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1www.eurosurveillance.org
R
Early transmission patterns of coronavirus disease 2019
(COVID-19) in travellers from Wuhan to ailand,
January 2020
Pilailuk Okada¹ , Rome Buathong² , Siripaporn Phuygun¹ , Thanutsapa Thanadachakul¹ , Sittiporn Parnmen¹ , Warawan
Wongboot¹ , Sunthareeya Waicharoen¹ , Supaporn Wacharapluesadee³ , Sumonmal Uttayamakul² , Apichart Vachiraphan2 ,
Malinee Chittaganpitch¹ , Nanthawan Mekha¹ , Noppavan Janejai¹ , Sopon Iamsirithaworn² , Raphael TC Lee , Sebastian Maurer-
Stroh4,5
1. Department of Medical Sciences, Ministry of Public Health, Thailand
2. Department of Disease Control, Ministr y of Public Health, Thailand
3. Thai Red Cross Emerging Infectious Diseases - Health Science Centre, Chulalongkorn Universit y, Thailand
4. Bioinformatics Institute, Agency for Science Technology and Research, Singapore
5. Department of Biological Sciences, National University of Singapore, Singapore
Correspondence: Pilailuk Okada (pilailuk.o@dmsc.mail.go.th)
Citation style for this article:
Okada Pilailuk , Buathong Rome , Phuygun Siripapor n , Thanadachaku l Thanutsapa , P arnmen Sittiporn , Wong boot Warawan , Waicharoen Sunthareeya ,
Wachara pluesadee Supap orn , Uttayamakul Sumonmal , Vachira phan Apichart , Chittag anpitch Malinee , Mekha Nanthawan , Janejai Nopp avan , Iamsirithaworn
Sopon , Lee Raphael T C , Maurer-Stroh Sebastian . Early transmission patter ns of coronaviru s disease 2019 (COVID -19) in travelle rs from Wuhan to Thailand, January
2020. Euro Surveill. 2020;25(8):pii=20 00097. https://doi.org/10.2807/1560-7917.ES.2020. 25.8.2000097
Article submit ted on 06 Feb 2020 / accepted on 27 Feb 2020 / publishe d on 27 Feb 2020
We report two cases of coronavirus disease 2019
(COVID-19) in travellers from Wuhan, China to
Thailand. Both were independent introductions on
separate flights, discovered with thermoscanners
and confirmed with RT-PCR and genome sequencing.
Both cases do not seem directly linked to the Huanan
Seafood Market in Hubei but the viral genomes are
identical to four other sequences from Wuhan, sug-
gesting early spread within the city already in the first
week of January.
In late December 2019, an outbreak with an initially
undiagnosed pneumonia was reported in the city of
Wuhan, Hubei Province, China, and linked to the Huanan
Seafood Market [1,2]. The causative pathogen was
identified as a novel betacoronavirus within the severe
acute respiratory syndrome (SARS) coronavirus (CoV)
family, recently termed SARS-CoV-2 [3-7]. In response
to the outbreak, several countries including Thailand,
established thermal screening at the airport for travel-
lers from Wuhan since 3 January. On 8 January and 13
January, suspected cases of infection with SARS-CoV-2
were identified at Bangkok Suvarnabhumi airport. We
report the investigation, basic clinical characteristics
and viral genomes derived from these cases.
Case 1
A woman in her early 60s from Wuhan developed a
fever with chills, sore throat and headache on 5 January
2020. She went to a local health facility in China and
received undisclosed medication. On 8 January 2020,
she took a direct ca 4 h flight to Thailand from Wuhan,
with five family members, as part of a tour group of 16
(including the case). Her measured temperature at the
arrival gate was 38.6 °C by thermoscanner, and con-
firmed with a tympanic thermometer. After being inter-
viewed by quarantine officers, she was transferred to
Bamrasnaradura Infectious Disease Institute (BIDI)
Hospital, Nonthaburi, for isolation and laborator y inves-
tigations. She reported a runny nose and sore throat
but no dyspnea or diarrhoea. Upon admission, her vital
signs were normal except for elevated blood pressure.
