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Journal of Protection, Vol. 75, No. 4, 2012, Pages 706–716 doi:10.4315/0362-028X.JFP-11-260 Copyright G, International Association for Food Protection

Microbiological Performance of a Management System in a Food Service Operation

E. LAHOU,* L. JACXSENS, J. DAELMAN, F. VAN LANDEGHEM, AND M. UYTTENDAELE

Department of Food Safety and , Laboratory of Food and , University of Ghent, Coupure Links, 653, 9000 Ghent, Belgium Downloaded from http://meridian.allenpress.com/jfp/article-pdf/75/4/706/1682672/0362-028x_jfp-11-260.pdf by guest on 02 October 2021 MS 11-260: Received 26 May 2011/Accepted 11 October 2011

ABSTRACT The microbiological performance of a food safety management system in a food service operation was measured using a microbiological assessment scheme as a vertical sampling plan throughout the production process, from raw materials to final product. The assessment scheme can give insight into the microbiological contamination and the variability of a production process and pinpoint bottlenecks in the food safety management system. Three production processes were evaluated: a high-risk sandwich production process (involving raw preparation), a medium-risk hot meal production process (starting from undercooked raw materials), and a low-risk hot meal production process (reheating in a bag). Microbial quality parameters, indicators, and relevant ( monocytogenes, , cereus, and O157) were in accordance with legal criteria and/or microbiological guidelines, suggesting that the food safety management system was effective. High levels of total aerobic (.3.9 log CFU/50 cm2) were noted occasionally on gloves of food handlers and on food contact surfaces, especially in high contamination areas (e.g., during handling of raw material, preparation room). Core control activities such as hand hygiene of personnel and cleaning and disinfection (especially in highly contaminated areas) were considered points of attention. The present sampling plan was used to produce an overall microbiological profile (snapshot) to validate the food safety management system in place.

Some individuals tend to eat out of the home, often at because of a lack of a well-functioning food safety food service operations such as cafeterias, canteens, fast management system, are contaminated ingredients, dirty food outlets, bars, and restaurants (40, 56). A national food food contact materials, poor personnel hygiene practices, consumption survey in Belgium revealed that in 2004 more inappropriate storage temperatures, and insufficient than 35% of the population consumed more than 25% of (17, 29–31, 58). In food service operations, various types of their daily energy intake out of the home (34). Eating out at raw (at-risk) materials are used and a wide variety of final food service operations seems to be no longer reserved for products are served, including hot meals, cold sandwiches, special occasions. However, food service operations can be and salads. This multitude of products, processes, and involved in foodborne disease outbreaks associated with a personnel involved makes it very important to ensure safe variety of pathogens, e.g., Salmonella, spp., food service and to have a well-functioning food safety Escherichia coli O157, Listeria monocytogenes, Bacillus management system, as requested from all food business cereus, perfringens, and Staphylococcus aureus operations in Regulation (EC) 852/2004 on the hygiene of (13, 14, 35). foodstuffs (1). The microbiological quality and safety of Kitchens with a history of association with foodborne is largely affected by the performance of the food outbreaks or consumer complaints about food safety issues safety management system (26, 27). The application of good have significantly more frequent problems with personnel manufacturing practices and good hygiene practices as parts hygiene and inadequate raw material storage than do other of a (HACCP) plan and kitchens (53). Food handlers were epidemiologically linked the use of ISO (International Organization for Standardiza- to 80% of the outbreaks reported in Belgium (9). tion, Geneva, Switzerland) method 9001:2008 can improve Food handlers’ malpractices contributed to 97% of product quality and safety (32, 33). Periodic verification of foodborne illnesses associated with food service operations the HACCP plan is recommended. (59). Adequate process controls and periodic verification are The main causes of microbiological contamination and more effective than control of only final products (44). growth, which occur in food service operations mainly Swanson and Anderson (51) stated that testing of final products is equivalent to finding a needle in a haystack, * Author for correspondence. Tel: (z32) 09-2649390; Fax: (z32) 09- particularly in food service operations where a wide variety 2255510; E-mail: [email protected]. of final products are generated as output for the consumers. J. Food Prot., Vol. 75, No. 4 MICROBIAL PERFORMANCE IN INSTITUTIONAL CATERING 707

