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1 History

A Short History of the Diagnosis and Treatment of Cerebral AVMs

As attested by F. Henschen (1955) angiomatous malformations and tumors have been, since Virchow’s time, a “problem child” of pathologists. Hamby (1958) defined the main problems posed in understanding the pathology of these lesions and his statements are valid even today:

“The origin and anatomy of the cerebral angiomas has frustrated pathologists over the years as much as their treatment has baffled surgeons. An extensive literature has developed, replete with picturesque nomenclature based upon attempts to describe the appearance of lesions seen at the operative table or at necropsy. The surgical descriptions are not entirely basic nor accurate because the bulk of the lesion is largely submerged under the cortex and hence invisible to the examiner. The pathologic descriptions have been faulty because of deflation of the lesion at the time of examination by lack of the expansile blood stream that characterizes them in life. Also confusing the picture of the dead lesion are the alterations produced in the component vessels by blood under arterial pressure, which dilates veins and “arterializes” them to withstand the added stress. Vascular resistance being lowered by the shunt, arteries dilate to carry more blood under less than usual pressure, and lose some of their usual characteristics.”

However, the introduction of cerebral angiography (Moniz 1927) together with the continuing improvements in the quality of angiograms and the remarkable developments in vascular catheterization techniques (Seldinger 1953, Djindjian 1962) has opened up new dimensions in the study of the morphological and hemodynamic aspects of AVMs.

This short historical review may help to understand how we have arrived at the present day interpretations of AVM pathology and development and how modes of treatment have evolved.

Pre-17th Century

Descriptions of vascular malformations of the skin and other visible organs such as eye, lips and ear with occasional comments about their often ugly appearance and the difficulty or impossibility of treatment may be seen in some of the earliest recorded historical manuscripts.

The Papyrus Ebers (ca. 1500 BC) contained descriptions of hemorrhoids, skin tumors, hydroceles, varicose veins and aneurysms. Kharadly (1956) showed that hernias and aneurysms were operated upon even in those times but not AVMs. The warning, “You must keep your hands off – Noli me tangere” is stated in the relevant chapter.

Virchow cited prominent physicians like Hippokrates, Galen, Celsus, Aetius, Avicenna, and Vidus Vidius, who were dealing with the diagnosis and treatment of different types of external vascular malformations. Von Bramann (1886) showed that Galen and Delia Groce knew of varicose pulsating swellings and took them to be simple arterial aneurysms. Osier (1915) noted that references to vascular malformations are to be found in the works of Antyllus (2nd Century) and Abulcasis (10th Century).

17th–19th Century

The great breakthroughs in the understanding of the systemic circulation and of the cerebral circulation were made by Harvey (1628) and Willis (1664) respectively.

William Hunter (1718–1783)

(By kind permission of the President and Council of the Royal College of Surgeons of England)

John Hunter (1728–1793)

The work of Harvey and Willis was subsequently complemented by the discovery of the capillary system by Malpighi (1661) and this paved the way for modern theories regarding the evolution and pathology of AVMs.

In the following century (1757) William Hunter was able to identify the clinical characteristics and some hemodynamic aspects of extracranial AVMs. In “Observations on arteriovenous malformation, London Medical Observations and Enquiries, 1762” he wrote: “Vascular malformations of the extremities are caused by an abnormal communication between arteries and veins.” Enthusiastic phlebotomists of that period prepared two perfect examples of arteriovenous aneurysm for W. Hunter, which he was quick to recognize (cit. Dandy 1928); at the point of communication between the artery and the vein, he recognized a loud hissing bruit and a strong tremulous thrill: large tortuous sacs were seen to pulsate; the brachial artery was greatly enlarged and serpentine cephalad to the arteriovenous fistula, but distal to it, the artery became smaller than on the other side. He was able to reduce the size of the vein, stop their pulsation and eliminate both the bruit and the thrill by pressing on a localized spot, which he recognized to be the opening between the artery and vein. It was William Hunter who first suggested the term “anastomosis” to denote the union of the two vessels, whereas the term “collateral” was introduced by his younger brother John Hunter who also ligated the femoral artery in a case with popliteal aneurysm and proved the efficiency of the collateral arterial system.

The broad scientific approach concerning the nature of these impressive aberrations began with pathologists and surgeons 200 years ago who described them as “erectile tumors” and swellings of the skin and organs. The advent of medical journals enabled the scientists to publish their observations.

After 1850 the number of publications concerning these erectile tumors increased rapidly. Between the time of William Hunter (1762) and Sonntag (1919), 65 such publications are to be found: Plenck (1776), Bell (1796), Cruveilhier (1816), Meckel (1818), Dupuytren (1834), Vidal (1846), Rokitansky (1846), Virchow (1851), Gerdy (1852), Schuh (1853, 1866), Busch (1854), Luschka (1854), Esmarch (1854), Lebert (1857), Bennet (1854), and Alibert (1871). More detailed information regarding these papers may be found in the works of Heine (1869), Weber (1869), Körte (1880) and Heineke (1882). Pathological classification based upon varied anatomical descriptions was already becoming clumsy and confusing. By 1894 Wagner had collected from the current literature 24 different nomenclatures. In parallel with changing pathological concepts, the surgery of extracranial AVMs was undergoing a gradual evolution.

Treatment of Extracranial AVM in Earlier and Present Time

The endeavours of general surgeons in dealing with the dangerous and disfiguring extracranial vascular malformations (scalp, external ear, eyelids, orbits, cheeks, lips, tongue, palate and neck) are most informative for the interested neurosurgeon (Beck, Berger, Billroth, Brodie, von Bruns, Bryant, Busch, Caradec, Clairmont, Dalrymple, Dupuytren, Emanuel, Enderlen, German, Goldmann, Heineke, Krause, Lefort, Lieblein, Nélaton, Pilz, Roth, Russell, Schwalbe, Schwartz). Their methods of treatment have, in the past, included:

1) Injection of the lesion with: ferrous chloride, glycerin, tannin, chlorzin, carbonic acid, alcohol,

2) Electrocauterization,

3) Ligation,

4) Extirpation.

The variety of modern therapy of external vascular malformations (Williams 1983) shows that therapeutic difficulties still remain in the treatment of these easily approachable lesions:

1) Corticotherapy (new born children),

2) Radiotherapy,

3) Electrocoagulation,

4) Cryotherapy,

5) Surgery,

6) Use of laser beam,

7) Embolization.

As in neurosurgery, the advice of most plastic surgeons is that simple ligation of feeding vessels is inadequate and inadvisable.

Intracranial Angiomas

The Contributions of Virchow and his Contemporaries

After exhaustive research work on cavernomas of the liver, Rokitansky (1842–46) came to the conclusion that these were either benign or malignant tumors independent of the surrounding vascular system. Volume 6 of Virchow’s Archive (1854) contains 3 remarkable papers: Esmarch (pp. 34–57): “Über cavernöse Blutgeschwülste”, Luschka (pp. 458–470): “Cavernöse Blutgeschwülste des Gehirns” and Virchow (pp. 526–554): Über cavernöse (erectile) Geschwülste und Teleangiektasien.” Esmarch und Luschka fully supported the neoplasia hypothesis of Rokitansky.

Luschka provided one of the earliest descriptions of an intracranial arteriovenous anomaly in a patient with a frontal cavernoma.

Luschka recognized two types of “Blut-Geschwülste”:

1) Telangiectases (non neoplastic) arising due to a metamorphosis of capillary systems.

2) Cavernous tumors (neoplastic) containing large blood-filled compartments.

