Molecular detection of anaplasma marginale in ticks naturally feeding on cattle

Abstract

The present study was carried out to morphological investigation of ticks naturally feeding on cattle, and molecular detection of A. marginale in these ticks using the conventional polymerase chain reaction (PCR) assay. Totally 25 infested cattle with ticks were selected from rural areas in Wasit province / Iraq, during March-2020 to June-2020. The findings of clinical observation reported that ticks were distributed onto different bodily parts; udder and testis (50.3%), neck (15.98%), perineal region (28.4%), and ear (5.33%). Although hard (Ixodid) tick was the only type detected, two species of different genera were identified among infested cattle; Hyalomma anatolicum (75.15%), and Rhipicephalus sanguineus (24.85%). Regarding tick species, H. anatolicum was more prevalent (P<0.05) than R. sanguineus in neck (18.11%) region; whereas, R. sanguineus was prevalent significantly (P<0.05) in udder and testis (61.9%) compared to H. anatolicum. Regarding bodily regions, H. anatolicum and R. sanguineus were prevalent significantly (P<0.05) in udder and testis (75.15% and 61.9% respectively). Also, the range and mean number of ticks on each animal was 2-34 and 12.59 respectively. Based on the life stage of collected study ticks, 47.93%, 33.73%, and 18.34% were male, female, and nymph, respectively. Ticks of each study cattle were considered as a one sample and subjected collectively to DNA extraction. Hence, the overall findings for testing 25 samples of ticks by PCR revealed that 4 (16%) of samples were positives for msp1β gene specific to A. marginale. Additionally, male Hyalomma anatolicum ticks were the only positives for A. marginale isolates.

