Molecular detection and associated risk factors of Anaplasma marginale, A. ovis and A. platys in sheep from Algeria with evidence of the absence of A. phagocytophilum. - 2024
Molecular detection and associated risk factors of Anaplasma marginale, A. ovis and A. platys in sheep from Algeria with evidence of the absence of A. phagocytophilum.
[en] Anaplasma species are obligate intracellular rickettsial pathogens that cause significant diseases in animals and humans. Despite their importance, limited information on Anaplasma infections in Algeria has been published thus far. This study aimed to assess the infection rate, characterize Anaplasma species, and identify associated risk factors in selected sheep farms across Oum El Bouaghi region in Algeria. In 2018, we collected 417 blood samples from sheep (Ovis aries) and performed molecular characterization of Anaplasma species infecting these animals. This characterization involved the use of 16S rRNA, msp2, rpoB, and msp5 genes, which were analyzed through nested PCR, qPCR, cPCR, DNA sequencing, and subsequent phylogenetic analysis. Our findings revealed infection rates of 12.7 % for Anaplasma species detected, with Anaplasma ovis at 10.8 %, Anaplasma marginale at 1.7 %, and Anaplasma platys at 0.2 %. Interestingly, all tested animals were found negative for Anaplasma phagocytophilum. Statistical analyses, including the Chi-square test and Fisher exact test, failed to establish any significant relationships (p > 0.05) between A. ovis and A. platys infections and variables such as age, sex, sampling season, and tick infestation level. However, A. marginale infection exhibited a significant association with age (p < 0.05), with a higher incidence observed in lambs (5.2 %) compared to other age groups. Remarkably, this study represents the first molecular detection of A. platys and A. marginale in Algerian sheep. These findings suggest that Algerian sheep may serve as potential reservoirs for these pathogens. This research contributes valuable insights into the prevalence and characteristics of Anaplasma infections in Algerian sheep populations, emphasizing the need for further investigation and enhanced surveillance to better understand and manage these diseases.
Disciplines :
Veterinary medicine & animal health
Author, co-author :
Chadi, Hafidha; Research Laboratory Management of Local Animal Resources, Higher National Veterinary School (ENSV), El Harrach, Algiers 16004, Algeria, Department of Applied Biology, Faculty of Exact Sciences and Nature and Life Sciences, University of Echahid Cheikh Larbi Tebessi, Tebessa 12000, Algeria. Electronic address: hafidha.chadi@univ-tebessa.dz
Moraga-Fernández, Alberto ; SaBio, Instituto de Investigación en Recursos Cinegéticos (IREC), Consejo Superior de Investigaciones Científicas (CSIC), Universidad de Castilla-La Mancha (UCLM)-Junta de Comunidades de Castilla-La Mancha (JCCM), Ronda de Toledo 12, Ciudad Real 13005, Spain
Sánchez-Sánchez, Marta ; SaBio, Instituto de Investigación en Recursos Cinegéticos (IREC), Consejo Superior de Investigaciones Científicas (CSIC), Universidad de Castilla-La Mancha (UCLM)-Junta de Comunidades de Castilla-La Mancha (JCCM), Ronda de Toledo 12, Ciudad Real 13005, Spain
Chenchouni, Haroun ; Higher National School of Forests, Khenchela 40000, Algeria
Fernández de Mera, Isabel G ; SaBio, Instituto de Investigación en Recursos Cinegéticos (IREC), Consejo Superior de Investigaciones Científicas (CSIC), Universidad de Castilla-La Mancha (UCLM)-Junta de Comunidades de Castilla-La Mancha (JCCM), Ronda de Toledo 12, Ciudad Real 13005, Spain
Garigliany, Mutien-Marie ; Université de Liège - ULiège > Département de morphologie et pathologie (DMP) > Pathologie générale et autopsies
de la Fuente, José ; SaBio, Instituto de Investigación en Recursos Cinegéticos (IREC), Consejo Superior de Investigaciones Científicas (CSIC), Universidad de Castilla-La Mancha (UCLM)-Junta de Comunidades de Castilla-La Mancha (JCCM), Ronda de Toledo 12, Ciudad Real 13005, Spain, Center for Veterinary Health Sciences, Department of Veterinary Pathobiology, Oklahoma State University, Stillwater, OK 74078, USA
Tennah, Safia; Research Laboratory Management of Local Animal Resources, Higher National Veterinary School (ENSV), El Harrach, Algiers 16004, Algeria
Sedrati, Tahar ; Research Laboratory Management of Local Animal Resources, Higher National Veterinary School (ENSV), El Harrach, Algiers 16004, Algeria, Department of Biology, University of Mohamed El Bachir El Ibrahimi, Bordj Bou Arréridj 34000, Algeria
Ghalmi, Farida; Research Laboratory Management of Local Animal Resources, Higher National Veterinary School (ENSV), El Harrach, Algiers 16004, Algeria
Language :
English
Title :
Molecular detection and associated risk factors of Anaplasma marginale, A. ovis and A. platys in sheep from Algeria with evidence of the absence of A. phagocytophilum.
