Trends in Food Science & Technology 18 (2007) 37e47

Viewpoint

Shelf-life estimation
from accelerated
storage data
Maria G. Corradini and
Micha Peleg*
Department of Food Science, Chenoweth Laboratory,
University of Massachusetts, Amherst, MA 01003, USA
(Tel.: D1 413 545 5852; fax: D1 413 545 1262;
e-mail: micha.peleg@foodsci.umass.edu)

Traditionally, deterioration rates at elevated temperatures are

extrapolated to lower ones assuming that their temperature dependence obeys the Arrhenius equation, or a similar model.
For such methods to succeed, the spoilage kinetics must be
known in advance and be completely defined by a single
rate constant that must be independent of the foods thermal
history. These assumptions may hold for certain foods and
model systems, but they cannot be universally applicable. In
a proposed alternative approach, no kinetics is assumed at
all and it is taken for granted that the foods thermal history
can and does affect the deterioration pattern. Consequently,
the isothermal chemical degradation or microbial growth
data are described in terms of empirical models that have
the needed number of temperature dependent parameters,
usually two or three. The temperature dependence of these
is also described by ad hoc empirical models that are used
for the extrapolation to lower temperatures. This enables the
estimation of not only the rate constant but also the whole
deterioration curve. The concept is demonstrated with the degradation of vitamin C in frozen spinach and the growth of
a bacterium and yeast at different temperatures. An example
of lowering the salt concentration as a way of accelerating
bacterial growth is also given.

* Corresponding author.
0924-2244/$ - see front matter 2006 Elsevier Ltd. All rights reserved.
doi:10.1016/j.tifs.2006.07.011

The quality of the predictions largely depends on the

quality of the data gathered under the accelerating conditions
and the proximity of these to the conditions of normal
handling and storage. At least theoretically, the proposed
method predictions can be extended to non-isothermal storage
conditions even when the rate is a function not only of the
momentary temperature but also of the foods previous
thermal history. In principle, the same methodology can be
used to predict quality improvement in products undergoing
aging.

Introduction
Accelerated storage has been a widely used method to
assess the shelf-life of foods, pharmaceuticals, cosmetics
and many other industrial products of limited durability.
Since such products are especially designed to undergo
minimal changes during their normal distribution and storage, accelerated storage is perhaps the only practical way
to predict when such products will have to be withdrawn
from the market, if not already consumed. Accelerated
storage can also be helpful in predicting the shelf-life of
perishable commodities, such as refrigerated dairy or
meat products.
The fundamentals of accelerated storage have been discussed in numerous publications. An excellent summary of
state of the art in the field can be found in the work of
Mizrahi (2004). In this book chapter, Mizrahi lucidly
explains the principles underlying the method, presents
several mathematical models to estimate the deterioration
rate of stored foods and alerts the reader to potential sources of error in the use of accelerated storage data. He also
stresses that although accelerated storage is almost always
associated with elevated temperature, in principle at least,
other accelerating factors can be used too, alone or in
combination with high temperature. Mizrahis comprehensive summary is based on a large number of works on
deterioration kinetics, published by several research groups
over at least two decades. Almost invariably, the starting
point of the deterioration kinetics models has been that
the reactions order is known or can be determined from
experimental data, and that the corresponding rate constants temperature dependence obeys the Arrhenius equation. These two assumptions are supported by a large body

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M.G. Corradini, M. Peleg / Trends in Food Science & Technology 18 (2007) 37e47

