In vitro and in vivo Studies of the Extent of Electrothrombotic Deposition of Blood Elements on the Surface of Electrolytically Detachable Coils

Endovascular treatment of intracranial aneurysms with electrolytically detachable coils is often claimed to be based on electrothrombosis, i.e. intra-aneurysmal thrombus formation through applied direct current. Despite the fact that this concept was described more than a century ago, the significance of electrothrombosis in the endovascular treatment of aneurysms remains debatable. Apart from electrothrombosis, mechanical obliteration of the aneurysmal lumen might be one of the many possible mechanisms to explain why and how detachable coils are effective in preventing aneurysms from (re-)rupture. The purpose of this experimental study was to investigate to what extent direct current comparable to that used for coil detachment would influence the adhesion of cellular and liquid blood components to the surface of electrolytically detachable platinum coils. For the in vitro study, electrolytically detachable platinum coils of various types were exposed to stagnant heparinised blood for a total of 16 h, without or with applied direct current for 30 or 90 s (1 mA, 4–6 V, coil as anode). For the in vivo study, electrolytically detachable platinum coils were exposed to flowing blood for 180 s, without or with applied direct current (2 mA, 4–6 V, coil as either anode or cathode), without anti-coagulation and after intravenous administration of 5000 U Heparin and again after the intravenous administration of 500 mg Aspisol in addition to Heparin. After exposure to blood according to these different experimental protocols, the coils were fixed in formalin solution, gold coated and examined by scanning electron microscopy. Thrombus formation on the surface of all unfibred coils was thin and highly variable both from coil to coil, and on different areas of any given coil. The application of direct current minimally enhanced thrombus formation in stagnant blood in vitro, but not in vivo. The cellular and fibrin adhesions on the coil surfaces without and with applied current did not effectively increase the diameter or volume of unfibred coils. Coils with attached nylon fibres, however, proved to be highly thrombogenic without or with application of current. In fibred coils, surface adhesions without and with applied current were voluminous enough to effectively increase the diameter of the coil, potentially important for the process of endosaccular aneurysm occlusion. Electrothrombosis plays no role in the endovascular treatment of intracranial aneurysms with electrolytically detachable coils. This explains why platinum coils with non-electrolytic detachment mechanisms show a similar efficiency and recurrence rate.

[1]  K. Inoue,et al.  Electrothrombosis as a Treatment of Cirsoid Angioma in the Face and Scalp and Varicosis of the Leg , 1982, Plastic and reconstructive surgery.

[2]  Z. Gokaslan,et al.  Long-term histopathologic changes in canine aneurysms embolized with Guglielmi detachable coils. , 1995, AJNR. American journal of neuroradiology.

[3]  A. Salazar.  Experimental Myocardial Infarction Induction of Coronary Thrombosis in the Intact Closed-Chest Dog , 2005 .

[4]  B. G. King,et al.  ELECTROTHERMIC COAGULATION OF AORTIC ANEURYSMS , 1938 .

[5]  R. R. Linton.  Intrasaccular Wiring of Abdomixalarterio- Sclerotic Aortic Aneurysms By the "Pack" Method , 1951, Angiology.

[6]  Charles M Strother,et al.  Effect of Guglielmi detachable coils on intraaneurysmal flow: experimental study in canines. , 2002, AJNR. American journal of neuroradiology.

[7]  J. W. Pate,et al.  Bio-electric phenomena as an etiologic factor in intravascular thrombosis. , 1953, The American journal of physiology.

[8]  J. Caillé,et al.  Selective vascular thrombosis induced by a direct electrical current: animal experiments. First clinical trials. , 1978, Journal of neuroradiology. Journal de neuroradiologie.

[9]  D. Power.  The palliative treatment of aneurysm by ‘wiring’ with Colt's apparatus , 1921 .

[10]  R. Moore,et al.  Guide wire thrombogenicity and its reduction. , 1974, Radiology.

[11]  R. R. Linton,et al.  Treatment of thoracic aortic aneurysms by the pack method of intrasaccular wiring. , 1952, The New England journal of medicine.

[12]  W. M. Thompson,et al.  Clinical use of transcatheter electrocoagulation. , 1978, Radiology.

[13]  森 惟明.  Experimental studies on electrically induced arterial thrombosis in dogs, with special reference to the treatment of intracranial aneurysms and arteriovenous malformations , 1967 .

[14]  S. Mullan,et al.  Electrically induced thrombosis in intracranial aneurysms. , 1965, Journal of neurosurgery.

[15]  K. Tabuchi,et al.  [Histological findings in aneurysm treated with IDC: scanning electron microscopical study]. , 1997, No shinkei geka. Neurological surgery.

