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(Stroke. 1995;26:1215-1220.)
© 1995 American Heart Association, Inc.

Articles

`Steal' Is an Unestablished Mechanism for the Clinical Presentation of Cerebral Arteriovenous Malformations

Henning Mast, MD; J. P. Mohr, MD; Andrei Osipov, MD; John Pile-Spellman, MD; Randolph S. Marshall, MD; Ronald M. Lazar, PhD; Bennett M. Stein, MD William L. Young, MD

From the Departments of Neurology (H.M., J.P.M., R.S.M., R.M.L.), Anesthesiology (A.O., W.L.Y.), Neurological Surgery (J.P.-S., B.M.S., W.L.Y.), and Radiology (J.P.-S., W.L.Y.), Columbia–Presbyterian Medical Center, New York, NY.

Correspondence to William L. Young, MD, Department of Anesthesiology, Box 46, Columbia University, 630 W 168th St, New York, NY 10032. E-mail wly1@columbia.edu.

	Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Background and Purpose Focal neurological deficits (FNDs) in patients with arteriovenous malformations (AVMs) have been widely attributed to the phenomenon of "cerebral steal." The incidence of focal deficits was investigated in a large prospective sample.

Methods Using data from patient history and examination, CT or MRI, and transcranial Doppler sonography, we studied 152 consecutive, prospective AVM patients for evidence of FNDs unrelated to a hemorrhagic event. Feeding mean arterial pressure was measured during superselective angiography.

Results Two (1.3%) of 152 patients met the criteria for a progressive FND. Nonprogressive FNDs were seen in 11 (7.2%) patients (stable in 4.6%, reversible in 2.6%). The median observation time period was 17 months (range, 1 to 60 months). There were no differences in transcranial Doppler mean velocities in feeding arteries in FND versus non-FND groups (118±44 versus 112±37 cm/s, P>.05) or pulsatility indexes (0.53±0.20 versus 0.55±0.15, P>.05). Feeding artery pressure was similar in FND (n=10) and non-FND (n=96) groups (39±16 versus 39±16 mm Hg at a systemic pressure of 82±18 versus 75±14 mm Hg, NS).

Conclusions Nonhemorrhagic focal neurological syndromes in AVM patients are infrequent. Progressive deficits are especially rare. There was no relation between feeding artery pressure or flow velocities and FND. There does not appear to be sufficient evidence to assign steal as an operative pathophysiological mechanism in the vast majority of AVM patients.

Key Words: cerebral arteriovenous malformations • diagnostic imaging • hemodynamics • perfusion

	Introduction

Top Abstract Introduction Subjects and Methods Results Discussion References

 
The concept of "steal" in arteriovenous malformations (AVMs) was initially fostered by the observation that adjacent brain structures frequently do not opacify with contrast angiography. More recently, the concept has been refined on the assumption that a high flow volume shunted through an AVM fistula may induce a decrease in cerebral perfusion pressure. Such a decrease may result from a combination of arterial hypotension and venous hypertension,¹ which has been described by many groups.^{2 3 4 5 6 7 8 9} If perfusion pressure is reduced sufficiently, symptomatic cerebral ischemia may be the result. The proposed clinical correlate is the development of progressive, but also stable and reversible, neurological deficits. Some authors have extended the steal hypothesis even further to account for the occurrence of seizures.¹⁰

The reported clinical frequency of cerebral steal in AVMs^{11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27} (Table 1) varies widely, but its importance as a pathophysiological principle in AVMs has been questioned.^{1 28} No large prospective study has yet examined the clinically detectable frequency of neurological deficits unrelated to hemorrhage. The AVM Data Bank of the Columbia–Presbyterian Medical Center offered the opportunity to investigate this question in a prospectively collected data sample.

