Food processors face serious challenges due to Listeria monocytogenes contamination. Environmental monitoring is used to control L. monocytogenes from the processing environment. Although frozen foods do not support the growth of L. monocytogenes, the moist and cold conditions in frozen food production environments are favorable for growth of L. monocytogenes. The purpose of the study was to determine the current state of awareness and practices applied across a variety of frozen food facilities related to environmental monitoring for Listeria. A survey tool was created to elicit information on existing environmental monitoring programs within the frozen food industry. The topics included cleaning and sanitizing applications and frequency, microbiological testing, and environmental areas of concern. The survey was reviewed by academic and industry experts with knowledge of microbiology and frozen food processing and was field tested by industry personnel with extensive knowledge of environmental monitoring. The survey was distributed and analyzed electronically via Qualtrics among 150 frozen food contacts. Data were gathered anonymously with a response rate of 31% (n = 46). The survey indicated that facilities are more likely to test for Listeria spp. in environmental monitoring zones 2 to 4 (nonfood contact areas) on a weekly basis. The major areas of concern in facilities for finding Listeria-positive results are floors, walls, and drains. At the time of the survey, few facilities incorporated active raw material and finished product testing for Listeria; instead, programs emphasized the need to identify presence of Listeria in the processing environment and mitigate potential for product contamination. Recognition of environmental monitoring as a key component of a comprehensive food safety plan was evident, along with an industry focus to further improve and develop verification programs to reduce prevalence of L. monocytogenes in frozen food processing environments.
Environmental monitoring practices vary throughout the frozen food industry.
Areas of concern of processing facilities for Listeria are floors, drains, and walls.
Listeria spp. sampling is most commonly performed weekly on nonfood contact surfaces.
The goal for an effective food safety plan is to prevent harborage of pathogens in the production environment and to reduce the potential for cross-contamination and consequently adulteration of the food being processed. Manufacturing facilities implement environmental monitoring programs as a means of verification to support their food safety plans. Effective environmental monitoring programs can provide evidence that an operation's food safety plan is contributing to the company's ability to produce a safe product. Factors that affect environmental monitoring plans include the design of the program to seek and destroy for pathogens of concern and the effectiveness of corrective actions that ensue any positive findings (20).
Cleaning and sanitation practices are followed to remove food residues and to reduce or eliminate microorganisms from food contact surfaces and the food processing environment. Presence and growth of Listeria in a food processing facility can be an indication of unsatisfactory cleaning and sanitation procedures (5). If a niche area harboring pathogens such as Listeria is found, effective corrective actions to remove the contamination should be performed (20). Although effective cleaning and sanitation programs help to produce a safe product, other factors may increase the risk of potential product contamination such as development of Listeria monocytogenes growth niches and harborages. These may include, but are not limited to, poorly designed equipment and facility infrastructure, lack of personnel hygiene, and absence of validated processes (13). Because of the complexity of factors that impact the prevalence and growth of Listeria in frozen food manufacturing facilities, the application of well-designed environmental monitoring programs is paramount.
Traditionally, frozen vegetables are used in food preparation where the products are heat treated, fully cooked, or both and hence considered to be not ready-to-eat. However, some of these frozen vegetables can be consumed subsequent to thawing and without an additional lethality step, such as use of peas in a salad. Hence, there is a need to ensure the microbiological safety of these products and to prevent contamination with L. monocytogenes. In Portugal, Mena et al. (17) reported L. monocytogenes contamination of frozen vegetables to be 14.8 to 22.6%. As determined by the National Food Processors Association study, L. monocytogenes prevalence in multiple products including cheeses, salad, seafood, and lunch meat was 1.82% of the total samples collected (8). High-risk populations for listeriosis include pregnant women, children, persons with immunocompromised conditions (e.g., cancer, HIV infection, dialysis, organ transplantation), and the elderly (3, 7, 9, 18). Although freezing the product can prevent growth of L. monocytogenes, storage at improper temperature can allow products to thaw and permit the growth of Listeria (12). Controlling for hazards through good manufacturing practices helps to prevent bacterial contamination from harborage sources (6). Increased focus on effective personnel training and proper design of equipment and facilities are necessary to reduce Listeria prevalence in food manufacturing facilities (1). The objective of the study was to determine the level of awareness and practices used in the frozen food industry related to environmental monitoring for Listeria spp. and L. monocytogenes. The survey aimed to identify areas of concern in processing environments through the interpretation of industry-generated data.
