Canine Hepatozoonosis and Babesiosis, and Feline Cytauxzoonosis

Veterinary Clinics of North America - Small Animal Practice

Volumn 39, Issue 6, 2009, Pages 1035-1053

  Holman, Patricia J ^a   Snowden, Karen F ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Apicomplexa; Hemoprotozoa; Parasite; Protozoa; Tick borne disease

Indexed keywords

ACARICIDE; AMITRAZ; ATOVAQUONE; ATROPINE; AZITHROMYCIN; BUPARVAQUONE; CLINDAMYCIN; COTRIMAZINE; DECOQUINATE; DECOXX; DIMINAZENE ACETURATE; DOXIROBE; DOXYCYCLINE; ENROFLOXACIN; IMIDOCARB DIPROPIONATE; NONSTEROID ANTIINFLAMMATORY AGENT; PARVAQUONE; PENICILLIN G; PREDNISOLONE; PYRIMETHAMINE; TETRACYCLINE; TOLTRAZURIL; UNCLASSIFIED DRUG;

ANTIBODY DETECTION; APICOMPLEXAN INFECTION; BABESIA; BABESIA CANIS; BABESIA CONRADAE; BABESIA GIBSONI; BABESIOSIS; CAT DISEASE; CLINICAL FEATURE; CYTAUXZOONOSIS; DIAGNOSTIC IMAGING; DOG DISEASE; DRUG EFFICACY; DRUG RESPONSE; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUID THERAPY; HEPATOZOONOSIS; INFECTION CONTROL; INSECT CONTROL; LABORATORY DIAGNOSIS; LIFE CYCLE ASSESSMENT; MONOTHERAPY; NONHUMAN; PARASITE IDENTIFICATION; PARASITE TRANSMISSION; PATHOGENESIS; POLYMERASE CHAIN REACTION; RECOMMENDED DRUG DOSE; REVIEW; TREATMENT DURATION; VECTOR CONTROL;

ANIMALS; CAT DISEASES; CATS; DOG DISEASES; DOGS; PROTOZOAN INFECTIONS, ANIMAL;

APICOMPLEXA; BABESIA; CYTAUXZOON; FELIDAE; HEPATOZOON; IXODIDA; PROTOZOA;

EID: 72149121866     PISSN: 01955616     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cvsm.2009.08.002     Document Type: Review

References (100)

