Accepted Manuscript

History, Evolution and Continuing Innovations of Intracranial Aneurysm Surgery

Leon T. Lai, MBBS, PhD, FRACS, Anthea H. ONeill, MPH

PII: S1878-8750(17)30166-3
DOI: 10.1016/j.wneu.2017.02.006
Reference: WNEU 5237

To appear in: World Neurosurgery

Received Date: 4 December 2016

Revised Date: 30 January 2017
Accepted Date: 1 February 2017

Please cite this article as: Lai LT, ONeill AH, History, Evolution and Continuing Innovations of
Intracranial Aneurysm Surgery, World Neurosurgery (2017), doi: 10.1016/j.wneu.2017.02.006.

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Title: History, Evolution and Continuing Innovations of Intracranial Aneurysm

Surgery

Authors: Leon T Lai,1,2,3 MBBS, PhD, FRACS; Anthea H ONeill,3,4 MPH

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Department of Neurosurgery, Monash Health, Melbourne, Australia

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Department of Surgery, Monash University, Melbourne, Australia

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Monash Neurovascular Institute, Melbourne, Australia

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Faculty of Medicine, Nursing and Health Sciences, Monash University, Melbourne,

Victoria, Australia
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Corresponding Author
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Leon Tat Lai, MBBS, PhD, FRACS

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Department of Neurosurgery
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Monash Health, Melbourne, Australia

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Email: leon.lai@monashhealth.org

Key Words: History, intracranial aneurysm, microsurgery, surgery

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Abbreviations: ACoA, anterior communicating artery; CCA, common carotid artery; CSF,

cerebrospinal fluid; ICA, internal carotid artery; ICG, indocyanine green; LSO, lateral

supraorbital; MCA, middle cerebral artery; NIR, near infrared; PCoA, posterior

communicating artery; PICA, posterior inferior cerebellar artery; STA, superficial temporal

artery

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Running Title: Evolution of aneurysm surgery

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Disclosure: The authors declare that they have no financial or other conflicts of interest in
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relation to this research and its publication. This research did not receive any specific grants

from funding agencies in the public, commercial, or not-for-profit sectors.

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Abstract

Evolution in the surgical treatment of intracranial aneurysms is driven by the need to refine

and innovate. From an early application of the Hunterian carotid ligation to modern-day

sophisticated aneurysm clip designs, progress was made through dedication and technical

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maturation of the cerebrovascular neurosurgeons to overcome challenges in their practices.

The global expansion of endovascular services has challenged the existence of aneurysm

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surgery, changing the complexity of aneurysm case mix and volume that are presently

referred for surgical repair. Concepts of how to best treat intracranial aneurysms have

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evolved over generations, and will continue to do so with further technological innovations.

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As with the evolution of any type of surgery, innovations frequently arise from the criticism
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of currently available techniques.
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Introduction

Technological advancement has facilitated cerebrovascular neurosurgeons to address the

broad spectrum of vascular disorders affecting the central nervous system. The development

of intracranial aneurysm surgery has benefited from these innovations. The origin of modern

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aneurysm surgery was established when the first silver clip was placed on the neck of an

intracranial aneurysm in 1936.1-3 However, the foundations upon which these operative

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principles were laid had been developed many generations back. The current study examined

key historical landmarks that have shaped the way aneurysm surgery is practiced in the

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contemporary era.

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The Hunterian Principle of Carotid Artery Ligation
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The first transformative concept in the surgical treatment of intracranial aneurysms was based

on the Hunterian principle of proximal ligation of the feeding artery. John Hunter (1728-
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1793), the Scottish scientist and surgeon, first described this technique in 1748 when he
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induced thrombosis within the aneurysm in the peripheral arteries.4,5 When Astley Paston
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Cooper (1768-1841) of London applied this technique to treat a cervical aneurysm in 1805,

the patient became hemiplegic and died a few weeks later.6 In 1808, Cooper persisted on a
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second attempt and successfully treated a pulsating tumor at the angle of the jaw.7 Figure 1
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outlines the key milestones in the surgical evolution of intracranial aneurysms since this

period to the present day.

