Articles Evolving epidemiology and transmission dynamics of coronavirus disease 2019 outside Hubei province, China: a descriptive and modelling study Juanjuan Zhang*, Maria Litvinova*, Wei Wang*, Yan Wang, Xiaowei Deng, Xinghui Chen, Mei Li, Wen Zheng, Lan Yi, Xinhua Chen, Qianhui Wu, Yuxia Liang, Xiling Wang, Juan Yang, Kaiyuan Sun, Ira M Longini Jr, M Elizabeth Halloran, Peng Wu, Benjamin J Cowling, Stefano Merler, Cecile Viboud, Alessandro Vespignani, Marco Ajelli†, Hongjie Yu† Summary Background The coronavirus disease 2019 (COVID-19) epidemic, caused by severe acute respiratory syndrome Lancet Infect Dis 2020 coronavirus 2 (SARS-CoV-2), began in Wuhan city, Hubei province, in December, 2019, and has spread throughout Published Online China. Understanding the evolving epidemiology and transmission dynamics of the outbreak beyond Hubei would April 2, 2020 provide timely information to guide intervention policy. https://doi.org/10.1016/ S1473-3099(20)30230-9 See Online/Comment Methods We collected individual information from official public sources on laboratory-confirmed cases reported https://doi.org/10.1016/ outside Hubei in mainland China for the period of Jan 19 to Feb 17, 2020. We used the date of the fourth revision of S1473-3099(20)30264-4 the case definition (Jan 27) to divide the epidemic into two time periods (Dec 24 to Jan 27, and Jan 28 to Feb 17) as the *Contributed equally date of symptom onset. We estimated trends in the demographic characteristics of cases and key time-to-event †Contributed equally intervals. We used a Bayesian approach to estimate the dynamics of the net reproduction number (Rt) at the provincial School of Public Health, Fudan level. University, Key Laboratory of Public Health Safety, Ministry Findings We collected data on 8579 cases from 30 provinces. The median age of cases was 44 years (33–56), with an of Education, Shanghai, China (J Zhang PhD, W Wang MSc, increasing proportion of cases in younger age groups and in elderly people (ie, aged >64 years) as the epidemic Y Wang MSc, X Deng MSc, progressed. The mean time from symptom onset to hospital admission decreased from 4·4 days (95% CI 0·0–14·0) Xing Chen BSc, M Li MSc, for the period of Dec 24 to Jan 27, to 2·6 days (0·0–9·0) for the period of Jan 28 to Feb 17. The mean incubation period W Zheng BSc, L Yi, Xin Chen BSc, for the entire period was estimated at 5·2 days (1·8–12·4) and the mean serial interval at 5·1 days (1·3–11·6). The Q Wu BSc, Y Liang BSc, X Wang PhD, J Yang PhD, epidemic dynamics in provinces outside Hubei were highly variable but consistently included a mixture of case Prof H Yu PhD); ISI Foundation, importations and local transmission. We estimated that the epidemic was self-sustained for less than 3 weeks, with Turin, Italy (M Litvinova PhD, mean Rt reaching peaks between 1·08 (95% CI 0·74–1·54) in Shenzhen city of Guangdong province and Prof A Vespignani PhD); Division 1·71 (1·32–2·17) in Shandong province. In all the locations for which we had sufficient data coverage of Rt, Rt was of International Epidemiology and Population Studies, estimated to be below the epidemic threshold (ie, <1) after Jan 30. Fogarty International Center, National Institutes of Health, Interpretation Our estimates of the incubation period and serial interval were similar, suggesting an early peak of Bethesda, MD, USA (K Sun PhD, infectiousness, with possible transmission before the onset of symptoms. Our results also indicate that, as the C Viboud PhD); Department of Biostatistics, College of Public epidemic progressed, infectious individuals were isolated more quickly, thus shortening the window of transmission Health, Health Professions, and in the community. Overall, our findings indicate that strict containment measures, movement restrictions, and Emerging Pathogens Institute, increased awareness of the population might have contributed to interrupt local transmission of SARS-CoV-2 outside University of Florida, Gainesville, FL, USA Hubei province. (Prof I M Longini Jr PhD); Vaccine and Infectious Disease Funding National Science Fund for Distinguished Young Scholars, National Institute of General Medical Sciences, Division, Fred Hutchinson and European Commission Horizon 2020. Cancer Research Center, Seattle, WA, USA (Prof M E Halloran DSc); Copyright © 2020 Elsevier Ltd. All rights reserved. Department of Biostatistics, University of Washington, Introduction An early report5 on the epidemiology of the COVID-19 Seattle, WA, USA (Prof M E Halloran); WHO Since December, 2019, an increasing number of atypical outbreak included analysis of the first 425 confirmed cases Collaborating Centre for pneumonia cases caused by severe acute respiratory detected in Wuhan up to Jan 22, 2020. Since then, the Infectious Disease syndrome coronavirus 2 (SARS-CoV-2) have been reported temporal dynamics and spatial dissemination of COVID-19 Epidemiology and Control, 