Abstract
Commercial poultry feed required for proper growth of birds and egg production contains essential nutrients with maize as key component. Inadequately dried maize is prone to aflatoxin contamination and therefore when used in feed formulation for poultry may compromise the safety of the feeds and poultry products. This study investigated the levels of aflatoxins in feed ingredients, feed and poultry products sampled from Eastern and Greater -Accra regions of Ghana. The aflatoxin levels of B1, B2, G1, and G2 were determined using a High-Performance Liquid Chromatography (HPLC) methodology. Main feed ingredients used were fishmeal, cotton seed cake, soya meal, rice, wheat and maize bran as well as maize grains. There was correlation between the level of aflatoxins and moisture content in poultry feed ingredients. All the poultry feeds (100 %) analysed showed the presence of aflatoxins with total aflatoxins recorded ranging from 5.32 to 29.88 μg/kg. Maize samples of the poultry feeds, from all two regions, revealed maize to be a major contributor to the overall total aflatoxin contents found in the feed. Five (5) out of ten (10) communities investigated in the two (2) regions where the poultry feeds were examined recorded total aflatoxin levels in maize above the Ghana Standard Authority (GSA) specification of 20 μg/kg. Aflatoxins G1 and G2 were not detected in all samples of chicken meat and eggs. Total aflatoxin levels recorded for all chicken meat and eggs were below GSA specification of 5 μg/kg; implying that these products were safe for consumption.
Keywords: Aflatoxins, Poultry feed, Poultry product, Poultry production
1. Introduction
Agriculture is one of the most important sectors in the world for ensuring food safety and economic progress. Poultry production in Ghana is a major contributing sector to agriculture and adds about 14 % to the country's Gross Domestic Product (GDP) [1,2]. Ghana's commercial poultry industry business employs around 2.5 million people and contributes approximately 34 % of domestic meat output [2]. In addition, the commercial poultry industry serves as a source of income, nutrition, and food security for many individuals in Ghana. Poultry products (chicken meat and eggs) are viewed as a more commonly available and less expensive form of animal protein in Ghana with eggs being the most usually consumed and readily available. FAOSTAT [3], reported that egg consumption per capita in Ghana reached 1.07 kg in 2020 and this accounted for 1.90 % increase over the previous year. Also, the per capita consumption of chicken meat in Ghana as at 2021 was 400,000 MT and was predicted to reach 460,000 MT in 2022, which is a 15 % increase over the 2021 estimates of 400,000 MT [1].
Poultry feed is food given to poultry birds including chicken. Poultry feed accounts for almost 70 % of the overall animal feed produced in Ghana [3]. Bukar and Saeed [4] emphasized the need for poultry feed to be prepared in such a way that it will contain essential and safe nutrients for proper growth of poultry birds. This is because the ingestion of any unsafe food material could not only affect the health of the bird, but would also find its way through the food chain into foods consumed by human beings [5]. Agricultural products including maize, rice, wheat, cotton seeds, soya bean and their by-products (maize bran, wheat bran and soya meal) are the ingredients used in preparing poultry feed, with maize as the key ingredient [6]. Approximately, 30 % of all maize produced in Ghana is used by the poultry industry [3]. When these ingredients are not adequately dried, they become susceptible to aflatoxin contamination [7,8].
Aflatoxins are a class of natural fungal toxins that produce toxic secondary metabolites [9]. They are a major source of concern in tropical and subtropical regions due to their adverse effects on food and feed ingredients because they affect animal and human health due to their carcinogenic nature. Recent study by Darwish et al. [10], reported that consuming small doses of aflatoxins over a long period or consuming high doses over a short period can result in chronic effect such as cancer. Ingestion of aflatoxins can affect animals either in a group or individual and may destroy organs such as the liver and kidney. The presence of Asperigillus flavus, Asperigillus nomius and Asperigillus parasitus in food causes aflatoxin contamination [11,12]. These microorganisms usually contaminate the food product and synthesize the toxins as metabolites in the presence of high content of carbohydrates and low levels of protein [12]. Aflatoxins production and contamination of agricultural products mostly occurs on the farm in the presence of high temperature, high relative humidity, high moisture content, and injury of products before or after harvesting [8]. Aflatoxins B1, B2, G1 and G2 are of great significance to food safety and security because these four (4) types are usually found in food and feed [13]. Aflatoxins in poultry feeds are therefore of major global concern. Previous studies, have all explained how aflatoxins in poultry adversely affect poultry performance; reducing egg production, low growth rate and illness in birds [6,14,15]. All these may lead to huge economic losses in poultry production. Also [16], emphasized that poultry feeds which are contaminated with aflatoxins may contain low nutritional composition. A review by Atitsogbey et al. [17], reported that there is a rising concern about the safety, quality and health risk linked to agricultural products in Ghanaian markets.
