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Food Research International 45 (2012) 852–862

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Food Research International

j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / f o o d r e s

Predictive modelling of Salmonella: From cell cycle measurements to e-models

Marina Muñoz-Cuevas, Aline Metris, József Baranyi ⁎
Institute of Food Research, Norwich Research Park, Norwich NR4 7UA, United Kingdom

a r t i c l e i n f o a b s t r a c t

Article history: The quantitative measurements of the growth of Salmonella can be traced back to the 1950s, when the
Received 18 February 2011 Copenhagen School studied its cell cycle. Although predictive food microbiology has only been recognised as a
Accepted 14 April 2011 discipline in its own right since the 1980s, the first predictive models on Salmonella, specifically on its thermal
inactivation, were published in the 1960s. Today this is the foodborne pathogen for which the most D-values can
Keywords:
be found in the literature. Being of concern in meat, growth models were developed mainly in poultry, other
Salmonella
Predictive modelling
meats, egg products and culture media. With the advent of the internet, predictive modelling has become more
Food safety advanced in terms of organising, analysing and visualising large amounts of data, and it has also become easier to
Food microbiology disseminate the resultant predictive software packages. We anticipate that computational developments will
generate further improvements, including complex scenario analysis, probabilistic and dynamic models.
© 2011 Elsevier Ltd. All rights reserved.

1. Introduction not propose a mathematical model to describe these effects, they

Salmonella is a potentially infectious bacterium that initially spread
with the trade of meat and is still a concern for food safety today
(D'Aoust, 2000). In this paper, we review the evolution of predictive
modelling for this foodborne pathogen. Predictive food microbiology
aims at describing mathematically, the effect of environmental
conditions on the bacterial response to the food environment in various
stages of the food chain.
Predictive microbiology began with the quantitative characterisa-
tion of the death rate of Clostridium botulinum for the canning industry
(Bigelow, 1921; Esty & Meyer, 1922). The first published predictive
models of Salmonella also focused on bacterial inactivation in egg
products, chicken meat and other food products (Anellis, Lubas, &
Raymond, 1954; Bayne, Garibaldi, & Lineweaver, 1965; Davidson,
Boothroyd, & Georgala, 1966; Osborne, Straka, & Lineweaver, 1954).
Along with Escherichia coli, Salmonella is commonly used as a model
organism in microbiological investigations (Neidhart et al., 1987)
and was the subject of early quantitative studies. Kjeldgaard, Maaloe,
and Schaechter (1958), members of a group known today as the
Copenhagen School, measured the cell concentration of Salmonella
enterica serovar Typhimurium by viable count and optical density. They
plotted the logarithm of the cell concentration (log CFU/mL) of a
growing culture as a function of time and estimated the maximum
specific growth rate of the cells by fitting a linear model to the
exponential phase of the observed growth curve. They also tested the
effect of the medium composition and temperature on the growth of the
cultures (Schaechter, Maaloe, & Kjeldgaard, 1958). Although they did
⁎ Corresponding author at: Institute of Food Research, Norwich Research Park,
Norwich NR4 7UA, United Kingdom. Tel.: + 44 1603 255 021; fax: + 44 1603 255 288.
E-mail address: jozsef.baranyi@bbsrc.ac.uk (J. Baranyi).
noticed that the shape of the curves remained the same at different
temperatures and that only their time scale changed. These investiga-
tions are similar to the approach used today in predictive microbiology
with two steps called the primary and secondary models. The primary
model aims at finding patterns in the variation of the cell concentration
with time in a constant environment, such as the linearity of the growth
curve on a log scale. The secondary model describes the effect of the
environment on some parameters of the pattern found in the first step.
The most analysed secondary models describe the effect of temperature
on the growth rate, defined as the maximum slope of the curve.
Two reasons contributed to the increase in demand for mathematical
modelling for microbiological safety. The first was some major food
poisoning outbreaks which led to public interest in safe and healthy
foods. Numerous outbreaks of foodborne salmonellosis around the
world were reported during the 1960s and 70s (Harvey, Price, Davis, &
Morley-Davis, 1961; Horwitz, Pollard, Merson, & Martin, 1977; Levy
et al., 1975; Morton & Woolfe, 1963; Vernon, 1969). Consequently, the
U.S. public health authorities, including the U.S. Food and Drug
Administration (Angelotti, 1973) and the U.S. Department of Agriculture
(Anonymous, 1969), issued recommendations for the control of salmo-
nellosis. The second reason was the need to enable users to produce
quick assessments on the safety of specific foods instead of traditional
laboratory methods which were lengthy and expensive. In particular,
increased attention was given to predicting the growth rate of micro-
organisms in specified environments.
With the advancement of predictive modelling and the development
of computing (McMeekin, Olley, Ross, & Ratkowsky, 1993; Roberts &
Jarvis, 1983), more and more detailed models were developed. Linear
growth models did not include the lag phase. Initially, the lag was
modelled by introducing a delay parameter in the primary model. The
transition from lag to the exponential phase was then more accurately