Early reports of aneurysm exposure were only made through serendipitous discovery during

the surgical approach for other intracranial pathologies. Victor Horsley (1857-1916) was

among the first to report on these findings. In 1885, Horsley reported a giant internal carotid

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artery (ICA) aneurysm that was compressing the optic chiasm, which he treated using

bilateral cervical carotid artery occlusion.2,8,9 Horsley later performed a carotid ligation

procedure in 1902 when he operated on a presumed middle fossa tumor that was in fact

discovered to be an ICA aneurysm upon surgical exposure.10

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Despite the overall skepticism of many surgeons at the time, proximal carotid ligation gave

the early cerebrovascular pioneers, for the first time, a treatment option for intracranial

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aneurysms.11 Over time, this technique was refined. In 1905, William Halsted (1852-1922)

promoted the idea of fractional ligation, in which gradual stricture of the carotid artery was

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performed in order to minimize surgical morbidity.12 This gave rise to the invention of the

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Dott, Crutchfield, Selverstone, Kindt and Drake vascular clamps or tourniquets (among
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others), which enabled surgeons to place the clamp across the artery and to gradually ligate

them over a period of days.13-17

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Many surgeons, however, remained doubtful of the therapeutic relevance of proximal carotid
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ligation for cerebral aneurysms. Throughout the mid-1900s, original research and reviews of
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the literature demonstrated that carotid ligature carried a high risk of operative morbidity and

mortality.18-20 The rate of aneurysm obliteration was low, with success often limited to ICA
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aneurysms.18-21 Winns report in 1977 established no difference in the rate of re-hemorrhage

for those aneurysms that were treated by carotid ligation as compared to those that were
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managed conservatively.22
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Extending the Hunterian Principle to Surgical Trapping of Intracranial Aneurysms

In 1932, Axel Herbert Olivecrona (1891-1980) performed the first successful unplanned

surgical trapping and excision of a large posterior inferior cerebellar artery (PICA)

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aneurysm.23,24 Based on this principle, Walter Edward Dandy (1886-1946) successfully

trapped a cavernous sinus aneurysm in 1935 by ligating the ICA within the neck, and then

intracranially.25 Dandy was also credited for performing the first vertebral artery ligation

beneath the atlas to treat a vertebral aneurysm in 1944.21 In 1948, Henry Schwartz described

his experience with a direct surgical approach to a large basilar artery aneurysm, which he

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successfully trapped using silver clips.26 Further, in 1956, Logue ligated the proximal

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dominant anterior cerebral artery in patients with ruptured anterior communicating artery

(ACoA) aneurysms.27 Later, Tindall and Odom described the ligation of the contralateral ICA

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in the neck to assist in aneurysm thrombosis in patients with ruptured ACoA aneurysms.28

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The Beginning of Direct Surgery on Intracranial Aneurysms
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The technology available in the 1930s made direct surgery on intracranial aneurysms a

significant undertaking. Ligatures and silver clips were the only devices developed at the
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time that were available in the cerebrovascular neurosurgeons armamentarium. The ability to
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maintain hemostasis in the event of aneurysm rupture was limited. Frustrated by the

outcomes of Hunterian carotid ligation, Sir Norman McComish Dott (1897-1973) in 1931
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planned and successfully treated a ruptured intracranial aneurysm by direct exposure and
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wrap reinforcement with muscle taken from the patients thigh - a technique that he might
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have acquired from Harvey Williams Cushing (1869-1939) during his residency in 1923 and

1924.2,29,30 In a monograph published in 1925, Cushing had already reported the use of

muscle to pack and wrap an intracranial aneurysm, combining this treatment with cervical

carotid artery ligation during surgery for a suspected tumor in the region of the Gasserian

ganglion.31

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Dott had already recognized that most aneurysms were located at arterial junction points and

associated with vessel wall weakness.29,32 He advocated for conservative treatment for many

anterior circulation aneurysms, but recommended carotid artery ligation for aneurysms

located proximal to the circle of Willis, and direct operative exposure and application of

muscle for those distal to the circle of Willis.29,32

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During this period, other surgeons had also established their experience with direct surgery

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on aneurysms using muscle wrap reinforcement techniques.33-36 In 1934, Wilhelm Tonnis

(1898-1978) split the corpus callosum to cover the surface of an ACoA aneurysm with a

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piece of muscle.33 Similarly, in Ireland in 1936, Adams McConnell (1884-1972) opened a

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subchiasmal ICA aneurysm and packed it with muscle.34 The patients vision was
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subsequently restored. Dutton and Selverstone introduced wrapping as a routine method for

treating intracranial aneurysms that were difficult and not amenable to direct clip ligation.35,36
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The Birth of Surgical Clipping of Intracranial Aneurysms

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In 1911, Harvey Cushing described the use of the silver clips to occlude when a ligature
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could not be made to encircle the vessel.37 However, it was not until 1937 that Dandy made

use of these clips to perform the first planned surgical neck ligation of a saccular intracranial
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aneurysm. On 16 February 1937, a 43-year-old patient presented to the John Hopkins

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Hospital with a painful right third cranial nerve palsy that had developed six days prior.

