pathogen environmental

monitoring program (PEM)

Presented by the Almond Board of California

Preventing
Salmonella
Recontamination:
Pathogen
Environmental
Monitoring
Program Guidance
Document

INTRODUCTION

Introduction

review of the history of the microbiological hazards associated with tree nuts and nut products, including almonds, shows that Salmonella spp. is one of the primary
target pathogens of concern at all stages of production
and handling. The Hazard Analysis Critical Control Point (HACCP)
approach is the most widely accepted food safety management
framework around the world and is endorsed by the Almond Board
of California for use by almond handlers for the production of safe
and wholesome products. HACCP is a systematic science-based approach that identifies, assesses and controls the risk of biological,
chemical and physical hazards in the product (1). The HACCP approach consists of seven principles, each of which must be followed
for successful implementation. The first HACCP principle states that
the HACCP team should conduct a hazard analysis that assesses
the food safety hazards that are reasonably likely to occur and that
must be controlled for the production of safe product. Since history
has revealed Salmonella spp. to be one of the reasonably likely food
safety hazards to occur within the almond production environment,
it is critical that an almond facilitys HACCP plan identifies, assesses,
and seeks to control and mitigate that risk.
An effective mechanism for controlling the risk of Salmonella in the
almond production environment is the implementation of a Pathogen Environmental Monitoring (PEM) program. As an integral component of an almond facilitys HACCP plan, a well developed PEM
program will control and mitigate the risk of Salmonella spp. contamination proactively in both the production and post-production
environment. This document is intended to outline the necessary
tools and steps to develop and implement such a program.

INTRODUCTION

Characteristics of Salmonella
The genus Salmonella consists of rod-shaped,
gram-negative, non-sporeforming, predominately motile cells that can grow either aerobically or anaerobically and are members of the
family Enterobacteriaceae. In nature, they are
found in both warm- and cold-blooded animals,
humans, and in the general environment, including the soil and water (2). Salmonella spp. can
grow in the temperature range of 41F (5C) to
113F (45C) with the optimum growth range of 95F (35C) to 109.4F (43C). Growth is
slow at temperatures below 50F (10C), and most strains do not grow at temperatures
44.6F (less than 7C). Salmonella spp. has a pH range for growth of pH 4 to 9 with an
optimum of 7 to 7.5. Almonds fall within this optimum pH range. Salmonella spp. is classified according to serotype, and over 2,400 serotypes have been described for the genus.
Since Salmonella spp. are vegetative bacteria, they are not as heat resistant as bacterial sporeformers. Strains of Salmonella do vary, however, in their ability to resist heat.
For example, the strain Salmonella Senftenberg 775W is about 10 to 20 times more heat
resistant than the average strain of Salmonella at high water activity (Aw). Aw is a measurement used to describe the water that is available in a food for the microorganisms
to grow. Under favorable conditions, Salmonella spp. can grow in the Aw range of 0.94 to
more than 0.99, with 0.99 being the optimum Aw for growth. Typically the water activity
of almonds under proper storage conditions is below the level required for Salmonella
growth. However, the addition of moisture or water can create conditions that allow Salmonella to grow if it is present on the nuts. Of particular relevance to almonds and other
nut products is the ability for Salmonella spp. to survive for long periods under dry conditions. Scientific studies have shown, for example, that Salmonella Enteriditis Phage Type
30 can survive for up to 550 days on almond kernels held under a variety of common
storage conditions (3). Numerous studies have shown that Salmonella spp. can survive
for long periods of time in foods and in farm/food plant environments, as well, when they
become desiccated (4, 5). Although low water activity will inhibit growth, Salmonella spp.
can also survive for extended periods of time in a low Aw environment. For example, one
study has shown that Salmonella spp. can survive for up to 24 weeks in peanut butter,
with a higher incidence of survivors in product stored at 41F (5C) versus 69.8F (21C)
(6). Furthermore, the Aw of a food product can impact the heat tolerance of Salmonella
spp. One investigation found that low Aw was detrimental to Salmonella survival at 131F
(55C) or 140F (60C), but that temperatures greater than 158F (greater than 70C)
were always protectivemeaning that the pathogen was harder to inactivate at the higher temperature (7). Research has shown that once Salmonella spp. contaminates peanut
butter, it is not realistically possible to eliminate it with heat treatmentthe reduced Aw
environment of peanut butter is highly protective of the pathogen (8).

INTRODUCTION

Salmonella and human illness

All serotypes of Salmonellae are considered human pathogens. However, the severity of
illness varies greatly depending on the strain involved and the susceptibility of the host.
Salmonellosis is the leading cause of food-borne illness in the United States, with a reported 16.2 cases per 100,000 population in 2008 reported by the Centers for Disease
Control and Prevention (9). Salmonellosis is an infection with symptoms consisting of
diarrhea, abdominal pain, chills, fever, nausea, vomiting, dehydration and headache (2).
The most susceptible individuals are infants, followed by the elderly and immunocompromised, and then the general population. Symptoms usually appear within 12 to 36 hours
with a range of 5 to 72 hours after ingestion of the contaminated food. Symptoms usually
resolve in healthy individuals within 2 to 5 days, and the disease is generally self-limiting.
In a small percentage of cases, complications can occur, including systemic infection and
reactive arthritis, which can have long-term, disabling effects on the patient. Overall, the
human mortality rate for salmonellosis is low (less than 1 percent), but can be as high as
20% depending on strain.
The infective dose for salmonellosis is dependent on a number of variables including the
strain of Salmonella spp. ingested, the susceptibility of the individual and the type of
food consumed. However, small numbers, as low as 15 to 20 cells, have been shown to
cause illness in humans; therefore, great care must be taken to prevent recontamination
of product once it has been pasteurized (10).
Persistence of Salmonella in the almond growing and production environments
Research has shown that Salmonella
Enteriditis Phage Type 30 has persisted
in a single almond orchard for over a
five-year period and that the same organism can persist and grow in almond
orchard soils for extended periods
of time (11, 12). Salmonella spp. can
survive for weeks in aquatic environments, including irrigation water used
for crops. And surveys have shown that
the organism can survive for months in
soils and sediments (13). Research has
also shown that Salmonella Enteriditis
Phage Type 30 can rapidly grow to
high levels in wet almond hull and shell
slurries and can survive drying of the hulls, which can become a source of recontamination during almond processing if not properly controlled (14). Salmonella spp. has been
found to colonize and persist on conveyor belts (dependent on type of belt material) and

INTRODUCTION

on various types of fabrics for weeks

(15, 16). Various serotypes of Salmonellae were found in the production environment of an oilmeal processing plant,
including the processing floor, dust
samples, employee shoes, brooms, conveyors and other sites (17). Research
has also shown that pests and vermin
such as rodents, birds, cockroaches and
houseflies can harbor, transmit and amplify the presence of Salmonella spp. in
the environment (18, 19, 20, 21).
Prevalence of Salmonella in almonds and other raw agricultural commodities
Almonds, as with most agricultural commodities such as grains, spices and raw cocoa,
have been found to harbor Salmonellae and other pathogens. Salmonella spp. has been
isolated from and shown to survive in pecans, peanuts, pistachios, dried edible seeds
(sesame, alfalfa, melon, sunflower, flax), Brazil nuts, hazelnuts, macadamia nuts, walnuts
and almonds (22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33). One study showed a Salmonella
incidence of 1.7% in raw almonds, and another study showed an overall isolation rate of
0.87% + 0.2% from raw California almonds sampled over a five-year period (28, 29). The
latter study showed that Salmonella spp. was present at low levels in positive samples.
Cases of human salmonellosis associated with almonds and other nuts
Given the existence of naturally occurring Salmonella spp. in the environment it is not
surprising to find the pathogen in raw nuts and similar products. These products need to
be handled by the processor as if they are contaminated with Salmonella spp., and measures must be taken to prevent recontamination of treated product.
Three documented salmonellosis outbreaks traced to the consumption of peanut butter
made with contaminated peanuts have occurred. The first outbreak occurred in 1996 in
South Australia and was traced to a single peanut butter manufacturer that used peanuts
from an outside supplier that were recontaminated after roasting with Salmonella Mbandaka, a relatively rare strain (34, 35). The other two peanut butter outbreaks occurred in
the United States in 2006 2007 and 2008 2009 (36, 37). Over 600 people were sickened in each of these outbreaks. The common theme to all three of these peanut butter
outbreaks were multiple major deficiencies in the manufacturing plant that led to recontamination of finished product prior to packaging.
Almonds have recently been the cause of several salmonellosis outbreaks. The first outbreak linked to the consumption of raw almonds occurred in 2000 2001 and caused ill-

INTRODUCTION

nesses in Canada and the United States due to a rare strain, Salmonella Enteriditis PT 30
(27). The second outbreak traced to the consumption of raw almonds occurred in 2003
2004, with illnesses again occurring in Canada and the United States, this time due
to Salmonella Enteriditis PT 9C (38). Product was recalled from more than 10 different
countries. This second outbreak led to the promulgation of the rule for the mandatory
treatment of raw almonds to achieve a minimum 4-log reduction of Salmonella (39). In
2005 - 2006, a cluster of illnesses caused by rare subtype Salmonella Enteriditis occurred
in Sweden that was epidemiologically linked to the consumption of raw almonds (40).
While the pathogen was not isolated from any of the almonds tested in the investigation,
statistically there was a very high matched-odds ratio in the case control study conducted by the Swedish authorities.
In early 2009, the U.S. Food and Drug Administration found multiple samples of pistachio
nuts and pistachio-containing products from one specific company to be contaminated
with multiple serotypes of Salmonellae, including Salmonella Montevideo, Salmonella Newport, and Salmonella Senftenberg (41, 42). While no definitive cases of salmonellosis have
been linked to pistachios, the Centers for Disease Control and Prevention reported that
one patient in Connecticut with a matching Salmonella strain DNA fingerprint reported
consuming a pistachio-containing product.
The issue of product recontamination
As discussed, there are many other food-borne illness outbreaks linked to the consumption of low moisture, low Aw foods,
including various edible nut and seed products, chocolate and
confections, dried dairy powders, and spices. It is indisputable
that raw agricultural commodities such as raw almonds occasionally contain various levels of Salmonellae. Salmonellae can persist in
dry products or in food production environments for long periods
of time. It is incumbent on the processor to ensure that lethality
steps such as steam or PPO treatments for almonds are validated to
achieve a minimum 4-log kill of Salmonellae. However, equally as important as the validated kill step is the prevention of product recontamination prior to packaging. It is wasted effort to implement a validated minimum
4-log kill step only to have the treated or pasteurized product recontaminated with
Salmonella prior to packaging.
Data indicates that post-lethality recontamination is a major cause of food-borne illness
and product recalls. A World Health Organization (WHO) survey conducted in Europe
found cross-contamination during processing to be the most important factor relating
to the presence of pathogens in prepared foods (43). A survey of food-borne outbreaks
in the United Kingdom found cross-contamination to be a significant contributing factor
in 32.1% of the cases (44). An investigation of Salmonella spp. cross-contamination in an

