Key findings:

The study identified Aspergillus flavus and Aspergillus fumigatus as dominant aflatoxigenic moulds in pepper-treated Kulikuli. Proximate analysis showed higher protein content in both spiced and non-spiced samples. Moisture content was slightly higher in spiced samples. The shape of the samples did not affect aflatoxin levels. Protein was the major nutrient in both types of Kulikuli.

What is known and what is new?

This study contributes new insights into fungal contamination and nutritional composition of pepper-treated Kulikuli. While the presence of aflatoxigenic moulds like Aspergillus flavus in Kulikuli is known, this research specifically identifies A. flavus and A. fumigatus as dominant strains. The finding that protein is the major nutrient in both spiced and non-spiced samples adds to the understanding of Kulikuli's nutritional profile. Additionally, the study's observation that sample shape does not influence aflatoxin levels provides valuable information for food safety practices in Kulikuli production.

What is the implication, and what should change now?

The implication of this study is significant for the food industry, particularly in the production of Kulikuli. The identification of dominant aflatoxigenic moulds underscores the importance of stringent quality control measures to prevent aflatoxin contamination. Additionally, the finding that protein is the major nutrient in Kulikuli highlights its nutritional value, which can be leveraged for marketing and consumer education. Moving forward, producers should prioritize measures to reduce fungal contamination, such as implementing better storage and processing practices, to ensure the safety and quality of Kulikuli products.

The standard of staples and their products, which include snacks and street foods that are consumed by humans is essential when we consider the universal endeavor towards increasing food safety. This is mostly in the environment where climatic, poor post-harvest processing and storage conditions results in microbial contamination of foods [1]. Snacks are quick, portable, and satisfying small portion of food generally eaten between meals. Snacks are sold or served in a variety of forms as small chops at parties, schools and even offices, as well as domestic refreshment at home. Excessive consumption of snacks by almost everyone especially by growing children makes it compulsory for it to be highly nutritious so as to help in countering nutritional deficiencies and malnutrition through nutritional programs. In Nigeria, and across other African countries, the utmost groups of snacks are prepared from staples such as cassava, groundnut, maize and wheat [2]. Groundnut (Arachis hypogeal) is a specie in the legume family Fabacae which is native to South America, Mexico and Central America. It is a plant that grows to 30cm to 50 cm (1 to 1½ ft) tall annually.

 It is grown throughout the tropical and warm temperature regions of the World [3]. Groundnut (Arachis hypogaea L.) is a nutrient rich agricultural produce with high fat and protein content which makes it very high in energy. The nut has very high content of fibre and oil [4]. They are good source of protein and vitamin E and its products are considered by all age groups as Ready-To-Eat (RTE) foods. They also serve as an important component in feed formulation in the poultry [5]. In Nigeria, groundnut products are majorly produced and processed in the northern part of the country. Some groundnut product derivatives include peanut butter (a paste made by milling roasted groundnut and used as spreads in many common diets), Kulikuli (fried remnant derived after groundnut oil extraction), Groundnuts are snacks that are often hawked in rural areas of Nigeria in different forms, they are available in raw, boiled (epa sise, daffafiyar gyada), caked (kulikuli), roasted (epa yiyan, marao marao, tupus), and balls(donkwa, tanfiri). Groundnut flour is also derived by grinding groundnut cakes which is used to make soups or stews, sauces, confectioneries and bakery products. “Yaji” is a groundnut flour that has been mixed with different bits of spices like alligator pepper, ginger and salt to taste [4]. Yaji act as seasonings in some food products such as Jollof rice, Fried yam, and Suya - a Nigeria meat delicacy [6]. Groundnut is a leguminous crop an ingredient of choice with other cereals (corn, sorghum and millets) in the production of snacks and weaning foods due to the protein and omega-6 fatty acids present [7].

