Parasitology Research

, Volume 118, Issue 1, pp 307–316 | Cite as

Seroprevalence of Toxoplasma gondii in one-humped camels (Camelus dromedarius) of Thal and Cholistan deserts, Punjab, Pakistan

  • Tabassam Fatima
  • Saba Mehnaz
  • Min Wang
  • Jichao Yang
  • Muhammad Sohail Sajid
  • Bang Shen
  • Junlong ZhaoEmail author
Protozoology - Original Paper


Toxoplasma (T.) gondii is an important zoonotic protozoan infecting humans and a wide range of animals. In this study, we determine the seroprevalence and risk factors associated with the seroprevalence of T. gondii in one-humped camels (Camelus dromedarius) in Pakistan. Camels are still an important mean of transportation in some desert areas in Pakistan. In addition, they are the main source of meat and milk for people in those regions; therefore, they have the potential to transmit T. gondii to humans. In order to estimate the seroprevalence of T. gondii, a total of 897 sera samples were collected from camels in the Thal (n = 359) and Cholistan (n = 440) deserts, along with other districts of Chakwal (n = 44) and Faisalabad (n = 54) Punjab, Pakistan, through convenient and snowball sampling techniques. These samples were then analyzed by an indirect enzyme-linked immune-sorbent assay (ELISA) for the presence of T. gondii-specific antibodies, using purified recombinant micronemal protein 3 (MIC3) as an antibody-catching antigen. Our results showed an overall seroprevalence of T. gondii as 40.1% (Thal = 45%; Cholistan = 35.9%; other districts = 33.7%). Risk factor analysis suggested that infection rate was higher in older animals (70.6%). In addition, female camels carried frequent infection (48.8%) than males (22.4%). What’s more, female animals having abortion history showed even higher infection rate (75%) compared to pregnant (68.4%) and non-pregnant (42.4%) animals. Our results reported high seroprevelance of T. gondii in camels in Pakistan which provided important information with respect to public health and disease controls.


Seroepidemiology Toxoplasma gondii Camel (Camelus dromedariesIndirect ELISA Pakistan 



Author would like to thanks Dr. Sohail Manzoor (Disease Investigation and Control Officer), Dr. Ramzan-ul-Haq (Veterinary Officer), Dr. Awais Masud (Assistant Disease Investigation Officer), Dr. Abdul Rehman (Deputy District Livestock Officer) and field staff who helped in sample collection.


