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Review Managing quality variance in the postharvest food chain Maarten L.A.T.M. Hertog a, * , Jeroen Lammertyn a , Bart De Ketelaere b , Nico Scheerlinck a and Bart M. Nicola ı a,c a BIOSYST-MeBioS, Katholieke Universiteit Leuven, W. de Croylaan 42, B-3001 Leuven, Belgium (Tel.: D32 16 322376; fax: D32 16 322955; e-mail: [email protected]) b BIOSYST-MeBioS, Katholieke Universiteit Leuven, Kasteelpark Arenberg 30, B-3001 Leuven, Belgium c Flanders Centre of Postharvest Technology, W. de Croylaan 42, B-3001 Leuven, Belgium Data generated in postharvest research are characterised by an inherent large amount of biological variance. This variance generally obscures the behaviour of interest, complicating both the statistical and conceptual interpretation of the data. To be able to manage the postharvest chain, clear insight is required in the propagation of biological variance during postharvest. Recently, biological variance has gained interest within the postharvest community. To analyse experimental data taking into account biological variance several (statistical) modelling techniques have been applied by different authors. These vary from models that can be solved analytically to an- alyse the effect of experimental design parameters (e.g., mixed effects models), via hybrid techniques which combine analyt- ical and numerical techniques, to pure numerical models for dynamic simulations based on ordinary differential equations (like the variance propagation algorithm) and/or partial differ- ential equations (e.g., the FokkerePlanck equation). Each of these techniques has its own possibilities and limitations in terms of the type of variance that can be accounted for, their technical complexity, and their applicability to practical situations. Using tomato colour as an example, the different tech- niques are applied and compared to highlight their strong and weak points in interpreting biological variance. The added value of these techniques is discussed within the framework of managing biological variance in the postharvest chain. Introduction What differentiates the postharvest chain from most other handling chains are (1) the fact that postharvest is dealing with living tissue that inherently is slowly changing with time, and (2) the large sources of biological variance. Postharvest product behaviour is thus inherently affected by the omnipresent biological variance. Most of the time, post- harvest management aims at controlling the average batch behaviour and limiting biological variance as much as pos- sible by sorting and grading the product at the different stages in the postharvest chain. From a marketing point of view, one mostly deals with such batches and not with the individual product items (or objects). Currently, the hor- ticultural industry is not capable of differentiating their postharvest treatments to such an extent that they can actu- ally take into account batch specific handling requirements. For this, much more insight is required into the dynamics of quality change in general and the propagation of biological variance through the postharvest chain. Identification and quantification of the different sources of variance (often referred to as error) is of utmost importance to compare batches and to predict how an initial variance in quality attributes propagates during time. Generally, postharvest scientists tend to ignore the be- haviour of the individual objects and focus on the averaged batch behaviour based on large sample sizes. However, treating biological variance as a nuisance instead of a central part of the modelling effort, can lead to inefficient estimation of means and even to misleading conclusions (Carroll, 2003; Tijskens, Konopacki, & Sim ` c, 2003). Only recently, new impulses have been given to take into account the underlying behaviour of the individual objects to interpret postharvest batch behaviour. One of the driving forces for this is the increased availability of non-destructive measuring techniques that allow monitoring of individual objects during time (De Baerdemaeker, Hertog, Nicola ı, * Corresponding author. 0924-2244/$ - see front matter Ó 2007 Elsevier Ltd. All rights reserved.
Transcript

Review

Managing quality

variance in

the postharvest

food chain

Maarten L.A.T.M. Hertoga,*,Jeroen Lammertyna, Bart DeKetelaereb, Nico Scheerlincka

and Bart M. Nicola€ıa,c

aBIOSYST-MeBioS, Katholieke Universiteit Leuven,W. de Croylaan 42, B-3001 Leuven, Belgium(Tel.: D32 16 322376; fax: D32 16 322955;

e-mail: [email protected])bBIOSYST-MeBioS, Katholieke Universiteit Leuven,Kasteelpark Arenberg 30, B-3001 Leuven, Belgium

cFlanders Centre of Postharvest Technology,W. de Croylaan 42, B-3001 Leuven, Belgium

Data generated in postharvest research are characterised by an

inherent large amount of biological variance. This variance

generally obscures the behaviour of interest, complicating

both the statistical and conceptual interpretation of the data.

To be able to manage the postharvest chain, clear insight is

required in the propagation of biological variance during

postharvest. Recently, biological variance has gained interest

within the postharvest community. To analyse experimental

data taking into account biological variance several (statistical)

modelling techniques have been applied by different authors.

These vary from models that can be solved analytically to an-

alyse the effect of experimental design parameters (e.g., mixed

effects models), via hybrid techniques which combine analyt-

ical and numerical techniques, to pure numerical models for

dynamic simulations based on ordinary differential equations

(like the variance propagation algorithm) and/or partial differ-

ential equations (e.g., the FokkerePlanck equation). Each of

these techniques has its own possibilities and limitations

in terms of the type of variance that can be accounted for,

their technical complexity, and their applicability to practical

situations.

Using tomato colour as an example, the different tech-

niques are applied and compared to highlight their strong

and weak points in interpreting biological variance. The added

value of these techniques is discussed within the framework of

managing biological variance in the postharvest chain.

IntroductionWhat differentiates the postharvest chain from most

other handling chains are (1) the fact that postharvest is

dealing with living tissue that inherently is slowly changing

with time, and (2) the large sources of biological variance.

Postharvest product behaviour is thus inherently affected by

the omnipresent biological variance. Most of the time, post-

harvest management aims at controlling the average batch

behaviour and limiting biological variance as much as pos-

sible by sorting and grading the product at the different

stages in the postharvest chain. From a marketing point

of view, one mostly deals with such batches and not with

the individual product items (or objects). Currently, the hor-

ticultural industry is not capable of differentiating their

postharvest treatments to such an extent that they can actu-

ally take into account batch specific handling requirements.

For this, much more insight is required into the dynamics of

quality change in general and the propagation of biological

variance through the postharvest chain. Identification and

quantification of the different sources of variance (often

referred to as error) is of utmost importance to compare

batches and to predict how an initial variance in quality

attributes propagates during time.

