Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-28T16:26:02.217Z Has data issue: false hasContentIssue false

Crowding effect on adult growth, pre-patent period and egg shedding of Fasciola hepatica

Published online by Cambridge University Press:  04 July 2006

M. A. VALERO
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Av. Vicent Andrés Estellés s/n, 46100 Burjassot – Valencia, Spain
M. DE RENZI
Affiliation:
Instituto Cavanilles de Biodiversidad y Biología Evolutiva, Universidad de Valencia, Apartado Postal 22085, 46071 Paterna-Valencia, Spain
M. PANOVA
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Av. Vicent Andrés Estellés s/n, 46100 Burjassot – Valencia, Spain
M. A. GARCIA-BODELON
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Av. Vicent Andrés Estellés s/n, 46100 Burjassot – Valencia, Spain
M. V. PERIAGO
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Av. Vicent Andrés Estellés s/n, 46100 Burjassot – Valencia, Spain
D. ORDOÑEZ
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Av. Vicent Andrés Estellés s/n, 46100 Burjassot – Valencia, Spain
S. MAS-COMA
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Av. Vicent Andrés Estellés s/n, 46100 Burjassot – Valencia, Spain

Abstract

Fascioliasis pathogenesis depends on fluke burden. In human hyperendemic zones, individual infection intensities reach very high levels and the majority of infected subjects should be in the advanced chronic phase. The rat model offers a useful approach for pathological research in the advanced chronic period. The influence of infection intensity per rat on fluke development, pre-patent period and egg shedding (eggs/g faeces/worm) was analysed in 3 groups (I: 1–3 worms/rat; II: 4–6; III: 7–9). Ontogenetic trajectories of fluke body measures followed a logistic model. Results showed that when the burden increases, the maximum values of fluke measures decrease. The crowding effect is manifest when fluke measures approximate their maximums in the advanced chronic stage. The pre-patent period and egg production decrease when the burden increases. This means that measurements of eggs per gramme of faeces tend to underestimate the fluke burden. The present study demonstrates how to quantify the fascioliasis experimental rat model crowding effect on adult growth, pre-patent period and egg production. This quantification may be of great interest in epidemiological studies and in experimental research on the in vivo actions of different anthelminthic drugs and vaccines, pathology, immunology and resistance studies.

Type
Research Article
Copyright
© 2006 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

