Alt h o u g h infratentorial AVMs comprise only

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1 Neurosurg Focus 26 (5):E12, 2009 Posterior fossa arteriovenous malformations Om a r M. Arn a o u t, B.A., 1 Br a d l e y A. Gr o s s, M.D., 2 Ch r i s t o p h e r S. Ed d l e m a n, M.D., Ph.D., 1 Be r n a r d R. Be n d o k, M.D., 1 Ch r i s t o p h e r C. Ge t c h, M.D., 1 a n d H. Hu n t Ba t j e r, M.D. 1 1 Department of Neurological Surgery, The Feinberg School of Medicine and McGaw Medical Center, Northwestern University, Chicago, Illinois; and 2 Department of Neurological Surgery, Brigham and Women s Hospital and Harvard Medical School, Boston, Massachusetts Arteriovenous malformations (AVMs) of the posterior fossa are complex neurovascular lesions that are less common than their supratentorial counterparts, accounting for < 15% of all AVMs. The majority of patients with these lesions present with intracranial hemorrhage, a factor that has been consistently shown to increase one s risk for subsequent bleeding. Studies have additionally shown a posterior fossa or deep AVM location to portend a more aggressive natural history. The authors reviewed the literature on posterior fossa AVMs, finding their annual rupture rates to be as high as 11.6%, an important factor that underscores the importance of aggressive treatment of lesions amenable to intervention as therapeutic options and results continue to improve. (DOI: / FOCUS0914) Ke y Wo r d s arteriovenous malformation infratentorial location posterior fossa natural history Alt h o u g h infratentorial AVMs comprise only 7 15% of intracranial AVMs, 1,2,8,10,26,38 accumulating data have demonstrated an independent association of infratentorial AVM location and hemorrhagic presentation. 19,26,38 This is alarming in light of the considerably greater morbidity and mortality associated with posterior fossa AVM rupture. 12,18 Fortunately, with accumulating surgical experience and the cultivation of multimodality AVM therapy, therapeutic success continues to improve. 18,21,25 This is particularly crucial in light of the growing body of modern literature pertaining to AVMs in which authors have detailed the aggressive natural history of these lesions. 12,15,18,24,40 Posterior Fossa AVMs Clinical Presentation Unlike their supratentorial counterparts, infratentorial AVMs are more likely to present with hemorrhage and rarely present with seizures. 2,4,8,11,18,26,27,29,34,38,39 With 6 of the larger surgical series combined, 207 (84%) of 246 patients harboring infratentorial AVMs presented with hemorrhage (Table 1). In the original Cooperative Abbreviations used in this paper: AVM = arteriovenous malformation; mrs = modified Rankin Scale. Neurosurg. Focus / Volume 26 / May 2009 Study, 27 7 (27%) of 26 patients died as a result of their presenting hemorrhage. Fults and Kelly 12 noted that less than half of their patients with posterior fossa AVMs survived an initial hemorrhage, and hemorrhagic mortality rates of up to 66.7% have been reported for posterior fossa AVM rupture. 34 In addition to the aforementioned surgical series, numerous recent observational studies have also demonstrated the greater rate of hemorrhagic presentation among patients with these lesions, 11,17,28,32,39 with only a few exceptions. 9,20,22 In a multivariate analysis targeted at elucidating the relationship between infratentorial location and hemorrhagic presentation, Khaw et al. 19 demonstrated that infratentorial AVMs were almost twice as likely to present with hemorrhage as supratentorial AVMs. Similarly, in the Toronto Study group (60%) of 35 patients with infratentorial AVMs presented with hemorrhage, compared with 125 (35%) of 355 patients with supratentorial AVMs and 88 (29%) of 299 patients with superficial AVMs. Kader et al. 17 reported similar findings in which 36 (86%) of 42 patients with infratentorial AVMs presented with hemorrhage compared with 221 (54%) 407 with supratentorial lesions. Progressive neurological deficits (including those secondary to mass effect, ischemia, and hydrocephalus) were the second most common mode of presentation, seen in up to 28% of patients (Table 1). With respect to 1

