Skip to main content
Log in

The jejunal cellular responses in chickens infected with a single dose of Ascaridia galli eggs

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

This histopathological study was carried out in order to investigate the cellular response in the jejunum to Ascaridia galli during the first 7 weeks of infection. Fourty-two ISA Brown chickens (7 weeks old) were infected orally with 500 embryonated A. galli eggs each while 28 chickens were left as uninfected controls. Six infected and four control chickens were necropsied at each time point 3, 7, 10, 14, 21, 28 and 42 days post-infection (dpi). Samples for histopathology were taken from three sites of the jejunoileum. Significantly higher eosinophil counts were seen in infected chickens compared to uninfected at 3, 7, 10, 14 and 28 dpi (P < 0.01). In both groups, the initial number of mast cells was high, but this high level of mast cells remained for a longer period in the infected group compared to the control group. Significantly higher counts were thus found in the infected group at 21 (P < 0.001), 28 (P < 0.01) and 42 dpi (P < 0.05). A. galli infection induced changes in the mucosal thickness as reduced villi length at 7, 10, 14, 21 and 28 dpi and in the degree of general cellular infiltration in the lamina propria of the mucosal layer. No adult worms were seen during the experiment; therefore, A. galli larvae have elicited a moderate cellular response in the lamina propria, mainly consisting of eosinophils in the early phase and later of mast cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Ackert JE (1923) On the habitat of Ascaridia perspicillum (Rud.). J Parasitol 10:101–103

    Article  Google Scholar 

  • Ackert JE (1931) The morphology and life history of the fowl nematode Ascaridia lineate (Schneider). Parasitol 23:360–379

    Article  Google Scholar 

  • Ackert JE, Herrick CA (1928) Effects of the nematode Ascaridia lineata (Schneider) on growing chickens. J Parasitol 15:1–13

    Article  Google Scholar 

  • Ackert J, Porter D, Beach T (1935) Age resistance of chickens to the nematode Ascaridia lineate (Schneider). J Parasitol 21:205–213

    Article  Google Scholar 

  • Andreasen CB, Latimer KS (1990) Cytochemical staining characteristics of chicken heterophils and eosinophils. Vet Clin Pathol 19:51–54

    Article  PubMed  Google Scholar 

  • Araujo P, Bressan C (1976) Observations on the second moult of the larvae of Ascaridia galli (author’s transl)]. Ann Parasitol Hum Comp 52:531–537

    Google Scholar 

  • Araujo P, Bressan CR (1977) Observations on the second moult of the larvae of Ascaridia galli. Annales de Parasitologie Humaine et Comparee 52:531–537

  • Bancroft JD, Stevens A (1996) Theory and practice of histological techniques, 4th edn. Churchill Livingstone, New York, p 776

    Google Scholar 

  • Dänicke S, Moors E, Beineke A, Gauly M (2009) Ascaridia galli infection of pullets and intestinal viscosity: consequences for nutrient retention and gut morphology. Br Poult Sci 50:512–520

    Article  PubMed  Google Scholar 

  • Darmawi BU, Hambal PBP (2013) Mucosal mast cells response in the jejunum of Ascaridia galli-infected laying hens. Media-Peternakan J Animal Sci Tech 36(2):113–119

    Article  Google Scholar 

  • Degen WG, Nv D, Rothwell L, Kaiser P, Schijns VE (2005) Th1/Th2 polarization by viral and helminth infection in birds. Vet Microbiol 105:163–167

    Article  CAS  PubMed  Google Scholar 

  • Ferdushy T, Nejsum P, Roepstorff A, Thamsborg SM, Kyvsgaard NC (2012) Ascaridia galli in chickens: intestinal localization and comparison of methods to isolate the larvae within the first week of infection. Parasitol Res 111:2273–2279

    Article  PubMed  Google Scholar 

  • Ferdushy T, Luna-Olivares LA, Nejsum P, Roepstorff A, Thamsborg SM, Kyvsgaard NC (2013) Population dynamics of Ascaridia galli following single infection in young chickens. Parasitol 140:1078–1084

    Article  Google Scholar 

  • Galli SJ, Maurer M, Lantz CS (1999) Mast cells as sentinels of innate immunity. Curr Opin Immunol 11:53–59

    Article  CAS  PubMed  Google Scholar 

  • Hansen M, Terhaar C, Turner D (1956) Importance of the egg shell of Ascaridia galli to the infectivity of its larva. J Parasitol 42:122–125

    Article  CAS  PubMed  Google Scholar 

  • Herd RP, McNaught DJ (1975) Arrested development and the histotrophic phase of Ascaridia galli in the chicken. Int J Parasitol 5:401–406

    Article  CAS  PubMed  Google Scholar 

  • Höglund J, Jansson DS (2011) Infection dynamics of Ascaridia galli in non-caged laying hens. Vet Parasitol 180:267–273

    Article  PubMed  Google Scholar 

  • Ikeme M (1971) Observations on the pathogenicity and pathology of Ascaridia galli. Parasitol 63:169–179

    Article  CAS  Google Scholar 

  • Ishikawa N, Horii Y, Nawa Y (1993) Immune-mediated alteration of the terminal sugars of goblet cell mucins in the small intestine of Nippostrongylus brasiliensis-infected rats. Immunol 78:303

    CAS  Google Scholar 

  • Jeurissen S, Janse E, Vermeulen A, Vervelde L (1996) Eimeria tenella infections in chickens: aspects of host-parasite: interaction. Vet Immunol Immunopathol 54:231–238

