PROFILE OF FUNGAL CONTAMINANTS OF MAIZE (ZEA MAYS) INTENDED FOR CONSUMPTION AND THEIR POTENTIAL HEALTH IMPLICATIONS IN THE HO MUNICIPALITY OF GHANA. (2023)

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INTRODUCTION

Fungi are inevitable to encounter in man's daily activities owing to their ubiquitous nature. Fungi have a host-pathogen relationship which could either be beneficial or harmful to the host. Harmful fungi cause diseases in plants, animals, and humans, as well as spoilage in food and feed [1]. Among the fungi classified as microorganisms, the filamentous fungi have the greatest economic significance. They do not only cause food spoilage during pre-and postharvest stages of production but may release various toxic secondary metabolites, referred to as mycotoxins [1]. Filamentous fungi pose serious health risks and have been implicated in the incidence of many diseases of Public Health concern.

Fungal infection of grains before and after harvest remains a major problem of food safety in most parts of Africa. Problems associated with this infection include loss of germination, mustiness, moldy smell [2, 3], and mycotoxin contamination [4-6]. These problems are, however, not effectively dealt with in most developing countries where no careful commodity screening and improved storage conditions are provided.

Maize (Zea mays L.), a staple crop for billions across the globe [7], is commonly consumed fresh or processed into cooked or fermented, milled, and beverage products [8, 9] especially in Africa. Intake levels of approximately 43- 46 kg/person/day of household consumption of maize in rural subsistence farming communities in Ghana have been reported by FAOSTAT [10] and [11]. Shiferaw et al. [12] emphasized that maize is consumed by over 200 million people in different forms globally. This consumption rate is increasing annually with FAO predicting that human and animal consumption demand for maize will be greater than before at nearly 300 million tons by 2030 [13]. Most importantly, it is frequently accompanied by groundnuts in complementary food formulations to help combat protein energy malnutrition although it contains some amino acids [14].

Maize is a stable, important, and very popular worldwide crop probably due to its great nutritional value. It is endowed with abundant macronutrients such as starch, fibre, protein, and fat as well as micronutrients like vitamin B complex, [beta]-carotene, and essential minerals such as magnesium, phosphorus, zinc, copper, and others. [15]. These nutrients make maize prone to colonization by different fungus species both in the field and postharvest. In particular, maize can be a good substrate for some of the best known mycotoxigenic fungi such as Aspergillus flavus, Fusarium verticillioides, and Fusarium graminearum. These mycotoxigenic fungi produce some of the most hazardous substances for humans and animals. The environment during field cultivation or postharvest can determine the conditions in which fungal species are more likely to develop [16].

In warm agricultural areas, the maize crop is frequently infested by Aspergillus section Flavi fungi [17] and contaminated with mycotoxins before, during, and after harvest [18]. Mycotoxins are highly toxic and carcinogenic compounds that negatively impact the health of both humans and livestock [19].

Although there have been some reported works done on the fungal contamination of maize in other parts of Ghana [20, 21], there is a paucity of data regarding the range of fungal contamination of maize in the Volta region. This study therefore aimed at investigating the fungal profile of maize sold and consumed in Ho Volta Region, Ghana.

MATERIALS AND METHODS

Study site

The Ho Municipal is one of the 260 Metropolitan, Municipal and District Assemblies (MMDAs) in Ghana. The population of Ho Municipality according to the 2021 population and Housing Census is 180, 420 (Fig. 1). The Municipality shares boundaries with Adaklu and Agotime-Ziope Districts to the South, Ho West District to the West, Hohoe Municipality to the North, and the Republic of Togo to the East. This study was quantitative and purely experimental. Microbiological analysis was conducted at the Microbiology Laboratory, School of Allied Health Sciences, University of Health and Allied Sciences, Ho, Volta Region, Ghana.

Sample collection

The maize sellers in each market (location) were conveniently sampled. About one kilogram (1kg) of raw maize samples were purchased from February to September 2020. Twenty (20) grams of each of the maize samples were fetched into sterile bags, placed on ice, and transported to the laboratory within the same day. Samples were then stored in a deep freezer at "20 [degrees]C until ready for mycological analysis [23].

Estimation of viable fungal colonies

Exactly 50 g of sample was weighed into 100 ml 0.1% peptone water in 250 ml Erlenmeyer flasks using an electronic weighing balance (OHAUS [R], UK) with a readability of 0.01g. The samples were shaken in a gallenkamp Orbital shaker (140 rev/minute) for 30 seconds. From the stock suspension, decimal serial dilutions up to 1:[10.sup.3] were prepared. Exactly 1ml aliquot of each dilution level was put into 20 ml of Sabouraud Dextrose Agar (SDA) or Dichlor Rose Bengal Chloramphenicol (DRBC) as previously outlined by Kortei et al. [24]. There were triplicate samples for each media and dilution level. The plates were incubated at 28-30 [degrees]C for up to 7 days until the fungi grew.

