CDC Weekly

Notes from the Field

A Reemergent Case of COVID-19 — City, Heilongjiang Province, China, April 9, 2020

Jun Xu1,&; Yong Zhang2,3,&; Xiang Zhao2,3,&; Dayan Wang2,3; Weiping Dai1; Guangyu Jiao1; Shiwen Wang2,3; Jun Liu2,3; Weifeng Shi4; Cao Chen2,3; Shuhong Chen1; Shichun Yan1; Hua Hua1; George F. Gao2,3,5; Wenbo Xu2,3,#; Guizhen Wu2,3,#

As of February 22, a total of 198 confirmed There was a total of eight nucleotide mutations COVID-19 cases were reported in Harbin, between them. This strain possessed the nucleotide Heilongjiang Province, and no new local cases were mutations C241T, C1059T, C3037T, C14408T, reported in Harbin over the next 54 days (1). A23403G, and G25563T, which were consistent with However, on April 9, a newly confirmed COVID-19 the characteristics of the North American branch of the case was reported with an unknown source of infection L lineage from Europe (Figure 1) (3). In addition, (2). The patient, a 54-year-old male, developed a fever sequence alignment also revealed two mutations on March 28 with the highest recorded temperature at C26636T and C27213T in the virus genome from this 37.5 ℃ . On April 7, the symptoms worsened and patient. Among them, C1059T, C14408T, A23403G, included dyspnea, cough, sputum, chest pain, and and G25563T caused amino acid substitutions, which other symptoms, though he did not experience chest were located on 5’-UTR, ORF1ab, S protein, and distress, heart palpitations, nausea and vomiting, ORF3a, respectively. This means that despite amino abdominal pain or diarrhea. He went to the fever clinic acid mutations in the virus, its biological of the Harbin Second Hospital and was admitted to characteristics, including its ability to bind to its the isolation ward with a temperature of 37.2°C. The receptor have not changed significantly. patient also had a history of diabetes. Epidemiological investigations showed that the The results of a routine blood examination were patient had no travel, residence, or stay history in 9 9 normal (WBC 5.15×10 /L; lymphocyte 1.66×10 /L, City and surrounding areas or other lymphocyte percentage 32.3%; neutrophil percentage communities with confirmed COVID-19 case 14 days 51.9%, c-reactive protein 36.56 mg/L). Chest before the onset of disease (March 14–March 28). computed tomography (CT) showed multiple lymph There was no contact with people with fever or node shadows in the mediastinum and multiple respiratory symptoms from Wuhan City and lamellar ground glass density shadows and mesh surrounding areas nor from communities with shadows in both lungs. On April 7, the throat swabs of confirmed case reports, nor did the patient have a the patients were tested by Harbin CDC by using real- history of overseas travel. time reverse transcription-polymerase chain reaction However, because this patient did not seek medical (real-time RT-PCR) targeting the ORF 1ab and N treatment and isolation immediately after the onset of genes of COVID-19 virus, and the results showed that fever, he still had normal social activities including the nucleic acid of COVID-19 virus of the throat swab holding a dinner party. Due to the prevalence of was positive. On April 8, Harbin CDC tested his asymptomatic COVID-19 infection, epidemiological pharyngeal swabs, blood, urine and stool samples investigation and virus tracking surrounding this case again. COVID-19 nucleic acids were detected, but the became more challenging. Although the local test for serum antibodies for COVID-19 was negative. transmission of the COVID-19 virus in the mainland The National Institute for Viral Disease Control and of China had been interrupted, COVID-19 is still an Prevention (IVDC) of China CDC conducted whole- epidemic in many other countries. Many cases of genome sequencing analysis on a pharyngeal swab COVID-19 and asymptomatic infections entering sample of the patient, which showed 99.97% nucleic China through airports and land ports have been acid similarity to the reference strain EPI_ISL_402119, detected (4). Therefore, it is necessary to strengthen which was isolated from Wuhan on January 7, 2020. COVID-19 surveillance in respiratory tract and stool

