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History

REVIEW

Alfred J Luessenhop and the dawn of a new superspecialty: endovascular neurosurgery Tanmoy Kumar Maiti, Shyamal Chandra Bir, Papireddy Bollam, Anil Nanda Department of Neurosurgery, LSU Health-Shreveport, Shreveport, Louisiana, USA Correspondence to Dr Anil Nanda, Department of Neurosurgery, LSU HealthShreveport, 1501 Kings Highway, Shreveport, LA 71130-3932, USA; [email protected] Received 4 November 2014 Revised 25 November 2014 Accepted 28 November 2014

ABSTRACT Endovascular neurosurgery, or interventional neuroradiology, has developed rapidly over the last 50 years and has posed a challenge to the established mode of open surgery. Alfred J Luessenhop, an American neurosurgeon, is credited with the first embolization of a cranial arteriovenous malformation and the first intracranial arterial catheterization to occlude an aneurysm. This review describes the life and work of the surgeon who can be regarded as the father of endovascular neurosurgery.

INTRODUCTION The field of endovascular neurosurgery has seen one of the most rapid growths in medical specialties over the last 50 years. This specialty has evolved in the bold hands of a few physicians who could foresee its potential and therefore did not hesitate to venture into uncharted territory. Although neuroradiologists, neurosurgeons, and neurologists are now vying for the leading role, neurosurgeons cannot deny their initial reluctance in this field. Professor Alfred J Luessenhop, despite being a neurosurgeon, stood apart from them. He was able to realize the potential, and will always be remembered as the first interventionist to embolize an arteriovenous malformation (AVM). The procedure, which he called artificial embolization,1 later became popular as surgical embolization.

LIFE AND NEUROSURGICAL CAREER

To cite: Maiti TK, Bir SC, Bollam P, et al. J NeuroIntervent Surg Published Online First: [please include Day Month Year] doi:10.1136/ neurintsurg-2014-011532

Alfred John Luessenhop was born in Chicago on 6 February 1926 and spent his childhood in Westfield, New Jersey where his family moved when he was 4 years old. His father was working at Western Electric Company where he was comptroller of manufacturing. He joined Yale University in July 1943. After completing the freshman year, his training was temporarily interrupted by World War II, when he served in the army in Europe as a medical technician. He went back to Yale University in July 1946 and, after two more years of pre-medical work, entered Harvard Medical School in September 1948 and graduated in 1952. He was trained as a surgical intern for 1 year at the University of Chicago. His growing interest in the surgical field made him pursue the residency training program in neurological surgery at Massachusetts General Hospital. During his first year he served as a Clinical and Research Fellow at Harvard. He was appointed as a Teaching Fellow in surgery at Harvard Medical School during his final year. After completing his residency program in June 1959, Dr Luessenhop became a visiting scientist at

the National Institutes of Health and simultaneously began clinical practice at the Georgetown University Medical Center in Washington DC. He joined Georgetown full time in 1962. Later on, at the age of 36, he became the chief of neurosurgery at Georgetown and remained in this capacity until his retirement from active practice in 1993 (figure 1). He served as chief of neurosurgical services at the District of Columbia General Hospital, Children’s Hospital of the District of Columbia, and the Veteran’s Administration Hospital, and as a consultant to many reputed organizations including the National Institutes of Health, National Naval Medical Center, Federal Aviation Administration, State Department and Central Intelligence Agency (CIA). He was duly recognized in the neurosurgical community. He served as the president of the First International Conference on Spontaneous Intracerebral Hemorrhage in Tokyo, Japan, in 1972. He was also honored by the American Association of Neurological Surgeons and the Congress of Neurological Surgeons in 1998 with an annual lecture named for him. He was interested in playing golf, collecting history and stamps. On a sad note, his life ended on 21 February 2009 when he unfortunately suffered poly-trauma from a golf cart accident.2 3

