Skip to main content Accessibility help
×
Home

The use of nuclear ribosomal DNA markers for the identification of bursate nematodes (order Strongylida) and for the diagnosis of infections

  • Neil B. Chilton (a1)

Abstract

Many bursate nematodes are of major importance to animal health. Animals are often parasitized by multiple species that differ in their prevalence, relative abundance and/or pathogenicity. Implementation of effective management strategies for these parasites requires reliable methods for their detection in hosts, identification to the species level and measurement of intensity of infection. One major problem is the difficulty of accurately identifying and distinguishing many species of bursate nematode because of the remarkable morphological similarity of their eggs and larvae. The inability to identify, with confidence, individual nematodes (irrespective of their life-cycle stage) to the species level by morphological methods has often led to a search for species-specific genetic markers. Studies over the past 15 years have shown that sequences of the internal transcribed spacers of ribosomal DNA provide useful genetic markers, providing the basis for the development of PCR-based diagnostic tools. Such molecular methods represent powerful tools for studying the systematics, epidemiology and ecology of bursate nematodes and, importantly, for the specific diagnosis of infections in animals and humans, thus contributing to improved control and prevention strategies for these parasites.

Copyright

Corresponding author

References

Hide All
Albonico, M, Crompton, DWT, Saviolli, L (1999) Control strategies for human intestinal nematode infections. Advances in Parasitology 42: 277341.
Anderson, RC (2000). Order Strongylida (the bursate nematodes) In: Nematode Parasites of Vertebrates. Their Development and Transmission. 2nd edn. Wallingford, UK: CAB International, University Press, pp. 41229.
Anderson, JC, Blouin, MS and Beech, RN (1998). Population biology of parasitic nematodes: applications of genetic markers. Advances in Parasitology 41: 219283.
Andrews, RH and Chilton, NB (1999). Multilocus enzyme electrophoresis: a valuable technique for providing answers to problems in parasite systematics. International Journal for Parasitology 29: 213253.
Arnheim, N (1983). Concerted evolution of multigene families. In: Nei, M and Koehn, RK, editors. Evolution of Genes and Proteins. Sunderland (MA): Sinauer, pp. 3861.
Arundel, JH (1985). Parasitic Diseases of the Horse Sydney: Post-Graduate Foundation in Veterinary Science, University of Sydney, pp. 426.
Arundel, JH, Barker, IK and Beveridge, I (1977). Diseases of marsupials. In: Stonehouse, B and Gilmore, D, editors. The Biology of Marsupials. Baltimore: University Park Press, pp. 141154.
Arundel, JH, Beveridge, I and Presidente, PJ (1979). Parasites and pathological findings in enclosed and free-ranging populations of Macropus rufus (Desmarest) (Marsupialia) at Menindee, New South Wales. Australian Wildlife Research 6: 361379.
Arundel, JH, Dempster, KJ, Harrigan, KE and Black, R (1990). Epidemiological observations on the helminth parasites of Macropus giganteus Shaw in Victoria. Australian Wildlife Research 17: 3951.
Audebert, F, Durette-Desset, MC and Chilton, NB (2000). Internal transcribed spacer rDNA can be used to infer the phylogenetic relationships of species within the genus Nematodirus (Nematoda: Molineoidea). International Journal for Parasitology 30: 187191.
Barton, NJ and Seward, DA (1993). Detection of Libyostrongylus douglassi in ostriches in Australia. Australian Veterinary Journal 70: 3132.
Beck, T, Moir, B and Meppen, T (1985). The cost of parasites to the Australian sheep industry. Quarterly Review of the Rural Economy 7: 336343.
Berrag, B and Cabaret, J (1996). Impaired pulmonary gas exchange in ewes naturally infected by small lungworms. International Journal for Parasitology 26: 13971400.
Berrag, B and Cabaret, J (1997). Assessment of the severity of natural infections of kids and adult male goats by small lungworms (Protostrongylidae, Nematoda) using macroscopic lesion scores. Veterinary Research (Paris) 28: 143148.
Beveridge, I (1979). Hypodontus macropi Mönnig, 1929, a hookworm-like parasite of macropodid marsupials. Journal of Helminthology 53: 229244.
Beveridge, I and Chilton, NB (2001). Co-evolutionary relationships between the nematode subfamily Cloacininae and its marsupial hosts. International Journal for Parasitology 31: 976996.
Beveridge, I, Chilton, NB and Spratt, DM (2002). The occurrence of species flocks in the nematode genus Cloacina (Strongyloidea: Cloacininae), parasitic in the stomachs of kangaroos and wallabies. Australian Journal of Zoology 50: 597620.
Blaxter, ML, De Ley, P, Garey, JR, Lui, LX, Scheldeman, P, Vierstraete, A, Vanfleteren, JR, Mackey, LY, Dorris, M, Frisse, LM, Vida, JT and Thomas, WK (1998). A molecular evolutionary framework for the phylum Nematoda. Nature 392: 7175.
Blouin, MS (2002). Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. International Journal for Parasitology 32: 527531.
