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PVSXXX10.1177/1531003513517010Perspectives in Vascular Surgery and Endovascular TherapyTallarita et al
Article
History of Carotid Surgery: From Ancient Greeks to the Modern Era
Perspectives in Vascular Surgery and Endovascular Therapy 2014, Vol. 25(3-4) 57–64 © The Author(s) 2013 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/1531003513517010 pvs.sagepub.com
Tiziano Tallarita, MD1, Maurizio Gerbino, PhD2, Carmelina Gurrieri, MD3, and Giuseppe Lanzino, MD1
Abstract A relationship between decreased carotid arterial flow and apoplectic manifestations was already suspected by the ancient Greeks. Early attempts at carotid surgery, however, were limited to emergency arterial ligation in patients with neck trauma. Attempts to suture arterial stumps together to restore blood flow paved the way for Carrel’s revolutionary idea of reconstructing the resected or injured arterial segment with an interposition vein graft. DeBakey and Eastcott were the first to perform carotid endarterectomy in North America and the United Kingdom, respectively. In 1959, DeBakey proposed a cooperative study to assess the effectiveness of carotid endarterectomy in the treatment and prevention of ischemic cerebrovascular disease. The study was officially designated the Joint Study of Extracranial Arterial Occlusion and represented the first trial in the United States in which large numbers of patients were randomly allocated to surgical or nonsurgical therapy. Keywords carotid endarterectomy, carotid surgical history, stroke, transient ischemic attack
Introduction Extracranial atherosclerosis affects the carotid arteries in approximately 1% of the general population older than 60 years.1 Efficient diagnostic tests are used for the diagnosis of extracranial carotid disease, and effective medical, surgical, and endovascular therapies are available for its treatment. Carotid endarterectomy, in particular, has been established as the standard of treatment for carotid stenosis in patients with symptomatic disease and for selected patients with asymptomatic stenosis. The development of carotid surgery, however, has been the result of a slow and progressive process through the efforts of several pioneers and has been characterized by alternating successes and setbacks. In this review, we describe the development of carotid surgery from early attempts at emergency arterial ligation in patients with trauma to the modern reconstructive era.
Carotid Surgery Hippocrates of Kos lived between the fifth and fourth centuries bc. He traveled throughout Greece after the Peloponnesian War, curing people affected by plague that spread because of the poor hygienic conditions established after the conflict. In the same period, he was the first to study the carotid artery circulation and explained
the term apoplexia as “to be struck with violence.”2,3 The ancient Greeks believed that there was a relationship between carotid arterial flow and apoplectic manifestations. Indeed, the term carotid derives from the Greek word karoo, which means “to stupefy” or “to fall asleep.”4 There was a lack of understanding, however, of the pathophysiology associated with impairment of carotid circulation. The first surgical treatments for carotid disease were emergency procedures in patients with neck injuries. In France, the celebrated surgeon Ambrose Paré, who was appointed surgeon to King Henry II, may have performed the first recorded surgical ligation of the carotid artery in 1551. “It was an enthusiastic desire of learning his profession that induced Paré to follow the French armies while yet very young.”5 During a battle, it was necessary to quickly control bleeding from the carotid artery of a wounded soldier, and Paré accomplished this by ligation of the carotid artery (Figure 1). Paré’s writings, however, 1
Mayo Clinic, Rochester, MN, USA University of Siena, Siena, Italy 3 University of Catania, Catania, Italy 2
Corresponding Author: Giuseppe Lanzino, MD, Department of Neurologic Surgery, Mayo Clinic, 200 First Street SW, Rochester, MN 55905, USA. Email: [email protected]
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Figure 1. Carotid artery ligation for internal carotid artery aneurysm.
Adapted from Bell C. Illustrations of the great operations of surgery: trepan, hernia, amputation, aneurism, and lithotomy. London, ca 1821.
did not provide a clear and detailed description of the operation. Thus, there is controversy about whether he indeed was the first to perform such an operation. One century later, the Civil War in England led to the expansion of Thomas Willis’s (personal physician to King Charles I) surgical experience. In his landmark contribution, Willis provided an anatomical explanation for the absence of complications after acute ligation of the internal carotid artery by observing passage of an injected staining solution from one carotid to the other through collateral channels: “the Carotid of one side might provide for either Province . . . Further, if both the Carotids should be stopt, the office of each might be supplied through the Vertebrals.”6 Probably unaware of Willis’s findings, Fleming, a naval surgeon, in 1803, provided a detailed description of a therapeutic common carotid artery ligation to arrest a lethal hemorrhage. In Fleming’s case, the patient had a self-inflicted penetrating neck injury.7 Following Hunter’s and others’ experiences with proximal ligation to treat peripheral aneurysms,8 surgeons started applying the same strategy to the treatment of carotid aneurysms in the neck. Toward the end of the 18th century and the beginning of the 19h century, Sir Astley Cooper (Figure 2) is credited as being the first to perform a carotid ligation for treatment of an aneurysm. He wrote, Mary Edwards, aged 44, was brought to my house by Mr. Robert Pugh of Gracechurch Street, that I might examine a tumor in the neck which was obviously an aneurysm of the right carotid artery . . . When the swelling was examined at the hospital, great doubts were entertained if there were sufficient space between the clavicle and the tumor for the application of a ligature.9
Her carotid artery was successfully ligated, but she died 1 week later due to mass effect on the pharynx and trachea
Figure 2. Sir Astley Cooper.
Adapted from Cooper, Life of Sir Astley Cooper, London, 1843.
caused by an inflammatory reaction in the large aneurysmal sac after carotid ligation. Showing a trait common to many surgical pioneers, Cooper persisted in his efforts despite his first disappointing experience. Three years later, another attempt was successful: A blunt iron probe constructed for the purpose was then passed under the artery, carrying a double ligature with it. Two ligatures being thus conveyed under the artery the lower was immediately tied. I next detached the artery from the surrounding parts to the extent of an inch above the lower ligature, and then tied the upper. Lastly, a needle and thread were passed through the artery above one ligature and below the other. The division of the artery was then performed.10
The patient recovered and returned to work. Several other reports of carotid surgery ensued, and in 1860, Ehrmann analyzed the results of 281 carotid ligation operations, noting high mortality after this procedure.11 A few years later, a mortality rate of 43% was reported based on an analysis of 600 cases of carotid ligation.12 Even in those earlier days, this mortality rate was felt to be too high. These early and less-than-ideal results encouraged surgeons of the time to seek alternative reconstructive procedures. Murphy reported invaginating one cut arterial end into another, in an end-to-end fashion, and used partial-thickness sutures to hold them in place (Figure 3).13 Jaboulay and Brian14 used an interrupted U-shaped suture to reunite the carotid arteries of donkey and dogs, and Doerfler described creating anastomoses
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It is important that this preliminary occlusion be made while the patient is fully conscious in order to obtain prompt information of the cerebral effects of the interruption of the blood current in the brain as these manifestations often appear the moment the occlusion takes place.17
In the same year, James Ramsay Hunt described the syndrome of occlusion of the internal carotid artery. He emphasized the importance of examination of the neck vessels in all cases presenting with cerebral symptoms of vascular origin: “for this purpose a section of the carotid artery is readily accessible to palpation, extending from the lower border of the thyroid cartilage to the angle of the jaw.”13 Furthermore, he observed that while inequality of pulsation on the two sides might be accidental, its occurrence in four cases all presenting the symptoms of extensive brain softening is rather significant, and the thought naturally arises that some obstructive lesion of the vessel or its entrance into the arch of the aorta has interfered with the free flow of blood to the brain.13
Figure 3. Murphy’s illustration of the technique used for the first successful clinical end-to-end arterial anastomosis. Adapted from Murphy JB. Resection of arteries and veins injured in continuity–end-to-end suture–experimental and cultural research. Med Rec. 1897;51:73.
