ABSTRACT
BACKGROUND: Foodborne pathogen transmission during food preparation is a common occurrence, and cross-contamination can be a contributing factor. Behaviors that lead to cross-contamination during meal preparation have not been well characterized. The study objective was to determine how hands and food handling behaviors (with a focus on handwashing and touch-based events) affect the risk of cross-contamination of kitchen surfaces and foods during meal preparation. METHODS: Data from a prior study in which participants were observed preparing turkey burgers inoculated with bacteriophage MS2 and a salad provided the data for analysis. Cross-contamination was assessed using environmental sampling data. Behavioral coding was performed for handwashing and touch-based behaviors. Cross-contamination risk was defined as the likelihood (number of contaminated surfaces) and degree (contaminant concentration) of MS2 on surfaces. Statistical analyses were performed in R, SPSS, and SigmaPlot. RESULTS: The significantly reduced risk of cross-contamination (P.ß<.ß.0001) was observed for participants who attempted handwashing or completed more handwashing steps. Scrubbing hands for 5.ßseconds, on average, reduced the risk of cross-contamination (P.ß<.ß.05). Cross-contamination regression models created using the most significant predictor variables showed that increased handwashing attempts, completion of more handwashing steps, and average scrub times>5.ßseconds all decreased the risk of cross-contamination (P.ß<.ß.05). CONCLUSIONS: This analysis can be used in future risk assessment modeling and for informing education and outreach to reduce pathogen transmission during food preparation.
Subject(s)
Food Handling , Hand , Humans , Hand DisinfectionABSTRACT
Essential food workers experience elevated risks of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection due to prolonged occupational exposures in food production and processing areas, shared transportation (car or bus), and employer-provided shared housing. Our goal was to quantify the daily cumulative risk of SARS-CoV-2 infection for healthy susceptible produce workers and to evaluate the relative reduction in risk attributable to food industry interventions and vaccination. We simulated daily SARS-CoV-2 exposures of indoor and outdoor produce workers through six linked quantitative microbial risk assessment (QMRA) model scenarios. For each scenario, the infectious viral dose emitted by a symptomatic worker was calculated across aerosol, droplet, and fomite-mediated transmission pathways. Standard industry interventions (2-m physical distancing, handwashing, surface disinfection, universal masking, ventilation) were simulated to assess relative risk reductions from baseline risk (no interventions, 1-m distance). Implementation of industry interventions reduced an indoor worker's relative infection risk by 98.0% (0.020; 95% uncertainty interval [UI], 0.005 to 0.104) from baseline risk (1.00; 95% UI, 0.995 to 1.00) and an outdoor worker's relative infection risk by 94.5% (0.027; 95% UI, 0.013 to 0.055) from baseline risk (0.487; 95% UI, 0.257 to 0.825). Integrating these interventions with two-dose mRNA vaccinations (86 to 99% efficacy), representing a worker's protective immunity to infection, reduced the relative infection risk from baseline for indoor workers by 99.9% (0.001; 95% UI, 0.0002 to 0.005) and outdoor workers by 99.6% (0.002; 95% UI, 0.0003 to 0.005). Consistent implementation of combined industry interventions, paired with vaccination, effectively mitigates the elevated risks from occupationally acquired SARS-CoV-2 infection faced by produce workers. IMPORTANCE This is the first study to estimate the daily risk of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection across a variety of indoor and outdoor environmental settings relevant to food workers (e.g., shared transportation [car or bus], enclosed produce processing facility and accompanying breakroom, outdoor produce harvesting field, shared housing facility) through a linked quantitative microbial risk assessment framework. Our model has demonstrated that the elevated daily SARS-CoV-2 infection risk experienced by indoor and outdoor produce workers can be reduced below 1% when vaccinations (optimal vaccine efficacy, 86 to 99%) are implemented with recommended infection control strategies (e.g., handwashing, surface disinfection, universal masking, physical distancing, and increased ventilation). Our novel findings provide scenario-specific infection risk estimates that can be utilized by food industry managers to target high-risk scenarios with effective infection mitigation strategies, which was informed through more realistic and context-driven modeling estimates of the infection risk faced by essential food workers daily. Bundled interventions, particularly if they include vaccination, yield significant reductions (>99%) in daily SARS-CoV-2 infection risk for essential food workers in enclosed and open-air environments.
