AFAB-Vol.2-Issue-1

Volume 2, Issue 1June 2012

Sooyoun Ahn Arkansas State University, USA

Walid Q. AlaliUniversity of Georgia, USA

Kenneth M. Bischoff NCAUR, USDA-ARS, USA

Claudia S. Dunkley University of Georgia, USA

Lawrence GoodridgeColorado State University, USA

Leluo GuanUniversity of Alberta, Canada

Joshua GurtlerERRC, USDA-ARS, USA

Yong D. HangCornell University, USA

Divya JaroniSouthern University, USA

Weihong Jiang Shanghai Institute for Biol. Sciences, P.R. China

Michael JohnsonUniversity of Arkansas, USA

Timothy KellyEast Carolina University, USA

William R. KenealyMascoma Corporation, USA

Hae-Yeong Kim Kyung Hee University, South Korea

W.K. KimUniversity of Manitoba, Canada

M.B. KirkhamKansas State University, USA

Todd KostmanUniversity of Wisconsin, Oshkosh, USA

Y.M. Kwon University of Arkansas, USA

Maria Luz Sanz MuriasInstituto de Quimica Organic General, Spain

Melanie R. MormileMissouri University of Science and Tech., USA

Rama NannapaneniMississippi State University, USA

Jack A. Neal, Jr.University of Houston, USA

Benedict OkekeAuburn University at Montgomery, USA

John PattersonPurdue University, USA

Toni Poole FFSRU, USDA-ARS, USA

Marcos RostagnoLBRU, USDA-ARS, USA

Roni ShapiraHebrew University of Jerusalem, Israel

Kalidas ShettyUniversity of Massachusetts, USA

EDITORIAL BOARD

EDITOR-IN-CHIEFSteven C. RickeUniversity of Arkansas, USA

EDITORSTodd R. CallawayFFSRU, USADA-ARS, USA

Cesar CompadreUniversity of Arkansas for Medical Sciences, USA

Philip G. CrandallUniversity of Arkansas, USA

EDITORIAL STAFFMANAGING EDITORS

Ellen J. Van LooGhent, BelgiumDave EdmarkFayetteville, Arkansas, USA

LAYOUT EDITORMelody Rust

Eureka Springs Arkansas, USA TECHNICAL EDITOR

Jessica C. ShabaturaFayetteville Arkansas, USA

ONLINE EDITION EDITORC.S. ShabaturaFayetteville Arkansas, USA

ABOUT THIS PUBLICATION

Agriculture, Food & Analytical Bacteriology (ISSN

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TABLE OF CONTENTS

The Story of the Arkansas Association for Food Protection (AAFP) M. Sostrin

4

A Team Approach for Management of the Elements of a Listeria Intervention and Control Program J. N. Butts

6

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

15

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

25

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

35

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

43

CONFERENCE PROCEEDINGS*

REVIEWS*

Instructions for Authors69

EXTRAS

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

46

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

56

* Arkansas Association for Food Protection (AAFP) Conference, Enhancing Food protection From Farm to Fork,

held on Sept. 28-29, 2011, Springdale, AR.

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

www.afabjournal.comCopyright © 2012

Agriculture, Food and Analytical Bacteriology

Michael SostrinSenior Manager, Food Safety RecallsWalmart Stores, [email protected]

CONFERENCE PROCEEDINGS*The Story of the Arkansas Association for Food Protection (AAFP)

M. SostrinSenior 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.

ABSTRACTThe Arkansas Association for Food Protection (AAFP) is a diverse group of Academia, Industry, Regula-tory 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 com-

mon 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. Togeth-

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 mem-

bership in the areas of food safety and quality.”

The AAFP was chartered in April of 2009 as an af-

filiate of the International Association for Food Pro-

tection (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 Confer-

ences in October 2009 and September 2010 have by

The story of the Arkansas Association for Food Protection (AAFP)

Agric. Food Anal. Bacteriol. • AFABjournal.com • Vol. 2, Issue 1 - 2012 5

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 Protec-

tion From Farm to Fork.” At each of these meeting

participants from academia, industry, retail and gov-

ernment 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, reg-

ulatory and retail professionals join together in pro-

viding 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 dis-

cuss 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 educa-

tional conference food safety and quality profession-

als gain access to a network of professional contacts

and organizations that can help them both person-

ally and professionally. AAFP through its educational

conference provides its members with access to in-

novative 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 mem-

bers 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 orga-

nization 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 Asso-

ciation 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.




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 Pre-

ventative 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, Con-

trol, AMI, Post Rinse, Investigation, Growth Niche

InTRoduCTIon

The control of Listeria in the U.S. federally inspect-

ed meat plants has dramatically improved in the last

twenty years (Figure 1). This effect is being measured

and monitored by FSIS sampling of finished prod-

uct from establishments hat produce post-lethality

exposed.

Correspondence: J. N. Butts, [email protected]

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 man-

aged in such a manner to minimize the transfer

of the Listeria.

3. Hurdles to entry into RTE area can minimize cross

contamination.

Please note that managing these factors will not to-

tally control or prevent product contamination (HACCP

CCP). These factors do, however, minimize the poten-

CONFERENCE PROCEEDINGS*A Team Approach for Management of the Elements of a Listeria Intervention

and Control ProgramJ. N. Butts1

1 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.



tial for contamination. The key to control is the

management of total system which I will call “pro-

cess management.”

Process management is based on managing

many interrelated factors. These include:

1. The development of Best Practices associat-

ed with AMI Principles of Sanitary Facility and

Equipment Design.

2. These principles and audit items, when com-

bined with the Global Food Safety Initiative

(GFSI) audit questions, provide establish-

ments 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 fully-

shared their Best Practices.

3. This “teamwork” is best demonstrated by the

AMI Listeria Intervention and Control Work-

shops. The presenters at each workshop con-

sist 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 supple-

ment the learning experience. Real life situ-

ations 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 con-

tinuous 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

FSIS Regulatory Testing for LM in RTE Products by Calendar Year 1990 - 2009*

(All Years All Projects)

4.61

4.03

3.613.44

2.903.02

2.91

2.25

2.54

1.91

1.451.32

1.03

0.760.91

0.68

0.48 0.43 0.42 0.37

0.00

0.50

1.00

1.50

2.00

2.50

3.00

3.50

4.00

4.50

5.00

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

Calendar Year*

Perc

en

t P

osi

tive

*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).


companies go through a series of transi-

tion phases as the success in Listeria control

evolved. These transition phases can be di-

vided into four stages (Table 1).

The evoluTIon oF envIRonmenTAl ConTRol

Individual stages are characterized by how a

plant views and controls Listeria, sampling meth-

ods and results along with their perspective on

the difference between samples taken for control

purposes versus verification of control. Specifi-

cally, 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 signifi-

cant 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 pro-

cess control measurements.” The measurement sys-

tem continues co-evolve. Verification sites grow in

numbers and size as the process control sites evolve.

The process control sites become “indicators of con-

trol” 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 veri-

fication becomes more precise and control mea-

sures 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

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 sam-pling of contact surfaces and environmental sites. Inter-mittent positives on contact surfaces. Routine positives on environmental sites

Recognize existence of growth niches. Sample con-tact 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 Con-tact Surface positives. No Product Positives. Investiga-tive facility based positives dominate RTE.

Potential Growth niches mapped. Some scheduled in-tervention practices in place. Managing “Critical Factors” of the Sanitation process. En-gaged in Equipment and Fa-cility redesign.

Product, Contact Surfaces & Primary Transfer Vectors in RTE Area

Predictive No Contact surface posi-tives. Zone 4 positives pre-dominate. Hurdle transfer point sampling produces rare positives.

Aggressive early warning sam-pling in place. Intervention practices in place with all RTE equipment. Focus on zone 4 and facilities. Advanced phas-es of both Equipment and Fa-cility redesign.

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

Table 1. Four stages of environmental control within plants.


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 account-able for achieving results

Bob Reinhard – Sara Lee

Figure 2. Management commitment model

When this commitment model is overlaid on a

continuous improvement model, we see plants mov-

ing 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 elimi-

nated and transfer vectors are going to exist whenever

a food product is exposed to the environment. Man-

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 3). The development and deployment of pre-

ventive practices eliminates “firefighting”. The success

of these practices leads to further implementation of

preventative practices. Success under supportive man-

agement 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 deploy-

ment. A preventative practice can become a predic-

tive practice when deployed based on a defined need.