of experimental data and they are taken for granted in

much of the literature on food spoilage, be it the result of
chemical processes or microbial growth, see also Labuzas
webpage (2000).
Yet, there is reason to suspect that while these two
assumptions have been appropriate and sufficient for predicting the deterioration rate of many foods and possibly
pharmaceutical and cosmetic products, there are spoilage
processes that do not follow this assumed pattern (Peleg,
Corradini, & Normand, 2004). The assumption that the
deterioration process can be characterized by a single
rate constant is limited to reactions that have a fixed
kinetic order, i.e., that their progress rate or logarithmic
rate, is not a function of time. Also, the use of the Arrhenius equation requires that under unchanged conditions,
e.g., constant pH, moisture content, the rate constant,
however defined, is only a function of temperature and
hence totally unaffected by the foods thermal history.
But consider a hypothetical deterioration reaction assumed
to be following the first order kinetics. According to the
Arrhenius model, if the food is kept at 45  C for
a week, say, and then cooled to and kept at 25  C, its
exponential deterioration rate from that point onward
must be exactly the same if it was initially kept at 5  C
for a week and then heated to and kept at 25  C. Obviously, this would be a very unlikely scenario in microbial
deterioration but one can also envision biochemical processes that, too, will not behave in such a manner. Although rarely questioned in the food literature, the
notion that all biochemical processes, regardless of their
mechanistic complexity and interactive pathways, must
have a single energy of activation is by no means selfevident. On the contrary, one can legitimately ask how
all the intermediate steps could be coordinated in such
a way that they will always produce a single temperature
independent energy of activation. If there is such a universal mechanism, which is highly doubtful, its existence has
yet to be demonstrated and explained. Until this is done,
one must consider systems that truly follow the Arrhenius
model as an exception rather than the rule. No doubt the
Arrhenius equation can sometimes provide an acceptable
approximation of the temperature effect on biochemical
reactions, especially when they take place in a model system. But it will be difficult to envision how this model
applies when the chemical environment drastically
changes during the reaction. This is especially the case
whenever microbial growth or decline is involved and
the same can be said about processes involving enzymes.
The above questions concerning the fundamentals of the
traditional theories of deterioration kinetics suggest that it
would be worthwhile to at least explore the merits of alternative modeling approaches. What follows will describe
a way to interpret accelerated storage data without any preconceived kinetic model and to provide demonstrations of
how the methodology could be used in shelf-life predictions from accelerated storage data.

Theoretical background
Accelerated spoilage, be it the result of chemical reactions or microbial growth, can be accomplished in more
than one way. Storage at an elevated temperature is the
most common, of course, followed by exposure to high
relative humidity. But in principle at least, the spoilage
rate can also be increased by the removal of an inhibitory
factor. For example, suppose that the microbial shelf-life
of a given meat product at ambient temperature is determined by the amount of salt that it contains. Then the
products spoilage would be accelerated if the salt concentration is intentionally lowered. Obviously, the two
methods, i.e., reducing the salt and elevating the temperature can be combined (see Mizrahi, 2004). The mathematical treatment of the results, however, might be much
more difficult e see below. But let us first concentrate on
the first two options. The main problem is how to devise
a reliable method, or methods, that will allow the extrapolation of the accelerated storage data in a manner that
will guarantee a correct prediction of what will happen
under normal storage and handling conditions. Had the
deterioration kinetics been completely known, e.g., the
reaction order could be established unambiguously and
so the temperature or salt concentration dependence of
the pertinent rate of the process, one could use the corresponding traditional mathematical model to calculate the
rate at any temperature or salt concentration of interest.
This holds good provided that there is evidence or good
reason to believe that the deterioration follows the same
kinetics under both the normal and accelerated storage
conditions.
There are situations, however, where the deterioration
kinetics is not known a priori and there is insufficient evidence to conclude that it follows any of the traditional
models. Or, worse still, there might be systems where there
is reason to suspect that any model based on a fixed reaction kinetic order, and consequently the Arrhenius equation,
must be inapplicable. Indeed, certain processes follow
models that have two or more temperature dependent
parameters, in which case the rate cannot be expressed
by a single constant, as the Arrhenius equation demands.
Microbial growth, as already mentioned, is a perfect example.
Many isothermal growth curves have a sigmoid shape
whose mathematical description requires no less than two
constants and in many cases at least three. Thus, a maximum specific rate vs. temperature relationship alone will
be insufficient to account for the phenomenon known as
lag, which can vary independently with temperature too.
The same can be said about the asymptotic growth level,
although it usually shows only weak temperature
dependence.
Degradation reactions or microbial inactivation that follows the Weibullian model (see Corradini & Peleg, 2004
and Eq. (1) below), would be another example if the shape
factor or power, n, happens to be temperature dependent.
But even when the power n could be fixed as a constant,

M.G. Corradini, M. Peleg / Trends in Food Science & Technology 18 (2007) 37e47

39

Non-linear degradation at elevated temperatures

Typical decay patterns at different temperatures are
shown in Fig. 1 e top left. The purpose of the accelerated
storage is to predict the curve shown at the top right of the
figure (i.e., at a lower temperature) from those shown at
the top left (i.e., at high temperatures). Fitting of isothermal
decay data can be done with more than one model, using any
of the many commercial software packages available. The
Weibullian model is one example (Corradini & Peleg, 2006):

the meaning of any energy of activation would remain

obscure. A Weibullian decay model, like many growth or
accumulation models, describes situations where the rate,
however defined, is not only a function of temperature
but of time too. How can such models be used for extrapolation? To answer the question, we will consider two kinds
of scenarios: one a chemical degradation process having
a non-linear kinetics and the other logistic (sigmoid)
microbial growth.

