A Microbial Assessment Scheme to measure microbial performance of Food Safety Management Systems

International Journal of Food Microbiology 134 (2009) 113–125

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International Journal of Food Microbiology

j ourna l homepage: www.e lsev ie r.com/ locate / i j foodmicro

A Microbial Assessment Scheme to measure microbial performance of Food SafetyManagement Systems

L. Jacxsens a,⁎, J. Kussaga a,b, P.A. Luning b, M. Van der Spiegel b, F. Devlieghere a, M. Uyttendaele a

a Department of Food Safety and Food Quality, Laboratory of Food Preservation and Food Microbiology, Faculty of Bioscience Engineering, Ghent University,Coupure Links, 653, 9000 Ghent, Belgiumb Product Design and Quality Management Group, Department of Agrotechnology and Food Sciences, Wageningen University, P.O. Box 8129, NL-6700 EV Wageningen, the Netherlands

⁎ Corresponding author. Mailing address: DepartmQuality, Laboratory of Food Microbiology and Food Pre9000 Ghent, Belgium. Tel.: +32 9 264 60 85; fax: +32

E-mail address: [email protected] (L. Jacxs

0168-1605/$ – see front matter © 2009 Elsevier B.V. Aldoi:10.1016/j.ijfoodmicro.2009.02.018

a b s t r a c t
a r t i c l e i n f o
Keywords:Food Safety Management SystemMicrobiological food safetyPerformance tool

A Food Safety Management System (FSMS) implemented in a food processing industry is based on GoodHygienic Practices (GHP), Hazard Analysis Critical Control Point (HACCP) principles and should address bothfood safety control and assurance activities in order to guarantee food safety. One of the most emergingchallenges is to assess the performance of a present FSMS. The objective of this work is to explain thedevelopment of a Microbial Assessment Scheme (MAS) as a tool for a systematic analysis of microbial countsin order to assess the current microbial performance of an implemented FSMS. It is assumed that lownumbers of microorganisms and small variations in microbial counts indicate an effective FSMS. The MAS is aprocedure that defines the identification of critical sampling locations, the selection of microbiologicalparameters, the assessment of sampling frequency, the selection of sampling method and method of analysis,and finally data processing and interpretation. Based on the MAS assessment, microbial safety level profilescan be derived, indicating which microorganisms and to what extent they contribute to food safety for aspecific food processing company. The MAS concept is illustrated with a case study in the pork processingindustry, where ready-to-eat meat products are produced (cured, cooked ham and cured, dried bacon).

© 2009 Elsevier B.V. All rights reserved.

1. Introduction

Microbial food safety has emerged to be a global concern (NØrrungand Buncic, 2008; Sofos, 2008). In response to the increasing numberof foodborne illnesses, governments all over theworld are intensifyingtheir efforts to improve food safety (Anonymous, 2002; CodexAlimentarius Commission, 2003; Orriss and Whitehead, 2000;Schlundt, 2002;Wallace et al., 2005). Regulations forced food businessoperators in the agri-food chain to design and implement a FoodSafety Management System (FSMS) in order to control the outbreaksof foodborne illnesses (Baird-Parker, 1995; Jacxsens et al., 2009;Luning et al., 2006; Schlundt, 2002; Tsalo et al., 2007). An FSMS can bedefined as a company specific system of control and assuranceactivities in order to realise and guarantee food safety. Controlactivities aim at keeping product and process conditions withinacceptable limits in order to realise food safety, while assuranceactivities concern the evaluation of system performance and organiz-ing necessary changes (Luning and Marcelis, 2007). Nowadays,several Quality Assurance (QA) standards are available, like ISO

ent of Food Safety and Foodservation, Coupure links 653,9 225 55 10.ens).

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22000 (ISO, 2005b), International Food Standard (IFS, 2007), andGlobal Standard for food safety (BRC, 2008), which are specificallydeveloped for food (processing) industries and against whichcertification is possible (often demanded by retailers). A big challengefor food business operators is to translate and to implement theserequirements in a company specific FSMS, in order to assure foodsafety and in many cases also food quality. A company specific FSMSshould be a translation of Good Hygienic Practices (GHP), HazardAnalysis Critical Control Point system (HACCP), management policies,traceability and recall systems into company specific setting (CIES,2007; FAO/WHO, 2007; Luning and Marcelis, in press; Jacxsens et al.,2009).

The performance of FSMS in practice is, however, still variable(Cormier et al., 2007; Manning et al., 2006; Tsalo et al., 2007), andattention is shifting from implementing QA standards to the betterunderstanding of the performance of an FSMS (Doménech et al., 2008;Luning et al., 2008; Stringer and Hall, 2007). As a consequence, variousaudit tools have been developed to determine the performance towardsQA standards (e.g. CIES, 2007; Cormier et al., 2007; Doménech et al.,2008;Wallace et al., 2005), but theybasicallycheckon compliance to theset requirements, for instance, during internal or external auditing (Vander Spiegel et al., 2005). Recently, an instrument has been developed todiagnose in a comprehensive and differentiatedway a company specificFSMS, independent of the QA standard that is implemented (Luninget al., 2008, in press).

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Table 1Distinct control strategies with core control activities as addressed by the FSMSdiagnostic instrument (based on Luning et al., in press) and linked to the identifiedcritical sampling locations (CSL) in the proposed case study (see Table 2).

Preventive measures CSL

These strategies are aimed at creating circumstances to prevent entry and or growth ofpathogens in food production systems by reducing the chance on (cross)contamination or growth

Indicators to assess design of preventive measures• Adequacy of product specific preventive measures (e.g. control of raw

materials)1

• Sophistication of hygienic design of equipment and facilities 2, 7/8/9• Adequacy of cooling facilities 3• Specificity of sanitation program 2, 7/8/9• Extent of personal hygiene requirements 2, 10/11/12

Intervention processesThese are distinguished from physical (like heat treatment, irradiation, high hydrostatic

pressure, drying), chemical (like the use of preservatives, salts, organic acids, smoke),and biological interventions (like the use of probiotics, lactic acid bacteria,fermentation, and natural antimicrobials like lysozyme)

Indicators to assess the design of intervention processes• Adequacy of intervention equipment 4• Specificity of maintenance program for intervention equipment• Effectiveness intervention methods 4

Monitoring systemThey affect food safety by providing information about the actual status of product or

process conditions, which enables process corrections, removal of non conformanceproducts, and system improvements in case of structural problems

Indicators to assess design of monitoring system• Appropriateness of CCP analysis• Appropriateness of standards and tolerances• Adequacy of measuring equipment to monitor process/product• Specificity of calibration program for measuring and analytical equipment• Specificity of sampling design/measuring plan• Extent of corrective actions

Operation of core control activities2

Indicators to assess actual operation of control activities• Actual availability of procedures1

• Actual compliance to procedures• Actual performance product specific measures• Actual hygienic performance of equipment and facilities• Actual cooling capacity• Actual process capability of intervention processes• Actual measuring equipment performance• Actual analytical equipment performance

1Procedures for cleaning, personal hygiene, maintenance and calibration interventionequipment, calibration and verification measuring and analytical equipment, CCPprocedures.2CSLs 5 and 6 indicate the performance of the overall food safety control activities.

114 L. Jacxsens et al. / International Journal of Food Microbiology 134 (2009) 113–125

According to Luning et al. (in press), a more sophisticated FSMSwould bebetter able to realise productswith lower contamination levelsand less variation in contamination loads. The FSMS diagnose on systemlevel gives, however, no indication of the actual microbial performanceof companies' FSMS. Food processing companies commonly usemicrobial testing of final products to assess if their products meet foodsafety criteria (e.g. ICMSF, 2002; Legan, 2001). These criteria are set bydifferent stakeholders or regulatory bodies, like EU and/or countryregulations and/or customers' requirements but are also used to guidethe manufacturing process enabling a proper evaluation and definepreventive actions (Anonymous, 2005; Kvenberg and Schwalm, 2000;Martins and Germano, 2008). Different authors recommended the useofmicrobial testing to evaluate Critical Control Points (e.g. Cormier et al.,2007; González-Miret et al., 2001; Kvenberg and Schwalm, 2000;Martins and Germano, 2008; Swanson and Anderson, 2000) and toevaluate procedures for Good Hygienic Practices (GHPs) and StandardOperating Procedures (SOPs) (e.g. Brown et al., 2000; Eisel et al., 1997;Leaper and Richardson, 1999). However, to our knowledge, nosystematic microbiological evaluation of an FSMS performance hasbeen described previously.

