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

Abstract

Background 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 COVID-19 outbreaks have not been reported. Methods We conducted an investigation of a pet shop-related COVID-19 outbreak due to Delta variant AY.127 involving at least three 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 RT-PCR-positive samples. Results 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 ELISA. 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. Conclusions 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.

Contribution of low population immunity to the severe Omicron BA.2 outbreak in Hong Kong

“…There was limited local transmission in January 2022 due to several Omicron variant-related clusters which could be traced to imported cases (n=836), including a BA.1 outbreak in a restaurant and a large Omicron BA.2 outbreak in a housing estate which we reported previously 40,41 (Figure 4A). There was also a cluster of pet-storerelated Delta variant AY.127 42 . Since early February, 2022, there was an exponential increase in cases from <200 cases per day before February 4 to a peak of 76,991 cases (56,827 con rmed by nucleic acid test and 20,164 con rmed by self-collected rapid antigen test on March 3, 2022 43,44 .…”

“…We have previously reported our viral genome sequencing results for specimens collected up to February 2, 2022, including those from an Omicron BA.1 restaurant outbreak 41 , an Omicron BA.2 housing estate outbreak 40 , and a Delta AY.127 outbreak related to pet stores 42 . Here, we have performed additional sequencing for specimens collected in Hong Kong up to March 11, 2022 (Supplementary Table S2).…”

“…Results of the surrogate NAb and live virus NAb against the ancestral virus for serum specimens collected between January and April 2021 was reported in our previous publication 30 , but the result of NAb against the Omicron sublineages BA.1 or BA.2 has not been reported before. For viral genome sequencing, 382 sequences were reported in our previous publications 40,41,42 . In the current study, we have performed genome sequencing for 163 randomly selected archived respiratory specimens collected from patients admitted to Queen Mary Hospital.…”

Lessons learned from the fifth wave of COVID-19 in Hong Kong in early 2022

“…There was no local transmission in the next 40 days until two crew members of Cathay Pacific Airlines brought the virus to our communities. Although we successfully contained the transmission of the Omicron variant from these two sources and that of the Delta variant from hamsters in the pet stores to humans [ 2 ], the highly transmissible BA.2 subvariant of Omicron outcompeted our containment efforts. The explosive spreading of BA.2 was retrospectively determined to initiate from an incident in a quarantine hotel, where a South Asian woman was infected by other foreign quarantinees staying in another room and with no face-to-face contact.…”

SARS‐CoV‐2 and natural infection in animals

“…50 The origin of this case was associated with the SARS‐CoV‐2 δ variant AY.127 in Hong Kong, and an epidemiological investigation of these patients revealed that they were all associated with a local pet store. 7 , 8 , 51 SARS‐CoV‐2‐positive samples were found in environmental and hamster samples from pet stores as well as in the associated supply warehouses. However, the hamsters were not exhibiting clinical signs.…”