View this table: [in this window] [in a new window]   Table 1. Symptoms and Signs in 1860 Patients With Arteriovenous Malformations

	Subjects and Methods

Top Abstract Introduction Subjects and Methods Results Discussion References

 
The AVM Data Bank of the Columbia–Presbyterian Medical Center is a prospective, observational database that records patient clinical course and various physiological data in a model based on the Stroke Databank.^{29 30} Using data from patient history, neurological examination, cranial CT or MRI, and transcranial Doppler sonography, we studied 152 consecutive, prospective cerebral AVM cases for evidence of focal neurological deficits (FNDs) unrelated to hemorrhagic events.

An FND was assumed to be present under the following conditions: (1) the physical examination at the time of the first clinical presentation revealed an FND, (2) the patient's history suggested a focal deficit at one time (reversible event), or (3) the patient spontaneously developed an FND after inclusion in the study (treatment complications from embolization and surgical procedures were not included). Patients with imaging evidence of hemorrhage coinciding with the onset of a focal syndrome were excluded from the FND group.

Patients presenting with a deficit on examination and a history or follow-up evaluation of a continuous or stepwise deterioration were judged as having "progressive" FNDs. Neither seizure disorders nor reversible postictal focal deficits were rated as FNDs. Reversible FNDs with no additional elementary (involuntary rhythmic motor activity or positive sensory signs) or complex (vigilance/mental changes) partial-seizure features were accepted for the FND group. All cases included in the study were investigated by CT or MRI and cerebral angiography.

In addition to the results from the neurological examination, the Glasgow Outcome Score (score of 5, no or minimal impairment; 4, moderate impairment, independent in everyday activities; 3, severe impairment, dependent on help for everyday activities; 2, persistent vegetative state; 1, dead) was used to estimate the functional impairment of the FND group patients.

To further determine the impact of morphological and hemodynamic factors on the development of focal syndromes, we analyzed flow velocities and pressure in feeding arteries, AVM size, drainage pattern, and AVM location. Data from FND and non-FND patients were compared with ² (frequencies) and t test (continuous variables) statistical methods.

Intravascular pressures were measured using methodology previously described.⁸ Feeding mean arterial pressure (FMAP) was measured just proximal to the nidus using an intracranial microcatheter, 1.5F at its distal tip (Chimiotherapie, Balt), immediately before the initial endovascular embolization procedure (cyanoacrylate) in eight patients and immediately before the second embolization procedure in two. In one case, FMAP was measured intraoperatively by direct puncture of a main AVM feeding artery with a 26-gauge needle before resection. The systemic mean arterial pressure either in the extracranial internal carotid or vertebral artery (embolization patients) or in the radial artery (surgical patient) was simultaneously recorded. FMAP in the FND group was compared by unpaired t test to that of a group of non-FND patients who had FMAP measured immediately before either the initial or second endovascular embolization procedure.

A case report is included to illustrate that chronic hypotension does not necessarily result in a loss of neuronal function (assessed by neurobehavorial testing). The patient was trained in several language tasks at the bedside using a computer³¹ ; included were naming, reading aloud, repetition, and fluency.³² Naming consisted of the presentation of pictures derived from the Boston Naming Test³³ ; the patient viewed each picture stimulus in the center of a notebook computer screen (Macintosh Duo 280c) and had 10 seconds to make a response. Single-word stimuli and sentences were presented on the computer screen for the reading-aloud test. Low- and high-frequency words and sentences were presented. Single-word stimuli were taken from the Wide Range Achievement Test.³⁴ Repetition was tested with sentences taken from the repetition subtest of the Boston Diagnostic Aphasia Examination.³⁵ Fluency was assessed by asking the patient to generate as many items in a single class as possible in 1 minute.

Superselective anesthetic injection consisted of sodium amobarbital (30 to 40 mg) followed by lidocaine (15 to 30 mg). The drugs were mixed with contrast and given through the superselective catheter, and an angiogram was obtained of the distribution of the drug/contrast mixture.^{36 37} Functional testing was carried out at baseline and after drug injection.