To prepare this indigenous snack (Kulikuli) peanuts are firstly roasted and then, grounded into a paste called “Labu”.This traditional Hausa snack is normally sold on roadside stands or markets, but it can also be found in a few packaged brands sold in Nigerian grocery stores or online. Kuli-kuli is a popular food item with long history of consumption in the diet of the low-resource classes of the population in West Africa [8]. Information on prevalence of mycotoxin and aflatoxin in particular are limited to the study areas. However, many people are concerned about the way it is handled after processing before it is sold to consumers.Information on the prevalence of mycotoxin and Aflatoxin in particular are limited in the study area, this study will provide reliable data on the fungal diversity of the samples as well as a novel information on the aflatoxin contents in Groundnut cake products in the sample areas. Due to the importance of these groundnut cake in daily living, this research work sought to evaluate the fungal species associated with vended groundnut cake (kulikuli), obtain information concerning the level of aflatoxin present in the product as an indication of what consumers might be exposed to and also to determine the nutritional and mineral composition of the samples studied. The main objective of the study is to determine fungal diversity, evaluate aflatoxin contamination levels in groundnut cake produced and processed in selected markets in Ibadan, Oyo state.

Sample collection Procedure

A total of one hundred and twenty (120) samples of both spiced (60) and non-spiced (60) kulikuli were purchased randomly from retail sales points in three different markets in Ibadan. Two kilograms each of the samples were purchased at the markets. The locations covered were within three geopolitical zones in Ibadan namely North East (NE), South West (SW) and North Central (NC) which are the major dumping site of these products. All collected samples was labelled and placed in a well insulated plastic box containing ice flakes and it was immediately transported to the laboratory and subjected to mycological and mycotoxin analysis.

Isolation and identification of fungi present in the groundnut samples

Potato Dextrose Agar plates was aseptically prepared using standard methods. Streptomycin sulphate (0.05mg/L) was added to the agar after sterilization to prevent bacterial growth [9]. Ten grams each of crushed groundnut cake samples (Kulikuli) was weighed into 90ml sterile distilled water and agitated using a vortex mixer. Using the pour plate method, 1ml of resulting mixture was inoculated into the cooled Potato dextrose agar (PDA) plates in triplicates and was incubated at room temperature (30 ± 2℃) for 5-7 days. Fungal growths were sub-cultured on fresh plates of PDA to obtain pure culture. Each fungal isolates were placed on a microscopic slide with few drops of 0.1% Lactophenol cotton blue and observed under the microscope. Cultural features were observed and characterization was done.

 Determination of Aflatoxin from Kulikuli samples

The method of Association of Analytical chemist (2006) was followed for purification of Aflatoxins from collected samples. The samples were milled (in triplicates of 5g samples each) and was put in different 250mL sterile ready-to use covered plastic containers and 25ml aliquot of 70% (v/v) methanol was introduced into the oily samples. The mixture was shaken for 5 minutes and the liquid portion was filtered using 24cm Whatman filter paper already containing 20g of sodium sulphate so as to absorb external contaminant in the solution in other to obtain pure extract. The separated lower aqueous layer phase was drained into another 250mLsterile plastic container. It was then extracted by adding 3-25mL dichloromethane to the aqueous phase and shaken vigorously for 30s. The phases separated and the lower dichloromethane layer was drained, collected and kept in a fume hood for 24 hours for it to evaporate. After 24 hours, 1mL dichloromethane was added to the dried extracts and placed in the fume hood for 6mins. The HTPLC plates was then placed into the solution for 20mins for it to develop. After, it was removed and allow to dry for 2mins. It was introduced into test wells of microtitre plates specific to the aflatoxin to be detected. It was placed in ultraviolet light box (CAMAG) to view the fluorescence of the extract under Ultraviolet light (UV) at 365nm. After the reactions, the colour changes in the wells and it was then placed into a TLC scanner to determine the quantity of aflatoxin present in the sample.

