REVIEWS
Shelf-life prediction: theory and
application
Bin Fu and Theodore P. Labuza*
Although most food companies have a distinct interest in the shelf-life of their food
products, little has been done to determine true shelf-life as a function of variable
environmental conditions. Research efforts are generally aimed at improving
quality with respect to a longer shelf-life. For true shelf-life prediction, especially
for refrigerated foods, knowledge of predictive microbiology is needed. Models
that describe influences of temperature and water activity on microbial deteriora-
tion are corn ared and the square-root model is found to be the best based on the
criteria of r P and mean square error. Appropriate approaches are presented for
prediction of remaining quality or shelf-life of foods undergoing fluctuating
temperature conditions. Finally, the Weibull hazard analysis technique for
determination of shelf-life is introduced.
Keywords: Shelf-life; prediction; microbial growth; model; Weibull hazard
INTRODUCTION
The shelf-life of a food is the time period for the
product to become unacceptable from sensory,
nutritional or safety perspectives. The criterion level
corresponding to the end of shelf-life is determined by
any legal requirement, e.g. the 80/80 rule for nutri-
tional loss in natural foods, as well as consumer taste
attributes, marketing distribution requirements and
cost. From the viewpoint of the food industry, shelf-life
is based on the extent of quality loss in a food that the
food company will allow prior to product consumption.
At that point, the food may still be organoleptically
acceptable. For consumers, the end of shelf-life is the
time when the food no longer has an acceptable taste.
Realizing that one can never satisfy all consumers all of
the time and that food systems, along with their
mechanisms of deterioration, are inherently complex, a
universal definition of shelf-life is thus virtually impos-
sible to establish. Despite this, shelf-life can be deter-
mined, and subsequently predicted, for individual food
Department of Food Science and Nutrition, University of
Minnesota, 1334 Eckles Avenue, St Paul, MN 55108, USA.
*To whom correspondence should be addressed. Presented at
the International Food Technology Exposition and Confer-
ence (IFTEC), 15-18 November 1992, The Hague, The
Netherlands
0956-7135/931030125-09 0 1993 B’utterwotth-Heinemann Ltd
analysis
products based on some primary mode of deteriora-
tion.
Microbiological decay is one of the major modes of
food deterioration, especially for fre$r or minimally
processed refrigerated products. Microorganisms may
cause spoilage of foods or result in foodborne diseases.
Processors should conduct shelf-life tests to determine
when spoilage occurs and should verify the effective-
ness of the various barriers to pathogenic growth, using
appropriate scientific studies to evaluate potential risk
of their food products (NFPA, 1988). Spoiled products,
even if no health hazard is present, are considered
adulterated in the USA under Section 402(a)(l) and
402(a)(3) of the Food, Drug and iCosmetic Act.
Accurate shelf-life prediction is an impbrtant aspect of
food science, not only to corporations but to govern-
ments and the general public as well. A premature loss
of shelf-life can lead to a loss of consumer confidence
and of revenues to the food manufackurer. Shelf-life
testing also allows the company to m nimize costs in
formulation and packaging. Open dat I ng (e.g. sell-by
date and best-if-used-by date) of foods must be based
on some type of shelf-life testing as well. With the new
EC requirements, all foods must have some type of
open date.
To predict the shelf-life of refrigerated foods based
on microbial growth, the concept of ‘predictive micro-
biology’ must be employed (e.g. Buchanan, 1993).
Growth of microorganisms are first studied under
Food Control 1993 Volume 4 Number 3 125
Shelf-life prediction: 6. Fu and T.P. Labuza
several different but fixed conditions. An appropriate
growth curve model (e.g. Gompertz model) can be
applied to the data (Zwietering er al., 1990), from
which growth parameters (such as specific growth rate
and lag time) are derived. Then another model is
employed to determine the effects of compositional and
environmental factors on the growth. The combination
of the above two steps can be used to predict the
microbial level and thus the shelf-life and safety of
perishable foods under commercial distribution con-
ditions. Models with one or two variables are practic-
ally useful, even though multivariant response surface
models (Buchanan et al., 1989; Gibson and Roberts,
1989; Buchanan and Phillips, 1990) can also be used to
predict the growth of microorganisms in response to
food formulation, packaging and environmental fluc-
tuations, as long as the limits of the model are not
exceeded. This latter approach is especially useful in
the stage of new product development.
The purpose of this paper is to present the mathe-
matical models that are available to describe quantita-
tive effects of temperature and water activity (a,,,), with
the emphasis on temperature, on microbial growth
parameters, particularly specific growth rate and lag
time and to demonstrate the applicability of these
models in predicting shelf-life of foods under real world
conditions. Since sensory evaluation is often used in
evaluating quality deterioration of perishable foods,
the Weibull hazard analysis technique is introduced for
shelf-life determination. Nutrient degradation reac-
tions, such as the browning reaction, vitamin C loss
and lipid oxidation, which are important to many other
foods (Labuza, 1984) will not be discussed.
MICROBIAL GROWTH AS A FUNCTION OF
TEMPERATURE AND WATER ACTIVITY
There are many temperature-dependent models to
describe microbial growth in the literature (Zwietering
et al., 1991; Labuza et al., 1992; Buchanan, 1993),
however, only a few are applicable for practical shelf-
life prediction. Based on Bayesian statistical analysis
(also known as Ockham’s Razor rule), the fewer
number of parameters in a model, the closer to reality
based on physical principles is the equation (Jefferys
and Berger, 1992). Thus a higher order model may give
a very good fit but then eliminates the ability to
determine the effects of various factors on the precision
of the measurement. Therefore, only simple models
with two or three parameters will be discussed below
with a comparison based on r2 and mean square error
(MSE).
Arrhenius model
Since microbial growth is a biochemical process, it is
expected that, for a certain temperature range, the
Arrhenius law would follow. Thus the temperature
dependence of the growth rate can be characterized by
an overall activation energy if all other ecological
factors are kept constant. This two-parameter function
takes the form:
126 Food Control 1993 Volume 4 Number 3
where k is the specific growth rate determined from the
growth curve, A is the collision factor, T is the absolute
temperature (K), R is the universal gas constant
(8.314 J mol-’ K-‘) and EA (J/mol) is called the activa-
tion energy, which is a measure of the temperature
sensitivity of the growth rate. The value of EA can be
determined from the slope of the plot of In k versus l/T.
Successful applications of Equation (1) for predictive
microbiology are available in the literature for many
different organisms if the temperature range used is
limited (Labuza et al., 1992). Significant deviation from
linearity for the plot of In k versus l/T has also been
noted by Ratkowsky et al. (1982) if too large a
temperature range is used. The Arrhenius relationship
can also be applied to model the temperature depend-
ence of the lag phase, which would be critical for
prediction of the shelf-life under variable temperature
conditions where there is an initial low microbial load.
The inverse of the lag time (l/t,, i.e. lag rate) is used to
make the Arrhenius plot. Kinetic parameters for the
exponential and lag phase are given in Table I for the
data of Fu et al. (1991).
Davey (1989) modified the Arrhenius equation for
predicting the combined effect of temperature and a,
on the growth rate of bacteria which took the form:
In k = CO+ C,IT+ C2/T2 + C, a, + C, aw2 (4
where C,, to C, are the five coefficients to be deter-
mined by multiple-linear regression. It generally gives
good fit due to added terms. This equation has also
been used for lag time data (Davey, 1991). When a, is
kept nearly constant, which could be true for most fresh
foods since it would require a significant moisture
content change to alter the a, significantly, Equation
(2) can be simplified to account only for the effect of
temperature. Table I shows that the Davey model gives
a higher r2 and lower MSE than the Arrhenius model
for both growth phases.
Square root model
Ratkowsky et al. (1982) proposed a simple two-
parameter empirical equation for the temperature
dependence of microbial growth up to the optimum
temperature (T,,,) as:
V/k= b(T- Tmin)
(3)
where k is the specific growth rate as before, b is the
slope of the regression line of ti versus temperature,
T is the test temperature (in either “C or K) and Tmin
is the notional microbial growth temperature where the
regression line cuts the temperature axis at fi = 0.
This equation generally gives a better linear fit from the
Tminup to and including the Topt.
Ratkowsky et al. (1982, 1983) showed that the
equation accurately described the growth rate data of
many organisms. However, since the actual Tmin for
growth may occur several degrees above the extra-
polated values, the growth predicted near the lower
extreme of growth temperature based on the square
root equation, could be more than would actually
occur. The kinetic parameters of the square root model
for Pseudomonas fragi growth are provided in Table I.
As seen it has a slightly larger r2 value and significantly
lower MSE for both phases, than does the Arrhenius;
 Shelf-life prediction: B. Fu and T.P. Labuza

