The role of ticks in the maintenance and transmission of Crimean-Congo hemorrhagic fever virus: A review of published field and laboratory studies

Abstract

This manuscript is part of a series of reviews that aim to cover published research on Crimean-Congo hemorrhagic fever (CCHF) and its etiological agent, CCHF virus (CCHFV). The virus is maintained and transmitted in a vertical and horizontal transmission cycle involving a variety of wild and domestic vertebrate species that act as amplification hosts, without showing signs of illness. These vertebrates have traditionally been considered reservoirs of CCHFV, but in fact they develop only a transient viremia, while the virus can persist in ticks for their entire lifespan, and can also be transmitted vertically to the next generation. As a result, ticks are now considered to be both the vector and the reservoir for the virus. CCHFV has been detected in a wide range of tick species, but only a few have been proven to be vectors and reservoirs, mainly because most published studies have been performed under a broad variety of conditions, precluding definitive characterization. This article reviews the published literature, summarizes current knowledge of the role of ticks in CCHFV maintenance and transmission and provides guidance for how to fill the knowledge gaps. Special focus is given to existing data on tick species in which vertical passage has been demonstrated under natural or experimental conditions. At the same time, we identify earlier reports that used unreliable methods and perceptions to ascribe a vector role to some species of ticks, and have contributed to confusion regarding viral transmission. We also examine epidemiological pathways of CCHFV circulation and discuss priority areas for future research.

Fig. 1

A schematic overview of the life cycle of ixodid ticks, with special focus on the implications for CCHFV circulation (Bente et al., 2013). The course of the tick life cycle is indicated by blue arrows, and specifically refers to species of the genus Hyalomma with two-host behavior, in which larvae and nymphs feed on the same host. Larvae hatch from eggs and, after feeding, molt to the nymph stage while remaining attached to the host. The nymphs feed again on the same host and return to the ground for molting. At this point (asterisk) nymphs may indirectly infect (via virus in saliva) simultaneously co-feeding larvae and nymphs. The resulting adults find a host, feed again and mate on the host, drop off, and the females lay thousands of eggs, which are left in decaying vegetation at protected sites with high relative humidity to ensure survival. At each bloodmeal, ticks can become integrated into the epidemiological chain of CCHFV transmission by means of transstadial (stage-to-stage) or transovarial (female-to-egg, also called vertical) transmission. Solid red arrows mark the possible transmission of CCHFV between ticks and mammals, or transmission between co-feeding ticks. For each form of virus transfer, the thickness of the red arrow indicates the efficiency from one stage of the tick to the next or to the eggs. Humans acquire infection through the bite of an infected tick or through exposure to body fluids of a viremic animal or a CCHF patient. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 2

Distribution of competent tick vectors of CCHFV in the Palearctic region, in which virus has either been detected in questing specimens and/or its transmission has been demonstrated by feeding previously infected ticks on naïve hosts. These species include: Dermacentor marginatus, Hyalomma marginatum, H. dromedarii, and H. impeltatum and Rhipicephalus rossicus. Note that within the reported distribution of H. marginatum is also that of H. turanicum; the map should be regarded as the combination of known distributions of both species. Data is presented in this form as these species are frequently reported without a clear delineation of their identity, and have been historically considered closely related, both previously regarded as subspecies of H. marginatum.

Fig. 3

Distribution of competent tick vectors of CCHFV in the pan-African region, in which virus has either been detected in questing specimens and/or its transmission has been demonstrated by feeding previously infected ticks on naïve hosts. These species include: Amblyomma variegatum, Hyalomma rufipes, H. truncatum, and Rhipicephalus e. evertsi.

Fig. 4

Distribution of competent tick vectors of CCHFV in southern and eastern Africa, in which virus has either been detected in questing specimens and/or its transmission has been demonstrated by feeding previously infected ticks on naïve hosts. These species include: Amblyomma hebraeum, Hyalomma spp., Rhipicephalus pulchellus, R. appendiculatus and R. evertsi mimeticus.