Veterinary Research Forum
Vet Res Forum

Association between proliferation status of infected and non-infected mononuclear cells with tissue lesions in acute bovine theileriosis

Document Type : Original Article

Authors

Afsaneh Doulatkhah 1
Mohsen Maleki 1
Ahmad Nematollahi 2
Javad Ashrafi Helan 2
Golamreza Razmi 1

1 Department of Pathobiology, Faculty of Veterinary Medicine, Ferdowsi University of Mashhad, Iran

2 Department of Pathobiology, Faculty of Veterinary Medicine, University of Tabriz, Iran

https://doi.org/10.30466/vrf.2023.1988500.3766
Abstract
Tropical or Mediterranean theileriosis in dairy cattle is widely distributed in many tropical regions of the world. The purpose of this study was to evaluate the proliferation status of mononuclear cells infected with Theileria annulata schizonts in different tissues and its relationship with the pathogenesis of the parasite in cattle by histopathology, immuno-histochemistry and polymerase chain reaction (PCR). Blood and tissue samples of eight Holstein cattle that had been lost due to theileriosis and eight healthy slaughtered cattle of the same breed were collected as a control group after necropsy. The piroplasms in the blood smears and the schizonts in the cytoplasm of the lymphocytes and macrophages of the lymph nodes were microscopically detected. Histopathologically, the proliferation of macrophages, lymphocytes, and plasma cells in lymph nodes and the heart, congestion, and bleeding in the red pulp of the spleen, portal tracts of the liver, interstitial tissue of the kidneys, multifocal necrosis and ulceration in the abomasum together with hyperemia and hemorrhages and lymphoblastic infiltration in the submucosa and lamina propria adjacent to these lesions and emphysema with ecchymotic hemorrhage in the lungs were evident. Immunohistochemistry identified the proliferated cells as mostly Cluster of Differentiation 3- Positive T lymphocytes and macrophage marker antibody 387- positive macrophages. Positive results of PCR for the Tams1 30.00 kDa gene were observed in lymph nodes, liver, lung and abomasum. It was concluded that the pathological changes were the result of schizont-infected macrophage proliferation leading to severe uncontrolled proliferation of uninfected T lymphocytes.