The young Virchow, who was involved with research into infection of blood vessels, also published (1851) a remarkable paper concerning “the dilatation of small vessels”. In this paper he described and discussed thoroughly his own observations and thoughts and clearly refuted the hypothesis of Rokitansky. In 1863 Virchow published a comprehensive study which may be called the first real milestone in the history of the AVM. In the 3rd volume of his monograph, 200 pages (pp. 306–496) are devoted to the phenomenon of the physiological and pathological changes of blood vessels in all organs. His descriptions profoundly contradicted contemporary opinion. He described telangiectases, venous, arterial, arteriovenous and cystic angiomas (nowadays angioblastomas), and their transitional types, and discussed in detail the pathogenesis of these malformations. He reflected on the atlas of Cruveilhier and the pioneering work of John Bell (The Principle of Surgery, London 1826, Volume 3, pp. 326–383, First Edition, London 1796). Bell described cavernoma, AVM and angioblastoma but gave all of them the nomenclature of “Aneurysm per Anastomosis”. Virchow said: “This description is still perfectly valid, (p. 328): Aneurysm per anastomosis is an entire change of structure; it is a dilatation of veins, in which they are forced and enlarged by the diseased action of their corresponding arteries. Those happen in consequence of original malformation, a violent action of arteries, and a mutual enlargement of arteries and veins, while the intermediate substance of the part is slowly distended into large intermediate cells, which are dilated to formidable reservoirs of blood. – The blood is poured into the cells of such a tumor by innumerable arteries: from these the blood is continually following into veins, which receive it with such patent orifices etc. The veins form a conspicious part of such a tumor, but the intermediate cells are an appreciable part of the structure… (p. 397). All this proves that it is a tissue of small arteries and veins; it fills not like a varix slowly; its filling is by distinct thrombs; it is filled by its small and numerous arteries, and its swelling is (like the erection of the penis) produced by the pulsation of the arteries, stroke after stroke, pouring out their blood into cells.”

“The tumor is a congeries of active vessels and the cellular substance through which these vessels are expanded, resembles the cellular parts of the penis, the gills of a turkey cock or the substance of the placenta, spleen worms.”

It is interesting to speculate as to whether Bell was describing a cavernoma or an AVM. It certainly sounds like the modern description of an AVM and its nidus.

Virchow (1854), cited Gerdy (1852), who differentiated eight types of “erectile tumors” and noted the great number of publications concerning the “erectile tumors” and the difficulties with their classification. He preferred the term of “angioma” which was introduced by J. Hughes Bennet (1854) instead of the term of “angionoma” which was advocated by Follin (1861). He credited to Plenck (1776) the term “cavernoma”, a nomenclature well recognized in the German literature (Meckel 1818).

Cushing and Bailey (1928) concluded, quite wrongly, that Virchow believed in the neoplastic nature of vascular malformations as proposed by Rokitansky. This error was most likely due to difficulties with translation of the original papers.

Virchow (1863) divided angiomas into cavernous, simple telangiectatic, racemose, and lymphatic types. Racemose angiomas were divided further into arterial and venous types.

Page 474 of Virchow’s 3rd Volume (1863) relates to a case of a large extracranial parietooccipital AVM in a man from Florence and described by Vidus Vidius in 1665. Virchow commented that this type of malformation originates through accommodation between artery and vein with consequent dilatation of them (arteriectasie and phlebectasie, p. 471). They are of congenital origin (p. 475). They may grow or spontaneously regress (p. 482). The following nomenclature has been used: aneurysma per anastomosis (Bell) or aneurysma anastomoseon (v. Walther), aneurysma per transfusionem (Dupuytren 1834) and other authors used the term of aneurysma arteriovenosum, or aneurysma varicosum.

Virchow argued (p. 472) that aneurysms would not arise as a result of arteriovenous communication in traumatic cases, therefore the best term would be aneurysma spurium arteriovenosum.

Virchow’s main concern was not so much nomenclature as the pathophysiology of the lesions. The founder of cellular pathology had a profound interest in pathophysiology. He performed injection studies on the pregnant uterus and placenta and was fascinated by the temporary but enormous increase in capacity of vessels during gestation. In 1851 he spoke of “The physiologic paradigm in the corpora cavernosa of sex organs and the paradigm of pathology in cavernoma and telangiectasis”, and further questioned as to whether one type of angioma can transform into another by changes in flow and pressure or by cellular proliferation.

Early Clinical Observations on Intracranial AVMs

Pfannenstiel (1887) and Kaufmann (1897) observed young (22 and 23 years) primipara patients, who died with acute cerebral symptoms. Autopsy study showed a ruptured varicose anomaly of left thalamus opticus and the vena Galeni in one case, and a ruptured varicose anterior callosal anomaly in another.

D’Arcy Power (1888) found, a large AVM in the left sylvian fissure at autopsy on a 20-year-old man who had suffered a hemiplegic stroke and died.

Steinheil (1894) described the history and pathologicoanatomical findings in a patient (59 years) with a large right frontal AVM which drained partially to the vein of Galen. He may thus be credited as being among the earliest to describe the symptomatology of the disease.

Rizzoli 1873 observed a right occipital pulsating swelling in a 9-year-old girl. The pulsation disappeared on compression of the left occipital artery. The girl died from an apparent meningitis (perhaps, in fact, from an intracranial hemorrhage). At autopsy she was found to have an AVM of the occipital region (-duralpial) with drainage to the transverse sinus. There was a defect in the occipital region of the skull so that the pulsation in the AVM could be felt externally.

The first clinical diagnosis of a cerebral AVM was made by Hoffmann (1898). Isenschmid followed the history of this patient, who was presented to medical colleagues in Heidelberg, and discussed the differential diagnoses (1912). He pointed out that the clinical diagnosis of cerebral angiomas had never before been made.

With the onset of operations for brain tumors around 1890, the number of cases of AVM observed clinically, pathologically and surgically began to rise sharply. At that time, contralateral parietal craniotomy for cases of Jacksonian epilepsy occasionally produced an unexpected AVM. Between 1890 and 1936 there were more than 90 reports of around 120 cases of cerebral AVMs. In the cases of Rizzoli (1873), Hoffmann (1898), Isenschmid (1912), Haenel (1926), Eimer and Mehlhose (1927) and in some of the cases of Dandy (1928) and Cushing and Bailey (1928) the diagnosis was made clinically.

The list of authors who published cases of AVM prior to the angiographic era includes:

Morris (1871), Rizzoli² (1873), von Braman (1886), Pfannenstiel (1887), D’Arcy Power (1888), Giordano¹ (1890), Guldenarm and Winkler¹ (1891), Péan¹ (1891), Starr and McCosh¹ (1894), Steinheil (1895), Lucas-Championnière¹ (1896), Kaufmann (1897), Emanuel (1898), Hoffmann² (1898), Ribbert (1898), Beadles (1899), Shoyer (1900), Struppler (1900), von Bergmann¹ (1901), Chipault¹ (1902), Deetz (1902), Rotgans and Winkler¹ (1902), Kreutz (1903), Bail (1904), Drysdale (1904), Heitmüller (1904), Simmonds (1905), Strominger (1905), Sternberg (1905, 1907), Falk (1906), Lavillette¹ (1906), Dürck (1907), Enders (1908), Krause¹ 1908), Stertzing (1908), Leischner¹ (1909), Ranzel (1909), Tuffier¹ (1909), Blank (1910), Therman (1910–13), Znojemsky¹ (1910), Abrikosoff (1911), Astwazaturoff (1911), Cassirer and Mühsam¹ (1911), Isenschmid² (1912), Schmolck (1912), Wichern (1912), von Eiselsberg and Ranzi¹ (1913), Kaiserling (1913), Wischnewski (1913), Castex and Bob (1914), Leunenschloss (1914), Maklakow¹ (1914), Orbison¹ (1915), Versé (1918), Bort (1920), Castex and Romano (1920), Schmidt (1920), Bannister (1921), Hammes (1921), Magnus¹ (1921), Nonne¹ (1921), Campbell and Ballance¹ (1922), Deist (1922), Worster-Drought and Ballance (1922), Müller (1923), Wohak (1923), Elkin (1924), von Lehoczky (1924), Mühsam¹ (1924), Rienhoff (1924), Esser (1925), Federoff and Bogorad (1925), Klimesch (1925), Laves¹ (1925), Marx (1925), Reid (1925), Dowling (1926), Globus and Strauss (1926), Haenel² (1926), Klimesch (1926), Leeser (1926), Bregman (1927), Eimer and Melhose (1927), Herzog (1927), Olivecrona and Lysholm¹ (1927), Perthes¹ (1927), Worster-Drought and Dickson (1927), Buckley (1928), Cushing and Bailey^1,2 (1928), Dandy¹ (1928), Ruehl (1929), Yates Paine Brockman^1,2 (1930), Brock and Dyke (1932), Krug and Samuels (1932), Dimitri and Balado (1933), Levine (1933), Love (1933), Schaltenbrand (1938), Sattler (1939).

