Parasitology Research

, Volume 118, Issue 3, pp 1031–1038 | Cite as

Worm burdens and associated histopathological changes caused by gastrointestinal nematodes in alpacas from Australia

  • Mohammed H. Rashid
  • Ian Beveridge
  • Jane L. Vaughan
  • Abdul JabbarEmail author
Helminthology - Short Communication


In this study, 100 gastrointestinal tracts of Australian alpacas were examined to assess the worm burden and to identify the species of nematode present. Faecal samples were collected from 97 alpacas and processed for faecal egg counts (FECs). For identification of the species, both molecular (multiplexed-tandem polymerase chain reaction [MT-PCR]) and morphological techniques were used. Total worm counts (TWCs) revealed a mean burden of 1300 worms, with the highest burden of 29,000 worms. The average egg count was 501 eggs per gram of faeces (EPG), with the highest count of 3500 EPG. Nineteen different species of gastrointestinal nematodes (GINs) were identified, and Graphinema auchenia, Camelostrongylus mentulatus and Trichuris tenuis were recovered from Australian alpacas for the first time. Haemonchus contortus was the most prevalent nematode (81%) followed by C. mentulatus (60%). The majority of the nematodes found are shared with sheep, goats and cattle. Findings of this study provide useful insights into the spectrum of GINs and their burden in Australian alpacas.


Gastrointestinal nematodes Alpaca Total worm count Camelostrongylus mentulatus Graphinema auchenia Haemonchus contortus 



We are grateful to alpaca farmers who provided the gastrointestinal and faecal samples for this study. We are thankful to Ms. Christine Andersen and Doctor of Veterinary Medicine Students for their technical assistance.


The financial assistance for this project was provided by the AgriFutures Australia and the Australian Alpaca Association. M.H.R. is a grateful recipient of the Australian Postgraduate Award through the University of Melbourne and the PhD top-up scholarship from the AgriFutures Australia.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interests.


