Advertisement

Mycotoxins in poultry feed and feed ingredients in Nigeria

  • Oyekemi O. Akinmusire
  • Abdul-Dahiru El-Yuguda
  • Jasini A. Musa
  • Oluwawapelumi A. Oyedele
  • Michael Sulyok
  • Yinka M. Somorin
  • Chibundu N. Ezekiel
  • Rudolf Krska
Open Access
Original Article
  • 252 Downloads

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.

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.

Notes

Funding Information

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

Compliance with ethical standard

Conflict of interest

None.

Supplementary material

12550_2018_337_MOESM1_ESM.docx (158 kb)
ESM 1 (DOCX 158 kb)

References

  1. Abia WA, Simo GN, Warth B, Suyolk M, Krska R, Tchana A, Moundipa PF (2013a) Determination of multiple mycotoxins levels in poultry feeds from Cameroon. Jpn J Vet Res 61(Suppl):S33–S39PubMedGoogle Scholar
  2. Abia WA, Warth B, Sulyok M, Krska R, Tchana AN, Njobeh PB, Dutton MF, Moundipa PF (2013b) Determination of multi-mycotoxin occurrence in cereals, nuts and their products in Cameroon by liquid chromatography tandem mass spectrometry (LC-MS/MS). Food Control 21:438–453CrossRefGoogle Scholar
  3. Adetunji MC, Atanda O, Ezekiel CN, Suyolk M, Warth B, Beltran E, Krska R, Obadina A, Bakare A, Chilaka CA (2014) Fungal and bacterial metabolites of stored maize from five agro-ecological zones of Nigeria. Mycotoxin Res 30:89–102CrossRefGoogle Scholar
  4. Atawodi SE, Atiku AA, Lamorde AG (1994) Aflatoxin contamination of Nigerian foods and feedingstuffs. Food Chem Toxicol 32:61–63CrossRefGoogle Scholar
  5. De Boevre M, Di Mavungu JD, Landschoot S, Audenaert K, Eeckhout M, Maene P, Haesaert G, De Saeger S (2012) Natural occurrence of mycotoxins and their masked forms in food and feed products. World Mycotoxin J 5(3):207–219CrossRefGoogle Scholar
  6. Egbontan AO, Afolabi CG, Kehinde IA, Enikuomehin OA, Ezekiel CN, Sulyok M, Warth B, Krska R (2017) A mini-survey of moulds and mycotoxins in locally grown and imported wheat grains in Nigeria. Mycotoxin Res 33(1):59–64CrossRefGoogle Scholar
  7. European Commission (2002) 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 L221:8–36Google Scholar
  8. Ezekiel CN, Bandyopadhyay R, Sulyok M, Warth B, Krska R (2012a) Fungal and bacterial metabolites in commercial poultry feed from Nigeria. Food Addit Contamin Part A 29:1288–1299CrossRefGoogle Scholar
  9. Ezekiel CN, Sulyok M, Warth B, Odebode AC, Krska R (2012b) Natural occurrence of mycotoxins in peanut cake from Nigeria. Food Control 27:338–342CrossRefGoogle Scholar
  10. Ezekiel CN, Sulyok M, Babalola DA, Warth B, Ezekiel VC, Krska R (2013) Incidence and consumer awareness of toxigenic Aspergillus section Flavi and aflatoxin B1 in peanut cake from Nigeria. Food Control 30:596–601CrossRefGoogle Scholar
  11. Ezekiel CN, Atehnkeng J, Odebode AC, Bandyopadhyay R (2014) Distribution of aflatoxigenic Aspergillus section Flavi in commercial poultry feed in Nigeria. Int J Food Microbiol 189:18–25CrossRefGoogle 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 (2019) Taxonomy of Aspergillus section Flavi and their production of aflatoxins, ochratoxins and other mycotoxins. Stud Mycol 93:1–63CrossRefGoogle Scholar
  13. Ginting E, Rahmianna AA, Yusnawan E (2018) Aflatoxin and nutrient content of peanut collected from local market and their processed foods. IOP Conf Ser: Earth Environ Sci 102:012–031Google Scholar
  14. Grenier B, Oswald I (2011) Mycotoxin co-contamination of food and feed: meta-analysis of publications describing toxicological interactions. World Mycotoxin J 4(3):285–313CrossRefGoogle Scholar
  15. Hossain SA, Haque N, Kumar M, Sontakke UB, Tyagi AK (2011) Mycotoxin residues in poultry product: their effect on human health and control. Wayamba J Anim Sci 2011:92–96Google Scholar
  16. Kana JR, Gnonlonfin BGJ, Harvey J, Wainaina J, Wanjuki I, Skilton RA, Teguia A (2013) Assessment of aflatoxin contamination of maize, peanut meal and poultry feed mixtures from different agroecological zones in Cameroon. Toxins 5:884–894CrossRefGoogle Scholar
