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Food Additives & Contaminants: Part A
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Mycotoxins in small grains and maize: Old problems,
new challenges
a
J. David Miller
a
Ottawa-Carleton Institute of Chemistry , Department of Chemistry, Carleton University ,
Ottawa, Ontario, Canada K1S 5B6
Published online: 20 Feb 2008.
To cite this article: J. David Miller (2008) Mycotoxins in small grains and maize: Old problems, new challenges, Food
Additives & Contaminants: Part A, 25:2, 219-230, DOI: 10.1080/02652030701744520
To link to this article: http://dx.doi.org/10.1080/02652030701744520
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www.tandfonline.com/page/terms-and-conditionsFood Additives and Contaminants, February 2008; 25(2): 219–230
Review
Mycotoxins in small grains and maize: Old problems, new challenges
J. DAVID MILLER
Ottawa-Carleton Institute of Chemistry, Department of Chemistry, Carleton University,
Ottawa, Ontario, Canada K1S 5B6
(Received 25 July 2007; accepted 8 October 2007)
Abstract
This paper reviews the challenges relating to chronic contamination of small grains and maize with deoxynivalenol and
related compounds, fumonisin and the use of ensiled cereals in cool dairy areas. Uncertainties in the tolerable daily intakes
for deoxynivalenol and fumonisin are discussed as they have the potential to affect current regulatory limits. In addition,
climate change is resulting in more extreme rainfall and drought events which favour formation of deoxynivalenol and
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fumonisin, respectively. The development and refinement of models for predicting mycotoxin accumulation from weather
data will become an essential tool for managing these events. Such models are also important for providing timely food aid
to developing countries, which experience increased occurrence of acute toxicities, especially in children. Chronic
contamination of silage in some areas with some Penicillium toxins deserves more attention in terms of their economic effects
and possible implications for the purity of milk.
Keywords: Deoxynivalenol, neurotoxicity, fumonisin, neural-tube birth defects, silage, roquefortine, festuclavine, PR toxin,
climate change
Introduction complex on ensiled materials and A. flavus on
many commodities. The major toxins that contam-
It seems timely to review the progress made on
mycotoxins research in cereals over the past 15 years inate maize and small grains (wheat, triticale, barley)
and consider the challenges remaining and new pre-harvest are deoxynivalenol (replaced in some
problems on the horizon. As noted in an earlier areas by nivalenol) and zearalenone, fumonisin and
review (Miller 1995), toxigenic fungi in crops have aflatoxin on maize. For two of these toxins, namely
been historically divided into two distinct groups. deoxynivalenol and fumonisin, there are unresolved
The first includes those that invade and produce issues that might affect their hazard assessment.
toxins before harvest and the second group, which Because they are common in grain, this represents
form toxins after harvest, are known as storage fungi. a level of uncertainty that perhaps deserve more
However, the source of the fungi in both instances is attention in this review.
the field (Miller 1995). Four types of toxigenic fungi There are other mycotoxins that can cause
can be identified: (1) plant pathogens, such as problems occasionally in small grains and maize,
Fusarium graminearum; (2) fungi that produce the most important being the Fusarium toxin, T-2,
mycotoxins on senescent or stressed plants, such as which is normally associated with a derivative, HT-2
F. verticillioides and Aspergillus flavus on maize and toxin. Alimentary toxic aleukia (ATA) disease was
A. carbonarious on grapes; (3) fungi that colonise the described prior to 1900 and was associated with the
plant and predispose the commodity to mycotoxin ingestion of overwintered grain. During World War
contamination after harvest e.g. A. flavus in sub- II, Russians were forced to eat grain left in the field.