Keywords

Cattle
Histopathology
Immunohistochemistry
PCR
Theileria annulata

Subjects

  1. Purnell RE. Theileria annulata as a hazard to cattle in countries on the northern Mediterranean littoral. Vet Sci Commun 1987; 2: 3-10.
  2. Perston PM, Theileriosis. In: Service MW (Ed). The encyclopedia of arthropod- transmitted infections of man and domesticated animals. Wallingford, UK: CAB International 2001; 268-274.
  3. Kalani H, Fakhar M, Pagheh A. An overview on present situation babesiosis and theileriosis and their distribution of ticks in Iran. Iran J Med Microbiol 2012; 5(4): 59-71.
  4. Perveen N, Muzaffar SB, Al-Deeb MA. Ticks and tick-borne diseases of livestock in the Middle East and North Africa: A review. Insects. 2021; 12(1): 83. doi: 10.3390/insects12010083.
  5. Hooshmand-Rad P. The pathogenesis of anaemia in Theileria annulata Res Vet Sci 1976; 20(3): 324-329.
  6. Liu J, Guan G, Yin H. Theileria annulata. Trends Parasitol 2022; 38(3): 265-266.
  7. Constable PD, Hinchcliff KW, Done SH. Veterinary medicine: A textbook of the diseases of cattle, horses, sheep, pigs, and goats, 11th St. Louis, USA: Elsevier 2017; 603-618.
  8. Brown DJ, Campbell JD, Russell GC, et al. T cell activation by Theileria annulata-infected macrophages correlates with cytokine production. Clin Exp Immunol 1995; 102(3): 507-514.
  9. Motevalli Haghi SM, Fakhar M, Sharif M, et al. An overview on different diagnostic methods for babesiosis. J Mazandaran Univ Med Sci 2014; 23(109): 283-295.
  10. Soosaraei M, Haghi MM, Etemadifar F, et al. Status of theileriosis among herbivores in Iran: A systematic review and meta-analysis. Vet World 2018; 11(3): 332-341.
  11. Rahbari S, Nabian S, Shayan P. Primary report on distribution of tick fauna in Iran. Parasitol Res 2017; 101(Suppl 2): S175-S177.
  12. Oryan A, Namazi F, Sharifiyazdi H, et al. Clinicopathological findings of a natural outbreak of Theileria annulata in cattle: an emerging disease in southern Iran. Parasitol Res 2013; 112(1): 123-127.
  13. Gupta A, Gupta K, Leishangthem GD, et al. Molecular and pathological studies on natural cases of bovine theileriosis. J Parasit Dis 2017; 41(1): 211-218.
  14. Ma Q, Liu J, Li Z, et al. Clinical and pathological studies on cattle experimentally infected with Theileria annulata in China. Pathogens 2020; 9(9):727. doi: 10.3390/pathogens9090727.
  15. Jain NC. Veterinary hematology. 4th Philadelphia, USA: Lea and Febiger, 1986; 237-241.
  16. Kiernan JA. Histological and histochemical methods: theory and practice. 5th Banbury, UK: Scion Publishing Ltd 2015; 58-60.
  17. d'Oliveira C, van der Weide M, Habela MA, et al. Detection of Theileria annulata in blood samples of carrier cattle by PCR. J Clin Microbiol 1995; 33(10): 2665-2669.
  18. Fry LM, Schneider DA, Frevert CW, et al. East coast fever caused by Theileria parva is characterized by macrophage activation associated with vasculitis and respiratory failure. PLoS One 2016; 11(5): e0156004. doi: 10.1371/journal.pone.0156004.
  19. Uilenberg G. International collaborative research: significance of tick-borne hemoparasitic diseases to world animal health. Vet Parasitol 1995; 57(1-3): 19-41.
  20. Hashemi-Fesharki R. Recent development in control of Theileria annulata in Iran. Parasite, 1998; 5(2): 193-196.
  21. Raoofi A, Fatemi M, Bokaie S, et al. Comparison of tolerance to theileriosis in different breed of cattle by evaluation of clinical signs and response to treatment. Iran J Vet Med 2020; 14(3): 231-237.
  22. Gill BS, Bhattacharyulu Y, and Kaur D. Symptoms and pathology of experimental bovine tropical theileriosis (Theileria annulata infection). Annal Parasitol Hum Comp 1977; 52(6): 597-608.
  23. Bansal GC, Gill BS, Bhattacharyulu Y, et al. Comparative pathogenicity of Theileria annulata Vet Q 1987; 9(2): 189-191.
  24. Preston PM, Brown CG, Bell-Sakyi L, et al. Tropical theileriosis in Bos taurus and Bos taurus cross Bos indicus calves: response to infection with graded doses of sporozoites of Theileria annulata. Res Vet Sci 1992; 53(2): 230-243.
  25. Branco S, Orvalho J, Leitão A, et al. Fatal cases of Theileria annulata infection in calves in Portugal associated with neoplastic-like lymphoid cell proliferation. J Vet Sci 2010; 11(1): 27-34.
  26. Li Z, Liu J, Ma Q, et al. Development and evaluation of a chemiluminescence immunoassay for detecting tropical theileriosis. Acta Trop 2020; 202: 105245. doi: 10.1016/j.actatropica.2019.105245.
  27. Forsyth LM, Minns FC, Kirvar E, et al. Tissue damage in cattle infected with Theileria annulata accompanied by metastasis of cytokine-producing, schizont-infected mononuclear phagocytes. J Comp Pathol 1999; 120(1): 39-57.
  28. Kirvar E, Ilhan T, Katzer F, et al. Detection of Theileria annulata in cattle and vector ticks by PCR using the Tams1 gene sequences. Parasitology 2000; 120(Pt 3): 245-254.
  29. Innes EA, Ouhelli H, Oliver RA, et al. The effect of MHC compatibility between parasite–infected cell line and recipient in immunization against tropical theileriosis. Parasite immunol 1989; 11(1): 47-56.
  30. Graham SP, Brown DJ, Vatansever Z, et al. Proinflammatory cytokine expression by Theileria annulata infected cell lines correlates with the pathology they cause in vivo. Vaccine 2001; 19(20-22): 2932-2944.
  31. Glass EJ. The balance between protective immunity and pathogenesis in tropical theileriosis: what we need to know to design effective vaccines for the future. Res Vet Sci 2001; 70(1): 71-75.
  32. Tajeri S, Langsley G. Theileria secretes proteins to subvert its host leukocyte. Biol Cell 2021: 113(4): 220-233.
  33. Kessy VM, Matovelo JA. Immunohistochemical characterization and quantification of lymphocytes infiltrating bovine lungs in East Coast Fever. Int J Appl Res Vet Med 2011; 9(1): 87-99.
Veterinary Research Forum
Volume 14, Issue 12
December 2023
Pages 643-648

  • Receive Date 09 February 2023
  • Revise Date 23 May 2023
  • Accept Date 24 May 2023

Home

Guide for Authors

Submit Manuscript

Reviewers

Contact Us