International Journal of Food Microbiology 100 (2005) 187 – 196

www.elsevier.com/locate/ijfoodmicro

Basis of predictive mycology

Philippe Dantigny*, Audrey Guilmart, Maurice Bensoussan
Laboratoire de Microbiologie, ENS.BANA, UMR INRA 1232-Université de Bourgogne, 1 Esplanade Erasme, F-21000 Dijon, France
Received 27 September 2004; accepted 6 October 2004

Abstract

For over 20 years, predictive microbiology focused on food-pathogenic bacteria. Few studies concerned modelling fungal
development. On one hand, most of food mycologists are not familiar with modelling techniques; on the other hand, people
involved in modelling are developing tools dedicated to bacteria. Therefore, there is a tendency to extend the use of models that
were developed for bacteria to moulds. However, some mould specificities should be taken into account. The use of specific
models for predicting germination and growth of fungi was advocated previously [Dantigny, P., Guilmart, A., Bensoussan, M.,
2003. Basis of predictive mycology. In Proceedings of the 4th International Conference of Predictive Modelling in Foods.
J.F.M. VanImpe, A.H. Geeraerd, I. Leguérinel, P. Mafart (Eds), 15_19 June, Quimper, pp 117_119.]. This paper provides a short
review of fungal modelling studies.
D 2004 Elsevier B.V. All rights reserved.

Keywords: Predictive model; Mycology; Mould; Fungi

1. Introduction Rauha, 1978). Another estimate from one bakery

Due to the appearance of visible hyphae and
production of unpleasant odours, fungal spoilage
of food causes economic losses. It is very difficult
to assess losses attributable to moulds. In the
baking industry, these losses varied between 1%
and 3% of products depending on season, type of
product and method of processing (Malkki and
* Corresponding author. Tel.: +33 380396671; fax: +33
380396640.
E-mail address: phdant@u-bourgogne.fr (P. Dantigny).
0168-1605/$ - see front matter D 2004 Elsevier B.V. All rights reserved.
doi:10.1016/j.ijfoodmicro.2004.10.013
in the US was 5% losses (Killian and Krueger,
1983). Unfortunately, no more recent data are
available. Although industrial standards have been
upgraded, food spoilage by fungi is still of great
concern. In addition, it was reported that 25% of
agriculture products are contaminated with myco-
toxins (Mannon and Johnson, 1985). Mycotoxin
ingestion by humans, which occurs mainly through
plant-based foods and the residues and metabolites
present in animal-derived foods, can lead to
deterioration of liver or kidney function (Sweeney
and Dobson, 1998) and therefore constitutes a risk
for human health. For example, aflatoxin is an
188 P. Dantigny et al. / International Journal of Food Microbiology 100 (2005) 187–196
extremely potent hepatotoxic and hepatocarcinogenic
agent (Borker et al., 1966). Mycotoxicosis was
obtained with rats fed with aflatoxin B1 (1 mg/kg)
for 1–15 consecutive days (Leszkowicz et al., 1999).
It has been demonstrated that the interaction between
DNA and toxin is the key step in cancerogenesis. In
addition, there is some evidence that another myco-
toxin (ochratoxin A) is related to endemic nephrop-
athy in the Balkans.
In order to improve food quality and safety, there is
a need for a tool allowing prediction of fungal
development. For 20 years, predictive microbiology
has been developed for predicting the occurrence of
food-borne pathogens, although these tools are
dedicated to bacteria. This paper develops the basis
of Tpredictive mycologyr that takes into account
mould specificities.
2. Mould specificities
Fungal growth involves germination and hyphal
extension, eventually forming mycelium. Spores are
widely disseminated in the environment, and they
are principally responsible for spoilage. Under
favourable conditions, spores will swell. Thereafter,
when the length of the germ tube is between one
half and twice the spore diameter (depending on the
source), the spore is considered to have germinated
(see Fig. 1).
Germination can be considered as the main step to
be focused on, because a product is spoiled as soon as
visible hyphae can be observed. However, few studies
have concerned germination kinetics. This shortage
can be explained by the difficulties of acquiring
sufficient, reproducible data. In fact, this kind of
study requires microscopic observation for evaluating
the length of the germ tube. Moreover, observations
and measurements should be carried out without
opening the dishes (Magan and Lacey, 1984) and
experimental devices should be developed for this
purpose (Sautour et al., 2001a,b). In contrast, more
work was dedicated to the measurement of hyphal
extension rate, which is usually reported as radial
growth rate (mm day
1).
Due to their ability of dividing, bacteria form
single cells and they can be easily enumerated
especially in liquid broth. In such a case, and at high
Phialide
Metula
Fig. 1. Life cycle in P. chrysogenum. Propagation occurs by means of
conidia that are produced in chains from a specialized cell (phialide).
Under favourable conditions, conidia (spores) are initiating germ
tubes eventually forming mycelium visible at the naked eye. New
conidia are borne from fertile hyphae (conidiophore).
cellular densities, bacterial growth can be estimated
automatically, for example, by using bioScreenR
device based on turbidity measurements. At lower
cellular densities and in solid media, CFU/g or CFU/
ml can be determined.
In contrast, moulds are forming mycelium whose
weight, except at the early stage of growth, does not
increase exponentially (Koch, 1975). It is therefore
useless to determine the weight of the mycelium for
estimating a growth rate parameter. In addition, it is
impossible to split the mycelium into individual cells.
Therefore, the CFU method can be applied to the
enumeration of spores only, (Vindeløv and Arneborg,
2002).
Temperature (T) is the main factor for controlling
bacterial growth, but the effect of water activity (a w)
on mould growth is more important than T (Holm-
quist et al., 1983). Oxygen is necessary for the growth
of food spoilage fungi. Therefore, the use of modified
atmospheres to prevent fungal growth and mycotoxin
production was evaluated to extend the shelf life of
some kinds of food (El Halouat and Debevere, 1997;
Taniwaki et al., 2001).
 P. Dantigny et al. / International Journal of Food Microbiology 100 (2005) 187–196 189

