Background: Severe fever with thrombocytopenia syndrome (SFTS) is an emerging infectious disease discovered in China in 2009. In July 2013, the first human infection with SFTS virus (SFTSV) was detected in Shaanxi Province, Western China. Methods: A seroprevalence study among humans was carried out in an SFTS endemic village; specifically, serum samples were collected from 363 farmers in an SFTS endemic village in Shaanxi Province. The presence of SFTSV antibodies in serum was determined using an ELISA. Results: SFTSV antibodies were found in a total of 20 people (5.51%), with no significant difference between males and females (6.93% and 4.42%, respectively; Chi-square = 1.29, p = 0.25). Moreover, the SFTSV antibody positive rate was not significantly different across different age groups (Chisquare = 2.23, p = 0.69). Conclusions: SFTSV readily infects humans with outdoor exposure. The results of the serological study indicate that the virus circulates widely in Shaanxi Province. SFTSV represents a public health threat in China

Chowell, Gerardo

Dong, Jian-Hua

Han, Zong-Qi

Li, Shen

Lv, Wen

Tian, Huai-Yu

Tian, Hui

Wang, Jing-Jun

Wei, Jing

Xu, Bing

Yu, Peng-Bo

International Journal of Infectious Diseases

English

ScholarWorks @ Georgia State University

Georgia State UniversityScholarWorks @ Georgia State UniversityPublic Health Faculty Publications School of Public Health2-2015The First Human Infection with Severe Fever withThrombocytopenia Syndrome Virus in ShaanxiProvince, ChinaJing WeiShaanxi Provincial Center for Disease Control and PreventionShen LiShaanxi Provincial Center for Disease Control and PreventionJian-Hua DongShaanxi Provincial Center for Disease Control and PreventionHui TianBaoji Center for Disease Control and PreventionGerardo ChowellGeorgia State University, gchowell@gsu.eduSee next page for additional authorsFollow this and additional works at: https://scholarworks.gsu.edu/iph_facpubPart of the Public Health CommonsThis Article is brought to you for free and open access by the School of Public Health at ScholarWorks @ Georgia State University. It has been acceptedfor inclusion in Public Health Faculty Publications by an authorized administrator of ScholarWorks @ Georgia State University. For more information,please contact scholarworks@gsu.edu.Recommended CitationJ. Wei, S. Li, J. H. Dong, H. Tian, G. Chowell, H. Y. Tian, W. Lv, Z. Q. Han, B. Xu, P. B. Yu and J. J. Wang. The First Human Infectionwith Severe Fever with Thrombocytopenia Syndrome Virus in Shaanxi Province, China. J Infect Dis, 35 37-9. doi: http://dx.doi.org/10.1016/j.ijid.2015.02.014AuthorsJing Wei, Shen Li, Jian-Hua Dong, Hui Tian, Gerardo Chowell, Huai-Yu Tian, Wen Lv, Zong-Qi Han, Bing Xu,Peng-Bo Yu, and Jing-Jun WangThis article is available at ScholarWorks @ Georgia State University: https://scholarworks.gsu.edu/iph_facpub/147Short CommunicationThe ﬁrst human infection with severe fever with thrombocytopeniasyndrome virus in Shaanxi Province, ChinaJing Wei a, Shen Li a, Jian-Hua Dong a, Hui Tian b, Gerardo Chowell c, Huai-Yu Tian d,Wen Lv a, Zong-Qi Han e, Bing Xu d,f, Peng-Bo Yu a,1,*, Jing-Jun Wang a,1,*a Shaanxi Provincial Center for Disease Control and Prevention, Xi’an, Shaanxi 710054, ChinabBaoji Center for Disease Control and Prevention, Baoji, Shaanxi, Chinac School of Public Health, Georgia State University, Atlanta, Georgia, USAd State Key Laboratory of Remote Sensing Science, College of Global Change and Earth System Science, Beijing Normal University, Beijing, Chinae Long County Center for Disease Control and Prevention of Shaanxi Province, Baoji, Shaanxi, ChinafMinistry of Education Key Laboratory for Earth System Modeling, Center for Earth System Science, School of Environment, Tsinghua University, Beijing, China1. IntroductionSevere fever with thrombocytopenia syndrome virus (SFTSV) isa newly identiﬁed novel Phlebovirus of the Bunyaviridae family,1which has been implicated as the causative agent of severe feverwith thrombocytopenia syndrome (SFTS) in China.2 The clinicalsymptoms of SFTS are non-speciﬁc and include high fever,gastrointestinal symptoms, thrombocytopenia, leukocytopenia,multi-organ dysfunction, and hemorrhagic tendency.1 Mostreported SFTS cases have involved hospitalized patients withrelatively serious clinical symptoms, with an average case-fatalityrate of 12%.3 Fatal cases of infection with SFTSV have recently beenreported in South Korea and Japan as well.4,5 Haemaphysalislongicornis ticks have been implicated as the vectors of SFTSV, and ahigh seroprevalence of SFTSV has been reported in domesticanimals.1The ﬁrst human case of SFTS in a rural area of Long County inShaanxi Province led to a seroprevalence study in the same villagewhere the ﬁrst case was detected, with the goal of estimating theseroprevalence of SFTSV in this population.2. Methods2.1. Sample and data collectionWe conducted a seroprevalence study in the village in LongCounty where the ﬁrst case of SFTS was detected. A total of363 serum samples were collected from 363 healthy volunteers. Astandardized questionnaire was used to collect information ondemographic characteristics including age, gender, and residentialaddress. The sampled population was divided into ﬁve age groups:0–6, 7–19, 20–39, 40–59, and 60 years.International Journal of