Food Control 70 (2016) 191e200

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Food Control
journal homepage: www.elsevier.com/locate/foodcont

Aflatoxins and fumonisins in rice and maize staple cereals in Northern

Vietnam and dietary exposure in different ethnic groups
Bui Thi Mai Huong a, b, Le Danh Tuyen b, Tran Thanh Do b, Henry Madsen a, Leon Brimer a,
Anders Dalsgaard a, *
a
Department of Veterinary Disease Biology, Faculty of Health and Medical Sciences, University of Copenhagen, DK-1870 Frederiksberg C, Copenhagen,
Denmark
b
National Institute of Nutrition, 48 Tang Bat Ho Street, Hanoi, Vietnam

a r t i c l e i n f o a b s t r a c t

Article history: Mycotoxins in food are increasingly a food safety hazard concern in particular in developing countries.
Received 4 January 2016 This study was performed to determine the occurrence and determinants of aflatoxin and fumonisin
Received in revised form contamination in rice and maize and to assess health risks through dietary intake exposure among ethnic
24 May 2016
minority groups in northern Vietnam. A total of 111 rice and 102 maize samples, were tested for
Accepted 29 May 2016
Available online 30 May 2016
occurrence of fungi and mycotoxins, i.e. aflatoxins (AF’s) and fuminisin B (FB). Results showed that 107
(96.4%) rice and 84 (82.4%) maize samples were contaminated by fungi. Aspergillus flavus was found in 68
(61.3%) rice and 30 (29.4%) maize samples, Aspergilus parasiticus in 40 (36.0%) rice and 27 (26.7%) maize
Keywords:
Aspergilus
samples. AF’s - were detected in 27 rice (24.3%) and 27 maize samples (26.4%) at minimum and
Fusarium maximum levels in rice of 2.06 and 77.8 ng/g and 20.5 and 110 ng/g in maize, respectively. Nine (8.1%)
Mycotoxins rice and 24 (23.5%) maize samples contained FB at ranges of 2.3e624 ng/g in rice and 5.6e89.8 ng/g in
Ethnic minority groups maize. Data collected through interviews and observations in households showed that type of crop,
Vietnam storage duration and presence of fungi, particularly mycotoxigenic fungi were important risk factors for
Liver cancer risk AF’s and FB contamination. Based on daily food consumption data, the estimated average exposure dose
of aflatoxin B1(AFB1) from rice was 21.7 ng/kg bw/day for adults and 33.7 ng/kg bw/day for children. For
FB, the rice based average exposure amounted to 536 ng/kg bw/day for adults and 1019 ng/kg bw/day for
children. The calculated excess risk of liver cancer incidence by ingestion of cereals containing AFB1 was
1.5 per 100,000 adults and 2.3 per 100,000 children per year. The average intake of FB was calculated to
be lower than the tolerable diet intake (TDI). Our findings highlight that rice and maize are contaminated
with mycotoxins at levels representing actual health hazards for the ethnic minority groups consuming
these stable cereals. Proper drying and storage conditions in households are likely to reduce the
mycotoxin contamination.
© 2016 Published by Elsevier Ltd.

1. Introduction
Rice (Oryza sativa L.) and maize (Zea mays L.) are two of the most
consumed staple foods worldwide (Kennedy, 2002). Rice contrib-
utes worldwide with 20% of total consumed staple food and 40% of
energy intake (Latham & Routledge, 1998). The Asian and Pacific
regions produce and consume about 90% of the world rice and in
* Corresponding author. Department of Veterinary Disease Biology, Groenne-
gaardsvej 15, Faculty of Health and Medical Sciences, University of Copenhagen, DK-
1870 Frederiksberg C, Copenhagen, Denmark.
E-mail address: adal@sund.ku.dk (A. Dalsgaard).
several countries, rice contributes with 40e80% of the food energy
and protein requirements (Singh, Woodheadb, & Papademetriouc,
2002). Asia contributes about one-third of the world’s total maize
production and maize is the second most important cereal crop
after rice in this region. Vietnam is among the world’s top five rice
producers and consumers (USDA, 2015) and maize is often a sub-
stitute in rural and mountainous areas, especially during periods of
rice shortage.
A nutritional surveillance (NIN, 2011) showed that the diet of
people in our study area in North West Vietnam is less diverse than
in the rest of the country. The different ethnic groups inhabiting
this area are all subsistence farmers and most of their daily food

