Stepwise Quantitatibe Risk Assessment of Microbiological Food Safety

Stepwise quantitative risk assessment as a tool for
characterization of microbiological food safety

S.J.C. van Gerwen
1
, M.C. te Giffel
1,2
, K. van `t Riet
1,3
, R.R. Beumer
1
and M.H. Zwietering
1,4
1
Department of Food Technology and Nutritional Sciences, Wageningen Agricultural University, Wageningen,
2
NIZO Food
Research, Ede,
3
TNO Nutrition and Food Research Institute, Zeist, The Netherlands and
4
CIRDC, Le Plessis Robinson,
France
7410/9/1999: received 28 September 1999, revised 28 January 2000 and accepted 1 February 2000
S. J. C. VAN GERWEN, M. C. TE GI FFEL, K. VAN ` T RI ET, R. R. BEUMER AND M. H. ZWI ETERI NG.
2000. This paper describes a system for the microbiological quantitative risk assessment for
food products and their production processes. The system applies a stepwise risk
assessment, allowing the main problems to be addressed before focusing on less important
problems. First, risks are assessed broadly, using order of magnitude estimates.
Characteristic numbers are used to quantitatively characterize microbial behaviour during
the production process. These numbers help to highlight the major risk-determining
phenomena, and to nd negligible aspects. Second, the risk-determining phenomena are
studied in more detail. Both general and/or specic models can be used for this and varying
situations can be simulated to quantitatively describe the risk-determining phenomena.
Third, even more detailed studies can be performed where necessary, for instance by using
stochastic variables. The system for quantitative risk assessment has been implemented as a
decision supporting expert system called SIEFE: Stepwise and Interactive Evaluation of
Food safety by an Expert System. SIEFE performs bacterial risk assessments in a
structured manner, using various information sources. Because all steps are transparent,
every step can easily be scrutinized.
In the current study the effectiveness of SIEFE is shown for a cheese spread. With this
product, quantitative data concerning the major risk-determining factors were not
completely available to carry out a full detailed assessment. However, this did not
necessarily hamper adequate risk estimation. Using ranges of values instead helped
identifying the quantitatively most important parameters and the magnitude of their impact.
This example shows that SIEFE provides quantitative insights into production processes
and their risk-determining factors to both risk assessors and decision makers, and highlights
critical gaps in knowledge.
I NTRODUCTI ON
Food safety is important for consumers, food producers
and inspection authorities for numerous reasons, including
consumer protection, producers' risk and international
trade. Food safety management systems, such as HACCP,
are often designed on the basis of qualitative data. More
quantitative insight into food safety issues can be obtained
by using quantitative risk assessment. Quantitative risk
assessment provides improved understanding of factors
involved in food safety. It consists of four steps: (i) hazard
identication, (ii) exposure assessment, (iii) hazard charac-
terization, and (iv) risk characterization (CODEX 1997).
Several quantitative risk assessments for specic micro-
biological hazards in products have been described in the
literature. For example, Listeria monocytogenes in soft
cheese (Bemrah et al. 1998), Salmonella enteritidis in pas-
teurized liquid eggs (Whiting and Buchanan 1997),
Salmonella in chicken products (Brown et al. 1998; Oscar
1998) and Escherichia coli O157:H7 in hamburgers (Cassin
et al. 1998; Marks et al. 1998).
In contrast to these examples for specic food products,
McNab (1998) presented an approach for quantitative risk
assessment for microbial food safety in general. The pre-
Correspondence to: S.J.C. van Gerwen, Unilever Research Vlaardingen,
Microbiology and Preservation, PO Box 114, 3130 AC Vlaardingen, The
Netherlands (e-mail: suzanne-van.gerwen@unilever.com).
Journal of Applied Microbiology 2000, 88, 938951
a 2000 The Society for Applied Microbiology
sent study also describes a general method for systematic
quantitative risk assessment for microbial safety of food
products. The rst part of this paper introduces the step-
wise and interactive method that has been developed for
bacteria. The second part describes the application of the
method for a cheese spread.
SI EFE AS A STRUCTURED METHOD FOR
QUANTI TATI VE RI SK ASSESSMENT
The stepwise method has been implemented as a decision
supporting expert system called SIEFE: Stepwise and
Interactive Evaluation of Food safety by an Expert system.
SIEFE has been developed for quantitative risk assessment
associated with microbial hazards for food products and
production processes. It uses three levels of detail, ranging
from semiquantitative, rough risk assessments to detailed
quantitative risk assessments. The stepwise approach
focuses on the aspects that quantitatively determine the
risk to a signicant extent and thus prevents important
aspects from being overlooked.
SIEFE starts with hazard identication. Hazards can be
identied at three levels of detail according to the hazard
identication procedure proposed by Van Gerwen et al.
(1997). The level of detail in the hazard identication pro-
cedure does not have to be the same as the level of detail in
the subsequent steps of SIEFE. Actually, the hazard identi-
cation procedure can be seen as a stand alone part of
SIEFE. The rst and second level of detail of the other
parts of SIEFE are described in the next sections.
Level 1 risk assessment
The rst level of detail is a rough, semiquantitative level.
This level provides rough estimates of risks related to the
consumption of a food product and identies risk-deter-
mining phenomena.
Level 1: Exposure assessment process identification.
At the rst level of detail, process steps and related data
for time, temperature (T), pH and water activity (a
w
) are
gathered, and entered in a table. Temperature, pH and a
w
are assumed to remain constant during a process step. The
estimated orders of magnitude in the rst level of detail are
generally conservative enough to be able to omit quantita-
tively negligible aspects without missing any potential rele-
vant ones. For certain process steps the estimates might be
too cautious. This will then be detected in level 2.
Level 1: Exposure assessment contamination. In the
rst level of detail it is assumed that all products are con-
taminated. The initial contamination level is assumed to be
one per serving, so N
0
=1 cfu serving
1
. A serving is
assumed to generally contain 100 g of the product. As a
consequence, exposure is actually based on the change of
the concentration of organisms in a serving, instead of
being estimated as a concentration of organisms present.