3. Associated mycoflora on foods and feeds less than 0.90. Almost all xerophilic fungi are
ascomycetes. The most common causes of spoilage
With respect to food spoilage, three important of dried cereals are Eurotium species (Pitt and
groups of fungi can be distinguished: Zygomycetes Hocking, 1999). However, deuteromycetes such as
(class), ascomycetes (subkingdom Ascomycotina) and Wallemia sebi and Aspergillus penicillioides are also
deuteromycetes (subkingdom Deuteromycotina). xerophilic, capable of rapid growth above about
From the food spoilage point of view, the outstanding 0.77 a w and of slow growth at 0.75 a w and
properties of Zygomycetes are: very rapid growth below—down to about 0.68 a w. Most of the cited
(generally greater than 10 mm day
1 at optimum moulds exhibited T min close to the freezing point. In
conditions, Table 1), inability to grow at lower water contrast, A. flavus was characterised by T min about
activities (no Zygomycetes are xerophiles); and lack 10 8C. The genus Aspergillus is typical, growing
of resistance to heat and chemical treatments. Zygo- readily at temperatures between 15 and 40 8C,
mycetes have rarely been reported to produce thereby responsible for many contaminations in
mycotoxins (Pitt and Hocking, 1999). tropical countries.
In contrast to Zygomycetes, ascomycetes and Ascospores are highly condensed, refractive spores,
deuteromycetes exhibit septate mycelium. Although which are often resistant to heat and chemicals.
it is out of the scope of this paper, the ascomycete– Ascomycetes (e.g., Byssochlamys species, Eupenicil-
deuteromycete connection should be mentioned. lium lapidosum, Neosartorya fischeri, Talaromyces
Many fungal species carry the genetic information to species) with ascospores of very high heat resistance
produce both ascospores (teleomorph state) and which can survive heat processing are responsible
conidia (anamorph state). For example, Byssochlamys for spoilage of pasteurized foods (see Table 2).
fulva is the teleomorph, Paecilomyces fulvus the Lacking ascospores, deuteromycetes are not usually
anamorph. heat-resistant, but conidia may be quite resistant to
Temperature and water activity limits for growth chemicals.
of some moulds are reported in Table 1. None of Fruits are usually quite acid, in the range pH 1.8–
the moulds cited was shown capable of growth below 2.2 (lemons) to 4.5–5.0 (tomatoes) and are quite
0.80 a w with the notable exception of Aspergillus resistant to invasion to bacteria. Therefore, microbial
flavus and Penicillium chrysogenum. In contrast, spoilage of fruit and fruit products is almost always
Zygomycetes such as Rhizopus and Mucor species, caused by fungi (Pitt and Hocking, 1999). Most
but also some deuteromycetes such as Fusarium and Penicillia can develop as low as pH 2 (Panasenko,
Trichoderma species, usually did not develop at a w 1967) and are fruit contaminants (Table 2). By far
the most common causes of citrus fruit decay
throughout the world are the Penicillium rots due
to Penicillium italicum and Penicillium digitatum,
Table 1
termed blue rot and green rot, respectively (Pitt and
Optimum conditions (on Potato Dextrose Agar medium) and limits
for growth of some moulds (from Sautour et al., 2002) Hocking, 1999).
Moulds l opt Topt a w(opt) T min a w(min)
Genera such as Aspergillus and Penicillium are
(mm (8C) (8C) of paramount importance in food spoilage. The
day
1) prevalence of one genus as compared to the other
Alternaria alternata 4.8 25 0.985 (
5) – 0 0.85 – 0.89 one is related to temperature. Penicillia are capable
Aspergillus flavus 9.7 31 0.970 6–8, 10–12 0.78 – 0.85 of developing and produce toxin at lower temper-
Cladosporium 4.4 25 0.985 (
5) – (
4) 0.84 – 0.88 atures than Aspergillii. In fact, many strains
cladosporioides belonging to these genera are responsible for
Mucor racemosus 13.3 25 0.985 (
4) – (
1) 0.91 – 0.94
Penicillium 4.6 25 0.985 (
4), 4 0.78 – 0.85
production of toxic metabolites: aflatoxin B 1
chrysogenum (AB1), ochratoxin A (OTA), citrinin (CIT), patulin
Rhizopus oryzae 56.8 35 0.985 2, 7–9 0.88 – 0.89 (PAT) and penicillic acid (PA). Namely, the main
Trichoderma 19.6 25 0.990 4 –5 0.91 moulds responsible for mycotoxins production are:
harzianum A. flavus (AB1), Aspergillus ochraceus (OTA, PA),
190 P. Dantigny et al. / International Journal of Food Microbiology 100 (2005) 187–196

