Content uploaded by Changwei Li
Author content
All content in this area was uploaded by Changwei Li on Sep 03, 2020
Content may be subject to copyright.
Community Outbreak Investigation of SARS-CoV-2 Transmission
Among Bus Riders in Eastern China
Ye Shen, PhD; Changwei Li, PhD; Hongjun Dong, MD; Zhen Wang, MD; Leonardo Martinez, PhD; Zhou Sun, MD;
Andreas Handel, PhD; Zhiping Chen, MD; Enfu Chen, MD; Mark H. Ebell, MD, MS; Fan Wang, MA; Bo Yi, MD;
Haibin Wang, MD; Xiaoxiao Wang, MD; Aihong Wang, MD; Bingbing Chen, MD; Yanling Qi, PhD;
Lirong Liang, MD, PhD; Yang Li, PhD; Feng Ling, MD; Junfang Chen, MD; Guozhang Xu, MD
IMPORTANCE Evidence of whether severe acute respiratory syndrome coronavirus 2
(SARS-CoV-2), the virus that causes coronavirus disease 2019 (COVID-19), can be transmitted
as an aerosol (ie, airborne) has substantial public health implications.
OBJECTIVE To investigate potential transmission routes of SARS-CoV-2 infection with
epidemiologic evidence from a COVID-19 outbreak.
DESIGN, SETTING, AND PARTICIPANTS This cohort study examined a community COVID-19
outbreak in Zhejiang province. On January 19, 2020, 128 individuals took 2 buses (60
[46.9%] from bus 1 and 68 [53.1%] from bus 2) on a 100-minute round trip to attend a
150-minute worship event. The source patient was a passenger on bus 2. We compared risks
of SARS-CoV-2 infection among at-risk individuals taking bus 1 (n = 60) and bus 2 (n = 67
[source patient excluded]) and among all other individuals (n = 172) attending the worship
event. We also divided seats on the exposed bus into high-risk and low-risk zones according
to the distance from the source patient and compared COVID-19 risks in each zone. In both
buses, central air conditioners were in indoor recirculation mode.
MAIN OUTCOMES AND MEASURES SARS-CoV-2 infection was confirmed by reverse
transcription polymerase chain reaction or by viral genome sequencing results. Attack rates
for SARS-CoV-2 infection were calculated for different groups, and the spatial distribution of
individuals who developed infection on bus 2 was obtained.
RESULTS Of the 128 participants, 15 (11.7%) were men, 113 (88.3%) were women, and the
mean age was 58.6 years. On bus 2, 24 of the 68 individuals (35.3% [including the index
patient]) received a diagnosis of COVID-19 after the event. Meanwhile, none of the 60
individuals in bus 1 were infected. Among the other 172 individuals at the worship event, 7
(4.1%) subsequently received a COVID-19 diagnosis. Individuals in bus 2 had a 34.3% (95% CI,
24.1%-46.3%) higher risk of getting COVID-19 compared with those in bus 1 and were 11.4
(95% CI, 5.1-25.4) times more likely to have COVID-19 compared with all other individuals
attending the worship event. Within bus 2, individuals in high-risk zones had moderately, but
nonsignificantly, higher risk for COVID-19 compared with those in the low-risk zones. The
absence of a significantly increased risk in the part of the bus closer to the index case
suggested that airborne spread of the virus may at least partially explain the markedly high
attack rate observed.
CONCLUSIONS AND RELEVANCE In this cohort study and case investigation of a community
outbreak of COVID-19 in Zhejiang province, individuals who rode a bus to a worship event
with a patient with COVID-19 had a higher risk of SARS-CoV-2 infection than individuals who
rode another bus to the same event. Airborne spread of SARS-CoV-2 seems likely to have
contributed to the high attack rate in the exposed bus. Future efforts at prevention and
control must consider the potential for airborne spread of the virus.
JAMA Intern Med. doi:10.1001/jamainternmed.2020.5225
Published online September 1, 2020.
Supplemental content
Author Affiliations: Author
affiliations are listed at the end of this
article.
Corresponding Authors: Feng Ling,
MD, Zhejiang Provincial Center for
Disease Control and Prevention,
3399 Binsheng Rd, Hangzhou, China
(fengl@cdc.zj.cn); Guozhang Xu, MD,
Ningbo Municipal Center for Disease
Control and Prevention,
237 YongfengRd, Ningbo, China
(xugz@nbcdc.org.cn).
Research
JAMA Internal Medicine | Original Investigation
(Reprinted) E1
© 2020 American Medical Association. All rights reserved.
Downloaded From: https://jamanetwork.com/ on 09/03/2020
Human infection by the severe acute respiratory syn-
drome coronavirus 2 (SARS-CoV-2) was first reported
in late 2019 in Wuhan city of Hubei province in
China.
