Food and Chemical Toxicology 47 (2009) 927–931

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Food and Chemical Toxicology

journal homepage: www.elsevier.com/locate/foodchemtox

Review of predictive models for Fusarium head blight and related mycotoxin
contamination in wheat
A. Prandini a,*, S. Sigolo a, L. Filippi a, P. Battilani b, G. Piva a
a
Institute of Food Science and Nutrition, Catholic University of Piacenza, Agricultural Faculty, Via Emilia Parmense 84, 29100 Piacenza, Italy
b
Institute of Entomology and Plant Pathology, Catholic University of Piacenza, Agricultural Faculty, Via Emilia Parmense 84, 29100 Piacenza, Italy

a r t i c l e i n f o a b s t r a c t

Article history: Mould growth and mycotoxin production are related to plant stress caused by environmental factors
Received 27 February 2007 such as: extreme weather; insect damage; inadequate storage conditions and incorrect fertilization;
Accepted 19 June 2008 these predispose plants to mycotoxin contamination in the field. Fusarium species infect wheat during
the flowering period. In addition to losses of yield, these fungi can also synthesize toxic components
(mycotoxins) in suitable environmental conditions, thus threatening animal and human health. Given
Keywords: the severe consequences and the fact that mycotoxins affect production throughout the world, the ability
FHB
to predict Fusarium head blight (FHB) and deoxynivalenol (DON) and other mycotoxin contamination is
Mycotoxins
Predictive models
important to reduce the year-to-year risk for producers. Owing to these dangerous consequences in
Wheat Argentina, Belgium, Canada, Italy, the United States and in Europe, computer models, based on weather
variables (temperature, rainfall and moisture level), have been developed to predict the occurrence of
FHB and DON contamination in wheat.
Ó 2008 Elsevier Ltd. All rights reserved.

1. Mycotoxins and predictive models mould growth and subsequent mycotoxin production in food prod-
ucts (Pardo et al., 2006).
Mycotoxins are toxic secondary metabolites produced by fungi Mould growth and mycotoxin production are related to: the
(commonly called moulds) that colonize crops in field or post-har- presence of fungal inoculum on susceptible crops; plant stress
vest and thus pose a potential threat to human and animal health. caused by extreme weather, faulty water and fertilization balance;
Only some moulds produce mycotoxins and they are referred to as insect damage; and inadequate storage conditions. In general, bio-
toxigenic. The major mycotoxin-producing fungal genera are tic and abiotic stresses (heat, water and insect damage) cause plant
Aspergillus, Fusarium and Penicillium. Many species of these fungi stress and predispose plants in the field to mycotoxin contamina-
produce mycotoxins; moulds can grow and mycotoxins can be pro- tion (Whitlow and Hagler, 2005), and there is an urgent need to
duced pre-harvest, during transport, processing or storage (Santin, know the level of contamination in real time or in advance. This as-
2005). The primary classes of mycotoxins are aflatoxins, zearale- pect stimulated efforts to develop models (Dantigny et al., 2005). A
nones, trichothecenes, fumonisins, ochratoxins and ergot alkaloids. disease forecasting system is principally based on the combined ef-
A practical definition of a mycotoxin is a secondary fungal metab- fects of host susceptibility, inoculum strength and meteorological
olite that causes an undesirable effect when animals or humans are conditions on disease development (Xu, 2003).
exposed to it. Usually, exposure is through consumption of con- A model is a simplified representation of a system, which is a
taminated food, which causes diseases known as mycotoxicosis. limited part of reality and contains interrelated elements, and at-
Mycotoxins exhibit a variety of biological effects in animals such tempts to summarise the main processes, to put forward hypothe-
as liver and kidney toxicity, effects on the central nervous system, ses and to verify their coherence and consequences (Rabbinge and
estrogenic effects (Whitlow and Hagler, 2005) and reduction of De Wit, 1989; van Maanen and Xu, 2003). The level of complexity
immunological defences, to name a few. It is important, both for needed for a specific model depends on the objectives and ques-
consumers’ health and the economic point of view, to prevent tions being asked of the model (Boote et al., 1996). Static and dy-
namic models can be developed, dependent if time is considered
in the model. Among dynamic models; those defined as ‘descrip-
tive’ simply trace the outlines of a system, and only show the exis-
Abbreviations: CPL, critical period length; DON, deoxynivalenol; FHB, fusarium
head blight; PI, prediction incidence; TOX-risk, risk of toxicity; ZEA, zearalenone.
tence of relations between elements, but do not explain these
* Corresponding author. Tel.: +39 523 599263; fax: +39 523 599259. relations. A more complicated approach is taken when the aim is
E-mail address: [email protected] (A. Prandini). to describe a more comprehensive system with its relations therein

