Hostname: page-component-848d4c4894-wg55d Total loading time: 0 Render date: 2024-05-31T09:19:46.779Z Has data issue: false hasContentIssue false

The Neglected saliva: medically important toxins in the saliva of human lice

Published online by Cambridge University Press:  16 March 2011

D. Jones
Affiliation:
Graduate Center for Toxicology, University of Kentucky, Lexington, KY 40536-0305, USA

Summary

Although there has been a great deal of research effort within the last two decades on identifying the active components of the saliva of blood-sucking ticks, mosquitoes, biting flies, fleas and bugs, essentially neglected have been the human lice. Despite initial reports in the early part of this century suggestive of vasodilatory, anticoagulant and immunosuppressive properties of the saliva, for the next 50 years there were no biochemical studies on the active principles. Very recently, anatomical and biochemical studies have begun to characterize the bioactive molecules in lice saliva. The louse stocks a salivary vasodilator in excess over what is needed for a single bite, and injects similar amounts at each successive bite. The vasodilator in lice saliva appears to have different pharmacological properties than peroxidative, oxidative and maxidilan types of vasodilators reported from other blood-sucking insects. Possible anticoagulant activities have also been characterized. This belated, but welcome, interest comes at a time of resurgence of lice-born disease in certain parts of Africa, and of resistance to chemical control in Europe and North America.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1998

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abdel Fattah, S. M., El Sedfy, H. H., Ed Sayed, H. L., Abdel Aziz, H., Morsy, T. A., Salama, M. M. & Hamdi, K. N. (1994). Seropositivity against pediculosis in children with cervical lymphadenopathy. Journal of the Egyptian Society for Parasitology 24, 5967.Google Scholar
Abebe, M., Ribeiro, J. M., Cupp, M. S. & Cupp, E. W. (1996). Novel anticoagulant from salivary glands of Simulium vittatum (Diptera: Simulidae) inhibits activity of coagulation factor V. Journal of Medical Entomology 33, 1173–176.CrossRefGoogle Scholar
Anonymous (1994). Epidemic typhus risk in Rwandan refugee camps. Weekly Epidemiological Record 69, 259.Google Scholar
Balbi, E. (1933). Studi allergici nella pediculosi. Soc. Medicine et Chirurgie Padova Atti. 11, 858881.Google Scholar
Bisgaard, H. (1987). Vascular effects of leukotriene D4 in human skin. Journal of Investigatory Dermatology 88, 109114.CrossRefGoogle Scholar
Boulton, A. (1995). Britain restricts lice treatment. British Medical Journal 311, 1322.CrossRefGoogle Scholar
Brain, S. D., Camp, R. D., Black, A. K., Dowd, P. M., Greaves, M. W., Ford-Hutchinson, A. W. & Charleson, S. D. (1995). Leukotrienes C4 and D4 in psoriatic skin lesions. Prostaglandins 29, 611619.CrossRefGoogle Scholar
Brummer-Korvenkontio, H., Palosuo, T., Francois, G. & Reunala, T. (1997). Characterization of Aedes communis, Aedes aegypti and Aedes stephensi mosquito saliva antigens by immunoblotting. International Archives of Allergy and Immunology 112, 169174.CrossRefGoogle Scholar
Burgess, I. F., Brown, C. M., Peock, S. & Kaufman, J. (1995). Head lice resistant to pyrethroid insecticides in Britain. British Medical Journal 311, 752.CrossRefGoogle Scholar
Buxton, P. A. (1947). The Louse. An Account Of The Lice Which Infest Man, Their Importance And Control. London: Edward & Co., pp. 1115.Google Scholar
Champagne, D. E. & Ribeiro, J. M. C. (1994). Sialokinin I and II: vasodilatory tachykinins from the yellow fever mosquito Aedes aegypti. Proceedings of the National Academy of Sciences, USA 91, 138–142.CrossRefGoogle Scholar
