Publications by authors named "Huaiyu Tian"

48 Publications

Modelling COVID-19.

Nat Rev Phys 2020 May 6:1-3. Epub 2020 May 6.

WHO Collaborating Centre for Infectious Disease Epidemiology and Control, School of Public Health, LKS Faculty of Medicine, The University of Hong Kong, Hong Kong SAR, China.

As the COVID-19 pandemic continues, mathematical epidemiologists share their views on what models reveal about how the disease has spread, the current state of play and what work still needs to be done.
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http://dx.doi.org/10.1038/s42254-020-0178-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7201389PMC
May 2020

A follow-up study shows that recovered patients with re-positive PCR test in Wuhan may not be infectious.

BMC Med 2021 03 15;19(1):77. Epub 2021 Mar 15.

State Key Laboratory of Remote Sensing Science, Center for Global Change and Public Health, College of Global Change and Earth System Science, Beijing Normal University, Beijing, China.

Background: Previous studies showed that recovered coronavirus disease 2019 (COVID-19) patients can have a subsequent positive polymerase chain reaction (PCR) test for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) after they are discharged from the hospital. Understanding the epidemiological characteristics of recovered COVID-19 patients who have a re-positive test is vital for preventing a second wave of COVID-19.

Methods: This retrospective study analyzed the epidemiological and clinical features of 20,280 COVID-19 patients from multiple centers in Wuhan who had a positive PCR test between December 31, 2019, and August 4, 2020. The RT-PCR test results for 4079 individuals who had close contact with the re-positive cases were also obtained.

Results: In total, 2466 (12.16%) of the 20,280 patients had a re-positive SARS-CoV-2 PCR test after they were discharged from the hospital, and 4079 individuals had close contact with members of this patient group. All of these 4079 individuals had a negative SARS-CoV-2 PCR test.

Conclusions: This retrospective study in Wuhan analyzed the basic characteristics of recovered COVID-19 patients with re-positive PCR test and found that these cases may not be infectious.
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http://dx.doi.org/10.1186/s12916-021-01954-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7956402PMC
March 2021

Association between coronavirus disease 2019 (COVID-19) and long-term exposure to air pollution: Evidence from the first epidemic wave in China.

Environ Pollut 2021 May 8;276:116682. Epub 2021 Feb 8.

Department of Occupational and Environmental Health Sciences, School of Public Health, Peking University, China. Electronic address:

People with chronic obstructive pulmonary disease, cardiovascular disease, or hypertension have a high risk of developing severe coronavirus disease 2019 (COVID-19) and of COVID-19 mortality. However, the association between long-term exposure to air pollutants, which increases cardiopulmonary damage, and vulnerability to COVID-19 has not yet been fully established. We collected data of confirmed COVID-19 cases during the first wave of the epidemic in mainland China. We fitted a generalized linear model using city-level COVID-19 cases and severe cases as the outcome, and long-term average air pollutant levels as the exposure. Our analysis was adjusted using several variables, including a mobile phone dataset, covering human movement from Wuhan before the travel ban and movements within each city during the period of the emergency response. Other variables included smoking prevalence, climate data, socioeconomic data, education level, and number of hospital beds for 324 cities in China. After adjusting for human mobility and socioeconomic factors, we found an increase of 37.8% (95% confidence interval [CI]: 23.8%-52.0%), 32.3% (95% CI: 22.5%-42.4%), and 14.2% (7.9%-20.5%) in the number of COVID-19 cases for every 10-μg/m increase in long-term exposure to NO, PM, and PM, respectively. However, when stratifying the data according to population size, the association became non-significant. The present results are derived from a large, newly compiled and geocoded repository of population and epidemiological data relevant to COVID-19. The findings suggested that air pollution may be related to population vulnerability to COVID-19 infection, although the extent to which this relationship is confounded by city population density needs further exploration.
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http://dx.doi.org/10.1016/j.envpol.2021.116682DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7868737PMC
May 2021

Population serology for SARS-CoV-2 is essential to regional and global preparedness.

Lancet Microbe 2020 Jul 3;1(3):e94. Epub 2020 Jun 3.

Center for Infectious Disease Dynamics, Department of Biology, Pennsylvania State University, University Park, PA 16802, USA.

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http://dx.doi.org/10.1016/S2666-5247(20)30055-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7832696PMC
July 2020

Crowding and the shape of COVID-19 epidemics.

Nat Med 2020 12 5;26(12):1829-1834. Epub 2020 Oct 5.

Department of Zoology, University of Oxford, Oxford, UK.

The coronavirus disease 2019 (COVID-19) pandemic is straining public health systems worldwide, and major non-pharmaceutical interventions have been implemented to slow its spread. During the initial phase of the outbreak, dissemination of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) was primarily determined by human mobility from Wuhan, China. Yet empirical evidence on the effect of key geographic factors on local epidemic transmission is lacking. In this study, we analyzed highly resolved spatial variables in cities, together with case count data, to investigate the role of climate, urbanization and variation in interventions. We show that the degree to which cases of COVID-19 are compressed into a short period of time (peakedness of the epidemic) is strongly shaped by population aggregation and heterogeneity, such that epidemics in crowded cities are more spread over time, and crowded cities have larger total attack rates than less populated cities. Observed differences in the peakedness of epidemics are consistent with a meta-population model of COVID-19 that explicitly accounts for spatial hierarchies. We paired our estimates with globally comprehensive data on human mobility and predict that crowded cities worldwide could experience more prolonged epidemics.
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http://dx.doi.org/10.1038/s41591-020-1104-0DOI Listing
December 2020

The effect of human mobility and control measures on the COVID-19 epidemic in China.

medRxiv 2020 Mar 6. Epub 2020 Mar 6.

