Development of acquired arteriovenous fistulas in rats due to venous hypertension

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✓ Dural sinus thrombosis has been hypothesized as a possible cause of dural arteriovenous fistulas (AVF's). The pathogenesis and evolution from thrombosis to actual development of an AVF are still unknown. To study dural fistula formation, a surgically induced venous hypertension model in rats was created by producing an arteriovenous shunt between the carotid artery and the external jugular vein. The external jugular vein beyond the anastomosis was ligated 2 to 3 months after surgery and angiography was performed to identify any new acquired AVF's.

Forty-six male Sprague-Dawley rats, each weighing approximately 300 gm, were used for this study. In Group I, 22 rats underwent a common carotid artery anastomosis to the external jugular vein, which is the largest draining vein from the transverse sinus via the posterior facial vein, followed by proximal external jugular vein ligation. In Group II, 13 rats underwent the same surgical procedure, followed by contralateral posterior facial vein occlusion. Group III served as the control group, in which 11 rats underwent only unilateral external jugular vein occlusion with or without contralateral posterior facial vein occlusion. The shunts in Groups I and II were ligated at 2 to 3 months following surgery, and transfemoral angiography was performed immediately before and after occlusion.

New acquired AVF's had developed in three rats (13.6%) in Group I, three rats (23.1%) in Group II, and no rats (0%) in Group III. One of these newly formed fistulas was located at the dural sinus, analogous to the human dural AVF. The other five were located in the subcutaneous tissue, including the face and neck. The dural AVF in the rat was present on follow-up angiography at 1 week after the bypass occlusion. It is concluded that chronic venous hypertension of 2 to 3 months' duration, without associated venous or sinus thrombosis, can induce new AVF's affecting the dural sinuses or the subcutaneous tissue.

Article Information

Address reprint requests to: Tomoaki Terada, M.D., Ph.D., Department of Neurological Surgery, Wakayama Medical College, 7 ban-cho 27, Wakayama City 640, Japan.

© AANS, except where prohibited by US copyright law.

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Figures

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    Diagram of shunt surgery. Abbreviations: s. = sinus; v. = vein. Arrows show the direction of blood flow.

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    Left common carotid angiograms, frontal (left) and lateral (right) views, in a Group I rat showing dilated veins, the transverse sinus, and the posterior part of the superior sagittal sinus (straight arrows). These veins drain into the right external jugular vein. Arterial structures are not well shown because of the steal phenomenon of the large arteriovenous shunt. The direction of blood flow is shown by curved arrows.

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    Right common carotid angiograms, frontal (left) and lateral (right) views, arterial phase, in a rat with a new dural arteriovenous fistula. Opacification of the posterior part of the superior sagittal sinus (arrows) can be seen.

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    Histopathological findings of the superior sagittal sinus in the Group I rat with a dural arteriovenous fistula. An enlarged superior sagittal sinus and marked thickening of the sinus wall are seen. There are numerous dilated vessels located within the sinus wall. H & E, × 118.

References

  • 1.

    Awad IALittle JRAkrawi WPet al: Intracranial dural arteriovenous malformations: factors predisposing to an aggressive neurological course. J Neurosurg 72:8398501990Awad 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
  • 2.

    Bederson JBWiestler ODBrüstle Oet al: Intracranial venous hypertension and the effects of venous outflow obstruction in a rat model of arteriovenous fistula. Neurosurgery 29:3413501991Bederson JB Wiestler OD Brüstle O et al: Intracranial venous hypertension and the effects of venous outflow obstruction in a rat model of arteriovenous fistula. Neurosurgery 29:341–350 1991

    • Search Google Scholar
    • Export Citation
  • 3.

    Butler AJEagleton MJWang Det al: Induction of the proliferative phenotype in differentiated myogenic cells by hypoxia. J Biol Chem 266:18250182581991Butler AJ Eagleton MJ Wang D et al: Induction of the proliferative phenotype in differentiated myogenic cells by hypoxia. J Biol Chem 266:18250–18258 1991

    • Search Google Scholar
    • Export Citation
  • 4.

    Chaudhary MYSachdev VPCho SHet al: Dural arteriovenous malformation of the major venous sinuses: an acquired lesion. AJNR 3:13191982Chaudhary 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
  • 5.

