antibody seroprevalence in the epicenter wuhan hubei and six selected provinces after CORD-Papers-2022-06-02 (Version 1)

Title: Antibody seroprevalence in the epicenter Wuhan Hubei and six selected provinces after containment of the first epidemic wave of COVID-19 in China
Abstract: BACKGROUND: China implemented containment measures to stop SARS-CoV-2 transmission in response to the COVID-19 epidemic. After the first epidemic wave we conducted population-based serological surveys to determine extent of infection risk factors for infection and neutralization antibody levels to assess the real infections in the random sampled population. METHODS: We used a multistage stratified cluster random sampling strategy to conduct serological surveys in three areas - Wuhan Hubei Province outside Wuhan and six provinces selected on COVID-19 incidence and containment strategy. Participants were consenting individuals >1 year old who resided in the survey area >14 days during the epidemic. Provinces screened sera for SARS-CoV-2-specific IgM IgG and total antibody by two lateral flow immunoassays and one magnetic chemiluminescence enzyme immunoassay; positive samples were verified by micro-neutralization assay. FINDINGS: We enrolled 34857 participants (overall response rate 92%); 427 were positive by micro-neutralization assay. Wuhan had the highest weighted seroprevalence (443% 95% confidence interval [95%CI]=348%-562%) followed by Hubei-ex-Wuhan (044% 95%CI=026%-076%) and the other provinces (<01%). Living in Wuhan (adjusted odds ratio aOR=1370 95%CI= 7912375) contact with COVID-19 patients (aOR=735 95%CI=5051069) and age over 40 (aOR=136 95%CI=107172) were significantly associated with SARS-CoV-2 infection. Among seropositives 101 (24%) reported symptoms and had higher geometric mean neutralizing antibody titers than among the 326 (76%) without symptoms (3024 vs 1521 p<0001). INTERPRETATION: The low overall extent of infection and steep gradient of seropositivity from Wuhan to the outer provinces provide evidence supporting the success of containment of the first wave of COVID-19 in China. SARS-CoV-2 infection was largely asymptomatic emphasizing the importance of active case finding and physical distancing. Virtually the entire population of China remains susceptible to SARS-CoV-2; vaccination will be needed for long-term protection. FUNDING: This study was supported by the Ministry of Science and Technology (2020YFC0846900) and the National Natural Science Foundation of China (82041026 82041027 82041028 82041029 82041030 82041032 82041033).
Published: 2021-02-05
Journal: Lancet Reg Health West Pac
DOI: 10.1016/j.lanwpc.2021.100094
DOI_URL: http://doi.org/10.1016/j.lanwpc.2021.100094
Author Name: Li Zhongjie
Author link: https://covid19-data.nist.gov/pid/rest/local/author/li_zhongjie
Author Name: Guan Xuhua
Author link: https://covid19-data.nist.gov/pid/rest/local/author/guan_xuhua
Author Name: Mao Naiying
Author link: https://covid19-data.nist.gov/pid/rest/local/author/mao_naiying
Author Name: Luo Huiming
Author link: https://covid19-data.nist.gov/pid/rest/local/author/luo_huiming
Author Name: Qin Ying
Author link: https://covid19-data.nist.gov/pid/rest/local/author/qin_ying
Author Name: He Na
Author link: https://covid19-data.nist.gov/pid/rest/local/author/he_na
Author Name: Zhu Zhen
Author link: https://covid19-data.nist.gov/pid/rest/local/author/zhu_zhen
Author Name: Yu Jianxing
Author link: https://covid19-data.nist.gov/pid/rest/local/author/yu_jianxing
Author Name: Li Yu
Author link: https://covid19-data.nist.gov/pid/rest/local/author/li_yu
Author Name: Liu Jianhua
Author link: https://covid19-data.nist.gov/pid/rest/local/author/liu_jianhua
Author Name: An Zhijie
Author link: https://covid19-data.nist.gov/pid/rest/local/author/an_zhijie
Author Name: Gao Wenjing
