Abstract
Tropical theileriosis, babesiosis, and anaplasmosis are the most dominant tick-borne infections in North Africa where they cause significant economic losses in ruminants’ industry. The aim of the present work was to study infections and co-infection patterns in 66 cattle with clinical signs of piroplasmosis and/or anaplasmosis in two localities, Beni Hamidene and Grarem Gouga, districts of Constantine and Mila (Northeast of Algeria), respectively. This study was conducted between early May and late September during four years 2017, 2018, 2020, and 2021. PCR showed that the most frequent pathogen in cattle with clinical signs of piroplasmosis and/or anaplasmosis was Theileria annulata (66/66; 100%) followed by Babesia bovis (21/66; 31.8%), Anaplasma marginale (15/66; 22.7%), and Babesia bigemina (3/66; 4.5%) (p < 0.001). Giemsa-stained blood smears examinations revealed that 66.7% (44/66); 10.6% (7/66); and 9.1% (6/66) of cattle were infected by T. annulata, Babesia spp., and A. marginale, respectively (p < 0.001). PCR revealed seven co-infection patterns: T. annulata/A. marginale (15/66; 22.7%), T. annulata/B. bovis (21/66; 31.8%), T. annulata/B. bigemina (3/66; 4.5%), T. annulata/A. marginale/B. bovis (7/66; 10.6%), T. annulata/B. bovis/B. bigemina (2/66; 3%), T. annulata/A. marginale/B. bigemina (1/66; 1.5%), and T. annulata/A. marginale/B. bigemina/B. bovis (1/66; 1.5%). Phylogenetic analyses showed that T. annulata Tams1 and B. bigemina gp45 sequences were identical to isolates from Mauritania and South Africa, respectively. The three A. marginale amplicons obtained herein had 99.63 to 99.88% similarity between them. This study provides data that can be used to improve control programs targeting these cattle hemopathogens.
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Data Availability
The datasets generated during the current study are available from the corresponding author on reasonable request.
References
Abdel-Shafy S, Abdullah HHAM, Elbayoumy MK et al (2022) Molecular epidemiological investigation of piroplasms and Anaplasmataceae Bacteria in Egyptian domestic animals and associated ticks. Pathogens 11:1194. https://doi.org/10.3390/pathogens11101194
Al-hamidhi S, Parveen A, Iqbal F et al (2022) Diversity and genetic structure of Theileria annulata in Pakistan and other endemic sites. Pathogens 11:334. https://doi.org/10.3390/pathogens11030334
AL-Hosary A, Răileanu C, Tauchmann O et al (2021) Tick species identification and molecular detection of tick-borne pathogens in blood and ticks collected from cattle in Egypt. Ticks Tick Borne Dis 12:101676. https://doi.org/10.1016/j.ttbdis.2021.101676
Asif M, Ben Said M, Parveen A et al (2022) Seasonal survey, risk factor’s analysis and genotyping of Theileria annulata infecting cattle in Punjab province. Pakistan. Acta Trop 234:106587. https://doi.org/10.1016/j.actatropica.2022.106587
Aubry P, Geale DW (2011) A review of bovine anaplasmosis. Transbound Emerg Dis 58:1–30. https://doi.org/10.1111/j.1865-1682.2010.01173.x
Ayadi O, Gharbi M, Benchikh Elfegoun MC (2016) Milk losses due to bovine tropical theileriosis (Theileria annulata infection) in Algeria. Asian Pac J Trop Biomed 6:801–802. https://doi.org/10.1016/j.apjtb.2016.06.014
Azhahianambi P, Madhanmohan M, Madan N et al (2021) Successful treatment of severe form of bovine tropical theileriosis in dairy cattle and genotyping of Theileria annulata isolates of Tamil Nadu. India. Vet Parasitol Reg Stud Reports 26:100628. https://doi.org/10.1016/j.vprsr.2021.100628
Battilani M, De Arcangeli S, Balboni A, Dondi F (2017) Genetic diversity and molecular epidemiology of Anaplasma. Infect Genet Evol 49:195–211. https://doi.org/10.1016/j.meegid.2017.01.021
