Vectors, Hosts, and the Possible Risk Factors Associated with Severe Fever with Thrombocytopenia Syndrome

Wang, Jin-Na; Li, Tian-Qi; Liu, Qin-Mei; Wu, Yu-Yan; Luo, Ming-Yu; Gong, Zhen-Yu

doi:https://doi.org/10.1155/2021/8518189

Canadian Journal of Infectious Diseases and Medical Microbiology

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Abstract Introduction Conclusions Data Availability Conflicts of Interest Authors’ Contributions Acknowledgments References Copyright Related Articles

Review Article | Open Access

Volume 2021 | Article ID 8518189 | https://doi.org/10.1155/2021/8518189

Vectors, Hosts, and the Possible Risk Factors Associated with Severe Fever with Thrombocytopenia Syndrome

Jin-Na Wang,¹Tian-Qi Li,¹Qin-Mei Liu,¹Yu-Yan Wu,¹Ming-Yu Luo,¹and Zhen-Yu Gong¹

Academic Editor: Marco Di Luca

Received10 Aug 2021

Revised26 Sept 2021

Accepted20 Oct 2021

Published03 Nov 2021

Abstract

Severe fever with thrombocytopenia syndrome (SFTS) is a disease caused by infection with the SFTS virus (SFTSV). SFTS has become a crucial public health concern because of the heavy burden, lack of vaccines, effective therapies, and high-fatality rate. Evidence suggests that SFTSV circulates between ticks and animals in nature and is transmitted to humans by tick bites. In particular, ticks have been implicated as vectors of SFTSV, where domestic or wild animals may play as the amplifying hosts. Many studies have identified antigens and antibodies against SFTSV in various animals such as sheep, goats, cattle, and rodents. Besides, person-to-person transmission through contact with blood or mucous of an infected person has also been reported. In this study, we reviewed the literature and summarized the vectors and hosts associated with SFTS and the possible risk factors.

1. Introduction

Severe fever with thrombocytopenia syndrome (SFTS) is an emerging infectious disease, caused by SFTS virus (SFTSV), a novel Phlebovirus in the Bunyaviridae family, which was first identified in China [1]. Since the first report in 2009, SFTS has attracted great public health attention in Asia, especially from China, Japan, and South Korea [2–4]. Besides, recently, a related study has also been reported in Vietnam [5]. The clinical manifestations of SFTS include fever, thrombocytopenia, gastrointestinal symptoms, hemorrhagic tendency, and multiple organ dysfunctions, with 5–14 days of incubation and a high initial case fatality rate of 30% [1, 6]. In total, 96.5% of the SFTS cases occurred from April to October, and in China, 93.3% of the cases were reported in middle-aged and elderly people with a spatially expanding trend [7]. Among them, farmers were the main high-risk population, and there were more cases in female than males [7]. Although the natural transmission mode of SFTSV among humans, hosts, and vectors remains unclear, increasing evidence has showed that ticks may be the transmission vector, while the domestic or wild animals may play as the amplifying hosts.

2. Main Text

Vectors, hosts, and the possible risk factors associated with SFTS.

2.1. Ticks

The infection rate of the ticks is varied in different species, developmental stages, genders, regions, or even the collected hosts. Studies showed the pooled infection rate of SFTSV in ticks was 0.08 [8], and the average minimum infection rate in larvae was 0.57%, nymphs 0.36%, males 0.90%, females 1.53%, fed ticks 18.2%, and unfed ticks 5.9% [9, 10]. In Table 1, more than 16 tick species collected from animals or vegetation were detected, with at least nine tick species including Haemaphysalis longicornis (H. longicornis), H. flava, H. concinna, H. formosensis, H. hystricis, H. megaspinosa, Ixodes nipponensis (I. nipponensis), Amblyomma testudinarium (A. testudinarium), and Rhipicephalus microplus (R. microplus) were found positive in SFTSV RNA detection [3, 9, 11, 15, 17–19]. The Haemaphysalis had attracted the most attention, and at least 6 species were test to be positive. The H. longicornis were suspected to be the major tick species in most areas, and the higher positive rate was 4.84% collected from animals in China [13] and 4.77% from vegetation in ROK [14]. There were also negative results of RNA detection in tick species, such as H. japonica, H. yeni, H. campanulata, H. phasiana, I. turdus, and Dermacentor sinicus (D. sinicus) [11, 13, 15, 16, 18]. Regarding the observed negative results, there were several possible explanations. First, due to the relatively small sizes and limitation of collection sites, the tick sample was not representative. Second, low positive rate of SFTSV in ticks and the limited viral loads may also be responsible for these negative results [22]. Tick bite has been considered to be the most important risk factor for SFTS, which was significantly associated with the SFTSV infection [17]. Ticks, especially the H. longicornis, which had higher density, wider distribution, and higher detection rate were suggested to be the primary reservoir and vector of SFTSV [23], with increasing supportive evidence. First, some SFTS patients have reported a history of tick bite, and the spatial and temporal distributions of SFTS human cases were consistent with the fluctuation of certain species of ticks in the endemic area [24–26]. Besides, the SFTSV-specific nucleotide sequences or virus isolated from ticks had high homology with those from the patients [27]. Second, the transmission feeding experiment found that H. longicornis fed on SFTSV-infected mice could acquire the virus and transstadially and transovarially transmit it to other developmental stages of ticks, and furthermore, the infected ticks could also transmit the virus to mice during feeding [28]. Besides, the transovarially and horizontally transmissions were also found in I. sinensis ticks [29]. Third, SFTSV RNA could be identified in larvae of ticks collected in vegetation without being blood fed, indicating the possibility of a vertical transmission and ticks as a putative reservoir host [30]. Except for ticks, mosquitoes and sandflies were also detected. In the first report of SFTSV, Yu et al. had already found that viral RNA was not detected in any of 5900 mosquitoes collected from the home environment of the patients [1]. Using experimental infections of mosquitoes with SFTSV, Liang et al. examined the role of mosquitoes in the transmission of the virus and did not detect viral replication in Culex pipiens pallens, Aedes aegypti, and Anopheles sinensis as revealed by the TaqMan quantitative real-time polymerase chain reaction (qRT-PCR) assay. Besides, the authors failed to isolate SFTSV from the Vero cells cultured with suspensions of SFTSV-infected mosquitoes [31]. Similarly, in another study, viral RNA was not detected in any tested mosquitoes, midges, and sandflies [11].