Surgical Treatment of Cerebral AVMs (1889–1930)

Most of these early procedures were carried out by general surgeons (Table 1.1). Giordano is credited to have operated upon the first cerebral AVM in 1889. Regarding his original paper, however, it is clear that he simply ligated a pathological vessel on the left parietal surface and did not expose the remainder of the AVM located in the deep subcortical tissue.

Jules Emile Péan (1830–1898)

(By kind permission of Prof. H. M. Koelbing, Director of the Institute of Medical History, University of Zurich)

The first complete excision of a cerebral AVM was made 98 years ago by the famous French surgeon Péan. He treated a 15-year-old boy who had suffered a left sided Jacksonian fit, and made a diagnosis of a right sided central tumor. The operation took place in May 1889 and was described thus by Péan:

“Au cours de l’opération, nous nous trouvâmes en présence d’un angiome des méninges en communication avec les sinus longitudinal supérieurs. Malgré sa richesse vasculaire, malgré son étendue, la tumeur put être enlevée en totalité, sans perte de sang, grâce au pincement temporaire et définitif des vaisseaux variqueux, dilatés, érectiles, dont elle était composée. A ce propos, nous avons recherché, dans la science les faits de ce genre, qui avaient été publies et nous n’en avons trouvé aucun qui fut exactement semblable, aucun surtout qui eût été opéré.” Péan’s conclusion is optimistic: “– De même qu’il existe des angiomes extracrâniens communiquants à travers la voute du crâne avec le sinus longitudinal supérieur, il existe une variété d’angiomes intracrâniens communicants également avec les sinus longitudinal supérieurs, mais développés dans l’épaisseur des méninges et situés entièrement à l’intérieure du crâne. Les tumeurs sont justiciables de la trépanation, l’hémorrhagie et notamment celle due à la communication avec les sinus, et facilement arrêstée par le pincement temporaire et définitif.”

Neurosurgical Approaches Prior to the Introduction of Angiography (1928)

Cushing (1909–1928) and Dandy (1921–1926) each described their operative experiences in 14 and 15 cases respectively, of venous and arteriovenous malformation and added cases from the literature. Both of their series were published in the same year (1928) and reading the original descriptions it seems likely that all their cases were true arteriovenous malformations. Dandy felt that the only way to cure an arteriovenous aneurysm was to ligate the entering arteries or to excise the whole vascular tumor. Earlier, he had lost one patient from hemorrhage during the operation and a second case from intracerebral hemorrhage following total extirpation and he wrote: “But the radical attempt at cure is attended by such supreme difficulties and is so exceedingly dangerous as to be contraindicated except in certain selected cases… As in most cerebral lesions, however, each case should be considered a law unto itself. There are large aneurysms and small ones; those which are mostly arterial, others mainly venous; some are superficial, others deep, some are in highly important areas of the brain, others in portions largely silent. All of these factors, and finally the patient’s wishes in the matter, must be weighed. An aneurysm in the left cerebral hemisphere in a right handed person is surely noli me tangere under all conditions. Any attempted cure, even if successful, would almost surely result in disturbances of speech or motor power, or of both… there is more reason to attempt to cure a patient who has an arteriovenous aneurysm in the right hemisphere.”

Cushing’s experience with operations for cerebral angiomas dated back to 1909. Some brief extracts from his excellent operative accounts follow:

Case 1: A 39-year-old patient presented with raised intracranial pressure thought to be due to a cerebral neoplasm and was operated upon on 3.2.1909: “Left subtemporal decompression was made… The dura was not particularly tense. When opened a large thin-walled venous lake was disclosed, from which branches spread in various directions… It seemed unwise to attempt it.”

Case 2: A 4-year-old child with right sided congenital exophthalmos and bulging in the right temporal area; September 4, 1920: “When the dura was reflected there came into view a mass of hugely dilated vessels, evidently veins, which covered the entire temporal lobe. Two of the main vessels were ligated but extirpation was obviously impossible.”

Case 3: 30-year-old male, operated on March 18, 1921: “A left osteoplastic exploration was made. When the dura was opened an enormous tangle of dilated veins was disclosed spreading upward from about the region of the arm-center. The larger vessels were fully as big as the little finger. The chief emerging vein was ligated but all attempts to get beneath or between the larger vessels were accompanied by so much bleeding that their ligation or extirpation was deemed impossible.”

Case 4: “April 25, 1921: … On reflecting the dura an exceedingly wet brain was disclosed with two huge veins on the surface, one running largely in the sylvian fissure. The other, more vertical, lay in the precentral fissure… Since the operator felt some regrets at not having been more radical in his attacks upon the lesion in the preceding case, a ligature was first thrown around the large descending vein at the point… A second ligature was then put on, which must have started trouble from stasis in the main varix which became hardened and swollen… Finally bleeding began to occur from around the sides of the varix and a rupture seemed imminent. There was evidently only one thing to do – to catch the base of the protruding lesion with a large curved clip and to throw a ligature around the whole mass. This desperate step was taken and the cavity, which continued to bleed after the ligature was placed, was finally filled with a slab of muscle taken from the patient’s leg, before the excessive venous hemorrhage could be controlled. There had been a sharp fall in blood pressure from which she finally recovered without transfusion… As was to be expected, the patient showed a postoperative right hemiplegia and aphasia… Nearly seven years since her operation, regards herself, aside from some remaining weakness of her right arm, as in normal health.”

Depressed following such an experience Cushing wrote:

“One could hardly have chosen a worse place than over the lower motor area of the leading hemisphere in which to attempt the surgical removal of a racemose varix.” The untoward results of the procedure in this case resulted in a more cautious attitude when a similar lesion was disclosed in the next patient (left postcentral region): “December 28, 1922: No attempt was made to treat the lesion by ligature or otherwise.”

Cushing reviewed the poor results of other workers and warned: “The surgical history of most of the reported cases shows not only the futility of an operative attack upon one of these angiomas, but the extreme risk of serious cortical damage which is entailed… How many less successful attempts, made by surgeons less familiar with intracranial procedures, have gone unrecorded may be left to the imagination.”

“The lesions, in short, when accidentally exposed by the surgeon, had better be left alone, and how much radiation may accomplish for them is undetermined though there are favourable experiences on record. So long ago as 1914 Wilhelm Magnus of Oslo unexpectedly exposed at operation a venous angioma of the left rolandic region, a decompression was made with the intention of treating the lesion with radium therapy which at that time was known favourably to influence cutaneous angiomas. After treatment, the decompression, which was bulging, receded, and the epileptiform attacks, from which the patient was suffering, became infrequent and finally disappeared …”

The publication of Reichert (1946) is unique, as he reported 15 cases of premotor vascular anomalies causing Jacksonian epilepsy, which were treated successfully by coagulation of the dural and pial vessels of the lesion (1935 to 1941).

