Download PDF
Thromb Haemost 1977; 38(04): 0850-0862
DOI: 10.1055/s-0038-1651903
Original Article
Schattauer GmbH

Depression of Collateral Blood Flow Following Arterial Thrombosis

Robert G. Schaub
*   College of Veterinary Medicine, University of Tennessee, Knoxville, TN 37901
,
Ronald Sande
**   College of Veterinary Medicine, Washington State University, Pullman, WA 99163 U.S.A.
,
Kenneth M. Meyers
**   College of Veterinary Medicine, Washington State University, Pullman, WA 99163 U.S.A.
› Author Affiliations
Further Information

Publication History

Publication Date:
04 July 2018 (online)

    Permissions and Reprints

Summary

Permanent ligation of the feline aorta at the iliac bifurcation is followed by rapid opening of pre-existing collateral blood vessels. However, if ligation is combined with formation of a clot, these protective collateral vessels do not function. This study was undertaken to determine if drugs which alter serotonin function can improve collateral blood flow after arterial thrombosis. Permanent ligations were placed at the iliac bifurcation, circumflex iliac and sixth lumbar arteries in all cats. A clot was produced in the aorta of 27 cats by injection of 0.1 ml of thromboplastin. Ligated clot-occluded cats were untreated (10); had blood serotonin depleted using a single dose of reserpine (0.1 mg/kg i. m.) followed by para-chlorophenylanine (p-CPA) (100 mg/kg orally) every 3 days (9) ; or were treated prior to surgery with a serotonin antagonist cinanserin HC1 (4 mg/kg i. v.) (8). Control cats (18) were acutely ligated. 9 of these cats were untreated, 5 were cinanserin HC1-treated, and 4 were reserpine/p-CPA-treated. Extent of collateral development was assessed by aortograms 3 days after occlusion and by neurologic rating. Aortograms of acutely ligated cats indicated a significant collateral blood flow around the segment of ligated aorta, while ligated clot-occluded cats had a severely depressed hind-limb perfusion. Reserpine/p-CPA-treated ligation clot-occluded cats had aortograms similar to acutely ligated cats. The cinanserin HC1-treated ligation clot-occluded cats had aortograms which indicated hind-limb perfusion was not as adequate as the acutely ligated cats. However, the perfusion of these animals was improved over untreated ligation clot-occluded cats. Neurologic rating correlated with aortograms. These results suggest: 1) the clinical consequences of arterial thrombosis cannot be entirely attributed to mechanical occlusion of an artery, but may be due to depression of protective collateral blood flow induced by thrombosis, 2) serotonin is an important factor in this depression of collateral blood flow, and 3) isolation of the factors responsible for collateral inhibition could permit the development of therapeutic interventions.

 