1,2
The World HealthOrganization declared the corona-
virus disease 2019 (COVID-19) outbreak a public health emer-
gency of international concern on January 30, 2020. The on-
going epidemic has since affected more than 150 countries and
territories. As of August 5, 2020, more than 18 million cases
have been confirmed and more than 650 000 people have
died.
3
Greater efforts are needed to contain and combat the vi-
rus; however, much remains unknown about SARS-CoV-2
transmission, limiting our ability to implement effective in-
terventions. Several studies have demonstrated transmis-
sion through close contact and respiratory droplets produced
when an infected person coughs or sneezes.
4-6
Whether
SARS-CoV-2 can be transmitted as an aerosol (ie, airborne)
through inhalation of virus suspended in the air is unknown.
Previous studies have suggested possible airborne transmis-
sion of other virulent coronaviruses, such as the severe acute
respiratory syndrome coronavirus and the Middle East respi-
ratory syndrome coronavirus.
7-11
Recent reports suggest that
closed environments may facilitate secondary transmission of
SARS-CoV-2.
12,13
An experimental study demonstrated that
SARS-CoV-2 can remain viable in aerosols for 3 hours or
longer,
14
and experimental evidence of transmission of
SARS-CoV-2 between ferrets via the air was also established.
15,16
Therefore, evidence supporting the potential for an airborne
transmission route of SARS-CoV-2 is emerging. However, epi-
demiologic evidence from actual community transmission in
human cohorts is lacking. To investigate the potential air-
borne transmission route, we present the investigation of an
outbreak of COVID-19 among lay Buddhists worshiping in a
temple in Zhejiang province.
Methods
Data Collection
Data on demographics, travel history, and soc ial and family ac-
tivities were collected by a standard questionnaire and addi-
tional phone or in-person interviews through epidemiologic
investigation carried out by local Centers for Disease Control
and Prevention staff between January 27 and February 23,
2020. The standard case report form and details regarding the
initiation of the outbreak investigation areprovided in the eAp-
pendix in the Supplement. The research protocol was ap-
proved by the institutional review board at the Zhejiang Pro-
vincial Centers for Disease Control and Prevention and all
human participants gave written informed consent.
Sample Collection and Diagnosis of COVID-19
Throat swabs (oropharynx and nasopharynx) were collected
for all individuals involved in the outbreak and their close con-
tacts identified through follow-up contact tracing. All samples
were tested by reverse transcription polymerase chain reac-
tion or by viral genome sequencing. Screened individuals were
categorized into noncases, suspected cases, and confirmed
cases of COVID-19. Criteria for COVID-19 case definitions and
disease severity are provided in the eAppendix in the
Supplement.
Statistical Analyses
Attack rates were estimated as the number of diagnosed
COVID-19 cases divided by the total number of people at risk,
excluding the source patientof the outbreak. We compared the
risk of COVID-19 between individuals taking the exposed bus
(bus 2) and individuals taking the unexposed bus (bus 1) as well
as the COVID-19 risk between individuals in bus 2 and all other
individuals attending the worship event, excluding bus 2. In
addition, we divided seats in bus 2 into high-risk and low-risk
zones according to the definition of close contact with
COVID-19 in travel-associated settings, an area within
2 meters
17
(classification 1) or 2 rows
18
(classification 2) of the
source patient. On bus 2, the distance between 2 rows was mea-
sured at 0.75 m, which converts 2 meters to 3 rows. There-
fore, the high-risk zone includes seats in the same row and
within 2 or 3 rows (rows 6-10 or rows 5-11)of the index patient
(seated in row 8); low-risk zones include seats in other rows
(Figure
17,18
). The COVID-19 risks in the 2 types of zones were
compared. All comparisons used χ
2
or Fisher exact tests. Both
risk ratios (RRs) and risk differences and corresponding 95%
confidence intervals were calculated. For an exposure-
disease category with no observations, we added a value of 0.5
to all cells.
19
A Spearman rank correlation test was performed
to test the correlation between the disease severity of those
who developed infection and the distance to the index pa-
tient on bus 2 (eAppendix in the Supplement). Analyses were
conducted using SAS, version 9.4 (SAS Institute), and statis-
tical significance was set at P< .05.
Results
Evidence from an outbreak suggesting airborne transmission
of SARS-CoV-2 is presented. Other materials associated with
the transmission dynamics of the outbreak are included in the
eAppendix in the Supplement.
Key Points
Question Is airborne transmission of severe acute respiratory
syndrome coronavirus 2 (SARS-CoV-2) a potential mean of
spreading coronavirus disease 2019 (COVID-19)?