Infectious Diseases 35 (2015) 37–39A R T I C L E I N F OArticle history:Received 19 December 2014Received in revised form 15 January 2015Accepted 18 February 2015Corresponding Editor: Eskild Petersen,Aarhus, DenmarkKeywords:Severe fever with thrombocytopeniasyndromePrevalenceBunyaviridaeEpidemiological characteristicS U M M A R YBackground: Severe fever with thrombocytopenia syndrome (SFTS) is an emerging infectious diseasediscovered in China in 2009. In July 2013, the ﬁrst human infection with SFTS virus (SFTSV) was detectedin Shaanxi Province, Western China.Methods: A seroprevalence study among humans was carried out in an SFTS endemic village;speciﬁcally, serum samples were collected from 363 farmers in an SFTS endemic village in ShaanxiProvince. The presence of SFTSV antibodies in serum was determined using an ELISA.Results: SFTSV antibodies were found in a total of 20 people (5.51%), with no signiﬁcant differencebetween males and females (6.93% and 4.42%, respectively; Chi-square = 1.29, p = 0.25). Moreover, theSFTSV antibody positive rate was not signiﬁcantly different across different age groups (Chi-square = 2.23, p = 0.69).Conclusions: SFTSV readily infects humans with outdoor exposure. The results of the serological studyindicate that the virus circulates widely in Shaanxi Province. SFTSV represents a public health threat inChina. 2015 Published by Elsevier Ltd on behalf of International Society for Infectious Diseases. This is an openaccess article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).* Corresponding authors. Tel.: +86 029 82221026; fax: +86 029 82211952.E-mail addresses: sxcdcy@21cn.com (P.-B. Yu), jingjunwang@china.com(J.-J. Wang).1 Jing Wei and Shen Li contributed equally to this article.Contents lists available at ScienceDirectInternational Journal of Infectious Diseasesjou r nal h o mep ag e: w ww .e lsev ier . co m / loc ate / i j idhttp://dx.doi.org/10.1016/j.ijid.2015.02.0141201-9712/ 2015 Published by Elsevier Ltd on behalf of International Society for Infectious Diseases. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).Long County is located in Central China (Figure 1) and had apopulation of a quarter million at the end of 2010. It has an annualaverage temperature of 8–16 8C, and the average rainfall is600 mm.2.2. Serological testingSamples were tested for the presence of SFTSV RNA byquantitative real-time reverse transcription PCR (RT-PCR). Anti-bodies (including IgG and IgM) in serum samples were detectedusing a double-antigen sandwich ELISA, as described previously.6Positive samples were further diluted to determine the antibodytiters.2.3. Case deﬁnitionThe patient was diagnosed based on the diagnosis andtreatment programs for severe fever with thrombocytopeniasyndrome issued by the Chinese Ministry of Health. The clinicalfeatures include abrupt onset of fever (38 8C) and respiratorytract or gastrointestinal symptoms, followed by a progressivedecline in platelets and white blood cells. A conﬁrmed case of SFTSwas deﬁned as a person who met these criteria and who also had atleast one of the following laboratory criteria for diagnosis: (1)detection of SFTSV RNA by a molecular method, (2) seroconversionor a 4-fold rise in antibody titers between two serum samplescollected at least 2 weeks apart, and (3) SFTSV isolated from clinicalspecimens.2.4. Statistical analysesAll statistical analyses were performed using SPSS 17.0 (SPSSInc., Chicago, IL, USA); the statistical signiﬁcance level was set at0.05. The Chi-square test or Fisher’s exact test was used to assessdifferences in SFTSV seroprevalence by gender and age group.3. ResultsThe ﬁrst human case of SFTS in Shaanxi Province was a 66-year-old man who had a sudden onset of fever on July 11, 2013, with atemperature of 38 8C, accompanied by chills, pharyngeal pain,nausea, vomiting, and abdominal pain. The patient’s family islocated in a rural area of Long County. The patient did not have ahistory of outdoor activities before illness onset, and the patient’scattle had reportedly not been out of the village for the last 3 years.Of the 363 volunteer participants, 173 (47.6%) were male and190 (54.9%) were female. The ages of the participants ranged from3 years to 80 years, and the median age was 42 years. A total of363 serum samples were obtained from the healthy volunteers andsent to the laboratory of Shaanxi Provincial Center for DiseaseFigure 1. Location of Baoji in China and the location of selected districts where serum samples of healthy persons were collected and tested in 2013.Table 1Seropositivity for SFTSV among healthy humans in Shaanxi, ChinaNumber of serumsamples testedNumber SFTSV-IgGseropositivePercentageseropositiveChi-square p-ValueGender 1.29 0.25Male 173 12 6.93Female 190 8 4.42Age, years 2.24 0.696 59 1 1.697–19 54 3 5.5620–39 68 4 5.8840–59 128 9 7.0360 54 3 5.56Total 363 20 5.51SFTSV, severe fever with thrombocytopenia syndrome virus.J. Wei et al. / International Journal of Infectious Diseases 35 (2015) 37–3938Control and Prevention (CDC). Overall, 6% (20/363) of serumsamples were seropositive for SFTSV (6.93% among males and4.21% among females). There was no statistically signiﬁcantdifference in seroprevalence between males and females (Chi-square = 1.29, p = 0.25) (Table 1).The sampled population was divided into ﬁve age groups (0–6,7–19, 