Source: NORTH CAROLINA STATE UNIV submitted to
BUILDING CAPACITY TO CONTROL VIRAL FOODBORNE DISEASE: A TRANSLATIONAL, MULTIDISCIPLINARY APPROACH
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
EXTENDED
Funding Source
Reporting Frequency
Annual
Accession No.
0225445
Grant No.
2011-68003-30395
Project No.
NC09805
Proposal No.
2015-08928
Multistate No.
(N/A)
Program Code
A4121
Project Start Date
Jun 1, 2011
Project End Date
May 31, 2018
Grant Year
2015
Project Director
Jaykus, L.
Recipient Organization
NORTH CAROLINA STATE UNIV
(N/A)
RALEIGH,NC 27695
Performing Department
Food, Bioprocessing, and Nutrition Sciences.
Non Technical Summary
Human noroviruses (HuNoV) are the leading cause of food borne disease (FBD), responsible for over 5 million cases in the U.S. annually. The major foods at-risk for contamination are molluscan shellfish, fresh produce, and foods that are extensively handled just prior to consumption. The most common means by which foods become contaminated with HuNoV is by direct contact with fecal matter on the hands of food workers who have not practiced adequate personal hygiene. This makes sense as HuNoV are shed in high numbers in the feces and vomit of infected individuals and they cause disease at very low doses. Individuals can shed virus in their fecal material before showing symptoms and/or long after they have recovered. Furthermore, HuNoV can persist for days to weeks in the environment; the vast majority of commercial hand and surface sanitizers are ineffective against these viruses; and they are resistant to many food processes. Despite their importance, most public health professionals, the food industry, and consumers continue to believe that bacteria, not viruses, are the most common cause of FBD. This is in large part because HuNoV are difficult to study: they cannot be cultivated outside of the human body, there are no commercial diagnostic tests available in the U.S., and only a few scientists are trained specifically in food virology. The purpose of this project is raise awareness of the importance of viruses, particularly HuNoV, to FBD; to increase our capacity to study these agents; and to use advanced tools to design targeted control measures. The USDA-NIFA Food Virology Collaborative will use an integrated, multidisciplinary approach combining the three traditional land grant missions (research, education, and extension) with substantial stakeholder involvement, to accomplish these goals. Research efforts will focus on developing improved tools to study HuNoV, including advanced culture techniques, molecular virology methods for detection, and mathematical modeling. These will be used to design and evaluate truly effective control measures, such as better sanitizers or food processing technologies specifically designed to inactivate viruses. Extension and outreach efforts will extend basic and applied research findings into real-world practices. Using surveys, educational interventions (website, interactive activities, posters, print materials, and video), and short courses, extension materials will be delivered by both traditional and novel (such as social media and the Internet) mechanisms, assuring wide audience reach. Educational efforts focus on building scientific capacity in food virology by improving information and materials exchange, and building human capacity, with a focus on increasing diversity in the context of interdisciplinary university-based training programs. The strong and diverse project management team has decades of experience in various aspects of food virology. Collectively, the output of this project will be enhanced understanding, surveillance, and control of food borne HuNoV, with the ultimate goal of reducing burden of FBD caused by viruses.
Animal Health Component
(N/A)
Research Effort Categories
Basic
33%
Applied
33%
Developmental
34%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
7124030104020%
7124030110110%
7124030117015%
7124030302010%
7124030303010%
7125010110115%
7125010303020%
Goals / Objectives
Human noroviruses (HuNoV) are the most common cause of food borne disease (FBD). The purpose of the USDA-NIFA Food Virology Collaborative is to develop improved knowledge, skills, and capacity to study food borne viruses across the farm-to-fork continuum. Six core areas (objectives) are identified along with projected outputs over the 5-year funding duration. Objective 1, Molecular Virology: Develop improved methods to study HuNoV and other viral causes of FBD. Outputs include: increased understanding of HuNoV replication with the goal of producing an in vitro culture system; relevant, validated, cultivable HuNoV surrogates; identification of new viral FBD agents; and mathematical models for predicting strain emergence. Objective 2, Detection: Develop sensitive, rapid, and practical methods to detect/genotype HuNoV in relevant sample matrices. Outputs include practical, broadly reactive, validated detection methods for clinical, food, and environmental samples; recommended practices for discriminating virus infectivity status; microarray method(s) for HuNoV genotyping; and proof-of-concept biosensor technology. Objective 3, Epidemiology and Risk Analysis: Collect/analyze population data on epidemiological significance of virus-associated FBD, including epidemiological attribution and characterization of risk/costs. Outputs include quantitative risk assessment models; comprehensive assessment of the burden of epidemic and endemic HuNoV disease; and food source attribution models. Objective 4, Prevention and Control: Improve understanding of HuNoV prevalence/behavior in the food safety continuum for development of scientifically justifiable, commercial control measures. Outputs include estimates of occurrence of HuNoV in fresh produce and molluscan shellfish; validation of alternative indicators for viral contamination; evaluation of novel hand and surface sanitizers with antinoroviral efficacy; mathematical models to predict virus inactivation kinetics; and validated method(s) to inactivate HuNoV in molluscan shellfish and produce items. Objective 5, Extension, Education and Engagement: Engage stakeholders so as to translate/ disseminate research findings into practices targeting relevant audiences. Outputs include: on-line courses designed for food safety/public health professionals; a food service-focused educational curriculum for government and retail/foodservice industry partners; improved consumer educational materials; and outreach to fresh produce, molluscan shellfish, and retail food sectors. Objective 6, Capacity Building: Build scientific and human capacity to support increased, sustained efforts in food virology into the future. Outputs include: a comprehensive, publicly accessible literature database; increased food virology capacity in state public health laboratories; a highly qualified and diverse scientific workforce; and an inter-institutional graduate curriculum in food virology. Through collaborative activities and stakeholder involvement, the Collaborative will build greater appreciation for the role of viruses to FBD for the long term goal of producing a measurable reduction in burden of viral FBD.
Project Methods
Human noroviruses (HuNoV) are the most common cause of food borne disease (FBD). The purpose of the USDA-NIFA Food Virology Collaborative is to develop improved knowledge, skills, and capacity to study food borne viruses across the farm-to-fork continuum. Six core areas (objectives) are identified along with projected outputs over the 5-year funding duration. Objective 1, Molecular Virology: Develop improved methods to study HuNoV and other viral causes of FBD. Outputs include: increased understanding of HuNoV replication with the goal of producing an in vitro culture system; relevant, validated, cultivable HuNoV surrogates; identification of new viral FBD agents; and mathematical models for predicting strain emergence. Objective 2, Detection: Develop sensitive, rapid, and practical methods to detect/genotype HuNoV in relevant sample matrices. Outputs include practical, broadly reactive, validated detection methods for clinical, food, and environmental samples; recommended practices for discriminating virus infectivity status; microarray method(s) for HuNoV genotyping; and proof-of-concept biosensor technology. Objective 3, Epidemiology and Risk Analysis: Collect/analyze population data on epidemiological significance of virus-associated FBD, including epidemiological attribution and characterization of risk/costs. Outputs include quantitative risk assessment models; comprehensive assessment of the burden of epidemic and endemic HuNoV disease; and food source attribution models. Objective 4, Prevention and Control: Improve understanding of HuNoV prevalence/behavior in the food safety continuum for development of scientifically justifiable, commercial control measures. Outputs include estimates of occurrence of HuNoV in fresh produce and molluscan shellfish; validation of alternative indicators for viral contamination; evaluation of novel hand and surface sanitizers with antinoroviral efficacy; mathematical models to predict virus inactivation kinetics; and validated method(s) to inactivate HuNoV in molluscan shellfish and produce items. Objective 5, Extension, Education and Engagement: Engage stakeholders so as to translate/ disseminate research findings into practices targeting relevant audiences. Outputs include: on-line courses designed for food safety/public health professionals; a food service-focused educational curriculum for government and retail/foodservice industry partners; improved consumer educational materials; and outreach to fresh produce, molluscan shellfish, and retail food sectors. Objective 6, Capacity Building: Build scientific and human capacity to support increased, sustained efforts in food virology into the future. Outputs include: a comprehensive, publicly accessible literature database; increased food virology capacity in state public health laboratories; a highly qualified and diverse scientific workforce; and an inter-institutional graduate curriculum in food virology. Through collaborative activities and stakeholder involvement, the Collaborative will build greater appreciation for the role of viruses to FBD for the long term goal of producing a measurable reduction in burden of viral FBD.

Progress 06/01/16 to 05/31/17

Outputs
Target Audience:Formalized extension and outreach activities are designed to improve understanding and expand the use of measures to reduce viral foodborne disease. Seven major stakeholder groups are involved in the project: (1) fresh produce industry; (2) molluscan shellfish industry; (3) retail/institutional, food service and grocery sectors; (4) detection technologies; (5) cleaning, sanitizing, and hygiene sector; (6) cruise line industry; and (7) food processors. Four major audiences are targeted for communications programs: (1) food safety and public health professionals; (2) food industry professionals (food production, processing, retail, and service); (3) consumers; and (4) students. A synopsis of year 6 efforts is provided below. --NoroCORE exhibited at the annual meeting of the International Association for Food Protection (IAFP) in St. Louis, MO, July 31-August 3, 2016. Informational and promotional materials were distributed. NoroCORE team members also attended and presented to several professional development groups, the purpose of which was to provide updates on activities and increase stakeholder involvement. A stakeholder reception, with about 60 attendees, was hosted on the evening before the IAFP opening session. NoroCORE also hosted an educational exercise in which attendees joined Team Virus or Team Humanity and scored points for their respective teams by interacting with one another in a specially designed card game. The Naughty Noro, our Twitter persona of a tweeting norovirus particle, gave running commentary for the game. --In year 6, 13 new blog posts for the NoroCORE website were published, and NoroCORE submitted seven guest posts at the request of USDA-NIFA for their blog. The first of these was published on August 25, 2016 and is accessible at http://blogs.usda.gov/2016/08/25/norocore-a-comprehensive-approach-to-a-near-perfect-human-pathogen/. In addition to the Virus/ Humanity IAFP exercise described above, five other social media campaigns were launched, including Norovirus Cultured (August 2016), showcasing the new in vitro cultivation method; National Norovirus Day (Nov 4, 2016) to mimic GII.4, the most common genotype; Thanksgiving without Norovirus (Nov 2016) giving tips on safe food preparation; Santa's got Norovirus (December 2016) to highlight a new educational handout on cleaning a home contaminated with norovirus; and #MustWashHands (Jan 2017), where 34 members of the public submitted 114 photos of "Employees must wash hands" signs in foodservice restrooms and were educated about the Food Code. Combined, these six campaigns had over 47,000 views and almost 8,000 engagements with the public, and resulted in over 1,000 downloads of NoroCORE educational materials. --A special social media campaign was launched after the publication of the in vitro cultivation method in Science. NoroCORE's Facebook page had a series of posts about the research, receiving a combined 29,413 views and 4,214 engagements (likes, comments, shares, and post clicks). The team also created an infographic describing the research, which has been downloaded over 500 times from the NoroCORE website and is featured on the CDC's norovirus webpage. This public event also included a crossword puzzle game with teaching points on the importance of the cultivation method. --Six synchronous web-based educational courses on foodborne viruses directed at food safety and public health professionals (train-the-trainer) were completed, including formal presentations on an e-Learning platform. --A special NoroCORE newsletter dedicated to the culture method was published in May 2017, giving a total of seven newsletters by the end of project year 6. --NoroCORE was highlighted a second time in Food Safety Magazine (April/May 2017 issue), this time with updates of what the Collaborative has accomplished since 2014. --NoroCORE staff composed a whitepaper entitled "The Importance of Norovirus: Why you should we have a good food safety program to control its spread" that appeared on the GOJO Industries website in Nov 2016. It was geared towards independent restaurant owners and advised them on how to prevent and manage norovirus outbreaks in their establishments. --Representatives from the Interstate Shellfish Sanitation Conference (ISSC) travelled to five recreational boat shows with an exhibit covering the importance of not discharging boat wastes directly into waters. The exhibit was titled "Don't Poo (or Spew) in the Blue" and in addition to NoroCORE handouts on preventing shellfish contamination, it included an interactive quiz for boaters to test their knowledge of wastewater management. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?--There is extensive graduate student training associated with the USDA-NIFA Food Virology Collaborative. To date, 55 graduate students (25 Ph.D. and 30 M.S.) have been, or are in training at collaborating universities under the auspices of this project. Sixteen post-doctoral research associates and three ORISE fellows have been, or are being supported. Many of our collaborators also support undergraduates working on various NoroCORE-related projects. In all cases, students have assigned mentors with whom they work closely. In addition to their mentors, most institutions have a post-doctoral professional development program. --A list of national and international conferences in which NoroCORE collaborators and their students/staff presented during project year 6 is provided below. The Collaborative had representation at many other regional and local meetings not listed here. American Society for Microbiology Annual Meeting, Boston, MA, June 16-20, 2016. Institute for Food Technologists Annual Meeting, Chicago, Illinois, July 16-19, 2016. FoodMicro 2016, Dublin, Ireland, July 18-20, 2016 International Association for Food Protection Annual Meeting, St. Louis, MO, July 31-Aug 3, 2016. International Society for Food and Environmental Virology, Kusatsu, Japan, Sept 13-16, 2016. Sixth International Calicivirus Conference, Savannah, GA, Oct 10-13, 2016. 5th Annual Vaccine Development Center Meeting, San Antonio, TX, Nov 10, 2016. Society for Risk Analysis Annual Meeting, San Diego, CA, Dec 11-15, 2016. International Association for Food Protection European Food Safety Symposium, Brussels, Belgium, March 29-31, 2017. American Chemical Society National Meeting, San Francisco, CA, April 5, 2017. Food Safety Summit, Rosemont, IL, May 8-11, 2017. -NoroCORE held a full Collaborator and Stakeholder meeting in Arlington, VA on April 13-15, 2016. There were over 150 attendees present at this two-day meeting, with 47 posters on display, and 23 presentations from members of the Collaborative, as well as a two hour open session for stakeholder comment. --The NoroCORE Food Virology Literature database continues to be updated (>3,200 entries). --Three graduate fellowships were awarded in year 6, with the students representing the following institutions: North Carolina State University, University of Arkansas, and Baylor College of Medicine. One of these fellows belongs to a historically under-represented group. The cumulative number of fellowships for the project is now 15. --Four paid, research-based summer internships were provided to undergraduates from historically under-represented groups in summer 2016. These were hosted by instigators at Illinois Institute of Technology, Emory University, North Carolina Central University, and Clemson University. This brings the cumulative number of internships to 16. How have the results been disseminated to communities of interest?Results have been disseminated using traditional mechanisms including (1) publications (peer reviewed research publications, conference proceedings, book chapters, and articles in the scientific and popular press); (2) presentations at scientific and professional meetings (poster and oral); fact sheets, videos, webinars, and PowerPoint presentations; website and blogs; (3) NoroCORE newsletters; (4) the NoroCORE booth at professional meetings; and (5) in-person and web-based stakeholder meetings. We have an active website and significant social media efforts. See section on Target Audiences and Efforts for details. What do you plan to do during the next reporting period to accomplish the goals?A full description of next year's activities is provided in the no-cost extension document that was filed in December 2017. There are no changes. Project will be complete May 31, 2018.

Impacts
What was accomplished under these goals? Molecular Virology Core: Investigators at Baylor College of Medicine (BCM) reported on the first reproducible cultivation system for human norovirus; the work was published in Science in Sep, 2016. The method uses monolayers of non-transformed human intestinal cell cultures (organoids) and specially designed media to promote virus propagation. Over 15 human norovirus strains have been successfully replicated with up to 3.5 log increases in viral RNA over 72 hours. At least ten other labs, including some associated with NoroCORE, have received hands-on training from BCM along with all the protocols, cell lines, controls, and some key media components required to replicate the method. The method has been independently replicated in most of these labs. Using a next generation sequencing protocol and an automated pipeline, clinical samples from foodborne outbreaks that previously tested negative for human norovirus and sapovirus were screened, but only occasionally were other viruses identified. Analysis of the data from the VP1 domain of 250 previously sequenced GII.4 strains showed that recombination events occur more frequently than previously recognized. Using a dual typing tool based on the ORF 1 polymerase (P) gene and the capsid (C) gene, further study has shown that changes in the GII.4 capsid protein are predictable over the short-term by the local branching index, providing a tool to aid in prediction of future strain emergence. Detection Core: The synthetic ligands (i.e., monoclonal and single chain antibodies, synbodies, peptides, and nucleic acid aptamers) previously reported as having high affinity and broad reactivity for variety of human norovirus virus-like particles (VLPs) continue to be screened; many are in the patenting pipeline. Biotin-labeled synthetic glycans of A and B histoblood group antigens (HBGAs) were produced and shown to successfully capture human norovirus from fecal samples. Comparative studies of methods to discriminate human norovirus infectivity status (based on capsid integrity) were expanded to include not only RNase-RT-qPCR and antibody receptor binding assay, but also aptamer receptor binding, Western blot, and protein gel electrophoresis. A full comparative study of these methods is now being done using the Tulane virus (TuV) cultivable surrogate so that molecular results can be directly compared to cell culture infectivity. To date, depending on the inactivation treatment (heat or chlorine) received by TuV, no one method directly mimics infectivity, with most being conservative (overestimating) infectivity loss by 1-2 log. The previously reported low-density DNA microarray continues to be field-tested. Epidemiology and Risk Analysis Core: A first-generation agent-based quantitative risk model (NoroOPTIMAL), focused on transmission of norovirus in elder care facilities, was completed. The new model includes a sub-model added to address virus exposure by aerosolized vomitus. Completion of model validation and a public demonstration will be done in year 7. A farm-to-fork risk model for norovirus transmission by frozen berries was completed; it was designed to simulate the outbreak that occurred in Germany in 2012 linked to frozen strawberries imported from China. Sensitivity analysis and manuscript preparation are on-going. Most of the planned work in characterizing the burden of endemic and epidemic human norovirus illness has been completed. For instance, in a study focusing on pediatric cases of hospital-acquired gastroenteritis, 3% of stool samples were positive for norovirus and 10% for rotavirus. Serologic testing of NHANES serum samples (N=2,148; screened against 7 VLPs) revealed 83% seropositivity to at least one VLP, and 4.9% for all seven VLPs tested. Two epidemiological attribution models have been developed, one using Kaplan criteria for ascribing norovirus etiology, and the second assessing food service worker contributions to virus transmission and the impact of relevant interventions. Draft or published papers have been completed describing most of this work related to epidemiology. Prevention and Control Core: Investigation of high pressure processing (HPP) and pulsed light (PL) continued in year 6, using the murine norovirus (MNV) surrogate and focusing on berries For strawberries, MNV inactivation of 3.3 log PFU was achieved after PL treatment for 120 sec at a distance of 10.8 cm. For HPP, >4 log reduction in MNV infectivity was observed for fresh and frozen strawberries at 400 MPa, but only 2 log inactivation of the virus for blueberries treated with 600 MPa. The Institute for Food Safety and Health (IFSH) team continues to work with commercial entities to further evaluate and apply these technologies. Surface disinfectant technologies studied this period were free chlorine and chlorine dioxide. Treatment of a representative food contact surface with chlorine dioxide gas at 4 mg/L reduced Tulane virus (TuV) infectivity by 4.5 log, while human norovirus (GII.4) genome copy number was reduced by 4 logs at 8 mg/L, both after a 5 min treatment. In TuV-inoculated strawberries, much higher concentrations and contact times (8 mg/L for up to 8 min) were necessary for complete virus inactivation, which resulted in unwanted product defects. Studies investigating sequentially higher concentrations of free chlorine (25 ppm up to 5,000 ppm) revealed that human norovirus may be more sensitive to this oxidant than previously believed (in some cases, 4 log inactivation after treatment of >200 ppm for 1 min), although there were strain-specific differences in susceptibility. A variety of commercial hand sanitizers were screened for anti-human norovirus efficacy using in vivo fingerpad assays. Compared to a 60% ethanol benchmark, which produced a 0.5-1.0 log inactivation after 1 min exposure, the products screened provided an added benefit ranging from nothing to an additional 2.0 log inactivation. Formulation influenced efficacy but no product was able to produce the targeted 4 log inactivation. Plant-based extracts, phytochemicals, and enzymes do not show promise for complete inactivation of human norovirus surrogates. Extension and Outreach Core: Analysis of samples (n > 4,700) collected in environmental monitoring studies (public and healthcare environments, n > 750) is complete and 61 presumptively positive samples are in confirmation. The editable model guidelines that focus on vomit and fecal matter cleanup for the retail and institutional food sectors have been completed. Pre- and post-test interviews with 40 educators are underway to evaluate ease of use and potential for compliance with the guidelines. As initially proposed by NoroCORE team members, the Conference for Food Protection is considering inclusion of written guidance on vomit/fecal matter cleanup in the next model Food Code document. The educational modules for food safety and public health professionals (i.e., History, Molecular Virology, Epidemiology, Prevention and Control, Detection and Communication) are complete and in final peer review prior to posting. Further details on other extension and outreach efforts are described above. Capacity Building Core: Efforts in reagent and information exchange, student training, and fostering communications amongst the NoroCORE team and with stakeholders are described elsewhere in the report. In year 6, two discretionary funding proposals were awarded. One of these focuses on creation of an "app" for public reporting of norovirus-like symptoms and subsequent regional mapping; the other on the ability of an existing crowdsourcing platform to identify, in real time, retail/food service associated norovirus outbreaks.

