Probable Animal-to-Human Transmission of Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Delta Variant AY.127 Causing a Pet Shop-Related Coronavirus Disease 2019 (COVID-19) Outbreak in Hong Kong.

Jasper Fuk Woo Chan1,2 Gilman Kit Hang Siu3 Shuofeng Yuan1 Jonathan Daniel Ip1 Jian Piao Cai1 Allen Wing Ho Chu1 Wan Mui Chan1 Syed Muhammad Umer Abdullah1 Cuiting Luo1 Brian Pui Chun Chan1 Terrence Tsz Tai Yuen1 Lin Lei Chen1 Kenn Ka Heng Chik1 Ronghui Liang1 Hehe Cao1 Vincent Kwok Man Poon1 Chris Chung Sing Chan1 Kit Hang Leung2 Anthony Raymond Tam4 Owen Tak Yin Tsang5 Jacky Man Chun Chan5 Wing Kin To6 Bosco Hoi Shiu Lam6 Lam Kwong Lee3 Hazel Wing Hei Lo3 Ivan Tak Fai Wong3 Jake Siu Lun Leung3 Evelyn Yin Kwan Wong3 Hin Chu1 Cyril Chik Yan Yip2 Vincent Chi Chung Cheng1,2 Kwok Hung Chan1 Herman Tse7 David Christopher Lung7,8 Kenneth Ho Leung Ng9 Albert Ka Wing Au9 Ivan Fan Ngai Hung4,10 Kwok Yung Yuen1,2 Kelvin Kai Wang To1,2
Affiliations 10 institutions
  1. State Key Laboratory for Emerging Infectious Diseases, Carol Yu Centre for Infection, Department of Microbiology, School of Clinical Medicine, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, People's Republic of China.
  2. Department of Microbiology, Queen Mary Hospital, Hong Kong Special Administrative Region, People's Republic of China.
  3. Department of Health Technology and Informatics, The Hong Kong Polytechnic University, Hong Kong Special Administrative Region, People's Republic of China.
  4. Department of Medicine, Queen Mary Hospital, Hong Kong Special Administrative Region, People's Republic of China.
  5. Department of Medicine and Geriatrics, Princess Margaret Hospital, Hong Kong Special Administrative Region, People's Republic of China.
  6. Department of Pathology, Princess Margaret Hospital, Hong Kong Special Administrative Region, People's Republic of China.
  7. Department of Pathology, Hong Kong Children's Hospital, Hong Kong Special Administrative Region, People's Republic of China.
  8. Department of Pathology, Queen Elizabeth Hospital, Hong Kong Special Administrative Region, People's Republic of China.
  9. Centre for Health Protection, Department of Health, Hong Kong Special Administrative Region, People's Republic of Chinaand.
  10. Department of Medicine, School of Clinical Medicine, Li Ka Shing Faculty of Medicine, Pokfulam, Hong Kong Special Administrative Region, People's Republic of China.

Abstract

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) can infect human and other mammals, including hamsters. Syrian (Mesocricetus auratus) and dwarf (Phodopus sp.) hamsters are susceptible to SARS-CoV-2 infection in the laboratory setting. However, pet shop-related Coronavirus Disease 2019 (COVID-19) outbreaks have not been reported. We conducted an investigation of a pet shop-related COVID-19 outbreak due to Delta variant AY.127 involving at least 3 patients in Hong Kong. We tested samples collected from the patients, environment, and hamsters linked to this outbreak and performed whole genome sequencing analysis of the reverse transcription polymerase chain reaction (RT-PCR)-positive samples. The patients included a pet shop keeper (Patient 1), a female customer of the pet shop (Patient 2), and the husband of Patient 2 (Patient 3). Investigation showed that 17.2% (5/29) and 25.5% (13/51) environmental specimens collected from the pet shop and its related warehouse, respectively, tested positive for SARS-CoV-2 RNA by RT-PCR. Among euthanized hamsters randomly collected from the storehouse, 3% (3/100) tested positive for SARS-CoV-2 RNA by RT-PCR and seropositive for anti-SARS-CoV-2 antibody by enzyme immunoassay. Whole genome analysis showed that although all genomes from the outbreak belonged to the Delta variant AY.127, there were at least 3 nucleotide differences among the genomes from different patients and the hamster cages. Genomic analysis suggests that multiple strains have emerged within the hamster population, and these different strains have likely transmitted to human either via direct contact or via the environment. Our study demonstrated probable hamster-to-human transmission of SARS-CoV-2. As pet trading is common around the world, this can represent a route of international spread of this pandemic virus.

