Microbiological Control a Prerequisite for Sustainable Food Safety: a Case Study in a Dairy Dessert Facility

Abstract

Dairy desserts have become a commercial product which produced in the industry and consumption is increasing worldwide. Ensuring food safety is becoming increasingly significant in dairy dessert which is microbiologically risky product. The combination of microbiological monitoring of both food products and the production environment is critical to provide food quality and safety. Environmental Monitoring Program (EMP) is a monitoring program which allows to evaluate effectiveness of general hygiene-sanitation operations and control programs to prevent possible microbial contamination of food. The aim of this study is to provide practical recommendations and strategies to build efficient EMP in the dairy desserts and food industry. During the implementation of the EMP (October 2019-March 2020), a total of 852 samples; dairy dessert (keskul) (n = 144), raw and auxiliary materials (n = 78), air (n = 96), water (n = 24), personnel (n = 144) and production surfaces (n = 366) microbiological conditions were examined within the parameters of Total Mesophilic Aerobic Bacteria (TMAB), coliform, Escherichia coli, Staphylococcus aureus and yeast-mold. The microbiological results of keskul before vs after the implementation of EMP was 3.81 vs. 2.55 log cfu/g for TMAB, 2.60 vs. 0.90 log cfu/g for coliforms, 0.58 vs. 0 log cfu/g for E. coli, 0 for S. aureus, 2.33 vs. 1.01 log cfu/g for yeast-mold and negative for Salmonella, respectively. Our study demonstrates that effective EMP plays a significant and crucial role in controlling microbiological hazards of final product.

Keywords:
Environmental monitoring program (EMP); dairy dessert; food safety; pathogenic microorganisms (PMO)

HIGHLIGHTS

Nowadays, despite the implementation of food safety systems and legal obligations in countries, foodborne diseases continue to affect millions of people and cause thousands of deaths.

Ensuring food safety is becoming significant in dairy dessert which are microbiologically risky product group.

Environmental Monitoring Program in food manufacturing plants can support to monitor daily operational activities, hygiene, and sanitation effectiveness to prevent the risk of contamination of pathogens.

Our study showed that implementing EMP is an early warning system for prevention of foodborne microbiological risks.

INTRODUCTION

Dairy desserts are consumed by a wide range of consumer groups due to their rich nutritional content, sensory properties, easy accessibility, and increasing consumer demand [¹, ²]. They have been rather popular in the EU and especially vanilla cream pudding, spangle, rice pudding is commercially available in many countries [³]. In addition, preference of functional dairy desserts increases among consumers due to fiber-rich diets [⁴]. Keskul is a custard-like dairy dessert commonly consumed in Turkey Cuisine due to light taste. Keskul dairy dessert which recipe includes pasteurized milk, sugar, corn, egg, starch, and rice flour, is thermally processed, then distributed and stored under refrigeration [⁵].

The dairy dessert can be considered high risky product due to rich nutritional components, water activity (aw) and pH that an ideal for microorganisms [⁶]. There are many factors affecting microbiological safety and quality of final products including the initial microbiota of raw materials, production environment circumstances, used water and post-process contamination of heat-treated products originating from personnel, equipment, and packaging materials [⁷,⁸]. Despite cooking at high temperatures, when the dairy desserts produced in improper hygienic conditions, they can be cross contaminated with various pathogenic microorganisms such as Salmonella spp., S. aureus, E. coli, B. cereus with L. monocytogenes pose potential health problems [⁹]. In addition, yeast-molds are secondary risky group microorganisms that cause spoilage and product losses of dairy dessert.

Nowadays, E. coli, Salmonella and S. aureus infections are rising hazards for the dairy dessert industry. Milk-based foods have been reported as a vector for the transmission of various microbiological infections, especially in countries where hygiene standards are not strictly enforced [¹⁰, ¹¹]. Salmonella enteritidis poisoning, which affected 90 people in Switzerland, was associated with a dairy dessert [¹²]. Enterotoxigenic S. aureus food poisoning occurred in Umbria, Italy affected 24 of 42 clients who had dinner at a regional cafe, on August 28, 2015 [¹³]. After examining the samples taken from the environment and food, it was reported that the poisoning was caused by the Salmonella within dairy cream [¹³]. In addition, Şahiner and coauthors [¹⁴] have reported that Salmonella spp. L. monocytogenes and E. coli were not found in 100 milk-based dessert samples in Turkey. However, levels of coliform and coagulase positive indicated that poor hygienic quality of samples, improper cleaning and sanitation program and personal hygiene practices applied in the production environment and retail market.