Blouin, MS, Dame, JB, Tarrant, CA and Courtney, CH (1992). Unusual population genetics of a parasitic nematode; mtDNA variation within and among populations. Evolution 46: 470476.
Blouin, MS, Yowell, CA, Courtney, CH and Dame, JB (1995). Host movement and the genetic structure of populations of parasitic nematodes. Genetics 141: 10071014.
Blouin, MS, Yowell, CA, Courtney, CH and Dame, JB (1997). Haemonchus placei and Haemonchus contortus are distinct species based on mtDNA evidence. International Journal for Parasitology 27: 13831387.
Bowen, T and Dover, GA (1995). PCR amplification of intergenic spacers in the ribosomal DNA of Drosophila melanogaster reveals high levels of turnover in length and copy-number of spacers in geographically separated populations. Molecular Ecology 4: 419427.
Bowman, DD, Hendrix, CM, Lindsay, DS and Barr, SC (2002). Feline Clinical Parasitology. Ames (IA): Iowa State University Press, pp. 241273.
Bowman, DD, Lynn, RC and Eberhard, ML (2003). Georgis' Parasitology for Veterinarians. 8th edn. Missouri: Elsevier Science, pp. 155196.
Buckler, ES IV, Ippolito, A and Holtsford, TP (1997). The evolution of ribosomal DNA: divergent paralogues and phylogenetic implications. Genetics 145: 821832.
Bucknell, D, Hoste, H, Gasser, RB and Beveridge, I (1996). The structure of the community of strongyloid nematodes of domestic equids. Journal of Helminthology 70: 185192.
Campbell, AJD, Gasser, RB and Chilton, NB (1995). Differences in a ribosomal DNA sequence of Strongylus species allows identification of single eggs. International Journal for Parasitology 25: 359365.
Carreno, RA and Nadler, SA (2003). Phylogenetic analysis of the Metastrongyloidea (Nematoda: Strongylida) inferred from ribosomal RNA gene sequences. Journal of Parasitology 89: 965973.
Chilton, NB and Gasser, RB (1999). Sequence differences in the internal transcribed spacers of rDNA among four species of hookworm (Ancylostomatoidea: Ancylostoma). International Journal for Parasitology 29: 19711977.
Chilton, NB, Gasser, RB and 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: 647651.
Chilton, NB, Gasser, RB and Beveridge, I (1997a). Phylogenetic relationships of Australian strongyloid nematodes inferred from ribosomal DNA sequence data. International Journal for Parasitology 27: 14811494.
Chilton, NB, Hoste, H, Hung, G-C, Beveridge, I and Gasser, RB (1997b). The 5.8S rDNA sequences of 18 species of bursate nematodes (Order Strongylida): comparison with rhabditid and tylenchid nematodes. International Journal for Parasitology 27: 119124.
Chilton, NB, Hoste, H, Newton, LA, Beveridge, I and Gasser, RB (1998). Common secondary structures for the second internal transcribed spacer pre-RNA of two subfamilies of trichostrongylid nematodes. International Journal for Parasitology 28: 17651773.
Chilton, NB, Newton, LA, Beveridge, I and Gasser, RB (2001). Evolutionary relationships of trichostrongyloid nematodes (Strongylida) inferred from ribosomal DNA sequence data. Molecular Phylogenetics and Evolution 19: 367386.
Chilton, NB, Huby-Chilton, F, Gasser, RB and Beveridge, I (2002). Review of Papillostrongylus Johnson & Mawson, 1939 (Nematoda: Strongyloidea) from wallabies and kangaroos (Marsupialia: Macropodidae) using morphological and molecular techniques, with the description of P. barbatus n. sp. Systematic Parasitology 51: 8193.
Chilton, NB, Huby-Chilton, F and Gasser, RB (2003). First complete large subunit rRNA sequence and secondary structure for a parasitic nematode: phylogenetic and diagnostic implications. Molecular and General Genetics 17: 3339.
Christensen, CM, Zarlenga, DS and Gasbarre, LC (1994a). Identification of a Haemonchus placei-specific DNA probes. Journal of the Helminthological Society of Washington 61: 249252.
Christensen, CM, Zarlenga, DS and Gasbarre, LC (1994b). Ostertagia, Haemonchus, Cooperia, and Oesophagostomum: construction and characterization of genus-specific DNA probes to differentiate important parasites of cattle. Experimental Parasitology 78: 93100.
Clayton, HM and Trawford, AF (1981). Anthelmintic control of lungworm in donkeys. Equine Veterinary Journal 13: 192194.
Cole, VG (1986). Animal Health in Australia. Volume 8. Helminth Parasites of Sheep and Cattle. Australian Agricultural Health and Quarantine Service Department of Primary Industry, Brisbane: Watson Ferguson and Co.
Coles, BH (1997). Avian Medicine and Surgery. Oxford: Blackwell Science, pp. 338341.
Conole, J, Chilton, NB, Järvis, T and Gasser, RB (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: 19351940.
Conole, J, Chilton, NB, Järvis, T and Gasser, RB (2001). Mutation scanning analysis of microsatellite variability in the second internal transcribed spacer (precursor ribosomal RNA) for three species of Metastrongylus (Strongylida: Metastrongyloidea). Parasitology 122: 195206.