Bedouhene A, Kelanemer R, Medrouh B et al (2022) Seasonal dynamics and predilection sites of ticks (Acari: Ixodidae) feeding on cows in the Western Parts of the Djurdjura. Algeria Front Trop Dis 3:856179. https://doi.org/10.3389/fitd.2022.856179
Benchikh Elfegoun MC, Gharbi M, Merzekani Z, Kohil K (2017) Bovine piroplasmosis in the provinces of Skikda and Oum El Bouaghi (Northeastern Algeria): epidemiological study and estimation of milk yield losses. Rev Élev Méd Vét Pays Trop 70:105–110. https://doi.org/10.19182/remvt.31519
Bilgiç HB, Karagenç T, Simuunza M et al (2013) Development of a multiplex PCR assay for simultaneous detection of Theileria annulata, Babesia bovis and Anaplasma marginale in cattle. Exp Parasitol 133:222–229. https://doi.org/10.1016/j.exppara.2012.11.005
Bilgic HB, Karagenc T, Bakirci S et al (2016) Identification and analysis of immunodominant antigens for ELISA-based detection of Theileria annulata. PLoS One 11:e0156645. https://doi.org/10.1371/journal.pone.0156645
Bock R, Jackson L, de Vos A, Jorgensen W (2004) Babesiosis of cattle. Parasitology 129:S247–S269. https://doi.org/10.1017/s0031182004005190
Bouattour A, Darghouth MA, Ben Miled L (1996) Cattle infestation by Hyalomma ticks and prevalence of Theileria in H. detritum species in Tunisia. Vet Parasitol 65:233–245. https://doi.org/10.1016/s0304-4017(96)00951-x
Boularias G, Azzag N, Galon C et al (2021) High-throughput microfluidic real-time PCR for the detection of multiple microorganisms in ixodid cattle ticks in Northeast Algeria. Pathogens 10:362. https://doi.org/10.3390/pathogens10030362
Boulkaboul A (2003) Parasitisme des tiques (Ixodidae) des bovins à Tiaret, Algérie. Rev Élev Méd Vét Pays Trop 56:157–162. https://doi.org/10.19182/remvt.9858
Boussaadoun MA, Gharbi M, Sayeh L et al (2015) Epidemiological situation of bovine tropical theileriosis (Theileria annulata infection) in the Northwest Tunisia. J Adv Parasitol 2:69–74. https://doi.org/10.14737/journal.jap/2015/2.4.69.74
Bureau d’hygiène communal - APC Beni Hamidene, Wilaya de Constantine (2022). Rapport d’activité annuelle. Accessed 20 Jan 2023
Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al revisited. J Parasitol 83:575–583
Ceylan O, Xuan X, Sevinc F (2021) Primary tick-borne protozoan and rickettsial infections of animals in Turkey. Pathogens 10:231. https://doi.org/10.3390/pathogens10020231
Chatanga E, Mosssad E, Abdo Abubaker H et al (2019) Evidence of multiple point mutations in Theileria annulata cytochrome b gene incriminated in buparvaquone treatment failure. Acta Trop 191:128–132. https://doi.org/10.1016/j.actatropica.2018.12.041
D’Oliveira C, van der Weide M, Habela MA et al (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
de la Fournière S, Paoletta MS, Guillemi EC et al (2021) Development of highly sensitive one step-PCR tests for improved detection of B bigemina and B bovis. Vet Parasitol 296:109493. https://doi.org/10.1016/j.vetpar.2021.109493
de la Fuente J, Naranjo V, Ruiz-Fons F, Höfle U, Fernández de Mera IG, Villanúa D et al (2005) Potential vertebrate reservoir hosts and invertebrate vectors of Anaplasma marginale and A. phagocytophilum in central Spain. Vector-Borne Zoonotic Dis 5:390–401. https://doi.org/10.1089/vbz.2005.5.390
De La Fuente J, Passos LMF, Van Den Bussche RA et al (2004) Genetic diversity and molecular phylogeny of Anaplasma marginale isolates from Minas Gerais, Brazil. Vet Parasitol 121:307–316. https://doi.org/10.1016/j.vetpar.2004.02.021
Direction des Services Agricoles de la Wilaya de Constantine (2018) Rapport d’activité annuelle
Direction des services agricoles de la wilaya de Mila (2022) Rapport d’activité annuelle
