0 Up votes0 Down votes

0 views15 pagescinetica de crecimiento-muerte demicroorganismos

Jun 19, 2019

© © All Rights Reserved

PDF, TXT or read online from Scribd

cinetica de crecimiento-muerte demicroorganismos

© All Rights Reserved

0 views

cinetica de crecimiento-muerte demicroorganismos

© All Rights Reserved

- Linear Regression
- knowledge claims and knowledge questions
- Baltagi-Econometrics
- Refresher2 Math
- THE BOUNDARY VALUE PROBLEM FOR SECOND ORDER ORDINARY LINEAR DIFFERENTIAL EQUATION WITH VARIABLE COEFFICIENT
- Velocity analysis using nonhyperbolic moveout
- A MatlabSimulink Toolbox for Inversion of Local Linear Model Trees.pdf
- lecture1.pdf
- Carascteristici ale catalizei drojdiei de bere
- Industrial Project Management
- Autonomous Calibration of Robots Using Planar Points
- Pamphlet Biotech
- UT Dallas Syllabus for math2420.501.10f taught by Zalman Balanov (zxb105020)
- Hominids Adapted to Metabolize Ethanol Long Before Human Directed Fermentation 2014
- 09 - ODE - 01 - Ordinary Difference Equation
- equations in enzyme kinetics
- 20131217 PSC Item XX Standard Component Dynamic List
- CIV340 Mock Exam
- Complex Reactions (1)
- 399-419

You are on page 1of 15

www.elsevier.com/locate/ijfoodmicro

microorganism growth–death kinetics in foods

E.W. Ross, I.A. Taub, C.J. Doona*, F.E. Feeherry, K. Kustin

US Army RDECOM, Natick Soldier Center, Combat Feeding Directorate, Combat Feeding Innovative Science Team, Kansas St.,

Natick, MA 01760-5018, USA

Received 16 March 2004; received in revised form 5 July 2004; accepted 26 July 2004

Abstract

Knowledge of the mathematical properties of the quasi-chemical model [Taub, Feeherry, Ross, Kustin, Doona, 2003. A

quasi-chemical kinetics model for the growth and death of Staphylococcus aureus in intermediate moisture bread. J. Food Sci.

68 (8), 2530–2537], which is used to characterize and predict microbial growth–death kinetics in foods, is important for its

applications in predictive microbiology. The model consists of a system of four ordinary differential equations (ODEs), which

govern the temporal dependence of the bacterial life cycle (the lag, exponential growth, stationary, and death phases,

respectively). The ODE system derives from a hypothetical four-step reaction scheme that postulates the activity of a critical

intermediate as an antagonist to growth (perhaps through a quorum sensing biomechanism). The general behavior of the

solutions to the ODEs is illustrated by several examples. In instances when explicit mathematical solutions to these ODEs are

not obtainable, mathematical approximations are used to find solutions that are helpful in evaluating growth in the early stages

and again near the end of the process. Useful solutions for the ODE system are also obtained in the case where the rate of

antagonist formation is small. The examples and the approximate solutions provide guidance in the parameter estimation that

must be done when fitting the model to data. The general behavior of the solutions is illustrated by examples, and the MATLAB

programs with worked examples are included in the appendices for use by predictive microbiologists for data collected

independently.

D 2004 Elsevier B.V. All rights reserved.

Keywords: Predictive food microbiology; Quasi-chemical model; Chemical kinetics; Differential equation system; Staphylococcus aureus;

Escherichia coli; Hurdles; High pressure processing

1. Introduction

* Corresponding author. Tel.: +1 508 233 5083; fax: +1 508

233 5200. death kinetics (Taub et al., 2003) is a unique

E-mail address: christopher.doona@natick.army.mil mathematical tool for predicting microbial kinetics

(C.J. Doona). in food substrates. The model was developed in

0168-1605/$ - see front matter D 2004 Elsevier B.V. All rights reserved.

doi:10.1016/j.ijfoodmicro.2004.07.019

158 E.W. Ross et al. / International Journal of Food Microbiology 99 (2005) 157–171

concert with the study of the growth kinetics of a models based on chemical reaction mechanisms, and

cocktail of Staphylococcus aureus strains in inter- this approach has been used effectively in under-

mediate moisture (IM) military bread (Feeherry et al., standing nonlinear chemical dynamics such as oscil-

2003) with variations in water activity (a w, as adjusted lating chemical reactions (Epstein and Pojman, 1998).

by desorptive and absorptive techniques), pH, and The chemically triggered alternation between inde-

temperature (T). In the latter study, both the logistic pendently living cells and cooperative aggregates of

equation and Gompertz equation successfully fit the the cellular slime mold Dictyostelium discoideum was

growth kinetics data and generated accurate estimates successfully modeled by introducing the chemical

for the lag time (k), maximum growth rate (l), and kinetics concept of autocatalysis (Goldbeter, 1991).

asymptotic maximum (called ratio of growth and Additionally, a predator–prey life cycle that was

denoted as R g). Some limitations with this approach successfully duplicated in a controlled experiment

were encountered. Microbial population data collected utilizing planktonic rotifers feeding on algae in a

after completion of the stationary phase showed a chemostat was also modeled by integrating a bio-

decline, characteristic of the death phase of the chemically based set of ODEs (Fussman et al., 2000).

bacterial life cycle (McMeekin et al., 1993; Bailey The quasi-chemical model postulates an underlying

and Ollis, 1986; Lynch and Poole, 1979). For some reaction scheme that combines autocatalytic growth

data profiles, distinguishing late stationary phase data and negative feedback, presumably in the form of a

from early death phase data was ambiguous, and the hypothetical antagonistic metabolite, which hastens

resulting estimated value of l depended on which the death of the actively multiplying cells. The actual

data was included in the kinetics growth curve. chemical identity of this antagonist and its biomolec-

