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Hemoglobin penetration in the wall of the rabbit basilar artery after subarachnoid hemorrhage and intracisternal hemoglobin injection

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Summary

The ability of hemoglobin (Hb) to penetrate the basilar arterial wallin vivo after experimental subarachnoid hemorrhage was examined using immunohistochemistry. The distribution of anti-Hb antibodies in rabbit basilar artery was studied following the injection of autologous blood in the cisterna magna. Vessels removed two or four days after subarachnoid hemorrhage exhibited varying degrees of vasospasm, and exhibited Hb immuno-fluorescence throughout the vessel wall. Hemoglobin immunofluorescence was most conspicuous in the adventitia but was also seen in the smooth muscle and endothelial cell layers in 7 of 10 animals. The degree of vasoconstriction correlated with the total amount of Hb-fluorescence present in the vessel wall. When Hb solution alone was injected into the subarachnoid space, vasoconstriction was evident but penetration into the vascular layers was not as extensive as that observed after injection of autologous blood.

These findings demonstrate that Hb is able to penetrate through the arterial wall after subarachnoid hemorrhage. The results provide direct support for the hypothesis that Hb-induced changes in smooth muscle and/or endothelial function can contribute to the pathogenesis of vasospasm.

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References

  1. Boullin DJ, Tagari P, duBoulay G, Aitken V, Hughes JT (1983) The role of hemoglobin in the etiology of cerebral vasospasm. J Neurosurg 59: 231–236

    PubMed  Google Scholar 

  2. Cook DA, Weir BKA, Okawuasaba FK, Kreuger CA (1979) Effects of hemoglobin on smooth muscle. Proc West Pharmacol Soc 22: 429–434

    PubMed  Google Scholar 

  3. Debdi M, Seylaz J, Sercombe R (1992) Early changes in rabbit cerebral artery reactivity after subarachnoid hemorrhage. Stroke 23: 1154–1162

    PubMed  Google Scholar 

  4. Fein JM, Flor WJ, Cohan SL, Parkhurst J (1974) Sequential changes of vascular ultrastructure in experimental cerebralsospasm. J Neurosurg 4: 49–58

    Google Scholar 

  5. Fujii S, Fujitsu K (1988) Experimental vasospasm in cultured smooth muscle cells. 1: contractile and ultrastructural changes caused by oxyhemoglobin. J Neurosurg 69: 92–97

    PubMed  Google Scholar 

  6. Fujiwara S, Kassell NF, Sasaki T, Nakagomi T, Lehman RM (1986) Selective hemoglobin inhibition of endothelium-dependent vasodilation of rabbit basilar artery. J Neurosurg 64: 445–452

    PubMed  Google Scholar 

  7. Hongo K, Ogawa H, Kassell NF, Nakagomi T, Sasaki T, Tsukahara T, Lehman RM (1988) Comparison of intraluminal and extraluminal inhibitory effects of hemoglobin on endothelium-dependent relaxation of rabbit basilar artery. Stroke 19: 1550–1555

    PubMed  Google Scholar 

  8. Kajikawa H, Ohta T, Yoshikawa Y, Funatsu N, Yamamoto M, Someda K (1979) Cerebral vasospasm and hemoglobins: clinical and experimental studies. Neurol Med Chir (Tokyo) 19: 61–71

    Google Scholar 

  9. Kanamaru K, Waga S, Kojima T, Fujimoto K, Niwa S (1987) Endothelium-dependent relaxation of canine basilar arteries. Part 2: inhibition by hemoglobin and CSF from patients with aneurysmal subarachnoid hemorrhage. Stroke 18: 938–943

    PubMed  Google Scholar 

  10. Koide T, Neichi T, Takato M, Matsushita H, Sugioka K, Nakano M, Hata S (1982) Possible mechanisms of 15-hydroperoxy-arachidonic acid-induced contraction of the canine basilar artery in vitro. J Pharmacol Exp Ther 221: 481–488

    PubMed  Google Scholar 

  11. Liszczak TM, Varsos G, Black PM, Kistler JP, Zervas NT (1983) Cerebral arterial constriction after experimental subarachnoid hemorrhage is associated with blood components within the arterial wall. J Neurosurg 58: 18–26