Alberch, P., Gould, S. J., Oster, F. and Wake, D. B. ( 1979). Size and shape in ontogeny and phylogeny. Paleobiology 5, 296317.CrossRefGoogle Scholar
Bjorland, J., Bryan, R. T., Strauss, W., Hillyer, G. V. and Mcauley, J. B. ( 1995). An outbreak of acute fascioliasis among Aymara Indians in the Bolivian Altiplano. Clinical Infectious Diseases 21, 12281233.CrossRefGoogle Scholar
Boray, J. C. ( 1967). Studies on experimental infections with Fasciola hepatica with particular reference to acute fascioliasis in sheep. Annals of Tropical Medicine and Parasitology 61, 439444.CrossRefGoogle Scholar
Boray, J. C. ( 1969). Experimental fascioliasis in Australia. Advances in Parasitology 8, 95210.CrossRefGoogle Scholar
Bush, A. O. and Lotz, J. M. ( 2000). The ecology of “crowding”. Journal of Parasitology 86, 212213.Google Scholar
Chatterjee, K. D. ( 1975). Fasciola hepatica. In Parasitology (Protozoology and Helminthology) 10th Edn ( ed. Chatterjee, K. D.), pp. 146148. S.N. Guha Ray At Sree Saraswaty Press Ltd, Calcutta.
Chen, M. G. and Mott, K. E. ( 1990). Progress in assessment of morbidity due to Fasciola hepatica infection: a review of recent literature. Tropical Diseases Bulletin 87, R1R38.Google Scholar
Coelho, P. M., Souza, R. C., Bredt, A. and Souza-Neto, J. A. ( 1976). The crowding effect in Schistosoma mansoni infection of hamsters: influence on worm size. Revista do Instituto de Medecina Tropical do São Paulo 18, 440442.Google Scholar
Dan, M., Lichtenstein, D., Lavochkin, J., Stavorowsky, M., Jedwab, M. and Shibolet, S. ( 1981). Human fascioliasis in Israel, an imported case. Israel Journal of Medical Sciences 17, 430432.Google Scholar
De Renzi, M. ( 1988). Shell coiling in some larger Foraminifera: general comments and problems. Paleobiology 14, 387400.CrossRefGoogle Scholar
De Renzi, M. ( 1995). Theoretical morphology of logistic coiling exemplified by tests of genus Alveolina (larger Foraminifera). Neues Jahrbuch für Geologie und Palaeontologie 195, 241251.CrossRefGoogle Scholar
Esteban, J. G., Flores, A., Aguirre, C., Strauss, W., Angles, R. and Mas-Coma, S. ( 1997 a). Presence of very high prevalence and intensity of infection with Fasciola hepatica among Aymara children from the Northern Bolivian Altiplano. Acta Tropica 66, 114.Google Scholar
Esteban, J. G., Flores, A., Angles, R., Strauss, W., Aguirre, C. and Mas-Coma, S. ( 1997 b). A population-based coprological study of human fascioliasis in a hyperendemic area of the Bolivian Altiplano. Tropical Medicine and International Health 2, 695699.Google Scholar
Esteban, J. G., Flores, A., Angles, R. and Mas-Coma, S. ( 1999). High endemicity of human fascioliasis between Lake Titicaca and La Paz valley, Bolivia. Transactions of the Royal Society of Tropical Medicine and Hygiene 93, 151156.CrossRefGoogle Scholar
Foster, J. R. ( 1981). A study of the initiation of biliary hyperplasia in rats infected with Fasciola hepatica. Parasitology 83, 253258.CrossRefGoogle Scholar
Franco, J., Fuman, J. E. and Fried, B. ( 1988). The effects of crowding on adults of Echinostoma revolutum (Digenea: Echinostomatidae) in experimentally infected golden hamsters, Mesocricetus auratus. Journal of Parasitology 74, 240243.CrossRefGoogle Scholar
Fried, B. and Nelson, P. D. ( 1978). Host-parasite relationships of Zygocotyle lunata (Trematoda) in the domestic chick. Parasitology 77, 4955.CrossRefGoogle Scholar
Gulsen, M., Savas, M. C., Koruk, M., Kadayifci, A. and Demirci, F. ( 2006). Fascioliasis: a report of five cases presenting with common bile duct obstruction. The Netherlands Journal of Medicine 64, 1719.Google Scholar
Hillyer, G. V., Soler De Galanes, M., Rodriguez-Perez, J., Bjorland, J., Silva De Lagrava, M., Ramirez Guzman, S. and Bryan, R. T. ( 1992). Use of the Falcon Assay Screening Test – Enzyme-Linked Immunosorbent Assay (FAST-ELISA) and the Enzyme-Linked Immunoelectrotransfer Blot (EITB) to determine the prevalence of human fascioliasis in the Bolivian Altiplano. American Journal of Tropical Medicine and Hygiene 46, 603609.CrossRefGoogle Scholar