Previous studies have reported the presence of aflatoxins B1, B2, G1, and G2 in poultry feed ingredients, feed and poultry products [[18], [19], [20]]. Nakavuma et al. [20] evaluated the knowledge of mycotoxins and the incidence of aflatoxins in chicken diets and feed components in various locations of Uganda, they reported a total aflatoxin concentration ranging from 6.79 to 412.59 g/kg. More recently [21] investigated aflatoxin levels in maize sampled from Volta region in Ghana and reported total aflatoxins level ranging from 1.89 to 444.01 μg/kg. Also [22], reported total aflatoxins level of 1.0–4.61 μg/kg for wheat bran. Pandey and Chauhan [18] reported highest aflatoxin B1 levels of 18.0 μg/kg in chicken meat and 1.4 μg/kg (eggs). In addition [19], investigated accumulation of aflatoxin B1 in hens, aged between 15 and 67 weeks, and reported aflatoxin B1 levels between 3.5 and 18.2 μg/kg in eggs. In Ghana, majority of previous studies on aflatoxins have focused on human foods with little information existing for animal feeds. A search through literature revealed that almost all the existing studies on aflatoxins contamination in Ghana have considered only the animal feed and excluded poultry products (egg and chicken meat) which serve as a source of protein for humans. It has therefore become imperative to investigate the possibility of transfer of aflatoxins from feed to poultry products along the poultry value chain. This study therefore sought to determine the levels of aflatoxins in poultry feed ingredients, feed and poultry products (chicken meat and egg) sampled from commercial poultry industries across Greater Accra and Eastern regions of Ghana.
2. Methodology
2.1. Solvents, reagents and materials
Methanol and acetonitrile (HPLC grade) were sourced from BDH Chemicals (Caton, United Kingdom), sodium chloride from BDH (Leuven, Belgium), aflatoxin standard from (R. Biopharm Rhone Ltd, Glasgow, Scotland) and Whatman No. 1 filter paper sourced from (Kent, United Kingdom).
2.2. Source of samples
A total of sixty (60) samples were used for this study. These samples included ten (10) each of maize, soya meal, wheat bran, poultry feed, chicken meat and eggs collected from five (5) poultry farmers each in Greater Accra and Eastern regions of Ghana. In Greater Accra region, samples were collected from the following communities, Adenta, Tema, Accra, Dansoman and Pokuase whilst in Eastern region samples were collected from Aburi, Koforidua, Bunso, Kade and Asamankese communities where commercial poultry farming is predominant. Greater Accra has a land area of 3245 km2, and is located between latitude 5°- 33′ North and longitude 0°- 12′ West with a population of 5,455,692 whilst Eastern region occupies an area of 19,323 km2, lies between latitude 6°- 30′ North and longitude 0°- 30′ West with a population of 2,925,653 [22]. Fig. 1 shows the two regions in Ghana where samples were obtained.
Fig. 1.
Map of Ghana showing regions where samples were collected for the study.
2.2.1. Sampling of feed ingredients, feeds and poultry products
Both feed ingredients and processed feeds were sampled from 50 kg bags. Sub-samples (400 g) from the 50 kg feed ingredients and feeds were sampled from three (3) different points (top, middle and bottom) into cleaned zip-lock bags, mixed thoroughly for homogeneity and kept in freezer until laboratory analysis. Eggs (mixture of yolk and albumin, without the shell) and chicken meat (thigh) from slaughtered and dressed birds (layer hens) were sampled after four (4) weeks from poultry birds fed with the same feed prepared from sampled feed ingredients. All samples were stored in zip-lock bags, labelled and transported in cold chain to CSIR-Food Research Institute Toxicology Laboratory for analysis.
2.2.2. Preparation of poultry feed
Approximately 650 kg whole maize grains (raw ingredient) were first cleaned by sieving with Grains Sieving Vibrator Machine to remove foreign materials such as stones. Sieved maize grains, 600 kg were milled to 0.45 mm particle size with Hammer Mill (Leabon, China) at 3000 rotation per minute (rpm) for 60 min. The milled maize, 550 kg was weighed into a Vertical Mixer (Leabon, China). The remaining feed ingredients were weighed individually. Based on Feed Standard Composition Figures used by poultry farmers in Ghana, Table 1 shows the weighted composition of feed ingredients. The resultant was mixed for approximately one (1) hour at a speed of 1450 rpm using a Vertical mixer (Leabon, China). The mixture, processed poultry feed (1000 kg) was allowed to cool for 30 min and bagged into 50 kg cleaned polypropylene bags and stored in a warehouse at a temperature of about 25 °C. The poultry birds under investigation were fed with the prepared processed feed.
Table 1.
Poultry feed ingredients composition of feed used in this study.
| Feed Ingredients | Weight (kg) | % |
|---|---|---|
| Whole Maize | 550 | 55.0 |
| Soya meal | 215 | 21.5 |
| Wheat Bran | 100 | 10.0 |
| Dicalcium phosphate | 5 | 0.5 |
| Fish meal | 5 | 0.5 |
| Oyster shells | 90 | 9.0 |
| Layer concentrate | 30 | 3.0 |
| Vitamins & Minerals premix, and salt | 5 | 0.5 |
| Total | 1000 | 100 |
*Feed standard composition figures of poultry feed for layer birds are as follows.