Indicator sites are established to signal this deploy-

ment. Indicator sites need to be located at points in

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 pasteuri-

zation of a conveyor belt for example. Regular sam-

pling of indicator sites then become the predictive trig-

ger 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 vali-

dation 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

Figure 4. Model for Listeria control

Figure 3. Commitment model combined with continuous improvement


of equipment that collect spatter from the initial rins-

ing process. Typical sites are the sides of machines,

framework, underneath assemblies and exposed com-

ponents that may receive spatter from other machine

parts and the floor. Post rinse sites can be composit-

ed 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 fol-

low with multiple days of daily sampling (i.e. 10). If a

positive is found in the follow up sampling then an in-

vestigation 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 clean-

ing 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 inves-

tigation is needed to locate the source of the organism

be it a growth niche or transfer vector bringing the or-

ganism into the RTE area. Indicator sites are not valida-

tion sites, but sites measuring the control at a specific

point in the process.

Teamwork is the deployment vehicle for the trans-

formation of the cultural change. Management must

make verification sites the key process indicators (KPI’s)

and reward employee success in finding out of toler-

ance 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 manage-

ment tool to develop and sustain the gains in envi-

ronmental 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 sanita-

tion 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 tech-

niques 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 Com-puter 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 de-

tailed 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, meth-ods 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


stroy (S&D) Investigation Process (Figure 7) is a

tool with many applications.

The Seek & Destroy Process is a scientific meth-

od to:

1. Find pathogenic growth niches

2. Find potential growth niches requiring mon-

itoring 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 Mis-

sion)

7. Validate effectiveness of equipment clean-

ing protocol

8. Validate effectiveness of intervention ap-

plied to a piece of equipment (heat treat-

ment or other method)

The piece of equipment should be complete-

ly 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 har-

boring in that piece of equipment.

TImed STudIeS

Transfer vectors are defined and measured us-

ing Timed Studies. Here is an example of a Timed

Study being used to locate a transfer vector bring-

ing 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 pos-

itive indicated a potential for contamination still

exists.

This method of sampling identifies the pathway

and vehicles of transport to a line from the environ-

ment. 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

Facility Design Team Charter

Purpose:

The purpose of the team is to maintain and con-tinuously improve the facility by evaluating the facility sanitary design and determining the ar-eas where improvements/repairs are needed.

Methods:

1. Utilize the AMI Sanitary Facility Design Check-list and SQF (GFSI) facility related audit require-ments.

2. Assign risk values to plant areas & checklist items

3. Use Risk assessment to assist in prioritizing ma-jor 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 re-sources are best utilized.

5. Recommend the purchase of additional equip-ment 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 pre-sentations.

9. Recommend capital expenditures to maintain and improve the facility.

Figure 6. Facility design team charter

Figure 7. “Seek and Destroy” process


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 ap-

proach 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 pro-

duction 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

InveSTIGATIon ToolS

Table 2. Scientific methods for investigation following a positive sample

Tool Source of Environmental Contamination

S&D Growth niche in line equipment

S&D Growth niche in ancillary equip-ment

Swat Team Growth niche in transient equip-ment

Timed Study Growth niche in facility

Timed Study Transfer of organism form out-side 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 op-

portunities for the development of growth niches.

Growth niches evolve because the organism enter-

ing into a hard-to-dissemble and clean area. A com-

mon 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 prod-

uct contact surface. Those growth niches that can-

not be exposed need an alternative source of con-

trol such as the application of heat to pasteurize the

equipment or equipment part.

Sanitary design of the facility and equipment sup-

plemented with Sanitation Process Control has been

effective in preventing product contamination. Sani-

Figure 8.


tation Process Control is defined by the critical fac-

tors 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 interven-

tions and periodic cleaning and sanitation proce-

dures. During operations transfer vectors are con-

trolled by:

• Distinct hygienic zones established in the fa-

cility

• 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 execut-

ed to establish control and to prevent cross-

contamination

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 de-

veloped 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 in-

terventions . Verification sites identify a loss of con-

trol. 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 effec-tive

• The Sanitation process and Sanitary Manufac-turing Operating Procedures are defined and repeatable.

• General employee and Sanitation Operator Training programs clearly define and effectively communicate the process requirements neces-sary 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 di-rect 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 sam-pling if process control appears to be violated.

• Growth niches in any location within the Ex-posed Product Area are identified and are ei-ther eliminated or managed.

• The environment within the Exposed Product Area is controlled to minimize microbial out-growth.

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


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

• Additions or changes to the process or equip-ment within the Exposed Product Area are monitored and qualified to not introduce or harbor microorganisms.Data from investiga-tion, indicator and verification sites should sup-port 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 peo-

ple 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.haccpal-

liance.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




ABSTRACT

To protect the American food supply, there is a need to educate graduate students and working pro-

fessionals in food and agriculture-related fields about food defense. Kansas State University, Purdue Uni-

versity, 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 re-

sults 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 mod-

ules 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 ques-

tions, 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

Correspondence: K. J. K. Getty, [email protected]: +1 -229-386-3363 Fax: +1-229-86-3239

CONFERENCE PROCEEDINGS*Development of a Food Defense Workshop and Graduate Certificate in Food

Safety and Defense for Working ProfessionalsK. J. K. Getty1

1 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




InTRoduCTIon

The agriculture and food sector has been formally

identified by the U.S. Department of Homeland Securi-

ty (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 at-

tacks, major disasters, and other emergencies. An in-

tentional 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 pro-

fessionals 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 Indi-

ana University-Purdue University at Indianapolis have

worked together to develop a graduate level interdis-

ciplinary, 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 knowl-

edge domains and skills needed by food safety and

defense professionals, (2) to validate findings from

the DACUM process through a survey sent to profes-

sionals working in food safety and defense, and (3) to

develop modules for a two-day food defense work-

shop for stakeholders, graduate students, and work-

ing 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 pro-

fessionals. 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 de-

scribe/define their job than anyone else, (2) any job can

be properly described in terms of the tasks that com-

petent 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 informa-

tion validated through the DACUM process.

Because food defense requires an interdisciplinary

approach, a multi-state university collaborative ap-

proach is required to develop a comprehensive cur-

riculum. Kansas State University, Iowa State Univer-

sity, 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 univer-

sity 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 as-

sembled to identify knowledge domains, learning ob-

jectives, and core educational competencies required

for food defense professionals. A survey was sent elec-


tronically to professionals in the food and agriculture

industry, academics, and public health. A total of 297

professional respondents validated 107 key knowl-

edge items from the DACUM process.

Key knowledge domains from the DACUM work-

shop were split into relevant categories by topic ar-

eas 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).

Food Defense Workshop

Information from the DACUM process and survey

were used to develop curriculum modules for a two-

day 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 mod-

ule 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 objec-

tives were met, along with general module self-per-

ception indicators of presentation value, knowledge

gained, an overall module “grade,” and additional

comments. Demographic information also was col-

lected.

Graduate Certificate in Food Safety and Defense

Faculty from Kansas State University, Iowa State

University, the University of Nebraska, and Univer-

sity of Missouri received a USDA-funded Higher

Education Challenge grant to assist in the devel-

opment of a Graduate Certificate in Food Safety

and Defense to be offered via distance or on-

campus. 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 sim-

plified access to courses offered across the other

cooperating institutions.

Core courses and elective courses were deter-

mined with a total credit hour equaling 12 hours

(AGIDEA, 2010). Each institution proposed the


through their respective Departments, Colleges,

Graduate Schools, and Faculty Senate. Courses

not offered by a home institution were proposed

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

Module Title

1. The Food and Agricultural System as a Crit-ical Infrastructure

2. The Food Agricultural System as a Potential Target of Attack

3. Policy and Risk Assessment

4., 5. Threats to Food and Agricultural Systems, Parts 1 and 2

6. 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


as new courses and assigned home institution

numbers. This would allow for a student to be en-

rolled at a home institution and take courses at the

other participating universities without having to pay

a different tuition rate or having the courses consid-

ered as transfer credits.

