Adjusted control rate closely associated with the epidemiologic evolution of the recent COVID-19 wave in Shanghai, with 94.3% of all new cases being asymptomatic on first diagnosis

Abstract

•In the recent omicron wave in Shanghai, 94.3% were asymptomatic, 3.8% of whom became symptomatic later.•The raw case fatality rate was 0.1% in all positive cases and 1.0% in all symptomatic cases.•Numbers of newly identified non-quarantined and daily new cases peaked on April 2 and 13, respectively.•The adjusted control rate (ACR) closely associated with the evolution of the omicron wave.•ACR increased in a linear manner from April 4 (94.4%) to 29 (100.0%), and remained nearly 100.0% until June 1. AbbreviationsADNCadjusted daily new casesTACtransformed asymptomatic casesACRadjusted control rateA prospective contact-tracing study1Huang L. Zhang X. Zhang X. et al.Rapid asymptomatic transmission of COVID-19 during the incubation period demonstrating strong infectivity in a cluster of youngsters aged 16-23 years outside Wuhan and characteristics of young patients with COVID-19: a prospective contact-tracing study.J Infect. 2020; 80: e1-e13Abstract Full Text Full Text PDF PubMed Scopus (215) Google Scholar previously published in Journal of Infection showed that COVID-19 caused by SARS-CoV-2 could be rapidly and efficiently transmitted from asymptomatic cases during the incubation period, demonstrating strong infectivity, and that COVID-19 developed in younger people had fast onset and nonspecific atypical manifestations much milder than in older patients. Close to the end of February, and right before the start of spring in 2022, a wave of COVID-19 emerged and quickly spread in Shanghai, China, with a population of 24.9 million. Based on data from the Shanghai Municipal Health Commission (https://wsjkw.sh.gov.cn/yqfk2020/), as of June 20, 2022, a total of 627,116 cases have been infected, including 591,511 (94.3%) asymptomatic carriers and 35,605 (5.7%) symptomatic cases on first diagnosis; 22,515 (3.8%) asymptomatic carriers on first diagnosis transformed to symptomatic cases during the later disease course; SARS-CoV-2 has directly or indirectly caused 588 deaths, with a raw case fatality rate of 0.1% in all positive cases, 1.0% in all symptomatic cases including those transformed from asymptomatic carriers on first diagnosis, and 1.7% in symptomatic cases on first diagnosis. It is deducible that without strict and comprehensive control measures, more cases may have died. The BA.2.2 sub-lineage of the omicron variant of SARS-CoV-2 (B.1.1.529)2Lippi G. Nocini R. Henry B.M. Analysis of online search trends suggests that SARS-CoV-2 Omicron (B.1.1.529) variant causes different symptoms.J Infect. 2022; 84: e76-ee7Abstract Full Text Full Text PDF PubMed Scopus (7) Google Scholar, 3Zhang Y. Li J. Jiang L. et al.Comparison of SARS-CoV-2 aerosol emission from patients with Omicron BA.1 or BA.2 subvariant infection.J Infect. 2022; Abstract Full Text Full Text PDF Scopus (1) Google Scholar, 4Hirotsu Y. Maejima M. Shibusawa M. et al.SARS-CoV-2 Omicron sublineage BA.2 replaces BA.1.1: genomic surveillance in Japan from September 2021 to March 2022.J Infect. 2022; Abstract Full Text Full Text PDF PubMed Scopus (6) Google Scholar, 5Dimeglio C. Loubes J.M. Migueres M. et al.Influence of vaccination and prior immunity on the dynamics of Omicron BA.1 and BA.2 sub-variants.J Infect. 2022; 84: 834-872Abstract Full Text Full Text PDF PubMed Scopus (3) Google Scholar with an R0 of 9.5 was identified as the culprit for this COVID-19 wave, while worldwide it only comprises a minor proportion of BA.2 (0.3% in the GISAID database); the feature mutations of BA.2.2 was not significantly associated with disease severity.6Zhang X. Zhang W. Chen S. Shanghai's life-saving efforts against the current omicron wave of the COVID-19 pandemic.Lancet. 