“Cryptic” Vascular Malformations of the Central Nervous System

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It is now more than 100 years since the first description of large arteriovenous malformations of the central nervous system and, since that time, they have been described so often that knowledge of their natural history and pathology is relatively complete. Although these lesions are rare, a significant number of large series have been reported,1,3,24,26,29,32,33,35,41,46,47,49,62,65,75,78,81,83,84,89,90,96,101,102,105,107 and a review of the literature reveals more than 1000 well documented cases.

Distinctly less common,

It is now more than 100 years since the first description of large arteriovenous malformations of the central nervous system and, since that time, they have been described so often that knowledge of their natural history and pathology is relatively complete. Although these lesions are rare, a significant number of large series have been reported,1,3,24,26,29,32,33,35,41,46,47,49,62,65,75,78,81,83,84,89,90,96,101,102,105,107 and a review of the literature reveals more than 1000 well documented cases.

Distinctly less common, yet still well documented, are certain syndromes which include vascular malformations of the brain, spinal cord, or meninges as an integral component. Some of these, such as the Sturge-Weber syndrome and the Louis-Bar syndrome, fall outside the scope of this review. A third, recently described and apparently rare syndrome of disseminated hemangiomatosis13 will be included in this discussion of small vascular hamartomas of the central nervous system. The Rendu-Osler-Weber syndrome, although at times associated with telangiectasis in the central nervous system, will not be considered in detail.17,70,89 The Sturge-Weber syndrome is excluded from this study.37,87 True vascular neoplasms, the hemangioblastomas, are also excluded from detailed consideration, but will be briefly discussed in relation to cerebellar and spinal cord malformations.55,71,72,85,89,94

Margolis et al. first called attention to a group of small vascular malformations when they reported four cases in which this type of lesion caused intracerebral hemorrhage.64 Russell, in reporting her observations in relation to various causes of intracranial hemorrhage, popularized the descriptive term “cryptic” for these small A–V malformations,88 namely those which are clinically silent and which measure less than 2–3 cm. in maximum size. She found 21 such malformations that caused hemorrhage.

There have been many single case reports and small series.1,2,4–6,8–18,21–23,25–28,30,31,34,36,39–42,43,45,48–51,57,59,61,63–66,70,71,73–77,79–80,82,91–93,97,98,101,103,104,107 We have studied 48 “cryptic” vascular malformations. Only four other series of comparable size have been published.19,20,52,54,106 This report of our cases includes a comprehensive review of all the cases in the references cited above.

Reviews of the many varied classifications of vascular malformation of the nervous system have been made by Noran,75 Raynor and Kingman,85 Russell and Rubinstein,89 and by Olivecrona and Ladenheim.78 This aspect will not be discussed in detail here, but has been examined in detail elsewhere.67 The terms telangiectasis, varix, cavernous angioma, venous angioma, and arteriovenous malformations are regarded as comprehensive enough to include the various types of “cryptic” malformations that we, as well as others, have encountered. The term “angiomatous meningioma” used by Noran75 is, in our opinion, a misnomer. This lesion is not a meningioma, but rather a vascular malformation which is confined to the leptomeninges.

Nature of 48 Cases in Our Series

Brains obtained from the autopsy services of the University of Tennessee and the University of Iowa were studied. The 48 specimens were obtained during the period 1953–1964. There were gross photographs in 32 of the cases, and all had microscopic sections. All malformations measured less than 3 cm. in maximal dimension.

The age of our 48 patients ranged from stillborn to 87 years. There were only 5 patients less than 21 years of age. The average age was 49 years. There were 31 females and 27 males.

Ten of the 48 patients had massive, fatal hemorrhages because of the malformations. Two others had minor hemorrhage associated with the malformations. The age of these patients with hemorrhages varied from 8 to 80 years; the average age was 38.6 years. Three were less than 21 years of age (8, 10, and 13 years). Six of the 10 malformations in which there was massive bleeding were located in the posterior fossa, 5 were in the cerebellum and 1 was in the pons.

The majority of the malformations were composed of admixtures of normal and abnormal arteries and veins, and were the usual type of arteriovenous malformation (Figs. 1, 2, and 3). The single vascular malformation found in the spinal cord most closely resembled a minute cavernous angioma. Twelve of the 48 malformations were of the type commonly classified as telangiectasia (Fig. 4); 8 of these were found in the pons. One malformation was confined to the tectum of the mesencephalon, but did not cause aqueductal stenosis. The exact location in the remaining 4 cases is not known. These 4, all occurring in the first years of the study, were described as left or right cerebral only.

Fig. 1.
Fig. 1.

A: Typical “cryptic” vascular malformation (venous angioma) in the convolutional white matter of the left middle frontal gyrus. There has been no hemorrhage from this 5 mm. lesion. B: Close-up of the 5 mm. malformation showing its irregular borders. ×3. C: Photomicrograph of the vascular malformation. This type represents the so-called venous angiomas. H. & E. ×100

Fig. 2.
Fig. 2.