Generally, postharvest scientists tend to ignore the be-

haviour of the individual objects and focus on the averaged

batch behaviour based on large sample sizes. However,

treating biological variance as a nuisance instead of a

central part of the modelling effort, can lead to inefficient

estimation of means and even to misleading conclusions

(Carroll, 2003; Tijskens, Konopacki, & Sim�cı�c, 2003).

Only recently, new impulses have been given to take into

account the underlying behaviour of the individual objects

to interpret postharvest batch behaviour. One of the driving

forces for this is the increased availability of non-destructive

measuring techniques that allow monitoring of individual

objects during time (De Baerdemaeker, Hertog, Nicola€ı,* Corresponding author.

0924-2244/$ - see front matter � 2007 Elsevier Ltd. All rights reserved.

& De Ketelaere, 2006; Galili, Shmulevich, & Benichou,

1998; Peirs, Scheerlinck, De Baerdemaeker, & Nicola€ı,

2003; Peirs, Tirry, Verlinden, Darius, & Nicola€ı, 2003;

Shmulevich, Ben-Arie, Sendler, & Carmi, 2003; Tijskens,

Hertog, Van Kooten, & Sim�cı�c, 1999; Zerbini et al.,

2006). With the increased awareness of the added value of

reporting data from individual objects as opposed to report-

ing only averaged batch values several authors started to

focus on explicitly including biological variance into their

(statistical) data analysis (e.g. De Ketelaere et al., 2004;

De Ketelaere, Lammertyn, Molenberghs, Nicola€ı, & De

Baerdemaeker, 2003; De Ketelaere, Stulens, Lammertyn,

Cuong, & De Baerdemaeker, 2006; Hertog, 2002, 2004;

Hertog, Lammertyn, Desmet, Scheerlinck, & Nicola€ı,

2004; Hertog, Lammertyn, Scheerlinck, & Nicola€ı, 2007;

Hertog, Scheerlinck, Lammertyn, & Nicola€ı, 2007;

Lammertyn, De Ketelaere, Marquenie, Molenberghs, &

Nicola€ı, 2003; Peirs, Scheerlinck, Perez, Jancsok, & Nicola€ı,

2002; Scheerlinck, Franck, & Nicola€ı, 2006; Scheerlinck,

Peirs, Desmet, Schenk, & Nicola€ı, 2004; Schouten,

Jongbloed, Tijskens, & van Kooten, 2004; Tijskens et al.,

2003; Tijskens, Konopacki, Sim�cı�c, & Hribar, 2000;

Tijskens & Wilkinson, 1996).

The major challenge is to develop predictive models that

assess the uncertainty of the predicted result. Since the

dependent model response variable is a function of one or

more stochastic independent variables it is no longer a

deterministic property. Given a simulation model, this prob-

lem reduces to the propagation of errors from the simula-

tion input to the simulated result. One major problem in

examining the impact of uncertainties in input data on sim-

ulation results is the ‘curse of dimensionality’ (Christie

et al., 2005). With an increasing number of random factors

it becomes practically impossible to establish the correct

model response. Generally some reduction is required by

identifying the most important (combinations of) input

parameters that capture most of the variability.

By introducing biological variance into (statistical)

models both the analysis and the subsequent prediction of

postharvest batch behaviour can be improved considerably.

In general, by identifying and quantifying the different

sources of variance in the experimental data and by assign-

ing them to the different parts of the model (uncertainties in

parameter values and remaining measurement error), large

parts of the between fruit variance can be accounted for en-

abling a much better interpretation of the remaining under-

lying generic postharvest behaviour. Also, if biological

variance is included in (statistical) models describing post-

harvest quality change, propagation of the initial biological

variance at harvest throughout the whole postharvest chain

can be predicted taking into account all relevant aspects

affecting postharvest fruit behaviour.

To analyse experimental data taking into account biolog-

ical variance several (statistical) modelling techniques have

been applied by the different authors mentioned before.

These vary from models that can be solved analytically to

analyse the effect of experimental design parameters

(e.g., mixed effects models), via hybrid techniques which

combine analytical and numerical techniques, to pure nu-

merical models for dynamic simulations based on differen-

tial equations (Nicola€ı, Scheerlinck, & Hertog, 2006;

Nicola€ı, Scheerlinck, Verboven & De Baerdemaeker,

2001; Scheerlinck, 2000). However, in the end the different

techniques all try to deal with the same issue of biological

variance. In order to incorporate this variance, some of the

model parameters can be considered as random or stochas-

tic variables. Random variables are, as a mathematical con-

cept, useful because they allow the quantification of

variability and random behaviour. In this way variability

can be expressed by statistical concepts such as mean

values, (co)variances, (joint) probability density functions

and confidence intervals.

Our aim is to provide a review of the different available

techniques that deal with biological variance in experimen-

tal time dependent data. The working principles of the dif-

ferent techniques will be outlined and some general aspects

will be compared. Using tomato colour as an example, the

different techniques are applied and compared to highlight

their strong and weak points in interpreting biological var-

iance. To facilitate comparison between the different tech-

niques they will be applied to the same set of data using the

same basic model to describe tomato colour as a function of

time and temperature. Finally, the added value of applying

these techniques is discussed within the framework of man-

aging biological variance in the postharvest chain.

Modelling techniquesMixed effects models

In a classical statistical analysis, one of the main aims is

to draw conclusions about the effect of experimental treat-

ments as defined by certain independent variables. These

independent variables are generally referred to as fixed ef-

fects. The classical fixed effects analysis is able to describe

the averaged observed batch behaviour as a function of the

independent variables. When repeated measurements are

taken on individual objects, classical fixed effects analysis

does not account for the relationship between serial obser-

vations on individual objects, affecting significance levels

of the parameters of interest. Our interest may not be

restricted to the fixed effects only, but may extend itself

to the behaviour of individual objects within a batch. This

variability in behaviour of individual objects around a group

average is called a random effect. Models that treat both

fixed and random effects were proposed by Laird and

Ware (1982) and are nowadays referred to as mixed effects

models. One may subdivide mixed effects models into a

linear and nonlinear class. In linear mixed effects models,

the fixed and random components enter the model function

in a linear way (Verbeke & Molenberghs, 2000), whereas

nonlinear mixed effects models are a natural extension

where fixed and random effects are allowed to enter in

a nonlinear way (Pinheiro & Bates, 2000).

