Article

Materials Express. 2023, 13, pp.316–326

Copyright © 2023 by American Scientific Publishers
All rights reserved. 2158-5849/2023/13/316/011
Printed in the United States of America doi:10.1166/mex.2023.2343

Toxic metals and aflatoxins occurrence in

smoked-dried fish and their health
risks assessment
H. Uguru1 ∗ , O. I. Akpokodje2 , A. E. Essaghah3 , Abeer M. Aljaadi4 , Rokayya Sami5 ∗ , Amani H. Aljahani6 ,
Amal Adnan Ashour7 , and Mahmoud Helal8 9
1
Department of Agricultural Engineering, Delta State University of Science and Technology, Ozoro, 1334111, Nigeria
2
Department of Civil and Water Resources Engineering, Delta State University of Science and Technology, Ozoro,
1334111, Nigeria
3
Department of Urban and Regional Planning, Delta State University of Science and Technology, Ozoro, 1334111, Nigeria
4
Clinical Nutrition Department, Faculty of Applied Medical Sciences, Umm Al-Qura University, P.O. Box 715, Makkah,
24382, Saudi Arabia
5
Department of Food Science and Nutrition, College of Sciences, Taif University, P.O. Box 11099, Taif, 21944, Saudi Arabia
6
Department of Physical Sport Science, College of Education, Princess Nourah bint Abdulrahman University, P.O. Box
84428, Riyadh, 11671, Saudi Arabia
7
Department of Oral & Maxillofacial Surgery and Diagnostic Sciences, Faculty of Dentistry, Taif University, P.O. Box 11099,
Taif, 21944, Saudi Arabia
8
Department of Mechanical Engineering, Faculty of Engineering,
IP: 197.210.84.168 On: Mon, Taif University,
10 Apr P.O. Box 11099, Taif, 21944, Saudi Arabia
2023 17:03:43
9
Production Engineering and Mechanical Copyright: American Scientific Publishers Mansoura University, P.O. Box
Design Department, Faculty of Engineering,
35516, Mansoura, Egypt Delivered by Ingenta

ABSTRACT
This study investigated the microbiological and toxic heavy metals contamination in smoked-dried fish, and
evaluates their health risk implications. Fifteen widely consumed fish species were sampled randomly, and
their aflatoxins, mercury “Hg,” cadmium “Cd” and lead “Pb” concentrations were evaluated though standard
guidelines. The results revealed that fish flesh Hg level ranged from 0.085–0.258 mg/kg, Cd concentration
ranged from 0.092–0.204 mg/kg, and Pb level varied from 0.173–0.329 mg/kg; the mean toxic metals level in
the freshwater fish tissue was lower, when compared to the levels in the saltwater fish (seafood). Regarding
toxic metal toxicity, the average Hg, Cd and Pb estimated daily intake values for children and adult were
0.1200 and 1.63 × 10−5 mg/kg bw/day, 2.13 × 10−4 and 7.57 × 10−5 mg/kg bw/day, and 2.48 × 10−4 and
1.24 × 10−4 mg/kg bw/day respectively. Likewise, children targeted hazard quotients (THQ) values were Hg
(0.585), Cd (0.151) and Pb (0.071), while adult THQ values were Hg (0.293), Cd (0.076) and Pb (0.035).
Children and adult hazard index (HI) values were 0.949 and 0.404 respectively; while Carcinogenic Risk (CR)
values indicated that Cd had higher chances of cancer risks when compared to Pb. Additionally, the aflatoxins
level in the fish species ranged from 0.564–9.422 ppb, with the seafood having lower aflatoxins level when
compared to the freshwater fish species. Aflatoxins estimated daily intakes (EDI) exposure was 4.81 × 10−3
and 2.41×10−3 g/kg bw/day for the children and adults respectively; while the aflatoxins HI value for children
was 7.300 × 10−4 , and for adults was 7.293 × 10−4 . Health risks assessment of heavy metal accumulation in
the fish, for both children and adults portrayed insignificant adverse health effects (THQ < 1), through the oral
consumption of the fishes. Aflatoxins level detected in the all fishes was within acceptable limits (10 ppb) as

∗
Authors to whom correspondence should be addressed.

316 www.aspbs.com/mex
Uguru et al. Toxic metals and aflatoxins occurrence in smoked-dried fish and their health risks assessment

approved by the World Health Organization; however, some of the values for freshwater fishes were above
the allowable limit (2 ppb) approved by the European Union. Though, the results depicted a very low risk of
toxic metals and aflatoxins poisoning, there is the need for proper evaluation of current fish processing and
storage methods to prevent human exposure to toxic metals and aflatoxins introduced through smoked-dried
fish consumption.

Keywords: Aflatoxins, Fish Tissue, Health Risk, Heavy Metals.