Ait Lbacha, H., Alali, S., Zouagui, Z., El Mamoun, L., Rhalem, A., Petit, E., Haddad, N., Gandoin, C., Boulouis, H.J., Maillard, R., High prevalence of Anaplasma spp. in small ruminants in Morocco. Transbound. Emerg. Dis. 64:1 (2017), 250–263.
Alim, M.A., Das, S., Roy, K., Masuduzzaman, M., Sikder, S., Hassan, M.M., Siddiki, A.Z., Hossain, M.A., Prevalence of hemoprotozoan diseases in cattle population of chittagong division, Bangladesh. Pak. Vet. J. 32:2 (2012), 221–224.
Allsopp, M.T.E.P., Visser, E.S., Du Plessis, J.L., Vogel, S.W., Allsopp, B.A., Different organisms associated with heartwater as shown by analysis of 16S ribosomal RNA gene sequences. Vet. Parasitol. 71:4 (1997), 283–300.
Almazán, C., Fourniol, L., Rouxel, C., Alberdi, P., Gandoin, C., Lagrée, A.C., Boulouis, H.J., de La Fuente, J., Bonnet, S.I., Experimental Ixodes ricinus-sheep cycle of Anaplasma phagocytophilum NV2Os propagated in tick cell cultures. Front. Vet. Sci., 7, 2020, 40.
Altay, K., Dumanli, N., Aktas, M., Ozupek, S., Survey of Anaplasma infections in small ruminants from east part of Turkey. Kafkas Üniv. Vet. Fakült. Derg. 20:1 (2014), 1–4 2014.
Aouadi, A., Leulmi, H., Boucheikhchoukh, M., Benakhla, A., Raoult, D., Parola, P., Molecular evidence of tick-borne hemoprotozoan-parasites (Theileria ovis and Babesia ovis) and bacteria in ticks and blood from small ruminants in Northern Algeria. Comp. Immunol. Microbiol. Infect. Dis. 50 (2017), 34–39.
Arraga-Alvarado, C.M., Qurollo, B.A., Parra, O.C., Berrueta, M.A., Hegarty, B.C., Breitschwerdt, E.B., Case report: molecular evidence of Anaplasma platys infection in two women from Venezuela. Am. J. Trop. Med. Hyg., 91(6), 2014, 1161.
Atif, F.A., Anaplasma marginale and Anaplasma phagocytophilum: Rickettsiales pathogens of veterinary and public health significance. Parasitol. Res. 114 (2015), 3941–3957.
Atif, F.A., Alpha proteobacteria of genus Anaplasma (Rickettsiales: Anaplasmataceae): epidemiology and characteristics of Anaplasma species related to veterinary and public health importance. Parasitology 143:6 (2016), 659–685.
Azzag, N., Petit, E., Gandoin, C., Bouillin, C., Ghalmi, F., Haddad, N., Boulouis, H.J., Prevalence of select vector-borne pathogens in stray and client-owned dogs from Algiers. Comp. Immunol. Microbiol. Infect. Dis. 38 (2015), 1–7.
Barry, D.M., Van Niekerk, C.H., Anaplasmosis in improved Boer goats in South Africa artificially infected with Anaplasma ovis. Small Rum. Res. 3:2 (1990), 191–197.
Battilani, M., De Arcangeli, S., Balboni, A., Dondi, F., Genetic diversity and molecular epidemiology of Anaplasma. Infect. Genet. Evol. 49 (2017), 195–211.
Belkahia, H., Ben Said, M., Alberti, A., Abdi, K., Issaoui, Z., Hattab, D., Gharbi, M., Messadi, L., First molecular survey and novel genetic variants' identification of Anaplasma marginale: A. centrale and A. bovis in cattle from Tunisia. Infect. Genet. Evol. 34 (2015), 361–371.
