Skip to main content Accessibility help

Gastrointestinal helminths in indigenous and exotic chickens in Vietnam: association of the intensity of infection with the Major Histocompatibility Complex

  • T. W. SCHOU (a1), A. PERMIN (a1) (a2), H. R. JUUL-MADSEN (a3), P. SØRENSEN (a4), R. LABOURIAU (a4), T. L. H. NGUYÊN (a5), M. FINK (a1) and S. L. PHAM (a6)...


This study compared the prevalence and intensity of infections of helminths in 2 chicken breeds in Vietnam, the indigenous Ri and the exotic Luong Phuong. Also, possible correlations with the Major Histocompatibility Complex (MHC) were tested. The most prevalent helminths were Ascaridia galli, Heterakis beramporia, Tetrameres mothedai, Capillaria obsignata, Raillietina echinobothrida and Raillietina tetragona. Differences in prevalence and intensity of infection were found between the 2 breeds. Comparing the 2 groups of adult birds, Ri chickens were observed to have higher prevalence and infection intensities of several species of helminths, as well as a higher mean number of helminth species. In contrast, A. galli and C. obsignata were shown to be more prevalent in Luong Phuong chickens. Furthermore, an age-dependent difference was indicated in the group of Ri chickens in which the prevalence and the intensity of infection was higher for the adult than the young chickens for most helminths. The most notable exception was the significantly lower prevalence and intensities of A. galli in the group of adult chickens. In contrast, the prevalence and intensity were very similar in both age groups of Luong Phuong chickens. Using a genetic marker located in the MHC, a statistically significant correlation between several MHC haplotypes and the infection intensity of different helminth species was inferred. This is the first report of an association of MHC haplotype with the intensity of parasite infections in chickens.


Corresponding author

Department of Veterinary Pathobiology, Section for Poultry Diseases, The Royal Veterinary and Agricultural University, Stigbojlen 4, DK-1870 Frederiksberg C, Denmark. Tel: +45 35283686. Fax: +45 35282757. E-mail:


Hide All


Ackert, J. E., Porter, D. A. and Beach, T. D. ( 1935). Age resistance of chickens to the nematode Ascaridia lineata (Schneider). Journal of Parasitology 21, 205213.
Agresti, A. ( 1990). Categorical Data Analysis. 1st Edn. John Wiley and Sons, New York.
Anderson, R. C. ( 1992). Nematode Parasites of Vertebrates: their Development and Transmission. 1st Edn. CAB International, Wallingford, UK.
Anderson, S. ( 2003). Animal genetic resources and sustainable livelihoods. Ecological Economics 45, 331339.
Baelmans, R., Parmentier, H. K., Nieuwland, M. G., Dorny, P., Demey, F. and Berkvens, D. ( 2005). Haemolytic complement activity and humoral immune responses to sheep red blood cells in indigenous chickens and in eight German Dahlem Red chicken lines with different combinations of major genes (dwarf, naked neck and frizzled) of tropical interest. Tropical Animal Health and Production 37, 173186.
Behnke, J. M. ( 1987). Evasion of immunity by nematode parasites causing chronic infections. Advances in Parasitology 26, 171.
Behnke, J. M., Iraqi, F., Menge, D., Baker, R. L., Gibson, J. and Wakelin, D. ( 2003). Chasing the genes that control resistance to gastrointestinal nematodes. Journal of Helminthology 77, 99110.
Behnke, J. M. and Wahid, F. N. ( 1991). Immunological relationships during primary infection with Heligmosomoides polygyrus (Nematospiroides dubius) – H-2 linked genes determine worm survival. Parasitology 103, 157164.
Bhowmik, M., Sasmal, N. and Chakraborty, A. ( 1982). Effect of Raillientina cesticillus infection on the meat and egg production of fowl. Indian Veterinary Medical Journal 6, 100102.
Bilqees, F. M. and Khan, A. ( 1985). Incidence of parasitic infection in fowls of Karachi. Pakistan Journal of Zoology 17, 306308.
Bumstead, N. ( 1996). Breeding for disease resistance. In Poultry Immunology (ed. Davison, T. F., Morris, T. R. and Payne, L. N.), 405415. pp. Carfax Publishing Company, Abingdon, Oxon, UK.
Bundy, D. A. ( 1988). Population ecology of intestinal helminth infections in human communities. Philosophical Transactions of the Royal Society of London, Series B. Biological Sciences 321, 405420.
Caron, L. A., Abplanalp, H. and Taylor, R. L. Jr. ( 1997). Resistance, susceptibility, and immunity to Eimeria tenella in major histocompatibility (B) complex congenic lines. Poultry Science 76, 677682.
Cheema, M. A., Qureshi, M. A. and Havenstein, G. B. ( 2003). A comparison of the immune response of a 2001 commercial broiler with a 1957 randombred broiler strain when fed representative 1957 and 2001 broiler diets. Poultry Science 82, 15191529.
Churchill, G. A. and Doerge, R. W. ( 1994). Empirical threshold values for quantitative trait mapping. Genetics 138, 963971.
Clare, R. A., Strout, R. G., Taylor, R. L. Jr., Collins, W. M. and Briles, W. E. ( 1985). Major histocompatibility (B) complex effects on acquired immunity to cecal coccidiosis. Immunogenetics 22, 593599.
Clare, R. A., Taylor, R. L. Jr., Briles, W. E. and Strout, R. G. ( 1989). Characterization of resistance and immunity to Eimeria tenella among major histocompatibility complex B-F/B-G recombinant hosts. Poultry Science 68, 639645.
Cotter, P. F., Taylor, R. L. Jr. and Abplanalp, H. ( 1998). B-complex associated immunity to Salmonella enteritidis challenge in congenic chickens. Poultry Science 77, 18461851.
Davison, A. C. and Hinkley, D. V. ( 1997). Bootstrap Methods and Their Application. 1st Edn. Cambridge University Press, New York.
Do, H. C., Nguyen, T. K. T. and Pham, S. L. ( 1999). Infestations of chickens with intestinal helminths in the Hanoi city. Khoa Hoc Ky Thuat Thu Y (Veterinary Sciences and Techniques) 6, 6974.
FAOSTAT ( 2005).
Fink, M., Chadfield, M., Christensen, J., Christensen, H. and Bisgaard, M. ( 2005). Investigations on the etiology and epidemiology of amyloid arthropathy in chickens in Denmark. Proceedings of the 14th World Veterinary Poultry Congress, Istanbul, Turkey, p. 228.
Fulton, J. E., Juul-Madsen, H. R., Ashwell, C. M., McCarron, A. M., Arthur, J. A., O'Sullivan, N. P. and Taylor, R. L. Jr. ( 2006). Molecular genotype identification of the Gallus gallus major histocompatibility complex. Immunogenetics 58, 407421.
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.
Giovambattista, G., Ripoli, M. V., Peral-Garcia, P. and Bouzat, J. L. ( 2001). Indigenous domestic breeds as reservoirs of genetic diversity: the Argentinean Creole cattle. Animal Genetics 32, 240247.