1. INTRODUCTION hence, toxic metals harmfulness is directly proportional

Fish is a major source of animal-based protein, preferred
by numerous people due to its lower low density lipids
content, and higher proportion of vitamins, antioxidants
content and polyunsaturated fatty acids content [1]. Fish
contains easily digestible protein with essential amino
acids which have several positive health implications.
Salvador et al. [2] reported that the essential compounds
present in fish body can help to manage severe aliments as
hypertension, liver problem, heart diseases and kidney fail-
ure. Despite the several advantages of fish consumption, it
has some negative health implications when contaminated
with pathogenic microorganisms’ and heavy metals, which
tend to accumulate in the fish flesh, bones and gills. The
rate at which poisonous substances buildup in an organ-
ism’s body is directly proportional
IP:to197.210.84.168
the organism feeding
On: Mon, 10 Aprimproper
behaviour; omnivorous animals tend to Copyright: American
accumulate
more Scientific
toxic substances than non-omnivorous animals [3]. Delivered byhumidity
Poor development planning and weak environmental
management practices have become major casual factors
of environmental pollution. Pollution resulting in accumu-
lation of heavy metals and pathogenic creatures in the
environment has become a major problem, because most
of these contaminants are virtually persistent and haz-
ardous in the environment [4]. Indiscriminate discharge
of untreated (toxic) waste materials into the environment,
causing water pollution is exacerbated by poor regional
and urban planning [5]. Additionally, Kortei et al. [4]
attributed heavy metals and microbial pollution of the
environment to leachates from poorly managed indus-
trial/domestic wastes, which is facilitated by poor urban
and regional planning. Fishery products acquire their met-
als contamination through polluted water bodies (fish’s
natural habitat), mostly from raw effluent discharges into
aquatic ecosystems [6]. Fumes from combustion of fos-
sil fuels, effluent from electronic, industrial, medical and
agricultural wastes, are major sources of heavy metal pol-
lution; hence proper regional planning and waste manage-
ment will alleviate their pollution rate [7]. Poorly planned
regions tend to have a higher degree of heavy metal
accumulation, when compared to communities with well-
planned city layouts [5].
Studies have revealed that the proportion of heavy
(toxic) metals in fish/animal tissues is directly correlated
to the toxic metals available in the aquatic ecological unit;
to the volume and concentration of pollutants (effluent)
the ecosystems received [8–10]. These elements (cadmium
“Cd,” Chromium “Cr,” arsenic “As,” lead “Pb” Cobalt
“Co” and mercury “Hg”) are considered as toxic metals,
because they don’t have known nutritional and biochem-
ical qualities, but rather their accumulation in the body,
even in minute quantities is detrimental to human health
[4]. Toxic metal poisoning tends to cause cancer, cardio-
vascular, brain, kidney, respiratory, reproductive, and neu-
rological problems in human beings, with children been
more susceptible to heavy metal toxicity [11].
Microbial infestation is the main cause of food deterio-
ration, resulting in food wastages and food insecurity. Food
usually gets contaminated with pathogenic microorganisms
through
harvesting, processing and storage oper-
2023 17:03:43
ations [12].
Warm environmental conditions, high relative
Publishers
Ingenta and high moisture content tend to favour rapid
multiplication of most fungi and bacteria contaminants
during food storage [13]. Due to poor processing and stor-
age methods in developing countries, dried fishes are often
susceptible to substantial microbial growth and spoilage
during storage and marketing operations [14]. Aflatoxins
(formed by fungi) are among the several types of myco-
toxins which are lethal to the human beings. Potent strains
of aflatoxins include: aflatoxin B1 (AFB1 ), aflatoxin B2
(AFB2 ), aflatoxin G1 (AFG1 ), and aflatoxin G2 (AFG2 );
whose trend in terms of magnitude of toxicity is as fol-
lows: AFB1 > AFG1 > AFB2 > AFB2 [15]. The M1 and
M2 flatoxins which are other potent forms of aflatox-
ins are considered as hydroxylated types of AFB1 and
AFB2 respectively [16]. According to the official web-
site portal of the International Agency for Research on
Cancer (IARC), the Aflatoxin B1 has been associated
with the formation of liver cancer, and degradation of the
body’s immune system. Others severe aliments associated
with aflatoxins include: cirrhosis, jaundice and miscarriage
[17, 18].
Fishes are preserved traditionally through the smoke-
drying technique, which significantly affects the toxicity
and microbial contamination levels. Drying inhibits micro-
bial activities in fish body, through the reduction of the
fish water activity; but it has insignificant effects on most
halophilic microorganisms and on the heavy metal con-
centrations in the fish flesh/tissue [19]. Although studies

