Survival of Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) and Influenza Virus on Human Skin: Importance of Hand Hygiene in Coronavirus Disease 2019 (COVID-19)

Abstract

Background: The stability of the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) on human skin remains unknown, considering the hazards of viral exposure to humans. We generated a model that allows the safe reproduction of clinical studies on the application of pathogens to human skin and elucidated the stability of SARS-CoV-2 on human skin.

Methods: We evaluated the stability of SARS-CoV-2 and influenza A virus (IAV), mixed with culture medium or upper respiratory mucus, on human skin surfaces and the dermal disinfection effectiveness of 80% (weight/weight) ethanol against SARS-CoV-2 and IAV.

Results: SARS-CoV-2 and IAV were inactivated more rapidly on skin surfaces than on other surfaces (stainless steel/glass/plastic); the survival time was significantly longer for SARS-CoV-2 than for IAV (9.04 hours [95% confidence interval, 7.96- 10.2 hours] vs 1.82 hours [1.65-2.00 hours]). IAV on other surfaces was inactivated faster in mucus versus medium conditions, while SARS-CoV-2 showed similar stability in the mucus and medium; the survival time was significantly longer for SARS-CoV-2 than for IAV (11.09 hours [10.22-12.00 hours] vs 1.69 hours [1.57-1.81 hours]). Moreover, both SARS-CoV-2 and IAV in the mucus/medium on human skin were completely inactivated within 15 seconds by ethanol treatment.

Conclusions: The 9-hour survival of SARS-CoV-2 on human skin may increase the risk of contact transmission in comparison with IAV, thus accelerating the pandemic. Proper hand hygiene is important to prevent the spread of SARS-CoV-2 infections.

Keywords: SARS-CoV-2; hand hygiene; human skin; influenza A virus; stability.

Figure 1.

 Outline of the pathogen stability evaluation model and its reproducibility. The pathogen stability evaluation model was constructed using human skin collected from forensic autopsy specimens (A). To evaluate the reproducibility of the model, IAV was applied to the 6 model skin samples and to the hand skin of 6 subjects (amount of virus: 1.0 × 10⁵ FFU), and the titer of the remaining viruses on the skin was measured. The 95% confidence interval (red bars) of the viable virus titer on the model skin at each elapsed time was within the 95% confidence interval (blue bars) of the viable virus titer on the skin of live individuals (B). Abbreviations: FFU, focus-forming units; IAV, influenza A virus.

Figure 2.

A–F, Fluctuations in the titer of SARS-CoV-2 and IAV surviving on the surface of stainless steel (A), borosilicate glass (B), polystyrene (C), and 3 skin samples (HS1 [D], HS2 [E], and HS3 [F]). SARS-CoV-2/IAV was mixed with DMEM or mucus and applied in 5-µL aliquots to each surface (amount of virus: 1.0 × 10⁵ FFU or 1.0 × 10⁵ TCID₅₀, respectively). Each surface was incubated in a constant environment (temperature: 25°C; humidity: 45–55%) for 0–120 hours. The remaining viruses on the surface were then recovered in 1 mL of culture medium and titrated. For each measurement, 3 independent experiments were performed, and the results are expressed as the mean ± standard error of the mean. Bars referring to the data below the detection limit were omitted. See Supplementary Figures 1 and 2 for raw data. Abbreviations: DMEM, Dulbecco’s modified Eagle’s medium; FFU, focus-forming units; IAV, influenza A virus; SARS-CoV-2, severe acute respiratory syndrome coronavirus 2; TCID₅₀, 50% tissue culture infectious dose.

Figure 3.

Evaluation of the disinfection effectiveness of 80% (w/w) ethanol against SARS-CoV-2 (upper panel) and IAV (lower panel) on human skin. Thirty minutes after the mixture of the DMEM/mucus and SARS-CoV-2/IAV was applied to each skin surface (HS1/HS2/HS3), 80% ethanol was further applied to the skin surfaces for 15 seconds, followed by disinfectant inactivation via dilution with culture medium. The surviving viruses on the skin surfaces were then titrated. For comparison, the surviving viruses on the skin surfaces in the absence of ethanol were also titrated over time. For each measurement, 3 independent experiments were performed, and the results are expressed as mean ± standard error values. Abbreviations: DMEM, Dulbecco’s modified Eagle’s medium; IAV, influenza A virus; SARS-CoV-2, severe acute respiratory syndrome coronavirus 2; TCID₅₀, 50% tissue culture infectious dose; w/w, weight/weight.