Meat Science 51 (1999) 115±121

Considerations of critical microorganisms and indicator enzymes in

connection with the pasteurization of meat products
K. Incze a,*, L. KoÈrmendy a, I. KoÈrmendy b, Gabriella ZsarnoÂczay a
a
Hungarian Meat Research Institute, 1097 Budapest, Gubacsi uÂt 6/b, Hungary
b
Department of Canning Technology, University of Horticulture and Food Industry, 1118 Budapest, MeÂnesi uÂt 45, Hungary

Received 4 October 1997; received in revised form 4 June 1998; accepted 21 June 1998

Abstract
The ®rst part of the work gives a general survey on critical microorganisms with regard to the pasteurization of meat products.
Comparison of heat resistance of two microorganisms, under isothermal conditions, is not problematic when both survivor curves
follow ®rst-order or nth order inactivation kinetics provided that reaction orders are the same. If not so or, when survivor curves
follow di€erent types of inactivation kinetics, a more complex situation arises. It is obvious that, when z-values of the microrgan-
isms to be compared di€er considerably, zA6ˆzB, the order of size of their heat resistance may be temperature dependent. The
equivalent pasteurization time (EPT) is analogous with the sterilizing (F) value, but the chosen reference temperature is below
100 C. In the present work, z and D values of various non-sporeforming microorganisms were collected from the literature, 12D
values were calculated for 60, 70 (=Tref) and 80 C and compared with those of `Str. faecalis-D' selected for basis of comparison.
Results demonstrated that, depending on temperature, Lb. viridescens, Moraxella-Acinetobacter and some members of Lance®eld D
group of streptococci appear somewhat more heat resistant than `Str. faecalis-D'. Problems of applicability of the acid phosphatase
in meat as a potential indicator enzyme when its z-value is not identical with the z value of the critical (`target') microorganism, are
also discussed. The EPT value of the entire heat processing curve, measured in the centre of the product, was calculated by the well
known Bigelow's `general method' and the above-mentioned considerations were extended to non-isothermal heating conditions.
# 1998 Elsevier Science Ltd. All rights reserved.

Nomenclature g{T} a function depending only on T [see Eq. (6)]

i (subscript) refers to the indicator micro-
d diameter of the cylindrical can (cm) organism
D decimal reduction time (min), the same at k=k{T} temperature dependent reaction rate con-
constant temperature T stant (minÿ1 or N1-n minÿ1)
Dref the same as D, but at the reference tempera- kref the same as k, but at the reference temperature
ture (min) (minÿ1 or N1-n minÿ1)
EPT equivalent pasteurization time (min) 1 length of the cylindrical can (cm)
EPTp0 EPT value recalculated from T to Tref with zp m (subscript)=measured value
(min) (see Table 2) n reaction order
fh slope index of the heating phase of the heat N concentration of surviving microorganisms
penetration curve (min) at time t (cmÿ3 or gÿ1)
fc slope index of the cooling phase of the heat No concentration of microorganisms at t=0
penetration curve (min) (cmÿ3 or gÿ1)
f{N} a function depending only on N [see Eq. (6)] N/No survivor ratio
F sterilizing value (min) as used in the canning p (subscript) refers to the acid phosphatase
industry (Tref=121.1 C) indicator enzyme
PA phosphatase units (mol phenol/1000 g test
material)
* Corresponding author. Tel.: +36-1-215-7350; fax: +36-1-215-0626. r (subscript)=required value

