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RAdvFoodSci: 2019: 2(4): 200-2016 ISSN: 2601-5412 200
MYCOTOXINS IN NIGERIAN CEREALS AND PUBLIC HEALTH
IMPLICATIONS
Annabella A. ADEWUNMI1 and Stephen O. FAPOHUNDA1*
1Department of Microbiology, Babcock University, Ilishan Remo, Nigeria (*[email protected])
Article History:
Received 7 September 2019
Revised 2 December 2019
Accepted 07 December 2019
Keywords:
Mycotoxins
Cereal grains
Public Health
Risk Assessment
Nigeria
Abstract:
Recent trends in the contamination of cereal grains by mycotoxins were
reported with respect to public health concerns. Mycotoxins are toxic fungal
secondary metabolites, poisonous to humans and animals, and having
maize, guinea corn, millet and rice as candidate crops. Reports on some
regulated mycotoxins such as aflatoxins, fumonisins, ochratoxin,
zearalenone, and some emerging ones like moniliformin and citrinin are
highlighted, with Aspergillus, Fusarium, Penicillium and Alternaria as major
producers. Although high-level occurrence in cereals in Nigeria have been
documented, risk assessment estimates for consumers have only been
done on the major mycotoxins with more focus on individual toxins. This
review represents a synthesis from a recent data collected on mycotoxin
contamination of some of the grains consumed as major staples in Nigeria,
and the possible health effect on consumers through the analysis of the risk
assessment estimates. It also touches on the possibility of guiding
government policy on international trade.
1. Introduction
Mycotoxigenic fungi are a group of
microorganisms found widely distributed in the
environment. They are often implicated in global
food safety concerns due to their ability to colonize
food commodities and farm crops [1]. These fungi
produce mycotoxins, which have adverse effects on
human health and export [2]. The mycotoxins are
secondary metabolites, which in minute doses are
poisonous to humans and animals [3]. Over 300
mycotoxins have been characterised but only a few
of them are regularly found in food and animal feed
including cereal grains and seeds [4]. The most
prominent mycotoxins found quite often in food are
aflatoxins, fumonisins, ochratoxins, zearalenone,
trichothecenes and patulin [5]. Others are citrinin,
penicillinic acid, tenuazonic acid, cytochalasins,
fusaric acid and Fusaric C [2-4]. A few genera of
filamentous fungi produce these mycotoxins and
they include Aspergillus, Fusarium, Penicilium, and
Alternaria [6-7, 16]. Grains such as sorghum, maize,
millet, soya beans, rice, plants which are extensively
used for food and feed manufacturing as sources of
protein, carbohydrate and oils, are susceptible to
contamination by filamentous fungi either as crops in
the farm or during storage as well as during
processing [8]. According to Pleadin [9], grains are
highly susceptible to mycotoxins pre- and post-
harvest and at any time during transit and
processing stages. To this end, fungi contaminating
grains have been categorised as either field fungi or
storage fungi. Aspergillus species are both pre- and
post-harvest plant pathogens [10]. Currently, over
25% of the world’s agricultural commodities are
estimated to be contaminated with mycotoxins [5],
leading to huge agricultural losses in billions of
dollars [11]. The prevalence of mycotoxins in farm
crops is a natural occurrence and cannot be
circumvented or entirely prevented either in the field
or during post field operations by current agricultural
practices. Risk assessment by regulatory bodies has
become necessary to help establish regulatory
Annabella A. Adewunmi and Stephen O. Fapohunda
Mycotoxins in Nigerian cereals and public health implications
RAdvFoodSci: 2019: 2(4): 200-216 ISSN: 2601-5412 201
guidelines to protect public health [12-13].
Furthermore, the emerging techniques in analytical
research, and the use of modern, highly sensitive
and state-of-the-art tools for mycotoxins analysis,
have made both the detection and quantification
very necessary and attractive. Local production of
cereals is still low in Nigeria, leaving little or none for
export, with sometimes, scanty reports of rejects and
bans from the importing countries. This review
represents a synthesis from a recent ten-year data
collected on mycotoxin contamination on selected
crops consumed in Nigeria, and the likely
pathological effects on consumers through the
analysis of the exposure risk assessment estimates.
Sorghum
Guinea corn, Sorghum bicolor (L.) Moench, is a
herbaceous cereal cultivated from the seed [14]. It is
ranked fifth in the world and second in Africa after
maize as the most important cereal, with a current
annual production of about 2.8 million tonnes [15]. It
is one of the principal staple cereals for millions of
people in sub-Saharan Africa (SSA) and Asia. In
most developed countries such as the Americas,
Europe and Australia, sorghum is used for animal
feed and for other industrial applications [16].
