Skip to main content
Log in

Experimental opisthorchiasis: Study of blood cell composition, hematopoiesis, and startle reflex in laboratory animals

  • Published:
Russian Journal of Genetics: Applied Research

Abstract

The Opisthorchis felineus (O. felineus), one of the species from the Opisthorchiidae family, causes severe disorders in the human and animal organism; therefore, it is the subject of topical scientific studies. In this work, a comparative study of the influence of the O. felineus invasions on the change in the blood cell composition, bone marrow hematopoiesis, and behavioral startle reflex was conducted in the C57BL/6 mice and Syrian hamsters two weeks after infection. Significant interspecies differences in many indices were found. It was established that the relative weight of the spleen (the main peripheral immune system organ) is significantly larger in mice than in hamsters. Moreover, the O. felineus invasion caused the hypertrophy of the spleen only in mice. More pronounced deviations from the norm in the blood cell composition, that were accompanied by the activation of myelo- and erythropoiesis, were observed in hamsters. The established changes in the blood in mice were not accompanied by changes in the bone marrow colony-forming activity. Mice also differed from hamsters by the startle reaction to the acoustic signal both by the severity of the reaction and prepulse inhibition value. No habituation reaction to the sound signal was observed in the infected hamsters. In addition, maturation of the O. felineus worms in hamsters occurred earlier than in mice. The data obtained indicate the increased resistance of mice to the O. feluneus infection; however, they do not exclude the possibility of using mice as a model during the study of the processes occurring in the host organism against the background of the experimental opisthorchiasis development.

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

  • Adams, A.M., Foodborne Trematodes. Foodborne Parasites, Ortega, Y.R., Ed., New York: Springer Science + Business Media, LLC, 2006, ch. 7.

  • Akhmedov, V.A. and Kritevich, M.A., Chronic opisthorchiasis as multiple organ pathology, Vestn. Nov. Gos. Univ., Ser. Biol. Klin. Med., 2009, vol. 7, no. 1, pp. 118–121.

    Google Scholar 

  • Bakshtanovskaya, I.V. and Stepanova, T.F., Analysis of the complex biochemical parameters of liver function in chronic opisthorchiasis, Med. Parazitol. Parazitar. Bolezni, 2005, vol. 4, pp. 18–21.

    Google Scholar 

  • Boonmars, T., Boonjaraspinyo, S., and Kaewsamut, B., Animal models for Opisthorchis viverrini infection, Parasitol. Res., 2009, vol. 104, pp. 701–703.

    Article  PubMed  Google Scholar 

  • Braff, D.L., Geyer, M.A., and Swerdlow, N.R., Human studies of prepulse inhibition of startle: Normal subjects, patient groups, and pharmacological studies, Psychopharmacology, 2001, vol. 156, pp. 234–258.

    Article  CAS  PubMed  Google Scholar 

  • Brazhnikova, N.A. and Tolkaeva, M.V., Features of clinic, diagnostics and treatment of opisthorchis liver abscesses, Ann. Khir. Gepatol., 2000, vol. 5, no. 1, pp. 37–42.

    Google Scholar 

  • Brazhnikova, N.A. and Tolkaeva, M.V., Cancer of the liver, biliary tract, and pancreas in chronic opisthorchiasis, Byull. Sib. Med., 2002, vol. 2, pp. 71–76.

    Google Scholar 

  • Bronshtein, A.M. and Luchshev, V.I., Liver trematodoses: Opisthorchiasis and clonorchiasis, Russ. Med. Zh., 1998, vol. 6, no. 3, pp. 140–148.

    Google Scholar 

  • Bychkov, V.G., Krylov, G.G., Sabirov, A.Kh., Zuevskii, V.P., Khadieva, E.D., and Zhandekov, A.K., The dynamics of cellular changes in the liver in experimental opisthorchiasis, Med. Parazitol. Parazitar. Bolezni, 2008, vol. 3, pp. 9–12.

    Google Scholar 

  • Choi, Y.K., Yoon, B.I., Won, Y.S., Lee, C.H., Hyun, B.H., Kim, H.C., Oh, G.T., and Kim, D.Y., Cytokine responses in mice infected with Clonorchis sinensis, Parasitol. Res., 2003, vol. 91, no. 2, pp. 87–93.

    Article  PubMed  Google Scholar 

  • D’Mello, C. and Swain, M.G., Liver-brain inflammation axis, Am. J. Physiol. Gastrointest. Liver Physiol., 2011, vol. 301, no. 5, pp. G749–G61.

