Redefined role of angiogenesis in the pathogenesis of dural arteriovenous malformations

Michael T. LawtonDivision of Neurological Surgery, Barrow Neurological Institute, St. Joseph's Hospital and Medical Center, Phoenix, Arizona; and Department of Mathematics, Arizona State University, Tempe, Arizona

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Ronald JacobowitzDivision of Neurological Surgery, Barrow Neurological Institute, St. Joseph's Hospital and Medical Center, Phoenix, Arizona; and Department of Mathematics, Arizona State University, Tempe, Arizona

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Robert F. SpetzlerDivision of Neurological Surgery, Barrow Neurological Institute, St. Joseph's Hospital and Medical Center, Phoenix, Arizona; and Department of Mathematics, Arizona State University, Tempe, Arizona

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Volume 87: Issue 2
DOI link:
https://doi.org/10.3171/jns.1997.87.2.0267
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✓ To investigate the role of angiogenesis in the pathogenesis of dural arteriovenous malformations (AVMs), 40 rats underwent common carotid artery—external jugular vein (CCA-EJV) anastomosis, bipolar coagulation of the vein draining the transverse sinus, and sagittal sinus thrombosis to induce venous hypertension. Fifteen rats underwent a similar surgical procedure, but venous hypertension was not induced. The 55 rats were divided into seven groups. Four groups, each containing 10 rats, underwent induced venous hypertension. The other three groups, each containing five rats, did not undergo induced venous hypertension. After 1, 2, or 3 weeks, dura mater was obtained from one group of hypertensive rats and from one group of nonhypertensive rats and was assayed for angiogenic activity (rabbit cornea bioassay). The remaining group of 10 hypertensive rats was not assayed to determine if sampling affected dural AVM formation. Unlike rats without CCA-EJV anastomosis, rats with CCA-EJV anastomosis had significantly increased postoperative sagittal sinus pressures (p < 0.0001). Mean angiogenesis indices were significantly greater in rats with venous hypertension than in rats without venous hypertension (p = 0.004). Dural AVMs formed in 42% of the 55 rats and facial AVMs formed in 51%. Angiogenic activity correlated positively with venous hypertension (ρ = 0.74). Development of dural AVMs correlated positively with both venous hypertension (p = 0.0009) and angiogenic activity (p = 0.04). These data indicate that venous hypertension may induce angiogenic activity either directly or indirectly by decreasing cerebral perfusion and increasing ischemia, and that dural AVM formation may be the result of aberrant angiogenesis.

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Address reprint requests to: Robert F. Spetzler, M.D., Neuroscience Publications, Barrow Neurological Institute, 350 West Thomas Road, Phoenix, Arizona 85013–4496. email: neuropub@mha.chw.edu.
  • 1.

    Aiello LP, , Northrup JM, & Keyt BA, et al: Hypoxic regulation of vascular endothelial growth factor in retinal cells. Arch Ophthalmol 113:1538–1544, 1995 Aiello LP, Northrup JM, Keyt BA, et al: Hypoxic regulation of vascular endothelial growth factor in retinal cells. Arch Ophthalmol 113:1538–1544, 1995

    • Search Google Scholar
    • Export Citation
  • 2.

    Aminoff MJ: Vascular anomalies in the intracranial dura mater. Brain 96:601–612, 1973 Aminoff MJ: Vascular anomalies in the intracranial dura mater. Brain 96:601–612, 1973

    • Search Google Scholar
    • Export Citation
  • 3.

    Awad IA, & Barrow DL: Conceptual overview and management strategies, in Awad IA, & Barrow DL (eds): Dural Arteriovenous Malformations. Park Ridge, Ill: American Association of Neurological Surgeons, 1993, pp 231–241 Awad IA, Barrow DL: Conceptual overview and management strategies, in Awad IA, Barrow DL (eds): Dural Arteriovenous Malformations. Park Ridge, Ill: American Association of Neurological Surgeons, 1993, pp 231–241

    • Search Google Scholar
    • Export Citation
  • 4.

