Molecular epizootiology of canine hepatozoonosis in Croatia

International Journal for Parasitology

Volumn 39, Issue 10, 2009, Pages 1129-1136

  Vojta, Lea ^a   Mrljak, Vladimir ^b   Ćurković, Snježana ^b   Živičnjak, Tatjana ^a   Marinculić, Albert ^a   Beck, Relja ^a  

^a UNIVERSITY OF ZAGREB   (Croatia)

^b UNIVERSITY OF ZAGREB   (Croatia)

Author keywords

Dogs; Hepatozoon; Heterogeneity; Isolate groups; Molecular detection; Sequence analysis

Indexed keywords

DNA; NUCLEOTIDE; PROTOZOAL DNA; RNA 18S;

CANID; GENE; HETEROGENEITY; MOLECULAR ANALYSIS; PARASITE; PROTOZOAN; RNA;

ANIMAL TISSUE; APICOMPLEXA; ARTICLE; BLOOD SAMPLING; CLETHRIONOMYS GLAREOLUS; CONSENSUS SEQUENCE; CONTROLLED STUDY; CROATIA; DNA ISOLATION; DOG; EPIZOOTIOLOGY; GENE MUTATION; GENETIC HETEROGENEITY; HEPATOZOON; HEPATOZOON CANIS; HEPATOZOONOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PREVALENCE; RNA SEQUENCE; UNINDEXED SEQUENCE; ANIMAL; COCCIDIOSIS; DOG DISEASES; GENETICS; MOLECULAR GENETICS; PARASITOLOGY; PROTOZOAN INFECTIONS, ANIMAL; VETERINARY;

ANIMALS; COCCIDIOSIS; CROATIA; DNA, PROTOZOAN; DOG DISEASES; DOGS; MOLECULAR SEQUENCE DATA; POLYMERASE CHAIN REACTION; PREVALENCE; PROTOZOAN INFECTIONS, ANIMAL; RNA, RIBOSOMAL, 18S;

CROATIA; EURASIA; EUROPE; SOUTHERN EUROPE;

CANIS FAMILIARIS; CLETHRIONOMYS GLAREOLUS; HEPATOZOON; HEPATOZOON CANIS;

EID: 67649447023     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2009.02.007     Document Type: Article

References (72)

