The Prevalence and Molecular Characterization of Bovine Babesia Species and the First Report of B. bovis from Kashmir Himalayas
-
Tawheed Ahmad Najar
,
Noor Alam Tufani
,
Idrees Mehraj Allaie
,
Shahana Riyaz Tramboo
,
Aijaz Ahmad Dar
,
Hamid Ullah Malik
Abstract
Background: Bovine babesiosis, a global disease, has not been studied so far in Kashmir valley, which is having temperate type of climate as compared to rest of India having tropical to sub-tropical climate, so we felt the need to investigate it.
Methods: To diagnose the babesiosis in clinically suspected cattle (n=450), peripheral blood film examination and PCR tests using generic and species-specific primers targeting Babesia/Theleria genera and B. bigemina, B. bovis as well as B. divergens, respectively were conducted. Four PCR products were sequenced and subjected to BLASTn analysis. Ticks were collected from the clinically suspected animals and identified as per the standard morphological keys.
Results: The prevalence of babesiosis among suspected cattle in central Kashmir by peripheral blood film examination and PCR technique was 11.11% and 33.62%, respectively. The 18S rRNA gene of Isolate B1 of Babesia spp. showed 99.0 to 100% nucleotide sequence homology with 18S rRNA gene of different isolates of B. bigemina registered in the GenBank, while as 18S rRNA gene of Isolate Z showed 98.5 to 99.2% and 93.1 to 93.9% nucleotide sequence homology with 18S rRNA gene of different isolates of Babesia spp. and B. bigemina, respectively, registered in the GenBank. Rhipicephalus spp. and Haemaphysalis spp. were the two major tick genera identified in the present study.
Conclusion: Bovine Babesiosis in Kashmir is attributed to B. bovis, B. bigemina and some other Babesia spp. or strains which needs further investigation. To our knowledge, this is the first report of Babesia bovis from northern India in cattle.
1. Walker GK, Edward JT. Some Diseases of Cattle in India. Calcutta: Government of India, pp 29. 1927.
2. Kolte SW, Larcombe SD, Jadhao SG, et al. PCR diagnosis of tick-borne pathogens in Maharashtra state, India indicates fitness cost associated with carrier infections is greater for crossbreed than native cattle breeds. PLoS One. 2017; 12(3): e0174595.
3. Indani JA. Babesia bovis as cause of red water in an Indian buffalo. Ind J Vet Sci Ani Hus. 1938; 9: 99-101.
4. Tufani NA, Hafiz A, Malik HU, Peer FU, Makhdoomi DM. Clinico-therapeutic management of acute babesiosis in bovine. Intas polivet. 2009; 10(1): 49-50.
5. Haq AU, Tufani NA, Malik HU, Hussain SA, Bhat RR, Amin U, Nabi SU. Cross sectional study on prevalence of ovine babesiosis in different breeds of Kashmir valley. Journal of Entomology and Zoology Studies. 2017; 5(6): 1492-1496.
6. Umar F, Tufani NA, Malik HU, Mir MS. Clinical and morphomolecular epidemiology of bovine theileriosis in Kashmir. Indian J Anim Res. 2018; 53(3): 375-381.
7. Almeria S, Castella J. Gutierrez JF. Bovine piroplasms in Minorca (Spain): A comparison of PCR-based and light microscopy detection. Vet Parasitol. 2001; 99(3): 249-259.
8. Figueroa JV, Chieves LP, Johnson GS. Buening GM. Detection of Babesia bigemina infected carriers by polymerase chain reaction amplification. J Clin Microbiol. 1992; 30(10): 2576-2582.
9. Zintl A, Macgrath G, Grady L. Changing incidence of bovine babesiosis in Ireland. Ir Vet J. 2014; 67: 19.
10. Kumar B, Maharana BR, Thakre B, Brahmbhatt NN, Joseph JP. 18S rRNA Gene-based piroplasmid PCR: An Assay for rapid and precise molecular screening of Theileria and Babesia species in animals. Acta Parasitol. 2022; 67: 1697-1707.
11. Bilgic HB, Kargenc T, Eren H, Weir W. Development of a multiplex PCR assay for simoultaneous detection of Theilaria annulata, Babesia bovis and Anaplasma marginale in cattle. Exp Parasitol. 2013; 133(2): 222-229.