with fine silk and a curved round needle.13 The latter demonstrated that it was possible to suture 2 vessel stumps with accurate approximation of all vessel wall layers without ensuing thrombosis. Furthermore, Doerfler stressed the great importance of adherence to the principles of aseptic technique to achieve good results.13 These attempts paved the way for Carrel’s (Figure 4A) revolutionary idea of reconstructing the resected segment with an interposition vein graft. He stated, “In such cases it would be possible to extirpate freely all the injured portions of the vessel and to re-establish the circulation by interposing a segment of vein between the cut ends of the artery” (Figure 4B).13 Further developments in carotid surgery were related to ongoing efforts to clarify the relationship between carotid artery disease and cerebral ischemia. The famous pathologist from Prague, Chiari, demonstrated a link between carotid stenosis and transient ischemic attack or stroke. He described ulcerating carotid plaques and suggested that emboli could break off from these plaques with resulting distant infarction.15 In a seminal contribution in 1914, the New Orleans surgeon Rudolf Matas (Figure 5) described a compression test of the carotid artery to assess the efficiency of collateral circulation while planning carotid artery ligation.16 He stated,
During the years of World War I, an increasing number of carotid injuries could be seen due to assault with bayonets and close combat. In this period, the field of reconstructive carotid surgery was further advanced by the reports of Von Parczewski who, in 1916, resected an arteriovenous aneurysm of the common carotid artery and restored continuity with an end-to-end anastomosis,18 and by von Haberer, Lexer, and Denck, who performed many end-to-end anastomoses in soldiers during the conflict.19 The revolutionary introduction of angiography provided in vivo documentation of carotid occlusive disease and gave further impetus to the development of surgical procedures in order to avoid its deleterious consequences. In Portugal, Egas Moniz developed cerebral angiography as a method to localize brain tumors in 1927 (Figure 6). Ten years later, Moniz described 4 cases of internal carotid occlusion associated with hemiplegia. In these patients, carotid occlusion was documented on angiography. He concluded, La thrombose de la carotide interne, bien que rare, est, cependant, plus frequente qu’on ne l’ avait pensé. . . . Nous pouvons dire que la thrombose de la carotide interne représente 0,8 pour 100 des malades chez lesquels nous avons fait l’artériographie cérébrale. Si nous l’avions faile sur une série de cas d’hémiplégies, le pourcentage serait certainement plus élevé. [Thrombosis of the internal carotid artery, although rare, is, however, more frequent than one would have thought. . . . We can say that thrombosis of the internal carotid was found in 0.8 per 100 patients in whom we performed cerebral arteriography. If we had used a series of cases of hemiplegia, the percentage would certainly be higher]20
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Figure 4. Carrel’s interposition vein graft. (A) Alexis Carrel. (B) (Top) Venous interposition graft by Carrel and Guthrie and (bottom) end-to-end anastomosis of vein graft into arterial circulation.
Figure A courtesy of the Rockefeller Archive Center, Sleepy Hollow, New York. Used with permission. Figure B adapted from Carrel A, Guthrie CC. Uniterminal and biterminal venous transplantation. Surg Gynecol Obstet. 1906;2:266.
Figure 5. Portrait of Matas by Thomas C. Corner.
Courtesy of the Rudolph Matas papers, Louisiana Research Collection, Tulane University, New Orleans, Louisiana. Used with permission.
In the 1930s in China, Chao and associates reported 2 cases of carotid occlusion treated with denervation of the
proximal carotid artery and excision of the thrombosed segment with the purpose of interrupting the “sympathetic impulses in the walls of the artery,” as described by the great French surgeon Leriche in the treatment of occlusive femoral disease.21 One of these 2 cases involved a 47-year-old Russian woman who worked as a switch operator on the Chinese Eastern Railway. Her eyesight had been impaired by recurrent emboli from a left carotid plaque. One day “she threw a switch the wrong way and caused the wreck of a locomotive and seven empty freight cars.”22 She underwent surgery with uneventful outcome. The second case was a 27-year-old Chinese mathematics student who could not read Chinese characters after a stroke. In both cases, after surgical intervention, improvement of their “mental functions” was observed. This led Chao to conclude that “excision of the thrombosed artery should be carried out.”22 As often happens in the history of surgical techniques, increasing experience with carotid surgery led to some abuses and the development of “fancy” procedures based on sketchy theoretical background. Along these lines, Sciaroni23 proposed the concept of “reversal of the circulation of the brain.” The background for his operation was the idea that a jugular-carotid fistula would reduce the perfusion within the carotid sinus with resulting increased levels of carbon dioxide. The effects of both reduced sinus perfusion and increased local carbon dioxide concentration would eventually lead to an increase in the cerebral perfusion pressure and blood flow, accompanied by peripheral vasoconstriction. Thus, in 1948, he
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plaque from the femoral artery with a “loop stripper” through one or more transverse or longitudinal arteriotomies. L’artère fut décourverte de l’arcade au canal de Hunter. Elle fut incise longitudinalement sur 2 centimètres à chaque extrémité. Un plan de clivage fut aisément trouvé entre le thrombus et la paroi. Avec une spatule mousse et un stylet, une bonne partie du caillot fut libéré en bas et en haut. Il tenait encore à la partie moyenne de l’artère [. . .] lui imprima quelques mouvements de rotation et finalement il fut enlevé en presque totalité. [The artery was dissected at the level of the adductor canal. It was incised longitudinally for 2 centimeters at each end. A cleavage plane was easily found between the thrombus and the wall. With a blunt spatula and a stylus, a great amount of the clot was released in the top and bottom parts of the artery. Clot remained in the middle part of the artery [. . .]. After applying some rotational movements, almost all of the clot was finally removed]24
Figure 6. Cerebral angiograms showing internal carotid occlusion (top) and stenosis (bottom). Adapted from Moniz et al.20 Used with permission.
