Transplacental transmission of Theileria orientalis occurs at a low rate in field-affected cattle: infection in utero does not appear to be a major cause of abortion

Abstract

BackgroundBovine theileriosis, caused by the haemoprotozoan Theileria orientalis, is an emerging disease in East Asia and Australasia. Previous studies have demonstrated transplacental transmission of various Theileria spp. but molecular confirmation of transplacental transmission of T. orientalis has never been confirmed in the field. In this study, cow-calf (< 48 h old) pairs were sampled across 3 herds; opportunistic samples from aborted foetuses or stillborn calves were also examined. Molecular (multiplex qPCR) and serological (ELISA) methods were used to determine infection prevalence and the presence of anti-Theileria antibodies in each herd. In addition, pregnant heifers and foetal calves were sampled at abattoir and tested for the presence of T. orientalis by qPCR.ResultsThe qPCR results indicated that, even though there was a high prevalence of T. orientalis infection in cows, the rate of transplacental transmission to their calves was low, with only one newborn calf from one herd and one foetus from the abattoir testing positive for T. orientalis DNA. Five aborted foetuses and stillborn calves, 3 of which were derived from a herd experiencing a high number of clinical theileriosis cases at the time of sampling, all tested negative for T. orientalis by qPCR. This suggests that in utero infection of calves with T. orientalis may not be a major driver of abortions during theileriosis outbreaks. Temporal monitoring of 20 calves born to T. orientalis-positive mothers indicated that T. orientalis was detectable in most calves between 10 and 27 days post-partum, consistent with prior field studies on adult cattle introduced to Theileria-affected herds. There was a positive correlation between the ELISA ratio of newborn calves and their mothers within 48 h of calving; however, maternal antibodies were only detectable in some calves and only for 4–4.5 weeks post-partum. All calves displayed high parasite loads peaking at 4–8 weeks post-partum, with only some calves subsequently mounting a detectable adaptive antibody response.ConclusionsThese findings indicate transplacental transmission of T. orientalis appears to play only a minor role in persistence of T. orientalis infection in the field; however calves are highly susceptible to developing high level T. orientalis infections at 4–8 weeks of age regardless of whether maternal antibodies are present post-partum.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-017-2166-9) contains supplementary material, which is available to authorized users.

The identification of Theileria bicornis in captive rhinoceros in Australia

“…Whether endemic Australian tick species are competent vectors of T. bicornis and other rhinoceros blood parasites is unclear, but they may lack the necessary mouthparts to achieve transmission. Transplacental transmission has been demonstrated for several piroplasmid species ( Phipps and Otter, 2004 , Fukumoto et al, 2005 , Mierzejewska et al, 2014 , Zakian et al, 2014 , Sudan et al, 2015 , Swilks et al, 2017 ) but tends to occur only at low frequencies and there was no evidence from this study that T. bicornis was transmitted via this route within the captive population.…”

Oriental Theileriosis

“…This mode of transmission has been demonstrated in species such as T. annulata [119] T. equi [120,121], and T. lestoquardi [122]. Transplacental transmission also occurs in T. orientalis infection [71,123,124]. Early studies [123] used blood film examination to demonstrate that transplacental transmission occurs in calves but at a low rate of 5% (5/100 calves that are 1-2 days old).…”

“…In contrast, another recent study in New Zealand [125] did not detect transplacental transmission despite using sensitive molecular techniques. Recently, an Australian study [124] used molecular methods to confirm transplacental transmission of T. orientalis in field-affected cattle, but at low rate of approximately 2% (2/98 calves) similar to the study of [123]. In that study, abortion did not appear to correlate with transplacental transmission of T. orientalis, instead the authors posited that, abortion may occur due to hypoxia in the foetal calves due to maternal anaemia, placental insufficiency, or other factors related to maternal pathology [123].…”

“…Some cases occurring in regions where adult cattle had previously been exposed T. orientalis reported calves at 6 to 14 weeks of age to have high mortality and severe morbidity [150,151] which coincides with high parasitaemias which are consistently observed in calves from Theileria-endemic areas [124]. While MPSP antibodies are sometimes detectable in the colostrum of dams and appear to be transferred to calves [101], any passive immunity appears to be short lived, with antibodies undetectable in calves by 4 weeks of age [124]. Lack of protection from maternal antibodies likely explains the high infection intensities and clinical disease observed in calves.…”

A U.S. Isolate of Theileria Orientalis, Ikeda Genotype, is Transmitted to Cattle by the Invasive Asian Longhorned Tick, Haemaphysalis Longicornis

“…Severely affected animals often exhibit pyrexia, weakness, pallor, and increased heart and respiratory rates [7,8]. Abortion is a common sequela to T. orientalis Ikeda infection, although transplacental transmission of the parasite from cows to calves is only observed in 10% of cases [9,10].…”