SpringerLink
Log in

Evaluation of tumor necrosis factor-alpha (TNF-α); gamma interferon (IFN-γ) genes and oxidative stress in sheep: immunological responses induced by Oestrus ovis (Diptera: Oestridae) infestation

  • Original Article
  • Published:
Journal of Parasitic Diseases Aims and scope Submit manuscript

Abstract

This study aimed to evaluate the cell mediated immune responses against Oestrus ovis (O. ovis) in sheep through measurement of the changes in mRNA expression of the tumor necrosis factor alpha (TNF-α) and gamma interferon (IFN-γ) cytokines using quantitative Real time-PCR (qRt-PCR). Also; to detect the role of Oestrus ovis infestation in the oxidative stress markers in sheep. Fifty sheep head were examined in Cairo abattoir from the period of May to August 2019. Sera were separated and collected for measurement of nitric oxide, zinc and malondialdehyde (MDA). While TNF-α and IFN-γ mRNA were extracted from nasal mucosa. Levels of IFN-γ and TNF-α were significantly higher in infested sheep than that in non-infested one. Also, oxidative stresses were indicated by high level of nitric oxide as one of reactive oxygen species (ROS) and serum MDA as oxidative stress marker and low antioxidant capacity (zinc concentration in serum) in infested sheep. The obtained results indicated that measurements of TNF-α and IFN-γ cytokines using qRT-PCR could be used as an association and reproducible quantitative method for the diagnosis of O. ovis infestation in sheep.

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

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ahaduzzaman M (2019) The global and regional prevalence of oestrosis in sheep and goats: a systematic review of articles and meta-analysis. Parasit Vectors 12(1):346

    PubMed  PubMed Central  Google Scholar 

  • Aktas MS, Kandemir FM, Kirbas A, Hanedan B, Aydin MA (2017) Evaluation of oxidative stress in sheep infected with Psoroptes Ovis using total antioxidant capacity, total oxidant status, and malondialdehyde level. J. Vet. Res. 61(2):197–201

    CAS  PubMed  PubMed Central  Google Scholar 

  • Alcaide M, Reina D, Sánchez J, Frontera E, Navarrete I (2003) Seasonal variations in the larval burden distribution of Oestrus ovis in sheep in the southwest of Spain Vet. Parasitol 30(8):235–241

    Google Scholar 

  • Alcaide M, Reina D, Sánchez-López J, Frontera E, Navarrete I (2005) Seroprevalence of Oestrus ovis (Diptera, Oestridae) infestation and associated risk factors in ovine livestock from southwestern Spain. J Med Entomol 42(3):327–331

    PubMed  Google Scholar 

  • Amin AR, Morsy TA, Shoukry A, Mazyad SA (1997) Oestrid head maggots in slaughtered sheep in Cairo abattoir. J Egypt Soc Parasitol 27:855–861

    CAS  PubMed  Google Scholar 

  • Angulo-Valadez CE, Ascencio F, Jacquiet P, Dorchies P, Cepeda-Palacios R (2011) Sheep and goat immune responses to nose bot infestation: a review. Med Vet Entomol 25(2):117–125

    CAS  PubMed  Google Scholar 

  • Attia MM, Soliman SM, Salaeh NMK (2019) Advanced and rapid serodiagnosis of oestrosis (Oestrus ovis; Diptera: Oestridae) in sheep using indirect and Dot-ELISA. Jordan J Biol Sci 12(3):275–281

    CAS  Google Scholar 

  • Aytekin I, Unubol Aypak S (2011) Levels of selected minerals, nitric oxide, and vitamins in aborted Sakis sheep raised under semitropical conditions. Trop Anim Health Prod 43:511–514

    PubMed  Google Scholar 

  • Boddu-Jasmine HC, Witchell J, Vordermeier M, Wangoo A, Goyal M (2008) Cytokine mRNA expression in cattle infected with different dosages of Mycobacterium bovis. Tuberculosis (Edinb). 88(6):610–615

    CAS  PubMed  Google Scholar 

  • Caracappa S, Rilli S, Zanghi P, Di Marco V, Dorchies Ph (2000) Epidemiology of ovine oestrosis (Oestrus ovis Linné 1761, Diptera: Oestridae) in Sicily. Vet Parasitol 92:233–237

    CAS  PubMed  Google Scholar 

  • Channappanavar R, Singh KP, Singh R, Umeshappa CS, Ingale SL, Pandey AB (2012) Enhanced proinflammatory cytokine activity during experimental bluetongue virus-1 infection in Indian native sheep. Vet Immunol Immunopathol 145(1–2):485–492