EMP allows to evaluate the efficiency of general hygiene-sanitation practices and is a control program to prevent possible microbial contamination of food [¹⁵, ¹⁶, ¹⁷]. Moreover, EMP can be defined as a pre-requisite program under food safety systems in food facilities, and this proactive approach can be used as a microbiological early warning indicator in conjunction with final product controls to prevent food contamination [¹⁵, ¹⁸]. In recent years, the FDA (Food and Drug Administration) has recommended the integration of the EMP into the Hazard Analysis Critical Control Point (HACCP) based food safety and management systems to ensure safe food production, avoid food-borne outbreaks and recalls [¹⁹, ²⁰]. Some guidelines [²¹, ²²,²³] and legal standards [²⁴, ²⁵] are available to support the application of the EMP. Although the methodology is clearly explained in these resources, the implementation of EMP is dependent on majorly characteristics of production plant, produced products, the types of pathogens and indicator microorganisms. On the other hand, EMP is a monitoring program and to ensure the food safety of the product from raw material to final consumption, dairy facilities must implement effective HACCP-based food safety systems (IFS, BRCGS, ISO 22000). Some study indicates that the most important practical barriers for implementation of HACCP-FSMS (Food Safety Management System) are financial support, knowledge, training, and personnel awareness [²⁶, ²⁷].

The study aimed to implement and verify of an effective EMP monitoring program in a dairy dessert plant to prevent microbial contamination, reduce risk of recall, ensure food safety, and increase client satisfaction. This is the first report on the dairy dessert facility implementation of EMP and provides recommendations for optimization of the EMP to serve the dairy and food industry.

MATERIAL AND METHODS

Application of EMP

This research was carried out in close cooperation with one of the industrial partners in a medium-sized dairy dessert plant that certified with ISO 22000:2018 Food Safety Management, located in the Bursa, Turkey. Production capacity of this facility is approximately 3000 tons/day and produced various dairy dessert that included pudding, rice-pudding, keskul and spangle. The EMP was designed, developed, and implemented in the facility between October 2019 and March 2020. Although an effective EMP design is specific to the individual food facility and individual operations within the facility, EMP was established in the dairy dessert plant by following key components in Figure 1 [²⁸].

Figure 1
Key components of EMP application

Establishment of the EMP team

The first step is to assemble EMP team who is aware of the microbiological hazards that may occur in the facility and experienced in hygiene-sanitation and food safety. EMP team consists of the quality control manager, microbiologist, production supervisor, maintenance supervisor, line operator and cleaning team, who are also active in the HACPP team. The EMP team should be able to predict the risk level of sites in the facility, the potential microbiological hazards of interest, where to take sample, how to take sample, frequency of sample, sample analysis, and how to evaluate results.

EMP zoning concept and sampling locations

The dairy dessert plant was divided into four zones from the highest risk (Zone 1) to lowest risk (Zone 4) in accordance to zoning concept to obtain mapping the processing plant. Zone 1 is defined as surfaces that come into direct contact with food (personnel hands, packaging machines, packaging materials, etc.) before the product is packaged and after killing steps such as heat treatment. Zone 2 is physically close to the food but not directly in contact with the product (work clothes, weighing scales, stoves, etc.). Surfaces (walls, doors, floors, trash cans, etc.) that are far from the product but still in the production environment, which could lead potential contamination hazard with indirect contact, are considered within the scope of Zone 3. Zone 4 areas outside of the processing range.

Totally 852 microbiological examinations were carried out over the 6-months period. Documentation of 47 sampling sites is provided the following table including from Zone 1 to Zone 4 (Table 1).

Determining the appropriate target microorganisms and baseline limits

Choosing target microorganisms based on microbial risk assessment is the essential point in developing an effective EMP. The historical data of microbiological analysis of final products and surface areas, customer complaints and legal requirements were examined to determine appropriate indicator and pathogen microorganisms and baseline limits. Target/baseline limits are unique for each facility and product types. Most of guidelines are intended to control pathogens in the food production environment, especially for Salmonella and Listeria species. A few of these guidelines focus on indicator organisms and even less on spoilage organisms [¹⁷]. European Commission [²⁹] has recommended microbial levels (Total Viable Counts) between 0 and 10 cfu/cm² for surfaces in contact with food in the production area after cleaning and sanitation although there is no worldwide legal limit for environmental monitoring analysis results. Manitoba (Canada) Food Safety Department supported that cleaning and sanitizing must be effective to a microbial level leading to specifications of <10 cfu/ cm² coliforms, aerobic plate count, yeast and mould, and coagulase positive Staphylococcus on product contact surface before packaging [³⁰]. Moreover, Almond Board of California [²¹] recommended target limits < 10 cfu/40 in²) for Aerobic Plate Count and coliform on after application of sanitizer.