Photomicrograph of “cryptic” vascular malformation from parietal lobe. The appearance of this type of malformation is essentially the same as the typical giant “bag-of-worms” arteriovenous malformation, and differs only in its much smaller size. This lesion measured 2.8×2.0×1.8 cm. H. & E. ×4.

Fig. 3.
Fig. 3.

A: Arteriovenous malformation of pons with fatal hemorrhage. B: Photomacrograph of pons demonstrating a portion of the A–V malformation, which is located in the tegmentum at this level. H.&E.×2½. C: Photomicrograph of A–V malformation in pontine tegmentum. H. & E. ×100.

Fig. 4.
Fig. 4.

Typical telangiectatic type of vascular malformation in striate portion of pons. These are the most common vascular malformation found in the pons at autopsy. H. & E. ×50.

The size of the malformations varied from 1 mm. to 2.8 cm. (Figs. 5678 A8 B9).

Fig. 5.
Fig. 5.

“Cryptic” vascular malformation (venous angioma) in cortex and convolutional white matter of frontal lobe. This lesion was thought grossly to be a petechia. H. & E. ×8.

Fig. 6.
Fig. 6.

Typical “cryptic” cavernous angioma in cerebellar folium. This lesion measured 2 mm. in diameter. H. & E. ×10.

Fig. 7.
Fig. 7.

“Cryptic” vascular malformations in left basal ganglia. No malformation could be found in or near the fatal hemorrhage on the right.

Fig. 8 A.
Fig. 8 A.

Large intraparenchymal hemorrhage in typical area for “hypertensive” hemorrhage. The cause of this hemorrhage was a “cryptic” arteriovenous malformation.

Fig. 8 B.
Fig. 8 B.

Malformation in edge of hemorrhage pictured above. The anomalous vessels making up this malformation do not form as compact a malformation as those previously illustrated. H. & E. ×60.

Fig. 9.
Fig. 9.

Typical “cryptic” cavernous vascular malformation in the cervical spinal cord demonstrating compact, thin-walled vessels. This malformation measured 1 mm. H. & E. ×30.

Discussion

The true incidence of “cryptic” vascular malformations is unknown. The number of large classical vascular malformations is commonly compared to that for saccular aneurysms or brain tumors. Evans and Courville33 found 62 saccular aneurysms and 22 A–V malformations. Falconer,35 Walker,105 and Russell88 found that the ratio of aneurysms to A–V malformations was 100:12, 201:84, and 92:21, respectively. In our material68 the ratio was 229:53. In these 5 series there were 684 berry aneurysms and 192 A–V malformations of all sizes. A number of cases with concurrence of aneurysms and vascular malformations have also been reported.11,40,81 The other “index” of frequency, that is, a ratio between the frequency of A–V malformations and brain tumors,78,89 is unsatisfactory.

Relation to hemangioblastomas

Many papers published since the monograph of Cushing and Bailey24 have discussed the vascular malformations of the central nervous system (C.N.S.) together with the hemangioblastomas. Some of the earlier papers on these lesions have been summarized by Noran,75 while Stein et al.,94 Morello and Bianchi,71 and Raynor and Kingman85 have recently reviewed the current concepts of the hemangioblastomas. Most authors would now agree that the hemangioblastomas are true neoplasms, and thus differ from the vascular malformations, which are non-neoplastic, developmental abnormalities. The case reported by Raynor and Kingman85 of the juxtapositional co-existence of a hemangioblastoma and a vascular malformation in the cerebellum of a young man is of interest, for it again brings before us the problem of etiology and pathogenesis of these 2 disorders. While it appears unlikely that the A–V malformation in their patient was merely greatly dilated vessels feeding and draining the hemangioblastoma, the phenomenon has been known to exist,55 and that possibility remains. Another apparently unique case is that of a possible intrapontine “hemangioblastoma” reported by Myers et al.72 None of the “cryptic” vascular malformations in our series bore close resemblance to hemangioblastomas, and none of the patients had stigmata of the von Hippel-Lindau syndrome. There were only 3 patients with hemangioblastomas, all cerebellar, found at autopsy during the period covered by this study.

