-Acta Iqurochirurgica
Acta Neurochir (Wien) (1992): 116:119 - 127
9 Springer-Verlag 1992 Printed in Austria
Arteriovenous Malformations of the Posterior Fossa* B. George, M. Celis-Lopez, T. Kato, and G. Lot Department of Neurosurgery, H6pital Lariboisi~re, Paris, France
Summary AVMs of the posterior fossa are reviewed on the basis of personal experience of 47 cases including 2 venous angiomas, 7 cavernous angiomas, 5 arteriovenous fistulas and 33 true arteriovenous malformations and of the few series reported in the literature. MRI is now an indispensable tool to define the exact localization of any malformation. Combined with angiography, it permits one to choose the most adequate therapeutic strategy and the best surgical approach. Radical cure is to be contemplated in most cases considering the often dramatic consequences of bleeding at the infratentorial level. Deep AVMs and moreover cavernous angiomas, even those located in highly functional structures such as the brain stem, can now be discussed for treatment. Encouraging results have already been obtained using, alone or in association, the recently advanced modalities of treatment: interventional neuroradiology, radiosurgery, and microsurgery. Keywords: Arteriovenous malformation; cavernous angioma; MRI; surgery.
T h o u g h all types o f A V M c a n be o b s e r v e d at the i n f r a t e n t o r i a l level, r e p o r t s o n a r t e r i o v e n o u s m a l f o r m a t i o n s ( A V M ) o f the p o s t e r i o r fossa are n o t n u m e r o u s 1, 7, 8, 19, 26, 31, 41. This is m a i n l y because they are u n c o m m o n lesions a n d thus surgical experience is generally limited.
Frequency A V M o f the p o s t e r i o r fossa includes true A V M , a r t e r i o v e n o u s fistula, c a v e r n o u s a n g i o m a , telengiectasis a n d the so-called venous a n g i o m a . Tables 1 a n d 2 indicate their respective frequencies at the s u p r a a n d i n f r a t e n t o r i a l level in o u r d e p a r t m e n t over the last 5 years a n d f r o m the w o r k o f M c C o r m i c k 2~ on a u t o p s y studies. Telengiectasis is the o n l y t y p e t h a t p r e d o m i -
* Invited Lecture, presented at the European Congress of Neurosurgery, Moscow, June 23-29, 1991
Table 1. Distribution of A VMs (Lariboisi~re series)
MAV CA FAV VA
Supratentorial
Infratentorial
171 7 5 2
33 36 53 13
Table2. Distribution ofAVMs (Mc Cormiek' series 1968)
MAV T CA VA
Supratentorial
Infratentorial
217 22 59 46
70 38 21 31
63% 7% 17% 13%
43% 24% 13% 19%
nates in the p o s t e r i o r fossa; for the others, d i s t r i b u t i o n at the infra a n d s u p r a t e n t o r i a l level is very similar.
Venous Angioma (VA) V A is the m o s t frequent v a s c u l a r m a l f o r m a t i o n f o u n d at a u t o p s y (2.6%) as it is less c o m m o n l y associated with bleeding. I n the p o s t e r i o r fossa, it is m a i n l y l o c a t e d in the d e p t h o f the cerebellum. C e r e b e l l a r localization a c c o u n t s for 2 5 % o f all V A s b u t represents 50% o f all V A s a s s o c i a t e d with h a e m a t o m a 22' 29, 32 Therefore, it m i g h t be c o n c l u d e d t h a t p o s t e r i o r fossa V A s s h o u l d be r e m o v e d in m o s t cases. H o w e v e r , a new c o n c e p t is t h a t this m a l f o r m a t i o n is in fact a n a b n o r m a l v e n o u s n e t w o r k which d e v e l o p e d to c o m p e n s a t e for the lack o f i m p o r t a n t n o r m a l d r a i n i n g veins 32' 35; SO its s u p p r e s s i o n can lead to severe consequences related to v e n o u s h y p e r t e n s i o n a n d infarction. M o r e o v e r , it has been s h o w n t h a t in some cases, the bleeding is in fact
120
B. George et at.: Arteriovenous Malformations of the Posterior Fossa
due to another associated malformation, especially a cavernous angioma 35' 47
Telangieetasis (T) T are small true capillary malformations. They generally cannot be identified by any current imaging tool. They can be the cause of some unexplained haematomas and particularly in the pons which is its c o m m o n site. However, from autopsy studies, T are mostly incidental: only one out of 38 cases had bled in Mc Cormick's report 2~ Table 3. Distribution
of CAs
Supratentorial Infratentorial
%
Mc Cormick et al. Simard et al. Robinson et al. Voigt and Ya~argil Lariboisi+re
58 109 58 126 43
21 18 13 38 7
26 14 18 23 14
Total
394
97
20
Table 4. Localization
o f C A in the Posterior Fossa
Cerebellum
Brain stem
Pons
Mc Corrnick et al. 2~ Simard et al. 34 Robinson et al. 28 Lariboisi6re
11 5 5
9 13 8
7 9
3
4
2
Total
24
34
18
Cavernous Angioma (CA) CAs of the posterior fossa account for about 25% of all cavernomas. Sex and mean age of discovery are similar at both supra and infratentorial levels. Localization in the posterior fossa is mainly in the brain stem and especially the pons 28' 34, 42, 44 (Tables 3 and 4). CAs are generally discovered after one or more bleeds which produce more or less dramatic neurological symptoms and signs. Since it is quite common that CA is associated with repeated minor bleeds, the clinical presentation may be a progressive worsening suggesting a tumour or a fluctuating deficit suggesting a demyelinating disease (multiple sclerosis). However, the density of highly functional structures in the brain stem explains that even minor leaks may lead to very significant and incapacitating deficits or even to death. So though the natural history of CA is not known 24, radical removal of posterior fossa lesions must be contemplated in each case. Since arterial feeders of cavernoma are very small, there is no possibility for endovascular treatment, The slow flow inside a CA led one to think that radiosurgery could be effective by inducing thrombosis. In fact, recently reported experience 43 of this treatment in 6 brain stem CAs has proven to be useless in all cases and even noxious in 3 cases due to radiation induced injury; in comparison, the same team treated surgically 7 similar cases with 6 good results and one with disability. Surgery is therefore the only adequate modality of treatment. M R I now provides not only the diagnosis with much certainty but also a precise anatomical locali-