Mater. Express, Vol. 13, pp. 316–326, 2023 317

Toxic metals and aflatoxins occurrence in smoked-dried fish and their health risks assessment Uguru et al.

have revealed a wide range of microbial and toxic met-
als contamination in smoked-dried fish [12, 20]. There is
still a scarcity of information on the heavy metals con-
tent and microbial contamination of most of the commonly
consumed smoked fish products. The scarcity of com-
prehensive information on the heavy metals content and
microbial contamination, of commonly consumed smoked
fish products is the major reason for this study. This
study has become imperative in view of the high level
of dried fish consumption and the need to provide rele-
vant health information to the public by policy makers,
in order to reduce disease pandemic levels in the society.
It is the intention of this study to assess the occurrence
of toxic metals and aflatoxins contamination in frequently
consumed smoke-dried fishes, and evaluate their health
implications.
the inedible parts (gills, scales and bones). The flesh was
then pulverized using a mechanical blinder.
2.3. Digestion and Toxic Metals Determination
Approximately 5 g of the pulverized fish flesh was
digested with concentrated nitric and sulphuric acids
(HNO3 and H2 SO4 ) mixed in a ratio of 1:1, under a tem-
perature of 90  C (inside a laboratory water bath) until
a clear solution was attained. This solution was cooled
under ambient laboratory temperature, then filtered into
a measuring cylinder and diluted with distilled water to
100 mL. The three common toxic metals (Hg, Cd and Hg)
level in the digested and diluted solution was measured
using an Atomic Absorption Spectrophotometer. There-
after, each toxic metal level in the digested fish solution
was expressed as mg/kg (ppm) of dry weight.

2.4. Aflatoxin Analysis

2. MATERIALS AND METHODS 100 g of the pulverized fish flesh was mixed with 10 g of
2.1. Sample Collection sodium chloride (NaCl) solution prepared with methanol.
Fifteen (15) smoked-dried fish species were sampled ran- Then the fish extract was prepared in accordance with pro-
domly from several fish retailers across Nigeria, between cedures described by Singh and Nsokolo [12]. The anal-
April 2022 and September, 2022. Two major categories of ysis of aflatoxins in the fish extract was done through
fish—native fish (freshwater) and saltwater fish, as shown the enzyme linked immunosorbent assay (ELISA) method,
in Table I were used for this study. The native fish are using the AgraQuant kit, as explained by Adesokan et al.
indigenous wild fish species which are mainly habitat in [21]. Then2023
the measurement
IP: 197.210.84.168 On: Mon, 10 Apr 17:03:43 of the total aflatoxins level in
freshwaters; while the saltwater fish Copyright:
are species American
that are Scientific
each fishPublishers
sample was expressed as parts per billion (ppb).
found in the sea and ocean waters, and are imported into by Ingenta
Delivered
the country. The Imported fish are here also referred to as 2.5. Fish Health Risks Analysis
seafood. Fish health risks were analysed using the estimated daily
intakes (EDI), targeted hazard quotients (THQs) and haz-
2.2. Sample Preparation ard index (HI) as indicated in the following procedures.
The fish samples were placed in aerated containers to
maintain their microbial load status, prior to laboratory 2.5.1. Estimated Daily Intakes (EDI)
analysis. For each fish sample, the edible part (mus- The fish EDI of both the heavy metals and aflatoxins was
cle/flesh/tissue) of the fish was carefully separated from calculated by using Eq. (1):
Cn × Cc
Table I. The fish samples. EDI = (1)
Bw
Freshwater fish species Saltwater fish species Where: EDI = mg/kg bw/day; Cn = Level of the substance
Africa Catfish (Clarias gariepinus), Atlantic mackerel (Scomber recorded in the fish tissue (mg/kg); Cc = Mean fish inges-
scombrus) tion (mg/day); Bw = Assumed body weight (kg).
Tilapia (Oreochromis niloticus) Herrings (Clupea harengus)
Silver Butter Catfish (Schilbe Horse Mackerel (Trachurus
intermedius) Trachurus) 2.5.2. Targeted Hazard Quotients (THQ)
Moon fish (Citharinus citharus) Blue whiting (Micromesistius This is the ratio of the metal’s EDI through oral ingestion
poutassou) to the metal’s RfD, and it is calculated through Eq. (2):
Stinging catfish (Heteropneustes White croacker
fossilis) (Genyonemus lineatus) EDI
THQ = (2)
Bullseye Snakehead (Channa RfD
marulius)
Mudfish (Ophicephalus striatus). 2.5.3. Hazard Index (HI)
Striped bagrid catfish (Mystus
This is equivalent to the arithmetic summation of all the
tengra)
Striped catfish (Rita rita) THQ results of each fish sample. It is calculated through
African weakly electric fish Eq. (3) [22].
(Marcusenius stanleyanus),
HI = THQ 1 + THQ 2 +    THQn (3)

