ORIGINAL RESEARCH

published: 11 January 2021

doi: 10.3389/fphy.2020.589963

Characterizing COVID-19
Transmission: Incubation Period,
Reproduction Rate, and
Multiple-Generation Spreading
Lin Zhang 1, Jiahua Zhu 2, Xuyuan Wang 1, Juan Yang 1, Xiao Fan Liu 3* and Xiao-Ke Xu 4*
1
School of Science, Beijing University of Posts and Telecommunications, Beijing, China, 2The First Hospital of Putian City, Putian,
China, 3Web Mining Laboratory, Department of Media and Communication, City University of Hong Kong, Hong Kong, China,
4
College of Information and Communication Engineering, Dalian Minzu University, Dalian, China

Understanding the transmission process is crucial for the prevention and mitigation of
COVID-19 spread. This paper contributes to the COVID-19 knowledge by analyzing the
incubation period, the transmission rate from close contact to infection, and the properties
Edited by:
Aristides (Aris) Moustakas, of multiple-generation transmission. The data regarding these parameters are extracted
Natural History Museum of Crete; from a detailed line-list database of 9,120 cases reported in mainland China from January
University of Crete, Greece
15 to February 29, 2020. The incubation period of COVID-19 has a mean, median, and
Reviewed by:
Gui-Quan Sun, North University of
mode of 7.83, 7, and 5 days, and, in 12.5% of cases, more than 14 days. The number of
China, China close contacts for these cases during the incubation period and a few days before
Chen Chu, hospitalization follows a log-normal distribution, which may lead to super-spreading
Yunnan University of Finance and
Economics, China events. The disease transmission rate from close contact roughly decreases in line
Wen-Xuan Wang, Beijing University of with the number of close contacts with median 0.13. The average secondary cases
Posts and Telecommunications
(BUPT), China
are 2.10, 1.35, and 2.2 for the first, second, and third generations conditioned on at least
*Correspondence:
one offspring. However, the ratio of no further spread in the 2nd, 3rd, and 4th generations
Xiao Fan Liu are 26.2, 93.9, and 90.7%, respectively. Moreover, the conditioned reproduction number
[email protected] in the second generation is geometrically distributed. Our findings suggest that, in order to
Xiao-Ke Xu
[email protected] effectively control the pandemic, prevention measures, such as social distancing, wearing
masks, and isolating from close contacts, would be the most important and least costly
Specialty section: measures.
This article was submitted to
Social Physics, Keywords: COVID-19, incubation period, close contacts, superspreading, effective reproduction number, spreading
a section of the journal tree
Frontiers in Physics
Received: 31 July 2020
Accepted: 16 November 2020 1 INTRODUCTION
Published: 11 January 2021

Citation: As of July 2020, the cumulative confirmed cases of COVID-19 worldwide have exceeded 17.4 million
Zhang L, Zhu J, Wang X, Yang J, with over 572 thousand dead. There are 22 countries with more than 100,000 confirmed cases of as of
Liu XF and Xu X-K (2021) July 14, 2020. The high transmissibility of the SARS-CoV-2 virus has substantially changed people’s
Characterizing COVID-19
hygiene habits, social relations, and forms of work and schooling during and after the pandemic [1].
Transmission: Incubation Period,
Reproduction Rate, and Multiple-
In the absence of pharmaceutical intervention measures, public policies such as city lockdowns and
Generation Spreading. workplace and school closures can mitigate the spread of disease, though with substantial economic
Front. Phys. 8:589963. and societal costs. The indecision regarding restarting the economy and stopping the pandemic has
doi: 10.3389/fphy.2020.589963 resulted in a wave of outbreaks in many countries [2].

