Hostname: page-component-7c8c6479df-94d59 Total loading time: 0 Render date: 2024-03-29T09:39:11.427Z Has data issue: false hasContentIssue false

Transmission dynamics and control options for Echinococcus granulosus

Published online by Cambridge University Press:  04 March 2004

P. R. TORGERSON
Affiliation:
Institute of Parasitology, University of Zurich, Winterthurestrasse 266a, 8057 Zurich, Switzerland
D. D. HEATH
Affiliation:
AgResearch Limited, Wallaceville Animal Research Centre, Ward Street, PO Box 40063, Upper Hutt, New Zealand

Abstract

Cystic echinococcosis, caused by the larval stage of Echinococcus granulosus, is a global public health problem. Whilst in a few localities, such as New Zealand, the parasite has been effectively controlled or even eradicated, in most endemic regions it remains a persistent problem. In some areas, such as the former Soviet Union, the disease incidence in humans has increased rapidly in recent years. It is important to have an understanding of the transmission dynamics, both between dogs and domestic livestock where the parasite maintains itself and from dogs to people. It is from this knowledge that effective control measures can be devised to reduce the prevalence of the parasite in animals and hence reduce the incidence of human disease. Mathematical models to describe the transmission of the parasite and the effects of different control strategies were first proposed over twenty years ago. Since then further information has been acquired, new technology has been developed and better computing technology has become available. In this review, we summarise these developments and put together a theoretical framework on the interpretation of surveillance information, how this affects transmission and how this information can be exploited to develop new intervention strategies for the control of the parasite. In particular, the parasite remains a persistent or re-emerging problem in countries of low economic output where resources for an intensive control programme, that has been successful in rich countries, are not available. By understanding of the transmission biology, including mathematical modelling, alternative and cost-effective means of control can be developed.

