the transition from hunterian ligation to intracranial

Ancient Times

The first description of an arterial aneurysm, attributedto Imhotep, can be found in the Ebers Papyrus. Records ofattempts to treat these lesions date back to 2725 BC, whenan Egyptian physician used a fire-glazed instrument totreat a bulging aneurysm.28 Although treatment of arterialdilation dates back to antiquity, the notion and underlyingcauses of the vascular changes predisposing patients tosuch aneurysms remained largely unknown. In 117 BC,Flaenius Rufus, an Ephesian physician trained in Alexan-dria, Egypt, provided the first insight into the underlyingcauses of this class of vascular lesions by suggesting thattheir origins might lie in trauma.10 Progress in treatmentsfor the disease and coining of the term “aneurysm” did notoccur until Galen described the entity in AD 200.31 Thenext 1500 years saw an expansion of our knowledge aboutaneurysms, mostly due to the work of Islamic physicians.The definition of the term “aneurysm” in its modern senseas a dilation of a weakened artery was made by Lancisis,who defined the concept in 1728.1,49 To treat these lesions,several approaches were used with various degrees of suc-cess, and the history of the evolution of surgical interven-tion is described herein. The gradual progression from su-ture ligation of the proximal artery, to surgical clipplacement, to endovascular coil occlusion, and the moremodern combination endovascular techniques, has madeit possible to treat these now mostly curable lesions.

Proximal Artery Ligation Era

The rapid progress in aneurysm surgery started with theadvent of proximal artery ligation. In a work publishedposthumously in the 1760s, Jean-Louis Petit reported hisdiscovery that there is no significant effect on the braineven if one of the carotid arteries is thrombosed.48 His pa-tient had an aneurysm at the bifurcation of the right com-mon carotid artery that was cured spontaneously. Sevenyears later, an autopsy performed in that patient showedthe lumen of the vessel to be completely occluded by anorganized thrombus. Arterial ligation was popularized inthe 1800s by John Hunter, who demonstrated safe andreproducible means of ligating certain peripheral arteries.7

Hunterian ligation, named in his honor, was adopted bymany surgeons for the treatment of aneurysms of the ICA.Operating in 1885 on a patient thought to suffer from atumor of the middle fossa, Victor Horsley (Fig. 1) pio-neered ligation of the ICA for intracranial aneurysm treat-ment.1,14 The patient was described by Keen to be “inextremely good health” 5 years after that operation.25 Ma-ny surgeons after Horsley have ligated the ICA on en-countering an intracranial aneurysm during an operation.It was not until 1928, however, that the first planned ICAligation was performed for the sole purpose of treating anontraumatic saccular aneurysm.43

The early, scattered cases of ICA ligation for aneurysmsencountered during a craniotomy for a suspected braintumor were not all as successful as Horsley’s case. Theseligations were quite frequently followed by cerebral in-farction.2,45 Many surgeons of the time, including HarveyCushing, were rather pessimistic about the surgical treat-

Neurosurg. Focus / Volume 20 / June, 2006

Neurosurg Focus 20 (6):E3, 2006

The transition from hunterian ligation to intracranialaneurysm clips: a historical perspective

NIKA V. POLEVAYA, B.S., M. YASHAR S. KALANI, PH.D., GARY K. STEINBERG, M.D., PH.D.,AND VICTOR C. K. TSE, M.D., PH.D.

Departments of Neurosurgery and Developmental Biology, Stanford University School of MedicineStanford, California; and Howard Hughes Medical Institute, Chevy Chase, Maryland

ü The description of cerebral aneurysms dates back to antiquity. Little was known, however, about the pathologicalmechanisms of aneurysm formation and treatment options for this disease until 200 years ago. The modern era ofaneurysm treatment began with the hunterian ligation of the proximal artery, followed by clip and coil occlusion. Inthis article, the authors describe the transition from conservative therapy to internal carotid artery (ICA) ligation andgradual occlusion of the ICA to the direct placement of clips on aneurysms. The driving forces and rationale behindeach major advancement are summarized, and the authors attempt to predict what these innovations mean for the futureof intracranial aneurysm management.

