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. 2018 Nov 27;35(2):149–155. doi: 10.1007/s12550-018-0337-y

Mycotoxins in poultry feed and feed ingredients in Nigeria

Oyekemi O Akinmusire 1, Abdul-Dahiru El-Yuguda 2, Jasini A Musa 2, Oluwawapelumi A Oyedele 3, Michael Sulyok 4, Yinka M Somorin 5, Chibundu N Ezekiel 3,4,, Rudolf Krska 4,6
PMCID: PMC6478637  PMID: 30484071

Abstract

Mycotoxins are toxic secondary fungal metabolites that can negatively affect animal productivity when ingested through feed. In order to assess mycotoxin contamination of poultry feed and feed ingredients vis-a-vis source tracking of feed contamination in Nigeria, 102 samples of feed (n = 30) and feed ingredients (n = 72) were collected from in-house mills of poultry farms across 12 states of Nigeria and analyzed for multiple mycotoxins using LC/MS-MS. One hundred and forty microbial metabolites were detected in the feed and feed ingredients. The most frequent mycotoxin in the feed was fumonisin B1, occurring in 97% of the samples at mean concentration of 1014 μg kg−1. AFB1 occurred in 83% of the feed samples at mean concentration of 74 μg kg−1 and in all feed ingredients except fish meal and other cereals (millet and rice). Feed samples analyzed in this study were contaminated with at least four mycotoxins: aflatoxins and fumonisin co-occurring in 80% of the samples. Peanut cake and maize contributed the most to the levels of aflatoxin and fumonisin, respectively, in the feed. Consequently, there is a need to explore other cereal- and protein-based ingredients for compounding feeds in order to reduce the risk associated with high mycotoxin (e.g. aflatoxin) intake in poultry.

Electronic supplementary material

The online version of this article (10.1007/s12550-018-0337-y) contains supplementary material, which is available to authorized users.

Keywords: Aflatoxin, Fumonisin, Peanut, Maize, Mycotoxins, Poultry

Introduction

The poultry industry in Nigeria is an essential subsector of agriculture that provides food, employment, and other economic resources for the country (Ezekiel et al. 2012a). Livestock production can be threatened when feeds are contaminated by fungi and their toxic metabolites. Several mycotoxins, including aflatoxins (AFs), cyclopiazonic acid (CPA), fumonisins (FUMs), nivalenol (NIV) and zearalenone (ZEN) have been reported to contaminate poultry feed and their ingredients (Labuda et al. 2005; De Boevre et al. 2012; Ezekiel et al. 2012a; Njobeh et al. 2012; Rodrigues and Naehrer 2012; Abia et al. 2013a; Kana et al. 2013; Streit et al. 2013a, 2013b). The occurrence of mycotoxins in feed ingredients depends on several factors that include climatic conditions, diversity of fungi contaminating the crops, harvesting methods of the individual crops, storage practices, and seasonal variations, while the types and levels of mycotoxins in the feed largely depend on the mycotoxins in the individual feed ingredients, the mix/proportion of feed ingredients, feed processing techniques, and storage practices (Warth et al. 2012; Ezekiel et al. 2014).

Mycotoxins pose a huge threat to the safety and security of livestock first and then to human beings that consume them due to their different toxic effects and their probable synergistic properties (Shephard 2008; Hossain et al. 2011; Njobeh et al. 2012). When animals ingest feed contaminated with high mycotoxin concentrations, mycotoxicoses, often marked by reduced animal productivity (reduced body weight gain, reduced litter sizes, deformed offspring, reduced egg production) and immune suppression (Shareef 2010; Hossain et al. 2011; Streit et al. 2013a), could result to severe economic losses.

Poultry feed ingredients are derived from a variety of raw materials that originate from plants and animals. It is usually a mixture of cereals (mostly maize) that serves as energy source, animal protein sources (fish meal, meat, and bone meal), and plant protein sources (soybean meal and peanut). Maize, the predominant grain used in poultry feeds, can be contaminated by mycotoxins from Aspergillus, Fusarium and Penicillium during processing and storage (Zinedine and Manes 2009; Adetunji et al. 2014). Peanut and its processed products, peanut cake, have been found to be highly susceptible to aflatoxin contamination (Ezekiel et al. 2012b, 2013; Kayode et al. 2013; Oyedele et al. 2017; Ginting et al. 2018).