12. Hilpertshauser H, Deplazes P, Schnyder M, Gern L, Mathis A. Babesia spp. Identified by PCR in ticks collected from domestic and wild ruminants in Southern Switzerland. Appl Environ Microbiol. 2006; 72(10): 6503-6507.
13. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990; 215(3): 403-410.
14. Nava S, Venzal J, Gonzalez-Acuna D, Martins T, Guglielmone A. Ticks of the Southern Cone of America: Diagnosis, Distribution and Hosts with Taxonomy, Ecology and Sanitary Importance. (Ist ed.) Academic Press, Elsevier. 2017.
15. Snedecor GW, Cochran WG. Statistical Methods. (6th ed.) Calcutta: Oxford and IBH Publishing Company. 1994.
16. Rather SA, Tak H, Kakru DK. Seroprevalence of Babesia bigemina and Anaplasma marginale in domestic animals of district Ganderbal. Sci J Vet Adv. 2015; 5: 74-79.
17. Shaw AA. Investigation on some infections in the exotic, pure and crossbred cattle of Kashmir valley. Indian J Comp Microbiol Immunol Infect Dis. 1989; 10: 33-38.
18. Velusamy R, Rani N, Ponnudurai G, et a. Influence of season, age, and breed on prevalence of haemoprotozoan diseases in cattle of Tamil Nadu India. Vet World. 2014; 7(8): 574-578.
19. Constable PD, Hinchcliff KW, Done SH, Gruenberg G. Veterinary Medicine: A textbook of the diseases of cattle, horses, sheep, pigs, and goats (11th Ed., 2 Volume sets) Elsevier, St. Louis, Missouri, USA. 2016. ISBN: 9780-7020-5246-8.
20. Kumar B, Verma SP, Sinha BS, Shekhar S. Epidemiological aspects of bovine babesiosis in Bihar’. Indian J Vet Med. 2006; 26(2): 141-142.
21. Ananda KJ, D’Souza, PE, Puttalakshmamma GC. Prevalence of haemoprotozoan diseases in crossbred cattle in Bangalore north. Vet World. 2009; 2(1): 15-16.
22. Kocan KM, dela-Fuente J, Bouin EF, Coetzee JF, Ewing SA. The natural history of Anaplasma marginale. Vet Parasitol. 2010; 167: 95-107.
23. Alim MA, Das S, Roy K, et al. Prevalence of Hemoprotozoan diseases in cattle population of Chittagong Division, Bangladesh’. Pak Vet J. 2012; 32: 221-24.
24. Kaur PJuyal PD, Sharma A, Bal MS, Singla LD. Seroprevalence of Babesia bigemina in dairy animals from low lying regions of Punjab, India. Indian J Anim Res. 2016; 50(3): 406-410.
25. Ganguly A, Bisla RS, Ganguly I, Singh H, Bharat V, Chaudhury SS. Direct blood PCR detection of Babesia bigemina and its effect on haematological and biochemical profile in cross-bred cattle of eastern Haryana. Indian J Anim Res. 2017; 51(1): 141-145.
26. Mahmoud MS, Kandil OM, Nasr SM, et al. Serological and molecular diagnostic surveys combined with examining hematological profiles suggests increased levels of infection and haematological response of cattle to babesiosis infections compared to native buffaloes in Egypt. Parasit Vectors. 2015; 8: 319.
27. McKenzie FE, Wongsrichanalai C, Magill AJ, et al. Gametocytemia in Plasmodium vivax and Plasmodium falciparum infections. J Parasitol. 2006; 92(6): 1281.
28. Sharma A, Singla LD, Tuli A, et al. Molecular prevalence of Babesia bigemina and Trypanosoma evansi in dairy animals from Punjab, India, by duplex PCR: a step forward to the detection and management of concurrent latent infections. Biomed Res Int. 2013; 2013:893862.
29. Pradeep RK, Nimisha M, Sruthi MK, et al. Molecular characterization of South Indian field isolates of bovine Babesia spp. and Anaplasma spp. Parasitol Res. 2019; 118: 617-630.