Fig. 1. Pre (left) and post-operative (right) MRI of a brain stem cavernoma discovered after Needing
B. George etal.: Arteriovenous Malformations of the Posterior Fossa
zation. This permits one to choose the most direct and the least harmful route to reach the lesion. CA in the cerebellum, whatever the depth, can be reached and removed with almost no morbidity. Many cases of successful removal in the brain stem 16' 46, 47 have been reported. The main point is to define which part of the cavernoma is the closest to the floor of the fourth ventricle or to the lateral aspect of the brain stem. Each time, a CA reaches the surface or is covered by a thin lamina of brain stem tissue, resection can reasonably be attempted (Fig. 1). Dissection into the brain stem is generally facilitated by the surrounding gliotic and haemorrhagic tissue; however, in some places, the CA is directly in contact and even sometimes adherent to the normal parenchyma because of old haemorrhagic scars. These adhesions can make the dissection very difficult and hazardous.
Arteriovenous Fistula (AVF) Dural AVFs of the posterior fossa are very uncommon. AVFs of the lateral sinus almost always drain into the veins of the cerebral hemisphere. However, a pouch on the cerebellar veins may be the cause of bleeding in some cases as we observed in 5 patients including 2 at the foramen magnum, 2 on the transverse sinus and one on the tentorium close to the straight sinus (Fig. 2). Treatment is first endovascular but may be surgical in case of failure of intravascular occlusion.
121
AVF of the brain tissue is another but still more exceptional possibility. It may be either alone as in the case reported by Mount 21 and fed by the anterior inferior cerebellar artery or associated with a true nidus of an AVM as we observed in 1 of our cases of posterior fossa AVMs. Endovascular techniques are also the treatment of choice in those fistulas.
Arteriovenous Malformation (AVM) Posterior fossa AVMs account for about 15% of all cerebral AVMs. The brain stem is involved in 25%, the cerebello-pontine angle in 5%; the most frequent localization is in the cerebellum (70% of the cases) where AVMs are mainly found in the vermis, the AVM being developed either partly or totally in it 1' 7, 8, 19, 20, 31, 41. The two third of our 24 cases had this vermian localization (Tables 5 and 6). Bleeding is the almost exclusive circumstance of discovery (Table 7) and in more than half of the cases, Table 5. Distribution of A VMs Supratentoriai Infratentorial % Autopsy series2~ 217 Clinical series3' 6, 8, 10, 11, 19. 26, 31 1807 Lariboisitre series Total
70 206
24 10
171
33
16
2195
309
12
Fig. 2. Dural AVF of the tentorium draining into the straight sinus, fed by the occipital artery and the tentorial branch of the internal carotid artery and responsible for a cerebellar haematoma
122
B. George et al.: ArteriovenousMalformationsof the Posterior Fossa
Table6. Localization of A VMs
Autopsy series~~ Clinical series8,19,z6,~1,41 Lariboisibre series
Cerebellum Brainstem
CPA
52 111 25
12 3
15 34 5
CPA: Cerebello-pontineangle Table 7. Occurrence of Haemorrhage in A V M
Autopsy series2~ Clinical series8' 19.26.31,41 Lariboisi~re series
Haemorrhage
Total
%
42 128 27
67 149 33
63 86 82
with several previous occurrences of haemorrhage. Other modes of discovery are much less frequent: progressive neurological deficit, intracranial hypertension or hydrocephalus. Bleeding from posterior fossa AVMs may have severe consequences; so even if from studies on the natural history 3' 6, H, 12, 13, 37, 40, the rate of rebleeding is likely similar to those located at the supratentorial level, the prevention of new haemorrhages is much more important. For instance, Kondliolka ~3 reported on a 16% overall mortality in their population of AVMs but it was 57% for cases of cerebellar location; Fults and Kelly observed five deaths and one vegetative state due to haemorrhage in a series of 12 cases followed over the course of 7-8 years on averagd ~ Decisions about treatment are based on clinical data, age, general condition, and neurological state and on parameters of the AVM including localization, size, feeders, and drainage. These parameters are best appreciated using a combined analysis of MRI and angiography. M R I is now mandatory for investigating any AVM~5, 17. It gives a nice definition of the anatomical relationship of the AVM with the functional areas including the brain stem, nucleus dentatus, and brachium pontis. In many cases, specially those located in the antero-superior part of the vermis, angiography is not able to differentiate those really involving the brain stem from those extending close to it or even compressing it, but remaining in an extrapial plane. On the contrary, MRI can generally demonstrate the integrity or the involvement of the brain stem (Figs. 3 and 4). This very important point has already been underlined
by Drake 7 at a time where MRI was not available and where the true extent of the AVM was discovered at surgery. MRI helps also determine the size of the nidus and often demonstrates very nicely the feeders and the draining veins. Therefore, with the great advantage of having views in the three spatial planes, MRI is an invaluable tool for defining the best surgical approach and the best therapeutic strategy. However, identification of feeders and draining veins still requires angiography. It gives their number and respective importance and can also reveal an associated aneurysm which is found in about 10% of cases on the arterial feeders 2' 4, 7, 20, 39. Questions concerning feeders and drainage are therefore well answered by these two examinations: which cerebellar artery is giving the main supply? Does any perforating branch participate in the AVM supply? What is the main venous drainage? Are the main arterial supply and the main drainage superimposed? What is the distance between the nidus and the functional structures? What is the number of feeders which is in fact closely related to the size of the nidus? Some of the above mentioned questions correspond to the items of the currently proposed classifications33' 36. However, these classifications do not fit very well with the AVMs of the