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Current IssueEditorial BoardOnline First ArticlesArchive

Research Article

volume 52 issue 11 (november 2018) : 1642-1648,   Doi: 10.18805/ijar.B-3413

Comparative evaluation of different diagnostic tests for B. gibsoni in dogs

N
Neelam Kushwaha
D
Debabrata Mondal
K
Karam Pal Singh
R
Rashmi Ranjan Mahapatra
1Division of Veterinary Medicine, ICAR-Indian Veterinary Research Institute, Bareilly- 243 122, Uttar Pradesh, India.
Cite article:- Kushwaha Neelam, Mondal Debabrata, Singh Pal Karam, Mahapatra Ranjan Rashmi (2017). Comparative evaluation of different diagnostic tests for B. gibsoni in dogs. Indian Journal of Animal Research. 52(11): 1642-1648. doi: 10.18805/ijar.B-3413.

ABSTRACT

Babesia gibsoni is the common cause of canine babesiosis in India. Its diagnosis by conventional diagnostic methods result in false negative condition, particularly in those cases in which parasitemia is low. Therefore the present study employed IFAT and PCR along with microscopic examination to overcome this situation. Microscopic examination of Giemsa-stained blood smears revealed presence of small pear-shaped, oval or signet ring shaped B. gibsoni within the erythrocytes of 1.34 % dogs. IFAT and PCR detected a total of 1.80 % and 1.82 % dogs positive for B. gibsoni, respectively. The sensitivity and specificity of IFAT was 93.10% and 88.89%, respectively whereas, sensitivity and specificity of microscopic examination was 71.26% and 95.56%, respectively. The agreement of IFAT and microscopic examination with PCR was 82.30% and 60.73%, respectively. The agreement between IFAT and microscopy was 60.99%. Therefore, IFAT is considered to be highly sensitive test for diagnosing B. gibsoni in subclinically or chronically infected dogs with significantly low level of parasitemia. 