http://dx.doi.org/10.1016/j.foodcont.2016.05.052
0956-7135/© 2016 Published by Elsevier Ltd.
192 B.T.M. Huong et al. / Food Control 70 (2016) 191e200
intake comes from maize and rice with some ethnic groups having
maize as their preferred stable crop (Thanh Ha et al., 2004, p. 42).
Thus, any hazardous substances in these stable cereals would
represent major food safety and health risks. The farmers in the
Northern highlands face different climate conditions, e.g. elevated
temperatures and higher relative humidity as compared to most
other parts of Vietnam (Pandey, Khiem, Waibel, & Thien, 2006).
Furthermore, possible different agricultural practices including
means of storage and drying harvested cereals, may provide the
basis for differences in fungal infestation and associated food safety
hazards as compared to those faced by low-land Vietnamese
farmers.
Rice and maize are reported as good substrates for fungal
growth and production of mycotoxins (Reddy, 2009; Reddy, Saritha,
Reddy, & Muralidharan, 2009; Trung, 2008) such as aflatoxins
(Reddy et al., 2009; Shephard, 2008) and fumonisins (Domijan,
Peraica, Jurjevic, Ivic, & Cvjetkovic, 2005; Nikiema, Worrillow,
Traore, Wild, & Turner, 2004). Aspergillus flavus shows optimal
production of aflatoxins at 28
C and 8e12% moisture content
whereas Fusarium verticillioides produce high levels of fumonisins
at temperatures between 20 and 26
C (Folcher et al., 2010; JECFA,
2002; Scott, 1993;; Reid et al., 1999) with toxin often produced pre-
harvest when cereals are stored in the field (JECFA, 2002). The
growth of fungi and their toxin production is increased by insect
damage and post-harvest storage conditions (FAO, 1989).
According to the Food and Agricultural Organization (FAO), 25%
of the world’s food crops may be affected by mycotoxins each year
(Boutrif & Canet, 1998). Amongst the known mycotoxins, aflatoxins,
deoxynivalenol and fumonisins pose the greatest threat to human
health worldwide (Reddy, 2009). The main producers of aflatoxins
are the fungi Aspergillus flavus and A. parasiticus (FAO, 1989). The
International Agency for Research of Cancer (IARC) has classified
aflatoxin B1 and natural mixtures of aflatoxins as group 1 carcino-
gens. IARC has further classified mycotoxins derived by
F. verticillioides which mainly are the fumonisins and fusarin C in
the group 2B as carcinogenic in animals and possibly also in
humans (IARC, 1993). The fumonisins are a group of chemically
related mycotoxins mainly produced by F. verticillioides (formely
Fusarium moniliforme). Fumonisins are mainly found in maize, but
has also been reported in rice products (Richard, 2007). Previous
surveys on mycotoxins in foods in Vietnam are few and with small
sample sizes, but they do indicate that aflatoxins are common in
maize kernel and maize flour at retail markets in Hanoi (Wang
et al., 1995). AFB1 was found in 10/15 (77%) of maize samples for
human consumption coming from different parts of Vietnam with
concentrations ranging from 11.3 ng to 126.5 ng/g dry weight while
fumonisins were found in 8/25 (32%) samples ranging from 400 to
3300 ng/g (Trung, 2008). Little is known about the occurrence of
mycotoxins in stable cereals (rice and maize) produced and
consumed by people in the rural and mountainous areas of
Northern Vietnam. The Vietnamese standards for maximum con-
tent of total aflatoxin and aflatoxin B1 are 10 mg/kg and 5 mg/kg
(Ministry of Health, 2011) as compared to the US standard of 20 mg/
kg for any type of food for human consumption (Food Safety Watch,
2013). The EU has lower maximum levels of 10 mg/kg for total
aflatoxin in ready-to-eat rice and corn products and as low as
0.1 mg/kg for processed cereal-based baby and infant food (EU,
2010). Both aflatoxins and fumonisins are resistant to processing
resulting in a high retention of those mycotoxins in consumed food
(Scott, 1993). WHO recently reported a much higher burden of
exposure of aflatoxin and fumonisin in low-income regions and
also identified priority issues that needed immediately action that
is quantifying human health impacts and burden of disease due to
the exposure of the mycotoxins and compiling an intervention
strategy to control mycotoxins (Strosnider et al., 2006).
The hypothesis of the study was that exposure to and health
risks caused by mycotoxins in staple cereals would be different
between ethnic groups as well as to farmers in other parts of
Vietnam due to the different climatic conditions and agricultural
practices. Thus, our study aimed to determine the occurrence and
determinants of aflatoxins and fumonisins contamination in rice
and maize and assess health risks through dietary intake exposures
among ethnic groups in Northern Vietnam.
2. Materials and methods
2.1. Study site and population
The study was conducted in Ta Phoi and Hop Thanh communes
in the mountainous province of Lao Cai, Northern Vietnam. These
are the poorest communes in Lao Cai district with 40% of house-
holds having monthly incomes less than 200,000 Vietnamese Dong
(approximately 10 USD per person). Households were mostly
located in highland villages and members represented seven ethnic
groups, i.e. Dao (18 households), Giay (21), Xapho (20), Tay (18), and
Hmong (20) with few Chinese households living there as well
(Department of Health Lao Cai district, 2008; Rheinla €nder,
Samuelsen, Dalsgaard, & Konradsen, 2010) (Table 1).
The Giay and Tay ethnic groups live in the lowland about one km
away from the center of Hop Thanh commune and typically grow
two rice crops per year (Department of Health Lao Cai district,
2008; Rheinla €nder et al., 2010). In addition, the Giay cultivates
two maize crops while one maize crop is produced by the Tay’s
annually. The Xapho people reside in a highland area of Hop Thanh
commune and grow two rice crops and one maize crop every year.
The Dao and Hmong people live in highland areas of Ta Phoi
commune. The Dao village is located five km from the commune
center and inhabitants grow one rice crop and one maize crop per
year. Compared with the other ethnic groups, the mountainous
Hmong village is the most isolated and least developed with only
one maize crop grown annually as the main staple food. The ethnic
Vietnamese Kinh group lives in quite developed households in a
lowland village in Ta Phoi commune and has a comparable higher
income. In contrast to the other ethnic groups which are almost
entirely subsistence farmers, the husbands of Kinh households
typically work in the local apatite mines and wives take care of
household matters. Most Kinh households buy rice and maize at
local markets whereas the other ethnic groups in general are self-
supplied with home grown rice and maize (Department of Health
Lao Cai district, 2008; Rheinla€nder et al., 2010).
The mean annual temperature is around 20e29
C, annual
rainfall about 1400e1700 mm and the average humidity above 80%.
2.2. Collection of maize and rice samples
A total of 213 samples of dried maize seed and rice were
randomly collected from separate purchased batches in October
2009 (Table 1). The samples were collected from three sources:
wholesale, retail and household. The “wholesale samples” repre-
sent samples purchased at the Coc Leu market, the largest whole-
sale market in Lao Cai city. Samples purchased at local markets in Ta
Phoi and Hop Thanh communes were catalogued as “retail sam-
ples”. The “household samples” were collected during visits to in-
dividual households. Only one rice and/or maize sample were
collected from each individual household. Samples were collected
from all stands in operation at the wholesale market and retail
(local) markets. This sampling strategy was chosen to obtain
adequate and representative sample numbers for analysis. Simi-
larly, we collected samples from all households in a particular
commune with children less than 5 years old resulting in different
 B.T.M. Huong et al. / Food Control 70 (2016) 191e200 193

Table 1
Characteristics of rice and maize samples collected for fungi and mycotoxins analyses from ethnic households in two communes in Lao Cai province, Northern Vietnam.