    Awad IA, , Little JR, & Akrawi WP, et al: Intracranial dural arteriovenous malformations: factors predisposing to an aggressive neurological course. J Neurosurg 72:839–850, 1990 Awad IA, Little JR, Akrawi WP, et al: Intracranial dural arteriovenous malformations: factors predisposing to an aggressive neurological course. J Neurosurg 72:839–850, 1990

    • Search Google Scholar
    • Export Citation
  • 5.

    Bederson JB: Pathophysiology and animal models of dural arteriovenous malformations, in Awad IA, & Barrow DL (eds): Dural Arteriovenous Malformations. Park Ridge, Ill: American Association of Neurological Surgeons, 1993, pp 23–33 Bederson JB: Pathophysiology and animal models of dural arteriovenous malformations, in Awad IA, Barrow DL (eds): Dural Arteriovenous Malformations. Park Ridge, Ill: American Association of Neurological Surgeons, 1993, pp 23–33

    • Search Google Scholar
    • Export Citation
  • 6.

    Bederson JB, , Wiestler OD, & Brüstle O, et al: Intracranial venous hypertension and the effects of venous outflow occlusion in a rat model of arteriovenous fistula. Neurosurgery 29:341–350, 1991 Bederson JB, Wiestler OD, Brüstle O, et al: Intracranial venous hypertension and the effects of venous outflow occlusion in a rat model of arteriovenous fistula. Neurosurgery 29:341–350, 1991

    • Search Google Scholar
    • Export Citation
  • 7.

    Borden JA, , Wu JK, & Shucart WA: A proposed classification for spinal and cranial dural arteriovenous fistulous malformations and implications for treatment. J Neurosurg 82:166–179, 1995 Borden JA, Wu JK, Shucart WA: A proposed classification for spinal and cranial dural arteriovenous fistulous malformations and implications for treatment. J Neurosurg 82:166–179, 1995

    • Search Google Scholar
    • Export Citation
  • 8.

    Chaudhary MY, , Sachdev VP, & Cho SH, et al: Dural arteriovenous malformation of the major venous sinuses: an acquired lesion. AJNR 3:13–19, 1982 Chaudhary MY, Sachdev VP, Cho SH, et al: Dural arteriovenous malformation of the major venous sinuses: an acquired lesion. AJNR 3:13–19, 1982

    • Search Google Scholar
    • Export Citation
  • 9.

    Conn G, , Bayne ML, & Soderman DD, et al: Amino acid and cDNA sequences of a vascular endothelial cell mitogen that is homologous to platelet-derived growth factor. Proc Natl Acad Sci USA 87:2628–2632, 1990 Conn G, Bayne ML, Soderman DD, et al: Amino acid and cDNA sequences of a vascular endothelial cell mitogen that is homologous to platelet-derived growth factor. Proc Natl Acad Sci USA 87:2628–2632, 1990

    • Search Google Scholar
    • Export Citation
  • 10.

    Conn G, , Soderman DD, & Schaeffer MT, et al: Purification of a glycoprotein vascular endothelial cell mitogen from a rat glioma-derived cell line. Proc Natl Acad Sci USA 87:1323–1327, 1990 Conn G, Soderman DD, Schaeffer MT, et al: Purification of a glycoprotein vascular endothelial cell mitogen from a rat glioma-derived cell line. Proc Natl Acad Sci USA 87:1323–1327, 1990

    • Search Google Scholar
    • Export Citation
  • 11.

    D'Amore PA, & Thompson RW: Mechanisms of angiogenesis. Annu Rev Physiol 49:453–464, 1987 D'Amore PA, Thompson RW: Mechanisms of angiogenesis. Annu Rev Physiol 49:453–464, 1987

    • Search Google Scholar
    • Export Citation
  • 12.