Moreover, sampling and microbiological analysis often are bags (no postprocessing contamination can occur) (process C). The perceived as costly. main difference between process B and process C was the A microbiological assessment scheme (MAS) devel- utilization of raw material in process B with its overall higher oped by Jacxsens et al. (26) includes minimal sampling and microbiological load and higher risk of contamination. analysis, but uses a systematic approach to assess the MAS. The MAS was developed as described by Jacxsens et microbiological performance of a company-specific food al. (26) and applied vertically throughout a production process. The safety management system (26). This sampling plan, when MAS (i) identifies critical sampling locations within the production accompanied by observations at the time of sampling and process, (ii) selects appropriate microbiological parameters to be discussion of results with the quality manager of the analyzed, (iii) defines the sampling procedures and analytical company, provides an overview of the microbiological methods, and (iv) helps in the interpretation of the results. Samples quality, hygiene, and safety level of products and processes were collected at various critical locations in the process A, B, and at a food business operation. Such information may help C processing lines from raw materials to final products and then managers identify bottlenecks in the core control activities analyzed to assess the microbiological performance of the core of an implemented food safety management system (37, 45). control activities in the implemented food safety management Downloaded from http://meridian.allenpress.com/jfp/article-pdf/75/4/706/1682672/0362-028x_jfp-11-260.pdf by guest on 02 October 2021 With this approach, samples are collected throughout the system. The same samples were collected and analyzed for the process from raw materials to final products at critical same parameters during three visits on three days in one restaurant of the food service operation to provide information on the locations on three different days (in a time period of maximum load and the distribution of the microbiological load at multiple weeks) and analyzed for multiple microbiological each sampling location in the production process. The visits took parameters. A microbiological profile of the production place in March 2009, February 2010, and March 2010. During process then can be established. each visit, 33 samples were collected and analyzed (Table 1). This The microbiological analyses to assess the food safety resulted in a total of 99 samples throughout the survey: 36 food management system performance are aimed at obtaining samples, 21 swabs for detection of L. monocytogenes, and 42 contamination profiles, which provide insight into the swabs for enumeration of hygiene indicators and determination of maximum microbiological counts and the distribution of the total viable bacteria count (TVC). A total of 147 analyses of the microbiological contamination. The sample analysis is quality parameters, 216 analyses of hygiene indicators, and 132 not meant as a guarantee of food safety but rather provides analyses of foodborne pathogens were performed. The number of verification of the preventive measures taken in the food samples was small, but they were collected as part of a periodic verification of the preventive measures implemented in the food service operation. The principle of the MAS is that a better service operation rather than as indicators of food safety. performing food safety management system would be better Samples were collected within the production processes on able to realize products with lower contamination levels and locations where loss of control will lead to unacceptable food less variation in contamination loads. MASs already have safety problems due to contamination with or growth and/or been applied in poultry meat preparation processing plants survival of (26). Those locations are referred to (45), a pork processing company (26), the lamb chain (42), critical sampling locations (CSLs) and are illustrated in Figure 1. and various dairy and meat processing plants in Europe In this study seven CSLs were identified. Samples were collected (27). In the present study, a MAS was developed for a food from at-risk (i.e., raw) materials at point of receipt (CSL 1) (e.g., service operation and was used in a vertical manner vegetables and frozen fish) to determine the initial contamination throughout the production process from raw materials to level of microorganisms and verify appropriate supplier selection. final products. Three different production processes in the Samples from intermediate products (CSL 2) (i.e., after regener- food service operation were evaluated to measure the ation and cooling) were collected throughout the production line where manual operations were performed and/or physical inter- microbiological performance of the food safety management vention processes occurred to verify good hygienic practices to system implemented in this food service operation. control microbiological growth and potential cross-contamination. Samples were collected from final products (CSL 3) after MATERIALS AND METHODS assemblage (sandwiches and salads) or at the where the Characterization of the food service operation. The food food was kept warm for prolonged periods in a hot bath (hot service operation selected for this case study comprised eight meal components) to verify the final storage and handling restaurants and 11 cafeterias at a university that were separated in conditions at the serving counter and thus maintain good different building areas in Ghent, Belgium. In the restaurants, hot microbiological quality. Sampling in the production environment meals, soups, sandwiches, and salads were served, whereas in the was conducted by taking swabs of gloves (CSL 4) and hands (CSL cafeterias no hot meals were available. In this catering establish- 5) of personnel that manipulated the food products (e.g., cutting ment, 650,000 hot meals and 29,000 sandwiches were served each vegetables or opening vacuum-packed bags of cooked chilled year. Each restaurant had its own regeneration kitchen where foods after final heat treatment) or taking swabs of food contact undercooked frozen or previously prepared foods delivered from surfaces (CSLs 6 and 7) (e.g., chopping boards, knives, and the supplier as frozen ( and freeze) or chilled (cook and chill) spoons) throughout the production processes. These environmental products were (re)heated and the cooking process was completed. samples were linked to samples of intermediate or final food Three main production processes were used in the food service products (Fig. 1). operation: (i) preparation of a sandwich and/or salad (process A), The microbiological parameters selected for this study (ii) production of a hot meal starting with unprocessed raw or differed depending on the type of food product (Table 1). undercooked frozen ingredients and preparation out of packaging Parameter selection was based on European legal criteria (2), (possibility of postprocessing contamination) (process B), and (iii) national action limits (15), and knowledge of the microbiological production of a hot meal starting with cooked products in reheating ecology of foods. Total aerobic bacteria, , 708

TABLE 1. Overview of critical sampling locations (CSLs) encompassing food products and production environment with the corresponding analyzed microbiological parameters and legal requirements (2, 3) or microbial guidelines (14, 49)a AL. ET LAHOU All processes Process A Process B Process C Criteriab Parameter Criteria (log CFU/g) Parameter Criteria (log CFU/g) Parameter Criteria (log CFU/g) Parameter (log CFU/16 cm2) Parameter CSL: 1, 2 3 1, 2, 3 1 2, 3 1 2, 3 2, 3 2 3 4, 5 6, 7 4, 5, 6, 7