TMAB, E. coli, coliform, S. aureus, yeast-mold were determined for final products and production areas to evaluate the general hygiene and sanitation status of the facility and to show the potential presence of pathogens that may cause significant health risks. In addition, European Union Microbiological Criteria Legislation and Requirements were met with the determined microorganisms.

Table 1
EMP sampling list for each zone

Zone 1	Zone 2	Zone 3	Zone 4
Personnel Hands Spatula Bowls Filling Machine Packaging Material Tray Pots Boilers Mixing Apparatus Mixers Blender Buckets Thermometer Water Air Nitrogen Gas	Personnel Uniforms Tables Scales Machine push button Grates Stoves Ovens Separators Transport Trolleys Stairs Ventilation Paddle Box Cold Storage	Walls Doors Floor Drains Lamp UV Lamp Windows Trash Cans Fire Cabinets Pallets Pallet Trucks Metal Detector Shelves	Staff Lockers Restaurants Offices (Desk, Pc, Calculator Max.) Toilets Care Room

Analysing plan (number of samples, analysing frequency and method)

Microbiological analysis of keskul

A 10 g of each keskul sample was weighed and added into sterile stomacher bags homogenize for 2-3 minutes in the stomacher by adding 90 mL of peptone water (0.1%) (3M™ Flip-Top Dilution Bottle, FTPW9060, Wroclaw, Poland). Serial dilutions (10^-1,10^-2,10^-3) for each sample were plated in duplicate on to Aerobic Count Plate (3M™ 06400 Petrifilm™, Wroclaw, Poland), Staph Express Count Plate (3M™ Petrifilm™, Wroclaw, Poland), Yeast and Mold Count Plate (3M™ Petrifilm™, Wroclaw, Poland), E. coli/Coliform Count Plate (3M™ Petrifilm™, Wroclaw, Poland) of TMAB, S. aureus, yeast-mold and E. coli-coliforms, respectively. While E. coli/Coliform Count Plate were incubated 37 °C for 24 h, Aerobic Count Plate and Staph Express Count Plate plates were incubated at 37 °C for 48 h, Yeast and Mold Count Plate plates were incubated at 25 °C 120 h [³¹, ³², ³³]. Salmonella analysis was performed in an external laboratory since the microbiology laboratory is close to production area. Food Safety System (BRCGS) have reported that pathogen testing (including pathogens tested as part of the environmental testing) shall be subcontracted to an external laboratory if laboratory is near to production to prevent an of product contamination.

Microbiological analysis of production surface, air and water

Sampling plan is the core of an effective and proficient EMP implementation. Routine sampling frequency was performed weekly or monthly depending on the zone concept, amount of product produced, risk and facility history. Sampling time was determined after sanitizing to measure of cleaning effectiveness. The number of samples taken in each surface area were changed depending on EMP methodology and the risk classification of the area (raw or finished/ processed product area). FDA draft guidance recommends that even the smallest facility takes 5 swabs each of food contact (Zone 1) and non-food contact (emphasizing Zone 2) surfaces. Sampling frequency, time and numbers of sample were summarized in Table 2.

Table 2
EMP sampling plan

Zone	Control Frequency	Sample Amount	Sampling Time	Microorganisms Limits
Zone 1	Weekly	5-8 pieces*	After Cleaning-Sanitation	TPC, coliform, S.aureus, yeast and mold <10 cfu/ cm2, E.coli Negative.
Zone 2	Weekly	5-8 pieces*		TPC, coliform, S.aureus, yeast and mold <10 cfu/ cm2, E.coli Negative
Zone 3	Monthly	5-8 pieces*		TPC, coliform, S.aureus, yeast and mold <10 cfu/ cm2, E.coli Negative
Zone 4	Monthly	3-5 pieces*		TPC, coliform, S.aureus, yeast and mold <10 cfu/ cm2, E.coli Negative

Each environmental surface samples were taken from nearly a 100 cm² area by a swab stick according to European standard guidelines sampling procedure and techniques. Petri which containing 20 mL of medium (Yeast-mold and TMAB) were kept open for approximately 15-30 minutes at different points in the production and packaging environments of the facility for air sample [³⁴]. Water samples were spread plated (0.1 mL) onto 3M PetrifilmTM Aqua Heterotrophic Count Plate and 3M PetrifilmTM Aqua Coliform Count agar plates without dilutions after membrane filtration (TS EN ISO 9308-1). Samples were placed into plastic bags and immediately transported under refrigeration temperature to incubation. Microbiological analyses were carried according to method used by Cinar and Onbaşı [¹⁸].

