Skip to main content
Top
Published in: BMC Public Health 1/2021

Open Access 01-12-2021 | COVID-19 | Research

Epidemiological features of COVID-19 patients with prolonged incubation period and its implications for controlling the epidemics in China

Authors: Zhi-Jie Zhang, Tian-Le Che, Tao Wang, Han Zhao, Jie Hong, Qing Su, Hai-Yang Zhang, Shi-Xia Zhou, Ai-Ying Teng, Yuan-Yuan Zhang, Yang Yang, Li-Qun Fang, Wei Liu

Published in: BMC Public Health | Issue 1/2021

Login to get access

Abstract

Background

COVID-19 patients with long incubation period were reported in clinical practice and tracing of close contacts, but their epidemiological or clinical features remained vague.

Methods

We analyzed 11,425 COVID-19 cases reported between January–August, 2020 in China. The accelerated failure time model, Logistic and modified Poisson regression models were used to investigate the determinants of prolonged incubation period, as well as their association with clinical severity and transmissibility, respectively.

Result

Among local cases, 268 (10.2%) had a prolonged incubation period of > 14 days, which was more frequently seen among elderly patients, those residing in South China, with disease onset after Level I response measures administration, or being exposed in public places. Patients with prolonged incubation period had lower risk of severe illness (ORadjusted = 0.386, 95% CI: 0.203–0.677). A reduced transmissibility was observed for the primary patients with prolonged incubation period (50.4, 95% CI: 32.3–78.6%) than those with an incubation period of ≤14 days.