Total viable zzm ~ 5 zzm ~ 5 m ~ 3 z m ~ 3 zz Good, #1; average. bacteriab M ~ 8 M ~ 7 M ~ 6 M ~ 6 #1.8; bad, #2.5; intolerable, .2.5 Lactic acid bacteriab zzm ~ 3 z m ~ 2 M ~ 7 M ~ 7 Yeastsb zzm ~ 3 z m ~ 2 M ~ 5 M ~ 5 Moldsb zzm ~ 3 z m ~ 2 M ~ 4 M ~ 3 B. cereus z m ~ 3c z m ~ 3b z m ~ 2b M ~ 4c M ~ 4b M ~ 5b Sulfite-reducing z m ~ 2 z m ~ 2 clostridiab M ~ 5 M ~ 5 L. monocytogenesd zzAbsent in 25 g or 2 zzAbsent in 25 g or 2 log CFU/g at end z Absent in 25 g or 2 log CFU/ z Absent on tested log CFU/g at end of g at end of shelf life surface of shelf life Salmonella zzAbsent in 25 gd zzAbsent in 25 gb,d z Absent in 25 gc,d E. coli O157b z Absent in 25 g Enterobacteriaceae z m ~ 2.7c zzm ~ 2b m~ 1.69b z m ~ 1c m ~ 1.69b zzGood, #1; average. M ~ 3.7c M ~ 3b M ~ 2.69b M ~ 2c M ~ 2.69b #1.8; bad, #2.5; intolerable, .2.5 E. coli zzm ~ 2d zzm ~ 2b m ~ ,1b z m ~ 1c m ~ ,1b zzAbsent on tested M ~ 3d M ~ 3b M ~ 1.69b M ~ 2c M ~ 1.69b surface S. aureus zzm ~ 2b zzm ~ 2b z m ~ 1c m ~ 2b zzAbsent on tested M ~ 3b M ~ 3b M ~ 2c M ~ 3b surface .Fo rt,Vl 5 o 4 No. 75, Vol. Prot., Food J. a CSL 1, raw materials at point of receipt; CSL 2, intermediated products; CSL 3, final products; CSLs 4 and 5, hands and gloves; CSLs 6 and 7, food contact surfaces. z, analysis was conducted for the parameter. m, maximum level of bacteria per test volume considered acceptable (food with values above this level in any sample is either marginally acceptable or unacceptable); M, maximum level of bacteria per test volume considered marginally acceptable (food with values at or above M in any sample is unacceptable). b According to microbiological guidelines of the LFMFP-UGent (54). c According to action limits of the FASFC (15).

d According to EU regulation 2073/2005 (2). Downloaded from http://meridian.allenpress.com/jfp/article-pdf/75/4/706/1682672/0362-028x_jfp-11-260.pdf by guest on 02 October 2021 October 02 on guest by http://meridian.allenpress.com/jfp/article-pdf/75/4/706/1682672/0362-028x_jfp-11-260.pdf from Downloaded J. Food Prot., Vol. 75, No. 4 MICROBIAL PERFORMANCE IN INSTITUTIONAL CATERING 709

overlayer and incubating for 72 h at 30uC) was used for the enumeration of lactic acid bacteria. extract glucose chloramphenicol selective medium (Bio-Rad, Hercules, CA), an AFNOR (Association Franc¸aise de Normalisation, Paris, France) validated method (NF V08-059 2002) (6), was used for enumeration of (incubation for 72 h at 22uC) and (incubation for 120 h at 22uC). Coli-ID chromogenic medium (bioMe´rieux, Marcy l’Etoile, France) (24 h of incubation at 44uC), an AFNOR validated method (BIO 12/5-01/99) (5), was used for enumeration of E. coli. ISO 21528-2:2004 (24) (plating on violet red bile agar with glucose with an overlayer and incubating for 24 to 48 h at 37uC) was used for enumeration of Enterobacteriaceae. ISO 6888-1:1999/Amd 1:2003 (20) (plating on Baird Parker agar and incubating for 24 to 48 h at 37uC) was used for enumeration of

