Source: UNIVERSITY OF CALIFORNIA, DAVIS submitted to
EVALUATION AND APPLICATION OF PRACTICES FOR CONTROLLING SALMONELLA IN NUTS AND NUT PRODUCTS
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
TERMINATED
Funding Source
OTHER GRANTS
Reporting Frequency
Annual
Accession No.
0219349
Grant No.
2009-51110-20146
Project No.
CA-D-FST-2035-OG
Proposal No.
2009-01951
Multistate No.
(N/A)
Program Code
111
Project Start Date
Sep 1, 2009
Project End Date
Aug 31, 2014
Grant Year
2009
Project Director
Harris, L. J.
Recipient Organization
UNIVERSITY OF CALIFORNIA, DAVIS
410 MRAK HALL
DAVIS,CA 95616-8671
Performing Department
Food Science and Technology
Non Technical Summary
This proposal is a collaboration among scientists from the University of California - Davis, University of Florida - Lake Alfred, and University of Georgia - Griffin and includes applied research and outreach aimed at reducing foodborne illness from consumption nuts and nut products. Once considered uncommon, outbreaks of salmonellosis from nuts and nut products have been recently recognized and may be underreported. Little is known about the ecology of Salmonella in nuts and their products. Our overall goal is to evaluate relative microbiological risk using three nut system models: peanuts, pecans, and pistachios selected for their distinct handling, lack of available data, broad applicability, and relevance to food safety. We propose to evaluate a range of commercial handling and treatment practices for their effects on infiltration, survival, growth, and inactivation of Salmonella in the model nuts. Factors affecting infiltration, survival during long-term storage, and inactivation during cleaning, conditioning, shelling, drying, and roasting will be studied. Results of these studies will be used for risk model development and for development of outreach training and publications. Information gained from this research will reveal the adequacy and appropriateness of practices currently used in the nut industry in terms of controlling and eliminating Salmonella in inshell nuts, nutmeats, and roasted nut products. This knowledge will form the scientific basis for the adequacy of or need to improve these practices. We will partner with the nut industry to disseminate this new information and to evaluate its application and implementation; ultimately improving the safety of these products.
Animal Health Component
(N/A)
Research Effort Categories
Basic
(N/A)
Applied
100%
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
7121211110034%
7121219110033%
7121830110033%
Knowledge Area
712 - Protect Food from Contamination by Pathogenic Microorganisms, Parasites, and Naturally Occurring Toxins;

Subject Of Investigation
1211 - Pecan; 1219 - Edible tree nuts, general/other; 1830 - Peanut;

Field Of Science
1100 - Bacteriology;
Goals / Objectives
Long-term Goal. This proposal integrates research and extension activities with a long-term goal to reduce foodborne illness associated with consumption of raw and processed nuts and nut-containing products. Our overall objective is to perform harvest and post-harvest microbiological risk assessments using three nut system models: peanuts, pecans, and pistachios. The specific objectives are: Objective 1. To identify points during harvest and post-harvest handling where Salmonella may be introduced or amplified. Objective 2. To evaluate the efficacy of sanitation procedures appropriate to the harvest and postharvest nut-handling environment and to develop scientifically-based recommendations based on these data. Objective 3. To evaluate the factors affecting the storage survival and thermal resistance of Salmonella in nuts. Objective 4. To disseminate, through workshops and on-line publications, practical nut-general and nut-specific best pre-and post-harvest handling practices that will minimize the risk of foodborne illness from consumption of nuts and nut products. The aim of this project is to evaluate a wide range of handling and treatment practices for their effects on infiltration, survival, growth, and inactivation of Salmonella on peanuts, pecans, and pistachios, and products produced from these nuts. Extrinsic and intrinsic factors affecting infiltration, survival during long-term storage, and inactivation during cleaning, conditioning, shelling, drying, and roasting processes commonly used in nut industries will be studied. Information gained from this research will reveal the adequacy and appropriateness of practices currently used in terms of controlling and eliminating Salmonella in in-shell nuts, nutmeats, and nut products. Modifications in some of these practices may be needed to assure that safety risks are minimal. Information gained from this research will reveal the adequacy and appropriateness of practices currently used in the nut industry in terms of controlling and eliminating Salmonella and will form the scientific basis for improving those practices, thereby reducing foodborne illness. The results of these studies will also provide tools for processors in particular to develop and validate their food safety programs.
Project Methods
Methods: Lack of adequate survival and inactivation data in nuts under different processing conditions hinders the ability to evaluate the relative risks of industry processes. Materials collected from pecan, pistachio and peanut growers, hullers/shellers or processors will be used in laboratory-based studies designed to mimic processing parameters. Special attention will be given to the influence of environmental humidity and moisture in test materials. A range of handling and treatment practices will be evaluated for their effects on amplification, infiltration, survival, and inactivation of Salmonella during hulling and/or shelling, drying and thermal processing particularly under conditions where cross-contamination may occur. These data will be used to identify risk reduction strategies that can be practically applied. Longer-term studies will be established first. Studies that require materials available only during harvest (e.g., pistachio or pecan hulls) will be limited to the fall but others such as thermal processing may be carried out at other times of the year. Laboratory-based studies are planned for year 1 and 2 with concurrent development of risk models. Extension activities will be carried out throughout the 3-year project but activities in years 2 and 3 will incorporate data generated from the research. Data will be analyzed using the appropriate statistical measures (ANOVA, T-test, etc) using statistical software to determine if statistically significant differences exist between different treatments. We will collaborate with nut industry organizations to both disseminate information (through joint workshops or webinars, preparation of extension materials) obtained from the proposed research and to evaluate the use of the information by industry members. The long-term impact of strategies developed for the nut industry would be a reduction in risks associated with Salmonella in raw and roasted (processed) peanuts, pecans, and pistachios and food products containing these nuts. This would include reductions in outbreaks, sporadic illnesses, and recalls. This impact can be realized through modifications of current harvesting, storage, and processing practices with the objectives of preventing contamination of nuts with Salmonella, applying treatments that will kill Salmonella, and protecting raw and post-processed nuts and nut products against contamination i.e., adhering to Good Agricultural Pratices and Good Manufacturing Practices. Simultaneously, interventions to achieve this goal would likely reduce risks associated with other foodborne pathogens, e.g., E. coli O157:H7. We have proposed to evaluate behavior change of the nut industry in collaboration with industry organizations. Selected individuals will be contacted several months post exposure to the workshops and to educational materials to determine behavior and organizational changes that have been made as a result of exposure, including whether any of the materials they received were used. Indicators will include knowledge gained, behavior change, and implementation of new safety controls.

