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Food Control 21 (2010) 319–330

Contents lists available at ScienceDirect

Food Control
journal homepage: www.elsevier.com/locate/foodcont

A swift Quantitative Microbiological Risk Assessment (sQMRA) tool


Eric G. Evers *, Jurgen E. Chardon
National Institute for Public Health and the Environment, P.O. Box 1, 3720 BA Bilthoven, The Netherlands

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

Article history: Classical full-scale QMRA is a valuable method to assess the effects of control measures on the public
Received 19 December 2008 health risk of a pathogen–food product combination. However, development of these QMRA models is
Received in revised form 11 June 2009 time consuming, data needs are substantial and it requires extensive modeling expertise. We therefore
Accepted 16 June 2009
developed a simplified QMRA model especially aimed at comparing the risk of pathogen–food product
combinations. The swift Quantitative Microbiological Risk Assessment (sQMRA) – tool is implemented
in Microsoft Excel. Special attention is given to make the sQMRA tool insightful, for educational purposes.
Keywords:
Like in full-scale QMRA, pathogen numbers are followed through the food chain, which in this case starts
Risk assessment
QMRA
at retail and ends with the number of human cases of illness. The model is deterministic and includes
Relative risk cross-contamination and preparation (heating) in the kitchen and a dose–response relationship. The gen-
Mathematical model eral setup of the sQMRA tool consists of consecutive questions for values of each of the 11 parameters,
Campylobacter always followed by intermediate model output broken down into categories of contamination, cross-con-
Salmonella tamination and preparation. In a separate sheet, model input and output are summarized and exposure as
well as cases are attributed to the distinguished categories. As a relative risk measure, intermediate and
final model outputs are always compared with results from a full-scale QMRA of Campylobacter on
chicken fillet. Example calculations with the sQMRA-tool were done for all combinations of Campylobac-
ter spp. and Salmonella spp. with chicken fillet, filet americain (raw minced beef with mayonnaise) and
table eggs. Data availability appeared to be partly poor. The predicted risk was highest for Salmonella
spp. in table eggs and Campylobacter spp. in chicken fillet. Results indicate that the sQMRA-tool is useful
for quickly obtaining relative risk estimates of pathogen–food combinations. It can thus serve as a guide
for selection of combinations for applying full-scale QMRA, or for risk management – by facilitating the
translation of the results of trend analysis or of a specific research project into terms of risk.
Ó 2009 Elsevier Ltd. All rights reserved.

1. Introduction simplified model will suffice and be preferred, where it must be


noted that the ability to estimate the effect of intervention mea-
A full scale quantitative microbiological risk assessment (QMRA) sures will be reduced. These applications include:
describes the propagation of a pathogenic micro-organism from
farm via slaughter and retail to the consumer’s home, using math- – Pre-selection of a pathogen–food product combination: when
ematical modeling techniques. In the last decade several studies considering a range of pathogens or food products, a simplified
covering the whole or part of this food chain were performed (e.g. model can select the most relevant pathogen–food combination
Cassin, Lammerding, Todd, Ross, & McColl, 1998; Nauta, Evers, Tak- to be analyzed by a full-scale QMRA.
umi, & Havelaar, 2001; Rosenquist, Nielsen, Sommer, Norrung, & – Many public health related National Authorities have large dat-
Christensen, 2003; Schlundt, 2000). The estimated exposure of con- abases of measurements of pathogens along the food chain,
sumers to a pathogen is input for the dose–response relationship which are constantly supplemented with new measurements.
which results in an estimate of the number of human cases. More Using a simplified technique, a continuous rough trend analysis
importantly, a QMRA model is capable of estimating the public in terms of public health risk can be performed.
health effect of interventions measures in terms of the reduction – The results of a research project can quickly be interpreted in
of this number. When economics is taken into account, even a terms of public health risk, given that pathogen concentrations
cost-utility analysis can be performed (Havelaar et al., 2007). are determined.
A disadvantage of the valuable QMRA technique is that it is – Education: a simplified model is better accessible and under-
time-consuming and expensive. For a number of applications a standable for scientists that are new in the QMRA research area
or are not very mathematically inclined. Also, QMRA under-
standing by policy makers that have to decide on the implemen-
* Corresponding author. Tel.: +31 30 274 41 49; fax: +31 30 274 44 34.
E-mail address: eric.evers@rivm.nl (E.G. Evers). tation of intervention measures will be enlarged.

0956-7135/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved.
doi:10.1016/j.foodcont.2009.06.013
320 E.G. Evers, J.E. Chardon / Food Control 21 (2010) 319–330