Vitamin C in Spinach
Isothermal Degradation

Prediction & Observation

0.8

0.8

C(t)/C0

-20C

0.6

0.6
-12C

0.4

0.4
-8C

0.2
0

0.2

-3C

25

50

75

100

50

Time (days)

150

200

1.5

0.1
b(T) = 0.077*exp[0.081 T]

n(T) = 1.44*exp[0.04 T]

0.08

1.25

0.06

n(T)

b(T) (days-n)

100

Time (days)

1
Extrapolated

0.04
Extrapolated

0.75
0.02

0
-24

-20

-16

-12

-8

-4

0.5
-24

100

-20

-16

-8

-4

-4

1.5
k1(T) = 8.5*exp[-0.11 T]

k2(T) = 0.15-0.05T

1.25

Extrapolated

Extrapolated

75

k2(T)

k1(T) (days)

-12

50

0.75
0.5

25
0.25
0
-24

-20

-16

-12

-8

Temperature (C)

-4

0
-24

-20

-16

-12

-8

Temperature (C)

Fig. 1. Prediction of vitamin C loss in frozen spinach using Eqs. (1) and (2) as models (solid and gray curves, respectively). The original data are from
Giannakourou and Taoukis (2003).

M.G. Corradini, M. Peleg / Trends in Food Science & Technology 18 (2007) 37e47

40

The one below is another:

right. Many of these can be described, with a comparable

degree of fit, by several three-parameter empirical models.
Among them is the shifted logistic function (Corradini &
Peleg, 2005, 2006):

Ct
t
Yt
1
C0
k1 k2 t



Nt
a
a
Yt log


N0
1 expktc  t 1 expktc

Yt

Ct
exp  btn
C0

In both models C(t) and C0 are, respectively, the

momentary and initial concentrations of the monitored
compound, be it a vitamin, pigment, etc. The constants,
b and n, or k1 and k2 are temperature dependent parameters.
The first order kinetic decay is just a special case of Eq. (1)
where n 1. The zero order kinetics is just a special case of
Eq. (2) where k2 0. Thus, all that follows will also apply
to the zero and first kinetics if and when they are encountered but not vice versa.
Similar models can be written for growth or accumulation. In Eq. (1), this can be done by reversing the sign of
the exponential argument and in Eq. (2) by changing the
sign of the second term on the right. Notice that both
models have two temperature dependent coefficients
b and n or k1 and k2. Although these two models often
have a very similar degree of fit, their continuation beyond
the experimental range diverges. Yet, there can be a substantial time span for which they can be used interchangeably (Peleg, 2006). Now, suppose we have enough
isothermal data to plot the temperature dependence of these
models coefficients and express them algebraically (after
curve fitting), the resulting empirical expressions can be
used to calculate the coefficients at any desired temperature. And if the two models hold over a certain pertinent
temperature range, one can construct the whole C(t)/C0
vs. time relationship at any specified temperature within
it. If the above method indeed works, then the predictions
obtained by using Eqs. (1) and (2) as models should be
close (Peleg et al., 2004). The same applies to any model
that fits the experimental data well, provided that it too is
used within the overlap range only. The agreement between the predictions of different models by itself is not
a proof that they are all correct, but it strongly suggests
that they might be. In reality, especially when the database
has only few and scattered entries, the divergence of the
curves will start close to the edge of the experimental
range, in which case only one or none of the models would
provide reasonable predictions. In any case, the decisive
test would be a comparison between the predicted curves
and those recorded experimentally. But, once the underlying model or models are affirmed in this way, then it or
they could be used to predict the deterioration pattern not
only under isothermal conditions, but also under almost
any non-isothermal temperature regime e see below.
Deterioration as a result of microbial growth
Most of the reported isothermal microbial growth curves
have a sigmoid shape of the kind shown in Figs. 2e4 e top

The power model is an alternative:



Nt
a0m tm
Yt log
m m
N0
b t

N(t) and N0 are the momentary and initial numbers, respectively, and a, k and tc or a0, m and b temperature dependent
coefficients.
According to these two models, at t 0, when
N(t) N0, Y(0) 0. As t / N, N(t) approaches a{11/
[1 exp(ktc)} in the first model and a0 m in the second.
[Three is the minimal number of adjustable parameters
that is required to describe the sigmoid growth curve of
many bacteria in a closed habitat. This is the main reason for choosing Eqs. (3) and (4) as models and not the
better known four-parameter Gompertz and Baranyi and
Roberts models.]
If in the accelerated storage experiment the growth
curve is determined at various temperatures, then and as
before, the temperature dependence of the coefficients of
Eq. (3) or (4) can be plotted and expressed algebraically
by ad hoc empirical models. Here again, if the same
model holds over the entire pertinent temperature range,
the terms a(T ), k(T ) and tc(T ) or a0 (T ), m(T ) and b(T ),
could be used to generate the complete growth curve at
any desired constant temperature within this range. Like
in chemical degradation, the models coefficients can be
converted into functions of time, i.e., a(t) a[T(t)],
k(t) k[T(t)], which in turn could be used to generate
non-isothermal growth curves (Corradini & Peleg, 2005;
Peleg, 2000).
Growth after removal of an inhibitory factor
The principles outlined above are also applicable to
accelerated storage achieved by lowering the level of an
inhibitory factor (Fig. 4). Consider microbial growth in
cured meats or cheeses as an example, be it of the products
natural microflora or of a pathogen. The presence of
salts usually suppresses microbial growth. In cured meats,
the salts are sodium chloride and sodium nitrite e part of
it added directly and part produced by reduction of the
also added sodium nitrate. In cheeses, the salt is primarily
sodium chloride sometimes supplemented by a chemical
preservative. In both products, lowered water activity also
contributes significantly to their relative stability. In principle, if one could maintain a constant water activity and temperature, then reducing the salt content would accelerate
the growth by removal of the inhibitory agent. As far as

M.G. Corradini, M. Peleg / Trends in Food Science & Technology 18 (2007) 37e47

41

Pseudomonas fluorescens in REM

Isothermal Growth

Prediction & Observation

10

10
20C

Y(t) = Log[N(t)/N0]

5C

15C

6
10C

0
0

50

100

150

200

250

100

200

300

400

Time (h)

Time (h)
a(T) = 10 (fixed)
125

0.125

tc(T) = 118.*exp(-0.09 T)

0.1

100

0.075

75

tc(T) (h)

k(T) (h-1)

k(T) = 0.017*exp(0.08 T)

Extrapolated

0.05

50

25

0.025

Extrapolated

10

15

20

25

10

15

20

25

20

25

a(T) = 2.5 (fixed)

3.5

150

m(T) = 2.3+0.004 T

b(T) = 139.4*exp(-0.09 T)

Extrapolated

100

m(T)

b(T) (h)

Extrapolated

2.5

2
50
1.5

10

15

20

Temperature (C)

25

10

15

Temperature (C)

Fig. 2. Prediction of Pseudomonas fluorescens growth in a ready-to-eat meal (REM) using Eqs. (3) and (4) as models with a fixed a and a0 , respectively.
The original data are from Tyrer, Ainsworth, Ibanoglu, and Bozkurt (2004).

the methodology is concerned, the procedure should be

very similar. The first step is to record the growth curves
of the organism of interest, or of the total microbial population, at different salt levels. Then the data should be fitted
with the appropriate model, Eq. (3) or (4), for example.
This would be followed by expressing these equations
coefficients as a function of the salt concentration, i.e.,

a(Csalt), k(Csalt) and tc(Csalt) or a0 (Csalt), m(Csalt) and

b(Csalt). Once these terms are determined, they could be
used to predict the growth patterns at any elevated salt concentration, provided that the chosen model indeed holds
over the entire pertinent salt concentration range. At least
in principle, the same can be achieved in other products
by elevating the pH or the amount of moisture, lowering

M.G. Corradini, M. Peleg / Trends in Food Science & Technology 18 (2007) 37e47

42

Candida sake in REM

Isothermal Growth

Prediction & Observation

Y(t) = Log[N(t)/N0]

20C

15C

5C

10C

0
0

50

100

150

200

250

100

200

300

400

Time (h)

Time (h)
a(T) = 7 (fixed)
0.1

150

k(T) = 0.02*exp(0.06 T)

tc(T) = 146.9*exp(-0.07 T)

125
0.075
Extrapolated

0.05

tc(T) (h)

k(T) (h-1)

