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Analysis and Evaluation of Preventive

Control Measures for the Control and
Reduction/Elimination of Microbial Hazards
on Fresh and Fresh-Cut Produce Executive
Summary
Table of Contents
(/7993/20170111183942/http://www.fda.gov/Food/FoodScienceResearch/SafePracticesforFoodProcesses/ucm
090977.htm)

Preface
Science Advisory Board
Scientific and Technical Panel
Reviewers
Additional Credits
Background
Current Status
Scope of Work
Executive Summary 

Preface
On September 30, 1998, the Food and Drug Administration (FDA) of the U.S. Department of Health and Human
Services signed a five-year contract with the Institute of Food Technologists (IFT) to provide scientific review and
analysis of issues in food safety, food processing and human health. Under the terms of the contract, FDA assigns
IFT task orders, which are categorized either as comprehensive or abbreviated reviews. IFT assembles Scientific and
Technical Panels comprised of experts in the topic area to address the assignment. The panels are charged with
providing scientific and technical review and analysis, but are not involved with setting policy.
This report is IFT's response to Task Order No. 3: Analysis and Evaluation of Preventive Control Measures for the
Control and Reduction/Elimination of Microbial Hazards on Fresh and Fresh-Cut Produce. The Background and
Scope of Work that FDA provided to IFT are included on the following pages. In October 1999, IFT assembled a
Scientific and Technical Panel comprised of food microbiology experts from government, academia, and industry. The
panel met in person and via conference calls throughout October 1999 and September 2001. IFT also assembled a
Science Advisory Board to advise IFT on the FDA contract and on the individual task orders.

The Institute of Food Technologists greatly appreciates the efforts of the Scientific and Technical Panels, the Science
Advisory Board, the many reviewers, staff and others who made this report possible. Compensation for such an effort
pales in comparison to the time, effort, and expertise expended. IFT is especially grateful to the FDA staff for their
cooperation, communication, and assistance at every stage of this project. IFT submits this report to make a
contribution to the understanding of microbiological safety aspects of fresh fruits and vegetables. 

Science Advisory Board

Roy G. Arnold, Ph.D.
Executive Associate Dean
College of Agricultural Science
Oregon State University

Lester M. Crawford, Ph.D., D.V.M.

Director
Center for Food and Nutrition Policy
Virginia Polytechnic Institute and State University

Ray A. Goldberg
George M. Moffett Professor of Agriculture
and Business Emeritus
Harvard Business School

Marcus Karel, Ph.D.

Professor Emeritus
Massachusetts Institute of Technology
and Rutgers University

Sanford A. Miller, Ph.D.

Adjunct Professor
Center for Food and Nutrition Policy
Virginia Polytechnic Institute and State University

Martha Rhodes Roberts, Ph.D.

Deputy Commissioner for Food Safety
Dept. of Agriculture
and Consumer Services State of Florida

G. Edward Schuh, Ph.D.

Freeman Chair Professor
Hubert H. Humphrey Institute of Public Affairs
University of Minnesota
Barbara O. Schneeman, Ph.D.
Professor of Nutrition
Department of Nutrition
University of California 

Institute of Food Technologists

Scientific and Technical Panel
Frank F. Busta, Ph.D.
Panel Chair and Senior Science Advisor
to the Institute of Food Technologists
University of Minnesota

Larry R. Beuchat, Ph.D.

University of Georgia

Jeffrey N. Farber, Ph.D.

Health Canada

Edith H. Garrett, M.S.

International Fresh-Cut Produce

Linda J. Harris, Ph.D.

University of California

Mickey E. Parish, Ph.D.

University of Florida

Trevor V. Suslow, Ph.D.

