Microbiological Decontamination of Cereal Grains

Hypotheses in Food Science
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Current and Future Technologies for
Concise Reviews &
Microbiological Decontamination of Cereal Grains

Agata Los , Dana Ziuzina , and Paula Bourke
Abstract: Cereal grains are the most important staple foods for mankind worldwide. The constantly increasing annual
production and yield is matched by demand for cereals, which is expected to increase drastically along with the global
population growth. A critical food safety and quality issue is to minimize the microbiological contamination of grains as
it affects cereals both quantitatively and qualitatively. Microorganisms present in cereals can affect the safety, quality, and
functional properties of grains. Some molds have the potential to produce harmful mycotoxins and pose a serious health
risk for consumers. Therefore, it is essential to reduce cereal grain contamination to the minimum to ensure safety both
for human and animal consumption. Current production of cereals relies heavily on pesticides input, however, numerous
harmful effects on human health and on the environment highlight the need for more sustainable pest management and
agricultural methods. This review evaluates microbiological risks, as well as currently used and potential technologies for
microbiological decontamination of cereal grains.
Keywords: cereal grains, decontamination, food safety, microflora, microbial inactivation
Introduction Currently, industrial production of cereals relies heavily on

Cereals are one of the most important agricultural products chemical input of pesticides, which brings high economic ben-
in the world, both as human foods and as the main constituent efits, minimizes labor input and improves yield and quality of
of animal feed. Development of agriculture in prehistoric times agricultural products. However, pesticides can be harmful also
was heavily associated with domestication of cereal grains and to nontarget organisms and have negative effects on human health
since their first cultivation most civilizations have become de- and the environment. Resistance to pesticides in most major pest
pendent upon cereals for the majority of its food supply (Cordain, species is also increasing. In 2009, the Directive on the sustainable
1999). Cereal grains are the most commonly consumed food group use of pesticides was adopted by the EU and its overall objective is
worldwide and they are grown on about 60% of the cultivated land “to achieve the sustainable use of pesticides by reducing the risks
in the world (Harlan, 1992, Koehler & Wieser, 2013). In order and impacts of pesticides use on human health and environment
to meet the requirements of a growing world population, world- and promoting the use of integrated pest management and other
wide production and yield of cereals has been increased for the last nonchemical alternatives to pesticides” (European Commission
50 years (Figure 1) (Food and Agriculture Organization [FAO], [EC], 2009). Within the next decade, the new regulations will
2017). Major types of cereal grains include maize, rice, wheat, drastically reduce the number of active substances permitted in
barley, sorghum, millet, oats, and rye (Figure 2) (FAO, 2017). crop production, which drives the research to develop new disrup-
Worldwide significance and extensive use of cereal grains and tive technologies that are environmentally and societally accept-
their products makes cereals preservation and decontamination able control methods for cereal grains preservation. This review
one of the most important food safety issues. Contamination of compares currently used technologies with novel and potential
stored grain with insects and microorganisms is a major concern methods for microbial decontamination of cereal grains.
of the grain industry as it affects the grains both quantitatively and
qualitatively (Yadav, Anand, Sharma, & Gupta, 2014). Microor- Microbial Challenges Associated with Cereal Grains
ganisms present in cereals constitute a principle control point since
The sources of microbial contamination of cereals
their development may affect the safety, quality and properties of
the grains. Some molds can potentially produce harmful myco- Microbial contamination of cereal grains occurs during crop
toxins and pose a serious health risk for consumers (Laca, Mousia, growth, harvesting and postharvest drying and storage (Magan &
Dı́az, Webb, & Pandiella, 2006). Losses of cereal grains during Aldred, 2006) and it derives from several sources, including air,
storage are estimated between 5 and 30% due to molds and my- dust, water, soil, insects, birds and rodents feces as well as contam-
cotoxins, 5% for insects and 2% for rodents, with an average yield inated equipment and unsanitary handling (Figure 3). The type
loss of 1% for developed and 10% to 30% for developing countries of microbial contamination varies according to the growing re-
(Rajendran, 2002). It is essential to reduce cereal grain contam- gion and is heavily influenced by environmental conditions such
ination to the minimum and ensure safety both for human and as drought, rainfall, temperature, and sunlight, as well as unsanitary
animal consumption. handling, harvesting and processing equipment, and poor storage
conditions (Bullerman & Bianchini, 2009; Nierop, 2006). High
rainfall just before harvest is a factor inducing extensive coloniza-
tion of the grain ears by Alternaria spp., causing black fungi discol-
JFDS-2018-0080 Submitted 1/16/2018, Accepted 4/10/2018. Authors are with
the Food and Health Research Centre, School of Food Science and Environmental
oration, that can be observable both on the surface of the kernels
Health, Dublin Inst. of Technology, Dublin 1, Ireland. Direct inquiries to author and as beneath the pericarp (Kosiak, Torp, Skjerve, & Andersen,
Bourke (E-mail: [email protected]). 2004). Doohan, Brennan, and Cooke (2003) investigated the in-
fluence of climatic factors on Fusarium species pathogenic to cereal
C 2018 Institute of Food Technologists

R
1484 Journal of Food Science r Vol. 83, Iss. 6, 2018 doi: 10.1111/1750-3841.14181
Further reproduction without permission is prohibited
Decontamination methods of cereal grains . . .
Concise Reviews &

3000 6.0
Figure 1–Worldwide production and yields of
cereals in 1961 to 2014 (FAO, 2017).
Area harvested (million ha)
Production (million metric tonnes)
2500 5.0
Yield (tonnes/ha)
Million metrix tonnes / million ha
2000 4.0
Tonnes/ha
1500 3.0
1000 2.0
500 1.0
0 0.0
1961 1971 1981 1991 2001 2011
Year
Figure 2–Most commonly cultivated cereal

grains in 2014, by type (FAO, 2017).
grains and found that they differ significantly in their climatic dis- dominant bacterial species (Flannigan, 1996; Noots et al., 1999).
tribution as well as in the optimum climatic conditions required Numerous bacteria belonging to Streptomyces genus were recently
for their persistence. found on barley and spring wheat grains. The authors also re-
ported the presence of antimycin A toxin-producing strains in
The field microflora barley, which is the first report of antimycin A in a food substance
The field microflora consists of microorganisms that occur on or (Rasimus-sahari, Mikkola, Andersson, Jestoi, & Salkinoja-salonen,
in grains until the time of harvest and depends on the conditions 2016).
under which the crops were grown. The kernels are numerically Filamentous fungi and yeasts. The fungi growing on crops
dominated by bacteria, with yeasts as the next most abundant have been traditionally divided into two groups—“field” and
component. The number of filamentous fungi increases during “storage” fungi (Pitt & Hocking, 2009). The main difference
the later stage of ripening (Noots, Delcour, & Michiels, 1999; between these groups is the time at which they invade the grains
Flannigan, 1996; Nierop, 2006). and growth conditions, however, the distinction between field and
Bacteria. Levels of cereal grains contamination with bacte- storage fungi is not absolute. It was found that although some field
rial pathogens are usually very low and although contamination fungi invade the grains on the field, they are still able to grow in
with species such as Salmonella, Escherichia coli, and Bacillus cereus storage conditions. Similarly, some fungi commonly classified as
can occur, bacteria associated with cereals are generally non- storage fungi may invade the grains at earlier stages (Christensen
pathogenic. The most often they belong to the families Pseu- & Meronuck, 1986).
domonadaceae, Micrococcaceae, Lactobacillaceae, and Bacillaceae (Hock- Field fungi, including species such as Alternaria, Cladosporium,
ing, 2003; Laca et al., 2006). Some species of enteric bacteria that Fusarium, and Helminthosporium, invade grain in the field at high
are found on cereal grains are plant saprophytes and their presence relative humidities (90% to 100%) when the grain is high in
is not related to fecal contamination (Harris, Shebuski, Danyluk, moisture (18% to 30%) (that is, at high a ) (Bullerman & Bian-
w
Palumbo, & Beuchat, 2013). Gram-negative bacteria numerically chini, 2009) Christensen & Meronuck, 1986). Significant in-
dominate the microflora of preharvest barley, with Erwinia her- crease in a number of infections with Fusarium species is often
bicola (now: Pantoea agglomerans) and Xanthomonas campestris as pre-
Vol. 83, Iss. 6, 2018 r Journal of Food Science 1485

