A modified Weibull model for describing the survival of Campylobacter jejuni in
minced chicken meat
Manuel González
a,
⁎, Panagiotis N. Skandamis
b
, Marja-Liisa Hänninen
a
a
University of Helsinki, Department of Food and Environmental Hygiene, Agnes Sjöberg katu 2, 00014 Helsinki, Finland
b
Agricultural University of Athens, Laboratory of Food Quality Control and Hygiene, Department of Food Science and Technology, Iera Odos 75, 11855 Athens, Greece
abstract article info
Article history:
Received 13 May 2009
Received in revised form 15 September 2009
Accepted 22 September 2009
Keywords:
Campylobacter jejuni
Chicken meat
Modelling
Linear model
Weibull model
Campylobacter is one of the leading causes of foodborne bacterial enteritis. Since chicken meat may be an
important source of C. jejuni, the aims of this study were (i) to evaluate the survival/inactivation of C. jejuni
strain 49/7R and its antimicrobial resistant variants (49/7RAT and 49/7RATCIP32) in minced chicken meat
during extended storage at temperatures ranging from -20 °C to 25 °C and (ii) to test the suitability of the
Weibull model for predicting the inactivation of C. jejuni in minced chicken meat in a wide range of
temperatures. Minced chicken meat samples were inoculated with C. jejuni and log CFU/g were counted after
different storage times at -20 °C, -5 °C, 4 °C, 15 °C or 25 °C. The log-linear and the Weibull models were
used to fit a total of 15 inactivation curves. The mean value of R
2
adjusted
for the correlation between the
surviving bacterial cells observed and predicted by the Weibull model ranged from 0.986 to 0.994, and from
0.895 to 0.925 for the log-linear model, indicating closer agreement between the data and the Weibull model
than for the log-linear one. From the Weibull model, p and δ parameters were described in a secondary
model as a function of temperature using third-order polynomial fitting curves. Information from the
secondary model served to predict survival curves for C. jejuni in minced chicken meat for an independent
set of storage temperatures. Additionally, since δ parameter of the Weibull model is related to the D concept
it served to determine the time (days) needed for the 1-log reduction of CFU/g; within the above mentioned
temperature range. The results revealed that antimicrobial resistant variants survived longer than did the
parent strains at all temperatures studied, indicated by the 1-log reduction time estimates.
© 2009 Elsevier B.V. All rights reserved.
1. Introduction
Campylobacter jejuni is a zoonotic enteric pathogen causing human
gastroenteritis. It has reservoirs in a wide variety of animal species,
including domestic animals. Adding to the human and economic costs
are the chronic sequelae associated with C. jejuni infection; Guillian-
Barré syndrome and reactive arthritis (Nachamkin et al., 1998;
Altekruse et al., 1999; Birk et al., 2004). The illness is transmitted
primarily through foods of animal origin. C. jejuni grows between 30 °C
and 45 °C with an optimal range of 42 °C to 45 °C, and a pH range of 5.8
to 8.0 (Kelana and Griffiths, 2003). The approximate body temperature
of the chicken (from 41 °C to 42 °C), and the environment of the chicken
gut contribute to making the chicken an optimum host for C. jejuni
(Nachamkin, 1995). The role of C. jejuni as a foodborne pathogen is
associated with its ability to survive in food during storage and handling.
Temperature is a key factor in the survival of C. jejuni. Nevertheless, its
survival ability in foods represents a human health risk due to the low
infectious dose (Lori et al., 2007).
C. jejuni survived longer at 4 °C than at room temperature in the
different media tested (Mihaljevic et al., 2007). Studies with chicken
meat have revealed that the colony-forming units (CFUs) of C. jejuni
decrease in ground chicken meat and on chicken skin during
refrigerated storage at 4 °C during one week by 0.81-log CFU/g and
during frozen storage at -20 °C from 0.57 to 1.57-log CFU/g in two
weeks (Bhaduri and Cottrell, 2004). Other groups obtained similar
results as well (Anonymous, 1996; Birk et al., 2006). Recently, Ritz
et al. (2007) studied the development of predictive models for the
survival of C. jejuni at -20 °C in chicken meat and concluded that
CFUs from different time points varied depending on the medium
they used for counting the cells, thereby, making the development of
survival models difficult.
The objectives of the present study were to model the survival of C.
jejuni wild-type 49/7R and its antimicrobial resistant variants 49/
7RAT and 49/7RATCIP32 at temperatures from -20 °C to 25 °C using
the logarithmic form of the Weibull model and establish secondary
model of inactivation kinetic parameters response to temperature. In
addition, predicted inactivation curves from the established model
were compared to literature dataset to assess the performance of the
International Journal of Food Microbiology 136 (2009) 52–58
⁎ Corresponding author. Department of Food and Environmental Hygiene, University
of Helsinki, P.O. Box 66 (Agnes Sjöbergin katu 2), 00014 Helsinki, Finland. Tel:+358 9
191 57559; fax: +358 9 191 57101.
E-mail address: manuel.gonzalez@helsinki.fi (M. González).
0168-1605/$ – see front matter © 2009 Elsevier B.V. All rights reserved.
doi:10.1016/j.ijfoodmicro.2009.09.022
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