KEY WORDS • intracranial aneurysm • clip occlusion • history of neurosurgery

1

Abbreviations used in this paper: CA = carotid artery; ICA =internal carotid artery; MR = magnetic resonance.

Unauthenticated | Downloaded 02/24/22 12:40 PM UTC

ment of intracranial aneurysms because of the high rate ofhemiplegia that was associated with CA ligation. Cushinghimself performed multiple ICA ligations during his tumorresections to treat the incidentally exposed aneurysms; how-ever, he did not report his experience with surgical manage-ment of cerebral aneurysms.9 Cushing’s “Little Black Book,”which contains all of his surgical cases, with patient namesand their diagnoses, lists several cases of ICA ligation thatwere followed by hemiplegia and/or “sudden death.”

Despite its discouraging side effects and the overallskepticism of many surgeons at the time, ICA ligation didhave several advantages. First, it could be performed undervisualization with the naked eye, which was an importantrequirement, because the surgical microscope had not yetentered the scene of neurosurgery. Second, it did not re-quire much equipment beyond a silk suture and a basic sur-gical instrument set. Third, it could be done without a sig-nificant amount of surgical planning, and hence could beused in the case of an incidental aneurysm discovery, whichhappened quite often in the late 1800s and early 1900s.Proximal ligation gave the pioneers of vascular neurosur-gery an aneurysm treatment option before cerebral angiog-raphy was developed by Moniz in 1927.35

The ICA ligation technique underwent some improve-ment over several decades of widespread practice. In1940, Schorstein43 reported 60 cases of CA ligation for the

treatment of nontraumatic saccular aneurysms, with mor-bidity and mortality rates of 13% each. In 1969, a largerseries of 461 patients with CA ligation was published bySahs and Locksley,42 in which they reported a 20.7% mor-tality rate and a 30% stroke rate. After the advent ofmicrosurgery and microtechniques, the formerly wide-spread use of proximal artery ligation was abandoned forsurgical clip placement to treat ordinary, smaller an-eurysms. Nevertheless, CA occlusion continues to play animportant role for certain giant aneurysms in these ves-sels. The danger of cerebral ischemia and infarction afterCA occlusion has been greatly reduced by decreasing therisk of thromboembolism and by preoperative studies todetermine the potential for collateral flow, which, if inad-equate, can be supplemented by a surgically created arte-rial bypass.16

The Transition Period

The outcomes of proximal artery ligation for aneurysmtreatment so frustrated many surgeons, including NormanDott of Edinburgh (Fig. 2), that he decided to take the riskof tackling an aneurysm directly.12 In 1931, with no angio-graphic assistance, he performed a frontal craniotomy in a53-year-old patient, discovering a 3-mm aneurysm of theICA, at which point he wrapped it with muscle from the pa-tient’s leg. Many other surgeons, including Harvey Cush-ing, also tried to strengthen the weakened walls of intracra-nial aneurysms in an attempt to stabilize the flow andprevent further expansion of the lesion. However, in thesporadic cases of such treatment, surgeons reported quitevariable degrees of success. These operations mainly oc-curred as a consequence of a craniotomy being performedfor some other purpose, such as to treat a suspected tumor,and were not planned initially for aneurysm obliteration.Recently, Sadasivan, et al.,41 revisited the wrapping ap-proach by using an experimental venous pouch aneurysmmodel in rats to test different wrapping materials’ poten-tial to strengthen the aneurysm wall. These authors foundthat cotton was the most suitable material for wrappinganeurysms, whereas traditional wrapping materials suchas muscle and bovine collagen were absorbed shortly afterapplication.

The advent of the Selverstone clamp in the 1950s in-fluenced aneurysm surgery profoundly. The clamp wasplaced around the ICA to reduce the blood pressure with-in the lesion, allowing the walls to thicken and clotting tooccur within the aneurysm sac. The Selverstone clampprovided surgeons with the ability to vary the degree ofocclusion postoperatively, because the tools used to tight-en the device extended from the clamp to the surface ofthe skin. This device could thus be reopened at the firstsign of insufficient collateral circulation.36 Nornes39 dem-onstrated that graded occlusion of the ICA with the Sel-verstone clamp provides superior outcomes to those expe-rienced with full occlusion. Silvani, et al.,44 showed thatcomplete clamp closure is likely to cause ischemic sideeffects.