Detection of Aflatoxin Genes

DNA Extraction

Fungal Genomic DNA was extracted according to the protocol described in Quick-DNA mini-prep plus kit (Zymo research, Biolab, USA). Fungal species that was isolated from spiced and non-spiced Kulikuli samples were inoculated on fresh Potato Dextrose Agar (PDA) plates and incubated at 25℃ for 72hours. A small amount of each fungus was transferred into sterile mortar and crushed with pestle in phosphate buffer solution (this preliminary step was to lyse the cell wall). A solution made up of 95µl of water, 95µl of solid tissue buffer and 10µl of proteinase K was added and mixed thoroughly using a vortex mixer. It was then incubated at 55ºC for 2 hrs and centrifuged to remove insoluble debris. Then 200µl of supernatant was transferred to a tube and 400µl of genomic binding buffer was added to it. The mixture was transferred to a Zymo-spin™ IIC-XL column in a collection tube and centrifuged (≥12000×g) for 1 minute, the collection tube was discarded with the flow through. To the column in a new collection tube, 400µl DNA Pre-wash buffer was added and centrifuged and the collection tube was emptied. Seven hundred micro litres (700µl) of g-DNA wash buffer was added and centrifuged for 1 minute and the collection tube was discarded with the flow n tube was emptied. Two hundred micro litres (200µl) of g-DNA wash buffer was added through. The Zymo-spin™ IIC-XL column was transferred to a 1.5ml Eppendorf tube and 50µl of elution buffer was used to elute the genomic DNA and was stored at -20ºC (Zymo Research Group, USA). The DNA quality was verified by running the DNA samples by electrophoresis in 1.5% agarose gel stained with 0.04% (v/v) ethidium bromide for 25 minutes  then documented under the UV light  prior to PCR amplification [10].

Polymerase chain reaction (PCR)

 Polymerase chain reaction was performed using a commercial kit (Quick-DNA mini-prep plus kit). Primers used are according to Cho et al., (2013) [11]. Each PCR reaction was performed using 25 µl of Taq PCR Master Mix Buffer 2X (New England BioLabs). The amplification reactions were performed in a thermocycler Techne TC-312 (England) in PCR tubes containing 25 µL of the following reaction mixture.; 1.0 µl of both the forward and reverse primers (10mM), 5.0µl of extracted fungal DNA, sterile distilled water added to One Taq Quick-Load 2X Master Mix Buffer (New Eng-land BioLabs). The amplification reactions were performed according to Oetari et al.,.(2018) [10]; the  initial denaturation was at 94℃ for 3 minutes, denaturation at 94^oC for 30seconds, annealing at 50^oC for 30seconds, extension at 68^oC for 30seconds and there was a final extension at 68℃ for 5 mins for 30 cycles. Ten (10 µl) of amplicon was resolved by 1.5% agarose gel electrophoresis.  All sequences of ITS regions of DNA determined in this study were deposited in the Gene bank. The Unidirectional sequence reads was performed by standard procedures and the contigs were assembled using bioedit (version 7.2.5.0) sequence program [12]. The evolutionary history was inferred using the neighbor-joining method [13]. The evolutionary distances were computed using the Juke-Cantor method and are in the unit of the number of base substitution per site [14].

Table 1: Reaction volume prepared for PCR Amplifications

Mix                                                                                          1x                                                          50x

DNA                                                                                        2.5ul                                                      -

Primer forward(1um/ul)                                                  1.0ul                                                     5.0ul

Primer reverse(1um/1ul)                                                 1.0ul                                                       5.0ul

Master Mix                                                                           12.5ul                                                 -

Sterile distilled water                                                         8.0ul                                                       -

Total                                                                               25ul                                                         1

Agarose gel electrophoresis 

Agarose gel (1.5%) was prepared by stirring 1.5g of agarose in 100ml 1 x TAE buffer and heating in microwave oven; the solution was allowed to cool and a drop of ethidium bromide (2mg/ml) was added; the solution was poured into a tray fixed with comb to create wells upon solidification. After cooling, the comb was carefully removed. Loading dye was added to the amplified PCR product, and carefully loaded into each well.Gels were run at a voltage of 120 for 90 minutes.

Statistical Analysis

All the analyses was performed in triplicates and the data generated was analyzed by analysis of variance (ANOVA) using  using the SPSS® statistical package(version 20) from IBM® Inc, USA. Differences between             means were evaluated by Duncan’s test. A significance difference was established at ᾳ= 0.05.

