Food Control 29 (2013) 221e225
Contents lists available at SciVerse ScienceDirect
Food Control
journal homepage: www.elsevier.com/locate/foodcont
Relating the biotracing concept to practices in food safety
Anca Ioana Nicolau a, *, Gary C. Barker b, Iuliana Aprodu a, Martin Wagner c
a
Faculty of Food Science and Engineering, “Dunarea de Jos” University of Galati, 111 Domneasca Street, 800201 Galati, Romania
Institute of Food Research, Norwich Research Park, Norwich, United Kingdom
c
Institute for Milk Hygiene, Department for Farm Animals and Veterinary Public Health, Vienna, Austria
b
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 23 December 2011
Received in revised form
27 April 2012
Accepted 9 May 2012
Biotracing, a new method developed to assist with food chain management and to control food safety, is
presented to highlight practical considerations, including logistic issues for its implementation. The main
differences between traceability and biotracing and between predictive microbiology and biotracing are
explained and examples of situations in which biotracing could be of real help are listed (foodborne
outbreaks, liability issues, HACCP, risk evaluation and decision making, education and training). Indications on how to access and interrogate two prototype models, called SimpleTrace and SimpleMatch,
as well as some other Bayesian networks, are given to encourage using of biotracing, while operational
biotracing is illustrated by an agent based model called AgentChain. The main types of inferences, which
point to sources that generate potential problems within a particular food chain, are revealed. Biotracing
is strongly recommended for introduction into continuous operations that include in line data collection,
and can be operated, alongside existing safety systems, without additional burden.
Ó 2012 Elsevier Ltd. All rights reserved.
Keywords:
Biotracing
Food safety
Liability
HACCP
Risk analysis
Outbreaks
Inferences
1. Introduction
Defined as “the ability to use down stream information to point
to materials, processes or actions within a particular food chain that
can be identified as the source of undesirable agents” (Barker,
Gomez, & Smid, 2009) or shorter “the ability to identify the sources of microbial contamination in a food chain” (Smid, Swart,
Havelaar, & Pielaat, 2011), biotracing/biotraceability is a new
research area that is fast developing and will soon become an
essential tool to assist food safety specialists in quantitative
assessment of microbial hazards. Although biotracing is strongly
connected with risk assessment, and takes a comparable system
wide view of contamination hazards, it concentrates on the identification of sources and origins rather than on the quantification of
end effects (see e.g. www.biotracer.org). In this respect biotracing is
a substantial addition to the food chain management process as it
supports decision making and targeted actions. Source tracing has
recently been identified as a powerful addition in many areas of
microbiological investigations (Dance, 2008).
Although predictive microbiology is an important element of
biotracing (Hoorfar, Wagner, Jordan, Boquin, & Skiby, 2011),
predictive microbiology and biotraceability are different concepts
(Table 1). Both use mathematical models for predictions and hence
imply a detailed knowledge of the microbial ecology and
* Corresponding author. Tel.: þ40 (0)336 130 177; fax: þ40 004 0236 460 165.
E-mail address: anca.nicolau@ugal.ro (A.I. Nicolau).
0956-7135/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.foodcont.2012.05.020
environment, but predictive microbiology estimates the growth,
survival or death of microorganisms (Ross & McMeekin, 2003),
while biotracing expresses posterior beliefs about possible microbial origins or causes of growth (sources) (Smid, Verloo, Barker, &
Havelaar, 2010). In this respect it is possible to consider predictive microbiology and biotracing as two sides of a coin, one causal
and one inferential, that relate to the population dynamics for
bacterial populations (and other agents) within a well defined food
chain system.
When compared to the traditional tracing process (Table 1),
which mainly involves monitoring, record keeping and summarizing permanent information on a label or tag, the biotracing
process is clearly distinct and complementary: biotracing establishes an information set and a belief system that can support the
identification or prioritization of potential initiation points or
processes based on uncertain detection of hazards or hazard
markers (Barker et al., 2009).
In addition to communication of the biotracing concept, to
producers, traders and decision-makers, this paper adds to the
development of biotraceability as a discipline and emphasizes its
potential as investigational and educational tool.
2. Biotracing models
In practice biotracing is highly multidisciplinary and involves
a strong integration of food chain and microbiological expertise
with mathematical modeling. As well as recently published models
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A.I. Nicolau et al. / Food Control 29 (2013) 221e225
Table 1
Differences between traceability, biotraceability and predictive microbiology.
