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

Contents lists available at ScienceDirect

International Journal of Food Microbiology

j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / i j f o o d m i c r o

A Microbial Assessment Scheme to measure microbial performance of Food Safety

Management 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, Belgium
b
Product Design and Quality Management Group, Department of Agrotechnology and Food Sciences, Wageningen University, P.O. Box 8129, NL-6700 EV Wageningen, the Netherlands

a r t i c l e i n f o a b s t r a c t

Keywords: A Food Safety Management System (FSMS) implemented in a food processing industry is based on Good
Food Safety Management System Hygienic Practices (GHP), Hazard Analysis Critical Control Point (HACCP) principles and should address both
Microbiological food safety food safety control and assurance activities in order to guarantee food safety. One of the most emerging
Performance tool challenges is to assess the performance of a present FSMS. The objective of this work is to explain the
development of a Microbial Assessment Scheme (MAS) as a tool for a systematic analysis of microbial counts
in order to assess the current microbial performance of an implemented FSMS. It is assumed that low
numbers of microorganisms and small variations in microbial counts indicate an effective FSMS. The MAS is a
procedure that defines the identification of critical sampling locations, the selection of microbiological
parameters, 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 profiles
can be derived, indicating which microorganisms and to what extent they contribute to food safety for a
specific food processing company. The MAS concept is illustrated with a case study in the pork processing
industry, 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 (NØrrung
and Buncic, 2008; Sofos, 2008). In response to the increasing number
of foodborne illnesses, governments all over the world are intensifying
their efforts to improve food safety (Anonymous, 2002; Codex
Alimentarius Commission, 2003; Orriss and Whitehead, 2000;
Schlundt, 2002; Wallace et al., 2005). Regulations forced food business
operators in the agri-food chain to design and implement a Food
Safety Management System (FSMS) in order to control the outbreaks
of foodborne illnesses (Baird-Parker, 1995; Jacxsens et al., 2009;
Luning et al., 2006; Schlundt, 2002; Tsalo et al., 2007). An FSMS can be
defined as a company specific system of control and assurance
activities in order to realise and guarantee food safety. Control
activities aim at keeping product and process conditions within
acceptable limits in order to realise food safety, while assurance
activities 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
⁎ Corresponding author. Mailing address: Department of Food Safety and Food
Quality, Laboratory of Food Microbiology and Food Preservation, Coupure links 653,
9000 Ghent, Belgium. Tel.: +32 9 264 60 85; fax: +32 9 225 55 10.
E-mail address: liesbeth.jacxsens@ugent.be (L. Jacxsens).
22000 (ISO, 2005b), International Food Standard (IFS, 2007), and
Global Standard for food safety (BRC, 2008), which are specifically
developed for food (processing) industries and against which
certification is possible (often demanded by retailers). A big challenge
for food business operators is to translate and to implement these
requirements in a company specific FSMS, in order to assure food
safety and in many cases also food quality. A company specific FSMS
should be a translation of Good Hygienic Practices (GHP), Hazard
Analysis 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), and
attention is shifting from implementing QA standards to the better
understanding of the performance of an FSMS (Doménech et al., 2008;
Luning et al., 2008; Stringer and Hall, 2007). As a consequence, various
audit tools have been developed to determine the performance towards
QA standards (e.g. CIES, 2007; Cormier et al., 2007; Doménech et al.,
2008; Wallace et al., 2005), but they basically check on compliance to the
set requirements, for instance, during internal or external auditing (Van
der Spiegel et al., 2005). Recently, an instrument has been developed to
diagnose in a comprehensive and differentiated way a company specific
FSMS, independent of the QA standard that is implemented (Luning
et al., 2008, in press).

0168-1605/$ – see front matter © 2009 Elsevier B.V. All rights reserved.
doi:10.1016/j.ijfoodmicro.2009.02.018
114 L. Jacxsens et al. / International Journal of Food Microbiology 134 (2009) 113–125
According to Luning et al. (in press), a more sophisticated FSMS
would be better able to realise products with lower contamination levels
and less variation in contamination loads. The FSMS diagnose on system
level gives, however, no indication of the actual microbial performance
of companies' FSMS. Food processing companies commonly use
microbial testing of final products to assess if their products meet food
safety criteria (e.g. ICMSF, 2002; Legan, 2001). These criteria are set by
different stakeholders or regulatory bodies, like EU and/or country
regulations and/or customers' requirements but are also used to guide
the manufacturing process enabling a proper evaluation and define
preventive actions (Anonymous, 2005; Kvenberg and Schwalm, 2000;
Martins and Germano, 2008). Different authors recommended the use
of microbial 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 to
evaluate procedures for Good Hygienic Practices (GHPs) and Standard
Operating Procedures (SOPs) (e.g. Brown et al., 2000; Eisel et al., 1997;
Leaper and Richardson, 1999). However, to our knowledge, no
systematic microbiological evaluation of an FSMS performance has
been described previously.
This paper presents a Microbial Assessment Scheme (MAS) that can
be used for systematic analysis of microbial counts to assess the microbial
performance of core control activities in an implemented FSMS. Microbial
analyses to assess the FSMS performance are aimed at obtaining insight
in contamination profiles, which means insight into the maximum level
of microbial counts and the distribution in microbial contamination. This
information gives insight into the dynamics of microbial contamination
as a result of the designed and applied control strategies in an FSMS. The
concept of MAS is illustrated with a case study in a pork processing
company, 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 the
start point for the development of MAS. It comprises a comprehensive
list of core control and grids to assess at which levels these activities are
executed. The systematic diagnosis reveals which core control activities
are addressed in companies' FSMS and at which level. The basic
assumption behind this assessment tool is that systems performing on a
higher level are more predictable and better able to achieve a desired
safety outcome, because of less ambiguity (due to more insight in the
underlying mechanisms) and less uncertainty (due to more accurate
information) (Luning and Marcelis, 2006; Luning et al., in press). Table 1
provides more detailed information about the core control activities in
the FSMS, diagnosed by the diagnostic instrument. A distinction is made
between preventive measures, intervention processes and monitoring
systems, each strategy contributes differently to the control of microbial
food safety (Luning et al., 2008).
2.2. Elaboration of Microbial Assessment Scheme (MAS)
The proposed concept of MAS is based on a comprehensive
literature study in this field, discussions with experts on the concept of
FSMS diagnosis (Luning and Marcelis, 2006, 2007; Luning et al., 2006,
in press) and practical experience in food processing companies in
implementing their FSMS and fulfilling the legal/retail/QA standards
requirements by the Laboratory of Food Microbiology and Food
Preservation of Ghent University, Belgium (LFMFP-UGent) (Jacxsens
et al., 2006, 2007). The MAS procedure includes different elements
which are discussed below.
2.2.1. Identification of critical sampling locations
Critical sampling locations (CSL) are defined as locations where
microbial sampling provides information about the performance of
Table 1
Distinct control strategies with core control activities as addressed by the FSMS
diagnostic instrument (based on Luning et al., in press) and linked to the identified
critical 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 of
pathogens 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 1
materials)
• 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 processes
These 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 system
They affect food safety by providing information about the actual status of product or
process conditions, which enables process corrections, removal of non conformance
products, 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
1
Procedures for cleaning, personal hygiene, maintenance and calibration intervention
equipment, calibration and verification measuring and analytical equipment, CCP
procedures.
2
CSLs 5 and 6 indicate the performance of the overall food safety control activities.
core control strategies as addressed in the FSMS diagnostic instrument
(Table 1). In other words, loss of control at these locations will lead to
unacceptable food safety problems due to contamination, growth
and/or survival of microorganisms. The locations, where samples are
taken, will differ depending on the control activities that are
addressed in the companies specific FSMS (Table 2 is exemplified for
the illustrating case study).
A first CSL is the point of receipt of raw materials because initial
concentrations of microorganisms give insight into the potential safety
risks of the raw materials, which puts demands on the FSMS. Eisel et al.
(1997) and Codex Alimentarius Commission (2003) recommended the
inspection of raw materials before processing and where necessary
laboratory tests should be made to establish fitness for use. According to
Luning et al. (in press) higher initial levels of pathogens require more
sophisticated and reliable FSMS. The microbial performance at this CSL
gives insight in the adequacy of the raw material control in the FSMS (e.g.
proper selection procedures of suppliers and specifications of raw
materials (Jacxsens et al., 2009; Luning et al., 2008)).
Another CSL, that is assigned in the MAS, is during processing of
raw materials such as portioning, deboning, cutting and mincing,
 L. Jacxsens et al. / International Journal of Food Microbiology 134 (2009) 113–125 115