0278-6915/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.fct.2008.06.010
928 A. Prandini et al. / Food and Chemical Toxicology 47 (2009) 927–931

and ‘explanatory’ models are developed in this case. During World Fusarium head blight (FHB) is well-suited for risk assessment
War II a rational approach was developed in order to study a sys- modelling because of the severity of epidemics, compounded
tem in detail: systems analysis. Systems analysis was developed losses resulting from mycotoxin contamination, and related nar-
basically as a tool to consider military options but it was demon- row time periods of pathogen sporulation, inoculum dispersal,
strated to be useful in different disciplines, where a system is stud- and host infection (De Wolf et al., 2003).
ied by distinguishing its major components, characterising their Computer models to predict the occurrence of FHB and deoxy-
changes, and the interconnecting elements (Leffelaar, 1993). The nivalenol (DON) contamination in wheat at harvest have been
system structure in plant pathology includes pathogen, host, envi- based on weather variables (temperature, rainfall and moisture)
ronment, human actions and their relationships (De Wit, 1993). (Moschini et al., 2001; Hooker et al., 2002; De Wolf et al., 2004;
Modelling can be split into three steps: model development, model Madden et al., 2004). In general, studies from outside the US in
analysis and hypothesis testing (van Maanen and Xu, 2003). A sim- spring and winter wheat regions (Europe, Canada, and Africa) indi-
ple way to represent a complicated system, like a pathosystem, is a cated interactions between disease intensity and occurrence of
relational diagram as a first step in model development (Leffelaar, DON comparable with or stronger than that found from US winter
1993). wheat areas, and weaker than those found in studies of US spring
Collection of information from different sources (step 1) is the wheat areas (Paul et al., 2005).
basis of ‘‘system analysis” that starts with drawing a relational dia-
gram translated into quantitative relationships that allow the quan- 2.1. Argentina
tification of states. Putting together all mathematical functions
(step 2), a simulation model able to predict fungal development is In Argentina, Moschini and Fortugno (1996) developed empiri-
finally obtained. Model validation and evaluation (step 3) is then cal equations to predict FHB incidence (Predictive Index: PI%) asso-
necessary before building up a final model used on a large scale. ciating mean head blight incidence of many wheat cultivars with
Explanatory models are significantly more complicated than temperature and moisture variables. Two of these equations were
descriptive. Due to the consideration of so many elements, as sug- validated subsequently by Moschini et al. (2001):
gested by De Wit, the explanatory models are too complicated to
PI% ¼ 20:37 þ 8:63  NP2  0:49  DD926 ð1Þ
be suitable for prediction in very different conditions.
The goal of this paper is to illustrate models developed for FHB PI% ¼ 18:34 þ 4:12  NP12  0:45  DD1026 ð2Þ
and related mycotoxin contamination in wheat, the most studied
disease related to mycotoxins because of the world wide distribu- where NP2 is the number of 2 day periods with precipitation
tion of wheat and Fusarium. Almost all models were developed as a (P0.2 mm) and relative humidity >81% on the first day and relative
descriptive model, and similar approaches have been followed in humidity P78% on the second day; NP12 is the total number of NP2
several countries, while an explanatory model, based on the sys- periods plus the total number of days with both precipitation
tem analysis, was developed in Italy. P0.2 mm and average relative humidity >83%. DD926 and DD1026
