Food and Chemical Toxicology 42 (2004) 1309–1314

www.elsevier.com/locate/foodchemtox

Natural occurrence of moulds and aflatoxin B1 in melon seeds

from markets in Nigeria
a,*
S.A. Bankole , B.M. Ogunsanwo b, O.O. Mabekoje a

a
Department of Biological Sciences, Olabisi Onabanjo University, P.M.B. 2002, Ago-Iwoye, Ogun State, Nigeria
b
Department of Chemical Sciences, Olabisi Onabanjo University, P.M.B. 2002, Ago-Iwoye, Ogun State, Nigeria
Received 14 December 2003; accepted 17 March 2004

Abstract
Shelled melon seeds (Colocynthis citrullus L.) were purchased from markets in randomly selected villages and towns in three states
in each of the rain forest (Ogun, Oyo and Osun) and Northern guinea savanna (Kaduna, Niger and Bauchi) zones of Nigeria. The
seed samples were analysed for incidence of visibly diseased seeds, moisture content, moulds and aflatoxin B1 contamination. The
incidence of diseased seeds ranged from 6.4% to 50.4% in the forest, and 4.3% to 34.3% in the savanna, and the moisture content was
5.6% to 12.6% and 4.5% to 10.3%, respectively. Mould evaluation revealed that Aspergillus was the most frequent genus, followed by
Penicillium, Botryodiplodia, Cladosporium and Rhizopus in decreasing sequential order. Aspergillus flavus had the highest individual
count in melon seed from both zones. Aflatoxin B1 was detected at levels above 5 lg/kg in 32.2% of samples, while only 3.5% of the
samples contained the toxin above the 20 lg/kg Nigerian tolerance level in food. The percentage of samples contaminated with
aflatoxin B1 was statistically comparable for the pooled data of villages and towns. The median level of aflatoxin B1 was less than 5
lg/kg in the seed samples, while the mean aflatoxin B1 levels was 14.1 lg/kg in the forest and 13.0 lg/kg in the savanna samples.
Ó 2004 Elsevier Ltd. All rights reserved.

Keywords: Aflatoxin B1 ; Shelled melon seeds; Surveillance; Markets; Moulds; Moisture content