The purpose of the certificate is to provide stu-

dents with specialized education so that they can

be better prepared to meet the challenges of ac-

cidental or deliberate food contamination within

the food industry to protect public health, pre-

vent 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 ad-

mission requirements of their selected home in-

stitution. In addition, students should have an un-

dergraduate degree in food science or otherwise

meet the prerequisite requirements for admission

to the Food Science Graduate Program. The con-

sortium faculty also determined program require-

ments and have developed learning outcomes, as-

sessment 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 se-

curity, and protect the environment, a food defense

professional provides leadership; evaluates food sys-

tems, facilities, property, products, people, and pro-

cedures for vulnerabilities; develops and implements

policies and preventative control measures for food

security/defense; and develops and implements ef-

fective food emergency responses by using analytical,

empirical, assessment, detection, communication,

observational techniques to address outcomes.”

A total of 297 participants responded to the DA-

CUM survey and 95 (30.2%) were from food manu-

Table 2. Example learning outcomes from se-lected 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 at-tractive 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 motiva-tions

• 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 vul-nerabilities in food and water systems

• Explain why vulnerability assessments are per-formed 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, juris-dictional authority, and statutes involved in re-sponding 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 af-ter a food defense incident.


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 safe-

ty 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 receiv-

ing some of the highest mean importance-frequen-

cy 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 de-

scribes your current job?” - 27% indicated industry,

22% were regulatory, 17% were students, 10% oth-

ers, and 2% didn’t indicate a sector. In regards to the

demographic question, “Before attending this work-

shop, 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-

0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0 4.5 5.0

Capsto

ne Exp

erience

Food and A

g Syste

ms

Food Safety

and D

efense

Comm

unicatio

n

Facilit

y and Site

Securit

y

Threat

Ass

essm

ent/Vulnera

bility

Risk A

nalysis

Policy I

ssues

Criminal

Justi

ce/ I

nvesti

gation

Emerg

ency M

anag

ement

Public H

ealth

Mea

n I-F

Val

ue

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.


Figure 2. Quartile breakdown of combined importance-frequency by each category from the DA-CUM 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.

0

5

10

15

20

25

Capsto

ne Exp

erience

Food and A

g Syste

m

Food Safety

and D

efense

Comm

unicatio

n

Facilit

y and Site

Securit

y

Threat

Ass

essm

ent/Vulnera

bility

Risk A

nalysis

Policy I

ssues

Criminal

Justi

ce/In

vesti

gation

Emerg

ency M

anag

ement

Public H

ealth

Num

ber

of

Kno

wle

dg

e It

ems

Q4 (#82-107)

Q3 (#55-81)

Q2 (#28-54)

Q1 (#1-27)

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”)

2 Food and Ag Systems Vulnerabilities in food and agriculture systems

3 Capstone Experience Necessary components of a food defense plan

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

5 Food Safety and Defense Potential food safety hazards (biological, chemical, physical, radiological)

6 Facility and Site Security How to implement appropriate security systems and procedures to prevent a deliberate food contamination event

7 Communication Proficiency in written and verbal communication

8 Food Safety and Defense Food defense plan development

9 Food and Ag Systems Food production systems and food product characteristics

10 Food Safety and Defense Traceability (methods, processes, and systems)

11 Food Safety and Defense Food processing facility and system operations

12 Food Safety and Defense How food processing systems prevent, control, and mitigate food safety hazards

13 Food Safety and Defense HACCP and associate prerequisite programs

14 Facility and Site Security Physical and operations security countermeasures

15 Food Safety and Defense Hazard detection, monitoring, and identification processes


ing a food defense plan, and modules that were

specific about food 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 re-

gards to the learning outcomes (Table 7).

dISCuSSIon

“Deliberate contamination of the nation’s food

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

Evaluation StatementMean Response± StandardDeviation

± Standard Deviation

Overall quality of program content.

4.41 ± 0.68

Overall quality of program modules.

4.21 ± 0.68

Overall quality of program presenters.

4.24 ± 0.74

Overall quality of handouts and materials.

4.10 ± 0.98

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

Did the program meet your needs?

2.97 ± 0.19

Did the program meet your expectations?

2.93 ± 0.26

Was the overall experience valuable to you?

3.00 ± 0.00

Would you recommend this workshop program to others?

3.00 ± 0.00

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

Table 5. Core and elective courses for the graduate certificate in food safety and de-fense.

Core Courses (Required): 8 or 9 credits• A Multidisciplinary Overview of Food Safety &

Security

• Microbiology of Food (2 credits) or Food Micro-biology (3 credits)

• Principles of HACCP

• Food Toxicants

Elective Courses:

• Food Protection and Defense – Essential Con-cepts

• Food Laws and the Regulatory Process

• Advanced Food Microbiology & Biotechnology

• Rapid Methods in Food Microbiology

• Microbiology of Fermented Foods

• Trade and Agricultural Health

• Ethnic Foods: Food Safety, Food Protection and Defense

Table 6. Learning outcomes for graduate cer-tificate 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 mi-crobial and chemical risks as they relate to food safety and defense issues in real world situa-tions.

3. Ability to apply the concepts of HACCP pro-grams, as well as other safety and defense pro-grams, 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 psy-

chological implications of an attack on the food sup-

ply 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


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 at-

tack on the food supply in September 1984. The Ra-

jneesh cult inoculated salad bars at local restaurants

with Salmonella Typhimurium so that the population

would not be able to vote in the local elections (Mill-

er et al., 2002). In late December 2002, 36 people

became ill after purchasing ground beef at a Michi-

gan supermarket. Following an investigation by the

U.S. Department of Agriculture (USDA), it was deter-

mined that a disgruntled employee had intention-

ally 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 na-

tion’s food supply to an intentional attack (NCFPD,

2006). The Center is composed of researchers and

investigators from food industry companies, govern-

mental agencies, and academic institutions. One of

the Center’s research needs is education programs

(NCFPD, 2006).

Homeland Security Presidential Directive 9 (HSPD-

9, 2004) states, “We should provide the best protec-

tion possible against a successful attack on the Unit-

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-assess-ment of your achievement of the program learning outcomes.

1 2 3 4 5

42.1 My ability to discuss the multi-faceted areas affected by Food Safety is-sues 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 Analy-sis 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, understand-ing, and appreciation of Food Safety issues in my institution, company or industry has increased.

42.8 My confidence to implement and advance the knowledge, understand-ing, and appreciation of Food Defense issues in my institution, com-pany or industry has increased.


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 profession-

als about food safety and defense.

Formal food defense courses are needed to con-

tinually 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 Kan-

sas 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 sup-

ply from accidental or deliberate contamination with

pathogenic microbes and/or toxicants (AGIDEA,

2010).

ACknoWledGemenT

The DACUM process and Food Defense Work-

shop was funded by USDA CSREES National In-

tegrated 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 prin-

cipal investigators and graduate students at each

university: Purdue University - Richard Linton (cur-

rently at Ohio State University), William Field, Alok

Chaturvedi, Clifford Racz; Indiana University – David

McSwane and Theodore Grain; Kansas State Uni-

versity – Abbey Nutsch,Kelly Getty, Justin Kastner,

Sheryl Hodge, Kelly Getty, Curtis Kastner, Dirk Maier,

Nigel Harper, Keith Pritts, Blair Tenhouse, and Kath-

ryn Krusemark; and National Registry of Food Safety

Professionals - Cynthia Woodley. Principal investiga-

tors 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 Nebras-

ka-Lincoln – Robert Hutkins.

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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 socio-

economic burden of a single nosocomial NoV out-

break 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, [email protected]: +1 -479-575-6515

are caused by transmission via contaminated food-

stuffs 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 packag-

ing of final product (i.e. deli meats, packaged salad

greens) (Malek et al., 2009); and 3) during prepara-

tion 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-

CONFERENCE PROCEEDINGS* - REVIEWHuman Noroviruses and Food Safety

K. E. Gibson1 and S. C. Ricke1

1University 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


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 sup-

ply chain.