represent 926 or 1026 degree days accumulated and are calculated
as:
2. Fusarium head blight (FHB) in wheat
DD926 ¼ r½ðMaxTÞ  26Þ þ ð9  MinTÞ ð3Þ
Fusarium head blight, which is caused by several fungal species
DD1026 ¼ r½ðMaxT  26Þ þ ð10  MinTÞ ð4Þ
with Fusarium or Fusarium-like anamorphs, is a serious disease of
wheat in many parts of the world (Rossi et al., 2003b). Though where MaxT is the maximum daily temperature >26 °C, MinT is the
FHB can be destructive, its severity varies greatly between years minimum daily temperature <9 °C or <10 °C, and summation occurs
and locations, as this disease is heavily dependent on favourable over the days of the critical period length (CPL). CPL is the time per-
epidemiological conditions (Rossi et al., 2004). iod beginning 8 days before the heading date and ending when 530
Infection by Fusarium spp. on wheat occurs during the flowering degree days were accumulated (base temperature: 0 °C).
period. In addition to yield losses, these fungi can also synthesize This study showed that meteorological based empirical equa-
toxic compounds (mycotoxins) in favourable environmental condi- tions developed for Pergamino can be useful for predicting disease
tions, thus representing an important threat for animal and human intensity at many northern locations in the Pampas region, making
health. (Detrixhe et al., 2003). Preventive actions are possible so as only a few changes in temperature thresholds. Fernandes et al.
control strategies; accurate predictions of DON in mature grain at (2004) used a linked process-based model to assess the risk of
wheat heading are needed to make decisions on whether a control FHB at three sites in South America, and stated that the highest risk
strategy is needed. If weather variables can be quantified into index of FHB was probably due to the presence of more rainy days
DON-response relationship, a model could be developed to predict during the autumn in a specific climate scenario (Fernandes et al.,
the concentration of DON using both forecasted and actual weather 2004).
data for specific fields (Hooker et al., 2002). On the basis of the
known relationship between fungal biomass and DON, more heav- 2.2. Belgium
ily colonized plant tissue is likely to have a greater fungal biomass,
and consequently, higher DON content than less colonized tissue. In Belgium, in order to assess the risk of head blight infection in
For this reason, visual estimates of disease could also serve as indi- winter wheat, an agro-meteorological model has been developed
rect measures of DON to screen for genotypes with low DON accu- on the basis of an interpolation of weather radar data (above all
mulation (Paul et al., 2005). rainfall events) to simulate the leaf wetness duration on a grid size
Attempts to predict head blight have emphasised the impor- of 1  1 km (Detrixhe et al., 2003). Leaf wetness duration has a
tance of both inoculum and the environment for disease epidemics strong relationship with the development and outbreak of plant
(Parry et al., 1995). In order to predict disease incidence and to in- diseases because many important pathogens require a layer of free
crease the ability of wheat producers to achieve good disease man- water to move on the surface of plant organs and start their infec-
agement, several FHB infection or mycotoxin risk assessment tive processes (Dalla Marta et al., 2005). This model is interesting
models have been developed (De Wolf et al., 2003, 2004; Detrixhe for two reasons: the first is the interpolation of meteorological data
et al., 2003; Madden et al., 2004; Schaafsma and Hooker, 2006). on an area of interest and particularly the use of weather radar
 A. Prandini et al. / Food and Chemical Toxicology 47 (2009) 927–931 929