    Dion J: Dural arteriovenous malformations: definition, classification, and diagnostic imaging, in Awad IA, & Barrow DL (eds): Dural Arteriovenous Malformations. Park Ridge, Ill: American Association of Neurolgoical Surgeons, 1993, pp 1–21 Dion J: Dural arteriovenous malformations: definition, classification, and diagnostic imaging, in Awad IA, Barrow DL (eds): Dural Arteriovenous Malformations. Park Ridge, Ill: American Association of Neurolgoical Surgeons, 1993, pp 1–21

    • Search Google Scholar
    • Export Citation
  • 13.

    Djindjian R, & Merland JJ: Super-Selective Arteriography of the External Carotid Artery. New York: Springer-Verlag, 1978, pp 34–35, 405–412 Djindjian R, Merland JJ: Super-Selective Arteriography of the External Carotid Artery. New York: Springer-Verlag, 1978, pp 34–35, 405–412

    • Search Google Scholar
    • Export Citation
  • 14.

    Folkman J: How is blood vessel growth regulated in normal and neoplastic tissue?—G.H.A. Clowes Memorial Award Lecture. Cancer Res 46:467–473, 1986 Folkman J: How is blood vessel growth regulated in normal and neoplastic tissue?—G.H.A. Clowes Memorial Award Lecture. Cancer Res 46:467–473, 1986

    • Search Google Scholar
    • Export Citation
  • 15.

    Folkman J: Successful treatment of an angiogenic disease. N Engl J Med 320:1211–1212, 1989 Folkman J: Successful treatment of an angiogenic disease. N Engl J Med 320:1211–1212, 1989

    • Search Google Scholar
    • Export Citation
  • 16.

    Folkman J: Tumor angiogenesis, in Mendelsohn J, , Howley PM, & Israel MA, et al (eds): The Molecular Basis of Cancer. Philadelphia: WB Saunders, 1995, pp 206–232 Folkman J: Tumor angiogenesis, in Mendelsohn J, Howley PM, Israel MA, et al (eds): The Molecular Basis of Cancer. Philadelphia: WB Saunders, 1995, pp 206–232

    • Search Google Scholar
    • Export Citation
  • 17.

    Folkman J, & Klagsbrun M: Angiogenic factors. Science 235:442–447, 1987 Folkman J, Klagsbrun M: Angiogenic factors. Science 235:442–447, 1987

    • Search Google Scholar
    • Export Citation
  • 18.

    Folkman J, & Klagsbrun M: A family of angiogenic peptides. Nature 329:671–672, 1987 Folkman J, Klagsbrun M: A family of angiogenic peptides. Nature 329:671–672, 1987

    • Search Google Scholar
    • Export Citation
  • 19.

    Gimbrone MA Jr, , Cotran RS, & Leapman SB, et al: Tumor growth and neovascularization: an experimental model using the rabbit cornea. J Natl Cancer Inst 52:413–427, 1974 Gimbrone MA Jr, Cotran RS, Leapman SB, et al: Tumor growth and neovascularization: an experimental model using the rabbit cornea. J Natl Cancer Inst 52:413–427, 1974

    • Search Google Scholar
    • Export Citation
  • 20.

    Goldberg MA, & Schneider TJ: Similarities between the oxygensensing mechanisms regulating the expression of vascular endothelial growth factor and erythropoietin. J Biol Chem 269:4355–4359, 1994 Goldberg MA, Schneider TJ: Similarities between the oxygensensing mechanisms regulating the expression of vascular endothelial growth factor and erythropoietin. J Biol Chem 269:4355–4359, 1994

    • Search Google Scholar
    • Export Citation
  • 21.

    Graeb DA, & Dolman CL: Radiological and pathological aspects of dural arteriovenous fistulas. Case report. J Neurosurg 64:962–967, 1986 Graeb DA, Dolman CL: Radiological and pathological aspects of dural arteriovenous fistulas. Case report. J Neurosurg 64:962–967, 1986

    • Search Google Scholar
    • Export Citation
  • 22.