INTRODUCTION

oilmeal processing plant found that controlling traffic flow (personnel and materials), rodents and airborne dust were key factors in reducing contamination rates (17). In two major peanut butter salmonellosis outbreaks, uncontrolled dust in the production facilities
was thought to be a major contributing factor (46). Published guidelines for minimizing
microbial cross-contamination in poultry feed mills indicate that dust control in the feed
milling facility is essential for controlling Salmonellae (45). Other key factors include the
control of employee traffic patterns to minimize the possibility of cross-contamination
and the control of rodents and wild birds. The International Commission on Microbiological Specifications for Foods (ICMSF) recognizes that, while it is not possible to prevent
the introduction of pathogens into food processing facilities, it is crucial to minimize their
presence (47). The ICMSF stresses a number of potential sources in food-processing areas that must be controlled in order to minimize the potential for product recontamination:
 @OeOU`WQcZbc`OZQ][[]RWbWSaacQVOa`Oec\^OabSc`WhSROZ[]\Ra`S_cW`S^VgaWQOZ
separation through plant design and layout in order to minimize entry of pathogens
into processed product areas.
 4]]RVO\RZS`aO\R[OW\bS\O\QS^S`a]\\SZQO\PSa]c`QSa]TQ]\bO[W\ObW]\O\R[cab
be trained in proper hygiene principles.
 >S`a]\OZQZ]bVW\UW\^O`bWQcZO`aV]SaQO\b`O\aTS`^ObV]US\aT`][]\SO`SOb]O\]bVS`
and must be controlled.
 /W`O\ReObS`[cabPSQ]\b`]ZZSR Compressed air filters, often used for blowing down
and cleaning processing equipment, can be a source of contamination if not properly
maintained. Water aerosols can disperse microorganisms throughout the facility if not
controlled.
 7\aSQbaO\R]bVS`^SabaQO\OQbOadSQb]`a]T^ObV]US\b`O\a[WaaW]\W\bVST]]R[O\cfacturing plant if not properly controlled.
 B`O\a^]`bS_cW^[S\bacQVOa`OQYab`]ZZSgaQO`baT]`YZWTbaO\RaW[WZO`S_cW^[S\bQO\
he important vectors for transferring microorganisms throughout a facility and should
be limited to use in specific areas.
All of these issues are relevant to the production of almonds and almond products. Dust
control is a critical factor that must be addressed. The introduction of moisture into the
environment should be minimized to the greatest extent possible. The combination of
dust and water can lead to the growth of Salmonellae and other pathogens to high levels
in the environment that can then be subsequently spread throughout the facility. Careful
thought and planning must be done in order to control dust and water in the environment.

SALMONELLA CONTROL ELEMENTS IN THE ALMOND PRODUCTION ENVIRONMENT

Salmonella Control Elements in the

Almond Production Environment

ach element in the Salmonella control equation must be addressed to minimize

the potential for product recontamination. Each one of these elements should
have a detailed, documented plan to address them. A lapse in any one element
increases substantially the risk of product recontamination.

The Grocery Manufacturers Association (GMA) has developed a document for food
manufacturers titled the Control of Salmonella in Low-Moisture Foods. This document
and its companion annex document
provide guidance on the control of
Salmonella when manufacturing lowmoisture foods such as almonds (48,
49). The GMA guidance document
outlines seven elements that should
be applied to control Salmonella in
low-moisture products. These seven
elements are consistent with the elements of the Salmonella control equation and include:
1. Prevent ingress or spread of Salmonella in the processing facility.
A hazard analysis should be conducted by a cross-functional team to determine the
potential sources of Salmonella spp. in the plant. Example of potential sources include
incoming raw materials (almonds and other materials), utensils and equipment, personnel and traffic flow, rodents and birds,
airflow, and overall facility design and integrity. Ingredients known to be contaminated with Salmonella should be segregated. Sanitation and cleaning procedures should be developed that limit the
use of water in the production environment. Employees must be educated on
the potential sources of contamination,
the need to adhere to traffic patterns,
and proper hygienic practices and procedures needed to prevent the spread of
Salmonella spp. in the facility.

key elements
The key elements
required for control
of Salmonella
recontamination in an
almond production
facility can be
conceptualized in the
Salmonella control
equation:
TRAFFIC CONTROL
(PERSONNEL &
EQUIPMENT)
+
DUST CONTROL
+
WATER CONTROL
+
SEPARATION OF
RAW & PASTEURIZED
PRODUCT
+
EFFECTIVE
CLEANING &
SANITATION
SALMONELLA
CONTROL

SALMONELLA CONTROL ELEMENTS IN THE ALMOND PRODUCTION ENVIRONMENT

2. Enhance the stringency of hygiene

practices and controls in the primary
Salmonella control area.
The Primary Salmonella Control Area
(PSCA) in a low-moisture product facility is the area where the handling
of ingredients and product requires
the highest level of hygiene control.
Examples within an almond processing facility include, but are not limited
to, sorting and packing lines, finishedgoods packaging, and pasteurization
equipment and the immediate surrounding areas. The key concept is to, protect product
open to the environment prior to packaging. The PSCA should be physically separated
from the rest of the facility. Movement of personnel and materials should be controlled
between the PSCA and the remainder of the facility. Facility layout should be such that
the PSCA is protected from recontamination from the rest of the facility to the greatest
extent possible.
3. Apply hygienic design principles to building and equipment design.
Building layout and equipment design should be based on solid hygienic principles (50).
In particular, the layout and design of equipment and processes in the PSCA should be
well thought out. All efforts should be made to minimize the accumulation of dust and to
exclude moisture from the processing environment through the use of proper dry-cleaning practices.
4. Prevent or minimize growth of Salmonella within the facility.
The control of moisture in the manufacturing environment is absolutely crucial to the prevention of Salmonella contamination in low-moisture products such as almonds. Dry conditions must be maintained at all times in the PSCA, except where controlled wet cleaning is deemed necessary in special cases such as a product contamination issue. If water
ingress occurs within the PSCA such as through a drain back-up, roof or wall leak, leaky
steam valves, or leaking water pipe, procedures must be implemented to immediately address the problem. Once the leak is repaired, the area must be returned to hygienic condition through proper cleaning and sanitation. If wet-cleaning procedures are used, the
area must be thoroughly dry before being put back into operation. Intensive sampling of
the environment for Salmonella and indicator organisms should be conducted to verify
that the cleaning and sanitation procedures were effective in returning the area back to
hygienic condition.

10

SALMONELLA CONTROL ELEMENTS IN THE ALMOND PRODUCTION ENVIRONMENT

5. Establish a raw materials/ingredients

control program.
An approved ingredient supplier program should be
implemented, particularly for those ingredients that
are considered Salmonella sensitive. These ingredients are those that have a known history of association with Salmonella spp. Salmonella sensitive
raw materials that have been pasteurized or treated
should be segregated upon receipt from other raw
ingredients that have not been treated. On-site audits of ingredient suppliers should evaluate food
safety procedures in their establishment. This means
an implemented and valid HACCP plan with proper
prerequisite programs including GMPs, an aggressive Pathogen Environmental Monitoring (PEM)
program, sanitation practices, raw materials/ingredients storage, process validation, employee training,
a finished-product hold-and-release program (if finished-product testing is performed),
traceability, and a corrective action plan if positive Salmonella results are found.
6. Validate control measures to inactivate
Salmonella
By government regulation, almonds must be processed to achieve a minimum 4-log inactivation of Salmonella spp. Proper protocols must be followed in order to validate the
process. The Almond Board of California has issued several guidance documents on the
validation of processes for almonds (51, 52, 53, 54, 55). An external process authority
should be used if internal expertise is not available to conduct proper validation protocols of the process. Once a process is validated to inactivate Salmonella, the challenge to
the processor is to prevent recontamination of that product through subsequent handling
and packaging.
7. Establish procedures for verification of Salmonella controls and corrective actions.
The most effective verification tool for determining the effectiveness of a facilitys Salmonella controls is the implementation of an aggressive Pathogen Environmental Monitoring
(PEM) program. A PEM program is an ongoing measure of the effectiveness of the overall
Salmonella control program in the plant. A PEM program, in itself, is not a Salmonella control program, but it provides feedback on where efforts need to be directed for the overall control program. The focus of an aggressive PEM program is in the PSCA, but areas
remote from the PSCA should be included and will be discussed in further detail.

The most
effective
verification tool
for determining
the effectiveness
of a facilitys
Salmonella
controls is the
implementation
of an aggressive
Pathogen
Environmental
Monitoring
program (PEM).

11

SALMONELLA CONTROL ELEMENTS IN THE ALMOND PRODUCTION ENVIRONMENT

Each manufacturer should decide on the value of testing finished product for Salmonella
spp. Producers need to understand the statistics behind finished-product testing. In general, finished-product testing as a sole measure of product safety is a poor approach in
the absence of a robust Salmonella control program. If finished-product testing is performed, it is critical that the lots be segregated, placed on hold, and then released into
commerce only after a negative result is obtained. If a sample tests positive for Salmonella spp., the lot is considered adulterated and should not be released into commerce. In
no case should the lot be retested for Salmonella spp. with the intention of negating the
initial positive result. Corrective actions must be taken and documented when Salmonellae are detected in either environmental or finished product samples.
Focusing on the seven Salmonella control elements discussed in the GMA guidance
document and the elements of the Salmonella control equation will significantly reduce
risk to the product and the consumer. Conversely, ignoring these principles will greatly
increase the risk of a Salmonella recontamination event and present increased risk to
the business and the consumer. Food recall costs can be astronomical, leading to bankruptcy and closure of the business. It has been estimated that the cost of the 20082009
peanut butter salmonellosis outbreak caused by the now defunct Peanut Corporation of
America could reach as high as $1 billion in lost production and sales by U.S. peanut producers (56). Clearly, adherence to the guidelines outlined in this document could have
avoided such a widespread disaster.