Fungal Enumeration and Identification

Fungal enumeration was done by a colony counter (STAR 8500, Funke Gerber, Germany) and then calculated as Colony-forming Unit per gram sample (CFU/g) using equation (1). Data obtained in standard units were transformed into the logarithmic form and presented as [log.sub.10] CFU/g samples [24]

CFU/g = No. of colonies x reciprocal dilution factor/The volume of the culture plate. (1)

Molds and yeasts that appeared were identified by their cultural and morphological characteristics (Table 1) using standard identification manuals [25]. Percentage occurrence of fungal species was calculated using the formula;

Percentage (%) occurrence of fungal species = Number of species/Total number of fungi isolated * 100. (2)

The overall occurrence of fungal species on maize samples were calculated using (3)

The overall occurrence of fungal species= Total fungal occurrence/Number of appearances (3)

Determination of Moisture Content (MC)

The MC of the maize samples used was determined based on the procedure outlined by Gyimah et al. [26]. Five grams of the crushed homogenate of the maize samples were weighed into Petri dishes and dried overnight (16 h) in an oven at 105 [degrees]C. Cooling of Petri dishes was done in a desiccator and the final weight was recorded with an Accu Lab ALC-150.3. The MC was determined using the following equation:

= W2-W3/W2-W1 x 100

Where; W1 is the weight of an empty Petri dish

W2 is the weight of sample + petri dish before drying W3 is the weight of sample + petri dish after drying

Data Analysis

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All procedures were carried out in triplicate and the data collected were subjected to a single-factor analysis of variance (ANOVA). Differences among means were separated using Duncan's multiple range test (DMRT) and significances were accepted at a 5% level (P < 0.05) using Statistical Package for the Social Sciences (SPSS) software version 22. The analysis was done using the mean counts expressed in standard forms which were transformed into logarithmic values and results reported as means + standard deviation. Linear Regression analysis was used to determine the association of fungal counts and moisture contents

RESULTS AND DISCUSSION

The moisture content of all maize samples ranged between 12.06 [+ or -]1.17-16.71 [+ or -]2.65% (Table 2), with the moisture content of HM1 being significantly not different (p>0.05) from the majority of maize samples from the different locations of the municipality except for HM4, HM7, HM9 and HM10 where it differed (p<0.05).

The results of the fungal counts of maize obtained from different locations in the Ho municipality of Ghana have been summarized in Table 3. Fungal counts on the SDA ranged between 2.77[+ or -]1.01-4.10[+ or -]0.81 [Log.sub.10] CFU/g corresponding to maize obtained from Ho Municipality areas 1 and 4 (HM1 and HM4) respectively. Statistically, there were no significant differences (p>0.05). On DRBC, the values of fungal counts recorded were within the range of 3.00[+ or -]1.13-4.08[+ or -]1.22 [Log.sub.10] CFU/g corresponding to HM1 and HM3 respectively. Again, all values were comparable (p>0.05). The fungal counts concerning location followed no particular trend.

Tables 4 and 5 show a total of sixteen (16) fungal species belonging to the eleven genera identified in this study. They included Aspergillus niger, A. flavus, A. fumigatus, A. tamarii, A. ochraceous, A. parasiticus, Cladosporium herbarium, Curvularia lunata, Penicillium citrinum, Fusarium moniliforme, Eurotium sp., Mucor racemosus, Rhizopus stolonifer, Paecilomyces variotii, Neurospora sitophilia and Rhodotorula sp.

The species of fungi recorded in this study as dominant included Fusarium spp. (29.3%), Penicillium spp. (28.59%) and Aspergillus spp. (25.0%) and were ranked in decreasing order of Fusarium spp. > Penicillium spp. > Aspergillus spp. Statistically, Aspergillus spp. was significantly lower (p<0.05) than Penicillium spp. and Fusarium spp. (Fig. 2)

A poor fit to linear the equations ([R.sup.2]= 0.1989, [R.sup.2]= 0.0047 for SDA and DRBC respectively) (Fig. 3) were derived from the regression analysis obtained from the plot of fungal counts and moisture contents in maize obtained from the Ho municipality.

Moisture Content

Cereal grains are common substrates that support the growth of a diversity of fungi, especially during storage [27]. The growth of most filamentous fungi and their subsequent mycotoxin production are to a large extent, influenced by environmental factors such as moisture, temperature, and relative humidity [28]. The results were in the same range of values recorded by Al-Shikli et al. [28] and Danso et al. [29] who reported 13.6-18% and 12.4-19% respectively. Findings from this study suggest that the range of moisture content recorded supports fungal growth, especially on the field before harvest.

In many African countries, especially Ghana, the ears of maize are traditionally left in the field on the plants after ripening until they are dry. Throughout this period, maize grains are exposed to unpredictable events, such as tropical downpours, which may occur daily and cause contamination [30]. However, more research should be conducted in the Ho municipality on the handling conditions of maize grains from harvest to storage/market, to confirm the possibility of contamination or otherwise.