2 O. M. Arnaout et al. TABLE 1: Summary of clinical presentations in patients with posterior fossa AVMs in surgical series No. of Posterior Fossa AVMs Hemorrhagic Presentation (%) Other Presentation (%) Perret et al., (81) 4 (13) symptomatic, 2 (6) incidental Batjer et al., (72) 9 (28) progressive deficits Drake et al., (92) 3 (5) headache, 2 (3) focal deficit Solomon et al., (92) 1 (8) gradual onset of symptoms Symon et al., (85.7) 4 (14) progressive deficits, 2 (7) occipital/retroauricular pain, 1 (4) headache only Kelly et al., 2008* (82) 9 (19) cranial nerve palsy, 8 (17) headache, 1 (2) hemiparesis, 11 (23) ataxia * Modes of presentation depicted for 48 patients with Spetzler-Martin Grade III V AVMs. asymptomatic posterior fossa AVMs, these reports are likely to underestimate the true prevalence as individuals in this subset may not present for clinical evaluation. However, the incidence of asymptomatic posterior fossa AVMs may rise in the future with the increasing use of advanced neuroimaging modalities for nonspecific symptomatology. Risk Factors for Hemorrhage Numerous studies on posterior fossa AVMs have demonstrated a correlation between the incidence of hemorrhage and an increased risk of subsequent rupture (Table 2) with few exceptions. 24,33 This phenomenon is perhaps most dramatically illustrated in the report by Mast et al., 23 in which annual hemorrhage rates of lesions that had previously bled were as high as 17.8%. The authors concluded that hemorrhagic presentation was the most important feature influencing subsequent hemorrhage rates. This was reinforced by Stapf et al. 30 who, in a multivariate model, reported annual rehemorrhage rates ranging from 4.5 to 34.3%, depending on lesion location and deep venous drainage. In their analysis of 678 patients, da Costa et al. 6 found that hemorrhage on presentation was an independent predictor of future bleeding. Interestingly, a proclivity toward hemorrhage clustering is underscored by the 6 15% annual rehemorrhage rates reported across the 1st year after hemorrhage in several studies. 6,13,14,16,40 Furthermore, recent studies of Halim et al., 14 Yamada et al., 40 da Costa et al., 6 and Hernesniemi et al. 15 have shown relatively elevated annual rehemorrhage rates of 5 6% up to 5 years after an initial hemorrhagic presentation. There is a growing body of evidence implicating a posterior fossa location as an independent risk factor for rupture (Table 3). Six of 8 studies evaluating infratentorial or deep location as a risk factor for hemorrhage demonstrated increased hemorrhage rates among these lesions. The University of Toronto Vascular Malformation Study Group 33 included 390 ly followed patients whose intracranial AVMs were grouped as deep (including basal ganglia, thalamus, cerebellum, and corpus callosum) and superficial (all other locations). While no individual location correlated with an increased risk of future hemorrhage, deep AVMs as a group correlated strongly with future hemorrhage in multivariate analysis, increasing the risk approximately 5-fold. Using the same stratification of AVM location in their analysis of the natural history of 305 AVMs, Yamada et al. 40 also noted that deep location was a risk factor for rupture. Whereas superficial AVMs had an annual rebleeding rate of 3.28%, deep AVMs had a statistically significantly greater annual rebleeding rate of 11.41%. Mine et al. 24 reported an annual bleed rate of 7.5% at 5 years and 5.0% at 10 years for deep AVMs whereas superficial lesions had an annual hemorrhage rate of 1.1% at 5 years and 1.4% at 10 years. In their multivariate statistical model, deep AVMs had an approximate 4-fold increase in the risk of rupture. Recently, Hernesniemi et al. 15 ly evaluated data obtained in 238 patients between 1942 