Field and experimental symptomless infections support wandering donkeys as healthy carriers of Trypanosoma vivax in the Brazilian Semiarid, a region of outbreaks of high mortality in cattle and sheep

Abstract

BackgroundThe Brazilian Semiarid is the home of the largest herd of donkeys in South America and of outbreaks of Trypanosoma vivax infection of high mortality in dairy cattle and sheep. For a comprehensive understanding of the underlying mechanisms of these outbreaks and epidemiological role of donkeys, we surveyed for T. vivax in wandering donkeys and follow the experimental infection of donkeys and sheep with a highly virulent isolate from the Semiarid.MethodsBlood samples from 180 randomly selected wandering donkeys from the Brazilian Semiarid region were employed for PCV and parasitemia assessments and tested using the T. vivax-specific TviCATL-PCR assay. PCR-amplifed Cathepsin L (CATL) sequences were employed for genotyping and phylogenetic analysis. Four wandering donkeys were experimentally infected with a T. vivax isolate obtained during an outbreak of high mortality in the Semiarid; the control group consisted of two non-inoculated donkeys.ResultsWe detected T. vivax in 30 of 180 wandering donkeys (16.6 %) using TviCATL-PCR. The prevalence was higher during the dry (15.5 %) than the wet season (1.1 %) and more females (23.1 %) than males (8.9 %) were infected. All the PCR-positive donkeys lacked patent parasitemia and showed normal values of body condition score (BCS) and packed cell volume (PCV). To evaluate the probable tolerance of donkeys to T. vivax, we inoculated five donkeys with a highly virulent isolate (TviBrRp) from the Semiarid. All inoculated donkeys became PCR-positive, but their parasitemia was always subpatent. A control goat inoculated with TviBrRp showed increasing parasitemia concurrently with fever, declining PCV, tachycardia, mucous membrane pallor, enlarged lymph nodes and anorexia. None of these signs were observed in donkeys. However, T. vivax from wandering donkeys shared identical or highly similar genotypes (identified by Cathepsin L sequences) with isolates from cattle and sheep outbreaks of acute disease in the Semiarid.ConclusionsThis is the first report of T. vivax in donkeys in Brazil and, to our knowledge, the first experimental infection of donkeys with T. vivax. The symptomless field and experimental infections corroborated that donkeys are more tolerant to T. vivax than other livestock species as shown in African countries. Therefore, farmers, veterinaries and control programmes should be aware of healthy carrier donkeys as a possible source of T. vivax for susceptible livestock species in the Brazilian Semiarid.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-015-1169-7) contains supplementary material, which is available to authorized users.

Equine trypanosomosis: enigmas and diagnostic challenges

“…For example, donkeys can carry an infection without developing classical signs of the diseases [45]. Typical, but not pathognomonic, are pyrexia, anaemia, ventral and genital oedema, urticarial plaques, conjunctivitis and keratitis, etc.…”

New insights from Gorongosa National Park and Niassa National Reserve of Mozambique increasing the genetic diversity of Trypanosoma vivax and Trypanosoma vivax-like in tsetse flies, wild ungulates and livestock from East Africa

“…This finding was corroborated by phylogenetic studies suggesting that T. vivax was introduced into the New World via cattle imported from WA by European colonisers [ 8 , 19 , 20 ]. In contrast with the genetic homogeneity of isolates from SA [ 8 , 13 , 19 , 21 ] and WA [ 4 , 8 , 22 , 23 ], studies have unveiled greater genetic diversity among isolates from Tanzania, Mozambique (MZ), Kenya and Ethiopia [ 2 , 7 , 19 , 24 – 27 ]. Sequences of gGAPDH from Tanzanian isolates obtained from tsetse flies diverged largely from those detected in cattle and nyala antelope from MZ, which were closer to WA/SA than to another EA T. vivax [ 25 , 26 ].…”

Variation in disease phenotype is marked in equine trypanosomiasis

“…The results of this study support a greater resilience to Trypanosoma spp. infection in donkeys compared to horses providing objective data to support previous subjective observations [12,26]. Historical evidence documents the problems encountered during repeated attempts to introduce the horse to the African continent which have been largely attributed to Trypanosoma spp.…”

“…prevalence (by PCR) was similar in a random sample of equids with no concerns noted by owner to those presenting for veterinary examination, however clinical examination findings were not reported [12]. Asymptomatic wandering donkeys infected with Trypanosoma vivax have also been identified in Brazil [26] and in sampled equid populations prevalence of disease in donkeys has been reported to be lower than in horses [12,14,15,27]. In horses, higher infection rates have been reported in female horses and horses > 1 year-old [14].…”