@article{escudero-abarca_goulter_manuel_leslie_green_arbogast_jaykus_2022, title={Comparative Assessment of the Efficacy of Commercial Hand Sanitizers Against Human Norovirus Evaluated by an in vivo Fingerpad Method}, volume={13}, ISSN={["1664-302X"]}, DOI={10.3389/fmicb.2022.869087}, abstractNote={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 log 10 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.}, journal={FRONTIERS IN MICROBIOLOGY}, author={Escudero-Abarca, Blanca I. and Goulter, Rebecca M. and Manuel, Clyde S. and Leslie, Rachel A. and Green, Kristen and Arbogast, James W. and Jaykus, Lee-Ann}, year={2022}, month={Apr} } @article{kirchner_everhart_doring_smits_faircloth_duong_goulter_goodson_shelley_shumaker_et al._2022, title={Cross-Contamination to Surfaces in Consumer Kitchens with MS2 as a Tracer Organism in Ground Turkey Patties}, volume={85}, ISSN={["1944-9097"]}, DOI={10.4315/JFP-22-060}, abstractNote={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.HIGHLIGHTSForty-eight percent of spice containers sampled showed evidence of MS2 cross-contamination.Spice containers had the highest MS2 concentrations across kitchen surfaces.Spice containers may be a key vehicle for cross-contamination.The thermometer safety intervention did not affect cross-contamination.The efficiency of MS2 transfer was relatively low, ranging from 0.002 to 0.07%.}, number={11}, journal={JOURNAL OF FOOD PROTECTION}, author={Kirchner, Margaret and Everhart, Savana and Doring, Lindsey and Smits, Caitlin and Faircloth, Jeremy and Duong, Minh and Goulter, Rebecca M. and Goodson, Lydia and Shelley, Lisa and Shumaker, Ellen Thomas and et al.}, year={2022}, month={Nov}, pages={1594–1603} } @article{escudero-abarca_goulter_bradshaw_faircloth_leslie_manuel_arbogast_jaykus_2022, title={Efficacy of an alcohol-based surface disinfectant formulation against human norovirus}, ISSN={["1365-2672"]}, DOI={10.1111/jam.15479}, abstractNote={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.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.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.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.}, journal={JOURNAL OF APPLIED MICROBIOLOGY}, author={Escudero-Abarca, Blanca I and Goulter, Rebecca M. and Bradshaw, Justin and Faircloth, Jeremy and Leslie, Rachel A. and Manuel, Clyde S. and Arbogast, James W. and Jaykus, Lee-Ann}, year={2022}, month={Feb} } @article{shumaker_kirchner_cates_shelley_goulter_goodson_bernstein_lavallee_jaykus_chapman_2022, title={Observational Study of the Impact of a Food Safety Intervention on Consumer Poultry Washing}, volume={85}, ISSN={["1944-9097"]}, DOI={10.4315/JFP-21-397}, abstractNote={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.}, number={4}, journal={JOURNAL OF FOOD PROTECTION}, author={Shumaker, Ellen Thomas and Kirchner, Margaret and Cates, Sheryl C. and Shelley, Lisa and Goulter, Rebecca and Goodson, Lydia and Bernstein, Christopher and Lavallee, Aaron and Jaykus, Lee-Ann and Chapman, Benjamin}, year={2022}, month={Apr}, pages={615–625} } @article{faircloth_goulter_manuel_arbogast_escudero-abarca_jaykus_2022, title={The Efficacy of Commercial Surface Sanitizers against Norovirus on Formica Surfaces with and without Inclusion of a Wiping Step}, ISSN={["1098-5336"]}, DOI={10.1128/aem.00807-22}, abstractNote={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.}, journal={APPLIED AND ENVIRONMENTAL MICROBIOLOGY}, author={Faircloth, Jeremy and Goulter, Rebecca M. and Manuel, Clyde S. and Arbogast, James W. and Escudero-Abarca, Blanca and Jaykus, Lee-Ann}, year={2022}, month={Aug} } @misc{kirchner_goulter_chapman_clayton_jaykus_2021, title={Cross-Contamination on Atypical Surfaces and Venues in Food Service Environments}, volume={84}, ISSN={["1944-9097"]}, DOI={10.4315/JFP-20-314}, abstractNote={Cross-contamination of raw food to other surfaces, hands, and foods is a serious issue in food service. With individuals eating more meals away from home, contracting a foodborne illness from a food service establishment is an increasing concern. However, most studies have concentrated on hands or food contact surfaces and neglected atypical and unusual surfaces (surfaces that are not typically identified as a source of cross-contamination) and venues. This review was conducted to identify atypically cross-contaminated surfaces and atypical venues where cross-contamination could occur that have not been examined thoroughly in the literature. Most surfaces that could be at risk for cross-contamination are frequently touched, are rarely cleaned and sanitized, and can support the persistence and/or growth of