Source Commune Village Ethnic group Number of sample Remarks

Rice Maize

Wholesale 8 2
Retail Hop Thanh 6 0
Ta Phoi 6 0
Household Hop Thanh Kip Tuoc Giay 21 16 Self supplied
Nam Ria Xa pho 16 20 Self supplied
Peng Tay 17 18 Self supplied
Ta Phoi Peng Dao 18 17 Self supplied
Tram Thai Kinh 19 9 Purchased at markets and self supplied
Lap May Kinh
U xi xung Hmong 20 0 Self supplied
Total 111 102

Table 2
Storage conditions of maize and rice samples among different ethnic groups in Lao Cai province, Vietnam.

Crop Source Ethnic N Container Storage place Storage condition No of insect

group positive samples
Closed Open Separate Roof Shelf Floor Mean ± SEM of Mean ± SEM of Mean ± SEM of storage
storage moisture content (%) temperature of samples duration (days)


( C)

Rice Retail or 20 1 19 0 0 0 20 10.9 ± 0.24 25.2 ± 0.34 7 ± 0.6 0

whole sale
Household Dao 18 12 6 0 0 0 18 14.3 ± 0.35 20.9 ± 0.22 10 ± 2.1 0
Giay 21 4 17 0 0 2 19 12.3 ± 0.38 26.5 ± 0.18 5 ± 0.8 0
Kinha 19 8 11 0 0 0 19 14.5 ± 0.36 25.0 ± 0.21 12 ± 2.0 0
Tay 17 2 15 0 2 0 15 23.3 ± 0.31 26.1 ± 0.16 21 ± 5.2 0
Xa pho 16 2 14 3 0 4 12 12.9 ± 0.12 26.5 ± 0.12 7 ± 1.8 0
Total 111 29 82 0 2 6 103 14.5 ± 0.28 25.1 ± 0.20 10 ± 2.9 0
Maize Retail or 2 0 2 0 0 0 2 8.6 ± 0.18 27.6 ± 0.32 90 ± 3.2 0
whole sale
Household Dao 17 0 17 0 16 0 1 14.7 ± 0.48 22.3 ± 0.21 95 ± 3.3 2
Giay 16 0 16 0 1 0 15 12.0 ± 0.58 26.2 ± 0.30 80 ± 7.6 2
Hmong 20 0 20 0 3 3 14 15.8 ± 0.67 24.6 ± 0.23 45 ± 10.2 0
Kinha 9 2 7 0 0 0 9 12.0 ± 0.71 25.0 ± 0.28 71 ± 10.3 2
Tay 18 1 17 0 3 1 14 11.7 ± 0.6 26.7 ± 0.22 88 ± 4.6 1
Xa pho 20 0 20 3 0 3 14 16.6 ± 0.62 27.3 ± 0.24 45 ± 7.8 2
Total 102 3 99 6 23 7 69 14.0 ± 0.52 25.5 ± 0.26 70 ± 6.4 9
a
Most samples purchased.