This work was supported by the Natural Science Foundation of Hubei Province (Project 2017CFA020).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Abu-Zeid Y (2002) Protein G ELISA for detection of antibodies against Toxoplasma SAGI in dromedaries. J Egypt Soc Parasitol 32:247–257Google Scholar
  2. Akram A, Wallyat AK and Bashir AS (1986) Desertification processes in Cholistan Desert, Technical Report, Pakistan Council of Research in Water Resources, (PCRWR) PP 5-16Google Scholar
  3. Al-Anazi AD (2011) Prevalence of Neospora caninum and Toxoplasma gondii antibodies in sera from camels (Camelus dromedarius) in Riyadh Province, Saudi Arabia. J Egypt Soc Parasitol 41:245–250Google Scholar
  4. Al-Anazi AD (2012) Antibodies in sera from camels (Camelus dromedarius) in western and southern regions of central province, Saudi Arabia. J Egypt Soc Parasitol 3:659–664Google Scholar
  5. Assmar M, Amirkhani A, Piazak N, Hovanesian A, Kooloobandi A, Etessami R (1997) Toxoplasmosis in Iran. Results of a seroepidemiological study. Bull Soc Pathol Exot 90:19–21Google Scholar
  6. Breulmann M, Boer B, Wernery U, Wernery R and El-Shaer H, et al (2007) A proposal towards combating desertification via establishment of camel farms based on fodder production from indigenous plants and halophytes. UNESCO-Doha, UAE, pp: 14Google Scholar
  7. Butler AB and William H (2005) Comparative vertebrate neuro anatomy: evolution and adaptation. Jhon Wiley and Sons PP: 215Google Scholar
  8. Cain JW, Krusman NPR, Turner JC (2006) Mechanisms of thermoregulation and water balance in desert ungulates. Wildl Soc Bull 34:570–581Google Scholar
  9. Cantos G, Prando MD, Siqueira MV, Teixeira RM (2000) Toxoplasmosis: occurrence of antibodies to Toxoplasma gondii and diagnosis. Rev Ass Med Bras 46:335–341Google Scholar
  10. Chaudhary UN, Ali AA, Ashraf S et al (2014) Seroprevalence of Toxoplasma gondii infection in camel (Camelus dromedarius) in and around Bahawalpur region of Pakistan. JIMB 2:16–18Google Scholar
  11. Chen XG, Tan F (2009) Toxoplasma gondii: past, present and future. Records 27:426–431Google Scholar
  12. Dehkordi FS, Rahimi E, Abdizadih R (2013) Detection of Toxoplasma gondii in raw caprine, ovine, buffalo, bovine and camel milk using cell cultivation, cat bioassay, capture ELISA and PCR methods in Iran. Foodborne Pathog Dis 10:120–125CrossRefGoogle Scholar
  13. Dereje M, Ud’en P (2005) The browsing dromedary camel. Behaviour, plant preference and quality of forage selected. Anim Feed Sci Technol 121:297–308CrossRefGoogle Scholar
  14. Dubey JP (1991) Toxoplasmosis: an overview. Southeast Asian J Trop Med Public Health 22:88–92Google Scholar
  15. Dubey JP (1998) Toxoplasmosis, sarcocystosis, isosporosis, and cyclosporosis. In: Palmer SR, Soulsby EJL, Simpson DJH (eds) Zoonoses. Oxford University Press, Oxford, pp 579–597Google Scholar
  16. Dubey JP (1999) Advances in the life cycle of Toxoplasma gondii. Int J Parasitol 28:1019–1024CrossRefGoogle Scholar
  17. Dubey JP (2010a) Toxoplasma gondii infections in chickens (Gallus domesticus): prevalence, clinical disease, diagnosis and public health significance. Zoonoses Public Health 57:60–73CrossRefGoogle Scholar
  18. Dubey JP (2010b) Toxoplasmosis of animals and humans. 2nd edition, CRC PressGoogle Scholar
  19. Elamin EA, Elias S, Daugschies A, Rommel M (1992) Prevalence of Toxoplasma gondii antibodies in pastoral camels (Camelus dromedarius) in the Butana plains, mid-eastern Sudan. Vet Parasitol 43:171–175CrossRefGoogle Scholar
  20. Ferrandiz J, Mercier C, Wallon M, Picot S, Cesbron-Delauw MF, Peyron F (2004) Limited value of assays using detection of immunoglobulin G antibodies to the two recombinant dense granule antigens, GRA1 and GRA6 Nt of Toxoplasma gondii, for distinguishing between acute and chronic infections in pregnant women. Clin Diagn Lab Immunol 11:1016–1021Google Scholar
  21. Garcia-Reguet N, Lebrun M, Fourmaux MN, Mercereau-Puijalon O, Mann T, Beckers CJM, Samyn B, van Beeumen J, Bout D, Dubremetz JF (2000) The microneme protein MIC3 of Toxoplasma gondii is a secretory adhesin that binds to both the surface of the host cells and the surface of the parasite. Cell Microbiol 2:353–364CrossRefGoogle Scholar
  22. Gaughan JB (2011) Which physiological adaptation allows camels to tolerate high heat load and what more can we learn? JCS 4:85–88Google Scholar