REFERENCES

  1. Adachi, K., Tateishi, M., Horii, Y., Nagatomo, H., Shimizu, T. and Makimura, S. (1994). Reactivity of serum antierythrocyte membrane antibody in Babesia gibsoni infected dogs. J. Vet. Med. Sci., 56: 997-999.
  2. Adachi, K., Ueno, C. and Makimura, S. (1993). Immunosuppression in dogs naturally infected with Babesia gibsoni. J. Vet. Med. Sci., 55:503–505.
  3. Amuta, E. U., Atu, B. O., Houmsou, R. S. and Ayashar, J. G. (2010). Rhipicephalus sanguineus infestation and Babesia canis infection among domestic dogs in Makurdi, Benue State-Nigeria. Int. J. Acad. Res., 2: 170– 172. 
  4. Ayoob, A. L. and Prittie, J. (2010). Clinical management of canine babesiosis. J. Vet. Emerg. Crit. Care., 20: 77-89.
  5. Aysul, N., Ural, K., Ulutas, B., Eren, H. and Karagenc, T. (2013). First detection and molecular identification of Babesia gibsoni in two dogs from the Aydyn Province of Turkey. Turk. J. Vet. Anim. Sci., 37: 226-229.
  6. Birkenheuer, A. J., Levy, M. G., Stebbins, M., Poore, M. and Breitschwerdt, E. (2003). Serosurvey of anti-Babesia antibodies in stray dogs and American pit bull terriers and American Staffordshire terriers from North Carolina. J. Am. Anim. Hosp. Assoc., 39: 551-557.
  7. Brandao, L. P., Hagiwara, M. K. and Myashiro, S. I. (2003). Humoral immunity and reinfection resistance in dogs experimentally inoculated with Babesia canis and either treated or untreated with imidocarb dipropionate. Vet. Parasitol., 114: 253-265.
  8. Caccio, S. M., Antunovic, B., Moretti, A., Mangili, V., Marinculic, A., Baric, R. R., et al. (2002). Molecular characterisation of Babesia canis canis and Babesia canis vogeli from naturally infected European dogs. Vet. Parasitol., 106:285-292.
  9. Chaudhuri, S. (2006). Studies on clinico-therapeutic aspects of babesiosis in dogs. M.V.Sc. Thesis, Indian Veterinary Research Institute, Izatnagar, India.
  10. Coles, E.H. (1986). Veterinary Clinical Pathology, 4th ed., WB Saunder’s Company, pp 321.
  11. DADF. (2012). Department of Animal Husbandry, Dairying and Fisheries, India. 
  12. Eljadar, M. S. M. (2010).Clinico-diagnostic studies on vector transmitted haemoprotozoan diseases in dogs. M.S. Thesis, GADVASU, Ludhiana, India.
  13. Fukumoto, S., Xuan, X., Shigeno, S., Kimbita, E., Igarashi, I., Nagasawa, H., Fujisaki, K. and Mikami, T. (2001). Development of a polymerase chain reaction method for diagnosing Babesia gibsoni infection in dogs. J. Vet. Med. Sci., 63: 977-981.
  14. Ganguly, A., Bisla, R. S., Ganguly, I., Singh, H., Bhanot, V. and Chaudhri, S. S. (2017). Direct blood PCR detection of Babesia bigemina and its effect on haematological and biochemical profile in crossbred cattle of eastern Haryana. Indian J. Anim. Res., 51: 141-145.
  15. Gotsch, S., Leschnik, M., Duscher, G., Burgstaller, J. P., Wille-Piazzai, W. and Joachim, A. (2009). Ticks and haemoparasites of dogs from Praia, Cape Verde. Vet. Parasitol., 166: 171-174.
  16. Inokuma, H., Yoshizaki, Y., Matsumoto, K., Okuda, M., Onishi, T., Nakagome, K., Kosugi, R. and Hirakawa, M. (2004). Molecular survey of Babesia infection in dogs in Okinawa, Japan. Vet. Parasitol., 121: 341-346.
  17. Ionita, M., Mitrea, I. L., Fister, K. P., Hamel, D., Buzatu, C. M. and Silaghi, C. (2012). Canine babesiosis in Romania due to Babesia canis and Babesia vogeli: a molecular approach. Parasitol. Res., 110: 1659-1664.
  18. Irizarry-Rovira, A. R., Stephens, J., Christian, J., Kjemtrup, A., De Nicola, D. B., Widmer, W. R. and Conrad, P. A. (2001). Babesia gibsoni infection in a dog from Indiana. Vet. Clin. Pathol., 30:180-188.
  19. Jadhav, R. K., Kumari, R. R., Javed, A. J. and Kumar, P. (2011). Emergence of Arthropod Transmitted infections in Kennel Dogs. Vet. World., 4: 522-528.
  20. Kaur, P., Juyal, P.D., Sharma A., Bal, M. S. and L. D. Singla (2016). Seroprevalence of Babesia bigemina in dairy animals from low lying regions of Punjab, India. Indian J. Anim. Res., 50 : 406-410. 
  21. Kumar, P, Kumar V, Gopal H, Sharma H and Wadhawan V M. (2015). Prevalence of Canine Babesiosis in and around Jalandhar (Punjab), India. Vet. Clin. Sci., 3: 01-03.
  22. Kumar, S. K., Vairamuthu, S. and Kathiresanl, D. (2009). Prevalence of haemoprotozoans in canines in Chennai City. Tamilnadu J. Vet. Anim. Sci., 5: 104–108.