Through the random effects and their associated distri-

bution (e.g., a normal distribution), mixed effects models

provide a flexible way to handle repeated measurement

data. Furthermore, they allow describing the variance due

to the natural heterogeneity of the batch, and the heterosce-

dasticity (non-constant variance) of the data. Heteroscedas-

ticity is encountered in many experiments and a correct

handling is crucial to properly estimate both fixed and

random model parameters and, hence, their significance

(De Ketelaere et al., 2006).

Coping with the natural batch heterogeneity is important

from an inferential and a practical point of view. While in

a classical regression procedure all remaining variability,

after subtraction of the population average, is considered

unexplained variance, the mixed effects model is capable

of dividing variance in different components, such as mea-

surement error, different sources of true biological variance

(batch heterogeneity) and unexplained variance. This is

needed in order to make accurate predictive models, or to

make inferences about the fixed effects, such as treatment

or cultivar effects. Furthermore, formal tests are available

to identify the significant components of variance.

Mixed effects models have been used in areas like image

analysis, psychology and medicine. Closer to the food

industry various examples are found on dietary studies

(Barton et al., 2005; Opsomer, Jensen, & Pan, 2003; Striegel-

Moore et al., 2006) several preharvest (De Silva & Balli,

1997; Usenik, Kastelec, & Stampar, 2005; Wei, Sykes, &

Clingeleffer, 2002) and postharvest studies (De Ketelaere

et al., 2003, 2004, 2006; Lammertyn et al., 2003).

Stochastic kinetic modelsThe stochastic kinetic model approach was developed

independently by Hertog (Hertog, 2002; Hertog et al.,

2004, Hertog, Lammertyn et al., 2007; Hertog, Scheerlinck

et al., 2007) and Schouten (Schouten, 2004; Schouten et al.,

2004). The basic model structure is given by some alge-

braic equation. This model formulation can be completely

empirical or can be derived from a kinetic model founded

on some mechanistic concept. This last approach is

strongly preferred as, in this way, one is forced to develop

a sound conceptual model of all processes involved to come

up with a plausible suggestion of how variance in some of

the model parameters might cause the observed biological

variance in the response variable. So the starting point is

an algebraic equation that contains one or more parameters,

some of which are of a stochastic nature which can be char-

acterised by a probability distribution function. The under-

lying assumption is that the probability to obtain a certain

model response is identical to the (combined) probability

of the (combination of) parameter value(s) leading to this

response. So, assuming the probability distribution func-

tions of the model parameters are known, the probability

distribution function of the modelled response variable

can be obtained by transforming the probability distribution

function of the stochastic model parameters using the

algebraic model equation. This is visualised in Fig. 1 for

the case of a single stochastic model parameter.

There are some mathematical limitations to this tech-

nique in that the inverse of the model equation should

exist and that this inverse function is differentiable. This

approach can be applied to models containing multiple

stochastic parameters (Hertog, 2004; Hertog, Lammertyn

et al., 2007; Hertog, Scheerlinck et al., 2007) that, theoret-

ically, do not necessarily need to follow a Gaussian

distribution.

As the model is based on an algebraic equation all inde-

pendent input variables are assumed constant with time.

More recently this approach was extended to the case where

the response variable is a function of some dynamically

changing input variable as in the case of a temperature depen-

dent rate constant (Hertog, Lammertyn et al., 2007). Thiswas

achieved by introducing the concept of physiological time

which is a transformation of the real time incorporating

environmental effects such as temperature (Lischke, Loffler,

& Fischlin, 1997; Schroder & Sondgerath, 1996; Trudgill,

Honek, Li, & Van Straalen, 2005; Van Straalen, 1983).

Within the light of this physiological time all processes

behave the same, regardless temperature, as physiological

time itself, relative to the real time, is the one being delayed

or accelerated by temperature.

So far, this stochastic kinetic technique has been exclu-

sively applied in the postharvest area describing the posthar-

vest batch behaviour of cucumber (Schouten et al., 2004),

strawberry (Schouten, 2004), tomato (Hertog, 2002; Hertog

et al., 2004, Hertog, Lammertyn et al., 2007) and Belgian

endive (Hertog, Scheerlinck et al., 2007).

Monte Carlo simulationsMonte Carlo simulation is a numerical stochastic tech-

nique used to solve mathematical problems. Credit for

X

Y

Y = f(X)

A

B

Fig. 1. Given the model equation Y¼ f(X ) defining how the model re-sponse (Y ) depends on the value of a single stochastic parameter (X ),the probability density distribution of the model response (B) is ob-tained by transforming (as indicated by the arrows) the original distri-bution of the stochastic model parameter (A) using the model

equation.

inventing the Monte Carlo method often goes to Stanislaw

Ulam (Eckhardt, 2005), a Polish born mathematician who

worked during World War II on the United States’ Manhat-

tan Project to build the first atomic bomb. The Monte Carlo

method, as it is understood today, encompasses any tech-

nique of statistical sampling employed to approximate solu-

tions to quantitative problems.

The term ‘Monte Carlo’ comes from the name of a city

in Monaco. The city’s main attractions are casinos, which

run games such as roulette wheels, dice and slot machines.

These games provide entertainment by exploiting the ran-

dom behaviour of each game. Similarly, Monte Carlo

methods randomly select values to create scenarios of

a problem. These values are taken from within a fixed range

and selected to fit a given probability distribution (Metro-

polis & Ulam, 1949). So, a Monte Carlo simulation is based

on some model system (either functions or differential

equations) that is defined as a function of random model

parameters characterised by their probability distribution

functions. Using the Monte Carlo method, the model

system is simulated multiple times after random sampling

parameter values from these probability distribution func-

tions. Based on the repeated simulations, the probability

density function of the response variable is constructed as

a function of time. Monte Carlo methods have been used

since the late 1940s, but only since the availability of large

computational power has the technique gained the status of

a numerical method capable of addressing large complex

applications. The technique is useful to obtain numerical

solutions to problems which are too complicated to solve

analytically. Generally, this technique is used for simula-

tion, not for statistical data analysis.