suggested that an arteriovenous fistula between the common carotid artery and the internal jugular vein through a side-to-side anastomosis would relieve symptoms of paralysis and epileptic seizures. Despite initial enthusiasm, results were not encouraging, and several years later this operation fell into disrepute.23
The Birth of Modern Carotid Endarterectomy The development of modern carotid endarterectomy was the result of continuous, onward evolution. The progression in carotid artery surgery for the prevention and care of ischemic cerebrovascular disease was often the extension of experience already accumulated with interventions in the peripheral circulation. In 1947, the Portuguese surgeon Cid Dos Santos showed that it was possible to remove a long occluding thrombus along with underlying
He is credited to be the father of endarterectomy as performed today. Dos Santos observed that since the atheroma is usually at the intima level, it is possible to easily find a cleavage plane between the diseased and nondiseased arterial wall. He also noted that, at times, a marked discontinuity could be seen between the intima and media at the distal point of the lesion, which needed to be beveled to minimize the risk of postoperative thrombosis. Otherwise, if the distal point of the endarterectomy had only lost adhesion to the underlying media, it could be secured with fine “tacking” sutures tied externally.24 After the early reports of Dos Santos, studies in the Experimental Surgical Laboratory of the University of California School of Medicine demonstrated the process of intimal regeneration after excision of the internal lining of the aorta in dogs.25,26 Some authors consider Bazy and Reboul to be the actual fathers of carotid endarterectomy. These 2 French surgeons, applying the Dos Santos technique of endarterectomy to carotid stenosis, performed a longitudinal arteriotomy as long as the atheroma, followed by the removal of the plaque and direct suture. Unfortunately, there are no clear references supporting the claims of these authors, generating doubts about the authenticity of the claim. The surgeons DeBakey27 (Figure 7) and Eastcott28 have often been credited as being the first to perform carotid endarterectomy in North America and in the United Kingdom, respectively. In DeBakey’s case, the diagnosis of carotid stenosis was made by angiography, which revealed a large “atheromatous plaque . . . at the origin of the internal, as well as the external, carotid artery,” with a fresh clot partially filling the residual lumen of the common carotid artery.27 DeBakey
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Figure 7. Michael DeBakey.
Adapted from Wikipedia. Available from: http://en.wikipedia.org/ wiki/File:Michael_E._DeBakey.jpeg. In the public domain. Courtesy of University of Houston Libraries.
published this case in 1975 and reported that the patient survived for 19 years without recurrence of cerebrovascular insufficiency until fatal heart failure occurred. The specifics surrounding the details of this operation are controversial, however, because the medical record of this patient was never found.29 In a similarly celebrated operation, Eastcott et al28 in 1954 restored continuity of flow by direct anastomosis between the common carotid artery and the stump of the internal carotid artery, after the removal of the atheromatous plaque at the carotid bifurcation. The carotid artery was clamped for 28 minutes, and good pulsation was observed in the vessels after removal of the clamps. Anticoagulants were not used.28 These early encouraging results led other surgeons to advocate for the application of surgical management of the involved carotid artery during neck surgery for neoplastic diseases. In the early 1950s, New York surgeon John J. Conley (Figure 8) performed a large series of operations on neoplasms of the neck. During these interventions, he often removed portions of the internal and common carotid arteries, followed by end-to-end anastomosis of the distal stumps of the internal and external carotid arteries. Only a few of these mattress sutures of 0000 silk on atraumatic needles are necessary to approximate the cut ends of the arteries, depending, of course, on the diameter of the lumens. If the diameter of one of the carotid arteries is larger than the other, this disproportion may be overcome by cutting the artery with the small diameter in an oblique manner, thus increasing its overall circumference.30
Figure 8. John J. Conley.
Adapted from American Head & Neck Society Past Presidents webpage. Available from: http://www.ahns.info/about-ahns/past_ presidents/conley. In the public domain. Courtesy of American Head & Neck Society.
Subsequently, he introduced the interposition saphenous vein bypass between the common and internal carotid arteries, with favorable results.30 In the same period, Strully et al31 published the first attempt to reopen an acute carotid thrombosis in which the thrombus extended to the intracranial carotid artery. A 2-cm longitudinal incision was made at the point of transition in the affected vessel, and a thrombus partially extruded itself through the opening. . . . With suction applied to the catheter at all times it was possible to remove additional thrombus. A total of 7 cm of clot was removed. . . . Retrograde flow of blood could not be obtained. Several attempts to remove the intracranial portion of the clot were unsuccessful. Because of the danger of dislodging clot in the intracranial portion of the internal carotid artery when the common artery clamp was removed, the vessel was occluded by transfixion ligatures and 2 cm portion was removed.31
Although it had been suspected, a clear-cut causal relationship between carotid steno-occlusive disease and ipsilateral ischemia was not uniformly accepted until Miller C. Fisher’s seminal description of 8 cases of obstruction of the carotid artery.32,33 In these reports, Fisher speculated that hemorrhagic infarction was often the result of embolism from carotid thrombosis: Later, due to fragmentation of the embolic material and possibly to relaxation of local vascular spasm, the embolus moves from its original position into more distal branches. This exposes the necrotic tissue to the full force of arterial
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Encouraged by increased understanding of the pathophysiology of cerebral ischemia, other surgeons tried to surgically reopen the carotid artery in cases of complete occlusion. Denman et al34 used lyophilized homografts to replace occluded carotid segments, with excellent results: 26 years after bilateral carotid arterial grafting, the patient, a 60-year-old woman, was still symptom free. In 1955, Carrea et al35 reconstructed an occluded internal carotid artery in a 41-year-old man with convulsions, aphasia, left eye blindness, and hemiparesis. “The internal carotid artery was cut about 5 mm above the abnormal area, the external carotid was also cut at the same level and the proximal carotid was anastomosed end-to-end to the distal portion of the internal carotid.”35 Postoperative vessel patency was confirmed angiographically. Three conditions had to be met, according to Carrea et al,35 to be able to perform this procedure: (a) the occlusion must be localized at the proximal portion of the internal carotid artery, (b) the diameter of the internal carotid artery must be large enough to allow for an adequate anastomosis, and (c) both portions of the internal and common carotid arteries to be anastomosed must be free of atherosclerotic plaques. Later refinements in carotid endarterectomy led to the procedure as we know it today. To reduce the ischemia time during carotid cross-clamping, in 1956, Cooley et al36 introduced a polyvinyl extravascular shunt to bypass the carotid stenosis, reducing the neurologic complications linked to temporary cerebral hypoperfusion. In their case report, brain protection during clamping was afforded with intravenous Pentothal (thiopental sodium) and “cooling of the cranium and brain [by] immersing the head in crushed ice.” After dissection of the carotid bifurcation, “a polyvinyl shunt, with needle points at both ends, was used to by-pass the carotid circulation during the period of occlusion.”36
Carotid Endarterectomy Becomes the Most Widely Studied Surgical Procedure At a meeting held in January 1959 in Washington, DC, Michael E. DeBakey, inspired by Fisher’s work, proposed a cooperative study to assess the effectiveness of carotid endarterectomy in the treatment and prevention of ischemic cerebrovascular disease. The study was officially designated the Joint Study of Extracranial Arterial Occlusion. The results were published in a series of articles in the Journal of the American Medical Association.37 The study concluded that “results of surgery are most
favorable in patients with transient ischemic attack or minor neurologic deficits in whom stenosis rather than occlusion of the extracranial arteries is found.”37 The Joint Study also led to better standardization of the methods for measurement of stenosis, definition of surgical contraindications, and characterization of various patient subgroups.38,39 This was the first trial in the United States in which a large number of patients was randomly allocated to surgical or nonsurgical therapy. The following years were characterized by a progressive increase in the number of carotid endarterectomies both for asymptomatic and symptomatic disease. This rapid increase led some to question the validity and efficacy of the procedure as it was being performed. Numerous large trials on carotid endarterectomy were subsequently conducted, which eventually would make carotid endarterectomy the most-studied surgical procedure, the indications for and efficacy of which are now based on the highest level of scientific evidence. Declaration of Conflicting Interests The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding The authors received no financial support for the research, authorship, and/or publication of this article.