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P R I N C I P L E S O F A PAT H O G E N E N V I R O N M E N TA L M O N I TO R I N G P R O G R A M

Principles of a Pathogen
Environmental Monitoring Program

he International Commission of Microbiological Specifications for Foods (ICMSF) has recognized that even with the optimal application of a HACCP plan or
a Good Hygienic Practices (GHP) program, it is no guarantee that recontamination within the processing environment will not occur (47). Despite strict control
of all critical control points (CCPs) in a process to ensure destruction of pathogens in
raw materials, foods can subsequently become contaminated through one of two ways:
1) the addition of a contaminated ingredient after a kill step, or, 2) recontamination from
the processing environment. In the almond-processing environment, recontamination of
the product can occur through myriad ways, including contact with raw and untreated
materials, processing equipment that is not properly cleaned, manufacturing activities,
maintenance activities, sanitation practices, workers, waste, product rework, pests, and
microbial pockets embedded in equipment and the structure of the building. Control of
recontamination is dependent upon a combination of factors such as those described in
the Salmonella control equation, and includes the following (57):

Q
Q
Q
Q

Hygienic design, construction and maintenance of the facility

Hygienic operation and maintenance of the processes and equipment
Application of appropriate (e.g., dry vs. wet) cleaning and disinfection procedures
Training of personnel in food safety and hygienic practices

Microbiological monitoring of the food-processing environment can be performed to

meet a number of objectives:

Q Verifying the effectiveness of cleaning and sanitation practices

Q Determining the frequency required for cleaning and sanitation
Q Determining the presence of food-borne pathogens or their indicators in the
environment
Q Discovering environmental sources of spoilage organisms
Q Determining the frequency required for special maintenance procedures (e.g.,
changing air filters)
Q Evaluatiing the hygienic design and fabrication of food-processing equipment and
facilities

13

P R I N C I P L E S O F A PAT H O G E N E N V I R O N M E N TA L M O N I TO R I N G P R O G R A M

The focus of this guidance document is on determining the presence of food-borne

pathogens including Salmonellae or their indicators in the environment of the facility
through the development and implementation of an aggressive Pathogen Environmental
Monitoring (PEM) program. An effective PEM program is a measure of the effectiveness
of the Salmonella controls that the facility has in placeproof of how well the facility is
managing all of the elements of the Salmonella control equation. A PEM program should
be thoughtful and aggressively applied. Employees should never be discouraged from
finding a positive result. If Salmonella is present in the manufacturing environment, finding it through an aggressive PEM program can allow you to do something about it. You
want to encourage employees to find it if it is there.
Getting started
Implementing a PEM program may, at first, seem like a daunting undertaking. However,
through the use of a systematic approach, an effective program can be developed in fairly short order. If your company does not have a food safety professional experienced in
the development and implementation of a PEM program, it is strongly recommended that
you make use of an experienced outside expert or process authority to guide you through
it. A PEM program is specific to the individual facility under consideration and specific
to the individual operations within the facility. There is no one size fits all program that
can be used outside of the common principles discussed in this guidance document. The
first order of business is to assemble your team that will develop and implement the PEM
program. It is desirable to have several individuals familiar with the operation help in identifying potential areas of risk and concern. Examples of such individuals include the plant
quality manager, the plant or corporate microbiologist, line supervisors or operators, and
sanitation supervisors or workers. If you are using an external process authority or expert
to help develop and implement your program, you still should make these individuals
available to work with the expert.
Sampling locations: The PEM zoning concept
Once your PEM team is assembled it is important to understand your process flow and
emphasize identifying potential points of product recontamination. As discussed in the
case of almond and nut processing, Salmonella spp. is the target organism of concern.
A flow diagram of the process can be very helpful, but it is absolutely essential that you
walk the plant floor to determine areas where the product may be vulnerable to recontamination after the lethality step. One useful tool that can help you in site selection and
managing your PEM program data is the PEM zoning concept. In the zoning concept,
plant operations are divided into four zones based on level of risk. These four zones are
illustrated in Figure 1 on page 19 and are defined as follows:

14

P R I N C I P L E S O F A PAT H O G E N E N V I R O N M E N TA L M O N I TO R I N G P R O G R A M

Zone 1Areas in the plant that are direct product contact surfaces after the lethality or microbial reduction step (e.g., roaster) and before the product is sealed in the primary package. If there is no lethality step in the process, Zone 1 areas are those where the product is
exposed to the plant equipment and environment prior to sealing in the primary packaging. Examples of Zone 1 surfaces in the almond production environment include:
Q
Q
Q
Q
Q
Q
Q

Conveyor belts and buckets

Utensils
Employee hands (if touching product)
Slicers and dicers
Product hoppers, bins and bin liners
Discharge chutes
Fillers

15

P R I N C I P L E S O F A PAT H O G E N E N V I R O N M E N TA L M O N I TO R I N G P R O G R A M

Zone 2Non-product contact areas in the plant that are closely adjacent to product contact surfaces. Examples of Zone 2 surfaces in the almond production environment
include:
Q
Q
Q
Q
Q
Q

16

Equipment framework
Drip shields and housings
Control panels and buttons
Overhead pipes directly over Zone 1 surfaces
Computer screens
Maintenance tools

P R I N C I P L E S O F A PAT H O G E N E N V I R O N M E N TA L M O N I TO R I N G P R O G R A M

Zone 3Nonproduct contact surfaces that are in open post-lethality product-processing

areas, but not closely adjacent to Zone 1 surfaces. Zone 3 surfaces, however, have the
possibility of leading to product cross-contamination. Examples of Zone 3 surfaces in the
almond production environment include:
Q
Q
Q
Q
Q
Q

Floors, walls, ceilings

Hoses
Air handling units
Condensate drip pans
Trolleys, forklifts, walk-alongs, carts
Trash containers

Q
Q
Q
Q
Q
Q

Pallets
Foot mats
Foot baths
Drains
Brooms, mops and squeegees
Toolboxes

17

P R I N C I P L E S O F A PAT H O G E N E N V I R O N M E N TA L M O N I TO R I N G P R O G R A M

Zone 4Areas remote from post-lethality product-processing areas. Zone 4 areas, if not
maintained in good hygienic condition, can lead to cross-contamination of Zones 1, 2 and
3. Examples of Zone 4 surfaces in the almond production environment include:
Q
Q
Q
Q
Q
Q

18

Hallways
Loading docks
Warehouses
Bathrooms
Locker rooms
Cafeteria and break rooms

Q Coolers and freezers

Q Maintenance shop
Q Office areas

P R I N C I P L E S O F A PAT H O G E N E N V I R O N M E N TA L M O N I TO R I N G P R O G R A M

Figure 1. Zone Concept to Illustrate Areas of Highest Risk (Zone 1) to Lowest Risk (Zone
4) for Product Contamination.

ZONE 4
locker rooms, cafeteria, halls
warehouse, loading dock

ZONE 3
phones, hand trucks, forklifts, walls,
floor and drains

ZONE 2
nonproduct contact surfaces in close
proximity to product (exterior of
equipment, chill units, framework,
equipment housing)

ZONE 1
product contact
surfaces (slicers,
conveyors, peelers,
strip tables, utensils,
racks, work tables,
employee hands,
dicers, pumps)

Following the principles of zoning allows you to take a rational approach to sample site
selection and managing the overall PEM program. It can also be used as an effective
teaching aid for plant personnel and senior management. It is important for you to define
what constitutes Zone 1 to 4 areas in your specific facility and be consistent. Once you
have determined Zones 1 to 4 in your facility, you then need to give careful consideration
to what specific test methods you are going to employ before you begin testing.

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P R I N C I P L E S O F A PAT H O G E N E N V I R O N M E N TA L M O N I TO R I N G P R O G R A M

PEM sampling in raw product areas

Raw product areas are not the primary focus of PEM monitoring, since it is assumed that
these areas will be contaminated with salmonellae from time to time. However, there is
value in monitoring these areas because it is not desirable to have high levels of salmonellae build up in raw product. The mandatory 4-log Salmonella lethality process, as required in the United States, would be inadequate if high levels of the pathogen (greater
than 104 CFUs) were present in raw almonds. It is not unexpected to occasionally find
salmonellae in raw product areas. However, a frequent incidence might suggest that
cleaning procedures for those areas are not adequate or that a niche or moisture in the
environment may be allowing the pathogen to persist and grow. One recommended
approach would be to use total Enterobacteriacae (TEB) counts as a quantitative indicator of the potential presence of salmonellae. The area should be monitored for both
salmonellae and TEB counts after cleaning to ensure effectiveness of those areas. If
TEB counts exceed 102 CFU per area sampled or per sponge, that suggests cleaning
procedures were not effective and need to be repeated (a 102 CFU action limit provides
a 2-log margin of safety for almonds that are going to be treated using a 4-log lethality process). The PEM zoning nomenclature can still be used for raw product areas with
slight modification to the definitions. Zone 1 areas are those where product comes into
contact with processing equipment. Zone 2 areas are those sites that are closely adjacent to Zone 1 areas. Zone 3 sites are those in the open product processing areas, and
Zone 4 sites are those remote from Zones 1, 2 and 3 areas. It is imperative that the response team carefully consider what actions need to be taken in the event of a positive
result in raw product areas.
Types of testing for pathogen environmental
monitoring
There are myriad methods that can be used for
your PEM program. The choice of method depends on a number of considerations. The first
consideration is to determine which elements
you want to include in your PEM program. It is
recommended that you include the following
components in your PEM program:
Q
Q
Q
Q

Surface sampling using sponges or swabs

Product residue scrapings/fines/dust samples
Water samples
Air samples

The second consideration is to determine the type of testing you are going to employ.
Generally there are two categories of methods you can use: 1) testing for indicator organ-

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P R I N C I P L E S O F A PAT H O G E N E N V I R O N M E N TA L M O N I TO R I N G P R O G R A M

isms, and 2) testing for the specific target pathogen (Salmonella spp.). Indicators are used
to measure the potential presence of pathogens and to assess the effectiveness of cleaning
and sanitation (58). Food safety indicators should meet the following important criteria:

1. Be easily and rapidly detectable

2. Be easily distinguishable from other members of the food microflora
3. Have a history of constant association with the pathogen whose presence it indicates (e.g., Salmonella spp.)
4. Always be present when the pathogen of concern is present
5. Be an organism whose numbers ideally should correlate with those of the pathogen
of concern
6. Possess growth requirements and a growth rate equaling or exceeding that of the
pathogen
7. Have a die-off rate that at least parallels that of the pathogen and ideally persists
slightly longer than the pathogen of concern
8. Be absent from foods that are free of the pathogen except perhaps at certain
minimum numbers

There are a number of indicator tests that can be used for PEM programs in almond-processing operations. One common indicator test is the coliform and Escherichia coli group,
which is commonly used in the food industry as sanitation and process integrity indicators and for HACCP verification (59). Another highly recommended indicator test is the
total Enterobacteriaceae (TEB) count, which has been widely used in Europe as a food
safety and process integrity indicator test. The Enterobacteriaceae group is superior to the
coliform group as an indicator of sanitation because this group, collectively, has greater
resistance to the environment than the coliforms, can colonize areas where sanitation and
cleaning have been insufficient, and members of this group are sensitive to sanitizers.
While the coliform/E. coli and the total Enterobacteriaceae groups are not perfect indicators of the presence of Salmonella spp. in the processing environment, they nevertheless
are good indicators of cleaning and sanitation practices. Although there is a lack of data
correlating TEB counts and Salmonellae in environmental samples from almond and nut
processing operations, data does exist showing the existence of a loose correlation between TEB counts and the occurrence of Salmonellae in environmental samples from a
dried-milk processing plant (60):
Total Enterobacteriaceae cfu/g

Salmonella positive in 50 g percentage

<2

0.5

2 - 100

0.9

100 - 500

8.7

> 500

9.0

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P R I N C I P L E S O F A PAT H O G E N E N V I R O N M E N TA L M O N I TO R I N G P R O G R A M