Table 2
Associated mycoflora on foods and feeds
Mould Type of food and raw products
Cereals Nuts FVeg Spic MEgg Fish Fats Chee BrPa LWAF PasF
Fiel Stor AciP AirS
Alternaria alternata þ
Alternaria spp. þ
A. candidus þ þ þ
A. flavus þ þ þ þ þ þ
A. fumigatus þ
A. niger þ þ
Aspergillus ochraceus þ
A. penicilloides þ
A. restrictus þ þ
A. sydowii þ
A. tamarii þ
A. terreus þ
A. versicolor þ þ þ þ þ
A. wentii þ
Byssochlamys fulva** þ þ
B. nivea** þ þ
Chrysosporium farinicola þ
C. fastidium þ
C. inops þ
C. xerophilum þ
Cladosporium spp. þ þ
Eupenicillium lapidosum** þ
Eurotium amstelodami** þ
E. chevalieri** þ
E. herbariorum** þ þ
Eurotium spp.** þ þ þ þ þ þ
Eremascus albus** þ
Er. Fertilis** þ
Fusarium moniliforme þ
Fusarium spp. þ þ
Mucor circinelloides* þ
Mucor racemosus* þ
Mucor spp.* þ
Neosartorya fisheri** þ
Paecilomyces variotii þ
Penicillium aurantigriseum þ þ
P. brevicompactum þ þ þ
P. citrinum þ þ
P. commune þ þ þ þ þ
P. crustosum þ þ þ þ
P. chrysogenum þ þ
P. digitatum þ
Penicillium discolor þ
P. echinulatum þ þ
P. expansum þ
P. funiculosum þ
P. glabrum þ þ
P. glandicola þ
P. hirsutum
P. hordei þ
P. islandicum þ
 P. Dantigny et al. / International Journal of Food Microbiology 100 (2005) 187–196 191