tropical maize and (4) fungi that are found in the soil Thousands of people were affected resulting in the
or decaying plant material that occur on the elimination of entire villages (Mirocha 1984;
developing kernels in the field and later Beardall and Miller 1994). Strains of fungi isolated
proliferate in storage if conditions permit, e.g. from the grains at the time were later shown to
Penicillium verrucosum on cereals, P. roqueforti produce T-2 and related toxins ( Joffre and
Correspondence: J. David Miller. E-mail: david_miller@carleton.ca
ISSN 0265–203X print/ISSN 1464–5122 online ß 2008 Taylor & Francis
DOI: 10.1080/02652030701744520220 J. D. Miller
Hagen 1977). These are mainly F. sporotrichioides dominate depends on temperature. These species
toxins, a species that grows on wet grain left in the also vary somewhat in pathogenicity; F. graminearum
field and to some extent on the glumes of small is regarded as the most virulent, although all three
grains (Miller 1994; Miller et al. 1998). In parts of species can cause epidemics. Wheat, maize and barley
Europe, F. langsethiae is also an important producer are most affected by these pathogens (Miller 1994;
of T-2 toxin on small grains (Thrane et al. 2004; Mesterhazy 2003; Snijders 2004) and by their toxins.
Torp and Nirenberg 2004). However, despite the These three crops comprise two thirds of the world’s
vast literature on T-2, incidence data show that cereal production. Contamination of oats, rye and
material concentrations of this toxin are uncommon triticale has also been reported to contain Fusarium
in most growing areas. This is because most grain is mycotoxins (Scott 1989; Gareis et al. 2003). In parts
harvested under warm, dry conditions. Modest levels of Europe, F. poae is also an important producer of
of contamination in grain observed at harvest in nivalenol on small grains (Thrane et al. 2004) and
parts of western Europe, primarily in cooler, wetter nivalenol is commonly reported in European oat
areas, are apparent exceptions to this generalization samples (Gareis et al. 2003).
(Gareis et al. 2001). The Provisional Maximum F. graminearum is associated with wheat and maize
Tolerable Daily Intake (PMTDI) of the Joint Expert grown in warmer areas (e.g. southern Ontario) and
Committee on Food Additives and Contaminants of F. culmorum, in cooler areas (e.g. northwestern
the World Health Organization/Food and Europe, but see below). The influence of tempera-
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Agricultural Organization (JECFA) for T-2/HT-2 ture relates to conditions that allow a sustained
toxin of 0.6 mg kg1 bw has a larger safety factor than period of warm weather (daytime temperatures
would normally be indicated. This is primarily due 430 C) regardless of daily means. The most
to a lack of experimental data (Larsen et al. 2004). pathogenic species, F. graminearum and F. culmorum,
This review and comment will focus on three are generally the most common species found. Since
broad topics. First, a perspective will be offered on the 1890s, Fusarium head blight has been common
research on the Fusarium toxins, deoxynivalenol and in wheat from North America and China
fumonisin, in small grains (wheat, barley, oats) and (Miller 1994; Wang and Miller 1988; Chen et al.
maize. These crops comprise two thirds of cereal 2000; Goswami and Kistler 2004). In the 1980s and
supply, which is currently in the order of 350 kg 1990s, F. culmorum was the dominant species in
person1 year1 (Dyson 2001). The reason for this cooler wheat-growing areas, such as Finland,
emphasis is that, for cereals contaminated by France, Poland and The Netherlands (Snijders and
aflatoxin, including rice, the guidelines applying to Perkowski 1990; Miller 1994; Toth et al. 2004), but
international trade are clear. This is regardless of this trend has apparently changed in recent years as
whether, for example. the difference between WHO European summers have reached record warm
and EU guidelines can be defended on a health basis temperatures such that F. graminearum largely
(Wu 2004). In contrast, there are some uncertainties dominates (Xu et al. 2006).
in the PMTDIs for deoxynivalenol and fumonisin Morphologically identical isolates of F. grami-
relating to aspects of the mechanism and human narum (Gibberalla zeae) can produce either DON
health effects that might affect current trade limits. and zearalenone or nivalenol and zearalenone as the
Second, factors that resulted in increased exposure principal toxic metabolites that accumulate in grain.
