The effects of mandatory HACCP implementation on microbiological indicators of process hygiene in meat processing and retail establishments in Serbia

Meat Science 114 (2016) 54–57

Contents lists available at ScienceDirect

Meat Science journal homepage: www.elsevier.com/locate/meatsci

Short communication

The effects of mandatory HACCP implementation on microbiological indicators of process hygiene in meat processing and retail establishments in Serbia Igor Tomasevic a,⁎, Jelena Kuzmanović b, Aleksandra Anđelković b, Miroslava Saračević b, Marija M. Stojanović b, Ilija Djekic c a b c

Department of Animal Source Food Technology, University of Belgrade, Faculty of Agriculture, Nemanjina 6, 11080 Belgrade, Serbia Center for Food Analysis, Zmaja od Nocaja 11, 11000 Belgrade, Serbia Food Safety and Quality Management Department, University of Belgrade, Faculty of Agriculture, Nemanjina 6, 11080 Belgrade, Serbia

a r t i c l e

i n f o

Article history: Received 28 August 2015 Received in revised form 24 November 2015 Accepted 15 December 2015 Available online 20 December 2015 Keywords: Meat processing Meat retail HACCP Process hygiene Food contact surfaces Aerobic colony count Enterobacteriaceae Staphylococcus

a b s t r a c t A total of 48,246 microbiological test results were collected from 130 meat processing plants and 220 meat retail facilities over a seven year period: 41 months before and 43 months after HACCP implementation. Our results confirm a strong positive effect of mandatory HACCP implementation on process hygiene indicators in meat establishments. Significant reductions were observed in the number of hygiene indicator organisms on all types of surfaces examined and types of meat establishments investigated. The improvement of process hygiene was articulated as aerobic colony count reduction of at least 1.0 log10 CFU/cm2 for food contact surfaces and over 2 log10 CFU/cm2 for cooling facilities (refrigerators, freezers and other meat cooling devices). Meat handlers' hands hygiene was least positively affected. The period after mandatory HACCP implementation was also marked by a steady decline of positive Enterobacteriaceae and Staphylococcus samples. Process hygiene advances for meat processing plants and meat retail facilities were similar. © 2015 Elsevier Ltd. All rights reserved.

1. Introduction Hygiene measures in meat production, processing and retail aim at assuring meat safety, preventing rapid spoilage of the meat and protecting its quality. Hazard Analysis and Critical Control Point (HACCP), which strongly relies on prerequisite programs including Good Hygiene Practices (GHPs) and Standard Sanitation Operating Procedures (SSOPs), provides improved process hygiene conditions that are necessary for the production of safe meat and meat products throughout the meat chain. By the end of the 20th century, HACCP had been mandated, implemented and was in routine operation in every meat company involved in international trade (Jenson & Sumner, 2012). Microbiological testing of carcasses is commonly used for HACCP verification in abattoirs. In the European Union (EU), this is accomplished by determining whether aerobic colony counts

⁎ Corresponding author. E-mail addresses: [email protected] (I. Tomasevic), [email protected] (J. Kuzmanović), [email protected] (A. Anđelković), [email protected] (M. Saračević), [email protected] (M.M. Stojanović), [email protected] (I. Djekic).

http://dx.doi.org/10.1016/j.meatsci.2015.12.008 0309-1740/© 2015 Elsevier Ltd. All rights reserved.