Note that in the above data Salmonellae were detected when TEB counts were at the
limit of detection of the method (less than 2 CFU/g). It must be emphasized that it is
possible for Salmonellae to be present when the TEB counts are negative (the same is
true for coliform/E. coli counts, as well). This is because enrichment methods used for
the detection of Salmonellae are more sensitive than quantitative TEB or coliform/E. coli
counts. However, the loose correlation in the previous table shows that the percentage
of positive environmental samples for Salmonellae dramatically increase with increasing TEB counts. Therefore the risk of having Salmonellae in your processing environment
increases with increasing TEB counts. Quantification of TEB and coliform/E. coli can be
conducted by standard plating or cultural techniques, including Most Probable Number
(MPN) methods (57). One convenient method that can be used for quantifying either
the TEB or coliform/E. coli groups is the 3M PetrifilmTM method (www.3M.com/product/
information/Petrifilm-plate.html) as shown in Figure 2 (61).1 These plates are provided by
the manufacturer in sealed foiled pouches that are stored under refrigeration until use or
until the end of the expiration date on the label.
A third indicator test that is widely used as a quality indicator for evaluating foods and
food-processing operations is the aerobic plate count (APC). APCs cannot be used as
safety indicators for pathogens (Salmonella spp.) because in almost all cases there is no
correlation between APCs and the presence of pathogens or their toxins. There are applications, however, where an APC count can be used as an indication of sanitation effectiveness of a process. APC data from dry processing environmental samples can be difficult to interpret because dry-cleaning procedures will not remove the entire microflora
present on equipment, including sporeforming bacteria. Consequently, APCs can vary
widely depending on the quality of ingredients or product processed on the line. APCs
can be conducted using standard pour-plate methods, the 3M PetrifilmTM methods, or by
the Most Probable Number (MPN) technique, among others (62).
Figure 2. 3M PetrifilmTM Plate Method

Add sample

22

Roll down film

Distribute sample
with spreader

Mention of commercial names does not constitute an endorsement by the Almond Board of California.

P R I N C I P L E S O F A PAT H O G E N E N V I R O N M E N TA L M O N I TO R I N G P R O G R A M

Environmental sampling techniques

Sampling procedures and techniques should be conducted by properly trained personnel, consistent with standard industry practice outlined in this guidance document. Testing of environmental samples, including fines, debris, sweepings, sponges, and swabs,
provide critical information and feedback on how effective your measures are in controlling Salmonellae in your almond manufacturing operations.
Procedures sampling equipment and environmental surfaces for salmonellae
When testing equipment and environmental surfaces for Salmonellae, it is
important to sample as large an area as
reasonably possible. The use of sterile
sponges or the 3MTM Sponge-Stick (Figure 3) (http://solutions.3M.com/wps/
Microbiology/FoodSafety/) is a very
useful means of sampling large areas
for Salmonellae. Prepared hydrated or
dry sponges in sterile Whirl-Pak bags
are available from a variety of vendors.
Sterile swabs such as the 3MTM Quick
Swab, the 3MTM Enviro Swab or culturette swabs can be used for sampling small areas such as cracks, crevices, holes, and
other hard-to-reach areas. If sanitizer is used as part of the normal sanitation procedure
in the plant, then sponges or swabs should be placed in sample with neutralizing buffer
(for example, D/E neutralizing buffer). This is essential to recovery of sub-lethally injured
Salmonellae and to ensure that they are able to grow out during culturing of the sponges
or swabs in the laboratory. Sponges/swabs with neutralizing buffer are commercially
available from many vendors.
Dust, fines, floor sweepings and vacuum canister debris can be collected with sterile
utensils such as scoops, scrapers and spatulas and placed in sterile Whirl-Pak bags. Such
sampling utensils may be purchased from a variety of venders, including eNasco (http://
www.enasco.com/page/wp_index). Sample collection should, where possible, proceed
throughout the almond-processing plant from Zone 1 to Zone 2 to Zone 3 to Zone 4 using the following procedure as a guide:

Figure 3. 3MTM
Sponge-Stick or
equivalent for Sampling Environmental
Surfaces

1.

Prelabel the sponge sample bags using a predetermined coding or numbering system. Make sure site descriptions indicate from which zone each sample is taken.
2. Thoroughly wash and dry hands. Sanitize hands with an appropriate hand sanitizer.
Put on sterile gloves.
3. Using sterile gloves, remove the sponge or 3MTM Sponge-Stick from the Whirl-Pak

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P R I N C I P L E S O F A PAT H O G E N E N V I R O N M E N TA L M O N I TO R I N G P R O G R A M

4.

5.

6.
7.

8.

9.

10.

bag or container.
Grasping the sponge and using constant pressure, sponge an area as large as reasonably possible. Typically, a range of 40 square inches to 400 square inches is used for
testing environmental surfaces. Replace the sponge back into the Whirl-Pak bag or
container and seal it.
Small areas such as cracks, crevices and screw holes may be more appropriately sampled using sterile swabs. Using sterile gloves, remove the swab from its container and
swab the sampling site. Return the swab back to its container.
Change gloves between sponge samples and use an alcohol-based sanitizer to minimize the potential for cross-contamination.
When Zone 1 sites are sampled with
premoistened sterile sponges the site should be wiped down with an alcohol-based
sanitizer after the sampling is done. Eco-WipeTM FCS single-use quaternary/alcoholbased wipes (http://www.ecolab.com) are particularly useful for this purpose. These
are approved for nonporous food contact surfaces and are useful in returning the
area swabbed back to hygienic condition, including removing any small amounts of
residual liquid left by the premoistened sponge.
Place the collected, sealed sponge samples into a clean container for transport to the
laboratory. Other disposable items such as used gloves, 3MTM Sponge-Stick handles,
Whirl-Pak bag tear strips, used Eco-WipeTM FCS wipes, and other items should be discarded in appropriate trash containers or another bag or container designated for that
purpose. These items should not be placed in the same container used to collect the
sealed sponge samples.
After sampling, immediately transport the samples to the laboratory and refrigerate
until they are tested. Samples should ideally be tested on the same day that they are
collected. In the case of shipping samples to an external laboratory, samples should
be tested no more than 48 hours after they have been taken. If samples are shipped
to an external testing laboratory, they should be appropriately packed with ice packs.
The receiving laboratory should check the temperature upon receipt to make sure
the samples did not warm up during shipment. Receiving temperatures should be no
higher than 45F upon receipt.
A negative control sample should be included with each batch of environmental samples taken. This is done by removing the sponge from the Whirl-Pak bag or container using sterile gloves and then replacing it back into the bag or container. It should
be coded such that the testing laboratory does not know that it is a negative control
sample.

Procedures for sampling equipment and environmental surfaces for total Enterobacteriaceae counts (indicator organisms)
It is recommended that preoperational Zone 1 surfaces be routinely tested for total Enterobacteriaceae (TEB) counts as part of your PEM program in lieu of Salmonella testing.
Zone 1 surfaces could be tested for Salmonella spp. However, if tested, the product made

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P R I N C I P L E S O F A PAT H O G E N E N V I R O N M E N TA L M O N I TO R I N G P R O G R A M

on that line must be held (if there is no documented sanitation break) until testing results
are available. The use of TEB counts obviates the need for hold-and-release testing of
product but can yield extremely valuable information regarding the hygienic status of the
almond-processing lines and equipment. The following procedure for sampling environmental and equipment surfaces for TEB counts should be used as a guide:
1.

2.
3.
4.

5.
6.

7.

8.

Prelabel the sponge sample bags or swab sample containers using a predetermined
coding or numbering system. Make sure site descriptions indicate from which zone
each sample is taken.
Thoroughly wash and dry hands. Sanitize hands with an appropriate hand sanitizer.
Put on sterile gloves.
Using sterile gloves, remove the sponge, the swab or 3MTM Sponge-Stick from the
Whirl-Pak bag or container.
Grasping the sponge or swab and using constant pressure, sponge an area of 200
square inches. If swabs are used, swab an area of 40 square inches. To facilitate accurate coverage of the area, a nonporous plastic template may be used. The template
should be sanitized using a suitable sanitizer such as Eco-WipeTM FCS wipes between
sampling sites. Replace the sponge back into the Whirl-Pak bag or container and
seal it. Smaller areas may be sampled with the sponge method if it is not possible to
sample a 200 square inch area. The counts per unit area must be adjusted if that is
the case.
Change gloves between sponge samples and use an alcohol-based sanitizer to minimize the potential for cross-contamination.
When Zone 1 sites are sampled with premoistened sterile sponges or swabs, the site
should be wiped down with an alcohol-based sanitizer after sampling is done. EcoWipeTM FCS single-use quaternary/alcohol-based wipes (http://www.ecolab.com) are
particularly useful for this purpose. These are approved for nonporous food contact
surfaces and are useful in returning the area swabbed back to hygienic condition,
including removing any small amounts of residual liquid left by the premoistened
sponge.
Place the collected, sealed sponge or swab samples into a clean container for transport to the laboratory. Other disposable items such as used gloves, 3MTM SpongeStick handles, Whirl-Pak bag tear strips, used Eco-WipeTM FCS wipes and other items
should be discarded in appropriate trash containers or another bag or container
designated for that purpose. These items should not be placed in the same container
used to collect the sealed sponge samples.
After sampling, immediately transport the samples to the laboratory and refrigerate
until they are tested. Samples should ideally be tested on the same day that they are
collected. In the case of shipping samples to an external laboratory, samples should be
tested no more than 48 hours after they have been taken. If samples are shipped to an
external testing laboratory, they should be appropriately packed with ice packs. The
receiving laboratory should check the temperature upon receipt to make sure the samples did not warm up during shipment. Receiving temperatures should be no higher

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P R I N C I P L E S O F A PAT H O G E N E N V I R O N M E N TA L M O N I TO R I N G P R O G R A M

9.

10.

11.

12.

than 45F upon receipt.

A negative control sample should be included with each batch of environmental samples taken. This is done by removing the sponge from the Whirl-Pak bag or container using sterile gloves and then replacing it back into the bag or container. It should
be coded such that the testing laboratory does not know that it is a negative control
sample.
Samples should be quantitatively sampled for TEB counts per the procedures outlined in the Compendium of Methods for the Microbiological Examination of Foods
(57). One convenient method is to employ the use of the 3M PetrifilmTM method for
conducting TEB counts.
Sponge samples are analyzed by adding
100 ml of sterile diluent (e.g., letheen neutralizing broth) to the sample bag. Vigorously massage the sponge for one minute or more to release the microorganisms
and plate according to the TEB method used. If swab samples are taken, vigorously
shake the container holding the swabs by making 50 complete cycles of 15 cm in 10
seconds, striking the palm of your other hand at the end of each cycle. Plate according to the TEB method used. Counts should be calculated and reported per unit area
sampled (e.g., TEB count per 200 square inches or TEB count per 40 square inches).
When unmeasured surface areas such as pipe interiors, nozzles, valves or gaskets have
been swabbed, the results should be reported on the basis of the entire sampling site
and reported as TEB count per swab or sponge.