Type
Research Article
Copyright
© 2003 Cambridge University Press

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

REFERENCES

AMINZHANOV, M. (1975). O prodoljitelnosti jizin Echinococcus granulosus v organizmaye sobaki. (The life span of Echinococcus granulosus in the dog.) Veterinariya, Moscow 12, 7072 [In Russian].Google Scholar
AMINZHANOV, M. (1976). Biologiya Echinococcus granulosus v organizmaye oviyets (Biology of Echinococcus granulosus in sheep). Veterinaya, Moscow 7, 6870 [in Russian].Google Scholar
ANDERSEN, F. L., TOLLEY, H. D., SCHANTZ, P. M., CHI, P., LIU, F. & DING Z. (1991). Cystic echinococcosis in the Xinjiang/Uygur Autonomous Region, People's Republic of China. II. Comparison of three levels of a local preventive and control program. Tropical Medicine and Parasitology 42, 110.Google Scholar
ANDERSON, R. M. & MAY, R. M. (1985). Herd immunity to helminth infections and implications for parasite control. Nature 315, 493496.CrossRefGoogle Scholar
ANDREASSEN, J. (1997). Interactions between intestinal tapeworms and their hosts: present knowledge and problems. Parassitologia 39, 259267.Google Scholar
BAI, Y., CHENG, N., JIANG, C., WANG, Q. & DARUENG, C. (2002). Survey on cystic echinococcosis in Tibetans, west China. Acta Tropica 82, 381385.CrossRefGoogle Scholar
CABRERA, P. A., HARAN, G., BENAVIDEZ, U., VALLEDOR, S., PERERA, G., LLOYD, S., GEMMELL, M. A., BARAIBAR, M., MORANA, A., MAISSONAVE, J. & CARBALLO, M. (1995). Transmission dynamics of Echinococcus granulosus, Taenia hydatigena and Taenia ovis in sheep in Uruguay. International Journal for Parasitology 25, 807813.CrossRefGoogle Scholar
CARMONA, C., PERDOMA, R., CARBO, A., ALVAREZ, C., MONTI, J., GRAUERT, R., STERN, D., PERERA, G., LLOYD, S., BZINI, R., GEMMELL, M. A. & YARZABAL, L. (1998). Risk factors associated with human cystic echinococcosis in Florida, Uruguay: results of a mass screening study using ultrasound and serology. American Journal of Tropical Medicine and Hygiene 58, 599605.CrossRefGoogle Scholar
COLLI, C. W. & WILLIAMS, J. F. (1972). Influence of temperature on the infectivity of eggs of Echinococcus granulosus in laboratory rodents. Journal of Parasitology 58, 422426.CrossRefGoogle Scholar
CHI, P., ZHANG, W., ZHANG, Z., HASYET, M., LIU, F., DING, Z., ANDERSEN, F. L., TOLLEY, H. D. & SCHANTZ, P. M. (1990). Cystic echinococcosis in the Xinjiang/Uygur autonomous region, People's Republic of China. 1. Demographic and epidemiological data. Tropical Medicine and Parasitology 41, 157162.Google Scholar
DEPLAZES, P. & ECKERT, J. (1988). Untersuchungen zur Infektion des Hundes mit Taenia hydatigena. Schweiz Arch Tierheilk 130, 289306.Google Scholar
DEPLAZES, P., THOMSON, R. C. A., CONSTANTINE, C. C. & PENHALE, W. J. (1994). Primary infection of dogs with Echinococcus granulosus: systemic and local (Peyer's patches) immune responses. Veterinary Immunology and Immunopathology 40, 171184.CrossRefGoogle Scholar
DOWLING, P., ABO-SHEHADA, M. & TORGERSON, P. R. (2000). Risk factors associated with human cystic echinococcosis in Jordan: results of a case-control study. Annals of Tropical Medicine and Parasitology 94, 6975.CrossRefGoogle Scholar
DOWLING, P. M. & TORGERSON, P. R. (2000). A cross sectional survey to analyse the risk factors associated with human cystic echinococcosis in an endemic area of mid-Wales. Annals of Tropical Medicine and Parasitology 94, 241245.CrossRefGoogle Scholar
DUEGER, E. L. & GILMAN, R. H. (2001). Prevalence, intensity, and fertility of ovine cystic echinococcosis in the central Peruvian Andes. Transactions of the Royal Society of Tropical Medicine and Hygiene 95, 379383.CrossRefGoogle Scholar