2.2. Domestic Animals

SFTSV is thought to circulate in an enzootic tick-vertebrate-tick cycle, yet the vertebrate hosts in nature have not been confirmed [30]. SFTS viral RNA was most commonly detected among domesticated animals, followed by ticks and humans [17]. One meta-analysis study found the pooled seroprevalence of anti-SFTSV antibodies was 45.70% in goats and sheep, 36.70% in cattle, 29.50% in dogs, 9.60% in chickens, 3.20% in rodents, and 3.20% in pigs, respectively [32]. In Table 2, SFTSV antibodies or RNA have been detected positive in more than ten kinds of domesticated animals, including dogs, goats, cattle, and pigs [4, 6, 11, 12, 17, 33, 39, 41, 42]. Among them, the highest antibody-positive rate was seen in cattle (97.92%) of China [36]. Additionally, high SFTSV antibody rates were also found in goats (74.77%), chickens (52.14%) [37], sheep (69.74%), dogs (68.18%), ducks (19.67%) [36], minks (8.43%) [6], cats (1.92%) [38], pigs (4.66%), and geese (1.67%) [35]. Besides, in ROK and China, SFTSV RNA was also found to be positive in cats (33.08%) [42], cattle (2.08%) [36], goats (1.93%) [39], pigs (1.67%) [41], and dogs (0.88%) [38]. Domestic animals, especially the companion animals, could increase the epidemic threat of SFTS due to the close interaction with humans [43]. Ticks predominantly feed on farm animals including goats, sheep, cattle, chicken, and also on companion animals such as dogs and cats [33, 34]. The domestic animals could acquire SFTS and play as the amplifying hosts and viral spread [24, 44]. Except for the vector of ticks, domestic animals could transmit SFTS in another way. High levels of SFTSV RNA loads could be detected in serum, eye swab, saliva, rectal swab, and urine of the domestic animals, indicating a risk of direct human infection from SFTS-infected animals [45]. A patient could acquire SFTS by blood splash when removed or burst ticks from the dogs with his bare hands [46]. Three SFTS patients had direct contact with body fluids of ill companion animals, and two SFTS patients had direct contact with saliva of an ill feral cat or pet dog, without a history of tick bite [47]. A woman was infected with SFTS two days after the bites from a sick cat [48]. From this perspective, the direct contact with body fluids of ill companion animals should be avoided. However, there were no direct evidence to support this viral transmission route. An experimental infection study in goats showed that the infected animals could not shed virus to the control animals through the respiratory or digestive tract route, and however, the control animals were infected after ticks’ infestation [49]. Thus, more evidence is still needed to prove that whether animals could transmit SFTSV directly.

2.3. Wild Animals

Among the wild animals, the migratory birds probably played a role in the transmission of the SFTSV. The migratory wild birds could carry the virus, either through their own infection or carrying attached ticks infected to distant regions via migratory flyways [30, 50, 51]. Besides, many other species of small wild animals infected with SFTSV may serve as the natural amplifying hosts. In Table 3, the SFTSV antibodies or RNA have been detected in more than 16 kinds of wild animals, namely, rodents, Asian house shrews, hedgehogs, water deer, wild deer, wild boars, Siberian roe deer, gorals, raccoon dogs, carrion crow, yellow weasels, hares, rock pigeons, pheasants, turtledoves, and mongooses [4, 23, 35, 36, 38, 40, 52–55]. The highest SFTSV antibody positive rate was seen in yellow weasels (91.11%) detected in China [36]. Besides, a high antibody positive rate was also found in hares (63.01%), pheasants (42.86%), hedgehogs (40.00%), rock pigeons (34.78%) [36], wild deer (25.00%), wild boars (25.00%) [4], and water deer (23.81%) [23]. It is noteworthy that the positive rate varied in the same kind animals in different studies. Up to now, no positive results have been found in Siberian roe deer, gorals, raccoon dogs, and carrion crows [23]. The highest SFTSV RNA-positive results were seen in water deer (4.76%) [23], wild boars (5.21%) [55] yellow weasels (2.22%), hares (2.74%) [36], Asian house shrews (2.6%), and rodents (0.7%) [52]. SFTSV has also been detected in the ticks collected from wild animals such as lizards and snakes, indicating that they may be the potential hosts of SFTSV [56]. Besides, the rhesus macaques could be infected with SFTS similar to human, which may be used to develop adequate animal models [57].