1. Allen K.E., Yihang L., Kaltenboeck B., Johnson E.M., Reichard M.V., Panciera R.J., and Little S.E. Diversity of Hepatozoon species in naturally infected dogs in southern United States. Vet. Parasitol. 154 (2008) 220-225
2. Alencar N.X., Kohayagawa A., and Santarém V.A. Hepatozoon canis infection of wild carnivores in Brazil. Vet. Parasitol. 70 (1997) 279-282
3. Arru R., Pau S., and Leoni A. Segnalazione di Hepatozoon canis in Sardegna. Riv. Parassitol. 43 (1982) 57-62
4. Assarasakorn S., Niwetpathomwat A., Techangamsuwan S., and Suvarnavibhaja S. A retrospective study of clinical hematology and biochemistry of canine hepatozoonosis on hospital populations in Bangkok, Thailand. Comp. Clin. Pathol. 15 (2006) 107-109
5. Baneth G., Harmelin A., and Presentey B.Z. Hepatozoon canis infection in two dogs. J. Am. Vet. Med. Assoc. 206 (1995) 1891-1894
6. Baneth G., Shkap V., Presentey B.Z., and Pipano E. Hepatozoon canis: the prevalence of antibodies and gametocytes in dogs in Israel. Vet. Res. Commun. 20 (1996) 41-46
7. Baneth G., and Weigler B. Retrospective case-control study of hepatozoonosis in dogs in Israel. J. Vet. Intern. Med. 11 (1997) 365-370
8. Baneth G., Aroch I., and Presentey B. Hepatozoon canis infection in a litter of Dalmatian dogs. Vet. Parasitol. 70 (1997) 201-206
9. Baneth G., Barta J.R., Martin D.S., Macintire D.K., and Vincent-Johnson N. Genetic and antigenic evidence supports the separation of Hepatozoon canis and Hepatozoon americanum at the species level. J. Clin. Microbiol. 38 (2000) 1298-1301
10. Baneth G., Samish M., Alekseev E., Aroch I., and Shkap V. Transmission of Hepatozoon canis to dogs by naturally-fed or percutaneously-injected Rhipicephalus sanguineus ticks. J. Parasitol. 87 (2001) 606-611
11. Baneth G., Mathew J.S., Shkap V., Macintire D.K., Barta J.R., and Ewing S.A. Canine hepatozoonosis-two disease syndromes caused by separate Hepatozoon species. Trends Parasitol. 19 (2003) 27-31
12. Baneth G., Samish M., and Shkap V. Life cycle of Hepatozoon canis (Apicomplexa: Adeleorina: Hepatozoidae) in the tick Rhipicephalus sanguineus and domestic dog (Canis familiaris). J. Parasitol. 93 (2007) 283-299
13. Beaufils J.P., Martin-Granel J., and Bertrand F. Hépatozoonose canine. 2e partie. Apropos de 28 cas. Prat. Med. Chir. Anim. Cie. 23 (1988) 281-293
14. Beaufils J.P., Martin-Granel J., and Bertrand F. Atteinte médullaire sélective et hématopoièse extra-médullaire chez un chien infecté par Ehrlichia canis et Hepatozoon canis. Prat. Med. Chir. Anim. Cie. 26 (1991) 347-353
15. Cacciò S.M., and Ryan U. Molecular epidemiology of giardiasis. Mol. Biochem. Parasitol. 160 (2008) 75-80
16. Conceicao-Silva F., Abranches P., Silva-Pereira M., and Janz J. Hepatozoonosis in foxes from Portugal. J. Wildl. Dis. 24 (1988) 344-347
17. Criado-Fornelio A., Martinez-Marcos A., Buling-Saraña A., and Barba-Carretero J.C. Molecular studies on Babesia, Theileria and Hepatozoon in southern Europe. Part I. Epizootiological aspects. Vet. Parasitol. 113 (2003) 189-201
18. Criado-Fornelio A., Martinez-Marcos A., Buling-Saraña A., and Barba-Carretero J.C. Molecular studies on Babesia, Theileria and Hepatozoon in southern Europe. Part II. Phylogenetic analysis and evolutionary history. Vet. Parasitol. 114 (2003) 173-194
19. Criado-Fornelio A., Ruas J.L., Casado N., Farias N.A., Soares M.P., Muller G., Brumt J.G., Berne M.E., Buling-Sarana A., and Barba-Carretero J.C. New molecular data on mammalian Hepatozoon species (Apicomplexa: Adeleorina) from Brazil and Spain. J. Parasitol. 92 (2006) 93-99