Keywords: Human norovirus, food safety, acute gastroenteritis, minimally processed, ready-to-eat,

prevention, calicivirus, person-to-person, environmental transmission



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 envi-

ronment and food handling environments.

key ChARACTeRISTICS oF humAn noRovIRuS

Virus structure and classification

As members of the Caliciviridae family, norovirus-

es are a group of evolutionarily related single-strand-

ed, positive-sense RNA viruses—some causing gas-

troenteritis 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 vi-

ruses, 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 ma-

jor 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 lim-

ited 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 in-

fection include acute onset of nausea, vomiting, ab-

dominal 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 expe-

rience more severe symptoms (i.e. fever and dehy-

dration) 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 re-

ported most frequently in association with scenarios

or environments that favor person-to-person con-

tact 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 re-

sponses related to infection with NoV are not well

understood due to the lack of a reproducible in vi-

tro 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 micros-

copy and molecular methods such as reverse tran-

scription PCR (RT-PCR) for detection. As a result,


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 gas-

troduodenal epithelial cells as ligands—similar to

the attachment of rabbit hemorrhagic disease virus,

also a member of the Caliciviridae family—and re-

vealed that NoV do in fact bind to specific carbohy-

drates 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 re-

lated carbohydrates found in secretions and on mu-

cosal 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 vi-

rus 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 im-

mune response can be induced), researchers have

been able to piece together key aspects of NoV im-

munity. With respect to the human challenge stud-

ies, 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 gen-

otypes throughout one’s life (LoBue et al., 2010). As

explained previously, HBGA receptors on the muco-

sal 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 geno-

types 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) (Don-

aldson et al., 2010). Finally, research has shown that

NoV evolves through the synergistic effects of anti-

genic drift and HBGA receptor switching—there is

an immense range of similar, yet distinct HBGA re-

ceptors available on the GI tract surfaces that can

interface with the NoV protein capsid carbohydrate

Pre-Harvest Post-Harvest Food Preparation

Field (produce)

Estuary (oysters)

Irrigation Water

Compost or Biosolids

Water impacted by sewage

Product Consumed Raw

Washing/Processing

Wash Water Quality

Environmental Surfaces

Product Consumed Ready-to-Eat

Prepared Foods

Food Handler

Food Contact Surfaces Water

Quality

AGI (individual or outbreak)

Figure 1. Potential points of human norovirus contamination at each node in the farm to fork sup-ply chain. AGI = acute gastrointestinal illness.


binding domain (Lindesmith et al., 2008). Recent pa-

pers 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 immuno-

logical aspects of NoV infection.

TRAnSmISSIon oF humAn noRovI-RuS

Transmission of NoV through food, water, fomite

(or inanimate) surfaces, and person-to-person is rela-

tively 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 period—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 domi-

nance 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 ini-

tial phase of the supply chain during pre-harvest.

With respect to fruits and vegetables, NoV may be

introduced to crops via contaminated irrigation wa-

ter 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 contami-

nated 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 in-

ternalized 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 sur-

vival on lettuce), ambient temperature, relative hu-

midity, 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 ad-

ditional information about current research involving

virus fate and transport in the environment.

Contamination of bivalve mollusks, specifically

oysters, with NoV during production has been well-

documented (Bosch and Le Guyader, 2010). Inher-

ent to the way oysters are produced, bay and estu-

ary 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 fil-

ter feeders and tend to accumulate and concentrate

viruses and other microorganisms within their diges-

tive 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 bio-

accumulates very efficiently in oysters while the GII.4

strain (i.e. the NoV strain which predominantly cir-

culates 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


as well as the efficacy of the methods used for

washing and sanitizing fresh produce. Some of

the harvesting practices that may allow fresh pro-

duce to become contaminated include: 1) bare-

hand harvesting combined with a lack of personal

hygiene (i.e. hand washing); 2) continuous use of

disposable (latex) gloves (e.g., accumulation of or-

ganic matter contaminated with NoV could allow

for wide-spread distribution within a crop) with-

out 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 prep-

aration is reportedly the most common cause of NoV

outbreaks with a known food commodity. Within the

food preparation environment, NoV may be trans-

ferred to food by contaminated surfaces, a food han-

dler infected with NoV (symptomatic or asymptomat-

ic) 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 dis-

ease 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 sur-

vival of pathogens in the food preparation environ-

ment, and reduction of contamination (Greig et al.,

2007). Because of the low infectious dose, high num-

ber of viruses shed during infection and non-envel-

oped 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 hu-mAn noRovIRuS

Because of their nonenveloped structure, NoV is

presumed to be relatively resistant to chemical inacti-

vation (i.e. chlorination) and environmental degrada-

tion (temperature, pH, ultraviolet radiation, desicca-

tion) 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 Calici-

viridae family; however, FCV (a feline respiratory virus)

belongs to the Vesivirus genus whereas MNV is locat-

ed 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 prod-

ucts (e.g., recommended sanitizing agents, disinfec-

tion 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. Tradi-

tional 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 monocyto-

genes, and Salmonella spp., and not viral pathogens

(Grove et al., 2006; Hirneisen et al., 2010; Koopmans

and Duizer, 2004). Additionally, most of the engi-

neering 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 on-

farm food safety, irrigation water should be tested

for more than just bacterial indicators (i.e. fecal co-


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, harvest-

ing practices related to fresh produce such as wash-

ing products with a sanitizing agent should be vali-

dated for efficacy against enteric viruses—chlorine

bleach is most commonly used though the concen-

tration and contact time may be ineffective against

viruses (Hirneisen et al., 2010). More advanced tech-

nologies such as high pressure processing (HPP)

have been reported as effective against MNV inocu-

lated 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 contamina-

tion 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 storm-

water runoff. Post-harvest, oysters are subjected to

a practice called depuration. During depuration,

oysters are placed in tanks of clean seawater and al-

lowed 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 bioaccu-

mulation and depuration of NoV in oysters demon-

strates 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 se-

questering of the virus (Nappier et al., 2008; Schwab

et al., 1998; Ueki et al., 2007). Oysters may also un-

dergo 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 prac-

tices (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 effective-

ly (Chapman et al., 2010). Education and training,

positive incentives, and reinforcement from manag-

ers 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 precau-

tions 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 dur-

ing 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 system-

atic surveillance for human norovirus—only a select

number of bacterial and parasitic pathogens are ac-

tively monitored (Centers for Disease Control and

Prevention, 2010). Passive monitoring is primarily

due to the short duration and overall nature (i.e. non-

febrile, no bloody diarrhea) of illness caused by NoV

as well as the lack of routine clinical tests for NoV


available in hospitals. Therefore, NoV is usually diag-

nosed 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 contami-

nated foodstuffs may have in the spread of NoV. En-

hancing the capacity of state and local laboratories

would significantly increase our knowledge about

the prevalence of NoV and would help capture unre-

ported outbreaks due to NoV. In addition to moni-

toring 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 de-

cade by using techniques such as real time quantita-

tive RT-PCR as well as advanced methods for con-

centration 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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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, con-

taminated 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 suc-

cess 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

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, [email protected]: +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 patho-

gens leading to foodborne illnesses are caused

Norovirus, non-typhoidal Salmonella, Clostridium

perfringens, Campylobacter spp., and Staphylococ-

cus aureus (CDC, 2011). CDC also recently present-

ed specific foodborne illness statistics for the year

CONFERENCE PROCEEDINGS*Development and Assessment of Success for Retail Food Safety

Programming in IndianaR. H. Linton1

1Department 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




2007. In 2007, the most common “combined patho-

gen-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 fac-

tors identified from actual outbreaks are significant

issues in retail food safety and minimizing their im-

pact 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 re-

tail and foodservice segments of the food industry

(FDA, 2009). The FDA Food Code provides practical,

science-based guidance and manageable, enforce-

able provisions for mitigating risk factors known to

cause food-borne illness. The FDA Food Code is a

reference document for regulatory agencies that en-

sure 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 De-

partment 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 regula-

tory 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 informa-

tion in the FDA Food Code serves as the most uni-

form resource for developing education and train-

ing 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 man-

ager’s certification exams that are offered on the na-

tional 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 lead-

ing food safety programs with certifications that are

provided to the retail food industry.

The retail segment of the food flow chain is im-

portant from a food safety perspective for many rea-

sons. This is usually the last step in the flow of food

where ready to consume food is handled, and be-

cause 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-contam-

ination, effective cleaning and sanitation programs

and purchasing foods from an approved source

(CDC, 2011).

The state of Indiana has been a leader in develop-

ing and delivering retail food safety programming.

At a statewide level, Purdue University, Indiana Uni-

versity, the retail food industry, and state/local regu-

latory agencies have partnered together to promote

food safety education and provide a variety of pro-

grams intended for management and sub-manage-

ment level food handlers.