  1. Altman DG (1991) Practical statistics for medical research. Chapman and Hall, LondonGoogle Scholar
  2. Anderson N (1972) Trichostrongylid infections of sheep in a winter rainfall region. 1. Epizootiological studies in the Western District of Victoria, 1966–67. Aust J Agric Res 23:1113–1129CrossRefGoogle Scholar
  3. Anderson N (1973) Trichostrongylid infections of sheep in a winter rainfall region. 2. Epizootiological studies in the Western District of Victoria, 1967–68. Aust J Agric Res 24:599–611CrossRefGoogle Scholar
  4. Averbeck GA, Scholtthauer JC, Hinueber JG (1981) Camelostrongylus mentulatus infection in a camel (Camelus dromedarius): a case report. J Zoo Anim Med 12:24–26CrossRefGoogle Scholar
  5. Ballweber LR (2009) Ecto- and endoparasites of new world camelids. Vet Clin North Am Food Anim Prac 25:295–310CrossRefGoogle Scholar
  6. Barger IA (1993) Control of gastrointestinal nematodes in Australia in the 21st century. Vet Parasitol 46:23–32CrossRefPubMedGoogle Scholar
  7. Becklund WW, Walker ML (1967) Nematodirus of domestic sheep, Ovis aries, in the United States with a key to the species. J Parasitol 53:777–781CrossRefPubMedGoogle Scholar
  8. Beldomenico PM, Uhart M, Bono MF, Marull C, Baldi R, Peralta JL (2003) Internal parasites of free-ranging guanacos from Patagonia. Vet Parasitol 118:71–77CrossRefPubMedGoogle Scholar
  9. Beveridge I, Ford GE (1982) The trichostrongyloid parasites of sheep in South Australia and their regional distribution. Aust Vet J 59:177–179CrossRefPubMedGoogle Scholar
  10. Beveridge I, Barker I, Rickard M, Burton J (1974) Experimental infection of sheep with Camelostrongylus mentulatus and associated gastritis. Aust Vet J 50:36–37CrossRefPubMedGoogle Scholar
  11. Beveridge I, Pullman AL, Henzell R, Martin RR (1987) Helminth parasites of feral goats in South Australia. Aust Vet J 64:111–112CrossRefPubMedGoogle Scholar
  12. Beveridge I, Pullman AL, Phillips PH, Martin RR, Barelds A, Grimson R (1989) Comparison of the effects of infection with Trichostrongylus colubriformis, T. vitrinus and T. rugatus in merino lambs. Vet Parasitol 32:229–245CrossRefPubMedGoogle Scholar
  13. Brunsdon RV (1971) Trichostronglye worm infection in cattle: further studies on problems of diagnosis and on seasonal patterns of occurrence. N Z Vet J 19:203–212CrossRefPubMedGoogle Scholar
  14. Bryan R, Kerr J (1989) The relation between the natural worm burden of steers and the faecal egg count differentiated to species. Vet Parasitol 30:327–334CrossRefPubMedGoogle Scholar
  15. Cafrune MM, Aguirre DH, Rickard LG (1999) Recovery of Trichuris tenuis Chandler, 1930, from camelids (Lama glama and Vicugna vicugna) in Argentina. J Parasitol 85:961–962CrossRefPubMedGoogle Scholar
  16. Carmichael IH (1999) Internal parasitism in alpacas in southern Australia. In: Australian Alpaca Fibre – Improving Productivity and Marketing. Rural Industries Research and Development Corporation, Canberra, pp. 92–130Google Scholar
  17. Chandler AC (1930) Specific characters in the genus Trichuris, with a description of a new species, Trichuris tenuis, from a camel. J Parasitol 16:198–206Google Scholar
  18. Contreras S, Chávez V, Pinedo V, Leyva V, Suárez A (2014) Helminthiasis in alpacas (Vicugna pacos) of two peasant communities in Macusani, Puno during the dry season. Rev Investig Vet Perú 25:268–275CrossRefGoogle Scholar
  19. Copland JW (1965) Ostertagia mentulata recorded in New South Wales. Aust Vet J 41:27–27CrossRefGoogle Scholar
  20. Dittmer KE, Hinkson JA, Dwyer C, Adlington B, van Andel M (2018) Prevalence of Candidatus Mycoplasma haemolamae, bovine viral diarrhoea virus, and gastrointestinal parasitism in a sample of adult New Zealand alpaca (Vicugna pacos). N Z Vet J 66:9–15CrossRefPubMedGoogle Scholar
  21. Gibbons LM, Khalil LF (1982) A key for the identification of genera of the nematode family Trichostrongylidae Leiper, 1912. J Helminthol 56:185–233Google Scholar
  22. Gordon HM, Whitlock H (1939) A new technique for counting nematode eggs in sheep faeces. J CSIR 12:50–52Google Scholar
  23. Hertzberg H, Kohler L (2006) Prevalence and significance of gastrointestinal helminths and protozoa in south American camelids in Switzerland. Berl Munch Tierarztl Wochenschr 119:291–294PubMedGoogle Scholar
  24. Hill F, Death A, Wyeth T (1993) Nematode burdens of alpacas sharing grazing with sheep in New Zealand. NZ Vet J 41:205–208CrossRefGoogle Scholar
  25. Hilton RJ, Barker IK, Rickard MD (1978) Distribution and pathogenicity during development of Camelostrongylus mentulatus in the abomasum of sheep. Vet Parasitol 4:231–242CrossRefGoogle Scholar