Progress 09/01/09 to 08/31/14

Outputs
Target Audience: The US grows significant portions of the world supply of nuts. In 2009 when this proposal was written the annual value of almonds, pecans, pistachios, and peanuts was 2.4, 0.43, 0.59, and 1.1 billion U.S., respectively. By 2012 these figures had grown to 4.3, 0.48, 1.1, and 2.3 billion U.S., respectively. The target audience for this project was the U.S. nut industry but we placed particular emphasis on pecans, peanuts and pistachios to fill important data gaps. The information generated was also of use to FDA and state regulators and other academics. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? This project provided significant training and professional development for graduate students (full or partial support to 2 M.S. and 1 Ph.D.), postdoctoral scholars (1), undergraduate students (multiple) and technical support staff (10) at three universities. The training included gaining laboratory techniques, interacting with the tree nut industry, and preparing abstracts, posters, oral presentations, and manuscripts. How have the results been disseminated to communities of interest? Throughout this project we have published 15 relevant lay and 7 published, 1 submitted and 2 in preparation scientific papers, 3 book chapters, and 19 published abstracts. While not all of these publications were fully supported by the grant, all used materials or information generated from the grant. We established and maintained substantial relationships with key players in the peanut, pecan, and pistachio industries and have provided feedback to these industries by giving 66 presentations at industry association meetings and to state and federal regulators. While the presentations at these meetings did not exclusively cover materials generated by this grant, all included some of the research output supported by the grant. At the stakeholders request, most of the outreach to the pecan industry was provided by short presentations on a topic of narrow focus at an industry meeting or as publications in an industry magazine. In contrast, the pistachio industry preferred research regular updates at food safety committee meetings. In 2014 we also delivered a workshop on "Validation or the Pistachio Industry" that was attended with representatives of most of the companies in this industry. Although this grant was targeted to the pecan, peanut, and pistachio industries, we have reached out to an academic from Oregon State who is working with the hazelnut industry. We have provided guidance on methodology, shared strains, and invited them to attend the validation workshop. The hazelnut industry (which is primarily in Oregon) is actively supporting food safety research after an outbreak of E. coli O157:H7 gastroenteritis in 2010 and several recalls due to the isolation of Salmonella. Several unique opportunities arose during the grant period. In 2009 we organized a nut safety training for the California Food Emergency Response Team (both state and FDA regulators), in 2013 we organized a California tree nut tour for a small group of scientists from FDA CFSAN who were working on documents related to the Food Safety Modernization Act, and we presented to a larger group of scientists at FDA CFSAN in College Park, MD and at the CDC in Atlanta. We have developed extensive on-line resources for the tree nut industry including a webpage devoted to tree nut food safety (http://ucfoodsafety.ucdavis.edu/Nuts_and_Nut_Pastes/) that includes materials generated from this grant. In addition, in 2013 the FDA informed the tree nut industry that they would be developing a quantitative microbial risk assessment over the next 1 to 2 years: http://www.fda.gov/Food/NewsEvents/ConstituentUpdates/ucm361206.htm. As a research team we were asked by our stakeholders (pecan and pistachio industries) to assist in the preparation of formal comments to the FDA. These comments included significant amounts of the data generated from this grant (both published and unpublished data). Subsequent to submitting those comments in December 2013 we have prepared additional supporting documents that include raw data from several of the published manuscripts. We are using these same raw data sets to submit data, as appropriate to ComBase (http://www.combase.cc) an online and free resource for quantitative and predictive microbiology. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? The major goals of identifying points during harvest and post-harvest handling where Salmonella may be introduced or amplified, to identify sanitation procedures appropriate to the harvest and postharvest nut-handling environment, evaluate the factors affecting the storage survival and thermal resistance of Salmonella in nuts. These goals were met. Briefly: The effect of pathogen concentration and storage temperature on the survival of Salmonella, Listeria monocytogenes and Escherichia coli O157:H7 on shelled peanuts and pecans and in-shell pistachios was determined. Nuts were separately inoculated with cocktails of Salmonella, L. monocytogenes and E. coli O157:H7 and stored at -20, 4 and 23C. Populations of all three bacteria decreased 1 to 2 logs during the initial 72 h drying after inoculation. Time did not impact populations at -20 and 4C; Linear rates of decline at 23C ranged from 0.15 to 0.32 log CFU/g/30 days for Salmonella, 0.34 to 0.45 for E. coli O157:H7, and 0.55 to 1.17 for L. monocytogenes. The effectiveness of conditioning treatments was evaluated for killing Salmonella in and on immersion- and surface-inoculated inshell pecans. Treatment of immersion-inoculated, pecans in 400 ppm chlorine reduced Salmonella by not more than 1.6 log. Treatment of pecans for 1 min in 200 ppm chlorinated water, soaking in water for 2 h at 21C, and heating for 10 min at 85-95C reduced Salmonella by >5.1 log; <0.6 log CFU/g of Salmonella was not eliminated when nuts were treated for 15 min at 90C. ≥6.4 log reductions were achieved in water at 90 or 95C for 80 s; treatment of nuts containing 1.8 log CFU/g at 95ºC for 10 min did not eliminate the pathogen. Salmonella was more resistant to conditioning treatments when inshell pecans were immersion- rather than surface-inoculated or when inoculated inshell pecans were stored. Results emphasize the importance of following common commercial practices when validating the lethality of conditioning treatments. The effectiveness of hot air drying and dry roasting was evaluated for pecans. Hot air treatment of 2.8 to 4.1% and 10 to 11% immersion-inoculated pecan nutmeats at 120C for 20 min reduced the number of Salmonella by 1.2 to 1.3 and 1.9 to 2.0 log CFU/g, respectively. Regardless of moisture content, hot air treatment at 120ºC for 20 min failed to eliminate 0.77 log CFU/g Salmonella inoculated onto pecan halves. >7 log reductions were observed when dry pieces were dry roasted at 160C for 15 min. Treatment of halves at 140, 150, or 170C for 20,15, or 10 min, respectively reduced Salmonella by 5 log CFU/g. The pathogen was slightly more heat resistant in immersion-inoculated nutmeats than on surface-inoculated nutmeats. Exposure of immersion-inoculated pieces to peanut oil at 127 or 132C for 1.5 or 1 min, respectively or halves at 138C for 2 min reduced Salmonella by 5 log CFU/g; treatment of halves at 132C for 2.5 to 4 min did not always achieve this reduction. Hot air treatment cannot be relied upon to reduce Salmonella by 5 log CFU/g on raw pecan nutmeats without changing sensory qualities. Treatment temperatures and times typically used to oil nutmeats appear to be sufficient to reduce Salmonella by 5 log CFU/g. Hot air heating was also evaluated for inshell pistachios. A 10-minute pretreatment with water or a saturated salt solution (applying salt brine prior to roasting is common) was also evaluated. Significantly greater reductions of Salmonella (about 1 log) were observed with the water pretreatment but not with the saturated salt pretreatment. The efficacy of aqueous (aQUAT) and isopropyl alcohol-based (ipQUAT) quaternary ammonium sanitizers on Salmonella, E. coli O157:H7, and L. monocytogenes populations on peanut and pistachio shell pieces was evaluated at 30C for 48 h. On peanut shells, the populations of all three pathogens increased from 3 to 5 log CFU/g when mixed with water and aQUAT. When ethanol or ipQUAT was added, these populations decreased 3 to 5 log CFU/g. On pistachio shells, Salmonella and E. coli O157:H7 increased 2 to 3 log CFU/g in water and aQUAT. When ethanol or ipQUAT was added, populations decreased by 2 to 4 log CFU/g, Population levels of L. monocytogenes did not change in water, while all other treatments decreased >5 log CFU/g. Studies were done to evaluate the efficacy of chlorine (200 - 1,000 microgram/ml), lactic acid (0.5 to 2 percent), levulinic acid (0.5 to 2 percent), sodium dodecyl sulfate (SDS, 0.05 percent), lactic acid plus SDS, levulinic acid plus SDS, and a mixed peroxyacid sanitizer (Tsunami 200, 80 microgram/ml) in killing Salmonella on/in immersion- and on surface-inoculated pecan nutmeats (USDA medium pieces and mammoth halves). Reductions did not exceed 1.1 log CFU/g of immersion-inoculated pieces and halves, regardless of sanitizer concentration or treatment time (up to 20 min). Reductions on surface-inoculated pieces and halves were 0.7 to 2.7 and 1.2 to 3.0 log CFU/g, respectively. Exposure of immersion-inoculated pecan pieces to chlorine (200 ppm), lactic acid (2 percent) and levulinic acid (2 percent) (with and without SDS), and Tsunami 200 (80 ppm) during intermittent vacuum and ambient atmospheric pressure treatments for up to 20 min reduced Salmonella by only 0.1 - 1.0 log CFU/g. In nut processing facilities where dust from shells exists as a possible source of cross contamination, ipQUAT should be used over aQUAT for sanitizing in the presence of dust. Once the edible nut is contaminated, the effectiveness of sanitizer treatments to eliminate Salmonella is minimal and survival on inshell nuts and their kernels is significant especially at cooler temperatures. The rate of decline of Salmonella is greater than that of either E. coli O157:H7 or L. monocytogenes at ambient storage temperatures; at 4 and -20C populations did not decline during storage. The knowledge generated through this research was extensively communicated to the target audience through industry and scientific presentations, workshops and lay and scientific publications.

