Hostname: page-component-8448b6f56d-sxzjt Total loading time: 0 Render date: 2024-04-25T04:07:14.665Z Has data issue: false hasContentIssue false
  • English
  • Français

Phenotypes of intermediate forms of Fasciola hepatica and F. gigantica in buffaloes from Central Punjab, Pakistan

Published online by Cambridge University Press:  04 June 2013

K. Afshan ,
M.A. Valero ,
M. Qayyum ,
R.V. Peixoto ,
A. Magraner  and
S. Mas-Coma
K. Afshan
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Av. Vicent Andrés Estellés s/n, 46100Burjassot, Valencia, Spain Department of Zoology, Pir Mehr Ali Shah-Arid Agriculture University, Rawalpindi46300, Pakistan
M.A. Valero*
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Av. Vicent Andrés Estellés s/n, 46100Burjassot, Valencia, Spain
M. Qayyum
Affiliation:
Department of Zoology, Pir Mehr Ali Shah-Arid Agriculture University, Rawalpindi46300, Pakistan
R.V. Peixoto
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Av. Vicent Andrés Estellés s/n, 46100Burjassot, Valencia, Spain
A. Magraner
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Av. Vicent Andrés Estellés s/n, 46100Burjassot, Valencia, Spain
S. Mas-Coma
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Av. Vicent Andrés Estellés s/n, 46100Burjassot, Valencia, Spain
*
*Fax: +34–96-354–44-90 E-mail: madela.valero@uv.es
Get access Rights & Permissions [Opens in a new window]

Abstract

Fascioliasis is an important food-borne parasitic disease caused by the two trematode species, Fasciola hepatica and Fasciola gigantica. The phenotypic features of fasciolid adults and eggs infecting buffaloes inhabiting the Central Punjab area, Pakistan, have been studied to characterize fasciolid populations involved. Morphometric analyses were made with a computer image analysis system (CIAS) applied on the basis of standardized measurements. Since it is the first study of this kind undertaken in Pakistan, the results are compared to pure fasciolid populations: (a) F. hepatica from the European Mediterranean area; and (b) F. gigantica from Burkina Faso; i.e. geographical areas where both species do not co-exist. Only parasites obtained from bovines were used. The multivariate analysis showed that the characteristics, including egg morphometrics, of fasciolids from Central Punjab, Pakistan, are between F. hepatica and F. gigantica standard populations. Similarly, the morphometric measurements of fasciolid eggs from Central Punjab are also between F. hepatica and F. gigantica standard populations. These results demonstrate the existence of fasciolid intermediate forms in endemic areas in Pakistan.

Type
Research Papers
Information
Journal of Helminthology , Volume 88 , Issue 4 , December 2014 , pp. 417 - 426
Copyright
Copyright © Cambridge University Press 2013 

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

Akahane, H., Harada, Y. & Oshima, T. (1970) Patterns of the variation of the common liver fluke (Fasciola sp.) in Japan. III. Comparative studies on the external form, size of egg and number of eggs in uterus of the fluke in cattle, goat and rabbit. Japanese Journal of Parasitology 6, 619–627.Google Scholar
Anonymous, (2001) The proven solution for image analysis. pp. 8/1–8/16Image-Pro® Plus, Version 4.5 for WindowsTM, start-up guide. Silver Spring, Maryland, USA, Media Cybernetics, Inc.Google Scholar
Ashrafi, K., Massoud, J., Holakouei, K., Mahmoodi, M., Joafshani, M.A., Valero, M.A., Fuentes, M.V., Khoubbane, M., Artigas, P., Bargues, M.D. & Mas-Coma, S. (2004) Evidence suggesting that Fasciola gigantica might be the most prevalent causal agent of fascioliasis in northern Iran. Iranian Journal of Public Health 33, 31–37.Google Scholar