Frontiers in Physics | www.frontiersin.org 1 January 2021 | Volume 8 | Article 589963

Zhang et al. Characterizing COVID-19 Transmission

Understanding the characteristics of the COVID-19 require a prerequisite setting of the transmission rate during
transmission process is crucial in finding a middle ground social gathering events to predict disease spreading range [18, 29,
between restoring economic and societal order and controlling 30]. For a better estimate of the reproduction number, a real data
the pandemic. Previous research has shown that COVID-19 can sample is a crucial ingredient. However, it is difficult to collect.
be infectious pre-symptomatically [3], i.e., the virus is Considering the demand of investigating the properties and
transmissive even without symptom onset. Finding out the modeling of COVID-19, fine data extracted from informative
incubation period’s duration and the virus reproducibility line-list records can provide supporting evidence for the existing
during the incubation period and shortly after symptom onset results and solid foundation for further study.
but before hospitalization is thus an urgent necessity [4]. In this work, we estimate the parameters of concern from a
Considering the incubation period, as of Jan. 26, the mean and large scale epidemiological line-list database, which contains the
median were 5 and 4.75 days (obtained by 125 patients) [5]. contact history and epidemiological timelines of 9,120 confirmed
Confirmed cases reported from Jan. 4 to Feb. 24 showed a COVID-19 cases in China [31]. The duration of the incubation
median incubation period of 5.1 days (obtained from 181 period and the details of close contacts and contact scenarios are
patients) [6]. By Jan. 22, using 425 patients, the mean extracted from the line-list. Spreading trees are reconstructed
incubation period was 5.2 days, and [7]. Reference [8] gave a from the potential transmission pairs in the line-list data set.
shorter incubation period of 4.2 days, inferring that COVID-19 Hidden in the line-list records of confirmed cases, we have
is more infectious than initially estimated. As of Mar. 31, the collected 421 chains of spreading with a total confirmed cases
mean incubation time is estimated as 8.0 with a standard number of 1,140. We fit proper distributions to the incubation
deviation of 4.75 [9]. Through a renewal process, the period as well as scale of close contact. The reproducibility is
estimated median of the incubation period is 8.1 days, which presented by the spreading tree, which can be referred to as the
is longer than other studies [10]. The mean and median of the effective reproduction number under strict containment
incubation periods were 5.84 and 5.0 days via bootstrap for measures in China.
groups with an age of ≥ 40, and they otherwise demonstrated a The incubation distribution is fitted by Weibull
significant difference [11]. By meta-analysis, the incubation distribution with a mean and median of 7.83 and 7 days,
period was modeled with a lognormal distribution, and the respectively; this is in agreement with [9]. Larger data size and
mean and median were 5.8 and 5.1 days [12]. longer observation period tend to result in larger incubation
The transmission rate is defined as the probability that an period, which is coincidence with the long tailed nature of
infection occurs among susceptible people within a specific Weibull distribution. For the secondary attack rate, there are
group. It is an important index for providing an indication of much fewer results due to the lack of data. We have obtained
how social interactions are related to transmission risk. Nine 412 close contact events to investigate the transmission rate. It
reports were listed in [13], showing a rate of 35% (95% CI 27–44), is revealed that the relationship between the contact scale and
depending on infection caused by different contact methods. transmission rate is not strongly related no matter if it is a
One of the most important indices for infectious disease is the linear or nonlinear relation. Moreover, the contact scale is
basic reproductive number. Numerous studies are devoted to its fitted by Lognormal distribution, and the empirical
estimate. It is estimated to be 2.2 [14], which is higher than SARS- distribution of transmission rate is also given. Finally, the
COV and MERS-CoV [15]. More estimates for the basic reproducibility of COVID-19 under strict containment
reproduction number are 4.7–6.6 [8], 2.24–3.58 [16], 3.77 measures is investigated by the multiple-generation
(95% CI 3.51–4.05) [5], and 3.60 (3.49–3.84) [17]. The spreading structure, revealing the effectiveness of the
effective reproduction number is changing with time; it containment measures in China. The key contributions of
changed from 2.35 (1.15–4.77) to 1.05 (0.41–2.39) due to our work are those that aim for a better understanding of the
lockdown in Wuhan within 1 week [18]. properties of COVID-19 spread.
The best-known model within infectious disease epidemiology The rest of the paper is organized as follows. Section 2
is the SEIR (susceptible-exposed-infectious-recovered) model describes the data and methods. Section 3 reports the
with different generalization. These models are utilized at the empirical analysis and models fitted. Section 4 discusses the
population level for the proportion of each state at given time, implications of results and provides an explanation based on
aiming to investigating the strategic decisions or effectiveness of branching process and the necessity of ultra-strict prevention
the mitigation measures. For illustration, effective containment measures.
can explains the subexponential growth in China [19], and effects
of containment measures in Italy are also analyzed by an SEIR-
like model [17]. More results can be found [20–27]. 2 DATA AND METHODS
Clinical investigations may suffer from a limited sample size
and biased sampling from the population, leading to geometrical The line-list database used in this paper contains hand-coded
or demographic-dependent results. Different samples and information extracted from 9,120 public reported cases by
different methods also lead to different results for data mainland China health commissions from January 15 to
analysis and estimates. Simulation of disease spread and February 29, 2020. A typically reported item is as follows:
mitigation policies require a precise setting of incubation
period [19, 28]. Metapopulation disease transmission models “Patient ID: Huainan-25.