Publications

  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Beuchat, L. R., D. A. Mann, and W. Q. Alali. 2012. Evaluation of sanitizers for inactivating Salmonella on in-shell pecans and pecan nutmeats. J. Food Prot. 75(11):19301938.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Beuchat, L. R., D. A. Mann, and W. Q. Alali. 2013. Efficacy of sanitizers in reducing Salmonella on pecan nutmeats during cracking and shelling. J. Food Prot. 76(5):770778.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Brar, P. K., L. G. Proano, L. M. Friedrich, L. J. Harris, and M. D. Danyluk. 2013. Survival of Salmonella, Escherichia coli O157:H7 and Listeria monocytogenes on pecans and peanuts and characterization of Salmonella isolates, (Abstract P3-80). Annual Meeting IAFP, Charlotte, NC, July 2831.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2013 Citation: Mann, D., L. Beuchat, and W. Alali. 2013. Efficacy of sanitizers in reducing Salmonella on pecan nutmeats during cracking and shelling, (Abstract P2-151). Annual Meeting IAFP, Charlotte, NC, July 2831.
  • Type: Other Status: Published Year Published: 2014 Citation: Harris, L. J., S. Yada, L. R. Beuchat, and M. D. Danyluk. 2014. Storage survival studies of foodborne pathogens on nuts, nut pastes, and seed paste products [Tables 12 and references]. In Survival of foodborne pathogens on nuts. Available at: http://ucfoodsafety.ucdavis.edu/Nuts_and_Nut_Pastes.
  • Type: Other Status: Published Year Published: 2014 Citation: Harris, L. J., L. R. Beuchat, M. D. Danyluk, and M. Palumbo. 2014. Outbreaks of foodborne illness associated with the consumption of tree nuts, peanuts, and sesame seeds [Table and references]. In Outbreaks from tree nuts, peanuts, and sesame seeds. Available at: http://ucfoodsafety.ucdavis.edu/Nuts_and_Nut_Pastes.
  • Type: Other Status: Published Year Published: 2014 Citation: Harris, L.J., Palumbo, M., L. R. Beuchat, and M. D. Danyluk. 2014. Prevalence and levels of foodborne pathogens on naturally-contaminated nuts and edible seeds [Tables 14 and references]. In Surveys for foodborne pathogens on nuts. Available at: http://ucfoodsafety.ucdavis.edu/Nuts_and_Nut_Pastes.
  • Type: Other Status: Published Year Published: 2014 Citation: Palumbo, M., L. R. Beuchat, M. D. Danyluk, and L. J. Harris. 2014. Recalls of tree nuts and peanuts in the U.S., 2001 to present [Table and references]. In U.S. recalls of nuts. Available at: http://ucfoodsafety.ucdavis.edu/Nuts_and_Nut_Pastes.
  • Type: Book Chapters Status: Published Year Published: 2013 Citation: Beuchat, L. R., and R. B. Pegg. 2013. Improving the safety and quality of pecans, p. 297329. In L. J. Harris (ed.), Improving the safety and quality of nuts. Woodhead Publishing Ltd., Cambridge, UK.
  • Type: Journal Articles Status: Under Review Year Published: 2014 Citation: Brar, P., L. Proano, L. Friedrich, L.J. Harris, and M.D. Danyluk. Survival of Salmonella, Escherichia coli O157:H7, and Listeria monocytogenes on raw peanut and pecan kernels stored at -24, 4 and 22�C. J. Food Prot.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Brar, P. K., and M. D. Danyluk. Thermal inactivation of an outbreak strain of Salmonella Tennessee and Enterococcus faecalis under stagnant dry heating conditions on peanuts. IFT 2014 Annual Meeting (New Orleans, LA, June 2124)
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Brar, P. K., and M. D. Danyluk. 2014 Determining validity of Enterococcus faecium as surrogate for Salmonella under stagnant dry heating of peanuts. (P1-171) IAFP Annual Meeting, Indianapolis, IN, August 36
  • Type: Conference Papers and Presentations Status: Published Year Published: 2012 Citation: Mann, D. A., W. Q. Alali, and L. R. Beuchat. 2012. Evaluation of sanitizers to inactivate Salmonella on in-shell pecans and pecan nutmeats. Annual Meeting, University of Georgia, Center for Food Safety, Atlanta, GA (p. 5).
  • Type: Conference Papers and Presentations Status: Published Year Published: 2012 Citation: McEgan, R., and M. D. Danyluk. 2012. Efficacy of aqueous and alcohol-based quaternary ammonium sanitizers in reducing Salmonella spp., Escherichia coli O157:H7, and Listeria monocytogenes from peanut and pecan shells, (Abstracts 035-70 [poster] and 315-04 [oral]). IFT Annual Meeting, Las Vegas, NV, June 2528.
  • Type: Book Chapters Status: Awaiting Publication Year Published: 2014 Citation: Frelka, J. C., and L. J. Harris. 2014. Nuts and nut pastes. In M. Doyle and J. Frank (ed.), The microbiological safety of low water activity foods and spices. Springer, New York. In Press.
  • Type: Other Status: Published Year Published: 2012 Citation: Beuchat, L. R. 2012. Evaluation of sanitizers for pecans. UGA Center for Food Safety, At-a-Glance 21(1):1-2.
  • Type: Websites Status: Published Year Published: 2014 Citation: We have developed extensive on-line resources for the tree nut industry including a webpage devoted to tree nut food safety (http://ucfoodsafety.ucdavis.edu/Nuts_and_Nut_Pastes/) that includes materials generated from this grant.
  • Type: Book Chapters Status: Published Year Published: 2013 Citation: Harris, L. J., J. R. Shebuski, M. D. Danyluk, M. S. Palumbo, and L. R. Beuchat. 2013. Chapter 9. Nuts, seeds, and cereals (p. 203221). In M. P. Doyle and R. L. Buchanan (ed.), Food microbiology: Fundamentals and frontiers, 4th ed., ASM Press, Washington, DC.