Subject(s)
COVID-19 , Occupational Exposure , Humans , SARS-CoV-2 , COVID-19/prevention & control , Respiratory Aerosols and Droplets , Occupational Exposure/prevention & control , Infection ControlABSTRACT
ABSTRACT: It is estimated that one in five cases of foodborne illnesses is acquired in the home. However, how pathogens move throughout a kitchen environment when consumers are preparing food is not well characterized. The purpose of this study was to determine the prevalence and degree of cross-contamination across a variety of kitchen surfaces during a consumer meal preparation event. Consumers (n = 371) prepared a meal consisting of turkey patties containing the bacteriophage MS2 as a tracer organism and a ready-to-eat lettuce salad. Half were shown a video on proper thermometer use before the trial. After meal preparation, environmental sampling and detection were performed to assess cross-contamination with MS2. For most surfaces, positivity did not exceed 20%, with the exception of spice containers, for which 48% of the samples showed evidence of MS2 cross-contamination. Spice containers also had the highest MS2 concentrations, at a mean exceeding 6 log viral genome equivalent copies per surface. The high level of MS2 on spice containers drove the significant differences between surfaces, suggesting the significance of spice containers as a vehicle for cross-contamination, despite the absence of previous reports to this effect. The thermometer safety intervention did not affect cross-contamination. The efficiency of MS2 transfer, when expressed as a percentage, was relatively low, ranging from an average of 0.002 to 0.07%. Quantitative risk assessment work using these data would aid in further understanding the significance of cross-contamination frequency and efficiency. Overall, these data will help create more targeted consumer messaging to better influence consumer cross-contamination behaviors.
Subject(s)
Food Handling , Foodborne Diseases , Animals , Turkeys , Lactuca , Food Microbiology , Food Contamination/analysisABSTRACT
Commonly used surface sanitizers often lack activity against human noroviruses (hNoVs). The impact of inactivation versus removal when these products are applied via wiping is poorly characterized. The purpose of this work was to assess the anti-hNoV efficacy of various surface sanitizer chemistries, as applied to a laminate material commonly used for restaurant tabletops, using standard surface assays (ASTM E1053-11) and a newly developed wiping protocol. Four commercially available products with different active ingredient(s) (i.e., ethanol [EtOH], acid + anionic surfactant [AAS], quaternary ammonium compound [QAC], and sodium hypochlorite [NaOCl]) and a water control were evaluated against hNoV GII.4 Sydney, hNoV GI.6, and the cultivable surrogate Tulane virus (TuV). Virus concentration was evaluated using RNase-reverse transcriptase (RT)-quantitative PCR (qPCR) (hNoV) and infectivity assay (TuV). Only the EtOH-based product significantly reduced virus concentration (>3.5 log10 reduction [LR]) by surface assay, with all other products producing ≤0.5 LR. The inclusion of a wiping step enhanced the efficacy of all products, producing complete virus elimination for the EtOH-based product and 1.6 to 3.8 LR for the other chemistries. For hNoVs, no detectable residual virus could be recovered from paper towels used to wipe the EtOH-based product, while high concentrations of virus could be recovered from the used paper towel and the wiped coupon (1.5 to 2.5 log10 lower genome equivalent copies [GEC] compared to control) for the QAC- and AAS-based products and for water. These results illustrate the variability in anti-hNoV activity of representative surface sanitizers and highlights the value of wiping, the efficacy of which appears to be driven by a combination of virus inactivation and removal. IMPORTANCE Human noroviruses (hNoVs) are the leading cause of acute gastroenteritis and food-borne disease worldwide. Noroviruses are difficult to inactivate, being recalcitrant to sanitizers and disinfectants commonly used by the retail food sector. This comparative study demonstrates the variability in anti-hNoV activity of representative surface sanitizers, even those allowed to make label claims based on the cultivable surrogate, feline calicivirus (FCV). It also highlights the importance of wiping in the process of sanitization, which significantly improves product efficacy through the action of physical removal of surface microbes. There is a need for more and better product formulations with demonstrated efficacy against hNoVs, which will likely necessitate the use of alternative cultivable surrogates, such as Tulane virus (TuV). These findings help food safety professionals make informed decisions on sanitizing product selection and application methods in order to reduce the risk of hNoV contamination and transmission in their facilities.
