Development and validation of a probabilistic second-order

exposure assessment model for Escherichia coli O157:H7

contamination of beef trimmings from Irish meat plants
E. Cummins
a,
*
, P. Nally
a
, F. Butler
a
, G. Duy
b
, S. OBrien
b
a
Biosystems Engineering, School of Agriculture, Food Science and Veterinary Medicine, University College Dublin, Earlsfort Terrace, Dublin 2, Ireland
b
The Ashtown Food Research Centre, Ashtown, Dublin 15, Ireland
Received 19 January 2007; received in revised form 20 August 2007; accepted 22 August 2007
Abstract
A second-order quantitative Monte Carlo simulation model was developed for Escherichia coli O157:H7 contamination of beef trim-
mings in Irish abattoirs. The assessment considers initial contamination levels, cross-contamination and decontamination events during
the cattle slaughter process. The mean simulated prevalence of E. coli O157:H7 on trimmings was 2.36% and the mean simulated counts
of E. coli O157:H7 on contaminated trimmings was 2.69log
10
CFU/g. A parallel validation survey provided some condence in the
model predictions. An uncertainty analysis indicated that microbial test sensitivity is a signicant factor contributing to model uncer-
tainty and requires further investigation while also indicating that risk reduction measures should be directed towards reducing the hide
to carcass transfer (correlation coecient 0.25) during dehiding and reducing the initial prevalence and counts on bovine hides (corre-
lation coecients 0.19 and 0.16, respectively). A characterisation of uncertainty and variability indicating that further research is
required to reduce parameter uncertainty and to achieve better understanding of microbial transfer in meat plants. The model developed
in this study highlights the need for further development of quantitative risk assessments in the food industry.
2007 Elsevier Ltd. All rights reserved.
Keywords: Exposure assessment; Simulation; Escherichia coli O157:H7; Beef
1. Introduction
Verocytotoxigenic Escherichia coli, in particular sero-
group O157, has emerged as a pathogen of major public
concern. High prole outbreaks have focused attention
on outbreaks connected to food products, in particular,
minced beef and beef burgers (CDC, 1993; Duy, Cum-
mins, Nally, OBrien, & Butler, 2006a). Preliminary gures
indicate that approximately 52 cases of E. coli O157:H7
poisoning occurred in Ireland during 2004 (HPSC, 2004),
while other suspected cases in 2005 are currently under
investigation. The current number of illnesses in Ireland
represents a worrying trend as the numbers remain at a rel-
atively high level with a peak of 88 occurring in 2003
(HPSC, 2004). Consequences of food borne poisoning
from the bacteria can vary from severe illness to kidney
failure, central nervous system damage and death.
The E. coli O157 bacterium is present in faeces and the
intestines of healthy bovines and can contaminate meat dur-
ing the slaughter process (Chapman, 2000). One of the most
signicant threats to food safety is the potential contamina-
tion of edible carcass tissues with the bacterium. The level of
this risk is related to the extent and nature of such contam-
ination and the stages which may distribute bacterial con-
tamination during the slaughter process (Gill, McGinnis,
& Badoni, 1996; McEvoy et al., 2001, 2003). Cross-contam-
ination can occur at multiple stages during the slaughter
process resulting in potential contamination of meat des-
tined for human consumption. Following removal of the
primal cuts of beef from the beef carcass the remaining cuts
0309-1740/$ - see front matter 2007 Elsevier Ltd. All rights reserved.
doi:10.1016/j.meatsci.2007.08.015
*
Corresponding author. Tel.: +353 1 7167476; fax: +353 1 4752119.
E-mail address: enda.cummins@ucd.ie (E. Cummins).
www.elsevier.com/locate/meatsci
Available online at www.sciencedirect.com
Meat Science 79 (2008) 139154
MEAT
SCIENCE
of meat, including ank and Jacobs ladder (part of the M.
serratus ventralis) are removed. These cuts are referred to
as beef trimmings and are later processed into saleable
products such as beef burgers. Given that beef trimmings
are processed into comminuted beef products for human
consumption, it stands to reason that beef trimmings should
be free from all sources of contamination, thus reducing
human exposure to potential hazards, including E. coli
O157:H7. Scientic evidence suggests that most E. coli
related food poisoning cases have been associated with
comminuted beef products (CDC, 1993), highlighting the
importance of investigating this source of contamination.
The objective of this work was to develop a quantitative
exposure assessment to model the contamination of beef
trimmings at Irish abattoirs in an eort to identify critical
points in the process and to assess the impact of process
stages on the prevalence and counts of E. coli O157:H7.
There exists previously published models of bacterial con-
tamination of beef trimmings in abattoirs (Cassin, Lam-
merding, Todd, Ross, & McColl, 1998; Jordan, McEwen,
Lammerding, McNab, & Wilson, 1999a; Roberts, Mal-
colm, & Narrod, 1999; Ebel et al., 2004; USDA, 2002).
However, few studies have conducted parallel validation
studies to ensure model predictions are an accurate repre-
sentation of reality. A unique element of this study was
the parallel microbial surveillance conducted at several
points in the abattoir, thus acting as a partial validation
for the model (OBrien et al., 2005; Carney et al., 2006;
Duy et al., 2005). We state partial validation as full vali-
dation would involve repeated comparisons between model
outputs and real data which would be unfeasible in a food
production situation due to limited time and resources.
However, the partial validation provides a snapshot of
how model outputs compare with real data and can pro-
vide an element of condence in model predictions. The
model used probability distributions to simulate both
uncertainty and variability in the construction of a sec-
ond-order model. The probability distributions of the com-
ponent variables were either derived from survey data or
estimated from the available literature. The output of the
model was a distribution of the prevalence of E. coli
O157:H7 on beef trimmings and a distribution for the num-
ber of organisms on contaminated beef trimmings. The
model used Monte Carlo simulation techniques (Vose,
2000) to create the output distributions. Monte Carlo
methods repeatedly select values randomly from distribu-
tions to create multiple scenarios of a problem. Together,
these scenarios give a range of possible solutions, some of
which are more probable and some less probable resulting
in a probability distribution for the solution parameter.
2. Materials and methods
2.1. Model development
The focus of the model was within the slaughterhouse.
The prevalence and counts of E. coli O157:H7 bacteria
were modelled at various stages along the slaughter line.
A ow diagram of the process is given in Fig. 1. The model
was created in Microsoft Excel 2000 with the add-on pack-
age @Risk (version 4.05, Palisade Corporation, New York,
USA).
Distributions can be used to represent the eect each
process stage has on microbial numbers by modelling inter-
mediary processing stages (e.g. dehiding, evisceration,
washing, chilling and boning out). As a result changes in
Decontamination
Stunning
Shackling/Hoisting
Neck Hide
opening
Removal of hooves
De-hiding
Head removal
Brisket sawing
Carcass splitting
Spinal Cord
removal
Trimming
Carcass grading,
weighing & stamping
Evisceration
Steam
Pasteurisation
Trimmings
Boxed Beef
trimmings (70VL)
Carcass
Washing
Chilling
Boning out
Fig. 1. Flow diagram of the stages involved in bovine slaughter and
subsequent production of beef trimmings. Ovals denote steps that may
either increase or decrease contamination. Rectangles denote steps with
little or no increase in contamination.
140 E. Cummins et al. / Meat Science 79 (2008) 139154
microbial counts on the carcass can be simulated as the car-