According to Astoreca et al. [16] more than 35% of
the world sorghum is cultivated and produced for
human consumption. In Nigeria, sorghum is used as
raw materials and ingredients for a variety of food
products, which are consumed by all age groups
including infants. In the food industry, these local
raw materials are used as adjuncts in the
manufacture of a variety of food products including
Infant Cereals, All-Family Cereals, beverages and
other consumable products. The expended grains
are useful in animal feed. In homes, and in Northern
Nigeria in particular, sorghum is used for both adult
and baby food, which are consumed as pap, (ogi or
akamu), porridge, local cakes (masa), gruel-like
drink (kunu-zaki) and fura. Sorghum is one of the
most frequently contaminated grains with
mycotoxigenic fungi [7]. This may be due to
favorable environmental conditions, which
encourage the growth of fungi, coupled with the
method of crop cultivation, harvesting, handling and
storage. Chala et al. [17] stated that sorghum and
many other crops are affected by many diseases as
a result of contamination by a range of fungi both in
the field and after harvest, leading to significant
qualitative and quantitative yield losses. Martin et al.
[18] stated that sorghum grains are often good
substrates for fungi contamination and growth when
poorly dried during storage. Fapohunda et al. [19]
also corroborated that post-harvest contamination of
crops by molds can occur if crops are not properly
dried, and storage conditions permit water to exceed
critical values. The growth of the spoilage fungi is
stimulated by a moisture content of up to 15-19%, a
situation favourable to toxin production. The fungal
species usually associated with spoilage of sorghum
grains are Fusarium, Penicillium, and Aspergillus [6-
7, 16]. Ssepuuya et al. [20] evaluated the safety,
type, level and prevalence of mycotoxins in sorghum
of four sub-Saharan African (SSA) countries
(Burkina Faso, Ethiopia, Mali and Sudan) using a
multi-analyte LC-MS/MS method for quantification of
23 mycotoxins. Out of 1533 samples analysed, 33%
were contaminated with at least one of the following
mycotoxins: aflatoxins, fumonisins, sterigmatocystin,
Alternaria toxins, OTA and zearalenone. Factors
such as country of origin, colour, source and
collection period of sorghum samples significantly
influenced the type, level and prevalence of
mycotoxins. Results showed that the most prevalent
mycotoxins in sorghum grains were products of
Fusarium species (fumonisins (17%) and
diacetoxyscirpenol (11%); and Aspergillus species
(sterigmatocystin (15%) and aflatoxins (13%) further
confirming that fumonisins and aflatoxins are the
most prevalent mycotoxins in sorghum [21]. The
concentrations were well above the European Union
Maximum Permitted level (EU MPL) in grains posing
a potential health risks to sorghum consumers in
Africa. In Nigeria, contamination of sorghum grains
by AFB1, OTA and ZEN both in freshly harvested
grains and during storage have been reported [22].
However, AFB1 contamination was higher in stored
(mean: 262.8 μg/kg) than from freshly harvested
grains of sorghum (mean: 9.88 μg/kg). This is
probably due to inclement storage facilities, but
which are acceptable for fungal growth and
mycotoxin production. Similarly, a comparative study
by Odoemelam and Osu [23] reported a higher level
of AFB1 in sorghum from northern Nigeria compared
to southern Nigeria with means values of
30.53µg/kg. A recent study by Apeh et al. [24]
indicated that 54% of sorghum grains from northern
Annabella A. Adewunmi and Stephen O. Fapohunda
Mycotoxins in Nigerian cereals and public health implications
RAdvFoodSci: 2019: 2(4): 200-216 ISSN: 2601-5412 202
Nigeria were contaminated with aflatoxins at levels
ranging from 0.96 to 21.71µg/kg and mean level of
5.31 μg/kg. In their study, most of the positive
samples were above the maximum limit (2 µg/kg) for
AFB1 for foods meant for human consumption in the
EU [13].
Maize
Maize (Zea mays L.) is one of the most important
Nigerian staples and a source of raw materials for
the food industry. Maize grains are highly
susceptible to fungal and mycotoxin contamination
in the field, during storage, in transit and during the
processing stages. Fungal species like Aspergillus
flavus, Fusarium verticillioides, F. proliferatum, F.