20–39, 40–59, and 60 years) and the correspondingseroprevalence levels were 1.69% (1/59), 5.56% (3/54), 5.88% (4/68), 7.03% (9/128), and 5.56% (3/54), respectively. Statisticalanalyses showed that the seroprevalence of antibodies against thevirus did not increase with age (Table 1). None of the seropositiveparticipants reported any of the disease symptoms that areassociated with SFTSV infections.4. DiscussionWe found an SFTSV seroprevalence level of 5.51% in an SFTSendemic village, which is similar to that reported in Hubei Province(6.37%) and Zhejiang Province (5.51%), but much higher than thatreported in Shandong Province (0.84%) and Jiangsu Province(0.94%).7–9 This discrepancy may be attributed to the season ofsample collection, age and sex of the subjects, previous exposure orlow level of infection, or differences in detection methodsemployed in different studies. Furthermore, the seropositivevolunteers in our study had not had contact with the ﬁrst reportedpatient before onset, which suggests that other infections in thevillage may have resulted from natural exposure to a reservoir.There was no statistical difference observed by sex, indicatingthat men and women in rural areas of Shaanxi are equally exposedto SFTSV; this is in line with the results of a prior study conductedin Jiangsu Province, China in 2011.10 However, surveillance datafrom 2012 and 2013 in Jiangsu Province have indicated that SFTSVantibodies are more prevalent in males than in females.11 Furtherstudies are needed to clarify this difference.Our study demonstrated that seroprevalence varied with age.Speciﬁcally, there were signiﬁcant differences among studied agegroups for SFTSV infection. The incidence rate of SFTS was higher inpatients between 20 and 60 years of age compared to patients aged<20 years. This suggests that the older age groups haveparticipated in long-term outdoor activities more than the otherage groups. However, the seroprevalence of SFTSV in healthypeople was not signiﬁcantly different among age groups inShandong Province, although SFTS patients were mainly elderly.12In conclusion, our study indicates signiﬁcant levels of SFTSVantibodies among healthy humans, which suggests subclinicalSFTSV infections or a relatively mild form of SFTS illness. Moreemphasis is needed on this novel disease, including enhancedsurveillance activities related to the virus in ticks and domesticanimals.AcknowledgementsThis work was supported by the Chinese National Science andTechnology Major Project (grant number 2013ZX10004202), theShaanxi Provincial Department of Science and Technology (grantnumbers 2013K12-04-02), and the National Research Program ofthe Ministry of Science and Technology, China (grant numbers2012CB955501, 2012AA12A407, 2013AA122003).Ethical statement: The study was approved by the ethics reviewcommittee of Shaanxi Provincial Center for Disease Control andPrevention. The sera were collected with the consent of thevolunteers.Conﬂict of interest: None for all authors.References1. Yu XJ, Liang MF, Zhang SY, Liu Y, Li JD, Sun YL, et al. Fever with thrombocyto-penia associated with a novel bunyavirus in China. N Engl J Med2011;364:1523–32.2. Chen H, Hu K, Zou J, Xiao J. A cluster of cases of human-to-human transmissioncaused by severe fever with thrombocytopenia syndrome bunyavirus. Int JInfect Dis 2013;17:e206–8.3. Zhang YZ, He YW, Dai YA, Xiong YE, Zheng H, Zhou DJ, et al. Hemorrhagic fevercaused by a novel bunyavirus in China: pathogenesis and correlates of fataloutcome. Clin Infect Dis 2012;54:527–53.4. Takahashi T, Maeda K, Suzuki T, Ishido A, Shigeoka T, Tominaga T, et al. The ﬁrstidentiﬁcation and retrospective study of severe fever with thrombocytopeniasyndrome in Japan. J Infect Dis 2014;209:816–27.5. Kim KH, Yi J, Kim G, Choi SJ, Jun KI, Kim NH, et al. Severe fever with thrombo-cytopenia syndrome, South Korea, 2012. Emerg Infect Dis 2013;19:1892–4.6. Sun J, Chai C, Lv H, Lin J, Wang C, Chen E, et al. Epidemiological characteristics ofsevere fever with thrombocytopenia syndrome in Zhejiang Province, China. Int JInfect Dis 2014;25:180–5.7. Zhan J, Huo X, Guan X, Jiang Y, Xu J, Li G, et al. Analysis on antibody levels againstsevere fever with thrombocytopenia syndrome bunyavirus among healthypopulation in Hubei Province. Chinese Journal of Health Laboratory Technology2013;23:922–3.8. Zhang WS, Zeng XY, Zhou MH, Jiao YJ, Wen T, Guo XL, et al. Seroepidemiology ofsevere fever with thrombocytopenia syndrome bunyavirus in Jiansu Province.(In Chinese) Dis Surveill 2011;26:676–8.9. Zhao L, Zhai S, Wen H, Cui F, Chi Y, Wang L, et al. Severe fever with thrombocy-topenia syndrome virus, Shandong Province, China. Emerg Infect Dis2012;18:963–5.10. Liang S, Bao C, Zhou M, Hu J, Tang F, Guo X, et al. Seroprevalence and risk factorsfor severe fever with thrombocytopenia syndrome virus infection in JiangsuProvince, China, 2011. Am J Trop Med Hyg 2014;90:256–9.11. Li Z, Hu J, Bao C, Li P, Qi X, Qin Y, et al. Seroprevalence of antibodies against SFTSvirus infection in farmers and animals, Jiangsu. China J Clin Virol 2014;60:185–9.12. Ding S, Niu G, Xu X, Li J, Zhang X, Yin H, et al. Age is a critical risk factor for severefever with thrombocytopenia syndrome. PLoS One 2014;9:e111736.J. Wei et al. / International Journal of Infectious Diseases 35 (2015) 37–39 39

