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© 1999 by CRC Press LLC

chapter five

Microbial and quality assessmentin thermal processing

Antonio Martínez, Carmen Rodrigo, Pablo S. Fernández, María J. Ocio, Francisco Rodrigo, and Miguel Rodrigo

Contents

Summary1 Introduction

2 Microbiological assessment3 Quality assessment References

Summary

The optimization and assessment of thermal processes requires accurate andreliable kinetic models and parameters. The importance of predictive micro-

biology is evident, and the need for equally good models of enzyme inacti-vation is particularly important in novel HTST (high temperature short timetreatments) processes. Aspects on the determination of microbial deathparameters and enzymic inactivation are discussed in this text, highlightingthe need for proper experimental methodologies.

1 Introduction

In recent years there have been important changes in habits and trends

related to food consumption (the incorporation of women in the workplace,community meals, fast food, etc.), scientific and technological advances (inter-pretation of nonenzymatic browning, development of thermostable and highlyimpermeable plastics, HTST followed by aseptic packaging, automation and

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computer-controlled processing, etc.), and in increased safety requirements(application of hazard analysis and critical control point (HACCP) systems,adjustment of national legislations to harmonize at the European Union level,

environmental protection, etc.). All these changes have acted as “drivingforces” promoting advances in food preservation and an increased knowl-edge base for alerting the consumer to food quality and safety.

One of the most commonly used, economical, and versatile techniquesfor food preservation is heat sterilization. Thermal treatment is also a tech-nique that is currently being proposed for combination with new technolo-gies (e.g., high pressures, pulsed electric fields) for inactivation of enzymesand destruction of spores, aspects practically impossible to achieve by thesenew technologies alone or else involving unjustifiably high costs.

The concept of preservation by heat, the process itself, and the equipmentused for its application have undergone major advances in the attempt toadapt to consumer demands (e.g., convenience, low cost, nutritive value)and health authority requirements, which call for greater control and microbiologic safety (e.g., application of the HACCP principle). In all processes inwhich heat is involved there are factors such as those related with microorgan-isms and quality factors that may affect microbiologic safety and the quality ofthe products manufactured. These factors include accuracy in the calculationof kinetic parameters and the deviations that may occur when values taken

from the literature, obtained in reference media, or over a range of conventionaltemperatures, are extrapolated to high temperatures (HTST conditions).In short, in order to achieve microbiologic safety and high quality in

thermally processed foods it is necessary to have correct kinetic data for bothmicroorganisms and quality factors, as well as inactivation or destructionpredictive models, with which it is possible to use time–temperature inte-grators that are widely applicable tools to evaluate the impact of heat onmicroorganisms and quality factors in a variety of novel processing situa-tions (see Chapter 2). This chapter explores the latest advances in these

aspects of thermal processing.

2 Microbiological assessment

For appropriate design and evaluation of sterilization processes it is essentialto have kinetic data for thermal inactivation of microorganisms that maypotentially contaminate the food (see Chapters 2 and 4).

The differences between the DT values obtained in reference media andthose obtained in real food samples may be considerable (Rodrigo et al.,1993; Fernández et al., 1994). Figure 1 is an example that shows a comparisonof the survival curves of Bacillus stearothermophilus in a reference mediumand in unacidified mushroom extract. As can be seen, the extract perceptiblyreduces the heat resistance of the spores. The same effect has been observedin Clostridium botulinum 213B (Brown and Martínez, 1992) and in Clostridiumsporogenes PA 3679 (Ocio et al., 1994). Environmental factors around thespores also affect their heat resistance. Xezones and Hutchings (1965) studied

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the inactivation of Clostridium botulinum in various groups of foods withdifferent pH values. The authors concluded that design, operation, and costsof sterilization were significantly affected by pH. Cameron et al. (1980) indi-cated that acidification to intermediate pH values could be used to achieve better utilization of sterilization for certain groups of food products. Rodrigoand Martínez (1988) studied the effect of an intermediate pH level of 5.2 onthe heat resistance of Clostridium sporogenes spores in artichoke extract andobserved DT values lower than those obtained in phosphate buffer, the phe-nomenon being more evident as treatment temperature increased.