Whole Maize 55–60 %.
Soya meal 20–25 %.
Wheat bran 10–15 %.
Others (fish meal, oyster shell, premix, toxin binders, etc) 5–10 %.
2.3. Moisture content analysis
Moisture content of feed ingredients (maize, soya meal and wheat bran) and processed poultry feeds were determined using air-oven method [23].
2.4. Aflatoxin analysis
The extraction protocol used for determination of aflatoxins B1, B2, G1 and G2 was by Stroka, and Anklam [24]. A test portion of 25 g sample was extracted with 200 mL methanol/water (80:20) solvent solution containing 5 g of sodium chloride. The sample extracts were filtered using Whatman No. 1 filter paper to prevent clogging of immune affinity column. Filtrate, 10 mL was diluted with 40 mL Millipore water. The diluted filtrate was swirled for 2 min and 60 mL phosphate buffer of pH 7.4 containing 0.2 g/L potassium chloride, 8 g/L sodium chloride, and 1.16 g/L anhydrous sodium dihydrogen phosphate was added for solid phase extraction. Resultant solution, 10 mL was passed through an immune affinity column (R-Biopharm Rhone Ltd. Glasgow, Scotland) containing antibodies specific for aflatoxin B1, B2, G1 and G2 at a rate of 1–2 drops/second. The column was washed thrice with 5 mL Millipore water. The extracted aflatoxins bound to the affinity column were eluted using 1 mL methanol at rate of 1–2 drops per second and elute was collected into a glass tube. The Aflatoxin level was quantified by reverse-phase high performance liquid chromatography (RP-HPLC) with post column derivatization (PCD) involving bromination. The PCD was achieved with pyrimidinum hydrobromide perbromide (PBPB) followed by fluorescence detection. HPLC system used for analyses was from Waters Associates (Milford, MA, USA) and included Waters 1525 Binary HPLC pump, Waters 2707 Autosampler, Waters Model 1500 Column Heater, Waters 2475 Multi λ Fluorescence Detector and Breeze 2 software. Separation of the aflatoxin was carried out on a Spherisorb S5 ODS-1 column of dimensions 25 × 4.6 mm packed with 5 μm particles (phase separation In., Norwalk, USA) maintained at 35 °C. The HPLC mobile-phase flow rate was 10 mL/min and post column bromine derivatization of Aflatoxin B1, B2, G1 and G2 was achieved by PBPB dissolved in 500 mL of demineralised water pumped at a flow rate of 1.0 mL/min using Elder precision metering pump (Elder laboratories Inc., Sam Carlos, USA). The excitation and emission wave length used were 360 nm and 440 nm respectively. The aflatoxins were identified by means of their retention times, and quantification was performed by comparing the peak areas of the samples to those of the standards prepared from pure aflatoxins standard solutions (obtained from R. Biopharm) under identified conditions.
2.5. Quality control of results
Samples were handled with caution to prevent contamination as a precaution to guarantee the accuracy of the results. The recovery of analytical method was 90.50, 76.56, 95.58 and 91.76 % for B1, B2, G1 and G2 respectively with linearity, R2 = 0.999. Limit of detection for aflatoxin B1, and B2 = 0.15 μg/kg and aflatoxin G1 and G2 = 0.13 μg/kg.
2.6. Data analysis
Standard deviations on mean values of triplicate samples were analysed using Statistical Package for Social Scientist (IBM SPSS, 2005) version 16. ANOVA, Duncan test was used to compare the means.
3. Results and discussion
3.1. Moisture content of feed ingredients and feeds
The moisture contents of inadequately dried feed ingredients, especially the maize component, is one of the major causes of aflatoxins found in poultry feeds [7,8]. The Ghana Standards Authority (GSA) has specified moisture content of ≤15 % for poultry feed ingredients and feeds. Moisture content recorded for feed ingredients; maize, soya meal and wheat bran collected from Greater Accra region ranged from 10.85 to 18.15 % (mean: 13.68 ± 2.65 %); 6.73–10.25 % (mean: 8.62 ± 1.18 %) and 5.11–10.98 % (mean: 8.63 ± 2.36) respectively. For Eastern region, the moisture contents for maize, soya meal and wheat bran were in the ranges 11.53–19.46 % (mean: 15.32 ± 2.64 %), 3.95 %–10.30 % (mean: 6.88 ± 2.40 %) and 4.82–12.94 % (mean: 9.14 ± 3.13 %), respectively. Maize is the main feed ingredient used for feed preparation in Ghana. The highest moisture content of 19.46 % was recorded for maize sampled from Aburi in Eastern region whilst the lowest of 10.85 % moisture content was obtained for maize samples from feed producers from Pokuase in Greater Accra Region and the difference was statistically significant at P ≤ 0.05 (ANOVA, Duncan test). The highest moisture content of 19.46 % obtained by maize sampled across the two regions in Ghana was far above the GSA specification of ≤15 % for feed ingredient. This makes the maize more susceptible to aflatoxin contamination. A previous study by Ref. [25] investigated aflatoxin content in poultry feed ingredient sampled in Cameroon and reported moisture content ranging from 11.70 to 17.70 % for maize which is similar to moisture content of 10.85–19.46 % recorded for maize in the present study. Soya meal samples gave moisture contents ranging from 3.95 to 10.30 % (mean: 8.62 ± 1.18 %) across Greater Accra and Eastern regions. These values are far lower than moisture content ranging from 11 to 15 % reported by Ref. [26] for soya meal. All the soya meal samples collected for this study recorded moisture contents that were equal or below the recommended GSA specification of ≤15 % for feed ingredient. The low moisture content recorded for soya meal samples in this study may be attributed to the fact that soya meal is a by-product of soya beans that have passed through several processes including heat treatment which would have resulted in removal of some moisture content before the final product (the soya meal) [27]. The moisture content for the wheat bran samples across Greater Accra and Eastern regions ranged from 4.82 to 12.94 % (mean: 8.89 ± 2.78 %) and were below the GSA specification of ≤15 %. Again, the low moisture content recorded for wheat bran could be linked to the fact that wheat bran is a by-product that has passed through several processes including heat treatment and therefore would have been properly dried at the time of use as a feed ingredient [27].
