
At least two case series have emerged describing the distal pos-
terior circulation. Arat and colleagues23 reported eight endovas-
cular procedures performed for aneurysms of the posterior
cerebral artery with a 12.5% morbidity rate, and Xavier and
coauthors24 reported three cases of P2 fusiform aneurysms treated
by endovascular permanent occlusion with no morbidity. Mycotic
aneurysms have a predilection for the distal circulation and have
also been treated with endovascular permanent occlusion; in one
study, 12 patients underwent the procedure with no postoperative
morbidity or mortality related to the operation.25,26
One of the principal controversies surrounding distal circula-
tion sacrifice is the need for distal PICA bypass in cases in
which PICA alone is deconstructed either microsurgically or

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3386 SECTION 12  Vascular
endovascularly. Because delayed cerebellar infarction is clinically
almost unheard of and largely unreported and the fact that brain-
stem perforators generally do not give off anything but the most
proximal PICA and in fact are often collateralized, the indications
for PICA-PICA bypass remains quite variable from institution to
institution and patient to patient.
CEREBRAL RESERVE TESTING
In nearly all cases of endovascular hunterian ligation, it is crucial
to preevaluate the effect of parent artery occlusion by temporary
inflation of an intra-arterial balloon. The patient’s ability to pass
this test is difficult to predict beforehand and depends primarily
on collateral blood flow, location, and the possibility of prior
damage to the area in question. Previous cerebrovascular disease
can increase collateral flow through hypoxia and induced angio-
genesis. Patients with moyamoya disease, arteriovenous shunting,
congenital abnormalities, and even prior transient ischemic
attacks show evidence of increased collateral circulation.
The first test occlusion was performed by Matas27 and Carrol
Allen in 1911, who advocated 20 to 30 minutes of carotid occlu-
sion percutaneously or after surgical exposure, with the use of
local anesthesia. This preliminary testing became known as the
Matas test, but it was widely thought to lack sensitivity because
it was difficult to effectively occlude the carotid artery fully for
such a long time when it was attempted percutaneously. The
modern endovascular version of this test has been extensively
evaluated in the literature. In 2000, van Rooij and colleagues28
showed that of 17 patients who successfully passed BTO and
subsequently underwent endovascular hunterian ligation, none
experienced complications.
There are many variations of the BTO protocol, ranging from
brief balloon inflation to an array of CRT and imaging under
various conditions. Initially, some patients were found to experi-
ence morbidity after permanent occlusion even though BTO had
produced no symptoms. Subsequently, additional testing included
a hypotensive challenge.29 In this procedure, BTO is performed
for 20 to 30 minutes, a neurological examination is conducted
every 5 minutes, and then mean arterial blood pressure is phar-
macologically reduced to 66% of the patient’s baseline and main-
tained at that level for 20 minutes. The addition of a hypotensive
challenge improved the sensitivity of CRT. Standard and associ-
ates30 showed that this testing reduced the rates of morbidity and
mortality associated with permanent occlusion to less than 5%.
A wide variety of adjunctive testing is currently available to
accompany BTO. These techniques include encephalography,
neurophysiologic monitoring, stump pressure evaluation, near-
infrared spectroscopy, transcranial Doppler ultrasonography,
technetium 99m–hexamethylpropyleneamine oxime (HMPAO)
single-photon emission computed tomography, positron emis-
sion tomography, stable xenon-labeled computed tomography
(Xe-CT), and patient-specific computer modeling.31-36 Synchro-
nous venous filling (<0.5-second delay) demonstrated on angiog-
raphy and on Xe-CT has also been correlated with increased
success after endovascular hunterian ligation.
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COMPLICATIONS
Lesions for which hunterian ligation is required are among the
most difficult to treat with common treatment modalities, and
their treatment is therefore more likely to have poor neurological
outcomes overall. The most common complication after endo-
vascular permanent occlusion is, of course, ischemic stroke. Post-
occlusion thromboembolism, coil migration, secondary aneurysm
development, and perforator occlusion can also occur.14,37,38 As
described earlier, enormous effort is being invested in minimizing
these complications through extensive preoperative hemody-
namic testing. In 1966, Nishioka39 reported a complication rate
of 10% among 160 patients and cited ischemic infarction in only
2 of those patients. Advances in preoperative testing, patient
selection, and endovascular occlusion techniques continue to
improve endovascular results as does the coadministration of
antiplatelet therapy in selected patients. In 2000, van Rooij and
colleagues28 reported no complications in 17 patients, and in 2005,
Abud and colleagues40 reported no complications in 60 patients
who underwent endovascular permanent occlusion of the ICA.
CONCLUSION
Endovascular hunterian ligation continues to be an important
technique in the treatment of extremely complex aneurysms
ineligible for surgical clipping, coil embolization, or endovascular
flow diversion. Preoperative CRT is generally thought to be
crucial, except when distal-bypass is already planned, and gener-
ally consists of BTO with a hypotensive challenge; adjunctive
maneuvers vary by institution. With appropriate patient selection
and preoperative testing, endovascular hunterian ligation can be
a safe and effective treatment modality for complex intracranial
vascular lesions. As the technology of flow-diverting devices
improves, vessel sacrifice will be necessary in fewer patients.
SUGGESTED READINGS
Drake CG, Peerless SJ, Ferguson GG. Hunterian proximal arterial occlu-
sion for giant aneurysms of the carotid circulation. J Neurosurg.
1994;81:656.
Hodes JE, Aymard A, Gobin YP, et al. Endovascular occlusion of intra-
cranial vessels for curative treatment of unclippable aneurysms: report
of 16 cases. J Neurosurg. 1991;75:694.
Matas RI. Testing the efficiency of the collateral circulation as a prelimi-
nary to the occlusion of the great surgical arteries. Ann Surg. 1911;53:1.
Polevaya NV, Kalani MY, Steinberg GK, et al. The transition from hun-
terian ligation to intracranial aneurysm clips: a historical perspective.
Neurosurg Focus. 2006;20(6):E3.
van Rooij WJ, Sluzewski M, Slob MJ, et al. Predictive value of angio-
graphic testing for tolerance to therapeutic occlusion of the carotid
artery. AJNR Am J Neuroradiol. 2005;26:175.
Winn HR, Richardson AE, Jane JA. Late morbidity and mortality of
common carotid ligation for posterior communicating aneurysms. A
comparison to conservative treatment. J Neurosurg. 1977;47:727.
See a full reference list on ExpertConsult.com

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