graminearum contaminate maize grains with their
corresponding mycotoxins: aflatoxins, fumonisins,
trichothecenes and zearalenone [18]. Aflatoxin
contaminates many foods, but it is most abundant in
maize and maize products, because maize could be
infected even in the field under specific
environmental conditions. Contamination of maize
depends on the co-existence of susceptibility of
hybrids and environmental conditions favourable for
proliferation of mycotoxigenic fungi [25]. These fungi
proliferate in maize with favourable storage
conditions such as high moisture, high temperature,
extended storage period, and high infestation by
insects and mites. Thus, contaminated stored maize
grains are potentially a health risk to humans and
animals [26]. Krnjaja et al. [27] reported the
presence of aflatoxin B1 (AFB1), Zearalenone
(ZEN), Deoxynivalenol (DON) and Fumonisin B1
(FB1) in stored maize. They were detected in all
tested samples with average concentrations of 1.39-
μg kg-1 for AFB1, 71.79-μg kg-1 for ZEN, 128.17-μg
kg-1 for DON, and 1610.83-μg kg-1 for FB1. All of the
samples in this study were positive and consistent
with other reports, on the presence of Fusarium
toxins, fumonisin B1, deoxynivalenol and
zearalenone [27-29]. Aflatoxins and fumonisins,
synthesized mainly by A. flavus and F. verticillioides,
respectively, are among the most important
mycotoxins that can cause economic losses in
maize production and public health concerns on
consumption. Anjorin et al. [30] isolated a range of
mycotoxins including known ones such as aflatoxins,
fumonisins, and 19 emerging mycotoxins namely;
beauvericin (BEAU), moniliformin (MON), nidurufin
(NID), norsolorinic acid (NA), citrinin (CIT),
macrosporin (MAC-A), sterigmatocystin (STER),
macrosporin, alternariol methyl ether (AME)
chanoclavine (CNV); agroclavine (AGV);
elymoclavine (ECV) and brevianamid (BVD-F) from
maize in Abuja, Nigeria. The possibility of synergy
among them heightens the scare on unsafe foods
and a serious potential health threat to consumers in
Nigeria. Chilaka et al. [31] in their study reported
Fusarium mycotoxins in maize in Nigeria. One
hundred and thirty-six (136) samples of maize
evaluated for the occurrence of Fusarium
mycotoxins showed that 13 out of the 18 toxins were
present in the maize samples, of which only four
(FB1, FB2, DON, and ZEN) are regulated by the
European Union (EU). The sum of fumonisins (FB1
+ FB2 + FB3) were in the ranges which exceeded
the maximum regulatory limit (MRL) of 1000 µg/kg
set by the European Union for the sum of FB1 and
FB2 [32] (Table 1), implying the possibility of
circulating toxin- laden food items in the country.
Similar studies in sub Saharan Africa have
corroborated the high incidence of fumonisins in
concentrations up to 53,863ug/kg [33].
Rice
Rice (Oryza sativa L.) is the most important
source of human calorie intake and is a staple food
in many countries [34]. It ranks as the sixth most
cultivated crops in Nigeria. In 2017, Nigeria’s rice
production increased to 5.8 million tons and has
increased every year with an annual growth rate of
1%. [4]. Despite the high rate of rice production,
Nigeria still imported about 2.3 million tons of rice in
2016 alone, while the consumption rate now stands
at 7.9 million tons. Rice is highly consumed in
Nigeria hence the shortage in the national annual
demand [35]. The increase in the rate of rice
consumption in Africa per year compared to other
staples, stands at about 5.5% (2000–2010 average).
This increase is due to lifestyle changes,
urbanization and the continuously growing
population of Africa [36]. Rice is cultivated in hot and
humid climatic conditions, and these encourage the
proliferation of fungi and subsequent mycotoxin
production. In addition, inappropriate storage and
climatic conditions such as floods and heavy rainfall
at the time of harvest aggravate the situation. Most
farmers practice sun-drying, a method which is not
Annabella A. Adewunmi and Stephen O. Fapohunda
Mycotoxins in Nigerian cereals and public health implications
RAdvFoodSci: 2019: 2(4): 200-216 ISSN: 2601-5412 203
sufficient to reduce the moisture content to
acceptable levels, thus making rice a conducive
substrate for fungal growth [37]. Makun et al. [35]
reported the detection of the major mycotoxins in 21
rice samples from Niger state, Nigeria, at different
levels of concentration. They reported total aflatoxin
of 28–372 µg/kg, OTA concentrations of 134–
341 µg/kg (in 66.7% of the samples) above
regulatory limits (2-50 μg/kg). Others were ZEN
53.4%, DON 23.8%, FB1 14.3% and FB2 4.8%
(Table 1). Ayejuyo [38] also reported OTA
concentrations in rice from Lagos market in Nigeria,
though within acceptable and safe limits. Whether
these mycotoxins occur at low levels or not in these
grains, it remains a public health issue. This is
because consumption of small doses over a long
time will result in chronic effects to the consumer
while large amounts of toxin in a short period will
cause acute toxicity to human organs. Nigeria is now
discouraging importation of rice, making local
monitoring for standards on mycotoxins, pesticides
and other contaminants expectedly easier.
Millet
Millet is an important cereal, nutritionally rich and
comparable or even superior to other major cereals
in Nigeria. Regular consumption of millet has been
linked to reduction in the risk of diabetes mellitus
[39] and gastrointestinal tract disorders [40]. Millet is
susceptible to infestation by a wide array of
opportunistic fungi especially Fusarium species and
mycotoxin contamination [41]. Jennings [42] also
stated that trichothecenes including deoxynivalenol
(DON), acetyl deoxynivalenol, nivalenol (NIV), and
fusarenone X, are common fungal contaminants.
Consumption of millet contaminated with these
toxins is a potential food safety problem for humans
and farm animals [43-44]. Apeh et al. [24] reported
millet contamination by aflatoxin AFB1 though at
lower levels of concentration (10µg/kg) than
sorghum. However, studies by Hertveldt [45]
indicated higher levels of concentration of AFB1
(mean: 159.5µg/kg) in millet from the northern part
of Nigeria. Makun et al. [46] reported that all
samples of millet taken from Niger state, Nigeria,
were contaminated with OTA at levels ranging from
10.2 – 46.57µg/kg, (mean: 24.74ug/kg), well above
EU limits of 5µg/kg for OTA. Contamination with high
concentrations of FUM, DON, and ZEN in millet in
Nigeria has also been reported [31], most of which
exceeded the maximum regulatory limits of
1000ug/kg set for total FUM by EU [13]. Conversely,
low levels of AFB1 [16] and FUM [47-48] were found
in finger millet and pearl millet, popularly used in
Nigeria and other West African countries for the
production of traditional beverages and cereal
products.