    Greene EC: Anatomy of the Rat. New York: Hafner, 1959 Greene EC: Anatomy of the Rat. New York: Hafner, 1959

  • 23.

    Hashimoto E, , Ogita T, & Nakaoka T, et al: Rapid induction of vascular endothelial growth factor expression by transient ischemia in rat heart. Am J Physiol 267:H1948–H1954, 1994 Hashimoto E, Ogita T, Nakaoka T, et al: Rapid induction of vascular endothelial growth factor expression by transient ischemia in rat heart. Am J Physiol 267:H1948–H1954, 1994

    • Search Google Scholar
    • Export Citation
  • 24.

    Herman JM, , Spetzler RF, & Bederson JB, et al: Genesis of a dural arteriovenous malformation in a rat model. J Neurosurg 83:539–545, 1995 Herman JM, Spetzler RF, Bederson JB, et al: Genesis of a dural arteriovenous malformation in a rat model. J Neurosurg 83:539–545, 1995

    • Search Google Scholar
    • Export Citation
  • 25.

    Hlatky L, , Tsionou C, & Hahnfeldt P, et al: Mammary fibroblasts may influence breast tumor angiogenesis via hypoxia-induced vascular endothelial growth factor up-regulation and protein expression. Cancer Res 54:6083–6086, 1994 Hlatky L, Tsionou C, Hahnfeldt P, et al: Mammary fibroblasts may influence breast tumor angiogenesis via hypoxia-induced vascular endothelial growth factor up-regulation and protein expression. Cancer Res 54:6083–6086, 1994

    • Search Google Scholar
    • Export Citation
  • 26.

    Houser OW, , Campbell JK, & Campbell RJ, et al: Arteriovenous malformation affecting the transverse dural venous sinus—an acquired lesion. Mayo Clin Proc 54:651–661, 1979 Houser OW, Campbell JK, Campbell RJ, et al: Arteriovenous malformation affecting the transverse dural venous sinus—an acquired lesion. Mayo Clin Proc 54:651–661, 1979

    • Search Google Scholar
    • Export Citation
  • 27.

    Hurst RW, , Hackney DB, & Goldberg HI, et al: Reversible arteriovenous malformation-induced venous hypertension as a cause of neurological deficits. Neurosurgery 30:422–425, 1992 Hurst RW, Hackney DB, Goldberg HI, et al: Reversible arteriovenous malformation-induced venous hypertension as a cause of neurological deficits. Neurosurgery 30:422–425, 1992

    • Search Google Scholar
    • Export Citation
  • 28.

    Ikeda E, , Achen MG, & Breier G, et al: Hypoxia-induced transcriptional activation and increased mRNA stability of vascular endothelial growth factor in C6 glioma cells. J Biol Chem 270:19761–19766, 1995 Ikeda E, Achen MG, Breier G, et al: Hypoxia-induced transcriptional activation and increased mRNA stability of vascular endothelial growth factor in C6 glioma cells. J Biol Chem 270:19761–19766, 1995

    • Search Google Scholar
    • Export Citation
  • 29.

    Ito M, , Sonokawa T, & Mishina H, et al: Reversible dural arteriovenous malformation-induced venous ischemia as a cause of dementia: treatment by surgical occlusion of draining dural sinus: case report. Neurosurgery 37:1187–1192, 1995 Ito M, Sonokawa T, Mishina H, et al: Reversible dural arteriovenous malformation-induced venous ischemia as a cause of dementia: treatment by surgical occlusion of draining dural sinus: case report. Neurosurgery 37:1187–1192, 1995

    • Search Google Scholar
    • Export Citation
  • 30.