Poultry feed analysed from Greater Accra and Eastern regions of Ghana recorded moisture content ranging from 8.29 to 17.18 % (mean: 11.96 ± 3.36 %) and 6.59–13.54 % (mean: 10.47 ± 2.58 %) respectively. The highest moisture content of 17.18 % was obtained for feed sampled from Tema in Greater Accra region and this was far above GSA specification of ≤15 % moisture content for poultry feed [28]. Fig. 2, shows the comparison of mean moisture content of poultry ingredients and feeds analysed. With exception of maize sampled from Eastern region, all feed ingredients and feeds analysed obtained moisture contents below GSA specification of ≤15 % for feed ingredient and feed [28].
Fig. 2.
Mean moisture content of poultry feed ingredients and feeds collected from GR and ER. Key: GR- Greater Accra region, ER- Eastern region, Ghana Standard Authority limits of ≤15 %.
3.2. Aflatoxins in feed ingredients
There were variations in the aflatoxin levels estimated for poultry feed ingredients and feeds randomly collected from GR and ER of Ghana. This may be partly linked to diverse agro-ecological zones of the two (2) regions where the study was carried out. Aflatoxin levels determined for maize sampled from Greater Accra and Eastern regions are shown in Table 2. Type of aflatoxins detected in maize included B1, B2, G1 and G2. The levels of aflatoxin B1, B2, G1, G2 recorded for maize sampled from Greater Accra region were in the range, 1.66–19.39 0.76–2.05, ND – 0.75 and ND – 0.21 μg/kg, respectively. For Eastern region, the levels of aflatoxin B1, B2, G1, G2 obtained for maize ranged from 14.49 to 45.80, 0.65–8.68, ND – 0.58 and ND – 0.90 μg/kg, respectively. The highest total aflatoxin content of 54.30 μg/kg was recorded for maize sampled from Aburi and was far above the GSA permissible limit of 20 μg/kg. There was a correlation between the moisture content and aflatoxin levels in maize analysed. For example, maize sampled from Aburi in Eastern region obtained the highest moisture content 19.46 % and also the highest aflatoxin content of 54.30 μg/kg. Previous study has reported that high moisture content is one of the major causes of aflatoxins production in feed ingredients and feeds [7]. The total aflatoxin levels recorded for all maize samples were in the range of 2.53–54.30 μg/kg (Table 2). A study by Ref. [25] investigated aflatoxins in commercial poultry feed in Cameroon and reported aflatoxins levels ranging from 2 to 42 μg/kg for maize, which is similar to total aflatoxin levels of 2.5–54.26 μg/kg recorded for maize in the present study. Also [21], reported total aflatoxins levels of 1.89 − 444.01 μg/kg for maize sampled from Volta region, Ghana. In addition [29], investigated aflatoxin prevalence in maize sampled from different ecological zones in Ghana and reported total aflatoxins ranging from 1 to 341 μg/kg for maize. All the maize samples analysed in the present study recorded 100 % occurrence of aflatoxins with 60 % obtaining total aflatoxin levels beyond GSA permissible limit of 20 μg/kg.
Table 2.
Levels of Aflatoxins in Maize sampled from GR and ER.