and Enterobacteriaceae counts, the so-called hygiene indicator organisms, are within given acceptable ranges (European Commission, 2005). However, satisfactory verification results from the slaughtering lines do not guarantee safe meat or meat products. Furthermore, microbial counts from food contact surfaces can be, in some cases, higher than microbial counts from carcasses, so that meat can sustain an increase in microbial load during passage through the meat cutting and processing rooms (Nortjé et al., 1989a, 1989b). Meat cutting and deboning operations, performed in meat processing plants, involve relatively intensive manipulation and handling of meat which markedly increases the microbial risks due to: (a) microbial cross-contamination via hands and utensils (knives, saws, conveyers, etc.); and (b) transfer of bacteria from the meat surface to the internal parts (Nørrung & Buncic, 2008). Personnel surfaces (hands and clothes) and other meat contact surfaces like equipment (saws and mincers), knives and cutting boards are also consistent contributors to contamination of meat and meat products at the retail level (Nortjé et al., 1989a). In Serbia, HACCP was mandated by the Veterinary Law (Anonymous, 2005) which obliged all animal source food producers, regardless of their size, to adopt and implement a food safety system based on the

I. Tomasevic et al. / Meat Science 114 (2016) 54–57

principles of GHP and HACCP (article 82). The deadline was initially January 1st 2009 but later, with the adoption of a new food safety law (Anonymous, 2009), this was extended to June 1st 2011. A recent survey revealed that 93.5% of Serbian abattoirs, meat processors and retailers have a complete and certified HACCP system in place, while 6.5% had implemented HACCP, but they had no third party certification (Tomašević et al., 2013). The effect of HACCP on process hygiene indicators in abattoirs has been examined before (Hutchison, Thomas, Small, Buncic, & Howell, 2007; Mackey & Roberts, 1993; Nastasijevic, Mitrovic, Popovic, Tubic, & Buncic, 2009), but to the best of our knowledge it has never been done for the continuing part of the meat supply chain: meat processing plants and meat retail facilities. Therefore, our study was designed to determine whether the mandatory implementation of HACCP systems in meat processing plants and meat retail facilities had any significant effect on their microbiological indicators of process hygiene. 2. Materials and methods 2.1. Sampling A total of 48,246 swab samples were analyzed from two types of meat establishments: 130 meat processing plants and 220 meat retail facilities. The period covered was seven years (2008 to 2014), divided into two terms: the first was from January 1st 2008 until May 31st 2011 (a period of 41 months and before mandatory HACCP implementation), and the second was from June 1st 2011 until December 31st 2014 (a period of 43 months and after HACCP became obligatory). Samples were taken from three types of surfaces: food (meat) contact surfaces (FCS) (cutting boards, machines, knives and slicers, tables and containers), cooling facilities (CF) (refrigerators, freezers and other meat and meat product cooling devices) and meat handlers' hands (HS). Swabs were obtained over a measured surface area using a sterile template (10 × 10 cm) and a viscose tip swab using a technique based on the ISO 18593 method. The number of samples per year and type of meat establishment and surface examined are presented in Table 1. 2.2. Microbiological methods During the first period (January 1st 2008–May 31st 2011), samples were analyzed according to the Regulation on methods for microbiological analysis and superanalysis of food, No 25/1980 C.F.R (1980) in force, for aerobic colony count (ACC) using methods coherent with ISO 4833:2003. The new Regulation on general and specific food hygiene requirements at any stage of production, processing and trade, No. 72/2010 C.F.R. (2010), effective from June 1st 2011, legally prescribed methods that were used in the second period of our investigation. All samples were analyzed according to ISO for ACC (ISO 4833:2003), Enterobacteriaceae (ISO 215282:2004), coagulase positive Staphylococcus (ISO 6888-1:1999),

