Endovascular Approach to Cerebral Revascularization: Historical Vignette

Journal Pre-proof Endovascular Approach to Cerebral Revascularization: Historical Vignette John S. Costello, BA, Sauson Soldozy, BA, Pedro Norat, MD, Jennifer D. Sokolowski, MD, PhD, Kaan Yagmurlu, MD, Khadijeh Sharifi, PhD, Petr Tvrdik, PhD, Min S. Park, MD, M. Yashar S. Kalani, MD, PhD PII:

S1878-8750(20)30090-5

DOI:

https://doi.org/10.1016/j.wneu.2020.01.072

Reference:

WNEU 14102

To appear in:

World Neurosurgery

Received Date: 13 October 2019 Revised Date:

9 January 2020

Accepted Date: 9 January 2020

Please cite this article as: Costello JS, Soldozy S, Norat P, Sokolowski JD, Yagmurlu K, Sharifi K, Tvrdik P, Park MS, Kalani MYS, Endovascular Approach to Cerebral Revascularization: Historical Vignette, World Neurosurgery (2020), doi: https://doi.org/10.1016/j.wneu.2020.01.072. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Elsevier Inc. All rights reserved.

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Endovascular Approach to Cerebral Revascularization: Historical Vignette

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*John S. Costello, BA,1 *Sauson Soldozy, BA,1 Pedro Norat, MD,1 Jennifer D. Sokolowski, MD, PhD,1 Kaan Yagmurlu, MD,1 Khadijeh Sharifi, PhD, 1 Petr Tvrdik, PhD,1 Min S. Park, MD,1 M. Yashar S. Kalani, MD, PhD1

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Department of Neurological Surgery, University of Virginia Health System, Charlottesville, Virginia

*These authors contributed equally Corresponding Author:

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Sauson Soldozy, BA1

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P.O. Box 800212

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Charlottesville, VA 22908

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Phone: 434-924-2735

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Fax: 434-924-9656

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[email protected]

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Conflict of Interests: The authors deny any conflicts of interest

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Total number of words in the abstract: 208 Total number of words in the text: 2,073 Total number of references: 40 Total number of tables/figures (combined): 3

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Abstract From their origins as cardiovascular research tools, endovascular techniques evolved to provide a

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minimally invasive means of diagnosis and therapy for individuals suffering from occlusive artery disease. First

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pioneered by William Harvey, his work would set the stage for all endovascular experiments that would be carried

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out after him. This includes the bold self-catheterization procedure performed by Werner Forssmann in 1929, which

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would lead to his dismissal by his superiors, only to regain respect within the medical community in 1956 upon

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receiving the Nobel Prize. Charles Dotter was the first to understand the true potential of endovascular approaches

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after a chance recanalization that would catapult arterial catheterization into first the cardiovascular surgical arena,

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followed thereafter into neurosurgery for intracranial stenoses. Having been meticulously evaluated and compared to

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open vascular procedures, endovascular neurosurgery has continued to be refined and optimized. Understanding the

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history and development of these techniques and their applications in neurosurgery is necessary in order to

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appreciate the current clinical utility of these procedures, serving to provide the vascular neurosurgeon a greater

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array of treatment options for patients. This paper explores the major scientific and technological advancements that

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facilitated the development of the endovascular approach to cerebral revascularization as well as current indications

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and ongoing clinical trials.

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Keywords: atherosclerosis; catheterization; cerebral revascularization; endovascular; neurosurgical history; stenting

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Origins The idea of utilizing the vascular system as a conduit for physiologic manipulation can be traced back to

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the 17th century. By 1628, an accurate description of cardiovascular physiology was demonstrated by English

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physician William Harvey. In his work, De Motu Cordis, he outlined experiments that led him to make observations

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on the circulatory nature of blood flow (Figure 1) 1. Harvey’s work sparked curiosity in several scholars, most

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notably Christopher Wren, who in 1656 wondered if the circulatory system was the means by which snake venom