[16]  V. Macellari,et al.  Electrothrombosis of saccular aneurysms via endovascular approach. Part 1: Electrochemical basis, technique, and experimental results. , 1991, Journal of neurosurgery.

[17]  A. Molyneux.  International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial , 2002, The Lancet.

[18]  A. Krisht,et al.  Histologic effects of collagen-filled interlocking detachable coils in the ablation of experimental aneurysms in swine. , 1996, AJNR. American journal of neuroradiology.

[19]  C M Strother,et al.  Effect of Guglielmi detachable coil placement on intraaneurysmal pressure: experimental study in canines. , 2001, AJNR. American journal of neuroradiology.

[20]  C. Riquelme,et al.  Endovascular Treatment of Berry Intracranial Aneurysms Using a New Detachable Coil System , 2001, Interventional neuroradiology : journal of peritherapeutic neuroradiology, surgical procedures and related neurosciences.

[21]  A. Blakemore.  Progressive Constrictive Occlusion of the Abdominal Aorta with Wiring and Electrothermic Coagulation: A One Stage Operation for Arteriosclerotic Aneurysms of the Abdominal Aorta , 1951 .

[22]  S. Endo,et al.  Electrothrombosis of spontaneous carotid-cavernous fistula by copper needle insertion. , 1984, Neurosurgery.

[23]  A. Blakemore.  Progressive constrictive occlusion of the abdominal aorta with wiring and electrothermic coagulation, a one-stage operation for arteriosclerotic aneurysms of the abdominal aorta. , 1951, Annals of surgery.

[24]  P. Sawyer.  BIOELECTRIC PHENOMENA AND INTRAVASCULAR THROMBOSIS: THE FIRST 12 YEARS. , 1964, Surgery.

[25]  A. Thron,et al.  The nature of early intraluminal thrombosis in terminal aneurysms occluded with guglielmi detachable coils. , 1997, Interventional neuroradiology : journal of peritherapeutic neuroradiology, surgical procedures and related neurosciences.

[26]  D. Dado,et al.  Experience with Electrothrombosis in the Treatment of Angiomas , 1987, Annals of plastic surgery.

[27]  O Levrier,et al.  Endovascular treatment of intracranial aneurysms. , 1996, AJNR. American journal of neuroradiology.

[28]  W. Feiden,et al.  Histopathologische Befunde in Hirnbasisarterienaneurysmen nach Embolisation mit Guglielmi detachable platinum coils (GDC) Zwei Fallberichte , 1999, Der Radiologe.

[29]  Y. Hosobuchi.  Electrothrombosis of carotid-cavernous fistula. , 1975, Journal of neurosurgery.

[30]  G. H. Colt.  Three cases of aneurysm of the aorta treated by wiring. I. Aneurysm of the abdominal aorta , 1925 .

[31]  K. Fujii,et al.  Tissue response of a small saccular aneurysm after incomplete occlusion with a Guglielmi detachable coil. , 1999, AJNR. American journal of neuroradiology.

[32]  E. Castro,et al.  Long-term histopathologic findings in two cerebral aneurysms embolized with Guglielmi detachable coils. , 1999, AJNR. American journal of neuroradiology.

[33]  H. Handa,et al.  Electrothrombosis of ateriovenous malformation. , 1977, Neurologia medico-chirurgica.

[34]  H. Tenjin,et al.  Effect of Guglielmi detachable coils on experimental carotid artery aneurysms in primates. , 1995, Stroke.

[35]  G. Guglielmi,et al.  Role of electrothrombosis in aneurysm treatment with Guglielmi detachable coils: an in vitro scanning electron microscopic study. , 2001, AJNR. American journal of neuroradiology.

[36]  C. Strother,et al.  Platinum coil coatings to increase thrombogenicity: a preliminary study in rabbits. , 1993, AJNR. American journal of neuroradiology.

[37]  G. Joseph,et al.  Treatment of Experimental Aneurysms Using Collagen‐coated Microcoils Experimental Study: 133 , 1995, Neurosurgery.

[38]  D. Rüfenacht,et al.  Treatment of carotid artery aneurysms with platinum coils: an experimental study in dogs. , 1990, AJNR. American journal of neuroradiology.

[39]  G. H. Colt,et al.  A Case of Aneurysm of the Abdominal Aorta treated by the Introduction of Silver Wire; with a Description of Instruments invented and constructed by Mr. G. H. Colt to facilitate the introduction of Wire into Aneurysms. , 1903, Medico-chirurgical transactions.

[40]  I. Saatci,et al.  Interlocking detachable coil occlusion in the endovascular treatment of intracranial aneurysms: preliminary results. , 1996, AJNR. American journal of neuroradiology.

