AFAB-Vol.2-Issue-1 by cielo shabatura

Volume 2, Issue 1 June 2012

EDITORIAL BOARD Sooyoun Ahn

W.K. Kim

Arkansas State University, USA

University of Manitoba, Canada

Walid Q. Alali

M.B. Kirkham

University of Georgia, USA

Kansas State University, USA

Kenneth M. Bischoff

Todd Kostman

NCAUR, USDA-ARS, USA

University of Wisconsin, Oshkosh, USA

Claudia S. Dunkley

Y.M. Kwon

University of Georgia, USA

University of Arkansas, USA

Lawrence Goodridge

Maria Luz Sanz

Colorado State University, USA

MuriasInstituto de Quimica Organic General, Spain

Leluo Guan

Melanie R. Mormile

University of Alberta, Canada

Missouri University of Science and Tech., USA

Joshua Gurtler

Rama Nannapaneni

ERRC, USDA-ARS, USA

Mississippi State University, USA

Yong D. Hang

Jack A. Neal, Jr.

Cornell University, USA

University of Houston, USA

Divya Jaroni

Benedict Okeke

Southern University, USA

Auburn University at Montgomery, USA

Weihong Jiang Shanghai

John Patterson

Institute for Biol. Sciences, P.R. China

Purdue University, USA

Michael Johnson

Toni Poole

University of Arkansas, USA

FFSRU, USDA-ARS, USA

Timothy Kelly

Marcos Rostagno

East Carolina University, USA

LBRU, USDA-ARS, USA

William R. Kenealy

Roni Shapira

Mascoma Corporation, USA

Hebrew University of Jerusalem, Israel

Hae-Yeong Kim

Kalidas Shetty

Kyung Hee University, South Korea

University of Massachusetts, USA

EDITORIAL STAFF EDITOR-IN-CHIEF Steven C. Ricke University of Arkansas, USA

EDITORS Todd R. Callaway FFSRU, USADA-ARS, USA Cesar Compadre University of Arkansas for Medical Sciences, USA Philip G. Crandall University of Arkansas, USA

MANAGING EDITORS

Ellen J. Van Loo Ghent, Belgium Dave Edmark Fayetteville, Arkansas, USA

LAYOUT EDITOR

Melody Rust Eureka Springs Arkansas, USA

TECHNICAL EDITOR

Jessica C. Shabatura Fayetteville Arkansas, USA

ONLINE EDITION EDITOR C.S. Shabatura Fayetteville Arkansas, USA

ABOUT THIS PUBLICATION Mailing Address: 637 S. Ray Ave. . Fayetteville, AR . 72701

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Agriculture, Food & Analytical Bacteriology (ISSN 2159-8967 is published quarterly, beginning with this inaugural issue.

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TABLE OF CONTENTS CONFERENCE PROCEEDINGS* 4 The Story of the Arkansas Association for Food Protection (AAFP) M. Sostrin

6 A Team Approach for Management of the Elements of a Listeria Intervention and Control Program

J. N. Butts

15 Development of a Food Defense Workshop and Graduate Certificate in Food Safety and Defense for Working Professionals K. J. K. Getty

35 Development and Assessment of Success for Retail Food Safety Programming in Indiana R. H. Linton

43 ConAgra Foods’ Salmonella Chester Outbreak In Marie Callender’s Cheesy Chicken and Rice Catalyzing Change: Next Generation of Food Safety J. Menke-Schaenzer

46 Food Safety For a Diverse Workforce; One Size Does Not Fit All J. A. Neal, M. Dawson, J. M. Madera

REVIEWS* 25 Human Noroviruses and Food Safety K. E. Gibson and S. C. Ricke

56 Isolation and Initial Characterization of Plasmids in an Acetogenic Ruminal Isolate O. K. Koo, S. A. Sirsat, P. G. Crandall and S. C. Ricke

EXTRAS 69

Instructions for Authors

* Arkansas Association for Food Protection (AAFP) Conference, Enhancing Food protection From Farm to Fork, held on Sept. 28-29, 2011, Springdale, AR.

CONFERENCE PROCEEDINGS* The Story of the Arkansas Association for Food Protection (AAFP) M. Sostrin Senior Manager, Food Safety Recalls Walmart Stores, Inc. * Arkansas Association for Food Protection (AAFP) Conference, Enhancing Food protection From Farm to Fork, held on Sept. 28-29, 2011, Springdale, AR.

The story of the Arkansas Association for Food Protection (aafp) ABSTRACT The Arkansas Association for Food Protection (AAFP) is a diverse group of Academia, Industry, Regulatory and Retail professionals, committed to providing a forum to encourage improvement of all areas of food safety and quality. AAFP is a unique organization in that it provides a forum where professionals join together in providing educational seminars and meetings that bring current trends, emerging issues and concerns into focus for the better understanding of all. The associations goal is to provide its members with practical information that they can take back to their workplace and apply to improve the safety and quality of food for not only Arkansans but also the World. Keywords: Arkansas Association for Food Protection, AAFP, Arkansas, International Associate for Food protection, IAFP, food safety, emerging issues, quality, educational seminars, collaboration Agric. Food Anal. Bacteriol. 2: 4-5, 2012

The story of the Arkansas Association for Food Protection (AAFP) is one of a shared vision to open communication and to increase collaboration in the area of Food Safety and quality by Retail, Industry, Academia and Regulatory. The AAFP was formed in early 2009 by Michael Sostrin of Walmart Stores Inc.; Scott Stilwell, Hillary Hagan, and Jerri Lynn Pickett of Tyson foods; and Michael Johnson and Steve Ricke of the University of Arkansas. All shared a common vision, to create a unique organization that was committed to provide an open forum to encourage improvement of all areas of food safety and quality through collaboration and sharing of ideas. TogethMichael Sostrin Senior Manager, Food Safety Recalls Walmart Stores, Inc. michael.sostrin@wal-mart.com

er, they created a mission for the Arkansas Affiliate of the International Association for Food Protection, “to promote the objectives of IAFP - and further, to provide a local forum to encourage improvement of all areas of food safety and quality; and to increase the knowledge and professional status of our membership in the areas of food safety and quality.” The AAFP was chartered in April of 2009 as an affiliate of the International Association for Food Protection (IAFP). During the 2009 IAFP annual meeting in Grapevine, TX the AAFP was presented with their charter and planning began for the Association first annual meeting in the October of 2009. Both of the Associations first two Annual Educational Conferences in October 2009 and September 2010 have by

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hosted at Tyson Foods Headquarters in Springdale, AR. Each of these was very well attended attracting nearly 100 attendees each time. The theme of the meeting in 2009 was “Retail Food Safety – A Catalyst for Change” and in 2010 “Enhancing Food Protection From Farm to Fork.” At each of these meeting participants from academia, industry, retail and government shared openly ideas and thoughts and had great debate on many emerging food safety and quality issues It is plain to see that the AAFP is an organization that provides a forum where academia, industry, regulatory and retail professionals join together in providing educational seminars and meetings that bring current trends, issues and concerns into focus for the better understanding of all. Through its annual educational conference and symposium the AAFP attracts members of academia, industry, regulatory and retail to come together in an open forum to discuss and debate the emerging issues in Food Safety and Quality. The meetings sessions are dedicated to the timely coverage of key issues or hot topics that cater to a broad mix of attendees. At the educational conference food safety and quality professionals gain access to a network of professional contacts and organizations that can help them both personally and professionally. AAFP through its educational conference provides its members with access to innovative scientific and technical information, as well as a connection to the food safety industry and some its top experts. AAFP’s goal is to provide its members with practical information that they can take back to their workplace and apply. I am proud to have been a part of the founding of AAFP and to able to bring to Arkansas an organization whose purpose is to improve the safety and quality of food for not only Arkansans but also the World. I look forward to a bright future for the Association as it continues to drive its mission forward, to provide a local forum to encourage improvement of all areas of food safety and quality for all.

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CONFERENCE PROCEEDINGS* A Team Approach for Management of the Elements of a Listeria Intervention and Control Program J. N. Butts1 Land O’Frost, Lansing, IL 60438 *Arkansas Association for Food Protection (AAFP) Conference, Enhancing Food Protection from Farm to Fork, held on Sept. 28-29, 2010, Springdale, AR. 1

ABSTRACT Listeria control in federally inspected processed meat plants has improved over the last 25 years. A model method is presented. This method couples local plant teams with investigative tools and a list of critical factors for process control. Diligence in the application of these tools and implementation of “Best Practices” enables the plant food safety culture to move from the Awareness phase to the Enlightenment phase; next to the Preventative phase and ultimately to the Predictive phase. Once the plant is in the Preventative and Predictive phases efforts spent firefighting problems are dramatically reduced and a state of control evolves. Keywords: S&D, Seek and Destroy, Timed Study, Swat Team, Firefighting, Critical Factors, Listeria, Environmental, Awareness, Enlightenment, Preventative, Predictive, Team, Teamwork, Intervention, Control, AMI, Post Rinse, Investigation, Growth Niche Agric. Food Anal. Bacteriol. 2: 6-14, 2012

Introduction The control of Listeria in the U.S. federally inspected meat plants has dramatically improved in the last twenty years (Figure 1). This effect is being measured and monitored by FSIS sampling of finished product from establishments hat produce post-lethality exposed.

This success has several interrelated factors: 1. Root causes (growth niches) can be identified and either eliminated or managed. 2. Transfer vectors within RTE area can be managed in such a manner to minimize the transfer of the Listeria. 3. Hurdles to entry into RTE area can minimize cross contamination.

Correspondence: J. N. Butts, john.butts@landofrost.com

Please note that managing these factors will not totally control or prevent product contamination (HACCP CCP). These factors do, however, minimize the poten-

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FSIS Regulatory Testing for LM in RTE Products by Calendar Year 1990 - 2009* (All Years All Projects) 5.00 4.61

4.50 4.00

4.03

Percent Positive

3.61

3.50 3.00 2.50

3.44

2.90

3.02

2.91 2.54 2.25 1.91

2.00

1.45

1.50

1.32 1.03

1.00

0.91 0.76

0.68 0.48 0.43

0.50

0.42

0.37

0.00 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009

Calendar Year* *Starting with CY2008, annual microbiological results are reported by sample collection date as opposed to analysis end date.

Figure 1. FSIS Regulatory testing for Listeria monocytogenes in RTE products by Calendar year 1990-2009 (FSIS, 2099). tial for contamination. The key to control is the management of total system which I will call “process management.” Process management is based on managing many interrelated factors. These include: 1. The development of Best Practices associated with AMI Principles of Sanitary Facility and Equipment Design. 2. These principles and audit items, when combined with the Global Food Safety Initiative (GFSI) audit questions, provide establishments and local management the basis for a continuous improvement system. The U.S. meat industry has agreed that food safety is not a competitive arena and they have fullyshared their Best Practices. 3. This “teamwork” is best demonstrated by the AMI Listeria Intervention and Control Work-

shops. The presenters at each workshop consist of a diverse group experienced in food safety. The focus and basis of the workshops is control and intervention. The scientific basis of control is presented and discussed. Case studies and group problem-solving supplement the learning experience. Real life situations are presented in an environment that enables the participants to share and apply “Best Practices” to control high risk situations. 4. The implementation of “Best Practices” has resulted in plant monitoring data showing the effect of process improvement. The continuous improvement cycle has been fueled by success after success. The net effect was a documented reduction in samples found to be positive for Listeria. 5. Microbiological process control over the past 25 years has seen our company and other

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Table 1. Four stages of environmental control within plants. Stage

Sampling Results

Control Methods

Verification

Awareness

Contact Surface and Product positives

Sample product. Recognition of environmental nature of Listeria.

Product

Enlightenment

Expanded and regular sampling of contact surfaces and environmental sites. Intermittent positives on contact surfaces. Routine positives on environmental sites

Recognize existence of growth niches. Sample contact surfaces and some floor and environmental areas. Starting the redesign phase.

Product & Contact Surfaces

Preventative

Early preventative phase positive results dominated by indicator sites such as post rinse. In final phase of preventative, only rare Contact Surface positives. No Product Positives. Investigative facility based positives dominate RTE.

Potential Growth niches mapped. Some scheduled intervention practices in place. Managing “Critical Factors” of the Sanitation process. Engaged in Equipment and Facility redesign.

Product, Contact Surfaces & Primary Transfer Vectors in RTE Area

Predictive

No Contact surface positives. Zone 4 positives predominate. Hurdle transfer point sampling produces rare positives.

Aggressive early warning sampling in place. Intervention practices in place with all RTE equipment. Focus on zone 4 and facilities. Advanced phases of both Equipment and Facility redesign.

Product, Contact Surfaces & Transfer Points (Zones 1, 2 & 3) in RTE Area

companies go through a series of transition phases as the success in Listeria control evolved. These transition phases can be divided into four stages (Table 1).

The Evolution of Environmental Control Individual stages are characterized by how a plant views and controls Listeria, sampling methods and results along with their perspective on the difference between samples taken for control purposes versus verification of control. Specifically, these stages are defined by action taken in response to Listeria species positives and high APC counts from investigation and monitoring programs. Table 1 relates sampling methods and results to actions taken. It defines perception of verification vs. control. Verification vs. control is easy when a

CCP exists. When no CCP exists, the most significant factors affecting control must be identified. These “critical factors” then become the focus and basis of control. Microbiological monitoring of these processes then becomes the basis of “microbiological process control measurements.” The measurement system continues co-evolve. Verification sites grow in numbers and size as the process control sites evolve. The process control sites become “indicators of control” and are verified by verification sites. Verification sites continue to move further and further away from the product and represent a decrease in risk level. The overall effect on the system is that verification becomes more precise and control measures more accurate. The transition points in the evolution require management to change their course of action and perspective. Management practices play a key role in the evolution of control. Bob Reinhard of Sara Lee

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has characterized the management commitment in the following manner (Figure 2):

Commitment Model Employee & Management •

Resistant – don’t believe it has value

•

Accepting – why not

• “Buy-in” – we will do it •

Engagement – involved in solution

•

Commitment – hold self and others accountable for achieving results Bob Reinhard – Sara Lee

(Figure 3). The development and deployment of preventive practices eliminates “firefighting”. The success of these practices leads to further implementation of preventative practices. Success under supportive management conditions, continuous improvement and preventive practices empowers the management team and workforce. A “dose of science” in the sampling methodology enables predictive practices for intervention deployment. A preventative practice can become a predictive practice when deployed based on a defined need. Indicator sites are established to signal this deployment. Indicator sites need to be located at points in

Figure 2. Management commitment model When this commitment model is overlaid on a continuous improvement model, we see plants moving away from a firefighting mode where the same problem is solved over and over again during the buy-in and engagement stages. Listeria control requires the identification of root causes (growth niches). They must be either eliminated or managed. Success requires commitment on the part of all employees. Not all growth niches can be eliminated and transfer vectors are going to exist whenever a food product is exposed to the environment. Man-

Figure 3. Commitment model combined with continuous improvement agement engagement and employee commitment is necessary for effective control. Next, the “Evolution of Control” is overlaid on the Commitment and Continuous Improvement Model

Figure 4. Model for Listeria control the system to provide an early warning of the presence of the organisms. These points include samples from a known or potential harborage site, hurdle to entry, or a transfer point that indicates the organism was located in an area that suggests harborage or could have been impregnated in the piece of equipment in the exposed product area below the normal level of disassembly. A positive indicator site (Ls+) could prompt the pasteurization of a conveyor belt for example. Regular sampling of indicator sites then become the predictive trigger for the application of an intervention to individual components, pieces of equipment, line components or an entire line. The effectiveness of a system of environmental validation sites and indicator sites can be monitored by a post rinse sampling program. Post Rinse samples are samples taken after disassembly and the initial rinse. The Post Rinse sites are located on large areas

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of equipment that collect spatter from the initial rinsing process. Typical sites are the sides of machines, framework, underneath assemblies and exposed components that may receive spatter from other machine parts and the floor. Post rinse sites can be composited therefore providing a large coverage area for one analysis. A post rinse positive does not mean there was contamination, but only indicates the presence of the organism in the area sampled. Action to take is to follow with multiple days of daily sampling (i.e. 10). If a positive is found in the follow up sampling then an investigation is warranted. A positive from post rinse can be from the following sources: 1. The organism may have entered the area from outside the exposed product RTE area and would be eliminated during the normal cleaning and sanitization procedures 2. A growth niche within a piece of equipment or within the facility may have shed the organism into the environment or 3. A transient site such as product tote, rework pan, electric pallet jack or trash container may have been responsible. After a second positive Post Rinse sample, an investigation is needed to locate the source of the organism be it a growth niche or transfer vector bringing the organism into the RTE area. Indicator sites are not validation sites, but sites measuring the control at a specific point in the process. Teamwork is the deployment vehicle for the transformation of the cultural change. Management must make verification sites the key process indicators (KPI’s) and reward employee success in finding out of tolerance or out of control indicator sites rather than taking punitive action This understanding enables the teams to focus on prevention and develop early detection methods. Teamwork has been a successful management tool to develop and sustain the gains in environmental pathogen control. Control systems can be broad, but must be focused on specific root causes. Investigational data identifies these critical factors over time. We have deployed two teams: one focused on equipment design and maintenance, as well as sanitation process control; the other is focused on the facility. These multi-disciplinary teams are held accountable

by management for attaining and maintaining control of environmental pathogens. They are empowered to take the appropriate action necessary for that task.

PROCESS CONTROL TOOL BOX Proven control methods and investigative techniques are used to investigate for the existence and location of growth niches. The Seek and De-

Seek & Destroy Team Charter Purpose: The purpose of the Seek and Destroy Team is to maintain and continuously improve the equipment design, Sanitation Process Control procedures, Operational GMP’s as well as providing corrective and preventative action for any microbiological monitoring issues. Methods: 1. Utilize the S&D audits to investigate, evaluate and qualify equipment and processes. 2. Assign projects to highest risk ranked projects 3. Utilize the Preventative Maintenance Computer program to schedule and help manage preventative sanitary practices Results Expected: 1. Monitor sanitation effectiveness 2. Conduct regular audits of lines in the RTE area. – Execute corrective action on those audit items that can be easily fixed – Assign projects to items needing more detailed correction action 3. Monitor all microbiological results and perform corrective and preventative action as necessary to maintain microbiological process control 4. Evaluate and qualify all new equipment to be used in the RTE area 5. Reach consensus on microbiological process control procedures 6. Develop or approve training materials, methods for GMP and Sanitation Process Control 7. Continuously monitor the effectiveness of GMP Training 8. Recommend or direct employee training as needed

Figure 5. Sanitation and Destroy Team Charter

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Facility Design Team Charter Purpose: The purpose of the team is to maintain and continuously improve the facility by evaluating the facility sanitary design and determining the areas where improvements/repairs are needed. Methods: 1. Utilize the AMI Sanitary Facility Design Checklist and SQF (GFSI) facility related audit requirements. 2. Assign risk values to plant areas & checklist items 3. Use Risk assessment to assist in prioritizing major projects Results Expected: 1. Determine room groupings as described in the AMI Sanitary Facility Design Checklist. 2. Conduct regular audits of the facility as a group and individually. 3. Revise audit results as conditions change 4. Analyze audit results to determine where resources are best utilized. 5. Recommend the purchase of additional equipment as needed to complete the purpose. 6. Recommend construction activities as needed to complete the purpose. 7. Prioritize construction projects. 8. Forward audit issues to Facilities maintenance in the form of work orders and Power Point presentations. 9. Recommend capital expenditures to maintain and improve the facility.

Figure 6. Facility design team charter

Figure 7. “Seek and Destroy” process

stroy (S&D) Investigation Process (Figure 7) is a tool with many applications. The Seek & Destroy Process is a scientific method to: 1. Find pathogenic growth niches 2. Find potential growth niches requiring monitoring and control 3. Define normal level of disassembly 4. Define periodic deep level of disassembly 5. Define frequency of periodic deep level of disassembly 6. Qualify a new piece of equipment (run for 90 days then conduct Seek & Destroy Mission) 7. Validate effectiveness of equipment cleaning protocol 8. Validate effectiveness of intervention applied to a piece of equipment (heat treatment or other method) The piece of equipment should be completely and fully disassembled. Samples are taken for both APC and Listeria species. Observations for excessive organic matter are conducted. Data is produced to determine if the organism was harboring in that piece of equipment.

TIMED STUDIES Transfer vectors are defined and measured using Timed Studies. Here is an example of a Timed Study being used to locate a transfer vector bringing the organism to a line (Figure 8). In this case the line equipment had been proven to not harbor the contaminant (S&D Mission had been performed and all sites were negative) but a subsequent positive indicated a potential for contamination still exists. This method of sampling identifies the pathway and vehicles of transport to a line from the environment. Once a Transfer Point in the Transfer Vector is identified, the Timed Study method is deployed to trace back to the source of contamination which

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Investigation tools Table 2. Scientific methods for investigation following a positive sample

Figure 8. may be a piece of equipment, facility harborage site, or a barrier failure separating the high risk area from other parts of the plant. Growth niches in transient sites such as rework tubs, product totes, product racks, electric pallet jacks, and hand tools are often the hardest to locate in a large facility. The “Swat Team” sampling approach is the most successful method to find these mobile sources of contamination.

SWAT TEAM SAMPLING •

Sample during an idle period after sanitation, before production, ie. Saturday when no production is running. • Sample large areas using sponges or gauze. • Sample areas not typically sampled during routine sampling We found a transient growth niche using this method – (spell out) COP basket handles

Tool

Source of Environmental Contamination

S&D

Growth niche in line equipment

S&D

Growth niche in ancillary equipment

Swat Team

Growth niche in transient equipment

Timed Study

Growth niche in facility

Timed Study

Transfer of organism form outside exposed product RTE area to inside exposed product RTE area

Timed Study

Transfer vectors moving the organism within the exposed product RTE area.