The pH value can affect the DT value of microorganisms in various ways.On the one hand, acid pH may reduce the heat resistance of the spores, aneffect directly reflected in the severity of the sterilization process since thelethality required for microbiologic safety depends, among other things, onthe DT value at a given temperature. On the other hand, the pH of the foodproduct may inhibit or diminish microbial growth, especially of spores sen-sitized to pH after heat treatment (Fernández et al., 1995), and consequentlyreduce the apparent heat resistance of the spore. This phenomenon may beconsidered as a further safety factor in addition to the effect of heat treatment.

Although there is a general consensus on the reduction of heat resistanceof spores as pH decreases, there are fairly recent studies in which it is shownthat this effect could depend on the microorganism in question and on thetreatment temperature. Brown and Martínez (1992) indicated that when

Figure 1 Survivors curves for Bacillus stearothermophilus spores at 115°C showing theeffect of the food substrate.

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spores of Clostridium botulinum 213B were heated between 121 and 130°C inmushroom extract with various pH values and two different acidulants, theydid not see a clear effect of reduction of pH on the heat resistance of thespores. In the case of Clostridium sporogenes PA 3679, it has been observed

that the effect of acidification on pH depends on the specific pH value(Cameron et al., 1980; Ocio et al., 1994). Figure 2 is an example of survivalcurves for PA 3679 in acidified (pH 6.2) and unacidified (pH 6.7) mushroomextract. If we consider Bacillus stearothermophilus, much used in time–tem-perature integrators, there are studies that indicate reductions in DT valueas the pH of the mushroom extract decreases (Fernandez et al., 1994). In viewof these and other studies that may be found in literature, it is fair to saythat the effect of pH on the DT value could depend on the microorganismgroup, aerobic or anaerobic.

An important aspect in heat inactivation kinetic studies is the form ofheating and the method used for analyzing experimental data. Thermobac-teriology studies have conventionally been carried out in isothermal condi-tions. Determination of kinetic parameters in these conditions is relativelysimple and produces conservative sterilization or pasteurization processes.However, during heat treatment microorganisms are subjected to conditions

Figure 2 Survival curves for Clostridium sporogenes spores heated at 115°C in mush-room substrate with different pH values.

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that often differ substantially from isothermal experimental conditions. Analternative is to apply nonisothermal heating methods. These methods offerthe advantage of subjecting the spores to dynamic temperature conditions,

such as those that occur in real thermal sterilization processes. Tucker (1985)reviewed the various nonisothermal methods used in accelerated methodsfor the stability study of pharmaceutical products. These methods can also be used for microbial inactivation studies. Tucker (1985) discussed the fol-lowing temperature increase programs: 1) uncontrolled temperatureincrease, 2) linear program, 3) linear program followed by an isothermalperiod, 4) polynomial program, and 5) hyperbolic program.

With nonisothermal heating processes it is possible to obtain much infor-mation (experimental data) with a single experiment, with consequent sav-

ings in material, time and labor costs. Moreover, they provide a wealth ofdata for subsequent development of predictive models.

Experimental data in microorganism inactivation studies are generallyanalyzed by means of two successive linear regressions. In the first, thelogarithm of the concentration of the thermolabile factor remaining after heattreatment is plotted against time, giving the DT value. In the second regres-sion the logarithm of DT is plotted against treatment temperature, giving thez value. This methodology generally provides high confidence ranges, dueto the small number of degrees of freedom (Lund, 1983). Arabshahi and

Lund (1985) presented a method for analyzing kinetic data for inactivationof thiamine that provided smaller confidence ranges than those obtained byusing two linear regressions. To do this they calculated the activation energy,Ea, from the original experimental data taken as a whole, applying nonlinearregressions in a single step. A possible drawback of this methodology is thehigh correlation that may exist between the parameters estimated, DT and zor kT and Ea, causing convergence and accuracy problems. Nevertheless, theconvergence can be improved if the equations are transformed by takingnatural logarithms or reparameterizing.

Inactivation predictive models can be an excellent tool for ensuring themicrobiologic safety of the thermal process. There is growing interest inpredictive microbiology because of its many potential applications, such asestimating the effect of changes or of errors in estimating specific microor-ganism parameters (McNab, 1997), for example, DT or z. The successfulapplication of these models depends on developing and validating them inreal conditions (McMeekin and Roos, 1996).