This technique is already extensively applied in the field

of food science, mainly related to food safety and risk anal-

ysis (e.g. Koutsoumanis, Taoukis, & Nychas, 2005; Nicola€ı

& Van Impe, 1996; Poschet et al., 2004; Poschet, Geeraerd,

Scheerlinck, Nicola€ı, & Van Impe, 2003; Poschet, Geer-

aerd, Van Loey, Hendrickx, & Van Impe, 2005; Tsutsui &

Kasuga, 2006) but also related to postharvest product

quality (Scheerlinck et al., 2004; Tijskens & Wilkinson,

1996; Tijskens et al., 1999, 2000, 2003) and to model the

effect of postharvest heat treatment for disinfestation pur-

poses (Verboven, Tanaka, Scheerlinck, Morita, & Nicola€ı,

2005).

FokkerePlanck equationStochastic systems theory provides a fundamental

approach, i.e. the FokkerePlanck equation, to compute

the propagation of variability through systems described

by differential equations with stochastic input variables. It

deals with those fluctuations of systems which originate

from many small disturbances, each of which changes the

response variable of the system in an unpredictable way.

The FokkerePlanck equation or forward diffusion equation

(Melsa & Sage, 1973) is a partial differential equation that

was first used to describe Brownian motion of a particle in

a fluid. It balances the effect of systematic changes in the

probability density due to a structured process (driving

force) with the effect of random drift due to random fluctua-

tions in the population.

In the case of multiple independent stochastic model

variables these can be represented by means of a multi-

dimensional probability density function. This joint proba-

bility density function defines the initial stochastic behaviour

of the dependent model variables which are the starting

point for the application of the FokkerePlanck equation.

The FokkerePlanck equation describes how the initial

probability density function propagates through the multi-

dimensional space as a function of time. Once the stochas-

tic behaviour of the dependent response variable is known

at all time points of interest, the multi-dimensional density

functions can be integrated, resulting in a one-dimensional

probability density function of the dependent model re-

sponse variable for each time point together defining the

complete time course.

For most realistic applications no closed form and gen-

eral solutions can be calculated for the FokkerePlanck

equation. Therefore, one has to rely on numerical solution

strategies. For a survey of the mathematical formulation

of FokkerePlanck and its computational challenges the

reader is referred to Scheerlinck et al. (2004).

The FokkerePlanck equation applies to a wide variety of

time dependent systems in which randomness plays a role

and is commonly used in physics, aerodynamics, mechani-

cal engineering and electronic engineering, e.g., the behav-

iour of buildings under random loads such as earthquakes

or to design auto mobiles, aircrafts and space shuttles.

However, it has also been applied to areas closely related

to food science like population biology (Soboleva &

Pleasants, 2003), soil science (Or, Leij, Snyder, &

Ghezzehei, 2000), air flow modelling (Wilson, Flesch,

& Swaters, 1993), and postharvest technology (Scheerlinck

et al., 2004, 2006).

Variance propagation algorithmFor most problems the joint probability density function

of the stochastic variables is very difficult to obtain, espe-

cially when the dimension of the system is large and/or the

system is highly nonlinear. However, stochastic systems

theory provides an alternative method to the solution of the

FokkerePlanck equation. The variance propagation algo-

rithm (Melsa & Sage, 1973) is a tool to derive first order

approximate solutions for the mean and the covariance of

the system variables (properties) or parameters. For a mathe-

matical description of this algorithm and details on how to

apply the algorithm for a given model structure, the reader

is referred to Scheerlinck et al. (2004). The method essen-

tially involves the solution of matrix differential equations

of the Lyapunov type. The variance propagation algorithm

is computationally less demanding as compared to Monte

Carlo methods and the solution of the FokkerePlanck

equation and provides the transient evolution of themean and

variance of the modelled response variable. The algorithm is

generally applicable and can easily be implemented.

The variance propagation algorithm is commonly used

in systems and control theory. In the food area this tech-

nique has been applied to account for stochastic sources

when describing heat conduction, either during thermal

food processing (Nicola€ı & DeBaerdemaeker, 1996, 1997;

Nicola€ı, Scheerlinck, Verboven, & De Baerdemaeker,

2000; Nicola€ı, Verboven, Scheerlinck, & De Baerdemaeker,

1998; Scheerlinck et al., 2000, 2001) or during cold storage

(Nicola€ı et al., 1999) and to model variability in fruit qual-

ity (Scheerlinck et al., 2004, 2005, 2006).

Selecting a techniqueThe various stochastic modelling techniques discussed

in the previous section all have their own strong and

weak points and can be suitable to different extents depend-

ing on the problem in question. At the same time, none of

these techniques are exclusive and can often be combined

to tackle the different aspects of interest. To give some

guiding in when the different techniques can be applied

a decision tree was developed (Fig. 2).

The first step in selecting a technique (step 1, Fig. 2)

would be to consider the number of random factors in-

volved. When the number of random effects increases, all

of the techniques become numerically quite demanding in

terms of computing time. Because of its simple concept

and equally long computing time, Monte Carlo simulations

would now be in favour. The Monte Carlo results will

mainly give information on the random model effects

showing the propagation of biological variance, allowing

for the reconstruction of 95% confidence intervals for the

stochastic dependent response variable.

When the number of random factors is limited one

should subsequently check (step 2, Fig. 2) whether there

is an analytic model description available or whether the

model only exists in the form of differential equations.

When the analytic solution is available one should consider

the main purpose of the modelling exercise (step 3a,

Fig. 2). When the aim is to statistically analyse the data es-

tablishing proper estimates and confidence bands for the

fixed effects, mixed effects models would be the first

choice. When the aim is to simulate the stochastic behav-

iour of the dependent response variable focussing on the

random effects of the model, the stochastic kinetic ap-

proach would be most suitable.