The knowledge rules presented in Table 3 highlight the
necessity of changing this assumption in cases where the
contamination level may greatly inuence risk.
Level 1: Exposure assessment growth & inactivation. At
level 1, orders of magnitude for inactivation and growth are
estimated by rst order kinetics. The logarithm of the
increase or decrease of micro-organisms can then be esti-
mated by the equation:
ln
N
N
0

= vtX
where N is the concentration of organisms (cfu serving
1
),
and N
0
is the initial concentration of organisms per ser-
ving.
For growth, v =m, where m is the maximum specic
growth rate of the organism (s
1
). The value for m is esti-
mated by means of the gamma model (Zwietering et al.
1996). The growth characteristics of the various pathogens
included in SIEFE were derived from the literature, and
placed into the so-called pathogen database (Van Gerwen
et al. 1997). Lag time is neglected in level 1 resulting in
fail safe predictions.
For inactivation, v =k. SIEFE estimates the value for
the inactivation rate k (s
1
) from D-values (D), with equa-
tion 1:
k = ln(10)aD (1)
D-values were reported for many pathogens under var-
ious conditions in the literature and these data were also
included in the pathogen database. For the selected hazard,
the expert system takes data from the pathogen database
and describes log(D) as a response variable of temperature
by linear regression. Then the 95% condence interval of
the estimated log(D
temp
) is calculated, and the 95% upper
limit is used as a worst-case estimate for D at the tempera-
ture of heat treatment.
Inactivation processes may theoretically result in less
than 1 cfu serving
1
. For example if N=10
4
, a reduction
of 10
6
results in 10
2
cfu serving
1
. Since this is not a rea-
listic gure, 10
2
cfu serving
1
is considered as 1 cfu per
100 servings, and SIEFE continues calculations with 1 cfu
serving
1
after inactivation. The probability of presence of
organisms after inactivation is described by the hazard
characteristic OC (òccurrence characterization'). OC is
dened as the logarithm of the theoretical amount of
939 STEPWI SE QUANTI TATI VE RI SK ASSESSMENT
a 2000 The Society for Applied Microbiology, Journal of Applied Microbiology, 88, 938951
organisms after inactivation (N
ai
, ài' indicating àfter inac-
tivation'), as shown in equation 2.
OC = log(N
ai
) (2)
In the above example, OC=2. If N
ai
is larger or equal
to one, OC is equal to zero. Reductions of 10
20
or more are
considered as complete inactivation; it is assumed that no
organisms survive the inactivation treatment. N
ai
then is
zero, and OC= o.
Level 1: Hazard characterization. Doseresponse data esti-
mate the probability of infection and illness after exposure
to a certain number of pathogens. Level 1 uses rst impres-
sions of pathogen infectivity, provided by attention values
for infection and intoxication (AV). Attention values can be
derived from, for instance, data on reported outbreaks,
expert knowledge, microbiological norms and MID-values
(minimal infectious dose). Attention values derived from
the literature have been incorporated in the pathogen data-
base. In case exposure to a pathogen is close to, equal to or
greater than AV (cfu serving
1
), the probability that pro-
blems will occur is realistic. Examples of AV values for a
variety of pathogens are shown in Table 1.
The probability of foodborne illness as a result of con-
suming a certain concentration of a hazard can be estimated
using the AV. This probability is described by the HC
value (`health problem characterization'). HC is dened as
Table1 Attention values (AV), doseresponse parameters for infection (r; the probability of an organism surviving and causing infection
after ingestion, for the Exponential model, and a, b; the parameters of the Beta-distribution, for the Beta-Poisson model) and mortality
ratios for various bacteria. These doseresponse data result in an estimate of the probability of a certain health effect occurring, given
consumption of a contaminated product
Bacteria Source* AV (cfu) Exponential (r) Beta-Poisson (a/b) Mortality ratio (%){{
Bacillus cereus 1 1 10
5
00010
Campylobacter spp. 2,3 0039/55 028,
C. jejuni 4 500
C. jejuni A3249 10 352 10
6
0145/7589
Clostridium botulinum type A 11,13 100 15
C. perfringens 4,6,7 1 10
5
010
Escherichia coli 5,6 1 10
4
030
E. coli O157:H7 7 20
L. monocytogenes 6,8,9 100 1179 10
10
32
Plesiomonas shigelloides 10 442 10
10
0057/1171
Salmonella spp. 2,3,4 1 033/1399 021,
S. typhi 2,7 021/5531 60
S. typhi Quailes 10 214 10
8
0203/29173
Shigella spp. 2,7 016/155 013
S. dysenteriae 1 2 05/100
S. dysenteriae 1 10 205 10
4
0157/916
Staphylococcus aureus** 6,12 1 10
6
010
Vibrio cholera classical 2 0097/13020
V. cholera El Tor 2 27 10
5
/133
V. cholerae 569b 10 176 10
9
0508/752 10
7
V. parahaemolyticus 3,4 1 10
4
0
*See References. 1 Notermans et al. (1997), 2 Rose and Gerba (1991), 3 Bean et al. (1996), 4 Shapton and Shapton (1991),
5 Rose et al. (1995), 6 Bean and Grifn (1990), 7 Todd (1989), 8 ICMSF (1994), 9 Buchanan et al. (1997), 10 Teunis et al.
(1996), 11 Hauschild (1993), 12 Jay (1992), 13 Ter Steeg and Cuppers (1995).
{(Fatal cases)/(total cases of illness or intoxication for the organism) 100.
{If several values were given in literature, the worst case value was taken.
,The average of deaths/cases for the organism of 198892 was used.
Pooled dataset for strains A-1 and M 131.
**Jay (1992) reported for Staph. aureus that r510
5
110
6
cfu g
1
must be present for food poisoning symptoms in man. Consequently,
for a serving size of 100 g AV should actually be 10
8
cfu serving
1
. AV=10
6
cfu serving
1
is, however, used because of the safety
perspective.