EL-SHEHABI, F. S., KAMHAWI, S. A., SCHANTZ, P. M., CRAIG, P. S. & ABDEL-HAFEZ, S. K. (2000). Diagnosis of canine echinococcosis: comparison of coproantigen detection with necropsy in stray dogs and red foxes from northern Jordan. Parasite 7, 8390.CrossRefGoogle Scholar
ESLAMI, A. & HOSSEINI, S. H. (1998). Echinococcus granulosus infection of farm dogs of Iran. Parasitology Research 84, 205207.CrossRefGoogle Scholar
GASSER, R. B., PARADA, L., ACUNA, A., BURGES, C., LAURENSON, M. K., GULLAND, F. M. D., REICHEL, M. P. & PAOLILLO, E. (1994). Immunological assessment of exposure to Echinococcus granulosus in a rural dog population in Uruguay. Acta Tropica 58, 179185.CrossRefGoogle Scholar
GEMMELL, M. A. (1990). Australasian contributions to an understanding of the epidemiology and control of hydatid disease caused by Echinococcus granulosus past, present and future. International Journal for Parasitology 20, 431456.CrossRefGoogle Scholar
GEMMELL, M. A., LAWSON, J. R. & ROBERTS, M. G. (1986). Population dynamics in echinococcosis and cysticercosis: biological parameters of Echinococcus granulosus in dogs and sheep. Parasitology 92, 599620.CrossRefGoogle Scholar
GEMMMELL, M. A., LAWSON, J. R. & ROBERTS, M. G. (1987). Population dynamics in echinococcosis and cysiticercosis. Evaluation of the biological parameters of Taenia hydatigina and Taenia ovis and comparison with those of Echinococcus granulosus. Parasitology 94, 161180.Google Scholar
HARRIS, R. E., REVFEIM, K. J. A. & HEATH, D. D. (1980). Stimulating control strategies for control of Echinococcus granulosus, Taenia hydatigena and T. ovis. Journal of Hygiene 84, 389404.CrossRefGoogle Scholar
HEATH, D. D., JENSEN, O. & LIGHTOWLERS, M. J. (2002). Progress in control of hydatidosis using vaccination – a review of formulation and delivery of the vaccine and recommendations for practical use in control programmes. Acta Tropica 85, 211221.Google Scholar
HEATH, D. D. & LAWRENCE, S. B. (1978). The effects of Mebendazole and Praziquantel on the cysts of Echinococcus granulosus, Taenia hydatigena and T. ovis in sheep. New Zealand Veterinary Journal 26, 1115.CrossRefGoogle Scholar
HEATH, D. D. & LAWRENCE, S. B. (1996). Antigenic polypeptides of Echinococcus granulosus oncospheres and definition of protective molecules. Parasite Immunology 18, 347357.CrossRefGoogle Scholar
HEATH, D. D. & LAWRENCE, S. B. (1981). Echinococcus granulosus cysts: early development in vitro in the presence of serum from infected sheep. International Journal for Parasitology 11, 261266.CrossRefGoogle Scholar
HEATH, D. D. & LAWRENCE, S. B. (1991). Daily egg-production of dogs infected with Echinococcus granulosus. XV extraordinary congress for the celebration of the 50 years of A.I.H. Archivos Internacionales de la Hidatidosis XXX, 321328.Google Scholar
HOFER, S., GLOOR, S., MULLER, U., MATHIS, A., HEGGLIN, D. & DEPLAZES, P. (2000). High prevalence of Echinococcus multilocularis in urban red foxes (Vulpes vulpes) and vole (Arvicola terrestris) in the city of Zürich, Switzerland. Parasitology 120, 135142.CrossRefGoogle Scholar
JONES, A. & WALTERS, T. M. H. (1992). A survey of taeniid cestodes in farm dogs in mid-Wales. Annals of Tropical Medicine and Parasitology 86, 137142.CrossRefGoogle Scholar
LARRIEU, E. J., COSTA, M. T., DEL CARPIO, M., MOGUILLANSKY, S., BIANCHI, G. & YADON, Z. E. (2002). A case control study of the risk factors for cystic echinococcosis among the children of Rio Negro province, Argentina. Annals of Tropical Medicine and Parasitology 96, 4352.CrossRefGoogle Scholar