2022; 399: 2011-2012Abstract Full Text Full Text PDF PubMed Scopus (34) Google Scholar With the implementation of strict and comprehensive public health measures with unprecedented joint efforts including largescale SARS-CoV-2 RNA and antigen testing for early diagnosis, timely quarantine of infected cases and tracing of close contacts, construction of shelter hospitals of different sizes in different locations, and lockdown of places with severe outbreaks, the situation has currently been well under control. The zero COVID-19 policy is operational in, and rather unique to China, as it is no longer employed in other countries. Dynamic zero COVID-19 community transmission was first achieved on April 29, 2022, and the number of daily new cases has now dropped to only 9, as of June 20, 2022 (Fig. 1). Resumption to normal life and work has been ongoing gradually and orderly.Looking into the epidemiologic evolution of the omicron wave, several intriguing aspects are noteworthy. The numbers of new cases by date are distributed in an almost symmetric manner, with the symmetry axis on April 13, 2022 when the number of adjusted daily new cases (ADNC; the number of reported new cases minus the number of transformed asymptomatic cases (TAC), define as symptomatic cases deriving from previously identified asymptotic cases) peaked at 27,605 (Fig. 1A). From April 7 when the ADNC first surpassed 20,000, there existed a significant number (Fig. 1B) and proportion (Fig. 1C) of TAC, and the number remained at a high level until May 1, 2022, and first dropped to below 50 on May 15, 2022. To control COVID-19, it would be important to early identify and quickly quarantine all newly infected cases, and the cases diagnosed in people not undergoing quarantine may indicate community transmission and pose a great challenge to COVID-19 control. The number of newly identified non-quarantined cases peaked at 1364 on April 2, 2022, 11 days before the peak day of new cases, and was also distributed almost symmetrically (Fig. 1D). The control rate, which is defined as the proportion of new cases identified in quarantined people relative to all new cases, may be closely associated with the evolution of the COVID-19 wave, and the adjusted control rate (ACR) with removal of transformed asymptotic cases in all new cases may be an even more robust indicator (Fig. 1E). During the initial phase of this wave, the ACR dropped to 40.4% on March 17, 2022, and then quickly returned to 88.9% on March 20, 2022, after which the ACR remained fluctuating until April 3, 2022 with the number of ADNC of 8935. Since April 4, 2022, when the ADNC number (13,350) first surpassed 10,000 (which might be associated with more comprehensive quarantine measures), the ACR increased in an almost linear manner until 100.0% with the first dynamic zero COVID-19 community transmission achieved on April 29, 2022, 16 days after the peak day of new cases (the peak day was 9 days after the start of this period) and 2 days after the first day with the number of ADNC first returning to below 10,000 (Fig. 1F). The period April 4 to 29, 2022 might represent an extremely important and critical period with numerous joint efforts and comprehensive control interventions which efficiently blocked the exacerbation of the wave and brought the situation under control. Between April 30 and June 1, 2022, the ACR remained nearly 100.0% with zero new cases identified in the non-quarantined community through repeated SARS-CoV-2 screening, and the number of ADNC first dropped to below 100 on May 29, 2022, and further decreased to only 10 on June 1, 2022, when people in Shanghai started to resume to normal activities. Between June 2 and 12, 2022, the ACR fluctuated largely (45.5% to 100.0%), and the number of ADNC returned to 36 on June 12, 2022. From June 13 until 20, 2022, the fluctuation degree of the ACR became smaller, with the number of new cases identified in non-quarantined people ranging between 0 and 3. Currently, proof of negative SARS-CoV-2 RNA test within 2 or 3 days is a necessity for using public transport and entering certain public places, and there are many fixed points offering free SARS-CoV-2 RNA tests, the results of which could usually be returned on the same day. This ensured active dynamic COVID-19 surveillance with large coverage during people resuming to normal activities. Notably, from time to time positive cases could still be detected in the non-quarantined community, indicating the possibly continuing risk of community transmission. The majority (94.3%) of newly diagnosed cases were asymptomatic, based on thorough, repeated, and combined SARS-CoV-2 RNA and antigen screening. Between April 4 and 26, 2022, when the ADNC number were above 10,000, the adjusted proportion of new symptomatic cases ranged between 1.5% and 12.7% (Fig. 1G). Except the outlier, the number of daily new symptomatic cases peaked at 3590 on April 15, 2022 (Fig. 1H), and the number of new asymptomatic cases were highest (25,173) on April 10, 2022 (Fig. 1I).Together, this report on the recent omicron wave in