940 S. J. C. VAN GERWEN ET AL.
the logarithm of the estimated concentration of the hazard
in the product (N) divided by the AV for the hazard (equa-
tion 3).
HC = log
N
AV

Y if NrAV then HC = 0 (3)
HC is a simple representation of log linearity of dose
response relations. For example, Buchanan et al. (1997)
also assumed log-linearity of the doseresponse relation for
Listeria monocytogenes.
Level 1: Risk characterization. SIEFE uses characteristic
numbers for risk characterization. Whereas the OC value
describes the probability of occurrence of a hazard in the
product, the HC value characterizes the probability of
health impairment, given occurrence of the hazard.
Together they characterize the probability of foodborne ill-
ness as a result of consuming a certain product. A measure
of this probability is the PC value (`probability characteri-
zation'). PC is dened as the sum of OC and HC (equation
4).
PC = OC HC (4)
In level 1, probabilities are categorized from very low to
very high, using the PC, OC and HC values, for example if
PCis less than 6 the probability of having problems is
considered to be `very low'; less then one in a million peo-
ple will have problems as a result of consuming a serving
(100 g) of the product (Table 2). The categories were cho-
sen by sensible reasoning and can be changed if required.
After characterizing the probability of foodborne illness
by PC, risk-determining phenomena of production pro-
cesses are found by calculating the step characteristic SC
(equation 5) and by considering knowledge rules.
SC = log
N
i
N
i 1

(5)
SC calculates the logarithmic change in pathogens per
process step. Process steps that are characterized by a high
value of SC are generally major determinants of risk.
Growth and inactivation have been categorized by means
of the absolute value of SC, ranging from low to complete
growth and inactivation (Table 2).
The knowledge rules for selecting the risk-determining
phenomena must explicitly be mentioned in the procedure
to allow transparency. Consequently, they can be scruti-
nized and changed if necessary. The knowledge rules are
shown in Table 3.
The goal of the rst level is to rank risks and efciently
establish risk-determining phenomena, using values that
are conservative. It is best to try several situations, and
vary several parameters in the rst level of detail, to be
sure that no relevant risk-determining phenomena are over-
looked.
Level 2 risk assessment
The risk-determining phenomena, identied in level 1, are
studied in a more quantitative way in the second level.
Level 2: Exposure assessment process identification.
Temperature is often a risk-determining factor since both
growth and inactivation greatly depend on it. For certain
specic process steps, such as cooling, changes in tempera-
ture deserve special attention with regard to food safety.
Below a practical example for estimation of temperature
gradients is shown.
Zwietering and Hasting (1997) derived practical equa-
tions for estimation of the temperature in the centre of
(semi)solid products in batch systems without product con-
Table2 Categorization of the probability of having problems, and of growth and inactivation by characteristic numbers PC (probability
characterization) and SC (step characterization). OC is the characteristic number for occurrence characterization and HC for health-
problem characterization
PC, OC and HC SC
growth
* SC
inactivation
*
Very low 6
Low 6 <PC5 <03 <1
Moderate 5 <PC4 03 SC<1 1 SC<5
High 4 <PC 3 1 SC<5 5 SC<10
Very high 3 <PC0 5 SC<10 10 SC<20
Complete r10 r20
*Absolute values of SC are given.
Table3 Knowledge rules to be used for support in establishing risk-determining phenomena and relevant scenarios in level 1 risk
assessments implemented in SIEFE (for denitions: see Table 2). The text printed in italics provides an explanation to the points 1174
1. If PC is very low, because of complete inactivation:
11. study recontamination after inactivation.
Since the inactivation is overwhelmingly large, it is not useful to study it more accurately. If recontamination occurs after inactivation, this may
completely determine risk; if high growth occurs, or a highly infectious pathogen is concerned, the prevalence of recontamination is mainly
important, if moderate or low growth occurs, the level of recontamination is important.
2. If PC is very low, because of high or very high inactivation:
21. study recontamination after inactivation,
22. study the parameters that determine growth,
23. study the steps that result in the largest changes (see SC values).
The hazard is inactivated to a very high extent. However, inactivation is not complete, and therefore it is interesting to study it more accurately.
Recontamination in an almost sterile product may completely determine risk. Small changes in process parameters may well change growth
opportunities after inactivation, and thereby result in risk-determining process steps, so it is interesting to study growth-determining parameters in a
scenario.
3. If PC is very low, with moderate, or low, or no inactivation:
31. study the initial contamination level,
The growth and inactivation kinetics appear not to be really relevant during the production process, so the initial contamination level can be risk-
determining. Also, small changes in process parameters may well change growth opportunities, and thereby result in risk-determining process steps.
It is therefore interesting to study growth determining parameters in a scenario.
4. If PC is moderate or low, because of high or very high inactivation, or complete inactivation with recontamination:
41. study doseresponse data,
42. study recontamination,
The hazard is largely inactivated. However, remaining organisms or organisms that recontaminate the product after inactivation may be able to
cause problems. Risk depends on which process step has the biggest inuence under certain circumstances. Accurate doseresponse data may also
be relevant, especially in the range of moderate risk estimates.
5. If PC is moderate or low, with moderate, or low, or no inactivation:
51. study the initial contamination level,
52. study doseresponse data,
54. study inactivation (if present),
The initial contamination level may be risk-determining, since growth and inactivation may exclude each other's effects. More accurate dose
response data may result in a different estimation of risk. Small changes in process parameters may well change growth opportunities and thereby
result in other risk-determining process steps (other steps showing the largest changes); so it is interesting to study growth-determining parameters
in a scenario. In level 1, inactivation is based on a worst-case value for the inactivation parameter k. Risk estimates may be lower if specic
values are used for k.
6. If PC is high or very high, because of high or very high growth:
61. study (re)contamination,
63. study the steps resulting in the largest changes (see SC values).
