Spinal Vascular Malformations: An Historical Perspective

Perry Black, M.D.

Disclosures

Neurosurg Focus. 2006;21(6) 

In This Article

The Modern Era: 1960 to the Present

Initiated in Sweden in the 1960s, subspecialization in neuroradiology rapidly spread to the US, England, France, and other countries. This subspecialization led to the emergence of interventional neuroradiology, which was essential for the development of precise imaging techniques for spinal vascular lesions. The intrathecal metrizamide computed tomography myelogram was introduced as a diagnostic screening test. Selective spinal angiography became the definitive diagnostic tool for evaluating spinal AVMs.[6] Embolization of vascular lesions added a further dimension to treatment options.

Also in the 1960s, the introduction of the operating microscope,[8] the development of microsurgical instruments, including bipolar forceps (invented by Greenwood in 1940[10] and subsequently refined by Malis[15]), and progress in anesthesiology empowered neurosurgeons to undertake procedures that were previously thought to be impossible.[11,12,14,16–19,21,24]

The advances in interventional neuroradiology and micro neurosurgery allowed detailed evaluations that enhanced understanding of the vascular anatomy as well as the pathophysiological features of the vascular lesions. For example, in 1977 Kendall and Logue[12] demonstrated that lesions formerly thought to be venous angiomas on the surface of the spinal cord were actually normal veins dilated by communication with arterial blood from a dural AVF. It was further observed that the pathophysiological mechanism of most spinal AVMs is associated with venous hypertension. It was shown that, in many cases, the irregular vascular pattern seen on myelography and at surgery represented arterialized draining veins, rather than the AVM itself.[1]

The remarkable strides that occurred in neuroimaging and in surgical technique resulted in a better understanding of the angioarchitecture and pathology of the lesions, which likewise enhanced clarity in classification of these entities. From the 1960s through the 1980s, major new and clinically useful insights emerged; these were largely the product of a collaborative effort among neuroradiologists and neurosurgeons in England, France, and the US. In England, neurosurgeon Valentine Logue (Fig. 4 left) worked with neuroradiologist Brian Kendall (Fig. 4 right) and with an associate, M. J. Aminoff, at the National Hospital for Neurology and Neurosurgery in London.[1,12] In France, the driving force was neuroradiologist René Djindjian (Fig. 5) at Hôpital Lariboisière in Paris.[7] In the US, the key center of spinal vascular activity was at the NIH in Bethesda, Maryland, where neuroradiologist John Doppman (Fig. 6 left) was a leading member of the NIH team, along with radiologist Giovanni Di Chiro (Fig. 6 center), and neurosurgeons Ayub Ommaya and Edward Oldfield (Fig. 6 right). Although the three centers worked independently of each other, there was considerable intellectual interaction at the personal level as well as through their respective publications.

Left: Portrait of Valentine Logue, the neurosurgeon who, along with neuroradiologist Brian Kendall and associate M. J. Aminoff, was a member of the English contingent of the "American/English/French connection" in introducing the modern era in the understanding and treatment of spinal vascular lesions (see also Fig. 7). (Photograph courtesy of the University College of London Institute of Neurology.) Right: Portrait of Brian Kendall, the neuroradiologist at the Institute for Neurology and Neurosurgery, Queen Square, London, who worked with Valentine Logue and A. M. Aminoff in the 1960s and 1970s. Together they studied the pathophysiology and clinical aspects of spinal vascular abnormalities. (Photograph courtesy of the University College London Institute of Neurology.)

Portrait of René Djindjian, a pioneer French neuroradiologist of Armenian descent, who made major contributions to selective spinal angiography at Hôpital Lariboisière in Paris. Djindjian led the French contingent of the "American/English/French connection" in pursuit of unraveling the enigma of spinal vascular malformations (see also Fig. 7). (Photograph courtesy of Professor Emmanuel Houdart.)

Left: Portrait of the neuroradiologist John Doppman, a leading member of the American team at the NIH in Bethesda, Maryland. Doppman and colleagues Giovanni Di Chiro, Ayub Ommaya, and Edward Oldfield were the American contingent of the "American/English/French connection" (see also Fig. 7). (Photograph courtesy of Anne Marie Doppman.) Center: Portrait of the radiologist Giovanni Di Chiro, a major contributor to the effort at the NIH. (Photograph courtesy of Barbara and Giovanna Di Chiro.) Right: Portrait of Edward Oldfield, who, along with neurosurgical colleague Ayub Ommaya, collaborated with radiologists John Doppman and Giovanni Di Chiro at the NIH from the 1960s to the 1980s.