Table 2 (continued)
Mould Type of food and raw products
Cereals Nuts FVeg Spic MEgg Fish Fats Chee BrPa LWAF PasF
Fiel Stor AciP AirS
P. italicum þ
P. nalgiovense þ
P. oxalicum þ
P. purpurogenum þ
P. roqueforti þ þ þ þ þ
P. smithii þ
P. solitum þ þ þ þ
P. thomii þ
P. variabile þ
P. verrucosum þ þ þ þ
P. viridicatum þ
Polypaecilum pisce þ þ
Rhizopus oryzae* þ
Rhizopus stolonifer* þ
Rhizopus spp.* þ
Scopulariopsis brevicaulis þ
S. candida þ þ
S. halophica þ
S. fusca þ
Scopulariopsis spp. þ
Talaromyces þ
bacillisporus**
T. macrosporus** þ
Xeromyces bisporus** þ
Wallemia sebi þ þ
Cereals also included corn, peas and beans (Fiel, under field conditions; Stor, stored; AciP, acid preserved; airtight storage); Nuts; FVeg, fruits
and vegetables; Spic, spices; MEgg, meat and eggs; Fish (mostly dried); Fats (margarine, etc...); Chee, cheese and related products; BrPa, bread
and pastries; LWAF, low water activity foods; PasF, pasteurized foods. Zygomycetes (*), ascomycetes (**). (Adapted mainly from Northold et
al. 1995).

Aspergillus parasiticus (AB1), Aspergillus terreus Penicillium verrucosum (OTA, CIT) and Penicillium
(PAT), Penicillium citrinum (CIT), Penicillium viridicatum (OTA, CIT, PA) (Frisvad and Thrane,
expansum (CIT, PAT), Penicillium patulum (PAT), 1995).

4. Models

4.1. Primary models

4.1.1. Inactivation models

The inactivation of spores was modelled by a classical first order equation:

dN =dt ¼
kN ð1Þ
where N is the number of surviving spores after treatment (cfu/ml), t is the time (min) and k is an inactivation
rate (min
1). Inactivation is described in an analogous way of the Bigelow model (Bigelow, 1921). The D value
(min) or decimal reduction time is the time that is needed to inactivate 90% of the spores at a given
temperature, D=(ln10)/k. The z value (8C) is the temperature increase required to have a 10-fold increase of the
D value.
192 P. Dantigny et al. / International Journal of Food Microbiology 100 (2005) 187–196

Ascospores are fairly resistant to heat treatment. Some ascomycetes can be ranked by a decreasing order of the
heat sensibility of their spores: B. fulva D 90=1.3–15 min, buffer pH 3.6, 168Brix (Bayne and Michener, 1979);
Talaromyces flavus D 88=7.8 min and N. fischeri D 88=1.4 min, apple juice (Scott and Bernard, 1987);
Byssochlamys nivea D 88=0.75–0.8 min, buffer pH 3.5 (Casella et al., 1990); and Eurotium herborarium
D 70=5.5 min, grape juice, 658Brix (Splittstoesser et al., 1989).
Conidiospores of deuteromycetes are more heat-sensitive than ascospores, Aspergillus niger D 59=3.3 min
(Baggerman and Samson, 1988), Botrytis cinerea D 45=2.6 min and Monilinia fructigena D 45=0.9 min (Marquenie
et al., 2002). The combinations of pulsed white light and UV-C or mild heat treatment to inactivate conidia of B.
cinerea and Monilia fructigena were modelled by a dynamic model consisting of two autonomous coupled
differential equations (Marquenie et al., 2003).