    Jakeman LB, , Winer J, & Bennett GL, et al: Binding sites for vascular endothelial growth factor are localized on endothelial cells in adult rat tissues. J Clin Invest 89:244–253, 1992 Jakeman LB, Winer J, Bennett GL, et al: Binding sites for vascular endothelial growth factor are localized on endothelial cells in adult rat tissues. J Clin Invest 89:244–253, 1992

    • Search Google Scholar
    • Export Citation
  • 31.

    Kalbag RM, & Woolf AL: Cerebral Venous Thrombosis, With Special Reference to Primary Aseptic Thrombosis. London: Oxford University Press, 1967 Kalbag RM, Woolf AL: Cerebral Venous Thrombosis, With Special Reference to Primary Aseptic Thrombosis. London: Oxford University Press, 1967

    • Search Google Scholar
    • Export Citation
  • 32.

    Kerber CW, & Newton TH: The macro and microvasculature of the dura mater. Neuroradiology 6:175–179, 1973 Kerber CW, Newton TH: The macro and microvasculature of the dura mater. Neuroradiology 6:175–179, 1973

    • Search Google Scholar
    • Export Citation
  • 33.

    Klagsbrun M, & D'Amore PA: Regulators of angiogenesis. Annu Rev Physiol 53:217–239, 1991 Klagsbrun M, D'Amore PA: Regulators of angiogenesis. Annu Rev Physiol 53:217–239, 1991

    • Search Google Scholar
    • Export Citation
  • 34.

    Kurata A, , Miyasaka Y, & Yoshida T, et al: Venous ischemia caused by dural arteriovenous malformation. Case report. J Neurosurg 80:552–555, 1994 Kurata A, Miyasaka Y, Yoshida T, et al: Venous ischemia caused by dural arteriovenous malformation. Case report. J Neurosurg 80:552–555, 1994

    • Search Google Scholar
    • Export Citation
  • 35.

    Ladoux A, & Frelin C: Expression of vascular endothelial growth factor by cultured endothelial cells from brain microvessels. Biochem Biophys Res Commun 194:799–803, 1993 Ladoux A, Frelin C: Expression of vascular endothelial growth factor by cultured endothelial cells from brain microvessels. Biochem Biophys Res Commun 194:799–803, 1993

    • Search Google Scholar
    • Export Citation
  • 36.

    Ladoux A, & Frelin C: Hypoxia is a strong inducer of vascular endothelial growth factor mRNA expression in the heart. Biochem Biophys Res Commun 195:1005–1010, 1993 Ladoux A, Frelin C: Hypoxia is a strong inducer of vascular endothelial growth factor mRNA expression in the heart. Biochem Biophys Res Commun 195:1005–1010, 1993

    • Search Google Scholar
    • Export Citation
  • 37.

    Lasjaunias P, & Berenstein A: Surgical Neuroangiography. Vol 2: Endovascular Treatment of Craniofacial Lesions. Berlin: Springer-Verlag, 1987, pp 273–315 Lasjaunias P, Berenstein A: Surgical Neuroangiography. Vol 2: Endovascular Treatment of Craniofacial Lesions. Berlin: Springer-Verlag, 1987, pp 273–315

    • Search Google Scholar
    • Export Citation
  • 38.

    Lasjaunias P, , Chiu M, & Ter Brugge K, et al: Neurological manifestations of intracranial dural arteriovenous malformations. J Neurosurg 64:724–730, 1986 Lasjaunias P, Chiu M, Ter Brugge K, et al: Neurological manifestations of intracranial dural arteriovenous malformations. J Neurosurg 64:724–730, 1986

    • Search Google Scholar
    • Export Citation
  • 39.

    Lasjaunias P, , Lopez-Ibor L, & Abanou A, et al: Radiological anatomy of the vascularization of cranial dural arteriovenous malformations. Anat Clin 6:87–99, 1984 Lasjaunias P, Lopez-Ibor L, Abanou A, et al: Radiological anatomy of the vascularization of cranial dural arteriovenous malformations. Anat Clin 6:87–99, 1984

    • Search Google Scholar
    • Export Citation
  • 40.