  23. Laha, R., Bhattacharjee, K., Sarmah, P. C., Das, M., Goswami, A., Sarma, D, and Sen, A. (2014). Babesia infection in naturally exposed pet dogs from a north-eastern state (Assam) of India: detection by microscopy and polymerase chain reaction. J. Parasit. Dis., 38: 389-393. 
  24. Macintire, D. K., Boudreaux, M. K., West, G. D, Bourne, C., Wright, J. C. and Conrad, P. A. (2002). Babesia gibsoni infection among dogs in the southeastern United States. J. Am. Vet. Med. Assoc., 220: 325-329.
  25. Megat Abd-Rani, P. A., Irwin, P. J., Coleman, G. T., Gatn, M. and Traub, R. J. (2011). A survey of canine tick-borne diseases in India. Parasit. Vectors, 4: 141 http://www.parasitesandvectors.com/content/4/1/141
  26. Megat Abd-Rani, P. A., Irwin, P. J., Gatne, M., Coleman, G. and Traub, R. (2010). Canine vector borne diseases in India: a review of literature and identification of existing knowledge gaps. Parasit. Vectors, 3: 28 http://www.parasitesandvectors.com/content/3/1/28.
  27. Mokhtar, A. S., Lim, S. F. and Tay, S. T. (2013). Molecular detection of Anaplasma platys and Babesia gibsoni in dogs in Malaysia. Trop. Biomed., 30: 345-348.
  28. O’Dwyer, L. H., Lopes, V. V. A, Rubini, A. S., Paduan, K. D. S. and Ribolla, P. E. M. (2009). Babesia spp. infection in dogs from rural areas of Sao Paulo State, Brazil. Rev. Bras. Parasitol. Vet., 18: 23–26.
  29. Rene-Martellet, M., Chene, J., Chabanne, L., Chalvet-Monfray, K. and Bourdoiseau, G. (2013). Clinical signs, seasonal occurrence and causative agents of canine babesiosis in France: Results of a multiregional study. Vet. Parasitol. 197: 50-58
  30. Saud, N. and Hazarika, G. C. (2000). Studies on the incidence and biochemical changes of Babesia infection in dogs. Indian Vet., J. 77: 944-947.
  31. Schnittger, L., Rodriguez, A. E., Florin-Christensen, M. and Morrison. D. A. (2012). Babesia: A world emerging. Infect. Genet. Evol., 12: 1788–1809.
  32. Singh, A., Singh, H., Singh, N. K., Singh, N. D. and Rath, S. S. (2014). Canine Babesiosis in Northwestern India: Molecular Detection and Assessment of Risk Factors. Biomed. Res. Int., Article ID 741785, 5 pages http://dx.doi.org/10.1155/2014/741785
  33. Singh, H., Jyoti, H. M., Singh, N. K. and Rath, S. S. (2011). Prevalence of canine parasitic infections in and around Ludhiana, Punjab. J. Vet. Parasitol., 25: 179-180.
  34. Singh, H., Singh, N. K. and Rath, S. S. (2012). A survey of canine babesiosis in and around ludhiana district, Punjab. Indian J. Canine Practice, 4: 165-167.
  35. Sudarshan, M. K., Mahendra, B. J., Madhusudana, S. N., Ashwoath Narayana, D. H., et al. (2006). An epidemiological study of animal bites in India: results of a WHO sponsored national multi-centric rabies surveys. J. Commun. Dis., 38: 32-39.
  36. Sundar, N., Balachandran, C. and Senthivelan, A. (2004). Incidence of Babesia gibsoni infection in dogs in Tamil Nadu. J. Vet. Parasitol., 18: 79–80.
  37. Talukder, M. H., Matsuu, A., Iguchi, A., Roy, B. C., Nishii, N. and Hikasa, Y. (2012). PCR based survey of vector-borne pathogens in dogs in Dhaka, Bangladesh. J. Bangladesh Agril. Univ., 10: 249–253.
  38. Varshney, J. P. and Dey, S. (1998). A clinical study on haemoprotozoan infections in referral canines. J. Remount Vet. Corps, 37: 83–89.
  39. Verdida, R. A., Hara, O. A., Xuan, X., Fukumoto, S., Igarashi, I., Zhang, S., Dong, J., et al. (2004). Serodiagnosis of Babesia gibsoni infection in dogs by an improved enzyme-linked immunosorbent assay with recombinant truncated P50. J. Vet. Med. Sci., 66: 1517-1521.
  40. Yamane, I., Gardener, I. A., Ryan, C. P., Levy, M., Urrico, J. and Conrad, P. A. (1994). Serosurvey of Babesia canis, Babesia gibsoni and Ehrlichia canis in pound dogs in California, USA. Prev. Vet. Med., 18: 293-304.
  41. Yamane, I., Thomford, J. W., Gardner, I. A., Dubey, J. P., Levy, M. and Conard, P. A. (1993). Evaluation of the indirect fluorescent antibody test for diagnosis of Babesia gibsoni infections in dogs. Am. J. Vet. Res., 54: 1579-1584. 
  42. Yao, D., Jiang, J., Yu, Z., Yao, D., Yang, D. and Zhao, Y. (2014). Canine Babesiosis in China caused by Babesia gibsoni: A molecular approach. Iranian J. Parasitol., 9: 163–168. 
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    Research Article