Neurosurgical Treatment of Intracranial AVM Following the Introduction of Angiography (1930)

As we have seen, surgical excision of AVMs was carried out between 1889 and 1930, both by general surgeons and neurosurgeons. Some of these cases met with success, others ended disastrously. After one or two bad results most surgeons did not risk further attempts at excision.

With the advent of cerebral angiography the position began to change, for it became possible not only to diagnose the AVM but also to obtain some idea as to its location, its size and construction and the number of feeding and draining vessels. Angiography, however, was still somewhat primitive and the contrast material imperfect. Only a few angiographic demonstrations of cerebral AVMs were published before 1936 (Dott 1929, Löhr and Jacobi 1933, Moniz 1934 and 1951, Olivecrona and Tönnis 1936). Dott provided the first demonstration of the angiographic aspects of cerebral AVMs at the Neurosurgical Conference in Stockholm in 1935. However, the full benefits of cerebral angiography came only with improved techniques which were not widely available until the 1950s.

Olivecrona had a disappointing experience in 1923 when exploring for an infratentorial tumor (case 65). He was confronted with a highly vascular AVM and the patient died. In another case (66), with right parietal AVM, two surgical attempts remained unsuccessful. In future years Olivecrona (1927) urged caution in attempting surgery for an AVM found unexpectedly at operation. In this respect, his attitude was similar to that of Cushing and Dandy.

Left carotid angiogram showing a frontoparietal AVM. In the monograph of Egas Moniz, “L’Angiographie Cérébrale”, Masson, Paris 1934.

On May 5, 1932 Olivecrona carried out his first successful radical removal of a left cerebellar AVM on a 37-year-old male. The preoperative diagnosis was tumor or tuberculoma. The stormy operation was performed under local anesthesia, took 8 hours and the patient needed a transfusion of 2000 ml. The postoperative course was uneventful and the patient left the hospital 3 months later. In the next case (a 52-year-old female with right temporal AVM) diagnosis had been made preoperatively and verified on angiography. Olivecrona’s 16 cases together with 6 cases operated upon by Tonnis and 4 venous angiomas were presented in their classical monograph in 1936 (Bergstrand et al. 1936). Out of 26 cases only 2 dural and 3 parenchymal AVMs could be extirpated. They were cautions in advising operation saying that “Some polar AVMs and those in silent areas of the right hemisphere have been declared to be extirpable and curable, but in most cases the situation seemed to be unfavourable. A successful removal can be accomplished if all the feeders are eliminated, but this is only possible in a few cases.” The authors did not recommend techniques of cerebral decompression or ligature of the internal carotid artery.

Twelve years later Olivecrona published his extensive experience in 64 cases and mentioned also the surgical results of Penfield and Erickson (1941) and Pilcher (1946 a, b) together with the 7 successfully extirpated cases described by Dott in a personal communication Olivecrona and Riives (1948). By 1954 Olivecrona had removed 81 cerebral AVMs with quite exceptional results (Table 1.2).

The overall mortality for the series was 9% (7 cases), but most of these were early cases. In between 1951 and 1956 there was only a single operative death.

The opinion that small to moderate sized AVMs in silent areas of the brain should be operated upon while, others in nonsilent areas were better left untouched, found general acceptance among neurosurgeons. Within 25 years (1932–1957) approximately 500 patients with cerebral AVMs had undergone surgery; Olivecrona and Lysholm 1927, Dott 1929, Tönnis 1934, Puusepp 1935, Bergstrand, Olivecrona and Tönnis 1936, Röttgen 1937, Moniz 1938, Seeger 1938, Sorgo 1938, Singleton 1939, Northfield 1940/1941, Krayenbühl 1941, Penfield and Erickson 1941, Asenjo and Uiberall 1945, Jaeger and Forbes 1946, 1950, Pilcher 1946, Dott 1948, Olivecrona and Riives 1948, Pluvinage 1948, Trupp and Sachs 1948, Norlén 1949, Olivecrona 1949, 1950, Sorgo 1949, McKissock 1950, Pilcher et al. 1950, Sunder-Plassmann 1950, Basset 1951, Gros and Martin 1951, Kraus 1951, Petit-Dutaillis and Guiot 1951, 1953, Thiébaut et al. 1951, Wechsler et al. 1951, Whitney 1951, Amyot 1953, Arné et al. 1953, Druckemiller and Carpenter 1953, Ebin 1953, Gillingham 1953, Krayenbühl and Yaşargil 1953, Laine and Delandsheer 1953, 1956, Lazorthes and Géraud 1953, McKenzie 1953, Montrieul et al. 1953, Pompeu and Niemeyer 1953, Selverstone and White 1953, Tönnis and Lange-Cosack 1953, Falconer 1954, Logue and Monckton 1954, Martin and Brihaye 1954, Milletti 1954, Pimenta and da Silva 1954, Pluvinage 1954, Scott et al. 1954, Carton and Hickey 1955, Gould et al. 1955, Olsen and Wood 1955, Potter 1955, Hayne et al. 1956, Leppo et al. 1956, Lundberg et al. 1956, Paillas et al. 1956, Paterson and McKissock 1956, Philippides et al. 1956, Asenjo et al. 1957, Baker 1957, Hamby 1957, Krayenbühl and Yaşargil 1957, 1958 (90 cases, 26 radical removal), Ley 1957 (23 cases, 9 extirpations), McKissock and Hankinson 1957 (100 cases, 68 operated), Milletti 1957, Niemeyer 1957, Norlén 1957, Olivecrona and Ladenheim 1957 (100 cases, 81 operated), Paterson 1957, Tolosa 1957, Tönnis 1957, Af Bjorkesten 1959, Paillas et al. 1959, Tönnis et al. 1958.

Diagram of a temporooccipital AVM. Published in “An Introduction to Clinical Anatomy”, 1932, London, by Traquair. The angiography was performed by Norman Dott in 1929 with sodium iodide. Also published in the monograph of Egas Moniz, “L’Angiographie Cérébrale”, Masson, Paris 1934.

The results achieved were remarkable. The mortality for small AVMs was between 0 to 5%, and for moderate sized AVMs was generally between 6 and 10%, although some authors found mortality rates of over 20%. Over 60% of patients returned to a full working capacity after operation and serious morbidity was around 10%. Norlén (1949) was particularly successful in that he was able to remove AVMs totally in 10 patients with no mortality and only a small and temporary morbidity. Norlén’s other principal contribution was his statement that “The malformation may cause cerebral circulatory failure. Notice that the arteries of the hemisphere surrounding the AVM, which are hardly seen in the preoperative angiogram, filled normally with contrast once the AVM has been removed. In most cases the postoperative angiograms show that the enlarged and tortuous proximal feeding vessels returned to a normal diameter usually within 2 or 3 weeks.” Following on from this concept, Murphy (1954) first described the concept of “cerebral steal syndrome”.

The First European Congress of Neurological Surgeons (Brussels 1957) included discussion on experience gained in operating on cerebral AVMs. It was generally accepted that palliative procedures such as decompression, ligation of the carotid artery or partial coagulation and partial removal of the lesion were ineffective and that complete removal should be the aim in all possible cases. There remained uncertainty regarding the operability of small or moderate sized lesions in eloquent areas of the brain and in cases of large AVMs. Nevertheless, the first approaches in this direction were already being made by Laine et al. (1956) and Houdart and Le Besnerais who published their results in 1963.

The Limitations of Surgery

Eloquent Areas of the Hemispheres

Pluvinage (1954) predicted a tendency towards more radical removal of all AVMs with the size, shape and location of the lesion becoming a secondary problem.