2.4. Risky Behavior

SFTS was mostly endemic in rural areas [58]. A case-control study conducted in Henan, Hubei, and Shandong provinces of China suggested that the cases were more likely to be farmers than controls (88.8% vs. 58.7%) [26]. Presence of weeds and shrubs in working areas or around the house, as well as domestic animals illness or death two weeks prior to disease onset, tick bites, tea-picking, grazing, farming, raising domestic animals, mowing, presence of rats, or contact with wild animals were risk factors for SFTSV infection [27, 35, 59, 60]. Farming activities may be one index of the SFTS etiologic diagnosis due to the facts that the farming activities around weeds and shrubs increase the exposure opportunities for ticks [27]. Raising animals may also increase the risk of tick contact and SFTS infection [44], and there were significant differences in the history of tick bite and breeding domestic animals between cases and controls [24]. Other epidemiological characteristics such as the seasonality and meteorological factors substantially differed across the affected area. Liu et al. found eight predictors were significantly associated with the occurrence of SFTSV, including temperature, rainfall, relative humidity, sunshine hours, elevation, distribution of H. longicornis ticks, cattle density, and coverage of forest [2]. The SFTS epidemic curve revealed that 83.7% cases occurred between May and July [58], which is consistent with local agricultural activities and the seasonal abundance of ticks. One study showed that the risk of SFTS was high in geographic areas where the farmland area begins to diminish and at midlevel altitudes [61].

2.5. Age and Sex

Age is an important determinant for SFTS morbidity and mortality, and elder age and high viral load were significantly associated with fatal clinical outcomes [62]. Li et al. found the mean age of seropositive farmers was 56.5 years and seroprevalence increased gradually with age [35]. One study analyzed 7721 laboratory-confirmed SFTS cases in China from 2010 to 2018 and found that residents more than 60 years old in rural areas with crop fields and tea farms were at an increased risk of SFTS [50]. Sex was another associated factor of SFTS, with the findings that the SFTSV antibodies were more prevalent in males than in females (1.87% vs. 0.71%, ) [35]. A study with 44 fatal SFTS cases showed that 16 (36.4%) were female and 28 (63.6%) were male [58]. As for the significant difference between age and sex, several hypotheses have been proposed. First, the decreased immune function and the more probability of comorbidities with chronic diseases in the elders may aggravate the SFTS fatality. Second, due to the fact that many young adults have moved to cities for better job opportunities, the elders from rural areas, especially the males, then have to assume the agricultural activities, which would make them more likely to be exposed to tick bites [2]. Besides, genetic susceptibility in the sexes may also be a reason for the difference in SFTSV infection and fatal outcome [63].

2.6. Person-to-Person Transmission

Person-to-person transmission of SFTSV has been proposed through close contact with blood or body secretions of infected patients [64]. The incubation period of the secondary patients was 10.0 days. The secondary attack rate (SAR) was 1.72–55.00%, and the average basic reproductive number (R0) was 0.13 (95% CI: 0.11–0.16) [65]. Risk factors assessment of the person-to-person transmission revealed that the major exposure factors may be blood contact without personal protection equipment (PPE) [66]. SFTSV could be transmitted through contact with patients’ cadaveric blood or bloody secretions by the unprotected skin or mucosa, indicating that SFTSV-infected blood may remain infectious for a long time, even after the death of patients [67]. A person was 25 times more likely to be infected with SFTS when contacted with blood [68], and the frequency of blood contact was found to be associated with the disease risk in a dose-response pattern [69]. Besides, contact with bloody secretions or feces [70], aerosol [71], and various body fluids including urine and tracheal aspirate contained SFTS virus [72] of the index patient without PPE may be potential sources of SFTS transmission.

2.7. Nosocomial Transmission

After investigating the possible contamination of hospital air and surfaces with SFTSV transmission, Ryu et al. found that the swab samples obtained from stethoscopes, doorknobs, and bed guardrails were positive, which were also seen in television monitors and sink tables despite being remote from the patients [73]. These findings indicated that the extensive environmental contamination of SFTSV occurred in rooms of critically ill patients with SFTS. Kim et al. found that of the 27 healthcare workers (HCWs) who contacted with a fatally ill patient with SFTS, four involved in cardiopulmonary resuscitation complained of fever and were diagnosed with SFTS [74]. Similarly, another study reported that among 25 HCWs who had direct contact with the index patient, five who had contact to blood or bloody respiratory secretions of the index patient without adequate use of PPE were infected with SFTS [75]. SFTS cases could also occur in hospital in other ways, such as needle-stick injury in medical activities [76] and handling sick animals [77]. One study examining the seroprevalence of SFTSV infection in veterinarian staff members found that 3 of 71 (4.2%) were seropositive for SFTSV-specific antibodies [42]. Consequently, the strict adherence to routine blood and body fluid precautions is necessary when HCWs have contact with any patient. Furthermore, universal precaution and full PPE is highly recommended when there are signs of bleeding.