[41]  E. Kwan,et al.  Endovascular packing of carotid bifurcation aneurysm with polyester fiber-coated platinum coils in a rabbit model. , 1993, AJNR. American journal of neuroradiology.

[42]  H. Plenk,et al.  Gross and microscopic histopathological findings in aneurysms of the human brain treated with Guglielmi detachable coils. , 1999, Journal of neurosurgery.

[43]  T. Thompson,et al.  SACCULAR ANEURYSM OF THE THORACIC AORTA: TREATED BY WIRING WITH COLT'S APPARATUS , 1935 .

[44]  J. W. Pate,et al.  Relations of abnormal and injury electric potential differences to intravascular thrombosis. , 1953, The American journal of physiology.

[45]  T. Koike,et al.  Scanning electron microscopic study of the migrated platinum coil after endovascular embolization of a giant cerebral aneurysm. , 1998, AJNR. American journal of neuroradiology.

[46]  G. Leclerc,et al.  Healing mechanisms in experimental aneurysms. I. Vascular smooth muscle cells and neointima formation. , 1999, Journal of neuroradiology. Journal de neuroradiologie.

[47]  S. Mullan,et al.  Stereotactic Copper Electric Thrombosis of Intracranial Aneurysms1 , 1969 .

[48]  G. Duckwiler,et al.  Electrothrombosis of saccular aneurysms via endovascular approach. Part 2: Preliminary clinical experience. , 1991, Journal of neurosurgery.

[49]  T. Rainer,et al.  Effect of stress hormones on the expression of fibrinogen-binding receptors in platelets. , 2002, Resuscitation.

[50]  J. W. Pate,et al.  Electrical potential differences across the normal aorta and aortic grafts of dogs. , 1953, The American journal of physiology.

[51]  J. Pile-Spellman,et al.  Coil embolization of aneurysms: angiographic and histologic changes. , 1997, AJNR. American journal of neuroradiology.

[52]  J. Finney.  THE WIRING OF OTHERWISE INOPERABLE ANEURISMS , 1912 .

[53]  P. Sawyer,et al.  Studies on direct-current coagulation. , 1961, Surgery.

[54]  J. Byrne,et al.  Endovascular coil occlusion of experimental aneurysms: partial treatment does not prevent subsequent rupture. , 1994, Neurological research.

[55]  R. Willinsky,et al.  Acute human histopathology of an intracranial aneurysm treated using Guglielmi detachable coils: case report and review of the literature. , 1998, Neurosurgery.

[56]  B. G. King,et al.  ANEURYSM OF THE INTERNAL CAROTID ARTERY WITHIN THE SKULL: WIRING AND ELECTROTHERMIC COAGULATION , 1941 .

[57]  J. F. Phillips.  Transcatheter electrocoagulation of blood vessels. , 1973, Investigative radiology.

[58]  A. Robinson,et al.  Experimental Closure of Arteriovenous Fistula by Transcatheter Electrocoagulation. , 1975, Radiology.

[59]  P. Flandroy,et al.  Selective endovascular treatment of intracranial aneurysms using micrus microcoils: preliminary results in a series of 78 patients. , 2002, Journal of neuroradiology. Journal de neuroradiologie.

[60]  P. Purdy,et al.  Scanning electron microscopic findings in a basilar tip aneurysm embolized with Guglielmi detachable coils. , 1997, AJNR. American journal of neuroradiology.

[61]  H. Handa,et al.  Management of spontaneous carotid-cavernous fistulae. , 1982, Surgical neurology.

[62]  B Lane,et al.  A mechanically detachable coil for the treatment of aneurysms and occlusion of blood vessels. , 1994, AJNR. American journal of neuroradiology.

[63]  J. Byrne,et al.  The nature of thrombosis induced by platinum and tungsten coils in saccular aneurysms. , 1997, AJNR. American journal of neuroradiology.

[64]  A. Thron,et al.  Microsurgically produced bifurcation aneurysms in a rabbit model for endovascular coil embolization. , 1996, Journal of neurosurgery.

[65]  S. Mullan.  Experiences with surgical thrombosis of intracranial berry aneurysms and carotid cavernous fistulas. , 1974, Journal of neurosurgery.

[66]  A. Wakhloo,et al.  Initial experience with collagen-filled Guglielmi detachable coils for endovascular treatment of experimental aneurysms. , 1997, AJNR. American journal of neuroradiology.

[67]  A. Eshner.  THE TREATMENT OF ANEURYSM OF THE AORTA BY THE INTRODUCTION OF WIRE AND THE PASSAGE OF A GALVANIC CURRENT , 1910 .