cass moves through the plant. Model inputs were derived
from Irish data where possible. A number of studies spe-
cic to Irish abattoir conditions (Carney et al., 2006; Duy
et al., 2005; McEvoy et al., 2000, 2001, 2003; OBrien et al.,
2005; Sheridan, Lynch, & Harrington, 1992) provided valu-
able input data; alternatively, international data and scien-
tic literature were consulted to improve the basis for the
model where Irish specic data were not available.
2.2. Uncertainty and variability
There is increasing emphasis being placed on quantify-
ing the impact of uncertainty and variability in risk assess-
ments (Bogen, 1995; Bogen & Spear, 1987; Borsuk, 2004;
Burmaster & Thompson, 1998; Cohen, Lampson, & Bow-
ers, 1996; Frey & Rhodes, 1996; Frey & Burmaster, 1999;
Kelly & Campbell, 2000; Nayak & Kundu, 2001; Pouillot,
Beaudeau, Denis, & Derouin, 2004). Variability refers to
the eect of chance and is a function of the system. It is
not reducible by further study. Variability represents a true
heterogeneity of the population. Uncertainty represents
our lack of knowledge about a particular parameter in
the model and can be reduced by further measurement or
study. Since ecological systems are highly variable and
our knowledge of model input parameters is uncertain, it
is important that models separate the eects of uncertainty
and variability (Regan et al., 2003). Separation of the two
will highlight the importance of uncertainty of the input
parameters by means of a sensitivity analysis and can pro-
vide greater accountability and transparency for key ele-
ments of the model. In a probabilistic risk assessment,
the term second-order is often used to describe the use
of probability distributions to represent variability and
uncertainty in the input parameters (Bogen & Spear,
1987; Frey, 1993; Price, Su, Harrington, & Keenan, 1996;
Vose, 2000). Variability and uncertainty in the input
parameters were incorporated in the construction of a sec-
ond-order model by means of probability distributions.
Previously published models of slaughterhouse contamina-
tion (Roberts et al., 1998; Cassin et al., 1998; Jordan et al.,
1999a, Jordan, McEwen, Lammerding, McNab, & Wilson,
1999b) were rst-order models and did not fully distinguish
between uncertainty and variability. Their separation in
this model allows us to understand the steps necessary to
reduce total uncertainty and allows us to gauge the value
of more information or some potential change to the sys-
tem. The second-order approach claries communication
of results to decision-makers, helping to identify sensitive
input parameters and future data collection requirements.
2.3. Model assumptions
Simulation models regularly require the use of unavoid-
able subjective assumptions. These assumptions can impact
on the results obtained in risk and exposure assessments,
hence models need to be viewed in the context of the
assumptions made. The following modelling assumptions
have been made in the development of this exposure
assessment:
The probability of one cow on the slaughter line being
infected is independent of the probability of another
cow on the slaughter line being infected. Random mix-
ing is assumed to occur.
Meat is normally sterile beneath exposed surfaces, but
some surface contamination with pathogens can occur
during the slaughter process.
The microbial prole of a production lot of beef trim-
mings is independent of previous lots processed at the
abattoir, i.e. that the plant environment is completely
sterilised between runs.
The model assumes homogenous distribution of feces on
bovine hides and carcass, assuming some clustering
may yield dierent results.
Contamination levels on a carcass following rupture of
the intestine were assumed to be the same as when a car-
cass is contaminated by the hide.
During storage and handling of meat, E. coli O157:H7
levels can increase.
An inability to obtain empirical data results in the appli-
cation of probability distributions to model process
stages; the model tries to err on the side of caution when
modelling inactivation and growth.
The model assumes no false positives for the partial val-
idation study used (i.e. specity equal to 100%).
Validation data points (Carney et al., 2006) are
assumed to be independent and identically (binomially)
distributed.
3. Model input parameters
For clarity, the model is compartmentalised into four
sections: (1) initiating parameters, (2) slaughter module,
(3) trimmings production module and (4) model run and
outputs. The model relies upon the generation of random
variables from input probability distributions and these
are represented in the model equations by the name of
the probability distribution (e.g. Poisson, triangular, etc.)
followed by the parameters in brackets. The input proba-
bilities for each of the sections, displayed in Figs. 2 and
3, were derived from the literature and expert opinion.
3.1. Initiating parameters (hide and gut prevalence)
The model starts with bovines entering the abattoir;
some initial parameters are needed at this stage. These
initiating parameters include the prevalence of E. coli
O157:H7 on bovine hides, in the bovine intestine and
on bovine carcasses. Table 1 summarises these input
distributions.
The prevalence of E. coli O157:H7 on the hides of live
cattle in Ireland was estimated from an extensive survey
carried out in conjunction with this research project (Duy
E. Cummins et al. / Meat Science 79 (2008) 139154 141
et al., 2006b), the details of which, including materials and
methods for detecting bacterial, are given in OBrien et al.
(2005). The survey was conducted at an Irish commercial
abattoir with a line speed of 4080 animals per hour. From
a sample of 1500 bovine hides, 109 hides were found to be
positive for the bacteria. If we have no prior information
about a prevalence, and do not wish to assume any prior
information, a uniform prior distribution is used (Vose,
2000), thus through Bayes theorem the posterior turns
out to be a beta distribution, which is a conjugate to the
Binomial distribution. A Beta distribution can be used to
model the condence one has about the probability of suc-
cess of a binomial trial p, where one has observed n inde-
pendent trials of which s were successes with the formula
p = beta (s + 1, n s + 1). A beta distribution with uni-
form prior is therefore used to model uncertainty about
prevalence estimates in this study. The prevalence (P
h
) on
animal hides was therefore modelled using a beta distribu-
tion (beta(109 + 1, 1500 109 + 1)) to represent parameter
uncertainty. The conrmatory test used during this survey
was the Immunomagnetic Separation test (IMS) (Duy
et al., 2005). Previous work has shown that test sensitivity
may be dependent on the condition of the animal hide (i.e.
wet or dry) as illustrated by OBrien et al. (2005). To
Tse: Test
sensitivity
P
h
: Prevalence on
hide
TR: Transfer
rate
P
ht
: True Prevalence
on Hide
I
h
: Counts on hide
(log CFU/100 cm
2
)
F
c
: Boolean Flag
CR: Growth during
chilling (log)
P
c
: Prevalence on
Carcass
Not
contaminated
I
ht
: True counts on
hide (log CFU/cm
2
)
Fi: Recovery
Factor
I
c
: Counts on Carcass
(log CFU/cm
2
)
R: Count
Reduction from
hide to carcass
B
ch,
B
cg
, B
cb
: Total
organisms on
contaminated surface
(log CFU)
A: Contaminated
surface area
(cm
2
)
N
d
, N
g
,N
b
: Total
organisms on
contaminated surface
following fabrication
(log CFU/carcass)
D1: Decontamination
(log)
G: Growth during
Fabrication (log)
n
d
, n
g
, n
b
: Total
organisms per unit
surface area (log
CFU/cm
2
)
A: Contaminated
surface area (cm
2
)
C
trim
: Total organisms
on a trimming (log
CFU)
Acontam:
Contaminated area
of a trimming (cm
2
)
C: Total Organisms on
a contaminated
trimming (Log CFU/g)
Mt: Mass of
trimming (g)
- Total Surface area (TSA)
- Trim per animal (Atrim)
- Contaminated surface area
I
t
: Infected
Trimmings
P: Prevalence of
contaminated
trimming
Nt: Total
trimmings
produced
D2: Decontamination
(log)
Input from Figure 2
I
n
i
t
i
a
t
i
n
g

