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Molecular epidemiological survey on the vectors of Thelazia gulosa, Thelazia rhodesi and Thelazia skrjabini (Spirurida: Thelaziidae)

Published online by Cambridge University Press:  17 October 2003

D. OTRANTO ,
E. TARSITANO ,
D. TRAVERSA ,
F. DE LUCA  and
A. GIANGASPERO
D. OTRANTO
Affiliation:
Department of Animal Health and Welfare, Faculty of Veterinary Medicine, P.O. Box 7, 70010, Valenzano, Bari, Italy
E. TARSITANO
Affiliation:
Department of Animal Health and Welfare, Faculty of Veterinary Medicine, P.O. Box 7, 70010, Valenzano, Bari, Italy
D. TRAVERSA
Affiliation:
Department of Comparative Biomedical Sciences, Faculty of Veterinary Medicine, Piazza Aldo Moro 45, 64100, Teramo, Italy
F. DE LUCA
Affiliation:
Istituto per la Protezione delle Piante-Sezione di Bari, CNR, Via Amendola 165, 70126, Bari, Italy
A. GIANGASPERO
Affiliation:
Department of Comparative Biomedical Sciences, Faculty of Veterinary Medicine, Piazza Aldo Moro 45, 64100, Teramo, Italy
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Abstract

A Polymerase Chain Reaction (PCR)- based assay developed for the specific identification of Thelazia gulosa, Thelazia rhodesi and Thelazia skrjabini (Nematoda, Spirurida), which cause bovine ocular thelaziosis, was evaluated for its usefulness in detecting the intermediate hosts and in estimating the infection prevalence of vectors in field conditions throughout 5 years (from 1997 to 2001). A total of 5190 flies were captured and identified as Musca larvipara, Musca osiris, Musca autumnalis, Musca tempestiva or Musca domestica. Genomic DNA was extracted from pools constituted by heads, thoraces, abdomens and wings of 10 flies of each species, and 2076 samples were subjected to a PCR assay to specifically detect the ribosomal ITS-1 sequence of bovine Thelazia. Amplicons were sequenced and subjected to digestion with CpoI restriction enzyme. M. autumnalis, M. larvipara, M. osiris and M. domestica species were shown to be PCR positive. T. gulosa was specifically detected by PCR in M. autumnalis, M. larvipara, M. osiris and M. domestica, whereas T. rhodesi is in M. autumnalis and M. larvipara. Of 27 positive samples, 23 were positive for T. gulosa and 4 for T. rhodesi, with a mean prevalence of 2·86% in the whole fly population collected. The highest mean prevalence values of infection were detected in M. autumnalis (4·46%) and M. larvipara (3·21%), and the former species was confirmed to be the vector of T. gulosa and T. rhodesi. This study is the first report of M. osiris as a vector of T. gulosa and M. larvipara as a vector of T. gulosa and T. rhodesi under natural conditions. The occurrence of Thelazia in fly populations in the Apulia region of Italy (in the 5 grazing seasons considered) indicates that cattle thelaziosis is enzootic in southern Italy. This molecular assay should be a useful epidemiological tool for assessing the role of different species of flies as intermediate hosts of thelaziae.

Keywords

Thelazia spp.eyewormsfliesintermediate hostPCRribosomal DNAITS-1
Type
Research Article
Information
Parasitology , Volume 127 , Issue 4 , October 2003 , pp. 365 - 373
Copyright
2003 Cambridge University Press