| Region | Community | Aflatoxins | Level | (μg/kg) | ||
|---|---|---|---|---|---|---|
| B1 | B2 | G1 | G2 | Total AFs | ||
| Adenta | 15.97 ± 0.23c | 1.03 ± 0.33c | 0.55 ± 0.08a | 0.18 ± 0.03a | 17.73 ± 0.08c | |
| Tema | 19.33 ± 0.06a | 2.03 ± 0.02a | 0.18 ± 0.01b | ND | 21.54 ± 0.17a | |
| GR | Accra | 1.62 ± 0.04d | 0.75 ± 0.01d | 0.16 ± 0.00b | ND | 2.53 ± 0.06e |
| Dansoman | 5.77 ± 0.07d | 0.96 ± 0.04d | 0.74 ± 0.01a | 0.16 ± 0.01a | 7.63 ± 0.01d | |
| Pokuase | 18.13 ± 0.28b | 1.77 ± 0.01b | ND | ND | 20.90 ± 0.13b | |
| Aburi | 45.70 ± 0.10a | 8.56 ± 0.12a | ND | ND | 54.26 ± 0.04a | |
| Koforidua | 35.80 ± 0.05b | 6.87 ± 0.17b | ND | ND | 42.67 ± 0.40b | |
| ER | Bunso | 21.32 ± 0.11c | 0.98 ± 0.02d | 0.52 ± 0.06a | ND | 22.82 ± 0.02c |
| Kade | 14.19 ± 0.30e | 0.64 ± 0.01d | 0.17 ± 0.02b | 0.86 ± 0.04a | 15.86 ± 0.14e | |
| Asamankese | 18.15 ± 0.14d | 2.17 ± 0.21c | ND | 0.14 ± 0.01b | 21.07 ± 0.25d |
Values are presented as means ± standard deviations. Values with different superscripts in the same column are significantly different (p < 0.05). Limit of Detection for aflatoxins: B1 & B2 is 0.15 μg/kg and G1 & G2 is 0.13 μg/kg. Key: GR- Greater Accra region; ER- Eastern region; ND-not detected.
Aflatoxin levels recorded for soya meal and wheat bran across Greater Accra and Eastern regions of Ghana are shown in Table 3, Table 4, respectively. Aflatoxin B1, B2, G1, and G2 levels obtained by soya meal across the two regions were in the range ND – 2.46 μg/kg, ND – 1.19 μg/kg, ND – 0.17 μg/kg and ND – 0.45 μg/kg respectively. Total aflatoxins recorded for all soya meal sampled across the two (2) regions were in the range ND – 3.27 μg/kg which is far less than the GSA specification of 20 μg/kg total aflatoxins for feed ingredient. Again, correlation was observed between moisture content and aflatoxin levels as all soya meal samples recorded low mean moisture content of ≤10 % across the two (2) regions (Fig. 1) and a responding low total aflatoxin level. The highest total aflatoxins level of 3.21 μg/kg obtained by soya meal was within the range of 3.25–20.32 μg/kg total aflatoxins reported by Ref. [22] when they investigated the occurrence of aflatoxins in poultry feed and feed ingredients collected from North-Western Iran. For wheat bran, aflatoxins B1, B2, G1, and G2 levels obtained were in the range ND – 4.17, ND – 1.13, ND – 0.17 μg/kg and ND, respectively. The low level of aflatoxins obtained by wheat bran could be related to low moisture content of ≤10 % recorded for wheat bran sampled across Greater Accra and Eastern regions. Total aflatoxins obtained by wheat bran was in the range ND – 5.27 μg/kg and the difference between the lowest and highest total aflatoxins was statistically significant at p ≤ 0.05 (ANOVA, Duncan test). The highest total aflatoxin level of 5.27 μg/kg recorded for wheat bran was far below the GSA specification of 20 μg/kg total aflatoxin for feed ingredient. Total aflatoxins of ND – 5.27 μg/kg recorded for wheat bran in the present study was slightly lower compared to total aflatoxins between 0.81 and 6.43 μg/kg reported by Ref. [30] for wheat bran collected from some selected areas in Ethiopia. The differences in total aflatoxins reported for wheat bran in present study and that reported by Ref. [30] may be as a result of the differences in geographical locations where samples were collected.
Table 3.
Levels of Aflatoxins in Soya meal sampled from GR and ER.
| Region | Community | Aflatoxins | Level | (μg/kg) | ||
|---|---|---|---|---|---|---|
| B1 | B2 | G1 | G2 | Total AFs | ||
| Adenta | 0.17 ± 0.01d | ND | ND | ND | 0.17 ± 0.01d | |
| Tema | 0.50 ± 0.02c | 0.77 ± 0.02a | ND | ND | 1.27 ± 0.01c | |
| GR | Accra | 2.24 ± 0.22a | 0.82 ± 0.01a | ND | 0.15 ± 0.01a | 3.21 ± 0.06a |
| Dansoman | 1.75 ± 0.05b | ND | ND | ND | 1.75 ± 0.05b | |
| Pokuase | 0.96 ± 0.01c | 0.30 ± 0.01b | 0.15 ± 0.02a | ND | 1.41 ± 0.05c | |
| Aburi | 1.01 ± 0.04b | ND | ND | ND | 1.01 ± 0.04b | |
| Koforidua | 1.18 ± 0.07b | 1.10 ± 0.09a | ND | 0.42 ± 0.03a | 2.70 ± 0.08a | |
| ER | Bunso | ND | ND | ND | ND | ND |
| Kade | 0.83 ± 0.02c | 0.15 ± 0.00c | ND | ND | 0.98 ± 0.07b | |
| Asamankese | 2.15 ± 0.23a | 0.63 ± 0.02b | ND | ND | 2.78 ± 0.13a |
Values are presented as means ± standard deviations. Values with different superscripts in the same column are significantly different (p < 0.05). Limit of Detection for aflatoxins: B1 & B2 is 0.15 μg/kg and G1 & G2 is 0.13 μg/kg. Key: GR- Greater Accra region; ER- Eastern region; ND-not detected.