Her physical examination was unremarkable including
inconspicuous lung sounds. Her complete blood count
suggested a viral infection from relatively decreased
neutrophil (48%; norm: 35–75%) to lymphocyte (40%;
norm: 20–59%) ratio [8]. The chest X-ray (CXR) results
on 8 January were compatible with pneumonia with
mild thickening lung marking at both lower lungs pos-
sibly because of crowded lung rather than infiltration.
It also showed borderline cardiomegaly. Repeat CXR
after 7 days showed no remarkable changes.
In the interview, the patient explicitly stated that she
had not visited the Huanan Seafood Market but she
was living near another local market, which she visited
daily until illness onset. This market was at ca 7.5 km
distance from the Huanan Seafood Market. The patient
also reported that she had not purchased live animals
and or visited stalls with live animals. She did not visit
Jinyintai Hospital or other hospitals in Wuhan. However,
she visited local dispensaries in Wuhan to obtain medi-
cation. She also repor ted no contact with persons with
respiratory symptoms.
Clinical specimens collected on admission included
the upper respiratory tract secretions and sputum.
These specimens tested positive on 12 January for the
2www.eurosurveillance.org
CoV family by using a conventional nested RT-PCR [9].
Genomic sequencing analysis included Sanger and
next generation sequencing were performed by the
Emerging Infectious Diseases Health Science Center,
the Thai Red Cross Society and the Thai National
Institute of Health, Department of Medical Sciences
and the sequence shared via the Global Initiative
on Sharing All Influenza Data (GISAID) EpiCoV data-
base (EPI_ISL_403962). The sequencing protocol and
details are provided in the Supplementary Materials.
The patient recovered after testing negative for SARS-
CoV-2, and returned to China without signs and symp-
toms on 18 January 2020.
Case 2
A woman in her mid-70s from Wuhan landed at
Suvarnabhumi airport on 13 January. She travelled
to Thailand with three family members as part of
a tour group of 20 (including the case). An airport
thermoscanner detected a fever of 38.0 °C that was
confirmed with a tympanic thermometer. The patient
reported a sore throat, that her fever onset date was 13
January and that she had a cough for an undetermined
period. The patient was hospitalised at BIDI. Upon
admission, she reported mild tachypnoea, and her
CXR was compatible with pneumonia. Similar to case
1, the first CXR taken on 13 January, showed thickening
interstitial lung marking at both lower lung fields and
both perihilar regions because of interstitial infiltra-
tion or crowded lung marking, mild cardiomegaly and
dilated aorta. Follow-up CXR on 17 January additionally
showed recent hazy with reticular opacities at left mid-
dle lung field. The patient was not in severe condition
but stable.
In the patient interview, she reported that she did not
visit the Huanan Seafood Market or other markets.
She also reported no contact with pigs, camels, other
F 1
Phylogenetic trees of Thai sequences in context of all coronavirus families (A) and structural mapping of mutations in the
spike glycoprotein between SARS CoV (PDB:6CG [12]) and the current SARS-CoV-2 using YASARA [20] (B)
Bovine respiratory coronavirus AH187/NC 012948/1-30969
Bovine coronavirus/NC 003045/1-31028
Bovine respiratory coronavirus bovine/US/OH-440-TC/1996/NC 012949/1-30953
Human enteric coronavirus strain 4408/NC 012950/1-30953
Human coronavirus OC43/NC 005147/1-30738
Porcine hemagglutinating encephalomyelitis virus/NC 007732/1-30480
Equine coronavirus/NC 010327/1-30992
Rabbit coronavirus HKU14/NC 017083/1-31100
Rat coronavirus Parker/NC 012936/1-31250
Murine hepatitis virus strain A59/NC 001846/1-31357
Murine hepatitis virus strain JHM/NC 006852/1-31526
