Source: UNIV OF MINNESOTA submitted to
DECONTAMINATION OF FOOD AND FOOD-PROCESSING SURFACES FROM VIRAL AND BACTERIAL PATHOGENS BY COLD PLASMA TECHNOLOGY
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
TERMINATED
Funding Source
Reporting Frequency
Annual
Accession No.
1011938
Grant No.
2017-67017-26172
Project No.
MINV-62-051
Proposal No.
2016-10275
Multistate No.
(N/A)
Program Code
A1331
Project Start Date
Feb 1, 2017
Project End Date
Jan 31, 2020
Grant Year
2017
Project Director
Goyal, S.
Recipient Organization
UNIV OF MINNESOTA
(N/A)
ST PAUL,MN 55108
Performing Department
Veterinary Population Medicine
Non Technical Summary
Foodborne pathogens are a major concern to food manufacturers, consumers, and governments since they are the cause of frequent foodborne gastroenteritis outbreaks which plague public health as well as world economies. Fresh produce and ready-to-eat foods are the most implicated foods in these outbreaks indicating the need for exploring novel non-thermal technologies for decontaminating food without causing adverse effects on their nutritive and organoleptic qualities. Most of the available non-thermal techniques are either non-effective or adversely affect the quality of treated food. Poultry and poultry products are another source of foodborne outbreaks especially for bacterial pathogens. Chemical disinfection used in poultry industry unfortunately affects the quality of meat besides restrictions on the use of chemicals in food industry. The cold atmospheric-pressure gaseous plasma (CGP) has shown promising antibacterial potential with minimal effect on food quality. Recently, we reported strong virucidal effects of CGP against foodborne viruses. However, CGP technology is still in its infancy and there is a need to design new CGP devices that are more efficient and cost-effective. In this proposal we propose to optimize conditions for in situ decontamination of foods and food-contact surfaces from viral and bacterial pathogens using our unique two dimensional air-based micro-discharge plasma array (2D-AMPA), which is efficiently biocidal and more cost-effective. We will compare this 2D-AMPA source with two previously described plasma sources and with UV-irradiation. Also, we will study the impact of 2D-AMPA on the nutritive and organoleptic qualities as well as the chemical safety of CGP-treated foods.
Animal Health Component
50%
Research Effort Categories
Basic
30%
Applied
70%
Developmental
0%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
72332601101100%
Knowledge Area
723 - Hazards to Human Health and Safety;

Subject Of Investigation
3260 - Poultry meat;