Ashrafi, K., Valero, M.A., Massoud, J., Sobhani, A., Solaymani-Mohammadi, S., Conde, P., Khoubbane, M., Bargues, M.D. & Mas-Coma, S. (2006a) Plant-borne human contamination by fascioliasis. American Journal of Tropical Medicine and Hygiene 75, 295–302.Google Scholar
Ashrafi, K., Valero, M.A., Panova, M., Massoud, J. & Mas-Coma, S. (2006b) Phenotypic analysis of adults of Fasciola hepatica, Fasciola gigantica and intermediate forms from the endemic region of Gilan, Iran. Parasitology International 55, 249–260.Google Scholar
Ashrafi, K., Massoud, J., HolakoueiNainei, K., Jo-Afshani, M.A., Mahmoodi, M., Ebedati, N., Rezvani, S.M., Artigas, P., Bargues, M.D. & Mas-Coma, S. (2007) Nuclear ribosomal DNA ITS-2 sequence characterization of Fasciola hepatica and Galba truncatula. Iranian Journal of Public Health 36, 42–49.Google Scholar
Bargues, M.D. & Mas-Coma, S. (2005) Reviewing lymnaeid vectors of fascioliasis by ribosomal DNA sequence analyses. Journal of Helminthology 79, 257–267.CrossRefGoogle ScholarPubMed
Bookstein, F.L. (1989) Size and shape: a comment on semantics. Systematic Zoology 38, 173–180.Google Scholar
Charlier, J., Duchateau, L., Claerebout, E., Williams, D. & Vercruysse, J. (2007) Associations between anti-Fasciola hepatica antibody levels in bulk tank milk samples and production parameters in dairy herds. Preventive Veterinary Medicine 78, 57–66.Google Scholar
Chaudhry, A.H. & Niaz, M. (1984) Liver fluke – a constant threat to livestock development. Pakistan Veterinary Journal 4, 42–43.Google Scholar
Chu, J.K. & Kim, Y.K. (1967) Taxonomical study on the Fasciolidae in Korea. Korean Journal of Parasitology 5, 139–146.Google Scholar
Cruz, R.V., Harasawa, H., Lal, M., Wu, S., Anokhin, Y., Punsalmaa, B., Honda, Y., Jafari, M., Li, C. & Huu Ninh, N. (2007) Asia. pp. 469–506in Parry, M.L., Canziani, O.F., Palutikof, J.P., van der Linden, P.J. & Hanson, C.E. (Eds) Climate change 2007: impacts, adaptation and vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, UK, Cambridge University Press.Google Scholar
Dos Reis, S.P., Pessoa, L.M. & Strauss, R.E. (1990) Application of size-free canonical discriminant analysis to studies of geographic differentiation. Brazilian Journal of Genetics 13, 509–520.Google Scholar
Dujardin, J.P. (2008) Morphometrics applied to medical entomology. Infection, Genetics and Evolution 8, 875–890.Google Scholar
Dujardin, J.P. & Le Pont, F. (2004) Geographical variation of metric properties within the neotropical sandflies. Infection, Genetics and Evolution 4, 353–359.Google Scholar
Elitok, B., Elitok, O.M. & Kabu, M. (2006) Field trial on comparative efficacy of four fasciolicides against natural liver fluke infection in cattle. Veterinary Parasitology 135, 279–285.Google Scholar
Farooq, A.B. & Khan, A.H. (2004) Climate change perspective in Pakistan. Proceedings of the Capacity Building APN Workshop on Global Change Research. Islamabad, pp. 39–46.Google Scholar
Fuentes, M.V., Valero, M.A., Bargues, M.D., Esteban, J.G., Angles, R. & Mas-Coma, S. (1999) Analysis of climatic data and forecast indices for human fascioliasis at very high altitude. Annals of Tropical Medicine and Parasitology 93, 835–850.Google Scholar
Fuentes, M.V., Malone, J.B. & Mas-Coma, S. (2001) Validation of a mapping and predicting model for human fasciolosis transmission in Andean very high altitude endemic areas using remote sensing data. Acta Tropica 79, 87–95.Google Scholar