Determination of corrective and preventive actions

The implementation of the EMP needs to be supported by well-designed corrective and preventive actions to eliminate the risk of microbial contamination. Corrective actions were taken immediately after determining inappropriate microorganisms (pathogenic or indicators) to prevent holding/implicating/recalling of product. Corrective actions will help to reduce and/or prevent to contamination of product with pathogenic microorganisms and thus reduce overall incidence of consumer illness. In this context, the following steps have been applied in the processes when the analysis results exceeded target limits and/or were positive.

1. EMP team immediately reassembled investigate root-cause.

2. Effected production line was stopped.

3. Final products were defined as an “inappropriate product” and hold until testing microbiological analysis. The Standard Operating Procedure (SOP) was followed for the approval and release of the Finished Product after negative microbiological analysis results were obtained for the transition from the production site to the supply.

4. The production area was examined thoroughly both visually and vector swabbing.

5. Sampling frequency was increased until getting three consecutive negative results.

6. Swab samples were taken from the surfaces to identify the source of contamination.

7. After the cause of contamination was determined, corrective actions were determined to eliminate the problem (inappropriate cleaning chemicals, ineffective cleaning of the personnel, inadequacy of controls, disruptions in Good Manufacturing Practice (GMP) applications, etc.)

RESULTS AND DISCUSSION

Before the implementation of EMP mean microbiological counts were 3.81 log cfu/g, 2.60 log cfu/g, 0.58 log cfu/g, 0, 2.33 log cfu/g and 0 for TMAB, coliform, E. coli, S. aureus, yeast-mold and Salmonella spp. respectively for keskul products (Figure 2). Comparatively, after the EMP application period analysis results were 2.55 log cfu/g, 0.90 log cfu/g, 0 log cfu/g, 0 log cfu/g, 1.01 log cfu/g and 0 log cfu/g (Figure 2). As a result of this study, it was concluded that the microorganism levels of keskul products (TMAB, coliform, E. coli and yeast-mold) decreased statistically significantly during the EMP application period (p<0.05). There are no stated microbiological limits for dairy dessert by the EC regulations [³⁵]. All Salmonella spp. and S. aureus (Staphylococcal enterotoxins) counts were met microbiological limit (Negative) for dairy dessert according to the Turkish Food Codex [³⁶]. There are several studies on microbiological quality of various dairy desserts in Turkey. Seçim and Uçar [³⁷] have analysed 10 keskul samples and found TMAB, coliform and yeast-mold count as 2.17, 0.93 and 1.05 log cfu/g, respectively. In another study conducted by Şahiner and coauthors [¹⁴] determined that number of TMAB, coliform and yeast-mold were on average 2.51 log cfu/g, 3.74 log cfu/g and 0.70 log cfu/g, respectively in keskul products. When the results are compared with ours, the TMAB and yeast mold results are similar to the results that we obtained after EMP (Figure 2). In addition, S. aureus and yeast-mold results after EMP met limits that shared by Vargas and coauthors [³⁸] for the dairy dessert (Dulce de leche) according to Mercosul legislation. On the other hand, coliform counts were higher than our results and it might result from the inadequacy production conditions and disobedience to hygienic rules, EMP program may not implemented in this facility, insufficient cooking heat or degree at the time of production. Although limits for E. coli are not specified for dairy dessert by EC regulation [³⁵] and Turkish Codex [³⁶], samples were analysed to identify potential unfavourable hygiene conditions and fecal contamination. E. coli was determined as 0.58 log cfu/g in October and 0.25 log cfu/g in January, and its presence could not be found in other months. The presence of E. coli has shown that there is contamination from personnel and unhygienic conditions in the dairy dessert facility. After finding positive results of E. coli, swab samples were taken unannounced from all personnel hands and uniforms to detect the root cause of contamination (Figure 3). All the personnel were trained to raise awareness about where E. coli comes from, how to wash hands (time, method, use of soap, etc.), and how to use personal protective equipment such as uniforms and gloves hygienically. We observed that disinfectant points were inadequate after the interviews with the staff. Eight disinfectant points have been added to different parts of the facility so that the personnel can easily access the disinfectant whenever they need it. Moreover, food safety culture trainings were given to change the perspective and behavior of the personnel in the facility on food safety. Food Safety Culture can be defined as the food safety attitudes, values and beliefs shared by all employees. The commitment and robustness of the personnel to the food safety management of the facility has been increased by personnel performance evaluation, awards, events, and project related to food safety. E. coli results were negative after EMP application, indicating that the corrective and preventive actions were effective.