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

No CSL Microbiological Frequencya Sampling method Interpretation of results

parameters
1 At point of receipt of — Aerobic mesophilic 3 times 1 sample Non-destructive method a) According to EU Regulation
raw materials plate count (APC) on 100 cm2 of raw pork 2073/2005 Category 2.1.2b
(raw pork meat parts) — Salmonella meat parts 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 and — APC 3 times 1 sample Non-destructive method M = 2.5 log CFU/cm2
cutting or portioning — Salmonella on 100 cm2 of raw pork b) According to EU Regulation
(fresh pork meat cuts) meat cuts 2073/2005 Category 2.1.4 Salmonella
absent in the area tested
— E. coli c) According to microbiological guide
values of LFMFP-UGente
— Enterobacteriaceae E. coli absent in the area tested
— L. monocytogenes L. monocytogenes: absent in the area tested
3 After intervention — APC 3 times 1 sample Destructive method on According to microbiological guide values
strategy; curing 30 g of raw cured bacon of LFMFP-UGent for meat preparations
(raw cured bacon). — Salmonella before packaging a) APC
m = 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/g
c) E. coli
m = 2.7 log CFU/cm2
M = 3.7 log CFU/g
d) Salmonella: absent in 25 g
e) L. monocytogenes: absent in 25 g
4 After chilling or cooling — APC 3 times 1 sample Destructive method on According to microbiological guide values
processes i.e. fast 30 g of cooked ham before of LFMFP-UGente for cooked products
cooling (cooked ham) packaging without post contamination
— Salmonella a) APC
m = 3.0 log CFU/g
— E. coli M = 4.0 log CFU/g
— Enterobacteriaceae b) Enterobacteriaceae
— L. monocytogenes Below detection limit
c) E. coli: Below detection limit
d) Salmonella: absent in 25 g
e) L. monocytogenes: absent in 25 g
5 After packaging of the — APC 3 times 1 sample Destructive method on According to microbiological guide
final product 30 g of packaged cooked values of LFMFP-UGente for cooked
(cooked ham) ham products with post contamination
— Salmonella a)APC
m = 3.0 log CFU/g
— E. coli M = 4.0 log CFU/g
— Enterobacteriaceae b) Enterobacteriaceae
— L. monocytogenes m = 1.0 log CFU/g
M = 2.0 log CFU/g
c) E. coli
m = b 10 CFU/g
M = 1.0 log CFU/g
d) Salmonella: absent in 25 g
e) L. monocytogenes: absent in 25 g
6 After packaging of the — APC 3 times 1 sample Destructive method on According to microbiological guide
final product 30 g of packaged raw values of LFMFP-UGente for raw
(raw cured bacon) cured bacon mildly salted meat products
— Salmonella a) APC
m = 4.0 log CFU/g
— E. coli M = 5.0 log CFU/g
— Enterobacteriaceae b) Enterobacteriaceae
— L. monocytogenes m = 2.0 log CFU/g
M = 3.0 log CFU/g
c) E. coli
m = 2.7 log CFU/cm2
M = 3.7 log CFU/g
d) Salmonella: absent in 25 g
e) L. monocytogenes: absent in 25 g
7 Working tables at deboning — APC 3 times 3 samples at start–middle Surface swabbing of According to microbiological guide values
section (initial stage of the and end of the production day 25 cm2 of the table of LFMFP-UGente
process — production area) — E. coli Salmonella and L. monocytogenes: absent
in the tested area
— Enterobacteriaceae
— Salmonella
— L. monocytogenes

(continued on next page)

