The first report on Hepatozoon canis in dogs and wolves in Poland: clinical and epidemiological features.
Canis lupus familiaris
Hepatozoon canis
Hepatozoonosis
PCR
Poland
Ticks
Wolves
Journal
Parasites & vectors
ISSN: 1756-3305
Titre abrégé: Parasit Vectors
Pays: England
ID NLM: 101462774
Informations de publication
Date de publication:
04 Sep 2023
04 Sep 2023
Historique:
received:
27
05
2023
accepted:
14
08
2023
medline:
6
9
2023
pubmed:
5
9
2023
entrez:
4
9
2023
Statut:
epublish
Résumé
Canine hepatozoonosis caused by Hepatozoon canis is a common infection in dogs, with frequent case reports from the Mediterranean region and more recently from several Central European countries, such as Hungary and Germany. Despite the high prevalence of H. canis in red foxes, no infections have been reported to date in dogs in Poland. We describe here the first autochthonous cases of H. canis infection in dogs, including their clinical features, and report the prevalence of H. canis in grey wolves from different regions of Poland. Thin smears prepared from blood samples collected from dogs were evaluated by microscopic examination. A total of 60 wolves and 47 dogs were tested. Infections were confirmed by PCR and sequencing. Gamonts of H. canis were found in > 50% of the neutrophils of two dogs and in < 10% of the neutrophils in another five dogs. Molecular typing by PCR sequencing of the 18S ribosomal RNA gene fragment confirmed infections in 11 dogs from different regions of Poland, in 2.7% of dogs attending veterinary practices in central Poland and in 35% of wolves from various geographical regions of Poland. Clinical features manifested mostly in older dogs, and the most common signs were anaemia and apathy. Young dogs usually remained asymptomatic. This is the first report of H. canis infection in dogs and wolves in Poland. Although the exact vector of the parasite is not known, veterinary practitioners should be aware of this new parasitosis and should consider appropriate diagnostics to confirm/exclude this infection. Further studies are needed to understand the transmission routes of H. canis in domestic and wild canids in Poland.
Sections du résumé
BACKGROUND
BACKGROUND
Canine hepatozoonosis caused by Hepatozoon canis is a common infection in dogs, with frequent case reports from the Mediterranean region and more recently from several Central European countries, such as Hungary and Germany. Despite the high prevalence of H. canis in red foxes, no infections have been reported to date in dogs in Poland. We describe here the first autochthonous cases of H. canis infection in dogs, including their clinical features, and report the prevalence of H. canis in grey wolves from different regions of Poland.
METHODS
METHODS
Thin smears prepared from blood samples collected from dogs were evaluated by microscopic examination. A total of 60 wolves and 47 dogs were tested. Infections were confirmed by PCR and sequencing.
RESULTS
RESULTS
Gamonts of H. canis were found in > 50% of the neutrophils of two dogs and in < 10% of the neutrophils in another five dogs. Molecular typing by PCR sequencing of the 18S ribosomal RNA gene fragment confirmed infections in 11 dogs from different regions of Poland, in 2.7% of dogs attending veterinary practices in central Poland and in 35% of wolves from various geographical regions of Poland. Clinical features manifested mostly in older dogs, and the most common signs were anaemia and apathy. Young dogs usually remained asymptomatic.
CONCLUSIONS
CONCLUSIONS
This is the first report of H. canis infection in dogs and wolves in Poland. Although the exact vector of the parasite is not known, veterinary practitioners should be aware of this new parasitosis and should consider appropriate diagnostics to confirm/exclude this infection. Further studies are needed to understand the transmission routes of H. canis in domestic and wild canids in Poland.
Identifiants
pubmed: 37667369
doi: 10.1186/s13071-023-05928-5
pii: 10.1186/s13071-023-05928-5
pmc: PMC10476436
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
313Subventions
Organisme : Polish National Science Centre
ID : 2020/39/B/NZ9/01829
Organisme : Polish National Science Centre
ID : 2019/35/O/NZ8/01550
Informations de copyright
© 2023. BioMed Central Ltd., part of Springer Nature.
Références
Baneth G. Perspectives on canine and feline hepatozoonosis. Vet Parasitol. 2011;181:3–11.
pubmed: 21620568
doi: 10.1016/j.vetpar.2011.04.015
Dantas-Torres F, Otranto D. Hepatozoonosis. In: Marcondes CB, editor. Arthropod borne diseases. Cham: Springer International Publishing; 2017. p. 363–8.