    volume 52 issue 11 (november 2018) : 1642-1648,   Doi: 10.18805/ijar.B-3413

    Comparative evaluation of different diagnostic tests for B. gibsoni in dogs

    N
    Neelam Kushwaha
    D
    Debabrata Mondal
    K
    Karam Pal Singh
    R
    Rashmi Ranjan Mahapatra
    1Division of Veterinary Medicine, ICAR-Indian Veterinary Research Institute, Bareilly- 243 122, Uttar Pradesh, India.
    Cite article:- Kushwaha Neelam, Mondal Debabrata, Singh Pal Karam, Mahapatra Ranjan Rashmi (2017). Comparative evaluation of different diagnostic tests for B. gibsoni in dogs. Indian Journal of Animal Research. 52(11): 1642-1648. doi: 10.18805/ijar.B-3413.

    ABSTRACT

    Babesia gibsoni is the common cause of canine babesiosis in India. Its diagnosis by conventional diagnostic methods result in false negative condition, particularly in those cases in which parasitemia is low. Therefore the present study employed IFAT and PCR along with microscopic examination to overcome this situation. Microscopic examination of Giemsa-stained blood smears revealed presence of small pear-shaped, oval or signet ring shaped B. gibsoni within the erythrocytes of 1.34 % dogs. IFAT and PCR detected a total of 1.80 % and 1.82 % dogs positive for B. gibsoni, respectively. The sensitivity and specificity of IFAT was 93.10% and 88.89%, respectively whereas, sensitivity and specificity of microscopic examination was 71.26% and 95.56%, respectively. The agreement of IFAT and microscopic examination with PCR was 82.30% and 60.73%, respectively. The agreement between IFAT and microscopy was 60.99%. Therefore, IFAT is considered to be highly sensitive test for diagnosing B. gibsoni in subclinically or chronically infected dogs with significantly low level of parasitemia. 