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

Table 2 (continued)
No CSL Microbiological Frequencya Sampling method Interpretation of results
parameters
8 Working tables at cured meat loins — APC 3 times 3 samples at start–middle Surface swabbing of
preparation (middle of the — E. coli and end of the production day 25 cm2 of the table
process — production area) — Enterobacteriaceae
— Salmonella
— L. monocytogenes
9 Working tables at packaging — APC 3 times 3 samples at start–middle Surface swabbing of
section (final stage of the — E. coli and end of the production day 25 cm2 of the table
process — packaging area) — Enterobacteriaceae
— Salmonella
— L. monocytogenes
10 Hands or gloves of food operators — E. coli 3 times 3 samples at start–middle Surface swabbing of According to microbiological guide values
at deboning section — production and end of the production day 25 cm2 of the hands of LFMFP-UGente
area — Enterobacteriaceae St. aureus: below detection limit
— S. aureus
11 Hands of food operators at cured — E. coli 3 times 3 samples at start–middle Surface swabbing of
meat loins preparation section (middle — Enterobacteriaceae and end of the production day 25 cm2 of the hands
of the process — production area) — S. aureus
12 Hands of food operators at the — E. coli 3 times 3 samples at start–middle Surface swabbing of
packaging area — Enterobacteriaceae and end of the production day 25 cm2 of the hands
— 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 consecutive
months (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 total
flora 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) has
concluded 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 properly
handled. The main sources of (cross)contamination during processing
come 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 of
various preventive measures addressed in companies' FSMS, such as
the extent of personal hygiene, specificity of sanitation program,
adequacy of product specific preventive measures, and hygienic
design equipment and facilities (Table 1).
A third distinct CSL is at the cooling facilities. Adequate cooling
capacity prevents the growth of mesophiles and mesophilic patho-
gens and the development of spores and limits the growth of
psychrotrophic microorganisms (ICMSF, 2005; Mossel et al., 1995).
Inadequate food temperature control is reported to be amongst one of
the most common causes of foodborne illness or food spoilage (Codex
Alimentarius Commission, 2003; Todd et al., 2007). Therefore, a CSL is
defined after critical cooling activities in order to assess the adequacy
of cooling facilities present in the food processing company.
Intermediate products directly after core intervention strategies, are
also considered as CSL. It provides information on the actual effectiveness
of the applied intervention processes in the FSMS. Different intervention
strategies are presented in Table 1. The level of microbial counts in final
products is another CSL, because it gives an indication of the overall
performance of an FSMS as a result of technology and managerial
dependent control activities that are executed to keep bacterial counts
below required limits (Luning and Marcelis, 2006, 2007).
The MAS also addresses food contact surfaces as critical sampling
locations, because it will give insight into the actual status of the
sophistication 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-Valls
et al., 2008; Jessen and Lammert, 2003) diverse food pathogenic bacteria
are able to attach to food contact surfaces, which can subsequently be
detached during production and contaminate food as it passes the
surface. Equipment and surfaces can be a source of direct contamination
when they have not been effectively cleaned or have been allowed to
remain moist between cleaning and use (e.g. Evans et al., 2004).
If during processing direct hand contact with the food product is
possible, also the hygiene of the hands/gloves of the food operators is
considered as a CSL, indicating the performance of personal hygiene as
a preventive measure in the FSMS (Table 1). Hands can contaminate
food through residential flora of the skin e.g. micrococci, staphylo-
cocci, propionic bacteria and corynebacteria; and contact between
hands and the environment, which contaminates hands with
transient flora such as fecal indicators E. coli and Salmonella (Aarnisalo
et al., 2006; Dijk et al., 2007).
2.2.2. Selection of the microbiological parameters
For each CSL, microbiological parameters must be defined. The
selected microbiological parameters will differ depending on the
production processes and food type that are addressed in the specific
company. Table 2 exemplifies this selection for the presented case study.
An FSMS is in the first place aiming at the production of safe food
according to the regulation and international guidelines (Anonymous,
2002; Codex Alimentarius Commission, 2003). Therefore, common
pathogenic microorganisms, relevant for the type of food product
processed in the company must be taken into consideration. Typically,
though not exclusively, Listeria monocytogenes and Salmonella spp. are
analysed 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 total
counts gives insight into the overall performance of the critical sample
location (ICMSF, 2002; Mossel et al., 1995). As an indicator of good
personnel hygiene and correct hand practices, Staphyloccocus aureus can
be selected (Aarnisalo et al., 2006; Dijk et al., 2007).
2.2.3. Assessment of sampling frequency
The first aim of MAS is to obtain a picture of the current
microbiological status of the core food safety control activities in an
 L. Jacxsens et al. / International Journal of Food Microbiology 134 (2009) 113–125
FSMS and their actual efficacy. Consequently, it is not the objective
to have a statistically underpinned sampling plan as described by
e.g. Augustin and Minvielle (2008), Baird-Parker (1995), Green
(1991) and Legan et al. (2001). It is as well not the aim to establish
attribute plans for food lot acceptance, as described by ICMSF 2 and
7 (Dahms, 2004; ICMSF, 1986, 2002; Legan et al., 2001). Therefore,
we propose to perform a MAS over three periods (e.g. three
consecutive months) in order to have insight in the distribution of
the microbial load at each CSL. For the environmental CSLs (food
contact surfaces and hands/gloves of food operators), also the
microbial contamination during the production day should be
followed by taking samples at the start of the production, at an
intermediate time, and at the end of the production. This gives
insight into the daily fluctuations.
2.2.4. Selection of sampling method and method of analysis
The selection of sampling method and method of analysis must be
performed in a reliable and systematic way. It is recommended to
follow-up the appropriate procedures as described in the ISO
standards issued by the ISO TC 34 SC9 on Microbiology of food and
animal feeding stuffs or the EU Regulation (Anonymous, 2005) where