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References

REFERENCES

BACHELLERIE, J. P. & QU, L. H. (1993). Ribosomal RNA probes for detection and identification of species. In Methods in Molecular Biology. Vol. 21: Protocols in Molecular Parasitology (ed. Hyde, J. E.), pp. 250–254. Humana Press. Inc., Totowa, NJ, USA.CrossRef
BLOUIN, M. S. (2002). Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. International Journal for Parasitology 32, 527–531.CrossRefGoogle Scholar
BRANCH, G. J. & STOFFOLANO, J. G. (1974). Face fly: invertebrate vector and host of a mammalian eyeworm in Massachussetts. Journal of Economic Entomology 67, 304–305.CrossRefGoogle Scholar
CHILTON, N. B. & GASSER, R. B. (1999). Sequence differences in the internal transcribed spacers of DNA among four species of hookworm (Ancylostomatoidea: Ancylostoma). International Journal for Parasitology 29, 1971–1977.CrossRefGoogle Scholar
CHILTON, N. B., GASSER, R. B. & BEVERIDGE, I. (1995). Differences in a ribosomal DNA sequence of morphologically indistinguishable species within the Hypodontus macropi complex (Nematoda: Strongyloidea). International Journal for Parasitology 25, 647–651.CrossRefGoogle Scholar
CHIRICO, J. (1994 a). A comparison of sampling methods with respect to cattle-visiting Muscidae and their nematode infections. Medical and Veterinary Entomology 8, 214–218.Google Scholar
CHIRICO, J. (1994 b). Prehibernating Musca autumnalis (Diptera: Muscidae) an overwintering host for parasitic nematodes. Veterinary Parasitology 52, 279–284.Google Scholar
CONOLE, J. C., CHILTON, N. B., JARVIS, T. & GASSER, R. B. (1999). Intraspecific and interspecific variation in the second internal transcribed spacer (ITS-2) sequence for Metastrongylus (Nematoda: Metastrongyloidea) detected by high resolution PCR-RFLP. International Journal for Parasitology 29, 1935–1940.CrossRefGoogle Scholar
CORBA, J. (1985). Die geographische Verbreitung der Thelaziose der Rinder in der Welt. Folia Veterinaria 12, 55.Google Scholar
D'ESPOSITO, L. (1949). Di alcuni casi di infezione del sacco congiuntivale dei bovini da Thelazia. Clinica Veterinaria 72, 108–118.Google Scholar
GASSER, R. B. (1999). PCR-based technology in veterinary parasitology. Veterinary Parasitology 84, 229–258.CrossRefGoogle Scholar
GASSER, R. B. & NEWTON, S. E. (2000). Genomic and genetic research on bursatenematodes: significance, implications and prospects. International Journal for Parasitology 30, 509–534.CrossRefGoogle Scholar
GASSER, R. B., WOODS, W. G. & BJØRN, H. (1998). Distinguishing Oesophagostomum dentatum from Oesophagostomum quadrispinulatum developmental stages by a single-strand conformation polymorphism method. International Journal for Parasitology 28, 1903–1909.CrossRefGoogle Scholar
GEDEN, C. J. & STOFFOLANO, J. G. (1980). Bovine thelaziasis in Massachussets. Cornell Veterinary 70, 344–359.Google Scholar
GEDEN, C. J. & STOFFOLANO, J. G. (1981). Geographic range and temporal patterns of parasitization of Musca autumnalis De Geer by Thelazia spp. in Massachussets with observation on Musca domestica as an unsuitable host. Journal of Medical Entomology 18, 449–456.Google Scholar
GEDEN, C. J. & STOFFOLANO, J. G. (1982). Development of the bovine eyeworm, Thelazia gulosa Railliet and Henry 1910 in experimentally infected female Musca autumnalis De Geer. Journal of Parasitology 68, 287–292.CrossRefGoogle Scholar
GIANGASPERO, A. (1997). Le Mosche di Interesse Veterinario. I Muscidae. Guida alla Conoscenza e al Riconoscimento. Edagricole, Bologna, Italy.
GIANGASPERO, A. & BROCE, A. B. (1993). Micromorphology of the prestomal teeth and feeding behaviour of Musca autumnalis, M. larvipara and M. osiris (Diptera: Muscidae). Medical and Veterinary Entomology 7, 398–400.Google Scholar