1. Introduction processing facilities, storage, transportation and skilled

Evidence abound in literature that the people of West
Africa are experiencing heavy dietary exposure to food-
borne mycotoxins especially aflatoxins (Bankole and
Adebanjo, 2003a). Exposure to aflatoxin is widespread
in west Africa, probably starting in the womb, and
blood tests have shown that very high percentage (over
90%) of the inhabitants tested positive to aflatoxin
markers (Wild, 1996; Gong et al., 2002). According to
the World Development Report (1993) diseases caused
by mycotoxins lead to reduced life expectancy in
developing countries (Miller, 1996). The West African
countries have tropical climate with an all year round
high ambient temperatures and relative humidity that
provide favourable condition for the growth of toxigenic
moulds. The sub-region also has poorly developed
*
Corresponding author. Tel.: +234-80-34547705; fax: +234-37-
431966.
E-mail address: sabankole@juno.com (S.A. Bankole).
0278-6915/$ - see front matter Ó 2004 Elsevier Ltd. All rights reserved.
doi:10.1016/j.fct.2004.03.015
human resources.
Aflatoxin contaminated diet has been associated with
the elevated rate of liver cancer, decreased immunity,
kwashiorkor and growth stunting in the sub-region
(Hendrickse, 1984; Turner et al., 2000; Gong et al., 2002;
Turner et al., 2003). Naturally occurring mixtures of
aflatoxins and aflatoxin B1 have been classified as group
1 human carcinogen (IARC, 1993).
Melon seeds (Colocynthis citrullus L.) is a protein and
oil-rich crop widely cultivated and consumed in west
Africa as an important source of oil and protein in the
diet of many people (Abaelu et al., 1979). It contains
about 50% oil, 28% crude protein along with some
important minerals and vitamins (Oyolu, 1977; Oke and
Umoh, 1978). They are consumed in egusi soup, melon
ball snacks and ‘ogiri’ a fermented condiment (Oyenuga,
1968; Odunfa, 1981), while some rural dwellers of
southeastern Nigeria mix ground melon seeds and
Pleurotus tuber-regium and mould them into balls to
replace meat in their food (Nwokolo and Sim, 1987).
The amino acid contents of melon seeds satisfy the
1310 S.A. Bankole et al. / Food and Chemical Toxicology 42 (2004) 1309–1314
protein and amino acid need of all human categories
when compared to the Food and Agricultural Organi-
sation/World Health Organisation Standards (Abaelu
et al., 1979; Nwokolo and Sim, 1987).
Little is known of the incidence of aflatoxins in melon
seeds, but Aspergillus flavus was one of the most domi-
nant fungi on stored seeds (Bankole, 1993). Melon seeds
supported the production of aflatoxin on artificial
inoculation of toxigenic A. flavus (Ogunsanwo et al.,
1989), while some melon ball snacks were contaminated
with aflatoxins (Bankole, 1995). The period of harvest-
ing of melon seeds often coincide with the time of peak
rainfall (July and August), thus the traditional sundry-
ing employed by the predominantly resource-poor
Nigeria farmers may be difficult and takes longer time.
Consequently farmers are forced to load seeds into
stores with high moisture content, which favour mould
infection and mycotoxin contamination. It is important
to screen all foods that may contribute to the total
aflatoxin load in the populace. This work concerns the
aflatoxin B1 levels in melon seeds collected from markets
in towns and villages in two ecological zones of Nigeria,
the rain forest and the Northern guinea savanna.
2. Materials and methods
Melon seed samples were purchased from open
markets in randomly selected villages and towns in three
states in each of the rain forest and Northern guinea
savanna zones of Nigeria from March to June, 2001.
The states in the rain forest were Ogun, Oyo and Osun
while Kaduna, Niger and Bauchi states represented
states in the savanna. The ambient temperature and
relative humidity values at the sampling points were
taking with a thermohydrograph. The villages used in
this study have all the dwellers as either farmers or
traders dealing in farm products, with a population
count of less than 2,000 people per village. The towns
selected for the survey all had human populations above
20,000. Approximately 1 kg seeds were collected at each
sampling. The proportion of visibly mouldy, rotten or
discoloured seeds via random sample of 400 seeds from
each sample was determined. The moisture content was
determined by drying at 105 °C to constant weight.
2.1. Isolation of moulds
About 150 seeds from each sample were surface
sterilized for 1 min in 1% NaOCl, rinsed thrice in sterile
distilled water, and 100 seeds (10 per plate) placed on
potato dextrose agar complemented with chloram-
phenicol. After incubation for 7–10 days at 28° ± 2 C,
the percentage of seeds with different fungi was deter-
mined. Identification of fungi was done by using the
method for each genus (Raper and Fennel, 1965; Pitt,
1979; Samson et al., 1984; Barnett and Hunter, 1987).
2.2. Aflatoxin analysis
The extraction and assay of aflatoxin B1 was per-
formed using the modified EEC method (Bankole et al.,
1996). Five hundred grams from each seed sample was
crushed with a Moulinex blender. Sub-samples (25 g
each) were homogenised in 125 ml of 7:3 methanol–
water for 30 min and defatted twice with 25 ml n-hexane
in a separatory funnel. The extract was clarified with
ammonium sulphate followed by partitioning to chlo-
roform. The chloroform extract was evaporated to near
dryness in a rotary evaporator. The residue was redis-
solved in 0.5 ml chloroform and spotted on silica gel (60
G plates). A series of standard aflatoxin B1 solution was
spotted on the same plate for comparison. The plates
were developed with a 90:30:2, v/v/v toluene/isoamylal-
cohol/methanol solvent system in a thin layer chroma-
tography tank. The levels of aflatoxin B1 was quantified
by visual comparison of extract fluorescent spots with
that of standard aflatoxin spots under long wave UV
light (365 nm). The identity of aflatoxin was confirmed
by derivatization with trifluoroacetic acid (Stack and
Pohland, 1975).
The minimum detection level of aflatoxin B1 was 5
lg/kg. Samples containing aflatoxin B1 were classed as
5–10, 10–15, 15–20 and >20 lg/kg in view of the Codex
Alimentarius tolerance level of 5 lg/kg and the maxi-
mum 20 lg/kg for all classes of food in Nigeria (FAO,
1997).
Recovery experiments were run to test the validity of
the TLC procedure used for aflatoxin B1 assay in melon
seeds. Freshly harvested and sun dried melon seeds were
spiked by adding known quantities of aflatoxin B1 (5–20
lg/kg), then extracted and analyzed by the method de-
scribed above. The average recovery of 86.5% with
standard deviations of 5.3% was found for 20 spiked
melon seed samples.
2.3. Statistical analysis
Aflatoxin B1 levels and other quantitative data were
log transformed, while values in percentages were
transformed to the arcsine of the square root to nor-
malize distributions. Data analysis was performed using
the t-test and correlation and regression analysis (Sokal
and Rolf, 1987). Significant tests were carried out at the
5% level of significance.
3. Results and discussion
The mean ambient humidity during the period of the
survey ranged from 45% to 86% in the forest and 32% to
 S.A. Bankole et al. / Food and Chemical Toxicology 42 (2004) 1309–1314 1311