The three transcontinental centers—the vanguard of the modern era—can be viewed as the "American/English/French connection" in terms of their combined effort in generating new insights concerning the angioarchitecture, pathophysiology, and treatment of spinal vascular lesions (Fig. 7). Their contributions led to the following classification, which consists of four types of lesions: Type I, dural AVFs (Fig. 8); Type II, glomus AVMs; Type III, juvenile AVMs; and Type IV, direct spinal AVFs (this type was introduced by Heros et al.;[11] see Appendix).

Chart depicting three centers in England, France, and the US, each actively pursuing studies on spinal vascular disorders from the 1960s through the 1980s. Although the three centers worked independently, there was considerable intellectual interaction, with their combined effort resulting in significant contributions to the understanding of the angioarchitecture, pathophysiological mechanisms, and treatment of spinal vascular lesions.

Artist's drawing of an intradural dorsal spinal AVF. Dural AVFs represent the majority of spinal vascular abnormalities. The intradural lesion shown here may be treated surgically by coagulation and transsection; those that are extradural may be effectively embolized. Reprinted with permission from Spetzler RF, Detwiler PW, Riina HA, Porter RW: Modified classification of spinal cord vascular lesions. J Neurosurg (Spine 2) 96:145-156, 2002.

As the pathophysiological mechanisms and spinal vascular anatomy became better understood, a number of talented practitioners brought the new therapeutic procedures into popular use. Among these were neuroradiologist Alex Berenstein[3] (Fig. 9) of New York City and a Swiss neurosurgeon of Turkish descent, Gazi Yasargil (Fig. 10 left), who learned microneurosurgical technique in the laboratory of the pioneer microneurosurgeon R. M. Peardon Donaghy (Fig. 10 right) at the University of Vermont in Burlington, Vermont. In the earlier years of the modern era, neurosurgeon Leonard Malis (Fig. 11) of New York City, among others, developed considerable surgical experience with spinal vascular disorders and taught the techniques to his residents and to practicing neurosurgeons.

Portrait of Alex Berenstein, a neuroradiologist who practiced at St. Luke's Roosevelt Hospital and at Beth Israel Hospital in New York City; he became a leading interventional specialist.

Left: Portrait of Gazi Yasargil. Along with his chief, Hugo Krayenbühl, Yasargil played an important role in bringing microsurgical techniques to popular use in spinal vascular disorders. (Reproduced with permission from Lippincott Williams & Wilkins. From Anonymous: Proceedings of the Congress of Neurological Surgeons. New York City, New York 1984. Clin Neurosurg 32:1-680, 1985.) Right: Portrait (inset) and photograph of R. M. Peardon Donaghy, the pioneer microneurosurgeon who introduced the microscope into neurosurgery. He taught a generation of neurosurgeons microvascular techniques that were then applied to spinal vascular lesions. (Portrait courtesy of the Society of Neurological Surgeons; candid photograph from M.G. Yasargil, Microsurgery Applied to Neurosurgery, Georg Thieme Verlag, Stuttgart, 1969. Reproduced with permission from Thieme.)

Portrait of Leonard Malis, of Mount Sinai Hospital in New York City, who made important contributions to microneurosurgery, with his refinement of Greenwood's original (1940) bipolar coagulator and introduction of video through the microscope. Malis gained considerable experience with surgery for spinal vascular disorders, developing techniques that he taught to his residents and to practicing neurosurgeons. (Photograph courtesy of the Society of Neurological Surgeons.)

In 2002, based on their experience with a large number of surgically treated cases of spinal vascular anomalies, clinicians at Hôpital Bicêtre[16] in France offered a classification with two broad categories: AVMs and AVFs. In addition, a genetic classification of arteriovenous shunts was proposed. In the same year that the Bicêtre classification was proposed, Spetzler and his coworkers[21] advanced a modification of the popular designation of Types I through IV, and they added neoplastic vascular lesions to their simplified nomenclature for purely vascular lesions: aneurysms and arteriovenous lesions (with subcategories); they also introduced AVMs of the conus medullaris as a new category of AVM (see Appendix).

Because diagnostic techniques and treatment options have significantly improved since the 1960s, it is now possible to identify patients for whom successful surgical or embolic occlusion can be expected. Modern diagnostic imaging likewise enables us to identify those with extensive involvement of the spinal cord, for whom neither surgical nor embolic treatment is feasible.[14–21]

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