    CAS  PubMed  Google Scholar 

  • Coussens PM, Verman N, Coussens MA, Elftman MD, McNulty AM (2004) Cytokine gene expression in peripheral blood mononuclear cells and tissues of cattle infected with mycobacterium avium subsp. paratuberculosis: evidence for an inherent proinflammatory gene expression pattern. Infect Immun 72(3):1409–1422

    CAS  PubMed  PubMed Central  Google Scholar 

  • Donahoe SL, Phalen DN, McAllan BM, O’Meally D, McAllister MM, Ellis J, Šlapeta J (2017) Differential gamma interferon- and tumor necrosis factor alpha-driven cytokine response distinguishes acute infection of a metatherian host with Toxoplasma gondii and Neospora caninum. Infect Immun 85(6):e00173

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dubey JP, Schares G (2011) Neosporosis in animals—the last five years. Vet Parasitol 180:90–108

    CAS  PubMed  Google Scholar 

  • El-Tahawy AS (2010) The prevalence of selected diseases and syndromes affecting Barki sheep with special emphasis on their economic impact. Small Rumin Res 90:83–87

    Google Scholar 

  • Gaaboub LA (1978) The distribution and seasonal dynamics of Oestrus ovis Linne infesting nasal cavities and sinuses of sheep in Egypt. Vet. Parasiotl 4(1):79–82

    Google Scholar 

  • Giulietti A, Overbergh L, Valckx D, Decallonne B, Bouillon R, Mathieu C (2001) An overview of real-time quantitative PCR: applications to quantify cytokine gene expression. Methods 25(4):386–401

    CAS  PubMed  Google Scholar 

  • Hassanin MA, Abdel-Gawad AM, Ramadan EI (1989) Incidence, monthly prevalence and bionomics of Oestrus ovis infesting sheep in Egypt. J Egypt Vet Med Assoc 49:431–443

    Google Scholar 

  • Heidarpour M, Mohri M, Borji H, Moghdass E (2013) Oxidant/antioxidant status in cattle with liver cystic echinococcosis. Vet Parasitol 195(1–2):131–135

    CAS  PubMed  Google Scholar 

  • Hidalgo A, Palma H, Oberg C, Fonseca-Salamanca F (2015) Oestrus ovis infection of grazing sheep during summer in southern Chile. Pesq. Vet. Bras. 35(6):497–500

    Google Scholar 

  • Kolodziejczyk L, Siemieniuk E, Skrzydlewska E (2005) Antioxidant potential of rat liver in experi-mental infection with Fasciola hepatica. Parasitol Res 96(6):367–372

    CAS  PubMed  Google Scholar 

  • Lacey N, Russell-Hallinan A, Zouboulis CC, Powell FC (2018) Demodex mites modulate sebocyte immune reaction: possible role in the pathogenesis of rosacea. BJD 179:252–253

    Google Scholar 

  • Mosmann TR, Coffman RL (1989) TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu Rev Immunol 7:145–173

    CAS  PubMed  Google Scholar 

  • Munoz C, Rios E, Olivos J, Brunser O, Oli-vares M (2007) Iron, copper and immunocompetence. Br J Nutr 98(Suppl 1):S24–S28

    CAS  PubMed  Google Scholar 

  • Nasr A, Allam G, Hamid O, Al-Ghamdi A (2014) IFN-gamma and TNF associated with severe falciparum malaria infection in Saudi pregnant women. Malar J. 13:314

    PubMed  PubMed Central  Google Scholar 

  • Page CM, Murphy TW, Van Emon ML, Bowman JGP, Wyffels SA, Stewart WC (2018) Blood serum mineral element concentrations of weaned Montana ram lambs and their relationship with water quality characteristics. Prof Anim Sci 34(5):410–420

    Google Scholar 

  • Picard-Sánchez A, Estensoro I, Del Pozo R, Piazzon MC, Palenzuela O, Sitjà-Bobadilla A (2019) Acquired protective immune response in a fish-myxozoan model encompasses specific antibodies and inflammation resolution. Fish Shellfish Immunol 90:349–362

    PubMed  Google Scholar 

  • Puech C, Dedieu L, Chantal I, Rodrigues V (2015) Design and evaluation of a unique SYBR Green real-time RT-PCR assay for quantification of five major cytokines in cattle, sheep and goats. BMC. Vet. Res. 11:65

    PubMed  PubMed Central  Google Scholar 

  • Ramadan MY, Khater HF, Omer SF, Abdel Rahman A (2013) Epidemiology of Oestrus ovis infesting Egyptian sheep. In: International congress of mediterranean federation of health and production of ruminants, pp 19–22