Network Science Institute, Northeastern University, Boston, United States.

The ongoing COVID-19 outbreak has expanded rapidly throughout China. Major behavioral, clinical, and state interventions are underway currently to mitigate the epidemic and prevent the persistence of the virus in human populations in China and worldwide. It remains unclear how these unprecedented interventions, including travel restrictions, have affected COVID-19 spread in China. We use real-time mobility data from Wuhan and detailed case data including travel history to elucidate the role of case importation on transmission in cities across China and ascertain the impact of control measures. Early on, the spatial distribution of COVID-19 cases in China was well explained by human mobility data. Following the implementation of control measures, this correlation dropped and growth rates became negative in most locations, although shifts in the demographics of reported cases are still indicative of local chains of transmission outside Wuhan. This study shows that the drastic control measures implemented in China have substantially mitigated the spread of COVID-19.
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http://dx.doi.org/10.1101/2020.03.02.20026708DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7239080PMC
March 2020

The impact of anthropogenic and environmental factors on human rabies cases in China.

Transbound Emerg Dis 2020 Nov 21;67(6):2544-2553. Epub 2020 May 21.

State Key Laboratory of Remote Sensing Science, College of Global Change and Earth System Science, Beijing Normal University, Beijing, China.

Human rabies is a public health problem in Asia, especially in less-developed regions where the disease is under-reported because of a lack of epidemiological surveillance. To address this gap, we collected data on human rabies in Yunnan Province, China, between 2005 and 2016. Using statistical mapping techniques, we correlated the occurrence of human rabies to environmental (elevation, precipitation, normalized difference vegetation index [NDVI], temperature and distance to the nearest main rivers) and anthropogenic (human and dog population density, distance to the nearest main roads and gross domestic product [GDP]) factors. We used a performance score, the average area under the receiver operator characteristic curve (0.88), to validate our risk model. Using this model, we found that environmental factors were more strongly associated with human rabies occurrence than anthropogenic factors. Areas with elevation below 2000 metres, GDP per capita between $750 and $4500/year and NDVI below 0.07 were associated with greater risk of human rabies. Rabies control in China should specifically target these areas.
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http://dx.doi.org/10.1111/tbed.13600DOI Listing
November 2020

An investigation of transmission control measures during the first 50 days of the COVID-19 epidemic in China.

Science 2020 05 31;368(6491):638-642. Epub 2020 Mar 31.

Department of Zoology, University of Oxford, Oxford, UK.

Responding to an outbreak of a novel coronavirus [agent of coronavirus disease 2019 (COVID-19)] in December 2019, China banned travel to and from Wuhan city on 23 January 2020 and implemented a national emergency response. We investigated the spread and control of COVID-19 using a data set that included case reports, human movement, and public health interventions. The Wuhan shutdown was associated with the delayed arrival of COVID-19 in other cities by 2.91 days. Cities that implemented control measures preemptively reported fewer cases on average (13.0) in the first week of their outbreaks compared with cities that started control later (20.6). Suspending intracity public transport, closing entertainment venues, and banning public gatherings were associated with reductions in case incidence. The national emergency response appears to have delayed the growth and limited the size of the COVID-19 epidemic in China, averting hundreds of thousands of cases by 19 February (day 50).
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http://dx.doi.org/10.1126/science.abb6105DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7164389PMC
May 2020

The effect of human mobility and control measures on the COVID-19 epidemic in China.

Science 2020 05 25;368(6490):493-497. Epub 2020 Mar 25.

Network Science Institute, Northeastern University, Boston, MA, USA.

The ongoing coronavirus disease 2019 (COVID-19) outbreak expanded rapidly throughout China. Major behavioral, clinical, and state interventions were undertaken to mitigate the epidemic and prevent the persistence of the virus in human populations in China and worldwide. It remains unclear how these unprecedented interventions, including travel restrictions, affected COVID-19 spread in China. We used real-time mobility data from Wuhan and detailed case data including travel history to elucidate the role of case importation in transmission in cities across China and to ascertain the impact of control measures. Early on, the spatial distribution of COVID-19 cases in China was explained well by human mobility data. After the implementation of control measures, this correlation dropped and growth rates became negative in most locations, although shifts in the demographics of reported cases were still indicative of local chains of transmission outside of Wuhan. This study shows that the drastic control measures implemented in China substantially mitigated the spread of COVID-19.
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http://dx.doi.org/10.1126/science.abb4218DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7146642PMC
May 2020

Assessing the role of live poultry trade in community-structured transmission of avian influenza in China.

Proc Natl Acad Sci U S A 2020 03 2;117(11):5949-5954. Epub 2020 Mar 2.