Microbial kinetics models generally fit either ular mechanism have not yet been confirmed. One

growth or death kinetics (Legan et al., 2002; Baranyi possibility is that the production of low levels of a

and Roberts, 2000; McMeekin et al., 1997; Whiting, diffusible metabolite by the bacterial cells acts as an

1995). Some alternative models have been proposed intercellular signalling molecule and inhibits growth

to account for microbial growth–decline data, such as in the cell density-dependent gene expression phe-

the three-step enzyme kinetics model (Whiting and nomenon commonly referred to as quorum sensing

Cygnarowicz-Provost, 1992). Other models combine (Smith et al., 2004; England et al., 1999; Novick,

expressions for growth and death into a single 1999; Bassler, 1999). Another possible negative

equation, such as the logistic model with a super- feedback mechanism would involve the accumulation

imposed Fermi term (Peleg, 1996), the Jones and of a waste product such as lactic acid (Vereecken et

Walker model (Jones and Walker, 1993; Jones et al., al., 2003). A mechanism involving nutrient depletion

1994), the Churchill model (Membré et al., 1997), and (Leroy and De Vuyst, 2004) is less likely for

a model combining two Baranyi-type equations for describing the growth of a pathogen such as S. aureus

yeast fermentation in a model wine system (Del in the nutrient-rich environment of a food product

Nobile et al., 2003). The Baranyi equation is a non- (Van Impe et al., 1999; McMeekin et al., 1993; Lynch

autonomous differential equation (Baranyi et al., and Poole, 1979).

1993; Baranyi and Roberts, 1994) that is used to From the proposed hypothetical mechanism, one

model microbial growth kinetics in foods (Membré et can establish a set of kinetics rate equations that

al., 1999), and whose mathematics have been studied form the basis for a system of ordinary differential

extensively (Baranyi and Roberts, 1995). equations (ODEs) that imbue the quasi-chemical

The quasi-chemical model combines the concepts model with mathematical attributes. These attributes

of chemical kinetics and predictive modeling in foods. of the quasi-chemical model were originally used

Applying chemical kinetics to the macroscopic (Taub et al., 2003) to fit growth–death kinetics data

behaviors of microbial populations requires a much- and death-only kinetics for S. aureus in bread as

simplified view of the network of biochemical functions of a w, pH, and temperature. Statistical

reactions occurring in the microorganism (Bray and analysis of the results from the quasi-chemical

White, 1966; Hinshelwood, 1953). Insight into these model produced mathematical relationships among

complex metabolic processes can be gained from the parameters that were used to delineate a growth/

E.W. Ross et al. / International Journal of Food Microbiology 99 (2005) 157–171 159

teresting comparison showed that the quasi-chemical Summary of mechanism and equations for the quasi-chemical

model

model estimated values of l for the growth–death

and growth-only data different from the value Reaction Rate ODEs

step equations

estimated with the Gompertz function (for the

MYM* v 1=k 1M dM =dt ¼ ð v1 Þ ¼ k 1 M ð1Þ

growth-only data). More recently, the quasi-chemical

model has been generalized (Feeherry et al., 2004) M*Y2M*+A v 2=k 2M* dM 4=dt ¼ ðv1 þ v2 v3 v4 Þ

to characterize the growth–death kinetics for other ¼ k1 M þ M 4ðG eAÞ ð2Þ

pathogens (Escherichia coli and Listeria monocyto- M*+AYD v 3=k 3M*A dA=dt ¼ ðv2 v3 Þ ¼ M 4ðk2 eAÞ ð3Þ

genes) in foods (IM turkey meat, ham, and cheese)

M*YD v 4=k 4M* dD=dt ¼ ðv3 v4 Þ ¼ M 4ðk4 þ eAÞ ð4Þ

under various experimental conditions (a w, pH,

U ðtÞ ¼ M ðtÞ þ M4ðtÞ ð5Þ

temperature, and lactate concentration). Additionally,

the quasi-chemical model was successfully tested to

account for the inactivation kinetics of E. coli in

model foods using the emerging non-thermal tech- The net natural growth rate, G ( Guk 2–k 4), depicts the

nology of high pressure processing (Feeherry et al., excess of the growth rate over the natural death rate.

2004). Presently, we explore the mathematical The parameter e relates to k 3 by e=hk 3, in which the

properties of the quasi-chemical kinetics model that scaling factor h (defined as h=e/k 3) is assigned the

make it a useful tool for predictive microbiology. value 109 (and consequently (0Vebb1) to facilitate

We examine the mathematical relationships among numerical solutions of the ODEs. The initial con-

the parameters that give the quasi-chemical model ditions at t=0 are as follows: M equals I (the inoculum

the ability to fit growth–death kinetics and (linear level, Ic103–104), and M*=A=D=0. Changes in the

and nonlinear) death kinetics satisfactorily. In microbial population size are represented by the

Appendix A, we list the MATLAB programs that quantity U=M+M* (in units of CFU/mL) and are

can be used to fit data by this model, and Appendix B derived from microbiological plate counts that do not

describes a worked example of a typical data set using distinguish lag phase (M) and growth phase (M*) cells

these programs. The authors would be pleased to (see Table 1, Eq. (5)). Fig. 1 (Taub et al., 2003) depicts

provide electronic versions of these programs upon the behavior of the individual entities in the quasi-

request. chemical mechanism (M, M*, A, D, and U) from the

fit of a typical set of growth–death kinetics data.