References 1. de Weerd M, Greving JP, Hedblad B, et al. Prevalence of asymptomatic carotid artery stenosis in the general population: an individual participant data meta-analysis. Stroke. 2010;41:1294-1297. 2. De la maladie sacrée 9 (L. 6:378 and 379); Prorrhetique, 118 (L. 5: 550 and 551); Des airs, des eaux et des lieux, 3 (L. 2:18 and 19). 3. Parr B. The London Medical Dictionary (Including, under distinct heads, every branch of medicine, viz. anatomy, physiology, and pathology, the practice of physic and surgery, therapeutics, and material medica; with whatever relates to medicine in natural philosophy, chemistry, and natural history). Vol. 2. Philadelphia: Mitchell, Ames, & White; 1819:105. 4. McHenry LC Jr. Garrison’s History of Neurology. Springfield, IL: Charles C. Thomas; ca 1969. 5. Baldwin, Cradock and Joy. The Retrospective Review. Ambrose Parey’s Works. Vol. XI (The works of that famous chirurgeon Ambrose Parey: translated out of Latin and compared with the French by Thomas Johnson [1634].) London; 1825:43. 6. Willis T. Cerebri Anatome. London, England: Roycroft, Martyn &Allestry; ca 1664:93-94. 7. Kleevil JJ. David Fleming and the operation for ligation of the carotid artery. Br J Surg. 1949;37(145):92-95.
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8. Sloffer CA, Lanzino G. Historical vignette: Dominique Anel: father of the Hunterian ligation? J Neurosurg. 2006;104:626-629. 9. Society of Physicians, ed. The Eclectic Repertory and Analytical Review: Medical and Philosophical. Philadelphia, PA: Finley; ca 1811. 10. Brock RC. Astley Cooper and carotid artery ligation. Guys Hosp Rep. 1968;117:219-224. 11. Hamby WB, Wilson WJ. The exorcism of a surgical literary ghost. Surg Gynecol Obstet. 1955;101:772-778. 12. Pilz C. Zur ligature der arteria carotis communis, nebst einer statistic dieser operation. Arch Klin Chirurgie. 1868;(9):257.4. 13. Friedman SG. A History of Vascular Surgery. Mount Kisco, NY: Futura; 1989. 14. Jaboulay M, Brian E. Recherches expérimentales sur la suture et la greffe artérielle. Lyon Méd. 1896;81:97. 15. Chiari H. Uber des verhalten des teilungswinkels der carotis communis bei der endarteritis chronica deformans. Verh Dtsch Ges Pathol. 1905;9:326-330. 16. Wang H, Lanzino G, Kraus RR, Fraser KW. Provocative test occlusion or the Matas test: who was Rudolph Matas? J Neurosurg. 2003;98:926-928. 17. Matas R. Testing the efficiency of the collateral circulation as a preliminary to the occlusion of the great surgical arteries. Ann Surg. 1911;53:1-43. 18. Gurdjian ES, Webster JE. Thrombosis of internal carotid artery in the neck and in the cranial cavity: symptoms and signs, diagnosis and treatment. Trans Am Neurol Assoc. 1951;56:241-242. 19. Monig SP, Walter M, Erasmi H, Pichlmaier H. Hans von Haberer: a forgotten pioneer in vascular surgery. Ann Vasc Surg. 1997;11:186-188. 20. Moniz E, Lima A, de Lacerda R. Par thrombose de la Carotide Interne. Presse Med. 1937;45:977-978. 21. Leriche R. Experimental and clinical basis for arterectomy in the treatment of localized arterial obliterations. Am J Surg. 1931;14:55-67. 22. Chao WH, Kwan ST, Lyman RS, Loucks HH. Thrombosis of the left internal carotid artery. Arch Surg. 1938;37:100111. 23. Sciaroni GH. Reversal of circulation of the brain; partial reversal in four humans treated for paralysis and mental conditions. Am J Surg. 1948;76:150-164. 24. Dos Santos JC. Sur la des obstruction des thrombus arterielles anciennes. Mem Acad Chir (Paris). 1947;73:409-411. 25. Wylie EJ. Thromboendarterectomy for arteriosclerotic thrombosis of major arteries. Surgery. 1952;32:275-292.