References

  • Al-AbediG J K,and Al-Amery A M A (2020) Molecular Diagnosis and Phylogenetic Analysis of Babesia Species Isolated from Ticks of Infested Cattle in Wasit Governorate, Iraq. Iraqi Journal of Agricultural Sciences, 51 (5), 1249-1260.
  • Al-Fatlawi M S H, and Al-Fatlawi M A A (2019). Molecular and phylogenetic study of Theileria SPP isolated from ticks in AL-Diwaniyah city, Iraq. The Iraqi Journal of Agricultural Science, 50(1), 475-479.
  • Aubry P, and Geale D W, (2011). A review of bovine anaplasmosis. Transboundary and emerging diseases, 58(1), 1-30.
  • Banafshi O, Hanafi-Bojd A A, Karimi M, Faghihi F, Beik-Mohammadi M, Gholami S, and Telmadarraiy Z. (2018). Tick ectoparasites of animals in borderline of Iran-Iraq and their role on disease transmission. Journal of Arthropod-Borne Diseases, 12(3), 252.
  • Battilani M, De Arcangeli S, Balboni A, and Dondi F. (2017). Genetic diversity and molecular epidemiology of Anaplasma. Infection, Genetics and Evolution, 49, 195-211.
  • Berman A. (2011). Invited review: Are adaptations present to support dairy cattle productivity in warm climates?. Journal of Dairy Science, 94(5), 2147-2158.
  • Bilgiç H B, Karagenç T, Simuunza M, Shiels B, Tait A, Eren H, and Weir W. (2013). Development of a multiplex PCR assay for simultaneous detection of Theileria annulata, Babesia bovis and Anaplasma marginale in cattle. Experimental Parasitology, 133(2), 222-229.
  • Blouin E F, and Kocan K M. (1998). Morphology and development of Anaplasma marginale (Rickettsiales: Anaplasmataceae) in cultured Ixodes scapularis (Acari: Ixodidae) cells. Journal of medical entomology, 35(5), 788-797.
  • Carelli G, Decaro N, Lorusso A, Elia G, Loruss E, Mari V, and Buonavoglia C. (2007). Detection and quantification of Anaplasma marginale DNA in blood samples of cattle by real-time PCR. Veterinary microbiology, 124(1-2), 107-114.
  • Carvalho W A, Ianella P, Arnoldi FG, Caetano A R, Maruyama SR, Ferreira B R, and de Miranda Santos I KF (2011). Haplotypes of the bovine IgG2 heavy gamma chain in tick-resistant and tick-susceptible breeds of cattle. Immunogenetics, 63(5), 319-324.
  • da Silva J B, da Fonseca A H, and Barbosa JD (2015). Molecular characterization of Anaplasma marginale in ticks naturally feeding on buffaloes. Infection, Genetics and Evolution, 35, 38-41.
  • de Echaide S T, Knowles D P, McGuire T C, Palmer G H, Suarez C E and McElwain T F (2001). Detection of Cattle Naturally Infected with Anaplasma marginale in a Region of Endemicity by Nested PCR and a Competitive Enzyme-Linked Immunosorbent Assay Using Recombinant Major Surface Protein 5. Journal of Clinical Microbiology, 39(3), 1207.
  • de la Fuente J, Blouin E F, Manzano-Roman R, Naranjo V, Almazán C, de la Lastra J M P and Kocan K M (2007). Functional genomic studies of tick cells in response to infection with the cattle pathogen, Anaplasma marginale. Genomics, 90(6), 712-722.
  • Eisen L, Eisen R J, and Lane R S (2014). Geographical distribution patterns and habitat suitability models for presence of host-seeking ixodid ticks in dense woodlands of Mendocino County, California. Journal of medical entomology, 43(2), 415-427.
  • Goff W, Barbet A, Stiller D, Palmer G, Knowles D, Kocan K, and McGuire T. (1988). Detection of Anaplasma-marginale-infected tick vectors by using a cloned DNA probe. Proceedings of the National Academy of Sciences, 85(3), 919-923.
  • Hasson R H (2012). Tick distribution and infestation among sheep and cattle in Baghdad’s south suburb. Kufa Journal For Veterinary Medical Sciences, 3(1), 77-90.
  • Iqbal A, Sajid M S, Khan M N, and Khan M K, (2013). Frequency distribution of hard ticks (Acari: Ixodidae) infesting bubaline population of district Toba Tek Singh, Punjab, Pakistan. Parasitology research, 112(2), 535-541.
  • Janbakhsh B. (1957). A research review about ticks responsible for relapsing fever in Iran. Journal of Faculty of Health and Institute of Public Health and Research, 484, 223-230.
  • Jonsson N N, Piper E K, and Constantinoiu C C (2014). Host resistance in cattle to infestation with the cattle tick R hipicephalus microplus. Parasite Immunology, 36(11), 553-559.
  • Khalaf J M, Mohammed I A, and Karim A J, (2018). The epidemiology of tick in transmission of Enterobacteriaceae bacteria in buffaloes in Marshes of the south of Iraq. Veterinary world, 11 (12), 1677.
  • Kocan K M, de la Fuente J, Blouin E F, Coetzee J F, and Ewing S A, (2010). The natural history of Anaplasma marginale. Veterinary parasitology, 167(2-4), 95-107.
  • Kocan K M, De La Fuente J, Blouin E F, and Garcia-Garcia J C (2002). Adaptations of the tick-borne pathogen, Anaplasma marginale, for survival in cattle and ticks. Experimental and applied acarology, 28(1-4), 9-25.
  • Kocan K M, De la Fuente J, Guglielmone A A, and Meléndez R D, (2003). Antigens and alternatives for control of Anaplasma marginale infection in cattle. Clinical microbiology reviews, 16(4), 698-712.
  • Kocan K M, Stiller D, Goff W L, Claypool P L, Edwards W, Ewing S A, and Barron S J (1992). Development of Anaplasma marginale in male Dermacentor andersoni transferred from parasitemic to susceptible cattle. American journal of veterinary research, 53(4), 499-507.