The capacity for collateral circulation of the circle ofWillis proved to be a major concern for both traditionalproximal artery ligation and graded occlusion of the ICAby using the Selverstone clamp. As a consequence, neuro-surgeons in the 1960s and 1970s devised various methods

N. V. Polevaya, et al.

2 Neurosurg. Focus / Volume 20 / June, 2006

FIG. 1. Portrait of Victor Horsley. (Obtained at http://www.neu-rosurgery.org/cybermuseum/portraithall/leaders/leaders.html.) Re-produced with permission from the American Association ofNeurological Surgeons, 5550 Meadowbrook Dr., Rolling Mead-ows, IL 60008.


of measuring the brain’s capacity for collateral circulationand of predicting the outcomes of gradual occlusion of theICA.39 Technological advancements such as extracranial–intracranial arterial bypass attempted to solve the problemof diminished collateral circulation resulting from the ICAocclusion. Silvani, et al.,44 suggested that extracranial–in-tracranial bypass minimized ischemic complications du-ring gradual occlusion of the ICA; however, unfortunate-ly it did not eliminate them completely.

Although the Selverstone clamp provided a temptingalternative to direct ICA ligation, several studies showedthat it might not be the ideal aneurysm treatment. Mount36

investigated the outcomes in a large patient series, indi-cating a mortality rate of 13.8% and a morbidity rate of40%. The outcome of gradual occlusion depended largelyon the aneurysm location and its overall size as well as siteaccessibility for clamp placement.24 Also, several sur-geons have shown that Selverstone clamp application maypuncture the artery and induce thrombosis within the arte-rial lumen, causing complete occlusion and possibly deathdue to ischemia.8

The advent of MR imaging imposed a new constrainton the implantable metallic devices used for aneurysmtreatment, along with improved accuracy for surgicalplanning and postoperative monitoring. Devices such asthe Selverstone clamp now were subject to MR compati-

bility scrutiny. Dujovny, et al.,19 conducted a series ofprominent studies in which they tested a wide range ofneurosurgical devices used for aneurysm treatment. Theyinvestigated the mechanical and metallurgical propertiesof a series of arterial clamps, including Crutchfield, Sel-verstone, Salibi, and Kindt clamps, with respect to theircomposition, surface cleanliness, magnetic properties, andcorrosion resistance. Crutchfield and Selverstone clampswere found to be nonferromagnetic. The Selverstoneclamp, however, turned out to be much more corrosion-prone than other devices, suggesting that it would not bean adequate long-term solution for patients.

Norman Dott13 introduced another method of directaneurysm attack when, in 1933, he attempted to ligate theneck of an aneurysm with surgical sutures. This approachwas popular among the surgeons of that time. It demand-ed agility and confidence from the operator. Direct sutureligation is an extremely technical exercise; it requires thesurgeon to dissect out the aneurysm neck and thread asuture around it. However, as reported by Sundt,47 the sur-gical clip soon displaced this method. The clip providedgreater closing pressure and easier application to the manypotential aneurysm sites for which surgical access was dif-ficult. Several other surgeons, including Campbell andBurklund6 in 1953, and Drake and Amacher in 1969,15

attempted to combine the suture ligation with excision ofaneurysms; however, these methods failed to gain wide-spread popularity and were abandoned for surgical clipplacement.

The Clip

A major revolution in the treatment of this class of vas-cular lesions occurred serendipitously, much like manyother phenomena in science and medicine. In 1911, in hisquest to develop tools for tumor resections, Harvey Cush-ing (Fig. 3) produced what was to become the first vascu-lar clip.9 Known as “the silver clip” or the Cushing clip, thetool was used in tumor surgeries for “placement on inac-cessible vessels, which, though within reach of a clamp, areeither too delicate or in a position too awkward for safe lig-ation.” Cushing, however, never used his invention for ob-literation of intracranial aneurysms. McKenzie modifiedthe Cushing clip and, somewhat ironically, in 1937, Cush-ing’s competitor Walter Dandy (Fig. 4) became the firstneurosurgeon to use this device to clip an aneurysm.19 Thenew clip allowed surgeons to exclude an aneurysm selec-tively from the parent circulation, a concept that markedthe beginning of the modern era of aneurysm surgery.