LAHMAR, S., KILANI, M. & TORGERSON, P. R. (2001). Frequency distribution of Echinococcus granulosus and other helminths in stray dogs in Tunisia. Annals of Tropical Medicine and Parasitology 95, 6976.CrossRefGoogle Scholar
LAHMAR, S., KILANI, M., TORGERSON, P. R. & GEMMELL, M. A. (1999). Echinococcus granulosus larvae in the livers of sheep in Tunisia: the effects of host age. Annals of Tropical Medicine and Parasitology 93, 7581.CrossRefGoogle Scholar
LAWSON, J. R. & GEMMELL, M. A. (1983). Hydatidosis and cysticercosis: the dynamics of transmission. Advances in Parasitology 22, 261308.CrossRefGoogle Scholar
LAWSON, J. R. & GEMMELL, M. A. (1990). Transmission of taeniid tapeworm eggs via blowflies to intermediate hosts. Parasitology 100, 143146.CrossRefGoogle Scholar
LIU, F. J. (1993). Prevalence of Echinococcus granulosus in dogs in the Xinjiang Uygur Autonomous Region, PRC. In Compendium on Cystic Echinococcosis with Special Reference to the Xinjiang Uygur Autonomous Region, The People's Republic Of China (ed. Anderson, F. L.), pp. 168176. Provo, UT, USA, Brigham Young University.
LIGHTOWLERS, M. W. & GAUCI, C. G. (2001). Vaccines against cysticercosis and hydatidosis. Veterinary Parasitology 101, 337352.CrossRefGoogle Scholar
LIGHTOWLERS, M. W., LAWRENCE, S. B., GAUCCI, C. G., YOUNG, J., RALSTON, M. J., MAAS, D. & HEATH, D. D. (1996). Vaccination against hydatidosis using a defined recombinant antigen. Parasite Immunology 18, 457462.CrossRefGoogle Scholar
MacPHERSON, C. N. L., WACHIRA, T. W., ZEHLE, E., ROMIG, T. & MacPHERSON, C. (1986). Hydatid disease research and control in Turkana. IV. The pilot control programme. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 196200.CrossRefGoogle Scholar
MING, R., TOLLEY, H. D., ANDERSEN, F. L., CHAI, J. & SULTAN, Y. (1992 a). Frequency distribution of Echinococcus granulosus hydatid cysts in sheep populations in the Xinjiang Uygur Autonomous Region, China. Veterinary Parasitology 44, 6775.Google Scholar
MING, R., TOLLEY, H. D., ANDERSEN, F. L., CHAI, J. & CHANG, Q. (1992 b). Frequency distribution of Echinococcus granulosus in dog populations in the Xinjiang Uygur Autonomous Region, China. Veterinary Parasitology 43, 233241.Google Scholar
MUKBEL, R. M., TORGERSON, P. R. & ABO-SHEHADA, M. N. (2000). Prevalence of hydatidosis among donkeys in northern Jordan. Veterinary Parasitology 88, 3542.CrossRefGoogle Scholar
OUHELLI, H., KADIRI, A., EL HASNAOUI, M. & KACHANI, M. (1997). Prevalence of Echinococcus granulosus in dogs in Morocco and potential role of dogs in transmission of cystic Echinococcosis. In Compendium on Cystic Echinococcosis in Africa and in Middle Eastern Countries with Special Reference to Morocco (ed. Andersen, Ouhelli, H. & Kachani, M.), pp. 145155. Provo, UT, USA, Brigham Young University Print Services.
PARADA, L., CABRERA, P., BURGES, C., ACUNA, A., BARCELONA, C., LAURENSON, M. K., GULLAND, F. M. D., AGULLA, J., PARIETTI, S., PAOLILLO, E. & BOTTA, B. (1995). Echinococcus granulosus infections of dogs in the Durano region of Uruguay. Veterinary Record 136, 389391.CrossRefGoogle Scholar
ROBERTS, M. G., LAWSON, J. R. & GEMMELL, M. A. (1986). Population dynamics of echinococcosis and cysticercosis: mathematical model of the life cycles of Echinococcus granulosus. Parasitology 92, 621641.CrossRefGoogle Scholar
ROBERTS, M. G., LAWSON, J. R. & GEMMELL, M. A. (1987). Population dynamics of echinococcosis and cysticercosis: mathematical model of the life cycles of Taenia hydatigena and Taenia ovis. Parasitology 94, 181197.CrossRefGoogle Scholar
