Molecular Diagnosis and Pathological Study of Toxoplasma gondii in Aborted Caprine and Ovine Fetuses in Borderline of Iran–Iraq

Abstract

Background

Infection with the protozoan parasite Toxoplasma gondii is widely prevalent in animals and humans. In goats and sheep this infection has a high economic impact as it causes abortions and lamb losses. Although there are several studies reporting seroprevalence in small ruminants in Iran, molecular-based information is scarce.

Purpose

This study aimed to screen caprine and ovine aborted fetuses for T. gondii infection by PCR and histopathology.

Methods

Brains of 121 aborted fetuses (10 caprine and 111 ovine) were collected from different parts of the Kordestan province, bordering with Iraq. Gestational age and the general status of each fetus such as freshness, autolysis, mummification and presence of macroscopic lesions in the fetus and foetal membranes was recorded. Individual brain tissues of fetuses were subjected to nested-PCR targeting the B1 gene, and histopathological sections prepared from brains were examined microscopically.

Results

PCR results revealed T. gondii-associated abortion in one caprine and nine ovine fetuses (8.3%). Microscopically, pathological lesions included non-purulent meningitis associated with gliosis, focal necrosis, and occasionally tissue cyst.

Conclusion

This paper reports for the first time T. gondii-associated abortion in goats in Iran. As organs from aborted fetuses do not necessarily show lesions, molecular confirmation is the unique diagnostic method and should be used in situations of an abortion epidemic.

This is a preview of subscription content, access via your institution.

Fig. 1

References

  1. 1.

    Djurković-Djaković O, Dupouy-Camet J, Van der Giessen J, Dubey JP (2019) Toxoplasmosis: overview from a one health perspective. Food Waterborne Parasitol 12:e00054

    Article  Google Scholar 

  2. 2.

    Montoya J, Liesenfeld O (2004) Toxoplasmosis. Lancet 363:1965–1976

    CAS  Article  Google Scholar 

  3. 3.

    Dubey J (2009) Toxoplasmosis in sheep—the last 20 years. Vet Parasitol 163(1–2):1–14

    CAS  Article  Google Scholar 

  4. 4.

    Dubey J (1987) Toxoplasmosis in goats. Agri-Pract 8(3):43–52

    Google Scholar 

  5. 5.

    Fthenakis G, Papadopoulos E (2018) Impact of parasitism in goat production. Small Ruminant Res 163:21–23

    Article  Google Scholar 

  6. 6.

    Giadinis ND, Lafi SQ, Ioannidou E, Papadopoulos E, Terpsidis K, Karanikolas G, Petridou EJ, Brozos C, Karatzias H (2013) Reduction of the abortion rate due to Toxoplasma in 3 goat herds following administration of sulfadimidine. Can Vet J 54(11):1080–1082

    PubMed  PubMed Central  Google Scholar 

  7. 7.

    Moeller RB Jr (2001) Causes of caprine abortion: diagnostic assessment of 211 cases (1991–1998). J Vet Diagn Invest 13(3):265–270

    Article  Google Scholar 

  8. 8.

    Stelzer S, Basso W, Silván JB, Ortega-Mora L, Maksimov P, Gethmann J, Conraths F, Schares G (2019) Toxoplasma gondii infection and toxoplasmosis in farm animals: risk factors and economic impact. Food Waterborne Parasitol e00037

  9. 9.

    Lopes WDZ, Rodriguez JDA, Souza FA, dos Santos TR, dos Santos RS, Rosanese WM, Lopes WRZ, Sakamoto CA, da Costa AJ (2013) Sexual transmission of Toxoplasma gondii in sheep. Vet Parasitol 195(1–2):47–56

    Article  Google Scholar 

  10. 10.

    Santana LF, Rossi GAM, Gaspar RC, Pinto VMR, de Oliveira GP, da Costa AJ (2013) Evidence of sexual transmission of Toxoplasma gondii in goats. Small Rumin Res 115(1–3):130–133

    Article  Google Scholar 

  11. 11.

    Dubey JP (2010) Toxoplasmosis of animals and humans. CRC Press, Boca Raton

    Google Scholar 

  12. 12.