MATERIALS AND METHODS
An electronic survey was created to provide an overview of the protocols for environmental monitoring that the frozen food industry implements in their manufacturing facilities. The survey was distributed through a listserv of food safety professionals working in frozen food manufacturing facilities. The participation in the research was voluntary, and no compensation was provided to encourage responses. Questions were written to establish an understanding of the operation, processes, and a general design of each facility while maintaining anonymity of participants.
Qualtrics (Provo, UT) software was used in the development and formatting of the questions in the electronic survey. The design of the survey was adapted to participants' responses. The software customized the survey outline based upon the answers provided to prior questions. This allowed the survey to provide follow-up questions for more in-depth responses. For example, if a participant indicated they implemented a protocol included in a specific question, the survey would follow up with a question asking about the frequency of the practice. If a participant indicated that they were not executing the protocol, the survey would continue with the next question.
The survey was designed with different question formats to ensure the questions provided comprehensive information. Figure 1 is an example of the survey that participants completed. Several questions were multiple choice where one or more answers could be chosen for each response. Other questions were designed as a matrix table, from which the participant could choose from multiple answer choices. The last type of question was an open-ended question for which participants provided a typed entry to the question. These were used sparsely and mostly as supplement questions to reduce the time and effort required to participate in the survey.
The survey was reviewed at different stages by academics and industry personnel with knowledge of food microbiology and commercial frozen food processing before implementation. The University of Georgia's Human Subjects Office reviewed and approved the standards and safety associated with the survey. In addition, legal counsel representing the frozen food industry reviewed the survey to ensure anonymity protection to all participants. Before the survey was distributed, a pilot test was performed using a small group of industry experts (n = 5) with extensive knowledge of environmental monitoring in commercial food processing facilities. Feedback provided from the pilot test was used to improve the survey.
The questions focused on various aspects that are important to designing an effective environmental monitoring program. The survey was divided into sections to depict the generic layout of the processing facility, sanitation protocols, and details on the environmental monitoring program being implemented in the facility. The section on the layout of the facility includes volume and size of the facility, design of the floor and drains, and conditions of the processing areas. Sanitation and cleaning questions are based upon good manufacturing practices and current industry practices. The environmental monitoring section focuses on testing protocols for product and environmental surfaces.
Distribution of the final Qualtrics survey link was done via e-mail to members of the American Frozen Food Institute with a statement indicating the purpose of the research. All responses were collected and compiled through the Qualtrics Web site, allowing participation in the survey to be anonymous to the researchers. The analysis of the data was performed with Qualtrics and Excel (Microsoft, Redmond, WA) to analyze the percentages of responses versus the total respondents for each question.
Of the 150 frozen food contacts that received the survey through a listserv, 46 contacts participated by completing a survey (31% response rate). In total there were 80 responses for categories of frozen foods, including vegetables (n = 39) and fruits (n = 17) as the leading foods produced (Fig. 2). Other facilities produced frozen meat, poultry, entrées, dessert, pizza, potato products, and appetizers. About half of the respondents manufacture at least two of the categories of food surveyed within one facility. The most common combinations of categories within a facility were vegetables with fruit, potatoes and appetizers, and entrée combined with meat and poultry. The processing facilities that participated were inspected by the U.S. Food and Drug Administration (FDA) and the U.S. Department of Agriculture, Food Safety Inspection Service, or both.