University of California, Davis 

Reviewers
Jerry Bartz
University of Florida

Laurence D. Bell
Fresh Express Fresh Foods

P.J. Blagoyevich
The HACCP Institute of Food Technologists

Fred Breidt, Jr. United States Dept. of Agriculture

Agriculture Research Service

Bruce Cords Ecolab Research Center

Dean O. Cliver
University of California, Davis

Frank J. Dainello
Texas A & M University
Michael P. Doyle
University of Georgia

Eduardo Fernandez Escartin

Centro Universitario
Queretaro, Mexico

Gillian A. Francis
University of Limerick
Ireland

Joseph F. Frank
University of Georgia

Gillian Heard
University New South Wales
Australia

Craig Hedberg
University of Minnesota

Joseph H. Hotchkiss
Cornell University

William Hurst
University of Georgia

Eric Johnson
University of Wisconsin

Thomas Montville
Rutgers -- The State University
Cook College

Nancy E. Nagle
Nagle Resources

Christopher Nguyen-the
Institute Nationale de la Recherche Agronomique, France

Steven Pao
University of Florida

Charles A. Pettigrew
The Procter & Gamble Company

Gerald M. Sapers
United States Dept. of Agriculture

Robert V. Tauxe
Centers for Disease Control and Prevension
Al B. Wagner, Jr.
Texas A & M University

Randy W. Worobo
New York State Agricultural
Experiment Station 

Additional Credits
Consultants

Scott Brooks
Taco Bell Corporation

Joan Rosen
Fresh Express Fresh Food

Mahipal R. Kunduru, Ph.D.

Fresh Vegetables, Inc.

James Roman Gorny, Ph.D.

International Fresh-Cut Produce Association 

Food and Drug Administration

Donald M. Kautter, Jr.
Contract Technical Officer
Division of HACCP Programs

 
Ed Arnold
Contracting Officer

Joyce Saltsman
Consumer Safety Officer

Institute of Food Technologists

Bruce R. Stillings, Ph.D.
1998-1999 President

Charles E. Manley, Ph.D.

1999-2000 President

Mary K. Schmidl, Ph.D.

2000-2001 President

Phillip E. Nelson, Ph.D.

2001-2002 President

Mark McLellan, Ph.D.

2002-2003 President Elect
Daniel E. Weber
Executive Vice President

Fred R. Shank, Ph.D.

Vice President, Science, Communications
and Government Relations

Jill A. Snowdon, Ph.D.

Director, Department of Science
and Technology Projects

Maria P. Oria, Ph.D.

Staff Scientist

Karen Arcamonte, M.S.

Information Specialist

Kendra Langeteig, Ph.D.

Administrative Assistant  

Background (Provided by FDA to IFT)

Fresh fruits and vegetables are important to the health and well being of the American consumer. Consumers enjoy
one of the safest supplies of fresh produce in the world. However, over the last several years, the detection of
outbreaks of foodborne illness associated with both domestic and imported fresh fruits and vegetables has increased.
In a January 1997 radio address, President Clinton announced a Food Safety Initiative to improve the safety of the
nation's food supply from farm-to-table. In May of 1997, as part of the President's Food Safety Initiative, the
Department of Health and Human Services, the U.S. Department of Agriculture, and the Environmental Protection
Agency sent to the President a report that identified produce as an area of concern. In October 1997, President
Clinton announced a plan entitled "Initiative to Ensure the Safety of Imported and Domestic Fruits and Vegetables"
(produce safety initiative) to provide further assurance that fruits and vegetables consumed by Americans, whether
grown domestically or imported from other countries, meet the highest health and safety standards.

Most fresh fruits and vegetables are grown in fields and orchards that are non-sterile environments. Growers have
less control over conditions in the field compared to an enclosed processing facility. The surfaces of produce have a
microflora which is generally composed of microorganisms that are not of human health significance. Occasionally,
low level, sporadic contamination of produce with human pathogens may occur. Usually, such contamination is not of
public health significance. For example, the pathogen may not survive until harvest, harvest workers may be
instructed to avoid harvesting produce with obvious contamination, such as bird droppings, or post-harvest
treatments, such as washing, cooking or peeling, may remove or inactivate pathogens. However, the processes
involved in further commercial manipulation (e.g. washing, cutting, slicing, packaging) of fresh produce offer
additional opportunities for product to become contaminated with pathogens or for pathogens on products to grow.