460 CCDC Weekly / Vol. 2 / No. 25 Chinese Center for Disease Control and Prevention China CDC Weekly

EPI ISL 421636|hCoV-19/Australia/NSWID930/2020|Oceania/Australia| EPI ISL 420238|hCoV-19/England/SHEF-C051C/2020|Europe/England| EPI ISL 424964|hCoV-19/USA/NY-NYUMC157/2020|North-America/USA| EPI ISL 422430|hCoV-19/Singapore/37/2020|Asia/Singapore| EPI ISL 422463|hCoV-19/USA/WI-GMF-00588/2020|North-America/USA| America-Branch EPI ISL 420791|hCoV-19/USA/NH 0004/2020|North-America/USA| EPI ISL 420081|hCoV-19//StPetersburg-RII3997/2020|Europe/Russia| EPI ISL 417693|hCoV-19/Iceland/25/2020|Europe/Iceland| EPI ISL 420150|hCoV-19/Norway/2084/2020|Europe/Norway| EPI ISL 418926|hCoV-19/USA/WA-UW359/2020|North-America/USA| EPI ISL 424202|hCoV-19/USA/WA-UW-1651/2020|North-America/USA| EPI ISL 418349|hCoV-19/Canada/ON PHL3650/2020|North-America/Canada| HLJ-0418-1-1 EPI ISL 422703|hCoV-19/Netherlands/NA 168/2020|Europe/Netherlands| EPI ISL 418219|hCoV-19/France/B1623/2020|Europe/France| EPI ISL 424963|hCoV-19/USA/NY-NYUMC156/2020|North-America/USA| EPI ISL 417018|hCoV-19/Belgium/ULG-6670/2020|Europe/Belgium| L-Lineage Europe-Branch L-Lineage EPI ISL 419296|hCoV-19//P1/2020|Asia/Japan| EPI ISL 419660|hCoV-19/Austria/CeMM0007/2020|Europe/Austria| EPI ISL 414626|hCoV-19/France/HF1684/2020|Europe/France| EPI ISL 424912|hCoV-19/USA/MA 9889/2020|North-America/USA| EPI ISL 420324|hCoV-19/Belgium/DVBJ-030468/2020|Europe/Belgium| EPI ISL 418390|hCoV-19/Finland/13M33/2020|Europe/Finland| EPI ISL 422623|hCoV-19/Netherlands/NA 314/2020|Europe/Netherlands| EPI ISL 412973|hCoV-19/Italy/CDG1/2020|Europe/Italy| EPI ISL 420010|hCoV-19/Australia/VIC319/2020|Oceania/Australia| EPI ISL 424616|hCoV-19/Iceland/596/2020|Europe/Iceland| EPI ISL 417530|hCoV-19/Luxembourg/LNS2128808/2020|Europe/Luxembourg| EPI ISL 414624|hCoV-19/France/N1620/2020|Europe/France| EPI ISL 416731|hCoV-19/England/SHEF-BFCC0/2020|Europe/England| EPI ISL 420623|hCoV-19/France/ARA13095/2020|Europe/France| EPI ISL 420080|hCoV-19/Russia/StPetersburg-RII3992/2020|Europe/Russia| EPI ISL 418355|hCoV-19/Canada/ON PHLU8150/2020|North-America/Canada| EPI ISL 419553|hCoV-19/USA/RI 0520/2020|North-America/USA| EPI ISL 415156|hCoV-19/Belgium/SH-03014/2020|Europe/Belgium| EPI ISL 417525|hCoV-19//CGMH-CGU-12/2020|Asia/Taiwan| EPI ISL 419559|hCoV-19/USA/FL 5125/2020|North-America/USA| EPI ISL 420555|hCoV-19/India/c32/2020|Asia/India| EPI ISL 418366|hCoV-19/Canada/ON PHL3350/2020|North-America/Canada| EPI ISL 416730|hCoV-19/England/SHEF-BFCB1/2020|Europe/England| EPI ISL 413997|hCoV-19/Switzerland/GE3895/2020|Europe/Switzerland| EPI ISL 419656|hCoV-19/Austria/CeMM0003/2020|Europe/Austria| EPI ISL 420877|hCoV-19/Australia/VIC-CBA3/2020|Oceania/Australia| EPI ISL 420129|hCoV-19/Spain/Valencia45/2020|Europe/Spain| EPI ISL 406862|hCoV-19/Germany/BavPat1/2020|Europe/Germany| EPI ISL 417732|hCoV-19/Iceland/94/2020|Europe/Iceland| EPI ISL 413016|hCoV-19/Brazil/SPBR-02/2020|South-America/Brazil| EPI ISL 420799|hCoV-19/Korea/BA-ACH 2604/2020|Asia/Korea| EPI ISL 420222|hCoV-19/England/SHEF-C02F7/2020|Europe/England| EPI ISL 406036|hCoV-19/USA/CA2/2020|North-America/USA| EPI ISL 424366|hCoV-19/Turkey/ERAGEM-001/2020|Europe/Turkey| EPI ISL 417444|hCoV-19/Pakistan/Gilgit1/2020|Asia/Pakistan| EPI ISL 414555|hCoV-19/Netherlands/Utrecht 16/2020|Europe/Netherlands| EPI ISL 420879|hCoV-19/Australia/QLDID931/2020|Oceania/Australia| S-Lineage EPI ISL 416445|hCoV-19/USA/WA-UW89/2020|North-America/USA| EPI ISL 416666|hCoV-19/USA/WA-UW128/2020|North-America/USA| EPI ISL 424673|hCoV-19/Mexico/CDMX-InDRE 06/2020|North-America/Mexico| EPI ISL 417871|hCoV-19/Iceland/9/2020|Europe/Iceland| EPI ISL 415584|hCoV-19/Canada/BC 41851/2020|North-America/Canada| EPI ISL 408478|hCoV-19//YC01/2020|Asia/China| EPI ISL 416886|hCoV-19/Malaysia/MKAK-CL-2020-6430/2020|Asia/Malaysia| EPI ISL 404253|hCoV-19/USA/IL1/2020|North-America/USA| EPI ISL 406801|hCoV-19/Wuhan/WH04/2020|Asia/China| EPI ISL 407976|hCoV-19/Belgium/GHB-03021/2020|Europe/Belgium| EPI ISL 402125|hCoV-19/Wuhan-Hu-1/2019|Asia/China| EPI ISL 407079|hCoV-19/Finland/1/2020|Europe/Finland| EPI ISL 403963|hCoV-19/Nonthaburi/74/2020|Asia/Thailand| EPI ISL 414487|hCoV-19/Ireland/COR-20134/2020|Europe/Ireland| EPI ISL 402119 |hCoV-19/Wuhan/IVDC-HB-01/2019|2019-12-30 EPI ISL 418269|hCoV-19/Vietnam/19-01S/2020|Asia/Vietnam| EPI ISL 407193|hCoV-19/South-Korea/KCDC03/2020|Asia/South-Korea| EPI ISL 408665|hCoV-19/Japan/TY-WK-012/2020|Asia/Japan| EPI ISL 413015|hCoV-19/Canada/ON-VIDO-01/2020|North-America/Canada|