Muga et al. [31] investigated the aflatoxin contamination of maize kernels at selected temperature, relative humidity, and moisture content levels. Samples of maize kernels at greater moisture content levels of 14, 15, 16, 18, and 20% (wb) were inoculated with Aspergillus flavus spores and incubated in a climatic test chamber for ten days at 20[degrees]C and 30[degrees]C, and a relative humidity of 60% and 90%. Their results indicated that aflatoxin contamination was significantly affected by temperature and relative humidity, whereas moisture content had no significant effect. In a related study, Raudiene et al. [32] showed grain with high MC has a high rate of respiration and Rogovskii et al. [33] also predicted an increase in temperature in grains with high MC. Likhayo et al. [34] also noted warm temperatures and high MC can result in rapid deterioration of maize and promote the growth and development of microorganisms and insects.

Inadequate storage techniques and environmental conditions trigger fungal growth and mycotoxin contamination of maize. The complex interaction of biotic and abiotic factors within the grain storage ecosystem determines the severity of fungal contamination of stored maize [35]. The primary factors that promote fungal contamination of stored maize are high temperature, grain moisture content, and relative humidity of the surrounding air [36].

Fungal Counts

The survival of fungi on dehydrated products is well known. Maize grains from different locations of the municipality resulted in varied (p<0.05) fungal counts on the media used (Table 2). Fungal counts obtained in this present study were slightly lower than fungal counts obtained from some previous studies. Fungal counts obtained by [37] were in the range of [10.sup.4] (4.0 [log.sub.10]) CFU/g. Jonathan et al. [38] also recorded a range of 4.43-4.92 [log.sub.10] CFU/ml from steeping water from soaked maize. However, the same range of values were reported by Fasoyiro et al. [39] recorded counts within a range of 1.69-2.78 [log.sub.10] CFU/g. While recently, Sserumaga et al. [40] recorded a range of 0-4.97 [log.sub.10] CFU/g from maize samples in Uganda.

Greater fungal counts were observed by Hackman [41] who recorded an initial fungal population in the mixed grain variety was 4.8 - 5.4 [log.sub.10] CFU/g and observed a decrease by 0.4 -1.3 log cycle after 2 months in maize grains obtained from the Ghana Food Distribution Corporation (GFDC) Warehouse at Balduzzi, Kumasi. In Ethiopia, Ayalew et al. [42] recorded mean levels of total fungal density which ranged from 3.46- 5.53 [log.sub.10] CFU/g in maize samples from Dire Dawa, Adama, and Ambo respectively. In South Africa, Ekwomadu et al. [43] recorded a range of 1.04-6.07 [log.sub.10] CFU/g for maize samples meant for consumption in commercial and small-scale settings. Agbetiameh et al. [44] reported a count of range 0.6-5.73 [log.sub.10] CFU/g in maize samples in Ghana. Jesperson et al. [45] also recorded a range of 3.91-6.18 [log.sub.10] CFU/g in maize kennels under different fermentation treatments.

The results suggested that environmental conditions and characteristics exceptional to each type of maize grain can exert an impact on microbial communities existing in that environment [24]. Furthermore, the variation in fungal counts may depend on the mycological medium used to culture the fungi since they are composed of different ingredients which have different capacities to support fungal growth [24].

Fungal Species

The contamination of agricultural products from the field, during storage and transportation are often linked to the genera Aspergillus, Fusarium, and Penicillium (toxicogenic fungi), presumably due to favorable environmental conditions of growth and proliferation in the tropics. They have the capacity to produce mycotoxins which have adverse health effects on humans and animals when ingested. Fungal contamination of grains during storage and transportation occurs commonly in the intercontinental trade of cereals. Spores from fungi are transferred across boundaries during these times. Wheat, rice, barley, com, and some other cereals are delimited for their mold (physical) and mycotoxin (chemical) contamination by the quarantine service of export and import harbors due to the danger they pose which is a major problem in food safety.

Fungal species identified in this present study corroborated with findings from similar previous studies globally. Organisms identified alongside A. flavus species by Dadzie et al. [37] included A. niger, Rhizopus sp, Fusarium moniliforme, Penicillium sp., Verticillium sp., Curvularia lunata, Trichoderma sp., Bipolaris sp. Trichothecium sp., Botryodiplodia sp. and Nigrospora sp. Among the fungal groups identified, five (A. flavus, A. niger, Rhizopus sp. Penicillium sp. and Fusarium sp.) were commonly found on the maize samples in most of the locations they surveyed.

Kieh [46] recorded a plethora of fungi causing maize ear rot in the major maize growing areas in the Ashanti Region of Ghana which included A. flavus, Penicillium sp., Fusarium sp., A. niger, Trichoderma, and Curvularia spp. with Colletotrichum sp. as the most prevalent fungus.