sample numbers from the different sources (Table 2). Means of
storage were different between and within ethnic groups and
households, e.g. not all means of storage were practiced by a
particular type of household (Table 2).
Samples of approximately 1 kg were obtained after a thorough
mixing from the different storage units used by the wholesalers,
retailers and households; including plastic and wooden containers,
bamboo baskets, cloth sacks, and plastic bags. Samples were
collected using disposable gloves and placed in sealed sterile plastic
bags which were encoded and stored at 20
C for a maximum of
five days before transport to the laboratory at the National Institute
of Nutrition in Hanoi. Here, samples were divided into five sub-
samples for examination of the appearance of insects, moisture
content analysis, fungi enumeration and mycotoxins detection,
respectively, the fifth being stocked.
During sampling, a simple check-list and questionnaire was
applied to collect information that could potentially be associated
with presence of fungi and mycotoxins. The collected data included
time and condition of storage as well as type of storage container.
Storage time was calculated as the number of days from the day the
cereal was husked to the day of sampling. Storage conditions
included information on the storage location, e.g. in separate stor-
age containers, on the roof, on a shelf or a platform and on the floor.
It was also noted whether the type of storage container was an
open or a closed container.
2.3. Determination of temperature and moisture content
The temperature of samples was measured in the original
storage container before sampling using a digital thermometer
(Hana Instrument, Germany). The moisture content was measured
by drying 10.0 g in an oven at 105
C for 17 h (Miren, Sonia, &
Vicente, 2008).
2.4. Identification and enumeration of fungi
Level of fungi contamination was assessed following a proce-
dure recommended by the US Food and Drug Administration (FDA,
2001). Briefly, 10 g of homogenized sample was suspended in
100 ml of 1% sterile agar water (Merck, Germany) at 45
C and used
to prepare a 10-fold serial dilution. Each dilution was added to
Dichloran Glycerol (DG 18) agar in duplicate (Merck, Germany) by
the pour plate method and allowed to solidify before incubation at
25
C in the dark for six days when colonies were enumerated. The
appropriate dilution factor was determined as plates that contained
10e30 colonies, and results expressed as colony forming units per
gram (cfu/g) of sample.
Presumptive fungi isolates were sub-cultured and purified on
potato dextrose agar to identify single spores of aflatoxin-
producing and fumonisin-producing fungi (FDA, 2001). Both
macroscopic characteristics of the colonies as well as
194 B.T.M. Huong et al. / Food Control 70 (2016) 191e200
morphological characteristics (Microscope Olympus, Japan) were
used for identification (Samson, , Hoekstra, , and Frisvad, , & eds.,
2004).
2.5. ELISA detection of mycotoxins
Direct competitive ELISA-based methods using AFB1 and FB1
standards and commercially available detection kits (AgraQuant®,
Romer, USA) was used for total aflatoxins (AFB1 þ B2 þ G1 þ G2;
AFT) (limit of detection is 1 ng/g) and FB1 (limit of detection is
0.25 mg/g) analyses according to manufacturer’s instructions.
Briefly, mycotoxins extraction was performed by blending 20 g of
ground rice or maize in 100 ml methanol: water (70:30 v/v) for
2 min. The suspension was centrifuged for 10 min at 4000 rpm. The
supernatant was collected for toxin detection. Optical density was
measured using a microtiter plate reader (Bio-Rad Plate Reader,
Bio-Rad, Hercules, CA, USA). The concentration of AFT and FB was
calculated on a dry weight basis according to the specifications of
the manufacturer. For each sample, one extract was produced then
duplicate determinations of the toxin were performed. Standard
curves were plotted using standard AFT (y ¼ 0.0183x þ 0.2719;
R2 ¼ 0.9868) and FB1 (y ¼ 0.54720.6321; R2 ¼ 0.9899). The pre-
cision of the two assays was tested by analyzing in duplicate four
different concentrations of aflatoxin (1, 2, 4 and 8 ng/g) and
fumonisins (0.25, 1, 2.5 and 5 mg/g). The experimental recovery
values (%) were 104.7 ± 6.7, 98.7 ± 3.3, 101.8 ± 2.0 and 99.8 ± 0.9 for
aflatoxin, respectively and 104.0 ± 2.8, 99.0 ± 4.9, 101.0 ± 4.1 and
102.0 ± 1.8 for fumonisins, respectively.
2.6. Dietary intake of study population
Data on maize and rice dietary intake were collected and esti-
mated to allow an assessment of the dietary exposure to aflatoxins
and fumonisins when household members consumed these ce-
reals. The consumptions of rice and maize by adults and children
were done in two separate ways: 1) consumption of rice and maize
by adults were extracted from a food consumption data set of adults
living in Lao Cai city collected in the first week of October 2009 by
the National Institute of Nutrition, Hanoi as part of a National
Survey on Food Consumption (National Institute of Nutrition, 2011)
and 2) the amounts of maize and rice consumed by children less
than five years of age were calculated based on information
collected from 24-hrs recall food intake interviews conducted by
our research group on three consecutive days combined with actual
weighing of the reported consumptions (EFSA, 2009; Swindale &
Vachaspati, 1999).
The national survey and our survey did collect data on dietary
intake by household interviews of the mother/grandmother on
types of dishes consumed in the last day, including information on
all ingredients used for food preparation. Supporting tools such as
spoon, table spoon, bowl, and cups were used to activate the
household member’s memory and to allow subsequent weighing of
the foods. Accordingly, the interviewer was instructed to weigh
available foods for confirming weight stated by household mem-
bers using an electronic scale.
2.7. Assessment of dietary exposure
The dietary exposure to a mycotoxin is determined by myco-
toxin contamination level (ng/g food) in the food consumed, the
actual amount of this food eaten per day (g food/day) and the in-
dividual’s body weight (kg bw). The value of body weight of adults
was assigned as 49 kg, equal to the average body weight of adults
living in north-east Vietnam (National Institute of Nutrition, 2007)
and 11.3 kg was estimated as the mean body weight of children
based on weights of 127 children (40 ± 12 months age) present in
households during the interviews (data not shown).
2.8. Risk assessment
Risk assessment of AFB1 was performed based on dietary
exposure to AFB1 and its potency in the induction of primary liver
cancer. Since AFB1 has been found to contribute about 60% of total
aflatoxin determined (Garrido, Hern andez Pezzani, & Pacin, 2012;
Khatoon et al., 2012; Mohamadi Sani, Azizi, & Naeejic, 2012), we
assumed that the contamination level of AFB1 was 60% of that of
total aflatoxins found by the analysis of the maize and rice samples.
The risk of liver cell cancer for the study population was assessed on
the basis of the result of the exposure data and an average potency
calculated using the prevalence of individuals being hepatitis B
surface antigen- (HbsAg) positive and having a potency of 0.3
cancers per year per 100,000 population per ng AFB1/kg body
weight (kg bw) per day and the negative individuals set to have 0.01
cancers per year per 100,000 population per ng AFB1/kg bwper day
(Liu & Wu, 2010; WHO, 1998). A previous study reported hepatitis B
positive prevalence rates in rural areas of Vietnam at 18.4± 5.0%,
20.5± 5.3% and 18.8± 3.1% in children, adolescent and adult,
respectively (David et al., 2003). Therefore, we used a
HbsAg þ prevalence rate of 20% in our risk assessment in line with
the 25% prevalence rate referred to by WHO (WHO, 1998) for
developing countries, giving an average potency for liver cell cancer
of 0.068. Population risk was obtained by multiplying dietary
exposure with average potency.
Population risk ¼ Exposure  average potency
Average potency ¼ 0:3  0:2 þ 0:01  0:8 ¼ 0:068