Copland, JW (1974). Metastrongylus spp. infections of village pigs in Papua New Guinea. Journal of Helminthology 48: 2532.
Corwin, RM (1997). Economics of gastrointestinal parasitism of cattle. Veterinary Parasitology 72: 451460.
Corwin, RM and Stewart, TB (1992). Internal parasites. In: Leman, AD, Straw, BE, Mengeling, WL, D'Allaire, S and Taylor, DJ, editors. Diseases of Swine. 7th edn. Ames (IA): Iowa State University Press, pp. 718734.
Dallas, JF, Irvine, RJ and Halvorsen, O (2000a). DNA evidence that Ostertagia gruehneri and Ostertagia arctica (Nematoda: Ostertagiinae) in reindeer from Norway and Svalbard are conspecific. International Journal for Parasitology 30: 655658.
Dallas, JF, Irvine, RJ, Halvorsen, O and Albon, SD (2000b). Identification by polymerase chain reaction (PCR) of Marshallagia marshalli and Ostertagia gruehneri from Svalbard reindeer. International Journal for Parasitology 30: 863866.
Dame, JB, Yowell, CA, Courtney, CH and Lindgren, WG (1991). Cloning and characterization of the ribosomal RNA gene repeat from Ostertagia ostertagi. Molecular and Biochemical Parasitology 45: 275280.
Demartini, JC and Davies, RB (1997). An epizootic of pneumonia in captive bighorn sheep with Muellerius sp. Journal of Wildlife Diseases 13: 117124.
Divina, BP, Wilhelmsson, E, Mattsson, JG, Waller, P and Höglund, J (2000). Identification of Dictyocaulus spp. in ruminants by morphological and molecular analyses. Parasitology 121: 193201.
Divina, BP, Wilhelmsson, E, Mörner, T, Mattsson, JG and Höglund, J (2002). Molecular identification and prevalence of Dictyocaulus spp. (Trichostrongyloidea: Dictyocaulidae) in Swedish semi-domestic and free-living cervids. Journal of Wildlife Diseases 38: 769775.
Dobson, RJ, Barnes, EH, Birclijin, SD and Gill, JH (1992). Survival of Ostertagia circumcincta and Trichostrongylus colubriformis in faecal culture as a source of bias in apportioning egg counts to worm species. International Journal for Parasitology 22: 10051008.
Dorris, M and Blaxter, M (2000). The small subunit ribosomal RNA sequence of Strongyloides stercoralis. International Journal for Parasitology 30: 939941.
Dorris, M, Viney, ME, and Blaxter, M (2002). Molecular phylogenetic analysis of the genus Strongyloides and related nematodes. International Journal for Parasitology 32: 15071517.
Duffy, MS, Waldrup, KA, Mackintosh, CG, Pearse, AJ, Taylor, MJ, Labes, RE and Burt, MDB (2001). Natural and experimental nematode infections in red deer (Cervus elaphus elaphus) and the potential for antemortem serodiagnosis of the tissue worm Elaphostrongylus cervi. Canadian Journal of Zoology 79: 22462256.
Durette-Desset, M-C (1980). Keys to genera of the superfamily Trichostrongyloidea. In: Anderson, RC, Chabaud, AG and Willmott, S, editors. C.I.H. Keys to the Nematode Parasites of Vertebrates. Wallingford (UK): CAB International, pp. 168.
Durette-Desset, M-C and Chabaud, AG (1981). Nouvel essai de classification des nématodes Trichostrongyloidea. Annales de Parasitologie Humaine et Comparée 3: 297312.
Durette-Desset, M-C and Chabaud, AG (1993). Nomenclature des Strongylida au-dessus du groupe famille. Annales de Parasitologie Humaine et Comparée 68: 111112.
Durette-Desset, M-C, Beveridge, I and Spratt, DM (1994). The origins and evolutionary expansion of the Strongylida (Nematoda). International Journal for Parasitology 24: 11391165.
Elder, JF and Turner, BJ (1995). Concerted evolution of repetitive DNA sequences in eukaryotes. Quarterly Review of Biology 70: 297320.
Ellis, RE, Sulston, JE and Coulson, AR (1986). The rDNA of C. elegans sequence and structure. Nucleic Acids Research 14: 23452364.
Elson-Riggins, JG, Al-Banna, L, Platzer, EG and Kaloshian, I (2001). Characterization of Otostrongylus circumlitus from Pacific harbor and northern elephant seals. Journal of Parasitology 87: 7378.
Epe, C, Samson-Himmelstjerna, GV, Schnieder, T (1997). Differences in a ribosomal DNA sequence of lungworm species (Nematoda: Dictyocaulidae) from fallow deer, cattle, sheep and donkeys. Research in Veterinary Science 62: 1721.
Eysker, M, Boersema, JH and Kooyman, FN (1990). Seasonally inhibited development of yathostome nematodes in Shetland ponies in The Netherlands. Veterinary Parasitology 36: 259264.