Girones, N., Valero, M.A., Garcia-Bodelon, M.A., Chico-Calero, M.I., Punzon, C., Fresno, M. & Mas-Coma, S. (2007) Immune supression in advanced chronic fascioliasis: an experimental study in a rat model. Journal of infectious Diseases 195, 1504–1512.Google Scholar
Itagaki, T., Sakaguchi, K., Terasaki, K., Sasaki, O., Yoshihara, S. & Van Dung, T. (2009) Occurrence of spermic diploid and aspermic triploid forms of Fasciola in Vietnam and their molecular characterization based on nuclear and mitochondrial DNA. Parasitology International 58, 81–85.Google Scholar
Kendall, S.B. (1954) Fascioliasis in Pakistan. Annals of Tropical Medicine and Parasitology 48, 307–313.Google Scholar
Kendall, S.B. & Parfitt, J.W. (1959) Studies on the susceptibility of some species of Lymnaea to infection with Fasciola gigantica and F. hepatica. Annals of Tropical Medicine and Parasitology 53, 220–227.CrossRefGoogle Scholar
Khan, M.K., Sajid, M.S., Khan, M.N., Iqbal, Z. & Iqbal, M.U. (2009) Bovine fasciolosis: prevalence, effects of treatment on productivity and cost benefit analysis in five districts of Punjab, Pakistan. Research in Veterinary Science 87, 70–75.Google Scholar
Khan, M.N., Sajid, M.S., Khan, M.K., Iqbal, Z. & Hussain, A. (2010) Gastrointestinal helminthiasis: prevalence and associated determinants in domestic ruminants of district Toba Tek Singh, Punjab, Pakistan. Parasitology Research 107, 787–794.Google Scholar
Kimura, S., Shimizu, A. & Kawano, J. (1984) Morphological observation on liver fluke detected from naturally infected carabaos in the Philippines. The Science Reports of the Faculty of Agriculture, Kobe University 16, 353–357.Google Scholar
Klingenberg, C.P. (1996) Multivariate allometry. pp. 23–49in Marcus, L.F., Corti, M., Loy, A., Naylor, G.J.P. & Slice, D. (Eds) Advances in morphometrics. Proceedings of the 1993 NATO-ASI on Morphometrics, NATO ASI, Ser. A, Life Sciences. New York, Plenum Publishers.Google Scholar
Maqbool, A., Arshad, M.J., Mahmood, F. & Hussain, A. (1994) Epidemiology and chemotherapy of fascioliasis in buffaloes. Assiut Veterinary Medical Journal 30, 115–123.Google Scholar
Maqbool, A., Hayat, C.S., Akhtar, T. & Hashmi, H.A. (2002) Epidemiology of fasciolosis in buffaloes under different managemental conditions. Veterinarski Arhiv 72, 221–228.Google Scholar
Marcilla, A., Bargues, M.D. & Mas-Coma, S. (2002) A PCR-RFLP assay for the distinction between Fasciola hepatica and F. gigantica. Molecular and Cellular Probes 16, 327–333.Google Scholar
Mas-Coma, S. (2005) Epidemiology of fascioliasis in human endemic areas. Journal of Helminthology 79, 207–216.Google Scholar
Mas-Coma, S. & Bargues, M.D. (1997) Human liver flukes: a review. Research and Reviews in Parasitology 57, 145–218.Google Scholar
Mas-Coma, S., Bargues, M.D. & Valero, M.A. (2005) Fascioliasis and other plant-borne trematode zoonosis. International Journal of Parasitology 35, 1255–1278.Google Scholar
Mas-Coma, S., Valero, M.A. & Bargues, M.D. (2008) Effects of climate change on animal and zoonotic helminthiases. Revue Scientifique et Technique de l'Office Internationale des Epizooties 27, 443–457.Google Scholar
Mas-Coma, S., Valero, M.A. & Bargues, M.D. (2009) Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control. Advances in Parasitology 69, 41–146.Google Scholar
Masud, F.S. & Majid, A. (1984) Incidence of fascioliasis in buffaloes and cattle of Multan division. Pakistan Veterinary Journal 4, 33–34.Google Scholar