Table 4.
Levels of Aflatoxins in Wheat bran sampled from GR and ER.
| Region | Community | Aflatoxins | Level | (μg/kg) | ||
|---|---|---|---|---|---|---|
| B1 | B2 | G1 | G2 | Total AFs | ||
| Adenta | ND | ND | ND | ND | ND | |
| Tema | ND | ND | ND | ND | ND | |
| GR | Accra | 1.30 ± 0.12b | 0.19 ± 0.02a | ND | ND | 1.49 ± 0.05b |
| Dansoman | 0.62 ± 0.01c | ND | 0.15 ± 0.02a | ND | 0.77 ± 0.01c | |
| Pokuase | 3.37 ± 0.07a | ND | ND | ND | 3.37 ± 0.07a | |
| Aburi | 2.19 ± 0.03b | 0.15 ± 0.00b | ND | ND | 2.34 ± 0.09b | |
| Koforidua | ND | ND | ND | ND | ND | |
| ER | Bunso | 4.02 ± 0.15a | 1.03 ± 0.10a | ND | ND | 5.05 ± 0.22a |
| Kade | 0.79 ± 0.22c | 0.15 ± 0.00b | ND | ND | 0.94 ± 0.02c | |
| Asamankese | 0.36 ± 0.01d | ND | ND | ND | 0.36 ± 0.01d |
Values are presented as means ± standard deviations. Values with different superscripts in the same column are significantly different (p < 0.05). Limit of Detection for aflatoxins: B1 & B2 is 0.15 μg/kg and G1 & G2 is 0.13 μg/kg. Key: GR- Greater Accra region; ER- Eastern region; ND-not detected.
3.3. Aflatoxins in poultry feed and product
Aflatoxin levels in poultry feed sampled from Ghana's Eastern and Greater Accra regions are displayed in Table 5. There were variations in levels of aflatoxins B1, B2, G1, and G2 obtained by poultry feeds collected from Greater Accra and Eastern regions of Ghana. Aflatoxins B1, B2, G1, and G2 levels in feeds were between 5.32 and 26.11, ND – 3.64, ND – 0.35 and ND – 0.21 μg/kg, respectively. Aflatoxin was detected in 100 % of the poultry feeds examined, with a total aflatoxins of 5.32–29.88 μg/kg detected. The presence of aflatoxins in 100 % of all poultry feeds analysed could results in aflatoxin transfer into poultry products which may lead to consumer health risk. There was a significant difference (p ≤ 0.05) between the lowest total aflatoxin of 5.32 μg/kg and the highest total aflatoxin (29.88 μg/kg) recorded for poultry feeds. Poultry feed sampled from Aburi in Eastern region recorded the highest total aflatoxin level of 29.88 μg/kg and the lowest total aflatoxin level of 5.28 μg/kg was obtained by feed from Dansoman in Greater Accra region. Five (5) out of ten (10) communities where feeds were collected recorded a total aflatoxin levels above GSA specification of 20 μg/kg. A previous study by Ref. [31], investigating for aflatoxins in poultry feed collected from Guyana, reported total aflatoxin level of 3.81–27.38 μg/kg and these values are similar to those obtained in this study. Also [25], investigated aflatoxins in poultry feed sampled from Cameroon and reported aflatoxin levels between 2 and 23 μg/kg. Nakavuma et al. [20], investigated the awareness of mycotoxins and occurrence of aflatoxins in poultry feeds and feed ingredients in selected regions of Uganda and reported total aflatoxins 6.79–412.59 μg/kg. The highest total aflatoxin content of 412.59 μg/kg recorded for feed samples analysed in Uganda was far above the highest total aflatoxin content of 29.88 μg/kg obtained by feed samples in the current study and this may be related to the differences in geographical locations where feed samples were collected. A previous study by Ref. [32], reported total aflatoxins ranging between 0.02 and 22.0 μg/kg for poultry feed when they investigated aflatoxins in poultry feed collected from commercial poultry farms in Ghana. The highest total aflatoxin level of 22.0 μg/kg reported by Ref. [32] is slightly lower compared to total aflatoxin level of 23.88 μg/kg obtained by poultry feed in the present study. Also [33], reported total aflatoxins level of 11.83–88.37 μg/kg for poultry feed sampled from commercial poultry farms in Ghana which is far above the total aflatoxin levels of 5.28–29.72 μg/kg recorded for poultry feed in the present study. Previous studies have reported that aflatoxins in poultry diets can cause carcinogenesis, anemia, hemorrhage, liver and kidney abnormalities, impaired immunity, and may induce mortality among poultry birds [[34], [35], [36]].
Table 5.