Publications

  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Yeargin, T., D. Buckley, A. Fraser, and X. Jiang. 2016. The survival and inactivation of enteric viruses on soft surfaces: A systematic review of the literature. American Journal of Infection Control, 44(11): 1365-1373. DOI: dx.doi.org/10.106/j.ajic.2016.03.018.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Ng TF, Maga�a L, Montmayeur A, Lopez MR, Gregoricus N, Oberste MS, and Vinj� J 2016. Characterization of a Salivirus (Picornaviridae) from a Diarrheal Child in Guatemala. Genome Announc, 4(1):pii: e01751-15. DOI: 10.1128/genomeA.01751-15.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Gonzalez MD, Langley LC, Buchan BW, Faron ML, Maier M, Templeton K, Walker K, Popowitch EB, Miller MB, Rao A, Liebert UG, Ledeboer NA, Vinj� J, and Burnham CA 2016. Multicenter Evaluation of the Xpert Norovirus Assay for Detection of Norovirus Genogroups I and II in Fecal Specimens. J Clin Microbiol, 54(1):142-7. DOI: 10.1128/JCM.02361-15.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Xiuli Dong, Jessica J. Broglie, Yongan Tang, and Liju Yang 2016. Evaluation of Bio-layer Interferometric Biosensors for Label-free Rapid Detection of Norovirus using Virus Like Particles. Journal of Analytical and Bioanalytical Techniques, 7:329. DOI: DOI: 10.4172/2155-9872.1000329.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Kirby, A.E., Streby, A., and Moe, C.L. 2016. Vomiting as a Symptom and Transmission Risk in Norovirus Illness: Evidence from Human Challenge Studies. PLoS One, 11(4):e0143759. DOI: 10.1371/journal.pone.0143759. eCollection 2016.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Atmar, R.L., Baehner, F., Cramer, J.P., Song, E., Borkowski, A., Mendelman, P.M., and NOR-201 Study Group 2016. Rapid Responses to 2 Virus-Like Particle Norovirus Vaccine Candidate Formulations in Healthy Adults: A Randomized Controlled Trial. J INfect Dis, 214(6):845-53. DOI: 10.1093/infdis/jiw259.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Ettayebi, K., Crawford, S.E., Murakami, K., Broughman, J.R., Karandikar, U., Tenge, V.R., Neill, F.H., Blutt, S.E., Zeng, X.L., Qu, L., Kou, B., Opekun, A.R., Burrin, D., Graham, D.Y., Ramani, S., Atmar, R.L., and Estes, M.K. 2016. Replication of human noroviruses in stem cell-derived human enteroids. Science, 353(6306):1387-93. DOI: 10.1126/science.aaf5211.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Shah, M. P., Wikswo, M. E., Barclay, L., Kambhampati, A., Shioda, K., Parashar, U. D., Vinj�, J., and Hall, A. J. 2017. Near real-time surveillance of U.S. norovirus outbreaks by the norovirus sentinel testing and tracking network - United States, August 2009-July 2015. MMWR Morb Mortal Wkly Rep, 66(7):185-189. DOI: 10.15585/mmwr.mm6607a1.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Ramani, S., Neill, F.H., Ferreira, J., Treanor, J.J., Frey, S.E., Topham, D.J., Goodwin, R.R., Borkowski, A., Baehner, F., Mendelman, P.M., Estes, M.K., and Atmar, R.L. 2017. B-Cell responses to intramuscular administration of a bivalent virus-like particle human norovirus vaccine. Clin Vaccine Immunol, 24(5):e00571-16. DOI: 10.1128/CVI.00571-16.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Sharma, S., Carlsson, B., Czako, R., Vene, S., Haglund, M., Ludvigsson, J., Larson, G., Hammarstrom, L., Sosnovtsev, S.V., Atmar, R.L., Estes, M.K., and Svensson, L. 2017. Human sera collected between 1979 and 2010 possess blocking-antibody titers to pandemic GII.4 noroviruses isolated over three decades. J Virol, 91(14):e00567-17. DOI: 10.1128/JVI.00567-17.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Hurwitz, A.M., Huang, W., Kou, B., Estes, M.K., Atmar, R.L., and Palzkill, T. 2017. Identification and characterization of single-chain antibodies that specifically bind GI noroviruses. PLoS One, 12(1):e0170162. DOI: 10.1371/journal.pone.0170162.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Hurwitz, A.M., Huang, W., Estes, M.K., Atmar, R.L., and Palzkill, T. 2017. Deep sequencing of phage-displayed peptide libraries reveals sequence motif that detects norovirus. Protein Eng Des Sel, 30(2): 129-139. DOI: 10.1093/protein/gzw074.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Angelo, K.M., Nisler, A.L., Hall, A.J., Brown, L.G., and Gould, L.H. 2017. Epidemiology of restaurant-associated foodborne disease outbreaks, United States, 1998-2013. Epidemiology and Infection, 145(3): 523-534.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Evans, H., M. Getty, M. Finney, C. Leone, and A. Fraser. 2016. Accuracy and Readability of Information about Human Noroviruses in Food Safety Education Materials Targeting Consumers. Food Protection Trends, 36(2): 133-139.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Evans, H., M. Chao, M. Finney, C. Leone, and A. Fraser. 2016. Content Analysis of Web-based Norovirus Education Materials Targeting Consumers: An Assessment of Alignment and Readability. Food Control, 65: 32-36.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Leone, C., L. Jaykus, S. Cates, and A. Fraser. 2016. A Review of State Licensing Regulations to Determine Alignment with Best Practices to Prevent Human Norovirus Infections in Child-Care Centers. Public Health Reports, 131(3): 449-460.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Gupta, N., Lainson, J.C., Belcher, P.E., Shen, L., Mason, H.S., Johnston, S.A., Diehnelt, C.W. 2017. Cross-Reactive Synbody Affinity Ligands for Capturing Diverse Noroviruses. Analytical Chemistry 89 (13): 7174-7181 DOI: 10.1021/acs.analchem.7b01337
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Hall, A.J. Norovirus Epidemiology and Food Safety. FDA Central Region Retail Food Protection Seminar, Milwaukee, WI, August 31, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Ye, M. Inactivation of Murine Norovirus on Berries by High Pressure Processing and Pulsed Light. International Society for Food and Environmental Virology, Kusatsu, Japan, September 13, 2016 - September 16, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Lee, A. Inactivation of viruses by light based technologies. Institute of Food Technologists 2016, Chicago, July 16, 2016 - July 19, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Atmar, R.L. Advances in replication of human norovirus. International Association for Food Protection (IAFP) 2016, St. Louis, MO, July 31, 2016 - August 03, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Lee, A., Zuber, S., and Manual, L. Balancing Food Quality and Virus Inactivation for Sensitive Foods (Symposium). IAFP European Food Safety Symposium 2016, Athens, Greece, May 11, 2016 - May 13, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: Hall, A.J. Norovirus outbreak associated with wedding cakes, Massachusetts, 2002. UGA Center for Food Safety Annual Meeting, Atlanta, GA, March 7, 2017.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: Hall, A.J. Epidemiology and genotype differences in foodborne norovirus outbreaks - United States, 2009-2015. 12th International Symposium of the UJNR Toxic Microorganisms Panel, Laurel, MD, May 16, 2017.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: Hall, A.J. Vaccines in the pipeline: norovirus and respiratory syncytial virus (RSV). National Adult and Influenza Immunization Summit, Atlanta, GA, May 10, 2017.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Kirby, A.E. Norovirus Seroprevalence in NHANES Specimens from the United States in 1999-2000 and 2003-2004. International Calicivirus Conference, Savannah GA, October 3, 2016 - October 9, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Estes, M.K. Keynote Lecture: Human Norovirus Mysteries - Old and New. 6th International Calicivirus Conference, Savannah, GA, October 10, 2016 - October 13, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Atmar, R.L. State of the Art Lecture. Norovirus Vaccines: Current Status and Future Prospects. 6th International Calicivirus Conference, Savannah, GA, October 10, 2016 - October 13, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Estes, M.K. Keynote Lecture. Norovirus Vaccines: Progress and Challenges. 5th Annual Vaccine Development Center of San Antonio Conference, San Antonio, TX, November 10, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Hall, A.J. The Global Burden of Norovirus Disease. International Calicivirus Conference, Savannah, GA, October 11, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Hall, A.J. Norovirus and Food Safety. FDA Rapid Response Teams Annual Meeting, Savannah, GA, November 16, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Hall, A.J. Norovirus and Restaurants. Southeast Regional OutbreakNet Meeting, Nashville, TN, November 30, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Beaulieu, S.M., Mokhtari, A., and Kelly, R. Transmission of Norovirus in Bioaerosols: An Exposure Modeling Approach. International Association of Food Protection, St. Louis, MO, July 31, 2016 - August 4, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Beaulieu, S.M., Mokhtari, A., Anderson, M., Kelly, R., and Jaykus, LA. Evaluating Intervention Strategies to Reduce the Burden of Foodborne Disease Caused by Human Norovirus: A Risk-Based Approach Using a Long-term Care Facility as Proof of Concept. International Association of Food Protection, St. Louis, MO, July 31, 2016 - August 4, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: Mertens, B.S, Moore, M.D., Jaykus, L.A., and Velev, O.D. New colloidal approaches for human norovirus cleanup and inactivation using surfactants and copper-ion based disinfectants. American Chemical Society National Meeting Spring 2017, San Francisco, CA, April 5, 2017.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Ettayebi, K., Crawford, S.E., Murakami, K., Broughman, J., Karankikar, U., Tenge, V.R., Neill, F.H., Blutt, S.E., Ramani, S., Zeng, X.L., Qu, L., Opekun, A.R., Burrin, D., Graham, D.Y., Atmar, R.L., and Estes, M.K. Strain-specific human norovirus replication in biologically relevant human enteroid cultures. 6th International Calicivirus Conference, Savannah, GA, October 10, 2016 - October 13, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Costantini, V., Ettayebi, K., Zeng, X.L., Crawford, S.E., Atmar, R.L., Estes, M.K., and Vinje, J. Human norovirus replication in human intestinal enteroids as a model to evaluate virus inactivation. 6th International Calicivirus Conference, Savannah, GA, October 10, 2016 - October 13, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Karankikar, U.C., Crawford, S.E., Ajami, N.J., Murakami, K., Kou, B., Ettayebi, K., Papanicolaou, G.A., Jongwutiwes, U., Perales, M.A., Shia, J., Mercer, D., Finegold, M.J., Vinje, J., Atmar, R.L., and Estes, M.K. Identifying intestinal cell types that can support replication of human norovirus in intestinal biopsies from immunocompromised patients and intestinal stem cell derived cultures. 6th International Calicivirus Conference, Savannah, GA, October 10, 2016 - October 13, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Wang, Q., Gao, X., Esseili, M., Saif, L., Lindesmith, L., Baric, R. S., Kou, B., Estes, M.K., and Atmar, R.L. Comparison of the binding of GII.4 and GI.1 human norovirus strains to lettuce. 6th International Calicivirus Conference, Savannah, GA, October 10, 2016 - October 13, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Shanker, S., Czako, R., Sapparapu, G., Alvarado, G., Viskovska, M., Moreno, R., Sankaran, B., Atmar, R.L., Crowe, J.E. Jr., Estes, M.K., and Venkataram Prasad, B.V. Structural basis for norovirus neutralization by an HBGA blocking human IgA antibody. 6th International Calicivirus Conference, Savannah, GA, October 10, 2016 - October 13, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Ramani, S., Neill, F.H., Ferreira, J., Treanor, J.J., Frey, S., Topham, D.J., Goodwin, R., Borkowski, A., Baehner, F., Mendelman, P.M., Estes, M.K., and Atmar, R.L. Antibody Secreting Cell (ASC) and memory B cell immune responses to intramuscular administration of a bivalent virus-like particle (VLP) human norovirus (HuNoV) vaccine candidate. 6th International Calicivirus Conference, Savannah, GA, October 10, 2016 - October 13, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: de Jusus Diaz, D.A., Ahorrio, C.N., Zeng, X.L., Ettayebi, K., Estes, M.K., and Green, K.Y. Screening Infectious Human Noroviruses Using A Human-Derived Small Intestine Enteroid Cell Culture System. 6th International Calicivirus Conference, Savannah, GA, October 10, 2016 - October 13, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Fraser, A.M. Intervention, Development, and Evaluation of Mixed-method Approaches for Retail, Consumer and Food Service. International Association of Food Protection, St. Louis, Missouri, August 1, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: Ye, M, Feng, D., Rolfe, C., and Lee, A. Pulsed light inactivation of murine norovirus, Escherichia coli, Listeria monocytogenes and Salmonella on strawberries. 2017 IFT-EFFoST International Nonthermal Processing Conference, Burr Ridge, IL, May 23, 2017 - May 25, 2017.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: Ye, M, Rolfe, C., Zhang, Y., and Lee, A. Application of high pressure processing on fresh and frozen strawberries and blueberries to inactivate murine norovirus and bacteriophage MS2. 2017 IFT-EFFoST International Nonthermal Processing Conference, Burr Ridge, IL, May 23, 2017 - May 25, 2017.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Shearer, A.E.H., and Kniel, K.E. Retention of Tulane Virus and Murine Norovirus by Zero-Valent Iron Treated by Various Elution Buffers. International Association for Food Protection, St. Louis, MO, July 31, 2016 - August 3, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Teichman, June, Wang, Q., and Kniel, K.E. Potential binding of Tulane virus to human intesntinal Caco-2 cells. American Society for Microbiology 2016 Annual Meeting, Boston, MA, June 16, 2016 - June 20, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Ye, M, Zuber, S, Butot, S, Cantergiani, F, and Lee, A. Inactivation of murine norovirus (MNV-1) on strawberries by pulsed light (PL). IAFP 2016, St Louis, July 31, 2016 - August 03, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Zhang, Y, Ye, M, Zhang, Q, Zuber, S, Butot, S, Grove, S, Sommerville, J, Cantergiani, F, and Lee, A. Application of High Pressure Processing on Fresh and Frozen Strawberries and Blueberries to Inactivate Murine Norovirus. IAFP 2016, St Louis, July 31, 2016 - August 3, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Zeng, J, Ye, M, Grove, S, and Lee, A. Inactivation of Murine Norovirus by Novel Sanitizers in Combination with High Power Ultrasound on Romaine Lettuce. IAFP 2016, St Louis, July 31, 2016 - August 3, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Fraser, A.M. Noroviruses and Hard Surfaces: Using the Results from a Multi-State Prevalence Study to Inform a Foodservice Intervention. International Association of Food Protection, St. Louis, Missouri, August 1, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Fraser, A.M. Reducing Viral and Parasitic Risk on Produce: Methods for Training. International Association of Food Protection, St. Louis, Missouri, August 1, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: Xiuli Dong, Marsha M. Moyer, Fan Yang, Ya-Ping Sun, and Liju Yang. Carbon Dots' Antiviral Functions Against Noroviruses. The 2017 annual meeting of the Institute of Biological Engineering (IBE), Salt Lake City, March 30, 2017 - April 1, 2017.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Yard, C, Morgan, M, D'Souza, D. H. Reduction of Tulane Virus (a Human Norovirus Surrogate) by Chlorine Dioxide (ClO2) Gas. IAFP annual meeting, St. Louis, MO, July 31, 2016 - August 3, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Anderson, M., Mokhtari, A., Beaulieu, S.M., and Jaykus, LA. Data Development for a Predictive Risk Assessment Model Used to Evaluate Intervention Strategies that Reduce the Burden of Foodborne Disease Caused by Human Norovirus. International Association for Food Protection, St. Louis, MO, July 31, 2016 - August 4, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Murakami, K., Tenge, V.R., Ettayebi, K., Crawford, S.E., Neill, F.H., Ramani, S., Zeng, X.L., Atmar, R.L., and Estes, M.K. Characterization of active components in bile that enhance GII.3 human norovirus replication in human intestinal enteroids. 6th International Calicivirus Conference, Savannah, GA, October 10, 2016 - October 13, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Palzkill, T., Huang, W., Soeung, V., Estes, M.K., and Atmar, R.L. Mapping norovirus antigen-antibody and protein-protein interactions with Jun-Fos assisted phage display and deep sequencing. 6th International Calicivirus Conference, Savannah, GA, October 10, 2016 - October 13, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Alvarado, G., Estes, M.K., Atmar, R.L., and Crowe, J.E. Jr. Isolation and characterization of GI and GII cross-reactive human monoclonal antibodies. 6th International Calicivirus Conference, Savannah, GA, October 10, 2016 - October 13, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Kambhampati, A., Vargas, B., Mushtaq, M., Perregaux, S., Atmar, R.L., Vinje, J., Parashar, U.D., Lopman, B., and Rodriguez-Barradas, M.C. NOVVA: Active surveillance to quantify the burden of viral gastroenteritis in U.S. Veterans Affairs (VA) patient population, Houston, 2015-2016. 6th International Calicivirus Conference, Savannah, GA, October 10, 2016 - October 13, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Kou, B., Neill, F.H., Estes, M.K., and Atmar, R.L. Unmasking hidden norovirus epitope to improve diagnostics. 6th International Calicivirus Conference, Savannah, GA, October 10, 2016 - October 13, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Chao, M.G., A. Dube, C. Moore, C. Leone, and A. Fraser Content Analysis of Vomit and Fecal Matter Clean-Up Procedures to Prevent the Spread of Enteric Agents in Retail/Foodservice Operations. International Association of Food Protection, St. Louis, Missouri, August 1, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Qu, L., Atmar, R.L., and Estes, M.K. Identification of a Novel Small Zinc finger Protein in Genogroup GI and GIII Noroviruses. 6th International Calicivirus Conference, Savannah, GA, October 10, 2016 - October 13, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Qu, L., Murakami, K., Broughman, J.R., Lay, M.K., Guix, S., Tenge, V.R., Atmar, R.L., and Estes, M.K. Replication of human norovirus RNA in mammalian cells reveals a lack of interferon response. 6th International Calicivirus Conference, Savannah, GA, October 10, 2016 - October 13, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Cramer, J., Baehner, F., Atmar, R.L., Song, E., Borkowski, A., and Mendelman, P.M. Antibody persistence and immune memory to norovirus VLP vaccine candidate formulations. 6th International Calicivirus Conference, Savannah, GA, October 10, 2016 - October 13, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Viskovska, M.A., Deng, L., Shanker, S., Kibe, A., Muhaxhiri, Z., Song, Y., Estes, M.K., and Venkataram Prasad, B.V. Structure of GII.4 Norovirus Protease - Potential for Design of Broad-Spectrum Protease Inhibitors. 6th International Calicivirus Conference, Savannah, GA, October 10, 2016 - October 13, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Choi, J.M., Lee, M., Park, Y.B., Viskovska, M., Estes, M.K., and VEnkataram Prasad, B.V. Virtual screening of ZINC library against norovirus non-structural proteins accelerated by OpenCl and Hadoop file system implementation. 6th International Calicivirus Conference, Savannah, GA, October 10, 2016 - October 13, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Moore, C., C. Leone, N. Braun, and A. Fraser Using Revised Bloom's Taxonomy to Develop a Knowledge-transfer Module about Noroviruses. International Association of Food Protection, St. Louis, Missouri, August 1, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Romero, A., M.G. Chao, C. Leone, L. Jayasekara, and A. Fraser Cleanliness of Environmental Surfaces in Elementary Schools as Determined by ATP levels. International Association of Food Protection, St. Louis, Missouri, July 31, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Buckley, D., J. Anderson, J. Shields, C. Pettigrew, X. Jiang, and A. Fraser Effect of multi-phase educational and motivational intervention on cleanliness of surfaces in a commercial kitchen. International Association of Food Protection, St. Louis, Missouri, August 1, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Bradshaw, E., Goulter, R.M., Chapman, B., Jaykus, L.A. The Go Noroviral Experiment: An Interactive Teaching Tool for Modeling Person-to-Person Disease Transmission. International Association for Food Protection, St. Louis, MO, August 1, 2016.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Overbey, K., Faircloth, J., Seymour, N., Bradshaw, E., Jaykus, L.A., Chapman, B. School Responses to Norovirus Outbreaks: Policies, Procedures and Potential for Improvement. International Association for Food Protection, St. Louis, MO, August 2, 2016
  • Type: Other Status: Other Year Published: 2016 Citation: Norovirus testing for detection and intervention: Hands-on laboratory training for public health, industry, and research lab applications. Workshop at the annual meeting of the International Association for Food Protection, July 29-30, 2016.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Bradshaw, E.S., Goulter, R.M., Chapman, B., and Jaykus, L.-A. 2017. The Go Noroviral Experiment: An interactive citizen science teaching tool for modeling norovirus transmission. Food Prot Trends, 37(4): 240-246.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Almand, E.A., M.D. Moore, and L. Jaykus. 2017. Virus-bacteria interactions: An emerging topic in human infection. Viruses 9(58): doi: 10.3390/v9030058.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Almand, E.A., M.D. Moore, and L.A. Jaykus. 2017. Human norovirus binding to select bacteria representative of human gut microbiota. PLoS One. Mar 3; 12(3): e0173124. doi:10.1371/journal.pone.0173124
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Moore, M.D., and L.-A. Jaykus. 2017. Development of a recombinase polymerase amplification assay for detection of epidemic human noroviruses. Sci Rep. Jan 9; 7: 40244. doi: 10.1038/srep40244.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Moore, M.D., B.I. Escudero-Abarca, and L.A. Jaykus. 2017. An enzyme-linked aptamer sorbent assay to evaluate aptamer binding. Methods Mol Biol. 1575: 291-302. doi: 10.1007/978-1-4939-6857-2_18.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Manuel, C., M. Moore, and L. Jaykus. 2017. Efficacy of a Disinfectant Containing Silver Dihydrogen Citrate Against GI.6 and GII.4 Human Norovirus. J Appl Microbiol. Jan; 122(1): 78-86. doi:10.1111/jam.13331.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Moore M.D., B.G. Bobay, B.Mertens, and L.-A. Jaykus. 2016. Human norovirus aptamer exhibits a high degree of target conformation-dependent binding similar to that of receptors and discriminates particle functionality. mSphere, 1(6): e00298-16.
  • Type: Books Status: Published Year Published: 2017 Citation: Svensson, L., Desselberger, U., Greenberg, H.B., and Estes, M.K. (eds.). 2016. Viral Gastroenteritis. Molecular Epidemiology and Pathogenesis. Academic Press, San Diego, CA.
  • Type: Book Chapters Status: Published Year Published: 2017 Citation: Atmar, R.L., and Estes, M.K. 2017. Human caliciviruses. In: Richman, D.D., Whitley, R.J., and Hayden, F.G. (eds.), Clinical Virology, 4. Churchill Livingstone, New York. Chapter 49, p. 1189-1208.
  • Type: Book Chapters Status: Published Year Published: 2016 Citation: Bradshaw, E., and Jaykus, L.-A. 2016. Chapter 17: Risk Assessment for Foodborne Viruses. In S. Goyal and J. Cannon (Eds.), Viruses in Foods, 2nd Edition. Switzerland: Springer International Publishing.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Shanker, S., Czako, R., Sapparapu, G., Alvarado, G., Viskovska, M., Sankaran, B., Atmar, R.L., Crowe, JE Jr., Estes, M.K., and Prasad, B.V.V. 2016. Structural basis for norovirus neutralization by an HBGA blocking human IgA antibody. Proc Natl Acad Sci USA, epub 2016 Sep 9. DOI: 10.1073/pnas.1609990113.
  • Type: Book Chapters Status: Published Year Published: 2017 Citation: Ramani, S., Estes, M.K., and Atmar, R.L. 2017. Immune response. In: Chan, P.K.S., Kwan, H.S., and Chan, M.C.W. (eds.), The Norovirus. Features, Detection, and Prevention of Foodborne Disease, 1. Academic Press, San Diego, CA. Chapter 7, p. 89-108.
  • Type: Book Chapters Status: Published Year Published: 2016 Citation: Venkataram Prasad, B.V., Shanker, S., Muhaxhiri, Z., Choi, J.M., Atmar, R.L., and Estes, M.K. 2016. Structural biology of noroviruses. In: Svensson, L., Dessekberger, U., Greenberg, H.B., and Estes, M.K. (eds.), Viral Gastroenteritis. Molecular Epidemiology and Pathogenesis, 1. Academic Press, San Diego, CA. Chapter 3.1, p. 329-354.
  • Type: Book Chapters Status: Published Year Published: 2016 Citation: Ramani, S., Estes, M.K., and Atmar, R.L. 2016. Norovirus vaccine development. In: Svensson, L., Desselberger, U., Greenberg, H.B., and Estes, M.K. (eds.), Viral Gastroenteritis. Molecular Epidemiology and Pathogenesis, 1. Academic Press, San Diego, CA. Chapter 3.6, p. 447-470.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Leone, C.M., C. Tang, J. Sharp, X. Jiang, and A. Fraser 2016. Presence of Human Noroviruses on Bathroom Surfaces: A review of the literature. International Journal of Environmental Health Research, 26(4):1-13.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: In, J.G., Foulke-Abel, J., Estes, M.K., Zachos, N.C., Kovbasnjuk, O., and Donowitz, M. 2016. Human mini-guts: new insights into intestinal physiology and host-pathogen interactions. Nat Rev Gastroenterol Hepatol, epub 2016 Sep 28. DOI: doi:10.1038/nrgastro.2016.142.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Prasad, B.V.V., Shanker, S., Muhaxhiri, Z., Deng, L., Choi, J.M., Estes, M.K., Song, Y., Palzkill, T., and Atmar, R.L. 2016. Antiviral targets of human noroviruses. Curr Opin Virol, 18:117-25. DOI: 10.1016/j.coviro.2016.06.002.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Mills, M., and Estes, M.K. 2016. Physiologically Relevant Human Tissue Models for Infectious Diseases. Drug Discovery Today. Drug Discov Today, 21(9):1540-52. DOI: 10.1016/j.drudis.2016.06.020.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Wang, Z., Lapinski, M., Quilliam, E., Jaykus, L., and Fraser, A. 2017. The Effect of Hand-Hygiene Interventions on Infectious Disease-Associated Absenteeism in Elementary Schools: A Systematic Literature Review. American Journal of Infection Control, 45:682-689. DOI: http://dx.doi.org/10.1016/j.ajic.2017.01.018.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Shanker, S., Hu, L., Ramani, S., Atmar, R.L., Estes, M.K., and Venkataram Prasad, B.V. 2017. Structural features of glycan recognition among viral pathogens. Curr Opin Struct Biol, 44:211-218. DOI: 10.1016/j.sbi.2017.05.007.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Xiuli Dong, Marsha M Moyer, Fan Yang, Ya-ping Sun, and Liju Yang 2017. Carbon Dots' Antiviral Functions Against Noroviruses. Scientific Reports, 7:519. DOI:10.1038/s41598-017-00675-x.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Cannon, J.L., Barclay, L, Collins, N.R., Wikswo, M.E., Castro, C.J., Maga�a, L.C., Gregoricus, N., Marine, R.L., Chhabra, P., and Vinj�, J. 2017. Genetic and Epidemiologic Trends of Norovirus Outbreaks in the US Demonstrated Emergence of Novel GII.4 Recombinant Viruses, 2013-2016. Journal of Clinical Microbiology, 55(7):2208-2221. DOI: 10.1128/JCM.00455-17.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Garnett, E, Gretsch, S., Null, C, and Moe, C.L. 2016. Consumer Response to Gastrointestinal Illness Perceived To Originate from Food Service Facilities. Journal of Food Protection, 79(10):1717-1724. DOI: 10.4315/0362-028X.JFP-15-444.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Yi, J, Sederdahl, B., Wahl, K., Jerris, R., Kraft, C., McCracken, C., Gillespie, S., Kirby, A.E., Shane, A, Moe, C.L., and Anderson, E. 2016. Rotavirus and Norovirus in Pediatric Healthcare-Associated Gastroenteritis. Open Forum Infectious Diseases. DOI: 10.1093/ofid/ofw181.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Qu, L., Murakami, K., Broughman, J.R., Lay, M.K., Guix, S., Tenge, V.R., Atmar, R.L., and Estes, M.K. 2016. Replication of human norovirus RNA in mammalian cells reveals a lack of interferon response. J Virol, 90(19): 8906-23. DOI: 10.1128/JVI.01425-16.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Menon, V.K., George, S., Sarkar, R., Giri, S., Samuel, P., Vivek, R., Saravanabavan, A., Liakath, F.B., Ramani, S., Iturriza-Gomara, M., Gray, J.J., Brown, D.W., Estes, M.K., and Kang, G. 2016. Norovirus Gastroenteritis in a Birth Cohort in Southern India. PLoS One, 11(6):e0157007. DOI: 10.1371/journal.pone.0157007.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Karandikar, U.C., Crawford, S.E., Ajami, N.J., Murakami, K., Kou, B., Ettayebi, K., Papanicolaou, G.A., Jongwutiwes, U., Perales, M.A., Shia, J., Mercer, D., Finegold, M.J., Vinj�, J., Atmar, R.L., and Estes, M.K. 2016. Detection of human norovirus in intestinal biopsies from immunocompromised transplant patients. J Gen Virol, 97: 2291-2300. DOI: 10.1099/jgv.0.000545.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Sapparapu, G., Czako, R., Alvarado, G., Shanker, S., Prasad, B.V.V., Atmar, R.L., Estes, M.K., and Crowe, JE Jr. 2016. Frequent use of the IgA isotype in human B cells encoding potent norovirus-specific monoclonal antibodies that block HBGA binding. PLoS Pathog, 12(6):e1005719. DOI: 10.1371/journal.ppat.1005719.