Although the incidence of foodborne illness linked to fresh produce is still low, there is evidence that it is increasing.
Fresh produce is of special concern because it is likely to be consumed raw, without any type of microbiologically
lethal processing. According to the Centers for Disease Control and Prevention (CDC), the number of reported
produce-related outbreaks per year doubled between the period 1983-l987 and 1988-1992, when illnesses due to
botulism and mushrooms and "salad" were excluded. Substantial increases in produce-related human illness were
also observed in 1995. Outbreak data linked Salmonella Stanley with alfalfa sprouts, Salmonella Hartford with orange
juice, Shigella spp. With lettuce and scallions, Escherichia coli O157:H7 with lettuce varieties, and hepatitis A virus
with tomatoes. More recently, there have been outbreaks linking Cryptosporidium with unpasteurized apple cider,
Cyclospora with raspberries, mesclun lettuce and basil/basil-containing products, E. coli 0157:117 with unpasteurized
apple cider and alfalfa/clover sprouts, hepatitis A virus in sliced, frozen strawberries, Salmonella Muenchen in orange
juice, and Salmonella spp. with clover and alfalfa sprouts. These are only limited examples of identified outbreaks
associated with fresh and minimally processed produce; a more comprehensive review of microbiological hazards
associated with produce can be found in a manuscript entitled "Microbiological safety evaluations and
recommendations on fresh produce" produced by the National Advisory Committee on Microbiological Criteria for
Foods (Food Control, 10, 1999).  

Current Status
In response to the produce safety initiative, FDA and USDA have issued guidance on good agricultural practices
(GAPs) for the produce industry. The guidance document, entitled "Guidance for Industry -- Guide to Minimize
Microbial Food Safety Hazards for Fresh Fruits and Vegetables," addresses microbial food safety hazards and good
agricultural and management practices common to the growing, harvesting, washing, sorting, packing, and
transporting of most fruits and vegetables sold to consumers in an unprocessed or minimally processed (raw) form.
The produce guide is guidance and not a regulation.

The guide is one of the first steps under the President's produce safety initiative to improve the safety of whole and
fresh-cut produce as it moves from the farm to the table. The guide focuses on the production and packing of fresh
produce.

FDA plans to issue specific guidance for certain raw agricultural products, such as sprouts, for which there is
particular concern due to an increasing number of associated outbreaks. In addition, HACCP systems may be
considered for intact and fresh-cut produce when sufficient information and data has been gathered to establish
appropriate preventive control measures. The International Fresh-Cut Produce Association (IFPA) defines fresh-cut
produce as "fruits or vegetables that have been trimmed and/or peeled and/or cut into 100% usable product that is
bagged or prepackaged to offer consumers high nutrition, convenience and value while still maintaining its
freshness."

In response to outbreaks of illness associated with juice products, FDA issues proposed procedures for safe and
sanitary processing in the manufacture of fruit and vegetable juices that were published in the Federal Register (April
24, 1998). The proposed rule would require that firms use HACCP systems for juice production. The same document
also proposed label warning statements for juices that have not been processed in a manner to achieve a 5-log
reduction in a pertinent pathogen. This rule was finalized in July 1998 (63 FR 3703 1) and was effective September
1998 for apple juice and November 1998 for other juice.  

Scope of Work (As Assigned by FDA to IFT)

Independently and not as an agent of the Government, the Contractor shall furnish the necessary materials, services,
facilities, and otherwise do all things necessary for or incident to the performance of the work set forth herein.

The Contractor shall (1) review the scientific literature, (2) consult with academic experts, and (3) consider the
requirements of other governmental bodies to address the following:

1. The Contractor shall do an in depth review of the production parameters that may contribute to pathogen
contamination of produce and fresh-cut produce. Particular attention shall be given to possible contamination
from 1) agricultural water (water used in the growing environment, such as irrigation water) and processing water
(water used for postharvest treatment of water, such as washing, cooling, waxing, and product transport), 2)
manure, biosolids, and animal feces, 3) rodents, insects, birds, and dirt in the processing environment, 4)
contributions of worker health and hygiene, including sanitary facilities, 5) poor field sanitation, and 6) conditions
at the packing facility and/or during transportation.
 2. The Contractor shall provide information on state and local restrictions or requirements on any of the
aforementioned production parameters, such as restrictions on the use of biosolids, or on state and local statutes
that may increase the likelihood of contamination, such as programs to increase the use of manure as a fertilizer.
3. The Contractor shall provide information on the pathogens that are of particular concern on produce and fresh-
cut produce (e.g., Shigella, Salmonella, E. coli, Listeria, Cyclospora, Cryptosporidium, Hepatitis A virus, etc.).
This information shall include product/pathogen interactions and information regarding particular locations on
plants that are most susceptible to contamination or plant characteristics that favor pathogen attachment,
internalization, entrapment and survival.
4. The Contractor shall perform a detailed review of information regarding the presence, incidence, survival and
growth of pathogens on post-harvest whole and fresh-cut produce. This information should include antimicrobial
properties of produce, environmental conditions that are most conducive to pathogen survival and growth,
pathogen internalization by intact or cut produce, and, with regard to fresh-cut produce, the growth and survival
of pathogens on or in the cut tissue.
5. The Contractor shall provide information on various methods of eliminating or reducing pathogens, while
maintaining fresh attributes, on whole and fresh-cut produce, including but not limited to the following:

a. treatments such as chlorine, ozone, organic acids, phosphates, irradiation (ultraviolet, gamma, etc.),
essential oils, plant pigments, detergents, physical removal (e.g., brushing, peeling), steam and
disinfectants. The contractor shall review how these treatments work, optimization of treatment conditions,
their effectiveness, limitations in use (temperature, pH, redox interactions), equipment/methods for
monitoring (e.g., active chlorine levels) to ensure treatment efficiency at the start of, and throughout,
treatment processes and cost/benefit information.
b. Packaging technologies, including modified atmosphere packaging (MAP) and controlled atmosphere
packaging (CAP) and any pertinent information on film types and film properties. This information should
include any additional pathogen risk incurred through use of packaging technologies (i.e., a modified
atmosphere that discourages survival/growth of some microorganisms (e.g., spoilage organisms), but that
may provide a suitable environment for survival/growth of pathogens). In addition, information shall be
provided on the use of cooling and storage to control pathogens on produce and availability of special
equipment of ruse during harvest and processing that would minimize microbial food safety hazards.
6. The Contractor shall provide information on which organisms of public health concern are the most resistant to
the treatments identified in Number 5.
7. For the technologies discussed in Number 5, the Contractor shall provide additional information on the suitability
of these technologies for use by large versus small businesses and barriers to the use of these technologies
(e.g., process approvals, loss of "organic" certification, consumer acceptance, etc.).
8. For purposes of validating the effectiveness of any of the above mentioned treatments, the Contractor shall
review indicator organisms that could be used to determine treatment effectiveness. This review shall consider
both surrogate organisms and naturally occurring microflora and the conditions under which they would be
appropriate for particular pathogens.  

Executive Summary
Over the last several years, there has been an increased concern about the microbiological safety of the world food
supply. As a reflection of this concern, new research and testing programs have been initiated in both domestic and
international arenas. International organizations, such as the World Health Organization, have declared food safety a
top priority. The control of microbiological hazards to protect public health has become a major area of focus for all
food regulatory agencies in the United States. There are a number of food products that are particularly vulnerable to
the contamination and subsequent survival and/or growth of microorganisms and could result in foodborne disease.
Among them are fresh and fresh-cut fruits and vegetables. Reasons for the risk of foodborne disease associated with
these foods include an increase in the consumption of fresh produce, changing global and domestic distribution
systems, lack of a processing step to eliminate pathogens and lack of systematic controls to prevent the presence of
pathogens in fruits and vegetables. Recognition of the need to evaluate factors affecting the safety of fresh and fresh-
cut produce by the regulatory, private sector, and academic community has resulted in a wealth of research data and
training programs and guidance for the industry. This report focuses mainly on: the status of the problem, such as
number of outbreaks, incidence of pathogens, and ability of pathogens to survive/growth (Chapter IV); research
activities to better understand the source of microbiological contamination (Chapter II); methods to minimize the
presence of pathogens and their growth in produce (Chapter V); effects of new technologies, such as packaging
methods on safety (Chapter VI); the economic impact of implementing methods to control pathogens (Chapter I); the
need for standardization of methods for determining the effectiveness of antimicrobials (Chapter III); and the role of
indicator and surrogate organisms to understand the behavior of pathogens during the production, processing and
storage of fruits and vegetables (Chapter VII).