The First Human Infection with Severe Fever with Thrombocytopenia Syndrome Virus in Shaanxi Province, China

Background: Severe fever with thrombocytopenia syndrome (SFTS) is an emerging infectious disease discovered in China in 2009. In July 2013, the first human infection with SFTS virus (SFTSV) was detected in Shaanxi Province, Western China.
Methods: A seroprevalence study among humans was carried out in an SFTS endemic village; specifically, serum samples were collected from 363 farmers in an SFTS endemic village in Shaanxi Province. The presence of SFTSV antibodies in serum was determined using an ELISA.
Results: SFTSV antibodies were found in a total of 20 people (5.51%), with no significant difference between males and females (6.93% and 4.42%, respectively; Chi-square = 1.29, p = 0.25). Moreover, the SFTSV antibody positive rate was not significantly different across different age groups (Chi-square = 2.23, p = 0.69).
Conclusions: SFTSV readily infects humans with outdoor exposure. The results of the serological study indicate that the virus circulates widely in Shaanxi Province. SFTSV represents a public health threat in China

Jing Wei

Shen Li

Jian-Hua Dong

Hui Tian

Gerardo Chowell

Huai-Yu Tian

Wen Lv

Zong-Qi Han

Bing Xu

Peng-Bo Yu

Jing-Jun Wang

Directory of Open Access Journals

The first human infection with severe fever with thrombocytopenia syndrome virus in Shaanxi Province, China