55

Salmonella (ISO 6579:2002) and Listeria monocytogenes (ISO 11290-1:1998). Samples were examined in an ISO/IEC 17025:2005 accredited laboratory. 2.3. Analysis of results Categorical variables (classes of surface hygiene) were expressed as percentages. Chi-square test for association was used to discover possible relationships between results of microbiological indicators of process hygiene and the period they were sampled. Yate's correction was calculated when the expected frequency was less than 5. The level of statistical significance was set at 0.05. Statistical processing was performed using Microsoft Excel 2010 and SPSS Statistics 17.0. 3. Results and discussion Bacterial numbers of 3.0 log10 CFU/cm2 once were regarded as indicative of good hygiene or of an efficient meat commercial operation (Sheridan & Lynch, 1979). Today, consumer demands for safer meat are continually commanding higher and stricter hygiene standards at all levels of the meat supply chain. The limit that distinguishes dirty (or unsatisfactory) from clean (or satisfactory) food contact surface is not defined by current Serbian or EU regulations. Recent research in the food service industry suggested different values for this limit, ranging from 1.7 log10 CFU/cm2 (de Oliveira et al., 2014) to 0.6 log10 CFU/cm2 (Garayoa, Díez-Leturia, Bes-Rastrollo, García-Jalón, & Vitas, 2014). For the purpose of our investigation, all the process hygiene indicator results (numbers of bacteria) (n) were divided into four classes as follows: Class I (n ≤ 1 log10 CFU/cm2); Class II (1 log10 CFU/cm2 b n ≤ 2 log10 CFU/cm2); Class III (2 log10 CFU/cm2 b n ≤ 2.7 log10 CFU/cm2); and Class IV (n ≥ 2.7 log10 CFU/cm2). Chi-square tests confirmed statistically significant associations between the classes of microbiological indicators of process hygiene results and the period they were sampled, before or after mandatory HACCP implementation, for all three types of surfaces examined and for both meat processing and meat retail establishments (Table 1). The most evident improvement of process hygiene indicators was observed for food contact surfaces. Before HACCP, 90.45% of the food contact surface ACCs in meat processing plants and 98.3% of the food contact surface ACCs in meat retail were above 2 log10 CFU/cm2. This is similar to the findings of Cetin, Kahraman, and Buyukunal (2006) in Turkish red meat processing plants, where the mean total mesophilic aerobic count on food contact surfaces was 2.58 log10 CFU/cm2 before HACCP was introduced. In our study, after mandatory HACCP implementation, these values dropped below 2 log10 CFU/cm2 in 96.38% of cases for meat plants and 85.8% of cases for meat retail (Table 1). This concurs with the study of Hutchison et al. (2007), and their conclusion that bacterial numbers from food contact surfaces in red meat processing plants decreased significantly in a period of four years after compulsory HACCP implementation in United Kingdom. The work of Evans, Russell, James, and Corry (2004) demonstrated that bacteria were present on all food refrigeration equipment

Table 1 Number of samples in meat establishments by types of surfaces.

Meat plants

Total Meat retail

Total

FCS HS CF FCS HS CF

2008

2009

2010

2011a

2011b

2012

2013

2014

Total

698 (84.9%) 81 (9.9%) 43 (5.2%) 822 4797 (88.1%) 495 (9.1%) 150 (2.8%) 5442

628 (83.1%) 67 (8.9%) 61 (8.1%) 756 2026 (72.6%) 614 (22%) 149 (5.3%) 2789

801 (82.1%) 103 (10.6%) 72 (7.4%) 976 2624 (69.8%) 867 (23.1%) 268 (7.1%) 3759

366 (86.9%) 26 (6.2%) 29 (6.9%) 421 1181 (66.7%) 430 (24.3%) 159 (9%) 1770

420 (81.1%) 54 (10.4%) 44 (8.5%) 518 2193 (67.2%) 719 (22%) 349 (10.7%) 3261

954 (79.7%) 147 (12.3%) 96 (8%) 1197 5129 (68.3%) 1351 (18%) 1026 (13.7%) 7506

1134 (84.1%) 140 (10.4%) 74 (5.5%) 1348 6008 (73%) 1269 (15.4%) 958 (11.6%) 8235

1164 (81.2%) 159 (11.1%) 111 (7.7%) 1434 5665 (70.7%) 1542 (19.2%) 805 (10%) 8012

6165 777 530 7472 29,623 7287 3864 40,774

N — represents the number of samples; (%) represents their share in the sample (totals may not equal to 100% because of rounding); FCS — food contact surfaces, HS — meat handlers' hands, CF — cooling facilities; 2011a — January 01st 2011–May 31st 2011; 2011b — June 01st 2011–December 31st 2011.