Conduct a hygiene zone assessment

A team knowledgeable with the layout of the manufacturing operation should walk the
plant floor to determine sampling locations. As discussed in section 2, the plant should
be segregated into hygiene zones based on the Primary Salmonella Control Area (PSCA)
concept. In almond-processing facilities, the PSCA is the area where the post-lethalitytreated product is exposed to the environment, such as sorting and packing lines, and
final packaging areas. These areas are sometimes referred to as the ready-to-eat (RTE)
area, the critical side of the operation, or the high-hygiene or high-risk area. Examples
of almond plant layout with different levels of hygiene zones are shown in Figure 4. The
objective of hygiene zones is to identify areas of high and low risk within the manufacturing operation. Once these hygiene zones have been identified, specific pathogen control
measures and monitoring programs can be developed. The focus is to prevent the spread
of Salmonellae into the PSCA where protection of the exposed post-lethality treatedproduct is critical.
Depending on the type of operation, an almond-processing or manufacturing facility can be
divided into one, two or three hygiene zones in addition to the nonprocessing areas. These
areas would typically be the PSCA, the basic GMP area and a transition area between the
two. An example of a transition area might be between a PSCA and pre-lethality step processing as a basic GMP zone.

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P R I N C I P L E S O F A PAT H O G E N E N V I R O N M E N TA L M O N I TO R I N G P R O G R A M

Figure 4. Examples of Almond Plant Layouts layout With Different Levels of Hygiene Control. Primary Salmonella Control Area (PSCA) in yellow and basic GMP
area in gray. White areas are non-process areas (adapted from Reference 48).

Brown Skin Facility With Huller/Sheller

warehouse 1
receiving raw
product

warehouse 2
finished goods

brown skin box

packing area

brown
skin bin
packing
area

transitional
area

hand sorting room

office
office

hall
rest
room

electronic
sorting,
metal
detection
area

hulling
and
shelling

incoming
brown
skin
staging
area

sizing

office
employee area
locker rooms/rest rooms

Primary Salmonella
Control Area (PSCA)

Basic GMP Area

Nonprocess Area

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P R I N C I P L E S O F A PAT H O G E N E N V I R O N M E N TA L M O N I TO R I N G P R O G R A M

hand
brown
sorting
skin
line
packing
area
area

office

raw
materials
incoming
product
staging

transitional
area

hall

rest
rooms

employee
break
room

Handling Facility With Treatment/Pasteurization

roaster
line 1
area
finished
goods
warehouse

roaster
line 2
area

incoming
product
warehouse

blanching
line 2
area

Primary Salmonella
Control Area (PSCA)

roasted/
blanched
packing
area

Basic GMP Area

Nonprocess Area

Custom Pasteurization Facility

pasteurization
unit

raw
product
receiving
staging
area

packing
area

cooling
chamber
conveying unit

employee
break room

rest
room

transitional
area 2

rest
room

transitional
area 1

finished product
staging area

rest
room

office
main entrance

Primary Salmonella
Control Area (PSCA)

28

Basic GMP Area

Nonprocess Area

P R I N C I P L E S O F A PAT H O G E N E N V I R O N M E N TA L M O N I TO R I N G P R O G R A M

The team should conduct a hygiene zone assessment of the entire facility and create a color-coded map of the facility using the following procedure:
Q Survey the entire facility, including all production areas, storage, receiving, warehousing
and loading docks, as well as employee facilities such as cafeterias, break rooms, locker
rooms, washrooms, maintenance areas, offices and conference rooms, and others.
Q Designate the PSCA, basic GMP areas, transition areas (if any) and nonprocessing areas.
Q Pay particular attention to areas within the facility where ingredients, products or the
environment could be a potential source of pathogen contamination and have a high
risk to cross-contaminate post-lethality-treated product. Also pay attention to nonprocess areas such as refuse and recycling, restrooms, forklift battery charging stations, boiler rooms, and others that could impact the PSCA.
PEM sampling site selection and frequency of monitoring
Once the team has mapped out the hygiene zones within the manufacturing facility, it
is now time to select the specific sampling sites within each area using the zoning concept discussed in section 3.2. Environmental sampling for Salmonellae is routinely conducted in Zones 2, 3 and 4. Zone 1 surfaces are normally tested for indicators such as TEB
counts. Only under special situations are Zone 1 surfaces sampled for Salmonellae, such
as investigational sampling due to a potential contamination events such as a roof leak or
a finished-product Salmonella-positive result. Zone 1 surfaces could be routinely sampled
for Salmonella; however, any Zone 1 testing for Salmonella or other specific pathogens
necessitates a stringent product hold program until results are received. Testing Zone 1
surfaces for TEB counts or other appropriate indicators obviates the need for a finishedproduct hold program.
Table 1 summarizes examples of sampling sites, type of microbiological test and minimum
recommended frequency of testing by zone. Also note that a Zone 1 designation may be
given to equipment surfaces and building structures (e.g., beams, catwalks, overheads,
ceilings, covers, conduit, HVAC units, pipes, etc.) that are directly above product-contact
surface. The assessment team, working together, should determine whether a surface
above a direct product contact surface constitutes a Zone 1 surface. This determination
will depend on a number of factors including the likelihood the surface will contaminate
the product immediately below it (e.g., and condensate formation, dust collection, etc.),
the ability to effectively clean and sanitize the surface on a regular basis, among others.
The number and location of environmental samples taken is determined by the risk levels
inherent to the product and process. Areas with water use, high traffic patterns, a history
of positive pathogen results, and areas where microbiologically sensitive raw materials are
handled or stored should be sampled at a higher frequency. Focus should be given to postlethality-treated open product areas (PSCAs) since this is where the risk of product recontamination is highest. In general, this will equate to a greater number of samples collected in

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Zone 2 and Zone 3 areas than are taken in Zone 4 areas. Sample sites should be identified
and rotated weekly according to shift and the day of the week. A rotation schedule should
be developed to allow all locations within Zones 1, 2 and 3 to be covered within a month.
Zone 4 sites should be rotated so that all sites are covered within a quarter. The sampling
plan must be flexible to allow for additional samples to be taken, as determined by the team.
The overall number of PEM samples taken each week depends on the size of the facility and
on the historical data from the facility.
Establishing your baseline: investigational sampling
Once potential areas for sampling are identified, it is useful to conduct preliminary intensive investigational sampling with the purpose of finding the target pathogen if it is there.
In the preliminary investigational phase, environmental samples are collected at a higher
frequency and number than is done for the ongoing PEM program. The selection of
samples is typically based on the experience of the investigator and the type of process
under consideration. Depending on the size and complexity of the operation, it is not
uncommon to take 25 to 50 samples or more per zone per day for the first month (rotating shifts in a multiple shift operation), then moving to a weekly schedule with the same
number of samples for the next two to five months. It is highly recommended that you
use a combination of indicator organisms and Salmonellae testing as part of your PEM
program. There are a number of indicator tests that you can use for your PEM program.
As previously discussed, it is recommended that you use total Enterobacteriaceae (TEB)
counts as your indicator test for evaluating Zone 1 and other surfaces. Whether you use
TEB counts or coliform counts as your quantitative indicator method, it is very important
to determine the baseline counts that would be expected under normal operating conditions and what counts that would be unacceptable. This entails doing work to establish
your baseline counts and action levels for counts that deviate from the baseline.
Zone 1 sites are normally tested for TEB counts preoperationally, before sanitizing and prior to start-up of the production line. Sampling after cleaning but before applying sanitizer
is a good measure of cleaning effectiveness. If Zone 1 sites are sampled after the sanitizer
step, then be sure to use a neutralizing buffer for the sample sponges or swabs, as previously discussed. Zone 1 sites should be tested individually and never composited. Zone 1
sites may be sampled during production, but this will require careful analysis and establishment of baseline data. This requires collecting TEB count data on your post-lethalitytreated product to determine the expected baseline TEB level. One approach would be
to sample Zone 1 sites intensively for six months to establish baseline levels (preliminary
investigational sampling). Any significant deviation (e.g., 1 log) above the baseline level
constitutes a special cause for corrective action. The team needs to take into consideration variables such as seasonality, geographic differences and supplier source that can
impact the baseline. In general, depending on the degree of post-lethality treatment, the
TEB levels should be very low in the product. The team needs to decide if it adds value to
sampling Zone 1 sites during production, versus taking more Zone 2 and 3 samples during

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TABLE 1: PEM sampling site examples, type of microbiological test, minimum sampling
frequency, and typical number of samples by zone.
Microbiological
Test

Minimum
Frequency of
Sampling

Typical
Number of
Samples1

Zone

Examples of Sampling Sites

Direct or indirect product contact surfaces2, e.g., sorting lines, product conveyors product discharge chutes,
pipeline interiors, storage hoppers, filler hoppers, nozzles,
product scrapers/utensils, employee hands handling product

Indicator organisms, e.g. Total

Enterobacteriaceae Counts
(TEB), total coliform counts. Salmonella testing
normally only
under special
situations

Weekly, postcleaning prior

to sanitizer application and
start-up. Also,
as needed for
investigational,
validation and/
or verification
purposes

Line
Dependent

II

Environmental surfaces immediately adjacent to product

contact surfaces, e.g., equipment framework/supports,
outside of tunnels or filling cabinets, below filling equipment, control panels, motor housings, catwalks, scales,
scrap containers, drains near zone 1 surfaces, HVAC vents

Salmonella

Weekly

10 - 15

III

Environmental surfaces further removed from product

contact surfaces in open product areas, e.g., hand trucks,
forklifts, walls, ductwork, drains, floors, ceilings, equipment
legs, tools, brooms, squeegees, floor scrubbers, trash containers, pallets, floor debris, ceiling drain pipes, wash stations, ingredient storage areas, wall/floor junctures

Salmonella

Weekly

10 - 15

IV

Areas remote from the processing area, e.g., warehouses,

bathrooms, locker rooms, maintenance areas, cafeteria/
break rooms, loading docks, boiler room, offices, plant entrance, refuse/recycle areas

Salmonella

Monthly

5 - 10

1
In general, the same or greater numbers of samples are taken in zone 2 than zone 3, and in zone 3 than zone 4. Larger or more complex operations may require more samples taken per zone than shown here.
2
Direct product contact surfaces (PCS) are surfaces exposed to product during normal equipment operation. Indirect
product contact surfaces are surfaces from which liquids or dust or other material may drain, drop, diffuse, or be
drawn into the product or into the container, and surfaces that touch product contact surfaces or the product container

production, combined with a finished product testing program. In some cases, processing equipment such as sorting lines and conveying systems can contain harborage niches
that can be detected only while in operation. If this is a concern, an alternative would be
to run operational Zone 1 testing as part of a periodic verification program rather than
part of the routine PEM program. Also, consideration must be given to weighing the potential risk of inadvertent cross-contamination of Zone 1 sites via sampling during production against the insights gained from the data through collecting operational Zone 1 samples. Factors such as ease of collecting the sample, implications of temporarily shutting
down the line for sample collection and others must be considered before implementing
Zone 1 sampling during production.
Zones 2 and 3 samples should be collected both preoperationally and operationally for
Salmonella. Operational samples should be taken throughout the production run (for example, just after start-up, three or four hours after start-up, and at the end of the run).