3. Results

2.1. The quasi-chemical model

3.1. Properties of the model

Table 1 briefly summarizes the theoretical basis of

the quasi-chemical model; namely, the hypothetical The growth–death profile of U(t) shown in Fig. 1

four-step reaction scheme, and the corresponding rate is based on a non-zero value of k 3 (k 3=100) and a

equations and system of ODEs (Taub et al., 2003). positive value of G (k 2–k 4=2). When the relative

The concentration of lag phase cells is denoted by M, values of the rate constants are varied, different

growth phase cells by M*, antagonist by A, and dead patterns for U as a function of time are observed.

cells by D. The concentrations and rate constants (k 1 Fig. 2 displays U(t) with GN0 and fixed values of

through k 4) have only non-negative values. The k 1=1, k 2=4, and k 4=2, while k 3 is varied incrementally

procedures for making initial estimates for these from 0 to 1000. With values of k 3N0, the calculated

parameters and determining quantities such as max- function for U (and also for M*—see Fig. 1) as a

imum logarithmic growth rate (l), lag time (k), function of time depicts growth to a maximum

maximum population size (called the ratio of growth followed by a decline. As k 3 becomes larger, the

and denoted R g) are described in subsequent sections. calculated U(t) function becomes more pulse-like,

160 E.W. Ross et al. / International Journal of Food Microbiology 99 (2005) 157–171

Fig. 1. Predicted plot of individual functions M, M*, A, D, and U versus time with k 1=1, k 2=4, k 3=100, and k 4=2.

reaching its maximum earlier and at a lower value. The ODE system (Table 1) is generally nonlinear

When k 3=0, the function U(t) shows limitless, nearly due mainly to the interaction between the variables

linear growth, which was not observed experimentally. M* and A in Eqs. (2) and (3), and solutions cannot

Fig. 2. Predicted effect of non-zero values of k 3 on growth–death behavior exhibited by U(t) with {k 1=1; k 2=4; k 3=0, 1, 10, 100, 1000; and

k 4=2}.

E.W. Ross et al. / International Journal of Food Microbiology 99 (2005) 157–171 161

always be expressed by exact formulas. An exception decreases. Moreover, the quantity [1e/(t )]V1,

is the solution to Eq. (1) which when inserted into Eq. (7) leads to

that shows that M undergoes an exponential decline Consequently, A(t) increases steadily from zero as

from I toward zero over time. The variable D is absent time increases, but its value remains below the upper

from Eqs. (1)–(3) and can be calculated from Eq. (4), bound of k 2/hk 3 (see Fig. 1). The relationship

after M* and A have been determined (see Table 1). between A and M*, Eq. (7), establishes an essential

Since D does not influence the other variables, and M feature of the ODE system (Table 1) when k 3p0. In

is known if k 1 is known, the relationship between M* the special case of k 3=0, this upper bound becomes

and A can be determined in the following way. First, irrelevant.

assume that M*(t) is known, then solve Eq. (3) by The interrelationship between A and M* in

elementary means (variation of parameters) according response to variations in the values of the rate

to Eq. (7) constants and their relative proportions can be seen

in phase-plane plots. Figs. 3 and 4 show trajectories in

h i the (M*, A) phase plane using values of A and M*

Aðt Þ ¼ ðk2 =eÞ 1 e/ðtÞ obtained by numerical solution of Eqs. (1)–(4) and

Z s¼t

representative values assigned to the k’s. The arrows

ðin which /ðt Þ ¼ e M 4ðsÞdsz0Þ ð7Þ in Figs. 3 and 4 indicate the direction of the respective

s¼0 trajectories as t increases from 0.1 to 10. In Fig. 3, the

value of the rate constants are set {k 1=1; k 2=2, 3, 4,

Eq. (7) is not a solution for A, since M* is not known, and 5; k 3=0; and k 4=4} such that k 3=0 and G ranges

but rather an integral relationship between A and from negative to positive values. In these cases with

M *. Differentiating Eq. (7) leads to dA /dt = k 3=0 and GN0, the model projects unrestrained

k 2M*(t)e/(t )N0, which implies that A(t) never growth of M* and A. With k 3=0 and Gb0, A increases

Fig. 3. Phase-plane plot [A, M*] showing trajectories interrelating A and M* with various values of G (=k 2k 4) when k 3=0.

162 E.W. Ross et al. / International Journal of Food Microbiology 99 (2005) 157–171

Fig. 4. Phase-plane plot [A, M*] showing trajectories for various values of G when k 3=100.

toward a limiting value, and M* changes only slightly, Eq. (9) is satisfied when M=0, Eqs. (11) and (12) are

then decreases. Fig. 4 illustrates phase-plane plots satisfied when M*=0, and Eq. (10) is satisfied when

with a set of rate constant values {k 1=1; k 2=2, 3, 4, M=M*=0. The lone critical point in this system occurs

and 5; k 3=100; and k 4=4} such that k 3N0 and G with M=M*=0 and is reached only in the limit as

ranges from negative to positive values. With k 3=100 t Yl. The values of D(t) and A(t), as mentioned

and GN0, the phase trajectories do not exhibit the previously for Eqs. (3) and (4), increase steadily

limitless growth seen in Fig. 3. Instead, both M* and towards constant values as t Yl (see Fig. 1, for

A increase initially, then M* eventually reaches a which k 3N0 and GN0).