GIANGASPERO, A., OTRANTO, D., VOVLAS, N. & PUCCINI, V. (2000). Thelazia gulosa Railliet & Henry, 1910 and T. skrjabini Erschow, 1928 infection in southern Europe (Italy). Parasite 7, 327–329.Google Scholar
GUPTA, V. P. (1970). Musca domestica an intermediate host of two spiruroid nematode parasites of livestock. Orissa Veterinary Journal 5, 147–150.Google Scholar
HØGLUND, J., WILHELMSSON, E., CHRISTENSSON, D., MORNER, T., WALLER, P. & MATTSSON, J. G. (1999). ITS2 sequences of Dictyocaulus species from cattle, roe deer and moose in Sweden: molecular evidence for a new species. International Journal for Parasitology 29, 607–611.CrossRefGoogle Scholar
HOSTE, H., CHILTON, N. B., BEVERIDGE, I. & GASSER, R. B. (1998). A comparison of the first internal transcribed spacer of ribosomal DNA in seven species of Trichostrongylus (Nematoda: Trichostrongylidae). International Journal for Parasitology 28, 1251–1260.CrossRefGoogle Scholar
HOSTE, H., CHILTON, N. B., GASSER, R. B. & BEVERIDGE, I. (1995). Differences in the second internal transcribed spacer (ribosomal DNA) between five species of Trichostrongylus (Nematoda: Strongylidae). International Journal for Parasitology 25, 75–80.CrossRefGoogle Scholar
HUNG, G. C., GASSER, R. B., BEVERIDGE, I. & CHILTON, N. B. (1999). Species-specific amplification by PCR of ribosomal DNA from some equine strongyles. Parasitology 119, 69–80.CrossRefGoogle Scholar
KEISEROVSKAYA, M. A. (1975). The biology of Thelazia rhodesi in Azerbaijzhan. In Issledovaniya po gelmintologii v Azerbaidzhane (ed. Mikailov, T. K.), pp. 66–69. Baku, USSR.
KIJEWSKA, A., ROKICKI, J., SITKO, J. & WEGRZYN, G. (2002). Ascaridoidea: a simple DNA assay for identification of 11 species infecting marine and freshwater fish, mammals, and fish-eating birds. Experimental Parasitology 101, 35–39.CrossRefGoogle Scholar
KLESOV, M. D. (1949). The biology of the nematode Thelazia rhodesi (Desmarest, 1827) Doklady Akademy Nauk SSSR 66, 309–311.Google Scholar
KLESOV, M. D. (1950). Contribution to the question of the biology of two nematodes of the same genus Thelazia Bosc 1819, parasites of the eyes of cattle. Doklady Akademy Nauk SSSR 75, 591–594.Google Scholar
KRAFSUR, E. S. & CHURCH, C. J. (1985). Bovine thelaziasis in Iowa. Journal of Parasitology 71, 279–286.CrossRefGoogle Scholar
KRASTIN, N. I. (1950 a). A study of the developmental cycle of the nematode Thelazia gulosa (Railliet & Henry, 1910) a parasite of the eyes of cattle. Doklady Akademy Nauk SSSR 70, 549–551.Google Scholar
KRASTIN, N. I. (1950 b). Elucidation of the biological life cycle of a second vector of thelaziasis. Veterinaryia 27, 20–21.Google Scholar
KRASTIN, N. I. (1958). Development of Thelazia rhodesi in the definitive host. In Contributions to Helminthology. Published to commemorate the 60th birthday of R. S. Shults by the Israel Program for Scientific Translations, pp. 206–213. Moscow Izdatelstvo, Akademy Nauk SSSR.
LYONS, E. T. & DRUDGE, J. H. (1975). Two eyeworms, Thelazia gulosa and Thelazia skrjabini in cattle in Kentucky. Journal of Parasitology 61, 1119–1122.CrossRefGoogle Scholar
MAR, P. H., YANG, I. C., CHANG, G. N. & FEI, A. C. (2002). Specific polymerase chain reaction for differential diagnosis of Dirofilaria immitis and Dipetalonema reconditum using primers derived from internal transcribed spacer region 2 (ITS2). Veterinary Parasitology 106, 243–252.CrossRefGoogle Scholar
MIYAMOTO, K., KANO, R., KANEKO, K., SHIMIZU, N., AKAMATSU, T., NAGASHIMA, A., NAGAOKA, S., EBINA, R., HAGINO, K. & MORITA, K. (1965). Studies on intermediate hosts of bovine thelazia. Investigations in Niikappu Pasture, Hokkaido. Japanese Journal of Sanity and Zoology 16, 194–200.Google Scholar
MOOLENBEEK, W. S. & SURGEONER, G. A. (1980). Southern Ontario survey of eyeworms Thelazia gulosa and Thelazia lacrymalis in cattle and larvae of Thelazia spp. in the face fly Musca autumnalis. Canadian Veterinary Journal 21, 50–52.Google Scholar