Figure 2
Final Products (Keskul) microbiological analysis results (log cfu/g)

Mean aerobic counts (TMAB) and yeast-mold of air samples before and after EMP ranged from 170 to 2 cfu/m³ and 150 to 1 cfu/m³ (Figure 4) and results showed that they were significantly lower after EMP (P<0.05). Unsatisfactory air results for TMAB and yeast-mold were recorded within the packing and production area. Upon inspection, condensation and untreated air were present on production environment. When the sources of contamination in the air were detected within the scope of environmental monitoring results, some investments were made to improve microbiological air quality. Positive air pressure was provided to prevent all kinds of dust, polluted air and microorganisms in the air that may enter from the outside in the dairy dessert production area. The microbial load of the air was reduced by integration of different variety of filters (paper filter, hepa filter, etc.) on the air entrance. An automatic peracetic acid dry fogging system was used to sterilize air 2 days in a week. In addition to these, the air sterilizer installed in the facility was cleaned ambient air by passing inside through UV and hepa filters. Stobnicka-Kupiec and coauthors [³⁹] reported the total bacterial and fungal results of commercial and conventional dairy air environment in the range of 70-860 cfu/m³ and 50-290 cfu/m³, respectively. In another study on air quality and its importance in dairy facilities, <150 cfu/m³ and <50 cfu/m³ are recommended for TMAB and yeast-mold [⁴⁰]. Our results are in accordance with those reported by Zacharski and coauthors [¹⁵] in a study of microbial safety of air and surface in a dairy plant (<4.72 log cfu/cm³ for TMAB and <0.16 log cfu/cm³ for yeast-mold). We used the settling plate technique, which requires a long exposure time (15-30 min). On the other hand, using active air sampling techniques provide detecting rapidly and sufficiently air samples.

Tap water provided by local water and sewerage enterprises (BUSKİ Bursa, Turkey) is used in the facilities. When TMAB and coliform results were examined, the maximum value was determined as 7 cfu/mL and 0, respectively, and results meet the EU and Turkish legal regulations [⁴¹, ⁴²].

TMAB are useful for the evaluation of the cleaning and disinfection process, satisfactory and unsatisfactory categories. Microbial level of TMAB for Zone 1, Zone 2, Zone 3, Zone 4 and personnel decreased from 2.82, 2.92, 3.10, 2.06 and 2.79 log cfu/cm² to 0.25, 0.30, 0.25, 0.03 and 0 log cfu/cm², respectively after implementation EMP (Figure 3,5,6,7 and 8). Differences between pre- and post-EMP samples were statistically significant (P<0,05). preventive and corrective actions were taken to eliminate unsatisfactory result for TMAB was over 10 cfu/cm² during EMP implementation process. The exceeded recommended limits of TMAB were suggestive of cross contamination, improper personal hygiene, poorly designed equipment, cleaning-sanitation applications deficiencies and absence of validated processes. External footbaths, hygiene points and auditing of their HACCP program were all strategically implemented and new adenosine triphosphate test (ATP) equipment’s was integrated in hygiene control applications to prevent cross-contamination. ATP swab results were used as a good indicator for facility standards and provided motivation for the cleaning staff as an incentive to achieve higher benchmarks. TMAB counts were determined above the limit values in trays and spatulas which used in keskul and have direct contact with final products. It was observed that cleaning and sanitation efficiency was inadequate as organic residue adhered to the surfaces after usage. The sanitation standards were provided for the trays by using the chemical immersion and holding method and for spatulas were sterilized in UV instrument. The difficulty of developing and evaluating an EMP is the lack of legal limits for both direct and indirect surfaces. On the other hand, The European Commission the European Commission (EC, 2001) [⁴³] has recommended microbial levels between 0 and 10 cfu/cm² for surfaces in contact with food in the production area after cleaning and sanitation. Moreover, Almond Board of California [²¹] has recommended target value is <10 cfu/cm² (1 log cfu/cm²) and the maximum limit value is <100 cfu/cm² (2 log cfu/cm²) for TMAB after application of sanitizer. Our findings were met the target microbiological limit for food contact surface both the EC [⁴³] and Almond Board of California [²¹]. Our TMAB result was similar to the range of 0 to 2.18 log cfu/cm² reported for dairy processing plant where Ireland a similar study was conducted [¹⁵]. Our findings emphasize that strictly followed and approved EMP and hygiene-sanitation procedures are curious to prevent or eliminate persistence nonconformities.