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These sampling times and sites can be rotated from week to week.
Zone 4 samples should typically be collected monthly. The focus should be on sites that
are adjacent to open product areas or where traffic (people and materials) flows into
or out of open product areas (PSCAs). Remote locations such as locker rooms, loading
docks, warehouses, cafeterias and break rooms, and other areas should also be included.
Employee lockers, if not properly cleaned and maintained, have been shown to be a
source of Salmonella contamination. The intent of Zone 4 sampling is to identify potential
harborage sites of the pathogen that could ultimately become a source for spreading it
throughout the production facility.
Once swab locations are selected, a master list can be compiled by zone throughout the facility. Each zone can be mapped for tracking purposes and entered into a master database.
A generator of random numbers can be used to select swab locations to be sampled each
week; however, you should ensure that each location is sampled rotationally so that they
are sampled at least four times, minimum, within a year. The same exact location within a
zone should not be sampled each time samples are collected unless data has shown it to be
a chronic problem location. The sampling plan needs to be flexible, allowing for additional
sample collecting based on the data obtained. The concept of follow the data should be
practiced at all times. A PEM program is dynamic and should be responsive to the data
generated by sampling.
Microbiological methods available for testing PEM samples
There are myriad microbiological methods available for the analyses of PEM samples.
Whatever method is selected, it is absolutely imperative that you validate the method on
your samples for your specific applications. It is recommended that you use an official or
industry-recognized method for testing samples. In the United States, the methods in the
FDAs Bacteriological Analytical Manual (BAM) are considered official methods for the
testing described in this guidance document (63). Other official and/or industry-recognized methods include:
Q ISO 6579 methods, which are considered official methods in Europe, but are increasingly recognized around the world (64)
Q American Public Health Associations Compendium of Methods for the Microbiological
Examination of Foods (57)
Q AOAC Internationals Official Methods of Analysis (65)
There are also country-specific and industry-specific methods published, but most of the
above-cited method references are universally recognized and accepted. Methods that
have been validated and found to be equivalent in specificity and sensitivity to these officially recognized methods may be used; however, you need to make sure the methods
are properly validated.

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There are a number of rapid methods available for the detection of Salmonellae in environmental, ingredient, and in-process or finished-product samples. Many of these methods are immunological-based Enzyme Linked Immunosorbent Assays (ELISAs) that utilize
specific antibodies for capture of the Salmonellae, modified cultural methods that often
utilize selective and differential media for the isolation and identification of Salmonellae,
and genetic-based methods such as the Real Time Polymerase Chain Reaction (RT-PCR)
assays that target gene sequences specific to Salmonellae. All of these methods have advantages and disadvantages and must be carefully considered and thoroughly validated
before being used for your samples. A validated rapid method is generally considered a
screening method, where negative results are accepted as such, but positive results need
confirmation (either cultural or by some other recognized method). Its advisable to proceed based on a presumptive Zone 1 positive result from an environmental sample from
a cleaning, sanitation and product disposition perspective. This approach is the most
conservative, gaining you time for cleaning and sanitation and other interdictive steps if,
indeed, it turns out to be a confirmed positive result.
Never composite environmental samples by combining multiple sponges or swabs into
one pre-enrichment. This practice may make it difficult to detect low levels of Salmonellae present in one sample because of increased background competitive microflora leading to a false negative result. Also, a positive result on a composited sample does not
allow you to identify the specific location(s) that are positive for Salmonellae. This makes
troubleshooting more difficult and results in broader corrective actions than otherwise
would be needed.

H A N D L E R

sterile
bag

sterile
bag

pre-enrichment

selective enrichment

L A B O R A T O R Y

It is highly recommended that all Salmonella isolates be serotyped and characterized by

a genetic typing method such as pulsed-field gel electrophoresis (PFGE), ribotyping, or
another validated and recognized method. Genetic typing methods are very useful in
troubleshooting and tracking data from your PEM program. Genetic typing maps can be
developed showing hot spots or problem areas in the plant. These maps are usually set
up using blueprints or diagrams of the relevant areas according to zones. It should be
understood that it is possible for multiple strains of Salmonella to be isolated from an en-

sterile
bag

Environmental samples may be pooled by combining up to 10 post-enriched samples into

one sample to run a rapid method such as RT-PCR or ELISA. The Pathatrix Auto is a commercially available system from Matrix MicroScience (www.matrixmsci.com) and approved
by the Association of Analytical Communities Research Institute (AOAC RI). Its based on
recirculating immunomagnetic separation and allows for the efficient pooling of environmental samples. If pooled samples yield a Salmonella-positive result, the individual pre-enrichment samples comprising the pooled sample are run individually to identify the positive
sample(s). Sample pooling has the advantage of significantly reducing the per-assay cost of
running samples. It is recommended that only samples from the same zone be pooled for
testing purposes. As with most rapid methods, the ability to pool samples is method-dependent and must be thoroughly validated for your specific applications.

swabs

petri dish

Sample pooling

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P R I N C I P L E S O F A PAT H O G E N E N V I R O N M E N TA L M O N I TO R I N G P R O G R A M

vironmental sample. Multiple strains of Salmonella have been isolated from raw nuts and
from production areas (33). Therefore, the presence of one strain of Salmonella in product and a different strain in the production environment does not necessarily mean they
have no commonality.
If your operation does not have its own microbiological testing laboratory, you should use
a reputable accredited independent testing laboratory. There are a number of resources
available to help you choose a properly accredited independent food microbiology testing
laboratory. The AOACs Analytical Laboratory Accreditation Criteria Committee (ALACC)
has published Laboratories Performing Microbiological and Chemical Analyses of Food
and Pharmaceuticals (ALACC Guide) which are guidelines based on the ISO 17025 requirements. Up-to-date information on these requirements may be found at http://www.
aoac.org/accreditation/faq2.htm. Other valuable resources that can be used in helping
you find accredited food microbiology testing laboratories include the American Association for Laboratory Accreditation (A2LA) (http://www.a2la.org/appsweb/food.cfm) and
the American Council of Independent Laboratories (ACIL) (http://www.acil.org/). The
value of using accredited laboratories is to ensure that they are producing accurate, reliable and consistent results using properly validated methods. There are also a number of
independent expert consultants that can be used to help you find and qualify a properly
accredited laboratory.
Data interpretation and corrective actions
Once preliminary investigational data is collected, it must be analyzed and interpreted. Intensive data from the preliminary investigational phase is used to set up the ongoing PEM
program. Data, during the preliminary investigational phase, should be continually monitored and used to guide ongoing sampling during that phase. If an area shows repeated
positives, then that area should be considered a potential harborage or problem area that
warrants continued attention. Once the ongoing PEM program is initiated, based on the
intensive data analyzed from the preliminary investigational phase, the frequencies and
typical number of samples per zone outlined in Table 1 may be implemented. It is critical
that corrective actions be implemented and documented whenever a Salmonella positive
occurs. With most environmental samples it is recommended that corrective actions be
initiated when a presumptive Salmonella result occurs. As discussed previously, this is the
most conservative route, gaining time in the event the sample is confirmed positive for
Salmonella. Confirmation can take up to a week; therefore, taking action on a presumptive positive minimizes your risk exposure while you wait for confirmed results.
The following are key considerations relative to taking proper corrective actions:
Q Your facility should have a predetermined action plan that would be implemented in
the event of a Salmonella-positive environmental sample result. The action plan should
be specific for each of the four zones and include protocols for:
- The type of immediate corrective actions to be taken by zone

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- Actions taken to verify that Salmonella has been eliminated from the area in question
- An analysis to find the root cause of the contamination so that it can be prevented
in the future
Q All corrective actions, including additional sample results, need to be properly documented. It is extremely useful to have a computer-based spreadsheet for tracking results and documenting corrective actions.
Q If a positive result is found in any sampling zone, the area needs to be thoroughly examined both visually and through vector swabbing to determine the extent of the contamination and to ascertain potential causes of the problem. Vector swabbing entails
taking additional multiple environmental samples around the initial positive site. Vector
sampling is usually done in a typical star-burst pattern around the initial positive site
as shown diagrammatically in Figure 5. Typically, 10 to 15 additional sponge or swab
samples are taken around the initial positive sites. Sampling, where possible, should radiate out from the initial positive site in all directions, including up and down, if appropriate. Troubleshooting samples are usually run as separate samples and not pooled as
discussed in section 3.8.
Q The specific corrective actions taken are based on an assessment of the likelihood
of finished-product contamination based on the location of the initial positive site. A
positive finding in Zones 2, 3 or 4 does not necessarily implicate finished product. That
decision should be made by the team and appropriate management personnel.

Figure 5. Vector Sponge/Swab

Sampling Starburst Pattern
Around the Initial Salmonella
Presumptive Positive Site.

initial
positive site

Hot
spot

Starburst
sampling
pattern

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P R I N C I P L E S O F A PAT H O G E N E N V I R O N M E N TA L M O N I TO R I N G P R O G R A M

Table 2 provides some examples of corrective actions following the initial positive Salmonella result in the plant environment. You should have a predetermined cross-functional
response team in place to conduct follow-up investigations on Salmonella positive findings.
The response team should consist of members from Microbiology/Food Safety, Quality
Assurance, Sanitation, Operations, Engineering, Maintenance, Management and other disciplines, as appropriate. All key personnel that can help troubleshoot find the root cause
of the problem and correct it should be part of the response team. The focus is on finding
and eliminating all potential sources of environmental contamination to the greatest extent
possible.
The response team should conduct a preliminary investigation into any positive Salmonella finding to determine potential sources of contamination. A report should be compiled that details all maintenance disruptions and activities, in-plant construction, unplanned line downtime or other nonstandard production activities (e.g., plant
R & D trials) in the area from the last full microbiological cleanup or sanitation to the current positive finding. Immediate actions should be taken to correct any obvious GMP or
other deficiencies based on the findings including:
Q Quarantine the suspect area and limit access to minimize spreading the contamination
to other parts of the plant.
Q Reinforce hygienic practices among employees, outside contractors and others, and retrain in GMPs and principles of food safety, if necessary.
Q Assess and adjust the type and frequency of cleaning and sanitation procedures, if
needed.
Q Eliminate sources of water and water accumulation, if found.
Q Repair structural damage (e.g., on floors, walls and other structures) as necessary.
Q Reexamine traffic patterns (both personnel and materials) and redirect them,
if feasible.
Q Audit handling practices (production, sanitation, maintenance and material handling)
and make adjustments where necessary.
Q Redesign and/or perform equipment maintenance as necessary.
Q Conduct interdictive cleaning such as floor scrubbing and sanitation, or cleaning of
overhead pipes and equipment.