26. Wylie EJ, Kerr E, Davies O. Experimental and clinical experiences with the use of fascia lata applied as a graft about major arteries after thrombo-endarteriectomy and aneurysmorrhaphy. Surg Gynecol Obstet. 1951;93:257272. 27. DeBakey ME. Successful carotid endarterectomy for cerebrovascular insufficiency: nineteen-year follow-up. JAMA. 1975;233:1083-1085. 28. Eastcott HH, Pickering GW, Rob CG. Reconstruction of internal carotid artery in a patient with intermittent attacks of hemiplegia. Lancet. 1954;267:994-996. 29. Robertson JT. Carotid endarterectomy: a saga of clinical science, personalities, and evolving technology: the Willis lecture. Stroke. 1998;29:2435-2441. 30. Conley JJ, Pack GT. Surgical procedure for lessening the hazard of carotid bulb excision. Surgery. 1952;31:845-858. 31. Strully KJ, Hurwitt ES, Blankenberg HW. Thrombo endarterectomy for thrombosis of the internal carotid artery in the neck. J Neurosurg. 1953;10:474-482. 32. Fisher M. Occlusion of the internal carotid artery. AMA Arch Neurol Psychiatry. 1951;65:346-377. 33. Fisher M, Adams RD. Observations on brain embolism with special reference to the mechanism of hemorrhagic infarction. J Neuropathol Exp Neurol. 1951;10:92-94. 34. Denman FR, Ehni G, Duty WS. Insidious thrombotic occlusion of cervical carotid arteries, treated by arterial graft: a case report. Surgery. 1955;38:569-577. 35. Carrea R, Molins M, Murphy G. Surgery of spontaneous thrombosis of the internal carotid in the neck; carotidocarotid anastomosis; case report and analysis of the literature on surgical cases in Spanish]. Medicina (B Aires). 1955;15:20-29. 36. Cooley DA, Al-Naaman YD, Carton CA. Surgical treatment of arteriosclerotic occlusion of common carotid artery. J Neurosurg. 1956;13:500-506. 37. Fields WS, North RR, Hass WK, et al. Joint study of extracranial arterial occlusion as a cause of stroke, I: organization of study and survey of patient population. JAMA. 1968;203:955-960. 38. Blaisdell WF, Clauss RH, Galbraith JG, Imparato AM, Wylie EJ. Joint study of extracranial arterial occlusion, IV: a review of surgical considerations. JAMA. 1969;209:18891895. 39. Fields WS, Maslenikov V, Meyer JS, Hass WK, Remington RD, Macdonald M. Joint study of extracranial arterial occlusion, V: progress report of prognosis following surgery or nonsurgical treatment for transient cerebral ischemic attacks and cervical carotid artery lesions. JAMA. 1970;211:1993-2003.
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research-article2013
PVSXXX10.1177/1531003513517010Perspectives in Vascular Surgery and Endovascular TherapyTallarita et al
Article
History of Carotid Surgery: From Ancient Greeks to the Modern Era
Perspectives in Vascular Surgery and Endovascular Therapy 2014, Vol. 25(3-4) 57–64 © The Author(s) 2013 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/1531003513517010 pvs.sagepub.com
Tiziano Tallarita, MD1, Maurizio Gerbino, PhD2, Carmelina Gurrieri, MD3, and Giuseppe Lanzino, MD1
Abstract A relationship between decreased carotid arterial flow and apoplectic manifestations was already suspected by the ancient Greeks. Early attempts at carotid surgery, however, were limited to emergency arterial ligation in patients with neck trauma. Attempts to suture arterial stumps together to restore blood flow paved the way for Carrel’s revolutionary idea of reconstructing the resected or injured arterial segment with an interposition vein graft. DeBakey and Eastcott were the first to perform carotid endarterectomy in North America and the United Kingdom, respectively. In 1959, DeBakey proposed a cooperative study to assess the effectiveness of carotid endarterectomy in the treatment and prevention of ischemic cerebrovascular disease. The study was officially designated the Joint Study of Extracranial Arterial Occlusion and represented the first trial in the United States in which large numbers of patients were randomly allocated to surgical or nonsurgical therapy. Keywords carotid endarterectomy, carotid surgical history, stroke, transient ischemic attack
Introduction Extracranial atherosclerosis affects the carotid arteries in approximately 1% of the general population older than 60 years.1 Efficient diagnostic tests are used for the diagnosis of extracranial carotid disease, and effective medical, surgical, and endovascular therapies are available for its treatment. Carotid endarterectomy, in particular, has been established as the standard of treatment for carotid stenosis in patients with symptomatic disease and for selected patients with asymptomatic stenosis. The development of carotid surgery, however, has been the result of a slow and progressive process through the efforts of several pioneers and has been characterized by alternating successes and setbacks. In this review, we describe the development of carotid surgery from early attempts at emergency arterial ligation in patients with trauma to the modern reconstructive era.
Carotid Surgery Hippocrates of Kos lived between the fifth and fourth centuries bc. He traveled throughout Greece after the Peloponnesian War, curing people affected by plague that spread because of the poor hygienic conditions established after the conflict. In the same period, he was the first to study the carotid artery circulation and explained
the term apoplexia as “to be struck with violence.”2,3 The ancient Greeks believed that there was a relationship between carotid arterial flow and apoplectic manifestations. Indeed, the term carotid derives from the Greek word karoo, which means “to stupefy” or “to fall asleep.”4 There was a lack of understanding, however, of the pathophysiology associated with impairment of carotid circulation. The first surgical treatments for carotid disease were emergency procedures in patients with neck injuries. In France, the celebrated surgeon Ambrose Paré, who was appointed surgeon to King Henry II, may have performed the first recorded surgical ligation of the carotid artery in 1551. “It was an enthusiastic desire of learning his profession that induced Paré to follow the French armies while yet very young.”5 During a battle, it was necessary to quickly control bleeding from the carotid artery of a wounded soldier, and Paré accomplished this by ligation of the carotid artery (Figure 1). Paré’s writings, however, 1
Mayo Clinic, Rochester, MN, USA University of Siena, Siena, Italy 3 University of Catania, Catania, Italy 2
Corresponding Author: Giuseppe Lanzino, MD, Department of Neurologic Surgery, Mayo Clinic, 200 First Street SW, Rochester, MN 55905, USA. Email: [email protected]
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Figure 1. Carotid artery ligation for internal carotid artery aneurysm.
Adapted from Bell C. Illustrations of the great operations of surgery: trepan, hernia, amputation, aneurism, and lithotomy. London, ca 1821.
did not provide a clear and detailed description of the operation. Thus, there is controversy about whether he indeed was the first to perform such an operation. One century later, the Civil War in England led to the expansion of Thomas Willis’s (personal physician to King Charles I) surgical experience. In his landmark contribution, Willis provided an anatomical explanation for the absence of complications after acute ligation of the internal carotid artery by observing passage of an injected staining solution from one carotid to the other through collateral channels: “the Carotid of one side might provide for either Province . . . Further, if both the Carotids should be stopt, the office of each might be supplied through the Vertebrals.”6 Probably unaware of Willis’s findings, Fleming, a naval surgeon, in 1803, provided a detailed description of a therapeutic common carotid artery ligation to arrest a lethal hemorrhage. In Fleming’s case, the patient had a self-inflicted penetrating neck injury.7 Following Hunter’s and others’ experiences with proximal ligation to treat peripheral aneurysms,8 surgeons started applying the same strategy to the treatment of carotid aneurysms in the neck. Toward the end of the 18th century and the beginning of the 19h century, Sir Astley Cooper (Figure 2) is credited as being the first to perform a carotid ligation for treatment of an aneurysm. He wrote, Mary Edwards, aged 44, was brought to my house by Mr. Robert Pugh of Gracechurch Street, that I might examine a tumor in the neck which was obviously an aneurysm of the right carotid artery . . . When the swelling was examined at the hospital, great doubts were entertained if there were sufficient space between the clavicle and the tumor for the application of a ligature.9
Her carotid artery was successfully ligated, but she died 1 week later due to mass effect on the pharynx and trachea
Figure 2. Sir Astley Cooper.