posterior fossa. In fact, especially regarding the surgical problems, feeders and drainage particularities which are not included in these classifications are of great importance in the posterior fossa. Consequently, besides the size and localization, it seems useful to add a classification based on the vascular presentation (Fig. 5). According to this last point, posterior fossa AVMs can be separated into: i) medial AVMs with their main supply from either the posteroinferior cerebellar artery (PICA) or the superior cerebellar artery (SCA) according to the more or less superior extension, and draining medially into the vein of Galen, the straight sinus and the transverse sinus; ii) lateral AVMs fed mainly by the anterior-inferior cerebellar artery (AICA) and draining laterally towards the petrosal vein and the sigmoid sinus; iii) deep AVMs supplied by perforating branches and draining into ependymal and periaxial veins; iv) extensive AVMs combining several of the above types. This classification is obviously related to the AVM localization but gives less importance to the size. Conversely, it stresses the difficulty of how to reach the main feeder. For instance, the control of the SCA in a supero-medial AVM by a posterior approach supposes the surgeon to be able to pass above the nidus
B. George etal.: Arteriovenous Malformations of the Posterior Fossa
A
C
123
B
Fig. 3. MRI definition of AVMs. A) AVM of the eulmen extending up to the quadrigeminal plate but remaining in the extrapial plane of the brain stem. B) AVM of the quadrigeminal plate with intraparenchymal extension (same case as Fig. 5 C). C) Superomedial AVM of the cerebellum. Notice the venous drainage towards the vein of Galen and the straight sinus
and to isolate the S C A f r o m the draining veins. The same c o m m e n t can be m a d e for a cerebello-pontine angle A V M with the A I C A and the petrosal vein. I n those cases, a pre-operative embolization o f these feeders m a y be o f great help.
M e t h o d s o f treatment for posterior fossa A V M s include interventional radiology, radiosurgery, and microsurgery. Embolization can reduce the vascular supply and the nidus size o f an A V M but it can achieve a complete cure only in very few cases 9, 27. So, it must
124
B. George etal.: Arteriovenous Malformations of the Posterior Fossa
Fig. 4. Brain stem AVM with development inside the medulla. Notice the venous drainage on angiography and on MRI
be generally included in a protocol where embolization is associated with surgery or with radiotherapy (Fig. 6). As already mentioned, it is the best treatment in cases of AVF. Embolization can be used to control arterial feeders which would necessitate a different surgical approach to that chosen for AVM resection. For example, a supero-medial AVM fed by the SCA would require a sub-occipital transtentorial or a subtemporal approach to expose and ligate this vessel and a posterior approach to remove the AVM. Intravascular occlusion of the SCA branches permits one to avoid one surgical stage, and embolization of the most anterior part of the nidus facilitates the surgical dissection in an area opposite to the posterior approach. In large and high flow AVMs where a break-through phenomenon might be expected and multistaged surgery is planned, embolization can replace one of the stages; however, no one case of this phenomenon has yet been reported in the literature after the removal of a posterior fossa AVM. Radiosurgery is essentially effective in small volume AVMs. It seems tempting to propose this technique in AVM located close to or in functional areas. However, we are not aware of any experience of treatment of brain stem AVM by this technique; the risk of radiation induced injury which seems to be around 3 %, probably prevents any attempt being made 23. So, radiotherapy
is indicated rather to complete the cure of a large AVM previously reduced by embolization or surgery. In fact, surgery is the best way to obtain a radical cure, the two other forms of treatment being complementary in some cases; pre-operative embolization to help control the vascular supply and radiosurgery to treat a post-operative remnant. Surgical principles for infratentorial AVMs are similar to those for supratentorial ones: a large exposure giving primary access to feeders, microsurgical dissection flush to the nidus, preservation of the main drainage until total control of the nidus has been achieved. Particular attention must be paid to coagulation of all tiny tortuous vessels surrounding the nidus; great care must be taken not to stretch these vessels by compressing the nidus and even by coagulating them so as to avoid their rupture and their retraction inside the parenchyma1,8; control of extent of the resection must be very careful and especially by looking inside the fourth ventricle in vermian and cerebello-pontine angle AVMs, since leaving some AVM behind, may be the source of post-operative haematoma. Post-operative haemorrhage is the main cause of death and disability in Drake's seriesS: 9 out of 66 cases. Haemostasis must be checked carefully and specially if the sitting position is used. Results of treatment in the published series and in
B. George etal.: Arteriovenous Malformations of the Posterior Fossa
125
Fig. 5. A) Medial AVM (superior) fed by the SCA and drained by the vein of Galen. B) Lateral AVM fed by the AICA (with an aneurysm) and drained by the petrosal vein. C) Deep AVM fed by a perforating branch (same case as Fig. 3 B). D) Extensive AVM fed by the three cerebellar arteries (SCA, AICA, and PICA)
ours indicated a rate of death and disability about twice that for the general series of cerebral AVMs; if brain stem angiomas are considered separately, results are far worse 4' s, 7, 18, 25, 30, 35, 38, 45 (Table 8). This is to be placed in parallel with the high rate of morbidity and mortality after posterior fossa A V M bleeding. How-
ever, better understanding of the localization and vascular arrangement of these AVMs with the help of a combined analysis of M R I and angiography should permit improvement of those results by a better definition of the most adequate therapeutic protocol and of the best surgical strategy.