This paper presents a Microbial Assessment Scheme (MAS) that canbeused for systematic analysis ofmicrobial counts to assess themicrobialperformanceof core control activities in an implementedFSMS.Microbialanalyses to assess the FSMS performance are aimed at obtaining insightin contamination profiles, which means insight into the maximum levelofmicrobial counts and the distribution inmicrobial contamination. Thisinformation gives insight into the dynamics of microbial contaminationas a result of the designed and applied control strategies in an FSMS. Theconcept of MAS is illustrated with a case study in a pork processingcompany, where ready-to-eat meat products are made.

2. Materials and methods

2.1. FSMS diagnostic instrument principle

The structure of the FSMS diagnostic instrument is applied as thestart point for the development of MAS. It comprises a comprehensivelist of core control and grids to assess at which levels these activities areexecuted. The systematic diagnosis reveals which core control activitiesare addressed in companies' FSMS and at which level. The basicassumption behind this assessment tool is that systems performing on ahigher level are more predictable and better able to achieve a desiredsafety outcome, because of less ambiguity (due to more insight in theunderlying mechanisms) and less uncertainty (due to more accurateinformation) (Luning andMarcelis, 2006; Luning et al., in press). Table 1provides more detailed information about the core control activities inthe FSMS, diagnosed by the diagnostic instrument. A distinction ismadebetween preventive measures, intervention processes and monitoringsystems, each strategy contributes differently to the control of microbialfood safety (Luning et al., 2008).

2.2. Elaboration of Microbial Assessment Scheme (MAS)

The proposed concept of MAS is based on a comprehensiveliterature study in this field, discussions with experts on the concept ofFSMS diagnosis (Luning and Marcelis, 2006, 2007; Luning et al., 2006,in press) and practical experience in food processing companies inimplementing their FSMS and fulfilling the legal/retail/QA standardsrequirements by the Laboratory of Food Microbiology and FoodPreservation of Ghent University, Belgium (LFMFP-UGent) (Jacxsenset al., 2006, 2007). The MAS procedure includes different elementswhich are discussed below.

2.2.1. Identification of critical sampling locationsCritical sampling locations (CSL) are defined as locations where

microbial sampling provides information about the performance of

core control strategies as addressed in the FSMS diagnostic instrument(Table 1). In other words, loss of control at these locations will lead tounacceptable food safety problems due to contamination, growthand/or survival of microorganisms. The locations, where samples aretaken, will differ depending on the control activities that areaddressed in the companies specific FSMS (Table 2 is exemplified forthe illustrating case study).

A first CSL is the point of receipt of raw materials because initialconcentrations of microorganisms give insight into the potential safetyrisks of the raw materials, which puts demands on the FSMS. Eisel et al.(1997) and Codex Alimentarius Commission (2003) recommended theinspection of raw materials before processing and where necessarylaboratory tests should bemade to establish fitness for use. According toLuning et al. (in press) higher initial levels of pathogens require moresophisticated and reliable FSMS. The microbial performance at this CSLgives insight in the adequacyof the rawmaterial control in theFSMS (e.g.proper selection procedures of suppliers and specifications of rawmaterials (Jacxsens et al., 2009; Luning et al., 2008)).

Another CSL, that is assigned in the MAS, is during processing ofraw materials such as portioning, deboning, cutting and mincing,

Table 2MAS procedure elaborated as a case study for the pork processing industry.

No CSL Microbiologicalparameters

Frequencya Sampling method Interpretation of results

1 At point of receipt ofraw materials(raw pork meat parts)

— Aerobic mesophilicplate count (APC)

3 times 1 sample Non-destructive methodon 100 cm2 of raw porkmeat parts

a) According to EU Regulation2073/2005 Category 2.1.2b

— Salmonella APC: mc=3.5 log CFU/cm2

— E. coli Md=4.5 log CFU/cm2

— Enterobacteriaceae Enterobacteriaceae:— L. monocytogenes m=1.5 log CFU/cm2

2 After deboning andcutting or portioning(fresh pork meat cuts)

— APC 3 times 1 sample Non-destructive methodon 100 cm2 of raw porkmeat cuts

M=2.5 log CFU/cm2

— Salmonella b) According to EU Regulation2073/2005 Category 2.1.4 Salmonellaabsent in the area tested

— E. coli c) According to microbiological guidevalues of LFMFP-UGente

— Enterobacteriaceae E. coli absent in the area tested— L. monocytogenes L. monocytogenes: absent in the area tested

3 After interventionstrategy; curing(raw cured bacon).

— APC 3 times 1 sample Destructive method on30 g of raw cured baconbefore packaging

According to microbiological guide valuesof LFMFP-UGent for meat preparations

— Salmonella a) APCm=5.7 log CFU/g

— E. coli M=6.7 log CFU/g— Enterobacteriaceae b) Enterobacteriaceae— L. monocytogenes m=3.7 log CFU/g

M=4.7 log CFU/gc) E. colim=2.7 log CFU/cm2

M=3.7 log CFU/gd) Salmonella: absent in 25 ge) L. monocytogenes: absent in 25 g

4 After chilling or coolingprocesses i.e. fastcooling (cooked ham)

— APC 3 times 1 sample Destructive method on30 g of cooked ham beforepackaging

According to microbiological guide valuesof LFMFP-UGente for cooked productswithout post contamination


— E. coli M=4.0 log CFU/g— Enterobacteriaceae b) Enterobacteriaceae— L. monocytogenes Below detection limit

c) E. coli: Below detection limitd) Salmonella: absent in 25 ge) L. monocytogenes: absent in 25 g

5 After packaging of thefinal product(cooked ham)

— APC 3 times 1 sample Destructive method on30 g of packaged cookedham

According to microbiological guidevalues of LFMFP-UGente for cookedproducts with post contamination

— Salmonella a)APCm=3.0 log CFU/g


M=2.0 log CFU/gc) E. colim=b 10 CFU/gM=1.0 log CFU/g

d) Salmonella: absent in 25 ge) L. monocytogenes: absent in 25 g

6 After packaging of thefinal product(raw cured bacon)

— APC 3 times 1 sample Destructive method on30 g of packaged rawcured bacon

According to microbiological guidevalues of LFMFP-UGente for rawmildly salted meat products



M=3.0 log CFU/gc) E. colim=2.7 log CFU/cm2

M=3.7 log CFU/gd) Salmonella: absent in 25 ge) L. monocytogenes: absent in 25 g

7 Working tables at deboningsection (initial stage of theprocess — production area)

— APC 3 times 3 samples at start–middleand end of the production day

Surface swabbing of25 cm2 of the table

According to microbiological guide valuesof LFMFP-UGente

— E. coli Salmonella and L. monocytogenes: absentin the tested area

— Enterobacteriaceae— Salmonella— L. monocytogenes

(continued on next page)

115L. Jacxsens et al. / International Journal of Food Microbiology 134 (2009) 113–125

Table 2 (continued)

No CSL Microbiologicalparameters

Frequencya Sampling method Interpretation of results

8 Working tables at cured meat loinspreparation (middle of theprocess — production area)


Surface swabbing of25 cm2 of the table— E. coli


9 Working tables at packagingsection (final stage of theprocess — packaging area)


Surface swabbing of25 cm2 of the table— E. coli


10 Hands or gloves of food operatorsat deboning section — productionarea

— E. coli 3 times 3 samples at start–middleand end of the production day

Surface swabbing of25 cm2 of the hands

According to microbiological guide valuesof LFMFP-UGente

— Enterobacteriaceae St. aureus: below detection limit— S. aureus

11 Hands of food operators at curedmeat loins preparation section (middleof the process — production area)

— E. coli 3 times 3 samples at start–middleand end of the production day

Surface swabbing of25 cm2 of the hands— Enterobacteriaceae

— S. aureus12 Hands of food operators at the

packaging area— E. coli 3 times 3 samples at start–middle

and end of the production daySurface swabbing of25 cm2 of the hands— Enterobacteriaceae

— S. aureus

a Frequency of MAS as explained in Section 2.2.3.: CSLs 1–6: 3 times are 3 days in 3 consecutive months (i.e. March, April and May); CSLs 7–12: 3 times are 3 days in 3 consecutivemonths (i.e. March, April and May) and 3 samples per time (day).

b Abrasive sponges are applied for the carcass/meat part swabbing, therefore, the process hygiene criteria, according to EU Regulation 2073/2005 need to be adapted (Anonymous,2005). Via the non-destructive method, it must be considered that only a fraction of the cells are captured. In Anonymous (2001) it is stated that with swabbing only 20% of the totalflora is captured. In a reviewing article of Capita et al. (2004) an average of 50% is mentioned. The Scientific Committee of the Food Safety Agency of Belgium (FAVV, 2006) hasconcluded that for both Enterobacteriaceae and total count with non-destructive method, the faction of captured cells is 0.5 log lower compared to the destructive method.Consequently, the process hygiene criteria need to be adapted by this 0.5 log unit.

c m = under limit.d M = upper limit.e LFMFP-UGent = Laboratory of Food Microbiology and Food Preservation, Ghent University.


which are potential sources of (cross)contamination if not properlyhandled. The main sources of (cross)contamination during processingcome from food contact surfaces, equipment and the food operators(Gill et al., 2001; McEvoy et al., 2004; Tsalo et al., 2007). Consequently,this CSL provides insight into the microbial performance as a result ofvarious preventive measures addressed in companies' FSMS, such asthe extent of personal hygiene, specificity of sanitation program,adequacy of product specific preventive measures, and hygienicdesign equipment and facilities (Table 1).