20. Criado-Fornelio A., Rey-Valeiron C., Buling A., Barba-Carretero J.C., Jefferies R., and Irwin P. New advances in molecular epizootiology of canine hematic protozoa from Venezuela, Thailand and Spain. Vet. Parasitol. 144 (2007) 261-269
21. Criado-Fornelio A., Buling A., Cunha-Filho N.A., Ruas J.L., Farias N.A., Rey-Valeiron C., Pingret J.L., Etievant M., and Barba-Carretero J.C. Development and evaluation of a quantitative PCR assay for detection of Hepatozoon sp. Vet. Parasitol. 150 (2007) 352-356
22. Criado-Fornelio A., Buling A., Pingret J.L., Etievant M., Boucraut-Baralon C., Alongi A., Agnone A., and Torina A. Hemoprotozoa of domestic animals in France: Prevalence and molecular characterization. Vet. Parasitol. (2008) 10.1016/j.vetpar.2008.10.012
23. Dantas-Torres F. The brown dog tick, Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae): from taxonomy to control. Vet. Parasitol. 152 (2008) 173-185
24. Deinert M., Kraft W., and Gothe R. Hepatozoon canis infection of dogs in Germany: case report and epidemiology. Tierarztl. Prax. 25 (1997) 254-256
25. Domina F., and Catarsini O. Hepatozoon canis: Rilievo occasionale di 9 casi. Atti. Soc. Ital. Sci. Vet. 36 (1982) 358-360
26. Eiras D.F., Basabe J., Scodellaro C.F., Banach D.B., Matos M.L., Krimer A., and Baneth G. First molecular characterization of canine hepatozoonosis in Argentina: evaluation of asymptomatic Hepatozoon canis infection in dogs from Buenos Aires. Vet. Parasitol. 149 (2007) 275-279
27. Fischer S., Hartmann K., and Gothe R. Hepatozoon canis: an important parasitic infection in dogs. Tierarztl. Prax. 22 (1994) 172-180
28. Fishman Z., Gonen L., Harrus S., Strauss-Ayali D., King R., and Baneth G. A serosurvey of Hepatozoon canis and Ehrlichia canis antibodies in wild red foxes (Vulpes vulpes) from Israel. Vet. Parasitol. 119 (2004) 21-26
29. Forlano M.D., Teixeira K.R.S., Scofield A., Elisei C., Yotoko K.S.C., Fernades K.R., Linhares G.F.C., Ewing S.A., and Massard C.L. Molecular characterization of Hepatozoon sp. from Brazilian dogs and it phylogenetic relationship with other Hepatozoon spp. Vet. Parasitol. 145 (2007) 21-30
30. Gal A., Harrus S., Arcoh I., Lavy E., Aizenberg I., Mekuzas-Yisaschar Y., and Baneth G. Coinfection with multiple tick-borne and intestinal parasites in a 6-week-old dog. Can. Vet. J. 48 (2007) 619-622
31. Garcia P., Acedo M.C., Lopez J.J., Sanchis M.C., and Morrilas F. Identificiacion de Hepatozoon canis (James, 1905) en Espana. Estudio epidemiologico de una enzootia en La Carolina (Jaén, Espana). Invest. Agr. Prod. Sanid. Anim. 5 (1990) 75-89
32. Gavazza A., Bizzeti M., and Papini R. Observations on dogs found naturally infected with Hepatozoon canis in Italy. Rev. Med. Vet. 154 (2003) 565-571
33. Glaser B., and Gothe R. Imported arthropod-borne parasites and parasitic arthropods in dogs. Species spectrum and epidemiologic analysis of the cases diagnosed in 1995/96. Tierarztl. Prax. Ausg. K. Kleintiere Heimtiere 26 (1998) 40-46
34. Gondim L.F.P., Kohayagawa A., Alencar N.X., Biondo A.W., Takahira R.F., and Franco S.R.V. Canine hepatozoonosis in Brazil: description of eight naturally occurring cases. Vet. Parasitol. 74 (1998) 319-323
35. Inokuma H., Yamamoto S., and Morita C. Survey of tick-borne diseases in dogs infested with Rhypicephalus sanguineus at a Kennel in Okayama Prefecture, Japan. J. Vet. Med. Sci. 60 (1998) 761-763
36. Inokuma H., Ohno K., and Yamamoto S. Serosurvey of Ehrlichia canis and Hepatozoon canis infection in dogs in Yamaguchi Prefecture, Japan. J. Vet. Med. Sci. 61 (1999) 1153-1155