Chapter 1. A complicating factor in determining the economics of produce safety systems is the diversity in business
models currently used. Large produce companies may be completely vertically integrated enterprises to include
growers (farmland owners or lessors)/shippers/processors completely in control of all aspects of production,
marketing and distribution. Other companies may simply grow specific crops and sell them to a marketer or distributor
who in turn sells to foodservice or retail accounts. Or a marketer/distributor may not grow any of the crops that they
market and distribute, but may own the label or brand and the packinghouse in which the products are packed in.

Like produce farms, packinghouse operations are not always controlled by large corporations that may have the
resources to apply effective safety procedures. Co-ops or commodity groups representing a group of small farmers
may not have the same level of resources as a corporation, yet they operate packing systems for many commodities.
Packinghouse operations are designed to preserve and package produce commodities and are currently included
under the Good Agricultural Practices (GAP) guidelines but exempted from the Good Manufacturing Practices (GMP)
regulations. Irrespective of the size of operation, food safety programs must be implemented at all packinghouses.

In an attempt to reduce liability, some buyers are promoting strict safety expectations through purchasing
specifications and third party audit requirements for their suppliers before any standards have been identified and
tested for effectiveness. These requirements continue to drive the supply side of the produce industry to seek proper
safety programs but the industry needs more scientific answers to reduce risk. Effective steps for reducing
contamination can be implemented throughout the distribution system through cooperation between each segment of
the supply chain.

In the next decade, mid-sized and large companies in the produce industry may experience unprecedented growth
through consolidation; mergers will continue to be one way to attempt to reduce costs and increase production. On
the other hand, small companies may flourish because of the demand for unique and more readily available choices
for niche markets. Diversity in marketing through increased imports, the use of biotechnology for development of new
varieties, continued demand for convenience foods and the quest for longer shelf life all affect the food safety aspects
of fruit and vegetable production. Intervention strategies developed to reduce or eliminate contamination must be
flexible to serve small and large farming and processing operations while assuring that they are affordable, effective,
and efficient controls. Otherwise, food safety will continue to be a confusing mix of old wives tales, scientific jargon
and sales pitches for the produce industry.

Chapter II. During the production of fruits and vegetables, there are many points at which produce can become
contaminated with pathogens. The majority of them are related to contamination with pathogenic microorganisms
through manure (for example through fertilization practices or run off contamination) and water (for example, irrigation
water). One of the factors influencing potential contamination of produce is the level of pathogens in manure.
Although certain animal farm practices may be associated with the level of pathogen shedding -and therefore may be
associated with contamination of produce-, the number of factors involved and interactions among them are not clear.
Feeding practices, stress, age of animals, and management of manure are some of the most likely factors
contributing to pathogen shedding. The low incidence of pathogen shedding and the variability in management
practices make it difficult to clearly correlate the presence of pathogens with specific practices.

Manure processing methods to minimize the level of pathogens is an active area of research but a safe and practical
level of reduction has not been identified. Federal regulations address composting of biosolids, but not the application
of composted or aged manure to agricultural land. Moreover, scientific documentation that justifies the current
regulations for biosolids is needed. When the appropriate methods are established, indicators or surrogates that
validate the process will be needed.

In addition to contaminating the soil, pathogenic microorganisms need to survive under the associated environmental
conditions for them to become a public health risk. The survival of microorganisms in the soil depends on several
factors, including the soil characteristics, the background microflora, and climate. Several factors that reduce the
survival and growth of pathogens during crop production, such as, desiccation of plant surfaces and UV irradiation,
also need to be considered. Controlled studies that address the impact of soil matrix potential cycling (wet-dry cycles)
and subsequent field preparation activities on survival are not available.

