Endemic, exotic and novel apicomplexan parasites detected during a national study of ticks from companion animals in Australia

Abstract

BackgroundApicomplexan tick-borne pathogens that cause disease in companion animals include species of Babesia Starcovici, 1893, Cytauxzoon Neitz & Thomas, 1948, Hepatozoon Miller, 1908 and Theileria Bettencourt, Franca & Borges, 1907. The only apicomplexan tick-borne disease of companion animals that is known to occur in Australia is babesiosis, caused by Babesia canis vogeli Reichenow, 1937 and Babesia gibsoni Patton, 1910. However, no molecular investigations have widely investigated members of Apicomplexa Levine, 1980 in Australian ticks that parasitise dogs, cats or horses, until this present investigation.ResultsTicks (n = 711) removed from dogs (n = 498), cats (n = 139) and horses (n = 74) throughout Australia were screened for piroplasms and Hepatozoon spp. using conventional PCR and Sanger sequencing. The tick-borne pathogen B. vogeli was identified in two Rhipicephalus sanguineus Latreille ticks from dogs residing in the Northern Territory and Queensland (QLD). Theileria orientalis Yakimov & Sudachenkov, 1931 genotype Ikeda was detected in three Haemaphysalis longicornis Neumann ticks from dogs in New South Wales. Unexpectedly, the exotic tick-borne pathogen Hepatozoon canis James, 1905 was identified in an Ixodes holocyclus Neumann tick from a dog in QLD. Eight novel piroplasm and Hepatozoon species were identified and described in native ticks and named as follows: Babesia lohae n. sp., Babesia mackerrasorum n. sp., Hepatozoon banethi n. sp., Hepatozoon ewingi n. sp., Theileria apogeana n. sp., Theileria palmeri n. sp., Theileria paparinii n. sp. and Theileria worthingtonorum n. sp. Additionally, a novel cf. Sarcocystidae sp. sequence was obtained from Ixodes tasmani Neumann but could not be confidently identified at the genus level.ConclusionsNovel species of parasites in ticks represent an unknown threat to the health of companion animals that are bitten by these native tick species. The vector potential of Australian ticks for the newly discovered apicomplexans needs to be assessed, and further clinical and molecular investigations of these parasites, particularly in blood samples from dogs, cats and horses, is required to determine their potential for pathogenicity.Electronic supplementary materialThe online version of this article (10.1186/s13071-018-2775-y) contains supplementary material, which is available to authorized users.

An Australian dog diagnosed with an exotic tick-borne infection: should Australia still be considered free from Hepatozoon canis?

“…Furthermore, only six R. sanguineus s.l. ticks from Sarina, Qld were tested during the previous study by Greay et al (2018). Regardless of the route of infection, we hypothesise that the dog subsequently developed a parasitaemia and it seems likely that H. canis was present in the I. holocyclus tick as a result of the ingestion of H. canis-infected blood from the dog.…”

“…During a molecular survey of ticks (n = 711) for apicomplexan parasites in 2017, H. canis DNA was detected in an engorged Ixodes holocyclus (paralysis tick) female that was removed from a 3-month-old Maremma Sheepdog from Sarina, Queensland (Qld, Australia)) in 2014 (Greay et al, 2018). The dog, born in the city of Rockhampton, Qld, 200 km south west of Sarina, was located and the owner consented to a blood test to evaluate the health and parasite status of the dog.…”

“…For molecular confirmation of H. canis in the blood sample, DNA was extracted using a DNeasy Blood & Tissue Kit (Qiagen, Hilden, Germany) following the manufacturer's recommendations. The 18S gene was amplified using conventional PCR with apicomplexan 18SApiF/18SApiR primers (Greay et al, 2018), Hepatozoon spp. HepF300/Hep900 primers (Ujvari et al, 2004) and Hepatozoon spp.…”

“…HEMO1/HEMO2 primers (Perkins and Keller, 2001) that target approximately 300 bp, 600 bp and 900 bp of 18S, respectively. The PCR, Sanger sequencing and sequence analysis methodologies were carried out as described in Greay et al (2018). The sequences obtained with the 18SApiF/18SApiR primer set (303 bp, GenBank® accession no.…”

“…Although H. canis DNA was not found in R. sanguineus s.l. (0/183; 95% confidence interval (CI), 0-2) or H. longicornis (0/75; 95% CI, 0-4.8) in the apicomplexan survey of ticks in Australia (Greay et al, 2018), the prevalence of H. canis in ticks collected from dogs in endemic areas overseas has been reported to be as low as 1.5% (4/267) (Dantas-Torres et al, 2012). Furthermore, only six R. sanguineus s.l.…”