appropriate.
2.2.4.1. Raw materials, intermediate products and final food products.
In the case of raw materials being meat carcasses (or parts) one is
referred to ISO 17604: 2003 which includes the use of destructive and
non-destructive techniques for the detection and enumeration of
microorganisms 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 carcass
sampling technique because the excision procedure achieves a higher
recovery of bacteria from meat carcasses as compared to swabbing
(Bolton, 2003; Capita et al., 2004). This is because swab sampling
removes only a proportion (often 20% or more) of the total flora
present on the meat surface (Anonymous, 2001; Capita et al., 2004).
Other studies, e.g. Byrne et al. (2005); Lindbald (2007), favor
swabbing to be efficient over excision because, the excision technique
samples a smaller area (typically 5 cm2) than swabbing (typically
100 cm2) and excision may not be the most suitable carcass sampling
technique for recovering enteric bacteria, which have a low incidence
and/or uneven distribution on meat carcasses. Moreover, meat from
healthy animals is internal sterile, hence excision sampling will not
produce a representative result for the surface contamination of the
fresh 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 of
food operators. ISO 18593: 2004 specifies horizontal methods for
sampling techniques using contact plates or swabs on surfaces in the
food industry environment (and food processing plants), with a view
of detecting or enumerating viable microorganisms (ISO, 2004a). The
same methodology is used to sample the hands or gloves of food
operators where a fixed surface (cm2) needs to be taken.
2.2.4.3. Analytical methods. Standardized methods (e.g. ISO
methods) are generally acknowledged as the reference method
and are recommended to be applied as the analytical methods for
MAS. However, also alternative (rapid) methods such as those
based on metabolic activity, immunoassays and nucleic acid based
tests, overviewed by Baylis (2005), can be applied, if they have
established performance characteristics or by preference are
validated according to ISO 16140: 2003 (ISO, 2003d). Analytical
methods are preferably executed in laboratories which operate
under quality assurance according to the principles of ISO 17025:
2005 (ISO, 2005a).
117
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 and
interpretation of obtained results. The data processing can easily be
done with Microsoft Office Excel in order to make graphs or tables to
illustrate visually the levels and distribution of microbial contamina-
tion over the three different sampling periods. No averages, standard
deviations or statistics need to be applied in order to evaluate the
variability over the three sampling periods on single company level.
Because, the microbial analyses for FSMS performance are aimed at
obtaining insight in contamination profiles, which means insight into
the maximum level of microbial counts and the distribution in
microbial contamination. This information gives insight into the
dynamics of microbial contamination as a result of the designed and
applied control strategies in an FSMS system.
The obtained results are evaluated in two ways. First, the obtained
results of each analysed microbiological parameter in a specific CSL are
interpreted. Therefore, the European Regulation on microbiological
criteria for foodstuffs should be applied if appropriate (Anonymous,
2005). If no legal requirements are set microbiological guidelines can
be applied. But it is recognized that although microbiological guide-
lines are widely used in the food industry, they have been published
rarely. They are mainly internal criteria applied by food business
operators (Stannard, 1997). These guidelines are aids to evaluate
whether the production process took place under controlled condi-
tions. If the legal requirements or the guide values are exceeded for a
specific microorganism in a CSL, it indicates that the specific control
activity in the FSMS, dedicated towards the defined CSLs according to
Table 1, is not working properly. Consequently, a corrective action (or
several) needs to be taken in order to change this non-conforming
situation and to improve the current FSMS performance.
Secondly, the concept of microbial safety level profiles is
introduced. For each microbiological parameter over the different
analysed CSLs a level is concluded. A microbial safety level can be
classified from 1 to 3, where level 3 is a good result (legal criteria or
guidelines are respected, no improvements are needed — current level
of FSMS is high enough to cover this hazard), level 2 is a medium
result (legal criteria or guidelines are exceeded, improvements need
to be made on a single control activity of the FSMS) and level 1 is a low
result (legal criteria or guidelines are exceeded, improvements need
to be made on multiple control activities of the FSMS). The sum of the
levels 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 processing
plant in Belgium. In this SME (approximately 50 people working in the
production area), an FSMS (certified for 4 years against the QA
standard BRC) has been implemented. The company specializes in
processing different ready-to-eat pork meat products. To evaluate the
microbiological performance of the FSMS by MAS, we selected in this
study the production of cooked ham and cured bacon. Cooked ham is
cured, cooked, cooled and packaged under vacuum conditions. The
raw cured bacon is dry cured, cured with brine, ripened in low
temperature conditions and is packaged under vacuum (final water
activity is approximately 0.96).
Along with MAS, we also conducted an FSMS diagnosis using the
instrument of Luning et al. (in press) via an in depth-interview in the
company (explained in Section 2.1). The levels of core control
activities were judged based on assessment grids. Level 1 indicates a
low level of the specific control activity in the FSMS and typically
related to the lack of scientific evidence, the use of company
experience/history, variable, unknown, unpredictable, based on
common materials/equipment, and not specific nor adapted for own
production system. Level 2 is an intermediate level of the specific
control activity in the FSMS that corresponds with best practice
118 L. Jacxsens et al. / International Journal of Food Microbiology 134 (2009) 113–125
knowledge/equipment, sometimes variable, not always predictable,
and based on generic information for the product sector. Level 3 is a
high level of the specific control activity in the FSMS typically
associated with proper scientific underpinning (accurate, complete),
stable, predictable, and tailored and tested for the specific food
production situation (Luning et al., in press). Where specific control
activities are not applicable or not relevant, level 0 is applied. The
interviewer with responsibility of quality and the manager of the