As organisms apparently are able to grow very well, prevalence of contamination, or recontamination after inactivation may completely determine
risk. In level 1, inactivation is based on a worst-case value of k. Risk estimates may change if specic values are used. It is therefore interesting
to re-estimate inactivation. Several inhibitory substances may result in less growth in practice, so the steps resulting in the largest changes are
important to study.
7. If PC is high or very high, with moderate, low, or no growth:
71. study (re)contamination,
72. study doseresponse data
74. study the steps resulting in the largest changes (see SC values).
Prevalence of contamination, or recontamination after inactivation may completely determine risk, since the presence of the hazard, even in small
amounts, results in high risk. Doseresponse data apparently are very important for risk. In level 1, inactivation is based on a worst-case estimate
of k. Risk estimates may change if specic values are used. It is therefore interesting to re-estimate inactivation.
vection. For example, in case the external resistance is neg-
ligible (often the case in food heat treatments), the centre-
temperature in a cylinder, with a height of two times the
radius (R), can be described by:
T
centre
= T
ext
(T
0
T
ext
) 20397
exp( 82514 Fo)
T
0
is the initial temperature in the centre of the product,
and T
ext
is the temperature of the heating or cooling med-
ium. This equation is valid for Fo >00864, with Fo being
the Fourier number:
Fo =
lst
c
p
srsL
2
where l is the thermal conductivity of the product (J s
1
m
1
K
1
), t is time (s), c
p
is the thermal coefcient of the
product (J kg
1
K
1
), r is the product density (kg m
3
)
and L is the characteristic dimension (m). In this example,
L is equal to the radius. Values for l, c
p
and r can be
found in the literature for various products, see for exam-
ple Tschubik and Maslow (1973) and Mohnsenin (1980). If
the values for a certain product are unknown, approximate
values of similar products can be used. In many cases
values for water, l =06 J s
1
m
1
K
1
; c
p
=4200 J kg
1
K
1
; r =1000 kg m
3
(Anonymous 1978), can be used as a
rst approximation, since water is the major constituent of
most food products.
Growth and inactivation at changing temperatures are
estimated for small time steps, assuming temperature to be
constant per time step.
Level 2: Exposure assessment initial contamination.
Food products can be contaminated via raw materials
(initial contamination) or by recontamination during the
production process. SIEFE uses data from various litera-
ture references to help the user in selecting realistic con-
tamination levels and incidences for the specic product
and hazard under study. These data are stored in the food
database (Van Gerwen et al. 1997). Table 4 shows an exam-
ple of data that have been stored in the database for con-
tamination of various dairy products.
If contamination level or incidence are risk-determining,
and there is a level of uncertainty in the estimates of con-
tamination, it is sensible to use a range of contamination
data to calculate exposure, for example N
0
=1 to 10
4
cfu
serving
1
. Then, the importance of a more accurate estima-
Table4 Example of contamination data stored in the food database
Product/
ingredient Genus
% positive
samples*
Number of
samples*
Concentration
(cfu g
1
) Remark Source{
Consumption milk Bacillus cereus 357 157 1 10
4
1
Consumption milk Clostridium perfringens 1 < 1 spore ml
1
2
Consumption milk Clostridium tyrobutyricum 02 < 02 spores ml
1
2
Raw cow milk Bacillus cereus 35 185 3
Raw cow milk Bacillus cereus 9 100 100 4
Raw cow milk Clostridium botulinum 0001 < 1 l
1
2
Pasteurized cow milk Bacillus cereus 100 38 01 5
Pasteurized cow milk Bacillus cereus 35 100 1000 4
Sterilized cow milk Bacillus cereus 40 148 4
Cheese Brucella abortus 0 63 6
Cheddar cheese Campylobacter jejuni 0 127 6
Cheddar cheese Clostridium botulinum 0 40 2
Cheddar cheese Bacillus cereus 14 50 100 4
Gouda cheese Clostridium botulinum 0 40 2
Soft cheese Escherichia coli 10 2000 6
Soft cheese Listeria monocytogenes 10 174 18 Imported from France 7
Soft cheese Listeria monocytogenes 60 333 20 From several countries 7
Oriental soft cheese Escherichia coli 25 240 6
*In case a range of values was given, the worst-case value was included in the database.
{See References. 1 Te Giffel et al. (1996b), 2 Collins-Thompson and Wood (1993), 3 Te Giffel et al. (1996a), 4 Doyle (1989), 5
Notermans et al. (1997), 6 Johnson et al. (1990), 7 Loncarevic et al. (1995).
tion of initial contamination can easily be deduced. Figure
1 shows an example where accurate estimation of contami-
nation is not relevant, since the hazard is completely inacti-
vated (reduction >10
20
) during heat treatment in process
step 5 for all scenarios of initial contamination from 1 to
10
4.
This example clearly illustrates that it is not relevant
to go into more detail when estimating a value (in this case
contamination level). The conclusion would remain the
same even if a very inaccurate value is used.
Level 2: Exposure assessment recontamination.
Recontamination of the product occurs in many ways, for
example, by workers' hands, micro-organisms present in
stagnant areas and contact surfaces. At present,
quantitative models to estimate recontamination are scarce.
Data in the literature can, however, be used for support in
estimation of recontamination. De Wit and Kampelmacher
(1981), for example, reported amounts of pathogens present
on hands of workers in various food industries. These data
can be used, and have been incorporated in the food data-
base. As for initial contamination, it is sensible to use a
range of values for recontamination if there is uncertainty
in the estimates. Figure 1 shows an example of the irrele-
vance of accurate estimation of the level of recontamina-
tion. Whatever level of recontamination is used, from Fig.
1 it can be concluded that large growth takes place in pro-
cess step 10, and the product will be unsafe in any case.
Level 2: Exposure assessment inactivation and growth.
In level 2, inactivation and growth can best be estimated by
several models and comparing the results of the models
(Van Gerwen and Zwietering 1998). Comparison of models
is useful, as no single model is currently able to accurately
predict microbial responses under all circumstances.