Table 1 tween moisture content and the incidence of diseased

Percentage of diseased seeds and moisture content of melon seeds from seeds in the forest (r ¼ 0:52) and savanna (r ¼ 0:64).
markets in the rain forest and Northern guinea savanna of Nigeria
The higher ambient relative humidity in the forest ac-
State No of samples Diseased Moisture counts for the higher moisture content and incidence of
seeds (%) content (%)
diseased seed.
Forest
Melon seeds are offered for sale in the shelled form,
Ogun Villages 32 8.8–39.5 5.8–12.6
Towns 28 7.4–42.3 6.2–10.8 while storage is done with the protective shells that
constitute barrier to invasion by moulds, and this may
Oyo Villages 26 6.4–33.7 5.5–11.6
have accounted for the higher proportion of diseased
Towns 29 8.5–50.4 5.7–12.1
seeds obtained in market samples in this study than the
Osun Villages 22 10.6–35.2 6.4–12.2 values obtained in the unshelled seeds from stores in an
Towns 24 5.6–29.2 5.6–11.4
earlier report (Bankole, 1998). The hawking operations
in the markets whereby traders pick back spilled seeds
Savanna
Kaduna Villages 35 4.3–34.3 5.1–8.7 into the basins used for display, thus introducing
Towns 26 5.5–20.4 5.3–8.4 microbial propagules may also have contributed to the
increased incidence of diseased seeds. Melon seeds also
Niger Villages 28 7.2–28.3 4.7–9.1
Towns 25 9.2–23.5 5.6–10.3 readily absorb more moisture in the shelled form than
when it is unshelled, and this may also have been
Bauchi Villages 23 8.8–30.3 4.5–9.6
responsible for the higher moisture content than that of
Towns 19 6.6–28.6 5.5–8.5
unshelled seeds.
The fungi identified in the 317 melon seeds samples
65% in the savanna, while the temperature was 26–33 showed that Aspergillus spp. was the most frequent
and 29–36 °C, respectively. The moisture content in genus, followed by Penicillium, Botryodiplodia, Clado-
melon seeds from markets varied from 5.6% to12.6% in sporium and Rhizopus in sequential order (Table 2). The
the rain forest, and 4.5% to 10.3% in the savanna (Table other four genera isolated at low frequencies were
1). The proportion of diseased seeds ranged from 6.4% Fusarium, Macrophomina, Mucor and Paecilomyces. A.
to 50.4% in the forest, and 4.3% to 34.3% in the sa- flavus had the highest individual count in terms of fre-
vanna. Statistical analysis by t-test shows that the pro- quency of occurrence in samples and abundance in both
portion of diseased seeds and the moisture contents were zones, in 70.8% of forest, and 52.8% in the savanna
significantly higher in the forest samples than in the samples, followed by A. niger, P. citrinum, B. theobro-
savanna samples, whereas no significant difference was mae, Cladosporium sp. and A. clavatus. The predomi-
found between the two parameters for rural and urban nance of Aspergillus spp. in the present study agrees with
areas. Significant positive correlation was found be- data previously reported (Aboaba and Amasike, 1991;