Figure 3
Analysis results of samples taken from personnel's (log cfu/cm²)

Figure 4
Microorganism results in air environment (cfu/m³).

Figure 5
Zone 1 microbiological analysis results (log cfu/cm²).

Prior to EMP, mean coliform counts were Personnel (2.49 log cfu/cm²), Zone 1 (2.44 log cfu/cm²), Zone 2 (2.74 log cfu/cm²), Zone 3 (2.20 log cfu/cm²) and Zone 4 (1.30 log cfu/cm²) respectively, whereas no coliform was detected in any swap results after EMP implementation (Figure 3,5,6,7 and 8). E. coli was detected in pre-EMP samples mean counts were respectively 1.88, 0.90, 0.33, 1.36 and 0.77 log cfu/cm². After the EMP was implemented, no E. coli was detected in any swab. Average counts were significantly (P<0.05) higher in pre-EMP than post-EMP samples for all environmental surfaces. Detection of Coliform and E. coli bacteria on food contact and non-contact surfaces in the production environment indicate improper cleaning (chemicals, cleaning materials, cleaning time) insanitary conditions, or post-process contamination from personnel or surfaces. In this study, Coliforms and E. coli were precursor indicators of particular pathogens. Using a disinfectant, the occurrence of these pathogens, such as Salmonella, is higher when attached to a surface than in suspension. It was shown by Møretrø and coauthors [⁴⁴] that a 70% ethanol-based disinfectant was able to eradicate Salmonella dried on stainless steel. The results of this work demonstrated that the disinfectant used did not attain to the complete surface where it was applied. This may be caused by several factors including insufficient contact time; disinfectant loses strength because of unknown storage conditions. For this reason, an automatic dosed disinfectant foam system was integrated into the facility to ensure that surfaces are cleaned more efficiently and cost-effectively. Disinfectant types used, dosage amount, and contact time with the equipment surface were determined according to the microbiological swab results taken prior to and post-disinfection. Sodium chloride-containing foam was applied, then it was left for 15-20 minutes to penetrate to all surfaces, afterwards, it was rinsed with water. Ramesh and coauthors [⁴⁵] reported that sodium chloride showed more activity against Salmonella when dried on surfaces compared to different disinfectants when containing quaternary ammonium compounds (QACs), sodium chloride, and hypochlorite, respectively.

A plausible cause for the increased levels of E. coli on the surface is most likely explained by cross-contamination either by personnel disregarding hygiene measures or malpractice during sampling. In addition to standard trainings (GMP, HACCP, Good Hygiene Practices (GHP)), employees were given intensive training on food pathogens, risk assessment, microbiological testing and food safety culture. Particular attention was given to the thorough understanding the importance of personal hygiene and raising awareness of the role of each person in avoiding the risk of cross-contamination in the EMP. Correct surface sanitation proved important for the elimination and reduction of microbial contamination in the food production environment and played an important role in providing food quality in the dairy dessert facility.

Figure 6
Zone 2 microbiological analysis results (log cfu/cm²).

Our coliform findings after EMP were met target microbiological limit (<10 cfu/cm²) for Almond Board of California and The European Commission. Coliform rates were 0-10 cfu/cm² for bakery, pastry, and pasta samples collected from French Agri-Food Industries, consistent with the results reported here [⁴⁶]. In another study which examined the hygienic condition of the food production environment, mean coliform bacteria count was detected 5x10²-4.1x10³ cfu/cm² (2.92-3.61 log cfu/cm²) and average E. coli 2.3x10¹-1.5x10² cfu/cm² (1.36-2.17 log cfu/cm²) on food contact surfaces (chopping board, countertop, and knife) [⁴⁷]. It was noted that the values obtained in research were higher than values in our studies. In this research, the most important causes of differences in terms of coliform group microorganism can be told as the microorganism load of raw materials used in the making of milky desserts, improper cleaning practice and hygiene rules, application of inadequate heat and time at cooking process and the occurrence of contaminations after heat process.