4.1.2. Germination models

The germination of spores of Fusarium moniliforme (Fusarium verticillioides) as a function of time was first
studied at different a w (Marı́n et al., 1996). The percentage of germination vs. time was modelled with the
modified Gompertz equation. In contrast to bacteria when the initial load N o is a critical parameter to be estimated,
the initial percentage of germination was always equal to 0%. The asymptotic value where the germination rate
becomes constant was 100% in most cases.
The percentage of germination can also be considered as the probability to have a single spore germinated.
Accordingly, the logistic function which is usually dedicated to probabilistic models:

P ¼ Pmax =ð1 þ expðk ðs
t ÞÞ ð2Þ

was used for describing the germination kinetics of Mucor racemosus (Dantigny et al., 2002). The parameter
P max was substituted for 100 because all spores were capable of germinating. In the objective of designing a
secondary model, the parameters of the logistic function can be expressed as a function of environmental
factors. The rate factor k was constant whatever the temperature, whereas s (time where P=P max/2) was
more discriminative. At present, no comparative study between both models is available. However, according
to our set of data (unpublished results), the logistic function seems to perform better than the Gompertz
equation.

4.1.3. Growth models

The primary model developed by Baranyi et al. (1993) was adapted to fit colony diameter growth curves of
Penicillium roqueforti (Valı́k et al., 1999), A. flavus (Gibson et al., 1994) and Penicillium brevicompactum
(Membré and Kubaczka, 2000). However, the radial growth rate (mm day
1) can also be calculated by a simple
linear model with breakpoint (see Fig. 2):

r ðmmÞ ¼ lðt
kÞ ð3Þ

It appeared a very simple but also very precise measurement, the regression coefficients being greater than 0.99.
Therefore, it is unlikely that other models such as those of Baranyi or Gompertz would demonstrate superiority
over the linear correlation. In addition, the parameters l and k can be obtained even when the Petri dish is not
entirely covered with mycelium. For example, the radial growth rate at 0.89 a w can be calculated after 2 weeks
whereas the radius of the colony was only about 10 mm (Fig. 2). In addition, early measurements of diameter of
the colony improve the accuracy of the lag period because this parameter is obtained by extrapolation of the
straight line. The lag time for growth has no biological significance because its calculation results from
macroscopic observations of mycelium. However, under carefully controlled inoculum, it was shown with M.
racemosus that the lag time defined as below coincided with the completion of the germination process, say more
than 99% of germination (Dantigny et al., 2002).
 P. Dantigny et al. / International Journal of Food Microbiology 100 (2005) 187–196 193

Fig. 2. Radial growth rate, l and lag time, k of P. chrysogenum grown on Potato Dextrose Agar medium at 25 8C, 0.97 a w (n), 0.92 a w (E) and
0.89 a w (.) (redrawn from Sautour, 2001).

In contrast to the percentage of germination, the lag time depends on the number of inoculated spores, but no
effect was noticed on the radial growth rate. The lag time decreases with increasing number of spores inoculated at
the same spot. This could be explained, because a large inoculum will form a colony more rapidly than a small one
(Sautour et al., 2003). The initial number of spores should be taken into account into the set of equations of models
describing fungal growth.