company assessed at which levels the various control activities in their
FSMS were 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 are
selected vertically through the production process and areas from raw
materials to the final products, including environmental samples. The
link between the identified CSLs for this case study and the FSMS
structure is illustrated in Table 1.
2.3.2. Selection of the microbiological parameters
The selected food safety parameters are, according to the MAS protocol
in Section 2.2.2, the pathogens Salmonella spp. and L. monocytogenes. As
hygiene indicators E. coli and Enterobacteriaceae are defined and as
indicator of personal hygiene Staphylococcus aureus. As indicator of overall
microbial quality, aerobic mesophilic plate counts are determined (utility
parameter) (Table 2).
2.3.3. Assessment of sampling frequency
MAS was performed during three visits in three consecutive
months, during each visit the 12 CSLs were sampled, as is motivated in
the MAS protocol in Section 2.2.3. The food stuffs (CSLs 1 until 6) were
each time single sampled, while the environmental samples (CSLs 7
until 12) were taken at three different times (beginning, middle and
end of the production day) during each visit (Table 2). Overall, a total
of 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) (CSLs
1 and 2). One site covering 100 cm2 for both raw pork meat parts
and fresh pork meat cuts, was sampled using abrasive sponges
(Envirosponge™, Biotrace International). Areas of sampling were
delimited by a sterile template. Sterile pre-moistened abrasive
sponges were used to swab vertically, horizontally and diagonally on
the delineated area. After swabbing, the abrasive sponges were
individually put in a sterile stomacher bag containing: 100 ml peptone
water for the enumeration of total mesophilic counts, Enterobacter-
iaceae, E. coli and L. monocytogenes; 100 ml buffered peptone water
for the detection of Salmonella spp; and 100 ml demi-Fraser solution
for the detection of L. monocytogenes. The samples were kept and
transported in a cool box maintained at ≤4 °C to the laboratory for
microbial analysis; and the samples were analysed within 6 h of
sampling.
2.3.4.2. Intermediate products and final meat products (CSLs 3 until 6).
Three hundred gram samples of raw cured bacon and cooked ham
were cut by using a sterile knife. The samples were aseptically stored in
stomacher bags and transported in a cool box maintained at ≤4 °C to
the laboratory; then the samples were analysed within 6 h of sampling.
2.3.4.3. Cotton swabs (hands or gloves and food contact surfaces) (CSLs 7
until 12). A sterile template was applied to delineate a 25 cm2 area
for sampling. Sterile pre-moistened cotton swabs (Cultiplast®) in 5 ml
peptone 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 solution
for the detection of L. monocytogenes were used to swab the working
tables. For enumeration of Enterobacteriaceae, E. coli and S. aureus on
hands or gloves of food operators, pre-moistened swabs in 5 ml
peptone water were used. A new sterile swab for each food contact
surface and analytical parameter was taken. Next, sampling swabs
were aseptically inserted back into their respective tubes containing
5 ml of the dilution media; the tubes were tightly closed, stored and
transported in cool box at ≤4 °C to the laboratory; and the samples
were analysed within 6 h of sampling.
2.3.4.4. Analytical methods. In the lab, 30 g subsamples were taken for
each food stuff per analytical parameter or group of analytical
parameters. Then, the samples were stomached for 30 s in the stomacher
with 270 ml of peptone water for enumeration of aerobic mesophilic
plate counts, Enterobacteriaceae, E. coli, and L. monocytogenes. Similarly,
25 g subsamples for each food stuff were taken and mixed with 225 ml of
either buffered peptone water for the detection of Salmonella spp. or
demi-Fraser solution for the detection of L. monocytogenes. For the
abrasive sponges, the samples were also stomached for 30 s; while for
the cotton swabs the tubes were vortex mixed for 10 s.
The samples to be subjected to an enumeration procedure initially
were serially diluted (1:9), then the resultant bacterial suspensions
were 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 results
The data processing is performed applying Microsoft Office Excel
2003. In Table 2 an overview is given for each CSL, which legal criteria
or microbiological guidelines were applied for the interpretation of
the results. If possible, the criteria from the European legislation are
applied (Anonymous, 2005). If legal criteria were not present for all
CSLs, then microbial guidelines, recommended by the Laboratory of
Food Microbiology and Food Preservation (LFMFP-UGent), Ghent
University (Debevere et al., 2006) were used.
3. Results
3.1. Results of FSMS diagnosis
The results of the diagnostic instrument of the assessment of core
control activities, as addressed in the companies' FSMS and explained
in Sections 2.1 and 2.3, are demonstrated in spider web diagrams.
These show the profiles of preventive measures design, intervention
process design, monitoring system design, and the actual operation of
the core control activities (Fig. 1A, B, C and D). These diagrams clearly
illustrate that a more coloured spiderweb is associated with control
activities that are elaborated at a higher level (level 3). The overall
level of the preventive measure design (Fig. 1A) is at level 3, only the
performance of the sanitation program scored level 2. The cleaning
and disinfection agents are based on knowledge from suppliers, but
are not adapted and tested for the specific food production
circumstances. Fig. 1B illustrates the intervention process design for
cooked ham and raw cured bacon separately because raw cured bacon
has no intervention equipment, whereas cooked ham does (i.e.
cooking and cooling). The used intervention steps are on level 3 (so
well tested for the specific production circumstances, and process
capability and effectiveness of intervention method are known),
which results in the reduction of the microbiological load. The results
of the monitoring system design are shown in Fig. 1C, where mainly
level 3 is obtained (i.e. scientific underpinned, systematic assessment,
sophisticated equipment for monitoring). However, the sampling
design and CCP analysis, for raw cured bacon, is on an intermediate
level (level 2) because both were designed based on, respectively,
empirical sampling plan and hygiene codes for the sector in
combination with expert support (which is typically level 2). Fig. 1D
 L. Jacxsens et al. / International Journal of Food Microbiology 134 (2009) 113–125
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): preventive measures design (A), intervention process design (B), monitoring system design (C), and operation of
food safety control system (FSCS) (D). (level 3 sophisticated situation, level 2 intermediated situation, level 1 low sophisticated situation, level 0 not appropriate).

