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      Spatial characteristics and the epidemiology of human infections with avian influenza A(H7N9) virus in five waves from 2013 to 2017 in Zhejiang Province, China

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          Abstract

          Background

          The five-wave epidemic of H7N9 in China emerged in the second half of 2016. This study aimed to compare the epidemiological characteristics among the five waves, estimating the possible infected cases and inferring the extent of the possible epidemic in the areas that have not reported cases before.

          Methods

          The data for the H7N9 cases from Zhejiang Province between 2013 and 2017 was obtained from the China Information Network System of Disease Prevention and Control. The start date of each wave was 16 March 2013, 1 July 2013, 1 July 2014, 1 July 2015 and 1 July 2016. The F test or Pearson’s chi-square test were used to compare the characteristics of the five waves. Global and local autocorrelation analysis was carried out to identify spatial autocorrelations. Ordinary kriging interpolation was analyzed to estimate the number of human infections with H7N9 virus and to infer the extent of infections in the areas with no cases reported before.

          Result

          There were 45, 94, 45, 34 and 80 cases identified from the first wave to the fifth, respectively. The death rate was significantly different among the five waves of epidemics ( χ 2 = 10.784, P = 0.029). The age distribution ( F = 0.903, P = 0.462), gender ( χ 2 = 2.674, P = 0.614) and occupation( χ 2 = 19.764, P = 0.407) were similar in each period. Most of the cases were males and farmers. A significant trend ( χ 2 = 70.328, P<0.001) was identified that showed a growing proportion of rural cases. There were 31 high-high clusters and 3 high-low clusters at the county level among the five waves and 12, 8, 2, 9 and 3 clusters in each wave, respectively. The total cases infected with the H7N9 virus were far more than those that have been reported now, and the affected areas continue to expand. The epidemic in the north of Zhejiang Province persisted in all five waves. Since the second wave, the virus spread to the south areas and central areas. There was an obvious decline in the infected cases in the urban areas, and the epidemics mostly occurred in the rural areas after the fourth wave. The epidemic was relatively dispersed since the third wave had fewer than two cases in most of the areas and showed a reinforcing trend again in the fifth wave.

          Conclusions

          The study revealed that there were few differences in the epidemiologic characteristics among the five waves of the epidemic. However, the areas where the possible epidemic circulated was larger than reported. The epidemic cross-regional expansion continued and mostly occurred in rural areas. Continuous closure of the live poultry market (LPM) is strongly recommended in both rural and urban areas. Illegal and scattered live poultry trading, especially in rural areas, must be forbidden. It is suggested too that a more rigorous management be performed on live poultry trade and wholesale across the area. Health education, surveillance of cases and pathogenicity should also be strengthened.

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          Most cited references28

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          Epidemiology of Human Infections with Avian Influenza A(H7N9) Virus in China

          New England Journal of Medicine, 370(6), 520-532
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            Comparative epidemiology of human infections with avian influenza A H7N9 and H5N1 viruses in China: a population-based study of laboratory-confirmed cases.

            The novel influenza A H7N9 virus emerged recently in mainland China, whereas the influenza A H5N1 virus has infected people in China since 2003. Both infections are thought to be mainly zoonotic. We aimed to compare the epidemiological characteristics of the complete series of laboratory-confirmed cases of both viruses in mainland China so far. An integrated database was constructed with information about demographic, epidemiological, and clinical variables of laboratory-confirmed cases of H7N9 (130 patients) and H5N1 (43 patients) that were reported to the Chinese Centre for Disease Control and Prevention until May 24, 2013. We described disease occurrence by age, sex, and geography, and estimated key epidemiological variables. We used survival analysis techniques to estimate the following distributions: infection to onset, onset to admission, onset to laboratory confirmation, admission to death, and admission to discharge. The median age of the 130 individuals with confirmed infection with H7N9 was 62 years and of the 43 with H5N1 was 26 years. In urban areas, 74% of cases of both viruses were in men, whereas in rural areas the proportions of the viruses in men were 62% for H7N9 and 33% for H5N1. 75% of patients infected with H7N9 and 71% of those with H5N1 reported recent exposure to poultry. The mean incubation period of H7N9 was 3·1 days and of H5N1 was 3·3 days. On average, 21 contacts were traced for each case of H7N9 in urban areas and 18 in rural areas, compared with 90 and 63 for H5N1. The fatality risk on admission to hospital was 36% (95% CI 26-45) for H7N9 and 70% (56-83%) for H5N1. The sex ratios in urban compared with rural cases are consistent with exposure to poultry driving the risk of infection--a higher risk in men was only recorded in urban areas but not in rural areas, and the increased risk for men was of a similar magnitude for H7N9 and H5N1. However, the difference in susceptibility to serious illness with the two different viruses remains unexplained, since most cases of H7N9 were in older adults whereas most cases of H5N1 were in younger people. A limitation of our study is that we compared laboratory-confirmed cases of H7N9 and H5N1 infection, and some infections might not have been ascertained. Ministry of Science and Technology, China; Research Fund for the Control of Infectious Disease and University Grants Committee, Hong Kong Special Administrative Region, China; and the US National Institutes of Health. Copyright © 2013 Elsevier Ltd. All rights reserved.
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              Human infection with avian influenza A H7N9 virus: an assessment of clinical severity