Human coronavirus HKU1/NC 006577/1-29926
Bat coronavirus HKU9-1/NC 009021/1-29114
Human betacoronavirus 2c EMC 2012/JX869059/1-30118
Bat coronavirus HKU5-1/NC 009020/1-30482
Bat coronavirus HKU4-1/NC 009019/1-30286
Bat coronavirus BtCoV/133/2005/NC 008315/1-30307
Bat coronavirus BM48-31/BGR/2008/NC 014470/1-29276
SARS coronavirus/NC 004718/1-29751
MG772933.1 Bat SARS-like coronavirus isolate bat-SL-CoVZC45/1-29802
MG772934.1 Bat SARS-like coronavirus isolate bat-SL-CoVZXC21/1-29732
BetaCoV/Nonthaburi/61/2020|EPI ISL 403962/1-29848
BetaCoV/Nonthaburi/74/2020|EPI ISL 403963/1-29859
Feline infectious peritonitis virus/NC 002306/1-29355
Human coronavirus NL63/NC 005831/1-27553
Human coronavirus 229E/NC 002645/1-27317
Bat coronavirus HKU2/NC 009988/1-27165
Scotophilus bat coronavirus 512/NC 009657/1-28203
Porcine epidemic diarrhea virus/NC 003436/1-28033
Bat coronavirus HKU8/NC 010438/1-28773
Bat coronavirus 1B/NC 010436/1-28476
Bat coronavirus 1A/NC 010437/1-28326
Turkey coronavirus/NC 010800/1-27657
Avian infectious bronchitis virus/NC 001451/1-27608
Beluga Whale coronavirus SW1/NC 010646/1-31686
Night-heron coronavirus HKU19/NC 016994/1-26077
Wigeon coronavirus HKU20/NC 016995/1-26227
Common-moorhen coronavirus HKU21/NC 016996/1-26223
Thrush coronavirus HKU12-600/NC 011549/1-26396
White-eye coronavirus HKU16/NC 016991/1-26041
Munia coronavirus HKU13-3514/NC 011550/1-26552
Magpie-robin coronavirus HKU18/NC 016993/1-26689
Sparrow coronavirus HKU17/NC 016992/1-26083
Porcine coronavirus HKU15/NC 016990/1-25437
100
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49
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94
100
100
49
85
52
81
A. B.
CoV: coronavirus; MERS: Middle East respiratory syndrome coronavirus; SARS: severe acute respiratory syndrome.
Panel A: blue: SARS-CoV-2; red: SARS; purple: MERS; green: common cold.
Panel B: cyan: ACE2 human host receptor; grey: CoV spike glycoprotein trimer (PDB:6ACG); red: mutations between SARS- CoV vs SARS-CoV-2.
The phylogenetic tree was created from whole genome alignment with MAFFT using the neighbour-joining method with maximum composite
likelihood (MCL) model, uniform site rates and 500 bootstrap tests using MEGA X .
3www.eurosurveillance.org
mammals (or areas with dead birds), or any consump-
tion of raw or undercooked foods. She stated that
she was not in contact with persons with respiratory
symptoms.
A conventional nested RT-PCR test of this patient was
positive for the CoV family [9]. Subsequent genome
sequencing was again compatible with the SARS-
CoV-2 and shared via the GISAID EpiCoV database
(EPI_ISL_ 403963). A nasopharyngeal swab also tested
positive by RT-PCR for adenovirus. The patient was no
longer febrile as of 17 January, and after testing nega-
tive for the CoV family by conventional nested RT-PCR,
she was discharged and she returned to China.
Genome sequence analysis
Comparing the two genome sequences with a non-
redundant selection of representatives from all known
CoV families by alignment [10] and phylogenetic tree
(Figure 1A) [11] shows that they belong to the SARS
family of betacoronaviruses and while related to SARS-
CoV (80% genome identity), they were most closely
related to SARS-like bat CoV from China (88% identity)
as closest known sequence at the time of emergence.
Structural mapping of mutations in the spike glyco-
protein between SARS CoV and the two cases of the
SARS-CoV-2 reported here shows only 76% identity
at the protein level (Figure 1B). This surface protein is
critical for ACE2 host receptor interaction and is also
a target of the immune response [12,13]. Given several
mutations in the binding interface, it may differ in host
cell binding efficiency compared with SARS-CoV which
could result in differences in virulence and transmis-
sion potential [14,15].