30. Nair AS. Surveillance of haemoprotozoan and haemo-rickettsial diseases of cattle of Northern Kerala’, Master`s Thesis, Kerala Agricultural University, Thrissur, Kerala. 2008
31. Nair AS, Ravindran R, Lakshmanan B, et al. Haemoprotozoa of cattle in northern Kerala, India. Trop Biomed. 2011; 28: 68-75.
32. Allred DR, Cinque RM, Lane TJ, Ahrens KP. Antigenic variation of parasite-derived antigens on the surface of Babesia bovis infected erythrocytes. Infect Immun.1994; 62: 91–98.
33. Olmeda AS, Armstrong PM, Rosenthal BM, Valladares B. A subtropical case of human Babesiosis. Acta Trop. 1997; 67: 229-234.
2. Kolte SW, Larcombe SD, Jadhao SG, et al. PCR diagnosis of tick-borne pathogens in Maharashtra state, India indicates fitness cost associated with carrier infections is greater for crossbreed than native cattle breeds. PLoS One. 2017; 12(3): e0174595.
3. Indani JA. Babesia bovis as cause of red water in an Indian buffalo. Ind J Vet Sci Ani Hus. 1938; 9: 99-101.
4. Tufani NA, Hafiz A, Malik HU, Peer FU, Makhdoomi DM. Clinico-therapeutic management of acute babesiosis in bovine. Intas polivet. 2009; 10(1): 49-50.
5. Haq AU, Tufani NA, Malik HU, Hussain SA, Bhat RR, Amin U, Nabi SU. Cross sectional study on prevalence of ovine babesiosis in different breeds of Kashmir valley. Journal of Entomology and Zoology Studies. 2017; 5(6): 1492-1496.
6. Umar F, Tufani NA, Malik HU, Mir MS. Clinical and morphomolecular epidemiology of bovine theileriosis in Kashmir. Indian J Anim Res. 2018; 53(3): 375-381.
7. Almeria S, Castella J. Gutierrez JF. Bovine piroplasms in Minorca (Spain): A comparison of PCR-based and light microscopy detection. Vet Parasitol. 2001; 99(3): 249-259.
8. Figueroa JV, Chieves LP, Johnson GS. Buening GM. Detection of Babesia bigemina infected carriers by polymerase chain reaction amplification. J Clin Microbiol. 1992; 30(10): 2576-2582.
9. Zintl A, Macgrath G, Grady L. Changing incidence of bovine babesiosis in Ireland. Ir Vet J. 2014; 67: 19.
10. Kumar B, Maharana BR, Thakre B, Brahmbhatt NN, Joseph JP. 18S rRNA Gene-based piroplasmid PCR: An Assay for rapid and precise molecular screening of Theileria and Babesia species in animals. Acta Parasitol. 2022; 67: 1697-1707.
11. Bilgic HB, Kargenc T, Eren H, Weir W. Development of a multiplex PCR assay for simoultaneous detection of Theilaria annulata, Babesia bovis and Anaplasma marginale in cattle. Exp Parasitol. 2013; 133(2): 222-229.
12. Hilpertshauser H, Deplazes P, Schnyder M, Gern L, Mathis A. Babesia spp. Identified by PCR in ticks collected from domestic and wild ruminants in Southern Switzerland. Appl Environ Microbiol. 2006; 72(10): 6503-6507.
13. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990; 215(3): 403-410.
14. Nava S, Venzal J, Gonzalez-Acuna D, Martins T, Guglielmone A. Ticks of the Southern Cone of America: Diagnosis, Distribution and Hosts with Taxonomy, Ecology and Sanitary Importance. (Ist ed.) Academic Press, Elsevier. 2017.
15. Snedecor GW, Cochran WG. Statistical Methods. (6th ed.) Calcutta: Oxford and IBH Publishing Company. 1994.
16. Rather SA, Tak H, Kakru DK. Seroprevalence of Babesia bigemina and Anaplasma marginale in domestic animals of district Ganderbal. Sci J Vet Adv. 2015; 5: 74-79.
17. Shaw AA. Investigation on some infections in the exotic, pure and crossbred cattle of Kashmir valley. Indian J Comp Microbiol Immunol Infect Dis. 1989; 10: 33-38.
