Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-20T04:12:30.378Z Has data issue: false hasContentIssue false

Acquisition of resistance after continuous infection with Ascaridia galli in chickens

Published online by Cambridge University Press:  08 July 2014

T. FERDUSHY*
Affiliation:
Section for Parasitology and Aquatic Diseases, Department of Veterinary Disease Biology, Faculty of Health and Medical Sciences, University of Copenhagen, Dyrlægevej 100, DK-1870, Frederiksberg C, Copenhagen, Denmark
T. W. SCHOU
Affiliation:
DHI, Environment and Toxicology, Agern Alle 5 Hørsholm, Denmark
L. R. NORUP
Affiliation:
Science and Technology, Department of Animal Science, Aarhus University, Blichers Alle 20, Post Box 50, 8830 Tjele, Denmark
T. S. DALGAARD
Affiliation:
Science and Technology, Department of Animal Science, Aarhus University, Blichers Alle 20, Post Box 50, 8830 Tjele, Denmark
S. M. THAMSBORG
Affiliation:
Section for Parasitology and Aquatic Diseases, Department of Veterinary Disease Biology, Faculty of Health and Medical Sciences, University of Copenhagen, Dyrlægevej 100, DK-1870, Frederiksberg C, Copenhagen, Denmark
P. NEJSUM
Affiliation:
Section for Parasitology and Aquatic Diseases, Department of Veterinary Disease Biology, Faculty of Health and Medical Sciences, University of Copenhagen, Dyrlægevej 100, DK-1870, Frederiksberg C, Copenhagen, Denmark
A. PERMIN
Affiliation:
DHI, Environment and Toxicology, Agern Alle 5 Hørsholm, Denmark
H. R. JUUL-MADSEN
Affiliation:
Science and Technology, Department of Animal Science, Aarhus University, Blichers Alle 20, Post Box 50, 8830 Tjele, Denmark
N. C. KYVSGAARD
Affiliation:
Section for Production and Health, Department of Large Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Grønnegårdsvej 2, DK-1870, Frederiksberg C, Copenhagen, Denmark
*
*Corresponding author: Section for Parasitology and Aquatic Diseases, Faculty of Health and Medical Sciences, University of Copenhagen, Dyrlægevej 100, DK-1870, Frederiksberg C, Copenhagen, Denmark. E-mail: [email protected]

Summary

Acquired resistance against Ascaridia galli infection was studied in seventy-two 18-week-old white Leghorn chickens allocated to six groups (G1–G6). In order to understand the population dynamics following trickle-infection (100 eggs per chicken twice weekly), chickens of subgroups of G1 were necropsied 3 days after 1, 6 or 12 inoculations (G1A, G1B and G1C respectively), while G2–G4 were inoculated for 6 weeks. G2 was necropsied 4 weeks after the last inoculation. The number of established larvae increased initially (between G1A and G1B) but decreased after repeated inoculations (G1C, G2). G3, G4 and G5 were used to measure the efficacy of anthelminthic treatment and to monitor the acquisition of resistance following a challenge infection. At week 7 G3, G4 and G5 were treated with flubendazole for 7 days in the feed. Two weeks after treatment the chickens in G4 and G5 were challenged with 500 eggs. G6 was left as uninfected control. Necropsy at week 10 after first inoculation revealed a lower establishment rate, an impaired development and a more posterior localization of the larvae in G4 (trickle-infected-treated-challenged) compared with G5 (treated-challenged). IgY level in serum reached noticeable level at 14 dpi in G2 and G4 chickens, and in G4 chickens IgY level further increased after challenge infection. The study provides evidence that acquired resistance against A. galli in chickens leads to a significant yet incomplete protection against re-infection.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2014 

