Decontamination of SARS-CoV-2 from cold-chain food packaging provides no marginal benefit in risk reduction to food workers

Abstract

Countries continue to debate the need for decontamination of cold-chain food packaging to reduce possible severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) fomite transmission among frontline workers. While laboratory-based studies demonstrate persistence of SARS-CoV-2 on surfaces, the likelihood of fomite-mediated transmission under real-life conditions is uncertain. Using a quantitative microbial risk assessment model of a frozen food packaging facility, we simulated 1) SARS-CoV-2 fomite-mediated infection risks following worker exposure to contaminated plastic packaging; and 2) reductions in these risks from masking, handwashing, and vaccination. In a frozen food facility without interventions, SARS-CoV-2 infection risk to a susceptible worker from contact with contaminated packaging was 1.5 × 10^-3 per 1h-period (5th - 95th percentile: 9.2 × 10^-6, 1.2 × 10^-2). Standard food industry infection control interventions, handwashing and masking, reduced risk (99.4%) to 8.5 × 10^-6 risk per 1h-period (5th - 95th percentile: 2.8 × 10^-8, 6.6 × 10^-5). Vaccination of the susceptible worker (two doses Pfizer/Moderna, vaccine effectiveness: 86-99%) with handwashing and masking reduced risk to 5.2 × 10^-7 risk per 1h-period (5th - 95th percentile: 1.8 × 10^-9, 5.4 × 10^-6). Simulating increased transmissibility of current and future variants (Delta, Omicron), (2-, 10-fold viral shedding) among a fully vaccinated workforce, handwashing and masking continued to mitigate risk (1.4 × 10^-6 - 8.8 × 10^-6 risk per 1h-period). Additional decontamination of frozen food plastic packaging reduced infection risks to 1.2 × 10^-8 risk per 1h-period (5th - 95th percentile: 1.9 × 10^-11, 9.5 × 10^-8). Given that standard infection control interventions reduced risks well below 1 × 10^-4 (World Health Organization water quality risk thresholds), additional packaging decontamination suggest no marginal benefit in risk reduction. Consequences of this decontamination may include increased chemical exposures to workers, food quality and hazard risks to consumers, and unnecessary added costs to governments and the global food industry.

Keywords: COVID-19; Cold-chain fomite-mediated transmission; Plastic packaging; Quantitative microbial risk assessment.

Fig. 1

Conceptual framework for fomite-mediated SARS-CoV-2 transmission involving exposure of a susceptible worker to individual plastic cartons, palletized cartons, and plastic wrap in a receiving warehouse under cold-chain conditions. This schematic depicts a representative frozen food manufacturing facility, initiating with two infected workers (left panel). Up to 10 contamination events per infected worker (0–10 coughs) can occur at three stages in the packaging pipeline (See Materials and methods): 1) contamination of the top-face of individual plastic cartons (144–216 individual cartons processed per hour) via respiratory droplet and aerosol fallout from the first infected worker (orange in schematic) while closing cartons filled with frozen product at the end of the tunnel freezer; 2) contamination of cartons via respiratory particle spray (droplets and aerosols) as cartons are placed (manually or via automation) on a pallet by the second infected worker (yellow in schematic); and 3) contamination of the plastic-wrapped palletized cartons by respiratory particle spray (droplet and aerosol) from the second infected worker (yellow in schematic). Four pallets, each containing approximately 36–54 individual plastic cartons, are processed per hour. All workers were assumed to be continuously wearing gloves (glove changes were not simulated) and the model assumed there was no indirect transfer of virus from the infected workers' hands to the plastic fomites along the packaging pipeline. Given current estimates of limited to no SARS-CoV-2 viral decay at and below 4 °C, the model assumed no loss in viral infectivity during the duration of cold-chain storage and shipment (−20 °C) of individual and plastic-wrapped palletized cartons prior to their handling and during unloading by a susceptible worker in a receiving warehouse. Infection risks resulting exclusively from fomite transmission were simulated as contacts between the susceptible worker's fingers and palms (of both hands) and the fomite surface (accounting for the surface area of the hand relative to the fomite surface); virus transfer from fomite to hands; and virus transfer from fingertips to facial mucous membranes (accounting for the surface area of the fingers relative to the combined surface area of the eyes, nose, and mouth). Gray boxes indicate infection control interventions implemented for the infected (masking, vaccination) and susceptible (handwashing, masking, vaccination) workers. In the scenarios with additional plastic surface decontamination, this was simulated prior to the susceptible worker contacting the fomites.

Fig. 2

Fomite-mediated SARS-CoV-2 infection risks associated with individual and combined standard infection control interventions (hourly handwashing of ungloved hands [2 log₁₀ virus removal efficiency] (Grove et al., 2015), surgical masking). Vaccination was incorporated into the model representing two doses of mRNA vaccine (Moderna/Pfizer) and was applied with and without the standard infection control interventions. Additional decontamination of plastic packaging [3 log₁₀ virus removal efficiency] (EPA, 2020) was applied in combination with the standard infection control interventions. Ventilation (two air changes per hour [ACH]) was applied to all simulations. An infectious to non-infectious particle ratio of 1:100 (Pitol & Julian, 2021) was applied to all viral shedding concentrations. Reductions in SARS-CoV-2 infection risk (%) to the susceptible worker relative to no interventions are reported below each panel. Panel A represents the impact of standard infection control interventions with and without vaccination on fomite-mediated SARS-CoV-2 risk. For the first vaccination scenario, we assumed only the susceptible worker was vaccinated with two doses of mRNA vaccine (Moderna/Pfizer) and vaccine effectiveness (VE) against susceptibility to infection was simulated across three vaccination states. These included: 1) no vaccination/no prior immunity; 2) lower VE ranging from 64% (Moustsen-Helms et al., 2021) - 80% (Khan & Mahmud, 2021) representative of reduced protection (variants of concern, waning immunity, immunocompromised and elderly or at-risk populations); and 3) optimal VE ranging from 86% (Andrejko et al., 2021; Pawlowski et al., 2021) – 99% (Swift et al., 2021) among healthy adults 14 days or more after second mRNA dose. Panel B: the second vaccine scenario represented vaccine effectiveness against transmission, where all workers are assumed to be vaccinated with two doses of mRNA vaccines and hence the model simulated breakthrough infections. Vaccine effectiveness against transmission (VET) was modeled by applying the combined effect of the reduction in risk of infection to the susceptible worker and the risk of transmissibility given a breakthrough infection among the vaccinated workers. We used the VET estimate (88.5% [95% CI: 82.3%, 94.8%]) derived from Prunas et al. (2021). VET was modeled across a range of three peak infectious viral shedding concentrations representative of possible increased transmissibility and/or infectiousness of variants of concern: 1) 8.1–9.4 log₁₀ viral particles; 2) 7.1–8.4 log₁₀ viral particles; and 3) 6.4–7.7 log₁₀ viral particles. These viral shedding levels represent 100-, 10-, and 2-times, respectively, the increased viral shedding concentration simulated in the base model analysis. Dashed lines represent 1:10,000 (black) and 1:1,000,000 (gray) infection risk targets. Results are presented as the median risk values with 5th and 95th percentile bars.