Received: 6 June 2017 | Revised: 21 September 2017 | Accepted: 19 October 2017

DOI: 10.1111/jfs.12422

ORIGINAL ARTICLE

Potentially toxigenic fungi from selected grains and grain

products

Vasiliki H. Tournas1 | Nicholas S. Niazi2

1
Center for Food Safety and Applied
Nutrition - FDA, College Park, Maryland
2
Georgetown University Medical School,
Georgetown University, Washington, DC
Correspondence
Vasiliki Tournas, Center for Food safety
and Applied Nutrition, HFS-711 Food and
Drug Administration 5001 Campus Drive
College Park, MD, USA.
Email: valerie.tournas@fda.hhs.gov
Abstract
A total of 85 grain and grain product samples (including corn meal, corn muffin mix, popcorn, vari-
ous types of rice, and self-rising, all-purpose unbleached and whole wheat flour) from U.S. retail
were tested for fungal contamination levels and profiles using conventional plating as well as
molecular methods. The results of this study showed that over 90% of wheat flour and corn prod-
uct samples and 73% of rice samples tested carried live fungi. Popcorn carried the highest fungal
levels reaching 5.45 log10 colony forming units (cfu) per gram followed by corn meal (reaching 5.38
log10 cfu/g). Mold and yeast counts in rice and wheat flour reached 3.30 log10 and 3.28 log10 cfu/
g, respectively. The predominant molds in wheat flour were aspergilli and fusaria found in 50 and
46% of samples, respectively; Fusarium spp. were the most frequent contaminants of corn-based
products found in 74% of the samples followed by penicillia (present in 44% of tested samples).
Rice, conversely, contained mainly Aspergillus, Fusarium, and yeasts (each found in 21% of the
samples).

Practical applications
Toxigenic molds are often contaminating stored grains and grain products and under improper
storage conditions could cause spoilage of these commodities accompanied with production of
toxic secondary metabolites, mycotoxins. Mycotoxins are known to cause illnesses in humans and
animals. Therefore, monitoring the presence and inhibiting the growth of these organisms is critical
for achieving and maintaining high quality products, suitable for human and animal consumption,
and free of health hazards. Establishing toxigenic mold profiles in stored grains and their deriva-
tives can point to correct storage management and thus reduction/elimination of spoilage and
mycotoxin production in these products. In this study we tested several corn, rice, and wheat flour
commodities for live potentially toxigenic fungal species. Our findings can help select proper
storage management techniques for these commodities.

1 | INTRODUCTION
Cereal grains usually carry a variety of fungi from the field (e.g., various
Fusarium and Alternaria species) and also contain some xerophilic
storage molds. The latter are capable of growing at very low water
activity (aw) and could cause spoilage during storage, if the moisture of
the commodity reaches levels above 12%. Determination of the myco-
logical quality of cereals and derived cereal products is a very important
issue since these commodities are used extensively as foods and animal
feeds and because some of the organisms encountered in these prod-
ucts are capable of producing toxic secondary metabolites, mycotoxins.
Past studies have reported that the most common molds causing
spoilage of cereals in storage are eurotia. Wallemia and a number of
aspergilli are also found in these commodities. Additionally, penicillia
(such as Penicillium citrinum, P. aurantiogriseum, P. brevicompactum,
P. chrysogenum, and P. crustosum) are present sometimes at high levels,
but it’s more likely that these organisms develop growth during drying
of the grains (Pitt & Hocking, 2009). Grain invasion and spoilage by the
storage fungi Aspergillus and Penicillium spp., and field molds such as
Alternaria and Fusarium was reported in past studies (Hernandez Nopsa
et al., 2015; Mislivec, 1981; Mislivec & Bruce, 1988; Talbot & Koehler,
2002). Mycotoxins, such as aflatoxins (AFs), deoxynivalenol (DON),