Subject(s)
Calicivirus, Feline , Disinfectants , Gastroenteritis , Norovirus , Animals , Cats , Disinfectants/pharmacology , Ethanol , Humans , Norovirus/genetics , Quaternary Ammonium Compounds , Virus Inactivation , WaterABSTRACT
Human noroviruses (hNoV) are the leading cause of acute non-bacterial gastroenteritis worldwide and contaminated hands play a significant role in the spread of disease. Some hand sanitizers claim to interrupt hNoV transmission, but their antiviral efficacy on human hands is poorly characterized. The purpose of this work was to characterize the efficacy of representative commercial hand sanitizers against hNoV using an in vivo fingerpad method (ASTM E1838-17). Eight products [seven ethanol-based and one benzalkonium chloride (BAK)-based], and a benchmark 60% ethanol solution, were each evaluated on 10 human volunteers using the epidemic GII.4 hNoV strain. Virus titers before and after treatment were evaluated by RT-qPCR preceded by RNase treatment; product efficacy was characterized by log10 reduction (LR) in hNoV genome equivalent copies after treatment. The benchmark treatment produced a 1.7 ± 0.5 LR, compared with Product A (containing 85% ethanol) which produced a 3.3 ± 0.3 LR and was the most efficacious (p < 0.05). Product B (containing 70% ethanol), while less efficacious than Product A (p < 0.05), performed better than the benchmark with a LR of 2.4 ± 0.4. Five of the other ethanol-based products (labeled ethanol concentration ranges of 62-80%) showed similar efficacy to the 60% ethanol benchmark with LR ranging from 1.3 to 2.0 (p > 0.05). Product H (0.1% BAK) was less effective than the benchmark with a LR of 0.3 ± 0.2 (p < 0.05). None of the products screened were able to completely eliminate hNoV (maximum assay resolution 5.0 LR). Product performance was variable and appears driven by overall formulation. There remains a need for more hand sanitizer formulations having greater activity against hNoV, a virus that is comparatively recalcitrant relative to other pathogens of concern in community, healthcare, and food preparation environments.
ABSTRACT
In-home pet food handling and food dish hygiene practices can have adverse health impacts for both humans and pets. Safe food and dish handling guidelines are not easily evidenced for pet owners. The study was designed to investigate dog owners' feeding habits and evaluate the impact of the Food and Drug Association (FDA) hygiene protocols on dog food dish contamination. Procedures and surveys were approved by North Carolina State University Institutional Animal Care and Use Committee and Institutional Review Board. Pet feeding and food dish hygiene data were collected from 417 dog owner surveys and 68 food dish swabs. Total aerobic plate counts (APC) were performed on 68 dishes and randomly assigned into Group A (FDA pet food handling and dish hygiene guidelines), Group B (FDA pet and human food handling and dish hygiene guidelines), or Group C (no guidelines). Hygiene protocols were instituted in-home for 1 week, followed by a second APC and follow-up survey. Survey from dog owners-households indicated: 4.7% were aware of FDA pet food handling and dish hygiene guidelines; 36% have individuals ≤ 13 years old and/or immunocompromised; 43% stored dog food 0-5 feet from human food; 34% washed their hands after feeding; and 33% prepared their dog food on human food preparation surfaces. The hygiene protocols followed by Groups A and B resulted in significant decreases in food dish APC (p<0.001; 1.4; (0.9, 2.0); p<0.05; 0.604 (0.02, 1.2), respectively), as compared to Group C (p≥0.05). Hot water (>160° F or 71.1°C) washing decreased APC (p<0.01; 1.5 (0.4, 2.6)) over cold/lukewarm water. In the follow-up survey, 8% of Group A and B respondents reported likely to adhere to protocols long-term. This study suggests a need for pet food handling and dish hygiene guideline education to minimize bacterial contamination of dishes, especially for high-risk populations.
