Prevalence of Theileria annulata infection in cattle in different regions and farming systems in Algeria
Published:
Nov 6, 2025
Updated:
2025-11-06
Versions:
2025-11-06 (2)
Keywords:
cattle Immunofluorescent antibody test PCR Tams Algeria
Abstract
Tropical theileriosis (TT) is a tick-borne disease of cattle caused by the apicomplexan parasite Theileria annulata. It poses a major threat to the health of imported exotic breeds and, to a lesser extent, native breeds which have a degree of resistance to the disease. The study aimed to determine the prevalence of T. annulata infection in cattle in the arid and semi-arid regions of Algeria using serological and molecular methods. Bovine blood was tested for the presence of T. annulata-specific antibodies using the immunofluorescent antibody test (IFAT) and for parasite DNA using a polymerase chain reaction (PCR) for the gene encoding the major merozoite/piroplasm surface protein (Tams1). One hundred and sixteen individuals were screened and overall prevalences of 50.0 ± 4.6 % (IFAT) and 64.7 ± 4.4 % (PCR) were determined. There was moderate agreement between IFAT and PCR tests for the diagnosis of TT, with a sensitivity of 74.6 % and a specificity of 95.1 % for IFAT when compared against the PCR. Potential risk factors identified in this study were breed (OR = 2.25, 95% CI: 1.07–5.07), season of sampling (OR = 4.29, 95% CI: 1.97–10.9) and breeding system (OR = 8.60, 95% CI: 1.41–57.6). Sequence analysis of Tams1 PCR amplicons revealed 97.5–100% identity with one another and, overall, they were found to bear similarity to previously sequenced isolates from North Africa, Europe and Asia.
Article Details
- How to Cite
-
Messaoudi, Z., Weir, W., Saidi, F., Kelanemer, R., Medrouh, B., Gomes, J., Bilgic, H., Karagenc, T., Hacilarlioglu, S., & Ziam, H. (2025). Prevalence of Theileria annulata infection in cattle in different regions and farming systems in Algeria. Journal of the Hellenic Veterinary Medical Society, 76(3), 9529–9544. https://doi.org/10.12681/jhvms.38690
- Issue
- Vol. 76 No. 3 (2025)
- Section
- Research Articles
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
Authors who publish with this journal agree to the following terms:
· Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution Non-Commercial License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
· Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g. post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
· Authors are permitted and encouraged to post their work online (preferably in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work.
Downloads
Download data is not yet available.
References
Abaker IA, Salih DA, Haj E, Ahmed LM, Osman RE, Ali MM (2017).
Prevalence of Theileria annulata in dairy cattle in Nyala, South Darfur
State, Sudan. Vet world 10: 1475–1480. https://doi.org/10.14202/
vetworld.2017.1475-1480
Ayadi O, Rjeibi MR, Benchikh Elfegoun MC, Gharbi M (2017) Prevalence
and risk factors of tropical theileriosis, and sequencing of
Theileria annulata, the causative pathogen, in Setif region (Algeria)
before and after tick season. Rev Elev Méd Vét des pays Trop 69:
Bandelt HJ, Forster P, Sykes BC, Richards MB, (1995) Mitochondrial
portraits of human populations using median networks. Genetics
(2), 743–753. https://doi.org/10.1093/genetics/141.2.743
Bedouhene A, Kelanemer R, Medrouh B, Kernif T, Saidi F, Tail G,
Ziam H (2022) Seasonal Dynamics and Predilection Sites of Ticks
(Acari: Ixodidae) Feeding on Cows in the Western Parts of the
Djurdjura, Algeria. Front Trop Dis 3: 34. https://doi.org/10.3389/
FITD.2022.856179
Benchikh Elfegoun MC, Gharbi M, Merzekani Z, Kohil K (2017). Piroplasmoses
bovines dans les provinces de Skikda et d’Oum El
Bouaghi (nord-est de l’Algérie) : étude épidémiologique et estimation
des pertes de production laitière. Rev Elev Méd Vét pays
Trop 70: 105. https://doi.org/10.19182/remvt.31519
Boulkaboul A (2003). Parasitisme des tiques (Ixodidae) des bovins à
Tiaret, Algérie. Rev Elev Méd Vét pays Trop 56: 157. https://doi.
org/10.19182/remvt.9858
Burridge MJ, Brown CGD, Kimber CD (1974) Theileria annulata:
Cross-reactions between a cell culture schizont antigen and antigens
of East African species in the indirect fluorescent antibody
test. Exp Parasitol 35: 374–380. https://doi.org/10.1016/0014-
(74)90043-5
Calleja-Bueno L, Sainz Á, García-Sancho M, Rodríguez-Franco F,
González-Martín JV, Villaescusa A (2017) Molecular, epidemiological,
haematological and biochemical evaluation in asymptomatic
Theileria annulata infected cattle from an endemic region in Spain. Ticks Tick Borne Dis 8: 936–941. https://doi.org/10.1016/J.
