Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-27T21:10:13.735Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  28 February 2007

Neil B. Chilton
Neil B. Chilton*
Affiliation:
Department of Biology, University of Saskatchewan, 112 Science Place, Saskatoon, Saskatchewan S7N 5E2, Canada
*
*E-mail: neil.chilton@usask.ca
Get access Rights & Permissions [Opens in a new window]

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.

Keywords

nuclear ribosomal DNADNA markersStrongylidadiagnosisinfections
Type
Research Article
Information
Animal Health Research Reviews , Volume 5 , Issue 2 , December 2004 , pp. 173 - 187
Copyright
Copyright © CAB International 2004

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

Albonico, M, Crompton, DWT, Saviolli, L (1999) Control strategies for human intestinal nematode infections. Advances in Parasitology 42: 277–341.CrossRefGoogle ScholarPubMed
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. 41–229.CrossRefGoogle Scholar
Anderson, JC, Blouin, MS and Beech, RN (1998). Population biology of parasitic nematodes: applications of genetic markers. Advances in Parasitology 41: 219–283.CrossRefGoogle ScholarPubMed
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: 213–253.Google ScholarPubMed
Arnheim, N (1983). Concerted evolution of multigene families. In: Nei, M and Koehn, RK, editors. Evolution of Genes and Proteins. Sunderland (MA): Sinauer, pp. 38–61.Google Scholar
Arundel, JH (1985). Parasitic Diseases of the Horse Sydney: Post-Graduate Foundation in Veterinary Science, University of Sydney, pp. 4–26.Google Scholar
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. 141–154.CrossRefGoogle Scholar
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: 361–379.CrossRefGoogle Scholar
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: 39–51.CrossRefGoogle Scholar
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: 187–191.CrossRefGoogle ScholarPubMed
Barton, NJ and Seward, DA (1993). Detection of Libyostrongylus douglassi in ostriches in Australia. Australian Veterinary Journal 70: 31–32.CrossRefGoogle ScholarPubMed
Beck, T, Moir, B and Meppen, T (1985). The cost of parasites to the Australian sheep industry. Quarterly Review of the Rural Economy 7: 336–343.Google Scholar
Berrag, B and Cabaret, J (1996). Impaired pulmonary gas exchange in ewes naturally infected by small lungworms. International Journal for Parasitology 26: 1397–1400.CrossRefGoogle ScholarPubMed
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: 143–148.Google Scholar
Beveridge, I (1979). Hypodontus macropi Mönnig, 1929, a hookworm-like parasite of macropodid marsupials. Journal of Helminthology 53: 229–244.CrossRefGoogle ScholarPubMed
Beveridge, I and Chilton, NB (2001). Co-evolutionary relationships between the nematode subfamily Cloacininae and its marsupial hosts. International Journal for Parasitology 31: 976–996.CrossRefGoogle ScholarPubMed
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: 597–620.CrossRefGoogle Scholar
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: 71–75.CrossRefGoogle ScholarPubMed
Blouin, MS (2002). Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. International Journal for Parasitology 32: 527–531.CrossRefGoogle ScholarPubMed
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: 470–476.CrossRefGoogle ScholarPubMed
Blouin, MS, Yowell, CA, Courtney, CH and Dame, JB (1995). Host movement and the genetic structure of populations of parasitic nematodes. Genetics 141: 1007–1014.CrossRefGoogle ScholarPubMed
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: 1383–1387.CrossRefGoogle ScholarPubMed
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: 419–427.CrossRefGoogle ScholarPubMed
Bowman, DD, Hendrix, CM, Lindsay, DS and Barr, SC (2002). Feline Clinical Parasitology. Ames (IA): Iowa State University Press, pp. 241–273.CrossRefGoogle Scholar
Bowman, DD, Lynn, RC and Eberhard, ML (2003). Georgis' Parasitology for Veterinarians. 8th edn. Missouri: Elsevier Science, pp. 155–196.Google Scholar
Buckler, ES IV, Ippolito, A and Holtsford, TP (1997). The evolution of ribosomal DNA: divergent paralogues and phylogenetic implications. Genetics 145: 821–832.CrossRefGoogle ScholarPubMed
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: 185–192.CrossRefGoogle ScholarPubMed