If there is no analytic solution available one should con-

sider whether the distributions of the random factors are

known (step 3b, Fig. 2). If so, the FokkerePlanck equation

allows to reconstruct the full stochastic behaviour including

the 95% confidence intervals of the dependent stochastic

response variable. If the distributions are not known, the

final option is to apply the variance propagation algorithm

to calculate the transient evolution of the mean and variance

of the modelled response variable.

Application areasThe techniques outlined above, all deal with variance in

complex systems but are not explicitly designed for or lim-

ited to a specific application area. Any application requiring

reliable predictions of complex phenomena has to deal with

sources of variance and requires techniques as outlined

above. The outlined techniques can be applied to perform

proper risk analysis in the nuclear weapon industry, the

oil industry, the financial world, for clinical trails, to eval-

uate building construction and also while safeguarding

food quality and food safety. Depending on the application

area, higher stakes might be involved to warrant a proper

full stochastic analysis of the complex system of interest.

When focussing on the wider food area, potential appli-

cations are manifold given the large sources of variance and

the batch oriented character of many food processes. From

an economical point of view, applications are more likely to

be worthwhile for products with a large added value, such

as functional foods. From a general food quality point of

view, proper insight is required in the propagation of vari-

ance when dealing with any food process that starts from

a highly variable raw product and tries to turn this into

a food product of a reproducible constant quality. Inher-

ently, batch oriented or semi-continuous processes, as gen-

erally applied in the food industry, all have to deal with

these constantly varying input streams.

Potential applications in the wider food area could focus

on production, processing or health related issues where

microbial food safety becomes important. Using a recent

volume of the current journal, Trends in Food Science &

Technology, as a guideline, topics were identified that could

Number of random

factors involved?

Analytic solution

available?

MC

Main purpose?Distribution

known?

MM VPSK FP

≤ > 33

NoYes

NoYesStatistical

inferenceSimulation

1

3a

2

3b

Fig. 2. Decision tree showing the steps of selecting the appropriatestochastic modelling techniques. (MM: Mixed effects models; SK:stochastic kinetic models; MC: Monte Carlo simulations; FP:

FokkerePlanck; VP: variance propagation algorithm).

potentially benefit from the use of stochastic modelling

techniques (Table 1). This list from Table 1 is far from

complete but just tries to raise the consciousness of the

huge potential of stochastic modelling techniques when

analysing time dependent data prone to variance.

Case studyPostharvest research produces experimental time depen-

dent data characterised by large sources of biological vari-

ance. Just to stay within our own comfort zone the case

study discussed in this section focuses on a typical posthar-

vest example on the ripening of tomatoes as indicated by

their colour.

General model behaviourUsing tomato colour as an example, the different tech-

niques are applied and compared to highlight their strong

and weak points in interpreting biological variance. All

techniques use the same colour change model as developed

by Hertog et al. (2004) to enhance comparison between the

techniques. The general behaviour of colour as a function

of time is depicted in Fig. 3 showing the meaning of the dif-

ferent model parameters. In addition, the rate constant is as-

sumed temperature dependent. The model can be either

applied in the form of its differential equations or using

the corresponding analytic solution (see Hertog et al.,

2004, for full model details).

The model describing hue colour as a function of time is

deterministic in the sense that time evolution of colour is

entirely predetermined by an exact knowledge of the tem-

perature conditions, colour (or biological age) at harvest,

the rate of colour change and the colour limits. Due to

biological variance and variability in the physiological state

some of the model parameters are inevitably subjected to

random variance introducing variance in the dependent

response variable hue.

Experimental dataThe experimental data used for this case study consists

of two parts. One part (Fig. 4) considers storage data

from three tomato cultivars (‘Quest’, ‘Style’ and ‘Tradiro’)

stored for 21 days at three different constant temperatures

(12 �C, 15 �C or 18 �C) using 20 fruit per condition.

The second part (Fig. 5) considers one large batch of

‘Tradiro’ tomatoes (300 fruit) stored for 11 days at varying

temperature conditions. Fore more detailed experimental

information see Hertog et al. (2004), Hertog, Lammertyn

et al. (2007). As shown by the data, one encounters a con-

siderable amount of colour variability between tomatoes at

harvest, the magnitude of which is mainly determined by

harvest criteria, and how accurately these are applied in

practice. This variability typically decreases with time be-

cause all tomatoes of a batch asymptotically evolve to

a similar red colour after storage. This clearly illustrates

the aspect of heteroscedasticity in hue colour with time.

Data analysisUpon completion of an experiment one is confronted with

an amount of experimental variance. This experimental var-

iance is partly induced by experimental factors (e.g.,

Table 1. Potential application areas for stochastic modelling tech-niques identified based on manuscripts published in 2005 inTrends in Food Science & Technology (volume 16)

Production and breedinge (Micro)nutrient enhancement in plant crops(e.g. Storozhenko et al., 2005)

Processinge Microbial growth in relation to fermentation technology(e.g. Hammes et al., 2005)e High pressure processing(e.g. Estrada-Giron, Swanson, & Barbosa-Canovas, 2005)e Drying and rehydration of foods(e.g. Sam Saguy, Marabi, & Wallach, 2005)e Increasing natural food (micro)nutrients through bioprocessing(e.g. Jagerstad et al., 2005)e Formation of carcinogens during food processing(e.g. Claeys, De Vleeschouwer, & Hendrickx, 2005)

Storage and transporte Antimicrobial effect of postharvest UV treatment(e.g. Shama & Alderson, 2005)e Quality changes during processing and storage(e.g. Wrolstad, Durst, & Lee, 2005)e Generation of aroma compounds(e.g. Hansen & Schieberle, 2005)e Food chain design(e.g. Apaiah, Hendrix, Meerdink, & Linnemann, 2005)