A third distinct CSL is at the cooling facilities. Adequate coolingcapacity prevents the growth of mesophiles and mesophilic patho-gens and the development of spores and limits the growth ofpsychrotrophic microorganisms (ICMSF, 2005; Mossel et al., 1995).Inadequate food temperature control is reported to be amongst one ofthe most common causes of foodborne illness or food spoilage (CodexAlimentarius Commission, 2003; Todd et al., 2007). Therefore, a CSL isdefined after critical cooling activities in order to assess the adequacyof cooling facilities present in the food processing company.

Intermediate products directly after core intervention strategies, arealso considered as CSL. It provides information on the actual effectivenessof the applied intervention processes in the FSMS. Different interventionstrategies are presented in Table 1. The level of microbial counts in finalproducts is another CSL, because it gives an indication of the overallperformance of an FSMS as a result of technology and managerialdependent control activities that are executed to keep bacterial countsbelow required limits (Luning and Marcelis, 2006, 2007).

The MAS also addresses food contact surfaces as critical samplinglocations, because it will give insight into the actual status of thesophistication of hygienic design equipment and facilities, and specifi-city of sanitation program present as a preventive measure in the FSMS(Table 1). According to the different studies (e.g. Aarnisalo et al., 2006;Bagge-Ravn et al., 2003; Cools et al., 2005; EHEDG, 2007; Fuster-Vallset al., 2008; Jessen and Lammert, 2003) diverse foodpathogenic bacteriaare able to attach to food contact surfaces, which can subsequently bedetached during production and contaminate food as it passes thesurface. Equipment and surfaces can be a source of direct contamination

when they have not been effectively cleaned or have been allowed toremain moist between cleaning and use (e.g. Evans et al., 2004).

If during processing direct hand contact with the food product ispossible, also the hygiene of the hands/gloves of the food operators isconsidered as a CSL, indicating the performance of personal hygiene asa preventive measure in the FSMS (Table 1). Hands can contaminatefood through residential flora of the skin e.g. micrococci, staphylo-cocci, propionic bacteria and corynebacteria; and contact betweenhands and the environment, which contaminates hands withtransient flora such as fecal indicators E. coli and Salmonella (Aarnisaloet al., 2006; Dijk et al., 2007).

2.2.2. Selection of the microbiological parametersFor each CSL, microbiological parameters must be defined. The

selected microbiological parameters will differ depending on theproduction processes and food type that are addressed in the specificcompany. Table 2 exemplifies this selection for the presented case study.An FSMS is in the first place aiming at the production of safe foodaccording to the regulation and international guidelines (Anonymous,2002; Codex Alimentarius Commission, 2003). Therefore, commonpathogenic microorganisms, relevant for the type of food productprocessed in the company must be taken into consideration. Typically,though not exclusively, Listeria monocytogenes and Salmonella spp. areanalysed for meat, fish, egg, vegetable, fruit and dairy processing(Anonymous, 2005; ICMSF, 2005). Campylobacter and Salmonella spp.should be included in the case of poultry processing (Habib et al., 2008;ICMSF, 2005). As indicators of (fecal) hygiene, E. coli and Enterobacter-iaceae can be monitored (Anonymous, 2005). The enumeration of totalcounts gives insight into the overall performance of the critical samplelocation (ICMSF, 2002; Mossel et al., 1995). As an indicator of goodpersonnel hygiene and correct handpractices, Staphyloccocus aureus canbe selected (Aarnisalo et al., 2006; Dijk et al., 2007).

2.2.3. Assessment of sampling frequencyThe first aim of MAS is to obtain a picture of the current

microbiological status of the core food safety control activities in an


FSMS and their actual efficacy. Consequently, it is not the objectiveto have a statistically underpinned sampling plan as described bye.g. Augustin and Minvielle (2008), Baird-Parker (1995), Green(1991) and Legan et al. (2001). It is as well not the aim to establishattribute plans for food lot acceptance, as described by ICMSF 2 and7 (Dahms, 2004; ICMSF, 1986, 2002; Legan et al., 2001). Therefore,we propose to perform a MAS over three periods (e.g. threeconsecutive months) in order to have insight in the distribution ofthe microbial load at each CSL. For the environmental CSLs (foodcontact surfaces and hands/gloves of food operators), also themicrobial contamination during the production day should befollowed by taking samples at the start of the production, at anintermediate time, and at the end of the production. This givesinsight into the daily fluctuations.

2.2.4. Selection of sampling method and method of analysisThe selection of sampling method and method of analysis must be

performed in a reliable and systematic way. It is recommended tofollow-up the appropriate procedures as described in the ISOstandards issued by the ISO TC 34 SC9 on Microbiology of food andanimal feeding stuffs or the EU Regulation (Anonymous, 2005) whereappropriate.

2.2.4.1. Raw materials, intermediate products and final food products.In the case of raw materials being meat carcasses (or parts) one isreferred to ISO 17604: 2003 which includes the use of destructive andnon-destructive techniques for the detection and enumeration ofmicroorganisms on the carcass surface of freshly slaughtered (red)meat animals and to EU legislation (Anonymous, 2005; ISO, 2003e).Some literature reports state excision as the most appropriate carcasssampling technique because the excision procedure achieves a higherrecovery of bacteria from meat carcasses as compared to swabbing(Bolton, 2003; Capita et al., 2004). This is because swab samplingremoves only a proportion (often 20% or more) of the total florapresent on the meat surface (Anonymous, 2001; Capita et al., 2004).Other studies, e.g. Byrne et al. (2005); Lindbald (2007), favorswabbing to be efficient over excision because, the excision techniquesamples a smaller area (typically 5 cm2) than swabbing (typically100 cm2) and excision may not be the most suitable carcass samplingtechnique for recovering enteric bacteria, which have a low incidenceand/or uneven distribution on meat carcasses. Moreover, meat fromhealthy animals is internal sterile, hence excision sampling will notproduce a representative result for the surface contamination of thefresh meat cuts.

For other food products, a representative sample is taken (10–30 g)and analysed according to ISO 6887-2: 2003 (ISO, 2003b).

2.2.4.2. Environmental sampling and sampling from hands and gloves offood operators. ISO 18593: 2004 specifies horizontal methods forsampling techniques using contact plates or swabs on surfaces in thefood industry environment (and food processing plants), with a viewof detecting or enumerating viable microorganisms (ISO, 2004a). Thesame methodology is used to sample the hands or gloves of foodoperators where a fixed surface (cm2) needs to be taken.

2.2.4.3. Analytical methods. Standardized methods (e.g. ISOmethods) are generally acknowledged as the reference methodand are recommended to be applied as the analytical methods forMAS. However, also alternative (rapid) methods such as thosebased on metabolic activity, immunoassays and nucleic acid basedtests, overviewed by Baylis (2005), can be applied, if they haveestablished performance characteristics or by preference arevalidated according to ISO 16140: 2003 (ISO, 2003d). Analyticalmethods are preferably executed in laboratories which operateunder quality assurance according to the principles of ISO 17025:2005 (ISO, 2005a).

2.2.5. Data processing and interpretation of the obtained results:microbial safety level profiles

The last part of the MAS protocol is the data processing andinterpretation of obtained results. The data processing can easily bedone with Microsoft Office Excel in order to make graphs or tables toillustrate visually the levels and distribution of microbial contamina-tion over the three different sampling periods. No averages, standarddeviations or statistics need to be applied in order to evaluate thevariability over the three sampling periods on single company level.Because, the microbial analyses for FSMS performance are aimed atobtaining insight in contamination profiles, which means insight intothe maximum level of microbial counts and the distribution inmicrobial contamination. This information gives insight into thedynamics of microbial contamination as a result of the designed andapplied control strategies in an FSMS system.