P
a
r
a
m
e
t
e
r
s

S
l
a
u
g
h
t
e
r

M
o
d
u
l
e

T
r
i
m
m
i
n
g
s

P
r
o
d
u
c
t
i
o
n

C
c
: Number of
infected carcasses
As: Animals
Slaughtered
Fig. 2. Diagrammatic representation of the simulation model together with the input parameters.
142 E. Cummins et al. / Meat Science 79 (2008) 139154
account for this, a test sensitivity parameter (T
se
) was
derived using bayesian inference techniques (Cummins,
Nally, Butler, Duy, & O Brien, 2007). Bayesian inference
can be used to combine multiple data sets and expert opin-
ion to give a posterior distribution. The true (P
ht
) preva-
lence was calculated by dividing the detected prevalence
on bovine hide (P
h
) by the test sensitivity (T
se
). The nature
of the test is such that test specicity is assumed to be
100%, thus the model assumes that there are no false
positives.
The prevalence of E. coli O157:H7 in the intestine of
Irish bovine animals (P
g
) was determined from McEvoy
et al. (2001, 2003) where it was found that two animals
from a sample of 250 were positive for the bacteria. The
prevalence in the intestine was thus modelled using a beta
distribution (beta(2 + 1, 250 2 + 1)).
3.2. Slaughter module
3.2.1. Dehiding
The dehiding stage can contaminate the carcass in sev-
eral ways including direct contact between a carcass and
a contaminated hide or cross-contamination via worker
handling. Transfer of contamination from hide surface to
carcass is eectively unavoidable due to the nature of the
process (McEvoy et al., 2000). McEvoy et al. (2003)
reported the greatest carcass contamination occurs at sites
associated with the opening of the hide. McEvoy et al.
(2000, 2003) found E. coli O157:H7 on three carcasses from
a sample of 36 carcasses following hide removal. It is
unknown whether these animals were shedding the bacteria
or had contaminated hides. However, the results highlight
the likely transfer of bacteria to the carcasses at this process
point. Bell (1997) reported high contamination on sites
associated with opening cuts and/or subject to hide contact
during hide removal. Elder et al. (2000) performed a survey
in the USA to estimate the frequency of enterohemorrhagic
E. coli O157:H7 in faeces and on hides within groups of
cattle from single lots presented for slaughter at meat pro-
cessing plants and found that faecal and hide prevalence
were signicantly correlated with carcass contamination.
Previous models (Cassin et al., 1998; Ebel et al., 2004) cre-
ated a cross-contamination factor between prevalence of
E. coli O17:H7 in bovine feces and the prevalence on
bovine carcass. However, given the evidence for signicant
cross-contamination from bovine hides (Elder et al., 2000;
Gill, McGinnis, & Bryant, 1989; McEvoy et al., 2003), the
model developed in this study assumes that contaminated
animal hide is the main vehicle for cross-contamination
to bovine carcasses at the hide removal stage. Thus, a
cross-contamination factor (TR) from bovine hide to
carcass was created using Irish surveillance data. From a
E: Probability
of gut rupture
P
g
: Prevalence in gut
Ef: Boolean Flag
Not
contaminated
Output to Figure 1
B
cg
: Total organisms
on contaminated
surface (log CFU)
I
n
i
t
i
a
t
i
n
g

P
a
r
a
m
e
t
e
r
s
S
l
a
u
g
h
t
e
r

M
o
d
u
l
e

Fig. 3. Diagrammatic representation of the simulation of intestinal contamination of a bovine carcass.
Table 1
Initiating parameters, distributions and inputs used in the model
Parameter Symbol Distribution/model Category Units
Animals slaughtered in a day A
s
350 Fixed value Animals
Prevalence in the gut P
g
beta(3, 247) Uncertainty Prevalence
Prevalence on the hide P
h
beta(110, 1390) Uncertainty Prevalence
Test sensitivity T
se
derived by Bayesian inference (see text) Uncertainty Factor
True prevalence P
ht
P
h
/T
se
Prevalence
Transfer ratio between hide and carcass TR beta(4, 32)/beta(110, 1390) Uncertainty Prevalence
Prob. of infected carcass P
c
TR P
ht
/(1 P
h
+ TR P
ht
) Calculation Ratio
Number of contaminated carcasses C
c
Binomial(A
s
, P
c
) Variability Animals
Total surface area of animal TSA 32,000 Fixed value cm
2
Mass of a combi bin M 2700 Fixed g
E. Cummins et al. / Meat Science 79 (2008) 139154 143
sample of 1500 bovine hides, 109 hides tested positive for
E. coli on entering the slaughter plant (OBrien et al.,
2005). Following hide removal, three carcasses from a sam-
ple of 36 carcasses tested positive for E. coli O157:H7
(McEvoy et al., 2001, 2003). The two resulting beta distri-
butions were combined to create a cross-contamination
factor from animal hide to carcass, TR:
TR beta3 1; 36 3 1=beta109 1; 1500 109 1:
1
The probability of a carcass being contaminated (P
c
) is
thus given by the equation
P
c
TRP
ht
=1 P
ht
TR P
ht
: 2
The number of contaminated carcasses (C
c
) processed on a
particular day can therefore be simulated using a binomial
distribution (binomial(A
s
, P
c
), with the total number of ani-
mals slaughtered on a particular day represented by A
s
.
For this work, A
s
was set to 350, representing a typical days
slaughter in an Irish abattoir. A similar approach was
taken by Cassin et al. (1998) in modelling carcass contam-
ination, while Ebel et al. (2004) simply used the cross-
contamination factor as a multiplier for the number of
animals infected in a cattle lot.
3.2.2. Initial bacterial load on bovine hide and carcasses
Following the calculation of the prevalence of infected
carcasses, each carcass was simulated individually and a
Boolean (truefalse) ag generated as a Bernoulli random
variate with p (the probability of a carcass being contami-
nated) equal to the prevalence. Each Boolean ag used a
binomial distribution with the total number of events equal
to 1. Thus, the result of each Boolean ag will be 1 (con-
taminated) or 0 (uncontaminated). This was used to con-
rm contamination, or otherwise, of the carcass (F
c
) and
intestine (F
g
) of each individual animal (see Figs. 2 and 3,
respectively). Should the ag conrm the presence of con-
tamination, the model continues to model the counts of
bacteria from hide to carcass and the eect subsequent pro-
cessing treatments have on bacterial counts.
The initial number of bacteria on animal hides (I
h
) was
modelled by tting a second-order continuous non-para-
metric distribution to a data set. The methodology is
detailed in Vose (2000). This procedure thus gives a sec-
ond-order model of the initial counts of bacteria on animal
hides. The technique allows the construction of a non-para-
metric second-order distribution for a continuous variable
given a limited experimental data set.
The initial levels of bacteria on animal hides (I
h
) used in
this analysis were from a survey conducted at a large Irish
abattoir by OBrien et al. (2005) where they evaluated
microbial populations on bovine hides. The bacterial
counts were estimated using direct plate methods (OBrien
et al., 2005). Sponge swab samples yielded mean E. coli
O157:H7 counts on the exterior hide ranging from 0.13
to 4.24log
10
CFU/100 cm
2
. Of the 109 positive samples,
82 were detected by direct plate and enumerated, while
27 samples were detectable by enrichment only, indicating
that their count was below the detectable level for direct
plating (taken as 1 CFU/100 cm
2
) and, hence, counts for
these samples were not obtained. The frequency data for
the distribution of the counts are shown in Table 2. If
the counts on a carcass were deemed to be below 1 CFU/
100 cm
2
, the count was modelled using a uniform distribu-
tion ranging from 0 to 1 CFU/100 cm
2
. For carcasses with
counts above 1 CFU/100 cm
2
, a second-order non-para-
metric distribution was tted to the data set. Fig. 4 repre-
sents the resulting second-order non-parametric
distribution used to model the initial bacterial load on
bovine hides. The mean distribution is indicated by the
bold line. The 5th and 95th percentile values for the uncer-
tainty distribution are also included, represented by the
vertical grey lines.
Reduction in bacterial recovery from bovine hide and
meat has previously been noted (Byrne, Bolton, Sheridan,
McDowell, & Blair, 2000; Chapman et al., 1993; Firsten-
berd, 1981; McEvoy et al., 2003; Nortje & Naude, 1981)
but is a parameter which appears to have been omitted
from previous models of bacterial contamination in abatt-
oirs. The reduction may be due to the irreversible binding
of some of the bacteria deposited; it has been described
Table 2
Frequency distribution for E. coli O157:H7 counts on bovine hides
(adopted from OBrien et al. (2005))
CFU/100 cm
2
Frequency
<1 27
a
<10 37
<100 34
<1000 9
<10,000 1
<100,000 1
<1,000,000 0
Total 109
a
Undetectable by direct plate.
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
1
-1.5 -0.5 0.5 1.5 2.5 3.5
Log
10
CFU/100 cm
2
C
u
m
u
l
a
t
i
v
e