Fumonisin diet exposure was compared to a Tolerable daily
intake (TDI) of 2000 ng per kg bodyweight per day (JECFA, 2002).
2.9. Data analysis
Mycotoxin concentrations or presence (detected/not detected)
were related to various potential predictors one by one (uni-vari-
able) using linear regression or logistic regression, respectively
(model 1). Categorical variables were coded as indicator variables
while some continuous factors were log transformed to the base 10.
In model 2, presence of the causative agents of mycotoxins (i.e.
fungi) was tested simultaneously (multi-variable) with predictors
from model 1 using a forward stepwise selection procedure (p for
removal and inclusion were set to 0.10 and 0.05, respectively).
3. Results
3.1. Storage condition, temperature and moisture content
Only 28/91 (30.8%) of rice samples and 3/100 (3.0%) of maize
samples were stored in closed containers (Table 2). With one
exception all retailers stored cereals in open containers. Overall
maize was more often stored in open containers than rice. With
little difference among ethnic groups the vast majority of house-
hold’s stored rice (92.8%) and maize (67.6%) on the floor except the
Dao households which stored maize under the roof. The moisture
content of rice and maize samples ranged from 8.6 to 23.3%, and
with a mean of 14.5%, the lowest values were found in samples from
retail or wholesales. Temperatures measured ranged from 20.9 to
27.6
C. The mean storage duration of rice samples was 10 days
ranging from 5 to 21 days. However, maize samples were stored
much longer averaging 70 days. Damage by insects was observed in
 B.T.M. Huong et al. / Food Control 70 (2016) 191e200
nine maize samples, but not in any rice samples (Table 2).
3.2. Fungal contamination
Data on the concentration of potential toxigenic fungi are
summarized in Table 3. Amongst the 111 rice and 102 maize sam-
ples tested, 107 and 84 were found to be contaminated by fungi,
respectively. A. flavus was detected in a total of 68 and 30 rice and
maize samples, i.e. in 61.3% and 29.4%, respectively. A. parasiticus
contamination occurred in six (5.4%) rice samples and in four (3.9%)
maize samples. Fusarium verticillioides was found in 40 (36.0%) rice
samples and in 27 (26.7%) maize samples. The mean number of
fungi in rice samples was 1.57  104 with a range from 37 to
2.80  105 CFU/g. This was lower than the mean concentration
found for maize, i.e. 3.34  105 (range from 1.00  104 to
2.58  105 CFU/g).
3.3. Occurrence of mycotoxins
The occurrence and concentrations of mycotoxins are shown in
Table 4 and Fig. 1. AF’s were detected in 27 rice (24.3%) and in 27
maize samples (26.4%). Minimum and maximum levels of AFT in
rice were 2.06 and 77.8 ng/g, respectively, while the levels in maize
were 20.5 and 110 ng/g. Nine rice samples and 24 maize samples
were found to contain fumonisin B1 with concentrations in rice
ranging from 2.3 to 624 ng/g and between 5.6 and 89.8 ng/g in
maize.
3.4. Risk factors for mycotoxins
AF’s were reported in four of the 22 samples from retail or
wholesales while 54 of 191 samples from households contained
aflatoxins. The proportion of samples contaminated with myco-
toxins did not differ among the different sources of samples. Most
rice and maize samples collected in households were self-
produced, but some Kinh households reported to have purchased
their cereals from retail or wholesale dealers. All samples from
retail or wholesales as well as samples from households reported to
have been purchased from these were excluded from subsequent
data analysis. The number of samples with A. parasiticus growth
was thereby reduced to three and therefore the counts of A. flavus
and A. parasiticus were pooled.
In uni-variable analyses, model 1 (variables that could be seen as
potential risk factors for fungal growth) showed that AF concen-
trations were on average 21.26 ng/g greater in maize samples than
in rice samples (p < 0.001) and was positively associated with
storage duration [log10(days)]. A one unit increase on a log scale (a
10-fold increase in storage time in days) was associated with
19.38 ng/g higher concentration of AFT in rice (p < 0.001) while no
other factors were significant. None of the model 1 factors were
significantly associated with FB1 concentration. Presence of AF’s
(concentration >1.0 ng/g) was not associated with any of the pre-
dictors while maize had a higher risk for being contaminated with
Table 3
Potential toxigenic fungi found in rice (n ¼ 111) and maize samples (n ¼ 102).
Fungi Rice
Na (%) Mean (CFU/g)
Total counts 107 (96.4) 1.57  104
A. flavus 68 (61.3) 1.62  103
A. parasiticus 6 (5.4) 5.82  103
F. moniliforme 40 (36.0) 3.35  102
a
N is the number of samples found contaminated with fungi.
195
FB1 than rice (OR ¼ 2.45, p < 0.05) and presence of FB1 was posi-
tively associated with storage duration (OR ¼ 2.86, p < 0.01).
Presence of AF’s at concentration >10 ng/g was more likely in maize
than in rice (OR ¼ 8.34, p < 0.01) and with storage time (odds ratio
for a 10-fold increase in storage time was 8.92). Ethnic group did
not appear as a significant predictor for mycotoxins presence or
concentration. Only duration of storage, however, remained in the
multivariable model (Table 5).
In the multivariable analysis (model 2), maize, growth of
Aspergillus spp. and duration of storage were associated with higher
total concentrations of AF’s (Table 5). Only growth of Fusarium spp.
was a significant predictor of FB1 concentration (Table 5).
Looking at presence/absence of AF’s instead of concentration
(Table 5), the multivariable analysis showed that maize and growth
of Aspergillus spp. were both associated with higher odds of having
AFB1 (Table 4). In the uni-variable tests only, growth of Fusarium
spp. was significantly associated with presence of FB1, while in the
multivariable model also duration of storage was significant
(Table 5).
3.5. Dietary exposure and risk assessment
Using mean consumption levels from the national survey of
adults (National Institute of Nutrition, 2011) and similar data
collected by the lead author for children, the dietary exposure to
AFB1 and FB1 were calculated (Tables 6 and 7). The average total
AFB1 exposure from both rice and maize was estimated to 21.7 ng/
kg bw/day for the adults and associated with an average risk of
excessive liver cancer of 1.5 cases per 100,000 individual per year
while for children the exposure was estimated to 33.7 ng/kg bw/
day and associated with an average risk of 2.3 cases per 100,000
individual per year. In our study, the mean FB1 exposure level from
intake of cereals was 536 ng/kg bw/day and 1019 ng/kg bw/day
equal to 26.8% and 51.0% of TDI of adults and children, respectively.
4. Discussion
The current study showed that contamination with fungi is
common in rice (96.4%) and maize (82.4%) consumed by ethnic
minority groups in Northern Vietnam. Aspergillus flavus and Fusa-
rium verticillioides, were isolated from 61.3% and 36.0% of rice
samples, respectively while a total of about 30% of maize samples
was contaminated with either one or both of these fungi. This
supports previous findings from Vietnam (Tran, Bailly, Querin, Le
Bars, & Guerre, 2001; Trung, 2008) and in Thailand (Pitt et al.,
1994) that A. flavus and Fusarium spp. are important contami-
nants of cereals. Traditional methods of drying rice directly along
roads or on the edge of fields as practiced by the study communities
are important transmission routes for fungal spores associated with
soil dust particles (Rogge, Medeiros, & Simoneit, 2007). Maize cups
were not dried along roads, but were stored and dried within
household perimeters on floors, shelves, and roofs with the Dao
ethnic group preferring storage on the roof (Table 2).
Maize
Range (CFU/g) Na (%) Mean (CFU/g) Range (CFU/g)
3.7  10e2.8  105 84 (82.4) 3.34  105 104e2.58  106
1.0  102e1.3  104 30 (29.4) 1.43  105 3  102e2.3  106
2.10e2.8  103 4 (3.9) 7.90  104 6  103e2  105
1.0  102e2  103 27 (26.7) 4.55  104 102e1.90  105
196 B.T.M. Huong et al. / Food Control 70 (2016) 191e200