to these toxins will be explored with suggestions Within the former group, some strains produce
about actions required to manage this change. DON by the 3-acetylated precursor and others make
Finally, the increased use of ensiled maize in north the 15 acetylated precursor. DON-producing strains
temperate dairy-producing areas (e.g. Quebec) will with the 15-acetylated precursor dominate in North
be examined in relation to uncertainties about toxins and South America. DON-producing strains with
associated with this feed source. the 3-acetylated precursor are common in Europe
and Asia (Miller et al. 1991). The Asian and New
World strains are genetically distinct (O’Donnell
Toxins associated with Fusarium head blight and
et al. 2000). Nivalenol-producing strains of
Gibberella ear rot
F. graminearum are common in parts of Europe,
Fusarium graminearum, F. culmorum and F. crookwel- Japan and Australasia but very uncommon in the
lense are closely related species that produce deox- Americas. F. culmorum produces DON and zearale-
ynivalenol (DON) or nivalenol and zearalenone, none ( Miller et al. 1991; Jennings et al. 2004; and
depending on the geographic origin of the isolate references cited therein; Toth et al. 2004). The
(Miller et al. 1991). These fungi cause Fusarium head crown rot form of F. graminearum Group 1 is now
blight in small grains and Gibberella ear rot in maize. called F. pseudograminearum (G. coronicola; Aoki and
These diseases are associated with temperate grain- O’Donnell 1999) but also produces deoxynivalenol
growing regions. Which of the three species will and nivalenol (Clear et al. 2006).Mycotoxins in small grains and maize 221
The use of susceptible wheat cultivars and (Hoyman 1941). Water extracts and then methanol
maize hybrids is largely responsible for incidence extracts of maize and barley cultures of F. grami-
of F. graminearum. Under epidemic conditions, nearum given intraperitoneally (i.p.) produced toxic
agronomic practices have modest impact on disease signs in nursing mice and swine, and in swine by
(Miller 1994; Schaafsma et al. 2001; Hooker et al. gavage, i.p. and intravenously (i.v.) by the mid 1960s
2005; Koch et al. 2006; Miller et al. 1998). As far as (Vesonder and Hesseltine 1981). Using strains
can be seen, only countries that enforce clear isolated from Fusarium head blight-affected cereals
requirements, such as reductions in Fusarium head provided by W.L. Gordon (Agriculture Canada),
blight (including DON measurements) (Wilde et al. Prentice et al. (1959) reported an emetic principle in
2007), have been able to reduce toxin amounts in organic solvent extracts from Fusarium cultures but
the harvested crop (Snijders 2004; see also Larsen were unable to determine the chemical structure
et al. 2004). (Prentice and Dickenson 1968). About the same
‘‘Red mold poisoning’’ was reported in rural Japan time, while investigating Fusarium-damaged maize
coincident with an increase in wheat production from (described as F. culmorum and F. graminearum
1800. Major epidemics were recorded in Japan for the by Booth) resulting in cattle toxicosis. Australian
1890, 1901, 1914, 1932, 1946, 1958, 1963 and 1970 researchers reported a toxic principle resulting
crops, with human and animal toxicoses reported in skin necrosis (Fisher et al. 1967). Finally,
throughout (Yozhizawa 1983; Udagawa 1988). US researchers re-reported DON as ‘‘vomitoxin’’
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Japanese researchers and officials were sensitive to from F. graminearum-contaminated maize in
the possibility of toxic chemicals from mold-damaged 1973 that had produced emesis in swine (Vesonder
food. The study of mycotoxins began in 1881 when a et al. 1973).
Japanese researcher showed that ethanol extracts of Humans appear to be quite sensitive to DON (Bhat
rice damaged by Penicillium citreonigrum were fatal to et al. 1989; Kuiper-Goodman 1994), but
dogs, rabbits and guinea pigs. This led to a the available information does not permit a dose–
commercial ban on the sale of rice damaged by that response to be reliably determined. The domestic
fungus (Pitt 1991). Well-documented reports of animal most affected by DON is swine and, as noted,
human toxicosis from the consumption of Fusarium the use of the second trivial name for DON,
head blight-damaged wheat and barley are available. vomitoxin, arose from the emetic effect in swine.
These describe the typical symptoms that consistently The minimum oral dose required for emesis is in the
include nausea, vomiting and diarrhoea (Yozhizawa order of 100 mg kg1 bw (Pestka et al. 1987).