S. aureus analysis results in Zone 1, Zone 2, and personnel changed from 0.84, 0.33 and 1.17 log cfu/cm² to 0 log cfu/cm² during study period (Figure 3,5 and 6). Our study showed that the number of S. aureus increase in Personnel during January because seasonal variation of S. aureus infection a higher in the cold weather of winter. Another study reported that seasonal variation of S. aureus infection has higher mortality in winter [⁴⁸]. Swab counts of S. aureus in prior to EMP were significantly (P< 0.05) higher than after-EMP. There were S. aureus positive swab samples after-cooking areas including gloves and uniform of packaging employees, door handle of packing area and the surface of the weigh table in packaging room during production of keskul. Considering that S. aureus, which may cause foodborne intoxication, is carried in the nose, throat, hair, and skin of humans, strict swap monitoring of personnel was implemented [⁴⁸]. Hand contamination of food handlers with S. aureus is an important risk factor for staphylococcal food poisoning. Handwashing, use of gloves and mask training was given after positive S. aureus results. Lee and coauthors [⁴⁹] reported in a study evaluating microbiological hand hygiene of food handlers that S. aureus counts of 3 staff higher than <10 cfu/cm² (1 log cfu/cm²) and 82 staff hand samples had no S. aureus microorganism. In addition, Yucel and coauthors [⁵⁰] determined that rate of coagulase (+) staphylococcus on the hands of kitchen staff was 21.8%. On the other hand, raw material microbiological quality is crucial because usage of sick animal’s milk (mastitis) for preparation dairy dessert since milky desserts may contain S. aureus [⁵¹].

Figure 7
Zone 3 microbiological analysis results (log cfu/cm²).

Figure 8
Zone 4 microbiological analysis results (log cfu/cm²).

Pre-EMP swab counts of yeast-mold in all environmental areas (Zone1,2,3 and 4) were significantly (P<0.05) higher than (4.09, 4.51, 4.79, 2.59 log cfu/cm²) compared with post-application (0, 0, 0.11 and 0 log cfu/cm²) (Figure 5,6,7 and 8). We investigated potential sources of yeast contamination and find yeast biofilm adhered to hard-to-reach process surface such as filling and packing machines and drains than developed targeted cleaning and sanitizing procedures to eliminate this unsuitability. Unsatisfactory environmental results for molds were also recorded within the same locations (drains, hard-to-reach points of machine) with yeast. Furthermore, it was found that the source of detected mold on the walls was condensation which formed during the warm moist air coming out of the cooking process. Our yeast-mold results after EMP are in accordance with a study of evaluation of an EMP for the microbial safety of air and surface in a dairy plant (<0.16 log cfu/cm³ for yeast-mold) [¹⁵]. In addition, Stobnicka-Kupiec and coauthors [³⁸] determined number of yeast and mould was in the range of 0-2.7 log cfu/cm² on dairy factories.

On the other hand, in another similar study, total yeast-mould counts were found between 1.1x10² cfu/cm² (2.04 log cfu/cm²) and 6.0x10² (2.77 log cfu/cm²) [⁴⁷]. It was observed that numbers of yeast-mould obtained were higher than at the end of our study values. The differences among researchers might result from raw material used, production technique, cleaning-sanitation efficiency, personnel hygiene, differences of air and environmental conditions.

Identification strengths and weaknesses of EMP's are critical for effective EMP applications. Two common weaknesses were identified in our study; first one lacked sufficient samples because not sampling enough amount and frequency defeats the purpose of EMP and puts your product at risk. The EMP sampling plan (Table 2), which includes the number of samples collected, sampling frequency and location, was created according to the risk-based approach and focusing on problem areas. The second weakness was lack of preventive and corrective action plan for inappropriate results and inability to follow. Corrective actions plan was implemented quickly in order to identify the root cause of the contamination and eliminate the potential risk of cross contamination to other surface or the food. Appropriate corrective and preventive actions were evaluated on a case-by-case basis by the EMP team and contained the following: (1) investigational sampling; (2) cleaning and disinfection; (3); review the workflow models (people and product flows); (4) “blocking and microbiological test” procedures for food; (5) resampling; and (6) training of staff [²²]. EMP, Hygiene- Sanitation, GMP and Food safety culture trainings and some practices such as performance evaluation, awards and events had positively affected the motivation of employees to adhere to safe handling practices. The number of disinfection region was increased in different parts of the production area for personnel easy access it when needed. Automatic dosed disinfectant foam system has been integrated into the facility to ensure that surfaces are cleaned more effectively and cost-effectively. Adenosine triphosphate test (ATP) equipment’s (which can be used to verify cleaning) were integrated to hygiene control and verification applications for determining the hygienic status of surfaces. Positive air pressure and different variety of filters (paper filter, hepa filter, etc.) was integrated to prevent all kinds of dust, polluted air and microorganisms in the air that may enter from the outside in the dairy dessert production area. The dry Peracetic acid (PAA) fogging system was used twice a week since Peracetic acid (PAA) is a powerful oxidant with bactericidal and fungicidal properties. Used high-efficiency UV and particulate air (HEPA) fan/filtration air sterilization systems to enhance inner air cleaning (especially in higher risk areas such as Zone 1). A study in a dairy plant environment noted that appropriate preventive and corrective actions, along with efficient monitoring would contribute to a reduction pathogen microorganism in the food chain [¹⁵].