It must be stressed that when applying a simplified model, the sheet parameter values are inserted, and calculation results are
resulting public health risk in terms of numbers of human cases presented at all intermediate points and at the end point. These in-
must be interpreted in a relative sense, comparing it with a refer- clude the resulting risk and intermediate results such as the num-
ence study or with other simplified pathogen–product calculations. ber of portions and number of cfu (colony forming units) per
The absolute values are not very reliable given that this is usually portion. In the results sheet, we present (1) a list of input parame-
even not the case for full-scale QMRAs. ter values, (2) attribution of exposure and of cases to the different
Previously, a number of simplified QMRA methods have been transmission routes and (3) the relative risk at several intermedi-
developed by others. A good approach was presented by Ross ate points and the end point (no. of human cases) in the
and Sumner (2002), who implemented their model in an accessible calculation.
Excel spread sheet, however, they used categories with inevitable The sQMRA model and tool will be described stepwise below,
arbitrary weighting factors and a somewhat artificial risk ranking using screenshots of the tool showing a fictitious example together
scale. McNab (2003) used data on exposure and on its impact from with the corresponding mathematical (left side of page) and Excel
farm to consumer in a MS Access application. Both did not include equations (right side). From the preparation step onwards, only
concentrations or numbers of pathogens, which is a necessary in- one example Excel equation will be given for each set of mathe-
put of the dose–response relationship and also, numbers of patho- matical equations. Thereafter, example calculations will be given
gens are more important for public health risk than prevalences on Campylobacter and Salmonella in/on chicken fillet, filet americ-
(Nauta & Havelaar, 2008; Rosenquist et al., 2003). Van Gerwen, ain and table eggs. Filet americain is a bread spread which contains
Te Giffel, Van’t Riet, Beumer and Zwietering (2000) describe a raw minced beef as the main ingredient (70%), together with a
framework with a stepwise approach including more detail when mayonnaise-based sauce and spices. It is sometimes called steak
a transmission route proves to be significant. No predefined model tartare.
equations are used; these are chosen ad hoc. Teunis, Medema, Kru- The tool is implemented in Microsoft Excel XP. Only built-in
idenier, and Havelaar (1997) describe a model for exposure to functionality and no VBA or macro code is used. Excel cells for in-
pathogens via drinking water and the risk of infection, which can put parameters have automatic data validation: only quantitative,
be relatively simple as the drinking water chain is more uniform positive values are accepted and percentages have to be between
than the food chain. 0% and 100%. All other cells in the tool are write protected. The
The objective of this paper is to present a simplified QMRA sQMRA tool can be obtained by sending an e-mail to the corre-
method which is implemented in Excel, the swift Quantitative sponding author.
Microbiological Risk Assessment (sQMRA)-tool. The sQMRA tool in-
cludes numbers of pathogens and uses predefined equations that
2.2. Model
take the inherent variation in processing in the food chain into ac-
count. Relative risk (compared with a reference value) is given for
2.2.1. Symbols
five model outputs, including the number of human cases. Special
attention is given to make the sQMRA tool insightful, for educa- A list of input parameters of the model can be found in Fig. 7,
which depicts the results sheet of the sQMRA-tool. Question num-
tional purposes. The sQMRA method builds on previous work by
Evers, van der Fels-Klerx, Nauta, Schijven, and Havelaar (2004, ber in the tool, parameter symbol, description and value are gi-
ven. Most used symbols are N for number of portions, S for
2008) in which human exposure for Campylobacter is estimated
for 31 transmission routes, including food, direct contact and water. subdivision of these numbers into fractions of categories of por-
tions, D for the dose (no. of cfu) of a pathogen and F for the frac-
Extensions include explicit modeling of food portions, cross-con-
tamination and preparation, and the addition of effect modeling. tion of these numbers that cross-contaminate or survive. Note
that (for educational purposes) fractions are presented as percent-
The sQMRA method is an example of comparative risk assess-
ment, a new approach in the set of methods used for human illness ages in the tool, whereas all actual calculations are done with
fractions.
attribution, which include microbial subtyping, epidemiological
approaches (study of sporadic infections and outbreaks), interven- Typically the subscripts of symbols consists of two parts sepa-
rated by a ‘/’. The first part describes the phase or process of the
tion studies and expert elicitation approaches (Pires et al., 2009). In
risk assessment: r for retail, cc for cross-contamination, pr for prep-
order to gain insight in the usefulness of the sQMRA method, cal-
aration, ing for ingestion, inf for infection, and ill for illness. The sec-
culations were done for Campylobacter and Salmonella in chicken
ond part describes portions categories: contamination at retail (+)
fillet, filet americain and table eggs. The results are presented here
or not (), occurrence of cross-contamination (cc+) or not (cc) or
to illustrate the method.
not specified (ccx) and the preparation method: prd is done, prh is
halfdone, prr is raw and pry is not specified. For example,
2. Materials and methods Npr/+,cc,prd stands for the number of portions after preparation that
were contaminated at retail, did not cause cross-contamination
2.1. General and were prepared done. In particular for S, the second part of
the subscript can be a phase or process as well, in which case S
The sQMRA model is a simple risk assessment model in which stands for a subdivision within a previous phase/process. For
the propagation of a pathogen is followed in the exposure assess- example, e.g. Scc/r stands for the percentage of portions that
ment part, which starts at the retail phase. Processes considered cross-contaminate the environment given that they are contami-
are cross-contamination and preparation (=heating, in the sense nated in retail.
of cooking, frying, etc. of the product) in the kitchen, which leads
to seven categories of portions. The resulting exposure is input
for the effect modeling part, which has risk in terms of infection 2.2.2. Title and case definition (Fig. 1)
and illness, per portion as well as at the population level, as output. Characteristics of a risk assessment have to be entered in the
The model is deterministic and does not include uncertainty and case definition box. These data are not used in the sQMRA calcula-
variability. tions, but have an administrative purpose: they are repeated in the
The sQMRA-tool is implemented in a spread sheet application results sheet as identification of the calculation results presented
and is divided into a model sheet and a results sheet. In the model there.
E.G. Evers, J.E. Chardon / Food Control 21 (2010) 319–330 321