GROWTH NICHE CONTROL Complex production equipment offers many opportunities for the development of growth niches. Growth niches evolve because the organism entering into a hard-to-dissemble and clean area. A common mode is from the rinsing process where the high pressure rinse water can force the organism into areas not disassembled such as press fit shafts on hollow rollers. The goal of sanitary design is to eliminate as many of these niches as possible. Those that cannot be eliminated by design need the ability to be easily exposed to the cleaning and sanitizing chemicals. Routine cleaning and sanitation including periodic deep cleaning should be able to maintain containment and prevent outgrowth to the point that shedding of the organism from growth niches creates a risk seeding a transfer vector capable of transferring the pathogen to the product or a product contact surface. Those growth niches that cannot be exposed need an alternative source of control such as the application of heat to pasteurize the equipment or equipment part. Sanitary design of the facility and equipment supplemented with Sanitation Process Control has been effective in preventing product contamination. Sani-

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tation Process Control is defined by the critical factors of the process. The critical factors cannot work alone; each must be effectively deployed during the cleaning and sanitizing cycle.

Sanitation Critical Factors • Degree of Disassembly • Chemical Sanitizer Treatment • Effective coverage (flood sanitation) • Time • Chemical concentration • Hand scrub contact surface • Heat Treatment • Small parts (COP tank) • Localized steam • Non Daily Scheduled Sanitation • Preventative and predictive deep cleaning • Equipment pasteurization • Effective GMP’s after flood sanitization Sanitation Process Control is supplemented with the control of transfer vectors, equipment interventions and periodic cleaning and sanitation procedures. During operations transfer vectors are controlled by: • Distinct hygienic zones established in the facility • Physical separation of raw ingredients from RTE finished product • Personnel and material flows are controlled to reduce hazards • Water accumulation is controlled inside the facility • Operational GMP’s are designed and executed to establish control and to prevent crosscontamination

Summary Process management is attained by Sanitation Process Control Critical Factors and Interventions for all equipment within the exposed product RTE area. Control methods and indicator site sampling are developed to maintain control.

Indicator sites are designed to provide an early warning of a potential breach of control. Indicator sites trigger deployment of specifically targeted interventions . Verification sites identify a loss of control. When control is breached or lost, the teams are responsible for regaining control. Verification sampling of product, contact surfaces and transfer points along the various transfer vectors of people, materials, equipment and product movement prove system capability. The elements of environmental control programs should address each of the following factors or items listed in Figure 9:

Requirements for an Effective Listeria Control Program •

The Sanitation process has been proven effective

•

The Sanitation process and Sanitary Manufacturing Operating Procedures are defined and repeatable.

•

General employee and Sanitation Operator Training programs clearly define and effectively communicate the process requirements necessary to maintain microbiological control.

•

Sanitation Process Control “Critical Factors” are identified and monitored.

•

Trained operators are used at each essential step.

•

If a new problem emerges, the monitoring and corrective action process will identify and direct the Corrective Action Team towards the location of the growth niche.

•

Random isolated strikes are proven to not be repeatable.

•

Consumer safety is assured by product sampling if process control appears to be violated.

•

Growth niches in any location within the Exposed Product Area are identified and are either eliminated or managed.

•

The environment within the Exposed Product Area is controlled to minimize microbial outgrowth.

•

Multiple barriers or hurdles create a “torturous pathway” to minimize the possibility of entry by a pathogenic organism from outside the Exposed Product Area.

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•

Physical transfer of microorganisms within the Exposed Product Area is addressed by the presence of multiple hurdles.

•

Additions or changes to the process or equipment within the Exposed Product Area are monitored and qualified to not introduce or harbor microorganisms.Data from investigation, indicator and verification sites should support each item. These items, when summarized, identify the pillars for microbiological process control technology: • • •

Apply interventions to eliminate the organism from exposed product area Control transfer of the organism Deploy process management techniques

Figure 9. Requirements for an effective Listeria control program “Teamwork is the fuel that allows common people to attain uncommon results” - Unknown

References AMI Listeria Intervention and Control Workshop, November 2000, Chicago, IL, Series 2000 - 2011. Bob Reinhard, personal communication. FSIS Directive, 12/09/2002. Microbial sampling of ready-to-eat (RTE) products for FSIS verification testing program. Available at http://www.haccpalliance.org/sub/food-safety/fsisdirective102403.pdf FSIS. 2009. FSIS Regulatory testing for LM in RTE prodcuts by calendar year 1990-2009. Available at http://www.fsis.usda.gov/PDF/Figure2_Micro_ Testing_RTE_1990-2009.pdf

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CONFERENCE PROCEEDINGS* Development of a Food Defense Workshop and Graduate Certificate in Food Safety and Defense for Working Professionals K. J. K. Getty1 Food Science Institute and Dept. Animals Sciences & Industry, Kansas State University, Manhattan, KS, 66506 *Arkansas Association for Food Protection (AAFP) Conference, Enhancing Food Protection from Farm to Fork, held on Sept. 28-29, 2010, Springdale, AR. 1

ABSTRACT To protect the American food supply, there is a need to educate graduate students and working professionals in food and agriculture-related fields about food defense. Kansas State University, Purdue University, and Indiana University-Purdue University at Indianapolis collaborated to develop a food defense curriculum for graduate students and working professionals. Thirteen stakeholders with expertise in food safety, food defense, and public health participated in a DACUM (Developing A CurriculUM) process that identified 210 knowledge domains for food defense professionals. A survey validated the DACUM results with 297 professionals participating. Survey participants ranked Food and Agricultural Systems, Food Safety and Defense, Communication, Threats to Food and Agriculture, and a Capstone Experience as key curriculum topics. Information from the DACUM process and survey were used to develop curriculum modules for a two-day workshop along with a one-day computer simulation/capstone experience. Fourteen modules were developed and presented by professors from all three universities and working professionals with expertise in each topic area. Each module contained learning outcomes, a set of notes, exam questions, and a recorded audio/video lecture for later use in distance education. Workshop participants (food defense stakeholders, graduate students, and working professionals – 41 total) indicated the quality of the workshop was “very good to excellent” on a five-point Likert scale and they unanimously said they would recommend the workshop to others. To further educate professionals about food defense, Kansas State University, Iowa State University, University of Missouri, and University of Nebraska jointly offer a Graduate Certificate in Food Safety and Defense. Keywords: DACUM, food protection, food defense, education, training, curriculum, distance education, graduate certificate, workshop, homeland security Agric. Food Anal. Bacteriol. 2: 15-24, 2012

Correspondence: K. J. K. Getty, kgetty@k-state.edu Tel: +1 -229-386-3363 Fax: +1-229-86-3239

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Introduction The agriculture and food sector has been formally identified by the U.S. Department of Homeland Security (DHS) as a critical infrastructure (Collins and Baggett, 2009), and Homeland Security Presidential Directive 9 (HSPD-9, 2004) establishes a national policy to defend the agriculture and food system against terrorist attacks, major disasters, and other emergencies. An intentional contamination of the food supply could have considerable public health, economic, and emotional impacts with significant destabilizing effects on the U.S. food industry. In order to protect the American food supply, there is a need to educate graduate students and working professionals in food and agriculture-related fields about food protection and defense. A review of literature and graduate-level listings indicated that there was limited information available for developing courses, learning modules, or a curriculum on food defense. Multi-state university consortiums have been formed to develop food defense courses, workshops, and a multi-state graduate certificate offered via distance. Purdue University, Kansas State University, and Indiana University-Purdue University at Indianapolis have worked together to develop a graduate level interdisciplinary, evidence-based, and comprehensive food safety and defense curriculum (Getty et al., 2009; 2010 and Linton et al., 2011). Three primary objectives of the consortium were: (1) to utilize the Developing A CurriculUM (DACUM) process to determine knowledge domains and skills needed by food safety and defense professionals, (2) to validate findings from the DACUM process through a survey sent to professionals working in food safety and defense, and (3) to develop modules for a two-day food defense workshop for stakeholders, graduate students, and working professionals and to validate the effectiveness of the workshop. The DACUM process was used to better determine the knowledge and skills needed by food defense professionals. This process provides an effective method for determining competencies or tasks that must be performed by persons employed in a given occupation area. DACUM has been used to analyze occupations

and assists in identifying content and knowledge gaps within an occupational category. The DACUM process operates on three important premises: (1) expert workers are better able to describe/define their job than anyone else, (2) any job can be properly described in terms of the tasks that competent workers in that occupation perform, and (3) all tasks have direct implications for the knowledge and attitudes that workers must have in order to perform the tasks correctly (Norton, 2008). The DACUM process starts by selecting key experts from an occupation being analyzed. They form a panel and work with a qualified DACUM facilitator to develop job profiles that can later be used for training programs or curriculum development. The information from the panel is then evaluated and validated through a survey by other practitioners and stakeholders in the field of study. Afterwards, educator teams can create learning modules, courses, and curricula based on the information validated through the DACUM process. Because food defense requires an interdisciplinary approach, a multi-state university collaborative approach is required to develop a comprehensive curriculum. Kansas State University, Iowa State University, University of Nebraska-Lincoln, and University of Missouri-Columbia also have been working together to develop and offer a distance Graduate Certificate in Food Safety and Defense (AGIDEA, 2010). The goal of the consortium is to bring together a group of food safety and defense courses that could be cross-listed at each university. A student would have a home university and then have an opportunity to take food safety and defense courses at four universities without the courses being classified as transfer credits.

Materials and Methods DACUM Process During a three day period with guidance from a trained facilitator from The National Registry of Food Safety Professionals, a panel of 13 stakeholders was assembled to identify knowledge domains, learning objectives, and core educational competencies required for food defense professionals. A survey was sent elec-

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tronically to professionals in the food and agriculture industry, academics, and public health. A total of 297 professional respondents validated 107 key knowledge items from the DACUM process. Key knowledge domains from the DACUM workshop were split into relevant categories by topic areas by the principal investigators prior to conducting a validation survey. A survey was sent electronically to professionals in the food and agricultural industry, academics, and public health and 297 professional respondents validated 107 key knowledge items from the DACUM process. All 107 items were ranked according to a combined Importance-Frequency (I-F) mean value, with the highest ranking item (1) having the highest I-F mean, and the lowest ranking item (107) having the lowest I-F mean. This ranked list was then split into quartiles (Q1=items ranked 1 to 27; Q2 = items ranked 28 to 54; Q3 = items ranked 55 to 81; Q4 = items ranked 82 to 107).

Table 1. Fourteen training module titles for the food defense workshop. Module Title 1.

The Food and Agricultural System as a Critical Infrastructure

The Food Agricultural System as a Potential Target of Attack

Policy and Risk Assessment

4., 5.

Threats to Food and Agricultural Systems, Parts 1 and 2

Vulnerability Assessment Methods

7. a, b Vulnerability Assessment Examples: a. Meat Industry and b. Grain Industry 8, 9.

Food Defense Plan Development, Parts 1 and 2

10.

Responding to Food Defense Incidents

11.

Emergency Management

12.

Public Health Systems

13., 14. Risk and Crisis Communication, Parts 1 and 2

Food Defense Workshop Information from the DACUM process and survey were used to develop curriculum modules for a twoday workshop (Getty et al., 2010; Linton et al., 2011) along with a one-day computer simulation/capstone experience (Harper et al., 2010). Fourteen modules were developed and presented by professors from all three universities and working professionals with expertise in each topic area (Table 1). Each module contained learning outcomes (Table 2), a set of notes, exam questions, and a live lecture that was audio/video recorded for distance education use. A brief survey was administered requesting feedback on the extent to which the module learning objectives were met, along with general module self-perception indicators of presentation value, knowledge gained, an overall module “grade,” and additional comments. Demographic information also was collected.

Graduate Certificate in Food Safety and Defense Faculty from Kansas State University, Iowa State

University, the University of Nebraska, and University of Missouri received a USDA-funded Higher Education Challenge grant to assist in the development of a Graduate Certificate in Food Safety and Defense to be offered via distance or oncampus. The basic concept was that the graduate certificate would be an inter-institutional program offered in conjunction with AGIDEA (www.agidea. org), an affiliate of the Great Plains Interactive Distance Education Alliance (GPIDEA). AGIDEA/ GPIDEA is a consortium of universities offering post-baccalaureate programs through distance education; the consortium framework provides students at each participating university with simplified access to courses offered across the other cooperating institutions. Core courses and elective courses were determined with a total credit hour equaling 12 hours (AGIDEA, 2010). Each institution proposed the Graduate Certificate in Food Safety and Defense through their respective Departments, Colleges, Graduate Schools, and Faculty Senate. Courses not offered by a home institution were proposed

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Table 2. Example learning outcomes from selected modules. Module Title and Learning Outcomes The Food and Agricultural System as a Potential Target of Attack •

Outline characteristics and attributes of the food and agricultural system that make it attractive as a target of intentional attack

•

List general groups of aggressors who might want to intentionally contaminate the food and agricultural system and their respective motivations

•

Identify and describe potential impacts of an incident involving intentional contamination of the food and agricultural system

Threats to Food and Agricultural Systems •

Understand the potential food safety hazards (biological, chemical, physical, radiological) and zoonotic diseases

•

Understand selected terrorist threats, hazards, and weapons

•

Realize the availability and accessibility of threat agents and hazards.

•

Understand the relevance of various threats to foods of different types

Vulnerability Assessment Methods •

Describe/discuss tools and methods that can be used by industry to identify and assess vulnerabilities in food and water systems

•

Explain why vulnerability assessments are performed in a food producing facility

•

Describe the factors that are considered when performing a risk assessment

Responding to Food Defense Incidents •

Describe and discuss response strategies, jurisdictional authority, and statutes involved in responding to a potential food defense incident.

•

Distinguish between law enforcement and public health goals regarding a food defense incident.

•

Describe the process of evidence gathering after a food defense incident.

as new courses and assigned home institution numbers. This would allow for a student to be enrolled at a home institution and take courses at the other participating universities without having to pay a different tuition rate or having the courses considered as transfer credits. The purpose of the certificate is to provide students with specialized education so that they can be better prepared to meet the challenges of accidental or deliberate food contamination within the food industry to protect public health, prevent foodborne illnesses, and facilitate or improve the profitability of food industries by minimizing health risks related to foodborne pathogens and toxicants. Students seeking admission to the Food Safety and Defense graduate certificate program must apply through and meet the standard admission requirements of their selected home institution. In addition, students should have an undergraduate degree in food science or otherwise meet the prerequisite requirements for admission to the Food Science Graduate Program. The consortium faculty also determined program requirements and have developed learning outcomes, assessment methods, and an exit survey.

Results DACUM Process The panel of stakeholders began the DACUM process by developing a job description for a food defense professional as follows: “To protect public health, preserve the economy, enhance national security, and protect the environment, a food defense professional provides leadership; evaluates food systems, facilities, property, products, people, and procedures for vulnerabilities; develops and implements policies and preventative control measures for food security/defense; and develops and implements effective food emergency responses by using analytical, empirical, assessment, detection, communication, observational techniques to address outcomes.” A total of 297 participants responded to the DACUM survey and 95 (30.2%) were from food manu-

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Ex pe d rie an nc d e Fo A od g Sy Sa st fe em ty s an d D ef en Co se m Fa m ci un lit Th ic y at re an io at d n As Si t se e ss Se m cu en rit t/V y ul ne ra bi lit y Ri sk An al Cr ys im is in Po al l ic Ju y st Iss ic ue e/ s Em In ve er st ge ig nc at io y M n an ag em en Pu t bl ic H ea lth Fo o

Mean I-F Value

5.0 4.5 4.0 3.5 3.0 2.5 2.0 1.5 1.0 0.5 0.0

Figure 1. Meana and standard deviation of importance-frequency (I-F) for each category from the DACUMb survey (n = 297). aCombined mean of importance and frequency score with each scored on a 5 point scale with 5 = extremely important or used all the time. bDACUM = Developing A CurriculUM.

facturing and 47 (14.9%) were from the agriculture production industry. In regards to level of education, 85 (28.6%) did not have a college degree, while 132 (43.3%) had a Bachelor’s degree and 59 (19.3%) had a Master’s degree. The follow-up survey confirmed the relevance of the competencies identified during the DACUM workshop, with mean knowledge areas importance ratings ranging from 3.4 to 4.6 (1=not at all important to 5=extremely important) whereas, frequency of use ranged from 2.8 to 4.3(1=never and 5=all the time). Knowledge domain categories related to a capstone experience, food and agricultural systems, food safety and defense, communication, and facility and site security received the highest Importance-Frequency (I-F) values of >3.9 on a 5 point scale (Figure 1) and ranked in the top quartile of 107 knowledge domains score (Figure 2). Examples of competencies receiving some of the highest mean importance-frequency ratings included those associated with assessing vulnerabilities within a food system, developing and implementing food defense plans, implementing security and defense measures, and responding to

food system incidents (Table 3).

Food Defense Workshop A total of 41 participants attended the workshop and included food defense stakeholders, graduate students, and working professionals. When asked, “Which of the following sectors most closely describes your current job?” - 27% indicated industry, 22% were regulatory, 17% were students, 10% others, and 2% didn’t indicate a sector. In regards to the demographic question, “Before attending this workshop, your knowledge about food protection and defense can be best described as:” - 15% responded great deal, 73% fair amount, 10% very little, and 2% didn’t respond. Overall, the quality of the workshop was found to be “very good” to “excellent” on a five-point Likert scale by the participants and they unanimously said they would recommend the workshop to others (Table 4). Participants commented that the workshop could have been strengthened with more examples of food defense scenarios, exercises focused on writ-

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Number of Knowledge Items

25 20 15

Q4 (#82-107)

Q3 (#55-81)

Q2 (#28-54) Q1 (#1-27)

Fo o

Ex pe rie Fo an nc od d e Ag Sa fe Sy ty st em an d D ef Co Fa en m Th ci se m lit re u y at ni a ca nd As tio se Si n te ss m Se en cu t/V rit ul y ne ra bi Ri lit sk y Cr An im al in ys al Po is Ju lic st y ic Iss Em e/ ue In er ve s ge st nc ig y at M io an n ag em Pu en bl t ic H ea lth

Figure 2. Quartile breakdown of combined importance-frequency by each category from the DACUM survey (n = 297). aCombined mean of importance and frequency score was ranked from 1 to 107 and divided into four quartiles. . bDACUM = Developing A CurriculUM. Table 3. Top 15 mean importance –frequency knowledge domains from the DACUM validation survey (n=297). Rank Category Knowledge Domain 1

Food and Ag Systems

Food industry best practices (GMPs, GAPs, and “prerequisite programs”)

Food and Ag Systems

Vulnerabilities in food and agriculture systems

Capstone Experience

Necessary components of a food defense plan

Capstone Experience

How to develop and implement a food defense plan for a specific facility

Food Safety and Defense

Potential food safety hazards (biological, chemical, physical, radiological)

Facility and Site Security

How to implement appropriate security systems and procedures to prevent a deliberate food contamination event

Communication

Proficiency in written and verbal communication

Food Safety and Defense

Food defense plan development

Food and Ag Systems

Food production systems and food product characteristics

Food Safety and Defense

Traceability (methods, processes, and systems)

Food Safety and Defense

Food processing facility and system operations

Food Safety and Defense

How food processing systems prevent, control, and mitigate food safety hazards

Food Safety and Defense

HACCP and associate prerequisite programs

Facility and Site Security

Physical and operations security countermeasures

Food Safety and Defense

Hazard detection, monitoring, and identification processes

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Table 4. Participants’ evaluation of the overall workshop program (n=29). Evaluation Statement

Mean Response ± Standard Deviation

± Standard Deviation

Table 5. Core and elective courses for the graduate certificate in food safety and defense. Core Courses (Required): 8 or 9 credits • A Multidisciplinary Overview of Food Safety & Security

Overall quality of program content.

4.41 ± 0.68

• Microbiology of Food (2 credits) or Food Microbiology (3 credits)

Overall quality of program modules.

4.21 ± 0.68

• Principles of HACCP

Overall quality of program presenters.

4.24 ± 0.74

Overall quality of handouts and materials.

4.10 ± 0.98

• Food Toxicants

Elective Courses: • Food Protection and Defense – Essential Concepts

Above means based on five-point Likert scale: 1 = poor, 2 = fair, 3 = good, 4 = very good, 5 = excellent

• Food Laws and the Regulatory Process

Did the program meet your needs?

2.97 ± 0.19

• Rapid Methods in Food Microbiology

Did the program meet your expectations?

2.93 ± 0.26

• Trade and Agricultural Health

Was the overall experience valuable to you?

3.00 ± 0.00

• Ethnic Foods: Food Safety, Food Protection and Defense

Would you recommend this workshop program to others?

3.00 ± 0.00

• Advanced Food Microbiology & Biotechnology • Microbiology of Fermented Foods

Above means based on three-point scale: 1 = no, 2 = somewhat/maybe, 3 = yes

ing a food defense plan, and modules that were specific about food defense.

Graduate Certificate in Food Safety and Defense The certificate program requires 12 credit hours comprised of core and elective courses (Table 5). Students must complete the required 12 credit hours with a cumulative GPA of at least 3.0 and may have no grade lower than a “B” in any certificate-program course. Learning outcomes (Table 6) also have been developed for the graduate certificate in food safety and defense. An exit survey is used as assessment tool and asks graduates to rate their abilities in regards to the learning outcomes (Table 7).

Discussion “Deliberate contamination of the nation’s food

Table 6. Learning outcomes for graduate certificate in food safety and defense. Learning Outcomes 1. Understanding the multi-faceted areas that are affected by food safety and defense issues and events. 2. Ability to apply the scientific principles of microbial and chemical risks as they relate to food safety and defense issues in real world situations. 3. Ability to apply the concepts of HACCP programs, as well as other safety and defense programs, in the food continuum and their critical role in food safety and defense. 4 Evidence that they can advance the knowledge, understanding, and appreciation of food safety and defense issues in the food industry. supply is a real possibility and the economic and psychological implications of an attack on the food supply are sobering. Some foods are more susceptible to deliberate contamination than others, but there is no practical way one can eliminate the possibility of being affected. Food terrorism utilizes a vector that affects everyone” (Stinson et al., 2007). The U.S. has

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Table 7. Self-assessment questions from the graduate certificate in food safety and defense exit survey. 1 - Strongly Disagree | 2 - Disagree | 3 - Neither Agree nor Disagree | 4 - Agree | 5 Strongly Agree. Question 42** required ** The Food Safety and Defense curriculum was designed to achieve specific learning outcomes upon successful completion of the program. Please provide a self-assessment of your achievement of the program learning outcomes.