Globally, mycotoxins in finished poultry feed have been reported (Labuda et al. 2005; De Boevre et al. 2012; Ezekiel et al. 2012a; Njobeh et al. 2012; Rodrigues and Naehrer 2012; Abia et al. 2013a; Kana et al. 2013; Streit et al. 2013b), but there is sparse information on the source tracking of mycotoxin contamination of the feed by individual ingredients, especially in Nigeria. Hence, this study aimed at investigating mycotoxins in poultry feed and the ingredients used in locally formulating the feed in Nigeria with a view to associate contamination of major ingredients to overall contamination in finished feed. This mini-survey provides snapshot data for the consideration of other cereal-based ingredients and protein sources that are less prone to AFs and FUMs contamination in feed formulation.

Materials and methods

Sampling plan and collection of feed samples

Poultry feed and feed ingredients were collected from feed mills in 12 states of Nigeria. The states were primarily selected based on accessibility for sampling and they include Adamawa, Benue, Borno, Delta, Kaduna, Katsina, Kebbi, Lagos, Niger, Oyo, Rivers, and Taraba states. Only in-house feed mills (i.e., feed mills owned by and situated at poultry farms) that had at least 40 bags each of feed and feed ingredients at the time of sampling were considered in the study. The poultry farms were thus the largest farms with in-house mills in the study states. Consequently, only one feed mill was selected per state and at least two feed samples were collected per feed mill. The poultry feed samples included growers’ mash, finisher feed, and layers’ mash, and the collection depended on poultry farm specialization. For every two feed samples collected, one set of ingredients (comprising of individual ingredients depending on use per mill) was obtained. Both feed (n = 30) and feed ingredients (n = 72) were sampled from bulk (50 kg) bags, and the feed ingredients collected were those used in the formulation of the feeds that were sampled. Feed ingredients were from local produce, and they include maize (n = 17), peanut cake (n = 11), wheat offal (n = 10), other cereals (n = 6), soybean (n = 11), bone (n = 9), fish meal (n = 5), and palm kernel (n = 3). Samples (n = 102) were collected for this study during June 2013.

Each sample (4 kg) consisted of four 1 kg representative subsamples: each pooled from a bulk bag of feed/ingredient that was randomly selected out of at least ten feed/ingredient bags. The four randomly selected bags for sampling of feed/ingredient were from the same batch of feed/ingredient in order to reduce variability and ensure the batch was well represented. Each 1 kg subsample consisted of three portions of respective feed/ingredient that weighed 300–350 g. The subsamples were collected by manually probing three points (top, middle, and bottom) of the 50 kg feed/ingredient bags. The samples were thoroughly mixed and quartered successively to give representative samples applied to multi-microbial metabolite analysis.

Quantification of microbial metabolites in feed and feed ingredients

Chemicals

Methanol (LC gradient grade) and glacial acetic acid (p.a.) were purchased from Merck (Darmstadt, Germany), acetonitrile (LC gradient grade) from VWR (Leuven, Belgium), and ammonium acetate (MS grade) from Sigma-Aldrich (Vienna, Austria). Standards for fungal and bacterial metabolites were obtained from various research groups and/or commercial sources. Water was purified successively by reverse osmosis with an Elga Purelab ultra analytic system from Veolia Water (Bucks, UK).

Extraction and estimation of matrix effects

Five grams of each representative sample were weighed into a 50-ml polypropylene tube (Sarstedt, Nümbrecht, Germany) and 20 ml of the extraction solvent (acetonitrile/water/acetic acid 79:20:1, v/v/v) added. For spiking experiments, 0.25 g samples were used for extraction. Samples were extracted for 90 min on a GFL 3017 rotary shaker (GFL, Burgwedel, Germany) and diluted with the same volume of dilution solvent (acetonitrile/water/acetic acid 20:79:1, v/v/v), and the diluted extracts were injected into the LC instrument (Sulyok et al. 2006). Centrifugation was not necessary due to sufficient sedimentation by gravity. Apparent recoveries of the analytes were cross-checked by spiking three different samples that were not contaminated with mycotoxins with a multi-analyte standard on one concentration level, since previously generated data are available (Ezekiel et al. 2012a; Warth et al. 2012; Abia et al. 2013b).