    Article  PubMed  Google Scholar 

  • Garrick, T., Morrow, N., Shalev, A.Y., and Eth, S., Stressinduced enhancement of auditory startle: An animal model of posttraumatic stress disorder, Psychiatry, 2001, vol. 64, pp. 346–354.

    Article  CAS  PubMed  Google Scholar 

  • Geyer, M.A. and Braff, D.L., Startle habituation and sensorimotor gating in schizophrenia and related animal models, Schizophr. Bull., 1987, vol. 13, no. 4, pp. 643–668.

    Article  CAS  PubMed  Google Scholar 

  • Graham, F., The more or less startling effects of weak prestimuli, Psychophysiology, 1975, vol. 12, pp. 238–248.

    Article  CAS  PubMed  Google Scholar 

  • Hoffman, H.S. and Searle, J.L., Acoustic and temporal factors in the evocation of startle, J. Acoust. Soc. Am., 1968, vol. 43, pp. 269–282.

    Article  CAS  PubMed  Google Scholar 

  • Hung, N.M., Madsen, H., and Fried, B., Global status of fish-borne zoonotic trematodiasis in humans, Acta Parasitol., 2013, vol. 58, no. 3, pp. 231–258.

    Article  PubMed  Google Scholar 

  • Jittimanee, J., Sermswan, R.W., Puapairoj, A., Maleewong, W., and Wongratanacheewin, S., Cytokine expression in hamsters experimentally infected with Opisthorchis viverrini, Parasite Immunol., 2007, vol. 29, no. 3, pp. 159–167.

    Article  CAS  PubMed  Google Scholar 

  • Keiser, J. and Utzinger, J., Food-borne trematodiasis: Current chemotherapy and advances with artemisinins and synthetic trioxolanes, Trends Parasitol., 2007, vol. 23, no. 11, pp. 555–562.

    Article  CAS  PubMed  Google Scholar 

  • King, K.Y. and Goodell, M.A., Inflammatory modulation of HSCS: Viewing the HSC as a foundation for the immune response, Nature, 2011, vol. 11, pp. 685–692.

    CAS  Google Scholar 

  • Kishkun, A.A., Klinicheskaya laboratornaya diagnostika (Clinical Laboratory Diagnostics), Moscow: GEOTARMedia, 2013.

    Google Scholar 

  • Kozlov, V.A., Zhuravkin, I.N., and Tsyrlova, I.G., Stvolovaya krovetvornaya kletka i immunnyi otvet (Stem Hematopoietic Cells and the Immune Response), Novosibirsk: Nauka, 1982.

    Google Scholar 

  • Labome.com., Laboratory mice and rats, Mat. Methods, 2012, vol. 2, p. 113. http://www.labome.com/method/Laboratory-Mice-and-Rats.html.

    Google Scholar 

  • Litvinova, L.S., Kolobovnikova, Yu.V., Knutareva, E.N., Grigor’eva, E.S., Suvorova, E.V., Novitskii, V.V., and Ryazantseva, N.V., The cytotoxic potential of eosinophilic granulocytes in patients with eosinophilia syndrome, Byull. Sib. Med., 2006, vol. 3, pp. 26–31.

    Google Scholar 

  • Lvova, M.N., Duzhak, T.G., Tsentalovich, Yu.P., Katokhin, A.V., and Mordvinov, V.A., The secretome of adult liver fluke Opisthorchis felineus, Parazitologiya, 2014, vol. 48, no. 3, pp. 26–31.

    Google Scholar 

  • Lvova, M.N., Zhukova, M.V., Kiseleva, E.V., Mayboroda, O.A., Hensbergen, P., Kizilova, E.A., Besprozvannykh, V.V., Sripa, B., Katokhin, A.V., and Mordvinov, V.A., Hemozoin in the gut contents of liver flukes (Opisthorchiidae family), Int. J. Parasitol., 2016, vol. 46, pp. 147–156. doi 10.1016/ j.ijpara.2015.12.003

    Article  CAS  PubMed  Google Scholar 

  • Lvova, M.N., Tangkawattana, S., Balthaisong, S., Katokhin, A.V., Mordvinov, V.A., and Sripa, B., Comparative histopathology of Opisthorchis felineus and Opisthorchis viverrini in a hamster model: An implication of high pathogenicity of the European liver fluke, Parasitol. Int., 2012, vol. 61, no. 1, pp. 167–172.