Health and safetye Microbial growth in relation to food safety(e.g. De Vuyst & Neysens, 2005)e Reactive oxygen species in food(e.g. Wiseman, 2005)e (Micro)nutrient bioavailability, intake and metabolism(e.g. Gregory III, Quinlivan, & Davis, 2005)

k

H+ ∞

H− ∞

H0

Preharvest Postharvest

time

Hue

colo

ur

tage

Href

harvest

Fig. 3. Tomato colour can be measured as hue values (H in �) changingfrom immature green (H�N in �) to a fully ripe red (HþN in �) colourfollowing a sigmoid pattern. Tomatoes change colour following a cer-tain rate constant (k in d�1) that depends on temperature. The tomatoesare harvested at some initial colour (H0 in

�). The biological age of anindividual tomato (tage in d ) is defined as the time required to changecolour from a certain given reference point (Href in

�) to the initial col-our observed at harvest (redrawn from Hertog et al., 2007).

temperature and cultivar effect) while remaining variability

is considered as residual (unexplained) variance. The classi-

cal statistical approach to analyse the hue colour data from

different cultivars stored at different temperatures would be

to perform a nonlinear regression analyses of the data fitting

the model per cultivar. For the constant temperatures the an-

alytic solution can be used while for dynamic temperature

data the ordinary differential equation formulation has to

be used. This model approach describes the averaged batch

behaviour perfectly well (Fig. 4) but tries not to explain the

remaining variance as all of it is regarded as residual error.

When comparing the parameter estimates between cultivars,

conclusions will be hampered by the inaccurate standard

errors of the estimates as they are biased by the incomplete

error analysis. Using the stochastic techniques outlined

above the unexplained residual error from the classical ap-

proach will be dissected further and assigned to the various

sources.

Identification of sources of varianceTo identify the main source(s) of variance one can start

with a classical analysis of the multiple individual objects

to build distributions for the various model parameters esti-

mated. This provides information on the type of distribution

(e.g., normal, Poisson) and the distribution parameters (e.g.,

mean, standard deviation) of the stochastic model parame-

ters including the possible correlation structure between

these stochastic model parameters. This information is cru-

cial for any of the stochastic techniques applied, except for

the variance propagation algorithm which is a distribution

free approach.

Subsequently one of the available stochastic techniques

can be selected to implement models with one or more sto-

chastic model parameters. The goodness of fit of these nested

models can be compared based on the various criteria avail-

able (e.g., root mean square error, likelihood ratio, Akaike in-

formation criterion, Bayesian information criterion; see

Forster and Sober, 1994, for a non-technical introduction to

these criteria). By doing so the model structure is restricted

to include only the most important stochastic variables.

The first source of variance is often most dominant and cor-

responds to inevitable natural biological variability between

the observed objects. Accounting for this source of variance

greatly reduces the unexplained variance term. Using the

final model structure with the main sources of variance

selected one can focus on analysing the data in more detail.

Statistically comparing groupsIn a mixed model context one has the tools (e.g., intro-

duction of random effects) to subdivide the variance com-

ponent into different sources of variance, such as variance

0 5 10 15 20

40

50

60

70

Quest

time (d)

40

50

60

70

Style

Hu

e (

°)

40

50

60

70

Tradiro12 °C

15 °C

18 °C

Fig. 4. Change in hue colour (H in �) of three tomato cultivars (‘Tra-diro’, ‘Style’ and ‘Quest’) stored at three constant temperatures(12 �C, 15 �C and 18 �C) as a function of storage time. The symbols in-dicate the averaged colour of 20 tomatoes while the bars enclose the95% confidence interval based on the standard errors of the measure-ments. The lines represent the general model describing the average

batch behaviour (redrawn from Hertog et al., 2004).

0 2 4 6 8 10

40

50

60

70

80

90

Hu

e (

°)

time (d)

12

14

16

18

T (

°C)

Fig. 5. Change in hue colour (H in �) as a function of storage timeof 300 ‘Tradiro’ tomatoes stored at a varying temperature regime asindicated in the top graph. The lines represent the colour change of

the individual tomatoes.

between objects, variance within objects, measurement var-

iance and unexplained variance. Furthermore, mixed

models offer a framework to test which of the sources of

(biological) variance are significantly present. This allows

accurate accounting for the typical varianceecovariance

structure of the experimental data set which is a prerequisite

for building accurate predictive models, and for appropriate

testing of the significance of the experimental factors (e.g.,

cultivar effects). Therefore, the mixed model framework is

perfectly suited to statistically compare groups of observa-

tions. In the present case study it is of interest to test

whether there are significant differences in colour profile

between the different batches (e.g., tomato cultivars). The

average colour profile per cultivar is characterised by two

fixed parameters: a colour change rate (k) and the asymp-

totic end colour (HþN). The test to identify significant dif-

ferences is based on the varianceecovariance structure of

these fixed effects. The latter can only be estimated cor-

rectly by accounting for the different sources of variance.

The two main sources of variance identified are one random

effect related to initial colour (H0) and one random effect

related to the asymptotic end colour (HþN). The remaining

variance is assumed to be random error.

Fig. 6 shows the 95% joint confidence ellipses for the

colour change rate and the asymptotic colour for the three

cultivars. The cultivar ‘Tradiro’ clearly has a higher colour

change rate and a lower asymptotic hue value compared to

the other two cultivars. The cultivars ‘Quest’ and ‘Style’

have partly overlapping confidence ellipses referring to

similar average colour profiles. An F-test indicates no

significant difference in colour behaviour between both cul-

tivars at the 5% significance level.

Propagation of biological varianceThe mixed effects model approach results in, among

others, the distribution parameters of the stochastic model

parameters including their covariance structure but, by

itself, does not provide information on the propagation of

biological variance with time. A quick way to get some

idea of the stochastic behaviour of hue colour is obtained

by the variance propagation algorithm that evaluates first

order approximations of the mean and variance of hue

with time without providing information on the shape of

the distribution of hue with time (Fig. 7B, C).

More detailed information on the model response is ob-

tained using the other techniques. Using the distributions of

40 41 42 43 44 45

1.2

1.3

1.4

1.5

1.6

1.7

k (

10

-3·

d-1

)

H+∞ (°)

Quest

Style

Tradiro

Fig. 6. Ninety-five percent joint confidence ellipses for the colourchange rate (k) and the asymptotic colour (HþN) for the three cultivars

stored at constant temperatures.