100
Extrapolated

75
50

0.025
25
0

10

15

20

25

10

15

20

25

20

25

a(T) = 2.35 (fixed)

3

150
b(T) = 159.*exp(-0.07 T)

m(T) = 2.3+0.003 T

125
Extrapolated

Extrapolated

2.5

m(T)

b(T) (h)

100
75

50
25
0

10

15

20

Temperature (C)

25

1.5

10

15

Temperature (C)

Fig. 3. Prediction of the growth of Candida sake in a ready-to-eat meal (REM) using Eqs. (3) and (4) as models with a fixed a and a0 , respectively. The
original data are from Tyrer et al. (2004).

the sugar(s) or a chemical preservative concentration, etc.

Such modifications, however, can influence the inhibitory
effect of synergistic co-factors. But if the collateral changes
are all manifested in the magnitude of a single inhibitory
factor, like the salt concentration, i.e., a(Csalt), k(Csalt),
then these could be used as such to predict the microbial
growth patterns. Otherwise, all the factors and their

interactions would have to be accounted for individually,

which would complicate the mathematical analysis considerably and require an expanded database.
Simultaneous alteration of two or more factors
Suppose one wants to accelerate a products chemical
deterioration by simultaneously elevating its temperature

M.G. Corradini, M. Peleg / Trends in Food Science & Technology 18 (2007) 37e47

43

Yersinia enterocolitica (% NaCl, 7C, pH = 7)

Iso-concentration Growth

Prediction & Observation

7

7
1%

Y(t) = Log[N(t)/N0]

2%

5
3%

5%

4%

6%

0
0

200

400

600

800

200

400

600

800

1000

Time (h)

Time (h)
a(T) = 6.5 (fixed)
0.08

700
k(T) = 0.07/{1+exp[0.8(T-2.6)]}

tc(T) = 26.7*exp(0.5 T)

600
500

tc(T) (h)

k(T) (h-1)

0.06

0.04

400
300
200

Extrapolated

0.02

Extrapolated

100
0

% NaCl

% NaCl

Fig. 4. Prediction of the salt suppressed growth of Yersinia enterocolitica using Eq. (3) as a model with a fixed a. The original data are from the Food
Standards Agency (undated).

and water activity or accelerate its microbial spoilage by

raising the temperature and lowering the salt content. In
the traditional kinetic models, at least in microbiology,
the rate constants temperature dependence is usually described by either the Arrhenius equation or the square
root model originally proposed by Ratkowski (McMeekin,
Olley, Ross, & Ratkowsky, 1993). When two or more influential factors are known to affect the growth or inactivation rate, pH and/or water activity, say, then the
Arrhenius model has been frequently amended by the
addition of a term or terms that are functions of the pH,
aw, etc. Such models can be used for curve fitting but
they have a serious conceptual problem. There is simply
neither evidence nor theoretical reason for the effects of
temperature, pH, aw, or any other factor for that matter,

to be additive or multiplicative as such models imply

(Peleg, 2006). More probably, any change in these factors,
affects the magnitude of the process rate equations coefficients, in a manner that can only be determined experimentally. For example, suppose that a certain deterioration
process follows the model expressed by Eq. (1) and the
temperature dependence of its rate parameter b(T ) is
given by the log logistic model (Corradini & Peleg,
2005, 2006):


bT loge 1 expkT  Tc 

where k and Tc are coefficients. These degradation coefficients, however, are functions of pH, salt concentration,
aw, and other factors, i.e., k k(pH, Csalt, aw, .) and