Georgia State University

Georgia State University
ScholarWorks @ Georgia State University
Public Health Faculty Publications School of Public Health
2-2015
The First Human Infection with Severe Fever with
Thrombocytopenia Syndrome Virus in Shaanxi
Province, China
Jing Wei
Shaanxi Provincial Center for Disease Control and Prevention
Shen Li
Shaanxi Provincial Center for Disease Control and Prevention
Jian-Hua Dong
Shaanxi Provincial Center for Disease Control and Prevention
Hui Tian
Baoji Center for Disease Control and Prevention
Gerardo Chowell
Georgia State University, gchowell@gsu.edu
See next page for additional authors
Follow this and additional works at: https://scholarworks.gsu.edu/iph_facpub
Part of the Public Health Commons
This Article is brought to you for free and open access by the School of Public Health at ScholarWorks @ Georgia State University. It has been accepted
for inclusion in Public Health Faculty Publications by an authorized administrator of ScholarWorks @ Georgia State University. For more information,
please contact scholarworks@gsu.edu.
Recommended Citation
J. Wei, S. Li, J. H. Dong, H. Tian, G. Chowell, H. Y. Tian, W. Lv, Z. Q. Han, B. Xu, P. B. Yu and J. J. Wang. The First Human Infection
with Severe Fever with Thrombocytopenia Syndrome Virus in Shaanxi Province, China. J Infect Dis, 35 37-9. doi: http://dx.doi.org/
10.1016/j.ijid.2015.02.014
Authors
Jing Wei, Shen Li, Jian-Hua Dong, Hui Tian, Gerardo Chowell, Huai-Yu Tian, Wen Lv, Zong-Qi Han, Bing Xu,
Peng-Bo Yu, and Jing-Jun Wang
This article is available at ScholarWorks @ Georgia State University: https://scholarworks.gsu.edu/iph_facpub/147
Short Communication
The ﬁrst human infection with severe fever with thrombocytopenia
syndrome virus in Shaanxi Province, China
Jing Wei a, Shen Li a, Jian-Hua Dong a, Hui Tian b, Gerardo Chowell c, Huai-Yu Tian d,
Wen Lv a, Zong-Qi Han e, Bing Xu d,f, Peng-Bo Yu a,1,*, Jing-Jun Wang a,1,*
a Shaanxi Provincial Center for Disease Control and Prevention, Xi’an, Shaanxi 710054, China
bBaoji Center for Disease Control and Prevention, Baoji, Shaanxi, China
c School of Public Health, Georgia State University, Atlanta, Georgia, USA
d State Key Laboratory of Remote Sensing Science, College of Global Change and Earth System Science, Beijing Normal University, Beijing, China
e Long County Center for Disease Control and Prevention of Shaanxi Province, Baoji, Shaanxi, China
fMinistry of Education Key Laboratory for Earth System Modeling, Center for Earth System Science, School of Environment, Tsinghua University, Beijing, China
1. Introduction
Severe fever with thrombocytopenia syndrome virus (SFTSV) is
a newly identiﬁed novel Phlebovirus of the Bunyaviridae family,1
which has been implicated as the causative agent of severe fever
with thrombocytopenia syndrome (SFTS) in China.2 The clinical
symptoms of SFTS are non-speciﬁc and include high fever,
gastrointestinal symptoms, thrombocytopenia, leukocytopenia,
multi-organ dysfunction, and hemorrhagic tendency.1 Most
reported SFTS cases have involved hospitalized patients with
relatively serious clinical symptoms, with an average case-fatality
rate of 12%.3 Fatal cases of infection with SFTSV have recently been
reported in South Korea and Japan as well.4,5 Haemaphysalis
longicornis ticks have been implicated as the vectors of SFTSV, and a
high seroprevalence of SFTSV has been reported in domestic
animals.1
The ﬁrst human case of SFTS in a rural area of Long County in
Shaanxi Province led to a seroprevalence study in the same village
where the ﬁrst case was detected, with the goal of estimating the
seroprevalence of SFTSV in this population.
2. Methods
2.1. Sample and data collection
We conducted a seroprevalence study in the village in Long
County where the ﬁrst case of SFTS was detected. A total of
363 serum samples were collected from 363 healthy volunteers. A
standardized questionnaire was used to collect information on
demographic characteristics including age, gender, and residential
address. The sampled population was divided into ﬁve age groups:
0–6, 7–19, 20–39, 40–59, and 60 years.
International Journal of Infectious Diseases 35 (2015) 37–39
A R T I C L E I N F O
Article history:
Received 19 December 2014
Received in revised form 15 January 2015
Accepted 18 February 2015
Corresponding Editor: Eskild Petersen,
Aarhus, Denmark
Keywords:
Severe fever with thrombocytopenia
syndrome
Prevalence
Bunyaviridae
Epidemiological characteristic
S U M M A R Y
Background: Severe fever with thrombocytopenia syndrome (SFTS) is an emerging infectious disease
discovered in China in 2009. In July 2013, the ﬁrst human infection with SFTS virus (SFTSV) was detected
in Shaanxi Province, Western China.
Methods: A seroprevalence study among humans was carried out in an SFTS endemic village;
speciﬁcally, serum samples were collected from 363 farmers in an SFTS endemic village in Shaanxi
Province. The presence of SFTSV antibodies in serum was determined using an ELISA.
Results: SFTSV antibodies were found in a total of 20 people (5.51%), with no signiﬁcant difference
between males and females (6.93% and 4.42%, respectively; Chi-square = 1.29, p = 0.25). Moreover, the
SFTSV antibody positive rate was not signiﬁcantly different across different age groups (Chi-
square = 2.23, p = 0.69).
Conclusions: SFTSV readily infects humans with outdoor exposure. The results of the serological study
indicate that the virus circulates widely in Shaanxi Province. SFTSV represents a public health threat in
China.
 2015 Published by Elsevier Ltd on behalf of International Society for Infectious Diseases. This is an open
access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
* Corresponding authors. Tel.: +86 029 82221026; fax: +86 029 82211952.
E-mail addresses: sxcdcy@21cn.com (P.-B. Yu), jingjunwang@china.com
(J.-J. Wang).
1 Jing Wei and Shen Li contributed equally to this article.
Contents lists available at ScienceDirect
International Journal of Infectious Diseases
jou r nal h o mep ag e: w ww .e lsev ier . co m / loc ate / i j id
http://dx.doi.org/10.1016/j.ijid.2015.02.014
1201-9712/ 2015 Published by Elsevier Ltd on behalf of International Society for Infectious Diseases. This is an open access article under the CC BY-NC-ND license (http://
creativecommons.org/licenses/by-nc-nd/4.0/).
Long County is located in Central China (Figure 1) and had a
population of a quarter million at the end of 2010. It has an annual
average temperature of 8–16 8C, and the average rainfall is
600 mm.
2.2. Serological testing
Samples were tested for the presence of SFTSV RNA by
quantitative real-time reverse transcription PCR (RT-PCR). Anti-
bodies (including IgG and IgM) in serum samples were detected
using a double-antigen sandwich ELISA, as described previously.6
Positive samples were further diluted to determine the antibody
titers.
2.3. Case deﬁnition
The patient was diagnosed based on the diagnosis and
treatment programs for severe fever with thrombocytopenia
syndrome issued by the Chinese Ministry of Health. The clinical
features include abrupt onset of fever (38 8C) and respiratory
tract or gastrointestinal symptoms, followed by a progressive
decline in platelets and white blood cells. A conﬁrmed case of SFTS
was deﬁned as a person who met these criteria and who also had at
least one of the following laboratory criteria for diagnosis: (1)
detection of SFTSV RNA by a molecular method, (2) seroconversion
or a 4-fold rise in antibody titers between two serum samples