and 2005 (mean follow-up 13.5 years). An AVM location in the posterior fossa was found to be an independent risk factor for hemorrhage in all 3 multivariate models used by the investigators. As a subgroup, infratentorial AVMs had the highest overall annual rupture rate 11.6% in the first 5 years after presentation and 6.7% overall. In their surgical series, Kelly et al. 18 reported an annual rupture rate of % for posterior fossa AVMs. The increased proclivity of posterior fossa AVMs to present with hemorrhage may depend on anatomical and hemodynamic factors, some unique to this location. In their series of 98 patients with posterior fossa AVMs, da Costa et al. 7 noted that the presence of aneurysms was an independent predictor of poor mrs score at final followup, consistent with other studies that associated the presence of aneurysms with an increased risk of AVM hemorrhage. 31,35 Another potential factor increasing hemorrhage risk may be perforator involvement, cited by Hernesniemi et al., 15 as these feeding vessels are less tolerant of high flow. Interestingly, perforator artery involvement and vertebrobasilar supply have been implicated as risk factors for hemorrhagic presentation of AVMs in other studies as well. 36 Furthermore, the increased frequency of deep 2 Neurosurg. Focus / Volume 26 / May 2009

3 Posterior fossa AVMs TABLE 2: Annual AVM hemorrhage rates stratified by hemorrhagic and nonhemorrhagic presentation* Annual Bleeding Rate (%) No. of Patients, No. Infratentorial Lesions, Study Type Mean Follow-Up Nonhem Hem Graf et al., , 11 infratentorial, 4.8 yrs yr: 6; after: 2 Crawford et al., , 10.4 yrs Itoyama et al., , 13.4 yrs 1 yr 4.8; 5 yr yr: 6.9; 5 yrs: 1.91 Pollock et al., , 10,939 patient-yrs Mast et al., , 30 infratentorial, 8.5 mos (hem) mos (nonhem) Halim et al., , 854 patient-yrs (hem) 2302 patient-yrs (nonhem) 1 yr: 3 5 yr: 2 10 yr: 2 1 yr: 6 5 yrs: 5 10 yrs: 3 Stapf et al., , 74 infratentorial, 2.3 yrs Yamada et al., , 105 deep, mixed 892 patient-yrs 3.1 overall: 6.8; 1st yr: 15.4; 5 yrs: 5.3 Hernesniemi et al., 2008** 238, 18 infratentorial, 13.5 yrs overall: 1.6; 5 yr: 2.3 overall: yrs: 6.2 da Costa et al., , 2.9 yrs overall: 4.6 1st yr: yrs: 4.0 >5 yrs: 3.9 * Hem = hemorrhage; nonhem = nonhemorrhage. Superficial location, not having exclusively deep venous drainage. Superficial location, exclusively deep venous drainage. Deep location, not having exclusively deep venous drainage. Deep location with exclusively deep venous drainage. ** Includes data from prior study of Ondra et al. Data presented for entire cohort versus hemorrhagic presentation. overall: 7.5 1st yr: yrs: 6.3 >5 yrs: 3.7 venous drainage seen with posterior fossa AVMs may also contribute by increasing the pressure gradient in the AVM nidus. Vinuela et al. 37 have described the possibility of hemodynamic changes resulting from the convergence of draining veins into the vein of Galen and the straight sinus as contributory factors for increased rupture rates. Finally, Willinsky et al. 39 have proposed that venous kinking at the level of the tentorium, producing a state of venous outflow stenosis which has been previously associated with increased rupture risk, 3,6,14 may also be a contributing factor. Other factors that may modify the risk of rupture of these lesions have been studied, but there is currently little agreement in the literature regarding the significance of their contribution. For instance, whereas several authors have noted small nidus size as a risk factor for rupture, 17,20 others have found that larger AVMs tended to bleed more frequently. 