Serial intervals and case isolation delays for COVID-19: a systematic review and meta-analysis

Abstract Background Estimates of the serial interval distribution contribute to our understanding of the transmission dynamics of coronavirus disease 2019 (COVID-19). Here, we aimed to summarize the existing evidence on serial interval distributions and delays in case isolation for COVID-19. Methods We conducted a systematic review of the published literature and preprints in PubMed on two epidemiological parameters namely serial intervals and delay intervals relating to isolation of cases for COVID-19 until 22 October, 2020 following predefined eligibility criteria. We assessed the variation in these parameter estimates by correlation and regression analysis. Results Of 103 unique studies identified on serial intervals of COVID-19, 56 were included providing 129 estimates and of 451 unique studies on isolation delays, 18 studies were included providing 74 estimates. Serial interval estimates varied from 1.0 to 9.9 days, while case isolation delays varied from 1.0 to 12.5 days which were associated with spatial, methodological and temporal factors. In mainland China, the pooled mean serial interval was 6.2 (range, 5.1-7.8) days before the epidemic peak and reduced to 4.9 (range, 1.9-6.5) days after the epidemic peak. Similarly, the pooled mean isolation delay related intervals were 6.0 (range, 2.9-12.5) days and 2.4 (range, 2.0-2.7) days before and after the epidemic peak, respectively. There was a positive association between serial interval and case isolation delay. Conclusions Temporal factors, such as different control measures and case isolation in particular led to shorter serial interval estimates over time. Correcting transmissibility estimates for these time-varying distributions could aid mitigation efforts.

[1]  F. Nolent,et al.  Investigation of a COVID-19 Outbreak on an Aircraft Carrier: An Epidemic Model Based on Real Data , 2021, SSRN Electronic Journal.

[2]  A. Vespignani,et al.  Infectivity, susceptibility, and risk factors associated with SARS-CoV-2 transmission under intensive contact tracing in Hunan, China , 2021, Nature Communications.

[3]  A. Vespignani,et al.  Transmission heterogeneities, kinetics, and controllability of SARS-CoV-2 , 2020, Science.

[4]  J. M. Griffin,et al.  Rapid review of available evidence on the serial interval and generation time of COVID-19 , 2020, BMJ Open.

[5]  H. Nair,et al.  The temporal association of introducing and lifting non-pharmaceutical interventions with the time-varying reproduction number (R) of SARS-CoV-2: a modelling study across 131 countries , 2020, The Lancet Infectious Diseases.

[6]  L. Naing,et al.  Analysis of SARS-CoV-2 Transmission in Different Settings, Brunei , 2020, Emerging infectious diseases.

[7]  Chong You,et al.  Epidemiological Characteristics and Factors Associated with Critical Time Intervals of COVID-19 in Eighteen Provinces, China: A Retrospective Study , 2020, International Journal of Infectious Diseases.

[8]  Stefan Ma,et al.  Effectiveness of Containment Measures Against COVID-19 in Singapore , 2020, Epidemiology.

[9]  Zigui Chen,et al.  Stringent containment measures without complete city lockdown to achieve low incidence and mortality across two waves of COVID-19 in Hong Kong , 2020, BMJ Global Health.

[10]  L. Fang,et al.  Epidemiological parameters of COVID-19 and its implication for infectivity among patients in China, 1 January to 11 February 2020 , 2020, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[11]  M. K. Verma,et al.  Transmission Dynamics of the COVID-19 Epidemic at the District Level in India: Prospective Observational Study , 2020, JMIR public health and surveillance.

[12]  M. Wang,et al.  Epidemiological Parameters of COVID-19: Case Series Study , 2020, Journal of medical Internet research.

[13]  Expert Taskforce Epidemiology of COVID-19 Outbreak on Cruise Ship Quarantined at Yokohama, Japan, February 2020 , 2020, Emerging infectious diseases.

[14]  Tzeng-Ji Chen,et al.  Analysis of community-acquired COVID-19 cases in Taiwan , 2020, Journal of the Chinese Medical Association : JCMA.

[15]  G. Gao,et al.  Evidence for pre‐symptomatic transmission of coronavirus disease 2019 (COVID‐19) in China , 2020, Influenza and other respiratory viruses.