Moghaddam, A.S., Massoud, J., Mahmoodi, M., Mahvi, A.H., Periago, M.V., Artigas, P., Fuentes, M.V., Bargues, M.D. & Mas-Coma, S. (2004) Human and animal fascioliasis in Mazandaran province, northern Iran. Parasitology Research 94, 61–69.CrossRefGoogle ScholarPubMed
Oshima, T., Akahane, H. & Shimazu, T. (1968a) Patterns of the variation of the common liver fluke (Fasciola sp.) in Japan. I. Variations in the sizes and shapes of the worms and eggs. Japanese Journal of Parasitology 17, 97–105(in Japanese with English summary).Google Scholar
Oshima, T., Akahane, H., Koyama, H., Shimazu, T. & Harada, Y. (1968b) Patterns of the variation of the common liver fluke (Fasciola sp.) in Japan. II. A comparative study of the flukes from cattle and goat. Japanese Journal of Parasitology 17, 534–539(in Japanese with English summary).Google Scholar
Peng, M., Ichinomiya, M., Ohtori, M., Ichikawa, M., Shibahara, T. & Itagaki, T. (2009) Molecular characterization of Fasciola hepatica, Fasciola gigantica, and aspermic Fasciola sp. in China based on nuclear and mitochondrial DNA. Parasitology Research 105, 809–815.Google Scholar
Periago, M.V., Valero, M.A., Panova, M. & Mas-Coma, S. (2006) Phenotypic comparison of allopatric populations of Fasciola hepatica and Fasciola gigantica from European and African bovines using a computer image analysis system (CIAS). Parasitology Research 99, 368–378.Google Scholar
Periago, M.V., Valero, M.A., El Sayed, M., Ashrafi, K., El Wakeel, A., Mohamed, M.Y., Desquesnes, M., Curtale, F. & Mas-Coma, S. (2008) First phenotypic description of Fasciola hepatica/Fasciola gigantica intermediate forms from the human endemic area of the Nile Delta, Egypt. Infection, Genetics and Evolution 8, 51–58.CrossRefGoogle ScholarPubMed
Qureshi, A.W., Tanveer, A., Qureshi, S.W., Maqbool, A., Gill, T.J. & Ali, S.A. (2005) Epidemiology of human fasciolosis in rural areas of Lahore, Pakistan. Punjab University Journal of Zoology 20, 159–168.Google Scholar
Rohlf, F.J. & Marcus, L.F. (1993) A revolution in morphometrics. Trends in Ecology and Evolution 8, 129–132.Google Scholar
Sahba, G.H., Arfaa, F., Faramandian, I. & Jalali, H. (1972) Animal fasciolosis in Khuzestan, Southwestern Iran. Journal of Parasitology 58, 172–176.Google Scholar
Schweizer, G., Braun, U., Deplazes, P. & Torgerson, P.R. (2005) Estimating the financial losses due to bovine fasciolosis in Switzerland. Veterinary Record 157, 188–193.Google Scholar
Siddiqi, M.N. & Shah, S.A.U. (1984) Natural infection of helminths in liver and respiratory tract of cattle of Peshawar and histology of Paramohistomum cervi. Pakistan Veterinary Journal 4, 100–107.Google Scholar
Srimuzipo, P., Komalamisra, C., Choochote, W., Jitpakdi, A., Vanichthanakorn, P., Keha, P., Riyong, D., Sukontasan, K., Komalamisra, N., Sukontasan, K. & Tippawangkosol, P. (2000) Comparative morphometry, morphology of egg and adult surface topography under light and scanning electron microscopies, and metaphase karyotype among three size-races of Fasciola gigantica in Thailand. Southeast Asian Journal of Tropical Medicine and Public Health 31, 366–373.Google Scholar
Terasaki, K., Noda, Y., Shibahara, T. & Itagaki, T. (2000) Morphological comparisons and hypotheses on the origin of polyploids in parthenogenetic Fasciola sp. Journal of Parasitology 86, 724–729.Google ScholarPubMed
Valero, M.A. & 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, 17–22.Google Scholar
Valero, M.A., Marcos, M.D., Fons, R. & Mas-Coma, S. (1998) Fasciola hepatica development in experimentally infected black rat, Rattus rattus. Parasitology Research 84, 188–194.CrossRefGoogle ScholarPubMed