Belkahia, H., Ben Said, M., El Hamdi, S., Yahiaoui, M., Gharbi, M., Daaloul-Jedidi, M., Mhadhbi, M., Jedidi, M., Darghouth, M.A., Klabi, I., Zribi, L., Messadi, L., First molecular identification and genetic characterization of Anaplasma ovis in sheep from Tunisia. Small Rumin. Res. 121:2–3 (2014), 404–410.
Belkahia, H., Ben Said, M., El Mabrouk, N., Saidani, M., Cherni, C., Ben Hassen, M., Bouattour, A., Messadi, L., Spatio-temporal variations and genetic diversity of Anaplasma spp. in cattle from the North of Tunisia. Vet. Microbiol. 208 (2017), 223–230.
Belkahia, H., Ben Said, M., El Mabrouk, N., Saidani, M., Cherni, C., Ben Hassen, M., Bouattour, A., Messadi, L., Seasonal dynamics, spatial distribution and genetic analysis of Anaplasma species infecting small ruminants from Northern Tunisia. Infect. Genet. Evol. 54 (2017), 66–73.
Belkahia, H., Ben Said, M., Sayahi, L., Alberti, A., Messadi, L., Detection of novel strains genetically related to Anaplasma platys in Tunisian one-humped camels (Camelus dromedarius). J. Infect. Dev. Ctries. 9:10 (2015), 1117–1125.
Ben Said, M., Belkahia, H., Messadi, L., Anaplasma spp. in North Africa: a review on molecular epidemiology, associated risk factors and genetic characteristics. Ticks Tick-Borne Dis. 9:3 (2018), 543–555.
Ben Said, M., Belkahia, H., Alberti, A., Zobba, R., Bousrih, M., Yahiaoui, M., Daaloul-Jedidi, M., Mamlouk, A., Gharbi, M., Messadi, L., Molecular survey of Anaplasma species in small ruminants reveals the presence of novel strains closely related to A. phagocytophilum in Tunisia. Vector-Borne Zoonotic Dis. 15:10 (2015), 580–590.
Ben Said, M., Belkahia, H., Karaoud, M., Bousrih, M., Yahiaoui, M., Daaloul-Jedidi, M., Messadi, L., First molecular survey of Anaplasma bovis in small ruminants from Tunisia. Vet. Microbiol. 179:3–4 (2015), 322–326.
Cannon, R.M., Roe, R.T., Livestock Disease Surveys: A Field Manual for Veterinarians Canberra: Australian Bureau of Animal Health. 1982, Australian Govt. Publishing Service.
Cardoso, L., Gilad, M., Cortes, H.C., Nachum-Biala, Y., Lopes, A.P., Vila-Viçosa, M.J., Simões, M., Rodrigues, P.A., Baneth, G., First report of Anaplasma platys infection in red foxes (Vulpes vulpes) and molecular detection of Ehrlichia canis and Leishmania infantum in foxes from Portugal. Parasit. Vectors 8 (2015), 1–8.
Ceci, L., Iarussi, F., Greco, B., Lacinio, R., Fornelli, S., Carelli, G., Retrospective study of hemoparasites in cattle in southern Italy by reverse line blot hybridization. J. Vet. Med. Sci. 76:6 (2014), 869–875.
Chaibi, R., Mimoune, N., Benaceur, F., Stambouli, L., Hamida, A., Khedim, R., Saidi, R., Kaidi, R., Benaissa, M.H., Gouzi, H., Neffar, S., Chenchouni, H., Extrinsic and intrinsic drivers of parasite prevalence and abundance of hard-bodied ticks (Acari: Ixodoidea) in one-humped camel (Camelus dromedarius). Front. Vet. Sci., 2023.
Chochlakis, D., Ioannou, I., Sharif, L., Kokkini, S., Hristophi, N., Dimitriou, T., Tselentis, Y., Psaroulaki, A., Prevalence of Anaplasma sp. in goats and sheep in Cyprus. Vector-Borne Zoonotic Dis. 9:5 (2009), 457–463.
Dahmani, M., Davoust, B., Benterki, M.S., Fenollar, F., Raoult, D., Mediannikov, O., Development of a new PCR-based assay to detect Anaplasmataceae and the first report of Anaplasma phagocytophilum and Anaplasma platys in cattle from Algeria. Comp. Immunol. Microbiol. Infect. Dis., 39 (2015), 39–45.