Concise Reviews & Decontamination methods of cereal grains . . .
F. avenaceum, and Microdochium nivale (formerly known as F. nivale)

cause diseases of small-grain cereals such as wheat and barley, corn
is usually attacked by F. graminearum, F. moniliforme, F. proliferatum,
and F. subglutinans (Doohan et al., 2003).
Hill and Lacey (1983) reported that by harvest even 50% to 85%
of barley kernels may be colonized by yeasts, with pink yeasts,
such as Sporobolomyces and Rhodotorula, being predominant (Flan-
nigan, 1996). Other species found on barley are Hansenula, Torulop-
sis, Candida, and Saccharomyces, while Cryptococcus and Trichosporon
were isolated from preharvest wheat (Flannigan, 1996). Flannigan
(1996) suggested that because of the strong resemblance between
other components of wheat and barley microfloras, similar yeasts
species are likely to be found on both cereals.
The storage microflora

Modern methods used for harvesting and proper storage prac-
tices ensuring the exclusion of water and lack of possibility for
birds, insects and rodents to contaminate the grain, are consid-
ered sufficient to prevent the microbial growth. However, these
conditions are not always met.
Bacteria. Generally, bacteria are not significantly involved in
the spoilage of dry grain due to storage conditions unfavorable
for their growth. However, it was found that some bacterial
pathogens and spore-forming species are able to survive dur-
ing storage and may contaminate processed products. Lactic acid
bacteria present in the raw grain may be carried over through
the processing and spoil doughs prepared from flour and cornmeal
(Bullerman & Bianchini, 2009; Justé et al., 2011). Gram-negative
coliforms, pseudomonads and actinomycetes were also found on
dry-stored cereals (Hill & Lacey, 1983). Wachowska, Stasiulewicz-
Paluch, Glowacka, Mikolajczyk, and Kucharska (2013) reported
that the number of bacteria of the genus Azotobacter colonizing
Figure 3–Sources and factors of microbial contamination during cereal winter wheat grain was relatively low at harvest, but the counts
grain processing. increased after 6 months of storage.
Filamentous fungi and yeasts. Spoilage of grains with fil-
amentous fungi during storage occurs usually due to inefficient
observed when ripening is performed during wet periods. Also, drying, what favors microbial growth and may result in increased
phyllosphere fungi are responsible for preharvest fungal contami- mycotoxins levels (Magan & Aldred, 2006; Harris et al., 2013). If
nation (Magan & Aldred, 2006). drying is delayed and the moisture content of the harvested grain
As high moisture content is required for field fungi, conditions is suitable, growth of the field fungi, for example, Fusarium spp.,
during the storage are not favorable for their growth, however, may occur (Flannigan, 1996).
some fungi including Penicillium and Fusarium species and various Storage fungi including species of Eurotium, Aspergillus, Penicil-
species of yeasts are able to invade seeds before harvest and con- lium, Rhizopus, Mucor, and Wallemia, invade stored-grains at low
tinue to grow during storage (Christensen & Meronuck, 1986). relative humidity’s (65% to 90%) and lower moisture contents
Although most Penicillium species are xerophiles and they usually (14% to 16%) of the grains (Bullerman & Bianchini, 2009). Stor-
are considered to be storage fungi, at certain conditions they can age temperature heavily influences the types and rates of microbial
also attack the grains before harvest – it was found that P. oxalicum spoilage – Penicillium species are dominant at cooler temperatures,
can infect preharvest maize due to insect damage or wounding while Aspergillus and Eurotium species are more common at am-
(Pitt & Hocking, 2009). bient temperatures (20 to 25 °C). Species of Rhizopus (common
Similarly, A. flavus, usually regarded as a storage fungus, was bread mold) and Neurospora (red bread mold) can also be found
found in freshly harvested maize (Lillehoj et al., 1976). Insect on grains at ambient temperatures, however, they are much more
damage to cobs and fungal invasion down the silks are the main common on baking products (Magan & Aldred, 2006).
factors increasing the risk of A. flavus contamination of corn (Lille- Among Penicillium species, P. verrucosum is important as contam-
hoj et al., 1980; Williams, Windham, Buckley, & Daves, 2006). ination with this fungus may result in the production of carcino-
The field fungus most frequently present in both barley and genic mycotoxin - ochratoxin a (OTA), especially in cool climates
wheat kernels is Alternaria (Christensen & Meronuck, 1986; Flan- (Lund & Frisvad, 2003). It was shown that P. verrucosum attacks
nigan, 1996). Kosiak et al. (2004) reported that the distribution wheat and barley only after harvest (Magan & Aldred, 2006; Pitt
of field fungi contamination varied significantly in wheat, bar- & Hocking, 2009). In tropical conditions other Penicillium species
ley and oats samples of reduced quality with dominant Fusarium are more common—P. citrinum is a fungus commonly detected in
species as compared to acceptable samples for which Alternaria was rice (Tonon, Marucci, Jerke & Garcia, 1997; Park, Choi, Hwang,
the most numerous. Fusarium species are a common contaminant & Kim, 2005; Trung, Bailly, Querin, Le Bars, & Guerre, 2001). In
of various cereal grains. While F. graminearum, F. culmorum, F. poae, maize, different Penicillium species occur depending on the stage
1486 Journal of Food Science r Vol. 83, Iss. 6, 2018

Concise Reviews &

of processing—some of them invade only preharvest grains neath the pericarp. A common result of invasion of the germs by
(P. funiculosum), other are associated only with the stored grain (P. Aspergillus species, such as A. restrictus, A. glaucus and A. candidus,
aurantiogriseum, P. viridicatum), whereas some species, such as P. cit- is germ-damaged wheat (the fungi grow only in the germ) that
rinum and P. oxalicum, are present all the time (Mislivec & Tuite, can often develop without visible sign of moldiness (Christensen
1970a, 1970b). & Meronuck, 1986). Bacon and Williamson (1992) investigated
Birck, Lorini, and Scussel (2005) compared fungal contamina- the interactions of F. moniliforme with corn. Studies based on scan-
tion in wheat grain during 180 days of storage. It was observed that ning electron microscopy showed distribution of the fungus mostly
Fusarium spp. was the most numerous fungus after harvest and after over the pericarp, however, contamination of the embryo and en-
30 days of storage, however, the counts decreased gradually until dosperm also occurred.
the end of the storage period. After 180 days of storage Aspergillus,
Fusarium and Penicillium were found in 96.7%, 46.7%, and 80.0% of Current and Potential Techniques for Control of Micro-
wheat samples, respectively. Krnjaja et al. (2015) investigated my- bial Spoilage of Cereal Grains
cobiota of maize—mycological analyses showed the presence of
Aspergillus, Fusarium, and Penicillium on both freshly harvested and Current techniques and their limitations
stored grains, however, the predominant species varied for each Current technologies applied to control microbial spoilage of
stage of processing. Similar observations were noted for maize— cereals successfully reduce the microbial load, however, they can
samples analyzed immediately after harvest showed predominance negatively affect the quality and technological properties of ce-
species of Alternaria, followed by species of Cladosporium and Peni- reals, as well as generate harmful environmental impacts. A brief
cillium, whereas after 120 days of storage the maize grains mycoflora description of current techniques and their limitations used for
consisted of various fungi belonging with predominance to Fusar- cereal grains preservation is summarized in Table 1.
ium, Aspegillus and Penicillum genera (Dudoiu, Cristea, Lupu, Popa, Pesticides. Worldwide cereal production heavily relies on pes-
& Oprea, 2016). ticides input, including fungicides, herbicides and insecticides.
Yeasts found on cereal grains during storage are often amylolytic The primary benefits of pesticides application are crop protec-
yeasts (Magan & Aldred, 2006). Similarly to lactic acid and spore- tion from the damaging influences of pests, higher yields and
forming bacteria, yeasts present on cereals may also be carried better quality of cereals. However, pesticides use raises several
through into processed products (Bullerman & Bianchini, 2009). concerns, related especially to its environmental impacts such as
biodiversity reduction, surface and ground water pollution, soil
Distribution of microorganisms within cereal grains contamination and decrease of fertility, as well as direct harmful
The typical structure of a cereal grain constitutes of three edible impact on humans and other nontarget species (Aktar, Sengupta,
parts: the bran which consists of the outer coat (pericarp, testa, & Chowdhury, 2009; Liu, Pan & Li, 2015). Repeated pesticide
and aleurone layers), the germ (the embryo) and the starchy en- use may lead to development of pesticides resistance in pest pop-
dosperm, and an inedible husk that protects the kernel (Figure 4) ulations previously susceptible to active agents used (Jess et al.,
(Dexter & Wood, 1996; Merali et al., 2013). Microbial coloniza- 2014). To reduce pesticides inputs and therefore the risks and
tion is generally restricted to the outer layers of cereal grains, impacts on human health and the environment, in 2009, the Eu-
that is, the husk, between the husk and pericarp, and within ropean Union introduced a strategy (EC, 2009) on the sustain-
the pericarp tissue (Briggs, 1998). Several studies showed that able use of pesticides through the use of Integrated Pest Manage-
after debranning—a controlled process in which the outer lay- ment (IPM), that is, combining chemical and nonchemical control
ers of the grains are removed, cereals are microbiologically purer methods and use alternative approaches such as nonchemical al-
(Bainotti & Perez, 2000; Laca et al., 2006). However, there are ternatives to reduce the reliability on pesticides (EC, 2009), which
species able to invade the inner part of the grains and penetrate is the most effective strategy to prevent the evolution of pesticide
into the endosperm, causing internal infections (Nierop, 2006). resistance.
Distribution of the microbial populations on various cereal Drying. Moisture content in the harvested cereal grains is nat-
grains has been studied by several authors. Microscopic observa- urally high. Drying is the phase of the postharvest processing dur-
tions of barley revealed a high number of microorganisms between ing which the grains are dried until the moisture content level
the husk and pericarp. It was observed that bacteria clustered as guaranteeing safe storage conditions, that is, equivalent to <0.70
randomly distributed micro-colonies with up to 200 cells (Petters, aw , is reached. A typical moisture content level of properly dried
Flannigan, & Austin, 1988). Laca et al. (2006) studied distribution grains is between 10% and 14%. Effective drying permits a reduc-
of microorganisms within wheat grains and found that most of tion of losses during storage, as it creates unfavorable conditions
bacteria and molds were concentrated on the surface of the grain for molds growth and proliferation of insects. However, these con-
in the pericarp surrounding the endosperm and the germ, there- ditions are not always met. Heat and moisture produced as a result
fore, removing some of the outer layers of the grains may be used of biological activity and respiration of grains during storage, are
to substantially reduce the microbial contamination. According major factors influencing spoilage. Damp or warm spots of grain
to the study, most of the contamination is located in the outer favor fungal growth, which leads to further production of heat
layers, that is, the first and second pearling fractions, which corre- and moisture, creating a self-generating process (Magan & Aldred,
sponds to a layer thickness of approximately 30 µm. Colonization 2006; Mrema, Gumbe, Chepete, & Agullo, 2011).
of the grains by Alternaria spp. (black fungi discoloration) is ob- One of the important limitations of grains drying is a difficulty
servable on the surface of the kernels as well as beneath the peri- to achieve a sufficient uniformity of the process as under- or
carp of wheat, barley and oats, and is believed to be a result of over-dried areas leads to grains with different moisture contents
rainfall just before harvest (Kosiak et al., 2004). Andersen and to be found in the same batch (Magan & Aldred, 2006; Raghavan,
Thrane (2006) reported that wheat and barley surface disinfection 1993). Using excessive temperatures damages grains, for example,
with sodium hypochlorite removed only 10–15% of Alternaria and cracking and loss of viability, as well as may cause economic losses.
Bipolaris, which indicates that the grains were contaminated be- For instance, 1 kg of grains at 15% moisture content weighs 885.4 g