The clip that Dandy used in his 1937 procedure evolvedsignificantly over the next several decades. It is noteworthythat in his writing in 1938 and in his textbook on brain sur-gery in 1945, Dandy addressed the issue of collateral cir-culation and the application of both ligation of the ICA inthe patient’s neck and intracranially with a silver clipplaced on the artery to “trap” the aneurysm. The simple V-shaped Dandy clip (the silver clip modified by McKen-zie) was subsequently modified by Olivecrona, who addedwinged blades to allow reopening of the device (the origi-nal Dandy clip could not be reopened).29 Schwartz intro-duced a miniature spring forceps clip to aid the reopeningand to avoid shearing and tearing of the aneurysm. May-field modified Schwartz’s clip in 1952 because the earlier


History of intracranial aneurysm treatment methods

3

FIG. 2. Portrait of Norman Dott. (Obtained at http://www.st-andrews.ac.uk/~sshm/dott.html.)


device was too large and its application into the smallspaces of the cranium was quite awkward. Mayfield alsoattempted to reduce the risk of slippage by adding serra-tions to the clip, and designed an applicator that had tweez-er-like dexterity and a drop lock.33 The evolution beyondthe Mayfield clip resulted in a series of devices with sig-nificantly greater closing pressures to avoid incompleteocclusion of the aneurysm neck. Further development ofaneurysm clips has been driven by balancing crucial fac-tors such as size (to reduce the visual obstruction of theoperating field), risk of slippage, potential damage to theaneurysm neck and the surrounding vasculature, and lastbut not least, the clip’s biosafety on MR imaging. Sugitaand Spetzler clips are beautiful examples of the currentsolution to finding such a balance.

The development of aneurysm clips was greatly influ-enced by two revolutionary inventions: cerebral angiogra-phy and the operating microscope. Angiography was thebrainchild of Egas Moniz,35 and produced in 1927. Duringthe following decade, many surgeons added this diagnos-tic tool to their arsenal for combating aneurysms. Sur-geons were no longer limited to addressing aneurysms ofthe ICA proper, and by the mid-1950s, many had extend-ed such treatment to aneurysms on the branches of ICA.21,

37,38 These advances paved the way for the development ofsurgical techniques for posterior circulation aneurysms.Kurze27 was the first neurosurgeon to use the operatingmicroscope in surgery for intracranial aneurysms (in 1957,

in Los Angeles). Nevertheless, the microscope was notreported as an adjunct to aneurysm surgery until 1966,40

after which Yasargil is widely credited with popularizingthis approach. The advent of microneurosurgery placedextra emphasis on clip development, demanding ever moreslender clips that would allow the approach to narrowspaces of the cranial anatomy.

Even as late as the 1960s, many neurosurgeons doubtedthe effectiveness of aneurysm surgery. To a significantextent, this skeptical outlook was based on some of the lesssuccessful outcomes reported in series of aneurysmpatients. In several small series, mortality rates as high as86% were reported,42,45 although a mean mortality rate of28.7% for aneurysm treatment with intracranial clip place-ment was reported by 1956.42 As detailed by Stein,45 Dandyhimself had considered clipping and ligature of aneurysmson branches of the ICA “hopeless.” In 1963, Merritt34

advised surgery only for the purpose of resolving largeassociated hematomas. Alvord and Thorn3 concluded in1977 that “no great difference in the number of survivors(the inverse of mortality) could be detected in previouslyreported series of cases regardless of the method of treat-ment, site or number of aneurysms, or any other factor



FIG. 4. Portrait of Walter Dandy. (Obtained at http://www.neu-rosurgery.org/cybermuseum/portraithall/leaders/DANDY.GIF.)Reproduced with permission from the American Association ofNeurological Surgeons, 5550 Meadowbrook Dr., Rolling Mea-dows, IL 60008.

FIG. 3. Photograph of Harvey Cushing. (Obtained at http://www.neurosurgery.org/cybermuseum/portraithall/leaders/leaders.html.)


which could then be analyzed.” By 1970, however, withadvances in microneurosurgery, clip occlusion of intracra-nial aneurysms was shown to have significantly betteroutcomes than CA ligation.32 The main factors influencingthe success of the outcome appeared to be dome size,aneurysm location, and the patient’s age.

