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

Kelcey D Dinkel,Kevin K Lahmers,Susan M Noh,David R Herndon,Massaro W Ueti,S Michelle Todd,Kathleen L Mason,Lindsay M Fry,Glen A Scoles

doi:10.1186/s13071-021-04659-9

Abstract

BackgroundTheileria 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.MethodsNymphal 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.ResultsAfter 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%.ConclusionsOur 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.Graphical

Highlights

Theileria orientalis is a tick-borne hemoparasite that causes anemia, ill thrift, and death in cattle globally
Sequence anzalysis Consensus sequences for all sequenced amplicons were identical to each other and to that of the Ikeda strain, similar to the analysis by Oakes [23]. These findings confirm that the U.S population of H. longicornis is a competent vector of T. orientalis Ikeda detected in beef cattle in VA, U.S in 2017 [23]. This is the first report of T. orientalis transmission by H. longicornis ticks in the U.S Our findings support the hypothesis that transmission of T. orientalis Ikeda within the Abermarle County, VA area is due to the abundance of H. longicornis
Since the T. orientalis Ikeda outbreak was detected 2017, concomitant with the introduction of H. longicornis to the U.S, it is possible that the tick and the parasite were imported together (e.g. T. orientalis Ikedainfected H. longicornis ticks were imported); it is possible that they were introduced separately (e.g. T. orientalis-infected cattle and uninfected H. longicornis ticks entered separately), and an outbreak occurred when the parasite and the tick arrived in the same area of VA at the same time

Summary

Introduction

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. 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. The Ikeda genotype results in severe infection in 1–6% of infected animals [5, 6], while infection with the Buffeli genotype is almost always clinically silent [3, 5]. Abortion is a common sequela to T. orientalis Ikeda infection, transplacental transmission of the parasite from cows to calves is only observed in 10% of cases [9, 10]

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