The definition of ready-to-eat (RTE) and not ready-to-eat (nRTE) was still in flux at the time of the study, but each participant defined their products based upon the intended use of their product. Survey participants defined their products based upon the manufacturer's determination of the product, by nRTE packages including cooking instructions on the package for consumers to follow, whereas RTE products are prepared to ensure the quality and taste of the final product is optimal for the consumer. Sixty-one percent of responders defined their products as nRTE and 28% as RTE. Eleven percent of responses produce both RTE and nRTE and stated the cleaning and sanitation procedures are the same for all their products.
Categories for volume of facilities in the survey was defined as small ($1 to $10 million in production per year), medium ($10 to $100 million per year), and large (>$100 million per year). These categories were established by literature and advice from industry professionals. Fifty-four percent (n = 25) were categorized as medium-sized facilities, 37% (n = 17) as large, and 9% (n = 4) as small.
Another measure of the facility is the square footage of the entire facility and the area of the processing room(s). Categories for the entire facility size included small (<2,400 m2), medium (2,400 to 10,000 m2), and large (>10,000 m2). No facilities were categorized as small in this survey, whereas 53% were medium-sized facilities (n = 25), and 47% (n = 22) were classified as large. Square footage of only the processing areas were defined as small (<1,100 m2), medium (1,100 to 4,600 m2), and large (>4,600 m2). Similar to the previous question, 60% (n = 28) of companies were classified as medium, 38% (n = 18) as large, and 2% (n = 1) as small.
Information was collected from the responders on the facility design and age. Facilities in this survey were older, with no facilities surveyed that were less than 10 years old. Thirty-nine responses included 19 facilities over 30 years old, 15 facilities 20 to 30 years old, and 5 facilities 10 to 20 years old. Only seven of the facilities performed a renovation less than a year ago, whereas 10 facilities performed a renovation over 15 years ago. Eight percent (n = 3) of the facilities have never performed a renovation to their facility. Of the renovations performed within the past 10 years, nine were renovated 1 to 5 years ago and eight were renovated 5 to 10 years ago.
All the facilities in this survey produced frozen food products. Facility layouts varied based upon company. Twenty-seven of 39 processing areas did not have a refrigerated processing area, whereas the other 12 processing areas were refrigerated. A majority of the facilities had either coated concrete floors (n = 24) or epoxy-coated floors (n = 20). The other flooring types were tile (n = 2) and noncoated concrete floors (n = 4). Of the facilities surveyed, 30 had trench drains, whereas 13 had cup drains. Sixty-four percent (n = 23) had three or fewer drains per 100 m2 in the processing area. In addition, 36% (n = 13) had four or more drains per 100 m2 of the processing area.
Implementation of good manufacturing practices is essential in all food manufacturing facilities, and the employees should be trained periodically (18). Key components to an environmental monitoring plan are the cleaning and sanitization steps. Cleaning and sanitation occur most commonly during pre- and postshift. The results from the survey revealed that ∼50% of the respondents performed cleaning and sanitation preshift, whereas the other half of the respondents cleaned and sanitized postshift (Fig. 3). Some respondents only clean during pre- or postshift, whereas some facilities indicated they clean preshift, midshift, and postshift. Some use additional cleaning times including midshift, multiple times during the shift, and weekly.
Eighty-seven percent (n = 33) of responders indicated that they have performed validation of their cleaning procedures. Validation steps included visual inspection by quality assurance technicians followed by ATP, aerobic plate count (APC), allergen swabs, or a combination after cleaning but before production starts. Additional cleaning was performed until ATP or APC swabs were within the appropriate range designated by the facility in case the standards were not met subsequent to initial cleaning and sanitation. Other validation measures performed by the facility management included academic reviews, professional reviews from a third-party laboratory, and in-plant historical reviews of current and past-process controls. These validation measures ensure that the cleaning trends follow an established pattern to confirm the facility conforms to their standards.