Progress 09/01/11 to 08/31/12

Outputs
OUTPUTS: Multiple presentations were given covering general and specific food safety concerns in the pre- and post-harvest environment of tree and ground nuts, and nut-specific HACCP training. Small to large-scale almond, pecan, walnut, pistachio, and peanut growers or processors were reached in separate meetings in California, Georgia, Nevada, and South Carolina. The number and diversity of meetings and presentations are indicative of the intense interest by the nut industry in food safety in general and for the research results generated by this grant. ALMOND: 8-2012, "Almond Food Safety Radar - Remaining Diligent on the Food Safety Front", Almond Quality and Food Safety Symposium, Visalia, CA. PECAN: Danyluk, M.D. 2-2012. "Update on pecan industry prevalence study", National Pecan Shellers Association, Charleston, SC, 9-2012; Danyluk, M.D. 2012. "Research into the prevalence of Salmonella on pecans. National Pecan Shellers Association, Las Vegas, NV. PISTACHIO: Harris, L.J. 2-2012, Research update. Pistachio Research Board, Fresno, CA. WALNUT: Harris, L.J. 8-2012. "Food safety issues for walnuts". Orchard Management Committee, California Walnut Board, Sacramento, CA. BROAD NUT INDUSTRY: Danyluk M.D. 8-12 Nut HACCP, several presentations, Athens, GA; Harris, L.J. 8-2012, Microbial food safety of tree nuts. Presentation to Roll Global, Davis, CA; Mann, D. A., W. Q. Alali, and L. R. Beuchat. 3-2012. "Evaluation of sanitizers to inactivate Salmonella on in-shell pecans and pecan nutmeats". Annu. Mtg., University of Georgia, Center for Food Safety, Atlanta, GA. INTERNATIONAL: Harris, L.J. 11-2011. "Low Moisture Foods and Ingredients: Are they a Risk for Foodborne Illness", at the Food Summit in China 2011/ 8th Annual Meeting of the Chinese Institute of Food Science and Technology PARTICIPANTS: Individuals - Technical Support: University of Georgia: David Mann, Jessica Tatum, Kia Stringer; University of California, Davis: Vanessa Morales, Christopher Theofel; University of Florida: Loretta Friedrich, Gwen Lundy, Luis Martinez; Partner Organizations, Collaborators, and Contacts: Don Schaffner, Rutgers University; Pecan Industry: Vicky Mabry and Jon Kreuger, National Pecan Shellers Association; Helen Watts, Young Pecan Inc.; Larry Wilson, Sunnyland Farms; Schermer Pecan Company. Clint Wills, South Georgia Pecan Co. Peanut Industry: Steve Calhoun, American Peanut Council; Darlene Cowart, Birdsong Peanut Company. Pistachios: Bob Klein, Administrative Committee for Pistachios; Paramount Farms; Randy Raber, Nichols Farms. Training or Professional Development: Martha Kimber, M.S. Student, UC Davis; Elisabetta Lambertini, Postdoctoral Scholar, UC Davis; Pardeepinder Brar, Ph.D. Student and Rachel McEgan, Ph.D. Student, University of Florida. TARGET AUDIENCES: The three PIs have worked closely with the target audiences for this project: the peanut, pecan, and pistachio industries (growers and processors) over the past year as evidenced by the list of presentations given to these groups. We have also shared information gained from this research with state and federal regulatory agencies. In addition to sharing research results we have also consulted with these groups in order to develop the most appropriate scientific experiments that will provide appropriate maximum information to assess and mitigate food safety risks with these foods. PROJECT MODIFICATIONS: Not relevant to this project.