Dahmani, M., Davoust, B., Rousseau, F., Raoult, D., Fenollar, F., Mediannikov, O., Natural Anaplasmataceae infection in Rhipicephalus bursa ticks collected from sheep in the French Basque Country. Ticks Tick-Borne Dis. 8:1 (2016), 18–24.
De Castro, J.J., Sustainable tick and tickborne disease control in livestock improvement in developing countries. Vet. Parasitol. 71:2–3 (1997), 77–97.
De la Fuente, J., Atkinson, M.W., Naranjo, V., Fernandez de Mera, I.G., Mangold, A.J., Keating, K.A., Kocan, K.M., Sequence analysis of the msp4 gene of Anaplasma ovis strains. Vet. Microbiol. 119:2–4 (2007), 375–381.
De la Fuente, J., Ayoubi, P., Blouin, E.F., Almazán, C., Naranjo, V., Kocan, K.M., Anaplasmosis: focusing on host-vector-pathogen interactions for vaccine development. Ann. N.Y. Acad. Sci. 1078:1 (2006), 416–423.
Djakaridja, B., Yao, K.P., Gragnon, B., Acapovi-Yao, G., Mavoungou, J., N'Goran, K., Situation épidémiologique des hémoparasites des bovins dans deux zones d’élevage de la Cote d'Ivoire: cas des anciennes régions des Savanes et de la vallée du Bandama. Rev. Méd. Vét. 165:9–10 (2014), 297–303.
Djiba, M.L., Mediannikov, O., Mbengue, M., Thiongane, Y., Molez, J.F., Seck, M.T., Fenollar, F., Raoult, D., Ndiaye, M., Survey of Anaplasmataceae bacteria in sheep from Senegal. Trop. Anim. Health Prod. 45 (2013), 1557–1561.
Dumler, J.S., Barbet, A.F., Bekker, C.P., Dasch, G.A., Palmer, G.H., Ray, S.C., Rikihisa, Y., Rurangirwa, F.R., Reorganization of genera in the families Rickettsiaceae and Anaplasmataceae in the order Rickettsiales: unification of some species of Ehrlichia with Anaplasma, Cowdria with Ehrlichia and Ehrlichia with Neorickettsia, descriptions of six new species combinations and designation of Ehrlichia equi and ‘HGE agent’ as subjective synonyms of Ehrlichia phagocytophila. Int. J. Syst. Evol. Microbiol. 51:6 (2001), 2145–2165, 10.1099/00207713-51-6-2145.
Franzén, P., Aspan, A., Egenvall, A., Gunnarsson, A., Åberg, L., Pringle, J., Acute clinical, hematologic, serologic, and polymerase chain reaction findings in horses experimentally infected with a European strain of Anaplasma phagocytophilum. J. Vet. Intern. Med. 19:2 (2005), 232–239.
Franzén, P., Berg, A.L., Aspan, A., Gunnarsson, A., Pringle, J.D., Death of a horse infected experimentally with Anaplasma phagocytophilum. Vet. Rec. 160:4 (2007), 122–125.
Friedhoff, K.T., Tick-borne diseases of sheep and goats caused by Babesia, Theileria or Anaplasma spp. Parassitologia 39:2 (1997), 99–109.
Ghai, R.R., Mutinda, M., Ezenwa, V.O., Limited sharing of tick-borne hemoparasites between sympatric wild and domestic ungulates. Vet. Parasitol. 226 (2016), 167–173.
Gharbi, M., Darghouth, M.A., A review of Hyalomma scupense (Acari, Ixodidae) in the Maghreb region: from biology to control. Parasite 21 (2014), 1–12.
Hornok, S., Elek, V., de La Fuente, J., Naranjo, V., Farkas, R., Majoros, G., Földvári, G., First serological and molecular evidence on the endemicity of Anaplasma ovis and A. marginale in Hungary. Vet. Microbiol. 122:3–4 (2007), 316–322.
Hornok, S., Sugár, L., Fernández de Mera, I.G., De La Fuente, J., Horváth, G., Kovács, T., Micsutka, A., Gönczi, E., Flaisz, B., Takács, N., Farkas, R., Tick-and fly-borne bacteria in ungulates: the prevalence of Anaplasma phagocytophilum, haemoplasmas and rickettsiae in water buffalo and deer species in Central Europe, Hungary. BMC Vet. Res. 14:1 (2018), 1–7.