    Article  CAS  PubMed  Google Scholar 

  • Jeurissen S, Wagenaar F, Janse EM (1999) Further characterization of M cells in gut-associated lymphoid tissues of the chicken. Poult Sci 78:965–972

    Article  CAS  PubMed  Google Scholar 

  • Kaiser P (2007) The avian immune genome a glass half-full or half-empty. Cyt Gen Res 117:221–230

    Article  CAS  Google Scholar 

  • Karaca T, Yörük M, Uslu S (2006) Age‐related changes in the number of mast cells in the avian lymphoid organs. Anat Histol Embryol 35(6):375–379

    Article  CAS  PubMed  Google Scholar 

  • Löscher T, Saathoff E (2008) Eosinophilia during intestinal infection. Best Prac Res Clin Gastr 22:511–536

    Article  Google Scholar 

  • Luna LG (1968) Manual of histological staining methods of the Armed Forces Institute of Pathology, 3rd edn. McGraw-Hill Book Company, New York, p 251

    Google Scholar 

  • Luna-Olivares LA, Ferdushy T, Kyvsgaard NC, Nejsum P, Thamsborg SM, Roepstorff A, Iburg TM (2012) Localization of Ascaridia galli larvae in the jejunum of chickens 3 days post infection. Vet Parasitol 185:186–193

    Article  PubMed  Google Scholar 

  • Marcos-Atxutegi C, Gandolfi B, Arangüena T, Sepulveda R, Arévalo M, Simon F (2009) Antibody and inflammatory responses in laying hens with experimental primary infections of Ascaridia galli. Vet Parasitol 161:69–75

    Article  CAS  PubMed  Google Scholar 

  • Miquel N (2005) Immune responses in experimental Ascaris suum single infections in pigs. Ph.D. Thesis. The Royal Veterinary and Agricultural University. Copenhagen. Denmark

  • Pearse AGE (1985) Histochemistry. Theorical and applied. Analytical Technology. 4th ed. vol 2

  • Permin A, Bisgaard M, Frandsen F, Pearman M, Kold J, Nansen P (1999) Prevalence of gastrointestinal helminths in different poultry production systems. Br Poult Sci 40:439–443

    Article  CAS  PubMed  Google Scholar 

  • Ramadan HH, Aboud znada NY (1992) Morphology and life history of Ascaridia galli in the domestic fowl that are raised in Jeddah. J KAU Sci 4:87–89

    Google Scholar 

  • Reid WM, Carmon JL (1958) Effects of numbers of Ascaridia galli in depressing weight gains in chicks. J Parasitol 44:183–186

    Article  CAS  PubMed  Google Scholar 

  • Schrank P Von F (1788) Verzeichniss der bisher hinlänglich bekannten Eingeweidewürmer, nebs einer Abhandlung über ihre Anverwandschaften. München, pp 116

  • Schummer A, Vollmerhaus B, Sinowatz F, Frewein J Waibl H (1992) Anatomie der Vögel. In Nickel, R., Schummer, A., Seiferle, E. (2.ed) Lehrbuch der Anatomie der Haustiere. Paul Parey, Berlin and Hamburg, Germany pp 203-204

  • Schwarz A, Gauly M, Abel H, Daş G, Humburg J, Rohn K, Breves G, Rautenschlein S (2011) Immunopathogenesis of Ascaridia galli infection in layer chicken. Dev Comparativ Immunol 35:774–784

    Article  CAS  Google Scholar 

  • Soulsby EJL (1982) Helminths, arthropods and protozoa of domesticated animals, 7th ed. Balliere Tindall. The English Language Book Society, London

  • Stenfeldt A, Wennerås C (2004) Danger signals derived from stressed and necrotic epithelial cells activate human eosinophils. Immunol 112:605–614

    Article  CAS  Google Scholar 

  • Tugwell RL, Ackert JE (1952) On the tissue phase of the life cycle of the fowl nematode Ascaridia galli (Schrank). J Parasitol 38:277–288

    Article  CAS  PubMed  Google Scholar 

  • Uribe C (1922) Observations on the development of Heterakis papillosa Bloch in the chicken. J Parasitol 8:167–176

    Article  Google Scholar 

  • Wells PD (1963) Mucin-secreting cells in rats infected with Nippostrongylus brasiliensis. Exp Parasitol 14:15–22

    Article  CAS  PubMed  Google Scholar 

  • Xu L, Carr M, Bland A, Hall G (1993) Histochemistry and morphology of porcine mast cells. Histochem J 25:516–522

    Article  CAS  PubMed  Google Scholar 

  • Yong L (1997) The mast cell: origin, morphology, distribution, and function. Exp Tox Path 49:409–424

    Article  CAS  Google Scholar 

Download references

Acknowledgements

DANIDA is thanked for financial support through grant DFC 09-054 LIFE. Thanks are given for the technical assistance from the Section of Pathology (Hanne Hornemann Møller, Betina Andersen and Lisbeth Kiørboe) and the Danish Centre for Experimental Parasitology (Lise-Lotte Christiansen), University of Copenhagen.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Luz Adilia Luna-Olivares.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Luna-Olivares, L.A., Kyvsgaard, N.C., Ferdushy, T. et al. The jejunal cellular responses in chickens infected with a single dose of Ascaridia galli eggs. Parasitol Res 114, 2507–2515 (2015). https://doi.org/10.1007/s00436-015-4450-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-015-4450-y

Keywords

Navigation