LC-MS/MS parameters

LC-MS/MS screening of target microbial metabolites was performed with a QTrap 5500 LC-MS/MS System (Applied Biosystems, Foster City, CA, USA) equipped with TurboIonSpray electrospray ionization (ESI) source and a 1290 Series HPLC System (Agilent, Waldbronn, Germany). Chromatographic separation was performed at 25 °C on a Gemini® C18-column, 150 × 4.6 mm ID, 5 μm particle size, equipped with a C18 4 × 3 mm ID security guard cartridge (Phenomenex, Torrance, CA, USA). The chromatographic method, chromatographic, and mass spectrometric parameters are as described by Malachová et al. (2014). ESI-MS/MS was performed in the time-scheduled multiple reaction monitoring (MRM) mode both in positive and negative polarities in two separate chromatographic runs per sample by scanning two fragmentation reactions per analyte. The MRM detection window of each analyte was set to its expected retention time ± 27 and ± 48 s in the positive and the negative modes, respectively. Confirmation of positive analyte identification was obtained by the acquisition of two MRMs per analyte (with the exception of moniliformin (MON), which exhibited only one fragment ion). This yielded 4.0 identification points according to European Commission decision 2002/657 (EU 2002). In addition, the LC retention time and the intensity ratio of the two MRM transitions agreed with the related values of an authentic standard within 0.1 min and 30%, respectively. The accuracy of the method is monitored on a routine basis by regular participation in proficiency testing organized by BIPEA (Gennevilliers, France). Eight hundred and twenty-four out of 875 results submitted overall, and 121 out of 129 results submitted for animal feed were in the satisfactory range of − 2 < z < 2 (results until March 2018 included).

Results and discussion

Overview of multiple microbial metabolite occurrences in feed and ingredients

The performance of the LC-MS/MS method is described in Table S1. A total of 140 microbial metabolites were detected in the feed (121 metabolites; Tables 1 and S2) and feed ingredients (132 metabolites; Tables 2, 3, S3, and S4). Major mycotoxins such as AFs, DON, FUMs, NIV, ochratoxin A (OTA), T-2 and HT-2, ZEN and their metabolites were found to contaminate the compounded feed and feed ingredients at different incidences and concentrations. The spectrum of metabolites including mycotoxins reported herein are quite similar to the metabolite diversity in Streit et al. (2013b) but more than those previously reported in feed and feed ingredients (De Boevre et al. 2012; Ezekiel et al. 2012a; Njobeh et al. 2012; Rodrigues and Naehrer 2012; Abia et al. 2013a; Streit et al. 2013b).

Table 1.

Occurrence levels of 23 major mycotoxins in 30 poultry feed samples from Nigeria

Metabolites Percenta Concentration (μg/kg)
Min Max Mean
Aflatoxin B1 83.3 0.5 760 74
Aflatoxin B2 50.0 1.7 188 21
Aflatoxin G1 56.7 1.6 79 19
Aflatoxin G2 13.3 0.5 7.6 3.5
Aflatoxin M1 23.3 1.7 41 9.9
Alternariol (AOH) 40.0 0.2 8.6 2.7
AOHmethylether 46.7 0.2 5.6 1.4
Beauvericin 100 0.5 127 13
Citrinin 16.7 38 2340 522
Cyclopiazonic acid 10.0 23 49 39
Deoxynivalenol 20.0 36 174 108
Fumonisin B1 (FB1) 96.7 37 3760 1014
Fumonisin B2 93.3 9.2 870 310
Fumonisin B3 90.0 9.0 149 62
Fumonisin B4 96.7 3.3 168 623
Hydrolyzed FB1 56.7 5820 86,800 28,958
Moniliformin 93.3 5.1 900 62
Nivalenol 23.3 13 647 114
Ochratoxin A 26.7 0.8 15 5.4
Ochratoxin B 20.0 1.2 24 9.3
Tenuazonic acid 70.0 5.2 315 44
Zearalenone (ZEN) 83.3 0.5 71 9.3
ZEN-sulfate 13.3 3.2 162 56

aIncidence of contamination expressed in percentage

Table 2.

Distribution of 23 major mycotoxins in 44 cereal and nut ingredients for poultry feed in Nigeria