Consumer Health implications of exposure to
mycotoxins in cereal grains
A few mycotoxins are regulated in food and feed
due to health concerns. Aflatoxin is the most
regulated fungi food toxin worldwide. AFB1 is the
most toxic of all known mycotoxins, and ranked as a
group 1 carcinogen [53]. Aflatoxins are genotoxic
agents, which cause alterations initiated at the DNA
level. It is a leading cause of hepatocellular
carcinoma in humans [54]. The recent increasing
cases of liver cancer is an invitation to focus more
on making human food more wholesome. Other
mycotoxins cause various pathological cases
referred to as mycotoxicosis. The major food borne
mycotoxins, their main producing fungal species, the
cereal commodity most frequently contaminated,
and their major health effects on animals and
humans are shown in table 2.
Annabella A. Adewunmi and Stephen O. Fapohunda
Mycotoxins in Nigerian cereals and public health implications
RAdvFoodSci: 2019: 2(4): 200-216 ISSN: 2601-5412 204
Table 1: Prevalence and levels of concentration of mycotoxins in sorghum, maize, millet and rice grains in Nigeria (2009-2018)
Grain Mycotoxin
Frequency of
contamination
/ (% positives)
Range of Concentration
(µg/kg)
Mean Concentration
(ug/kg) Source
Sorghum AFB1 91/168 (55) *ND -1164 199.51 [22]
Sorghum AFB1 19/35 (54.29) 0.96 – 17.33 - [24]
Sorghum AFB2 4/35 (11.43) 1.26 - 2.24 - [24]
Sorghum AFG1 1/35 (2.86) 7.11 - [24]
Sorghum FUM - 5 - 1340 131 [48]
Sorghum FUM 9/110 (8) Max. 180 83 [31]
Sorghum DON 3/110 (3) Max. 199 100 [31]
Sorghum OTA 16/17 (94) *ND – 29.5 8.28 [46]
Sorghum ZEA 1/110 (1) 38 [31]
Sorghum ZEA 62/168 (37) *ND - 1454 184.76 [22]
Maize AFB1 17/56 (30) 0.7 - 440 74 [49]
Maize AFB1 47/70 (67) 0.4 – 673.8 394 [50]
Maize AFB2 38/70 (54) 1 - 644 44 [50]
Maize AFG1 11/70 (16) 1 - 264 47 [50]
Maize AFG2 4 / 70 (6) 0.7 - 52 16 [50]
Maize AFM1 34/70 (49) 1.3 - 120 14.5 [50]
Maize FUM 88/136 (65) Max. 8508 935 [31]
Maize FUM 5 - 2860 228 [48]
Maize FB1 65/70 (93) 1.8 - 10447 1552 [50]
Maize FB2 59/70 (84) 12.8 - 3455 442 [50]
Maize FB3 59/70 6.4 - 720 161 [50]
Maize Hydrolysed FBI 37/70 (53) 0.4 -135 11 [50]
Annabella A. Adewunmi and Stephen O. Fapohunda
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RAdvFoodSci: 2019: 2(4): 200-216 ISSN: 2601-5412 205
Maize DON 70/70 (100) 11 - 479 60 [50]
Maize DON glucoside 7/70 (10) 0.1 - 76 11 [50]
Maize DON 22/136 (16) Max 225 99 [31]
Maize NIV 38/70 (54) 0.7 - 164 14 [50]
Maize OTA 16/17 (94) *ND – 139.2 26.96 [46]
Maize OTA 7/170 (10) 4 - 580 111 [50]
Maize Ochratoxin α 1/70 (1) 11 - 11 11 [50]
Maize OTB 5/70 (7) 2 - 26 7.5 [50]
Maize ZEA 12/70 (17) 0.4 – 204.4 174 [50]
Maize α-ZEA 1/17 (1) 17-17 17 [50]
Maize Β-ZEA 1/17 (1) 13-13 13 [50]
Maize ZEA 1/136 (1) - 65 [31]
Maize AFB1 - - 27.93 [51]
Maize AFB2 - - 9.4 [51]
Maize AFG1 - - 18.60 [51]
Maize AFG2 - - 17.63 [51]
Maize OTA - - 139.50 [51]
Maize ZEA - - 64.95 [51]
Maize AFB1 - - 14.92 [51]
Maize AFB2 - - 4.30 [51]
Maize AFG1 - - 9.40 [51]
Maize AFG2 - - 7.96 [51]
Maize OTA - - 112.05 [51]