Progress 06/01/15 to 05/31/16

Outputs
Target Audience:Formalized extension and outreach activities are designed to improve understanding and expand the use of measures to reduce viral foodborne disease. Seven major stakeholder groups are involved in the project: (1) fresh produce industry; (2) molluscan shellfish industry; (3) food service and grocery sectors; (4) detection technologies; (5) cleaning, sanitizing, and hygiene sector; (6) cruise line industry; and (7) food processors. Four major audiences are targeted for communications programs: (1) food safety and public health professionals; (2) food industry professionals (food production, processing, retail, and service); (3) consumers; and (4) students. A synopsis of year 5 efforts is provided below. -- NoroCORE exhibited at the annual meeting of the International Association for Food Protection (IAFP) in Portland, OR, July 25-28, 2015. Informational and promotional materials were distributed. NoroCORE team members also attended and presented to several professional development groups, the purpose of which was to provide updates on activities and increase stakeholder involvement. A stakeholder reception, with about 50 attendees, was hosted on the evening before the IAFP opening session. -- In year 5, the following social media activities were undertaken: (1) a "Go Noroviral" citizen science exercise was conducted at IAFP, 2015; (2) two creative informational campaigns were launched [i.e., the "Naughty Noro" campaign, in which a personified norovirus (NoV) finds people talking about the virus and tweets back at them; and the "My Norovirus Nightmare" campaign, in which the public was encouraged to share their personal experiences with NoV infection]. Twenty-nine blog posts were produced on the website, including special posts for Global Hand Washing Day and Food Safety Month. The Traveling Microbiologist blog, which covers travel-related foodborne infection control topics, posted five blogs in year 5. In the last 12 months, the NoroCORE Facebook page has gained 99 followers, with 472 likes total. --NoroCORE was represented at regional and national fresh produce safety and molluscan shellfish meetings. --NoroCORE investigators delivered formal training to NC schoolteachers in the form of a "simulated" outbreak that can be used in the middle school classroom environment. --The content for six synchronous web-based educational courses on foodborne viruses directed at food safety and public health professionals (train-the-trainer) has been finalized. These are being prepared for presentation on an e-Learning platform. --NoroCORE team members worked with various companies developing virus detection technologies, providing them recommendations and guidance for marketing, research, and development. --A focused laboratory-based study to validate the efficacy of select commercial surface disinfectants against human NoV was initiated with support from the cruise line and sanitation and hygiene industry sectors. --Two studies published by NoroCORE investigators received significant media attention. The first demonstrated the efficacy of copper for inactivation of human NoV. The second used a simulated vomiting device to provide additional evidence of virus aerosolization associated with projectile vomiting. Over 200 media outlets picked up the latter. An associated YouTube video of the vomiting machine (https://www.youtube.com/watch?v=jGvqb87DXSI) received over 40,000 views. -- Two NoroCORE newsletters were produced (released July, 2015 and April, 2016), giving a total of six by the end of project year 5. --NoroCORE was highlighted in the August 2015 issue of Food Technology magazine in a story entitled "Going Viral." --Two NoroCORE investigators were invited participants at the European Food Safety Authority-sponsored Foodborne Viruses Workshop in London, UK, February 22-25, 2016. The purpose of the workshop was to identify future foodborne virus research priorities. Changes/Problems:A collaborative investigator (and member of the executive board) from University of Georgia has left the university, although she will continue serving as the scientific supervisor for key institutional graduate students and staff. Her administrative roles have been transferred to a colleague and no interruption of work, or changes in contributions, are anticipated. What opportunities for training and professional development has the project provided?--There is extensive graduate student training associated with the USDA-NIFA Food Virology Collaborative. To date, 55 graduate students (25 Ph.D. and 30 M.S.) have been, or are in training at collaborating universities under the auspices of this project. Sixteen post-doctoral research associates and 3 ORISE fellows have been, or are being supported. Many of our collaborators also support undergraduates working on various NoroCORE-related projects. In all cases, students have assigned mentors with whom they work closely. In addition to their mentors, most institutions have a post-doctoral professional development program. --A list of national and international conferences in which NoroCORE collaborators and their students/staff presented during project year 5 is provided below. The Collaborative had representation at many other regional and local meetings not listed here. American Society for Virology Meeting (ASV) annual meeting, London, Ontario, CA, July11-15, 2015. Institute for Food Technologists annual meeting, Chicago, IL, July 11-14, 2015. International Association for Food Protection (IAFP) annual meeting, Portland, OR, July 25-28, 2015. International Conference on Emerging Infectious Diseases, Atlanta, GA, August 24-26, 2015. Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC) annual meeting, San Diego, CA, September 17-21, 2015 IDWeek 2015, San Diego, CA, October 7-11, 2015. Interstate Shellfish Sanitation Conference (ISSC) annual meeting in Salt Lake City, UT, October 24-29, 2015 American Institute of Chemical Engineers annual meeting, Salt Lake City, UT, November 8-13, 2015. Integrated Foodborne Outbreak Response and Management (InFORM) meeting, Phoenix, AZ, November 17-20, 2015. Society for Risk Analysis annual meeting, Arlington, VA, December 6-10, 2015. 18th International Conference on Emerging Infectious Diseases (EID), Bethesda, MD, January 11-12, 2016. UK Food Safety Authority-European Food Safety Authority Foodborne Viruses Workshop, London, UK, February 22-25, 2016. American Chemical Society annual meeting, San Diego, CA, March 10-15, 2016. Noro2016, Lubeck, Germany, March 17-19, 2016. Foundation Merieux annual meeting, Annecy, France, March 21-23, 2016. Food Safety Summit, Rosemont, IL, May 9-11, 2016. International Association for Food Protection European Food Safety Symposium, Athens, Greece, May 11-13, 2016. --The NoroCORE Food Virology Literature database continues to be updated (>2,200 entries) and the reagent and protocol program is quite active (over 20 exchanges in year 5). NoroCORE continues to increase its Internet presence by website and social media, and 29 blog posts were produced in year 5. --Three paid, research-based summer internships were provided to undergraduates from historically under-represented groups in summer, 2015. These were hosted by investigators from Emory, Ohio State University, and Clemson. --Four graduate fellowships were awarded in year 5, with the students representing the following institutions: University of Georgia, Georgia State University, Emory, and NCSU. One of these fellows belongs to a historically under-represented group. --The food virology graduate curriculum and supporting animations continues to move forward. How have the results been disseminated to communities of interest?Results have been disseminated using traditional mechanisms including (1) publications (peer reviewed research publications, conference proceedings, book chapters, and articles in the scientific and popular press); (2) presentations at scientific and professional meetings (poster and oral); fact sheets, videos, webinars, and PowerPoint presentations; website and blogs; (3) NoroCORE newsletters; (4) the NoroCORE booth at professional meetings; and (5) in-person and web-based stakeholder meetings. We have an active website and significant social media efforts. See section on Target Audiences and Efforts for details. What do you plan to do during the next reporting period to accomplish the goals?A full description of next year's activities is provided in the no-cost extension document that was filed in December 2015. There are no changes.

Impacts
What was accomplished under these goals? The Molecular Virology Core: Investigators at Baylor College of Medicine have made substantial progress on a new cultivation system for human norovirus (NoV). This system involves infection of human intestinal cell cultures, banks of which have been frozen and recultured for over two years. Stool filtrates containing various human NoV strains have been used to infect these cultures and the viruses have demonstrated productive replication. The system has been replicated successfully in three independent laboratories. This work is highly significant as the most important limiting factor for human NoV research has been the absence of an in vitro cultivation system. Using a next generation sequencing protocol and an automated pipeline, the complete genomes of 57 human NoV and 30 sapovirus strains were sequenced. Initial analysis of more than 200 GII.4 complete capsid sequences corresponding to U.S. human NoV outbreaks from 2009-2016 is in progress. These data will be used develop models to predict evolution and strain emergence. Detection Core: This team has created various types of synthetic ligands (i.e., monoclonal and single chain antibodies, synbodies, peptides, nucleic acid aptamers, and synthetic glycans) that have high affinity and broad reactivity for variety of human NoV virus-like particles (VLPs). They also bind virus in stool samples derived from outbreaks and have been used for concentrating and purifying virus from artificially contaminated food. Proof-of-concept that graphene oxide can be used for human NoV adsorption and elution was demonstrated, with recovery efficiencies of 80-90% as applied to 25 ml samples of artificially contaminated produce wash water. Two general approaches are being compared to discriminate human NoV infectivity status (based on capsid integrity) using RT-qPCR amplification, i.e., receptor binding assays and RNase pre-treatment. Nucleic acid aptamers were found to perform similarly to synthetic histoblood group antigens (HBGAs) and antibodies in receptor binding assays. However, in comparative studies (receptor binding, RNase pre-treatment, protein gel electrophoresis, and electron microscopy), the receptor binding assays were extremely sensitive to the antiviral effects of representative physical and chemical disinfection methods. This suggests that receptor binding may underestimate virus infectivity status. The low-density DNA microarray previously reported is being used in field samples for detection and genotyping of human NoV and hepatitis A virus (HAV). Epidemiology and Risk Analysis Core: A first-generation agent-based quantitative risk model (NoroOPTIMAL) has been developed, which focuses on transmission of NoV in elder care facilities. Prototype software was uploaded to a web server and the model will be Beta tested in year 6. A second model that addresses transmission of human NoV in food service will also be completed this year. Supporting data was produced for these models, including estimates of virus concentration in emesis (>10^5 genome copies/ml) and degree virus aerosolization during projectile vomiting (<0.1% which corresponds to thousands of particles). Over 2,000 serum samples from the NHANES serum bank have been tested against seven human NoV VLPs. A preliminary analysis found that most samples (82.8%) were seropositive to at least one VLP, and 4.9% of samples were seropositive against all seven VLPs. Two epidemiological attribution models were also completed. The first uses epidemiologic and clinical criteria for ascribing NoV etiology in the absence of laboratory confirmation. The second will be used for assessing food service worker contributions to NoV transmission and evaluation of the impact of worker interventions (such as exclusion of ill workers or vaccination) on disease burden. Prevention and Control Core: High pressure processing (HPP) pulsed light (PL), and high power ultrasound (HPU) were investigated in year 5. In artificially contaminated oysters and fresh berries, the efficacy of HPP on inactivation of NoV surrogates was highest (3-4 log) at combinations of higher pressure (350-400 MPa) and lower temperature (<4 C), with some matrix effects. For decontamination of food contact surfaces and berries, PL showed efficacy (3 log inactivation or more) when treatment was close to the light source and for over 1 min. HPU provided additional value (0.5-1 log) in removal of virus from Romaine lettuce when used in conjunction with surface disinfectants. The Institute for Food Safety and Health (IFSH) team continues to work with commercial entities to further evaluate and apply these technologies. Several groups worked on compounds for use as components of novel anti-noroviral liquid disinfectants (e.g., electrolyzed water, chlorine dioxide, products containing silver ions or hydrogen peroxide). Data vary by product and application method, but in general, over 4 log inactivation of human NoV on surfaces was achieved in 5-30 min at maximum recommended concentrations. Addition of soil load significantly reduced efficacy. Nanotechnology-based approaches are also being investigated. A combination of titanium dioxide nanoparticles bound to stainless steel surfaces and exposed to UV-A light demonstrated over 5 log inactivation of surrogate NoV infectivity at UV-A dose of 8100 mJ/cm^2; slightly higher doses were required to inactivation of HAV. Carbon dots and Au-CuS core-shell nanoparticles were screened for inactivation of VLPs with varying degrees of success. Relative to copper, investigators showed that the Cu(I) ion has much greater anti-noroviral efficacy (lower concentration and shorter contact time) than the Cu(II) ion. As little as 5 min were required to induce at least 4 log reduction in Tulane virus and full reduction in HBGA-VLP binding at 0.1 mM and 0.01 mM Cu(I) ions, respectively. Nanoparticle loading of copper ions was demonstrated. Extension and Outreach Core: Sample collection (n=5,500) for environmental monitoring studies (public and healthcare environments) was completed and all samples screened. Editable model guidelines that focus on vomit and fecal matter cleanup for the retail and institutional food sectors have been developed and vetted by relevant industries. These are largely designed for use by small food service establishments. Curriculum materials on enteric viruses to be included in the NSSP/ISSC National Shellfish Harvester and Dealer Training Program were completed. The ISSC has also updated their educational DVD on overboard waste dumping and pump stations, and are in the process of identifying how best to disseminate educational information to recreational boat owners. Other extension and outreach efforts are reported above. Capacity Building Core: Efforts in reagent and information exchange, student training, and fostering communications amongst the NoroCORE team and with stakeholders are described elsewhere in the report. In year 5, three discretionary funding proposals were awarded to address the following emerging topics: (1) production of an online predictive tool to investigate human NoV mitigation alternatives for the food service industry; (2) development of a participatory human NoV surveillance platform (new subcontract to NYU); and (3) transfer of culture model to collaborative institutions and proof-of-concept for its use in food and environmental virology.