Tönnis (Tönnis and Schiefer 1959, Tönnis 1961) carried out careful studies of general and localized blood flow and presented 215 patients with cerebral AVMs in which he had achieved complete removal in 118 cases, with 54 AVMs being in eloquent areas. He felt that total removal of an AVM was certainly possible and was the best form of treatment. Preoperative deficits frequently declined after operation and newly acquired deficits were mostly of a temporary nature.

He concluded that

1) The location of an AVM is not a primary reason for inoperability,

2) The preoperative neurological deficits may be reduced after surgery,

3) The mortality in selected cases was 9.5%,

4) Major contraindications to surgery were large voluminous AVMs and elderly patients.

Kunicki and Zoltan described their experience at the 1967 Madrid Meeting of the Congress of European Neurological Surgeons:

Kunicki had successfully removed 2 AVMs from the motor-sensory area and Zoltan described 38 cases of removal of AVMs lying predominantly in the motor cortex or speech areas, in the region of the middle cerebral artery. Of these patients, 4 died postoperatively, and just 2 had mild postoperative neurological disorders. Of 5 patients who had suffered severe hemiplegias following previous hemorrhage 3 were improved after surgery. These authors felt that the main reasons for their success were that the vessels comprising the anomaly did not contribute in any way to the cerebral circulation and that the parenchyma included within and immediately adjacent to the angioma was functionally useless. Zoltan (1968) reemphasized this latter point. Further successes in operating upon AVMs in delicate areas of the brain were presented by Petit-Dutaillis et al. (1953), Laine et al. (1956, 1957), Achslogh et al. (1957), Houdart and Le Besnerais (1963), Pertuiset et al. 1963 and Christensen (1967).

Deep Seated AVMs

Deep seated AVMs lying within the striate, thalamic, parathalamic, limbic, intra- and paraventricular and callosal areas together with most infratentorial AVMs and those within the brain stem had always been generally declared inoperable. However, several surgeons did approach these lesions before microsurgical techniques became available. Olivecrona (1923), David et al. (1934), Alpers and Forster (1945), Boldrey and Miller (1949), Guillaume et al. (1950), Hamby (1952), French and Peyton (1954), Logue and Monckton (1954), McGuire et al. (1954), Carton and Hickey (1955), Strully (1955), Laine et al. (1956, 1957), Leppo et al. (1956), Poppen (1958), Caram et al. (1960), Dereux et al. (1959), Bonnal et al. (1960), Litvak et al. (1960), Pampus et al. (1960), Poppen and Avman (1960), Ralston and Papatheodorou (1960), Odom et al. (1961), Verbiest (1961), Ciminello and Sachs (1962), Levine et al. (1962), Houdart and le Besnerais (1963), Pertuiset et al. (1963), Castellano et al. (1964), Kunc (1965), Mount (1965), Pool and Potts (1965), Laine and Galibert (1966), Walter and Bischof (1966), Lapras et al. (1968), Milhorat (1970), Montant et al. (1971), Fényes et al. (1973), Ribaric (1974).

Kunc (1967) declared that: “For arteriovenous malformations in the basal ganglia and thalamus, ligation of feeding arteries may be the procedure of choice. This, however, carries the danger of producing unintentional infarction owing to the great anatomical variability of the blood vessels at the basal structures of the brain. The same operation can be very successful in one case and produce serious consequences in another. Very good results were achieved with this simple procedure in 2 cases of arteriovenous malformation on the anterior inferior cerebellar artery. To limit the operation to the ligature of supplying arteries is inadequate when the lesion is widespread for the arteriovenous shunt will increasingly attract blood from its small tributaries, which very soon become enormously dilated. Radical removal is the only effective method of treatment, if it is feasible.”

Morello (1967), at the congress in Madrid was of the opinion that “The outlook for patients with angiomas of the basal ganglia is very poor. There are a few accounts of fortunate cases in which the malformation, being small and emerging in the lateral ventricle, could be attacked directly with success, but unfortunately they are often large and cannot be removed.”

Nevertheless, Schürmann and Brock (1967) stated that “The reservations concerning the surgery of AVMs located in vital brain stem centers remain justified. The operability of such lesions seemed to depend upon site, size and clearcut delineation of the angioma, the number, caliber and source of the afferent vessels also whether their origin be uni- or bilateral, and the age of the patient together with the clinical course and picture of the illness.”

In 1967 microtechniques (including the operating microscope, bipolar coagulation, microinstruments and suture material) were introduced and the initial experience in 14 cases (including 4 deep seated AVMs) was published in the monograph of Yaşargil (1969). Splenial and large cerebellar AVMs could be completely removed with good results as presented to the 4th European Congress in Prague 1971.

The Symposium in Giessen (1974) was devoted to the problem of cerebral AVMs and the contributions were published by Pia in 1975. The papers showed a tendency toward more active surgery (Lapras 1975), with the introduction of new techniques such as microtechniques (Pia 1975, Bushe et al. 1975), electrothrombosis (Handa et al. 1975), cryosurgery (Walder 1975) and stereotaxy (Riechert 1975).

The Sixth International Congress of Neurological Surgery in Sao Paulo (1977) dealt once more with deep seated AVMs of the brain. Kunc gave an excellent survey of the achievement and limitations: “It must be recognized that deep seated AVMs are the cause of greater disability and mortality than those at other sites. Hemorrhages threaten function and vitally important structures.”

The large series from the Burdenko Institute was presented by Filatov et al. (1978). In 160 cases the AVM was totally removed, in 60 patients endovascular occlusion of the feeding arteries was performed and 56 other patients underwent various palliative procedures. Of 60 deep seated AVMs, 37 were totally removed and in 16 cases balloon occlusion was performed. There was only one death.

Steiner’s presentation at this meeting, showing results in 35 patients treated with stereotactically directed gamma rays, was a further milestone in the treatment of AVMs. Lesions up to 3 cm in diameter showed startling resolution after such treatment. Another promising radiation technique, especially for large lesions was presented by Kjellberg et al. (1977) in 33 patients.

Conservative versus Surgical Treatment

Cerebral AVMs may now be treated by conventional or loupe surgery, microsurgery, embolization and radiation techniques, either alone, or in combination. With each advance and refinement of these methods, especially together with the improvement of neuroanesthetic techniques, and the increase of our knowledge concerning cerebral hemodynamics, there has followed a greater tendency throughout the world towards intervention in cases of AVM, as soon as the diagnosis has been made. This has lead to a good deal of uncertainty regarding the natural history of untreated lesions and to a continuation of the uneasy feeling expressed by many authors that in a great many instances the outcome might be more favourable if the patient is left untreated. Until very recently (Crawford et al. 1986) the outcome in untreated cases had usually been described in only a very small number of patients in any given series. Comparison of treated and untreated groups is also made difficult by virtue of possibly selecting out of favourable cases for surgery i. e. patients who might anyway have had a favourable outcome had they been left untreated.

Olivecrona and Riives (1948) stated that in the end, probably most, if not all unoperated patients die of hemorrhage or are completely incapacitated. Olivecrona (1957) found that 25% of his untreated patients were to die of further bleeding, one third were to suffer serious morbidity, but that 25% were to remain healthy and almost asymptomatic many years after diagnosis. He stressed that the two groups of operated and non-operated patients could not be compared as they were no doubt selected according to differing points of view.

Botterell (1966) pointed out that progressive neurological deterioration may occur even though follow-up arteriography showed no change in the size of an AVM and he contributed this to progressive gliosis of surrounding cerebral tissue.