collected at least 2 weeks apart, and (3) SFTSV isolated from clinical
specimens.
2.4. Statistical analyses
All statistical analyses were performed using SPSS 17.0 (SPSS
Inc., Chicago, IL, USA); the statistical signiﬁcance level was set at
0.05. The Chi-square test or Fisher’s exact test was used to assess
differences in SFTSV seroprevalence by gender and age group.
3. Results
The ﬁrst human case of SFTS in Shaanxi Province was a 66-year-
old man who had a sudden onset of fever on July 11, 2013, with a
temperature of 38 8C, accompanied by chills, pharyngeal pain,
nausea, vomiting, and abdominal pain. The patient’s family is
located in a rural area of Long County. The patient did not have a
history of outdoor activities before illness onset, and the patient’s
cattle had reportedly not been out of the village for the last 3 years.
Of the 363 volunteer participants, 173 (47.6%) were male and
190 (54.9%) were female. The ages of the participants ranged from
3 years to 80 years, and the median age was 42 years. A total of
363 serum samples were obtained from the healthy volunteers and
sent to the laboratory of Shaanxi Provincial Center for Disease
Figure 1. Location of Baoji in China and the location of selected districts where serum samples of healthy persons were collected and tested in 2013.
Table 1
Seropositivity for SFTSV among healthy humans in Shaanxi, China
Number of serum
samples tested
Number SFTSV-IgG
seropositive
Percentage
seropositive
Chi-square p-Value
Gender 1.29 0.25
Male 173 12 6.93
Female 190 8 4.42
Age, years 2.24 0.69
6 59 1 1.69
7–19 54 3 5.56
20–39 68 4 5.88
40–59 128 9 7.03
60 54 3 5.56
Total 363 20 5.51
SFTSV, severe fever with thrombocytopenia syndrome virus.
J. Wei et al. / International Journal of Infectious Diseases 35 (2015) 37–3938
Control and Prevention (CDC). Overall, 6% (20/363) of serum
samples were seropositive for SFTSV (6.93% among males and
4.21% among females). There was no statistically signiﬁcant
difference in seroprevalence between males and females (Chi-
square = 1.29, p = 0.25) (Table 1).
The sampled population was divided into ﬁve age groups (0–6,
7–19, 20–39, 40–59, and 60 years) and the corresponding
seroprevalence levels were 1.69% (1/59), 5.56% (3/54), 5.88% (4/
68), 7.03% (9/128), and 5.56% (3/54), respectively. Statistical
analyses showed that the seroprevalence of antibodies against the
virus did not increase with age (Table 1). None of the seropositive
participants reported any of the disease symptoms that are
associated with SFTSV infections.
4. Discussion
We found an SFTSV seroprevalence level of 5.51% in an SFTS
endemic village, which is similar to that reported in Hubei Province
(6.37%) and Zhejiang Province (5.51%), but much higher than that
reported in Shandong Province (0.84%) and Jiangsu Province
(0.94%).7–9 This discrepancy may be attributed to the season of
sample collection, age and sex of the subjects, previous exposure or
low level of infection, or differences in detection methods
employed in different studies. Furthermore, the seropositive
volunteers in our study had not had contact with the ﬁrst reported
patient before onset, which suggests that other infections in the
village may have resulted from natural exposure to a reservoir.
There was no statistical difference observed by sex, indicating
that men and women in rural areas of Shaanxi are equally exposed
to SFTSV; this is in line with the results of a prior study conducted
in Jiangsu Province, China in 2011.10 However, surveillance data
from 2012 and 2013 in Jiangsu Province have indicated that SFTSV
antibodies are more prevalent in males than in females.11 Further
studies are needed to clarify this difference.
Our study demonstrated that seroprevalence varied with age.
Speciﬁcally, there were signiﬁcant differences among studied age
groups for SFTSV infection. The incidence rate of SFTS was higher in
patients between 20 and 60 years of age compared to patients aged
<20 years. This suggests that the older age groups have
participated in long-term outdoor activities more than the other
age groups. However, the seroprevalence of SFTSV in healthy
people was not signiﬁcantly different among age groups in
Shandong Province, although SFTS patients were mainly elderly.12
In conclusion, our study indicates signiﬁcant levels of SFTSV
antibodies among healthy humans, which suggests subclinical
SFTSV infections or a relatively mild form of SFTS illness. More
emphasis is needed on this novel disease, including enhanced
surveillance activities related to the virus in ticks and domestic
animals.
Acknowledgements
This work was supported by the Chinese National Science and
Technology Major Project (grant number 2013ZX10004202), the
Shaanxi Provincial Department of Science and Technology (grant
numbers 2013K12-04-02), and the National Research Program of
the Ministry of Science and Technology, China (grant numbers
2012CB955501, 2012AA12A407, 2013AA122003).
Ethical statement: The study was approved by the ethics review
committee of Shaanxi Provincial Center for Disease Control and
Prevention. The sera were collected with the consent of the
volunteers.
Conﬂict of interest: None for all authors.
References
1. Yu XJ, Liang MF, Zhang SY, Liu Y, Li JD, Sun YL, et al. Fever with thrombocyto-
penia associated with a novel bunyavirus in China. N Engl J Med
2011;364:1523–32.
2. Chen H, Hu K, Zou J, Xiao J. A cluster of cases of human-to-human transmission
caused by severe fever with thrombocytopenia syndrome bunyavirus. Int J
Infect Dis 2013;17:e206–8.
3. Zhang YZ, He YW, Dai YA, Xiong YE, Zheng H, Zhou DJ, et al. Hemorrhagic fever
caused by a novel bunyavirus in China: pathogenesis and correlates of fatal
outcome. Clin Infect Dis 2012;54:527–53.
4. Takahashi T, Maeda K, Suzuki T, Ishido A, Shigeoka T, Tominaga T, et al. The ﬁrst
identiﬁcation and retrospective study of severe fever with thrombocytopenia
syndrome in Japan. J Infect Dis 2014;209:816–27.
5. Kim KH, Yi J, Kim G, Choi SJ, Jun KI, Kim NH, et al. Severe fever with thrombo-
cytopenia syndrome, South Korea, 2012. Emerg Infect Dis 2013;19:1892–4.
6. Sun J, Chai C, Lv H, Lin J, Wang C, Chen E, et al. Epidemiological characteristics of
severe fever with thrombocytopenia syndrome in Zhejiang Province, China. Int J
Infect Dis 2014;25:180–5.
7. Zhan J, Huo X, Guan X, Jiang Y, Xu J, Li G, et al. Analysis on antibody levels against
severe fever with thrombocytopenia syndrome bunyavirus among healthy
population in Hubei Province. Chinese Journal of Health Laboratory Technology
2013;23:922–3.
8. Zhang WS, Zeng XY, Zhou MH, Jiao YJ, Wen T, Guo XL, et al. Seroepidemiology of
severe fever with thrombocytopenia syndrome bunyavirus in Jiansu Province.
(In Chinese) Dis Surveill 2011;26:676–8.
9. Zhao L, Zhai S, Wen H, Cui F, Chi Y, Wang L, et al. Severe fever with thrombocy-
topenia syndrome virus, Shandong Province, China. Emerg Infect Dis
2012;18:963–5.
10. Liang S, Bao C, Zhou M, Hu J, Tang F, Guo X, et al. Seroprevalence and risk factors
for severe fever with thrombocytopenia syndrome virus infection in Jiangsu
Province, China, 2011. Am J Trop Med Hyg 2014;90:256–9.
11. Li Z, Hu J, Bao C, Li P, Qi X, Qin Y, et al. Seroprevalence of antibodies against SFTS
virus infection in farmers and animals, Jiangsu. China J Clin Virol 2014;60:185–9.
12. Ding S, Niu G, Xu X, Li J, Zhang X, Yin H, et al. Age is a critical risk factor for severe
fever with thrombocytopenia syndrome. PLoS One 2014;9:e111736.
J. Wei et al. / International Journal of Infectious Diseases 35 (2015) 37–39 39