Publications

  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Hall, A.J. Predictable patterns of winter vomiting: Using time series regression models and big data to estimate the US norovirus burden. Internation Association for Food Protection, Portland, Oregon, July 25-28, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Kniel, K.E. Indicators for Viral Foodborne Pathogens: Get Your Coliforms out of Here. International Association of Food Protection Annual Meeting, Portland, OR, July 25-28, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Atmar, R.L., and O'Ryan, Miguel Norovirus Vaccines - Meet the Experts. ICAAC 2015, San Diego, CA, September 21, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Jaykus, L. Detection of Norovirus in food and environmental samples: The poster child for sample preparation. Knowledge Foundation Rapid Detection in Food Safety, Bethesda, MD. June 22-23, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Atmar, R.L. Norovirus. IDWeek 2015, San Diego, CA, October 07, 2015 - October 11, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Jaykus, L. Norovirus: A near perfect pathogen. North Carolina Public Health Laboratories Lunch and Learn Session, Raleigh, NC. June 11, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Jaykus, L. Recent insights on norovirus: Detection, epidemiology, and control. American Frozen Foods Institute Webinar, September 17, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Jaykus, L. Norovirus detection in food and environmental samples: Where do we stand today? Annual meeting of the Association for Official Analytical Chemists (AOAC), Los Angeles, CA. September 27-30, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Atmar, R.L. Immune Response and Correlates of Protection from Norovirus: Lessons from Challenge Studies and Clinical Trials. Correlates of Enteric Vaccine-Induced Protection. Fondation Merieux, Annecy, France, March 21, 2016 - March 23, 2016.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Atmar, R.L. Norovirus Infections: Beyond Safety and Dose Finding. Workshop on Controlled Human Infection Models (CHIM) for Malaria and Other Infectious Diseases, Leiden, Netherlands, May 04, 2016 - May 06, 2016.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Beaulieu, S.M. Core 3: Epidemiology and Risk Assessment Quantitative Risk Model NorOPTIMAL Norovirus On-line Predictive Tool to Investigate Mitigation ALternatives. NoroCORE Full Stakeholder Meeting, Arlington, VA, April 13, 2016 - April 15, 2016.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Hall, A.J. Norovirus epidemiology and food safety. Food Safety Summit, Rosemont, IL, May 11, 2016.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Lee, A., Zuber, S., and Manual, L. Balancing food quality and virus inactivation for sensitive foods (Symposium). IAFP European Food Safety Symposium 2016, Athens, Greece, May 11, 2016 - May 13, 2016.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Mertens, B.S., Moore, M.D., Jaykus, L.A., and Velev, O.D. Rational development of safe and efficient Norovirus disinfectants with ionic copper. NoroCORE Full Collaborators and Stakeholders Meeting, Washington, DC, April 15, 2016.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Moe, C.L. Core 3: Endemic Disease Studies Update. NoroCORE Full Collaborative and Stakeholders' Meeting, Crystal City, VA, April 14, 2016.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Velev, O.D. Scalable Liquid-Based Manufacturing of New Classes of Particles with Special Shape and Enhanced Functionality. Unilever Research, Unilever Colsworth Research Center, UK, June 18, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Velev, O.D., and Mertens, B.S. Characterization of Norovirus colloidal interactions as means of controlling virus stability and infectivity. 251st ACS National Meeting, San Diego, CA, March 10, 2016 - March 15, 2016.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Hall, A.J. Active surveillance for medically-attended acute gastroenteritis (MAAGE) and norovirus infection in a US managed care population. Vaccines for Enteric Diseases, Edinburgh, Scotland, July 08, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Shanker, S., Czako, R., Sapparapu, G., Alvarado, G., Sankaran, B., Viskovska, M., Atmar, R.L., Crowe, J.E. Jr., Estes, M.K., and Prasad, B.V.V. Structural analysis of human neutralizing monoclonal antibody 5I2 complex with norovirus P domain reveals mechanism of neutralization. American Society for Virology Meeting (ASV 2015), London, Ontario, Canada, July 11-15, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Mertens, B.S., Moore, M., Jaykus, L.A., and Velev, O.D. Characterization and Control of Norovirus Interactions and Their Impact on Virus Stability and Infectivity. European Colloids and Interfaces Society 2015 Meeting, Bordeaux, France, September 08, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Fabiszewski De Aceituno, A., Newman, K., Jaykus, L.A., and Leon, J.S. Norovirus Transmission during Produce Harvest and Packing: A Quantitative Microbial Risk Assessment Model Approach. International Association for Food Protection 2015 Annual Meeting, Portland, OR, July 25-28, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Estes, M.K. Human intestinal enteroids. 18th International Conference on Emerging Infectious Diseases (EID), Bethesda, MD, January 11, 2016 - January 12, 2016.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Estes, M.K. Cultivation of human norovirus. The U.S.-Japan Cooperative Medical Sciences Program (Viral Diseases Panel Meeting, Bethesda, MD, January 13, 2016 - January 14, 2016.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Overbey, K., Seymour, N., Bradshaw, E., Jaykus, L.A., and Chapman, B. Working Knowledge and Communication Practices of Public Health Officials in Response to Norovirus Outbreaks in Schools. International Association for Food Protection 2015 Annual Meeting, Portland, OR, July 25-28, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Seymour, N., Bradshaw, E., Overbey, K., Jaykus, L.A., and Chapman, B. Evaluating the Evidence-base of Outbreak Management and Clean-up Guidelines Available to Schools Experiencing Norovirus Outbreaks. International Association for Food Protection 2015 Annual Meeting, Portland, OR, July 25-28, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Beaulieu, S.M., Mokhtari, A., Anderson, M., and Jaykus, LA NorOPTIMAL- An Agent-based Model to Identify Cost-Effective Control Measures for Human Norovirus in Long-term Care Facilities. Society for Risk Analysis, Arlington, VA, December 09, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Kang, W., and Cannon, J.L.. 2015. A Novel Membrane-Based Electro-Separation (MBES) Method for Sample Clean-Up and Norovirus Concentration . International Association for Food Protection, Portland, OR, July 25-28, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Moyer, M., and Yang, L. Effect of Polymer Functionalized Carbon Dots on Norovirus Virus-like Particles (VLPs) . NCCU Graduate School Research Symposium, North Carolina Central University, Durham, NC, April 16, 2016.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Mertens, B.S., Moore, M.D., Jaykus, L.A., and Velev, O.D. Characterization and control of Norovirus interactions and their impact on virus stability and infectivity. Annual Triangle Soft Matter Workshop, Duke University, Durham, NC, May 09, 2016.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Shanker, S., Moreno, R., Czako, R., Sapparapu, G., Alvarado, G., Vusjivsjam N,, Sankaran, B., Atmar, R.L., Crowe, J.E., Jr., Estes, M.K., and Venkataram Prasad, B.V. Structure of a Human Norovirus in Complex with a Neutralizing Ig A Antibody Reveals its Mechanism of Neutralization. Noro2016, Lubeck, Germany, March 17, 2016 - March 19, 2016.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Anderson, BM, Kotwal, G, and Cannon, J.L.. 2015. Efficacy of Natural Antimicrobials on Norovirus and Hepatitis A Virus.. International Association for Food Protection, Portland, OR, July 25-28, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Buckley, D., Jiang, X., and Fraser, A. Developing Methods for Efficient Norovirus Recovery from Carpets. International Association of Food Protection, Portland, Oregon, July 25-28, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Handy, E. , Reynnells, R., Callahan, M.T., Roberts, C., Markland, S., Kniel, K., and Sharma, M. Survival of Escherchia coli O157:H7, Salmonella Typhimurium, Murine Norovirus, and Tulane Virus on Foliar Surfaces of Spinach Plants. International Association of Food Protection Annual Meeting, Portland, OR, July 25-28, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Markland, S., Craighead, S., and Kniel, K. Plant-microbe Interactions Associated with Norovirus and Leafy Greens. International Association of Food Protection Annual Meeting, Portland, OR, July 25-28, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Shearer, A.E.H., Castaneda Saldana, R., Pantuliano, P.E., and Kniel, K.E. Effect of Zero-valent Iron on Tulane Virus and Murine Norovirus. International Association of Food Protection Annual Meeting, Portland, OR, July 25-28, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Wang, Q., and Kniel, K.E. Survival and Transfer of Murine Norovirus within a Hydroponic System during Kale and Mustard Microgreen Harvesting. International Association of Food Protection Annual Meeting, Portland, OR, July 25-28, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Kniel, K.E. Bacterial and Viral Uptake in Hydroponically Grown Kale and Mustard Microgreens. Institute for Food Technologists Annual Meeting, 2015, Chicago, IL, July 11, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Barclay, L., Wikswo, M.E., Gregoricus, N., Hall, A.J., and Vinje, J. Emergence of norovirus GI.3 outbreaks in the United States, 2013-2014. International Conference on Emerging Infectious Diseases, Atlanta, GA, August 24-26, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Shioda, K., Kambhampati, A., Hall, A.J., and Lopman, B.A. Global age distribution of pediatric norovirus cases. International Conference on Emerging Infectious Diseases, Atlanta, GA, August 24, 2015 - August 26, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Kambhampati, A., Shioda, K., Sharp, D., and Hall, A.J. Assessment of food safety regulations for norovirus prevention: A state by state analysis. International Conference on Emerging Infectious Diseases, Atlanta, GA, August 24-26, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Wikswo, M.E., Barclay, L., DeSalvo, T., Davis, T., Salehi, E., Brandt, E., Saupe, A.M., Cebelinski, E., Garman, K., Woron, A., Williamson, K., Biggs, C., Vinje, J., and Hall, A.J. NoroSTAT: Enhanced norovirus outbreaks surveillance network. International Conference on Emerging Infectious Diseases, Atlanta, GA, August 24-26, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Coatsworth, A.M., Halasa, N., Hall, A., Garman, K., Constantine-Renna, L., Chappell, J., Wikswo, M., Payne, D., and Dunn, J. Sporadic norovirus surveillance and outbreak trends, Tennessee, 2012-2014. International Conference on Emerging Infectious Diseases, Atlanta, GA, August 24-26, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Manikonda, K., Gress, B., Wikswo, M., Roberts, V., Hall, A., Wade, D., Yoder, J., and Gould, L. Implementing automated reporting of outbreak data to the National Outbreak Reporting System (NORS). International Conference on Emerging Infectious Diseases, Atlanta, GA, August 24-26, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Jayasekara, L., Leone, C., Sharp, J., and Fraser, A. Environmental Sanitation in Food Preparation Areas in Long-term Care Facilities in South Carolina. International Association of Food Protection, Portland, Oregon, July 25-28, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Escudero-Abarca, B. and Jaykus, L.A. Use of Graphene Oxide for Concentration of Human Norovirus. International Association for Food Protection 2015 Annual Meeting, Portland, OR, July 25-28, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Tang, C., Leone, C., Dharmasena, M., Sharp, J., Jiang, X., and Fraser, A. Prevalence of Human Noroviruses in Commercial Retail Food and Foodservice Establishments without a Recently Reported Outbreak of Acute Gastroenteritis. International Association for Food Protection, Portland, Oregon, July 25-28, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Overbey, K., Seymour, N., Bradshaw, E., Jaykus, L.A., and Chapman, B. A Review of School-linked Norovirus Outbreaks: Lessons Learned. International Association for Food Protection 2015 Annual Meeting, Portland, OR, July 25-28, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Baugher, J., Simmons, O., and Jaykus, L.A. Binding Dynamics of Human Norovirus to Berries and Berry-associated Microflora. International Association for Food Protection 2015 Annual Meeting, Portland, OR, July 25-28, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Moore, M., and Jaykus, L.A. Evaluation of a Rapid Isothermal Amplification Method for the Direct Detection of Human Norovirus in Complex Samples. International Association for Food Protection 2015 Annual Meeting, Portland, OR, July 25-28, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Almand, E., Goulter, R., and Jaykus, L.A. Binding of Human Norovirus to Naturally Occurring Human Fecal Bacterial Isolates. International Association for Food Protection 2015 Annual Meeting, Portland, OR, July 25-28, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Manuel, C., Jaykus, L.A., Williams, L., Khatiwada, J., Quinoy, M., and Brown, R. Efficacy of a Portable Aerosolized Hydrogen Peroxide Delivery Method for Inactivating Human Norovirus and Its Surrogates. International Association for Food Protection 2015 Annual Meeting, Portland, OR, July 25-28, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Anderson, M., Mokhtari. A., Beaulieu, S.M., and Jaykus, LA. Data Development to Support Development of Cost-Effective Control Strategies for Human Norovirus in a Long-Term Care Facility. NoroCORE Full Stakeholder Meeting, Arlington, VA, April 13, 2016 - April 15, 2016.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Fox, R.J., Mertens, B.S., and Velev, O.D. Deactivation of Norovirus using Copper-Infused Lignin Nanoparticles. American Institute of Chemical Engineers National Meeting, Salt Lake City, UT, November 09, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Gleason, J. NMSU Visual Media for NoroCORE Education and Outreach. NoroCORE Full Collaborative and Stakeholders Meeting , Washington DC, April 13, 2016 - April 15, 2016.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Kirby, A.E., Barton, J., Sizemore, M., Anderson, E., Vinje, J., and Moe, C.L. Norovirus Seroprevalence in NHANES Specimens From the United States in 1999-2000 and 2003-2004. NoroCORE Full Collaborative and Stakeholders' Meeting, Crystal City, VA, April 13, 2016 - April 15, 2016.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Mertens, B.S., Moore, M., Jaykus, L.A., and Velev, O.D. Characterization and control of Norovirus interactions and their impact on virus stability and infectivity. Schoenborn Graduate Research Symposium, North Carolina State University, Raleigh, NC, January 25, 2016.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Mertens, B.S., Moore, M.D., Jaykus, L.A., and Velev, O.D. Rational development of safe and efficient Norovirus disinfectants with ionic copper. NoroCORE Full Collaborators and Stakeholders Meeting, Washington, DC, April 14, 2016 - April 15, 2016.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Mertens, B.S., Moore, M.D., Jaykus, L., and Velev, O.D. Characterization and control of Norovirus interactions and their impact on virus stability and infectivity. Annual Triangle Soft Matter Workshop, Duke University, Durham, NC, May 09, 2016.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Mertens, B.S., and Velev, O.D. Characterization and control of surfactant-mediated Norovirus interactions. NoroCORE Full Collaborators and Stakeholders Meeting, Washington, DC, April 14, 2016 - April 15, 2016.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Mokhtari, A., Beaulieu, S.M., Anderson, M., Kelly, R., Houghteling,W, Swanson, S., and Jaykus, LA. Agent-based Modeling of a Long-Term Care Facility (LTCF): Developing Cost-Effective Control Strategies for Human Norovirus. NoroCORE Full Stakeholder Meeting, Arlington, VA, April 13, 2016 - April 15, 2016.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Moyer, M. Dong, X., Edmondson, R., Gregory E. LeCroy, F.Y., Sun, Y.P, and Yang, L. Effect of polymer functionalized carbon dots on norovirus virus-like particles (VLPs) . 2016 Annual Meeting of the Biological Engineering Engineering (IBE), Greenville, SC, April 07, 2016 - April 09, 2016.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Williams, L.L., and Khatiwada, J.R. Efficacy of crude extract from select plants against surrogates of human norovirus. Annual Norocore meeting, Crystal City, VA, April 13, 2016 - April 15, 2016.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Janes, M.E.., Montazeri, N., and Maite, M. 2015. Norovirus and Oysters in Louisiana. Louisiana Agriculture, 58, No. 4:12-13. Fall 2015.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Evans, H., Chao, M., Finney, M., Leone, C., and Fraser, A. 2016. Content Analysis of Web-based Norovirus Education Materials Targeting Consumers: An Assessment of Alignment and Readability. Food Control, 65:32-36.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Leone, C., Jayasekara, L., Sharp, J., and Fraser, A.M. 2015. Prevention and control practices for human noroviruses in long-term care facilities in South Carolina. American Journal of Infection Control, 43:1276-80.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Leone, C., Jaykus, L.A., Cates, S., and Fraser, A. 2016. A Review of State Licensing Regulations to Determine Compliance with Evidence-based Practices to Prevent Human Norovirus Infections in Child-Care Centers. Public Health Reports, 131(3):449-460.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Xiuli Dong, and Yang, L. Evaluation of a label-free interferometric biosensor for rapid detection of norovirus using virus like particles . 2016 Annual Meeting of the Biological Engineering Engineering (IBE), Greenville, SC, April 07, 2016 - April 09, 2016.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Evans, H., Getty, M., Finney, M., Leone, C., and Fraser, A. 2016. Accuracy and Readability of Information about Human Noroviruses in Food Safety Education Materials Targeting Consumers. Food Protection Trends, 36(2):133-139.
  • Type: Other Status: Published Year Published: 2015 Citation: Gleason, J., and Chamberlin, B. Communicating Findings & Strategies for Food Safety. Enhancement of Microbial Food Safety by Risk Analysis - Multistate S1056 Food Safety Conference, Narragansett, RI, October 06, 2015 - October 07, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Bradshaw, E.S. and Bradshaw, J.M. The Nightmare Buffet: An introduction to epidemiological practices for general biology students. Association of Southeastern Biologists Meeting, Concord, NC, April 2, 2016.
  • Type: Other Status: Other Year Published: 2016 Citation: Jaykus, L. Food Virology: The Past, Present, and Future. Invited presentation, University of Massachusetts, Amherst, MA, February 5, 2016.
  • Type: Other Status: Other Year Published: 2016 Citation: Jaykus, L. Norovirus and Hepatitis A - Control options for viruses in the food chain. Invited presentation, FSA-EFSA UK Food Safety Authority-European Food Safety Authority Foodborne Viruses Workshop, London, UK, February 22-25, 2016.
  • Type: Other Status: Other Year Published: 2016 Citation: Jaykus, L. Norovirus and Food Safety: A Future Role for Testing? Invited presentation, Neogen Scientific Review Committee, East Lansing, MI, April 5, 2016.
  • Type: Other Status: Other Year Published: 2016 Citation: Jaykus, L. Lessons Learned from Managing an Interdisciplinary, Multi-Institutional Collaborative: The NoroCORE Project. Invited presentation, Johnson C. Smith University, Charlotte, NC, May 17, 2016
  • Type: Other Status: Other Year Published: 2016 Citation: Jaykus, L. Five Years of Food Virology Research: The NoroCORE Project. Invited presentation, FDA Center for Food Safety and Applied Nutrition (CFSAN), May 25, 2016.
  • Type: Book Chapters Status: Published Year Published: 2015 Citation: Fraser, A.M., and Simmons, O. 2015. Food Safety Education: Training Farm Workers in the U.S. Fresh Produce Sector. In: Bhat, R. (eds.), Sustainability Challenges in the Agrofood Sector, 1st. Wiley & Sons, Ltd., London. Chapter 1, p. 16.
  • Type: Journal Articles Status: Accepted Year Published: 2015 Citation: Aliabadi, N., Lopman, B.A., Parashar, U.D., and Hall, A.J. 2015. Progress toward norovirus vaccines: Considerations for further development and implementation in potential target populations. Expert Reviews in Vaccines, 14(9): 1241-1253.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Williams, L.L., Iloghalu, U., Khatiwada, P., and Khatiwada, J. 2015. Phytochemicals: Natural remedies for emerging viral infection. Medicinal and Aromatic Plants, 4:5. DOI:10.4172/2167-0412.1000213
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Graaf de, M., Beek van, J., Vennema, H., Podkolzin, A.T., Hewitt, J., Bucardo, F., Templeton, K., Mans, J., Nordgren, J., Reuter, G., Lynch, M., Rasmussen, L.D., Iritani, N., Chan, M.C., Martella, V., Ambert-Balay, K., Vinje, J., White, P.A., and Koopmans, M.P. 2015. Emergence of a novel GII.17 norovirus - End of the GII.4 era?. Eurosurveillance, 20(26). DOI: http://dx.doi.org/10.2807/1560-7917.ES2015.20.26.21178
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Yeargin, T., Fraser, A.M., Huang, G., and Jiang, X. 2015. Recovery and disinfection of two human norovirus surrogates, feline Calicivirus and murine norovirus, from hard non-porous and soft porous surfaces. J. of Food Prot., 78(10): 1842-1850.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Park, G.W., Lee, D., Treffiletti, A., Hrsak, M., Shugart, J., and Vinj�, J. 2015. Evaluation of a new environmental sampling protocol for detection of human norovirus on inanimate surfaces. Appl. Environ. Microbiol., 81(17):5987-92.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Hill, V.R., Narayanan, J., Gallen, R.R., Ferdinand, K.L., Cromeans, T., and Vinj�, J. 2015. Development of a nucleic acid extraction procedure for simultaneous recovery of DNA and RNA from diverse microbes in water. Pathogens, 4:335-354.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Shioda, K., Kambhampati, A., Hall, A.J., and Lopman, B.A. 2015. Global age distribution of pediatric norovirus cases. Vaccine, 33(33): 4065-4068.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Montazeri, N., Goettert, D., Achberger, E.C., Johnson, C.N., Prinyawiwatkul, W., and Janes, M.E. 2015. Pathogenic enteric viruses and microbial indicators during secondary treatment of municipal wastewater. Appl. Environ. Microbiol., 81:6436-45.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Afolayan, O.T., Webb, C.C., and Cannon, J.L. 2015. Evaluation of a porcine gastric mucin and RNase A assay for the discrimination of infectious and non-infectious GI.1 and GII.4 norovirus following thermal, ethanol, or levulinic acid plus sodium dodecyl sulfate treatments. Food and Environmental Virology, 8(1):70-8. DOI: 0.1007/s12560-015-9219-z.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Hagstrom, A.E., Garvey, G., Paterson, A.S., Dhamane, S., Adhikari, M., Estes, M.K., Strych, U., Kourentzi, K., Atmar, R.L., and Willson, R.C. 2015. Sensitive detection of norovirus using phage nanoparticle reporters in lateral-flow assay. PLoS One, 10(5):e0126571. DOI: 10.1371/journal.pone.0126571.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Atmar, R.L., Bernstein, D.I., Lyon, G.M., Treanor, J.J., Al-Ibrahim, M.S., Graham, D.Y., Vinj�, J., Jiang, X., Gregoricus, N., Frenck, R.W., Moe, C.L., Chen, W.H., Ferreira, J., Barrett, J., Opekun, A.R., Estes, M.K., Borkowski, A., Baehner, F., Goodwin, R., Edmonds, A., and Mendelman, P.M. 2015. Serological correlates of protection against a GII.4 norovirus. J. Infect. Dis., 22(8):923-929. DOI: 10.1128/CVI.00196-15.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Manuel, C.S., M. D. Moore, and L.A. Jaykus. 2015. Destruction of the capsid and genome of GII.4 human norovirus occurs during exposure to metal alloys containing copper. Appl. Environ. Microbiol., 81(15):4940-4946.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Bartsch, S.M., Lopman, B., Hall, A.J., Ozawa, S., and Lee, B.Y. 2016. Global economic burden of norovirus gastroenteritis. PLoS One, 11(4):e0151219.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Broglie, J.J., Alston, B., Yang, C., Ma, L., Adcock, A.F., Chen, W., and Yang, L. 2015. Antiviral activity of gold/copper sulfide core/shell nanoparticles against human norovirus virus-like particles. PlosOne, 10(10):e0141050. DOI: 10.1371/journal.pone.0141050.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Newman, K., Moe, C.L., Kirby, A.E., Flanders, D., Parkos, C., and Leon, J. 2015. Human norovirus infection and the acute serum cytokine response. Clin. and Experimental Immun., Epub. DOI: 10.1111/cei.12681.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Knight, A., J. Haines. A Stals, D. Li, M. Uyttendaele, A. Knight, and L. Jaykus. 2015. A systematic review of human norovirus survival reveals a greater persistence of human norovirus RT-qPCR signals compared to those of cultivable surrogate viruses. Int. J. Food Microbiol., 216:40-49.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Tung-Thompson, G. D.A. Libera, K.L. Koch, F.L. de los Reyes, and L.A. Jaykus. 2015. Aerosolization of a human norovirus surrogate, bacteriophage MS2, during simulated vomiting. PLoS One, Aug 19;10(8):e0134277. doi: 10.1371/journal.pone.0134277.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Moore, M.D., B.I. Escudero-Abarca, S.-H. Suh, and L. Jaykus. 2015. Generation and characterization of nucleic acid aptamers targeting the capsid P domain of a human norovirus GII.4 strain. J. Biotechnol., 10;209:41-9. DOI: 10.1016/j.jbiotec.2015.06.389.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Chaifetz, A. and Chapman, B. 2015. Evaluating North Carolina food pantry food safety-related operating procedures. J. of Food Prot., 78(11):2033-2042. DOI: 10.4315/0362-028X.JFP-15-084.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Chen, H., Hagstrom, A.E., Kim, J., Garvey, G., Paterson, A., Ruiz-Ruiz, F., Baja, B., Strych, U., Rito-Palomares, M., Kourentzi, K., Conrad, J.C., Atmar, R.L., and Willson, R.C. 2016. Flotation immunoassay: Masking the signal from free reporters in sandwich immunoassays. Sci. Rep., 6:24297. DOI: 10.1038/srep24297.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Costantini ,V.P., Cooper, E.M., Hardaker, H.L., Lee, L.E., Bierhoff, M., Biggs, C., Cieslak, P.R., Hall, A.J., and Vinj�, J. 2015. Epidemiologic, virologic, and host genetic factors of norovirus outbreaks in long-term care facilities. Clinical Infectious Diseases, 1:1-10. DOI: 10.1093/cid/civ747.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Gonzalez, M.D., Langley, L.C., Buchan, B.W., Faron, M.L., Maier, M., Templeton, K., Walker, K., Popowitch, E.B., Miller, M.B., Rao, A., Liebert, U.G., Ledeboer, N.A., Vinj�, J., and Burnham, C.A. 2016. Multicenter evaluation of the Xpert norovirus assay for detection of norovirus. J. Clin. Microbiol., 54(1):142-7. DOI: 10.1128/JCM.02361-15.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Grytdal, S.P., Blake, E., DeBess, E., Lee, L., Blythe, D., Ryan, P., Biggs, C., Cameron, M., Schmidt, M., Parashar, U.D., and Hall, A.J. 2016. Incidence of norovirus and other viral pathogens that cause acute gastroenteritis (AGE) among Kaiser Permanente member populations in the United States, 2012-2013. PLoS One, 11(4):e0148395.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Hall, A.J., Glass, R.I., and Parashar, U.D. 2016. New insights into the global burden of noroviruses and opportunities for prevention. Expert Review of Vaccines, May:1-3. DOI: PMID: 27142965.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Hesse, S., Neill, F.H., Estes, M.K., Shanker, S., Prasad, B.V., and Ferreira, J. 2016. Serological responses to a norovirus nonstructural fusion protein after vaccination and infection. Clin. Vaccine Immunol., 23(2):181-183. DOI: 10.1128/CVI.00595-15.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Jones, M.K., Grau, K.R., Costantini, V., Kolawole, A.O., de Graaf, M., Freiden, P., Graves, C.L., Koopmans, M., Wallet, S.M., Tibbetts, S.A., Schultz-Cherry, S., Wobus, C.E., Vinj�, J., and Karst, S.M. 2015. Human norovirus culture in B cells. Nature Protocols, 12:1939-47. DOI: 10.1038/nprot.2015.121
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Leone, C.M., Tang, C., Sharp, J., Jiang, X., and Fraser, A. 2016. Presence of human noroviruses on bathroom surfaces: a review of the literature. International Journal of Environmental Health Research, 20:1-13.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Kang, W., and Cannon, J.L. 2015. A membrane-based electro-separation method (MBES) for sample clean-up and norovirus concentration. PLoS One, 10(10):na. DOI: 10.1371/journal.pone.0141484
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Kirby, A.E., Streby, A., and Moe, C.L. 2016. Vomiting as a symptom and transmission risk in norovirus illness: Evidence from human challenge studies. PLOS One, 11(4):e0143759. doi: 10.1371/journal.pone.0143759.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Kou, B., Huang, W., Neill, F.H., Palzkill, T., Estes, M.K., and Atmar, R.L. 2015. Norovirus antigen detection with a combination of monoclonal and single-chain antibodies. J. Clin. Microbiol., 53(12):3916-3918. DOI: 10.1128/JCM.02371-15.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Jayasekara, L., Leone, C.M., Sharp, J., and Fraser, A.M. 2015. Preventing and controlling human noroviruses in South Carolina long-term care facilities: An analysis of institutional policies and procedures. American Journal of Infection Control, 44(1): 24-29. DOI: 10.1016/j.ajic.2015.07.038.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Mertens, B.S., and Velev, O.D. 2015. Characterization and control of surfactant-mediated norovirus interactions. Soft Matter, 11:8621-8631. DOI: 10.1039/C5SM01778E.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Newman, K., Moe, C.L., Kirby, A.E., Flanders, D., Parkos, C., and Leon, J. 2016. Norovirus in symptomatic and asymptomatic individuals: cytokines and viral shedding. Clinical and Experimental Immunology, 184:347-357. DOI:10.1111/cei.12772.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Ng, T.F., Maga�a, L., Montmayeur, A., Lopez, M.R., Gregoricus, N., Oberste, M.S., and Vinj� J. 2016. Characterization of a Salivirus (Picornaviridae) from a diarrheal child. Genome Announc., 4(1):pii: e01751-15. DOI: 10.1128/genomeA.01751-15.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Ramani, S., Estes, M.K., and Atmar, R.L. 2016. Correlates of protection against norovirus infection and disease-Where are we now, where do we go?. PLoS Pathogens, 12(4):e1005334. DOI: 10.1371/journal.ppat.1005334.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Yeargin, T., Fraser, A.M., Huang, G., and Jiang, X. 2015. Recovery and disinfection of two human norovirus surrogates, feline Calicivirus and Murine norovirus, from hard non-porous and soft porous surfaces. J. of Food Prot., 78(10):1842-1850. DOI: 10.4315/0362-028X.JFP-14-515.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Yeargin, T., Buckley D., Fraser, A., and Jiang, X. 2016. The survival and inactivation of enteric viruses on soft surfaces. American Journal of Infection Control, [Epub] DOI: dx.doi.org/10.106/j.ajic.2016.03.018.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Yi, J., Wahl, K., Sederdahl, B., Jerris, R., Kraft, C., McCracken, C., Gillespie., S., Anderson, E., Kirby, A.E., Shane, A, and Moe, C.L. 2015. Molecular epidemiology of norovirus in children and the elderly in Atlanta, Georgia, United States. Journal of Medical Virology, Epub. DOI: 10.1002/jmv.24436.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Wang, Q., and Kniel, K.E. 2015. Survival and transfer of murine norovirus within a hydroponic system during kale and mustard microgreen harvesting. Applied and Environmental Microbiology, 82(2):705-713. DOI: 10.1128/AEM.02990-15.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Liu, L., Yemmireddy, K., Hung, Y.-C., and Cannon, J.L.. 2015. Investigation of food-borne virus disinfection by UV-A activated TiO2-coated surfaces. International Association for Food Protection - USDA Collaborators' Meeting, Portland, OR, July 25-28, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Hall, A.J., and Vinje, J. Norovirus sentinel testing and tracking network (NoroSTAT). Integrated Foodborne Outbreak Response and Management (InFORM), Phoenix, AZ, November 17, 2015 - November 20, 2015.


Progress 06/01/14 to 05/31/15

Outputs
Target Audience:Formalized extension and outreach activities are designed to improve understanding and expand the use of measures to reduce viral foodborne disease. Initially, six major stakeholder groups were identified: (1) fresh produce industry; (2) molluscan shellfish industry; (3) retail and institutional food sectors; (4) detection technologies; (5) the cleaning, sanitizing, and hygiene sector; and (6) food processing industries. In year 4, we added the cruise line industry and elementary schools as additional stakeholder groups. Three major audiences are targeted for communications programs: (1) food safety and public health professionals; (2) food industry professionals (food production, processing, retail, and foodservice); and (3) consumers. Students, both graduate and undergraduate, could also be considered stakeholders. A synopsis of year 4 efforts is provided below: -- NoroCORE exhibited at the annual meeting of the International Association for Food Protection (IAFP) in Indianapolis, IN August 2-6, 2014. Informational and promotional materials were distributed. NoroCORE team members also attended and presented to a number of professional development groups, the purpose of which was to raise awareness of food virology and NoroCORE activities, and to increase stakeholder involvement. A stakeholder reception, with about 50 attendees, was hosted on the evening before the IAFP opening session. --NoroCORE team members worked with various companies developing virus detection technologies, providing them recommendations and guidance for marketing, research, and development. --The comprehensive social media effort continues. In year 4, the following activities were undertaking: (1) a #findnorocore awareness contest was hosted at IAFP, 2014; (2) four creative informational campaigns were launched [i.e., two costumed norovirus soft plushies (for Halloween and March Madness); norovirus vs. influenza sticky notes; and a YouTube holiday video featuring The Twelve Days of Norovirus]; and (3) creation of a foldable paper model of the HuNoV capsid for educational purposes and distribution. Over 25 blog posts were produced on the website, including one for WHO World Health Day. --NoroCORE was represented at regional and national fresh produce safety and molluscan shellfish meetings. --NoroCORE co-sponsored and participated in an Interstate Shellfish Sanitation Conference (ISSC) informational meeting, the purpose of which was to review the data on usefulness of male specific coliphages (MSC) as an indicator for enteric viruses, particularly norovirus. The outcome of the meeting was expert panel consensus and recommendations supporting the formation of a work group to develop proposed language by the National Shellfish Sanitation Program (NSSP) for approved use of MSC in instances of suspected human sewage contamination of shellfish growing waters. --NoroCORE was represented (as part of expert panels) at two meetings sponsored by the Cruise Lines Industry Association (CLIA) (Orlando and Geneva, Switzerland) to review the evidence supporting anti-noroviral activity of emerging sanitizers and disinfectants. The output from these meetings is a comprehensive effort to evaluate the most promising technologies. -- Two NoroCORE newsletters were produced (released July and October, 2014), giving a total of four by the end of project year 4. --NoroCORE was represented at the following public health venues: (1) the Annual CaliciNet Users meeting (Dec, 2014); (2) the CDC/Gates Technical Expert Group Meeting: Global Burden ofNorovirusand Prospects for Vaccine Development (Feb, 2015). In addition, based on year 3 information provided to the CDC-FSMA Surveillance Working Group, NoroCORE team members participated in writing the 2014 annul report to the Secretary of HHS. --NoroCORE investigators delivered formal training to NC schoolteachers in the form of a "simulated" outbreak that can be used in the middle school classroom environment. --The content for the food virology graduate curriculum is now complete. NCSU and New Mexico State University Media Productions developed two 3-dimensional animations providing an orientation to HuNoV structure that will be used to support the curriculum. Changes/Problems:A new project evaluation team was identified and a contract established in year 4, replacing our previous evaluation team. Key personnel involved in the risk assessment activities have changed institutions, and the award for that work is in process of being moved to the new institution. What opportunities for training and professional development has the project provided?--There is extensive graduate student training associated with the USDA-NIFA Food Virology Collaborative. To date, over 30 graduate students have been, or are in training at the collaborating universities under the auspices of this project. About 10 post-doctoral research associates have been, or are being supported. Many of our collaborators also support undergraduates working on various NoroCORE-related projects. In all cases, students have assigned mentors with whom they work closely. In addition to their mentors, most institutions have a post-doctoral professional development program in which most of our post-docs participate. --A list of national and international conferences in which NoroCORE collaborators and their students/staff presented during project year 4 is provided below. The Collaborative had representation at many other regional and local meetings not listed here American Society for Microbiology Annual Meeting, Boston, MA, May 17-20, 2014. Association for Professionals in Infection Control and Epidemiology, Anaheim, CA, June 8, 2014. Institute of Food Technologists (IFT) Annual Meeting, New Orleans, LA, June 19-23, 2014. American Society for Virology Annual Meeting, Fort Collins, CO, June 21-25, 2014. Council for State and Territorial Epidemiologists Annual Conference, Nashville, TN, June 25, 2014. International Conference and Exhibition on Food Processing and Technology, Las Vegas, NV, July 21-23, 2014. International Life Sciences Institute (ILSI) North America Food, Nutrition and Safety Program mid-year meeting, Washington, D.C., July 23, 2014. International Association for Food Protection (IAFP) Annual Meeting, Indianapolis, IN, August 2-6, 2014. International Union of Food Science and Technology Biennial Meeting, Montreal, Quebec, Canada, August 20, 2014. International Society for Food and Environmental Virology Conference, Corfu, Greece, September 2-5, 2014. Interscience Conference on Antimicrobial Agents and Chemotherapy(ICAAC) 2014: Noroviruses in the 21st Century, Washington, DC, September 6-8, 2014. Canadian Institute of Public Health Inspectors, Edmonton, Alberta, September 25, 2014. Microal 2014, Iguazu Falls, Parana, Brazil, October 14-15, 2014. ID Week 2014, Philadelphia, PA, October 8-12, 2014. American Society of Tropical Medicine and Hygiene (ASTMH) Annual Meeting, New Orleans, LA, November 2-6, 2014. National Food Safety Education Conference, Arlington, VA, December 4-5, 2014. International Association for Food Protection (IAFP) European Food Safety Symposium, Cardiff, Wales, April 20-22, 2015. University of Georgia Center for Food Safety Annual Meeting, Atlanta, GA, March 4, 2015. Food Safety Summit, Baltimore, MD, April 28-30, 2015. --The NoroCORE Food Virology Literature database continues to be updated and the reagent and protocol exchange lists expanded.In year 4, the NoroCORE website was redesigned and the blog posts maintained (>20 for year 4). --Four paid, research-based summer internships were provided to undergraduates from historically under-represented groups in summer, 2014. These were hosted by investigators from UGA, Clemson, Emory, and NCSU. --Four graduate fellowships were awarded in year 4, with the students representing the following universities: Emory, UGA, Georgia State University, and NCSU. One of these fellows belongs to a historically under-represented group. --The food virology graduate curriculum and supporting animations described above are also relevant to this section. How have the results been disseminated to communities of interest?Results have been disseminated using traditional mechanisms including: publications (peer reviewed research publications, conference proceedings, book chapters, and articles in the scientific and popular press); presentations at scientific and professional meetings (poster and oral); fact sheets, videos, webinars, and PowerPoint presentations; website and blogs; NoroCORE newsletters; NoroCORE booth at professional meetings; and in-person and web-based stakeholder meetings. We have an active website and significant social media efforts. See section on Target Audiences and Efforts for details. What do you plan to do during the next reporting period to accomplish the goals?A full description of next year's activities is provided in the Year 4 renewal package. There are no changes.