Champagne, D. E., Smartt, C. T., Ribeiro, J. M. C. & James, A. A. (1995). The salivary of gland-specific apyrase of the Aedes aegypti is a member of the 5′-nucleotidase family. Proceedings of the National Academy of Sciences, USA 92, 694–698.CrossRefGoogle Scholar
Champagne, D. E. & Valenzuela, J. G. (1996). Pharmacology of haematophagous arthropod saliva. In The Immunology or Host-Ectoparasitic Arthropod Relationships (ed. Wikel, S. K.), pp. 85107. Wallingford: CAB International.Google ScholarPubMed
Chan, C. C. & Ford-Hutchinson, A. (1985). Effects of synthetic leukotrienes on local blood flow and vascular permeability in porcine skin. Journal of Investigatory Dermatology 84, 154157.CrossRefGoogle Scholar
Clark, P. H. & Cole, M. M. (1967). Resistance of body lice to carbaryl. Journal of Economic Entomology 60, 398400.CrossRefGoogle Scholar
Clore, E. R. & Longyear, L. A. (1990). Comprehensive screening programs for elementary schools. Journal of School Health 60, 212214.CrossRefGoogle Scholar
Cross, M. L., Cupp, E. W. & Enriquez, F. J. (1994 a). Differential modulation of murine cellular immune responses by salivary gland extract of Aedes aegypti. American Journal of Tropical Medicine and Hygiene 51, 690696.Google Scholar
Cross, M. L., Cupp, E. W. & Enriquez, F. J. (1994 b). Modulation of murine cellular immune responses and cytokines by salivary gland extract of of the black fly Simulium vittatum. Tropical and Medical Parasitology 45, 119124.Google Scholar
Cupp, E. W., Cupp, M. S. & Ramberg, F. B. (1994). Salivary apyrase in African and New World vectors of Plasmodium species and its relationship to malaria transmission. American Journal of Tropical Medicine and Hygiene 50, 235240.CrossRefGoogle Scholar
De Jong, J., Wilkinson, R. J., Schaeffers, P., Sondorp, H. E. & Davidson, R. N. (1995). Louse-born relapsing fever in southern Sudan. Transactions of the Royal Society of Tropical Medicine and Hygiene 89, 621.CrossRefGoogle Scholar
Donnelly, E., Lipkin, J., Clore, E. R. & Altschuler, D. Z. (1991). Pediculosis prevention and control strategies of community health and school nurses: a descriptive study. Journal of Community Health Nursing 8, 8595.CrossRefGoogle Scholar
Dusbabeck, F., Borsky, I., Jelinek, F. & Uhlir, J. (1995). Immunosuppression and feeding success of Ixodes ricinus nymphs on Balb/c mice. Medical and Veterinary Entomology 9, 133140.CrossRefGoogle Scholar
EdmundsLh, jr Lh, jr. (1995). Why cardiopulmonary bypass makes patients sick: strategies to control the blood-synthetic surface interface. Advances in Cardiac Surgery 6, 131167.Google Scholar
Feingold, B. F., Behjamani, E. & Michaeli, D. (1968). The allergic response to insect bites. Annual Review of Entomology 13, 137158.CrossRefGoogle Scholar
Garcia, E. S., Mello, C. B., Azambuja, P. & Ribeiro, J. M. (1994). Rhodinus prolixus: salivary antihemostatic compounds decrease with Trypanosome rangeli infection. Experimental Parasitology 78, 287293.CrossRefGoogle Scholar
Gordon, J. R. & Allen, J. R. (1991). Factors V and VII anticoagulant activities in the salivary glands of feeding Dermacentor andersoni ticks. Journal of Parasitology 77, 167170.CrossRefGoogle Scholar
Hoffman, D. R. (1995). Allergic reactions to biting insects. In Monograph of Insect Allergins, (ed. Levine, M I., Lockey, R. F.) 3rd ed., ch. 14, pp. 99108. Milwaukee: American Academy of Allergy and Immunology.Google Scholar
Izri, M. A. & Briere, C. (1995). First cases of resistance of Pediculus capitis Linne 1758 to malathion in France (letter) Presse Medicale 24, 1444.Google Scholar
Jacobs, J. W., Cupp, E. W., Sardana, M. & Friedman, P. A. (1990). Isolation and characterization of a factor Xa inhibitor from blackfly salivary glands. Thrombosis and Haemostasis 64, 235238.Google Scholar
Jones, D. & Coudron, T. (1993). Venoms of parasitic hymenoptera as investigatory tools. In Parasites and Pathogens of Insects (ed. Beckage, N. E., Thompson, S. N. & Federici, B.) pp. 227–245.CrossRefGoogle Scholar