size in retail differs from portion size at the moment of


consumption.
The dose per portion (no. of cfu) for contaminated and uncon-
taminated portions, Dr/+ (cell J46) and Dr/ (Cell J47), equals
Dr=þ ¼ C r=þ M J46 ¼ G40  G24
Dr= ¼ 0 J47 ¼ 0
where Cr/+ (Question 4) is the average concentration of the pathogen
in contaminated portions (cfu/g). Again it must be noted that in
principle this average includes the concentrations in false negative
portions. From here on, we will concentrate on contaminated
portions.
The total dose Dtotr/+ (no. of cfu; cell K46) stands for the sum of
Fig. 1. Case definition part of the Model sheet of the sQMRA tool.
the number of cfu over all portions, which is related to the case
definition (Fig. 1). It equals:
2.2.3. Consumption data (Fig. 2) Dtotr=þ ¼ Dr=þ Nr=þ K46 ¼ J46  I46
Consumption data necessary for the risk calculations are the
number of portions N (Question 1) given the case definition
2.2.5. Cross-contamination (Fig. 3)
(Fig. 1) and the average size of the portion M in grams (Question
It is assumed that a certain part of the portions causes cross-
2). Ideally these variables are obtained from a national food con-
contamination in the kitchen prior to heating and the other part
sumption survey.
does not. The fractions Scc/+,cc+ (cell H64) and numbers Ncc/+,cc+ (cell
I64) of contaminated portions causing cross-contamination can be
2.2.4. Retail (Fig. 2)
calculated as follows:
The number of contaminated Nr/+ (cell I35) and uncontaminated
portions Nr/ (cell I36) in retail equals Scc=þ;ccþ ¼ Sr=þ Scc=r H64 ¼ H35  G54
Nr=þ ¼ NSr=þ I35 ¼ G22  H35 Ncc=þ;ccþ ¼ Nr=þ Scc=r I64 ¼ I35  G54
Nr= ¼ Nð1  Sr=þ Þ ¼ NSr= I36 ¼ G22  H36 where Scc/r (Question 5) is the fraction of the portions contaminating
the environment given that the portion is contaminated. Analo-
where Sr/+ (Question 3; cell H35) and Sr/ = 1  Sr/+ (cell H36) are the
gously, the fractions Scc/+,cc (cell H65) and numbers Ncc/+,cc (cell
fractions of contaminated and uncontaminated portions at retail,
I65) of contaminated portions not causing cross-contamination are
respectively.
It must be noted that Sr/+ includes the false negatives (non de- Scc=þ;cc ¼ Sr=þ ð1  Scc=r Þ H65 ¼ H35  ð1  G54Þ
tects), so in general it will be higher than the value that is e.g. ob- Ncc=þ;cc ¼ Nr=þ ð1  Scc=r Þ I65 ¼ I35  ð1  G54Þ
tained from national monitoring programs. Not including a
correction for false negatives will lead to an underestimation of Further, it is assumed that cross-contamination is a two-step
the risk, however, the calculation results will still be useful when process. First, prior to food preparation, a certain part of the patho-
one is aware of this and taking into account the fact that the ne- gens on the portion Fcc (Question 6) transfers to the environment.
glected concentrations will be relatively low. The unit ‘portion’ is This environment can e.g. be kitchen equipment or the hands of
used at this phase, although it can be a virtual concept when sale the person preparing the meal. When cross-contamination occurs,

Fig. 2. Consumption data and Retail part of the Model sheet of the sQMRA tool.
322 E.G. Evers, J.E. Chardon / Food Control 21 (2010) 319–330

Fig. 3. Cross-contamination part of the Model sheet of the sQMRA tool.

the dose that remains in the portion Dcc/+,cc+ (no. of cfu; cell J64) In case of cross-contamination, the dose in the portion that is
and the dose that ends up in the environment Decc/+,cc+ (no. of eventually ingested by the consumer Ding/+,cc+,pry (no. of cfu/por-
cfu; cell K64) are: tion; cells L100–L102) consists of the dose remaining after heating
and the dose from cross-contamination and equals
Dcc=þ;ccþ ¼ Dr=þ ð1  F cc Þ J64 ¼ J46  ð1  G59Þ
Decc=þ;ccþ ¼ Dr=þ F cc K64 ¼ J46  G59 Ding=þ;ccþ;pry ¼ Dpr=þ;ccþ;pry þ Deicc=þ;ccþ e:g: L100 ¼ J100 þ K100

When there is no cross-contamination, the dose in the portion When there is no cross-contamination, the dose ingested by the
Dcc/+,cc (no. of cfu; cell J65) does not change and the environment consumer Ding/+,cc,pry (no. of cfu/portion; cells L103–L105) is sim-
is not contaminated (cell K65). ply equal to the dose remaining after heating:

Dcc=þ;cc ¼ Dr=þ J65 ¼ J46 Ding=þ;cc;pry ¼ Dpr=þ;cc;pry e:g: L103 ¼ J103


Decc=þ;cc ¼ 0 K65 ¼ 0 The total dose at the moment of ingestion Dtoting/+,ccx,pry (no. of cfu;
cells M100–M105) corresponding to the case definition becomes
Second, a part (Fei; Question 7) of the pathogens in the environ-
ment transfers back to the portion or another part of the meal after Dtoting=þ;ccx;pry ¼ Ding=þ;ccx;pry Npr=þ;ccx;pry e:g: M100 ¼ L100  I100
heating, if any, and will be ingested by the consumer. The size of and the sum of Dtoting/+,ccx,pry (no. of cfu; cell M107) for the six con-
this dose Deicc/+,cc+ (no. of cfu; cell K76) is taminated categories is the total number of pathogens ingested by
Deicc=þ;ccþ ¼ Decc=þ;ccþ F ei K76 ¼ K64  G71 the considered population.

The rest of the dose Decc/+,cc+, Delcc/+,cc+ (no. of cfu; cell L76), remains 2.2.7. Infection and illness (Fig. 5)
in the environment: The probability of infection for an ingested dose of pathogens,
Delcc=þ;ccþ ¼ Decc=þ;ccþ ð1  F ei Þ L76 ¼ K64  ð1  G71Þ Pinf/+,ccx,pry (cells I122–I127), is calculated with the exponential
dose–response relationship:

2.2.6. Preparation (Fig. 4) Pinf =þ;ccx;pry ¼ 1  erDing=þ;ccx;pry e:g: I122 ¼ 1  er  H122
We distinguish three categories of heating of the portion: done,
where r is the probability of infection for one single pathogen (Haas,
half-done and raw (=no heating). The fractions Spr/+,ccx,pry (cells
1983). It can simply be derived that
H100–H105) and numbers Npr/+,ccx,pry (cells I100–I105) of contami-
nated portions that do (x = +) or do not (x = ) cause cross-contam- ln 2 ln 2
r¼ r¼
ination and are prepared done (y = d), half-done (y = h) or raw ID50 G112
(y = r) are calculated as follows: where the ID50 value (Question 10) is the dose per portion that
Spr=þ;ccx;pry ¼ Scc=þ;ccx Spry=cc e:g: H100 ¼ H64  G86 causes infection in half of the exposed population (Pinf = 0.5). In
the sQMRA tool the ID50 value is used as input, as this is a value
N pr=þ;ccx;pry ¼ Ncc=þ;ccx Spry=cc e:g: I100 ¼ I64  G86
that is better understandable for non-risk assessors and comes close
where Spry/cc (Question 8) is the fraction of the portions prepared to the often used concept of the infectious dose.
done, half-done or raw given that the portion is contaminated and It is assumed that the probability to get ill given infection (Pill/inf;
has caused cross-contamination or not. Question 11) is a fixed value, independent of the dose. So the prob-
The three heating categories are characterized by different frac- ability of illness per portion (Pill/+,ccx,pry; cells J122–J127) becomes:
tions survival of the pathogen: Fprd, Fprh and Fprr, respectively
Pill=þ;ccx;pry ¼ Pinf =þ;ccx;pry Pill= inf e:g: J122 ¼ I122  G117
(Question 9). The dose that remains in the portion after heating
Dpr/+,ccx,pry (no. of cfu/portion; cells J100–J105) equals The corresponding numbers of infections (Iinf/+,ccx,pry; cells L122–
L127) and cases (Iill/+,ccx,pry; cells M122–M127) given the case defini-
Dpr=þ;ccx;pry ¼ Dcc=þ;ccx F pry e:g: J100 ¼ J64  G94 tion are
E.G. Evers, J.E. Chardon / Food Control 21 (2010) 319–330 323

Fig. 4. Preparation part of the Model sheet of the sQMRA tool.