0309-1740/98/$Ðsee front matter # 1998 Elsevier Science Ltd. All rights reserved
PII: S0309 -1 740(98)00107 -7
116 K. Incze et al./Meat Science 51 (1999) 115±121
t time of heating under isothermal conditions
(min)
 time of heating under non-isothermal condi-
tions (min)
t{T,N} processing value (inactivation time at constant
temperature; min) when T6ˆTref. If T=Tref,
t{Tref,N}EPT
T heating temperature ( C)
T{} time dependent temperature variation ( C)
Tref reference temperature (70 C in this paper)
Tcmax maximum centre temperature attained in the
product during heat treatment ( C)
To initial temperature of ham at =0 ( C)
TR temperature of heating medium ( C)
TW temperature of cooling water ( C)
TDT thermal death time [for de®nition see Ball
and Olson, 1957)
TTI time-temperature integrator
z inverse slope of the thermal inactivation
equation representing the temperature
dependence of the t=t{T,N} relation ( C)
1. Introduction
In the pasteurization of meat products the choice of
critical microorganism (also called reference micro-
organism or indicator microorganism) has been the
object of several discussions (Reichert et al., 1988). In
principle, such microorganism should be the most heat
resistant among undesirable vegetative pathogenic bac-
teria or other microbes potentially causing spoilage,
discoloration, rancidity, o€-¯avor, etc. in meat and
meat products. It is widely accepted that in the case of
mild heat treatment below 90 C only vegetative bacteria
can be chosen for this purpose, because spores are
hardly destroyed during pasteurization. An adequate
heat treatment destroying critical microorganisms in the
product should indicate that all harmful microorgan-
isms (including viruses) are reduced to a harmless level.
This study has been mainly based on the pioneer work
of P¯ug and Christensen (1980), P¯ug (1987), Hendrickx
et al. (1995) and Van Loey et al., (1995, 1996a,b) who
presented solutions for the heat sterilization process cal-
culation problems as well as theoretical considerations
and mathematical formulae for the use of time±tempera-
ture integrators (TTIs) as thermal process evaluation
tools. Their considerations have also been adapted in this
study with special regard to canned hams and to the acid
phosphatase of meat as a possible indicator enzyme.
Furthermore, the present authors intend to deepen the
theoretical background of the concept critical micro-
organism.
We have also made use of some previous concepts
related to heat inactivation kinetics (KoÈrmendy and
KoÈrmendy, 1997).
2. Theoretical considerations
2.1. Principles when comparing the heat resistance of
di€erent microorganisms
In this paper, a general survey is given on these ques-
tions even if some of them are already known by scien-
tists specialized in thermobacteriology and thermal
processing of foods.
The heat resistance of two microbial populations is
compared: A with B, by considering ®rst an isothermal
heating pro®le, i.e. the ®ctitious situation when the
temperature of the product (T) is constant during the
entire thermal processing. (In practice, such heat treat-
ments are only used for setting up survivor curves in
laboratory circumstances.)
The classic thermal inactivation equations (Bigelow et
al., 1920; Ball and Olson, 1957; Stumbo, 1973), applied
for microorganisms A and B, are, according to the TDT
concept, as follows:
tfT; NgA
log ˆ 1=zA
…70 ÿ T† …1†
EPTA
tfT; NgB
log ˆ 1=zB
…70 ÿ T† …2†
EPTB
where z is the inverse slope of the corresponding ther-
mal inactivation Eq. (1) or Eq. (2), representing the
temperature dependence of inactivation times (proces-
sing values: t=t{T,N}).
EPT is the equivalent pasteurization time in min. This
term is analogous with the sterilizing value, F, used in
the canning industry, but EPT is related to a reference
temperature below 100 C; if T6ˆTref, the notation
t=t{T,N}, called processing value, is used instead of
EPT (EPTt{Tref,N}). N is the concentration of micro-
organisms per unit mass or unit volume, surviving the
heat treatment at time t; (No=initial concentration of
microorganisms per unit mass or unit volume at t=0).
A clear distinction has to be made between required
EPT and actual EPT of the process.
Several researchers chose 70 C as the reference tem-
perature (e.g. Reichert et al., 1979, 1988; Weng et al.,
1991; Carlier et al., 1996b).
The object of this study is also to examine the relative
heat resistance of microorganisms as a function of tem-
perature, taking account of di€erent inactivation kinetics.
Subtracting Eq. (1) from Eq. (2) and rearranging, we
obtain
tfT; NgA
log tA =tB ˆ log ˆ …1=zA ÿ 1=zB †:…70 ÿ T†
tfT; NgB …3†
‡ logEPTA =EPTB
 K. Incze et al./Meat Science 51 (1999) 115±121
The thermal resistance of a microorganism can be
de®ned as the time necessary to reach a given heat
destruction level under well determined, isothermal
