Molecular identification of Anaplasma phagocytophilum in cattle and sheep of Gilan province
Subject Areas :
Veterinary Clinical Pathology
nasrollah Vahedi Nouri
1
(
Assistant Professor, Parasitic Diseases Research Department, Razi Vaccine and Serum Research Institute, Agricultural Research, Education and Extension Organization (AREEO), Karaj, Iran.
)
Vahid Noaman
2
(
Associate Professor, Parasitic Diseases Research Department, Razi Vaccine and Serum Research Institute, Agricultural Research, Education and Extension Organization (AREEO), Karaj, Iran.
)
Ebrahim Rahimabadi
3
(
Instructor, Parasitic Diseases Research Department, Razi Vaccine and Serum Research Institute, Agricultural Research, Education and Extension Organization (AREEO), Karaj, Iran.
)
Received: 2020-07-28
Accepted : 2020-12-23
Published : 2020-10-22
Keywords:
Sheep,
cattle,
Gilan,
Molecular identification,
Anaplasma phagocytophilum,
Abstract :
Anaplasma phagocytophilum is one of the emerging pathogenic bacteria transmitted by mites, which causes zoonotic disease, between humans and many animals. Hence, its importance in public health is significant. The aim of this study was molecular identification of Anaplasma phagocytophilum in cattle and sheep of Gilan province. For this purpose, during 2018, 200 blood samples of cattle, and 200 blood samples from sheep were collected randomly via the jugular vein from different parts of Gilan province. The extracted DNA from blood cells were amplified by Anaplasma-all primers, which amplify an approximately 1468bp DNA fragment from region of 16S rRNA gene from various members of the genus Anaplasma. All 70 bovine positive specimens wereanalyzed for the presence of A. phagocytophilum with proprietary nested-PCRand 66 of blood samples (33%) were positive for A. phagocytophilum. In addition, 38 sheeppositive samples with proprietary nested-PCR wereanalysed for the presence of A.phagocytophilum and 10 of sheep blood samples (5%) were positive for A. phagocytophilum. The chi-squaretest was used to compare the percentage of A.phagocytophilum contamination of cattle and sheep in association with different seasons, different ages, animal gender, sea level, carriers and type of animal husbandry (semi-industrial-traditional). The results of this comparison indicated that only the abundance of A. phagocytophilum in sheep of Gilan province had a significant difference between the first and second half of the year (p <0.05). The results of this study showed that A.phagocytophilum is a common species of Anaplasma in livestock of Gilan province. Given the role of this species in the occurrence of granulocytic anaplasmosis in humans, this issue is important in terms of public health.
References:
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●Annen, K., Friedman, K., Eshoa, C., Horowitz, M., Gottschall, J. and Straus, T. (2012) Two cases of transfusion-transmitted Anaplasma phagocytophilum. American Journal of Clinical Pathology, 137(4): 562-565
● Barlough, J.E., Madigan, J.E., DeRock, E. and Bigornia, L. (1996). Nested polymerase chain reaction for detection of Ehrlichia equi genomic DNA in horses and ticks (Ixodes pacificus). Veterinary Parasitology, 63(3-4): 319-329.
● Bashiribod, H, Kazemi, K., Eslami, G., Bigdeli, S., Bandehpour, M., Rahbarian, N., et al. (2004). First molecular detection of Anaplasma phagocytophilum in Ixodes ricinus ticks in Iran. Journal of Medical Sciences, 4(4): 282-286.
●Ben Said, M.B., Belkahia, H. and Messadi, L. (2018). Anaplasma spp. in North Africa: a review on molecular epidemiology, associated risk factors and genetic characteristics. Vector-borne and zoonotic diseases, 9(3): 543-555.
● de la Fuente, J., Estrada-Peña, A., Cabezas-Cruz, A. and Kocan, K.M. (2016). Anaplasmaphagocytophilum uses common strategies for infection of ticks and vertebrate hosts. Trends in Microbiology, 24(3): 173-180.
● de la Fuente, J., Naranjo, V., Ruiz- Fons, F., Hofle, U., Fernandez De Mera, I.G., Villanua, D., et al. (2005b). Potential vertebrate reservoir hosts and in vertebrate vectors of Anaplasma marginale and A. phagocytophilum in central Spain. Vector Borne Zoonotic Diseases, 5(4): 390-401.
● Eisawi, N., El Hussein, A., Hassan, D., Musa, A., Hussien, M., Enan, K., et al. (2020) A molecular prevalence survey on Anaplasma infection among domestic ruminants in Khartoum State, Sudan. Tropical Animal Health and Production, 52(4): 1845-1852.