Fig. 5. Infection and illness part of the Model sheet of the sQMRA tool.

Iinf =þ;ccx;pry ¼ Pinf =þ;ccx;pry Npr=þ;ccx;pry e:g: L122 ¼ I122  K122 routes at the population level. The calculation of absolute expo-
Iill=þ;ccx;pry ¼ Pill=þ;ccx;pry Npr=þ;ccx;pry e:g: M122 ¼ J122  K122 sures (no. of cfu) for the different transmission routes is presented
in Table 1. It must be noted that the cross-contamination route in-
The sum of these numbers over the categories gives the total num- cludes all cfu’s that are ingested via cross-contamination (i.e., the
ber of infections and cases (cells L130 and M130). route via the environment and back), regardless of the way of prep-
aration, whereas the three preparation routes refer to ingestion of
2.2.8. Model overview cfu’s that stayed in the portion and survived the heating (if any).
A model overview is given in Fig. 6. The attribution of exposure (the relative importance) is calculated
by dividing the absolute exposures (Table 1) by the total exposure
2.3. Model input and output (RESULTS – sheet; Fig. 7) (=the sum of the exposures given in Table 1, or cell M107 in the
MODEL sheet). The calculations are located in a separate section
The intention of the RESULTS sheet is to present the most essen- of the sheet (AB50–AC56) (not shown). The result is given in cells
tial model input (input parameters) and output (exposure, effect, K17–M22 and in the corresponding pie chart (cells K6–M16).
relative risk) in a concise format.
2.3.3. Attribution of effect
2.3.1. Input parameters
For attribution of cases a concept is used which is analogous to
The section ‘input parameters’ starts with repeating the case
the Population Attributable Risk (PAR) in public health epidemiol-
definition (cells D6–G10; see also Fig. 1). Then, all input parameter
ogy studies. We estimate the number of cases when a transmission
values from the MODEL sheet are presented in a list, including
route is switched off (Iill/attr) and determine the decrease in number
question number, parameter symbol, a shortened version of the
of cases relative to the base scenario with best estimates for all 11
question and the inserted value (cells D11–G28). The time point
input parameters (Iill/base; cell M130 in the MODEL sheet). In
of calculation is captured with a time stamp (cell D30–F30).
formula:

2.3.2. Attribution of exposure


Iill=base  Iill=attr
Attribution of exposure is defined here as the relative impor- attribution of cases ¼
Iill=base
tance of the end point of exposure for the different transmission
324 E.G. Evers, J.E. Chardon / Food Control 21 (2010) 319–330

Table 2
Retail Scenarios used to calculate attribution of cases. For explanation of symbols see Fig. 7.

Transmission route Scenario for attribution Equivalent MODEL


Sr/+ Excel sheet cell values
Cross-contamination Scc/r = 0 G54 = 0
Scc/r Prepared done Fprd = 0 G94 = 0
Prepared half-done Fprh = 0 G95 = 0
(1-Fcc) Fcc Prepared raw Fprr = 0 G96 = 0

Uncontaminated Preparation Cross-contamination


Spry/cc Due to the non-linearity of the dose–response relationship, the
Fei attribution values for the four transmission routes will usually not
Fpry add up to 1. Table 2 gives the scenarios used for switching off
transmission routes. The calculations are located in a separate sec-
tion of the sheet (AB38–AV47) (not shown). The result is given in
cells O17–S22 and in the corresponding bar chart (cells O6–S16).
Exposure
2.3.4. Relative risk
Pinf/+,ccx,pry Intermediate and end-point model outputs are compared with
modeling results from the extensive CARMA (Campylobacter Risk
Management and Assessment) study (Nauta, Jacobs-Reitsma,
Infection
Evers, van Pelt, & Havelaar, 2005; Nauta, Jacobs-Reitsma, & Have-
Pill/inf laar, 2007) to put the model outputs in perspective (Table 3). The
CARMA study is a quantitative microbiological risk assessment
(QMRA) study on Campylobacter on chicken fillet. The relative risk
Illness is defined as the quotient of model outputs and CARMA values. The
CARMA estimations of no. of cfu were kindly calculated by Maarten
Fig. 6. Outline of the sQMRA model. Dotted line: uncontaminated portions. Solid Nauta specially for this application, being non-standard output of
line: contaminated (or all) portions. Long dashed line: cross-contaminated patho-
the CARMA model. The sQMRA and CARMA estimates and the rel-
gens corresponding to contaminated portions. Short dashed line: effect of a
consumed portion. ative risks are given in cells K27–S33.

Fig. 7. Results sheet of the sQMRA tool.

Table 1
Calculation of exposure via the distinguished transmission routes. Deicc/+,cc+ is the dose of pathogens that transfers back from the environment and will be ingested by the
consumer (no. of cfu/portion); Npr/+,ccx,pry are numbers of contaminated portions that do (x = +) or do not (x = ) cause cross-contamination and are prepared done (y = d), half-
done (y = h) or raw (y = r); Dpr/+,ccx,pry is the dose that remains in the portion after heating using the same subscript convention (no. of cfu/portion).