    Lawton MT, , Shetter AG, & Shapiro W, et al: Angiogenesis factors and their clinical applications. BNI Quarterly 9:46–54, 1993 Lawton MT, Shetter AG, Shapiro W, et al: Angiogenesis factors and their clinical applications. BNI Quarterly 9:46–54, 1993

    • Search Google Scholar
    • Export Citation
  • 41.

    Leung DW, , Cachianes G, & Kuang WJ, et al: Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 246:1306–1312, 1989 Leung DW, Cachianes G, Kuang WJ, et al: Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 246:1306–1312, 1989

    • Search Google Scholar
    • Export Citation
  • 42.

    Levy AP, , Levy NS, & Wegner S, et al: Transcriptional regulation of the rat vascular endothelial growth factor gene by hypoxia. J Biol Chem 270:13333–13340, 1995 Levy AP, Levy NS, Wegner S, et al: Transcriptional regulation of the rat vascular endothelial growth factor gene by hypoxia. J Biol Chem 270:13333–13340, 1995

    • Search Google Scholar
    • Export Citation
  • 43.

    MacKenzie ET, , Strandgaard S, & Graham DI, et al: Effects of acutely induced hypertension in cats on pial arteriolar caliber, local cerebral blood flow, and the blood-brain barrier. Circ Res 39:33–41, 1976 MacKenzie ET, Strandgaard S, Graham DI, et al: Effects of acutely induced hypertension in cats on pial arteriolar caliber, local cerebral blood flow, and the blood-brain barrier. Circ Res 39:33–41, 1976

    • Search Google Scholar
    • Export Citation
  • 44.

    Malik GM, , Pearce JE, & Ausman JI, et al: Dural arteriovenous malformations and intracranial hemorrhage. Neurosurgery 15:332–339, 1984 Malik GM, Pearce JE, Ausman JI, et al: Dural arteriovenous malformations and intracranial hemorrhage. Neurosurgery 15:332–339, 1984

    • Search Google Scholar
    • Export Citation
  • 45.

    Minchenko A, , Bauer T, & Salceda S, et al: Hypoxic stimulation of vascular endothelial growth factor expression in vitro and in vivo. Lab Invest 71:374–379, 1994 Minchenko A, Bauer T, Salceda S, et al: Hypoxic stimulation of vascular endothelial growth factor expression in vitro and in vivo. Lab Invest 71:374–379, 1994

    • Search Google Scholar
    • Export Citation
  • 46.

    Monacci WT, , Merrill MJ, & Oldfield EH: Expression of vascular permeability factor/vascular endothelial growth factor in normal rat tissues. Am J Physiol 264:C995–C1002, 1993 Monacci WT, Merrill MJ, Oldfield EH: Expression of vascular permeability factor/vascular endothelial growth factor in normal rat tissues. Am J Physiol 264:C995–C1002, 1993

    • Search Google Scholar
    • Export Citation
  • 47.

    Morcos JJ, & Heros RC: Supratentorial arteriovenous malformations, in Carter LP, , Spetzler RF, & Hamilton MG (eds): Neurovascular Surgery. New York: McGraw-Hill, 1995, pp 979–1004 Morcos JJ, Heros RC: Supratentorial arteriovenous malformations, in Carter LP, Spetzler RF, Hamilton MG (eds): Neurovascular Surgery. New York: McGraw-Hill, 1995, pp 979–1004

    • Search Google Scholar
    • Export Citation
  • 48.

    Namiki A, , Brogi E, & Kearney M, et al: Hypoxia induces vascular endothelial growth factor in cultured human endothelial cells. J Biol Chem 270:31189–31195, 1995 Namiki A, Brogi E, Kearney M, et al: Hypoxia induces vascular endothelial growth factor in cultured human endothelial cells. J Biol Chem 270:31189–31195, 1995

    • Search Google Scholar
    • Export Citation
  • 49.

