A stochastic approach for integrating strain variability in modeling Salmonella
enterica growth as a function of pH and water activity
Alexandra Lianou, Konstantinos P. Koutsoumanis ⁎
Laboratory of Food Microbiology and Hygiene, Department of Food Science and Technology, School of Agriculture, Aristotle University of Thessaloniki, Thessaloniki 54124, Greece
abstract article info
Article history:
Received 16 February 2011
Received in revised form 8 June 2011
Accepted 3 July 2011
Available online 13 July 2011
Keywords:
Salmonella enterica
Strain variability
Stochastic growth model
Strain variability of the growth behavior of foodborne pathogens has been acknowledged as an important
issue in food safety management. A stochastic model providing predictions of the maximum specific growth
rate (μ
max
) of Salmonella enterica as a function of pH and water activity (a
w
) and integrating intra-species
variability data was developed. For this purpose, growth kinetic data of 60 S. enterica isolates, generated
during monitoring of growth in tryptone soy broth of different pH (4.0–7.0) and a
w
(0.964–0.992) values,
were used. The effects of the environmental parameters on μ
max
were modeled for each tested S. enterica
strain using cardinal type and gamma concept models for pH and a
w
, respectively. A multiplicative without
interaction-type model, combining the models for pH and a
w
, was used to describe the combined effect of
these two environmental parameters on μ
max
. The strain variability of the growth behavior of S. enterica was
incorporated in the modeling procedure by using the cumulative probability distributions of the values of
pH
min
, pH
opt
and a
wmin
as inputs to the growth model. The cumulative probability distribution of the observed
μ
max
values corresponding to growth at pH 7.0–a
w
0.992 was introduced in the place of the model's parameter
μ
opt
. The introduction of the above distributions into the growth model resulted, using Monte Carlo simulation,
in a stochastic model with its predictions being distributions of μ
max
values characterizing the strain variability.
The developed model was further validated using independent growth kinetic data (μ
max
values) generated for
the 60 strains of the pathogen at pH 5.0–a
w
0.977, and exhibited a satisfactory performance. The mean, standard
deviation, and the 5th and 95th percentiles of the predicted μ
max
distribution were 0.83, 0.08, and 0.69 and
0.96 h
-1
, respectively, while the corresponding values of the observed distribution were 0.73, 0.09, and 0.61 and
0.85 h
-1
. The stochastic modeling approach developed in this study can be useful in describing and integrating
the strain variability of S. enterica growth kinetic behavior in quantitative microbiology and microbial risk
assessment.
© 2011 Elsevier B.V. All rights reserved.
1. Introduction
Quantitative microbiology, employing mathematical models that
predict microbial behavior (growth or survival/inactivation), allows
for the evaluation of microbial food-related risks, with the latter being
critical for the development and implementation of effective
mitigation strategies (Nauta, 2002). Due to the high level of variation
characterizing microbial dynamics, the value of deterministic models
(i.e., models that provide point estimates of microbial concentrations)
in food safety management has been questioned (Nicolaï and Van
Impe, 1996; Poschet et al., 2003). The information provided by
deterministic models is often insufficient with regard to advanced
quantitative microbiology applications, such as hazard analysis and
critical control points (HACCP) and risk analysis projects (Poschet et
al., 2003). Such a deficiency highlighted the need for the development
of models capable of incorporating the variation of model parameters,
and motivated the commencement of the so-called “stochastic
predictive microbiology” (Nicolaï and Van Impe, 1996). Stochastic
(or probabilistic) models take into account the variation of various
factors affecting microbial behavior by using probability distributions
of the input data, and provide predictions in the form of probability
density functions instead of point estimates (Koutsoumanis et al.,
2010; Poschet et al., 2003).
Accounting for the variation characterizing microbial growth,
stochastic predictive models are expected to be more efficient than
other traditional modeling approaches, by allowing for a balanced
relationship between food safety management and cost-effectiveness
of employed processes (Couvert et al., 2010; Juneja et al., 2003).
Several stochastic predictive modeling approaches, aiming at quan-
tifying and integrating different variation sources, have been
described the last decade (Augustin et al., 2011; Delignette-Muller
et al., 2006; Membré et al., 2005). The approaches embraced in the
above and other studies account for variation on empirical data and/or
model parameters, and are pertinent to various issues of food safety
International Journal of Food Microbiology 149 (2011) 254–261
⁎ Corresponding author. Tel./fax: + 30 2310991647.
E-mail address: kkoutsou@agro.auth.gr (K.P. Koutsoumanis).
0168-1605/$ – see front matter © 2011 Elsevier B.V. All rights reserved.
doi:10.1016/j.ijfoodmicro.2011.07.001
Contents lists available at ScienceDirect
International Journal of Food Microbiology
journal homepage: www.elsevier.com/locate/ijfoodmicro