Table 1 Model equations and kinetic parameters determined for Pseudomonas frugi in a simulated milk”

Arrhenius model Davey model Square root model Linear model Exponential model

Exponential phase
Equation Ink=30.10- Ink= -160.97+ d/k = O.O306(T+ k- -0.0315(1 - k = 0.088 e”.“” T
(8.90 x 103/T) (99.92 x 10”IT) - 7.85) l.17T)
(15.48 x w/T*)

Parameters InA = 30.10 c,= -160.97 b = 0.0306 h-“‘“C a = -0.0315 h-’ k,, =+0.088 h-’
EA = 73.9OkJlmol C, = 99.92 x 10’ Tmi. = -7.85”C c= -1.17”C s=o.llo”c~-’
c*= -15.48X10h

r2 0.984 0.999 0.998 0.976 0.977

MSEb 0.00260 0.00013 0.00007 0.00144 0.00420

Lag phase
Equation In (l/t,) = 29.90- In(l/t,) = -237.75 l/v/t, = 0.0172 (T+ l/r, = -0.0093(1 - l/t, = 0.026 e”.“3 ’
(9.17 x 103/T) + (143.24 x 7.65) I .22 T)
103/T)-(2168x
lob/T*)

Parameters In A = 29.90 C, = -237.75 b = 0.0172 h-“*“C a = -0.0093 h-’ k,-O.O26h-’