42.1 My ability to discuss the multi-faceted areas affected by Food Safety issues has increased. 42.2 My ability to discuss the multi-faceted areas affected by Food Defense issues has increased. 42.3 My ability to develop and apply in real-world situations the scientific principles of microbial, chemical, and physical risks as they relate to Food Safety issues has increased. 42.4 My ability to develop and apply in real-world situations the scientific principles of microbial, chemical, and physical risks as they relate to Food Defense issues has increased. 42.5 My ability to develop and apply the concepts of HACCP (Hazard Analysis Critical Control Point) within food systems has increased. 42.6 My ability to develop and apply Food Defense programs within food systems has increased. 42.7 My confidence to implement and advance the knowledge, understanding, and appreciation of Food Safety issues in my institution, company or industry has increased. 42.8 My confidence to implement and advance the knowledge, understanding, and appreciation of Food Defense issues in my institution, company or industry has increased.

been dealing with the possibility of a terrorist attack on the food supply for years (CDC, 2003; Krusemark, 2009; Miller et al., 2002; Roth et al., 2008). The Dalles, Oregon, was the site of a terrorist attack on the food supply in September 1984. The Rajneesh cult inoculated salad bars at local restaurants with Salmonella Typhimurium so that the population would not be able to vote in the local elections (Miller et al., 2002). In late December 2002, 36 people became ill after purchasing ground beef at a Michigan supermarket. Following an investigation by the U.S. Department of Agriculture (USDA), it was determined that a disgruntled employee had intentionally contaminated over 200 pounds of product with the insecticide Black Leaf 40, an ingredient used for the production of nicotine (CDC, 2003). In 2007, the Food and Drug Administration (FDA) launched an investigation into the cause of unexplained deaths of several cats and dogs. The FDA determined that

the chemical melamine had been added to wheat gluten to falsify the protein content (Ibens, 2009; Lin et al., 2008). Based on these incidents and others, the U.S. government and academic institutions have begun and continue education efforts in the area of food defense. The National Center for Food Protection and Defense (NCFPD) was founded in 2004 as a Department of Homeland Security (DHS) Center of Excellence to research the vulnerabilities of the nation’s food supply to an intentional attack (NCFPD, 2006). The Center is composed of researchers and investigators from food industry companies, governmental agencies, and academic institutions. One of the Center’s research needs is education programs (NCFPD, 2006). Homeland Security Presidential Directive 9 (HSPD9, 2004) states, “We should provide the best protection possible against a successful attack on the Unit-

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ed States agriculture and food system, which could have catastrophic health and economic effects.” Educating current and future professionals in the food and agriculture systems about food defense is a means of providing information so that protection systems can be developed and implemented. Since there was a lack of comprehensive curriculum data on food defense, the DACUM process outlined a specific set of knowledge and skills needed for food defense professionals. The DACUM process assisted in identifying specific learning outcomes that could be implemented into modules for the food defense workshop. Overall, the workshop was effective in teaching graduate students and working professionals about food safety and defense. Formal food defense courses are needed to continually education professionals. The food defense workshop modules were revised and are included in a two-credit distance course (Food Protection and Defense – Essential Concepts) offered through Kansas State University and Purdue University. Lastly, the distance education Graduate Certificate in Food Safety and Defense serves the needs of the industry and agencies that must protect the human food supply from accidental or deliberate contamination with pathogenic microbes and/or toxicants (AGIDEA, 2010).

Acknowledgement The DACUM process and Food Defense Workshop was funded by USDA CSREES National Integrated Food Safety Initiative Award Number 06-51110-03595 and the National Center for Food Protection and Defense. The author has compiled education and research efforts by the following principal investigators and graduate students at each university: Purdue University - Richard Linton (currently at Ohio State University), William Field, Alok Chaturvedi, Clifford Racz; Indiana University – David McSwane and Theodore Grain; Kansas State University – Abbey Nutsch,Kelly Getty, Justin Kastner, Sheryl Hodge, Kelly Getty, Curtis Kastner, Dirk Maier, Nigel Harper, Keith Pritts, Blair Tenhouse, and Kathryn Krusemark; and National Registry of Food Safety

Professionals - Cynthia Woodley. Principal investigators for the Graduate Certificate in Food Safety and Defense include: Kansas State University – Abbey Nutsch, Deanna Retzlaff, and Curtis Kastner; Iowa State University – Suzanne Henrich; University of Missouri – Azlin Mustapha; and University of Nebraska-Lincoln – Robert Hutkins.

References AGIDEA. 2010. Programs, Degrees, and Courses: Food Safety and Defense. http://www.agidea.org. Accessed December, 2010. Centers for Disease Control and Prevention (CDC). 2003. Nicotine poisoning after ingestion of contaminated ground beef—Michigan. MMWR 52:413-6. Collins, P. A. and R. K. Baggett. 2009. Homeland security and critical infrastructure protection. Praeger Security International, Westport, CT. 2667 p. Getty, K. J. K., K. Pritts, N.M. Harper, A. L. Nutsch, R. H. Linton, W. Field, C. Racz, D. McSwane, S. Hodge, J. L. Kastner, C. L. Kastner, D. Maier, and M. M. Turner. 2010. Development of modules for a food defense workshop for graduate students and working professionals. Ann. Mtg., Inst. Of Food Technologist, Chicago, IL, July 17 – 20. Program Book. P. 95. (Abstr.) Getty, K. J. K., C. D. Woodley, D. McSwane, R. H. Linton, A. L. Nutsch, and S. Hodge. 2009. Development of a graduate curriculum in food safety and defense. Ann. Mtg., Inst. of Food Technologists, Anaheim, CA, June 9 – 12 (100-09) (Oral and Poster Presentation). http://www.ift.org/meetings-andevents/past-meeting-resources/Technical%20Abstract%20Search%20Details.aspx?id=2857. (Abstr.) Harper, N. M., T. H. Bhett, R. H. Linton, K. J. K. Getty, and A. R. Chaturvedi. 2010. Development of a capstone food protection and defense computerbased simulation for graduate students and working professionals. Ann. Mtg. International Assoc. Food Protection, Anaheim, CA August 1 – 4. http:// www.foodprotection.org/files/annual_meeting/ iafp-2010-abstracts-posters-2010.pdf. (Abstr.) HSPD-9. 2004. Homeland Security Presidential Di-

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rective/HSPD-9: Defense of United States agriculture and food. Weekly Compilation of Presidential Documents 40:183-187. http://www.hsdl.org/?vie w&doc=24144&coll=public. Accessed December, 2010. Ibens, D. 2009. The great melamine scare. Food Quality 16:18-20, 22-23. Krusemark, K.S. 2009. Decision-making applications in food safety and food defense. M.S. thesis. Kansas State University, Manhattan, KS. Lin, M., L. He, J. Awika, L. Yang, D. R. Ledoux, H. Li, and A. Mustapha. 2008. Detection of melamine in gluten, chicken feed, and processed foods using surface enhanced raman spectroscopy and HPLC. J. Food Sci. 73:T129-T134. Linton, R., A. Nutsch, D. McSwane, J. Kastner, T. Bhatt, S. Hodge, K. Getty, D. Maier, C. Kastner, A. Chaturvedi, and C. Woodley. Use of a stakeholderdriven DACUM process to define knowledge areas for food protection and defense. J. Homeland Security and Emergency Management. (In-press). Miller, J., S. Engelberg, and W. Broad. 2002. Germs: Biological weapons and America’s secret war. Simon and Schuster, New York, NY. 407 p. National Center for Food Protection and Defense (NCFPD). 2006. Program Summary of National Center for Food Protection and Defense. http:// www.ncfpd.umn.edu/about/reports/NCFPDprogramsummary.pdf. Accessed October, 2008. Norton, R. E. 2008. DACUM handbook. 3rd ed. Center on Education and Training for Employment, The Ohio State University, Columbus, OH. Roth, A. V., A. A. Tsay, M. E. Pullman, and J. V. Gray. 2008. Unraveling the food supply chain: strategic insights from China and the 2007 recalls*. J. Supply Chain Manag. 44:22-39. Stinson, T. F., J. Kinsey, D. Degeneffe, and K. Ghosh. 2007. Defending America’s food supply against terrorism: who is responsible? who should pay? Choices 22:67-71.

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CONFERENCE PROCEEDINGS* - REVIEW Human Noroviruses and Food Safety K. E. Gibson1 and S. C. Ricke1 University of Arkansas, Division of Agriculture, Department of Food Science *Arkansas Association for Food Protection (AAFP) Conference, Enhancing Food Protection from Farm to Fork, held on Sept. 28-29, 2010, Springdale, AR. 1

ABSTRACT Foodborne disease outbreaks occur each year in the United States, and the most common etiological agent is human norovirus causing an estimated 58% of all illnesses. Key characteristics of human norovirus (NoV) (i.e. resistance to environmental degradation and high concentration of viral shedding) allow food to be vulnerable to contamination with NoV at each step of the supply chain: pre-harvest, post-harvest, processing, and preparation. This review will highlight key characteristics of NoV, the sources and routes of contamination in particularly susceptible food items (i.e. bivalve mollusks, fresh produce, and ready-to-eat products), and the ways to potentially control and prevent the transmission of NoV in the farm to fork supply chain. Keywords: Human norovirus, food safety, acute gastroenteritis, minimally processed, ready-to-eat, prevention, calicivirus, person-to-person, environmental transmission Agric. Food Anal. Bacteriol. 2: 25-34, 2012

Introduction Human noroviruses (NoV) are estimated to cause 21 million cases of acute gastroenteritis each year—more than 90% of all nonbacterial outbreaks of gastroenteritis—and are the primary cause of foodborne disease outbreaks in the United States (Patel et al., 2009; Scallan et al., 2011). The socioeconomic burden of a single nosocomial NoV outbreak in a healthcare setting costs nearly $660,000 in lost revenue, sick leave and cleaning expenses (Johnston et al., 2007). The majority of NoV cases

Correspondence: Kristen E. Gibson, keg005@uark.edu Tel: +1 -479-575-6515

are caused by transmission via contaminated foodstuffs such as leafy vegetables, salads, sandwiches, oysters, baked goods, frosting, and fresh berries (Centers for Disease Control and Prevention, 2010). These foods may become contaminated with NoV: 1) at the source due to environmental inputs such as poor quality irrigation water, estuarine water, as well as organic fertilizers (i.e. municipal biosolids and compost) (Berger et al., 2010; Gentry et al., 2009; Wei and Kniel, 2010); 2) during manufacturing or packaging of final product (i.e. deli meats, packaged salad greens) (Malek et al., 2009); and 3) during preparation of a food item by an infected food handler (Tuan Zainazor et al., 2010). A recent report by Scallan et al. (2011) identified human norovirus as the ma-

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jor etiologic agent in foodborne illnesses acquired each year in the United States causing an estimated 58% of reported illnesses. This review highlights the 1) key characteristics of NoV; 2) transmission of NoV along the farm to fork supply chain; and 3) control and prevention of NoV within both the natural environment and food handling environments.

Key Characteristics of Human Norovirus Virus structure and classification As members of the Caliciviridae family, noroviruses are a group of evolutionarily related single-stranded, positive-sense RNA viruses—some causing gastroenteritis in humans. Noroviruses are 27 to 35 nm diameter in size, and their RNA genome (~7.5 kb) is surrounded by a nonenveloped, icosahedral protein capsid (Green, 2007). The capsid is composed of two viral proteins (VP)—a major protein capsid known as VP1 and a smaller basic structural protein known as VP2 (Hutson et al., 2004). Similar to other enteric viruses, NoV are divided into genogroups on the basis of genetic similarity across areas of the genome that are highly conserved, such as the RNA-dependent RNA polymerase (RdRp) (i.e. an essential enzyme that catalyzes the replication of RNA) and the VP1 capsid protein or shell domain (Green, 2007). To be classified in the same genogroup, NoV strains share at least 60% amino acid sequence identity in the major capsid protein VP1 (Hutson et al., 2004). There are five genogroups (GI, GII, GIII, GIV, GV) that have been identified along with more than 40 recognized genetic clusters, or genotypes, designated as GI.1 indicating genotype 1 within genogroup I (Atmar, 2010; Koopmans, 2008). Each genotype identified may also contain variant or recombinant strains which have been most recently outlined by Bull et al. (2007). The genogroups associated with human illnesses are GI, GII, and GIV with GII being the most common followed by GI (Atmar, 2010). Genogroup II and GIV also contain porcine-specific genotypes (GII.11, GII.18, GII.19) and a feline-specific genotype of norovirus, respectively, while GIII and GV are as-

sociated with bovine and murine hosts, respectively (Glass et al., 2009).

Epidemiology Human noroviruses enter the body primarily through the fecal-oral route, though transmission via aerosol droplets due to vomiting has also been reported (Marks et al., 2000; 2003). Based on limited volunteer studies and numerous epidemiologic studies, the incubation period for NoV ranges from 10 to 51 hours followed by an average of 2 to 3 days of illness (Glass et al., 2009). Symptoms of NoV infection include acute onset of nausea, vomiting, abdominal cramps, general malaise, and non-bloody diarrhea. Human noroviruses infect people of all ages, though recent outbreaks demonstrate that children under 5 years of age and elderly may experience more severe symptoms (i.e. fever and dehydration) requiring hospitalization (Patel et al., 2009). For the most part, infection with NoV is less severe than other diarrheal infections (such as those caused by Escherichia coli O157:H7 and Campylobacter). Asymptomatic infections are estimated to occur in one-third of all infected persons (Glass et al., 2009). Both outbreaks of NoV and sporadic cases can occur year-round, though they tend to peak in the colder months. In addition, NoV outbreaks have been reported most frequently in association with scenarios or environments that favor person-to-person contact such as nursing homes, hospitals, cruise ships, military, camping trips, and schools (Isakbaeva et al., 2005; Malek et al., 2009; Wadl et al., 2010; Wu et al., 2005).

Immunity Host susceptibility and specific immunological responses related to infection with NoV are not well understood due to the lack of a reproducible in vitro cell culture systems or small animal models for the cultivation of NoV (Duizer et al., 2004). Thus, the study of NoV has relied on immune electron microscopy and molecular methods such as reverse transcription PCR (RT-PCR) for detection. As a result,

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Pre-Harvest

Irrigation Water

Compost or Biosolids

Water impacted by sewage

Field (produce)

Estuary (oysters)

Post-Harvest Wash Water Quality

Environmental Surfaces

Washing/Processing

Product Consumed Raw

Food Preparation Food Contact Food Handler Surfaces Water Quality Prepared Foods

Product Consumed Ready-to-Eat

AGI (individual or outbreak)

Figure 1. Potential points of human norovirus contamination at each node in the farm to fork supply chain. AGI = acute gastrointestinal illness. the cellular receptors for NoV attachment had not been characterized until recently. Marionneau et al. (2002) hypothesized that NoV use carbohydrates (i.e. histo-blood group antigens) present on human gastroduodenal epithelial cells as ligands—similar to the attachment of rabbit hemorrhagic disease virus, also a member of the Caliciviridae family—and revealed that NoV do in fact bind to specific carbohydrates found on the exterior epithelial cell surfaces. Carbohydrate binding is a common method used by many viruses and other microorganisms to attach to their host cells (Hutson et al., 2004). In the case of NoV, the capsid (VP1 and VP2) binds to histo-blood group antigens (HBGA)—a group of structurally related carbohydrates found in secretions and on mucosal surfaces (Huang et al., 2003). Certain enzymes are important in the synthesis of HBGAs including fucosyl transferase-2 (FUT-2, secretor enzyme), FUT-3 (Lewis enzyme) and the A and B enzymes. Research has demonstrated that the FUT-2 enzyme plays a particularly important role in host susceptibility to NoV infection as individuals who are non-secretors (i.e. do not secrete FUT-2) do not become infected after challenge with NoV (Lindesmith et al., 2003). Based on a combination of human challenge studies, carbohydrate binding assays with NoV virus like particles (VLP; NoV capsid proteins VP1 and

VP2) and HBGA phenotyped salivary samples, and inoculation of inbred mice with NoV VLP (e.g., mice cannot be infected with human norovirus but an immune response can be induced), researchers have been able to piece together key aspects of NoV immunity. With respect to the human challenge studies, researchers demonstrated that immunity to NoV is short-lived (e.g., partial immunity retained for 6 to 14 weeks) making persons susceptible to repeated NoV infections with both different and identical genotypes throughout one’s life (LoBue et al., 2010). As explained previously, HBGA receptors on the mucosal surfaces of the gastrointestinal (GI) tract play a role in NoV infection; however, this only holds true for certain genotypes (i.e. susceptibility to some genotypes of NoV can be independent of secretor status) (Marionneau et al., 2002; Nordgren et al., 2010). In addition, resistance to NoV infection stems from a combination of genetic factors (i.e. non-secretors vs. secretors of certain HBGA carbohydrate receptors) and acquired immunity (i.e. recent infection) (Donaldson et al., 2010). Finally, research has shown that NoV evolves through the synergistic effects of antigenic drift and HBGA receptor switching—there is an immense range of similar, yet distinct HBGA receptors available on the GI tract surfaces that can interface with the NoV protein capsid carbohydrate

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binding domain (Lindesmith et al., 2008). Recent papers by Lindesmith et al. (2010a,b), Donaldson et al. (2010) and Teunis et al. (2008) provide more in depth examinations of the host susceptibility and immunological aspects of NoV infection.

Transmission of Human Norovirus Transmission of NoV through food, water, fomite (or inanimate) surfaces, and person-to-person is relatively easy owing primarily to the low infectious dose (median, approximately 18 viral particles) and the high concentrations shed in feces (1011 genomic copies per gram) over a prolonged periodâ&#x20AC;&#x201D;virus particles can be shed up to 4 weeks after exposure with peak amounts shed usually after physical signs of infection (Chan et al., 2006; Teunis et al., 2008; Tu et al., 2008). In addition, viral shedding of GII has been reported to be 100-fold higher than GI therefore possibly explaining GII dominance in outbreaks and persistence in the population (Chan et al., 2006). For the purposes of this review, transmission of NoV at critical nodes along the farm to fork supply chain will be addressed (Figure 1).

Pre-harvest Contamination of fruit and vegetable crops and bivalve mollusks with NoV may occur during the initial phase of the supply chain during pre-harvest. With respect to fruits and vegetables, NoV may be introduced to crops via contaminated irrigation water and agricultural lands (Mara and Sleigh, 2010; Wei and Kniel, 2010). Soil and source water used for irrigation may become contaminated by leakage of onsite sewage systems (septic systems) or sewer pipes and runoff of municipal biosolids or contaminated soil from nearby land due to flooding or heavy rain. Because of these contamination scenarios, several studies have investigated the ability of NoV to survive in the environment (Dawson et al., 2005), adsorb to biosolids and food surfaces, and to be internalized by produce, specifically leafy vegetables (Wei et al., 2010a; 2010b). In general, NoV survival in the environment or on plant surfaces is dependent

on the type of fruit or vegetables (e.g., increased survival on lettuce), ambient temperature, relative humidity, and type of soil (i.e. faster movement through a soil column to groundwater source if coarse or through a finger-flow soil) (McLeod et al., 2001). A recent review paper by Wei and Kniel (2010) provides an overview of the potential vehicles of pre-harvest viral contamination of fresh produce crops and additional information about current research involving virus fate and transport in the environment. Contamination of bivalve mollusks, specifically oysters, with NoV during production has been welldocumented (Bosch and Le Guyader, 2010). Inherent to the way oysters are produced, bay and estuary environments impacted by fecal matter through land runoff, sanitary sewer overflows, or wastewater effluent discharge (Gentry et al., 2009; Shieh et al., 2003) are the primary vehicles of contamination. The susceptibility of oysters to contamination with NoV can also be attributed to the fact that oysters are filter feeders and tend to accumulate and concentrate viruses and other microorganisms within their digestive system over time. A recent article by Le Guyader (2006) helped to further elucidate the association of oysters with NoV by demonstrating that oysters were found to have A-like carbohydrate structures along their digestive ducts which are indistinguishable from human blood group A antigens (Le Guyader et al., 2006). The research by Le Guyader and others (2006) indicates that NoV-specific binding may occur in oysters thus making control of NoV contamination in oysters even more challenging. In addition, strain dependent NoV bioaccumulation in oysters has also been demonstrated recently in which GI.1 strain bioaccumulates very efficiently in oysters while the GII.4 strain (i.e. the NoV strain which predominantly circulates within the population) bioaccumulates very poorly (Maalouf et al., 2011). Maalouf et al. (2011) indicate the difference in binding is due to ligand expression in the oyster digestive tissues.

Post-harvest and processing Post-harvest food product contamination is mostly related to on-farm harvesting practices

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as well as the efficacy of the methods used for washing and sanitizing fresh produce. Some of the harvesting practices that may allow fresh produce to become contaminated include: 1) barehand harvesting combined with a lack of personal hygiene (i.e. hand washing); 2) continuous use of disposable (latex) gloves (e.g., accumulation of organic matter contaminated with NoV could allow for wide-spread distribution within a crop) without appropriate sanitation (LGMA, 2010); and 3) contaminated harvest containers and tools (Luo, 2011). After harvesting in the field, fresh produce may also become contaminated through contact with wash water used for cleaning and sanitation.

Food preparation Human norovirus contamination during food preparation is reportedly the most common cause of NoV outbreaks with a known food commodity. Within the food preparation environment, NoV may be transferred to food by contaminated surfaces, a food handler infected with NoV (symptomatic or asymptomatic) and not utilizing best practices (i.e. hand washing, glove use), or the use of sanitizing agents ineffective against NoV (Newell et al., 2010). A nine part review series on food workers and spread of foodborne disease published in Journal of Food Protection from 2007 to 2010 highlights NoV as the primary etiologic agent in these scenarios and discusses the factors contributing to outbreaks, the transmission and survival of pathogens in the food preparation environment, and reduction of contamination (Greig et al., 2007). Because of the low infectious dose, high number of viruses shed during infection and non-enveloped structure, NoV can spread easily and persist for extended periods of time in the food preparation environment even if proper hygiene and sanitation procedures are followed.