    PubMed  Google Scholar 

  12. Macdonald RL, Weir BKA (1991) A review of hemoglobin and the pathogenesis of cerebral vasospasm. Stroke 22: 971–982

    PubMed  Google Scholar 

  13. Martin W, Villani GM, Jothianandan D, Furchgott RF (1985) Selective blockade of endothelium-dependent and glyceryl trinitrate-induced relaxation by hemoglobin and by methylene blue in the rabbit aorta. J Pharmacol Exp Ther 232: 708–716

    PubMed  Google Scholar 

  14. Mayberg MR, Okada T, Bark DH (1990) Role of hemoglobin in arterial narrowing after subarachnoid haemorrhage. J Neurosurg 72: 634–640

    PubMed  Google Scholar 

  15. Mayberg MR, Okada T, Bark DH (1990) The significance of morphological changes in cerebral arteries after subarachnoid hemorrhage. J Neurosurg 72: 626–633

    PubMed  Google Scholar 

  16. Misra HP, Fridovich I (1972) The generation of superoxide radical during the autooxidation of hemoglobin. J Biol Chem 247: 6960–6962

    PubMed  Google Scholar 

  17. Ohlstein EH, Storer BL (1992) Oxyhemoglobin stimulation of endothelin production in cultured endothelial cells. J Neurosurg 77: 274–278

    PubMed  Google Scholar 

  18. Ohta T, Satoh G, Kuroiwa T (1992) The permeability change of major cerebral arteries in experimental vasospasm. Neurosurgery 30(3): 331–336

    PubMed  Google Scholar 

  19. Okamoto S, Handa H, Handa Y (1985) Hemolysate-induced release of prostaglandin like substances from the canine cerebral arteries. Surg Neurol 23: 421–424

    PubMed  Google Scholar 

  20. Sasaki T, Wakai S, Asano T, Watanabe T, Kirino T, Sano K (1982) The effect of lipid hydroperoxide of arachidonic acid on the canine basilar artery. J Neurosurg 54: 357–365

    Google Scholar 

  21. Takenaka K, Yamada H, Sakai H, Ando T, Nakashima T, Nishimura Y, Okano Y, Nozawa Y (1991) Cytosolic calcium changes in cultured rat aortic smooth muscle cells induced by oxyhemoglobin. J Neurosurg 74: 620–624

    PubMed  Google Scholar 

  22. Tanashima T (1980) Cerebral vasospasm: contractile activity of hemoglobin in isolated canine basilar arteries. J Neurosurg 53: 787–793

    PubMed  Google Scholar 

  23. Toda N (1990) Mechanisms of contracting action of oxyhemoglobin in isolated monkey and dog cerebral arteries. Am J Physiol 258: H 57-H 63

    Google Scholar 

  24. Toda N, Shimizu K, Ohta T (1980) Mechanism of cerebral arterial contraction induced by blood constituents. J Neurosurg 53: 312–322

    PubMed  Google Scholar 

  25. Toda W (1988) Hemolysate inhibits cerebral artery relaxation. J Cereb Blood Flow Metab 8: 46–53

    PubMed  Google Scholar 

  26. Vollmer DG, Hongo K, Kassell NF, Ogawa H, Tsukahara T, Lehman RM (1989) Effect of intracisternal antithrombin III on subarachnoid hemorrhage-induced arterial narrowing. J Neurosurg 20: 599–604

    Google Scholar 

  27. Wellum GR, Irvine TW, Zervas NT (1980) Dose responses of cerebral arteries of the dog, rabbit, and man to human hemoglobin in vitro. J Neurosurg 53: 486–490

    PubMed  Google Scholar 

  28. Zervas NT, Liszczak TM, Mayberg MR, Black PMcL (1982) Cerebrospinal fluid may nourish cerebral vessels through pathways in the adventitia that may be analogous to systemic vasa vasorum. J Neurosurg 56: F475–481

    Google Scholar 

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Authors and Affiliations

  1. Department of Neurological Surgery, University of Virginia, Charlottesville, VA, USA

    P. L. Foley, N. F. Kassell, S. B. Hudson & K. S. Lee

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  1. P. L. Foley
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  2. N. F. Kassell
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  3. S. B. Hudson
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  4. K. S. Lee
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Foley, P.L., Kassell, N.F., Hudson, S.B. et al. Hemoglobin penetration in the wall of the rabbit basilar artery after subarachnoid hemorrhage and intracisternal hemoglobin injection. Acta neurochir 123, 82–86 (1993). https://doi.org/10.1007/BF01476290

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