Findings In this cohort study of 128 individuals who rode 1 of 2
buses and attended a worship event in Eastern China, those who
rode a bus with air recirculation and with a patient with COVID-19
had an increased risk of SARS-CoV-2 infection compared with
those who rode a different bus. Airborne transmission may
partially explain the increased risk of SARS-CoV-2 infection among
these bus riders.
Meaning These results suggest that future efforts at prevention
and control must consider the potential for airborne spread of
SARS-CoV-2, which is a highly transmissiblepathogen in closed
environments with air recirculation.
Research Original Investigation Community Outbreak Investigation of SARS-CoV-2 Transmission Among Bus Riders in Eastern China
E2 JAMA Internal Medicine Published online September 1, 2020 (Reprinted) jamainternalmedicine.com
© 2020 American Medical Association. All rights reserved.
Downloaded From: https://jamanetwork.com/ on 09/03/2020
Outbreak of COVID-19 Among Lay Buddhists
Worshiping in the Temple
The COVID-19 outbreak started on January 19, 2020, among
293 lay Buddhists, 2 bus drivers,and 5 monks attending an out-
door worship event held in a temple in Ningbo city of Zheji-
ang province. Ningbo city, loc atedapproximately 700 km (900
km through the highway) to the east of Wuhan city, is one of
the most populated cities in Zhejiang province, with a total
population of more than 8 million in 2010. It has an area of
9816.23 km
2
. Before January 19, 2020, no confirmed COVID-19
cases were reported in Ningbo city. Lay Buddhists live in the
broader community rather than living within a religious or-
der. Of all the lay Buddhists, 126 traveled to the temple in 2
buses, with 59 participants (46.8%) in bus 1 and the other 67
(53.2%) in bus 2. Each bus also had a driver, and all passen-
gers on the 2 buses were from the same district of the city.The
2 buses were similar in design, with an air conditioning sys-
tem on a heating and recirculating mode (ventswere below the
windows) and 4 openable windows (2 on each side); neither
had an attached toilet. All other individuals traveled to the
temple through other methods of transportation. The 2 bus-
ses came from 1 district in Ningbo city (Haishu District) to the
temple, which is located in another district of Ningbo city (Yin-
zhou District). The travel duration to and from the temple on
the bus was 50 minutes each way (100 minutes total). Passen-
gers, including the index patient, remained seatedin their own
seats during the bus rides and did not change seats on the way
back. The weather was sunny with a gentle breeze during the
day (33.8 °F-50°F). The worship event lasted 150 minutes, be-
ginning at 10:00 AM and ending at 12:30 PM. The event
Figure. Schematic Diagram of Bus 2, the Bus Carrying the Coronavirus Disease 2019 (COVID-19) Initial Patient (IP)
Classification 1 Classification 2
Front window
Door
NC
NC Row 1
NC NC Row 2
Row 2
Row 1
NC NC NCRow 3 NC NC Row 3
NC NC NCRow 6 NC C14 0Row 6
Row 4 NC C2 0Row 4NC C1C23 3 0
Row 5 NC C28 0Row 5NC NCC31 1
Row 7 NC C4 0NC C17C26 4 0 Row 7
Row 8 C15 NCIP
1NC Row 8
Row 9 NC NCC22 0C13 C20 02 Row 9
Row 10 NC C18C19 0 4 C6 NC3Row 10
NC NC NCRow 11 NC C32 0Row 11
Row 12 NC C30C16 1 0 NC NC Row 12
NC NC NCRow 13 NC NC Row 13
Row 14 NC C25NC 0C27 NC0Row 14
Row 15 NC NCC10 0C5 NC1Row 15
Zone 2Zone 2 Zone 1
Zone 2 Zone 2Zone 1
Noncase Asymptomatic case Mild case Moderate case #No. of tertiary
cases infected
Air vents (warm air)
The index patient
(a moderate case)
Classification 1
17
and 2.
18
Two different approaches to define high-risk and
low-risk COVID-19zones are indicated: zone 1 (high-risk zone) and zone 2
(low-risk zones). Severity levels of cases were indicated. Windows are indicated
with ovals, and there are 4 green side windows and that could be opened for
fresh air. C indicates case; NC, noncase.
Community Outbreak Investigation of SARS-CoV-2 Transmission Among Bus Riders in Eastern China Original Investigation Research
jamainternalmedicine.com (Reprinted) JAMA Internal Medicine Published online September 1, 2020 E3
© 2020 American Medical Association. All rights reserved.
Downloaded From: https://jamanetwork.com/ on 09/03/2020
included a luncheon, with 10 attendees sitting at each round
table in a spacious room with no recirculating central air con-
ditioning systems on. The lunch lasted 15 to 30 minutes. Pas-
sengers from bus 2 did not sit together and were randomly
mixed at lunch. All 293 layBuddhists (including those who trav-
eled on the 2 buses and the others) and the 5 monks pre-
sented at the worship place and they were mixed into large
crowds. None of the event participants wore mask or any pre-
vention during the rides and worshiping on January 19, 2020,
as there was no public awareness of COVID-19 in the city at that
time.
