Detection of DNA of Babesia canis in tissues of laboratory rodents following oral inoculation with infected ticks

. 2020 Apr 03 ; 13 (1) : 166. [epub] 20200403

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid32245520

Grantová podpora
PCCDI 57/2018 UEFISCDI

Odkazy

PubMed 32245520
PubMed Central PMC7118908
DOI 10.1186/s13071-020-04051-z
PII: 10.1186/s13071-020-04051-z
Knihovny.cz E-zdroje

BACKGROUND: Babesia spp. are apicomplexan parasites which infect a wide range of mammalian hosts. Historically, most Babesia species were described based on the assumed host specificity and morphological features of the intraerythrocytic stages. New DNA-based approaches challenge the traditional species concept and host specificity in Babesia. Using such tools, the presence of Babesia DNA was reported in non-specific mammalian hosts, including B. canis in feces and tissues of insectivorous bats, opening questions on alternative transmission routes. The aim of the present study was to evaluate if B. canis DNA can be detected in tissues of laboratory rodents following oral inoculation with infected ticks. METHODS: Seventy-five questing adult Dermacentor reticulatus ticks were longitudinally cut in two halves and pooled. Each pool consisted of halves of 5 ticks, resulting in two analogous sets. One pool set (n = 15) served for DNA extraction, while the other set (n = 15) was used for oral inoculation of experimental animals (Mus musculus, line CD-1 and Meriones unguiculatus). Blood was collected three times during the experiment (before the inoculation, at 14 days post-inoculation and at 30 days post-inoculation). All animals were euthanized 30 days post-inoculation. At necropsy, half of the heart, lung, liver, spleen and kidneys were collected from each animal. The presence of Babesia DNA targeting the 18S rRNA gene was evaluated from blood and tissues samples. For histopathology, the other halves of the tissues were used. Stained blood smears were used for the light microscopy detection of Babesia. RESULTS: From the 15 pools of D. reticulatus used for the oral inoculation, six were PCR-positive for B. canis. DNA of B. canis was detected in blood and tissues of 33.3% of the animals (4 out of 12) inoculated with a B. canis-positive pool. No Babesia DNA was detected in the other 18 animals which received B. canis-negative tick pools. No Babesia was detected during the histological examination and all blood smears were microscopically negative. CONCLUSIONS: Our findings demonstrate that B. canis DNA can be detected in tissues of mammalian hosts following ingestion of infected ticks and opens the question of alternative transmission routes for piroplasms.

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Solano-Gallego L, Baneth G. Babesiosis in dogs and cats: expanding parasitological and clinical spectra. Vet Parasitol. 2011;181:48–60. doi: 10.1016/j.vetpar.2011.04.023. PubMed DOI

Schnittger L, Rodriguez AE, Florin-Christensen M, Morrison DA. Babesia: a world emerging. Infect Genet Evol. 2012;12:1788–1809. doi: 10.1016/j.meegid.2012.07.004. PubMed DOI

Vannier EG, Diuk-Wasser MA, Mamoun CB, Krause PJ. Babesiosis. Infect Dis Clin N Am. 2015;29:357–370. doi: 10.1016/j.idc.2015.02.008. PubMed DOI PMC

Alvarado-Rybak M, Solano-Gallego L, Millán J. A review of piroplasmid infections in wild carnivores worldwide: importance for domestic animal health and wildlife conservation. Parasit Vectors. 2016;9:538. doi: 10.1186/s13071-016-1808-7. PubMed DOI PMC

Hunfeld K, Hildebrandt A, Gray JS. Babesiosis: recent insights into an ancient disease. Int J Parasitol. 2008;38:1219–1237. doi: 10.1016/j.ijpara.2008.03.001. PubMed DOI

Irwin P. Canine babesiosis: from molecular taxonomy to control. Parasit Vectors. 2009;2(Suppl. 1):S4. doi: 10.1186/1756-3305-2-S1-S4. PubMed DOI PMC