Traceability
Biotraceability
Predictive modeling
Relationship to food chain
Capabilities
Compulsory along the food chain
Able to identify origins, to establish
the history of a food product (showing
from where the food comes) and track
the process
Complementary
Able to predict micro-organism
development (estimating cell
numbers) and indicate potential
problems
Supported by
Codes on labels or tags
Data collected by
Monitoring and recording
Data format
Non-standardized, although increasing
uniformity
Relational
Complementary
Able to identify, assess and
rank vulnerabilities in the
food chain (revealing where
did the problem arise and
what was the most probable cause
Surveillance, information technology
and statistical inference
Multiple information streams from
biology, process and historical record
Probabilistic formulation of evidence,
Bayesian interpretation of beliefs
Inferential
Character
that describe biotracing for Salmonella in the pork chain (Smid
et al., 2011), and Staphylococcus aureus in the milk chain (Barker
& Gomez-Tome, 2011) other models currently being developed
include Salmonella in the feed chain and Listeria in cheese. Additionally several models that partially express biotracing ideas have
been published including source tracing for foodborne norovirus
(Verhoef et al., 2010) and for Listeria in Gorgonzola cheese
(Lomonaco et al., 2009).
Operational biotracing involves significant efforts and developments in techniques for sampling, analysis and diagnostic
modeling. These advances have resulted from massively improved
rapid (molecular) methods for identification and enumeration of
bacteria, e.g. Fourier transform infrared microscopy (Carlos,
Maretto, Poppi, Sato, & Ottoboni, 2011), and molecular typing
methods (Foley, Lynne, & Nayak, 2009). Additionally biotracing
often includes an emerging use of advanced (Bayesian) computational methods for inference (Jarman et al., 2008).
Two simple computational models, called SimpleTrace and
SimpleMatch, have been used to illustrate the biotracing concept
and to identify distinct patterns and motifs that are important in
food chain biotracing. SimpleTrace is based on Bayesian inference
within a well defined chain of uncertain events, while SimpleMatch is based on the statistics of type matching within a system of
agent types and uncertain sources (See Table 2).
These models, and some other Bayesian networks, are fully
documented and can be accessed and interrogated on a development website hosted by HUGIN BIOTRACER (http://bbn.ifr.ac.uk). In
very simple terms each of these models allows a user to use an
observation (down stream information) to establish belief (posterior probability) about whether particular sources were significant
in leading to the evidence. Both these schemes rely on Bayesian
inference and both operate, consistently, even when information is
incomplete or uncertain. In practical situations the inversion of
causal reasoning, SimpleTrace, is often the easiest scheme to
Historical data supplies and
mathematical models
Microbiological experiments
and analysis
Standardized and organized as
searchable databases
Causal
interpret but, with an increasing ability to type and subtype
harmful agents (particularly bacteria) the matching process may
become the dominant biotracing process in the future. These two
models illustrate an important property of operational biotracing;
they can be used, consistently, with sequential pieces of evidence
without ongoing development. However, in practice, it is often
straight forward to employ a data stream both as a continuous
source of evidence to identify problematic sources and also as
support for a developing model that either increases confidence in
inference or accommodates slow trends in the data supply.
Computer learning techniques are compatible with the Bayesian
network structures used to implement biotracing.
The complex nature of decisions that surround food chain
management, and hence operational biotracing, are illustrated by
an agent based model, called AgentChain (See Table 2), that can be
accessed and interrogated online (http://bbn.ifr.ac.uk). The
AgentChain system includes spatially distinct chains, stochastic
sources of agents, operational hurdles, batch partition, unit
dispersion, agent population kinetics, unit consumption events,
doseeresponse behavior and case identifications. The system is
augmented by agent typing, record keeping and event monitors.
This model shows that the sampling frequency and the decision
taken on actionable evidence contribute to overall efficiency and
safety of a process but that overall optimization is a complex task
that could be aided by biotracing information.
3. Sources and inferences
In practice biotracing often begins with the identification and
definition of sources that characterize potential problems within
a particular food chain. The identification of sources is the first step
to the realization of a biotracing question e what is the most likely
place that an observed problem has arisen. Within the context of
biotracing a ‘source’ is quite loosely defined. Whilst it is clear that in
Table 2
Simple models illustrating biotracing operations.
Model
Model type
Location
Biotracing principal illustrated
Example application
SimpleTrace
Bayesian network
1
Inverting chain probabilities
SimpleMatch
Bayesian Network
2
Statistics of type matches
AgentChain
Agent based simulation
3
Complex optimization
Separation of milk chain sources
based on coupled measurements
of enzymes and bacteria
Elimination of food handler sources
based on type mismatches
Designing sample frequency to achieve
an optimum chain efficiency and safety
1 e http://bbn.ifr.ac.uk/btmodeller/index.php/SimpleTrace.