Maize ZEA - - 43.40 [51]
Millet AFB1 6/87 (7) 8.6-384.9 159 [45]
Annabella A. Adewunmi and Stephen O. Fapohunda
Mycotoxins in Nigerian cereals and public health implications
RAdvFoodSci: 2019: 2(4): 200-216 ISSN: 2601-5412 206
Millet AFB1 19/31 (61.29) 1.05 -10.06 - [24]
Millet AFB2 12/31 (38.71) 1.86 – 4.90 - [24]
Millet AFG1 *ND (0) [24]
Millet FUM 12/87 (14) Max: 22064 2113 [31]
Pearl Millet FUM 12/87 (14) 6-29 18 [48]
Millet DON 11/87 (13) Max: 543 151 [31]
Millet OTA 18/18 (100) 10.2-46.57 24.74 [46]
Millet ZEA 12/87 (14) Max: 1399 419 [31]
Fonio Millet AFB1 13/16 (68) 0.08-14 0.4 [52]
Fonio Millet AFB2 4/16 (25) 0.07-0.1 0.08 [52]
Fonio Millet AFG1 4/16 (25) 0.2-2 0.6 [52]
Rice AFB1 21/21 (100) 4.1-309.0 37.2 [35]
Rice AFB2 21/21 (100) 1.3-24.2 8.3 [35]
Rice AFG1 21/21 (100) 5.5-76.8 22.1 [35]
Rice AFG2 19/21 (95) 3.6-44.4 14.7 [35]
Rice TOTAL AF 21/21 (100) 27.7-371.9 82.5 [35]
Rice OTA 14/21 (66) *ND -341.3 141.7 [35]
Rice ZEA 11/21 (52) *ND -41.9 10.6 [35]
Rice DON 5/21 (23.8) *ND -112.2 18.9 [35]
Rice FB1 3/21(14) 0.4 - 4.4 0.2 [35]
Rice FB2 1/21 (4.7) 132.5-132.5 6.0 [35]
Rice FB3 *ND/21 (0) - - [35]
Rice PAT *ND/21 (0) - [35]
Rice OTA 1/25 (4) *ND- 2.18 0.34 [38]
ND = Not detectable
Annabella A. Adewunmi and Stephen O. Fapohunda
Mycotoxins in Nigerian cereals and public health implications
RAdvFoodSci: 2019: 2(4): 200-216 ISSN: 2601-5412 207
Table 2: Major food borne mycotoxins, producing fungal species, the food most contaminated, and their
major health effects on animals and humans; source: Koppen et al. [55], Medeiros et al. [56].
Mycotoxins Producing Fungal
Species
Food
Contaminated Affected Species Health Effects
Aflatoxins
(AFB1, AFB2,
AFG1, AFG2,
AFM1, AFM2)
Aspergillus flavus,
A. nomius,
A. parasiticus,
A. arachidicola,
A. bombycis
A. pseudotamarii,
A. minisclerotigenes,
A. rambellii,
A. ochraceoroseus,
Emericella astellata,
E. venezuelensis,
E. olivicola
Maize, wheat, rice,
spices, sorghum,
ground nuts, tree
nuts, almonds,
milk, oilseeds,
dried fruits,
cheese, spices,
eggs, meat.
Birds: Duckling,
turkey, poultry,
pheasant chick,
mature chicken,
quail; Mammals:
Young pigs,
pregnant sows,
dog, calf, mature
cattle, sheep, cat,
monkey, human,
Fish, Laboratory
animals
Carcinogenic,
mutagenic,
teratogenic,
hepatotoxic,
nephrotoxic,
immunosuppressive,
hemorrhage of
intestinal tract and
kidneys, liver
disease.
Fumonisins
(FB1, FB2, FB3)
Fusarium anthophilum,
F. dlamini,
F. napiforme,
F. proliferatum,
F. nygamai,
F. verticillioides
Maize, maize
based products,
corn based
products, sorghum,
asparagus, rice,
milk
Horses, swine,
rats, humans
Hepatotoxic,
immunotoxic,
cause necrosis,
cerebral oedema
Trichothecenes
(T-2 and HT-2
toxin,
diacetoxyscirpe
nol, Neosolaniol,
nivalenol,
deoxynivalenol,
3acetylDON, 15-
acetylDON,
fusarenon X)
Fusarium sporotrichioides
F. poae,
F. acuminatum,
F. culmorum,
F. equiseti,
F. graminearum,
F. cerealis,
F. moniliforme,
F. myrothecium,
F. lunulosporum,
Cephalosporium sp.
Myrothecium sp.,
Trichoderma sp.,
richothecium sp.,
Phomopsis sp.,
Stachybotrys sp.