S. aureus. Because low numbers were expected for S. aureus, 1ml Downloaded from http://meridian.allenpress.com/jfp/article-pdf/75/4/706/1682672/0362-028x_jfp-11-260.pdf by guest on 02 October 2021 of inoculum was spread on three plates. Enumeration of B. cereus was performed with ISO 7932:2004 (25) (plating on mannitol egg yolk polymyxin agar and incubating for 24 h at 30uC). Tryptose sulfite cycloserine selective medium with an overlayer (24 h of incubation at 37uC), an AFNOR validated method (XP V 08-061 1996) (4), was used for enumeration of sulfite-reducing anaerobic bacteria. ISO 16654:2001 (21) (an immunomagnetic separation FIGURE 1. Schematic overview of the main production processes method) was used for detection of E. coli O157:H7. The detection in a food service operation. Critical sampling locations (CSLs) of L. monocytogenes was performed using VidasLMO2 (bioMe´- within the processes were identified: CSL 1, raw materials; CSL 2, rieux), an AFNOR validated -linked fluorescent assay intermediate materials; CSL 3, final food products; CSLs 4 and 5, (ELFA) (BIO 12/11-03/04) (7). When positive results were gloves and/or hand of workers; CSLs 6 and 7, food contact surfaces. obtained, L. monocytogenes was enumerated from the same , production of a sandwich (process A); R, production of a hot sample according to ISO 11290-2:1998/Amd 1:2004 (19). meal starting with unprocessed raw or undercooked frozen Salmonella was detected using Vidas Easy SLM (bioMe´rieux), ingredients (process B); , production of a hot meal starting an AFNOR validated ELFA (BIO-12/16-09/05) (8). with cooked products with ‘‘reheating in bag’’ (process C). Data analysis and interpretation: microbiological safety yeasts, and molds were selected as indicators of overall quality. level profiles. Data were manipulated with MS Excel (Microsoft, Enterobacteriaceae, E. coli, and S. aureus were selected as Redmond, WA) to develop graphics and tables to illustrate visually hygiene indicators. The presence of the foodborne pathogens the levels and distribution of microbiological contamination during Salmonella, L. monocytogenes, E. coli O157:H7, B. cereus, and the three sampling periods. No means, standard deviations, or sulfite-reducing clostridia (as indicator for C. perfringens) was statistical analyses were needed to evaluate the variability in this food evaluated when appropriate for the food type. operation service because the microbiological analyses for measuring For food products, 300 g was aseptically collected with a the food safety management system performance were designed only sterile spoon or forceps and transferred to a sterile sampling bag. to obtain microbiological safety level profiles (MSLPs). These Food contact surfaces and gloves and hands were swabbed in a profiles provide insight into the maximum microbial counts and the delimited area of 50 cm2 using a sterile rayon swab premoistened distribution of microbial contamination, i.e., where to find in 7 ml of sterile peptone water (for microbial enumeration) or 5 ml contamination in the production process (26), and into the dynamics of demi-Fraser enrichment medium (for detection of L. monocy- of microbial contamination occurring as a result of the design and togenes). For knives, an area of 10 cm2 was swabbed because of application of the control strategies in a food safety management the limited surface area. The food samples and the moistened system. The results for each process were evaluated in two ways. swabs were transported in a cool box at #4uC to the laboratory. Individual results for each analyzed parameter were evaluated Microbiological analyses were performed in the laboratory within for each specific sampling location within the production process. 6 h of sample collection. For enumeration, 10 g of each food The results obtained at each location (e.g., CSL 1) were compared sample was homogenized for 2 min in 90 ml of sterile peptone with defined legal criteria (2, 3). In the absence of legal criteria, water. For detection of Salmonella and L. monocytogenes, a 25-g microbiological values established by the Laboratory of Food subsample was weighed in a stomacher bag and homogenized for Microbiology and Food Preservation of the University of Ghent 2 min in 225 ml of the respective (semi)selective medium, i.e., (LFMFP-UGent) (54) or the action limits established by the buffered peptone water for the detection of Salmonella and demi- Belgian Federal Agency for the Safety of the Food Chain (FASFC) Fraser for the detection of L. monocytogenes. Swab samples were version June 2010 (15) were used for comparison (Table 1). The vortexed for 10 s and incubated for detection of specific organisms. score attribution system is summarized in Table 2. When the legal Tenfold serial dilutions were made in sterile peptone water for requirements or the guidelines are exceeded (score 0) for a specific microbial enumeration. in a specific sampling location, the specific control For each microorganism, standardized methods (ISO) or activity in the food safety management system at that location is alternative (rapid) methods validated according to ISO 16140:2003 not working properly. Corrective action(s) is then needed to change (22) were applied. The reference method ISO 4833:2003 (23) this noncompliance situation and improve the current food safety (plating on plate count agar and incubating for 72 h at 30uC) was management system performance. used for the enumeration of aerobic mesophilic bacteria. ISO Individual results for each analyzed parameter also were 15214:1998 (18) (plating on de Man Rogosa Sharpe agar with an evaluated across sampling locations (CSL 1 to CSL 7) within the 710 LAHOU ET AL. J. Food Prot., Vol. 75, No. 4

TABLE 2. Score attribution systema Food products

Legal criteria, action Score limits of FASFC LFMFP-UGent Food contact surfaces (LFMFP-UGent)