Shanghai with some new concepts like ACR proposed may provide important epidemiologic dynamics data as useful hints and references for COVID-19 prevention, surveillance, and control. The zero COVID-19 policy is operational in, and now unique to China. Still, besides vaccination, timely, powerful, precise, stratified, and dynamic prevention and control measures including the One Health approach are greatly warranted to effectively and efficiently control the COVID-19 pandemic.1Huang L. Zhang X. Zhang X. et al.Rapid asymptomatic transmission of COVID-19 during the incubation period demonstrating strong infectivity in a cluster of youngsters aged 16-23 years outside Wuhan and characteristics of young patients with COVID-19: a prospective contact-tracing study.J Infect. 2020; 80: e1-e13Abstract Full Text Full Text PDF PubMed Scopus (215) Google Scholar,7Huang L. Zhang X. Xu A. Effectiveness of interventions as part of the One Health approach to control coronavirus disease 2019 and stratified case features in Anhui Province, China: a real-world population-based cohort study.One Health. 2021; 12100224Crossref PubMed Scopus (6) Google Scholar, 8Huang L. Zhang X. Zhang L. et al.Swab and sputum SARS-CoV-2 RNA-negative, CT-positive, symptomatic contacts of COVID-19 cases: a hypothesis-generating prospective population-based cohort study of eight clusters.Front Med. 2021; 8685544Google Scholar, 9Huang L. Liang P. Xu Y. Xu A. Wei Z. Development of coagulation disorders, malnutrition, and anaemia and duration of virus shedding in COVID-19: implications for disease mechanism and management.Int J Clin Pract. 2021; 75: e14353Crossref PubMed Scopus (2) Google Scholar, 10Huang L. Computed tomography-positive, SARS-CoV-2 RNA-negative symptomatic contacts of COVID-19 patients: what are their nature and implications?.Future Virol. 2021; Crossref PubMed Scopus (1) Google ScholarAuthor’ contributionsConception or design: Huang L. Acquisition, analysis, or interpretation of data: Huang L. Drafting of the manuscript: Huang L. Critical revision of the manuscript for important intellectual content: Huang L. Statistical analysis: Huang L. Administrative, technical, or material support: Huang L. Huang L has approved the current version of the manuscript for submission and publication. AbbreviationsADNCadjusted daily new casesTACtransformed asymptomatic casesACRadjusted control rate adjusted daily new cases transformed asymptomatic cases adjusted control rate A prospective contact-tracing study1Huang L. Zhang X. Zhang X. et al.Rapid asymptomatic transmission of COVID-19 during the incubation period demonstrating strong infectivity in a cluster of youngsters aged 16-23 years outside Wuhan and characteristics of young patients with COVID-19: a prospective contact-tracing study.J Infect. 2020; 80: e1-e13Abstract Full Text Full Text PDF PubMed Scopus (215) Google Scholar previously published in Journal of Infection showed that COVID-19 caused by SARS-CoV-2 could be rapidly and efficiently transmitted from asymptomatic cases during the incubation period, demonstrating strong infectivity, and that COVID-19 developed in younger people had fast onset and nonspecific atypical manifestations much milder than in older patients. Close to the end of February, and right before the start of spring in 2022, a wave of COVID-19 emerged and quickly spread in Shanghai, China, with a population of 24.9 million. Based on data from the Shanghai Municipal Health Commission (https://wsjkw.sh.gov.cn/yqfk2020/), as of June 20, 2022, a total of 627,116 cases have been infected, including 591,511 (94.3%) asymptomatic carriers and 35,605 (5.7%) symptomatic cases on first diagnosis; 22,515 (3.8%) asymptomatic carriers on first diagnosis transformed to symptomatic cases during the later disease course; SARS-CoV-2 has directly or indirectly caused 588 deaths, with a raw case fatality rate of 0.1% in all positive cases, 1.0% in all symptomatic cases including those transformed from asymptomatic carriers on first diagnosis, and 1.7% in symptomatic cases on first diagnosis. It is deducible that without strict and comprehensive control measures, more cases may have died. The BA.2.2 sub-lineage of the omicron variant of SARS-CoV-2 (B.1.1.529)2Lippi G. Nocini R. Henry B.M. Analysis of online search trends suggests that SARS-CoV-2 Omicron (B.1.1.529) variant causes different symptoms.J Infect. 