Metabolites Maize (na = 17; nb = 84) Peanut cake (na = 11; nb = 68) Wheat offal (na = 10; nb = 106) Other cereals (na = 6; nb = 39)
Percentc Concentration (μg/kg) Percentc Concentration (μg/kg) Percent Concentration (μg/kg) Percentc Concentration (μg/kg)
Min Max Mean Min Max Mean Min Max Mean Min Max Mean
Aflatoxin B1 47.1 6.1 567 176 90.9 61 3860 639 30.0 1.3 80 53 n.d n.d n.d n.d
Aflatoxin B2 23.5 3.3 61 35 90.9 6.6 895 126 10.0 5.9 5.9 0.0 n.d n.d n.d n.d
Aflatoxin G1 41.2 2.0 725 110 90.9 17 568 157 20.0 13 14 14 n.d n.d n.d n.d
Aflatoxin G2 5.9 60 60 0.0 54.5 2.5 68 27 n.d n.d n.d n.d n.d n.d n.d n.d
Aflatoxin M1 17.6 25 70 45 72.7 14 254 49 20.0 5.1 5.3 5.2 16.7 1.6 1.6 0.0
Alternariol (AOH) 11.8 0.4 0.4 0.4 n.d n.d n.d n.d 70.0 2.7 23 12 n.d n.d n.d n.d
AOHmethylether 23.5 0.3 1.0 0.5 9.1 0.1 0.1 0.0 90.0 0.4 8.9 4.2 n.d n.d n.d n.d
Beauvericin 100 0.1 33 7.7 100 0.8 9.7 2.3 90.0 2.3 37 13 83.3 1.4 8.7 5.6
Citrinin 17.6 789 9400 4229 9.1 150 150 0.0 n.d n.d n.d n.d n.d n.d n.d n.d
Cyclopiazonic acid 5.9 98 98 0.0 27.3 34 204 93 n.d n.d n.d n.d n.d n.d n.d n.d
Deoxynivalenol n.d n.d n.d n.d n.d n.d n.d n.d 50.0 348 837 578 16.7 22 22 0.0
Fumonisin B1 (FB1) 100 164 2090 825 27.3 4.7 910 308 50.0 2.8 67 37 16.7 0.9 0.9 0.0
Fumonisin B2 100 46 710 262 18.2 0.9 340 171 50.0 1.3 15 7.9 16.7 1.5 1.5 0.0
Fumonisin B3 100 10 186 69 9.1 62 62 0.0 10.0 6.9 6.9 0.0 n.d n.d n.d n.d
Fumonisin B4 100 16 253 98 9.1 55 55 0.0 40.0 3.5 6.0 5.0 n.d n.d n.d n.d
Hydrolyzed FB1 76.5 3500 80,500 24,089 n.d n.d n.d n.d 10.0 3150 3150 0.0 n.d n.d n.d n.d
Moniliformin 88.2 12 246 74 81.8 0.3 16 6.0 100 4.8 60 17 66.7 4.5 307 102
Nivalenol 23.5 9.7 17 14 9.1 64 64 0.0 10.0 4.7 4.7 0.0 n.d n.d n.d n.d
Ochratoxin A 11.8 1.3 3.1 2.2 54.5 0.1 127 35 20.0 0.6 1.0 0.8 33.3 0.5 3.6 2.0
Ochratoxin B 5.9 3.7 3.7 0.0 18.2 158 302 230 n.d n.d n.d n.d n.d n.d n.d n.d
Tenuazonic acid 5.9 7.8 7.8 0.0 n.d n.d n.d n.d 90.0 60 679 190 66.7 34 80 53
Zearalenone (ZEN) 64.7 0.1 4.8 1.2 18.2 0.7 1.1 0.9 90.0 0.4 67 19 n.d n.d n.d n.d
ZEN-sulfate n.d n.d n.d n.d n.d n.d n.d n.d 20.0 31.8 33 33 n.d n.d n.d n.d

n.d not detected

aNumber of samples analyzed

bNumber of metabolites detected

cIncidence of contamination expressed in percentage

Table 3.

Occurrence levels of 23 major mycotoxins in 28 other ingredients for poultry feed in Nigeria