  • References

  • 1 Ashcroft G. W, Sharman D. F. 1962; Drug-induced changes in the concentration of 5-OR indolyl compounds in cerebrospinal fluid and caudate nucleus. British Journal of Pharmacology 19: 153.
    PubMedGoogle Scholar
  • 2 Baumgartner H. R. 1969; 5-hydroxytryptamine uptake and release in relation to aggregation of rabbit platelets. Journal of Physiology 201: 409.
    CrossrefPubMedGoogle Scholar
  • 3 Baumgartner H. R, Born G. V. R. 1968; Effects of 5-hydroxytryptamine on platelet aggregation. Nature, London 218: 137.
    CrossrefPubMedGoogle Scholar
  • 4 Bell III H. W, Sundt T. M, Nolzinger J. D. 1967; The response of cortical vessels to serotonin in experimental cerebral infarction. Journal of Neurosurgery 26: 203.
    CrossrefPubMedGoogle Scholar
  • 5 Bellman S, Frank H, Lambert P. B, Roy A. J. 1959; Studies of collateral vascular responses. I. Effects of selective occlusions of major trunk with an extensively anastomosing system. Angiology 10: 214.
    CrossrefPubMedGoogle Scholar
  • 6 Berkowitz B. A, Lee C. H, Spector S. 1974; Disposition of serotonin in the rat blood vessels and heart. Clinical and Experimental Pharmacology and Physiology 1: 397.
    CrossrefPubMedGoogle Scholar
  • 7 Buckly J. K, Ryan G. B. 1969; Increased vascular permeability: The effect of histamine and serotonin on the rat mesenteric blood vessels in vivo. American Journal of Pathology 55: 329.
    PubMedGoogle Scholar
  • 8 Butler H. C. 1968; An investigation into the relationship of an aortic embolus to posterior paralysis in the cat. Journal of Small Animal Practice 12: 141.
    PubMedGoogle Scholar
  • 9 Carlson A, Shore P. A, Brodie B. B. 1957; Release of serotonin from blood platelets by reserpine in vitro. Journal of Pharmacology and Experimental Therapy 120: 334.
    PubMedGoogle Scholar
  • 10 Chait A, Moltz A, Nelson Jr. J. H. 1968; The collateral arterial circulation in the pelvis. An angiographic study. American Journal of Roentgenology 102: 392.
    CrossrefPubMedGoogle Scholar
  • 11 Conrad M. C, Anderson III J. L, Garrett Jr. J. B. 1971; Chronic collateral growth after femoral artery occlusion in the dog. Journal of Applied Physiology 31: 550.
    CrossrefPubMedGoogle Scholar
  • 12 Day H. J, Ang G. A. T, Holmsen H. 1972; Platelet release reaction during clotting of native human platelet rich plasma. Proceedings of the Society of Experimental Biology and Medicine 139: 717.
    PubMedGoogle Scholar
  • 13 Derrick J. R. 1962; The effect of blood pressure on collateral flow. American Journal of Surgery 28: 493.
    PubMedGoogle Scholar
  • 14 Dible J. H. 1958; Some pathological adaptation in the peripheral circulation. The Lancet I: 7029.
    PubMedGoogle Scholar
  • 15 Eckstein R. W, Gregg D. E, Pritchard W. H. 1941; The magnitude and tone of development of the collateral circulation in occluded femoral, carotid, and coronary arteries. American Journal of Physiology 132: 351.
    PubMedGoogle Scholar
  • 16 Engel King W, Derrer E. C. 1975; Drugs blocking the muscle damaging effects of 5-HT and Noradrenaline in aorta ligature rats. Nature 254: 151.
    CrossrefPubMedGoogle Scholar
  • 17 Erspamer V, Faustini R. 1953; Über den 5-hydroxytryptamine (Enteramin Serotonin) Gehalt des Serums und des Milzgewebes bei Wirbeltieren sowie der Hämolymphe bei Octopoden. Naturwissenschaften 40: 317.
    PubMedGoogle Scholar
  • 18 Frederic M. 1971. Cerebrovascular disease in cardiac and vascular disease. Vol. II. Horwitz D, Conn H. L. (eds.) Lea and Febeger; Philadelphia: 1479.
    Google Scholar
  • 19 Fulton W. F. M. 1965. Coronary arteríes. Springfield, Ill.: Charles C. Thomas.;
    Google Scholar
  • 20 Furgiuele A. R, High J. P, Horowitz Z. P. 1965; Some central effects of (sq. 10,641) a potent serotonin antagonist. Archives of International Pharmacodynamics 155: 235.
    PubMedGoogle Scholar