SHAW, D. J., GRENFELL, B. T. & DOBSON, A. P. (1998). Patterns of macroparasite aggregation in wildlife host populations. Parasitology 117, 597610.CrossRefGoogle Scholar
SWEATMAN, G. K. & WILLIAMS, R. J. (1963). Comparative studies on the biology and morphology of Echinococcus granulosus from domestic livestock, moose and reindeer. Parasitology 53, 339390.CrossRefGoogle Scholar
SWEATMAN, G. K., WILLIAMS, R. J., MORIATY, K. M. & HENSHALL, T. C. (1963). On acquired immunity to Echinococcus granulosus in sheep. Research in Veterinary Science 4, 187198.Google Scholar
THOMPSON, R. C. A. & McMANUS, D. P. (2001). Aetiology: Parasites and Life Cycles. In Manual on Echinococcosis in Humans and Animals – A Public Health Problem of Global Concern (ed. Eckert J., Gemmell, M. A., Meslin, F.-X. and Pawlowski, Z. S. ), pp. 119. Paris, World Organisation for Animal Health (OIE).
THOMPSON, R. C. A. & McMANUS, D. P. (2002). Towards a taxonomic revision of the genus Echinococcus. Trends in Parasitology 18, 452457.CrossRefGoogle Scholar
TORGERSON, P. R. (2003). The use of mathematical models to simulate control options for echinococcosis. Acta Tropica 85, 211221.CrossRefGoogle Scholar
TORGERSON, P. R., KARAEVA, R. R., CORKERI, N., ABDYJAPAROV, T. A. & KUTTUBAEV, O. T. (2003 c). Cystic echinococcosis in humans in Kyrgystan: an epidemiological study. Acta Tropica 85, 5161.Google Scholar
TORGERSON, P. R., PILKINGTON, J., GULLAND F. M. D. & GEMMELL, M. A. (1995). Further evidence for the long distance dispersal of taeniid eggs. International Journal for Parasitology 25, 265267.CrossRefGoogle Scholar
TORGERSON, P. R., SHAIKENOV, B. S., RYSMUKHAMBETOVA, A. T., ABDYBEKOVA, A. M., USENBAYEV, A. E. & BAITURSINOV, K. K. (2003 a). Modelling the transmission dynamics of Echinococcus granulosus in sheep and cattle in Kazakhstan Veterinary Parasitology 114, 143153.Google Scholar
TORGERSON, P. R., SHAIKENOV, B. S., RYSMUKHAMBETOVA, A. T., ABDYBEKOVA, A. M., USENBAYEV, A. E. & BAITURSINOV, K. K. (2003 b). Modelling the transmission dynamics of Echinococcus granulosus in dogs in rural Kazakhstan. Parasitology 126, 417424.Google Scholar
TORGERSON, P. R., WILLIAMS, D. H. & ABO-SHEHADA, M. N. (1998). Modelling the prevalence of Echinococcus and Taenia species in small ruminants of different ages in northern Jordan. Veterinary Parasitology 79, 3551.CrossRefGoogle Scholar
WACHIRA, T. M., MacPHERSON, C. N. L. & GATHUMA, J. M. (1991). Release and survival of Echinococcus eggs in different environments in Turkana, and their possible impact on the incidence of hydatidosis in man and livestock. Journal of Helminthology 65, 5561.CrossRefGoogle Scholar
WANG, Q., QIU, J., SCHANTZ, P., HE, J., ITO, A. & LIU, F. (2001). Investigation of risk factors for development of human hydatidosis among households raising livestock in Tibetan areas of western Sichuan Province. Chinese Journal of Parasitology and Parasitic Diseases 19, 9396.Google Scholar
WILSON, K., GRENFELL, B. T. & SHAW, D. J. (1996). Analysis of aggregated parasite distributions: a comparison of methods. Functional Ecology 10, 592601.CrossRefGoogle Scholar
YONG, W. K., HEATH, D. D. & Van KNAPEN, F. (1984). Comparison of cestode antigens in an enzyme-linked immunosorbent assay for the diagnosis of Echinococcus granulosus, Taenia hydatigena and T. ovis infections in sheep. Research in Veterinary Science 36, 2431.Google Scholar
ZHANG, W., YOU, H., ZHANG, Z., TURSON, G., HASYET, A. & McMANUS, D. P. (2001). Further studies on an intermediate host murine model showing that a primary Echinococcus granulosus infection is protective against subsequent oncospheral challenge. Parasitology International 50, 279283.CrossRefGoogle Scholar