3. Conclusions

In conclusion, there is increasing evidence suggesting that ticks may be the primary vector of SFTSV, while domestic or wild animals play as the reservoir of the virus. Raising animals, as well as farming and grazing activities, especially among people characterized by elder age and male may be risk factors for SFTSV infection. Person-to-person transmission and nosocomial transmission have also been identified. Furthermore, the main host animals and mechanisms of transmissions need more deep-in research.

Data Availability

The data used to support the findings of this study are included within the article.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Authors’ Contributions

Jin-Na Wang and Tian-Qi Li contributed equally to this study.

Acknowledgments

This work was granted by the Zhejiang Medical and Health Technology Project (2021KY119) and the National Critical Project for Science and Technology on Infectious Diseases of China (2017ZX10303404).

References

X. J. Yu, M. F. Liang, S. Y. Zhang et al., “Fever with thrombocytopenia associated with a novel bunyavirus in China,” New England Journal of Medicine, vol. 364, no. 16, pp. 1523–1532, 2011.
View at: Publisher Site | Google Scholar
K. Liu, H. Zhou, R. X. Sun et al., “A national assessment of the epidemiology of severe fever with thrombocytopenia syndrome, China,” Scientific Reports, vol. 5, Article ID 9679, 2015.
View at: Publisher Site | Google Scholar
S.-M. Yun, B. G. Song, W. Choi et al., “First isolation of severe fever with thrombocytopenia syndrome virus from Haemaphysalis longicornis ticks collected in severe fever with thrombocytopenia syndrome outbreak areas in the Republic of Korea,” Vector Borne and Zoonotic Diseases, vol. 16, no. 1, pp. 66–70, 2016.
View at: Publisher Site | Google Scholar
T. Kimura, A. Fukuma, M. Shimojima et al., “Seroprevalence of severe fever with thrombocytopenia syndrome (SFTS) virus antibodies in humans and animals in Ehime prefecture, Japan, an endemic region of SFTS,” Journal of Infection and Chemotherapy, vol. 24, no. 10, pp. 802–806, 2018.
View at: Publisher Site | Google Scholar
S. W. Han, J. G. Kang, A. R. Byeon, Y. K. Cho, K. S. Choi, and J. S. Chae, “Severe fever with thrombocytopenia syndrome in canines from the Republic of Korea,” Ticks and tick-borne diseases, vol. 11, no. 4, Article ID 101454, 2020.
View at: Publisher Site | Google Scholar
G.-S. Wang, J.-B. Wang, F.-L. Tian et al., “Severe fever with thrombocytopenia syndrome virus infection in minks in China,” Vector Borne and Zoonotic Diseases, vol. 17, no. 8, pp. 596–598, 2017.
View at: Publisher Site | Google Scholar
X. X. Huang, J. D. Li, A. Q. Li, S. W. Wang, and D. X. Li, “Epidemiological characteristics of severe fever with thrombocytopenia syndrome from 2010 to 2019 in mainland China,” International Journal of Environmental Research and Public Health, vol. 18, no. 6, Article ID 3092, 2021.
View at: Publisher Site | Google Scholar
X. Y. Huang, Z. Q. He, B. H. Wang, K. Hu, Y. Li, and W. S. Guo, “Severe fever with thrombocytopenia syndrome virus: a systematic review and meta-analysis of transmission mode,” Epidemiology and Infection, vol. 148, Article ID e239, 2020.
View at: Publisher Site | Google Scholar
S.-W. Park, B. Song, E. Shin et al., “Prevalence of severe fever with thrombocytopenia syndrome virus in Haemaphysalis longicornis ticks in South Korea,” Ticks Tick Borne Diseases, vol. 5, no. 6, pp. 975–977, 2014.
View at: Publisher Site | Google Scholar
S.-M. Yun, W.-G. Lee, J. Ryou et al., “Severe fever with thrombocytopenia syndrome virus in ticks collected from humans, South Korea, 2013,” Emerging Infectious Diseases, vol. 20, no. 8, pp. 1358–1361, 2014.
View at: Publisher Site | Google Scholar
H. Tian, P. Yu, S. Li et al., “Severe fever with thrombocytopenia syndrome virus in humans, domesticated animals, ticks, and mosquitoes, shaanxi province, China,” The American Journal of Tropical Medicine and Hygiene, vol. 96, no. 6, pp. 1346–1349, 2017.
View at: Publisher Site | Google Scholar
L. E. Yang, Z. Zhao, G. Hou et al., “Genomes and seroprevalence of severe fever with thrombocytopenia syndrome virus and Nairobi sheep disease virus in Haemaphysalis longicornis ticks and goats in Hubei, China,” Virology, vol. 529, pp. 234–245, 2019.
View at: Publisher Site | Google Scholar