    Debrun GChartres A: Infra- and supratentorial arteriovenous malformations. A general review about two cases of spontaneous supratentorial arteriovenous malformation of the dura. Neuroradiology 3:1841921972Debrun G Chartres A: Infra- and supratentorial arteriovenous malformations. A general review about two cases of spontaneous supratentorial arteriovenous malformation of the dura. Neuroradiology 3:184–192 1972

    • Search Google Scholar
    • Export Citation
  • 6.

    Djindjian RMerland JJ: Super-Selective Arteriography of the External Carotid Artery. Berlin: Springer-Verlag1978Djindjian R Merland JJ: Super-Selective Arteriography of the External Carotid Artery. Berlin: Springer-Verlag 1978

    • Search Google Scholar
    • Export Citation
  • 7.

    Folkman JKlagsbrun M: Angiogenic factors. Science 235:4424471987Folkman J Klagsbrun M: Angiogenic factors. Science 235:442–447 1987

    • Search Google Scholar
    • Export Citation
  • 8.

    Franklin KJ: The physiology and pharmacology of veins. Physiol Rev 8:3463641928Franklin KJ: The physiology and pharmacology of veins. Physiol Rev 8:346–364 1928

    • Search Google Scholar
    • Export Citation
  • 9.

    Gelwan MJChoi ISBerenstein Aet al: Dural arteriovenous malformations and papilledema. Neurosurgery 22:107910841988Gelwan MJ Choi IS Berenstein A et al: Dural arteriovenous malformations and papilledema. Neurosurgery 22:1079–1084 1988

    • Search Google Scholar
    • Export Citation
  • 10.

    Grady MSPobereskin L: Arteriovenous malformations of the dura mater. Surg Neurol 28:1351401987Grady MS Pobereskin L: Arteriovenous malformations of the dura mater. Surg Neurol 28:135–140 1987

    • Search Google Scholar
    • Export Citation
  • 11.

    Griffith JQ JrFarris EJ: The Rat in Laboratory Investigation. Philadelphia: JB Lippincott1942 pp 4043Griffith JQ Jr Farris EJ: The Rat in Laboratory Investigation. Philadelphia: JB Lippincott 1942 pp 40–43

    • Search Google Scholar
    • Export Citation
  • 12.

    Hieshima GBCahan LDBerlin MSet al: Calvarial, orbital and dural vascular anomalies in hereditary hemorrhagic telangiectasia. Surg Neurol 8:2632671977Hieshima GB Cahan LD Berlin MS et al: Calvarial orbital and dural vascular anomalies in hereditary hemorrhagic telangiectasia. Surg Neurol 8:263–267 1977

    • Search Google Scholar
    • Export Citation
  • 13.

    Houser OWBaker HL JrRhoton AL Jret al: Intracranial dural arteriovenous malformations. Radiology 105:55641972Houser OW Baker HL Jr Rhoton AL Jr et al: Intracranial dural arteriovenous malformations. Radiology 105:55–64 1972

    • Search Google Scholar
    • Export Citation
  • 14.

    Houser OWCampbell JKCampbell RJet al: Arteriovenous malformation affecting the transverse dural venous sinus — an acquired lesion. Mayo Clinic Proc 54:6516611979Houser OW Campbell JK Campbell RJ et al: Arteriovenous malformation affecting the transverse dural venous sinus — an acquired lesion. Mayo Clinic Proc 54:651–661 1979

    • Search Google Scholar
    • Export Citation
  • 15.

    Kataoka KTaneda M: Angiographic disappearance of multiple dural arteriovenous malformations. Case report. J Neurosurg 60:127512781984Kataoka K Taneda M: Angiographic disappearance of multiple dural arteriovenous malformations. Case report. J Neurosurg 60:1275–1278 1984

    • Search Google Scholar
    • Export Citation
  • 16.

    Kerber CWNewton TH: The macro- and microvasculature of the dura mater. Neuroradiology 6:1751791973Kerber CW Newton TH: The macro- and microvasculature of the dura mater. Neuroradiology 6:175–179 1973

    • Search Google Scholar
    • Export Citation
  • 17.

    Kohler TRKirkman TRClowes AW: The effect of rigid external support on vein graft adaptation to the arterial circulation. J Vasc Surg 9:2772851989Kohler TR Kirkman TR Clowes AW: The effect of rigid external support on vein graft adaptation to the arterial circulation. J Vasc Surg 9:277–285 1989

    • Search Google Scholar
    • Export Citation
  • 18.