Impacts
Data generated by this project are being communicated to the nut industry on an on-going basis and are being used to develop training materials for year 3. CHANGE IN KNOWLEDGE: EQUIPMENT SURFACE SANITIZERS: The efficacy of aqueous (aQUAT) and isopropyl alcohol-based (ipQUAT) quaternary ammonium sanitizers on Salmonella spp, Escherichia coli O157:H7, and Listeria monocytogenes populations on peanut and pistachio shell pieces was evaluated. Shell pieces were mixed with inoculum (5 strains Salmonella and E. coli O157:H7, 4 strains L. monocytogenes; ca. 5.5 log CFU/g) before 1ml of water, 70 percent ethanol, aQUAT, or ipQUAT was added. Mixtures were incubated at 30 degrees C for 48h and populations enumerated on selective and non-selective agar. On peanut shells, Salmonella increased 3 log CFU/g in water and aQUAT. When ethanol or ipQUAT was added, populations decreased 4 log CFU/g. E. coli O157:H7 increased 5 log CFU/g in water and aQUAT, and decreased 3 log CFU/g in ethanol and ipQUAT. L. monocytogenes increased 2 and 4 log CFU/g in water and aQUAT, and decreased by 5 and 4 log CFU/g in ethanol and ipQUAT, respectively. Likewise on pistachio shells, Salmonella increased 2 log CFU/g in water and aQUAT. When ethanol or ipQUAT was added, populations decreased by 4 log CFU/g, respectively. E. coli O157:H7 increased 2 and 3 log CFU/g in water and aQUAT, respectively and decreased 2 log CFU/g in ethanol and ipQUAT. Population levels of L. monocytogenes did not change in water, while all other treatments decreased less then 5 log CFU/g. For Salmonella and E. coli O157:H7, no significant differences were noted between water and aQUAT or ethanol and ipQUAT. No significant differences were observed among the strains of pathogens. SANITIZERS FOR NUTMEATS: Studies were done to evaluate the efficacy of chlorine (200 - 1,000 microgram/ml), lactic acid (0.5 to 2 percent), levulinic acid (0.5 to 2 percent), sodium dodecyl sulfate (SDS, 0.05 percent), lactic acid plus SDS, levulinic acid plus SDS, and a mixed peroxyacid sanitizer (Tsunami 200, 80 microgram/ml) in killing Salmonella on/in immersion- and on surface-inoculated pecan nutmeats (USDA medium pieces and Mammoth halves). Reductions did not exceed 1.1 log CFU/g of immersion-inoculated pieces and halves, regardless of sanitizer concentration or treatment time (up to 20 min). Reductions on surface-inoculated pieces and halves were 0.7 to 2.7 and 1.2 to 3.0 log CFU/g, respectively. Exposure of immersion-inoculated pecan pieces to chlorine (200 ppm), lactic acid (2 percent) and levulinic acid (2 percent) (with and without SDS), and Tsunami 200 (80 ppm) during intermittent vacuum and ambient atmospheric pressure treatments for up to 20 min reduced Salmonella by only 0.1 - 1.0 log CFU/g. These studies emphasize the importance of preventing contamination of pecan nutmeats. SUMMARY: In nut processing facilities where dust from shells exists as a possible source of cross contamination, ipQUAT should be used over aQUAT for sanitizing in the presence of dust. Once the edible nut is contaminated, the effectiveness of sanitizer treatments to eliminate Salmonella is minimal.

Publications

  • Beuchat,L. R., D. A. Mann, and W. Q. Alali. 2012. Evaluation of sanitizers for inactivating Salmonella on in-shell pecans and pecan nutmeats. J. Food Prot.75:1930-1938
  • Kimber, M. A., H. Kaur, L. Wang, M.D. Danyluk, and L.J. Harris. 2012. Survival of Salmonella, Escherichia coli O157:H7, and Listeria monocytogenes on inoculated almonds and pistachios stored at minus 19, 4,and 24 degrees C. J. Food Prot. 75:1394-1403
  • Harris, L.J. 2012. Prevention and control of Salmonella and enterohemorrhagic E. coli in tree nuts (pp 1-4). FAO, Emergency Prevention System (EMPRES) Food Safety, Lessons Learned Series No. 2. http://www.fao.org/fileadmin/templates/agns/pdf/EMPRES_FS_SeriesNo2.p df
  • Mann, D. A., and L. R. Beuchat. 2012. Evaluation of sanitizers to inactivation Salmonella on in-shell pecans and pecan nutmeats. IAFP Annual Meeting, Providence, RI (P2-108)


