Effect of trypanosomiasis on hematologic characteristics of bream (Abramis brama)


  • T. B. Lapirova I. D. Papanin Institute for Biology of Inland Waters RAS http://orcid.org/0000-0001-7477-4795
  • E. A. Zabotkina I. D. Papanin Institute for Biology of Inland Waters RAS
Keywords: Trypanosoma sp.; common bream; blood cells; hemoglobin; total protein; glucose; circulating immune complexes.

Abstract

Trypanosomes are flagellated protozoa; they parasitize in the blood of a wide range of vertebrates and invertebrates, including fish, for which leeches are carriers. The metabolites released by trypanosomes are toxic to the host, cause disruption of homeostasis, which leads to illness and even death. Parasites in fish living in hot climates are the most common and better studied. Trypanosomes were first detected in common bream (Abramis brama L.) from the Uglich Reservoir (Upper Volga) in August 2015. The aim of this work is to study the effect of these parasites on the hematological parameters of the fish. As a control, blood indices of uninfected fish were used. The condition factor of infected fish did not differ from that of healthy fish. There were no significant differences between the two groups of fish in contents of total serum protein and glycemia. This may indicate a low level of bream parasitemia. At the same time, a significant increase in the leukocyte abundance index was detected, which indirectly indicates an increase in the number of these cells in the infected fish compared with the control ones, statistically significant differences were found in the leukogram: the proportion of eosinophils in the diseased fish increased almost 6 times while the relative number of lymphocytes decreased. The pattern of red blood also changed: the proportion of immature erythrocytes increased in the infected fish; a small number of microcytes and amitoses of erythrocytes and differences in the cytometric characteristics of red blood cells were found. The level of hemoglobin significantly decreased. A sharp increase in the content of circulating immune complexes indicates a shift in antigenic homeostasis caused by the presence of parasites. A similarity in the reaction of a number of indicators of the blood system of bream with trypanosomiasis to that of animals of higher systematic groups was revealed. The interpretation of the results obtained during the study of the effect of parasites on the host organism requires consideration of its physiological status and habitat conditions, the stage of the disease and the mechanism of adaptation of the parasite to the host defense system.

References

Bienek, D. R., & Belosevic, M. (1999). Macrophage or fibroblast-conditioned medium potentiates growth of Trypanosoma danilewskyi Laveran & Mesnil 1904. Journal of fish diseases, 22(5), 359–367.


Bienek, D. R., Plouffe, D. A., Wiegertjes, G. F., & Belosevic, M. (2002). Immunization of goldfish with excretory/secretory molecules of Trypanosoma danilewskyi confers protection against infection. Developmental and Comparative Immunology, 26(7), 649–657.


Brand, T. von (1973). Biochemistry of parasites. Academic Press, New York.


Clauss, T. M., Dove, A. D. M., & Arnold, J. E. (2008). Hematologic disorders of fish. Veterinary Clinics: Exotic Animal Practice, 11, 445–462.


Correa, L. L., Oliveira, M. S. B., Tavares-Dias, M., & Ceccarelli, P. S. (2016). Infections of Hypostomus spp. by Trypanosoma spp. and leeches: A study of hematology and record of these hirudineans as potential vectors of these hemoflagellates. Brazilian Journal of Veterinary Parasitology, 25(3), 299–305.


Debol'skij, V. K., Grigor'eva, I. L., & Komissarov, A. B. (2010). Sovremennaja gidrohimicheskaja harakteristika reki Volga i ee vodohranilisch [Modern hydrochemical characteristics of the Volga River and its reservoirs]. Voda: Himija i Ekologija, 11, 2–12 (in Russian).


Dyková, I., & Lom, J. (1979). Histopathological changes in Trypanosoma danilewskyi Laveran & Mesnil, 1904 and Trypanoplasma borelli Laveran & Mesnil, 1902 infections of goldfish, Carassius auratus (L.). Journal of Fish Diseases, 2(5), 381–390.


Ehdel'shtejn, K. K. (1998). Vodohranilishcha Rossii: Ekologicheskie problemy, puti ih resheniya [Reservoirs of Russia: Environmental problems, ways to solve them]. GEOS, Moscow (in Russian).


Evans, D. L., & Gratzek, J. B. (1989). Immune defense mechanisms in fish to protozoan and helminth infections. Integrative and Comparative Biology, 29(2), 409–418.