TTBDIS.2017.08.006
Chae JS, Lee JM, Kwon OD, Holman PJ, Waghela SD, Wagner GG,
(1998) Nucleotide sequence heterogeneity in the small subunit ribosomal
RNA gene variable (V4) region among and within geographic
isolates of Theileria from cattle, elk and white-tailed deer. Vet Parasitol
Glascodine J, Tetley L, Brown D, Shiels B, (1990) Development expression
of a Theileria
annulata merozoite surface antigen. Mol. Biochem. Parasitol., 40, 105-
d’Oliveira C, Van Der Weide M, Habela MA, Jacquiet P, Jongejan F,
(1995) Detection of Theileria annulata in blood samples of carrier
cattle by PCR. J Clin Microbiol 33: 2665-2669. https://doi.
org/10.1128/JCM.33.10.2665-2669.1995
Darghouth MA, Bouattour A, Kilani M (2003) Theilérioses. In: Les
maladies infectieuses et parasitaires du bétail des régions chaudes.
Lefèvre PC, Blancou J, Chermette R (Eds.). Lavoisier, TEC & Doc,
EM International. Paris: pp. 1585-1597
Darghouth M, Bouattour A, Miled L, Ben Sassi L, (1996a) Diagnosis
of Theileria annulata infection of cattle in Tunisia: comparison of
serology and blood smears. Vet Res 27: 613–621.
Darghouth MEA, Bouattour A, Ben Miled L, Kilani M, Brown CGD,
(1996b). Epidemiology of tropical theileriosis (Theileria annulata
infection of cattle) in an endemic region of Tunisia: characterisation
of endemicity states. Vet Parasitol 65: 199-211. https://doi.
org/10.1016/s0304-4017(96)00974-0
Dobbelaere DAE, Rottenberg S, (2003) Theileria-induced leukocyte
transformation. Curr. Opin. Microbiol. 6, 377–382. https://doi.
org/10.1016/S1369-5274(03)00085-7
Dumanli N, Aktas M, Cetinkaya B, Cakmak A, Koroglu E, Saki CE,
Erdogmus Z, Nalbantoglu S, Ongor H, Simşek S, (2005) Prevalence
and distribution of tropical theileriosis in eastern Turkey. Vet
Parasitol 127: 9–15.
El Damaty HM, Yousef SG, Mahmmod YS, El-Balkemy FA, Mweu
MM, (2021) Sensitivity and specificity of piroplasm indirect fluorescent
antibody test and PCR for Theileria annulata infection
in clinically asymptomatic large ruminants using Bayesian latent
class analysis. Vet Parasitol Reg Stud Reports 24: 100563. https://
doi.org/10.1016/J.VPRSR.2021.100563
Estrada-Peña A, Bouattour A, Camicas JL, Walker AR, (2004) Ticks
of domestic animals in the Mediterranean region, academia.edu.
University of Zaragoza. https://doi.org/https://www.academia.edu/
download/45161360/Ticks_of_Domestic_Animals_in_the_Mediter20160428-
-mg36yy.pdf
Flach EJ, Ouhelli H, (1992) The epidemiology of tropical theileriosis
(Theileria annulata infection in cattle) in an endemic area of
Morocco. Vet Parasitol 44: 51–65. https://doi.org/10.1016/0304-
(92)90143-W
Foughali AA, Ziam H, Aiza A, Boulkrout H, Berber A, Bitam I, Gharbi
M, (2021) Cross-sectional survey of cattle haemopathogens in
Constantine, Northeast Algeria. Vet Med Sci 00: 1–8. https://doi.
org/10.1002/vms3.459
Gargano V, Blanda V, Gambino D, La Russa F, Di Cataldo S, Gentile A,
Schirò G, Torina A, Millán J, Vicari D, (2021), U., 2021. Serological
Survey and Molecular Characterization of Theileria annulata
in Sicilian Cattle. Pathogens 10(2): 101. https://doi.org/10.3390/
pathogens10020101
Gharbi M, Darghouth MA, Elati K, AL-Hosary AAT, Ayadi O, Salih
DA, El Hussein AM, Mhadhbi M, Khamassi Khbou M, Hassan SM,
Obara I, Ahmed LS, Ahmed J, (2020) Current status of tropical
theileriosis in Northern Africa: A review of recent epidemiological
investigations and implications for control. Transbound Emerg Dis
(1): 8–25. https://doi.org/10.1111/TBED.13312
Gharbi M, Touay A, Khayeche M, Laarif J, Jedidi M, Sassi L, Darghouth
MA, (2011) Ranking control options for tropical theileriosis in
at-risk dairy cattle in Tunisia, using benefit-cost analysis. Rev Sci
Tech 30, 763–778. https://doi.org/10.20506/rst.30.3.2074
Gubbels MJ, Katzer F, Hide G, Jongejan F, Shiels BR, (2000) Generation
of a mosaic pattern of diversity in the major merozoite-piroplasm
surface antigen of Theileria annulata. Mol Bioch Parasitol 110:
Haied N, Foufou A, Chaab S, Azlaoui M, Khadri S, Benzahia K, Benzahia
I, (2017) Drought assessment and monitoring using meteorological
indices in a semi-arid region. Energ Proced 119: 518–529.