56

I. Tomasevic et al. / Meat Science 114 (2016) 54–57

Table 2 Relative contribution of aerobic colony counts in meat establishments before and after mandatory implementation of HACCP. Class I Meat plants

Meat retail

Class II

Class III

Class IV

Total

Food contact surfaces 0 (0%) BHa 1869 (50.9%) AHb χ2 = 4792.986; P b 0.001

238 (9.55%) 1670 (45.48%)

1190 (47.73%) 118 (3.21%)

1065 (42.72%) 15 (0.41%)

2493 (100%) 3672 (100%)

Hand swabs 0 (0%) BHa 13 (2.6%) AHb Yates' χ2 = 331.364; P b 0.001

7 (2.53%) 1 (0.2%)

124 (44.77%) 485 (97%)

146 (52.71%) 1 (0.2%)

277 (100%) 500 (100%)

Cooling facilities 0 (0%) BHa AHb 290 (89.23%) χ2 = 476.34; P b 0.001

20 (9.76%) 35 (10.77%)

121 (59.02%) 0 (0%)

64 (31.22%) 0 (0%)

205 (100%) 325 (100%)

Food contact surfaces 0 (0%) BHa 7488 (39.42%) AHb χ2 = 19,575.262; P b 0.001

181 (1.7%) 8812 (46.39%)

3550 (33.41%) 720 (3.79%)

6896 (64.89%) 1975 (10.4%)

10,627 (100%) 18,995 (100%)

Hand swabs 0 (0%) BHa 12 (0.25%) AHb χ2 = 2991.798; P b 0.001

33 (1.37%) 29 (0.59%)

1144 (47.53%) 4830 (98.96%)

1230 (51.1%) 10 (0.2%)

2407 (100%) 4881 (100%)

Cooling facilities 0 (0%) BHa AHb 2615 (83.33%) χ2 = 3563.594; P b 0.001

21 (2.89%) 496 (15.81%)

427 (58.82%) 24 (0.76%)

278 (38.29%) 3 (0.1%)

726 (100%) 3138 (100%)

N — represents the number of samples from food establishments during the observed period; (%) —represents their share in the sample (totals may not equal to 100% because of rounding); BH — period before mandatory implementation of HACCP; AH — period after mandatory implementation of HACCP; a,b — periods denoted with different letters have significantly different results at P b 0.001; Class I (n ≤ 1 log10 CFU/cm2); Class II (1 log10 CFU/cm2 b n ≤ 2 log10 CFU/cm2); Class III (2 log10 CFU/cm2 b n ≤ 2.7 log10 CFU/cm2); Class IV (n N 2.7 log10 CFU/cm2).

examined, with the highest degree of the contamination for raw red meat cooling facilities. Our results showed that before HACCP implementation, Class I (n ≤ 1 log10 CFU/cm2) for ACC for meat cooling facilities was effectively non-existent, while after HACCP and its prerequisite programs were successfully executed, this class accounted for 89.23% of meat plant and 83.33% of meat retail ACCs (Table 2). Class IV (n ≥ 2.7 log10 CFU/cm2) prevailed for hand swab ACCs in meat processing plants (52.71%) and meat retail (51.1%) until May 31st 2011, before HACCP implementation. This is similar to a South African meat retail hygiene study, where the mean count from hand swabs was 3.27 log10 CFU/cm2 (Nortjé et al., 1989a). In the current study, in the 43 month period that followed HACCP implementation, Class III (2 log10 CFU/cm2 b n ≤ 2.7 log10 CFU/cm2) took precedence, with 97% of hand swab ACCs from meat processing plants and 98.96% of hand swab ACCs from meat retail falling into this class (Table 2). We can conclude that meat handlers' hand hygiene was the least, although still positively, affected by the mandatory HACCP implementation, among the surfaces we examined. Also, mean ACC numbers on