0.000,050

FIGURE 1. Phylogenetic tree based on the genome sequences of COVID-19 virus. The genome of COVID-19 virus of the case in Harbin City and Wuhan City were highlighted in shades of yellow and red, respectively. S- or L-lineage of COVID-19 virus were marked and colored on the right.

Chinese Center for Disease Control and Prevention CCDC Weekly / Vol. 2 / No. 25 461 China CDC Weekly specimens among overseas visitors. of Medical Sciences, Taian, , China; 5 Chinese Center for Disease Control and Prevention, , China. Fundings: This work was supported by National & Joint first authors. Key Research and Development Program of China (Program No. 2018YFC1200305), National Science Submitted: June 12, 2020; Accepted: June 15, 2020 and Technology Major Project of China (Project No. 2018ZX10102001, 2018ZX10711001, 2018ZX1071 REFERENCES 3002, 2017ZX10104001)

doi: 10.46234/ccdcw2020.127 1. Harbin Municipal People’s Government. COVID-19 Situation in Harbin, 22 February 2020. http://www.harbin.gov.cn/art/2020/2/ # Corresponding authors: Wenbo Xu, [email protected]; 23/art_98_877381.html. [2020-02-22]. (In Chinese). Guizhen Wu, [email protected]. 2. Harbin Municipal People’s Government. COVID-19 Situation in 1 Heilongjiang Center for Disease Control and Prevention, Harbin, Harbin, 9 April 2020. http://www.harbin.gov.cn/art/2020/4/10/art_ Heilongjiang, China; 2 National Health Commission Key Laboratory 98_892639.html. [2020-04-9]. (In Chinese). for Medical Virology, National Health Commission Key Laboratory 3. Tang XL, Wu CC, X, Song YH, Yao XM, Wu XK, et al. On the for Biosafety, National Institute for Viral Disease Control and origin and continuing evolution of SARS-CoV-2. Natl Sci Rev 2020. Prevention, Chinese Center for Disease Control and Prevention, http://dx.doi.org/10.1093/nsr/nwaa036. 3 Beijing, China; Center for Biosafety Mega-Science, Chinese Academy 4. Li ZJ, Chen QL, Feng LZ, Rodewald L, Xia YY, Yu HL, et al. Active of Sciences, Wuhan, , China; 4 Key Laboratory of Etiology and case finding with case management: the key to tackling the COVID-19 Epidemiology of Emerging Infectious Diseases in Universities of pandemic. Lancet 2020. http://dx.doi.org/10.1016/S0140-6736(20) Shandong, Shandong First Medical University & Shandong Academy 31278-2.

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