18. Velusamy R, Rani N, Ponnudurai G, et a. Influence of season, age, and breed on prevalence of haemoprotozoan diseases in cattle of Tamil Nadu India. Vet World. 2014; 7(8): 574-578.
19. Constable PD, Hinchcliff KW, Done SH, Gruenberg G. Veterinary Medicine: A textbook of the diseases of cattle, horses, sheep, pigs, and goats (11th Ed., 2 Volume sets) Elsevier, St. Louis, Missouri, USA. 2016. ISBN: 9780-7020-5246-8.
20. Kumar B, Verma SP, Sinha BS, Shekhar S. Epidemiological aspects of bovine babesiosis in Bihar’. Indian J Vet Med. 2006; 26(2): 141-142.
21. Ananda KJ, D’Souza, PE, Puttalakshmamma GC. Prevalence of haemoprotozoan diseases in crossbred cattle in Bangalore north. Vet World. 2009; 2(1): 15-16.
22. Kocan KM, dela-Fuente J, Bouin EF, Coetzee JF, Ewing SA. The natural history of Anaplasma marginale. Vet Parasitol. 2010; 167: 95-107.
23. Alim MA, Das S, Roy K, et al. Prevalence of Hemoprotozoan diseases in cattle population of Chittagong Division, Bangladesh’. Pak Vet J. 2012; 32: 221-24.
24. Kaur PJuyal PD, Sharma A, Bal MS, Singla LD. Seroprevalence of Babesia bigemina in dairy animals from low lying regions of Punjab, India. Indian J Anim Res. 2016; 50(3): 406-410.
25. Ganguly A, Bisla RS, Ganguly I, Singh H, Bharat V, Chaudhury SS. Direct blood PCR detection of Babesia bigemina and its effect on haematological and biochemical profile in cross-bred cattle of eastern Haryana. Indian J Anim Res. 2017; 51(1): 141-145.
26. Mahmoud MS, Kandil OM, Nasr SM, et al. Serological and molecular diagnostic surveys combined with examining hematological profiles suggests increased levels of infection and haematological response of cattle to babesiosis infections compared to native buffaloes in Egypt. Parasit Vectors. 2015; 8: 319.
27. McKenzie FE, Wongsrichanalai C, Magill AJ, et al. Gametocytemia in Plasmodium vivax and Plasmodium falciparum infections. J Parasitol. 2006; 92(6): 1281.
28. Sharma A, Singla LD, Tuli A, et al. Molecular prevalence of Babesia bigemina and Trypanosoma evansi in dairy animals from Punjab, India, by duplex PCR: a step forward to the detection and management of concurrent latent infections. Biomed Res Int. 2013; 2013:893862.
29. Pradeep RK, Nimisha M, Sruthi MK, et al. Molecular characterization of South Indian field isolates of bovine Babesia spp. and Anaplasma spp. Parasitol Res. 2019; 118: 617-630.
30. Nair AS. Surveillance of haemoprotozoan and haemo-rickettsial diseases of cattle of Northern Kerala’, Master`s Thesis, Kerala Agricultural University, Thrissur, Kerala. 2008
31. Nair AS, Ravindran R, Lakshmanan B, et al. Haemoprotozoa of cattle in northern Kerala, India. Trop Biomed. 2011; 28: 68-75.
32. Allred DR, Cinque RM, Lane TJ, Ahrens KP. Antigenic variation of parasite-derived antigens on the surface of Babesia bovis infected erythrocytes. Infect Immun.1994; 62: 91–98.
33. Olmeda AS, Armstrong PM, Rosenthal BM, Valladares B. A subtropical case of human Babesiosis. Acta Trop. 1997; 67: 229-234.
| Files | ||
| Issue | Vol 19 No 1 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijpa.v19i1.15211 | |
| Keywords | ||
| Babesiosis Babesia bovis Cattle Prevalence Kashmir | ||
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How to Cite
1.
Ahmad Najar T, Tufani N, Allaie I, Tramboo S, Dar A, Malik H. The Prevalence and Molecular Characterization of Bovine Babesia Species and the First Report of B. bovis from Kashmir Himalayas. Iran J Parasitol. 2024;19(1):86-97.