Based on the clinical findings, Dandy diagnosed a cerebral aneurysm and proposed that the

lesion would have most likely arisen from the right ICA or posterior communicating artery

(PCoA). On 23 March 1937, Dandy performed a right frontotemporal craniotomy

(hypophyseal approach) to expose a pea-sized aneurysm that originated from the ICA

adjacent to the PCoA. Having identified the neck of the aneurysm, Dandy placed a Cushing-

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McKenzie silver clip across its neck and cauterized its dome.38 He observed that the dome

pulsation ceased and became softer as the clip was applied. This gave rise to modern

aneurysm surgery.

In the years to follow, Dandy continued direct surgical clipping and collected a large patient

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series. In 1944, he published the first monograph describing aneurysm surgery, Intracranial

Arterial Aneurysms,21 in which he described his surgical experience with 64 aneurysms found

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at operation. In 36 operations, Dandy reported a 25% mortality rate, with 55% of the patients

considered to be cured.

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The ability to visualize aneurysm prior to surgery through angiography, first developed by

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Egas Moniz in June 1927, further encouraged neurosurgeons to innovate in the planned
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treatment of intracranial aneurysms.39
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By the 1950s and early 1960s, however, it was noted that surgical morbidity associated with

direct treatment of intracranial aneurysms remained high. For this reason, many surgeons
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continued to favor the indirect method of proximal vessel ligation. McKissock and colleagues
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performed the first randomized neurosurgical trial and demonstrated that the results of

conservative treatment were better than that of direct attack on ACoA aneurysms.40
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Microsurgical Era of Aneurysm Treatment

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The next leap in the evolution of aneurysm surgery was the introduction of the operating

microscope to neurosurgery. The application of microsurgical techniques in the late 1960s

and their propagation in the 1970s, 1980s and 1990s greatly influenced the operative results

for intracranial aneurysms. The earliest series of microsurgery for intracranial aneurysms

were reported by Kurze,41 Pool and Colton,42 and Rand and Jannetta.43 In 1969, following

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publications by Lougheed and Marshall44 and Yasargil,45 microsurgery swept through the

discipline of neurosurgery and became a standard for surgical approaches to intracranial

aneurysms. For the first time, vascular neurosurgeons could effectively illuminate and see the

aneurysm. Refinements in operative corridors were made, and a new level of understanding

of the cisternal, microsurgical and operative anatomy was quickly recognized.45-49 In this

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regard, the revolutionary work of Professor Albert Rhoton Jr. and Professor Evandro de

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Oliveira since the 1970s has greatly contributed to, and influenced, our understanding of

cerebrovascular microanatomy and modern-day operative aneurysm outcomes.50-59

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Perhaps the greatest impact of the operating microscope was not just in enhancing the results

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of experienced aneurysm surgeons, but also in accelerating the learning curve of young
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neurosurgeons. This remarkable improvement, facilitated by both technological

developments and an improved understanding of the microsurgical anatomy, produced a new

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generation of dedicated cerebrovascular neurosurgeons that include, but are not limited to,

Drake,16 Sundt,60-63 Spetzler,64-67 Dolenc,68-70 Samson,71,72 and Yasargil.45-49

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Surgical Approaches to Posterior Circulation Aneurysms

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The approach to posterior circulation aneurysms lagged considerably behind that of the
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anterior circulation. A central figure in this evolution was Charles George Drake (1920-
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1998), whose greatest contribution to vascular neurosurgery was in the understanding of the

complex anatomy of posterior circulation aneurysms and in enhancing the surgical outcomes

for these lesions. As late as 1968, Ken Jamieson, an accomplished neurosurgeon with 28

cases of posterior circulation aneurysm surgeries, reported it is clear that the basilar

bifurcation is no place for the faint of heart. Only time and greater experience will indicate

whether it is a place for neurosurgeons at all.73

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Drake adopted the use of the operating microscope in 1971 after his co-worker Dr Sydney

Peerless returned from Zurich. In 1996, Drake, Peerless and Hernesniemi published a

monograph on the unprecedented and since unmatched series of 1,767 vertebrobasilar

aneurysms, an astonishing experience amassed over a 40-year span.16 Drake had set the

standard for the surgical treatment of posterior circulation aneurysms.