Fermino, B. R., Paiva, F., Soares, P., Tavares, L. E. R., Viola, L. B., Ferreira, R. C., Botero-Arias, R., De-Paula, C. D., Campaner, M., Takata, C. S. A., Teixeira, M. M. G., & Camargo, E. P. (2015). Field and experimental evidence of a new caiman trypanosome species closely phylogenetically related to fish trypanosomes and transmitted by leeches. International Journal for Parasitology: Parasites and Wildlife, 4(3), 368–378.


Ferreira, M. L., & Avenant-Oldewage, A. (2013). Notes on the occurrence of Trypanosoma sp. (Kinetoplastida: Trypanosomatidae) in freshwater fishes from South Africa. Onderstepoort Journal of Veterinary Research, 80(1), 529.


Fink, I. R., Ribeiro, C. M. S., Forlenza, M., Taverne-Thiele, A., Rombout, J. H. W. M., Savelkoul, H. F. J., & Wiegertjes, G. F. (2015). Immune-relevant thrombocytes of common carp undergo parasite-induced nitric oxide-mediated apoptosis. Developmental and Comparative Immunology, 50(2), 146–154.


Forlenza, M., Scharsack, J. P., Kachamakova, N. M., Taverne-Thiele, A. J., Rombout, J. H. W. M., & Wiegertjes, G. F. (2008). Differential contribution of neutrophilic granulocytes and macrophages to nitrosative stress in a host – parasite animal model. Molecular Immunology, 45, 3178–3189.


Fudjimoto, R. Y., Neves, M. S., Santos, R. F. B., Souza, N. C., Do Couto, M. V. S., Lopes, J. N. S., Diniz, D. G., & Eiras, J. C. (2013). Morphological and hematological studies of Trypanosoma spp. infecting ornamental armored catfish from Guamá River-Pa, Brazil. Anais da Academia Brasileira de Ciências, 85(3), 1149–1156.


Goodwin, L. G. (1985). Trypanosomiasis: Introduction. British Medical Bulletin, 41(2), 103–104.


Grybchuk-Ieremenko, A., Losev, A., Kostygov, A. Y., Lukeš, J., & Yurchenko, V. (2014). High prevalence of trypanosome co-infections in freshwater fishes. Folia Parasitologica, 61(6), 495–504.


Gupta, N., & Gupta, D. K. (1987). Dimorphism in Trypanoplasma (Cryptobia) maguri n. sp.: Effect on blood glucose level of host. Revista Iberica de Parasitologia, 47(4), 317–324.


Gupta, N., & Gupta, D. K. (2012). Erythropenia in piscine trypanosomiasis. Trends in Parasitology, 1, 1–6.


Haag, J., O'h Uigin, C., & Overath, P. (1998). The molecular phylogeny of trypanosomes: Evidence for an early divergence of the Salivaria. Molecular and Biochemical Parasitology, 91(1), 37–49.


Hamnueva, T. R. (2001). Raznoobrazie i ekologija kinetoplastid (Kinetoplastida: Kinetoplastidea) – parazitov ryb ozera Bajkal [Diversity and ecology of Kinetoplastidae (Kinetoplastida: Kinetoplastidea) – parasites of fish of Lake Baikal]. Ulan-Ude (in Russian).


Hayes, P. M., Lawton, S. P., Smit, N. J., Gibson, W. C., & Davies, A. J. (2014). Morphological and molecular characterization of a marine fish trypanosome from South Africa, including its development in a leech vector. Parasites and Vectors, 7, 50.


Islam, A. K. M. N., & Woo, P. T. K. (1991a). Anemia and its mechanism in goldfish Carassius auratus infected with Trypanosoma danilewskyi. Diseases of Aquatic Organisms, 8, 37–43.


Islam, A. K. M. N., & Woo, P. T. K. (1991b). Anorexia in goldfish Carassius auratus infected with Trypanosoma danilewsky. Diseases of Aquatic Organisms, 11, 45–48.


Jesus, R. B., Gallani, S. U., Valladão, G. M. R., Pala, G., Silva, T. F. A., Costa, J. C., Kotzent, S., & Pilarski, F. (2018). Trypanosomiasis causing mortality outbreak in Nile tilapia intensive farming: Identification and pathological evaluation. Aquaculture, in press.


