Skip to main content
Log in

Hematological and immunological properties of herring gull (Larus argentatus) nestlings experimentally infected with Diphyllobothrium dendriticum (Cestoda: Pseudophyllidae)

  • Zoology
  • Published:
Biology Bulletin Aims and scope Submit manuscript

Abstract

The morphological structure of the blood in herring gull nestlings and their immune system response to experimental infection with tapeworm Diphyllobothrium dendriticum have been studied. The leukocyte reaction pattern and the dynamics of immunoglobulin synthesis and populations of immunocompetent cells in the blood of nestlings during early invasion indicated a short duration of the cellular immune response and an insignificant humoral response. A pronounced trend to decrease in the hemoglobin level in the blood of infected nestlings has been revealed and this reduction was in part compensated by intensified erythropoiesis. It is shown, that the changes in hematologic and immune responses of the obligate definitive host provide for the mutual host-parasite adaptation.

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.

Similar content being viewed by others

References

  • Arinkin, A.V., Effect of Mixed Invasions on Immune and Biological Reactivity in Chicken, Veterinariya, 1996, no. 3, pp. 38–41.

  • Astaf’ev, B.A., Immunopatologicheskie proyavleniya i oslozhneniya gel’mintozov (Immunopathological Manifestations and Complications of Helminthiases), Moscow: Poligrafist, 1987.

    Google Scholar 

  • Barriga, O., Immunomodulation by Nematodes: A Review, Vet. Parasitol., 1984, vol. 14, no. 314, pp. 293–320.

    Google Scholar 

  • Belov, A.P., Fais, D., and Leutskaya, Z.K., Chicken Serum Immunoglobulins: Fractionation and Identification, in Immunologicheskie i biokhimicheskie aspekty vzaimootnoshenii gel’minta i khozyaina: Tr. Gel’mintol. lab. AN SSSR. T. XXXVI (Immunological and Biochemical Aspects of the Host-Helminth Interaction), Moscow: Nauka, 1988, pp. 47–55.

    Google Scholar 

  • Berezantsev, Yu.A., Gavrilova, E.P., and Oparin, E.N., Inhibition of Phagocytic and Chemotactic Activities of Leukocytes by Larvae of Certain Cestode and Nematode Species, Zh. Evol. Biokhim. Fiziol., 1976, vol. 12, no. 3, pp. 240–244.

    Google Scholar 

  • Berezhko, V.K., Immune Reactivity, Immune Diagnosis, and Immune Prevention in Animal Helminthiases (Theoretical Bases and Experimental Study), Extended Abstract of Doctoral (Biol.) Dissertation, Moscow: VIGIS, 1994.

    Google Scholar 

  • Blagov, N.A., Baryshev, M.D., and Firsov, V.N., Certain Indices of Cell Immunity in Patients Infected with Intestinal Nematodes, Med. Parazitologiya i Parazitar. Bolezni, 1987, no. 5, pp. 85–86.

  • Bolotnikov, I.A. and Konopatov, Yu.V., Prakticheskaya immunologiya sel’skokhozyaistvennoi ptitsy (Practical Immunology of Agricultural Birds), St. Petersburg: Nauka, 1993.

    Google Scholar 

  • Boroskova, Z., Benkova, M., and Alexander, R., Zmeny Poctu T-a B-Lymfocytov v Krvi Parasiat po Experimentalney Ascaridoze, Vet. Med, 1982, vol. 27, pp. 741–746.

    CAS  Google Scholar 

  • Buzmakova, R.A., The Role of Tissue Eosinophilia in the State of the Host-Parasite System, Agrarnaya Nauka, 1999, no. 11, pp. 11–12.

  • Chebyshev, N.V., Bogoyavlenskii, Yu.K., and Grishina, E.A., Gel’mintozy: organno-sistemnye protsessy v ikh patogeneze i lechenii (Helminthiases: Organic and Systemic Processes and Treatment), Moscow: Meditsina, 1998.