Field Of Science
1101 - Virology;
Goals / Objectives
Objectives: In situ decontamination of foods and food-contact surfaces from viral and bacterial pathogens with cold gaseous plasma (CGP) generated by a unique two dimensional air-based micro-discharge plasma array (2D-AMPA) and to compare this novel plasma source with two previously described plasma sources and with a non-thermal non-plasma based antimicrobial method.Specific aims:Aim 1: To in situ optimize the virucidal and bactericidal activities of our unique 2D-APMA on foodborne pathogens e.g., hepatitis A virus (HAV), human Norovirus (NoV), Campylobacter jejuni, and Salmonella enterica serovar Heidelberg. Aim 2: To study the changes in nutritive value and quality attributes of CGP-treated foods to ensure that there is no negative effect on food palatability, organoleptic properties, and nutritive value.Aim 3: Compare the virucidal and bactericidal efficacy of our 2D-APMA setup with two other plasma sources that have been used previously and a well-established non-thermal non-plasma based method e.g., ultraviolet light.
Project Methods
Plasma source: The 2D-APMA (Figure 4) operates in filtered air at atmospheric pressure. The electrode geometry consists of two unequal ultra-thin metal electrodes, nickel and gold, which are coated and separated by 500 μm thick layer of alumina, consistingof 105 through-holes, arranged in a grid-like array and evenly distributed in a 6.25 cm2 total area (25×25 mm). Each hole has a diameter of 600 μm, in which the discharge is created. The coaxial-hollow micro discharge source is embedded in a polytetrafluoroethane holder attached to a polycarbonate tube to allow for an air flow and the electrical connections. The sinusoidal high voltage (HV) signal at 20 kHz is generated by an AC power source. The discharge power is measured by Lissajous figure analysis of the high voltage and the charge in the discharge (66). The airflow through the source is measured and controlled by a rotameter. The discharge has been intensively tested in static air up to approximately 100 standard liter per minute. It also operates in Ar -O2 mixtures or pure N2 allowing to (at least partly) controlling the reactive oxygen and nitrogen species production.Strain 255 of FCV, strain P3 of MNV-1, and strain HM175 of HAV will be used. FCV, MNV, and HAV will be propagated and titrated in Crandell-Reese feline kidney (CRFK) cells, RAW 264.7 cells (ATCC TIB-71), and FRhK-4, (ATCC CRL-1688) cells, respectively.Virus titration: For FCV titration, 50% tissue culture infective dose (TCID50) method described in (2) will be used while MNV and HAV will be titrated by plaque assay method as described in (19, 49). For human NoV which cannot be grown and titrated perfectly in cell culture (56), we will use a quantitative reverse transcript PCR (qRT-PCR) technique for NoV titration.Preparation and titration of bacterial cultures: Isolates of S. Heidelberg and C. jejuni will be cultured and enumerated by the methods described in (35, 80). Briefly, frozen cultures from both will be revived and cultured in tryptic soy broth (TSB) medium overnight at 37°C incubator in anaerobic packs. For enumeration, 10-fold serial dilutions of each bacterium will be prepared in buffered peptone water (BPW) followed by plating on tryptic soy agar (TSA) using the pour plate technique. The plates will be incubated at 37°C for 24 -48 h before counting the number of colonies. When using antibiotic-resistant bacterial strain, a corresponding antibiotic will be added to the medium.Sample preparation for tests: Two food and three food-contact surfaces will be used for performing the in situ study on the virucidal effects of cold plasma. Lettuce leaves and fresh strawberry will be used as models for fresh-eaten vegetables. In addition, stainless steel, plastic, and wood specimens will be sued as models of food-processing surfaces. The protocols of survival study of viruses will start by spreading ~5-6 log unit µL (in volumes ≤ 20 µL) of each virus stock on small discs or squares of the tested surface (plastic, wood and stainless steel) or food sample (Lettuce leaves and strawberry fruit) After drying in biosafety cabinet, the samples will be exposed to cold plasma at certain level combination of the tested factors based on the RSM design. Viruses will be eluted from samples by vortex and shaking in elution buffer (3% beef extract-0.05M glycine solution pH 7.2). The eluents will be titrated and viral inactivation will be determined by the difference between titers of treated and untreated (control) viruses.For antibacterial experiments, the same steps mentioned above with viruses will be followed with some modification. The initial counts of bacterial cells will be adjusted using a 0.5 McFarland turbidity standard and then ~5-6 log CFU will be deposited on the surface of the tested sample (plastic, wood, stainless steel, lettuce leaves, strawberry, chicken breast meat, and red meat). After drying and plasma exposure at the tested condition the survived bacterial cells will be recovered from the surface of samples using BPW and then enumerated as mentioned above.Especially for bacteria we will study in a separate experiment the effect of the bacterial growth stage on the bactericidal activity of plasma. In this regard, we will grow the bacterial cultures for different times (28, 10, and 14 h) to prepare the tested cultures at stationary phase, mid-exponential phase, and late-exponential phase, respectively. Then use the same steps mentioned above to test each culture at the optimal operational conditions.Organoleptic analysis of plasma-treated vegetable samples - A consumer taste panel will be used to compare the sensory quality of vegetable samples with and without cold plasma treatment. Sensory analysis tests will be carried out using 10 panelists in individual booths with white illumination. The volunteers will be recruited from the staff and students of University of Minnesota for the sensory panel. Five each of lettuce leaves and strawberry will be served in dishes coded with random three-digit numbers, and panelists will be asked to evaluate samples for appearance, color, odor, texture-touch, taste, and overall appearance and acceptability, using a 1-10 scale. Evaluations will be made for each sample with respect to overall acceptance and appearance. The sensory results will be analyzed by two-factor (panelist and product) ANOVA test.Color change measurement - A portable spectrophotometer, CM-600 d (Konica Minolta, USA) will be used for the color analysis of raw and treated vegetables.Surface morphology- Scanning electron microscopy (SEM) analysis will be done following the method of Keskinen et al., with minor modifications. Food samples (1 × 1 cm) with and without 2D-APMA treatment will be fixed with 1.0 ml 2.5% glutaraldehyde. The samples will be rinsed twice with 3 ml 0.1 M imidazole and then dehydrated in 50%, 80%, and absolute ethanol. Samples will be further dried in a critical point drying apparatus using liquid CO2. The samples will be mounted on stubs and sputter-coated with a thin layer of gold. They will be then observed using a scanning electron microscope with an accelerating voltage of 5-10 kV in the high vacuum, in the secondary electron imaging mode.Nutritive value - To determine the effect of cold plasma on nutritive value of foods under investigation, vitamin C will be determined in treated and non-treated foods using AOAC method #985.33.Chemical safety of treated foods-Determination of nitrate and nitrite in treated foods- Concentration of nitrite and nitrate in plasma treated and untreated food will be determined using the method described by Jackson and Dilli (54) based on high-performance liquid chromatography.Determination of N-nitrosamines in meat- Concentrations of N-nitrosamines in plasma treated and untreated meat samples will be determined by liquid extraction combined with gas chromatography-methanol chemical ionization/mass spectrometry described by Scheeren et al. (96). As an alternative method we may use gas chromatographic method of Jurado-Sánchez et al. (58).Using the same RSM methodology we will optimize the biocidal activities of Dyn-A-Mite and ns pulsed plasma sources and UV irradiation system. We will perform this pre-comparison optimization step on feline calicivirus and S. Heidelberg on lettuce leaves only. Then, using the optimal operational conditions of each source we will compare the virucidal and bactericidal efficacy of all of them against the other pathogens and the impact on nutritive and sensory qualities of all selected foods (lettuce, strawberry, chicken breasts, and red meat). The same methods described above in Aim 1 and 2 will be used for conducting this study. We will use a UV source and treatment as described in Fino and Kniel, (43) and Rodriguez-Romo and Youssef (91).