15,24,33 Other factors thought to be associated with rupture risk include age, 5,11,30,40 sex, 23,40 and venous drainage patterns 17,20,22,28 for which the data were similarly inconsistent. Neurosurg. Focus / Volume 26 / May 2009 Treatment and Outcomes Accumulating experience with the treatment of posterior fossa AVMs and the incorporation of multimodality approaches, including radiosurgery, endovascular therapy, and improved microsurgical techniques, have significantly contributed to continuously improving outcomes (Table 4). The their classic series detailing surgical outcomes in the treatment of posterior fossa AVMs, Drake et al. 8 reported a 92% obliteration rate with 71% of patients having an excellent to good outcome. Batjer and Samson 2 reported a 100% obliteration rate with 80% of patients experiencing excellent to good outcomes in their experience with 30 posterior fossa AVMs. Kelly et al. 18 have also described their experience with treating AVMs located in the posterior fossa, although the analysis included only the 48 lesions that were Spetzler-Martin Grades III V and the rate of angiographic obliteration was 52%, whereas 81% of patients had excellent to good outcomes. Finally, in their series of 98 posterior fossa AVMs, 3

4 O. M. Arnaout et al. TABLE 3: Studies reviewing infratentorial and/or deep AVM location as a risk factor for hemorrhage Fults et al., 1984 Pollock et al., 1996 Mine et al., 2000 Stefani et al., 2002 Stapf et al., 2006 Yamada et al., 2007 da Costa et al., 2008 Hernesniemi et al., 2008 No. of Patients, No. Infratentorial, Study Type 131, 10 infratentorial, 315, 97 deep,* 55, 16 deep, 390, 35 infratentorial, 622, 74 infratentorial, 305, 105 deep, mixed 678, 85 deep, 238, 18 infratentorial Mean Follow-Up Location as a Risk Factor (deep &/or infratentorial) 8.7 yrs yes (infratentorial) 10,939 patient-yrs yes (deep on univariate) Annual Infratentorial Hemorrhage Rates 10.5 yrs yes (deep/infratentorial) 5 yrs: 7.5%; 10 yrs: 5.0% 3.1 yrs yes (deep/infratentorial) 2.3 yrs no (infratentorial) 892 patient-yrs yes (deep/infratentorial) if prior hem: 11.4%; if no hem: 4.4% 2.9 yrs no (deep/infratentorial) 13.5 yrs yes (infratentorial) overall: 6.7%; 5 yrs: 11.6% * Thalamus, basal ganglia, corpus callosum, or brainstem. Thalamus, basal ganglia, brain stem or cerebellum. Insular, thalamus, basal ganglia, corpus callosum, brain stem, or cerebellum. Deep white matter tracts, basal ganglia and thalamus, peri-ventricular regions, or posterior fossa. da Costa et al. 7 reported good mrs outcomes in 67% of cases whereas in 28% of the cases patients suffered from poor outcomes but also presented that way, implying that the final outcome was related to the mrs score on initial presentation. Conclusions Infratentorial AVMs are complex neurovascular lesions that, as opposed to their supratentorial counterparts, pose an increased risk for hemorrhagic presentation as well as increased morbidity and mortality due to their presence in the narrow confines of the posterior fossa and in proximity to many critical structures including the brainstem, cranial nerves, and small perforator vessels. An intimate understanding of the natural behavior of these lesions is paramount to allow one to develop a timely management plan. Although the risks of treatment are considerable, outcomes are reassuring. It is clear that intracranial AVMs comprise a heterogeneous group of vascular lesions with variable natural history; posterior fossa AVMs merit multimodality intervention when feasible in most cases because of their higher risk of rupture and higher potential for morbidity and mortality. Disclaimer The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper. References 1. Al-Shahi R, Warlow C: A systematic review of the frequency and prognosis of arteriovenous malformations of the brain in adults. Brain 124: , Batjer H, Samson D: Arteriovenous malformations of the posterior fossa: clinical presentation, diagnostic evaluation and surgical treatment. Neurosurg Rev 9: , Brown RD Jr, Wiebers DO, Forbes G, O Fallon WM, Piepgras DG, Marsh WR, et al: The natural history of unruptured intracranial arteriovenous malformations. J Neurosurg 68: , Brown RD Jr, Wiebers DO, Torner JC, O Fallon WM: Frequency of intracranial hemorrhage as a presenting symptom and subtype analysis: a population-based study of intracranial vascular malformations