Moreover, it gives an indication of the uncertainty and
variability in estimation of growth and inactivation. Van
Gerwen and Zwietering (1998) employed several primary
and secondary models that can be applied for general pre-
dictive purposes, and these models have all been imple-
mented in SIEFE. Also, the literature on specic growth
and inactivation models (often response surface models) for
various pathogens has been cited in SIEFE.
In addition to comparison by various models it is sensi-
ble to study the growth and inactivation parameters of the
hazard in more detail in level 2. In level 1 worst-case esti-
mates of these parameters were used, which may result in
predictions that are unnecessarily conservative for the spe-
cic situation studied.
Level 2: Hazard characterization. In level 2 doseresponse
curves are created with the doseresponse parameters avail-
able. In practice, there are relatively few doseresponse
data available to describe the probability of infection and
they relate to a few infectious and toxico-infectious patho-
gens only. The problems associated with the extrapolation
10
10
Process steps
l
o
g
(
N
)
0
0
8
6
4
2
9 8 7 6 5 4 3 2 1
Fig. 1 The use of various scenarios for (re)contamination in exposure estimations. Initial contamination level varies between log(N
0
) =0
(lower line) and log(N
0
) =4 (upper line). During heat treatment (step 5), the pathogen is completely inactivated (reduction >10
20
),
pictured as log(N) =0. Immediately after heat treatment, recontamination occurs. Recontamination level varies between log(N
rec
) =0
(lower line) and log(N
rec
) =4 (upper line). After recontamination, the maximum amount of pathogens (N=10
10
cfu serving
1
) is reached
during storage (step 10)
of experimental doseresponse results to real-life situations
have frequently been mentioned in the literature (Haas
1983; Rose and Gerba 1991; ILSI Risk Science Institute
1996; Buchanan et al. 1997). Models to generate dose
response curves are, for example, the Exponential model
and the Beta-Poisson model (Haas 1983; Teunis et al.
1996). Some of the reported values of doseresponse para-
meters for several bacteria with these two models are
shown in Table 1. The doseresponse data result in an esti-
mate of P
h
, being the probability of a certain health effect,
for example infection and illness, given consumption of a
contaminated product.
Severity (S) is a phenomenon that needs to be quantied
for estimation of consumer risk, regarding the CODEX
(1997) denition of risk: a function of the probability of an
adverse health effect and the severity of that effect, conse-
quential to a hazard(s) in food. Severity can be considered
as a weighing factor enabling hazard and risk ranking and
facilitating health resource allocations. None of the for-
merly mentioned papers on quantitative risk assessment
(Whiting and Buchanan 1997; Brown et al. 1998; Cassin
et al. 1998) included quantitative data on the burden of dis-
ease into the risk estimates. The CAST report (1994) gives
a straightforward, qualitative categorization of severity
varying from `mild, self-limiting, for 1 day' to `severe,
for months' that can be used as a practical tool for risk
ranking.
Since there are very few quantitative data on severity of
foodborne illness at the moment, it was decided to use S=
1 in SIEFE for all risk assessments. Actually, this results in
an estimate of the probability of having problems, instead
of the actual risk. Supplemented by the qualitative cate-
gories presented by the CAST report (1994), the probabil-
ity of having problems can still be used for risk and hazard
ranking.
Level 2: Risk characterization. The risk characterization
procedure estimates the risk of a certain health effect
occurring as a consequence of the consumption of a certain
food product. The risk to the consumer of a single con-
sumption is:
Consumer risk = P
e
P
h
S (6)
where P
e
is the probability of a contaminated serving, S is
a measure for severity (assumption S=1) and P
h
is the
probability of a certain health effect (h) occurring. P
h
is
based on doseresponse data and data on foodborne disease
outbreaks. For example, the probability of mortality can be
described as (Haas et al. 1993; Teunis et al. 1996):
P
h
= P(ije)P(illji)P(djill) (7)
where P(i|e) is the probability of infection, given a certain
exposure (e). P(i|e) can for example be estimated with the
Beta-Poisson model. P(ill|i) is the conditional probability
of illness after infection. This probability was assumed to
be independent of the ingested dose. If quantitative data
are not available, P(ill|i) is assumed to be one (worst-case).
P(d|ill) is the conditional probability of dying after devel-
oping disease. P(d|ill) can for example be based on food-
borne outbreaks of disease (Table 1), assuming that a
constant fraction of infected individuals suffers from severe
outcomes.
Following equation 6, the risk of not having problems
after n servings per year is:
Risk
no prob
= (1 P
e
P
h
S)
n
(8)
The risk of having one or more problems by consuming
n servings of a certain product per year can therefore be
estimated by:
Risk = 1 (1 P
e
P
h
S)
n
(9)
Like in level 1 the quantitative determination of the phe-
nomena that are most inuential needs to be conducted
subsequently.
If the estimates for P
h
and P
e
are very uncertain, it is
best to estimate risk using ranges of values and test the
importance of more accurate estimation of these para-
meters. This is presented for cheese spread in the present
study. If parameter-estimates clearly affect risk estimations,
it is sensible to accurately study the parameters in a third
level of detail, for example, by experimental studies, a
more extensive literature search and/or stochastic descrip-
tion of the parameters.
RESULTS
SIEFE applied to cheese spread
Hazard identification cheese spread. The SIEFE
method was applied to a processed cheese, namely cheese
spread, dened by CODEX as à product made by grind-
ing, mixing, melting, and emulsifying with the aid of heat
and emulsifying agents, one or more varieties of cheese,
with or without addition of milk components and/or food-
stuffs'.
The hazard identication procedure, presented by Van
Gerwen et al. (1997) selected Clostridium botulinum type A
and Cl. botulinum type B proteolytic as the most obvious
hazards for cheese spread. These organisms were reported
to have caused outbreaks related to the consumption of
cheese spread in the past (Meyer and Eddie 1951; Briozzo
et al. 1983). It is advisable to rst estimate risk for these
pathogens, before focusing on other hazards.