Transmission route Model formula (total no. of cfu) for exposure Equivalent MODEL Excel sheet equations
P
Cross-contamination Deicc=þ;ccþ y N pr=þ;ccþ;pry K100  (I100 + I101 + I102)
P
Prepared done N D I100  J100 + I103  J103
Px pr=þ;ccx;prd pr=þ;ccx;prd
Prepared half-done N D I101  J101 + I104  J104
Px pr=þ;ccx;prh pr=þ;ccx;prh
Prepared raw x N pr=þ;ccx;prr Dpr=þ;ccx;prr I102  J102 + I105  J105
E.G. Evers, J.E. Chardon / Food Control 21 (2010) 319–330 325

Table 3 pathogen–food product combinations are Campylobacter – chicken


Model outputs and corresponding CARMA values used to calculate relative risk fillet and Salmonella – table eggs. Looking at the intermediate steps
values. CARMA stands for Campylobacter Risk Management and Assessment (Nauta
et al., 2007).
shown in Table 7, all pathogen–product combinations start at a
higher number of portions consumed than the reference value
Model output Equivalent MODEL CARMA value (QMRA Campylobacter chicken fillet, Nauta et al., 2007), whereas
Excel sheet cells
Symbol Explanation the percentages all decrease to ‘contaminated portions’ and de-
N Portions consumed G22 8.5E7 portions crease further to ‘total number of cfu’s before kitchen’. This is of
Nr/+ Contaminated portions I35 3.3E7 portions course due to lower prevalence and concentration values com-
(at retail) consumed pared to the reference study.
Dtotr/+ Total number of cfu’s K46 7.0E10 cfu
Towards the next step, ‘total number of cfu’s after kitchen’, the
before kitchen
P behavior differs between pathogen–product combinations. For
x;y Dtot ing=þ;ccx;pry Total number of cfu’s M107 6.1E6 cfu
after kitchen chicken fillet (Campylobacter and Salmonella), the percentage re-
P
x;y Iill=þ;ccx;pry Number of people ill M130 1.2E4 cases mains at the same level. This will be explained below (sQMRA
vs. QMRA); we note here already that in sQMRA, as in the refer-
ence study, transmission is only via cross-contamination (see val-
2.4. Data for example calculations ues of Spry/cc and Fpry in Tables 4–6). For filet americain
(Campylobacter and Salmonella), the percentage increases, which
Data for calculations of Campylobacter and Salmonella in/on is due to the fact that there is no loss either through cross-con-
chicken fillet, filet americain and table eggs were obtained from tamination or through preparation (see values of Scc/r, Spry/cc, and
scientific papers, reports, databases, personal communications or Fpry). For Salmonella in table eggs, the percentage also increases,
estimated by the authors. The parameter values are shown in the mainly due to the relative importance of transmission via the
Tables 4–6 and the clarification of data sources and further expla- preparation route (see values of Scc/r, Fcc, Fei, Spry/cc, and Fpry). For
nation is given in Appendix A. all pathogen–product combinations, the percentage decreases
again in the last step towards ‘number of people ill’, which is
3. Results due to the fact that an exponential dose–response model with a
fixed dose is used as opposed to the BetaPoisson model with a var-
The results of the sQMRA calculations are shown in Table 7 and iable dose in the reference study.
Fig. 8. Fig. 8 clearly shows that the only public health relevant Focusing on QMRA (Nauta et al., 2007) vs. sQMRA (this study)
Campylobacter chicken fillet, the five times higher value for por-
tions consumed in the latter is due to the fact that these are all
chicken fillet portions consumed and not only the number of com-
Table 4
Food product specific parameter values used for sQMRA example calculations. For bined portions of chicken and salad. This difference in presentation
explanation of symbols see Fig. 7. remains up until and including the point of total number of cfu’s
before kitchen. The sQMRA percentage decreases in the steps ‘con-
Number Input parameter Chicken fillet Filet americain Table eggs
taminated portions’ and ‘total number of cfu’s before kitchen’, due
1 N (no. of portions) 4.27  108 1.05  108 1.78  109
to lower values for prevalence and concentration in the sQMRA,
2 M (g) 100.3 40.0 44.3
5 Scc/r (%) 18.8 0 3.63 which are measured values as opposed to the calculated values
6 Fcc (%) 2.14 0 1.00 in the QMRA. At ‘total number of cfu’s after kitchen’ the above
7 Fei (%) 2.14 0 1.00 mentioned difference in presentation is gone, but the sQMRA is
8 Sprd/cc (%) 99.8 0 73.63 still higher. This will be due to the fact that in sQMRA the QMRA
Sprh/cc (%) 0.2 0 25.74
Sprr/cc (%) 0 100 0.63
cross-contamination model (which includes variability) is replaced
by a simple calculation with two equal point estimates for Fcc and
Fei, even though these are derived from the QMRA model. The de-
Table 5 crease in sQMRA percentage at ‘number of people ill’ is due to
Campylobacter (-food product) specific parameter values used for sQMRA example using different dose–response models and in- or excluding vari-
calculations. For explanation of symbols see Fig. 7.
ability, as referred to in the previous sentence.
Number Input parameter Chicken fillet Filet americain Table eggs Comparing pathogens within food products (Table 7), it appears
3 Sr/+ (%) 27.8 0.325 0 that the differences between pathogens arise through differences
4 Cr/+ (cfu/g) 14.2 0.04 0 in retail (Sr/+, C), and effect (ID50 and Pill/inf). Cross-contamination
9 Fprd (%) 0 0 0 and preparation in the kitchen does not differ between pathogens
Fprh (%) 0 0 0
as all parameter values are identical here (Fpry in table eggs differs,
Fprr (%) 100 100 100
but these are arbitrarily set for Campylobacter, being irrelevant at
10 ID50 (no. of cfu) 897
Sr/+ = 0). Comparing food products within pathogens, differences
11 Pill/inf (%) 33
between food products arise through differences in almost all
parameters related to portions consumed, retail, and cross-con-
Table 6 tamination and preparation in the kitchen. Parameter values for ef-
Salmonella (-food product) specific parameter values used for sQMRA example fect modeling are assumed to be identical.
calculations. For explanations of symbols see Fig. 7.
The uncertainty of the sQMRA model output depends on param-
Number Input parameter Chicken fillet Filet americain Table eggs eter uncertainty, the specific food product or pathogen–product
3 Sr/+ (%) 10 0.712 0.302 combination, and on the point of the model output (portions con-
4 Cr/+ (cfu/g) 1.8 0.04 15.5 sumed or number of people ill or a point in between). Parameter
9 Fprd (%) 0 0 4.08E4 uncertainty depends on data availability. Comparing the different
Fprh (%) 0 0 6.37
parameters, in general it can be stated that the values on consump-
Fprr (%) 100 100 100
tion and prevalence (N, M, Scc/r) have relatively good data availabil-
10 ID50 (no. of cfu) 9661 ity. The other parameters show varying data availability for this
11 Pill/inf (%) 100
specific set of pathogens and food products, where the availability
326 E.G. Evers, J.E. Chardon / Food Control 21 (2010) 319–330

