Journal Article

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

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

2021

Overview

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. Graphical Abstract

• Publisher: BioMed Central,BioMed Central Ltd,Springer Nature B.V,BMC
• Subject: adults / Anaemia / Anemia / Animals / Asia / Asian longhorned tick / Biomedical and Life Sciences / Biomedicine / blood / Calves / Cattle / Cattle Diseases - parasitology / Cattle Diseases - transmission / cattle industry / Causes of / cell biology / Cohorts / Cytology / death / Disease Outbreaks - veterinary / Disease transmission / Diseases / Distribution / DNA / Economic impact / Economics / Ectoparasites / Entomology / Epidemics / Feeds / Genotype / Genotype & phenotype / Genotypes / Glands / Haemaphysalis longicornis / hemoparasites / herds / Ikeda genotype / Impact analysis / Infections / Infectious Diseases / Invasive species / Male / Molting / monitoring / Moulting / Nucleotide sequence / Nymphs / Parasitemia / Parasitemia - epidemiology / Parasites / Parasites of veterinary importance / Parasitology / PCR / Risk factors / Salivary gland / Salivary glands / Theileria / Theileria - genetics / Theileria - isolation & purification / Theileria orientalis / Theileriasis - parasitology / Theileriasis - transmission / Tick-borne diseases / Ticks / Ticks - parasitology / Transmission / Tropical Medicine / United States - epidemiology / Vectors / Veterinary Medicine/Veterinary Science / Virginia / Virology / virulence