Valero, M.A., Darce, N.A., Panova, M. & Mas-Coma, S. (2001a) Relationships between host species and morphometric patterns in Fasciola hepatica adults and eggs from the Northern Bolivian Altiplano hyperendemic region. Veterinary Parasitology 102, 85–100.Google Scholar
Valero, M.A., Panova, M. & Mas-Coma, S. (2001b) Development differences in the uterus of Fasciola hepatica between livestock liver fluke populations from Bolivian highland and European lowlands. Parasitology Research 87, 337–342.Google Scholar
Valero, M.A., Panova, M., Comes, A.M., Fons, R. & Mas-Coma, S. (2002) Patterns in size and shedding of Fasciola hepatica eggs by naturally and experimentally infected murid rodents. Journal of Parasitology 88, 308–313.Google Scholar
Valero, M.A., Santana, M., Morales, M., Hernandez, J.L. & 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, 787–793.Google Scholar
Valero, M.A., Panova, M. & Mas-Coma, S. (2005) Phenotypic analysis of adults and eggs of Fasciola hepatica by computer image analysis system. Journal of Helminthology 79, 217–225.Google Scholar
Valero, M.A., Navarro, M., Garcia-Bodelon, M.A., Marcilla, A., Morales, M., Garcia, J.E., Hernandez, J.L. & Mas-Coma, S. (2006) High risk of bacterobilia in advanced experimental chronic fasciolosis. Acta Tropica 100, 17–23.Google Scholar
Valero, M.A., Girones, N., Garcia-Bodelon, M.A., Periago, M.V., Chico-Calero, I., Khoubbane, M., Fresno, M. & Mas-Coma, S. (2008) Anaemia in advanced chronic fasciolosis. Acta Tropica 108, 35–43.Google Scholar
Valero, M.A., Perez-Crespo, I., Periago, M.V., Khoubbane, M. & Mas-Coma, S. (2009a) Fluke egg characteristics for the diagnosis of human and animal fascioliasis by Fasciola hepatica and F. gigantica. Acta Tropica 111, 150–159.Google Scholar
Valero, M.A., Ubeira, F.M., Khoubbane, M., Artigas, P., Muiño, L., Mezo, M., Pérez-Crespo, I., Periago, M.V. & Mas-Coma, S. (2009b) MM3-ELISA evaluation of coproantigen release and serum antibody production in sheep experimentally infected with Fasciola hepatica and F. gigantica. Veterinary Parasitology 159, 77–81.Google Scholar
Valero, M.A., Periago, M.V., Pérez-Crespo, I., Rodríguez, E., Perteguer, M.J., Gárate, T., González-Barberá, E.M. & Mas-Coma, S. (2012a) Assessing the validity of an ELISA test for the serological diagnosis of human fascioliasis in different epidemiological situations. Tropical Medicine and International Health 17, 630–636.Google Scholar
Valero, M.A., Periago, M.V., Perez-Crespo, I., Angles, R., Villegas, F., Aguirre, C., Strauss, W., Espinoza, J.R., Herrera, P., Terashima, A., Tamayo, H., Engels, D., Gabrielli, A.F. & Mas-Coma, S. (2012b) Field evaluation of a coproantigen detection test for fascioliasis diagnosis and surveillance in human hyperendemic areas of Andean countries. PLoS Neglected Tropical Diseases 6, e1812.Google Scholar
Valero, M.A., Perez-Crespo, I., Khoubbane, M., Artigas, P., Panova, M., Ortiz, P., Maço, V., Espinoza, J.R. & Mas-Coma, S. (2012c) Fasciola hepatica phenotypic characterization in Andean human endemic areas: valley versus altiplanic patterns analysed in liver flukes from sheep from Cajamarca and Mantaro, Peru. Infection, Genetics and Evolution 12, 403–410.Google Scholar
Varma, A.K. (1953) On Fasciola indica n. sp. with some observations on F. hepatica and F. gigantica. Journal of Helminthology 27, 185–198.Google Scholar
Watanabe, S. (1962) Fasciolosis of ruminants in Japan. Bulletin de l'Office International des Epizooties 58, 313–322.Google Scholar
Watanabe, S. & Iwata, S. (1954) Fasciola species in Japan. Journal of Japanese Veterinary Medical Association 7, 124–126.Google Scholar