Level 1: Exposure assessment cheese spread. The
production process of cheese spread used in this example
was based on the literature (Caric and Kalab 1993) and
practice, and is shown in Table 5. Growth and inactivation
as well as SC values were estimated (Table 5). Cl. botulinum
type A is completely inactivated (SC< 20) and proteoly-
tic type B is highly inactivated during heat treatment (SC
=961). OC=log(N
ai
) =o and 935, respectively,
meaning very low occurrence in both cases (Table 2).
Level 1: Hazard characterization cheese spread. For
both types of Cl. botulinum, AV was assumed to be 10
2
cfu
serving
1
(Ter Steeg and Cuppers 1995).
HC was estimated to be very high for Cl. botulinum: HC
=log(132/100) =188.
Level 1: Risk characterization cheese spread. PC was
estimated to be very low for both types of organisms: PC
=o188 =o for Cl. botulinum type A and PC=
935188 =1123 for proteolytic type B. Heat inacti-
vation is obviously a risk-determining phenomenon that
needs closer study for Cl. botulinum type B. For Cl. botuli-
num type A the reduction is overwhelmingly large and clo-
ser study is not necessary. Table 3 shows that other risk-
determining phenomena are: recontamination after inacti-
vation and the parameters that determine growth after
incomplete inactivation.
Various situations were simulated (four scenarios in
total: cs1 to cs4) to get rst impressions on the importance
of varying parameters. Table 5 shows the results of the
simulations for Cl. botulinum type B proteolytic.
Table5 Production process of cheese spread with characteristic numbers. Bold values indicate quantitatively important steps. The value
`000' means very little growth or inactivation that could not be expressed in two decimals. The value `0' for SC values means no growth
or inactivation
Process step Time
Temp.
(
o
C)
SC
type A/B*
SC type B
scenario cs1{
SC type B
scenario cs2{
SC type B
scenario cs3,
SC type B
scenario cs4
Trimming cheeses 1 h 20 007 007 007 007 007
Blending 2 h 20 015 015 015 015 015
Shredding (grinding, milling) 15 min 20 002 002 002 002 002
Addition emulsiers 15 min 20 002 002 002 002 002
Heat treatment 2 s 145 <20/961 063 <20 961 961
Creaming 30 min 90 000 000 000 000
Packaging 10 min 70 000 000 000 000
Cooling1** 15 min 37 010 010 010 010
Cooling2 15 min 20 002 002 002 002
Storage 8 weeks 10 0 000 10 10
N
ai
0/10
935
0427 0 10
935
1
N 132 132 0 10
10
10
10
AV 10
2
10
2
10
2
10
2
10
2
OC o/935 037 o 935 0
HC 188 188 o 0 0
PC o/1123 225 o 935 0
Probability of having problems Very low High Very low Very low Very high
*Growth characteristics of Cl. botulinum type A and type B proteolytic: T
min
= 10
o
C, T
opt
= 35
o
C, T
max
= 50
o
C, pH
min
= 46, pH
opt
= 7,
pH
max
= 9, a
w,min
=093 (Mitscherlich and Marth 1984; Shapton and Shapton 1991; ICMSF 1996); m
opt
=1 h
1
, from FDSS (Wijtzes et al.
1998). The worst-case inactivation parameter k
145
# for Cl. botulinum type A: k
145
#=18210
3
min
1
; for Cl. botulinum type B proteolytic
k
145
#=671 min
1.
Data from ICMSF (1996) were used for estimation of k.
{Heat treatment at 130
o
C, for 3 s.
{Heat treatment at 145
o
C, for 6 s.
,Non-cooled storage at 20
o
C.
Recontamination after heat treatment (1 cfu serving
1
), non-cooled storage at 20
o
C.
**Stepwise cooling was assumed.
Situation cs1, heat treatment: 130
o
C, for 3 s (Caric and
Kalab 1993). Application of this heat treatment results in a
very high probability of having problems, PC= 291 for
Cl. botulinum type A and 225 for proteolytic type B.
The AV for Cl. botulinum was low, 10
2
cfu serving
1
, so
even with only 1 cfu serving
1
present, HC=log(1/10
2
) =
2. It is obvious that presence of the hazard and AV are
important for risk, and that a low PC can only be achieved
by a low OC value (by high inactivation).
o
C, for 6 s. Application
of this heat treatment results in a very low probability of
having problems (PC=o). Cl. botulinum is completely
inactivated (SC<20), so heat treatment is risk-deter-
mining. The inactivation is, however, so overwhelmingly
large that it needs no further study. In this case it would
be interesting to study recontamination more accurately,
since this will probably completely determine risk (Table
3).
Situation cs3, storage 20
o
C (compared with 10
o
C), for
8 weeks. The simulation results in very low probabilities
for Cl. botulinum type B, PC=935. If NrAV, as in
this situation, then HC=0, so PC=OCHC=OC.
Consequently, inactivation is an important risk-determining
phenomenon in this situation. If organisms remain in the
product after inactivation (theoretically one in 10
935
pro-
ducts), or recontamination occurs, the organisms are well
able to grow at this temperature (SC=10, the maximum
value of SC). It is therefore also sensible to study growth
during storage and (re)contamination more accurately
(Table 3). Other phenomena can be omitted.
o
C, for 2 s, recontami-
nation after inactivation and non-cooled storage at 20
o
C.
As expected, very high probabilities for the hazards (PC=
0) were predicted by simulation of this situation.
Recontamination was assumed to occur, so OC=0 in this
situation. Heat treatment is therefore not relevant for risk.
Prevention of recontamination clearly is important, espe-
cially in case of non-cooled storage (SC
storage
= 10).
Storage and prevalence of recontamination are risk-deter-
mining phenomena in this scenario that need to be studied
more accurately.
Heat treatment appeared to be risk-determining in sev-
eral of the previous situations, provided that recontamina-
tion does not occur afterwards. If recontamination does
occur, however, it is an important determinant of risk,
especially in case of non-cooled storage. As an example,
level 2 risk assessment will be performed for situation cs3
for Cl. botulinum type B proteolytic as this is the most heat
resistant of the two hazards under study.