3 R # m R # target R # 10 CFU/16 cm2 Absent in x gramsb Absent on surfacec 2 m , R , M Target , R # tolerance 10 CFU/16 cm2 , R # 69 CFU/16 cm2 1 R ~ M Tolerance , R # use-by date or best-before date 69 CFU/ 16 cm2 , R # 350 CFU/16 cm2 0 R . M R . use-by date or best-before date R . 350 CFU/16 cm2 Present in x gramsb Present on surfacec a R, result in CFU per gram (food products) or CFU per 16 cm2 (food contact surfaces); m, maximum level of bacteria per test volume considered acceptable; M, maximum level of bacteria per test volume considered marginally acceptable (food with values at or above M in Downloaded from http://meridian.allenpress.com/jfp/article-pdf/75/4/706/1682672/0362-028x_jfp-11-260.pdf by guest on 02 October 2021 any sample is unacceptable). b Specifically for L. monocytogenes, E. coli O157, and Salmonella. c Specifically for E. coli, L. monocytogenes, and S. aureus. production process. A microbiological safety level was attributed microbiological safety level was established for each to each type of microbiological parameter to obtain an overall view microbiological parameter over all sampling locations of microbiological quality, hygiene, and the safety level of within the production process to evaluate the current products and processes at the food service operation. Each microbiological status of the food safety management microbiological parameter was given a score from 1 to 3. Level system. The overall MSLP score (Fig. 2) for process A 3 is the best result (legal criteria or guidelines are met, and no (the production of a sandwich or salad) was 31 of a possible improvements are needed); the current level of the food safety management system is deemed high enough to cope with any 33 (11 microbiological parameters with a maximum hazards. Level 2 is a moderate result (bacterial values exceed legal microbiological safety level of 3), and for process B criteria or guidelines, and improvements are needed in a single (production of a hot meal starting with unprocessed raw or control activity of the food safety management system), and level 1 undercooked frozen ingredients) the score was 32 of a is a poor result (bacterial values exceed legal criteria or guidelines, possible 33. For process C (production of a hot meal starting and improvements are needed in multiple control activities of the with cooked products and reheating in a bag) the score was food safety management system). The sum of the levels of all 23 of a possible 24. The maximum for this process was microbiological parameters results in an MSLP score, which gives only 24 because no at-risk raw material was present (i.e., an indication of the actual performance level of the food safety products were cooked in bags) and no samples of raw management system (26, 45). When the MSLP score is lower than material were collected; therefore, no analyses of lactic acid the maximum achievable value, then improvement of the current bacteria, yeasts, and molds were conducted. For each food safety management system is possible. Examination of the details of the MSLP results for each microbiological parameter, process, the maximum MSLP score was nearly obtained observations during sampling, and discussion with the quality (Fig. 2), indicating that the current food safety management manager of the operation may provide insight into the points of system has no major flaws in its ability to produce safe and attention and result in useful recommendations for follow-up. hygienic food products. However, continuous verification of the implemented HACCP system by microbiological Hand hygiene. In the present case study, hand hygiene was analyses of raw materials and final products, regular identified as a point of attention. To evaluate the general hand supplier audits, and continuous training of personnel in hygiene of the food handlers, extra swab samples of gloves and good hygienic practices is recommended. Results of other hands were collected during a 6-month period and analyzed for studies have indicated that inherent barriers to effective TVC and the hygiene indicators E. coli, S. aureus, and implementation of HACCP systems exist in catering Enterobacteriaceae. A sterile rayon swab premoistened in 7 ml of sterile peptone water was used to swab a delimited area of companies (16), and more effort should be made to apply 50 cm2 and then placed aseptically into its tube. The swabs were HACCP principles (39). In a study of catering establish- stored and transported in a cool box at #4uC. Microbiological ments, Marzano and Balzaretti (39) found that a percentage analyses were performed in the laboratory within 6 h of sampling. of samples did not meet microbiological reference standards A total of 93 extra samples were collected from employees for L. monocytogenes, S. aureus, E. coli, and total coliforms. working at different restaurants and performing different activities Evaluation of the details of each type of production in the food service operation. Descriptive statistical analysis of the process in the present study revealed no E. coli O157 or data was performed with MS Excel. Salmonella. The results for the spore-forming pathogens B. cereus and sulfite-reducing clostridia were below the RESULTS AND DISCUSSION detection limit of the analytical method (100 CFU/g) at all The 99 samples collected during the initial three visits sampling times. Only in the sandwich production process were analyzed for multiple parameters (147 analyses of (process A) was L. monocytogenes detected in a sandwich quality parameters, 216 analyses of hygiene indicators, and made with a spread of raw meat prepared with Worcester- 132 analyses of foodborne pathogens; Table 3), and a shire sauce during the first visit (Table 3). The level of L. TABLE 3. Detailed results of the microbiological assessment schemea Food safety indicators (log CFU) Hygiene indicators (log CFU) Overall CATERING INSTITUTIONAL IN PERFORMANCE MICROBIAL indicators (log CFU) 4 No. 75, Vol. Prot., Food J. E. coli L. monocy- Enterobac- Process CSL Sample O157 Salmonella togenes B. cereus SRCb E. coli teriaceae S. aureus TVCc LABd Yeasts Molds