● Elhassan, A.M., Mansour, M.E.A., Shamon, A.A.A., and El Hussein, A.M. (2014) A Serological Survey of Akabane Virus Infection in Cattle in Sudan. ISRN. Veterinary Science, 2014: 123904.
●Gaowa Yoshikawa, Y., Ohashi, N., Wu, D., Kawamori, F., Ikegaya, A., Watanabe, T., et al. (2014). Anaplasma phagocytophilum antibodies in humans, Japan, 2010-2011. Emerging Infectious Diseases, 20(3): 508-509.
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● Hayder N.A., Yahia I.K. and Qassim H.K. (2019). Molecular detection and phylogenetic analysis of Anaplasma spp in cattle in Al-Qadisiyah province of Iraq. Macedonian Veterinary Review, 42(2): 181-188.
● Hamzah, K.J. and Hasso, S.A. (2019). Molecular prevalence of Anaplasma phagocytophilum in sheep from Iraq. Open Veterinary Journal, 9(3): 238-245.
● Hanène, B., Mourad, B.S., Alberto, A., Khaoula, A.Z.I., Dorra, H., Mohamed, G., et al. (2015). First molecular survey and novel genetic variants’ identification of Anaplasma marginale, A.centrale and A.bovis in cattle from Tunisia. Infection, Genetics and Evolution, 34(1): 361-371.
● Hofmann-Lehmann, R., Meli, M.L., Dreher, U.M., Gonczi, E., Deplazes, P., Braun, U., et al. (2004). Concurrent infections with vector-borne pathogens associated with fatal hemolytic anemia in a cattle herd in Switzerland. Journal of Clinical Microbiology, 42(8): 3775-3780.
● Hosseini-Vasoukolaei, N., Oshaghi, M.A., Shayan, P., Vatandoost, H., Babama hmoudi, F., Yaghoobi -Ershadi, M.R., et al. (2014). Anaplasma Infection in ticks, livestock and human in Ghaemshahr, Mazandaran province, Iran. Iranian Journal of Arthropod Borne Disease, 8(2): 204-211.
● Hulínská, D., Langøová, K., Pejèoch, M., and Pavlásek, I. (2004). Detection of Anaplasmaphagocytophilum in animals by real-time polymerase chain reaction. Journal of Pathology, Microbiolgy and Immunology, 112(4-5): 239-247.
● Jalali, S.M., Khaki, Z., Kazemi, B., Bandehpour, M., Rahbari, S., Jalali M.R., et al. (2013). Molecular detection and identification of Anaplasma species in sheep from Ahvaz, Iran. Iranian Journal of Veterinary Research, 14(1): 50-56.
● Kiilerich, A.M., Christensen, H. and Thamsborg, S.M. (2009). Anaplasma phagocytophilum in Danish sheep: confirmation by DNA sequencing. Acta Veterinaria Scandinnavia, 51(1): 55.
● Kocan, K.M., de la Fuente, J., Guglielmone, A.A. and Melendez, R.D. (2003). Antigens and alternatives for control of Anaplasma marginale infection in cattle. Clinical Microbiology Reviews, 16(4): 698-712.
● Laloy, E., Petit, E., Boulouis, H.J., Gandoin, C., Bouillin, C., Gounot, G., et al. (2009). Dynamics of natural infection by Anaplasma phagocytophilum in a dairy cattle herd in Brittany, France. Clinical Microbiology and Infection, 15(2): 24-25.
● Leatch, G. (1973). Preliminary studies on the transmission of Anaplasma marginale by Boophilusmicroplus. Australian Veterinary Journal, 49(1): 16-19.
● Muhammad, S.S., Rao Muhammmad, S.S., Ahmad Khan, Z.I. and Muhammad, N.K. (2014). Prevalence and Risk Factors of Anaplasmosis in Cattle and Buffalo Populations of District Khanewal, Punjab, Pakistan. Global Veterinaria, 12(1): 146-153.
● Noaman, V. (2017) A review of anaplasmosis and the prevalence of Anaplasma marginale in cattle in Iran and the world. Veterinary Researches & Biological Products, 116(3): 2-15. [In Persian]
● Noaman, V. (2019). A review on Anaplasma phagocytophilum as a zoonotic agent. Tehran University Medical Journal, 76(12): 778-785. [In Persian]
● Noaman, V., Allameh, S.K. and Nabavi, R. (2017). Anaplasmosis in Ruminants of Iran: An Overview. Advanced Techniques in Clinical Microbiology, 1(2): 1-3.