SummaryBackgroundSevere fever with thrombocytopenia syndrome (SFTS) is an emerging infectious disease discovered in China in 2009. In July 2013, the first human infection with SFTS virus (SFTSV) was detected in Shaanxi Province, Western China.MethodsA seroprevalence study among humans was carried out in an SFTS endemic village; specifically, serum samples were collected from 363 farmers in an SFTS endemic village in Shaanxi Province. The presence of SFTSV antibodies in serum was determined using an ELISA.ResultsSFTSV antibodies were found in a total of 20 people (5.51%), with no significant difference between males and females (6.93% and 4.42%, respectively; Chi-square=1.29, p=0.25). Moreover, the SFTSV antibody positive rate was not significantly different across different age groups (Chi-square=2.23, p=0.69).ConclusionsSFTSV readily infects humans with outdoor exposure. The results of the serological study indicate that the virus circulates widely in Shaanxi Province. SFTSV represents a public health threat in China

Elsevier - Publisher Connector 

International Journal of Infectious Diseases 35 (2015) 37–39Short Communication
The ﬁrst human infection with severe fever with thrombocytopenia
syndrome virus in Shaanxi Province, China
Jing Wei a, Shen Li a, Jian-Hua Dong a, Hui Tian b, Gerardo Chowell c, Huai-Yu Tian d,
Wen Lv a, Zong-Qi Han e, Bing Xu d,f, Peng-Bo Yu a,1,*, Jing-Jun Wang a,1,*
a Shaanxi Provincial Center for Disease Control and Prevention, Xi’an, Shaanxi 710054, China
bBaoji Center for Disease Control and Prevention, Baoji, Shaanxi, China
c School of Public Health, Georgia State University, Atlanta, Georgia, USA
d State Key Laboratory of Remote Sensing Science, College of Global Change and Earth System Science, Beijing Normal University, Beijing, China
e Long County Center for Disease Control and Prevention of Shaanxi Province, Baoji, Shaanxi, China
fMinistry of Education Key Laboratory for Earth System Modeling, Center for Earth System Science, School of Environment, Tsinghua University, Beijing, China
A R T I C L E I N F O
Article history:
Received 19 December 2014
Received in revised form 15 January 2015
Accepted 18 February 2015
Corresponding Editor: Eskild Petersen,
Aarhus, Denmark
Keywords:
Severe fever with thrombocytopenia
syndrome
Prevalence
Bunyaviridae
Epidemiological characteristic
S U M M A R Y
Background: Severe fever with thrombocytopenia syndrome (SFTS) is an emerging infectious disease
discovered in China in 2009. In July 2013, the ﬁrst human infection with SFTS virus (SFTSV) was detected
in Shaanxi Province, Western China.
Methods: A seroprevalence study among humans was carried out in an SFTS endemic village;
speciﬁcally, serum samples were collected from 363 farmers in an SFTS endemic village in Shaanxi
Province. The presence of SFTSV antibodies in serum was determined using an ELISA.
Results: SFTSV antibodies were found in a total of 20 people (5.51%), with no signiﬁcant difference
between males and females (6.93% and 4.42%, respectively; Chi-square = 1.29, p = 0.25). Moreover, the
SFTSV antibody positive rate was not signiﬁcantly different across different age groups (Chi-
square = 2.23, p = 0.69).
Conclusions: SFTSV readily infects humans with outdoor exposure. The results of the serological study
indicate that the virus circulates widely in Shaanxi Province. SFTSV represents a public health threat in
China.
 2015 Published by Elsevier Ltd on behalf of International Society for Infectious Diseases. This is an open
access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Contents lists available at ScienceDirect
International Journal of Infectious Diseases
jou r nal h o mep ag e: w ww .e lsev ier . co m / loc ate / i j id1. Introduction
Severe fever with thrombocytopenia syndrome virus (SFTSV) is
a newly identiﬁed novel Phlebovirus of the Bunyaviridae family,1
which has been implicated as the causative agent of severe fever
with thrombocytopenia syndrome (SFTS) in China.2 The clinical
symptoms of SFTS are non-speciﬁc and include high fever,
gastrointestinal symptoms, thrombocytopenia, leukocytopenia,
multi-organ dysfunction, and hemorrhagic tendency.1 Most
reported SFTS cases have involved hospitalized patients with
relatively serious clinical symptoms, with an average case-fatality
rate of 12%.3 Fatal cases of infection with SFTSV have recently been
reported in South Korea and Japan as well.4,5 Haemaphysalis* Corresponding authors. Tel.: +86 029 82221026; fax: +86 029 82211952.
E-mail addresses: sxcdcy@21cn.com (P.-B. Yu), jingjunwang@china.com
(J.-J. Wang).
1 Jing Wei and Shen Li contributed equally to this article.
http://dx.doi.org/10.1016/j.ijid.2015.02.014
1201-9712/ 2015 Published by Elsevier Ltd on behalf of International Society for Infect
creativecommons.org/licenses/by-nc-nd/4.0/).longicornis ticks have been implicated as the vectors of SFTSV, and a
high seroprevalence of SFTSV has been reported in domestic
animals.1
The ﬁrst human case of SFTS in a rural area of Long County in
Shaanxi Province led to a seroprevalence study in the same village
where the ﬁrst case was detected, with the goal of estimating the
seroprevalence of SFTSV in this population.
2. Methods
2.1. Sample and data collection
We conducted a seroprevalence study in the village in Long
County where the ﬁrst case of SFTS was detected. A total of
363 serum samples were collected from 363 healthy volunteers. A
standardized questionnaire was used to collect information on
demographic characteristics including age, gender, and residential
address. The sampled population was divided into ﬁve age groups:
0–6, 7–19, 20–39, 40–59, and 60 years.ious Diseases. This is an open access article under the CC BY-NC-ND license (http://
Figure 1. Location of Baoji in China and the location of selected districts where serum samples of healthy persons were collected and tested in 2013.
J. Wei et al. / International Journal of Infectious Diseases 35 (2015) 37–3938Long County is located in Central China (Figure 1) and had a
population of a quarter million at the end of 2010. It has an annual
average temperature of 8–16 8C, and the average rainfall is
600 mm.
2.2. Serological testing
Samples were tested for the presence of SFTSV RNA by
quantitative real-time reverse transcription PCR (RT-PCR). Anti-
bodies (including IgG and IgM) in serum samples were detected
using a double-antigen sandwich ELISA, as described previously.6
Positive samples were further diluted to determine the antibody
titers.
2.3. Case deﬁnition
The patient was diagnosed based on the diagnosis and
treatment programs for severe fever with thrombocytopenia
syndrome issued by the Chinese Ministry of Health. The clinical
features include abrupt onset of fever (38 8C) and respiratory
tract or gastrointestinal symptoms, followed by a progressive
decline in platelets and white blood cells. A conﬁrmed case of SFTS
was deﬁned as a person who met these criteria and who also had at
least one of the following laboratory criteria for diagnosis: (1)
detection of SFTSV RNA by a molecular method, (2) seroconversionTable 1
Seropositivity for SFTSV among healthy humans in Shaanxi, China
Number of serum
samples tested
Number SFTSV-IgG
seropositive
Gender 
Male 173 12 
Female 190 8 
Age, years 
6 59 1 
7–19 54 3 
20–39 68 4 
40–59 128 9 
60 54 3 
Total 363 20 
SFTSV, severe fever with thrombocytopenia syndrome virus.or a 4-fold rise in antibody titers between two serum samples