126
B. George et al.: Arteriovenous Malformations of the Posterior Fossa
Fig. 6. Medial AVM (superior) treated by embolization and radiosurgery. Left and center: before embolization; right: after embolization before radiosurgery
Table 8. Results of Surgical Treatment of A VMs Worsened C e r e b e l l u m 8, 19,
31, 41
Literature Lariboisi6re Brain stem4' 5, 7, 18, 25, 30, 35, 38,45 Literature Lariboisi6re Total
Died
N = 87 N = 13
7 1
N = 23 N = 2
-
N = 125
13
7 -
5
2 9
References 1. Batjer H, Sanson D (1986) Arteriovenous malformations of the posterior fossa. Clinical presentation, diagnostic evaluation and surgical treatment. J Neurosurg 64:849-856 2. Batjer H, Suss RA, Samson D (1986) Intracranial arteriovenous malformations associated with aneurysms. Neurosurgery 18: 2935 3. Brown RD, Wiebers DO, Forbes G, O'Fallow WM, Peipgras DG, Marsh WR, Maciunas RJ (1988) The natural history of unruptured intracranial arteriovenous malformations. J Neurosurg 68:352-357 4. Chou SN, Erickson DL, Ortiz-Suarez HJ (1975) Surgical treatment of vascular lesions in the brain stem. J Neurosurg 42: 2331 5. Chyatte D (1989) Vascular malformations on the brain stem. J Neurosurg 70:847-852 6. Crawford PM, West CR, Chadwick DW, Shaw MDM (1986) Arteriovenous malformations of the brain: Natural history in unoperated patients. J Neurol Neurosurg Psychiatry 49:1-10 7. Drake CG (1975) Surgical removal of arteriovenous malformations from the brain stem and cerebello-pontine angle. J Neurosurg 43:661-670 8. Drake CG, Friedman AH, Peerless SJ (1986) Posterior fossa arteriovenous malformations. J Neurosurg 6 4 : t - 1 0
9. Fournier D, Terbrugge KG, Willinsky R, Lasjaunias P, Montanera W (1991) Endovascular treatment of intracerebral arteriovenous malformations: experience in 49 cases. J Neurosurg 75:228-233 10. Fults D, Kelly DL Jr (1984) Natural history of arteriovenous malformations of the brain: a clinical study. Neurosurgery 15: 658-662 11. Graf CJ, Perret GE, Torner JC (1983) Bleeding from cerebra1 arteriovenous malformations as part of their natural history. J Neurosurg 58:331-337 12. Itoyama Y, Uemura S, Ushio Y, Kuratsu J, Nonaka N, Wada H, Sano Y, Fukumura A, Yoshida K, Yano T (1989) Natural course ofunoperated intracranial arteriovenous malformations: study of 50 cases. J Neurosurg 71:805-809 13. Kondliolka D, Humphreys RP, Hoffman HJ, Hendrick EB, Drake JM (1990) Arteriovenous malformations of the brain in children: A 40 year experience with 132 cases. Abstract of papers. J Neurosurg 72: 359A 14. Lasjaunias P, Terbrugge K, Rodesch G, Willinsky R, Burrows P, Pruvost Ph, Piske R (1989) Vraies et fausses 16sions veineuses c~r6brales. Pseudo-angiomes veineux et h~mangiomes caverneux. Neurochirurgie 35:132-139 !5. Leblanc R, Levesque M, Comair Y, Ethier R (1987) Magnetic resonance imaging of cerebral arteriovenous malformations. Neurosurgery 21:15-20 16. Ledoux MS, Aronin PA, Odrezin GT (1991) Surgically treated cavernous angiomas of the brain stem: Report of two cases and review of the literature. Surg Neurol 35:395-399 17. Lee BCP, Herzberg O, Zimmerman RD, Deck MDF (1985) MR Imaging of cerebral vascular malformations. AJNR 6:863-870 18. Martin NA, Stein BM, Wilson CB (1984) Arteriovenous malformations of the posterior fossa. In: Wilson CB, Stein BM (eds) Intracranial arteriovenous malformations. Williams and Wilkins, Baltimore, pp209-221 19. Matsumara H, Makita Y, Someda K, Kondo A (1977) Arteriovenous malformations in the posterior fossa. J Neurosurg 47: 50-56 20. Mc Cormick WF, Hardman JM, Boulter TR (1968) Vascular malformations (angiomas) of the brain with special reference to those occurring in the posterior fossa. J Neurosurg 28:241-251
B. George etal.: Arteriovenous Malformations of the Posterior Fossa 21. Mount LA (1964) Arteriovenous angioma derived from the anterior inferior cerebellar artery. Its diagnosis and treatment. J Neurosurg 612-614 22. Numaguchi Y, Kitamura K, Fukui M, Ikeda J, Hasuo K, Kishikawa T, Okudera T, Uemura K, Matsuura K (1982) Intracranial venous angiomas. Surg Neurol 18:193-202 23. Ogilvy CS (1990) Radiation therapy for arteriovenous malformations: a review. Neurosurgery 26:725-735 24. Otten P, Pizzolato GP, Rilliet B, Berney J (1989) Apropos de 11 cas d'angiomes caverueux (cavernomes) du S.N.C. rep+r~s par l'analyse r&rospective de 24 535 autopsies. Neurochirurgie 35:82-83 25. Patil AA (1980) Surgical excision ofarteriovenous malformation of the cerebellum and brain stem: A case presentation. Acta Neurochir (Wien) 54:117-125 26. Perret