S. Wang, D. Li, Z. Bi et al., “SFTS virus in ticks in an endemic area of China,” The American Journal of Tropical Medicine and Hygiene, vol. 92, no. 4, pp. 684–689, 2015.
View at: Publisher Site | Google Scholar
Y.-S. Jo, J.-G. Kang, J.-B. Chae et al., “Prevalence of severe fever with thrombocytopenia syndrome virus in ticks collected from national parks in Korea,” Vector Borne and Zoonotic Diseases, vol. 19, no. 4, pp. 284–289, 2019.
View at: Publisher Site | Google Scholar
S. M. Yun, Y. J. Lee, W. Choi et al., “Molecular detection of severe fever with thrombocytopenia syndrome and tick-borne encephalitis viruses in ixodid ticks collected from vegetation, Republic of Korea, 2014,” Ticks Tick Borne Diseases, vol. 7, no. 5, pp. 970–978, 2016.
View at: Publisher Site | Google Scholar
H. Ham, S. Jo, J. Jang, and S. Choi, “No detection of severe Fever with thrombocytopenia syndrome virus from ixodid ticks collected in seoul,” Korean Journal of Parasitology, vol. 52, no. 2, pp. 221–224, 2014.
View at: Publisher Site | Google Scholar
X. Xing, X. Guan, L. Liu et al., “Natural transmission model for severe fever with thrombocytopenia syndrome bunyavirus in villages of Hubei province, China,” Medicine, vol. 95, no. 4, Article ID e2533, 2016.
View at: Publisher Site | Google Scholar
Y. Sato, H. Mekata, P. E. Sudaryatma et al., “Isolation of severe fever with thrombocytopenia syndrome virus from various tick species in area with human severe fever with thrombocytopenia syndrome cases,” Vector Borne and Zoonotic Diseases, vol. 21, no. 5, pp. 378–384, 2021.
View at: Publisher Site | Google Scholar
H. Liu, Z. Li, Z. Wang et al., “The first molecular evidence of severe fever with thrombocytopenia syndrome virus in ticks in Jilin, Northeastern China,” Ticks and Tick-borne Diseases, vol. 7, no. 6, pp. 1280–1283, 2016.
View at: Publisher Site | Google Scholar
J. Lee, K. Moon, M. Kim et al., “Seasonal distribution of Haemaphysalis longicornis (Acari: ixodidae) and detection of SFTS virus in gyeongbuk province, Republic of Korea, 2018,” Acta Tropica, vol. 221, Article ID 106012, 2021.
View at: Publisher Site | Google Scholar
M. G. Seo, B. E. Noh, H. S. Lee, T. K. Kim, B. G. Song, and H. I. Lee, “Nationwide temporal and geographical distribution of tick populations and phylogenetic analysis of severe fever with thrombocytopenia syndrome virus in ticks in Korea, 2020,” Microorganisms, vol. 9, no. 8, Article ID 1630, 2021.
View at: Publisher Site | Google Scholar
D. Hayasaka, S. Shimada, K. Aoki et al., “Epidemiological survey of severe fever with thrombocytopenia syndrome virus in ticks in nagasaki, Japan,” Tropical Medicine and Health, vol. 43, no. 3, pp. 159–164, 2015.
View at: Publisher Site | Google Scholar
S.-S. Oh, J.-B. Chae, J.-G. Kang et al., “Detection of severe fever with thrombocytopenia syndrome virus from wild animals and ixodidae ticks in the Republic of Korea,” Vector Borne and Zoonotic Diseases, vol. 16, no. 6, pp. 408–414, 2016.
View at: Publisher Site | Google Scholar
J. Sun, Z. Gong, F. Ling et al., “Factors associated with severe fever with thrombocytopenia syndrome infection and fatal outcome,” Scientific Reports, vol. 6, Article ID 33175, 2016.
View at: Publisher Site | Google Scholar
B. Xu, L. Liu, X. Huang et al., “Metagenomic analysis of fever, thrombocytopenia and leukopenia syndrome (FTLS) in Henan Province, China: discovery of a new bunyavirus,” PLoS Pathogens, vol. 7, no. 11, Article ID e1002369, 2011.
View at: Publisher Site | Google Scholar
F. Ding, X. H. Guan, K. Kang et al., “Risk factors for bunyavirus-associated severe Fever with thrombocytopenia syndrome, China,” PLoS Neglected Tropical Diseases, vol. 8, no. 10, Article ID e3267, 2014.
View at: Publisher Site | Google Scholar
J. Hu, Z. Li, L. Hong et al., “Preliminary fast diagnosis of severe fever with thrombocytopenia syndrome with clinical and epidemiological parameters,” PLoS One, vol. 12, no. 7, Article ID e0180256, 2017.
View at: Publisher Site | Google Scholar
L.-M. Luo, L. Zhao, H.-L. Wen et al., “Haemaphysalis longicornisTicks as reservoir and vector of severe fever with thrombocytopenia syndrome virus in China,” Emerging Infectious Diseases, vol. 21, no. 10, pp. 1770–1776, 2015.
View at: Publisher Site | Google Scholar