GRAPHPAD SOFTWARE ( 2005). GraphPad Prism, 4.03 for Windows. San Diego California, USA.
Hayes, K. S., Bancroft, A. J. and Grencis, R. K. ( 2004). Immune-mediated regulation of chronic intestinal nematode infection. Immunological Reviews 201, 7588.
Hughes, A. L. ( 2002). Natural selection and the diversification of vertebrate immune effectors. Immunological Reviews 190, 161168.
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.
Ikeme, M. M. ( 1971 a). Observations on the pathogenicity and pathology of Ascaridia galli. Parasitology 63, 169179.
Ikeme, M. M. ( 1971 b). Weight changes in chickens placed on different levels of nutrition and varying degrees of repeated dosage with Ascaridia galli eggs. Parasitology 63, 251260.
Ikeme, M. M. ( 1973). The significance of age and previous experience of repeated uptake of infective eggs of Ascaridia galli (Schrank, 1788) (Nematoda, Ascarididae) on the epidemiology of ascaridiosis in the domestic chicken. Acta Parasitologica Polonica 21, 359368.
Irungu, L. W., Kimani, R. N. and Kisia, S. M. ( 2004). Helminth parasites in the intestinal tract of indigenous poultry in parts of Kenya. Journal of the South African Veterinary Association-Tydskrif Van Die Suid-Afrikaanse Veterinere Vereniging 75, 5859.
Jeffery, K. J. and Bangham, C. R. ( 2000). Do infectious diseases drive MHC diversity? Microbes and Infection 2, 13351341.
Juul-Madsen, H. R., Hedemand, J. E., Salomonsen, J. and Simonsen, M. ( 1993). Restriction fragment length polymorphism analysis of the chicken B-F and B-L genes and their association with serologically defined B haplotypes. Animal Genetics 24, 243247.
Khalil, L. F., Jones, A. and Bray, R. A. ( 1994). Key to the Cestode Parasites of Vertebrates. 1st Edn. CAB International, Wallingford, UK.
Lamont, S. J., Bolin, C. and Cheville, N. ( 1987). Genetic resistance to fowl cholera is linked to the major histocompatibility complex. Immunogenetics 25, 284289.
Lillehoj, H. S., Ruff, M. D., Bacon, L. D., Lamont, S. J. and Jeffers, T. K. ( 1989). Genetic control of immunity to Eimeria tenella. Interaction of MHC genes and non-MHC linked genes influences levels of disease susceptibility in chickens. Veterinary Immunology and Immunopathology 20, 135148.
Liu, W., Miller, M. M. and Lamont, S. J. ( 2002). Association of MHC class I and class II gene polymorphisms with vaccine or challenge response to Salmonella enteritidis in young chicks. Immunogenetics 54, 582590.
Luong, V. H. ( 1997). Helminth parasites of poultry in 6 provinces of South Vietnam. Khoa Hoc Ky Thuat Thu Y (Veterinary Sciences and Techniques) 4, 6371.
Magwisha, H. B., Kassuku, A. A., Kyvsgaard, N. C. and Permin, A. ( 2002). A comparison of the prevalence and burdens of helminth infections in growers and adult free-range chickens. Tropical Animal Health and Production 34, 205214.
Martin, S. W., Meek, A. H. and Willeberg, P. ( 1987). Veterinary Epidemiology. 1st Edn. Iowa State University Press, Ames, IA, USA.
McDougald, L. R. ( 2003). Cestodes and trematodes. In Diseases of Poultry (ed. Saif, Y. M., Barnes, H. J., Glisson, J. R., Fadly, A. M., McDougald, L. R. and Swayne, D. E.), pp. 961971. Iowa State University Press. Ames, IA, USA.
Mendelsohn, R. ( 2003). The challenge of conserving indigenous domesticated animals. Ecological Economics 45, 501510.
Miller, M. M., Bacon, L. D., Hala, K., Hunt, H. D., Ewald, S. J., Kaufman, J., Zoorob, R. and Briles, W. E. ( 2004). 2004 Nomenclature for the chicken major histocompatibility (B and Y) complex. Immunogenetics 56, 261279.
Outteridge, P. M., Andersson, L., Douch, P. G., Green, R. S., Gwakisa, P. S., Hohenhaus, M. A. and Mikko, S. ( 1996). The PCR typing of MHC-DRB genes in the sheep using primers for an intronic microsatellite: application to nematode parasite resistance. Immunology and Cell Biology 74, 330336.
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.
Permin, A., Esmann, J. B., Hoj, C. H., Hove, T. and Mukaratirwa, S. ( 2002). Ecto-, endo- and haemoparasites in free-range chickens in the Goromonzi District in Zimbabwe. Preventive Veterinary Medicine 54, 213224.
Permin, A. and Hansen, J. W. ( 1998). Epidemiology, Diagnosis and Control of Poultry Parasites. FAO Animal Health Manual No. 4, Rome, Italy.
Permin, A., Magwisha, H., Kassuku, A. A., Nansen, P., Bisgaard, M., Frandsen, F. and Gibbons, L. ( 1997). A cross-sectional study of helminths in rural scavenging poultry in Tanzania in relation to season and climate. Journal of Helminthology 71, 233240.