1 School of Public Health, Li Ka in Wuhan, a city in the Chinese province of Hubei. As of has changed, with 17% of cases reported outside of Hubei Shing Faculty of Medicine, Feb 17, 2020, 72 436 cases of coronavirus disease 2019 in mainland China as of Feb 17. In provinces outside University of Hong Kong, Hong (COVID-19), including 1868 deaths, had been reported Hubei, the COVID-19 epidemic is characterised by a Kong Special Administrative in mainland China.2 The outbreak has now spread to mixture of local transmission and importation of cases Region, China (P Wu PhD, 198 countries, areas, or territories beyond China.3 On from Hubei.6 A report6 based on the 44 672 confirmed Prof B J Cowling PhD); Bruno Kessler Foundation, Trento, Jan 30, 2020, WHO declared the COVID-19 outbreak a cases detected in mainland China up to Feb 11, gave a Italy (S Merler MSc, public health emergency of international concern.4 description of the characteristics of COVID-19 cases for www.thelancet.com/infection Published online April 2, 2020 https://doi.org/10.1016/S1473-3099(20)30230-9 1 Articles M Ajelli PhD); and Laboratory for the Modeling of Biological Research in context and Socio-technical Systems, Northeastern University, Evidence before this study outside Hubei province up to Feb 17, accounting for 69% of all Boston, MA USA On March 12, 2020, we searched PubMed and Web of Science 12 447 reported cases at that time. We analysed changes in (Prof A Vespignani) for papers published after Jan 1, 2020, using the search terms demographic characteristics, key time-to-event intervals Correspondence to: (“nCoV” OR “COVID” OR “novel coronavirus” OR “severe acute (eg, incubation period, serial interval, and time from symptom Dr Marco Ajelli, Bruno Kessler respiratory syndrome coronavirus 2”) AND (“evolving onset to hospital admission), and the dynamics of the net Foundation, Trento, Italy [email protected] epidemiology” OR “epidemiological characteristics” OR reproduction number (Rt) at the provincial level. We found or “transmission dynamics” OR “net reproduction number”). significant differences in the epidemiology of COVID-19 as the Prof Hongjie Yu, Fudan No language restrictions were applied. We identified 24 papers epidemic continued to spread across China. The time from University, School of Public published in peer-reviewed journals. We also included two symptom onset to hospital admission decreased from 4·4 days Health, Key Laboratory of Public relevant papers that had yet to be indexed by PubMed or (95% CI 0·0–14·0) in the period of Dec 24 to Jan 27, to 2·6 days Health Safety, Ministry of Web of Science. The study of the first confirmed 425 cases (0·0–9·0) in the period from Jan 28 to Feb 17. The mean Education, Shanghai 200032, China in Wuhan reported a mean incubation period of 5·2 days and incubation period was estimated at 5·2 days (95% CI 1·8–12·4) [email protected] a mean serial interval of 7·5 days. One study, based on and the mean serial interval at 5·1 days (1·3–11·6). 291 patients in China, estimated a median incubation period Most importantly, as of Feb 8, 2020, we estimated Rt to be of 4 days, and another four studies estimated the incubation below the epidemic threshold in provinces outside Hubei that period of cases outside Wuhan or Hubei ranging from 5 to have reported the largest number of cases (Hunan, Shandong, 6·7 days. One mathematical modelling study estimated that Shenzhen city [Guangdong province], Anhui, Henan, the median daily net reproduction number in Wuhan declined Jiangsu, Jiangxi, Shaanxi, and Zhejiang). from 2·35 (95% CI 1·15–4·77) 1 week before travel restrictions Implications of all the available evidence were introduced on Jan 23 to 1·05 (0·41–2·39) 1 week after. We show that the epidemiology and transmission dynamics of A report from the Chinese Center for Disease Control and the COVID-19 epidemic are rapidly changing and should be Prevention that was based on the analysis of 44 672 confirmed closely monitored. Our findings suggest that strict containment cases up to Feb 11, 2020, provided an overall description of measures, movement restrictions, and increased awareness of the characteristics of coronavirus disease 2019 (COVID-19) the population might have contributed to controlling the cases in China as a whole and in Hubei province. However, that COVID-19 outbreak outside Hubei province in China. Given that study did not provide estimates of key time-to-event intervals the reproduction number is positively related to the growth rate nor of the reproduction number. Until now, there has been of the epidemic and the length of the serial interval, the shorter scarce information to understand the changing serial interval estimated here (5·1 days vs 7·5 days) implies that epidemiological features and transmission dynamics of the transmissibility of severe acute respiratory syndrome COVID-19 outbreak beyond Hubei province.