foodborne pathogens. These surfaces include menus, spice and condiment containers, aprons and coveralls, mobile devices and tablets, and money. Venues that are explored, such as temporary events, mobile vendors, and markets, are usually limited in space or infrastructure, have low compliance with proper hand washing, and provide the opportunity for raw and ready-to-eat foods to come into contact with one another. These factors create an environment in which cross-contamination can occur and potentially impact food safety. A more comprehensive cleaning and sanitizing regime encompassing these surfaces and venues could help mitigate cross-contamination. This review highlights key surfaces and venues that have the potential to be cross-contaminated and have been underestimated or not fully investigated. These knowledge gaps indicate where further work is needed to fully understand the role of these surfaces and venues in cross-contamination and how it can be prevented.}, number={8}, journal={JOURNAL OF FOOD PROTECTION}, author={Kirchner, Margaret and Goulter, Rebecca M. and Chapman, Benjamin J. and Clayton, James and Jaykus, Lee-Ann}, year={2021}, month={Jul}, pages={1239–1251} } @article{duong_shumaker_cates_shelley_goodson_bernstein_lavallee_kirchner_goulter_jaykus_et al._2020, title={An Observational Study of Thermometer Use by Consumers When Preparing Ground Turkey Patties}, volume={83}, ISBN={1944-9097}, DOI={10.4315/JFP-19-594}, abstractNote={The purpose of this study was to test the effectiveness of an intervention for consumer thermometer use by using a randomized experimental design and direct observation of meal preparation. The study was conducted in test kitchen facilities in two locations in North Carolina (one urban and one rural). Cameras recorded participants' actions at various locations throughout the kitchen and recorded the meal preparation from beginning to end. Before preparing the meal, a randomized treatment group watched a 3-min U.S. Department of Agriculture (USDA) food safety video “The Importance of Cooking to a Safe Internal Temperature and How to Use a Food Thermometer.” Participants in the control and treatment groups were observed while cooking turkey burgers and preparing a salad to determine whether a thermometer was used to check the doneness of the turkey patties. Following meal preparation, all participants responded to a postobservation interview about food handling behaviors. Treatment group participants were also asked about the intervention. A total of 383 people participated in the study (201 in the control group and 182 in the treatment group). Participants who viewed the video were twice as likely to use a thermometer to check the doneness of the turkey patties compared with the participants who were not exposed to the video (75 versus 34%) and twice as likely to place the thermometer in the correct location (52 versus 23%). Sixty-seven percent of participants who watched the video reported that it influenced their behavior in the kitchen. This study demonstrates the importance of timing and framing of a behavioral intervention for thermometer use and highlights considerations for the development of additional messages (e.g., proper insertion). Participants who viewed a food safety video were twice as likely to use a thermometer. Participants who viewed the video were more likely to place thermometer correctly. Most (67%) of the participants who watched the video said it influenced their behavior.}, number={7}, journal={JOURNAL OF FOOD PROTECTION}, author={Duong, Minh and Shumaker, Ellen Thomas and Cates, Sheryl C. and Shelley, Lisa and Goodson, Lydia and Bernstein, Christopher and Lavallee, Aaron and Kirchner, Margaret and Goulter, Rebecca and Jaykus, Lee-Ann and et al.}, year={2020}, month={Jul}, pages={1167–1174} } @article{escudero-abarca_goulter_arbogast_leslie_green_jaykus_2020, title={Efficacy of alcohol-based hand sanitizers against human norovirus using RNase-RT-qPCR with validation by human intestinal enteroid replication}, volume={71}, ISSN={["1472-765X"]}, DOI={10.1111/lam.13393}, abstractNote={Successful human norovirus (HuNoV) cultivation in stem cell-derived human intestinal enteroids (HIE) was recently reported. The purpose of this study was to evaluate the anti-HuNoV efficacy of two alcohol-based commercial hand sanitizers and 60% ethanol by suspension assay using RNase-RT-qPCR, with subsequent validation of efficacy by HuNoV cultivation using the HIE model. In suspension, when evaluated by RNase-RT-qPCR, 60% ethanol resulted in less than one log10 reduction in HuNoV genome equivalent copies (GEC) regardless of contact time (30 or 60s) or soil load. The two commercial products outperformed 60% ethanol regardless of contact time or soil load, providing 2·2-3·2 log10 HuNoV GEC reductions by suspension assay. Product B could not be validated in the HIE model due to cytotoxicity. Following a 60s exposure, viral replication in the HIE model increased 1·9 ± 0·2 log10 HuNoV GEC for the neutralization (positive) control and increased 0·9 ± 0·2 log10 HuNoV GEC in challenged HIE after treatment with 60% ethanol. No HuNoV replication in HIE was observed after a 60 s exposure to Product A.