1983; Udagawa 1988). Russian officials reported the The emetic response in dogs appears to occur at a
same symptoms from humans consuming bread similar dose (Ueno 1983). However, DON seldom
baked from scabby grain in 1923 (Prentice and causes overt toxicity, including emesis, in swine
Dickensen 1968). DON was isolated by Japanese because its presence in feed limits consumption.
researchers from grain that had made humans ill This anorexic effect typically results in decreased feed
(Morooka et al. 1972). This toxin was responsible for consumption and growth in swine at concentrations
a large-scale incident of human toxicosis in the of more than 1 mg g1 in diets containing naturally
Kashmir Valley of India in 1988 (Bhat et al. 1989; contaminated grains. Trichothecenes in general,
Medical Research Council of India, unpublished including DON, have a variety of immunological
report). The same symptoms were seen in Indians effects in laboratory animals at very low exposures. In
consuming bread made from highly contaminated experimental situations, this leads to increased
wheat. Acute human toxicoses have been reported in susceptibility to bacterial, viral and fungal diseases
China, Japan and Korea, among other countries with strong implications for human disease (Bondy
( Yoshizawa 1983; Beardall and Miller 1994; Kuiper- and Pestka 2000; Pestka and Smolinski 2005).
Goodman 1994; Li et al. 1999). There is, therefore, a long and clear historic
Fusarium head blight-damaged grain began to be association between DON and animal disease. After
a problem in the Midwest US and Canada coin- consumption of grains affected by Fusarium head
cident with the dominance of Marquis wheat during blight, similar symptoms in human have been
WW I. By the 1920s, large cultivar-screening consistently reported in many populations since the
programs were underway in Minnesota (Schroeder turn of the 19th century. There is no uncertainty that
and Christensen 1963). In 1928, there was a massive consumption of contaminated wheat results in DON
epidemic in the mid west, where US scientists exposure in humans (Turner et al. 2007). For the last
showed that damaged barley resulted in emesis 25 years, health authorities have acted to reduce
in swine (Mundkur 1934). By 1941, a water extract human consumption of this toxin. Considering the
of barley contaminated by a fungus described as available toxicology data, Health Canada established
G. saubentii [an invalid name that included F. a tentative tolerable daily intake in 1982 of
graminearum], induced emesis in swine by gavage 3 mg kg1 bw per day and half that for infants222 J. D. Miller
(Kuiper-Goodman 1985). Based on a much changes in the membranes of more resistant types
expanded database, the JECFA established a PMTI (Snijders and Kreching 1992; Cossette and Miller
that was slightly lower in 2001 (Canady et al. 2001). 1995; Miller and Ewen 1997). It is reasonable to
These factors (and others discussed in the speculate that modest effects on membranes asso-
following section) led to a series of recommendations ciated with the emesis centre might be responsible
on future research on DON at an ILSI–EU meeting for the neurotoxicity as the receptor structure would
held in Dublin (Larsen et al. 2004). In relation to be altered and, hence, binding affinity.
either increasing or decreasing the PMTDI, two The ILSI–EU meeting suggested that the estab-
issues were raised that deserve repeating. There lishment of an acute reference dose (ARfD) for
is wide agreement that the mechanism causing DON would be valuable. It was also agreed that the
neurotoxicity (emesis and feed refusal) needed to ethical problems in doing a human study would be
be determined. profound, indicating that perhaps a non-human
In the mid-1990s, a great deal of work was done to primate study would be desirable (Larsen et al.
try and resolve this question for DON in swine. 2004), in my opinion, would be less important than
Dosing by a continuous-exposure osmotic pump, determining the mechanism of neurotoxicity. There
implanted intraperitoneally, resolved that the effects are human clinical data available from the use of
could not be due to taste or learned responses another trichothecene, DAS (also known as angui-
(Prelusky 1997). A single dose of 0.25 mg kg1 bw dine), as a chemotherapy agent in many studies.