Progress 02/01/17 to 01/31/20

Outputs
Target Audience: Food technology and food safety scientists, students, and researchers. Food industry professionals. Cold plasma technology specialists, scientists, students, and researchers. We reached the above-mentioned communities though our publications, educational presentations and seminars and through our contributed and invited/plenary presentation in several scientific and professional meetings. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? The team of SMG provided research training for six months to two visiting Scholars: -Yan Feng: Zhejiang Provincial Center for Disease Control and Prevention, China. -Angie Quinonez: College of Food, Agricultural and Natural Resource Sciences-University of Minnesota through the program of MAST International. The team of SMG provided research training for three month to a Scholar (Taylor Westfall- McCoy) belonging to the University of Minnesota TRIO Ronald E. McNair Scholars Program. http://www.cehd.umn.edu/events/7130/ The team of PJB provided research training to graduate students of Mechanical engineering on the foods and agricultural applications of CAP. Student names are: Ankit Moldgy and Gaurav Nayak). The team of PJB provided training to a group of capstone design students (seniors in Mech. Eng) for developing a batch reactor for plasma decontamination. The names of these trainees are: Jude Sauve, Albert Hubbard, Keegan O`Donnell and Yeeleng Thao. How have the results been disseminated to communities of interest?The results have been disseminated to communities of interest though our publications, educational presentations and seminars and through our contributed and invited/plenary presentations in several scientific and professional meetings. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? Achievements We completed cultural, morphologic, molecular, and proteomics studies to understand the biological impacts of Argon/oxygen-based radio frequency plasma jet setup on the viral capsid and viral genome that lead to inactivation of FCV in liquids. We found that cold argon-oxygen plasma species oxidizes and disintegrates the capsid protein of feline calicivirus. We built a two-dimensional air-based coaxial microhollow dielectric barrier discharge plasma setup (remote 2D-DBD setup) and studied the effects of its operational parameters on inactivation of feline calicivirus (FCV), as a surrogate of human norovirus. Based on this study we identified the operational parameters that show efficient inactivation of viral pathogen. We performed a plasma diagnostic study to identify the reactive species responsible for the inactivation of FCV by the remote 2D-DBD setup. It was found that humidity of the bio?sample for gas?phase treatment in dry air is required to achieve >5 log10 reduction in FCV titer within 3 min. The gas?phase FCV inactivation was found to be due to a combination of ozone (O3) and reactive nitrogen species (RNS). We optimized a quantitative molecular method [ethidium monoazide-coupled RT-qPCR (EMA-RT-qPCR)] for determining human norovirus inactivation by cold plasma. Then we studied the in-situ virucidal efficacy of the air-based remote 2D-DBD plasma setup against human norovirus GII.4 and FCV on stainless steel and Romaine lettuce leaves. The remote 2D-DBD plasma was effective on both FCV and HuNoV GII.4. However, the log reduction in HuNoV observed by EMA-RT-qPCR was lower than that of FCV measured by cell culture titration. To assess this discrepancy, we studied CAP's effect on FCV by the cell culture method and by the EMA-coupled RT-qPCR method. It was found that the molecular titration method (EMA-RT-qPCR) underestimates the level of virus reduction by cold plasma. We also found that fecal matter residues in HuNoV samples were responsible for partial suppression of cold plasma efficacy against HuNoV. We studied the efficacy of cold atmospheric-pressure plasma (CAP), generated by the air-based remote 2D-DBD plasma setup, against a multi-drug resistant strain of Salmonella enterica serovar Heidelberg (SH) on stainless steel, romaine lettuce, and chicken breast. Cold plasma showed high efficacy against SH on all tested surfaces. Complete inactivation was achieved on stainless steel and lettuce but for longer treatment time. However, complete inactivation on chicken breasts was not achieved during 10min exposure. \The differences in the topology and nature of these three surfaces explained this observed difference in efficacy. We designed and built three other plasma generation sources to allow comparison of inactivation efficacies of different plasma sources. These sources are: -Direct Dielectric Barrier Discharge; -Gliding arc plasma setup; and -Volumetric remote DBD batch box setup ? Volumetric remote DBD batch box setupWe performed a comprehensive comparative study on virucidal efficacy of three different dielectric barrier discharge (DBD) setups operating in air versus UV-C treatment using FCV. Significant enhancement of the energy efficiency was achieved with a lab?scale batch reactor prototype, which employed surface DBD, leading to similar energy per unit area requirements as that for UV?C. A key advantage of plasma over UV?based disinfection systems is that plasmas are not limited by shadowing effects. Nonetheless, unlike UV?C, the virucidal efficacy of plasma is significantly reduced for dry samples and remote plasma treatment is only effective against wet samples. We conducted a study to understand how each plasma source inactivates viruses and bacteria; and to identify differences in plasma produced reactive species and how these differences correlate to differences in biocidal effect of each plasma source. We completed a comparative study on the germicidal efficacy of the remote DBD plasma setup and the gas phase ozone treatment against a wide spectrum of viral and bacterial pathogens on stainless steel surface. The study was conducted to ensure the efficiency of our plasma technology against several pathogens that might contaminate surfaces. In addition, we wanted to confirm that the mode of disinfection by plasma does depend only on ozone (generated in plasma process) but also on other generated species such as nitrogen species which makes plasma distinct and even more efficient. We tested both technologies against: -Five bacteria including Gram positive and Gram negative, aerobic and microaerophilic, non-drug resistant and drug resistant bacteria e.g., Escherichia coli, Bacillus subtilis, Micrococcus luteus, Salmonella enterica, and Campylobacter jejuni. - Six viruses including foodborne and waterborne, enveloped and nonenveloped, RNA and DNA viruses e.g., feline calicivirus (FCV), Tulane virus (TuV), hepatitis A virus (HAV), SA-11 rotavirus, poliovirus, and porcine reproductive and respiratory syndrome virus (PRRSV). One of our main objectives was to reduce the energy consumption of plasma treatment to facilitate the adoption of this technology by the industry. Based on our understanding of the inactivation pathways of viral and bacterial pathogens by the remote DBD plasma setup, we designed and built a novel remote batch reactor of intermittently operated plasma, which consumes minimal energy for complete inactivation of viral and bacterial pathogens on food and food contact surfaces. We optimized operational conditions of the new batch reactor for efficient germicidal effect and studied the virucidal and bactericidal efficacy against FCV and E. coli on stainless steel, iceberg lettuce, Romaine lettuce, and spinach. We found that the new batch reactor is efficient in inactivating FCV and E. coli on steel lettuce and spinach. We observed differences between he germicidal efficacies on Romaine and Iceberg lettuce. We performed sample treatments for a study on the safety of CAP-treated foods by tracking the changes in the chemical structure of the macromolecules of foods such as carbohydrates, proteins, and lipids employing liquid chromatography and mass spectrometric techniques. This work is in collaboration with Dr. Chi Chen, Food Science and Nutrition Department, University of Minnesota. We performed a proteomic study on FCV and TuV treated by the remote DBD plasma to understand its impact on viral capsid proteins that lead to viral inactivation. The results of this study will help us understand the mode of action of CAP virucidal activity in relation to its underlying plasma chemistry that we studied previously. This work has been done in collaboration with Dr. LeeAnn Higgins, Center for Mass Spectrometry and Proteomics, College of Biological Sciences, University of Minnesota. The data analysis is pending the waiting list schedule of submitted samples to the lab.