Among all patients who receiveda COVID-19 diagnosis dur-
ing this outbreak, the presumed index patient, a lay Buddhist
in their 60s, was the only person exposed to residents from
Wuhan. On January 17, the individual had dinner at the same
table with a group of 10 individuals, among whom 4 had travel
histories to Hubei province. The index patient was also the first
to develop clinical symptoms. As such, the index patient was
presumed to be the source of transmission in this outbreak.
The individual was initially asymptomatic during the bus trip
but started to have cough, chills, and myalgias on the eve-
ning after returning from the temple. The next day, the pa-
tient felt better after bathing in a hot tub. However, the pa-
tient’s spouse and child started to have fever and cough on
January 22, 2020, and the entire family went to a hospitalseek-
ing treatment. During the hospital visit, the index patient had
a normal body temperature. On January 25, 2020, the index
patient’schild received a diagnosis of suspected COVID-19, and
consequently the entire family was admitted to a hospital for
quarantine, where a computed tomography scan showed exu-
dative inflammation in the lungsof the index patient. All 3 fam-
ily members had confirmed COVID-19 positiveresults f romre-
verse transcription polymerase chain reaction assays on
January 28, 2020. The index patient’s spouse and child did not
participate in the worship event on January 19, 2020. Other
secondary patients also started to develop symptoms within
a relatively short period after the worship event.A detailed rec-
ord for the length of time to first symptoms for all secondary
cases and beyond (the secondary cases went on to transmit the
disease to others) is included in eFigure 1 in the Supplement,
and the corresponding transmission dynamics are presented
in eFigure 2 in the Supplement. Many of these individuals were
close contacts of the secondary cases, but they did not par-
ticipate in the worship event.
Analyses Suggesting That the Transmission
Largely Occurred on Bus 2
Bus 2 carried 68 individuals (67 lay Buddhist passengers and
a driver), of whom 24 passengers (35.3% [including the index
patient]) developed infection and received a COVID-19 diag-
nosis after the event. None of the 60 individuals (59 lay Bud-
dhist passengers and a driver) on bus 1 received a subsequent
diagnosis of COVID-19. In addition, among the other 172 indi-
viduals (167 individuals [97.1%] who traveled to the worship
event through other methods of transportation and 5 monks
[2.9%]) at the worship event, 7 (4.1%) received a subsequent
diagnosis of COVID-19, and all of them described being in close
contact with the index patient during the event. Overall, 30
of the 299 individuals (10.0%) at risk during the event devel-
oped COVID-19 (excluding the index patient). Compared with
individuals in the nonexposed bus (bus 1), those in the ex-
posed bus (bus 2) were 42.2 (95% CI, 2.6-679.3) times more
likely to develop COVID-19(Table), and the risk difference was
34.3% (95% CI, 23.0%-45.7%). Compared with all other indi-
viduals attending the worship event, passengers in bus 2 had
an 11.4 (95% CI, 5.1-25.4) times higher chance of developing
COVID-19 (Table).
Analyses Suggesting Potential
Airborne Transmission in Bus 2
We were able to identify seats for each passenger in the ex-
posed bus (Figure). The bus had 15 rows of seats. Starting from
the third row, each row had 3 seats on 1 side of the aisle and 2
seats on the other side of the aisle. The index patient sat in the
middle seat on the 3-seat side of the eighth row. Other than
the passengers sitting close to the index patient, the seats of
other cases were scattered in the bus. Passengers in the high-
risk zones had moderately but nonsignificantly higher risk of
getting COVID-19 than those in the low-risk zones using either
classification 1 (RR, 1.6; 95% CI, 0.8-3.2)or classific ation 2 (RR,
1.8; 95% CI, 0.9-3.3) (Table). On the 3-seat side of the bus, ex-
cept for the passenger sitting next to the index patient, none
of the passengers sitting in seats close to the bus window de-
veloped infection. In addition, the driver and passengers sit-
ting close to the bus door also did not develop infection, and
only 1 passenger sitting by an openable window developedin-
fection. The index patient developed moderate symptoms
(Figure). Among passengers who eventually developed
COVID-19 on bus 2, 2 were asymptomatic, 3 had mild symp-
toms, and the remaining 17 had moderate symptoms. The dis-
ease severity of the secondary patients was not associated with
their proximity to the index patienton the bus (Spearman cor-
relation coefficient, 0; P= .99). In a further contact investiga-
tion of the 23 patients with COVID-19 on bus 2, the numbers
of tertiary cases transmitted by each of them were reported
(Figure).