Figure 4–Microbial contamination within

a cereal grain.
Table 1–Current methods and technologies used for cereal grains preservation.
Method/technology Description Limitations References

r
Pesticides Chemicals designed to prevent and control
the occurrence of pests causing harm
r High environmental impacts
Direct negative impact on human
Liu et al. (2015); Jess et al. (2014);
Aktar et al. (2009)
to crops - molds (fungicides), weeds
(herbicides) and insects (insecticides)
r health
Increasing resistance against
pesticides
r
Drying Grains are dried to a low moisture content
r Lack of uniformity of the process
Over-drying may damage
Varga et al. (2010); Magan & Aldred,
2006
the grains and cause economic
losses as well as increase
mycotoxin contamination
Debranning Process during which the bran layers are
r Not completely suitable for wheat Laca et al. (2006); Dexter and Wood
removed from the endosperm by friction due to the crease on the wheat (1996)
and abrasion
r kernels
Whole-grain demand in
the market
Chlorine and Due to their oxidizing capacity, chlorine and
r Low inactivation of fungal spores Delaquis and Bach (2012); Virto et al.
hypochlorite hypochlorite treatments are one of the on cereal grains&&generation of (2005); Andrews et al. (1997); Sauer
most widely used processes for microbial toxic by-products after and Burroughs (1986)
control the treatment
Irradiation Exposing food to a certain amount of
r Can negatively modify the quality Lung et al. (2015); Farkas et al. (2014);
ionizing radiation and technological properties of Lynch, Tauxe, and Hedberg (2009)
cereals and cereal products
Ozone Triatomic oxygen formed by addition of
r The cost of treatment can be Greene et al. (2012); Environmental
a free radical of oxygen to molecular relatively high due to complex Protection Agency [EPA] (1999)
oxygen technology
at 4% moisture content, causing a loss in the value in the market starchy endosperm is difficult to achieve in the debranning process
(Yaciuk, 1980; Mrema et al., 2011). Also, it increases the risk of (Dexter & Wood, 1996).
growth of mycotoxin producing molds, which usually colonize Chlorine and hypochlorite. Due to their oxidizing capacity,
only damaged parts of plants (Varga, Kocsube, Peteri, Vagvolgyi, chlorine-based methods are widely used in the industry for food
& Toth, 2010). produce disinfection and microbial control. These techniques are
Mechanical debranning. Debranning is an advanced milling inexpensive and easy to use; however, they bring concerns due
process during which the bran layers of a grain are separated to generating toxic by-products as well as off-tastes and odours
from the endosperm and removed by friction and abrasion. This after the treatment (Richardson et al., 1998; Virto, Manas, Al-
technique can improve the yield and degree of refinement of flour, varez, Condon, & Raso, 2005). The need to reduce environmental
as well as allowing the production of good-quality milled prod- chlorine emissions has led to the consideration of nonchlorinated
ucts from lower quality grains (Dexter & Wood, 1996). Laca et al. alternatives.
(2006) showed that after debranning, grains are microbiologically It was found that using chlorine for inactivation of microor-
purer. It was reported that by removal from the surface of 4% ganisms on cereal grains was ineffective for highly contaminated
of the total weight of the grain, that the total microbial contam- products - 0.4% chlorine solution did not inactivate sufficient
ination was reduced up to 87%. Due to the complex anatomy fungal spores to produce less than 20% contamination when ini-
of a wheat kernel which has a longitudinal crease that extends tial contamination levels were greater than 104 per gram of barley
to the center of the kernel, complete separation of the bran from (Andrews, Pardoel, Harun, & Treloar, 1997; Delaquis & Bach,