Hikosaka K, Watanabe YI, Tsuji N, Kita K, Kishine H, Arisue N, Marie
N, Palacpac Q, Kawazu SI, Sawai H, Horii T, Igarashi I, Tanabe
K, (2009) Divergence of the Mitochondrial Genome Structure in
the Apicomplexan Parasites, Babesia and Theileria. Mol Biol Evol
(5):1107-1116. https://doi.org/10.1093/molbev/msp320
Ilhan T, (2000) Diagnostic Methods for Epidemiological Studies (Theileria
annulata infection of cattle). University of Edinburgh. 292
pages. http://hdl.handle.net/1842/30299 [accessed 24 August 2024]
Inci A, Ica A, Yildirim A, Vatansever Z, Cakmak A, Albasan H, Cam Y,
Atasever A, Sariozkan S, Duzlu O, (2007) Economical impact of
tropical theileriosis in the Cappadocia region of Turkey. Parasitol
Res 101(2): 171–174 https://doi.org/10.1007/s00436-007-0693-6
Jacquiet P, Colas F, Cheikh D, Thiam E, Ly BA, (1994) Epidémiologie
descriptive de la theileriose bovine à Theileria annulata en
Mauritanie, Afrique de l’Ouest sub-saharienne. Rev Elev Méd Vét
pays Trop 47(2): 147–155. https://doi.org/10.19182/REMVT.9099
Katzer F, Mckellar S, Ben Miled L, D’oliveira C, Sheils S, (2006)
Selection of antigenic diversity of Tams1, the major merozoïte
antigen of Theileria annulata. Annal N Y Acad Sci 849: 96-108.
Kernif T, Medrouh B, Harrat Z, Saidi F, Ziam H, (2024) Characterisation
of field tropical theileriosis and associated risk factors in two
bioclimatic areas of Algeria. Ticks Tick Borne Dis 15: 380-381.
Kiara H, Steinaa L, Nene V, Svitek N, (2018) Theileria in Ruminants.
In: Parasitic Protozoa of Farm Animals and Pets. Florin-Christensen
M, Schnittger L. (eds). Springer, Cham. https://doi.org/10.1007/978-
-319-70132-5_8
Kumar S, Stecher G, Suleski M, Sanderford M, Sharma S, Tamura K,
(2024) MEGA12: Molecular Evolutionary Genetic Analysis version
for adaptive and green computing. Mol Biol Evol 41(12): 1–9.
Kundave VR, Nehra AK, Ram H, Kumari A, Shahzad M, Vinay TS,
Garg R, Banerjee PS, Singh G, Tiwari AK, (2021) Genetic diversity
in the Tams1 gene of Theileria annulata (Duschunkowsky and
Luhs, 1904) infecting cattle. Acta Trop 224: 106121. https://doi.
org/10.1016/j.actatropica.2021.106121
Leemans I, Brown D, Hooshmand-Rad P, Kirvar E, Uggla A, (1999)
Infectivity and cross-immunity studies of Theileria lestoquardi
and Theileria annulata in sheep and cattle: I. In vivo responses.
Vet Parasitol 82: 179-192. https://doi.org/https://doi.org/10.1016/
S0304-4017(99)00013-8
Mans BJ, Pienaar R, Latif AA, (2015) A review of Theileria diagnostics
and epidemiology. Int J Parasitol Parasites Wildl 4: 104-118. https://
doi.org/10.1016/J.IJPPAW.2014.12.006
Martín-Sánchez J, Viseras J, Adroher FJ, García-Fernández P, (1999)
Nested polymerase chain reaction for detection of Theileria annulata
and comparison with conventional diagnostic techniques: Its
use in epidemiology studies. Parasitol Res 85: 243-245. https://doi.
org/10.1007/S004360050541
McHugh ML, (2012) Interrater reliability: the kappa statistic. Biochem
Med 22: 276–282. https://hrcak.srce.hr/89395
Minami T, Spooner PR, Irvin AD, Ocama JGR, Dobbelaere DAE, Fujinaga
T, (1983) Characterisation of stocks of Theileria parva by
monoclonal antibody profiles. Res Vet Sci 35: 334–340. https://doi.
org/10.1016/S0034-5288(18)32029-0
Purnell RE, (1978) Theileria annulata as a hazard to cattle in countries
on the northern Mediterranean littoral. Vet Sci Commun 2: 3-10.