Cereals, cereal
based products
Swine, cattle,
chicken, turkey,
horse, rat, dog,
mouse, cat, human
Immuno-
depressants,
mutagenic,
gastrointestinal
haemorrhaging,
neurotoxic
Zearalenone
(ZEN)
F. graminearum,
F. culmorum,
F. crookwellense,
F. equiseti,
F. sporotrichioides
F. graminearum,
F. culmorum,
F. crookwellense,
F. equiseti,
Barley, oats, wheat
rice, sorghum,
sesame, soy
beans, cereal
based products
Swine, dairy cattle,
chicken, turkey,
lamb, rat, mouse,
guinea pig
Estrogenic activity
(infertility, vulval
oedema, vaginal
prolapse, mammary
hypertrophy in
females,
feminisation of
males)
Annabella A. Adewunmi and Stephen O. Fapohunda
Mycotoxins in Nigerian cereals and public health implications
RAdvFoodSci: 2019: 2(4): 200-216 ISSN: 2601-5412 208
Ochratoxins
(OTA, OTB,
OTC)
A. alutaceus,
A. alliaceus,
A. auricomus,
A. glaucus,
A. niger,
A. carbonarius,
A. melleus,
A. albertensis,
A. citricus,
A. flocculosus,
A. fonsecaeus,
A. lanosus,
A. ochraceus,
A. ostianus,
A. petrakii,
A. sulphureus,
A. pseudoelegans,
A. Roseoglobulosus,
A. sclerotiorum,
A. steynii,
A. westerdijkiae,
Neopetromyces muricatus,
Penicillium viridicatum,
P. verrucosum,
P. cyclopium,
P. carbonarius
Cereals, dried vine
fruit, wine, coffee,
oats, spices, rye,
raisins, grape juice
Swine, dairy cattle,
chicken, turkey,
lamb, rat, mouse,
guinea pig
Carcinogenic,
mutagenic,
nephrotoxic,
hepatotoxic,
teratogenic,
immunodepression,
carcinogenic
(urinary tract
tumors), inhibition of
protein synthesis
Patulin A. clavatus,
A. longivesica,
A. terreus,
P. expansum,
P. griseofulvum,
Byssochlamys sp.
Apples, apple
juice, cherries,
cereal grains,
grapes, pears,
bilberries
Birds: Chicken,
chicken embryo,
quail; Mammals:
Cat, cattle, mouse,
rabbit, rat, human
Others: Brine
shrimp, guppie,
zebra
Immuno-depressant,
pulmonary and
cerebral oedema,
nausea, gastritis,
paralysis,
convulsions,
capillary damage,
carcinogenic
Ergot alkaloids Claviceps africanana,
C. purpurea,
C. fusiformis,
C. paspali,
Neotyphodium
coenophialum
Wheat, rye, hay,
barley, millet, oats,
sorghum, triticale
fish larvae, pigs,
cattle, swine,
horses, swine,
human
Gangrenous form:
vasoconstrictive
activity (edema of
the legs, paraesthe-
sias, gangrene at
the tendons);
Convulsive form:
gastrointestinal
symptoms (nausea,
vomiting), effects on
the central nervous
system (drowsiness,
ataxia, convulsions,
blindness and
paralysis.)
Annabella A. Adewunmi and Stephen O. Fapohunda
Mycotoxins in Nigerian cereals and public health implications
RAdvFoodSci: 2019: 2(4): 200-216 ISSN: 2601-5412 209
In the developed countries of the world, human
exposure to mycotoxins, especially of children, is at
minimal level because of observance of regulatory
standards. This is not the same in the developing
countries, such as Nigeria, where monitoring and
enforcement of standards are almost absent, and
the staple foods are often susceptible to mycotoxins.
Generally, in sub-Saharan Africa, people are
exposed to unsafe levels of various multi-
mycotoxins, with attendant serious public health
consequences [57]. This is why mycotoxin
contamination in food is poverty related.
Nevertheless, issues on standards and regulations
are progressively being taken seriously because all
countries recognize that addressing mycotoxin
contamination in food commodities and feeds will
not only reduce public health issues and costs, but
also offer gains with respect to export trade.
Individual countries thus set their regulatory limits
based on the final use of the commodity, local and
export expectations.
Several mycotoxins related human health
problems have been documented in Nigeria. They
include the death of children who consumed moldy
groundnut cake [58], and the presence of aflatoxin in
the urine of liver disease patients in Zaria, Nigeria.
Aflatoxin was also detected post mortem in blood
and some organs of children who died of
kwashiorkor in Western Nigeria as well as in human
semen, breast milk, and in the blood of umbilical
cord of babies [59-61].
Exposure Risk Assessments
In order to assess potential health problems from
the presence of mycotoxins in grains, the extent to
which actual dietary intake approach or exceed a
toxicologically acceptable daily intake (ADI) should
be determined. Risk assessments have been
conducted for at least the five major mycotoxins
namely aflatoxin, fumonisins, Ochtatoxin A,
Deoxynivalenol and Zearalenone by various
regulatory agencies for the purpose of setting food
safety guidelines. However, these measures and
guidelines have very little impact on the remote rural
and subsistence farming communities in developing
countries such as Nigeria, compared to developed
countries where regulation are strictly enforced to
reduce and /or eliminate mycotoxin contamination.
Therefore, due to lack of exposure and poverty,
these populations are still at risk of exposure to
these mycotoxins and the subsequent health risks.