    Lasjaunias PBerenstein A: Surgical neuroangiography in Lasjaunias PBerenstein A (eds): Endovascular Treatment of Craniofacial Lesions. Berlin: Springer-Verlag1987 pp 273315Lasjaunias P Berenstein A: Surgical neuroangiography in Lasjaunias P Berenstein A (eds): Endovascular Treatment of Craniofacial Lesions. Berlin: Springer-Verlag 1987 pp 273–315

    • Search Google Scholar
    • Export Citation
  • 19.

    Lasjaunias PMing CTer Brugge Ket al: Neurological manifestations of intracranial dural arteriovenous malformations. J Neurosurg 64:7247301986Lasjaunias P Ming C Ter Brugge K et al: Neurological manifestations of intracranial dural arteriovenous malformations. J Neurosurg 64:724–730 1986

    • Search Google Scholar
    • Export Citation
  • 20.

    MacKenzie ETStrandgaard SGraham DIet al: Effects of acutely induced hypertension in cats on pial arteriolar caliber, local cerebral blood flow, and the blood-brain barrier. Circ Res 39:33411976MacKenzie 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
  • 21.

    Malik GMPearce JEAusman JLet al: Dural arteriovenous malformations and intracranial hemorrhage. Neurosurgery 15:3323391984Malik GM Pearce JE Ausman JL et al: Dural arteriovenous malformations and intracranial hemorrhage. Neurosurgery 15:332–339 1984

    • Search Google Scholar
    • Export Citation
  • 22.

    Miano JMVlasic NTota RRet al: Smooth muscle cell immediate-early gene and growth factor activation follows vascular injury. A putative in vivo mechanism for autocrine growth. Arterioscler Thromb 13:2112191993Miano JM Vlasic N Tota RR et al: Smooth muscle cell immediate-early gene and growth factor activation follows vascular injury. A putative in vivo mechanism for autocrine growth. Arterioscler Thromb 13:211–219 1993

    • Search Google Scholar
    • Export Citation
  • 23.

    Nabors MWAzzman CJAlbanna FJet al: Delayed postoperative dural arteriovenous malformations. Report of two cases. J Neurosurg 66:7687721987Nabors MW Azzman CJ Albanna FJ et al: Delayed postoperative dural arteriovenous malformations. Report of two cases. J Neurosurg 66:768–772 1987

    • Search Google Scholar
    • Export Citation
  • 24.

    Nishijima MTakaku AEndo Set al: Etiological evaluation of dural arteriovenous malformations of the lateral and sigmoid sinuses based on histopathological examinations. J Neurosurg 76:6006061992Nishijima 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
  • 25.

    Pile-Spellman JMDBaker KFLiszczak TMet al: Highflow angiopathy: cerebral blood vessel changes in experimental chronic arteriovenous fistula. AJNR 7:8118151986Pile-Spellman JMD Baker KF Liszczak TM et al: Highflow angiopathy: cerebral blood vessel changes in experimental chronic arteriovenous fistula. AJNR 7:811–815 1986

    • Search Google Scholar
    • Export Citation
  • 26.

    Strandgaard SJones JVMacKenzie ETet al: Upper limit of cerebral blood flow autoregulation in experimental renovascular hypertension in baboon. Circ Res 37:1641671975Strandgaard S Jones JV MacKenzie ET et al: Upper limit of cerebral blood flow autoregulation in experimental renovascular hypertension in baboon. Circ Res 37:164–167 1975

    • Search Google Scholar
    • Export Citation
  • 27.

    Strandgaard SOlesen JSkinhoj Eet al: Autoregulation in brain circulation in severe arterial hypertension. BMJ 1:5075101973Strandgaard S Olesen J Skinhoj E et al: Autoregulation in brain circulation in severe arterial hypertension. BMJ 1:507–510 1973

    • Search Google Scholar
    • Export Citation
  • 28.

    Watanabe ATakahara YIbuchi Yet al: Two cases of dural arteriovenous malformation occurring after intracranial surgery. Neuroradiology 26:3753801984Watanabe A Takahara Y Ibuchi Y et al: Two cases of dural arteriovenous malformation occurring after intracranial surgery. Neuroradiology 26:375–380 1984

    • Search Google Scholar
    • Export Citation

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