in Olmsted Country, Minnesota. J Neurosurg 85:29 32, Crawford PM, West CR, Chadwick DW, Shaw MD: Arteriovenous malformations of the brain: natural history in unoperated patients. J Neurol Neurosurg Psychiatry 49:1 10, da Costa L, Wallace MC, Ter Brugge KG, O Kelly C, Willinsky RA, Tymianski M: The natural history and predictive features of hemorrhage from brain arteriovenous malformations. Stroke 40: , da Costa LB, Thines L, Dehdashti AR, Wallace MC, Willinsky RA, Schwartz M, et al: Management and clinical outcome of posterior fossa arteriovenous malformations: report on a single-center 15-year experience. J Neurol Neurosurg Psychiatry 80: , Drake CG, Friedman AH, Peerless SJ: Posterior fossa arteriovenous malformations. J Neurosurg 64:1 10, Duong DH, Young WL, Vang MC, Sciacca RR, Mast H, Koennecke HC, et al: Feeding artery pressure and venous drainage pattern are primary determinants of hemorrhage from cerebral arteriovenous malformations. Stroke 29: , Fleetwood IG, Steinberg GK: Arteriovenous malformations. Lancet 359: , Fullerton HJ, Achrol AS, Johnston SC, McCulloch CE, Higashida RT, Lawton MT, et al: Long-term hemorrhage risk 4 Neurosurg. Focus / Volume 26 / May 2009

5 Posterior fossa AVMs TABLE 4: Operative results of surgical series dealing with posterior fossa AVMs No. of Patients Presentation (%) Obliteration Rate (%) Op Detail (%) Batjer & Samson, hem, 28 progressive neurological deficits morbidity, 7 mortality Drake et al., hem, 5 headache, 3 focal deficits 92 successful resection 25 morbidity, 15 mortality Solomon & Stein, 1986* hem, 8 progressive neurological deficits morbidity, 0 mortality Symon et al., hem, 14 progressive deficits morbidity, 8.6 mortality Lawton et al., hem, 9 progressive neurological deficits, 3 seizure, 3 incidental 43 (initially), 72 (after incorporating 9 morbidity, 0 mortality Kelly et al., 2008 radiosurgery) hem 52.1 complete angiographic obliteration 14.6, reduction 8.3, reduction 6.3, reduction 10.4, 50 reduction 10.4 morbidity, 8.3 mortality (across all treatment modalities) * Brainstem AVMs only. Obliteration rate for 9 AVMs removed surgically. Basal ganglia, thalamus, and brainstem AVMs. Kelly et al. treatment data include only 48 patients with Spetzler-Martin AVMs Grades III V; data from all 76 patients included in the presentation column. in children versus adults with brain arteriovenous malformations. Stroke 36: , Fults D, Kelly DL Jr: Natural history of arteriovenous malformations of the brain: a clinical study. Neurosurgery 15: , Graf CJ, Perret GE, Torner JC: Bleeding from cerebral arteriovenous malformations as part of their natural history. J Neurosurg 58: , Halim AX, Johnston SC, Singh V, McCulloch CE, Bennett JP, Achrol AS, et al: Longitudinal risk of intracranial hemorrhage in patients with arteriovenous malformation of the brain within a defined population. Stroke 35: , Hernesniemi JA, Dashti R, Juvela S, Vaart K, Niemela M, Laakso A: Natural history of brain arteriovenous malformations: a long-term follow-up study of risk of hemorrhage in 238 patients. Neurosurgery 63: , Itoyama Y, Uemura S, Ushio Y, Kuratsu J, Nonaka N, Wada H, et al: Natural course of unoperated intracranial arteriovenous malformations: study of 50 cases. J Neurosurg 71: , Kader A, Young WL, Pile-Spellman J, Mast H, Sciacca RR, Mohr JP, et al: The influence of hemodynamic and anatomic factors on hemorrhage from cerebral arteriovenous malformations. Neurosurgery 34: , Kelly ME, Guzman R, Sinclair J, Bell-Stephens TE, Bower R, Hamilton S, et al: Multimodality treatment of posterior fossa arteriovenous malformations. J Neurosurg 108: , Khaw AV, Mohr JP, Sciacca RR, Schumacher HC, Hartmann A, Pile-Spellman J, et al: Association of infratentorial brain arteriovenous malformations with hemorrhage at initial presentation. Stroke 35: , Langer DJ, Lasner TM, Hurst RW, Flamm ES, Zager EL, King JT Jr: Hypertension, small size, and deep venous drainage are associated with risk of hemorrhagic presentation of cerebral