Environmental monitoring plans were based on the zone concept and defined by FDA (23). Zone 1 was classified as food contact surfaces, whereas zones 2, 3, and 4 are nonfood contact surfaces. Sanitizer and cleaning compounds used differed between facilities. Detergent and water with soap were described as the most common cleaning compounds. Detergents were used in zones 1 (n = 28) and 2 (n = 28) more than in zone 3 (n = 25) and 4 (n = 19); however, water with soap was consistent throughout all zones (Fig. 4). Solvent-based cleaners were consistently used throughout all the zones (n = 14 per zone).
Sanitizers used most by facilities were quaternary ammonium compounds followed by peroxyacetic acid (Fig. 5). Other sanitizers less commonly used in the facilities included hypochlorite, chlorine dioxide, and iodophors. The responses showed that sanitizers were applied in zones 1 (n = 73) and 2 (n = 65) at a higher proportion than in zones 3 (n = 60) and 4 (n = 41). To determine how sanitizers were applied the survey delved into each sanitizer's application method. The application methods for sanitizers include spraying the sanitizer onto the equipment, using liquid and water as a clean-in-place process or soaking the equipment, and foaming the surface. Quaternary ammonium compounds were most commonly applied by spray method (n = 21), followed by liquid and water (n = 16) and foam (n = 12) applications. Peroxyacetic acid was applied by the spray (n = 15) and liquid and water (n = 14) methods. Five responders applied chlorine samples as liquid and water and one as gas. Hypochlorite was applied by foam (n = 10), spray (n = 7), and liquid and water (n = 6).
Environmental monitoring practices focus on testing for indicator organisms and pathogens to ensure that facilities are reducing risk to their consumers. Indicators used in zone 1 included APC (n = 24) and ATP (n = 29), followed by coliforms (n = 18) (Fig. 6). In zones 2 (n = 31), 3 (n = 32), and 4 (n = 30), Listeria spp. were most commonly monitored. The facilities that test for L. monocytogenes indicated they also test for Listeria spp. The responses for the “other microorganisms” category stated the processors tested for Salmonella and/or yeast and molds.
Frequency of testing indicators and pathogens within establishments was based on scientific literature and individual company policy. APC and ATP were tested preshift in all zones, with a focus on zone 1 (Figs. 7 and 8). Coliforms were tested weekly in all zones and preshift in zone 1 (Fig. 9). Approximately two-thirds of the respondents that tested for ATP or APC also indicated they test for coliforms. Listeria spp. were most commonly tested weekly in zones 2 to 4 (n = 58). Almost every respondent combined indicator testing for APC or ATP in zone 1 with testing for Listeria spp. in zones 2 to 4. Additional frequencies for Listeria spp. in zones 2 to 4 were midshift (n = 32), preshift (n = 21), and monthly (n = 28) (Fig. 10). L. monocytogenes was also indicated as being tested weekly in zones 2 to 4 (n = 18) (Fig. 11). Within the other organisms category, the most commonly tested organism was Salmonella, and it was tested weekly in zones 2 to 4 (Fig. 12). The facilities that tested for other microorganisms were commonly facilities that tested for Listeria spp. as well.
Supplemental to environmental sampling, some facilities performed final product testing for Listeria and L. monocytogenes as part of their program. More than 70% of respondents indicated they do not test for Listeria spp. or L. monocytogenes in raw materials (n = 26) or products during processing (n = 25). However, 47% (n = 17) of respondents indicated they do not test finished product for Listeria. For finished products, 8% (n = 3) tested for Listeria spp., 27% (n = 10) tested for L. monocytogenes, and 17% (n = 6) tested for both. All respondents who stated they test for Listeria species in final product indicated that when a positive result was found further testing was performed to determine whether the positive sample was L. monocytogenes.
For both Listeria spp. and L. monocytogenes, the areas of concern in the manufacturing environment for a positive test result were drains, floors, and walls. For Listeria spp., survey respondents indicated the most common areas to focus on for environmental monitoring were drains (n = 27), floors (n = 25), and walls (n = 4) (Fig. 13). The most common areas for L. monocytogenes during environmental monitoring were also drains (n = 13), floors (n = 9), and walls (n = 5) (Fig. 14).