Progress 09/01/10 to 08/31/11

Outputs
OUTPUTS: Multiple presentations were given covering general and specific food safety concerns in the pre- and post-harvest environment of tree and ground nuts, and nut-specific HACCP training. Over 500 small to large-scale almond, pecan, walnut, pistachio, and peanut growers or processors were reached in over 10 separate meetings in California, Florida, Georgia, Louisiana, Tennessee, and Washington, D.C. The number and diversity of meetings and presentations are indicative of the intense interest by the nut industry in food safety in general and for the research results generated by this grant. A 2-day workshop was organized for and at the request of the California Food Emergency Response Team (California Department of Public Health and US Food and Drug Administration). Beuchat, L. R.: 12-01-10. Pecans as a potential source of Salmonella and other foodborne pathogens. Georgia Food Safety and Defense Task Force Meeting, Atlanta, GA. 03-09-2011. Validation of oil roasting for killing Salmonella on pecans. Georgia Agricultural Commodity Commission for Pecans, Georgia Farm Bureau, Macon, GA. 04-19-21-11. Safety concerns in the pre-and post-harvest environment of peanuts and pecans. HACCP Workshop for Nut Processors, University of Georgia, Athens, GA. 05-24-2011. Pecan safety and sanitation practices. Georgia Food Manufacture Symposium, Georgia Institute of Technology, 24 May, Atlanta, GA. Danyluk, M. D.: 2010. Looking for Salmonella in all the wrong places. Citrus Research and Education Center, Plant Production Seminar, University of Florida, Lake Alfred, FL. 2010. Research into the prevalence of Salmonella on pecans. National Pecan Shellers Association Semi-Annual meeting, Memphis, TN. 2011. Update on Pecan Industry Prevalence Study, National Pecan Shellers Association Mid-winter meeting, New Orleans, LA. 2011. Harris, L. J.: 01-13-10. A hazard assessment of California walnuts for Salmonella and other foodborne pathogens. Mid-state district meeting of the Dried Fruit and Nut Association, Stockton, CA. 01-13-11 AND 04-21-11. Risk assessment for pistachios. Technical Committee of the Administrative Committee for Pistachios. Fresno, CA. 04-04-11 Perspectives on Sampling California Treenuts. Workshop on approaches to setting intervention targets with limited data for low-moisture food commodities. Washington, D.C. 06-28-11. Assessing postharvest risks for Salmonella in pistachios. Center for Produce Safety Research Meeting, Orlando, FL. 07-13-11. "10 years, what have we learned" Almond Board of California Food Safety Meeting, Lodi, CA. Harris L.J. and Danyluk, M.D. November 2-3, 2010. Training in Nut Safety for the California Food Emergency Response Team. Sacramento, CA. PARTICIPANTS: Individuals - Technical Support: University of Georgia: David Mann, Jessica Tatum, Kia Stringer; University of California, Davis: Vanessa Morales, Christopher Theofel, Harbir Kaur; University of Florida: Loretta Friedrich, Gwen Lundy, Luis Martinez, Pardeepinder Brar, Katie Jones, Brian Buzzie, Liseth Proano; Partner Organizations, Collaborators, and Contacts: Don Schaffner, Rutgers University; Pecan Industry: Vicky Mabry and Jon Kreuger, National Pecan Shellers Association; Helen Watts, Young Pecan Inc.; Larry Wilson, Sunnyland Farms; Schermer Pecan Company. Clint Wills, South Georgia Pecan Co. Peanut Industry: Steve Calhoun, American Peanut Council; Darlene Cowart, Birdsong Peanut Company. Pistachios: Bob Klein, Administrative Committee for Pistachios; Paramount Farms; Randy Raber, Nichols Farms; Andrew Howe, Horizon Growers. Training or Professional Development: Martha Kimber, M.S. Student, UC Davis; Elisabetta Lambertini, Postdoctoral Scholar, UC Davis; Lisseth Proano, Visiting Scholar, University of Florida TARGET AUDIENCES: The three PIs have worked closely with the target audiences for this project: the peanut, pecan, and pistachio industries (growers and processors) over the past year as evidenced by the list of presentations given to these groups. We have also shared information gained from this research with state and federal regulatory agencies. In addition to sharing research results we have also consulted with these groups in order to develop the most appropriate scientific experiments that will provide appropriate maximum information to assess and mitigate food safety risks with these foods. PROJECT MODIFICATIONS: Not relevant to this project.

Impacts
Data on this project are being communicated to the nut industry on an on-going basis and are being used to develop training materials for year 3. The effect of pathogen concentration and storage temperature on the survival of Salmonella, Listeria monocytogenes (LM) and Escherichia coli O157:H7 (ECO157) on shelled peanuts, pecans and in-shell pistachios was determined. Nuts were separately inoculated with cocktails of Salmonella, LM and ECO157 and stored at -20, 4 and 23C. Populations of all three bacteria decreased 1 to 2 logs during the initial 72 h drying after inoculation. With the exception of ECO157 in refrigerated almonds (-0.09 log CFU/month), time did not impact populations at -20 and 4C; Linear rates of decline at 23C ranged from 0.15 to 0.32 for Salmonella, 0.35 to 0.45 for ECO157, and 0.55 to 0.86 for LM. Current studies are evaluating the differential survival of the five serovars of Salmonella inoculated onto the nuts after 365 days. Effectiveness of conditioning treatments was evaluated for killing Salmonella in and on immersion-and surface- inoculated inshell pecans. Treatment of immersion-inoculated pecans in 400 ppm chlorine reduced Salmonella by not more than 1.6 log. Treatment of pecans for 1 min in 200 ppm chlorinated water, soaking in water for 2h at 21C and heating for 10 min at 85-95C reduced Salmonella by more than 5.1 log; less than 0.6 log CFU/g of Salmonella was eliminated when nuts were treated for 15 min at 90C. Approximately 6.4 log reductions were achieved in water at 90 or 95C for 80 s; treatment of nuts containing 1.8 log CFU/g at 95C for 10 min did not eliminate the pathogen. Salmonella was more resistant to conditioning treatments when inshell pecans were immersion-rather than surface-inoculated or when inoculated inshell pecans were stored. Results emphasize the importance of following common commercial practices when validating the lethality of conditioning treatments. The effectiveness of hot air drying and dry roasting was evaluated for pecans. Hot air treatment of 2.8 to 4.1 percent and 10 to 11 percent moisture immersion-inoculated pecan nutmeats at 120C for 20 min reduced the number of Salmonella by 1.2 to 1.3 and 1/9 to 2.0 log CFU/g, respectively. Regardless of moisture content, hot air treatment at 120C for 20 min failed to eliminate 0.77 log CFU/g Salmonella inoculated onto pecan halves. More than 7 log reductions were observed when dry pieces were dry roasted at 160C for 15 min. Treatment of halves at 140,150 or 170C for 20, 15 or 10 min, respectively reduced Salmonella by 5 log CFU/g. The pathogen was slightly more heat resistant in immersion-inoculated nutmeats than on surface-inoculated nutmeats. Exposure of immersion-inoculated pieces to peanut oil at 127 or 132C for 1.5 or 1 min, respectively or halves at 138C for 2 min reduced Salmonella by 5 log CFI/g; treatment of halves at 132C for 2.5 to 4 min did not always achieve this reduction. Hot air treatment cannot be relied upon to reduce Salmonella by 5 log CFU/g on raw pecan nutmeats without changing sensory qualities. Treatment temperatures and times typically used to oil nutmeats appear to be sufficient to reduce Salmonella by 5 log CFU/g.