Control and Prevention of Human Norovirus Because of their nonenveloped structure, NoV is presumed to be relatively resistant to chemical inacti-

vation (i.e. chlorination) and environmental degradation (temperature, pH, ultraviolet radiation, desiccation) which aids in the ease of transmission (Green, 2007). However, the persistence of infectious NoV in water sources, on food contact surfaces and in food products under various conditions (i.e. temperature, pH, ultraviolet radiation) has been difficult to study due to the lack of reproducible cell culture systems for propagation and detection of viable NoV (Duizer et al., 2004). Thus viral surrogates including murine norovirus (MNV), feline calicivirus (FCV), and MS2 bacteriophage have been utilized for studying the physicochemical properties of human norovirus (Bae and Schwab, 2008; Belliot et al., 2008; Nappier et al., 2008). Both FCV and MNV are members of the Caliciviridae family; however, FCV (a feline respiratory virus) belongs to the Vesivirus genus whereas MNV is located within the Norovirus genus (genogroup V) making it morphologically and genetically similar to human norovirus. Until recently, FCV was the predominant surrogate used for studying NoV, and as a result, many guidelines and recommendations for NoV are based on the characteristics of FCV with respect to control and prevention in the environment and in food products (e.g., recommended sanitizing agents, disinfection of drinking water, thermal inactivation, etc.).

Fresh Produce For the control of NoV contamination from farm to fork, food safety guidelines need to be revamped to include both viral and bacterial pathogens. Traditional parameters (i.e. pH, temperature, water activity) for control and inactivation of microorganisms during food processing have historically focused on bacterial pathogens, such as E coli O157:H7, Listeria monocytogenes, and Salmonella spp., and not viral pathogens (Grove et al., 2006; Hirneisen et al., 2010; Koopmans and Duizer, 2004). Additionally, most of the engineering processes or interventions along the supply chain are also focused on the control of bacterial pathogens and should be adjusted to target viruses as well (Mormann et al., 2010). With respect to onfarm food safety, irrigation water should be tested for more than just bacterial indicators (i.e. fecal co-

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liforms) as previous studies have demonstrated that these bacteria poorly correlate with the presence of human enteric viruses (Gerba et al., 1979; Gibson et al., 2011; Harwood et al., 2005). In addition, harvesting practices related to fresh produce such as washing products with a sanitizing agent should be validated for efficacy against enteric viruses—chlorine bleach is most commonly used though the concentration and contact time may be ineffective against viruses (Hirneisen et al., 2010). More advanced technologies such as high pressure processing (HPP) have been reported as effective against MNV inoculated in fresh vegetables and produce; however, HPP may affect the quality of the product and may only be suitable for fruits intended for frozen storage (Lou et al., 2011).

Oysters For the control and prevention of NoV contamination in oysters, the primary goal is to maintain good water quality in estuaries. Some regulations such as the Clean Vessel Act (33 U.S.C. 1322, 106 Stat 5039) have been put in place to prevent the discharge of sewage in oyster harvesting areas (USFWS, 1992). In addition, estuary sites should be located away from wastewater effluent discharge (i.e. upstream instead of downstream), and these sites should be in areas protected against the impacts of potential sanitary sewer overflows, septic system failures, and stormwater runoff. Post-harvest, oysters are subjected to a practice called depuration. During depuration, oysters are placed in tanks of clean seawater and allowed to resume normal pumping (filtration) activity for a period of time that may range from a few hours to days in order to expel microbial contaminants (Lee et al., 2008). However, research involving bioaccumulation and depuration of NoV in oysters demonstrates that there is a selective retention mechanism for NoV within oysters possibly due to the similarity in NoV binding sites between humans and oysters indicating attachment of NoV rather than simple sequestering of the virus (Nappier et al., 2008; Schwab et al., 1998; Ueki et al., 2007). Oysters may also undergo HPP during whole oyster processing to inac-

tivate bacterial and viral pathogens that have been sequestered in the oyster. During HPP, the oysters are killed by the high pressure treatment therefore this intervention would only be applicable to oysters sold as meat without the shell (Grove et al., 2006).

Food Preparation In the food preparation environment, control and prevention of NoV starts with good handling practices (GHP) and strict personal hygiene. Regular and consistent hand washing by food handlers can be a very effective tool in preventing the spread of microbial contaminants when promoted effectively (Chapman et al., 2010). Education and training, positive incentives, and reinforcement from managers may increase the frequency and quality of hand washing by food handlers (Moe, 2008). In addition, food handlers who experience an episode of acute gastrointestinal illness should communicate this information to their employer and proper precautions should be taken such as exclusion of ill workers during the period of illness—two to three days has been recommended; however, viral shedding occurs over a much longer period of time (Parashar et al., 2001). In general, minimal bare-hand contact during preparation of foodstuffs and proper disinfection of environmental surfaces is crucial to prevention. A list of antimicrobial products effective against NoV is available through the USEPA Office of Pesticide Programs; however, it should be noted that most of the products listed have only been proven effective against FCV and not specifically against NoV(USEPA, 2009).

CONCLUSIONS In the United States there is currently no systematic surveillance for human norovirus—only a select number of bacterial and parasitic pathogens are actively monitored (Centers for Disease Control and Prevention, 2010). Passive monitoring is primarily due to the short duration and overall nature (i.e. nonfebrile, no bloody diarrhea) of illness caused by NoV as well as the lack of routine clinical tests for NoV

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available in hospitals. Therefore, NoV is usually diagnosed only when an outbreak occurs as opposed to sporadic, individual cases. This passive approach to monitoring NoV in the United States presents a wide knowledge gap with respect to the endemic nature of NoV as well as the true magnitude that contaminated foodstuffs may have in the spread of NoV. Enhancing the capacity of state and local laboratories would significantly increase our knowledge about the prevalence of NoV and would help capture unreported outbreaks due to NoV. In addition to monitoring the population for NoV, steps should be taken to monitor for NoV in high-risk foodstuffs (i.e. fresh produce and oysters). Methods for the detection of NoV have improved dramatically over the past decade by using techniques such as real time quantitative RT-PCR as well as advanced methods for concentration of NoV from food and water. To do this, a standard protocol for the isolation and detection of NoV from food, water, and fomite surfaces should be established. Overall, we should begin to shift the approach used for monitoring and control strategies and move from being reactive to being proactive and focus on prevention. This can be done through understanding of the key characteristics of human noroviruses.

Acknowledgement Support is gratefully acknowledged from a NIFSI (2010-51110-21004) grant to author Ricke.

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2003. Molecular surveillance of enterovirus and Norwalk-like virus in oysters relocated to a municipal-sewage-impacted gulf estuary. Appl. Environ. Microbiol. 69:7130-7136. Teunis, P. F., C. L. Moe, P. Liu, S. E. Miller, L. Lindesmith, R. S. Baric, J. Le Pendu and R. L. Calderon. 2008. Norwalk virus: How infectious is it? J. Med. Virol. 80:1468-1476. Tu, E.T., R. A. Bull, M. J. Kim, C. J. McIver, L. Heron, W. D. Rawlinson and P. A. White. 2008. Norovirus excretion in an aged-care setting. J. Clin. Microbiol. 46:2119-2121. Tuan Zainazor, C., M. S. Hidayah, L. C. Chai, R. Tunung, F. M. Ghazali and R. Son. 2010. The scenario of norovirus contamination in food and food handlers. J. Microbiol. Biotechnol. 20:229-237. Ueki, Y., M. Shoji, A. Suto, T. Tanabe, Y. Okimura, Y. Kikuchi, N. Saito, D. Sano and T. Omura. 2007. Persistence of caliciviruses in artificially contaminated oysters during depuration. Appl. Environ. Microbiol. 73:5698-5701. USEPA. 2009. List G: EPA’s registered antimicrobial products effective against norovirus (Norwalk-virus). US Environmental Protection Agency, Office of Pesticide Programs, January 9, 2009. Available at: http://www.epa.gov/oppad001/chemregindex. htm Accessed on: March 1, 2011. USFWS. 1992. Clean Vessel Act. 33 U.S.C. 1322, 106 Stat 5039. Wadl, M., K. Scherer, S. Nielsen, S. Diedrich, L. Ellerbroek, C. Frank, R. Gatzer, M. Hoehne, R. Johne, G. Klein, J. Koch, J. Schulenburg, U. Thielbein, K. Stark and H. Bernard. 2010. Food-borne norovirusoutbreak at a military base, Germany, 2009. BMC Infect. Dis. 10:30. Wei, J. and K. E. Kniel. 2010. Pre-harvest viral contamination of crops originating from fecal matter. Food Environ. Virol. 2:195-206. Wei, J., Y. Jin, T. Sims and K. E. Kniel. 2010a. Survival of murine norovirus and hepatitis A virus in different types of manure and biosolids. Foodborne Pathog. Dis. 7:901-906. Wei, J., Y. Jin, T. Sims and K. E. Kniel. 2010b. Manureand biosolids-resident murine norovirus 1 attachment to and internalization by romaine lettuce.

Appl. Environ. Microbiol. 76:578-583. Wu, H. M., M. Fornek, K. J. Schwab, A. R. Chapin, K. Gibson, E. Schwab, C. Spencer and K. Henning. 2005. A norovirus outbreak at a long-term-care facility: The role of environmental surface contamination. Infect. Control Hosp. Epidemiol. 26:802-810.

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CONFERENCE PROCEEDINGS* Development and Assessment of Success for Retail Food Safety Programming in Indiana R. H. Linton1 Department of Food Science and Technology, The Ohio State University, Columbus, Ohio 43210 *Arkansas Association for Food Protection (AAFP) Conference, Enhancing Food Protection from Farm to Fork, held on Sept. 28-29, 2010, Springdale, AR. 1

ABSTRACT The Centers for Disease Control and Prevention estimates 47.8 million cases of foodborne illnesses, 127,839 hospitalizations, and 3,037 deaths occur each year in the United States. The most common risk factors leading to foodborne illness are; poor personal hygiene, improper holding temperatures, contaminated equipment, inadequate cooking, and food from an unsafe source. All of these are important food handling practices for food handlers that work in retail food establishments. The focus of the current study was to evaluate the collective success of different retail food safety programs in Indiana including the ServSafe® program, SafeMarkTM program, and the “Purdue University Food Safety Day” program. Success was documented over an 11 year period (2000-2010) based on the number of participants involved in the program, passing rate and scores on national retail protection certification exams and positive changes made in food handling behavior. In the 11-year period, nearly 16,000 retail food handlers were successful in passing the retail food manager’s certification exam. Three months after participating in one of the three offered programs, over 15,000 participants responded to a survey. The results of the survey indicated that food handling behavior changes were made in hand washing, cooking, cooling, separation of raw from ready-to-eat foods, and in sanitation programs. The most important learning lesson gained from this success was to work with stakeholders in your state to identify and implement effective food safety educational programs. Keywords: retail, foodservice, food safety, food protection manager’s certification, behavior changes Agric. Food Anal. Bacteriol. 2: 35-42, 2012

Introduction The newest foodborne statistics provided by the Centers for Disease Control and Prevention (CDC) estimate 47.8 million cases of foodborne illnesses, 127,839 hospitalizations, and 3,037 deaths occur Correspondence: R. H. Linton, linton@purdue.edu Tel: +1 -765-494-6481 Fax: +1-765-494-7953

each year in the United States. These CDC estimates translate into approximately 1 in every 6 Americans becoming sick because of a foodborne illness each year. CDC data show that the most common pathogens leading to foodborne illnesses are caused Norovirus, non-typhoidal Salmonella, Clostridium perfringens, Campylobacter spp., and Staphylococcus aureus (CDC, 2011). CDC also recently presented specific foodborne illness statistics for the year

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2007. In 2007, the most common “combined pathogen-commodity pairs” that were responsible for the most outbreak-related illnesses were: Norovirus in leafy vegetables (315 illnesses), E. coli O157:H7 in beef (298 illnesses), and, Clostridium perfringens in poultry (281 illnesses) (CDC, 2010). All of the risk factors identified from actual outbreaks are significant issues in retail food safety and minimizing their impact is important to retail food handlers. The U. S. Food and Drug Administration (FDA) publishes the FDA Food Code, a model code that assists food control jurisdictions at all levels of government by providing them with a scientifically sound technical and legal basis for regulating the retail and foodservice segments of the food industry (FDA, 2009). The FDA Food Code provides practical, science-based guidance and manageable, enforceable provisions for mitigating risk factors known to cause food-borne illness. The FDA Food Code is a reference document for regulatory agencies that ensure food safety in foodservice establishments, retail food stores, other food establishments at the retail level, and institutions, such as nursing homes and child care centers. Contributors to the development of the FDA Food Code are CDC, U.S. Department of Health and Human Services (HHS), and the Food Safety and Inspection Service (FSIS) of the US Department of Agriculture (USDA). The Conference for Food Protection (CFP) provides recommendations for FDA Food Code standards. Local, state, tribal, and federal regulators use the FDA Food Code as a model to develop or update their own food safety rules and to be consistent with national food regulatory policy. The full version of the FDA Food Code is published every 4 years. To date, 48 of 56 States and territories have adopted food codes patterned after one of the five versions of the FDA Food Code, beginning with the 1993 edition. Those 48 states and territories represent 79% of the U.S. population. While regulations may differ for food handling among different states and jurisdictions, the information in the FDA Food Code serves as the most uniform resource for developing education and training programs in retail food safety. A wide variety of food safety training programs have been developed

by academic institutions, food industry associations, and the federal government. Some of these training programs are linked with retail food protection manager’s certification exams that are offered on the national level. The ServSafe® program offered by the Educational Foundation of the National Restaurant Association, and the SafeMarkTM Program offered by the Food Marketing Institute, are examples of leading food safety programs with certifications that are provided to the retail food industry. The retail segment of the food flow chain is important from a food safety perspective for many reasons. This is usually the last step in the flow of food where ready to consume food is handled, and because of this, risk of foodborne hazard transmission and growth can be greatly impacted. Within retail food establishments, food safety education focuses on managing CDC foodborne illness risk factors that are known to be leading causes of foodborne illness. These factors include temperature and time control, good personal hygiene, prevention of cross-contamination, effective cleaning and sanitation programs and purchasing foods from an approved source (CDC, 2011). The state of Indiana has been a leader in developing and delivering retail food safety programming. At a statewide level, Purdue University, Indiana University, the retail food industry, and state/local regulatory agencies have partnered together to promote food safety education and provide a variety of programs intended for management and sub-management level food handlers. Retail food safety education programs are generally offered with or without a national retail food protection manager’s certification exam. The CFP is an independent voluntary organization that has identified essential components of a nationally recognized retail food protection manager certification program and established a mechanism to determine if certification organizations meet these standards. States where manager certification is required, and an updated listing of food manger certification requirements, by state, can be found at www.retailfoodsafety.org. or at http://www.nrfsp.com/state_ regulations/.

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In Indiana, food retail protection manager certification is required by State law. And, while training is not a mandatory component of this law in Indiana, there is growing need for retail food safety education to prepare food handlers to take the certification exam. Two nationally recognized training programs linked to a retail food manager’s certification exams were offered through the Purdue University Cooperative Extension Service. The National Restaurant Association’s ServSafe® program (NRA 2011) is targeted for restaurant and food service operations. It is offered as a 2-day training program, with the certification exam being given following the training. The Food Marketing Institute’s SafeMarkTM program (FMI, 2011) targets grocery store and convenience store operations and is offered using a similar training and exam format. Both of these programs are directed toward food manager level personnel. Content includes information about foodborne hazards, prevention of foodborne hazards, interventions that can be used throughout the food flow, sanitation programs, pest control, food safety management programs, and retail food safety regulations. Another program, called “Food Safety Day,” was developed at Purdue University and this 2-hour program is intended for sub-management level personnel. The focus of the program is to teach the basic principles of fooborne hazards, time and temperature control, good personal hygiene, effective sanitation and cross-contamination prevention. The overall intent of this paper is to describe a journey that we have taken in the state of Indiana to develop effective retail food safety educational programs. As part of this journey, a needs assessment, success on retail food protection manager’s certification exams, positive changes in food handling behavior, and lessons learned will be described.

Materials and Methods Food Safety Assessment

Programming

Needs

state of Indiana. The simple survey contained one question: What type of food safety programs are needed in the state of Indiana? Five options were provided including: 1) hazard analysis critical control point training, 2) sanitation training, 3) training of good manufacturing practices, 4) the FDA better process control school, and 5) Other (which provided an option to write in alternative training needs and ideas). The survey was distributed to stakeholders in the state that represented the food industry, regulatory agencies, academic institutions and other affiliated food safety-related organizations. The data was then recorded and presented as percent positive response to each of the different programming options.

Programming Statistics Since 2000, for each food program that was offered through Purdue University Cooperative Extension, questions were asked of participants in the programs via a survey instrument that was provided to each participant 3 months after the food safety training program. The survey contained questions about participant demographics and experience, questions about participant changes in food safety behavior, and questions about future training. The results from each of these question sets were tabulated. Actual numbers were recorded for demographic and experience questions, and, percentage of participants was plotted against participant response for the behavioral and training-based questions.

Demographic Questions

and

Experience

Four questions were asked to each participant to understand some of our demographics as well as experience as a food handling. These questions are provided on the following page with possible responses to each question.

In 1998, a survey was created and distributed to over 3,000 food safety-related stakeholders in the Agric. Food Anal. Bacteriol. • AFABjournal.com • Vol. 2, Issue 1 - 2012

1. My current job position is: ____ Chef or cook ____ Management ____ Server or wait staff ____ Other _____________

or “Already Doing.” Data were pooled and the mean values and standard deviations were determined. Differences between samples were determined using a Student’s t-test, with Microsoft Excel (Microsoft Windows XP), and were considered to be significant when p<0.05.

2. I have worked in food service: ____ Less than 1 year ____ 1 to 3 years ____ More than 3 years

Further Training Questions Two additional questions were used to determine if the food safety training had an impact on further training. These include: 1. I have conducted training in safe food handling practices for staff. 2. I have received more training in safe food handling practices. For these two questions, participants were asked to answer as either “Yes”, or “No.”

3. My highest level of education is: ____ Less than high school ____ High school graduate or GED ____ Technical school or some college ____ College graduate or beyond 4. My ethnic group is: ____ African American ____ Asian ____ Caucasian ____ Hispanic ____ Other _____________

Changes Questions

Food

Success and Scores on National Food Protection Manager’s Certification Exams

Safety

Behavior

Five questions were used to assess changes in food safety behavior and changes in food handling practices. These include: 1. I or my staff washes hands more frequently during food preparation and service. 2. I or my staff checks the temperature of food to make sure that it is cooked to a safe temperature. 3. I or my staff takes the temperature of food to make sure that it has been cooled quickly to a safe temperature. 4. I or my staff keeps raw foods (such as fish, poultry, and ground beef) separate from ready-to-eat foods (such as cooked foods, fresh fruit and vegetables). 5. I or my staff makes sure that all work surfaces, equipment, and utensils have been cleaned and sanitized before preparing and serving foods. For each question stated above, participants were asked to answer as either “Yes”, “No”, “Sometimes,”

Scores and passing rates for national food protection manager’s certification were recorded over the period of 2000-2010. Scores were obtained by the Educational Foundation of the National Restaurant Association (ServSafe® exams) and by the National Registry of Food Safety Professionals (SafeMarkTM exams).

Results Food Safety Programming Needs Assessment A total of 843/3,000 surveys were returned. Results from the stakeholder survey showed that the food safety programming that was identified as the most important need was “retail food safety programming.” This was a surprising outcome since retail food safety programming was not an original choice; rather it was a write in choice under “other.” More than 80% of respondents indicated the need to retail food safety programs, followed by 65%, 44%, and 28% indicating the need for hazard analysis critical control programs, good

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My current job position is:

My highest level of education is:

Chef or cook

Server or wait staﬀ

Less than high school

Management

Other

Technical school or some college

Less than 1 year 1 to 3 years More than 3 years

10% 15% 75%

28%

African American High school graduate 3% or GED Hispanic 3% College graduate Asian 2% or beyond Other 2% 11% Caucasian 18% 90%7%

25%

36%

26%

49%

n= 15,819 n= 15,819

I have worked in food service: Less than 1 year 1 to 3 years More than 3 years 10%

My ethnic group is: African American Asian Caucasian

Hispanic Other 3% 3%

15%

2%2%

75% 90%

n= 15,819 n= 15,819

Figure 1. Demographic and experience questions asked to participants of Indiana retail food safety training programs for: a) job position, b) level of education, c) years worked in foodservice, and d) ethnic group.

manufacturing practices and sanitation, and the FDA better process control school. As it turns out, the State of Indiana was in the process of approving mandatory retail food manager’s certification statewide. The new law would require retail food managers to pass an approved national certification exam. While training was not required in the new law, certainly statewide training would be needed.

Demographic and Experience Questions Figure 1 provides information for the demographics and experience of the participants that have been involved in all of the food safety training programs. The data provides a good representation of the retail industry (Figure 1a) including those that prepare foods, those that serve foods, and those that manage the day-to-day operations. Nearly all of

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20 10

% Participants

70 60

Sometimes No Already Doing Participant Response "I or my staff takes the temperature of food to make sure that it has been cooled quickly to a safe temperature." a

Yes

b c

20 10

4 1 35

Yes

Yes 60 Sometimes 50 No Already Doing 40

62 12 b 8 20

"I or my staff checks the temperature of food to make sure that it is cooked to a safe temperature." 70 a 62

b c

Yes

Sometimes No Already Doing Participant Response

60 50

40 30

Yes 58 20 Sometimes 2 10 No 1c 0 Already Doing 38 Yes Sometimes No

c Already Doing

Participant Response

Sometimes No Already Doing Participant Response

Figure 2. Changes in food handling behaviors for participants of Indiana retail food safety training programs for: a) hand washing, b) cooking, c) cooling, separation of raw from readyto-eat foods, and, e) sanitation (n=15,819). Different low case letters above each bar indicate significant difference (P<0.05).