Metabolites Bone (na = 9; nb = 59) Fish meal (na = 5; nb = 25) Palm kernel (na = 3; nb = 68) Soybean (na = 11; nb = 52)
Percentc Concentration (μg/kg) Percentc Concentration (μg/kg) Percentc Concentration (μg/kg) Percentc Concentration (μg/kg)
Min Max Mean Min Max Mean Min Max Mean Min Max Mean
Aflatoxin B1 33.3 1.9 52 19 n.d n.d n.d n.d 100 32 397 162 45.5 0.7 91 38
Aflatoxin B2 11.1 9.0 9.0 0.0 n.d n.d n.d n.d 100 6.9 57 25 18.2 5.9 8.0 6.9
Aflatoxin G1 11.1 6.3 6.3 0.0 n.d n.d n.d n.d 100 6.5 198 71 45.5 0.3 20 4.9
Aflatoxin G2 n.d n.d n.d n.d n.d n.d n.d n.d 33.3 12 12 0.0 n.d n.d n.d n.d
Aflatoxin M1 n.d n.d n.d n.d n.d n.d n.d n.d 33.3 21 21 0.0 9.1 3.5 3.5 0.0
Alternariol (AOH) n.d n.d n.d n.d n.d n.d n.d n.d 100 4.0 12 8.1 9.1 1.3 1.3 0.0
AOHmethylether 11.1 0.6 0.6 0.0 n.d n.d n.d n.d 100 7.1 8.8 8.1 18.2 0.2 0.6 0.4
Beauvericin 11.1 4.2 4.2 0.0 100 0.1 0.5 0.3 100 0.2 9.9 3.5 90.9 0.5 4.8 1.5
Cyclopiazonic acid n.d n.d n.d n.d n.d n.d n.d n.d 33.3 44 44 0.0 n.d n.d n.d n.d
Fumonisin B1 (FB1) n.d n.d n.d n.d n.d n.d n.d n.d 66.7 58 122 90 18.2 44 46 45
Fumonisin B2 n.d n.d n.d n.d n.d n.d n.d n.d 66.7 29 33 31 18.2 12 17 15
Fumonisin B3 n.d n.d n.d n.d n.d n.d n.d n.d 33.3 4.1 4.1 0.0 9.1 1.8 1.8 0.0
Fumonisin B4 11.1 0.9 0.9 0.0 n.d n.d n.d n.d 66.7 5.2 8.4 6.8 9.1 5.6 5.6 0.0
Hydrolyzed FB1 n.d n.d n.d n.d n.d n.d n.d n.d 33.3 5750 5750 0.0 n.d n.d n.d n.d
Moniliformin n.d n.d n.d n.d n.d n.d n.d n.d 100 7.2 17 14 18.2 28 63 45
Ochratoxin A 11.1 0.1 0.1 0.0 n.d n.d n.d n.d 33.3 1.0 1.0 0.0 9.1 3.7 3.7 0.0
Ochratoxin B n.d n.d n.d n.d n.d n.d n.d n.d n.d n.d n.d n.d 9.1 15 15 0.0
Tenuazonic acid 11.1 22 22 0.0 100 13 47 36 33.3 4.2 4.2 0.0 27.3 12 128 55
Zearalenone (ZEN) 11.1 6.5 6.5 0.0 n.d n.d n.d n.d 66.7 0.3 0.6 0.4 54.5 0.3 1.0 0.6
ZEN-sulfate 11.1 1.2 1.2 0.0 n.d n.d n.d n.d n.d n.d n.d n.d n.d n.d n.d n.d

n.d not detected

aNumber of samples analyzed

bNumber of metabolites detected

cIncidence of contamination expressed in percentage

Occurrence of major mycotoxins in feed and feed ingredients

Twenty-three mycotoxins were found in the compounded feed samples (Table 1) and their ingredients (Tables 2 and 3). The most frequently detected mycotoxin in the feed was fumonisin B1 (FB1; incidence, 97%; range, 37–3760 μg kg−1; mean, 1014 μg kg−1). FUMs were also quantified in all feed ingredients except bone and fish meal (Tables 2 and 3). Fumonisin B1 occurred in all (100%) the maize samples (range, 164–2090 μg kg−1; mean, 825 μg kg−1), and surprisingly was detected in 27% of 11 peanut cake samples due to co-storage of bags of maize grains and processed peanut cake in non-ventilated warehouses leading to deposited maize grain dust on the peanut cakes. The reported incidence and concentration of FUMs in feed samples in the present study are higher than previous reports of relatively high FUM levels in feed from poultry farms in Cameroon (100%; range, 16–1930 μg kg−1; mean, 468 μg kg−1; Abia et al. 2013a), commercially produced feed from Nigeria (83%; range, 31–2733 μg kg−1; mean, 964 μg kg−1; Ezekiel et al. 2012a), and commercially compounded feed from South Africa (87%; range, 104–2999 μg kg−1; mean, 903 μg kg−1; Njobeh et al. 2012). The high-FUM contamination level of feed in the present study may reflect the higher FUM contamination of maize samples used to formulate the feed samples in our study compared to the commercially processed feed analyzed by the other studies. This is also suggested by the significant correlation (r2 = 0.405, p = 0.03) obtained for total FUM concentrations in maize and in the compounded feed.

Aflatoxin B1 was detected in 83% of the analyzed feed samples (range, 0.5–760 μg kg−1; mean, 74 μg kg−1) (Table 1) and in all feed ingredients except fish meal and other cereals (millet and rice; Tables 2 and 3). The AFB1 content in feed ingredients reached 397 μg kg−1 and 3860 μg kg−1 in palm kernel and peanut cake, respectively, with the highest mean level (639 μg kg−1) recorded in peanut cake and the lowest found in bone (19 μg kg−1). Other aflatoxin types, B2, G1, G2, and M1, were also found in the feed and ingredient samples albeit at lower incidences (and levels). The vast contamination of the feed and feed ingredients with AFs agrees with several previous reports of high aflatoxin contamination of cereals, nuts, legumes, oilseeds, and their products in Nigeria (Ezekiel et al. 2012b, 2013; Adetunji et al. 2014; Egbontan et al. 2017; Oyedele et al. 2017) as well as with the aflatoxin contamination of feed samples from different countries (Cameroon, India, Nigeria, and South Africa), albeit at a relatively higher contamination level than samples from these previous studies (Oluwafemi et al. 2009; Njobeh et al. 2012; Abia et al. 2013a; Kehinde et al. 2014; Kotinagu et al. 2015). However, our previous paper on commercial poultry feed in Nigeria reported higher concentrations (max, 1067 μg kg−1; mean, 198 μg kg−1) (Ezekiel et al. 2012a) than the present study. The disparity in aflatoxin contamination data in the several studies including the present paper may be attributed to a combination of factors ranging from climatic factors, agricultural, and processing (handling and storage) practices for raw materials, to the formulation mix utilized during compounding of the feed. A significant correlation (r2 = 0.473, p = 0.03) was recorded for AFB1 levels in peanut cake and in the analyzed feed. This agrees with the report of Atawodi et al. (1994) that food and feed containing peanut are most contaminated with AFs: a possible reason for the high AF levels in feed samples in the present study.