Publications

  • Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: P. Bruggeman. Peter Mark Memorial Award Lecture: Plasma-bio Interactions: Investigating Mechanisms to Enable New Applications, AVS 65th International Symposium and Exhibition, October 21-26, 2018, Long Beach, CA, USA
  • Type: Conference Papers and Presentations Status: Published Year Published: 2019 Citation: Moldgy, A.; Nayak, G.; Aboubakr, H. A.; Goyal, S. M.; and Bruggeman, P. J. (2019). On the comparison of direct and remote plasma treatment with UV disinfection for virus inactivation. 24th International Symposium on Plasma Chemistry. Naples (Italy), June 9-14, 2019.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2019 Citation: Bruggeman P.J., Plasma-liquid interactions: fundamental studies elucidating biomedical and environmental applications, XL Annual Meeting of Brazilian Vacuum Society (CBrAVIC), October 7-10, 2019, State University of Sao Paulo, Guaratinguet�, Brazil - invited presentation.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2019 Citation: Moldgy A., G. Nayak, A.H. Aboubakr, S.M. Goyal and P.J. Bruggeman, The influence of surface humidity on disinfection using cold plasmas, IEEE Pulsed Power and Plasmas Conference, June 23-28, 2019, Orlando, Florida, USA  invited presentation.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Nayak, G., Aboubakr, H. A., Goyal, S. M., & Bruggeman, P. J. (2017). Reactive species responsible for the inactivation of feline calicivirus by a two?dimensional array of integrated coaxial microhollow dielectric barrier discharges in air. Plasma Processes and Polymers. DOI:10.1002/ppap.201700119
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Aboubakr, H. A., Mor, S. K., Higgins, L., Armien, A., Youssef, M. M., Bruggeman, P. J., & Goyal, S. M. (2018). Cold argon-oxygen plasma species oxidize and disintegrate capsid protein of feline calicivirus. PloS one, 13(3), e0194618.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Aboubakr, H. A., Parra, F. S., Collins, J., Bruggeman, P., & Goyal, S. M. (2020). �n situ inactivation of human norovirus GII. 4 by cold plasma: Ethidium monoazide (EMA)-coupled RT-qPCR underestimates virus reduction and fecal material suppresses inactivation. Food Microbiology, 85, 103307.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Aboubakr, H. A., Nisar, M., Nayak, G., Nagaraja, K. V., Collins, J., Bruggeman, P. J., & Goyal, S. M. (2020). Bactericidal Efficacy of a Two-Dimensional Array of Integrated, Coaxial, Microhollow, Dielectric Barrier Discharge Plasma Against Salmonella enterica Serovar Heidelberg. Foodborne Pathogens and Disease, 17(3), 157-165.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Moldgy, A., Aboubakr, H., Nayak, G., Goyal, S., & Bruggeman, P.(2020). Comparative evaluation of the virucidal effect of remote and direct cold air plasmas with UV?C. Plasma Processes and Polymers, e1900234.
  • Type: Journal Articles Status: Under Review Year Published: 2020 Citation: Moldgy, A., Nayak, G., Aboubakr H.A., Goyal, S.M, and Bruggeman, P.J. (2020) Inactivation of virus and bacteria using cold atmospheric pressure air plasmas and the role of reactive nitrogen species. Journal of Physics D: Applied physics (Under review)
  • Type: Journal Articles Status: Other Year Published: 2020 Citation: Aboubakr, H. A., Moldgy, A., Bruggeman, P. J., & Goyal, S. M. (2020). Comparative germicidal efficacies of cold atmospheric-pressure air plasma and gas phase ozone treatment against a wide spectrum of viral and bacterial pathogens. (In preparation to be submitted to Food Control)
  • Type: Theses/Dissertations Status: Published Year Published: 2017 Citation: Aboubakr, H.A. Decontamination of food and food-processing surfaces from norovirus by cold atmospheric-pressure gaseous plasma. Department of Veterinary Population Medicine, College of Veterinary Medicine, University of Minnesota. December 2017
  • Type: Theses/Dissertations Status: Published Year Published: 2019 Citation: Moldy, A. Surface decontamination using cold atmospheric pressure plasma, MS thesis  University of Minnesota. June 2019
  • Type: Conference Papers and Presentations Status: Published Year Published: 2017 Citation: Aboubakr H.A.; Nisar M.; Nagaraja K.V.; Collins J.; Bruggeman P.J.; & Goyal S.M. (2017). Decontamination of chicken breast meat, romaine lettuce, and stainless steel surfaces from a multidrug-resistant strain of Salmonella enterica serovar Heidelberg using a 2D- air based DBD plasma microdischarge array. The Annual Meeting of International Association for Food Protection (IAFP), Tampa, Florida, USA. July 9-12, 2017. https://iafp.confex.com/iafp/2017/webprogram/Paper15478.html
  • Type: Conference Papers and Presentations Status: Published Year Published: 2017 Citation: Aboubakr H.A., Nayak G., Collins J., Bruggeman P.J., Goyal S.M. (2017). Decontamination of food and food contact surfaces from human norovirus GII 4 using a novel 2D air-based microdischarge cold plasma array. 2017-ASM Biothreats: Research, Response and Policy. February 6-8, Washington DC. http://www.abstractsonline.com/pp8/#!/4357/presentation/725
  • Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: Bruggeman, P.J. (2017) Plasma water vapor kinetics and plasma-liquid interactions, International Conference on Physics of Low Temperature Plasma, June 5-9, 2017, Kazan, Russia (plenary speaker).
  • Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: Bruggeman, P.J. (2017) Towards an understanding of plasma-liquid interactions in plasma medicine, 10th EU-Japan Joint Symposium on Plasma Processing, December 4-7, 2017, Bankoku Shinryokan, Okinawa, Japan (invited presentation)
  • Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: Bruggeman, P.J. (2017) Plasma-liquid interactions: multiphase transport, 14th International Conference on Flow Dynamics (ICFD2017), November 1-3, 2017, Sendai, Japan (invited speaker).
  • Type: Conference Papers and Presentations Status: Published Year Published: 2017 Citation: Aboubakr H.A; Westfall-MCcoy T.; Nayak G.; Bruggeman P.; Goyal S. (2017) Cold plasma for decontamination of chicken breast, romaine lettuce, and stainless steel surfaces from multi-drug resistant salmonella enterica serovar Heidelberg. Poster presentation, Twenty- Sixth Annual McNair Scholars Poster Presentation & Reception, Coffman Memorial Union, University of Minnesota. (August 3rd 2017) http://www.cehd.umn.edu/assets/docs/trio/posters/Westfall-McCory2017FinalPoster.pdf
  • Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: Aboubakr H.A.; Nisar M.; Nagaraja K.V.; Collins J.; Bruggeman P.J.; & Goyal S.M. Cold plasma for decontamination of chicken breast meat and other food and food-contact surfaces from a multidrug-resistant strain of Salmonella enterica serovar Heidelberg. Poster Presentation, Point of Pride Research Day, College of Veterinary Medicine, University of Minnesota. (October 4, 2017)
  • Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: Aboubakr H.A.; Collins J.; Bruggeman P.J.; Goyal S.M. Factors affecting the virucidal activity of cold atmospheric pressure gaseous plasma against human norovirus on food and food-processing surfaces. Poster Presentation, Point of Pride Research Day, College of Veterinary Medicine, University of Minnesota. (October 4, 2017).
  • Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: Aboubakr H.A.; Nisar M.; Nagaraja K.V.; Collins J.; Bruggeman P.J.; & Goyal S.M. (2018). The nature of treated food and initial bacterial cell load influence the antibacterial efficacy of cold atmospheric-pressure plasma against a multidrug-resistant strain of Salmonella enterica serovar Heidelberg. 3rd International Conference on One Medicine One Science (iCOMOS). Minneapolis, MN, USA. April 29-May 2, 2018.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2017 Citation: Nayak G., Aboubakr H.A., Goyal S.M. & Bruggeman P.J. (2017). Inactivation of feline calicivirus (FCV) by 2D-array of micro-discharges in air on metal surface and in solution. 23rd International Symposium on Plasma Chemistry (ISPC), July 3- August 4 2017, Montr�al, Canada.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: Moldgy, A.; Aboubakr H.; Nayak, G.; Goyal M.S.; Bruggeman P. (2018). Biocidal efficacy of non-equilibrium plasma sources: a comparative study. The 45th IEEE International Conference on Plasma Science (ICOPS 2018). June 24-28, 2018, Denver, Colorado, USA.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: Nayak, G.; Aboubakr H.; Nayak, G.; Goyal M.S.; Bruggeman P. (2018). Role of reactive nitrogen species in Inactivation of feline calicivirus using Two-dimensional array of microdischarges in air. 45th IEEE International Conference on Plasma Science (ICOPS 2018). June 24-28, 2018, Denver, Colorado, USA.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: Aboubakr H.A.; Yang, Y.; Collins J.; Bruggeman P.J.; & Goyal S.M. (2018). Factors affecting the virucidal efficacy of cold plasma against HuNoV as compared to its surrogate, feline calicivirus. The annual meeting of International Association for Food Protection (IAFP), Salt Lake City, Utah, USA. July 8-11, 2018.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: P. Bruggeman, Invited presentation: Plasma-bio interactions: Linking plasma-induced liquid phase chemistry with the biological impact of plasma, MRS 2018 Material Research Society Fall Meeting and Exhibit, November 25-30, 2018, Boston, Massachusetts, USA