0 5 10 15 20

2

3

4

5

C

time (d)

40

45

50

55

60

B

μH (

°)

0

20

40

60

80

100A

% f

ruit

H (

°)

12 °C

15 °C

18 °C

Fig. 7. A. Batch ripening expressed as the cumulative percentage offruit that reached a critical hue value of 50�. B. Propagation of the av-eraged hue colour (m) as predicted by the variance propagation algo-rithm. C. Propagation of the standard deviation of hue colour (s) aspredicted by the variance propagation algorithm. All graphs were

made for the cultivar ‘Quest’ stored at 12 �C, 15 �C or 18 �C.

the stochastic model parameters as identified by the mixed

effects model, Monte Carlo simulations can be performed

to generate an approximation of the full stochastic behav-

iour of the model showing the propagation of biological

variance in hue with time (Fig. 8). These results describe

in full detail the stochastic behaviour of the modelled re-

sponse variable with the accuracy depending on the number

of runs. To get smooth surfaces one typically has to do five

to ten thousand simulation runs. Using the stochastic

kinetic model approach or the FokkerePlanck equation,

the same response surface is obtained in a single run,

with the stochastic kinetic model approach being the less

computational intensive one of the three approaches.

When using the FokkerePlanck equation one would also

start from the distributions of the stochastic model para-

meters as derived from a classical analysis on the multiple

individual objects or as identified by the mixed effects

model. In the case of hue colour, biological variance can

be explicitly incorporated through the introduction of three

correlated random variables, i.e., initial hue colour (H0), the

rate of colour change (k) and the asymptotic colour value

(HþN). The random variables can be represented by means

of a three dimensional joint probability density function us-

ing a trivariate Gaussian distribution. The FokkerePlanck

equation describes how this density function propagates

through the three dimensional space as a function of

time. After integrating the three dimensional density distri-

butions the final result is obtained, which is comparable to

that of an approximate solution generated by a Monte Carlo

simulation (Fig. 8).

In case of the stochastic kinetic approach one can either

start from already established distributions of the stochastic

model parameters or one could actually fit the model

response surface on the observed data thus establishing

the distribution parameters for the stochastic model param-

eters while applying this stochastic kinetic technique. How-

ever, the standard errors of these estimates would not be as

statistically correct as when using mixed effects models.

The final result on the simulated bath behaviour is however

identical to that established through either Monte Carlo

simulations or by using the FokkerePlanck equation

(Fig. 8).

Batch acceptanceOnce the full stochastic behaviour of hue as a function

of time has been established this information can be used

to answer questions like which part of the batch is likely

to have a quality below or beyond a certain critical quality

limit. Even though the averaged batch quality might still be

acceptable some part of the batch might have crossed these

limits (Fig. 7A). This can be simply done by integrating the

area under the probability distribution function of hue as

a function of time. This kind of information basically

reduces the complex information from the probabilistic

response surface into a manageable form for the industry.

As can be seen from Fig. 7A, the rate at which batch

acceptance changes is directly related to temperature, as

the rate at which biological variance propagates is directly

related to the rate of colour change of the individual tomatoes

in the batch. For dynamic temperature conditions (Fig. 5),

temperature, and thus the rate of propagation changes by

the hour. However, using the stochastic kinetic model

approach, these dynamic temperature scenarios can be ana-

lysed as well (Fig. 9A). It can be seen how, during periods

of high temperature (Fig. 9A, going from day 1 to day 4),

the variation in hue colour propagates faster, than during

periods of lower temperature (Fig. 9A, going from day 0 to

day 1). This is directly reflected in the percentage of fruit

reaching the critical quality limit of 50�, increasing more or

less steeply depending on temperature (Fig. 9B).

Comparative overviewHaving come this far in reading this review on stochastic

modelling techniques one might have noticed that, although

the various techniques could all be applied to the same case

study, they do have their own specific possibilities and

limitations, both regarding technical and practical issues.

In this section we will explicitly summarise the main issues.

Model formulationGenerally two types of model formulations are encoun-

tered, the ordinary differential equations or the analytic so-

lution derived from them (an algebra€ıc equation). Mixed

effects models and stochastic kinetic models can only

deal with analytic model formulations while the variance

propagation algorithm and the FokkerePlanck equation

are based on the differential equation model formulation.

Monte Carlo simulations can be applied to either type of

model formulation. Still there is some flexibility as the

40 45 50 5560

6570 75

0

5

10

15

20

0.0

0.1

0.2

0.3

18 °C15 °C

12 °C

freq

uen

cy

tim

e (d)

Hue (°)

Fig. 8. Propagation of the relative frequency distribution of hue colour(H in �) of ‘Quest’ tomatoes stored at 12 �C, 15 �C or 18 �C. Startingfrom one and the same batch with a certain initial distribution ofhue (the front black curve) the frequency distributions propagate fasteror slower towards lower hue values depending on storage temperature

(the three ridges).

two types of model formulations can often be converted to

each other. The differential equations can be integrated to

obtain an analytic solution while an algebra€ıc equation

can be differentiated to obtain differential equations.

Prime purposeWhen using mixed effects models, emphasis is on analy-

sing data to establish proper estimators of the fixed and ran-

dom effects, thus allowing proper statistical inference. The

numerical techniques (Monte Carlo simulation, Fokkere

Planck equation and variance propagation algorithm) are

focussing on prediction of the complex system behaviour.

Theoretically one could combine this with parameter esti-

mation as well but generally this becomes rapidly unman-

ageable from a computational point of view. However,

modern computational algorithms and parallel computing

facilities allow to manage computational analysis of such

complex systems. The stochastic kinetic model approach

takes an intermediate position. As it works with an alge-

bra€ıc equation it is still feasible to use it for parameter

estimation while at the same time it can be used to predict

the stochastic system behaviour.