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

REFERENCES

Ackert, J. E. (1923). On the habitat of Ascaridia perspicillum (Rud). Journal of Parasitology 10, 101103.CrossRefGoogle Scholar
Ackert, J. E. (1931). The morphology and life history of the fowl nematode Ascaridia lineata (Schneider). Parasitology 23, 360379.Google Scholar
Ackert, J. E. and Herrick, C. A. (1928). Effects of the nematode Ascaridia lineata (Schneider) on growing chickens. Journal of Parasitology 15, 113.Google Scholar
Ackert, J. E., Eisenbrandt, L. L., Wilmoth, J. H., Glading, B. and Pratt, I. (1935). Comparative resistance of five breeds of chickens to the nematode Ascaridia lineata (Schneider). Journal of Agricultural Research 50, 607624.Google Scholar
Araujo, P. and Bressan, C. R. (1977). Observations on the second moult of the larvae of Ascaridia galli. Annales de Parasitologie Hymaine et Comparee 52, 531537.CrossRefGoogle ScholarPubMed
Anonymous (1999). Council directive 1999/74/EC laying down minimum standards for the protection of laying hens. Official Journal of the European Communities L 203, 53.Google Scholar
Chadfield, M., Permin, A., Nansen, P. and Bisgaard, M. (2001). Investigation of the parasitic nematode Ascaridia galli (Schrank 1788) as potential vector for Salmonella enterica dissemination in poultry. Parasitology Research 87, 317325.Google Scholar
Das, G., Kaufmann, F., Abel, H. and Gauly, M. (2010). Effect of extra dietary lysine in Ascaridia galli-infected grower layers. Veterinary Parasitology 170, 238243.CrossRefGoogle ScholarPubMed
Degen, W. G. J., van Daal, N., Rothwell, L., Kaiser, P. and Schijns, V. E. J. C. (2005). Th1/Th2 polarization by viral and helminth infection in birds. Veterinary Microbiology 105, 163167.Google Scholar
Eysker, M. (1997). Some aspects of inhibited development of trichostrongylids in ruminants. Veterinary Parasitology 72, 265283.Google Scholar
Ferdushy, T., Nejsum, P., Roepstorff, A., Thamsborg, S. M. and Kyvsgaard, N. C. (2012). Ascaridia galli in chickens: intestinal localization and comparison of methods to isolate the larvae within the first week of infection. Parasitology Research 111, 22732279.Google Scholar
Ferdushy, T., Luna-Olivares, L. A., Nejsum, P., Roepstorff, A., Thamsborg, S. M. and Kyvsgaard, N. C. (2013). Population dynamics of Ascaridia galli following single infection in young chickens. Parasitology 140, 10781084.CrossRefGoogle ScholarPubMed
Gauly, M., Homann, T. and Erhardt, G. (2005). Age related differences of Ascaridia galli egg output and worm burden in chickens following a single dose infection. Veterinary Parasitology 128, 141148.CrossRefGoogle ScholarPubMed
Herd, R. P. and McNaught, D. J. (1975). Arrested development and the histotrophic phase of Ascaridia galli in the chicken. International Journal for Parasitology 5, 401406.Google Scholar
Höglund, J. and Jansson, D. S. (2011). Infection dynamics of Ascaridia galli in non-caged hens. Veterinary Parasitology 180, 267273.CrossRefGoogle ScholarPubMed
Idi, A., Permin, A. and Murrell, K. D. (2004). Host age only partially affects resistance to primary and secondary infections with Ascaridia galli (Schrank, 1788) in chickens. Veterinary Parasitology 122, 221231.CrossRefGoogle ScholarPubMed
Idi, A., Permin, A., Jensen, S. K. and Murrell, K. D. (2007). Effect of a minor vitamin A deficiency on the course of infection with Ascaridia galli (Schrank, 1788) and the resistance of chickens. Helminthologia 44, 39.CrossRefGoogle Scholar
Ikeme, M. M. (1970). Retarded metamorphosis in larvae of Ascaridia galli following repeated challenge of poultry with infective eggs. Veterinary Record 87, 725726.CrossRefGoogle ScholarPubMed
Jansson, D. S., Vågsholm, I., Nyman, A., Christensson, D., Göransson, M., Fossum, O. and Höglund, J. (2010). Ascarid infections in laying hens kept in different housing systems. Avian Pathology 39, 525532.Google Scholar