State Key Laboratory of Remote Sensing Science, College of Global Change and Earth System Science, Beijing Normal University, 100875 Beijing, China;

The live poultry trade is thought to play an important role in the spread and maintenance of highly pathogenic avian influenza A viruses (HP AIVs) in Asia. Despite an abundance of small-scale observational studies, the role of the poultry trade in disseminating AIV over large geographic areas is still unclear, especially for developing countries with complex poultry production systems. Here we combine virus genomes and reconstructed poultry transportation data to measure and compare the spatial spread in China of three key subtypes of AIV: H5N1, H7N9, and H5N6. Although it is difficult to disentangle the contribution of confounding factors, such as bird migration and spatial distance, we find evidence that the dissemination of these subtypes among domestic poultry is geographically continuous and likely associated with the intensity of the live poultry trade in China. Using two independent data sources and network analysis methods, we report a regional-scale community structure in China that might explain the spread of AIV subtypes in the country. The identification of this structure has the potential to inform more targeted strategies for the prevention and control of AIV in China.
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http://dx.doi.org/10.1073/pnas.1906954117DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7084072PMC
March 2020

Evolutionary selection of biofilm-mediated extended phenotypes in Yersinia pestis in response to a fluctuating environment.

Nat Commun 2020 01 15;11(1):281. Epub 2020 Jan 15.

State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, 100071, China.

Yersinia pestis is transmitted from fleas to rodents when the bacterium develops an extensive biofilm in the foregut of a flea, starving it into a feeding frenzy, or, alternatively, during a brief period directly after feeding on a bacteremic host. These two transmission modes are in a trade-off regulated by the amount of biofilm produced by the bacterium. Here by investigating 446 global isolated Y. pestis genomes, including 78 newly sequenced isolates sampled over 40 years from a plague focus in China, we provide evidence for strong selection pressures on the RNA polymerase ω-subunit encoding gene rpoZ. We demonstrate that rpoZ variants have an increased rate of biofilm production in vitro, and that they evolve in the ecosystem during colder and drier periods. Our results support the notion that the bacterium is constantly adapting-through extended phenotype changes in the fleas-in response to climate-driven changes in the niche.
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http://dx.doi.org/10.1038/s41467-019-14099-wDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6962365PMC
January 2020

Intrinsic and extrinsic drivers of transmission dynamics of hemorrhagic fever with renal syndrome caused by Seoul hantavirus.

PLoS Negl Trop Dis 2019 09 23;13(9):e0007757. Epub 2019 Sep 23.

State Key Laboratory of Remote Sensing Science, College of Global Change and Earth System Science, Beijing Normal University, Beijing, China.

Seoul hantavirus (SEOV) has recently raised concern by causing geographic range expansion of hemorrhagic fever with renal syndrome (HFRS). SEOV infections in humans are significantly underestimated worldwide and epidemic dynamics of SEOV-related HFRS are poorly understood because of a lack of field data and empirically validated models. Here, we use mathematical models to examine both intrinsic and extrinsic drivers of disease transmission from animal (the Norway rat) to humans in a SEOV-endemic area in China. We found that rat eradication schemes and vaccination campaigns, but below the local elimination threshold, could diminish the amplitude of the HFRS epidemic but did not modify its seasonality. Models demonstrate population dynamics of the rodent host were insensitive to climate variations in urban settings, while relative humidity had a negative effect on the seasonality in transmission. Our study contributes to a better understanding of the epidemiology of SEOV-related HFRS, demonstrates asynchronies between rodent population dynamics and transmission rate, and identifies potential drivers of the SEOV seasonality.
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http://dx.doi.org/10.1371/journal.pntd.0007757DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6776365PMC
September 2019

New evidence for the east-west spread of the highly pathogenic avian influenza H5N1 virus between Central Asian and east Asian-Australasian flyways in China.

Emerg Microbes Infect 2019 ;8(1):823-826

a Research Institute of Forest Ecology, Environment and Protection, Chinese Academy of Forestry, Key Laboratory of Forest Protection of State Forestry and Grassland Administration , National Bird Banding Center of China , Beijing , People's Republic of China.

The spread of highly pathogenic avian influenza (HPAI) H5N1 virus is associated with wild fowl migration in East Asian-Australasian (EA) and Central Asian (CA) flyways. However, the spread of H5N1 virus between the two flyways is still unclear. Here, the movements of wild waterfowl were obtained from satellite tracking data covering seven bar-headed geese and three great black-headed gulls breeding in the Qinghai Lake area (along the EA flyway), and 20 whooper swans wintering in the Sanmenxia Reservoir area (at the CA flyway). From the 2688 samples that were screened from wild birds at Qinghai Lake after an outbreak of H5N1 in July 2015, four genomes of H5N1 virus were obtained from bar-headed geese. The results of phylogenetic analysis indicated that these H5N1 viruses belonged to clade 2.3.2.1c and their gene fragments were highly homologous with A/whooper swan/Henan/SMX1/2015 (H5N1) virus (ranging from 99.76% to 100.00%) isolated from a dead whooper swan from the Sanmenxia Reservoir area along the EA flyway in January 2015. Furthermore, the coincidental timing of the H5N1 outbreak with spring migration, together with phylogenetic evidence, provided new evidence of the east-to-west spread of HPAI H5N1 between the EA and CA migratory flyways of China.
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http://dx.doi.org/10.1080/22221751.2019.1623719DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6567254PMC
September 2019

Contrasting effects of host species and phylogenetic diversity on the occurrence of HPAI H5N1 in European wild birds.

