A U.S. isolate of Theileria orientalis, Ikeda genotype, is transmitted to cattle by the invasive Asian longhorned tick, Haemaphysalis longicornis

Abstract

Background Theileria orientalis is a tick-borne hemoparasite that causes anemia, ill thrift, and death in cattle globally. The Ikeda strain of T.orientalis is more virulent than other strains, leading to severe clinical signs and death of up to 5% of affected animals. Within the Asia–Pacific region, where it affects 25% of Australian cattle, T.orientalis Ikeda has a significant economic impact on the cattle industry. In 2017, T.orientalis Ikeda was detected in a cattle herd in Albermarle County, Virginia, United States. Months earlier, the U.S. was alerted to the invasion of the Asian longhorned tick, Haemaphysalis longicornis, throughout the eastern U.S. Abundant H.longicornis ticks were identified on cattle in the T.orientalis-affected herd in VA, and a subset of ticks from the environment were PCR-positive for T.orientalis Ikeda. A strain of T.orientalis from a previous U.S. outbreak was not transmissible by H.longicornis; however, H.longicornis is the primary tick vector of T.orientalis Ikeda in other regions of the world. Thus, the objective of this study was to determine whether invasive H.longicornis ticks in the U.S. are competent vectors of T.orientalis Ikeda. Methods Nymphal H.longicornis ticks were fed on a splenectomized calf infected with the VA-U.S.-T.orientalis Ikeda strain. After molting, a subset of adult ticks from this cohort were dissected, and salivary glands assayed for T.orientalis Ikeda via qPCR. The remaining adult ticks from the group were allowed to feed on three calves. Calves were subsequently monitored for T.orientalis Ikeda infection via blood smear cytology and PCR. Results After acquisition feeding on a VA-U.S.-T.orientalis Ikeda-infected calf as nymphs, a subset of molted adult tick salivary glands tested positive by qPCR for T.orientalis Ikeda. Adult ticks from the same cohort successfully transmitted T.orientalis Ikeda to 3/3 naïve calves, each of which developed parasitemia reaching 0.4–0.9%. Conclusions Our findings demonstrate that U.S. H.longicornis ticks are competent vectors of the VA-U.S.-T.orientalis Ikeda strain. This data provides important information for the U.S. cattle industry regarding the potential spread of this parasite and the necessity of enhanced surveillance and control measures.

Coinfection of cattle in Virginia with Theileria orientalis Ikeda genotype and Anaplasma marginale

“…The LOD of A. marginale was a 10 -5 dilution of reference DNA, extracted from a clinically positive sample according to our in-house PCR. Although a standard curve was not run alongside this PCR assay, extrapolating from a similar assay run in our laboratory (supplementary data 8 ) suggests that 1 × 10 9 pmol of Chitose gBlock is ~16 gene copies; 10 8 pmol of Ikeda gBlock is ~25 gene copies.…”

“…16 T. orientalis Ikeda has recently been identified in cattle in Virginia, affecting animals that were also parasitized with H. longicornis ticks 12 ; this tick has been confirmed as a competent vector in Virginia for T. orientalis Ikeda. 8 The animals that were clinically affected in this outbreak had the typical signs of anemia, icterus, and general malaise. In Virginia, this clinical presentation is identical to the blood infection caused by the bacterium Anaplasma marginale.…”

Approaches to Integrated Parasite Management (IPM) for Theileria orientalis with an Emphasis on Immunity

“…The full spectrum of biological vectors (or definitive) hosts for T. orientalis has not been resolved. Amongst arthropods, the 3-host ixodid tick Haemaphysalis longicornis (Neumann, 1901) [ 38 ] has been confirmed in transmission trials as one biological vector for T. orientalis in early studies [ 8 ] in Australia [ 26 , 39 ] and the USA [ 19 ]. H. longicornis has a predicted, widespread distribution in countries with temperate climates [ 40 ], including Australia, New Zealand, Fiji, New Caledonia, China, former USSR, Korea and Japan [ 41 , 42 ], the USA, and several other Pacific Islands, including Hawaii [ 43 ].…”

“…Of these genotypes, 1 and 2 cause the majority of clinical disease in cattle in Australia [ 13 , 14 ], and elsewhere [ 5 ]. These pathogenic genotypes are recognised in many countries including Australia [ 15 ], New Zealand [ 16 ], Japan [ 17 ], Korea [ 18 ], and USA [ 19 ]. The disease has been estimated to cost the livestock industries in Japan and Korea around USD $100 million annually [ 17 , 18 ].…”

Rapid Discovery and Detection of Haemaphysalis longicornis through the Use of Passive Surveillance and Collaboration: Building a State Tick-Surveillance Network

“…and Hepatozoon canis), and human pathogens (e.g., Borrelia, Ehrlichia, Rickettsia, and several viruses) [6]. Recently, investigators in Virginia determined field-collected H. longicornis were infected with the Theileria orientalis Ikeda genotype and demonstrated that study ticks were competent experimental vectors for the Ikeda strain of the pathogen in local cattle [7][8][9][10].…”