44

M.G. Corradini, M. Peleg / Trends in Food Science & Technology 18 (2007) 37e47

Tc Tc(pH, Csalt, aw, .). The exact nature of these functions is usually unknown and hence they too ought to be
determined from actual data. The same applies to the
coefficients of all the other models (Eqs. (3)e(5)), where,
k1 k1(T, pH, aw, .), k2 k2(T, pH, aw, .), tc tc(T,
pH, aw, .), etc. These functions, as already mentioned,
must be determined experimentally and there is no reason to assume that any of them follow a universal rule.
This means that determining these functions and their
own coefficients will require a considerable experimental
effort, and expense, making the whole attempt unattractive for most food systems. Perhaps there are reactions
or growth patterns, where the effects of factors like
pH, aw, the presence of salts and the like can be expressed by simple algebraic terms, but they are yet to
be identified.
Demonstration of the concept with published
experimental chemical degradation and microbial
growth data
Vitamin C loss in frozen spinach
Published degradation curves of vitamin C in frozen
spinach stored at three temperatures, 3, 8 and 12  C,
are shown in Fig. 1 (top left). Superimposed on the reported data is the fit of two different empirical models
(Eqs. (1) and (2)). The temperature dependence of these,
fitted with yet another set of ad hoc models, is also
shown in the figures. If these secondary models could
be extrapolated to lower temperatures, as shown in the
middle and bottom plots, then one could predict the degradation curve at 20  C. The predicted curves are
shown at the top right corner of the figure together
with the corresponding experimental data. Although the
first models prediction was an underestimate and that
of the second an overestimate, see Fig. 1 (top right),
both predictions were fairly close to actual observations,
despite that the extrapolation was based on three temperatures only. Alone, this demonstration would be insufficient to support the proposed approach. Yet, the fact
that two very different empirical models yielded a similar
prediction suggests, at least, that the method might have
merit.
Pseudomonas growth in a ready-to-eat meal
Sigmoid growth curves of Pseudomonas fluorescens in
a ready-to-eat meal stored at 20, 15 and 10  C are shown
in Fig. 2 (top left). Also shown in the figure is the fit of
the slightly modified logistic function (Eq. (3)) and the
power model (Eq. (4)). Eq. (3) has three adjustable parameters, the minimum necessary to describe sigmoid curves
of the kind investigated. The parameter a, is a marker
of the asymptotic growth level, specified by a{1
1/[1 exp(ktc)]}, where k is a marker of the curves steepness around its inflection point and tc a marker of the latters
location. For economy, and in order to avoid a large scatter

or unreasonable secondary model parameters, the value of

a was fixed. The same was done with the alternative model
(Eq. (4)) and for the same reasons. [Since the original published growth data have a considerable scatter, standard nonlinear regression, which is solely based on minimizing the
mean squared error, can yield parameters that are physically
meaningless.] The temperature dependence of the two
models parameters is also shown in the figure. As
before, each was described by an ad hoc empirical model,
which was subsequently used for extrapolation to the
lower temperature. Comparison of the predicted growth
curves at 5  C calculated by the two models with experimental observations is also shown in Fig. 2. Both models
predictions were higher than the experimental data, with
the discrepancy reaching about one log unit at the more
advanced growth stage. But in light of the considerable
scatter in the original high temperature data and that
there were only three temperatures to work with, the
match is not unreasonable. That the two models, despite
their different mathematical construction, gave almost
identical predictions suggests that the discrepancy was
due primarily to the original datas imperfections and
not to a methodological flaw in the procedure. Surprising
as it might sound, it is not easy to find high quality microbial growth data at several temperatures. Moreover, because usually the published curves were only determined
once, even a slightly shifted curve at one temperature
could have a large effect on the secondary models parameters and consequently on the model predictions
reliability.

Candida sake in a ready-to-eat meal

The method used for predicting the growth of P. fluorescens at 5  C was also used to predict the growth pattern of Candida sake (a yeast) at this temperature. The
original growth data with the two growth models fit
(Eqs. (3) and (4)) are shown in Fig. 3 (top left). The figure also shows the temperature dependence of the growth
parameters and the secondary models that describe
them e middle and bottom plots e together with the empirical expressions used in the extrapolation. The modified logistic models prediction almost perfectly
matched the actual growth curve of the Candida (see
figure). The prediction of the power model (Eq. (4)),
whose fit was somewhat worse than that of the modified
logistic function at 10  C (see figure), was slightly higher
than the actual observation. Still, the maximum discrepancy hardly exceeded a half log unit, i.e., it was only
slightly larger than the scatter in the experimental growth
data. The better overall predictions than in the Pseudomonas case are most probably due to the considerably
smaller spread of the Candidas high temperatures
data because here too there were only three growth
curves available to determine the model and its coefficients temperature dependence.