conditions, therefore, Eq. (3) gives resistance ratios for
®xed N and No at di€erent temperatures (in this sense,
thermal resistance is equal to the processing value).
In the following part of this paper, conditions are
treated using a theoretical comparison of the heat resis-
tance of microorganism A with B.
When both survivor curves (A and B) follow a
straight-line semilogarithmic model i.e. ®rst-order (or
pseudo-®rst order) inactivation kinetics (P¯ug, 1987),
their comparison is easy. In this case, at T=Tref,
EPTA =EPTB ˆ Dref;A =Dref;B ˆ kref;B =kref;A …4†
where Dref and kref are the decimal reduction time and
reaction rate constant at the reference temperature.
It can be demonstrated [by substituting T=Tref and
®rst order kinetic equations into Eq. (3)] that terms in
Eq. (4) are constant for any survivor ratio, if NA/
NoA=NB/NoB.
To our best knowledge, no concrete thermal inacti-
vation process has been described so far which follows
nth order (or pseudo nth order) inactivation kinetics, if
n6ˆ1. However, in principle, one cannot exclude the
possibility of ®nding such an inactivation process in
practice (Hendrickx et al., 1995; KoÈrmendy, 1987, 1991,
1994; Taoukis and Labouza, 1989; Van Loey et al.,
1996a). Consequently, this model, as its use may be
encountered in the future, has also been included in the
discussion. When both survivor curves (A and B) follow
nth order inactivation kinetics (n6ˆ1) then, in contrast to
previous ®rst order kinetics, survivor ratio, N/No, is not
independent of No. Thus, for an unambiguous compar-
ison, No and N have to be the same for both A and B
(NoA=NoB=No and NA=NB=N).
The heat resistance ratio will be here as follows, if
T=Tref:
kref;B
…nB ÿ 1† N…1ÿnA † ÿ No…1ÿnA †
EPTA =EPTB ˆ
…5†
kref;A
…nA ÿ 1† N…1ÿnB † ÿ No…1ÿnB †
where k=k{T)=temperature dependent reaction rate
constant, n=reaction order.
If both reaction orders are the same (nA=nB), then
EPTA =EPTB ˆ kref;B =kref;A
which is analogous to the case represented by Eq. (4).
On the other hand, when reaction orders are not
identical (nA6ˆnB), then EPTA/EPTB in Eq. (5) will not
be constant, but will depend, under isothermal condi-
tions, on the chosen levels of NA=NB=N and NoA=-
NoB=No.
117
If survivor curves follow di€erent types of inactivation
kinetics, however, each model belongs to the type which
can be characterized by the relation:
t ˆ gfTg
ffNg …6†
their comparison leads to similar results as in the pre-
vious case (T=Tref) when nA6ˆnB [see Eq. (5)]. EPTA/
EPTB will also depend here on the chosen levels of
NA=NB=N and NoA=NoB=No. [In Eq. (6), t is the
heating time at constant temperature T; N is the con-
centration of survivors at time t; g{T} is a function
depending only on T; f{N} is another function depend-
ing only on N (KoÈrmendy and KoÈrmendy, 1997)]. [E.g.
the Casolari model belongs to the type represented by
Eq. (6) (Casolari, 1981; Garzaroli et al., 1996b)].
Consequently, Eqs. (1±3) are not suitable for heat
resistance comparisons if the survivor curves do not
satisfy the requirement formulated by Eq. (6), as in the
case when they have two distinct inactivation phases
[see Eq. (6) in the paper of Kamau et al., 1990]. Biphasic
curves (Hiatt, 1964), multicomponent systems (Van
Liew, 1962), log-normal heat resistance distributions
(Hiatt, 1964), the Whiting±Buchanan model (Buchanan
et al., 1994; Garzaroli et al., 1996a; Zanoni et al., 1997),
etc., also do not conform to Eq. (6). Moreover, the
classic Bigelow's `general method' (Bigelow et al., 1920;
Ball and Olson, 1957; Stumbo, 1973) cannot be used in
these cases to calculate the actual EPT by integrating
the time±temperature e€ect under non-isothermal con-
ditions. Special mathematical analysis is needed for each
concrete situation, when Eq. (6) is not valid. Simple
graphical methods were proposed to assess whether
empirical survivor curves correspond to the relation
presented by Eq. (6) (KoÈrmendy, 1966, 1982; KoÈrmendy
and KoÈrmendy, 1997; Zanoni et al., 1997).
If, for instance, EPTA>EPTB i.e. microorganism A is
more resistant than microorganism B at a constant
reference temperature, it is obvious that the reverse
conclusion (tA<tB) may be true for temperatures dif-
fering from the reference one, when zA6ˆzB (Brown,
1992; Gaze, 1992). This is a logical consequence which
can be derived from Eq. (3).
In practice, however, where temperature of the heat
treated product is never constant during processing,
called non-isothermal heating pro®le by Hendrickx et
al. (1995) and Van Loey et al., (1995, 1996b), all these
considerations concern the time±temperature history,
measured often in the central area (cold zone).
3. Comparison of the heat resistance of microorganisms
based on data from the literature
z and D values for numerous microorganisms: `Str.
faecalis D' (Reichert et al., 1979, 1988; Michalski, 1995),
118 K. Incze et al./Meat Science 51 (1999) 115±121