The mycoflora commonly associated with groundnut and groundnut product samples belong to the genera Aspergillus, Penicillium, Rhizopus and Fusarium and some were found present in the samples studied. Ncube et al., (2020) [15] recorded the occurrence of these species of fungi among others in their work on groundnut from Zimbabwe. These fungal species are reported to be commonly associated with product preparation, packaging or storage of finished product. As shown in Table 1, this study identified three fungal strains from the test groundnut cake (Kulikuli) samples collected from the three markets in Ibadan city, they include Aspergillus flavus, Aspergillus fumigatus and Aspergillus niger. Based on the percentage incidence, Aspergillus flavus and A. fumigatus were the most dominant fungal species associated with the studied kulikuli samples. This is consistent with results obtained elsewhere in previous studies [16-18]. Aflatoxin was detected in all the samples investigated whether spiced or non-spiced. Aflatoxins B₂ and B₁ appeared to be the most prevalent aflatoxins while aflatoxins G₁ and G₂ recorded no value (that is, it was below detection limit). The analysis of Kulikuli samples showed that aflatoxins level was higher than the permissible limits in almost all the samples over the permissible limits set up by NAFDAC (0.5-15ug/kg). Bodija Flat shaped Kulikuli spiced samples (5.5ug/kg) AFB₂ was within the permissible limits set up by NAFDAC (0.5-15ug/kg) while AFB₂ was seen higher than the permissible limits (109.5ug/kg) in the Bodija Ring shaped kulikuli non-spiced samples. In Oja-Oba samples, AFB₁  was seen to be over the permissible limits for only the Ring shaped kulikuli non-spiced samples (34.5ug/kg) while the Cube shaped kulikuli spiced samples was within the permissible limit (9.5ug/kg). In Oja-Oba samples AFB₂ showed no aflatoxin level over the permissible limits in both the spiced (Cube shape) and non-spiced (Ring shape) Kulikuli samples. The level of total aflatoxins in kulikuli was higher than the maximum acceptable level of the EU commission (4 μg/kg) and FDA standard (20 μg/kg). The present findings of high aflatoxin occurrence in groundnut cake (kulikuli) agrees well with reports of Vabi et al.,2020. Shape has no effect on the level of toxin, therefore it is not a factor that may be used as an intervention strategy.Contamination is traceable to storage pattern where pest infestation leads to infection by aflatoxin producing microorganisms initiating the process of contamination. To achieve the lowest possible levels of contamination of these groundnut cake storage method should be looked into. The proximate composition analysis of the groundnut cake in the study revealed a higher percentage protein content, Fat content, and moisture content in spiced kulikuli samples compared with the non-spiced Kulikuli samples in same parameters that recorded a lower percentage. The percentage Ash content and Crude fibre content recorded higher in the kulikuli non-spiced samples as compared with the Kulikuli spiced samples. The percentage range of crude protein recorded in kulikuli spiced samples (38.36±0.15%) was higher than that of Kulikuli non-spiced samples (32.86±0.15%). Fat content in Kulikuli spiced samples (10.56±0.15%) was also higher than the kulikuli non-spiced samples (7.13±0.15%). The moisture content range of Kulikuli spiced samples (8.76±0.20%) was also higher than that of the kulikuli non-spiced samples (8.33±0.05%). The Ash content range is also higher in kulikuli non-spiced samples (6.66±0.15%) as compared to Kulikuli spiced samples (5.13±0.15%). The percentage crude fibre content was also higher in kulikuli non-spiced samples (6.76±0.15%) than that of kulikuli spiced samples (5.03±0.15%). This study has revealed that kulikuli spiced samples was richer than kulikuli non-spiced samples in protein (38.36%), moisture and fat ((8.76% and10.56%) respectively, whereas it is poorer in ash (5.13%), and crude fibre content (5.03%) as the study indicated. This study also employed DNA based detection system as a tool for detecting and identifying aflatoxin producing fungi. Aspergillus flavus and A. fumigatus have previously been isolated from peanuts as the dominant fungal species in Nigeria. These Aspergillus strains are characterized with a unique conidial head; for example, Aspergillus flavus has conidial head with shades of yellow-green to brown and somehow dark sclerotia and A. fumigatus has a columnar head with shades of greenish to greyish colouration [16]. Most of the previous works to distinguish these Aspergillus strains made use of growth attributes, types of metabolite produced by each strain, and their spores or mycelial morphology [19]. However, due to the complex and diverse characteristics of these Aspergillus strains, it is now common practice to combine morphological and molecular characteristics for their identification. The single band obtained in this study after DNA amplification of the ITS region of all the fungi isolates confirmed that the isolates were obtained from pure cultures. This study affirms that protein is the major nutrient in both spiced and non-spiced kulikuli samples. It was also observed that A. flavus and A. fumigatus were the major aflatoxigenic fungal strains associated with the sampled kulikuli across all the markets. Detected aflatoxin contents of the samples were generally above the tolerance limit and aflatoxins B2 and B1 appeared to be the most prevalent. Specifically, pepper additive were observed to significantly reduce the incidence of fungi and aflatoxin contamination of some of the kulikuli samples. More detailed studies are however still needed for continuous spotting and checking of aflatoxigenic agents in different Nigerian foods. The preliminary information obtained in this study indicates that there is a need for a more routinely and regular evaluation of the occurrence of both aflatoxins and toxigenic A. flavus strains in groundnut products in the studied areas as well as the processing methods embraced for the preparation of kulikuli. Therefore, it is recommended that the production of kulikuli should be carried out under standard hygienic procedures, including storage and selling methods. Adequate relevant quality control units must be reactivated to assess the quality of the Groundnut kernels from which groundnut cake and other products are made. Also, research has to be done to breed Groundnut varieties that are resistant to Aspergillus spp. which subsequently lead to aflatoxin contamination of kernels. Farmers association and extension agents should also be encouraged to create awareness about aflatoxins, and dangers surrounding the commercialization and consumption of mouldy foods.