2 e http://bbn.ifr.ac.uk/btmodeller/index.php/SimpleMatch.
3 e http://bbn.ifr.ac.uk/gary/biotracer/agentchain/Chain6.html.
A.I. Nicolau et al. / Food Control 29 (2013) 221e225
some cases individual materials or ingredients might carry exceptional bacterial loads and therefore act as sources of contamination
problems it is equally possible that manufacturing processes that
are designed to reduce load might not operate fully and so also
manifest as a contamination sources. In this way the biotracing
sources, to some extent, parallel the initial loads and reduction
steps included in a safety assessment that involves a food safety
objective (Gorris, 2005). For biotracing sources can be effectively
grouped together, e.g. all the post process contamination opportunities might initially be collected as a single source, and should be
exclusive; but not necessarily exhaustive (that is each source can be
identified only once in the list of sources but there might be
unknown sources that are not identified in the list).
In practice the inference step is a process of assigning probabilities to the sources based on evaluation of observed evidence. In
the majority of normal operating conditions the ‘posterior’ probabilities are not significantly different from those that represented
initial (prior) beliefs and are included in the biotracing model.
However, exceptionally, evidence arises that expresses increased
probabilities for one (or more) sources. The significant change in
probability is a ‘biotrace’. In practice, largely based on legal precedent, the posterior probability is converted to another measure,
called the likelihood ratio, as the basis for decision making (Taroni,
Aitken, Garbolino, & Biedermann, 2006).
The identification of sources and evaluation of posterior probabilities is sufficient to answer questions that relate to the sources
of contamination hazards. Typical questions include: “for a set of
possible sources, which is the most likely cause of actionable
evidence?”; “for a particular source is the likelihood of initiating
a hazard acceptable?”; “does evidence support the existence of
unidentified sources?” and “for a particular source does evidence
indicate fluctuations or a significant trend?”. In initial biotracing
applications the first question has dominated.
4. Applications of biotracing
Biotracing has a multitude of potential applications. Some
situations in which biotracing could help are presented below:
4.1. Foodborne outbreaks
Public health investigations often trace an outbreak of foodborne illness to a particular food or to a specific geographical
source. The trace is often based on consumption patterns alone but
sometimes is based on a matching process for the pathogen of
concern. Although this trace is sufficient to prevent escalation or
immediate repeat it is often not enough to identify a particular
ingredient or process failure as the source of problems. In this
respect the trace is often the precursor for much larger and more
expensive investigations to seek the root cause of the problem.
Food chain biotracing can go further by including evidence from
contamination levels or typing, collected as part of an epidemiological process, into an inference scheme that targets further
investigation on particular food chain operations.
For a recent outbreak of staphylococcal food poisoning in
Austria, arising from School milk (Schmid et al., 2009), it is clear
that a biotracing model, such as the one published by Barker and
Gomez-Tome (2011), would have rapidly indicated post process
contamination at the dairy as the most likely source of problems.
4.2. Liability issues
Although not directly identified with food safety the process of
assigning liability is a strong influence of the development of food
safety procedures and it is clear that biotracing can influence this
223
process. A mathematical model which connects the transfer of
liability with biotracing and indicates a global improvement of food
safety as a consequence has been developed by Pouliot and Sumner
(2008). In such cases a biotrace acts as a silent witness but in other
situations, such as those involving feed and food liability insurance,
could support decisions regarding payments.
4.3. Hazard analysis and critical control points(HACCP)
Despite the fact that HACCP has been in use for more than 50
years and is recognized as the most effective approach available for
producing safe food, it is still a challenge for food companies. More
than that, specialists often identify errors at the operational level of
many HACCP systems indicating misinterpretation and implementation problems. Critical limits are one of the specific errors
made by food companies in their self-monitoring plans designed
using the HACCP method (Panunzio, Antoniciello, Pisano, & Rosa,
2007). In such cases, biotracing models may assist food specialists
in making calculations for resetting critical limits of microbiological
parameters that are crucial for safety of a particular food
manufacturing process.
4.4. Risk evaluations/decision making
It is clear that biotracing is closely related to risk assessments
and, in practice, is driven by similar information supplies and
understanding e the hazard domain. However the increased
sensitivity of monitors (particularly those based on PCR type
techniques) and the increased ability to reason in uncertain
situations, that is brought about by systematic application of
Bayes theorem and machine learning, ensures that additional
decision opportunities arise from a biotracing approach. Decision
processes based on risk assessment usually use a threshold for
a particular endpoint measure as the trigger for particular action;
most visible a shutdown and recall. In contrast a biotracing
system might define action levels based on posterior beliefs
about sources and hence may pre-empt more intrusive interventions based on endpoints. This preventative or corrective
possibility is particularly attractive to decision makers and,
potentially, provides an important commercial advantage that can
drive the uptake of biotracing.