M.G. Corradini, M. Peleg / Trends in Food Science & Technology 18 (2007) 37e47

The inhibitory effect of salt on Yersinia enterocoliticas

growth
The previous examples were based on extrapolation
from high temperatures to low. However, the proposed
methodology can also be applicable when the accelerating factor is a lower salt concentration. Published growth
curves of Y. enterocolitica (a food borne pathogen usually transmitted through improperly cooked meats) at
7  C and pH 7 in the presence of 1, 2, 3 and 4%
NaCl, are shown at the top left of Fig. 4. Superimposed
on the experimental data is the fit of the modified version
of the logistic function (Eq. (3)). The temperature dependence of its parameters, also shown in the bottom plot of
the figure, was fitted with ad hoc empirical models as before. These were used to predict the growth curves at 5%
and 6% salt concentrations as seen in the plots at the top
right of the figure. Although the match between the predictions and the reported experimental growth data is far
from being perfect, it is certainly not unreasonable in
the 5% salt case, where the discrepancies were mostly
on the order of half to one log unit. As for the 6%
salt, the experimental results themselves had a large
spread, even by microbiological standards. Yet, the predicted growth curve was not totally out of line, considering the data scatter at the low salt concentrations,
particularly when the storage exceeded 400 h. As
before, each of the individual predictions might not be
considered as convincing evidence to the fact that the
methodology has merits. But that the same method
gave predictions of similar quality in very different systems, described by totally different mathematical models
(Eqs. (1)e(4)), and even for different kinds of accelerating factors, suggests that the concept is not totally unrealistic. And once more, no prediction, be it of the growth
of Yersinia in salty habitat, growth of Candida and Psuedomona at various temperatures or of vitamin loss in
cold storage, has been based on any special preconceived
kinetics. On the contrary, very different mathematical
models could produce similar results, demonstrating
that uniqueness is not a prerequisite. Therefore, the
choice of a model should be guided primarily by practical considerations and not by any attempt to conform to
a traditional kinetic theory.
Simulation of deterioration processes under
non-isothermal conditions
Once the deterioration model has been found and the
temperature dependence of its parameters expressed algebraically, it can be converted into a differential rate equation that can be solved numerically for almost any
conceivable thermal history. This is true for both degradation processes, such as those that can be characterized by
Eq. (1) or (2), and for growth/accumulation processes like
those that can be characterized by Eq. (3) or (4) (Peleg
et al., 2004). The same can be said about alternative mathematical models.

45

As an example, consider the vitamin C loss in frozen

spinach (Fig. 1), the kinetics of which can be expressed
by Eqs. (1) and (5). Under non-isothermal conditions, this
model will become (Corradini & Peleg, 2006):
nTt1


dCt

bTtexp  bTttnTt nTtt nTt
C0 dt

where T(t) is the temperature profile and t* is the inverse of

Eq. (1), i.e., the time that corresponds to the momentary
ratio C(t)/C0.
Eq. (6) is an ordinary differential equation (ODE) and
can be solved in Mathematica with the NDSolve command for almost any conceivable T(t), including discontinuous profiles whose expression requires if statements.
Examples of simulated scenarios of vitamin C loss in
frozen storage under fluctuating temperatures are shown
in Fig. 5 e left. [Although the shown degradation curves
were produced by Mathematica, they can also be produced by other advanced mathematical programs. They
can even be produced by general purpose software like
MS Excel, after conversion of the models rate equation
into a difference equation. In this form, however, difficulties may arise if the temperature fluctuations are too
sharp.]
All the above also pertains to the deterioration caused by
microbial growth. Consider Candidas growth in the readyto-eat meal (Fig. 3), when described by Eq. (3) as the
primary model. The asymptotic growth level was fixed,
i.e., a(T ) 7.0 and the temperature dependence of the parameters k(T ) and tc(T ) was characterized by the algebraic
expressions that are shown in the figure. These, as well as
the temperature profile, T(t), can be incorporated into the
rate models equation, which becomes (Corradini & Peleg,
2005):


dYt kTtaTtexp kTtftc Tt  t g

7
2

dt
1 expkTtftc Tt  t g
where, again, t* is the inverse of Eq. (3), i.e., the time that
corresponds to the momentary growth ratio, Y(t).
Eq. (7) was used to generate the non-isothermal growth
curves that are shown in Fig. 5 e right, together with the
corresponding temperature histories. These plots demonstrate that the temperature history and the rate equations
complexities are not a hindrance to the rate equations solution. Despite the cumbersome appearance of the resulting mathematical expression, the model is solved almost
instantaneously by Mathematica and probably by other
mathematical programs. In fact, the simulations can be
repeated with random histories, thus allowing estimation
of the probabilities of spoilage as a function of time under
uncertain temperature conditions. This, however, is a totally separate topic that is discussed in detail elsewhere
(Corradini, Normand, & Peleg, in press). Whats important here is the demonstrated possibility to develop