The obtained results are evaluated in two ways. First, the obtainedresults of each analysedmicrobiological parameter in a specific CSL areinterpreted. Therefore, the European Regulation on microbiologicalcriteria for foodstuffs should be applied if appropriate (Anonymous,2005). If no legal requirements are set microbiological guidelines canbe applied. But it is recognized that although microbiological guide-lines are widely used in the food industry, they have been publishedrarely. They are mainly internal criteria applied by food businessoperators (Stannard, 1997). These guidelines are aids to evaluatewhether the production process took place under controlled condi-tions. If the legal requirements or the guide values are exceeded for aspecific microorganism in a CSL, it indicates that the specific controlactivity in the FSMS, dedicated towards the defined CSLs according toTable 1, is not working properly. Consequently, a corrective action (orseveral) needs to be taken in order to change this non-conformingsituation and to improve the current FSMS performance.

Secondly, the concept of microbial safety level profiles isintroduced. For each microbiological parameter over the differentanalysed CSLs a level is concluded. A microbial safety level can beclassified from 1 to 3, where level 3 is a good result (legal criteria orguidelines are respected, no improvements are needed— current levelof FSMS is high enough to cover this hazard), level 2 is a mediumresult (legal criteria or guidelines are exceeded, improvements needto bemade on a single control activity of the FSMS) and level 1 is a lowresult (legal criteria or guidelines are exceeded, improvements needto be made on multiple control activities of the FSMS). The sum of thelevels is resulting in the microbial food safety level profile.

2.3. Case study — pork processing company

For illustration purposes, MAS was performed in a pork processingplant in Belgium. In this SME (approximately 50 peopleworking in theproduction area), an FSMS (certified for 4 years against the QAstandard BRC) has been implemented. The company specializes inprocessing different ready-to-eat pork meat products. To evaluate themicrobiological performance of the FSMS by MAS, we selected in thisstudy the production of cooked ham and cured bacon. Cooked ham iscured, cooked, cooled and packaged under vacuum conditions. Theraw cured bacon is dry cured, cured with brine, ripened in lowtemperature conditions and is packaged under vacuum (final wateractivity is approximately 0.96).

Along with MAS, we also conducted an FSMS diagnosis using theinstrument of Luning et al. (in press) via an in depth-interview in thecompany (explained in Section 2.1). The levels of core controlactivities were judged based on assessment grids. Level 1 indicates alow level of the specific control activity in the FSMS and typicallyrelated to the lack of scientific evidence, the use of companyexperience/history, variable, unknown, unpredictable, based oncommon materials/equipment, and not specific nor adapted for ownproduction system. Level 2 is an intermediate level of the specificcontrol activity in the FSMS that corresponds with best practice


knowledge/equipment, sometimes variable, not always predictable,and based on generic information for the product sector. Level 3 is ahigh level of the specific control activity in the FSMS typicallyassociated with proper scientific underpinning (accurate, complete),stable, predictable, and tailored and tested for the specific foodproduction situation (Luning et al., in press). Where specific controlactivities are not applicable or not relevant, level 0 is applied. Theinterviewer with responsibility of quality and the manager of thecompany assessed at which levels the various control activities in theirFSMSwere executed. These data are presented in spider web diagrams(Fig. 1).

2.3.1. Identification of critical sampling locations (CSL)According to the MAS protocol (see Section 2.2.1), 12 CSLs were

defined for this type of production processes (Table 2). The CSLs areselected vertically through the production process and areas from rawmaterials to the final products, including environmental samples. Thelink between the identified CSLs for this case study and the FSMSstructure is illustrated in Table 1.

2.3.2. Selection of the microbiological parametersThe selected foodsafetyparameters are, according to theMASprotocol

in Section 2.2.2, the pathogens Salmonella spp. and L. monocytogenes. Ashygiene indicators E. coli and Enterobacteriaceae are defined and asindicator of personal hygieneStaphylococcus aureus. As indicator of overallmicrobial quality, aerobic mesophilic plate counts are determined (utilityparameter) (Table 2).

2.3.3. Assessment of sampling frequencyMAS was performed during three visits in three consecutive

months, during each visit the 12 CSLs were sampled, as is motivated inthe MAS protocol in Section 2.2.3. The food stuffs (CSLs 1 until 6) wereeach time single sampled, while the environmental samples (CSLs 7until 12) were taken at three different times (beginning, middle andend of the production day) during each visit (Table 2). Overall, a totalof 156 samples were taken.

2.3.4. Selection of sampling method and method of analysis

2.3.4.1. Carcasses and fresh meat cuts (non-destructive sampling) (CSLs1 and 2). One site covering 100 cm2 for both raw pork meat partsand fresh pork meat cuts, was sampled using abrasive sponges(Envirosponge™, Biotrace International). Areas of sampling weredelimited by a sterile template. Sterile pre-moistened abrasivesponges were used to swab vertically, horizontally and diagonally onthe delineated area. After swabbing, the abrasive sponges wereindividually put in a sterile stomacher bag containing: 100ml peptonewater for the enumeration of total mesophilic counts, Enterobacter-iaceae, E. coli and L. monocytogenes; 100 ml buffered peptone waterfor the detection of Salmonella spp; and 100 ml demi-Fraser solutionfor the detection of L. monocytogenes. The samples were kept andtransported in a cool box maintained at ≤4 °C to the laboratory formicrobial analysis; and the samples were analysed within 6 h ofsampling.

2.3.4.2. Intermediate products and final meat products (CSLs 3 until 6).Three hundred gram samples of raw cured bacon and cooked hamwere cut by using a sterile knife. The sampleswere aseptically stored instomacher bags and transported in a cool box maintained at ≤4 °C tothe laboratory; then the sampleswere analysedwithin 6 h of sampling.

2.3.4.3. Cotton swabs (hands or gloves and food contact surfaces) (CSLs 7until 12). A sterile template was applied to delineate a 25 cm2 areafor sampling. Sterile pre-moistened cotton swabs (Cultiplast®) in 5mlpeptone water for enumeration of total mesophilic count, Enterobac-teriaceae, E. coli and L. monocytogenes; in 5 ml buffered peptone water

for the detection of Salmonella spp. and in 5 ml demi-Fraser solutionfor the detection of L. monocytogenes were used to swab the workingtables. For enumeration of Enterobacteriaceae, E. coli and S. aureus onhands or gloves of food operators, pre-moistened swabs in 5 mlpeptone water were used. A new sterile swab for each food contactsurface and analytical parameter was taken. Next, sampling swabswere aseptically inserted back into their respective tubes containing5 ml of the dilution media; the tubes were tightly closed, stored andtransported in cool box at ≤4 °C to the laboratory; and the sampleswere analysed within 6 h of sampling.

2.3.4.4. Analytical methods. In the lab, 30 g subsamples were taken foreach food stuff per analytical parameter or group of analyticalparameters. Then, the sampleswere stomached for 30 s in the stomacherwith 270 ml of peptone water for enumeration of aerobic mesophilicplate counts, Enterobacteriaceae, E. coli, and L. monocytogenes. Similarly,25 g subsamples for each food stuffwere taken andmixedwith 225mlofeither buffered peptone water for the detection of Salmonella spp. ordemi-Fraser solution for the detection of L. monocytogenes. For theabrasive sponges, the samples were also stomached for 30 s; while forthe cotton swabs the tubes were vortex mixed for 10 s.

The samples to be subjected to an enumeration procedure initiallywere serially diluted (1:9), then the resultant bacterial suspensionswere plated and incubated according to the appropriate ISO methods(ISO 1996, 1998, 2001, 2002, 2003a, 2003c, 2004b).

2.3.5. Data processing and interpretation of the obtained resultsThe data processing is performed applying Microsoft Office Excel

2003. In Table 2 an overview is given for each CSL, which legal criteriaor microbiological guidelines were applied for the interpretation ofthe results. If possible, the criteria from the European legislation areapplied (Anonymous, 2005). If legal criteria were not present for allCSLs, then microbial guidelines, recommended by the Laboratory ofFood Microbiology and Food Preservation (LFMFP-UGent), GhentUniversity (Debevere et al., 2006) were used.