Murata T, Inoue M, Tateyama S, Taura Y, Nakama S. Vertical transmission of Hepatozoon canis in dogs. J Vet Med Sci. 1993;55:867–8.
pubmed: 8286548
doi: 10.1292/jvms.55.867
James SP. On a parasite found in the white corpuscles of the blood of dogs. Calcutta: Office of the Superintendent of Government; 1905.
Andersson M, Turcitu MA, Stefanache M, Tamba P, Barbuceanu F, Chitimia L. First evidence of Anaplasma platys and Hepatozoon canis co-infection in a dog from Romania—a case report. Ticks Tick Borne Dis. 2013;4:317–9.
pubmed: 23528989
doi: 10.1016/j.ttbdis.2012.12.006
Andersson MO, Tolf C, Tamba P, Stefanache M, Waldenström J, Dobler G, et al. Canine tick-borne diseases in pet dogs from Romania. Parasit Vectors. 2017;10:155.
pubmed: 28335825
pmcid: 5364683
doi: 10.1186/s13071-017-2092-x
Ciuca L, Martinescu G, Miron LD, Roman C, Acatrinei D, Cringoli G, et al. Occurrence of Babesia species and co-Infection with Hepatozoon canis in symptomatic dogs and in their ticks in eastern Romania. Pathogens. 2021;10:1339.
pubmed: 34684287
pmcid: 8538781
doi: 10.3390/pathogens10101339
Dantas-Torres F. Climate change, biodiversity, ticks and tick-borne diseases: the butterfly effect. Int J Parasitol Parasites Wildl. 2015;4:452–61.
pubmed: 26835253
pmcid: 4699983
doi: 10.1016/j.ijppaw.2015.07.001
Hansford KM, Pietzsch ME, Cull B, Gillingham EL, Medlock JM. Potential risk posed by the importation of ticks into the UK on animals: records from the tick surveillance scheme. Vet Rec. 2018;182:107–107.
pubmed: 29217768
doi: 10.1136/vr.104263
Hornok S, Tánczos B, de Fernández Mera IG, de la Fuente J, Hofmann-Lehmann R, Farkas R. High prevalence of Hepatozoon-infection among shepherd dogs in a region considered to be free of Rhipicephalus sanguineus. Vet Parasitol. 2013;196:189–93.
pubmed: 23499483
doi: 10.1016/j.vetpar.2013.02.009
Hamel D, Silaghi C, Zapadynska S, Kudrin A, Pfister K. Vector-borne pathogens in ticks and EDTA-blood samples collected from client-owned dogs, Kiev, Ukraine. Ticks Tick Borne Dis. 2013;4:152–5.
pubmed: 23069260
doi: 10.1016/j.ttbdis.2012.08.005
Mitkova B, Hrazdilova K, Novotna M, Jurankova J, Hofmannova L, Forejtek P, et al. Autochthonous Babesia canis, Hepatozoon canis and imported Babesia gibsoni infection in dogs in the Czech Republic. Vet Med (Praha). 2017;62:138–46.
doi: 10.17221/152/2016-VETMED
Helm CS, von Samson-Himmelstjerna G, Liesner JM, Kohn B, Müller E, Schaper R, et al. Identical 18S rRNA haplotypes of Hepatozoon canis in dogs and foxes in Brandenburg, Germany. Ticks Tick Borne Dis. 2020;11:101520.
pubmed: 32993940
doi: 10.1016/j.ttbdis.2020.101520
Attipa C, Maguire D, Solano-Gallego L, Szladovits B, Barker EN, Farr A, et al. Hepatozoon canis in three imported dogs: a new tickborne disease reaching the United Kingdom. Vet Rec. 2018;183:716.