Subject(s)
Food Handling , Hygiene , Animals , Dogs , Food Contamination/prevention & control , Humans , Pets , Surveys and Questionnaires , WaterABSTRACT
The antinoroviral effect of copper ions is well known, yet most of this work has previously been conducted in copper and copper alloy surfaces, not copper ions in solution. In this work, we characterized the effects that Cu ions have on human norovirus capsids' and surrogates' integrity to explain empirical data, indicating virus inactivation by copper alloy surfaces, and as means of developing novel metal ion-based virucides. Comparatively high concentrations of Cu(II) ions (>10 mM) had little effect on the infectivity of human norovirus surrogates, so we used sodium ascorbate as a reducing agent to generate unstable Cu(I) ions from solutions of copper bromide. We found that significantly lower concentrations of monovalent copper ions (â¼0.1 mM) compared to divalent copper ions cause capsid protein damage that prevents human norovirus capsids from binding to cell receptors in vitro and induce a greater than 4-log reduction in infectivity of Tulane virus, a human norovirus surrogate. Further, these Cu(I) solutions caused reduction of GII.4 norovirus from stool in suspension, producing about a 2-log reduction of virus as measured by a reverse transcriptase-quantitative polymerase chain reaction. Sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) data indicate substantial major capsid protein cleavage of both GI.7 and GII.4 norovirus capsids, and TEM images show the complete loss of capsid integrity of GI.7 norovirus. GII.4 virus-like particles (VLPs) were less susceptible to inactivation by copper ion treatments than GI.7 VLPs based upon receptor binding and SDS-PAGE analysis of viral capsids. The combined data demonstrate that stabilized Cu(I) ion solutions show promise as highly effective noroviral disinfectants in solution that can potentially be utilized at low concentrations for inactivation of human noroviruses.
Subject(s)
Copper , Norovirus , Virus Inactivation , Alloys/pharmacology , Capsid Proteins , Catalysis , Copper/pharmacology , Ions , Norovirus/drug effects , Norovirus/physiologyABSTRACT
AIM: To evaluate the anti-noroviral efficacy of PURELL® surface sanitizer and disinfectant spray (PSS, an alcohol-based formulation) using human norovirus GII.4 Sydney [hNoV, by RT-qPCR and human intestinal enteroid (HIE) infectivity assay] and its cultivable surrogate, Tulane virus (TuV, infectivity assay), compared to sodium hypochlorite (NaOCl) solutions. METHODS AND RESULTS: PSS efficacy was evaluated in suspension and on surfaces [stainless steel (SS)] using ASTM methods. Results were expressed as log10 reduction (LR) of genome equivalent copy number (GEC, for hNoV, assayed by RT-qPCR) and plaque forming units (PFU, for TuV, per infectivity assay). In suspension, PSS achieved a 2.9 ± 0.04 LR hNoV GEC irrespective of contact time (30 or 60 s) and soil load (2.5% or 5%). Under all treatment conditions, infectious TuV could not be recovered following exposure to PSS, corresponding to the assay limit of detection (3.1-5.2 log10 PFU). Infectious hNoV could not be detected in the HIE model after exposure to PSS. On SS and 2.5% soil, PSS produced a 3.1 ± 0.1 LR hNoV GEC, comparable to 500 ppm NaOCl for 60 s. With 5.0% soil, PSS produced a 2.5 ± 0.2 LR hNoV GEC, which was similar to 1000-5000 ppm NaOCl for 60 s. CONCLUSIONS: PSS showed high anti-hNoV efficacy by RT-qPCR and in in vitro (TuV) and ex vivo (HIE) infectivity assays and performed similar to 1000-5000 ppm NaOCl for a 60-s contact time on SS with added soil. SIGNIFICANCE AND IMPACT OF STUDY: hNoV remains a significant cause of morbidity globally, partly due to its resistance to numerous surface disinfectants. RT-qPCR results from this study indicate PSS efficacy against hNoV is comparable to NaOCl efficacy. Infectivity assays leveraging TuV and the HIE model for hNoV support and confirm loss of virus infectivity. Collectively, these results indicate the product's ability to inactivate hNoV quickly, which could be beneficial in settings having elevated risk for hNoV transmission.
Subject(s)
Disinfectants , Norovirus , Disinfectants/pharmacology , Disinfection/methods , Ethanol , Humans , Norovirus/genetics , Sodium Hypochlorite/pharmacology , Soil , Stainless SteelABSTRACT
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.
ABSTRACT
ABSTRACT: This study was conducted to test the effectiveness of a consumer poultry washing educational intervention that included video observation of meal preparation with participants who self-reported washing poultry. Treatment group participants received three e-mail messages containing information that the U.S. Department of Agriculture has used on social media sites (video and infographics) related to poultry preparation, including advising against washing chicken. Participants were observed cooking chicken thighs (inoculated with traceable nonpathogenic Escherichia coli strain DH5α) and preparing a salad to determine whether they washed the chicken and the extent of cross-contamination to the salad and areas of the kitchen. After meal preparation, participants responded to an interview about food handling behaviors, including questions about the intervention for treatment group participants. Three hundred people participated in the study (158 control, 142 treatment). The intervention effectively encouraged participants not to wash chicken before cooking; 93% of treatment group participants but only 39% of control group participants did not wash the chicken (P < 0.0001). The high levels of E. coli DH5α detected in the sink and on the salad lettuce suggest that microbes transferred to the sink from the chicken, packaging, or contaminated hands are a larger cause for concern than is splashing contaminated chicken fluids onto the counter. Among chicken washers, 26 and 30% of the lettuce from the prepared salad was contaminated for the control and treatment groups, respectively. For nonwashers, 31 and 15% of the lettuce was contaminated for the control and treatment groups, respectively. Hand-facilitated cross-contamination is suspected to be a factor in explaining this resulting lettuce cross-contamination. This study demonstrates the need to change the frame of "don't wash your poultry" messaging to instead focus on preventing contamination of sinks and continuing to emphasize the importance of hand washing and cleaning and sanitizing surfaces.