Publications

  • Beuchat, L. R. 2010. Behavior of Salmonella on high-moisture pecans. Pecan South. 43(9):38-40.
  • Beuchat, L. R, and D. A. Mann. 2010. Survival and growth of Salmonella in high-water activity pecan nutmeats, inshell pecans, inedible nut components, and orchard soil. J. Food Prot. 73:1975-1985.
  • Beuchat, L. R., and D. A. Mann. 2011. Inactivation of Salmonella on in-shell pecans during conditioning preceding cracking and shelling. J. Food Prot. 74:588-602.
  • Beuchat, L. R., and D. A. Mann. 2011. Inactivation of Salmonella on pecan nutmeats by hot air treatment and oil roasting. J. Food Prot. 74:1441-1450.
  • Beuchat, L. R. 2011. Reduction of Salmonella on pecans by hot treatment. UGA Center for Food Safety, At-a-Glance. 20(1):2.
  • Beuchat, L. R. 2011. Conditioning treatment reduce Salmonella. The Pecan Grower Magazine. 23(4):24-26.
  • Beuchat, L. R. 2011. Inactivation of Salmonella by hot air and oil roasting. Pecan South. 44(7):26-28.
  • Proano Peralta, L.G., L.M. Friedrich, L.J. Harris, and M.D. Danyluk. 2011. Survival of Salmonella spp., Listeria monocytogenes and Escherichia coli on inoculated peanut and pecan kernels stored at -20, 4 and 23C. IAFP Annual Meeting, Milwaukee, WI. (P3-113).
  • Kaur, H, M. Kimber, M.D. Danyluk, and L.J. Harris. 2011. Long-term survival of Salmonella pp., Escherichia coli O157:H7, and Listeria monocytogenes on inoculated almonds and in-shell pistachios at three storage temperatures. IAFP Annual Meeting, Milwaukee, WI. (P3-114).
  • Morales, V.M., H. Kaur, I.Y. Zhao, and L.J. Harris. 2011. Behavior of inoculated Salmonella spp. in postharvest pistachio handling. IAFP Annual Meeting, Milwaukee, WI. (P3-115).
  • Kimber, M.A., and L.J. Harris. 2011. Changes in total aerobic and coliform counts on pistachios during postharvest processing. IFT Annual Meeting, New Orleans, LA (199-06).
  • Lambertini, E., M.D. Danyluk, D.W. Schaffner, C.K. Winter, and L.J. Harris. 2011. Risk of salmonellosis from consumption of almonds in the North American market. ASM Annual Meeting, New Orleans, LA (4512).
  • Beuchat, L. R., and D. A. Mann. 2011. Behavior of Salmonella on high-moisture pecan shucks, shells, and middle septum tissue, and in pecan orchard soil. Abstr., Proc. Southeast Regional Fruit and Vegetable Conf. and Georgia Pecan Growers Assoc. Savannah, GA. p. 2.
  • Mann, D. A., and L. R. Beuchat. 2011. Inactivation of Salmonella on pecan nutmeats by hot air and oil roast treatments. Annu. Mtg., Int. Assoc. Food Protection, 32 July - August 3, Milwaukee, WI. J. Food Prot. Suppl. A. 74:200. (2,500)
  • Mann, D. A., and L. R. Beuchat. 2011. Lethality of hot air and oil roasting treatment to Salmonella on pecan nutmeats. Annu. Mtg., University of Georgia, Center for Food Safety, Atlanta, GA. p. 7.


Progress 09/01/09 to 08/31/10

Outputs
OUTPUTS: Multiple presentations were given covering general and specific food safety concerns in the pre- and post-harvest environment of tree and ground nuts, and nut-specific HACCP training. Small to large-scale pecan, walnut, pistachio, hazelnut, and peanut growers or processors were reached in over 16 separate meetings in California, Georgia, Louisiana, North Carolina, Oregon, and Tennessee. The number and diversity of meetings and presentations are indicative of the intense interest by the nut industry in food safety in general and for the research results generated by this grant. Beuchat, L.R. "Safety concerns in the pre- and post-harvest environment of peanuts and pecans", Danyluk, M.D. "Safety considerations in pre- and post-harvest environment of almonds", "Applying the 7 HACCP principles", and HACCP Principles 3, 4 & 5." HACCP for Nut and Nut Product Manufacturers, Nov. 17-19, 2009, Athens, GA.; Beuchat, L.R. "Pecan safety research - University of Georgia. "Georgia Pecan Growers Association Meeting, Jan. 8-10, 2010, Savannah, GA.; Beuchat, L.R. "Update on pecan safety research at the University of Georgia. "National Pecan Shellers Association. Feb. 18-20, 2010, New Orleans, LA; Harris, L.J. "Pathogens of Concern - Dried Nuts (and Fruits)." Dried Fruit and Nut Association Annual Meeting, Feb. 19, 2010, Monterey, CA.; Beuchat, L.R. "Contamination, survival, and elimination of Salmonella on pecans in pre-harvest and post-harvest environments." Annual Convention, Southeastern Pecan Growers Association, Feb. 26-28, 2010, Sandestin, FL.; Beuchat, L.R. "Observations on the behavior of Salmonella on pecans." Annual Meeting, Center for Food Safety, University of Georgia, March 2-3, 2010, Atlanta, GA." Beuchat, L.R. "Evaluation of pecan shelling and storage practices for effectiveness in reducing the risk of contamination with Salmonella." Georgia Agricultural Commodity Commission for Pecans, April 6, 2010, Macon, GA; Harris, L.J. "Microbial food safety issues associated with plant farm products", "An Overview of the Grocery Manufacturers' Association Nut Processors' Handbook", "Sanitation for Nut Processing - Lessons Learned for Almonds", and "Process Validation and Critical Control Points." Hazelnut Industry Food Safety Seminar, May 24-25 2010, Aurora, OR; Harris, L.J. "Salmonella in low-moisture foods (tree nuts)" Dried Fruit & Nut Association of California, June 8, 2010, Sacramento, CA; Beuchat, L.R. Safety concerns in the pre- and post-harvest environment of peanuts and pecans. HACCP Workshop for Nut Processors, Danyluk, M.D. "Safety considerations in pre- and post-harvest environment of almonds", "Applying the seven HACCP principles", and HACCP Principles 3, 4 & 5." July 13-15, 2010, Athens, GA.; Beuchat, L.R. Recent observations enabling better management of safety risks associated with produce and pecans. North Carolina Fresh Produce Symposium, Sept. 9, 2010, Raleigh, NC; Beuchat, L.R. Update on pecan safety research. Annual Meeting National Pecan Shellers Association, Sept. 16-18, 2010, Memphis, TN.; Beuchat, L.R. Heat inactivation of Salmonella on pecan. Center for Food Safety, University of Georgia, Sept. 21, 2010, Atlanta, GA. PARTICIPANTS: Individuals - Technical Support: University of Georgia: David Mann; University of California, Davis: Vanessa Morales, Christopher Theofel, Harbir Kaur; University of Florida: Loretta Friedrich, Gwen Lundy, Luis Martinez; Partner Organizations, Collaborators, and Contacts: Don Schaffner, Rutgers University; Pecan Industry: Vicky Mabry and Jon Kreuger, National Pecan Shellers Association; Helen Watts, Young Pecan Inc.; Larry Wilson, Sunnyland Farms; Schermer Pecan Company. Peanut Industry: Steve Calhoun, American Peanut Council; Darlene Cowart, Birdsong Peanut Company. Pistachios: Bob Klein, Administrative Committee for Pistachios; Paramount Farms; Nichols Farms; Horizon Growers. Training or Professional Development: Martha Kimber, M.S. Student, UC Davis; Elisabetta Lambertini, Postdoctoral Scholar, UC Davis; Lisseth Proano, Visiting Scholar, University of Florida. TARGET AUDIENCES: The three PIs have worked closely with the target audiences for this project: the peanut, pecan, and pistachio industries (growers and processors) over the past year as evidenced by the list of presentations given to these groups. In addition to sharing research results we have also consulted with these groups in order to develop the most appropriate scientific experiments that will provide appropriate maximum information to assess and mitigate food safety risks with these foods. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.