Str. faecalis P-2A (Magnus et al., 1988), Str. faecalis
var. zymogenes (MuÈller, 1989), Str. faecium E-20 (Hou-
ben, 1982; Magnus et al., 1988), Str. faecium P1-A
(Magnus et al., 1988), E. coli 262 (Wojciechowski,
1980), E. coli O157:H7 (Doyle and Schoeni, 1984),
Micrococcus radiodurans R1 (Duggan et al., 1963),
Moraxella-Acinetobacter (Firstenberg-Eden et al.,
1980), Leuconostoc spp., coagulase positive Staph. aur-
eus, Lactobacillus spp., Salmonella spp., Salmonella
senftenberg, Mycobacterium tuberculosis, Brucella spp.
and Coxiella burnetti (Stumbo, 1973), `Lactobacilli' and
`Micrococci' (Reichert et al., 1979), Lb. viridescens
NCIB 8965 (Milbourne, 1983), Y. enterocolitica serotype
O:8 (Shenoy and Murano, 1996), L. monocytogenes
(Linton et al., 1990; Carlier et al., 1996a), Aerococcus
viridans (Incze, 1963) and C. botulinum type B strain
KAP 5 spores (Juneja and Eblen, 1995), were collected
from the literature.
Owing to the considerable in¯uence of various factors
on D and z, such as large experimental error, composi-
tion of heating menstruum, age of culture, sublethal
heat shock, etc. (Filppi and Banwart, 1974; Skinner and
Hugo, 1976; Druesne, 1996), for lack of more reliable
data, these values should be handled with criticism and
caution.
For example, data for Aerococcus viridans were
obtained in broth and not in meat (Incze, 1963). Fur-
thermore, z values were often extrapolated from the
experimental temperature range. D70 values, if not indi-
cated in the corresponding paper, were calculated with
the help of the respective z-value, from D55, D60, etc.,
values. If data were available, increased thermo-
tolerance caused by sublethal heat shock was also taken
into account. [Unfortunately, we could not ®nd survivor
curves for FMD-virus from the literature (Csapo and
KoÈrmendy, 1996)].
12D values of the above listed microorganisms were
calculated from 70 to 60 and 80 C and compared with
those of `Str. faecalis D', serving as reference basis
(Reichert et al., 1979, Reichert et al., 1988). The z values
of these microorganisms varied from 2.9 C (Str. faecalis
var. zymogenes) to 38.5 C (Lb. viridescens; the latter
value has been accepted with a certain scepticism by
some microbiologists). [The EPT=12D70=1392 min
value of C. botulinum type B, KAP B5 spores (Juneja
and Eblen, 1995) was also included in the calculations].
Calculations were carried out in the following manner:
. The EPT values (Tref=70 C), assuming ®rst-order
inactivation kinetics, were taken for 12D70 and
were considered arbitrarily as required equivalent
pasteurization times for the inactivation of the
respective microorganisms.
. Processing values, t{T,10ÿ12No), were converted
from Tref=70 C to T=60 C and 80 C with the
help of equation
logtfT; 10ÿ12 No g ˆ 1=z:…70 ÿ T† ‡ logEPT …7†
Eq. (7) comes from Eq. (1) or (2); substitution
N=10ÿ12No means N/No=10ÿ12 survival ratio has been
chosen.
Processing values, under isothermal conditions, (at
60, 70 or 80 C), exceeding those of the basis of com-
parison (`Str. faecalis D'), can be seen in Table 1.
4. Problems concerning critical microorganisms and
indicator enzymes
Reichert et al., (1979, 1988) and also Martin, (1984,
1996) proposed the use of `Str. faecalis D', with
zi=10 C, as the critical (indicator) microorganism in
the heat treatment of semi-preserved meat products,
assuming that this one is the most heat resistant among
potentially harmful vegetative bacteria occurring in
meat. [However, higher z and D values, exceeding those
of Reichert et al., (1979, 1988), were recently found also
by Fery et al. (1995) for Enterococcus faecalis].
On the other hand, the acid phosphatase of meat with
zp=6.94 C, corresponding to the condition presented