In Nigeria, Exposure Assessment (EA) of aflatoxin
for consumers of maize grains has been
documented in adults [50], and in infants and young
children [62]. Exposure assessment (EA) was
calculated based on the average maize consumption
of 57g/bw / day in Nigeria [63], as modified by [62],
since there are no conclusive daily consumption
records in Nigeria. Other parameters used were the
mean of means of aflatoxin concentration
(137.3ng/g) in stored grains obtained from the five
agro-ecological zones of Nigeria, and the average
body weight depending on whether the consumers
are adults, young children or infants.
Mathematically represented as:
PDIm =µX × Cc / Bw
Where:
PDIm: Probable daily intake for each mycotoxin
(µg·kg−1 bw·day−1)
µX: Mean of means of mycotoxin concentration
Cc: Average consumption of maize in Nigeria
Bw: Body weight for the population groups
(infants, children, and adults) [62]
Similarly, Exposure Assessment for other grains
such as rice, sorghum and millet can be calculated
based on the mean concentrations of each major
mycotoxins and average consumption /bw/day as
shown in table 3. The Probable daily intake for rice
is calculated using 70g/bw/day as daily consumption
in Nigeria [64]. The probable daily intake for
Sorghum and millet is calculated using a daily
consumption of 57g/bw/day [62], as there is no data
for sorghum & millet daily consumption in Nigeria,
and the mean concentrations of the major
mycotoxins are adapted from Table 1.
Annabella A. Adewunmi and Stephen O. Fapohunda
Mycotoxins in Nigerian cereals and public health implications
RAdvFoodSci: 2019: 2(4): 200-216 ISSN: 2601-5412 210
Table 3: Exposure Assessment for Nigerian Grains based on Probable Daily intake (PDI) of grains
contaminated with major mycotoxins in adults (60kg bw), young children (25kg bw) and infants (10kg bw).
Grain Mycotoxin
Mean
concentration
µg/kg
Probable Daily
Intake (PDI)
Infant
µg/kg/bw/day
Probable Daily
Intake (PDI)
Young children
µg/kg/bw/day
Probable Daily
Intake (PDI)
Adult
µg/kg/bw/day
Sorghum AFB1 199.51a 1137.2 454.88 189
Sorghum FUM 131b 746.7 298.68 124.45
Sorghum FUM 83c 473.1 189.24 78.85
Sorghum DON 100c 570 228 95
Sorghum OTA 8.28a 47.19 18.87 7.86
Sorghum ZEA 38c 216.6 86.64 36.1
Sorghum ZEA 184.76a 1053.1 421.25 175.5
Millet AFB1 159d 906.3 362.52 151
Millet FUM 2113c 12044 4817.64 2007.35
Millet DON 151c 860.7 344.28 143.45
Millet OTA 24.74a 141 56.4 23.50
Millet ZEA 419c 2388.3 955.32 398
Fonio
Millet
Total AFs 0.36e 2.05 0.82 0.34
Rice AFB1 37.20a 260.4 104.16 43.4
Rice Total AFs 82.5a 577.5 231 96.25
Rice OTA 141.7a 991.9 396.76 165.31
Rice ZEA 10.6a 74.2 29.68 12.36
Rice DON 18.9a 132.3 52.92 22.05
Rice Total FB 3.1a 21.7 8.68 3.61
Maize AFB1 74f 421.8 168.72 70.3
Maize Total AFs 515.5g 2938.35 1175.34 489.72
Maize AFB1 394g 2245.8 898.3 374.3
Annabella A. Adewunmi and Stephen O. Fapohunda
Mycotoxins in Nigerian cereals and public health implications
RAdvFoodSci: 2019: 2(4): 200-216 ISSN: 2601-5412 211
Maize FUM 935c 5329.5 2131.8 888.25
Maize FUM 228h 1299.6 519.84 216.6
Maize Total FBs 541g 3083.7 1233.48 513.95
Maize Total DON 35.5g 202.35 80.94 33.73
Maize DON 99c 564.3 225.72 94
Maize OTA 111g 632.7 253 105.45
Maize ZEA 174g 991.8 396.72 165.3
Sources of statistical data: a [22]; b[48]; c[31]; d[45]; e[57]; f[49]; g[50]; h[48].
From the above simulations, AFB1 Probable
Daily Intake (PDI) in Sorghum for infants
(1137.2µg/kg/bw/day), young children
(454.88µg/kg/bw/day) and adults (189µg/kg/bw/day)
has exceeded the provisional maximum tolerable
daily intake (PMTDI) for AFB1
(0.00000001µg/kg/bw/day) [65], indicating the high
risk of Hepatocellular carcinoma (HCC) in Nigerian
consumers. AFB1 in rice, millet and maize were also
above the PMTDI limit. Majeed et al. [65] stated that
there is no Acceptable Daily Intake (ADI) for
aflatoxins as they are genotoxic and carcinogenic.