1. Panciera R.J., and Ewing S.A. American canine hepatozoonosis. Anim Health Res Rev 4 1 (2003) 27-34
2. Craig T.M., Smallwood J.E., Knauer K.W., et al. Hepatozoon canis infection in dogs: clinical, radiographic and hematologic findings. J Am Vet Med Assoc 173 (1978) 967-972
3. Vincent-Johnson N.A., Macintire D.K., Lindsay D.S., et al. A new Hepatozoon species from dogs: description of the causative agent of canine hepatozoonosis in North America. J Parasitol 83 (1997) 1165-1172
4. Baneth G., Mathew J.S., Shkap V., et al. Canine hepatozoonosis: two disease syndromes caused by separate Hepatozoon spp. Trends Parasitol 19 1 (2003) 27-31
5. Macintire D.K., Vincent-Johnson N.A., and Craig T.M. Hepatozoon americanum infection. In: Greene C.J. (Ed). Infectious diseases of the dog and cat. 3rd edition (2006), WB Saunders, St Louis MO 705-711
6. Vincent-Johnson N.A. American canine hepatozoonosis. Vet Clin North Am Small Anim Pract 33 (2003) 905-920
7. Allen K., Li Y., Kaltenboeck B., et al. Diversity of Hepatozoon species in naturally infected dogs in the southern United States. Vet Parasitol 154 (2008) 220-225
8. Li Y., Wang C., Allen K.E., et al. Diagnosis of canine Hepatozoon spp. infection by quantitative PCR. Vet Parasitol 157 (2008) 50-58
9. Murata T., Inoue M., Tateyama S., et al. Vertical transmission of Hepatozoon canis in dogs. J Vet Med Sci 55 (1993) 867-868
10. Garrett J.J., Kocan A.A., Panciera M.V., et al. Experimental infection of adult and juvenile coyotes with domestic dog and wild coyote isolates of Hepatozoon americanum (Apicomplexa: Adeleorina). J Wldl Dis 41 3 (2005) 588-592
11. Mercer S.H., Jones L.P., Rappole J.H., et al. Hepatozoon sp. in wild carnivores in Texas. J Wildl Dis 24 (1988) 574-576
12. Johnson E.M., Allen K.E., Breshears M.A., et al. Experimental transmission of Hepatozoon americanum to rodents. Vet Parasitol 151 (2008) 164-169
13. Ewing S.A., Panciera R.J., and Mathew J.S. Persistence of Hepatozoon americanum (Apicomplexa: Adeleorina) in a naturally infected dog. J Parasitol 89 3 (2003) 611-613
14. Drost W.T., Cummings C.A., Mathew J.S., et al. Determination of time of onset and location of early skeletal lesions in young dogs experimentally infected with Hepatozoon americanum using bone scintigraphy. Vet Radiol Ultrasound 44 1 (2003) 86-91
15. Mercer S.H., and Craig T.M. Comparison of various staining procedures in the identification of Hepatozoon canis gamonts. Vet Clin Pathol 17 (1988) 63-65
16. Mathew J.S., Saliki J.T., Ewing S.A., et al. An indirect enzyme-linked immunosorbent assay for diagnosis of American canine hepatozoonosis. J Vet Diagn Invest 13 (2001) 17-21
17. Criado-Fornelio A., Buling A., Cunha-Filho N.A., et al. Development and evaluation of a quantitative PCR assay for detection of Hepatozoon sp. Vet Parasitol 150 (2007) 352-356
18. Rubini A.S., Paduan K.D.S., Lopes V.V.A., et al. Molecular and parasitological survey of Hepatozoon canis (Apicomplexa: Hepatozoidae) in dogs from rural area of Sao Paulo state, Brazil. Parasitol Res 102 (2008) 895-899
19. Macintire D.K., Vincent-Johnson N.A., Kane C.W., et al. Treatment of dogs infected with Hepatozoon americanum: 53 cases (19897-1998). J Am Vet Med Assoc 218 1 (2001) 77-82
20. Kjemtrup A.M., Wainwright K., Miller M., et al. Babesia conradae, sp. nov., a small canine Babesia identified in California. Vet Parasitol 138 1/2 (2006) 103-111
21. Birkenheuer A.J., Neel J., Ruslander D., et al. Detection and molecular characterization of a novel large Babesia species in a dog. Vet Parasitol 124 (2004) 151-160
22. Holman PJ, Backlund B, Wilcox A et al. First out of state case of canine babesiosis caused by a large unnamed piroplasm originally described in North Carolina. J Am Vet Med Assoc, in press.
23. Levine N.D. Apicomplexa: the piroplasms. Veterinary protozoology. 1st edition (1985), Iowa State University Press, Ames (IA) 291-328
24. Groves M.G., and Yap L.F. Babesia gibsoni (Patton, 1910) from a dog in Kuala Lumpur. Med J Malaya 22 (1968) 229
25. Anderson J.F., Magnarelli L.A., Donner C.S., et al. Canine Babesia new to North America. Science 204 (1979) 1431-1432