3. Results

3.1. Results of FSMS diagnosis

The results of the diagnostic instrument of the assessment of corecontrol activities, as addressed in the companies' FSMS and explainedin Sections 2.1 and 2.3, are demonstrated in spider web diagrams.These show the profiles of preventive measures design, interventionprocess design, monitoring system design, and the actual operation ofthe core control activities (Fig. 1A, B, C and D). These diagrams clearlyillustrate that a more coloured spiderweb is associated with controlactivities that are elaborated at a higher level (level 3). The overalllevel of the preventive measure design (Fig. 1A) is at level 3, only theperformance of the sanitation program scored level 2. The cleaningand disinfection agents are based on knowledge from suppliers, butare not adapted and tested for the specific food productioncircumstances. Fig. 1B illustrates the intervention process design forcooked ham and raw cured bacon separately because raw cured baconhas no intervention equipment, whereas cooked ham does (i.e.cooking and cooling). The used intervention steps are on level 3 (sowell tested for the specific production circumstances, and processcapability and effectiveness of intervention method are known),which results in the reduction of the microbiological load. The resultsof the monitoring system design are shown in Fig. 1C, where mainlylevel 3 is obtained (i.e. scientific underpinned, systematic assessment,sophisticated equipment for monitoring). However, the samplingdesign and CCP analysis, for raw cured bacon, is on an intermediatelevel (level 2) because both were designed based on, respectively,empirical sampling plan and hygiene codes for the sector incombination with expert support (which is typically level 2). Fig. 1D

Fig.1. Results of the diagnosis of core control activities in an FSMS of a pork processing SME, according to Luning et al. (in press): preventivemeasures design (A), intervention process design (B), monitoring system design (C), and operation offood safety control system (FSCS) (D). (level 3 sophisticated situation, level 2 intermediated situation, level 1 low sophisticated situation, level 0 not appropriate).

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shows the assessment of the actual operation of core control activities,showing level 2 for compliance to procedures because the majority ofoperators are familiar with existence of procedures (but not alwaysexact content); tasks are executed based on habits. Operators arecontrolled on compliance to procedures on a regular basis. Fig. 1D alsoindicates a level 2 for the appropriateness of procedures, meaning thatthe procedures are available at location (often paper-based) andunderstandable for most users but are kept up-to-date on ad-hocbasis. The activity ‘actual analytical equipment performance’ scored 0because no in-company laboratory activities are present. Overall, thecore control activities as addressed in their FSMS are at level 3, withsome at level 2 (which corresponds with aspects such as availablepractice/equipment, experts knowledge and guidelines), indicating awell elaborated FSMS, according to Luning et al. (in press).

3.2. Results for pathogens Salmonella spp. and L. monocytogenes

For each of the pathogens, 45 samples were analysed includingboth food stuffs and environmental samples of food contact surfacesas well as hands/gloves of food operators (Table 2). For none of thesamples, neither Salmonella spp. nor L. monocytogenes were detectedin 25 g product or 25 cm2 of food contact surface/hand or 100 cm2

carcass area.

3.3. Results for CSLs 1 until 6 (food stuffs)

Aerobicmesophilic plate counts (APC) at the different CSLs (1 until6) are shown in Fig. 2. APC increased over CSLs 1, 2 and 3 during visits1 and 2 but remained at the same level during visit 3. Over all visits,the Enterobacteriaceae and E. coli count were very low or below thedetection limit on the CSLs 1 until 3: on the rawmaterials (CSL 1) bothEnterobacteriaceae and E. coli were found below the detection limit(b1 CFU/cm2). Enterobacteriaceae were quantified on the fresh meatcuts (CSL 2) but in low numbers (highest count of 30 CFU/100 cm2).Also on the intermediate cured meat (CSL 3) Enterobacteriaceae andE. coli were found below the detection limit (b10 CFU/g).

In two visits, APCwere below the detection limit (b10 CFU/g) at CSL4 (the chilled cooked hamwhichwas sampled just after cooking and fastcooling) (Fig. 2). Enterobacteriaceae andE. coliwerebelow thedetectionlimit (b10 CFU/g) in CSL 4. After packaging the cooked ham (CSL 5), anaverage increase of 1 log occurred (compared to CSL 4) in APC. However,for cured bacon, an average decrease of 1 log occurred (APC comparingCSL 6with CSL 3) (Fig. 2). But Enterobacteriaceae and E. coliwere belowthe detection limit (b10 CFU/g) on the final products.

3.4. Results for CSLs 7 until 9 (food contact surfaces)

The results obtained from the environmental swabbing over thethree visits and three sampling times are shown in Fig. 3A (aerobic

Fig. 2. Distribution of aerobic mesophilic plate counts for CSLs 1–6: first visit sampling(x); second visit sampling (■); third visit sampling (◯) CSLs 1 and 2 (log CFU/100 cm2—

detection limit: b0 log CFU/cm2); CSLs 3–6 (log CFU/g— detection limit: b1 log CFU/g).

mesophilic plate counts) and B (Enterobacteriaceae and E. coli) for theCSLs 7, 8 and 9. The highest APC (1,10×105 CFU/25 cm2) was detectedat CSL 7; the working tables at the deboning area; the first part of theprocessing line, but CSL 8 obtained similar results ranging from 103–105 CFU/25 cm2. The APC on CSL 9 (working tables in the packagingarea) was lower (ranging from 102–104 CFU/25 cm2) as compared toCSLs 7 and 8 (production area). Variation in numbers of APC is noticedbetween the visits and times of sampling during production but nosystematic build up of the total counts can be detected. Enterobacter-iaceae were often (17/27 samples) recovered from the food contactsurfaces with numbers ranging from 10 to 470 CFU/25 cm2, CSL 8being the most contaminated, CSL 9 to a lesser extent. E. coli was onlyrarely detected (4/27 samples) with a maximum of 10 CFU/25 cm2

(Fig. 3B).

3.5. Results for CSLs 10 until 12 (hands/gloves of food operator)

The results obtained from swabbing the hands or gloves of foodoperators over the three visits and three sampling times duringproduction are shown in Fig. 4A (S. aureus) and B (Enterobacteriaceaeand E. coli) for the CSLs 10, 11 and 12.

E. coli was detected only twice, with the highest number (45 CFU/25 cm2) counted on the hands of food operators working at thepackaging area (CSL 12). The hands/gloves at CSL 11were shown to bethe most vulnerable CSL for the occurrence of Enterobacteriaceae. CSL11 was the hands of a person preparing the cured meat. Numbersranged from 10–100 CFU/25 cm2. As is shown in Fig. 4A, S. aureuswasfound on the hands from the food operators, not wearing gloves,during the three visits and incidentally over the whole production/packaging area. The counts ranged from 10–1000 CFU/25 cm2

(Fig. 4A). The highest contamination of 1000 CFU/25 cm2 wasquantified on the hands of a food operator packaging grilled cookedham on CSL 12.

3.6. Microbial safety level profile

Based on the results obtained of the 156 samples taken over the 12CSLs in the 3 month period, a microbial safety level profile can bederived for this case study for each microorganism over the differentCSL's to evaluate the current microbiological status of the FSMS(Fig. 5). For the pathogens Salmonella spp. and L. monocytogenes, level3 can be attributed because no pathogens are detected. These resultsare acceptable according with the legal requirements and/or guide-lines (Table 2). Also for E. coli a level of 3 is obtained as this fecalhygiene indicator is only found sporadic, in low amounts and not onfood stuffs. The obtained results are in accordance with the legalrequirements and/or guidelines (Table 2). S. aureus was detected onthe hands of food operators, both in the production and the packagingareas (Fig. 4A). These results are not in line with the guidelines(Table 2). This indicates that a specific improvement regardingpersonal (hand) hygiene in the current FSMS is needed to solve thisproblem and therefore level 2 is attributed (one specific controlactivity in the FSMS needs to be improved). High counts are found onthe food contact surfaces for Enterobacteriaceae and APC. On the foodstuffs itself, these parameters were in accordance with the legalcriteria/guidelines. Therefore, a level 2 is attributed resulting in anecessary improvement of sanitation processes in the current FSMS. Atotal microbiological safety level profile of 15 is obtained in the casestudy (Fig. 5).

