| Background The Bunyavirales is the largest RNA virus order,comprised of more than 560 viruses divided into twelve families,among which most members could infect humans and animals,thus posing great potential threat to public health.In China,investigations were focused on the spatial distribution and ecological niches of Hemorrhagic fever with renal syndrome(HFRS)and Severe fever with thrombocytopenia syndrome(SFTS),two of the most severe Bunyavirales-related infectious diseases,while little attention is paid to the other diseases caused by Bunyavirales pathogens.Crimean-Congo hemorrhagic fever(CCHF),also known as Xinjiang hemorrhagic fever(XHF)in China,first occurred in 1965 in Xinjiang Autonomous Region,with 10 deaths of the 11 infected patients.This disease had a short incubation period,rapid onset and high fatality;therefore,it came into the view of researchers.However,few studies about the risk of CCHF occurrence have shown inconsistent picture,that a study showed high risks in Xinjiang,northwestern China and areas in the southwest border,while another study showed that the high risk was located in the central region.Besides,an imported case of Rift Valley fever(RVF),another infectious disease related to Bunyavirales mainly distributed in Africa and expanding to Arabian Peninsula,was first identified in Beijing in 2016.With frequent international travel and the global climate change,China have possessed almost all the transmission conditions of Rift Valley fever virus(RVFV),which suggests the necessity for surveillance and risk assessment of RVFV invasion and indigenous transmission.Owing to the increasing varieties and epidemic of Bunyavirales pathogens,a systematic understanding of nation-wide distributions,epidemiological characteristics,and ecological niches of Bunyavirales pathogens is still lacking.Such an understanding is needed for developing diagnostic and treatment guidelines and control programs.Objective(1)To present a systematic review on the spatiotemporal trends and map distributions of the order Bunyavirales pathogens detected from vectors,animals and humans in China;(2)To assess the contributions of relevant environmental,ecoclimatic and biological factors to the environmental suitability of two important viral pathogens belonging to the order Bunyavirales,including Crimean-Congo hemorrhagic fever virus(CCHFV)and RVFV,and map the model-projected risks,which can help to guide future surveillance and control of the viruses from an ecological perspective.Methods The database of the order Bunyavirales pathogens occurrence in China was collected from a variety of sources,including(1)the report data of human confirmed SFTS cases(2010-2020)and HFRS cases(1997-2020)from China Information System for Disease Control and Prevention(CISDCP),(2)literature reporting the occurrence of Bunyavirales pathogens,published between January,1951 and June,2021,(3)unpublished Bunyavirales pathogens data from the Gen Bank database.A standardized form was used to collate data on the following variables: year of publication,study year,study subjects,laboratory method used to identify viral pathogens belonging to the order Bunyavirales,the number of samples tested and positive case,geo-referenced study sites,and the baseline information on the study subjects.The distribution of Bunyavirales pathogens was summarized and mapped at the city level if data were available or at province level otherwise,including the overall numbers of human confirmed cases,the overall positive rate of humans with serological evidence,and the distribution of vectors and animals(livestock and wild animals).In addition,the matrix diagram of these Bunyavirales pathogens and their infected vectors and animal hosts were drawn.The occurrence records of CCHFV were extracted from the database of Bunyavirales pathogens in China.The boosted regression tree(BRT)models were used to examine environmental suitability of CCHFV occurrence at the 10 km×10 km pixel level in China.The probability maps of CCHFV occurrence was converted into a binary map(high risk or low risk)by using the cut-off values at which the Youden index of the test set was maximum as the threshold,and based on that,the area and population at risk for CCHFV were calculated.Meanwhile,the relative contribution of each variable in the model was calculated,and the main influencing variables of CCHFV was analyzed.Another database of RVFV occurrence in RVF endemic areas(Africa and the Arabian Peninsula)was supplemented from Global Animal Disease Information System(EMPRES-i)database and literatures.The native presence/absence niche model with occurrence records and explanatory covariates extracted from RVFV endemic area(Africa and the Arabian Peninsula)was established,making projection using explanatory covariates from China to examine the environmental suitability if RVFV invasion to an as-yet uninvaded area.Meanwhile,the imported risk index per city in China was measured as the possibility of importing population at risk from the infected countries in RVFV endemic