data to spatialise rainfall events in this area. The second is the use lated daily for F. graminearum and F. culmorum, and accumulated
of the estimation of leaf wetness duration instead of relative over the growing season until harvest:
humidity, in order to obtain a better characterization of risk of
TOX-risk ¼ SPO  DIS  INF  GS  INV ð8Þ
Fusarium head blight infection in winter wheat. Further calibra-
tion/validation tests are in progress to optimise the model devel- where SPO is the sporulation rate, DIS is the dispersal rate, INF is the
oped (Detrixhe et al., 2003). infection rate, GS is the host growth stage, and INV is the invasion
rate (Rossi et al., 2003b). Rates are influenced by air temperature,
2.3. Canada relative humidity, rainfall, sequences of rainy days, wetness dura-
tion, and free water in the host tissue (aw); fungal species and the
In Canada, Hooker et al. (2002) developed three equations to host growth stage are also considered. Production of DON and
predict DON in mature grain at wheat heading, based on rainfall ZEA in the kernels is then calculated by two regression equations,
and temperature data, and their timing. They measured the con- elaborated from artificial-inoculation experiments:
centration of DON in 399 farm fields in southern Ontario, Canada,
ln DON ¼ 3:0894  lnðTOX-riskÞ  3:5231 ð9Þ
from 1996 to 2000.
Eq. (5) predicts DON using weather information from 4 to 7
ln ZEA ¼ 0:2113  expð0:054  TOX-riskÞ ð10Þ
days before heading:
The model produces two indices: one for the risk of FHB on
DON ¼ exp½0:30 þ 1:84RAINA  0:43ðRAINAÞ2 wheat and one of mycotoxin content of kernels. Comparison be-
 0; 56TMIN  0:1 ðR2 ¼ 0:55Þ ð5Þ tween the actual content of both mycotoxins and the values esti-
1
mated showed good concordance (Rossi et al., 2003a).
where DON is the concentration of DON (lg g ), RAINA is the num-
ber of days of rain >5 mm day1 in the period 4–7 days before head- 2.5. The United States
ing, and TMIN is the number of days of temperature <10 °C between
4 and 7 days before heading. A series of severe Fusarium head blight epidemics experienced
Eqs. (6) and (7) predicted DON using weather information from in the United States of America led to a project to create a forecast-
7 days before heading to 10 days after heading: ing model. Using weather data, crop growth stage and disease
when RAINB >0, then observations from seven states, both spring and winter wheat pro-
DON ¼ exp½2:15 þ 2:21RAINA  0:61ðRAINAÞ2 duction areas, prediction models for FHB of wheat were imple-
mented (De Wolf et al., 2004; van Maanen and Xu, 2003). The
þ 0:85RAINB þ 0:52RAINC  0:30TMIN  1:10TMAX
final models used hourly temperature, humidity and rainfall to
 0:1 ðR2 ¼ 0:79Þ ð6Þ predict the risk of disease severity greater than 10%. The model de-
ployed in 2004 also contained variables that allowed users to spec-
and when RAINB = 0, then
ify type of wheat (winter vs. spring) and whether winter wheat
DON ¼ expð0:84 þ 0:78RAINA þ 0:40RAINC was planted into corn residue. Model accuracy was estimated to
 0:42TMINÞ  0:1 ðR2 ¼ 0:56Þ ð7Þ be near 80% based on data used to validate the model that was de-
ployed for 23 states in 2004 as part of the National Fusarium Head
1
where DON = concentration of DON (lg g ), RAINA is the number Blight Prediction Center (www.wheatscab.psu.edu). Modelling of
of days of rain >5 mm day1 in the period 4–7 days before heading, these field data showed that environmental conditions prior to
RAINB is the number of days of rain >3 mm day1 in the period 3–6 flowering were more important than those during anthesis (Xu,
days after heading, RAINC is the number of days of rain >3 mm day1 2003). The validation of the model and the development of an up-
in the period 7–10 days after heading, TMIN is the number of days dated version for scab risk prediction are based on additional scab
of temperature <10 °C between 4 and 7 days before heading, and observations, weather data for different time windows, and the
TMAX is the number of days with temperature >32 °C between 4 integration of empirical observations of epidemics with results
and 7 days before heading. from field and laboratory studies on scabs. The model was gener-
DONcast, a robust site specific DON forecaster (Hooker and ally accurate in field testing, but improvements in accuracy are
Schaafsma, 2003) was commercialised for wheat and has been needed (Madden et al., 2004).
used commercially for 5 years (Schaafsma and Hooker, 2006). For
the first time, in 2004, a web-based interactive model, which al- 3. Limits of predictive models
lowed input of field-specific weather and agronomic variables,
was developed for industry. The predictions have explained 76% Mycotoxins can be produced in field as well as during food stor-
of the variability in DON using a database from 1996 to 2003 (Hoo- age and different meteorological, environmental and agronomic
ker et al., 2004). factors affect their production. For this reason, it is difficult to pre-
dict the occurrence of fungal diseases and toxin contamination in
2.4. Italy foodgrains.
Crop models have many current and potential uses for answer-
In Italy, a predictive model regarding the risk of Fusarium head ing questions in research, crop management and policy. The
blight and mycotoxin contamination (DON and ZEA) in wheat was descriptive models are easy to comprehend, often require fewer in-
developed on the basis of meteorological data and information puts, and often are easier to use and apply, but they have to be cal-
about wheat growth stages Rossi et al. (2003a, 2003b) developed a ibrated to each new site. On the other hand, the explanatory
dynamic simulation model for the risk of Fusarium head blight on models are better able to model genotype X environment interac-
wheat based on systems analysis. The model calculates a daily infec- tion, but their complexity makes them more difficult to understand
tion risk based on sporulation, spore dispersal and infection of the and to use and apply, and they also require more input informa-
host tissue of the four main species causing the disease (Gibberella tion. In many cases the outputs of the explanatory models may
zeae, Fusarium culmorum, Giberella avenacea, Monographella nivalis). be less stable, particularly if the given information was incorrectly
The model was validated over 22 wheat-growing areas of north- modelled. Cautions and limitations (Table 1) in the model uses are
ern Italy in 2002. In each area, a risk index (TOX-risk) was calcu- suggested, because appropriate use for a particular purpose
930 A. Prandini et al. / Food and Chemical Toxicology 47 (2009) 927–931