Table 1
Processing values (EPTt{70 C,10ÿ12No}, t{60 C, 10ÿ12No} and t{80 C, 10ÿ12 No}) of microorganisms exceeding those of `Str. faecalis D' under
isothermal conditions

Microorganisms EPTt{70 C, 10ÿ12No} z t{60 C, 10ÿ12No} t{80 C, 10ÿ12No}

(min) ( C) (min) (min)

`Str. faecalis D' (basis of comparison) 36 10 360 3.6

Str. faecium P1-A 95a 7.46 2074a 4.3a
Str. faecium E-20 56a 7.46 1237a 2.6
Str. faecalis var.zymogenes 0.55 2.9 1549a 1.9710ÿ4
Moraxella-Acinetobacter 55a 7.7 915a 2.31
Lb. viridescens NCIB 8965 200a 38.5 364a 110a
C. botulinum type B strain KAP5B spores 1392a 9.21 16960a 114a
a
If t{T, 10ÿ12No} is greater than the corresponding processing value of the reference microorganism `Str. faecalis D', a ®ctitious isothermal `Str.
faecalis D cook' would be, in principle, insucient to fully inactivate the given microbe.
 K. Incze et al./Meat Science 51 (1999) 115±121 119

by Eq. (6) has been proposed as a potential indicator
enzyme for determining the extent of heating in the
central area of canned hams (Lind, 1987; KoÈrmendy et
al., 1987, 1992, 1995; Cattaneo and Lorenzi, 1994).
(Alternative TTIs can also be applied for this purpose;
see, e.g. Blackwell, 1996; Ang et al., 1996). Therefore,
according to the classi®cation of Hendrickx et al. (1995)
and Van Loey et al. (1996a), the acid phophatase
enzyme of meat can be considered here as a post fac-
tum, single component, intrinsic, enzymatic time-tem-
perature integrator and the `target attribute' will be the
thermal inactivation of `Str. faecalis D' with zi=10 C
and EPTi=80 min. [The latter value, regardless of
exceeding 12D, has been chosen for practical con-
siderations (Fery et al., 1995; KoÈrmendy et al., 1992)].
It was established that, by heating cured hams in very
thin pouches at a constant temperature of 70 C, for
80 min, under isothermal conditions, the mean residual
acid phosphatase activity was PA=628 units (KoÈr-
mendy et al., 1992). Neglecting mathematical statistical
considerations we could simply say that, if this value is
considered as a limit value, PA>628 would mean that
the ham is `undercooked' and PA<628, that it is `over-
cooked'. Consequently, if the residual phosphatase
activity in the central area of a ham is equal or less than
PA=628 units, the presumed requirement for a `su-
cient' heat treatment, referred to 70 C constant tem-
perature, is ful®lled.
By substituting the respective z values (10 and 6.94 C)
in Eqs. (1) and (2), it can easily be seen that, with a ®c-
titious isothermal equivalent heat treatment at 60 C, the
real processing value of the ham will be underestimated
with the phosphatase assay, i.e. the ham appears to be
erroneously `undercooked' (see also Table 2).
Nevertheless, at 80 C, the `real' processing value will
be overestimated with the phosphatase assay, i.e. the
ham appears to be erroneously `overcooked' (see
Table 2).
Needless to say that, in practice, with the control of
the extent of heating of meat products, overestimation is
much more dangerous than underestimation.
5. Materials and methods
Cured hams and picnics were prepared from lean
pork with 10±15% brine addition (containing NaCl,
Na5P3O10, NaNO2 Na-ascorbate and sucrose) in a
Hungarian meat enterprise, in the usual way, applying a
tumbling procedure. The cured raw materials were then
packed in rectangular (oblong and pullman), pear-
shaped and cylindrical cans of various sizes (Table 3)
and they were submitted to water bath pasteurization in
a cook tank at constant temperature, TR. Heat pene-
tration curves were registered with thermocouples (Tes-
toterm GmbH, Lenzkirch, Germany) in the central area
of the product. The main heat treatment parameters of
some products are shown in Table 3.
It has long been known that, when temperature of the
heated product is changing with time , T=T{}, the
actual EPT value of the entire heating process, includ-
ing the cooling phase, can be calculated by Bigelow's
`general method' (Bigelow et al., 1920; Ball and Olson,
1957; Stumbo, 1973). The integration can be performed
numerically. The computer program of ZukaÂl (1996)
has been used for this purpose. In this way, EPT values
of the entire heat treatment (including the cooling
phase) were calculated with the help of z values (lying