119
120 L. Jacxsens et al. / International Journal of Food Microbiology 134 (2009) 113–125
shows the assessment of the actual operation of core control activities,
showing level 2 for compliance to procedures because the majority of
operators are familiar with existence of procedures (but not always
exact content); tasks are executed based on habits. Operators are
controlled on compliance to procedures on a regular basis. Fig. 1D also
indicates a level 2 for the appropriateness of procedures, meaning that
the procedures are available at location (often paper-based) and
understandable for most users but are kept up-to-date on ad-hoc
basis. The activity ‘actual analytical equipment performance’ scored 0
because no in-company laboratory activities are present. Overall, the
core control activities as addressed in their FSMS are at level 3, with
some at level 2 (which corresponds with aspects such as available
practice/equipment, experts knowledge and guidelines), indicating a
well 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 including
both food stuffs and environmental samples of food contact surfaces
as well as hands/gloves of food operators (Table 2). For none of the
samples, neither Salmonella spp. nor L. monocytogenes were detected
in 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)
Aerobic mesophilic plate counts (APC) at the different CSLs (1 until
6) are shown in Fig. 2. APC increased over CSLs 1, 2 and 3 during visits
1 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 the
detection limit on the CSLs 1 until 3: on the raw materials (CSL 1) both
Enterobacteriaceae and E. coli were found below the detection limit
(b1 CFU/cm2). Enterobacteriaceae were quantified on the fresh meat
cuts (CSL 2) but in low numbers (highest count of 30 CFU/100 cm2).
Also on the intermediate cured meat (CSL 3) Enterobacteriaceae and
E. coli were found below the detection limit (b10 CFU/g).
In two visits, APC were below the detection limit (b10 CFU/g) at CSL
4 (the chilled cooked ham which was sampled just after cooking and fast
cooling) (Fig. 2). Enterobacteriaceae and E. coli were below the detection
limit (b10 CFU/g) in CSL 4. After packaging the cooked ham (CSL 5), an
average increase of 1 log occurred (compared to CSL 4) in APC. However,
for cured bacon, an average decrease of 1 log occurred (APC comparing
CSL 6 with CSL 3) (Fig. 2). But Enterobacteriaceae and E. coli were below
the 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 the
three 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 the
CSLs 7, 8 and 9. The highest APC (1,10 × 105 CFU/25 cm2) was detected
at CSL 7; the working tables at the deboning area; the first part of the
processing line, but CSL 8 obtained similar results ranging from 103–
105 CFU/25 cm2. The APC on CSL 9 (working tables in the packaging
area) was lower (ranging from 102–104 CFU/25 cm2) as compared to
CSLs 7 and 8 (production area). Variation in numbers of APC is noticed
between the visits and times of sampling during production but no
systematic build up of the total counts can be detected. Enterobacter-
iaceae were often (17/27 samples) recovered from the food contact
surfaces with numbers ranging from 10 to 470 CFU/25 cm2, CSL 8
being the most contaminated, CSL 9 to a lesser extent. E. coli was only
rarely 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 food
operators over the three visits and three sampling times during
production are shown in Fig. 4A (S. aureus) and B (Enterobacteriaceae
and 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 the
packaging area (CSL 12). The hands/gloves at CSL 11 were shown to be
the most vulnerable CSL for the occurrence of Enterobacteriaceae. CSL
11 was the hands of a person preparing the cured meat. Numbers
ranged from 10–100 CFU/25 cm2. As is shown in Fig. 4A, S. aureus was
found 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 was
quantified on the hands of a food operator packaging grilled cooked
ham on CSL 12.
3.6. Microbial safety level profile
Based on the results obtained of the 156 samples taken over the 12
CSLs in the 3 month period, a microbial safety level profile can be
derived for this case study for each microorganism over the different
CSL's to evaluate the current microbiological status of the FSMS
(Fig. 5). For the pathogens Salmonella spp. and L. monocytogenes, level
3 can be attributed because no pathogens are detected. These results
are acceptable according with the legal requirements and/or guide-
lines (Table 2). Also for E. coli a level of 3 is obtained as this fecal
hygiene indicator is only found sporadic, in low amounts and not on
food stuffs. The obtained results are in accordance with the legal
requirements and/or guidelines (Table 2). S. aureus was detected on
the hands of food operators, both in the production and the packaging
areas (Fig. 4A). These results are not in line with the guidelines
(Table 2). This indicates that a specific improvement regarding
personal (hand) hygiene in the current FSMS is needed to solve this
problem and therefore level 2 is attributed (one specific control
activity in the FSMS needs to be improved). High counts are found on
the food contact surfaces for Enterobacteriaceae and APC. On the food
stuffs itself, these parameters were in accordance with the legal
criteria/guidelines. Therefore, a level 2 is attributed resulting in a
necessary improvement of sanitation processes in the current FSMS. A
total microbiological safety level profile of 15 is obtained in the case
study (Fig. 5).
4. Discussion
The two outputs of MAS (i.e. evaluation of each microbiological
parameter in a specific CSL and the microbial safety level profiles) give
insight in the actual microbiological status/performance of the
current FSMS present in a company. First, the MAS results give
 L. Jacxsens et al. / International Journal of Food Microbiology 134 (2009) 113–125
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 production
day for visit 1 –visit 2 –visit 3 □. B. Enterobacteriaceae (log CFU/25 cm2 — detection limit b 1 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 production day for visit 1 –visit 2 –visit 3 □, ⁎ indicates E. coli counted on the detection limit (b 1 log CFU/25 cm2).