    Article  CAS  PubMed  Google Scholar 

  • Mairiang, E., Laha, T., Bethony, J.M., Thinkhamrop, B., Kaewkes, S., Sithithaworn, P., Tesana, S., Loukas, A., Brindley, P.J., and Sripa, B., Ultrasonography assessment of hepatobiliary abnormalities in 3359 subjects with Opisthorchis viverrini infection in endemic areas of Thailand, Parasitol. Int., 2012, vol. 61, no. 1, pp. 208–211.

    Article  PubMed  Google Scholar 

  • Maksimova, G.A., Zhukova, N.A., Kashina, E.V., Lvova, M.N., Katokhin, A.V., Tolstikova, T.G., Ogorodova, L.M., Kaminskii, I.P., Sazonov, A.E., and Mordvinov, V.A., The experimental model of opisthorchiasis in hamsters (Mesocricetus auratus), Byull. Sib. Med., 2012, vol. 6, pp. 59–65.

    Google Scholar 

  • Maltby, S., Hansbro, N.G., Tay, H.L., Stewart, J., Plank, M., Donges, B., Rosenberg, H.F., and Foster, P.S., Production and differentiation of myeloid cells driven by proinflammatory cytokines in response to acute pneumovirus infection in mice, J. Immunol., 2014, vol. 193, no. 8, pp. 4072–4082.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marshall, R.D. and Garakani, A., Psychobiology of the acute stress response and its relationship to the psychobiology of post-traumatic stress disorder, Psychiat. Clin. N. Am., 2002, vol. 25, no. 2, pp. 385–395.

    Article  Google Scholar 

  • Megías, J., Yáñez, A., Moriano, S., O’Connor, J.E., Gozalbo, D., and Gil, M.L., Direct Toll-like receptormediated stimulation of hematopoietic stem and progenitor cells occurs in vivo and promotes differentiation toward macrophages, Stem Cells, 2012, vol. 30, no. 7, pp. 1486–1495.

    Article  PubMed  Google Scholar 

  • Mordvinov, V.A. and Furman, D.P., The digenea parasite Opisthorchis felineus: A target for the discovery and development of novel drugs, Infect. Disord. Drug Targets, 2010, vol. 10, no. 5, pp. 385–401.

    Article  CAS  PubMed  Google Scholar 

  • Mordvinov, V.A., Yurlova, N.I., Ogorodova, L.M., and Katokhin, A.V., Opisthorchis felineus and Metorchis bilis are the main agents of liver fluke infection of humans in Russia, Parasitol. Int., 2012, vol. 61, no. 1, pp. 25–31.

    Article  PubMed  Google Scholar 

  • Nacheva, L.V. and Lityagina, A.V., Cell reactions in helminthoses, Ross. Parazitol. Zh., 2012, vol. 3, pp. 80–86.

    Google Scholar 

  • Novitskii, V.V., Ryazantseva, N.V., Litvinova, L.S., Tkachenko, S.B., Kolobovnikova, Yu.V., Lepekhin, A.V., Chernyshova, N.P., Grigor’eva, E.S., Suvorova, E.V., and Zima, A.P., Changes in the production of key cytokines, regulators of eosinophilic granulocytes, under opisthorchosis invasion, Klin. Lab. Diagn., 2008, vol. 2, pp. 38–42.

    Google Scholar 

  • Ogorodova, L.M., Freidin, M.B., Sazonov, A.E., Fedorova, O.S., Gerbek, I.E., Cherevko, N.A., and Lebedeva, N.Y., A pilot screening of prevalence of atopic states and opisthorchosis and their relationship in people of Tomsk oblast, Parasitol. Res., 2007, vol. 101, no. 4, pp. 1165–1168.

    Article  CAS  PubMed  Google Scholar 

  • Paylor, R. and Crawley, J.N., Inbred strain differences in prepulse inhibition of the mouse startle response, Psychopharmacology, 1997, vol. 132, pp. 169–180.

    Article  CAS  PubMed  Google Scholar 

  • Pozio, E., Armignacco, O., Ferri, F., Gomez Morales, M.A., Opisthorchis felineus, an emerging infection in Italy and its implication for the European Union, Acta Trop., 2013, vol. 126, no. 1, pp. 54–62.

    Article  PubMed  Google Scholar 

  • Prokopenko, V.D. and Volina, E.G., Struktura i funktsii immunnoi sistemy cheloveka (The Structure and Function of the Human Immune System), Moscow: RUDN, 2001.