Impacts
What was accomplished under these goals? The Molecular Virology Core: Investigators at Baylor College of Medicine produced small intestinal enteroids originating from isolated crypt cells derived from tissues of bariatric surgery patients. Investigators at The Ohio State University (OSU) were not able to demonstrate productive HuNoV infection in tissues and cells derived from challenged severe combined immunodeficient (SCID) gnotobiotic piglets, however they did demonstrate that the in vivo gnotobiotic pig model could be used to evaluate the efficacy of high pressure processing of virus-contaminated oysters. CDC scientists sequenced stool samples from outbreaks of unexplained etiology in an effort to better understand the role of enteric virus in such outbreaks. Full genome sequencing of 200 GII.4 HuNoV outbreak strains from the last decade has been completed and these data will form the basis for future models of strain evolution. Detection Core: This group continued to evaluate novel ligands for capture and detection of HuNoV. Synthetic ligands created or investigated included (1) monoclonal antibodies specific to regions of the HuNoV P domain; (2) peptides expressed on bacterial phage; (3) single chain antibodies; (4) synbodies; (5) nucleic acid aptamers; and (6) synthetic glycans. Most of these reagents have been screened for reactivity with a panel of virus-like particles (VLPs) and on stool samples derived from outbreaks; in a few cases, they have also been used to concentrate virus from artificially contaminated food. Some had broader reactivity than previous reagents, and efforts now focus on combining ligands to produce detection and concentration methods with improved sensitivity and specificity. Investigators at UGA are comparing the ISO 15216-1 (CEN) method to a more rapid variation of that method as applied to the recovery of hepatitis A virus (HAV) and GII.4 HuNoV from fresh and dried produce items. In comparing the behavior of candidate process control viruses (e.g., MS2, Tulane, FCV, Mengovirus) in virus extraction from food, NCSU scientists concluded that a commercial Mengovirus preparation provided the best recovery efficiency. Two general approaches are being compared to discriminate HuNoV infectivity status (based on capsid integrity) after RT-qPCR amplification, i.e., receptor binding assays and RNase pre-treatment. In comparative analyses, the approaches performed similarly when used to evaluate the efficacy of some inactivation methods (e.g., exposure to copper, heat) and others continue to be evaluated. The low density DNA microarray produced by USDA-ARS scientists to be used for detection and genotyping HuNoV and HAV was further refined and is being tested with field samples (environmental waters and fresh product). Presumptively positive results have been obtained. Epidemiology and Risk Analysis Core: The agent-based quantitative risk model for HuNoV transmission (NoroOPTIMAL) continues to be developed. In year 4, a comprehensive design document was produced. Activity-specific mathematical formulations were developed for the eldercare facility example and a list of model parameters and expected outputs was produced. Key contamination pathways (e.g., personal contacts, tactile events, exposure to aerosolized particles) were implemented and data collection has been initiated. Several members of the Collaborative published supporting data to be used for modeling release of virus during vomiting and virus transfer between surfaces and hands. Efforts to characterize endemic disease continued. Stool specimens and clinical data were collected by Emory and CDC scientists from several surveillance platforms, with a focus on pediatric and geriatric populations. Data analysis continues. Of the over 2,000 samples submitted for the NHANES seroprevalence study, all have been tested against six VLPs, with one more to be completed. A preliminary data analysis suggests that theseroprevalencetoHuNoVis lower than previously reported. Enhancements to state and national outbreak surveillance systems and CaliciNet continue, and data from real-time reporting in sentinel states (NoroSTAT) for outbreak characterization has been analyzed. All of these efforts will contribute to creation of attribution models in year 5. Prevention and Control Core: Several studies to determine the underlying prevalence of HuNoV contamination in public environments are underway; all told, over 5,500 samples will be tested and analyzed based on location and other risk factors. Produce-associated efforts (done at University of Delaware, OSU, UGA, and NCSU) focused on characterizing virus persistence and internalization, as well as plant-virus binding interactions. Overall, the body of evidence collected thus far suggests that HuNoV (or surrogate) internalization is relatively inefficient (<0.001% of input virus internalized) with the exception of hydroponically grown products. HuNoV and HAV were shown to be quite persistent (survived for weeks) on dried produce items. While HuNoV binds tenaciously to raspberries and strawberries (>90%), this binding did not appear to be mediated by HBGA-like moieties or native berry-associated microflora. Studies continue to elucidate virus-produce binding mechanisms. The efficacy of novel surface disinfection methods was also evaluated. For instance, collaborators at the Institute of Food Safety and Health (IFSH) reported that exposure of surfaces to high intensity pulsed light at a 10.8 cm distance resulted in reduction of the murine norovirus (MNV) surrogate by 2-3 log and 5-6 log after 20 sec and 50 sec exposures, respectively. UGA scientists found that natural antimicrobials [e.g., grape seed extract (GSE), pycogenol] used alone or in combination with surfactants produced 1-2.5 log inactivation of HuNoV and MNV, and may relevant as produce washes. NCSU demonstrated that alloy surfaces containing >70% copper were highly effective (>5 log inactivation) against HuNoV after 2 hour exposures. OSU showed that very high doses (>15 kGy) of e-beam radiation were necessary to eliminate (>6 log) MNV and Tulane virus (TV) on food. The IFSH team continues to work with manufacturers of high pressure and pulsed light technologies relative to commercialization. Extension and Outreach Core: Most of this work is reported above, with in-progress work described here. Editable model guidelines that focus on vomit and fecal matter clean-up for the retail and institutional sectors are being developed. The content for four web-based educational courses on foodborne viruses directed at food safety and public health professionals (train-the-trainer) has been collected, and an e-Learning platform is being designed. A content analysis of traditional food safety extension documents has been completed and is being used to guide development of supplementary information on foodborne viruses for addition to these documents. NoroCORE continues to be involved in curriculum development activities for national groups including the PSA and ISSC. Capacity Building Core: Efforts focus on reagent and information exchange, student training, and fostering communications amongst the group and with stakeholders. Those efforts are described elsewhere in the report. In year 4, five discretionary funding proposals were awarded to study the following emerging topics: (1) immunocompromised individuals as a reservoir for HuNoV strain emergence; (2) chlorine dioxide gas for surface decontamination of fresh produce; (3) magnetic nanoparticles for virus concentration and detection; and (4) Big Data to evaluate HuNoV transmission risk at retail. Additional funds were also awarded to further the previous synbody work.

Publications

  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Grove, S. F., Suriyanarayanan, A., Puli, B., Zhao, H., Li, M., Schaffner, D.W., and Lee, A. 2015. Norovirus cross-contamination during preparation of fresh produce. Inter J of Food Microbiol, 198 (2015): 43-49.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Vinj�, J. 2015. Advances in Laboratory Methods for Detection and Typing of Norovirus. J Clin Microbiol, Feb;53(2):373-81. doi: 10.1128/JCM.01535-14.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Pringle, K., Lopman, B., Vega, E., Vinj�, J., Parashar, U.D., and Hall, A.J. 2015. Noroviruses: Epidemiology, immunity, and prospects for prevention. Future Microbiol, 10: 53-67.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Predmore, A., Sanglay, G.C., DiCaprio, E., Li J, Uribe R.M., and Lee, K. 2015. Electron beam inactivation of Tulane virus on fresh produce, and mechanism of inactivation of human norovirus surrogates by electron beam irradiation. Inter J of Food Microbiol, 198: 28-36.
  • Type: Book Chapters Status: Published Year Published: 2014 Citation: Markland, S.M., D'Souza, D., and Kniel, K.E. 2014. Cases of public emetic events due to foodborne virus infections. In: J. Hoorfar (ed.), Global Safety of Fresh Produce, 1st Ed. Woodhead Publishing Series in Food Science, Technology, and Nutrition, Philadelphia, PA. Chapter 22, p. 314-324.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Manuel, C., Moore, M., and Jaykus, L.A. Rapid Destruction of Human Norovirus Capsid and Genome Occurs during Exposure to Copper-containing Surfaces. International Association for Food Protection Annual Meeting, Indianapolis, IN, August 6, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Mertens, B.S., Moore, M., Jaykus, L.A., and Velev, O.D. Characterization and Control of Surfactant and Copper-Mediated Norovirus Interactions. ACS Colloids and Surface Science Symposium, University of Pennsylvania, Philadelphia, PA, June 23, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Hall, A.J., Pringle, K., Wikswo, M.E., Gould, L.H., and Parashar, U.D. Epidemiologic attribution of foodborne norovirus outbreaks, United States, 2009-2012. International Association for Food Protection Annual Meeting, Indianapolis, IN, August 05, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Hall, A.J. and NoroSTAT Network. Impact of the emergent norovirus GII.4 Sydney in the United States. Council for State and Territorial Epidemiologists Annual Conference, Nashville, TN, June 25, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Afolayan, O.T., Webb, C., and Cannon, J.L. 2014. Evaluation of a PGM-Binding Method for the Discrimination of Infectious and Non-Infectious Norovirus Following Inactivation with Heat or a Levulinic Acid plus Sodium Dodecyl Sulfate Sanitizer. International Association for Food Protection Annual Meeting, Indianapolis, IN, August 05, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Afolayan, O.T., and Cannon, J.L. 2014. Discrimination of infectious and non-infectious human norovirus GI.1: Evaluation of a PGM-binding method following inactivation with heat or a levulinic acid plus sodium dodecyl sulphate sanitizer. Institute of Food Technologists Annual Meeting, New Orleans, LA, June 23, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Grytdal, S. Incidence of norovirus-associated acute gastroenteritis in four Veteran's Affairs Medical Center populations in the United States, 2011-2012. IDWeek 2014, Philadelphia, PA, October 11, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Moore, M., Escudero-Abarca, B.I., Suh, S.H., and Jaykus, L.A. Use of a Nucleic Acid Aptamer-based Method to Study Thermal Inactivation of Human Norovirus. International Association for Food Protection Annual Meeting, Indianapolis, IN, August 06, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Escudero-Abarca, B.I., Moore, S., Suh, S.H., and Jaykus, L.A. Use of Aptamer Magnetic Capture and Quantitative Real-time PCR (AMC-RT-qPCR) for Detection of Human Norovirus in a Model Food . International Association for Food Protection Annual Meeting, Indianapolis, IN, August 05, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Moore, M., Escudero-Abarca, B.I., Suh, S.H., and Jaykus, L.A. Development and Characterization of Nucleic Acid Aptamers for the Detection of Human Norovirus across a Broad Group of Genotypes. International Association for Food Protection Annual Meeting, Indianapolis, IN, August 05, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Cannon, J.L. 2014. Challenges in detecting infectious foodborne viruses in produce. Institute of Food Technologists Annual Meeting, New Orleans, LA, June 23, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Cannon, J.L. 2014. Emerging ligands to facilitate norovirus capture in food and environmental samples. International Association for Food Protection Annual Meeting, Indianapolis, IN, August 06, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Moore, M., Escudero-Abarca, B.I., and Jaykus, L.A. Development of a Recombinase Polymerase Amplification Assay for the Rapid Isothermal Detection of Human Norovirus. International Association for Food Protection Annual Meeting, Indianapolis, IN, August 05, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Gentry-Shields, J., and Jaykus, L.A. Evaluating Viral Process Controls: Turnip Crinkle Virus and Tulane Virus Demonstrate Similar RNA Extraction Efficiencies to Norovirus Genogroups I and II. International Association for Food Protection Annual Meeting, Indianapolis, IN, August 05, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Hannes, A., Tung-Thompson, G., and Jaykus, L.A. Analysis of the Environmental Persistence of Tulane Virus, a Novel Cultivable Surrogate for Human Norovirus. International Association for Food Protection Annual Meeting, Indianapolis, IN, August 05, 2014.
  • Type: Other Status: Other Year Published: 2014 Citation: Jaykus, L. Noroviruses: A near perfect foodborne pathogen? ILSI North America Food, Nutrition and Safety Program mid-year meeting, Washington, DC, July 23, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Gentry-Shields, J., and Jaykus, L.A. Evaluation of norovirus genogroup I and II process controls during RNA extraction, PEG precipitation, and elution from foods: Murine norovirus, MS2 coliphage, Tulane virus, and Turnip crinkle virus. International Society for Food and Environmental Virology, Corfu, Greece, September 02, 2014 - September 05, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Escudero-Abarca, B.I., Suh, H.W., Manuel, C., and Jaykus, L.A. Nucleic Acid Aptamers Mimick Histo-Blood Group Antigens for ProbingThermal Inactivation of Human Norovirus Strains. International Society for Food and Environmental Virology, Corfu, Greece, September 02, 2014 - September 05, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Manuel, C., Moore, M., and Jaykus, L.A. Exposing Human Norovirus Outbreak Strains and Human Norovirus Virus-Like Particles to Copper Alloy Surfaces Results in Rapid Destruction of the ViralGenome and Capsid and a Loss of Histo-Blood Group Antigen Binding Ability. International Society for Food and Environmental Virology, Corfu, Greece, September 02, 2014 - September 05, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Tung-Thompson, G., Libera, D., de los Reyes, F., and Jaykus, L.A. Aerosolization of Virus Particles through Vomiting. International Society for Food and Environmental Virology, Corfu, Greece, September 02, 2014 - September 05, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Goulter, R.M., and Jaykus, L.A. Norovirus Interactions with Gastrointestinal Microflora. International Society for Food and Environmental Virology, Corfu, Greece, September 02, 2014 - September 05, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Cannon, J.L. 2014. A Comparison of Molecular Methods for Estimating Human Norovirus Infectivity. Institute of Food Technologists Annual Meeting, New Orleans, LA, June 24, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Escudero-Abarca, B.I., Suh, S.H., Moore, M., Dwivedi, H., and Jaykus, L.A. Selection, Characterization and Application of Nucleic Acid Aptamers for the Capture and Detection of Human Norovirus Strains. International Society for Food and Environmental Virology, Corfu, Greece, September 02, 2014 - September 05, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Yearing, T., Fraser, A.M., and Jiang, X. Development of a standardized method for Norovirus virucidal testing on soft surfaces. International Association for Food Protection Annual Meeting, Indianapolis, IN, June 06, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Cannon, J.L. 2014. Foodborne Viruses: An International Food Safety Concern. International Union of Food Science and Technology Bi-annual Meeting, Montreal, Quebec, Canada, August 20, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Lee, A. Novel Processing Technologies to Manage the Risk of Foodborne Viruses. IAFP European Symposium on Food Safety, Budapest, Hungary, May 07, 2014 - May 09, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Lee, A., and Grove, S. Non-thermal Processing Technologies to Inactivate Foodborne Viruses. 3rd International Conference and Exhibition on Food Processing and Technology, Las Vegas, NV, July 21, 2014 - July 23, 2014.
  • Type: Other Status: Other Year Published: 2014 Citation: Jaykus, L. Norovirus challenges and how NoroCORE is contributing to solutions. Annual CDC CaliciNet Users meeting, Nashville, TN. December 10, 2015
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Hall, A.J. Handle with Care - Norovirus. IDWeek 2014, Philadelphia, PA, October 9, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Hall, A.J. The Global Burden of Norovirus. American Society of Tropical Medicine and Hygiene 63rd Annual Meeting, New Orleans, LA, November 3, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Cannon, J.L. Foodborne Viruses: An International Food Safety Concern. Microal 2014, Iguazu Falls, Parana, Brazil, October 14, 2014 - October 15, 2014.
  • Type: Other Status: Other Year Published: 2015 Citation: Estes, M.K. Update on cell culture systems. Technical Expert Group Meeting: Global Burden of Norovirus and Prospects for Vaccine Development, Atlanta, GA, February 23, 2015 - February 25, 2015.
  • Type: Other Status: Other Year Published: 2015 Citation: Hall, A.J. Food Handlers as a Potential Target Group for Norovirus Vaccination. Global Burden of Norovirus and Prospects for Vaccine Development, Technical Expert Group Meeting: Global Burden of Norovirus and Prospects for Vaccine Development Atlanta, GA, February 25, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Lee, A., Grove, S., Zhou, Z., Zhao, H., and Krishnamurthy, K. The Use of High Intensity Pulsed Light to Inactivate Murine Norovirus on Various Food Contact Surfaces. 4th ISFEV Food and Environmental Virology Conference, Corfu, Greece, September 02, 2014 - September 05, 2014.
  • Type: Other Status: Other Year Published: 2015 Citation: Cannon, J.L. Are Certain Foods 'Borne' for Viruses? Updates on Foodborne Virus Detection and Survival. UGA Center for Food Safety Annual Meeting, Atlanta, GA, March 4, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Jaykus, L. Norovirus at retail and food service: What you need to know. Food Safety Summit, Washington, DC, April 30, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Fraser, A.M. Knowledge of Norovirus prevention and control among infection preventionists. Association for Professionals in Infection Control and Epidemiology, Anaheim, CA, June 08, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Shearer, A.E.H., and Kniel, K. Effect of Plant Proteases on Infectivity of Tulane Virus. International Association for Food Protection Annual Meeting, Indianapolis, IN, August 03, 2014 - August 06, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Wang, Q., and Kniel, K. Inactivation of Human Norovirus and Its Surrogates on Alfalfa Seeds by Aqueous Ozone. International Association for Food Protection Annual Meeting, Indianapolis, IN, August 03, 2014 - August 06, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Wang, Q., Markland, S., and Kniel, K. A Comparative Study Investigating the Inactivation of Human Norovirus and Its Surrogates Using Aqueous Ozone and Chlorine. American Society for Microbiology, Boston, MA, May 17, 2014 - May 20, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Yu, C.F., Hida, K., Papafragkou, E., Yang, Z., Leonard, S., and Kulka, M. Evaluation of Molecular Methods for Detection and Genotyping of Norovirus. International Association for Food Protection Annual Meeting, Indianapolis, IN, August 03, 2014 - August 06, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Kirby, A.E., Yi, J., Sederdahl, B., Anderson, E., Shane, A.L., Wahl, K., and Moe, C.L. Norovirus and Rotavirus Prevalence in Stool Specimens from Children and the Aged in a Southeastern United States Community, 2012-2013. American Society for Virology, Fort Collins, CO, June 22, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Janes, M.E., and Maite, M. Extraction of Human Norovirus from seawater with zeolite granules. Institute of Food Technologists Annual Meeting, New Orleans, LA, June 21, 2014 - June 24, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Lee, A., Grove, S., Zhou, Z., Zhao, H., and Krishnamurthy, K. Inactivation of Murine Norovirus by High Intensity Pulsed Light Treatment on Various Food Contact Surfaces. International Association for Food Protection Annual Meeting, Indianapolis, IN, August 02, 2014 - August 06, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Lee, A., Zhou, Z., Grove, S., and Krishnamurthy, K. Effect of Pulsed Light Treatment on the Surface Temperature of various Food Contact Surfaces. Institute of Food Technologists Annual Meeting, New Orleans, LA, June 21, 2014 - June 24, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Janes, M.E., Montazeri, N., and Goetteri, D. Noroviruses, enteric viruses and microbial indicators in wastewater treatment plant influent and effluent. Institute of Food Technologists Annual Meeting, New Orleans, LA, June 21, 2014 - June 24, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Janes, M.E., Montazeri, M., and Da, L. Noroviruses, enteric viruses and microbial indicators in American oysters (Crassostrea virginica) along Mississippi River Delta. Institute of Food Technologists Annual Meeting, New Orleans, LA, June 20, 2014 - June 24, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Zeller, M., Finney, M., Getty, M., and Fraser, A. Content Analysis of Food Safety Education Materials. International Association for Food Protection Annual Meeting, Indianapolis, IN, August 04, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Finney, M., Carney, M., Kosa, K., Cates, S., Brophy, J., Fraser, A., and Fraser, A.M. Need for Education about Noroviruses: Findings from a Nationally Representative Survey of U.S. Adults. International Association for Food Protection Annual Meeting, Indianapolis, IN, August 05, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Kotwal, G., Lee, C.C., Kang, W., and Cannon, J.L. 2014. Comparative study of Human Finger-pads and Porcine Skins used to Quantify Cross-Contamination by Norovirus and Salmonella during Glove Application and Food Handling. International Association for Food Protection Annual Meeting, Indianapolis, IN, August 05, 2014.
  • Type: Other Status: Other Year Published: 2014 Citation: Kang, W., and Cannon, J.L. A Novel Membrane-based Electro-separation Method for Sample Clean-up and Norovirus Concentration. UGA Center for Food Safety Annual Meeting, Atlanta, GA, March 3, 2015 - March 4, 2015.
  • Type: Other Status: Other Year Published: 2015 Citation: **Anderson, B., Kotwal, G., and Cannon, J.L. Efficacy of Natural Antimicrobials on Norovirus and Hepatitis A Virus. UGA Center for Food Safety Annual Meeting, Atlanta, GA, March 3, 2015 - March 4, 2015.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Chapman, B.J. Novel strategies to connect with food handlers: setting the stage. Food Safety Summit, Baltimore, MD, April 28, 2015.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Kosa, K., Cates, S., Hall, A.J., Brophy, J., and Fraser, A.M. 2013. Gaps in Food Safety Professionals Knowledge about Noroviruses. J Food Prot, 77(8): 1336-1341.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Cromeans, T., Park, G.W., Constantini, V., Lee, D., Wang, Q., Farkas, T., Lee, A., and Vinj�, J. 2014. Comprehensive Comparison of Cultivable Norovirus Surrogates in Response to Different Inactivation and Disinfection Treatments. Appl Environ Microbiol. 80(18): 5743-51.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Czak�, R., Atmar, R.L., Opekun, A.R., Gilger, M.A., Graham, D.Y., and Estes, M.K. 2015. Experimental human infection with Norwalk virus elicits a surrogate neutralizing antibody response with cross-genogroup activity. Clin Vaccine Immunol, 22(2): 1-8. DOI: 10.1128/CVI.00516-14.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Janes, M.E. Montazeri, N., Maite, M., Liu, D., Cormier, J., Landry, Shackleford, J., Lampila, L.E., and Achberger, E.C. 2015. Surveillance of Enteric Viruses and Microbial Indicators in the Eastern Oysters (Crassostrea virginica) and Harvest Waters Along Louisiana Gulf Coast. J. Food Sci, 80(5): 1075-82.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Kou, B., Crawford, S.E., Ajami, N.J., Czak�, R., Neill, F.H., Tanaka, T.N., Kitamoto, N., Palzkill, T.G., Estes, M.K., and Atmar, R.L. 2015. Characterization of cross-reactive norovirus-specific monoclonal antibodies. Clin Vaccine Immunol, 22(2): 1-8. DOI: 10.1128/CVI.00519-14.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Katayama, K., Murakami, K., Sharp, T.M., Guix, S., Oka, T., Takai-Todaka, R., Nakanishi, A., Crawford, S.E., Atmar, R.L., Estes, M.K. 2014. A plasmid based human norovirus reverse genetics system produces reported-tagged progeny virus containing infectious genomic RNA. PNAS, Sep 23;111(38):E4043-52. doi: 10.1073/pnas.1415096111.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Huang, W., Samata, M., Crawford, S.E., Estes, M.K., Neill, F., Atmar, R.L., Palzkill, T. 2014. Identification of human single-chain antibodies with broad reactivity for noroviruses. Protein Eng Des Sel, Oct;27(10):339-49. doi: 10.1093/protein/gzu023.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Qu, L., Vongpunsawad, S., Atmar, R.L., Prasad, BVV, Estes, M.K. 2014. Development of a Gaussia luciferase-based human norovirus protease reporter system: cell type-specific profile of Norwalk virus protease precursors and evaluation of inhibitors. J Virol, 88(18): 10312-26.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Wang, Q., and Kniel, K.E. 2014. Effectiveness of calcium hypochlorite on viral and bacterial contamination of alfalfa seeds. Foodborne Pathogens and Disease, 11(10): 759-768.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Chapman, B.J., Raymond, B.J., and Powell, D. 2014. Potential of social media as a tool to combat foodborne illness. Perspect Publ Health, 134(4): 225-230.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Broglie, J.J., Moore, M.D., Jaykus, L.A., and Yang, L 2014. Design and Evaluation of Three Immuno-based Assays for Rapid Detection of Human Norovirus Virus-like Particles. Journal of Analytical and Bioanalytical Techniques, 5: 220. DOI: 10.4172/2155-9872.1000220.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Escudero-Abarca, B.I., S.-H. Suh, M. Moore, H.P. Dwivedi, and L. Jaykus. 2014. Selection, characterization and application of nucleic acid aptamers for the capture and detection of human norovirus strains. PLoS One, E106805.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Tung-Thompson, G., J. Gentry-Shields, A. Fraser, and L. Jaykus. 2014. Persistence of human norovirus RT-qPCR signals in simulated gastric fluid. Food Environ Virol. 2015 Mar;7(1):32-40. doi: 10.1007/s12560-014-9170-4.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Viator, K., Blitstein, J., Brophy, J., and Fraser, A.M. 2015. Preventing and Controlling Foodborne Disease in Commercial and Institutional Foodservice Settings: A Systematic Review. J Food Prot, 78(2): 446-456.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: DiCaprio E., Culbertson, D., and Li, J. 2015. Evidence of the Internalization of Animal Calciviruses via the Roots of Growing Strawberry Plants and Dissemination of the Fruit. Appl Environ Microbiol, 81(8): 2727-2734.
  • Type: Journal Articles Status: Accepted Year Published: 2015 Citation: Lou, F., Neetoo, H., Chen, H., and Li, J. 2015. High Hydrostatic Pressure Processing: A Promising Nonthermal Technology to Inactivate Viruses in High-Risk Foods. Ann Rev Food Sci Technol, 6: 389-409.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Cates, S., Kosa, K., Brophy, J, Hall, A.J., and Fraser, A.M. 2015. Consumer Education Needed on Norovirus Prevention and Control: Findings from a Nationally Representative Survey of U.S. Adults. J Food Prot, 78(3): 484-90.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Moore, M.D., R.M. Goulter, and L. Jaykus. 2015. Human norovirus as a foodborne pathogen: Challenges and developments. Ann Rev Food Sci Technol, 6:411-433.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Prasad, B.V., Shanker, S., Hu, L., Choi, J.M., Crawford, S.E., Ramani, S., Czako, R., Atmar, R.L., and Estes, M.K. 2014. Structural basis of glycan interaction in gastroenteric viral pathogens. Curr Opin Virol, 7C: 119-127. DOI: 10.1016/j.coviro.2014.05.008.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Verhoef, L., Hewitt, J., Barclay, L., Ahmed, S., Lake, R., Hall, A.J., Lopman, B., Kroneman, A., Vennema, H., Vinj�, J., and Koopmans, M. 2015. Norovirus Genotype Profiles Associated with Foodborne Transmission, 1999-2012. Emerg Infect Dis, 21(4): 592-9.