A 1 Raw material A A A NA NA ,1.0 NA ,1.0 3.7–4.2 2.4–3.3 2.7–3.5 ,2–2.3 Raw material A A A NA NA ,1.0 NA ,1.0 6.0–6.3 3.1–5.5 4.4–4.6 2.0–2.6 Raw material A A A NA NA ,1.0 NA ,1.0 4.2–4.9 2.4–2.6 3.0–3.2 2.0–2.9 2 Raw material in AA A NANA,1.0 NA ,1.0 3.8–5.3 2.3–3.1 3.2–3.9 ,2.0–3.0 cool bar Raw material in AA A NANA,1.0 NA ,1.0 5.9–6.9 2.9–5.1 4.3–4.6 ,2–2.9 cool bar Raw material in AA A NANA,1.0 NA ,1.0 4.3–6.8 2.3–3.9 3.1–5.0 2.0–2.7 cool bar 3 Sandwich NA A P (,2 log ,2NA,1.0–1.0 2.5–3.5 ,1.0 4.7–5.4 3.2–4.7 3.3–4.9 ,2.0–3.0 CFU) 4 Gloves NA NA NA NA NA A ,1.0 ,1.0 2.1–4.3 NA NA NA (2/3)e 5 Gloves NA NA NA NA NA A ,1.0–2.4 ,1.0 2.1–4.3 NA NA NA (2/3)e 6 Gastronorm NA NA A NA NA A ,1.0 A ,1.0–1.9 NA NA NA 7 Cutting board (in NA NA A NA NA A ,1.0 A ,1–5.3 NA NA NA use) (1/3)e Knife (in use) NA NA A NA NA A ,1.0 A ,1.0–5.8 NA NA NA (1/3)e B 1 Raw material NA A A NA NA ,1.0 ,1.0 ,1.0 2.8–4.1 ,1.0–2.7 ,2.0–2.9 ,2.0–2.0 2 After regeneration NA A A ,2.0 ,1.0 ,1.0 ,1.0 ,1.0 ,1.0–3.9 NA NA NA 3 In buffet NA A A ,2.0 ,1.0 ,1.0 ,1.0 ,1.0 ,1.0 NA NA NA 4 Gloves NA NA NA NA NA A ,1.0 ,1.0 ,1.0–2.3 NA NA NA 5 Gloves clean NA NA NA NA NA A ,1.0 ,1.0 ,1.0–1.7 NA NA NA Gloves NA NA NA NA NA A ,1.0 ,1.0 ,1.0–1.2 NA NA NA 6 Gastronorm NA NA A NA NA A ,1.0 A ,1.0–3.9 NA NA NA (1/3)e 7 Spoon NA NA A NA NA A ,1.0 A ,1.0–1.9 NA NA NA C 2 After regeneration NA A A ,2.0 ,1.0 ,1.0 ,1.0 ,1.0 ,1.0 NA NA NA 3 In buffet NA A A ,2.0 ,1.0 ,1.0 ,1.0 ,1.0 1.0–1.6 NA NA NA 4 Gloves NA NA NA NA NA A ,1.0 ,1.0 2.3–4.1 NA NA NA (1/3)e 5 Gloves NA NA NA NA NA A ,1.0 ,1.0 0–1.5 NA NA NA 6 Gastronorm NA NA A NA NA A ,1.0 A ,1.0 NA NA NA 7 Spoon NA NA A NA NA A ,1.0 A ,1.0 NA NA NA a A, absent in 25-g sample or on 50 or 10 cm2; P, present in 25-g sample or 50 or 10 cm2; NA, parameter not analyzed for this product or critical sampling location. Results are in log CFU per gram for food products and in log CFU/50 cm2 for environment samples. Values with , symbol are below the quantification limit. b SRC, sulfite-reducing clostridia. c TVC, total viable bacteria count. 711 d LAB, lactic acid bacteria.

e Values in parentheses are the number of samples exceeding legal criteria or guidelines/number of samples tested. Downloaded from http://meridian.allenpress.com/jfp/article-pdf/75/4/706/1682672/0362-028x_jfp-11-260.pdf by guest on 02 October 2021 October 02 on guest by http://meridian.allenpress.com/jfp/article-pdf/75/4/706/1682672/0362-028x_jfp-11-260.pdf from Downloaded 712 LAHOU ET AL. J. Food Prot., Vol. 75, No. 4

FIGURE 2. Microbial safety level profile for three production processes in the catering establishment: process A, sand- wich production; process B, production of hot meal starting with raw or undercooked material; process C, production of a hot meal by reheating in a bag. For each parameter, a microbial safety level was determined: 1, low; 2, moderate; 3, high. Dashed line indicates the maximum score that could be obtained for each process. Downloaded from http://meridian.allenpress.com/jfp/article-pdf/75/4/706/1682672/0362-028x_jfp-11-260.pdf by guest on 02 October 2021

monocytogenes in this sample was ,100 CFU/g and thus All results obtained for Enterobacteriaceae, an indica- did not exceed the European Commission Regulation 2073/ tor of overall good manufacturing practices, and E. coli, as a 2005 criterion (2) for L. monocytogenes in ready-to-eat fecal hygiene indicator, in each process line were satisfac- foods at the time of consumption (38). Upon reporting of tory. Enterobacteriaceae were present in the sandwich this L. monocytogenes result to the quality manager of the production process at 2.5 to 3.5 log CFU/g. These results are food service operation, steps were taken by the catering within acceptable levels as defined by the action limits of establishment for follow-up sampling of a second batch of the FASFC (Table 1). The presence of Enterobacteriaceae this sandwich spread. This second sample also was in this sandwich probably was due to the presence of contaminated with L. monocytogenes, indicating that the vegetables, which generally carry high levels of Entero- source of L. monocytogenes was most likely located at the bacteriaceae (35). For the personal hygiene indicator S. supplier (11). Further investigation at the supplier of the aureus, no unacceptable levels were found. sandwich spread revealed L. monocytogenes on the For the quality parameters of lactic acid bacteria, yeasts, equipment in the production area. This pathogen can adhere and molds (Table 3) in processes A and B, all results were to surfaces and form on various materials in food within microbiological reference standards. However, high processing facilities (10). Based on this information, the TVCs (.4.3 log CFU/50 cm2) were found on gloves (CSLs food service operation changed suppliers for this type of 4 and 5) of food operators and on food contact surfaces sandwich spread, and no L. monocytogenes was found in (CSL 7) in process A during various visits (Table 3). this spread during the two subsequent visits. This example Microbiological reference standards for TVCs were exceed- illustrates the impact of supplier selection on the perfor- ed on gloves, which is inevitable in the present context mance of the food safety management system. because of manipulation of raw materials with high The number of samples analyzed for pathogen detection microbiological loads, i.e., vegetables. The TVCs of the in the present MAS was limited. The objective of this analyzed food products (ready-to-eat sliced mixed lettuce, sampling plan was to provide an overall microbiological tomatoes, and cucumber) in the sandwich production profile (snapshot) to evaluate the current food safety process were 3.7 to 6.9 log CFU/g. High TVCs on gloves management system. Statistically based on-going monitor- can be controlled by changing gloves on a regular basis to ing of pathogens in raw materials and final products should avoid cross-contamination (49). TVCs for food contact complement the MAS as a sampling plan to allow veri- surfaces, i.e., the cutting board and knife, also exceeded the fication of proper implementation of HACCP principles on microbiological guidelines. Further investigation revealed a continuous basis. However, in particular for pathogenic that these utensils were not replaced during the service organisms with low prevalence (,1to5%), inherent period, a total of 4 h. However, Schaffner et al. (46) found limitations in sampling schemes determine the level of that changes in the bacterial population on a plastic cutting contamination detectable. board for a 5-min interval ranged from a decrease of 4 CFU/ J. Food Prot., Vol. 75, No. 4 MICROBIAL PERFORMANCE IN INSTITUTIONAL CATERING 713