Subject(s)
Escherichia coli , Poultry , Animals , Food Contamination/analysis , Food Contamination/prevention & control , Food Handling/methods , Food Microbiology , Food Safety , Hand , HumansABSTRACT
The SARS-CoV-2 global pandemic poses significant health risks to workers who are essential to maintaining the food supply chain. Using a quantitative risk assessment model, this study characterized the impact of risk reduction strategies for controlling SARS-CoV-2 transmission (droplet, aerosol, fomite-mediated) among front-line workers in a representative indoor fresh fruit and vegetable manufacturing facility. We simulated: 1) individual and cumulative SARS-CoV-2 infection risks from close contact (droplet and aerosols at 1-3 m), aerosol, and fomite-mediated exposures to a susceptible worker following exposure to an infected worker during an 8 h-shift; and 2) the relative reduction in SARS-CoV-2 infection risk attributed to infection control interventions (physical distancing, mask use, ventilation, surface disinfection, hand hygiene, vaccination). Without mitigation measures, the SARS-CoV-2 infection risk was largest for close contact (droplet and aerosol) at 1 m (0.96, 5th - 95th percentile: 0.67-1.0). In comparison, risk associated with fomite (0.26, 5th - 95th percentile: 0.10-0.56) or aerosol exposure alone (0.05, 5th - 95th percentile: 0.01-0.13) at 1 m distance was substantially lower (73-95%). At 1 m, droplet transmission predominated over aerosol and fomite-mediated transmission, however, this changed by 3 m, with aerosols comprising the majority of the exposure dose. Increasing physical distancing reduced risk by 84% (1-2 m) and 91% (1-3 m). Universal mask use reduced infection risk by 52-88%, depending on mask type. Increasing ventilation (from 0.1 to 2-8 air changes/hour) resulted in risk reductions of 14-54% (1 m) and 55-85% (2 m). Combining these strategies, together with handwashing and surface disinfection, resulted in <1% infection risk. Partial or full vaccination of the susceptible worker resulted in risk reductions of 73-92% (1 m risk range: 0.08-0.26). However, vaccination paired with other interventions (ACH 2, mask use, or distancing) was necessary to achieve infection risks <1%. Current industry SARS-CoV-2 risk reduction strategies, particularly when bundled, provide significant protection to essential food workers.
ABSTRACT
Human norovirus is the leading cause of foodborne illness globally. One of the challenges in detecting noroviruses is the identification of a completely broadly reactive ligand; however, all detection ligands generated to date target the viral capsid, the outermost of which is the most variable region of the genome. The VPg is a protein covalently linked to the viral genome that is necessary for replication but hitherto remains underexplored as a target for detection or therapeutics. The purpose of this work was to generate nucleic acid aptamers against human norovirus (Norwalk) and cultivable surrogate (Tulane) VPgs for future use in detection and therapeutics. Eight rounds of positive-SELEX and two rounds of counter-SELEX were performed. Five and eight unique aptamer sequences were identified for Norwalk and Tulane VPg, respectively, all of which were predicted to be stable (∆G < -5.0) and one of which occurred in both pools. All candidates displayed binding to both Tulane and Norwalk VPg (positive:negative > 5.0), and all but two of the candidates displayed very strong binding (positive:negative > 10.0), significantly higher than binding to the negative control protein (p < 0.05). Overall, this work reports a number of aptamer candidates found to be broadly reactive and specific for in vitro-expressed VPgs across genus that could be used for future application in detection or therapeutics. Future work characterizing binding of the aptamer candidates against native VPgs and in therapeutic applications is needed to further evaluate their application.