Progress 06/01/13 to 05/31/14

Outputs
Target Audience: Stakeholder engagement is a common theme in all project activities. Formalized extension and outreach activities are designed to improve understanding and expand use of measures to reduce viral foodborne disease risks. Six major stakeholder groups have been identified for this project: (1) fresh produce industry; (2) molluscan shellfish industry; (i) retail/institutional food sectors; (4) detection technologies; (5) the cleaning, sanitizing, and hygiene sector; and (6) food processing industries. We are also beginning to work with the cruise ship industry. Three major audiences are being targeted for communications programs: (1) food safety and public health professionals; (2) food industry professionals (food production, processing, retail, and foodservice); and (3) consumers. Both graduate and undergraduate internships are being offered. A synopsis of year 3 efforts is provided below: -- NoroCORE exhibited at the annual meeting of the International Association for Food Protection (IAFP) in Charlotte, NC, July 28-31, 2013. Informational and promotional materials were distributed, NoroCORE team members also attended and presented to a number of professional development groups, the purpose of which was to raise awareness of Food Virology and NoroCORE activities, and to increase stakeholder involvement. A stakeholder reception was hosted on the evening before the IAFP opening session. One IAFP symposium was sponsored by NoroCORE; another was sponsored by NoroCORE for the IAFP European Symposium in May, 2013 in Marseille, France. -- NoroCORE collaborators provided expert opinion to the National Advisory Committee on Microbiological Criteria for foods (NACMCF) relative to their Norovirus charge. --NoroCORE was represented at several national meetings relevant to retail stakeholders, including the National Restaurant Association and the Conference for Food Protection. --In terms of consumers, various informational extension modules were produced. --A comprehensive social media effort has been undertaken using “emerging issues” funds. These funds will be used to update the existing website; develop an “app” and other approaches to gather data on norovirus-like illnesses; and to distribute information to the general population about human norovirus (HuNoV) using credible sources. We will also use website analytics to assess traffic and use patterns to gauge public reach. --NoroCORE was represented at several a regional and national fresh produce safety meetings. Extension staff member Simmons is a member of the Produce Safety Alliance (PSA) subcommittee on Outreach and Extension. In response to recent virus outbreaks associated with berries, fact sheets specific to production, harvest, and packing of this product were produced for distribution. --NoroCORE was represented at a several of regional and national meetings dealing with the safety of molluscan shellfish. Extension staff member Simmons is a member of the Interstate Shellfish Sanitation (ISSC) subcommittee to oversee the development of a national training curriculum for growers and harvesters. An in-person meeting of the NoroCORE Shellfish Advisory Panel was convened, resulting in awarding “emerging issues” funds to provide assistance to harvesting states in the design and implementation of the ISSC Harvester and Dealer Continuing Education program; address the overboard boat waste dumping problem; and help support a symposium on the use of male specific coliphages for early identification of human fecal contamination of molluscan shellfish. --NoroCORE staff worked closely with the Emetphobia Recovery System (http://emetophobiarecovery.com/) in producing accurate norovirus information for their website and an infographic. -- The second NoroCORE newsletter was designed and produced. --The NoroCORE Food Virology Literature database continues to be updated, the blog post maintained, and the reagent and protocol exchange lists expanded. --Practical laboratory-based on-site training in Food Virology was provided by NoroCORE investigators (at North Carolina State University, NCSU) to NC A&T State University and Ohio State Univerisity (OSU); and between CDC and Clemson University. --Three paid, research-based summer internships were provided to undergraduates from historically-underrepresented groups in summer, 2013. These were hosted by investigators from Clemson, Baylor, and NCSU. --Five graduate fellowships were awarded; one of these is from an underrepresented population. The students represent the following universities: Baylor, Emory, Rutgers, OSU, and NC Central. An additional four were selected for project Year 4. Changes/Problems: The existing evaluation contract was terminated and a new evaluation team have been identified and retained. What opportunities for training and professional development has the project provided? --There is extensive graduate student training associated with the USDA-NIFA Food Virology Collaborative. To date, 32 graduate students have been, or are in training at the collaborating universities under the auspices of this project. About 10 post-doctoral research associates have been, or are being supported. Many of our collaborators also support undergraduates working on various NoroCORE-related projects. In all cases, students have assigned mentors with whom they work closely. In addition to their mentors, most institutions have a post-doctoral professional development program in which most of our post-docs participate. --The project sponsors a formal undergraduate and graduate fellowship program in Food Virology, with a focus on recruiting under-represented student populations. Our year 3 efforts in these programs are detailed in the “Target Audiences” section. --A list of regional, national and international conferences in which NoroCORE collaborators and their students/staff presented during project year 3 is provided below. The Collaborative had representation at many other local meetings not listed here. 61st Annual Conference of the American Society of Mass Spectrometry, Minneapolis, MN, June 9-13 2013. Center for Produce Safety (UC-Davis) Annual Meeting, Rochester, NY, June 26, 2013. 2013 National Environmental Health Association (NEHA) Educational Conference and Exhibition, Washington, D.C., July 9-11, 2013. Annual Meeting of the Institute of Food Technologists (IFT), Chicago, IL, July 15, 2013. American Society of Virology (ASV), State College, PA, July 20-23, 2013. 102nd Annual meeting of the International Association for Food Protection (IAFP), Charlotte, NC, July 28-31, 2013. European Congress of Virology, Lyon, France, September 12, 2013. IDWeek 2013, San Francisco, CA, October 2-6, 2013. National Restaurant Association, Executive Leadership Meeting, Baltimore, MD, October 7, 2013 5th International Conference on Caliciviruses, Beijing, China, October 12-15, 2013 IAFP 3rd Asia Pacific International Conference on Food Safety, Taipei, Taiwan, October 29 - November 1, 2013. 8th International Conference for Food Safety and Quality, Las Vegas, NV, November 5-6, 2013. 62nd Annual Meeting of the American Society of Tropical Medicine and Hygiene, Washington, DC, November 13-17, 2013. InForm: Integrated Foodborne Outbreak Response and Management, San Antonio, TX, November 20, 2013. ISSC Biennial Meeting in San Antonio, TX, January 27- 30, 2014. Global Food Safety Initiative Consumer Goods Forum, Anaheim, CA, on February 27, 2014. 247th American Chemistry Society (ACS) National Meeting and Exposition, Dallas, TX , March 16-20, 2014. 16th International Congress on Infectious Diseases (ICID), Cape Town, South Africa, April 2-5, 2014. Food Safety Summit, Washington, DC, April 10, 2014 66th Interstate Seafood Seminar in Virginia Beach, VA, on April 18, 2014. 30th Annual Clinical Virology Symposium and Annual Meeting of the Pan American Society for Clinical Virology, Daytona Beach, FL, April 27-30, 2014. Partnership for Food Safety Education Partners Meeting, Washington, D.C., April 30, 2014. Conference for Food Protection Biennial Meeting, Orlando, FL, May 3-7, 2014. 32nd Annual Meeting of the European Society for Paediatric Infectious Diseases (ESPID), Dublin, Ireland, May 6-10, 2014. IAFP European Symposium on Food Safety 2014, Budapest, Hungary, May 7-9, 2014. American Society for Microbiology 114th General Meeting, Boston, Massachusetts, May 17-20, 2014. --Practical laboratory-based on-site training in Food Virology was provided by NoroCORE investigators (at North Carolina State University, NCSU) to NC A&T State University and Ohio State Univerisity (OSU); and between CDC and Clemson University. How have the results been disseminated to communities of interest? Results have been disseminated using traditional mechanisms including: publications (peer reviewed research publications, conference proceedings, book chapters, and articles in the scientific and popular press); presentations at scientific and professional meetings (poster and oral); fact sheets, videos, webinars, and PowerPoint presentations; website and blogs; NoroCORE newsletters; NoroCORE booth at professional meetings; and in-person and web-based stakeholder meetings. We have an active website and are beginning social media efforts. See section on Target Audiences and Efforts for details. What do you plan to do during the next reporting period to accomplish the goals? A full description of next year’s activities is provided in the Year 3 renewal package. There are no changes.

Impacts
What was accomplished under these goals? In project year 3, the Molecular Virology Core continued to focus on developing an in vitro cultivation method for HuNoV and evaluating emerging cultivable surrogate viruses. Non--transformed human intestinal cells and human intestinal organoids for HuNoV propagation have still not yielded productive infection, but various protocol modifications (different cell types and media) are being investigated. The Baylor group is also developing advanced molecular tools to facilitate and expedite future screening experiments. In seeking an animal model, investigators at Ohio State University (OSU) characterized the pathogenesis of bovine NoV (GIII.2) in gnotobiotic (Gn) calves, finding some evidence of viral infection. Their future work will focus on similar studies in Gn pgs. Comprehensive comparisons of the behaviors of novel cultivable surrogate viruses [i.e., Tulane virus (TV), porcine sapovirus (SaV), and aichivirus] to conventional surrogates [i.e., feline calicivirus (FCV) and murine norovirus (MNV)] when exposed to extremes of pH, heat, alcohol, chlorine, desiccation, and high hydrostatic pressure have been completed. Each surrogate virus demonstrated a different inactivation profile. Based on its genomic and physical similarity to HuNoV, as well as its relatively high degree of resistance to commonly used physical and chemical treatments, TV was deemed a good surrogate. However, choice of surrogate virus should also consider its intended use (treatment or condition to be evaluated). Full genome sequencing of about 150 GII.4 HuNoV strains derived from outbreaks between 2009 and 2013 has been completed and the data form the basis for models of strain evolution. The Detection Core continued to evaluate novel ligands for capture and detection of HuNoV. Synthetic ligands included (i) antibodies specific to regions of the HuNoV P domain; (ii) VLP-binding peptides expressed on bacterial phage; (iii) single chain antibodies; (iv) synbodies; and (v) nucleic acid aptamers. Many of these were screened for their reactivity against a panel of VLPs. While none reacted with all HuNoV VLPs (or viruses) tested, they did show some degree of broad reactivity. Applications of these ligands to virus concentration and detection in outbreak stools and food samples was demonstrated. Porcine gastric mucin as a natural virus capture material also showed promise. A study comparing the behavior of candidate internal process controls (e.g., cultivable HuNoV surrogates, F-RNA coliphage, and turnip crinkle virus) to HuNoV during virus extraction steps indicated that losses during RNA extraction exceeded those during elution or precipitation, and recovery of all the viruses varied widely. Three approaches are being studied to help discriminate HuNoV infectivity status (based on capsid integrity) using RT-qPCR, i.e., binding assays using procine mucin or nucleic acid aptamers; and RNase pre-treatment. In general, HuNoV titers estimated by RT-qPCR after near-lethal treatments (heat, chlorine) are reduced when pre-treatment was applied (compared to non-pre-treated samples), but signals were not completely abolished even though infectivity was presumed to be destroyed. Version 4 of a low density DNA micoraaray for genotyping HuNoV and hepatitis A virus was produced and is being used for detection and characterization of strains identified in environmental (water) samples. An agent-based approach serves as the basis for the quantitative microbial risk assessment model being developed, referred to as NoroOPTIMAL. Key characteristics of the microenvironment (restaurants, child and elder care facilities) have been parameterized, and the modeling framework designed. Efforts to characterize the burden of endemic HuNoV disease involve many collaborations. Year 3 efforts to characterize endemic HuNoV disease burden focused on collection of stool specimens and clinical data across a variety of surveillance platforms, with a focus on pediatric and geriatric populations. Most samples have been analyzed for HuNoV and genotyped, and those data are being analyzed in conjunction with clinical information. NHANES samples have been obtained and testing for seroprevalence begun. Enhancements to state and national outbreak surveillance systems and CaliciNet continue, and data from real-time reporting in sentinel states (NoroSTAT) for outbreak characterization has been analyzed. Efforts of the Prevention and Control Core focused evaluating HuNoV persistence and transfer, and inactivation in molluscan shellfish and fresh produce, as well as surface decontamination, largely using surrogates. Relative to the former, virus transfer efficiency between surfaces could be as high as 50% and transfer continued to occur on sequential touching between skin and lettuce. Persistence and transfer of HuNoV were confirmed in a clinical study looking at prevalence of virus on hands of infected individuals. Environmental sample collection from public restrooms in commercial food service establishments (n=1500) in SC, NJ, and OH has been completed and analysis of HuNoV prevalence underway. Studies on the dynamics of virus contamination in various fresh produce items showed the following: (1) prolonged virus persistence (weeks) in sprouts, leafy greens, and irrigation and recirculating waters; and (2) an influence of abotic stress and soil on internalization and dissemination of viruses in leafy greens. Based on an approximate 3 log inactivation or more as effective, physical processing technologies evaluated included high pressure (variable efficacy in berries and shellfish); high intensity pulsed light (effective on various surfaces); and heat (ineffective at traditional milk pasteurization conditions). Chemical methods evaluated included aqueous ozone (modestly effective in alfalfa seeds, 1-2 log inactivation); chlorine dioxide and aerosolized hydrogen peroxide (both effective on surfaces). Copper-based surfaces were found to be effective at inactivating HuNoV when copper content exceeded 60-70%. The Institute of Food Safety and Heath (IFSH) team is negotiating with several companies relative to commercialization of inactivation technologies. Efforts of the Extension and Outreach Core focus on various audiences. Educational interventions for food service managers and workers are being developed based on a previously reported systematic review. Data analysis of a web-enabled consumer panel showed relatively high awareness of HuNoV (50-85%) but poor knowledge about the role of foods in its transmission (20%). This is juxtaposed to the results of a similar survey targeting food safety and public health practitioners’ knowledge, in which 66% identified HuNoV as a leading cause of foodborne disease, but only 5% identified the most common settings for transmission. There were also significant gaps in knowledge about restriction of ill food worker, and effective disinfection and sanitizing practices. Based on survey results, web-based modules are being developed to increase knowledge of public health practitioners, and various approaches targeting consumer knowledge, including social media messaging. NoroCORE continues to be involved in curriculum development activities for national groups including the Produce Safety Alliance and the Interstate Shellfish Sanitation Conference, and have engaged in a large educational initiative with the latter. Capacity Building Core efforts focus on student training and fostering communications amongst the group and with stakeholders. Most of these efforts are described elsewhere in the report.

Publications

  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Hyser, J.M., Crawford, S.E., Ettayebi, K., Zeng, X.L., Broughman, J.R., Karandikar, U., Opekun, A.R., Graham, D.Y., Donowitz, M., and Estes, M.K. Human Intestinal Enteroids as a Model of Enteric Virus Pathogenesis. Digestive Disease Week 2014, Chicago, IL, May 03, 2014 - May 06, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Lee, A. Intervention strategies to control foodborne viruses during processing and handling. 65th Pacific Fisheries Technologists Conference, Monterey, CA, February 23, 2014 - February 26, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Chapman, B.J. Using the data and changing the map for food safety behavior. Global Food Safety Initiative Consumer Goods Forum, Anaheim, CA, February 27, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Jaykus, L.A. Viruses in Foods: The next frontier in Food Safety?. General Mills Corporate Office, Minneapolis, MN, February 10, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Jaykus, L.A. Viruses in Foods: Controversies in Food Safety Session. Food Safety Summit, Baltimore, MD, April 10, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Velev, O.D., Mertens, B.S., Moore, M., and Jaykus, L.A. Characterization and control of surfactant and copper-mediated norovirus interactions. Triangle Soft Matter Workshop, UNC-Chapel Hill, Chapel Hill, NC, May 08, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Jenkins-Broglie, J. and Yang, L. Progress towards eradicating foodborne disease: Rapid immunomagnetic capture of human norovirus virus-like particles. The Institute of Biological Engineering (IBE) 2014 Annual Meeting, Lexington, KY, March 06, 2014 - March 08, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Wahl, K., Yi, J., Kirby, A.E., Anderson, E., Jerris, R., Shane, A., and Moe, C.L. Norovirus and rotavirus prevalence in pediatric patients with underlying gastrointestinal dysfunction in Atlanta, GA, 2012-2013. 30th Annual Clinical Virology Symposium and Annual Meeting of the Pan American Society for Clinical Virology, Daytona Beach, FL, April 27, 2014 - April 30, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Qui�ones, B., and Lee, B. Use of low-density DNA microarrays and photopolymerization for genotyping foodborne-associated noroviruses. American Society for Microbiology 114th General Meeting, Boston, MA, May 17, 2014 - May 20, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Fraser, A., and Gensel, C.L. NoroCORE Consumer Outreach. Partnership for Food Safety Education Partners Meeting, Washington, D.C., April 30, 2014.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Schaeffer, J., Le Saux, J.C., Lora, M., Atmar, R.L., and Le Guyader, F.S. 2013. Norovirus contamination on French marketed oysters. Int. J. Food Microbiol., 166(2):244-248. Epub [doi: 10.1016/j.ijfoodmicro.2013.07.022].
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Miura, T., Parnaudeau, S., Grodzki, M., Okabe, S., Atmar, R.L., and Le Guyader, F.S. 2013. Environmental detection of GI, GII and GIV norovirus using a generic real-time RT-PCR assay. Appl. Environ. Microbiol., Epub [Aug. 16, 2013].
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Liu, P., Escudero, B., Jaykus, L., Montes, J., Goulter, R. M., Lichtenstein, M., Fernandez, M., Lee, J. C., DeNardo, E., Kirby, A.E., Arbogast, J. W., and Moe, C.L. 2013. Laboratory evidence of norwalk virus contamination on the hands of infected individuals. Appl Environ Microbiol, 79 (24): 7875-81. DOI: 10.1128/AEM.02576-13.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Shearer, A.E.H., Hoover, D.G, and Kniel, K.E. 2014. Effect of bacterial cell-free supernatants on infectivity of norovirus surrogates. J Food Prot, 77(1):145-149. DOI: 10.4315/0362-028X.JFP-13-204.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Kniel, K.E. 2014. The makings of a good human norovirus surrogate. Curr Opin Virol, 4:85-90. DOI: 10.1016/j.coviro.2014.01.002. Feb 1. [Epub]
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Kosa, K., Cates, S., Brophy, J., Hall, A.J., and Fraser, A.M. 2014. Knowledge of norovirus prevention and control among infection preventionists. Am J Infect Control, 42: 676-8.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Munir, N., Liu, P., Gasta�aduy, P., Montes, J., Shane, A., Moe, C. 2013. Norovirus infection in immunocompromised children and children with hospital-acquired acute gastroenteritis. J Med Virol, Sep 30 [epub ahead of print].
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Vega, E., Barclay, L., Gregoricus, N., Shirley, S.H., Lee, D., and Vinj�, J. 2014. Genotypic and Epidemiologic Trends of Norovirus Outbreaks in the United States, 2009-2013. J Clin Microbiol, 52(1): 147-55.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Escudero-Abarca, B.I., Rawsthorne, H., Goulter, R.M., Suh, S.H., and Jaykus, L.A. 2014. Molecular methods used to estimate thermal inactivation of a prototype human norovirus: More heat resistant than previously believed? Food Microbiol, 41:91-95.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Jaykus, L.A., and Hall, A.J. The USDA-NIFA Food Virology Collaborative (NoroCORE): A Model for an Integrated, Multidisciplinary Approach to Addressing the Leading Cause of Foodborne Disease. Annual Meeting International Association for Food Protection, Charlotte, NC, July 28-31, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Fanaselle, W., Lhotka, L., Otto, C., Cannon, J.L., Lewis, G., and Marcello, J. Preventing Norovirus Outbreaks: Applying the Science to Food Safety Programs. National Environmental Health Association (NEHA) 2013 Annual Educational Conference & Exhibition, Washington, D.C., July 9-11, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Fraser, A.M. Challenges and Successes to Modifying Human Behavior in an Effort to Prevent Foodborne Transmission of Human NoV. International Association of Food Protection Annual Meeting, Charlotte, NC, July 28-31, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Cannon, J.L. Research results update for USDA-AFRI Program Area A4131-funded projects. Annual Project PI and Co-PI's meeting. Institute for Food Technologists Annual Meeting. Chicago, I.L. July 16, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Hall, A.J. Surveillance for Norovirus Disease Using Google: An Example of Digital Epidemiology. Annual Meeting of International Association for Food Protection, Charlotte, NC, July 28-31, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Hall, A.J. Burden of Human Norovirus Disease and Attribution to Food. Annual Meeting of International Association for Food Protection, Charlotte, NC, July 28-31, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Hall, A.J. CDC Norovirus Program. NACMCF Norovirus Sub-committee Meeting, Washington, D.C., June 4, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Lee, A., and Vinje, J. What is the best surrogate for human norovirus? Annual Meeting of International Association for Food Protection, Charlotte, NC, July 29, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Janes, M.E. Control and Detection of Enteric viruses in Seawater and Molluscan Shellfish. Annual Meeting of International Association for Food Protection, Charlotte, NC, July 28-31, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Lee, A. Emerging technologies to inactivate human NoV in foods. Annual Meeting International Association for Food Protection, Charlotte, NC, July 28-31, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Afolayan, O.T., and Cannon, J.L. Virus Titer and Suspension Matrix Impacts Estimates of Human Norovirus Infectivity Following Thermal Inactivation by Enzyme Pre-Treatment with Proteinase K and Rnase A Prior to RT-qPCR. Georgia Association for Food Protection Annual Meeting, Athens, GA, September 19, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Cannon, J.L., Erickson, M.C., and Habteselassie, M. The likelihood of cross contamination of head lettuce by E. coli O157:H7, Salmonella and norovirus during hand harvest and recommendations for glove sanitizing and use. Center for Produce Safety (UC-Davis) Annual Meeting, Rochester, N.Y., June 26, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Estes, M.K. Norovirus Vaccine Development: A bench to bedside story. Swedish Society for Virology, Smogen, Sweden, August 22-25, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Qui�ones, B. Low-Density Microarray Technologies for Rapid Human Norovirus Genotyping. International Association for Food Protection Meeting. Annual Meeting of International Association for Food Protection, Charlotte, NC, July 28-31, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: DiCaprio, E., Purgianto, A., Ma, Y., Hughes, J., and Li, J. Attachment and localization of human norovirus and animal caliciviruses in fresh produce. Institute of Food Technologists, Chicago, IL, July 14-17, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Lou, F., Li, X., Huang, P., Gurtler, J., Niemira, B., Jiang, X., Chen, H., and Li, J. High pressure inactivation of human norovirus virus-like particles: factors that affect the efficacy. Institute of Food Technologists, Chicago, IL, July 14-17, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Yeap, J.W., Lou, F., Kaur, S., Morgan, M., Linton, R., and Li, J. Inactivation Kinetics and Mechanism of a Norovirus Surrogate on Stainless Steel Coupons Using Chlorine Dioxide Gas. Institute of Food Technologists, Chicago, IL, July 14-17, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Yeap, J.W., Lee, J., Linton, R., and Li, J. Development of a Human Norovirus Indicator using Enterococcus sp. 16S rRNA and Bacteroides fragilis gyrB Gene as a Rapid Detection (Monitoring) Tool in Various Environments. Annual Meeting International Association for Food Protection, Charlotte, NC, August 28-31, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Cormier, J., and Janes, M.E. Extraction of hepatitis A virus from seawater with zeolite granules. Annual Meeting of International Association for Food Protection, Charlotte, NC, July 28-31, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Kotwal, G and Cannon, J.L. Norovirus Cross-contamination Associated with Bare Hands and Gloves during Produce Handling. Annual Meeting International Association for Food Protection, Charlotte, NC, July 28-31, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Afolayan, O., and Cannon, J.L. Virus Titer and Suspension Matrix Impacts Estimates of Human Norovirus Infectivity Following Thermal Inactivation by Enzyme Pre-Treatment with Proteinase K and RNase Prior to RT-qPCR. Annual Meeting International Association for Food Protection, Charlotte, NC, July 28-31, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Shanker, S., Czako, R., Atmar, R.L., Estes, M.K., and Prasad, B.V. Structural analysis of HBGA binding in a GI.7 norovirus variant. 32nd Annual Meeting of the American Society for Virology, University Park, PA, July 20-24, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Han, L., Kitoval, N.E., Tan, M., Jiang, X., and Klassen, J. Binding Affinities Determination of the Norovirus P Particle with HBGA Oligosaccharides. 61st Annual Conference of the American Society of Mass Spectrometry, Minneapolis, MN, June 9-13 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Jaykus, L.A. Human norovirus detection in foods and the environment: Is this a practical reality? S-10. Annual Meeting of the International Association for Food Protection, Charlotte, NC, July 28-31, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Manuel, C., and Jaykus, L.A. Comparison of a nested two-step qPCR and a non-nested one-step RT-qPCR for detection of genogroup II noroviruses in diluted clinical fecal samples. T4-09. Annual Meeting of the International Association for Food Protection, Charlotte, NC, July 28-31, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Vinje, J. Keynote Lecture. European Congress of Virology, Lyon, France, September 12, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Langley, C., Freeman, M.C., and Cannon, J.L. Comparison of Human Norovirus Recovery using Magnetic Beads Coated with Porcine Gastric Mucin or Monoclonal Antibodies. International Association for Food Protection Annual Meeting, Charlotte, NC, July 28-31, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Li, J., Lou, F., and Jiang, X. High pressure inactivation of human norovirus and virus-like particles. American Society for Virology, College Station, PA, July 20-24, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Vinje, J. Invited Presentation. Vessel Sanitation Program Meeting, Ft. Lauderdale, FL, June 27, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Cates, S., Kosa, K., Brophy, J., and Fraser, A.M. Food Safety Professionals: Gaps in Their Knowledge about Noroviruses. Annual Meeting International Association of Food Protection Annual Meeting, Charlotte, NC, July 28-31, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: DiCaprio, E., Purgianto, A. and Li, J. The effect of abiotic stress on the internalization and dissemination of human norovirus surrogates in Romaine lettuce. American Society for Virology, College Station, PA, July 20-24, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Ettayebi, K., Zeng, X.-L., Crawford, S.E., Hyser, J.M., Ajami, N.J., Broughman, J., Qu, L., Lloyd, R.E., Opekun, A.R., Graham, D.Y., Sherman, V., Zachos, B.C., Kovbasnjuk, O., De Jonge, H.R., Donowitz, M., and Estes, M.K. Human jejunal enteroid cultures as a functional model of human small intestine to study infection with human enteric viruses. 32nd Annual Meeting of the American Society for Virology, University Park, PA, July 20-24, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Bolinger, H., and Schaffner, D.W. Bacterial Surrogates for the Detection of Norovirus on Common Surfaces. Nutrition, Endocrinology & Animal Biosciences Graduate Student Conference, New Brunswick, NJ, April 17, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Janes, M.E., and Montazeri, N. Detection of norovirus in American Oyster (Crassostrea virginica) from Louisiana Gulf coasts using two real-time RT-PCR assays. Annual Meeting of International Association for Food Protection, Charlotte, NC, July 28-31, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Suh, S.H., Escudero-Abarca, B., and Jaykus, L.A. Capture and detection of a representative human norovirus strain using target-specific nucleic acid aptamers: Proof of concept. P3-54. Annual Meeting of the International Association for Food Protection, Charlotte, NC, July 28-31, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Tung, G., Libera, D., de los Reyes, F., and Jaykus, L.A. Modeling norovirus transmission from an episode of vomiting. P2-97. Annual Meeting of the International Association for Food Protection, Charlotte, NC, July 28-31, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Tung, G., Wilson, C., Jaykus, L.A., Ganee, A., Cassard, S., and Mabilat, C. Evaluation of a novel surface sampling wipe for recovery of human noroviruses prior to detection using RT-qPCR. P2-99. Annual Meeting of the International Association for Food Protection, Charlotte, NC, July 28-31, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Escudero-Abarca, B., Suh, S., and Jaykus, L.A. Characterization of nucleic acid aptamers with broad reactivity to human norovirus strains. P2-98. Annual Meeting of the International Association for Food Protection, Charlotte, NC, July 28-31, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Goulter, R.M., and Jaykus, L.A. Using the ApoH protein to capture and concentrate human norovirus particles and virus-like particles from various matrices. P3-55. Annual Meeting of the International Association for Food Protection, Charlotte, NC, July 28-31, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Yeh, L. The Norovirus Workshop-Outbreak-Attack. Teachersworkshop. BRITE/NCCU, August 8, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Chapman, B.J. I just tweeted that I barfed: Food safety in the time of social media. Illinois Food Safety Symposium, Bloomington, IL, September 25, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Hall, A.J., Lopman, B.A., Payne, D.C., Patel, M.M., Gasta�aduy, P.A., Vinj�, J., and Parashar, U.D. Norovirus Disease Burden in the United States: Review of Recent Progress and Improved Estimates. Vaccines for Enteric Diseases Meeting, Bangkok, Thailand, November 06, 2013 - November 08, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Jaykus, L.A. Noroviruses and foodborne disease: Challenges and Perspectives. Biennial Meeting of the CDC Food Safety Modernization Act Surveillance Working Group, Atlanta, GA, December 09, 2013 - December 10, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Lou, F., Li, X., Huang, P., Gurtler, J., Niemira, B., Jiang, X., Chen, H., Kingsley, D., and Li, J. Estimation of human norovirus survival during high pressure processing. 5th International Calicivirus Conference, Beijing, China, January 24, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Czako, R., Opekun, A.R., Gilger, M.A., Graham, D.Y., Atmar, R.L., and Estes, M.K. Human norovirus infection elicits cross-reactive surrogate neutralizing antibodies. 5th International Conference on Caliciviruses, Beijing, China, October 12, 2013 - October 15, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Chapman, B.J. Food safety discussions: Shifting from dinner table discussion to Twitter feed hashtags. Kraft Annual Food Safety Meeting, Chicago, IL, September 24, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Chapman, B.J. Food Science, Technology and Safety Communication with the Media. International Beverage and Citrus Conference, Clearwater Beach, FL, September 19, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Barclay, L. Norovirus Outbreak: A Collaborative Approach. InForm meeting: Integrated Foodborne Outbreak Response and Management, San Antonio, TX, November 20, 2013 - November 20, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Kirby, A.E., Streby, A., and Moe, C.L. Norovirus GI and GII Titers in Emesis. 5th International Conference on Caliciviruses, Beijing, China, October 12, 2013 - October 15, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Oka, T., Stoltzfus, G., Zhu, C., Jung, K., Wang, Q., and Saif, L.J. Attempts to grow human and animal noroviruses in vitro. The 5th International Conference on Caliciviruses, Beijing, China, October 12, 2013 - October 16, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Wikswo, M.E., Desai, R., Edwards, K.M., Staat, M.A., Szilagyi, P.G., Weinberg, G.A., Curns, A.T., Lopman, B., Vinj�, J., Parashar, U.D., Payne, D.C., and Hall, A.J. Clinical Profile of Children with Norovirus Disease in Rotavirus Vaccine Era. Vaccines for Enteric Diseases Meeting, Bangkok, Thailand, November 06, 2013 - November 08, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Leshem, E., Wikswo, M., Barclay, L., Brandt, E., Storm, W., Salehi, E., DeSalvo, T., Davis, T., Saupe, A., Dobbins, G., Booth, H.A., Biggs, C., Garman, K., Woron, A.M., Parashar, U.D., Vinje, J., and Hall, A.J. Impact and Clinical Significance of the Emergent Norovirus GII.4 Sydney Strain -- United States, 2012-2013. Vaccines for Enteric Diseases Meeting, Bangkok, Thailand, November 06, 2013 - November 08, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Hall, A.J., Wikswo, M.E., Manikonda, K., Roberts, V.A., Yoder, J.S., and Gould, L.H. National Surveillance for Acute Gastroenteritis Outbreaks through the National Outbreak Reporting System, United States, 2009-2012. InFORM 2013: Integrated Foodborne Outbreak Response and Management, San Antonio, TX, November 18, 2013 - November 21, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Velev, O.D., Mertens., B.S., Moore, M., and Jaykus, L.A. Characterization and Control of Surfactant-Mediated Norovirus Colloidal Stability and Surface Adhesion. Molecular Biotechnology Program Annual Symposium, North Carolina State University, Raleigh, NC, November 13, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Estes, M.K., Qu, L., and Vongunsawad, S. NoroGLuc: a cell-based human norovirus protease reporter system. 5th International Conference on Caliciviruses, Beijing, China, October 12, 2013 - October 15, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Atmar, R.L., Kou, B., Crawford, S.E., Ajami, N.J., Czako, R., Neill, F.H., Tanaka, T.N., Kitamoto, N., Palzkill, T.G., and Estes, M.K. Characterization of cross-reactive norovirus-specific monoclonal antibodies. 5th International Conference on Caliciviruses, Beijing, China, October 12, 2013 - October 15, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Miura, K., Parnaudeau, S., Okabe, S., Atmar, R.L., and Le guyader, S.F. A generic real-time RT-PCR assay to detect norovirus in shellfish. 5th International Conference on Caliciviruses, Beijing, China, October 12, 2013 - October 15, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Chapman, B., and Jaykus, L.A. NoroCORE: The USDA NIFA Food Virology Collaborative. National Restaurant Association, 2013 Quality Assurance Executive Study Group Meeting, Baltimore, MD, October 07, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Simmons, O.D. Enhancing Food Security through Pre-Harvest Food Safety: Current Research and Outreach for Practical Solutions. Fulbright Scholars, Raleigh, N.C., November 05, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Simmons, O.D. Whats that in your pomegranate seeds?? Recent microbial threats linked to fresh fruits and vegetables. 28th Annual Southeast Vegetable and Fruit Growers Expo, Myrtle Beach, SC, December 04, 2013 (not invited).
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Fraser, A.M. Cleaning and Sanitizing of Food-Contact Surfaces. International Sanitation Suppliers Association (ISSA), Las Vegas, NV, November 20, 2013.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Lee, A., and Jaykus, L.A. A Serve of Enteric Virus with Your Salad? Managing the Risk of Foodborne Viruses. IAFP European Symposium on Food Safety 2014, Budapest, Hungary, May 07, 2014 - May 09, 2014.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Li, J. An integrated approach to minimize foodborne viruses in fresh produce. USDA Food Safety Meeting, Washington DC, May 07, 2014 - May 08, 2014.