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rapidly exerted its effects. Wren invented a method of fluid administration in which he utilized “slender syringes or

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quills, fastened to bladders… containing the matter to be injected,” and in doing so was the first individual to

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perform an intravenous injection 2. Thomas Willis, who worked closely with Wren, would adapt this principle in his

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anatomical studies. Injecting a dyed liquor into the carotid arteries assisted him in his depiction of the circle of

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Willis 3. This marked the first time that intra-arterial injections aided in the visualization of neurovascular structures,

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a principle that would later be reapplied in cerebral angiography by Egas Moniz in 1927 4. Direct injection was also

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used in the earliest endovascular procedures, such as in Robert Dawbarn’s “starvation operation;” he employed a

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mixture of Vaseline and paraffin to embolize malignant tumors of the external carotid artery (ECA) in 1904 5.

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The first steps toward what would eventually become modern day catheterization began in 1711 with

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Stephan Hales, an English clergyman and scientist, who was the first to measure arterial blood pressure 6. Hales’

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first experiment involved the insertion of a brass pipe into the left crural artery of a living mare. Using the trachea of

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a goose as a flexible connector, a glass tube of 9 feet in length was fixed to the pipe, and this was used to measure

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blood pressure. (Figure 2). He would carry out other experiments, including filling the chambers of a beating heart

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with molten wax to determine cardiac output 7. In 1848, chemist and physicist Claude Bernard, who coined the term

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catheterization, attempted to measure the temperature of blood within the heart. After exposing a horse’s jugular

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vein and carotid artery, Bernard utilized a retrograde approach to insert a glass tube and, ultimately, a mercury

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thermometer, into the right and left ventricles 6. In the 1860s, French veterinarian Auguste Chauveau and physician

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Etienne Jules Marey created a double-lumen catheter which they utilized to measure intracardiac pressures, an idea

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that would later be exploited by André F. Cournand in 1975 8.

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The earliest descriptions of human cardiac catheterization occurred in 1905 by Germans Frizt Bleichroeder,

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Ernst Unger and Walter Loeb. Performing experiments on each other, Unger passed a catheter into Bleichroeder’s

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basilic vein, believing they reached the heart when Bleichroeder experienced severe chest pain. Given the lack of x-

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ray documentation and, in their opinion, the lack of significance of their work, no record was published at the time 8.

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Werner Forssmann, a German surgical resident, performed the first successful cardiac catheterization on himself in

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1929 (Figure 3) 9. Against the wishes of his superiors, Forssmann anesthetized his left cubital fossa and inserted a

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ureteral catheter 65 cm into his right atrium and confirmed its location with an x-ray. After publishing his findings,

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Forssmann received criticism from several prominent physicians, including Unger, who claimed Forssmann

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plagiarized his work. It would not be until 1956 that Forssmann gained the respect of his colleagues when he was

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awarded the Nobel prize for pioneering catheterization, along with physicians André Cournand and Dickinson

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Richards who elaborated upon his work 8. Catheterization provided many advantages over direct injection

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techniques, setting the stage for modern endovascular procedures.

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Angioplasty and Stenting Following Forssmann’s discovery, catheterization became utilized for bedside monitoring and gave

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physicians a critical tool to study cardiovascular pathophysiology; however, vascular procedures continued to be

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performed as open surgeries, requiring anesthesia and inpatient care 6. The theme of minimally invasive treatment in

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neurosurgery was ingeniously heralded by Giancarlo Piazza and Giulio Gaist in 1960, when they described

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“milking” a bullet that was lodged in a patient’s middle cerebral artery (MCA) down to the intracranial internal

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carotid artery (ICA) 10. In 1962, Ricketts and Abrams applied the percutaneous method, described by Sven

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Seldinger, to make the femoral artery approach less invasive 11. A pioneering technique still used today, noninvasive

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percutaneous catheterization was introduced by Seldinger in 1953 12. Ironically, this development was not

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considered sufficient to earn his doctorate by his Department Chair 13. The noninvasive potential of endovascular