Table 1
The predictive models

Predictive Disease/ Crop Limits References Year

models mycotoxin
Argentina FHB Wheat Site- and year-specific Moschini & 1996
Fortugno
Fernandes et al. 2004
Belgium FHB Winter wheat Instrumental (radar) availability Detrixhe et al. 2003
Dalla Marta et al. 2005
Canada DON Cereal grain Do not consider: crop rotation, crop variety, tillage, Hooker et al. 2002
fertilization, etc. Hooker & 2003 & 2004
Schaafsma
Schaafsma & 2006
Hooker
Italy FHB, DON, ZEA Wheat Low accuracy for high TOX-risk Rossi et al. 2003a & 2003b
The United FHB Spring and winter Low accuracy De Wolf et al. 2004
States wheat Van Maanen & Xu 2003
Xu 2003
Madden et al. 2004
Italy F. verticillioides Maize Aspect of dynamic cycle of fungi are needed Rossi et al. 2003a; 2003b &
2006
Europe P. verrucosum Cereal grain Lack of field and storage management effects Pardo et al. 2006

depends on whether the model has been correctly developed and Nevertheless, predictive models may present some limits of
validated in diverse environments (Boote et al., 1996): application and accuracy, and precise information on the ap-
proach to be taken for their development is needed before correct
 the level of complexity depends on the amount of information use can be guaranteed. As stated before, descriptive models are
(data) and time available for model building and testing. Most sufficiently reliable in the geographic area of development or in
computer models relate only meteorological variables and do other very similar places. The amount of information requested
not include field-specific effects such as crop rotation, crop vari- is limited and they can be developed in a reasonably short time.
ety, tillage, etc.; Explanatory models are based on a considerable amount of infor-
 some simple, descriptive models have parameters that are site mation and it takes several years to produce and process the nec-
and year-specific, so that the model has little predictive ability essary data, both for model development and validation. Then,
for other locations; they can be run in different areas, and can include different vari-
 field and storage management and human behaviour (habits, ables, such as meteorological, phenological and cropping system
customs, etc.) influence the mycotoxin problem; these factors data and the output is precise and reliable. The accuracy of this
are normally not included in model development, because they kind of model largely depends on the accuracy of the weather
are difficult to quantify. forecast.
In conclusion, modelling is a strategic tool for crop manage-
The application of predictive models, like many weather-driven ment aimed at preventing mycotoxin prevention contamination,
prediction systems, will depend on the availability, resolution, and but a lot of work is necessary to develop explanatory models
reliability of weather data. As suggested by De Wolf et al. (2003), with a good predictive capacity. More research is needed, taking
a potential limitation of models A (temperature  humidity combi- into account other abiotic factors and fungal interactions to im-
nation variable postanthesis) and B (model A  variables summa- prove the microbiological safety and shelf-life of food products
rizing pre-anthesis weather interaction) was the dependence on (Pardo et al., 2006). According to Paul et al. (2005) differences
weather information during anthesis. While it may be possible to between models could be due to factors such as the genotypes
overcome this limitation by using forecasted weather, the uncer- planted, the weather conditions, the pathogen population, crop
tainty of predicted weather variables may reduce model prediction production, and disease management practices, as well as other
accuracy (De Wolf et al., 2003). Further, there is a tendency to ex- unknown random effects; consideration of moderator variables
tend the use of models that were developed for bacteria to moulds, attempts to explain some between-study variability (Paul et al.,
but one important specificity of fungi should be taken in account: 2005). As demonstrated by Baranyi et al. (1996), the advice of
spore germination. Free water or near saturation moisture on the McMeekin on parsimony is vital for predictive models, not only
host surface is essential for germination and penetration of the host for simplicity but also to improve the accuracy of predictions
for many pathogens. Thus a single parameter indicating water avail- (Baranyi et al., 1996 reference therein).
ability is used in several forecasting systems; but, very few models
aimed at assessing the influence of environmental factors on spore Conflict of interest statement
germination (Dantigny et al., 2005; van Maanen and Xu, 2003).
All authors are professionals employed by the Catholic Univer-
4. Conclusions sity of Sacred Heart of Piacenza and as such do not have any inter-
ests that may conflict with the contents of the article above.
In order to predict the incidence of diseases and mycotoxin con- This study was subsidized by the European Commission in the
tamination and to increase the ability of producers to achieve good SAFEFOODS project in the EU6th Framework programme.
disease management, several epidemics or mycotoxins risk assess-
ment models have been set up. The employment of models may be Acknowledgement
useful for decision-making purposes: to prevent/reduce yield
losses and hazards for human and animal health based on the cor- This study was supported by the research project ‘‘Promoting
rect time for spraying chemicals; predict the final level of contam- Food Safety through a New Integrated Risk Analysis Approach for
ination and better organise post-harvest management. Foods (SAFE FOODS)” (Food-CT-2004-506446).
 A. Prandini et al. / Food and Chemical Toxicology 47 (2009) 927–931 931

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