"I or my staff keeps raw foods separate from ready-to-eat-foods."

% Participants

Yes Sometimes No Already Doing

"I or my staff makes sure that all work surfaces, equipment, and utensils have been cleaned and sanitized before preparing and serving foods." 70

% Participants

"I or my staff washes hands more frequently during food preparation and service."

% Participants

40 30 20 10 0

Yes

40 Agric. Food Anal. Bacteriol. • AFABjournal.com • Vol. 2, Issue 1 - 2012

Sometimes No Already Doing Participant Response

Table 1. Number of participants involved in retail food protection manager’s certification programs in Indiana from 2000-2110, exams scores, and percent certified. Year

Participants

2000

596

91.3

93.8

2001

611

90.8

92.4

2002

783

91.8

92.8

2003

919

92.1

93.1

2004

1,981

91.5

92.5

2005

2,245

92.0

94.1

2006

1856

92.4

95.1

2007

1498

91.5

2008

1617

92.0

91.3

2009

1366

94.3

95.3

2010

2813

93.7

94.2

16,285

Ave = 93%

Ave = 94%

Scores (%) Certified (%)

the participants had a high school graduate degree or higher (Figure 1b) and have worked in the industry for 3 or more years (Figure 1c). The ethnic group identified in this survey was mostly Caucasian (Figure 1d).

Changes Questions

well as future training that they may lead for their staff. A total of 63% of participants indicated that they conducted more training as a result of this training, and 45% received further training in food safety.

Food

Safety

Behavior

Figure 2 presents perhaps the most interesting data. This data identifies changes in behavior as a result of the food safety training programs. Note that with all questions asked, there was a positive change noted from the survey in all aspects of food handling behaviors. The food safety training programs seemed to make an important difference. As a result of the training, food handling practices were improved for areas identified by CDC as important risk factors including hand washing, cooking, cooling, separation of raw from ready to eat (cross-contamination control), and for sanitation programs.

Further Training Questions Finally, participants were also asked questions about future training that they may have as a result of the food safety training programs in Indiana as

Success and Scores on National Food Protection Manager’s Certification Exams Table 1 provides data over an 11 year period for success on Retail Food Protection Manager certification exams. Over this time period average exam scores were nearly 93%, and, the overall passing rate was 94%. As a comparison, the national average for passing rates on the ServSafe® and SafeMarkTM exams is typically between 80-90%.

Discussion There are many considerations when developing effective retail food safety training programs and there are many learning lessons to be gained. The State of Indiana has embarked on a decade long journey to make a difference in retail food safety programming. Some of the important learning lessons we have learned are: • Work with your stakeholder groups in the state and ask them what they need relative to retail food safety training. If you respond to these needs, you will have strong stakeholder support. • Form a partnership with key state stakeholders. In Indiana, Purdue University formed a 3-way partnership with academic institutions (Purdue University, Indiana University, Purdue University Cooperative Extension), food industry organizations (Indiana Retail Grocers Association, Indiana Restaurant and Hospitality Association) state regulatory agencies (Indiana State Department of Health and local health departments). • Use the partnership with stakeholders to identify critical programming needs in your state, to help develop programs, and to help market your program. In Indiana, we also created a partnership of food safety trainers where Purdue Cooperative Extension staff co-teach programs with local health departments.

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• Develop an evaluation system that continually allows you to improve your programs. In Indiana, we have seen great increases in participation and interest in retail food safety training. In 2000, approximately 500 people participated in retail food manager’s certification programs (ServSafe® or SafeMarkTM) and, in 2010, this number grew to over 6-fold to more than 3,000 people. The 10-year collective passing rate is over 94% of national retail food protection mangers certification exams. Participation in the Purdue University Food Safety Day program has increased from approximately 800 people in 2000 to over 9000 people in 2010. When evaluating success of a food safety training program, there are many metrics that can be used. An increase in number of participants helps to reaffirm that there is a need and interest in retail food safety education. Successful passing rate on national food protection manager’s certification exams helps to show that a certain level of knowledge and competence has been met. In this program, we have also shown that participants indicate positive changes in food safety behavior and interest for more training opportunities. This really helps to demonstrate overall programmatic impact. We are continuing to develop better metrics that will help to clarify behavioral changes. The next step is to visually observe actual changes in food handling practices within retail food establishment settings and relate these observations to retail food safety programming. We still have a long way to go to improve food safety risks in this country, but, certainly education for retail food handlers will be a critical component. In 2007, members of the food safety task force in Indiana partnered with five land grant institutions and three science associations to form the RetailFoodservice Food Safety Consortium (RFSC). The RFSC, through networking, information sharing, and strategic planning of activities, enhances the ability of food safety professionals to work more effectively with the retail food industry. As part of this effort, a national website was created (www.retailfoodsafety.org). The website provides a centralized site for comprehensive retail food safety information for educators, trainers and learners for a wide variety of

topics in different educational formats, languages and audiences.

Acknowledgement The author of this paper would like to sincerely thank members of the Indiana Retail Food Safety Task Force (Vickie Hadley, Brenda Hagedorn, Karen Richey, Joan Younce, Linda Souchon, Dr. David McSwane, Scott Gilliam, John Livengood, and Debbie Scott) for all of their efforts to promote food safety education in the state of Indiana. Special thanks are extended to Kevin Hamstra for developing a webbased survey based instrument that was used to collect our data and for the development of the Retail Food-Service Food Safety Consortium website.

References Centers for Disease Control and Prevention (CDC). 2010. Surveillance of Foodborne Disease Outbreaks: United State, 2007. http://www.cdc.gov/ mmwr/preview/mmwrhtml/mm5931a1.htm?s_ cid=mm5931a1_w Centers for Disease Control and Prevention (CDC). 2011. CDC Estimates of Foodborne Illness in the United States. http://www.cdc.gov/ foodborneburden/2011-foodborne-estimates. html Educational Foundation of the National Resturant Association (NRA). 2011. ServSafe® Training and Certification. http://www.servsafe.com/FoodSafety/. Food and Drug Administration (FDA). 2009. FDA Food Code. Food Marketing Institute (FMI). 2011. SafeMarkTM http://fmi.org/. http://www.fda.gov/Food/FoodSafety/RetailFoodProtection/FoodCode/default.htm.

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CONFERENCE PROCEEDINGS* ConAgra Foods’ Salmonella Chester Outbreak In Marie Callender’s Cheesy Chicken and Rice Catalyzing Change: Next Generation of Food Safety J. Menke-Schaenzer1 ConAgra Foods *Arkansas Association for Food Protection (AAFP) Conference, Enhancing Food Protection from Farm to Fork, held on Sept. 28-29, 2010, Springdale, AR. 1

ABSTRACT ConAgra’s voluntary recall in June 2010 of Marie Callender’s Cheesy Chicken and Rice meal because of a possible link to a Salmonella Chester outbreak led to a cooperative investigation with several federal and state government agencies. After the investigation and following resumption of ConAgra’s shipments of the product, the Centers for Disease Control commended ConAgra for its “quick and decisive action” in removing the potentially harmful product and preventing additional infections. ConAgra has built upon the incident to advance its current programs into a “Next Generation Food Safety Plan.” Keywords: Recall, Salmonella Chester, ConAgra, Marie Callender’s, outbreaks, CDC, FDA, USDA, HACCP Agric. Food Anal. Bacteriol. 2: 43-45, 2012

ConAgra Foods is a leading branded food company located in Omaha, Nebraska. ConAgra Foods brands include Egg Beaters®, Healthy Choice®, Slim Jim®, Orville Redenbacher®, and Marie Callender’s®. Moreover, 97 percent of American households have at least one ConAgra Foods product in their pantry, refrigerator, or freezer. The Marie Callender’s® Cheesy Chicken and Rice was the 10th-best selling frozen meal nationally in 2010. This product was not “ready to eat” and had validated cooking instructions listed on the packaging. In June 2010, ConAgra Foods voluntarily recalled Marie Callender’s® Cheesy Chicken and Rice meal

due to a possible link of the product to a Salmonella Chester outbreak. On June 10, the State of Oregon and the Centers for Disease Control (CDC) notified ConAgra Foods of a potential link to a Salmonella outbreak and the Cheesy Chicken and Rice meal (among other potential food products being tracked at the time). On June 11, ConAgra Foods participated in joint calls with the CDC, Food & Drug Administration (FDA), United States Department of Agriculture (USDA) and 10 states. ConAgra Foods then held daily calls with the CDC to assist in its investigation by providing information and updates. On June 17, before any definitive link had been established to the Salmonella outbreak, ConAgra Foods decided to voluntarily recall the Cheesy

Correspondence: J. Menke-Schaenzer

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Figure 1. Distribution of illnesses linked to Marie Callender’s® Cheesy Chicken and Rice meal.

Chicken and Rice meal and shut down production and further distribution of the meal. Product samples were obtained from consumers, and, on June 18, the first sample was received that tested positive for Salmonella. After a thorough investigation of the affected plant and ingredient suppliers, ConAgra Foods resumed shipments of the product on July 21. The CDC closed the investigation on August 15. Over the course of the outbreak, there were a total of 43 illnesses in 19 states, as seen in Figure 1. Root cause analysis began with a plant investigation, which included finished-product testing, environmental swabs, and component testing. More than 1,500 finished-product tests were conducted. Two tested positive for Salmonella. All environmental swabs and component tests were negative. There were six positive results for Salmonella from 25 product sample tests received from a variety of states. Three production codes were associated with the positive results. The raw material investigation revealed common suppliers for all three implicated code dates for cheese, IQF rice, onions, and pre-cooked poultry. However, there were no common lots of raw materials. The associated product ingredient usage was reviewed along with the ingredient usage percentage. The Certificates of Analysis (COAs) for the precooked chicken were all Salmonella negative. Further investigation into the chicken supplier revealed three of the six chicken houses were common to the

positive production codes. The CDC commended ConAgra Foods in its Aug. 2 “Public Health Matters Blog” for the “quick and decisive action taken by ConAgra, as well as the successful collaboration among the many local, state, and federal public health, agriculture, and regulatory agencies involved. The immediate action probably prevented more people from being infected with Salmonella by removing the potentially harmful product from store shelves and consumers’ homes early in the outbreak.” Prior to the recall, ConAgra Foods’ food safety programs were in line with industry standards. Suppliers followed strict, contractually mandated adherence to regulatory requirements. The company conducted unannounced audits and testing. Plants followed and verified Good Manufacturing Practices. ConAgra Foods also maintained strict Hazard Analysis of Critical Control Points (HACCP) and COA verification programs. This incident caused ConAgra Foods to take yet a deeper look into advancing its current programs into a “Next Generation Food Safety Plan.” This included the development of new programs to explore non-traditional testing and process control microbiology of finished product, in-process product, and raw materials. Additionally, deeper investigations into all suppliers began by looking beyond the COAs and learning how each supplier takes steps to maintain food safety. While upholding a food safety culture was already a priority supported by ConAgra Foods’ senior management, this incident gave an even greater emphasis to the necessity of food safety at each step of production. Moreover, proactive relationships that had been established with the CDC and other regulatory agencies prior to the recall proved to be key in early notification and facilitated fast action. Throughout the process, ConAgra Foods maintained a high level of transparency with all regulatory agencies and supported thorough and rigorous testing of products and facilities. Because pathogens can occur in raw materials, the food industry must view the world through a public health lens to ensure consumers’ health and safety is

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at the forefront of its efforts. Testing is an essential verification step to help prevent potential issues early in the process, but supplier relationships, company culture and communication both within and outside the company also play critical roles in this area.

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CONFERENCE PROCEEDINGS* Food Safety For a Diverse Workforce; One Size Does Not Fit All J. A. Neal1, M. Dawson1, J. M. Madera1 1

Conrad N. Hilton College of Hotel and Restaurant Management, University of Houston, 229 C. N. Hilton Hotel and College, Houston, Texas 77204-3028, USA *Arkansas Association for Food Protection (AAFP) Conference, Enhancing Food Protection from Farm to Fork, held on Sept. 28-29, 2010, Springdale, AR.

ABSTRACT Food safety information is readily available in Spanish and to a lesser extent Chinese and other languages. While food service managers may be able to purchase comprehensive sets of food safety training and educational resources in multiple languages, they are still responsible for implementing the training programs and language barriers can be problematic. Therefore, food service managers must identify where communication barriers to food safety occur, learn communication techniques to teach proper food safety to non-English speakers and develop a delivery method that is effective. The purpose of this study was to examine the relationship between safety-communication barriers and food safety behaviors. Additionally, the perceived effectiveness of using nonverbal communication was investigated. The analyses showed significant relationships between perceived safety-communication barriers and food safety behaviors. In particular, the more safety-communication barriers participants perceived the fewer times they washed their hands (r = -0.27), checked that the food was cooked to appropriate temperatures (r = -0.21), and checked for cross contamination (r = -0.23). By identifying where key safety-communication barriers exist, food service managers may be able to use more effective non-verbal methods of communicating to non-English speaking employees and reduce the risk of foodborne illness outbreaks. Keywords: food safety; communication barriers; non-English speakers; training Agric. Food Anal. Bacteriol. 2: 46-55, 2012

Introduction Foodborne illnesses continue to be a public health problem in the United States costing the food industry billions of dollars annually. Health-related costs from acute foodborne illness in the U.S. are estimatReceived: August 31, 2011, Accepted: October 19, 2011. Released Online Advance Publication: July 1, 2011. Correspondence: Jay Neal, JNeal@Central.UH.EDU Tel: +1 -229-386-3363 Fax: +1-229-86-3239

ed to be $152 billion yearly (Scharff, 2010). CDC estimates that each year roughly 1 out of 6 Americans (or 48 million people) get sick, 128,000 are hospitalized, and 3,000 die from foodborne diseases (Scallan et al., 2011). Training and education of food handlers is critical since workers mishandling the product causes the majority of foodborne illness outbreaks reported in the food industry (WHO, 2000). One of the bigger challenges of providing this training and

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education is language barriers. Difficulties due to language barriers are common in the food industry and are perceived to be a major barrier to promoting U.S. food service standards to limited or non-English speakers (Fraser and Alani, 2009). Currently, there are approximately 311 languages (162 indigenous and 149 immigrant languages) spoken in the U. S. (Vistawide, 2009). In 2008, 15.6% (24.1 million people) of the U. S. labor force were foreign born. Hispanics comprised 49.4% of the foreign-born labor force and Asians made up 22.4% (Bureau of Labor Statistics, 2009). More specifically, the food service industry provided work for approximately 1.4 million immigrants, representing more than 10% of the food service labor force (NRA, 2006). The foodservice industry is the single largest employer of immigrants in the United States (Jackson, 2008). The term “foreign-born” may include legally-admitted immigrants, refugees, and temporary residents such as students and undocumented immigrants. Roughly 46% of foreign-born workers have limited English proficiency (Capps et al., 2003) and 26% of employees in the foodservice industry do not speak English at home, but rather another language such as Spanish, Chinese or Vietnamese (NRA, 2006). Research has previously shown that immigrant workers believe that not speaking English is a consistent disadvantage (Castro et al., 2006). Language fluency is often related to employee’s belief that they are valued by the organization. As a result, when they do not feel valued, employees experienced lower levels of job satisfaction thus, were less committed to the organization (Sanchez, 2006). Feelings of fear, anxiety, helplessness, and frustration, and a longing to return home are not uncommon to the immigrant (Au et al., 1998). Language skills are increasingly linked to an individual’s opportunity to advance in the U.S. workplace (Canziani, 2006). In a study conducted with Chinese restaurant employees, workers attributed language barriers and lack of skills and knowledge due to their low educational backgrounds as reasons for being dissatisfied (Au et al., 1998). The risk associated with eating outside the home

has been well documented (Friedman et al., 2004; Green and Selman, 2005; Jones et al., 2004; Kassenborg et al., 2004; Kassenborg 2004; Kimura et al., 2004; Soble et al., 2000) however, the food service industry is making improvements (Scallan et al., 2011). For example, between 1998 and 2008, significant improvements were made for poor personal hygiene and improper holding/time and temperature risk factors. These were reported with no significant regressions for any of the foodborne illness risk factors (Scallan et al., 2011). Much of this success can be attributed to better training. Researchers have worked hard to identify beliefs targeted to improve food service employees’ intentions for performing proper food safety behavior. Employee attitudes toward specific behaviors have been identified as a consistent predictor for employee behaviors and food safety in general (Pilling et al., 2008). Although attitudes may be an important factor in predicting behavior, the question must be asked if attitudes towards food safety differ among non-English speakers, therefore, making it more challenging for managers to communicate safe food handling procedures. Food safety classes are offered in multiple languages such as Spanish or Chinese and are necessary; however, many of these classes do not address behaviors tempered by cultural upbringing (Niode et al., 2011). Mitchell et al. (2007) reported that cultural background and upbringing, justification, and/ or motivation for the particular behavior may be effected by predisposing factors to improper food safety behavior, therefore; there may be common cultural misconceptions concerning food safety. Cho et al. (2010) stated that Latino(a) restaurant employees believe that when they follow proper food safety practices, both customers’ and managements’ satisfaction and efficacy in the kitchen may increase. They may demonstrate better food safety behavior as well. It has been suggested that this is a result of the cultural characteristics of the Latino (a) population. Santiago-Rivera (2002) noted that collectivist cultures, such as those found in Mexico and other Latin American countries have a tendency to focus on the interest of a group, a family or extended relationships rather than on individual interests or con-

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cerns. Hence, not only do food service managers need to address communication barriers, there may be cultural misconceptions concerning food safety that must also be overcome. Providing food safety education and training in multiple languages is still an important starting point. Food safety knowledge is a precursor to safe food handling practices which is vital to preventing foodborne illness (Fraser and Alani, 2009). In order to obtain knowledge, the food service employee must first understand what is being taught therefore presenting essential information in their native language is a key component to promoting proper food handling practices. Taylor (2005) reported that delivering food safety information in the language that one understands best can improve productivity, compliance, and morale. Currently, food safety information is readily available in Spanish and to a lesser extent Chinese. The most comprehensive listing of non-English materials based on U.S. standards is available at www.foodsafetyweb.info/resources/NonEnglish.php; however, this site has not been updated since 2006 (Fraser and Alani, 2009). While other material is available online, sometimes it is not clear how the material was reviewed for technical or translation accuracy. In order to help limited or non-English speaking food service workers succeed, comprehensive sets of food safety training and educational resources based on the U.S. Food and Drug Administration’s (FDA’s) Food Code are needed in multiple languages at minimal costs (Fraser and Alani, 2009). In the meantime, researchers and educators are working hard to develop food safety educational materials that focus on specific target audiences (Latinos, Chinese) and specific types of organizations (delis, ethnic food restaurants). Much of this material is based on theory-based models such as the Theory of Planned Behavior (TPB), Gradual Release of Responsibility Model (GRRM) or the Health Action Model (HAM). Nieto-Montenegro et al.. (2005) used HAM to develop food safety educational materials for Hispanic workers in the mushroom industry and reported that this model was an effective guide in developing customized food safety educational ma-

terials. Key to its success consist of 5 constructs or systems, all of which influence behavior and include: (a) knowledge system: baseline food safety knowledge; (b) normative system: worksite norms and rules; (c) motivational system: motivational elements in the company; (d) belief system: values and beliefs of the target audience: and (e) worksite environmental system: worksite physical conditions (NietoMontenegro et al., 2005). While all of the constructs are important and interdependent, the motivational system is critical to influencing behavioral intent and relies heavily on management during the implement and follow-up of a food safety program (Hennum et al., 1983). While food service managers may be able to purchase comprehensive sets of food safety training and educational resources in multiple languages, they are still responsible for implementing the training programs and language barriers can be problematic. Wilcock et al. (2011) reported that communicating concepts during training was a common barrier for non-English speaking employees or for whom English was not their first language. Language barriers may lead to ineffective management techniques in directing culturally diverse employees (Lee and Chon, 2000). For example, research shows that immigrant workers are more likely to be involved in workplace injuries than native workers, because they lack the language skills to read and understand safety rules (Azaroff et al., 2003). Also, employees with limited English report a lack of training and direction from their managers because of their limited English skills (Castro et al., 2006). One common approach to overcome language barriers that occur in the workplace is functional multilingualism, which has been described as muddling through relying on a mix of languages, pidgins and gestures to communicate by whatever means the parties have at their disposal (Hagen, 1999; Freely and Harzing, 2003). While functional multilingualism is sometimes the only communication tool managers have at their disposal, being able to speak more than one language adds an important aspect to communicative competence (Callahan, 2005). Other challenges that managers face when teaching food safety practices include working with a low-

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Table I. Correlations between perceived food safety communication behaviors and food safety practices.

Safety Communication Barriersa

Pearson Correlation

Safety HandCommunication washing Barriersa

Check No Cross Nonverbal Temperature Contamination Behaviorsb

-0.267**

-0.210*

-0.225*

-0.367**

0.006

0.032

0.024

0.000

Sig. (2-tailed) Handwashing

Check Temperature

No Cross Contamination

Nonverbal Behaviorsb

106

103

105

101

106

Pearson Correlation

-0.267**

0.060

0.228*

0.221*

Sig. (2-tailed)

0.006

0.550

0.023

0.025

103

Pearson Correlation

-0.210*

0.060

0.447**

-0.037

Sig. (2-tailed)

0.032

0.550

0.000

0.706

105

103

105

101

105

Pearson Correlation

-0.225*

0.228*

0.447**

-0.110

Sig. (2-tailed)

0.024

0.023

0.000

101

Pearson Correlation

-0.367**

0.221*

-0.037

-0.110

Sig. (2-tailed)

0.000

0.025

0.706

0.272

106

103

105

101

skilled labor force and high employee turnover rates. Based on levels of education, limited or non-English speakers may or may not be able to read in their native language, therefore, simply presenting written food safety training material in additional languages may have limited success. In addition, due to the notoriously high turnover rates of the food service industry, managers may not want to invest a lot of time, money or effort into developing food safety training programs for an individual employee because within months of training, the employee may leave (Niode, 2011). Food service managers must identify where cultural barriers to food safety occur, learn effective methods for communicating proper food safety practices to non-English speakers, and develop a delivery method that is quick and effective. Thus, the purpose of this study was to examine the relationship between safety-communication bar-

0.272

106

riers and food safety behaviors; such as the number of times participants washed their hands, checked the temperature of the food, and avoided cross contamination. In addition, the researchers examined the perceived effectiveness of using nonverbal communication and how this construct relates to perceived safety-communication barriers in a context of working in a kitchen where communication barriers exist. This study sought to answer the following research questions: 1. Is there a correlation between communication barriers and food safety behaviors? 2. What are the most frequent types non-verbal forms of communication used in a kitchen setting? 3. How effective are various types of nonverbal behaviors in regard to the performance (temporal performance, food quality, and food accuracy)?