37. Inokuma H., Okuda M., Ohno K., Shimoda K., and Onishi T. Analysis of the 18S rRNA gene sequence of a Hepatozoon detected in two Japanese dogs. Vet. Parasitol. 106 (2002) 265-271
38. Jeanmougin F., Thompson J.D., Gouy M., Higgins D.G., and Gibson T.J. Multiple sequence alignment with Clustal X. Trends Biochem. Sci. 23 (1998) 403-405
39. Jittapalapong S., Rungphisuthipongse O., Maruyama S., Schaefer J.J., and Stich R.W. Detection of Hepatozoon canis in stray dogs and cats in Bangkok, Thailand. Ann. NY Acad. Sci. 1081 (2006) 479-488
40. Karagenc T.I., Pasa S., Kirli G., Hosgor M., Bilgic H.B., Ozon Y.H., Atasoy A., and Eren H. A parasitological, molecular and serological survey of Hepatozoon canis infection in dogs around the Aegean coast of Turkey. Vet. Parasitol. 135 (2006) 113-119
41. Kontos V., and Koutinas A. Canine hepatozoonosis: a review of 11 naturally occurring cases. Eur. J. Comp. Anim. Pract. 2 (1991) 26-30
42. Kumar S., Nei M., Dudley J., and Tamur K. MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform. 9 (2008) 299-306
43. Li Y., Wang C., Allen K.E., Little S.E., Ahluwalia S.K., Gao D., Macintire D.K., Blagburn B.L., and Kaltenboeck B. Diagnosis of canine Hepatozoon spp. infection by quantitative PCR. Vet. Parasitol. 157 (2008) 50-58
44. Mancitire D.K., Vincent-Johnson N.A., Dillon A.R., Blagburn B., Lindsay D.S., Whitley E.M., and Banfield C. Hepatozoonosis in dogs: 22 cases (1989-1994). J. Am. Vet. Med. Assoc. 210 (1997) 916-922
45. Macintire D.K., Vincent-Johnson N., Kane C.W., Lindsay D.S., Blagburn B.L., and Dillon A.R. Treatment of dogs infected with Hepatozoon americanum: 53 cases (1989-1998). J. Am. Vet. Med. Assoc. 218 (2001) 77-82
46. Majláthová V., Hurníková Z., Majláth I., and Petko B. Hepatozoon canis infection in Slovakia: imported or autochthonous?. Vector Borne Zoonotic Dis. 7 (2007) 199-202
47. Mathew J.S., Van Den Bussche R.A., Ewing A.S., Malayer J.R., Latha B.R., and Panciera R.J. Phylogenetic relationships of Hepatozoon (Apicomplexa: Adeleorina) based on molecular, morphologic and life-cycle characters. J. Parasitol. 86 (2000) 366-372
48. Metzger B., dos Santos Paduan K., Rubini A.S., de Oliveira T.G., Pereira C., and O'Dwyer L.H. The first report of Hepatozoon sp. (Apicomplexa: Hepatozoidae) in neotropical felids from Brazil. Vet. Parasitol. 152 (2008) 28-33
49. Mundim A.V., de Morais I.A., Tavares M., Cury M.C., and Santos Mundim M.J. Clinical and hematological signs associated with dogs naturally infected by Hepatozoon sp. and with other hematozoa: a retrospective study in Uberlândia, Minas Gerais, Brazil. Vet. Parasitol. 153 (2008) 3-8
50. Mylonakis M.E., Koutinas A.F., Baneth G., Polizopoulou Z., and Fytianou A. Mixed Ehrlichia canis, Hepatozoon canis, and presumptive Anaplasma phagocytophilum infection in a dog. Vet. Clin. Pathol. 33 (2004) 249-251
51. O'Dwyer L.H., Massard C.L., and Pereira de Souza J.C. Hepatozoon canis infection associated with dog ticks of rural areas of Rio de Janiero State, Brazil. Vet. Parasitol. 94 (2001) 143-150
52. O'Dwyer L.H., Saito M.E., Hasegawa M.Y., and Kohayagawa A. Tissue stages of Hepatozoon canis in naturally infected dogs from São Paulo State, Brazil. Parasitol. Res. 94 (2004) 240-242
53. O'Dwyer L.H., Saito M.E., Hasegawa M.Y., and Kohayagawa A. Prevalence, hematology and serum biochemistry in stray dogs naturally infected by Hepatozoon canis in São Paulo. Arq. Bras. Med. Vet. Zootec. 58 (2006) 688-690
54. Oyamada M., Davoust B., Boni M., Dereure J., Bucheton B., Hammad A., Itamoto K., Okuda M., and Inokuma H. Detection of Babesia canis rossi, B. canis vogeli, and Hepatozoon canis in dogs in a village of eastern Sudan by using a screening PCR and sequencing methodologies. Clin. Diagn. Lab. Immunol. 2 (2005) 1343-1346