Relation to large malformation

Another important aspect of “cryptic” vascular malformations is a consideration of their frequency relative to that of the large classic forms. The literature is of little help. In our series the ratio of “cryptic” to classic malformations was 48:5. The majority of the large series deal only with the classic forms, but a few comparative figures can be found. Evans and Courville33 had at least 3 cases in which there were “cryptic” malformations; 1 of these consisted of multiple lesions. Wolf and Brock,107 in their series of 9 malformations, had 4 cases of this type. Other authors, such as Mackenzie,62 and Paterson and McKissock81 classified the malformations into “large” and “small.” Seven of the 50 malformations studied by Mackenzie were classified “small,” whereas 39 of the 110 malformations reported by Paterson and McKissock were regarded as “small.” Unfortunately, in neither of these reports were the terms “large” and “small” adequately defined. Papatheodorou et al.79 found 8 cases of “cryptic” malformations in a series of 30 arteriovenous malformations. It seems likely that the great disparity between our series and those in the literature can be explained by the fact that the majority of the reported cases were found in surgical patients whose lesions were manifest clinically. In general, only those “cryptic” malformations in which there was bleeding have been reported, a fact that has been stressed by Anderson and Korbin.1

Supratentorial vs. infratentorial location

It is clear that a striking majority of large A–V malformations are supratentorial.1,24,26,31,33,35,38,46,47,53,58,60,62,65,75,78,80,81,83,85,89,90,95,96,101,102,105,107 Among the more than 500 A–V malformations reported in 7 series,46,62,78,81,101,102,105 only about 50 were in infratentorial locations. This contrasts sharply with the location of the “cryptic” vascular malformations, where the distribution between supra- and infratentorial sites was almost equal (Figs. 10 and 11). By combining our “cryptic” malformation cases with those in the literature, 44 were found in the cerebellum, 85 in the brain stem, 18 in the spinal cord, and 161 above the tentorium cerebelli.

Fig. 10.
Fig. 10.

Chart indicating location of the 48 “cryptic” vascular malformations observed in this study.

Fig. 11.
Fig. 11.

Chart illustrating the location of 308 “cryptic” vascular malformations; 260 in the literature and 48 in this series.

Epilepsy, commonly found in the classic supratentorial A–V malformations,31,36,39,80 was not present in our 48 patients. It has, however, been reported in a number of cases with temporal lobe “cryptic” malformations.

Relation to spontaneous cerebellar hemorrhage

The relationship between “cryptic” malformations and spontaneous cerebellar hemorrhage is of particular interest. McKissock et al.69 found angiomas to be the cause of 6 to 34 spontaneous cerebellar hemorrhages. Four additional cerebellar hemorrhages due to “cryptic” angiomas were reported by Odom et al.,76 while Thrash100 recorded 3 more examples. In our own material, there were 13 “cryptic” malformations confined to the cerebellum, 5 of which had bled. Of 21 “spontaneous” cerebellar hemorrhages studied by us during the period 1953–64, 24 per cent were due to proven vascular malformations. Rey-Bellet, however, could not demonstrate vascular malformations in any of his 21 cases of cerebellar hemorrhage.86 The hemorrhage was described as “very extensive” in 14 of his cases, and a small malformation could easily have been largely or completely destroyed and escaped detection.

Incidence in spinal cord

Vascular malformations of the spinal cord are being reported with increasing frequency.2,3,9,12,29,32,41,42,44,49,51,56,73,77,89,99 The majority are large3,9,32,41,44,49,73,99 but a number of “cryptic” malformations have been reported2,9,12,29,42,51,77,89 (Fig. 11). One of our “cryptic” malformations occurred in the spinal cord. The apparent low incidence of small vascular malformations of the cord in autopsy studies is probably due more to the infrequency of adequate examination of the spinal cord than to true rarity.

“Spontaneous” cerebral hemorrhage

The small size of the “cryptic” vascular malformation, together with their relative frequency, makes them a likely cause for some of the spontaneous hemorrhages usually ascribed to hypertension.64,66,69,70,76,77,79,88,100 While cerebral hemorrhage is less frequent than cerebellar, many proven examples are available.52,54,63,64,76,88,89 Margolis and his colleagues63,64 have emphasized that the small size of the malformation, and its frequent partial destruction by hemorrhage, makes clear recognition difficult. In several of our patients we had to make many sections from the walls of the hemorrhage before finding the causative malformation (Fig. 7). The massive size of many “typical” lenticulostriate hemorrhages may obscure, or even totally destroy, “cryptic” vascular malformations. No one knows exactly what percentage of cerebral hemorrhages are actually due to “cryptic” vascular malformations, but we believe that the relationship is significant.

Relation to pontine hemorrhage

This same argument, and belief on our part, holds for the so-called “primary” pontine hemorrhages. “Cryptic” malformations are known to be common in the pons (Figs. 10 and 11) and numerous examples of fatal pontine hemorrhage due to such malformations have been reported8,13,16,45,48,57,59,70,98 (Fig. 3).

Comparison with major series

In 1954, Russell88 reported 21 patients (including 11 children) with “cryptic” vascular malformations, 20 of which were solitary and all of which had bled.

In her book,89 Russell mentions 6 telangiectases located in the pons and 1 in the spinal cord. Courville19,20 reported 22 patients with “cryptic” malformations, 21 of which were solitary and only 1 of which had bled. There were 19 supratentorial malformations and 3 cerebellar.