4. Discussion

The two outputs of MAS (i.e. evaluation of each microbiologicalparameter in a specific CSL and themicrobial safety level profiles) giveinsight in the actual microbiological status/performance of thecurrent FSMS present in a company. First, the MAS results give

Fig. 3. A. Mesophilic aerobic plate counts (log CFU/25 cm2 — detection limit b1 log CFU/25 cm2) on food contact surfaces CSLs 7–8–9: time 1 beginning of the production day–time 2 middle of the production day–time 3 end of the productionday for visit 1 –visit 2 –visit 3□. B. Enterobacteriaceae (log CFU/25 cm2 — detection limit b1 log CFU/25 cm2) on food contact surfaces CSLs 7–8–9: time 1 beginning of the production day–time 2middle of the production day–time 3 endof the production day for visit 1 –visit 2 –visit 3 □, ⁎ indicates E. coli counted on the detection limit (b1 log CFU/25 cm2).

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Fig. 4. A. S. aureus (log CFU/25 cm2— detection limit b1 log CFU/25 cm2) on hands/gloves of food operators CSLs 10–11–12: time 1 beginning of the production day–time 2middle of the production day–time 3 end of the production day for visit1 –visit 2 –visit 3□. B. Enterobacteriaceae (log CFU/25 cm2 — detection limit b1 log CFU/25 cm2) on hands/gloves of food operators CSLs 10–11–12: time 1 beginning of the production day–time 2middle of the production day–time 3 endof the production day for visit 1 –visit 2 –visit 3 □, ⁎ indicates E. coli counted on the detection limit (b1 log CFU/25 cm2).

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Fig. 5. Microbial safety level profile for the pork processing company: profile isconstructed by levels: total mesophilic counts, S. aureus, Enterobacteriaceae,E. coli, L. monocytogenes, Salmonella. □ indicates the remaining microbial safetylevel according to the maximum of 18, where improvement in the FSMS can be made.


information concerning the performance of a specific control activityin an FSMS (in the case study demonstrated by results in Sections 3.2until 3.5 linked to control activities of an FSMS shown in Table 1).Secondly, the microbial safety profiles provide additional informationconcerning the nature of the microbiological problem (in the casestudy illustrated by Fig. 5).

In this case study, pathogenic microorganisms were not detectedin any of the CSLs for thewhole period of the study. Therefore, it can besuggested that the current FSMS in the company, with respect topathogens, is effective. This output from MAS can be combined withthe overall FSMS diagnosis (Fig. 1): although the FSMS diagnosisshows a level 2 (intermediate level) on some control activities, theMAS results demonstrate that they appear to be effective at thismoment. Thus, the current FSMS does not require improvementsregarding the control of the pathogens.

The incoming rawmaterials had low initial levels of contaminationwith respect to the APC and Enterobacteriaceae compared to the legalrequirements (Table 2). Also the variation of the APC was small,ranging from 60–380 CFU/100 cm2 which indicates an efficientcontrol of raw material. It is reported that the higher number of APCusually relates to poor quality and a reduced shelf life of meat andmeat products (Eglezos et al., 2008; Eisel et al., 1997; Stopforth et al.,2006). These MAS results suggest a good relationship with thesuppliers and robust procedures for the selection of suppliers in thecompanies' FSMS. This was confirmed in the diagnosis of the FSMSwith the evaluation of the ‘product specific preventive measures’ onlevel 3 (Fig. 1A).

A limited (and variable) increase in the microbial contamination ofthe fresh meat cuts was noticed in the first stage of the productionprocess; deboning and trimming. The results correspond to the onesobtained by Augustin and Minvielle (2008) who did a study onmicrobiological contamination of pork meat cuts of 9 French cuttingplants from 1999 to 2003; finding that Enterobacteriaceae mean logcounts ranged from 0.6 to 2.2 log CFU/cm2. However, the surfacecontamination on the meat cuts stayed below the legal criteria/guidelines (Table 2). These results are suggesting that no improve-ments need to be made on ‘preventive measures’ in the controlactivities of the FSMS (Table 1) in the production area. If we comparethe intermediate product to the final product raw cured bacon, areduction in aerobic mesophilic counts is seen due to the shortripening process at low temperatures before packaging as well as areduction inwater activity (final water activity is approximately 0.96).The raw cured bacon did not undergo an intervention strategy (drycuring followed by brine curing at low temperatures) to eliminate themicroorganisms but to reduce them to an adequate level. Therefore,this product should be regarded as a high risk product. These findingsare in line with the intermediate level of the diagnosis of the ‘CCPanalysis of raw cured bacon’ (level 2 in Fig. 1C). Consequently, thecompanies' CCP analysis of raw cured bacon needs to be furtherelaborated.

A very low contamination was detected on the cooked ham afterthe fast cooling process (CSL 4). This is indicating that their coolingcapacity and process is adequate. This result was further confirmed bythe FSMS diagnosis of the ‘adequacy of the cooling facilities’ and the‘intervention process design of cooked meat products’ at level 3(Fig. 1A and B).

In the production area where raw meat parts and cuts areprocessed, high APC and Enterobacteriaceae counts were found onfood contact surfaces. However, it did not led to an increase inmicrobiological contamination of the fresh cut cuts. But when thecooked ham was further processed in the packaging area, recontami-nation occurred (Fig. 2). It is clear that a recontamination from theproduct originates from the environment in the packaging area.Different studies have reported working tables, equipment and handsof food operators as the potential sources of cross contamination infood processing industry (Gill et al., 2001; McEvoy et al., 2004; Tsaloet al., 2007). The FSMS diagnosis revealed also that the ‘specificity oftheir sanitation program’ is at level 2 (Fig.1A) and can be improved. Byapplying a more sophisticated sanitation program (i.e. typified bycleaning agents adapted for the specific product and processsituations and involving a complete full-step cleaning procedure),the microbiological load of food contact surfaces should be reduced.

The actual microbial performance of hand hygiene, resulting in thepresence of S. aureus in the hands in both the production andpackaging area, demonstrates that the hand hygienewas insufficientlyrespected. Although the ‘extent of personal hygiene requirements’wasassessed at level 3 (i.e. high requirements, for all food operators, onclothing, personal care and health, with tailored facilities to supportpersonal hygiene, and specific training and hygiene instructions)(Fig. 1A), the MAS results showed unsatisfactory performance, whichmight be due to ‘inadequate compliance to procedures’, indicated bythe diagnostic instrument (level 2 in Fig. 1D). Nel et al. (2004)emphasised that although basic personal and hygiene practices areavailable they need to be optimised and regularly checked in practiceto be effective. Although the design is good, inadequate compliance toprocedures and instructions and/or their misinterpretation maycontribute to safety problems (Azanza and Zamora-Luna, 2005;Gilling et al., 2001). Improvement can be obtained by the requirementthat all food operators are wearing gloves and training them in goodpersonnel hygiene and practices (Dijk et al., 2007).

A totalmicrobiological safety level profile of 15 is obtained in the casestudy, while themaximum level is 18 (i.e. 6 microbiological parameterswith amicrobial safety level of 3) (Fig. 5). Consequently, this companies'FSMS still has opportunities for improvement, specifically on themicrobial safety levels of S. aureus, Enterobacteriaceae and total counts.

In conclusion, the MAS gives an indication of the current microbialperformance of the different control activities in an FSMS, while theFSMS diagnose indicates the level on which control activities areconducted. The combination of these two tools can help foodprocessing industries to analyse their current FSMS in a systematicway and can lead to define possibilities for improvements of aneffective FSMS.

Further, MAS can be applied as a tool for the (yearly) verification ofan FSMS on company level, as demanded by Codex Alimentarius (CAC,2003; Hong et al., 2008; Jacxsens et al., 2009; Scott, 2003; Wallaceet al., 2005). The presented MAS protocol can easily be transferredtowards other sectors as meat product processes. The microbial safetyprofiles can also be used to compare the current microbiologicalperformance of different companies with the same type of productionprocesses and food products. As such, microbiological problems in asector can be identified, independent from company level.

Acknowledgments

The research performed has been part of the project FOOD-CT-2005-007081 (PathogenCombat) supported by the European


Commission through the Sixth Framework Programme for Researchand Development. Also our special appreciation goes to the personnelfrom the Accredited Lab, Laboratory of Food Preservation and FoodMicrobiology, Faculty of Bioscience Engineering, Ghent University;who assisted in microbiological analysis. We thank the pork proces-sing company for the possibility of using their results for the casestudy.

References

Aarnisalo, K., Tallavaara, K., Wirtanen, G., Maijala, R., Raaska, L., 2006. The hygienicworking practices of maintenance personnel and equipment hygiene in the Finnishfood industry. Food Control 17, 1001–1101.