Joerink, M., Groeneveld, A., Ducro, B., Savelkoul, H. F. J., & Wiegertjes, G. F. (2007). Mixed infection with Trypanoplasma borreli and Trypanosoma carassii induces protection: Involvement of cross-reactive antibodies. Developmental and Comparative Immunology, 31(9), 903–915.


Khan, R. A. (1977). Blood changes in atlantic cod (Gadus morhua) infected with Trypanosoma murmanensis. Journal Fisheries Research Board Canada, 34(11), 2185–2192.


Khan, R. A. (2012). Host-parasite interactions in some fish species. Review article. Journal of Parasitology Research, 2012, article ID 237280.


Kharat, S., & Kothavade, S. (2012). Hematological study of Clarias batrachus with reference to trypanosomiasis. Trends in Fisheries Research, 1(1), 6–9.


Kuklina, M. M., & Kuklin, V. V. (2011). Biohimicheskie i gematologicheskie pokazateli moevki Rissa tridactyla (Linnaeus, 1758) pri invazii tsestodami Alcataenia larina (Krabbe, 1869) (Cestoda: Dilepididae) [Biochemical and haematological parameters of the kittiwake Rissa tridactyla (Linnaeus, 1758) during the invasion of cestodes Alcataenia larina (Krabbe, 1869) (Cestoda: Dilepididae)]. Rossijskij Parazitologicheskij Zhurnal, 3, 62–67 (in Russian).


Kutyrev, I. A., Pronin, N. M., & Dugarov, Z. N. (2011). Composition of leucocytes of the head kidney of the crucian carp (Carassius auratus gibelio, Cypriniformes: Cyprinidae) as affected by invasion of cestode Digramma interrupta (Cestoda; Pseudophyllidea). Biology Bulletin, 38(6), 653–657.


Lapkina, L. N., Zharikova, T. I., Svirskij, A. M. (2002). Zarazhennost' ryb pijavkami (sem. Piscicolidae) v volzhskih vodohranilischah [Infection of fish with leeches (family Piscicolidae) in the Volga reservoirs]. Parazitologija, 36(2), 132–139 (in Russian).


Lazareva, G. A. (2016). Otsenka kachestva vod Uglichskogo vodohranilischa po integral'nym gidrohimicheskim pokazateljam [Assessment of the Uglich reservoir water quality by integral hydrochemical indicators]. Vestnik Moskovskogo Gosudarstvennogo Oblastnogo Universiteta, Serija Estestvennye Nauki, 2, 158–164 (in Russian).


Lemos, M., Fermino, B. R., Simas-Rodrigues, C., Hoffmann, L., Silva, R., Camargo, E. P., Teixeira, M. M. G., & Souto-Padrón, T. (2015). Phylogenetic and morphological characterization of trypanosomes from Brazilian armoured catfishes and leeches reveal high species diversity, mixed infections and a new fish trypanosome species. Parasites and Vectors, 8, 573.


Levinsky, R. (1981). Role of circulating immune complexes in renal diseases. Journal of Clinical Pathology, 34, 1214–1222.


Lom, J., & Dykova, I. (1984). Pathogenicity of some protozoan parasites of cyprinid fishes. Symposia Biological Hungarica, 23, 99–118.


Maqbool, A., & Ahmed, I. (2016). Haematological response of snow barbell, Schizothorax plagiostomus Heckel, naturally infected with a new Trypanosoma species. Journal of Parasitic Diseases, 40(3), 791–800.


Mork, J. (2011). Prevalence of the haemoflagellate Trypanosoma sp. in some common Norwegian marine fish species. Sarsia, 73(4), 263–266.


Oladiran, A., Beauparlant, D., & Belosevic, M. (2011). The expression analysis of inflammatory and antimicrobial genes in the goldfish (Carassius auratus L.) infected with Trypanosoma carassii. Fish and Shellfish Immunology, 31(4), 606–613.


Osman, H. A. M., Fadel, N. G., & Ali, A. T. (2009). Biochemical and histopathological alterations in catfish, Clarias gariepinus, infected with trypanosomiasis with special reference to immunization. Egypt Journal of Comparative Pathology and Clinical Pathology, 22, 164–181.


Plouffe, D. A., & Belosevic, M. (2006). Antibodies that recognize α- and β-tubulin inhibit in vitro growth of the fish parasite Trypanosoma danilewskyi, Laveran and Mesnil, 1904. Developmental and Comparative Immunology, 30(8), 685–697.