collected at least 2 weeks apart, and (3) SFTSV isolated from clinical
specimens.
2.4. Statistical analyses
All statistical analyses were performed using SPSS 17.0 (SPSS
Inc., Chicago, IL, USA); the statistical signiﬁcance level was set at
0.05. The Chi-square test or Fisher’s exact test was used to assess
differences in SFTSV seroprevalence by gender and age group.
3. Results
The ﬁrst human case of SFTS in Shaanxi Province was a 66-year-
old man who had a sudden onset of fever on July 11, 2013, with a
temperature of 38 8C, accompanied by chills, pharyngeal pain,
nausea, vomiting, and abdominal pain. The patient’s family is
located in a rural area of Long County. The patient did not have a
history of outdoor activities before illness onset, and the patient’s
cattle had reportedly not been out of the village for the last 3 years.
Of the 363 volunteer participants, 173 (47.6%) were male and
190 (54.9%) were female. The ages of the participants ranged from
3 years to 80 years, and the median age was 42 years. A total of
363 serum samples were obtained from the healthy volunteers and
sent to the laboratory of Shaanxi Provincial Center for DiseasePercentage
seropositive
Chi-square p-Value
1.29 0.25
6.93
4.42
2.24 0.69
1.69
5.56
5.88
7.03
5.56
5.51
J. Wei et al. / International Journal of Infectious Diseases 35 (2015) 37–39 39Control and Prevention (CDC). Overall, 6% (20/363) of serum
samples were seropositive for SFTSV (6.93% among males and
4.21% among females). There was no statistically signiﬁcant
difference in seroprevalence between males and females (Chi-
square = 1.29, p = 0.25) (Table 1).
The sampled population was divided into ﬁve age groups (0–6,
7–19, 20–39, 40–59, and 60 years) and the corresponding
seroprevalence levels were 1.69% (1/59), 5.56% (3/54), 5.88% (4/
68), 7.03% (9/128), and 5.56% (3/54), respectively. Statistical
analyses showed that the seroprevalence of antibodies against the
virus did not increase with age (Table 1). None of the seropositive
participants reported any of the disease symptoms that are
associated with SFTSV infections.
4. Discussion
We found an SFTSV seroprevalence level of 5.51% in an SFTS
endemic village, which is similar to that reported in Hubei Province
(6.37%) and Zhejiang Province (5.51%), but much higher than that
reported in Shandong Province (0.84%) and Jiangsu Province
(0.94%).7–9 This discrepancy may be attributed to the season of
sample collection, age and sex of the subjects, previous exposure or
low level of infection, or differences in detection methods
employed in different studies. Furthermore, the seropositive
volunteers in our study had not had contact with the ﬁrst reported
patient before onset, which suggests that other infections in the
village may have resulted from natural exposure to a reservoir.
There was no statistical difference observed by sex, indicating
that men and women in rural areas of Shaanxi are equally exposed
to SFTSV; this is in line with the results of a prior study conducted
in Jiangsu Province, China in 2011.10 However, surveillance data
from 2012 and 2013 in Jiangsu Province have indicated that SFTSV
antibodies are more prevalent in males than in females.11 Further
studies are needed to clarify this difference.
Our study demonstrated that seroprevalence varied with age.
Speciﬁcally, there were signiﬁcant differences among studied age
groups for SFTSV infection. The incidence rate of SFTS was higher in
patients between 20 and 60 years of age compared to patients aged
<20 years. This suggests that the older age groups have
participated in long-term outdoor activities more than the other
age groups. However, the seroprevalence of SFTSV in healthy
people was not signiﬁcantly different among age groups in
Shandong Province, although SFTS patients were mainly elderly.12
In conclusion, our study indicates signiﬁcant levels of SFTSV
antibodies among healthy humans, which suggests subclinical
SFTSV infections or a relatively mild form of SFTS illness. Moreemphasis is needed on this novel disease, including enhanced
surveillance activities related to the virus in ticks and domestic
animals.
Acknowledgements
This work was supported by the Chinese National Science and
Technology Major Project (grant number 2013ZX10004202), the
Shaanxi Provincial Department of Science and Technology (grant
numbers 2013K12-04-02), and the National Research Program of
the Ministry of Science and Technology, China (grant numbers
2012CB955501, 2012AA12A407, 2013AA122003).
Ethical statement: The study was approved by the ethics review
committee of Shaanxi Provincial Center for Disease Control and
Prevention. The sera were collected with the consent of the
volunteers.
Conﬂict of interest: None for all authors.
References
1. Yu XJ, Liang MF, Zhang SY, Liu Y, Li JD, Sun YL, et al. Fever with thrombocyto-
penia associated with a novel bunyavirus in China. N Engl J Med
2011;364:1523–32.
2. Chen H, Hu K, Zou J, Xiao J. A cluster of cases of human-to-human transmission
caused by severe fever with thrombocytopenia syndrome bunyavirus. Int J
Infect Dis 2013;17:e206–8.
3. Zhang YZ, He YW, Dai YA, Xiong YE, Zheng H, Zhou DJ, et al. Hemorrhagic fever
caused by a novel bunyavirus in China: pathogenesis and correlates of fatal
outcome. Clin Infect Dis 2012;54:527–53.
4. Takahashi T, Maeda K, Suzuki T, Ishido A, Shigeoka T, Tominaga T, et al. The ﬁrst
identiﬁcation and retrospective study of severe fever with thrombocytopenia
syndrome in Japan. J Infect Dis 2014;209:816–27.
5. Kim KH, Yi J, Kim G, Choi SJ, Jun KI, Kim NH, et al. Severe fever with thrombo-
cytopenia syndrome, South Korea, 2012. Emerg Infect Dis 2013;19:1892–4.
6. Sun J, Chai C, Lv H, Lin J, Wang C, Chen E, et al. Epidemiological characteristics of
severe fever with thrombocytopenia syndrome in Zhejiang Province, China. Int J
Infect Dis 2014;25:180–5.
7. Zhan J, Huo X, Guan X, Jiang Y, Xu J, Li G, et al. Analysis on antibody levels against
severe fever with thrombocytopenia syndrome bunyavirus among healthy
population in Hubei Province. Chinese Journal of Health Laboratory Technology
2013;23:922–3.
8. Zhang WS, Zeng XY, Zhou MH, Jiao YJ, Wen T, Guo XL, et al. Seroepidemiology of
severe fever with thrombocytopenia syndrome bunyavirus in Jiansu Province.
(In Chinese) Dis Surveill 2011;26:676–8.
9. Zhao L, Zhai S, Wen H, Cui F, Chi Y, Wang L, et al. Severe fever with thrombocy-
topenia syndrome virus, Shandong Province, China. Emerg Infect Dis
2012;18:963–5.
10. Liang S, Bao C, Zhou M, Hu J, Tang F, Guo X, et al. Seroprevalence and risk factors
for severe fever with thrombocytopenia syndrome virus infection in Jiangsu
Province, China, 2011. Am J Trop Med Hyg 2014;90:256–9.
11. Li Z, Hu J, Bao C, Li P, Qi X, Qin Y, et al. Seroprevalence of antibodies against SFTS
virus infection in farmers and animals, Jiangsu. China J Clin Virol 2014;60:185–9.
12. Ding S, Niu G, Xu X, Li J, Zhang X, Yin H, et al. Age is a critical risk factor for severe
fever with thrombocytopenia syndrome. PLoS One 2014;9:e111736.


The first human infection with severe fever with thrombocytopenia syndrome virus in Shaanxi Province, China 

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The First Human Infection with Severe Fever with Thrombocytopenia Syndrome Virus in Shaanxi Province, China

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