M.G. Corradini, M. Peleg / Trends in Food Science & Technology 18 (2007) 37e47

Temperature (C)

46

Vitamin C in Spinach

Candida sake in REM

TEMPERATURE PROFILE

TEMPERATURE PROFILE

20

-5

15

-10

10

-15

-20

10

15

20

25

30

25

DEGRADATION CURVES

50

75

100

125

150

125

150

GROWTH CURVES
7

Y(t) = Log[N(t)/N0]

C(t)/C0

0.75

0.5

0.25

5
4
3
2
1

10

15

20

25

Time (days)

30

25

50

75

100

Time (h)

Fig. 5. Simulated non-isothermal vitamin C degradation and Candida sake growth curves generated with Eqs. (6) and (7) (left and right, respectively).
Notice that the complexity of the temperature history has no noticeable effect on the solution of the models rate equations. Also, once the models
coefficients have been determined from the isothermal data e the actual values are shown in Figs. 1 and 3 e they can be used to generate spoilage
curves under almost any conceivable temperature regime within the range of the models applicability.

a predictive deterioration model from accelerated storage

data without having to assume a kinetic order. If and
when such a model can be derived for a given food,
then, as shown in Fig. 5, it could be used to predict the
quality consequences of an almost unlimited variety of
storage conditions.

Concluding remarks
Shelf-life estimation from accelerated storage results,
in the form of chemical degradation or microbial growth
data, does not require that the process kinetics be assumed a priori. On the contrary, there is good reason
to believe that many, or perhaps even most of the deterioration processes in foods might not follow any of the
standard kinetic models. The assumption that the process
or reaction must follow a particular kinetic is therefore
unnecessary. The same can be said about the use of
the Arrhenius equation to describe the deterioration
rates temperature dependence. It too need not apply,

especially when the isothermal deterioration curve is

not log linear. Reasonable predictions of what happens
at low temperatures, and in one case at high salt concentration, could be obtained by more than one model and
without any prior knowledge of the processs details. It
is even suggested that at least two different mathematical models should be used for mutual verification, thus
increasing the predictions reliability. The described
method is consistent with the fact that the deterioration
rate, however defined, need not be a function of temperature only (and, other factors like pH, water activity,
etc.), but also of time. Thus, in contrast with the traditional Arrhenius equation, the role of the foods thermal
history is not only acknowledged but also becomes an
integral part of the deterioration model itself. The mathematical models to describe the deterioration can be
chosen solely on the basis of their fit and convenience;
they do not have to conform to any theoretical requirement. However, since they are used for extrapolation,
their usefulness is limited to conditions that are not

M.G. Corradini, M. Peleg / Trends in Food Science & Technology 18 (2007) 37e47

too different from those that exist in the accelerated

storage experiments. For example, they cannot be extended to low temperatures if freezing occurs or to exceedingly high salt concentrations that might kill the
organisms rather than merely inhibit its growth. Within
the applicable temperature range, the method could be
used not only to predict isothermal deterioration but
also changes induced by regular and irregular temperature fluctuations. The mathematical procedure to obtain
an isothermal prediction does not require special programming, only access to common non-linear regression
software. The predictions reliability will be primarily
determined by the quality of the accelerated storage
experimental results and their reproducibility. It will
also depend on how many elevated temperature levels
have been employed, or the number of levels of any other
accelerating factors. The more numerous the levels, and
the closer they are to the normal storage conditions, the
higher would be the predictions reliability. In practice,
though, feasibility considerations will dictate the number
and range of the accelerating conditions and these will determine the predictions quality. Because foods rarely have
exactly the same composition, some discrepancies between
the predictions and reality would be inevitable, regardless of
the method used to obtain them. Therefore, an occasional
discrepancy between reality and expectation does not
necessarily invalidate the concept. Theoretically, the methodology can be extended to situations where several factors
affecting the deterioration are altered simultaneously. However, the mathematical treatment of such accelerated storage
experimental results might be too elaborate and the required
database too large for practical implementation.
In principle at least, the same methodology can be
used in reverse, i.e., to predict the beneficial effects
of aging, for example, from short term experiments. But
since we have no data of this kind to work with, it is
merely a speculation at this point. Admittedly, the number
of successful predictions that we have presented in this
article is rather small. Yet, it is probably sufficient to
demonstrate that the concept might work at least in
selected systems.

47

Acknowledgment
Contribution of the Massachusetts Agricultural Experiment Station.
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