FIGURE 3. Distribution of bacterial contamination on hands and/or gloves of all food handlers (A) and of food handlers performing a specific food activity (B). Downloaded from http://meridian.allenpress.com/jfp/article-pdf/75/4/706/1682672/0362-028x_jfp-11-260.pdf by guest on 02 October 2021 cm2 to an increase of 13 CFU/4 cm2. When a cutting board TVCs for assessing hand hygiene, guidelines were based on is used for 60 min, it usually will become contaminated with hygiene scores for surfaces after cleaning and disinfection in more than 50 CFU/4 cm2. As a consequence, cleaning or a companies because of a lack of guidelines change of cutting boards during the food service period is specific for food contact surfaces in food service operations recommended to reduce the probability of formation or for hand hygiene (50, 54). According to these guidelines, and cross-contamination (41, 43, 46). 43% of the gloves and/or hand samples collected in the In process B (production of a hot meal starting with regeneration area, 57% of samples from the (buffet) counter, unprocessed raw or undercooked frozen ingredients), high 59% of the samples from the sandwich bar, and 25% of the TVCs (3.9 log CFU/50 cm2) also were found on food samples from the self-service counter would be classified as contact surfaces (CSL 6), namely an inox serving tray, due unsatisfactory (.3 log CFU/50 cm2) based on the TVCs on to contact with raw frozen fish filets, which is a high-risk gloves and/or hands (Fig. 3). However, the hygiene raw material with high microbiological loads. These results indicator E. coli was absent in all analyzed samples, and indicated that improvements in some of the core control S. aureus was detected in only one sample. Enterobacteri- activities in the food safety management system of the food aceae were detected in 18 (19%) of the 93 samples service operation were needed, e.g., cleaning and disinfec- (Table 4). tion of food contact surfaces, switching gloves and washing The results of the supplementary samples collected hands on a regular basis, and cleaning the utensils properly from hands and/or gloves of food handlers (Fig. 3) indicate during service (48). Schaffner et al. (46) found that surfaces a difference in total microbiological contamination of the with high mean microbiological levels and a high hands and/or gloves of food handlers performing different percentage of samples with bacteria that were ‘‘too activities. For example, a significant difference (P , 0.05) numerous to count’’ tended to be plastic. Dome´nech- in TVC on the hands and/or gloves was found between food Sa´nchez et al. (12) found that 26.0% (n ~ 4,611) of the handlers working at the cash desk and food handlers surfaces analyzed had microbiological levels higher than the working at the counter, sandwich bar, or regeneration area. recommended standards of ,1.3 log CFU/cm2. A significant difference (P , 0.05) in TVC on the hands In process C (production of a hot meal starting with and/or gloves also was found between food handlers cooked products and reheating in a bag), TVCs of 2.3 to 4.1 refilling the self-service counter and food handlers working log CFU/50 cm2 were found on the gloves of a food at the (buffet) counter or sandwich bar. No significant operator (CSL 4) in the regeneration area. This finding was difference (P . 0.05) in TVC on the hands and/or gloves in contrast to the very low levels of bacteria on the gloves of was found between food handlers working in the regener- a food operator on the buffet line, which were ,1.0 to 1.5 ation area and those working at the counter, sandwich bar, log CFU/50 cm2 (Table 3). This difference may be due to or self-service counter. No significant difference in TVC on the highly contaminated surfaces of cupboards, refrigera- the hands and/or gloves was found between food handlers tors, ovens, etc. in the regeneration room. On the buffet line, working at the counter and those working at the sandwich food operators serve customers with clean (thus less bar and between food handlers working at the cash desk and contaminated) utensils. This contrast illustrates the difficulty those refilling the self-service counter. inherent in using the TVC as an indicator. For trend A lower level of total microbiological contamination monitoring, appropriate guidelines for food contact surfaces (1.0 log CFU/50 cm2) was established for activities at the and gloves should be developed taking into account the cash desk, and a higher level (2.0 log CFU/50 cm2) was various activities that occur at different locations, direct or established for activities at the self-service counter and the indirect contact with foods, and the type of foods handled. regeneration area. The highest microbiological contamina- Because hand hygiene was identified as a point of tion (3.0 log CFU/50 cm2) was noted for activities at the attention, extra samples were collected from gloves and (buffet) counter, and the sandwich bar (Fig. 3). hands of food handlers working in different kitchen areas to Results of these supplementary samples supported the evaluate general hand hygiene. For interpretation of the recommendation that specific microbiological guidelines 714 LAHOU ET AL. J. Food Prot., Vol. 75, No. 4