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(i.v.) changed neurotransmitter concentrations in These studies have demonstrated that nausea and
the hypothalamus, frontal cortex and cerebellum up vomiting occurred in 50% of the patients at doses
to 8 days post-dosing. Norepinephrine increased in of between 200 and 400 mg kg1 bw i.v. (Bukowski
all three tissues, whereas dopamine was decreased. et al. 1982; DeSimone et al. 1997). Considering the
In contrast, serotonin increased and then decreased relative acute toxicities of DAS to DON, this would
in the hypothalamus, it was decreased in the frontal translate into an emetic dose for DON in adults of
cortex and no change was observed in the cerebel- 4800 mg kg1 bw. This suggests that the minimum
lum (Prelusky et al. 1992). A lower dose (10 mg kg1 emetic dose for DON in swine is a reasonable
bw i.v.) resulted in changes in cerebral spinal fluid approximation of the human equivalent. It was also
neurotransmitters (Prelusky 1993). Serotonin-recep- suggested that studies of interactions between
tor antagonists prevented DON-induced vomiting, trichothecenes be performed (Larsen et al. 2004),
while 5HT2-receptor antagonists were moderately which, in my opinion, would have little value.
effective in high doses. Other anticholinergic actives It is known that there are interactions between
were also effective but by acting directly at the trichothecenes in model systems (Koshinshy and
emetic centre preventing emesis regardless of the Khachatourians 1992) and in animals (Schiefer et al.
cause (Prelusky et al. 1992). This suggested that, 1986; Bhavanishankar et al. 1988), but their dimen-
although there is no doubt that the emetic centre is sion is modest (Mycotoxins in small grains and maize 223
F. verticillioides (¼G. fujikuroi) and F. proliferatum. Since the discovery of fumonisin in 1988, a great
In warmer corn-growing areas, F. verticillioides is one deal has been learned about its effects. Consumption
of the most important ear diseases (Miller 2001). of maize contaminated with fumonisin has a number
F. proliferatum (which also produces moniliformin) of toxic effects on domestic animals, including
becomes dominant under different environmental equine leucoencephalomalacia in horses (ELEM),
conditions than F. verticillioides (De La Campa and pulmonary edema and immunosuppression in
et al. 2005). swine. The toxin is carcinogenic in rodents.
Below 25–28 C, F. graminearum grows well, with The mechanism for all these phenomena is directly
growth virtually ceasing above that temperature, and or indirectly due to the effects of fumonisin on
in that range, assuming that there is sufficient rain, sphingolipid biosynthesis; this work has been
this fungus out-competes F. verticillioides. Many reviewed extensively (IPCS 2000; Bolger et al.
studies on fumonisin from natural occurrence and 2001; SCF 2003). JECFA established a PMTI
experimental infections have demonstrated the using the renal toxicity of fumonisin as the endpoint.
importance of drought rather than temperature (Voss et al. 1995; NTP 2001).
stress. F. verticillioides grows well at temperatures Fusarium kernel rot was associated with animal
above 28 C (Reid et al. 1999) and there is evidence disease in the US midwest in 1904 and there were
that fumonisin can only accumulate in stressed or large epidemics of ELEM in the US during
senescing kernel tissue (Reid et al. 1999; Miller the drought years of the 1930s. In 1971, corn
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2001). This is consistent with considerable field contaminated by the fungus, now called F. verticil-
data; for example, in a US study, fumonisin liodes, was shown to cause ELEM (IPCS 2000).
concentrations were inversely proportional to June A South African group studying elevated esophageal
rainfall (Shelby et al. 1994). In the cool corn- cancer in the Transkei and a French group working
growing area of southern Ontario, accumulation was on ELEM independently described fumonisin as the
cause of disease in 1988 (Marasas 2001) and then in
limited to drought-stressed fields. Comparing three
1989 (as macrofusin; Laurent et al. 1989).
counties with similar temperatures, the three with
There has also been the association of regular
the highest average FB1 concentrations (1.4 mg g1)
consumption of large amounts of maize-based foods,
had half the rainfall of the counties with the lowest
regularly infected with F. verticilliodes, with esopha-
average FB1 (0.4 mg g1; Miller et al. 1995).