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procedures excited individuals such as Charles Dotter, who foresaw catheterization assuming more than a diagnostic

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role, envisioning its potential therapeutic applications. In 1963, Dotter performed the first arterial recanalization,

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although inadvertently. During an abdominal aortogram procedure, Dotter passed a percutaneously introduced

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catheter retrogradely through an occluded right iliac artery and accidentally recanalized it 14. Dotter reported this

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event at the Czechoslovak Radiological Congress, famously stating:

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The diagnostic catheter can be more than a tool for passive means for diagnostic observation; used with

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imagination, it can become an important surgical instrument.

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Charles T. Dotter (1920 – 1985) 15

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In 1964 Dotter performed the first planned arterial recanalization on an 82-year-old woman with a cold, pulseless,

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continuously painful left lower extremity with an ischemic ulcer and progressing gangrene of three toes. Dotter

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identified a stenotic region of the superficial femoral artery and, after performing what would later be known as

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percutaneous transluminal angioplasty (PTA), re-established blood flow. Saving the patient from amputation, Dotter

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noted that the patient’s leg became warm and pulsatile within minutes 14,16. In 1969, in an attempt to combat the

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complication of restenosis, Dotter introduced the transluminal placement of a coil spring endarterial tube graft, or

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stent, using proof-of-concept experiments in dogs 17. In addition to endoluminal stenting, Dotter also entertained the

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idea of using balloons to dilate arteries. Developed by Thomas Fogarty, these balloons were initially designed to aid

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in the removal of arterial and venous emboli 18,19. Progress continued with the development of a balloon capable of

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dilating peripheral arteries by a cardiologist from Zurich, Andreas Gruentzig 14. Gruentzig utilized his balloon

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catheter in 5 cases of percutaneous transluminal coronary angioplasty, which he described in 1978 20,21.

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Transition into Neurosurgery

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Balloon PTA was first applied in neurosurgery in 1980 by T. M. Sundt. Noting its success in the treatment

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of coronary, renal, and iliofemoral stenoses, Sundt applied transluminal angioplasty in patients with basilar artery

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(BA) stenosis 21. In 1982, Sundt reported the outcome of four patients with BA stenosis after PTA: 3 were disabled

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by progressive symptoms and one remained stable 22. Transluminal angioplasty was performed again on a patient

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with BA stenosis in 1987, but the patient suffered a brainstem infarction after treatment. The authors noted a high

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degree of risk associated with the procedure, in part due to the perforating arteries supplying the brainstem 23. In

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1990, Philip Purdy experienced more success, reporting a case of improved regional cerebral blood flow (rCBF)

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after angioplasty of an atherosclerotic MCA. Despite restenosis, the patient appeared to improve and her rCBF

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remained elevated on follow-up 24. Rostomily et al. reported success in using PTA to treat a patient with high-grade

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stenosis of the petrous internal carotid artery (ICA), who remained asymptomatic on follow-up two years afterward

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vertebral artery (VA) stenosis, BA stenosis, or both. Of note were the 3 cases involving patients with BA stenosis. In

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one patient, PTA was performed via direct puncture of the VA at the C1 segment under general anesthesia. Despite a

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widely patent BA postoperatively, the patient suffered a pontine stroke and died 6 weeks later. A transfemoral

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approach under local anesthesia was performed on the other two patients, made possible by the implementation of a

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newer PTA balloon system. These two patients fared much better on follow-up. Due to the high-risk nature of BA

. Randall et al., in 1993, reported the successful application of transluminal angioplasty in patients with either

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stenosis, the authors recommended that only patients who have failed anticoagulation therapy should be considered

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for angioplasty 26.