Hodžić A, Alić A, Fuehrer HP, Harl J, Wille-Piazzai W, Duscher GG. A molecular survey of vector-borne pathogens in red foxes (Vulpes vulpes) from Bosnia and Herzegovina. Parasit Vectors. 2015;8:88.
pubmed: 25889961
pmcid: 4367825
doi: 10.1186/s13071-015-0692-x
Mierzejewska EJ, Dwużnik D, Koczwarska J, Stańczak Ł, Opalińska P, Krokowska-Paluszak M, et al. The red fox (Vulpes vulpes), a possible reservoir of Babesia vulpes, B. canis and Hepatozoon canis and its association with the tick Dermacentor reticulatus occurrence. Ticks Tick Borne Dis. 2021;12:101551.
pubmed: 33002808
doi: 10.1016/j.ttbdis.2020.101551
Hodžić A, Mrowietz N, Cézanne R, Bruckschwaiger P, Punz S, Habler VE, et al. Occurrence and diversity of arthropod-transmitted pathogens in red foxes (Vulpes vulpes) in western Austria, and possible vertical (transplacental) transmission of Hepatozoon canis. Parasitology. 2018;145:335–44.
pubmed: 28835291
doi: 10.1017/S0031182017001536
Duscher GG, Fuehrer HP, Kübber-Heiss A. Fox on the run—molecular surveillance of fox blood and tissue for the occurrence of tick-borne pathogens in Austria. Parasit Vectors. 2014;7:521.
pubmed: 25413694
pmcid: 4243377
Karbowiak G, Majláthová V, Hapunik J, Petko B, Wita I. Apicomplexan parasites of red foxes (Vulpes vulpes) in northeastern Poland. Acta Parasitol. 2010;55:210–4.
doi: 10.2478/s11686-010-0030-6
Majláthová V, Hurníková Z, Majláth I, Peťko B. Hepatozoon canis infection in Slovakia: imported or autochthonous? Vector Borne Zoonotic Dis. 2007;7:199–202.
pubmed: 17627439
doi: 10.1089/vbz.2006.0598
Najm NA, Meyer-Kayser E, Hoffmann L, Pfister K, Silaghi C. Hepatozoon canis in German red foxes (Vulpes vulpes) and their ticks: molecular characterization and the phylogenetic relationship to other Hepatozoon spp. Parasitol Res. 2014;113:2679–85.
pubmed: 24802869
doi: 10.1007/s00436-014-3923-8
Farkas R, Solymosi N, Takács N, Hornyák Á, Hornok S, Nachum-Biala Y, et al. First molecular evidence of Hepatozoon canis infection in red foxes and golden jackals from Hungary. Parasit Vectors. 2014;7:303.
pubmed: 24985073
pmcid: 4086283
doi: 10.1186/1756-3305-7-303
Hodžić A, Georges I, Postl M, Duscher GG, Jeschke D, Szentiks CA, et al. Molecular survey of tick-borne pathogens reveals a high prevalence and low genetic variability of Hepatozoon canis in free-ranging grey wolves (Canis lupus) in Germany. Ticks Tick Borne Dis. 2020;11:101389.
pubmed: 32008999
doi: 10.1016/j.ttbdis.2020.101389
Bajer A, Mierzejewska EJ, Rodo A, Bednarska M, Kowalec M, Welc-Falęciak R. The risk of vector-borne infections in sled dogs associated with existing and new endemic areas in Poland: part 1: a population study on sled dogs during the racing season. Vet Parasitol. 2014;202:276–86.
pubmed: 24491396
doi: 10.1016/j.vetpar.2013.12.033
Zygner W, Górski P, Wędrychowicz H. Detection of the DNA of Borrelia afzelii, Anaplasma phagocytophilum and Babesia canis in blood samples from dogs in Warsaw. Vet Rec. 2009;164:465–7.
pubmed: 19363228
doi: 10.1136/vr.164.15.465
Wężyk D, Romanczuk K, Rodo A, Kavalevich D, Bajer A. Haematological indices and immune response profiles in dogs naturally infected and co-infected with Dirofilaria repens and Babesia canis. Sci Rep. 2023;13:2028.
pubmed: 36739305
pmcid: 9899214
doi: 10.1038/s41598-023-29011-2
Bajer A, Kowalec M, Levytska VA, Mierzejewska EJ, Alsarraf M, Poliukhovych V, et al. Tick-borne pathogens, Babesia spp. and Borrelia burgdorferi s.l., in sled and companion dogs from central and North-Eastern Europe. Pathogens. 2022;11:499.
pubmed: 35631020
pmcid: 9144822
doi: 10.3390/pathogens11050499
Szewczyk M, Nowak S, Niedźwiecka N, Hulva P, Špinkytė-Bačkaitienė R, Demjanovičová K, et al. Dynamic range expansion leads to establishment of a new, genetically distinct wolf population in Central Europe. Sci Rep. 2019;9:19003.