p
r
o
b
a
b
i
l
i
t
y
x<=-0.61
5.0%
x<=2.44
95.0%
Fig. 4. Cumulative distribution for E. coli O157:H7 counts on bovine
hides including separation of uncertainty (represented by the presence of
multiply lines) and variability (each line is a variability distribution).
144 E. Cummins et al. / Meat Science 79 (2008) 139154
as a two-stage process by McEvoy et al. (2003) whereby ini-
tial reversible absorption becomes irreversible over time.
Hence, the values estimated in the survey may themselves
be the subject of uncertainty due to this reduction in recov-
ery. Research was carried out by OBrien et al. (2004)
whereby a known number of E. coli O157:H7 bacteria were
inoculated onto an animal hide and recovery of the bacte-
ria from the hide was carried out using direct plate methods
(as used in the commercial survey). Successive tests
revealed that the recovered bacterial count could vary
between 0.50 and 1.50log
10
compared to the initial inocu-
lum level. To account for this, a recovery factor (F
i
) for
the initial counts of bacteria was incorporated into the
model with uniform uncertainty distribution ranging from
0.50 to 1.50log
10
. The true count (log
10
CFU/cm
2
) on ani-
mal hide (I
ht
) was modelled by taking account of the factor
increase due to the likely reduced bacterial recovery and is
represented by
I
ht
log10
I
h
F
i

=100: 3
Bacon, Belk, Sofos, & Smith (2000) evaluated microbial
populations on animal hides and changes in carcass micro-
bial population at various stages in the slaughtering pro-
cess in the USA. Sponge swab samples yielded mean
generic E. coli on the exterior hide of 5.507.50log
10
CFU/100 cm
2
with corresponding concentration levels on
the carcass (after hide removal but before any decontami-
nation intervention) of 2.605.30log
10
CFU/100 cm
2
. The
reduction in counts from animal hide to carcass (R) was
thus obtained by tting a continuous empirical cumulative
distribution to this data (Fig. 5). The initial counts
(log
10
CFU/cm
2
) on a carcass (I
c
) were therefore obtained
by subtracting the log reduction factor (R) from the true
initial counts on the animal hide (I
ht
) as given by
I
c
I
ht
R: 4
There are no scientic studies available to estimate the total
contaminated surface area (A) of a carcass. This model
used the same approach as suggested by Ebel et al.
(2004) as follows:
A 10
Triangularlog30;log300;log3000
: 5
This is based on the fact that initial runs of their model
indicated a maximum contamination area of 3000 cm
2
and the minimum contamination area arbitrarily set to
30 cm
2
. The total organisms (log
10
CFU/carcass) on a con-
taminated carcass after dehiding (B
c,h
) is therefore given as
B
c;h
log10
Ic
A: 6
3.2.3. Decontamination after dehiding
A number of decontamination steps are employed fol-
lowing dehiding, including knife trimming to remove visi-
ble spots of faecal contamination and/or a series of
washing treatments. The eectiveness of knife trimming is
highly variable (Prasai et al., 1995). In particular, work
by Smeltzer, Peel, and Collins (1998) and Sheridan et al.
(1992) have shown that equipment such as knives, gloves
and aprons can act as reservoirs for bacteria. Gill et al.
(1996) suggested that trimming can extensively decontami-
nate parts of the carcass. Scientic studies relating to car-
cass washing give conicting results. Typically animals
are washed with potable water at a temperature of 35
40 C. McEvoy et al. (2003) reported no signicant change
in generic E. coli counts following washing while Reagan
et al. (1996) concluded that carcass washing can have the
eect of reducing counts of bacteria. There is also evidence
that some washing procedures may redistribute bacteria to
other parts of the carcass (Bell, 1997; Castillo, Lucia,
Goodson, Savell, & Acu, 1998; McEvoy et al., 2003). Cas-
sin et al. (1998) modelled the reduction in counts due to
decontamination at this stage by using a uniform
distribution with minimum of 1 and a maximum of
2.50log
10
CFU/cm
2
reduction. In the present study, to cap-
ture the variability, reduction by decontamination (D1)
was modelled using a triangular distribution with a mini-
mum reduction of zero, a most likely of D1
mm
and maxi-
mum of D1
max
. A triangular density distribution is used
as a modelling tool where the range and most likely value
within a range can be estimated. The triangular distribu-
tion oers considerable exibility in its shape while
accounting for the uncertainty within the given range
(Vose, 2000). Gill (1999) reported a reduction in generic
E. coli counts of 0.32 log
10
CFU/cm
2
following rinsing
while (Dorsa, 1997) reported a 0.70log
10
CFU/cm
2
reduc-
tion of E. coli following rinsing. The uncertainty about
the most likely value (D1
mm
) was thus modelled using a
uniform distribution (uniform(0.30, 0.70)). The uncertain
maximum value was arbitrary set to vary between 0.80
and 1.20log
10
CFU/cm
2
(D1
max
= uniform(0.80, 1.20)).
3.2.4. Evisceration
Evisceration represents another opportunity for con-
tamination of the carcass to occur. If the intestine of an
animal is positive for E. coli O157:H7 and the intestine is
inadvertently ruptured during the evisceration process,
gross-contamination of the carcass may occur due to
X <= 3.91
95.0%
X <= 0.54
5.0%
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
1
log reduction in counts from animal hide to carcass (R)
C
u
m
u
l
a
t
i
v
e