arteriovenous malformations. Neurosurgery 42: , 1998 Neurosurg. Focus / Volume 26 / May Lawton MT, Hamilton MG, Spetzler RF: Multimodality treatment of deep arteriovenous malformations: thalamus, basal ganglia, and brain stem. Neurosurgery 37:29 35, Marks MP, Lane B, Steinberg GK, Chang PJ: Hemorrhage in intracerebral arteriovenous malformations: angiographic determinants. Radiology 176: , Mast H, Young WL, Koennecke HC, Sciacca RR, Osipov A, Pile-Spellman J, et al: Risk of spontaneous haemorrhage after diagnosis of cerebral arteriovenous malformation. Lancet 350: , Mine S, Hirai S, Ono J, Yamaura A: Risk factors for poor outcome of untreated arteriovenous malformation. J Clin Neurosci 7: , Natarajan SK, Ghodke B, Britz GW, Born DE, Sekhar LN: Multimodality treatment of brain arteriovenous malformations with microsurgery after embolization with onyx: single-center experience and technical nuances. Neurosurgery 62: , Ondra SL, Troupp H, George ED, Schwab K: The natural history of symptomatic arteriovenous malformations of the brain: a 24-year follow-up assessment. J Neurosurg 73: , Perret G, Nishioka H: Report on the Cooperative Study of Intracranial Aneurysms and Subarachnoid Hemorrhage. Section VI. Arteriovenous malformations. An analysis of 545 cases of cranio-cerebral arteriovenous malformations and fistulae reported to the cooperative study. J Neurosurg 25: , Pollock BE, Flickinger JC, Lunsford LD, Bissonette DJ, Kondziolka D: Factors that predict the bleeding risk of cerebral arteriovenous malformations. Stroke 27:1 6, Solomon RA, Stein BM: Management of arteriovenous malformations of the brain stem. J Neurosurg 64: , Stapf C, Mast H, Sciacca RR, Choi JH, Khaw AV, Connolly ES, et al: Predictors of hemorrhage in patients with untreated brain arteriovenous malformation. Neurology 66: ,

6 O. M. Arnaout et al. 31. Stapf C, Mohr JP, Pile-Spellman J, Sciacca RR, Hartmann A, Schumacher HC, et al: Concurrent arterial aneurysms in brain arteriovenous malformations with haemorrhagic presentation. J Neurol Neurosurg Psychiatry 73: , Stefani MA, Porter PJ, terbrugge KG, Montanera W, Willinsky RA, Wallace MC: Angioarchitectural factors present in brain arteriovenous malformations associated with hemorrhagic presentation. Stroke 33: , Stefani MA, Porter PJ, terbrugge KG, Montanera W, Willinsky RA, Wallace MC: Large and deep brain arteriovenous malformations are associated with risk of future hemorrhage. Stroke 33: , Symon L, Tacconi L, Mendoza N, Nakaji P: Arteriovenous malformations of the posterior fossa: a report on 28 cases and review of the literature. Br J Neurosurg 9: , Thompson RC, Steinberg GK, Levy RP, Marks MP: The management of patients with arteriovenous malformations and associated intracranial aneurysms. Neurosurgery 43: , Turjman F, Massoud TF, Vinuela F, Sayre JW, Guglielmi G, Duckwiler G: Correlation of the angioarchitectural features of cerebral arteriovenous malformations with clinical presentation of hemorrhage. Neurosurgery 37: , Vinuela F, Nombela L, Roach MR, Fox AJ, Pelz DM: Stenotic and occlusive disease of the venous drainage system of deep brain AVM s. J Neurosurg 63: , Wilkins RH: Natural history of intracranial vascular malformations: a review. Neurosurgery 16: , Willinsky R, Lasjaunias P, Terbrugge K, Pruvost P: Brain arteriovenous malformations: analysis of the angio-architecture in relationship to hemorrhage (based on 152 patients explored and/or treated at the hopital de Bicetre between 1981 and 1986). J Neuroradiol 15: , Yamada S, Takagi Y, Nozaki K, Kikuta K, Hashimoto N: Risk factors for subsequent hemorrhage in patients with cerebral arteriovenous malformations. J Neurosurg 107: , 2007 Manuscript submitted January 15, Accepted February 26, Address correspondence to: H. Hunt Batjer, M.D., Department of Neurological Surgery, Feinberg School of Medicine, Northwestern University, 676 North St. Clair Street, Suite 2210, Chicago, Illinois h-batjer@northwestern.edu. 6 Neurosurg. Focus / Volume 26 / May 2009