26. Farwell G.E., Le Grand E.K., and Cobb C.C. Clinical observations of Babesia gibsoni and Babesia canis infections in dogs. J Am Vet Med Assoc 5 (1982) 507-511
27. Birkenheuer A.J., Correa M.T., Levy M.G., et al. Geographic distribution of babesiosis among dogs in the United States and association with dog bites: 150 cases (2000-2003). J Am Vet Med Assoc 227 (2005) 942-947
28. Bostrom B., Wolf C., Greene C., et al. Sequence conservation in the rRNA first internal transcribed spacer region of Babesia gibsoni genotype Asia isolates. Vet Parasitol 152 1/2 (2008) 152-157
29. Kjemtrup A.M., Kocan A.A., Whitworth L., et al. There are at least three genetically distinct small piroplasms from dogs. Int J Parasitol 30 (2000) 1501-1505
30. Zahler M., Rinder H., Zweygarth E., et al. 'Babesia gibsoni' of dogs from North America and Asia belong to different species. Parasitology 120 (2000) 365-369
31. Kjemtrup A.M., and Conrad P.A. A review of the small canine piroplasms from California: Babesia conradae in the literature. Vet Parasitol 138 1/2 (2006) 112-117
32. Meinkoth J.H., Kocan A.A., Loud S.D., et al. Clinical and hematology effects of experimental infection of dogs with recently identified Babesia gibsoni-like isolates from Oklahoma. J Am Vet Med Assoc 220 (2002) 185-189
33. Boozer A.L., and Macintire D.K. Canine babesiosis. Vet Clin North Am Small Anim Pract 33 (2003) 885-904
34. Birkenheuer A.J., Levy M.G., Stebbins M., et al. 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 (2003) 551-557
35. Birkenheuer A.J., Levy M.G., Savary K.C., et al. Babesia gibsoni infection in dogs from North Carolina. J Am Anim Hosp Assoc 35 (1999) 125-128
36. Macintire D.K., Boudreaux M.K., West G.D., et al. Babesia gibsoni infection among dogs in the southeastern United States. J Am Vet Med Assoc 220 (2002) 325-329
37. Irizarry-Rovira A.R., Stephens J., Christian J., et al. Babesia gibsoni infection in a dog from Indiana. Vet Clin Pathol 30 (2001) 180-188
38. Kocan A.A., Kjemtrup A., Meinkoth J., et al. A genotypically unique Babesia gibsoni -like parasite recovered from a dog in Oklahoma. J Parasitol 87 (2001) 437-438
39. Stegeman J., Birkenheuer A.J., Kruger J.M., et al. Transfusion-associated Babesia gibsoni infection in a dog. J Am Vet Med Assoc 222 (2003) 959-963
40. Matsuu A., Kawabe A., Koshida Y., et al. Incidence of canine Babesia gibsoni infection and subclinical infection among Tosa dogs in Aomori Prefecture, Japan. J Vet Med Sci 66 (2004) 893-897
41. Higuchi S., Konno H., Hoshi F., et al. Observations of Babesia gibsoni in the ovary of the tick, Haemaphysalis longicornis. Kitasato Arch Exp Med 65 Suppl (1993) 153-158
42. Higuchi S., Fujimori M., Hoshi F., et al. Development of Babesia gibsoni in the salivary glands of the larval tick, Rhipicephalus sanguineus. J Vet Med Sci 57 1 (1995) 117-119
43. Swaminath C.S., and Shortt H.E. The arthropod vector of Babesia gibsoni. Indian J Med Res 25 2 (1937) 499-503
44. Yamane I., Gardner I.A., Telford III S.R., et al. Vector competence of Rhipicephalus sanguineus and Dermacentor variabilis for American isolates of Babesia gibsoni. Exp Appl Acarol 17 (1993) 913-919
45. Fukumoto S., Suzuki H., Igarashi I., et al. Fatal experimental transplacental Babesia gibsoni infections in dogs. Int J Parasitol 35 (2005) 1031-1035
46. Jefferies R.R., Jardine U.M., Broughton J., et al. Bull Terriers and Babesiosis: further evidence for direct transmission of Babesia gibsoni in dogs. Aust Vet J 85 11 (2007) 459-463
47. Inokuma H., Okuda M., Yoshizaki Y., et al. Clinical observations of Babesia gibsoni infection with low parasitaemia confirmed by PCR in dogs. Vet Rec 156 4 (2005) 116-118
48. Botros B.A.M., Moch R.W., and Barsoum I.S. Some observations on experimentally induced infection of dogs with Babesia gibsoni. Am J Vet Res 36 (1975) 293-296
49. Yamane I., Gardener I., Ryan C., et al. Serosurvey of Babesia canis, Babesia gibsoni, and Ehrlichia canis in pound dogs in California, USA. Prev Vet Med 18 (1994) 293-304