Concise Reviews &

2012). Sodium hypochlorite has also been used frequently, how- was a very effective method for inactivation of 96.9% of fungal
ever, studies show that this kind of treatment does not completely spores associated with wheat. In this study, higher treatment effi-
inactivate fungal spores neither on the surface of corn nor wheat cacy was achieved when temperature and water activity of wheat
(Sauer & Burroughs, 1986; Sun et al., 2017). were increased, what confirms the results obtained by Allen et al.
Irradiation. Irradiation in food processing is a process that (2003). Bactericidal effect of ozone was observed by Naito, Okada,
involves exposing food to a certain amount of ionizing radia- and Sakai (1988)—gaseous ozone inactivated up to 3 log units of
tion. Three major types of this technology are: (a) gamma-rays Bacillus spp. and Micrococcus spp. on cereal grains, peas, beans and
generated from the radioactive isotopes of cobalt-60 (60 Co) or spices. It was also found that the treatment efficacy depends on
cesium-137 (137 Cs); (b) electron beam processing; (c) X-rays cre- ozone concentration, relative humidity and treatment tempera-
ated by electron accelerators. The mechanism of microbial inacti- ture. Dodd et al. (2011) investigated the effect of ozonation on
vation by irradiation includes direct DNA damage and the produc- malting barley—the treatment did not lead to significant reduc-
tion of reactive molecules, such as hydrogen peroxide, hydroxyl tions in aerobic plate counts, but it decreased mold and yeast counts
radicals and hydrogen atoms. These molecules can damage cellular by 1.5-log in the final malt. In the study, gaseous ozone did not
metabolic pathways inside the cells, promote intracellular oxida- negatively influence any aspect of malt quality.
tion and consequently lead to cell lysis (Farkas, Ehlermann, & Ozonated water was also reported to be effective for microbial
Mohácsi-Farkas, 2014; Lung et al., 2015). inactivation of a range of foods, including grains, and can be an
Irradiation has been successfully used for control of microor- alternative to chlorinated water before milling. Dhillon, Wiesen-
ganisms on cereals and flours since 1950s (comprehensively re- born, Dhillon, and Wolf-Hall (2010) found that although washing
viewed by Lorenz & Miller, 1975). The use of 0.5 kGy radiation durum wheat grains with ozonated water did not show high an-
for the prevention of pest contamination in wheat and flour was timicrobial efficacy when used alone, it was effective in combina-
approved by the United States Food and Drug Administration tion with acetic acid. Similarly, a combination of gaseous ozone,
(USFDA) in 1963 and the technology has been applied for preser- acetic acid, and ozonated water, using a fluidized bed system, was
vation and decontamination of various crops (Lung et al., 2015). the most effective in reducing microbial counts on durum wheat
Ozone. The use of ozone in food processing has become in- in another study (Dhillon et al., 2010). In both studies, however,
creasingly important since it gained GRAS (Generally Recognized grain moisture content increased after the treatment.
as Safe) status in 1997 (Graham et al., 1997) and four years later
it was approved by US Food and Drug Administration (FDA) as
a secondary direct food additive and antimicrobial agent for all Future trends for decontamination of cereal grains
food types (O’Donnell, Tiwari, Cullen, & Rice, 2012). Ozone Limitations of conventional methods used for inactivation of
(O3) is the triatomic oxygen formed by addition of a free radical microorganisms associated with cereals suggest that there is a huge
of oxygen to molecular oxygen. When generated from dried air, demand for new technologies, which will be rapid and cost ef-
ozone is a blue gas. Ozone generation from high-purity oxygen fective. An ideal method should reduce microbial loads uniformly
leads to formation of a colorless gas (Greene, Guzel-Seydim, & on all the treated grains, without formation of toxic, nontarget
Seydim, 2012). Ozone can be applied in the gaseous or aqueous residues and by-products after the treatment. Potential techniques
state. It has been demonstrated that after treatment ozone decom- for cereals preservation (Table 2) should not affect their quality as
poses into molecular oxygen and hence does not leave hazardous the consumers expect high-quality processed foods with minimal
residues on the food product (Graham et al., 1997). changes in nutritional and sensory properties.
Microbial inactivation by ozone have been studied against a wide Microwave (MW) treatment. Microwaves are electromag-
variety of microorganisms. The bactericidal effect of ozone has netic waves with frequency within 300 MHz to 300 GHz (Chan-
been studied against both Gram-positive and Gram-negative bac- drasekaran, Ramanathan, & Basak, 2013). Microwave inactiva-
teria as well as spores and vegetative cells. Microbial inactivation by tion of microorganisms is achieved at temperatures lower than
ozone is a complex process—Victorin (1992) identified two major that of conventional pasteurization, however, many studies sug-
mechanisms of ozone destruction of microorganisms: (1) oxida- gest that microwaves inactivate microbes mainly by a thermal ef-
tion of sulfhydryl groups and amino acids of enzyme, peptides fect, including irreversible heat-denaturation of enzymes, proteins,
and proteins to shorter peptides; and (2) oxidation of polyunsat- nucleic acids or other cellular constituents, leading to cell death.
urated fatty acids to acid peroxides. Disruption or disintegration a second possible mode of action are nonthermal (“athermal”)
of the cell envelope leads to cell lysis and inactivation of microor- effects, caused by the intrinsic nature of microwaves and not re-
ganisms (Greene et al., 2012). lated to increase of the temperature during the MW treatment
The use of ozone as a fungicide for decontamination of cereal (Heddleson & Doores, 1993). It was found that higher microbial
grains has been investigated in several studies. Kells, Mason, Maier, reduction levels of microwave treatment are achieved in presence of
and Woloshuk (2001) used gaseous ozone to reduce the contami- other stresses, such as acidic pH or increased temperature (Kozem-
nation level of Aspergillus parasiticus on the kernel surface of corn pel, Annous, Cook, Scullen, & Whiting, 1998). Kozempel et al.
by 63%. In another study (Allen, Wu, & Doan, 2003), 96% of (1998) emphasizes that efficacy of using microwave energy for mi-
inactivation was achieved for spores or a mixture of spores and crobial inactivation depends on the type of microorganism-food
a small number of mycelia on barley after 5 min of treatment. system.
It was observed that increases in water activity and temperature The number of studies investigating microwave treatment for
of grains enhanced the fungicidal efficacy of ozone. Kottapalli, inactivation of microorganisms associated with cereal grains is
Wolf-Hall, and Schwarz (2005) reported a significant decrease limited. Reddy, Raghavan, Kushalappa, and Paulitz (1998) suc-
(24% to 36%) of Fusarium survival after 15 min of exposure at cessfully reduced the seedborne F. graminearum infection of wheat
either 11000 or 26000 ppm ozone concentration in naturally in- to below 7%, maintaining the commercially acceptable seed ger-
fected malting barley. Wu, Doan, and Cuenca (2006) used gaseous mination threshold, that is, 85%. It was observed that seed viabil-
ozone to preserve stored wheat and found that ozone treatment ity and seedling vigour decreased after the microwave treatment.

Table 2–Potential methods and technologies for cereal grains preservation.
Method/technology Description Limitations References

Microwave (MW) Electromagnetic waves with frequency
r Seed viability and seedling vigour can Chandrasekaran et al. (2013);
treatment within 300 MHz to 300 GHz; microbial
inactivation based mainly on thermal effect
r be decreased after the treatment
Higher microbial reduction levels in
Reddy et al. (1998);
Kozempel et al. (1998); Heddleson
presence of other stresses, such as acidic and Doores (1993)
pH or increased temperature
Pulsed UV light Short-duration, high-power pulses of a broad
r Low ability to penetrate grains because Barbosa-Canovas, Schaffner, Pierson,
spectrum of white light from the UV (50%
of the spectrum), to the near infrared
r of their irregular and complex surface
Can decrease germination rate of
and Zhang (2000); Maftei et al.
(2013); Keklik et al. (2012);
region the seeds Keklik, Demirci, and Puri (2010)
Nonthermal (cold) Partially ionized gas consisting of highly
r Efficiency of the method depends on Niemira (2012); Schlüter et al. (2013)
plasma reactive chemical species the specific properties of the food
product and its surface
Organic acids Antimicrobial agents due to the reduction of
r Can increase moisture content and Sabillon et al. (2016, 2017); Ölmez
the environmental pH penetrate into the endosperm of grains and Kretzschmar (2009)
Microwave energy can also be used for control of stored-grain Cold plasma can be generated at atmospheric as well as low
insects (Vadivambal, Jayas, & White, 2007). pressure and consists of UV photons, neutral or excited atoms
Pulsed ultraviolet (UV) light treatment. Pulsed UV light and molecules, negative and positive ions, free radicals, and free
treatment is an emerging nonthermal technology that can be used electrons. The technique has recently found an extensive range of
both for decontamination of foods and food contact surfaces. It applications for microbiological decontamination due to chemical
involves the use of short-duration, high-power pulses of a broad and bioactive radicals generated during electrical discharge, includ-
spectrum of white light from the ultraviolet (UV), which makes ing reactive oxygen species (ROS), and reactive nitrogen species
50% of the total spectrum, to the near infrared region (Keklik, (RNS) (Laroussi & Leipold, 2004; Scholtz, Pazlarova, Souskova,
Krishnamurthy, & Demirci, 2012). Pulsed UV light is considered Khun, & Julak, 2015).
to be more efficient in microbial inactivation than continuous UV Application of cold plasma for decontamination of cereal grains
light, offering a safer and faster decontamination (Krishnamurthy, has been studied recently. Selcuk, Oksuz, and Basaran (2008) stud-
Tewari, Irudayaraj, & Demirci, 2010). Microbial inactivation by ied the low pressure cold plasma inactivation of two pathogenic
UV light, which can be classified into four spectrum regions, is fungi, Aspergillus spp. and Penicillum spp. artificially inoculated on
primarily due to DNA structure alternation. UV-C light, with surface of various seeds, including wheat, barley, rye, and corn.
the peak of maximum effectiveness at wavelengths of about 260– Within 15 min of plasma treatment the fungal attachment to seeds
265 nm what corresponds with the peak of maximum DNA ab- was reduced below 1% of initial load. The treatment efficacy
sorption, is the most effective for inactivating microorganisms. was dependent on the initial contamination level of the seeds.
Formation of cyclobutane pyrimidine dimers during UV light In the study, the germination quality of the seeds remained unaf-
treatment leads to mutagenesis and cell death (Gayán, Condón, fected after the treatment. Filatova et al. (2013) used RF air plasma
& Álvarez, 2014). Although the technology is able to kill vegeta- for treatment of maize, spring wheat and lupinus seeds. The re-
tive cells and bacterial spores, as well as fungal spores and viruses, sults showed that the treatment reduced both bacterial and fungal
it has not been applied yet at industrial scale in food processing contamination of tested seeds, as well as positively influenced their
(Keklik et al., 2012; Ortega – Rivas, 2012). germination. Kordas, Pusz, Czapka, and Kacprzyk (2015) investi-
Although it is believed that pulsed UV light is not an ade- gated the effect of “packed bed” low temperature plasma on fungi
quate technology for cereals due to their rough and uneven sur- colonizing winter wheat grain. It was found that plasma treat-
faces (Oms-oliu, Martı́n-belloso, & Soliva-fortuny, 2010), the an- ment resulted in the reduction of the number of colonies of fungi
timicrobial efficacy of this technology against microorganisms on grains, however, the reduction varied heavily for the fungal
occurring on stored cereal grains has been demonstrated. Maftei, species examined. Brasoveanu, Nemtanu, Surdu-Bob, Karaca, and
Ramos-villarroel, Nicolau, Mart, and Soliva-fortuny (2013) stud- Erper (2015) applied glow discharge plasma to barley and corn
ied the potential of pulsed light technology for the decontamina- seeds to reduce the number of seed-borne fungi and found that
tion of naturally occurring molds on wheat grains and achieved the fungal loads decreased with the increasing plasma treatment
a reduction of about 4 log CFU/g, with the seed germination per- times. After 20 min treatment the initial number of fungi was
centage slightly decreased. It was also found that the initial mold decreased by 25% for barley seeds. In the same study, treatment
load of grains is an important factor for the treatment efficacy. of 10 min reduced the fungal load on corn seeds by 40%. In dif-
Nonthermal (cold) plasma. Plasma, considered as a fourth ferent study, wheat grains artificially contaminated with Bacillus
state of matter, is a partially or fully ionized gas. The terminology amyloliquefaciens endospores, were treated using low pressure cir-
“cold” or “nonthermal” describing plasmas refers to the physical culating fluidized bed reactor. Within 30 s of treatment, the reduc-
parameter. As compared to thermal plasmas generated at high tem- tion by over two logarithmic units was achieved (Butscher et al.,
peratures, cold plasmas are generated at or near room temperature, 2015). Butscher, Zimmermann, Schuppler, and Rudolf von Rohr
therefore, mechanism of microbial inactivation does not rely on (2016) investigated the inactivation of Geobacillus stearothermophilus
thermal destruction of microorganisms. As a nonthermal process, endospores deposited on either polypropylene substrates or wheat
cold plasma causes little or no thermal damage to the food product grains. It was observed that endospore inactivation is possible on
after treatment (Niemira, 2012; Niemira, Boyd, & Sites, 2014). wheat grains, however, it is much more challenging than the