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https://doi.org/10.1111/jfs.12422
2 of 6 | TOURNAS
ochratoxin A (OTA), and B fumonisins (FBs), have also been found in
stored cereal grains (Birck, Lorini, & Scussel, 2006; Dhivya, 2013;
Magan, Aldred, Mylona, & Lambert, 2010; Mylona, Sulyok, & Magan,
2012; Talbot & Koehler, 2002). Food grade preservatives such as propi-
onate, sorbate, and benzoate salts as well as chemical fungicides have
been used to control spoilage of stored grains (Birck et al., 2006;
Magan et al., 2010; NASS-USDA, 2010; Vandegraft, Hesseltine, &
Shotwell, 1973). In recent years, however, there is a trend toward
reducing the use of certain pesticides or substituting them with other,
less toxic chemicals. Because disease management practices evolve
and different fungicides are used over time while utilization of some
old ones is discontinued, it is important to determine if such changes
have caused alterations in fungal profiles in grains and grain derivatives.
Therefore, we deemed it appropriate to revisit the issue of fungal con-
tamination in grains in an effort to assess the present mycological qual-
ity of these commodities.
2 | MATERIALS AND METHODS
2.1 | Materials
A total of 85 grain and grain product samples (including corn meal, corn
muffin mix, popcorn, various types of rice, and self-rising, unbleached
and whole wheat flour) were purchased from local supermarkets in the
Washington, DC area either in their unopened packages or from cov-
ered bulk trays and jars (1-lb portions or larger). All samples were kept
at room temperature under dry conditions from the time of purchase
until analysis commenced. Analysis was conducted within 48 hr from
the time of purchase.
2.2 | Chemicals, reagents and other supplies
Polymerase chain reaction (PCR) reagents and DNA ladder were pur-
chased from Fisher Scientific (Houston, TX); DNA extraction kits were
obtained from Norgen Biotek Corp. (Thorold, ON, Canada); primers
were purchased from Integrated DNA Technologies (Coralville, IA); and
agarose gels were obtained from Bio-Rad (Hercules, CA). All
mycological media utilized for the isolation and conventional plating
identification of fungal specimens were prepared in-house according to
methods and formulas described in the Bacteriological Analytical
Manual (BAM Online, 2001) and in Fungi and Food Spoilage (Pitt &
Hocking, 2009).
2.3 | Mold and yeast isolation and quantification
Samples were tested as follows: Fifty grams of each product were
aseptically removed and transferred to sterile blender jars. Subse-
quently, each sample was blended in 450 ml of 0.1% peptone for 45 s.
Serial dilutions of the homogenate (in 0.1% peptone) were surface
plated on duplicate DG18 agar plates (0.1 ml/plate) and plates were
incubated for 5 days at 258C. Colonies were counted and counts
were reported as colony forming units per gram (cfu/g); mold isolates
were purified on PDA agar (DIFCO, Detroit, MI) and further cultured
for microscopic examination and identification.
AND NIAZI
2.4 | Identification of isolated fungal strains
Recovered isolates were purified by reculturing on PDA agar plates and
identified to genus or species level using the conventional methods
and keys described in “Identification of Common Aspergillus Species”
(Klich, 2002), “A Laboratory Guide to Common Penicillium Species”
(Pitt, 1985), “Fusarium Species: An Illustrated Manual for Identification”
(Nelson, Toussoun, & Marasas, 1983), and “Fungi and Food Spoilage”
(Pitt & Hocking, 2009). Isolates that could not be identified by conven-
tional plating methods were speciated using molecular techniques as
described below.
2.5 | Molecular method
2.5.1 | DNA extraction
DNA from fungal strains recovered from various grains and grain
products was isolated as follows: The fungal isolates were grown on
solid media at 258C for 5 days; then a small culture portion from each
isolate was transferred to a 15-ml conical tube containing potato dex-
trose broth and incubated at 308C for 24 hr. After the incubation
period, samples were centrifuged for 10 min at 10,000 rpm to pellet
and the supernatants were discarded. Subsequently, 10 ml of PBS
buffer were added to each tube and the pellets were homogenized
using a vortex. The tubes were centrifuged again under the same as
above conditions and the supernatants were discarded. Then, 1 ml of
PBS buffer was added to each sample and the tubes were vortexed.
Subsequently, 50 ll were removed from each tube and transferred to
2.0-ml microcentrifuge tubes to proceed with DNA extraction. DNA
extraction was facilitated using the Norgen Biotek Fungi/Yeast
Genomic DNA Isolation Kit according to manufacturer’s instructions.
2.5.2 | PCR amplification and identification
PCR amplification of fungal DNA and speciation was accomplished
using the method described by Tournas, Niazi, and Kohn (2015).
3 | RESULTS
During the course of this study the mycological quality of corn and
corn-derived products, rice, and various wheat flours was examined.
One hundred percent of corn meal, 91% of popcorn and 94% of the
corn muffin mix samples carried live fungi. Corn meal, popcorn, and
corn muffin mix also had the highest mold infestation levels sometimes
reaching above 5.00 log10 cfu/g (Table 1). The most frequent fungi in
these commodities were fusaria with F. verticillioides predominating;
the latter was present in 80% of the cornmeal, 28% of corn muffin mix,
and 54% of the popcorn samples. A. flavus was also very common,
found in 60% of cornmeal and 45% of popcorn samples at levels some-
times exceeding 4.00 log10 cfu/g (Table 2). Penicillia were isolated from
all types of corn commodities examined here, but their levels were for
the most part low, not exceeding 2.50 log10 cfu/g. Only two cornmeal
samples had Penicillium counts above 4.20 log10 cfu/g, while one
popcorn sample carried 4.08 cfu/g of P. verruculosum. Trichoderma was
found in only one corn muffin mix sample but its levels were above
TOURNAS AND NIAZI | 3 of 6