G, Nishioka H (1966) Report on the Cooperative Study of intracranial aneurysms and subarachnoid haemorrhage. Section VI. Arteriovenous malformations. An analysis of 545 cases of cerebral arteriovenous malformations and fistulae reported to the Cooperative Study. J Neurosurg 25:467-490 27. Picard L, Moret J0 Lepoire J (1984) Traitement endovasculaire des angiomes art~rio-veineux intra-crrrbraux. J Neuroradiology 11:9-28 28. Robinson JR, Little JR, Awad IA (1990) The natural history of cavernous angiomas. Abstract of papers. J Neurosurg 72: 333A 29. Rothfus WE, Albright AL, Casey KF, Latchaw RE, Roppolo HMN (1984) Cerebellar venous angioma: "Benign entity". AJNR 5:61-66 30. Russo RH, Dicks RE (1977) Arteriovenous malformations of the brain stem in childhood. Surg Neurol 8:167-170 31. Samson D, Batjer H (1985) Arteriovenous malformations of the cerebellar vermis. Neurosurgery 16:341-349 32. Senegor M, Dohrmann GJ, Wollmann RL (1983) Venous angiomas of the posterior fossa should be considered as anomalous venous drainage. Surg Neurol 19:26-32 33. Shi Y, Chen W (1986) A proposed scheme for grading intracranial arteriovenous malformations. J Neurosurg 65:484-489 34. Simard JM, Garcia B, Engochea F, Ballinger WE, Mickle JP, Guisling RG (1986) Cavernous angioma: A review of 126 collected and 12 new clinical cases. Neurosurgery 18:162-172
127 35. Solomon RA, Stein BM (1986) Management of arteriovenous malformations of the brain stem. J Neurosurg 64:857-864 36. Spetzler RF, Martin NA (1986) A proposed grading system for arteriovenous malformations. J Neurosurg 65:476-483 37. Stahl SM, Johnson KP, Malamud N (1980) The clinical and pathological spectrum of brain stem vascular malformations. Long term course simulates multiple sclerosis. Arch Neurol 37: 25-29 38. Sugiura K, Baba M (1990) Total removal of an arteriovenous malformation embedded in the brain stem. Surg Neuro134: 327330 39. Suzuki J, Onuma T (1979) Intracranial aneurysms associated with arteriovenous malformations. J Neurosurg 50:742-746 40. Troupp H, Martila I, Halonen V (1970) Arteriovenous malformations of the brain. Prognosis without operation. Acta Neurochir (Wien) 22:125-128 41. Viale GL, Pau A, Viale ES (1979) Surgical treatment of arteriovenous malformations of the posterior fossa. Surg Neurol 12:379-384 42. Voigt K, Ya~argil MG (1976) Cerebral cavernous hemangiomas or caveruomas. Nenrochirurgia (Stuttg) 19:59-68 43. Weil S, Tew JM, Steiner L (1990) Comparison of radiosurgery and microsurgery for treatment of cavernous malformation of the brain stem. Abstract of papers. J Neurosurg 72: 336A 44. Tashiro Y, Uno A, Ishikawa M, Asato R (1986) Intracranial and orbital cavernous angiomas. A review of 30 cases. J Neurosurg 64:197-208 45. Yonekawa Y, Handa H, Taki W (1983) Total removal of a brain stem arteriovenous malformation: Case report. Neurosurgery 13:443-446 46. Yoshimoto T, Suzuki J (1986) Radical surgery on cavernous angioma of the brain stem. Surg Neurol 26:72-78 47. Zimmerman RS, Spetzler RF, Stuart Lee K, Zabramski JM, Hargraves RW (1991) Cavernous malformations of the brain stem. J Neurosnrg 75:32-39
Correspondence and Reprints: Prof. B. George, Service de Neuro-Chirurgie, H6pital Lariboisirre, 2 rue Ambroise Parr, F75010 Paris, France.
Acta Neurochir (Wien) (1992): 116:119 - 127
9 Springer-Verlag 1992 Printed in Austria
Arteriovenous Malformations of the Posterior Fossa* B. George, M. Celis-Lopez, T. Kato, and G. Lot Department of Neurosurgery, H6pital Lariboisi~re, Paris, France
Summary AVMs of the posterior fossa are reviewed on the basis of personal experience of 47 cases including 2 venous angiomas, 7 cavernous angiomas, 5 arteriovenous fistulas and 33 true arteriovenous malformations and of the few series reported in the literature. MRI is now an indispensable tool to define the exact localization of any malformation. Combined with angiography, it permits one to choose the most adequate therapeutic strategy and the best surgical approach. Radical cure is to be contemplated in most cases considering the often dramatic consequences of bleeding at the infratentorial level. Deep AVMs and moreover cavernous angiomas, even those located in highly functional structures such as the brain stem, can now be discussed for treatment. Encouraging results have already been obtained using, alone or in association, the recently advanced modalities of treatment: interventional neuroradiology, radiosurgery, and microsurgery. Keywords: Arteriovenous malformation; cavernous angioma; MRI; surgery.