Jones, D. & Wache, S. (1998). Structure of salivary glands of human body lice and erythematous and immunogenic properties of their salivary toxins. Medical and Veterinary Entomology (in press).Google Scholar
Jones, D. & Wozniak, M. (1991). Regulatory mediators in the venom of Chelonus sp.: their biosynthesis and subsequent processing in homologous and heterologous systems. Biochemical and Biophysical Research Communications 178, 213220.CrossRefGoogle Scholar
Kubes, M., Fuchsberger, N., Labuda, M., Zuffova, E. Z. & Nuttall, P. A. (1994). Salivary glands extracts of partially fed Dermacentor reticulatus ticks decrease natural killer cell activity in vitro. Immunology 82, 113116.Google Scholar
Law, J., Ribeiro, J. M. C. & Wells, M. A. (1992). Biochemical insights derived from insect diversity. Annual Review of Biochemistry 61, 87111.CrossRefGoogle Scholar
Lee, R. (1974). Structure and function of the fascicular stylets, and the lebral and cibarial sense organs of male and female Aedes aegypti. Quaestiones Entomologica 10, 187215.Google Scholar
Lehane, M. J. (1991). Biology of Blood-Sucking Insects. Cambridge: The University Press.CrossRefGoogle Scholar
Lerner, E. A. & Shoemaker, C. (1992). Maxadilan, cloning and functional expression of the gene encoding this potent vasodilator. Journal of Biological Chemistry 267, 10621066.CrossRefGoogle Scholar
Mant, M. J., & Parker, K. R. (1981). Two platelet aggregation inhibitors in Tsetse (Glossina) saliva with studies of roles of thrombin and citrate in in vitro platelet aggregation. British Journal of Hematology 48, 601608.CrossRefGoogle Scholar
Maragannore, J. M. & Adelman, B. A. (1996). A direct thrombin inhibitor for management of acute coronary syndromes. Coronary and Artery Disease 7, 438448.Google Scholar
Mckenzie, C. R., Abbendscein, D. R. & Eisenberg, P. R. (1996). Sustained inhibition of wholeblood clot procoagulant activity by inhibition of thrombusas-sociated Factor Xa. Arteriosclerosis Thrombosis and Vascular Biology 16, 12851291.CrossRefGoogle Scholar
Mekasha, A. & Meharie, S. (1996). Outbreak of louse borne relapsing fever in Jimma, south western Ethiopia. East Africa Medical Journal 73, 5458.Google Scholar
Mellanby, K. (1946). Man's reaction to mosquito bites. Nature 158, 554.CrossRefGoogle Scholar
Miller, R. N., Wisseman, C. L., Sweeney, G. W., Verscheuren, A. & Fabrikant, I. B. (1972). First report of resistance of human body lice to malathion. Transactions of the Royal Society for Tropical Medicine and Hygiene 66, 372374.CrossRefGoogle Scholar
Moore, W. (1918). An interesting reaction to louse bites. Journal of the American Medical Association 71, 14811482.CrossRefGoogle Scholar
Morsy, T. A., Alafy, M. S., Sabry, A. H., Fikry, A. A. & El Sharkawy, I. M. (1996). Abnormal distribution of the histocompatibility antigens (HLA) in lousy patients. Journal of the Egyptian Society for Parasitology 26, 227235.Google Scholar
Mumcuoglu, K. Y. (1996). Control of human lice (Anoplura: Pediculidae) infestations: past and present. American Entomologist 42, 175178.CrossRefGoogle Scholar
Mumcuoglu, K. Y., Hemingway, J., Miller, J., Loffeuspensky, I., Klaus, S., Ben-Ishai, F. & Galun, R. (1995). Permethrin resistance in the head louse Pediculus capitis from Israel. Medical and Veterinary Entomology 9, 427432.CrossRefGoogle Scholar
Mumcuoglu, K. Y., Galun, R., Kaminchik, Y., Panet, A. & Levanon, A. (1996). Antihemostatic activity in salivary glands of the human body Pediculus humanus (Anoplura: Pediculidae). Journal of Insect Physiology 42, 10831087.CrossRefGoogle Scholar
Nelson, W. A., Bell, J. F., Clifford, C. M., & Keirans, J. E. (1977). Interaction of ectoparasites and their hosts. Journal of Medical Entomology 13, 389428.CrossRefGoogle Scholar