    Google Scholar 

  • Daugalieva, E.Kh. and Filippov, V.V., Immunnyi status i puti ego korrektsii pri gel’mintozakh sel’skokhozyaistvennykh zhivotnykh (Immune Status and Its Correction in Helminthiases of Agricultural Animals), Moscow: Agropromizdat, 1991.

    Google Scholar 

  • Delyamure, S.L., Skryabin, A.S., and Serdyukov, A.M., Diphyllobothriids—Tapeworm Parasites of Humans, Mammals, and Birds, in Osnovy tsestodologii T. XI (General Cestodology. Vol. XI), Moscow: Nauka, 1985.

    Google Scholar 

  • Dissanaeake, S., Khan, N., Shahin, A., et al., Induction of Immunoglobulin G1, Interleukin-6 and Interleukin-10 by Taenia crassiceps Metacestode Carbohydrates, Immunol., 2002, vol. 107, no. 4, pp. 411–420.

    Article  Google Scholar 

  • Dubovskaya, A.Ya., Study of Proteolytic Activity in Some Cestode Species, Parazitol., 1973, vol. 7, no. 2, pp. 154–159.

    CAS  Google Scholar 

  • Galaktionov, V.G., Immunologiya (Immunology), Moscow: Akademiya, 2004.

    Google Scholar 

  • Gerasimova, A.V., Blagov, N.A., Rzhenitsin, V.V., et al., The Role of Goals in Diphyllobothriasis Distribution, in Mater. nauch. konf. Vsesoyuz. o-va gel’mintologov. Ch. 2. (Proc. Sci. Conf. of the Russian Helminthogical Society. Part 2), Moscow, 1969, pp. 189–187.

  • Gosteva, L.A., Sergeeva, V.T., and Makarevich, N.I., Lysozyme Activity in Diphyllobothriasis Patients, Med. Parazitologiya I Parazitar. Bolezni, 1991, no. 2, pp. 11–13.

  • Izvekova, G.I., Feeding Adaptations in Lower Cestodes Parasitic in Fishes, in Parazitologicheskie issledovaniya v Sibiri i na Dal’nem Vostoke: Mater. II Mezhregion. nauch. konf. parazitologov Sibiri i Dal’nego Vostoka, Novosibirsk, 15–20 sentyabrya 2005 g. (Parasitological Studies in Siberia and Far East: Proc. II Int. Sci. Conf. Parasitology in Siberia and Far East. Novosibirsk, September 15–20, 2005), 2005, pp. 78–80.

  • Karmanska, K. and Milchalska, Z., The Role T-Lymphocytes in the Course of Experimental Trichinellosis in Mice, Wiad. Parasitol., 1981, vol. 27, no. 3, pp. 499–508.

    CAS  Google Scholar 

  • Lebedev, K.A. and Ponyakina, I.D., Immunnaya nedostatochnost’ (vyyavlenie i lechenie) (Immune Deficiency (Detection and Treatment)), Moscow: Med. Kniga, 2003.

    Google Scholar 

  • Maiboroda, A.A., Timoshenko, T.M., Kozakova, A.A., et al., The Structure of a Natural Diphyllobothriasis Focus in the Region of the Maloe More Bay in Lake Baikal, in Respubl. sb. nauch. tr. “Gel’mintozy cheloveka” (Republican Collected Papers on Human Helminthiases), Leningrad: NII epidemiol. i mikrobiol. im. Pastera, 1987, pp. 56–62.

    Google Scholar 

  • Mityushnikov, V.M., Estestvennaya rezistentnost’ sel’skokhozyaistvennoi ptitsy (Natural Resistance of Agricultural Birds), Moscow: Rossel’khozizdat, 1985.

    Google Scholar 

  • Nikitin, V.N., Gematologicheskmi atlas sel’skokhozyaistvennykh i laboratornykh zhivotnykh (Helminthological Atlas of Agricultural and Laboratory Animals), Moscow: Sel’khozgiz, 1956.

