Document Type : Original Article

Authors

1 Department of Parasitology, Faculty of Veterinary Medicine, Shahid Chamran University of Ahvaz, Ahvaz, Iran

2 Department of Immunology, Faculty of Veterinary Medicine, Shahid Chamran University of Ahvaz, Ahvaz, Iran

3 Department of Biochemistry and Molecular Biology, Faculty of Veterinary Medicine, Shahid Chamran University of Ahvaz, Ahvaz, Iran

Abstract

Linguatula serrata is a worldwide zoonotic food-borne parasite. The parasite is responsible for linguatulosis and poses a concern to human and animal health in endemic regions. This study investigated the hematological changes, oxidant/antioxidant status and immunological responses in goats and sheep naturally infected with L. serrata. Hematological changes, antioxidant enzymes and malondialdehyde (MDA) levels were measured. The level of inter-leukin-2 (IL-2), IL-4, IL-5, IL-10, and tumor necrosis factor alpha (TNF-α) mRNA expression was investigated in lymph nodes. According to the hemogram results, eosinophils were significantly increased in the infected goats and sheep, and Horizontal Gene Transfer (HGT), hematocrit (HCT), and mean corpuscular hemoglobin concentration (MCHC) were significantly decreased. The levels of MDA and the activity of glutathione peroxidase (GPx) were significantly higher in infected animals than in non-infected animals. However, the activity of superoxide dismutase (SOD) and catalase (CAT) was significantly lower in infected animals than in non-infected animals. A comparison of the cytokine mRNA expression in lymph nodes from infected and non-infected animals showed higher cytokine expression in the infected animals. Infection with L. serrata caused microcytic hypochromic and normocytic hypochromic anemia in goats and sheep. The inconsistent results of immunological changes were found in infected goats and sheep. In both animals, oxidative stress occurred and led to an increase in lipid peroxidation. L. serrata created a cytokine microenvironment biased towards the type 2 immune responses.