Level 2: Exposure assessment situation cs3, cheese
spread. Heat treatment, prevalence of (re)contamination
and growth during storage are the risk-determining phe-
nomena for situation cs3 that need further study on this
level.
Inactivation of Cl. botulinum type B proteolytic was stu-
died by the exponential model as the primary inactivation
model. Tailing was not taken into account because there
was no indication in the literature of deviations from log-
linearity during heat inactivation at 145
o
C.
As in level 1, the worst-case value k
145
#=671 min
1
was used and the log reduction was estimated to be 961.
In level 2, inactivation was estimated using both k
145
# and
the point estimate k
145
. The point estimate k
145
was calcu-
lated as k
145
=ln(10)/D
145
(equation 1), where D
145
was
estimated from the linear regression line of D-values given
by ICMSF (1996). D
145
=10510
3
min, so k
145
=21910
3
min
1
, and the log reduction >>20. Considering the fact
that both log reductions of 961 (by the worst-case value)
and of >> 20 are very high, it was decided to consider
the inactivation complete (Table 6, row 2). Because of this
complete inactivation, it is not necessary to study preva-
lence of contamination more accurately.
Growth during storage was estimated assuming the three
product characteristics: temperature = 20
o
C, pH=60,
water activity (a
w
) =0975. The following primary models
were compared: the lag-exponential model (Van Gerwen
and Zwietering 1998), the Baranyi model (Baranyi and
Roberts 1994), and the reparameterized Gompertz model
(Zwietering et al. 1990). The secondary growth models that
were compared are: the gamma model (Zwietering et al.
1996) and the CTPM (Rosso et al. 1995). The comparisons
showed that there were no relevant differences between
these models; they all estimated growth to be very high (N
= N
max
= 10
10
).
The Central Composite Model and the Extended Total
Model of Ter Steeg and Cuppers (1995) were used to com-
pute the time to a 100-fold increase (t
100
) of proteolytic Cl.
botulinum in cheese spread. The models predicted t
100
=17
and t
100
=3 weeks, respectively. Evidently, this results in
too much growth in 8 weeks of storage.
In this case, the USDA Pathogen Modelling Program
version 50 could not be used, since a
w
=0975 was outside
the model limits. The Tanaka model as described by Ter
Steeg and Cuppers (1995) could not be used either, since
this model was only applicable for 30
o
C.
Based on the above results it must be concluded that it
is likely that substantial growth occurs during 8 weeks of
storage at 20
o
C. Using the simplest models available: the
exponential and gamma models, growth was estimated to
be N/N
0
=10
10.
The actual value of N can be neglected,
since growth is too high anyway. The exposure was there-
fore estimated as e =10
10
cfu serving
1
(Table 6, row 5).
SIEFE informs the user that it is important to realize
that the presence of various specic growth-inhibiting sub-
stances is not included in most growth models and conse-
quently growth estimates are fail safe.
The prevalence of recontamination is an important risk-
determining factor in this example. If recontamination
occurs after complete inactivation, Cl. botulinum type B
proteolytic is well able to grow in the cheese spread used in
this example. Considering the good safety record of pro-
cessed cheese (Wagenaar and Dack 1958; Collins-
Thompson and Wood 1993), it is assumed that prevalence
is very low, but quantitative estimation of prevalence (P
e
)
was not possible with the available information. For that
reason, risk was estimated with P
e
ranging from 10
20
to 1
(Table 6, row 4).
Level 2: Hazard characterization situation cs3, cheese
spread. The probability of infection, illness, or mortality
(P(i|e)) can be estimated by doseresponse parameters for
the hazard. In this example, however, no doseresponse
data for Cl. botulinum type B proteolytic were available
besides the AV of 10
2
cfu serving
1
.
Since the estimated amount of cfu serving
1
(e =10
10
) is
much higher than the AV, it was assumed that all servings
contain toxin if they are contaminated and P(i|e) for intox-
ication was estimated to be 1 (Table 6, row 7).
Intoxication was assumed to denitely result in illness,
so P(ill|i) =1. If ill, the probability of dying was estimated
as the mortality ratio; P(d|ill) =015 (Hauschild 1993).
Severity (S) was assumed to be one. The qualitative
categories presented in the CAST report (1994) indicated
severe problems, for week to months.
Level 2: Risk characterization situation cs3, cheese
spread. The cheese used in this example is a hypothetical
cheese, since its characteristics were based on the literature.
Consequently, it was not known how many jars of the
cheese spread are sold per year in a certain population, for
instance in The Netherlands. For that reason, n was
assumed to vary between 10
6
and 10
9
servings per year.
Risk as a function of P
e
and n is shown in Fig. 2.
Relevant assumptions for estimation of risk are shown in
Table 6. For example, if prevalence is 10
9
(one in 10
9
jars
contains 1 cfu), and 10
8
servings are consumed per year,
the probability that one or more people die in a year in
The Netherlands as a result of consuming cheese spread is
149 10
2
(Fig. 2). This probability can be interpreted as
one or more people dying of Cl. botulinum intoxication by
this product every 70 years.
The consumer risk of dying from eating one serving of
cheese spread is P
e
P(i|e)P(ill|i)P(d|ill)S=P
e
1 1
015 1. This shows that risk is totally determined by pre-
valence, and that really low frequencies (unmeasurable)
should be achieved to control safety by frequency.
Recommendations for study in a third level of detail. Risk
was estimated assuming that Cl. botulinum type B proteoly-
tic is well able to grow in the product. Since growth esti-
mates are probably worst-case, it is sensible to check
growth experimentally by challenge testing in level 3.