MORALES-HOJAS, R., POST, R. J., SHELLEY, A. J., MAIA-HERZOG, M., COSCARON, S. & CHEKE, R. A. (2001). Characterisation of nuclear ribosomal DNA sequences from Onchocerca volvulus and Mansonella ozzardi (Nematoda: Filarioidea) and development of a PCR-based method for their detection in skin biopsies. International Journal for Parasitology 31, 169–177.CrossRefGoogle Scholar
NEWTON, L. A., CHILTON, N. B., BEVERIDGE, I. & GASSER, R. B. (1998 a). Genetic evidence indicating that Cooperia surnabada and Cooperia oncophora are one species. International Journal for Parasitology 28, 331–336.Google Scholar
NEWTON, L. A., CHILTON, N. B., BEVERIDGE, I. & GASSER, R. B. (1998 b). Differences in the second internal transcribed spacer of four species of Nematodirus (Nematoda: Molineidae). International Journal for Parasitology 28, 337–341.Google Scholar
O'HARA, J. E. & KENNEDY, M. J. (1989). Prevalence and intensity of Thelazia spp. (Nematoda: Thelazioidea) in a Musca autumnalis (Diptera: Muscidae) population from central Alberta. Journal of Parasitology 75, 803–806.Google Scholar
O'HARA, J. E. & KENNEDY, M. J. (1991). Development of the nematode Thelazia skrjabini (Nematoda: Thelazioidea) in experimentally infected face flies Musca autumnalis (Diptera: Muscidae). Journal of Parasitology 77, 417–425.CrossRefGoogle Scholar
OTRANTO, D., TARSITANO, E., TRAVERSA, D., GIANGASPERO, A., DE LUCA, F. & PUCCINI, V. (2001). Differentiation among three species of bovine Thelazia (Nematoda: Thelaziidae) by PCR-RFLP of the ITS-1 (rDNA). International Journal for Parasitology 31, 1693–1698.CrossRefGoogle Scholar
PANEBIANCO, F. (1955). La telaziosi oculare del bovino. Segnalazioni di alcuni focolai in Calabria e Sicilia. Zooprofilassi 10, 653–658.Google Scholar
PONT, A. C. (1986). A revision of the Fannidae and Muscidae described by J. W. Meigen. Insecta: Diptera. Annals of Naturist Museum of Wien 87, 197–253.Google Scholar
POWERS, T. O., TODD, T. C., BURNELL, A. M., MURRAY, P. C. B., FLEMING, C. C., SZALANSKI, A. L., ADAMS, B. A. & HARRIS, T. S. (1997). The rDNA internal transcribed spacer region as a taxonomic marker for nematodes. Journal of Nematology 29, 441–450.Google Scholar
PUCCINI, V., GIANGASPERO, A. & BISCEGLIA, D. (1988). La telaziosi dei bovini. Obiettivi e Documenti Veterinari 9, 17–19.Google Scholar
SKRJABIN, K. I., SOBOLEV, A. A. & IVASHKIN, V. M. (1967). Principles of Nematology Vol. IX. Spirurata of Animals and Man and the Disease Caused by Them. Part. 4: Thelazioidea. Published by the Israel Program for Scientific Translations. Washington, USA.
STOFFOLANO, J. G. (1970). Nematodes associated with the genus Musca (Diptera: Muscidae). Bulletin of the Entomological Society of America 16, 194–203.CrossRefGoogle Scholar
THOMPSON, J. D., GIBSON, T. J., PLEWNIAK, F., JEANMOUGIN, F. & HIGGINS, D. G. (1997). The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 24, 4876–4882.CrossRefGoogle Scholar
VILAGIOVA, I. (1962). Supplement to the hitherto knowledge on developmental cycle of Thelazia gulosa Railliet and Henry 1910. Zoologicke Listy Brno 11, 332–334.Google Scholar
VILAGIOVA, I. (1967). Results of experimental studies on the development of pre-invasive stage of worms of the genus Thelazia Bosc 1819 (Nematoda: Spirurata) parasitic in the eye in the cattle. Folia Parasitologica 74, 275–280.Google Scholar
VILAGIOVA, I. (1968). Ecological specificity of intermediate hosts of Thelazia in cattle and the relation of their infective larvae to some unusual hosts. Helminthologia 9, 563–566.Google Scholar
YAMAGUTI, S. (1961). Sistema Helminthum. Vol. III. The Nematodes of Vertebrates Part I. Interscience Publishers, Inc., New York, USA.
ZHU, X., GASSER, R. B. & CHILTON, N. B. (1998). Differences in the 5·8S rDNA sequences among ascarid nematodes. International Journal for Parasitology 28, 617–622.CrossRefGoogle Scholar