Impacts
Research is in progress. While these data are being communicated to the nut industry on an on-going basis they are also being used to develop training materials for year 3 of this project. A brief summary of findings to date: Studies (12-18 months)to determine the survival of a mixture of Salmonella serovars on pecans (both in-shell and kernel), peanuts, and pistachios at storage temperatures of -20, 4, and 24C (and for pecans at 35 C) will be complete in mid 2011. However, preliminary data show that populations of Salmonella are stable at -20 and 4 C across the nut types over 6+ months. Reductions at 24 C are slow but significant; preliminary data suggest that rates of reduction on pistachios are very similar to those previously determined for almonds. Studies were also initiated to compare survival of Salmonella on pistachios and almonds stored at low and high relative humidity - no significant difference in survival was observed. Dusts from peanut and pistachio processing facilities were collected, characterized and are being inoculated with Salmonella to determine growth and survival of this organism and ability to cross-contaminate via dust. Thermal resistance of Salmonella on almonds and pistachios were compared in model oil and dry roasts. Increased moisture significantly increases the heat sensitivity of Salmonella in oil roasting but the impact is diminished in a dry roast. A study was done to determine the infiltration and survival characteristics of Salmonella in pecans. The rate of infiltration of water into in-shell nuts varied among six varieties evaluated and was significantly affected by the extent of shell damage. The rate of infiltration into nuts at -20 or 4 C was lower than at 21 or 37 C when nuts were immersed in water at 21 C. Salmonella that infiltrated in-shell nuts reached the kernel and remained viable after drying and during subsequent storage at 4 C. Results emphasize the importance of applying process treatments that will inactivate Salmonella. The survival and growth of Salmonella on high-moisture (water activity of 0.96 to 0.99) pecan nutmeats, in-shell pecans, and inedible components (shuck, shell, and middle septum tissue) of in-shell pecans was determined. Salmonella did not grow on high-moisture nutmeat halves, pieces, or granules stored at 4 C for up to 48 h. Growth did occur at 21, 30, and 37 C. Small decreases in populations of Salmonella on and in high-moisture in-shell pecans (kernel water activity of 0.94)stored at 4, 21, 30, and 37 C over 8 days. The pathogen grew on the surface of high-moisture (water activity of 0.99) pecan shucks and shells but died on middle septum tissue stored at 21, 30, and 37 C for up to 6 days. Salmonella died in water extracts of shucks and in pecan orchard soil saturated with water or shuck extract, but survived well for at least 18 weeks in dry soil. The ability of the pathogen to grow on high-moisture nutmeats and some of the inedible components of pecans emphasizes the importance of controlling or limiting the time pecans are exposed to water in preharvest and post harvest environments.

Publications

  • Beuchat, L. R. 2010. Research funding for pecan safety. The Pecan Grower Magazine. 21(3):16-17.
  • Beuchat, L. R., and D. A. Mann. 2010. Factors affecting infiltration and survival of Salmonella on inshell pecans and pecan nutmeats. J. Food Prot. 73:1257-1268.
  • Beuchat, L. R. 2010. Research Update: Observations on the behavior of Salmonella on pecans. Rept. to National Pecan Association, Southwestern Pecan Growers; Council, and Georgia Pecan Growers Association, 12 February, 9 pp.
  • Beuchat, L. R. 2010. Contamination, survival, and elimination of Salmonella on pre-harvest and post-harvest pecans. Proc. Southeastern Pecan Growers Association, 103rd Annu. Conv., Meeting, 27-28 February, Sandestin, FL. p. 88-92.
  • Beuchat, L. R. 2010. Behavior of Salmonella in high-aw pecans. UGA Center for Food Safety. At-a-Glance. 19(1):1-2.
  • Beuchat, L. R. 2010. Infiltration of Salmonella in pecans. The Pecan Grower Magazine. 22(1):18-22.
  • Beuchat, L. R. 2010. Research Update: Observations on the behavior of Salmonella on pecans. Rept. to National Pecan Shellers Association, Southwestern Pecan Growers' Association, and Georgia Pecan Growers Association, 7 September, 11 pp.
  • Mann, D. A., and L. R. Beuchat. 2010. Infiltration, survival, and growth of Salmonella on pecans as affected by environmental conditions. Abstr., Proc. Southeast Regional Fruit and Vegetable Conf., 8-10 January, Savannah, GA. p. 44. (2,180).
  • Mann. D. A., and L. R. Beuchat. 2010. Behavior of Salmonella in high-moisture pecan nutmeats inshell pecans, inedible nut components, and orchard soil. Annu. Mtg., University of Georgia Center for Food Safety, 2-3 March, Atlanta, GA. p. 4-6. (140).
  • Mann, D. A., and L. R. Beuchat. 2010. Behavior of Salmonella in high water activity pecan nutmeats, inedible nut components, and orchard soil. Annu. Mtg., Int. Assoc. Food Protection, 1-4 August, Anaheim, CA. p. 170. (2,200).
  • Beuchat, L. R., and D. A. Mann. 2010. Fate of Salmonella on in-shell pecans during cleaning and conditioning treatments before shelling. 22nd Int. ICFMH Symposium, FoodMicro 2010, 30 August - 3 September, Copenhagen, Denmark. p. 269. (700).
  • Beuchat, L. R. 2010. Factors affecting survival, growth, and inactivation of Salmonella on pecans, with comparisons to other tree nuts and peanuts. IFT 10 Annu. Mtg and Food Expo, 18-20 July, Chicago, IL. /presentation 103-01. Available online: http://www.abstractsonline.com/plan/ViewAbstract.aspxmID=02...(110) http://www.abstractsonline.com/plan/ViewAbstract.aspxmID=2525 (110).