Skip to main content
SpringerLink
Log in

A study on the status of inflammatory systems in camels naturally infected with Toxoplasma gondii

  • Regular Articles
  • Published:
Tropical Animal Health and Production Aims and scope Submit manuscript

Abstract

Toxoplasma gondii is a unique intracellular parasite with a worldwide distribution. This parasite infects a variety of cells in a wide range of animal species such as dromedary camels (Camelus dromedarius). In order to evaluate the pattern of possible changes in the blood level of some inflammatory mediators and antioxidant enzymes in camels infected with T. gondii, blood samples were taken from a total of 493 dromedary camels and serum concentrations of inflammatory mediators, acute phase proteins and antioxidant enzymes were measured. According to serological data, no seropositivity was found for anti-T. gondii IgM in serum samples; however, 49 camels (9.93 %) showed positive titrations for anti-Toxoplasma IgG. The analyses of data in seropositive animals showed significant increases (P < 0.05) in the serum level of IL-1β and adenosine deaminase activity; however, IFN-γ and TNF-α demonstrated no significant changes in serum samples of the infected camels. In addition, while major acute phase proteins (haptoglobin (Hp) and serum amyloid A (SAA)) were markedly elevated in infected camels, the activity of antioxidant enzymes (SOD and GPX) was remarkably decreased in the blood samples of infected animals. Thus, during the chronic infection in camels, T. gondii can promote significant rises in concentrations of some cytokines (such as IL-1β), acute phase proteins and adenosine deaminase.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Arthington, J.D., Eicher, S.D., Kunkle, W.E. and Martin, F.G., 2003. Effect of transportation and commingling on the acute-phase protein response, growth, and feed intake of newly weaned beef calves. Journal of Animal Science, 81, 1120–1125

    CAS  PubMed  Google Scholar 

  • Chang, H.R., Grau, G.E. and Pechère, J.C., 1990. Role of TNF and IL-1 in infections with Toxoplasma gondii. Immunology, 69(1), 33–37

    PubMed Central  CAS  PubMed  Google Scholar 

  • Cozon, G.J.N., Ferrandiz, J., Nebhi, H., Wallon, M. and Peyron, F., 1998. Estimation of the avidity of immunoglobulin G for routine diagnosis of chronic Toxoplasma gondii infection in pregnancy women. European Journal of Clinical Microbiology & Infectious Diseases, 17, 32–36

    Article  CAS  Google Scholar 

  • Dubey, J.P., 2010. Toxoplasmosis of Animals and Humans, 2nd ed. CRC Press, Inc, Boca Raton, FL, USA

    Google Scholar 

  • Eckersall, P.D., 2000. Recent advances and future prospects for the use of acute phase proteins as markers of disease in animals. Revue de Medecine Veterinaire, 151, 577–584

  • Elamin, E.A., Elias, S., Daugschies, A. and Rommel, M., 1992. Prevalence of Toxoplasmab gondii antibodies in pastoral camels (Camelus dromedarius) in the Butana plains, mid-eastern Sudan. Veterinary Parasitology, 43,171–175

  • Flohe, L., (1971) Glutathione peroxidase: enzymology and biological aspects. Klinische Wocllenschrift, 49, 669–683

    Article  CAS  Google Scholar 

  • Grewal, A., Ahuja, C.S., Singh, S.P. and Chaudhary, K.C., 2005. Status of lipid peroxidation, some antioxidant enzymes and erythrocytic fragility of crossbred cattle naturally infected with Theileria annuluta. Veterinary Research Communications, 29, 387–394

  • Gruys, E., Toussaint, M.J.M., Niewold, T.A. and Koopmans, S.J., 2005. Acute phase reaction and acute phase proteins. Journal of Zhejiang University Science B 6, 1045–1056.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hafeman, D.G., Sunde, R.A. and Hoekstra, W.G., 1974. Effect of dietary selenium on erythrocyte and liver glutathione peroxidase in rat. Journal of Nutrition, 104, 580–587