maximum and later declines, while A tends continu-

ously toward a limiting maximum value. With k 3=100 3.3. Behavior near t =0

and Gb0, the trajectory behaves similarly to its k 3=0

and Gb0 counterpart (Fig. 3). These results indicate Approximate solutions of the following form are

that non-zero values of k 3 and positive values of G are useful near the beginning of the process (when tc0)

needed to produce growth–death kinetics. and can be found by a Taylor series expansion about

t =0:

3.2. Behavior as t Yl

k 2 t2

The critical points of the system (i.e. the points at M cI 1 k1 t þ 1 ð13Þ

2

which the system as a whole is stationary) must satisfy

the following conditions

dM =dt ¼ 0 ¼ k1 M ð9Þ ðG k1 Þt 2

M 4ck1 I t þ ð14Þ

2

dM 4=dt ¼ 0 ¼ k1 M þ M 4ðG eAÞ ð10Þ

dA=dt ¼ 0 ¼ M 4ðk2 eAÞ ð11Þ

k1 k2 It 2

dD=dt ¼ 0 ¼ M 4ðk4 þ eAÞ ð12Þ Ac ð15Þ

2

E.W. Ross et al. / International Journal of Food Microbiology 99 (2005) 157–171 163

k1 k4 =t 2

Dc ð16Þ influence in the early stages, and the approximate

2 solutions for k 3=0 (Eqs. (18)–(22)) can be used.

Gk1 t 2

U cI 1 þ ð17Þ U cM 4c k1 I=mÞeGt and lnðU Þclnð k1 I=mÞ þ Gt

2

Eq. (14) shows that M* increases initially from 0 When k 3=0, Eqs. (2) and (3) lead to the equation

approximately linearly, while A and D increase more dU =dt ¼ dM =dt þ dM4=dt ¼ GM 4

slowly and in a quadratic fashion according to the

ratio ¼ Gk1 If ðt; mÞeGt

c that U always increases with t if GN0, and corre-

D k4

spondingly U always decreases if Gb0. Growth–

U increases if GN0, and decreases if Gb0. In all cases decline kinetics (Taub et al., 2003) cannot be

at t=0, dU/dt=0, and the model predicts that U(t) predicted by the formulas derived with k 3=0 in Eqs.

always exhibits a non-zero value for the initial lag, (18)–(22). Relatively large values of k 3 are needed for

although its duration may be immeasurably small. the quasi-chemical model to depict the growth–death

None of these approximations is affected by k 3. At phenomenon characteristic of the microbial life cycle.

sufficiently early times, solutions with k 3=0 are there- The relation of the maximum (logarithmic) growth

fore acceptable approximations to the true solutions. rate (l) and G is consistent with these findings. Let

3.4. Approximation when k 3=0 L ¼ Lðt Þ ¼ log10 fU ðt Þg; then Lclog10 ð k1 I=mÞ þ BGt

In examples with k 3=0, the nonlinear terms approximately constant,

disappear from the ODE system, and the effect of A

on the microbial kinetics is negligible. In this case, dL=dtcBG

exact solutions for M*, A, and U can be found by

elementary means as follows: lumaxf dL=dt g ð23Þ

Since dL/dt is approximately constant, this equation

M 4 ¼ k1 If ðt; mÞeGt ð18Þ

yields the relation

U ¼I emt þ k1 f ðt; mÞgeGt ¼ I ek 1t þ k1 f ðt; mÞeGt lcBG ð24Þ

ð19Þ Fig. 5 shows a plot of l versus G using previously

reported values obtained from modeling the growth–

A ¼ ð Ik1 k2 =mÞf f ðt; GÞ f ðt; k1 Þg ð20Þ death kinetics of S. aureus in IM bread at various

conditions of a w, pH, and temperature (Taub et al.,

with the definitions

2003). The straight-line graph of Eq. (24) shows that

m ¼ G þ k1 ¼ k1 þ k2 k4 ð21Þ the latter is a good predictor of this relationship,

except possibly when |G| is near zero. This estimate is

consistent with the conclusion that l usually occurs

f ðt; mÞ ¼ ð1 emt Þ=m ð22Þ

early enough in the process to justify the application

A special case occurs when k 1 is very large. These of the approximate solutions obtained for k 3=0.

conditions are uncommon and require special circum-

stances that will be discussed later. Specifically, when 3.5. The death-only case

k 1NN|G|, the value of mck 1NN1, and accordingly

f(t,m)c1/m. After a brief time increment elapses, The quasi-chemical model also fits death-only

MbbM* and UcM*. kinetics observed as a result of bno-growthQ con-

164 E.W. Ross et al. / International Journal of Food Microbiology 99 (2005) 157–171

Fig. 5. Linear relationship of l and G (values obtained from fitting with the quasi-chemical model) in accordance with Eq. (24) (l=BG).

ditions of a w, pH, and T (Taub et al., 2003), or from (especially those involving high pressures), the plot of

the application of high hydrostatic pressure (Feeherry log(U) versus t is approximately linear, and Eqs. (18)–

et al., 2004). The fitting procedure in these cases leads (22) show that [ G (fast set)ck 1(slow set)]. Although the

to two entirely different sets of parameters (called the functions U are nearly identical in both sets, the

bfast setQ and the bslow setQ) that fit the data equally different parameters calculate very distinct temporal

well. For example, the fitted lines calculated by the functions for M, M*, A, and D (Figs. 6 and 7). The

bfastQ and bslowQ sets for the high pressure ( P=50,000 most notable differences are the rapid decay of M and

psi) inactivation of E. coli in whey protein (Feeherry rapid production of M* in the fast set (Fig. 6), in

et al., 2004) are nearly identical, and the correspond- comparison to the slow decay of M and the slow rise–

ing estimates of l are also very similar (lc0.12, fall kinetics of M* generated by the slow set (Fig. 7).