The parameters that define the inactivation of microorganisms by heatin nonisothermal conditions by analyzing experimental data obtained in realsubstrates by means of single-step nonlinear regressions are of great valuefor the development of inactivation models that relate the DT value to envi-ronmental factors of importance in the canning industry, such as pH, sodiumchloride concentration, anaerobiosis, or water activity. Figure 3 shows anexample of a response surface relating the DT value to pH and treatmenttemperature. These models can be incorporated into a hazard analysis andcritical control point plan, to safeguard the sterilization process against any

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eventuality during the manufacturing process which might affect the DT valueof the microorganisms, potentially causing spoilage of the food product.

Finally, process evaluation occupies an important place within the microbiologic safety of the sterilization process. Over the years, various techniqueshave been developed for evaluating sterilization processes, which take place

in sealed cans or continuously by means of heat exchangers. Experimentalinoculation of cans with Clostridium sporogenes was one of the first proceduresused (NCA, 1968). Yawger (1978) developed the count reduction system, inwhich cans containing the product were inoculated with bacterial spores andsubjected to heat treatment in the same way as in the experimental inocula-tion of cans. Subsequently, procedures were developed in which the sporeswere confined in small containers made of glass, metal, or plastic, whichwere inserted in the can together with the food product (Michiels, 1972;Pflug, 1982). Recently, time–temperature integrators have been developed

by immobilizing spores in artificial food particles, polyacrylamide gel, oralginate containing food puree (Brown et al., 1984; Rönner, 1990, Ocio et al.,1997). This new generation of biological indicators is suitable for evaluating both conventional and heat exchanger sterilization processes, allowing inter-actions between the product and the spores immobilized in the particle(Rodrigo, 1997).

Figure 3 Surface response plot showing the relationship between pH, D value, andtemperature of treatment for Bacillus stearothermophilus spores heated in acidifiedmushroom substrate.

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3 Quality assessment

Nowadays there is a demand for natural-processed foods, without additives

and with characteristics that come closer to the fresh product — fresh like product, invisible manufacturing — without impairing microbiologic safety.Despite these consumer demands and the scientific and technologicaladvances recorded in recent years, some foods are still sterilized by meansof conventional systems and conditions or at temperatures that extract a highprice in terms of quality and process yield. A typical example is cannedasparagus, where heat has an appreciable impact on quality, revealed in lossof texture and weight, phenomena that are more evident in green asparagus.

Most of the studies related to the thermal destruction of enzymes and

quality factors in high temperature short time conditions have been per-formed with dairy products, and there is little information on other foods(Holdsworth, 1992). Application of these sterilization processes by usingnovel heating technologies may partly solve the loss of quality in productssuch as asparagus, if we bear in mind the good results obtained in juicesand milk. It has been verified that at high temperatures the rate of destructionof microorganisms is greater than the rate of loss of quality. It is this differ-ence that allows optimization of thermal processes in terms of retention ofnutrients and quality factors, including texture. However, this new situationmay create a problem that does not appear in canned products sterilized bymore conventional methods or at more conventional temperatures. Enzymesare also inactivated more slowly than microorganisms, so that there is adanger of residual enzymatic activity, which, by itself or by regeneration ofthe enzyme, may produce a degradation of food quality during storage. Thiskind of problem can be solved by application of optimized sterilizationprocesses, for which it is necessary to ascertain the precise kinetic parametersfor inactivation and regeneration of control enzymes (enzymes with greaterheat resistance) and the parameters for the most appropriate quality factors,which in the case of asparagus would be destruction of texture and weightloss, all obtained at high temperatures.

Peroxidase has traditionally been chosen as a control for establishingheat processes for foods. It is one of the most heat-resistant enzymes, it isfound in numerous vegetables, and the Food and Drug Administration(FDA) of the United States considers its inactivation necessary to reducequality losses during storage of manufactured foods (Whitaker, 1992). Onecharacteristic of peroxidase is its ability to regenerate after a sterilization pro-cess. The extent of the regeneration seems to depend on the type of vegetable,the isoenzyme considered, and basically on the heating time at a specific tem-

perature (Adams, 1978). Consequently, HTST sterilization processes may beless effective for irreversible inactivation of peroxidase than conventional pro-cedures. Therefore, in order to apply the new sterilization systems, it is neces-sary to study and develop models capable of interpreting the kinetics of inac-tivation and regeneration and of calculating the parameters that define them.