Gajadhar, A, Steeves-Gurnsey, T, Kendall, J, Lankester, M and Stéen, M (2000). Differentiation of dorsal-spined elaphostrongyline larvae by polymerase chain reaction amplification of ITS-2 of rDNA. Journal of Wildlife Diseases 36: 713722.
Gasser, RB (1997). Mutation scanning methods for the analysis of parasite genes. International Journal for Parasitology 27: 14491463.
Gasser, RB (1999). PCR-based technology in veterinary parasitology. Veterinary Parasitology 84: 29258.
Gasser, RB and Chilton, NB (2000). Applications of single-strand conformation polymorphism (SSCP) to taxonomy, diagnosis, population genetics and molecular evolution of parasitic nematodes. Veterinary Parasitology 101: 201213.
Gasser, RB and Hoste, H (1995). Genetic markers for closely-related parasitic nematodes. Molecular and Cellular Probes 9: 315320.
Gasser, RB and Newton, SE (2000). Genomic and genetic research on bursate nematodes: significance, implications and prospects. International Journal for Parasitology 30: 509534.
Gasser, RB and Zhu, XQ (1999). Sequence-based analysis of DNA fragments by mutation detection techniques. Parasitology Today 15: 462465.
Gasser, RB, Chilton, NB, Hoste, H and Beveridge, I (1993). Rapid sequencing of rDNA from single worms and eggs of parasitic helminths. Nucleic Acids Research 21: 25252526.
Gasser, RB, Chilton, NB, Hoste, H and Stevenson, LA (1994). Species identification of trichostrongyle nematodes by PCR-linked RFLP. International Journal for Parasitology 24: 291293.
Gasser, RB, Nansen, P and Gulberg, P (1996a). Fingerprinting sequence variation in ribosomal DNA of parasites by DGGE. Molecular and Cellular Probes 10: 95103.
Gasser, RB, Stevenson, LA, Chilton, NB, Nansen, P, Bucknell, DG and Beveridge, I (1996b). Species markers for equine strongyles detected in intergenic rDNA by PCR-RFLP. Molecular and Cellular Probes 10: 371378.
Gasser, RB, Stewart, LE and Speare, R (1996c). Genetic markers in ribosomal DNA for hookworm identification. Acta Tropica 62: 1521.
Gasser, RB, Monti, JR, Zhu, X-Q, Chilton, NB, Hung, G-C and Guldberg, P (1997). Polymerase chain reaction-linked single-strand conformation polymorphism of ribosomal DNA to fingerprint parasites. Electrophoresis 18: 15641566.
Gasser, RB, Monti, JR, Qian, B-Z, Polderman, AM, Nansen, P and Chilton, NB (1998a). A mutation scanning approach for the identification of hookworm species and analysis of population variation. Molecular and Biochemical Parasitology 92: 303312.
Gasser, RB, Zhu, X, Chilton, NB, Newton, LA, Nedergaard, T and Gulberg, P (1998b). Analysis of sequence homogenisation in rDNA arrays of Haemonchus contortus by denaturing gel electrophoresis. Electrophoresis 19: 23912395.
Gasser, RB, Rossi, L and Zhu, Q (1999a). Identification of Nematodirus species (Nematoda: Molineidae) from wild ruminants in Italy using ribosomal DNA markers. International Journal for Parasitology 29: 18091817.
Gasser, RB, Woods, WG, Huffman, MA, Blotkamp, J and Polderman, AM (1999b). Molecular separation of Oesophagostomum stephanostomum and Oesophagostomum bifurcum (Nematoda: Strongyloidea) from non-human primates. International Journal for Parasitology 29: 10871091.
Gasser, RB, Zhu, X, Beveridge, I and Chilton, NB (2001). Mutation scanning analysis of sequence heterogeneity in the second internal transcribed spacer (rDNA) within some members of the Hypodontus macropi (Nematoda: Strongyloidea) complex. Electrophoresis 22: 10761085.
Gasser, RB, Zhu, X and Chilton, NB (2002). The value of mutation scanning approaches for detecting genetic variation–implications for studying intestinal nematodes of humans. In: Holland, CV and Kennedy, MW, editors. World Class Parasites, Volume 2. The Geohelminths: Ascaris, Trichuris and Hookworm. Boston (MA): Kluwer Academic Press, pp. 219234.
Georgi, JR and McCulloch, CE (1989). Diagnostic morphometry: identification of helminth eggs by discriminant analysis of morphometric data. Proceedings of the Helminthological Society of Washington 56: 4457.
Gibbons, LM and Höglund, J (2002). Dictyocaulus capreolus n. sp. (Nematoda, Trichostrongyloidea) from roe-deer, Capreolus capreolus and moose, Alces alces in Sweden. Journal of Helminthology 76: 119124.
Gouÿ de Bellocq, J, Ferté, H, Depaquit, J, Justine, J-L, Tillier, A. and Durette-Desset, M-C (2001). Phylogeny of the Trichostrongylina (Nematoda) inferred from 28S rDNA sequences. Molecular Phylogenetics and Evolution 19: 430442.