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Given the incidence of restenosis in many cases after angioplasty, stenting in intracranial circulation

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emerged as a treatment option for occluded cerebral vasculature. First introduced in 1996 by Feldman et al. for the

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treatment of right internal carotid artery (ICA) stenosis 27, stenting was beginning to show evidence of superior

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outcomes when compared to angioplasty alone. In 1998, Dorros et al. reported a flow-limiting dissection after

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angioplasty of a stenotic petrous ICA that was corrected by a balloon-expandable coronary stent 28. A year later, the

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first case report of an intra-arterial stent for the treatment of an occluded BA was made 29. Other cases that year also

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reported successful application of stenting in the treatment of BA stenosis 30–32. The advantage of stenting was

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particularly evident when Joseph et al. reported its ability to treat basilar stenosis after several failed attempts with

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balloon angioplasty 33. Not all cases were met with positive outcomes. In 2001, Levy et al. performed a retrospective

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analysis on 11 patients, all treated with PTA and stenting for VA or BA stenosis. Periprocedural death occurred in 3

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patients, with one delayed death after a pontine stroke, resulting in a 36.4% mortality rate 34. In 2004, the Stenting of

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Symptomatic Atherosclerotic Lesions in the Vertebral or Intracranial Arteries (SSYLVIA) study released its results

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on the NEUROLINK System (Guidant Corporation). The NEUROLINK System comprises a balloon dilatation

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catheter and a stent and delivery catheter designed specifically for cerebral vasculature. Enrolling 61 patients, the

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SSYLVIA study reported 95% successful stent placement, with stroke occurring in 6.6% of patients within 30 days

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and in 7.3% of patients between 30 days and 1 year. Restenosis occurred in 35% of patients, although 61% were

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asymptomatic 35. In 2005, the Food and Drug Administration (FDA) approved the Wingspan stent (Boston

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Scientific, Fremont, CA, USA) for patients with symptomatic intracranial stenosis >50% who are refractory to

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medical treatment 36.

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In response to the high incidence of restenosis after stenting, biologically active or drug-eluting stents

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(DES) have emerged to inhibit intimal proliferation 37. Given the success of DES in reducing risk of in-stent stenosis

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of coronary arteries, Abou-Chebl and colleagues reported their experience with 8 patients with intracranial stenoses.

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Treated with Cypher (Cordis Corp) and Taxus (Boston Scientific Inc.) stents, mean stenosis was reduced from

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84.4% to 2.5%, with no complications or restenosis on 11-month follow-up 38. This proved to be a major

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improvement over bare metal stents. In 2014, the first case report describing the use of DES in a patient with

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moyamoya disease was published. A 43-year-old woman with moyamoya disease demonstrated stenosis of her right

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M1, right distal ICA, and left MCA. Right-sided superficial temporal artery (STA)-MCA bypass and

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encephaloduroarteriosynangiosis were performed; however, 1 month later her symptoms returned, and angiography

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revealed restenosis of her left ICA to 90%. Endovascular DES treatment was performed and after 18 months follow-

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up, she had no in-stent stenosis with resolution of ischemic symptoms, suggesting a role for DES in patients with

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moyamoya disease 39. Still in its infancy, physicians continued to remain unsure of when to best apply transluminal

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angioplasty and stenting in the treatment of patients with atherosclerotic intracranial stenoses. Ongoing innovations

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in catheter and stent technology are promising, but care should be taken not to forget that antiplatelets remain an

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effective treatment for the majority of patients 40.

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Conclusion

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The idea that the vascular system could be a means of delivering foreign agents for research and medicinal

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purposes began after William Harvey’s work on the circulatory system nearly 400 years ago. This would lead

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Christopher Wren to develop intravenous injections for the first time in 1656, and ultimately prompt pioneering

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physicians to develop modern day catheterization, a term coined by Claude Bernard in 1848. It was not until Werner

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Forssmann performed right heart catheterization on himself in 1929 that the technique began to gain ground. From

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the discovery of cerebral angiography by Egas Moniz, to modern day percutaneous transluminal angioplasty by

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Charles Dotter, the origins of these techniques can be traced back to the original catheter. By the 1980s, physicians

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readily applied endovascular techniques in neurosurgery as minimally invasive techniques to treat human pathology.