Benson-Obuor et al. [47] isolated fungal species Aspergillus flavus, Colletotrichum gleosporioides, Fusarium sp., Lasiodiplodia theobromae, Penicillium sp. and Rhizopus sp. on maize grains before storage and A. flavus, A. niger, Fusarium sp., L. theobromae, Penicillium sp. and Rhizopus sp. No Colletotrichum gleosporioides was identified. Six different storage fungal species were again isolated from the maize samples after six months of storage from three maize varieties; "Obaatanpa", "aburohemaa", and "abontem" from the Brong-Ahafo region of Ghana.

Interestingly, a mixed flora comprising Candida, Saccharomyces, Trichosporon, Kluyveromyces, and Debaryomyces species were isolated from raw maize, during steeping and early phases of fermentation, and later Penicillium, Aspergillus, and Fusarium species, including potential mycotoxin producers, were isolated from raw maize for 'kenkey' production in Ghana by Jespersen et al. [45]. The findings are in line with other studies done in Ghana [37, 41, 44, 46]. Hackman [41] also isolated fifteen different fungal species, Aspergillus flavus, A. niger, A. sulphureus, A. tamarii, Penicillium brevicompactum, P. chrysogenum, P. citrinum, P. cyclopium, P. digitatum, P. glabrum, P. oxalicum, Cladosporium herbarum, Fusarium moniliforme, F. roseum and Mucor haemalis were isolated from maize grains obtained from the Ghana Food Distribution Corporation (GFDC) Warehouse at Balduzzi, Kumasi where Aspergillus species (A. flavus, A. niger, A. sulphureus, A. tamarii) and Penicillium species (P. brevicompactum, P. chiysogenum, P. citrinum, P. cyclopium, P. digitatum) preponderated. The toxigenic mycobiota recorded in Haitian maize kernels confirmed the well-known existence of favorable conditions for Aspergillus spp. infection in tropical and subtropical latitudes [44].

Several studies by researchers from other African countries [42] (Ethiopia), [43] (South Africa), [48] (Cameroun) have highlighted the mycoflora of maize and implicated the same three toxigenic genera (Aspergillus, Fusarium and Penicillium) of fungi which dominate the contamination of maize grains. Jonathan et al. [38] also isolated Aspergillus spp., Penicillium spp., Fusarium spp., Rhizopus spp. and Saccharomyces cerevisiae from stored maize and the isolation of Aspergillus spp. and Penicillium spp. from fresh maize. In many instances, most Aspergillus sp is recorded as the most dominant.

Contrariwise, the results of this study agreed with the findings of Kpodo [6] who isolated different species (verticilloides, semitectum, equiseti, oxysporum, and graminaerum) of the Fusaria genus from maize grains in Ghana which was a deviation from the norm were the dominant genera have been Aspergillus which were always known to contaminate maize meant for consumption in Ghana. Likewise, the published findings of [49, 50, 51] all pointed to Fusarium verticilliodes, F. graminearum, F. subglutinans as the most prevalent fungal species of maize.

The predominance of Penicillium spp. in the maize mycobiota has also been previously found by other authors [41, 52] in association with nonoptimal conditions during storage. Similarly, Ngoko et al. [48] also recorded Nigrospora sp as the most prevalent fungus in maize from humid forest and western highlands of Cameroun.

Studies have also reported that maize samples with greater occurrence of Fusarium verticillioides are less likely to be infested with A. flavus and have been shown to be negatively linked with other fungal species [53]. This could be an explanation to the overall lower incidence of Aspergillus and Penicillium sp. as well as some other fungal isolates as reported in this study.

Rheedar et al. [53] emphasized climatic factors (temperature, precipitation, drought, and atmospheric carbon dioxide, a biological environment of crops such as the abundance of pests and plant pathogens) greatly impact agriculture and gradually but surely affect the quality of grains produced. Darfour and Rosentrater [11] also explained that storage of maize is a common practice in the market where maize samples were collected is characteristic of most markets in Ghana and in Sub Saharan Africa. This practice of hording is usually done to preserve maize grains until the time that fresh ones will come out in the subsequent season. However, maize grains are often contaminated by fungi during storage when fungal spores in the air enter the maize grains through the pores of the storage materials that are used to store the grains. Therefore, there is a need to unremittingly monitor the quality of grain to assess possible climatic effects and be able to take measures before any outbreak. This is because several genera and species of filamentous fungi produce mycotoxins that have significant agricultural, epidemiological, economic, and health bearings. It is worthy to note that the impacts of climate change on growth and development of fungi and their direct bearing on food safety and food security are stern issues which require devotion. A spot light on the health implications of the major genera of toxigenic fungi (Fusarium, Aspergillus, and Penicillium) associated with maize in this present study is considered.