  17. Kayode OF, Sulyok M, Fapohunda SO, Ezekiel CN, Krska R, Oguntona CRB (2013) Mycotoxins and fungal metabolites in groundnut- and maize-based snacks from Nigeria. Food Addit Contamin Part B Surveill 6(4):294–300CrossRefGoogle Scholar
  18. Kehinde MT, Oluwafemi F, Itoandon EE, Orji FA, Ajayi OI (2014) Fungal profile and aflatoxin contamination in poultry feeds sold in Abeokuta, Ogun State, Nigeria. Nig Food J 32:73–79CrossRefGoogle Scholar
  19. Kotinagu K, Mohanamba T, Kumari LR (2015) Assessment of aflatoxin B1 in livestock feed and feed ingredients by high-performance thin layer chromatography. Vet World 8:1396–1399CrossRefGoogle Scholar
  20. Labuda R, Parich A, Veikru E, Tancinova D (2005) Incidence of fumonisins, moniliformin and Fusarium species in poultry feed mixtures from Slovakia. Ann Agric Environ Med 12:81–86PubMedGoogle Scholar
  21. Malachová A, Sulyok M, Beltrán E, Berthiller F, Krska R (2014) 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 1362:145–156CrossRefGoogle Scholar
  22. Njobeh PB, Dutton MF, Aberg AT, Haggblom P (2012) Estimation of multi-mycotoxin contamination in South African compound feeds. Toxins 4:836–848CrossRefGoogle Scholar
  23. Oluwafemi F, Kehinde MT, Elegbede FF, Alfia OM, Dike CC (2009) Determination of aflatoxin levels in commercial poultry feeds sold in some parts of southwestern Nigeria. J Nat Sci Engr Tech 8:34–41Google Scholar
  24. Oyedele OA, Ezekiel CN, Sulyok M, Adetunji MC, Warth B, Atanda OO, Krska R (2017) Mycotoxin risk assessment of consumers of groundnut in domestic markets in Nigeria. Int J Food Microbiol 25:24–32CrossRefGoogle Scholar
  25. Rodrigues I, Naehrer K (2012) A three-year survey on the worldwide occurrence of mycotoxins in feedstuffs and feeds. Toxins 4:663–675CrossRefGoogle Scholar
  26. Shareef AM (2010) Molds and mycotoxins in poultry feeds from farms of potential mycotoxicosis. Iraqi J Vet Sci 24(1):17–25Google Scholar
  27. Shephard GS (2008) Determination of mycotoxins in human foods. Chem Soc Rev 37:2468–2477CrossRefGoogle Scholar
  28. Streit E, Nahrer K, Rodrigues I, Schatzmayr G (2013a) Mycotoxin occurrence in feed and feed raw materials worldwide: long-term analysis with special focus on Europe and Asia. J Sci Food Agric 93(12):2892–2899CrossRefGoogle Scholar
  29. Streit E, Schwab C, Sulyok M, Naehrer K, Krska R, Schatzmayr G (2013b) Multimycotoxin screening reveals the occurrence of 139 different metabolites in feed and feed ingredients. Toxins 5:504–523CrossRefGoogle Scholar
  30. Sulyok M, Berthiller F, Krska R, Schuhmacher R (2006) 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 20:2649–2659CrossRefGoogle Scholar
  31. Warth B, Parich A, Atehnkeng J, Bandyopadhyay R, Schuhmacher R, Sulyok M, Krska R (2012) Quantitation of mycotoxins in food and feed from Burkina Faso and Mozambique using a modern LC-MS/MS multitoxin method. J Agric Food Chem 60(36):9352–9363CrossRefGoogle Scholar
  32. Zinedine A, Manes J (2009) Occurrence and legislation of mycotoxins in food and feed from Morrocco. Food Control 20:334–344CrossRefGoogle Scholar

Copyright information

© The Author(s) 2018

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  • 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
  1. 1.Department of MicrobiologyUniversity of MaiduguriMaiduguriNigeria
  2. 2.Department of Veterinary MicrobiologyUniversity of MaiduguriMaiduguriNigeria
  3. 3.Department of MicrobiologyBabcock UniversityIlishan RemoNigeria
  4. 4.Center for Analytical Chemistry, Department of Agrobiotechnology (IFA-Tulln)University of Natural Resources and Life Sciences Vienna (BOKU)TullnAustria
  5. 5.Microbiology, School of Natural SciencesNational University of IrelandGalwayIreland
  6. 6.Institute for Global Food Security, School of Biological SciencesQueen’s University BelfastBelfastUK

Personalised recommendations