[16]  Marloes H. Maathuis,et al.  Diagnostic serial interval as a novel indicator for contact tracing effectiveness exemplified with the SARS-CoV-2/COVID-19 outbreak in South Korea , 2020, International Journal of Infectious Diseases.

[17]  Yongdai Kim,et al.  Transmission onset distribution of COVID-19 , 2020, International Journal of Infectious Diseases.

[18]  Zhihang Peng,et al.  COVID-19 Outbreak Following a Single Patient Exposure at an Entertainment Site: An Epidemiological Study. , 2020, Transboundary and emerging diseases.

[19]  E. Lau,et al.  Serial interval of SARS-CoV-2 was shortened over time by nonpharmaceutical interventions , 2020, Science.

[20]  N. J. Haw,et al.  Epidemiological profile and transmission dynamics of COVID-19 in the Philippines , 2020, Epidemiology and Infection.

[21]  A. Londei,et al.  Ranking the effectiveness of worldwide COVID-19 government interventions , 2020, Nature Human Behaviour.

[22]  Yukun Liu,et al.  Estimation of incubation period and generation time based on observed length‐biased epidemic cohort with censoring for COVID‐19 outbreak in China , 2020, Biometrics.

[23]  A. Deng,et al.  [Analysis on the cluster epidemic of coronavirus disease 2019 in Guangdong Province]. , 2020, Zhonghua yu fang yi xue za zhi [Chinese journal of preventive medicine].

[24]  H. Kwon,et al.  Epidemiological Characteristics of COVID-19 Outbreak at Fitness Centers in Cheonan, Korea , 2020, Journal of Korean medical science.

[25]  Y. Lyu,et al.  The descriptive epidemiology of coronavirus disease 2019 during the epidemic period in Lu'an, China: achieving limited community transmission using proactive response strategies , 2020, Epidemiology and Infection.

[26]  S. Bhatt,et al.  Suppression of a SARS-CoV-2 outbreak in the Italian municipality of Vo’ , 2020, Nature.

[27]  Zigui Chen,et al.  Epidemiological characteristics of the first 100 cases of coronavirus disease 2019 (COVID-19) in Hong Kong Special Administrative Region, China, a city with a stringent containment policy , 2020, International journal of epidemiology.

[28]  L. Naing,et al.  Epidemiological Investigation of the First 135 COVID-19 Cases in Brunei: Implications for Surveillance, Control, and Travel Restrictions , 2020, medRxiv.

[29]  Wing Yin Venus Lau,et al.  Evidence for transmission of COVID-19 prior to symptom onset , 2020, eLife.

[30]  S. Chuang,et al.  The epidemiology of COVID-19 cases and the successful containment strategy in Hong Kong–January to May 2020 , 2020, International Journal of Infectious Diseases.

[31]  V. Viego,et al.  Incubation period and serial interval of Covid-19 in a chain of infections in Bahia Blanca (Argentina) , 2020, medRxiv.

[32]  L. Yang,et al.  Estimation of incubation period and serial interval of COVID-19: analysis of 178 cases and 131 transmission chains in Hubei province, China , 2020, Epidemiology and Infection.

[33]  Xiao Fan Liu,et al.  Reconstruction of Transmission Pairs for Novel Coronavirus Disease 2019 (COVID-19) in Mainland China: Estimation of Superspreading Events, Serial Interval, and Hazard of Infection , 2020, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[34]  F. Najafi,et al.  Serial interval and time-varying reproduction number estimation for COVID-19 in western Iran , 2020, New Microbes and New Infections.

[35]  Nuno R. Faria,et al.  Serial interval distribution of SARS-CoV-2 infection in Brazil , 2020, medRxiv.

[36]  B. Cowling,et al.  Effect of Nonpharmaceutical Interventions on Transmission of Severe Acute Respiratory Syndrome Coronavirus 2, South Korea, 2020 , 2020, Emerging infectious diseases.

[37]  Hyojung Lee,et al.  Epidemiological characteristics of and containment measures for COVID-19 in Busan, Korea , 2020, Epidemiology and health.

[38]  R. Nikbakht,et al.  Estimation of the serial interval and basic reproduction number of COVID‐19 in Qom, Iran, and three other countries: A data‐driven analysis in the early phase of the outbreak , 2020, Transboundary and emerging diseases.