Hurtado, O.J.B., Giraldo-Ríos, C., Economic and health impact of the ticks in production animals. Ticks Tick-Borne Pathog. 9 (2018), 1–9.
Hussain, M., Junaid, A., Gul, R., Jamal, M.A., Ahmed, I., Talpur, M.Z., Rahim, K., Fatima, M., Munir, S., First detection on prevalence of Anaplasma marginale in sheep and goat in Karak District, Pakistan. Asian Pac. J. Trop. Dis. 79 (2017), 531–535.
Jafar Bekloo, A., Ramzgouyan, M.R., Shirian, S., Faghihi, F., Bakhshi, H., Naseri, F., Sedaghat, M., Telmadarraiy, Z., Molecular characterization and phylogenetic analysis of Anaplasma spp. and Ehrlichia spp. isolated from various ticks in southeastern and northwestern regions of Iran. Vector-Borne Zoonotic Dis. 18:5 (2018), 252–257.
Jalali, S.M., Khaki, Z., Kazemi, B., Bandehpour, M., Rahbari, S., Razi Jalali, M., Yasini, S.P., Molecular detection and identification of Anaplasma species in sheep from Ahvaz, Iran. Iran. J. Vet. Res. 14:1 (2013), 50–56.
Kabbout, N., Merzoug, D., Chenchouni, H., Ecological status of phlebotomine sandflies (Diptera: Psychodidae) in rural communities of Northeastern Algeria. J. Arthropod-Borne Dis. 10 (2016), 24–38.
Kaewmongkol, G., Lukkana, N., Yangtara, S., Kaewmongkol, S., Thengchaisri, N., Sirinarumitr, T., Jittapalapong, S., Fenwick, S.G., Association of Ehrlichia canis, Hemotropic mycoplasma spp. and Anaplasma platys and severe anemia in dogs in Thailand. Vet. Microbiol. Vet. Microbiol. 201 (2017), 195–200.
Kasozi, K.I., Welburn, S.C., Batiha, G.E.S., Marraiki, N., Nalumenya, D.P., Namayanja, M., Matama, K., Zalwango, K.K., Matovu, W., Zirintunda, G., Ekou, J., Molecular epidemiology of anaplasmosis in small ruminants along a human-livestock-wildlife interface in Uganda. Heliyon, 7(1), 2021, e05688.
Kimura, M., A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16 (1980), 111–120.
Kocan, K.M., De La Fuente, J., Blouin, E.F., Garcia-Garcia, J.C., Anaplasma marginale (Rickettsiales: Anaplasmataceae): recent advances in defining host–pathogen adaptations of a tick-borne rickettsia. Parasitology 129:S1 (2004), S285–S300.
Kocan, K.M., de la Fuente, J., Guglielmone, A.A., Meléndez, R.D., Antigens and alternatives for control of Anaplasma marginale infection in cattle. Clin. Microbiol. Rev. 16:4 (2003), 698–712.
Kolo, A., Anaplasma Species in Africa—A Century of Discovery: A Review on Molecular Epidemiology, Genetic Diversity, and Control. Pathogens, 12(5), 2023, 702.
Kumar, S., Stecher, G., Li, M., Knyaz, C., Tamura, K., MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol. Biol. Evol. 35:6 (2018), 1547–1549.
Lee, S.H., Mossaad, E., Ibrahim, A.M., Ismail, A.A., Moumouni, P.F.A., Liu, M., Ringo, A.E., Gao, Y., Guo, H., Li, J., Efstratiou, A., Detection and molecular characterization of tick-borne pathogens infecting sheep and goats in Blue Nile and West Kordofan states in Sudan. Ticks Tick-Borne Dis. 9:3 (2018), 598–604.
Li, H., Zheng, Y.C., Ma, L., Jia, N., Jiang, B.G., Jiang, R.R., Huo, Q.B., Wang, Y.W., Liu, H.B., Chu, Y.L., Song, Y.D., Human infection with a novel tick-borne Anaplasma species in China: a surveillance study. Lancet Infect. Dis. 15:6 (2015), 663–670.
Li, Y., Chen, Z., Liu, Z., Liu, J., Yang, J., Li, Q., Li, Y., Luo, J., Yin, H., Molecular survey of Anaplasma and Ehrlichia of red deer and sika deer in Gansu, China in 2013. Transbound. Emerg. Dis. 63:6 (2016), e228–e236.