HISTORICAL BACKGROUND OF INTERVENTION The concept of embolization of vascular malformations developed with a series of events beginning in the 1930s. Brooks,4 in 1930, was thought to be the first to describe a case of carotid–cavernous fistula treated by injecting a muscle fragment connected with a silver clip into the internal carotid artery. However, Vitek and Smith,5 in their fascinating article, showed that the so-called ‘Brooks method’ was misinterpreted by Hamby and Gardner, who had actually masterminded it.6 With that groundwork, in the 1950s several researchers introduced multiple-sized particles into the cerebral circulation and looked for their effects on the vascular system and the brain parenchyma.7 8 It was also known that the major feeding arteries are greatly enlarged and therefore lead to far greater flow to the malformation than to the surrounding brain. Based on these hemodynamic and anatomic studies, Dr Luessenhop postulated that an embolus of predetermined size and configuration would always find a way to a malformation.

FIRST CRANIAL INTERVENTION Only a few months after completing his residency, in the infancy of his neurosurgical career, Dr Luessenhop performed a landmark procedure. He

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History Box 1 Report of the case

Figure 1 Alfred J Luessenhop (from Wikipedia).

reported the case in the Journal of the American Medical Association as artificial embolization of cerebral arteries (box 1).1 His senior co-author, Dr William Spence (1908–1992), had been using a highly refined methyl methacrylate for cranioplasty since 19479 and was probably the motivator for using it as emboli. To our surprise, we did not find any other articles where both were co-authors. Dr Spence remained famous for his development of acrylic cranioplasty, for which he held the patent for many years. He is also regarded as one of the pioneers of carotid endarterectomy for atherosclerotic plaque.10 Dr Luessenhop acknowledged his residents Drs Velasquez and Wissinger for their unpublished data regarding the course of metallic spheres through the larger leptomeningeal arteries of the dog and concluded that these metallic spheres had a tendency for transient arrests at bifurcations causing gradual dilation of the proximal and distal ends leading to a salutatory course into one of the larger branches. This is how the neurological deficit may fluctuate and even permanently reverse with a distal shift of emboli.11 Dr Velasquez has co-authored other landmark articles as well.11 12 Although his paper was highly appreciated, when Rosenbluth et al13 tried to follow the same procedure in a patient with a large parietal and occipital AVM filling principally from the right posterior communicating–posterior cerebral artery they found that the emboli were not carried to the malformation but instead lodged in the distal carotid siphon. They concluded that the procedure may be more applicable to vascular malformations which are fed principally by the anterior and middle cerebral arteries.

FIRST CATHETERIZATION OF INTRACRANIAL ARTERIES: FIRST ATTEMPT TO OCCLUDE AN ANEURYSM Based on the success in management of AVM, Dr Luessenhop further planned to maneuver a catheter within the intracranial arteries. He, together with Dr Velasquez, designed a glass model of an internal carotid artery to check the suitability of various plastic and rubber catheters alone and then along with embolus to negotiate into it. Subsequent studies were carried out in the abdominal aortas of dogs, which correspond in size to the common carotid artery in humans. Eventually they devised a silicon coated glass bulb that was suitable for a 2.5 mm spherical embolus to carry a flexible Silastic tube accepting a #22 needle (figure 3A). After they were happy with the results in the animal studies, they applied their knowledge to the clinical setting in three patients and published their findings on these patients in the Journal of Neurosurgery in 1964.12 2