Hughes, D. L., Harness, E. and Doy, T. G. ( 1976). The establishment and duration of Fasciola hepatica infections in two strains of rats and the development of acquired resistance. Research in Veterinary Science 20, 207211.Google Scholar
Kabaalio, A., Çubuk, M., Zeno, U., Cevikol, C., Karaali, K., Apaydin, A., Sindel, T. and Lüleci, E. ( 2000). Fascioliasis: US, CT, and MRI findings with new observations. Abdominal Imaging 25, 400404.CrossRefGoogle Scholar
Mas-Coma, S. ( 2004 a). Human fascioliasis: epidemiological patterns in human endemic areas of South America, Africa and Asia. Southeast Asian Journal of Tropical Medicine and Public Health 35, 111.Google Scholar
Mas-Coma, S. ( 2004 b). Human fascioliasis. In World Health Organization (WHO), Waterborne Zoonoses: Identification, Causes and Control ( ed. Cotruvo, J. A., Dufour, A., Rees, G., Bartram, J., Carr, R., Cliver, D. O., Craun, G. F., Fayer, R. and Gannon, V. P. J.), pp. 305322. IWA Publishing, London.Google Scholar
Mas-Coma, S. ( 2005). Epidemiology of fascioliasis in human endemic areas. Journal of Helminthology 79, 207216.CrossRefGoogle Scholar
Mas-Coma, S. and Bargues, M. D. ( 1997). Human liver flukes: a review. Research and Reviews in Parasitology 57, 145218.Google Scholar
Mas-Coma, S., Esteban, J. G. and Bargues, M. D. ( 1999 a). Epidemiology of human fascioliasis: a review and proposed new classification. Bulletin of the World Health Organization 77, 340346.Google Scholar
Mas-Coma, S., Bargues, M. D. and Esteban, J. G. ( 1999 b). Human fasciolosis. In Fasciolosis ( ed. Dalton, J. P.), pp. 411434. CAB International Publishing, Wallingford, Oxon.
Mas-Coma, S., Bargues, M. D. and Valero, M. A. ( 2005). Fascioliasis and other plantborne trematode zoonoses. International Journal for Parasitology 35, 12551278.CrossRefGoogle Scholar
Mas-Coma, S., Bargues, M. D., Marty, A. M. and Neafie, R. C. ( 2000). Hepatic Trematodiases. In Pathology of Infectious Diseases, Vol. 1. Helminthiases ( ed. Meyers, W. M., Neafie, R. C., Marty, A. M. and Wear, D. J.), pp. 6992. Armed Forces Institute of Pathology and American Registry of Pathology, Washington, DC.
Mas-Coma, S., Bargues, M. D., Valero, M. A. and Fuentes, M. V. ( 2003). Adaptation capacities of Fasciola hepatica and their relationships with human fascioliasis: from below sea level up to the very high altitude. In Taxonomy, Ecology and Evolution of Metazoan Parasites Vol. 2 ( ed. Combes, C. and Jourdane, J.), pp. 81123. Presses Universitaires de Perpignan, Perpignan.
Mas-Coma, S., Angles, R., Strauss, W., Esteban, J. G., Oviedo, J. A. and Buchon, P. ( 1995). Human fasciolasis in Bolivia: a general analysis and a critical review of existing data. Research and Reviews in Parasitology 55, 7393.Google Scholar
Mas-Coma, S., Angles, R., Esteban, J. G., Bargues, M. D., Buchon, P., Franken, M. and Strauss, W. ( 1999 c). The Northern Bolivian Altiplano: a region highly endemic for human fascioliasis. Tropical Medicine and International Health 4, 454467.Google Scholar
Montgomerie, R. F. ( 1928). Observations on artificial infestation of sheep with Fasciola hepatica and on a phase in the development of the parasite. Journal of Helminthology 6, 167174.CrossRefGoogle Scholar
Nollen, P. M. ( 1989). Effects of concurrent infections on growth, development, distribution, and infectivity of adult of Philophthalmus megalurus and Philophthalmus gralli. Journal of Parasitology 75, 102107.CrossRefGoogle Scholar
Norusis, J. M. ( 1994). SPSS Advanced Statistics. Chicago, SPSS, Inc.
O'Neill, S. M., Parkinson, M., Strauss, W., Angles, R. and Dalton, J. P. ( 1998). Immunodiagnosis of Fasciola hepatica (Fascioliasis) in a human population in the Bolivian Altiplano using purified cathepsin L cysteine proteinase. American Journal of Tropical Medicine and Hygiene 58, 417423.CrossRefGoogle Scholar
Rajasekariah, G. R. and Howell, M. J. ( 1977). Fasciola hepatica in rats: effects of age and ineffective dose. International Journal for Parasitology 7, 119121.CrossRefGoogle Scholar