Progress 06/01/12 to 05/31/13

Outputs
Target Audience: Stakeholder engagement is a common theme in all project activities. Formalized extension and outreach activities are designed to improve understanding and expand use of measures to reduce viral foodborne disease risks. Six major stakeholder groups have been identified for this project: (i) fresh produce industry; (ii) molluscan shellfish industry; (iii) retail/institutional food sectors; (iv) detection technologies; (v) the cleaning, sanitizing, and hygiene sector; and (vi) food processing industries. Three major audiences are being targeted for communications programs: (i) food safety and public health professionals; (ii) food industry professionals (food production, processing, retail, and foodservice); and (iii) consumers. Both graduate and undergraduate internships are being offered. A synopsis of year 2 efforts is provided below: --The first NoroCORE full Collaborative meeting which included all PIs, select students and staff, and key stakeholders, was held in November, 2012. This included a one-day informational meeting introducing the Collaborative (morning) and formal stakeholder presentations (afternoon). The second day was an open listening session in which stakeholders directly interacted with researchers and extension professionals, identifying the most critical food virology needs of each stakeholder group. -- A formal NoroCORE display booth was designed for exhibiting at professional conferences. -- The first NoroCORE newsletter was designed and produced. --NoroCORE was represented at a variety of regional and national fresh produce safety meetings. PI Jaykus presented an overview of the project to the United Fresh Produce Association Food Safety and Technology Council. A virus module was designed and submitted for inclusion in the National Good Agricultural Practices (GAPs) program being developed by the Produce Safety Alliance (PSA). --Abstracts associated with the searchable NoroCORE Food Virology Literature database were made publicly available on the NoroCORE website in project year 2. --Practical laboratory-based training (done on-site) in Food Virology was provided by NoroCORE investigators (NCSU) to Louisiana State University. --Practical laboratory-based training (done on-site) provided by NoroCORE investigators (CDC) to Clemson University. --Many one-on-one calls with representatives from the detection stakeholder sector were done to discuss the feasibility and market for norovirus testing in foods and environmental samples. --NoroCORE sponsored a symposium at the annual meeting of the Institute of Food Technologists in June, 2012. --NoroCORE investigators produced information sheets and other extension documents focused on the role of hand hygiene in controlling foodborne viral disease transmission; virus contamination risks in restaurants; virus persistence in frozen produce items; and recommended hygiene practices in child care settings. --An active blog post was maintained on the NoroCORE website. --Materials to support a Foodborne Virus Outbreak workshop to train middle school teachers were prepared. The workshop was offered to over 75 NC teachers in project year 2. --Two paid, research-based summer internships were provided to undergraduates from historically-underrepresented populations in summer, 2012. These were hosted by investigators from Clemson and North Carolina State universities. --Five graduate fellowship awardees were identified to receive funding in project year 3. One of these is from an underrepresented population. The students represent the following universities: Baylor, Emory, Rutgers, Ohio State, and NC Central. --Two of the four modules for the formalized Food Virology graduate minor were completed in year 2. Changes/Problems: Additional reporting requirements include filing of progress reports (delivered to the NPL) every four months. No changes or problems to report this period. What opportunities for training and professional development has the project provided? --There is extensive graduate student training associated with the USDA-NIFA Food Virology Collaborative. To date, 34 graduate students have been, or are in training at the collaborating universities under the auspices of this project. About 10 post-doctoral research associates are also supported. Many of our collaborators also support undergraduates working on various NoroCORE-related projects. In all cases, students have assigned mentors with whom they work closely. In addition to their mentors, most institutions have a post-doctoral professional development program in which most of our post-docs participate. --The project sponsors a formal undergraduate and graduate fellowship program in Food Virology, with a focus on recruiting under-represented student populations. Our year 2 efforts in these programs are detailed in the “Target Audiences” section. --A list of regional, national and international conferences in which NoroCORE collaborators and their students/staff presented during project year 2 is provided below. The Collaborative had representation at many other local meetings not listed here. 113th General Meeting of the American Society for Microbiology, Denver, CO. May 21, 2013. Expanded Food and Nutrition Education Program Multi-State Meeting, Charlotte, North Carolina, May 15, 2013. Epidemic Intelligence Service Conference, Atlanta, Georgia, April 22-26, 2013. Consumer Federation of America Food Policy Conference, Washington, D.C., April 16, 2013. VIROCLIME Conference, Cardiff, United Kingdom, March 13, 2013. Center for Food Safety Annual Meeting, Griffin, Georgia, March 6, 2013. U.K. Food Safety Authority Foodborne Viruses Research Conference, London, January 15-16, 2013. 39th Annual East Coast Commercial Fishermen’s and Aquaculture Trade Exposition, Ocean City, Maryland, January 18-20, 2013. Southeast Regional Vegetable Growers meeting, Savannah, Georgia, January 10-11, 2013. Annual meeting of the Merieux Research Grants Program, Annecy, France, October 22, 2012. IDWeek (Joint meeting of IDSA, SHEA, HIVMA, and PIDS), San Diego, California, October 17-21, 2012. 3rd Food and Environmental Virology Congress, Lisbon, Portugal, October 7-10, 2012. 8th United Fresh Produce Association Food Safety and Technology Council, Washington, D.C., October 1, 2012. Annual OutbreakNet Conference, Atlanta, Georgia, August 30, 2012FDA Northeast Region Annual Food Protection Seminar, Portsmouth, New Hampshire, August 22, 2012. 101st Annual Meeting of the International Association for Food Protection, Providence, Rhode Island, July 22-25, 2012. 31st Annual Meeting of the American Society for Virology, Madison, Wisconsin, July 21-25, 2012. Annual Meeting of Center for Produce Safety, Davis, California, June 27, 2012. --Practical laboratory-based training (done on-site) in Food Virology was provided by NoroCORE investigators to Louisiana State University. --Practical laboratory-based training (done on-site) provided by NoroCORE investigators (CDC) to Clemson University. How have the results been disseminated to communities of interest? Results have been disseminated using traditional mechanisms including: publications (peer reviewed research publications, conference proceedings, book chapters, and articles in the scientific and popular press); presentations at scientific and professional meetings (poster and oral); fact sheets, videos, and Powerpoint presentations; website and blogs; NoroCORE newsletters; NoroCORE booth at professional meetings; and in-person and web-based stakeholder meetings. See section on Target Audiences and Efforts for details. What do you plan to do during the next reporting period to accomplish the goals? A full description of next year’s activities is provided in the Year 3 renewal package. There are no changes.

Impacts
What was accomplished under these goals? In project year 2, the Molecular Virology Core continued to focus on developing an in vitro cultivation method for human noroviruses (HuNoV) and evaluating emerging cultivable surrogate viruses. Non--transformed human intestinal cells and human intestinal organoids for HuNoV propagation continued to be investigated, focusing on the use of different cell types derived from biopsy specimens from secretor positive individuals. While viral RNA was infectious in these sorts of models, fully permissive virus replication has not yet been demonstrated. Efforts also continued on the use of gnotobiotic pigs as a potential animal model for HuNoV replication. While virus shedding occurred intermittently and at relatively low titer using this model, further studies are needed to improve this model. Comprehensive comparisons of the behaviors of novel cultivable surrogate viruses [i.e., Tulane virus (TV), porcine sapovirus (SaV), and aichivirus] to conventional surrogates [i.e., feline calicivirus (FCV) and murine norovirus (MNV)] when exposed to extremes of pH, heat, alcohol, chlorine, desiccation, and high hydrostatic pressure were done using infectivity assay. Each novel surrogate virus demonstrated a different inactivation profile, and differences between cultivable surrogates were most pronounced for sensitivity to alcohols and exposure to dry conditions. Aichivirus had the most resistant profile. It appears that there will not be a “one size fits all” surrogate, but rather the appropriate surrogate virus will need to be chosen based on its intended use. The Detection Core continued to evaluate novel ligands to facilitate capture of HuNoV. Both naturally occurring and synthetic ligands were investigated. The use of porcine gastric mucin (PGM) or saliva in conjunction with traditional virus concentration methods (e.g., filtration and precipitation) appeared to enhance HuNoV recovery from complex samples. Proof-of-concept studies also demonstrated that apolipoprotein H (ApoH), a human plasma protein previously shown to have affinity to viruses, could be used to capture select GII.2 and GII.4 virus-like particles (VLPs) and HuNoV in microtiter plate-based and magnetic capture assays linked to RT-qPCR. Additional studies are needed on ApoH and PGM to characterize binding specificity and capture efficiency. Manufactured ligands investigated included (i) antibodies specific to regions of the HuNoV P domain; (ii) VLP-binding peptides expressed on bacterial phage; (iii) single chain antibodies; (iv) synbodies; and (v) nucleic acid aptamers. Candidate ligands were manufactured and many of these screened for their reactivity against a broad range of VLPs. While none of the ligands were able to capture and detect all HuNoV VLPs (or viruses), combining ligands may result in more broadly reactive detection approaches. In preparation for future studies to compare the efficacy of candidate methods to discriminate between infectious and non-infectious virus using molecular approaches, a comprehensive review of such methods was published in year 2. The Detection Core also developed the second generation of a rapid, colorimetric low-density DNA microarray for HuNoV detection and genotyping. This is currently being evaluated using a large, inclusive panel of HuNoV strains. The Epidemiology and Risk Analysis Core is combining clinical and laboratory-based capacity, and engaging medical and public health professionals in an effort to better characterize the endemic and epidemic burden of foodborne viral disease. Preliminary mathematical constructs were designed for development of our quantitative risk models. Qualitative data on foodborne HuNoV outbreaks was obtained through key informant interviews. These, along with primary data, have resulted in preliminary disease burden cost estimates. Efforts to characterize the burden of endemic and epidemic HuNoV disease involve many collaborative institutions. In year 2, these collaborations were strengthened, IRB approvals were sought, and sample collection and testing protocols established. Collection of stool specimens and clinical data by CDC has continued across the three surveillance platforms being used to characterize endemic disease burden: Veterans Affairs, New Vaccine Surveillance Network, and FoodNet. Emory is collecting similar data/samples from pediatric and geriatric populations. Emory also received approval to receive National Health and Nutrition Examination Survey (NHANES) samples for their upcoming HuNoV seroprevalence study. For epidemic disease, CDC moved forward with additional enhancements to the national outbreak surveillance systems (NORS) and CaliciNet. These include release of a revamped user interface for NORS; improved data download capabilities; initial integration of NORS and CaliciNet; and real-time reporting in sentinel states (NoroSTAT). During Year 2, the efforts of the Prevention and Control Core focused on molluscan shellfish and fresh produce. Relative to the former, a project at Louisiana State University was initiated to investigate HuNoV prevalence in oysters and seawater along the U.S. Gulf Coast, and assess the correlations between the presence of HuNoV and levels of common indicator microorganisms. Efforts have also focused on improved understanding of the dynamics of virus contamination (including attachment, internalization and persistence) in fresh produce (spinach, alfalfa seeds and sprouts, strawberries and raspberries, and green onions). The efficacy of sanitizers (e.g., chlorine, quaternary ammonium compounds) in removing and/or inactivating HuNoV and surrogates from food contact surfaces and fresh produce (lettuce and strawberry) was also investigated, finding that virus inactivation/removal was significantly improved when liquid sanitizers were supplemented with surfactants. Two collaborative institutions worked on evaluating novel non-thermal processing technologies to inactivate viruses in foods at elevated risk for contamination (berries, lettuce, and oysters). Technologies included high pressure, E-beam, gamma irradiation, UV, and pulsed light. High pressure processing parameters (e.g., pressure, holding time, and temperature) were optimized for inactivation of HuNoV, the cultivable surrogates, and rotavirus in the oyster matrix. It appears that, at 600 MPa for 2 min, all of these viruses could be effectively be inactivated. The Extension and Outreach Core is working to improve understanding and expand use of measures to reduce foodborne viral disease risks as a function of commodity. Year 2 efforts focused on evaluating current food virology outreach materials and defining the state of knowledge of key audiences. A systematic literature review to determine best practices for designing and delivering educational interventions in the foodservice environment was completed. Using the USDA Food Safety Education and Training Database, researchers at Clemson identified food safety materials targeting adult consumers and reviewed these for content relative to foodborne viruses, in preparation for design of information that can be included in these existing materials. To gauge consumer knowledge about foodborne viruses, a web-enabled national survey of 1,000 adults was completed. A similar survey was administered to 1,500 food safety and public health professionals. Analysis of these data is on-going. Capacity Building Core efforts focus on student training and fostering communications amongst the group. In year 2, our complete Food Virology Literature Database was released to all collaborators; this is updated monthly. A comprehensive reagent and protocol exchange amongst collaborators was established and has since been widely used, fostering standardization and collaboration. Other capacity-building efforts are described above in the “Target Audiences” section.

Publications

  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Ajami, N.J., Barry, M.A., Carillo, B., Muhaxhiri, Z., Neill, F.H., Prasad, B.V.V., Opekun, A., Gilger, M.A., Graham, D.Y., Atmar, R.L., and Estes, M.K. 2012. Antibody responses to norovirus genogroup GI.1 and GII.4 proteases in volunteers administered Norwalk virus. Clin. Vaccine Immunol. 19:1980-1983.
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Koo, H.L., Neill, F.H., Estes, M.K., Munoz, F.M., Cameron, A., DuPont, H.L., and Atmar, R.L. 2012. Noroviruses: the most common pediatric viral enteric pathogen at a large university hospital after introduction of rotavirus vaccination. J. Pediatr. Infect. Dis. Soc. 2012:1-4. [DOI:10.1093/JPIDS/PIS070]
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Zhang, X.F., Dai, Y.C., Zhong, W., Tan, M., Lv, Z.P., Zhou, Y.C., and Jiang, X. 2012. Tannic acid inhibited norovirus binding to HBGA receptors, a study of 50 Chinese medicinal herbs. Bioorg. Med. Chem. 20:1616-23.
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Wang, Q., Erickson, M.E., Ortega, Y.R., and Cannon, J.L. 2012. The Fate of Murine Norovirus and Hepatitis A Virus During Preparation of Fresh Produce by Cutting and Grating. Food Environ. Virol. 5(1):52-60.
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Wang, Q., Erickson, M.E., Ortega, Y.R., and Cannon, J.L. 2012. Physical Removal and Transfer of Murine Norovirus and Hepatitis A Virus from Contaminated Produce by Scrubbing and Peeling. J. Food Prot. 76(1):85-92.
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Liu, P., Jaykus, L.A., Wong, E., and Moe, C.L. Persistence of Norwalk Virus, Male-specific Coliphage, and Escherichia coli on Stainless Steel Coupons and in Phosphate-buffered Saline. J. Food Prot. 2012:75(12):2151-2157.
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Wikswo, M.E., and Hall, A.J. 2012. Outbreaks of acute gastroenteritis transmitted by person-to-person contactUnited States, 20092010. MMWR Surveillance Summaries. 61(SS-9):1-12.
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Trivedi, T.K., DeSalvo, T., Lee, L., Palumbo, A., Moll, M., Curns, A., Hall, A.J., Patel, M., Parashar, U.D., and Lopman, B.A. 2012. Hospitalizations and mortality associated with norovirus outbreaks in nursing homes, 2009-2010. JAMA. 308(16):1668-75.
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Hall, A.J., Eisenbart, V.G., Lehman, E., A., Gould, L.H., Lopman, B.A., and Parashar, U.D. 2012. Epidemiology of foodborne norovirus outbreaks, United States, 2001-2008. Emerg. Infect. Dis. 18(10):1566-1573.
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: DiCaprio, E., Ma,Y., Purgianto, A., Hughes, J., and Li, J. 2012. Internalization and dissemination of human norovirus and animal caliciviruses in hydroponically grown Romaine lettuce. Appl. Environ. Microb. 78(17):6143-6152 [AEM01081-12].
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Lou, F., Huang, P., Neetoo, H., Gurtler, J., Niemira, B., Chen, H., Jiang, X. and Li, J. 2012. High pressure inactivation of human norovirus virus-like particles provides evidence that the capsid of human norovirus is highly pressure resistant. Appl. Environ. Microb. 78(15):5320-5327 [AEM00532-12].
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Feliciano, L., Li, J., and Pascall, M. 2012. Efficacies of sodium hypochlorite and quaternary ammonium sanitizers for reduction of norovirus and selected bacteria during ware-washing operations. Plos One. 7(12) e50273 (December 2012).
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Esseili, M., Wang, Q., Zhang, Z., and Saif, L.J. 2012. Internalization of sapovirus, a surrogate for Norovirus, in romaine lettuce and the effect of lettuce latex on virus infectivity. Appl. Environ. Microbiol. 78:6271-9.
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Hirneisen, K.A., and Kniel, K.E. 2012. Comparison of ELISA attachment and infectivity assays for murine norovirus. J. Virol. Methods. 186(1-2):14-20.
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Fraser, A., Arbogast, J., Jaykus, L.A., Linton, R., and Pittet, D. 2012. Rethinking Hand Hygiene in the Retail and Foodservice Industries: Are Recommended Procedures Based on the Best Science and Practical under Real-world Conditions? Food Protection Trends. 32(12):750-759.
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Cannon, J.L., Kotwal, G. and Wang, Q. 2012. Inactivation of Norovirus Surrogates after Exposure to Atmospheric Ozone. Ozone: Sci. Eng., 35(3);217-219.
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Finkbeiner, S.R., Zeng, X.L., Utama, B., Atmar, R.L., Shroyer, N.F., and Estes, M.K. 2012. Stem cell-derived human intestinal organoids as an infection model for rotaviruses. mBio, 3(4):e00159-12.
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Trivedi, T.K., Desai, R., Hall, A.J., Patel, M., Parashar, U.D., and Lopman, B.A. 2012. Clinical characteristics of norovirus associated-deaths: A systematic literature review. Am. J. Infect. Control, December 21 [Epub ahead of print].
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Bolton, S.L., Kotwal, G., Harrison, M.A., Law, S.E., Harrison, J.A., and Cannon, J.L. 2013. Sanitizer Efficacy against Murine Norovirus, a Surrogate for Human Norovirus, on Stainless Steel Surfaces Using Three Application Methods. Appl. Environ. Microbiol. 79(4): 1368-77.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Hirneisen, K.A., and Kniel, K.E. 2013. Comparing human norovirus surrogates: murine norovirus and tulane virus. J. Food Prot. 1:139-143.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Hirneisen, K.A., and Kniel, K.E. 2013. Norovirus Surrogate Survival on spinach during preharvest growth. Phytopathology. 103(4): 389-394.
  • Type: Book Chapters Status: Published Year Published: 2013 Citation: Atmar, R.L., Estes, M.K. 2013 (2007 revised 2013). Rotaviruses, noroviruses and other viral agents of gastroenteritis. In: Engleberg, N.C., DiRita, V., and Dermody, T. (eds.), Schaechters Mechanisms of Microbial Disease, 5th Edition. Lippincott Williams & Wilkins, New York, New York. Chapter 37, p. 382-387.
  • Type: Book Chapters Status: Published Year Published: 2013 Citation: DSouza, D.H., Moe, C.L., and Jaykus, L.A. 2013. Foodborne Viral Pathogens. In: Doyle, M., and Beuchat, L. (eds.), Food Microbiology: Fundamentals and Frontiers 4th Edition. American Society for Microbiology Press.
  • Type: Book Chapters Status: Published Year Published: 2013 Citation: Hall, A.J., Lopman, B.A., and Vinj�, J. 2013. Sapovirus. In: Morris J.G., and Potter M.E. (eds.), Foodborne Infections and Intoxications, 4th Edition. Elsevier, London, U.K. p. 313319.
  • Type: Book Chapters Status: Published Year Published: 2013 Citation: Hall, A.J., Patel, M.M., Lopman, B.A., and Armah, G.E. 2013. Norovirus. In: Magill, A.J., Ryan, E.T., Hill, D.R., and Solomon, T. (eds.), Hunters Tropical Medicine and Emerging Infectious Diseases 9th Edition. Saunders, London, U.K. Chapter 30.2, p. 280-283.
  • Type: Book Chapters Status: Published Year Published: 2013 Citation: Gasta�aduy, P.A., Hall, A.J., Parashar, U.D. 2013. Rotavirus. In: Morris J.G, and Potter M.E., (eds.), Foodborne Infections and Intoxications, 4th Edition. Elsevier, London, U.K. 303311.
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Li, D., Baert, L., Zhang, D., Xia, M., Zhong, W.,Van Coillie, E., and Jiang, X. 2012. The Effect of Grape Seed Extract on Human Noroviruses GII.4 and Murine Norovirus-1 in Viral Suspensions, on Stainless Steel Discs, and in Lettuce Wash Water. Appl. Enviro. Microbiol. 78(21):7572-7578. [DOI 10.1128/AEM.01987-12]
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Hirneisen, K.A., Sharma, M., and Kniel, K.E. 2012. Human Enteric Pathogen Internalization by Root Uptake into Food Crops. Foodborne Pathogens and Disease. 9(5): 396-405. doi:10.1089/fpd.2011.1044.
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Bitler, E.J., Matthews, J.E., Dickey, B.W., Eisenberg, J.N.S., and Leon, J.S. 2012. Norovirus outbreaks: a systematic review of commonly implicated transmission routes and vehicles. Epidemiol. Infect. FirstView Article:1-9.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Yen, C., and Hall, A.J. 2013. Challenges to estimating norovirus disease burden. Journal of the Pediatric Infectious Diseases Society, 2(1):61-62.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Le Guyader, F.S., Atmar, R.L., Maalouf, H., and Le Pendu, J. 2013. Shellfish contamination by norovirus: strain selection based on ligand expression? Clin. Virol. (Journal of the Japanese Society of Clinical Virology), 41:1-16.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Estes, M.K., Graham, D.Y., Opekun, A.R., Neill, F.H., Ramani, S., Czak�, R., Crawford, S.E., Ajami, N.J., Prasad, B.V.V., Gilger, M.A., and Atmar, R.L. 2013. Norovirus vaccine development: A bench to bedside story. Clin. Virol. (Journal of the Japanese Society of Clinical Virology), 41:17-29.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Hirneisen, K.A., and Kniel, K.E. 2013. Comparative uptake of enteric viruses into spinach and green onions. Food and Environ. Virol. 5(1): 24-34.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Tian, P., Yang, D., Quigley, C., Chou, M., and Jiang, X. 2013. Inactivation of the tulane virus, a novel surrogate for the human norovirus. J Food Prot. 76(4):712-8.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Gasta�aduy, P.A., Hall, A.J., Curns, A.T., Parashar, U.D., and Lopman, B.A. 2013. Burden of norovirus gastroenteritis in the ambulatory settingUnited States, 20012009. J. Infect. Dis. 207(7):105865.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Hida, K., Kulka, M., and Papafragkou, E. 2013. Development of a rapid total nucleic acid extraction method for the isolation of hepatitis A virus from fresh produce. Int. J. Food Microbiol. 161:143-150.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Leshem, E., Barclay, L., Wikswo, M., Gregoricus, N., Vinj�, J., Lopman, B., Parashar, U., and Hall, A. 2013. Notes from the field: Emergence of new norovirus strain GII.4United States, 2012. MMWR Morbidity and Mortality Weekly Report 2013. 62(3):55. Reprinted in Journal of the American Medical Association 2013: 309:979.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Payne D.C., Vinj�, J., Szilagyi, P.G., Edwards, K.M., Staat, M.A., Weinberg, G.A., Hall, C.B., Chappell, J., Bernstein, D.I., Curns, A.T., Wikswo, M., Shirley, S.H., Hall, A.J., Lopman, B., and Parashar, U.D. 2013. Norovirus and medically attended gastroenteritis in U.S. children. New Engl. J. Med. 368(12):1121-30.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2012 Citation: Desai, R., Hembree, C.D., Handel, A., Matthews, J.E., Dickey, B.W., McDonald, S., Hall, A.J., Parashar, U.D., Leon, J.S., and Lopman, B. 2012. Severe outcomes are associated with genogroup 2 genotype 4 norovirus outbreaks: A systematic literature review. International Conference on Emerging Infectious Diseases, Atlanta, Georgia. March 11-14, 2012.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2012 Citation: Cannon, J.L. Food Safety Strategies/Technologies to Reduce the Risk of Norovirus in Meat Processing and Retail Operations. Institute for Food Technologists Annual Meeting and Food Expo. 2012, Las Vegas, Nevada, June 25-28, 2012.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2012 Citation: Li, J. Inactivation of foodborne viruses by emerging processing technologies. Institute of Food Technologists Annual Conference, Las Vegas, Nevada, June 26-28, 2012.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2012 Citation: Li, J. Attachment, internalization, and dissemination of human norovirus surrogates in Romaine lettuce. International Association of Food Protection Annual Meeting, Providence, Rhode Island, July 22-25, 2012.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2012 Citation: Hirneisen, K., and Kniel, K.E. Norovirus Survival on Spinach during Pre-harvest Growth. International Association for Food Protection Annual Meeting, Providence, Rhode Island, July 22-25, 2012 (T4-01).
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Herbst-Kralovetz, M.M., Radtke, A.L., Lay, M.K., Hjelm, B.E., Bolick, A.N., Sarker, S.S., Atmar, R.L., Kingsley, D.H., Arntzen, C.J., and Estes, M.K., Nickerson, C.A. 2013. Lack of norovirus replication and histo-blood group antigen expression in 3-dimensional intestinal epithelial cells. Emerg. Infect. Dis. 19:431-438.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Cacao, E., Sherlock, T., Nasrullah, A., Kemper, S., Knoop, J., Kourentzi, K., Ruchhoeft, P., Stein, G.E., Atmar, R.L., and Willson, R.C. 2013. Helium beam shadowing for high spatial resolution patterning of antibodies on microstructured diagnostic surfaces. Biointerphases. 8:9.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Rogers, J.D., Ajami, N.J., Fryszczyn, B.G., Estes, M.K., Atmar, R.L., and Palzkill, T. 2013. Identification and characterization of a peptide affinity reagent for the detection of noroviruses in clinical samples. J. Clin. Microbiol. 51:4803-1808 [Epub].
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Menon, V.K., George, S., Shanti, A.A., Saravanabavan, A., Samuel, P., Ramani, S., Estes, M.K., and Kang, G. 2013. Exposure to human and bovine noroviruses in a birth cohort in Southern India, 2002-2006. J. Clin. Microbiol. Apr 24 [Epub].
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Chapman, B., and Powell, D. 2013. Video observation and data coding methods to assess food handling practices at food service. Food Protection Trends.33:146-156.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2012 Citation: Noroviruses: Little Pathogens with a Big Impact. Institute of Food Technologists Annual Meeting 2012, Las Vegas, Nevada, June 28, 2012.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2012 Citation: Lee, A. Norovirus Cross-Contamination in Retail Food Service. International Association for Food Protection, Providence, Rhode Island, July 2012.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2012 Citation: Trivedi, T., DeSalvo, T., Lee, L., Palumbo, A., Moll, M.E., Curns, A.T., Hall, A.J., Patel, M., Parashar, U.D., and Lopman, B.A. Excess Hospitalizations and Mortality Associated with Norovirus Outbreaks in Nursing Homes - Oregon, Pennsylvania, and Wisconsin, 2009-2010. IDWeek (Joint meeting of IDSA, SHEA, HIVMA, and PIDS), San Diego, California, October 17-21, 2012.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2012 Citation: Li, J. High pressure inactivation of human norovirus in foods and environment. Presented at International Conference for Chemical Engineering, Ixatapa, Mexico, 2012.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2012 Citation: Hida, K., Kulka, M., and Papafragkou, E. Development of a rapid total nucleic acid extraction method for isolation of hepatitis A virus from fresh produce. Third Food and Environmental Virology Conference, Lisbon, Portugal, October 2012.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2013 Citation: Cannon, J.L. Norovirus Current Research and NoroCORE Activities. Center for Food Safety Annual Meeting, Georgia, March 6, 2013.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2012 Citation: Cannon, J.L., Erickson, M.C., and Habteselassie, M.Y. The likelihood of cross-contamination of head lettuce by E. coli O157:H7, Salmonella and norovirus during hand harvest and recommendations for glove sanitizing and use. Center for Produce Safety-UC Davis Annual Meeting, Davis, California, June 27, 2012.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2012 Citation: Wang, Q., Esseili, M.A., Zhang, Z., and Saif, L.J. Enhanced persistence of a food-borne enteric calicivirus in/on physically damaged lettuce. Proc. 31st American Society for Virology Annual mtg, Abstract #P23-19, Madison, Wisconsin, July 21-25, 2012.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2013 Citation: Leshem, E., Barclay, L., Wikswo, M., Gregoricus, N., Vinj�, J. Parashar, U., Hall, A. Emergence of GI.6 Norovirus - United States, 2009-2012. Epidemic Intelligence Service Conference, Atlanta, Georgia, April 22-26, 2013.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2013 Citation: Simmons, O. attended Southeast Regional Vegetable Growers meeting, Savannah, Georgia, January 10-11, 2013.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2013 Citation: Simmons, O. attended 39th Annual East Coast Commercial Fishermens and Aquaculture Trade Exposition, Ocean City, Maryland, January 18-20, 2013.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2012 Citation: Hirneisen, K., Markland, S.,Wang, Q., and Kniel, K.E. Enteric Virus Survival on Alfalfa Seeds and Sprouts. American Phytopathological Society Human Pathogens on Plants Workshop, Hyattsville, Maryland, February 13-15, 2012.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2012 Citation: Beaulieu, S.M. An Integrated Modeling Platform for Human and Ecological Exposure and Risk in Multimedia Environmental Systems (HE2RMES). Society of Toxicology, Workshop on Multi-scale Integration of Human Health and Environmental Data. RTP, North Carolina, May 8-11, 2012.