Paterson and McKissock (1956) stressed that the follow-up of untreated cases in their series did not contribute substantially to the knowledge of what might be termed the natural history of intracranial angiomas, largely because insufficient time had elapsed since their patients had been diagnosed. Yet it was worthy of note that few of them were severely incapacitated even after many years. Although angiomas may, through hemorrhage, lead to death or permanent incapacity, they felt they were much less likely to rupture than intracranial aneurysms. They felt that Potter (1955) had published figures which lent support to their view; 27% of his patients survived for more than 20 years after the onset of symptoms and more than half of them had only slight disability or none at all.

The increasingly aggressive attitude toward the surgical treatment of AVMs raised two controversial and interrelated issues:

1. Many retrospective series, although based on relatively small numbers of patients, seemed to prove that unoperated patients had a better prognosis.

2. The mortality and morbidity rates of operated cases’ in some series were not low (up to 18%).

Svien and McRae (1965) from the Mayo Clinic considered that 85% of patients with angiomas were best treated conservatively.

Perret and Nishioka (1966) analyzed 545 cases of AVM in a Cooperative Study and stated that the operative mortality should be less than 10% and the postoperative morbidity should be better than, or comparable to patients treated conservatively, for surgery to be justifiable. They found that the mortality in unoperated cases was 5% and in operated cases was 12%. These authors included palliative surgical treatments such as carotid ligation or partial resection in their surgically treated group. Therefore it is clear that a true comparison between operated and unoperated groups is impossible.

Pool and Potts (1965) collected 523 cases from the available literature. They found that the mortality and morbidity of the conservatively treated group was 56%, while that for 187 patients treated by radical excision was only 26%. They suggested that “on the basis of these data, excision of a symptomatic AVM seems advisable whenever surgery can be done with reasonable safety since it offers the best chance of saving a patient from progressive neurological and mental deterioration, epileptic seizures, or death from hemorrhage. This is because excision improves the circulation to those areas deprived of normal blood supply by the arteriovenous malformation of normal blood supply and removes the threat of a serious hemorrhage. On the other hand, excision is obviously contraindicated if the patient may become worse after surgery due to his age, condition, or the location and extent of the lesions. Excision of lesions in the occipital lobe or the posterior part of the temporal lobe may, for example, lead to permanent homonymous hemianopsia, but this seems a small price to pay for relief from the threat of progressive brain damage or a fatal hemorrhage. Under favourable conditions, moreover, an arteriovenous malformation can usually be excised without sacrificing significant amounts of intact tissue, even if this does lie adjacent to the sensory or motor cortex or involves the dominant temporal lobe.”

“As a rule children tolerate excision particularly well. Good results can also be expected from excision if the arteriovenous malformation is small and the patient is under 50 years of age and in a good preoperative condition. In patients over 50 years of age the need for excision is less urgent than in younger ones, since progressive enlargement of the arteriovenous malformation is less likely.” They concluded: “In our experience, approximately 75% of patients recover well following excision while some reports indicate even better results.”

French et al. (1964) considered that “AVMs are not in any sense to be considered new growths, but they may enlarge with time by expansion of the vessels and dilatation of aneurysmal sacs”. This seemed an important factor to be included in the evaluation of the necessity of surgical excision. On this basis the practice of surgical intervention seemed unquestionably superior to nonsurgical management.

However, in 1970, Troupp reported on 137 patients seen between 1942 and 1969 with angiographically verified AVMs. These were not operated upon, except for exploratory craniotomy in 2 cases (Troupp et al. 1969, 1970). At that time, he felt their follow-up figures indicated a more cheerful outcome than that postulated by others, notably Olivecrona and Riives (1948), Pampus et al. (1960) and Norlén (1966).

After 7 years Troupp reviewed the same 137 cases and changed his mind somewhat, for only 27 cases were well. Fourteen were described as fair but 28 were disabled and 9 more had died from hemorrhage (total 23). The only factor of interest he could relate concerning the prognosis was the location of the AVM. Of those situated in the frontal, temporal and occipital regions, only 2 patients died from bleeding while 21 of those situated in the parietal, central and infratentorial regions ruptured fatally.

Drake’s observations (1979) concurred with the view that while the initial course of an AVM is reasonably benign, the long-term outcome is less favourable.

Waltimo (1973) discussed the increasing size of an AVM in terms of prognosis: In a study of 21 patients with AVM subjected to serial angiograms (with a median time between examinations of 44 months), it was noted that 12 of the lesions increased in size, 8 remained unchanged, and one became smaller. He also found that smaller AVMs were the most likely to increase in size and the largest were the most likely to reduce in size.

Höök and Johanson (1958) found that in 12 cases: 8 increased in size, 4 remained unchanged and 1 disappeared and Stein (1984) found in his series that one third increased, one third remained unchanged and one third became smaller.

Kelly et al. (1969) followed 33 patients for an average of 15.5 years after their initial hemorrhage from an AVM. There was a mortality rate of 28% and half of the patients had little, if any disability.

Fults and Kelly (1984) found that the prognosis for patients presenting with seizures was more favourable than for patients presenting with hemorrhage, and that the mortality associated with recurrent hemorrhage did not increase significantly with successive bleeds. Patients with posterior fossa AVMs fared considerably worse than patients with an AVM located elsewhere in the brain. Pellettieri (1979), however, found that the risk of death in an unoperated group of patients followed over a period at 18 years, to be 2.5 times greater than in an operated group. The prognosis for children with intracranial AVM was not different to that for adults. The size of the AVM did not dictate either the clinical outcome for the patient or the risk of hemorrhage. There seemed to be no correlation between pregnancy (or delivery) and hemorrhage from a cerebral AVM in a female patient.

The publication of Pellettieri et al. (1979) was a milestone in the literature on the natural history of the AVM as the authors applied a differential analysis to their cases. By relating the results to 6 or 7 variables (age, sex, AVM-size, AVM-location, symptoms at onset and neurological findings at admission) it was possible to grade each variable with respect to prognostic importance. The most favourable risk factors were age below 40 years, absence of a neurological deficit, a superficial and small AVM in a silent area, female sex, and SAH at onset. These variables were assigned numerical values, and grouped on a scale ranging from +16 to −16. The AVMs with values of −10 or below were found to have a poor prognosis whether the condition was treated surgically or conservatively. In those ranked −8 or above, surgical treatment was considered to give consistently better results and in the AVMs with risk values between −2 and +2, a significantly better outcome could be expected with surgical or conservative management.

Their conclusions probably reflect the opinion of most neurosurgeons: “A favourable combination of variables gives relatively good results with both modes of therapy. Results deteriorate proportionally with falling values on the risk scale in both groups. Although surgery tends to give better results, the difference is only significant within a limited range on the risk scale. This probably explains the controversy between those who advocate surgery and those who prefer conservative treatment.”

Calica et al. (1984), recently took the idea of risk prediction a step further, using a complicated regression formula involving 14 variables to assess outcome (6). When they applied this formula to their 78 patients with intracerebral AVMs, it divided 85% of them into low (3% became impaired), medium (42% became impaired), and high (94% became impaired) risk groups.

Citing the paper of Calica et al., Wilkins (1985) has predicted that it may become possible with additional experience to use computerized paradigms to predict with greater accuracy the outcome of an intracranial AVM without surgery or with any of several possible treatment protocols so that the best approach can be planned. Until then, we must still rely on fragmentary published information about the “natural history” of such lesions and on a realistic assessment of our ever-changing abilities to deal with them surgically. Wilkins felt it had been difficult to assess the natural history of intracranial vascular malformations because they are varied in nature, they are frequently silent clinically, they are often treated when they are discovered and untreated lesions are not often followed in an organized way.

We would add to this argument the fact that many published data relate to unsufficiently analyzed cases. We agree also with the remarks of Mohr (1984), “The enormously accumulated studies concerning the natural history of the AVM is retrospective and the rarity of these lesions precludes any definitive prospective study of the natural history. Furthermore, the clinical picture of many of these lesions spans years if not decades. The remarkable variation of clinical material from center to center has become apparent and with it a hesitancy to offer such experience for publication.”