  • Liu X Y and Bonnet S I (2014). Hard tick factors implicated in pathogen transmission. PLoS Negl Trop Dis, 8(1), e2566.
  • Moghaddam A G, Seyed M R, Rasouli M, Hosseinzade S, Darvishi MM, Rakhshanpour A, and Rahimi M T (2014). Survey on cattle ticks in Nur, north of Iran. Asian Pacific journal of tropical biomedicine, 4(3), 209-212.
  • Molad T, Mazuz ML, Fleiderovitz L, Fish L, Savitsky I, Krigel Y, and Shkap V. (2006). Molecular and serological detection of A. centrale-and A. marginale-infected cattle grazing within an endemic area. Veterinary microbiology, 113(1-2), 55-62.
  • Monfared A L, Mahmoodi M, and Fattahi R (2015). Prevalence of ixodid ticks on cattle, sheep and goats in Ilam County, Ilam Province, Iran. Journal of parasitic diseases, 39 (1), 37-40.
  • Nair A S, Ravindran R, Lakshmanan B, Sreekumar C, Kumar S S, Raju R, and Saseendranath M R. (2013). Bovine carriers of Anaplasma marginale and Anaplasma bovis in South India. Trop Biomed, 30 (1), 105-12.
  • Ndhlovu D N, Makaya P V, and Penzhorn B L, (2009). Tick infestation, and udder and teat damage in selected cattle herds of Matabeleland South, Zimbabwe. Onderstepoort Journal of Veterinary Research, 76(2), 235-248.
  • Palmer GH. (2009). Sir Arnold Theiler and the discovery of anaplasmosis: a centennial perspective. Onderstepoort Journal of Veterinary Research, 76(1), 75-79.
  • Quiroz-Castañeda E R, Amaro-Estrada I, and Rodríguez-Camarillo S D (2016). Anaplasma marginale: diversity, virulence, and vaccine landscape through a genomics approach. BioMed research international, 2016.
  • Rajput Z I, Hu S H, Arijo A G, Habib M, and Khalid M (2005). Comparative study of Anaplasma parasites in tick carrying buffaloes and cattle. Journal of Zhejiang University. Science. B, 6(11), 1057.
  • Regasa T D, KebedeTsegay A, and Waktole H (2015). Prevalence of major ectoparasites of calves and associated risk factors in and around Bishoftu town. African Journal of Agricultural Research, 10(10), 1127-1135.
  • Rehman A, Nijhof A M, Sauter-Louis C, Schauer B, Staubach C and Conraths F J. (2017). Distribution of ticks infesting ruminants and risk factors associated with high tick prevalence in livestock farms in the semi-arid and arid agro-ecological zones of Pakistan. Parasites and vectors, 10(1), 190.
  • Ribeiro M F B and Lima J D (1996). Morphology and development of Anaplasma marginale in midgut of engorged female ticks of Boophilus microplus. Veterinary parasitology, 61(1-2), 31-39.
  • Sajid M S, Iqbal Z, Khan M N, Muhammad G, Needham G, and Khan M K (2011). Prevalence, associated determinants, and in vivo chemotherapeutic control of hard ticks (Acari: Ixodidae) infesting domestic goats (Capra hircus) of lower Punjab, Pakistan. Parasitology research, 108(3), 601-609.
  • Sophia P, Battsetseg G, Kass Philip H, and Foley Janet E (2013). Detection and Epidemiology of Tick-Borne Pathogens in Free-Ranging Livestock in Mongolia. Journal of Clinical & Experimental Pathology, 1, 2161-0681.
  • Tajedin L, Bakhshi H, Faghihi F, and Telmadarraiy Z. (2016). High infection of Anaplasma and Ehrlichia spp. among tick species collected from different geographical locations of Iran. Asian Pacific Journal of Tropical Disease, 6(10), 787-792.
  • Tessema T, and Gashaw A. (2010). Prevalence of ticks on local and crossbred cattle in and around Asella town, southeast Ethiopia. Ethiopian Veterinary Journal, 14(2), 79-89.
  • Torina A, Agnone A, Blanda V, Alongi A, D’Agostino R, Caracappa S, and de la Fuente J. (2012). Development and validation of two PCR tests for the detection of and differentiation between Anaplasma ovis and Anaplasma marginale. Ticks and tick-borne diseases, 3(5-6), 283-287.
  • Vimonish R, Johnson W C, Mousel M R, Brayton K A, Scoles G A, Noh SM, and Ueti M W (2020). Quantitative analysis of Anaplasma marginale acquisition and transmission by Dermacentor andersoni fed in vitro. Scientific reports, 10(1), 1-9.
  • Walker AR (2003). Ticks of domestic animals in Africa: a guide to identification of species. Bioscience Reports, Edinburgh. Pp: 3-210.
  • Wikel SK (2018). Ticks and tick-borne infections: complex ecology, agents, and host interactions. Veterinary sciences, 5(2), 60-81.
  • Yasini S P, Khaki Z, Rahbari S, Kazemi B, Amoli JS, Gharabaghi A, and Jalali SM. (2012). Hematologic and clinical aspects of experimental ovine anaplasmosis caused by Anaplasma ovis in Iran. Iranian journal of parasitology, 7(4), 91.
  • Ybanez A P, Sivakumar T, Battsetseg B, Battur B, Altangerel K, Matsumoto K, and Inokuma H (2012). Specific molecular detection and characterization of Anaplasma marginale in Mongolian cattle. Journal of Veterinary Medical Science, 12-0361.
  • Yu P, Liu Z, Niu Q, Yang J, Abdallah M O, Chen Z, and Yin H. (2017). Molecular evidence of tick-borne pathogens in Hyalomma anatolicum ticks infesting cattle in Xinjiang Uygur Autonomous Region, Northwestern China. Experimental and Applied Acarology, 73(2), 269-281.

License

This is an open access article distributed under the Creative Commons Attribution License which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.