J Anim Ecol 2019 07 10;88(7):1044-1053. Epub 2019 May 10.

Resource Ecology Group, Wageningen University, Wageningen, The Netherlands.

Studies on the highly pathogenic avian influenza (HPAI) H5N1 suggest that wild bird migration may facilitate its long-distance spread, yet the role of wild bird community composition in its transmission risk remains poorly understood. Furthermore, most studies on the diversity-disease relationship focused on host species diversity without considering hosts' phylogenetic relationships, which may lead to rejecting a species diversity effect when the community has host species that are only distantly related. Here, we explored the influence of waterbird community composition for determining HPAI H5N1 occurrence in wild birds in a continental-scale study across Europe. In particular, we tested the diversity-disease relationship using both host species diversity and host phylogenetic diversity. Our results provide the first demonstration that host community composition-compared with previously identified environmental risk factors-can also effectively explain the spatial pattern of H5N1 occurrence in wild birds. We further show that communities with more higher risk host species and more closely related species have a higher risk of H5N1 outbreaks. Thus, both host species diversity and community phylogenetic structure, in addition to environmental factors, jointly influence H5N1 occurrence. Our work not only extends the current theory on the diversity-disease relationship, but also has important implications for future monitoring of H5N1 and other HPAI subtypes.
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http://dx.doi.org/10.1111/1365-2656.12997DOI Listing
July 2019

Impacts of Road Traffic Network and Socioeconomic Factors on the Diffusion of 2009 Pandemic Influenza A (H1N1) in Mainland China.

Int J Environ Res Public Health 2019 04 5;16(7). Epub 2019 Apr 5.

Ministry of Education Key Laboratory for Earth System Modeling, Department of Earth System Science, Tsinghua University, Beijing 100084, China.

The 2009 pandemic influenza virus caused the majority of the influenza A virus infections in China in 2009. It arrived in several Chinese cities from imported cases and then spread as people travelled domestically by all means of transportation, among which road traffic was the most commonly used for daily commuting. Spatial variation in socioeconomic status not only accelerates migration across regions but also partly induces the differences in epidemic processes and in responses to epidemics across regions. However, the roles of both road travel and socioeconomic factors have not received the attention they deserve. Here, we constructed a national highway network for and between 333 cities in mainland China and extracted epidemiological variables and socioeconomic factors for each city. We calculated classic centrality measures for each city in the network and proposed two new measures ( and ). We evaluated the correlation between the centrality measures and epidemiological features and conducted a spatial autoregression to quantify the impacts of road network and socioeconomic factors during the outbreak. The results showed that epidemics had more significant relationships with both our new measures than the classic ones. Higher population density, higher per person income, larger and , more hospitals and college students, and lower per person GDP were associated with higher cumulative incidence. Higher population density and number of slaughtered pigs were found to advance epidemic arrival time. Higher population density, more colleges and slaughtered pigs, and lower were associated with longer epidemic duration. In conclusion, road transport and socioeconomic status had significant impacts and should be considered for the prevention and control of future pandemics.
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http://dx.doi.org/10.3390/ijerph16071223DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6480969PMC
April 2019

Aedes mosquitoes acquire and transmit Zika virus by breeding in contaminated aquatic environments.

Nat Commun 2019 03 22;10(1):1324. Epub 2019 Mar 22.

Tsinghua-Peking Joint Center for Life Sciences, School of Medicine, Tsinghua University, 100084, Beijing, People's Republic of China.

Zika virus (ZIKV) is a mosquito-borne flavivirus that predominantly circulates between humans and Aedes mosquitoes. Clinical studies have shown that Zika viruria in patients persists for an extended period, and results in infectious virions being excreted. Here, we demonstrate that Aedes mosquitoes are permissive to ZIKV infection when breeding in urine or sewage containing low concentrations of ZIKV. Mosquito larvae and pupae, including from field Aedes aegypti can acquire ZIKV from contaminated aquatic systems, resulting in ZIKV infection of adult females. Adult mosquitoes can transmit infectious virions to susceptible type I/II interferon receptor-deficient (ifnagr-/-) C57BL/6 (AG6) mice. Furthermore, ZIKV viruria from infected AG6 mice can causes mosquito infection during the aquatic life stages. Our studies suggest that infectious urine could be a natural ZIKV source, which is potentially transmissible to mosquitoes when breeding in an aquatic environment.
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http://dx.doi.org/10.1038/s41467-019-09256-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6430813PMC
March 2019

The ecological dynamics of hantavirus diseases: From environmental variability to disease prevention largely based on data from China.

PLoS Negl Trop Dis 2019 02 21;13(2):e0006901. Epub 2019 Feb 21.

Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biosciences, University of Oslo, Blindern, Oslo, Norway.