    CAS  PubMed  Google Scholar 

  • Hamidinejat, H., Ghorbanpouri, M., Rasooli, A., Nouri, M., Hekmatimoghaddam, S.H., Namavari, M.M., Pourmehdi-Borojeni, M. and Sazmand, A., 2013. Occurrence of anti-Toxoplasma gondii and Neospora caninum antibodies in camels (Camelus dromedarius) in the center of Iran. Turkish Journal of Veterinary and Animal Sciences, 37, 277–281

    Google Scholar 

  • Johnson, A.M., McDonald, P.J. and Neoh, S.H., 1983. Monoclonal antibodies to Toxoplasma cell membrane surface antigens protect mice from toxoplasmosis. The Journal of Protozoology, 30, 351–356

    Article  CAS  PubMed  Google Scholar 

  • Kelly, C. D., Russo, C.M., Rubin, B.Y., and Murray, H.W., 1989. Antigen stimulated human interferon gamma generation: role of accessory cells in their expressed or secreted products. Clinical and Experimental Immunology, 77, 397–402

    PubMed Central  CAS  PubMed  Google Scholar 

  • Latimer, K.S., Mahaffey, E.A. and Prasse, K.W., 2003. Veterinary Laboratory Medicine. Clinical Pathology. 4th edn., Iowa State Press., Iowa, pp:3–45, 260–270

    Google Scholar 

  • Mauel, J., 1984. Mechanisms of survival of protozoan parasites in mononuclear phagocytes. Parasitology, 88, 579–592

    Article  CAS  PubMed  Google Scholar 

  • Murata, H., Shimada, N. and Yoshioka, M., 2004. Current research on acute phase proteins in veterinary diagnosis: an overview. Veterinary Journal, 168, 28 –40

    Article  CAS  Google Scholar 

  • McCabe, R.E., Luft, B.J. and Remington, J.S., 1984. Effect of murine interferon gamma on murine toxoplasmosis. Journal of Infectious Diseases, 150, 961–962

    Article  CAS  PubMed  Google Scholar 

  • Nazifi, S., Razavi, S.M., Esmailnejad, Z. and Gheisari, H., 2009. Study on acute phase proteins (haptoglobin,serum amyloid A, fibrinogen, and ceruloplasmin) changes and their diagnostic values in bovine tropical theileriosis. Parasitology Research, 105, 41–46

  • Nazifi, S., Razavi, S.M., Kianiamin, P. and Rakhshandehroo, E., 2011. Evaluation of erythrocyte antioxidant mechanisms: antioxidant enzymes, lipid peroxidation and serum trace elements associated with progressive anemia in ovine malignant theileriosis. Parasitology Research, 109, 275–281

    Article  CAS  PubMed  Google Scholar 

  • Paglia, D.E. and Valentine, W.N., 1967. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. The Journal of Laboratory and Clinical Medicine, 70,158 − 169

    CAS  PubMed  Google Scholar 

  • Pelloux, H., Chumpitazi, B.F., Santoro, F., Polack, B., Vuillez, J.P. and Ambroise-Thomas, P., 1992. Sera of patients with high titers of immunoglobulin G against Toxoplasma gondii induce secretion of tumor necrosis factor alpha by human monocyte. Infection and Immunity, 60(7), 2672–2676

    PubMed Central  CAS  PubMed  Google Scholar 

  • Pieiro, M., Pineiro, C., Carpintero, R., Morales, J., Campbell, F.M., Eckersall, P.D., Toussaint, M.J. and Lampreave, F., 2007. Characterization of the pig acute phase protein response to road transport. Veterinary Journal, 173, 669–674

    Article  Google Scholar 

  • Razavi, S.M., Nazifi, S., Bateni, M. and Rakhshandehroo, E. 2011. Alterations of erythrocyte antioxidant mechanisms: Antioxidant enzymes, lipid peroxidation and serum trace elements associated with anemia in bovine tropical theileriosis. Veterinary Parasitology, 180, 209–214

    Article  CAS  PubMed  Google Scholar 

  • Remington, J.S. and Krahenbuhl, J.L., 1982. Immunology of Toxoplasma gondii. In Comprehensive immunology, Vol. 9: Immunology of human infections, part II (A.J. Nahmias and R.J. O'Reilly, eds.). Plenum Publishing Corp., New York, 327–371

  • Sadrebazzaz, A., Haddadzadeh, H. and Shayan, P., 2006. Seroprevalence of Neospora caninum and Toxoplasma gondii in camels (Camelus dromedarius) in Mashhad, Iran. Parasitology Research, 98, 600–601.