Table 2
Moulds isolated on marketed melon seeds from the rain forest and Northern guinea savanna of Nigeria
Fungi Forest (n ¼ 161) Savanna (n ¼ 156)
No of samples Mean incidence No of samples Mean incidence
Aspergillus clavatus 24(14.9)a 2.6b 42(26.9)a 4.3b
A. flavus 114(70.8) 42.3 83(53.2) 31.8
A. fumigatus 15(9.3) 1.7 31(19.9) 3.6
A. niger 70(43.5) 34.3 76(48.7) 42.5
A. ochraceus 9(5.6) 1.7 ) )
Aspergillus spp. 21(13.4) 1.3 25(16.0) 2.5
Botryodiplodia theobromae 43(26.7) 8.3 36(23.1) 7.5
Cladosporium sp. 32(19.9) 4.1 46(29.5) 6.5
Curvularia spp. – – 8(5.1) 1.3
Fusarium spp. 21(13.0) 2.5 15(19.6) 3.8
Mucor spp. 12(7.5) 1.3 32(20.5) 3.7
Paecilomyces variotii 10(6.2) 1.3 18(11.5) 1.7
Penicillium citrinum 38(23.6) 3.1 44(28.2) 4.5
P. chrysogenum 18(11.2) 2.0 7(4.5) 1.3
P. aurantiogriseum 16(9.9) 3.3 27(17.3) 2.6
Penicillium spp. 12(7.5) 1.5 9(5.8) 1.3
Rhizopus spp. 32(19.9) 2.8 14(9.0) 1.7
Sterile mycelia 15(9.3) 1.2 12(7.7) 1.3
a
Figures in parenthesis indicate the percentage of samples from which each fungus was isolated.
b
Calculated as mean incidence of each fungus in contaminated samples.
1312 S.A. Bankole et al. / Food and Chemical Toxicology 42 (2004) 1309–1314

Bankole, 1993) who described this genus as the most
frequent on unshelled melon seeds in stores. Of all the
fungi isolated only B. theobromae, Fusarium sp. and M.
phaseolina were found on freshly harvested sundried
melon seeds, suggesting most of the fungi found on
marketed seeds aroused through careless handling. It is
therefore not surprising that majority of the fungi
recovered in this study are those contaminating other
Nigerian food products displayed for sale in the markets
(Atanda et al., 1990; Bankole and Adebanjo, 2003b).
The results presented in Table 3 shows that aflatoxin
B1 was detected at levels greater than 5 lg/kg in 32.2%
of the 317 melon seed samples analyzed (35.4% in the
forest and 28.8% in the savanna). The percentage of
samples with detectable levels of aflatoxin was 33.7% in
the villages (35.0% in the forest and 32.6% in the sa-
vanna) and 30.5% in the towns (35.8% in the forest and
24.3% in the savanna). The percentage aflatoxin con-
tamination was not significantly different between the
pooled data for the villages and towns, though the
incidence of contamination was significantly higher in
the villages than those from towns for the savanna.
Aflatoxin B1 was above the maximum residue limit of 20
lg/kg permitted in Nigerian foods in 3.5% of samples
(4.3% in the forest and 2.6% in the savanna). For the
pooled data, the percentage of samples with aflatoxin B1
above the Nigerian regulatory limit was 2.5% in the
villages and 0.9% in the towns. The results indicated that

Table 3
Distribution of aflatoxin B1 in marketed melon seeds from the rain forest and Northern guinea savanna of Nigeria
State No of samples Number of samples with aflatoxin B1 (lg/kg)
analysed <5 5 to <10 10 to <15 15 to 20 >20
Forest
Ogun Villages 32 23 3 4 – 2
Towns 28 20 2 3 3 –
Oyo Villages 26 16 6 2 – 2
Towns 29 22 – 4 2 1
Osun Villages 22 13 4 2 2 1
Towns 24 10 6 4 3 1