Other major mycotoxins found in the analyzed feed samples include citrinin (CIT), deoxynivalenol (DON), NIV, OTA, and ZEN (Table 2). Citrinin was detected in 17% of the feed (max, 2340 μg kg−1; mean, 522 μg kg−1), while the trichothecenes, DON and NIV, contaminated at least 20% of the samples at concentrations reaching 174 μg kg−1 (mean, 108 μg kg−1) and 647 μg kg−1 (mean, 114 μg kg−1), respectively. The mean concentrations of OTA and ZEN in the feed were less than 10 μg kg−1. The mean levels for the aforementioned mycotoxins, except CIT, as observed in this study, are lower than those previously reported in commercial feed from Nigeria (Ezekiel et al. 2012a) and South Africa (Njobeh et al. 2012), and from feed collected on farms in Cameroon (Abia et al. 2013a). Similar to the report of Abia et al. (2013a), CIT was found in feed samples, albeit at much higher concentrations. Furthermore, we document the uncommon presence of tenuazonic acid in feed and almost all the ingredients; a mycotoxin recently reported in members of the Aspergillus section Flavi (Frisvad et al. 2019), which are common contaminants of several stored food items including grains and fish products.

Overall, all feed samples in this study were contaminated with at least four mycotoxins, with AFs and FUM co-occurring in 80% of the samples. Mixtures of several mycotoxins such as those observed in this study have been suggested to induce a range of antagonistic, additive, or synergistic effects in various cells and organs of animals including poultry (Grenier and Oswald 2011); however, the toxicity effects of mycotoxin combinations are not always predicted based on individual toxin toxicities. In addition, despite the toxin contamination data shown in this mini-survey, categorical views on the possible adverse health impacts will be premature in view of the low numbers of feed and ingredient samples analyzed and underrepresentation of the country in this study.

This mini-survey has shown that mycotoxin contamination of locally formulated poultry feed in some parts of Nigeria may be high, with maize and peanut contributing significantly to the respective FUM and AF levels in the studied feed samples. The co-contamination of feed samples with diverse mycotoxins/metabolites of varying concentrations suggests possible health risk to the animals and reduced profitability for the farmers. The following options are therefore suggested for implementation in an integrated manner to control mycotoxins in the poultry sector: (1) adoption of good agricultural practices including the application of available biological control products to crops in order to lower the contamination levels, (2) provision of good storage conditions for grains intended for poultry feed formulation to limit fungal proliferation and further toxin accumulation, (3) monitoring of mycotoxins in locally compounded feed and feed ingredients, (4) exploration of alternative and easily accessible crops (e.g., bambara nut, millet, sorghum) that may be less prone to AF and FUM contamination, and (5) educational training programs on mycotoxin reduction strategies for farmers and millers involved with the poultry industry.

Electronic supplementary material

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Funding Information

Open access funding provided by University of Natural Resources and Life Sciences Vienna (BOKU).

Compliance with ethical standard

Conflict of interest

None.