● Noaman, V. and Moradi, M. (2019). Molecular epidemiology and risk factors assessment of Anaplasma spp. on dairy cattle in Southwest of Iran. Acta Veterinaria Eurasia, 45(1): 30-36.
● Noaman, V., Nabinejad, A., Shahmoradi, A. and Esmaeilkhanian, S. (2016). Molecular detection of bovine leukocytic Anaplasma species in Isfahan, Iran. Research in Molecular Medicine, 4(2): 47-51.
●Noaman, V. and Shayan, P. (2010). Comparison of Microscopy and PCR-RFLP for detection of Anaplasma marginale in carrier cattle. Iranian Journal of Microbiology, 2(2): 89-94.
● Ooshiro, M., Zakimi, S., Matsukawa, Y., Katagiri, Y. and Inokuma, H. (2008). Detection of Anaplasma bovis and Anaplasma phagocytophilum from cattle on Yonaguni Island, Okinawa, Japan. Veterinary Parasitology, 154(3-4): 360-364.
● Razmi, G.R., Dastjerdi, K., Hosseini, H., Naghibi, A., Barati, F. and Aslani, M.R. (2006). An epidemiological study on Anaplasma infection in cattle, sheep and goats in Mashhad suburb, Khorasan province, Iran. Annals of the New York Academy of Sciences, 1078(1): 479-481.
● Salehi-Guilandeh, S., Sadeghi-Dehkordi, Z., Sadeghi Nasab, A. and Yousefi, A. (2018). Molecular detection of Anaplasma spp. in cattle of Talesh County, North of Iran. Bulgarian Journal of Veterinary Medicine, 22(4): 457-465.
● Scharf, W., Schauer, S., Freyburger, F., Petrovec, M., Schaarschmidt- Kiener, D., Liebisch, G., et al. (2011). Distinct host species correlate with Anaplasma phagocytophilum ankA gene clusters. Journal of Clinical Microbiology, 49(3): 790-796.
● Stuen, S., Granquist, E.G. and Silaghi, C. (2013). Anaplasma phagocytophilum: a widespread multi-host pathogen with highly adaptive strategies. Frontiers in Cellular and Infection Microbiology, 3(3): 31.
● Stuen, S., Pettersen, K.S., Granquist, E.G., Bergström, K., Bown, K.J. and Birtles, R.J. (2013). Anaplasma phagocytophilum variants in sympatric red deer (Cervus elaphus) and sheep in southern Norway. Ticks and Tick Borne Disease, 4(3):197-201.
● Stuen S., Torsteinbo, W.O., Bergstrom, K. and Bardsen, K. (2009). Superinfection occurs in Anaplasmaphagocytophilum infected sheep irrespective of infection phase and protection status. Acta Veterinaria Scandinavica, 51(41): 1-6.
● Tay, S.T., Koh, F.X., Kho, K.L. and Ong, B.L. (2014). Molecular survey and sequence analysis of Anaplasma spp. in cattle and ticks in a Malaysian farm. Tropical Biomedicine, 31(4): 769-776.
● Torina, A. and Caracappa, S. (2007). Anaplasmosis in cattle in Italy. Veterinary Research Communications, 31(1): 73-78.
● Torina, A., Alongi, A., Naranjo, V., Scimeca, S., Nicosia, S., Di Marco, V., et al. (2008b). Characterization of Anaplasma infections in Sicily, Italy. Annals of the New York Academy of Sciences, 1149(1): 90-93.
●Torina, A., Galindo, R.C., Vicente, J., Di Marco, V., Russo, M., Aronica, V., et al. (2010). Characterization of Anaplasma phagocytophilum and A. ovis infection inanaturally infected sheep flock with poor health condition. Tropical Animal Health and Production, 42(7): 1327-31.
● Vahedi Noori, N. and Noaman, V. (2020). Molecular Identification of Anaplasma pathogenic species in Sheep in Mazandaran Province. Veterinary Researches & Biological Products, 33(2): 29-41. [In Persian]
●Weisburg, W.G., Barns, S.M., Pelletier, D.A. and Lane, D.J. )1991(. 16S ribosomal DNA amplification for phylogenetic study. Journal of Bacteriology, 173(2): 697-703.