Table 7
Results of the sQMRA calculations for the selected pathogen–food combinations, expressed as absolute values and (between brackets) as relative risk, i.e. percentage of the values
found in the QMRA Campylobacter chicken fillet of Nauta et al. (2005), Nauta et al. (2007)1, which is presented in the first row.

Pathogen Food Portions consumed Contaminated Total number of Total number of Number of
portions (at retail) cfu’s before kitchen cfu’s after kitchen people ill
Campylobacter Chicken fillet1 8.5E7 (100) 3.3E7 (100) 7.0E10 (100) 6.1E6 (100) 1.2E4 (100)
Chicken fillet 4.3E8 (502) 1.2E8 (360) 1.7E11 (242) 1.5E7 (239) 3.7E3 (30)
Filet americain 1.1E8 (124) 3.4E5 (1.0) 5.5E5 (0.001) 5.5E5 (9.0) 1.4E2 (1.1)
Table eggs 1.8E9 (2093) 0 (0) 0 (0) 0 (0) 0 (0)
Salmonella Chicken fillet 4.3E8 (502) 4.3E7 (129) 7.7E9 (11) 6.6E5 (11) 4.8E1 (0.39)
Filet americain 1.1E8 (124) 7.5E5 (2.3) 1.2E6 (0.002) 1.2E6 (20) 8.6E1 (0.70)
Table eggs 1.8E9 (2093) 5.4E6 (16) 3.7E9 (5.3) 8.4E7 (1373) 6.0E3 (48)

50
Relative risk (% of human cases)

40

30

20

10

0
Campy-chicken Campy-filet Campy-eggs Salmonella- Salmonella-filet Salmonella-
americain chicken americain eggs

Fig. 8. Relative risk in terms of human cases resulting from sQMRA calculations. The relative risk is expressed as the percentage of the value found in the QMRA
Campylobacter chicken fillet of Nauta et al. (2005, 2007).

of the full-scale QMRA of Nauta et al. (2007) is important as data different points in the food chain (with little budget or time limi-
source for (Campylobacter-) chicken fillet. tations for the QMRA study), that of sQMRA is to make a rapid esti-
Apart from data availability, model output uncertainty can be mation of relative risk, while also giving attention to educational
influenced by the specific food product. Filet americain for in- aspects. The absolute risk values are thought to be not very reliable
stance, is consumed raw and it is unlikely that cross-contamina- as these are even uncertain when produced by QMRA. In short,
tion plays a significant role. This implies that uncertain sQMRA and QMRA each has its own niche.
parameters related to this (Fcc, Fei, Fpry) are redundant for this prod- When using relative risk as the most important model output, a
uct, thus decreasing the uncertainty of the model output. Model good anchor point is necessary in order to be able to interpret the
output uncertainty is absent for pathogen–product combinations model output, in other words to put it in perspective. Epidemiolog-
where Sr/+ is assumed to be zero, such as Campylobacter in table ical estimates are less suitable for this compared to QMRA esti-
eggs. Then all other parameters are redundant. mates, given the often found bad agreement between these two
Finally, model output uncertainty will be relatively small at the in the estimated number of cases of illness. The QMRA for Campylo-
first relative risk point of ‘portions consumed’. Going further down bacter in chicken fillet by Nauta et al. (2007) is generally seen as a
the calculation chain, the number of uncertain parameters that study of good quality and for practical reasons (it was performed at
have to be included in the calculation will increase, so in general, the authors’ department) this study was chosen as reference point.
model output uncertainty will increase along the calculation chain When the risk of several pathogen–product combinations is calcu-
and be highest at the model end point of the number of human lated, an additional comparison can be made, which is comparing
cases. the risk of these combinations among themselves.
In the sQMRA-tool relative risk is determined at a number of
4. Discussion points (see Fig. 7) from ‘portions consumed’ to ‘number of people
ill’. Actually, this last one is the most important model output.
In this paper a new method is introduced to evaluate risks and it The reason to present the intermediate outputs is (apart from edu-
must be stressed here that sQMRA has important differences from cational considerations) that in practice parameter values can
QMRA, in the method itself and in the application options. Impor- prove to be not available or very unreliable, especially when mov-
tant differences in the sQMRA compared to the QMRA method are ing further in the calculation chain than Sr/+. In such cases interme-
that variability and uncertainty is not included and that the model diate outputs (such as ‘contaminated portions consumed’) can be a
starts at the retail phase and not in the farm. These differences are good alternative.
related to the intended applications. Whereas the primary aim of In calculating the attribution of effect, we chose to express this
QMRA is to evaluate the effect of intervention measures taken at as the percentage decrease in number of cases when switching off
E.G. Evers, J.E. Chardon / Food Control 21 (2010) 319–330 327