see Table 2). With the slow set, the production of A is also

Both the bfastQ and bslowQ parameter sets have significantly delayed and the evolution of D is slightly

negligible values for k 3, and solutions are approxi- attenuated.

mated using Eqs. (18)–(22). The bfast setQ features

large values of k 1 (k 1NN1), and M*NNM shortly after 3.6. Model fitting and parameter estimation

t=0, while the bslow setQ has small values of k 1 and

M*bbM. In cases with negligibly small lag times Nonlinear least-squares analysis was used to

obtain best-fit values of the model parameters (rate

constants k 1 through k 4) by solving numerically the

ODE system for the four state variables M, M*, A,

Table 2 and D which lead to the estimate of the measure-

bFast setQ and bslow set Q from fitting microbial inactivation data

ment variable, U(t). This procedure was carried out

k1 k2 k3 k4 G l using MATLAB software, specifically the stiff

bFastQ 34.30 0.96 0 10.25 0.282 0.12 differential equation solver ODE15s, in conjunction

bSlowQ 0.282 0.70 0 19.31 18.62 0.12 with the nonlinear regression analysis program

E.W. Ross et al. / International Journal of Food Microbiology 99 (2005) 157–171 165

Fig. 6. Plots predicting M, M*, A, D, and U versus time for death kinetics using bfast setQ of parameters.

LSQNONLIN. These programs (see Appendices A squares fitting procedure worked well for data that

and B) require initial estimates for the k’s and were not too noisy, but the goodness of fit depended

iteratively seek the values of k’s that generate the on fortuitous initial estimates of the k’s. Like many

smallest sum of squared errors. Generally, the least- nonlinear searching programs, LSQNONLIN may fail

Fig. 7. Plots predicting M, M*, A, D, and U versus time for death kinetics using bslow setQ of parameters.

166 E.W. Ross et al. / International Journal of Food Microbiology 99 (2005) 157–171

if the initial choices are bad. Also, the initial estimates 4. Discussion

can appear to influence the final results if the data are

irregular or too sparse. While no general procedure The current models used most commonly for

will help in all cases, it is possible to state the microorganism kinetics (Gompertz or logistic

following rules of thumb using the information about equations) tend to focus exclusively on either

the mathematical properties of the model described growth or inactivation, and generally ignore the

above: death phase when it succeeds growth. The quasi-

chemical model (Taub et al., 2003), like some

(A) If the data appear to start by growing, choose reported alternatives, has the capacity to model

initial estimates having k 2Nk 4, and choose k 2bk 4 continuously growth–death kinetics and incorpo-

if the data decline with time. rates death data in the estimation of the growth

(B) Increasing k 1 generally speeds up the process. kinetics parameters. This feature is advantageous,

(C) If there is enough data near the start of the when there is a paucity or irregularity in the

process, Eqs. (13) and (17) may suggest an growth data, and also eliminates the need for

initial estimate of G. subjectivity when determining which stationary

(D) In program SD in Appendix A, the line that phase data constitute the endpoints of the growth

begins LB=[. . . allows the user to specify lower curve.

and upper bounds in the search for parameter The quasi-chemical model consists of four

values. For example, if we think that k 1c2, we autonomous ODEs for four variables (M, M*, A,

can simplify the search by setting LB=[1.9 1 1 and D) which together specify the system and the

1]; UB=[2.1 1 1 1] on that line. predicted microorganism concentration, U(t). Even

this rudimentary representation of the microbial

The value of l was estimated by numerically life cycle provides some insight into the metabolic

differentiating L(t)=log10(U(t)) to find its slope and activities governing the closed-system behavior of

searching for the maximum of that slope. In cases the bacterial cell. Specifically, the model predicts

where only death occurred, l was determined from (at least) two different pathways to death, one that

the minimum slope of L(t) as a negative growth occurs in no-growth conditions and another that

rate. If the time at which l occurs is defined as t l , prevails after a period of robust growth through a

then the lag (denoted k) is estimated from the mechanism involving negative feedback. Bacteria

formula are known to produce substances that inhibit

growth, some in the form of diffusible molecules

k ¼ tl Ll Lo =l: that act in a cell density-dependent way to

influence specific gene expression, called quorum

where sensing (Smith et al., 2004; England et al., 1999;

Novick, 1999; Bassler, 1999), and others in the

Lo ¼ Lð0Þ and Ll ¼ L tl form of organic acids (Vereecken et al., 2003).

We do not present experimental evidence to

The ratio of growth (R g) characterizes the extent of confirm the presence, identity, or mechanism of

multiplication of the initial organism concentration the hypothetical antagonist in the quasi-chemical

(asymptotic maximum). The quantity R g is model that is proposed to act in a manner

expressed by the relation analogous to these known inhibitors. The present

results do not contradict the hypothesis that there

Rg ¼ log10 fmax½U ðt Þ =U ð0Þg ð25Þ is more than one pathway to death of the

organism, and that metabolic by-products influence

The quantity R g applies only to situations involving the rate of the alternate pathways.

growth, and R g has the value of zero, in cases when The quasi-chemical model is an ODE model

only death kinetics are observed (bno-growthQ based on the simple premise that the mathematical

conditions). model comprises one or more differential equa-

E.W. Ross et al. / International Journal of Food Microbiology 99 (2005) 157–171 167

tions. Presently, the ODE model contains four ization of the death rate as (l), but other

parameters (k 1 through k 4) that specify the model definitions are possible and could be a subject

behavior and are estimated by fitting the data (U). for future study. In cases where only growth