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: 359–365.CrossRefGoogle Scholar
Carreno, RA and Nadler, SA (2003). Phylogenetic analysis of the Metastrongyloidea (Nematoda: Strongylida) inferred from ribosomal RNA gene sequences. Journal of Parasitology 89: 965–973.CrossRefGoogle ScholarPubMed
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: 1971–1977.CrossRefGoogle ScholarPubMed
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: 647–651.CrossRefGoogle Scholar
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: 1481–1494.CrossRefGoogle ScholarPubMed
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: 119–124.CrossRefGoogle ScholarPubMed
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: 1765–1773.CrossRefGoogle Scholar
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: 367–386.CrossRefGoogle ScholarPubMed
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: 81–93.CrossRefGoogle Scholar
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: 33–39.Google ScholarPubMed
Christensen, CM, Zarlenga, DS and Gasbarre, LC (1994a). Identification of a Haemonchus placei-specific DNA probes. Journal of the Helminthological Society of Washington 61: 249–252.Google Scholar
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: 93–100.CrossRefGoogle ScholarPubMed
Clayton, HM and Trawford, AF (1981). Anthelmintic control of lungworm in donkeys. Equine Veterinary Journal 13: 192–194.CrossRefGoogle ScholarPubMed
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.Google Scholar
Coles, BH (1997). Avian Medicine and Surgery. Oxford: Blackwell Science, pp. 338–341.Google Scholar
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: 1935–1940.CrossRefGoogle ScholarPubMed
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: 195–206.CrossRefGoogle ScholarPubMed
Copland, JW (1974). Metastrongylus spp. infections of village pigs in Papua New Guinea. Journal of Helminthology 48: 25–32.CrossRefGoogle ScholarPubMed
Corwin, RM (1997). Economics of gastrointestinal parasitism of cattle. Veterinary Parasitology 72: 451–460.CrossRefGoogle ScholarPubMed
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. 718–734.Google Scholar
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: 655–658.CrossRefGoogle ScholarPubMed
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: 863–866.CrossRefGoogle ScholarPubMed
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: 275–280.CrossRefGoogle ScholarPubMed
Demartini, JC and Davies, RB (1997). An epizootic of pneumonia in captive bighorn sheep with Muellerius sp. Journal of Wildlife Diseases 13: 117–124.CrossRefGoogle Scholar
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: 193–201.CrossRefGoogle ScholarPubMed
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: 769–775.CrossRefGoogle ScholarPubMed
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: 1005–1008.CrossRefGoogle ScholarPubMed
Dorris, M and Blaxter, M (2000). The small subunit ribosomal RNA sequence of Strongyloides stercoralis. International Journal for Parasitology 30: 939–941.CrossRefGoogle ScholarPubMed
Dorris, M, Viney, ME, and Blaxter, M (2002). Molecular phylogenetic analysis of the genus Strongyloides and related nematodes. International Journal for Parasitology 32: 1507–1517.CrossRefGoogle ScholarPubMed
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: 2246–2256.CrossRefGoogle Scholar
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. 1–68.Google Scholar
Durette-Desset, M-C and Chabaud, AG (1981). Nouvel essai de classification des nématodes Trichostrongyloidea. Annales de Parasitologie Humaine et Comparée 3: 297–312.CrossRefGoogle Scholar
Durette-Desset, M-C and Chabaud, AG (1993). Nomenclature des Strongylida au-dessus du groupe famille. Annales de Parasitologie Humaine et Comparée 68: 111–112.CrossRefGoogle Scholar
Durette-Desset, M-C, Beveridge, I and Spratt, DM (1994). The origins and evolutionary expansion of the Strongylida (Nematoda). International Journal for Parasitology 24: 1139–1165.CrossRefGoogle ScholarPubMed
Elder, JF and Turner, BJ (1995). Concerted evolution of repetitive DNA sequences in eukaryotes. Quarterly Review of Biology 70: 297–320.CrossRefGoogle ScholarPubMed