121
 122
L. Jacxsens et al. / International Journal of Food Microbiology 134 (2009) 113–125
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 2 middle of the production day–time 3 end of the production day for visit
1 –visit 2 –visit 3 □. B. Enterobacteriaceae (log CFU/25 cm2 — detection limit b 1 log CFU/25 cm2) on hands/gloves of food operators CSLs 10–11–12: time 1 beginning of the production day–time 2 middle of the production day–time 3 end
of the production day for visit 1 –visit 2 –visit 3 □, ⁎ indicates E. coli counted on the detection limit (b1 log CFU/25 cm2).
 L. Jacxsens et al. / International Journal of Food Microbiology 134 (2009) 113–125
Fig. 5. Microbial safety level profile for the pork processing company: profile is
constructed by levels: total mesophilic counts, S. aureus, Enterobacteriaceae,
E. coli, L. monocytogenes, Salmonella. □ indicates the remaining microbial safety
level according to the maximum of 18, where improvement in the FSMS can be made.
information concerning the performance of a specific control activity
in an FSMS (in the case study demonstrated by results in Sections 3.2
until 3.5 linked to control activities of an FSMS shown in Table 1).
Secondly, the microbial safety profiles provide additional information
concerning the nature of the microbiological problem (in the case
study illustrated by Fig. 5).
In this case study, pathogenic microorganisms were not detected
in any of the CSLs for the whole period of the study. Therefore, it can be
suggested that the current FSMS in the company, with respect to
pathogens, is effective. This output from MAS can be combined with
the overall FSMS diagnosis (Fig. 1): although the FSMS diagnosis
shows a level 2 (intermediate level) on some control activities, the
MAS results demonstrate that they appear to be effective at this
moment. Thus, the current FSMS does not require improvements
regarding the control of the pathogens.
The incoming raw materials had low initial levels of contamination
with respect to the APC and Enterobacteriaceae compared to the legal
requirements (Table 2). Also the variation of the APC was small,
ranging from 60–380 CFU/100 cm2 which indicates an efficient
control of raw material. It is reported that the higher number of APC
usually relates to poor quality and a reduced shelf life of meat and
meat products (Eglezos et al., 2008; Eisel et al., 1997; Stopforth et al.,
2006). These MAS results suggest a good relationship with the
suppliers and robust procedures for the selection of suppliers in the
companies' FSMS. This was confirmed in the diagnosis of the FSMS
with the evaluation of the ‘product specific preventive measures’ on
level 3 (Fig. 1A).
A limited (and variable) increase in the microbial contamination of
the fresh meat cuts was noticed in the first stage of the production
process; deboning and trimming. The results correspond to the ones
obtained by Augustin and Minvielle (2008) who did a study on
microbiological contamination of pork meat cuts of 9 French cutting
plants from 1999 to 2003; finding that Enterobacteriaceae mean log
counts ranged from 0.6 to 2.2 log CFU/cm2. However, the surface
contamination 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 control
activities of the FSMS (Table 1) in the production area. If we compare
the intermediate product to the final product raw cured bacon, a
reduction in aerobic mesophilic counts is seen due to the short
ripening process at low temperatures before packaging as well as a
reduction in water activity (final water activity is approximately 0.96).
The raw cured bacon did not undergo an intervention strategy (dry
curing followed by brine curing at low temperatures) to eliminate the
microorganisms but to reduce them to an adequate level. Therefore,
this product should be regarded as a high risk product. These findings
are in line with the intermediate level of the diagnosis of the ‘CCP
analysis of raw cured bacon’ (level 2 in Fig. 1C). Consequently, the
companies' CCP analysis of raw cured bacon needs to be further
elaborated.
123
A very low contamination was detected on the cooked ham after
the fast cooling process (CSL 4). This is indicating that their cooling
capacity and process is adequate. This result was further confirmed by
the 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 are
processed, high APC and Enterobacteriaceae counts were found on
food contact surfaces. However, it did not led to an increase in
microbiological contamination of the fresh cut cuts. But when the
cooked ham was further processed in the packaging area, recontami-
nation occurred (Fig. 2). It is clear that a recontamination from the
product originates from the environment in the packaging area.
Different studies have reported working tables, equipment and hands
of food operators as the potential sources of cross contamination in
food processing industry (Gill et al., 2001; McEvoy et al., 2004; Tsalo
et al., 2007). The FSMS diagnosis revealed also that the ‘specificity of
their sanitation program’ is at level 2 (Fig. 1A) and can be improved. By
applying a more sophisticated sanitation program (i.e. typified by
cleaning agents adapted for the specific product and process
situations 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 the
presence of S. aureus in the hands in both the production and
packaging area, demonstrates that the hand hygiene was insufficiently
respected. Although the ‘extent of personal hygiene requirements’ was
assessed at level 3 (i.e. high requirements, for all food operators, on
clothing, personal care and health, with tailored facilities to support
personal hygiene, and specific training and hygiene instructions)
(Fig. 1A), the MAS results showed unsatisfactory performance, which
might be due to ‘inadequate compliance to procedures’, indicated by
the diagnostic instrument (level 2 in Fig. 1D). Nel et al. (2004)
emphasised that although basic personal and hygiene practices are
available they need to be optimised and regularly checked in practice
to be effective. Although the design is good, inadequate compliance to
procedures and instructions and/or their misinterpretation may
contribute to safety problems (Azanza and Zamora-Luna, 2005;
Gilling et al., 2001). Improvement can be obtained by the requirement
that all food operators are wearing gloves and training them in good
personnel hygiene and practices (Dijk et al., 2007).
A total microbiological safety level profile of 15 is obtained in the case
study, while the maximum level is 18 (i.e. 6 microbiological parameters
with a microbial safety level of 3) (Fig. 5). Consequently, this companies'
FSMS still has opportunities for improvement, specifically on the
microbial safety levels of S. aureus, Enterobacteriaceae and total counts.
In conclusion, the MAS gives an indication of the current microbial
performance of the different control activities in an FSMS, while the
FSMS diagnose indicates the level on which control activities are
conducted. The combination of these two tools can help food
processing industries to analyse their current FSMS in a systematic
way and can lead to define possibilities for improvements of an
effective FSMS.
Further, MAS can be applied as a tool for the (yearly) verification of
an FSMS on company level, as demanded by Codex Alimentarius (CAC,
2003; Hong et al., 2008; Jacxsens et al., 2009; Scott, 2003; Wallace
et al., 2005). The presented MAS protocol can easily be transferred
towards other sectors as meat product processes. The microbial safety
profiles can also be used to compare the current microbiological
performance of different companies with the same type of production
processes and food products. As such, microbiological problems in a
sector 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
124 L. Jacxsens et al. / International Journal of Food Microbiology 134 (2009) 113–125
Commission through the Sixth Framework Programme for Research
and Development. Also our special appreciation goes to the personnel
from the Accredited Lab, Laboratory of Food Preservation and Food
Microbiology, 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 case
study.
References
Aarnisalo, K., Tallavaara, K., Wirtanen, G., Maijala, R., Raaska, L., 2006. The hygienic
working practices of maintenance personnel and equipment hygiene in the Finnish
food industry. Food Control 17, 1001–1101.
Anonymous, 2001. Commission Decision 2001/471/EC of 8 June 2001 laying down rules
for the regular checks on the general hygiene carried out by the operators in
establishments according to Directive 64/433/EEC on health conditions for the
production and marketing of fresh meat and Directive 71/118/EEC on health
problems 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 the
Council of 28 January 2002 laying down the general principles and requirements of
food law, establishing the European Food Safety Authority and laying down
procedures 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 2005
on microbiological criteria for foodstuffs. Official Journal of the European
Communities 7/12/2007 (inclusive EU Regulation 1441/2007).
Augustin, J., Minvielle, B., 2008. Design of control charts to monitor the microbiological
contamination of pork meat cuts. Food Control 19, 82–89.