50. Conrad P.A., Thomford J., Yamane I., et al. Hemolytic anemia caused by Babesia gibsoni infection in dogs. J Am Vet Med Assoc 199 (1991) 601-605
51. Wozniak E.J., Barr B.C., Thomford J.M., et al. Clinical, anatomic, and immunopathologic characterization of Babesia gibsoni infection in the domestic dog (Canis familiaris). J Parasitol 83 4 (1997) 692-699
52. Eaton P. Piroplasma canis in Florida. J Parasitol 20 (1934) 312-313
53. Hauschild S., Shayan P., and Schein E. Characterization and comparison of merozoite antigens of different Babesia canis isolates by serological and immunological investigations. Parasitol Res 81 (1995) 638-642
54. Schetters T.H.P.M., Moubri K., Precigout E., et al. Different Babesia canis isolates, different diseases. Parasitology 115 (1997) 485-493
55. Uilenberg G., Franssen F.F.J., Perié N.M., et al. Three groups of Babesia canis distinguished and a proposal for nomenclature. Vet Q 11 (1989) 33-40
56. Zahler M., Schein E., Rinder H., et al. Characteristic genotypes discriminate between Babesia canis isolates of differing vector specificity and pathogenicity to dogs. Parasitol Res 84 7 (1998) 544-548
57. Martinod S., Laurent N., and Moreau Y. Resistance and immunity of dogs against Babesia canis in an endemic area. Vet Parasitol 19 (1986) 245-254
58. Hill M.W.M., and Bolton B.L. Canine babesiosis in Queensland. Aust Vet J 42 (1966) 391-392
59. Freeman M.J., Kirby B.M., Panciera D.L., et al. Hypotensive shock syndrome associated with acute Babesia canis infection in a dog. J Am Vet Med Assoc 204 1 (1994) 94-96
60. Breitschwerdt E.B., Malone J.B., MacWilliams P., et al. Babesiosis in the greyhound. J Am Vet Med Assoc 182 (1983) 978-982
61. Hauschild S., and Schein E. The subspecies specificity of Babesia canis. Berl Munch Tierarztl Wochenschr 109 (1996) 216-219
62. Bansal S.R., Kharole M.U., and Banerjee D.P. Clinicopathological studies in experimental Babesia canis infection in dogs. J Vet Parasitol 4 1 (1990) 21-25
63. Ristic M., Lykins J.D., Smith A.R., et al. Babesia canis and Babesia gibsoni: soluble and corpuscular antigens isolated from blood of dogs. Exp Parasitol 30 (1971) 385-392
64. Brown G.K., Canfield P.J., Dunstan R.H., et al. Detection of Anaplasma platys and Babesia canis vogeli and their impact on platelet numbers in free-roaming dogs associated with remote Aboriginal communities in Australia. Aust Vet J 84 9 (2006) 321-325
65. Lehtinen L.E., Birkenheuer A.J., Droleskey R.E., et al. In vitro cultivation of a newly recognized Babesia sp. in dogs in North Carolina. Vet Parasitol 151 2/4 (2008) 150-157
66. Mehlhorn H., and Schein E. The piroplasms: life cycle and sexual stages. Adv Parasitol 23 (1984) 37-103
67. Anderson J.F., Magnarelli L.A., and Sulzer A.J. Canine babesiosis: indirect fluorescent antibody test for a North American isolate of Babesia gibsoni. Am J Vet Res 41 (1980) 2102-2105
68. Jefferies R., Ryan U.M., and Irwin P.J. PCR-RFLP for the detection and differentiation of the canine piroplasm species and its use with filter paper-based technologies. Vet Parasitol 144 1/2 (2007) 20-27
69. Vercammen F., De Deken R., and Maes L. Prophylactic treatment of experimental canine babesiosis (Babesia canis) with doxycycline. Vet Parasitol 66 (1996) 251-255
70. Adeyanju B.J., and Aliu Y.O. Chemotherapy of canine ehrlichiosis and Babesiosis with imidocarb dipropionate. J Am Anim Hosp Assoc 18 (1982) 827-830
71. Penzhorn B.L., Lewis B.D., de Waal D.T., et al. Sterilisation of Babesia canis infections by imidocarb alone or in combination with diminazene. J S Afr Vet Assoc 66 (1995) 157-159
72. Matsuu A., Koshida Y., Kawahara M., et al. Efficacy of atovaquone against Babesia gibsoni in vivo and in vitro. Vet Parasitol 124 (2004) 9-18
73. Birkenheuer A.J., Levy M.G., and Breitschwerdt E.B. Efficacy of combined atovaquone and azithromycin for therapy of chronic Babesia gibsoni (Asian genotype) infections in dogs. J Vet Intern Med 18 (2004) 494-498
74. Jefferies R., Ryan U.M., and Jardine J. Babesia gibsoni: detection during experimental infections and after combined atovoquone and azithromycin therapy. Exp Parasitol 117 (2007) 115-123