● Yang, J., Liu, Z., Niu, Q., Liu, G., Han, R., Guan, G., et al. (2016). Anaplasma phagocytophilum in sheep and goats in central and southeastern China. Parasites and Vectors, 9(593): 1-7
●Yang, J., Liu, Z., Guan, G., Liu, Q., Li, Y., Chen, Z., et al. (2013). Prevalence of Anaplasmaphagocytophilum in ruminants, rodents and ticks in Gansu, North-Western China. Journal of Medical Microbiology, 62(2): 254-258.
●Yousefi, A., Rahbari, S., Shayan, P., Sadeghi-Dehkordi, Z. and Ahomar, A.B. (2017). Molecular evidence of Anaplasma phagocytophilum: An emerging tick-borne pathogen in domesticated small ruminant of Iran; first report. Comparative Clinical Pathology, 26(3): 637-642.
_||_Ahmadi-Hamedani, M., Khaki, Z., Rahbari, S., Kazemi, B. and Bandehpour, M. (2009). Molecular identification of anaplasmosis in goats using a new PCR-RFLP method. Iranian Journal of Veterinary Research, 10(29): 367-372.
● Aktas, M. and Özübek, S. (2015). Bovine anaplasmosis in Turkey: First laboratory confirmed clinical cases caused by Anaplasma phagocytophilum. Veterinary Microbiology, 178(3-4): 246-251.
● Awad, H., Antunes, S., Galindo, R.C., do Rosario, V.E., de la Fuente, J., Domingos, A., et al. (2011) Prevalence and genetic diversity of Babesia and Anaplasma species in cattle in Sudan, Veterinary Parasitology, 181(2-4): 146-152.
●Annen, K., Friedman, K., Eshoa, C., Horowitz, M., Gottschall, J. and Straus, T. (2012) Two cases of transfusion-transmitted Anaplasma phagocytophilum. American Journal of Clinical Pathology, 137(4): 562-565
● Barlough, J.E., Madigan, J.E., DeRock, E. and Bigornia, L. (1996). Nested polymerase chain reaction for detection of Ehrlichia equi genomic DNA in horses and ticks (Ixodes pacificus). Veterinary Parasitology, 63(3-4): 319-329.
● Bashiribod, H, Kazemi, K., Eslami, G., Bigdeli, S., Bandehpour, M., Rahbarian, N., et al. (2004). First molecular detection of Anaplasma phagocytophilum in Ixodes ricinus ticks in Iran. Journal of Medical Sciences, 4(4): 282-286.
●Ben Said, M.B., Belkahia, H. and Messadi, L. (2018). Anaplasma spp. in North Africa: a review on molecular epidemiology, associated risk factors and genetic characteristics. Vector-borne and zoonotic diseases, 9(3): 543-555.
● de la Fuente, J., Estrada-Peña, A., Cabezas-Cruz, A. and Kocan, K.M. (2016). Anaplasmaphagocytophilum uses common strategies for infection of ticks and vertebrate hosts. Trends in Microbiology, 24(3): 173-180.
● de la Fuente, J., Naranjo, V., Ruiz- Fons, F., Hofle, U., Fernandez De Mera, I.G., Villanua, D., et al. (2005b). Potential vertebrate reservoir hosts and in vertebrate vectors of Anaplasma marginale and A. phagocytophilum in central Spain. Vector Borne Zoonotic Diseases, 5(4): 390-401.
● Eisawi, N., El Hussein, A., Hassan, D., Musa, A., Hussien, M., Enan, K., et al. (2020) A molecular prevalence survey on Anaplasma infection among domestic ruminants in Khartoum State, Sudan. Tropical Animal Health and Production, 52(4): 1845-1852.
● Elhassan, A.M., Mansour, M.E.A., Shamon, A.A.A., and El Hussein, A.M. (2014) A Serological Survey of Akabane Virus Infection in Cattle in Sudan. ISRN. Veterinary Science, 2014: 123904.
●Gaowa Yoshikawa, Y., Ohashi, N., Wu, D., Kawamori, F., Ikegaya, A., Watanabe, T., et al. (2014). Anaplasma phagocytophilum antibodies in humans, Japan, 2010-2011. Emerging Infectious Diseases, 20(3): 508-509.
● Grøva, L., Olesen, I., Steinshamn, H. and Stuen, S. (2011). Prevalence of Anaplasma phagocytophilum infection and effect on lamb growth. Acta Veterinaria Scandinnavia, 53(1): 30.