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P R I N C I P L E S O F A PAT H O G E N E N V I R O N M E N TA L M O N I TO R I N G P R O G R A M

TABLE 2: Examples of corrective actions by zone that should be taken after initial Salmonella positive environmental result
Zone I Corrective Actions
Product should always be placed on hold if zone 1 Salmonella testing is to be done
Quarantine the suspect area and limit access to that area
Break down the line from the initial positive site on for visual inspection, additional vector
sponge/swab sampling, and cleaning and sanitation activities
Conduct vector sampling in zones 1, 2, and 3 around the area of the initial positive result prior to
cleaning. Precaution should be taken not to spread contamination to other areas of the plant
Thoroughly clean and sanitize the line and surrounding area using dry, controlled wet, and/or wet
cleaning procedures appropriate for low moisture environments (47, 49)
Conduct pre-operational inspections on the line equipment and area prior to start-up and take
additional vector samples of the area prior to start-up. It is highly advisable not to start-up the
line until all vector sampling results are obtained (if the line is started prior to obtaining all vector
sampling results, then product must be put on hold until negative results are obtained)
Increase the frequency of intensive sampling of the line and adjacent areas from weekly to daily
(zones 1 3). After three consecutive days of negatives are obtained, the normal routine PEM
sampling plan may be reinstituted
The response team should make a careful decision on disposition of finished product that is put
on hold as a result of a zone 1 positive Salmonella finding. All finished product from full microbiological clean-up/sanitation to full microbiological clean-up/sanitation must be addressed by the
team. Product should be re-worked, if possible, or condemned according to all legal and regulatory statutes. It is not an acceptable practice to test lots of finished product for Salmonella in response to a confirmed zone 1 result for the purposes of releasing product.

Zone II Corrective Actions

Stop production and prepare the system for cleaning and sanitation
Quarantine the suspect area and limit access to that area
Break down the line from the initial positive site on for visual inspection, additional vector
sponge/swab sampling, and cleaning and sanitation activities
Conduct vector sampling in zones 2, and 3 around the area of the initial positive result prior to
cleaning. Precaution should be taken not to spread contamination to other areas of the plant
Thoroughly clean and sanitize the line and surrounding area using dry, controlled wet, and/or wet
cleaning procedures appropriate for low moisture environments (47, 49)
Conduct pre-operational inspections on the line equipment and area prior to start-up and take
additional vector samples of the area prior to start-up. Do not restart the line until satisfactory
vector swab results have been obtained.
Increase the frequency of intensive sampling of the line and adjacent areas from weekly to daily
(zones 2, 3). After three consecutive days of negatives are obtained, the normal routine PEM
sampling plan may be reinstituted

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P R I N C I P L E S O F A PAT H O G E N E N V I R O N M E N TA L M O N I TO R I N G P R O G R A M

Zone III Corrective Actions

The response team should make the decision whether or not to stop production based on the
proximity of the initial positive site to product contact areas
Quarantine the suspect area and limit access to that area, if feasible
Visually inspect the area and conduct additional vector sponge/swab sampling prior to cleaning
and sanitation activities
Conduct vector sampling in zones 2, and 3 around the area of the initial positive result prior to
cleaning (zone 2 sampling is done to ensure that contamination has not spread closer to open
product areas). Precaution should be taken not to spread contamination to other areas of the
plant
Thoroughly clean and sanitize the area (at least a 50 foot radius, if possible) using dry, controlled
wet, and/or wet cleaning procedures appropriate for low moisture environments (47, 49)
Conduct pre-operational inspections on the line equipment and area prior to start-up and take
additional vector samples of the area prior to start-up. Do not restart the line until satisfactory
vector swab results have been obtained.
Increase the frequency of intensive sampling of the line and adjacent areas from weekly to daily
(zones 2, 3). After three consecutive days of negatives are obtained, the normal routine PEM
sampling plan may be reinstituted

Zone IV Corrective Actions

A Salmonella positive finding in a zone 4 location does not implicate finished product, but it
does provide information on non-production areas and the potential for spread of contamination
throughout the facility
Quarantine the suspect area and limit access to that area, if feasible
Visually inspect the area and conduct additional vector sponge/swab sampling prior to cleaning
and sanitation activities
Conduct vector sampling in selected zone 3 areas adjacent to the location of the initial zone 4
positive location, if appropriate, and zone 4 sites around the area of the initial positive result prior
to cleaning (selected zone 3 sampling is done to ensure that contamination has not spread closer
to open product areas). Precaution should be taken not to spread contamination to other areas
of the plant
Thoroughly clean and sanitize the area (at least a 50 foot radius, if possible) using dry, controlled
wet, and/or wet cleaning procedures appropriate for low moisture environments (47, 49)
Take additional vector samples of the area after cleaning and sanitation to verify effectiveness of
those procedures
Increase the frequency of intensive sampling of the areas from monthly to daily (zone 4 and selected zone 3 areas adjacent to the location of the initial zone 4 positive). After three consecutive
days of negatives are obtained, the normal routine PEM sampling plan may be reinstituted.

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It would not be unexpected to occasionally find a Salmonella-positive result in Zone 4

areas such as high-traffic hallways and employee locker rooms. However, a positive finding needs to be aggressively addressed in order to minimize the potential for spread of
the pathogen to other parts of the facility. A Zone 3 positive in the absence of any Zone
2 positives should be considered as an early indication of the need to make the cleaning
and sanitation program more robust or to address other potential issues in the plant like
traffic flow, and structural or maintenance issues.
If vector samples test positive for Salmonella in any zone, then additional samples must
be taken to define the scope of the problem. Additionally, aggressive actions must be undertaken to eliminate the problem. The finding of persistent problem areas or hot spots
over time is an indication that the primary contamination source may be a harborage site
where the pathogen has established itself and may be multiplying. In the case of repeated or persistent problem areas, aggressive corrective actions must be taken to contain
and correct the problem. The following steps should be taken as part of the root cause
analysis by the response team:
Q Map the locations of positive samples on a facility diagram to help define the scope of
the problem.
Q Implement daily vector sampling of the environment until the situation is corrected.
Q Restrict traffic flow in these areas to the extent possible.
Q Visually inspect areas for potential harborage sites and intensify cleaning efforts in these
areas
Q Reinforce GMP and food safety practices with line operators and other personnel.
Q Visually monitor handling practices (production, sanitation, maintenance, material handling) and make adjustments where necessary.
Q Scrutinize equipment cleaning and preventive maintenance practices, then modify if
necessary.
Q Repair structural damage (e.g., floors, walls, other structures) as necessary.
Q Redesign and/or perform equipment maintenance as necessary.
Q Zone 1 sampling or finished-product testing may need to be implemented or intensified in the event of persistent Zone 2 positives.
In extreme cases where a hot spot cannot be eliminated or contained, serious consideration must be given by the response team to taking that production line or piece of
equipment out of service and physically restricting or segregating that area from the rest
of the plant until a permanent solution can be found.
When using a quantitative indicator such as TEB or coliform counts, none of these organisms should be present on equipment after cleaning and sanitation activities. Table 3
lists recommended guidelines for aerobic plate count coliform and TEB counts on clean
equipment surfaces before and after application of sanitizer. Typically, preoperational
sampling is done after cleaning but before application of sanitizer. This gives a better in-

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P R I N C I P L E S O F A PAT H O G E N E N V I R O N M E N TA L M O N I TO R I N G P R O G R A M

dication of the effectiveness of cleaning. Samples that are taken after application of sanitizer must include the use of proper neutralizing solutions as discussed in section 3.4.1 to
ensure that residual sanitizer does not inhibit recovery of injured cells, if present.
If operational samples are collected for TEB or coliforms, it is critical that a baseline be
established under normal operating conditions, as discussed in section 3.7. An upward
trend or a sudden deviation from the established baseline would be cause to initiate an
investigation and corrective actions. The response team must carefully evaluate trend
data over time to establish what constitutes a significant trend.
Table 3. Recommended Microbiological Indicator Limits for Equipment Cleaning Before
and After Application of Sanitizer
Quantitative
Microbiological Indicator
Test
Aerobic Plate Count

Coliforms

Total Enterobacteriaceae

Target/
Acceptable Limits

Post-Heat Treatment
Taken Before Sanitizer
(cfu/40 in2)

Post-Heat Treatment
Pre-op Taken After
Sanitizer (cfu/40 in2)

Target

< 100

< 10

Acceptable

< 500

< 100

Target

< 10

< 10

Acceptable

< 100

< 50

Target

< 10

< 10

Acceptable

< 100

< 50

Plant construction, equipment installation, and major repairs

It is well documented that activities such as plant construction, equipment installation
and major repair work can lead to increased recontamination risk to the product if not
properly managed. In the event of such activities, increased control procedures are required, including:
Q Setting up temporary control barriers within the plant, as appropriate. This may include
physically separating the area through the use of temporary walls, ceiling-to-floor plastic curtains or other suitable containment barriers.
Q Modifying traffic flow in the area to minimize the risk of spreading contamination
throughout the rest of the facility.
Q Increasing the amount of cleaning and sanitation during construction or equipmentrelated activities.
Q Reinforcing GMP and hygiene practices with plant personnel and, especially, outside
contractors.
Q If used equipment from outside the plant is installed, it is highly recommended that the
equipment be cleaned and sanitized before it enters the plant. The effectiveness of the
cleaning and sanitation should be verified through sponge or swab sampling before

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THE ROLE OF AUDITS IN MANAGING A PEM PROGRAM

installation.
Q Airflow and air pressure in the area should also be evaluated and adjusted if necessary
to minimize airborne transmission of dust and contaminants.
Sampling the environment for Salmonella should be performed during construction or
other major activities at an increased frequency and number to ensure that no problems are being created. Sampling sites and frequency should be determined by the team
based on an evaluation of:
Q Location of construction or other activities.
Q Type of construction or activity (e.g., demolition, installation, major repair, material
removal).
Q Time duration of the activities.
Q Types of environmental controls implemented.
Once construction or major equipment-related activities are completed, the area needs to
be thoroughly cleaned and sanitized. Verification of cleaning and sanitation effectiveness
must be performed by intensively sampling the area for Salmonella contamination before
the area is released for production activities. An aggressive PEM protocol should be followed during commissioning of the area or equipment. Depending on the magnitude of
the construction or major activities, this often entails taking hundreds of sponge or swab
samples of the environment. If positive results are obtained, then the area or equipment
must be recleaned/resanitized and resampled until negative results are obtained.