Ellis, RE, Sulston, JE and Coulson, AR (1986). The rDNA of C. elegans sequence and structure. Nucleic Acids Research 14: 2345–2364.CrossRefGoogle ScholarPubMed
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: 73–78.CrossRefGoogle ScholarPubMed
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: 17–21.CrossRefGoogle Scholar
Eysker, M, Boersema, JH and Kooyman, FN (1990). Seasonally inhibited development of yathostome nematodes in Shetland ponies in The Netherlands. Veterinary Parasitology 36: 259–264.CrossRefGoogle ScholarPubMed
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: 713–722.CrossRefGoogle ScholarPubMed
Gasser, RB (1997). Mutation scanning methods for the analysis of parasite genes. International Journal for Parasitology 27: 1449–1463.CrossRefGoogle ScholarPubMed
Gasser, RB (1999). PCR-based technology in veterinary parasitology. Veterinary Parasitology 84: 29–258.CrossRefGoogle ScholarPubMed
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: 201–213.CrossRefGoogle Scholar
Gasser, RB and Hoste, H (1995). Genetic markers for closely-related parasitic nematodes. Molecular and Cellular Probes 9: 315–320.CrossRefGoogle ScholarPubMed
Gasser, RB and Newton, SE (2000). Genomic and genetic research on bursate nematodes: significance, implications and prospects. International Journal for Parasitology 30: 509–534.CrossRefGoogle ScholarPubMed
Gasser, RB and Zhu, XQ (1999). Sequence-based analysis of DNA fragments by mutation detection techniques. Parasitology Today 15: 462–465.CrossRefGoogle ScholarPubMed
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: 2525–2526.CrossRefGoogle ScholarPubMed
Gasser, RB, Chilton, NB, Hoste, H and Stevenson, LA (1994). Species identification of trichostrongyle nematodes by PCR-linked RFLP. International Journal for Parasitology 24: 291–293.CrossRefGoogle ScholarPubMed
Gasser, RB, Nansen, P and Gulberg, P (1996a). Fingerprinting sequence variation in ribosomal DNA of parasites by DGGE. Molecular and Cellular Probes 10: 95–103.CrossRefGoogle ScholarPubMed
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: 371–378.CrossRefGoogle ScholarPubMed
Gasser, RB, Stewart, LE and Speare, R (1996c). Genetic markers in ribosomal DNA for hookworm identification. Acta Tropica 62: 15–21.CrossRefGoogle ScholarPubMed
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: 1564–1566.CrossRefGoogle ScholarPubMed
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: 303–312.CrossRefGoogle ScholarPubMed
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: 2391–2395.CrossRefGoogle Scholar
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: 1809–1817.CrossRefGoogle ScholarPubMed
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: 1087–1091.CrossRefGoogle ScholarPubMed
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: 1076–1085.3.0.CO;2-8>CrossRefGoogle ScholarPubMed
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. 219–234.CrossRefGoogle Scholar
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: 44–57.Google Scholar
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: 119–124.CrossRefGoogle Scholar
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: 430–442.CrossRefGoogle ScholarPubMed
Gray, GD (1987). Genetic resistance to haemonchosis in sheep. Parasitology Today 3: 253–255.CrossRefGoogle ScholarPubMed
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: 536–540.CrossRefGoogle ScholarPubMed
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: 393–414.Google ScholarPubMed
Haupt, W (1966). Ein Beitrag zur Morphologie der Knötchenwürmer des Hausschweines, ihrer Eier sowie der dritten invasionstüchtigen Larvenstadien. Archiv für Experimentelle Veterinarmedizin 20: 701–711.Google Scholar
Herd, RP (1986). Epidemiology and control of parasites in northern temperate regions. Veterinary Clinics of North America: Equine Practice 2: 337–356.Google ScholarPubMed
Hillis, DM and Dixon, MT (1991). Ribosomal DNA: molecular evolution and phylogenetic inference. Quarterly Review of Biology 66: 411–453.CrossRefGoogle ScholarPubMed
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. 193–227.CrossRefGoogle Scholar
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: 1427–1435.CrossRefGoogle ScholarPubMed
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: 607–611.CrossRefGoogle ScholarPubMed