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An aspect to be borne in mind when seeking to carry out studies onthermal inactivation kinetics is the equipment to be used and how the sampleis to be heated. In order to study the heat resistance of enzymes such as

peroxidase, direct or indirect heating methods may be used. In indirectheating methods the sample is inserted in a tube, can, etc., and receives heatthrough an intermediate barrier. A possible disadvantage of these methodsis the relatively high period of heating inertia, which at high temperaturesmay affect the correct interpretation of experimental results. In direct heatingmethods the sample is in close contact with the heating medium, which inmost cases is saturated steam. These methods have the advantage that thelatent heat of steam is capable of producing extremely rapid heating. Thisgroup includes thermoresistometers, sophisticated devices in which it is

possible to achieve very short periods of inertia, 0.3 to 0.4 seconds, thusobtaining greater accuracy in the results. Thermoresistometers have beenmainly applied to the study of microorganism inactivation kinetics and littleis known of their suitability for studying enzyme inactivation kinetics. Rod-rigo et al. (1997) studied the inactivation kinetics of horseradish and aspar-agus peroxidase in a high-temperature thermoresistometer and concludedfor the suitability of the equipment. The thermoresistometer enabled thestudy of the inactivation kinetics of the more labile fraction of horseradishperoxidase at temperatures above 100°C.

As mentioned earlier, in order to optimize HTST sterilization processesit is essential to have precise kinetic data for inactivation of microorganismsand enzymes and for quality losses over the high temperature range. Thekinetic models employed for predicting and quantifying the impact of heattreatment on food constituents and the most reliable mathematical methodsfor determining the kinetic parameters for the degradation of those constit-uents are of the following types:

• First-order model

• nth

order model• Consecutive reactions model• Multifraction model

The first-order model is the most elementary chemical approach, con-sisting in considering the degradation of a quality factor or constituent as afirst-order reaction in which the reaction rate is proportional to the concen-tration of the constituent in question:

EN is the native species, ER is an inactive intermediate species, which, byheating, can be transformed reversibly into EN and irreversibly into EI , aninactive species; Keq is the equilibrium constant between EN and ER, and kI

E E ENK

R

keq← → → 1 1

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is the reaction rate constant for the inactivation of ER. This is the model mostcommonly employed for describing bacterial and enzymatic kinetics.

In the n-th order model it is assumed that the reaction rate is not pro-

portional to the concentration of the constituent but to some power of it. Theevolution of the concentration of a quality factor in relation to time corre-sponds to the following equation:

The model of consecutive reactions consists in assuming that the originalcomponent, E1, is transformed into an intermediate component, E2, which

has a different thermostability and is in turn inactivated and transformedinto E3:

The inactivation of E1 and E2 follows a first-order kinetics with reactionrate constants k1 and k2, respectively. The intermediate component may havean activity that differs from that of the original. This model has been suc-cessfully applied to inactivation of various enzymes (Henley and Sadana,

1984a, 1984b, 1985) and also specifically to explain the inactivation kineticsof peroxidase (Clochard and Guern, 1973; Wang and Dimarco, 1972; Saraivaet al., 1996).

In the multifraction model it is assumed that the original componentconsists of several components (two in the simplest case), with differentthermostabilities: a stable component (ES) and a labile component (EL), bothfollowing a first-order inactivation kinetic with reaction rate constants kSand kL respectively. This is the case with enzymes that consist of differentisoenzymes (Ling and Lund, 1978), microorganisms that present various

types of spores (Sapru and Labuza, 1993), or texture consisting of two sub-strates with differing thermal stability. An outline of this model could be thefollowing:

Texture has always been an important attribute of food, but in recentyears it has begun to receive more attention. A decade ago texture was almosta forgotten attribute, but now it is recognized as a saleable characteristic thatindicates the high quality sought by consumers; texture can lead to rejectionor substantial differentiation of a food product that may increase its sales. Itcan be said that a good food product texture is an indicator of high qualityand excellent preparation (Szczesniak, 1990). As has already been shown,

E E n k tn n T1

01 1−( ) −( )= − −( )

E E Ek k1 2 31 2

→ →

E E

E E

s

k

I

L

k

IL

s

S

L

→

→

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the optimization of sterilization processes for green asparagus also calls fora knowledge of the kinetics of texture loss during heat treatment. However,there are few models relating texture loss to heat treatment similar to those

that exist to represent the kinetics of microorganisms, enzymes, and foodcolor (Lund, 1982).