Hantaviruses can cause hantavirus pulmonary syndrome (HPS) in the Americas and hemorrhagic fever with renal syndrome (HFRS) in Eurasia. In recent decades, repeated outbreaks of hantavirus disease have led to public concern and have created a global public health burden. Hantavirus spillover from natural hosts into human populations could be considered an ecological process, in which environmental forces, behavioral determinants of exposure, and dynamics at the human-animal interface affect human susceptibility and the epidemiology of the disease. In this review, we summarize the progress made in understanding hantavirus epidemiology and rodent reservoir population biology. We mainly focus on three species of rodent hosts with longitudinal studies of sufficient scale: the striped field mouse (Apodemus agrarius, the main reservoir host for Hantaan virus [HTNV], which causes HFRS) in Asia, the deer mouse (Peromyscus maniculatus, the main reservoir host for Sin Nombre virus [SNV], which causes HPS) in North America, and the bank vole (Myodes glareolus, the main reservoir host for Puumala virus [PUUV], which causes HFRS) in Europe. Moreover, we discuss the influence of ecological factors on human hantavirus disease outbreaks and provide an overview of research perspectives.
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http://dx.doi.org/10.1371/journal.pntd.0006901DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6383869PMC
February 2019

A maximum curvature method for estimating epidemic onset of seasonal influenza in Japan.

BMC Infect Dis 2019 Feb 20;19(1):181. Epub 2019 Feb 20.

Ministry of Education Key Laboratory for Earth System Modeling, Department of Earth System Science, Tsinghua University, Beijing, 100084, China.

Background: Detecting the onset of influenza epidemic is important for epidemiological surveillance and for investigating the factors driving spatiotemporal transmission patterns. Most approaches define the epidemic onset based on thresholds, which use subjective criteria and are specific to individual surveillance systems.

Methods: We applied the empirical threshold method (ETM), together with two non-thresholding methods, including the maximum curvature method (MCM) that we proposed and the segmented regression method (SRM), to determine onsets of influenza epidemics in each prefecture of Japan, using sentinel surveillance data of influenza-like illness (ILI) from 2012/2013 through 2017/2018. Performance of the MCM and SRM was evaluated, in terms of epidemic onset, end, and duration, with those derived from the ETM using the nationwide epidemic onset indicator of 1.0 ILI case per sentinel per week.

Results: The MCM and SRM yielded complete estimates for each of Japan's 47 prefectures. In contrast, ETM estimates for Kagoshima during 2012/2013 and for Okinawa during all six influenza seasons, except 2013/2014, were invalid. The MCM showed better agreement in all estimates with the ETM than the SRM (R = 0.82, p < 0.001 vs. R = 0.34, p < 0.001 for epidemic onset; R = 0.18, p < 0.001 vs. R = 0.05, p < 0.001 for epidemic end; R = 0.28, p < 0.001 vs. R < 0.01, p = 0.35 for epidemic duration). Prefecture-specific thresholds for epidemic onset and end were established using the MCM.

Conclusions: The Japanese national epidemic onset threshold is not applicable to all prefectures, particularly Okinawa. The MCM could be used to establish prefecture-specific epidemic thresholds that faithfully characterize influenza activity, serving as useful complements to the influenza surveillance system in Japan.
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http://dx.doi.org/10.1186/s12879-019-3777-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6383251PMC
February 2019

Transmission dynamics of re-emerging rabies in domestic dogs of rural China.

PLoS Pathog 2018 12 6;14(12):e1007392. Epub 2018 Dec 6.

KU Leuven, Department of Microbiology and Immunology, Rega Institute, Laboratory of Evolutionary and Computational Virology, Leuven, Belgium.

Despite ongoing efforts to control transmission, rabies prevention remains a challenge in many developing countries, especially in rural areas of China where re-emerging rabies is under-reported due to a lack of sustained animal surveillance. By taking advantage of detailed genomic and epidemiological data for the re-emerging rabies outbreak in Yunnan Province, China, collected between 1999 and 2015, we reconstruct the demographic and dispersal history of domestic dog rabies virus (RABV) as well as the dynamics of dog-to-dog and dog-to-human transmission. Phylogeographic analyses reveal a lower diffusion coefficient than previously estimated for dog RABV dissemination in northern Africa. Furthermore, epidemiological analyses reveal transmission rates between dogs, as well as between dogs and humans, lower than estimates for Africa. Finally, we show that reconstructed epidemic history of RABV among dogs and the dynamics of rabid dogs are consistent with the recorded human rabies cases. This work illustrates the benefits of combining phylogeographic and epidemic modelling approaches for uncovering the spatiotemporal dynamics of zoonotic diseases, with both approaches providing estimates of key epidemiological parameters.
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http://dx.doi.org/10.1371/journal.ppat.1007392DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6283347PMC
December 2018

Spatial heterogeneity of hemorrhagic fever with renal syndrome is driven by environmental factors and rodent community composition.

PLoS Negl Trop Dis 2018 10 24;12(10):e0006881. Epub 2018 Oct 24.

State Key Laboratory of Remote Sensing Science, College of Global Change and Earth System Science, Beijing Normal University, Beijing, China.

