Co-circulation of two SARS-CoV-2 variant strains within imported pet hamsters in Hong Kong.

Kin-Hang Kok1,2 Shuk-Ching Wong3 Wan-Mui Chan1 Lei Wen1 Allen Wing-Ho Chu1 Jonathan Daniel Ip1 Lam-Kwong Lee4 Ivan Tak-Fai Wong4 Hazel Wing-Hei Lo4 Vincent Chi-Chung Cheng1,3,5 Alex Yat-Man Ho6 Bosco Hoi-Shiu Lam6 Herman Tse7 David Lung8 Ken Ng Ho-Leung Ng9 Albert Ka-Wing Au9 Gilman Kit-Hang Siu4 Kwok-Yung Yuen1,2,5
Affiliations 9 institutions
  1. State Key Laboratory of Emerging Infectious Diseases, Carol Yu Centre for Infection, Department of Microbiology, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, People's Republic of China.
  2. bCentre for Virology, Vaccinology and Therapeutics, Hong Kong Science and Technology Park, Hong Kong Special Administrative Region, People's Republic of China.
  3. Infection Control Team, Queen Mary Hospital, Hong Kong West Cluster, Hong Kong Special Administrative Region, People's Republic of China.
  4. Department of Health Technology and Informatics, The Hong Kong Polytechnic University, Hong Kong Special Administrative Region, People's Republic of China.
  5. Department of Microbiology, Queen Mary 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 China.

Abstract

During the investigation of a pet shop outbreak of severe acute respiratory coronavirus 2 (SARS-CoV-2) with probable hamster-to-human transmission, the environmental and hamster samples in epidemiologically linked pet shops were found positive for SARS-CoV-2 Delta variant AY.127 strains which are phylogenetically closely related to patients and reported European strains. This interspecies' spill-over has triggered transmission in 58 patients epidemiologically linked to three pet shops. Incidentally, three dwarf hamsters imported from the Netherlands and centralized in a warehouse distributing animals to pet shops were positive for SARS-CoV-2 spike variant phylogenetically related to European B.1.258 strains from March 2020. This B.1.258 strain almost disappeared in July 2021. While no hamster-to-human transmission of B.1.258-like strain was found in this outbreak, molecular docking showed that its spike receptor-binding domain (RBD) has a similar binding energy to human ACE2 compared to that of Delta variant AY.127. Therefore, the potential of this B.1.258-related spike variant for interspecies jumping cannot be ignored. The co-circulation of B.1.258-related spike variants with Delta AY.127, which originated in Europe and was not previously found in Hong Kong, suggested that hamsters in our wholesale warehouse and retail pet shops more likely have acquired these viruses in the Netherlands or stopovers during delivery by aviation than locally. The risk of human-to-hamster reverse zoonosis by multiple SARS-CoV-2 variants leading to further adaptive spike mutations with subsequent transmission back to humans cannot be underestimated as an outbreak source of COVID-19. Testing imported pet animals susceptible to SARS-CoV-2 is warranted to prevent future outbreaks.

Supporting text Virus Host Location
Animal 6 coronavirus 195 hamster 4 interspecies 3 SARS-CoV-2 550 transmission 55 COVID-19 425 SARS-CoV-2 453 Animals 1948 Cricetinae 41 Hong Kong 21 Humans 1440 Molecular Docking Simulation 5 Spike Glycoprotein, Coronavirus 274 SARS-CoV-2 variants 86

Evidence records

5 total
Zoonotic Surveillance
2 records · 1 evidence types
Evidence type
2 records
OVE5622
Key finding

Environmental and hamster samples from epidemiologically linked Hong Kong pet shops tested positive for SARS-CoV-2 Delta variant AY.127 strains.

Virus
Host
Location
Supporting text

Environmental and hamster samples in epidemiologically linked pet shops were found positive for SARS-CoV-2 Delta variant AY.127 strains which are phylogenetically closely related to patients and reported European strains.

Method
viral RNA detection | genomic sequencing | phylogenetic analysis
Sample type
environmental samples | hamster specimens
Geographic raw
Hong Kong
Country inferred
CHN
OVE5623
Key finding

Three dwarf hamsters imported from the Netherlands were positive for SARS-CoV-2 spike variant phylogenetically related to European B.1.258 strains.

Virus
Host
Location
Supporting text

Three dwarf hamsters imported from the Netherlands and centralized in a warehouse distributing animals to pet shops were positive for SARS-CoV-2 spike variant phylogenetically related to European B.1.258 strains from March 2020.

Method
viral RNA detection | genomic sequencing | phylogenetic analysis
Sample type
hamster specimens
Geographic raw
Netherlands | Hong Kong
Country inferred
NLD | CHN
Transmission Evidence
1 records · 1 evidence types
Evidence type
1 records
OVE5624
Key finding

Probable hamster-to-human spillover of SARS-CoV-2 Delta variant AY.127 occurred during a pet shop outbreak in Hong Kong, resulting in 58 human infections.

Virus
Host
Location
Supporting text

During the investigation of a pet shop outbreak of severe acute respiratory coronavirus 2 (SARS-CoV-2) with probable hamster-to-human transmission, the environmental and hamster samples in epidemiologically linked pet shops were found positive for SARS-CoV-2 Delta variant AY.127 strains which are phylogenetically closely related to patients and reported European strains. The co-circulation of B.1.258-related spike variants with Delta AY.127, which originated in Europe and was not previously found in Hong Kong, suggested that hamsters in our wholesale warehouse and retail pet shops more likely have acquired these viruses in the Netherlands or stopovers during delivery by aviation than locally.

Method
virus detection | phylogenetic analysis | epidemiological linkage
Study design
epidemiological outbreak investigation
Transmission direction
animal-to-human
Geographic raw
Hong Kong
Country inferred
CHN
Genomic Evolution
2 records · 1 evidence types
Evidence type
2 records
OVE5626
Key finding

Hamster-derived SARS-CoV-2 Delta variant AY.127 strains were phylogenetically closely related to human patient and European AY.127 strains.

Virus
Host
Location
Not specified
Supporting text

Environmental and hamster samples ... were found positive for SARS-CoV-2 Delta variant AY.127 strains which are phylogenetically closely related to patients and reported European strains.

Analysis methods
phylogenetic analysis
OVE5627
Key finding

Dwarf hamsters imported from the Netherlands carried a SARS-CoV-2 spike variant phylogenetically related to European B.1.258 strains from March 2020, indicating co-circulation with Delta AY.127 in Hong Kong pet shops.

Virus
Host
Location
Not specified
Supporting text

Three dwarf hamsters imported from the Netherlands and centralized in a warehouse distributing animals to pet shops were positive for SARS-CoV-2 spike variant phylogenetically related to European B.1.258 strains from March 2020.

Genes or proteins
spike protein
Analysis methods
phylogenetic analysis