TABLE 4. Detection of hygiene indicators on hands and/or gloves of food handlers performing specific activities in institutional catering No. of samples postive for a:

Location No. of samples tested E. coli Enterobacteriaceae S. aureus

Regeneration area 23 0 4 1 Counter 23 0 6 0 Cash desk 9 0 1 0 Sandwich bar 22 0 6 0 Self-service 16 0 1 0 Total 93 0 18 1 a Samples were considered positive when the level of microorganisms was at or above the limit of detection of the method, which was 1 log CFU/50 cm2 for E. coli and Enterobacteriaceae and 2 log CFU/50 cm2 for S. aureus. Downloaded from http://meridian.allenpress.com/jfp/article-pdf/75/4/706/1682672/0362-028x_jfp-11-260.pdf by guest on 02 October 2021 should be formulated for hands and/or gloves for each According Luning et al. (37), the concept behind food location. These guidelines can be developed after establish- safety management system diagnosis is that companies ing an overall baseline by taking daily, weekly, or monthly operating in a high-risk context need an advanced food samples at each location and performing trend analysis. This safety management system to achieve high levels of food analysis can allow identification of problem areas in the safety. In a moderate-risk context, an average food safety process that need more attention (36). With these baseline management system may be sufficient for adequate food results, in particular by sampling contact materials and safety, whereas in a low-risk context even a basic food hands when food handlers are using good manufacturing safety management system would be sufficient to maintain practices (e.g., changing gloves between handling raw and acceptable microbiological quality, hygiene, and safety. cooked products, according the protocol, and When the food safety services operation obtains some changing cutting boards during service when there is no power in supplier relationships, the risks associated with time to clean them), a microbiological guideline can be set. inadequate raw materials may be reduced by evaluating the Schaffner et al. (46) recommended the use of microbiolog- current specifications and systematically auditing the food ical modeling and Monte Carlo simulation as tools for safety management system of the supplier (37). These steps evaluating cutting board polices and setting appropriate lead to systematic quality improvement, which is beneficial sanitary microbiological criteria. for both consumer and supplier, because food safety will be In this study of the food service operation, the period enhanced. Therefore, to have a better control on food safety between the first and the last visit covered 1 year. During in a food service operation, microbiological specifications this year, a snapshot of the performance of the food safety must be present for all incoming food products (37, 52). management system was taken at each visit, allowing The hot meals in the operation in the current study were validation of the preventive measures implemented in the almost all produced from bagged cooked chilled foods that food safety management system. By comparing the MSLPs, had been partially prepared by the supplier and subjected to which reflect performance, conclusions can be reached only reheating in bag on the food service premises. That concerning decline, stabilization, or improvement in perfor- type of food product has already been subjected to a (mild) mance. During the first and last visits, the operation was less heat treatment at the supplier, which results in a less busy, whereas during the second visit it was very busy; contaminated product entering the food service operation. however, the MSLPs of the processes remained stable Therefore, outsourcing of basic steps in food preparation (comparable results) across all visits (Fig. 2), which is an means there will be a smaller amount of high-risk material indication of a stable and well-performing food safety (e.g., raw meat and poultry, raw vegetables) entering the management system. Those kinds of results may not be food service operation, and the pressure on the food safety obvious in food service establishments because of high staff management system of the operation is reduced (37). turnover, laborious production processes, and a complex Reheating in a bag also reduces the risk for introduction variety of (raw) material and food products (57). and dispersion of microbiological contamination in the The positive assessment of the food safety management production environment and thus fewer critical control system performance also was due to proper supplier points in the food safety management system (37, 47). selection and to outsourcing of basic steps of food Even with medium-risk food products, which are still preparation. Proper supplier selection (according to micro- raw in the center but have been subjected to some heat biological specifications and auditing) results in the delivery treatment (e.g., or ) on the outside, there is a of high-quality food products, thus putting less pressure on lower chance of contaminating the kitchen environment the food safety management system of a food service than when completely raw materials are processed. At the operation (37). High-quality raw materials are less likely to time of slaughter, the muscle tissue of a healthy animal is have undesirably high initial contamination levels or allow essentially sterile, but the surface of the meat becomes growth or survival of pathogens; therefore, they contribute contaminated during slaughter and subsequent handling to a low-risk environment. (28). The same is true for the majority of and J. Food Prot., Vol. 75, No. 4 MICROBIAL PERFORMANCE IN INSTITUTIONAL CATERING 715 vegetables. 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