  23. Gebremedhin EZ, Yunus HA, Tesfamaryam G, Tessema TS, Dawo F, Terefe G, di Marco V, Vitale M (2014) First report of Toxoplasma gondii in camels (Camelus dromedarius) in Ethiopia: bioassay and seroepidemiological investigation. BMC Vet Res 10:222–234CrossRefGoogle Scholar
  24. Grigg G, Beard L, Dorges B, Heucke J, Coventry J, Coppock A, Blomberg S (2009) Strategic (adaptive) hypothermia in bull dromedary camels during rut; could it increase reproductive success? Biol Lett 5:853–856CrossRefGoogle Scholar
  25. Hussein A (2016) Camels and adaptation to water lack: mirror of research in veterinary sciences and animals (MRVSA) 5 (1st) on camel diseases and management. PP: 64–69Google Scholar
  26. Hussein MF, Bakkar MN, Basmaeil SM (1988) Prevalence of toxoplasmosis in Saudi Arabian camels (Camelus dromedarius). Vet Parasitol 28:175–178CrossRefGoogle Scholar
  27. Janků J (1923) Pathogenesa a pathologická anatomie tak nazvaného vrozeného kolobomu žluté skvrny v oku normálně velikém a mikrophthal-mickéém s nálezem parazitu v sítnici. Čas Lék Česk 39–43:1021–7. 1054–9, 1081–5, 1111–5, 1138–44Google Scholar
  28. Jiang T, Gong D, Ma LA, Nie H, Zhou Y, Yao B, Zhao J (2008) Evaluation of recombinant MIC3 based latex agglutination test for the rapid sero diagnosis of Toxoplasma gondii infection in swine. Vet Parasitol 158:51–55Google Scholar
  29. Kamani J, Mani AU, Egwu GO (2010) Seroprevalence of Toxoplasma gondii infection in domestic sheep and goats in Borno state, Nigeria. Trop Anim Health Prod 42:793–797CrossRefGoogle Scholar
  30. Kataria N, Kataria AK, Agarwal VK, Garg SL, Shana MS (2001a) Changes in glomerular filtration rate and effective renal plasma flow during seasonal water restriction in Indian camel (Camelus dromedarius). J Camel Pract Res 8:215–220Google Scholar
  31. Kataria N, Kataria AK, Agarwal VK, Garg SL, Sahani MS (2001b) Filtered and excreted loads of urea in different climatic conditions and hydration states in dromedary camel. J Camel Pract Res 8:203–207Google Scholar
  32. Khalil MK, Elrayah IE (2011) Seroprevalence of Toxoplasma gondii antibodies in farm animals (camels, cattle, and sheep) in Sudan. J Vet Med Anim Health 3:36–39Google Scholar
  33. Kittas S, Kittas C, Paizi-Biza P, Henry L (1984) A histological and immunohistochemical study of the changes induced in the brains of white mice by infection with Toxoplasma gondii. Br J Exp Pathol 65:67–74Google Scholar
  34. Lopes WD, Santos TR, da Silva R et al (2010) Seroprevalence of and risk factors for Toxoplasma gondii in sheep raised in the Jaboticabal microregion, Sao Paulo State, Brazil. Res Vet Sci 88:104–106CrossRefGoogle Scholar
  35. Manal YI, Maijd AM (2008) Association of diarrhea with congenital toxoplasmosis in calf-camel (Camelus dromedarius). Int J Trop Med 3:10–11Google Scholar
  36. Tuck MK, Daniel WC, David C, Andrew KG, William EG, Karl EK, William R, Martin S, Lynn S, Sanford S, Wendy W, Dean EB (2009) J Proteome Res 8:113–117Google Scholar
  37. Montoya JG, Liesenfeld O (2004) Toxoplasmosis. Lancet 363:1965–1976CrossRefGoogle Scholar
  38. Njiru GK (1993) Economics of camel production. In: S.P. Simpkin (Ed.): Camel Production. A series of lectures given by FARM-Africa at Nairobi University, Nairobi, KenyaGoogle Scholar
  39. Ouajd O, Kamel B (2009) Physiological particularities of dromedary (Camelus dromedarius) and experimental implications. Scand J Lab Anim Sci 36:19–29Google Scholar
  40. Pakistan economic survey (2016–2017) Ministry of finance. Govt. of PakistanGoogle Scholar
  41. Pakistan livestock census (2006) Punjab Province. Govt. Pakistan. Stat. Div., Agri. Census OrganizationGoogle Scholar
  42. Pietkiewicz H, Hiszczynska-Sawicka E, Kur J et al (2004) Usefulness of Toxoplasma gondii-specific recombinant antigens in serodiagnosis of human toxoplasmosis. J Clin Microbiol 42:779–781CrossRefGoogle Scholar
  43. Ramzan M, Akhtar M, Muhammad F, Hussain I, Hiszczyńska-Sawicka E, Haq AU, Mahmood MS, Hafeez MA (2009) Seroprevalence of Toxoplasma gondii in sheep and goats in Rahim Yar Khan (Punjab), Pakistan. Trop Anim Health Prod 41:1225–1229CrossRefGoogle Scholar
  44. Randall L, Zarnke S, Dubey JP et al (2000) Seroprevalence for T. gondii in selected wild species from Alaska. J Wildl Dis 36:219–224CrossRefGoogle Scholar
  45. Raziq A (2009) Portrayal of camelids in pastoral economy of north-eastern herders of Baluchistan. PhD Diss., Department of Livestock Management, University of Agriculture Faisalabad, PakistanGoogle Scholar