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M. Muñoz-Cuevas et al. / Food Research International 45 (2012) 852–862
described by sigmoid functions, for example logistic, Gompertz
(Zwietering, Jongenburger, Rombouts, & Van't Riet, 1990). These models
also included the stationary phase, in which the cell concentration
reaches its maximum value characteristic of the growth environment.
After these initial steps to mathematical modelling, it became clear
that empirical models were unsatisfactory to characterise the early
phase of growth, especially the lag phase. Furthermore, it was not
straightforward to generalise the used primary models for fluctuating
environments. The model of Baranyi and Roberts (1994), based on a set
of two coupled differential equations, was the first to analyse the effect
of dynamically changing environments on the lag time. The model has
since been implemented in several Salmonella studies (Alvseike,
Nerbrink, Skjerve, & Nesbakken, 2000; Koutsoumanis, Taoukis, Tassou,
& Nychas, 1999; Skandamis, Tsigarida, & Nychas, 2002).
Meanwhile, secondary models were developed to describe the effect
of the temperature on the growth rate, such as the square root model
(McMeekin et al., 1993; Ratkowsky, Olley, McMeekin, & Ball, 1982) or
the Cardinal Temperature Values model of Rosso, Lobry, and Flandrois
(1993). The number of environmental factors taken into account in the
secondary models increased, so the predictions became more accurate
(Koutsoumanis, Tassou, Taoukis, & Nychas, 1998; Membre, Majchrzak, &
Jolly, 1997), though frequently less robust. For multi-factor descriptions,
the Gamma concept of Zwietering, De Wit, and Notermans (1996) or
multivariate response surface models (Gibson, Bratchell, & Roberts,
1988; Oscar, 1999a, 1999b, 1999c) became commonly used.
Historically, the inactivation of microorganisms by heat or other
technologies has been described using first-order kinetics. However,
curves with a shoulder or/and tailing are frequently observed and the
significant deviations from linearity required the development of more
complex models (Cole, Davies, Munro, Holyoak, & Kilsby, 1993; Peleg &
Cole, 1998; Zwietering et al., 1990). Some inactivation models were the
mirror images of growth models (Geeraerd, Valdramidis, & Van Impe,
2005), some were used specifically for inactivation, like that of Weibull
(Bialka, Demirci, & Puri, 2008; Guan, Chen, & Hoover, 2005; Leguerinel,
Spegagne, Couvert, Coroller, & Mafart, 2007; Mattick et al., 2001;
Stasiewicz, Marks, Orta-Ramirez, & Smith, 2008) or log-logistic (Raso,
Alvarez, Condón, & Sala Trepat, 2000). A theoretical study was published
by Baranyi and Pin (2001) on when a survival curve can be modelled by
a mirror image of a growth function, with special attention on the multi-
hit and multi-target models of inactivation (Casolari, 1988).
With the recognition of Salmonella as an important pathogen,
publications on predictive models describing its behaviour in various
foods have increased as shown in Fig. 1. In the mid 1990s, two software
packages, the Pathogen Modelling Program, PMP (Buchanan, 1991) in the
US, and Food MicroModel, (McClure et al., 1994), in the UK, were launched
to support the use of predictive modelling. Currently, growth and
inactivation models are available on websites such as ComBase
Fig. 1. Number of publications on modelling of Salmonella spp in the last 60 years
(source: Web of Knowledge http://wok.mimas.ac.uk/). ( ) Thermal inactivation; ( )
sigmoid growth models; ( ) others: dynamic growth models, lag time models,
probability models and neuron networks models.
853
(www.combase.cc), PMP-Online (pmp.arserrc.gov/PMPOnline.aspx) or
Symprevius (www.symprevius.org).
Due to the demand for minimally processed food, conditions where
only a few cells within a population can grow, and the growth/no
growth boundary in the space of the environmental factors, have
increasingly become the focus of research. These conditions require
modelling by a stochastic process for the primary model (Krieter, 2004;
Latimer, Jaykus, Morales, Cowen, & Crawford-Brown, 2002; Whiting
et al., 2000) and describing the effect of the environment on the
probability of growth for the secondary model (Koutsoumanis, Kendall,
& Sofos, 2004; Lanciotti, Sinigaglia, Gardini, Vannini, & Guerzoni, 2001).
Non-thermal inactivation models are also being developed as new
technologies emerge (Alvarez, Manas, Sala, & Condon, 2003; Erkmen,
2009b; Kim, Rhee, Kim, Lee, & Kim, 2007; Liao, Kong, Zhang, Liao, & Hu,
2010).
In this study, first some inactivation models, then traditional
models of growth, their implementation and their validity region are
reviewed. Finally, anticipated future developments are summarised.
2. Thermal inactivation
The simplest mathematical description of thermal inactivation can
be summarised by the concept of linear inactivation modelling. This
means that both the ‘log cell concentration vs. time’ curve (primary
model) and the ‘log k vs. temperature’ curve (secondary model),
where k denotes the slope of the primary model, are assumed to be
linear. Commonly, D = 1/k, the time for one decimal reduction in cell
concentration, is used to characterise the primary, while the recipro-
cal of the slope of the log(D) vs. temperature curve, the z-value, is
used to characterise the secondary model. Although the assumptions
of linearity for the primary and secondary models are independent
of each other, it is generally the combination of the two, which is
referred to as the linear inactivation model.
Thermal inactivation of pathogens, including Salmonella, has been
studied extensively resulting in a wide range of D- and z-values
(Doyle & Mazzotta, 2000; ICMSF, 1996; Katzin, Sandholzer, & Strong,
1943). Van Asselt and Zwietering (2006) compared the D-values of
foodborne pathogens collected from the literature. They found the
most D-values for Salmonella (1161). The authors generated an overall
model for the relationship between the log D-values and heating
temperatures for different food products and laboratory media:
 €
Log D = logDref − T−Tref = z
where z and Dref are the z- and D-values, respectively, at the heating
temperature T = Tref, arbitrarily fixed to 70 °C for vegetative cells.
They found that, for Salmonella, the linear relationship between log
D and temperature was suitable between 48 and 90 °C and concluded
that the food matrix, except for chocolate, which has a very low water
activity, did not have a significant influence on the D-values.
We fitted the D-values, obtained by linear regression of some
datasets of the ComBase database (www.combase.cc), using the
above equation. A total of 1180 D-values, some of which were also
included in the study of van Asselt and Zwietering (2006), were
plotted against the temperature values at which they were measured.