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Refinement of these endovascular approaches to revascularization evolved through case reports, case series, and

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clinical trials, which have created its current application in medicine today as a viable alternative to medical

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management and traditional bypass surgeries.

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Funding – No funding was received for this research.

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Conflict of Interest: All authors certify that they have no affiliations with or involvement in any organization or

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entity with any financial interest (such as honoraria; educational grants; participation in speakers' bureaus;

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membership, employment, consultancies, stock ownership, or other equity interest; and expert testimony or patent-

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licensing arrangements), or non-financial interest (such as personal or professional relationships, affiliations,

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knowledge or beliefs) in the subject matter or materials discussed in this manuscript.

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Ethical Approval and Consent for Publication: This article does not contain any studies with human participants

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performed by any of the authors and therefore does not require consent to publish.

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Availability of data and materials statement: This article is a review and does not contain original data that can be

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made publicly available.

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Authors Contributions: MK was responsible for conception, design, and oversight of this project. SS and JC were

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responsible for performing the historical literature review, analyzing and interpreting studies, planning and writing

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the manuscript. SS identified and sourced the included figures. PN, JS, KY, and KS were responsible for organizing

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and contributing to the manuscript, while providing feedback on the report. MP and PT assisted with interpreting the

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findings of the results, providing feedback, as well as preparation of the manuscript. All authors approved of the

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final manuscript.

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Acknowledgements: The authors have no acknowledgements to declare

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Figure 1. William Harvey’s illustration of venous valves.

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This image depicts William Harvey’s observation that he could not push blood in the vein down the arm, while he was able to push blood in the vein up the arm with ease, demonstrating the unidirectional nature of venous flow 1. Image courtesy of Claude Moore Health Sciences Library, University of Virginia Health System.

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Figure 2. Blood pressure experiments.

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Page 16 of Stephen Hale’s work, Haemastaticks, depicting data from his blood pressure measurement experiments in horses 7. Image courtesy of Claude Moore Health Sciences Library, University of Virginia Health System.

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Figure 3. Right-heart catheterization

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First documentation of right-heart catheterization by Werner Forssmann. Reprinted by permission from Springer Nature: Klinische Wochenschrift, Die Sondierung des Rechten Herzens, Werner Forssmann,1929 9.

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List of abbreviations: MCA – middle cerebral artery ICA – internal carotid artery PTA – percutaneous transluminal angioplasty BA – basilar artery rCBF – regional cerebral blood flow VA – vertebral artery SSYLVIA – Stenting of Symptomatic Atherosclerotic Lesions in the Vertebral or Intracranial Arteries FDA – Food and Drug Administration DES – drug-eluting stents STA – superficial temporal artery CAS – carotid artery stenting ASA/AHA – American Stroke Association and the American Heart Association CEA – carotid endarterectomy SAPPHIRE – Stenting and Angioplasty with Protection in Patients at High Risk for Endarterectomy CAVATAS – Carotid and Vertebral Artery Transluminal Angioplasty Study CREST – Carotid Revascularization for Primary Prevention of Stroke MI – myocardial infarction IMM – intensive medical management ASITN – American Society of Interventional and Therapeutic Neuroradiology SIR – Society of Interventional Radiology ASNR - American Society of Neuroradiology EC/IC – Extracranial-Intracranial Bypass study SAMMPRIS – Stenting and Aggressive Medical Management for the Prevention of Recurrent Stroke in Intracranial Stenosis VISSIT – Vitesse Intracranial Stent Study for Ischemic Stroke Therapy CASSISS – China Angioplasty and Stenting for Symptomatic Intracranial Severe Stenosis VERiTAS – Vertebrobasilar Flow Evaluation and Risk of Transient Ischemic Attack TIA – transient ischemic attack

VB – vertebrobasilar qMRA – quantitative magnetic resonance IV-tPA – intravenous-tissue plasminogen activator CVST – central venous sinus thrombosis ISCVT – International Study on Cerebral Vein and Dural Sinus Thrombosis