    REFERENCES

    1. Adachi, K., Tateishi, M., Horii, Y., Nagatomo, H., Shimizu, T. and Makimura, S. (1994). Reactivity of serum antierythrocyte membrane antibody in Babesia gibsoni infected dogs. J. Vet. Med. Sci., 56: 997-999.
    2. Adachi, K., Ueno, C. and Makimura, S. (1993). Immunosuppression in dogs naturally infected with Babesia gibsoni. J. Vet. Med. Sci., 55:503–505.
    3. Amuta, E. U., Atu, B. O., Houmsou, R. S. and Ayashar, J. G. (2010). Rhipicephalus sanguineus infestation and Babesia canis infection among domestic dogs in Makurdi, Benue State-Nigeria. Int. J. Acad. Res., 2: 170– 172. 
    4. Ayoob, A. L. and Prittie, J. (2010). Clinical management of canine babesiosis. J. Vet. Emerg. Crit. Care., 20: 77-89.
    5. Aysul, N., Ural, K., Ulutas, B., Eren, H. and Karagenc, T. (2013). First detection and molecular identification of Babesia gibsoni in two dogs from the Aydyn Province of Turkey. Turk. J. Vet. Anim. Sci., 37: 226-229.
    6. Birkenheuer, A. J., Levy, M. G., Stebbins, M., Poore, M. and Breitschwerdt, E. (2003). Serosurvey of anti-Babesia antibodies in stray dogs and American pit bull terriers and American Staffordshire terriers from North Carolina. J. Am. Anim. Hosp. Assoc., 39: 551-557.
    7. Brandao, L. P., Hagiwara, M. K. and Myashiro, S. I. (2003). Humoral immunity and reinfection resistance in dogs experimentally inoculated with Babesia canis and either treated or untreated with imidocarb dipropionate. Vet. Parasitol., 114: 253-265.
    8. Caccio, S. M., Antunovic, B., Moretti, A., Mangili, V., Marinculic, A., Baric, R. R., et al. (2002). Molecular characterisation of Babesia canis canis and Babesia canis vogeli from naturally infected European dogs. Vet. Parasitol., 106:285-292.
    9. Chaudhuri, S. (2006). Studies on clinico-therapeutic aspects of babesiosis in dogs. M.V.Sc. Thesis, Indian Veterinary Research Institute, Izatnagar, India.
    10. Coles, E.H. (1986). Veterinary Clinical Pathology, 4th ed., WB Saunder’s Company, pp 321.
    11. DADF. (2012). Department of Animal Husbandry, Dairying and Fisheries, India. 
    12. Eljadar, M. S. M. (2010).Clinico-diagnostic studies on vector transmitted haemoprotozoan diseases in dogs. M.S. Thesis, GADVASU, Ludhiana, India.
    13. Fukumoto, S., Xuan, X., Shigeno, S., Kimbita, E., Igarashi, I., Nagasawa, H., Fujisaki, K. and Mikami, T. (2001). Development of a polymerase chain reaction method for diagnosing Babesia gibsoni infection in dogs. J. Vet. Med. Sci., 63: 977-981.
    14. Ganguly, A., Bisla, R. S., Ganguly, I., Singh, H., Bhanot, V. and Chaudhri, S. S. (2017). Direct blood PCR detection of Babesia bigemina and its effect on haematological and biochemical profile in crossbred cattle of eastern Haryana. Indian J. Anim. Res., 51: 141-145.
    15. Gotsch, S., Leschnik, M., Duscher, G., Burgstaller, J. P., Wille-Piazzai, W. and Joachim, A. (2009). Ticks and haemoparasites of dogs from Praia, Cape Verde. Vet. Parasitol., 166: 171-174.
    16. Inokuma, H., Yoshizaki, Y., Matsumoto, K., Okuda, M., Onishi, T., Nakagome, K., Kosugi, R. and Hirakawa, M. (2004). Molecular survey of Babesia infection in dogs in Okinawa, Japan. Vet. Parasitol., 121: 341-346.
    17. Ionita, M., Mitrea, I. L., Fister, K. P., Hamel, D., Buzatu, C. M. and Silaghi, C. (2012). Canine babesiosis in Romania due to Babesia canis and Babesia vogeli: a molecular approach. Parasitol. Res., 110: 1659-1664.
    18. Irizarry-Rovira, A. R., Stephens, J., Christian, J., Kjemtrup, A., De Nicola, D. B., Widmer, W. R. and Conrad, P. A. (2001). Babesia gibsoni infection in a dog from Indiana. Vet. Clin. Pathol., 30:180-188.
    19. Jadhav, R. K., Kumari, R. R., Javed, A. J. and Kumar, P. (2011). Emergence of Arthropod Transmitted infections in Kennel Dogs. Vet. World., 4: 522-528.
    20. Kaur, P., Juyal, P.D., Sharma A., Bal, M. S. and L. D. Singla (2016). Seroprevalence of Babesia bigemina in dairy animals from low lying regions of Punjab, India. Indian J. Anim. Res., 50 : 406-410. 
    21. Kumar, P, Kumar V, Gopal H, Sharma H and Wadhawan V M. (2015). Prevalence of Canine Babesiosis in and around Jalandhar (Punjab), India. Vet. Clin. Sci., 3: 01-03.
    22. Kumar, S. K., Vairamuthu, S. and Kathiresanl, D. (2009). Prevalence of haemoprotozoans in canines in Chennai City. Tamilnadu J. Vet. Anim. Sci., 5: 104–108.