Nutall, G. H. F. (1918 a). Biology of Pediculus humans. Parasitology 10, 1185.Google Scholar
Nutall, G. H. F. (1918 b). The pathological effects of Phthirus pubis. Parasitology 10, 375379.Google Scholar
Pavlovsky, E. N. & Stein, A. K. (1925). Uber die Ursachen der Kirkung der Lause der Gattung Pediculus aug die integumenta des Menschen. Revue Russe d'Entomologie, 19, 1720.Google Scholar
Peck, S. M., Wright, W. H. & Gant, J. Q. (1943). Cutaneous reactions due to the body louse (Pediculus humans). Journal of the American Medical Association 123, 821825.CrossRefGoogle Scholar
Peng, Z. & Simmons, F. E. (1997). Comparison of proteins, IgE and IgG binding antigens, and skin reactivity, in commercial and laboratory-made mosquito extracts. Annals of Allergy, Asthma, and Immunology 77, 371376.CrossRefGoogle Scholar
Perez De Leon, A. A., Ribeiro, J. M., Tabachnick, W. I. & Valenuela, J. G. (1997). Identification of a salivary vasodilator in the primary North American vector of blue-tongue virus, Culicoides variipennis. American Journal of Tropical Medicine and Hygiene 57, 375381.CrossRefGoogle Scholar
Rahlenbeck, S. I. & Gebre-Yohannes, A. (1995). Louse-borne relapsing fever and its treatment. Tropical and Geographical Medicine 47, 4952.Google Scholar
Renunala, T., Brummer-Korvenkontio, H., Palosuo, K., Miyanij, M., Ruiz-Maldonado, R., Love, A., Francois, G. & Palosuo, T. (1994). Frequent occurrence of IgE and IgG4 antibodies against saliva of Aedes communis and Aedes aegypti mosquitoes in children. International Archives of Allergy and Immunology 104, 366371.CrossRefGoogle Scholar
Replogle, J., Lord, W. D., Budowle, B., Meinking, T. L., Taplin, D. (1994). Identification of host Dna by amplified fragment length polymorphism analysis: preliminary analysis of human crab louse (Anoplura: Pediculidae) excreta. Journal of Medical Entomology 31, 686690.CrossRefGoogle Scholar
Ribeiro, J. M. C. (1987). Role of saliva in blood-feeding by Arthropods. Annual Review of Entomology 32, 463478.CrossRefGoogle Scholar
Ribeiro, J. M. C. (1992). Characterization of a vasodilator from the salivary glands of the yellow fever mosquito Aedes aegypti. Journal of Experimental Biology 165, 6171.CrossRefGoogle Scholar
Ribeiro, J. M. C. (1995 a). Blood-feeding arthropods: live syringes or invertebrate pharmacologists? Infectious Agents and Diseases 4, 143152.Google Scholar
Ribeiro, J. M. C. (1995 b). How ticks make a living. Parasitology Today 11, 9193.CrossRefGoogle Scholar
Ribeiro, J. M. C. & Garcia, E. S. (1980). The salivary and crop apyrase activity of Rhodnius prolixus. Journal of Insect Physiology 26, 303307.CrossRefGoogle Scholar
Ribeiro, J. M. C. & Garcia, E. S. (1981). The role of the salivary glands in feeding in Rhodnius prolixus. Journal of Experimental Biology 94, 219230.CrossRefGoogle Scholar
Ribeiro, J. M. C., Jefferson, A. V. & Azad, A. F. (1990). Characterization of the salivary apyrase activity of three rodent flea species. Comparative Biochemistry and Physiology 95B, 215219.Google Scholar
Ribeiro, J. M. C. & Nussenzveig, R. H. (1993). The salivary catechol oxidase/peroxidase activities of the mosquito Anopheles albimanus. Journal of Experimental Biology 179, 273287.CrossRefGoogle Scholar
Ribeiro, J. M. C., Rossignol, P. A. & Spielman, A. (1985). Salivary gland apyrase determines probing time in Anopheline mosquitoes. Journal of Insect Physiology 31, 689692.CrossRefGoogle Scholar
Ribeiro, J. M. C., Rossignol, P. A. & Spielman, A. (1986). Bloodfinding strategy of a capillary feeding sandfly, Lutzomyia longipalpis. Comparative Biochemistry and Physiology 83A, 683686.CrossRefGoogle Scholar
Ribeiro, J. M. C. & Sarkis, J. J. F. (1982). Antithromboxane activity in Rhodinus prolixus salivary secretion. Journal of Insect Physiology 28, 655660.CrossRefGoogle Scholar