the specific transmission route, as this fits in with the epidemiolog- Another issue related to prevalence are portions with approxi-
ical approach. An obvious alternative would be to calculate the mately 1 cfu or less. In full-scale QMRA this is dealt with by e.g.
percentage of the number of cases for each route with all other taking the number of cfu as the mean value of a Poisson distribu-
routes turned off. Summing these up will give a percentage larger tion, so that part of the portions is effectively uncontaminated
than 100%, whereas the method we chose will give a percentage and prevalence decreases. In sQMRA, prevalence is not affected
lower than 100%, which is both caused by the non-linear dose–re- by decreasing numbers of cfu per portion. In addition, fractional
sponse relationship. An additional argument to use our approach is numbers of cfu per portion can occur. However, we think that
that it is less realistic to switch off all transmission routes except the effect of these aspects on the (intermediate) calculation results
one. Another alternative would be to set the size of a flow to zero, is limited.
e.g. of Sprd/cc. Assuming total consumption remains constant this A more important issue is that sQMRA uses point estimations,
would ask for upscaling the other categories which makes things thus neglecting variability and uncertainty, which are important
complicated and less insightful. properties of QMRA. For this aspect, sQMRA certainly is a rough
In the sQMRA-tool we use the exponential dose–response model approximation of QMRA and the magnitude of the difference in
and not the Beta Poisson model which might be preferred theoret- model output or the increase in uncertainty is generally not
ically as it incorporates variation in infectivity between individual known, awaiting studies comparing the two approaches. In QMRA
pathogens and/or hosts (Teunis & Havelaar, 2000). The Beta Poisson studies it is often found that the tails of variability distributions are
model has a less steep slope compared with the exponential model important in determining risk (e.g. Nauta et al., 2007; Rieu, Duhem,
which will influence the estimated probability of infection. In the Vindel, & Sanaa, 2007) and this might be a general phenomenon. It
tool we chose for the exponential model as this is the simplest can be argued that when working with relative risk (as in sQMRA)
model with non-linear behavior, which we wanted to include for this effect might cancel out (as both parameters/variables have this
educational reasons. One must also realize that the emphasis in tail) and that point estimates give sufficient information. It would
the sQMRA-tool is on relative risks and not on absolute risks. This be worthwhile to study which point estimate (arithmetic or geo-
makes the choice of the dose–response model less important. Final- metric mean, median, etc.) is best as a surrogate for variability dis-
ly, the choice for the simple exponential model is more in line with tributions, although in practice this will often be a non-discussion
the large simplifications in the exposure part of sQMRA. as there will be little or no data available at all to estimate a point
In the sQMRA tool both attribution of exposure and of cases is estimate with.
presented, to stress the difference between the two. This difference Within the sQMRA model, introduction of variability will have
is caused by the non-linearity of the dose–response model, which no effect on the model output in the exposure part, as the model
(on a linear scale) consists of a decreasing slope with increasing is fully linear in that part. The effect will occur in the effect
dose. The magnitude of non-linear effects when calculating the (dose–response) part, where the nature of the effect will depend
attribution of cases is related to both the dose in the base scenario on the combination of the exposure variability distribution and
and in the attribution scenario, per portion category. In the ficti- the dose–response model (shapes, locations) and the location of
tious example (Fig. 7) this results in an attribution of 50 and 40% the original exposure point estimate.
to cross-contamination for exposure and cases, respectively. These The primary aim of the example calculations was to gain expe-
considerations also stress the importance to distinguish between rience with the method, to see whether it is useful in practice and
exposure and cases in comparative risk assessment. For instance, what problems are encountered. We think the results indicate the
in Evers et al. (2008) exposure was the modeling endpoint, method is useful to obtain a quick rough estimate of risk. It is, how-
whereas the US FDA-USDA-CDC study on Listeria monocytogenes ever, also clear that even for the simple sQMRA method, data avail-
in ready-to-eat foods (2003) used cases. ability is a problem. Although we did not perform extensive
An interesting observation is that attribution of cases can have a literature research as we were imitating the sQMRA-process as it
negative value in the sQMRA-tool. At first sight this might look like were, we do not have the feeling this would have brought us much
an error, but it is a logical result of the calculations and a realistic further. At this point it is important to note that full-scale QMRA’s
result. It occurs e.g. for a product which is only consumed raw and work with this same set of data, and we wonder whether there is a
when significant cross-contamination occurs. When setting Scc/r = 0 proper balance between data and modeling in these QMRA’s in
(the scenario to determine attribution of cross-contamination), the general. The limited data availability partly explains the fact that
result is a negative value for this attribution. The reason for this is in the example calculations kitchen processing is product specific
that in the base scenario a part of the pathogens is lost to the envi- and not pathogen specific.
ronment via cross-contamination. When this route is switched off Sr/+ and Cr/+ were intended to include non-detects as these con-
this no longer occurs, all pathogens go via the raw product, result- stitute a risk also. However, detection limits are often not avail-
ing in a higher exposure and risk than in the base scenario. So in able. As stated in the model description, the underestimation of
principle it would be advantageous to cross-contaminate the envi- risk related to this aspect will usually be low. When available,
ronment for products that are consumed raw. detection limits can be incorporated in the calculations by making
Making a simplified model implies making assumptions and a rough estimate of the increase in Sr/+ and the decrease in Cr/+ or
accepting a higher uncertainty of the results. One example of this alternatively, when data allow, a distribution (e.g. lognormal) can
is that in the model, we work with portions from the retail phase be fitted to concentration data to improve the estimate of these
onwards, whereas portions are usually made during the kitchen parameters.
phase. This is related to the estimation of the prevalence of por- sQMRA and QMRA results for Campylobacter – Chicken fillet
tions, where the issue is that contamination in retail (=contamina- were moderately different, despite the very different methods.
tion of e.g. 1 kg of minced meat, or of a sample of 25 g) refers to a The picture is a bit complex: partly the same data were used, partly
different amount than contamination immediately before con- sQMRA uses additional data; cross-contamination is based on the
sumption (=a meatball of 100 g on the plate). However, we expect same data but modeled differently; both models effectively ex-
that this problem is minor: most monitoring investigations take clude the preparation route for transmission; different dose–re-
one or a few samples per batch, where in most cases batches will sponse models are used.
be clearly contaminated or not (i.e. not with a concentration of For future work, several adjustments to sQMRA are considered.
approximately the detection limit). So prevalence in retail can Important is the change from point estimates to variability distri-
roughly be translated to prevalence at the plate of the consumer. butions. Other issues are:
328 E.G. Evers, J.E. Chardon / Food Control 21 (2010) 319–330