Savanna
Kaduna Villages 35 26 4 2 3 –
Towns 26 20 2 3 1
Niger Villages 28 17 5 3 2 1
Towns 25 20 1 2 2 –
Bauchi Villages 23 15 3 1 2 2
Towns 19 13 2 2 1 1

Table 4
Incidence and levels of aflatoxin B1 in marketed melon seeds from the rain forest and Northern guinea savanna of Nigeria
State Total no of samples analysed No of AFB +ve Samples Levels of aflatoxin B1 (lg/kg)
Maximum Mean ± sd
Forest
Ogun Villages 32 9 36 14.9 ± 6.7
Towns 28 8 18 13.1 ± 2.9
Oyo Villages 26 10 50 14.2 ± 7.6
Towns 29 7 23 15.4 ± 4.3
Osun Villages 22 9 26 13.6 ± 4.7
Towns 24 14 26 12.4 ± 5.4

Savanna
Kaduna Villages 35 9 16 11.4 ± 2.6
Towns 26 6 15 11.3 ± 2.4
Niger Villages 28 11 25 12.3 ± 5.1
Towns 25 5 17 12.0 ± 2.3
Bauchi Villages 23 8 30 15.4 ± 5.6
Towns 19 6 28 14.3 ± 5.2
sd––standard deviation.
 S.A. Bankole et al. / Food and Chemical Toxicology 42 (2004) 1309–1314
10.7%, 10.1% and 6.6% had aflatoxin B1 in the range 5
to <10, 10 to <15, and 15 to <20 lg/kg.
The median aflatoxin B1 in the pooled 317 samples
was less than 5 lg/kg, while the median levels for villages
and towns in each zone was also less than 5 lg/kg. The
maximum levels of aflatoxin B1 ranged from 18 to 50 lg/
kg in the forest, and 15–30 lg/kg in the savanna (Table
4). The mean aflatoxin B1 ranged from 12.1 to 15.4
lg/kg in the forest and 11.4 to 13.0 lg/kg in the savanna.
The mean aflatoxin B1 of the pooled samples was
14.1 and 13.0 lg/kg in the forest and savanna, respec-
tively.
There was a significant positive correlation between
levels of diseased seeds and aflatoxin B1 in the forest
(r ¼ 0:62) and the savanna (r ¼ 0:78). This indicates
that the extent of seed deterioration could indicate the
probability of aflatoxin contamination in marketed
melon seeds. The higher aflatoxin levels in samples in the
forest reflect differences in the climatic conditions in the
two areas, the higher incidence of diseased seeds and
the somewhat higher moisture contents.
Though storage fungi particularly A. flavus occurred
at very high levels in the market melon seeds surveyed in
this study, however, the incidence and levels of aflatoxin
were lower than those of other Nigerian food products
displayed for sales in markets such as kulikuli (Akano
and Atanda, 1990), tiger nut (Bankole and Eseigbe,
1996) and dried plantain chips (Bankole and Adebanjo,
2003b). This agrees with an earlier report in which A.
flavus constituted 60% of total fungi isolated from melon
ball snacks, but aflatoxin contamination was actually
detected in only 11% of samples (Bankole, 1995).
However, the fact that 32.2% of the samples contained
aflatoxin above the Codex limit and that melon seeds is
produced solely for human consumption means that
steps must be taken to find out ways by which the
contamination levels can be minimized. This is particu-
larly so, because the increasing awareness of the haz-
ardous effect of aflatoxin may lead to reduction in the
current tolerance level in Nigerian foodstuffs.
Acknowledgements
This work was supported by the International
Foundation for Science, Stockholm, Sweden and the
Standing Committee on Scientific and Technological
Cooperation of the Organisation of Islamic Conference,
Islamabad, Pakistan through a grant (E/2978-1) to Dr
S.A. Bankole.
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