TA BL E 1 Yeast and mold (YM) counts in various grains and grain those found in corn, not exceeding 3.30 log10 cfu/g in any of the sam-
products from U.S. retail ples. Aspergilli and fusaria were among the most common molds iso-
Number of a
YM counts range lated, occasionally reaching or exceeding 3.00 log10 cfu/g. A. flavus was
Product samples tested (log10 cfub/g) Frequencyc isolated from all commodities except Basmati rice. Black aspergilli were
Corn products found only in Basmati rice and whole wheat flour, while A. ochraceus
Cornmeal 10 3.69–5.38 100 (3.15 log10 cfu/g) was present in one Basmati rice sample. Low Alterna-
Corn muffin mix 18 <2.00–4.32 94
ria counts were found in all types of flour and in Basmati rice. Penicillia
Popcorn 11 <2.00–5.45 91
were present in whole wheat and unbleached flour and in Basmati rice,
Rice but their levels were lower than 3.00 log10 cfu/g. Low levels of eurotia
Basmati 16 <2.00–3.30 69
were found in self-rising and whole wheat flour and in some rice sam-
Otherc 8 <2.00–3.28 75
ples while yeasts were isolated from unbleached wheat flour and rice
Wheat flour
(Table 3). Yeast presence is mostly evident in products undergone
Self-rising 5 2.48–3.00 100
Unbleached 12 <2.00–3.11 83 extended processing and is usually associated with inadequate hygienic
Whole wheat 5 2.65–3.28 100 practices.
a
cfu 5 colony forming units.
b
Percent contaminated samples. 4 | DISCUSSION
c
This group included medium grain, parboiled and brown rice (two sam-
ples each), and white long grain and jasmine rice (one sample each).
Field fungi like Alternaria and Fusarium species were found in all prod-
ucts tested in this study. Fusarium spp. were found more frequently
4.00 log10 cfu/g. Low levels of Eurotium spp. were found only in one and at higher levels (sometimes exceeding 5.0 log10 cfu/g) in corn-
popcorn sample. Small numbers of yeasts were also present in all types based products such as cornmeal and popcorn. These findings are in
of corn products, but only one cornmeal sample reached 3.00 log10 agreement with results of past studies which demonstrated that corn
cfu/g (Table 2). contamination with fusaria was an on-going problem (Mislivec, Bruce,
Although live fungi were present in a high percentage of the wheat & Andrews, 1979; Vincelli & Parker, 2002). Lower levels of fusaria in
and rice samples, the levels of these contaminants were lower than corn muffin mix were probably due to destruction of these organisms