Discussion
Previous investigations have reported respiratory droplets,
either through close contact or the touching of inanimate ob-
jects (ie, fomites), as the major transmission route for COVID-
19. As a result, washing hands using soap under running wa-
ter for 20 seconds and masking mouths and noses when
coughing or sneezing is widely suggested for disease
prevention.
17
Through detailed epidemiologic analysis, air-
borne transmission within a bus with recycled air seems likely
to have contributed to a COVID-19 outbreak in eastern China.
A natural occurrence involved in the outbreak helped to iden-
tify where most the transmission occurred. A review study on
transmission of infectious diseases assessed the quality of evi-
dence from various sources and considered “epidemiologic evi-
dence of transmission through air over long distances” as very
strong evidence of aerosol transmission.
8
Our study provides
such evidence and adds to other sources of existing evidence
Research Original Investigation Community Outbreak Investigation of SARS-CoV-2 Transmission Among Bus Riders in Eastern China
E4 JAMAInternal Medicine Published online September 1, 2020 (Reprinted) jamainternalmedicine.com
© 2020 American Medical Association. All rights reserved.
Downloaded From: https://jamanetwork.com/ on 09/03/2020
showing experimental infection in animal models through the
aerosol route, as well as viable pathogens detected in air at am-
bient conditions for hours in laboratory media.
14-16
During the aforementioned outbreak, the index patientwas
the only person exposed to individuals from Wuhan and the
first at the event to receive a diagnosis of COVID-19, suggest-
ing a high probability that they were the source of the out-
break. The 2 buses mimicked a quasiexperiment and the sec-
ond unexposed bus, which left and arrived at the temple at
similar times with similar individuals, provided a credible con-
trol group. Both buses had an air conditioning system on a re-
circulating mode, which may have facilitated the spread of the
virus in the exposed bus. Attack rates on the exposed and un-
exposed buses were distinct (34.3% vs 0%), suggesting that the
exposure and the environment in which the exposure took
place contributed to this outbreak. Additionally, passengers sit-
ting closer to the index patient on the exposed bus did not have
statistically higher risks of COVID-19 as those sitting further
away. If COVID-19 transmission occurred solely through close
contact or respiratory droplets during this outbreak, the risk
of COVID-19 would likely be associated with distance from the
index patient, and high-risk zones on the bus would havemore
infected cases. The index patient on bus 2, likely a super
spreader of the outbreak, only developed symptoms on the eve-
ning after returning from the temple and was asymptomatic
during the bus rides, suggesting that individuals with infec-
tion may be able to shed virus by breathing and cause second-
ary cases before they become symptomatic, echoing the find-
ings from earlier presymptomatic reports.
20,21
Our findings suggesting that airborne transmission of
COVID-19 aligns with past reports of a severe acute respira-
tory syndrome outbreak on a plane and a recent COVID-19 out-
break in a restaurant.
10,22
Severe acute respiratory syndrome
and COVID-19 are caused by coronaviruses and all 3 out-
breaks occurred in relatively enclosed spaces with aircondi-
tioned systems. The high attack rate in bus 2 is also consis-
tent with an outbreak of influenza aboard a commercial airliner
in which an inoperative ventilation system resulted in a high
infection rate among passengers involved in a jet delay.
23
Mean-
while, transmission at the worship event between the bus rides
only led to few infections, and all of those reported close con-
tact with the index patient. The worship event occurred largely
outdoors. The findings echo a recent study in which aerosol-
ized traces of viral RNA were found in poorly ventilated spaces
of 2 hospitals.
24
Specifically, their study found the highest aero-
sol particles concentration in a toilet that lacked ventilation,
and we provide epidemiological evidence of a superspread-
ing event resulted from the potentialhigh aerosol particles con-
centration on a bus. These data suggest that forced, circulat-
ing air might play an important role in airborne spread of the
virus, and gatherings in enclosed settings with minimal air ven-
tilation should be limited.