As with chemical reactions, texture changes due to heating are studied by using kinetic models depending on time and temperature, the data beingexpressed in terms of their reaction rate constants kT, or in terms of the DTvalue (Bourne, 1989). The major property of fruit and vegetable texture isfirmness. In general, texture is characterized by a physical quantity, such as,for example, the maximum force needed to cut an asparagus spear, and thisproperty is measured in relation to time and temperature.

Historically, two models have been applied to analyze experimental dataof texture degradation: the first-order model (Nagel and Vaughn, 1954, Pau-lus and Saguy, 1980), and the two-fraction model (Huang and Bourne, 1983).In the latter model it is assumed that the vegetable tissue consists of twosubstrates, A and B, with different thermal resistances, each with its kineticparameters and following first-order kinetics. For short times, the fasterprocess, corresponding to degradation of the labile substrate A, is dominant,and for longer times the dominant process is the degradation of the moreresistant substrate B, which has the slower kinetic process. Rodrigo et al.

(1997) studied the thermal degradation of green asparagus texture whenasparagus spears were heated between 70 and 100°C, and in the softeningcurve they observed a rapid initial reduction in firmness, which was almostlinear and coincided with first-order kinetics, but the softening ratedecreased with time and a second straight line with a new slope appearedfor longer heating times. The slopes of these two straight lines represent thereaction rate constants for mechanisms 1 and 2, respectively. However, whenthe samples were heated over a temperature range of 100 to 130°C, a first-order kinetics was observed that could correspond to the degradation of the

more resistant component (Rodrigo et al., 1997).In order to determine the kinetic model of thermal destruction of a foodcomponent during heating, traditionally two different approaches have beenused (Lenz and Lund, 1980): the steady-state approach (heating at constanttemperature, or isothermal methods), and the unsteady-state approach (heatingat a nonconstant temperature, or nonisothermal methods). The selection ofthe steady-state or unsteady-state procedure depends on the features of theheating equipment and the type of experiment being performed, i.e., whetherheating and cooling inertia time can be discounted or not.

Sadeghi and Swartzel (1990) found large differences in the values ofkinetic parameters obtained by the steady-state and unsteady-state methods.De Cordt et al. (1992) also observed differences in the parameters obtained by making an isothermal and a nonisothermal analysis. In HTST kineticstudies performed with relatively large samples, the theoretical temperatureof the assay is not the temperature of the entire sample during the heatingperiod, so that in these cases it is particularly important to consider the

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thermal profile of the sample and estimate kinetic parameters by usingunsteady-state methods. Most studies connected with the calculation ofkinetic parameters are carried out using the steady-state approach due to

the difficulty of obtaining prediction models for sample temperature profilesas a result of the natural complexity of foods. However, some researchershave used unsteady-state methods, as in the case of Svensson and Eriksson(1974), who studied thermal inactivation of lipoxygenase in the skin andcotyledons of whole peas by considering the pea divided into 17 concentricelements. Naveh et al. (1982) and Luna et al. (1986) studied thermal destruc-tion of peroxidase during blanching of corn-on-the-cob by considering thecob as a finite homogeneous cylinder, and Nasri et al. (1993) studied thermaldestruction of thiamine using a mathematical method for temperature pre-

diction based on finite differences (Nasri et al., 1993). In the case of theheating of whole asparagus it is clear that, given its characteristics, thetemperature of the spear will not be constant, at least during a good part ofthe heating and cooling. This distribution of temperatures varying withposition and time affects the sensory quality of the asparagus (texture) andits weight. Therefore, more precise unsteady-state methods are needed forthe calculation of kinetics and estimation of texture destruction and weight lossparameters. The use of mathematical heat-transfer models for estimating theevolution of temperatures inside a cylinder and the incorporation of the exper-

imentally calculated thermal properties of asparagus have made it possible toimprove the estimations of the kinetic parameters (Rodrigo et al., 1998).The data found in literature on weight loss during heating are mainly

for food of animal origin, types of meat, which generally have first-orderreaction kinetics and activation energies of the order of 13 kcal/mol for vealmuscle (Bertola et al., 1994). Rodrigo et al. (1997) studied the kinetics ofweight loss in asparagus heated between 100 and 130°C, obtaining an Ea of8.9 kcal/mol.

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