    Google Scholar 

  • Schuster, R., Dell, K., Nöckler, K., Vöster, J., Schwartz-Porsche, D., and Haider, W., Liver enzyme activity and histological changes in the liver of silver foxes (Vulpes vulpes fulva) experimentally infected with opisthorchiid liver flukes. A contribution to the pathogenesis of opisthorchiidosis, Parasitol. Res., 2003, vol. 89, no. 5, pp. 414–418.

    CAS  PubMed  Google Scholar 

  • Sripa, B. and Kaewkes, S., Relationship between parasitespecific antibody responses and intensity of Opisthorchis viverrini infection in hamsters, Parasite Immunol., 2000, vol. 22, no. 3, pp. 139–145.

    Article  CAS  PubMed  Google Scholar 

  • Sripa, B., Bethony, J.M., Sithithaworn, P., Kaewkes, S., Mairiang, E., Loukas, A., Mulvenna, J., Laha, T., Hotez, P.J., and Brindley, P.J., Opisthorchiasis and opisthorchis-associated cholangiocarcinoma in Thailand and Laos, Acta Trop., 2011, vol. 120, pp. S158–168.

    Article  PubMed  Google Scholar 

  • Sripa, B., Kaewkes, S., Sithithaworn, P., Mairiang, E., Laha, T., Smout, M., Pairojkul, C., Bhudhisawasdi, V., Tesana, S., Thinkamrop, B., Bethony, J.M., Loukas, A., and Brindley, P.J., Liver fluke induces cholangiocarcinoma, PLoS Med., 2007, vol. 4, no. 7, pp. 1148–1155.

    Article  Google Scholar 

  • Sripa, B., Thinkhamrop, B., Mairiang, E., Laha, T., Kaewkes, S., Sithithaworn, P., Periago, M.V., Bhudhisawasdi, V., Yonglitthipagon, P., Mulvenna, J., Brindley, P.J., Loukas, A., and Bethony, J.M., Elevated plasma IL-6 associates with increased risk of advanced fibrosis and cholangiocarcinoma in individuals infected by Opisthorchis viverrini, PLoS Negl. Trop. Dis., 2012, vol. 6, no. 5, pp. 1–9.

    Article  Google Scholar 

  • Stepanova, T.F., Bakshtanovskaya, I.V., and Skichko, S.I., Indicators of the thyroid status in patients with acute and super-invasive opisthorchiasis, Fund. Issled., 2004, vol. 6, pp. 103–104.

    Google Scholar 

  • Stepanova, T.F. and Podkletnova, L.F., Parazitotsenoticheskie aspekty invazionno-infektsionnoi patologii (opistorkhoz i tuberkulez) (Parasitocoenotic Aspects of Invasive-Infectious Pathology (Opisthorchiasis and Tuberculosis)), Tyumen: TGU, 2002.

    Google Scholar 

  • Yongvanit, P., Thanan, R., Pinlaor, S., Sithithaworn, P., Loilome, W., Namwat, N., Techasen, A., and Dechakhamphu, S., Increased expression of TLR-2, COX-2, and SOD-2 genes in the peripheral blood leukocytes of opisthorchiasis patients induced by Opisthorchis viverrini antigen, Parasitol. Res., 2012, vol. 110, no. 5, pp. 1969–1977.

    Article  PubMed  Google Scholar 

  • Zelentsov, A.G., Susceptibility of linear mice to helminths. II. Development of Opistorchis felineus in mouse lines A/Ne, CBA/Lac, CC57M/Mv, C57B1/6J, DBA/2J, and SWR, Med. Parazitol. Parazitar. Bolezni, 1974, vol. 43, no. 1, pp. 95–98.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D. F. Avgustinovich.

Additional information

Original Russian Text © D.F. Avgustinovich, I.A. Orlovskaya, L.B. Toporkova, G.B. Vishnivetskaya, A.V. Katokhin, M.N. Lvova, E.V. Kashina, N.P. Bondar, N.A. Feofanova, V.A. Mordvinov, 2016, published in Vavilovskii Zhurnal Genetiki i Selektsii, 2016, Vol. 20, No. 2, pp. 155–164.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Avgustinovich, D.F., Orlovskaya, I.A., Toporkova, L.B. et al. Experimental opisthorchiasis: Study of blood cell composition, hematopoiesis, and startle reflex in laboratory animals. Russ J Genet Appl Res 7, 82–92 (2017). https://doi.org/10.1134/S2079059717010038

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S2079059717010038

Keywords

Navigation