Anonymous, 2001. Commission Decision 2001/471/EC of 8 June 2001 laying down rulesfor the regular checks on the general hygiene carried out by the operators inestablishments according to Directive 64/433/EEC on health conditions for theproduction and marketing of fresh meat and Directive 71/118/EEC on healthproblems affecting the production and placing on the market of fresh poultry meat.Official Journal of the European Communities.

Anonymous, 2002. Regulation (EC) No 178/2002 of the European Parliament and of theCouncil of 28 January 2002 laying down the general principles and requirements offood law, establishing the European Food Safety Authority and laying downprocedures in matters of food safety. Official Journal of the European Communities(01/02/2002).

Anonymous, 2005. Commission Regulation (EC) No 2073/2005 of 15 November 2005on microbiological criteria for foodstuffs. Official Journal of the EuropeanCommunities 7/12/2007 (inclusive EU Regulation 1441/2007).

Augustin, J., Minvielle, B., 2008. Design of control charts to monitor the microbiologicalcontamination of pork meat cuts. Food Control 19, 82–89.

Azanza, M.P.V., Zamora-Luna, M.B.V., 2005. Barriers of HACCP team members toguideline adherence. Food Control 16, 15–22.

Bagge-Ravn, D., Ng, Y., Hjlem, M., Christiansen, J.N., Johansen, C., Gram, L., 2003. Themicrobial ecology of processing equipment in different fish industries—analysis ofthe microflora during processing and following cleaning and disinfection.International Journal of food Microbiology 87, 239–250.

Baird-Parker, A.C., 1995. Development of industrial procedures to ensure themicrobiological safety of food. Food Control 6, 29–36.

Baylis, C., 2005. Rapid microbiological test methods. Food & Beverage International —Special Safety Supplement, april 2005, pp. 1–8.

Bolton, D.J., 2003. The EC decision of the 8th June 2001 (EC/471/2001): excision versusswabbing. Food Control 14, 207–209.

British Retail Consortium (BRC), 2008. Global standard for food safety. Ed. TSO, PO Box29, Norwich NR3 1GN, UK, p. 82.

Brown, M.H., Gill, C.O., Hollingsworth, J., Nickelson, R., Seward, S., Sheridan, J.J.,Stevenson, T., Sumner, J.L., Theno, D.M., Usborne, W.R., Zink, D., 2000. The role ofmicrobiological testing in systems for assuring the safety of beef. InternationalJournal of Food Microbiology 62, 7–16.

Byrne, B., Dunne, G., Lyng, J., Bolton, D.J., 2005. Microbiological carcass samplingmethods to achieve compliance with 2001/471/EC and new regulations. Researchin Microbiology 156, 104–106.

Capita, R., Prieto, M., Alonso-Calleja, C., 2004. Review — sampling methods formicrobiological analysis of red meat and poultry carcasses. Journal of FoodProtection 67, 1303–1308.

CIES, 2007.Global FoodSafety InitiativeGuidanceDocument, 5thedition. [email protected], 41 pp. Accessed 8th of July 2008.

Codex Alimentarius Commission (CAC), 2003. Recommended International code ofpractice general principles of food hygiene. CAC/RCP1-1969.

Cools, I., Uyttendaele, M., Cerpentier, J., D’Haese, E., Nelis, J.H., Debevere, J., 2005.Persistence of Campylobacter jejuni on surfaces in a processing environment and oncutting boards. Letters in Applied Microbiology 40, 418–423.

Cormier, R.J., Mallet, M., Chiasson, S., Magnússon, H., Valdimarsson, G., 2007. Effectivenessand performance of HACCP-based programs. Food Control 18, 665–671.

Dahms, S., 2004. Microbiological sampling plans — statistical aspects. Mitteilungen ausLebensmitteluntersuchung und Hygiene 95, 32–44 (http://www.icmsf.iit.edu/main/articles_papers.html Accessed 8th of July 2008).

Debevere, J., Uyttendaele, M., Devlieghere, F., Jacxsens, L., 2006. Microbiological guidevalues and legal microbiological criteria. Laboratory of Food Microbiology and FoodPreservation (LFMFP-UGent), Ghent University, Belgium, p. 66.

Dijk, R., van den Berg, D., Beumer, R.R., de Boer, E., Dijkstra, A., Kalkmand, P., Stegeman,H., Uyttendaele, M., Veenendaal, H., 2007. Microbiologie van Voedingsmiddelen:methoden, principes en criteria (vierde druk). Uitgeverij Keesing Noordervliet,Houten, Nederland — ISBN 978-90-72072-77-1, pp. 730.

Doménech, E., Escriche, I., Martorell, S., 2008. Assessing the effectiveness of criticalcontrol points to guarantee food safety. Food Control 19, 557–565.

European Hygienic Engineering Design Group (EHEDG), 2007. Integration of hygienicand aseptic systems. Trends in Food Science and Technology 18, 48–58.

Eglezos, S., Dykes, G.A., Huang, B., Fegan, N., Stuttard, E., 2008. Bacteriological profile ofraw, frozen chicken nuggets. Journal of Food Protection 71 (3), 613–615.

Eisel, W.G., Linton, R.H., Muriana, P.M., 1997. A survey of microbial levels for incomingraw beef, environmental sources, and ground beef in a red meat processing plant.Food Microbiology 14, 273–282.

Evans, J.A., Russell, S.L., James, C., Corry, J.E.L., 2004. Microbial contamination of foodrefrigeration equipment. Journal of Food Engineering 62, 225–232.

FAO/WHO, 2007. FAO/WHO guidance to governments on the application of HACCP insmall and/or less-developed food businesses. FAO Food and Nutrition Paper. ISSN0254-4725.

FAVV, 2006. Proceshygiënecriteria met betrekking tot het aëroob kiemgetal, Entero-bacteriaceae en Salmonella (dossier Sci Com 2006/11) 8pp. http://www.favv.be/home/com-sci/avis06_nl.asp Accessed 10th of July 2008.

Fuster-Valls, N., Hernández-Herrero,M., Marín-de-Mateo, M., Rodríguez-Jerez, J.J., 2008.Effect of different environmental conditions on the bacteria survival on stainlesssteel surfaces. Food Control 19, 308–314.

Gill, C.O., Bryant, J., Badoni, M., 2001. Effects of hot water pasteurizing treatments on themicrobiological condition of manufacturing beef used for hamburger pattymanufacture. International Journal of Food Microbiology 63, 243–256.

Gilling, S.J., Taylor, E.A., Kane, K., Taylor, J.Z., 2001. Successful hazards analysis criticalcontrol point implementation in the United Kingdom: understanding the barriersthrough the use of a behavioral adherence model. Journal of Food Protection 64 (5),710–715.

González-Miret, M.L., Coello, M.T., Alonso, S., Heredia, F.J., 2001. Validation ofparameters in HACCP verification using univariate and multivariate statistics.Application to the final phases of poultry meat production. Food Control 12,261–268.

Green, S.B., 1991. How many subjects does it take to do a regression analysis?Multivariate Behavioral Research 26, 499–510.

Habib, I., Sampers, I., Uyttendaele, M., Berkvens, D., De Zutter, L., 2008. Baseline datafrom a Belgium-wide survey of Campylobacter species contamination in chickenmeat preparations and considerations for a reliable monitoring program. Appliedand Environmental Microbiology 74, 5483–5489.

Hong, C.H., Todd, E.C.D., Bahk, G.J., 2008. Aerobic plate count as a measure of hazardanalysis critical control point effectiveness in a pork processing plant. Journal ofFood Protection 71, 1248–1252.

ICMSF (International Commission on Microbiological Specifications for Foods), 1986.Microorganisms in Foods 2: Sampling for Microbiological Analysis: Principles andSpecific Applications. University of Toronto Press, p. 293. ISBN 080205638.

ICMSF, 2002. Microorganisms in Foods 7: Microbiological Testing in Food Safety Manage-ment. Kluwer Academic/Plenum Publishers, New York, p. 362. ISBN 030642627.

ICMSF, 2005. Microorganisms in Foods 6, second edition. Kluwer Academic/PlenumPublishers, New York, p. 763. ISBN 030648675.

International Food Standard (IFS), 2007. Standard for auditing, retailer and wholesalerbranded food products. Ed. HDE Trade Services, Berlin, Germany, pp. 117.

ISO, 1996. Microbiology of Food and Animal Feeding Stuffs—Horizontal Method for theDetection and Enumeration of Listeria monocytogenes—Part 1: Detection Method.(ISO 11290-1:1996/Amd 1: 2004).