2022; 84: e76-ee7Abstract Full Text Full Text PDF PubMed Scopus (7) Google Scholar, 3Zhang Y. Li J. Jiang L. et al.Comparison of SARS-CoV-2 aerosol emission from patients with Omicron BA.1 or BA.2 subvariant infection.J Infect. 2022; Abstract Full Text Full Text PDF Scopus (1) Google Scholar, 4Hirotsu Y. Maejima M. Shibusawa M. et al.SARS-CoV-2 Omicron sublineage BA.2 replaces BA.1.1: genomic surveillance in Japan from September 2021 to March 2022.J Infect. 2022; Abstract Full Text Full Text PDF PubMed Scopus (6) Google Scholar, 5Dimeglio C. Loubes J.M. Migueres M. et al.Influence of vaccination and prior immunity on the dynamics of Omicron BA.1 and BA.2 sub-variants.J Infect. 2022; 84: 834-872Abstract Full Text Full Text PDF PubMed Scopus (3) Google Scholar with an R0 of 9.5 was identified as the culprit for this COVID-19 wave, while worldwide it only comprises a minor proportion of BA.2 (0.3% in the GISAID database); the feature mutations of BA.2.2 was not significantly associated with disease severity.6Zhang X. Zhang W. Chen S. Shanghai's life-saving efforts against the current omicron wave of the COVID-19 pandemic.Lancet. 2022; 399: 2011-2012Abstract Full Text Full Text PDF PubMed Scopus (34) Google Scholar With the implementation of strict and comprehensive public health measures with unprecedented joint efforts including largescale SARS-CoV-2 RNA and antigen testing for early diagnosis, timely quarantine of infected cases and tracing of close contacts, construction of shelter hospitals of different sizes in different locations, and lockdown of places with severe outbreaks, the situation has currently been well under control. The zero COVID-19 policy is operational in, and rather unique to China, as it is no longer employed in other countries. Dynamic zero COVID-19 community transmission was first achieved on April 29, 2022, and the number of daily new cases has now dropped to only 9, as of June 20, 2022 (Fig. 1). Resumption to normal life and work has been ongoing gradually and orderly. Looking into the epidemiologic evolution of the omicron wave, several intriguing aspects are noteworthy. The numbers of new cases by date are distributed in an almost symmetric manner, with the symmetry axis on April 13, 2022 when the number of adjusted daily new cases (ADNC; the number of reported new cases minus the number of transformed asymptomatic cases (TAC), define as symptomatic cases deriving from previously identified asymptotic cases) peaked at 27,605 (Fig. 1A). From April 7 when the ADNC first surpassed 20,000, there existed a significant number (Fig. 1B) and proportion (Fig. 1C) of TAC, and the number remained at a high level until May 1, 2022, and first dropped to below 50 on May 15, 2022. To control COVID-19, it would be important to early identify and quickly quarantine all newly infected cases, and the cases diagnosed in people not undergoing quarantine may indicate community transmission and pose a great challenge to COVID-19 control. The number of newly identified non-quarantined cases peaked at 1364 on April 2, 2022, 11 days before the peak day of new cases, and was also distributed almost symmetrically (Fig. 1D). The control rate, which is defined as the proportion of new cases identified in quarantined people relative to all new cases, may be closely associated with the evolution of the COVID-19 wave, and the adjusted control rate (ACR) with removal of transformed asymptotic cases in all new cases may be an even more robust indicator (Fig. 1E). During the initial phase of this wave, the ACR dropped to 40.4% on March 17, 2022, and then quickly returned to 88.9% on March 20, 2022, after which the ACR remained fluctuating until April 3, 2022 with the number of ADNC of 8935. Since April 4, 2022, when the ADNC number (13,350) first surpassed 10,000 (which might be associated with more comprehensive quarantine measures), the ACR increased in an almost linear manner until 100.0% with the first dynamic zero COVID-19 community transmission achieved on April 29, 2022, 16 days after the peak day of new cases (the peak day was 9 days after the start of this period) and 2 days after the first day with the number of ADNC first returning to below 10,000 (Fig. 1F). The period April 4 to 29, 2022 might represent an extremely important and critical period with numerous joint efforts and comprehensive control interventions which efficiently blocked the exacerbation of the wave and brought the situation under control. Between April 30 and June 1, 2022, the ACR remained nearly 100.0% with zero new