              Summary Background Characterisation of the severity profile of human infections with influenza viruses of animal origin is a part of pandemic risk assessment, and an important part of the assessment of disease epidemiology. Our objective was to assess the clinical severity of human infections with avian influenza A H7N9 virus, which emerged in China in early 2013. Methods We obtained information about laboratory-confirmed cases of avian influenza A H7N9 virus infection reported as of May 28, 2013, from an integrated database built by the Chinese Center for Disease Control and Prevention. We estimated the risk of fatality, mechanical ventilation, and admission to the intensive care unit for patients who required hospital admission for medical reasons. We also used information about laboratory-confirmed cases detected through sentinel influenza-like illness surveillance to estimate the symptomatic case fatality risk. Findings Of 123 patients with laboratory-confirmed avian influenza A H7N9 virus infection who were admitted to hospital, 37 (30%) had died and 69 (56%) had recovered by May 28, 2013. After we accounted for incomplete data for 17 patients who were still in hospital, we estimated the fatality risk for all ages to be 36% (95% CI 26–45) on admission to hospital. Risks of mechanical ventilation or fatality (69%, 95% CI 60–77) and of admission to an intensive care unit, mechanical ventilation, or fatality (83%, 76–90) were high. With assumptions about coverage of the sentinel surveillance network and health-care-seeking behaviour for patients with influenza-like illness associated with influenza A H7N9 virus infection, and pro-rata extrapolation, we estimated that the symptomatic case fatality risk could be between 160 (63–460) and 2800 (1000–9400) per 100 000 symptomatic cases. Interpretation Human infections with avian influenza A H7N9 virus seem to be less serious than has been previously reported. Many mild cases might already have occurred. Continued vigilance and sustained intensive control efforts are needed to minimise the risk of human infection. Funding Chinese Ministry of Science and Technology; Research Fund for the Control of Infectious Disease; Hong Kong University Grants Committee; China–US Collaborative Program on Emerging and Re-emerging Infectious Diseases; Harvard Center for Communicable Disease Dynamics; US National Institute of Allergy and Infectious Disease; and the US National Institutes of Health.
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                Author and article information

                Contributors
                Role: Data curationRole: Formal analysisRole: MethodologyRole: Writing – original draft
                Role: SupervisionRole: Writing – review & editing
                Role: Writing – review & editing
                Role: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: Resources
                Role: Data curationRole: Resources
                Role: Data curationRole: Resources
                Role: ConceptualizationRole: Supervision
                Role: ConceptualizationRole: SupervisionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                27 July 2017
                2017
                : 12
                : 7
                : e0180763
                Affiliations
                [1 ] Zhejiang Province Center for Disease Control and Prevention, Hangzhou, Zhejiang Province, China
                [2 ] Key Laboratory for Vaccine, Prevention and Control of Infectious Disease of Zhejiang Province, Hangzhou, Zhejiang Province, China
                [3 ] Hangzhou Centre for Disease Control and Prevention, Hangzhou, Zhejiang, Province, China
                [4 ] Kingston University UK, London, United Kingdom
                Icahn School of Medicine at Mount Sinai, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0003-1851-3704
                Article
                PONE-D-17-03760
                10.1371/journal.pone.0180763
                5531501
                28750032
                6e4b1d8b-ed48-4b17-8d04-db61a4ac64e8
                © 2017 Wu et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 17 February 2017
                : 21 June 2017
                Page count
                Figures: 7, Tables: 4, Pages: 17
                Funding
                Funded by: Provincial Medical Research Fund of Zhejiang
                Award ID: 2015RCB008
                Award Recipient :
                Funded by: Zhejiang Province Center for Disease Control and Prevention
                Award ID: 2017KY131
                Award Recipient :
                This work was supported by grants from Provincial Medical Research Fund of Zhejiang, China (grant number were 2015RCB008 and 2017KY131). The document in website were http://www.zjmed.org.cn/previewerlet.do?id=8DD1BAEA38B99297 and http://www.zjmed.org.cn/previewerlet.do?id=00B32CCF219B843D. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
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                Organisms
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                Orthomyxoviruses
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                H7N9
                Biology and life sciences
                Microbiology
                Medical microbiology
                Microbial pathogens
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