Several preventive measures to minimize the contamination of produce are already in place; however, the
effectiveness of these measures is still questionable. For instance, although current recommendations or buyer
specifications state that a period of 60 or 100 d is necessary between application of manure to soil and planting,
neither of these recommendations has been evaluated and there is no scientifically based determination of a safe
temporal separation between aged manure and planting. Other production practices, however, clearly represent a
high public health risk and they need to be avoided by growers. These include the use of raw sludge to fertilize (not
very common, but used by some). In addition, the use of compost and manure teas in foliar applications is a popular
practice and may also pose unacceptable risks to fresh produce consumers. Currently, management choices (for
example, method of irrigation) are often based on economics and variability of markets. These decisions may affect
produce safety. Therefore more dialogue is needed between scientists and growers in order to avoid compromising
public health. The dissemination of human microbial pathogens through agricultural soils and the potential to
contaminate produce by water contamination through water run-off has also been reviewed. Growers should follow
strict responsible production practices that would ensure the microbiological quality of the agricultural water. The
protection of groundwater sources through properly maintained wells is a must. Special care should be taken when
reclaimed or run-off water is used for agricultural purposes, especially since there are no regulations regarding the
microbiological quality of agricultural water. It needs to also be noted that the quality of reclaimed water varies
according to the disinfection treatment provided. For instance, the use of reclaimed water that meets the high-level
disinfection criteria established in the EPA's Guidelines for Water Reuse poses negligible concerns for fresh produce
consumers. The persistence of pathogens on produce items due to irrigation is not clear. Some irrigation methods
such as overhead irrigation present safety risks. More research needs to be pursued to assess the extent of this risk
for a broader range of pathogens in relation to broader production environmental parameters.

At harvest, control measures for a variety of harvesting practices would decrease the risk of pathogen contamination.
Although the control steps for different crops would vary, key elements are field worker hygiene, field sanitation,
equipment sanitation, container sanitation, truck sanitation, and temperature control. Awareness of the potential
contamination at each harvesting operation and a continued dialogue between production managers and extension
specialists would help prevent contamination from those sources.

Post-harvesting operations, such as packing present several potential risk factors, many of which are related to the
quality of the water and good manufacturing practices. Proper design of the processing plant can also reduce the risk
of pathogen contamination on produce. The goal of preventing foodborne illness also involves transportation issues.
Temperature control is critical, but because shipments frequently include mixed loads, other factors, such as
temperature, ethylene, and moisture product compatibility need to be considered. Although temperature control is
important at all stages of production, and particularly with long storage or shipping times, each commodity and
pathogen concern require special consideration, and attention should be given to chill-sensitive items and inherent
respiration rates of each product.

Chapter III. The efficacy of sanitizers in killing human pathogenic microorganisms on a wide range of whole and
fresh-cut fruits and vegetables has been studied extensively. Numerous challenge studies to determine the effects of
storage conditions on survival and growth of pathogens on raw produce have also been reported. Results of these
studies are often difficult to assess due to the lack of sufficient reporting of methodologies, or comparatively because
of variations in procedures for preparing and applying inocula to produce, conditions for treatment and storage, and
procedures for enumerating pathogens. There is a need for a standard method to accurately determine the presence
and populations of pathogenic microorganisms on produce. The adoption of standard, well-characterized reference
strains would benefit a comparative assessment of a basic method between laboratories. A single protocol will not be
suitable for all fruits and vegetables. Modifications of a basic method will be necessary to achieve maximum recovery
of pathogens on various types of produce subjected to different sanitizer or storage treatments. Parameters that must
be considered in the course of developing a basic standard method and making subsequent modifications are
delineated.

Chapter IV. Numerous microorganisms, most of them from enteric environments (for example, Salmonella spp.,
Escherichia coli O157:H7, Campylobacter jejuni) but also from other sources (for example, Clostridium botulinum and
Listeria monocytogenes). Although isolation rates can be high, they are not consistent. The percentage of samples
contaminated ranges from 0 to 50%, depending upon the product and target pathogen. Because of differences in
their production systems, surface morphology, or other factors, some produce items such as lettuce, berries, seed
sprouts, and melons seem to provide conditions for survival and/or growth.