cases identified in the non-quarantined community through repeated SARS-CoV-2 screening, and the number of ADNC first dropped to below 100 on May 29, 2022, and further decreased to only 10 on June 1, 2022, when people in Shanghai started to resume to normal activities. Between June 2 and 12, 2022, the ACR fluctuated largely (45.5% to 100.0%), and the number of ADNC returned to 36 on June 12, 2022. From June 13 until 20, 2022, the fluctuation degree of the ACR became smaller, with the number of new cases identified in non-quarantined people ranging between 0 and 3. Currently, proof of negative SARS-CoV-2 RNA test within 2 or 3 days is a necessity for using public transport and entering certain public places, and there are many fixed points offering free SARS-CoV-2 RNA tests, the results of which could usually be returned on the same day. This ensured active dynamic COVID-19 surveillance with large coverage during people resuming to normal activities. Notably, from time to time positive cases could still be detected in the non-quarantined community, indicating the possibly continuing risk of community transmission. The majority (94.3%) of newly diagnosed cases were asymptomatic, based on thorough, repeated, and combined SARS-CoV-2 RNA and antigen screening. Between April 4 and 26, 2022, when the ADNC number were above 10,000, the adjusted proportion of new symptomatic cases ranged between 1.5% and 12.7% (Fig. 1G). Except the outlier, the number of daily new symptomatic cases peaked at 3590 on April 15, 2022 (Fig. 1H), and the number of new asymptomatic cases were highest (25,173) on April 10, 2022 (Fig. 1I). Together, this report on the recent omicron wave in Shanghai with some new concepts like ACR proposed may provide important epidemiologic dynamics data as useful hints and references for COVID-19 prevention, surveillance, and control. The zero COVID-19 policy is operational in, and now unique to China. Still, besides vaccination, timely, powerful, precise, stratified, and dynamic prevention and control measures including the One Health approach are greatly warranted to effectively and efficiently control the COVID-19 pandemic.1Huang L. Zhang X. Zhang X. et al.Rapid asymptomatic transmission of COVID-19 during the incubation period demonstrating strong infectivity in a cluster of youngsters aged 16-23 years outside Wuhan and characteristics of young patients with COVID-19: a prospective contact-tracing study.J Infect. 2020; 80: e1-e13Abstract Full Text Full Text PDF PubMed Scopus (215) Google Scholar,7Huang L. Zhang X. Xu A. Effectiveness of interventions as part of the One Health approach to control coronavirus disease 2019 and stratified case features in Anhui Province, China: a real-world population-based cohort study.One Health. 2021; 12100224Crossref PubMed Scopus (6) Google Scholar, 8Huang L. Zhang X. Zhang L. et al.Swab and sputum SARS-CoV-2 RNA-negative, CT-positive, symptomatic contacts of COVID-19 cases: a hypothesis-generating prospective population-based cohort study of eight clusters.Front Med. 2021; 8685544Google Scholar, 9Huang L. Liang P. Xu Y. Xu A. Wei Z. Development of coagulation disorders, malnutrition, and anaemia and duration of virus shedding in COVID-19: implications for disease mechanism and management.Int J Clin Pract. 2021; 75: e14353Crossref PubMed Scopus (2) Google Scholar, 10Huang L. Computed tomography-positive, SARS-CoV-2 RNA-negative symptomatic contacts of COVID-19 patients: what are their nature and implications?.Future Virol. 2021; Crossref PubMed Scopus (1) Google Scholar Author’ contributionsConception or design: Huang L. Acquisition, analysis, or interpretation of data: Huang L. Drafting of the manuscript: Huang L. Critical revision of the manuscript for important intellectual content: Huang L. Statistical analysis: Huang L. Administrative, technical, or material support: Huang L. Huang L has approved the current version of the manuscript for submission and publication. Conception or design: Huang L. Acquisition, analysis, or interpretation of data: Huang L. Drafting of the manuscript: Huang L. Critical revision of the manuscript for important intellectual content: Huang L. Statistical analysis: Huang L. Administrative, technical, or material support: Huang L. Huang L has approved the current version of the manuscript for submission and publication. None exist. Gratefulness should be given to all people contributing to the control of the recent omicron wave in Shanghai.