Concurrent severe fever with thrombocytopenia syndrome virus outbreaks on multiple fox farms, China, 2023

Abstract

The role of farmed animals in the viral spillover from wild animals to humans is of growing importance. Between July and September of 2023 infectious disease outbreaks were reported on six Arctic fox (Vulpes lagopus) farms in Shandong and Liaoning provinces, China, which lasted for 2-3 months and resulted in tens to hundreds of fatalities per farm. Severe Fever with Thrombocytopenia Syndrome Virus (SFTSV) was identified in tissue/organ and swab samples from all the 13 foxes collected from these farms. These animals exhibited loss of appetite and weight loss, finally resulting in death. In autopsy and histopathology, prominently enlarged spleens and extensive multi-organ hemorrhage were observed, respectively, indicating severe systemic effects. Viral loads were detected in various tissues/organs, including brains from 9 of the 10 foxes. SFTSV was also detected in serum, anal swabs, as well as in environmental samples, including residual food in troughs used by dying foxes in follow-up studies at two farms. The 13 newly sequenced SFTSV genomes shared >99.43% nucleotide identity with human strains from China. Phylogenetic analyses showed that the 13 sequences belonged to three genotypes, and that two sequences from Liaoning were genomic reassortants, indicative of multiple sources and introduction events. This study provides the first evidence of SFTSV infection, multi-tissue tropism, and pathogenicity in farmed foxes, representing an expanded virus host range. However, the widespread circulation of different genotypes of SFTSV in farmed animals from different provinces and the diverse transmission routes, highlight its increasing and noticeable public health risk in China.

Keywords: Arctic fox; Severe fever with thrombocytopenia syndrome viruses; disease outbreak; fur farms; phylogenetic analysis.

Figure 1.

Gross and hispathological lesions in SFTSV-infected foxes and uninfected control foxes. (A) Compared to control foxes, the spleen in SFTSV-infected fox is visibly enlarged. (B–H) Pathological changes in spleen, heart, liver, trachea, lung, kidney, and bladder from SFTSV-infected foxes are labelled with arrows: (B) red blood cells infiltrate the white pulp of the spleen, with fewer lymphocytes surrounded by hemosiderin deposits; (C) the heart shows reduced cardiomyocyte nuclei size, thinner myocardial fibres, and minor fibre breakage; (D) liver central veins are dilated and congested with hemosiderin deposition; (E) the trachea exhibits epithelial detachment and submucosal capillary congestion; (F) lungs display widened alveolar septa and fluid-filled alveolar spaces; (G) enlarged kidney glomeruli with tubular degeneration; (H) severe sloughing of the bladder mucosal epithelium. Panels B–H, original magnification ×40.

Figure 2.

Phylogenetic analysis of 13 SFTSV genomes from the farm outbreaks and representative sequences available from GenBank. Branch colours in the L, M, and S gene segment phylogenetic trees represent SFTSV clade: denoted C1–C6 (equivalent to genotypes A∼F in another classification scheme). The red, blue, brown, light brown, light blue, and grey triangles denote the 13 SFTSV strains identified from six farms in this study. The trees are mid-point rooted and the scale bars represent the number of nucleotide substitutions per site.