  • 21 Geller I, Hartman R. J, Croy D. J, Haber B. 1974; Attenuation of conflict behavior with cinanserin, a serotonin antagonist: reversal of the effects with 5-hydroxytryptophan and dimethyltryptamine. Research Communication in Chemistry, Pathology, and Pharmacology 7: 165.
    PubMedGoogle Scholar
  • 22 Gregg D. E. 1974; The natural history of coronary collateral development. Circulation Research 35: 335.
    CrossrefPubMedGoogle Scholar
  • 23 Harland W. A, Holburn A. M. 1966; Coronary thrombosis and myocardial infarction. Lancet II: 1158.
    PubMedGoogle Scholar
  • 24 Harvey S. C, Ferris H. W. 1925; A physiological study of the development of collateral circulation in the leg of the dog. Proceedings of the Society of Experimental Biology and Medicine 22: 383.
    PubMedGoogle Scholar
  • 25 Hoak J. C. 1964; Structure of thrombi produced by injections of fatty adds. British Journal of Experimental Pathology 45: 44.
    PubMedGoogle Scholar
  • 26 Hoff H. F, Gottlob R. 1967; Afine structure of injury to the endothelial cells of the rabbit abdominal aorta by various stimuli. Angiology 18: 440.
    CrossrefPubMedGoogle Scholar
  • 27 Hollings H. E. 1972. Peripheral vascular diseases diagnosis and management. J. B. Lippincott; Philadelphia.:
    Google Scholar
  • 28 Holman E. 1949; Problems in dynamics of blood flow; conditions controlling collateral circulation in the presence of an arteriovenous fistula and following ligation of an artery. Surgery 26: 889.
    PubMedGoogle Scholar
  • 29 Imhoff R. D. 1961; Production of aortic occlusion resembling acute aortic embolism syndrome in cats. Nature (London) 192: 979.
    CrossrefPubMedGoogle Scholar
  • 30 John H. T, Warren R. 1961; The Stimulus to collateral circulation. Surgery 49: 14.
    PubMedGoogle Scholar
  • 31 Koe K. B, Weissman A. 1966; P-chlorophenylalanine: A specific inhibitor of brain serotonin. Journal of Pharmacology and Experimental Therapy 154: 499.
    PubMedGoogle Scholar
  • 32 Latschenberger J, Deahna A. 1976; Beiträge zur Lehre von der reflektorischen Erregung der Gefäßmuskeln. Archives Ges. Physiology 12: 157.
    PubMedGoogle Scholar
  • 33 Levin D. C. 1974; Pathways and functional significance of the coronary collateral circulation. Circulation 50: 831.
    CrossrefPubMedGoogle Scholar
  • 34 Lewis T. 1940; The adjustment of blood flow to the affected limb in arteriovenous fistula. Clinical Science 4: 277.
    PubMedGoogle Scholar
  • 35 Majno G, Gilmore U, Levinthal M. 1967; On the mechanism of vascular leake caused by histamine type receptors. Circulation Research 21: 832.
    PubMedGoogle Scholar
  • 36 Majno G, Palade G. E. 1961; Studies on inflammation. I. The effect of histamine and serotonin on vascular permeability: An electron microscopic study. Journal of Biophysiology, Biochemistry, and Cytology 11: 571.
    PubMedGoogle Scholar
  • 37 Meyer J. S, Walch K. M. A, Shigsmichi O, Shimazu K. 1974 Disordered neurotransmitters function – demonstration by measurement of nosepinephrine and 5-hydroxytryptamine in CSF of patients with recent cerebral infarction.
    PubMedGoogle Scholar
  • 38 Mitchell J. R. A, Schwartz C. J. 1965. Arterial disease. Blackwell; London.:
    Google Scholar
  • 39 Mulvihill D. A, Harvey S. C. 1931; The mechanism of the development of collateral circulation. New England Journal of Medicine 204: 1032.
    CrossrefPubMedGoogle Scholar
  • 40 Page I. H. 1952; The vascular action of natural serotonin, 5- and 7-hydroxytryptamine and tryptamine. Journal of Pharmacology and Experimental Therapy 105: 58.
    PubMedGoogle Scholar
  • 41 Pearse H. E. 1927; An experimental study of arterial collateral Circulation. Annals of Surgery 86: 850.
    CrossrefPubMedGoogle Scholar
  • 42 Pitt B. 1959; Interarterial coronary anastomoses. Occurence in normal hearts and certain pathological conditions. Circulation Research 22: 816.
    PubMedGoogle Scholar
  • 43 Rand M, Reid G. 1951; Source of serotonin in serum. Nature (London) 168: 385.
    PubMedGoogle Scholar
  • 44 Rees J. R, Redding V. J. 1967; Anastomotic blood flow in experimental myocardial infarction. Cardiovascular Research 1: 169.