TA BL E 2 Fungal species and levels recovered from selected corn-derived products

Contamination levels (log10 cfua/g—range)

Organism Cornmeal (n 5 10)b Corn muffin mix (n 5 18) Popcorn (n 5 11)

Alternaria spp. ND c
<2.00–2.60 (11) d
ND

Aspergillus spp. ND <2.00–3.00 (11) <2.00–3.00 (27)

Aspergillus flavus <2.00–4.00 (60) ND <2.00–4.61 (45)

Aspergillus niger ND ND <2.00–3.08 (18)

Eurotium spp. ND ND <2.00–2.30 (9)

Fusarium spp <2.00–4.49 (20) <2.00–3.95 (33) <2.00–2.00 (9)

Fusarium verticillioides <2.00–5.30 (80) <2.00–3.30 (28) <2.00–5.45 (54)

Penicillium spp. <2.00–4.28 (20) <2.00–2.90 (39) ND

Penicillium aurantiogriseum ND <2.00–2.00 (6) ND

Penicillium oxalicum <2.00–2.78 (10) ND ND

Penicillium polonicum ND <2.00–2.00 (6) ND

Penicillium purpurogenum <2.00–4.48 (30) ND ND

Penicillium verruculosum ND ND <2.00–4.08 (18)

Trichoderma spp. ND <2.00–4.08 (6) ND

Yeasts <2.00–3.00 (10) <2.00–2.30) (22) <2.00–2.84 (18)

No growth (0) (6) (9)

a
cfu 5 colony forming units.
b
n 5 number of samples tested.
c
Numbers in parentheses indicate % samples contaminated with respective organisms.
d
ND 5 not detected.
4 of 6 | TOURNAS AND NIAZI

TA BL E 3 Fungal species and levels recovered from rice and wheat flour
Contamination levels (log10 cfua/g—range)
Wheat flour Rice
Organism Self-rising (n 5 5)b Unbleached (n 5 12) Whole wheat (n 5 5) Basmati (n 5 16) Otherc (n 5 8)

Alternaria spp. <2.00–2.30 (20)d <2.00–2.00 (8) <2.00–2.00 (20) <2.00–2.00 (12) ND

Aspergillus spp. <2.00–2.48 (20) <2.00–3.00 (8) <2.00–3.00 (40) <2.00–2.30 (6) <2.00–2.30 (25)

Aspergillus flavus <2.00–2.60 (40) <2.00–2.00 (8) <2.00–2.48 (20) ND <2.00–2.48 (12)

Aspergillus niger ND e
ND ND <2.00–2.30 (6) ND

Aspergillus ochraceus ND ND ND <2.00–3.15 (6) ND

Aspergillus terreus <2.00–2.95 (40) ND <2.00–3.08 (20) ND ND

Aspergillus tritici <2.00–2.00 (20) <2.00–2.30 (17) <2.00–2.60 (20) ND ND

Aspergillus tubingensis ND ND <2.00–2.48 (20) ND ND

Aspergillus versicolor <2.00–2.48) (20) ND ND ND ND

Cladosporium spp. <2.00–2.00 (20) ND <2.00–2.30 (20) ND <2.00–2.00 (12)

Eurotium spp. <2.00–2.00 (20) ND ND ND ND

Eurotium chevalieri <2.00–2.00 (20) ND <2.00–2.95 (40) ND <2.00–2.30 (12)

Eurotium repens ND ND ND ND <2.00–2.95 (12)

Eurotium rubrum ND ND <2.00–2.00 (20) ND ND

Fusarium spp <2.00–2.00 (60) <2.00–3.00 (42) <2.00–2.90 (40) <2.00–3.00 (12) <2.00–3.20 (38)

Fusarium graminearum ND <2.00–2.00 (8) ND ND ND

Fusarium verticillioides ND ND ND ND <2.00–2.30 (12)

Penicillium spp. ND <2.00–2.78 (17) ND <2.00–2.78 (25) ND

Penicillium brevissimum ND ND ND <2.00–2.00 (6) ND

Penicillium polonicum ND ND <2.00–2.00 (20) ND ND

Yeasts ND <2.00–2.30 (8) ND <2.00–2.90 (25) <2.00–2.48 (12)