T h o u g h all types o f A V M c a n be o b s e r v e d at the i n f r a t e n t o r i a l level, r e p o r t s o n a r t e r i o v e n o u s m a l f o r m a t i o n s ( A V M ) o f the p o s t e r i o r fossa are n o t n u m e r o u s 1, 7, 8, 19, 26, 31, 41. This is m a i n l y because they are u n c o m m o n lesions a n d thus surgical experience is generally limited.
Frequency A V M o f the p o s t e r i o r fossa includes true A V M , a r t e r i o v e n o u s fistula, c a v e r n o u s a n g i o m a , telengiectasis a n d the so-called venous a n g i o m a . Tables 1 a n d 2 indicate their respective frequencies at the s u p r a a n d i n f r a t e n t o r i a l level in o u r d e p a r t m e n t over the last 5 years a n d f r o m the w o r k o f M c C o r m i c k 2~ on a u t o p s y studies. Telengiectasis is the o n l y t y p e t h a t p r e d o m i -
* Invited Lecture, presented at the European Congress of Neurosurgery, Moscow, June 23-29, 1991
Table 1. Distribution of A VMs (Lariboisi~re series)
MAV CA FAV VA
Supratentorial
Infratentorial
171 7 5 2
33 36 53 13
Table2. Distribution ofAVMs (Mc Cormiek' series 1968)
MAV T CA VA
Supratentorial
Infratentorial
217 22 59 46
70 38 21 31
63% 7% 17% 13%
43% 24% 13% 19%
nates in the p o s t e r i o r fossa; for the others, d i s t r i b u t i o n at the infra a n d s u p r a t e n t o r i a l level is very similar.
Venous Angioma (VA) V A is the m o s t frequent v a s c u l a r m a l f o r m a t i o n f o u n d at a u t o p s y (2.6%) as it is less c o m m o n l y associated with bleeding. I n the p o s t e r i o r fossa, it is m a i n l y l o c a t e d in the d e p t h o f the cerebellum. C e r e b e l l a r localization a c c o u n t s for 2 5 % o f all V A s b u t represents 50% o f all V A s a s s o c i a t e d with h a e m a t o m a 22' 29, 32 Therefore, it m i g h t be c o n c l u d e d t h a t p o s t e r i o r fossa V A s s h o u l d be r e m o v e d in m o s t cases. H o w e v e r , a new c o n c e p t is t h a t this m a l f o r m a t i o n is in fact a n a b n o r m a l v e n o u s n e t w o r k which d e v e l o p e d to c o m p e n s a t e for the lack o f i m p o r t a n t n o r m a l d r a i n i n g veins 32' 35; SO its s u p p r e s s i o n can lead to severe consequences related to v e n o u s h y p e r t e n s i o n a n d infarction. M o r e o v e r , it has been s h o w n t h a t in some cases, the bleeding is in fact
120
B. George et at.: Arteriovenous Malformations of the Posterior Fossa
due to another associated malformation, especially a cavernous angioma 35' 47
Telangieetasis (T) T are small true capillary malformations. They generally cannot be identified by any current imaging tool. They can be the cause of some unexplained haematomas and particularly in the pons which is its c o m m o n site. However, from autopsy studies, T are mostly incidental: only one out of 38 cases had bled in Mc Cormick's report 2~ Table 3. Distribution
of CAs
Supratentorial Infratentorial
%
Mc Cormick et al. Simard et al. Robinson et al. Voigt and Ya~argil Lariboisi+re
58 109 58 126 43
21 18 13 38 7
26 14 18 23 14
Total
394
97
20
Table 4. Localization
o f C A in the Posterior Fossa
Cerebellum
Brain stem
Pons
Mc Corrnick et al. 2~ Simard et al. 34 Robinson et al. 28 Lariboisi6re
11 5 5
9 13 8
7 9
3
4
2
Total
24
34
18
Cavernous Angioma (CA) CAs of the posterior fossa account for about 25% of all cavernomas. Sex and mean age of discovery are similar at both supra and infratentorial levels. Localization in the posterior fossa is mainly in the brain stem and especially the pons 28' 34, 42, 44 (Tables 3 and 4). CAs are generally discovered after one or more bleeds which produce more or less dramatic neurological symptoms and signs. Since it is quite common that CA is associated with repeated minor bleeds, the clinical presentation may be a progressive worsening suggesting a tumour or a fluctuating deficit suggesting a demyelinating disease (multiple sclerosis). However, the density of highly functional structures in the brain stem explains that even minor leaks may lead to very significant and incapacitating deficits or even to death. So though the natural history of CA is not known 24, radical removal of posterior fossa lesions must be contemplated in each case. Since arterial feeders of cavernoma are very small, there is no possibility for endovascular treatment, The slow flow inside a CA led one to think that radiosurgery could be effective by inducing thrombosis. In fact, recently reported experience 43 of this treatment in 6 brain stem CAs has proven to be useless in all cases and even noxious in 3 cases due to radiation induced injury; in comparison, the same team treated surgically 7 similar cases with 6 good results and one with disability. Surgery is therefore the only adequate modality of treatment. M R I now provides not only the diagnosis with much certainty but also a precise anatomical locali-
Fig. 1. Pre (left) and post-operative (right) MRI of a brain stem cavernoma discovered after Needing
B. George etal.: Arteriovenous Malformations of the Posterior Fossa
zation. This permits one to choose the most direct and the least harmful route to reach the lesion. CA in the cerebellum, whatever the depth, can be reached and removed with almost no morbidity. Many cases of successful removal in the brain stem 16' 46, 47 have been reported. The main point is to define which part of the cavernoma is the closest to the floor of the fourth ventricle or to the lateral aspect of the brain stem. Each time, a CA reaches the surface or is covered by a thin lamina of brain stem tissue, resection can reasonably be attempted (Fig. 1). Dissection into the brain stem is generally facilitated by the surrounding gliotic and haemorrhagic tissue; however, in some places, the CA is directly in contact and even sometimes adherent to the normal parenchyma because of old haemorrhagic scars. These adhesions can make the dissection very difficult and hazardous.