Homer MJ, Aguilar-Delfin I, Telford SR, 3rd, Krause PJ, Persing DH. Babesiosis. Clin Microbiol Rev. 2000;13:451–469. doi: 10.1128/CMR.13.3.451. PubMed DOI PMC

Uilenberg G, Gray J, Kahl O. Research on Piroplasmorida and other tick-borne agents: are we going the right way? Ticks Tick Borne Dis. 2018;9:860–863. doi: 10.1016/j.ttbdis.2018.03.005. PubMed DOI

Schreeg ME, Marr HS, Tarigo JL, Cohn LA, Bird DM, Scholl EH, et al. Mitochondrial genome sequences and structures aid in the resolution of Piroplasmida phylogeny. PLoS One. 2016;11:e0165702. doi: 10.1371/journal.pone.0165702. PubMed DOI PMC

Beck A, Tatjana Z, Beck R, Vojta L, Mrljak V, Marinculic A, et al. Diversity of Babesia and Theileria species in symptomatic and asymptomatic dogs in Croatia. Int J Parasitol. 2009;39:843–848. doi: 10.1016/j.ijpara.2008.12.005. PubMed DOI

Gallusová M, Qablan MA, D’Amico G, Obomik M, Petrželková KJ, Modrý D. Piroplasms in feral and domestic equines in rural areas of the Danube Delta, Romania, with survey of dogs as a possible reservoir. Vet Parasitol. 2014;206:287–292. doi: 10.1016/j.vetpar.2014.10.018. PubMed DOI

Criado-Fornelio A, Martinez-Marcos A. Presence of Mycoplasma haemofelis, Mycoplasma haemominutum and piroplasmids in cats from southern Europe: a molecular study. Vet Microbiol. 2003;93:307–317. doi: 10.1016/S0378-1135(03)00044-0. PubMed DOI

Vilhena H, Martinez-Diaz VL, Cardoso L, Vieira L, Altet L, Francino O, et al. Feline vector-borne pathogens in the north and centre of Portugal. Parasit Vectors. 2013;6:99. doi: 10.1186/1756-3305-6-99. PubMed DOI PMC

Földvári G, Pave Š, Szekeres S, Majoros G, Sprong H. Dermacentor reticulatus: a vector on the rise. Parasit Vectors. 2016;9:314. doi: 10.1186/s13071-016-1599-x. PubMed DOI PMC

Olivieri E, Zanzani SA, Latrofa MS, Lia RP, Dantas-Torres F, Otranto D, et al. The southernmost foci of Dermacentor reticulatus in Italy and associated Babesia canis infection in dogs. Parasit Vectors. 2016;9:213. doi: 10.1186/s13071-016-1502-9. PubMed DOI PMC

Solano-Gallego L, Sainz Á, Roura X, Estrada-Peña A, Miró G. A review of canine babesiosis: the European perspective. Parasit Vectors. 2016;9:336. doi: 10.1186/s13071-016-1596-0. PubMed DOI PMC

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. doi: 10.1186/s13071-015-1052-6. PubMed DOI PMC

Corduneanu A, Sándor AD, Mihalca AD, Hrazdilová K, Modrý D, Hornok S. Molecular evidence of canine pathogens in tissues of European bats. In: Proc. 17th International bat research conference Durban, South Africa. 2016; p. 50–1. https://www.researchgate.net/publication/332833641.