Jensen et al.52 reported 21 patients with “minute” vascular malformations diagnosed by angiography. The tissues from only 11 of these malformations were examined. All of their cases were supratentorial, and all were apparently associated with hemorrhage.

White et al.106 reported 48 cases of “cryptic” malformations found incidentally at autopsy. The pons was the most common site (17 patients). The cerebellum was involved in 5 patients. Ninety per cent of the patients in this series were 40 years of age or older.

Papatheodorou et al.79 described 8 “cryptic” malformations, all of which bled and were supratentorial and identified by angiography. The age of their patients was 5 to 42 years, with 3 less than 20 years.

Krayenbühl and Siebenmann54 were able to demonstrate 15 malformations in 24 patients, all 24 of whom bled and were considered to have small vascular malformations. All of their malformations were supratentorial. The age range in the 15 patients with proven malformations was 8 to 54 years, with 5 patients less than 20 years of age.

Thus, these 6 series yielded 91 patients with proven “cryptic” malformations, 65 of whom had suffered hemorrhage from their malformations. The relative youth of the patients was stressed by most authors.

Our own material reveals a much lower incidence of spontaneous hemorrhage. This almost certainly reflects the different methods by which the material was collected. Our cases, as were those of Courville and of White et al., come from autopsy material, whereas the other reported cases were from clinical services. The fact that those of our patients who had bled were younger than those in whom no bleeding had occurred, was in agreement with the findings of others.52,54,79,88

Summary

This review indicates increasing recognition of small, usually clinically silent, “cryptic” vascular malformations in the C.N.S. Although they are not reported as frequently as the large, classical arterio-venous malformations, they are much more common.

We have reported and analyzed our series of 48 cases. We have discussed the frequency with which these malformations bleed and have drawn particular attention to the relative frequency of cerebellar hemorrhages.

We have suggested that “cryptic” vascular malformations may be responsible for a significant percentage of so-called hypertensive hemorrhages.

We have assembled a comprehensive review of comparable or related cases reported in the English language, and have emphasized characteristic features.

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Presented in part at meeting of the Tennessee State Pathology Society, Memphis, Tennessee, April 9, 1962, and at meeting of the Iowa Association of Pathologists. Iowa City, Iowa, December 12, 1964.

Article Information

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    A: Typical “cryptic” vascular malformation (venous angioma) in the convolutional white matter of the left middle frontal gyrus. There has been no hemorrhage from this 5 mm. lesion. B: Close-up of the 5 mm. malformation showing its irregular borders. ×3. C: Photomicrograph of the vascular malformation. This type represents the so-called venous angiomas. H. & E. ×100

  • View in gallery

    Photomicrograph of “cryptic” vascular malformation from parietal lobe. The appearance of this type of malformation is essentially the same as the typical giant “bag-of-worms” arteriovenous malformation, and differs only in its much smaller size. This lesion measured 2.8×2.0×1.8 cm. H. & E. ×4.

  • View in gallery

    A: Arteriovenous malformation of pons with fatal hemorrhage. B: Photomacrograph of pons demonstrating a portion of the A–V malformation, which is located in the tegmentum at this level. H.&E.×2½. C: Photomicrograph of A–V malformation in pontine tegmentum. H. & E. ×100.

  • View in gallery

    Typical telangiectatic type of vascular malformation in striate portion of pons. These are the most common vascular malformation found in the pons at autopsy. H. & E. ×50.

  • View in gallery

    “Cryptic” vascular malformation (venous angioma) in cortex and convolutional white matter of frontal lobe. This lesion was thought grossly to be a petechia. H. & E. ×8.

  • View in gallery

    Typical “cryptic” cavernous angioma in cerebellar folium. This lesion measured 2 mm. in diameter. H. & E. ×10.

  • View in gallery

    “Cryptic” vascular malformations in left basal ganglia. No malformation could be found in or near the fatal hemorrhage on the right.

  • View in gallery

    Large intraparenchymal hemorrhage in typical area for “hypertensive” hemorrhage. The cause of this hemorrhage was a “cryptic” arteriovenous malformation.

  • View in gallery

    Malformation in edge of hemorrhage pictured above. The anomalous vessels making up this malformation do not form as compact a malformation as those previously illustrated. H. & E. ×60.

  • View in gallery

    Typical “cryptic” cavernous vascular malformation in the cervical spinal cord demonstrating compact, thin-walled vessels. This malformation measured 1 mm. H. & E. ×30.

  • View in gallery

    Chart indicating location of the 48 “cryptic” vascular malformations observed in this study.

  • View in gallery

    Chart illustrating the location of 308 “cryptic” vascular malformations; 260 in the literature and 48 in this series.

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