hand swabs in meat retail in our study were lower than the 3.27 log10 CFU/cm2 observed in South African meat retail (Nortjé et al., 1989a). During the 43 month period after the mandatory implementation of HACCP, the incidence of Enterobacteriaceae steadily declined both in meat processing plants and in meat retailers for all types of surfaces examined (Table 3). The improvement in microbiological indicators of process hygiene was more obvious in meat retail facilities, especially regarding Enterobacteriaceae detected on food contact surfaces, where the incidence of this bacterial group dropped from 31.4% in the second half of 2011 to 14.4% in 2014. During the same period, there was a 10% reduction in the incidence of Enterobacteriaceae on food contact surfaces in meat processing plants (Table 3). Meat handlers' hands showed the highest incidence of Staphylococcus among the surfaces examined, with 13% of hands in meat processing plants being positive during the second half of 2011 and 5.2% being positive in meat retailers in 2013 (Table 3). Although the effect of HACCP was not that apparent as in the case of Enterobacteriaceae, there is

Table 3 Positive samples of Enterobacteriaceae and Staphylococcus in meat establishments after mandatory implementation of HACCP.

Enterobacteriaceae

FCS HS CF

Staphylococcus

FCS HS CF

MP MR MP MR MP MR MP MR MP MR MP MR

2011b

2012

2013

2014

80 (19.0%) 689 (31.4%) 10 (18.5%) 88 (12.2%) 4 (9.1%) 56 (16%) 7 (1.7%) 27 (1.2%) 7 (13%) 18 (2.5%) 0 (0.0%) 1 (0.3%)

137 (14.4%) 1335 (26.0%) 10 (6.8%) 150 (11.1%) 5 (5.2%) 147 (14.3%) 6 (0.6%) 47 (0.9%) 5 (3.4%) 61 (4.5%) 1 (1.0%) 2 (0.2%)

112 (9.9%) 989 (16.5%) 13 (9.3%) 105 (8.3%) 4 (5.4%) 63 (6.6%) 1 (0.1%) 23 (0.4%) 10 (7.1%) 66 (5.2%) 0 (0.0%) 2 (0.2%)

105 (9.0%) 815 (14.4%) 16 (10.1%) 127 (8.2%) 7 (6.3%) 45 (5.6%) 3 (0.3%) 18 (0.3%) 9 (5.7%) 40 (2.6%) 0 (0.0%) 0 (0.0%)

n — represents the number of positive samples; (%) — represents their share in the sample (totals may not equal to 100% because of rounding); FCS — food contact surfaces, HS — meat handlers' hands, CF — cooling facilities; 2011b — June 01st 2011–December 31st 2011; MP — meat plants; MR — meat retail.

I. Tomasevic et al. / Meat Science 114 (2016) 54–57

good reason to believe that the decline of Staphylococcus was due to the mandatory adoption of HACCP. After HACCP was fully implemented, Salmonella was detected on only one, and L. monocytogenes on two, food contact surfaces in meat plants during 2012. Regarding meat retail food contact surfaces, Salmonella was present on one surface during 2012 and two in 2013 while L. monocytogenes was detected on five in 2011, 15 in 2012 and one in 2014. In contrast to the findings of Evans et al. (2004), where Enterococcus and Staphylococcus aureus were found most frequently in cooling facilities of red meat processing plants, our study detected L. monocytogenes only once in cooling facilities, while Staphylococcus was never detected. 4. Conclusion The decline in bacterial numbers on food contact surfaces, meat handlers' hands and cooling facilities in our study presents strong evidence of improved process hygiene indicators and justifies the adoption of GHPs and SSOPs in meat establishments. This relatively large-scale study found that implementation of HACCP was associated with an improvement in process hygiene in meat establishments. However, this finding is necessarily limited in scope, as it is not currently possible to determine whether such improvements will have, or have had, any similar positive effect on the incidence of meatborne disease. Clearly, to establish that, further research is necessary, both in Serbia and elsewhere. Conflict of interest None of the authors has a financial or personal relationship with other individuals or organizations that could inappropriately influence or bias the contents of this paper. References Anonymous (2005). Veterinary law. Official Gazette of the Republic of Serbia, vol. 91 No. 05. Anonymous (2009). Food safety law. Official Gazette of the Republic of Serbia, vol. 41 No. 09.