geal cancer in South Africa and northern Italy
Since drought stress results in greater insect
(IARC 1993, 2002; IPCS 2000). South Africa has
herbivory on maize, it is not possible to totally
been growing maize at least since the 17th century
separate these variables from other complications
and it is now grown across Africa (Desjardins and
(Miller 2001). However, there is a strong consistent
McCarthy 2004; McCann 2005). In Latin America,
relationship between insect damage and Fusarium
food is prepared primarily from tortilla flours
ear rot. Within a year or two of the availability of prepared by heating with base which reduces
fumonisin analytical standards, a field survey fumonsin concentrations. However, in Africa, fumo-
demonstrated that the incidence of the European nisin is not affected by traditional methods of
corn borer increased Fusarium kernel rot and cooking (De La Campa et al. 2004; Shephard et al.
fumonisin concentrations (Lew et al. 1991). Maize 2002; Fandohan et al. 2005), but sorting does
genotypes containing the anti-insectan Bt protein effectively reduce fumonisin concentrations
have reduced amounts of fumonisin compared to (Desjardins et al. 2000; Riley and Miller 2003).
non-Bt genotypes (Bakan et al. 2002; Hammond The earliest reports of esophageal cancer in rural
et al. 2004; De La Campa et al. 2005). black populations (studies from 1955–1969; Rose
De La Campa et al. 2005) were able to integrate 1973 and references cited therein) noted the extra-
this information in a study of factors that affected ordinarily high rates of this cancer in the Transkei.
fumonisin accumulation in maize. Insect damage This was striking compared to other parts of the
and weather variables in four periods around silking world and other parts of Africa (Day, 1975). Since
explained most of the variation in fumonisin no biomarkers are available, it has proven impos-
concentrations at harvest. The first critical period sible, so far, to establish fumonisin as a causative
for fumonisin accumulation was 4–10 days before factor in this pattern of esophageal cancer. In the last
silking when temperatures of224 J. D. Miller
demonstrated dietary exposure) and, if reliably summer or is water-limited. Since 1961, China has
demonstrated, the IARC classification would increased cereal production 5-fold from 100 to
change from 2B to 2A (probable human carcino- 400 kg person1, with maize and wheat increasing
gen), which might require a re-evaluation of the roughly in proportion. Maize has been grown in
PMTDI. China since the 16th century (Desjardins and
After the setting of the JECFA TDI, it was found McCarthy 2004) and currently has a much larger
that fumonisin causes neural tube birth defects production than wheat. For food, wheat is nearly
(NTDs) in mouse somites (Sadler et al. 2002) and equal to rice, a well-established food crop since the
a rodent model in vivo (Gelineau-van Waes et al. 6th century (Myer 1978). The ratio of rice to
2005). These studies arose from a transient increase wheat þ maize production has changed from 1.2:1
in NTDs from 10 to 27 per 10,000 live births in to 0.8:1 (Tong et al. 2003). Fusarium head blight
Mexican-Americans in Cameron County Texas epidemics have been greatly increasing in frequency
(Hendricks 1999; Marasas et al. 2004). A follow- in recent years (Chen et al. 2001) and, as noted
up study found that increased NTD risk was above, there is exposure to DON in China from both
associated with fumonisins exposure (Missmer wheat and maize, although it is not well documented
et al. 2006) and, for a number of reasons, animal (Canady et al. 2001; Meky et al. 2003).
models had failed to predict this possibility (IPCS The situation in Africa is much different. During
2000). The mechanism relates to material exposure the period 1960–2003, cereal production increased
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to fumonisin prior to the formation of the placenta. 2.5-fold (half that of China) but, approximately over
Fumonisin affects folate transport, which results in the same period, declined on a per capita basis from
lowered folate in the embryo (Sadler et al. 2002; 150 to 125 kg person1 (Dyson 2001). As with
Marasas et al. 2004). A study of tortilla production China, there has been a modest change in the ratio of
in Cameron County revealed that some preparation maize production to that of the other staple crops
methods in local facilities left intact fumonisin in the (sorghum, millet, rice). However, of these, maize is
final product (De La Campa et al. 2004) and NTDs uniquely susceptible to fumonisin, DON and zear-
are very high in fumonisin endemic areas (Marasas alenone and co-exposures with aflatoxin are certainly
et al. 2004). At the time of writing, there is no common (Doko et al. 1996; Ngoko et al. 2001)
published study of NTDs in a regulatory strain of Africa has become extremely vulnerable to
rodent [The strain used in the Gelineau-van Waes exposure from mycotoxins found in maize (Riley
(2005) study is specialized for NTD research]. and Miller 2003; Azziz-Baumgartner et al. 2005).