    Sharif M, Sarvi S, Shokri A, Teshnizi SH, Rahimi M, Mizani A, Ahmadpour E, Daryani A (2015) Toxoplasma gondii infection among sheep and goats in Iran: a systematic review and meta-analysis. Parasitol Res 114(1):1–16

    CAS  Article  Google Scholar 

  13. 13.

    Daryani A, Sarvi S, Aarabi M, Mizani A, Ahmadpour E, Shokri A, Rahimi M-T, Sharif M (2014) Seroprevalence of Toxoplasma gondii in the Iranian general population: a systematic review and meta-analysis. Acta Trop 137:185–194

    Article  Google Scholar 

  14. 14.

    Rahimi MT, Daryani A, Sarvi S, Shokri A, Ahmadpour E, Teshnizi SH, Mizani A, Sharif M (2015) Cats and Toxoplasma gondii: a systematic review and meta-analysis in Iran. Onderstepoort J Vet Res 82(1):01–10

    Article  Google Scholar 

  15. 15.

    Sarvi S, Daryani A, Rahimi MT, Aarabi M, Shokri A, Ahmadpour E, Mizani A, Sharif M (2015) Cattle toxoplasmosis in Iran: a systematic review and meta-analysis. Asian Pac J Trop Med 8(2):120–126

    Article  Google Scholar 

  16. 16.

    Sazmand A, Joachim A (2017) Parasitic diseases of camels in Iran (1931–2017)—a literature review. Parasite 24:21

    Article  Google Scholar 

  17. 17.

    Khademvatan S, Foroutan M, Hazrati-Tappeh K, Dalvand S, Khalkhali H, Masoumifard S, Hedayati-Rad F (2017) Toxoplasmosis in rodents: a systematic review and meta-analysis in Iran. J Infect Public Health 10(5):487–493

    Article  Google Scholar 

  18. 18.

    Shokri A, Sharif M, Teshnizi SH, Sarvi S, Rahimi MT, Mizani A, Ahmadpour E, Montazeri M, Daryani A (2017) Birds and poultries toxoplasmosis in Iran: a systematic review and meta-analysis. Asian Pac J Trop Med 10(7):635–642

    Article  Google Scholar 

  19. 19.

    Rassouli M, Razmi G, Bassami M, Movassaghi A, Azizzadeh M (2011) Study on ovine abortion associated with Toxoplasma gondii in affected herds of Khorasan Razavi Province, Iran based on PCR detection of fetal brains and maternal serology. Parasitology 138(6):691–697

    CAS  Article  Google Scholar 

  20. 20.

    Habibi G, Imani A, Gholami M, Hablolvarid M, Behroozikhah A, Lotfi M, Kamalzade M, Najjar E, Esmaeil-Nia K, Bozorgi S (2012) Detection and identification of Toxoplasma gondii type one infection in sheep aborted fetuses in Qazvin Province of Iran. Iran J Parasitol 7(3):64–72

    PubMed  PubMed Central  Google Scholar 

  21. 21.

    Danehchin L, Razmi G, Naghibi A (2016) Isolation and genotyping of Toxoplasma gondii strains in ovine aborted fetuses in Khorasan Razavi Province, Iran. Kor J Parasitol 54(1):15–20

    CAS  Article  Google Scholar 

  22. 22.

    Nourmohammadi M, Hamidinejat H, Tabandeh M, Goraninejad S, Bahrami S (2017) Genotyping of zoonotic Toxoplasm gondii isolated from aborted fetuses of ewes of Lorestan Province based on SAG2، SAG3 and GRA6 molecular markers. J Ardabil Univ Med Sci 17(3):343–352 (Article in Persian with English abstract)

  23. 23.

    Burg JL, Grover CM, Pouletty P, Boothroyd J (1989) Direct and sensitive detection of a pathogenic protozoan, Toxoplasma gondii, by polymerase chain reaction. J Clin Microbiol 27(8):1787–1792

    CAS  Article  Google Scholar 

  24. 24.

    Abdulla SH, Al-Taie LH (2011) Seroprevalance of toxoplasmosis in sheep and goat: Iraq/Sulaimania. Iraqi J Vet Med 35(1):16–24

    Google Scholar 

  25. 25.