p
r
o
b
a
b
i
l
i
t
y
-0.5 0 0.5 1 1.5 2 2.5 3 3.5 4 4.5
Fig. 5. Log reduction in counts from animal hide to carcass (R) (based on
Bacon et al., 2000).
E. Cummins et al. / Meat Science 79 (2008) 139154 145
spilling of the intestine contents. However, research by
McEvoy et al. (2003) reported that evisceration did not
appear to contribute to carcass contamination with
E. coli O157:H7, which is in agreement with other studies
(Nottingham & Harrison, 1974). Cassin et al. (1998) and
Roberts et al. (1999) neglected to consider the possible
impact of evisceration in their models. This is likely to be
due to the small number of occasions that an intestine is
ruptured at evisceration. In the present study, it was
decided to model the evisceration stage similarly to that
done by Ebel et al. (2004). The number of times eviscera-
tion resulted in a ruptured intestine was determined to be
relatively small (between 1 in 100 and 1 in 1000) as indi-
cated by the abattoir workers and plant manager (oral
communication). Thus, the probability of intestine con-
tents spilling (E) during evisceration was modelled as
E 10
uniform2;3
: 7
The model therefore uses another Boolean ag to simulate
the rupture of the intestine of an individual carcass (E
f
). If
the intestines of an animal are split and the animal does not
have an infected intestine it is assumed that the carcass is
not infected. Only when an intestine is positive for the bac-
teria and the intestine is ruptured will contamination of a
carcass occur through this route. The counts of bacteria
on a carcass after rupture (B
c,e
) were assumed to be the
same as when the carcass was contaminated from the ani-
mal hide (i.e. B
c,e
= B
c,h
). The model combines counts from
both sources in the unlikely event of a carcass being con-
taminated during dehiding and during evisceration.
3.2.5. Decontamination after evisceration
After carcass splitting and spinal cord removal, some
knife trimming is carried out to remove visible spots of fae-
cal contamination. Steam pasteurisers are installed in a
small number of meat plants in Ireland. Its eciency was
assessed by Phebus et al. (1997). Reductions of E. coli
O157:H7 were found to be approximately 3.53 (0.49)
log
10
CFU/cm
2
. Technical diculties have meant limited
use of these pasteurisers to date in Irish plants. In this anal-
ysis, the model considers production in a plant which does
not have steam pasteurisation in place, as it is more repre-
sentative of current abattoir practices in Ireland. After
splitting and spinal cord removal, animals are typically
washed with potable water at a temperature ranging from
35 to 40 C. A second decontamination step (D2) was con-
sidered in the model to take account of this. Similar eec-
tiveness of the rst decontamination step was assumed, as
the processes are similar (i.e. carcass washing). The process
was modelled, similarly to D1, using a triangular
distribution with uncertainty about the most likely value
[D2
mm
= uniform(0.30, 0.70)] and uncertainty about the
maximum reduction [D2
max
= uniform(0.80, 1.20)].
3.2.6. Chilling
It has been reported that chilling is not likely to have
any noticeable eect on E. coli prevalence or counts (Cassin
et al., 1998; McEvoy et al., 2003). McEvoy et al. (2003)
reported a reduction in prevalence on carcasses after chill-
ing for 24 h. McEvoy et al. (2003) hypothesised that chill-
ing may stress the bacterial cells due to the synergistic
eect of low water activity (a
w
) and temperature. Similarly,
Gill et al. (1996) reported a reduction in coliforms and
E. coli on carcasses following cooling processes of between
0.50log
10
and 2.00log
10
units. McEvoy et al. (2003) sug-
gested that cross-contamination between carcasses might
also occur during chilling, however, there was a lack of evi-
dence to support this claim. Sheridan (2000) noted that car-
cass contamination may increase, decrease or remain
unchanged following chilling and depended on parameters
such as temperature, air speed and relative humidity. In the
model, growth or decline is assumed to occur only on car-
casses that are contaminated on entering the chiller. Cassin
et al. (1998) modelled the potential growth using a triangu-
lar distribution with minimum growth of 2, a mode of 0
and a maximum of 5 generations. Similarly Roberts et al.
(1999) used a triangular distribution to model the chilling
stage with a minimum reduction of 0log
10
reduction and
a maximum and most likely reduction of 1.00log
10
. Similar
to Ebel et al. (2004), the change in counts on contaminated
carcasses during chilling (CR) was assumed to be normally
distributed and was modelled in this study using a normal
distribution with an uncertain mean (CR
m
) ranging from
0.50 to 0.50log
10
and a standard deviation (CR
stdev
) of
1, thus remaining within the bounds given in previous stud-
ies. Therefore, the most likely eect is that there is no eect
from chilling while allowing for some variability.
3.2.7. Growth in the boning hall
Growth of E. coli O157:H7 may occur at various stages
along the slaughter line. The boning hall in particular has
proven to be an area where signicant growth can occur.
Growth of generic E. coli has been shown to occur at this
stage (McEvoy et al., 2003) with a mean increase of
approximately 0.33log
10
. Sheridan et al. (1992) reported
that the level of contamination on the beef cuts as a result
of boning was related to the amount of trimming and
work-up the cuts received. The study also found that both
surfaces and personnel were sources of contamination of
the meat. While growth may occur during boning other
research has suggested that the prevalence does not
increase following the process (McEvoy et al., 2003). Bon-
ing halls are typically kept at 10 C, but there may be large
variations around this. Roberts et al. (1999) modelled the
growth during fabrication as a normal distribution with a
mean of 1 and a standard deviation of 0.5. Cassin et al.
(1998) modelled growth during processing in terms of gen-
erations, using a triangular distribution with a minimum of
2, most likely of 0 and a maximum of 5 generations of
growth. The latter represents a growth of approximately
1.50logs. A study of four abattoirs found an increase in
generic E. coli ranging from 0 to 2.00log
10
(Gill, 1999).
In the model developed in this study, growth (G) was mod-
elled using a triangular distribution with a minimum of
146 E. Cummins et al. / Meat Science 79 (2008) 139154
0logs of growth, most likely value of 0.33 and a maximum
growth of 2.00logs, in line with published literature from
Gill (1999) and Sheridan et al. (1992) and remaining within
the bounds indicated by other authors (Cassin et al., 1998;
McEvoy et al., 2003; Roberts et al., 1999).
3.2.8. Contamination of carcasses
The contamination level on a carcass can be calculated
following dehiding, washing, chilling and boning out oper-
ations by combining the eects of successive operations on
bacterial counts. The number of organisms will depend on
the source of contamination, for example the carcass may
have been contaminated during dehiding, evisceration or
both operations. The number of organisms (log
10
CFU/
carcass) following contamination after dehiding (N
d
) is
given as
N
d
B
c;h
D1 D2 CR G: 8
The number of organisms (log
10
CFU/carcass) following
contamination after evisceration (N
e
) is represented by
N
e
B
c;e
D1 D2 CR G: 9
If the carcass is contaminated from both sources (N
b
), the
number of organisms (log
10
CFU/carcass) is given as
N
b
log10
B
c;h
10
D1
10
Bc;e
D2 CR G: 10
The log number of bacteria per unit area (density) on con-
taminated carcasses can therefore be calculated, again
depending on the initial source of cross-contamination.
The density (log
10
CFU/cm
2
) on a carcass contaminated
from the hide (n
d
) is given as
n
d
log
10
N
d
A
_ _
: 11
The density (log
10
CFU/cm
2
) on a carcass contaminated
during evisceration (n
e
) is given as
n
e
log
10
N
e
A
_ _
12
while the density (log
10
CFU/cm
2
) on a carcass contami-
nated from both sources (n
b
) is given as
n
b
Log
10
N
b
A
_ _
: 13
These calculations and the distributions used are summa-
rised in Table 3.
3.3. Trimmings production module
3.3.1. Boxes of trimmings
In Irish abattoirs, beef trimmings are separated from
beef primals in the boning hall and boxed in cardboard
boxes at a xed mass (M) of 27.5 kg. As part of this study,
a survey was conducted to estimate a distribution for:
1. the number of 70% visually lean (70VL) trimmings
removed from a side of beef,
2. the number of trimmings it takes to ll a 27.5 kg box,
3. the weight of 70VL trimmings,
4. surface area of 70VL trimmings.
The number of 70VL trimmings removed per carcass
(N
c
) was modelled using a triangular distribution. Each
side of a carcass consistently produces three pieces of
70VL trimmings consisting of, what is referred to in the
industry as, the plate and the Jacobs ladder (part of the
M. serratus ventralis) from the fore-quarter and one piece
from the hind quarter. Slight variability was allowed
around this by including a minimum of ve trimmings,
most likely of six trimmings and a maximum number of
seven 70VL trimmings per carcass.
The number of trimmings a carcass contributes to a box
(N
tc
) can vary depending on such parameters as process
speed and trim weight. In order to account for this variabil-
ity, the number of trimmings a carcass contributes to a box
was modelled using a uniform distribution with a minimum
of four trimmings and maximum equal to N
c
. The mass of
trim a carcass (denoted a) contributes to a box (M
c,a
)
can therefore be calculated by Eq. (14).
M
c;a

Ntc
i1
M
trim;i
: 14
The cumulative mass in a box (C
m
), which should never ex-
ceed 27.5 kg, is thus given by Eq. (15).
C
m