EA = 76.20 kJ/mol C, = 143.24 x lo3 Tmi. = - 7.65”C c = - I .22”C’ s=o.113”c-’
C, = 21.68 x lo6

r2 0.963 0.994 0.993 0.980 0.956

MSE 12.79 2.79 2.53 175.72 13.99

“Based on the data of Fu et al. (1991)

bMSE = Z[(observed - predicted)%]

and similar r* but lower MSE than does the three-
parameter Davey model.
McMeekin et al. (1987) modified the basic square
root equation to incorporate a,:
d/k = Cv(a,,,- MINa,)(T- Tmin)
where C is a constant and MINa, is the theoretical
minimum a, for growth of the organism. This equation
may be used for predicting the growth rate at any
combination of a, and T as long as they are in the test
range (McMeekin et al., 1987).
Linear model
Spencer and Baines (1964) proposed a linear model
based on the research of microbial growth on white
fish. They postulated that the effect of temperature on
the rate of spoilage of fish stored at a constant
temperature between -1 and 25°C was found to be
approximately linear and could be expressed in the
form:
on r2 value but the MSE is very high for the lag phase
data.
Exponential model
(4) If the temperature range of concern is no more than 20
to 30 degrees, then a simple plot of thei specific growth
rate on semilog graph paper versus temperature
(instead of inverse absolute temperature) also gives a
straight line. The exponential model has the following
form:
k = kOexp (ST) (6)
where k is the specific rate at T in “C, and k,, is the
specific rate at O”C, s is the slope of a plot of Ink
versus T. This model is also applicable tb lag phase data
or shelf-life data (Labuza, 1984). As s own in Table 2,
the exponential model has essentially % t e lowest r2 for
both phases, the highest MSE for the exponential phase
and the second to highest MSE for ; the lag phase.
Overall speaking, the square root model best fits both
the lag and exponential phase data of p. fragi growth.

k=a(l+cT) (5) Qro and other models

where k is the specific growth rate at storage tempera-
ture T(“C), a is the rate at 0°C and c is the
temperature coefficient (UC). Thus a plot of the
growth rate k versus T gives a straight line. Such a
response would be expected if both the temperature
range and the EA were small and if the organism was
able to grow at a few degrees below 0°C.
Jorgensen et al. (1988) reported that the shelf-life of
iced whole cod can be predicted using a linear model
but not that of vacuum-packed fillets because of the
greater variability of bacterial activity in packaged fish.
The parameters for the same data from Fu et al. (1991)
are shown in Table I. As seen, it fits fairly well based
Q,o is defined as the temperature isensitivity of a
reaction.It is the increase in reaction (or growth) rate
or the decrease in shelf life for a~ 10°C increase
in temperature. It has been used to predict quality or
nutrient losses for many foods and potency degradation
for drugs. The Qio is usually assumed’constant over a
narrow range of temperature. Reporte, L Qio values for
microbial growth under refrigeration conditions range
from 2 to 10. The relationship of Qio~with previously
discussed models and the Qio values for P. fragi growth
(Fu et al., 1991) are shown in Tab@ 2. As seen, a
different temperature model can lead to a different (2 i.
value at the same reference temperature.

Food Control 1993 Volume 4 Number 3 127

Shelf-life prediction: 6. Fu and T.P. Labuza
Table 2 The relationship of Q,(, with other models and Q,,) values for P. fragi growth
Model type Q,,) expression
Arrhenius
Davey exp
(-lOC,
(T+ 10 - T,i,)’
T(T+ 10) - 10&(2T+
T*(T+ lo)2
Square root
(T- T,i,)*
IOC
Linear 1+-
l+cT
Exponential exp (10s)
“Based on the parameters in Table I and calculated at T = 4°C
SHELF-LIFE PREDICTION IN THE REAL
WORLD
General consideration
Under the ideal conditions, the level of microbial
growth or shelf-life of a food based on microbial growth
can be easily predicted by using the following
equations:
N = No exp [k(t - tL)]
ts = In (N,IN,)Ik + tL
where No is the initial microbial load, N is the microbial
level at time t, N, is the microbial level corresponding
to the end of shelf-life, t, is the shelf-life at that constant
temperature, k and tL are the specific growth rate and
lag time at a constant storage temperature, which can
be predicted from an appropriate model, such as the
square root model as discussed earlier. For example,
Griffiths and Phillips (1988) were able to predict the
shelf-life of pasteurized milk at different constant
storage temperatures using the square root model for
microbial growth developed from several other con-
stant temperatures ranging from 2-14°C.
Unfortunately, the reality is not that simple. Shelf-
life depends on the initial level of contamination of the
product. However, the initial microbial load is usually
not well controlled in real foods. With pasteurized
milk, Maxcy and Wallen (1983) noted considerable
variation in initial levels of contamination which was
responsible for differences in product shelf-life. This
presents a serious problem for shelf-life prediction, but
may be overcome by specifying a maximum initial level
of the contamination organisms of concern. A rela-
tively stable initial No value can be set by employing the
hazard analysis and critical control point (HACCP)
system and good manufacturing practice (GMP) pro-
cedures and taking into account the shelf-life required
for a particular market. No more than 10 pseudo-
monads per ml was deemed to be appropriate for
pasteurized milk (Chandler and McMeekin, 1989).
In addition, the variety of species that make up the
initial population is not always known. If two types of
microbes or strains with different Q,, values are
responsible for the quality loss in a food, the one
128 Food Control 1993 Volume 4 Number 3
Q,,) for P. fragi growth”
Lag phase Exponential phase
3.2 3.1
10)
>
3.7 3.4
3.5 3.4
4.1 4.2
3.1 3.2
with the higher Q,u may predominate at higher
temperatures and the other with the lower Q,, may
predominate at the lower storage condition, confound-
ing the prediction. Spoilage at different temperatures
could be attributed to the growth of different groups of
bacteria and could be influenced by package type. On
the other hand, a product-dependent factory flora may
be established, specifically selected/adapted to growth
in the conditions prevailing in the food or factory
environment. Such a flora may modify the spoilage
(7a) characteristic and shelf-life of a product.
Another consideration is the correlation of microbial
(7b) level with the quality or shelf-life. In general, a
bacterial level of 106-10’ cfu/unit (Ns) indicates the end
of shelf-life. However, in some products, the number of
microbes may not be a valid indicator for shelf-life. In
these cases, the quality deterioration caused by micro-
bial growth may be better evaluated by other indices,
e.g. organoleptic quality change. If a toxin-producing
pathogen is concerned, then the shortest lag time
before the toxin can be detected may be used as the end
of shelf-life (Baker and Genigeorgis, 1990).
To predict the growth under variable time-
temperature conditions, researchers usually run kinetic
experiments at several constant temperatures to obtain
kinetic growth parameters for the organism. Because of
the possible shift of dominant microorganisms and
the minimum-optimum-maximum temperature
behaviour, the choice of the temperature range for such
a study is quite limited. Suggested values for refriger-
ated foods are 4-15°C with controls stored at just
above the freezing point.
One more concern is the history effect, which is
defined as the situation in which the actual growth rate
that is measured after a temperature shift is signifi-
cantly different from that predicted by a model under-
going the same temperature shift. Several varying
temperature studies of microbial growth showed some
history effects (Ng et al., 1962; Shaw, 1967; Fu et al.,
1991), yet others did not find any history effect within
the temperature range studied (Langeveld and
Cuperus, 1980; Simpson et al., 1989). If there is a
history effect, the prediction for microbial growth rate
and lag time using any model may significantly deviate
from the real growth. In the following discussion, we
assume there is no history effect or that the effect is
negligible.
 Shelf-life prediction: B. Fu and T.P. Labuza