El-Dakhly KM, Arafa WM, Soliman S et al (2020) Molecular detection, phylogenetic analysis, and genetic diversity of Theileria annulata, Babesia bigemina, and Anaplasma marginale in cattle in three districts of Egypt. Acta Parasitol 65:620–627. https://doi.org/10.2478/s11686-020-00189-z
Elhachimi L, Rogiers C, Casaert S et al (2021) Ticks and tick-borne pathogens abound in the cattle population of the Rabat-Sale kenitra region. Morocco Pathogens 10:1594. https://doi.org/10.3390/pathogens10121594
Fedorina EA, Arkhipova AL, Kosovskiy GY, Kovalchuk SN (2019) Molecular survey and genetic characterization of Anaplasma marginale isolates in cattle from two regions of Russia. Ticks Tick Borne Dis 10:251–257. https://doi.org/10.1016/j.ttbdis.2018.10.011
Fesseha H, Mathewos M, Eshetu E, Tefera B (2022) Babesiosis in cattle and ixodid tick distribution in Dasenech and Salamago Districts, southern Ethiopia. Sci Rep 12:6385. https://doi.org/10.1038/s41598-022-10416-4
Foughali AA, Amairia S, Bitam I et al (2021a) Knowledge, attitude and perception of bovine piroplasmosis by cattle owners in Constantine, North-East of Algeria, using participatory epidemiology. Trop Anim Heal Prod 53:167. https://doi.org/10.1007/s11250-021-02608-3
Foughali AA, Ziam H, Aiza A et al (2021b) Cross-sectional survey of cattle haemopathogens in Constantine, Northeast Algeria. Vet Med Sci 7:1237–1244. https://doi.org/10.1002/vms3.459
Ganzinelli S, Byaruhanga C, Primo ME et al (2022) International interlaboratory validation of a nested PCR for molecular detection of Babesia bovis and Babesia bigemina, causative agents of bovine babesiosis. Vet Parasitol 304:109686. https://doi.org/10.1016/j.vetpar.2022.109686
Gharbi M, Darghouth MA (2014) A review of Hyalomma scupense (Acari, Ixodidae) in the Maghreb region: From biology to control. Parasite 21:2. https://doi.org/10.1051/parasite/2014002
Gharbi M, Mhadhbi M, Darghouth MA (2012) Diagnostic de la theilériose tropicale du bœuf (infection par Theileria annulata) en Afrique du Nord. Rev Méd Vét 163:563–571
Gharbi M, Rekik B, Mabrouk M et al (2015) Impact of the carrier state by Theileria annulata on milk yield in Tunisian crossbred (Bos taurus) cattle. Asian Pacific J Trop Dis 5:884–887. https://doi.org/10.1016/S2222-1808(15)60950-1
Gharbi M, Darghouth MA, Elati K et al (2020) Current status of tropical theileriosis in Northern Africa: a review of recent epidemiological investigations and implications for control. Transbound Emerg Dis 67(S1):8–25. https://doi.org/10.1111/tbed.13312
Ghoneim AM, El-Fayomy AO (2014) Targeting tams-1 gene results in underestimation of Theileria annulata infection in diseased cattle in Egypt. Acta Parasitol 59:85–90. https://doi.org/10.2478/s11686-014-0211-9
Gomes J, Salgueiro P, Inácio J et al (2016) Population diversity of Theileria annulata in Portugal. Infect Genet Evol 42:14–19. https://doi.org/10.1016/j.meegid.2016.04.023
Guglielmone AA (1995) Epidemiology of babesiosis and anaplasmosis in South and Central America. Vet Parasitol 57:109–119. https://doi.org/10.1016/0304-4017(94)03115-d
Kaur R, Yadav A, Rafiki SI et al (2021) Epidemiology, haematology and molecular characterization of haemoprotozoon and rickettsial organisms causing infections in cattle of Jammu region. North India BMC Vet Res 17:219. https://doi.org/10.1186/s12917-021-02915-9
Khan Z, Shehla S, Alouffi A et al (2022) Molecular survey and genetic characterization of Anaplasma marginale in ticks collected from livestock hosts in Pakistan. Animals 12:1708. https://doi.org/10.3390/ani12131708
Kocan KM, de la Fuente J, Guglielmone AA, Meléndez RD (2003) Antigens and alternatives for control of Anaplasma marginale infection in cattle. Clin Microbiol Rev 16:698–712. https://doi.org/10.1128/CMR.16.4.698-712.2003
Kuibagarov M, Makhamed R, Zhylkibayev A et al (2023) Theileria and Babesia infection in cattle – first molecular survey in Kazakhstan. Ticks Tick Borne Dis 14:102078. https://doi.org/10.1016/j.ttbdis.2022.102078