● Hayder N.A., Yahia I.K. and Qassim H.K. (2019). Molecular detection and phylogenetic analysis of Anaplasma spp in cattle in Al-Qadisiyah province of Iraq. Macedonian Veterinary Review, 42(2): 181-188.
● Hamzah, K.J. and Hasso, S.A. (2019). Molecular prevalence of Anaplasma phagocytophilum in sheep from Iraq. Open Veterinary Journal, 9(3): 238-245.
● Hanène, B., Mourad, B.S., Alberto, A., Khaoula, A.Z.I., Dorra, H., Mohamed, G., et al. (2015). First molecular survey and novel genetic variants’ identification of Anaplasma marginale, A.centrale and A.bovis in cattle from Tunisia. Infection, Genetics and Evolution, 34(1): 361-371.
● Hofmann-Lehmann, R., Meli, M.L., Dreher, U.M., Gonczi, E., Deplazes, P., Braun, U., et al. (2004). Concurrent infections with vector-borne pathogens associated with fatal hemolytic anemia in a cattle herd in Switzerland. Journal of Clinical Microbiology, 42(8): 3775-3780.
● Hosseini-Vasoukolaei, N., Oshaghi, M.A., Shayan, P., Vatandoost, H., Babama hmoudi, F., Yaghoobi -Ershadi, M.R., et al. (2014). Anaplasma Infection in ticks, livestock and human in Ghaemshahr, Mazandaran province, Iran. Iranian Journal of Arthropod Borne Disease, 8(2): 204-211.
● Hulínská, D., Langøová, K., Pejèoch, M., and Pavlásek, I. (2004). Detection of Anaplasmaphagocytophilum in animals by real-time polymerase chain reaction. Journal of Pathology, Microbiolgy and Immunology, 112(4-5): 239-247.
● Jalali, S.M., Khaki, Z., Kazemi, B., Bandehpour, M., Rahbari, S., Jalali M.R., et al. (2013). Molecular detection and identification of Anaplasma species in sheep from Ahvaz, Iran. Iranian Journal of Veterinary Research, 14(1): 50-56.
● Kiilerich, A.M., Christensen, H. and Thamsborg, S.M. (2009). Anaplasma phagocytophilum in Danish sheep: confirmation by DNA sequencing. Acta Veterinaria Scandinnavia, 51(1): 55.
● Kocan, K.M., de la Fuente, J., Guglielmone, A.A. and Melendez, R.D. (2003). Antigens and alternatives for control of Anaplasma marginale infection in cattle. Clinical Microbiology Reviews, 16(4): 698-712.
● Laloy, E., Petit, E., Boulouis, H.J., Gandoin, C., Bouillin, C., Gounot, G., et al. (2009). Dynamics of natural infection by Anaplasma phagocytophilum in a dairy cattle herd in Brittany, France. Clinical Microbiology and Infection, 15(2): 24-25.
● Leatch, G. (1973). Preliminary studies on the transmission of Anaplasma marginale by Boophilusmicroplus. Australian Veterinary Journal, 49(1): 16-19.
● Muhammad, S.S., Rao Muhammmad, S.S., Ahmad Khan, Z.I. and Muhammad, N.K. (2014). Prevalence and Risk Factors of Anaplasmosis in Cattle and Buffalo Populations of District Khanewal, Punjab, Pakistan. Global Veterinaria, 12(1): 146-153.
● Noaman, V. (2017) A review of anaplasmosis and the prevalence of Anaplasma marginale in cattle in Iran and the world. Veterinary Researches & Biological Products, 116(3): 2-15. [In Persian]
● Noaman, V. (2019). A review on Anaplasma phagocytophilum as a zoonotic agent. Tehran University Medical Journal, 76(12): 778-785. [In Persian]
● Noaman, V., Allameh, S.K. and Nabavi, R. (2017). Anaplasmosis in Ruminants of Iran: An Overview. Advanced Techniques in Clinical Microbiology, 1(2): 1-3.
● Noaman, V. and Moradi, M. (2019). Molecular epidemiology and risk factors assessment of Anaplasma spp. on dairy cattle in Southwest of Iran. Acta Veterinaria Eurasia, 45(1): 30-36.
● Noaman, V., Nabinejad, A., Shahmoradi, A. and Esmaeilkhanian, S. (2016). Molecular detection of bovine leukocytic Anaplasma species in Isfahan, Iran. Research in Molecular Medicine, 4(2): 47-51.
●Noaman, V. and Shayan, P. (2010). Comparison of Microscopy and PCR-RFLP for detection of Anaplasma marginale in carrier cattle. Iranian Journal of Microbiology, 2(2): 89-94.