The results, shown in Fig. 2, were consistent with those reported by
those authors. The effect of food matrix was not significant, except for
meringue analogues which have a very low water activity (0.87). The
z-values were similar: z = 10.7 °C for ComBase data, and 9.1 °C for the
data of van Asselt and Zwietering (2006). This means that, in the
inactivation region, the temperature needs to be increased by 9.1
(or 10.7) °C in order to decrease the time to one decimal reduction
by one log10 unit. The log Dref = − 0.15 log(min) value at 70 °C, as
obtained from the ComBase data, was higher than that obtained by
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854 M. Muñoz-Cuevas et al. / Food Research International 45 (2012) 852–862
4
3
2 history"
log (D, min)
1 Enteritidis PT4 phage
0 analogue
-1
-2
-3
45 55 65 75
Temperature (°C)
Fig. 2. Heat resistance of Salmonella spp. in food and laboratory media. The data were extracted from ComBase (www.comBase.cc) and fitted by a linear secondary model. The results
are compared with the respective regression line of van Asselt and Zwietering (2006).
the authors, which was − 0.83 log(min), but within their 95% confi-
dence interval.
These results indicate that temperature is the most significant
environmental factor to be taken into account in the secondary
models of inactivation. However, the physical and chemical charac-
teristics of food such as low pH, food structure or decreased moisture
content also affect heat resistance. It has often been quoted that the
pH of the heating medium is the main environmental factor that can
reduce the bacterial heat resistance (Blackburn, Curtis, Humpheson,
Billon, & McClure, 1997; Casadei, Ingram, Hitchings, Archer, & Gaze,
2001). Water activity (aw) may also have a significant effect on
bacterial heat resistance, as reported for example in chocolate and
meringue, both of which have low aw (Doyle & Mazzotta, 2000;
ICMSF, 1996). Blackburn et al. (1997) reported that a decrease in
water activity produced by high salt or sugar concentrations increased
the heat resistance of Salmonella.
The D-value can also depend on the specific strain of Salmonella. For
example, Salmonella Enteritidis phage type 4 has been selected as a heat
resistant strain by Humphrey (1990). Salmonella senftenberg 775W
proved to be another strain that is notorious for its heat resistance
(Bayne et al., 1965; Davidson et al., 1966; Ng, Bayne, & Garibaldi, 1969).
However, as Fig. 2 shows, the strain effect is not greater than that of the
food matrix.
The initial physiological state of the culture also has an influence on
the D-value (Sherman & Albus, 1923). Ng et al. (1969) demonstrated
that S. senftenberg 775W was more heat resistant in the stationary phase
than in the exponential phase. Another example is the temperature at
which the bacteria were grown prior to the heat treatment, which also
affects the physiological state of the cells. Mackey and Derrick (1986)
found that sub-lethal heat shocks can build up resistance to the
subsequent heat treatment. However, reports are conflicting. According
to Sherman and Cameron (1934), cells grown at lower temperatures
were more heat resistant. Ng et al. (1969) found higher heat resistance
in cells of S. senftenberg 775W grown at 44 °C than at 15 °C. The D-values
from ComBase data, for which the effect of incubation temperature was
investigated, are shown in Fig. 2, but again the effect was not greater
than that of the food matrix.
Van Asselt and Zwietering (2006) tested, using subsets of their data,
whether including an initial transition period, the shoulder, in the
primary modelling makes the secondary model significantly different.
They found that the effect on the secondary model was negligible.
McKee & Gould (1988) showed that, for physiological reasons, the
linearity of the secondary model is restricted to a limited range of
ComBase data
ComBase data with "temperature
ComBase data of Salmonella
ComBase data in meringue
Regression with ComBase data
(excluding meringue)
95% CL Regression with Combase
data
Regression from van Asselt and
Zwietering, 2006
85 95
temperatures. This deviation from linearity also applies where the
inactivation is weak and stochastic, and may explain the slight deviation
of the data from the 95% confidence limits at the lower temperatures in
Fig. 2.
3. Modelling growth
Until the 1990s, the Gompertz function was the most popular
primary model to describe the variation of concentration of bacteria in a
batch culture with time (Gibson, Bratchell, & Roberts, 1987). It fitted the
data well, was easy to program and the statistical properties of the
estimates were favourable. The Gompertz equation was used to describe
the growth of Salmonella in several media (Bratchell, Gibson, Truman,
Kelly, & Roberts, 1989; Broughall & Brown, 1984; Gibson et al., 1988;
Mackey & Kerridge, 1988; Mackey, Roberts, Mansfield, & Farkas, 1980).
Secondary models describe the dependence of the parameters of the
primary model on specified environmental conditions, for example,
temperature, pH, water activity, atmosphere composition, naturally
occurring organic acids or added preservatives. For multivariate
secondary models, polynomial response surfaces are commonly used,
mainly because they are easy to implement in statistical packages. These
are empirical models and the parameters do not have any biological
meaning. The effects of pH, sodium chloride and storage temperature on
the growth of Salmonella Thompson, S. Stanley and S. Infantis in tryptone
soya broth were modelled with such polynomial equations by Gibson
et al. (1988). Thayer, Muller, Buchanan, and Phillips (1987) used similar
response surface models to describe the growth of S. Typhimurium ATCC
14028 as a function of temperature, pH, NaCl concentration and
atmosphere in chemically defined medium. Other examples of response
surface models for Salmonella spp. were reported by Oscar (1999a,
1999b, 1999c).
Various types of secondary models were developed for the
growth/death of Salmonella spp. in meat (Dickson, Siragusa, & Wray,
1992; Mackey & Kerridge, 1988). Polynomial models were used by
Koutsoumanis, Tassou, et al. (1998) and Oscar (1999a, 1999b, 1999c).
Square root type models (Ratkowsky et al., 1982) were preferred by
Erkmen (2009b), Gumudavelli, Subbuh, Thippareddi, Velugoti, and
Froning (2007), Iturriaga, Tamplin, and Escartin (2007), Juneja et al.
(2007), Juneja, Melendres, Huang, Subbiah, and Thippareddi (2009),
Smith (1985), and Velugoti et al. (in press). Cardinal parameter model
(Rosso et al., 1993) was used by Coroller et al. (2005) and Pinon et al.
(2004); and Arrhenius type models by Davey and Daughtry (1995)
and Erkmen (2009b). Artificial neural networks were also proposed to
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M. Muñoz-Cuevas et al. / Food Research International 45 (2012) 852–862 855