On September 11, 1959 a 47-year-old woman … was admitted to the Georgetown University hospital about 4 h after the rapid onset of a severe generalized headache, drowsiness, and impairment of vocal expression. Since early childhood she had frequent episodes of syncope. For 15 years prior to admission she had occasional episodes of transient numbness and weakness of the right arm and leg, a slight loss of skilled movements of her right fingers, and periods during which she had difficulty in finding ‘the right word’. On examination she had mild right hemiparesis and expressive dysphasia. A lumbar puncture revealed high opening pressure without xanthochromia. A percutaneous carotid angiogram on the left side was made 10 h after admission, and one was made on the right side 2 days later … the angiogram on the left side revealed a large arteriovenous malformation intimately involving the areas of motor, speech whereas the angiogram of the right side showed virtually no contribution to the malformation. The middle cerebral trunk on the left side was increased in diameter to about 5 mm up to its point of division (figure 2A). Over the next 8 h the patient’s headache and weakness improved with worsening of dysphasia. On September 18, 7 days after admission, a left common carotid bifurcation was exposed under local anesthesia. Four spherical emboli, made of methyl methacrylate, were introduced at intervals of about 15 min. They measured successively about 2.5, 3.0, 4.0, and 4.2 mm in maximum diameter. After introduction of each embolus, the strength of the right arm and speech were tested and X-rays were taken to determine the site of arrest. Immediately after introduction of the fourth embolus the patient became drowsy and showed increasing weakness of the right hand but no alteration of speech. The angiogram made shortly thereafter … malformation was reduced to a slight stain and, for the first time, normal filling of the anterior and middle cerebral arteries was evident. The emboli, identifiable by metallic fragments within the plastic coating, had come to arrest at the beginning of the malformation. The patient developed transient worsening of her weakness which improved over the next 14 h. At 7 weeks after surgery she was able to write legibly with her right hand. At no time during her postoperative course was there any recurrence of her dysphasia or loss of cortical sensory function. Skull X-rays taken 5 days after surgery showed that the fourth embolus, represented by the large round fragment, had moved to a position closer to the malformation. This embolus, being larger than the others, had temporarily lodged too far proximal to the malformation and had thereby caused her transient neurological defect. The follow-up angiogram of the left carotid artery, made 26 days after surgery, showed excellent filling of the normal arteries and only a remnant of the malformation persisted (figure 2B). J Am Med Assoc 1960;172:1153–5. Case 1 A 33-year-old housewife and waitress was diagnosed with an AVM supplied primarily by enlarged Sylvian branches and penetrating branches from the middle cerebral trunks. Dr Luessenhop used 30 spherical Silastic emboli like those he used in his previous method and was able to eliminate a larger portion of the Sylvian contribution. For the residue, in the second stage, he introduced a 2.5 mm and then a 3 mm Maiti TK, et al. J NeuroIntervent Surg 2014;0:1–5. doi:10.1136/neurintsurg-2014-011532

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History Figure 2 Images of first embolization. (A) Lateral view of preoperative arteriogram showing malformation. (B) Arteriogram made 26 days after surgery; remnant of malformation persists. Published with permission from Luessenhop and Spence.1

embolus attached to a 4–0 silk suture. In the third stage he repeated the procedure with 3.5 mm emboli. The patient did well and was able to return to work.

Case 2 A 51-year-old housewife was diagnosed with a large AVM with an aneurysm at the junction of the posterior communicating artery and the right internal carotid artery, the major feeding artery to the malformation. These lesions were judged inoperable. Dr Luessenhop found the nidus occupied the right posterior frontal area. A catheter consisting of delicate flexible Silastic tubing with an enlarged inflatable tip was then introduced and the tip was maneuvered to the intraluminal

orifice of the saccular aneurysm and inflated with 50% Hypaque. An angiogram with the catheter in place showed that the diameter of the artery had increased at the site of the balloon, thus permitting passage of the medium around it and a faint filling of the aneurysm. As the maximum safe inflation of the tube was attained, further distention and complete occlusion could not be achieved. The patient developed a transient neurologic deficit which improved within the next 6 months.

Case 3 A 31-year-old housewife was admitted with subarachnoid hemorrhage and soon became bilaterally decerebrate. Bilateral

Figure 3 Images of first catheterization of intracranial arteries. (A) External glass catheterization chamber. (B) Arteriogram showing a saccular aneurysm arising from the internal carotid artery at approximately the origin of the ophthalmic artery (left). Arrow shows metallic marker in an embolus situated at the intraluminal orifice of the aneurysm (right). (C) Angiogram showing embolus in place at the orifice of the saccular aneurysm. The decreased contrast filling of the distal arteries is probably secondary to dilution of the medium in the glass bulb. Published with permission from Luessenhop and Velasquez.12