Concise Reviews &

treatment of PP granules, possibly due to a grain anatomy— ment, whilst at the same time do not affect the grains quality.
a rough surface and a deep ventral furrow. Cold plasma effect Prevention of contamination with fungi is the most rational and
on various microorganisms on wheat seeds has also been inves- economical approach to reduce the risks associated with the pres-
tigated by Zahoranova et al. (2015). Treatment of 120 s reduced ence of mycotoxins in cereal food and feed products. However, in
the natural microflora of wheat seeds—reduction of 1 log CFU/g current production systems even the best agricultural and manu-
was achieved for bacteria, while yeasts and filamentous fungi were facturing practices cannot fully prevent mycotoxin contamination,
completely inactivated. Inactivation levels of wheat seeds artifi- therefore, potential technologies will need to be used for degra-
cially contaminated with filamentous fungi (F. nivale, F. culmo- dation and elimination of these toxic metabolites.
rum, T. roseum, A. flavus, and A. clavatus) were hugely depen-
dent on the fungal type, with Aspergillus spp. as the most resistant Acknowledgments
to the treatment. Dasan, Boyaci, and Mutlu (2017) achieved sig- This work was funded through Science Foundation Ireland (SFI)
nificant reductions of 5.48 and 5.20 log (CFU/g) of A. flavus and under Grant Number 14/IA/2626.
A. parasiticus inoculated on maize after 5 min air plasma treatment,
as well as more than 3 log reduction after 3 min of native microbial References
flora of maize grains. Aktar, W., Sengupta, D., & Chowdhury, A. (2009). Impact of pesticides use in agriculture:
Their benefits and hazards. Interdisciplinary Toxicology, 2(1), 1–12. https://doi.org/10.2478/
Except of cereal grains, cold plasma has been also used for v10102-009-0001-7
decontamination of grain-like granular particles (Basaran, Basaran- Allen, B., Wu, J., & Doan, H. (2003). Inactivation of fungi associated with barley grain by
Akgul, & Oksuz, 2008; Dasan et al., 2017; Dasan, Boyaci, & gaseous ozone. Journal of Environmental Science and Health. Part. B, Pesticides, Food Contaminants,
and Agricultural Wastes, 38(5), 617–630. https://doi.org/10.1081/PFC-120023519
Mutlu, 2016; Deng, Shi, & Kong, 2006; Hertwig et al., 2015a; Andersen, B., & Thrane, U. (2006). Food-borne fungi in fruit and cereals and their production
Hertwig, Reineke, Ehlbeck, Knorr, & Schluter, 2015b; Vleugels of mycotoxins. Advances in Experimental Medicine and Biology, 571, 137–152. https://doi.org/
10.1007/0-387-28391-9_8
et al., 2005) and bacterial contaminants in grain model media (Los, Andrews, S., Pardoel, D., Harun, A., & Treloar, T. (1997). Chlorine inactivation of fungal spores
Ziuzina, Boehm, Cullen, & Bourke, 2017). on cereal grains. International Journal of Food Microbiology, 35(2), 153–162. https://doi.org/
10.1016/S0168-1605(96)01214-7
Organic acids. Organic acids are used as food additives and Bacon, C. W., & Williamson, J. W. (1992). Interactions of Fusarium moniliforme, its metabolites and
preservatives due to the reduction of the environmental pH, what bacteria with corn. Mycopathologia, 117(1–2), 65–71. https://doi.org/10.1007/BF00497280
Bainotti, A. E., & Perez, E. S. (2000). Microbiological evaluation of processed rice consumed in
prevents food deterioration (Ölmez & Kretzschmar, 2009). Addi- Japan. World Journal of Microbiology and Biotechnology, 16, 77–79.
tion of organic acids such as propionic, sorbic, and acetic acids, as Barbosa-Canovas, G. V., Schaffner, D. W., Pierson, M. D., & Zhang, Q. H. (2000).
Pulsed light technology. Journal of Food Science, 65, 82–85. https://doi.org/10.1111/j.1750-
well as their salts, prevent the mold spoilage of bakery products, 3841.2000.tb00621.x
however, relatively high concentrations are needed due to low ef- Basaran, P., Basaran-Akgul, N., & Oksuz, L. (2008). Elimination of Aspergillus parasiticus from nut
surface with low pressure cold plasma (LPCP) treatment. Food Microbiology, 25(4), 626–632.
ficacy (Magan & Aldred, 2006). Organic acids can also be used for https://doi.org/10.1016/j.fm.2007.12.005
grain preservation. Sabillon, Stratton, Rose, Flores, and Bianchini Birck, N. M. M., Lorini, I., & Scussel, V. M. (2005). Fungus and mycotoxins in wheat grain at
post harvest. Paper presented at International Working Conference on Stored Product Protection, Sao
(2016) evaluated the efficacy of adding organic acids (acetic, cit- Paolo, Brazil. Passo Fundo, RS, Brazil: Brazilian Post-harvest Association.
ric, lactic, or propionic) or combination of organic acids and NaCl Brasoveanu, M., Nemtanu, M. R., Surdu-Bob, C., Karaca, G., & Erper, I. (2015). Effect of
added to tempering water to reduce microbial contamination in glow discharge plasma on germination and fungal load of some cereal seeds. Romanian Reports
in Physics, 67(2), 617–624.
hard wheat and noted a significant reduction of microbial load af- Briggs, D. E. (1998). Malting and brewing science. London, UK: Blackie Academic & Professional.
ter the treatment. It was reported that the combination lactic acid Bullerman, L. B., & Bianchini, A. (2009). Food safety issues and the microbiology of cereals and
cereal products. In N. Heredia, I. Wesley, & S. Garcia (Eds.), Microbiologically safe foods (pp.
(5.0%) and NaCl (52%) was the most effective against aerobic plate 315–335). New York, U.S.A.: John Wiley & Sons.
count (APC) and Enterobacteriaceae (Eb), achieving an average re- Butscher, D., Schlup, T., Roth, C., Müller-Fischer, N., Gantenbein-Demarchi, C., & Rudolf
Von Rohr, P. (2015). Inactivation of microorganisms on granular materials: Reduction
duction of 4.3 and 4.7 log CFU/g, respectively. In a further study, of Bacillus amyloliquefaciens endospores on wheat grains in a low pressure plasma circulat-
the impact of tempering solutions on the functional properties of ing fluidized bed reactor. Journal of Food Engineering, 159, 48–56. https://doi.org/10.1016/
j.jfoodeng.2015.03.009
resulting whole-grain (WGF) and straight-grade flours (SGF) was Butscher, D., Zimmermann, D., Schuppler, M., & Rudolf von Rohr, P. (2016). Plasma inactiva-
evaluated and it was found that tested solutions had different effects tion of bacterial endospores on wheat grains and polymeric model substrates in a dielectric bar-
rier discharge. Food Control, 60, 636–645. https://doi.org/10.1016/j.foodcont.2015.09.003
on the properties of each type of flour. While tempering solutions Chandrasekaran, S., Ramanathan, S., & Basak, T. (2013). Microwave food processing – a review.
did not have significant overall effects on pasting or mixing prop- Food Research International, 52(1), 243–261.
Christensen, C. M., & Meronuck, R. A. (1986). Quality maintenance in stored grains and seeds.
erties of SGF, treatment of WGF resulted in a numeric decrease in Minneapolis, U.S.A.: University of Minessota Press.
several pasting parameters and an increase in bread grittiness, indi- Cordain, L. (1999). Cereal grains: Humanity’s double-edged sword. World Review Nutrition Diet,
84, 19–73. https://doi.org/10.1186/1550-2783-10-30
cating limited penetration of the organic acids into the endosperm Dasan, B. G., Boyaci, I. H., & Mutlu, M. (2017). Nonthermal plasma treatment of Aspergillus spp.
of the grain (Sabillon, Bianchini, Stratton, & Rose, 2017). spores on hazelnuts in an atmospheric pressure fluidized bed plasma. Journal of Food Engineering,
196, 139–149. https://doi.org/10.1016/j.jfoodeng.2016.09.028
Dasan, B. G., Mutlu, M., & Boyaci, I. H. (2016). Decontamination of Aspergillus flavus and
Conclusions Aspergillus parasiticus spores on hazelnuts via atmospheric pressure fluidized bed plasma
Potential microbiological risks associated with cereal grains re- reactor. International Journal of Food Microbiology, 216, 50–59. https://doi.org/10.1016/
j.ijfoodmicro.2015.09.006
main a major concern of the grain industry as they may hugely Delaquis, P., & Bach, S. (2012). Resistance and sublethal damage. Produce contamination. In
affect the quality and properties of the grains. Current technolo- V. M. Gomez-Lopez (Ed.), Decontamination of fresh and minimally processed produce (pp. 77–86).
N.J., U.S.A.: Wiley-Blackwell Publishing.
gies applied for control of microbial spoilage of cereals success- Deng, X. T., Shi, J., & Kong, M. G. (2006). Physical mechanisms of inactivation of Bacillus subtilis
fully reduce the microbial load, however, they can negatively af- spores using cold atmospheric plasmas. IEEE Transactions on Plasma Science, 34, 1310–1316.
Dexter, J. E., & Wood, P. J. (1996). Recent applications of debranning of wheat before
fect the quality and technological properties of cereals, as well as milling. Trends in Food Science & Technology, 7(2), 35–41. https://doi.org/10.1016/0924-
generate harmful environmental impacts. In order to overcome 2244(96)81326-4
Dhillon, B., Wiesenborn, D., Dhillon, H., & Wolf-Hall, C. (2010). Development and evaluation
the limitations of conventional technologies, recent works have of a fluidized bed system for wheat grain disinfection. Journal of Food Science, 75(6), E372–8.
been focused on developing new techniques, such as microwave https://doi.org/10.1111/j.1750-3841.2010.01668.x
Dodd, J. G., Vegi, A., Vashisht, A., Tobias, D., Schwarz, P., & Wolf-Hall, C. E. (2011). Effect of
treatment, pulsed UV light, cold plasma and organic acids, that can ozone treatment on the safety and quality of malting barley. Journal of Food Protection, 74(12),
be used for microbial decontamination of cereals. Further studies 2134–2141. https://doi.org/10.4315/0362-028X.JFP-11-193
Doohan, F. M., Brennan, J., & Cooke, B. M. (2003). Influence of climatic factors on Fusar-
are needed to ensure that these potential technologies could pro- ium species pathogenic to cereals. European Journal of Plant Pathology, 109(7), 755–768.
vide an efficient microbial inactivation and rapid, uniform treat- https://doi.org/10.1023/A:1026090626994