Author link: https://covid19-data.nist.gov/pid/rest/local/author/gao_wenjing
Author Name: Wang Xiaoli
Author link: https://covid19-data.nist.gov/pid/rest/local/author/wang_xiaoli
Author Name: Sun Xiaodong
Author link: https://covid19-data.nist.gov/pid/rest/local/author/sun_xiaodong
Author Name: Song Tie
Author link: https://covid19-data.nist.gov/pid/rest/local/author/song_tie
Author Name: Yang Xingfen
Author link: https://covid19-data.nist.gov/pid/rest/local/author/yang_xingfen
Author Name: Wu Ming
Author link: https://covid19-data.nist.gov/pid/rest/local/author/wu_ming
Author Name: Wu Xianping
Author link: https://covid19-data.nist.gov/pid/rest/local/author/wu_xianping
Author Name: Yao Wenqing
Author link: https://covid19-data.nist.gov/pid/rest/local/author/yao_wenqing
Author Name: Peng Zhibin
Author link: https://covid19-data.nist.gov/pid/rest/local/author/peng_zhibin
Author Name: Sun Junling
Author link: https://covid19-data.nist.gov/pid/rest/local/author/sun_junling
Author Name: Wang Liping
Author link: https://covid19-data.nist.gov/pid/rest/local/author/wang_liping
Author Name: Guo Qing
Author link: https://covid19-data.nist.gov/pid/rest/local/author/guo_qing
Author Name: Xiang Nijuan
Author link: https://covid19-data.nist.gov/pid/rest/local/author/xiang_nijuan
Author Name: Liu Jun
Author link: https://covid19-data.nist.gov/pid/rest/local/author/liu_jun
Author Name: Zhang Bike
Author link: https://covid19-data.nist.gov/pid/rest/local/author/zhang_bike
Author Name: Su Xuemei
Author link: https://covid19-data.nist.gov/pid/rest/local/author/su_xuemei
Author Name: Rodewald Lance
Author link: https://covid19-data.nist.gov/pid/rest/local/author/rodewald_lance
Author Name: Li Liming
Author link: https://covid19-data.nist.gov/pid/rest/local/author/li_liming
Author Name: Xu Wenbo
Author link: https://covid19-data.nist.gov/pid/rest/local/author/xu_wenbo
Author Name: Shen Hongbing
Author link: https://covid19-data.nist.gov/pid/rest/local/author/shen_hongbing
Author Name: Feng Zijian
Author link: https://covid19-data.nist.gov/pid/rest/local/author/feng_zijian
Author Name: Gao George F
Author link: https://covid19-data.nist.gov/pid/rest/local/author/gao_george_f
sha: c735fd8a07cce1668cb31fc24d174b1d3787e449
license: no-cc
license_url: [no creative commons license associated]
source_x: Elsevier; Medline; PMC
source_x_url: https://www.elsevier.com/https://www.medline.com/https://www.ncbi.nlm.nih.gov/pubmed/
pubmed_id: 33585828
pubmed_id_url: https://www.ncbi.nlm.nih.gov/pubmed/33585828
pmcid: PMC7864613
pmcid_url: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7864613
url: https://api.elsevier.com/content/article/pii/S2666606521000031 https://doi.org/10.1016/j.lanwpc.2021.100094 https://www.sciencedirect.com/science/article/pii/S2666606521000031 https://www.ncbi.nlm.nih.gov/pubmed/33585828/
has_full_text: TRUE
Keywords Extracted from Text Content: Wuhan SARS-CoV-2 COVID-19 COVID-19 patients outer ZL bal-anced Hubei-ex-Wuhan and 2 specimens −71 XY GMT appendix pp 6-9 appendix p 20 GMTs outer taste LFA Wuhan [8 IgG IgM Wuhan, participants CIs −40 °C −0 LW, QG persons 20-39 −5 Wuhan City NT tests ZP BALF NPIs 1-81year-olds LL Wuhan) appendix p 15 IgG antibody patients coronavirus 2 Hubei Hubei ( −100 residents WX appendix pp 2-4 Lines LL, HS NIVDC COVID-19 patients ZA serum samples Lockdown WY HS, NH sera ZZ NAb ≥ 4 Innovita 2019-nCoV antibody samples subject-perceived LL, HS, NH Vaccines 17-August 16) [29] [30] [31] [32] [33] blood donors respondents children SARS-CoV-2-specific IgG NAb plus 3 LR HL Hubei. 10,632 throat COVID-19 appendix p 16 PUE Wuhan Hubei's people measles bronchoaveolar lavage fluids appendix pp [17] [18] immunodeficiency −58 JY NAb UN2814 SARS-CoV-2-specific NAb first-wave NAb GMTs SARS-CoV-2-specific neutralizing antibodies Wuhan [16 Spain's shortness-of-breath -Wuhan blood samples human WG ±2 • 1 appendix pp 9-10 −2 XG persons Hubeiex-Wuhan SARS-CoV-2 Jiangsu SARS-CoV-2-specific neutralizing antibody Hubei-ex-Wuhan NX, JL coronavirus COVID-19 vaccines appendix p 6 Wuhan -Wuhan sera IgG Hubei-ex-Wuhan COVID-19 participants Hubei Province SARS-CoV-2-specific IgM county- lateral