Hemorrhagic fever with renal syndrome (HFRS) is a rodent-borne disease caused mainly by two hantaviruses in China: Hantaan virus and Seoul virus. Environmental factors can significantly affect the risk of contracting hantavirus infections, primarily through their effects on rodent population dynamics and human-rodent contact. We aimed to clarify the environmental risk factors favoring rodent-to-human transmission to provide scientific evidence for developing effective HFRS prevention and control strategies. The 10-year (2006-2015) field surveillance data from the rodent hosts for hantavirus, the epidemiological and environmental data extracted from satellite images and meteorological stations, rodent-to-human transmission rates and impacts of the environment on rodent community composition were used to quantify the relationships among environmental factors, rodent species and HFRS occurrence. The study included 709 cases of HFRS. Rodent species in Chenzhou, a hantavirus hotspot, comprise mainly Rattus norvegicus, Mus musculus, R. flavipectus and some other species (R. losea and Microtus fortis calamorum). The rodent species played different roles across the various land types we examined, but all of them were associated with transmission risks. Some species were associated with HFRS occurrence risk in forest and water bodies. R. norvegicus and R. flavipectus were associated with risk of HFRS incidence in grassland, whereas M. musculus and R. flavipectus were associated with this risk in built-on land. The rodent community composition was also associated with environmental variability. The predictive risk models based on these significant factors were validated by a good-fit model, where: cultivated land was predicted to represent the highest risk for HFRS incidence, which accords with the statistics for HFRS cases in 2014-2015. The spatial heterogeneity of HFRS disease may be influenced by rodent community composition, which is associated with local environmental conditions. Therefore, future work should focus on preventing HFRS is moist, warm environments.
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http://dx.doi.org/10.1371/journal.pntd.0006881DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6218101PMC
October 2018

Migratory Whooper Swans Cygnus cygnus Transmit H5N1 Virus between China and Mongolia: Combination Evidence from Satellite Tracking and Phylogenetics Analysis.

Sci Rep 2018 05 4;8(1):7049. Epub 2018 May 4.

Harbin Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Harbin, 150040, China.

In late 2014, a highly pathogenic avian influenza (hereafter HPAI) H5N1 outbreak infected whooper swans Cygnus cygnus wintering at the Sanmenxia Reservoir area, China, and raised concerns about migratory linkages between wintering and breeding grounds of whooper swans. In this study, 61 swans were satellite tracked from 2013 to 2016 to determine the spatial association of their migration routes and H5N1 outbreaks, and 3596 fecal samples were collected along the migration routes for virology testing. Swans departed the wintering grounds and migrated along the Yellow River, and flew over the Yin Mountains in China. The Brownian bridge movement model showed there was a high degree of spatiotemporal overlap between the core use area along the spring migration pathway and historical H5N1 events in China and Mongolia from 2005 to 2015. The H5N1 strain was isolated and phylogenetic analyses confirmed that the HA gene sequence generated is genetically similar to that of the epidemic strain at a previous wintering site (the Sanmenxia Reservoir area) along its flyway. Our results identified a previously unknown migratory link of whooper swans in central China with Mongolia and confirmed that the swans could carry the HPAI H5N1 virus during migration, resulting in long-distance transmission.
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http://dx.doi.org/10.1038/s41598-018-25291-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5935751PMC
May 2018

Urbanization prolongs hantavirus epidemics in cities.

Proc Natl Acad Sci U S A 2018 05 17;115(18):4707-4712. Epub 2018 Apr 17.

Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biosciences, University of Oslo, N-0316 Oslo, Norway

Urbanization and rural-urban migration are two factors driving global patterns of disease and mortality. There is significant concern about their potential impact on disease burden and the effectiveness of current control approaches. Few attempts have been made to increase our understanding of the relationship between urbanization and disease dynamics, although it is generally believed that urban living has contributed to reductions in communicable disease burden in industrialized countries. To investigate this relationship, we carried out spatiotemporal analyses using a 48-year-long dataset of hemorrhagic fever with renal syndrome incidence (HFRS; mainly caused by two serotypes of hantavirus in China: Hantaan virus and Seoul virus) and population movements in an important endemic area of south China during the period 1963-2010. Our findings indicate that epidemics coincide with urbanization, geographic expansion, and migrant movement over time. We found a biphasic inverted U-shaped relationship between HFRS incidence and urbanization, with various endemic turning points associated with economic growth rates in cities. Our results revealed the interrelatedness of urbanization, migration, and hantavirus epidemiology, potentially explaining why urbanizing cities with high economic growth exhibit extended epidemics. Our results also highlight contrasting effects of urbanization on zoonotic disease outbreaks during periods of economic development in China.
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http://dx.doi.org/10.1073/pnas.1712767115DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5939059PMC
May 2018

Westward Spread of Highly Pathogenic Avian Influenza A(H7N9) Virus among Humans, China.

Emerg Infect Dis 2018 06 17;24(6):1095-1098. Epub 2018 Jun 17.

We report infection of humans with highly pathogenic avian influenza A(H7N9) virus in Shaanxi, China, in May 2017. We obtained complete genomes for samples from 5 patients and from live poultry markets or farms in 4 cities. Results indicate that H7N9 is spreading westward from southern and eastern China.
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http://dx.doi.org/10.3201/eid2406.171135DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6004833PMC
June 2018

Landscape and rodent community composition are associated with risk of hemorrhagic fever with renal syndrome in two cities in China, 2006-2013.

BMC Infect Dis 2018 01 12;18(1):37. Epub 2018 Jan 12.

State Key Laboratory of Remote Sensing Science, College of Global Change and Earth System Science, Beijing Normal University, Beijing, 100875, China.