account for the complexities of bacterial growth (Oscar, 2009a; Xiong,
Xie, Edmondson, & Meullenet, 2002).
Data shown in Table 1 summarise the models of Salmonella in the
papers cited in the reference list, classified in different food products,
culture media and mathematical models. Because data generated in a
culture medium are more accurate, therefore more suitable for
modelling than data acquired in a food matrix, more publications can
be found on experiments in culture media than in food. The growth rates
in food are frequently estimated by extrapolation, using the models
generated in culture medium and the bias factor of Ross (1996). Food-
specific models are also commonly developed based on data generated
in the food in question. The most predictive models of Salmonella, based
on data generated in food environments, refer to poultry and other
meats, including beef and pork.
4. Modelling the physiological state of the cells and the effect of
dynamically changing environments
Zwietering et al. (1990) reparameterised the Gompertz equation to
obtain parameters with biological interpretation such as lag time and
maximum specific growth rate. The authors compared the regression
performances of different sigmoid functions (logistic, Gompertz,
Richards, Schnute and Stannard) and concluded that the Gompertz
equation gave the best fit for a large dataset on Lactobacillus plantarum.
A number of authors have used this new reparameterisation to fit
Salmonella growth data measured by different methods: plate counts
(Juneja et al., 2007; Juneja et al., 2009; Oscar, 2007); conductance
(Koutsoumanis, Tassou, et al., 1998); and absorbance measurements
(Park, Seo, & Ha, 2007). Models were generated in specific foods such as
meat (Juneja et al., 2009), egg (Pradhan, Li, Swem, & Mauromoustakos,
2005) and poultry (Juneja et al., 2007; Oscar, 2007; Yang, Wang, Li, &
Johnson, 2002).
Using the Gompertz function to model the variation of the logarithm of
the cell population with time is an empirical approach, regardless of its
parameterisation (Baranyi & Roberts, 1994), and therefore unsuitable for
situations when the environment changes during growth (dynamic
conditions). Besides, it does not include the effect of the subculture
conditions (history effect) on the lag time. Baranyi and Roberts (1994)
proposed a model, which used an adjustment function, α(t) to express the
process of gradual improvement in the physiological state of the bacterial
population after inoculation. The initial physiological state of the cells,
α(0)=α0 is a fraction between 0 and 1, from which α(t) is converging to
1 as the culture approaches the exponential phase. This α0 parameter
reflects the history-effect, similarly to the inoculum level. This model was
applied to numerous studies of Salmonella growth in different food
products. It was used in isothermal conditions for ground pork (Velugoti
et al., in press) and egg products (Gumudavelli et al., 2007; McQuestin,
Musgrove, & Tamplin, 2010). Juneja et al. (2009) compared the per-
formance of this model with that of the Gompertz, the logistic and the
authors' own model. They concluded that, using isothermal data, there
was no major difference between them in terms of goodness of fit. Re-
cently, Fernandez-Saiz, Soler, Lagaron, and Ocio (2010) used the model of
Baranyi and Roberts (1994) to describe the antimicrobial effectiveness of
chitosonium acetate films on the growth of Salmonella spp in a fish soup.
Fluctuating conditions were studied by Van Impe, Nicolai, Martens,
Baerdemaeker, and Vandewalle (1992), Hills and Mackey (1995), Hills
and Wright (1994), Baranyi, Robinson, Kaloti, and Mackey (1995),
Baranyi et al. (1996) and McKellar (2001). Bovill et al. (2000) and Bovill,
Bew, and Baranyi (2001) applied the model of Baranyi and Roberts
(1994) to dynamic temperature profiles, when growing Salmonella in
milk and meat products. Other dynamic approaches for the growth of
Salmonella have been described by Dickson et al. (1992), who applied
their model during cooling. Gumudavelli et al. (2007) validated a
dynamic model under various temperature profiles for Salmonella

