Bourbon Virus in Field-collected Ticks, Missouri, USA

Harry M. Savage; Kristen L. Burkhalter; Marvin S. Godsey, Jr.; Nicholas A. Panella; David C. Ashley; William L. Nicholson; Amy J. Lambert

Disclosures

Emerging Infectious Diseases. 2017;23(12):2017-2022. 

In This Article

Discussion

We isolated BRBV from 3 pools of A. americanum ticks collected in northwestern Missouri: 1 pool of male adults and 2 pools of nymphs. The first detection of BRBV was from a fatal case in a man from nearby Bourbon County, Kansas;[1] this man reported tick exposure and an engorged tick on his shoulder shortly before he became ill. Tick exposure combined with laboratory findings of leukopenia and thrombocytopenia suggested that BRBV might be transmitted to humans by ticks. Detection of BRBV in field-collected A. americanum ticks from Missouri supports the premise that A. americanum, a species that is aggressive, feeds on humans,[8] and is abundant in Kansas and Oklahoma,[9] the states where the 2 persons with BRBV infection resided, is a vector of BRBV to humans.

Tick transmission of BRBV also is consistent with our knowledge of the vector status and phylogenetic relationships within the genus Thogotovirus and related viruses in the family Orthomyxoviridae (Figure 2). Viruses that have been placed in the genus Thogotovirus include BRBV,[1] Thogoto virus,[10,11] Araguari virus,[10,12] Dhori virus,[10,11] Jos virus,[10,13] and Upolu virus.[13,14] To our knowledge, the closely related Aransas Bay virus[14] has not been placed in genus Thogotovirus. All of these viruses, except Araguari virus, which has been isolated only from vertebrates, are believed to be transmitted by a variety of hard and soft tick species.[15–22] Of these tick-transmitted viruses (Figure 2), only Thogoto virus, Dhori virus, and BRBV have been associated with human disease,[1,18] and only BRBV and Aransas Bay virus are known to occur in North America. Aransas Bay virus has been isolated from the soft tick Ornithodoros capensis, a parasite of seabirds.[19,23]

Dhori virus, the virus most closely related to BRBV,[4] is an Old World virus known from Europe, North Africa, and western and central Asia. Dhori virus has been isolated primarily from metastriate ticks (hard ticks other than genus Ixodes), including Hyalomma dromedarii, H. marginatum (reported as H. plumbeum plumbeum in the former Soviet Union), H. scupense, and Dermacentor marginatus.[16,18,20,24] On rare occasions, Dhori virus also has been isolated from mosquitoes, including Anopheles hyrcanus,[24] and from 1 mixed pool of Aedes caspius caspius and Culex hortensis mosquitoes collected near the Naryn River in Kyrgyzstan.[20] Human disease associated with Dhori virus infection is characterized by acute illness with severe fever, headache, general weakness, and retrobulbar pain; encephalitis occurs in ≈40% of patients, and convalescence is long (2 months).[18] In addition, 5 laboratory infections resulting from aerosol exposure, 2 of which were characterized by encephalitis, have been reported.[25]

Infection prevalence for BRBV in field-collected A. americanum ticks varied. The infection prevalence for nymphs, the stage with the largest sample size, was 0.31/1,000 or 1/3,226 nymphs at site 27. Nymphs collected at other sites were virus negative, resulting in a very low infection prevalence of 0.07/1,000 when all nymphal collections were combined for the 2013 season. For comparison, HRTV was detected in nymphs collected at 4 of the 6 sampled sites, and the infection prevalence for HRTV in nymphs from all sites during the 2013 season was 1.79/1,000, or 1 infected nymph of 559 nymphs tested.[5]

The BRBV infection prevalence for adult male A. americanun ticks from site 2a on June 12, 2013, was very high (19.11/1,000), whereas the infection prevalence for adult male A. americanum ticks from site 2a during the entire 2013 season was 7.35/1,000, or 1 infected male adult among every 136 tested. However, the infection prevalence for all adult male A. americanum ticks from all sites combined during the 2013 season was 0.32/1,000, or 1 of 3,125 adult male ticks tested. Infection prevalence for adult male ticks appears higher than for nymphs; however, BRBV infection prevalence for male adults and nymphs from all sites combined during the 2013 season did not differ significantly.

Infection prevalence for BRBV in potential vectors remains poorly known; our interpretations are preliminary and await additional field studies. However, the very low infection prevalence for nymphs and varying rates for male adults suggest the possibility that other transmission cycles for BRBV might exist and that A. americanum ticks, although most likely an important vector to humans because of their aggressive host-seeking behavior and preference for medium and large mammals, might not be an important enzootic vector of BRBV. We hypothesize that A. americanum ticks acquire BRBV from occasional blood meals from >1 vertebrate hosts; that the virus successfully replicates and is transstadially transmitted in A. americanum ticks; and that A. americanum ticks transmit the virus to incidental hosts, such as humans. The pool of male adult A. americanum ticks, MO-2013-1246, also was positive for HRTV,[5] suggesting some overlap in the transmission cycles of HRTV and BRBV. BRBV and antibodies to BRBV have not been detected in vertebrates, other than the 2 humans, and the natural history of the virus remains unknown.

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