Retail food safety education programs are gen-

erally 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 rec-

ognized 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 re-

quirements, by state, can be found at www.retail-

foodsafety.org. or at http://www.nrfsp.com/state_

regulations/.


In Indiana, food retail protection manager certifi-

cation 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 educa-

tion 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 Coop-

erative Extension Service. The National Restaurant

Association’s ServSafe® program (NRA 2011) is tar-

geted for restaurant and food service operations. It

is offered as a 2-day training program, with the cer-

tification 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 train-

ing and exam format. Both of these programs are

directed toward food manager level personnel. Con-

tent 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. Anoth-

er program, called “Food Safety Day,” was devel-

oped 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 pro-

grams. As part of this journey, a needs assessment,

success on retail food protection manager’s certifica-

tion exams, positive changes in food handling be-

havior, and lessons learned will be described.


Food Safety Programming Needs Assessment

In 1998, a survey was created and distributed to

over 3,000 food safety-related stakeholders in the

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 con-

trol 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, regu-

latory agencies, academic institutions and other af-

filiated food safety-related organizations. The data

was then recorded and presented as percent posi-

tive response to each of the different programming

options.

Programming Statistics

Since 2000, for each food program that was of-

fered through Purdue University Cooperative Ex-

tension, 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 tabulat-

ed. Actual numbers were recorded for demographic

and experience questions, and, percentage of par-

ticipants was plotted against participant response

for the behavioral and training-based questions.

Demographic and Experience Questions

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 re-

sponses to each question.


1. My current job position is:

____ Chef or cook

____ Management

____ Server or wait staff

____ Other _____________

2. I have worked in food service:

____ Less than 1 year

____ 1 to 3 years

____ More than 3 years

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 in Food Safety Behavior Questions

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, poul-

try, 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 sani-

tized before preparing and serving foods.

For each question stated above, participants were

asked to answer as either “Yes”, “No”, “Sometimes,”

or “Already Doing.” Data were pooled and the mean

values and standard deviations were determined. Dif-

ferences between samples were determined using a

Student’s t-test, with Microsoft Excel (Microsoft Win-

dows XP), and were considered to be significant when

p<0.05.

Further Training Questions

Two additional questions were used to determine if

the food safety training had an impact on further train-

ing. These include:

1. I have conducted training in safe food han-

dling practices for staff.

2. I have received more training in safe food han-

dling practices.

For these two questions, participants were asked to

answer as either “Yes”, or “No.”

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

Scores and passing rates for national food protec-

tion manager’s certification were recorded over the

period of 2000-2010. Scores were obtained by the Edu-

cational Foundation of the National Restaurant Asso-

ciation (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. Re-

sults 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 un-

der “other.” More than 80% of respondents indi-

cated the need to retail food safety programs, fol-

lowed by 65%, 44%, and 28% indicating the need

for hazard analysis critical control programs, good


manufacturing practices and sanitation, and the

FDA better process control school. As it turns out,

the State of Indiana was in the process of approv-

ing mandatory retail food manager’s certification

statewide. The new law would require retail food

managers to pass an approved national certifica-

tion exam. While training was not required in the

new law, certainly statewide training would be

needed.

Demographic and Experience Ques-tions

Figure 1 provides information for the demograph-

ics and experience of the participants that have

been involved in all of the food safety training pro-

grams. 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

Chef or cook 25%Server or wait staff 11%Management 36%Other 28%

25%

11%

36%

28%

My current job position is:

Chef or cook Server or wait staff

Management Other

n= 15,819

Less than high school 7%Technical school or some college26%High school graduate or GED 49%College graduate or beyond 18%

7% 26%

49%

18%

My highest level of education is:

Less than high school

Technical school or some college

High school graduate or GED

College graduate or beyond

n= 15,819

a b

Less than 1 year 10%1 to 3 years 15%More than 3 years 75%

10% 15%

75%

I have worked in food service:

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

n= 15,819

African American 3%Hispanic 3%Asian 2%Other 2%Caucasian 90%

3% 3% 2% 2%

90%

My ethnic group is:

African American Hispanic Asian Other Caucasian

n= 15,819

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

c d


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

Yes 48Sometimes 25No 2Already Doing 15

0

10

20

30

40

50

60

% P

arti

cip

ants

"I or my staff washes hands more

frequently during food preparation and service."

Yes Sometimes No Already Doing

a

b

c

b

Participant Response


0 10 20 30 40 50 60 70

% P

arti

cip

ants

"I or my staff checks the temperature of food to make sure

that it is cooked to a safe temperature."


a

c d

b


a


0 10 20 30 40 50 60 70

% P

arti

cip

ants

"I or my staff takes the temperature of food to make sure that it has been cooled quickly to a safe

temperature."


a

c d

b


c


0

10

20

30

40

50

60

70

% P

arti

cip

ants

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

serving foods."


a

c c

b


e

b



0

10

20

30

40

50

60

70

% P

arti

cip

ants

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


a

c c

b

d


the participants had a high school graduate degree

or higher (Figure 1b) and have worked in the indus-

try for 3 or more years (Figure 1c). The ethnic group

identified in this survey was mostly Caucasian (Figure

1d).

Changes in Food Safety Behavior Questions

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 pro-

grams 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, cool-

ing, separation of raw from ready to eat (cross-con-

tamination 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

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 train-

ing, and 45% received further training in food safety.

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 certifi-

cation 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 ex-

ams 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 pro-

gramming. 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 stakehold-

ers. In Indiana, Purdue University formed a 3-way

partnership with academic institutions (Purdue Uni-

versity, Indiana University, Purdue University Coop-

erative Extension), food industry organizations (Indi-

ana Retail Grocers Association, Indiana Restaurant

and Hospitality Association) state regulatory agen-

cies (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.

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 Scores (%) Certified (%)

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 93

2008 1617 92.0 91.3

2009 1366 94.3 95.3

2010 2813 93.7 94.2

16,285 Ave = 93% Ave = 94%


• Develop an evaluation system that continually

allows you to improve your programs.

In Indiana, we have seen great increases in par-

ticipation 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 col-

lective passing rate is over 94% of national retail

food protection mangers certification exams. Partici-

pation in the Purdue University Food Safety Day pro-

gram 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 reaf-

firm 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 com-

petence has been met. In this program, we have also

shown that participants indicate positive changes

in food safety behavior and interest for more train-

ing opportunities. This really helps to demonstrate

overall programmatic impact. We are continuing to

develop better metrics that will help to clarify behav-

ioral changes. The next step is to visually observe ac-

tual changes in food handling practices within retail

food establishment settings and relate these obser-

vations 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 Retail-

Foodservice 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.retailfood-

safety.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 Mc-

Swane, 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 web-

based survey based instrument that was used to col-

lect 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 Out-

breaks: 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 Ill-

ness 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/FoodSafe-

ty/.

Food and Drug Administration (FDA). 2009. FDA

Food Code.

Food Marketing Institute (FMI). 2011. SafeMarkTM

http://fmi.org/.

http://www.fda.gov/Food/FoodSafety/RetailFood-

Protection/FoodCode/default.htm.




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

ConAgra Foods is a leading branded food com-

pany 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 packag-

ing.

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 partici-

pated in joint calls with the CDC, Food & Drug Ad-

ministration (FDA), United States Department of Ag-

riculture (USDA) and 10 states. ConAgra Foods then

held daily calls with the CDC to assist in its investiga-

tion 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

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

1 ConAgra Foods*Arkansas Association for Food Protection (AAFP) Conference, Enhancing Food Protection from Farm to Fork, held on



Correspondence: J. Menke-Schaenzer


Chicken and Rice meal and shut down production

and further distribution of the meal. Product sam-

ples 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 investiga-

tion, which included finished-product testing, en-

vironmental swabs, and component testing. More

than 1,500 finished-product tests were conducted.

Two tested positive for Salmonella. All environ-

mental 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 materi-

als. The associated product ingredient usage was

reviewed along with the ingredient usage percent-

age. The Certificates of Analysis (COAs) for the pre-

cooked chicken were all Salmonella negative. Fur-

ther 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 suc-

cessful collaboration among the many local, state,

and federal public health, agriculture, and regula-

tory agencies involved. The immediate action prob-

ably 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. Sup-

pliers followed strict, contractually mandated ad-

herence to regulatory requirements. The company

conducted unannounced audits and testing. Plants

followed and verified Good Manufacturing Practices.