    Dubey JP (2010) Toxoplasmosis in goats (Capra hircus). In: Dubey JP (ed) Toxoplasmosis of animals and humans, 2nd edn. CRC Press, New York, pp 137–144

    Google Scholar 

  26. 26.

    de Freitas Silva Filho M, Erzinger É, da Cunha IAL, Bugni FM, Hamada FN, Marana ERM, Freire RL, Garcia JL, Navarro IT (2008) Toxoplasma gondii: abortion outbreak in a goatherd from Southern Brazil. Semina: Ciências Agrárias 29(4):887–894

  27. 27.

    Sreekumar C, Rao J, Mishra A, Ray D, Joshi P, Singh R (2004) Detection of toxoplasmosis in experimentally infected goats by PCR. Vet Rec 154(20):632–635

    CAS  Article  Google Scholar 

  28. 28.

    Shahmoradi A, Rezaeian M, Dali Asl A (1993) Sheep-an important reservoir of human toxoplasmosis in Iran. Med J Islam Republic Iran 7(3):173–174

    Google Scholar 

  29. 29.

    Khezri M, Mohammadian B, Esmailnia K, Khezri O (2012) Toxoplasmosis in sheep from Kurdistan province, Iran. Afr J Microbiol Res 6(18):3989–3992

    Article  Google Scholar 

  30. 30.

    Zia-Ali N, Fazaeli A, Khoramizadeh M, Ajzenberg D, Dardé M, Keshavarz-Valian H (2007) Isolation and molecular characterization of Toxoplasma gondii strains from different hosts in Iran. Parasitol Res 101(1):111–115

    CAS  Article  Google Scholar 

  31. 31.

    Armand B, Solhjoo K, Kordshooli MS, Davami MH, Pourahmad M, Orfaee V (2017) Toxoplasma gondii type I, predominant genotype isolated from sheep in South of Iran. Vet World 10(4):386–392

    CAS  Article  Google Scholar 

  32. 32.

    Razmi GR, Ghezi K, Mahooti A, Naseri Z (2010) A serological study and subsequent isolation of Toxoplasma gondii from aborted ovine fetuses in Mashhad area, Iran. J Parasitol 96(4):812–814

    CAS  Article  Google Scholar 

  33. 33.

    Rassouli M, Razmi GR, Movassaghi AR, Bassami MR, Sami M (2013) Pathological description and immunohistochemical demonstration of ovine abortion associated with Toxoplasma gondii in Iran. Kor J Vet Res 53(1):1–5

    Article  Google Scholar 

  34. 34.

    Abu-Dalbouh MA, Ababneh MM, Giadinis ND, Lafi SQ (2012) Ovine and caprine toxoplasmosis (Toxoplasma gondii) in aborted animals in Jordanian goat and sheep flocks. Trop Anim Health Prod 44(1):49–54

    Article  Google Scholar 

  35. 35.

    Moreno B, Collantes-Fernández E, Villa A, Navarro A, Regidor-Cerrillo J, Ortega-Mora L (2012) Occurrence of Neospora caninum and Toxoplasma gondii infections in ovine and caprine abortions. Vet Parasitol 187(1–2):312–318

    CAS  Article  Google Scholar 

  36. 36.

    Hill D, Dubey JP (2002) Toxoplasma gondii: transmission, diagnosis and prevention. Clin Microbiol Infect 8(10):634–640

    CAS  Article  Google Scholar 

Download references

Acknowledgements

This study was partially supported by Bu-Ali Sina University of Hamedan, Iran. The authors wish to thank Sakineh Azami for her kind assistance in the laboratory, and Dr. Ali Sadeghinasab for his help in statistical analyses.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Zainab Sadeghi-Dehkordi.

Ethics declarations

Conflict of interest

The 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

Verify currency and authenticity via CrossMark

Cite this article

Partoandazanpoor, A., Sadeghi-Dehkordi, Z., Ekradi, L. et al. Molecular Diagnosis and Pathological Study of Toxoplasma gondii in Aborted Caprine and Ovine Fetuses in Borderline of Iran–Iraq. Acta Parasit. 65, 187–192 (2020). https://doi.org/10.2478/s11686-019-00147-4

Download citation

Keywords

  • Toxoplasmosis
  • Zoonosis
  • Parasitic infection
  • Small ruminants
  • PCR
  • Histopathology