Y. Y. Hu, L. Zhuang, K. Liu et al., “Role of three tick species in the maintenance and transmission of severe fever with thrombocytopenia syndrome virus,” PLoS Neglected Tropical Diseases, vol. 14, no. 6, Article ID e0008368, 2020.
View at: Publisher Site | Google Scholar
Z. Li, C. Bao, J. Hu et al., “Ecology of the tick-borne phlebovirus causing severe fever with thrombocytopenia syndrome in an endemic area of China,” PLoS Neglected Tropical Diseases, vol. 10, no. 4, Article ID e0004574, 2016.
View at: Publisher Site | Google Scholar
S. Y. Liang, H. L. Chu, X. L. Guo et al., “Experimental infections of mosquitoes with severe fever with thrombocytopenia syndrome virus,” Infectious Diseases of Poverty, vol. 6, no. 1, Article ID 78, 2017.
View at: Publisher Site | Google Scholar
C. Chen, P. Li, K.-F. Li et al., “Animals as amplification hosts in the spread of severe fever with thrombocytopenia syndrome virus: a systematic review and meta-analysis,” International Journal of Infectious Diseases, vol. 79, pp. 77–84, 2019.
View at: Publisher Site | Google Scholar
S.-H. Lee, H.-J. Kim, J.-W. Byun et al., “Molecular detection and phylogenetic analysis of severe fever with thrombocytopenia syndrome virus in shelter dogs and cats in the Republic of Korea,” Ticks and Tick-borne Diseases, vol. 8, no. 4, pp. 626–630, 2017.
View at: Publisher Site | Google Scholar
S.-H. Lee, H.-J. Kim, M.-J. Lee et al., “Prevalence of antibodies against severe fever with thrombocytopenia syndrome virus in shelter dogs in the Republic of Korea,” Ticks and Tick-borne Diseases, vol. 9, no. 2, pp. 183–187, 2018.
View at: Publisher Site | Google Scholar
Z. Li, J. Hu, C. Bao et al., “Seroprevalence of antibodies against SFTS virus infection in farmers and animals, Jiangsu, China,” Journal of Clinical Virology, vol. 60, no. 3, pp. 185–189, 2014.
View at: Publisher Site | Google Scholar
X. Y. Huang, Y. H. Du, H. F. Wang et al., “Prevalence of severe fever with thrombocytopenia syndrome virus in animals in Henan Province, China,” Infectious Diseases of Poverty, vol. 8, no. 1, Article ID 56, 2019.
View at: Publisher Site | Google Scholar
S. Ding, H. Yin, X. Xu et al., “A cross-sectional survey of severe fever with thrombocytopenia syndrome virus infection of domestic animals in Laizhou City, Shandong Province, China,” Japanese Journal of Infectious Diseases, vol. 67, no. 1, pp. 1–4, 2014.
View at: Publisher Site | Google Scholar
A. Matsuu, E. Hamakubo, and M. Yabuki, “Seroprevalence of severe fever with thrombocytopenia syndrome virus in animals in Kagoshima Prefecture, Japan, and development of Gaussia luciferase immunoprecipitation system to detect specific IgG antibodies,” Ticks and Tick-Borne Diseases, vol. 12, no. 5, Article ID 101771, 2021.
View at: Publisher Site | Google Scholar
K.-M. Yu, M.-A. Yu, S.-J. Park et al., “Seroprevalence and genetic characterization of severe fever with thrombocytopenia syndrome virus in domestic goats in South Korea,” Ticks and Tick-borne Diseases, vol. 9, no. 5, pp. 1202–1206, 2018.
View at: Publisher Site | Google Scholar
Y. Kuba, H. Kyan, Y. Azama et al., “Seroepidemiological study of severe fever with thrombocytopenia syndrome in animals and humans in Okinawa, Japan,” Ticks Tick Borne Diseases, vol. 12, no. 6, Article ID 101821, 2021.
View at: Publisher Site | Google Scholar
J.-G. Kang, S.-S. Oh, Y.-S. Jo, J.-B. Chae, Y.-K. Cho, and J.-S. Chae, “Molecular detection of severe fever with thrombocytopenia syndrome virus in Korean domesticated pigs,” Vector Borne and Zoonotic Diseases, vol. 18, no. 8, pp. 450–452, 2018.
View at: Publisher Site | Google Scholar
T. Ando, T. Nabeshima, S. Inoue et al., “Severe fever with thrombocytopenia syndrome in cats and its prevalence among veterinarian staff members in nagasaki, Japan,” Viruses, vol. 14, no. 6, Article ID 1142, 2021.
View at: Publisher Site | Google Scholar
K. Kida, Y. Matsuoka, T. Shimoda et al., “A case of cat-to-human transmission of severe fever with thrombocytopenia syndrome virus,” Japanese Journal of Infectious Diseases, vol. 72, no. 5, pp. 356–358, 2019.
View at: Publisher Site | Google Scholar
X. Xing, X. Guan, L. Liu et al., “A case-control study of risk sources for severe fever with thrombocytopenia syndrome in Hubei province, China,” International Journal of Infectious Diseases, vol. 55, pp. 86–91, 2017.
View at: Publisher Site | Google Scholar
