mycotoxins in nigerian cereals and public health … · 2020. 9. 21. · cereals is still low in...

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

mailto:[email protected]

Annabella A. Adewunmi and Stephen O. Fapohunda

Mycotoxins in Nigerian cereals and public health implications


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




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




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.




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]




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]




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




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)




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.)




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.




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




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




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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