Dudoiu, R., Cristea, S., Lupu, C., Popa, D., & Oprea, M. (2016). Micoflora associated with Lillehoj, E. B., Kwolek, W. F., Peterson, R. E., Shotwell, O. L., & Hesseltine, C. W. (1976).
maize grains during storage period. AgroLife Scientific Journal, 5(1), 63–68. Aflatoxin contamination, fluorescence, and insect damage in corn infected with Aspergillus
Environmental Protection Agency. (1999). Wastewater Technology Fact Sheet - Ozone Disin- flavus before harvest. Cereal Chemistry, 53, 505–512.
fection. Retrieved from https://www3.epa.gov/npdes/pubs/ozon.pdf Liu, Y., Pan, X., & Li, J. (2015). A 1961 – 2010 record of fertilizer use, pesticide application
European Commission. (2009). Directive 2009/128/EC of the European Parliament and of the and cereal yields: A review. Agronomy for Sustainable Development, 35, 83–93. https://doi.org/
Council of 21 October 2009 establishing a framework for Community action to achieve 10.1007/s13593-014-0259-9
the sustainable use of pesticides. Official Journal, L309, 71. Retrieved from https://eur-lex Lorenz, K., & Miller, B. S. (1975). Irradiation of cereal grains and cereal grain products.
.europa.eu/legal-content/EN/TXT/HTML/?uri=CELEX:32009L0128&from=EN CRC Critical Reviews in Food Science and Nutrition, 6(4), 317–382. https://doi.org/10.1080/
Farkas, J., Ehlermann, D. A. E., & Mohácsi-Farkas, C. (2014). Food technologies: 10408397509527195
Food irradiation. Encyclopedia of Food Safety, 3, 178–186. https://doi.org/10.1016/B978- Los, A., Ziuzina, D., Boehm, D., Cullen, P. J., & Bourke, P. (2017). The potential of atmo-
0-12-378612-8.00259-6 spheric air cold plasma for control of bacterial contaminants relevant to cereal grain produc-
Filatova, I., Azharonok, V., Lushkevich, V., Zhukovsky, A., Gadzhieva, G., & Spasi, K. (2013). tion. Innovative Food Science and Emerging Technologies, 44, 36–45. https://doi.org/10.1016/
Plasma seeds treatment as a promising technique for seed germination improvement. Paper j.ifset.2017.08.008
presented at International Conference on Phenomena in Ionized Gases, Granada, Spain.
Lund, F., & Frisvad, J. C. (2003). Penicillium verrucosum in wheat and barley indicates pres-
Flannigan, B. (1996). The microflora of barley and malt. In F. G. Priest & I. Campbell (Eds.),
ence of ochratoxin A. Journal of Applied Microbiology, 95(5), 1117–1123. https://doi.org/
Brewing microbiology (pp. 83–125). https://doi.org/10.1007/978-1-4419-9250-5_4
10.1046/j.1365-2672.2003.02076.x
Food and Agriculture Organization of the United Nations. (2017). FAOSTAT Database. Re-
trieved from https://faostat.fao.org/site/567/default.aspx#ancor/ Lung, H. M., Cheng, Y. C., Chang, Y. H., Huang, H. W., Yang, B. B., & Wang, C. Y. (2015).
Gayán, E., Condón, S., & Álvarez, I. (2014). Biological aspects in food preservation by ultra- Microbial decontamination of food by electron beam irradiation. Trends in Food Science and
violet light: A review. Food and Bioprocess Technology, 7(1), 1–20. https://doi.org/10.1007/ Technology, 44(1), 66–78. https://doi.org/10.1016/j.tifs.2015.03.005
s11947-013-1168-7 Lynch, M. F., Tauxe, R. V., & Hedberg, C. W. (2009). The growing burden of food borne
Graham, D. M., Pariza, M. W., Glaze, W. H., Erdman, J. W., Newell, G. W., & Borzelleca, J. F. outbreaks due to contaminated fresh produce: Risks and opportunities. Epidemiology & Infection,
(1997). Use of ozone for food processing. Food Technology, 51(6), 72–76. 137, 307–315.
Greene, A. K., Guzel-Seydim, Z. B., & Seydim, A. C. (2012). Chemical and physical properties Maftei, N. A., Ramos-villarroel, A. Y., Nicolau, A. I., Mart, O., & Soliva-fortuny, R. (2013).
of ozone. In C. O’Donnell, B. K. Tiwary, P. J. Cullen, & R. G. Rice (Eds.), Ozone in food Pulsed light inactivation of naturally occurring moulds on wheat grain. Journal of the Science of
processing (pp. 26–28). UK: Blackwell Publishing Ltd. Food and Agriculture, 94, 721–726. https://doi.org/10.1002/jsfa.6324
Harlan, J. R. (1992). Crops and man. Madison, U.S.A.: American Society of Agronomy. Magan, N., & Aldred, D. (2006). Managing microbial spoilage in cereals and baking products. In
Harris, L., Shebuski, J., Danyluk, M., Palumbo, M., & Beuchat, L. (2013). Nuts, seeds, and C. de Blackburn (Ed.), Food spoilage microorganisms (pp. 194–212). Cambridge, UK: Woodhead
cereals. In M. Doyle & R. Buchanan (Eds.), Food microbiology (pp. 203–221). Wash., U.S.A.: Publishing Ltd.
ASM Press. Merali, Z., Ho, J. D., Collins, S. R. A., Gall, G. Le, Elliston, A., Käsper, A., & Wal-
Heddleson, R. A., & Doores, S. (1993). Factors affecting microwave heating of foods and dron, K. W. (2013). Characterization of cell wall components of wheat straw follow-
microwave induced destruction of foodborne pathogens—A review. Journal of Food Protection, ing hydrothermal pretreatment and fractionation. Bioresource Technology, 131, 226–234.
11, 1025–1037. https://doi.org/10.1016/j.biortech.2012.12.023
Hertwig, C., Reineke, K., Ehlbeck, J., Erdogdu, B., Rauh, C., & Schluter, O. (2015a). Mislivec, P. B., & Tuite, J. (1970a). Species of Penicillium occurring in freshly-harvested and in
Impact of remote plasma treatment on natural microbial load and quality parameters stored dent corn kernels. Mycologia, 62, 67–74.
of selected herbs and spices. Journal of Food Engineering, 167, 12–17. https://doi.org/ Mislivec, P. B., & Tuite, J. (1970b). Temperature and relative humidity requirements of species
10.1016/j.jfoodeng.2014.12.017 of Penicillium isolated from yellow dent corn kernels. Mycologia, 62, 75–88.
Hertwig, C., Reineke, K., Ehlbeck, J., Knorr, D., & Schluter, O. (2015b). Decontamination Mrema, G., Gumbe, L., Chepete, H., & Agullo, J. (2011). Grain crop drying, handling and
of whole black pepper using different cold atmospheric pressure plasma applications. Food storage. In FAO Rural Structures in the tropics: Design and development (pp. 363–383). ISBN
Control, 55, 221–229. https://doi.org/10.1016/j.foodcont.2015.03.003 978–92–5-107047-5. Rome, Italy: FAO.
Hill, R. A., & Lacey, J. (1983). The microflora of ripening barley grain and the effects of Naito, S., Okada, Y., & Sakai, T. (1988). Changes in microflora of ozone-treated cereals, grains,
pre-harvest fungicide application. Annals of Applied Biology, 102, 455–465. peas, beans, spices during storage. Nippon Shokuhin Kogyo Gakkaishi, 35(2), 69–77.
Hocking, A. D. (2003). Microbiological facts and fictions in grain storage ochratoxin A. In E. J. Niemira, B. A. (2012). Cold plasma decontamination of foods. Annual Review of Food Science and
Wright, M. C. Webb, & E. Highley (Eds.), Stored grain in Australia 2003. Paper presented at Technology, 3, 125–142. https://doi.org/10.1146/annurev-food-022811-101132
Australian Postharvest Technical Conference, Canberra, Australia. Niemira, B. A., Boyd, G., & Sites, J. (2014). Cold plasma rapid decontamination of food