Keywords

  1. Hajipour N, Tavassoli M. Prevalence and associated risk factors of Linguatula serrata infection in definitive and intermediate hosts in Iran and other countries: A systematic review. Vet Parasitol Reg Stud Reports 2019; 16: 100288. doi: 10.1016/j.vprsr.2019.100288.
  2. Mehlhorn H. Encyclopedic reference of parasitology. 3rd Heidelberg, Germany: Springer-Verlag 2008; 1114-1118.
  3. Islam R, Anisuzzaman, Hossain MS, et al. Linguatula serrata, a food-borne zoonotic parasite, in livestock in Bangladesh: Some pathologic and epidemiologic aspects. Vet Parasitol Reg Stud Reports 2018; 13: 135-140.
  4. Yılmaz H, Cengiz ZT, Ciçek M, et al. A nasopharyngeal human infestation caused by Linguatula serrate nymphs in Van province: a case report. Turkiye Parazitol Derg 2011; 35(1): 47-49.
  5. Yazdani R, Sharifi I, Bamorovat M, et al. Human linguatulosis caused by Linguatula serrata in the city of Kerman, south-eastern Iran- case report. Iran J Parasitol 2014; 9(2): 282-285.
  6. Tabibian H, Yousofi Darani H, Bahadoran-Bagh-Badorani M, et al. A case report of Linguatula serrata infestation from rural area of Isfahan city, Iran. Adv Biomed Res 2012; 1: 42. doi:4103/2277-9175.100142.
  7. Hajipour N, Ketzis J, Esmaeilnejad B, et al Pathological characteristics of Linguatula serrata (aberrant arthropod) infestation in sheep and factors associated with prevalence in Iran. Prev Vet Med 2019; 15: 172: 104781. doi:10.1016/j.prevetmed.2019.104781.
  8. Azizi H, Nourani H, Moradi A. Infestation and pathological lesions of some lymph nodes induced by Linguatula serrata nymphs in sheep slaughtered in Shahrekord Area (Southwest Iran). Asian Pac J Trop Biomed 2015; 5(7): 574-578.
  9. Yakhchali M, Tehrani A. The mesenteric lymph nodes pathology by nymph stage of Linguatula serrata in cattle. J Res Appl Basic Med Sci 2019; 5(2): 111-115.
  10. Jones ML, Allison RW. Evaluation of the ruminant complete blood cell count. Vet Clin North Am Food Anim Pract 2007; 23(3): 377-402.
  11. Gurram RK, Zhu J. Orchestration between ILC2s and Th2 cells in shaping type 2 immune responses. Cell Mol Immunol 2019; 16(3): 225-235.
  12. Klose CSN, Artis D. Innate lymphoid cells as regulators of immunity, inflammation and tissue homeostasis. Nat Immunol 2016; 17: 765-774.
  13. Alborzi AR, Hosseini M, Bahrami S, et al. Evaluation of complement and lysozyme activity and determination of antibody titers in the sera of Linguatula serrata -infected intermediate hosts by indirect hemagglutination [Persian]. Vet Res Biol Prod (Pajouhesh-va-Sazandegi) 2022; 35(2): 49-56.
  14. Koroliuk MA, Ivanova LI, Maĭorova IG, et al. A method of determining catalase activity [Russian]. Lab Delo. 1988; 1: 16-19.
  15. Mihara M, Uchiyama M. Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem 1978; 86(1): 271-278.
  16. Forlenza M, Kaiser T, Savelkoul HF, et al. The use of real-time quantitative PCR for the analysis of cytokine mRNA levels. Methods Mol Biol 2012; 820: 7-23.
  17. Madu AJ, Ughasoro MD. Anaemia of chronic disease: An in-depth review. Med Princ Pract 2017; 26(1): 1-9.
  18. Nemeth E, Ganz T. The role of hepcidin in iron metabolism. Acta Haematol 2009; 122(2-3): 78-86.
  19. Shomali W, Gotlib J. World Health Organization-defined eosinophilic disorders: 2019 update on diagnosis, risk stratification, and management. Am J Hematol 2019; 94(10): 1149-1167.
  20. Cojocariu IE, Bahnea R, Luca C, et al. Clinical and biological features of adult toxocariasis. Rev Med Chir Soc Med Nat Iasi 2012; 116(4): 1162-1165.
  21. Kovalszki A, Weller PF. Eosinophilia. Prim Care 2016; 43(4): 607-617.
  22. Dede S, Değer Y, Kahraman T, et al. Oxidation products of nitric oxide and the concentrations of antioxidant vitamins in parasitized goats. Acta Vet Brno 2002; 71: 341-345.
  23. Abd Ellah MR. Involvement of free radicals in parasitic infestations. J Appl Anim Res 2013; 41(1): 69-76.
  24. Popova MP, Popov CS. Damage to subcellular structures evoked by lipid peroxidation. Z Naturforsch C J Biosci 2002; 57(3-4): 361-365.
  25. Bouchery T, Kyle R, Camberis M, et al. ILC2s and T cells cooperate to ensure maintenance of M2 macrophages for lung immunity against hookworms. Nat Commun 2015; 6: 6970. doi: 10.1038/ncomms7970.
  26. Rajavelu P, Das SD. Th2-type immune response observed in healthy individuals to sonicate antigen prepared from the most prevalent Mycobacterium tuberculosis strain with single copy of IS6110. FEMS Immunol Med Microbiol 2005; 45(1): 95-102.
  27. Couper KN, Blount DG, Riley EM. IL-10: the master regulator of immunity to infection. J Immunol 2008; 180(9): 5771-5777.
  28. Muñoz-Carrillo JL, Contreras-Cordero JF, Gutiérrez-Coronado O, et al. Cytokine profiling plays a crucial role in activating immune system to clear infectious pathogens. In: Immune response activation and immunomodulation. Tyagi K, Bisen P (Eds). London, UK: Intech Open 2018; 1-30.