Arteriovenous Fistula (AVF) Dural AVFs of the posterior fossa are very uncommon. AVFs of the lateral sinus almost always drain into the veins of the cerebral hemisphere. However, a pouch on the cerebellar veins may be the cause of bleeding in some cases as we observed in 5 patients including 2 at the foramen magnum, 2 on the transverse sinus and one on the tentorium close to the straight sinus (Fig. 2). Treatment is first endovascular but may be surgical in case of failure of intravascular occlusion.
121
AVF of the brain tissue is another but still more exceptional possibility. It may be either alone as in the case reported by Mount 21 and fed by the anterior inferior cerebellar artery or associated with a true nidus of an AVM as we observed in 1 of our cases of posterior fossa AVMs. Endovascular techniques are also the treatment of choice in those fistulas.
Arteriovenous Malformation (AVM) Posterior fossa AVMs account for about 15% of all cerebral AVMs. The brain stem is involved in 25%, the cerebello-pontine angle in 5%; the most frequent localization is in the cerebellum (70% of the cases) where AVMs are mainly found in the vermis, the AVM being developed either partly or totally in it 1' 7, 8, 19, 20, 31, 41. The two third of our 24 cases had this vermian localization (Tables 5 and 6). Bleeding is the almost exclusive circumstance of discovery (Table 7) and in more than half of the cases, Table 5. Distribution of A VMs Supratentoriai Infratentorial % Autopsy series2~ 217 Clinical series3' 6, 8, 10, 11, 19. 26, 31 1807 Lariboisitre series Total
70 206
24 10
171
33
16
2195
309
12
Fig. 2. Dural AVF of the tentorium draining into the straight sinus, fed by the occipital artery and the tentorial branch of the internal carotid artery and responsible for a cerebellar haematoma
122
B. George et al.: ArteriovenousMalformationsof the Posterior Fossa
Table6. Localization of A VMs
Autopsy series~~ Clinical series8,19,z6,~1,41 Lariboisibre series
Cerebellum Brainstem
CPA
52 111 25
12 3
15 34 5
CPA: Cerebello-pontineangle Table 7. Occurrence of Haemorrhage in A V M
Autopsy series2~ Clinical series8' 19.26.31,41 Lariboisi~re series
Haemorrhage
Total
%
42 128 27
67 149 33
63 86 82
with several previous occurrences of haemorrhage. Other modes of discovery are much less frequent: progressive neurological deficit, intracranial hypertension or hydrocephalus. Bleeding from posterior fossa AVMs may have severe consequences; so even if from studies on the natural history 3' 6, H, 12, 13, 37, 40, the rate of rebleeding is likely similar to those located at the supratentorial level, the prevention of new haemorrhages is much more important. For instance, Kondliolka ~3 reported on a 16% overall mortality in their population of AVMs but it was 57% for cases of cerebellar location; Fults and Kelly observed five deaths and one vegetative state due to haemorrhage in a series of 12 cases followed over the course of 7-8 years on averagd ~ Decisions about treatment are based on clinical data, age, general condition, and neurological state and on parameters of the AVM including localization, size, feeders, and drainage. These parameters are best appreciated using a combined analysis of MRI and angiography. M R I is now mandatory for investigating any AVM~5, 17. It gives a nice definition of the anatomical relationship of the AVM with the functional areas including the brain stem, nucleus dentatus, and brachium pontis. In many cases, specially those located in the antero-superior part of the vermis, angiography is not able to differentiate those really involving the brain stem from those extending close to it or even compressing it, but remaining in an extrapial plane. On the contrary, MRI can generally demonstrate the integrity or the involvement of the brain stem (Figs. 3 and 4). This very important point has already been underlined
by Drake 7 at a time where MRI was not available and where the true extent of the AVM was discovered at surgery. MRI helps also determine the size of the nidus and often demonstrates very nicely the feeders and the draining veins. Therefore, with the great advantage of having views in the three spatial planes, MRI is an invaluable tool for defining the best surgical approach and the best therapeutic strategy. However, identification of feeders and draining veins still requires angiography. It gives their number and respective importance and can also reveal an associated aneurysm which is found in about 10% of cases on the arterial feeders 2' 4, 7, 20, 39. Questions concerning feeders and drainage are therefore well answered by these two examinations: which cerebellar artery is giving the main supply? Does any perforating branch participate in the AVM supply? What is the main venous drainage? Are the main arterial supply and the main drainage superimposed? What is the distance between the nidus and the functional structures? What is the number of feeders which is in fact closely related to the size of the nidus? Some of the above mentioned questions correspond to the items of the currently proposed classifications33' 36. However, these classifications do not fit very well with the AVMs of the posterior fossa. In fact, especially regarding the surgical problems, feeders and drainage particularities which are not included in these classifications are of great importance in the posterior fossa. Consequently, besides the size and localization, it seems useful to add a classification based on the vascular presentation (Fig. 5). According to this last point, posterior fossa AVMs can be separated into: i) medial AVMs with their main supply from either the posteroinferior cerebellar artery (PICA) or the superior cerebellar artery (SCA) according to the more or less superior extension, and draining medially into the vein of Galen, the straight sinus and the transverse sinus; ii) lateral AVMs fed mainly by the anterior-inferior cerebellar artery (AICA) and draining laterally towards the petrosal vein and the sigmoid sinus; iii) deep AVMs supplied by perforating branches and draining into ependymal and periaxial veins; iv) extensive AVMs combining several of the above types. This classification is obviously related to the AVM localization but gives less importance to the size. Conversely, it stresses the difficulty of how to reach the main feeder. For instance, the control of the SCA in a supero-medial AVM by a posterior approach supposes the surgeon to be able to pass above the nidus
B. George etal.: Arteriovenous Malformations of the Posterior Fossa
A
C
123
B
Fig. 3. MRI definition of AVMs. A) AVM of the eulmen extending up to the quadrigeminal plate but remaining in the extrapial plane of the brain stem. B) AVM of the quadrigeminal plate with intraparenchymal extension (same case as Fig. 5 C). C) Superomedial AVM of the cerebellum. Notice the venous drainage towards the vein of Galen and the straight sinus
and to isolate the S C A f r o m the draining veins. The same c o m m e n t can be m a d e for a cerebello-pontine angle A V M with the A I C A and the petrosal vein. I n those cases, a pre-operative embolization o f these feeders m a y be o f great help.