Prediction with known time-temperature history Table 3 Simulated variable time-temperature history and the
calculated microbial counts after each condition based on the square
The food industry has for many years used some type of root equation
temperature recording devices for monitoring distri-
Time Temperature N, = Microbial count”
bution, especially for frozen or refrigerated foods
(h) (“C) (cfu/ml)
(Anonymous, 1992). Originally these devices were
wind-up motors with a bimetallic sensor that gave an o-12 4 1.0x 10’
ink pen trace on a chart. One had to scan the chart 12-24 8 3.11 x IO’
visually at the end of distribution to determine if the 24-30 12 2.4 x lo*
30-36 16 6.4 x IO’
trace showed potential damage, e.g. going below 36-42 I4 1.0x IO5
freezing for fresh produce. The next generation of 42-48 IO 6.6 x IO5
recorders used thermocouples or platinum-iridium 48-60 8 1.4x 10’
thermistors and battery driven charts. Finally, the use 60-12 6 8.8 x 10’

of computer chips resulted in very small programmable Time to reach lOh cfu/ml (h) Slh
units with a memory chip, which records the time-
temperature exposure for subsequent down-loading of ‘Calculated for the end of each period assuming N,, - 10 cfu/ml and
no history effect
the data to a spread sheet. All these recorders will
provide time-temperature history information for a
practical distribution. There are several ways to inter- variable time-temperature conditions. Table 3 shows a
pret these data. simulted time-temperature history and the calculated
microbial counts after each condition Ifor the P. fragi
Numerical integration approach growth using the square root model. As shown, with
Since temperature fluctuations with time are usually N0 = lOcfu/ml and N, = lO”cfu/ml, the square root
random and no simple mathematical expression can be model predicts a shelf life of 51 h.
used to describe the time-temperature history, one
of the accepted approaches is to divide the time- Effective temperaturelequivalent time abproaches
temperature history into short, assumed-constant To calculate the cumulative effects of a variable
temperature intervals and determine the lag time from time-temperature history, the concept ~of an effective
Equation (8a) and the growth from Equation (8b) temperature (T,,) can be introduced, hich is defined
as the constant temperature that resu1 ts in the same
tr = $J At; with 2 (IltLi) Ati = 1 for Odt<tL growth or quality change as the variable temperature
,=I i=l distribution over the same period of time. Then:
(84 N = No exp [k( Teff) t] = No exp (k,, ‘t) for t > tL

for t > tLd (8b) (9)

The rate constant at that defined temperature is termed
the effective rate constant (keff). The1 expressions for
Any good temperature-dependent growth model can
T,, and keff as well as tL using the square root model
be used to get the value of tLi, kj for that small time
are listed in Table 4. It should be noted that due to the
segment. This approach was originally used to evaluate
different temperature sensitivities between the two
the organoleptic shelf-life of frozen foods and called
growth phases and the different time-temperature
the TIT (time-temperature tolerance) approach
history they are exposed to, the effective temperature
(Gaudagni, 1957).
for the exponential phase is usually difjferent from that
The shelf-life and microbial growth kinetics of chilled of the lag phase.
reconstituted orange juice (Kopelman and Efroni,
Similarly, one can introduce the’ concept of an
1977) and of fresh citrus juices from Shamouti orange
equivalent time (t,,), which is defined~ as the time at a
(Kopelman and Rauchwerger, 1984) were studied using reference temperature (krer as the specific rate) result-
Arrhenius kinetics. The kinetic data were used success- ing in the same amount of growth or quality change
fully for the prediction of microbial growth under as the variable time-temperature distribution. Then
variable time-temperature conditions using the TIT
Equation (10) can be written as:
method. Similarly Saguy (1992) emphasized this
approach to predict the extent of Listeria growth under N = NOexp (k,,f t,,) (10)
Table 4 Simulated calculation of effective rate constant, effective temperature and equivalent time for the data in Table 3