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THE ROLE OF AUDITS IN MANAGING A PEM PROGRAM

The Role of Audits in Managing

a PEM Program

he food industry has become increasingly reliant on independent third-party

audits and certification to ensure that their processes, personnel and establishments conform to food safety and other standards. However, third-party audits
have recently come under fire due to several large-scale food-borne outbreaks
linked to establishments that have received high scores from third-party auditing firms
including the 20082009 peanut butter outbreak caused by the Peanut Corporation of
America (37, 66). There are a number of factors that have led to this variability in the
quality and consistency of food safety audits:
Q Differences in Experience Levels of Individual auditorsEven though auditors may be
specific to a segment of the food industry (e.g. almond handling and processing), their
experience level can vary greatly. This can lead to difficulties in asking the right questions or in focusing on the right issues.
Q Auditors Are Not Jack-of-All-TradesIt is very rare to find an auditor experienced in
all the various aspects of engineering that are germane to food processing, including
process, packaging, mechanical, electrical, and design or system engineering. Most
auditors are not experts in product formulation, food processing, sanitary design, microbiology and food safety, or other relevant disciplines. Many auditors come from a
quality-assurance background rather than a food safety background.
Q Time and CostMany audits are done in one day or less. This is definitely not enough
time to conduct a comprehensive food safety audit. Some companies look for the
cheapest alternative, which can lead to glaring mistakes.
Q Deceit on Part of the Facility Being Audited It is extremely difficult for auditors to
address withheld information or data that is pertinent to the audit or to pick up on fabricated or falsified data.
Q Too Much Paper Review and Not Enough Time Spent on the Plant FloorAuditors
must strike a balance between documentation review (which is important) and time
spent in the plant observing infrastructure and practices (which is crucial).
Q Lack of Follow-UpOften, there is no or little followup by auditors to ensure that deficiencies have been addressed in a timely manner.

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THE ROLE OF AUDITS IN MANAGING A PEM PROGRAM

Q Lack of Audit DepthVirtually all audits do not encompass on-site audits of suppliers
providing ingredients and materials to the facility being audited. The same is also true
for external testing laboratories that the facility being audited may be using for microbiological and other critical testing.
Q Over-Reliance on Audits by the FacilitySome companies believe that if they pass an
audit, everything must be in order, and they become complacentuntil the next audit.
Q Announced vs. Unannounced AuditsMost third-party audits are announced, giving
the facility time to prepare for the audit. Some certification bodies and auditors provide advice to the facility on how to prepare for the upcoming audit. The audit is not
reflective of the true operating conditions in the facility.
Q Implicit Versus Explicit Conflict of InterestBoth accreditation bodies that set the audit standard and the auditing firm that certifies the facility conforms to the auditing
standard go to great lengths to try to ensure impartiality and prevent explicit conflictof-interest issues with auditors. However, most accreditation bodies and auditing firms
are for-profit entities; therefore, issues with implicit conflict of interest may persist,
since the facility undergoing the audit pays for the audit. Some auditors may tend not
to be as tough in their evaluation as they otherwise might be for fear of losing the
business.
Q Companies Do Little or Nothing With Audit ResultsSome companies do not react with
a sense of urgency in addressing audit results, particularly on those items that are characterized as minor deficiencies. Some companies even address major deficiencies such
as roof leaks with only temporary or stop-gap measures and do not devote the proper
investment and resources to the correct long-term solution.
Some skeptics believe that third-party audits are not truly independent and, by nature, are
suspect and of minimal or no value. In fact, however, third-party audits do provide value,
but you must recognize they are not infallible. The value your company gets out of thirdparty audits is directly proportional to your commitment to aggressively following through
on audit findings, including minor deficiencies. You must recognize that minor deficiencies,
if not addressed in a timely manner, at some point will become major issues. It is much better to address them when they occur rather than let them become major problems for you.
There are a number of resources available to you to use in developing or strengthening
your third-party certification program. The U.S. FDA has issued a guidance document on
voluntary third-party certification programs for foods and feeds (67). This document describes the general attributes that FDA believes a certification program should include to
provide high-quality verification of food safety. This document outlines the attributes of a
strong third-party certification program. including:
Q Authority of the certification body to perform audit activities
- Authority to examine and gather records and other information
- Authority to collect and analyze samples
- Authority to assess and report on compliance with certification criteria
Q Qualification and training of auditors

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THE ROLE OF AUDITS IN MANAGING A PEM PROGRAM

Q Effective audit program elements

- Risk-based
- Written policies and procedures
- Verification that the establishment meets certification criteria
- Process for addressing establishment complaints about audits
- Documentation and recordkeeping
Q Quality assurance program for audits and
auditors
- Field evaluation of audits to verify audits are consistent
- Audit report evaluation
- Sample report evaluation
- Individual auditor performance
Q Compliance and corrective actions
- Apply a risk-based approach to determine when an investigation, followup and reaudit are necessary
- Evaluate whether the establishment has executed proper corrective actions
- Withdraw certification if the establishment fails to take corrective actions
Q Industry relations
- The certification body (auditing company) should provide establishments seeking
certification with information about current FDA requirements and guidance
- It is preferable that the certification body be actively involved in regulatory, scientific, industry and other external activities
Q Resources
- The third-party certification body should have sufficient resources to accomplish the
elements of the certification program
Q Self-assessment of the overall certification
program
- Assesses performance and identifies strengths and weaknesses
Q Laboratories
- The certification body should have access to the appropriate laboratory services
needed to support the audit
Q Ability and willingness to notify the FDA
- Product safety issues
- Certification withdrawal
- Changes to the certification program
Q Attention to conflict of interest
- The certification body and its auditors should be free of any conflicts of interest that
threaten impartiality
An in-depth evaluation of your PEM program and data should always be a part of an
overall independent third-party audit. This also includes an in-depth review of all documented corrective actions, procedures and other information discussed in this guidance
document. The PEM program is a major tool that is critical to demonstrating the effec-

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tiveness of your facilitys GMPs, hygienic practices and food safety plan. Therefore, it is
crucial it be part of every third-party food safety audit that is conducted.
A strong third-party auditing and certification program, if conducted properly, can be a
meaningful investment and tangible evidence of your companys commitment to food
safety. In the end, the rewards you get from a strong program are directly related to the
time, diligence and commitment you put into the program.

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P E R S O N N E L E D U C AT I O N A N D T R A I N I N G A N D M A N AG E M E N T C O M M I T M E N T

Personnel Education and Training

and Management Commitment

t is incumbent upon the company to ensure that employees are properly trained in
effective GMPs, hygienic practices, food safety principles, and other practices and
procedures that enable them to do their job in an effective manner that will not
jeopardize the product or the consumer. Plant personnel can have a direct impact
on the safety of the foods produced in the facility. The risk of product recontamination
within the facility can be significantly reduced with effective training and monitoring of
ongoing employee practices.
The FDAs GMP regulations stipulate that Personnel responsible for identifying sanitation failures or food contamination should have a background of education or experience,
or a combination thereof, to provide a level of competency necessary for production of
clean and safe food. Food handlers and supervisors should receive appropriate training in
proper food handling techniques and food-protection principles and should be informed
of the danger of poor personal hygiene and insanitary practices (68). The FDA also
states, as part of its GMP modernization initiative, that ineffective training of employees
is a problem at the food manufacturer level relative to controlling microbiological hazards in foods (69). In their analysis, the FDA states that it is not clear that current training
methods are sufficient and that the training many companies conduct may be too generic. They also believe that other impediments to effective training may include training the
wrong people not training enough people or not providing enough training. The FDA has
articulated the following beliefs about training (70):

Q Food production workers should have appropriate training in the principles of

food hygiene and food protection, and this training should include the importance of employee health and personal hygiene.
Q Training must be delivered in a form that is readily understandable to all personnel and delivered in a manner that is easily understood by the trainee.
Q Food processors must maintain a record of this training for each employee.
Q Certain core principles of food safety, equipment sanitation and regulatory compliance must be included in the training of all food workers and supervisors.

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P E R S O N N E L E D U C AT I O N A N D T R A I N I N G A N D M A N AG E M E N T C O M M I T M E N T

The FDAs focus on the importance of employee health and personal hygiene is supported by the fact that many food-borne outbreaks and illnesses, including those caused by
Salmonella, have been traced to recontamination of the food directly by food handlers.
The Center for Disease Control (CDC) publishes an annual list of infectious and communicable diseases that are transmitted through handling foods (Table 4) (71). Stressing the
importance of complying with good personal hygiene and hygienic practices, including
proper hand washing, is critical in any employee GMP training program.
Table 4. CDCs List of Pathogens Transmitted by Food Contaminated by Infected Handlers
or From Food That is Cross-Contaminated During Processing or Preparation
Pathogens Frequently Transmitted by Food Through
Infected Handlers

Pathogens Occasionally Transmitted by Food

Through Infected Handlers or Through CrossContamination During Processing/Preparation

Noroviruses

Campylobacter jejuni

Hepatitis A virus

Cryptosporidium spp.

Salmonella Typhi

Entamoeba histolytica

Sapoviruses

Enterohemorrhagic
Escherichia coli

Shigella spp.

Enterotoxigenic Escherichia coli

Staphylococcus aureus

Giardia intestinalis

Streptococcus pyogenes

Nontyphoidal Salmonella
Taenia solium
Vibrio cholerae
Yersinia enterocolitica

Effective training is also a key part of a successful PEM program. Employees must understand that effective monitoring of the environment is a critical measure of the success of
the companys food safety commitment. Employees should never be discouraged from
aggressively trying to find the pathogen in the plants environment. If Salmonellae are
present in the plant environment, you want to find it. Only if you can find it can you control it and reduce the risk to the franchise and your consumers. The FDA also believes
that third-party validation of test results can be useful to further establish confidence in
your environmental sampling results (69). It is highly recommended that your company
have a qualified outside expert validate your PEM program.
You must also understand that education and training go hand-in-hand. Food safety education focuses more on the why food safety is important, and food safety training focuses more on the how to do food safety (72). The reason food safety education and training are stressed so much is that they focus on influencing the employees behavior. Research has shown that if education and training materials can be personalized, then they
are much more effective in influencing behavior than by just showing facts or statistics.

Effective training
is also a key part
of a successful
PEM program.
Employees
should never be
discouraged from
aggressively
trying to find
the pathogen
in the plants
environment.

47

REFERENCES

Overall, the success of any PEM program is directly dependent on support and commitment throughout the organization, starting with top management and cascading down.
If management does not provide sufficient resources, both in terms of capital and personnel to do an effective job, then it will ultimately fail. If management is more worried
about meeting the numbers than supporting a robust food safety culture throughout
the organization, then it will fail. In high-performing, successful companies, food safety
is not considered just a program; it is a pervasive part of the companys culture. The
leaders in successful companies take a systems-based, behavior-based approach to creating a food safety culture throughout the organization (72, 73). Food safety should not
be viewed as a cost. Sure, there are costs associated with a commitment to food safety,
but senior management must realize that investing in food safety, including investing in a
solid PEM program, is a smart investment. It is an investment no different than in investing in sales and advertising, production and distribution, or new product development.
Research shows that companies that are dedicated to food safety and those that instill
a culture of food safety throughout the organization are big winners in the marketplace.
The company wins, the employees win, and the consumer wins.

48

REFERENCES

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Almond Board of California, 1150 Ninth Street, Suite 1500, Modesto, CA 95354 USA