M e t h o d s o f treatment for posterior fossa A V M s include interventional radiology, radiosurgery, and microsurgery. Embolization can reduce the vascular supply and the nidus size o f an A V M but it can achieve a complete cure only in very few cases 9, 27. So, it must
124
B. George etal.: Arteriovenous Malformations of the Posterior Fossa
Fig. 4. Brain stem AVM with development inside the medulla. Notice the venous drainage on angiography and on MRI
be generally included in a protocol where embolization is associated with surgery or with radiotherapy (Fig. 6). As already mentioned, it is the best treatment in cases of AVF. Embolization can be used to control arterial feeders which would necessitate a different surgical approach to that chosen for AVM resection. For example, a supero-medial AVM fed by the SCA would require a sub-occipital transtentorial or a subtemporal approach to expose and ligate this vessel and a posterior approach to remove the AVM. Intravascular occlusion of the SCA branches permits one to avoid one surgical stage, and embolization of the most anterior part of the nidus facilitates the surgical dissection in an area opposite to the posterior approach. In large and high flow AVMs where a break-through phenomenon might be expected and multistaged surgery is planned, embolization can replace one of the stages; however, no one case of this phenomenon has yet been reported in the literature after the removal of a posterior fossa AVM. Radiosurgery is essentially effective in small volume AVMs. It seems tempting to propose this technique in AVM located close to or in functional areas. However, we are not aware of any experience of treatment of brain stem AVM by this technique; the risk of radiation induced injury which seems to be around 3 %, probably prevents any attempt being made 23. So, radiotherapy
is indicated rather to complete the cure of a large AVM previously reduced by embolization or surgery. In fact, surgery is the best way to obtain a radical cure, the two other forms of treatment being complementary in some cases; pre-operative embolization to help control the vascular supply and radiosurgery to treat a post-operative remnant. Surgical principles for infratentorial AVMs are similar to those for supratentorial ones: a large exposure giving primary access to feeders, microsurgical dissection flush to the nidus, preservation of the main drainage until total control of the nidus has been achieved. Particular attention must be paid to coagulation of all tiny tortuous vessels surrounding the nidus; great care must be taken not to stretch these vessels by compressing the nidus and even by coagulating them so as to avoid their rupture and their retraction inside the parenchyma1,8; control of extent of the resection must be very careful and especially by looking inside the fourth ventricle in vermian and cerebello-pontine angle AVMs, since leaving some AVM behind, may be the source of post-operative haematoma. Post-operative haemorrhage is the main cause of death and disability in Drake's seriesS: 9 out of 66 cases. Haemostasis must be checked carefully and specially if the sitting position is used. Results of treatment in the published series and in
B. George etal.: Arteriovenous Malformations of the Posterior Fossa
125
Fig. 5. A) Medial AVM (superior) fed by the SCA and drained by the vein of Galen. B) Lateral AVM fed by the AICA (with an aneurysm) and drained by the petrosal vein. C) Deep AVM fed by a perforating branch (same case as Fig. 3 B). D) Extensive AVM fed by the three cerebellar arteries (SCA, AICA, and PICA)
ours indicated a rate of death and disability about twice that for the general series of cerebral AVMs; if brain stem angiomas are considered separately, results are far worse 4' s, 7, 18, 25, 30, 35, 38, 45 (Table 8). This is to be placed in parallel with the high rate of morbidity and mortality after posterior fossa A V M bleeding. How-
ever, better understanding of the localization and vascular arrangement of these AVMs with the help of a combined analysis of M R I and angiography should permit improvement of those results by a better definition of the most adequate therapeutic protocol and of the best surgical strategy.
126
B. George et al.: Arteriovenous Malformations of the Posterior Fossa
Fig. 6. Medial AVM (superior) treated by embolization and radiosurgery. Left and center: before embolization; right: after embolization before radiosurgery
Table 8. Results of Surgical Treatment of A VMs Worsened C e r e b e l l u m 8, 19,
31, 41
Literature Lariboisi6re Brain stem4' 5, 7, 18, 25, 30, 35, 38,45 Literature Lariboisi6re Total
Died
N = 87 N = 13
7 1
N = 23 N = 2
-
N = 125
13
7 -
5
2 9
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Correspondence and Reprints: Prof. B. George, Service de Neuro-Chirurgie, H6pital Lariboisirre, 2 rue Ambroise Parr, F75010 Paris, France.