    Nishijima M, , Takaku A, & Endo S, et al: Etiological evaluation of dural arteriovenous malformations of the lateral and sigmoid sinuses based on histopathological examinations. J Neurosurg 76:600–606, 1992 Nishijima M, Takaku A, Endo S, et al: Etiological evaluation of dural arteriovenous malformations of the lateral and sigmoid sinuses based on histopathological examinations. J Neurosurg 76:600–606, 1992

    • Search Google Scholar
    • Export Citation
  • 50.

    Nomura M, , Yamagishi S, & Harada S, et al: Possible participation of autocrine and paracrine vascular endothelial growth factors in hypoxia-induced proliferation of endothelial cells and pericytes. J Biol Chem 270:28316–28324, 1995 Nomura M, Yamagishi S, Harada S, et al: Possible participation of autocrine and paracrine vascular endothelial growth factors in hypoxia-induced proliferation of endothelial cells and pericytes. J Biol Chem 270:28316–28324, 1995

    • Search Google Scholar
    • Export Citation
  • 51.

    Piton J, , Guilleux MH, & Guibert-Tranier F, et al: Fistulae of the lateral sinus. J Neuroradiol 11:143–159, 1984 Piton J, Guilleux MH, Guibert-Tranier F, et al: Fistulae of the lateral sinus. J Neuroradiol 11:143–159, 1984

    • Search Google Scholar
    • Export Citation
  • 52.

    Plate KH, , Breier G, & Millauer B, et al: Up-regulation of vascular endothelial growth factor and its cognate receptors in a rat glioma model of tumor angiogenesis. Cancer Res 53:5822–5827, 1993 Plate KH, Breier G, Millauer B, et al: Up-regulation of vascular endothelial growth factor and its cognate receptors in a rat glioma model of tumor angiogenesis. Cancer Res 53:5822–5827, 1993

    • Search Google Scholar
    • Export Citation
  • 53.

    Rekate HL: Circuit diagram of the circulation of cerebrospinal fluid. Pediatr Neurosurg 21:248–253, 1994 Rekate HL: Circuit diagram of the circulation of cerebrospinal fluid. Pediatr Neurosurg 21:248–253, 1994

    • Search Google Scholar
    • Export Citation
  • 54.

    Rekate HL, , Brodkey JA, & Chizeck HJ, et al: Ventricular volume regulation: a mathematical model and computer simulation. Pediatr Neurosci 14:77–84, 1988 Rekate HL, Brodkey JA, Chizeck HJ, et al: Ventricular volume regulation: a mathematical model and computer simulation. Pediatr Neurosci 14:77–84, 1988

    • Search Google Scholar
    • Export Citation
  • 55.

    Rowbotham GF, & Little E: Circulations of the cerebral hemispheres. Br J Surg 52:8–21, 1965 Rowbotham GF, Little E: Circulations of the cerebral hemispheres. Br J Surg 52:8–21, 1965

    • Search Google Scholar
    • Export Citation
  • 56.

    Shweiki D, , Itin A, & Soffer D, et al: Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 359:843–845, 1992 Shweiki D, Itin A, Soffer D, et al: Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 359:843–845, 1992

    • Search Google Scholar
    • Export Citation
  • 57.

    Shweiki D, , Neeman M, & Itin A, et al: Induction of vascular endothelial growth factor expression by hypoxia and by glucose deficiency in multicell spheroids: implications for tumor angiogenesis. Proc Natl Acad Sci USA 92:768–772, 1995 Shweiki D, Neeman M, Itin A, et al: Induction of vascular endothelial growth factor expression by hypoxia and by glucose deficiency in multicell spheroids: implications for tumor angiogenesis. Proc Natl Acad Sci USA 92:768–772, 1995

    • Search Google Scholar
    • Export Citation
  • 58.

