Ecology of the Tick-Borne Phlebovirus Causing Severe Fever with Thrombocytopenia Syndrome in an Endemic Area of China

Abstract

Background: Severe fever with thrombocytopenia syndrome (SFTS) is caused by SFTS virus (SFTSV), a tick-borne phlebovirus in family Bunyaviridae. Studies have found that humans, domestic and wildlife animals can be infected by SFTSV. However, the viral ecology, circulation, and transmission remain largely unknown.

Methodology/principal findings: Sixty seven human SFTS cases were reported and confirmed by virus isolation or immunofluorescence assay between 2011 and 2014. In 2013-2014 we collected 9,984 ticks from either vegetation or small wild mammals in the endemic area in Jiangsu, China, and detected SFTSV-RNA by real-time RT-PCR in both questing and feeding Haemaphysalis longicornis and H. flava. Viral RNA was identified in larvae of H. longicornis prior to a first blood meal, which has never been confirmed previously in nature. SFTSV-RNA and antibodies were also detected by RT-PCR and ELISA, respectively, in wild mammals including Erinaceus europaeus and Sorex araneus. A live SFTSV was isolated from Erinaceus europaeus captured during the off tick-feeding season and with a high SFTSV antibody titer. Furthermore, SFTSV antibodies were detected in the migratory birds Anser cygnoides and Streptopelia chinensis using ELISA.

Conclusions/significance: The detection of SFTSV-RNA in non-engorged larvae indicated that vertical transmission of SFTSV in H. longicornis might occur in nature, which suggests that H. longicornis is a putative reservoir host of SFTSV. Small wild mammals such as Erinaceus europaeus and Sorex araneus could be infected by SFTSV and may serve as natural amplifying hosts. Our data unveiled that wild birds could be infected with SFTSV or carry SFTSV-infected ticks and thus might contribute to the long-distance spread of SFTSV via migratory flyways. These findings provide novel insights for understanding SFTSV ecology, reservoir hosts, and transmission in nature and will help develop new measures in preventing its rapid spread both regionally and globally.

Fig 1. Distribution of Sampling Sites for Ticks and Wild Animals in Jiangsu, an SFTS Endemic Area.

A, Map of P. R. China; B, Map of Jiangsu Province. Sampling sites were where SFTS cases were reported.

Fig 2. Phylogenetic analysis of SFTSV strains isolated from Jiangsu Province during 2011 and 2014, compared with SFTSV strains from other areas.

The phylogenetic tree was constructed by using the Neighbor-Joining method with the MEGA5.1 software. The reliability values indicated at the branch nodes were determined using 1,000 bootstrap replications. Isolated SFTSV strains from places located in the north of the Yangtze River were labeled by black solid circles; Isolated SFTSV strains from places located in the south of the Yangtze river were labeled by black solid squares; Isolated SFTSV strains distributed in Japanese clades were labeled by black solid triangles. Phylogenetic relationship of SFTSV with other bunyaviruses, based on the complete L segment sequences, is shown in the figure.