Kumar B, Maharana BR, Prasad A et al (2016) Seasonal incidence of parasitic diseases in bovines of south western Gujarat (Junagadh), India. J Parasit Dis 40:1342–1346. https://doi.org/10.1007/s12639-015-0686-9
Laamari A, Kharrim KEL, Mrifag R et al (2012) Dynamique des populations de tiques parasites des bovins de la région du Gharb au Maroc. Rev Élev Méd Vét Pays Trop 65:57–62. https://doi.org/10.19182/remvt.10123
Lotfi D, Karima K (2021) Identification and incidence of hard tick species during summer season 2019 in Jijel Province (northeastern Algeria). J Parasit Dis 45:211–217. https://doi.org/10.1007/s12639-020-01296-4
M’ghirbi Y, Hurtado A, Brandika J et al (2008) A molecular survey of Theileria and Babesia parasites in cattle, with a note on the distribution of ticks in Tunisia. Parasitol Res 103:435–442. https://doi.org/10.1007/s00436-008-0995-3
Magunda F, Thompson CW, Schneider DA, Noh SM (2016) Anaplasma marginale actively modulates vacuolar maturation during intracellular infection of its tick vector, Dermacentor andersoni. Appl Environ Microbiol 82:4715–4731. https://doi.org/10.1128/AEM.01030-16
Mercado-Uriostegui MA, Castro-Sánchez LA, Batiha GE-S et al (2022) The GP-45 Protein, a highly variable antigen from Babesia bigemina, contains conserved B-Cell Epitopes in geographically distant isolates. Pathogens 11:591. https://doi.org/10.3390/pathogens11050591
Moraga-Fernández A, Ortiz JA, Jabbar A et al (2022) Fatal cases of bovine anaplasmosis in a herd infected with different Anaplasma marginale genotypes in southern Spain. Ticks Tick Borne Dis 13:101864. https://doi.org/10.1016/j.ttbdis.2021.101864
Mtshali MS, Mtshali PS (2013) Molecular diagnosis and phylogenetic analysis of Babesia bigemina and Babesia bovis hemoparasites from cattle in South Africa. BMC Vet Res 9:154. https://doi.org/10.1186/1746-6148-9-154
Parodi P, Armúa-Fernández MT, Schanzembach M et al (2022) Characterization of strains of Anaplasma marginale from clinical cases in bovine using major surface protein 1a in Uruguay. Front Vet Sci 9:990228
QGIS Development Team (2022). QGIS Geographic Information System. Open Source Geospatial Foundation Project. https://qgis.osgeo.org. Accessed 20 May 2023
Ramos IAS, Herrera HM, Mendes NS et al (2019) Phylogeography of msp4 genotypes of Anaplasma marginale in beef cattle from the Brazilian Pantanal. Rev Bras Parasitol Vet 28:451–457. https://doi.org/10.1590/S1984-29612019049
Rar V, Tkachev S, Tikunova N (2021) Genetic diversity of Anaplasma bacteria: twenty years later. Infect Genet Evol 91:104833. https://doi.org/10.1016/j.meegid.2021.104833
Rocha JF, Martínez R, López-Villalobos N, Morris ST (2019) Tick burden in Bos taurus cattle and its relationship with heat stress in three agroecological zones in the tropics of Colombia. Parasit Vectors 12:73. https://doi.org/10.1186/s13071-019-3319-9
Sallemi S, Rjeibi MR, Rouatbi M et al (2017) Molecular prevalence and phylogenetic analysis of Theileria annulata and Trypanosoma evansi in cattle in Northern Tunisia. Vet Med Sci 4:17–25. https://doi.org/10.1002/vms3.79
Santos M, Soares R, Costa P et al (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
Schnittger L, Rodriguez AE, Florin-Christensen M, Morrison DA (2012) Babesia: a world emerging. Infect Genet Evol 12:1788–1809. https://doi.org/10.1016/j.meegid.2012.07.004
Schwartz D (1993) Méthodes statistiques à l’usage des médecins et des biologistes, 3rd edn. Flammarion Médecine-Sciences, Paris, France
Silva MG, Marques PX, Oliva A (2010) Detection of Babesia and Theileria species infection in cattle from Portugal using a reverse line blotting method. Vet Parasitol 174:199–205. https://doi.org/10.1016/j.vetpar.2010.08.038