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Πολλο χον Πεπερονι αλλ Αβρυζζεσε Ινγρεδιεντσ: • 2 Βελλ πεππερσ (1 ρεδ ανδ1 γρεεν) • 1.5 λβ. Τοματοεσ • 2 οζ ολιϖε οιλ • 5 χηιχκεν βρεαστσ • 1 μεδ ονιον • Σαλτ ανδ πεππερ το ταστε • Γαρνιση ωιτη χηοππεδ βασιλ Διρεχτιονσ: 1. Χηαρ τηε πεππερσ οϖερ α γασ φλαμε υντιλ τηε σκιν ισ βλαχκ. Ρυβ οφφ τηε βλαχκενεδ σκιν υνδερ χολδ ρυννινγ ωατερ. Ρεμοϖε ανδ δισχαρδ τηε σεεδσ ανδ χορε ανδ χυτ τηε πεππερσ ιντο μεδιυμ στριπσ. 2. Πεελ, σεεδ ανδ χηοπ τηε τοματοεσ. 3. Ηεατ τηε ολιϖε οιλ ιν α λαργε σαυτ παν. 4. Σεασον τηε χηιχκεν βρεαστσ ωιτη σαλτ ανδ πεππερ. Βροων τηεμ ιν ολιϖε οιλ. Ωηεν τηεψ αρε ωελλ βροωνεδ, ρεμοϖε ανδ σετ τηεμ ασιδε. 5. Αδδ τηε πεππερσ ανδ ονιονσ ανδ σαυτ. βριεφλψ, υντιλ ωιλτεδ. 6. Αδδ τηε τοματοεσ ανδ αδδ τηε χηιχκεν το τηε παν. Χοϖερ ανδ χοοκ ον τηε ρανγε υντιλ τηε χηιχκεν ισ δονε (165oΦ) Τηε ϖεγεταβλεσ σηουλδ γιϖε οφφ ενουγη μοιστυρε το βραισε τηε χηιχκεν, βυτ χηεχκ τηε παν φρομ τιμε το τιμε το μακε συρε ιτ ισ νοτ δρψ. 7. Ωηεν τηε χηιχκεν ισ δονε, ρεμοϖε τηεμ φρομ τηε παν ανδ κεεπ τηεμ ηοτ. Ιφ τηερε ισ α λοτ οφ λιθυιδ ιν τηε παν, ρεδυχε ιτ οϖερ ηιγη ηεατ υντιλ τηερε ισ ϕυστ ενουγη το φορμ α λιττλε σαυχε φορ τηε ϖεγεταβλεσ. 8. Αδϕυστ τηε σεασονινγ. Σερϖε τηε χηιχκεν τοππεδ ωιτη τηε ϖεγεταβλεσ.

Figure 1. Recipe in Cyrillic Alphabet.

Materials and Methods Sample One hundred and seven students (49% men and 51% women) at a four-year university majoring in hotel and restaurant management participated in the study. The participants’ average age was 22.10 (SD

= 3.4). The majority of the participants (69%) held a current part- or full-time job in the hospitality industry. Of the employed participants, 33% held a management position. Additionally, 44% of the participants reported “frequently” working with nonEnglish speaking employees. In regard to ethnicity/ race, 42% identified as Caucasian, 25% as Asian, 21% as Hispanic, 5% as African-American/Black, and 7% reported as “other.”

Experimental Design and Procedure The researchers used a behavioral manipulation of perspective-taking (Madera et al., 2011) to place the participants in the role of non-English speaking employees, which allowed the researchers to test the research questions in the context of communication barriers. In this paradigm, participants were randomly assigned into groups of 4 to 5 people and were instructed to prepare a menu entree in silence, imagining that they could not speak and or understand English. The recipes and instructions provided to the participants were in an abstract, non-English language using Cyrillic letters (Figure 1). One participant from each group was assigned the role of manager who was provided with the recipe and instructions in English. The groups completed the recipes in silence and relied only on non-verbal methods of communications during the task. The same kitchen laboratory space was used for all the groups.

Instrumentation Perceived safety-communication barriers were measured using a scale adopted from Madera et al. (2011). The scale included seven items relating to not being able to communicate safety information when working with food. Example items were, “I could not alert others (hot plates, knives, behind you),” “I could not communicate or receive information about cleanliness,” and “I could not communicate or receive information about cross-contamination.” Respondents used a 5-point scale (1) strongly disagree to (5) strongly agree. The scale had an alpha reliability of .86.

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Sanitation behaviors were measured by using definitions from the CDC’s identified risk factors for foodborne illness as well as with WHO’s factors leading to foodborne illness (CDC 2009; WHO 2007). In particular, the participants reported the number of times they washed their hands, checked the temperature of the food, and avoided cross contamination while preparing the recipes. Thus, a frequency count was used to measure these three items. Perceived nonverbal communication was measured using a scale adopted from Dawson et al. (2011). The scale included four items about the effectiveness of four nonverbal communication methods: gestures, demonstrating, pointing, and approval. Approval can be shown through a head nod, gestured approval, smile, or a “thumbs up.” These four nonverbal communication methods have been shown to be the most frequently used method when working in an environment where communication barriers exist (Dawson et al., 2011a; Dawson et al., 2011b). Respondents used a 5-point scale (1) strongly ineffective to (5) very effective. The scale had an alpha reliability of 0.77.

Results Correlations were used to examine the relationships between perceived safety-communication barriers, sanitation behaviors, and perceived nonverbal communication effectiveness. The analyses showed significant relationships between perceived safetycommunication barriers and the food safety behaviors. In particular, the more safety-communication barriers participants perceived the less times they washed their hands (r = -0.27), checked that the food was cooked to appropriate temperatures (r = -0.21), and checked that they did not cross contaminate (r = -0.23). In addition, perceived safety-communication barriers were significantly related to perceived nonverbal communication. The less effective the participants’ perceived their nonverbal communication methods were when working with others, the more safety-communication barriers they perceived (r = -0.37). Perceived nonverbal communication was

significantly related to the frequency of hand washing (r =0 .22), but not to the number of times the participants checked the temperature of the food (r = -0.04, n.s.) and avoided cross contamination (r = -0.11, n.s.). Please see Table 1. The results showed that leaders’ most frequent nonverbal behavior were gestures (46%), and pointing (36%), followed by demonstrating (9%), touching (6%), and eye contact (3%). In order to provide feedback or approval, leaders gave a head nod (56%), gestured approval (25.4%), smiled (12.6%), or a “thumbs up” (5.8%). The results for the group members’ nonverbal behavior were similar to those of the leaders. In particular, the most frequent nonverbal behavior were gestures (48%) and pointing (35%), followed by touching (7%), demonstrating (4%), and eye contact (4%). Approval was shown through a head nod (61%), gestured approval (21%), smiles (12%), or a “thumbs up” (6%).

Discussion and CONCLUSIONs Managing a food service operation successfully is difficult and working with employees who do not speak the same language can be challenging. However, by knowing where the communication barriers exist and how to compensate for these barriers, managers can successfully communicate with non-English speakers and teach proper food safety behaviors. Therefore, the first goal of this study was to identify where safety-communication barriers existed. The participants found that the most frequent communication barriers were not being able to alert others about basic safety issues, such as moving through the kitchen with hot pots or pans, or sharp knives and other utensils. According to the National Safety Council (2009), in 2004 alone, there were a total of 95,380 nonfatal occupational injuries in the hospitality industry; contact with an object or equipment as the most frequent cause. The food service industry leads the number of workplace injuries, accounting for almost 6% of the reported injury cases of the entire U. S. private industry (Bureau of Labor Statistics, 2009). The vast majority of accidents and

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injuries occurred in food preparation areas. These results can be applied directly to constructs two and five of the Health Action Model which include: normative system (worksite norms and rules) and worksite environmental system (worksite physical conditions). Professional kitchens can be very busy places with multiple opportunities for accidents. Worksite norms and rules must be communicated to employees effectively to ensure both consistencies and safety. These results may identify where safety guidelines such as pictures or other non-verbal safety practices may be incorporated and help create a safe and healthy work environment that includes a multi-lingual workforce. One possible solution foodservice managers may consider is zoning high injury risk areas within a kitchen such as the pot washing or hot food preparation areas in order to alert employees of potential accidents. Examples may include painting or marking critical areas to communicate accident prone areas. Similar approaches have been used with color coding equipment and utensils to prevent cross contamination. The physical environment itself can be altered to communicate non-verbally potential risks and therefore, possibly change employee behavior. The second most frequent issue participants’ reported related to cross-contamination and instructions to what needs to be done with food products. These results are important considering that the Center for Disease Control and Prevention (CDC) reported that there were 1270 outbreaks of foodborne disease outbreaks in the U.S. with the most cases associated with poultry, leafy vegetables, and fruits and nuts (CDC, 2009). In order to address this issue, foodservice managers may consider identifying “Critical Control Actions.” A “Critical Control Action’ can be defined as a behavior or activity that must be performed to accomplish a critical control point within a HAACP plan such as the action of taking a temperature to ensure a Critical Control Point has been met. Based on HACCP principles, “Critical Control Actions” can be identified within Critical Control Points of a HACCP system and allow managers to identify what key actions must be taken by employees in order to prevent foodborne illness

outbreaks. Again, signs, pictures or graphs using images to communicate non-verbally the necessary actions could be placed a key locations such as the hand washing sinks, food preparation and dish washing areas. The participants found that a combination of gestures and demonstrating the desired behavior were the most effective non-verbal communication methods. This outcome is consistent with the common non-verbal communication methods, whereby gestures that demonstrate actions are most effective in teaching such actions. Gestures are used in all cultures, tend to be tied to speech processes, and are usually automatic (Lozano and Tversky, 2006). Food service managers will be expected to lead and train employees who may possess limited or have no grasp of the language, therefore, including gestures while training may be an effective form of communication (Raybould and Wilkins, 2005). Despite these implications, the current study also has limitations and directions for future research. First, the students were provided instructions to not speak and given a recipe in a non-English, abstract language. This exercise only simulates a non-English speaker’s environment. Therefore, it might not be the same as the occurrences that immigrants or someone who speaks English as a second language experience. Future research might examine these issues with a sample of non-English speakers. Further studies might also examine the methods and techniques that managers use to communicate with nonEnglish speaking employees. Not only do food service managers need to address communication barriers, there may be cultural misconceptions concerning food safety that must also be overcome and should be addressed in future studies. In addition, studies investigating the effectiveness of “zoning” for food safety and using Critical Control Actions should be conducted. In the current study, gestures, pointing, and demonstrating were the most frequent methods that student managers used with their employees. The continual push for international expansion in the hospitality industry in combination with new and different types of workers in the U.S. workforce is cre-

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ating a multicultural urgency for managers (Testa, 2007). Given the increasing number of immigrants in the food service industry (NRA, 2006); this research primarily takes a United States focus rather than a global perceptive. However, in cities around the world, but particularly in Western Europe, Australia, and the Persian Gulf, immigrants play a fundamental role in the labor force (Benton-Short and Price, 2007). Further research would be advantageous in order to establish if these results could be duplicated in other countries among other languages and cultural norms. Given the increasing number of immigrants and multiculturalism in the food service industry, it is imperative to be proactive rather than reactive to the demographic changes.

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tion certification training in Moorhead, Minnesota. Dairy and Food Sanitation 3: 208-214. Jackson, S. 2008. Making growth make sense for retail and franchise businesses. J. Bus. Strategy 29:48-50. Jones, T., B. Imhoff, M. Samuel, P. Mshar, K. McCombs, M. Hawkins, V. Dennen, M. Cambridge, and S. Olsen, for the Emerging Infections Program Food-Net Working Group. 2004. Limitations to successful investigation and reporting of foodborne outbreaks: An analysis of foodborne disease outbreaks in FoodNet catchment areas, 1998-99. Clin. Infect. Dis. 38:S297-S302. Kassenborg, H., C. Hedberg, M. Hoekstra, M. Evans, A. Chin, R. Marcus, D. Vugia, K. Smith, S. Ahuja, L. Slutsker, P. Griffin, for the Emerging Infections Program Food-Net Working Group. 2004. Farm visits and undercooked hamburgers as major risk factors for sporadic Escherchia coli O157:H7 infection: Data from a case-control study in 5 foodNet sites. Clin. Infect. Dis. 38:S271-S278. Kassenborg, H., K. Smith, D. Vugia, T. Rabatsky-Her, M. Bates, M. Carter, N. Dumas, M. Cassidy, N. Marano, R. Tauxe, and F. Angula, for the Emerging Infections Program Food-Net Working Group. 2004. Fluoroquinolone-resistant Campylobacter infections: Eating poultry outside the home and foreign travel are risk factors. Clin. Infect. Dis. 38: S279-S284. Kimura, A. V. Reddy, R. Marcus, P. Cieslak, J. MohleBoetani, H. Kassenborg, S. Segler, F. Hardnett, T. Barrett, and D. Swerdlow, for the Emerging Infections Program Food-Net Working Group. 2004. Chicken consumption is a newly identified risk factor for sporadic Salmonella Enterica serotype Enteritidis infections in the United States, A casecontrol study in FoodNet sites. Clin. Infect. Dis. 38: S244-S252. Lee, C., and K. S. Chon. 2000. An investigation of multicultural training practices in the restaurant industry: the training cycle approach. Int. Journal Contemporary Hospitality Manag. 12:126-134. Lozano, S., B. Tversky. 2006. “Communicative gestures facilitate problem solving for both communicators and recipients,” J. Mem. Lang., Vol. 55, p.

47-63. Madera, J. M., J. A. Neal & M. Dawson. 2011. Strategies for diversity training: Focusing on empathy in the workplace. J. Hospitality Tourism Res. Forthcoming. Mitchell, R. E., A. M. Fraser, and L. B. Bearon. 2007. Preventing foodborne illness in food service establishments: Broadening the framework for intervention and research on safe food handling behaviors. Int. J. Environ. Health Res. 17:9-24. National Restaurant Association 2005. National Restaurant Association highlights new guide for immigrants. [Press Release]. Available at: http://www. restaurant.org/pressroom/pressrelease/print/index.cfm?ID=1111. Accessed February 13, 2011. National Restaurant Association 2006. Restaurant industry facts. Retrieved from http://www.restaurant. org/research/ind_glance.cfm. National Safety Council. 2009. Reports on Injuries in America: highlights from injury facts, 2009 edition. Available at: http://www.nsc.org/news_resources/ injury_and_death_statistics/Pages/HighlightsFromInjuryFacts.aspx. Accedssed February 21, 2011. Niode, O., C. Bruhn, and A. H. Simmone. 2011. Insight into Asian and Hispanic restaurant manager needs for safe food handling. Food Control, 22:3442. Nieto-Montenegro, S., J. L. Brown, and L. F. LaBorde. 2005. Using the Health Action Model to plan food safety educational materials for Hispanic workers in the mushroom industry. Food Control 17:757767. Pilling, V. K., L. A. Brannon, C. W. Shanklin, A. D. Howells and K. R. Roberts. 2008. Indentifying specific beliefs to target to improve restaurant employee’s intentions for performing three important food safety behaviors. J. Am. Diet. Assoc. 108:991-997. Raybould, M. and Wilkins, H. C. 2005. Over qualifies and under experiences: turning graduates into hospitality managers. Int. J. Contemporary Hospitality Manag. 17: 203-216. Sanchez, R. 2006. The role of language fluency selfefficacy in organizational commitment and perceived organizational support. J. Foodservice

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Business Res. 9:49 – 65. Santiago-Rivera, A., P. Arredondo, and M. CooperGallardo. 2002. Counseling Latinos and la famila: a practical guide. Thousand Oaks: Sage. Scallan, E., R. M. Hoekstra, F. J. Angulo, R. V. Tauxe, M. A. Widdowson, S. L. Roy, and P. M. Griffin. 2010. Foodborne illness acquired in the United States – Major pathogens. Available at: http://www.cdc. gov/eid/content/17/1/pdfs/09-1101p1.pdf Accessed on: January 25, 2011. Scharff, R. L. 2010. Health-related costs from foodborne illness in the United States. Produce Safety Project at Georgetown University, Pew Charitable Trusts, Washington D.C. Soble, J., A. Hirshfeld, K. McTigue, C. Burnett, S. Alterkruse, F. Brenner, G. Malcom, S. Mottice, C. Nichols, and D. Swerdlow. 2000. The pandemic of Salmonella Enteritidis phage type 4 reaches Utah: a complex investigationconfirms the need for counting rigorous control measures. Epidemiol. Infect. 125:1-8. Taylor, K. 2005. Clean Language. HRMAGIZINE, 50: 66-70. Testa, M. 2007. A deeper look at national culture and leadership in the hospitality industry. Int. J. Hospitality Manag. 26: 268-284. United States Food and Drug Administration. 2004. FDA report on the occurance of foodborne illness risk factors in selected institutional food service, restaurant, and retail food store facility types. Available at: http://www.cfsan.fda.gov/~dms/retrsk2. html. Accessed February 21, 2011. Vistawide. 2009. Top 20 countries by number of languages. Available at: http://www.vistawide.com/ languages/20_countries_most_languages.htm. Accessed February 13, 2011. Wilcock, A., B. Ball, and A. Fajumo. 2011. Effective implementation of food safety initiatives: managers’, food safety coordinators’ and production workers’ perspectives. Food Control 22:27-33. World Health Organization. 2000. Foodborne Disease: A focus for health education. Genev: World Health Organization. World Health Organization. 2007. Basic food safety for health workers. Available at: http://www.who.

int/foodsafety/publications/capacity/healthworkers/en/index.html. Accessed February 21, 2011.

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CONFERENCE PROCEEDINGS*- REVIEW Physical and Chemical Control of Salmonella in Ready-To-Eat Products O. K. Koo1, S. A. Sirsat2, P. G. Crandall1 and S. C. Ricke1 Center for Food Safety, Dept. of Food Science, University of Arkansas, Fayetteville, AR 72704 Conrad N. Hilton College of Hotel and Restaurant Management, University of Houston, Houston, TX 77204-3028 1

*Arkansas Association for Food Protection (AAFP) Conference, Enhancing Food Protection from Farm to Fork, held on Sept. 28-29, 2010, Springdale, AR.

ABSTRACT The focus on post-processing contamination of foodborne pathogens in ready-to-eat (RTE) products has been mostly associated with outbreaks by Listeria monocytogenes. However, recently USDA-FSIS announced a guideline for small plants on RTE meat to control pathogens including L. monocytogenes as well as Salmonella due to an increase in outbreaks. Salmonella causes the second highest illness among foodborne pathogens and the growth of this pathogen needs to be inhibited since RTE products are minimally cooked. For physical control methods, heating is the most common method employed but irradiation has also been actively studied for RTE products. Organic acids are a common method for chemical control of Salmonella. Essential oils are recommended as a natural antimicrobial agent and they are effective against foodborne pathogens. However, they can change the flavor and texture of the food product. Multiple hurdle technology with the combination of physical, chemical or biological agents can be more effective if combinations can be optimized for maximum effect. Hurdle technology can also reduce the chances of microbial resistance against antimicrobial agents. Microarray analysis of gene expression profile by antimicrobial treatments may help to identify the most applicable treatments to target pathogens and maximize the effectiveness of hurdle technology. Application of appropriate control methods to RTE products is required for effective control of target pathogens without affecting organoleptic properties. Keywords: ready-to-eat, Salmonella spp, antimicrobial, hurdle technology Agric. Food Anal. Bacteriol. 2: 56-68, 2012

Foodborne pathogens Contamination of pathogen in food products has been a constant concern for humans due to severe health threats and economical loss. Annually, 9.4 million illnesses are caused by foodborne pathoReleased Online Advance Publication: July 1, 2011. Correspondence: Steven C. Ricke, sricke@uark.edu Tel: +1 -479-575-4678 Fax: +1-479-575-6936

gens with 55,961 hospitalizations and 1,351 deaths. Among the number of illness, 5.5 million (58%) people are infected by norovirus and the second highest is 1.0 million illness (11%) by nontyphoidal Salmonella spp (Scallan et al., 2011). Nontyphoidal Salmonella spp, norovirus, Campylobacter spp and T. gondii caused the most hospitalizations; and nontyphoidal Salmonella spp, T. gondii, L. monocytogenes and norovirus caused the most deaths (Scallan et al.,

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2011). Overall cost for foodborne illness in the US was estimated to be 152 billion dollars annually, out of which 39 billion dollars was associated with fresh, canned and processed produce (Moran, 2010).