Table 1
Classification of published articles of Salmonella spp. according to the mathematical model and the food product used.

Product Mathematical models (referencesa)

Inactivation Growth Othersb

Culture medium 23 14 10
a
(1,2,6,7,16,20,24,25,26,27,31,34,35,51,53,57,60,63,69,71,72,79,92) (8,29,30,40,41,52,55,58,64,66,81,89,94,99) (11,12,15,18,59,61,74,75,76,100)
Egg and egg products 8 5 1
(3,4,5,9,10,70,80,103) (62,73,78,91,104) (33)
Poultry 6 11 2
(13,45,49,50,87,97) (17,23,38,46,82,83,84,85,88,90,106) (19,86)
Other meat 6 12 1
(39,42,43,47,48,49) (8,17,22,36,40,44,66,67,68,95,96,107) (102)
Milk and milk products 2 2 1
(21,32) (98,101) (19)
Others 6 2 1
(14,54,56,65,77,93) (37,28) (105)
a
1. (Aljarallah & Adams, 2007); 2. (Alvarez et al., 2003); 3. (Alvarez, Niemira, Fan, & Sommers, 2006); 4. (Alvarez, Niemira, Fan, & Sommers, 2007a); 5. (Alvarez, Niemira, Fan, &
Sommers, 2007b); 6. (Alvarez-Ordonez, Fernandez, Lopez, & Bernardo, 2009); 7. (Alvarez-Ordonez, Fernandez, Lopez, Arenas, & Bernardo, 2008); 8. (Alvseike et al., 2000) 9. (Amiali,
Ngadi, Smith, & Raghavan, 2007); 10. (Anellis et al., 1954); 11. (Basti & Razavilar, 2004); 12. (Basti, Misaghi, & Khaschabi, 2007); 13. (Bayne et al., 1965); 14. (Bialka & Demirci, 2008);
15. (Bidlas, Du, & Lambert, 2008); 16. (Blackburn et al., 1997); 17. (Borneman, Ingham, & Ane, 2009); 18. (Bovill et al., 2001); 19. (Bovill et al., 2000); 20. (Casadei et al., 2001); 21.
(Dega, Amundson, & Goepfert, 1972); 22. (Dickson et al., 1992); 23. (Dominguez & Schaffner, 2008); 24. (Erkmen, 2000); 25. (Erkmen, 2009a); 26. (Erkmen, 2009b); 27. (Erkmen &
Karaman, 2001); 28. (Fernandez-Saiz et al., 2010); 29. (Gabriel & Nakano, 2010); 30. (Gibson et al., 1988) ;31. (Greenacre, Brocklehurst, Waspe, Wilson, & Wilson, 2003); 32. (Guan
et al., 2005); 33. (Gumudavelli et al., 2007); 34. (Humphrey, 1990); 35. (Humphrey, Slater, Mcalpine, Rowbury, & Gilbert, 1995); 36. (Ingham et al., 2009); 37. (Iturriaga et al., 2007);
38. (Jimenez, Caliusco, Tiburzi, Salsi, & Pirovani, 2007); 39. (Juneja, 2003); 40. (Juneja, Marks, & Huang, 2003); 41. (Juneja & Marks, 2006); 42. (Juneja & Eblen, 2000); 43. (Juneja,
2004); 44. (Juneja et al., 2009); 45. (Juneja, Eblen, & Marks, 2001); 46. (Juneja et al., 2007); 47. (Juneja, Marks, & Mohr, 2003); 48. (Juneja, Hwang, & Friedman, 2010); 49. (Juneja,
Eblen, & Ransom, 2001); 50. (Juneja, 2007); 51. (Kim et al., 2007); 52. (Kobilinsky, Nazer, & Dubois-Brissonnet, 2007); 53. (Korolczuk et al., 2006); 54. (Koutsoumanis,
Lambropoulou, & Nychas, 1999); 55. (Koutsoumanis, Lambropoulou, et al., 1999); 56. (Koutsoumanis, Lampropoulou, Taoukis, & Nychas, 1998); 57. (Koutsoumanis, Tassou et al.,
1998); 58. (Koutsoumanis, Taoukis, et al., 1999); 59. (Koutsoumanis et al., 2004); 60. (Koutsoumanis & Sofos, 2004); 61. (Lanciotti et al., 2001); 62. (Latimer et al., 2002); 63.
(Leguerinel et al., 2007); 64. (Lianou & Koutsoumanis, in press); 65. (Liao et al., 2010); 66. (Mackey & Derrick, 1984); 67. (Mackey & Kerridge, 1988); 68. (Mackey et al., 1980); 69.
(Manas et al., 2001); 70. (Manas, Pagan, Alvarez, & Uson, 2003); 71. (Mattick, Jorgensen, Legan, Lappin-Scott, & Humphrey, 2000); 72. (Mattick et al., 2001); 73. (McQuestin et al.,
2010); 74. (Mellefont, McMeekin, & Ross, 2003); 75. (Mellefont, McMeekin, & Ross, 2004); 76. (Mellefont, McMeekin, & Ross, 2005); 77. (Membre et al., 1997); 78. (Musgrove,
McQuestin, Tamplin, & Kelley, 2009); 79. (Ng et al., 1969); 80. (Osborne et al., 1954); 81. (Oscar, 1999a); 82. (Oscar, 1999b); 83. (Oscar, 1999c); 84. (Oscar, 2002); 85. (Oscar, 2007);
86. (Oscar, 2009a); 87. (Oscar & Singh, 2009); 88. (Oscar, 2009b); 89. (Park et al., 2007); 90. (Payne, Osborne, Jenkins, & Sheldon, 2007); 91. (Pradhan et al., 2005); 92. (Raso et al.,
2000); 93. (Sampedro, Rodrigo, & Martinez, 2011); 94. (Schaechter et al., 1958); 95. (Skandamis et al., 2002); 96. (Smith, 1985); 97. (Stasiewicz et al., 2008); 98. (Tamagnini, de
Sousa, Gonzalez, Revelli, & Budde, 2005); 99. (Thayer et al., 1987); 100. (Theys et al., 2010); 101. (Theys, Geeraerd, & Van Impe, 2009); 102. (Velugoti et al., in press); 103. (Verde,
Tenreiro, & Botelho, 2004); 104. (Whiting et al., 2000); 105. (Xiong et al., 2002); 106. (Yang et al., 2002); 107. (Yoon, Geornaras, Kendall, & Sofos, 2009).
b
Dynamic growth models, lag time models, probability models and neuron network models.