Levels of Aflatoxins in Poultry Feed collected from GR and ER.
| Region | Community | Aflatoxins | Level | (μg/kg) | |||
|---|---|---|---|---|---|---|---|
| B1 | B2 | G1 | G2 | Total AFs | |||
| Adenta | 12.25 ± 0.49c | 0.58 ± 0.10c | ND | ND | 12.83 ± 0.37c | ||
| Tema | 8.03 ± 0.22d | 0.40 ± 0.00d | ND | ND | 8.43 ± 0,19d | ||
| GR | Accra | 15.01 ± 0.16b | 0.96 ± 0.12b | ND | ND | 15.97 ± 0.23b | |
| Dansoman | 5.28 ± 0.04e | ND | ND | ND | 5.28 ± 0.04e | ||
| Pokuase | 22.09 ± 0.17a | 1.00 ± 0.02a | ND | ND | 23.09 ± 0.31a | ||
| Aburi | 26.04 ± 0.07a | 3.50 ± 0.14a | ND | 0.18 ± 0.03a | 29.72 ± 0.16a | ||
| Koforidua | 21.76 ± 0.06b | 0.17 ± 0.02d | ND | ND | 21.93 ± 0.15c | ||
| ER | Bunso | 19.73 ± 0.19c | 2.10 ± 0.01b | 0.19 ± 0.02a | ND | 22.02 ± 0.10b | |
| Kade | 8.35 ± 0.03d | 1.33 ± 0.03c | ND | ND | 9.68 ± 0.02d | ||
| Asamankese | 19.91 ± 0.11c | 1.17 ± 0.01c | 0.34 ± 0.01a | 0.15 ± 0.01a | 21.57 ± 0.08c | ||
Values are presented as means ± standard deviations. Values with different superscripts in the same column are significantly different (p < 0.05). Limit of Detection of aflatoxins: B1 & B2 is 0.15 μg/kg and G1 & G2 is 0.13 μg/kg. Key: GR- Greater Accra region; ER- Eastern region; ND-not detected.
Table 6 shows the level of aflatoxins found in chicken meat samples. Aflatoxins determined in chicken meat include B1, B2, G1 and G2. All chicken meat collected from both Greater Accra and Eastern regions of Ghana did not have aflatoxins G1 and G2. The level of aflatoxin B1 and B2 recorded for chicken meat was in the range 0–0.18 μg/kg and 0–0.05 respectively. The presence of aflatoxins in the chicken meat samples is an indication of a possible transfer of aflatoxins from feed to poultry birds. Total aflatoxins obtained by chicken meat sampled from the two regions were between 0 and 0.24 μg/kg. The highest total aflatoxin level of 0.24 μg/kg found in chicken meat samples from Aburi in Eastern region was far lower compared to GSA specification of 5 μg/kg total aflatoxins in food. Previous studies have reported that continuous exposure (via dietary source) to low concentrations of aflatoxins can cause cancer in animal and humans [37,38]. A previous study by Ref. [39] investigated aflatoxins in poultry feed and product sampled in Nigeria and reported that 48 % of the chicken meat samples had aflatoxins B1 ranging from 0.02 to 0.07 μg/kg. However, their highest value of 0.07 μg/kg for aflatoxin B1 was far below what was found in the present study. The differences in aflatoxin B1 levels recorded in present study and that reported by Ref. [38] could be related to differences in geographical locations of the two studies. Also [40], reported total aflatoxins level ranging from 0.03 to 0.10 μg/kg for chicken meat after feeding birds with high level of aflatoxins (101–150 μg/kg) contaminated feed for twenty-one (21) days. This implies that when birds were fed with contaminated feeds, it leads to transfer of aflatoxins from feed to chicken meat. Globally, chicken meat is consumed by many. However, consuming chicken meat contaminated with aflatoxins can cause immune suppression, liver cancer and stunted growth in children [41,42].
Table 6.
Levels of Aflatoxins in Chicken meat collected from GR and ER.
| Region | Community | Aflatoxins | Level | (μg/kg) | ||
|---|---|---|---|---|---|---|
| B1 | B2 | G1 | G2 | Total AFs | ||
| Adenta | ND | ND | ND | ND | ND | |
| Tema | ND | ND | ND | ND | ND | |
| GR | Accra | 0.06 ± 0.01b | ND | ND | ND | 0.06 ± 0.01b |
| Dansoman | ND | ND | ND | ND | ND | |
| Pokuase | 0.15 ± 0.03a | ND | ND | ND | 0.15 ± 0.03a | |
| Aburi | 0.17 ± 0.01a | 0.05 ± 0.00a | ND | ND | 0.22 ± 0.02a | |
| Koforidua | 0.10 ± 0.00b | ND | ND | ND | 0.10 ± 0.00b | |
| ER | Bunso | 0.11 ± 0.00b | ND | ND | ND | 0.11 ± 0.00b |
| Kade | ND | ND | ND | ND | ND | |
| Asamankese | 0.09 ± 0.02c | ND | ND | ND | 0.09 ± 0.02c |
Values are presented as means ± standard deviations. Values with different superscripts in the same column are significantly different (p < 0.05). Limit of Detection of aflatoxins: B1 & B2 is 0.05 μg/kg and G1 & G2 is 0.05 μg/kg. Key: GR- Greater Accra region; ER- Eastern region; ND- Not detected.