The invention of MR imaging has influenced modernclip development as well as the development of arterialclamps. Dujovny and colleagues17,18 performed a detailedanalysis of the ferromagnetic properties of the Yasargil,Sugita, and Perneczky clips and discovered great variabili-ty in these properties among different clips (even betweenclips of the same type) in response to MR imaging, sug-gesting that clips be tested before their application. Severalintracranial clip fractures due to long-term corrosion havebeen reported, motivating meticulous investigation ofstress corrosion properties of the various modern clips.26

The availability of modern metallurgical analysis tools hasenabled this group of investigators to assess the microstruc-tures, hardness, chemical composition, and susceptibility tostress corrosion failure of various clips,20 providing a ratio-nale for the improvement of clip design, materials used,and individual testing of clips before application.

Unfortunately, clip occlusion continues to pose severalmajor limitations. Not all aneurysms are amenable to clipplacement. Aneurysms in which the dome-to-neck ratio istoo small are much more difficult to clip, with fusiformand dissecting aneurysms being extreme examples. Also,any clip placement procedure poses the risk of incompleteocclusion, which may predispose the aneurysm toregrowth or rebleeding. Another risk that patients faceduring cerebral aneurysm surgery is that of an intraopera-tive aneurysm rupture due to clip placement. Perhaps in

the future, malleable clips that conform to the angioarchi-tecture of a particular patient may help to circumventsome of these problems.

Conclusions

With the advancement of neurosurgical technology, thelimitations of conservative management of aneurysms be-came increasingly apparent. Nonsurgical treatment groupsin various studies tended to demonstrate significantlyhigher overall morbidity and mortality rates, with manypatients dying of fatal subarachnoid hemorrhage and va-sospasm.4,11,22,23,30 In cases of higher-grade aneurysms,mortality rates reached 80 to 90% for conservatively treat-ed patients, even with modern treatments to lower bloodpressure.11 The prognosis for conservative therapy for in-tracranial aneurysms was worse in comparison with bothICA ligation treatment and direct clip placement, both ofwhich showed much higher patient improvement rates(70–80%).11,30 Because of these grim outcomes, most sur-geons now argue for early and urgent surgical treatmentfor intracranial aneurysms, especially in the case of high-grade lesions, ones that have ruptured, or apparent in-crease from the original aneurysm size.4,11,23

Historically, the poor outcome associated with conserv-ative therapy prompted the neurosurgical pioneers to usehunterian ligation; complete ligation at first, then followedby the transitional practice of gradual occlusion. Althoughoccasionally used to this day for cases of giant, fusiform,and complex lesions,16,46 hunterian ligation did not proveto be the optimal treatment for intracranial aneurysms dueto its ischemic and embolic complications in many pa-tients, prompting continuation of the search for bettertreatments (Fig. 5). Aneurysm clips had initially compet-



5

FIG. 5. Timeline of major events in aneurysm treatment history.


ed with the practice of graded ICA ligation; however,technological improvements to the clip, the advent of theoperating microscope, cerebral angiography, and MRimaging resulted in significantly more consistent and bet-ter outcomes for clip occlusion of aneurysms.

Currently, patients undergoing aneurysm surgery have amuch lower risk of death or gross neurological morbidity.Hence, the concept of a “good outcome” is now subject torevision, because it requires a more subtle analysis of theneuropsychiatric state of the patient.5 Through the persis-tence, curiosity, and courage of the many neurosurgicalpioneers, the clip has become a relatively safe and effec-tive tool for aneurysm treatment and provides minimalobstruction of the operating field, optimal closing pres-sure, and small probability of slippage and tissue damage.These surgeons and their ingenious tools have transform-ed the natural history of aneurysm progression from aonce discouraging and lethal vascular pathological entityinto a mostly curable neurosurgical lesion.

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Manuscript received March 16, 2006.Accepted in final form May 11, 2006.Address reprint requests to: Victor C. K. Tse, M.D., Ph.D., De-

partment of Neurosurgery, Stanford University School of Medicine,MSLS Room P310, Stanford, California 94305-5327. email:[email protected].



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the transition from hunterian ligation to intracranial

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