The genomes of the two separate cases of coronavi-
rus disease 2019 (COVID-19) are identical over the full
length of close to 30 kb and are furthermore identical
to five other sequences (four from Wuhan and one from
Zhejiang); together these sequences form the largest
cluster of identical cases within the early outbreak,
comprising a core of at least indirectly linked cases
(Figure 2). Within-outbreak sequence divergence is
generally low with 0–9 nt differences over the whole
genome and mutations unique to individual strains are
possibly related to quality differences of the samples
and noise of the methods used for sequencing.
Follow-up of contacts
Case 1 travelled in a tour group with 15 others and 40
close contacts were identified: 15 members of the tour
group, 15 people sitting within two rows in front and
back of the seat of case 1 on the same airplane, nine
crew members and one port health officer. They were
F 2
Within-outbreak SARS-CoV-2 sequence divergence and clusters, China and Thailand, January 2020
4
2019-12-24 WUHAN/IPBCAMS-WH-01
2019-12-30 WUHAN/HBCDC-HB-01
2019-12-30 WUHAN/IPBCAMS-WH-02
2019-12-30 WUHAN/IPBCAMS-WH-03
2019-12-30 WUHAN/IPBCAMS-WH-04
2019-12-30 WUHAN/IVDC-HB-01
2019-12-30 WUHAN/IVDC-HB-05
2019-12-30 WUHAN/WIV02
2019-12-30 WUHAN/WIV04
2019-12-30 WUHAN/WIV05
2019-12-30 WUHAN/WIV06
2019-12-30 WUHAN/WIV07
2020-01-01 WUHAN/IVDC-HB-04
2020-01-08 NONTHABURI/61
2020-01-13 NONTHABURI/74
2020-01-14 GUANGDONG/20SF012
2020-01-15 GUANGDONG/20SF013
2020-01-15 GUANGDONG/20SF014
2020-01-15 GUANGDONG/20SF025
2020-01-16 ZHEJIANG/WZ-01
2020-01-17 GUANGDONG/20SF028
2020-01-18 GUANGDONG/20SF040
2020-01-17 ZHEJIANG/WZ-02
9 7
4 2 7
3 1 6 1
3 1 6 1 0
5 3 8 3 2 2
5 3 8 3 2 2 4
3 1 6 1 0 0 2 2
5 3 8 3 2 2 4 4 2
3 1 6 1 0 0 2 2 0 2
5 3 8 3 2 2 4 4 2 4 2
6 4 9 4 3 3 5 5 3 5 3 5
3 1 6 1 0 0 2 2 0 2 0 2 3
3 1 6 1 0 0 2 2 0 2 0 2 3 0
6 4 9 4 3 3 5 5 3 5 3 5 6 3 3
6 4 9 4 3 3 5 5 3 5 3 5 6 3 3 0
4 2 7 2 1 1 3 3 1 3 1 3 4 1 1 4 4
6 4 9 4 3 3 5 5 3 5 3 5 6 3 3 0 0 4
5 3 8 3 2 2 4 3 2 4 2 4 5 2 2 5 5 3 5
4 2 7 2 1 1 3 3 1 3 1 3 4 1 1 4 4 2 4 3
3 1 6 1 0 0 2 2 0 2 0 2 3 0 0 3 3 1 3 2 1
4 2 7 2 1 1 3 3 1 3 1 3 4 1 1 4 4 2 4 3 0 1
2019-12-
24
WUHAN-
/IPB-
CAMS-W
H-01
2019-12-
30
WUHAN-
/HB-
CDC-HB-
01
2019-12-
30
WUHAN-
/IPB-
CAMS-
WH-02
2019-12-
30
WUHAN-
/IPB-
CAMS-
WH-03
2019-12-
30
WUHAN-
/IPB-
CAMS-W
H-04
2019-12-
30
WUHAN-
/IVDC-H
B-01
2019-12-
30
WUHAN-
/IVDC-H
B-05
2019-12-
30
WUHAN-
/WIV02
2019-12-
30
WUHAN-
/WIV04
2019-12-
30
WUHAN-
/WIV05
2019-12-
30
WUHAN-
/WIV06
2019-12-
30
WUHAN-
/WIV07
2020-01
-01
WUHAN-
/IVDC-H
B-04
2020-01
-08
NONTH-
ABURI/
61
2020-01
-13
NONTH-
ABURI/7
4
2020-01
-14
GUANG-
DONG/2
0SF012
2020-01
-15
GUANG-
DONG/2
0SF013
2020-01
-15
GUANG-
DONG/2
0SF014
2020-01
-15
GUANG-
DONG/2
0SF025
2020-01
-16
ZHEJI-
ANG/W
Z-01
2020-01
-17
GUANG-
DONG/2
0SF028
2020-01
-17
ZHEJI-
ANG/W
Z-02
2020-01
-18
GUANG-
DONG/2
0SF040
Number of pair-wise nt dif ferences across whole genomes colour-coded from zero (green) to nine (red). Blue: Thai sample names. Orange:
samples with sequences identical to each other and the Thai sequences.