x
a1
M
c;a
: 15
The number of trimmings placed in a box is, therefore,
determined by the mass of each trimming placed in the
box, i.e. in Eq. (15), the number of trimmings (x) is selected
such that C
m
= 27.5 kg.
The mass of a 70VL trimming i (M
trim,i
) was assumed to
be normally distributed and modelled using a normal
distribution with uncertainty about the mean (M
m
) and
uncertainty about the standard deviation (M
stdev
). Both
uncertainty parameters were obtained by bootstrapping a
survey data set (n = 50). Bootstrapping is a modelling
technique commonly used to characterise the uncertainty
in a distribution (Efron & Tibshirani, 1991, 1993; Frey &
Rhodes, 1996; Frey & Burmaster, 1999; Vose, 2000).
For this model, a sample of 50 trim weights was obtained
from survey data (Table 4), while 50 Bootstrap calculations
were made to yield a mean and standard deviation for the
new Bootstrap data sets. This data set forms a Bootstrap
estimate of the true distribution; a random point is taken
from the distribution with replacement to yield 50 Boot-
strap samples. The data (n = 50) are represented as a cumu-
lative probability graph (heavy line) as shown in Fig. 6; the
Bootstrap samples (representing uncertainty in the distribu-
tion) are represented by the light lines. The mean and stan-
dard deviation of the mass of a trim was calculated for this
Bootstrap sample. Running 1000 iterations of the model
produced the Bootstrap uncertainty distribution for both
the mean and standard deviation.
E. Cummins et al. / Meat Science 79 (2008) 139154 147
The surface area of the trimmings (S
trim,i
) was estimated
from a small trial (n = 6) where the mass of individual trim-
mings was noted and the area of individual trimmings was
traced out on aluminium foil and subsequently measured.
A table of measurements is given in Table 5. A uniform dis-
tribution with a minimum of 0.10 cm
2
/g and a maximum of
0.50 cm
2
/g was used in the model to reect the large uncer-
tainty due to the small sample size. The total surface area
placed in a box by an animal (A
trim,i
) could therefore be
calculated by
A
trim;i
M
trim;i
S
trim;i
; 16
Table 3
Model inputs and distributions for simulation of carcass contamination
Parameter Symbol Distribution/model Category Units
Flag for carcass infected F
c
Binomial(1, P
c
) Variability Boolean ag
Flag for infected gut F
g
Binomial(1, P
g
) Variability Boolean ag
Initial number on hide I
h
Second-order continuous non-parametric
distribution tted to data
Variability and
uncertainty (see text)
log
10
CFU/
100 cm
2
Factor increase for test se F
i
Uniform(0.5, 1.5) Uncertainty
True number on hide I
ht
log10
IhF i
=100 Calculation log
10
CFU/
cm
2
Log factor for decrease from hide to carcass R Cumulative distribution tted to data Variability Factor
Initial number introduced during dehiding (on carcass) I
c
I
ht
R Variability log
10
CFU/
cm
2
Total contaminated surface area A 10

Triangularlog30; log300; log3000 Variability cm

2
Total organisms on contam carcass at dehiding B
c,h
log10
Ic
A Variability log
10
CFU/
carcass
Most likely reduction due to decontam D1
mm
Uniform(0.3, 0.7) Uncertainty log
10
Maximum reduction due to decontam D1
max
Uniform(0.8, 1.2) Uncertainty log
10
Decontamination D1 Triangular(0, D1
mm
, D1
max
) Variability log
10
Probability of contam at evis E 10
Uniform2; 3
Uncertainty Probability
Cut at evis ag E
f
Binomial(1, E) Variability Boolean ag
Total organisms on contam carcass due to evis B
c,e
log10
Ic
A Calculation log
10
CFU/
carcass
Most likely decontamination D2
mm
Uniform(0.3, 0.7) Uncertainty log
10
Most likely max decontamination D2
max
Uniform(0.8, 1.2) Uncertainty log
10
Decontamination (pasteurise) D2 Triangular(0, D2
mm
, D2
max
) Variability log
10
Mean change in numbers during chilling CR
m
Uniform(0.5, 0.5) Uncertainty log
10
Chill, stdev CR
stdev
1 Fixed value log
10
Chill change in numbers CR Normal(CR
m
, CR
stdev
) Variability log
10
Change in numbers in boning hall (growth) G Triangular(0, 0.33, 2) Variability log
10
Number of organisms per carcass after boning out
(contam at dehiding only)
N
d
B
c,h
D
1
D
2
+ CR + G Calculation log
10
E. coli
organisms
Number of organisms per carcass after boning out
(contam at evis only)
N
e
B
c,e
D
1
D
2
+ GR + G Calculation log
10
E. coli
organisms
Number of organisms per carcass after boning out
(contam at eviseration and dehiding)
N
f
log10
Bc;h
10
D1
10
Bc;e
D2 CR G Calculation log
10
E. coli
organisms
Density on carcass (hide only) n
d
log10
Nd
=A Calculation log
10
/cm
2
Density on carcass (evis only) n
e
log10
Ne
=A Calculation log
10
/cm
2
Density on carcass (both) n
b
log10
Nf
=A Calculation log
10
/cm
2
Table 4
A frequency analysis for the mass of a piece of 70VL ank (n = 50)
Mass of trimming (g) Number of observations
<1000 0
10002000 5
20003000 9
30004000 4
40005000 1
50006000 0
60007000 4
70008000 8
80009000 9
900010,000 5
10,00011,000 2
11,00012,000 3
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
1
0 2000 4000 6000 8000 10000 12000 14000
Trim mass (g)
C
u
m
u
l
a
t
i
v
e

p
r
o
b
a
b
i
l
i
t
y
Fig. 6. Cumulative probability distribution for trim mass with separation
of uncertainty and variability.
148 E. Cummins et al. / Meat Science 79 (2008) 139154
where i is a counter for the trimming in question, i.e.
1, 2, 3, . . .
The contaminated surface area per trim is likely to be
Poisson distributed, as the probability of a contaminated
unit area (cm
2
) is likely to be small over a large number
of observations. Hence, the expected contaminated area
per trimming (A
contam,i
) was calculated as
A
contam;i
Poisson A
trim;i

i
x0
A
contam;x
TSA

i
x0
A
trim;x
_ _ _ _
: 17
TSA is the total outside surface area of a carcass and is ta-
ken as a xed value of 32,000 cm
2
. The expected contami-
nated area (cm
2
) a carcass contributes to a box (Ac
a
) is the
sum of the contaminated trimmings that go into the box
and is given as
Ac
a

x
i0
A
contam;i
: 18
The count of E. coli O157:H7 on contaminated trimmings
will depend on the initial source of contamination (i.e. hide,
intestine or both) and is likely to be Poisson distributed, as
the number of bacteria is likely to be small in a xed spatial
area. The counts (CFU) resulting from contamination
from hide only is represented by
C
trim;i
Poisson10
n
d
A
contam;i
: 19
If contamination is only via perforation of the intestine at
evisceration the counts (CFU) on contaminated trimmings
are given as
C
trim;i
Poisson10
ne
A
contam;i
: 20
If both sources of contamination occur, the bacterial count
(CFU) is given as
C
trim;i
Poisson10
n
b
A
contam;i
: 21
The total bacterial load (TBL) in a box of trimmings can
also be calculated by summing the total bacterial load of
each trimming from each carcass that contributes to a
box and is given as
TBL

x
a1

Nt
i1
C
trim;a;i
: 22
A count of the number of infected trimmings (I
t
) can there-
fore be obtained from the simulation by counting the num-
ber of trimmings which have a count greater than zero. An
estimate of the prevalence of contaminated trimmings can
be calculated by dividing the number of infected trimmings
by the total trimmings produced (N
t
). The model makes use
of the central limit theorem to create an uncertainty distri-
bution around this prevalence. The central limit theorem
states that the mean of a set of n variables drawn indepen-
dently from the same distribution will be normally distrib-
uted. It follows from this that the sum of n variables drawn
independently from the same distribution has an uncer-
tainty distribution of the form Normalnl;

n
p
r.
The mean (TC
m
) and standard deviation (TC
stdev
) for
the number of trimmings per carcass can be calculated
from the distribution used for N
c
. The total trimmings pro-
duced (T
p
) can therefore be calculated using the central
limit theorem and is given as
T
p
normalA
s
TC
m
;

A
s
_
TC
stdev
: 23
The probability that a contaminated carcass will produce a
contaminated trimming (P
c
) is calculated from the model
by setting F
c
to a value of 1 and running the model for
10,000 iterations. Recall that F
c
is a Boolean ag indicating
whether a carcass is contaminated or not. By setting F
c
to a
value of 1, the model is eectively calculating the probabil-
ity that an infected carcass (i.e. F
c
= 1) will produce an in-
fected trimming (i.e. P
c
). The total contaminated trimmings
(T
ip
) can therefore be calculated as
T
ip
binomialnormalC
c
TC
m
;