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History carotid angiograms showed a saccular aneurysm at the junction of the internal carotid and ophthalmic arteries on the left, 3 mm distal to the anterior crinoid process (figure 3B). About 12 h after admission the bifurcation of the left common carotid artery was exposed and the catheterization bulb was joined to the external carotid artery. As the preliminary maneuver, a spherical Silastic embolus 2.5 mm in diameter with an attached suture was introduced to measure the precise distance to the aneurysmal orifice. When the embolus was held stationary at the intraluminal orifice, it passed into the neck of the aneurysm. Angiography immediately thereafter showed contrast medium passing the site of the aneurysm and filling the intracranial arteries without filling the aneurysm (figure 3C). However, the patient died and at autopsy there was an adherent clot in the neck of the aneurysm but the dome of the aneurysm was not clotted. There was no obstruction to flow through the parent circulation. With the success of these procedures Dr Luessenhop wrote: “Catheterization as well as embolization of the intracranial arteries may have therapeutic usefulness, particularly in the treatment of aneurysms and AVMs”.12

DAYS OF AUTOMATIC COMPUTERIZED TRANSVERSE AXIAL (ACTA) SCANNER Dr Luessenhop also made a significant contribution by being a crucial member of the team which used the automatic computerized transverse axial (ACTA) scanner. It is regarded as the first commercially available whole-body scanner and is recognized as a key step in the revolution of the CT scan, thus changing the history of imaging (figure 4).14 15 Ledley, the inventor of the ACTA scanner, acknowledged Dr Luessenhop for his constant support and willingness to use it.16 His other publications also reflect his attraction for newer modalities of neuroimaging.17–19

FIRST AND FOREMOST A NEUROSURGEON Along with performing numerous embolization procedures, Dr Luessenhop continued to practice conventional neurosurgery. In December 1986 he led the neurosurgery team that removed a tumor from the brain of CIA Director William J Casey in a 5 h operation. He also treated many Washington Redskins players, including Dexter Manley, Mike Bass and Pat Fischer. Dr Luessenhop also contributed to the fields of functional, epilepsy, pediatric and spinal neurosurgery.20–22 However, he was

fascinated by AVMs and their multimodal management and by other topics in vascular neurosurgery. A Pubmed search yielded 48 articles of which more than half were on various topics of vascular neurosurgery. He also wrote many book chapters.23 In 1977 he proposed a simple grading system for supratentorial AVMs based on the number of participating arteries which are of sufficient anatomic constancy and size.24 Later he included the size of the AVM with grades I, II, III, and IV representing AVMs of 6 cm, respectively. He also proposed the indications for and the results of surgery, and the role of intravascular techniques based on his classification.25 Although this article has been cited 72 times to date, a grading system introduced by Dr Spetzler a few years later in 1986 gained wider acceptance.26

LEGACY With due respect to previous authors, the 1960s can safely be designated as the time when the specialty of endovascular neurosurgery saw its early blossoming. The contributions of other authors in those early days also deserve a mention.27 The thrombosis of aneurysms was tried using magnets and iron spheres by Alksne and Fingerhut28 29 and electric current was used by Mullan et al.30 31 In 1974 the field of endovascular neurosurgery got a huge boost when Dr Serbinenko, a neurosurgeon from the Burdenko Neurosurgical Institute in Moscow, published his paper on the endovascular treatment of more than 300 patients using detachable and non-detachable balloons.32 Dr Debrun from France also contributed with his pioneer works on inflatable and detachable balloons in the early 1970s.33 34 When analyzing all the initial events of this developing discipline, the modern stalwarts of endovascular neurosurgery have acknowledged the legacy of Dr Luessenhop. In describing the endovascular revolution, Dr G Guglielmi,35 the inventor of the Guglielmi detachable coil, started his discussion with the contribution of Dr Luessenhop in endovascular navigation. Tarr,36 while addressing the future directions, paid tribute to the equally important pioneer works of Serbinenko and Luessenhop. Apart from his revolutionary work, he was also successful in generating enough interest in his students who contributed significantly to the further development of this specialty.37 History lovers will find Dr Luessenhop’s article, “Interventional Neuroradiology: a Neurosurgeon’s Perspective”, to be visionary.38 In this article he documented the efficacy of interventional neuroradiology at that time. He polled 75 directors of neurosurgical programs in the USA with a questionnaire and his results showed the complex relationship between interventional neuroradiology and neurosurgical practice. He also showed the future direction of interventional neuroradiology by suggesting the following proposals: to make structured fellowships mandatory for the interventionist; the criteria for the success of the procedures should be made more rigid; and, most importantly, close integration of neurosurgeons with interventionists should be established to reduce the risk for the patient.