	Results

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Descriptive data for the total sample are given in Table 2. The frequencies of presenting symptoms and signs other than FNDs in our sample were similar to those reported in the literature (Table 1).^{11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27} Two (1.3%) of 152 patients met the criteria for progressive FND (Table 3). One of them had a cerebellopontine angle AVM with a large venous aneurysm compressing the brain stem. Nonprogressive FNDs were seen in 11 (7.2%) patients (stable in 4.6%, reversible in 2.6%). No FND was discovered after study inclusion. The median observation time period was 17 months (range, 1 to 60 months).

View this table: [in this window] [in a new window]   Table 2. Age, Sex, and Size and Location of Arteriovenous Malformation in 152 Patients

View this table: [in this window] [in a new window]   Table 3. Neurological Deficit, Glasgow Outcome Scale Score, and Size and Location of Arteriovenous Malformations in 13 Patients With Focal Neurological Deficits Unrelated to Hemorrhage

The functional impairment rated by the Glasgow Outcome Scale for the two patients with progressive FNDs was moderate in one case and severe in the other and mild to moderate for patients with stable syndromes (Table 3). AVM size in the 13 FND cases (Table 4) was similar to those in non-FND cases. There was no difference in the presence of deep venous drainage. Transcranial Doppler mean flow velocities in feeding arteries or pulsatility indexes also were similar between FND and non-FND groups.

View this table: [in this window] [in a new window]   Table 4. Physiological Variables

Table 4 shows FMAP and associated data for 10 of the 13 FND patients who underwent intravascular pressure measurements. Compared with patients presenting with symptoms and signs other than FND who also underwent intravascular pressure measurements, FMAPs were similar in the FND and non-FND groups.

Case Report
The patient was a 25-year-old right-handed female journalist with a left temporal AVM who presented with seizures manifested by speech arrest but who was otherwise intact. There was no measurable aphasic disorder on comprehensive neuropsychological evaluation.

To determine the arterial supply to the language area, five vessels were superselectively catheterized. Each vessel was injected with anesthetic (amobarbital followed by lidocaine) with language evaluation before and after each injection. Panels A and B of the Figure show a lateral view of a carotid injection with the studied branches labeled in panel A and the corresponding territories indicated in panel B.

View larger version (154K): [in this window] [in a new window]   Figure 1. Angiograms show results of superselective anesthetic injection (see text for further explanation). Panels A and B show a lateral view of a carotid injection with the studied branches labeled in panel A and the corresponding territories indicated in panel B. An angular-branch superselective injection is shown in panels C and D. Panel C shows the arterial phase of the injection (the small arrow indicates the tip of the catheter and the large arrow the main arterial branch). Panel D shows the capillary stain of the territory. When feeding arteries 1 and 2 to the arteriovenous malformation (AVM) were injected, no neurological deficits were noted. When the frontal opercular ("cand. op."), insular, or angular branches were injected, the patient became aphasic. The angular branch pressure was 25 mm Hg at a systemic mean of 55 mm Hg. Thus, the angular artery territory subserved sensory language function despite a markedly reduced arterial input pressure. CA indicates conduction aphasia; SA, sensory aphasia; and NL, normal (no deficit).

When feeding arteries 1 and 2 to the AVM were injected, no neurological deficits were noted. When the frontal opercular branch (labeled "cand. op." in the Figure) was injected, the patient became mute and developed mild comprehension deficits. When the insular branch was injected, she developed decreased repetition capabilities and paraphasic errors (conduction aphasia); comprehension was intact. When the angular branch was injected, the patient developed a dense sensory (Wernicke's) aphasia. Fluency was intact, but naming and comprehension were markedly impaired. The angular branch pressure was 25 mm Hg at a systemic mean of 55 mm Hg. Thus, we were able to demonstrate that the angular artery territory subserved sensory language function despite a markedly reduced arterial input pressure in a patient who was not aphasic. The angular-branch superselective injection is shown in panels C and D. Panel C shows the arterial phase of the injection (the small arrow indicates the tip of the catheter and the large arrow the main arterial branch). Panel D shows the capillary stain of the territory.

	Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Our results suggest that nonhemorrhagic focal neurological syndromes in AVMs are infrequent. Progressive deficits—a hallmark of the "steal" notion—were especially rare. These findings are at variance with several other reports in the literature.^{11 13} Furthermore, we could not demonstrate a relationship between feeding artery pressure or flow velocities and FND. Finally, we present a case report to illustrate that chronic cerebral hypotension does not necessarily impair higher cognitive function, suggesting an adaptive process.⁸

AVM size was not a strong determinant of FNDs. Flow velocities and intravascular pressure in feeding arteries also had little impact. The latter finding is of particular importance, since some authors^{13 38} have reported that AVMs with clinical features of steal show significantly higher flow velocities than AVMs with other modes of presentation, an observation that seemed to lend support for the concept of "misery perfusion." We were unable, however, to replicate these results with a larger data set. We also found no case histories in the reported samples^{13 38} that permitted an independent assessment of the basis for the diagnosis of progressive deficits.

The lack of clinical and hemodynamic evidence for steal is further supported by results from other reported pathophysiological studies. A positron emission tomography study of 14 AVM patients showed that, although cerebral blood flow in brain tissues surrounding AVMs was low, there was no corresponding increase in parenchymal blood volume. Furthermore, glucose and oxygen extraction fractions were normal.²⁸ This constellation of physiological findings is not predicted on the basis of "misery perfusion," in which there should be an increase in blood volume as well as an increase in substrate extraction fraction.³⁹

There are accumulating data that autoregulation is preserved in cerebral regions adjacent to AVMs.⁸ We have proposed that there is an adaptive leftward shift of the lower limits of the autoregulation flow-pressure curve in hypotensive regions adjacent to AVMs.⁸ Despite chronic hypotension well below a mean cerebral arterial pressure of 50 mm Hg, function remains intact and vasoparalysis in the arteriolar resistance bed does not necessarily occur. Cerebral perfusion pressure below 50 mm Hg has been suggested by several authors to exceed the lower limits of cerebral autoregulation.^{40 41} Reports describing maintained CO₂ responsiveness in AVM patients lend further support to the hypothesis of an intact autoregulatory capacity.⁴²

The question remains: why do some AVM patients present with focal deficits not due to hemorrhage? Mass effects of AVMs in "strategic regions" such as the posterior fossa may explain at least some of the syndromes.⁴³

The inclusion of reversible FNDs in a steal group may be questionable, since a postictal etiology cannot be ruled out completely. However, exclusion of such patients from the analysis further reduces the number of cases with possible steal from 8.6% to 5.9% and has no effect on the results in the comparison of morphological and hemodynamic parameters. Another potential influence on our results could be patient referral bias. Because Columbia–Presbyterian Medical Center is a tertiary referral center, there may be an overrepresentation of AVM cases that are more likely to pose difficult treatment problems, such as staged embolization before surgery. But if there is any bias resulting from this factor, we think it should also produce a higher rather than a lower frequency of cases with focal syndromes. It is also possible that patients initially may have had subclinical signs or symptoms of cerebral ischemia that were masked or overwhelmed by an intracerebral hemorrhage, but this is probably a rare occurrence.

Because most of our patients began a course of staged embolization procedures, the chances of finding progressive deficits during the time following study inclusion may have been reduced. Consequently, we cannot exclude the possibility that patients who presented with a stable or reversible deficit would later have developed a progressive course. However, the reported frequencies in the literature on FNDs largely reflect data from the initial clinical evaluation. Prospective long-term natural-course studies are not available (and may be regarded as ethically problematic, given the current treatment possibilities). The discrepancies between our findings and the high frequencies of FNDs in other samples^{11 13} therefore are not attributable to differences in study design. Small sample sizes and a retrospective design are principle sources of error in clinical studies. To our knowledge, this study addresses the question of focal deficits in the largest prospective sample of AVM patients.

In summary, the low frequency of FNDs not attributable to hemorrhage in AVM patients and the lack of associated hemodynamic derangements argue strongly against an uncritical acceptance of the steal concept.