Lima, M.L.F., Soares, P.T., Ramos, C.A.N., Araújo, F.R., Ramos, R.A.N., Souza, I.I.F., Faustino, M.A.G., Alves, L.C.A., Molecular detection of Anaplasma platys in a naturally-infected cat in Brazil. Braz. J. Microbiol. 41 (2010), 381–385.
Liu, Z., Ma, M., Wang, Z., Wang, J., Peng, Y., Li, Y., Guan, G., Luo, J., Yin, H., Molecular survey and genetic identification of Anaplasma species in goats from central and southern China. Appl. Environ. Microb. 78:2 (2012), 464–470.
Lorusso, V., Wijnveld, M., Latrofa, M.S., Fajinmi, A., Majekodunmi, A.O., Dogo, A.G., Igweh, A.C., Otranto, D., Jongejan, F., Welburn, S.C., Picozzi, K., Canine and ovine tick-borne pathogens in camels, Nigeria. Vet. Parasitol. 228 (2016), 90–92.
Lorusso, V., Wijnveld, M., Majekodunmi, A.O., Dongkum, C., Fajinmi, A., Dogo, A.G., Thrusfield, M., Mugenyi, A., Vaumourin, E., Igweh, A.C., Jongejan, F., Tick-borne pathogens of zoonotic and veterinary importance in Nigerian cattle. Parasit. Vectors 9:1 (2016), 1–13.
Machado, R.Z., Teixeira, M.M.G., Rodrigues, A.C., André, M.R., Gonçalves, L.R., Barbosa da Silva, J., Pereira, C.L., Molecular diagnosis and genetic diversity of tick-borne Anaplasmataceae agents infecting the African buffalo Syncerus caffer from Marromeu Reserve in Mozambique. Parasit. Vectors 9:1 (2016), 1–9.
Maggi, R.G., Mascarelli, P.E., Havenga, L.N., Naidoo, V., Breitschwerdt, E.B., Co-infection with Anaplasma platys, Bartonella henselae and Candidatus Mycoplasma haematoparvum in a veterinarian. Parasit. Vectors 6:1 (2013), 1–10.
Mediannikov, O., Fenollar, F., Looking in ticks for human bacterial pathogens. Microb. Pathog. 77 (2014), 142–148.
Ogden, N.H., Casey, A.N.J., Woldehiwet, Z., French, N.P., Transmission of Anaplasma phagocytophilum to Ixodes ricinus ticks from sheep in the acute and post-acute phases of infection. Infect. Immun. 71:4 (2003), 2071–2078.
Parola, P., Raoult, D., Ticks and tickborne bacterial diseases in humans: an emerging infectious threat. Clin. Infect. Dis. 32:6 (2001), 897–928.
Pereira, A., Parreira, R., Nunes, M., Casadinho, A., Vieira, M.L., Campino, L., Maia, C., Molecular detection of tick-borne bacteria and protozoa in cervids and wild boars from Portugal. Parasit. Vectors 9 (2016), 1–9.
Rar, V., Golovljova, I., Anaplasma, Ehrlichia, and “Candidatus Neoehrlichia” bacteria: pathogenicity, biodiversity, and molecular genetic characteristics, a review. Infect. Genet. Evol. 11:8 (2011), 1842–1861.
Rar, V., Tkachev, S., Tikunova, N., Genetic diversity of Anaplasma bacteria: twenty years later. Infect. Genet. Evol., 91, 2021, 104833.
Renneker, S., Abdo, J., Salih, D.E.A., Karagenç, T., Bilgiç, H., Torina, A., Oliva, A.G., Campos, J., Kullmann, B., Ahmed, J., Seitzer, U., Can Anaplasma ovis in small ruminants be neglected any longer?. Transbound. Emerg. Dis. 60 (2013), 105–112.
Rjeibi, M.R., Ayadi, O., Rekik, M., Gharbi, M., Molecular survey and genetic characterization of Anaplasma centrale, A. marginale and A. bovis in cattle from Algeria. Transbound. Emerg. Dis. 65:2 (2018), 456–464.
Rodríguez, R., Ojeda, M., Pérez, L., Rosado, J., 2011. Epidemiología y control de Rhipicephalus (Boophilus) microplus en México. In: Quiroz H, Figueroa J, Ibarra F, López M, (eds). Epidemiología de Enfermedades Parasitarias en Animales Domésticos. México: UNAM, pp. 477–504.