Adapted from Cooper, Life of Sir Astley Cooper, London, 1843.
caused by an inflammatory reaction in the large aneurysmal sac after carotid ligation. Showing a trait common to many surgical pioneers, Cooper persisted in his efforts despite his first disappointing experience. Three years later, another attempt was successful: A blunt iron probe constructed for the purpose was then passed under the artery, carrying a double ligature with it. Two ligatures being thus conveyed under the artery the lower was immediately tied. I next detached the artery from the surrounding parts to the extent of an inch above the lower ligature, and then tied the upper. Lastly, a needle and thread were passed through the artery above one ligature and below the other. The division of the artery was then performed.10
The patient recovered and returned to work. Several other reports of carotid surgery ensued, and in 1860, Ehrmann analyzed the results of 281 carotid ligation operations, noting high mortality after this procedure.11 A few years later, a mortality rate of 43% was reported based on an analysis of 600 cases of carotid ligation.12 Even in those earlier days, this mortality rate was felt to be too high. These early and less-than-ideal results encouraged surgeons of the time to seek alternative reconstructive procedures. Murphy reported invaginating one cut arterial end into another, in an end-to-end fashion, and used partial-thickness sutures to hold them in place (Figure 3).13 Jaboulay and Brian14 used an interrupted U-shaped suture to reunite the carotid arteries of donkey and dogs, and Doerfler described creating anastomoses
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It is important that this preliminary occlusion be made while the patient is fully conscious in order to obtain prompt information of the cerebral effects of the interruption of the blood current in the brain as these manifestations often appear the moment the occlusion takes place.17
In the same year, James Ramsay Hunt described the syndrome of occlusion of the internal carotid artery. He emphasized the importance of examination of the neck vessels in all cases presenting with cerebral symptoms of vascular origin: “for this purpose a section of the carotid artery is readily accessible to palpation, extending from the lower border of the thyroid cartilage to the angle of the jaw.”13 Furthermore, he observed that while inequality of pulsation on the two sides might be accidental, its occurrence in four cases all presenting the symptoms of extensive brain softening is rather significant, and the thought naturally arises that some obstructive lesion of the vessel or its entrance into the arch of the aorta has interfered with the free flow of blood to the brain.13
Figure 3. Murphy’s illustration of the technique used for the first successful clinical end-to-end arterial anastomosis. Adapted from Murphy JB. Resection of arteries and veins injured in continuity–end-to-end suture–experimental and cultural research. Med Rec. 1897;51:73.
with fine silk and a curved round needle.13 The latter demonstrated that it was possible to suture 2 vessel stumps with accurate approximation of all vessel wall layers without ensuing thrombosis. Furthermore, Doerfler stressed the great importance of adherence to the principles of aseptic technique to achieve good results.13 These attempts paved the way for Carrel’s (Figure 4A) revolutionary idea of reconstructing the resected segment with an interposition vein graft. He stated, “In such cases it would be possible to extirpate freely all the injured portions of the vessel and to re-establish the circulation by interposing a segment of vein between the cut ends of the artery” (Figure 4B).13 Further developments in carotid surgery were related to ongoing efforts to clarify the relationship between carotid artery disease and cerebral ischemia. The famous pathologist from Prague, Chiari, demonstrated a link between carotid stenosis and transient ischemic attack or stroke. He described ulcerating carotid plaques and suggested that emboli could break off from these plaques with resulting distant infarction.15 In a seminal contribution in 1914, the New Orleans surgeon Rudolf Matas (Figure 5) described a compression test of the carotid artery to assess the efficiency of collateral circulation while planning carotid artery ligation.16 He stated,
During the years of World War I, an increasing number of carotid injuries could be seen due to assault with bayonets and close combat. In this period, the field of reconstructive carotid surgery was further advanced by the reports of Von Parczewski who, in 1916, resected an arteriovenous aneurysm of the common carotid artery and restored continuity with an end-to-end anastomosis,18 and by von Haberer, Lexer, and Denck, who performed many end-to-end anastomoses in soldiers during the conflict.19 The revolutionary introduction of angiography provided in vivo documentation of carotid occlusive disease and gave further impetus to the development of surgical procedures in order to avoid its deleterious consequences. In Portugal, Egas Moniz developed cerebral angiography as a method to localize brain tumors in 1927 (Figure 6). Ten years later, Moniz described 4 cases of internal carotid occlusion associated with hemiplegia. In these patients, carotid occlusion was documented on angiography. He concluded, La thrombose de la carotide interne, bien que rare, est, cependant, plus frequente qu’on ne l’ avait pensé. . . . Nous pouvons dire que la thrombose de la carotide interne représente 0,8 pour 100 des malades chez lesquels nous avons fait l’artériographie cérébrale. Si nous l’avions faile sur une série de cas d’hémiplégies, le pourcentage serait certainement plus élevé. [Thrombosis of the internal carotid artery, although rare, is, however, more frequent than one would have thought. . . . We can say that thrombosis of the internal carotid was found in 0.8 per 100 patients in whom we performed cerebral arteriography. If we had used a series of cases of hemiplegia, the percentage would certainly be higher]20
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Figure 4. Carrel’s interposition vein graft. (A) Alexis Carrel. (B) (Top) Venous interposition graft by Carrel and Guthrie and (bottom) end-to-end anastomosis of vein graft into arterial circulation.
Figure A courtesy of the Rockefeller Archive Center, Sleepy Hollow, New York. Used with permission. Figure B adapted from Carrel A, Guthrie CC. Uniterminal and biterminal venous transplantation. Surg Gynecol Obstet. 1906;2:266.
Figure 5. Portrait of Matas by Thomas C. Corner.
Courtesy of the Rudolph Matas papers, Louisiana Research Collection, Tulane University, New Orleans, Louisiana. Used with permission.