    Google Scholar 

  • Perevozchikova, N.G. and Ivanova, O.V., Hepatic Cysticercosis as a Model of Self-Governing Parasite System, in Aktual’nye problemy infektologii i parazitologii. Mater. 1-i Mezhdunar. yubil. Konf. Tomsk, 2–5 aprelya 2001 g. (Urgent Problems in Infectology and Parasitology. Proc. 1st Int. Anniv. Conf. Tomsk, April 2–5, 2001), 2001, p. 32.

  • Plotnikov, N.N., The Clinical Picture, Pathogenesis, and Therapy of Diphyllobothriasis-Induced Anemia, Klin. Meditsina, 1955, no. 7, pp. 38–43.

  • Pronin, N.M., Parasites of Fishes and Other Aquatic Animals in the Baikal Region Dangerous for Humans, in Problemy obshchei i regional’noi parazitologii (Problems of General and Regional Parasitology), Ulan-Ude: Izd-vo Buryat. s.-kh. akademii, 2000, pp. 134–140.

    Google Scholar 

  • Pronin, N.M. and Pronina, S.V., The Dynamics of Salmonid Infection with Diphyllobothrium dendriticum Plerocercoids, in Dinamika zarazhennosti zhivotnykh gel’mintami (Dynamics of Animal Infection by Helminths), Ulan-Ude: Buryat. nauch. tsentr. SO AN SSSR, 1991, pp. 60–75.

    Google Scholar 

  • Pronin, N.M., Pronina, S.V., and Sanzhieva, S.D., Rate of Fish Infection with Gull-Tapeworm Plerocercoids in the Baikal Basin, Med. Parazitol. i Parazitar. Bolezni, 1988, no. 4, pp. 64–67.

  • Pronin, N.M., Pronina, S.V., and Timoshenko, T.M., Golden Hamsters as a Model Parasite System, in Tez. dokl. XII Vsesoyuz. konf. po prirodnoi ochagovosti boleznei (Proc. XII All-Russian Conf. on Natural Infection Nidi), Novosibirsk, 1989a.

  • Pronin, N.M., Timoshenko, T.M., and Sanzhieva, S.D., The Dynamics of Egg Production and Fecundity of Cestode Diphyllobothrium dendriticum (Nitsch, 1824) (Cestoda, Pseudophyllidae), Parazitologiya, 1989b, vol. 23, no. 2, pp. 146–151.

    CAS  Google Scholar 

  • Pronina, S.V. and Pronin, N.M., Vzaimootnosheniya v sistemakh gel’minty-ryby (Interactions in the Helminth-Fish Systems), Moscow: Nauka, 1988.

    Google Scholar 

  • Pronina, S.V. and Timoshenko, T.M., Effect of Gull-Tapeworm Diphyllobothrium dendriticum (Nitsch, 1824) on the Micromorphological Picture of Digestive Organs in Golden Hamster, Sib. Ekol. Zh., 1991, no. 2, pp. 47–52.

  • Pronina, S.V., Davydov, V.G., and Kuperman, B.I., A Histological Study of Some Caryophyllid, Pseudophyllid, and Proteocephallid Cestodes, in Gidrobiologiya i gidroparazitologiya Pribaikal’ya i Zabaikal’ya (Hydrobiology and Hydroparasitology in the Baikal region and Transbaikalia), Novosibirsk: Nauka. Sib. otd-nie, 1985, pp. 153–167.

    Google Scholar 

  • Rodrigues-Sosa, M., Satoskar, A.R., Calderon, R., et al., Chronic Helminth Infection Induces Alternatively Activated Macrophages Expressing High Levels of CCR5 with Low Interleukin-12 Production and Th2-Biasing Ability, Infect Immunol., 2002, vol. 70, no. 7, pp. 3656–3664.