The genus Aspergillus is almost synonymous with aflatoxin production. Aflatoxins are secondary metabolites produced by toxic strains of A. flavus and A. parasiticus and to a lesser extent by A. nomius. The presence of aflatoxins in maize is well known. There are five different types; aflatoxins [B.sub.1], [B.sub.2], [G.sub.1], [G.sub.2], and [M.sub.1] produced primarily in cow milk by cows eating contaminated silage. Prolonged consumption of aflatoxins has been reported to cause impaired immune function, malnutrition and stunted growth in children, teratogenic, mutagenic disabilities, and eventual death [40, 54]. Aflatoxin as a well-categorized class 1 carcinogenic toxin (IARC) is known to have adverse effects on reproductive health and associated with cirrhosis, hepatitis B and C infections, and liver cancer [54]. Recently, Richard et al. [55] reported on the novel neurotoxic and neuro-immunotoxic capabilities of aflatoxins on the nervous system. There has also been a reported correlation between hepatitis B and aflatoxin consumption in Africa and liver damage occurrence by aflatoxins, which differed over a 5-fold range and was strongly associated with estimated levels of aflatoxins [56].

Varietal differences in A. flavus infection and aflatoxin production in foods have been documented [5, 44, 57, 58]. This probably partly explains the differences in the susceptibility of the local maize varieties to infection by A. flavus especially those obtained from other regions of Ghana. Future studies with focus on varietal differences in susceptibility to potential mycotoxigenic fungi from the different agro-ecological zones of Ghana will provide a clear understanding of this phenomenon. Although A.niger is not known to produce aflatoxins, it possesses the ability to produce other toxins such as ochratoxin A, malformin, and nigerone [59]. Ochratoxin A is lipid soluble produced by A. alutaceus (= A. ochraceus) and A. carbonarius and is not expelled efficiently and thus accumulates in meat which exposes humans to health risk after entering contaminated meat [60].

Penicillium citinum was among the frequently isolated contaminants in stored maize in this present study. More than 80 Penicillium species are documented toxin producers [58]; the most important are ochratoxin A, citreoviridin, penitrem A, roquefortine, and secalonic acid. The genus has major importance in the natural environment as well as food and drug production industry. The first citrinin producer described was Penicillium citrinum, other species such as P. miczynski, P. hirsutum, P. verrucossum, P. westling, P.expansum, P.stechii, P. cyclopium have been reported to also produce citrinin [60]. Besides, several species included in the genera Aspergillus and Monascus have also been reported to be able to produce this toxin. Other variants or species of Penicillium such as P. verrucosum, P. viridicatum produce ochratoxins, cyclopiazonic acid, penicillic acid and citrinin. Observed in higher latitudes, P. verrucosum is the primary producer of ochratoxin A and this toxin is relatively ten times more toxic than citrinin [62]. The chief target organ of citrinin is the kidney, and its ingestion is related to weight loss because of renal degeneration. This nephrotoxin causes damage in the proximal tubules of the kidney, and it is considered one possible cause of porcine nephropathy. Few reports are available about the acute toxicity of citrinin. Oral [LD.sub.50] in mice has been established as 110 and 134 mg [kg.sup.-1] in rabbits [63].

Fusarium species isolated from maize seeds produce several mycotoxins such as biologically active trichothecenes, which when ingested in high concentrations, cause vomiting and diarrhea in humans. Trichothecenes are also associated with reduced weight gain and immune dysfunction in animals [64]. Human uterotrophic (anti-reproduction) effects are caused in animals and pigs by zearalenone [58, 65]. Another Fusarium species, F. verticillioides (F. moniliforme), isolated in this study produces fumonisins which have been reported to have a neurotoxic effects in animals and is associated with oesophageal cancer in Sub-Saharan -Africa [66]. Consumers are entreated to be cautious of the kind of maize they choose in the preparation of their meals and beverages since improperly treated (dried and stored) maize grains are a cause for alarm. Toxigenic fungi have a penchant for growing on maize and besides their presence, also exude some natural metabolites (mycotoxins) which are detrimental to the health of both humans and animals.

Results showed a wider range of mycotoxigenic fungi that contaminate local maize and there is a need to widen the scope of mycotoxin analysis to cover possible mycotoxins such as fumagillin (A. fumigatus) Ochratoxin A (P. verrucosum), Fumonisins (Fusarium spp.) which have demonstrated to have human health implications. Furthermore, F. oxysporum isolated in this study ranks among the ten (10) most wilt destroying fungal pathogens worldwide [65]. Its presence in maize seeds could devastate crop productivity in the field.

Good agricultural practice (GAP), good manufacturing practices (GMP), as well as good hygiene practices (GHP), are vital to avert the growth of filamentous fungi and possibly mycotoxins in the field and during storage. By discouraging fungal growth and subsequent mycotoxin formation in maize, public health is protected and economic losses can be avoided. Monitoring maize for the presence of possible fungal contamination in a consistent manner is judicious to evaluate the public level of awareness.

CONCLUSION

The results obtained were able to ascertain the degree of contamination and occurrence of a wide range of filamentous fungal species in maize destined for human and animal consumption in Ho municipality of Ghana. The findings on the fungal diversity of maize from this area of the country may be an addition to the microbial assemblage in the ecosystems of Ghana and Africa at large. It can be construed from this present work that local maize was contaminated with a total of sixteen (16) fungal species belonging to eleven (11) genera were identified in this study. They included Aspergillus niger, A. flavus, A. fumigatus, A. tamarii, A. ochraceous, A. parasiticus, Cladosporium herbarium, Curvularia lunata, Penicillium citrinum, Fusarium moniliforme, Eurotium sp., Mucor racemosus, Rhizopus stolonifer, Paecilomyces variotii, Neurospora sitophilia and Rhodotorula sp. The genus Fusarium was found to be the most overriding fungus.