Extracted Text Content in Record: First 5000 Characters:Background: China implemented containment measures to stop SARS-CoV-2 transmission in response to the COVID-19 epidemic. After the first epidemic wave, we conducted population-based serological surveys to determine extent of infection, risk factors for infection, and neutralization antibody levels to assess the real infections in the random sampled population. * Corresponding authors. 1 These authors contributed equally to this project. The Lancet Regional Health -Western Pacific 8 (2021) 10 0 094 provinces ( < 0 • 1%). Living in Wuhan (adjusted odds ratio aOR = 13 • 70, 95%CI = 7 • 91-23 • 75), contact with COVID-19 patients (aOR = 7 • 35, 95%CI = 5 • 05-10 • 69), and age over 40 (aOR = 1 • 36, 95%CI = 1 • 07-1 • 72) were significantly associated with SARS-CoV-2 infection. Among seropositives, 101 (24%) reported symptoms and had higher geometric mean neutralizing antibody titers than among the 326 (76%) without symptoms (30 ±2 • 4 vs 15 ±2 • 1, p < 0 • 001). Interpretation: The low overall extent of infection and steep gradient of seropositivity from Wuhan to the outer provinces provide evidence supporting the success of containment of the first wave of COVID-19 in China. SARS-CoV-2 infection was largely asymptomatic, emphasizing the importance of active case finding and physical distancing. Virtually the entire population of China remains susceptible to SARS-CoV-2; vaccination will be needed for long-term protection. gies to safely immunize populations and enable selective lifting of non-pharmaceutical interventions that are currently maintaining elimination of SARS-CoV-2 transmission. Prevention and control of COVID-19 will be a long-term effort, requiring considerable domestic work and effective global collaboration. Evidence before this study Accurately measuring the prevalence of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) antibodies in populations can help increase knowledge about immunity, transmission, response strategies, surveillance, and eventually vaccination of COVID-19. We searched PubMed for peer-reviewed articles on September 28, 2020, with no limitations of start date or language, using the terms, "COVID-19 , "SARS-CoV-2 , "antibody", "seroprevalence", and "seroepidemiology". Most serosurveys used convenience samples in hospital settings or were conducted among selected populations such as health care workers, blood donors, factory workers, or local community residents, limiting their ability to provide unbiased population seroprevalence estimates. Few studies were conducted immediately following containment of a COVID-19 epidemic, limiting comparability of containment by country or region. Added value of this study Between two and three weeks after the end of the first-wave of COVID-19 in China, we conducted population-based serological surveys to estimate prevalence of SARS-CoV-2-specific neutralizing antibodies (NAbs) among representative samples totaling 34,857 participants. We surveyed three areas -Wuhan City, Hubeiex-Wuhan, and six provinces selected on the basis of containment strategy and COVID-19 incidence to ensure inclusion of the highest incidence provinces. Resulting seroprevalence estimates were: Wuhan, 4 • 43%; Hubei-ex-Wuhan, 0 • 44%; and the six other provinces, < 0 • 1%. Seroprevalence was highly correlated with reported COVID-19 incidence. Most subjects with serologic evidence of infections were asymptomatic (76%). To our knowledge, this is the first nationally representative estimate