Gray, GD (1987). Genetic resistance to haemonchosis in sheep. Parasitology Today 3: 253255.
Gulland, FMD, Werner, L, Neill, SO, Lowenstine, LJ, Trupkietwitz, J, Smith, D, Royal, B and Strubel, I (1996). Baseline coagulation assay values for northern elephant seals (Mirounga angustirostris) and disseminated intravascular coagulation in this species. Journal of Wildlife Diseases 32: 536540.
Hancock, JM, Tautz, D and Dover, GA (1988). Evolution of the secondary structures and compensatory mutations of the ribosomal RNAs of Drosophila melanogaster. Molecular Biology and Evolution 5: 393414.
Haupt, W (1966). Ein Beitrag zur Morphologie der Knötchenwürmer des Hausschweines, ihrer Eier sowie der dritten invasionstüchtigen Larvenstadien. Archiv für Experimentelle Veterinarmedizin 20: 701711.
Herd, RP (1986). Epidemiology and control of parasites in northern temperate regions. Veterinary Clinics of North America: Equine Practice 2: 337356.
Hillis, DM and Dixon, MT (1991). Ribosomal DNA: molecular evolution and phylogenetic inference. Quarterly Review of Biology 66: 411453.
Hoberg, EP, Kocan, AA and Rickard, LG (2001). Gastrointestinal strongyles in wild ruminants. In: Samuel, WM, Pybus, MJ and Kocan, AA, editors. Parasitic Diseases of Wild Animals. London: Mason Publishing, pp. 193227.
Hodgkinson, JE, Lichtenfels, JR, Mair, TS, Cripps, P, Freeman, KL, Ramsey, YH, Love, S and Matthews, JB (2003). A PCR-ELISA for the identification of cyathostomin fourth-stage larvae from clinical cases of larval cyathostominosis. International Journal for Parasitology 33: 14271435.
Höglund, J, Wilhelmsson, E, Christensson, D, Mörner, T, Waller, P and Mattsson, JG (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: 607611.
Höglund, J, Morrison, DA, Divina, BP and Mattsson, JG (2003). Phylogeny of Dictyocaulus (lungworms) from eight species of ruminants based on analyses of ribosomal RNA data. Parasitology 127: 179187.
Hoste, H, Gasser, RB, Chilton, NB, Mallet, S and Beveridge, I (1993). Lack of intraspecific variation in the second internal transcribed spacer (ITS-2) of Trichostrongylus colubriformis ribosomal DNA. International Journal for Parasitology 23: 10691071.
Hoste, H, Chilton, NB, Gasser, RB and Beveridge, I (1995). Differences in the second internal transcribed spacer (ribosomal DNA) between five species of Trichostrongylus (Nematoda: Trichostrongylidae). International Journal for Parasitology 25: 7580.
Hoste, H, Chilton, NB, Beveridge, I and Gasser, RB (1998). A comparison of the first internal transcribed spacer of ribosomal DNA in seven species of Trichostrongylus (Nematoda: Trichostrongylidae). International Journal for Parasitology 28: 12511260.
Hu, M, Höglund, J, Chilton, NB, Zhu, X and Gasser, RB (2002). Mutation scanning analysis of mitochondrial cytochrome c oxidase subunit 1 reveals limited gene flow among bovine lungworm subpopulations in Sweden. Electrophoresis 23: 33573363.
Hu, M, Chilton, NB and Gasser, RB (2003). The mitochondrial genomics of parasitic nematodes of socio-economic importance: recent progress, and implications for population genetics and systematic studies. Advances in Parasitology 56: 134212.
Huchzermeyer, FW (1998). Diseases of Ostriches and Other Ratites. Pretoria: Promedia, pp. 182186.
Huby-Chilton, F, Beveridge, I, Gasser, RB and Chilton, NB (2001). Single-strand conformation polymorphism analysis of genetic variation in Labiostrongylus longispicularis from kangaroos. Electrophoresis 22: 19251929.
Huby-Chilton, F, Beveridge, I and Chilton, NB (2002). Redescription of Zoniolaimus mawsonae Beveridge, 1983 (Nematoda: Strongyloidea) and the description of Z. latebrosus n. sp. from the red kangaroo, Macropus rufus (Marsupialia: Macropodidae) based on morphological and molecular data. Systematic Parasitology 51: 135147.
Hung, G-C, Jacobs, DE, Krecek, RC, Gasser, RB and Chilton, NB (1996). Strongylus asini (Nematoda: Strongylidae): genetic relationships with other Strongylus species determined by ribosomal DNA. International Journal for Parasitology 26: 14071411.
Hung, G-C, Chilton, NB, Beveridge, I, McDonnell, A, Lichtenfels, JR and Gasser, RB (1997). Molecular delineation of Cylicocyclus nassatus and C. ashworthi (Nematoda: Strongylidae). International Journal for Parasitology 27: 601605.
Hung, G-C, Chilton, NB, Beveridge, I and Gasser, RB (1999a). Secondary structure model for the ITS-2 precursor rRNA of strongyloid nematodes of equids: implications for phylogenetic inference. International Journal for Parasitology 29: 19491964.