Previous studies have focused on mycotoxin analysis of maize narrowing down to the aflatoxin groups by and large, but not on other equally potent mycotoxins. Results from this study showed that a broader spectrum of mycotoxigenic fungi infect maize grown in the study area. This suggests the need to widen the scope of mycotoxin analysis to cover possible mycotoxins such as fumagillin (A. fumigatus), ochratoxin A (P. verrucosum), and fumonisin (Fusarium spp.), which have been confirmed to have human adverse health implications. Furthermore, F. moniliforme isolated in this study ranks among the 10 most destructive wilt fungal pathogens worldwide. Its presence in maize seeds could devastate crop productivity in the field.

ACKNOWLEDGEMENTS

Authors are indebted to the microbiology laboratory technicians of the Department of Nutrition and Dietetics, School of Allied Health Sciences, University of Health and Allied Sciences, as well as the Food Microbiology Division, CSIR-Food Research Institute, Accra for their contribution to the mycological analysis. Not forgetting the enormous support of Prof. G.T. Odamtten Mycology Unit, Department of Plant and Environmental Biology of the University of Ghana who helped in the identification of some species of fungi. Our heartfelt thanks go to the families of the authors for their never-ending backing.

AUTHOR CONTRIBUTIONS

NKK, DA, W-KM, EKE, COT, AAA and TA performed the experiments and wrote the manuscript. EKE, JGD, DA, and COT were responsible for statistical analysis. W-KM, JGD and NKK helped conceive the experiments and prepare the manuscript. NKK, TA, and AAA conceived the original study and COT, EKE, NKK, and AAA led the sampling and study in Ghana. All authors read and approved the final manuscript.

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Kortei NK (1*), Amanor D (1), Wiafe-Kwagyan M (2), Annan T (3), Boakye AA (4), Essuman EK (1), Deku JG (5) and CO Tettey (4)

(*) Corresponding author email: nkkortei@uhas.edu.gh

(1) Department of Nutrition and Dietetics, School of Allied Health Sciences, University of Health and Allied Sciences, PMB 31, Ho, Ghana

(2) Department of Plant and Environmental Biology, College of Basic and Applied Sciences, University of Ghana, P. O. Box LG 55, Legon, Ghana

(3) Food Microbiology Division, Council for Scientific and Industrial Research- Food Research Institute, P. O. Box M20, Accra

(4) Department of Biomedical Sciences, School of Basic and Biomedical Sciences, University of Health and Allied Sciences, PMB 31, Ho, Ghana

(5) Department of Medical Laboratory Sciences, School of Allied Health Sciences, University of Health and Allied Sciences, PMB 31, Ho, Ghana