Progress 02/01/18 to 01/31/19

Outputs
Target Audience: Food technology and food safety scientists, students, and researchers. Food industry professionals. Cold plasma technology specialists, scientists, students, and researchers. Co-PI Bruggeman established and launched as responsible editor for plasmas in Journal of Physics D: Applied Physics an initiative on Advances in Plasmas for a Sustainable Future with as goal to provide larger visibility of exciting research in this area which include plasmas for agricultural applications and food systems. The initiative is managed by two newly appointed topic editors and a special issue on plasmas in agriculture and food systems is planned. We reached the above-mentioned communities though our publications, educational presentations and seminars and through our contributed and invited/plenary presentations in several scientific and professional meetings. Changes/Problems: 1. Because of the recent exploration of a method to grow human norovirus on human enteroid cells (Ettayebi, et al., 2016), we thought to adopt that technique to test the efficacy of CAP against human norovirus itself using this novel technique. Currently we are in the process of getting our post-doc trained on this technique. He will be visiting the lab of Mary Estes, Department of Molecular Virology and Microbiology, Baylor College of Medicine, Texas. Ref. 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. and Kou, B., 2016. Replication of human noroviruses in stem cell-derived human enteroids. Science, p.aaf5211. 2. We recently found that in some conditions the humidification process of the substrate, (we showed previously in the framework of this project that a humid substrate is important for effective plasma-induced) decontamination, can impact the decontamination efficacy. We plan to perform some more detailed experiments to assess this effect quantitatively as we believe this can be crucial in the determination of optimal plasma treatment conditions. What opportunities for training and professional development has the project provided? The team of PI Sagar Goyal provided research training for six months to two visiting Scholars: Yan Feng: Zhejiang Provicial Center for Disease Control and Prevention, China. Angie Quinonez: College of Food, Agricultural and Natural Resource Sciences-University of Minnesota through the program of MAST International. The team of co-PI Bruggeman provided research training to two graduate students in Mechanical engineering (Ankit Moldy and Gaurav Nayak) on the foods and agricultural applications of CAP. The team of co-PI Bruggeman provided training to a group of capstone design students (seniors in Mech. Eng) for developing a batch reactor for plasma decontamination. The trainees were Jude Sauve, Albert Hubbard, Keegan O`Donnell and Yeeleng Thao. How have the results been disseminated to communities of interest?The results havebeen disseminated to communities of interestthough our publications, educational presentations and seminars and through our contributed and invited/plenary presentations in several scientific and professional meetings. What do you plan to do during the next reporting period to accomplish the goals?Future Work. Developing optimized treatment protocol using the new designed batch reactor design with the remote DBD plasma against various pathogens (viruses and bacteria) on various food and food-contact surfaces. This optimization includes minimizing energy consumption, decontamination efficacy and minimizing off target effects on food samples. We will study the changes in nutritive value and quality attributes of CAP-treated foods to ensure that there is no negative effect on food palatability, organoleptic properties, and nutritive value. Finalizing some of the ongoing work and prepare unpublished results obtained this year for publication.