Jess, S., Kildea, S., Moody, A., Rennick, G., Murchie, A. K., & Cooke, L. R. (2014). European contact surfaces contaminated with Salmonella biofilms. Journal of Food Science, 79(5), M917–
Union policy on pesticides: Implications for agriculture in Ireland. Pest Management Science, 22. https://doi.org/10.1111/1750-3841.12379
70(11), 1646–1654. https://doi.org/10.1002/ps.3801 Nierop, S. Van. (2006). The impact of microorganisms on barley and malt quality - A review.
Justé, A., Malfliet, S., Lenaerts, M., De Cooman, L., Aerts, G., Willems, K. A., & Lievens, B. Journal of the American Society of Brewing Chemists, 64(2), 69–78. https://doi.org/10.1094/
(2011). Microflora during malting of barley: Overview and impact on malt quality. Brewing asbcj-64-0069
Science, 64(3–4), 22–31. Noots, I., Delcour, J. A., & Michiels, C. W. (1999). From field barley to malt: Detection and
Keklik, N. M., Demirci, A., & Puri, V. M. (2010). Decontamination of unpackaged and vacuum- specification of microbial activity for quality aspects. Critical Reviews in Microbiology, 25(2),
packaged boneless chicken breast with pulsed ultraviolet light. Poultry Science, 89(3), 570–581. 121–153. https://doi.org/10.1080/10408419991299257
https://doi.org/10.3382/ps.2008-00476 O’Donnell, C., Tiwary, B. K., Cullen, P. J. & Rice, R. G. (2012). Status and Trends of Ozone
Keklik, N. M., Krishnamurthy, K., & Demirci, A. (2012). Microbial decontamination of food in Food Processing. In O’Donnell, C., Tiwary, B. K., Cullen, P. J. & Rice, R. G. (Eds.),
by ultraviolet (UV) and pulsed UV light. In A. Demirci & M. O. Ngadi (Eds.), Microbial Ozone in Food Processing (pp. 1–2). UK: Blackwell Publishing Ltd.
decontamination in the food industry - Novel methods and applications (pp. 344–369). Cambridge, Ölmez, H., & Kretzschmar, U. (2009). Potential alternative disinfection methods for organic
UK: Woodhead Publishing Limited. fresh-cut industry for minimizing water consumption and environmental impact. LWT-Food
Kells, S. A., Mason, L. J., Maier, D. E., & Woloshuk, C. P. (2001). Efficacy and fumigation Science and Technology, 42, 686–693.
characteristics of ozone in stored maize. Journal of Stored Products Research, 37, 371–382. Oms-oliu, G., Martı́n-belloso, O., & Soliva-fortuny, R. (2010). Pulsed light treatments for food
Koehler, P., & Wieser, H. (2013). Chemistry of cereal grains. In M. Gobetti & M. Gaenzle preservation. A review. Food and Bioprocess Technology, 3(1), 13–23. https://doi.org/10.1007/
(Eds.), Handbook of sourdough biotechnology (pp. 11–45). New York, USA: Springer. s11947-008-0147-x
Kordas, L., Pusz, W., Czapka, T., & Kacprzyk, R. (2015). The effect of low-temperature plasma Ortega-Rivas, E. (2012). Pulsed light technology. In Non-thermal food engineering operations (pp.
on fungus colonization of winter wheat grain and seed quality. Polish Journal of Environmental 263–273). N.Y., U.S.A.: Springer Science+Business Media.
Studies, 24(1), 433–438. Park, J. W., Choi, S. Y., Hwang, H. J., & Kim, Y. B. (2005). Fungal mycoflora and mycotoxins
Kosiak, B., Torp, M., Skjerve, E., & Andersen, B. (2004). Alternaria and Fusarium in Norwe- in Korean polished rice destined for humans. International Journal of Food Microbiology, 103,
gian grains of reduced quality—A matched pair sample study. International Journal of Food 305–314.
Microbiology, 93(1), 51–62. https://doi.org/10.1016/j.ijfoodmicro.2003.10.006 Petters, H. I., Flannigan, B., & Austin, B. (1988). Quantitative and qualitative studies of the
Kottapalli, B., Wolf-Hall, C. E., & Schwarz, P. (2005). Evaluation of gaseous ozone and hydrogen microflora of barley malt production. Journal of Applied Bacteriology, 65, 279.
peroxide treatments for reducing Fusarium survival in malting barley. Journal of Food Protection, Pitt, J. I., & Hocking, A. D. (2009). Fresh and perishable foods. In Fungi and food spoilage (pp.
68(6), 1236–1240. 395–403). N.Y., U.S.A.: Springer Science+Business Media.
Kozempel, M., Annous, B., Cook, R., Scullen, O. J., & Whiting, R. (1998). Inactivation of Raghavan, G. S. V. (1993). Microwave drying of cereal grains: Advantages and limitations.
microorganisms with microwaves at reduced temperatures. Journal of Food Protection, 61(5), Postharvest News and Information, 4(3), 79–83.
582–585. Rajendran, S. (2002). Postharvest pest losses. In D. Pimentel (Ed.), Encyclopedia of pest management
Krishnamurthy, K., Tewari, J. C., Irudayaraj, J., & Demirci, A. (2010). Microscopic and spectro- (pp. 654). London, UK: CRC Press.
scopic evaluation of inactivation of Staphylococcus aureus by pulsed UV light and infrared heating. Rasimus-sahari, S., Mikkola, R., Andersson, M. A., Jestoi, M., & Salkinoja-salonen, M.
Food and Bioprocess Technology, 3, 93–104. https://doi.org/10.1007/s11947-008-0084-8 (2016). Streptomyces strains producing mitochondriotoxic antimycin A found in cereal
Krnjaja, V., Lukic, M., Delic, N., Tomic, Z., Mandic, V., Bijelic, Z., & Gogic, M. (2015). grains. International Journal of Food Microbiology, 218, 78–85. https://doi.org/10.1016/
Mycobiota and mycotoxins in freshly harvested and stored maize. Biotechnology in Animal j.ijfoodmicro.2015.11.007
Husbandry, 31(2), 291–302. https://doi.org/10.2298/BAH1502291K Reddy, M. V. B., Raghavan, G. S. V., Kushalappa, A. C., & Paulitz, T. C. (1998). Effect of
Laca, A., Mousia, Z., Dı́az, M., Webb, C., & Pandiella, S. S. (2006). Distribution of mi- microwave treatment on quality of wheat seeds infected with Fusarium graminearum. Journal of
crobial contamination within cereal grains. Journal of Food Engineering, 72(4), 332–338. Agricultural Engineering Research, 71, 113–117.
https://doi.org/10.1016/j.jfoodeng.2004.12.012 Richardson, S. D., Thruston, Jr A. D., Caughran, T. V., Collette, T. W., Patterson, K. S., &
Laroussi, M., & Leipold, F. (2004). Evaluation of the roles of reactive species, heat, and UV Lykins, Jr W. W. (1998). Chemical by-products of chlorine and alternative disinfectants. Food
radiation in the inactivation of bacterial cells by air plasmas at atmospheric pressure. Interna- Technology, 52, 58–61.
tional Journal of Mass Spectrometry, 233(1–3), 81–86. https://doi.org/10.1016/j.ijms.2003.11. Sabillon, L., Bianchini, A., Stratton, J., & Rose, D. J. (2017). Effect of saline organic acid solutions
016 applied during wheat tempering on flour functionality. Cereal Chemistry, 94(3), 1–21.
Lillehoj, E. B., Kwolek, W. F., Horner, E. S., Widstrom, N. W., Josephson, L. M., Franz, A. Sabillon, L., Stratton, J., Rose, D. J., Flores, R. A., & Bianchini, A. (2016). Reduction in
O., & Catalano, E. A. (1980). Aflatoxin contamination of preharvest corn: Role of Aspergillus microbial load of wheat by tempering with organic acid and saline solution. Cereal Chemistry,
flavus inoculum and insect damage. Cereal Chemistry, 57, 255–257. 93, 638–646.