	Acknowledgments

 
This work was supported by National Institutes of Health grant RO1-NS27713. The authors wish to thank Joyce Ouchi for expert assistance in preparation of the manuscript and the Neuroradiology technologist staff for expert technical assistance. The authors gratefully acknowledge the support and contributions of the other members of the Columbia University AVM study project. The following members of the Columbia University AVM Study Project also participated in this work: I.A. Soussis, PhD; Noeleen Ostapkovich, REPT; Abraham Kader, MD; Tara Jackson, BS; Kristy Z. Baker, MD; Robert R. Sciacca, EngScD; Lofti Hacein-Bey, MD; John DeMeritt, MD; Patricia Fogarty-Mack, MD; Steven M. Marshall, BS; and Dennis Lu, MS.

Received January 13, 1995; revision received April 6, 1995; accepted April 20, 1995.

	References

Top Abstract Introduction Subjects and Methods Results Discussion References

 
1. Wade JPH, Hachinski VC. Cerebral steal: robbery or maldistribution? In: Wood JH, ed. Cerebral Blood Flow: Physiologic and Clinical Aspects. New York, NY: McGraw-Hill Book Co; 1987:chap 30:467-480.

2. Spetzler RF, Martin NA, Carter LP, Flom RA, Raudzens PA, Wilkinson E. Surgical management of large AVM's by staged embolization and operative excision. J Neurosurg. 1987;67:17-28. [Medline] [Order article via Infotrieve]

3. Barnett GH, Little JR, Ebrahim ZY, Jones SC, Friel HT. Cerebral circulation during arteriovenous malformation operation. Neurosurgery. 1987;20:836-842. [Medline] [Order article via Infotrieve]

4. Hassler W, Steinmetz H. Cerebral hemodynamics in angioma patients: an intraoperative study. J Neurosurg. 1987;67:822-831. [Medline] [Order article via Infotrieve]

5. Duckwiler G, Dion J, Vinuela F, Jabour B, Martin N, Bentson J. Intravascular microcatheter pressure monitoring: experimental results and early clinical evaluation. AJNR. 1990;11:169-175. [Abstract]

6. Jungreis CA, Horton JA, Hecht ST. Blood pressure changes in feeders to cerebral arteriovenous malformations during therapeutic embolization. AJNR. 1989;10:575-578. [Abstract]

7. Young WL, Kader A, Pile-Spellman J, Ornstein E, Stein BM, Columbia University AVM Study Project. Arteriovenous malformation draining vein physiology and determinants of transnidal pressure gradients. Neurosurgery. 1994;35:389-396.[Medline] [Order article via Infotrieve]

8. Young WL, Pile-Spellman J, Prohovnik I, Kader A, Stein BM, Columbia University AVM Study Project. Evidence for adaptive autoregulatory displacement in hypotensive cortical territories adjacent to arteriovenous malformations. Neurosurgery. 1994;34:601-611. [Medline] [Order article via Infotrieve]

9. Fleischer LH, Young WL, Pile-Spellman J, terPenning B, Kader A, Stein BM, Mohr JP. Relationship of transcranial Doppler flow velocities and arteriovenous malformation feeding artery pressures. Stroke. 1993;24:1897-1902. [Abstract/Free Full Text]

10. Luessenhop AJ. Natural history of cerebral arteriovenous malformations. In: Wilson CB, Stein BM, eds. Intracranial Arteriovenous Malformations. Baltimore, Md: Williams & Wilkins Co; 1984:12-23.