ConAgra Foods also maintained strict Hazard Analy-

sis of Critical Control Points (HACCP) and COA veri-

fication 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 ex-

plore non-traditional testing and process control mi-

crobiology of finished product, in-process product,

and raw materials. Additionally, deeper investiga-

tions 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 safe-

ty 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 sup-

ported 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

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


at the forefront of its efforts. Testing is an essential

verification step to help prevent potential issues ear-

ly in the process, but supplier relationships, company

culture and communication both within and outside

the company also play critical roles in this area.




ABSTRACT

Food safety information is readily available in Spanish and to a lesser extent Chinese and other languag-

es. 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 pro-

grams 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 sig-

nificant relationships between perceived safety-communication barriers and food safety behaviors. In par-

ticular, 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 ser-

vice 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

InTRoduCTIon

Foodborne illnesses continue to be a public health

problem in the United States costing the food indus-

try billions of dollars annually. Health-related costs

from acute foodborne illness in the U.S. are estimat-

Received: August 31, 2011, Accepted: October 19, 2011. Released Online Advance Publication: July 1, 2011. Correspondence: Jay Neal, [email protected]: +1 -229-386-3363 Fax: +1-229-86-3239

ed to be $152 billion yearly (Scharff, 2010). CDC es-

timates that each year roughly 1 out of 6 Americans

(or 48 million people) get sick, 128,000 are hospital-

ized, 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

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 Col-lege, 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.



education is language barriers.

Difficulties due to language barriers are com-

mon in the food industry and are perceived to be

a major barrier to promoting U.S. food service stan-

dards 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 spe-

cifically, 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 (Jack-

son, 2008). The term “foreign-born” may include

legally-admitted immigrants, refugees, and tempo-

rary 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 con-

sistent 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 indi-

vidual’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; Kas-

senborg et al., 2004; Kassenborg 2004; Kimura et al.,

2004; Soble et al., 2000) however, the food service in-

dustry is making improvements (Scallan et al., 2011).

For example, between 1998 and 2008, significant im-

provements were made for poor personal hygiene

and improper holding/time and temperature risk

factors. These were reported with no significant re-

gressions for any of the foodborne illness risk factors

(Scallan et al., 2011). Much of this success can be at-

tributed 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 consis-

tent predictor for employee behaviors and food safe-

ty 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 commu-

nicate safe food handling procedures.

Food safety classes are offered in multiple lan-

guages such as Spanish or Chinese and are neces-

sary; however, many of these classes do not address

behaviors tempered by cultural upbringing (Niode

et al., 2011). Mitchell et al. (2007) reported that cul-

tural 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 employ-

ees believe that when they follow proper food safety

practices, both customers’ and managements’ sat-

isfaction 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) popula-

tion. 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 re-

lationships rather than on individual interests or con-


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 there-

fore 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 avail-

able 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.food-

safetyweb.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 re-

viewed 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 (La-

tinos, Chinese) and specific types of organizations

(delis, ethnic food restaurants). Much of this mate-

rial 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 knowl-

edge; (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 environ-

mental system: worksite physical conditions (Nieto-

Montenegro 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 lan-

guages, they are still responsible for implementing

the training programs and language barriers can be

problematic. Wilcock et al. (2011) reported that com-

municating 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 man-

agement techniques in directing culturally diverse

employees (Lee and Chon, 2000). For example, re-

search shows that immigrant workers are more likely

to be involved in workplace injuries than native work-

ers, 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 multilingual-

ism, 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 lan-

guage adds an important aspect to communicative

competence (Callahan, 2005).

Other challenges that managers face when teach-

ing food safety practices include working with a low-


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 na-

tive 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 be-

cause 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 effec-

tive.

Thus, the purpose of this study was to examine

the relationship between safety-communication bar-

riers and food safety behaviors; such as the number

of times participants washed their hands, checked

the temperature of the food, and avoided cross con-

tamination. In addition, the researchers examined

the perceived effectiveness of using nonverbal com-

munication and how this construct relates to per-

ceived safety-communication barriers in a context of

working in a kitchen where communication barriers

exist. This study sought to answer the following re-

search 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 set-

ting?

3. How effective are various types of nonverbal

behaviors in regard to the performance (tem-

poral performance, food quality, and food ac-

curacy)?

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

Communication Barriersa

Hand-washing

Check Temperature

No Cross Contamination

Nonverbal Behaviorsb

Safety Communication Barriersa

Pearson Correlation

1 -0.267** -0.210* -0.225* -0.367**

Sig. (2-tailed) 0.006 0.032 0.024 0.000

N 106 103 105 101 106

Handwashing Pearson Correlation

-0.267** 1 0.060 0.228* 0.221*

Sig. (2-tailed) 0.006 0.550 0.023 0.025

N 103 103 103 99 103

Check Temperature

Pearson Correlation

-0.210* 0.060 1 0.447** -0.037

Sig. (2-tailed) 0.032 0.550 0.000 0.706

N 105 103 105 101 105

No Cross Contamination

Pearson Correlation

-0.225* 0.228* 0.447** 1 -0.110

Sig. (2-tailed) 0.024 0.023 0.000 0.272

N 101 99 101 101 101

Nonverbal Behaviorsb

Pearson Correlation

-0.367** 0.221* -0.037 -0.110 1

Sig. (2-tailed) 0.000 0.025 0.706 0.272

N 106 103 105 101 106



Sample

One hundred and seven students (49% men and

51% women) at a four-year university majoring in ho-

tel 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 in-

dustry. Of the employed participants, 33% held a

management position. Additionally, 44% of the par-

ticipants reported “frequently” working with non-

English 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 communi-

cation 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 under-

stand English. The recipes and instructions provided

to the participants were in an abstract, non-English

language using Cyrillic letters (Figure 1). One partici-

pant from each group was assigned the role of man-

ager who was provided with the recipe and instruc-

tions 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 dis-

agree to (5) strongly agree. The scale had an alpha

reliability of .86.

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 (165οΦ) 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.


Sanitation behaviors were measured by using

definitions from the CDC’s identified risk factors for

foodborne illness as well as with WHO’s factors lead-

ing to foodborne illness (CDC 2009; WHO 2007). In

particular, the participants reported the number of

times they washed their hands, checked the temper-

ature 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 mea-

sured using a scale adopted from Dawson et al.

(2011). The scale included four items about the ef-

fectiveness of four nonverbal communication meth-

ods: gestures, demonstrating, pointing, and ap-

proval. 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) strong-

ly ineffective to (5) very effective. The scale had an

alpha reliability of 0.77.

ReSulTS

Correlations were used to examine the relation-

ships between perceived safety-communication bar-

riers, sanitation behaviors, and perceived nonverbal

communication effectiveness. The analyses showed

significant relationships between perceived safety-

communication barriers and the food safety behav-

iors. 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-communica-

tion barriers were significantly related to perceived

nonverbal communication. The less effective the

participants’ perceived their nonverbal communica-

tion 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 wash-

ing (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 point-

ing (36%), followed by demonstrating (9%), touching

(6%), and eye contact (3%). In order to provide feed-

back 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 mem-

bers’ 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. How-

ever, by knowing where the communication bar-

riers exist and how to compensate for these barri-

ers, 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 ex-

isted.

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 equip-

ment as the most frequent cause. The food service

industry leads the number of workplace injuries, ac-

counting 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


injuries occurred in food preparation areas.

These results can be applied directly to constructs

two and five of the Health Action Model which in-

clude: normative system (worksite norms and rules)

and worksite environmental system (worksite physi-

cal 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 safe-

ty practices may be incorporated and help create a

safe and healthy work environment that includes a

multi-lingual workforce. One possible solution food-

service 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 employ-

ees 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 environ-

ment itself can be altered to communicate non-ver-

bally potential risks and therefore, possibly change

employee behavior.