Table 2
In¯uence of heating temperature (T; under isothermal conditions) and z value ( C) of the critical microorganism (zi) and indicator enzyme (zp) on
EPT values (EPTi and EPTp0 ), when EPTi=EPTp at Tref=70 C. (Source: Van Loey et al., 1995)

T zi>zp zi<zp

T<Tref EPTi>EPTp0underestimation EPTi<EPTp0 overestimation

T>Tref EPTi<EPTp0 overestimation EPTi>EPTp0 underestimation

EPTp0 =EPT value recalculated from T to Tref with zp.

Table 3
Main heat treatment characteristics of canned hams and ham patties used in the experiments

Serial number Type Can size (cm) TR To Tcmax Tw

1 Oblong can (12 lb) 10.316.932.3 74 7±9 70 12±14

2 Pullman can (8 lb) 101037 76 5±9 70 12±14
3 Pullman can (8 lb) 101037 81 5±9 72 12±14
4 Pear-shaped can (3 lb) 6.914.819.3 78 5±10 73 12±14
5 Cylindrical can (4 lb) d=9.9; 1=24.3 78 5±10 72 12±14
6 Cylindrical can (12-oz) (Ham patties) d=9.9; 1=5.5 74 7±9 72 12±14
7 Cylindrical can (12-oz) (Ham patties) d=9.9; 1=5.5 76 5±10 74 12±14

TR=temperature of heating medium,  C (water); To=initial temperature ( C) of ham at =0; Tcmax= maximum centre temperature ( C) in the
ham attained during cooking; Tw=temperature ( C) of cooling water; d=diameter; 1=length.
120 K. Incze et al./Meat Science 51 (1999) 115±121

Table 4
EPT values of critical microorganisms not having reached the `required' level (12D70) during heat treatment (products have been listed in Table 3).
Results obtained for `Str. faecalis D' and for acid phosphatase are also presented

Serial number from Table 3 1 2 3 4 5 6 7

Critical microorganism EPTr EPTm EPTm EPTm EPTm EPTm EPTm EPTm

Str. faecium P1-A (z=7.46 C) 95 80 53 79 69 79 68 90
Lb. viridescens NCIB 8965 (z=38.5 C) 200 175 93 87 68 90 73 68
C. botulinum type B strain KAP 5 1392 90 58 76 66 78 67 81
spores (z=9.21 C)
`Str. faecalis D' (z=10 C) 36 94 60 76 65 78 67 78
Acid phosphatase (z=6.94 C) 80? 77 52 81 70 80 69 94

EPTr=12D70=EPT required (min); EPTm=EPT measured (min); Tref=70 C.