In this respect it is clear that biotracing schemes may also
extend the decision process to make use of additional endpoint
observations, not necessarily those directly related to food safety, as
these may provide evidence that is more easily accessible (i.e.
markers) and can support source level inference (Jordan, Wagner, &
Hoorfar, 2011). In the future it may become possible to incorporate
biotracing at the point of process design to ensure that contamination problems are immediately traceable and unintrusive intervention is possible without safety endpoints moving out of the
allowable range.
4.5. Education and training
Biotracing can make a significant contribution to education and
training for food professionals. Biotracing, uniquely, emphasizes
causes rather than effects for food hazards and, therefore, is more
directly related to practical considerations and prevention rather
than detection and remedial processes. When revealing the cause
of a certain microbiological effect that is observed at the endpoint
or delivery point of production, students and operators learning
about food safety will understand better the importance of
correctly executing particular operations to maintain food safety.
Nowadays, it is well recognized the importance of education and
training in performing correct actions related to food production,
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A.I. Nicolau et al. / Food Control 29 (2013) 221e225
Fig. 1. Biotracing in action: the endpoint is passed through the core biotrace to discriminate among sources and to detect both critical and operating problems.
processing, storage, transport and distribution. Simple prototype
implementations, such as SimpleTrace and SimpleMatch, highlight the causal nature involved with biotracing and can act as
strong communications tools.
5. Logistic issues for implementation of biotracing
The statistical inference that is the core of a biotrace is only one
part of a biotracing system that can support improved safety in food
chain operations. In practice biotracing involves monitors, alerts,
Data from
QC and
HACCP
Data from
QC and
HACCP
Data from
QC and
HACCP
Biotrace 1
Biotrace 2
Biotrace 3
Farm
Food Plant
Market
Safe product
Consumer
Core biotrace (mathematical model displaying posterior probabilities or likelihood ratios)
Operational biotrace (decision taken to assure the food products safety)
Fig. 2. Biotracing in food chain configurations; input data streams are linked by biotracing activities.
A.I. Nicolau et al. / Food Control 29 (2013) 221e225
data collection, decision support and many other activities.
However the biotracing concept remains simple e an output signal
is analyzed to discriminate between different components of the
input (Fig. 1). Biotracing acts as an accumulator of information and
so it is practical for beliefs developed from one tracing operation to
behave as inputs to further biotracing; in operational systems
different biotracing activities might link along a food chain (Fig. 2).
Biotracing is ideally suited to operations that include continuous,
in line, data collection. Each new datum can be used automatically to
evaluate sources and, in the majority of cases, this will lead to beliefs
that no actions are required. However, by using computational
techniques usually called ‘machine learning’, the information
stream can be used to reduce uncertainties associated with normal
chain operations, in so doing, lead to increased confidence in beliefs
that indicate abnormal behavior. The learning process can also be
configured to account for trends and slow variations, such as seasonality, that sometimes mask significant deviations.
6. Conclusions
The case for the introduction of biotracing into food chain
management is clear: an effective efficient use of information that
helps to eliminate or reduce the uncertainty associated with decisions taken in relation to safety in the food chain. The opportunity
for the development has arisen, recently, because of advances in
rapid methods for detection and enumeration of organisms and
markers and because of significant changes in the collection,
storage and manipulation of large volumes of data relating to food
manufacture. Increasingly it is apparent that biotracing can also
have commercial benefits; after an initial implementation a biotracing system can be operated, alongside existing safety systems,
without additional burden and, in practice, may offset substantial
costs of chain closure and product recall by indicating targeted preemptive in operation actions.
Development of detailed biotracing models includes substantial
food chain and microbiological expertise whereas, in other fields,
many Bayesian networks are constructed directly from case databases using a computer learning process. As the digital environment for food manufacturing expands the data driven approach to
development of biotracing will be increasingly practical. A series of
bacterial and physical measurements at strategic time points in
a manufacturing process may be used to represent a single ‘case’
and a case database with a few hundred records may be sufficient
to capture important correlations and deviations from normal
behavior. Machine learning methods may have increasing significance particularly in relation to high throughput data sources that
are increasingly relevant to food safety management.
Some research units across Europe are already prepared to start
tracing pathogens in specific food chains; these include red meat
and game, dairy, fish and shellfish.
225
Acknowledgments
The work was supported by the European Union-funded Integrated Project BIOTRACER (contract 036272) under the 6th RTD
Framework.
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