    23. Laha, R., Bhattacharjee, K., Sarmah, P. C., Das, M., Goswami, A., Sarma, D, and Sen, A. (2014). Babesia infection in naturally exposed pet dogs from a north-eastern state (Assam) of India: detection by microscopy and polymerase chain reaction. J. Parasit. Dis., 38: 389-393. 
    24. Macintire, D. K., Boudreaux, M. K., West, G. D, Bourne, C., Wright, J. C. and Conrad, P. A. (2002). Babesia gibsoni infection among dogs in the southeastern United States. J. Am. Vet. Med. Assoc., 220: 325-329.
    25. Megat Abd-Rani, P. A., Irwin, P. J., Coleman, G. T., Gatn, M. and Traub, R. J. (2011). A survey of canine tick-borne diseases in India. Parasit. Vectors, 4: 141 http://www.parasitesandvectors.com/content/4/1/141
    26. Megat Abd-Rani, P. A., Irwin, P. J., Gatne, M., Coleman, G. and Traub, R. (2010). Canine vector borne diseases in India: a review of literature and identification of existing knowledge gaps. Parasit. Vectors, 3: 28 http://www.parasitesandvectors.com/content/3/1/28.
    27. Mokhtar, A. S., Lim, S. F. and Tay, S. T. (2013). Molecular detection of Anaplasma platys and Babesia gibsoni in dogs in Malaysia. Trop. Biomed., 30: 345-348.
    28. O’Dwyer, L. H., Lopes, V. V. A, Rubini, A. S., Paduan, K. D. S. and Ribolla, P. E. M. (2009). Babesia spp. infection in dogs from rural areas of Sao Paulo State, Brazil. Rev. Bras. Parasitol. Vet., 18: 23–26.
    29. Rene-Martellet, M., Chene, J., Chabanne, L., Chalvet-Monfray, K. and Bourdoiseau, G. (2013). Clinical signs, seasonal occurrence and causative agents of canine babesiosis in France: Results of a multiregional study. Vet. Parasitol. 197: 50-58
    30. Saud, N. and Hazarika, G. C. (2000). Studies on the incidence and biochemical changes of Babesia infection in dogs. Indian Vet., J. 77: 944-947.
    31. Schnittger, L., Rodriguez, A. E., Florin-Christensen, M. and Morrison. D. A. (2012). Babesia: A world emerging. Infect. Genet. Evol., 12: 1788–1809.
    32. Singh, A., Singh, H., Singh, N. K., Singh, N. D. and Rath, S. S. (2014). Canine Babesiosis in Northwestern India: Molecular Detection and Assessment of Risk Factors. Biomed. Res. Int., Article ID 741785, 5 pages http://dx.doi.org/10.1155/2014/741785
    33. Singh, H., Jyoti, H. M., Singh, N. K. and Rath, S. S. (2011). Prevalence of canine parasitic infections in and around Ludhiana, Punjab. J. Vet. Parasitol., 25: 179-180.
    34. Singh, H., Singh, N. K. and Rath, S. S. (2012). A survey of canine babesiosis in and around ludhiana district, Punjab. Indian J. Canine Practice, 4: 165-167.
    35. Sudarshan, M. K., Mahendra, B. J., Madhusudana, S. N., Ashwoath Narayana, D. H., et al. (2006). An epidemiological study of animal bites in India: results of a WHO sponsored national multi-centric rabies surveys. J. Commun. Dis., 38: 32-39.
    36. Sundar, N., Balachandran, C. and Senthivelan, A. (2004). Incidence of Babesia gibsoni infection in dogs in Tamil Nadu. J. Vet. Parasitol., 18: 79–80.
    37. Talukder, M. H., Matsuu, A., Iguchi, A., Roy, B. C., Nishii, N. and Hikasa, Y. (2012). PCR based survey of vector-borne pathogens in dogs in Dhaka, Bangladesh. J. Bangladesh Agril. Univ., 10: 249–253.
    38. Varshney, J. P. and Dey, S. (1998). A clinical study on haemoprotozoan infections in referral canines. J. Remount Vet. Corps, 37: 83–89.
    39. Verdida, R. A., Hara, O. A., Xuan, X., Fukumoto, S., Igarashi, I., Zhang, S., Dong, J., et al. (2004). Serodiagnosis of Babesia gibsoni infection in dogs by an improved enzyme-linked immunosorbent assay with recombinant truncated P50. J. Vet. Med. Sci., 66: 1517-1521.
    40. Yamane, I., Gardener, I. A., Ryan, C. P., Levy, M., Urrico, J. and Conrad, P. A. (1994). Serosurvey of Babesia canis, Babesia gibsoni and Ehrlichia canis in pound dogs in California, USA. Prev. Vet. Med., 18: 293-304.
    41. Yamane, I., Thomford, J. W., Gardner, I. A., Dubey, J. P., Levy, M. and Conard, P. A. (1993). Evaluation of the indirect fluorescent antibody test for diagnosis of Babesia gibsoni infections in dogs. Am. J. Vet. Res., 54: 1579-1584. 
    42. Yao, D., Jiang, J., Yu, Z., Yao, D., Yang, D. and Zhao, Y. (2014). Canine Babesiosis in China caused by Babesia gibsoni: A molecular approach. Iranian J. Parasitol., 9: 163–168. 
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