The quantitative estimation of risk appeared to rely to a
large extent on the prevalence of recontamination, P
e
, and
the amount of servings consumed, n. Risk estimates should
therefore be based on a more accurate estimation of these
Table6 Relevant assumptions for estimation of risk for Clostridium botulinum type B proteolytic in cheese spread
Assumption Parameter Ill Mortality
1. The production process is shown in Table 5
2. Complete inactivation during heat treatment
3. Recontamination of the product after inactivation
4. Prevalence of recontamination ranges from P
e
=10
20
to P
e
=1 P
e
10
20
1 10
20
1
5. Very high growth after recontamination, resulting in an estimated exposure;
e =10
10
cfu per serving
e 10
10
10
10
6. The organism is very well able to grow, and therefore also able to form toxin
7. Since (e =10
10
) >>(AV=10
2
), it was assumed that every serving contains signicant
amounts of toxin, so the probability of intoxication; P(i|e)
tox
=1
P(i|e)
tox
1 1
8. Illness will denitely occur after consumption; it was assumed that P(ill|i) =1 P(ill|i) 1 1
9. The value for the mortality ratio, given illness; P(d|ill) =015 P(d|ill) 015
10. Severity was estimated as S=1 S 1 1
11. Amount of servings consumed per year in The Netherlands varies between n =10
6
and n =10
9
n 10
6
10
9
10
6
10
9
12. Risk = 1(1-P
e
P(i|e)P(ill|i)P(d|ill)S)
n
Risk Fig. 2 Fig. 2
parameters. n should normally be simple to estimate in
practice, since sales data are generally known for most pro-
ducts per time period. Variations in n can be included in
the risk assessment by describing n as a stochastic para-
meter. However, given the accuracy of prevalence estimates
this probably does not largely improve the risk estimate.
P
e
and variations in P
e
are more difcult to estimate,
since no specic quantitative data on P
e
are available, and
very low frequencies are practically impossible to measure.
Regarding food safety control, it is a better strategy to
focus on the design of a cheese spread composition that
does not allow growth of Cl. botulinum or on measures that
prevent recontamination, rather than to focus on accurate
quantitative estimation of the prevalence of recontamina-
tion.
DI SCUSSI ON
This paper describes a system (SIEFE) for microbial quan-
titative risk assessment for food products and production
processes. The system is based on an approach to micro-
biological risk assessment that is different to other
approaches by considering various levels of detail in the
process of assessing risks. This stepwise approach avoids
complexity and allows one to focus on the main problems.
The rst, rough level of detail results in a rst estimate of
risk and identies risk-determining phenomena. It was
shown that the risk-determining phenomena related to the
normal process can be used to nd pertinent failure scenar-
ios and helps assure that no relevant risk-determining phe-
nomena are overlooked. The rst level of detail uses the
relatively simple characteristic numbers SC, OC, HC and
PC for identication of the risk-determining phenomena.
The opportunity for hazard and risk ranking in the rst
level of detail was not shown in this paper. If risks were
assessed for various hazards, they could have been ranked
according to their relevance for food safety by the PC
values. The simplicity of the characteristic numbers makes
them easy to understand. They provide clear quantitative
insight into production processes which supports manage-
ment decisions on control strategies.
The second level of detail studied the risk-determining
phenomena more accurately. Quantitative data from various
references in the literature were compared in addition to
general and/or specic models for estimation of growth
and inactivation. In this way, the problem could be studied
from several points of view, and the risk could be estimated
on a broad basis. The example showed that quantitative
estimates of risk-determining phenomena are not always
available either because of a lack of specic quantitative
data or because of a lack of models and model parameters.
It was shown that this shortcoming does not necessarily
prevent risk estimation. Worst-case estimates were shown
to be sufcient for some risk-determining phenomena,
whereas other risk-determining phenomena were described
by a range of values. For more accurate risk assessments,
the worst-case or ranging estimates could be studied in a
third level of detail by stochastic description, by experi-
ments, or by a more extensive literature search.
SIEFE is interactive and uses several information
sources. Expert and literature knowledge have been cap-
tured in knowledge rules. Due to the clear denitions of
0
0
log(P(e))
l
o

g
(
R
i
s
k
)
13
4
3
2
1
11 9 7 5 3 1
Fig. 2 log(Risk) of having one or more problems per year as a function of the logarithm of the prevalence of recontamination, log(P
e
), for
Clostridium botulinum type B proteolytic in cheese spread. Log(Risk) for death (mortality ratio P(d|ill) =015) is represented by (&) for n
=10
6
; (*) for n =10
7
; (~) for n =10
8
; (!) for n =10
9
. Log(Risk) for illness is shown by (&) for n =10
6
; and (!) for n =10
9
. The
dashed lines represent log(Consumer risk) for illness (&), and for death (&), for consumption of one serving of cheese spread
the knowledge rules they can be scrutinized and changed
when necessary. This supports the user in critically using
the system thereby assessing most risks realistically. SIEFE
can best be used by experienced microbiologists, as they
are able to make the best use of the knowledge rules and
can best interpret the system's estimates critically. With
these advantages, and the fact that SIEFE focuses on pro-
ducts and their production processes, the system can be
valuable as a component of a HACCP team. In this role it
can be used proactively to support decisions on optimiza-
tion of production processes according to a certain risk.
By rst selecting the quantitatively most important phe-
nomena through SIEFE, quantitatively negligible aspects
can be omitted based on explicit reasoning. Only for the
risk-determining phenomena a high level of detail and sto-
chastic assumptions have to be made. So, no resources are
wasted in looking for less relevant parameters and stochas-
tic data. By pinning down the problem, risk-determining
variability and uncertainty can be revealed and handled
efciently.
ACKNOWLEDGEMENTS
We would like to thank Michiel Steffelaar and Alexander
Korf for their contributions to SIEFE, and Geke
Naaktgeboren for her useful comments on the example.
We are also grateful to Frans Rombouts, Arie Havelaar,
Peter Teunis, Jaap Jansen, Matthe van den Broek, Hugo de
Sitter, Jan Smelt, Serve Notermans and Taco Wijtzes for
valuable discussions and comments, and to Michael Smith
and Leon Gorris for reading the manuscript.
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