 including a growth model prior to preparation/cross- Based on the original data (Nauta, perscom.) it is estimated that
contamination; on average 0.0456% of the pathogens on chicken fillets is trans-
 inclusion of a module that uses the detection limit to adapt ferred to raw salad and will be ingested. To make this value oper-
prevalence and concentration to real values; ational in the sQMRA-model we take the square root of this value
 simplification of the cross-contamination calculation (given the which is 2.14% and use this value for both Fcc and Fei.
lack of data); Filet americain: Values set to zero as cross-contamination is as-
 offering a choice between the exponential and the Beta-Poisson sumed to play no role.
dose–response model, and extending the number of cases to Table eggs: No data were found on transfer factors related to the
estimate the number of disability adjusted life years (DALYs) breaking of eggs. We guess that 1% of the pathogens transfers to
(Havelaar et al., 2007). hands (Fcc), and that 1% of the pathogens on hands will be ingested
(Fei).
Leading in the consideration of including an adjustment must
be whether it improves the sQMRA estimation of relative risk, tak-
A.4. Spry/cc
ing the limited data availability into account. Maybe different ver-
sions for different applications, such as educational purposes and
Chicken fillet: No data were found on the frequency of consumer
professional use by risk assessment experts, will be developed.
preparation behavior. We guess that the frequency of half done
preparation is 0.2% and that chicken fillet is not consumed raw.
Acknowledgements Filet americain: This product is consumed raw in The Netherlands.
Table eggs: We derived our estimates from Fig. 3–31 in FSIS
The authors wish to thank Maarten Nauta and Arie Havelaar for (2005), which represents the outcome of an exposure assessment
their help and useful discussions. model based on data from the United Kingdom (Humphrey, White-
head, Gawler, Henley, & Rowe, 1991). We assigned the cooking cat-
egories to the preparation categories from the sQMRA-tool as
Appendix A
follows: ‘‘soft boiled” and ‘‘sunny side” were assigned to ‘‘half-
done”, ‘‘over easy”, ‘‘scrambled omelet’s”, and ‘‘hard boiled” were
A.1. N, M
assigned to ‘‘done” and ‘‘none” was assigned to ‘‘raw”.

The number of portions consumed N and the average portion


A.5. Sr/+ Campylobacter
size M are taken from the last general Dutch Food Consumption
Survey (Kistemaker, Bouman, & Hulshof, 1998). The survey was
Chicken fillet value: Taken from Table 7 in Van der Zee, Wit, and
carried out in 1997/1998 and the full electronic database is avail-
Vollema (2005).
able at RIVM. N stands for the number of portions consumed by
Filet americain value: preliminary data from survey ‘monitoring
the whole Dutch population (16 million people) in a whole year.
filet americain’ (perscom. Wit, Dutch Food and Consumer Product
Safety Authority, 2007). Specific test results are 3 Campylobacter
A.2. Scc/r
positives in 924 samples.
Table egg value: No prevalence data were found in literature or
Chicken fillet: Cross-contamination is only considered relevant
elsewhere. Also, no outbreaks attributed to Campylobacter in table
when raw salad and chicken breast are prepared together for a
eggs were found. Therefore, a prevalence of 0% is assumed.
meal. In the Netherlands this occurs 85 million times a year (Nauta
et al., 2005). During a consumer behavior study, cross-contamina-
tion was observed in 52 out of 55 prepared portions of chicken A.6. Cr/+ Campylobacter
breast salad (Nauta et al., 2008). Using N this leads to
Scc/r = (52/55)  (85E6/427E6) = 18.8%. Chicken fillet: Luber, Brynestad, Topsch, Scherer, and Bartelt
Filet americain: This product is supposed to be consumed raw (2006) give 11 measurements of the sum of Campylobacter num-
and it is assumed that no cross-contamination occurs in the kitch- bers on five breast fillets. The mean value per fillet is 1427 cfu.
en. Therefore we set this value to zero. Combined with the value for M above (100.3 g), Cr/+ can be calcu-
Table eggs: The sQMRA considers all table eggs consumed. How- lated to be 14.2 cfu/g. This value is an underestimation (of 67%
ever, it is assumed that cross-contamination only plays a role when maximum) as at the most 2 of 5 fillets may be uncontaminated.
eggs are fried. In the Netherlands, 42.5% of the table egg portions It is used here in the absence of better data.
are fried (Kistemaker et al., 1998). We guess that the probability Filet americain: No concentration data were found. Assuming the
is 50% that hands will be contaminated with egg white through campylobacters are randomly distributed in this product and
breaking the egg shells prior to frying. According to the Belgian observing the low prevalence, almost all positive samples will con-
food consumption survey (Devriese, Huybrechts, Moreau, & Van tain only 1 cfu. As sample size is 25 g (pers.com. Wit, Dutch Food
Oyen, 2006), 17.1% of the consumers directly continue cooking and Consumer Product Safety Authority, 2007), Cr/+ is estimated
after breaking the egg shells. Using these numbers Scc/r for table to be 1/25 = 0.04 cfu/g.
eggs can be calculated to be 0.425  0.5  0.171 = 3.63%. Table eggs: As Sr/+ is set to zero, Cr/+ will be set to zero also.

A.3. Fcc and Fei A.7. Fpry Campylobacter

No relevant data were found distinguishing between pathogen Obviously raw preparation has no influence on the number of
transfer from portions to environment and from the environment micro-organisms, so Fprr = 100 for all food products.
to ingestion. We therefore used identical values for Fcc and Fei in Chicken fillet: We used the inactivation model and Table 1 from
the calculations. Van Asselt and Zwietering (2006) to estimate the surviving fraction
Chicken fillet: In Nauta et al. (2008) transfer factors are deter- of micro-organisms after preparation, assuming that the micro-
mined describing pathogen transfer from portions to ingestion. organisms reside on the outside of the chicken fillet. We estimated
E.G. Evers, J.E. Chardon / Food Control 21 (2010) 319–330 329

a preparation time of 2 min at 130 °C and 4 min at 130 °C for half- A.14. Pill/inf Salmonella
done and done preparation, respectively. Entering these values in
the inactivation model resulted in a survival of 0% for all pathogens This parameter is redundant (see ID50 Salmonella) and set at
in both cases. 100%.
Filet americain: For this product Fprd and Fprh are redundant as it
is only consumed raw. They are set to zero.
Table eggs: For this product Fprd and Fprh are not relevant as the References
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