Subject(s)
Aptamers, Nucleotide/genetics , Caliciviridae/genetics , Genome, Viral , Nucleic Acids/genetics , SELEX Aptamer Technique/methods , Viral Proteins/genetics , DNA, Single-Stranded/genetics , DNA, Single-Stranded/metabolism , Humans , Nucleic Acids/metabolism , Viral Proteins/metabolismABSTRACT
In the agricultural setting, core global food safety elements, such as hand hygiene and worker furlough, should reduce the risk of norovirus contamination on fresh produce. However, the effect of these practices has not been characterized. Using a quantitative microbial risk model, we evaluated the individual and combined effect of farm-based hand hygiene and worker furlough practices on the maximum risk of norovirus infection from three produce commodities (open leaf lettuce, vine tomatoes, and raspberries). Specifically, we tested two scenarios where a harvester's and packer's norovirus infection status was: 1) assumed positive; or 2) assigned based on community norovirus prevalence estimates. In the first scenario with a norovirus-positive harvester and packer, none of the individual interventions modeled reduced produce contamination to below the norovirus infectious dose. However, combined interventions, particularly high handwashing compliance (100%) and efficacy (6 log10 virus removal achieved using soap and water for 30 s), reduced produce contamination to <1-82 residual virus. Translating produce contamination to maximum consumer infection risk, 100% handwashing with a 5 log10 virus removal was necessary to achieve an infection risk below the threshold of 0.032 infections per consumption event. When community-based norovirus prevalence estimates were applied to the harvester and packer, the single interventions of 100% handwashing with 3 log10 virus removal (average 0.02 infection risk per consumption event) or furlough of the packer (average 0.03 infection risk per consumption event) reduced maximum infection risk to below the 0.032 threshold for all commodities. Bundled interventions (worker furlough, 100% glove compliance, and 100% handwashing with 1-log10 virus reduction) resulted in a maximum risk of 0.02 per consumption event across all commodities. These results advance the evidence-base for global produce safety standards as effective norovirus contamination and risk mitigation strategies.
Subject(s)
Caliciviridae Infections , Norovirus , Rubus , Caliciviridae Infections/prevention & control , Food Contamination/analysis , Food Contamination/prevention & control , Hand Disinfection , Humans , LactucaABSTRACT
BACKGROUND: Countries continue to debate the need for decontamination of cold-chain food packaging to reduce possible SARS-CoV-2 fomite transmission among 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. METHODS: Using a quantitative risk assessment model, we simulated in a frozen food packaging facility 1) SARS-CoV-2 fomite-mediated infection risks following worker exposure to contaminated plastic packaging; and 2) reductions in these risks attributed to masking, handwashing, and vaccination. FINDINGS: In a representative facility with no specific interventions, SARS-CoV-2 infection risk to a susceptible worker from contact with contaminated packaging was 2·8 × 10 -3 per 1h-period (95%CI: 6·9 × 10 -6 , 2·4 × 10 -2 ). Implementation of standard infection control measures, handwashing and masks (9·4 × 10 -6 risk per 1h-period, 95%CI: 2·3 × 10 -8 , 8·1 × 10 -5 ), substantially reduced risk (99·7%). Vaccination of the susceptible worker (two doses Pfizer/Moderna, vaccine effectiveness: 86-99%) combined with handwashing and masking reduced risk to less than 1·0 × 10 -6 . Simulating increased infectiousness/transmissibility of new variants (2-, 10-fold viral shedding) among a fully vaccinated workforce, handwashing and masks continued to mitigate risk (2·0 × 10 -6 -1·1 × 10 -5 risk per 1h-period). Decontamination of packaging in addition to these interventions reduced infection risks to below the 1·0 × 10 -6 risk threshold. INTERPRETATION: Fomite-mediated SARS-CoV-2 infection risks were very low under cold-chain conditions. Handwashing and masking provide significant protection to workers, especially when paired with vaccination. FUNDING: U.S. Department of Agriculture.