Prior knowledgeIn all cases one needs the model structure (either as dif-

ferential equations or as an algebra€ıc equation). For all

techniques but the variance propagation algorithm, one

has to decide on the type of distribution function underlying

the random effects. As the variance propagation algorithm

is a distribution free technique there is no need to identify

the type of distribution when using this approach. For the

numerical techniques one also needs prior knowledge on

all model parameter values (fixed effects) including the ini-

tial distribution parameters (e.g. average and standard devi-

ation) of the random effects responsible for the stochastic

model behaviour.

Stochastic dimensionalityThe more stochastic variables are included the more re-

alistic system behaviour can be obtained, but the more

computational intensive it becomes. In all of the mentioned

techniques every parameter could theoretically be consid-

ered a stochastic variable with an additional residual error

term containing that part of the observed variance that re-

mains unexplained by the stochastic model. When looking

at the food related literature the number of stochastic sour-

ces is generally limited to one to three.

System boundary conditionsWhen using an algebra€ıc model formulation, system

boundary conditions like temperature and gas conditions

have to be kept constant with time as the system behaviour

is generally affected by changing these boundary condi-

tions. When the model has to be able to cope with a system

responding to dynamic boundary conditions, the use of the

differential equation formulation is imperative. Conse-

quently, the numerical modelling techniques discussed

can be applied to both constant and dynamic boundary con-

ditions while the mixed effects models can only be applied

in the case of constant boundary conditions. The stochastic

kinetic model approach forms again an exception as in

some case one can work around the problem of dynamic

boundary conditions as was done for instance by introduc-

ing the physiological time concept. Consequently, also the

stochastic kinetic model approach can be applied to both

constant and dynamic boundary conditions.

Prime outcomeThe prime outcome of a mixed effect model approach is

the set of parameter values and their confidence intervals

describing the fixed and random effects. The prime out-

come of the stochastic kinetic model approach is the

4050

60

70

80 0

2

4

6

810

0.00

0.05

0.10

0.15

0.20

0.25

rela

tive f

req

uen

cy

Hue (°)tim

e (d

)

A

0 2 4 6 8 10

40

60

80

100

time (d)

% f

ruit

B

Fig. 9. A. Propagation of the relative frequency distribution of hue col-our (H in �) of ‘Tradiro’ tomatoes stored at dynamic temperature con-ditions (Fig. 5) showing the observed frequencies (symbols) ascompared to the modelled frequency distributions (curves; redrawnfrom Hertog, Lammertyn et al., 2007). B. Batch ripening of the samebatch of fruit expressed as the cumulative percentage of fruit reaching

a critical hue value of 50�.

density distribution of the response variable as a function of

time combined with the parameter estimates. In the case of

Monte Carlo simulations the prime outcome is a collection

of multiple individual simulations of the complex system

which can afterwards be collated into the full density distri-

bution of the response variable as a function of time. The

variance propagation algorithm provides as its prime out-

come the transient evolution of the mean and variance of

the modelled response variable. Finally, the FokkerePlanck

equation provides as its prime outcome the density distribu-

tion of the response variable as a function of time. So

depending on the research question one should choose

one or more of the proposed techniques.

ImplementationThe main statistical software packages, nowadays, have

standard procedures implemented to run mixed effects

models. All other techniques are either only supported by

highly dedicated software packages or have to be imple-

mented in engineering software taking into account the spe-

cific requirements from the particular model studied. From

these, Monte Carlo simulation is the most straightforward

technique to implement while the remaining three tech-

niques require a larger conceptual effort.

Computational requirementsWith increasing number of stochastic dimensions all of

the proposed techniques will exhibit a computational time

that is exponentially increasing. In these cases the only fea-

sible technique remaining is the Monte Carlo approach as

the others become too complex to manage. When using

up to three stochastic parameters all of the techniques are

feasible within acceptable computational time scales (in

the range of minutes) with the exact timing depending

on, for instance, the choice of starting values when estimat-

ing parameter values, and the numerical fine-tune strategies

applied for all of the numerical techniques.

Practical applicationThe stochastic modelling techniques advocated in this re-

view can be applied either within a research or a practical

commercial context. Within the research context emphasis

would be on the aspect of analysing experimental data to in-

crease insight in and understanding of the behaviour of the

food product of interest. These techniques provide, for in-

stance, a solid base to statistically screen different groups

(whether these are cultivars, growers, years, or growing con-

ditions) for fixed effects taking into account the full range of

variance observed. Within a practical commercial context

emphasis would be on the simulation aspect to take into ac-

count the full impact of the various sources of variance

when handling a certain batch of food products. These mod-

elling approaches can be either applied at the level of a single

process or at that of a whole chain. The stochastic modelling

techniques can be incorporated in a model predictive control

environment to optimise and control (parts of) the food

processing chain.With model predictive control, the control-

ler relies on an empirical model of the process which predicts

the behaviour of dependent variables of a dynamical system

based on independent variables to compute a costminimizing

control. Although model predictive control originates from

the chemical industries it has found its way to the agro-

food industry as well (Verdijck, Hertog, Weiss, & Preisig,

1999). The introduction of stochastic modelling techniques

in model predictive control would further enhance its poten-

tial value as it allows the controller to take into account batch

variance.

The added advantage of including stochastic information

in descriptive and predictive chain models will be obvious

when dealing with the real life situation of a complex logis-

tic food chain. Generally, when modelling a logistic chain,

Operation Research models are applied (Slats, Bhola,

Evers, & Dijkhuizen, 1995) that focus on the operational

side of the logistic chain. The number of management

models that do include product models (Broekmeulen,

2001) are relatively limited or often use fully empirical

models (Bogataj, Bogataj, & Vodopivec, 2005). The sto-

chastic model approaches discussed can potentially contrib-

ute to existing logistic chain models by allowing them to

optimise the operational ‘quality’ of the chain taking into

account the actual quality of the food products including

the complete range of variance presence.

AcknowledgementsThe authors gratefully acknowledge the financial support

from the Institute for the Promotion of Innovation by Science

and Technology in Flanders (Project IWT 030807 and IWT

040726). Nico Scheerlinck is postdoctoral fellow with the

Flemish Fund for Scientific Research (FWO-Vlaanderen)

and Bart De Ketelaere is postdoctoral fellow with the Indus-

trial Research Fund (IOF) of the K.U. Leuven.

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