We gratefully acknowledge the authors, the originating and submit ting laboratories for their sequence and metadata shared through GISAID,
on which this research is based (as listed in Supplementary Table 1).
4www.eurosurveillance.org
monitored for COVID-19 with RT-PCR tests on days 1, 12
and 14 ; all tested negative.
Case 2 travelled in a tour group with 19 others and 44
close contacts were identified: 19 members of the tour
group, 15 within two rows front and back of the seat of
case 2, nine crew members and one port health officer.
All were monitored for COVID-19 with RT-PCR tests on
days 1, 12 and 14 and all tested negative.
Discussion and conclusion
According to the cases’ history, the two impor ted
COVID-19 cases described here are not directly linked,
yet their genomes are identical. Further, according to
information provided by the cases, they have no direct
link to the Huanan Seafood Market but their genomes
are identical to four sequences from Wuhan collected
on 30 December 2019 and sequenced by three differ-
ent laboratories, indicating potential wider distribution
in the city. Although within-outbreak sequence diver-
gence is low for this virus, identical genomes of up to
30 kb are rare and a strong sign of recent transmis-
sion linkage, albeit with unknown number of genera-
tions within the transmission chain. The missing link to
the market, the time of travel and onset of symptoms
in the two COVID-19 cases together with the incuba-
tion period of mean 6.4 days (range: 5.6–7.7) [16] and
the time of closest genome neighbours obtained from
sequences in Wuhan, suggest that transmission within
Wuhan beyond the Huanan Seafood Market is likely to
have occurred in the first week of Januar y or earlier.
People travelling out of the city since then may have
spread the virus further before travel restrictions were
enforced on 23 January [17].
Thailand implemented measures for screening
patients travelling from Wuhan since 3 January 2020
at Suvarnabhumi Airport, Don Mueang, Phuket and
Chiang Mai airpor ts, and stepped up sur veillance at
public and private hospitals. The two cases described
here who tested positive for SARS-CoV-2 were the first
confirmed exported cases from China, suggesting
early international spread. Therefore, while one can-
not exclude the possibility that asymptomatic cases in
their incubation period would be missed and become
infectious later, screening of incoming travellers from
an affected area proved successful at least in these
two instances, when COVID-19 cases were detected,
isolated, observed and only discharged once they
tested negative for SARS-CoV-2. Rapid response includ-
ing genome sequencing and sharing via GISAID [18,19]
(https://www.gisaid.org/) enabled fast dissemination
of results and provided a glimpse of early transmission
patterns in this outbreak.
Acknowledgements
The authors wish to thank all the participants in this study.
We would like to thank GISAID President Peter Bogner for
help in sharing with GISAID and Dr Opart Karnkawinpong
(Director General of Depar tment of Medical Sciences) for his
support and guidance during the investigation.
Conflict of interest
None declared.
Authors’ contributions
PO, SPh, TT, SPa, WW, SWai, MC, NM and NJ contributed
work in the Department of Medical Sciences; RB, AV, SU and
SI in the Department of Disease Control; and SWac in the
Health Science Centre. RTCL and SMS provided the sequence
analysis and figures. PO and SMS drafted the manuscript.
All authors saw and agreed to the final version.
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