Background: Hemorrhagic fever with renal syndrome (HFRS) is a rodent-borne disease caused by hantaviruses. Landscape can influence the risk of hantavirus infection for humans, mainly through its effect on rodent community composition and distribution. It is important to understand how landscapes influence population dynamics for different rodent species and the subsequent effect on HFRS risk.

Methods: To determine how rodent community composition influenced human hantavirus infection, we monitored rodent communities in the prefecture-level cities of Loudi and Shaoyang, China, from 2006 to 2013. Land use data were extracted from satellite images and rodent community diversity was analyzed in 45 trapping sites, in different environments. Potential contact matrices, determining how rodent community composition influence HFRS infection among different land use types, were estimated based on rodent community composition and environment type for geo-located HFRS cases.

Results: Apodemus agrarius and Rattus norvegicus were the predominant species in Loudi and Shaoyang, respectively. The major risk of HFRS infection was concentrated in areas with cultivated land and was associated with A. agrarius, R. norvegicus, and Rattus flavipectus. In urban areas in Shaoyang, Mus musculus was related to risk of hantavirus infection.

Conclusions: Landscape features and rodent community dynamics may affect the risk of human hantavirus infection. Results of this study may be useful for the development of HFRS prevention initiatives that are customized for regions with different geographical environments.
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http://dx.doi.org/10.1186/s12879-017-2827-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5767038PMC
January 2018

Emergence and Adaptation of a Novel Highly Pathogenic H7N9 Influenza Virus in Birds and Humans from a 2013 Human-Infecting Low-Pathogenic Ancestor.

J Virol 2018 01 2;92(2). Epub 2018 Jan 2.

National and Regional Joint Engineering Laboratory for Medicament of Zoonoses Prevention and Control, College of Veterinary Medicine, South China Agricultural University, Guangzhou, China

Since its emergence in 2013, the H7N9 low-pathogenic avian influenza virus (LPAIV) has been circulating in domestic poultry in China, causing five waves of human infections. A novel H7N9 highly pathogenic avian influenza virus (HPAIV) variant possessing multiple basic amino acids at the cleavage site of the hemagglutinin (HA) protein was first reported in two cases of human infection in January 2017. More seriously, those novel H7N9 HPAIV variants have been transmitted and caused outbreaks on poultry farms in eight provinces in China. Herein, we demonstrate the presence of three different amino acid motifs at the cleavage sites of these HPAIV variants which were isolated from chickens and humans and likely evolved from the preexisting LPAIVs. Animal experiments showed that these novel H7N9 HPAIV variants are both highly pathogenic in chickens and lethal to mice. Notably, human-origin viruses were more pathogenic in mice than avian viruses, and the mutations in the PB2 gene associated with adaptation to mammals (E627K, A588V, and D701N) were identified by next-generation sequencing (NGS) and Sanger sequencing of the isolates from infected mice. No polymorphisms in the key amino acid substitutions of PB2 and HA in isolates from infected chicken lungs were detected by NGS. In sum, these results highlight the high degree of pathogenicity and the valid transmissibility of this new H7N9 variant in chickens and the quick adaptation of this new H7N9 variant to mammals, so the risk should be evaluated and more attention should be paid to this variant. Due to the recent increased numbers of zoonotic infections in poultry and persistent human infections in China, influenza A(H7N9) virus has remained a public health threat. Most of the influenza A(H7N9) viruses reported previously have been of low pathogenicity. Now, these novel H7N9 HPAIV variants have caused human infections in three provinces and outbreaks on poultry farms in eight provinces in China. We analyzed the molecular features and compared the relative characteristics of one H7N9 LPAIV and two H7N9 HPAIVs isolated from chickens and two human-origin H7N9 HPAIVs in chicken and mouse models. We found that all HPAIVs both are highly pathogenic and have valid transmissibility in chickens. Strikingly, the human-origin viruses were more highly pathogenic than the avian-origin viruses in mice, and dynamic mutations were confirmed by NGS and Sanger sequencing. Our findings offer important insight into the origin, adaptation, pathogenicity, and transmissibility of these viruses to both poultry and mammals.
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http://dx.doi.org/10.1128/JVI.00921-17DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5752946PMC
January 2018

Increasing airline travel may facilitate co-circulation of multiple dengue virus serotypes in Asia.

PLoS Negl Trop Dis 2017 Aug 3;11(8):e0005694. Epub 2017 Aug 3.

State Key Laboratory of Remote Sensing Science, College of Global Change and Earth System Science, Beijing Normal University, Beijing, China.

The incidence of dengue has grown dramatically in recent decades worldwide, especially in Southeast Asia and the Americas with substantial transmission in 2014-2015. Yet the mechanisms underlying the spatio-temporal circulation of dengue virus (DENV) serotypes at large geographical scales remain elusive. Here we investigate the co-circulation in Asia of DENV serotypes 1-3 from 1956 to 2015, using a statistical framework that jointly estimates migration history and quantifies potential predictors of viral spatial diffusion, including socio-economic, air transportation and maritime mobility data. We find that the spread of DENV-1, -2 and -3 lineages in Asia is significantly associated with air traffic. Our analyses suggest the network centrality of air traffic hubs such as Thailand and India contribute to seeding dengue epidemics, whilst China, Cambodia, Indonesia, and Singapore may establish viral diffusion links with multiple countries in Asia. Phylogeographic reconstructions help to explain how growing air transportation networks could influence the dynamics of DENV circulation.
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http://dx.doi.org/10.1371/journal.pntd.0005694DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5542384PMC
August 2017

Severe Fever with Thrombocytopenia Syndrome Virus in Humans, Domesticated Animals, Ticks, and Mosquitoes, Shaanxi Province, China.