  26. Hutchinson G (2009) Nematode parasites of small ruminants, camelids and cattle: diagnosis with emphasis on anthelmintic efficacy and resistance testing. Aquatic and Terrestrial Australian and New Zealand Standard Diagnostic Procedures (ANZSDPs)
  27. Hyuga A, Matsumoto J (2016) A survey of gastrointestinal parasites of alpacas (Vicugna pacos) raised in Japan. J Vet Med Sci 78:719–721CrossRefPubMedGoogle Scholar
  28. Jabbar A, Campbell AJD, Charles JA, Gasser RB (2013) First report of anthelmintic resistance in Haemonchus contortus in alpacas in Australia. Parasit Vectors 6:243CrossRefPubMedPubMedCentralGoogle Scholar
  29. McKenna PB (1981) The diagnostic value and interpretation of faecal egg counts in sheep. N Z Vet J 29(8):129–132CrossRefPubMedGoogle Scholar
  30. Michel JF (1969a) Observations on the faecal egg count of calves naturally infected with Ostertagia ostertagi. Parasitology 59:829–835Google Scholar
  31. Michel JF (1969b) The regulation of egg output by Ostertagia ostertagi in calves infected once only. Parasitology 59:767–774Google Scholar
  32. Presidente PJA (2007) Alpaca parasites & their control: recent experiences. Australian Alpaca Veterinarians Annual Conference, Australia, pp 1–14Google Scholar
  33. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria Google Scholar
  34. Rashid MH, Gebrekidan H, Jabbar A (2018a) Multiplexed-tandem PCR (MT-PCR) assay to detect and differentiate gastrointestinal nematodes of alpacas. Parasit Vectors 11:370CrossRefPubMedPubMedCentralGoogle Scholar
  35. Rashid MH, Stevenson MA, Waenga S, Mirams G, Campbell AJD, Vaughan JL, Jabbar A (2018b) Comparison of McMaster and FECPAKG2 methods for counting nematode eggs in the faeces of alpacas. Parasit Vectors 11:278CrossRefPubMedPubMedCentralGoogle Scholar
  36. Rashid MH, Vaughan JL, Stevenson MA, Campbell AJD, Saeed MA, Indjein L, Beveridge I, Jabbar A (2019a) Epidemiology of gastrointestinal nematodes of alpacas in Australia: I. a cross-sectional study. Parasitol Res.
  37. Rashid MH, Vaughan JL, Stevenson MA, Saeed MA, Campbell AJD, Beveridge I, Jabbar A (2019b) Epidemiology of gastrointestinal nematodes of alpacas in Australia: II. A longitudinal study. In: Parasitol res.
  38. Rickard LG (1993) Parasitic gastritis in a llama (Lama glama) associated with inhibited larval Teladorsagia spp. (Nematoda: Trichostrongyloidea). Vet Parasitol 45:331–335CrossRefPubMedGoogle Scholar
  39. Rickard LG, Bishop JK (1991) Redescription of Trichuris tenuis Chandler, 1930, from llamas (Lama glama) in Oregon with a key to the species of Trichuris present in north American ruminants. J Parasitol 77:70–75CrossRefPubMedGoogle Scholar
  40. Roberts F (1957) Reactions of calves to infestation with the stomach worm, Haemonchus placei (place, 1893) ransom, 1911. Aust J Agric Res 8:740–767CrossRefGoogle Scholar
  41. Roeber F, Jex AR, Gasser RB (2013) Comparative evaluation of two DNA isolation techniques for PCR-based diagnosis of gastrointestinal nematode infections in sheep. Mol Cell Probes 27:153–157CrossRefPubMedGoogle Scholar
  42. Rogers WP (1939) Nematode parasites of sheep in Western Australia. J Helminthol 17:151–158CrossRefGoogle Scholar
  43. Rose JH, Small AJ (1980) Transmission of Oesophagostomum spp. among sows at pasture. Vet Rec 107:223–225CrossRefPubMedGoogle Scholar
  44. Rubin R (1967) Some observations on the interpretation of fecal egg counts. Amer J Vet Clin Path 1:145–148Google Scholar
  45. Schmäschke R (2015) Endo-and ectoparasites of south American camelids and their control. Tierarztl Prax Ausg G Grosstiere Nutztiere 43:169–179CrossRefPubMedGoogle Scholar
  46. Stevenson M, Nunes T, Heuer C, Marshall J, Sanchez J, Thornton R, Reiczigel J, Robison-Cox J, Sebastiani P, Solymos P, Yoshida K, Jones G, Pirikahu S, Firestone S, Kyle R, Popp J, Mathew J (2018) epiR: tools for the analysis of epidemiological data. Faculty of Veterinary and Agricultural Sciences, the. University of Melbourne, MelbourneGoogle Scholar
  47. Tait SA, Kirwan JA, Fair CJ, Coles GC, Stafford KA (2002) Parasites and their control in south American camelids in the United Kingdom. Vet Rec 150:637–638CrossRefPubMedGoogle Scholar
  48. Thomas RJ, Boag B (1973) Epidemiological studies on gastro-intestinal nematode parasites of sheep. The control of infection in lambs on contaminated pasture. Res Vet Sci 14:11–20CrossRefPubMedGoogle Scholar
  49. Welchman DB, Parr J, Wood R, Mead A, Starnes A (2008) Alpaca and llama nematodes in Britain. Vet Rec 162:832–832CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Veterinary Biosciences, Melbourne School of Veterinary ScienceThe University of MelbourneWerribeeAustralia
  2. 2.Cria GenesisOcean GroveAustralia

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