The number of foodborne illness outbreaks linked to fresh produce and reported to the United States Centers for
Disease Control and Prevention (CDC) has increased in the recent years. Some of this increase is due to improved
surveillance, but other factors may also come into play, such as increase in consumption, change in consumers'
habits, and complex distribution systems. Foodborne illness resulting from the consumption of any food is dependant
upon a number of factors. For example, the produce must be contaminated with a pathogen that survives and/or
grows to infective dose levels at the time of consumption. Temperature abuse and growth are not always necessary
for foodborne illness to occur.

Conditions for survival and/or growth of pathogens necessary for illness are influenced by the type of microorganism,
produce item, and environmental conditions in the field and subsequent handling and storage. For example, free
moisture on leaves resulting from condensation, rain, or irrigation may promote survival and growth of microbial
populations in an otherwise inhospitable environment. After harvest, pathogens will survive but not grow on the outer
surface of most fresh fruits and vegetables. In some cases, pathogen levels will decline on the outer surface. The rate
of decline is dependent upon the produce type, humidity, and temperature, as well as the atmosphere and type of
packaging used. An important factor that influences microbial growth is the epidermal barrier. Survival and
multiplication of pathogens on produce is significantly enhanced once the protective epidermal barrier has been
broken either by physical damage, such as punctures or bruising, by degradation from plant pathogens, or by
processing (for example in fresh-cut produce), especially at nonrefrigerated temperatures. At refrigerated
temperatures the ability of the microorganisms to multiply is controlled with the exceptions of psychrotrophic
pathogens (for example, non-proteolytic C. botulinum, L. monocytogenes, Yersinia enterocolitica).

Under some circumstances (for example, pressure differentials) wash water may enter intact fruit through the stem
scar or other opening, permitting pathogen infiltration. Access to nutrients inside the product may allow pathogen
multiplication to hazardous levels. Conditions that reduce infiltration of plant pathogens should also prevent infiltration
of human pathogens. Another factor to consider is packaging of the product. Packaging of the product under modified
atmospheres changes the growth rate of pathogens which may become a concern (for example, growth and toxin
production by C. botulinum). It should also be noted that specifications requiring very low microbial counts may, in
some cases, compromise produce safety because the high populations of nonpathogenic bacteria are potentially a
barrier to pathogen growth and reduce the risk of illness associated with fresh-cut products. Extensive tables on
incidence, outbreak data, and survival and growth of pathogens in fresh and fresh-cut produce are presented.

Chapter V. Much research has been directed towards seeking new methods of reducing pathogenic microorganisms
on fresh produce. The primary method to eliminate, or significantly reduce, pathogens on produce is strict adherence
to GAPs, GMPs, Hazard Analysis Critical Control Point (HACCP) programs, and other relevant strategies that prevent
contamination from occurring. This includes the concept of "good management practices" as described in the FDA
Guide to Minimize Microbial Food Safety Hazards for Fresh Fruits and Vegetables. Although the incidence of produce
contamination by pathogens is thought to be very small, there are no known mitigation strategies that will completely
remove pathogens after contamination has occurred without compromising sensory qualities. A variety of mitigation
regimens and sanitizers are available to reduce microbial populations depending upon the type of produce involved.
Washing and sanitizing efficiencies depend on several factors, including characteristics of the produce surface, water
quality, cleaner/sanitizer used, contact time, and presence and type of scrubbing action. Based on reported data, it is
likely that different sanitation mitigation strategies are needed for different produce items.