Conclusions

The study provides evidence supporting a prolonged incubation period that exceeded 2 weeks in over 10% for COVID-19. Longer monitoring periods than 14 days for quarantine or persons potentially exposed to SARS-CoV-2 should be justified in extreme cases, especially for those elderly.
Appendix
Available only for authorised users
Literature
2.
go back to reference Hassan F, Yamey G, Abbasi K. Profiteering from vaccine inequity: a crime against humanity? BMJ. 2021;374:n2027.CrossRef Hassan F, Yamey G, Abbasi K. Profiteering from vaccine inequity: a crime against humanity? BMJ. 2021;374:n2027.CrossRef
3.
go back to reference Moon S, Alonso Ruiz A, Vieira M. Averting future vaccine injustice. N Engl J Med. 2021;385(3):193–6.CrossRef Moon S, Alonso Ruiz A, Vieira M. Averting future vaccine injustice. N Engl J Med. 2021;385(3):193–6.CrossRef
4.
go back to reference Lopez Bernal J, Andrews N, Gower C, Gallagher E, Simmons R, Thelwall S, et al. Effectiveness of COVID-19 vaccines against the B.1.617.2 (delta) variant. N Engl J Med. 2021;385(7):585–94.CrossRef Lopez Bernal J, Andrews N, Gower C, Gallagher E, Simmons R, Thelwall S, et al. Effectiveness of COVID-19 vaccines against the B.1.617.2 (delta) variant. N Engl J Med. 2021;385(7):585–94.CrossRef
6.
go back to reference Duhon J, Bragazzi N, Kong JD. The impact of non-pharmaceutical interventions, demographic, social, and climatic factors on the initial growth rate of COVID-19: a cross-country study. Sci Total Environ. 2021;760:144325.CrossRef Duhon J, Bragazzi N, Kong JD. The impact of non-pharmaceutical interventions, demographic, social, and climatic factors on the initial growth rate of COVID-19: a cross-country study. Sci Total Environ. 2021;760:144325.CrossRef
7.
go back to reference Mendez-Brito A, El Bcheraoui C, Pozo-Martin F. Systematic review of empirical studies comparing the effectiveness of non-pharmaceutical interventions against COVID-19. J Inf Secur. 2021;83(3):281–93. Mendez-Brito A, El Bcheraoui C, Pozo-Martin F. Systematic review of empirical studies comparing the effectiveness of non-pharmaceutical interventions against COVID-19. J Inf Secur. 2021;83(3):281–93.
8.
go back to reference Moore S, Hill EM, Tildesley MJ, Dyson L, Keeling MJ. Vaccination and non-pharmaceutical interventions for COVID-19: a mathematical modelling study. Lancet Infect Dis. 2021;21(6):793–802.CrossRef Moore S, Hill EM, Tildesley MJ, Dyson L, Keeling MJ. Vaccination and non-pharmaceutical interventions for COVID-19: a mathematical modelling study. Lancet Infect Dis. 2021;21(6):793–802.CrossRef
10.
go back to reference Dhouib W, Maatoug J, Ayouni I, Zammit N, Ghammem R, Fredj SB, et al. The incubation period during the pandemic of COVID-19: a systematic review and meta-analysis. Syst Rev. 2021;10(1):101.CrossRef Dhouib W, Maatoug J, Ayouni I, Zammit N, Ghammem R, Fredj SB, et al. The incubation period during the pandemic of COVID-19: a systematic review and meta-analysis. Syst Rev. 2021;10(1):101.CrossRef
11.
go back to reference Qiu C, Deng Z, Xiao Q, Shu Y, Deng Y, Wang H, et al. Transmission and clinical characteristics of coronavirus disease 2019 in 104 outside-Wuhan patients, China. J Med Virol. 2020;92(10):2027–35.CrossRef Qiu C, Deng Z, Xiao Q, Shu Y, Deng Y, Wang H, et al. Transmission and clinical characteristics of coronavirus disease 2019 in 104 outside-Wuhan patients, China. J Med Virol. 2020;92(10):2027–35.CrossRef
12.
go back to reference Bai Y, Yao L, Wei T, Tian F, Jin DY, Chen L, et al. Presumed asymptomatic carrier transmission of COVID-19. JAMA. 2020;323(14):1406–7.CrossRef Bai Y, Yao L, Wei T, Tian F, Jin DY, Chen L, et al. Presumed asymptomatic carrier transmission of COVID-19. JAMA. 2020;323(14):1406–7.CrossRef
13.
go back to reference Wang Y, Wang Q, Wang K, Song C, Guo Z, Hu W. A case of COVID-19 with an ultralong incubation period. Infect Control Hosp Epidemiol. 2021;42(2):242–3.CrossRef Wang Y, Wang Q, Wang K, Song C, Guo Z, Hu W. A case of COVID-19 with an ultralong incubation period. Infect Control Hosp Epidemiol. 2021;42(2):242–3.CrossRef
14.
go back to reference Zhang J, Litvinova M, Wang W, Wang Y, Deng X, Chen X, et al. Evolving epidemiology and transmission dynamics of coronavirus disease 2019 outside Hubei province, China: a descriptive and modelling study. Lancet Infect Dis. 2020;20(7):793–802.CrossRef Zhang J, Litvinova M, Wang W, Wang Y, Deng X, Chen X, et al. Evolving epidemiology and transmission dynamics of coronavirus disease 2019 outside Hubei province, China: a descriptive and modelling study. Lancet Infect Dis. 2020;20(7):793–802.CrossRef
15.
go back to reference Qi H, Xiao S, Shi R, Ward MP, Chen Y, Tu W, et al. COVID-19 transmission in mainland China is associated with temperature and humidity: a time-series analysis. Sci Total Environ. 2020;728:138778.CrossRef Qi H, Xiao S, Shi R, Ward MP, Chen Y, Tu W, et al. COVID-19 transmission in mainland China is associated with temperature and humidity: a time-series analysis. Sci Total Environ. 2020;728:138778.CrossRef
17.
go back to reference Koufakou A, Ortiz EG, Georgiopoulos M, Anagnostopoulos GC, Reynolds KM. A scalable and efficient outlier detection strategy for categorical data. In: 19th IEEE International Conference on Tools with Artificial Intelligence (ICTAI 2007); 2007. p. 210–7. Koufakou A, Ortiz EG, Georgiopoulos M, Anagnostopoulos GC, Reynolds KM. A scalable and efficient outlier detection strategy for categorical data. In: 19th IEEE International Conference on Tools with Artificial Intelligence (ICTAI 2007); 2007. p. 210–7.
18.