Parameters Equations Lag phase Exponential phase

19.1 0.303

5.6 10.1

T(r) - Trmn 2 dt

kc,(h) 24.9 122.1

Trer- Tmin1

“Assume T,,, = 4°C

Food Control 1993 Volume 14 Number 3 129

Shelf-life prediction: B. Fu and T.P. Labuza
The expression of teq for the square root model is given
in Table 4, in which the calculated effective rate
constant, effective temperature and equivalent time for
the simulated data in Table 3 are also shown. Based on
the parameters in Table 4, the predicted growth
determined by the effective temperature approach is
about 9.1 X lO’cfu/ml, while the equivalent time
approach predicts the same amount of growth as that
observed in Table 3. These approaches will be able to
provide information on remaining quality or shelf-life
of the food at a target storage temperature after
exposure to a variable time-temperature history. It can
also be used to compare the effectiveness of different
distribution chains.
Applications
Charm et al. (1972) correlated spoilage of fish at
different temperatures to the shelf-life at ice storage.
From this, they developed the ‘shelf-life prediction
slide rule’ (Ronsivalli and Charm, 1975), which was
essentially based on the equivalent time approach using
the exponential model that allowed a rapid estimate of
the remaining shelf-life of lean fish. Electronic time-
temperature recorders are now being used with the
product in distribution where one of the predictive
models is used in a software package to do the
calculation. Nixon (1977) developed a temperature
function integrator to assess storage conditions in fish
holds, which can predict the remaining shelf-life of the
product at 0°C. Daud et al. (1978) used the same
integrator to predict the remaining shelf-life of poultry
tissues. There was close agreement between the rela-
tive growth rates of spoilage bacteria in poultry
predicted by the integrator with experimental values at
storage temperatures up to 16°C. A versatile time-
temperature function integrator (TTFI) for predicting
the degree of bacterial spoilage occurring in chilled
foods during storage was described by Owen and
Nesbitt (1984). The equivalent time approach was used
to predict the remaining shelf-life at the reference
temperature, or any other temperature in the psycho-
trophic range. The key to all these systems is the use of
the proper equations for modelling of growth and an
understanding of kinetics.
The advantage of using an electronic recorder or
a computer is that one knows the exact time-
temperature history, which helps one to find the
troublesome point in the distribution easily. On the
other hand, all of these recorder devices are relatively
expensive (US$20 to > US$SOO) and monitor the
environment of a case, pallet load, truck, train, etc.,
not necessarily the individual food pack. In addition,
the recorded information usually ends once the product
is delivered to the supermarket or the retailer, especi-
ally to the consumer. Since none of these devices give
useful information to the consumer, the idea for an
individual package time-temperature monitoring
device that is consumer friendly, was born.
Prediction with unknown time-temperature history
Physical/chemical time-temperature indicators/
integrators can be used to integrate a time-
temperature distribution function to which a perishable
130 Food Control 1993 Volume 4 Number 3
product is subjected from the point of manufacture to
the display shelf of the retail outlet if on the case, or
eventually to the consumer if on the individual food
package (Taoukis et al., 1991). The change of a time-
temperature indicator is usually expressed as a simple
and easily readable response in the form of a mech-
anical deformation, colour development and colour
movement. The rate constant for the change follows
the Arrhenius relationship. The EA(7TI) values of the
commercially available indicators cover the range of
the most important deteriorative reactions in foods (Fu
and Labuza, 1992).
Effective temperaturelequivalent time approaches
The correlation of time-temperature indicators with
foods can be based on either the effective temperature
approach or the equivalent time approach. From the
responses of a TTI tag, one can calculate TewCrrIj or
t=n-w at a reference temperature, then with the
assumption of Teff(nI) = Teff(food) or feq(7TI) = kq(food),
one can calculate the quality change or shelf-life
remaining after exposed to a variable time-
temperature distribution without knowing the exact
history. For the above relationships to be held, the
following requirement must be met, i.e. EACmIj =
EACfoodj.If the difference is large, then an error will be
introduced in the prediction, which has been discussed
by Taoukis et al. (1991). For a specific food to be
monitored, the key is to choose a right ITI tag.
Equivalent point approach
Since almost all TTI tags tested so far follow the
Arrhenius relationship, in this section the Arrhenius
equation will be used to introduce the equivalent point
approach. For the TI’I response, f(x), one can write:
f(x) = ~OI exp[- EAU-I-I)VWIt (11)
Let f(n)lkol = Y, then the above equation can be
transformed into:
In Y = - E,,,,j(RT) + In c (12)
If there are two or more TII tags with different
temperature sensitivities (i.e. different activation
energy values) on the package, then a plot of In Y
versus Ea(nr) g ives a straight line. From the slope, T,
can be calculated and te can be calculated from the
intercept. That is, the unique point of (T,, t,) for a
variable time- temperature is defined. Thus, for any
quality deterioration reaction, the change can be
predicted for the same variable time-temperature
distribution, as long as the value of ,!?A@&) falls in the
range of the ITIs. For microbial growth, the following
equation can be used:
(13)
where tLe is the lag time at the temperature of T,.
The advantage of this approach is that it eliminates
the strict requirement of E,+(fOod)= EACmIj. However,
it may be too costly to use two or more different types
of TTI tags on the same case or package. An alternative
approach would be to design a tag which contains two
or more chemical or biological components showing
different temperature sensitivities.