of SARS-CoV-2 seroprevalence in China. Implications of all the available evidence The low overall seroprevalence, the steep gradient of seropositivity from Wuhan to Hubei-ex-Wuhan to the other provinces, and the high correlation with COVID-19 incidence provide evidence supporting the impact of China's centrally-coordinated, locallyimplemented, "whole-of-government, whole-of-society" effort to contain the coronavirus. The low seroprevalence shows that the first wave of COVID-19 infected a relatively small number of individuals in China, leaving virtually the entire population susceptible to SARS-CoV-2 infection. That most infections were asymptomatic supports the importance of contact tracing strategies to stop transmission. Long-term protection of the population and the economy will necessitate using COVID-19 vaccination strate- In late December 2019, a cluster of patients with severe pneumonia of unknown etiology (PUE) was reported. A new coronavirus, now called SARS-CoV-2, was discovered in the PUE patients' bronchoaveolar lavage fluids (BALF), identified, and sequenced, and was reported to the World Health Organization (WHO) [1] [2] [3] . SARS-CoV-2 is highly contagious, and its human disease, COVID-19, causes significant morbidity and mortality [4] . WHO declared COVID-19 as a pandemic on March 11, 2020 , and by the end of November, there have been over 62 million cases and 1.4 million deaths reported worldwide [5] . China took unprecedented stringent measures in respon
Keywords Extracted from PMC Text: CIs ZL people shortness-of-breath CI=0•26%−0•76 SARS-CoV-2′′ Hubei. GMT 57%−71 WG Hubei ( 4•4 residents −40 °C sera Lockdown JY COVID-19′′ immunodeficiency HS, NH 44%−58 [aOR]=13•70 SARS-CoV-2-specific neutralizing antibodies UN2814 Wuhan, WY appendix p 16 appendix p 15 ZA NX, JL 33±2•1 subject-perceived blood donors ZP appendix pp 9–10 serum samples " NAb 40–59 ZZ IgG outer IgM appendix p 20 Hubei's respondents Wuhan LL, HS, NH human Hubei-ex-Wuhan blood samples LFA throat samples XG NAb GMTs SARS-CoV-2-specific neutralizing antibody XY lateral NIVDC SARS-CoV-2-specific NAb HL first-wave COVID-19 patients persons WX LL PUE blood measles GMTs CI=5•05–10•69 CI=1•07–1•72 Jiangsu Hubei NAb ≥ 4 NAb plus 3 LW, QG Wuhan City SARS-CoV-2-specific IgG COVID-19 vaccines SARS-CoV-2 LR children appendix pp 6–9 appendix pp 17–18 IgG antibody Spain's patients Wuhan [8 Innovita 2019-nCoV antibody 10,632 specimens Vaccines NT tests LL, HS coronavirus Lines" appendix p 6 taste 13–65 Wuhan) coronavirus 2 BALF county- COVID-19 Wuhan [16 appendix participants
Extracted PMC Text Content in Record: First 5000 Characters:Evidence before this study Accurately measuring the prevalence of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) antibodies in populations can help increase knowledge about immunity, transmission, response strategies, surveillance, and eventually vaccination of COVID-19. We searched PubMed for peer-reviewed articles on September 28, 2020, with no limitations of start date or language, using the terms, "COVID-19′′, "SARS-CoV-2′′, "antibody", "seroprevalence", and "seroepidemiology". Most serosurveys used convenience samples in hospital settings or were conducted among selected populations such as health care workers, blood donors, factory workers, or local community residents, limiting their ability to provide unbiased population seroprevalence estimates. Few studies were conducted immediately following containment of a COVID-19 epidemic, limiting comparability of containment by country or region. Added value of this study Between two and three weeks after the end of the first-wave of COVID-19 in China, we conducted population-based serological surveys to estimate prevalence of SARS-CoV-2-specific neutralizing antibodies (NAbs) among representative samples totaling 34,857 