Chapter VI. Many new packaging materials, with a variety of characteristics are being studied for preserving fresh
fruits and vegetables. In general, however, research has focused mainly in the extension of product shelf life through
modification of the atmosphere. Oxygen, carbon dioxide (CO2), and nitrogen (N2), are most often used in modified
atmosphere packaging (MAP) and control atmosphere systems (CAS). Carbon dioxide has a direct antimicrobial
effect on aerobic microorganisms, resulting in an increased lag phase and generation time during the logarithmic
phase of growth. Although other gases such as nitrous and nitric oxides, sulfur dioxide, ethylene, and chlorine, as well
as ozone and propylene oxide have been investigated, they have not been applied commercially due to safety,
regulatory, or cost considerations. The recommended percentage of O2 in a modified atmosphere for fruits and
vegetables for both safety and quality falls between 1 and 5%, although the O2 level will realistically reach levels
below 1% in MAP produce.

The concern when using MAP for fruits and vegetables arises from the potential for foodborne pathogens which may
be resistant to moderate to high levels of CO2 (< 50%) and outgrow spoilage microorganisms, which may be sensitive
to the modified atmosphere. It is generally believed that with the use of permeable films, spoilage will occur before
toxin production is an issue; MAP of produce, however, should always incorporate packaging materials that will not
lead to an anoxic package environment when the product is stored at the intended temperature. Spoilage of fresh
produce is mainly due to the background microorganisms that can vary greatly for each product and storage
conditions. The elimination or significant inhibition of spoilage microorganisms should not be practiced, as their
interaction with pathogens may play an integral role in product safety.

Another area of active research is edible films for use in MAP systems. However, as with other MAP, these films can
create a very low O2 environment where anaerobic pathogens such as C. botulinum may thrive. Antimicrobial
compounds that can be incorporated into the coating are also being currently investigated.

There have been many studies investigating the migration of antimicrobials such as sodium benzoate, benzoic acid,
propionic acid, and potassium sorbate from coatings into food. It appears that the most advantageous use of these
films for antimicrobial properties would be the formation of a monolayer lipid and sorbic acid film, or a bilayer film
composed of a hydrophilic base layer coated with a thin layer of lipid containing sorbic acid. The main issue involves
the production of coatings with good surface tension that will stick to produce.

Successful control of both product respiration and ethylene production and preservation by MAP can result in a fruit
or vegetable product of high sensory quality; however, control of these processes is dependent on temperature
control. Along the entire food continuum, that is, processing, storage, transportation, and retailing, one needs to
maintain optimum temperatures. Maintaining proper storage temperatures is often most difficult at retail level.
Currently, there is concern with psychrotrophic foodborne pathogens such as L. monocytogenes, Y. enterocolitica and
Aeromonas hydrophila, as well as non-proteolytic C. botulinum, although clearly a number of other microorganisms,
especially Salmonella, E. coli O157:H7 and Shigella spp., can be potential health risks when present on MAP
produce.

Although only two MAP produce products, coleslaw mix and ready-to- eat salad vegetables, have been implicated in
foodborne illness outbreaks (botulism and salmonellosis) the potential for growth of pathogens exists. The success
and microbiological safety of MAP is dependent on controlled low temperature storage and the product's
characteristics.

Chapter VII. Indicators and surrogate microorganisms may be used for evaluating safety of fresh or fresh-cut fruit
and vegetable products by assessing or validating the effectiveness of microbial control measures. Although
frequently used on an informal basis within a specific company, use of indicators is highly dependent upon
microbiological criteria that are in place for the specific produce item or category. All the considerations that must be
addressed in establishing microbiological criteria must also be in place if indicators are to be utilized in process
verification. Sampling design, stringency, and statistical significance are critical to the evaluation of indicators or
surrogates in the assurance of food safety. General ideal qualities of indicators and surrogates are valuable starting
points when developing a safety program. The importance of selecting the significant target pathogen for the specific
product, its source, handling practices, and distribution practices cannot be overemphasized. The same is true for
selection of the indicator or surrogate to represent those pathogens. The extensive lists of considerations and
procedures should be helpful when using indicators and surrogates with fresh and fresh-cut produce. The use and
limitations of indicators and surrogates to determine or validate treatment effectiveness have been delineated.
Challenges are identified for selection of an indicator or surrogate for the specific situation and conditions of an
individual produce item, including growing, harvesting, processing, handling, storage, and packaging.

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