area,accounting for the volume of air travel from airports originated from such countries and for their population at risk.Finally,the occurrence risk and imported risk of RVFV were combined to evaluate the comprehensive risk of RVFV in China.ResultsEighty-nine viral species belonging to the order Bunyavirales were reported in China from January 1951 to June 2021,and the highest richness of viruses occurred in Hubei province,followed by Zhejiang province,Yunnan province and Xinjiang Autonomous Region.In total,19 viruses belonging to five families were identified to cause human infections,and a total of 447,848 cases infected with Bunyavirales pathogens were reported and hantavirus,Dabie bandavirus and Crimean-Congo hemorrhagic fever virus(CCHFV)had the severest disease burden.There also significant differences in the types of viruses carried by different vectors,among which Nairoviridae and Phenuiviridae were mainly carried by ticks,Peribunyaviridae mainly carried by mosquitoes,and Hantaviridae and Arenaviridae mainly carried by Rodentia.Meanwhile,Bunyavirales viruses carried by ticks were not found in mosquitoes,and the converse was also true.Compared with mosquitoes and rodents which were widely distributed in China,there was noticeable geographic cluster for ticks carrying Bunyavirales viruses,especially in northeastern China,Xinjiang and Shandong provinces.Model-predicted high-risk areas for CCHFV occurrence were mainly distributed in Xinjiang Autonomous Region,with more focalized areas at high risk in south-west border area of Yunnan province.The probability of CCHFV presence to be particularly determined by the distribution of Hyalomma asiaticum tick,contributing 68.6% to the distribution of CCHFV in the model.The model-predicted high-risk areas of CCHFV presence were more extensive than those have been recorded,with the area at risk increased from 2,700 km2 to 1,305,500 km2 and the population size at risk increased from 0.3 million to 135.1 million people.The BRT model predicted that spatial and temporal variation was evident in the frequency of risk in China.In terms of spatial distribution,the south was more suitable than the north,and the east was more suitable than the west.However,northern Xinjiang and areas centered around eastern Inner Mongolia and stretched over Shanxi,Shaanxi and Ningxia showed more suitability from July to September.Our models showed higher livestock density and more precipitation in previous month were the two most important risk factors,respectively contributing 21.6% and 21.2% to the model.Meanwhile,the imported risk of RVFV results showed that Guangzhou,Beijing and Shanghai were the cities with the highest imported risk,and seven cities including Urumqi were the cities with medium imported risk.The travelers from Egypt,South Africa,Saudi Arabia and Kenya,in where there was high risk for its importing to China.Comprehensively assessing the occurrence and imported risk of RVFV,we found that the environmental suitability of RVFV transmission,as well as the risk of imported cases,were always high in Guangzhou city all year round.The same situation should also be paid attention to in Beijing,Shanghai and southern Xinjiang only in summer from June to September.Conclusion Based on the established database,the distribution of 89 species of Bunyavirales viruses in China from January 1951 to June 2021 were defined,among which hantavirus,Dabie bandavirus and CCHFV had the severest disease burden,suggesting the importance of the monitoring of HFRS,SFTS and CCHF high-risk groups.It was necessary to establish a rapid response mechanism for taking treatment measures in time after the patients were diagnosed.Meanwhile,the high richness of viruses of the order Bunyavirales were mainly distributed in Hubei,Zhejiang,Yunnan and Xinjiang,suggesting that distributions of pathogens had an overall correlation with the ecogeographical faunal region for specific vectors because the abundance of tick species or mosquito species in these areas was also in the forefront.Ticks and mosquitoes were the vectors carrying the highest variety of viruses,so it was important to focus on the hotspot of ticks and mosquitoes in China and strengthen the monitoring of ticks,mosquitoes,tick-borne and mosquitoe-borne Bunyavirales viruses.The ecological niche models show that Xinjiang and southwestern Yunnan had high environmental suitability for CCHFV,mainly depended on the probability of Hyalomma asiaticum presence,while southern China had the highest environmental suitability for RVFV transmission throughout the whole year when its importance,mainly depended on the higher livestock density and more mean precipitation in previous month.Meanwhile,the travelers from Egypt,South Africa,Saudi Arabia and Kenya,in where there was high risk for its importing to China,should also be closely monitored.Our study can help to promote the understanding of risk distribution and disease burden of Bunyavirales pathogens in China,and inform targeted surveillance and control of them at predicted high-risk areas. |