participants. We surveyed three areas – Wuhan City, Hubei-ex-Wuhan, and six provinces selected on the basis of containment strategy and COVID-19 incidence to ensure inclusion of the highest incidence provinces. Resulting seroprevalence estimates were: Wuhan, 4•43%; Hubei-ex-Wuhan, 0•44%; and the six other provinces, <0•1%. Seroprevalence was highly correlated with reported COVID-19 incidence. Most subjects with serologic evidence of infections were asymptomatic (76%). To our knowledge, this is the first nationally representative estimate of SARS-CoV-2 seroprevalence in China. Implications of all the available evidence The low overall seroprevalence, the steep gradient of seropositivity from Wuhan to Hubei-ex-Wuhan to the other provinces, and the high correlation with COVID-19 incidence provide evidence supporting the impact of China's centrally-coordinated, locally-implemented, "whole-of-government, whole-of-society" effort to contain the coronavirus. The low seroprevalence shows that the first wave of COVID-19 infected a relatively small number of individuals in China, leaving virtually the entire population susceptible to SARS-CoV-2 infection. That most infections were asymptomatic supports the importance of contact tracing strategies to stop transmission. Long-term protection of the population and the economy will necessitate using COVID-19 vaccination strategies to safely immunize populations and enable selective lifting of non-pharmaceutical interventions that are currently maintaining elimination of SARS-CoV-2 transmission. Prevention and control of COVID-19 will be a long-term effort, requiring considerable domestic work and effective global collaboration. In late December 2019, a cluster of patients with severe pneumonia of unknown etiology (PUE) was reported. A new coronavirus, now called SARS-CoV-2, was discovered in the PUE patients' bronchoaveolar lavage fluids (BALF), identified, and sequenced, and was reported to the World Health Organization (WHO) [1], [2], [3]. SARS-CoV-2 is highly contagious, and its human disease, COVID-19, causes significant morbidity and mortality [4]. WHO declared COVID-19 as a pandemic on March 11, 2020, and by the end of November, there have been over 62 million cases and 1.4 million deaths reported worldwide [5]. China took unprecedented stringent measures in response to COVID-19, managing it as a Category A disease (the highest level) with a centrally-coordinated, locally-implemented, "whole-of-government, whole-of-society" effort to contain the virus geographically and stop its transmission. Active case finding and isolation, contact tracing and management were implemented throughout China, and physical distancing measures were implemented in varying degrees depending on local transmission risk [6,7]. Lockdown travel restrictions were implemented for Wuhan City on January 23. After an epidemic surge of two months, the incidence of COVID-19 declined. By the end of March, 81,554 confirmed COVID-19 cases had been reported throughout China - 50,007 from Wuhan [8]. After confirming lack of local transmission, the Chinese government lifted Wuhan travel restrictions on April 8, 2020. The end of the first wave of the COVID-19 epidemic in the first country affected by the pandemic provides an opportunity to assess the extent of infection of the population following a managed epidemic wave. COVID-19 surveillance and reporting in China mainly relies on polymerase chain reaction (PCR)–based testing of symptomatic individuals and close contacts of the infected persons. However, extent of infection can only be determined by population-based serological surveys, as asymptomatic infections are invisible to symptom-based surveillance, and individuals not seeking medical care would be unlikely to be id
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