    Article  CAS  PubMed  Google Scholar 

  • Senesi, S., Batoni, G., Bianchi, F., Freer, G., Dolfi, A., Campa, M. and Lupetti, M., 1990. Questioning the role of adenosine deaminase in the development of B lymphocytes in chicken bursa. Developmental and Comparative Immunology, 14, 95–104

    Article  CAS  PubMed  Google Scholar 

  • Shaapan, R.M. and Khalil, A.M.F., 2008. Evaluation of different Toxoplasma gondii isolates as antigens used in the modified agglutination test for the detection of toxoplasmosis in camels and donkeys. Eurasian Journal of Agricultural and Environmental Sciences, 3(6), 837–841

    Google Scholar 

  • Shiono, H., Yagi, Y., Chikayama, Y., Miyazaki, S. and Nakamura I., 2003a. The influence of oxidative bursts of phagocytes on red blood cell oxidation in anemic cattle infected with Theileria sergenti. Free Radical Research, 37, 1181–1189

    Article  CAS  PubMed  Google Scholar 

  • Shiono, H., Yagi, Y., Chikayama, Y., Miyazaki, S. and Nakamura, I., 2003b. Oxidative damage and phosphatidylserine expression of red blood cells in cattle experimentally infected with Theileria sergenti. Parasitology Research, 89, 228–234

    PubMed  Google Scholar 

  • Suzuki, Y., Orellana, M.A., Schreiber, R.D. and Remington, J.S., 1988. Interferon-gamma: the major mediator of resistance against Toxoplasma gondii. Science, 240, 516–518

    Article  CAS  PubMed  Google Scholar 

  • Tajik, J., Moghaddar, N., Nikjou, D. and Taleban, Y., 2011. Occurrence of gastrointestinal helminthes in Bactrian camel in Iran. Tropical Biomedicine, 28(2), 362–365

    CAS  PubMed  Google Scholar 

  • Ungerer, J.P.J., Oosthuizen, H.M., Bissbort, S.H. and Wermaak, W.J.H., 1992. Serum adenosine deaminase; isoenzymes and diagnostic application. Clinical Chemistry, 38, 1322–1326

    CAS  PubMed  Google Scholar 

  • Utuk, A.E., Kirbas, A., Babur, C. and Balkaya, I., 2012. Detection of Toxoplasma gondii antibodies and some helminthic parasites in camels from Nevsehir province of Turkey. Israel Journal of Veterinary Medicine, 67,106-108

    Google Scholar 

  • Yasodhara, P., Ramalakshmi, B.A., Sarma, M.K., 2001. A new approach to differentiate recent vs chronic Toxoplasma infection:avidity ELISA in Toxoplasma serology. Indian Journal of Medical Microbiology, 19, 145–8.

Download references

Acknowledgments

The authors would like to thank the Research Council of Shiraz University and School of Veterinary Medicine, Shiraz University for financial and technical support of this study (Grant No.71-GR-VT-5).

Conflict of interest statement

We declare that we have no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Pathobiology, School of Veterinary Medicine, Shiraz University, Shiraz, Iran

    Fatemeh Azma, Seyed Mostafa Razavi, Ehsan Rakhshandehroo & Ahmad Reza Sanati

  2. Department of Clinical Studies, School of Veterinary Medicine, Shiraz University, P.O. Box: 1731–71345, Shiraz, Iran

    Saeed Nazifi

Authors
  1. Fatemeh Azma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Seyed Mostafa Razavi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Saeed Nazifi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ehsan Rakhshandehroo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ahmad Reza Sanati
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Saeed Nazifi.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Azma, F., Razavi, S.M., Nazifi, S. et al. A study on the status of inflammatory systems in camels naturally infected with Toxoplasma gondii . Trop Anim Health Prod 47, 909–914 (2015). https://doi.org/10.1007/s11250-015-0807-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11250-015-0807-6

Keywords

Search

Navigation