}, number={6}, journal={LETTERS IN APPLIED MICROBIOLOGY}, author={Escudero-Abarca, B. I. and Goulter, R. M. and Arbogast, J. W. and Leslie, R. A. and Green, K. and Jaykus, L. -A.}, year={2020}, month={Dec}, pages={605–610} } @article{almand_goulter_jaykus_2016, title={Capture and concentration of viral and bacterial foodborne pathogens using apolipoprotein H}, volume={128}, ISSN={["1872-8359"]}, DOI={10.1016/j.mimet.2016.07.014}, abstractNote={The need for improved pathogen separation and concentration methods to reduce time-to-detection for foodborne pathogens is well recognized. Apolipoprotein H (ApoH) is an acute phase human plasma protein that has been previously shown to interact with viruses, lipopolysaccharides (LPS) and bacterial proteins. The purpose of this study was to determine if ApoH was capable of binding and efficiently capturing two representative human norovirus strains (GI.1 and GII.4), a cultivable surrogate, and four bacterial pathogens (Escherichia coli O157:H7, Listeria monocytogenes, Salmonella enterica serovar Enteritidis, and Staphylococcus aureus). Experiments were carried out using an ApoH-conjugated magnetic bead-based capture followed by pathogen detection using nucleic acid amplification. For all three viruses studied, > 10% capture efficiency (< 1 Log10 loss in RT-qPCR amplifiable units) was observed. The same capture efficiencies were observed for the bacterial pathogens tested, with the exception of E. coli O157:H7 (approximately 1% capture efficiency, or 2 Log10 loss in CFU equivalents). The efficiency of the capture steps did not vary as a consequence of input target concentration or in the presence of an abundance of background microflora. A complementary plate-based capture assay showed that ApoH bound to a variety of human norovirus virus-like particles. ApoH has the potential to be a broadly reactive ligand for separating and concentrating representative foodborne pathogens, both bacteria and viruses.}, journal={JOURNAL OF MICROBIOLOGICAL METHODS}, author={Almand, Erin A. and Goulter, Rebecca M. and Jaykus, Lee-Ann}, year={2016}, month={Sep}, pages={88–95} } @article{moore_goulter_jaykus_2015, title={Human Norovirus as a Foodborne Pathogen: Challenges and Developments}, volume={6}, ISSN={["1941-1413"]}, DOI={10.1146/annurev-food-022814-015643}, abstractNote={Human noroviruses (NoVs) are the leading cause of foodborne illness in the United States, and they exact a considerable human and economic burden worldwide. In fact, the many challenging aspects of human NoV have caused some to call it the nearly perfect foodborne pathogen. In this review, a brief overview of NoVs and their genetic structure is provided. Additionally, the challenges and recent developments related to human NoVs regarding viral evolution, transmission, epidemiology, outbreak identification, cultivation, animal and human models, and detection are presented.}, journal={ANNUAL REVIEW OF FOOD SCIENCE AND TECHNOLOGY, VOL 6}, author={Moore, Matthew D. and Goulter, Rebecca M. and Jaykus, Lee-Ann}, year={2015}, pages={411–433} } @article{goulter_taran_gentle_gobius_dykes_2014, title={Escherichia coli strains expressing H12 antigens demonstrate an increased ability to attach to abiotic surfaces as compared with E-coli strains expressing H7 antigens}, volume={119}, ISSN={["1873-4367"]}, DOI={10.1016/j.colsurfb.2014.04.003}, abstractNote={The role of Escherichia coli H antigens in hydrophobicity and attachment to glass, Teflon and stainless steel (SS) surfaces was investigated through construction of fliC knockout mutants in E. coli O157:H7, O1:H7 and O157:H12. Loss of FliCH12 in E. coli O157:H12 decreased attachment to glass, Teflon and stainless steel surfaces (p < 0.05). Complementing E. coli O157:H12 ΔfliCH12 with cloned wildtype (wt) fliCH12 restored attachment to wt levels. The loss of FliCH7 in E. coli O157:H7 and O1:H7 did not always alter attachment (p > 0.05), but complementation with cloned fliCH12, as opposed to cloned fliCH7, significantly increased attachment for both strains compared with wt counterparts (p < 