R Core Team, (2021) A language and environment for statistical computing.
R Foundation for Statistical Computing. [WWW Document].
Rahali T, Sahibi H, Sadak A, Hamou SA, Losson B, Goff WL, Rhalem
A, (2014) Séroprévalence et facteurs de risque des hémoparasitoses
(theilériose, babésiose et anaplasmose) chez les bovins dans quatre
grandes régions d’élevage du Maroc. Rev Elev Méd Vét des pays
Trop 67: 235-240. https://doi.org/10.19182/remvt.20566
Rozas J, Ferrer-Mata A, Sanchez-DelBarrio JC, Guirao-Rico S, Librado
P, Ramos-Onsins SE, Sanchez-Gracia A, (2017) DnaSP 6: DNA
sequence polymorphism analysis of large data sets. Mol Biol Evol
(12): 3299–3302. https://doi.org/10.1093/molbev/msx248
Sadeddine R, Diarra AZ, Laroche M, Mediannikov O, Righi S, Benakhla
A, Dahmana H, Raoult D, Parola P, (2020) Molecular identification of protozoal and bacterial organisms in domestic animals and their
infesting ticks from north-eastern Algeria. Ticks Tick Borne Dis 11,
Santos M, Soares R, Costa P, Amaro A, Inácio J, Gomes J, (2013)
Revisiting the Tams1-encoding gene as a species-specific target
for the molecular detection of Theileria annulata in bovine blood
samples. Ticks Tick Borne Dis 4: 72–77. https://doi.org/10.1016/J.
TTBDIS.2012.07.006
Sergent E, Donatien A, Parrot L, Lestoquard F, (1945) Etudes sur les
piroplasmoses bovines. Arch. l’Institut Pasteur Tunis Inst. Pasteur
Algérie 1: 1-816.
Tamura K, (1992) Estimation of the number of nucleotide substitutions
when there are strong transition-transversion and G+C-content biases.
Mol Biol Evol 9(4): 678–687. https://doi.org/10.1093/oxfordjournals.
molbev.a040752
Uilenberg G, (1995) International collaborative research: significance
of tick-borne hemoparasitic diseases to world animal health. Vet
Parasitol 57: 19-41. https://doi.org/10.1016/0304-4017(94)03107-8
Uilenberg G, (1981) Theilerial Species of Domestic Livestock. Adv.
Control Theileriosis 4-37. https://doi.org/10.1007/978-94-009-
-5_2
Ullah R, Shams S, Khan MA, Ayaz S, Akbar N, Din Q, Khan A, Leon
R, Zeb J, (2021) Epidemiology and molecular characterization of
Theileria annulata in cattle from central Khyber Pakhtunkhwa.
Pakistan. PLoS One 16:1-17. https://doi.org/10.1371/JOURNAL.
PONE.0249417
Valente D, Dutra AP, Carolino N, Gomes J, Coelho AC, Espadinha P,
Pais J, Carolino I, (2023) Prevalence and Risk Factors Associated
with Theileria annulata Infection in Two Bovine Portuguese Autochthonous
Breeds. Pathogens 12(5): 669. https://doi.org/10.3390/
pathogens12050669
Viera AJ, Garrett JM, (2005) Understanding interobserver agreement:
the kappa statistic. Fam Med 37(5): 360–363.
World Organisation for Animal Health, (2021) Theileriosis, in: Manuel
Des Tests de Diagnostic et Des Vaccins Pour Les Animaux Terrestres.
Paris: pp. 1185–1209.
Zeggane H, Ghernaout R, Boutoutaou D, Abdullah S, Remin, B, Kasi O,
(2021) Multidimensional analysis of precipitation in central-northern
region of Algeria. Larhyss J 18(3): 107-129.
Ziam H, (2016) Epidémiologie des piroplasmoses bovines dans le
nord de l’Algérie. Cas des theilérioses chez les bovins. Université
Houari Boumedienne des Sciences et de la Technologies, Alger.
Thèse de doctorat 130 pages. https://dspace.usthb.dz/bitstream/
handle/123456789/4985/TH8449.pdf?sequ
Ziam H, Kelanamer R, Aissi M, Ababou A, Berkvens D, Geysen D,
(2015) Prevalence of bovine theileriosis in North Central region
of Algeria by real-time polymerase chain reaction with a note on
its distribution. Trop Anim Health Prod 47: 787–796. https://doi.
org/10.1007/s11250-015-0772-0
Ziam H, Tahar K, Saidani K, Rabah K, Hammaz Z, Dirk G, (2020)
Bovine piroplasmosis-anaplasmosis and clinical signs of tropical
theileriosis in the plains of Djurdjura (north Algeria). Vet Med Sci
: 1-10. https://doi.org/10.1002/vms3.305