ABSTRACT
The SARS-CoV-2 global pandemic poses significant health risks to workers who are essential to maintaining the food supply chain. Using a quantitative risk assessment model, this study characterized the impact of risk reduction strategies for controlling SARS-CoV-2 transmission (droplet, aerosol, fomite-mediated) among front-line workers in a representative enclosed food manufacturing facility. We simulated: 1) individual and cumulative SARS-CoV-2 infection risks from close contact (droplet and aerosols at 1-3m), aerosol, and fomite-mediated exposures to a susceptible worker following exposure to an infected worker during an 8h-shift; and 2) the relative reduction in SARS-CoV-2 infection risk attributed to infection control interventions (physical distancing, mask use, ventilation, surface disinfection, hand hygiene). Without mitigation measures, the SARS-CoV-2 infection risk was largest for close contact (droplet and aerosol) at 1m (0.96, 95%CI: 0.67-1.0). In comparison, risk associated with fomite (0.26, 95%CI: 0.10-0.56) or aerosol exposure alone (0.05, 95%CI: 0.01-0.13) at 1m distance was substantially lower (73-95%). At 1m, droplet transmission predominated over aerosol and fomite-mediated transmission, however, this changed by 3m, with aerosols comprising the majority of the exposure dose. Increasing physical distancing reduced risk by 84% (1 to 2m) and 91% (1 to 3m). Universal mask use reduced infection risk by 52-88%, depending on mask type. Increasing ventilation (from 0.1 to 2-8 air changes/hour) resulted in risk reductions of 14-54% (1m) and 55-85% (2m). Combining these strategies, together with handwashing and surface disinfection, resulted in <1% infection risk. Current industry SARS-CoV-2 risk reduction strategies, particularly when bundled, provide significant protection to essential food workers. SIGNIFICANCE STATEMENT: Using mathematical modeling, we find that workers in enclosed food manufacturing facilities are at higher risk of SARS-CoV-2 infection from close contact transmission (exposure to large droplets and small aerosol particles) than fomite transmission. Thus, strategies protecting workers should prioritize close contact transmission pathways, such as physical distancing, universal mask use, and room air changes, with surface disinfection (reducing fomite transmission) and handwashing of secondary importance. Our work supports current international (EU-OSHA), domestic (FDA, OSHA), and food industry-standard guidance for managing COVID-19 transmission in essential workers in the food manufacturing sector. Although our model was designed for an indoor food manufacturing setting, it can be readily adapted to other indoor environments and infectious respiratory pathogens.
ABSTRACT
Cantaloupes contaminated with pathogens have led to many high-profile outbreaks and illnesses. Since bacterial virulence genes (VGs) can act in tandem with antibiotic-resistance and mobile genetic elements, there is a need to evaluate these gene reservoirs in fresh produce, such as cantaloupes. The goal of this study was to assess the distribution of antibiotic-resistance, virulence, and mobile genetic elements genes (MGEGs) in cantaloupe farm environments. A total of 200 samples from cantaloupe melons (n = 99), farm workers' hands (n = 66), and production water (n = 35) were collected in México. Each sample was assayed for the presence of 14 antibiotic-resistance genes, 15 VGs, and 5 MGEGs by polymerase chain reaction. Our results indicated that tetracycline (tetA and tetB) (18% of cantaloupe, 45% of hand samples) and sulfonamide (sul1) (30% of cantaloupe, 71% of hand samples) resistance genes were frequently detected. The colistin resistance gene (mcr1) was detected in 10% of cantaloupe and 23% of farm workers' hands. Among VGs, Salmonella genes invA and spiA were the most abundant. There was a significantly higher likelihood of detecting antibiotic-resistance, virulence, and MGEGs on hands compared with water samples. These results demonstrate a diverse pool of antibiotic-resistance and VGs in cantaloupe production.
Subject(s)
Drug Resistance, Microbial , Farms , Food Contamination/analysis , Salmonella/isolation & purification , Anti-Bacterial Agents/pharmacology , Cucumis melo/microbiology , Drug Resistance, Bacterial , Environmental Microbiology , Food Handling/methods , Food Microbiology , Mexico , Microbial Sensitivity Tests , Salmonella/genetics , Salmonella/pathogenicity , VirulenceABSTRACT
Human norovirus (NoV) is the leading cause of acute viral gastroenteritis and a major source of foodborne illness. Detection of NoV in food and environmental samples is typically performed using molecular techniques, including real-time reverse transcription polymerase chain reaction (RT-PCR) and less frequently, nested real-time PCR. In this study, we conducted a controlled comparison of two published NoV detection assays: a broadly reactive one-step real-time RT-PCR and a two-step nested real-time PCR assay. A 20% human fecal suspension containing a genogroup II human NoV was serially diluted, genome extracted, and subjected to amplification using the two assays compared via PCR Units. Additional amplicon confirmation was performed by dot blot hybridization using digoxigenin (DIG)-labeled oligonucleotide probes. Both assays displayed similar amplification standard curves/amplification efficiencies; however, the nested assay consistently detected one log10 lower virus. Dot blot hybridization improved the detection limit of the nested real-time PCR by one log10 NoV genome copies but impaired the detection limit of the one-step real-time RT-PCR by one log10 NoV genome copies. These results illustrate the complexities in designing and interpreting molecular techniques having a sufficient detection limit to detect low levels of viruses that might be anticipated in contaminated food and environmental samples.