pubmed: 31831858
pmcid: 6908625
doi: 10.1038/s41598-019-55273-w
Alsarraf M, Bednarska M, Mohallal EME, Mierzejewska EJ, Behnke-Borowczyk J, Zalat S, et al. Long-term spatiotemporal stability and dynamic changes in the haemoparasite community of spiny mice (Acomys dimidiatus) in four montane wadis in the St. Katherine Protectorate, Sinai, Egypt. Parasit Vectors. 2016;9:195.
pubmed: 27059180
pmcid: 4826546
doi: 10.1186/s13071-016-1471-z
Inokuma H, Okuda M, Ohno K, Shimoda K, Onishi T. Analysis of the 18S rRNA gene sequence of a Hepatozoon detected in two Japanese dogs. Vet Parasitol. 2002;26:265–71.
doi: 10.1016/S0304-4017(02)00065-1
Tołkacz K, Kowalec M, Alsarraf M, Grzybek M, Dwużnik-Szarek D, Behnke JM, et al. Candidatus Neoehrlichia mikurensis and Hepatozoon sp. in voles (Microtus spp.): occurrence and evidence for vertical transmission. Sci Rep. 2023;13:1733.
pubmed: 36720952
pmcid: 9889374
doi: 10.1038/s41598-023-28346-0
Benson DA, Cavanaugh M, Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, et al. GenBank. Nucleic Acids Res. 2017;45:D37-42.
pubmed: 27899564
doi: 10.1093/nar/gkw1070
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35:1547–9.
pubmed: 29722887
pmcid: 5967553
doi: 10.1093/molbev/msy096
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30:2725–9.
pubmed: 24132122
pmcid: 3840312
doi: 10.1093/molbev/mst197
Gabrielli S, Kumlien S, Calderini P, Brozzi A, Iori A, Cancrini G. The first report of Hepatozoon canis identified in Vulpes vulpes and ticks from Italy. Vector Borne Zoonotic Dis. 2010;10:855–9.
pubmed: 20420538
doi: 10.1089/vbz.2009.0182
Orkun Ö, Nalbantoğlu S. Hepatozoon canis in Turkish red foxes and their ticks. Vet Parasitol Reg Stud Rep. 2018;13:35–7.
De Bonis A, Colombo M, Terragni R, Bacci B, Morelli S, Grillini M, et al. Potential role of Hepatozoon canis in a fatal systemic disease in a puppy. Pathogens. 2021;10:1193.
pubmed: 34578225
pmcid: 8469705
doi: 10.3390/pathogens10091193
Baneth G, Weigler B. Retrospective case-control study of hepatozoonosis in dogs in Israel. J Vet Intern Med. 1997;11:365–70.
pubmed: 9470163
doi: 10.1111/j.1939-1676.1997.tb00482.x
Sasanelli M, Paradies P, Lubas G, Otranto D, de Caprariis D. Atypical clinical presentation of coinfection with Ehrlichia, Babesia and Hepatozoon species in a dog. Vet Rec. 2009;164:22–3.
pubmed: 19122221
doi: 10.1136/vr.164.1.22
Otranto D, Dantas-Torres F, Tarallo VD, de Ramos RAN, Stanneck D, Baneth G, et al. Apparent tick paralysis by Rhipicephalus sanguineus (Acari: Ixodidae) in dogs. Vet Parasitol. 2012;188:325–9.
pubmed: 22546547
doi: 10.1016/j.vetpar.2012.04.005
Uiterwijk M, Vojta L, Šprem N, Beck A, Jurković D, Kik M, et al. Diversity of Hepatozoon species in wild mammals and ticks in Europe. Parasit Vectors. 2023;16:27.
pubmed: 36694253
pmcid: 9872412
doi: 10.1186/s13071-022-05626-8
Smith TG. The genus Hepatozoon (Apicomplexa: Adeleina). J Parasitol. 1996;82:565–85.
pubmed: 8691364
doi: 10.2307/3283781
Johnson EM, Allen KE, Panciera RJ, Ewing SA, Little SE, Reichard MV. Field survey of rodents for Hepatozoon infections in an endemic focus of American canine hepatozoonosis. Vet Parasitol. 2007;150:27–32.
pubmed: 17942230
doi: 10.1016/j.vetpar.2007.08.050
Schäfer I, Müller E, Nijhof AM, Aupperle-Lellbach H, Loesenbeck G, Cramer S, et al. First evidence of vertical Hepatozoon canis transmission in dogs in Europe. Parasit Vectors. 2022;15:296.