In the 1930s in China, Chao and associates reported 2 cases of carotid occlusion treated with denervation of the
proximal carotid artery and excision of the thrombosed segment with the purpose of interrupting the “sympathetic impulses in the walls of the artery,” as described by the great French surgeon Leriche in the treatment of occlusive femoral disease.21 One of these 2 cases involved a 47-year-old Russian woman who worked as a switch operator on the Chinese Eastern Railway. Her eyesight had been impaired by recurrent emboli from a left carotid plaque. One day “she threw a switch the wrong way and caused the wreck of a locomotive and seven empty freight cars.”22 She underwent surgery with uneventful outcome. The second case was a 27-year-old Chinese mathematics student who could not read Chinese characters after a stroke. In both cases, after surgical intervention, improvement of their “mental functions” was observed. This led Chao to conclude that “excision of the thrombosed artery should be carried out.”22 As often happens in the history of surgical techniques, increasing experience with carotid surgery led to some abuses and the development of “fancy” procedures based on sketchy theoretical background. Along these lines, Sciaroni23 proposed the concept of “reversal of the circulation of the brain.” The background for his operation was the idea that a jugular-carotid fistula would reduce the perfusion within the carotid sinus with resulting increased levels of carbon dioxide. The effects of both reduced sinus perfusion and increased local carbon dioxide concentration would eventually lead to an increase in the cerebral perfusion pressure and blood flow, accompanied by peripheral vasoconstriction. Thus, in 1948, he
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plaque from the femoral artery with a “loop stripper” through one or more transverse or longitudinal arteriotomies. L’artère fut décourverte de l’arcade au canal de Hunter. Elle fut incise longitudinalement sur 2 centimètres à chaque extrémité. Un plan de clivage fut aisément trouvé entre le thrombus et la paroi. Avec une spatule mousse et un stylet, une bonne partie du caillot fut libéré en bas et en haut. Il tenait encore à la partie moyenne de l’artère [. . .] lui imprima quelques mouvements de rotation et finalement il fut enlevé en presque totalité. [The artery was dissected at the level of the adductor canal. It was incised longitudinally for 2 centimeters at each end. A cleavage plane was easily found between the thrombus and the wall. With a blunt spatula and a stylus, a great amount of the clot was released in the top and bottom parts of the artery. Clot remained in the middle part of the artery [. . .]. After applying some rotational movements, almost all of the clot was finally removed]24
Figure 6. Cerebral angiograms showing internal carotid occlusion (top) and stenosis (bottom). Adapted from Moniz et al.20 Used with permission.
suggested that an arteriovenous fistula between the common carotid artery and the internal jugular vein through a side-to-side anastomosis would relieve symptoms of paralysis and epileptic seizures. Despite initial enthusiasm, results were not encouraging, and several years later this operation fell into disrepute.23
The Birth of Modern Carotid Endarterectomy The development of modern carotid endarterectomy was the result of continuous, onward evolution. The progression in carotid artery surgery for the prevention and care of ischemic cerebrovascular disease was often the extension of experience already accumulated with interventions in the peripheral circulation. In 1947, the Portuguese surgeon Cid Dos Santos showed that it was possible to remove a long occluding thrombus along with underlying
He is credited to be the father of endarterectomy as performed today. Dos Santos observed that since the atheroma is usually at the intima level, it is possible to easily find a cleavage plane between the diseased and nondiseased arterial wall. He also noted that, at times, a marked discontinuity could be seen between the intima and media at the distal point of the lesion, which needed to be beveled to minimize the risk of postoperative thrombosis. Otherwise, if the distal point of the endarterectomy had only lost adhesion to the underlying media, it could be secured with fine “tacking” sutures tied externally.24 After the early reports of Dos Santos, studies in the Experimental Surgical Laboratory of the University of California School of Medicine demonstrated the process of intimal regeneration after excision of the internal lining of the aorta in dogs.25,26 Some authors consider Bazy and Reboul to be the actual fathers of carotid endarterectomy. These 2 French surgeons, applying the Dos Santos technique of endarterectomy to carotid stenosis, performed a longitudinal arteriotomy as long as the atheroma, followed by the removal of the plaque and direct suture. Unfortunately, there are no clear references supporting the claims of these authors, generating doubts about the authenticity of the claim. The surgeons DeBakey27 (Figure 7) and Eastcott28 have often been credited as being the first to perform carotid endarterectomy in North America and in the United Kingdom, respectively. In DeBakey’s case, the diagnosis of carotid stenosis was made by angiography, which revealed a large “atheromatous plaque . . . at the origin of the internal, as well as the external, carotid artery,” with a fresh clot partially filling the residual lumen of the common carotid artery.27 DeBakey
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Figure 7. Michael DeBakey.
Adapted from Wikipedia. Available from: http://en.wikipedia.org/ wiki/File:Michael_E._DeBakey.jpeg. In the public domain. Courtesy of University of Houston Libraries.
published this case in 1975 and reported that the patient survived for 19 years without recurrence of cerebrovascular insufficiency until fatal heart failure occurred. The specifics surrounding the details of this operation are controversial, however, because the medical record of this patient was never found.29 In a similarly celebrated operation, Eastcott et al28 in 1954 restored continuity of flow by direct anastomosis between the common carotid artery and the stump of the internal carotid artery, after the removal of the atheromatous plaque at the carotid bifurcation. The carotid artery was clamped for 28 minutes, and good pulsation was observed in the vessels after removal of the clamps. Anticoagulants were not used.28 These early encouraging results led other surgeons to advocate for the application of surgical management of the involved carotid artery during neck surgery for neoplastic diseases. In the early 1950s, New York surgeon John J. Conley (Figure 8) performed a large series of operations on neoplasms of the neck. During these interventions, he often removed portions of the internal and common carotid arteries, followed by end-to-end anastomosis of the distal stumps of the internal and external carotid arteries. Only a few of these mattress sutures of 0000 silk on atraumatic needles are necessary to approximate the cut ends of the arteries, depending, of course, on the diameter of the lumens. If the diameter of one of the carotid arteries is larger than the other, this disproportion may be overcome by cutting the artery with the small diameter in an oblique manner, thus increasing its overall circumference.30
Figure 8. John J. Conley.
Adapted from American Head & Neck Society Past Presidents webpage. Available from: http://www.ahns.info/about-ahns/past_ presidents/conley. In the public domain. Courtesy of American Head & Neck Society.