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856 M. Muñoz-Cuevas et al. / Food Research International 45 (2012) 852–862
Enteritidis growing in egg yolk while Velugoti et al. (in press) used their
model to estimate the growth of Salmonella spp in ground pork.
Whilst the maximum specific growth rate is commonly modelled
as a function of environmental conditions, models describing the lag
time received attention only recently. The lag time depends not only
on factors like the composition of the medium and environmental
factors such as the temperature, but also on the pre-culture conditions
of cells before inoculation, reflected by the initial physiological state of
the cells, which was summarised by a single parameter, α0, in the
model of Baranyi and Roberts (1994). Two approaches have been used
for lag time modelling: either the lag and growth rate are modelled
independently or the lag time is considered to be correlated with the
growth rate. The secondary models described above were used mainly
with the first approach. Zwietering, De Koos, Hasenack, De Wit, and
Van't Riet (1991) selected a hyperbolic equation as the best model to
describe the dependence of lag time on temperature. Oscar (2002)
compared this approach with the Arrhenius model (Daughtry, Davey,
& King, 1997; Davey, 1989, 1991) and the inverse square root model of
Ratkowsky (Duh & Schaffner, 1993; Wijtzes, De Wit, Huis In't Veld,
Van't Riet, & Zwietering, 1995) to predict the lag time as a function of
temperature and concluded that the hyperbola fitted best.
For the second approach, Baranyi and Roberts (1994) considered the
α0 initial physiological state to be constant, independently of the growth
temperature, assuming that the history of the cultures was the same.
Mellefont and Ross (2003) defined the relative lag time (RLT), the ratio
between the lag and the generation time. Since -ln(α0) is the product of
the specific rate and the lag time, the assumption that the initial
physiological state is constant is equivalent to the one that RLT is
constant. Mellefont and Ross (2003) pointed out that this holds only
for a small interval of the growth temperature range. In ComBase
(www.combase.cc), a default lag time is predicted by assuming a
constant initial physiological state based on data generated from
standardised subculture procedures. To facilitate the comparison of
data in food with predictions in broth, the predictions can be superposed
to the growth curve and the lag time adjusted in the prediction by
modifying the value of α0.
Fig. 3A shows an example set of query criteria that can be sub-
mitted to ComBase by its user interface (http://browser.combase.cc/
BrowserHome/SearchOptions/Search.aspx). For the bacterial environ-
ment, the users can select either culture medium or a range of food
categories. They can also select microorganisms and environmental
conditions (temperature, pH, water activity and other, secondary
conditions, like atmosphere, preservatives, etc). Fig. 3B is a display of
available growth and survival curves of the wanted microorganisms
measured in the given media/food and in the selected range of environ-
mental conditions. Fig. 3C shows the prediction given by ComBase
Predictor (http://modelling.combase.cc/ComBase_Predictor.aspx), su-
perposed on a particular response curve stored in ComBase, that satisfies
the query.
Recently, growth/no growth models for Salmonella as a function of
water activity, pH, temperature, ethanol concentration, potassium
sorbate, have been proposed by some authors (Basti & Razavilar,
2004; Koutsoumanis et al., 2004; Lanciotti et al., 2001; Theys,
Geeraerd, Devlieghere, & Van Impe, 2010). Koseki and Yamamoto
(2007) combined growth/no growth data and kinetics data for
secondary modelling. Though the interest in the application of
probabilistic models is strong, they are somewhat less developed
than the kinetic models because they demand more data but are less
accurate. This is a consequence of the fact that probabilistic models
are most important near the boundary of growth, where the interest is
stronger but data generation is less consistent.
5. Computational implementation and interpolation region
By the 1990s, the potential of predictive microbiology had attracted
considerable research interest and the usefulness of the approach
became widely accepted. Recognising the advantages of applying these
techniques in the food industry, the Ministry of Agriculture Fisheries and