In summary, this study investigated the microbiological status and efficiency of EMP in a medium-sized dairy dessert facility. Overall, our data indicate that significant mean differences (P<0,05) between microbial levels (TMAB, coliform, E. coli and yeast-mold) before and after EMP. These differences distinguished the surfaces with inefficient cleaning and sanitizing operations, especially wall, drain, air, personnel hand, door handles, spatulas, trays, floor. Similar to our findings, a number of other researchers have reported the Listeria-positive results are floors, walls, and drains [¹⁶, ⁵²]. Moreover, our study evidence provided that an effective EMP is key component of food safety. Zacharski and coauthors [¹⁵] recommended EMP optimization to control measures and hazard assessment regarding existing contamination issues. In another study on the frozen fruits and vegetable reported that EMP is an early warning system to detect pathogen-indicator microorganisms and plays crucial role in the monitor of microbiological hazards in food facility [¹⁸]. The survey on EMP practices in the food industries in France demonstrated that the interest in EMP practices by almost all participants and that this practice was in place for a large part of the agri-food industries [⁴⁶].

The difficulty of implementing an EMP is the lack of a fit-in-all procedure and information about EMP’s practical applications. It is known that EMP is highly specific and depends on food facility, type of produced products, hazard types and points, types of hygiene-sterilization practices, the size and architecture of facility etc. [¹⁷]. Our study provides a road map and key-information’s such as time, area, amount and frequency of sampling, baseline and target value and type of microorganism for implementation of scientifically supported efficient EMP. Providing periodical training, financial support and implementing effective FSMS are essential elements for sustainable EMP.

CONCLUSION

Nowadays, tendency to dairy desserts that ready to eat consumption products, is increasing due to globalization and intense lifestyle. Providing food safety and quality in these products is a very crucial issue in terms of public health and economy while they acknowledged as microbiologically risky product group. Monitoring the production environment as well as food products is an important combination to improve food safety and quality. EMP is a monitoring system that provides valuable information to evaluate the efficiency of hygiene-sanitation applications in food facilities and to prevent cross-contamination. The strength of the EMP is not to assess product acceptance, but to detect unacceptable microbiological contamination in the food processing environment in a timely manner so that corrective action can be taken. This study investigated the microbiological conditions of keskul final products, the raw materials, auxiliary materials, the production environment zone (tool, machine, air, surface, etc.) and staff during October 2019-March 2020 in a medium size dairy dessert plant. Provided evidence through statistical analysis demonstrate that an effective EMP plays a significant and crucial role in controlling microbiological hazards (p<0,05). EMP is only an early warning indicator and monitoring program, it must be supported by corrective and preventive actions to achieve safe food production. This is the first study on the implementation of EMP to dairy dessert products and provides current and scientific model to improve, implement and sustainable EMP’s for food industry. Currently, there is a lack of specification about EMPs specific limit for each zone. Determination of specific microorganisms and limits for each zone is crucial for interpretation the regionally test results. This identified gap can be filled by future studies on EMP.

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• Funding:
  This research funded by the Bursa Technical University Scientific Research Projects Coordination Unit with project No. 190Y022. Also, this study based on MSc thesis of Elif Onbasi.

Edited by

• Editor-in-Chief:
  Bill Jorge Costa

• Associate Editor:
  Bill Jorge Costa

Publication Dates

• Publication in this collection
  15 Nov 2024
• Date of issue
  2024

History

• Received
  27 Dec 2022
• Accepted
  19 July 2024