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: 179–187.CrossRefGoogle ScholarPubMed
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: 1069–1071.CrossRefGoogle ScholarPubMed
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: 75–80.CrossRefGoogle ScholarPubMed
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: 1251–1260.CrossRefGoogle ScholarPubMed
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: 3357–3363.3.0.CO;2-B>CrossRefGoogle ScholarPubMed
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: 134–212.Google Scholar
Huchzermeyer, FW (1998). Diseases of Ostriches and Other Ratites. Pretoria: Promedia, pp. 182–186.Google Scholar
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: 1925–1929.3.0.CO;2-7>CrossRefGoogle ScholarPubMed
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: 135–147.CrossRefGoogle Scholar
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: 1407–1411.CrossRefGoogle ScholarPubMed
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: 601–605.CrossRefGoogle Scholar
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: 1949–1964.CrossRefGoogle ScholarPubMed
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: 285–291.CrossRefGoogle ScholarPubMed
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: 69–80.CrossRefGoogle ScholarPubMed
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: 95–103.CrossRefGoogle ScholarPubMed
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: 831–836.CrossRefGoogle ScholarPubMed
Kaplan, RM (2002). Anthelmintic resistance in nematodes of horses. Veterinary Research 33: 491–507.CrossRefGoogle ScholarPubMed
Klei, TR (1991). Recent observation on the epidemiology, pathogenesis and immunology of equine helminth infections. Equine Infectious Diseases 6: 129–136.Google Scholar
Klei, TR and French, DD (1998). Small strongyles: an emerging parasite problem for horses. Equine Practitioner 20: 26–30.Google Scholar
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: 135–143.CrossRefGoogle ScholarPubMed
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. 228–278.CrossRefGoogle Scholar
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: 606–611.CrossRefGoogle ScholarPubMed
Leignel, V, Cabaret, J and Humbert, JF (2002). New molecular evidence that Teladorsagia circumcincta (Nematoda: Trichostrongylidea) is a species complex. Journal of Parasitology 88: 135–140.CrossRefGoogle ScholarPubMed
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. 1–41.Google Scholar
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. 1–26.Google Scholar
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: 225–245.CrossRefGoogle ScholarPubMed
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: 65–79.CrossRefGoogle Scholar
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: 337–342.CrossRefGoogle ScholarPubMed
Lyons, ET, Tolliver, SC and Drudge, JH (1999). Historical perspective of cyathostomes: prevalence, treatment and control programs. Veterinary Parasitology 85: 97–112.CrossRefGoogle ScholarPubMed
Love, S, Murphy, D and Mellor, D (1999). Pathogenicity of cyathostome infections. Veterinary Parasitology 85: 113–122.CrossRefGoogle Scholar
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: 202–203.Google ScholarPubMed
Matthee, S, Krecek, RC, and Milne, SA (2000). Prevalence and biodiversity of helminth parasites in donkeys from South Africa. Journal of Parasitology 86: 756–762.CrossRefGoogle ScholarPubMed
Matthee, S, Krecek, RC, and Gibbons, LM (2002). Cylicocyclus asinus n.sp. (Nematoda: Cyathostominae) from donkeys, Equus asinus, in South Africa. Systematic Parasitology 51: 29–35.CrossRefGoogle ScholarPubMed
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: 649–659.CrossRefGoogle ScholarPubMed
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: 252–257.Google ScholarPubMed
McManus, DP and Bowles, J (1996). Molecular genetic approaches to parasite identification: their value in diagnostic parasitology and systematics. International Journal for Parasitology 26: 687–704.CrossRefGoogle ScholarPubMed
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. 279–300.CrossRefGoogle Scholar
Migaki, G, Vandyke, D and Hubbard, RG (1971). Some histopathologic lesions caused by helminths in marine mammals. Journal of Wildlife Diseases 7: 281–289.CrossRefGoogle ScholarPubMed