    Spetzler RF, , Daspit CP, & Pappas CTE: The combined supra- and infratentorial approach for lesions of the petrous and clival regions: experience with 46 cases. J Neurosurg 76:588–599, 1992 Spetzler RF, Daspit CP, Pappas CTE: The combined supra- and infratentorial approach for lesions of the petrous and clival regions: experience with 46 cases. J Neurosurg 76:588–599, 1992

    • Search Google Scholar
    • Export Citation
  • 59.

    Spetzler RF, , Wilson CB, & Weinstein P, et al: Normal perfusion pressure breakthrough theory. Clin Neurosurg 25:651–672, 1978 Spetzler RF, Wilson CB, Weinstein P, et al: Normal perfusion pressure breakthrough theory. Clin Neurosurg 25:651–672, 1978

    • Search Google Scholar
    • Export Citation
  • 60.

    Stein I, , Neeman M, & Shweiki D, et al: Stabilization of vascular endothelial growth factor mRNA by hypoxia and hypoglycemia and coregulation with other ischemia-induced genes. Mol Cell Biol 15:5363–5368, 1995 Stein I, Neeman M, Shweiki D, et al: Stabilization of vascular endothelial growth factor mRNA by hypoxia and hypoglycemia and coregulation with other ischemia-induced genes. Mol Cell Biol 15:5363–5368, 1995

    • Search Google Scholar
    • Export Citation
  • 61.

    Strandgaard S, , Olesen J, & Skinhøj E, et al: Autoregulation in brain circulation in severe arterial hypertension. Br Med J 1:507–510, 1973 Strandgaard S, Olesen J, Skinhøj E, et al: Autoregulation in brain circulation in severe arterial hypertension. Br Med J 1:507–510, 1973

    • Search Google Scholar
    • Export Citation
  • 62.

    Sundt TM Jr, & Piepgras DG: The surgical approach to arteriovenous malformations of the lateral and sigmoid dural sinuses. J Neurosurg 59:32–39, 1983 Sundt TM Jr, Piepgras DG: The surgical approach to arteriovenous malformations of the lateral and sigmoid dural sinuses. J Neurosurg 59:32–39, 1983

    • Search Google Scholar
    • Export Citation
  • 63.

    Tamargo RJ, , Bok RA, & Brem H: Angiogenesis inhibition by minocycline. Cancer Res 51:672–675, 1991 Tamargo RJ, Bok RA, Brem H: Angiogenesis inhibition by minocycline. Cancer Res 51:672–675, 1991

    • Search Google Scholar
    • Export Citation
  • 64.

    Terada T, , Higashida RT, & Halbach VV, et al: Development of acquired arteriovenous fistulas in rats due to venous hypertension. J Neurosurg 80:884–889, 1994 Terada T, Higashida RT, Halbach VV, et al: Development of acquired arteriovenous fistulas in rats due to venous hypertension. J Neurosurg 80:884–889, 1994

    • Search Google Scholar
    • Export Citation
  • 65.

    White CW, , Sondheimer HM, & Crouch EC, et al: Treatment of pulmonary hemangiomatosis with recombinant interferon ALFA-2a. N Engl J Med 320:1197–1200, 1989 White CW, Sondheimer HM, Crouch EC, et al: Treatment of pulmonary hemangiomatosis with recombinant interferon ALFA-2a. N Engl J Med 320:1197–1200, 1989

    • Search Google Scholar
    • Export Citation
  • 66.

    Willinsky R, , Terbrugge K, & Lasjaunias P, et al: The variable presentations of craniocervical and cervical dural arteriovenous malformations. Surg Neurol 34:118–123, 1990 Willinsky R, Terbrugge K, Lasjaunias P, et al: The variable presentations of craniocervical and cervical dural arteriovenous malformations. Surg Neurol 34:118–123, 1990

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