75. Matjila P.T., Penzhorn B.L., Leisewitz A.L., et al. Molecular characterisation of Babesia gibsoni infection from a pit-bull terrier pup recently imported into South Africa. J S Afr Vet Assoc 78 1 (2007) 2-5
76. Wagner J.E. Cytauxzoonosis in domestic cats (Felis domestica) in Missouri. J Am Vet Med Assoc 167 (1975) 874
77. Wagner J.E. A fatal cytauxzoonosis-like disease in cats. J Am Vet Med Assoc 68 (1976) 585-588
78. Kier AB. The etiology and pathogenesis of feline cytauxzoonosis. 1979. PhD Dissertation, University of Missouri, Columbia, MO.
79. Bendele R.A., Schwartz W.L., and Jones L.P. Cytauxzoonosis-like disease in Texas cats. Southwestern Vet 29 (1976) 244-246
80. Wightman S.R., Kier A.B., and Wagner J.E. Feline cytauxzoonosis: clinical features of a newly described blood parasite disease. Feline Pract 7 (1977) 23-26
81. Hauck W.N. Cytauxzoonosis in a native Louisiana cat. J Am Vet Med Assoc 180 (1982) 1472-1474
82. Glenn B.L., and Stair E.L. Cytauxzoonosis in domestic cats: report of 2 cases in Oklahoma, with review and discussion of the disease. J Am Vet Med Assoc 184 (1984) 822-825
83. Hoover J.P., Walker D.B., and Hedges J.D. Cytauxzoonosis in cats: 8 cases (1985-1992). J Am Vet Med Assoc 205 (1994) 455-460
84. Ferris D.H. A progress report on the status of a new disease of American cats: cytauxzoonosis. Comp Immunol Microbiol Infect Dis 1 (1979) 269-276
85. Walker D.B., and Cowell R.L. Survival of a domestic cat with naturally acquired cytauxzoonosis. J Am Vet Med Assoc 206 (1995) 1363-1365
86. Meinkoth J., Kocan A.A., Whitworth L., et al. Cats surviving natural infections with Cytauxzoon felis: 18 cases (1997-1998). J Vet Intern Med 14 (2000) 521-525
87. Greene C.E., Latimer K., Hopper E., et al. Administration of diminazene aceturate or imidocarb dipropionate for treatment of cytauxzoonosis in cats. J Am Vet Med Assoc 215 4 (1999) 497-500
88. Birkenheuer A.J., Le J.A., Valenzisi A.M., et al. Cytauxzoon felis infection in cats in the mid-Atlantic states: 34 cases (1998-2004). J Am Vet Med Assoc 228 4 (2006) 568-571
89. Haber M.D., Tucker M.D., Marr H.S., et al. The detection of Cytauxzoon felis in apparently healthy free-roaming cats in the USA. Vet Parasitol 146 3/4 (2007) 316-320
90. Jackson C.B., and Fisher T. Fatal cytauxzoonosis in a Kentucky cat (Felis domesticus). Vet Parasitol 139 (2006) 192-195
91. Kier A.B., Wagner J.E., and Kinden D.A. The pathology of experimental cytauxzoonosis. J Comp Pathol 97 (1987) 415-432
92. Blouin E.F., Kocan A.A., Glenn B.L., et al. Transmission of Cytauxzoon felis (Kier, 1979) from bobcats, Lynx rufus (Schreber), to domestic cats by Dermacentor variabilis (Say). J Wildl Dis 20 (1984) 241-242
93. Reichard M.V., Baum K.A., Cadenhead S.C., et al. Temporal occurrence and environmental risk factors associated with cytauxzoonosis in domestic cats. Vet Parasitol 152 (2008) 314-320
94. Kier A.B., Wagner J.E., and Morehouse L.G. Experimental transmission of Cytauxzoon felis from bobcats (Lynx rufus) to domestic cats (Felis domesticus). Am J Vet Res 43 (1982) 97-101
95. Glenn B.L., Kocan A.A., and Blouin E.F. Cytauxzoonosis in bobcats. J Am Vet Med Assoc 183 (1983) 1155-1158
96. Birkenheuer A.J., Mar H.S., Warren C., et al. Cytauxzoon felis infections are present in bobcats (Lynx rufus) in a region where cytauxzoonosis is not recognized in domestic cats. Vet Parasitol 153 (2008) 126-130
97. Meinkoth J., Cowell R.L., and Cowell A.K. What is your diagnosis? 10-year-old vomiting, anorexic cat. Vet Clin Pathol 25 (1996) 48
98. Birkenheuer A.J., Marr H., Alleman A.R., et al. Development and evaluation of a PCR assay for the detection of Cytauxzoon felis DNA in feline blood samples. Vet Parasitol 137 (2006) 144-149
99. Motzel S.L., and Wagner J.E. Treatment of experimentally induced cytauxzoonosis in cats with parvoquone and buparvaquone. Vet Parasitol 35 (1990) 131-138
100. Uilenberg G., Franssen F.F.J., and Perié N.M. Relationships between Cytauxzoon felis and African piroplasmids. Vet Parasitol 26 (1987) 21-28