[39]  D. He,et al.  Estimating the serial interval of the novel coronavirus disease (COVID‐19) based on the public surveillance data in Shenzhen, China, from 19 January to 22 February 2020 , 2020, Transboundary and emerging diseases.

[40]  J. Knight,et al.  Estimating effective reproduction number using generation time versus serial interval, with application to covid-19 in the Greater Toronto Area, Canada , 2020, Infectious Disease Modelling.

[41]  L. Naing,et al.  What do we know about SARS-CoV-2 transmission? A systematic review and meta-analysis of the secondary attack rate, serial interval, and asymptomatic infection , 2020, medRxiv.

[42]  Marc Choisy,et al.  The first 100 days of SARS-CoV-2 control in Vietnam , 2020, medRxiv.

[43]  Victor M Corman,et al.  Investigation of a COVID-19 outbreak in Germany resulting from a single travel-associated primary case: a case series , 2020, The Lancet Infectious Diseases.

[44]  S. Gu,et al.  [Study on transmission dynamic of 15 clusters of coronavirus disease 2019 cases in Ningbo]. , 2020, Zhonghua liu xing bing xue za zhi = Zhonghua liuxingbingxue zazhi.

[45]  C. Macintyre,et al.  Basic epidemiological parameter values from data of real-world in mega-cities: the characteristics of COVID-19 in Beijing, China , 2020, BMC Infectious Diseases.

[46]  Ying-jian Liang,et al.  Household Transmission of SARS-CoV-2, Zhuhai, China, 2020 , 2020, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[47]  Dong Yang,et al.  Nosocomial outbreak of COVID-19 pneumonia in Wuhan, China , 2020, European Respiratory Journal.

[48]  A. Tatem,et al.  Effect of non-pharmaceutical interventions to contain COVID-19 in China , 2020, Nature.

[49]  Hsien-Ho Lin,et al.  Contact Tracing Assessment of COVID-19 Transmission Dynamics in Taiwan and Risk at Different Exposure Periods Before and After Symptom Onset , 2020, JAMA internal medicine.

[50]  M. Jit,et al.  Estimating number of cases and spread of coronavirus disease (COVID-19) using critical care admissions, United Kingdom, February to March 2020 , 2020, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[51]  H. Pan,et al.  Epidemiological and clinical characteristics of 333 confirmed cases with coronavirus disease 2019 in Shanghai, China , 2020, Transboundary and emerging diseases.

[52]  A. Vespignani,et al.  Changes in contact patterns shape the dynamics of the COVID-19 outbreak in China , 2020, Science.

[53]  Yongsheng Wu,et al.  Epidemiology and transmission of COVID-19 in 391 cases and 1286 of their close contacts in Shenzhen, China: a retrospective cohort study , 2020, The Lancet Infectious Diseases.

[54]  K. Tao,et al.  The characteristics of household transmission of COVID-19 , 2020, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[55]  Peng Wu,et al.  Impact assessment of non-pharmaceutical interventions against coronavirus disease 2019 and influenza in Hong Kong: an observational study , 2020, The Lancet Public Health.

[56]  Xihong Lin,et al.  Association of Public Health Interventions With the Epidemiology of the COVID-19 Outbreak in Wuhan, China. , 2020, JAMA.

[57]  Jingjing Xu,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 , 2020, Journal of Infection.

[58]  Gang Wu,et al.  Household transmission of SARS-CoV-2 , 2020, Journal of Infection.

[59]  Hyung-Ju Kim,et al.  The Delay in Confirming COVID-19 Cases Linked to a Religious Group in Korea , 2020, Journal of preventive medicine and public health = Yebang Uihakhoe chi.

[60]  Chonggang Xu,et al.  High Contagiousness and Rapid Spread of Severe Acute Respiratory Syndrome Coronavirus 2 , 2020, Emerging infectious diseases.

[61]  A. Vespignani,et al.  Evolving epidemiology and transmission dynamics of coronavirus disease 2019 outside Hubei province, China: a descriptive and modelling study , 2020, The Lancet Infectious Diseases.

[62]  C. Faes,et al.  Estimating the generation interval for coronavirus disease (COVID-19) based on symptom onset data, March 2020 , 2020, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[63]  J. Tang,et al.  Epidemiological characteristics of the first 53 laboratory-confirmed cases of COVID-19 epidemic in Hong Kong, 13 February 2020 , 2020, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[64]  G. Leung,et al.  First-wave COVID-19 transmissibility and severity in China outside Hubei after control measures, and second-wave scenario planning: a modelling impact assessment , 2020, The Lancet.