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Development of Cranial Base Approaches to Intracranial Aneurysms

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An important technical advancement in aneurysm surgery was the gradual maturation of

cranial base surgical approaches (Figure 2). Earlier, Norman Dott used a bicoronal scalp flap

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for a left subfrontal approach to a supraclinoid carotid aneurysm.29 Dandy described the
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frontolateral approach for anterior circulation aneurysms in 1944.21 Several other approaches
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were introduced, including the bifrontal bone flap74,75 and unilateral frontal approach.76

Yasargil and Fox popularized the pterional approach under the microscope for all proximal
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anterior circulation aneurysms in the late 1960s and this rapidly became the standard
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approach, marking the modern era of aneurysm surgery.47

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Over the last three decades, the popularization of radical skull base techniques has unveiled

important microsurgical corridors to access deep-sited and midline intracranial aneurysms.

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Key operative strategies encompassed the anterolateral transsylvian,48 lateral

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subtemporal,24,77 posterolateral suboccipital,78 and orbitozygomatic79 approaches and their

various modifications over the years.68,80-82 These techniques reduced the distance between

the surgeon and the aneurysm, increased surgical maneuverability, and minimized retraction

on neighboring neurovascular structures to improve safe aneurysm clipping. Midline

transoral, transcervical and transfacial approaches were also attempted with varying degree of

success for aneurysms in the retroclival region.83-85 However, anterior microsurgical

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approaches were quickly discouraged due to high postoperative risk of cerebrospinal fluid

(CSF) leakage and meningitis.86-91

Recent progress in the evolution of aneurysm surgery has also witnessed the development of

mini-craniotomies for selected anterior circulation aneurysms. These techniques have been

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adopted to minimize the risks associated with exposure of large areas of the cerebral cortex,

while maintaining the ability to expose a relevant operative corridor that allows for adequate

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clip reconstruction of the target pathology.48,92-97

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Refinement of Aneurysm Clip Designs

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The first aneurysm clip, as used by Dandy, was a V-shaped, malleable silver clip, initially

developed by Cushing in 1911, and later modified by McKenzie, and then Duane Jr (Figure
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3).37,38,98 This clip could not be reopened after it was applied; the procedure was, therefore,

unforgiving and required total precision and accuracy. Recognizing this limitation, Norlen
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and Olivecrona modified the original silver clip design by adding winged blades, an
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innovation that allowed the clip to be reopened if placement was suboptimal.2 These clips,
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however, could crush the aneurysm neck and provoke shearing and tearing, but it is the

concept of repositionable clips that remains central to all modern aneurysm clip designs.
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Schwartz developed the cross-action alpha clip originally intended for use in temporary
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occlusion in the 1950s. Although excellent in concept, the Schwartz clip was difficult to use

during aneurysm surgery.99 It wasnt until the early 1950s that Frank Mayfield provided

subtle, but important, improvements in several aspects of clip technology. He and George

Kees narrowed the shank as much as possible and produced clips of various lengths (from 6

to 26 mm), angles (bayoneted, forward or lateral angle blades), and wider blade openings.

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Serrations were also added to the blades to increase their purchase and minimize the risk of

slippage. The Mayfield-Kees clip became the most popular clip of the 1950s and 1960s,

providing the neurovascular surgeon with greater flexibility during surgery.99,100

In treating many posterior circulation aneurysms, Drake recognized the need to develop a clip

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that would allow access to the neck of an aneurysm without compromising vessels that were

in the way. He modified the Mayfield-Kees clip with this idea and gave rise to modern-day

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fenestrated aneurysm clip designs.101,102

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Thoralf Sundt Jrs (1930-1992) encircling clip-graft was another significant innovation in

aneurysm clip technology that allowed for repair of vessel tears or small irregularities that are

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untreatable by ordinary clipping methods.103 Dujovny introduced very sophisticated
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techniques to measure the closing force at different points along the blades of the clip, which

allowed better design and quality control.104

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Further modifications to the aneurysm clip were based on metallurgy and different design
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configurations. Yasargil, Sundt, and Sugita (among others) introduced a series of clips made
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of noncorrosive alloys and with predictable closing pressures.46 Many of these clips included

metals that were compatible with magnetic resonance imaging (as introduced by Spetzler);105
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thus, the modern standard of aneurysm surgery unfolded. Axel Perneczky (1945-2009)
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modified the clip-applier relationship to allow the use of a slimmer clip applier profile,
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enabling the applier head to be on the inside of the clip handles.106 Furthermore, the

application of clip on clip concept, Booster clips, developed by Kees, Sundt, Piepgras and

Marsh further enhanced the ability to treat giant aneurysms or calcified aneurysm necks.107

Bypassing the Aneurysm: From Extracranial to Intracranial Techniques

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In 1969, Yasargil described the superficial temporal artery (STA)-middle cerebral artery