go back to reference Tabachnick BG, Fidell LS, Ullman JB. Using multivariate statistics. 7th ed. Boston: Pearson; 2007. Tabachnick BG, Fidell LS, Ullman JB. Using multivariate statistics. 7th ed. Boston: Pearson; 2007.
19.
go back to reference Stoltzfus JC. Logistic regression: a brief primer. Acad Emerg Med. 2011;18(10):1099–104.CrossRef Stoltzfus JC. Logistic regression: a brief primer. Acad Emerg Med. 2011;18(10):1099–104.CrossRef
21.
go back to reference Virlogeux V, Fang VJ, Wu JT, Ho LM, Peiris JS, Leung GM, et al. Brief report: incubation period duration and severity of clinical disease following severe acute respiratory syndrome coronavirus infection. Epidemiology. 2015;26(5):666–9.CrossRef Virlogeux V, Fang VJ, Wu JT, Ho LM, Peiris JS, Leung GM, et al. Brief report: incubation period duration and severity of clinical disease following severe acute respiratory syndrome coronavirus infection. Epidemiology. 2015;26(5):666–9.CrossRef
22.
go back to reference Virlogeux V, Park M, Wu JT, Cowling BJ. Association between severity of MERS-CoV infection and incubation period. Emerg Infect Dis. 2016;22(3):526–8.CrossRef Virlogeux V, Park M, Wu JT, Cowling BJ. Association between severity of MERS-CoV infection and incubation period. Emerg Infect Dis. 2016;22(3):526–8.CrossRef
23.
go back to reference Petrosillo N, Viceconte G, Ergonul O, Ippolito G, Petersen E. COVID-19, SARS and MERS: are they closely related? Clin Microbiol Infect. 2020;26(6):729–34.CrossRef Petrosillo N, Viceconte G, Ergonul O, Ippolito G, Petersen E. COVID-19, SARS and MERS: are they closely related? Clin Microbiol Infect. 2020;26(6):729–34.CrossRef
24.
go back to reference Ho MS, Chen WJ, Chen HY, Lin SF, Wang MC, Di J, et al. Neutralizing antibody response and SARS severity. Emerg Infect Dis. 2005;11(11):1730–7.CrossRef Ho MS, Chen WJ, Chen HY, Lin SF, Wang MC, Di J, et al. Neutralizing antibody response and SARS severity. Emerg Infect Dis. 2005;11(11):1730–7.CrossRef
25.
go back to reference Lee H, Kim K, Choi K, Hong S, Son H, Ryu S. Incubation period of the coronavirus disease 2019 (COVID-19) in Busan, South Korea. J Infect Chemother. 2020;26(9):1011–3.CrossRef Lee H, Kim K, Choi K, Hong S, Son H, Ryu S. Incubation period of the coronavirus disease 2019 (COVID-19) in Busan, South Korea. J Infect Chemother. 2020;26(9):1011–3.CrossRef
26.
go back to reference Nie X, Fan L, Mu G, Tan Q, Wang M, Xie Y, et al. Epidemiological characteristics and incubation period of 7015 confirmed cases with coronavirus disease 2019 outside Hubei province in China. J Infect Dis. 2020;222(1):26–33.CrossRef Nie X, Fan L, Mu G, Tan Q, Wang M, Xie Y, et al. Epidemiological characteristics and incubation period of 7015 confirmed cases with coronavirus disease 2019 outside Hubei province in China. J Infect Dis. 2020;222(1):26–33.CrossRef
27.
go back to reference Hermesh T, Moltedo B, López CB, Moran TM. Buying time-the immune system determinants of the incubation period to respiratory viruses. Viruses. 2010;2(11):2541–58.CrossRef Hermesh T, Moltedo B, López CB, Moran TM. Buying time-the immune system determinants of the incubation period to respiratory viruses. Viruses. 2010;2(11):2541–58.CrossRef
28.
go back to reference Tan WYT, Wong LY, Leo YS, Toh MPHS. Does incubation period of COVID-19 vary with age? A study of epidemiologically linked cases in Singapore. Epidemiol Infect. 2020;148:e197.CrossRef Tan WYT, Wong LY, Leo YS, Toh MPHS. Does incubation period of COVID-19 vary with age? A study of epidemiologically linked cases in Singapore. Epidemiol Infect. 2020;148:e197.CrossRef
29.
go back to reference Cowling BJ, Muller MP, Wong IO, Ho LM, Louie M, McGeer A, et al. Alternative methods of estimating an incubation distribution: examples from severe acute respiratory syndrome. Epidemiology. 2007;18(2):253–9.CrossRef Cowling BJ, Muller MP, Wong IO, Ho LM, Louie M, McGeer A, et al. Alternative methods of estimating an incubation distribution: examples from severe acute respiratory syndrome. Epidemiology. 2007;18(2):253–9.CrossRef
30.
go back to reference Chan KH, Peiris JS, Lam SY, Poon LL, Yuen KY, Seto WH. The effects of temperature and relative humidity on the viability of the SARS coronavirus. Adv Virol. 2011;2011:734690.CrossRef Chan KH, Peiris JS, Lam SY, Poon LL, Yuen KY, Seto WH. The effects of temperature and relative humidity on the viability of the SARS coronavirus. Adv Virol. 2011;2011:734690.CrossRef
31.
go back to reference Shephard RJ, Shek PN. Cold exposure and immune function. Can J Physiol Pharmacol. 1998;76(9):828–36.CrossRef Shephard RJ, Shek PN. Cold exposure and immune function. Can J Physiol Pharmacol. 1998;76(9):828–36.CrossRef
32.
go back to reference Chin AWH, Chu JTS, Perera MRA, Hui KPY, Yen HL, Chan MCW, et al. Stability of SARS-CoV-2 in different environmental conditions. Lancet Microbe. 2020;1(1):e10.CrossRef Chin AWH, Chu JTS, Perera MRA, Hui KPY, Yen HL, Chan MCW, et al. Stability of SARS-CoV-2 in different environmental conditions. Lancet Microbe. 2020;1(1):e10.CrossRef
Metadata
Title
Epidemiological features of COVID-19 patients with prolonged incubation period and its implications for controlling the epidemics in China
Authors
Zhi-Jie Zhang
Tian-Le Che
Tao Wang
Han Zhao
Jie Hong
Qing Su
Hai-Yang Zhang
Shi-Xia Zhou
Ai-Ying Teng
Yuan-Yuan Zhang
Yang Yang
Li-Qun Fang
Wei Liu
Publication date
01-12-2021
Publisher
BioMed Central
Keyword
COVID-19
Published in
BMC Public Health / Issue 1/2021
Electronic ISSN: 1471-2458
DOI
https://doi.org/10.1186/s12889-021-12337-9

Other articles of this Issue 1/2021

BMC Public Health 1/2021 Go to the issue