[65]  Minah Park,et al.  A Systematic Review of COVID-19 Epidemiology Based on Current Evidence , 2020, Journal of clinical medicine.

[66]  M. Wang,et al.  Epidemiological parameters of coronavirus disease 2019: a pooled analysis of publicly reported individual data of 1155 cases from seven countries , 2020, medRxiv.

[67]  V. Demicheli,et al.  The early phase of the COVID-19 outbreak in Lombardy, Italy , 2020, 2003.09320.

[68]  Benjamin Er,et al.  Evaluation of the Effectiveness of Surveillance and Containment Measures for the First 100 Patients with COVID-19 in Singapore — January 2–February 29, 2020 , 2020, MMWR. Morbidity and mortality weekly report.

[69]  L. Meyers,et al.  Serial Interval of COVID-19 among Publicly Reported Confirmed Cases , 2020, Emerging infectious diseases.

[70]  Eric H. Y. Lau,et al.  Temporal dynamics in viral shedding and transmissibility of COVID-19 , 2020, Nature Medicine.

[71]  P. Teunis,et al.  Strongly Heterogeneous Transmission of COVID-19 in Mainland China: Local and Regional Variation , 2020, Frontiers in Medicine.

[72]  M. Lipsitch,et al.  Estimating clinical severity of COVID-19 from the transmission dynamics in Wuhan, China , 2020, Nature Medicine.

[73]  X. Dong,et al.  [Epidemiological characteristics of confirmed COVID-19 cases in Tianjin]. , 2020, Zhonghua liu xing bing xue za zhi = Zhonghua liuxingbingxue zazhi.

[74]  Chuansha Wu,et al.  Epidemiological and Clinical Characteristics of COVID-19 in Adolescents and Young Adults , 2020, The Innovation.

[75]  Shu Huan,et al.  Transmission of corona virus disease 2019 during the incubation period may lead to a quarantine loophole , 2020, medRxiv.

[76]  N. Linton,et al.  Serial interval of novel coronavirus (COVID-19) infections , 2020, International Journal of Infectious Diseases.

[77]  P. Klepac,et al.  Feasibility of controlling COVID-19 outbreaks by isolation of cases and contacts , 2020, The Lancet Global Health.

[78]  Yongli Cai,et al.  Estimating the Serial Interval of the Novel Coronavirus Disease (COVID-19): A Statistical Analysis Using the Public Data in Hong Kong From January 16 to February 15, 2020 , 2020, Frontiers in Physics.

[79]  Yuan Zhang,et al.  Estimation of the time-varying reproduction number of COVID-19 outbreak in China , 2020, International Journal of Hygiene and Environmental Health.

[80]  Moran Ki,et al.  Epidemiologic characteristics of early cases with 2019 novel coronavirus (2019-nCoV) disease in Korea , 2020, Epidemiology and health.

[81]  Yan Zhao,et al.  Clinical Characteristics of 138 Hospitalized Patients With 2019 Novel Coronavirus-Infected Pneumonia in Wuhan, China. , 2020, JAMA.

[82]  Jing Zhao,et al.  Early Transmission Dynamics in Wuhan, China, of Novel Coronavirus–Infected Pneumonia , 2020, The New England journal of medicine.

[83]  N. Linton,et al.  Incubation Period and Other Epidemiological Characteristics of 2019 Novel Coronavirus Infections with Right Truncation: A Statistical Analysis of Publicly Available Case Data , 2020, medRxiv.

[84]  Wenjun Ma,et al.  Transmission dynamics of 2019 novel coronavirus (2019-nCoV) , 2020, bioRxiv.

[85]  Jonathan Dushoff,et al.  Inferring generation-interval distributions from contact-tracing data , 2019, bioRxiv.

[86]  D. Moher,et al.  Preferred reporting items for systematic reviews and meta-analyses: the PRISMA Statement , 2009, BMJ : British Medical Journal.

[87]  M. Lipsitch,et al.  How generation intervals shape the relationship between growth rates and reproductive numbers , 2007, Proceedings of the Royal Society B: Biological Sciences.