E. S. Park, M. Shimojima, N. Nagata et al., “Severe Fever with Thrombocytopenia Syndrome Phlebovirus causes lethal viral hemorrhagic fever in cats,” Scientific Reports, vol. 9, no. 1, Article ID 11990, 2019.
View at: Publisher Site | Google Scholar
J. K. Chung, C. M. Kim, D.-M. Kim et al., “Severe fever with thrombocytopenia syndrome associated with manual de-ticking of domestic dogs,” Vector Borne and Zoonotic Diseases, vol. 20, no. 4, pp. 285–294, 2020.
View at: Publisher Site | Google Scholar
Y. Kobayashi, H. Kato, T. Yamagishi et al., “Severe fever with thrombocytopenia syndrome, Japan, 2013-2017,” Emerging Infectious Diseases, vol. 26, no. 4, pp. 692–699, 2020.
View at: Publisher Site | Google Scholar
M. Tsuru, T. Suzuki, T. Murakami et al., “Pathological characteristics of a patient with severe fever with thrombocytopenia syndrome (SFTS) infected with SFTS virus through a sick cat’s bite,” Viruses, vol. 13, no. 2, Article ID 204, 2021.
View at: Publisher Site | Google Scholar
Y. Jiao, X. Qi, D. Liu et al., “Experimental and natural infections of goats with severe fever with thrombocytopenia syndrome virus: evidence for ticks as viral vector,” PLoS Neglected Tropical Diseases, vol. 9, no. 10, Article ID e0004092, 2015.
View at: Publisher Site | Google Scholar
D. Miao, M. J. Liu, Y. X. Wang et al., “Epidemiology and ecology of severe fever with thrombocytopenia syndrome in China, 2010-2018,” Clinical Infectious Diseases, vol. 1561, 2020.
View at: Google Scholar
Y. Yun, K. T. Kwon, S. Y. Ryu et al., “Phylogenetic analysis of severe fever with thrombocytopenia syndrome virus in South Korea and migratory bird routes between China, South Korea, and Japan,” The American Journal of Tropical Medicine and Hygiene, vol. 93, no. 3, pp. 468–474, 2015.
View at: Publisher Site | Google Scholar
J.-W. Liu, H.-L. Wen, L.-Z. Fang et al., “Prevalence of SFTSV among Asian house shrews and rodents, China, January-August 2013,” Emerging Infectious Diseases, vol. 20, no. 12, pp. 2126–2128, 2014.
View at: Publisher Site | Google Scholar
H. S. Lee, J. Kim, K. Son et al., “Phylogenetic analysis of severe fever with thrombocytopenia syndrome virus in Korean water deer (Hydropotes inermis argyropus) in the Republic of Korea,” Ticks and Tick-Borne diseases, vol. 11, no. 2, Article ID 101331, 2020.
View at: Publisher Site | Google Scholar
L. Uchida, D. Hayasaka, M. M. Ngwe Tun, K. Morita, Y. Muramatsu, and K. Hagiwara, “Survey of tick-borne zoonotic viruses in wild deer in Hokkaido, Japan,” Journal of Veterinary Medical Science, vol. 80, no. 6, pp. 985–988, 2018.
View at: Publisher Site | Google Scholar
J. M. Rim, S. W. Han, Y. K. Cho et al., “Survey of severe fever with thrombocytopenia syndrome virus in wild boar in the Republic of Korea,” Ticks Tick Borne Diseases, vol. 12, no. 6, Article ID 101813, 2021.
View at: Publisher Site | Google Scholar
J.-H. Suh, H.-C. Kim, S.-M. Yun et al., “Detection of SFTS virus inIxodes nipponensisandAmblyomma testudinarium(ixodida: ixodidae) collected from reptiles in the Republic of Korea,” Journal of Medical Entomology, vol. 53, no. 3, pp. 584–590, 2016.
View at: Publisher Site | Google Scholar
C. Jin, H. Jiang, M. Liang et al., “SFTS virus infection in nonhuman primates,” The Journal of Infectious Diseases, vol. 211, no. 6, pp. 915–925, 2015.
View at: Publisher Site | Google Scholar
T. Wang, X. L. Li, M. Liu et al., “Epidemiological characteristics and environmental risk factors of severe fever with thrombocytopenia syndrome in Hubei province, China, from 2011 to 2016,” Frontiers in Microbiology, vol. 8, Article ID 387, 2017.
View at: Publisher Site | Google Scholar
S. Liang, H. Ge, Q. Lu et al., “Seroprevalence and risk factors for severe fever with thrombocytopenia syndrome virus infection in Jiangsu Province, China, 2011,” The American Journal of Tropical Medicine and Hygiene, vol. 90, no. 2, pp. 256–259, 2014.
View at: Publisher Site | Google Scholar
Y. Lyu, F. Ding, J. Sun et al., “Seroprevalence and risk factors of severe fever with thrombocytopenia syndrome virus infection in endemic areas,” Infectious Diseases, vol. 48, no. 7, pp. 544–549, 2016.
View at: Publisher Site | Google Scholar
K. Yasuo and H. Nishiura, “Spatial epidemiological determinants of severe fever with thrombocytopenia syndrome in Miyazaki, Japan: a GWLR modeling study,” BMC Infectious Diseases, vol. 19, no. 1, Article ID 498, 2019.
View at: Publisher Site | Google Scholar