The second most frequent issue participants’ re-

ported related to cross-contamination and instruc-

tions 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 food-

borne 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 identify-

ing “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 tak-

ing a temperature to ensure a Critical Control Point

has been met. Based on HACCP principles, “Criti-

cal Control Actions” can be identified within Critical

Control Points of a HACCP system and allow man-

agers 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 wash-

ing 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 com-

mon non-verbal communication methods, whereby

gestures that demonstrate actions are most effec-

tive 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 communi-

cation (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-Eng-

lish 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 is-

sues with a sample of non-English speakers. Further

studies might also examine the methods and tech-

niques that managers use to communicate with non-

English speaking employees.

Not only do food service managers need to ad-

dress 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 effec-

tiveness of “zoning” for food safety and using Criti-

cal Control Actions should be conducted.

In the current study, gestures, pointing, and dem-

onstrating 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 dif-

ferent types of workers in the U.S. workforce is cre-


ating a multicultural urgency for managers (Testa,

2007). Given the increasing number of immigrants in

the food service industry (NRA, 2006); this research

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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).

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other countries among other languages and cultural

norms. Given the increasing number of immigrants

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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 an-

nounced 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 mini-

mally cooked. For physical control methods, heating is the most common method employed but irradia-

tion 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 effec-

tive 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 pro-

file 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

FoodBoRne PAThoGenS

Contamination of pathogen in food prod-

ucts has been a constant concern for humans due to

severe health threats and economical loss. Annually,

9.4 million illnesses are caused by foodborne patho-

Released Online Advance Publication: July 1, 2011. Correspondence: Steven C. Ricke, [email protected]: +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%) peo-

ple are infected by norovirus and the second highest

is 1.0 million illness (11%) by nontyphoidal Salmonel-

la spp (Scallan et al., 2011). Nontyphoidal Salmonel-

la 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.,

CONFERENCE PROCEEDINGS*- REVIEWPhysical and Chemical Control of Salmonella in Ready-To-Eat Products

O. K. Koo1, S. A. Sirsat2, P. G. Crandall1 and S. C. Ricke1

1 Center for Food Safety, Dept. of Food Science, University of Arkansas, Fayetteville, AR 727042 Conrad N. Hilton College of Hotel and Restaurant Management, University of Houston, Houston, TX 77204-3028

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



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 con-

tamination 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; how-

ever 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). Salmo-

nella can cause systemic disease by invading intes-

tinal cells, and subsequently be transported to liver,

spleen and mesenteric lymph nodes. The pathogen

further causes neutrophil infiltration, tissue injury, flu-

id accumulation and diarrhea (Bhunia, 2008). A sep-

tic 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 in-

creasingly 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 food-

safety concern, since consumers eat the products

without further cooking. Without any proper pro-

cess to eliminate foodborne pathogens, the patho-

gens in the contaminated food product will be able

to survive and grow during storage. Contamination

can occur during packaging or further processing af-

ter 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 patho-

gen 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 im-

munocompromised and pregnant women by caus-

ing spontaneous abortion (Lecuit, 2007). There have

been several outbreaks due to listeriosis; delicates-

sen 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 contamina-

tion in RTE products. For instance, salami contami-

nated 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 investiga-

tion revealed that the contamination occurred after

the salami underwent lethality steps, the raw ingre-

dients (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


score for both high and low risk population, while

L. monocytogenes exhibited a high-risk score mostly

for high-risk population such as immuno-compro-

mised individuals (Matargas et al., 2008).

Recently, USDA-FSIS released updated informa-

tion on the Salmonella compliance guide for small

plants on RTE meat products (USDA-FSIS, 2011).

USDA-FSIS tests for Salmonella positive RTE prod-

ucts using two test programs; the random testing

program and the risk-based testing program. Half

of all positive products were found to be from head-

cheese, pork barbecue, and sausage products. The

source of contamination in pork barbeque could be

either from the meat or the sauce which raw ingre-

dients were mixed with. Even though the incidence

of Salmonella contamination is lower than L. mono-

cytogenes, Salmonella contamination can be indica-

tive of not only under-processing but also serious

deficiencies in sanitary practices. For the production

of RTE meat products, USDA-FSIS requires Salmo-

nella 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 ful-

ly cooked poultry products (9 CFR 381.150) (USDA-

FSIS, 1999). For other types of RTE meat products

such as cooked meat patties, dried, fermented sau-

sages, 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 atten-

tion 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 approximate-

ly 1400-reported illness due to Salmonella. Specifi-

cally the peppers were contaminated with S. Saint-

paul (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 per-

sistence 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 pea-

nut butter caused illness in 628 persons in 47 states

(during 2006-2007) due to S. Tennessee contamina-

tion (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 dur-

ing cooking (CDC, 2008). A savory snack imported

from Israel in 1994 to 1995 was implicated in a S. ag-

ona outbreak affected young children in the US and

UK (Killalea et al., 1996). Tainted German chocolates

resulted in 439 cases due to S. Oranienburg con-

tamination 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 patho-

gens 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 ef-

ficient 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 spoil-

age and pathogenic bacteria is reduced. However,


some bacteria such as L. monocytogenes and Yer-

sinia enterocolitica can survive at 1°C. In these cas-

es, 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 inacti-

vation of target bacteria varies based on strain, food

product, and environmental factors (Doyle and Beu-

chat, 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 micro-

organisms in foods (Gould, 2000). Trials performed

using hot water on poultry carcass have been shown

to reduce Salmonella numbers substantially (Morri-

son et al. 1985). The use of hot water as a hurdle is

based on the principle of increasing the surface tem-

perature of the carcass. For instance, dipping meat

samples in 95°C hot water for 3 s increased the sur-

face 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 result-

ed in less than 1 log cycle reduction in the total mi-

croflora 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 bac-

teria from heat treatment. Osaili and others (2007)

performed thermal inactivation experiments (at 55 to

70ºC) on E. coli O157:H7, Salmonella, and L. monocy-

togenes in breaded pork patties. The study showed

that salts added to the product enabled water mol-

ecules to bind and caused poor heat penetration for

bacteria to survive in the product. In addition, the

breading ingredients, which consist mostly of carbo-

hydrates 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 re-

duction of E. coli O157:H7, Salmonella, and L. mono-

cytogenes, 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 le-

thality 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 de-

pending on the food ingredients to kill target bac-

teria.

Thermal resistance can also be different between

whole-muscle and ground meat. A Salmonella cock-

tail 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. Ther-

mal resistance can increase significantly by lower wa-

ter 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 inac-

tivate microorganisms mostly at ambient tempera-

tures. 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


discharges are routinely used to inactivate bacteria,

yeast, and molds in foods. This method has been

used for jams, juices, avocado dip, and salad dress-

ings 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 tech-

nology has proven to be able to inactivate vegeta-

tive 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 thy-

mine 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 popula-

tion (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 exam-

ined 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 grape-

fruit.

There have been limited studies on the nonthermal

processing to inactivate Salmonella in RTE products

and most of these studies were focused on irradia-

tion. Studies in RTE products such as carrot, cucum-

ber, sprouts and pineapple have demonstrated that 2

kGy of radiation worked effectively to reduce Salmo-

nella 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 ra-

diation 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 in-

volved 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 sau-

sages to inactivate S. Enteritidis and S. Typhimurium

without any sensory change. At 1 kGy, the odor and

taste did not exhibit detectable differences when com-

pared with untreated sausages, however off-odors and

off-taste increased significantly at 2 and 3 kGy. Mean-

while, color change occurred especially on the redness,

which was reduced significantly due to the production

of heme-pigment with carbon monoxide ligand forma-

tion, and the lightness increased while yellowness was

not affected. Also the off-color by irradiation could in-

crease 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. para-

haemolyticus were 1.1, 1.3, 1.2 and 1.2 kGy, respective-

ly. 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. parahae-

molyticus, respectively. Overall results demonstrated

that S. enterica had stronger resistance to X-ray treat-

ment than other pathogens (Mahmoud, 2009).

ChemICAl ConTRol on RTe

Chemical methods include use of organic acids,


salts, chlorine, spices, or oils. Organic acids, which

are generally recognized as safe (GRAS), are the

most common method to control the growth of mi-

croorganisms in foods. In the meat industry, chemi-

cals 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 environ-

ment, 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, sal-

ads 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 concen-

tration of 2 to 4%. Studies have been conducted us-

ing 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. Typhimuri-

um exhibited 2.0 to 2.4 log cycles and 1.6 to 1.9 log

cycles reduction after postchill acid treatment (Cas-

tillo et al., 2001). Min and Yoon treated potassium

lactate (PL) and sodium diacetate (SDA) to reduce S.