References

  1. Abia WA, Simo GN, Warth B, Suyolk M, Krska R, Tchana A, Moundipa PF. Determination of multiple mycotoxins levels in poultry feeds from Cameroon. Jpn J Vet Res. 2013;61(Suppl):S33–S39. [PubMed] [Google Scholar]
  2. Abia WA, Warth B, Sulyok M, Krska R, Tchana AN, Njobeh PB, Dutton MF, Moundipa PF. Determination of multi-mycotoxin occurrence in cereals, nuts and their products in Cameroon by liquid chromatography tandem mass spectrometry (LC-MS/MS) Food Control. 2013;21:438–453. doi: 10.1016/j.foodcont.2012.10.006. [DOI] [Google Scholar]
  3. Adetunji MC, Atanda O, Ezekiel CN, Suyolk M, Warth B, Beltran E, Krska R, Obadina A, Bakare A, Chilaka CA. Fungal and bacterial metabolites of stored maize from five agro-ecological zones of Nigeria. Mycotoxin Res. 2014;30:89–102. doi: 10.1007/s12550-014-0194-2. [DOI] [PubMed] [Google Scholar]
  4. Atawodi SE, Atiku AA, Lamorde AG. Aflatoxin contamination of Nigerian foods and feedingstuffs. Food Chem Toxicol. 1994;32:61–63. doi: 10.1016/0278-6915(84)90038-3. [DOI] [PubMed] [Google Scholar]
  5. De Boevre M, Di Mavungu JD, Landschoot S, Audenaert K, Eeckhout M, Maene P, Haesaert G, De Saeger S. Natural occurrence of mycotoxins and their masked forms in food and feed products. World Mycotoxin J. 2012;5(3):207–219. doi: 10.3920/WMJ2012.1410. [DOI] [Google Scholar]
  6. Egbontan AO, Afolabi CG, Kehinde IA, Enikuomehin OA, Ezekiel CN, Sulyok M, Warth B, Krska R. A mini-survey of moulds and mycotoxins in locally grown and imported wheat grains in Nigeria. Mycotoxin Res. 2017;33(1):59–64. doi: 10.1007/s12550-016-0264-8. [DOI] [PubMed] [Google Scholar]
  7. European Commission Commission Decision (EC) No. 2002/657 of 12th August 2002. Implementing Council Directive EC No 96/23 concerning the performance of analytical methods and the interpretation of results. Off J Eur Union. 2002;L221:8–36. [Google Scholar]
  8. Ezekiel CN, Bandyopadhyay R, Sulyok M, Warth B, Krska R. Fungal and bacterial metabolites in commercial poultry feed from Nigeria. Food Addit Contamin Part A. 2012;29:1288–1299. doi: 10.1080/19440049.2012.688878. [DOI] [PubMed] [Google Scholar]
  9. Ezekiel CN, Sulyok M, Warth B, Odebode AC, Krska R. Natural occurrence of mycotoxins in peanut cake from Nigeria. Food Control. 2012;27:338–342. doi: 10.1016/j.foodcont.2012.04.010. [DOI] [Google Scholar]
  10. Ezekiel CN, Sulyok M, Babalola DA, Warth B, Ezekiel VC, Krska R. Incidence and consumer awareness of toxigenic Aspergillus section Flavi and aflatoxin B1 in peanut cake from Nigeria. Food Control. 2013;30:596–601. doi: 10.1016/j.foodcont.2012.07.048. [DOI] [Google Scholar]
  11. Ezekiel CN, Atehnkeng J, Odebode AC, Bandyopadhyay R. Distribution of aflatoxigenic Aspergillus section Flavi in commercial poultry feed in Nigeria. Int J Food Microbiol. 2014;189:18–25. doi: 10.1016/j.ijfoodmicro.2014.07.026. [DOI] [PubMed] [Google Scholar]
  12. Frisvad JC, Hubka V, Ezekiel CN, Hong S-B, Novakova A, Chen AJ, Arzanlou M, TO L, Sklenar F, Mahakarnchanakul W, Samson RA, Houbraken J. Taxonomy of Aspergillus section Flavi and their production of aflatoxins, ochratoxins and other mycotoxins. Stud Mycol. 2019;93:1–63. doi: 10.1016/j.simyco.2018.06.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ginting E, Rahmianna AA, Yusnawan E. Aflatoxin and nutrient content of peanut collected from local market and their processed foods. IOP Conf Ser: Earth Environ Sci. 2018;102:012–031. [Google Scholar]
  14. Grenier B, Oswald I. Mycotoxin co-contamination of food and feed: meta-analysis of publications describing toxicological interactions. World Mycotoxin J. 2011;4(3):285–313. doi: 10.3920/WMJ2011.1281. [DOI] [Google Scholar]
  15. Hossain SA, Haque N, Kumar M, Sontakke UB, Tyagi AK. Mycotoxin residues in poultry product: their effect on human health and control. Wayamba J Anim Sci. 2011;2011:92–96. [Google Scholar]