between 2.9 C and 38.5 C) of the previously listed
microorganisms and results were compared with the
`required' EPT (12D70) values (see Table 4). The z value
of the acid phosphatase inactivation in meat was also
included in the calculations (KoÈrmendy et al., 1992).
6. Results and discussion
Results of experiments described in Materials and
methods and shown in Table 4 suggest the following
conclusions:
. As seen in Table 4, beside C. botulinum type B
strain KAPS spores, the applied heat treatments
were insucient to reach the `required' 12D70
values for Str. faecium P1-A and L. viridescens
NCIB 8965.
. The phosphatase assay (with zp=6.94 C) slightly
underestimates (see cans with serial numbers 1 and
2; Tcmax=Tref) or slightly overestimates (see cans
with serial numbers 3, 4, 5, 6, 7; Tcmax>Tref) the
integrated EPT value obtained with `Str. faecalis,
D' (with zi=10 C).
. Integrated EPT values are either steadily increas-
ing (see cans with serial numbers 1 and 2) or
decreasing (see can with serial number 7) or pass
through a minimum (see cans with serial numbers
3, 4, 5 and 6) in function of z. This is because,
under industrial heat processing conditions, the
slope indices of the heating and cooling curves are
not equal (|fh|6ˆ|fc|) and the cooling lags are also
rather variable. Consequently, the cooling phase
of these empirical heat processing curves, repre-
senting 30±50% of the entire EPT in our experi-
ments, does not follow the known mathematical
model derived from the Fourier equation (Stumbo,
1973). Consequently, following the guideline in
Table 2 and comparing Tcmax to Tref (Van Loey et
al., 1996b), one cannot predict with certainty in
every case whether underestimation or over-
estimation will occur. If Tcmax was equal or less
than Tref=70 C, EPTz=6:94 was always below
EPTz=10. On the other hand, if Tcmax exceeded
Tref=70 C, EPTz=6:94 was often, but not always,
slightly greater than EPTz=10.
. For Lb. viridescens, assuming that z=38.5 C, the
gap between EPT required (EPTr=12D70) and
actual EPTm of the process, except for serial
number 1, is very large: EPTm << EPTr .
. As also seen in Table 1, in principle, Str. faecium
P1-A (Magnus et al., 1988) and Lb. viridescens
NCIB 8965 (Milbourne, 1983), related to the same
surviving ratio, seem to be more heat resistant
than `Str. faecalis D' (Reichert et al., 1979, 1988)
under heat treatment conditions used for pasteur-
ization of canned hams. (Considerations on prac-
tical importance of this ®nding falls beyond the
scope of this paper.)
7. Conclusions
As Hendrickx et al. (1995) and Van Loey et al.
(1996a,b) pointed out, zTTI should be as near as possible
to ztarget. It is clear that, in principle, the true zTTIzp
(or energy of activation, Ea) of the acid phosphatase of
meat is a given value and cannot be varied like the z-
value of some extrinsic TTIs (Weng et al., 1991). On the
contrary, the measured (apparent) z value of the acid
phosphatase of meat seems to depend on assay condi-
tions (pH value, initial substrate concentration), due
presumably to a `heat treatmentisoenzymemethod',
interaction (KoÈrmendy et al., 1987; KoÈrmendy et al.,
1992). However, the apparent z value of this enzyme (zp)
could hardly be adjusted to ztargetzi by manipulating
assay conditions. As seen in Table 4, since zp<ziztarget,
underestimation or overestimation of the EPTi
EPTtarget has to be expected with the phosphatase assay
in canned hams; the former being more favourable than
the latter. As long as EPT and z values for the FMD
virus and other exotic viruses are not available, the
possible choice of `Str. faecium P1-A (with z=7.46 C)
for critical microorganism, instead of `Str. faecalis D'
 K. Incze et al./Meat Science 51 (1999) 115±121
(with z=10 C), could noticeably reduce the gap
between zp and zi.
Special care has to be taken to reach the required
EPT in the case of small sized products, having a steep
core temperature rise during heating; one but not the
sole possibility would be the extension of the cooling
phase. The above considerations strongly suggest that
heat processing conditions of pasteurized canned pro-
ducts must be carefully planned; each type of product
needs special examination in this respect.
Acknowledgements
The authors are grateful to Mr. E. ZukaÂl for prepar-
ing the computer program for heat treatment equivalent
calculation. A part of this research work has been
sponsored by the National Funds of Scienti®c Research
(Hungarian Academy of Sciences), Code T014965.
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