Y. Chen, B. Jia, Y. Liu, R. Huang, J. Chen, and C. Wu, “Risk factors associated with fatality of severe fever with thrombocytopenia syndrome: a meta-analysis,” Oncotarget, vol. 8, no. 51, pp. 89119–89129, 2017.
View at: Publisher Site | Google Scholar
J. Sun, Y. Tang, F. Ling et al., “Genetic susceptibility is one of the determinants for severe fever with thrombocytopenia syndrome virus infection and fatal outcome: an epidemiological investigation,” PLoS One, vol. 10, no. 7, Article ID e0132968, 2015.
View at: Publisher Site | Google Scholar
Y. Wang, B. Deng, J. Zhang, W. Cui, W. Yao, and P. Liu, “Person-to-person asymptomatic infection of severe fever with thrombocytopenia syndrome virus through blood contact,” Internal Medicine, vol. 53, no. 8, pp. 903–906, 2014.
View at: Publisher Site | Google Scholar
X. Fang, J. Hu, Z. Peng et al., “Epidemiological and clinical characteristics of severe fever with thrombocytopenia syndrome bunyavirus human-to-human transmission,” PLoS Neglected Tropical Diseases, vol. 15, no. 4, Article ID e0009037, 2021.
View at: Publisher Site | Google Scholar
X. L. Jiang, S. Zhang, M. Jiang et al., “A cluster of person-to-person transmission cases caused by SFTS virus in Penglai, China,” Clinical Microbiology and Infections, vol. 21, no. 3, pp. 274–279, 2015.
View at: Publisher Site | Google Scholar
H. Chen, K. Hu, J. Zou, and J. Xiao, “A cluster of cases of human-to-human transmission caused by severe fever with thrombocytopenia syndrome bunyavirus,” International Journal of Infectious Diseases, vol. 17, no. 3, pp. e206–e208, 2013.
View at: Publisher Site | Google Scholar
C. Ye and R. Qi, “Risk factors for person-to-person transmission of severe fever with thrombocytopenia syndrome,” Infection Control & Hospital Epidemiology, vol. 42, no. 5, pp. 582–585, 2021.
View at: Publisher Site | Google Scholar
X. Tang, W. Wu, H. Wang et al., “Human-to-human transmission of severe fever with thrombocytopenia syndrome bunyavirus through contact with infectious blood,” Journal of Infectious Diseases, vol. 207, no. 5, pp. 736–739, 2013.
View at: Publisher Site | Google Scholar
C.-J. Bao, X.-L. Guo, X. Qi et al., “A family cluster of infections by a newly recognized bunyavirus in eastern China, 2007: further evidence of person-to-person transmission,” Clinical Infectious Diseases, vol. 53, no. 12, pp. 1208–1214, 2011.
View at: Publisher Site | Google Scholar
Y. Zhu, H. Wu, J. Gao et al., “Two confirmed cases of severe fever with thrombocytopenia syndrome with pneumonia: implication for a family cluster in East China,” BMC Infectious Diseases, vol. 17, no. 1, Article ID 537, 2017.
View at: Publisher Site | Google Scholar
Y. Liu, Q. Li, W. Hu et al., “Person-to-person transmission of severe fever with thrombocytopenia syndrome virus,” Vector Borne and Zoonotic Diseases, vol. 12, no. 2, pp. 156–160, 2012.
View at: Publisher Site | Google Scholar
B. H. Ryu, J. Y. Kim, T. Kim et al., “Extensive severe fever with thrombocytopenia syndrome virus contamination in surrounding environment in patient rooms,” Clinical Microbiology and Infection, vol. 24, no. 8, pp. 911–e4, 2018.
View at: Publisher Site | Google Scholar
W. Y. Kim, W. Choi, S.-W. Park et al., “Nosocomial transmission of severe fever with thrombocytopenia syndrome in Korea,” Clinical Infectious Diseases, vol. 60, no. 11, pp. 1681–1683, 2015.
View at: Publisher Site | Google Scholar
I. Y. Jung, W. Choi, J. Kim et al., “Nosocomial person-to-person transmission of severe fever with thrombocytopenia syndrome,” Clinical Microbiology and Infection, vol. 25, no. 5, pp. 633–e4, 2019.
View at: Publisher Site | Google Scholar
Y. Chen, B. Jia, R. Huang et al., “Occupational severe fever with thrombocytopenia syndrome following needle-stick injury,” Infection Control and Hospital Epidemiology, vol. 38, no. 6, pp. 760–762, 2017.
View at: Publisher Site | Google Scholar
A. Yamanaka, Y. Kirino, S. Fujimoto et al., “Direct transmission of severe fever with thrombocytopenia syndrome virus from domestic cat to veterinary personnel,” Emerging Infectious Diseases, vol. 26, no. 12, pp. 2994–2998, 2020.
View at: Publisher Site | Google Scholar

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Copyright © 2021 Jin-Na Wang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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