The ODEs are generally nonlinear due to the kinetics data are collected, a cursory exploration

interaction of M* and A in the proposed mecha- of existing data suggested that in the fitting

nism, and this relationship is critical for reproduc- process the resulting estimates of the k’s might

ing growth–death kinetics. Solutions to the ODEs sometimes depend on the initial estimates of these

obtained through various approximations show that parameters. However, as in the death-only case,

the behavior of U depends principally on certain the changes in the k’s did not appear to affect the

values for the quantities k 3 and G. Specifically, estimates of U or l significantly.

only if k 3N0 and GN0, will U(t) show growth–

decline behavior. If k 3z0 and Gb0, then only

death occurs. The value of l is linearly related to Acknowledgements

G (see Eq. (24) or Fig. 7), but k and R g are not

closely associated with G or the k’s. The parameter k 1 The authors wish to express their gratitude to

affects primarily the overall time-scale of the process, Mr. James Doona (Mathematician), Dr. Jack Briggs

and the relation between M* and A is not directly (Senior Food Technologist), and Dr. Fred Allen

affected by changing k 1 (Eq. (7)). The approximations (Chemical Engineer) for providing helpful discus-

made when k 3=0 are influenced by the quantity m, sions and insight into issues regarding mathe-

which depends on k 1 (Eq. (21)). If k 3=0, the model matics, fermented food products and bioprocess

predicts that U grows without limit when GN0, and engineering.

declines when Gb0. None of the data exhibited

unlimited growth.

The quasi-chemical model adequately character- Appendix A. MATLAB programs for fitting the

izes the death-only case (when Gb0) in the sense ODE model

that it can satisfactorily fit the U(t) data and

estimate a value for l. In its present form, the These programs for fitting the data by the ODE

model lacks uniqueness, since at least two sets of model consist of a MATLAB script, SD, that

parameters may provide equally good fits of the invokes the nonlinear least-squares function

data. In fact, all sufficiently large values of k 1 in LSQNONLIN which calls the function, ED, to

the bfast setQ that induce M to become negligible assist in the fitting. ED uses MATLAB program

quickly will also produce nearly identical values ODE15S to solve the ODE system which is defined

of U(t). Eq. (19) justifies this statement; the in the function FD. The separate MATLAB script

relationship mck 1NN1 implies k 1f(t,m)c1, and PredODE simply calculates the solutions, M, M*,

UcIeGt (i.e. U depends only on G and not k 1). For A, D, and U, given the k values and the initial

some purposes, this non-uniqueness is not detri- variable values; it does not involve any fitting of

mental. It suggests that the model in its current data but does solve the ODE system. Each of these

form may be over-parameterized for death-only programs must be stored in a file having the same

kinetics, but also leaves open the question of name as the program, e.g. SD must be stored in a

which parameter set more closely resembles the file named SD.m. The percent symbol, %, in the

true dynamics. Both parameter sets are equally programs denotes that the remaining text on that

valid in terms of mathematics, and more exper- line is merely commentary. In these programs, the

imental data would be needed to distinguish which variables M, M*, A, and D are re-named in matrix

is more appropriate from a microbiological per- fashion as follows:

spective. This uncertainty does not affect the

determination of U(t) or l, although there is M ¼ x1 ¼ xð :; 1Þ; M * ¼ x2 ¼ xð :; 2Þ; A ¼ x3

ambiguity in the definition of l when Gb0. The

present definition leads to quantitative character- ¼ xð :; 3Þ; D ¼ x4 ¼ xð :; 4Þ:

168 E.W. Ross et al. / International Journal of Food Microbiology 99 (2005) 157–171

E.W. Ross et al. / International Journal of Food Microbiology 99 (2005) 157–171 169

Appendix B. Output of comparison calculations Next is the command, SD, to execute the script SD.

This is followed by output from SD. The first block

Below we show the input and output for a of output gives information about the intermediate

MATLAB fitting of a typical data set. First, we steps in the repetitive process that LSQNONLIN

display the results for the ODE model. The uses. Generally, f(x) and the Norm of Step should

solicitation symbol, NN, displayed by MATLAB, both decrease, but the latter may occasionally

indicates that we are expected to enter something increase slightly from one iteration to the next. We

from the keyboard. The first three entries are the do not list below all the steps in the iteration, but

input, which defines the quantities td, xd, the time only the first few and last few. The output may

and concentration, i.e. the test data that we are trying depend slightly on the computer and operating

to fit, and k, our initial guesses for the parameters. system on which this is run.

170 E.W. Ross et al. / International Journal of Food Microbiology 99 (2005) 157–171

calculates l, k, and R g and makes a smoother graph of

the predicted U than SD does. Bailey, J.E., Ollis, D.F., 1986. Biochemical Engineering Funda-

mentals. McGraw-Hill, New York.

Baranyi, J., Roberts, T.A., 1994. A dynamic approach to predicting

bacterial growth in food. Int. J. Food Microbiol. 23, 277 – 294.

Baranyi, J., Roberts, T.A., 1995. Mathematics of predictive food

microbiology. Int. J. Food Microbiol. 25, 199 – 218.

Baranyi, J., Roberts, T.A., 2000. Principles and applications of

predictive modeling of the effects of preservative factors on

microorganisms. In: Lund, B.M., Baird-Parker, T.C., Gould,

G.W. (Eds.), The Microbiological Safety and Quality of Food,

vol. 1. Aspen Publishers, Gaithersburg, pp. 342 – 358.

