The Anticoagulant Effects of the Hookworm, Ancylostoma ceylanicum: Observations on Human and Dog Blood In Vitro and Infected Dogs In Vivo

Summary

Extracts of adult Ancylostoma ceylanicum prolonged the prothrombin time (PT) and partial thromboplastin time with kaolin (PPTK) of both human and dog plasmas in vitro. Excret-ory/secretory (E/S) products of these worms had similar effects while larval extract prolonged the PTTK only. Thus, the anticoagulant activities of this parasite are dependent upon the stage of the worm’s life cycle. Collagen- and ADP-induced platelet aggregation were inhibited by adult and larval extracts. When the peripheral blood and bleeding times of dogs with varying worm burdens were examined, the only abnormality was shortening of the PTTK in the most heavily infected animals. Homogenates of dog small bowel subjacent to adult hookworms prolonged the PT of dog plasma and electron microscopical examination of this tissue revealed aggregation of platelets in blood venules without fibrin deposition. Thus, this study provides evidence that the anticoagulant properties of hookworms may have biological significance in infected animals.

Keywords

Ancylostoma ceylanicum - Hookworm - Anticoagulant effects

• References

• 1 Bugnion E. On the epidemic caused by ankylostomum among the workmen in the St. Gotthard tunnel. Br Med J 1881; 1: 382
• 2 Boycott AE. Ankylostoma infection. Lancet 1911; 1: 717-721
• 3 Lane C. Hookworm anaemia; outline in basic of current knowledge and opinion. Trop Dis Bull 1937; 34: 1-14
• 4 Roche M, Layrisse M. Nature and causes of “hookworm anemia”. Am J Trop Med Hyg 1966; 15: 1031-1100
• 5 Loeb L, Smith AJ. The presence of a substance inhibiting the coagulation of the blood in anchylostoma. Proc Pathol Soc Philadelphia 1904; 7: 173-178
• 6 Thorson RE. The effect of extracts of the amphidial glands, excretory glands and esophagus of adults of Ancylostoma caninum on the coagulation of dog’s blood. J Parasitol 1956; 42: 26-30
• 7 Eiff JA. Nature of an anticoagulant from the cephalic glands of Ancylostoma caninum. J Parasitol 1966; 52: 833-843
• 8 Spellman GG, Nossel HL. Anticoagulant activity of dog hookworm. Am J Physiol 1971; 220: 922-927
• 9 Carroll SM, Grove DI, Dawkins HJ S, Mitchell GF, Whitten LK. Infections with a Malaysian dog strain of Ancylostoma ceylanicum in outbred, inbred and immunocompromised mice. Parasitology 1983; 87: 229-238
• 10 Carroll SM, Karthigasu KT, Grove DI. Serodiagnosis of human strongyloidiasis by an enzyme-linked immunosorbent assay. Trans R Soc Trop Med Hyg 1981; 75: 706-709
• 11 Hartree EF. Determination of protein: a modification of the Lowry method that gives a linear photometric response. Anal Biochem 1972; 48: 422-427
• 12 Dacie JA, Lewis SM. Practical Haematology. Churchill Livingstone; Edinburgh: 1976
• 13 Proctor RR, Rapaport SI. The partial thromboplastin time with kaolin. A simple screening test for the first stage clotting factor deficiencies Am J Clin Pathol 1961; 36: 212-219
• 14 Nilsson IM, Olow B. Fibrinolysis induced by streptokinase in man. Acta Chir Scand 1962; 123: 247-266
• 15 Thompson RC A, Dunsmore JD, Hayton AR. Echinococcus granulosus: Secretory activity of the rostellum of the adult cestode in situ in the dog. Exp Parasitol 1979; 48: 144-163
• 16 Graham R, Kamovsky MJ. The early stages of absorption of injected horseradish peroxidase in proximal tubules of mouse kidney. Ultrastructural cytochemistry by a new technique J Histochem Cytochem 1966; 14: 291-302
• 17 Forbes CD, Prentice CR M. Physiology and biochemistry of blood coagulation and fibrinolysis. In: Blood and Its Disorders. Hardisty RM, Weatherall DJ. (eds) Blackwell Scientific Publications; Oxford: 1982. pp 1075-1104
• 18 Hardisty RM. Platelets, blood vessels and hemostasis; disorders of platelets and vascular function. In: Blood and Its Disorders. Hardisty RM, Weatherall DJ. (eds) Blackwell Scientific Publications; Oxford: 1982. pp 1021-1074
• 19 Bensusan HB, Koh TL, Henry KG, Murray BA, Culp LA. Evidence that fibronectin is the collagen receptor on platelet membranes. Proc Natl Acad Sci USA 1978; 75: 5864-5868
• 20 Kao KJ, Pizzo SV, McKee PA. Demonstration and characterization of specific binding sites for factor VIII/von Willebrand factor on human platelets. J Clin Invest 1979; 63: 656-664
• 21 Crawford GP, Howse DJ, Grove DI. Inhibition of human blood clotting by extracts of Ascaris suum. J Parasitol 1982; 68: 1044-1047
• 22 Kalkofen UP. Intestinal trauma resulting from feeding activities of Ancylostoma caninum. Am J Trop Med Hyg 1974; 23: 1046-1053
• 23 Astrup T. Assay and content of tissue thromboplastin in different organs. Thrombos Diathes Haemorrh 1965; 14: 401-416