11. Diehl RR, Henkes H, Nahser H-C, Kuhne D, Berlit P. Blood flow velocity and vasomotor reactivity in patients with arteriovenous malformations. Stroke. 1994;25:1574-1580. [Abstract]

12. Norbash AM, Marks MP, Lane B. Correlation of pressure measurements with angiographic characteristics predisposing to hemorrhage and steal in cerebral arteriovenous malformations. Am J Neuroradiol. 1994;15:809-813. [Abstract]

13. Manchola IF, De Salles AAF, Foo TK, Ackerman RH, Candia GT, Kjellberg RN. Arteriovenous malformation hemodynamics: a transcranial Doppler study. Neurosurgery. 1993;33:556-562. [Medline] [Order article via Infotrieve]

14. Redekop GJ, Elisevich KV, Gaspar LE, Wiese KP, Drake CG. Conventional radiation therapy of intracranial arteriovenous malformations: long-term results. J Neurosurg. 1993;78:413-422. [Medline] [Order article via Infotrieve]

15. Lunsford LD, Kondziolka D, Flickinger JC, Bissonette DJ, Jungreis CA, Maitz AH, Horton JA, Coffey RJ. Stereotactic radiosurgery for arteriovenous malformations of the brain. J Neurosurg. 1991;75:512-524. [Medline] [Order article via Infotrieve]

16. Marks MP, Lane B, Steinberg G, Chang P. Vascular characteristics of intracerebral arteriovenous malformations in patients with clinical steal. AJNR. 1991;12:489-496. [Abstract]

17. Albert P, Salgado H, Polaina M, Trujillo F, Ponce de Leon A, Durand F. A study on the venous drainage of 150 cerebral arteriovenous malformations as related to haemorrhagic risks and size of the lesion. Acta Neurochir (Wien). 1990;103:30-34. [Medline] [Order article via Infotrieve]

18. Graf CJ, Perret GE, Torner JC. Bleeding from cerebral arteriovenous malformations as part of their natural history. J Neurosurg. 1983;58:331-337. [Medline] [Order article via Infotrieve]

19. Waltimo O. The relationship of size, density and localization of intracranial arteriovenous malformations to the type of initial symptom. J Neurol Sci. 1973;19:13-19. [Medline] [Order article via Infotrieve]

20. Forster DMC, Steiner L, Hakanson S. Arteriovenous malformations of the brain: a long-term clinical study. J Neurosurg. 1972;37:562-570. [Medline] [Order article via Infotrieve]

21. Troupp H, Marttila I, Halonen V. Arteriovenous malformations of the brain: prognosis without operation. Acta Neurochir (Wien). 1970;22:125-128. [Medline] [Order article via Infotrieve]

22. Henderson WR, Gomez R de RL. Natural history of cerebral angiomas. Br Med J. 1967;4:571-574.

23. 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. 1966;25:467-490. [Medline] [Order article via Infotrieve]

24. Hook O, Johanson C. Intracranial arteriovenous aneurysms: a follow-up study with particular attention to their growth. AMA Archives of Neurology and Psychiatry. 1958;80:39-54.

25. Tonnis W, Schiefer W, Walter W. Signs and symptoms of supratentorial arteriovenous aneurysms. J Neurosurg. 1958;15:471-480. [Medline] [Order article via Infotrieve]

26. Potter JM, Chir B. Angiomatous malformations of the brain: their nature and prognosis (Hunterian Lecture delivered at the Royal College of Surgeons of England on 6th January 1955). Ann R Coll Surg Engl. 1955;16:227-243. [Medline] [Order article via Infotrieve]

27. Mackenzie I. The clinical presentation of the cerebral angioma: a review of 50 cases. Brain. 1953;76:184-214. [Free Full Text]

28. Fink GR. Effects of cerebral angiomas on perifocal and remote tissue: a multivariate positron emission tomography study. Stroke. 1992;23:1099-1105. [Abstract/Free Full Text]

29. Kittner SJ, Sharkness CM, Sloan MA, Price TR, Dambrosia JM, Tuhrim S, Wolf PA, Mohr JP, Hier DB. Features on initial computed tomography scan of infarcts with a cardiac source of embolism in the NINDS Stroke Data Bank. Stroke. 1992;23:1748-1751. [Abstract/Free Full Text]

30. Massaro A, Sacco RL, Mohr JP, Foulkes MA, Tatemichi TK, Price TR, Hier DB, Wolf PA. Clinical discriminators of lobar and deep hemorrhages: the Stroke Data Bank. Neurology. 1991;41:1881-1885. [Abstract/Free Full Text]

31. Lazar RM, Binder JR, Benjamin JL, Mohr JP. The measurement of hemineglect in aphasic patients. Neurology. 1992;42(suppl 3):222. Abstract.