CONCLUSION

Figure 4 The 0100 automated computerized transverse axial (ACTA) scanner, the world’s first whole-body scanner. Published with permission from Sittig et al.16 4

Dr Alfred J Luessenhop performed the first successful embolization of a cranial AVM and the first catheterization of intracranial arteries to occlude an aneurysm. These landmark procedures sowed the seeds of modern endovascular neurosurgery. By becoming a pioneer in the field, he answered the much discussed question at its very beginning as to whether or not a neurosurgeon should become an interventional neuroradiologist. With so many ‘firsts’ associated with his name, Dr Luessenhop can surely be considered as the ‘Father of Endovascular Neurosurgery’. Maiti TK, et al. J NeuroIntervent Surg 2014;0:1–5. doi:10.1136/neurintsurg-2014-011532

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History Contributors TM and SB conceived and designed the study and took part in preparing the manuscript. PB and AN contributed to the review. Competing interests None.

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Provenance and peer review Not commissioned; externally peer reviewed. Data sharing statement Data sharing can be performed with simple letter agreement.

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Luessenhop AJ, Spence WT. Artificial embolization of cerebral arteries. Report of use in a case of arteriovenous malformation. J Am Med Assoc 1960;172:1153–5. Sullivan P. Alfred J. Luessenhop, Pioneering Georgetown U. Neurosurgeon. Washington Post Staff Writer 2009 Mar 6. Carter BS, David C. AANS/CNS Joint Cerebrovascular Section Newsletter. Winter 2009. Brooks B. The treatment of traumatic arteriovenous fistula. South Med J 1930;23:100–6. Vitek JJ, Smith MJ. The myth of the Brooks method of embolization: a brief history of the endovascular treatment of carotid-cavernous sinus fistula. J Neurointerv Surg 2009;1:108–11. Hamby WB, Gardner WJ. Treatment of pulsating exophthalmus with report of two cases. Arch Surg 1933;27:676–85. Steegmann AT, De La Fuen J. Experimental cerebral embolism. II. Microembolism of the rabbit brain with seran polymer resin. J Neuropathol Exp Neurol 1959;18:537–58. Swank RL, Hain RF. The effect of different sized emboli on the vascular system and parenchyma of the brain. J Neuropathol Exp Neurol 1952;11:280–99. Spence WT. Form-fitting plastic cranioplasty. J Neurosurg 1954;11:219–25. Laws ER Jr. William T. Spence (1908–1992). Neurosurgery 1992;30:971. Luessenhop AJ, Gibbs M, Velasquez AC. Cerebrovascular response to emboli. Observations in patients with arteriovenous malformations. Arch Neurol 1962;7:264–74. Luessenhop AJ, Velasquez AC. Observations on the tolerance of the intracranial arteries to catheterization. J Neurosurg 1964;21:85–91. Rosenbluth PR, Grossman R, Arias B. Accurate placement of artificial emboli. A problem in the treatment of cerebral angiomas by the embolization method. JAMA 1960;174:308–9. Ledley RS. Introduction to computerized tomography. Comput Biol Med 1976;6:239–46. Luessenhop AJ, Axelbaum SP, Schellinger D, et al. [Design and clinical experience with ACTA scanner (whole body automatic computerized transeverse axial tomographic scanner)]. Rinsho Hoshasen 1976;21:163–8. Sittig DF, Ash JS, Ledley RS. The story behind the development of the first whole-body computerized tomography scanner as told by Robert S. Ledley. J Am Med Inform Assoc 2006;13:465–9. Curl FD, Harbert JC, Luessenhop AD, et al. Radionuclide cerebral angiography in a case of bilateral carotid-cavernous fistula. Radiology 1972;102:391–2. Luessenhop AJ, Sweet WH, Robinson J. Possible use of the neutron capturing isotope lithium in the radiation therapy of brain tumors. Am J Roentgenol Radium Ther Nucl Med 1956;76:376–92.