  46. Schork MA and Remington RD (2010) Statistics with applications to the biological and health sciences. 3rd ed, Lexington, KY, USAGoogle Scholar
  47. Selseleh MM, Keshavarz H, Mohebali M, Shojaee S, Modarressi M, Eshragian M et al (2012) Production and evaluation of Toxoplasma gondii recombinant surface antigen 1 (SAG1) for serodiagnosis of acute and chronic Toxoplasma infection in human sera. Iran J Parasitol 7:1Google Scholar
  48. Shaapan RM, Kahlil FAM (2008) Evaluation of different Toxoplasma gondii isolates as antigens used in the modified agglutination test for the detection of toxoplasmosis in camels and donkeys. Am Eurasian J Agric Environ Sci 3:837–841Google Scholar
  49. Shanmugham R, Thirumeni N, Rao VS, Pitta V, Kasthuri S, Singanallur NB, Lingala R, Mangamoori LN, Villuppanoor SA (2010) Immunocapture enzyme-linked immunosorbent assay for assessment of in vitro potency of recombinant hepatitis B vaccines. Clin Vaccine Immunol 17(8):1252–1260CrossRefGoogle Scholar
  50. Sial N (1989) Fauna of Cholistan Desert (Birds, Mammals, and statistical data of wildlife). Research Report, Published by Cholistan Institute of Desert Studies, Islamia University, BahawalpurGoogle Scholar
  51. Simenew KW (2014) Characterization of Camelus dromedarius in Ethiopia: production system, reproduction performances and infertility: 9Google Scholar
  52. Simenew K, Mekuriaw M, Tesfaye ST, Fekadu R, Wesinew A et al (2013) Reproductive performance of Camelus dromedarius kept under Afar pastoral management system using progeny history testing. J Camelid Sci 6:100–115Google Scholar
  53. Smith JE (1995) Aubiquitous intracellular parasite, the cellular biology of T. gondii. Int J Parasitol 25:1301–1309CrossRefGoogle Scholar
  54. Sohail MA (1983) The role of the Arabian camel (Camelus dromedarius) in animal production. World Rev Anim Prod 19:38–40Google Scholar
  55. Soliman MK (2015) Functional anatomical adaptations of dromedary (Camelus dromedarius) and ecological evolutionary impacts in KSA. International Conference on Plant, Marine and Environmental Sciences, Kuala Lumpur, MalaysiaGoogle Scholar
  56. Souilem O, Djegham M (1994) La digestion gastriquechez le dromadaire (Camelus dromedarius). Rec Méd Vét 172:199–208Google Scholar
  57. Tenter AM (2009) Toxoplasma gondii in animals used for human consumption. Instituto Oswaldo Cruz, Ministério da Saúde 104:364–369Google Scholar
  58. Thrusfield M (2007) Veterinary epidemiology, 3rd edn. Black Well Science Publishers, Oxford, p 195Google Scholar
  59. Utuk AE, Kirbas A, Babur C, Balkaya I (2012) Detection of Toxoplasma gondii antibodies and some helminthic parasites in camels from Nevsehir province of Turkey. Isr J Vet Med 67:106–108Google Scholar
  60. van der Puije WN, Bosompem KM, Canacoo EA et al (2000) The prevalence of anti-Toxoplasma gondii antibodies in Ghanaian sheep and goats. Acta Trop 76:21–26CrossRefGoogle Scholar
  61. Wang CR, Qiu JH, Gao JF, Liu LM, Wang C, Liu Q, Yan C, Zhu XQ (2011) Seroprevalence of Toxoplasma gondii infection in sheep and goats in northeastern China. Small Rumin Res 97:130–133CrossRefGoogle Scholar
  62. Willmer P, Ston G, Johnston I (2006) Environmental physiology of animals, 2nd edn. Blackwell Publishing, MaldenGoogle Scholar
  63. Xiao Y, Yin J, Jiang N, Xiang M, Hao L, Lu H, Sang H, Liu X, Xu H, Ankarklev J, Lindh J, Chen Q (2010) Seroepidemiology of human Toxoplasma gondii infection in China. BMC Infect Dis 10:4CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Tabassam Fatima
    • 1
  • Saba Mehnaz
    • 2
  • Min Wang
    • 1
  • Jichao Yang
    • 1
  • Muhammad Sohail Sajid
    • 2
  • Bang Shen
    • 1
    • 3
  • Junlong Zhao
    • 1
    • 3
    • 4
    Email author
  1. 1.State Key Laboratory of Agricultural Microbiology, College of Veterinary MedicineHuazhong Agricultural UniversityWuhanPeople’s Republic of China
  2. 2.Department of Parasitology, Faculty of Veterinary ScienceUniversity of AgricultureFaisalabadPakistan
  3. 3.Hubei Cooperative Innovation Center for Sustainable Pig ProductionWuhanPeople’s Republic of China
  4. 4.Key Laboratory for Development of Veterinary Diagnostic Products, Ministry of AgricultureHuazhong Agricultural UniversityWuhanPeople’s Republic of China

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