Hung, G-C, Chilton, NB, Beveridge, I, Zhu, X, Lichtenfels, JR and Gasser, RB (1999b). Molecular evidence for cryptic species within Cylicostephanus minutus (Nematoda: Strongylidae). International Journal for Parasitology 29: 285291.
Hung, G-C, Gasser, RB, Beveridge, I and Chilton, NB (1999c). Species-specific amplification by PCR of ribosomal DNA from some equine strongyles. Parasitology 119: 6980.
Hung, G-C, Chilton, NB, Beveridge, I and Gasser, RB (2000). A molecular systematic framework for equine strongyles based on ribosomal DNA sequence data. International Journal for Parasitology 30: 95103.
Kaye, JN, Love, S, Lichtenfels, JR and McKeand, JB (1998). Comparative sequence analysis of the intergenic spacer region of cyathostome species. International Journal for Parasitology 28: 831836.
Kaplan, RM (2002). Anthelmintic resistance in nematodes of horses. Veterinary Research 33: 491507.
Klei, TR (1991). Recent observation on the epidemiology, pathogenesis and immunology of equine helminth infections. Equine Infectious Diseases 6: 129136.
Klei, TR and French, DD (1998). Small strongyles: an emerging parasite problem for horses. Equine Practitioner 20: 2630.
Krecek, RC, Reinecke, RK and Horak, IG (1989). Internal parasites of horses on mixed grassveld and bushveld in Transvaal, Republic of South Africa. Veterinary Parasitology 34: 135143.
Lankester, MW (2001). Extrapulmonary lungworms of cervids. In: Samuel, WM, Pybus, MJ and Kocan, AA, editors. Parasitic Diseases of Wild Animals. London: Mason Publishing, pp. 228278.
Leignel, V, Humbert, JF and Elard, L (1997). Study by ribosomal DNA ITS-2 sequencing and RAPD analysis on the systematics of four Metastrongylus species (Nematoda: Metastrongyloidea). Journal of Parasitology 83: 606611.
Leignel, V, Cabaret, J and Humbert, JF (2002). New molecular evidence that Teladorsagia circumcincta (Nematoda: Trichostrongylidea) is a species complex. Journal of Parasitology 88: 135140.
Lichtenfels, JR (1980a) Keys to genera of the superfamily Strongyloidea. In: Anderson, RC, Chabaud, AG and Willmott, S, editors. C.I.H. Keys to the Nematode Parasites of Vertebrates. Wallingford, UK: CAB International, pp. 141.
Lichtenfels, JR (1980b) Keys to genera of the superfamilies Ancylostomatoidea and Diaphanocephaloidea. In: Anderson, RC, Chabaud, AG and Willmott, S, editors. C.I.H. Keys to the Nematode Parasites of Vertebrates. Wallingford, UK: CAB International, pp. 126.
Lichtenfels, JR, Hoberg, EP and Zarlenga, DS (1997). Systematics of gastrointestinal nematodes of domestic ruminants: advances between 1992 and 1995 and proposals for future research. Veterinary Parasitology 72: 225245.
Lichtenfels, JR, Kharchenko, VA, Krecek, RC and Gibbons, LM (1998). An annotated checklist by genus and species of 93 species level names for 51 recognised species of small strongyles (Nematoda: Strongyloidea: Cyathostominea) of horses, assess and zebras of the world. Veterinary Parasitology 79: 6579.
Lichtenfels, JR, Gibbons, LM and Krecek, RC (2002). Recommended terminology and advances in the systematics of the Cyathostominea (Nematoda: Strongyloidea) of horses. Veterinary Parasitology 107: 337342.
Lyons, ET, Tolliver, SC and Drudge, JH (1999). Historical perspective of cyathostomes: prevalence, treatment and control programs. Veterinary Parasitology 85: 97112.
Love, S, Murphy, D and Mellor, D (1999). Pathogenicity of cyathostome infections. Veterinary Parasitology 85: 113122.
Malan, FS, Gruss, B, Roper, NA, Aschburner, AJ, and du Plessis, CA (1988). Resistance of Libyostrongylus douglassi in ostriches to levamisole. Journal of the South African Veterinary Association 59: 202203.
Matthee, S, Krecek, RC, and Milne, SA (2000). Prevalence and biodiversity of helminth parasites in donkeys from South Africa. Journal of Parasitology 86: 756762.
Matthee, S, Krecek, RC, and Gibbons, LM (2002). Cylicocyclus asinus n.sp. (Nematoda: Cyathostominae) from donkeys, Equus asinus, in South Africa. Systematic Parasitology 51: 2935.
McDonnell, A, Love, S, Tait, A, Lichtenfels, JR and Matthews, JB (2000). Phylogenetic analysis of partial mitochondrial cytochrome oxidase c subunit I and large ribosomal RNA sequences and nuclear internal transcribed spacer I sequences from species of Cyathostominae and Strongylinae (Nematoda, Order Strongylida), parasites of the horse. Parasitology 121: 649659.
McKenzie, ME, and Davidson, WR (1989). Helminth parasites of intermingling axis deer, wild swine and domestic cattle from the Island of Molokai, Hawaii. Journal of Infectious Diseases 25: 252257.