Azanza, M.P.V., Zamora-Luna, M.B.V., 2005. Barriers of HACCP team members to
guideline adherence. Food Control 16, 15–22.
Bagge-Ravn, D., Ng, Y., Hjlem, M., Christiansen, J.N., Johansen, C., Gram, L., 2003. The
microbial ecology of processing equipment in different fish industries—analysis of
the 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 the
microbiological 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 versus
swabbing. Food Control 14, 207–209.
British Retail Consortium (BRC), 2008. Global standard for food safety. Ed. TSO, PO Box
29, 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 of
microbiological testing in systems for assuring the safety of beef. International
Journal of Food Microbiology 62, 7–16.
Byrne, B., Dunne, G., Lyng, J., Bolton, D.J., 2005. Microbiological carcass sampling
methods to achieve compliance with 2001/471/EC and new regulations. Research
in Microbiology 156, 104–106.
Capita, R., Prieto, M., Alonso-Calleja, C., 2004. Review — sampling methods for
microbiological analysis of red meat and poultry carcasses. Journal of Food
Protection 67, 1303–1308.
CIES, 2007. Global Food Safety Initiative Guidance Document, 5th edition. foodsafety@ciesnet.
com, 41 pp. Accessed 8th of July 2008.
Codex Alimentarius Commission (CAC), 2003. Recommended International code of
practice 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 on
cutting boards. Letters in Applied Microbiology 40, 418–423.
Cormier, R.J., Mallet, M., Chiasson, S., Magnússon, H., Valdimarsson, G., 2007. Effectiveness
and performance of HACCP-based programs. Food Control 18, 665–671.
Dahms, S., 2004. Microbiological sampling plans — statistical aspects. Mitteilungen aus
Lebensmitteluntersuchung 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 guide
values and legal microbiological criteria. Laboratory of Food Microbiology and Food
Preservation (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 critical
control points to guarantee food safety. Food Control 19, 557–565.
European Hygienic Engineering Design Group (EHEDG), 2007. Integration of hygienic
and 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 of
raw, 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 incoming
raw 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 food
refrigeration equipment. Journal of Food Engineering 62, 225–232.
FAO/WHO, 2007. FAO/WHO guidance to governments on the application of HACCP in
small and/or less-developed food businesses. FAO Food and Nutrition Paper. ISSN
0254-4725.
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 stainless
steel surfaces. Food Control 19, 308–314.
Gill, C.O., Bryant, J., Badoni, M., 2001. Effects of hot water pasteurizing treatments on the
microbiological condition of manufacturing beef used for hamburger patty
manufacture. International Journal of Food Microbiology 63, 243–256.
Gilling, S.J., Taylor, E.A., Kane, K., Taylor, J.Z., 2001. Successful hazards analysis critical
control point implementation in the United Kingdom: understanding the barriers
through 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 of
parameters 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 data
from a Belgium-wide survey of Campylobacter species contamination in chicken
meat preparations and considerations for a reliable monitoring program. Applied
and Environmental Microbiology 74, 5483–5489.
Hong, C.H., Todd, E.C.D., Bahk, G.J., 2008. Aerobic plate count as a measure of hazard
analysis critical control point effectiveness in a pork processing plant. Journal of
Food Protection 71, 1248–1252.
ICMSF (International Commission on Microbiological Specifications for Foods), 1986.
Microorganisms in Foods 2: Sampling for Microbiological Analysis: Principles and
Specific 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/Plenum
Publishers, New York, p. 763. ISBN 030648675.
International Food Standard (IFS), 2007. Standard for auditing, retailer and wholesaler
branded food products. Ed. HDE Trade Services, Berlin, Germany, pp. 117.
ISO, 1996. Microbiology of Food and Animal Feeding Stuffs—Horizontal Method for the
Detection 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 the
Detection and Enumeration of Listeria monocytogenes—Part 2: Enumeration
Method. (ISO 11290-2:1998/Amd 1: 2004).
ISO, 2001. Microbiology of food and animal feeding stuffs—horizontal method for the
enumeration of β-glucoronidase positive Escherichia coli. Part 2: Colony-count
Technique 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 the
Detection of Salmonella spp (ISO 6579:2002).
ISO, 2003a. Microbiology of Food and Animal Feeding Stuffs—Horizontal Method for
the Enumeration of Microorganisms—Colony Count Technique at 30 °C (ISO
4833:2003).
ISO, 2003b. Microbiology of Food and Animal Feeding Stuffs —Preparation of Test
Samples, Initial Suspension and Decimal Dilutions for Microbiological Examination
(ISO 6887-2:2003).
ISO, 2003c. Microbiology of food and animal feeding stuffs—horizontal method for the
enumeration of coagulase positive Staphylococcus aureus and other species—Part 1:
technique using Baird–Parker agar medium. Amendment 1: Inclusion of precision
data (ISO 6888-1: 1999/Amd.1:2003).
ISO, 2003d. Microbiology of Food and Animal Feeding Stuffs — Protocol for the
Validation of Alternative Methods (ISO 16140:2003).
ISO, 2003e. Microbiology of Food and Animal Feeding Stuffs —Carcass Sampling for
Microbiological Analysis (ISO 17604:2003).
ISO, 2004a. Microbiology of Food and Animal Feeding Stuffs — Horizontal Methods for
Sampling Techniques from Surfaces Using Contact Plates and Swabs (ISO
18593:2004).
ISO, 2004b. Microbiology of Food and Animal Feeding Stuffs—Horizontal Method for the
Detection and Enumeration of Enterobacteriaceae — Part 2: Colony-count Method
(ISO 21528-2:2004).
ISO, 2005a. General Requirements for the Competence of Testing and Calibration
Laboratories (ISO 17025:2005).
ISO, 2005b. Food Safety Management Systems — Requirements for Any Organization in
the 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 the
food 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 drug
administrative perspective. Journal of Food Protection 63, 810–814.
Leaper, S., Richardson, P., 1999. Validation of thermal process control for the assurance
of food safety. Food Control 10, 281–283.
 L. Jacxsens et al. / International Journal of Food Microbiology 134 (2009) 113–125
Legan, J.D., Vandeven, M., Dahms, S., Cole, M., 2001. Determining the concentration of
microorganisms controlled by attributes sampling plans. Food Control 12, 137–147.
Lindbald, M., 2007. Microbiological sampling of swine carcasses: a comparison of data
obtained by swabbing with medical gauze and data collected routinely by excision
at Swedish abattoirs. International Journal of Food Microbiology 118, 180–185.
Luning, P.A., Marcelis, W.J., 2006. A techno-managerial approach to food quality
management. Trends in Food Science and Technology 17, 378–385.
Luning, P.A., Marcelis, W.J., 2007. A food quality management functions model from a
techno-managerial perspective. Trends in Food Science and Technology 18,
159–166.
Luning, P.A., Marcelis, W.J., in press. Food Quality Management: techno-managerial
principles and practices. Wageningen: Wageningen Academic Publishers.
Luning, P.A., Devlieghere, F., Verhé, R., 2006. Safety in Agri-Food Chains. Wageningen
Academic Publishers, Wageningen. ISBN: 9076998779, p. 681.
Luning, P.A., Bango, L., Kussaga, J., Rovira, J., Marcelis, W.J., 2008. Comprehensive
analysis and differentiated assessment of food safety control systems: a diagnostic
instrument. 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., in
press. Assurance activities in food safety management systems: how to diagnose
them? Trends in Food Science and Technology.
Martins, E.A., Germano, P.M.L., 2008. Microbiological indicators for the assessment of
performance in the hazard analysis and critical control points (HACCP) system in
meat lasagne production. Food Control 19, 764–771.
Manning, L., Baines, R., Chadd, S., 2006. Food safety management in broiler meat
production. 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 EU
Decision 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 Microbiology
of 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 hygiene
practices in the deboning room of a high throughput red meat abattoir. Food
Control 15, 571–578.
125
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) as
a part of an overall quality assurance system in international food trade. Food
Control 11, 345–351.
Schlundt, J., 2002. New directions in foodborne disease prevention. International
Journal 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 of
Food Protection 63, 815–818.
Todd, E.C.D., Greig, J.D., Bartleson, C.A., Michaels, B.S., 2007. Outbreaks where food
workers have been implicated in the spread of foodborne disease. Part 3. Factors
contributing to outbreaks and description of outbreak categories. Journal of Food
Protection 70 (9), 2199–2217.
Tsalo, E., Drosinos, E.H., Zoiopoulos, P., 2007. Impact of poultry slaughter house
modernisation and updating of food safety management systems on the
microbiological 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 of
the 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 standardized
HACCP assessment. British Food Journal 107, 723–742.