Subsequently, he introduced the interposition saphenous vein bypass between the common and internal carotid arteries, with favorable results.30 In the same period, Strully et al31 published the first attempt to reopen an acute carotid thrombosis in which the thrombus extended to the intracranial carotid artery. A 2-cm longitudinal incision was made at the point of transition in the affected vessel, and a thrombus partially extruded itself through the opening. . . . With suction applied to the catheter at all times it was possible to remove additional thrombus. A total of 7 cm of clot was removed. . . . Retrograde flow of blood could not be obtained. Several attempts to remove the intracranial portion of the clot were unsuccessful. Because of the danger of dislodging clot in the intracranial portion of the internal carotid artery when the common artery clamp was removed, the vessel was occluded by transfixion ligatures and 2 cm portion was removed.31
Although it had been suspected, a clear-cut causal relationship between carotid steno-occlusive disease and ipsilateral ischemia was not uniformly accepted until Miller C. Fisher’s seminal description of 8 cases of obstruction of the carotid artery.32,33 In these reports, Fisher speculated that hemorrhagic infarction was often the result of embolism from carotid thrombosis: Later, due to fragmentation of the embolic material and possibly to relaxation of local vascular spasm, the embolus moves from its original position into more distal branches. This exposes the necrotic tissue to the full force of arterial
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Encouraged by increased understanding of the pathophysiology of cerebral ischemia, other surgeons tried to surgically reopen the carotid artery in cases of complete occlusion. Denman et al34 used lyophilized homografts to replace occluded carotid segments, with excellent results: 26 years after bilateral carotid arterial grafting, the patient, a 60-year-old woman, was still symptom free. In 1955, Carrea et al35 reconstructed an occluded internal carotid artery in a 41-year-old man with convulsions, aphasia, left eye blindness, and hemiparesis. “The internal carotid artery was cut about 5 mm above the abnormal area, the external carotid was also cut at the same level and the proximal carotid was anastomosed end-to-end to the distal portion of the internal carotid.”35 Postoperative vessel patency was confirmed angiographically. Three conditions had to be met, according to Carrea et al,35 to be able to perform this procedure: (a) the occlusion must be localized at the proximal portion of the internal carotid artery, (b) the diameter of the internal carotid artery must be large enough to allow for an adequate anastomosis, and (c) both portions of the internal and common carotid arteries to be anastomosed must be free of atherosclerotic plaques. Later refinements in carotid endarterectomy led to the procedure as we know it today. To reduce the ischemia time during carotid cross-clamping, in 1956, Cooley et al36 introduced a polyvinyl extravascular shunt to bypass the carotid stenosis, reducing the neurologic complications linked to temporary cerebral hypoperfusion. In their case report, brain protection during clamping was afforded with intravenous Pentothal (thiopental sodium) and “cooling of the cranium and brain [by] immersing the head in crushed ice.” After dissection of the carotid bifurcation, “a polyvinyl shunt, with needle points at both ends, was used to by-pass the carotid circulation during the period of occlusion.”36
Carotid Endarterectomy Becomes the Most Widely Studied Surgical Procedure At a meeting held in January 1959 in Washington, DC, Michael E. DeBakey, inspired by Fisher’s work, proposed a cooperative study to assess the effectiveness of carotid endarterectomy in the treatment and prevention of ischemic cerebrovascular disease. The study was officially designated the Joint Study of Extracranial Arterial Occlusion. The results were published in a series of articles in the Journal of the American Medical Association.37 The study concluded that “results of surgery are most
favorable in patients with transient ischemic attack or minor neurologic deficits in whom stenosis rather than occlusion of the extracranial arteries is found.”37 The Joint Study also led to better standardization of the methods for measurement of stenosis, definition of surgical contraindications, and characterization of various patient subgroups.38,39 This was the first trial in the United States in which a large number of patients was randomly allocated to surgical or nonsurgical therapy. The following years were characterized by a progressive increase in the number of carotid endarterectomies both for asymptomatic and symptomatic disease. This rapid increase led some to question the validity and efficacy of the procedure as it was being performed. Numerous large trials on carotid endarterectomy were subsequently conducted, which eventually would make carotid endarterectomy the most-studied surgical procedure, the indications for and efficacy of which are now based on the highest level of scientific evidence. Declaration of Conflicting Interests The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding The authors received no financial support for the research, authorship, and/or publication of this article.
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26. Wylie EJ, Kerr E, Davies O. Experimental and clinical experiences with the use of fascia lata applied as a graft about major arteries after thrombo-endarteriectomy and aneurysmorrhaphy. Surg Gynecol Obstet. 1951;93:257272. 27. DeBakey ME. Successful carotid endarterectomy for cerebrovascular insufficiency: nineteen-year follow-up. JAMA. 1975;233:1083-1085. 28. Eastcott HH, Pickering GW, Rob CG. Reconstruction of internal carotid artery in a patient with intermittent attacks of hemiplegia. Lancet. 1954;267:994-996. 29. Robertson JT. Carotid endarterectomy: a saga of clinical science, personalities, and evolving technology: the Willis lecture. Stroke. 1998;29:2435-2441. 30. Conley JJ, Pack GT. Surgical procedure for lessening the hazard of carotid bulb excision. Surgery. 1952;31:845-858. 31. Strully KJ, Hurwitt ES, Blankenberg HW. Thrombo endarterectomy for thrombosis of the internal carotid artery in the neck. J Neurosurg. 1953;10:474-482. 32. Fisher M. Occlusion of the internal carotid artery. AMA Arch Neurol Psychiatry. 1951;65:346-377. 33. Fisher M, Adams RD. Observations on brain embolism with special reference to the mechanism of hemorrhagic infarction. J Neuropathol Exp Neurol. 1951;10:92-94. 34. Denman FR, Ehni G, Duty WS. Insidious thrombotic occlusion of cervical carotid arteries, treated by arterial graft: a case report. Surgery. 1955;38:569-577. 35. Carrea R, Molins M, Murphy G. Surgery of spontaneous thrombosis of the internal carotid in the neck; carotidocarotid anastomosis; case report and analysis of the literature on surgical cases in Spanish]. Medicina (B Aires). 1955;15:20-29. 36. Cooley DA, Al-Naaman YD, Carton CA. Surgical treatment of arteriosclerotic occlusion of common carotid artery. J Neurosurg. 1956;13:500-506. 37. Fields WS, North RR, Hass WK, et al. Joint study of extracranial arterial occlusion as a cause of stroke, I: organization of study and survey of patient population. JAMA. 1968;203:955-960. 38. Blaisdell WF, Clauss RH, Galbraith JG, Imparato AM, Wylie EJ. Joint study of extracranial arterial occlusion, IV: a review of surgical considerations. JAMA. 1969;209:18891895. 39. Fields WS, Maslenikov V, Meyer JS, Hass WK, Remington RD, Macdonald M. Joint study of extracranial arterial occlusion, V: progress report of prognosis following surgery or nonsurgical treatment for transient cerebral ischemic attacks and cervical carotid artery lesions. JAMA. 1970;211:1993-2003.
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