Table 4
Contamination level of mycotoxins by crops and ethnic groups.

Ethnic Crop N Number of samples contaminated above the maximum Contamination level (ng/g)
levela

Aflatoxins (>10 ng/g) Fumonisins (>1000 ng/g) Aflatoxins Fumonisins

b
Dao Rice 18 2 0 Mean 3.13 30.74
Min 19.06 182.30
Max 21.23 358.42
Maize 17 5 0 Mean 26.45 11.80
Min 21.23 5.88
Max 109.64 69.03
Giay Rice 21 0 0 Meana 1.06 31.67
Min 2.06 2.30
Max 2.21 624.48
Maize 16 6 0 Mean 33.87 1.83
Min 24.86 5.64
Max 108.19 15.01
Hmong Maize 20 3 0 Meana 11.88 11.31
Min 58.91 65.24
Max 101.67 89.79
Kinh Rice 19 5 0 Meana 12.04 NDc
Min 13.26 ND
Max 77.75 ND
Maize 9 4 0 Meana 48.00 1.64
Min 103.12 7.03
Max 110.36 7.74
Tay Rice 17 0 0 Meana 1.90 17.92
Min 3.21 140.35
Max 8.67 164.22
Maize 18 3 0 Meana 8.67 5.77
Min 103.12 5.90
Max 106.74 11.48
Xa pho Rice 16 0 0 Meana 1.00 23.02
Min 2.06 163.45
Max 3.08 193.42
Maize 20 5 0 Meana 18.46 3.90
Min 20.51 5.90
Max 103.12 28.71
Total Rice 91 7 0 Mean 3.82 69.37
Maize 100 26 0 Mean 24.51 2.44
a
Maximum level adopted by Vietnam Government (Ministry of Health, 2011).
b
Mean is less than minimum since including many negative samples.
c
Not detected.

Furthermore, long time storage and storing cereals on humid
ground floors or in kitchens at elevated temperatures, as practiced
by the ethnic minority groups, may promote growth of fungi and
development of mycotoxins (Hettiarachchi, Gooneratne &
Hirimburegama, 2001; Noomhorm & Cardona, 1989). In our
study, moisture content in rice and maize varied between 10.9% to
23.3% and 8.6%e16.6%, respectively (Table 2). Generally, it is
assumed moisture content below 12% protects against fungal
growth (Hettiarachchi et al., 2001; Noomhorm & Cardona, 1989).
However, our risk factor analysis did not find a significant associ-
ation between moisture content as well as temperature (overall
range from 20.9
C to 27.6
C) and presence and level of the my-
cotoxins in rice and maize (Table 5). In agreement with other
studies, duration of storage (rice: 7e21 days; maize: 45e95 days)
was the only parameter significantly associated with aflatoxin
concentration as well as risk for presence of mycotoxins (Table 5)
(Hettiarachchi et al., 2001; Noomhorm & Cardona, 1989). In
contrast to our study hypothesis, ethnic group did not appear as a
significant predictor for mycotoxins presence or concentration.
The occurrence of AF’s in rice and maize was about 25% (Fig. 1)
with concentrations ranging from 2.06 to 77.8 ng/g in rice and from
20.5 to 110 ng/g in maize samples (Table 4). These levels are lower
than previously reported for cereals in Vietnam (Nguyen,
Tozlovanu, Tran, & Pfohl-Leszkowiczb, 2007; Trung, 2008) and
other countries with similar climatic conditions (Reddy et al., 2009;
Sugita-Konishi et al., 2010; Wang et al., 1995). However, still many
samples including some rice samples had higher AFT concentra-
tions than allowed in most developed countries and certainly much
higher than the maximum value (4 mg/kg) set by the EU (EU, 2010).
Fumonisin was found in 8.1% of rice samples and 23.5% of maize
samples (Fig. 1) showing mean concentrations from 2.3 to 624 in
rice and from 5.6 to 89.8 ng/g in maize (Table 4). Our results show a
lower prevalence of fumonisin contamination in the cereals but a
higher concentration of the toxin as compared with previous re-
ports from Vietnam and other Southeast Asian countries (Wang
et al., 1995; Yamashita et al., 1995; Yoshizawa, Yamashita, &
Chokethaworn, 1996). Amongst ethnic groups, Kinh adults were
observed to have the highest exposure to AFB1 through consump-
tion of both rice and maize with a mean level of 63.6 ng/kg bw/day
while this was 7.6 ng/kg bw/day among Xapho people. The expo-
sure of the other ethnic groups ranged from 10.2 ng/kg bw/day to
18.8 ng/kg bw/day. Furthermore it should be noted, that apart from
assigning samples showing analytical results less than the limit of
detection to non-detects, a lower bound could have been used to
estimate the dietary exposure giving rise to a higher total result. In
China, total aflatoxin dietary exposure was estimated at
11.7e2027 ng/kg bw/day, from a diet in which rice contribute with
about 30% of recommended energy intake (Kenny, 2001), and in
Thailand at 6.5e53 ng/kg bw/day (Williams et al., 2004). Similarly,
Sugita-Konishi et al. (2010) stated based on analysis of relative few
rice samples from Korea that the level of AFB1 contamination in rice
in several Asian countries could be a serious food safety problem,
 B.T.M. Huong et al. / Food Control 70 (2016) 191e200 197

Fig. 1. Distribution of mycotoxins found in rice (n ¼ 111) and maize samples (n ¼ 102).