Impacts
What was accomplished under these goals? Foodborne pathogens are a major concern to food manufacturers, consumers, and governments since they are the cause of frequent foodborne gastroenteritis outbreaks, which plague the public health as well as world economies. Consumption of contaminated food results in one illness per 10 people and leads to 420,000 deaths every year as estimated by WHO, 2015. Human norovirus (HuNoV) is the leading cause of gastroenteritis outbreaks linked to contaminated food in the US and worldwide (CDC, 2017). About 50% of all foodborne disease outbreaks due to a single known cause reported to the Centers for Disease Control and Prevention, are attributed to HuNoV. Globally, HuNoV is responsible for 685 million gastroenteritis cases including 200 million cases among children <5 years old (CDC, 2017). The annual global economic burden of HuNoV was estimated to be $4.2 billion in direct health system costs and $60.3 billion in societal costs. In the United States, HuNoV is one of the top five pathogens with respect to the total cost of foodborne illnesses. It causes 19-21 million cases of acute gastroenteritis annually in the U.S. including 1.7-1.9 million outpatient visits, 400,000 emergency room visits, 56,000-71,000 hospitalizations, and 570-800 deaths, mostly among young children (CDC, 2017). Fresh produce and leafy vegetables are the most commonly implicated foods in HuNoV outbreaks. Unfortunately, studies on a variety of foods have revealed that non-thermal and minimal food processing (freezing, cooling, salting, and mild heat treatment) have low inactivation efficiency against foodborne viruses. This represents a critical barrier to ensuring the safety of fresh produce. Similarly, poultry and poultry products are another source of foodborne outbreaks especially for bacterial pathogens such as Salmonella spp. and Campylobacter spp. In the U.S., 1.2 million illnesses were caused by salmonellosis, which resulted in 19,000 hospitalizations and 380 deaths annually. There is thus a real and urgent need for alternative approaches and technologies to destroy microbial pathogens on contaminated poultry, production surfaces, and other foods. There is thus a real and urgent need for alternative approaches and technologies to destroy microbial pathogens on contaminated poultry, production surfaces, and other foods. Cold atmospheric-pressure gaseous plasmas (CAPs) are ionized gases, which are driven by high electric fields, and are often referred to as "the fourth state of matter". CAP is a proposed non-thermal technology that has shown promising antibacterial potential with minimal effect on food quality. . With the framework of this USDA-NIFA grant, we showed strong virucidal effects of CAP against foodborne viruses and Salmonella on food surfaces. We are in the process of optimizing conditions for in-situ decontamination of foods and food-contact surfaces from viral and bacterial pathogens using our unique two dimensional air-based plasma micro-discharge plasma array (2D-APMA). Preliminary comparative studies with other plasma sources and UV look very promising. During the last year of the grant, we will study the impact of 2D-AMPA on the nutritive and organoleptic qualities as well as the chemical safety of CAP-treated foods. Specific aims of the project: Aim 1: To in situ optimize the virucidal and bactericidal activities of our unique 2D-APMA on foodborne pathogens e.g., hepatitis A virus (HAV), human Norovirus (NoV), Campylobacter jejuni, and Salmonella enterica serovar Heidelberg. Aim 2: To study the changes in nutritive value and quality attributes of CGP-treated foods to ensure that there is no negative effect on food palatability, organoleptic properties, and nutritive value. Aim 3: Compare the virucidal and bactericidal efficacy of our 2D-APMA setup with two other plasma sources that have been used previously and a well-established non-thermal non-plasma based method e.g., ultraviolet light. Achievements We completed a study on inactivation of bacteria on food substrates. The study evaluated the impact of morphology and composition of treated food and the initial bacterial count on CAP's bactericidal efficacy. We designed and built three other plasma generation sources to allow comparison of inactivation efficacies of different plasma sources. These sources are: Direct Dielectric Barrier Discharge Gliding arc plasma setup Volumetric remote DBD setup We performed a comprehensive-comparative study between virucidal and bactericidal efficacies of all plasma setups versus UV-C treatment using various pathogens (i.e. FCV, TuV, HAV and Salmonella enterica Heidelberg). An initial assessment on energy efficiency was performed. We conducted a study to understand how each plasma source inactivates viruses and bacteria; and to identify differences in plasma produced reactive species and how these differences correlate to differences in biocidal effect of each plasma source. One of our main objectives is to reduce the energy consumption of plasma treatment to facilitate the adoption of this technology by industry. Based on our current understanding of the inactivation pathways of viral and bacterial pathogens by the remote DBD plasma setup, we designed a novel remote batch reactor of plasma and are in the process of developing a treatment protocol. The protocol is being developed for the batch reactor to allow for minimal energy efficiency for complete inactivation of viral and bacterial pathogens on food and foods. We found preliminary promising plasma decontamination conditions with potential for food treatment that we will further explore towards optimized implementation and minimum effect on organoleptic properties on food samples.

Publications

  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Aboubakr, H.A., Mor, S.K., Higgins, L., Armien, A., Youssef, M.M., Bruggeman, P.J. and Goyal, S.M., 2018. Cold argon-oxygen plasma species oxidize and disintegrate capsid protein of feline calicivirus. PloS one, 13(3), p.e0194618.
  • Type: Journal Articles Status: Under Review Year Published: 2018 Citation: Aboubakr H.A.; Sampedro F.; Collins J.; Bruggeman P.J. & Goyal S.M. (2018). In situ inactivation of human norovirus GII-4 by cold plasma: ethidium monoazide (EMA)-coupled RT-qPCR underestimates virus reduction and fecal material suppresses inactivation. Food Microbiology (Under review)
  • Type: Journal Articles Status: Submitted Year Published: 2018 Citation: Aboubakr, H.A.; Nisar, M.; Nayak, G.; Nagaraja, K.V.; Collins, J.; Bruggeman, P.J.; and Goyal, S.M. Bactericidal efficacy of a 2-D array integrated coaxial microhollow DBD plasma discharge against Salmonella enterica serovar Heidelberg. Food Control (Submitted)
  • Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: Aboubakr H.A.; Nisar M.; Nagaraja K.V.; Collins J.; Bruggeman P.J.; & Goyal S.M. (2018). The nature of treated food and initial bacterial cell load influence the antibacterial efficacy of cold atmospheric-pressure plasma against a multidrug-resistant strain of Salmonella enterica serovar Heidelberg. 3rd International Conference on One Medicine One Science (iCOMOS). Minneapolis, MN, USA. April 29-May 2, 2018.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: Moldgy, A.; Aboubakr H.; Nayak, G.; Goyal M.S.; Bruggeman P. (2018). Biocidal efficacy of non-equilibrium plasma sources: a comparative study. The 45th IEEE International Conference on Plasma Science (ICOPS 2018). June 24-28, 2018, Denver, Colorado, USA.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: Nayak, G.; Aboubakr H.; Nayak, G.; Goyal M.S.; Bruggeman P. (2018). Role of reactive nitrogen species in Inactivation of feline calicivirus using Two-dimensional array of microdischarges in air. The 45th IEEE International Conference on Plasma Science (ICOPS 2018). June 24-28, 2018, Denver, Colorado, USA
  • Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: Aboubakr H.A.; Yang, Y.; Collins J.; Bruggeman P.J.; & Goyal S.M. (2018). Factors affecting the virucidal efficacy of cold plasma against HuNoV as compared to its surrogate, feline calicivirus. The annual meeting of International Association for Food Protection (IAFP), Salt Lake City, Utah, USA. July 8-11, 2018.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: P. Bruggeman, Invited presentation: Plasma-bio interactions: Linking plasma-induced liquid phase chemistry with the biological impact of plasma, MRS 2018 Material Research Society Fall Meeting and Exhibit, November 25-30, 2018, Boston, Massachusetts, USA
  • Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: P. Bruggeman. Peter Mark Memorial Award Lecture: Plasma-bio Interactions: Investigating Mechanisms to Enable New Applications, AVS 65th International Symposium and Exhibition, October 21-26, 2018, Long Beach, CA, USA