Most recently (1986) Crawford et al. reported upon 217 out of a total of 343 patients with cerebral AVMs, who were managed without surgery. He followed them for a mean of 10.4 years and, using life survival analyses, found that there was a 42% risk of hemorrhage, 29% risk of death, 18% risk of epilepsy and 27% risk of neurological deficit over a 20-year period. This represents the largest series of untreated cases studied over a long time span. He found, interestingly, that although small AVMs, as described by many authors, are more likely to present with hemorrhage in the first instance (82%) they did not subsequently carry a higher risk of recurrent hemorrhage. The operative rate in this series was only 34% with the tendency to leave untreated those AVMs which were large and deep, more posteriorly situated, in the left hemisphere or crossing the midline. However, the authors felt that the size, depth, and possibly the site of the arteriovenous malformations did not significantly affect outcome. The main influencing factors in their opinion were recurrent hemorrhage and increased age at diagnosis. Although the overall mortality at 20 years was 29%, only 65% of the deaths could be attributed directly to the AVM and then most commonly from hemorrhage. The risk of epilepsy is increased with temporal lobe lesions.

There are reasons other than those put forward by Mohr which make comparisons between operative and conservative management difficult:

a) The inclusion of ligation of extra- or intracranial vessels, coagulation and partial removal of the lesion and complete removal of the AVM under the term: “operated cases” is incorrect (Paterson and McKissock 1956, Pool and Potts 1965) (Tables 1.3 and 1.4).

The retrospective study of the 186 AVM cases of Krayenbühl (1936–1966) required separation of the patients into 3 groups: I Untreated, II Palliative treatment and III Complete removal of the AVM (Table 1.5).

A second analysis 15 years later (1984) clearly proved that the patients with complete removal of the cerebral AVM presented much better late results than the patients in group I–II (Table 1.5).

Twenty-one patients (20%) out of groups I–II had recurrent hemorrhages, whereas group III no case of recurrent hemorrhage occurred. Long-term clinical examinations have shown that only 15% of non-operated cases with large and moderate sized AVMs remain in a good clinical condition. The remainder of the cases develop within the following 10 to 15 years after diagnosis a progressive clinical deterioration characterized either by repeated hemorrhages or a progressive mental and neurological symptomatology ultimately leading to irreversible invalidism or even death. A precise analysis of these cases will be provided in Vol. III B.

b) Differences in retrospective studies are mainly caused by analyzing collected cases using different criteria applied to unoperated and operated cases. The statistics may give satisfactory information concerning age, sex, symptoms of the patient and size and site of the lesion, but they cannot necessarily provide a guide to treatment, as an “inoperable” lesion for some neurosurgeons, is deemed operable by others. It is remarkable that in some series 30–50% of AVMs are still deemed inoperable.

c) Authors with conservative attitudes may argue that the operated cases are “easy” lesions whereas the unoperated patient would be regarded as having more high risk characters (size, site etc.). This argument is only partially correct. Many operated cases are not elective “easy” lesions, but occur as emergency cases because of hemorrhage or progressive neurological and mental deficits. Some patients with “easy” operable lesions refuse surgery as they will not accept any operative risk. Some informed patients prefer to gamble on an early favourable clinical course in order to await further technological advances (Drake 1979).

d) Some patients accept surgical risk only after deterioration of their symptoms. Such cases which have been conservatively treated are, however, most often not included in the statistics of unoperated cases, but rather in those of operated cases. Without this recourse to surgery the statistical outlook of unoperated cases might be less favourable. Intracerebral hemorrhage is the most serious complication. Its frequency varies from about 40% to 68% in most series (Pia 1975) with those cases presenting initially with hemorrhage being at greater risk (Crawford et al. 1986).

e) As a result of discussion between neurologists, neuropathologists and particularly neurosurgeons, technical developments within the last 30 years (microsurgery, modern neuroanesthesia, high energy radiation, selective embolization) have offered new approaches in treatment. In many publications with large series of operated cases there is no clear separation of statistical data, as to which cases have been operated using conventional surgical technique, pure microsurgical techniques or using combined techniques such as embolization and microsurgery or surgery and radiation. These data are more clearly given in publications of smaller series, especially those concerning the surgery of “deep seated AVMs”.

f) Other variables have rarely been considered. It is necessary to indicate not just the size of an AVM, in cm² or cm³, but also its precise construction (single or multiple niduses and compartments, single or multiple AVMs, plexiform, fistulous or diffuse) and its relation to the venous system (Dobbelaere et al. 1979, Vinuela et al. 1985). The precise location should be given not just as frontal, parietal, temporal etc., but as a location within a lobe (polar, dorsal, ventral, lateral, medial, superficial or sulcal etc.).

g) Statistics concerning the surgical mortality and morbidity are rarely discussed in detail. Generally, the operative mortality in the collected literature is 11.0% (among this number are large – giant AVMs, deep seated AVMs, patients in condition IV-V, some with large hematomas). The statement that the mortality is 5–6% in good risk cases and 20–30% in poor risk cases is helpful but not sufficient to obtain a proper indication as to individual operability.

Useful information has been provided in the series of 81 patients of Haerer (1982) (Tables 1.6 and 1.7).

h) The simultaneous development of three new techniques, microsurgery, embolization and radiation, over the past 20 years has provided, to some extent, healthy competition, yet it has also been exasperating. The success of stereotactic gamma-radiation in the treatment of small to moderate sized AVMs (up to 3 cm in diameter) was and is a factor which reduces just that number of surgically suitable cases for the teaching of young neurosurgeons. In cases of large to giant AVMs, selective embolization and proton beam application are attempts at treatment in otherwise hopeless situations. The results have not as yet been convincing.

The information gained from CT, MRI and selective angiography concerning size, site, shape, precise construction and composition of an AVM, and the studies with Doppler sonography, PET etc. (see Chapter 4: Hemodynamics) still does not allow us to make any prognostic conclusion about the behavior of the AVM with regard to hemorrhage, ischemia, and growth. Statistical studies showing that AVMs are more benign lesions than aneurysms (Crawford et al. 1986) are unsatisfactory. For a given single patient, nobody can readily predict what is going to happen. The exact risk that these lesions present is far from clear (Symon 1976). It remains a ‘perplexing disease’ (Fults and Kelly 1984).

Over the past 30 years the number of publications on cerebral AVM and the number of operated cases have increased enormously:

Anderson and Korbin 1958, Höök and Johanson 1958, Tönnis et al. 1958 (134 cases), Guillaume et al. 1959, Paillas et al. 1959 (70 cases), (80 cases), Poppen 1960, Krenchel 1961 (98 cases), Margolis et al. 1961, Dott and MacCabe 1963, Frugoni and Ruberti 1963 (54 cases), Houdart and Le Besnerais 1963 (44 cases, 3), Sano 1964, Kunc 1965, 1974, 1975, 1977, Pool and Potts 1965 (523 collected cases), Sharkey 1965, Svien and McRae 1965 (95 cases), Perret and Nishioka 1966 (545 collected cases), Pool 1965, 1968, Schatz and Botterell 1966, Walter and Bischof 1966 (72 cases), Henderson and Gomez 1967, Houdart 1967, Carrea and Girado 1968, Castaigne et al. 1968 (53 cases), Kempe 1968, Kunicki 1968, Pertuiset 1968, Verbiest 1968, Weir et al. 1968, French and Chou 1969, Salibi 1969, Vianello 1969, Bartal and Yahel 1970 (43 cases, 37 operated), Maspes and Marini 1970, Milhorat 1970, Müller et al. 1970 (99 cases), Troupp et al. 1970, 1977 (137 cases), Montaut et al. 1971, Perria et al. 1971, Raskind 1971, Amacher et al. 1972 (55 cases), Bushe et al. 1972 (42 cases, 10 operated), Forster et al. 1972 (150 cases between 1930–1960), Green and Vaughan 1972, Krayenbühl and Yaşargil 1972 (523 cases, 303 operated; 187 extirpated), Pia 1972, Amacher and Shillito 1973, French and Seljeskog 1973, Morello and Borghi 1973 (154 cases, 102 operated), Peserino and Frugoni 1973 (91 cases), Waltimo 1973 (43 cases), Boldrey and Pevehouse 1975, Bushe et al. 1975 (56 cases, 46 operated), Chou et al. 1975, Pia 1975 (124 cases), Sano et al. 1975 (205 cases, 165 operated), Pertuiset et al. 1976, Towfighi et al. 1976, Yaşargil et al. 1976, French 1977, Luessenhop and Gennarelli 1977 (300 cases, 49 operated), Filatov et al. 1978 (588 diagnosed, 276 operated, 160 radical removal, 60 endovascular occlusion, 56 palliative procedures), Juhasz 1978, Kosary et al. 1978 (12 cases), Mingrino 1978 (196 cases, 98 operated), Patterson and Voorhies 1978 (50 cases), So 1978, Vigouroux et al. 1978, Andreussi et al. 1979, Dobbelaere et al. (Laine) 1979 (370 cases), Drake 1979 (166 cases, 140 radically operated), Pellettieri et al. (Norlen) 1979 (166 cases, 119 operated), Pertuiset et al. 1979 (162 cases), Sundt 1979 (38 cerebral cases, I†), Wilson et al. 1979 (183 cases, 65 radically operated), Da Pian et al. 1980, Guidetti and Delitala 1980 (145 cases, 95 operated, 92 radically, 50 conservatively), Laine et al. 1980, 1981 (500 cases), Parkinson and Bachers 1980 (100 cases, 90 operated, 10†), Viale et al. 1980, Gerosa et al. 1981, Pertuiset et al. 1981, Aimard 1982 (100 cases), Albert 1982 (178 cases, 140 operated), Debrun et al. 1982 (46 cases, acrylate), Heros 1982, Malis 1982, Martin and Wilson 1982 (116 cases, 16 occl. operated), Patterson 1982, Smith et al. 1982, Suzuki 1982, Graf et al. 1983 (191 cases between 1976–80), Hassler et al. 1983 (35 cases), Ojemann and Crowell 1983, Yonekawa et al. 1983, Black and Farhat 1984, Fujita and Matsumoto 1984, Fults and Kelly 1984 (131 cases, 48 operated between 1979–82), Grisoli et al. 1984, Martin et al. 1984, Rutka and Tucker 1984, Wilson and Stein 1984 (180 cases, 175 radically, 5 subtotally operated, 2†), Adelt et al. 1985 (43 cases), Aoki and Mizutani 1985, Bonnal 1985, Davis and Symon 1985 (129 cases, 69 operated between 1948–1980, 1†), Jomin et al. 1985 (128 cases), Salcman et al. 1985, Samson and Batjer 1985, 1985, Waga et al. 1985, Crawford et al. 1986, Drake 1986.

Monographs

Comprehensive monographs including history, embryology, anatomy, pathological and clinical considerations, analyses of results in operated and nonoperated patients with intracranial AVMs have been published since 1928 by:

Cushing and Bailey 1928, Dandy 1928, Bergstrand, Olivecrona and Tönnis 1936 (in German), Asenjo and Uiberall 1945 (in Spanish), Olivecrona and Ladenheim 1957 (in English), Ley 1957 (in Spanish), Pool and Potts 1965, Lange-Cosack two separate chapters in Olivecrona and Tönnis: Handbook of Neurosurgery, Vol. IV, 1966, Norlén in Olivecrona and Tönnis: Handbook of Neurosurgery, Vol. IV, 1966, Smith, Haerer and Russel 1982, Ojemann and Crowell 1983, Wilson and Stein 1984, Fein and Flamm 1985.

Summary and Outlook

Five aspects of vascular malformations have always been, and still remain, controversial:

1) Pathogenesis,

2) Nomenclature,

3) Classification,

4) Diagnosis,

5) Treatment.

The first 3 aspects are discussed on pages 49–61.

Diagnosis

A vast increase in the number of angiographic studies performed from 1928 onwards, has given rise to the impression that AVMs of all types have become more frequent in their presentation to the clinician. Once any of these lesions have become symptomatic it is generally felt that it has become a more dangerous lesion to that patient. Whether this is true for all types of vascular malformation is uncertain. There is even an argument as to the frequency of occurrence of the various types of anomaly. Earlier, it was generally considered that venous and cavernous malformations were rare, but McCormick (1985) in his large pathological series found that the opposite was true and that venous malformations were 10 times more common than the arterial or arteriovenous forms. The next most frequent form of malformation was the cavernoma. Improved angiographic techniques (Constans et al. 1968, Wendling et al. 1976, Preissig et al. 1976) and the routine use of CT scanning and radionucleide scanning (Partain et al. 1979, Fierstien et al. 1979) demonstrated the increasingly frequent occurrence of venous malformations. The incidence of cavernous malformations has also apparently increased enormously since the intruduction of the MRI scan. Huang et al. (1984) have further revived the 200 year old dispute regarding nomenclature.

Surgery

In terms of surgical treatment:

a) Decompression (Ray 1941 and others), and extra- or intracranial ligature of carotid arteries are now techniques of the past. Potter’s criticism is valid: “The ligature invited arterial blood from somewhere on the ‘easy term’ of low resistance at the expense of normal brain.”

b) Radical excision is the surgical goal whenever possible, but must minimize damage to the normal parenchyma and function of the brain. Hypotension, temporary occlusion of involved vessels (Gillingham 1953), identification of afferent and efferent vessels with fluorescein angiography (Feindel et al. 1965), intracranial, intraoperative flow measurement (Nornes and Grip 1980), multiple stage operations (Pertuiset and Sichez 1978) and interdisciplinary attack (embolization by neuroradiologist and removal by neurosurgeon, Stein and Wolpert 1980) are recently available useful technical adjuncts. Stereotactic approaches (Guiot et al. 1960, Riechert and Mundinger 1964, Wijnalda and Bosch 1975, Kandel and Peresedov 1977), electrothrombosis (Handa et al. 1977), and cryosurgery (Walder et al. 1970) have not found widespread acceptance. Techniques of hypothermia, circulatory arrest and circulatory bypass and the use of steroids (Edgerton 1983, Nagamine et al. 1983) have all been employed with some success. Yet other techniques such as gamma radiation (Steiner et al. 1972), proton beam therapy (Kjellberg 1978) and selective embolization (Brooks 1930, Luessenhop and Spence 1960, Sano et al. 1965, Djindjian 1970, Doppman et al. 1971, Serbinenko 1974, Hilal et al. 1974, Wolpert and Stein 1975, Debrun et al. 1975, Russell and Berenstein 1981, Merland et al. 1983, and others) have great potential.

If the associated disadvantages of these techniques can be overcome it would be a great dream to eliminate the kidnapper of the normal cerebral circulation in a non-surgical way. It seems probable for the present, that we shall need to develop even more effective surgical techniques to provide results which can then be compared with those of modern radiation. This will only be possible by the application of perfect microsurgery, which necessitates training in the laboratory to gain competence in manipulating brain vessels, in taming and controlling abnormal vessels and thus in effecting complete removal of the malformation.

¹ Diagnosis made at exploration

² Diagnosis made clinically rest: Diagnosis made at autopsy