pubmed: 35999592
pmcid: 9396588
doi: 10.1186/s13071-022-05392-7
Giannelli A, Ramos RAN, Di Paola G, Mencke N, Dantas-Torres F, Baneth G, et al. Transstadial transmission of Hepatozoon canis from larvae to nymphs of Rhipicephalus sanguineus. Vet Parasitol. 2013;196:1–5.
pubmed: 23537949
doi: 10.1016/j.vetpar.2013.02.017
Hamšíková Z, Silaghi C, Rudolf I, Venclíková K, Mahríková L, Slovák M, et al. Molecular detection and phylogenetic analysis of Hepatozoon spp. in questing Ixodes ricinus ticks and rodents from Slovakia and Czech Republic. Parasitol Res. 2016;115:3897–904.
pubmed: 27245074
doi: 10.1007/s00436-016-5156-5
Dhiab O, D’Amico M, Selmi S. Experimental evidence of increased carcass removal along roads by facultative scavengers. Environ Monit Assess. 2022;195:216.
pubmed: 36539565
doi: 10.1007/s10661-022-10829-8
Bhadra A, Bhattacharjee D, Paul M, Singh A, Gade PR, Shrestha P, et al. The meat of the matter: a rule of thumb for scavenging dogs? Ethol Ecol Evol. 2016;28:427–40.
doi: 10.1080/03949370.2015.1076526
Mysłajek RW, Stachyra P, Figura M, Nędzyńska-Stygar M, Stefański R, Korga M, et al. Diet of the grey wolf Canis lupus in Roztocze and Solska Forest, south-east Poland. J Vertebr Biol. 2022;71:22040.
doi: 10.25225/jvb.22040
Mysłajek RW, Tomczak P, Tołkacz K, Tracz M, Tracz M, Nowak S. The best snacks for kids: the importance of beavers Castor fiber in the diet of wolf Canis lupus pups in north-western Poland. Ethol Ecol Evol. 2019;31:506–13.
doi: 10.1080/03949370.2019.1624278
Bajer A, Welc-Falęciak R, Bednarska M, Alsarraf M, Behnke-Borowczyk J, Siński E, et al. Long-term spatiotemporal stability and dynamic changes in the haemoparasite community of bank voles (Myodes glareolus) in NE Poland. Microb Ecol. 2014;68:196–211.
pubmed: 24604428
pmcid: 4103999
doi: 10.1007/s00248-014-0390-9
Marchetti V, Lubas G, Baneth G, Modenato M, Mancianti F. Hepatozoonosis in a dog with skeletal involvement and meningoencephalomyelitis. Vet Clin Pathol. 2009;38:121–5.
pubmed: 19228365
doi: 10.1111/j.1939-165X.2008.00080.x
Sakuma M, Nakahara Y, Suzuki H, Uchimura M, Sekiya Z, Setoguchi A, et al. A case report: a dog with acute onset of Hepatozoon canis infection. J Vet Med Sci. 2009;71:835–8.
pubmed: 19578300
doi: 10.1292/jvms.71.835
Gherman CM, Mihalca AD. A synoptic overview of golden jackal parasites reveals high diversity of species. Parasit Vectors. 2017;10:419.
pubmed: 28915831
pmcid: 5603039
doi: 10.1186/s13071-017-2329-8
Aguirre AA. Wild canids as sentinels of ecological health: a conservation medicine perspective. Parasit Vectors. 2009;2:S7.
pubmed: 19426446
pmcid: 2679399
doi: 10.1186/1756-3305-2-S1-S7
Hornok S, Estók P, Kováts D, Flaisz B, Takács N, Szőke K, et al. Screening of bat faeces for arthropod-borne apicomplexan protozoa: Babesia canis and Besnoitia besnoiti-like sequences from Chiroptera. Parasit Vectors. 2015;8:441.
pubmed: 26315069
pmcid: 4552134
doi: 10.1186/s13071-015-1052-6
Bajer A, Dwuznik D, Tolkacz K, Alsarraf M, Mierzejewska EJ. Comparison of the detection efficiency of haemoparasite DNA in blood and faecal samples—the way to eco-epidemiological studies. Ann Agric Environ Med. 2019;26:538.
pubmed: 31885225
doi: 10.26444/aaem/109664