32. Lazar RM, Marshall RS, Mohr JP. Aphasia in stroke. In: Bougouslavsky J, Caplan L, eds. Stroke Syndromes. Cambridge, England: Cambridge University Press. In press.

33. Kaplan E, Goodglass H, Weintraub S. Boston Naming Test. Philadelphia, Pa: Lea and Febiger; 1983.

34. Jastak E, Wikinson GS. The Wide Range Achievement Test—Revised Administration Manual. Wilmington, Del: Jastak Assessment Systems; 1984.

35. Goodglass H, Kaplan E. The Assessment of Aphasia and Related Diseases, 2nd ed. Phildelphia, Pa: Lea & Febiger; 1983.

36. Young WL, Pile-Spellman J. Anesthetic considerations for interventional neuroradiology. Anesthesiology. 1994;80:427-456. [Medline] [Order article via Infotrieve]

37. Purdy PD, Batjer HH, Samson D, Risser RC, Bowman GW. Intraarterial sodium amytal administration to guide preoperative embolization of cerebral arteriovenous malformations. J Neurosurg Anesth. 1991;3:103-106.

38. Lindegaard K-F, Grolimund P, Aaslid R, Nornes H. Evaluation of cerebral AVM's using transcranial Doppler ultrasound. J Neurosurg. 1986;65:335-344. [Medline] [Order article via Infotrieve]

39. Powers WJ, Raichle ME. Positron emission tomography and its application to the study of cerebrovascular disease in man. Stroke. 1985;16:361-376. [Free Full Text]

40. Spetzler RF, Wilson CB, Weinstein P, Mehdorn M, Townsend J, Telles D. Normal perfusion pressure breakthrough theory. Clin Neurosurg. 1978;25:651-672. [Medline] [Order article via Infotrieve]

41. Nornes H, Grip A. Hemodynamic aspects of cerebral arteriovenous malformations. J Neurosurg. 1980;53:456-464. [Medline] [Order article via Infotrieve]

42. Young WL, Prohovnik I, Ornstein E, Ostapkovich N, Sisti MB, Solomon RA, Stein BM. The effect of arteriovenous malformation resection on cerebrovascular reactivity to carbon dioxide. Neurosurgery. 1990;27:257-267. [Medline] [Order article via Infotrieve]

43. Kumar AJ, Fox AJ, Vinuela F, Rosenbaum AE. Revisited old and new CT findings in unruptured larger arteriovenous malformations of the brain. J Comput Assist Tomogr. 1984;8:648-655.[Medline] [Order article via Infotrieve]

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				The Arteriovenous Malformation Study Group Arteriovenous Malformations of the Brain in Adults N. Engl. J. Med., June 10, 1999; 340(23): 1812 - 1818. [Full Text] [PDF]

				R. M. Lazar, K. Connaire, R. S. Marshall, J. Pile-Spellman, L. Hacein-Bey, R. A. Solomon, M. B. Sisti, W. L. Young, and J. P. Mohr Developmental Deficits in Adult Patients With Arteriovenous Malformations Arch Neurol, January 1, 1999; 56(1): 103 - 106. [Abstract] [Full Text] [PDF]

				D. H. Duong, W. L. Young, M. C. Vang, R. R. Sciacca, H. Mast, H.-C. Koennecke, A. Hartmann, S. Joshi, J. P. Mohr, and J. Pile-Spellman Feeding Artery Pressure and Venous Drainage Pattern Are Primary Determinants of Hemorrhage From Cerebral Arteriovenous Malformations Stroke, June 1, 1998; 29(6): 1167 - 1176. [Abstract] [Full Text] [PDF]

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