Table 2: Morphological and microscopic characteristics of the fungal strains associated with Kulikuli

                Fungal Species                  Morphological/microscopic feature on PDA

              Aspergillus flavus                              Appear yellowish-green becoming green with age but creamish yellow reverse.

                                                                      Appears to have radiating conidial heads,

                                                                       long verrucose and hyaline stripe with a small metulae.

                Aspergillus niger                               Appear Blackish-brown often with yellow mycelium.

                                                                        Conidial head appears to be globose, dividing with age.

                                                                       They produce dark or dark brown spores.

                Aspergilus fumigatus                         Appears Bluish-green at upper and creamish-yellow  in its reverse. 

                             Its head is columnar in shape, metulae is absent.

           The conidia is flobose and greenish.

Three aflatoxin species was identified altogether in all the Kulikuli samples from the three markets. Aspergillus flavus and Aspergillus fumigatus has the highest prevalence in Kulikuli samples gotten from the three markets while the least prevalent ones was Aspergillus niger. Two Species of Fungi was identified from the Groundnut cake samples (Kulikuli) collected from Oje market, as Aspergillus flavus and Aspergillus fumigatus. Three species of fungi was identified from the samples collected from Oja-Oba market, the most frequent was Aspergillus flavus and Aspergillus fumigatus while the least prevalent was Aspergillus niger. Two species were identified from the samples from Bodija market, as Aspergillus flavus and Aspergillus fumigatus. 

There are no shape effects on the aflatoxin levels. This means that modelling the shapes during processing may not be a control method for aflatoxin in food

Table 3: Proximate composition (%) of representative ready-to-eat groundnut cake samples

PARAMETER                         SPICED KULIKULI (%)             NON-SPICED KULIKULI(%)

MOISTURE                                                      8.76 ± 0.20                                             8.33 ± 0.05

PROTEIN                                                       38.36 ± 0.15                                          32.86 ± 0.15

FAT                                                                 10.56 ± 0.15                                            7.13 ± 0.15

ASH                                                                   5.13 ± 0.15                                             6.66 ± 0.15 

CRUDE FIBRE                                                 5.03 ± 0.15                                             6.76 ± 0.15

FIG 1: Bar Chart representation of aflatoxin concentrations in groundnut cake sample (Kulikuli) in three markets in Ibadan metropolis.

KEY:  KRB- Bodija Kulikuli Flat shaped (Spiced), K1- Bodija Kulikuli Ring shaped (Non-spiced), KF- Oje Kulikuli Rod shaped (Spiced), KRO- Oje Kulikuli Ring shaped ( Non-Spiced), DS- Oja-Oba Kulikuli Cube shaped (Spiced), D1- Oja-Oba Kulikuli Ring shaped (Non-Spiced)

TABLE 4: Aflatoxin B₁ concentrations in groundnut cake samples (spiced and non-spiced)

Values are presented as mean ± standard error of triplicate determination 

Values in each row with different superscript letter differ significantly at level p<0.05

TABLE 5: Aflatoxin B₂ concentrations in groundnut cake samples (spiced and non-spiced)

Values are presented as mean ± standard error of triplicate determination

Values in each row with different superscript letter differ significantly at level p<0.05

Conflict of Interest

The authors declare that they have no conflict of interest.

Funding: No funding sources 

Ethical approval: The study was approved by the Institutional Ethics Committee of Babcock University

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