The survey provides an overview of current frozen food industry practices related to environmental monitoring. The data revealed there is an industry focus on current environmental monitoring programs to improve and develop extensive practices to reduce prevalence of L. monocytogenes in frozen food processing environments. There were variations in responses related to specific practices. This could be due to differences in facilities, types of products processed, company policies, or a combination. It could also indicate some uncertainty within the food industry as to the best environmental monitoring practices.
A factor that can affect the design of an environmental monitoring plan can be the type of food being processed. RTE foods require a more extensive plan than nRTE foods because there are no additional postprocess preventive control steps required with RTE foods for consumers to reduce contamination levels. A challenge study in Europe found it difficult to establish a distinct difference between RTE foods that do support the growth of Listeria versus products do not support the growth of Listeria (2). RTE foods such as deli meats have higher prevalence of L. monocytogenes (5%) in finished products (14). Consumers' use of the product may vary from the manufacturers' intended use for the product, as some consumers may eat an nRTE product without further cooking assuming the product is to be consumed as an RTE product. Manufacturers should continue to add detailed information and try to educate the consumers through improved communication methods to ensure that the food products are consumed in the way intended by the manufacturer.
Size, age, and design of facility
The facilities in the survey defined their production capacity predominately as medium and large by volume in dollars of production per year and size based upon area of production facility in square meters. Larger facilities may have more experience in designing a food safety program; this experience can provide guidance for smaller facilities that are beginning to design their protocols. Most of the facilities surveyed were more than 30 years old. These facilities are most likely operating under conditions that were designed without new technological improvements that could provide better means for reducing hazards in the food being processed in them. The design of the facility may be based upon the technology and industry practices when the facility was built (19). Older facilities may increase their production capacity more than what they were originally designed for owing to higher demand for products. The higher demand for the products leads to increased production and an increased need for better and faster sanitation and cleaning procedures (16).
Drains and floors
Floors in the survey mostly contained coated concrete or epoxy-coated floors. The epoxy coating is a good balance of cost and durability because it helps to adjust to thermal expansion exposure of extreme temperature (6). A majority of the surveyed facilities (n = 30) were designed with trench drains compared to cup drains. Trench drains have a high capacity for flow, but the extensive open grating requires a higher need for cleaning because microorganisms can spread across the drain (6). Facility design should include adequate number of drains to provide proper removal of water. The participants indicated more facilities (64%) have fewer than three drains per 100 m2. Cleaning of the drains should not be performed when food is exposed to the environment. A clean-in-place system can be used to clean drains similar to other equipment (6).
Cleaning and sanitation
Cleaning and sanitation should be implemented in a facility to provide clean manufacturing operations to produce safe and wholesome products (21). Basic procedures for cleaning and sanitation include application of a cleaning compound to remove residue, followed by a sanitizer to reduce the microbial load (16). The cleaning compound is applied first because its efficiency in removing the soil and food residue on food contact surfaces can affect the effectiveness of sanitizer applied subsequently. Factors that affect the cleaning and sanitation performance are time, temperature, concentration, surface type, material, and workers performing cleanup (16). Deep cleaning that includes additional time and labor compared with a traditional facility cleaning can help reduce L. monocytogenes prevalence in facilities with a high prevalence of L. monocytogenes, by up to 26% (10). Most of the facilities indicated they performed a validation of their cleaning procedures. Monitoring and verification of cleaning and sanitation protocols varied based on each individual facility's procedures (11). The descriptions of the cleaning validation protocols provided a wide range of answers including indicator and pathogen testing, third-party consulting, and academic or in-plant reviews. The differences in the validation methods indicate discrepancy in industry practices and encourage more data to determine the preferred method of validating protocols.
