Transfer Rate of Enveloped and Nonenveloped Viruses between Fingerpads and Surfaces

Abstract

Fomites can represent a reservoir for pathogens, which may be subsequently transferred from surfaces to skin. In this study, we aim to understand how different factors (including virus type, surface type, time since last hand wash, and direction of transfer) affect virus transfer rates, defined as the fraction of virus transferred, between fingerpads and fomites. To determine this, 360 transfer events were performed with 20 volunteers using Phi6 (a surrogate for enveloped viruses), MS2 (a surrogate for nonenveloped viruses), and three clean surfaces (stainless steel, painted wood, and plastic). Considering all transfer events (all surfaces and both transfer directions combined), the mean transfer rates of Phi6 and MS2 were 0.17 and 0.26, respectively. Transfer of MS2 was significantly higher than that of Phi6 (P < 0.05). Surface type was a significant factor that affected the transfer rate of Phi6: Phi6 is more easily transferred to and from stainless steel and plastic than to and from painted wood. Direction of transfer was a significant factor affecting MS2 transfer rates: MS2 is more easily transferred from surfaces to fingerpads than from fingerpads to surfaces. Data from these virus transfer events, and subsequent transfer rate distributions, provide information that can be used to refine quantitative microbial risk assessments. This study provides a large-scale data set of transfer events with a surrogate for enveloped viruses, which extends the reach of the study to the role of fomites in the transmission of human enveloped viruses like influenza and SARS-CoV-2. IMPORTANCE This study created a large-scale data set for the transfer of enveloped viruses between skin and surfaces. The data set produced by this study provides information on modeling the distribution of enveloped and nonenveloped virus transfer rates, which can aid in the implementation of risk assessment models in the future. Additionally, enveloped and nonenveloped viruses were applied to experimental surfaces in an equivalent matrix to avoid matrix effects, so results between different viral species can be directly compared without confounding effects of different matrices. Our results indicating how virus type, surface type, time since last hand wash, and direction of transfer affect virus transfer rates can be used in decision-making processes to lower the risk of viral infection from transmission through fomites.

Keywords: MS2; Phi6; bacteriophages; enveloped virus; fomite; fomites; hand hygiene; surfaces; transfer; virus; virus transfer.

FIG 1

Pathway of transmission from contaminated fomites. First, the individual contacts a surface from which the individual picks up or deposits invective virus particles. Finally, the individual transfers the infective virus from their hand to an area of their body, where infection occurs, or to an additional surface.

FIG 2

Outline of experimental procedure up until the contact events. The procedure outlines the initial hand-washing step, followed by the wait time for experiment A or B, an example of surface inoculation, an example of hand inoculation, the wait time for the inoculum to dry, and the contact events. In the example surface inoculation, the leftmost square represents where the virus was not applied but where the transfer from the fingerpad to the surface would occur. The middle square represents where the virus was applied (indicating transfer from the surface to the fingerpad), and the rightmost is the control. In the example hand inoculation, the hands are duplicates. On the middle fingerpad and thumb there is no virus applied, but it represents where the transfer from the chosen surface and 2nd surface to the fingerpad will occur. Virus is applied on the index fingerpad and ring fingerpad, where transfer between the fingerpad and the respective surfaces will occur. The pinky is a control.

FIG 3

Boxplots of transfer rates for different surfaces. The upper and lower whiskers show the maximum and minimum values, respectively (excluding outliers defined by the interquartile range criterion). The lower and upper edges of the box represent the lower and upper quartile, respectively. The horizontal line within the box indicates the median. The points beyond the whiskers represent outliers. The data are broken down by virus type, surface type, time since last hand wash, and direction of transfer. Unwashed represents 1 h since last hand wash, and washed represents 0 h since last hand wash. F->S represents fingerpad-to-surface transfer, and S->F represents surface-to-fingerpad transfer.

FIG 4

Phi6 (A) and MS2 (B) histogram distributions, overlaid with probability distribution functions. The y axis shows the density or number of observations for the transfer values. The functions used to model the data are beta distributions. The alpha and beta shape parameters, as well as the goodness-of-fit P values, are also shown.