Another factor that might result in the re-evaluation China is producing sufficient food for residents of
of the JECFA TDI would be the results of a rural areas to purchase food (Gale et al. 2005),
well-designed study in a regulatory strain of
which means that diets are much more diverse in
fumonisin.
China compared to Africa. In regions where weather
conditions result in (more) severe mycotoxin
Exposure to maize and wheat borne toxins is increasing problems, very high exposures are inevitable with
The existence of a widely accepted JECFA PMTI for the potential for acute toxicoses (Riley and Miller
DON and fumonisin are major achievements; 2003; Azziz-Baumgartner et al. 2006). While this
however, in the recent past, exposure of young has long been known for aflatoxin in Africa, the
children has been close to the PMTDI in the PMTDI for fumonisin, as noted, is exceeded in
Netherlands (Pieters et al. 2004), Denmark Africa, with the upper 10th percentile of the
(Rasmussen et al. 2007) and Canada (Kuiper- population being approximately three times that of
Goodman et al. 2008). The PMTDI is exceeded in the PMTDI ( JECFA 2001). In areas where the
other countries – dramatically so in Africa and in occurrence of fumonisin is chronic, this materially
parts of Latin America (JECFA 2001) and there is understates the situation. Shephard et al. (2007)
no doubt that this would be more dramatic if estimated fumonisin exposure in some areas of rural
exposures were calculated for wheat-consuming South Africa at 2–19 times the PMTDI and
population in endemic areas lacking a diverse exposure in rural Bukino Faso was found to be
source of cereals, as opposed to the standard 12–60 times the PMTDI (Nikiema et al. 2004).
GEMS diet. The situation for fumonisin exposure Against this broad background, in both the fully
is similar, except much worse in parts of Africa developed market economies and due to the limited
(Bolger et al. 2001; Shephard et al. 2005, 2007). diversity of the food supply in developing countries,
As noted above, large areas of arable land have increased climate variability will produce more
come under wheat and maize production in China frequent epidemics of Fusarium head blight and
since 1961 (Dyson 2001; Tong et al. 2003). Most Gibberella ear rot. As described above, the former
arable land is in areas prone to humidity in the requires rain at anthesis or silk emergence and warmMycotoxins in small grains and maize 225
conditions while Fusarium kernel rot requires dry DON-tolerant domestic animals (cattle) after appro-
conditions but permissive temperatures. priate dilution. For DON and fumonisin in maize,
At the end of 2006, the number of weather-related Hooker and Schaafsma (2005) and, in greater detail
disasters in Canada has increased 10-fold since 1900 for fumonisin in maize, De La Campa et al. (2006)
and 4-fold since 1960, most of which are related to have demonstrated that such models are feasible.
heavy rainfall (http://www.ec.gc.ca/TKEI/graphs/ While these models are meant for areas with on-line
w_disasters_095_e.xls). These disasters have been meteorological data and information on emergent
associated with the flooding of rivers, caused by insect populations, some modeling might be feasible
prolonged rain during rapid snowmelt, of drainage from remote-sensing information.
pathways, primarily caused by short-duration, inten- Rainfall timing, water stress and permissive
sive rainfall from thunderstorms or the residue of temperatures are the key factors for DON and
hurricanes coming up from the US southeast. These fumonisin accumulation. Modeling of drought and
phenomena have also been felt in Europe (Ekström vegetation indices are a component of the Famine
et al. 2005; Lehner et al. 2006; Wilson 2007). In the Early Warning System, which assesses remotely
principal Canadian maize-production area sensed data, ground-based sources and other factors
(Ontario), each of the last five summers has been affecting local food availability (http://www.fews.
hotter than the previous 30, on average, which net/). These data could form the basis of models
creates one of the conditions for increased risk of that might be developed for DON, fumonisin and
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fumonisin accumulation. The other condition is possibly aflatoxin, adding an important early
drought (Miller et al. 1995; Miller 2001), which is warning capacity to managing contaminated crops.
also predicted to occur more often in most of the Potentially, toxin-predictive modelling is an
corn regions over the coming decades (Lehner et al. important research direction for both vulnerable
2006). An increased prevalence of extreme weather populations and due to increased climate variability
events is now anticipated worldwide over the next in countries with commercial agriculture.
century (Zhang et al. 2007).