(MCA) bypass for the management of complex aneurysms, which redirected extracranial

flow to the intracranial circulation with a single end-to-side anastomosis.108 Despite the

negative results of the Carotid Occlusion Surgery Study, this technique has been widely

adopted for complex aneurysms that cannot be managed with conventional microsurgical or

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endovascular techniques.109,110 In response to problems with limited flow, a second-

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generation technique was subsequently developed utilizing high-flow interposition grafts

connected to donor sites in the patients neck.111-126 Four types of reconstructive bypasses

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have been described that included in situ, reimplantation, reanastamosis, and intracranial

bypass grafts.127-130 Bypassing the aneurysm provides an alternative operative strategy for

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complex aneurysms and represents a key evolutionary progress in the cerebrovascular
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surgical armamentarium.
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Intraoperative Fluorescence Visualization in Intracranial Aneurysm Surgery

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A recent development in the evolution of surgical treatment of intracranial aneurysms has

been the development of simple, rapid, and effective intraoperative angiography, using
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fluorescent dyes. Fluorescein sodium angiography, such as Yellow 560, first described for
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use in intracranial aneurysm surgery by Wrobel in 1994, has been shown to be effective in
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visualizing blood flow intraoperatively, especially in very small or deep perforating

arteries.131,132 In 2003, Andreas Raabe and the team at the Barrow Neurological Institute

introduced the use of intraoperative near-infrared (NIR) indocyanine green (ICG)

videoangiography to vascular neurosurgery.133 The application of this technique during

intracranial aneurysm surgery enables real-time intraoperative assessment of the degree of

aneurysm obliteration, exclude parent vessel compromise, and evaluate patency of

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perforators.134-141 More importantly, it obviates the need for intraoperative catheter-based

angiography in most cases.141-143

Since its application to aneurysm surgery, numerous reports have demonstrated the safety and

efficacy of the ICG technique.134-143 Notably, a few studies have described instances of parent

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artery stenosis necessitating clip repositioning undetected by Doppler ultrasound, which were

able to be elucidated using ICG.135,141,144 The flash fluorescence technique, developed by

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Rodriguez-Hernandez and Lawton, enables identification of an appropriate superficial

recipient artery in the trapping and bypass of distal MCA aneurysms, making this challenging

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surgery safer, faster and less demanding.145

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Endoscopic Transnasal Corridor and the Surgical Treatment of Intracranial
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Aneurysms

The development and technological maturation of endoscopic surgery in recent years have
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encouraged neurosurgeons, who are already familiar with the transsphenoidal techniques, to
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consider expanded endonasal approaches for the treatment of more complex cranial base
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pathologies. The surgical relevance of an endoscopic transnasal access for the clip

reconstruction of intracranial aneurysms is a natural extension of the philosophy underlying

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this evolution. Kassam reported the first purely endoscopic endonasal clipping of a coiled
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vertebral artery aneurysm via the transclival approach.146 Since then, many other reports have

been published demonstrating the feasibility of this technique on various aneurysm locations

along the skull base.147-159 The validity of such a technique, however, has yet to be defined.

The therapeutic revelance of this approach can be judged only when dedicated endonasal

instruments have been developed, and a statistically meaningful number of clinical cases

have been performed.

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Conclusion

The success of the future is built upon the dedication and innovative thinking of the

neurovascular neurosurgeon to overcome present challenges. Microsurgical treatment of

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intracranial aneurysms has reached a high level of sophistication, yet the need for surgical

expertise and innovation in the management of aneurysms continues. As in the evolution of

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any type of surgery, innovations often arise from the criticism of currently available

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techniques. Neurosurgeons must therefore continue to maintain their role as innovators in

aneurysm surgery, in order to take aneurysm repair to a new level.

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FIGURE CAPTIONS

Figure 1. Milestones in the evolution of surgical management of intracranial aneurysms.

STA-MCA, superficial temporal artery-middle cerebral artery; ICG, indocyanine green

Figure 2. Evolution of Cranial Base Approaches in the Surgical Treatment of Intracranial

Aneurysms

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Figure 3. Refinement of Aneurysm Clip Designs.

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Pictures reproduced from: A,B Louw et al.160; C Mayfield Brain & Spine161; D Del
Maestro101; H Lawton et al.105; I Mizuho162

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HIGHLIGHTS: History, Evolution and Continuing Innovations of Intracranial

Aneurysm Surgery

Evolution in aneurysm surgery is driven by the need to refine and innovate

Hunterian carotid ligation has progressed to sophisticated cranial base approaches

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Aneurysm clips and microsurgical instruments have been important advances

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Recent developments include ICG and the endoscopic endonasal approach

Further technological maturation will occur through criticism of current practice

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