Table 5
Risk factor analysis for concentration and occurrence of mycotoxins (aflatoxin or fuminosin) in rice and maize samples. Factors were tested one at the time (univariable) or all
together in a forward stepwise selection procedure (multivariable).

Factors Regression coefficient (ng/g) Exponentiated regression coefficient (odds ratio)

Aflatoxin Fuminosin Aflatoxin present Fumonisin present Aflatoxin

concentration concentration (conc>10 ng/g)

Uni Multi Uni Multi Uni Multi Uni Multi Uni Multi

Model 1 variables
Commune ns ns ns ns ns
Village ns ns ns ns ns
Ethnic group ns ns ns ns ns
Crop (rice the base group) 21.26c ns ns 2.45a 8.34b
Type of container ns ns ns ns ns
Storage place ns ns ns ns ns
Moisture content (%) ns ns ns ns ns
Temperature (
C) ns ns ns ns ns
Storage duration (log10[days]) 19.38c 19.38c ns ns 2.86b 2.86b 8.92c 8.92c
Insect damage ns ns ns ns ns
Model 2 variables (including also some variables from model 1)
Fungi presence ns ns ns ns ns
Aspergillus spp. presence 25.31c 42.33c ns 55.94 194.37c ns 20.60c 182.60c
b
Fusarium presence ns 1.92 17.89a 17.89 a
ns 15.46c 24.27 c
ns
Crop (rice the base group) 21.26 28.95c ns ns 8.00b 2.45 8.34b 92.10c
Storage duration (log10[days]) 19.38 9.85a ns ns 2.86 4.86c 8.92c
a
,p < 0.05; b, p < 0.01; c, p < 0.001; ns, not significant; uni, uni-variable; multi, multi-variable.

except in Japan where a three year survey demonstrated levels of
aflatoxins lower than limit of detection in rice, rice ball, maize and
maize products (Sugita-Konishi et al., 2010).
Based on available toxicity data, the Joint FAO/WHO Expert
Committee on Food Additives set a group TDI for fumonisins (B1
and its analogues B2 and B3), which are considered to be associated
with a range of toxic syndromes, at 2 mg per kg body weight per day
(JECFA, 2002). The intake of FB1 was different amongst ethnic
groups, of which the highest exposure was found in the Giay
(245.1 ng/kg bw/day) almost entirely originating from rice con-
sumption (244.6 ng/kg bw/day) whereas the lowest estimated
exposure was for the Tay group (140.0 ng/kg bw/day) (Table 6).
It is well recognized that children in particular are vulnerable to
foodborne hazards due to their higher food consumption per kg
body weight and differences in physiology compared to adults. Due
to significant postnatal development of different organ systems
during childhood, children are more sensitive to some neurotoxic,
endocrine and immunological effects up to four years of age (Boon,
Bakker, Van Klaveren & Van Rossum, 2009). We therefore esti-
mated the exposure of children to AFB1 and FB1 separately. Since
maize was not fed to children in the study population, toxin
exposure level of children was only estimated using the data on rice
consumption (Table 7). The mean consumption of children was
166.0 g rice/day. Kinh children consumed the highest amount with
198 B.T.M. Huong et al. / Food Control 70 (2016) 191e200

Table 6
Mycotoxins exposure assessment and risk characterization by crop and ethnic group e assumed adult body weight is 49 kg; population risk is calculated on the assumption of
HbsAg þ prevalence 20% (WHO 1998) and mean level of the mycotoxins contamination of all samples.

Ethnic Crop Mean of consumption (g/day) Aflatoxin B1a Fumonisins

Contamination Exposure (ng/kg bw/day) Riskb Contamination Exposure (ng/kg bw/day)

level (ng g) level (ng/g)