Baranyi, J., Roberts, T.A., McClure, P.J., 1993. A non-autonomous

differential equation to model bacterial growth. Food Microbiol.

10, 43 – 59.

Bassler, B.L., 1999. How bacteria talk to each other: regulation of

gene expression by quorum sensing. Curr. Opin. Microbiol. 2

(6), 582 – 587.

E.W. Ross et al. / International Journal of Food Microbiology 99 (2005) 157–171 171

Bray, H.G., White, K., 1966. Kinetics and Thermodynamics in McMeekin, T.A., Brown, J., Krist, K., Miles, D., Neumeyer, K.,

Biochemistry. Academic Press, New York, pp. 364 – 404. Nichols, D.S., Olley, J., Presser, K., Ratkowsky, D.A., Ross,

Del Nobile, M.A., D’Amato, D., Altieri, C., Corbo, M.R., T., Salter, M., Soontranon, S., 1997. Quantitative Micro-

Sinigaglia, M., 2003. Modeling the yeast growth-cycle in a biology: a basis for food safety. Emerg. Infect. Dis. 3 (4),

model wine system. J. Food Sci. 68 (6), 2080 – 2085. 541 – 549.

England, R.R., Hobbs, G., Bainton, N.J., Roberts, D.M., 1999. Membré, J.M., Thurette, J., Catteau, M., 1997. Modeling the

Microbial Signaling and Communication, 57th Symposium of growth, survival, and death of Listeria monocytogenes. J. Appl.

the Society for General Microbiology. Cambridge University Microbiol. 82, 345 – 350.

Press, Cambridge. Membré, J.M., Kubaczka, M., Chéné, C., 1999. Combined effects

Epstein, I.R., Pojman, J.A., 1998. An Introduction to Nonlinear of pH and sugar on growth rate of Zygosaccharomyces rouxii, a

Chemical Dynamics. Oxford University Press, New York. bakery product spoilage yeast. Appl. Environ. Microbiol. 65

Feeherry, F.E., Doona, C.J., Taub, I.A., 2003. Effect of water (11), 4921 – 4925.

activity on the growth kinetics of Staphylococcus aureus in Novick, R.P., 1999. Regulation of pathogenicity in Staphylococcus

ground bread crumb. J. Food Sci. 68 (3), 982 – 987. aureus by a peptide-based density-sensing system. In: Dunny,

Feeherry, F.E., Ross, E.W., Doona, C.J., 2004. A quasi-chemical G.M., Winans, S.C. (Eds.), Cell–Cell Signaling in Bacteria.

model for the growth and death of microorganisms in foods by ASM Press, Washington, DC, pp. 129 – 146.

non-thermal and high pressure processing. Int. J. Food Micro- Peleg, M., 1996. A model of microbial growth and decay in a closed

biol. (in press). habitat based on a combined Fermi’s and the logistic equation. J.

Fussman, G.F., Ellner, S.P., Shertzer, K.W., Hairston, N.G., 2000. Sci. Food Agric. 71, 225 – 230.

Crossing the Hopf bifurcation in a live predator–prey system. Smith, J.L., Fratamico, P.M., Novak, J.S., 2004. Quorum sensing: a

Science 290, 1358 – 1360. primer for food microbiologists—review. J. Food Prot. 67 (5),

Goldbeter, A., 1991. Biochemical Oscillations and Cellular 1053 – 1070.

Rhythms. Cambridge University Press, London. Taub, I.A., Feeherry, F.E., Ross, E.W., Kustin, K., Doona, C.J.,

Hinshelwood, C.N., 1953. Autosynthesis. J. Chem. Soc., 1947 – 2003. A quasi-chemical kinetics model for the growth and

1956. death of Staphylococcus aureus in intermediate moisture bread.

Jones, J.E., Walker, S.J., 1993. Advances in modeling microbial J. Food Sci. 68 (8), 2530 – 2537.

growth. J. Ind. Microbiol. 12, 200 – 205. Van Impe, J.F., Versyck, K.J., Vereecken, K.M., Geeraerd,

Jones, J.E., Walker, S.J., Sutherland, J.P., Peck, M.W., Little, A.H., Dens, E.J., Bernaerts, K., 1999. Predictive micro-

C.L., 1994. Mathematical modeling of the growth, survival, biology of structured foods: development of a unifying

and death of Yersinia enterocolitica. Int. J. Food Microbiol. 23, modeling framework and application to microbial interac-

433 – 447. tions and the selection of advanced model building blocks.

Legan, D., Vandeven, M., Stewart, C., Cole, M., 2002. Modeling In: Tuijtelaars, A.C.J., Samson, R.A., Rombouts, F.M., Noter-

the growth, survival, and death of bacterial pathogens in foods. mans, S. (Eds.), Food Microbiology and Food Safety into the

In: de W. Blackburn, C., McClure, P.J. (Eds.), Foodborne Next Millenium. Ponsen & Looyen, Wageningen, Netherlands,

Pathogens: Hazards, Risk Analysis, and Control. Woodhead pp. 913 – 918.

Publishing, Cambridge, pp. 53 – 95. Vereecken, K.M., Devlieghere, F., Bockstaele, A., Debevere, J., Van

Leroy, F., De Vuyst, L., 2004. Growth of the bacteriocin-producing Impe, J.F., 2003. A model for lactic acid-induced inhibition of

Lactobacillus sakei strain CTC 494 in MRS broth is strongly Yersinia enterocolitica in mono- and co-culture with Lactoba-

reduced due to nutrient exhaustion: a nutrient depletion model cillus sakei. Food Microbiol. 20, 701 – 713.

for the growth of lactic acid bacteria. Appl. Environ. Microbiol. Whiting, R.C., 1995. Microbial modeling in foods. Crit. Rev. Food

67 (10), 4407 – 4413. Sci. Nutr. 35 (6), 467 – 494.