57

Cetin, O., Kahraman, T., & Buyukunal, S. K. (2006). Microbiological evaluation of food contact surfaces at red meat processing plants in Istanbul, Turkey. [Article]. Italian Journal of Animal Science, 5(3), 277–283. European Commission (2005). Commission Regulation (EC) No. 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. Official Journal of the European Union, L 338/1. Evans, J. A., Russell, S. L., James, C., & Corry, J. E. L. (2004). Microbial contamination of food refrigeration equipment. Journal of Food Engineering, 62(3), 225–232. Garayoa, R., Díez-Leturia, M., Bes-Rastrollo, M., García-Jalón, I., & Vitas, A. I. (2014). Catering services and HACCP: Temperature assessment and surface hygiene control before and after audits and a specific training session. Food Control, 43(0), 193–198. Hutchison, M. L., Thomas, D. J. I., Small, A. H., Buncic, S., & Howell, M. (2007). Implementation of compulsory hazard analysis critical control point system and its effect on concentrations of carcass and environmental surface bacterial indicators in United Kingdom red meat slaughterhouses. Journal of Food Protection, 70(7), 1633–1639. Jenson, I., & Sumner, J. (2012). Performance standards and meat safety — developments and direction. Meat Science, 92(3), 260–266. Mackey, B. M., & Roberts, T. A. (1993). Improving slaughter hygiene using HACCP and monitoring. Fleischwirtschaft, 73(1), 58–61. Nastasijevic, I., Mitrovic, R., Popovic, K., Tubic, M., & Buncic, S. (2009). The effects of a nonintervention HACCP implementation on process hygiene indicators on bovine and porcine carcasses. Meso, XI(4), 232–239. Nørrung, B., & Buncic, S. (2008). Microbial safety of meat in the European Union. Meat Science, 78(1–2), 14–24. Nortjé, G. L., Nel, L., Jordaan, E., Naudé, R. T., Holzapfel, W. H., & Grimbeek, R. J. (1989a). A microbiological survey of fresh meat in the supermarket trade. Part 1: Carcasses and contact surfaces. Meat Science, 25(2), 81–97. Nortjé, G. L., Nel, L., Jordaan, E., Naudé, R. T., Holzapfel, W. H., & Grimbeek, R. J. (1989b). A microbiological survey of fresh meat in the supermarket trade. Part 2: Beef retail cuts. Meat Science, 25(2), 99–112. de Oliveira, A. B. A., da Cunha, D. T., Stedefeldt, E., Capalonga, R., Tondo, E. C., & Cardoso, M. R. I. (2014). Hygiene and good practices in school meal services: Organic matter on surfaces, microorganisms and health risks. Food Control, 40(0), 120–126. Regulation on general and specific food hygiene requirements at any stage of production, processing and trade, no. 72/2010 C.F.R. (2010). Regulation on methods for microbiological analysis and superanalysis of food, no. 25/1980 C.F.R(1980). Sheridan, J. J., & Lynch, B. (1979). Effect of microbial contamination on the storage of beef carcasses in an Irish meat factory. Irish Journal of Food Science and Technology, 3(1), 43–52. Tomašević, I., Šmigić, N., Đekić, I., Zarić, V., Tomić, N., & Rajković, A. (2013). Serbian meat industry: A survey on food safety management systems implementation. Food Control, 32(1), 25–30.