C
c
_
TC
stdev
; P
c
:
24
The distributions and calculations used in this section of
the model are summarised in Table 6.
3.4. Model run and outputs
The input parameters were combined into a spreadsheet
(Microsoft Excel 2000) running the @Risk add-on package
(Palisade Software, Neweld, USA). The simulation was
run with 10,000 iterations of the model using Latin Hyper-
cube sampling and run initially without any separation of
uncertainty and variability. Outputs from the model are
distributions describing the prevalence and counts of
E. coli O157:H7 in beef trimmings destined for processing
into saleable products such as minced meat and beef bur-
gers. A table of the outputs recorded is given in Table 7.
In an attempt to identify the specic uncertainty param-
eters responsible for the wide spread of the probability
distributions for both prevalence and counts, a sensitivity
analysis was performed using the Spearmans rank order
correlation coecient. A sensitivity analysis is a systematic
evaluation of model inputs and assumptions. The parame-
ters are ranked in accordance with the magnitude of eect
the parameters are having on model predictions.
3.5. Partial validation
Validation is necessary to ensure model predictions are
realistic and also provides justication for model inputs.
Table 5
Surface area measurement of 70VL beef trimmings (n = 6)
Trimming Mass (g) Area (m
2
) Area/unit mass (cm
2
/g)
1 3925 0.10 0.25
2 2235 0.07 0.32
3 2350 0.09 0.38
4 1830 0.09 0.48
5 4418 0.22 0.50
6 4018 0.20 0.50
E. Cummins et al. / Meat Science 79 (2008) 139154 149
The validation stage for this model consisted of a survey of
the prevalence and counts of E. coli O157:H7 on beef
trimmings produced in an Irish abattoir and involved the
sampling of 1351 beef trimmings and testing for E. coli
O157:H7 contamination followed by enumeration where
possible. Ideally validation would involve multiple compar-
isons between model outputs and real data. However, this
is unlikely to be unfeasible in the food industry. Hence the
survey conducted by Carney et al. (2006) can be considered
a partial validation stage, providing snap shot comparison
between model predictions and real data. Survey results,
materials and methods for detecting bacterial are discussed
in Carney et al. (2006). The survey resulted in 32 positive
samples. Uncertainty around this data were modelled using
a beta distribution (beta(32 + 1, 1351 32 + 1)), thus,
allowing for comparison and partial validation with model
predictions.
3.6. Uncertainty
The inuence of uncertainty can be assessed by running
the model while xing on one random value from the
uncertainly distributions for each simulation and sampling
from the variability distributions for successive iterations
within that simulation (i.e. second-order modelling). To
interpret the outcomes, the resulting simulations can be
plotted alongside a cumulative plot of the output without
any separation of uncertainty and variability. The spread
in the distribution will indicate whether uncertainty or var-
iability is dominating the model. If uncertainty is the dom-
inant force, a cumulative plot of successive simulation
results will be almost perpendicular, intersecting the cumu-
lative graph where no separation has occurred. If variabil-
ity is the dominant force, a plot of successive simulations
will take a similar line to the graph where uncertainty has
not been separated. To simulate the role uncertainty was
playing in this model, a separate model run with 10,000
iterations (representing variability) and 1000 simulations
(representing uncertainty) was carried out.
4. Results
A plot of the simulated prevalence of E. coli O157:H7 in
Irish beef trimmings compared with survey results is given
in Fig. 7. The mean calculated prevalence of contaminated
trimmings was 2.36% with 90th percentile range between
Table 6
Summary of inputs used for simulating trimming contamination
Parameter Symbol Distribution/model Category Units
Mean mass of trimming (70VL) M
m
Bootstrap on data set (see text) Uncertainty g
Standard deviation for mass trimming M
stdev
Bootstrap on data set (see text) Uncertainty g
Mass of trimming (70VL) M
trim,i
Normal(M
m
, M
stdev
, Truncate(2000)) Variability g
Total scrap wt, Mass of trim a carcass contributes to a box M
c,a

Ntc
i1
M
trim;i
g
Cumulative mass in box C
m

a1
x M
c;a
g
Number of trimming per carcass (70VL) N
c
Triangular(5, 6, 7) Variability Trimmings
Number of trimmings a carcass contributes to a box N
tc
Uniform(4, N
c
) Variability Trimmings
Surface area of trim Sa
trim,i
Uniform(0.1, 0.5) Uncertainty cm
2
/g
Total cm
2
placed in a box by animal A
trim,i
M
trim,i
Sa
trim,i
cm
2
Expected number of contaminated cm
2
per trimming A
contam,i
Poisson A
trim;i

i
x0
Acontam;x
TSA

i
x0
Atrim;x
_ _ _ _
Variability cm
2
Expected number of contaminated cm
2
a carcass contributes
to a box
Ac
a

x
i0
A
contam;i
Calculation cm
2
E. coli numbers, hide only C
trim,i
Poisson(10
nd
A
contam,i
) Variability CFU
E. coli numbers, gut only C
trim,i
Poisson(10
ne
A
contam,i
) Variability CFU
E. coli numbers, both C
trim,i
Poisson(10
nf
A
contam,i
) Variability CFU
Infected trimmings I
t
Count if (C
trim
> 0) Calculation Trimmings
Total E. coli in combi

x
a1

Nt
i1
C
trim;a;i
Calculation CFU
Mean trimmings per carcass TC
m
From N
c
distribution Trimmings
Standard deviation of trimmings per carcass TC
stdev
From N
c
distribution Trimmings
Total trimmings produced T
p
Normal(A
s
TC
m
, SQRT(A
s
) TC
stdev
) Trimmings
Probability that a contaminated carcass will produce a
contaminated trim
P
c
Procedure in model, see text Probability
Total infected trimmings T
ip
Binomial(Normal(C
c
TC
m
,
SQRT(C
c
) TC
stdev
), P
c
)
Trimmings
Table 7
Summary of simulated model outputs
Parameter Symbol Distribution/model Category Units
Total number of trimmings produced N
t
i such that

Ntc
i1
M
trim;i
6 M Output Trimmings
Prevalence of infected trimmings P N
t
/I
t
Output Prevalence
Uncertainty distribution for contaminated trimmings P T
p
/T
ip
Output Prevalence
Counts of E. coli on contam trimmings C C
trim,i
/M
trim,i
Output CFU/g
150 E. Cummins et al. / Meat Science 79 (2008) 139154
1.00% and 5.00%. The parallel validation study also estab-
lished a prevalence of 2.37% (32/1351) which provides
some condence in the model predictions. However, as
can be seen in Fig. 7, the condence bounds for the simu-
lation are much wider due to parameter uncertainty.
Results from the second-order model are presented in
Fig. 8. Each light line represents an individual simulation,
while the heavy line represents the scenario with no separa-
tion of uncertainty or variability (i.e. cumulative distribu-
tion of Fig. 7). The spread of the distribution indicates
that the main driving parameters in the model are the
uncertainty parameters and better understanding of the
system dynamics may be achieved by reducing this uncer-
tainty of the model parameters. The wide spread and
almost vertical lines intersecting the cumulative plot
(Fig. 8) with no separation (heavy line) indicates that var-
iability is having very little impact on model predictions
and the model uncertainty is the main driving force and
is responsible for the wide distribution spread.
The calculated mean number of counts of E. coli
O157:H7 on contaminated trimmings was 2.69log
10
CFU/g, yet the model highlighted that much higher counts
are possible (Fig. 9). The contaminated trim samples which
were enumerated in the surveillance survey varied from
0.70 to 1.61log
10
CFU/g (Carney et al., 2006). The sensitiv-
ity of the prevalence and counts of E. coli O157:H7 on
contaminated trimmings to input values were measured
by Spearmans rank order correlation. The analysis
indicated the inputs having the greatest impact on contam-
inated trimmings prevalence were: test sensitivity (T
se
), hide
to carcass transfer rate (TR), initial hide prevalence (P
h
)
and the decontamination treatment (D
1max
), with Spear-
mans rank order correlation coecients of: 0.27, 0.26,
0.20 and 0.12, respectively. The parameters having the
greatest impact on hide counts were: initial count on
bovine hides (I
h
); the contaminated surface area (A); the
decrease from hide to carcass (R), with Spearmans rank
order correlations of: 016, 0.07, 0.07 and 0.05,
respectively.
5. Discussion
The observed prevalence of contaminated trimmings
(2.36%) is similar to the prevalence reported for minced
beef products, i.e. 2.80% (Cagney et al., 2004), which high-
lights the likely transfer of contaminated beef trimmings
into the food chain in the form of comminuted beef prod-
ucts. The mean values for the prevalence of contaminated
trimmings from the simulation and the survey (2.37%)
are similar, even though the simulated distribution is con-
siderably wider, highlighting the uncertainty of the input
parameters.
Simulated counts include situations where the simulated
value is less than the detection limit of the direct plate
method (i.e. <0.70log
10
units). Therefore, this has the eect
of pulling the graph in Fig. 9 to the left. The enumeration
technique of direct plating onto CT-SMAC as used by Car-
ney et al. (2006) is not sensitive at low concentrations. As a
Survey
Mean=0.0251
Simulation
Mean=0.024
X <=0.01
2.5%
X <=0.05
97.5%
0
10
20
30
40
50
60
70
80
0.00 0.02 0.05 0.07
Prevalence
P
r
o
b
a
b
i
l
i
t
y