Strengths and Limitations
Our study has several strengths. First, the outbreak in this re-
port had a clear index and source patient and we were able to
collect detailed information on the environment in which the
outbreak occurred and exposure opportunities. Second, the bus
outbreak mimicked a quasiexperiment in which 2 buses, 1 with
an individual with disease and 1 without, carried similar pas-
sengers at similar times, providing a credible unexposed con-
trol group. The same outbreak also included an indoor (bus
ride) and outdoor component (the worship event) of similar
lengths, allowing a comparison between those settings. All
Table. COVID-19 Risk Assessment of Different Sections of the Exposed Bus and Between the Exposed Bus and Unexposed Controls
a
Characteristic Total
No. with
COVID-19
% (95% CI) Relative risk
(95% CI) Pvalue
Relative risk
(95% CI) PvalueAttack rate Risk difference
Exposed bus and other attendees of the worship event, excluding the index patient
Bus1 60 0 0(0to
6.0)
0 [Reference] NA 1 [Reference]
NA
NA
NA
All individuals
except bus 2
232 7 3.0 (1.3 to
6.2)
NA 0 [Reference] NA 1 [Reference]
Bus 2 67 23 34.3 (24.1 to
46.3)
34.3 (23.0 to
45.7)
31.3 (19.7 to
42.9)
42.2 (2.6 to
679.3)
<.01 11.4 (5.1 to
25.4)
<.01
Overall 299 30 10.0 (7.1 to
14.0) NA
Different sections of the exposed bus, excluding the index patient
Classification 1
17
Low-risk zones
(rows 1-4,
12-15)
34 9 26.5 (14.4 to
43.3)
0 [Reference]
NA
1 [Reference] NA
NA NA
High-risk zone
(rows 5-11)
33 14 42.4 (27.2 to
59.2)
16.0 (−6.5 to
38.4)
1.6 (0.8 to
3.2)
.17
Classification 2
18
Low-risk zones
(rows 1-5,
11-15)
44 12 27.3 (16.2 to
42.0)
0 [Reference]
NA
1 [Reference] NA
NA NA
High-risk zone
(rows 6-10)
23 11 47.8 (29.2 to
67.0)
20.6 (−3.7 to
44.8)
1.8 (0.9 to
3.3)
.09
Abbreviations: COVID-19, coronavirus disease 2019; NA, not applicable.
a
For exposure-disease categories with 0 counts, we added a value of 0.5to all cells to calculate risk ratio.
Community Outbreak Investigation of SARS-CoV-2 Transmission Among Bus Riders in Eastern China Original Investigation Research
jamainternalmedicine.com (Reprinted) JAMA Internal Medicine Published online September 1, 2020 E5
© 2020 American Medical Association. All rights reserved.
Downloaded From: https://jamanetwork.com/ on 09/03/2020
participants were mixed into largec rowdsat the worship event,
but most of the infected cases were from bus 2. The result sug-
gested that the transmission largely occurred in the exposed
bus, where a much higher attack rate in a closed environment
with recirculating air was observed. The potential role of me-
chanical air circulation for COVID-19 spread is also supported
by a recent study that observed virus-contaminated air ex-
haust outlets.
25
Further, numerous nonairborne transmis-
sion options were considered through detailed epidemio-
logic investigations of the passengers in the exposed bus and
their seating information, and the overall possibility was de-
termined low. Therefore, it is hard to explain the lack of dif-
ference in the attack rate between individuals sitting close to
the index patient and those clearly separated by distance with-
out possible airborne transmission. For instance, cases C5 and
C10 seated in the last row were more than5mfromtheindex
patient on the bus and neither reported direct contact nor shar-
ing of spaces with the index patients during the event,yet they
both developed infection. Lastly, the outbreak consisting of a
social outdoor event with public transportation is a common
daily event, providing potentiallygreater generalizability to our
results.
Our study also has limitations. During the worship event
outbreak, alternative sources of infection cannot be ruled out
completely. Howe ver, there were no confirmed cases in Ningbo
city before January 19, 2020 (when the worship event oc-
curred). The first confirmed case of COVID-19 in Ningbo city
was reported on January 20, 2020, and the city had a total of
69 confirmed cases by the end of January.Apparently, the out-
break occurred during the early stage of a modest level of dis-
ease spread in Ningbo city. Considering that Ningbo is a city
with a total population of more than 8 million, the possibility
of having more than 1 source patient at the worship event on
January 19 would be quite low. Meanwhile, most secondary
cases started to show symptoms after January 21, 2020, more
than 2 days after the worship event.The c urrentliteratures sug-
gest that presymptomatic transmission often occurs within a
2-day or 3-day window before symptom onset (ie, viral shed-
ding may begin 2 to 3 days before the appearance of the first
symptoms).
21
In addition, no one else on bus 2 had recent travel
history to Wuhan or reported being in contact with someone
from Wuhan. Considering these factors, the possibility of hav-
ing another person on the bus who was able to spread the vi-
rus at the time of the bus ride was relatively low, if not com-
pletely impossible. Our sample size of infected cases within
the exposed bus was somewhat limited, which could havecon-
tributed to the nonsignificant results regarding the associa-
tion of distance from the index patient with infection risk.
While the high attack rate and the distribution of cases on bus
2 is consistent with airborne transmission, there is no way to
rule out a common surface, such as a pole, because of pos-
sible insufficient recall. However, given that there were par-
ticipants with infection sitting in the last row, airborne trans-
mission is likely to be a partial transmission route.
Conclusions
We investigated a COVID-19 outbreak in Zhejiang province and
found that airborne transmission likely contributed to the high
attack rate seen. The investigations suggestthat, in closed en-
vironments with air recirculation, SARS-CoV-2is a highly trans-
missible pathogen. Our finding of potential airborne transmis-
sion has important public health significance, and future efforts
at prevention and control shouldconsider the potential for air-
borne spread of COVID-19.