Dao Rice 378.5 Meanc 1.9 14.5 1.0 Meanc 30.7 237.5
Min 11.4 88.3 6.0 Min 182.3 1408.2
Max 12.7 98.4 6.7 Max 358.4 2768.6
Maize 13.3 Mean 15.9 4.3 0.3 Mean 11.8 3.2
Min 12.7 3.5 0.2 Min 5.9 1.6
Max 65.8 17.9 1.2 Max 69.0 18.7
Both crops 391.8 Meanc 17.7 18.8 1.3 Meanc 42.5 240.7
Min 24.2 91.8 6.2 Min 188.2 1504.7
Max 78.5 116.3 7.9 Max 427.5 3417.9
Giay Rice 378.5 Meanc 0.6 4.9 0.3 Mean 31.7 244.6
Min 1.2 9.5 0.6 Min 2.5 17.8
Max 1.3 10.2 0.7 Max 624.5 4823.8
Maize 13.3 Mean 20.3 5.5 0.4 Meanc 1.8 0.5
Min 14.9 4.0 0.3 Min 5.6 1.5
Max 64.9 17.6 1.2 Max 15.0 4.1
Both crops 391.8 Mean 21.0 10.4 0.7 Meanc 33.5 245.1
Min 16.2 13.6 0.9 Min 7.9 63.5
Max 66.2 27.9 1.9 Max 639.5 5113.3
Hmong Maize 166.4 Meanc 7.1 24.2 1.6 Meanc 11.3 38.4
Min 35.3 120.0 8.2 Min 65.2 221.5
Max 61.0 207.2 14.1 Max 89.8 304.9
Kinh Rice 378.5 Meanc 7.2 55.8 3.8 Mean NDd e
Min 8.0 61.5 4.2 Min ND e
Max 46.7 360.3 24.5 Max ND e
Maize 13.3 Meanc 28.8 7.8 0.5 Meanc 1.6 0.4
Min 61.9 16.8 1.1 Min 7.0 1.9
Max 66.2 18.0 1.2 Max 7.7 2.1
Both crops 391.8 Mean 36.0 63.6 4.3 Mean ND e
Min 69.8 78.2 5.3 Min ND e
Max 112.9 378.3 25.7 Max ND e
Tay Rice 378.5 Meanc 1.1 8.8 0.6 Meanc 17.9 138.4
Min 1.9 14.9 1.0 Min 140.4 1084.1
Max 5.2 40.2 2.7 Max 164.2 1268.5
Maize 13.3 Meanc 5.2 1.4 0.1 Meanc 5.8 1.6
Min 61.9 16.8 1.1 Min 5.9 1.6
Max 64.0 17.4 1.2 Max 11.5 3.1
Both crops 391.8 Mean 6.3 10.2 0.7 Meanc 23.7 140.0
Min 63.8 31.7 2.2 Min 146.3 1169.4
Max 69.2 57.6 3.9 Max 175.7 1404.9
Xa pho Rice 378.5 Mean 0.6 4.6 0.3 Meanc 23.0 177.8
Min 1.2 9.5 0.6 Min 163.5 1262.6
Max 1.8 14.3 1.0 Max 193.4 1494.1
Maize 13.3 Meanc 11 3.0 0.2 Meanc 3.9 1.1
Min 12 3.3 0.2 Min 5.9 1.6
Max 62 16.8 1.1 Max 28.7 7.8
Both crops 391.8 Meanc 12 7.6 0.5 Meanc 26.9 178.9
Min 14 12.9 0.9 Min 169.4 1354.1
Max 64 31.1 2.1 Max 222.1 1776.1
Total Rice 378.5 Mean 2 17.7 1.2 Mean 69.4 535.8
Maize 13.3 Mean 15 4.0 0.3 Mean 2.4 0.7
Both crops 391.8 Mean 17 21.7 1.5 Mean 71.8 536.5
a
Assumed aflatoxin B1 concentration contributes about 60% of total aflatoxins detected in samples.
b
Liver cancer cases per 100,000 population per year.
c
Mean is less than minimum since including many negative samples.
d
Not detected.

about 179 g/day, followed by Giay (171 g/day), Tay (167 g/day), Dao
(164 g/day), and Xa pho (155 g/day). Hence, similar to Kinh adults,
Kinh children were exposured to a high level of AFB1 from rice
(114.4 ng/kg bw/day). The lowest exposure to AFB1 was found in Xa
pho children with a level of 8.2 ng/kg bw/day (Table 7). The mean
AFB1 exposure amongst all children was 33.7 ng/kg bw/day. The FB1
intake level of children from rice consumption was much higher
than in adults with a mean of 1019 ng/day; ranging from 34.8 to
9455.6 ng/day (Table 7).
Since AFB1 is the most abundant of the aflatoxins analogues and
also the most biologically active, the European Food Safety
Authority has approved to use data on AFB1 exposure for health risk
assessments (EFSA, 2007). The assessment of health risk associated
with consumption of rice and maize contaminated with aflatoxins
showed that adults (4.3 cases per 100,000 individuals per year) and
children (7.8 cases per 100,000 individuals per year) of the Kinh
ethnic group experienced the highest risk of liver cancer in com-
parison with the other ethnic groups. In comparison, the mean
excess cancer risk for all ethnic groups was calculated as 1.5 cases
for adults and 2.3 cases for children per 100,000 individuals per
year (Tables 6 and 7). Only few data on liver cancer risk estimation
are published from Asian countries with rice as the main staple
 B.T.M. Huong et al. / Food Control 70 (2016) 191e200 199

Table 7
Mycotoxins exposure assessment and risk characterization by crop and ethnic group e assumed child body weight is 11.3 kg; population risk is calculated on the assumption of
HbsAg þ prevalence 20% (WHO 1998) and mean level of the mycotoxins contamination of all samples.

Ethnic Mean of consumption (g/day) Aflatoxin B1a Fumonisins

Contamination Exposure (ng/kg bw/day) Riskb Contamination Exposure (ng/kg bw/day)

level (ng/g) level (ng/g)

Dao 164.1 Mean 1.9 27.2 1.9 Meanc 30.7 446.4

Minc 11.4 166.1 11.3 Min 182.3 2647.4
Max 12.7 185.0 12.6 Max 358.4 5205.0
Giay 171.1 Mean 0.6 9.6 0.7 Mean 31.7 479.6
Min 1.2 18.7 1.3 Min 2.3 34.8
Max 1.3 20.1 1.4 Max 624.5 9455.6
Kinh 178.9 Meanc 7.2 114.4 7.8 Mean NDd e
Min 8.0 126.0 8.6 Min ND e
Max 46.7 738.6 50.2 Max ND e
Tay 167.4 Meanc 1.1 16.9 1.1 Meanc 17.9 265.5
Min 1.9 28.5 1.9 Min 140.4 2079.2
Max 5.2 77.1 5.2 Max 164.2 2432.8
Xa pho 154.6 Meanc 0.6 8.2 0.6 Meanc 23.0 314.9
Min 1.2 16.9 1.1 Min 163.5 2236.2
Max 1.8 25.3 1.7 Max 193.4 2646.3
Total 166 Mean 2.3 33.7 2.3 Mean 69.4 1019.1
a
Assumed aflatoxin B1 concentration contributes about 60% of total aflatoxins detected in samples.
b
Liver cancer cases per 100,000 population per year.
c
Mean is less than minimum since including many negative samples.
d
Not detected.

food. An excess risk of 0.021 cases per 100,000 individuals of References

population per year was observed in Japan. There is a strong
observed synergy between AFB1 exposure and being a hepatitis B
surface antigen-positive individual, i.e. aflatoxin is about 30 times
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2009). Food safety hazards associated with fungi and their myco-
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lent with foreseen climate chances.
Acknowledgment
The study was supported by the Danish International Develop-
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