Subject(s)
Caliciviridae Infections/genetics , Feces/virology , Norovirus/genetics , RNA, Viral/genetics , Real-Time Polymerase Chain Reaction , Reverse Transcriptase Polymerase Chain Reaction , Caliciviridae Infections/diagnosis , Caliciviridae Infections/metabolism , Female , Genome, Viral , Humans , Male , RNA, Viral/metabolismABSTRACT
BACKGROUND: Sodium intake in the USA exceeds recommendations. The replacement of added sodium chloride (NaCl) with potassium chloride (KCl) provides a potential strategy to reduce sodium intake. OBJECTIVE: The purpose of this study was to quantitatively estimate changes in intakes of sodium and potassium by the US population assuming use of potassium-based NaCl replacers in top dietary sodium sources. METHODS: Data collected in the What We Eat in America (WWEIA) component of the 2015-2016 and 2009-2010 NHANES were used to identify top-ranking sources of dietary sodium among the population aged 2 y and older based on contributions from food categories aligning with the FDA draft guidance for voluntary sodium reduction. Predicted nutrient intakes were estimated in models assuming total and feasible and practical (F&P) replacement of added NaCl with KCl in foods and ingredients within the top food sources of sodium. An expert elicitation was conducted to collect information on the F&P KCl replacement of added NaCl. RESULTS: Using 2015-2016 consumption data, the total replacement of added NaCl with KCl in the 18 top-ranking sources of dietary sodium results in a predicted sodium intake of 2004 mg/d from the replacement of 1406 mg/d sodium with 1870 mg/d potassium as KCl. Modeled F&P replacement predicted sodium intakes of 3117 mg/d (range of 2953 to 3255 mg/d) from the replacement of 294 mg/d sodium (155 to 457 mg/d) with 390 mg/d potassium (206 to 608 mg/d). Similar results are seen with 2009-2010 data. CONCLUSIONS: The F&P replacement of NaCl with KCl in top-ranking sources of dietary sodium modeled in this study can result in decreased sodium to a level consistent with the short-term intake goal targeted by the FDA of 3000 mg/d, with the mean potassium intake remaining in the range recommended for the apparently healthy population.
Subject(s)
Models, Biological , Nutrition Surveys , Potassium Chloride/administration & dosage , Potassium, Dietary/administration & dosage , Sodium, Dietary/administration & dosage , Cross-Sectional Studies , Food , Humans , United StatesABSTRACT
Cantaloupe melons, which have been responsible of an increasing number of foodborne disease outbreaks, may become contaminated with microbial pathogens during production. However, little information is available on the microbial populations in the cantaloupe farm environment. The purpose of this work was to characterize the bacterial communities present on cantaloupe farms. Fruit, soil, and harvester hand rinsates were collected from two Mexican cantaloupe farms, each visited three times. Microbiome analysis was performed by sequencing 16sRNA and analyzed using qiime2 software. Correlations were determined between sample type and microbial populations. The α and ß diversity analysis identified 2777 sequences across all samples. The soil samples had the highest number and diversity of unique species (from 130 to 1329 OTUs); cantaloupe (from 112 to 205 OTUs), and hands (from 67 to 151 OTUs) had similar diversity. Collectively, Proteobacteria was the most abundant phyla (from 42 to 95%), followed by Firmicutes (1-47%), Actinobacteria (< 1 to 23%), and Bacteroidetes (< 1 to 4.8%). The most abundant genera were Acinetobacter (20-58%), Pseudomonas (14.5%), Erwinia (13%), and Exiguobacterium (6.3%). Genera with potential to be pathogenic included Bacillus (4%), Salmonella (0.85%), Escherichia-Shigella (0.38%), Staphylococcus (0.32%), Listeria (0.29%), Clostridium (0.28%), and Cronobacter (0.27%), which were found at lower frequencies. This study provides information on the cantaloupe production microbiome, which can inform future research into critical food safety issues such as antimicrobial resistance, virulence, and genomic epidemiology.