Supporting text Virus Host Location
2 1 CoV 3 Delta variant AY.127 1 hamsters 1 pet 3 SARS 6 transmission 55 COVID-19 425 SARS-CoV-2 453 Animals 1948 Cricetinae 41 Disease Outbreaks 170 Female 289 Hong Kong 21 Humans 1440 Mammals 92 RNA, Viral 193 SARS-CoV-2 variants 86

Evidence records

6 total
Zoonotic Surveillance
3 records · 2 evidence types
Evidence type
2 records
OVE5720
Key finding

Euthanized hamsters from the storehouse tested positive for SARS-CoV-2 RNA by RT-PCR.

Virus
Host
Location
Supporting text

Among euthanized hamsters randomly collected from the storehouse, 3% (3/100) tested positive for SARS-CoV-2 RNA by RT-PCR.

Method
RT-PCR
Sample type
hamster samples
Geographic raw
storehouse
OVE5719
Key finding

Environmental specimens from the pet shop and warehouse contained detectable SARS-CoV-2 RNA by RT-PCR.

Virus
Host
Not specified
Location
Supporting text

17.2% (5/29) and 25.5% (13/51) environmental specimens collected from the pet shop and its related warehouse, respectively, tested positive for SARS-CoV-2 RNA by RT-PCR.

Method
RT-PCR
Sample type
environmental specimens
Geographic raw
pet shop | warehouse
Evidence type
1 records
OVE5721
Key finding

Randomly collected storehouse hamsters were seropositive for anti-SARS-CoV-2 antibody by enzyme immunoassay.

Virus
Host
Location
Not specified
Supporting text

Among euthanized hamsters randomly collected from the storehouse, 3% (3/100) tested positive for SARS-CoV-2 RNA by RT-PCR and seropositive for anti-SARS-CoV-2 antibody by enzyme immunoassay.

Method
enzyme immunoassay
Transmission Evidence
2 records · 2 evidence types
Evidence type
1 records
OVE5723
Key finding

The study demonstrated probable hamster-to-human transmission of SARS-CoV-2 Delta variant AY.127 during a pet shop-related outbreak in Hong Kong.

Virus
Host
Location
Supporting text

Our study demonstrated probable hamster-to-human transmission of SARS-CoV-2. We conducted an investigation of a pet shop-related COVID-19 outbreak due to Delta variant AY.127 involving at least 3 patients in Hong Kong.

Method
whole genome sequencing | RT-PCR | serological assay | environmental sampling
Study design
outbreak investigation with genomic analysis
Transmission direction
animal-to-human
Geographic raw
Hong Kong
Country inferred
CHN
Evidence type
1 records
OVE5718
Key finding

An investigation in Hong Kong identified a pet shop–related COVID-19 outbreak caused by SARS-CoV-2 Delta variant AY.127 involving at least three human patients.

Virus
Host
Location
Supporting text

We conducted an investigation of a pet shop-related COVID-19 outbreak due to Delta variant AY.127 involving at least 3 patients in Hong Kong.

Method
outbreak investigation | RT-PCR | whole genome sequencing
Transmission direction
animal-to-human
Geographic raw
Hong Kong
Country inferred
CHN
Outbreak setting
pet shop
Outbreak scale
at least 3 patients
Genomic Evolution
1 records · 1 evidence types
Evidence type
1 records
OVE5722
Key finding

Whole genome phylogenetic analysis of SARS-CoV-2 Delta variant AY.127 from the pet shop outbreak showed at least three nucleotide differences among genomes from patients and hamster cages, indicating multiple related viral strains within the outbreak.

Virus
Host
Location
Not specified
Supporting text

Whole genome analysis showed that although all genomes from the outbreak belonged to the Delta variant AY.127, there were at least 3 nucleotide differences among the genomes from different patients and the hamster cages.

Genes or proteins
whole genome
Analysis methods
whole genome sequencing | phylogenetic analysis