The levels of aflatoxins recorded for eggs collected from Greater Accra and Eastern regions of Ghana has been reported in Table 7. Types of aflatoxins determined in eggs include aflatoxins B1, B2, G1, and G2. Aflatoxins G1 and G2 could not be detected in all eggs analysed. However, aflatoxins B1 and B2 present in egg samples ranged from ND – 0.14 and ND – 0.08 μg/kg, respectively. The total aflatoxin levels recorded for eggs analysed was in the range ND – 0.20 μg/kg. The highest total aflatoxin level of 0.20 μg/kg obtained by eggs was far lower compared to GSA specification of 5 μg/kg total aflatoxins in food. A study by Pourelmi et al. [43], reported total aflatoxins ranging from 0.050 to 0.083 μg/kg for eggs sampled from seven (7) different zones in Iran, which are slightly lower to those found in eggs in the present study. Previous study by Amirkhizi et al. [44], investigated aflatoxins in eggs sampled from poultry farms in Iran and reported aflatoxin B1 levels ranging from 0.30 to 16.36 μg/kg in eggs and these are higher than those recorded for eggs in this study. Aflatoxins can be transferred through dietary exposure from poultry feed to laying hen, then to eggs and finally to human diet which can have negative effects on human body [45,46]. A review by Ref. [47] reported that the presence of aflatoxins can lead to reduced egg production, poor egg quality and also can cause death in laying hens.
Table 7.
Levels of Aflatoxins in Eggs collected from GR and ER.
| Region | Community | Aflatoxins | Level | (μg/kg) | ||
|---|---|---|---|---|---|---|
| B1 | B2 | G1 | G2 | Total AFs | ||
| Adenta | 0.05 ± 0.00b | ND | ND | ND | 0.05 ± 0.00b | |
| Tema | ND | ND | ND | ND | ND | |
| GR | Accra | ND | ND | ND | ND | ND |
| Dansoman | ND | ND | ND | ND | ND | |
| Pokuase | 0.12 ± 0.02a | ND | ND | ND | 0.12 ± 0.02a | |
| Aburi | 0.12 ± 0.01a | 0.07 ± 0.01b | ND | ND | 0.19 ± 0.01a | |
| Koforidua | 0.07 ± 0.00b | ND | ND | ND | 0.07 ± 0.00c | |
| ER | Bunso | 0.13 ± 0.01a | ND | ND | ND | 0.13 ± 0.01b |
| Kade | ND | ND | ND | ND | ND | |
| Asamankese | 0.09 ± 0.02b | ND | ND | ND | 0.09 ± 0.02c |
Values are presented as means ± standard deviations. Values with different superscripts in the same column are significantly different (p < 0.05). Limit of Detection of aflatoxins: B1 & B2 is 0.05 μg/kg and G1 & G2 is 0.05 μg/kg. Key: GR- Greater Accra region; ER- Eastern region; ND- Not detected.
Poultry farmers, feed producers, and feed vendors must be educated on aflatoxin awareness, occurrence, promoting factors, and effects on animals and humans to reduce the presence of aflatoxins and their effects on poultry production, bird health, and human health. In addition, educational tools such as brochures, leaflets, stickers and posters on aflatoxins’ awareness can be made available to poultry farmers, feed producers and feed vendors. Also, it is recommended that, poultry farmers must analyse their feeds for aflatoxin content in order to prevent birds from eating aflatoxin-contaminated diet.
4. Conclusion
In most nations, particularly in Sub-Saharan Africa, aflatoxin contamination of poultry feed has been a serious concern. The current study reveals the prevalence of aflatoxin in feed constituent (especially in maize) from the Eastern and Greater Accra regions of Ghana. The highest total aflatoxin content of 54.30 μg/kg was recorded for maize collected from Aburi in the Eastern region and was far above the GSA permissible limit of 20 μg/kg. However, aflatoxins G1 and G2 were not detected in the chicken meat and eggs but in cases where they were detected, they were below Ghana Standard Authority specifications of 5 μg/kg. Nevertheless, this study found a correlation between aflatoxin levels in the feed ingredients and feed moisture content. It is therefore worth knowing that poultry farmers and feed producers will be sensitized on drying procedures for feed ingredients especially maize to reduce the effect in the poultry industry.
Data availability statement
Data will be made available on request.
CRediT authorship contribution statement
Benedicta Nsiah: Writing – original draft, Methodology, Formal analysis, Data curation, Conceptualization. Hayford Ofori: Writing – review & editing, Writing – original draft, Supervision, Methodology, Formal analysis, Conceptualization. Charlotte Oduro-Yeboah: Writing – review & editing, Supervision, Conceptualization. Emmanuel Kyereh: Writing – review & editing, Supervision, Conceptualization. Paa-Nii T. Johnson: Writing – review & editing, Supervision, Conceptualization.
Declaration of competing interest
The auth\ors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
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Data Availability Statement
Data will be made available on request.