Typhimurium and Staphylococcus aureus and evalu-

ated 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-re-

sistant bacteria due to use of organic acids as well

as the disposal of the wastewater for environmental

reasons (Dickens et al., 1994; Dickens and Whitte-

more, 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 en-

zymes to prevent normal functioning of the cell (Lil-

lard, 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 am-

monium 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 ex-

tremely 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. Typhimuri-

um attached to chicken skin (Kim et al. 1994). The

results demonstrated that TSP was successful in re-

ducing 2 log CFU/cm2 Salmonella. It has been sug-

gested 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 in-

terest 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 activ-

ity against Gram-negative organisms. EOs have

hydroxyl groups and allylic side chains, which may


increase the antimicrobial effect on Salmonella con-

taminated iceberg lettuce and carrots. Oregano and

thyme also showed the strongest antimicrobial activ-

ity 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). Minimal-

ly processed fruits and vegetables are required pro-

tection 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 re-

duction (Belletti et al., 2008).

In general, EOs have an organoleptic impact on

food products. However, citron did not cause un-

desirable 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 ter-

penes 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 ter-

peneless Valencia orange oil was effective against E.

coli O157:H7 and L. monocytogenes but not against

Salmonella (Friedly et al., 2009). Studies on EO indi-

cates that further investigation is required to find a

suitable EO at an appropriate concentration against

Salmonella that will not negatively impact the organ-

oleptic properties of the product.

Chemical antimicrobial methods are often com-

bined with other control methods including biologi-

cal 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 com-

pound, ρ-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 antimi-

crobial effects by individual compound, however

with a minimal concentration of 0.3 ppm of nisin and

2.5 ppm of ρ-cymene, it was able to eliminate the

pathogens at 4°C (Rattanachaikunsopon and Phum-

khachorn, 2010).

Nisin is a bacteriocin that is mostly effective

against Gram-positive bacteria. However when

combined with a chelating agent such as ethyl-

enediamine tetraacetic acid (EDTA), it can increase

the antimicrobial efficiency against Gram-negative

bacteria. Synergistic effects of whey protein iso-

late 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 reduc-

tion of S. Typhimurium. The combination showed an

additive rather than synergistic effect on Salmonella.

The treatments were more effective against L. mono-

cytogenes 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 com-

pounds (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 com-

bined 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 im-

portant approach to consider. Sequential sublethal

stress treatments cause the target microorganism to


face the challenge of a hostile environment leading

to metabolic exhaustion and death. Hurdle technol-

ogy can target a single function of a microbial cell

such as cell membrane, DNA, pH, and water activ-

ity 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 abil-

ity 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 bio-

logical 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 un-

der 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 patho-

gens during storage up to 8 weeks at 9°C (Sommers

et al., 2003). Milillo and others investigated the com-

binational 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 syn-

ergistic reduction was primarily caused by cell mem-

brane 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 under-

stand 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 identify-

ing 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 na-

lidixic acid and evaluated differential regulation of

SPI-1 and 2 and induction of multidrug resistance ef-

flux 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 (Alva-

rez et al., 2003) as well as real-time PCR for detect-

ing 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 pro-

cessing the product. Therefore, proper handling

practices are required to minimize any cross-contam-

ination and for the safe consumption after purchase.

It is important for the workers in the processing plant

to apply the appropriate sanitary practices. Patho-

gens can easily be transmitted by food workers, es-

pecially 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 dis-

cussed. Antimicrobial agent coated packages may

also be a great strategy to protect the RTE product

from post-processing contamination. However, bac-


terial resistance against antimicrobial agents and

cross-protection against different hurdle treatment

are also an increasing issue since this may limit han-

dling 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 bacte-

rial resistance for individual control methods. Future

research should focus on developing strategies such

as genomic screening to design optimal multi-hur-

dle conditions to lower the potential growth of Sal-

monella in RTE food.

ACknoWledGemenTS

This review was supported by National Integrated

Food Safety Initiative grants (NIFSI) (2008-51110-

04339) to S. C. Ricke and to P. G. Crandall (2010-

51110-21004) and a USDA Food Safety Consortium

grant to S. C. Ricke.

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sponsibility for errors that result in the final publication.

PuBlICATIon ChARGeS

AFAB has two publication charge options: conven-

tional 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 com-

munication, 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 quan-

tity 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.


mAnuSCRIPT ConTenT ReQuIRemenTS

Preparing the Manuscript File

Manuscripts must be written in grammatically

correct English. AFAB offers a fee based language

service upon request ([email protected]).

Manuscripts should be typed double-spaced, with

lines and pages numbered consecutively. All docu-

ments 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 sym-

bols 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 fol-

low these instructions will cause delays of the pro-

cessing 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 abbre-

viations 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 cor-

responding author should be indicated with an aster-

isk e.g., * Corresponding author. The title page shall

include the name and full address of the correspond-

ing author. Telephone and e-mail address must also

be provided for the corresponding author, and email-addresses must be provided for all authors.

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 au-

thors may need to provide a list of abbreviations

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 ta-

bles, 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 sepa-

rate page after the title page. The abstract should

provide a justification of your work, objectives, meth-

ods, results, discussion and implications of study or

review findings . Your abstract must consist of com-

plete 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 index-

ing. Ideally, these keywords should include signifi-

cant words from the title.

Introduction

The introduction should clearly present the foun-

dation 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 ob-

jectives must be clearly stated in the final sentence

of the last paragraphs of the introduction.

Materials and Methods

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)].


Variability, Replication, and Statistical Analysis

To properly assess biological systems indepen-

dent 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 com-

monly 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 experimen-

tal unit is the smallest unit to which an individual

treatment is imposed. For bacterial growth stud-

ies, 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. Mea-

surements on the same experimental unit over time

are also not independent and must not be consid-

ered as independent experimental units. For analy-

sis 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.

DiscussionThe 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 re-

viewed shall have authors’ institutions omitted to re-

tain anonymity.

References

a) Citing References In Text

Authors of cited papers in the text are to be pre-

sented 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 pa-

rentheses, 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 alphabeti-

cally 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 un-

published work should be listed in the text as “(J.

Adams, unpublished data).” Personal communica-

tions 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 ci-

tations designated by et al. in the text have the same

first author, then even if the other authors are differ-

ent these references in the text and the references

section must be identified by a letter. For example


“(James et al., 2010a,b)” in text, refers to “James,

Smith, and Elliot. 2010a” and “James, West, and Ad-

ams. 2010b” in the reference section.

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 refer-

ence section followed by the designation: “(submit-

ted)”, “(accepted)’, or “(In Press), respectively. If the

DOI number of unpublished references is available,

you must give the number. The year of publication fol-

lows the authors’ names. All authors’ names must be

included in the citation in the Reference section. Jour-

nals must be abbreviated. First and last page num-

bers must be provided. Sample references are given

below. Consult recent issues of AFAB for examples

not included in the following section.

Journal manuscript:

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:

Hungate, R. E. 1966. The rumen and its microbes.

Academic Press, Inc., New York, NY. 533 p.

Book 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:

Maciorowski, K. G. 2000. Rapid detection of Salmo-

nella 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 Salmo-

nella in laying hens. M.S. thesis. Texas A&M Uni-

versity, College Station, TX.

Van Loo, E. 2009. Consumer perception of ready-to-

eat deli foods and organic meat. M.S. thesis. Uni-

versity 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.

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

Patent #_____

Author(s). Year. Article title. Journal title [abbreviated].

Volume number:inclusive pages.

Author(s) [or editor(s)]. Year. Title. Edition or volume (if

relevant). Publisher name, Place of publication. Number

of pages.

Author(s) of the chapter. Year. Title of the chapter. In:

author(s) or editor(s). Title of the book. Edition or vol-

ume, if relevant. Publisher name, Place of publication.

Inclusive pages of chapter.

Author. Date of degree. Title. Type of publication, such

as Ph.D. Diss or M.S. thesis. Institution, Place of institu-

tion. Total number of pages.


Abstracts and Symposia Proceedings:

Fischer, J. R. 2007. Building a prosperous future in

which agriculture uses and produces energy effi-

ciently 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 experi-

mental 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 sub-

mit 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 com-

parison 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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