    Article  Google Scholar 

  • Rodrigues-Sosa, M., Satoskar, A.R., David, J.R., and Terrazas, L.I., Altered T-Helper Responses in CD40 and Interleukin-12 Deficient Mice Reveal a Critical Role for Th1 Responses in Eliminating the Helminthes Parasite Taenia Crassiceps, Int. J. Parasitol., 2003, vol. 33, no. 7, pp. 703–711.

    Article  Google Scholar 

  • Sergeeva, E.G. and Beer, S.A., Factors of the Parasite-Host Specificity, in Aktual’nye problemy obshchei parazitologii: Tr. In-ta parazitologii. T. XLII (Urgent Problems of General Parasitology. Proc. Inst. Parasitol. Vol. XLII), Moscow: Nauka, 2000.

    Google Scholar 

  • Sergeeva, E.G. and Petrosyan, R.A., Induction of the Host Immune Responses to Different Parasite Types, in Teoreticheskie i prikladnye problemy parazitologii: Tr. In-ta parazitologii. T. XLIII (Theoretical and Applied Problems of Parasitology. Proc. Inst. Parasitol. Vol. XLIII), Moscow: Nauka, 2002, pp. 200–205.

    Google Scholar 

  • Shchul’ts, R.S. and Gvozdev, E.V., Pathology and Immunology in Helminthiases, in Osnovy obshchei gel’mintologii. T 3 (Basis of General Helminthology. Vol. 3), Moscow: Nauka, 1976.

    Google Scholar 

  • Shlyakhov, E.N. and Andriesh, L.P., Immunologiya (Immunology), Chisinau: Shtiintsa, 1985.

    Google Scholar 

  • Smirnov, L.P., The Role of Lipids and Proteins in the Development of Biochemical Adaptations in Ectotherms, Extended Abstract of Doctoral (Biol.) Dissertation, Petrozavodsk: RIO KNTs, 2005.

    Google Scholar 

  • Smyth, J.D., Introduction to Animal Parasitology, London: Univ. Press, 1962.

    Google Scholar 

  • Totolyan, A.A. and Freidlin, I.S., Kletki immunnoi sistemy (Cells of the Immune System), St. Petersburg: Nauka, 2000.

    Google Scholar 

  • Vuylsteke, P., Bertrand, C., Verhoef, G.E., and Vandenberghe, P., Case of Megaloblastic Anemia Caused by Intestinal Taeniasis, Ann. Hematol., 2004, vol. 83, no. 7, pp. 487–488.

    Article  PubMed  Google Scholar 

  • Vysotskaya, R.U., Krupnova, M.Yu., Kuklina, M.M., et al., Effect of Helminth Infection on Lysozyme Activity in Tissues of Gull Larus marinus L.), in Parazitologicheskie issledovaniya v Sibiri i na Dal’nem Vostoke: Mater. II Mezhregion. nauch. konf. parazitologov Sibiri i Dal’nego Vostoka. Novosibirsk, 15–20 sentyabrya 2005 g. (Parasitological Studies in Siberia and Far East. Proc. II Int. Conf. of Parasitologists in Siberia and Far East. Novosibirsk, September 15–20, 2005), 2005 pp. 36–37.

  • Yoshimura, Y., Significance of Local Immunity in Hen Reproductive Organs, Animal Sci. J., 2004, vol. 75, no. 3, p. 183.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Original Russian Text © O.E. Mazur, N.M. Pronin, L.V. Tolochko, 2007, published in Izvestiya Akademii Nauk, Seriya Biologicheskaya, 2007, No. 4, pp. 420–427.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mazur, O.E., Pronin, N.M. & Tolochko, L.V. Hematological and immunological properties of herring gull (Larus argentatus) nestlings experimentally infected with Diphyllobothrium dendriticum (Cestoda: Pseudophyllidae). Biol Bull Russ Acad Sci 34, 346–352 (2007). https://doi.org/10.1134/S1062359007040061

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1062359007040061

Keywords

Navigation