Food (MAFF) in the U.K. initiated a coordinated programme to collect
data on the growth and death of bacterial pathogens, which resulted in
the development of a predictive microbiology software package Food
MicroModel. It included models on growth, survival and thermal death
of the major foodborne pathogens and a food spoilage organism, based
on data generated by several partner laboratories (McClure et al., 1994).
The primary model used to fit the growth curves was that of Gompertz,
as described by Gibson et al. (1988). Linear kinetics were used to fit
thermal inactivation data (Peck, Fairbairn, & Lund, 1993), although the
log-logistic approach of Cole et al. (1993) was also used when the
deviation from linearity was too strong. In most cases, multivariate
polynomials were used as secondary models to describe the kinetic
parameters of the primary model as a function of environmental factors
such as temperature, pH, and water activity (McClure et al., 1994).
At the same time, the Agriculture Research Service of the United
States Department of Agriculture (USDA-ARS) funded a similar
project in the U.S. and a predictive microbiology software tool called
the Pathogen Modelling Program (PMP) was launched. PMP and Food
MicroModel were based on the same principles. Food MicroModel
was developed on a larger dataset, but operated on a yearly
subscription basis, while PMP was free of charge. Since 2000, the
Internet has become the most popular platform for the implementa-
tion of predictive models. The term “e-model” introduced in this
paper refers to predictive software tools accessed via the internet. Not
only it is an efficient dissemination tool but, with the aid of servers
with sufficient capacity, both the predictive models and the large
datasets, on which the model were generated, can be integrated in a
single package.
When using predictive software tools, it is vital to know the range
of environmental factors in which the predictions are valid. Table 2
shows the minimum and maximum values of those environmental
factors, inside which the Salmonella growth curves of Gibson et al.
(1988) were generated. They define a brick in the 3D space of the
environmental factors. This brick, A, is inside the brick defined by the
minimum and maximum values of temperature, pH and water activity
(Brick B), where Salmonella is able to grow at all. Brick A is bigger than
the model validity region, since the organism can grow, for example,
at low water activity only if the other two factors are close to their
optimum level.
Fig. 4 illustrates this at low temperature and low water activity
conditions for different pH values. The diamonds indicate those
environmental factor combinations in the 3D space where growth
curves were generated. These growth curves are part of a set of exper-
iments (Gibson et al., 1988) that provide the basis of the predictions in
culture medium, both in PMP (http://ars.usda.gov/Services/docs.htm?
docid=6788) and ComBase Predictor (http://modelling.combase.cc/
ComBase_Predictor.aspx). The conditions where growth was observed
define a convex hull (see for example SAS (1990) for a definition), inside
which a prediction is interpolation; outside it is extrapolation (Baranyi
et al., 1996; Le Marc, Pin, & Baranyi, 2005). In the first inset, two
interpolated predictions from ComBase Predictor and PMP, respectively,
are provided for temperature 10 °C, water activity 0.974 (corresponding
to 4.5% NaCl) and pH 6. They are compared with an observed growth
curve represented by the key B301_71 in the ComBase database. The
reason why the two predictions are not the same is the difference in the
primary model used and in the method of modelling the lag phase. In the
second inset plot, similar predictions for the same values of temperature
and water activity, but at pH 5.6, are given. These two predictions are
extrapolation. The pH value 5.6 is far from the minimum pH for growth,
but here all three environmental factors are limiting. The record with
key B419_47 in the ComBase database shows that, at the same
temperature and water activity values, Salmonella does not grow at
pH 5.4. Therefore, the prediction at pH 5.6 is very uncertain. Close to the
growth/no growth boundary, it is desirable to introduce the probability
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M. Muñoz-Cuevas et al. / Food Research International 45 (2012) 852–862 857