Progress 02/01/17 to 01/31/18

Outputs
Target Audience: Food technology and food safety scientists, students, and researchers. Food industry professionals. Cold plasma technology specialists, scientists, students, and researchers. We reached the above-mentioned communities though our publications, educational presentations and seminars and through our contributed and invited/plenary presentation in several scientific and professional meetings. Changes/Problems:When we in-situ tested the virucidal efficacy of 2D-APMA against HuNoV GII-4, lower efficacy was observed as compared to its efficacy against feline calicivirus. To investigate the reasons for this difference, two hypotheses were formulated: i) the presence of organic fecal impurities in the HuNoV sample competes with the viral particles to interact with CAP reactive species and ii) the EMA-RT- qPCR method underestimates viral inactivation. Inactivation of FCV by CAP as determined by cell culture method was compared to inactivation of FCV and HuNoV-GII-4 as determined by EMA- RT-qPCR method. In addition, CAP-inactivation of FCV suspended in distilled water (free of fecal impurities) was compared to that of FCV-suspended in fecal extract mimicking the conditions in which HuNoV was treated. The results showed that the inactivation of FCV determined by cell culture method was higher than that determined by the EMA-RT-qPCR method for the same sample indicating that the latter method (used for HuNoV titration) underestimates the amount of virus inactivated. We also found that fecal impurities present in HuNoV samples partially suppress the virucidal activity of CAP. What opportunities for training and professional development has the project provided? Nothing Reported How have the results been disseminated to communities of interest?We reached the above-mentioned communities though our publications, educational presentations and seminars and through our contributed and invited/plenary presentation in several scientific and professional meetings. What do you plan to do during the next reporting period to accomplish the goals?1- We will compare the virucidal and bactericidal efficaciesof fourdifferent cold plasma setups including the 2D-APMA as a reference. 2- We will study the bactericidal efficacy of 2D-APMA setup against a multidrug-resistant strain ofCampylobacter jejunion various food and food-contact surfaces. 3-The influenceof the nature of treated food and the initial bacterial count on CAP's bactericidal efficacy will be studied.

Impacts
What was accomplished under these goals? Foodborne pathogens are a major concern to food manufacturers, consumers, and governments since they are the cause of frequent foodborne gastroenteritis outbreaks, which plague the public health as well as world economies. Consumption of contaminated food results in one illness per 10 people and leads to 420,000 deaths every year as estimated by WHO, 2015. Human norovirus (HuNoV) is the leading cause of gastroenteritis outbreaks linked to contaminated food in the US and worldwide (CDC, 2017). About 50% of all foodborne disease outbreaks due to a single known cause reported to the Centers for Disease Control and Prevention, are attributed to HuNoV. Globally, HuNoV is responsible for 685 million gastroenteritis cases including 200 million cases among children <5 years old (CDC, 2017). The annual global economic burden of HuNoV was estimated to be $4.2 billion in direct health system costs and $60.3 billion in societal costs. In the United States, HuNoV is one of the top five pathogens with respect to the total cost of foodborne illnesses. It causes 19-21 million cases of acute gastroenteritis annually in the U.S. including 1.7-1.9 million outpatient visits, 400,000 emergency room visits, 56,000-71,000 hospitalizations, and 570-800 deaths, mostly among young children (CDC, 2017). Fresh produce and leafy vegetables are the most commonly implicated foods in HuNoV outbreaks. The high number of outbreaks linked to fresh produce is due to surface cross-contamination of such foods through contact with fecal contaminated soil and irrigation water or due to low sanitation in post-harvest processing environments including infected food handlers and/or contaminated equipment (cutting boards, knives, and working surfaces). Contemporary consumer desires to eat foods with high nutritive value, which has resulted in a high demand for fresh produce and leafy vegetables. The sales of fresh produce are increasing each year; packaged salad is the second- fastest-selling item in U.S. following bottled water. This has led to an increased risk of HuNoV outbreaks, which has necessitated the development of so called non-thermal technologies. Unfortunately, studies on a variety of foods have revealed that non-thermal and minimal food processing (freezing, cooling, salting, and mild heat treatment) have low inactivation efficiency against foodborne viruses. This represents a critical barrier to ensuring the safety of fresh produce. Poultry and poultry products are another source of foodborne outbreaks especially for bacterial pathogens such as Salmonella spp. and Campylobacter spp. In the U.S., 1.2 million illnesses were caused by salmonellosis, which resulted in 19,000 hospitalizations and 380 deaths annually. Salmonella Heidelberg (SH) is the most common serovar found in retail poultry. Antimicrobial drug resistance in this serovar is notable and has increased in recent years. Campylobacter is one of the most common causes of diarrheal illness in the United States. An estimated 2.1 to 2.4 million cases of human campylobacteriosis (illnesses ranging from loose stools to dysentery) occur each year. About 14 cases are diagnosed each year for each 100,000 persons in the US population. It has been estimated that approximately 76 persons with Campylobacter infections die each year. Deaths from C. jejuni infection are rare and occur primarily in infants, the elderly, and patients with other underlying illnesses. Most cases of campylobacteriosis are associated with eating raw or undercooked poultry meat or from cross-contamination of other foods or water by these items. Contamination rates of Campylobacter spp. on poultry purchased at retail establishments in the United States and the United Kingdom range from 68% to 83%. One way to combat food and food animal contamination with Campylobacter, Salmonella, and other multidrug resistant bacteria is the application of a comprehensive control strategy in poultry farms, slaughter houses and food processing plants. Although various processes have been proposed to eliminate or substantially decrease bacterial populations on poultry carcasses, most of these approaches have not been completely acceptable because of the problems of chemical residues, discoloration of chicken carcasses, and/ or high cost associated with limited effectiveness. Chlorine rinses generally are used during processing of poultry for pathogen reduction but is coming under increasing scrutiny by regulators because of toxicity issues and disinfection by-products. Therefore, there is a real and urgent need for alternative approaches and technologies to destroy microbial pathogens on contaminated poultry, production surfaces, and other foods. Cold atmospheric-pressure gaseous plasmas (CAPs) are ionized gases, which are driven by high electric fields, and are often referred to as "the fourth state of matter". CAP is a proposed non-thermal technology that has shown promising antibacterial potential with minimal effect on food quality. Recently, we reported strong virucidal effects of CAP against foodborne viruses. However, CAP technology is still in its infancy and there is a need to design new CAP devices that are more efficient and cost-effective. With this USDA-NIFA grant, we plan to optimize conditions for in-situ decontamination of foods and food-contact surfaces from viral and bacterial pathogens using our unique two dimensional air-based plasma micro-discharge plasma array (2D-APMA) which is more biocidal-efficient and more cost-effective. We will compare this source with two previously described plasma sources and with UV-irradiation. Also, we will study the impact of 2D-AMPA on the nutritive and organoleptic qualities as well as the chemical safety of CGP-treated foods. Specific aims: Aim 1: To in situ optimize the virucidal and bactericidal activities of our unique 2D-APMA on foodborne pathogens e.g., hepatitis A virus (HAV), human Norovirus (NoV), Campylobacter jejuni, and Salmonella enterica serovar Heidelberg. Aim 2: To study the changes in nutritive value and quality attributes of CGP-treated foods to ensure that there is no negative effect on food palatability, organoleptic properties, and nutritive value. Aim 3: Compare the virucidal and bactericidal efficacy of our 2D-APMA setup with two other plasma sources that have been used previously and a well-established non-thermal non-plasma based method e.g., ultraviolet light. Achievements Built a two-dimensional air-based plasma microdischarge array (2D-APMA) setup. The effects of the 2D-APMA operational parameters on inactivation of feline calicivirus, as a surrogate of human norovirus, were studied. A quantitative molecular method for determining human norovirus inactivation by cold plasma was optimized. The in-situ virucidal activity of 2D-APMA against human norovirus GII-4 on stainless steel and Romaine lettuce leaves was studied. Performed comparison of virucidal efficacy of cold plasma with that of ultraviolet light C using direct and indirect exposures. Decontamination of chicken breast and Romaine lettuce leaves from a multidrug-resistant strain of Salmonella enterica serovar Heidelberg was successfully performed. Two additional plasma sources (direct DBD and remote DBD) have been constructed and are ready to be tested and compared.