Reddington, J. J., Leid, R. W. and Wescott, R. B. ( 1984). Effect of inoculum on the size and location of Fasciola hepatica subsequently recovered from the livers of rats. Veterinary Parasitology 14, 1319.CrossRefGoogle Scholar
Roberts, L. S. ( 2000). The crowding effect revisited. Journal of Parasitology 86, 209211.Google Scholar
Ross, J. G. ( 1965). Experimental infections of cattle with Fasciola hepatica: a comparison of low and high infection rates. Nature, London 208, 907.CrossRefGoogle Scholar
Shostak, A. W. and Scott, M. E. ( 1993). Detection of density-dependent growth and fecundity of helminths in natural infections. Parasitology 106, 527539.CrossRefGoogle Scholar
Sykes, A. R., Coop, R. L. and Rushton, B. ( 1980). Chronic and subclinical fascioliasis in sheep: effects on food intake, food utilization and blood constituents. Research in Veterinary Science 28, 6370.Google Scholar
Thorpe, E. ( 1965). Liver damage and the host-parasite relationship in experimental fascioliasis in the albino rat. Research in Veterinary Science 6, 498509.Google Scholar
Valero, M. A. and Mas-Coma, S. ( 2000). Comparative infectivity of Fasciola hepatica metacercariae from isolates of the main and secondary reservoir animal host species in the Bolivian Altiplano high human endemic region. Folia Parasitologica 47, 1722.CrossRefGoogle Scholar
Valero, M. A., De Renzi, M. and Mas-Coma, S. ( 1991). Ontogenetic trajectories: a new approach in the study of parasite development, with special reference to Digenea. Research and Reviews in Parasitology 51, 125138.Google Scholar
Valero, M. A., Marcos, M. D. and Mas-Coma, S. ( 1996). A mathematical model for the ontogeny of Fasciola hepatica in the definitive host. Research and Reviews in Parasitology 56, 1320.Google Scholar
Valero, M. A., Varea, M. T. and Marin, R. ( 2000). Fasciola hepatica: lithogenic capacity in experimentally infested rats and chemical determination of the main stone components. Parasitology Research 86, 558562.CrossRefGoogle Scholar
Valero, M. A., Panova, M. and Mas-Coma, S. ( 2001 a). Development differences in the uterus of Fasciola hepatica between livestock liver fluke populations from Bolivian highland and European lowlands. Parasitology Research 87, 337342.Google Scholar
Valero, M. A., Panova, M. and Mas-Coma, S. ( 2005). Phenotypic analysis of adults and eggs of Fasciola hepatica by computer image analysis system. Journal of Helminthology 79, 217225.CrossRefGoogle Scholar
Valero, M. A., Marcos, M. D., Fons, R. and Mas-Coma, S. ( 1998). Fasciola hepatica development in the experimentally infected black rat Rattus rattus. Parasitology Research 84, 188194.CrossRefGoogle Scholar
Valero, M. A., Darce, N. A., Panova, M. and Mas-Coma, S. ( 2001 b). Relationships between host species and morphometric patterns in Fasciola hepatica adults and eggs from the Northern Bolivian Altiplano hyperendemic region. Veterinary Parasitology 102, 85100.Google Scholar
Valero, M. A., Marcos, M. D., Comes, A. M., Sendra, M. and Mas-Coma, S. ( 1999). Comparison of adult liver flukes from highland and lowland populations of Bolivian and Spanish sheep. Journal of Helminthology 73, 341345.CrossRefGoogle Scholar
Valero, M. A., Panova, M., Comes, A. M., Fons, R. and Mas-Coma, S. ( 2002). Patterns in size and shedding of Fasciola hepatica eggs by naturally and experimentally infected murid rodents. Journal of Parasitology 88, 308313.CrossRefGoogle Scholar
Valero, M. A., Santana, M., Morales, M., Hernandez, J. L. and Mas-Coma, S. ( 2003). Risk of gallstone disease in advanced chronic phase of fascioliasis: an experimental study in a rat model. Journal of Infectious Diseases 188, 787793.CrossRefGoogle Scholar
Wilson, R. A., Smith, G. and Thomas, M. R. ( 1982). Fascioliasis. In Population Dynamics of Infectious Diseases. Theory and Applications. Population and Community Biology Series ( ed. Anderson, R. M.), pp. 262361. Chapman and Hall, London-New York.CrossRef
Yao, G., Huffman, J. E. and Fried, B. ( 1991). The effects of crowding on adults of Echinostoma caproni in experimentally infected golden hamsters. Journal of Helminthology 65, 248254.CrossRefGoogle Scholar