Ribeiro, J. M. C., Vacheereau, A., Modi, G. B. & Tesh, R. B. (1989). A novel vasodilatory peptide from the salivary glands of the sand fly Lutzomyia longipalpis. Science 243, 212214.Google Scholar
Robert, P. & Nguyen, V. X. (1995). Resistance of lice to insecticides: a serious public health problem. Canadian Journal of Public Health 86, 3031.Google Scholar
Rossignol, P. A., Ribeiro, J. M. C. & Spielman, A. (1984). Salivary apyrase of Aedes aegypti: characterization and secretory fate. Comparative Biochemistry and Physiology 79B, 8186.Google Scholar
Rupes, V., Moravec, J., Chmela, J., Ledvinka, J. & Jelenkova, J. (1995). A resistance of head lice (Pediculus capitus) to permethrin in Czech Republic. Central European Journal of Public Health 3, 3032.Google Scholar
Sarkis, J. J. F., Guimaraes, J. A. & Ribeiro, J. M. C. (1986). Salivary apyrase of Rhodnius prolixus. Biochemical Journal 233, 885891.CrossRefGoogle Scholar
Scowen, P. (1995). Government restricts the use of carbaryl for head lice. Professional Care of Mother and Child 5, 163.Google Scholar
Seboxa, T. & Rahlenbeck, S. I. (1995). Treatment of louse borne relapsing fever with low dose penicillin or tetracycline: a clinical trial. Scandanavian Journal of Infectious Disease 27, 2931.CrossRefGoogle Scholar
Shan, E. Z., Taniguchi, Y., Shimizu, M., Ando, K., Chinzei, Y., Suto, C., Ohtaki, T. & Ohtaki, N. (1995). Immunoglobulins specific to mosquito salivary gland proteins in the sera of persons with common or hypersensitive reactions to mosquito bites. Journal of Dermatology 22, 411418.CrossRefGoogle Scholar
Silverton, N. (1972). Malathion-resistant Pediculus capitis. British Medical Journal 3, 646647.CrossRefGoogle Scholar
Sokoloff, F. (1994). Identification and management of pediculosis. Nurse Practitioner 19, 6264.CrossRefGoogle Scholar
Soter, N. A., Lewis, R. A., Covey, E. & Austen, K. F. (1983). Local effects of synthetic leukotrienes (LTC4, LTD4, LTE4, and LTB4) in human skin. Journal of Investigatory Dermatology 80, 115119.CrossRefGoogle Scholar
Stein, A. K. (1931). Theorie des spezifischen Einflusses der wirksamen Elemente der animalen und vegetabilischen Natur auf die Entstehung der Dermatite. Ada Dermato Venerologica 12, 483493.Google Scholar
Theodos, C. M. & Titus, R. G. (1993). Salivary gland material from the sand fly Lutzomyia longipalpis has an inhibitory effect on macrophage function in vitro. Parasite Immunolology 15, 481.CrossRefGoogle Scholar
Titus, R. G. & Ribeiro, J. M. C. (1990). The role of vector saliva in transmission of arthropod-borne disease. Parasitology Today 6, 157160.CrossRefGoogle Scholar
Urioste, S., Hall, L. R., Telford, S. R. & Titus, R. G. (1994). Saliva of the lyme disease vector, Ixodes dammini, blocks cell activation by a nonprostaglandin E2-dependent mechanism. Journal of Experimental Medicine 180, 10771086.CrossRefGoogle Scholar
Waxman, L., Smith, D. E., Arcuri, K. E. & Vlasuk, G. P. (1990). Tick anticoagulant peptide (TAP) is a novel inhibitor of blood coagulation factor Xa. Science 248, 593596.CrossRefGoogle Scholar
White, D. J., Smith, P. F., Hechemy, K. E., Veltman, M. E., Deibel, R., Gallo, R., Stevens, R. W. & Ionascu, N. (1990). Possible typhus-group infection in New York State: presentation of four suspect cases. Annals of the New York Academy of Sciences 590, 256265.CrossRefGoogle Scholar
Wikel, S. K. (1982). Immune responses to arthropods and their products. Annual Review of Entomology 27, 2148.CrossRefGoogle Scholar
Wikel, S. K. & Osburn, R. I. (1982). Immune responsiveness of the bovine host to repeated low-level infestation with Dermacentor andersoni. Annals of Tropical Medicine and Parasitology 76, 405414.CrossRefGoogle Scholar
Wirtz, H. p. (1988). Quantitating histamine in the saliva and salivary glands of two palearctic blackfly species (Diptera: Simuliidae). Tropical Medicine and Parasitology 39, 309312.Google Scholar