Fig. 3. Browsing ComBase for data on Salmonella and comparing the result with model predictions (www.combase.cc). A. Query by food type, organism and environmental factors
such as temperature, pH and water activity ranges. B. One record represents a growth or inactivation curve. This example shows the growth of Salmonella in chicken at 22 °C. C. The
growth curve in chicken is compared with predictions, with and without typical lag, based on data generated in culture medium.
 Author's personal copy
858 M. Muñoz-Cuevas et al. / Food Research International 45 (2012) 852–862
Table 2
A. Model domain, defined by the intervals of environmental factors where the growth
of Salmonella can be predicted, based on the data of Gibson et al. (1988). B. Growth
domain, defined by the intervals where Salmonella can grow (ICMSF, 1996).
Temperature (°C) pH Water activity
Model domain Minimum 7 3.9 0.97
(A) Maximum 30 7.4 1 would be assigned to any particular growth parameter, such as
Growth domain Minimum 5 3.8 0.94
(B) Maximum 46 9.5 1
of growth as another primary model and describe it as a function of the
environmental factors as another secondary model. Such probabilistic
considerations become increasingly important in risk assessment.
Note that even in one dimension (for example temperature), the
growth/no growth boundary can present difficulties. Current models
can be used with confidence at growth temperatures or at inactiva-
tion temperatures, but in between the bacterial response is highly
unpredictable.
6. Future trends
The following caveats in predictive microbiology need to be
addressed and might constitute the subject of future research.
1. In practical situations, the physiological state of a cell cannot be
known a priori because it depends on the stresses the cell has
endured. Therefore, the user needs to make assumptions and try
different hypotheses. Persistence and recovery models need to be
expanded (McMeekin et al., 2008). In particular, models to predict
the time required for cells to repair damage due to stress (Metris,
George, Mackey, & Baranyi, 2008) and the mechanisms by which cells
recover, is a current topic of investigation in our research group.
2. Apart from some factors like temperature, it is not easy to quantify
the physico-chemical properties of the environment around the cells,
such as the food structure. Also as the cells grow they may change the
environment by producing, for example, organic acids which lower
the pH. As a consequence, interactions between spoilage and
Fig. 4. Conditions (diamond), where growth curves were observed and used to
generate predictions, define a convex hull in the space of the environmental factors.
The inset assigned to the diamond at 10 °C, water activity 0.974 and pH 6 shows the
respective observed growth curve with key B301_71 from ComBase. It is superposed by
two predicted sigmoid curves, produced by ComBase Predictor and PMP, respectively.
Predictions can also be obtained at the same temperature and water activity but pH 5.6
(triangle, second inset), for which no observation is available; the prediction is
extrapolation. According to the ComBase record with key B419_47 (circle), Salmonella
does not grow at the same temperature and water activity, but pH 5.4. Therefore, the
prediction at pH 5.6 has high uncertainty and, without probabilistic modelling, could be
misleading.
pathogenic bacteria are time-dependent, and only a system of linked
differential equations can model such a scenario.
3. At the boundary of growth/no growth, there is some uncertainty
inherent to the biological response of the organism. We propose to
express this uncertainty using conditional growth models. In
statistical terms this means that a conditional probability distribution
growth rate or time to reach a certain bacterial concentration. At a
given time point, the probability that the bacterial concentration is
above a certain level should be calculated as the product of the
probability that the organism grows and the probability that its
concentration is above the critical level, assuming that it grows. This
concept integrates the probabilistic and the kinetic models of
predictive microbiology, having significance mainly in risk assess-
ment. A simple example can be followed as below:
Using ComBase Predictor (http://modelling.combase.cc/ComBase_
Predictor.aspx) one can extrapolate that Salmonella could grow one
log10 unit in a day, in rich medium, at temperature 30 °C, pH 5.5 and
6.5% NaCl. This is an extrapolation indeed, because no data are
available above 4.5% NaCl. According to Koutsoumanis (2008), at
this combination of environmental factors, the probability of growth
for a single cell is between 0.1 and 0.5. With p = 0.3, and omitting the
lag (for the sake of demonstration), the chance that a single cell
generated subpopulation reaches more than one log10 increase in a
day is 0.5p = 0.15. The situation is complicated further if the lag
time distribution of the single cells (Baranyi, 1998) is also taken into
account.
4. Traditional predictive models describe the growth of the population
from large inocula. However, foods are likely to be contaminated by
low numbers of pathogenic bacteria and the cell to cell variability
may become significant. Studies of the behaviour of single cells have
been carried out during or after stress (Francois et al., 2006; Guillier
& Augustin, 2006; Metris et al., 2008). As mentioned in the previous
point, the stochastic nature of the kinetics of single cells presents a
complex problem to risk assessors.
5. A major advancement could be made by creating software tools that
would use probabilistic modelling approaches integrated in a risk
assessment framework. The core of such a tool would be a software
engine integrating databases and mathematical models. The most
important computational means would be Monte-Carlo simulations.
It is often forgotten that the decisive element of these simulations are
the underlying probability distributions. Development and valida-
tion of these probability distributions is as important as for kinetic
models. Unfortunately two major properties of probabilistic model-
ling work against each other: it demands a large amount of data and
it has significance near the boundaries of growth. This is the region
where the lest experimental data are available because it is difficult
to evaluate whether the negative outcome is due to experimental
error or biological stochasticity. However, automated electronic data
recording and pooling common databases can help this. An example
for such an initiative is the Microbial Response Viewer (Koseki,
2009).
To conclude, we suggest that combining computational and
mathematical modelling tools, primarily Internet-based tools, will
enhance the potential of predictive modelling and can address the
above caveats. In those regions of environmental factors where growth
or inactivation of cells is uncertain, probabilistic models will be
necessary; especially if the increasing demand for more accurate risk
assessments is considered. Because analyses need large numbers of
observations, the data must be recorded in systematically formatted
databases; e-models are the ideal platform to do so. Salmonella is likely
to remain a major pathogen, a primary target for which the developed
predictive tools should be used.
 Author's personal copy
M. Muñoz-Cuevas et al. / Food Research International 45 (2012) 852–862
Acknowledgements
Marina Munoz-Cuevas was supported by Marie Curie Actions
(Intra-European Fellowships, LAGSAL grant under FP7). A. Metris and
J. Baranyi were funded by the Biological and Biotechnological
Research Council. We acknowledge S. George for her help with the
manuscript.
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