Transmission of 'Candidatus Anaplasma camelii' to mice and rabbits by camel-specific keds, Hippobosca camelina

Author summary Hematophagous flies such as Tabanids and Stomoxys, and other biting flies, are mechanical transmitters of various pathogens such as African trypanosomes and Anaplasma species. However, little is known about the role of common camel-specific biting keds (also known as camel flies or louse flies, genus Hippobosca) in pathogen transmission. Keds inflict painful bites to access host blood, and in the process may transmit bacterial hemopathogens. We demonstrated using amplicon sequencing that camel keds can transmit 'Candidatus Anaplasma camelii' from naturally-infected camels to healthy mice and rabbits via blood feeding. The high prevalence of camel anaplasmosis throughout the year in northern Kenya could be attributed to keds, which infest camels all year round. Unlike ticks, keds can fly from one host to another and thus promote disease transmission among and between camel herds. Although our study focused on the transmission of Anaplasma sp. by camel keds, these flies could possibly also transmit other hemopathogens through a similar mechanism. Notably, in the absence of their preferred hosts, keds occasionally bite humans and other vertebrates they come across in search of bloodmeals, and in the process could transmit zoonotic pathogens. Anaplasmosis, caused by infection with bacteria of the genus Anaplasma, is an important veterinary and zoonotic disease. Transmission by ticks has been characterized but little is known about non-tick vectors of livestock anaplasmosis. This study investigated the presence of Anaplasma spp. in camels in northern Kenya and whether the hematophagous camel ked, Hippobosca camelina, acts as a vector. Camels (n = 976) and > 10,000 keds were sampled over a three-year study period and the presence of Anaplasma species was determined by PCR-based assays targeting the Anaplasmataceae 16S rRNA gene. Camels were infected by a single species of Anaplasma, 'Candidatus Anaplasma camelii', with infection rates ranging from 63-78% during the dry (September 2017), wet (June-July 2018), and late wet seasons (July-August 2019). 10-29% of camel keds harbored 'Ca. Anaplasma camelii' acquired from infected camels during blood feeding. We determined that Anaplasma-positive camel keds could transmit 'Ca. Anaplasma camelii' to mice and rabbits via blood-feeding. We show competence in pathogen transmission and subsequent infection in mice and rabbits by microscopic observation in blood smears and by PCR. Transmission of 'Ca. Anaplasma camelii' to mice (8-47%) and rabbits (25%) occurred readily after ked bites. Hence, we demonstrate, for the first time, the potential of H. camelina as a vector of anaplasmosis. This key finding provides the rationale for establishing ked control programmes for improvement of livestock and human health.

Automated summary

This study demonstrates that camel keds can transmit 'Candidatus Anaplasma camelii' from infected camels to mice and rabbits through blood-feeding, serving as a potential vector of anaplasmosis. The high prevalence of 'Ca. Anaplasma camelii' in camels in northern Kenya suggest that keds play a significant role in pathogen transmission. Establishment of ked control programs may help improve livestock and human health in the region.