ATP swab results are used as a good indicator for facility standards and provide motivation for the cleaning crew as an incentive to achieve higher benchmarks (10). Data indicated that indicator organisms including ATP, APC, and coliforms are monitored in zone 1, the food contact surface. Indicator organisms are used by the industry to monitor the cleaning and sanitation procedures performed in the facility. Testing for APC and ATP is commonly used indicator of cleanliness of the surface, but does not detect presence of pathogens. Although indicator testing does not detect pathogens, the testing can help to determine areas of concern for the presence of pathogens if APC or ATP identifies sections of improper cleaning and sanitation practices. These testing methods are used preshift to help verify the effectiveness of the cleanup before a new production shift is about to start. The ATP test results (relative light units) can correlate with sanitation effectiveness and provide real-time measurement of microorganisms on a surface (16).
Frequency of testing for pathogens
Data also identified several facilities were testing for the presence of Listeria spp. or L. monocytogenes postsanitation or before production (preshift). With a preshift testing model, a positive result would indicate there is contamination of the surface before production. Most facilities use indicator organisms or ATP testing preshift as a verification of the effectiveness of the cleaning and sanitation program. There are two issues with conducting preshift Listeria spp. or L. monocytogenes testing. (i) It may indicate there is uncertainty concerning the effectiveness of the cleaning and sanitation program. This should prompt the food safety team to review these programs and identify potential limiting factors, such as revalidation of sanitation effectiveness, retraining of sanitation personnel, or identification of appropriate chemicals and processes. (ii) It is recommended these facilities review their sampling strategy on the timing of sample collection. The midshift testing protocol helps to determine pathogen contamination during the production shift and not before production. A robust environmental monitoring plan focused on eliminating the pathogen of concern should test for the pathogen at the highest frequency of finding a positive. The guidance documents from the FDA suggest testing for pathogens during shift approximately 3 to 4 h into production (23). Collecting environmental monitoring samples 3 to 4 h into production allows L. monocytogenes (if present) to emerge from harborage sites to contaminate food contact surfaces, products, and the environment (23).
Listeria and L. monocytogenes testing
Listeria spp. and L. monocytogenes were frequently tested in zones 2 to 4, the nonfood contact surfaces, on a weekly basis. Facilities monitor for food contact surfaces and nonfood contact surfaces, but the frequency of monitoring and collection times for this activity are determined on an individual basis (25). Few facilities test for Listeria in raw materials or products during production, with greater emphasis on monitoring placed on preventing product contamination in the processing environment. The areas of concern in facilities for finding Listeria-positive results are floors, drains, and walls.
The zero-tolerance approach for L. monocytogenes in RTE foods adopted by the U.S. food industry regulators encourages higher performance standards in manufacturing facilities but may have a detrimental effect on environmental monitoring practices because facilities are prone to conduct fewer tests to reduce the possibility of collecting positive results for Listeria and L. monocytogenes (24). The FDA released a new draft guidance document in 2017 updating their 2008 document to establish more effective environmental monitoring procedures, allowing the first environmental Listeria-positive test to be an indicator that there is a problem without triggering an automatic recall (22, 23). This approach by the FDA is promoting the “seek and destroy” method in environmental monitoring wherein facilities are encouraged to find the problem and couple that with intensified cleaning and sanitizing activities to reduce the contamination potential in their facility (15).
Industry and data trends
Industry continues to advocate for improvements in environmental monitoring programs. The pathogen environmental monitoring programs are meaningful assessments of the effectiveness of a facility's food safety plans (4). The responses in the survey vary due to differences in environmental monitoring plans. This is because each food safety plan is individualized per facility. Collecting data across the industry of current environmental monitoring practices can help improve food safety plans in all organizations. The collection of data from current implemented effective food safety and environmental monitoring plans provides information to new facilities designing their individualized protocols.
Listeria-related recalls within the frozen food industry have created greater concern for mitigating Listeria contamination problems within the food processing environment. The survey collected information about facilities including age of the facility, time of most recent renovations, products produced, production size, and production volume. Because most of the facilities classified as medium and large in volume and size, the information from their responses can help smaller processors that are trying to develop their environmental monitoring plan. Although these data are only from frozen food facilities, they can provide insight for Listeria prevention practices in other segments of the food industry.
This material is based upon work supported by the Frozen Food Foundation and by the Georgia Agricultural Experiment stations.