Concise Reviews &

Sauer, D. B., & Burroughs, R. (1986). Disinfection of seed surfaces with sodium hypochlorite. Virto, R., Manas, P., Alvarez, I., Condon, S., & Raso, J. (2005). Membrane damage and microbial
Phytopathology, 76, 745–749. inactivation by chlorine in the absence and presence of a chlorine-demanding substrate. Applied
Schlüter, O., Ehlbeck, J., Hertel, C., Habermeyer, M., Roth, A., Engel, K. H., & Eisenbrand, Environmental Microbiology, 71(9), 5022–5028. https://doi.org/10.1128/AEM.71.9.5022
G. (2013). Opinion on the use of plasma processes for treatment of foods. Molecular Nutrition Vleugels, M., Shama, G., Deng, X. T., Greenacre, E., Brocklehurst, T., & Kong, M. G. (2005).
and Food Research, 57(5), 920–927. https://doi.org/10.1002/mnfr.201300039 Atmospheric plasma inactivation of biofilm-forming bacteria for food safety control. IEEE
Scholtz, V., Pazlarova, J., Souskova, H., Khun, J., & Julak, J. (2015). Nonthermal plasma - Transactions on Plasma Science, 33(2), 824–828. https://doi.org/10.1109/TPS.2005.844524
A tool for decontamination and disinfection. Biotechnology Advances, 33(6), 1108–1119. Wachowska, U., Stasiulewicz-Paluch, A. D., Glowacka, K., Mikolajczyk, W., & Kucharska,
https://doi.org/10.1016/j.biotechadv.2015.01.002 K. (2013). Response of epiphytes and endophytes isolated from winter wheat grain to
Selcuk, M., Oksuz, L., & Basaran, P. (2008). Decontamination of grains and legumes infected biotechnological and fungicidal treatments. Polish Journal of Environmental Studies, 22(1), 267–
with Aspergillus spp. and Penicillum spp. by cold plasma treatment. Bioresource Technology, 99(11), 273.
5104–5109. https://doi.org/10.1016/j.biortech.2007.09.076 Williams, W. P., Windham, G. L., Buckley, P. M., & Daves, C. A. (2006). Aflatoxin accumulation
Sun, C., Zhu, P., Ji, J., Sun, J., Tang, L., Pi, F., & Sun, X. (2017). Role of aqueous chlorine in corn hybrids infested at different growth stages with southwestern corn borer (Lepidoptera:
dioxide in controlling the growth of Fusarium graminearum and its application on contaminated Crambidae). Journal of Agricultural and Urban Entomology, 23, 97–103.
wheat. LWT - Food Science and Technology, 84, 555–561. https://doi.org/10.1016/j.lwt.2017. Wu, J., Doan, H., & Cuenca, M. A. (2006). Investigation of gaseous ozone as an anti-fungal
03.032 fumigant for stored wheat. Journal of Chemical Technology and Biotechnology, 81(7), 1288–1293.
Tonon, S. A., Marucci, R. S., Jerke, G., & Garcia, A. (1997). Mycoflora of paddy and milled https://doi.org/10.1002/jctb.1500
rice produced in the region of Northeastern Argentina and Southern Paraguay. International Yaciuk, G. (1980). Agricultural applications of solar energy. In: Solar Energy Conversion II, Selected
Journal of Food Microbiology, 37, 231–235. Lectures from the 1980 International Symposium on Solar Energy Utilization (pp. 337–353). Oxford,
Trung, T. S., Bailly, J. D., Querin, A., Le Bars, P., & Guerre, P. (2001). Fungal contamination UK: Pergamon Press.
of rice from south Vietnam, mycotoxinogenesis of selected strains and residues in rice. Revue Yadav, D. N., Anand, T., Sharma, M., & Gupta, R. K. (2014). Microwave technology for
de Médecine Vétérinaire, 152, 555–560. disinfestation of cereals and pulses: An overview. Journal of Food Science and Technology, 51(12),
Vadivambal, R., Jayas, D. S., & White, N. D. G. (2007). Wheat disinfestation using mi- 3568–3576. https://doi.org/10.1007/s13197-012-0912-8
crowave energy. Journal of Stored Products Research, 43(4), 508–514. https://doi.org/10.1016/ Zahoranova, A., Henselova, M., Hudecova, D., Kalinakova, B., Kovacik, D., Medvecka, V., &
j.jspr.2007.01.007 Cernak, M. (2015). Effect of cold atmospheric pressure plasma on the wheat seedlings vigor
Varga, J., Kocsube, S., Peteri, Z., Vagvolgyi, C., & Toth, B. (2010). Chemical, physical and and on the inactivation of microorganisms on the seeds surface. Plasma Chemistry and Plasma
biological approaches to prevent ochratoxin induced toxicoses in humans and animals. Toxins, Processing, 36(2), 397–414. https://doi.org/10.1007/s11090-015-9684-z
2(7), 1718–1750. https://doi.org/10.3390/toxins2071718
Victorin, K. (1992). Review of the genotoxicity of ozone. Mutation Research, 277, 221–238.

Microbiological Decontamination of Cereal Grains

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Hypotheses in Food Science

Microbiological Decontamination of Cereal Grains

Keywords: cereal grains, decontamination, food safety, microflora, microbial inactivation

Introduction Currently, industrial production of cereals relies heavily on

C 2018 Institute of Food Technologists

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Figure 2–Most commonly cultivated cereal

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F. avenaceum, and Microdochium nivale (formerly known as F. nivale)

The storage microflora

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Figure 4–Microbial contamination within

Method/technology Description Limitations References

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Table 2–Potential methods and technologies for cereal grains preservation.

Method/technology Description Limitations References

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