ARTICLE INFORMATION
Accepted for Publication: August 11, 2020.
Published Online: September 1, 2020.
doi:10.1001/jamainternmed.2020.5225
Author Affiliations: Department of Epidemiology
and Biostatistics, University of Georgia College of
Public Health, Athens (Shen, C. Li, Handel, Ebell);
Department of Epidemiology, Tulane University
School of Public Health and Tropical Medicine, New
Orleans, Louisiana (C. Li); Ningbo Municipal Center
for Disease Control and Prevention, Ningbo, China
(Dong, Yi, A. Wang, Xu); Zhejiang Provincial Center
for Disease Control and Prevention, Hangzhou,
China (Z. Wang, Z. Chen, E. Chen, X. Wang, Ling);
Division of Infectious Diseases and Geographic
Medicine, Stanford University School of Medicine,
Stanford, California (Martinez); Hangzhou
Municipal Center for Disease Control and
Prevention, Hangzhou, China (Sun, J. Chen); Health
Informatics Institute, University of Georgia College
of Public Health, Athens (Handel); Center for the
Ecology of Infectious Diseases, University of
Georgia, Athens (Handel); Renmin University of
China School of Statistics, Beijing, China (F.Wang,
Y.Li); Statistical Consulting Center, Renmin
University of China, Beijing, China (F.Wang, Y. Li);
Haishu Center for Disease Control and Prevention,
Ningbo, China (H. Wang, B. Chen); Department of
Health Care Administration, California State
University Long Beach, College of Health and
Human Services, Long Beach (Qi); Department of
Clinical Epidemiology and Tobacco Dependence
Treatment Research, Beijing Chaoyang Hospital,
Beijing, China (Liang); Center for Applied Statistics,
Renmin University of China, Beijing, China (Y. Li).
Author Contributions: Dr Ling had full access to all
of the data in the study and takes responsibility for
the integrity of the data and the accuracy of the
data analysis. Drs Shen, C. Li, Dong,Z. Wang, and Y.
Li are co–first authors. Drs Ling, J. Chen, and Xu are
co–senior authors.
Conflict of Interest Disclosures: None reported.
Funding/Support: This study was funded by a
Ningbo Science and Technology Major Project
Grant (2020C50001) and Zhejiang Science and
Technology Major Project Grant (2020C03124).
Role of the Funder/Sponsor:The funding
organizations had no role in the design and conduct
of the study; collection, management, analysis, and
interpretation of the data; preparation, review, or
approval of the manuscript; and decision to submit
the manuscript for publication.
REFERENCES
1. Li Q, Guan X, Wu P, et al. Early transmission
dynamics in Wuhan, China, of novel
coronavirus-infected pneumonia. N Engl J Med.
2020;382(13):1199-1207. doi:10.1056/
NEJMoa2001316
2. Chen N, Zhou M, Dong X, et al. Epidemiological
and clinical characteristics of 99 cases of 2019
novel coronavirus pneumonia in Wuhan, China:
a descriptive study.Lancet. 2020;395(10223):507-
513. doi:10.1016/S0140-6736(20)30211-7
3. World Health Organization. Coronavirus disease
2019 (COVID-19) situation report—197. Accessed
August 5, 2020.https://www.who.int/docs/default-
source/coronaviruse/situation-reports/
20200804-covid-19-sitrep-197.pdf?sfvrsn=
94f7a01d_2
4. Chan JF-W, YuanS, Kok K-H, et al. A familial
cluster of infection associated with the 2019 novel
coronavirus indicating possible person-to-person
transmission during the incubation period. Lancet.
2020;395(10223):514-523. doi:10.1016/S0140-6736
(20)30154-9
5. Yu P,Zhu J, Zhang Z, Han Y, Huang L. A familial
cluster of infection associated with the 2019 novel
coronavirus indicating potential person-to-person
transmission during the incubation period. J Infect Dis.
2020;221(11):1757-1761. doi:10.1093/infdis/jiaa077
6. Phan LT,Nguyen TV, Luong QC, et al.
Importation and human-to-human transmission of
Research Original Investigation Community Outbreak Investigation of SARS-CoV-2 Transmission Among Bus Riders in Eastern China
E6 JAMA Internal Medicine Published online September 1, 2020 (Reprinted) jamainternalmedicine.com
© 2020 American Medical Association. All rights reserved.