Applications
ITI tags have been used to monitor distribution
effectiveness, manage inventory, indicate quality or
shelf-life as well as predict food safety. Some actual
application cases are given by Taoukis et al. (1991).
Potential use of TTIs as indicators of temperature
abuse of modified atmosphere packaged products has
also been discussed (Fu and Labuza, 1993). Sherlock
et al. (1991) examined the applicability of some
consumer-readable TITS for monitoring the end of
shelf-life of refrigerated foods. The survey done by
Sherlock and Labuza (1992) showed consumer accept-
ance for TTI use for dairy products. One of the
limitations of using a ‘IT1 tag is that it senses only the
package or case surface temperature, not the internal
temperature of the food itself. This could result in the
unnecessary disposal of safe food with acceptable
quality (Malcata, 1990). The cost of a TTI may also be
another limitation for its current application, which is
about OS-50 US cents/unit.
WEIBULL HAZARD ANALYSIS FOR
PREDICTION OF SHELF-LIFE
To evaluate the quality of foods, food scientists use
microbiological tests and objective chemical or physical
analytical methods which must ultimately be correlated
with organoleptic data to establish their reliability as a
quality index. For many years the shelf-life of the
majority of foods has only been evaluated from
observing the time taken to arrive at undesirable
sensory or microbiological changes. The extreme
differences in spoilage rates of individual units within
sample sets indicated sensory evaluation of multiple
samples to be the most logical, simple criterion for
evaluating shelf-life. In addition, because of the
variable sensitivity of consumers to taste and odour,
large panels are needed for statistical analysis. Statisti-
cal techniques are available to establish the accuracy of
estimates desired (Maxcy and Wallen, 1983; Labuza
and Schmidl, 1988).
A fundamental assumption underlying statistical
analysis of shelf-life testing experiments is that the
shelf-life distribution of a food product belongs to a
family of probability distributions. Parameters of a
shelf-life distribution are estimated by use of shelf-life
testing experimental data. Once the parameters of a
shelf-life model have been estimated, it can be used to
predict the probabilities of various events, such as
future failures. The other assumption here is that the
observations are statistically independent. Both statis-
tical and biological rationale should be considered in
selecting a distribution function. It seems that the
Weibull distribution fits best for a food system and is a
technique that allows for the use of smaller sample sizes
(Gacula and Kubala, 1975; Labuza and Schmidl, 1988).
The Weibull hazard analysis method is a graphical
method also known as the maximum likelihood pro-
cedure. This procedure is done by first estimating the
end of shelf-life which becomes the estimated time limit
of the study that is fairly close to the actual or desirable
end of shelf-life. The total time is then divided into
equal time segments, at which points panellists rate the
product as acceptable or unacceptable, with additional
Shelf-life prediction: 6. Fu and T.P. Labuza
panellists added at a constant number for each sub-
sequent time period to maximize the number near the
end of the test. When the product is identified at any
time as unacceptable by 50% or more of the panellists,
the number of testers for the next period is increased by
the number of failed samples plus the constant number.
The interval between sample times is, also shortened
since one is closer to the end of shelf-life. The test ends
when no more samples or panellists ari: available. The
scores are ranked in reverse order, i.e., the sample that
was spoiled first receives the highesl rank and the
sample that was spoiled last receives the lowest rank =
1. Then hazard values (H) are calcblated for each
sample using their rank scores, i.e. Ht lOO/Rank and
the cumulative hazard values are calcdlated. Thus, the
critical probability, pc, can be calcdlated from the
following equation:
pc= lOO(l-exp(-CH/lOO)) (15)
A pc of 50% corresponds to an accqmulated hazard
value of 69.3%.
The relationship between the logaliithm of storage
time (log t) and the logarithm of hazard value (logZ,H)
is linear, as shown below:
logt=(llb)logCH+loga (16)
where b is the shape parameter and a is the scale
parameter. The shelf-life can then be determined based
on the desired probability level allobed for product
failure. The lower the probability, the phorter the shelf-
life. This plot then allows one to ma&e a management
decision with respect to the probabilitk of displeasing a
certain fraction of consumers. It is~ hoped that the
distribution time is such that greater ithan 99% of the
product is consumed before the end df shelf-life based
on displeasing less than X% of consqmers where X is
the economic value. A detailed exaqple was given by
Labuza and Schmidl(l988). It should be noted that any
simple objective test may be used dnd some quality
level is set as the unacceptability lidit. For microbial
testing, a criterion such as lo6 cfu/unitl can then be used
as the negative response. This propedure does not
require control samples.
For example, a fish processor is ~more interested
in ensuring that a sufficiently larde proportion of
customers finds his/her products ac4eptable and will
want to base the shelf-life on such a cliiterion. Different
criteria for the limit of shelf-life give different estimates
for the shelf-life but a marketing-jriented criterion
which requires at least 70% (i.e. F<30%) of the
population to express some degree of liking gives a
shelf-life for iced cod of betweed day 9 and 12
depending on the method of presenkation (Howgate,
1985). Figure 1 is an example of tieibull plot for a
refrigerated food based on assumed dbta. A shelf-life of
16 days is found at pc = 50% from the graph.
The Weibull distribution has beed used for several
food products (Wittinger and Smith, ~1986;Labuza and
Schmidl, 1988; Schmidt and Bouma, 1992). This type of
testing could be done at several temperatures or for a
product in a real distribution as wa$ done by Gacula
(1975) for the shelf-life of refrige ated cured meat