No growth (0) (17) (0) (31) (25)

a
cfu 5 colony forming units.
b
n 5 number of samples tested.
c
This group included medium grain, parboiled and brown rice (2 samples each), and white long grain and jasmine rice (1 sample each).
d
Numbers in parentheses indicate % samples contaminated with respective organisms.
e
ND 5 not detected.

during processing. The frequent presence and high levels of Fusarium
spp. in some of the products are worrisome because these organisms
are capable of producing a wide spectrum of toxic secondary metabo-
lites such as FBs, DON, T-2 toxin, nivalenol (NIV), enniatins (ENNs),
and zearalenone (ZEA) with fumonisins being the most common Fusar-
ium toxins found in corn (Vincelli & Parker, 2002). Alternaria spp.,
although potentially toxigenic, were present in very low numbers and
probably are not of any significance. Low levels of aspergilli, penicillia,
and eurotia perhaps indicated that the water activities of the commod-
ities were low enough not to allow substantial growth of these organ-
isms during storage. Among the aspergilli recovered, A. flavus was
found at relatively high levels in cornmeal and popcorn; this is a cause
of concern since many strains of this organism are capable of producing
mycotoxins (B aflatoxins and/or cyclopiazonic acid) (Frisvad & Thrane,
2002). A. flavus as well as members of the genus Eurotium (A. glaucus
group) were found in grains and grain products during a study by Misli-
vec et al. (1979), whereas AF-tainted grain products were reported by
Cassel, Campbell, Draper, and Epperson (2001) and Trombete et al.
(2014).
Fusaria, aspergilli, eurotia, and Alternaria spp. were also recovered
from rice and wheat flour, but at much lower levels than the ones in
corn products. Mislivec et al. (1979) had repeatedly isolated Alternaria
spp. from wheat flour and brown rice while Birck et al. (2006) had
reported the presence of Aspergillus, Penicillium, and Fusarium species in
stored wheat grain. The most common molds isolated during the latter
study were aspergilli followed by fusaria. These investigators examined
the same wheat samples for mycotoxin contamination and found that
31% of the tested samples contained FB1. Several Fusarium species
(F. graminearum, F. avenaceum, F. poae, and F. culmorum) and their
toxins (DON, ZEA, ENNs, NIV, etc.) were also reported in a study on
TOURNAS AND NIAZI
stored wheat grain by Lindblad et al. (2013). According to this study,
F. avenaceum, F. poae, and F. graminearum were the most common
fusaria detected while ENNs were the most prevalent mycotoxins fol-
lowed by DON. Flour and other grain products made from mycotoxin-
containing grain can also carry active toxin, since most mycotoxins are
not completely destroyed by processing. Contamination of grain
products (e.g., wheat flour, bran, and processed maize) with Fusarium
mycotoxins such as DON, NIV, ZEA, HT-2, and T-2 toxins has been
reported in the literature (Schollenberger, Terry-Jara, Suchy, Drochner,
& Muller, 2002, 2005). Low levels of eurotia were found in wheat flour
and some rice samples. These organisms are deemed as the most com-
mon spoilers of grains in storage, but in our study they seemed to be
of minimal significance since their levels were limited.
Several Penicillium species were isolated during our study from var-
ious commodities tested; P. verruculosum, P. purpurogenum, P. aurantiog-
riseum (P. cyclopium), P. oxalicum, and P. polonicum were recovered from
corn products while P. polonicum was found in whole wheat flour and
P. brevissimum in Basmati rice. Among the isolated penicillia, only
P. verruculosum and P. purpurogenum were found at relatively high lev-
els. P. verruculosum is of certain significance since some members of
the species have the ability to produce the potent tremorgenic myco-
toxin verruculogen (VERR). VERR has been associated with tremor and
blockage of the Ca21-activated K1 in animals ingesting products conta-
minated with the toxin. P. purpurogenum is a rubratoxin (RT) producer.
RT is known to cause hepatotoxicity in animals (Lockard, Watson, Siraj,
Hayes, & O’Neal, 1981). Therefore, the presence of these organisms in
grains at elevated levels is troublesome and should be avoided. Past
studies have also shown the frequent incidence of Penicillium species in
grains and grain products (Mislivec, 1981; Mislivec et al., 1979). These