    CrossrefPubMedGoogle Scholar
  • 45 Reichart F. L. 1924; An experimental study of the anastomotic circulation in the dog. Bull John Hopkins Hospital 35: 385.
    PubMedGoogle Scholar
  • 46 Reuse-Blom S. 1976 Cerebral vasospasm in the rabbit. IXth World Conference European Society for Microcirculation. Abstracts 81.
    PubMedGoogle Scholar
  • 47 Roddie I. C, Shepherd J. T, Whelan R. F. 1955; The action of 5-hydroxytryptamine on the blood vessels of the human hand and forearm. British Journal of Experimental Pathology 10: 445.
    PubMedGoogle Scholar
  • 48 Rosenthal S. L, Guyton A. C. 1968; Hemodynamics of collateral vasodilation following femoral artery occlusion in anesthetized dogs. Circulation Research 23: 239.
    CrossrefPubMedGoogle Scholar
  • 49 Rowley D. A. 1964; Venous constriction as the cause of vascular permeability produced by 5-hydroxytryptamine, histamine, bradykinin, and 48/80 in the rat. British Journal of Experimental Pathology 45: 56.
    PubMedGoogle Scholar
  • 50 Roy A. J, Lambert P. B, Frank H. A. 1964; Immediate responses of collateral vessels to abrupt arterial occlusion. American Journal of Physiology 206: 1299.
    PubMedGoogle Scholar
  • 51 Rubin B, Piala J. J, Burshe J. C, Craver B. N. 1964; A new, potent and specific serotonin inhibitor, (sq. 10,641) 2’-(3-demethylamimpropylthis) cinamanilide hydrochloride: antiserotonin activity on uterus and on gastrointestinal, vascular, and respiratory systems of animals. Archives of International Pharmacodynamics 152: 132.
    PubMedGoogle Scholar
  • 52 Rubin B, Waugh M. H. 1965; Antiphlogistic effects of antiserotonin (sq. 10,641) and aminopyrene in rats versus endotoxin and other agents. Procedures of the Society of Experimental Biology 119: 438.
    PubMedGoogle Scholar
  • 53 Schaper W. 1971. Collateral circulation of the heart. Amsterdam: North Holland Publishing Company.;
    Google Scholar
  • 54 Schaper W, Jageneau A, Xhonneux R. 1967; Development of collateral circulation in the pig and dog heart. Cardiologia 51: 321.
    CrossrefPubMedGoogle Scholar
  • 55 Schaub R. G, Meyers K. M, Sande R. D, Hamilton G. 1976; Inhibition of feline collateral vessel development following experimental thrombolic occlusion. Circulation Research 39: 736.
    CrossrefPubMedGoogle Scholar
  • 56 Shore P. A. 1972; Transport and storage of biogenic amines. Annals Review of Pharmacology 12: 209.
    PubMedGoogle Scholar
  • 57 Stefani A. 1886; Della influenza del sistema nervosa sulla circolazione collaterals. Sperimentale 58: 225.
    PubMedGoogle Scholar
  • 58 Swank R. L, Fellman J. H, Gissen W. W. 1963; Aggregation of blood cells by 5-hydroxytryptamine (Serotonin). Circulation Research 13: 66.
    PubMedGoogle Scholar
  • 59 Welch K. M. A, Hashi K, Meyer J. S. 1973; Cerebrovascular response to intracarotid injection of serotonin before and after middle cerebral artery occlusion. Journal of Neurology, Neurosurgery, and Psychiatry 36: 724.
    CrossrefPubMedGoogle Scholar
  • 60 Welch K. M. A, Meyer J. S, Teraura T, Hashi K, Shinmaru S. 1972; Ischemic anoxia and cerebral serotonin levels. Journal of Neurological Sciences 16: 85.
    CrossrefPubMedGoogle Scholar
  • 61 Wipple G. H, Peterson M. A, Harnes V, Leasner E, McKinnon E. 1972. “Acute myocardial infarction” in acute coronary care. Little, Brown, and Company; 41.
    Google Scholar
  • 62 Winbold J. N, Reemtsma K, Vernhet J. L, Laville L. P, Cruch O. 1959; Eteologic mechanisms in the development of collateral circulation. Surgery 45: 105.
    PubMedGoogle Scholar
  • 63 Zervas N. T, Kwwayama A, Rosoff C, Salzman E. 1971; Cerebral vascular spasm and reduction of platelet serotonin. Surgery Forum 22: 426.
    PubMedGoogle Scholar
  • 64 Zucker M. B. 1947; Platelet agglutination and vasoconstriction as factors in spontaneous hemostasis in normal, thrombocytopenic, heparinized and hypothrombinemicrats. American Journal of Physiology 148: 275.
    PubMedGoogle Scholar