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Zhang et al. Characterizing COVID-19 Transmission

TABLE 1 | Numbers of different types of close contact events.

Type Number of cases Proportion (%)

Living 386 93.69

Dining 7 1.70
Working 3 0.73
Traveling 1 0.24
Others 15 3.64

FIGURE 1 | The empirical distribution and Weibull distribution fitting of

incubation time. The Weibull distribution has density function fW (x; A, B)

k−1
e−(x/λ) , x ≥ 0 with λ
9.93, and k
1.79. The K–S test is 0.17, which
k

λ λ
k x

means that Weibull distribution is proper for the data.

The patient Huainan-25 is a 59-year-old woman who is the

wife of the Huainan-26 patient. On February 12, she developed
fever, muscle soreness, and other symptoms. On February 14, she
went to the hospital for treatment and stayed at the hospital for
observation. On February 15, her nucleic acid test was tested FIGURE 2 | The empirical distribution of scale of close contact events
positive, and doctors diagnosed her as a suspected patient. Two with log-normal density fitting. The density function of this log-normal
(lnx−μ)2
days later, she was confirmed. Doctors have traced back 3 close distribution is fLN (x)
σx√1 2πe− 2σ 2 , where the fitting parameters are
contacts, all of whom have been quarantined for medical μ
2.495, σ
0.745. The p-value of the K–S test for log-normal
observation. During the New Year’s holiday, she had close distribution is 0.18. The notion that the scale is log-normal distributed is not
contact with her daughter, son-in-law, and granddaughter. Her rejected.
son-in-law, an asymptomatic patient with a history of suspicious
exposure in Hefei, stayed at a designated hospital for observation.
Doctors have traced back his 46 close contacts, all of whom have an infected individual depends on this variable. The quarantine
been quarantined for medical observation.” was usually 14 days for COVID-19. However, for strict
The original extracted line-list database contains the prevention, it was suggested at the Information Office of
epidemiology timelines, e.g., the possible date of virus Beijing Municipality press conference on June 28 that after the
exposure and date of symptom onset, for each case. We define first 14 days, another 14-day quarantine is necessary in some
the incubation period as the time between virus exposure and high-risk areas.
symptom onset. There are 457 cases with both dates of exposure The reason why another 14 days quarantine is necessary can
and date of symptoms reported in the line-list database. be found from the distribution of incubation time. The sample
Close contact events are social events and scenarios such as with 457 incubation time reveals that it is a skewed
living together, dining together, traveling together, and working distribution, see Figure 1. The mean, median, and mode
together. There were 412 close contact events with the numbers of calculated from the sample data are 7.83, 7, and 5 days,
close contacts and secondary infections reported. Multiple- respectively. Moreover, the empirical probability of
generation transmissions can form tree structures that incubation period exceeds 14 is
originated from an initial infection. There are 421
transmission chains identified from the line-list. P
Incubation period ≥ 14 days
0.125.

That is to say, the chance of an asymptomatic infected

3 RESULTS individual turning into symptomatic after 14 days is about
12.5%. For strict control of COVID-19, longer quarantine is
3.1 Duration of the Incubation Period necessary. A Weibull distribution is fitted to the empirical
The incubation period is a vital variable considering the control of data, with shift 1 to the right for avoiding zero. The density
the pandemic. The quarantine period of close contact people with function is

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Zhang et al. Characterizing COVID-19 Transmission

tailed nature of the close contact scale reveals a non-neglectable

possibility of super-spreading events. Therefore, in order to
effectively control the pandemic, maintaining social distance
and wearing masks should be effective measures.