Progress 06/01/11 to 05/31/12

Outputs
OUTPUTS: Activities: In Project Year 1, the Molecular Virology Core activities focused on developing an vitro cultivation method for human noroviruses (HuNoV), developing microarrays for foodborne virus (FBV) genotyping, and evaluating emerging human norovirus (HuNoV) surrogates. The Detection Core has been developing novel ligands for use in capturing FBV from complex samples like feces and foods, as well as establishing standard operating procedures (SSOPs) for virus detection. The Epidemiology and Risk Analysis Core is combining clinical and laboratory-based capacity, and engaging medical and public health professionals, so that it is possible to better characterize the endemic and epidemic burden of FBV disease. This core is also developing mathematical models to estimate the economic costs and risks associated with FBVs. During Year 1, the efforts of the Prevention and Control Core focused on evaluating novel surface sanitizers for removal/inactivation of HuNoV from fresh produce, and investigating emerging food processing technologies for their potential antiviral efficacy. The Extension and Outreach Core is working to improve understanding and expand use of measures to reduce FBV disease risks as a function of commodity, by first characterizing audience knowledge so as to create appropriate training materials for audience-specific stakeholders. Capacity Building Core efforts focus on student training and fostering communications amongst the group. Events: The project Executive Board met twice in Year 1. Team members presented scientific findings at the following venues: 2011 annual meetings of the International Association for Food Protection (IAFP), American Society for Virology, Infectious Disease Society of America, International Conference on Antimicrobial Agents and Chemotherapy, International Conference on Emerging Infectious Disease, and the University of Georgia Center for Food Safety. Presentations were also made at the 2012 biennial meeting of the Conference for Food Protection; Noro2012; Western Food Safety Summit; National Advisory Committee on Microbiological Criteria for Foods (NACMCF); and by invitation at various other venues. The team was officially represented at meetings of the Produce Safety Alliance (PSA); Interstate Shellfish Sanitation Conference (ISSC); FoodCORE Vision meeting; and Epidemic Intelligence Service (EIS) Conference. Products: During the reporting period, the Collaborative produced a jointly shared Food Virology Literature Database; invention disclosures and patents and/or applications relative to levulinic acid as an antiviral agent, and peptides, synbodies, and nucleic acid aptamers as HuNoV capture and detection ligands. Our website was launched (http://norocore.ncsu.edu/). Dissemination and outreach: Official Industry and Government Scientific Advisory Committees were formed and the goals/strategies to be employed by the project have been shared with them. Other stakeholders were identified and contacted through one-on-one communication with relevant professional and trade associations. PI Jaykus was extensively interviewed subsequent to public announcement of funding in July, 2011. PARTICIPANTS: The organizational structure of the USDA-NIFA Food Virology Collaborative (NoroCORE) consists of institutional tiers. At the highest level is PI Lee-Ann Jaykus of North Carolina State University (NCSU). Dr. Jaykus manages the day-to-day operations of the project, including facilitating communications; managing financial aspects; interfacing with the funding agency and industry/government advisory committees; and representing the group as a whole. Other NCSU faculty members with NoroCORE involvement include Benjamin Chapman, David Green, Trevor Phister, and Christopher Gunter. The NoroCORE administrative staff at NCSU consists of Malakai Erskine (administrative director); Catherine Gensel (communications specialist); O.D. Simmons (research assistant professor); and Christina Moore (curriculum development specialist). Laboratory-based research efforts at NCSU are headed by senior researcher staff members Helen Rawsthorne, Blanca Escudero-Abarca, and Rebecca Goulter. Currently, 4 NCSU graduate students are supported on the project. At the next organizational tier are the institutions with which the co-PDs are affiliated (8 in total). The co-PDs lead the Collaboratives six core functions. The role of the cores is to shape the project scientific plan; identify and prioritize key activities in research, extension, and training; manage the progress of projects; and serve as a liaison and representative for core activities. The lead (Dr. Jaykus) and core PDs also constitute the NoroCORE Executive Committee. The Molecular Virology core is directed by Jan Vinje [U.S. Centers for Disease Control and Prevention (CDC)] and Mary Estes (Baylor College of Medicine). The Detection core is directed by Robert Atmar (Baylor College of Medicine) and Jennifer Cannon (University of Georgia). The efforts of the Epidemiology and Risk Analysis core are coordinated by Christine Moe (Emory University), Aron Hall (CDC), and Stephen Beaulieu (Research Triangle Institute International). The Prevention and Control core is directed by Alvin Lee [University of Illinois and the National Institute of Food Safety and Health] and Leonard Williams (North Carolina A&T State University). The Extension and Outreach core is coordinated by Angela Fraser of Clemson University, in collaboration with Dr. Moe of Emory. Finally, the activities of the Capacity Building core are directed by both Dr. Jaykus and Li-An Yeh of North Carolina Central University. At the third tier are the institutions housing the Collaborating Investigators, including: Kali Kniel (University of Delaware); Richard Linton, Linda Saif, and Jianrong Li, and Qiahong Wang (The Ohio State University); Robert Mandrell (USDA Agricultural Research Service); Charles Arntzen (Arizona State University); Jason Jiang (Cincinnati Childrens Hospital); and Donald Schaffner (Rutgers University). Several state health departments and VA medical centers are involved in the project. A full accounting of all the project participants is beyond the scope of this narrative, but additional details are available on request. TARGET AUDIENCES: Stakeholder engagement is a common theme in all NoroCORE activities. Formalized extension and outreach activities are designed to improve understanding and expand use of measures to reduce viral foodborne disease (FBD) risks as a function of commodity. The three major commodity groups identified for NoroCORE efforts are the (i) fresh produce, (ii) molluscan shellfish, and (iii) retail/institutional food sectors. From a broader perspective, three major audiences are being targeted for communications programs: (i) food safety and public health professionals; (ii) food industry professionals (food production, processing, retail, and foodservice); and (iii) consumers. Initial (Year 1) efforts at stakeholder engagement focused on identifying members of the formal Industry and Government Advisory Committees. The role of the advisory committees is to chart the course of the project; provide advice on research, training, and extension/outreach efforts; review project outcomes; and aid in evaluating program success. Multiple stakeholder engagement meetings are being planned for project year 2, both with the formal advisory committees as well as with the broader stakeholder community. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.

Impacts
In this reporting period, Collaborative investigators produced promising preliminary results suggesting the potential to propagate HuNoV on stem cell-derived human intestinal organoids, taking us one step closer to a cultivable human strain. A first generation prototype high density microarray was produced for genotyping HuNoV. Investigators also evaluated two novel cultivable surrogates (porcine sapovirus and Tulane virus) for their physico-chemical stabilities. While neither surrogate fully mimicked the behavior of HuNoV, each may be used on a case-by-case basis, thereby increasing the potential tools for studying the environmental behavior of these viruses. An expert panel was convened to preliminarily identify SSOPs for virus detection in complex sample matrices. The Detection Core produced antibodies, small peptide ligands, and nucleic acid aptamers that are being further evaluated for specificity, broad reactivity, and binding affinity in preparation for their use in facilitating HuNoV capture from complex samples. The epidemiological infrastructure and laboratory capacity necessary to support studies to evaluate the endemic and epidemic burden of FBV disease has been established. The Prevention and Control core have demonstrated that a levulinic acid formulation is a promising method for inactivating viral contamination on gloves and food processing surfaces in the fresh produce harvesting and processing environment. On the other hand, investigators demonstrated the physico-chemical basis for the high degree of resistance of HuNoV and their surrogates to ionizing radiation and high pressure, suggesting that these alternative food processes are not likely to effectively inactivate viruses if used alone. The Extension and Outreach core has designed sampling protocols and surveys targeting the consumer, retail, and public health sectors which will be used to assess baseline knowledge/practice before implementing educational interventions. Information on FBV has been incorporated as part of Good Agricultural Practices (GAPs) curricula for the fresh produce industry. Capacity Building activities have included cross-training between collaborators, establishment of a more formalized mechanism to promote protocol and reagent exchange, and implementation of an undergraduate internship program, with a focus on training historically underrepresented populations. We also have developed a Food Virology curriculum that will form the basis for training at the graduate level. These outcomes are illustrated by tangible end-products that include many peer-reviewed publications; >15 graduate students in training; a jointly shared Food Virology literature database; a functional website that is continuously updated to provide up-to-date information on foodborne viruses; and the high degree of synergy between the Collaborative members, including free exchange of expertise and ideas between basic and applied science researchers, as well as those involved directly in extension, outreach, and education activities. A formal plan to evaluate these interactions, as well as those with stakeholders, has been put in place.

Publications

  • Desai, R., Hembree, C.D., Handel, A., Matthews, J.E., Dickey, B.W., McDonald, S., Hall, A.J., Parashar, U.D., and Lopman, B. 2012. Severe outcomes are associated with genogroup 2 genotype 4 norovirus outbreaks: A systematic literature review. International Conference on Emerging Infectious Diseases (ICEID), Atlanta, Georgia, March 11-14, 2012
  • Hall, A.J., Curns, A.T., McDonald, L.C., Parashar, U.D., and Lopman, B.A. 2011. The roles of norovirus and Clostridium difficile among gastroenteritis deaths in the United States, 1999 -2007. 49th Annual Meeting of the Infectious Disease Society of America (IDSA), Boston, Massachusetts, October 20-23, 2011
  • Cannon, J.L., Erickson, M.C., and Habteselassie, M.Y. 2012. The likelihood of cross contamination of head lettuce by E. coli O157:H7, Salmonella and norovirus during hand harvest and recommendations for glove sanitizing and use. Western Food Safety Summit, Hartnell College, Salinas, California, May 10, 2012
  • Smith, C.B., Roache, K.F., Ma, C., Hung, Y.C., and Cannon, J.L. 2012 Norovirus and hepatitis A virus inactivation on stainless steel and gloves by electrolyzed oxidizing water and levulinic acid plus SDS. Center for Food Safety Annual Meeting, 2012, Atlanta, Georgia, March 6, 2012
  • Smith, C.B., Ma, C., Roache, K.F., Mantri, V., Habteselassie, M., Gaskin, J.W., Harrison, J.A., and Cannon, J.L. 2012. Are organisms that can cause foodborne illness suppressed in organically managed soils Georgia Organics Annual Meeting, Columbus, Georgia, February 25, 2012
  • Bolton, S.L., Smith, C.B., Roache, K.F., Kotwal, G., Gaskin, J.W., Harrison, M.A., Tate, R.I., Harrison, J.A., and Cannon, J.L. How produce washing and sanitizing food preparation counters can help prevent foodborne illnesses from viruses and bacteria. Georgia Organics Annual Meeting, Columbus, Georgia, February 25, 2012
  • Cannon, J.L. 2012. Recommendations to prevent cross-contamination during hand harvest. Western Food Safety Summit, Hartnell College, Salinas, California, May 11, 2012
  • Arntzen, C. 2012. Norovirus: The Modern Scourge of Food and Family. Invited symposium participant at AAAS Annual meetings, Vancouver, British Columbia, February 17, 2012
  • Takanashi, S., Saif, L.J., Hughes, J.H., Meulia, T., Jung, K., Scheuer, K., and Wang, Q. 2012. Attempts to propagate human noroviruses in three-dimensional cell cultures. Proc. Noro2012-Norovirus and other viruses on the rise, Lubeck, Germany, March 20-22, 2012 (P30)
  • Hall AJ. 2012. Epidemiology and infectivity of norovirus. Center for Food Safety Annual Meeting, Atlanta, Georgia, March 6-7, 2012
  • Hall AJ. 2012. Norovirus epidemiology: Burden, attribution, and surveillance. Conference for Food Protection Workshop: Controlling Norovirus and Other Viruses at Retail and Food Service, Indianapolis, Indiana, April 14, 2012
  • Jaykus, L. 2012. Noroviruses at retail: Current challenges and future opportunities. Conference for Food Protection Workshop: Controlling Norovirus and Other Viruses at Retail and Food Service, Indianapolis, Indiana, April 14, 2012
  • Escudero-Abarca, B.I., Rawsthorne, H., Gensel, C. and Jaykus, L.A. 2012. Persistence and Transferability of Noroviruses on and between Common Surfaces and Foods. J. Food Prot.75:927-935.
  • Li, J., Predmore, A. Divers, E., and Lou, F. 2012. New interventions against human norovirus: progress, opportunities, and challenges. Ann. Rev. Food Sci. Technol. 3:331-352.
  • Li, D., Baert, L., Xia, M., Zhong, W., Van Coillie, E., Jiang, X., and Uyttendaele, M. 2012. Evaluation of methods measuring the capsid integrity and/or functions of noroviruses by heat inactivation. J. Virol. Meth. 181(1):1-5.
  • Shanker, S., Choi, J.M., Sankaran, B., Atmar, R.L., Estes, M.K., and Prasad, B.V. 2011. Structural analysis of HBGA binding specificity in a norovirus GII.4 epidemic variant: implications for epochal evolution. 30th Annual Meeting of the American Society for Virology, Minneapolis, Minnesota, July 16-20, 2011 (W26-3)
  • Shanker, S., Choi, J.M., Sankaran, B., Estes, M.K., Atmar, R.L., and Prasad, B.V. 2011. Structural analysis of HBGA binding specificity in a norovirus GII.4 epidemic variant: Implications for epochal evolution. International Union of Microbiological Society Congress, Sapporo, Japan, October 12-17, 2011
  • Muhaxhiri, Z., Shanker, S., Song, Y., Palzkill, T.G., Estes, M.K., and Prasad, B.V. 2011. Structural basis for substrate specificity and protease inhibition in Norwalk virus protease. 30th Annual meeting of the American Society for Virology, Minneapolis, Minnesota, July 16-20, 2011 (W26-5)
  • Hall, A.J., Curns, A.T., McDonald, L.C., Parashar, U.D., and Lopman, B.A. 2012. Gastroenteritis Deaths on the Rise in the United States: The Emerging Roles of Clostridium difficile and Norovirus. International Conference on Emerging Infectious Diseaess (ICEID), Atlanta, Georgia, March 11-14, 2012
  • Hall, A.J., Arvelo, W., Estevez, A., Parashar, U.D., and Lindblade, K.A. 2012. Population-Based Surveillance for Norovirus in Guatemala: Estimation of Disease Burden and Clinical Severity. International Conference on Emerging Infectious Diseaess (ICEID), Atlanta, Georgia, March 11-14, 2012
  • Wang, Q., Zhang, Z. and Saif, L.J. 2012. A cultivable porcine sapovirus surrogate for human caliciviruses: stability and attachment to lettuce. Appl. Environ. Microbiol. 78:3932-40.
  • Cannon, J.L. 2012. A comparison of human norovirus recovery using magnetic beads coated with porcine gastric mucins, saliva or monoclonal antibodies. Southern Section AOAC Annual Meeting, Atlanta, Georgia, May 1, 2012
  • Wang, Q., Downer, S.J., Erickson, M.C., Ortega, Y.R., and Cannon, J.L. 2011. Cross-contamination of Fresh Produce and Kitchen Utensils by Norovirus and Hepatitis A Virus during Preparation. International Association for Food Protection Annual Meeting, Milwaukee, Wisconsin, August 1, 2012
  • Wikswo, M.E., and Hall, A.J. 2012. A novel surveillance system for person-to-person enteric disease outbreaks, United States. International Conference on Emerging Infectious Diseases (ICEID), Atlanta, Georgia, March 11-14, 2012
  • Kang. G., Estes, M.K., and Atmar, R.L. 2011. Calicivirus infections. In: R.L., Guerrant, D.H. Walker, and P.F. Weller (eds.), Tropical Infectious Diseases 3rd edition. Saunders/Elsevier, St Louis, MO. p. 411-415.
  • Clarke, I.N., Estes, M.K., Green, K.Y., Hansman, G.S., Knowles, N.J., Koopmans, M.K., Matson, D.O., Meyers, G., Neill, J.D., Radford, A., Smith, A.W., Studdert, M.J., Thiel, H.J. and Vinje, J. 2012. Caliciviridae. In: A.M.Q. King, M. J. Adams, E.B. Carstens, and E. Lefkowitz (eds.), Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. Academic Press, London, U.K. p. 977-986.
  • Payne, D.C., Shaparov, U., Hall, A.J., and Hu, D.J. 2011. Foodborne viruses. In: O.A. Oyarzabal and S. Backert (eds.), Microbial Food Safety: An Introduction. Springer, New York, NY. p. 73-94.
  • Le Guyader, F.S., Atmar, R.L., and Le Pendu, J. 2012. Transmission of viruses through shellfish: when specific ligands come into play. Curr. Opin. Virol., 2:103-110.
  • Hall, A.J. 2012. Noroviruses: The perfect human pathogens J. Infect. Dis., 205(11):1622-1624.
  • Lopman, B., Gastanaduy, P., Park, G.W., Hall, A.J., Parashar, U.D., and Vinje, J. 2012. Environmental transmission of norovirus gastroenteritis. Curr. Opin. Virol., 2(1):96-102.
  • Vega, E., Barclay, L., Gregoricus, N., Williams, K., Lee, D., and Vinje, J. 2011 CaliciNet: A novel surveillance network for norovirus gastroenteritis outbreaks in the United States. Emerg. Infect. Dis. 17(8):1389-1395.
  • Lopman, B., Gastanaduy, P., Park, G.W., Hall, A.J., Parashar, U.D., and Vinje, J. 2011 Environmental transmission of norovirus gastroenteritis. Curr. Opinion Virol. 2:1-7
  • Lindesmith, L., Debbink, K., Swanstrom, J., Vinje, J., Costantini, V., Baric, R., and Donaldson, E. 2012. Monoclonal antibody based antigenic mapping of Norovirus GII.4-2002. J. Virol. 86(2):873-83
  • Bresee, J.S., Marcus, R., Venezia, R.A., Keene, W.E., Morse, D., Thanassi, M., Brunett, P., Bulens, .S, Beard, R.S., Dauphin, L.A., Slutsker, L., Bopp, C., Eberhard, M., Hall, A., Vinje, J., Monroe, S.S., Glass, R.I. and the U.S. Acute Gastroenteritis Etiology (AGE) Study Team. 2012. The etiology of severe acute gastroenteritis among adults visiting emergency departments in the United States. J. Infect. Dis. 205(9):1374-1381.
  • Liu, P., Hill, V.R., Hahn, D., Johnson, T.B., Pan, Y., Jothikumar, N. and Moe, C.L. 2012. Hollow-fiber ultrafiltration for simultaneous recovery of viruses, bacteria and parasites from reclaimed water. J. Microbiol. Methods 88:155-161.