Hornok S, Szöke K, Kováts D, Estók P, Görföl T, Boldogh SA, et al. DNA of piroplasms of ruminants and dogs in ixodid bat ticks. PLoS One. 2016;11:e0167735. doi: 10.1371/journal.pone.0167735. PubMed DOI PMC

Baneth G, Samish M, Shkap V. Life cycle of Hepatozoon canis (Apicomplexa: Adeleorina: Hepatozoidae) in the tick Rhipicephalus sanguineus and domestic dog (Canis familiaris) J Parasitol. 2007;93:283–299. doi: 10.1645/GE-494R.1. PubMed DOI

Murata T, Inoue M, Tateyama S, Taura Y, Nakama S. Vertical transmission of Hepatozoon canis in dogs. J Vet Med Sci. 1993;55:867–868. doi: 10.1292/jvms.55.867. PubMed DOI

Mathew JS, Ewing SA, Panciera RJ, Woods JP. Experimental transmission of Hepatozoon americanum to dogs by the Gulf Cost tick, Amblyomma maculatum. Vet Parasitol. 1998;80:1–14. doi: 10.1016/S0304-4017(98)00189-7. PubMed DOI

Forlano M, Scofield A, Elisei C, Fernandes KR, Ewing SA, Massard CL. Diagnosis of Hepatozoon spp. in Amblyomma ovale and its experimental transmission in domestic dogs in Brazil. Vet Parasitol. 2005;134:1–7. doi: 10.1016/j.vetpar.2005.05.066. PubMed DOI

Rubini AS, dos Santos Paduan K, Cavalcante GG, Ribolla PE, OʼDwyer LH. Molecular identification and characterization of canine Hepatozoon species from Brazil. Parasitol Res. 2005;97:91–93. doi: 10.1007/s00436-005-1383-x. PubMed DOI

Široký P, Kamler M, Modrý D. Prevalence of Hemolivia mauritanica (Apicomplexa: Adeleina: Haemogregarinidae) in natural populations of tortoises of the genus Testudo in the East Mediterranean region. Folia Parasitol. 2005;52:359–361. doi: 10.14411/fp.2005.049. PubMed DOI

Paperna I. Hemolivia mauritanica (Haemogregarinidae: Apicomplexa) infection in the tortoise Testudo graeca in the Near East with data on sporgonous development in the tick vector Hyalomna aegypticum. Parasite. 2006;13:267–273. doi: 10.1051/parasite/2006134267. PubMed DOI

Široký P, Kamler M, Frye FL, Fictum P, Modrý D. Endogenous development of Hemolivia mauritanica (Apicomplexa: Adeleina: Haemogregarinidae) in the marginated tortoise Testudo marginata (Reptilia: Testudinidae): evidence from experimental infection. Folia Parasitol. 2007;54:13–18. doi: 10.14411/fp.2007.002. PubMed DOI

Kvičerová J, Hypša V, Dvořáková N, Mikulíček P, Jandzik D, Gardner MG, et al. Hemolivia and Hepatozoon: haemogregarines with tangled evolutionary relationships. Protist. 2014;165:688–700. doi: 10.1016/j.protis.2014.06.001. PubMed DOI

de Sousa KC, Fernandes MP, Herrera HM, Benevenute JL, Santos FM, Rocha FL, et al. Molecular detection of Hepatozoon spp. in domestic dogs and wild mammals in southern Pantanal, Brazil with implications in the transmission route. Vet Parasitol. 2017;237:37–46. doi: 10.1016/j.vetpar.2017.02.023. PubMed DOI

Giannelli A, Lia RP, Annoscia G, Buonavoglia C, Lorusso E, Dantas-Torres F, et al. Rhipicephalus turanicus, a new vector of Hepatozoon canis. Parasitology. 2017;144:730–737. doi: 10.1017/S003118201600250X. PubMed DOI

Demoner LC, Magro NM, da Silva MRL, de Paula Antunes JMA, Calabuig CIP, O’Dwyer LH. Hepatozoon spp. infections in wild rodents in an area of endemic canine hepatozoonosis in south-eastern Brazil. Ticks Tick Borne Dis. 2013;78:59–64. PubMed

Estrada-Peña A, Mihalca AD, Petney TN. Ticks of Europe and North Africa. A guide to species identification. Cham: Springer; 2017.