Riley and Miller (2003) argued for increased use Uncertainties associated with the increased use
of forecasting methods to predict mycotoxins on a of short season maize hybrids and silage
countywide-scale. There is a long history of the use
of models to predict crop diseases, including In eastern Canada, the use of maize silage in dairy
Fusarium head blight (De Wolf et al. 2003; Del production has increased approximately 5-fold over
Ponte et al. 2005; Carranza et al. 2007) however, the past 25 years. This is mainly attributed to the
there are comparatively few reports on models availability of short season maize hybrids suitable for
predicting the potential for mycotoxins in field both eastern North America and parts of western
crops – the most useful being developed Schaafsma Europe. In addition, as long as there is adequate
and colleagues (Hooker et al. 2002; Schaafsma et al. protein available, maize silage has a high starch
2006; Schaafsma and Hooker 2008). These models content and is a useful high-energy feed for cows
need to be developed against a large background (e.g. Dawo et al. 2007). Silage production has
dataset of DON and weather within a particular area remained fairly stable in most of Europe in recent
as the relationship between disease symptoms and decades but there has been a shift towards maize
toxin accumulation is cultivar-specific (Miller et al. silage in some countries (e.g. Denmark,
1984; Paul et al. 2006). Such work has also been The Netherlands; Wilkinson and Toivonen 2003).
attempted for Gibberella ear rot (Mansfield et al. In recent years, there has been increased recogni-
2006). tion that silage is quite frequently contaminated by
Although there are some recent studies on models toxins, mainly from Penicillium roqueforti (Seglar et al.
for predicting DON in wheat (Eiblmeier 2006; 1997; Auerbach et al. 1998; Seglar 1999). This
Forrer et al. 2006), only one predictive model for appears to be due to a combination of changes in feed
DON, DONcast, has been published and commer- production technology (e.g. increased reliance on
cialized (Hooker et al. 2002). This model, which maize fodder instead of transporting grain maize
adapted to Uruguay (Schaafsma et al. 2006) and from the Midwest US or southern Ontario) and/or
French conditions (Schaafsma and Hooker 2008), increased farm sizes (making it more likely that small
allows decision-makers to implement changes in changes in herd health will be noticed). At first, this
agronomic (fungicide application) or harvesting was, and often still is, attributed to the presence of
practices, to be aware where emerging DON low levels of Fusarium toxins in maize. Since these do
problems exist and to take the necessary manage- not affect cows or cattle, this is not the explanation.
ment steps. These might involve diverting the In contrast, a number of toxic phenomena in cows,
harvest from the affected fields away from human associated silage contaminated by P. roqueforti group,
food-use to alternative uses, including use in have been observed. Severe toxicoses in cows,226 J. D. Miller
associated with the latter fungi growing on silage, Acknowledgements
were first reported from Japan and the US in the
I thank colleagues at Agriculture Canada and
1960s ( Wei et al. 1973; Omomo et al. 1994). This
Carleton University, Clive James, Maya Pineiro,
issue remained unresolved and largely ceased to be a
Art Schaafsma, David Hooker, Kristian Nielsen,
practical problem. More recently, P. roquefori sensu
Jens Frisvad, as well as the Natural Sciences &
lato has been associated with reports of two syn-
Engineering Research Council of Canada and
dromes in cows: serious toxicoses associated with P.
TUBITAK, for financial support. I thank John
roqueforti and a general ill-thrift associated with P.
Gilbert and Hamide Z. Senyuva for inviting me to
paneum (Sumarah et al. 2005). Both of these fungi
discuss this topic.
produce roquefortine but the former produces PR
toxins and the later festuclavine, a compound long
associated with ill-thrift in cows (Nielsen et al. 2006;
O’Brien et al. 2006).
Good silage practice eliminates these fungi References
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