Transmission of Candidatus Anaplasma camelii to laboratory animals by camel-specific keds, Hippobosca camelina

Abstract

Anaplasmosis, caused by infection with bacteria of the genus Anaplasma is an important veterinary and zoonotic disease. The characterization of transmission has concentrated on ticks and 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 Candidatus Anaplasma camelii occurring 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 whether Anaplasma positive camel keds could transmit Ca. Anaplasma camelii to small laboratory animals via blood-feeding. We show competence in pathogen transmission and subsequent infection in mice and rabbits by both direct detection in blood smears and subsequent molecular identification 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 basis for establishing ked control programmes for improvement of livestock and human health. Author summaryHematophagous flies such as Tabanids and Stomoxys, among 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 frequently detected in both camels and their keds. We confirmed by experimental blood-feeding, gene amplification, and amplicon sequencing that camel keds can transmit "Candidatus Anaplasma camelii" from naturally-infected camels to healthy mice and rabbits. The high prevalence of camel anaplasmosis throughout the year in northern Kenya could be explained by the infestation camel-specific H. camelina, whose capacity as efficient fliers, unlike ticks, promotes disease transmission and maintenance within and among camel herds. Although this study focused on the transmission of Anaplasma sp. by camel keds, it is possible that other hemopathogens could also be transmitted by these flies through a similar mechanism. Notably, in the absence of their preferred hosts, keds occasionally bite humans and other vertebrates they come across in order to acquire bloodmeals, and in the process could transmit zoonotic pathogens.