3.3 Transmission Rate and the Scale of

Close Contact Events
We define the transmission rate as the number of people infected
in one close contact event over the number of people in that event.
Figure 3 shows the scatter plot between the transmission rate and
the scale of close contact events. It can be seen that the rate drops
as the scale of events increases in a non-linear fashion.
Let p be the transmission rate and N the total number of people
in the close contact events. Based on our sample, given the value
FIGURE 3 | The scatter plot of N vs. the mean of p, together with of N, the mean p is calculated. The relationship between N and p
exponential function fitting. The relationship between N and p can be fitted can be fitted with the following exponential function:
with function p
a p exp(−b p N) + c, where the fitting parameters are
a
0.453, b
0.121, and c
0.092, and the goodness of fit index is p
a p exp(−b p N) + c,
R2
0.706.
where the fitting parameters are a
0.453, b
0.121, and
c
0.092, and the goodness of fit index is R2
0.706. The
k x k−1 k exponential relation reveals that a larger scale of close contact
fW (x; A, B)
  e−(x/λ) , x ≥ 0, tends to smaller secondary incidence p. However, the fitting is not
λ λ
convinced enough. The correlation coefficient between N and p is
with λ
9.93, and k
1.79. The K–S test is 0.17, which means −0.29, implying that neither a linear nor a nonlinear relation
that Weibull distribution is proper for the data. between N and p is significant. In other words, p can be treated as
a natural feature of COVID-19, with weak monotonic decrease of
3.2 Scale of Close Contact Events N. The mean and median of the transmission rate is 0.20 and 0.13
The scale of close contact events is the number of people involved in with an interquartile range 0–0.3. The empirical distribution of
one event of where people have gathered together in a specific way. transmission rate is also given in Figure 4. Protective measures to
Table 1 shows the number of different types of social events and decrease the transmission rate would be the least cost ways to
scenarios that can potentially facilitate disease spreading. Among the prevent the pandemic, such as maintaining social distance,
412 close contact events, more than 93.7% happened by way of living wearing masks, and washing hands.
together.
The period of our dataset is the early stage of COVID-19
3.4 Spreading Tree Structures
Transmission events can create tree structures to map disease
spread in China. The distribution of the scale in close contact
spread. There are in total 421 chains verified from the record data.
events is a natural feature seen when people are free from
Among the chains, there are 311 chains with secondary cases, out
movement regardless of the COVID-19 pandemic. The contact
scale is intrinsically positive, with a few enormously high data
points typically arising. The lognormal distribution is an ideal
descriptor of such data, with a positive range, right skewness,
heavy right tail, and easily computed parameter estimates.
Supported by the K-S test with a value of 0.18, the log-normal
distribution shows the proper fitting among the positive, skewed,
heavy-tailed distribution candidate. The mechanism of
lognormal distributed data in ecology can be obtained by
stochastic differential equation [32], which would be another
topic for further investigation. The result is shown in Figure 2,
The density function of this log-normal distribution is
1 (lnx−μ)2
fLN (x)
√ e− 2σ2 ,
σx 2π
where the fitting parameters are μ
2.495, σ
0.745. The p-value
of the K-S test for log-normal distribution is 0.18. It is not a
rejected notion that the scale is log-normal distributed. Though FIGURE 4 | The empirical distribution of the transmission rate. The mean
and median of the transmission rate is 0.20 and 0.13 with an interquantile
there are various prevention measures worldwide, various contact
range 0–0.3. No proper common distribution fits the empirical distribution.
events result in a heterogeneous scale of close contact. The heavy-

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Zhang et al. Characterizing COVID-19 Transmission

TABLE 2 | The reproduction number in each generation of transmission in the

spreading tree.

Tree depth (Size) Ratio of no child (Size) Conditioned mean Mean

1(421) 26.2% (110) 2.10 1.55

2(654) 93.9% (614) 1.35 0.08
3(54) 90.7% (49) 2.2 0.20
4(11) 100.0% (11) 0 0

of which there are 654 children in the second generation.