Sun M, Guan G, Liu Z et al (2020) Molecular survey and genetic diversity of Babesia spp. and Theileria spp. in cattle in Gansu Province. China Acta Parasitol 65:422–429. https://doi.org/10.2478/s11686-020-00179-1
Tamura K, Peterson D, Peterson N et al (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. https://doi.org/10.1093/molbev/msr121
Trueman KF, Blight GW (1978) The effect of age on resistance of cattle to Babesia bovis. Aust Vet J 54:301–305. https://doi.org/10.1111/j.1751-0813.1978.tb02465.x
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
Ullah R, Shams S, Khan MA et al (2021) Epidemiology and molecular characterization of Theileria annulata in cattle from central Khyber Pakhtunkhwa Pakistan. PLoS One 16:e0249417. https://doi.org/10.1371/journal.pone.0249417
Ullah N, Ashraf K, Rehman A et al (2022) Propagation of Babesia bigemina in rabbit model and evaluation of its attenuation in Cross-bred calves. Animals 12:2287. https://doi.org/10.3390/ani12172287
Viseras J, Hueli LE, Adroher FJ, García-Fernández P (1999) Studies on the transmission of Theileria annulata to cattle by the tick Hyalomma lusitanicum. J Vet Med B 46:505–509. https://doi.org/10.1111/j.1439-0450.1999.tb01242.x
Walker AR, Bouattour A, Camicas JL et al (2014) Ticks of domestic animals in Africa : a guide to identification of species. Bioscience Reports, Edinburgh, UK
Wang J, Yang X, Wang Y et al (2014) Genetic diversity and phylogenetic analysis of Tams1 of Theileria annulata isolates from three continents between 2000 and 2012. Cent Eur J Immunol 39:476–484. https://doi.org/10.5114/ceji.2014.47732
Yokoyama N, Suthisak B, Hirata H et al (2002) Cellular localization of Babesia bovis merozoite rhoptry-associated protein 1 and its erythrocyte-binding activity. Infect Immun 70:5822–5826. https://doi.org/10.1128/IAI.70.10.5822-5826.2002
Ziam H, Kelanamer R, Aissi M et al (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, Ababou A, Kazadi JM et al (2016) Prévalences et signes cliniques associés des piroplasmoses bovines dans les Wilayates d’Annaba et El Tarf, Algérie. Rev Méd Vét 167:241–249
Acknowledgements
The authors would like to thank Dr Halima Boulkrout and Nadjet Redjem for their collaboration. The authors would also like to thank all cattle farmers of Beni Hamidene and Grarem Gouga who accepted that we handle their animals.
Funding
This work was funded by the Laboratoire d’épidémiologie des infections enzootiques des herbivores en Tunisie: application à la lutte’ (LR16AGR01) (Ministère de l’enseignement supérieure et de la recherche scientifique, Tunisie).
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Asma Amina Foughali designed this study, analyzed and interpreted molecular data, and wrote the original draft. Moez Mhadhbi and Asma Amina Foughali performed the lab analysis. Safa Amairia helped in the methodology of the study. Asma Amina Foughali and Mokhtar Dhibi identified the ticks. Idir Bitam and Ali Berbar are responsible for the work administration. Asma Amina Foughali and Hadjer Boukaabache collected samples. Phylogenetic analysis was carried out by Asma Amina Foughali and Mohamed Ridha Rjeibi. Mohamed Gharbi and Asma Amina Foughali performed the statistical analyses. Moez Mhadhbi, Asma Amina Foughali, and Mohamed Gharbi supervised and revised the manuscript.
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Foughali, A.A., Mhadhbi, M., Amairia, S. et al. Cattle co-infection patterns by hemopathogens and their phylogenetic analysis during the tick season in Constantine and Mila, Northeast Algeria. Parasitol Res 122, 2245–2257 (2023). https://doi.org/10.1007/s00436-023-07916-1
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DOI: https://doi.org/10.1007/s00436-023-07916-1