4.2. Secondary models

The influence of environmental factors (water activity, temperature, pH) on germination was assessed
previously for different a w depressants (Sautour et al., 2001a,b). A response surface methodology illustrates how
the germination time can be predicted (Fig. 3). pH, which is usually associated to other environmental factors to
prevent bacterial growth, has no marked influence on mould germination and growth in the range 4–6.5 (Magan
and Lacey, 1984). Water activity had a greater effect on mould development than temperature, whereas an
interactive effect between T and a w was noticed.
The effects of temperature and water activity on growth rate of food spoilage moulds were compared using
normalised variables: l dim, T dim and a w(dim) within Belehrádek-type equations: l dim=[T dim]a and l dim=[a w(dim)]b
(Sautour et al., 2002). It was reported that the moulds studied were characterised by a values ranging from 0.81 to
1.54 and b values from 1.50 to 2.44.
Due to the lack of specific models for moulds, there is a tendency to apply models that have been developed for
bacteria. For example, the square-root model was used to describe the effect of T on the growth of Rhizopus
microsporus (Han and Nout, 2000). It is clear that the effect of the temperature on moulds cannot be modelled by
the square-root model because of a values close to 1. It has been demonstrated that the use of the square-root
model when a is less than 2 leads to under-estimation of T min (Dantigny and Molin, 2000). Similarly, some doubt
can be raised with the use of the cardinal model with inflexion, CMI, described by Rosso et al. (1993) for
describing the effect of T on fungal growth rate. For example, a T min value, as low as
12 8C, has been reported
for P. roqueforti using the CMI model (Cuppers et al., 1997).
194 P. Dantigny et al. / International Journal of Food Microbiology 100 (2005) 187–196

Fig. 3. Contour plot of the influence of water activity and temperature at pH 5 on time T 90 to obtain 90% of the conidia of P. chrysogenum
germinated on Yeast Nitrogen Base-Glucose Agar medium for glycerol as humectant (from Sautour et al., 2001b).

Contrarily, the CMI model was used satisfactorily for describing the effect of a w on fungal growth rate, l (mm
day
1) (Rosso and Robinson, 2001; Sautour et al., 2001c), as suggested by the b values close to 2.

2
lopt aw
awðmaxÞ aw
awðminÞ
l¼




 ð4Þ
awðoptÞ
awðminÞ awðoptÞ
awðminÞ aw
awðoptÞ
awðoptÞ
awðmaxÞ awðoptÞ þ awðminÞ
2aw

where l opt (mm day
1), radial growth rate at optimum conditions, a w(opt), water activity at which l=l opt, a w(min)
and a w(max), minimum and maximum water activities, respectively, at which no growth is observed.
It should be noted also that in contrast to previous model described by Gibson et al. (1994), the CMI model
allows an estimation of a w(min) which is not easily determinable because fungal growth can well occur after several
months of incubation.

5. Perspectives should be focused on spore germination. Although

In the objective of modelling fungal kinetics, the
tools that were developed for bacteria can be used,
but mould specificities should be taken into account.
As a primary step of fungal development, attention
no definition of the germination time is widely
accepted, this variable provides a pertinent insight on
how fast spores are germinating. In order to
determine accurately this variable, spore germination
kinetics should be monitored thus leading to regular
 P. Dantigny et al. / International Journal of Food Microbiology 100 (2005) 187–196
microscopic observations and development of spe-
cific experimental setup.
Fungal growth, which is usually reported as radial
growth rate, can be easily determined by macroscopic
observations. The linear section of the graph can be
extrapolated to a zero increase in diameter and the
intercept on the time axis defined as the lag for
growth. In order to substitute a microscopic obser-
vation for a macroscopic one, a relationship between
lag for growth and germination time was found
provided that the inoculum size was carefully
controlled. Some more studies should be conducted
in this direction.
Secondary models concerned mainly the influence
of environmental factors on fungal growth rate. At
present, very few models aimed at assessing the
influence of these factors on spore germination. In
addition, these models are polynomial and the provided
results can hardly be extrapolated to other moulds. We
are currently developing secondary models based on
parameters with biological significance (e.g., cardinal
values) to determine the influence of environmental
factors on spore germination parameters.
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