A concept basically similar to that of Dandy was introduced by Kaplan and Meier (1958). Based on observations made in specimens obtained at autopsy, they concluded that arteriovenous malformations within the cerebral hemisphere represent a perpetuation of a primitive arteriovenous communication, which otherwise would be replaced by an intervening capillary network during the normal embryological development of the cerebral vascular system.
Hamby (1958) approached the problem from a hemodynamic standpoint, concluding that the basic characteristic of arteriovenous malformations is a lack of vascular resistance in the area involved by the lesion. Since the normal cerebral vasculature resistance is provided by the capillary bed, Hamby’s concept is similar to that of Olivecrona and Ladenheim and based on the agenesis of capillaries.
Gold et al. (1964) and Lagos (1977) recognized two types of vascular malformation: 1) a direct end-to-end anastomosis between the arteries and veins of normal structure, representing arteriovenous fistulae and 2) a network of poorly differentiated and immature vessels interposed between the arterial and venous system, representing typical arteriovenous malformations.
Stein and Wolpert (1980) and Warkany et al. (1984) assumed an arrest of normal development of primitive arteries, capillaries and veins, resulted in the formation of direct arteriovenous communications through immature, poorly differentiated vessels, without an intervening capillary bed.
Parkinson and Bachers (1980) maintained that the essential feature of arteriovenous malformations is a shunt responsible for the short-circuiting of the arteriocapillary bed and proposed the descriptive definition of a “congenital arteriovenous fistulous malformation” occurring as a consequence of a local angioblastic error.
Based on Sabin’s (1917) original concept of the development of the primitive vascular plexus, Garretson (1985) recently proposed that AVMs arise from persistent direct connections between the future arterial and venous sides of the primitive vascular plexus, with failure to develop an interposed network.
In summary, most of the theories developed to explain the origin of cerebral vascular malformations have in common the hypothetical concept of total agenesis, or poor development of the capillary network. It is known, however, that normal angiogenesis takes place in a capillarofugal direction and that the predisposing factor for the formation of arteries and veins lies within this primordial capillary network. If there is a primary agenesis of the capillary network and therefore of the driving force for the development of arteries and veins, then this territory must be ultimately avascular.
If, however, the theory of primary capillary agenesis is not correct, one must assume a secondary destruction or disappearance of capillaries, in order to explain the absence of a capillary network as the pathogenetic mechanism for vascular malformations. Such a secondary destruction would have to occur through the action of a factor having the capacity to destroy capillary vessels after arteries and veins have been formed from them. In such a situation the arteries and veins would then form direct communications.
A capillary destroying factor has not yet been found. Also, if this theory of secondary destruction of capillaries is correct, one would expect to see only cases with direct arteriovenous fistulae, rather than all the commonly known varieties of AVMs in which coiling convoluted vessels are interposed between arteries and veins.
For this reason it seems appropriate to discuss another hypothesis: There is neither a primary agenesis nor a secondary destruction of capillaries, but a local or regional disease of capillaries. In a given primitive vascular territory, the normal development of capillaries is disturbed, however, these capillaries do not disappear entirely, but proliferate and thereby develop metamorphotic, dysplastic vessels (Luschka 1854, Dandy 1928). This disease may be defined as a ‘proliferative capillaropathy’ of unknown origin (Fig 3.1). It is characterized by maldevelopment of an area of the primordial capillary plexus into metamorphotic vessels. These vessels do not fulfil the histologic criteria of arteries, veins or capillaries. It is, in fact, well known, that it is difficult if not impossible to typify histologically the vessels comprising the core of a vascular malformation. These vessels have been called “unidentifiable type of vessels” by Hamby (1958) (Fig 3.2) and “structural hybrids” by Burger and Vogel (1976).
Fig 3.1A–G Artist’s drawing of the different types of cerebral vascular malformations.
A Arterial malformation.
B Arteriovenous fistulous malformation.
C Arteriovenous plexiform malformation.
D Arteriovenous plexiform micro-malformation.
E Cavernous malformation.
F Capillary malformation (telangiectasia).
G Venous malformation.
Fig 3.2 The unique drawing of Hamby (1958) showing the complex vascular composition of AVM-nidus.
In a histologic study of three cases of arteriovenous malformations, Sorgo (1938) classified the vessels constituting the malformation into three main types, according to the composition of their wall. He also found similarities between the wall of vessels composing arteriovenous malformations and the wall of normal embryonic vessels. Based on his observations he postulated that at least one of the described types of vessels may well arise from capillaries.
The results of recent electron microscopic studies are in accordance with our proposed concept. Meyermann and Yaşargil (1981) found that the ultrastructural composition of small vessels of 41 surgically obtained arteriovenous malformations could be divided into two distinct types; vessels with a closed and vessels with a fenestrated endothelial cell layer. This second type of vessel, characterized by a fenestrated endothelial coat is clearly abnormal, since fenestrations of endothelial cells do not occur in the normal brain vasculature with exception of the area postrema, choroid plexus, pineal and pituitary glands, intercolumnar tubercle, and certain nuclei within the hypothalamus (Lee 1971). Another observation of this study was the sprouting of new capillaries in the fibrotic arachnoid surrounding superficial pathological vessels. This finding supports the concept of a proliferative capillaropathy (Figs 3.3, 3.4).
Depending on the extension and distribution of the capillary disease involving the primitive vascular plexus, vascular malformations may therefore be defined as localized, multiple or diffuse collections of metamorphotic vessels, abnormal in number, in structure and in function.
The result of this primary disease of capillaries is a mal-production and therefore a mal-formation of both arteries (or arterioles) and veins (or venules), i.e. a metamorphotic angiodysplasia or capillaropathy.
Fig 3.3A–B A Sinusoid-type vessels of AVMs are coated by fenestrated endothelial cells. The fenestrae are indicated by arrows. In the normal cerebral vasculature this type of endothelial coat is only present in certain distinct areas of the CNS. The cytoplasm of the endothelial cells is filled with cross-sectioned filaments and some vacuoles. The arrowhead indicates a so called Weibel-Palade body. This organelle can only be found in endothelia, and is a rare feature in a normal cerebral vessel wall. Bar = 1 μm B Although some gaps in the endothelial cell layer of AVM are demonstrated as in A, some cell contacts of adjacent endothelia are tight as seen in normal cerebral vessels. Bar = 1 μm. By courtesy of Dr. R. Meyermann.