SARS-CoV and SARS-CoV-2 are transmitted through the air between ferrets over more than one meter distance

Abstract

SARS-CoV-2 emerged in late 2019 and caused a pandemic, whereas the closely related SARS-CoV was contained rapidly in 2003. Here, an experimental set-up is used to study transmission of SARS-CoV and SARS-CoV-2 through the air between ferrets over more than a meter distance. Both viruses cause a robust productive respiratory tract infection resulting in transmission of SARS-CoV-2 to two of four indirect recipient ferrets and SARS-CoV to all four. A control pandemic A/H1N1 influenza virus also transmits efficiently. Serological assays confirm all virus transmission events. Although the experiments do not discriminate between transmission via small aerosols, large droplets and fomites, these results demonstrate that SARS-CoV and SARS-CoV-2 can remain infectious while traveling through the air. Efficient virus transmission between ferrets is in agreement with frequent SARS-CoV-2 outbreaks in mink farms. Although the evidence for virus transmission via the air between humans under natural conditions is absent or weak for SARS-CoV and SARS-CoV-2, ferrets may represent a sensitive model to study interventions aimed at preventing virus transmission.

Fig. 1. Experimental transmission set-up.

Schematic representation of the set-up to assess transmission over >1 m distance. An inoculated donor ferret is housed in the bottom cage and the next day, an indirect recipient ferret is added to the top cage. The cages are connected through a hard duct system consisting of four 90° turns. The system is built of several horizontal and vertical 15 cm wide PVC pipes that allow upward airflow from the donor to the indirect recipient animal. The average length of the duct system is 118 cm with the shortest and longest length 73 and 163 cm, respectively. A steel grid is placed over the inlet and outlet of the duct system. The bottom five cm of the grid was closed to prevent spill-over of food, feces, and other large particles into the tube system. Orange arrows indicate the direction of airflow (100 L/min). Set-ups were placed in class III isolators in a biosafety level 3+ laboratory.

Fig. 2. Virus RNA shedding in ferrets.

A/H1N1 (a), SARS-CoV-2 (b), and SARS-CoV (c) RNA were detected by qRT-PCR in the throat (gray) and nasal (white) swabs collected from a donor (bars) and recipient (circles) ferrets every other day. An individual donor-recipient pair is shown in each panel.

Fig. 3. Infectious virus shedding in ferrets.

A/H1N1 virus (a), SARS-CoV-2 (b), and SARS-CoV (c) titers were detected in the throat (gray) and nasal (white) swabs collected from inoculated donor (bars) and indirect recipient (circles) ferrets. An individual donor-recipient pair is shown in each panel. The dotted line indicates the detection limit.

Fig. 4. Antibody responses in donor and recipient ferrets.

Sera were collected from donor and recipient ferrets on the indicated days. Antibody responses against A/H1N1 virus (a) were measured by hemagglutination inhibition (HI) assay, whereas responses against SARS-CoV-2 (b) and SARS-CoV (c) were assessed using a nucleoprotein (NP) ELISA. Dotted lines indicate the detection limit of each assay. OD: Optic density.

Fig. 5. Detection of SARS-CoV RNA on the fur of donor ferrets.

SARS-CoV RNA was detected by qRT-PCR in swabs collected from the fur on the left (dark gray) and right (light gray) flank of all four donor ferrets. An infectious virus was not detected in these samples.