Publications

  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Nayak, G., Aboubakr, H. A., Goyal, S. M., and Bruggeman, P. J. (2017). Reactive species responsible for the inactivation of feline calicivirus by a two?dimensional array of integrated coaxial microhollow dielectric barrier discharges in air. Plasma Processes and Polymers. DOI:10.1002/ppap.201700119
  • Type: Journal Articles Status: Under Review Year Published: 2018 Citation: Aboubakr, H. A., Mor, S., Higgins, L., Armien, A., Youssef, M.M., Bruggeman, P. J., and Goyal, S. M. (2018). Cold argon-oxygen plasma species oxidize and disintegrate capsid protein of feline calicivirus. PlosOne (under review).
  • Type: Theses/Dissertations Status: Awaiting Publication Year Published: 2017 Citation: Aboubakr, H.A. (2017). Decontamination of food and food-processing surfaces from norovirus by cold atmospheric-pressure gaseous plasma. VMed Graduate Program, Department of Veterinary Population Medicine, College of Veterinary Medicine, University of Minnesota.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2017 Citation: Aboubakr H.A.; Nisar M.; Nagaraja K.V.; Collins J.; Bruggeman P.J.; & Goyal S.M. (2017). Decontamination of chicken breast meat, romaine lettuce, and stainless steel surfaces from a multidrug-resistant strain of Salmonella enterica serovar Heidelberg using a 2D- air based DBD plasma microdischarge array. The Annual Meeting of International Association for Food Protection (IAFP), Tampa, Florida, USA. July 9-12, 2017. https://iafp.confex.com/iafp/2017/webprogram/Paper15478.html
  • Type: Conference Papers and Presentations Status: Published Year Published: 2017 Citation: Nayak G., Aboubakr H.A., Goyal S.M. & Bruggeman P.J. (2017). Inactivation of feline calicivirus (FCV) by 2D-array of micro-discharges in air on metal surface and in solution. 23rd International Symposium on Plasma Chemistry (ISPC), July 3- August 4 2017, Montr�al, Canada.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2017 Citation: Aboubakr H.A., Nayak G., Collins J., Bruggeman P.J., Goyal S.M. (2017). Decontamination of food and food contact surfaces from human norovirus GII 4 using a novel 2D air-based microdischarge cold plasma array. 2017-ASM Biothreats: Research, Response and Policy. February 6-8, Washington DC.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: Bruggeman, P.J. (2017) Plasma water vapor kinetics and plasma-liquid interactions, International Conference on Physics of Low Temperature Plasma, June 5-9, 2017, Kazan, Russia (plenary speaker).
  • Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: Bruggeman, P.J. (2017) Towards an understanding of plasma-liquid interactions in plasma medicine, 10th EU-Japan Joint Symposium on Plasma Processing, December 4-7, 2017, Bankoku Shinryokan, Okinawa, Japan (invited presentation)
  • Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: Bruggeman, P.J. (2017) Plasma-liquid interactions: multiphase transport, 14th International Conference on Flow Dynamics (ICFD2017), November 1-3, 2017, Sendai, Japan (invited speaker).
  • Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: Aboubakr H.A; Westfall-MCcoy T.; Nayak G.; Bruggeman P.; Goyal S. (2017) Cold plasma for decontamination of chicken breast, romaine lettuce, and stainless steel surfaces from multi-drug resistant salmonella enterica serovar Heidelberg. Poster presentation, Twenty-Sixth Annual McNair Scholars Poster Presentation & Reception, Coffman Memorial Union, University of Minnesota. (August 3rd 2017)
  • Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: " Aboubakr H.A.; Nisar M.; Nagaraja K.V.; Collins J.; Bruggeman P.J.; & Goyal S.M. Cold plasma for decontamination of chicken breast meat and other food and food-contact surfaces from a multidrug-resistant strain of Salmonella enterica serovar Heidelberg. Poster Presentation, Point of Pride Research Day, College of Veterinary Medicine, University of Minnesota. (October 4, 2017)
  • Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: " Aboubakr H.A.; Collins J.; Bruggeman P.J.; Goyal S.M. Factors affecting the virucidal activity of cold atmospheric pressure gaseous plasma against human norovirus on food and food-processing surfaces. Poster Presentation, Point of Pride Research Day, College of Veterinary Medicine, University of Minnesota. (October 4, 2017).