Am J Trop Med Hyg 2017 Jun;96(6):1346-1349

Ministry of Education Key Laboratory for Earth System Modelling, Department of Earth System Science, Tsinghua University, Beijing, China.

AbstractThe first human infection with severe fever with thrombocytopenia syndrome virus (SFTSV) was detected in Shaanxi Province, China, in 2013, although the virus had been reported in 13 other provinces of China since 2010. We collected and analyzed a total of 4,011 samples, including 936 human serum samples, 155 animal serum samples, 895 ticks, 1,950 mosquitoes, 30 midges, and 20 sandflies. SFTSV antibodies were found in 44 human samples (4.7%) with no significant differences between males and females or across counties. The incidence rate of severe fever with thrombocytopenia syndrome was significantly higher among individuals 20-60 years of age. Moreover, SFTSV-specific antibodies were detected in goats (66.7%), cattle (13.2%), and dogs (15.0%), but not in pigs (0%). We detected the virus in ticks with a prevalence rate of 21.3% (17/80 pools). All mosquito, midge, and sandfly samples were negative for SFTSV. These results support wide circulation of the virus in western China. ticks may serve as a novel SFTSV vector, and the role of these ticks requires further investigation.
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http://dx.doi.org/10.4269/ajtmh.16-0333DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5462569PMC
June 2017

Interannual cycles of Hantaan virus outbreaks at the human-animal interface in Central China are controlled by temperature and rainfall.

Proc Natl Acad Sci U S A 2017 07 10;114(30):8041-8046. Epub 2017 Jul 10.

State Key Laboratory of Remote Sensing Science, College of Global Change and Earth System Science, Beijing Normal University, Beijing 100875, China;

Hantavirus, a rodent-borne zoonotic pathogen, has a global distribution with 200,000 human infections diagnosed annually. In recent decades, repeated outbreaks of hantavirus infections have been reported in Eurasia and America. These outbreaks have led to public concern and an interest in understanding the underlying biological mechanisms. Here, we propose a climate-animal-Hantaan virus (HTNV) infection model to address this issue, using a unique dataset spanning a 54-y period (1960-2013). This dataset comes from Central China, a focal point for natural HTNV infection, and includes both field surveillance and an epidemiological record. We reveal that the 8-y cycle of HTNV outbreaks is driven by the confluence of the cyclic dynamics of striped field mouse () populations and climate variability, at both seasonal and interannual cycles. Two climatic variables play key roles in the ecology of the HTNV system: temperature and rainfall. These variables account for the dynamics in the host reservoir system and markedly affect both the rate of transmission and the potential risk of outbreaks. Our results suggest that outbreaks of HTNV infection occur only when climatic conditions are favorable for both rodent population growth and virus transmission. These findings improve our understanding of how climate drives the periodic reemergence of zoonotic disease outbreaks over long timescales.
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http://dx.doi.org/10.1073/pnas.1701777114DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5544290PMC
July 2017

Cross-border spread, lineage displacement and evolutionary rate estimation of rabies virus in Yunnan Province, China.

Virol J 2017 06 3;14(1):102. Epub 2017 Jun 3.

State Key Laboratory of Remote Sensing Science, College of Global Change and Earth System Science, Beijing Normal University, Beijing, China.

Background: Rabies is an important but underestimated threat to public health, with most cases reported in Asia. Since 2000, a new epidemic wave of rabies has emerged in Yunnan Province, southwestern China, which borders three countries in Southeast Asia.

Method: We estimated gene-specific evolutionary rates for rabies virus using available data in GenBank, then used this information to calibrate the timescale of rabies virus (RABV) spread in Asia. We used 452 publicly available geo-referenced complete nucleoprotein (N) gene sequences, including 52 RABV sequences that were recently generated from samples collected in Yunnan between 2008 and 2012.

Results: The RABV N gene evolutionary rate was estimated to be 1.88 × 10 (1.37-2.41 × 10, 95% Bayesian credible interval, BCI) substitutions per site per year. Phylogenetic reconstructions show that the currently circulating RABV lineages in Yunnan result from at least seven independent introductions (95% BCI: 6-9 introductions) and represent each of the three main Asian RABV lineages, SEA-1, -2 and -3. We find that Yunnan is a sink location for the domestic spread of RABV and connects RABV epidemics in North China, South China, and Southeast Asia. Cross-border spread from southeast Asia (SEA) into South China, and intermixing of the North and South China epidemics is also well supported. The influx of RABV into Yunnan from SEA was not well-supported, likely due to the poor sampling of SEA RABV diversity. We found evidence for a lineage displacement of the Yunnan SEA-2 and -3 lineages by Yunnan SEA-1 strains, and considered whether this could be attributed to fitness differences.

Conclusion: Overall, our study contributes to a better understanding of the spread of RABV that could facilitate future rabies virus control and prevention efforts.
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http://dx.doi.org/10.1186/s12985-017-0769-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5457581PMC
June 2017