Salmonella pathogenesis Salmonella is Gram-negative, non-spore forming bacillus, and facultative anaerobe that can grow at 5 to 45°C and form long filamentous chains at extreme conditions, such as 4 to 8°C or 44°C and pH 4.4 or 9.4 (Bhunia, 2008). Poultry is a major source of contamination particularly in high-density farms where transfer of pathogens can occur rapidly between birds. Moreover, Salmonella colonizes the intestine of the bird and can cross-contaminate the carcass during slaughter (Bryan and Doyle, 1995; Park et al. 2008). Salmonellosis is an animal origin foodborne disease including poultry, meat, milk and eggs; however more recent Salmonella outbreaks have also involved in other foods such as fruits, vegetables, and ready to eat (RTE) products. These outbreaks are mostly due to nontyphoidal Salmonella and the symptoms are self-limiting and subside within 3 to 4 days for healthy individuals. However, the symptoms can be severe and potentially fatal in young children and the elderly (Pegues and Miller, 2010). Salmonella can cause systemic disease by invading intestinal cells, and subsequently be transported to liver, spleen and mesenteric lymph nodes. The pathogen further causes neutrophil infiltration, tissue injury, fluid accumulation and diarrhea (Bhunia, 2008). A septic shock can develop as well. Infectious doses can be vary from 1 to 109 CFU/g. A human subject based study demonstrated on infectious dose with at least 105 cells, however outbreaks have been associated with as low as 10 cells (Todd et al., 2008).

Ready to eat products Ready to eat (RTE) food products have been increasingly popular in recent years since they involve very little preparation time and the consumer does not require extensive cooking skills. RTE products include seafood, meat and poultry, dairy products,

confectionaries, fruits and vegetables and RTE meal segment. USDA-FSIS defined the RTE meat and poultry product as “a product that is in a form that is edible without additional preparation to achieve food safety and can include frozen meat and poultry products” (9 CFR part 430) (USDA-FSIS, 1999). This meat product as described by USDA-FSIS represents as popular and easily consumed component of the human diet. However, RTE products can be a foodsafety concern, since consumers eat the products without further cooking. Without any proper process to eliminate foodborne pathogens, the pathogens in the contaminated food product will be able to survive and grow during storage. Contamination can occur during packaging or further processing after cooking the product at the manufacturing facility, retail store or at the domestic environment. RTE meats have often been implicated with L. monocytogenes contamination, a foodborne pathogen that can survive under extreme conditions such as low temperature and high sodium concentration. L. monocytogenes causes severe disease with high mortality rate and is particularly deadly to the immunocompromised and pregnant women by causing spontaneous abortion (Lecuit, 2007). There have been several outbreaks due to listeriosis; delicatessen turkey in 2000 and 2002 for 30 and 54 cases, hot dogs in 1998 to 1999 for 108 cases in multistate in the US, 279 cases in France in 1992 by pork tongue in jelly, and 366 cases in 1987 to 1989 by Paté in the UK (Swaminathan and Gerner-Smidt, 2007). Recently, Salmonella has also been implicated in contamination in RTE products. For instance, salami contaminated with Salmonella Montevideo resulted in 272 cases in 44 states during 2009 to 2010 (CDC, 2010). The origin of contamination was found to be the dried black pepper spice in the salami. Further investigation revealed that the contamination occurred after the salami underwent lethality steps, the raw ingredients (i.e. in this case the black pepper spice) were added to the salami (CDC, 2010). The Risk Ranger program assessed high on Salmonella risk in all food categories in pork and poultry meat products, raw, partially cooked and processed meat (Matargas et al., 2008). Salmonella was shown to have a high-risk

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score for both high and low risk population, while L. monocytogenes exhibited a high-risk score mostly for high-risk population such as immuno-compromised individuals (Matargas et al., 2008). Recently, USDA-FSIS released updated information on the Salmonella compliance guide for small plants on RTE meat products (USDA-FSIS, 2011). USDA-FSIS tests for Salmonella positive RTE products using two test programs; the random testing program and the risk-based testing program. Half of all positive products were found to be from headcheese, pork barbecue, and sausage products. The source of contamination in pork barbeque could be either from the meat or the sauce which raw ingredients were mixed with. Even though the incidence of Salmonella contamination is lower than L. monocytogenes, Salmonella contamination can be indicative of not only under-processing but also serious deficiencies in sanitary practices. For the production of RTE meat products, USDA-FSIS requires Salmonella lethality performance standards to be a 6.5 log reduction for roasted, cooked and corned beef products (9 CFR 318.17) and a 7 log reduction for fully cooked poultry products (9 CFR 381.150) (USDAFSIS, 1999). For other types of RTE meat products such as cooked meat patties, dried, fermented sausages, and salt-cured products, FSIS recommends at least a 5 log reduction of Salmonella (USDA-FSIS, 2011). Other types of RTE products such as fruits and vegetables as well as foods with low water content including nuts and cereals are receiving more attention due to the recent outbreaks. For example, celery was contaminated with L. monocytogenes causing 7 illness and 5 deaths in 2010 (Outbreak database, 2010) and bagged spinach was contaminated with E. coli O157:H7 causing 238 cases and 5 deaths in 2006 (CDC, 2006). In 2008, jalapeno and serrano pepper imported from Mexico caused approximately 1400-reported illness due to Salmonella. Specifically the peppers were contaminated with S. Saintpaul (Klontz et al., 2010). Tomato related Salmonella Newport outbreaks in 2002 (510 cases) in 26 states and 2005 (72 cases) in 16 states were caused by persistence of the pathogen in tomato fields (Greene et

al., 2008). S. Wandsworth was found in commercial RTE vegetable-coated snack food with 69 patients from 23 states and 93% were aged 10 months to 3 years (Sotir et al., 2009). A more detailed discussion on Salmonella contamination in fresh produce can be found in a comprehensive review by Hanning et al. (2009). Other types of RTE products such as peanut butter caused illness in 628 persons in 47 states (during 2006-2007) due to S. Tennessee contamination (CDC, 2007). Salmonellosis was reported in 41 states (401 cases) due to the presence of Salmonella in frozen potpies and failure to kill the pathogen during cooking (CDC, 2008). A savory snack imported from Israel in 1994 to 1995 was implicated in a S. agona outbreak affected young children in the US and UK (Killalea et al., 1996). Tainted German chocolates resulted in 439 cases due to S. Oranienburg contamination over several European countries mostly affecting young children (Werber et al., 2005). Multi ingredient RTE foods with a high fat content such as cheese, chocolate, ice cream and egg-based foods are more likely to be a vector for foodborne pathogens since the fats may protect the pathogen that Traverse the gastrointestinal tract (Todd et al., 2008). These Salmonella related outbreaks demonstrate that RTE products should not be considered safe from a food safety standpoint and require more efficient and targeted control to minimize pathogen contamination. This environmentally persistent pathogen is highly morbid and can cause huge economic losses worldwide. Several physical and chemical treatments may be employed to combat this pathogen in RTE foods and are discussed in the following sections.

Physical control on RTE Thermal treatments Physical methods include exposure to heat, cold, and packaging methods. Temperature control is one of the more conventional approaches for limiting the growth of microorganisms in a food product. Under refrigerated condition, the growth rate of the spoilage and pathogenic bacteria is reduced. However,

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some bacteria such as L. monocytogenes and Yersinia enterocolitica can survive at 1°C. In these cases, shelf life and sell-by dates play an important role (Herbert et al. 2000). Heat has been used in the form of pasteurization at various times and temperatures to inactivate certain microorganisms. Thermal inactivation of target bacteria varies based on strain, food product, and environmental factors (Doyle and Beuchat, 2007). Sterilization techniques are employed to inactivate bacterial spores. Heat is considered one of the standard commercial methods and is one of the most efficient methods for inactivating microorganisms in foods (Gould, 2000). Trials performed using hot water on poultry carcass have been shown to reduce Salmonella numbers substantially (Morrison et al. 1985). The use of hot water as a hurdle is based on the principle of increasing the surface temperature of the carcass. For instance, dipping meat samples in 95°C hot water for 3 s increased the surface temperature of meat to 82°C (Ellebracht et al. 1999). Hot water at various temperatures has been used to study log reductions of pathogenic bacteria on meat surfaces. Immersion at 70°C for 20 s resulted in less than 1 log cycle reduction in the total microflora with about 2 log cycles reduction in numbers of Enterobacteriaceae. Water used at 74°C reduced E. coli O157:H7 by 2.6 log colony forming unit (CFU) (Dorsa et al., 1997), whereas water at 95°C reduced E. coli O157:H7 by 3.7 log CFU (Castillo et al., 1998). Heat treatment of RTE meat product may be more challenging to inactivate bacteria. This is because the product has already gone through a cooking process, which promotes resistance to the survived pathogens by food ingredients that protect the bacteria from heat treatment. Osaili and others (2007) performed thermal inactivation experiments (at 55 to 70ºC) on E. coli O157:H7, Salmonella, and L. monocytogenes in breaded pork patties. The study showed that salts added to the product enabled water molecules to bind and caused poor heat penetration for bacteria to survive in the product. In addition, the breading ingredients, which consist mostly of carbohydrates and coat the pork patties, also increased the chances for bacteria to be thermal resistant. Fat content of the product did not have any effect on

the thermal resistance for this study. D-values at 55 to 70ºC were 69.48 to 0.29 min and the z-values were 6.2ºC for pork patties. In order to achieve a 7 log reduction of E. coli O157:H7, Salmonella, and L. monocytogenes, the heat treatment time at 70ºC must be 0.56 min or higher, 2.03 min or higher, and 3.01 min or higher, respectively (Osaili et al., 2007). Thermal treatment in chicken-fried beef patties evaluated the D-values at 55 to 70ºC to be 67.68 to 0.22 min and z-value to be 6.0ºC for Salmonella. The process lethality to achieve a 6.5 log reduction at a reference temperature of 70ºC for E. coli O157:H7, Salmonella, and L. monocytogenes was 0.26 min or higher, 1.43 min or higher, and 2.02 min or higher, respectively (Osaili et al., 2006). These two studies demonstrate that an appropriate heat treatment is necessary depending on the food ingredients to kill target bacteria. Thermal resistance can also be different between whole-muscle and ground meat. A Salmonella cocktail showed stronger resistance in whole-muscle with D-value of 2.7 min than ground meat with a D-value of 1.2 min when treated at 60ºC (Mogollon et al., 2009). This study revealed that increasing fat content increased the heat resistant of Salmonella. Also, segregated fat tissue in the whole-muscle was able to protect Salmonella from the heat. In the ground beef samples, thermal protection may have been lost by the homogenous distribution of fat as well as increased osmotic potential in muscle cells members even though the moisture content would be considered the same as the whole-muscle. Thermal resistance can increase significantly by lower water activity of meat (Mogollon et al., 2009).

Nonthermal treatments Relatively newer physical methods are the use of high hydrostatic pressure (HPP), ultrasonication, electroporation, high intensity light, and irradiation and these methods have been employed to inactivate microorganisms mostly at ambient temperatures. The advantage of using a nonthermal process is that it preserves the flavor, color and nutrient value of the food products. HPP and high voltage electric

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discharges are routinely used to inactivate bacteria, yeast, and molds in foods. This method has been used for jams, juices, avocado dip, and salad dressings and other RTE products. The use of HPP for poultry can be combined with other treatments, and hence prevent the growth of pathogenic bacteria and increase the shelf life of the product (Raso and Barbosa-Canovas 2003). A combination of pressure at 20 MPa with carbon dioxide reduced Salmonella by 6 log cycles while E. coli was reduced 3 log cycles in orange juice and apple cider (Balaban et al., 2001). When used at high intensities, ultrasonication technology has proven to be able to inactivate vegetative bacteria and heat-resistant spores. High intensity light such as UV radiation has been used to effectively sterilize packaging materials used for foods. UV radiation induces the formation of thymine dimers and enables polymerase to replicate new DNA strands (Rastogi et al., 2010). Kuo et al (1997) contaminated the surface of shell eggs with S. Typhimurium, treated with UV radiation (620 μW/ cm2) and the result indicated a 3 log reduction after 1 min. In addition, the UV radiation for 15 min was able to significantly reduce mold and yeast population (Kuo et al., 1997). Irradiation has been approved for variety of foods to reduce pathogens and to extend the shelf life. Foods that have been examined include; wheat flour, white potatoes, fruits and vegetables, herbs and spices, fresh meat, pork and poultry and the dose range is from 0.05 to 0.15 kGy for potatoes to 4.5 kGy for fresh meat (Tauxe, 2001). It was reported that low doses of radiation could kill 99.9% of Salmonella in poultry and E. coli O157:H7 in ground beef (Olson, 1998). The WHO stated that no toxins or other hazards were associated with high doses of irradiation when used to decontaminate food surfaces. However, the quality of the food has been a concern due to off-odors of meat with high fat content, texture change of egg white and grapefruit. There have been limited studies on the nonthermal processing to inactivate Salmonella in RTE products and most of these studies were focused on irradiation. Studies in RTE products such as carrot, cucumber, sprouts and pineapple have demonstrated that 2

kGy of radiation worked effectively to reduce Salmonella and did not have any adverse effects on texture, nutritional, or organoleptic properties of the produce (Dhokane et al., 2006; Saroj et al., 2006). Gamma radiation processing uses radioactive materials such as cobalt-60 and cesium-137. This process was used for S. Typhimurium in RTE pineapples with 2-kGy dose to reduce 5 log CFU/g of Salmonella. No growth was detected for 12 days at 4 and 10ºC (Shashidhar et al., 2007). In sprouts, D-values of S. Typhimurium ranged from 0.192 to 0.208 kGy and with 2 kGy demonstrated complete elimination of 4 log CFU/g of S. Typhimurium (Saroj et al., 2006). Electron beam irradiation can only penetrate limited depth without any radioactivity involved and hence is mostly used for thin layers of food products. Cabeza and others (2009) tested E-beam irradiation in vacuum-packed RTE dry fermented sausages to inactivate S. Enteritidis and S. Typhimurium without any sensory change. At 1 kGy, the odor and taste did not exhibit detectable differences when compared with untreated sausages, however off-odors and off-taste increased significantly at 2 and 3 kGy. Meanwhile, color change occurred especially on the redness, which was reduced significantly due to the production of heme-pigment with carbon monoxide ligand formation, and the lightness increased while yellowness was not affected. Also the off-color by irradiation could increase the concern on using irradiation on RTE meat products (Cabeza et al., 2009). X-ray treatment, which is an alternative to gamma rays and penetrates foods in greater depth than E-beam irradiation, was used on S. enterica, E. coli O157:H7, Shigella flexneri and Vibrio parahaemolyticus in frozen RTE shrimp. The D-values for E. coli O157:H7, S. enterica, Sh. flexneri and V. parahaemolyticus were 1.1, 1.3, 1.2 and 1.2 kGy, respectively. In order to reduce 5 log CFU, the shrimp samples had to be treated with 2.0, 3.0, 2.0, and 2.0 kGy for E. coli O157:H7, S. enterica, Sh. flexneri and V. parahaemolyticus, respectively. Overall results demonstrated that S. enterica had stronger resistance to X-ray treatment than other pathogens (Mahmoud, 2009).

Chemical control on RTE Chemical methods include use of organic acids,

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salts, chlorine, spices, or oils. Organic acids, which are generally recognized as safe (GRAS), are the most common method to control the growth of microorganisms in foods. In the meat industry, chemicals rinses using organic acids are employed to rinse animal carcasses. Acetic acid, lactic acids, and citric acids at concentrations of 1.5 to 2.5% are applied as sprays for carcass decontamination (USDA-FSIS, 1996). These acids reduce the pH of the food and hence lower the internal pH of bacteria to control the growth of microorganisms. At a low pH environment, the membrane of the bacteria is saturated with hydrogen ions, which alter the permeability of the cell or reduce the proton motive force, and this eventually affects the ability of bacteria to reproduce (Banwart, 1989; Ricke, 2003). Organic acids are the most effective when applied over the carcass shortly after hide removal (Huffman, 2002). Organic acids have been used for low pH sauces, mayonnaises, salads dressings, and fruit juices. Weak acids and esters such as sorbate, benzoate, and propionate are used to preserve pickles, soft drinks, breads, cakes, and grains. Nitrite is used routinely to preserve cured meats (and Gould, 2003). Lactic acid is most effective when applied at higher temperatures and a concentration of 2 to 4%. Studies have been conducted using a 4% L-lactic acid solution at 55°C on chilled beef carcass in order to reduce bacterial contamination on meat surfaces. E. coli O157:H7 and S. Typhimurium exhibited 2.0 to 2.4 log cycles and 1.6 to 1.9 log cycles reduction after postchill acid treatment (Castillo et al., 2001). Min and Yoon treated potassium lactate (PL) and sodium diacetate (SDA) to reduce S. Typhimurium and Staphylococcus aureus and evaluated the shelf life in RTE pork. Combinations of PL and SDA (1.46% PL and 0.10% SDA and 2.18% PL and 0.16% SDA) were able to delay the growth of pathogens by causing a significant increase in lag time and a significant decrease in growth rate at 10, 17, 24 and 30ºC. This study showed the potential to store RTE pork at room temperature (Min and Yoon, 2010). However, there are growing concerns in the food industry about increasing number of acid-resistant bacteria due to use of organic acids as well as the disposal of the wastewater for environmental

reasons (Dickens et al., 1994; Dickens and Whittemore, 1994; Kwon and Ricke, 1998). Chlorine is another compound, which is routinely used as an antimicrobial. The most effective form of chlorine is hypochlorous acid, which can penetrate bacterial cell wall and react with key respiratory enzymes to prevent normal functioning of the cell (Lillard, 1980). Yang and others (1998) studied the effect of four different antimicrobial treatments on poultry carcass after inoculating the carcass with Salmonella. They used 10% trisodium phosphate, 2% lactic acid, 0.5% cetylpyridinium chloride (CPC), and 5% sodium bisulfate treatments at 35°C and a pressure of 413 kPa for 17 s. They found that 0.5% CPC was the most effective treatment for reducing Salmonella on the carcasses (Yang et al., 1998). CPC is a quaternary ammonium compound that has been shown to reduce bacterial counts on beef carcasses by up to 6 log CFU (Cutter et al., 2000). On fresh-cut vegetables such as broccoli, cauliflower and radishes, 0.5% CPC treatments significantly reduced L. monocytogenes, S. Typhimurium and E. coli O157:H7 by 3.7, 3.15 and 1.56 log CFU/g, respectively (Wang et al., 2001). The effects of chlorine have only been evaluated on RTE vegetables. Trisodium phosphate (TSP) has an extremely high pH of 10 to 13. This is detrimental to the pathogen as it is not able to carry out its normal cellular functions at this pH. Scientists conducted a study to check the effect of 10% TSP on S. Typhimurium attached to chicken skin (Kim et al. 1994). The results demonstrated that TSP was successful in reducing 2 log CFU/cm2 Salmonella. It has been suggested that TSP is effective in reducing Salmonella on chicken since it affects the binding kinetics of the bacteria on the carcass (Kim et al., 1994). Plant essential oils (EO) have been a growing interest as natural and safe preservatives with a broad spectrum of antimicrobial activity. EO generally works more effectively against Gram-positive than Gram-negative bacteria. However, Guiterez and others (2008) showed that EO in RTE vegetables was effective against Salmonella. Among a variety of EOs, marjoram and basil showed some activity against Gram-negative organisms. EOs have hydroxyl groups and allylic side chains, which may

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increase the antimicrobial effect on Salmonella contaminated iceberg lettuce and carrots. Oregano and thyme also showed the strongest antimicrobial activity due to the high phenolic compounds, however these compounds exhibited strong flavor (Gutierrez et al., 2008). Another study revealed reduction on spoilage bacteria, Salmonella, E. coli O157:H7 and L. monocytogenes in RTE fruit salads using pure citral and citron essential oil (Belletti et al., 2008). Minimally processed fruits and vegetables are required protection during storage and especially low-acid fruits can be more of a concern since they can allow the growth of pathogen easily. L. monocytogenes was reduced by 5 log CFU/g during 9 days of storage at 9ºC, S. Enteritidis E4 was reduced by 2.5 log CFU/g and E. coli O157:H7 exhibited a 1.2 log CFU/g reduction (Belletti et al., 2008). In general, EOs have an organoleptic impact on food products. However, citron did not cause undesirable change on color and damage to the fruit tissues but a demonstrated negative effect on taste. Interestingly, different EO extraction fractions from the same origin can target different pathogens. In orange oil, orange terpenes, d-limonene and terpenes from orange essence showed inhibition against 11 different Salmonella serotypes by a disk diffusion assay (O’Bryan et al., 2008). Limonene also exhibited inhibitory effects against E. coli O157:H7 (Nannapaneni et al., 2008) while cold pressed terpeneless Valencia orange oil was effective against E. coli O157:H7 and L. monocytogenes but not against Salmonella (Friedly et al., 2009). Studies on EO indicates that further investigation is required to find a suitable EO at an appropriate concentration against Salmonella that will not negatively impact the organoleptic properties of the product. Chemical antimicrobial methods are often combined with other control methods including biological agents such as bacteriocins. Biological methods may be classified as natural antimicrobial agents and a detailed review has been provided by Sirsat and others (2009). A natural aromatic organic compound, r-cymene was added to RTE pork sausage to control the growth of S. Typhi. This compound is a constituent of EO from oregano and thyme and

it was combined with nisin to achieve a synergistic effect on target pathogen. There were no antimicrobial effects by individual compound, however with a minimal concentration of 0.3 ppm of nisin and 2.5 ppm of r-cymene, it was able to eliminate the pathogens at 4°C (Rattanachaikunsopon and Phumkhachorn, 2010). Nisin is a bacteriocin that is mostly effective against Gram-positive bacteria. However when combined with a chelating agent such as ethylenediamine tetraacetic acid (EDTA), it can increase the antimicrobial efficiency against Gram-negative bacteria. Synergistic effects of whey protein isolate coating incorporated with grape seed extract (GSE), nisin, malic acid (MA), and EDTA in turkey frankfurter was studied for their potential to inhibit L. monocytogenes, E. coli O157:H7, S. Typhimurium (Gadang et al., 2008). The results demonstrated a 1 log reduction of S. Typhimurium after 28 days at 4°C when a combination of nisin, GSE and MA was used. However, MA alone showed a 3.3 log reduction of S. Typhimurium. The combination showed an additive rather than synergistic effect on Salmonella. The treatments were more effective against L. monocytogenes and showed a 4.8 log reduction when the frankfurters were stored for 28 days at 4°C. In order to kill or inhibit the growth of Salmonella with acids, the disruption of outer membrane is prerequisite and MA has low molecular weight compared to nisin and GSE (Alakomi et al., 2000). Therefore MA was more effective alone than in combination of all compounds (Gadang et al., 2008). Other studies added lysozyme and nisin to calcium arginate coated RTE smoked salmon, which resulted in a 2.7 log CFU/g reduction of L. monocytogenes. Nisin alone was not effective against S. Anatum, however when combined with lysozyme and nisin with calcium alginate coating showed 2.25 log CFU/g reduction after 35 days at 4ºC (Datta et al., 2008).