products. In this case the end of sh,i If-life was due to
off-odour and slime as a result of jnicrobial growth.
Thus the exponential modei can be lapplied to predict
Food Control 1993 Volume 4 Number 3 131
Shelf-life prediction: B. Fu and T.P. Labuza
Probability (%)
0.1 1 IO 50
1 1 1 I
2 _____-_---------
*
z
‘0
%
3 chloride,
1 temperature and salt concentration/water activity on the growth
.Ol .l 100
Figure 1 An example of Weibull plot for a refrigerated
shelf life of 16 days is found at pc = 50%
the shelf-life under different storage conditions. The
reliability of this approach for predicting the shelf-life
under fluctuating environmental conditions has rarely
been evaluated, especially for refrigerated foods.
CONCLUSION
The shelf-life of a product can be determined using
kinetically designed experiments as well as Weibull
hazard analysis. The goal for the food industry is not an
absolute value of the shelf-life, but rather the assurance
that shelf-life is longer than the time of normal product
distribution and consumption. Knowledge of kinetics
and modelling of microbial growth as well as experi-
mental design will help one to determine the shelf-life
of a food at a targetted storage temperature and to
predict the shelf-life of the food under fluctuating
environmental conditions.
It should be noted that many other factors influence
microbial growth and food stability of refrigerated
foods. For example, gas composition is critical for the
safety and stability of chilled modified atmosphere
packaged products (Labuza et al., 1992). In addition, in
many cases shelf-life studies are done with product
made in the pilot plant using fresh ingredients, whereas
in the real world the ingredients also have their own
shelf-lives and the final formula and package may be
different from that which was tested. Therefore,
confirmatory field shelf-life test would be desired.
ACKNOWLEDGEMENTS
The research was supported in part by a 1992-1993
Graduate Dissertation Fellowship of the University of
Minnesota and the Minnesota-South Dakota Dairy
Research Center. It is published as paper No. 20 108 of
the contribution series of the Minnesota Agricultural
Experiment Station.
REFERENCES
Anonymous (1992) Transit Temperature Recording-Origin
History Cox Recording Co., Long Beach, CA
Baker, D.A. and Genigeorgis, C. (1990) Predicting the safe storage of
fresh fish under modified atmospheres with respect to Clostridium
132 Food Control 1993 Volume 4 Number 3
botulinurn toxigenesis by modeling length of the lag phase of
99.99 growth. J. Food Prot. 53, 131-140
I Buchanan, R.L. (1993) Predictive food microbiology. Trends Food
Sci. Technol. 4, 6-11
Buchanan, R.L. and Phillips, J.G. (1990) Response surface model for
predicting the effects of temperature, pH, sodium chloride
content, &hum nitrite concentration, and atmosphere on the
growth of Listeria monocytogenes. J. Food Prot. 53,370-376,381
Buchanan, R.L., Stahl, H.G. and Whiting, R.C. (1989) Effects
and interactions of temperature, pH, atmosphere, sodium
and sodium nitrite on the growth of Listeria mono-
cytogenes. J. Food Prot. 52, 844-851
Chandler, R.E. and McMeekin, T.A. (1989) Combined effect of
1000 rate of Halobacterium spp. J. Appl. Bacterial. 67, 71-76
Charm, S.E., Learson, R.J., Ronsivalli, L.J. and Schwartz, M.
food. A (1972) Organoleptic technique predicts refrigeration shelf life
of fish. Food Technol. 26, 65-68
Daud, H.B., McMeekin, T.A. and Olley, J. (1978) Temperature
function integration and the development and ‘metabolism of
poultry spoilage bacteria. Appl. Environ. Microbioi. 36,650-654
Davey, K.R. (1989) A predictive model for combined temperature
and water activity on microbial growth during the growth phase.
J. Appl. Bacterial. 67, 483-488
Davey, K.R. (1991) Applicability of the Davey (linear Arrhenius)
predictive model to the lag phase of microbial growth. J. Appl.
Bacterial. 70, 253-257
Fu, B. and Labuza, T.P. (1992) Considerations for the application of
time-temperature integrators in food distribution. J. Food
Distrib. Res. 23, 9-17
Fu, B. and Labuza, T.P. (1993) Potential use of time-temperature
indicators as an indicator of temperature abuse of MAP products.
In: Principles of Modified Atmosphere and SowVide Product
Packaainn (Eds J. Farber and K. Dodds) Technomic Publishine
Co., Iic.: Lancaster, PA
Fu, B., Taoukis, P.S. and Labuza, T.P. (1991) Predictive micro-
biology for monitoring spoilage of dairy products with time-
temperature integrators. J. Food Sci. 56, 1209-1215
Gacula, M.C. (1975) The design of experiments for shelf life study. J.
Food Sci. 40,399~403
Gacula, MC. and Kubala, J. (1975) Statistical models for shelf life
failures. J. Food Sci. 40, 404-409
Gaudagnl, D.G. (1957) Time-temperature tolerance of frozen foods.
Food Technol. 11, 387-397
Gibson, A.M. and Robe& T.A. (1989) Predicting microbial growth:
development of a mathematical model to predict bacterial growth
responses. Food Aust. 41, 1075-1079
Griffiths, M.W. and Phillips, J.D. (1988) Prediction of the shelf-life
of pasteurized milk at different storage temperatures. J. Appl.
Bacterial. 65, 269-278
a Howgate, P. (1985) The shelf life of fish products. J. Sci. Food Agric.
36, 126-127
Jefferys, W.H. and Berger, J.O. (1992) Ockham’s Razor and
Bayesian analysis. Am. Sci. 80, 64-72
Jorgensen, B.R., Gibson, D.M. and Huss, H.H. (1988) Microbio-
logical quality and shelf life prediction of chilled fish. Int. J. Food
Microbial. 6, 295-307
Kopelman, I.J. and Efroni, D. (1977) Shelf life and microbial growth
kinetics of chilled reconstituted orange juice. Lebensm. Wiss.
Technof. 10, 131-134
Kopebnan, LJ. and Rauchwerger, M. (1984) Shelf life and microbial
growth kinetics of fresh citrus juices: Shamouti orange. J. Food
Proc. Preserv.. 8, 241-250
Laburn, T.P. (1984) Application of chemical kinetics to deterioration
of foods. J. Chem. Educ. 61,348-358
Labuza, T.P. and Schmidl, M.K. (1988) Use of sensory data in the
shelf life testing of foods: principles and graphical methods for
evaluation. Cereal Foods World 33, 193-206
and Labuza, T.P., Fu, B. and Taoukis, P.S. (1992) Prediction for shelf life
and safety of minimally processed CAP/MAP chilled foods. J.
Food Prot. 55, 741-750
Langeveld, L.P.M. and Cuperus, F. (1980) The relation between