Only an ADI of zero will result in no risk. However,
‘zero risk’ could be achieved only by eliminating all
possible exposure, which is not possible since
aflatoxins are naturally occurring carcinogens in
foods. Therefore, the intake should be reduced to
‘As Low As Reasonably Achievable’, the ALARA
principle. According to Adetunji [62], the risk
characterization for genotoxic and carcinogenic
compounds such as aflatoxins should be based on
Margin of Exposures (MOEs) calculated thus:
MOE = Benchmark dose lower limit (BMDL) for
aflatoxins (0.170µg/kg/bw /day)
Toxin exposure for each population
They posit that where MOEs is lower than
10,000, a public health concern is indicated which
implied that aflatoxin exposure above
0.000017µg/kg/bw/day (i.e. 0.170µg/kg/bw/day /
10,000) is of public health risks. MOEs for infants,
young children and adults in the above simulations
are 0.15, 0.37 and 0.89 respectively indicating a
high risk of HCC among consumers.
Table 3 also shows the risk of exposure of all the
three populations to other non-genotoxic and non-
carcinogenic mycotoxins such as fumonisins, DON,
OTA, and ZEN. Fumonisins PDI in Sorghum grain in
infants (746.7µg/kg/bw/day), young children
(298.68µg/kg/bw/day) and adults
(124.45µg/kg/bw/day) were higher than the
Tolerable Daily Intake (TDI) of 2µg/kg/bw/day set by
FAO/WHO [66]. PDI of fumonisins in millet, maize
and rice were also above the TDI limits set for the
three populations (infants, young children and
adults). These indicate a high risk of mycotoxicosis
and serious health risk for consumers of these
grains. The PDI of OTA in all the grains (sorghum,
millet, rice and maize) exceeded the TDI values of
0.0171µg/kg/bw/day set by EFSA [67]. OTA
amounts in these grains occurred in the following
order: Rice > maize > millet > sorghum and in the
same direction for the three populations. The PDI of
DON in sorghum, maize, millet and rice were also
above the TDI values of 1µg/kg/bw/day set by EFSA
[68] for DON in food. DON was highest in millet,
followed by Sorghum and maize. Rice had the least
amounts of DON based on the simulations in Table
3. These DON results are higher than
0.08µg/kg/bw/day reported for cereal based food for
infants in Spain [69]. Similarly, the PDI for ZEN in all
the grains were higher than the TDI value of
0.25ug/kg/bw/day set by EFSA [70] for the three
populations.
In general, daily consumption of mycotoxins
(genotoxic and carcinogenic or non-genotoxic and
non-carcinogenic) whether in low concentrations or
not, will eventually lead to public health issues.
Aflatoxin B1 has been implicated in HCC patients in
Annabella A. Adewunmi and Stephen O. Fapohunda
Mycotoxins in Nigerian cereals and public health implications
RAdvFoodSci: 2019: 2(4): 200-216 ISSN: 2601-5412 212
Nigeria and from the above exposure assessment
calculations, the whole population of Nigerians are
at risk whether infant, young children or adults.
Exposure to other mycotoxins also leads to several
pathological effects, which could be teratogenic,
mutagenic, immunosuppressive, haemorrhagic,
hepatotoxic, nephrotoxic, neurotoxic and have
potential to increase susceptibility to HIV [7, 71, 72].
The health effects of mycotoxins in humans are the
rationale behind the reactions and rejections of
Nigerian grains by importing countries like the EU.
Conclusions and Future perspective
Exposure to food borne mycotoxins due to
consumption of contaminated cereal grains in
Nigeria presents serious public health concerns.
Reports on the exposure assessment based on
probable daily intake of the five major mycotoxins in
grains in Nigeria indicates high risk of pathological
cases of HCC and general mycotoxicosis. A daily
consumption survey of the Nigerian population is
necessary to perform a refined exposure
assessment. This will enable proper estimate of
each mycotoxin in all the major cereal grains
consumed daily by Nigerians. Furthermore, in
nature, several mycotoxigenic molds usually
colonize the same food commodity and exist as a
consortium of fungi. These fungi also produce multi-
mycotoxins in the single food item. Risk assessment
has been done on the major mycotoxins as singular
units in the same food, and only considers the effect
of each toxin on human health and not their
combined effect. A major challenge is to determine
the degree of exposure to multi-mycotoxins, as there
is inadequate data on risk assessment of humans
potentially exposed to multi-mycotoxins in food.
Exposure risk assessment should take into
consideration the simultaneous occurrence, the
synergism or antagonism with other mycotoxins in
the same food commodity. For example, where
toxigenic Aspergillus flavus and Aspergillus
ochraceus are isolated in a food unit, it is most likely
that aflatoxin B1 and ochratoxin A will be found
there. Risk assessment has been done for both
individually, but must be performed together
considering the toxicological interactions of the two
mycotoxins and the resultant health effects. For a
better monitoring of food items for mycotoxins,
regulatory authorities should have a controlling
power of assessment of, and compliance to
standards on food items. This makes it necessary
that local production of raw and processed food
items should be vigorously encouraged in each
African country.
Authors Contribution:
AAA chose the topic, researched literature and
wrote the manuscript. SOF gave guidance and
direction, reviewed and edited the manuscript.
Conflict of Interest:
There is no conflict of interest.
Acknowledgement:
We appreciate the contributions of Dr. Chibundu
N. Ezekiel of the department of Microbiology,
Babcock University, Ilishan Remo. Nigeria, for the
suggestions on the initial manuscript.
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