0.05). Hydrophobicity determined using bacterial adherence to hydrocarbons and contact angle measurements differed with fliC expression but was not correlated to the attachment to materials included in this study. Purified FliC was used to functionalise silicone nitride atomic force microscopy probes, which were used to measure adhesion forces between FliC and substrates. Although no significant difference in adhesion force was observed between FliCH12 and FliCH7 probes, differences in force curves suggest different mechanism of attachment for FliCH12 compared with FliCH7. These results indicate that E. coli strains expressing flagellar H12 antigens have an increased ability to attach to certain abiotic surfaces compared with E. coli strains expressing H7 antigens.}, journal={COLLOIDS AND SURFACES B-BIOINTERFACES}, author={Goulter, Rebecca M. and Taran, Elena and Gentle, Ian R. and Gobius, Kari S. and Dykes, Gary A.}, year={2014}, month={Jul}, pages={90–98} } @article{escudero-abarca_rawsthorne_goulter_suh_jaykus_2014, title={Molecular methods used to estimate thermal inactivation of a prototype human norovirus: More heat resistant than previously believed?}, volume={41}, ISSN={["1095-9998"]}, DOI={10.1016/j.fm.2014.01.009}, abstractNote={Two molecular-based methods for estimating capsid integrity as a proxy for virus infectivity were used to produce thermal inactivation profiles of Snow Mountain virus (SMV), a prototype human norovirus (HuNoV). Monodispersed virus suspensions were exposed to 77, 80, 82 and 85 °C for various times, pre-treated with either propidium monoazide (PMA) or RNase, and subjected to RNA isolation followed by RT-qPCR amplification. D-values were 25.6 ± 2.8, 3.1 ± 0.1, 0.7 ± 0.04 and 0.2 ± 0.07 min at 77, 80, 82 and 85 °C, respectively for PMA-treated SMV; and 16.4 ± 0.4, 3.9 ± 0.2 0.9 ± 0.3 and 0.12 ± 0.00 min at 77, 80, 82 and 85 °C, respectively for RNase-treated SMV. Corresponding zD values were 3.80 °C and 3.71 °C for PMA and RNase-treated virus, respectively. Electron microscopy data applied to heat-treated virus-like particles supported this relatively high degree of thermal resistance. The data suggest that SMV is more heat resistant than common cultivable HuNoV surrogates. Standardized thermal inactivation methods (such as milk pasteurization) may not be stringent enough to eliminate this virus and perhaps other HuNoV.}, journal={FOOD MICROBIOLOGY}, author={Escudero-Abarca, B. I. and Rawsthorne, H. and Goulter, R. M. and Suh, S. H. and Jaykus, L. A.}, year={2014}, month={Aug}, pages={91–95} } @article{liu_escudero_jaykus_montes_goulter_lichtenstein_fernandez_lee_de nardo_kirby_et al._2013, title={Laboratory Evidence of Norwalk Virus Contamination on the Hands of Infected Individuals}, volume={79}, ISSN={["1098-5336"]}, DOI={10.1128/aem.02576-13}, abstractNote={ABSTRACT Human norovirus (NoV) outbreak investigations suggest that the hands of infected individuals play an important role in NoV transmission. However, there is no experimental evidence documenting the likelihood and degree of NoV contamination on hands. As part of a clinical trial designed to evaluate the efficacy of high-pressure processing for Norwalk virus (NV) inactivation in oysters, 159 hand rinse samples were collected from 6 infected and 6 uninfected subjects. NV was concentrated from the samples by polyethylene glycol precipitation, followed by RNA extraction using an automated guanidinium isothiocyanate-silica method. NV RNA was detected and quantified using multiple NV-specific reverse transcription-quantitative PCR (RT-qPCR) assays. A total of 25.4% (18/71) of the hand rinse samples collected from 6 infected volunteers were presumptively positive for NV, with an average of 3.86 log 10 genomic equivalent copies (GEC) per hand. Dot blot hybridization of PCR products obtained using a different primer set, and DNA sequencing of selected amplicons, provided further confirmation of the presence of NV in the hand rinses. NV contamination was also detected in two hand rinse samples obtained from one uninfected subject. These findings provide definitive evidence of NV contamination on the hands of infected subjects observed under controlled clinical research conditions. Such data support the need for better hand hygiene strategies to prevent NoV transmission.}, number={24}, journal={APPLIED AND ENVIRONMENTAL MICROBIOLOGY}, author={Liu, Pengbo and Escudero, Blanca and Jaykus, Lee-Ann and Montes, Julia and Goulter, Rebecca M. and Lichtenstein, Meredith and Fernandez, Marina and Lee, Joong-Chul and De Nardo, Elizabeth and Kirby, Amy and et al.}, year={2013}, month={Dec}, pages={7875–7881} }