Kaufmann, F., Das, G., Sohnrey, B. and Gauly, M. (2011). Helminth infections in laying hens kept in organic free range systems in Germany. Livestock Science 141, 182187.CrossRefGoogle Scholar
Kerr, K. B. (1955). Age of chickens and the rate of maturation of Ascaridia galli. Journal of Parasitology 3, 233235.Google Scholar
Luna-Olivares, L. A., Ferdushy, T., Kyvsgaard, N. C., Nejsum, P., Thamsborg, S. M., Roepstorff, A. and Iburg, T. M. (2012). Localization of Ascaridia galli larvae in the jejunum of chickens 3 days post infection. Veterinary Parasitology 185, 186193.Google Scholar
Luna-Olivares, L. A., Kyvsgaard, N. C., Ferdushy, T., Nejsum, P., Thamsborg, S. M., Roepstorff, A. and Iburg, T. M. (2014). The jejunal cellular responses in chickens infected with a single dose of Ascaridia galli eggs. Parasitology Research in press.Google Scholar
Marcos-Atxutegi, C., Gandolfi, B., Arangüena, T., Sepúlveda, R., Arévalo, M. and Simón, F. (2009). Antibody and inflammatory responses in laying hens with experimental primary infections of Ascaridia galli. Veterinary Parasitology 161, 6975.Google Scholar
Michel, J. F. (1974). Arrested development of nematodes and some related phenomena. Advances in Parasitology 12, 279366.CrossRefGoogle ScholarPubMed
Norup, L. R., Dalgaard, T. S., Pleidrup, J., Permin, A., Schou, T. W., Jungersen, G., Flink, D. R. and Juul-Madsen, H. R. (2013). Comparison of parasite-specific immunoglobulin in two chicken lines during sustained infection with Ascaridia galli. Veterinary Parasitology 191, 187190.CrossRefGoogle ScholarPubMed
Permin, A. and Hansen, J. W. (1998). Epidemiology, Diagnosis and Control of Poultry Parasites. FAO Animal Health Manual No. 4. Food and Agricultural Organization of the United Nations, Rome, Italy.Google Scholar
Permin, A. and Ranvig, H. (2001). Genetic resistance to Ascaridia galli infections in chickens. Veterinary Parasitology 102, 101111.Google Scholar
Permin, A., Bojsen, M., Nansen, P., Bisgaard, M., Frandsen, F. and Pearman, M. (1997). Ascaridia galli populations in chicken following single infections with different dose level. Parasitology Research 83, 614617.Google Scholar
Permin, A., Bisgaard, M., Frandsen, F., Pearman, M., Kold, J. and Nansen, P. (1999). Prevalence of gastrointestinal helminths in different poultry production systems. British Poultry Science 40, 439443.Google Scholar
Phiri, I. K., Phiri, A. M., Ziela, M., Chota, A., Masuku, M. and Monrad, J. (2007). Prevalence and distribution of gastrointestinal helminths and their effects on weight gain in free-range chickens in central Zambia. Tropical Animal Health and Production 39, 309315.Google Scholar
Roepstorff, A., Eriksen, L., Slotved, H. C. and Nansen, P. (1997). Experimental Ascaris suum infection in the pig: worm population kinetics following single inoculations with three doses of infective eggs. Parasitology 115, 443452.Google Scholar
Schou, T., Permin, A., Roepstorff, A., Sørensen, P. and Kjær, J. (2003). Comparative genetic resistance to Ascaridia galli infections of 4 different commercial layer-lines. British Poultry Science 44, 182185.CrossRefGoogle ScholarPubMed
Schwarz, A., Gauly, M., Abel, H., Das, G., Humburg, J., Rohn, K., Breves, G. and Rautenschlein, S. (2011). Immunopathogenesis of Ascaridia galli infection in layer chicken. Developmental and Comparative Immunology 35, 774784.Google Scholar
Schummer, A., Vollmerhaus, B., Sinowatz, F., Frewein, J. and Waibl, H. (1992). Anatomie der vögel. In Lehrbuch der anatomie der Haustiere (ed. Nickel, R., Schummer, A. and Seiferle, E.), 2nd Edn, pp. 203204. Paul Parey, Berlin, Germany.Google Scholar
Tugwell, R. L. and Ackert, J. E. (1952). On the tissue phase of the life cycle of the fowl nematode Ascaridia galli (Schrank). Journal of Parasitology 38, 277288.Google Scholar