  • Saleh MA (2008) Circulating oxidative stress status in desert sheep naturally infected with Fasciola hepatica. Vet Parasitol 154(3–4):262–269

    CAS  PubMed  Google Scholar 

  • Samadieh H, Mohammadi GR, Maleki M, Borji H, Azizzadeh M, Heidarpour M (2017) Relationships between oxidative stress, liver, and erythrocyte injury, trace elements and parasite burden in sheep naturally infected with Dicrocoelium dendriticum. Iran J. Parasitol 12(1):46–55

    PubMed  PubMed Central  Google Scholar 

  • Sandeman RM (1996) Immune responses to mosquitoes and flies. In: Wikel SK (ed) The immunology of host-ectoparasitic arthropod relationship. CAB International, Wallingford, pp 175–203

    Google Scholar 

  • Scala A, Solinas G, Citterio CV, Kramer LH, Genchi C (2001) Sheep oestrosis (Oestrus ovis Linné 1761, Diptera: Oestridae) in Sardinia, Italy. Vet Parasitol 102(1–2):133–141

    CAS  PubMed  Google Scholar 

  • Silva BF, Bassetto CC, Amarante AF (2012) Immune responses in sheep naturally infected with Oestrus ovis (Diptera: Oestridae) and gastrointestinal nematodes. Vet Parasitol 190(1–2):120–126

    CAS  PubMed  Google Scholar 

  • Şimşek S, Yüce A, Ütük AE (2006) Determination of serum malondialdehyde levels in sheep naturally infected with Dicrocoelium dendriticum. F. U. Saglık Bil. Dergisi. 20(3):217–220

    Google Scholar 

  • Singh PK, Singh SV, Saxena VK, Singh MK, Singh AV, Sohal JS (2013) Expression profiles of different cytokine genes in peripheral blood mononuclear cells of goats infected experimentally with native strain of Mycobacterium avium subsp. paratuberculosis. Biotechnol 24(3):187–197

    CAS  Google Scholar 

  • Smeed JA, Watkins CA, Rhind SM, Hopkins J (2007) Differential cytokine gene expression profiles in the three pathological forms of sheep paratuberculosis. BMC Vet Res. 3:18

    PubMed  PubMed Central  Google Scholar 

  • Soulsby EJL (1986) Helminths, Arthropods & Protozoa of Domesticated Animals, 7th edn. Bailliere Tindall, London

    Google Scholar 

  • Tabouret G, Bret-Bennis L, Dorchies P, Jacquiet P (2003) Serine protease activity in excretory-secretory products of Oestrus ovis (Diptera: Oestridae) larvae. Vet Parasitol 114:305–314

    CAS  PubMed  Google Scholar 

  • Uner N, Oruç EO, Canli M, Sevgile Y (2001) Effects of cypermethrin on antioxidant enzyme activities and lipid peroxidation in liver and kidney of the freshwater fish. Oreochromis niloticus and Cyprinus carpio (L.). Bull Environ Contam Toxicol 67(5):657–664

    CAS  PubMed  Google Scholar 

  • Zumpt F (1965) Myiasis in man and animals in the old world. Butterworth, London

    Google Scholar 

Download references

Funding

No funding supporting this work.

Author information

Authors and Affiliations

  1. Parasitology Department, Faculty of Veterinary Medicine, Cairo University, Giza, 12211, Egypt

    Marwa M. Attia & Sohila M. El-Gameel

  2. Department of Veterinary Hygiene and Management, Faculty of Veterinary Medicine, Cairo University, Giza, 12211, Egypt

    Elshaimaa Ismael

Authors
  1. Marwa M. Attia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sohila M. El-Gameel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Elshaimaa Ismael
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors sharing in the aim of works; Marwa M. Attia: collect the samples and identify the clinical sign on the sheep; Marwa M. Attia and Sohila M. El-Gameel Identify the parasites; applying the clinical works; Elshaimaa Ismael applying of statistical analysis of the results. All authors sharing in writing and revised this manuscript.

Corresponding author

Correspondence to Marwa M. Attia.

Ethics declarations

Conflict of interest

All authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Attia, M.M., El-Gameel, S.M. & Ismael, E. Evaluation of tumor necrosis factor-alpha (TNF-α); gamma interferon (IFN-γ) genes and oxidative stress in sheep: immunological responses induced by Oestrus ovis (Diptera: Oestridae) infestation. J Parasit Dis 44, 332–337 (2020). https://doi.org/10.1007/s12639-020-01220-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12639-020-01220-w

Keywords

Search

Navigation