Transmission of the Human Relapsing Fever Spirochete Borrelia persica by the Argasid Tick Ornithodoros tholozani Involves Blood Meals from Wildlife Animal Reservoirs and Mainly Transstadial Transfer

Abstract

Borrelia persica, transmitted by the argasid tick Ornithodoros tholozani, causes human tick-borne relapsing fever in the Middle East and Central Asia. Infection is acquired often when visiting tick-infested caves and reported to be transmitted mainly transovarially between ticks, occasionally infecting humans. To study the epidemiology of this infection, ticks were trapped in 24 caves in 12 geographic zones covering all of Israel and identified morphologically. DNA was extracted from larvae, nymphs, and adult stages from each location and PCR followed by DNA sequencing was performed to identify Borrelia infection, tick species, and tick blood meal sources. We collected 51,472 argasid ticks from 16 of 24 caves surveyed. We analyzed 2,774 O. tholozani ticks, and 72 (2.6%) from nine caves were PCR positive for B. persica Infection rates in male, female, and nymphal ticks (4.4%, 3%, and 3.2%, respectively) were higher than in larva (P < 0.001), with only 3 (0.04%) positive larvae. Presence of blood meal was associated with B. persica infection in ticks (P = 0.003), and blood meals of golden jackals, red foxes, and Cairo spiny mouse were associated with infection (P ≤ 0.043). PCR survey of 402 wild mammals revealed B. persica infection with the highest rates in social voles (22%), red foxes (16%), golden jackals (8%), and Cairo spiny mice (3%). In conclusion, although transovarial tick transmission of B. persica occurs at low levels, ticks apparently acquire infection mainly from wildlife canid and rodents and may eventually transmit relapsing fever borreliosis to humans who enter their habitat.IMPORTANCEBorrelia persica is a spirochete that causes tick-borne relapsing fever in humans in an area that spans from India to the Mediterranean. Until now, it was thought that the soft tick vector of this infection, Ornithodoros tholozani, is also its main reservoir and it transmits B. persica mostly transovarially between tick generations. This study showed that tick infection with B. persica is associated with feeding blood from wild jackals, foxes, and rodents and that transovarial transmission is minimal. Since O. tholozani ticks are found in isolated caves and ruins, it is assumed that wild canids who migrate over long distances have a major role in the transmission of B. persica between remote tick populations, and it is then maintained locally also by rodents and eventually transferred to humans during tick bites. Prevention of human infection could be achieved by restricting entrance of canines and humans to habitats with O. tholozani populations.

Keywords: Argasidae; Borrelia persica; Ornithodoros tholozani; blood meal; relapsing fever.

FIG 1

Map showing the tick collection sites represented with circles, where red circles symbolize sites where B. persica-infected ticks were found and circle size represents the number of ticks collected in each site. Numbers in the map represent the cave identity number.

FIG 2

Maximum-likelihood phylogram comparing 270- to 273-bp DNA sequences of the flaB gene from B. persica detected in O. tholozani ticks included in the study to sequences corresponding to other B. persica GenBank accession numbers and from other Borrelia spp.; B. burgdorferi (GenBank accession no. X75200.1) was used as outgroup. The Tamura 3-parameter model was chosen with a pairwise deletion procedure. Numbers at nodes correspond to a percentage confidence level higher than 70% in a bootstrap test performed on 1,000 replicates. New sequences derived from this study are marked with black diamond squares and deposited in GenBank. The scale bar corresponds to a distance of 0.05 nucleotide substitution per site.

FIG 3

Locations where insectivores and wild canids were sampled, indicating the presence or absence of infection with B. persica. Locations where B. persica was detected are noted in red, and their names are included. Twelve collections sites corresponding to 12 wild canid samples were unknown, including an area where a positive sample was collected.