researchers reported the presence of P. cyclopium, P. viridicatum, P. bre-
vicompactum, and P. oxalicum in stored corn and P. urticae, P. cyclopium,
P. viridicatum, P. islandicum, and P. citrinum in small grains and/or wheat
flour. The Penicillium profiles reported by Mislivec and his co-workers
differ from ours perhaps due to different microbial control procedures
and other processes employed at that time and due to possibly
different product origination.
Specifications for fungal contamination of cereal grains and grain-
derived products acceptable by different manufacturers vary widely.
Berghofer, Hocking, Miskelly, and Jansson (2003), after analyzing over
600 samples from various wheat milling companies, concluded that
acceptable quality limits for mold and yeast in wheat flour would be
103 cfu/g. The International Commission on Microbiological Specifica-
tions for Foods (ICMSF) has set fungal tolerance for flour and cereal
products at 102–104 cfu/g (ICMSF, 1986). The fungal levels recovered
from some products during our study surpassed those recommended
by ICMSF.
Inhibition of mold growth in grains and prevention of mycotoxin
production and accumulation is crucial, because these metabolites are
stable at ambient temperature and very resistant to thermal processing
(Scudamore, 2005). Consumption of grain contaminated with mycotox-
ins is problematic as they cause serious acute or chronic illness in
humans and animals. In addition to health risks due to the presence of
mold/mycotoxin in grains and grain products, huge economic losses
| 5 of 6
can occur when the spoilage and toxin production are spread to large
grain amounts. Richard et al. (2003) reported an estimated annual
stored-grain loss of about 1 billion dollars due to mycotoxin contamina-
tion in the United States. Adherence to Good agricultural practices
(GAPs) and Good manufacturing practices (GMPs) during cultivation,
harvest, transport, and storage will help keep mold propagules at a min-
imum, thus resulting in negligible contamination of the stored product.
Another important factor affecting mold spoilage during storage is the
presence of various pests which can serve as vectors, transferring
spores, and other mold entities within and between storage units;
therefore, an effective pest control is crucial for the avoidance of mold
spreading and spoilage (Stack, 2000). Even when the best practices and
controls are employed, some mold contaminants will remain on the
harvested kernels and could grow under the right conditions. Since
mold growth and subsequent mycotoxin production are a function of
moisture and temperature, controlling these two parameters, at levels
unfavorable for fungal germination and proliferation, would result in
maintaining high quality product. Quick drying of grains and grain prod-
ucts to a moisture level below 12% (Aw < 0.60) and storage under cool
and dry conditions with sufficient aeration are essential for the produc-
tion and preservation of high quality grains, safe for human and animal
consumption.
5 | CONCLUSIONS
All types of grains and grain-derived commodities tested during the
course of this study contained potentially toxigenic molds. Some corn
meal and popcorn samples fostered high levels (over 4.0 log10 cfu/g) of
live fusaria and A. flavus, while a high percentage of wheat flour sam-
ples contained low levels of Aspergillus and Fusarium species. Some of
the rice samples were also contaminated with low levels of Aspergillus,
Penicillium, and/or Fusarium spp. The fungal levels recovered during this
study may not reflect the actual MYC contaminating these commod-
ities before refining, milling, and other postharvest treatments since
these types of processing may be detrimental to some fungi. Mycotox-
ins, which are not likely to be removed or inactivated by the above
processes, could still pose a health hazard. Therefore, testing for such
metabolites is advisable.
ACK NOWLE DGME NT S
We are indebted to Jeffrey Kohn (Office of Regulatory Affairs/FDA)
for his assistance during the preparation of the manuscript.
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How to cite this article: Tournas VH, Niazi NS. Potentially toxi-
genic fungi from selected grains and grain products. J Food Saf.
2017;e12422. https://doi.org/10.1111/jfs.12422