Zintl A, Finnerty EJ, Murphy TM, De Waal T, Gray JS. Babesias of red deer (Cervus elaphus) in Ireland. Vet Res. 2011;42:7. doi: 10.1186/1297-9716-42-7. PubMed DOI PMC

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. doi: 10.1186/s13071-015-0692-x. PubMed DOI PMC

Corduneanu A, Hrazdilová K, Sándor AD, Matei IA, Ionică AM, Barti L, et al. Babesia vesperuginis, a neglected piroplasmid: new hosts and geographical records, and phylogenetic relations. Parasit Vectors. 2017;10:598. doi: 10.1186/s13071-017-2536-3. PubMed DOI PMC

Teeling EC, Springer MS, Madsen O, Bates P, O’Brien SJ, Murphy WJ. A molecular phylogeny for bats illuminates biogeography and the fossil record. Science. 2005;307:580–584. doi: 10.1126/science.1105113. PubMed DOI

Jones G. Bats. In: MacDonald D, editor. The encyclopedia of mammals (2nd ed.). Oxford: Oxford University Press; 2001. p. 754–75.

Dietz C, Nill D, von Helversen O. Bats of Britain, Europe and Northwest Africa. London: A&C Black; 2009.

Krüger F, Clare EL, Symondson WO, Keišs O, Pētersons G. Diet of the insectivorous bat Pipistrellus nathusii during autumn migration and summer residence. Mol Ecol. 2014;23:3672–3683. doi: 10.1111/mec.12547. PubMed DOI

Wray AK, Jusino MA, Banik MT, Palmer JM, Kaarakka H, White JP, et al. Incidence and taxonomic richness of mosquitoes in the diets of little brown and big brown bats. J Mammal. 2018;99:668–674. doi: 10.1093/jmammal/gyy044. DOI

Johnson EM, Panciera RJ, Allen KE, Sheets ME, Beal JD, Ewing SA, et al. Alternate patway of infection with Hepatozoon americanum and the epidemiologic importance of predation. J Vet Intern Med. 2009;23:1315–1318. doi: 10.1111/j.1939-1676.2009.0375.x. PubMed DOI

Malagon F, Tapia JL. Experimental transmission of Babesia microti infection by the oral route. Parasitol Res. 1994;80:645–648. doi: 10.1007/BF00932947. PubMed DOI

Dkhil MA. Hepatic tissue damage induced in Meriones ungliculatus due to infection with Babesia divergens - infected erythrocytes. Saudi J Biol Sci. 2010;17:129–132. doi: 10.1016/j.sjbs.2010.02.005. PubMed DOI PMC

Dkhil MA, Abdel-Baki AS, Al-Quraishy S, Abdel-Moneim AE. Hepatic oxidative stress in Mongolian gerbils experimentally infected with Babesia divergens. Ticks Tick Borne Dis. 2013;4:346–351. doi: 10.1016/j.ttbdis.2013.01.002. PubMed DOI

Dkhil MA, Al-Quraishy S, Al-Khalifa MS. The effect of Babesia divergens infection on the spleen of Mongolian gerbils. BioMed Res Int. 2014;2014:483854. doi: 10.1155/2014/483854. PubMed DOI PMC

Irwin PJ, Hutchinson GW. Clinical and pathological findings of Babesia infection in dogs. Aust Vet J. 1991;68:204–209. doi: 10.1111/j.1751-0813.1991.tb03194.x. PubMed DOI

Máthé A, Dobos-Kovács M, Vӧrӧs K. Histological and ultrastructural studies of renal lesions in Babesia canis infected dogs treated with imidocarb. Acta Vet Hung. 2007;55:511–523. doi: 10.1556/AVet.55.2007.4.10. PubMed DOI

Wozniak EJ, Barr BC, Thomford JW, Yamane I, Donough SP, Moore PF, et al. Clinical, anatomic, and immunopathologic characterization of Babesia gibsoni infection in the domestic dog (Canis familiaris) J Parasitol. 1197;83:692–699. doi: 10.2307/3284248. PubMed DOI

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