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McCullough DC, Luessenhop AJ. Evaluation of photoscanning of the diffusion of intrathecal RISA in infantile and childhood hydrocephalus. J Neurosurg 1969;30:673–8. Luessenhop AJ. Thalamotomies and other stereotaxic surgery in childhood. Clin Proc Child Hosp Dist Columbia 1966;22:293–302. Luessenhop AJ. Interhemispheric commissurotomy: (the split brain operation) as an alternate to hemispherectomy for control of intractable seizures. Am Surg 1970;36:265–8. Manz HJ, Luessenhop AJ, Robertson DM. Cervical myelopathy due to atlantoaxial and subaxial subluxation in rheumatoid arthritis. Arch Pathol Lab Med 1983;107:94–8. Luessenhop AJ. Surgical treatment for deep-seated or large AVMs. Advances in Surgery for Cerebral Stroke: Proceedings of the International Symposium on Surgery for Cerebral Stroke, Sendai 1987. Berlin: Springer-Verlag, 1988:467–74. Luessenhop AJ, Gennarelli TA. Anatomical grading of supratentorial arteriovenous malformations for determining operability. Neurosurgery 1977;1:30–5. Luessenhop AJ, Rosa L. Cerebral arteriovenous malformations. Indications for and results of surgery, and the role of intravascular techniques. J Neurosurg 1984;60:14–22. Spetzler RF, Martin NA. A proposed grading system for arteriovenous malformations. J Neurosurg 1986;65:476–83. Horowitz MB, Levy E, Kassam A, et al. Endovascular therapy for intracranial aneurysms: a historical and present status review. Surg Neurol 2002;57:147–58. Alksne JF, Fingerhut AG. Magnetically controlled metallic thrombosis of intracranial aneurysms. A preliminary report. Bull Los Angeles Neurol Soc 1965;30:153–5. Alksne JF. Stereotactic thrombosis of intracranial aneurysms using a magnetic probe. Confin Neurol 1969;31:95–8. Mullan S, Beckman F, Vailati G, et al. An experimental approach to the problem of cerebral aneurysm. J Neurosurg 1964;21:838–45. Mullan S, Raimondi AJ, Dobben G, et al. Electrically induced thrombosis in intracranial aneurysms. J Neurosurg 1965;22:539–47. Serbinenko FA. Balloon catheterization and occlusion of major cerebral vessels. J Neurosurg 1974;41:125–45. Debrun G, Lacour P, Caron JP, et al. [Treatment of arteriovenous fistulas and of aneurysms using an inflatable and releasable balloon. Experimental principles. Application to man]. Nouv Presse Med 1975;4:2315–18. Debrun G, Coscas G. [Treatment of carotido-cavernous fistulas and intracavernous aneurysms by means of a balloon catheter, which can be inflated and enlarged]. Bull Soc Ophtalmol Fr 1975;75:857–64. Guglielmi G. History of endovascular endosaccular occlusion of brain aneurysms: 1965–1990. Interv Neuroradiol 2007;13:217–24. Tarr RW. Personal reflections on the future directions of endovascular neurological intervention. In: Maciunas RJ. ed. Endovascular neurological intervention. 1st edn. Thieme, 1995:285–8. Alexander MJ. Preface. In: Alexander MJ, Spetzler RF, eds. Pediatric neurovascular disease: surgical, endovascular and medical management. 2006:xi–xii. Luessenhop AJ. Interventional neuroradiology: a neurosurgeon’s perspective. AJNR Am J Neuroradiol 1990;11:625–9.

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Alfred J Luessenhop and the dawn of a new superspecialty: endovascular neurosurgery Tanmoy Kumar Maiti, Shyamal Chandra Bir, Papireddy Bollam and Anil Nanda J NeuroIntervent Surg published online December 24, 2014

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Alfred J Luessenhop and the dawn of a new superspecialty: endovascular neurosurgery.

Endovascular neurosurgery, or interventional neuroradiology, has developed rapidly over the last 50 years and has posed a challenge to the established...
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