  16. Kana JR, Gnonlonfin BGJ, Harvey J, Wainaina J, Wanjuki I, Skilton RA, Teguia A. Assessment of aflatoxin contamination of maize, peanut meal and poultry feed mixtures from different agroecological zones in Cameroon. Toxins. 2013;5:884–894. doi: 10.3390/toxins5050884. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kayode OF, Sulyok M, Fapohunda SO, Ezekiel CN, Krska R, Oguntona CRB. Mycotoxins and fungal metabolites in groundnut- and maize-based snacks from Nigeria. Food Addit Contamin Part B Surveill. 2013;6(4):294–300. doi: 10.1080/19393210.2013.823626. [DOI] [PubMed] [Google Scholar]
  18. Kehinde MT, Oluwafemi F, Itoandon EE, Orji FA, Ajayi OI. Fungal profile and aflatoxin contamination in poultry feeds sold in Abeokuta, Ogun State, Nigeria. Nig Food J. 2014;32:73–79. doi: 10.1016/S0189-7241(15)30098-9. [DOI] [Google Scholar]
  19. Kotinagu K, Mohanamba T, Kumari LR. Assessment of aflatoxin B1 in livestock feed and feed ingredients by high-performance thin layer chromatography. Vet World. 2015;8:1396–1399. doi: 10.14202/vetworld.2015.1396-1399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Labuda R, Parich A, Veikru E, Tancinova D. Incidence of fumonisins, moniliformin and Fusarium species in poultry feed mixtures from Slovakia. Ann Agric Environ Med. 2005;12:81–86. [PubMed] [Google Scholar]
  21. Malachová A, Sulyok M, Beltrán E, Berthiller F, Krska R. Optimization and validation of a quantitative liquid chromatography–tandem mass spectrometric method covering 295 bacterial and fungal metabolites including all regulated mycotoxins in four model food matrices. J Chromatogr A. 2014;1362:145–156. doi: 10.1016/j.chroma.2014.08.037. [DOI] [PubMed] [Google Scholar]
  22. Njobeh PB, Dutton MF, Aberg AT, Haggblom P. Estimation of multi-mycotoxin contamination in South African compound feeds. Toxins. 2012;4:836–848. doi: 10.3390/toxins4100836. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Oluwafemi F, Kehinde MT, Elegbede FF, Alfia OM, Dike CC. Determination of aflatoxin levels in commercial poultry feeds sold in some parts of southwestern Nigeria. J Nat Sci Engr Tech. 2009;8:34–41. [Google Scholar]
  24. Oyedele OA, Ezekiel CN, Sulyok M, Adetunji MC, Warth B, Atanda OO, Krska R. Mycotoxin risk assessment of consumers of groundnut in domestic markets in Nigeria. Int J Food Microbiol. 2017;25:24–32. doi: 10.1016/j.ijfoodmicro.2017.03.020. [DOI] [PubMed] [Google Scholar]
  25. Rodrigues I, Naehrer K. A three-year survey on the worldwide occurrence of mycotoxins in feedstuffs and feeds. Toxins. 2012;4:663–675. doi: 10.3390/toxins4090663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Shareef AM. Molds and mycotoxins in poultry feeds from farms of potential mycotoxicosis. Iraqi J Vet Sci. 2010;24(1):17–25. doi: 10.33899/ijvs.2010.5581. [DOI] [Google Scholar]
  27. Shephard GS. Determination of mycotoxins in human foods. Chem Soc Rev. 2008;37:2468–2477. doi: 10.1039/b713084h. [DOI] [PubMed] [Google Scholar]
  28. Streit E, Nahrer K, Rodrigues I, Schatzmayr G. Mycotoxin occurrence in feed and feed raw materials worldwide: long-term analysis with special focus on Europe and Asia. J Sci Food Agric. 2013;93(12):2892–2899. doi: 10.1002/jsfa.6225. [DOI] [PubMed] [Google Scholar]
  29. Streit E, Schwab C, Sulyok M, Naehrer K, Krska R, Schatzmayr G. Multimycotoxin screening reveals the occurrence of 139 different metabolites in feed and feed ingredients. Toxins. 2013;5:504–523. doi: 10.3390/toxins5030504. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Sulyok M, Berthiller F, Krska R, Schuhmacher R. Development and validation of a liquid chromatography/tandem mass spectrometric method for the determination of 39 mycotoxins in wheat and maize. Rapid Commun Mass Spectrom. 2006;20:2649–2659. doi: 10.1002/rcm.2640. [DOI] [PubMed] [Google Scholar]
  31. Warth B, Parich A, Atehnkeng J, Bandyopadhyay R, Schuhmacher R, Sulyok M, Krska R. Quantitation of mycotoxins in food and feed from Burkina Faso and Mozambique using a modern LC-MS/MS multitoxin method. J Agric Food Chem. 2012;60(36):9352–9363. doi: 10.1021/jf302003n. [DOI] [PubMed] [Google Scholar]
  32. Zinedine A, Manes J. Occurrence and legislation of mycotoxins in food and feed from Morrocco. Food Control. 2009;20:334–344. doi: 10.1016/j.foodcont.2008.07.002. [DOI] [Google Scholar]

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