However, due to effective prevention, there are only 54 and 11
children in the third and fourth generations, respectively. No fifth
generation is observed in our dataset.
The reproduction number of an infection is the number of
secondary infectees infected by the same confirmed individual.
We define the reproduction number in each generation by
dividing the number of infected people in the next generation FIGURE 5 | The empirical distribution of infection numbers in the second
by the present one. Based on the existence of at least one child in generation with geometric fitting. The geometric distribution law is
the next generation, the mean reproduction number in the first, P(ksecondary cases)
p(1 − p)k−1 for k ≥ 1. The parameter is p
0.50, and
second, and third generations are 2.10, 1.35, and 2.2. However, the K–S test value is 0.73.

without the conditional restriction, the mean are 1.55, 0.08, and
0.2, respectively, see Table 2.
Using the sample of number of secondary cases caused by the 311
Theoretically, the reproduction number, say R, is a
infectors in the first generation, empirical distribution, together with
determining index quantifying the transmissibility. To control
geometric fitting is shown in Figure 5. The geometric distribution
the pandemic, R should be less than one. Borrowed from the
law is P(k secondary cases)
p(1 − p)k−1 for k ≥ 1. The parameter
theory of branching processes, there is a phase transition with a
is p
0.50, and the K–S test value is 0.73.
critical value R
1. If R < 1, then, with a probability of one, the
spread of a certain disease will die out with exponential speed.
4 DISCUSSION However, when R > 1, the rate of spread will exponentially
increase. The probability of exponential increas can be
In this study, based on the details of confirmed cases reported by the obtained as the minimum nonnegative solution to the
mass media, the following features are explored: the Weibull equation f (s)
s for s ∈ (0, 1), where f (s) is the generating
distribution of the incubation period, the Log-normal distribution function of the reproduction number. From this point of view,
of the scale of close contact events, the geometric distribution of the the propagation of COVID-19 is an issue of “all or nothing.”
reproduction number in different generations of virus transmissions, From this point of view, the control measures would be as strict as
and the statistical feature of secondary attack rate. possible to avoid the possibility of exponential increase.
As far as we know, the distribution of the close contacts’ scale is
released for the first time that it is log-normal distributed due to lack
of data. This heavy-tailed distribution reveals a relatively larger DATA AVAILABILITY STATEMENT
possibility of super spreading events comparing to light-tailed
The datasets presented in this study can be found in online
distributions. To reduce the secondary infection, it is important
repositories. The names of the repository/repositories and
to take adequate measures to reduce the scale of close contact and
accession number(s) can be found below: https://github.com/
reduce the secondary infections. Moreover, efforts should be made to
PDGLin/COVID19_EffSerialInterval_NPI
trace back the close contacts to cut off the possible spreading chain in
advance.
It is notable that the method here is universal to all infectious AUTHOR CONTRIBUTIONS
diseases. The crucial step is the line-list record of each confirmed case
and the detailed transmission relationship in the spreading tree LZ and JZ contributed equally as first authors. JZ, X-FL, and
structure. For infectious diseases where only non-pharmaceutical X-KX designed the analysis, LZ, XW, JY, and X-KX analyzed the
measurement can be applied to prevent its spreading, detailed data. LZ and X-FL wrote the paper.
record keeping of each confirmed case and the contact history is
crucial. The tree structure is good evidence for the spreading trend and FUNDING
helpful for the precise estimation of the effective reproductive number.
Moreover, contact history is useful to nip severe infectious diseases in This work was jointly supported by the Fundamental
the bud. Research Funds for the Central Universities (No. 2019XD-

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Zhang et al. Characterizing COVID-19 Transmission

A11), the National Natural Science Foundation of China 61773091), the LiaoNing Revitalization Talents Program
(Grant Nos. 11971074, 61671005, 61672108, 61976025, (XLYC1807106).

18. Kucharski AJ, Russell TW, Diamond C. Early dynamics of transmission and
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Frontiers in Physics | www.frontiersin.org 6 January 2021 | Volume 8 | Article 589963