Permin, A. and Ranvig, H. ( 2001). Genetic resistance to Ascaridia galli infections in chickens. Veterinary Parasitology 102, 101111.
Plachy, J., Kaiser, P. and Hála, K. ( 2003). Genetics of the immune system. In Poultry Genetics, Breeding and Biotechnology (ed. Muir, W. M. and Aggrey, S. E.), pp. 293309. CABI Publishing, Wallingford, UK.
Plachy, J., Pink, J. R. L. and Hala, K. ( 1992). Biology of the chicken MHC (B-complex). Critical Reviews in Immunology 12, 4779.
Poulsen, J., Permin, A., Hindsbo, O., Yelifari, L., Nansen, P. and Bloch, P. ( 2000). Prevalence and distribution of gastro-intestinal helminths and haemoparasites in young scavenging chickens in upper eastern region of Ghana, West Africa. Preventive Veterinary Medicine 45, 237245.
Qureshi, M. A. and Havenstein, G. B. ( 1994). A comparison of the immune performance of a 1991 commercial broiler with a 1957 randombred strain when fed “typical” 1957 and 1991 broiler diets. Poultry Science 73, 18051812.
Rothschild, M. F., Skow, L. and Lamont, S. J. ( 2000). The major histocompatibility complex. In Breeding for Disease Resistance in Farm Animals (ed. Axford, R. F. E., Bishop, S. C., Nicholas, F. W. and Owen, J. B.), pp. 73105. CABI Publishing, Wallingford, UK.
Ruff, M. D. ( 1999). Important parasites in poultry production systems. Veterinary Parasitology 84, 337347.
Ruff, M. D. and Norton, R. A. ( 2003). Nematodes and acanthocephalans. In Diseases of Poultry (ed. Saif, Y. M., Barnes, H. J., Glisson, J. R., Fadly, A. M., McDougald, L. R. and Swayne, D. E.), pp. 931961. Iowa State University Press, Ames, IA, USA.
Schou, T., Permin, A., Roepstorff, A., Sorensen, P. and Kjaer, J. ( 2003). Comparative genetic resistance to Ascaridia galli infections of 4 different commercial layer-lines. British Poultry Science 44, 182185.
Soulsby, E. J. L. ( 1982). Helminths, Arthropods and Protozoa of Domesticated Animals. 7th Edn. Baillière Tindall, East Sussex.
Ssenyonga, G. S. Z. ( 1982). Prevalence of helminth-parasites of domestic fowl (Gallus domesticus) in Uganda. Tropical Animal Health and Production 14, 201204.
Stear, M. J., Hetzel, D. J., Brown, S. C., Gershwin, L. J., Mackinnon, M. J. and Nicholas, F. W. ( 1990). The relationships among ecto- and endoparasite levels, class I antigens of the bovine major histocompatibility system, immunoglobulin E levels and weight gain. Veterinary Parasitology 34, 303321.
Stear, M. J., Park, M. and Bishop, S. C. ( 1996). The key components of resistance to Ostertagia circumcincta in lambs. Parasitology Today 12, 438441.
Tongson, M. S. and McCraw, B. M. ( 1967). Experimental ascaridiasis: influence of chicken age and infective egg dose on structure of Ascaridia galli populations. Experimental Parasitology 21, 160172.
Tran, D. T. ( 2002). Village poultry production in Vietnam. E-Conference, International Network for Family Poultry Development: The Bangladesh Model and Other Experiences in Family Poultry Development.
Turner, J. D., Faulkner, H., Kamgno, J., Cormont, F., Van, S. J., Else, K. J., Grencis, R. K., Behnke, J. M., Boussinesq, M. and Bradley, J. E. ( 2003). Th2 cytokines are associated with reduced worm burdens in a human intestinal helminth infection. Journal of Infectious Diseases 188, 17681775.
Wassom, D. L., David, C. S. and Gleich, G. J. ( 1979). Genes within the Major Histocompatibility Complex influence susceptibility to Trichinella spiralis in the mouse. Immunogenetics 9, 491496.
Wassom, D. L. and Kelly, E. A. B. ( 1990). The role of the major histocompatibility complex in resistance to parasite infections. Critical Reviews in Immunology 10, 3152.
Wegner, K. M., Kalbe, M., Schaschl, H. and Reusch, T. B. ( 2004). Parasites and individual major histocompatibility complex diversity – an optimal choice? Microbes and Infection 6, 11101116.
Woolhouse, M. E. J. ( 1998). Patterns in parasite epidemiology: the peak shift. Parasitology Today 14, 428434.
Yadav, A. K. and Tandon, V. ( 1991). Helminth parasitism of domestic fowl (Gallus domesticus L.) in a subtropical high-rainfall area of India. Beiträge zur tropischen Landwirtschaft und Veterinärmedizin 29, 97104.
Yoo, B. H. and Sheldon, B. L. ( 1992). Association of the major histocompatibility complex with avian-leukosis virus-infection in chickens. British Poultry Science 33, 613620.
Zoorob, R., Auffray, C. and Chaussé, A. M. ( 1998). Réactifs et méthodes pour la détection des gènes liés au CMH d'oiseaux d'élevage tels que le poulet. Patent Number: PCT/FR98/02501, France.



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