Qadri, S. S. (1962). An experimental study of the life cycle of Trypanosoma danilewskyi in the Leech, Hemiclepsis marginata. Journal of Eukaryotic Microbiology, 9(3), 254–258.


Ranzani-Paiva, M. J. T., Ishikawa, C. M., Campos, B. E. S., & Eiras, A. C. (1997). Haematological characteristics associated with parasitism in mullets, Mugil platanus Günther, from the estuarine region of Cananéia, São Paulo, Brazil. Revista Brasileira de Zoologia, 14(2), 329–339.


Ribeiro, C. M. S., Pontes, M. J. S. L., Bird, S., Chadzinska, M., Scheer, M., Verburg-van Kemenade, B. M. L. (2010). Trypanosomiasis-induced Th17-like immune responses in carp. PLoS One, 5(9), e13012.


Rodrigues, R. N., Oliveira, M. S. B., Tavares-Dias, M., & Corrêa, L. L. (2018). First record of infection by Trypanosoma sp. of Colossoma macropomum (Serrasalmidae), a neotropical fish cultivated in the Brazilian Amazon. Journal of Applied Aquaculture, 30(1), 29–38.


Shahi, N., Yousuf, A. R., Rather, M. I., Ahmad, F., & Yaseen, T. (2013). First report of blood parasites in fishes from Kashmir and their effect on the haematological profile. Open Veterinary Journal, 3(2), 89–95.


Sitja-Bobadilla, A. (2008). Living off a fish: A trade-off between parasites and the immune system. Fish and Shellfish Immunology, 25, 358–372.


Stafford, J. L., & Belosevic, M. (2003). Transferrin and the innate immune response of fish: Identification of a novel mechanism of macrophage activation. Developmental and Comparative Immunology, 27(6–7), 539–554.


Steinhagen, D., Kruse, P., & Körting, W. (1990). Some haematological observations on carp, Cyprinus carpio L., experimentally infected with Trypanoplasma borreli Laveran & Mesnil, 1901 (Protozoa: Kinetoplastida). Journal Fish Diseases, 13(2), 157–162.


Sypek, J. P., & Burreson, E. M. (1983). Influence of temperature on the immune response of juvenile summer flounder, Paralichthys dentatus, and its role in the elimination of Trypanoplasma bullocki infections. Developmental and Comparative Immunology, 7(2), 277–286.


Tkachenko, A. V. (2009). Vlijanie strongiloidoznoj invazii na morfologicheskie, biohimicheskie i immunobiologicheskie pokazateli krovi i razrabotka me-todov ih korrektsii pri terapii loshadej [Influence of strongyloid infection on morphological, biochemical and immunobiological indicators of blood and development of methods for their correction in the therapy of horses]. Tjumen' (in Russian).


Wang, M., Yan, S., Wang, Y., Lun, Z. R., & Yang, T. B. (2015). Occurrence of trypanosomiasis in net cage cultured groupers (Cromileptes altivelis and Epinephelus fuscoguttatus) in Nanshan port of Sanya, Hainan province, China. Aquaculture Research, 46(5), 1039–1043.


Wiegertjes, F. G., & Forlenza, M. (2010). Nitrosative stress during infection-induced inflammation in fish: Lessons from a host-parasite infection model. Current Pharmaceutical Design, 16(38), 4194–4202.


Woo, P. T. K. (1981). Acquired immunity against Trypanosoma danilewskyi in goldfish, Carassius auratus. Parasitology, 83, 343–346.


Woo, P. T. K. (2001). Cryptobiosis and its control in North American fishes. International Journal for Parasitology, 31, 566–574.


Zintl, A., Poole, W. R., Voorheis, H. P., & Holland, C. V. (1997). Naturally occurring Trypanosoma granulosum infections in the european eel, Anguilla anguilla L. from County Mayo, Western Ireland. Journal of Fish Diseases, 20(5), 333–341.


Zuo, X., & Woo, P. T. K. (2000). In vitro haemolysis of piscine erythrocytes by purified metallo-protease from the pathogenic haemoflagellate, Cryptobia salmositica Katz. Journal of Fish Diseases, 23, 227–230.

Published
2018-05-11
How to Cite
Lapirova, T. B., & Zabotkina, E. A. (2018). Effect of trypanosomiasis on hematologic characteristics of bream (Abramis brama). Regulatory Mechanisms in Biosystems, 9(3), 309-314. https://doi.org/https://doi.org/10.15421/021845

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