https://doi.org/10.18697/ajfand.115.21645

Table 1: Cultural and morphological characteristics of identified fungiFungal Cultural CharacteristicsSpecieMucor spp Large white colonies which turn into black later.Rhizopus spp. White cottony mycelia with black dots and covers the entire plate.Penicillium Fast-growing colonies inspp. green color with dense felt conidiophoreAspergillus Yellow to green, and blackspp. colonies with a distinct marginCurvularia Fast-growing colonies ofSpp. suede-like with downy, brown to blackishCladosporium Colonies are mostly greyish-spp olive appearance and later powderyFusarium spp. White-pink, sparse aerial mycelia becoming feltyRhodotorula Soft, smooth, moist, andspp. mucoidEurotium spp. Broad zones of flat dull green to greyish green coloniesNeurospora Ascomata are ostiolate, darkspp. brown to black, smooth or downy with loose hyphaeFungal Morphological CharacteristicsSpecieMucor spp Erect sporangiophores are formed. Sporangiophore swell at the tip to form sporangia which are globular shaped. Columella is present.Rhizopus spp. Sporangiospores are produced inside a spherical sporangium. Columella is present on the top of the sporangiophore. Root-like rhizoids are foundPenicillium Branched conidiophores with chains of conidia lookspp. like a brush.Aspergillus Conidiophores arise from a foot cell. Club shapedspp. vesicles on top of the conidiophores. Conidia are found in chainsCurvularia Conidiophores are erect, straight to flexuous, septate,Spp. often geniculate (producing conidia in sympodial succession)Cladosporium Conidiophores arising laterally or terminally from thespp hyphae. Bears chains of conidiaFusarium spp. Macro conidia sparse, borne on phalides with branched conidiophores (Septate banana-shaped).Rhodotorula Round or oval-shaped budding cells.spp.Eurotium spp. Asci are globose to subglobose. Ascospores single- celled, lenticular, small, smooth-rough surfaceNeurospora Ascospores are uniseriate or somewhat overlapping,spp. initially hyaline, becoming yellowish-brown to black with maturity, one-celled ellipsoidal or elongate, ascospores wall surface with global ornate pitsSources: [36, 37]
Table 2: Moisture content of maize samples obtained from various locations in HoLocation Moisture Mean [+ or -] standard deviation Content (%)HM1 13.42 12.06 [+ or -]1.17a 11.38 11.41HM2 11.24 13.59 [+ or -]2.10ab 14.27 15.28HM3 15.22 13.85 [+ or -]1.55ab 14.18 12.17HM4 14.48 15.93 [+ or -]1.25bc 16.68 16.65HM5 13.11 13.81 [+ or -]1.16ab 15.16 13.17HM6 10.14 14.03 [+ or -]3.51ab 16.97 14.99HM7 15.84 15.06 [+ or -]1.19bc 13.69 15.09HM8 11.63 14.31 [+ or -]2.38ab 16.21 15.09HM9 17.77 16.71 [+ or -]2.65d 18.67 13.69HM10 15.78 15.70 [+ or -]0.55bc 16.21 15.11Means in a column with the same superscript letters are not statistically different (p>0.05) HM1= Ho Municipality area 1, HM2= Ho Municipality area 2, HM3= Ho Municipality area 3, HM4= Ho Municipality area 4, HM5= Ho Municipality area 5, HM6= Ho Municipality area 6, HM7= Ho Municipality area 7, HM8= Ho Municipality area 8, HM9= Ho Municipality area 9 HM10= Ho Municipality area 10
Table 3: Fungal counts of maize enumerated on two (2) different media (SDA and DRBC) incubated for 5-7 days at 36[+ or -]1 [degrees]C SDA [Log.sub.10] CFU/g Mean + Standard Grand Mean + Deviation Standard deviationHM1 2.83[+ or -]0.61 2.77[+ or -]1.01a 2.92[+ or -]1.20 2.58[+ or -]1.20HM2 3.03[+ or -]0.30 3.72[+ or -]0.90a 4.73[+ or -]1.11 3.42[+ or -]1.32HM3 3.83[+ or -]0.50 3.33[+ or -]0.81a 3.05[+ or -]0.70 3.11[+ or -]1.21HM4 3.80[+ or -]0.90 4.10[+ or -]0.81a 5.20[+ or -]1.22 3.31[+ or -]0.50HM5 3.19[+ or -]0.50 3.44[+ or -]0.71a 3.90[+ or -]0.90 3.25[+ or -]0.41HM6 3.45[+ or -]1.10 2.91[+ or -]0.90a 3.05[+ or -]1.42 2.25[+ or -]0.30HM7 3.78[+ or -]1.10 3.84[+ or -]141a 3.26[+ or -]1.10 4.49[+ or -]0.62HM8 4.30[+ or -]1.11 4.08[+ or -]141a 4.55[+ or -]1.00 3.38[+ or -]1.90HM9 3.92[+ or -]1.10 3.19[+ or -]0.60a 2.84[+ or -]0.22 2.80[+ or -]0.71HM10 3.72[+ or -]0.81 3.62[+ or -]0.80a 3.01[+ or -]0.92 4.13[+ or -]0.70 DRBC [Log.sub.10] CFU/g Mean + Standard Grand Mean + deviation Standard deviationHM1 2.77[+ or -]1.21 3.00[+ or -]1.13ab 2.79[+ or -]142 3.44[+ or -]0.70HM2 