D
e
n
s
i
t
y
Fig. 7. Simulation vs. survey results (including uncertainty analysis) for
the prevalence of E. coli O157:H7 on beef trimmings.
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
1
0 0.01 0.02 0.03 0.04 0.05 0.06 0.07
Prevalence
C
u
m
u
l
a
t
i
v
e

P
r
o
b
a
b
i
l
i
t
y
Fig. 8. Second-order cumulative probability for the prevalence of E. coli
O157:H7 on beef trimmings. (Heavy line represents no separation of
uncertainty and variability; thin lines represent successive simulations with
separation of uncertainty and variability).
Mean = -2.69
X <=-0.55
95%
X <=-4.14
5%
0
0.1
0.2
0.3
0.4
0.5
0.6
-5 -4 -3 -2 -1 0 1 2
Counts (Log
10
CFU/g)
P
r
o
b
a
b
i
l
i
t
y

D
e
n
s
i
t
y
Fig. 9. Simulated counts of E. coli O157:H7 on contaminated beef
trimmings.
E. Cummins et al. / Meat Science 79 (2008) 139154 151
result, in most samples (25/32 of the beef trimming sam-
ples) the pathogen was detectable by enrichment only, sug-
gesting that the pathogen numbers are low i.e. <0.70log
10
units. This substantiates the models low estimate for bacte-
rial contamination on beef trimmings and provides some
condence in model results. However, given the estimated
small dose required to cause illness resulting from the
ingestion of E. coli O157:H7 (Cassin et al., 1998), these pre-
dictions may be a cause for concern. Cognisance needs to
be made of the impact of model assumptions as detailed
in Section 2.3, many of which tend to err on the side of cau-
tion, while also recognising that a change in these assump-
tions may yield dierent results.
The sensitivity analysis reveals the need for further
research; in particular, the analysis reveals the need for fur-
ther experimental work to reduce the uncertainty about the
microbial test sensitivity (T
se
). In addition, further research
should be directed at reducing cross-contamination at the
hide removal stage thus reducing TR. The fact that the ini-
tial microbial counts on animal hides (I
h
) and the initial
prevalence on animal hides (P
h
) are ranked highly in the
sensitivity analyses highlights the importance of minimising
microbial contamination of animals when presented for
slaughter. Possible interventions can be devised from con-
trollable variables which have a large impact on model pre-
dictions, for example reducing cross-contamination at the
hide removal stage, or reducing prevalence and counts on
bovine hides on entry into the plant. The analysis reveals
that additional eorts are also needed to understand the
processes involved in the initial transfer of E. coli to the
carcass and to reduce or limit such a transfer; this has also
been highlighted by McEvoy et al. (2001).
Hide prevalence was signicantly correlated with carcass
contamination, indicating a role for the control of E. coli
O157:H7 in live cattle; this is in agreement with previously
published surveillance studies (Elder et al., 2000). The anal-
ysis also reveals the impact successive decontamination
treatments may have on reducing bacterial contamination.
This supports the concept of using decontamination pro-
cesses in meat plants as a means of improving microbiolog-
ical quality of beef products. Measures used in the abattoir
may represent an important initial barrier in protecting
beef from contamination, and thus reducing human expo-
sure to E. coli O157:H7 through the food chain.
The initial count on the animal hide (I
h
) was the param-
eter having the greatest impact on count predictions in the
model, highlighting the need to investigate the uncertainty
about this parameter. The contaminated surface area (A)
and decrease from hide to carcass (R) were also having
an impact on model predictions, highlighting the increased
requirement to better understand microbial transfer
dynamics. Other input parameters in the model had a smal-
ler eect on model predictions.
The qualitative and quantitative validation data
obtained about E. coli O157:H7 on beef trimmings during
the parallel surveillance study and detailed in Carney et al.
(2006) provided a sound microbiological basis for the par-
tial validation of this risk assessment model, which is essen-
tial but currently rare in this area. The model ts well with
observed data suggesting that the mathematical approxi-
mations of all real life variables are justied while also
highlighting the impact of model assumptions and uncer-
tainty, as seem from the wide distribution for the simulated
data. The model validation provides sucient condence
that the model can be considered valid for estimating the
likely prevalence of contaminated trimmings in beef abatt-
oirs and estimating the likely bacterial counts on contami-
nated trimmings.
6. Conclusions
The model developed in this study predicted the preva-
lence and counts of E. coli O157:H7 in Irish beef trimmings
and provided partial validation of the results with reference
to an extensive parallel survey carried out at a commercial
abattoir in Ireland and conducted by Carney et al. (2006),
thus providing a degree of condence in model predictions.
The probability distributions used in the model allowed
quantication of inputs that are not well characterised
due to lack of knowledge (uncertainty) and model inputs
that are heterogeneous (variable). The model encompasses
available information about the processing, treatment and
production of beef trimmings and model results indicate
that there may be cause for concern if E. coli counts are
not reduced at a later stage during processing. The model
can play a vital role in the control and management of
food-borne hazards, such as E. coli O157:H7, and result
in an increased understanding of bacterial transmission
and exposure pathways.
Results need to be viewed in the context of uncertainties
and assumptions, which are implicit in the structure of
these models. Dierent model assumption can have an
eect on the results obtained in risk assessments, highlight-
ing the issue of model uncertainty. However, such assump-
tions tend to err on the side of caution, thus providing an
upper estimate of risk. Model complexity can be an issue
for those not familiar with the modelling process. This
highlights the need for clear, unambiguous descriptions
of model inputs, associated uncertainties and assumptions
to ensure transparency of the model and research process.
A sensitivity analysis provides a systematic and trans-
parent tool for exploring assumptions in risk assessment
procedures. Risk managers will be interested in the sensitiv-
ity analysis as it reveals the eects the input parameters
have on model predictions and where further resources
should be directed towards reducing model uncertainty
and improving model accuracy. The model can also pro-
vide an appropriate decision support tool aiding risk miti-
gation strategies in the slaughter plant in an eort to
protect human health. Model validation is an important
component of this exercise; given the comparability
between model predictions and survey results, the use of
the input distributions seems justied. The model is an
appropriate decision-support tool representing current sci-
152 E. Cummins et al. / Meat Science 79 (2008) 139154
entic knowledge with regard to the slaughter process. The
model highlights the need for further research in the area of
process simulation and microbial risk assessment.
Acknowledgements
The authors acknowledge the Department of Agricul-
ture for their funding of this project under the Food Insti-
tute Research Measure.
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