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: 71–78.CrossRefGoogle ScholarPubMed
Morales, GA and Helmboldt, CF (1971). Verminous pneumonia in the Californian sea lion (Zalophus californianus). Journal of Wildlife Diseases 7: 22–27.CrossRefGoogle Scholar
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: 2989–3996.CrossRefGoogle ScholarPubMed
Nadler, SA (1990). Molecular approaches to studying helminth population genetics and phylogeny. International Journal for Parasitology 20: 11–19.CrossRefGoogle ScholarPubMed
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: 1099–1106.CrossRefGoogle ScholarPubMed
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: 588–601.CrossRefGoogle ScholarPubMed
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: 149–153.CrossRefGoogle ScholarPubMed
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: 331–336.CrossRefGoogle ScholarPubMed
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: 337–341.CrossRefGoogle ScholarPubMed
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: 1781–1789.CrossRefGoogle ScholarPubMed
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: 1–15.CrossRefGoogle ScholarPubMed
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: 218–224.CrossRefGoogle ScholarPubMed
Paterson, MW, Gibbs, C, Wotton, PR and Day, MJ (1993). Angiostrongylus vasorum infection in seven days. Veterinary Record 133: 565–570.Google Scholar
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: 169–176.CrossRefGoogle ScholarPubMed
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: 611–615.CrossRefGoogle ScholarPubMed
Roos, MH and Grant, WN (1993). Species-specific PCR for the parasitic nematodes Haemonchus contortus and Trichostrongylus colubriformis. International Journal for Parasitology 23: 419–421.CrossRefGoogle ScholarPubMed
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: 119–126.CrossRefGoogle Scholar
Samson-Himmelstjerna, G, von Harder, A and Schneider, T (2002). Quantitative analysis of ITS2 sequences in trichostrongyle parasites. International Journal for Parasitology 32: 1529–1535.CrossRefGoogle Scholar
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: 417–418.CrossRefGoogle ScholarPubMed
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: 392–394.CrossRefGoogle ScholarPubMed
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: 1–105.Google Scholar
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: 483–488.CrossRefGoogle Scholar
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: 1123–1126.CrossRefGoogle Scholar
Stewart, TB and Gasbarre, LC (1989). The veterinary importance of nodular worms (Oesophagostomum spp). Parasitology Today 5: 209–213.CrossRefGoogle Scholar
Stockdale, PHG (1970). The pathogenesis of the lesions elicited by Aelurostrongylus abstrusus during its prepatent period. Pathologia Veterinaria 7: 102–115.CrossRefGoogle ScholarPubMed
Sweeny, JC and Gilmartin, WG (1974). Survey of diseases in free-living Californian sea lions. Journal of Wildlife Diseases 10: 370–376.CrossRefGoogle Scholar
Taylor, DJ (1995). Pig Diseases. Bury St Edmunds, UK: St Edmundsbury Press, pp. 236–239.Google Scholar
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: 899–910.CrossRefGoogle ScholarPubMed
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: 789–801.CrossRefGoogle ScholarPubMed
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: 137–142.CrossRefGoogle ScholarPubMed
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: 726–731.CrossRefGoogle ScholarPubMed
Waller, PJ (1997). Anthelmintic resistance. Veterinary Parasitology 72: 391–412.CrossRefGoogle ScholarPubMed
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: 405–411.CrossRefGoogle ScholarPubMed
Wilkinson, GT, Scott, PP and Cotchin, E (1966). Diseases of the cat. Oxford: Pergamon Press, pp. 304–308.Google Scholar
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: 137–139.Google Scholar
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: 28–36.CrossRefGoogle ScholarPubMed
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: 245–257.CrossRefGoogle ScholarPubMed
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: 806–812.CrossRefGoogle Scholar
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: 199–209.CrossRefGoogle ScholarPubMed