McManus, DP and Bowles, J (1996). Molecular genetic approaches to parasite identification: their value in diagnostic parasitology and systematics. International Journal for Parasitology 26: 687704.
Measures, LN (2001). Lungworms of marine mammals. In: Samuel, WM, Pybus, MJ and Kocan, AA, editors. Parasitic Diseases of Wild Animals. London: Mason Publishing, pp. 279300.
Migaki, G, Vandyke, D and Hubbard, RG (1971). Some histopathologic lesions caused by helminths in marine mammals. Journal of Wildlife Diseases 7: 281289.
Monti, JR, Chilton, NB, Qian, B-Z and Gasser, RB (1998). Specific amplification of Necator americanus or Ancylostoma duodenale DNA by PCR using markers in ITS-1 rDNA, and its implications. Molecular and Cellular Probes 12: 7178.
Morales, GA and Helmboldt, CF (1971). Verminous pneumonia in the Californian sea lion (Zalophus californianus). Journal of Wildlife Diseases 7: 2227.
Musters, W, Boon, K, van der Sande, CAFM, van Heerikuizen, H and Planta, RJ (1990). Functional analysis of transcribed spacers of yeast ribosomal DNA. EMBO Journal 9: 29893996.
Nadler, SA (1990). Molecular approaches to studying helminth population genetics and phylogeny. International Journal for Parasitology 20: 1119.
Nadler, SA, Adams, BJ, Lyons, ET, DeLong, RL and Melin, SR (2000a). Molecular and morphometric evidence for separate species of Uncinaria (Nematoda: Ancylostomatidae) in California sea lions and northern fur seals: hypothesis testing supplants verification. Journal of Parasitology 86: 10991106.
Nadler, SA, Hoberg, EP, Hudspeth, DSS and Rickard, LG (2000b). Relationships of Nematodirus species and Nematodirus battus isolates (Nematoda: Trichostrongyloidea) based on nuclear ribosomal DNA sequences. Journal of Parasitology 86: 588601.
Newton, LA, Chilton, NB, Bjørn, H, Monti, JR, Várady, M, Christensen, CM and Gasser, RB (1997). Rapid PCR-based delineation of the porcine nodular worms, Oesophagostomum dentatum and O. quadrispinulatum. Molecular and Cellular Probes 11: 149153.
Newton, LA, Chilton, NB, Beveridge, I and Gasser, RB (1998a). Genetic evidence indicating that Cooperia surnabada and Cooperia oncophora are one species. International Journal for Parasitology 28: 331336.
Newton, LA, Chilton, NB, Beveridge, I and Gasser, RB (1998b). Differences in the second internal transcribed spacer of four species of Nematodirus (Nematoda: Molineidae). International Journal for Parasitology 28: 337341.
Newton, LA, Chilton, NB, Beveridge, I and Gasser, RB (1998c). Systematic relationships of some members of the genera Oesophagostomum and Chabertia (Nematoda: Chabertiidae) based on ribosomal DNA sequence data. International Journal for Parasitology 28: 17811789.
Newton, LA, Chilton, NB, Beveridge, I, Hoste, H, Nansen, P and Gasser, RB (1998d). Genetic markers for strongylid nematodes of livestock defined by PCR-based restriction analysis of spacer rDNA. Acta Tropica 69: 115.
Onderka, DK (1989). Prevalence and pathology of nematode infections in the lungs of ringed seals (Phoca hispida) of the western arctic of Canada. Journal of Wildlife Diseases 25: 218224.
Paterson, MW, Gibbs, C, Wotton, PR and Day, MJ (1993). Angiostrongylus vasorum infection in seven days. Veterinary Record 133: 565570.
Romstad, A, Gasser, RB, Monti, JR, Polderman, AM, Nansen, P, Pit, DSS and Chilton, NB (1997). Differentiation of Oesophagostomum bifurcum from Necator americanus by PCR using genetic markers in spacer ribosomal DNA. Molecular and Cellular Probes 11: 169176.
Romstad, A, Gasser, RB, Nansen, P, Polderman, AM and Chilton, NB (1998). Necator americanus (Nematoda: Ancylostomatidae) from Africa and Malaysia have different ITS-2 rDNA sequences. International Journal for Parasitology 28: 611615.
Roos, MH and Grant, WN (1993). Species-specific PCR for the parasitic nematodes Haemonchus contortus and Trichostrongylus colubriformis. International Journal for Parasitology 23: 419421.
Samson-Himmelstjerna, G, von Woidtke, S, Epe, C and Schnieder, T (1997). Species-specific polymerase chain reaction for the differentiation of larvae from Dictyocaulus viviparus and Dictyocaulus eckerti. Veterinary Parasitology 68: 119126.
Samson-Himmelstjerna, G, von Harder, A and Schneider, T (2002). Quantitative analysis of ITS2 sequences in trichostrongyle parasites. International Journal for Parasitology 32: 15291535.