55. Paludo G.R., Dell'Porto A., de Castro e Trindade A.R., McManus C., and Friedman H. Hepatozoon spp.: report of some cases in dogs in Brasília, Brazil. Vet. Parasitol. 118 (2003) 243-248
56. Paludo G.R., Friedmann H., Dell'Porto A., Macintire D.K., Whitley E.M., Boudreaux M.K., Baneth G., Blagburn B.L., and Dykstra C.C. Hepatozoon spp.: pathological and partial 18S rRNA sequence analysis from three Brazilian dogs. Parasitol. Res. 97 (2005) 167-170
57. Rajamanickam C., Wiesenhutter E., Zin F., and Hamid J. The incidence of canine hematozoa in peninsular Malaysia. Vet. Parasitol. 17 (1985) 151-157
58. Rebelo M.E. Hepatozoon canis em canídeos domésticos na zona do Alto-Douro, concelho de alijó. Rep. Trab. LINV 21 (1989) 99-102
59. Rosati S. Segnalazione di Hepatozoon canis nella provincia di Imperia. Ann. Fac. Med. Vet. Torino 31 (1986) 156-162
60. Rubini A.S., Paduan K.S., Cavalcante G.G., Ribolla P.E.M., and O'Dwyer L.H. Molecular identification and characterization of canine Hepatozoon species from Brazil. Parasitol. Res. 97 (2005) 91-93
61. Rubini A.S., Dos Santos Paduan K., Perez R.R., Ribolla P.E., and O'Dwyer L.H. Molecular characterization of feline Hepatozoon species from Brazil. Vet. Parasitol. 137 (2006) 168-171
62. Rubini A.S., dos Santos Paduan K., Von Ah Lopes V., and O'Dwyer L.H. Molecular and parasitological survey of Hepatozoon canis (Apicomplexa: Hepatozoidae) in dogs from rural area of São Paulo state, Brazil. Parasitol. Res. 102 (2008) 895-899
63. Sasaki M., Omobowale O., Ohta K., Tozuka M., Matsuu A., Hirata H., Nottidge H.O., Ikadai H., and Oyamada T. A PCR-based epidemiological survey of Hepatozoon canis in dogs in Nigeria. J. Vet. Med. Sci. 70 (2008) 743-745
64. Sloboda M., Kamler M., Bulantová J., Votýpka J., and Modrý D. Rodents as intermediate hosts of Hepatozoon ayorgbor (Apicomplexa: Adeleina: Hepatozoonidae) from the African ball python, Python regius?. Folia Parasitol. (Praha) 55 (2008) 13-16
65. Smith T.G. The genus Hepatozoon (Apicomplexa: Adeleina). J. Parasitol. 82 (1996) 565-585
66. Stenzenberger I., and Gothe R. Arthropodenübertragene parasitäre Infektionen und Zecken bei Hunden auf Teneriffa. Tierärztl. Prax. 27 (1999) 47-52
67. Thompson J.D., Higgins D.G., and Gibson T.J. CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res. 22 (1994) 4673-4680
68. Tsachev I., Ivanov A., Dinev I., Simeonova G., and Kanakov D. Clinical Ehrlichia canis and Hepatozoon canis co-infection in a dog in Bulgaria. Revue Méd. Vét. 159 (2008) 68-73
69. Vincent-Johnson N.A., Macintire D.K., and Baneth G. Canine hepatozoonosis: pathophysiology, diagnosis and treatment. Comp. Cont. Educ. Pract. Vet. 19 (1997) 51-65
70. Vincent-Johnson N.A., Macintire D.K., Lindsay D.S., Lenz S.D., Baneth G., Shkap V., and Blagburn B.L. A new Hepatozoon species from dogs: description of the causative agent of canine hepatozoonosis in North America. J. Parasitol. 83 (1997) 1165-1172
71. Voyvoda H., Pasa S., and Uner A. Clinical Hepatozoon canis infection in a dog in Turkey. J. Small Anim. Pract. 45 (2004) 613-617
72. Yabsley M.J., McKibben J., Macpherson C.N., Cattan P.F., Cherry N.A., Hegarty B.C., Breitschwerdt E.B., O'Connor T., Chandrashekar R., Paterson T., Perea M.L., Ball G., Friesen S., Goedde J., Henderson B., and Sylvester W. Prevalence of Ehrlichia canis, Anaplasma platys, Babesia canis vogeli, Hepatozoon canis, Bartonella vinsonii berkhoffii, and Rickettsia spp. in dogs from Grenada. Vet. Parasitol. 151 (2008) 279-285