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. 51,472 argasid ticks were collected from 16 of 24 caves surveyed. 2,774 O. tholozani were analyzed 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 rate 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. Importance Borrelia 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, Orhinthodoros 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 its 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.

Infection and seroprevalence of Borrelia persica in domestic cats and dogs in Israel

“…In the present study from Israel, infection in cats and dogs was prevalent in both sexes, all ages, different animal breeds, urban and rural settings, Mediterranean and semi-arid climates and all five geographic areas of residence included in the study. The geographic distribution of infection is in agreement with that reported in other studies on B. persica infection in ticks, wildlife and humans in Israel, which describe infection in almost all areas of the country, except for the very southern part close to the Red Sea [ 2 , 12 , 25 , 26 ]. Urban and rural settings in Israel often provide suitable conditions for the survival O. tholozani , the argasid tick vector of B. persica ; these include shady areas characterized by high humidity and mild temperature [ 4 ].…”

“…Borrelia persica infection accompanied by high spirochetemia levels and clinical disease was reported in domestic dogs and cats in Israel in 2016 [ 10 ]. Additional studies conducted in Israel using PCR detected B. persica infection in golden jackals ( Canis aureus ), red foxes ( Vulpes vulpes ), Indian crested porcupines ( Hystrix indica ), rock hyraxes ( Procavia capensis ), Cairo spiny mice ( Acomys cahirinus ) and other wildlife mammals [ 11 , 12 ]. Wildlife canids were recognized as the main reservoirs for tick infection based on blood meal analysis [ 12 ].…”

“…Additional studies conducted in Israel using PCR detected B. persica infection in golden jackals ( Canis aureus ), red foxes ( Vulpes vulpes ), Indian crested porcupines ( Hystrix indica ), rock hyraxes ( Procavia capensis ), Cairo spiny mice ( Acomys cahirinus ) and other wildlife mammals [ 11 , 12 ]. Wildlife canids were recognized as the main reservoirs for tick infection based on blood meal analysis [ 12 ]. Other relapsing fever Borrelia spp., such as Borrelia turicatae and Borrelia hermsii , have been reported to cause disease in dogs in North America [ 13 – 15 ], and Borrelia hispanica was associated with disease in a dog in Europe [ 16 ].…”

Comparative Analysis of Tick-Borne Relapsing Fever Spirochaetes from Ethiopia and Nigeria

“…The overall Borrelia prevalence of 1.3% in O. savignyi ticks from this study is lower than the 6.1% reported in pooled ticks from Nigeria [ 25 ] but comparable to 2.6% reported in soft ticks from Israel [ 59 ]. It is difficult to determine the precise level of infectivity from the earlier study among the pooled ticks.…”

“…Interestingly, the B. theileri from Israel KP191622 did not align next to any of the B. theileri flagellin sequences on the phylogenetic tree ( Figure 8 ); instead, it aligned next to B. lonestari from the US and formed a sister clade next to B. persica reported in O. tholozani ticks and humans in Israel [ 59 ]. Whether this report represents an initial misidentification remains to be ascertained.…”