Multiple hurdle technology In food safety, multiple hurdle technology is an important approach to consider. Sequential sublethal stress treatments cause the target microorganism to

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face the challenge of a hostile environment leading to metabolic exhaustion and death. Hurdle technology can target a single function of a microbial cell such as cell membrane, DNA, pH, and water activity for additive effects or target multiple elements of the cells, which can cause synergistic effects by disturbing homeostasis of the cell in several aspects. With additive effects, the cells could lose the ability to recover and the damage becomes irreversible (Leistner, 2000). This approach can be beneficial for the food product since the dosage of antimicrobial agent or treatment may require less than a single treatment. The treatment can be a combination of three different methods; physical, chemical or biological method. Examples of the combination of chemical and biological methods are indicated in the earlier section. Irradiation can be combined with other chemical methods to enhance the reduction of target pathogens. For instance, without SDA and PL treatment, L. monocytogenes exhibited radiation resistance and it was able to grow during storage under refrigerated condition. In order to reduce 1 log of L. monocytogenes, 0.56 kGy of irradiation without SDA and PL was required in bologna. However, the combination of SDA 0.07% and PL 1% increased the sensitivity of pathogen to irradiation to 0.46 kGy for 1 log reduction and 3 kGy with SDA 0.07% and PL 1% prevented the growth of radiation-damaged pathogens during storage up to 8 weeks at 9°C (Sommers et al., 2003). Milillo and others investigated the combinational effect of thermal and acidified organic acid treatment on S. Typhimurium (Milillo and Ricke, 2010; Milillo et al., 2011). Sodium propionate 2.5% at pH 4 was able to exhibit a 4 log reduction of S. Typhimurium at 55 and 60°C within 1 min. The synergistic reduction was primarily caused by cell membrane disruption and microarray analysis revealed the specific genes involved during the combination treatment (Milillo et al., 2011). Microarray assays can be a great source to understand the hurdle technology for the gene expression profiling of Salmonella to identify the most effective combinations of different antimicrobial treatments (Sirsat et al., 2010). Transcriptomics to study the gene expression will provide information on which

treatment on Salmonella would regulate the survival pathway and biochemical mechanism with identifying and quantifying different genes. For the broad range of gene and protein level analysis, microarrays are advantageous since we can analyze the whole gene profile of target pathogen (Sirsat et al., 2009). Dowd et al. (2007) exposed S. Typhimurium to nalidixic acid and evaluated differential regulation of SPI-1 and 2 and induction of multidrug resistance efflux pumps and outer membrane lipoproteins using microarray. Microarrays have also been utilized to access S. Enteritidis and S. Typhimurium responses when these microorganisms were exposed to butyric acid and have shown to exhibit down-regulation of SPI-1 genes including hilA and hilD (Gantois et al., 2006). Detection of different Salmonella serovars have also been employed with this technique (Alvarez et al., 2003) as well as real-time PCR for detecting Salmonella from RTE meats (Patel and Bhagwat, 2008). Understanding the pathogen responses to the stressors would be effective to minimize cross protection of target pathogen, which in turn would potentially decrease the level of virulence expressed by these organisms when RTE foods are consumed.

CONCLUSIONs The major cause of contamination in RTE food products appears to be after cooking or after processing the product. Therefore, proper handling practices are required to minimize any cross-contamination and for the safe consumption after purchase. It is important for the workers in the processing plant to apply the appropriate sanitary practices. Pathogens can easily be transmitted by food workers, especially when handling raw food to generate RTE products such as potato salad, and sliced ham where bare hand contact may happen. Along with proper hygiene, it is also important to be careful to avoid temperature abuse during storage. In this review, physical and chemical control methods to inhibit the growth of Salmonella in RTE products were discussed. Antimicrobial agent coated packages may also be a great strategy to protect the RTE product from post-processing contamination. However, bac-

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terial resistance against antimicrobial agents and cross-protection against different hurdle treatment are also an increasing issue since this may limit handling Salmonella in RTE products. As discussed in the review, hurdle technology with the combination of the physical, chemical or biological methods may be an ideal tool for efficient control against bacterial resistance for individual control methods. Future research should focus on developing strategies such as genomic screening to design optimal multi-hurdle conditions to lower the potential growth of Salmonella in RTE food.

Acknowledgements This review was supported by National Integrated Food Safety Initiative grants (NIFSI) (2008-5111004339) to S. C. Ricke and to P. G. Crandall (201051110-21004) and a USDA Food Safety Consortium grant to S. C. Ricke.

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Rapid Communications Under normal circumstances, AFAB aims for receipt-to-decision times of approximately one month or less. Accepted papers will have priority for publication in the next available issue of AFAB. However, if an author chooses or requires a much more rapid

peer review, the journal editorial office has the capability to shorten the review timing to one week or less. Any type of manuscript whether it be a full length manuscript, brief communication or review paper can be submitted as a rapid communication. There will be additional costs for processing and page charges will be double the normal rate. Authors who choose this option must select Rapid Communications as the paper type when submitting the paper and the editors will judge whether a rapid review is possible and let the author know immediately.

Brief Communications Brief communications are short research notes giving the results of complete experiments but are considered less comprehensive than full-length articles with three (3) figures and/or tables or less. Manuscripts should be prepared with the same subheadings as full length research papers. The running head above the title of the paper is “Brief Communications.”

Unsolicited Review Papers Review papers are welcome on any topic listed in the focus section and have no page limits. Reviews are assessed the same pages charges as all other manuscripts. All AFAB guidelines for style and form apply. Major headings to include are: Abstract, Introduction, Main discussion topics and appropriate subheadings, Conclusions, Acknowledgements (optional) and References. Review papers shorter than 20 pages of double spaced text and references will be considered mini-reviews with the subheading above the title on the first page. The running head above the title of the paper is either “Review” or “Mini-review”.

Solicited Review Papers Solicited reviews will have no page limits. The editor-in-chief will send invitations to the authors and then review these contributions when they are submitted. Nominations or suggestions for potential timely reviews are welcomed by the editors or edito-

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rial board members and should be sent to submit@ afabjournal.com. There will be no page charges for solicited review papers but the solicitation must originate from the editor-in-chief or one of the editors. Requests from authors will automatically be classified as unsolicited review papers. The running head above the title of the paper will be “Invited Review.”

Conference and Special Issues Reviews AFAB welcomes opportunities to publish papers from symposia, scientific conference, and/or meetings in their entirety. Conference organizers need simply to contact AFAB at submit@afabjournal.com and a rapid decision is guaranteed. If in agreement, the conference organizers must guarantee delivery of a set number of peer reviewed manuscripts within a specified time and submitted in the same format as that described for unsolicited review papers. Conference papers must be prepared in accordance with the guidelines for review articles and are subject to peer review. The conference chair must decide whether or not they wish to serve as Special Issue Editor and conduct the editorial review process. If the conference chair/organizer chooses to serve as special issue editor, this will involve review of the papers and, if necessary, returning them to the authors for revision. The conference organizer then submits the revised manuscripts to the journal editorial office for further editorial examination. Final revisions by the author and recommendations for acceptance or rejection by the chair must be completed by a mutually agreed upon date between the editor and the conference organizer. Manuscripts not meeting this deadline will not be included in the published symposium proceedings but if submitted later can still be considered as unsolicited review papers. Although offprints and costs of pages are the same as for all other papers, the symposium chair may be asked to guarantee an agreed upon number of hard copies to be purchased by conference attendees. If the decision is not to publish the symposium as a special issue, the individual authors retain the right to submit their papers for consideration for the journal as ordinary unsolicited review manuscripts.

Book Reviews AFAB publishes reviews of books considered to be of interest to the readers. The editor-in-chief ordinarily solicits reviews. Book reviews shall be prepared in accordance to the style and form requirements of the journal, and they are subject to editorial revision. No page charges will be assessed solicited reviews while unsolicited book reviews will be assigned the regular page charge rate.

Opinions and Current Viewpoints The purpose of this section will be to discuss, critique, or expand on scientific points made in articles recently published in AFAB. Drafts must be received within 6 months of an article’s publication. Opinions and current perspectives do not have page limits. They shall have a title followed by the body of the text and references. Author name(s) and affiliation(s) shall be placed between the end of the text and list of references. If this document pertains to a particular manuscript then the author(s) of the original paper(s) will be provided a copy of the letter and offered the opportunity to submit for consideration a reply within 30 days. Responses will have the same page restrictions and format as the original opinion and current viewpoint, and the titles shall end with “Opinions.” They will be published together. Letters and replies shall follow appropriate AFAB format and may be edited by the editor-in-chief and a technical editor. If multiple letters on the same topic are received, a representative set of opinions concerning a specific article will be published. A disclaimer will be added by the editorial staff that the opinion expressed in this viewpoint is the authors alone and does not necessarily represent the opinion of AFAB or the editorial board.

COPYRIGHT AGREEMENT The copyright form is published in AFAB as space permits and is available online (www.afabjournal.com).

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AFAB grants to the author the right of re-publication in any book of which he or she is the author or editor, subject only to giving proper credit to the original journal publication of the article by AFAB. AFAB retains the copyright to all materials accepted for publication in the journal. If an author desires to reprint a table or figure published from a non-AFAB source, written evidence of copyright permission from an authority representing that source must be obtained by the author and forwarded to the AFAB editorial office.

PEER REVIEW PROCESS Authors will be requested to provide the names and complete addresses including emails of five (5) potential reviewers who have expertise in the research area and no conflict of interest with any of the authors. Except for manuscripts designated as Rapid Communication each reviewer has two (2) weeks to review the manuscript, and submit comments electronically to the editorial office. Authors have three (3) weeks to complete the revision, which shall be returned to the editorial office within six (6) weeks after which the authors risk having their manuscript removed from AFAB files if they fail to ask the editorial office for an extension by email. Deleted manuscripts will be reconsidered, but they will have to be processed as new manuscripts with an additional processing fee assessed upon submission. Once reviewed, the author will be notified of the outcome and advised accordingly. Editors handle all initial correspondence with authors during the review process. The editor-in chief will notify the author of the final decision to accept or reject. Rejected manuscripts can be resubmitted only with an invitation from the editor or editor-in chief. Revised versions of previously rejected manuscripts are treated as new submissions.

PRODUCTION OF PROOFS Accepted manuscripts are forwarded to the editorial office for technical editing and layout. The manuscript is then formatted, figures are reproduced, and author proofs are prepared as PDFs. Author proofs of all manuscripts will be provided to the correspond-

ing author. Author proofs should be read carefully and checked against the typed manuscript, because the responsibility for proofreading is with the author(s). Corrections must be returned by e-mail. Changes sent by e-mail to the technical editor must indicate page, column, and line numbers for each correction to be made on the proof. Corrections can also be marked using “track changes” in Microsoft Word or using e-annotation tools for electronic proof correction in Adobe Acrobat to indicate necessary changes. Author alterations to proofs exceeding 5% of the original proof content will be charged to the author. All correspondence of proofs must be agreed to by the editorial office and the author within 48 hours or proof will be published as is and AFAB will assume no responsibility for errors that result in the final publication.

PUBLICATION CHARGES AFAB has two publication charge options: conventional page charges and rapid communication. The current charge for conventional publication is $25 per printed page in the journal. There is no additional charge for the publication of pages containing color images, micrographs or pictures. For authors who wish to have their papers processed as a rapid communication, authors will pay the rapid communication fee when proofs are returned to the editorial office in addition to twice the conventional page charges. Charges for rapid communications are $1000 per manuscript for guaranteed peer review within one week and $100 per journal page.

HARD COPY OFFPRINTS If you are wishing to obtain a physical hard copy of the AFAB journal, offprints are available in any quantity at an additional charge: $100/page for black-white and $150/page for color prints. You may order your offprints at any time after publication on our website. Scientific conference organizers may be expected to agree to a set number of offprints as a part of their agreement with AFAB.

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MANUSCRIPT CONTENT REQUIREMENTS Preparing the Manuscript File Manuscripts must be written in grammatically correct English. AFAB offers a fee based language service upon request (language@afabjournal.com). Manuscripts should be typed double-spaced, with lines and pages numbered consecutively. All documents must be submitted in Microsoft Word (.doc or .docx, PC or Mac). All special characters (e.g., Greek, math, symbols) should be inserted using the symbols palette available in this font. Tables and figures should be placed in separate sections at the end of the manuscript (not placed in the text). Failure to follow these instructions will cause delays of the processing and review of the manuscript.

Title Page At the very top of the title page, include a title of not more than 100 characters. Format the title with the first letter of each word capitalized. No abbreviations should be used. Under the title, the authors names are listed. Use the author’s initials for both first and middle names with a period (full-stop) between initials (e.g., W. A. Afab). Underneath the authors, a list affiliations must be listed. Please use numerical superscripts after the author’s names to designate affiliation. If an authors address has changed since the research was completed, this new information must be designated as “Current address:”. The corresponding author should be indicated with an asterisk e.g., * Corresponding author. The title page shall include the name and full address of the corresponding author. Telephone and e-mail address must also be provided for the corresponding author, and emailaddresses must be provided for all authors.

at the beginning of the manuscript. In vivo, in vitro and bacterial names must be italicized (obligatory). Authors must avoid single sentence paragraphs and merge such paragraphs appropriately. Authors must not begin sentences with “Figure or Table shows…” as these are inanimate objects and cannot “show” anything. When number are reported in text or in tables, always put a zero in front of decimal numbers: “0.10” instead of “.10”.

Manuscript Sections Abstract The abstract provides an abridged version of the manuscript. Please submit your abstract on a separate page after the title page. The abstract should provide a justification of your work, objectives, methods, results, discussion and implications of study or review findings . Your abstract must consist of complete sentences without references to other work or footnotes and must not exceed 250 words. On the same page as your abstract, please provide at least ten (10) keywords to be used for linking and indexing. Ideally, these keywords should include significant words from the title.

Introduction The introduction should clearly present the foundation of the manuscript topic and what makes the research or the review unique. The introduction should validate why this topic is important based on previously published literature, and the relevance of the current research. Overall goals and project objectives must be clearly stated in the final sentence of the last paragraphs of the introduction.

Materials and Methods Editing Author-derived abbreviations should be defined at first use in the abstract and again in the body of the manuscript. If abbreviations are extensive authors may need to provide a list of abbreviations

Information on equipment and chemicals used must include the full company name, city, and state (country if outside the United States or Province if in Canada) [i.e., (Model 123, ACME Inc., Afab, AR)].

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Variability, Replication, and Statistical Analysis To properly assess biological systems independent replication of experiments and quantification of variation among replicates is required by AFAB. Reviewers and/or editors may request additional statistical analysis depending on the nature of the data and it will be the responsibility of the authors to respond appropriately. Statistical methods commonly used in the bacteriology do not need to be described in detail, but an adequate description and/or appropriate references should be provided. The statistical model and experimental unit must be designated when appropriate. The experimental unit is the smallest unit to which an individual treatment is imposed. For bacterial growth studies, the average of replicate tubes per single study per treatment is the experimental unit; therefore, individual studies must be replicated. Repeated time analyses of the same sample usually do not constitute independent experimental units. Measurements on the same experimental unit over time are also not independent and must not be considered as independent experimental units. For analysis of time effects, assess as a rate of change over time. Standard deviation refers to the variability in the biological response being measured and is presented as standard deviation or standard error according to the definitions described in statistical references or textbooks.

Results Results represent the presentation of data in words and all data should be described in same fashion. No discussion of literature is included in the results section.

Discussion The discussion section involves comparing the current data outcomes with previously published work in this area without repeating the text in the results section. Critical and in-depth dialogue is encouraged.

Results and Discussion Results and discussion can be under combined or separate headings.

Conclusions State conclusions (not a summary) briefly in one paragraph

Acknowledgments Acknowledgments of individuals should include institution, city, and state; city and country if not U.S.; and City or Province if in Canada. Copies being reviewed shall have authors’ institutions omitted to retain anonymity.

References a) Citing References In Text Authors of cited papers in the text are to be presented as follows: Adams and Harry (1992) or Smith and Jones (1990, 1992). If more than two authors of one article, the first author’s name is followed by the abbreviation et al. in italics. If the sentence structure requires that the authors’ names be included in parentheses, the proper format is (Adams and Harry, 1982; Harry, 1988a,b; Harry et al., 1993). Citations to a group of references should be listed first alphabetically then chronologically. Work that has not been submitted or accepted for publication shall be listed in the text as: “G.C. Jay (institution, city, and state, personal communication).” The author’s own unpublished work should be listed in the text as “(J. Adams, unpublished data).” Personal communications and unsubmitted unpublished data must not be included in the References section. Two or more publications by the same authors in the same year must be made distinct with lowercase letters after the year (2010a,b). Likewise when multiple author citations designated by et al. in the text have the same first author, then even if the other authors are different these references in the text and the references section must be identified by a letter. For example

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“(James et al., 2010a,b)” in text, refers to “James, Smith, and Elliot. 2010a” and “James, West, and Adams. 2010b” in the reference section.

Book Chapter: Author(s) of the chapter. Year. Title of the chapter. In: author(s) or editor(s). Title of the book. Edition or volume, if relevant. Publisher name, Place of publication.

b) Citing References In Reference Section In the References section, references are listed in alphabetical order by authors’ last names, and then chronologically. List only those references cited in the text. Manuscripts submitted for publication, accepted for publication or in press can be given in the reference section followed by the designation: “(submitted)”, “(accepted)’, or “(In Press), respectively. If the DOI number of unpublished references is available, you must give the number. The year of publication follows the authors’ names. All authors’ names must be included in the citation in the Reference section. Journals must be abbreviated. First and last page numbers must be provided. Sample references are given below. Consult recent issues of AFAB for examples not included in the following section. Journal manuscript: Author(s). Year. Article title. Journal title [abbreviated]. Volume number:inclusive pages.

Examples: Chase, G. and L. Erlandsen. 1976. Evidence for a complex life cycle and endospore formation in the attached, filamentous, segmented bacterium from murine ileum. J. Bacteriol. 127:572-583. Jiang, B., A.-M. Henstra, L. Paulo, M. Balk, W. van Doesburg, and A. J. M. Stams. 2009. A typical one-carbon metabolism of an acetogenic and hydrogenogenic Moorella thermioacetica strain. Arch. Microbiol. 191:123-131. Book: Examples: Author(s) [or editor(s)]. Year. Title. Edition or volume (if relevant). Publisher name, Place of publication. Number

Inclusive pages of chapter.

Examples: O’Bryan, C. A., P. G. Crandall, and C. Bruhn. 2010. Assessing consumer concerns and perceptions of food safety risks and practices: Methodologies and outcomes. In: S. C. Ricke and F. T. Jones. Eds. Perspectives on Food Safety Issues of Food Animal Derived Foods. Univ. Arkansas Press, Fayetteville, AR. p 273-288. Dissertation and thesis: Author. Date of degree. Title. Type of publication, such as Ph.D. Diss or M.S. thesis. Institution, Place of institution. Total number of pages.

Maciorowski, K. G. 2000. Rapid detection of Salmonella spp. and indicators of fecal contamination in animal feed. Ph.D. Diss. Texas A&M University, College Station, TX. Donalson, L. M. 2005. The in vivo and in vitro effect of a fructooligosacharide prebiotic combined with alfalfa molt diets on egg production and Salmonella in laying hens. M.S. thesis. Texas A&M University, College Station, TX. Van Loo, E. 2009. Consumer perception of ready-toeat deli foods and organic meat. M.S. thesis. University of Arkansas, Fayetteville, AR. 202 p. Web sites, patents: Examples: Davis, C. 2010. Salmonella. Medicinenet.com. http://www.medicinenet.com/salmonella /article. htm. Accessed July, 2010.

of pages.

Hungate, R. E. 1966. The rumen and its microbes. Academic Press, Inc., New York, NY. 533 p.

Afab, F. 2010, Development of a novel process. U.S. Patent #_____

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Abstracts and Symposia Proceedings: Fischer, J. R. 2007. Building a prosperous future in which agriculture uses and produces energy efficiently and effectively. NABC report 19, Agricultural Biofuels: Tech., Sustainability, and Profitability. p.27 Musgrove, M. T., and M. E. Berrang. 2008. Presence of aerobic microorganisms, Enterobacteriaceae and Salmonella in the shell egg processing environment. IAFP 95th Annual Meeting. p. 47 (Abstr. #T6-10) Vianna, M. E., H. P. Horz, G. Conrads. 2006. Options and risks by using diagnostic gene chips. Program and abstracts book , The 8th Biennieal Congress of the Anaerobe Society of the Americas. p. 86 (Abstr.)

Data Presentation in Tables and Figures Figures and tables to be published in AFAB must be constructed in such a fashion that they are able to “stand alone” in the published manuscript. This

means that the reader should be able to look at the figure or table independently of the rest of the manuscript and be able to comprehend the experimental approach sufficiently to interpret the data. Consequently, all statistical analyses should be very carefully presented along with variation estimates and what constitutes an independent replication and the number of replicates used to calculate the averages presented in the table or figure. Each table and figure must be on a separate page in the submitted paper. If your manuscript is accepted for publication, you will need to submit all data for charts, tables and figures in Excel spreadsheet format. All figures should be clearly presented with well defined axis and units of measurement. Symbols, lines, and bars must be made distinct as “stand alone” black and white presentations. Stippling, dashed lines etc. are encouraged for multiple comparison but shades of gray are discouraged. Color images, micrographs, pictures are recommended and there is no additional fee for their submission.

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