Sadeddine, R., Diarra, A.Z., Laroche, M., Mediannikov, O., Righi, S., Benakhla, A., Dahmana, H., Raoult, D., Parola, P., Molecular identification of protozoal and bacterial organisms in domestic animals and their infesting ticks from north-eastern Algeria. Ticks Tick-borne Dis., 11(2), 2020, 101330.
Shabana, I.I., Alhadlag, N.M., Zaraket, H., Diagnostic tools of caprine and ovine anaplasmosis: a direct comparative study. BMC Vet. Res. 14:1 (2018), 1–8.
Shoaib, M., Rashid, M.I., Akbar, H., Sheikh, A.A., Farooqi, S.H., Khan, M.A., Khan, F.A., Khan, R., Prevalence and molecular characterization of Anaplasma marginale in cattle population of Khyber Pakhtunkhwa Province, Pakistan. Int. J. Agric. Biol. 25:5 (2021), 1016–1023.
Singh, H., Haque, M., Singh, N.K., Rath, S.S., Molecular detection of Anaplasma marginale infection in carrier cattle. Ticks Tick-Borne Dis. 3:1 (2012), 55–58, 10.1016/j.ttbdis.2011.10.002.
Soosaraei, M., Haghi, M.M., Etemadifar, F., Fakhar, M., Teshnizi, S.H., Asfaram, S., Esboei, B.R., Status of Anaplasma spp. infection in domestic ruminants from Iran: a systematic review with meta-analysis. Parasit. Epidemiol. Control, 11, 2020 p.e00173.
Stoltsz, W.H., Ovine and caprine anaplasmosis. Infectious diseases of livestock, Volume One, (Ed. 2), 2004, Tustin RC, Coetzer J, 617–624.
Stuen, S., Nevland, S., Moum, T., Fatal cases of tick-borne fever (TBF) in sheep caused by several 16S rRNA gene variants of Anaplasma phagocytophilum. Ann. N.Y. Acad. Sci. 990:1 (2003), 433–434.
Tanveer, M., Farooq, M., Amjad, M., Asif, M., Kashif, M., Latif, M., Khan, A., Aktas, M., Said, M.B., Iqbal, F., Molecular prevalence, associated risk factors and phylogeny of Anaplasma marginale, Theileria ovis and T. lestoquardi in sheep from Pakistan. Comp. Immunol. Microbiol. Infect. Dis., 86, 2022, 101822.
Taylor, M., Coop, R., Wall R., 2016.Veterinary entomology. In: Taylor, M., Coop, R., Wall, R. (eds.) Veterinary Parasitology. 4th ed. UK: Wiley-Blackwell, pp. 161–258.
Thrusfield, M., Veterinary Epidemiology 3rd ed, 2007, 227–247.
Tumwebaze, M.A., Lee, S.H., Moumouni, P.F.A., Mohammed-Geba, K., Sheir, S.K., Galal-Khallaf, A., Abd El Latif, H.M., Morsi, D.S., Bishr, N.M., Galon, E.M., Byamukama, B., First detection of Anaplasma ovis in sheep and Anaplasma platys-like variants from cattle in Menoufia governorate, Egypt. Parasitol. Int., 78, 2020, 102150.
Tuomi, J., Experimental studies on bovine tick-borne fever. 1. Clinical and haematological data, some properties of the causative agent, and homologous immunity. Acta Pathol. Acta Pathol. Microbiol. Scand. 70:3 (1967), 429–445.
Woldehiwet, Z., In-vitro studies on the susceptibility of ovine strains of Anaplasma phagocytophilum to antimicrobial agents and to immune serum. J. Comp. Pathol. 143:2–3 (2010), 94–100.
Worthington, R.W., Bigalke, R.D., A review of the infectious diseases of African wild ruminants. Onderstepoort J. Vet. Res. 68 (2001), 291–323.
Yabsley, M.J., Davidson, W.R., Stallknecht, D.E., Varela, A.S., Swift, P.K., Devos, J.C. Jr., Dubay, S.A., Evidence of tick-borne organisms in mule deer (Odocoileus hemionus) from the Western United States. Vector-Borne Zoonotic Dis. 5:4 (2005), 351–362.
Yousefi, A., Rahbari, S., Shayan, P., Sadeghi-dehkordi, Z., Bahonar, A., Molecular detection of Anaplasma marginale and Anaplasma ovis in sheep and goat in west highland pasture of Iran. Asian Pac. J. Trop. Biomed. 7:5 (2017), 455–459.