temperature and growth rate in pasteurized milk of different types
of bacteria which are important to the deterioration of that milk.
Neth. Milk Dairy J. 34, 106-124
Malcata, F.X. (1990) The effect of internal thermal gradients on the
reliability of surface mounted full-history time-temperature
indicators. J. Food Proc. Preserv. 14, 481-497
Marcy, R.B. and Wallen, S.E. (1983) Heterogeneity of samples as a
problem in shelf life prediction. J. Food Prot. 46, 542-544
McMeekin, T.A., Chandler, R.E., Doe, P.E., Garland, C.D., Olley,
J., Putro, S. and Ratkowsky, D.A. (1987) Model for combined
effect of temperature and salt concentration/water activity on the
growth rate of Staphylococcus xylosus. J. Appl. Bacterial. 62,
543-550
NFPA (National Food Processors Association) (1988) Safety consider-
ations for new generation refrigerated foods. Dairy Food Sanit. 8,
5-7
Ng, H., Ingraham, J.L. and Marr, A.G. (1962) Damage and
derepression in Escherichia coli resulting from growth at low
temperatures. J. Bacterial. 84, 331-339
Nixon, P.A. (1977) Temperature function integrator. U.S. Patent
41,061,033
Owen, D. and Nesbitt, M. (1984) A versatile time temperature
function integrator. Lab. Pratt. 33, 70-75
Ratkowsky, D.A., Olley, J., McMeekin, T.A. and Ball, A. (1982)
Relationship between temperature and growth rate of bacterial
cultures. J. Bacterial. 149, 1-5
Ratkowsky, D.A., Lowry, R.K., McMeekin, T.A., Stokes, A.N. and
Chandler, R.E. (1983) Model for bacterial culture growth rate
throughout the entire biokinetic temperature range. J. Bacterial.
154, 1222-1226
Ronsivalli, L.J. and Charm, S.E. (1975) Spoilage and shelf-life
prediction of refrigerated fish. Marine Fisheries Rev. 37, 32-34
Shelf-life prediction: 8. Fu and T.P. Labuza
Saguy, I. (1992) Simulated growth of Listeria monocytogenes in
refrigerated foods stored at variable temperature. Food Technol.
46, 69-71
Schmidt, K. and Bouma, J. (1992) Estimating shelf-life of cottage
cheese using hazard analysis. J. Dairy Sci. 75. 2922-2927
Shaw, M. (1967) Effect of abrupt temperature shift on the growth of
mesophilic and psychrophilic yeasts. J. Bactediol. 93, 1332-1336
Sherlock, M. and Labuza, T-P. (1992) Consuqer perceptions of
consumer type time-temperature indicators or use on refriger-
ated dairy foods. Dairy Food Envion. Sanit. 4 2, 559-565
Sherlock, M., Fu, B., Taoukis, P.S. and Lab ?a, T.P. (1991) A
systematic evaluation of time-temperature ii dicators for use as
consumer tags. J. Food Prot. 54, 885-889
Simpson, R., Li, K.Y. and Torres, J.A. (1989) A banagement tool to
improve microbial quality of refrigerated foqds. In: Proceeding
of International Conference on Technical Inn vations in Freezing
and Refrigeration of Fruits and Vegetables t niversity of Cali-
fornia, Davis, pp. 171-184
Spencer, R. and Baines, C.R. (1964) The effect of(temperature on the
spoilage of wet white fish. I. Storage at codstant temperatures
between - 1 and 25”. Food Technol. 18, 175c179
Taoukis, P.S., Fu, B. and Labuza, T.P. (1991):Time-temperature
indicators. Food Technol. 45, 70-82
Wittinger, S.A. and Smith, D.E. (1986) Effect’ of sweeteners and
stabilizers on selected sensory attributes add shelf life of ice
cream. J. Food Sci. 51, 1463-1466, 1470
Zwietering, M.H., Jongenburger, I., Romhouts, d.M. and Van’t Riet,
K. (1990) Modeling of the bacterial growth c&e. Appl. Environ.
Microbial. 56, 1875-1881
Zwieterlng, M.H., De Koos, J., Hasenack, B.E4, De Wit, J.C. and
Van’t Riet, K. (1991) Modeling of bacterial rowth as a function
of temperature. Appl. Environ. Microbial. 5,c , 1094-1101
Food Control 1993 Volume’ 4 Number 3 133