372[+ or -]0.83 4.06[+ or -]0.81ab 4.55[+ or -]1.20 3.72[+ or -]0.11HM3 4.30[+ or -]1.10 4.08[+ or -]1.22ab 4.55[+ or -]1.21 3.38[+ or -]1.21HM4 343[+ or -]1.70 3.48[+ or -]1.04ab 3.72[+ or -]0.81 3.28[+ or -]0.51HM5 3.92[+ or -]1.11 4.07[+ or -]1.11ab 2.84[+ or -]0.20 2.80[+ or -]040HM6 342[+ or -]1.60 3.04[+ or -]0.81ab 3.30[+ or -]1.20 2.74[+ or -]0.82HM7 2.99[+ or -]0.92 3.21[+ or -]1.12ab 3.35[+ or -]1.51 3.31[+ or -]0.81HM8 3.06[+ or -]0.73 3.43[+ or -]0.52ab 3.50[+ or -]0.71 3.75[+ or -]0.61HM9 4.27[+ or -]1.50 3.78[+ or -]0.90ab 3.39[+ or -]0.62 3.69[+ or -]0.82HM10 2.57[+ or -]0.91 3.18[+ or -]0.61ab 4.17[+ or -]0.53 2.81[+ or -]042Means in a column with the same superscript letters are not statistically different (p>0.05) HM1= Ho Municipality area 1, HM2= Ho Municipality area 2, HM3= Ho Municipality area 3, HM4= Ho Municipality area 4, HM5= Ho Municipality area 5, HM6= Ho Municipality area 6, HM7= Ho Municipality area 7, HM8= Ho Municipality area 8, HM9= Ho Municipality area 9 HM10= Ho Municipality area 10
Table 4: Fungal species and their percentage (%) occurrence in maize from various locations in Ho cultured on two (2) different media (SDA and DRBC) and incubated for 5-7 days at 36[+ or -]1 [degrees]C Location of sampling HM1 HM2 HM3 HM4 HM5 S D S D S D S D S D % % % % % % % % % %FungirecordedAspergillus 43. 24. 17. 6.3 14.8 17. 45.flavus 5 5 4 2 7A.niger 2.0 4.1 20. 25. 13.8 24. 6.0 5 5 2A.fumigatus 44.8 13.8 11.1 13. 65.2 8A.tamarii 4.8 4.1 13 3.0A.ochraceous 17.1A.parasiticus 5.1 3.0 12.2Cladosporium 6.9 3.6 6.0herbarumCurvularia lunata 4.1 7.4 3.4Penicillium 46. 51. 17.2 10 20.8 29.7 24. 22.6citrinum 3 9 2Fusarium 6.9 46. 31. 24.2 30.0 20. 6.0moniliforme 3 7 8Eurotium sp. 1.3Mucor 5.1 7.0 22.racemosus 5Rhizopus 7.7 6.9 15. 17.5stolonifer 5Paecilomyces 3.4 4.3 3.4 7.8variotiiNeurospora 1.5sitophiliaRhodotorula sp. 7.7 3.4 Location of sampling HM6 HM7 HM8 HM9 HM10 S D S D S D S D S D % % % % % % % % % %FungirecordedAspergillus 34.6 24. 44.0 23. 37 2.4flavus 1 9A.niger 38. 21. 5.0 6.8 15 5.0 1 7A.fumigatus 18.3 13. 24. 8 6A.tamarii 3.5A.ochraceous 8.2 3.4 7.3A.parasiticus 4.6Cladosporium 7.6 16 20herbarumCurvularia lunata 8.2 3.4 5.6Penicillium 16.3 17. 9.5 26 15. 78 45citrinum 2 7Fusarium 13. 28. 35. 5.1 95 31. 35moniliforme 7 6 2 8Eurotium sp. 5.0Mucor 10.racemosus 5Rhizopus 23. 14 28 15stolonifer 8Paecilomyces 2.0 3.4variotiiNeurospora 10.sitophilia 8Rhodotorula sp. 5.2 22.9 5.0S= Sabouraud Dextrose Agar (SDA), D= Dichlor Rose Bengal Chloramphenicol (DRBC)HM1= Ho Municipality area 1, HM2= Ho Municipality area 2, HM3= Ho Municipality area 3, HM4= Ho Municipality area 4, HM5= Ho Municipality area 5, HM6= Ho Municipality area 6, HM7= Ho Municipality area 7, HM8= Ho Municipality area 8, HM9= Ho Municipality area 9 HM10= Ho Municipality area 10.
Table 5: Pooled data of total fungi isolated from maize obtained from the Ho municipality, GhanaAspergillus niger Van [Tieghem.sup.HM1, HM2, HM3, HM4, HM5, HM7, HM9,HM10]A. flavus [Link.sup.HM1, HM3, HM4, HM5, HM6, HM8, HM9, HM10]A. fumigatus [Fresen.sup.HM2, HM3, HM4, HM5, HM6, HM7]A. ochraceus [Wilhelm.sup.HM2, HM6, HM8]A. parasiticus [Speare.sup.HM2, HM5]A. tamarii [Kita.sup.HM1, HM2, HM5, HM9]Cladosporium herbarum (Pers.) [Link.sup.HM2, HM3, HM5, HM6, HM8]Curvularia [lunata.sup.HM3, HM4, HM6, HM7]Penicillium citrinum [Thom.sup.HM1, HM2, HM3, HM4, HM5, HM6, HM7, HM8,HM10]Fusarium moniliforme [Schlecht.sup.HM2, HM3, HM4, HM5, HM6, HM7, HM8,HM9, HM10]Eurotium sp. [Mangin.sup.HM2, HM9]Mucor racemosus [Fres..sup.HM2, HM4, HM5, HM6]Rhizopus stolonifer (Ehrenb.) [Lind..sup.HM1, HM2, HM3, HM7, HM8, HM10]Paecilomyces variotii [Bain.sup.HM1, HM3, HM5, HM6]Neurospora [sitophilia.sup.HM3, HM9]Rhodotorula sp. (A. Jorg) F.C. [Harrison.sup.HM1, HM3, HM6, HM7, HM9]Note: Superscripts show the treatments in which the fungal species appeared inHM1= Ho Municipality area 1, HM2= Ho Municipality area 2, HM3= Ho Municipality area 3, HM4= Ho Municipality area 4, HM5= Ho Municipality area 5, HM6= Ho Municipality area 6, HM7= Ho Municipality area 7, HM8= Ho Municipality area 8, HM9= Ho Municipality area 9 HM10= Ho Municipality area 10

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