Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2020 Nov 13;10(1):19802.
doi: 10.1038/s41598-020-76844-2.

Dynamics and within-host interaction of Theileria lestoquardi and T. ovis among naive sheep in Oman

Hoyam Awad  1 , Amal A H Gadalla  2 , Milagros Postigo  1 , Salama Al-Hamidhi  3 , Mohammed H Tageldin  4 , Sini Skariah  5 , Ali A Sultan  5 , Eugene H Johnson  4 , Brian Shiels  6 , Arnab Pain  7   8 , Joanne Thompson  9 , Hamza A Babiker  10
Affiliations

Dynamics and within-host interaction of Theileria lestoquardi and T. ovis among naive sheep in Oman

Hoyam Awad et al. Sci Rep. .

Abstract

Mixed species infections of Theileria spp. are common in nature. Experimental and epidemiological data suggest that mixed species infections elicit cross-immunity that can modulate pathogenicity and disease burden at the population level. The present study examined within-host interactions, over a period of 13 months during natural infections with two Theileria spp., pathogenic (T. lestoquardi) and non-pathogenic (T. ovis), amongst a cohort of naive sheep in Oman. In the first two months after exposure to infection, a high rate of mortality was seen among sheep infected with T. lestoquardi alone. However, subsequently mixed-infections of T. lestoquardi and T. ovis prevailed, and no further death occurred. The overall densities of both parasite species were significantly higher as single infection vs mixed infection and the higher relative density of pathogenic T. lestoquardi indicated a competitive advantage over T. ovis in mixed infection. The density of both species fluctuated significantly over time, with no difference in density between the very hot (May to August) and warm season (September to April). A high degree of genotype multiplicity was seen among T. lestoquardi infections, which increased with rising parasite density. Our results illustrate a potential competitive interaction between the two ovine Theileria spp., and a substantial reduction in the risk of mortality in mixed parasite infections, indicating that T. ovis confers heterologous protection against lethal T. lestoquardi infection.

PubMed Disclaimer

Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
T. ovis (A) and T. lestoquardi (B) 18s rRNA standard curves. Standard curves generated from eight points of tenfold serial dilutions of T. lestoquardi and T. ovis 18s rRNA purified pooled PCR products (amplified from pure T. lestoquardi culture and a natural infection with only T. ovis genomic DNA), with detection range of 9.26 × 107–9.26 18s rRNA copies/ μl DNA) and 5.3 × 107–5.3 18s rRNA copies/μl blood for T. lestoquardi and T. ovis 18s rRNA, respectively. Y axis represents the qPCR cycle threshold (CT). X axis represent log10 18s rRNA copy number.
Figure 2
Figure 2
Proportions of T. lestoquardi and T. ovis infection and mortality in a cohort of sheep (n = 50), over a period of 13 months (May 2016 to May 2017) in a farm in Sharqiyah region, Oman. 7 animals died, 4 (8%) in May 2016 and 3 (7%) in June 2016, while no deaths occurred after June 2016.
Figure 3
Figure 3
T. lestoquardi density (blue) and T. ovis density within mixed species infection. T. lestoquardi density was higher than T. ovis density throughout study period, except in May 2016. Error bars represent 95%CI.
Figure 4
Figure 4
Estimated density in single (T. lestoquardi alone) and mixed infection (T. lestoquardi plus T. ovis) of sheep. There was a significant increase in T. lestoquardi density in single infection over time (Log likelihood: − 630.08, dF: 9, x2: 13.658, P < 0.001). Error bars represent 95% CI.
Figure 5
Figure 5
Effect of multiplicity of infection on T. lestoquardi density: There is a positive association between the Log10 T. lestoquardi density and the estimated mean number of clones. Black squares represent the mean values of Log10 T. lestoquardi density at each MNC. Error pars represent 95% CI of the mean value.
See this image and copyright information in PMC

References

    1. Mayxay M, Pukrittayakamee S, Newton PN, White NJ. Mixed-species malaria infections in humans. Trends Parasitol. 2004;20(5):233–240. doi: 10.1016/j.pt.2004.03.006. - DOI - PubMed
    1. Iseki H, Alhassan A, Ohta N, Thekisoe OM, Yokoyama N, Inoue N, Nambota A, Yasuda J, Igarashi I. Development of a multiplex loop-mediated isothermal amplification (mLAMP) method for the simultaneous detection of bovine Babesia parasites. J. Microbiol. Methods. 2007;71(3):281–287. doi: 10.1016/j.mimet.2007.09.019. - DOI - PubMed
    1. Jalali SM, Jolodar A, Rasooli A, Darabifard A. Detection of Theileria lestoquardi cross infection in cattle with clinical theileriosis in Iran. Acta Parasitol. 2016;61(4):756–761. doi: 10.1515/ap-2016-0104. - DOI - PubMed
    1. Zaeemi M, Haddadzadeh H, Khazraiinia P, Kazemi B, Bandehpour M. Identification of different Theileria species (Theileria lestoquardi, Theileria ovis, and Theileria annulata) in naturally infected sheep using nested PCR–RFLP. Parasitol. Res. 2011;108(4):837–843. doi: 10.1007/s00436-010-2119-0. - DOI - PubMed
    1. Györke A, Pop L, Cozma V. Prevalence and distribution of Eimeria species in broiler chicken farms of different capacities. Parasite. 2013;20:1–8. doi: 10.1051/parasite/2013052. - DOI - PMC - PubMed

Publication types