ISO, 1998. Microbiology of Food and Animal Feeding Stuffs—Horizontal Method for theDetection and Enumeration of Listeria monocytogenes—Part 2: EnumerationMethod. (ISO 11290-2:1998/Amd 1: 2004).

ISO, 2001. Microbiology of food and animal feeding stuffs—horizontal method for theenumeration of β-glucoronidase positive Escherichia coli. Part 2: Colony-countTechnique at 44 °C Using 5-bromo-4-chloro-3-indolyl β-D-glucuronide (ISO 16649-2:2001).

ISO, 2002. Microbiology of Food and Animal Feeding Stuffs—Horizontal Method for theDetection of Salmonella spp (ISO 6579:2002).

ISO, 2003a. Microbiology of Food and Animal Feeding Stuffs—Horizontal Method forthe Enumeration of Microorganisms—Colony Count Technique at 30 °C (ISO4833:2003).

ISO, 2003b. Microbiology of Food and Animal Feeding Stuffs —Preparation of TestSamples, Initial Suspension and Decimal Dilutions for Microbiological Examination(ISO 6887-2:2003).

ISO, 2003c. Microbiology of food and animal feeding stuffs—horizontal method for theenumeration of coagulase positive Staphylococcus aureus and other species—Part 1:technique using Baird–Parker agar medium. Amendment 1: Inclusion of precisiondata (ISO 6888-1: 1999/Amd.1:2003).

ISO, 2003d. Microbiology of Food and Animal Feeding Stuffs — Protocol for theValidation of Alternative Methods (ISO 16140:2003).

ISO, 2003e. Microbiology of Food and Animal Feeding Stuffs —Carcass Sampling forMicrobiological Analysis (ISO 17604:2003).

ISO, 2004a. Microbiology of Food and Animal Feeding Stuffs — Horizontal Methods forSampling Techniques from Surfaces Using Contact Plates and Swabs (ISO18593:2004).

ISO, 2004b. Microbiology of Food and Animal Feeding Stuffs—Horizontal Method for theDetection and Enumeration of Enterobacteriaceae — Part 2: Colony-count Method(ISO 21528-2:2004).

ISO, 2005a. General Requirements for the Competence of Testing and CalibrationLaboratories (ISO 17025:2005).

ISO, 2005b. Food Safety Management Systems — Requirements for Any Organization inthe Food Chain (ISO 22000:2005).

Jacxsens, L., Moens, E., Van Hoecke, V., 2006. Autocontrole in België. Voedingsmidde-lentechnologie 1/2 (January 2007).

Jacxsens, L., Moens, E., Van Hoecke, H., Devlieghere, F., Uyttendaele, M., Debevere, J.,2007. Traceerbaarheid in de agrovoedingsketen. Het Ingenierusblad (april 2007).

Jacxsens, L., Devlieghere, F., Uyttendaele, M., 2009. Quality management systems in thefood industry. Book in the Framework of Erasmus. 978-90-5989-275-0.

Jessen, B., Lammert, L., 2003. Biofilm and disinfection in meat processing plants.International Biodeterioration & Biodegradation 51, 265–269.

Kvenberg, J.E., Schwalm, D.J., 2000. Use of microbial data for HACCP— food and drugadministrative perspective. Journal of Food Protection 63, 810–814.

Leaper, S., Richardson, P., 1999. Validation of thermal process control for the assuranceof food safety. Food Control 10, 281–283.



http://www.icmsf.iit.edu/main/articles_papers.html

http://www.icmsf.iit.edu/main/articles_papers.html

http://www.favv.be/home/com-sci/avis06_nl.asp

http://www.favv.be/home/com-sci/avis06_nl.asp


Legan, J.D., Vandeven, M., Dahms, S., Cole, M., 2001. Determining the concentration ofmicroorganisms controlled by attributes sampling plans. Food Control 12, 137–147.

Lindbald, M., 2007. Microbiological sampling of swine carcasses: a comparison of dataobtained by swabbing with medical gauze and data collected routinely by excisionat Swedish abattoirs. International Journal of Food Microbiology 118, 180–185.

Luning, P.A., Marcelis, W.J., 2006. A techno-managerial approach to food qualitymanagement. Trends in Food Science and Technology 17, 378–385.

Luning, P.A., Marcelis, W.J., 2007. A food quality management functions model from atechno-managerial perspective. Trends in Food Science and Technology 18,159–166.

Luning, P.A., Marcelis, W.J., in press. Food Quality Management: techno-managerialprinciples and practices. Wageningen: Wageningen Academic Publishers.

Luning, P.A., Devlieghere, F., Verhé, R., 2006. Safety in Agri-Food Chains. WageningenAcademic Publishers, Wageningen. ISBN: 9076998779, p. 681.

Luning, P.A., Bango, L., Kussaga, J., Rovira, J., Marcelis, W.J., 2008. Comprehensiveanalysis and differentiated assessment of food safety control systems: a diagnosticinstrument. Trends in Food Science and Technology 1, 1–13.

Luning, P.A., Marcelis, W.J., Van der Spiegel, M., Rovira, J., Uyttendaele, M., Jacxens, L., inpress. Assurance activities in food safety management systems: how to diagnosethem? Trends in Food Science and Technology.

Martins, E.A., Germano, P.M.L., 2008. Microbiological indicators for the assessment ofperformance in the hazard analysis and critical control points (HACCP) system inmeat lasagne production. Food Control 19, 764–771.

Manning, L., Baines, R., Chadd, S., 2006. Food safety management in broiler meatproduction. British Food Journal 108, 605–621.

McEvoy, J.M., Sheridan, J.J., Blair, I.S., McDowell, D.A., 2004. Microbiological contamina-tion of beef carcasses in relation to hygiene assessment based on criteria used in EUDecision 2001/47/EC. International Journal of Food Microbiology 92, 217–225.

Mossel, D.A.A., Corry, J.E.L., Struijk, C.B., Bard, R.M., 1995. Essentials of the Microbiologyof Food. A Textbook for Advanced Studies. John Wiley & Sons, Chichester, UK. ISBN:0 471 930369, p. 699.

Nel, S., Lues, J.F.R., Buys, E.M., Venter, P., 2004. The personal and general hygienepractices in the deboning room of a high throughput red meat abattoir. FoodControl 15, 571–578.

Nørrung, B., Buncic, S., 2008. Microbial safety in the European union. Meat Science 78,14–24.

Orriss, G.D., Whitehead, A.J., 2000. Hazard analysis and critical control point (HACCP) asa part of an overall quality assurance system in international food trade. FoodControl 11, 345–351.

Schlundt, J., 2002. New directions in foodborne disease prevention. InternationalJournal of Food Microbiology 78, 17–25.

Scott, V., 2003. How does industry validate elements of HACCP plans? Food Control 16,497–503.

Sofos, J.N., 2008. Challenges to meat safety in the 21st century. Meat science 78, 3–13.Stannard, C., 1997. Development and use of microbiological criteria for foods. Food

Science and Technology Today 11, 137–449.Stopforth, J.D., Lopes, M., Shultz, J.E., Miksch, R.R., Samadpour, M., 2006. Microbiological

status of fresh beef cuts. Journal of Food Protection 69, 1456–1459.Stringer, M.F., Hall, M.N., 2007. A generic model of the integrated food supply chain to

aid the investigation of food safety breakdowns. Food Control 18, 755–765.Swanson, K.M.J., Anderson, J.E., 2000. Industry perspectives on the use of microbial data

for hazard analysis and critical control point validation and verification. Journal ofFood Protection 63, 815–818.

Todd, E.C.D., Greig, J.D., Bartleson, C.A., Michaels, B.S., 2007. Outbreaks where foodworkers have been implicated in the spread of foodborne disease. Part 3. Factorscontributing to outbreaks and description of outbreak categories. Journal of FoodProtection 70 (9), 2199–2217.

Tsalo, E., Drosinos, E.H., Zoiopoulos, P., 2007. Impact of poultry slaughter housemodernisation and updating of food safety management systems on themicrobiological quality and safety of products. Food Control 19, 423–431.

Van der Spiegel, M., Luning, P.A., Ziggers, G.W., Jongen, W.M.F., 2005. Development ofthe instrument IMAQE—food to measure effectiveness of quality management.International Journal of Quality & Reliability Management 22 (3), 234–255.

Wallace, C.A., Powell, S.C., Holyoak, L., 2005. Development of methods for standardizedHACCP assessment. British Food Journal 107, 723–742.

Documents

A Microbial Assessment Scheme to measure microbial performance of Food Safety Management Systems