Santin-Durán, M, de la Fuente, C, Alunda, JM, Rosenthal, BM and Hoberg, EP (2002). Identical ITS-1 and ITS-2 sequences suggest Spiculopteragia asymmetrica and Spiculopteragia quadrispiculata (Nematoda: Trichostrongylidae) constitute morphologically distinct variants of a single species. Journal of Parasitology 88: 417418.
Schnieder, T, Epe, C, von Samson-Himmelstjerna, G (1996). Species differentiation of lungworms (Dictyocaulidae) by polymerase chain reaction/restriction-fragment-length polymorphism of second internal transcribed spacers of ribosomal DNA. Parasitology Research 82: 392394.
Spratt, DM, Beveridge, I and Walter, E (1991). A catalogue of Australasian marsupials and monotremes and their recorded helminth parasites. Records of the South Australian Museum Monograph Series 1: 1105.
Stevenson, LA, Chilton, NB and Gasser, RB (1995). Differentiation of Haemonchus placei from H. contortus (Nematoda: Trichostrongylidae) by the ribosomal DNA second internal transcribed spacer. International Journal for Parasitology 25: 483488.
Stevenson, LA, Gasser, RB and Chilton, NB (1996). The ITS-2 rDNA of Teladorsagia circumcincta, T. trifurcata and T. davtiani indicates these taxa are one species. International Journal for Parasitology 26: 11231126.
Stewart, TB and Gasbarre, LC (1989). The veterinary importance of nodular worms (Oesophagostomum spp). Parasitology Today 5: 209213.
Stockdale, PHG (1970). The pathogenesis of the lesions elicited by Aelurostrongylus abstrusus during its prepatent period. Pathologia Veterinaria 7: 102115.
Sweeny, JC and Gilmartin, WG (1974). Survey of diseases in free-living Californian sea lions. Journal of Wildlife Diseases 10: 370376.
Taylor, DJ (1995). Pig Diseases. Bury St Edmunds, UK: St Edmundsbury Press, pp. 236239.
van der Sande, CAFM, Kwa, M, van Nues, RW, van Heerikhuizen, H, Raué, HA and Planta, RJ (1992). Functional analysis of internal transcribed spacer 2 of Saccharomyces cerevisiae ribosomal DNA. Journal of Molecular Biology 223: 899910.
van Nues, RW, Venema, J, Rientjes, MJ, Dirks-Mulder, A and Raué, HA (1995). Processing the eukaryotic pre-rRNA: the role of the transcribed spacers. Biochemical and Cellular Biology 73: 789801.
Verweij, JJ, Polderman, AM, Wimmenhove, MC and Gasser, RB (2000). PCR assay for the specific amplification of Oesophagostomum bifurcum DNA from human faeces. International Journal for Parasitology 30: 137142.
Verweij, JJ, Pit, DSS, van Lieshout, L, Baeta, SM, Dery, GD, Gasser, RB and Polderman, AM (2001). Determining the prevalence of Oesophagostomum bifurcum and Necator americanus infections using specific PCR amplification of DNA from faecal samples. Tropical Medicine and International Health 6: 726731.
Waller, PJ (1997). Anthelmintic resistance. Veterinary Parasitology 72: 391412.
Watson, H, Lee, DL and Hudson, PJ (1987). The effect of Trichostrongylus tenuis on the caecal mucosa of young, old and anthelmintic-treated wild red grouse, Lagopus lagopus scoticus. Parasitology 94: 405411.
Wilkinson, GT, Scott, PP and Cotchin, E (1966). Diseases of the cat. Oxford: Pergamon Press, pp. 304308.
Wilson, RB and Presnell, JC Jr (1990). Chronic gastritis due to Ollulanus tricuspis infection in a cat. Journal of the American Animal Hospital Association 26: 137139.
Zarlenga, DS, Stringfellow, F, Nobary, M and Lichtenfels, JR (1994). Cloning and characterisation of ribosomal RNA genes from three species of Haemonchus (Nematoda: Trichostrongyloidea) and identification of PCR primers for rapid differentiation. Experimental Parasitology 78: 2836.
Zarlenga, DS, Gasbarre, LC, Boyd, PC, Leighton, E and Lichtenfels, JR (1998a). Identification and semi-quantitation of Ostertagia ostertagi eggs by enzymatic amplification of ITS-1 sequences. Veterinary Parasitology 77: 245257.
Zarlenga, DS, Hoberg, EP, Stringfellow, F and Lichtenfels, JR (1998b). Comparisons of two polymorphic species of Ostertagia and phylogenetic relationships within the Ostertagiinae (Nematoda, Trichostrongyloidea) inferred from ribosomal DNA repeat and mitochondrial sequences. Journal of Parasitology 84: 806812.
Zarlenga, DS, Chute, MB, Gasbarre, LC and Boyd, PC (2001). A multiplex PCR assay for differentiating economically important gastrointestinal nematodes of cattle. Veterinary Parasitology 97: 199209.

Keywords

Related content

Powered by UNSILO

The use of nuclear ribosomal DNA markers for the identification of bursate nematodes (order Strongylida) and for the diagnosis of infections

  • Neil B. Chilton (a1)

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.