● Ooshiro, M., Zakimi, S., Matsukawa, Y., Katagiri, Y. and Inokuma, H. (2008). Detection of Anaplasma bovis and Anaplasma phagocytophilum from cattle on Yonaguni Island, Okinawa, Japan. Veterinary Parasitology, 154(3-4): 360-364.
● Razmi, G.R., Dastjerdi, K., Hosseini, H., Naghibi, A., Barati, F. and Aslani, M.R. (2006). An epidemiological study on Anaplasma infection in cattle, sheep and goats in Mashhad suburb, Khorasan province, Iran. Annals of the New York Academy of Sciences, 1078(1): 479-481.
● Salehi-Guilandeh, S., Sadeghi-Dehkordi, Z., Sadeghi Nasab, A. and Yousefi, A. (2018). Molecular detection of Anaplasma spp. in cattle of Talesh County, North of Iran. Bulgarian Journal of Veterinary Medicine, 22(4): 457-465.
● Scharf, W., Schauer, S., Freyburger, F., Petrovec, M., Schaarschmidt- Kiener, D., Liebisch, G., et al. (2011). Distinct host species correlate with Anaplasma phagocytophilum ankA gene clusters. Journal of Clinical Microbiology, 49(3): 790-796.
● Stuen, S., Granquist, E.G. and Silaghi, C. (2013). Anaplasma phagocytophilum: a widespread multi-host pathogen with highly adaptive strategies. Frontiers in Cellular and Infection Microbiology, 3(3): 31.
● Stuen, S., Pettersen, K.S., Granquist, E.G., Bergström, K., Bown, K.J. and Birtles, R.J. (2013). Anaplasma phagocytophilum variants in sympatric red deer (Cervus elaphus) and sheep in southern Norway. Ticks and Tick Borne Disease, 4(3):197-201.
● Stuen S., Torsteinbo, W.O., Bergstrom, K. and Bardsen, K. (2009). Superinfection occurs in Anaplasmaphagocytophilum infected sheep irrespective of infection phase and protection status. Acta Veterinaria Scandinavica, 51(41): 1-6.
● Tay, S.T., Koh, F.X., Kho, K.L. and Ong, B.L. (2014). Molecular survey and sequence analysis of Anaplasma spp. in cattle and ticks in a Malaysian farm. Tropical Biomedicine, 31(4): 769-776.
● Torina, A. and Caracappa, S. (2007). Anaplasmosis in cattle in Italy. Veterinary Research Communications, 31(1): 73-78.
● Torina, A., Alongi, A., Naranjo, V., Scimeca, S., Nicosia, S., Di Marco, V., et al. (2008b). Characterization of Anaplasma infections in Sicily, Italy. Annals of the New York Academy of Sciences, 1149(1): 90-93.
●Torina, A., Galindo, R.C., Vicente, J., Di Marco, V., Russo, M., Aronica, V., et al. (2010). Characterization of Anaplasma phagocytophilum and A. ovis infection inanaturally infected sheep flock with poor health condition. Tropical Animal Health and Production, 42(7): 1327-31.
● Vahedi Noori, N. and Noaman, V. (2020). Molecular Identification of Anaplasma pathogenic species in Sheep in Mazandaran Province. Veterinary Researches & Biological Products, 33(2): 29-41. [In Persian]
●Weisburg, W.G., Barns, S.M., Pelletier, D.A. and Lane, D.J. )1991(. 16S ribosomal DNA amplification for phylogenetic study. Journal of Bacteriology, 173(2): 697-703.
● Yang, J., Liu, Z., Niu, Q., Liu, G., Han, R., Guan, G., et al. (2016). Anaplasma phagocytophilum in sheep and goats in central and southeastern China. Parasites and Vectors, 9(593): 1-7
●Yang, J., Liu, Z., Guan, G., Liu, Q., Li, Y., Chen, Z., et al. (2013). Prevalence of Anaplasmaphagocytophilum in ruminants, rodents and ticks in Gansu, North-Western China. Journal of Medical Microbiology, 62(2): 254-258.
●Yousefi, A., Rahbari, S., Shayan, P., Sadeghi-Dehkordi, Z. and Ahomar, A.B. (2017). Molecular evidence of Anaplasma phagocytophilum: An emerging tick-borne pathogen in domesticated small ruminant of Iran; first report. Comparative Clinical Pathology, 26(3): 637-642.