Downloaded From: https://jamanetwork.com/ on 09/03/2020
a novel coronavirus in Vietnam. N Engl J Med.2020;
382(9):872-874.doi:10.1056/NEJMc2001272
7. Tellier R, Li Y,Cowling BJ, Tang JW.Recognition
of aerosol transmission of infectious agents:
a commentary. BMC InfectDis. 2019;19(1):101.
doi:10.1186/s12879-019-3707-y
8. Jones RM, Brosseau LM. Aerosol transmission of
infectious disease. J Occup Environ Med. 2015;57
(5):501-508. doi:10.1097/JOM.
0000000000000448
9. Wong TW, Lee CK, TamW, et al; Outbreak Study
Group. Cluster of SARS among medical students
exposed to single patient, Hong Kong. Emerg Infect
Dis. 2004;10(2):269-276. doi:10.3201/eid1002.
030452
10. Olsen SJ, Chang HL, Cheung TY, et al.
Transmission of the severeacute respiratory
syndrome on aircraft. N Engl J Med. 2003;349(25):
2416-2422. doi:10.1056/NEJMoa031349
11. Yu IT, Li Y, Wong TW, et al. Evidence of airborne
transmission of the severe acute respiratory
syndrome virus. N Engl J Med. 2004;350(17):1731-
1739. doi:10.1056/NEJMoa032867
12. Nishiura H, Oshitani H, Kobayashi T,et al.
Closed environments facilitate secondary
transmission of coronavirus disease 2019
(COVID-19). medRxiv. Preprint posted online March
3, 2020. doi:10.1101/2020.02.28.20029272
13. Hodcroft EB. Preliminary case report on the
SARS-CoV-2cluster in the UK, France, and Spain.
Swiss Med Wkly. 2020;150(9-10). doi:10.4414/smw.
2020.20212
14. van Doremalen N, Bushmaker T, Morris DH,
et al. Aerosol and surface stability of SARS-CoV-2as
compared with SARS-CoV-1. N Engl J Med.2020;
382(16):1564-1567. doi:10.1056/NEJMc2004973
15. Kim YI, Kim SG, Kim SM, et al. Infection and
rapid transmission of SARS-CoV-2 in ferrets. Cell
Host Microbe. 2020;27(5):704-709.e2. doi:10.1016/
j.chom.2020.03.023
16. Richard M, Kok A, de Meulder D, et al.
SARS-CoV-2is transmitted via contact and via the
air between ferrets. Nat Commun. 2020;11(1):3496.
doi:10.1038/s41467-020-17367-2
17. WHO recommended measures for persons
undertaking international travel from areas affected
by severe acute respiratory syndrome (SARS). Wkly
Epidemiol Rec. 2003;78(14):97-99.
18. Hertzberg VS, Weiss H. On the 2-row rule for
infectious disease transmission on aircraft. Ann
Glob Health. 2016;82(5):819-823. doi:10.1016/j.
aogh.2016.06.003
19. Pagano M, Gauvreau K. Principles of
Biostatistics. CRC Press; 2018.
20. Arons MM, Hatfield KM, Reddy SC, et al; Public
Health–Seattle and King County and CDC COVID-19
Investigation Team.Presymptomatic SARS-CoV-2
infections and transmission in a skilled nursing
facility.N Engl J Med. 2020;382(22):2081-2090.
doi:10.1056/NEJMoa2008457
21. He X, Lau EHY, Wu P, et al. Temporal dynamics
in viral shedding and transmissibility of COVID-19.
Nat Med. 2020;26(5):672-675. doi:10.1038/s41591-
020-0869-5
22. Lu J, Gu J, Li K, et al. COVID-19outbreak
associated with air conditioning in restaurant,
Guangzhou, China, 2020. Emerg InfectDis.2020;
26(7):1628-1631. doi:10.3201/eid2607.200764
23. Moser MR, Bender TR, Margolis HS, Noble GR,
Kendal AP, Ritter DG. An outbreak of influenza
aboard a commercial airliner. Am J Epidemiol. 1979;
110(1):1-6. doi:10.1093/oxfordjournals.aje.a112781
24. Liu Y, Ning Z, Chen Y, et al. Aerodynamic
analysis of SARS-CoV-2in two Wuhan hospitals.
Nature. 2020;582(7813):557-560.doi:10.1038/
s41586-020-2271-3
25. Ong SWX, Tan YK, Chia PY, e t al. Air, surface
environmental, and personal protective equipment
contamination by severe acute respiratory
syndrome coronavirus 2 (SARS-CoV-2)from a
symptomatic patient. JAMA. 2020;232(16):1610-1612.
doi:10.1001/jama.2020.3227
Community Outbreak Investigation of SARS-CoV-2 Transmission Among Bus Riders in Eastern China Original Investigation Research
jamainternalmedicine.com (Reprinted) JAMA Internal Medicine Published online September 1, 2020 E7
© 2020 American Medical Association. All rights reserved.
Downloaded From: https://jamanetwork.com/ on 09/03/2020