Lynch, J.M., Poole, N.J., 1979. Microbial Ecology: A Conceptual Whiting, R.C., Cygnarowicz-Provost, M.L., 1992. A quantitative

Approach. John Wiley & Sons, New York. model for bacterial growth and decline. Food Microbiol. 9,

McMeekin, T.A., Olley, J.N., Ross, T., Ratkowsky, D.A., 1993. 269 – 277.

Predictive Microbiology: Theory and Application. Research

Studies Press, Somerset.

- Linear RegressionUploaded bySpiffyladd
- knowledge claims and knowledge questionsUploaded byapi-242697958
- Baltagi-EconometricsUploaded byshishirkashyap
- Refresher2 MathUploaded byHary Kriz
- THE BOUNDARY VALUE PROBLEM FOR SECOND ORDER ORDINARY LINEAR DIFFERENTIAL EQUATION WITH VARIABLE COEFFICIENTUploaded byGMAIL
- Velocity analysis using nonhyperbolic moveoutUploaded byaziz
- A MatlabSimulink Toolbox for Inversion of Local Linear Model Trees.pdfUploaded byAfi LA
- lecture1.pdfUploaded byvivekzz
- Carascteristici ale catalizei drojdiei de bereUploaded byloxy88
- Industrial Project ManagementUploaded byhugo_trindade_7
- Autonomous Calibration of Robots Using Planar PointsUploaded by徐锐
- Pamphlet BiotechUploaded byRhenzo Yu
- UT Dallas Syllabus for math2420.501.10f taught by Zalman Balanov (zxb105020)Uploaded byUT Dallas Provost's Technology Group
- Hominids Adapted to Metabolize Ethanol Long Before Human Directed Fermentation 2014Uploaded byGaby Arguedas
- 09 - ODE - 01 - Ordinary Difference EquationUploaded bySalam Daeng Bengo
- equations in enzyme kineticsUploaded byAndrew Sam
- 20131217 PSC Item XX Standard Component Dynamic ListUploaded bySabaMannan123
- CIV340 Mock ExamUploaded byapi-3707273
- Complex Reactions (1)Uploaded byAdara Afifah Fadhilah
- 399-419Uploaded byNguyễn Yến Tịnh
- Sol Man 2807Uploaded byRozaimi Abu Samah
- Ch5 Forecasting HeizerUploaded byabdul samad
- 06 Reliability and Maintenance Lecture #6Uploaded byFelipe
- Simulation and Modeling of DC Motor by Current Response ModelUploaded byNarendarkrish
- DE ZG535Uploaded byRaaj Thevar
- de applicationsUploaded bynoteasytobeboo
- UGCUploaded byBangaru Babu
- Introduction_to_EconometricsUploaded bybhumikajindal
- Poles as Natural ModesUploaded byZia Azam
- tfnUploaded byTimothy Fields

- 6818807Uploaded byNguyễn Sun
- FST Handbook 2014-Final Copy 1.pdfUploaded byDelvon Downer
- Kinetics Simple ModelsUploaded bykadosa
- ChaplinUploaded byr0803
- 3 Enzyme KineticsUploaded byLee Ping Shin
- jrrysn.docxUploaded byEureca Parra
- Lecture Notes Growth Kinetics Growth PhasesUploaded bySAMUEL
- Colistin stimulates the activity of neutrophil elastase and.pdfUploaded byMaria Lutenco
- A Rapid Pro-hemostatic Approach to Overcome Direct Oral AnticoagulantsUploaded byAllan John Barcena
- Dtn410k USER Manual Rev01Uploaded byFranco Veliz Flores
- EnzymesUploaded byCatherine Merilleno
- Enz Act ProbUploaded byksboopathi
- Laporan Kinetika Reaksi EnzymeUploaded byWahyuniAntari
- Introductory Biochemistry - David ShintaniUploaded byDạy Kèm Quy Nhơn Official
- LAB 8 CHE506.docxUploaded byAeyrul Khairul
- 17 Modelling BiofilmsUploaded byJose Suarez
- ph_and_enzyme_0Uploaded byMechAttack
- Lignin Peroxidase of Phanerochaete ChrysosporiumUploaded byLee Laam
- B-Gal Michaelis-Menten App NoteUploaded byCamilo Ernesto Araujo Barabas
- Exam 2 ReviewUploaded byjohnreese162
- Comparison of Different Models of Substrate and Product InhibitionUploaded bymaricee
- Grivennikova Et Al Fumarate Reductase 93xx 120806Uploaded byjenjavier
- Problems for Zero-Order Kinetics and First-Order KineticsUploaded byRoger B Verosil
- The Enzymes, Mechanisms of Catalysis- David S. SigmanUploaded byFriendlyGoodGirl
- Unit II 2 Environmental Engineering IUploaded bySushmita Shruti
- UT Dallas Syllabus for chem6361.001.07s taught by Donovan Haines (haines)Uploaded byUT Dallas Provost's Technology Group
- GATE Life Sciences 2008Uploaded byvishnukesavieam1
- MSc Biotechnology Assignment QuestionpapersUploaded byAISHA MUHAMMAD
- Enzyme Kinetics FinalUploaded byprashant_cool_4_u
- 9647_2016Uploaded bydharshanaab

## Much more than documents.

Discover everything Scribd has to offer, including books and audiobooks from major publishers.

Cancel anytime.