318 Mater. Express, Vol. 13, pp. 316–326, 2023

Uguru et al. Toxic metals and aflatoxins occurrence in smoked-dried fish and their health risks assessment

From literature: the assumed body weight for children 3. RESULTS AND DISCUSSION
(below 18 years) is Bw = 35 kg, and for adult (over 18 3.1. Toxic Metals Concentration
years) is Bw = 70 kg, while the mean fish ingestion “Cc” The results of toxic metals concentration in all the fish
is 0.0365 mg/ person/day; and RfDs values for the three species are presented in Figures 2 and 3. In the indige-
measured common toxic metals are Hg = 0.0003, Cd = nous fish species, Figure 1, Hg level varied from 0.085–
0.001 and Pb = 0.0035 [23]. 0.198 mg/kg, Cd level ranged from 0.092–0.204 mg/kg,
and Pb level varied between 0.173 and 0.329 mg/kg. Like-
2.5.4. Carcinogenic Analysis of the Toxic Metals wise, in the imported fish species Figure 2, Hg content
The cancer risk (CR) value is an indicator of the possi- varied between 0.204 and 0.258 mg/kg, Cd concentration
bility of developing cancer cells through the ingesting of ranged from 0.092–0.194 mg/kg, and Pb level varied from
contaminants, and it is calculated using Eq. (4) [24, 25]. 0.239–0.284 mg/kg. The toxic metals accumulation rate in
CR = EDI × Cf x × 10−3 (4) the fish’s body is similar to the range obtained by Molina
[28] in fishes sampled from Laguna de Bay and Anko-
where Cf = oral slope factor. From literature [26], brah basin. Furthermore, the Cd level in the fish bodies
Cadmium’s Cf = 63 mg/kg/day and lead’s Cf = observed in this finding was considerably lower than the
00085 mg/kg/day, and there is no recorded slope factor
for Hg.
0.35
Hg
2.6. Aflatoxins Health Risks Evaluation 0.30 Cd
Toxic metals level in the
fresh water fish (mg/kg)
The evaluation of health risks of orally ingested fish flesh Pb
was carried by measuring the hazard index (HI), margin of 0.25
exposure (MOE) and estimated liver cancer risk (ELCR)
0.20
as shown in Eqs. (5)–(7) respectively.
0.15
2.6.1. Hazard Index (HI) of Aflatoxins
Aflatoxins HI level in the fish IP:
was197.210.84.168 the Mon, 10 Apr0.10
calculated usingOn: 2023 17:03:43
expression presented in Eq. (5): Copyright: American Scientific Publishers
0.05
EDI Delivered by Ingenta
HI = (5) 0.00
TD50 × 50 000 ish ia ish ish h ad ish ish ish fish
C atf ilap atf on f atfis kehe udf catf catf tric
Where the 50,000 is a safety factor and TD50 T rC o c M rid ed lec
ric
a
te M ing Sna
(g/kg/BW/day) is the microbial dose required to induce Af ut g y e ag trip ly e
er B
S
n
ti llse ed b S eak
v u p
cancerous tumor [27]. Sil B str
i nw
ca ri
Af
2.6.2. Margin of Exposures (MOE) of the Aflatoxins
Fig. 1. Toxic metals level in the freshwater fish.
The MOE of the fish was calculated through Eq. (6) [18].
EDI EDI g/kg bw/day
MOE = (6)
170000 g/kg bw/day 0.30

2.6.3. Estimated Liver Cancer Risk 0.25

Toxic metals level in
the seafood (mg/kg)

The estimated chance of liver cancer occurrence in adult,

due to smoked fish consumption was calculated using 0.20
Eq. (7).
0.15
Cancer risk = EDI × Average potency (7)
Hg
The average potency of cancer chances per 100,000 peo- 0.10 Cd
ple in Nigeria is 0.04944 [18]. Pb
0.05
2.7. Statistical Analysis
0.00
All data acquired in this study were analyzed by using l gs l g er
re re itin ck
the SPSS 20.0 for Windows, to evaluate the effect of fish cke rrin cke h oa
ma He M
a
ue
w
ec
r
species on the aflatoxins content of the fish flesh. The ntic orse Bl hit
la H W
means will be separated by using the Deacum Multiple At
range Test (DMRT). Also the mean values of results will
be plotted by using Microsoft Excel for Windows. Fig. 2. Toxic metals level in the seafood.

Mater. Express, Vol. 13, pp. 316–326, 2023 319

Toxic metals and aflatoxins occurrence in smoked-dried fish and their health risks assessment
12
10
Aflatoxins (ppb)
6 .4 9 4 6 .9 3 8
6 5 .1 7 7
2
Fig. 3. Smoke-dried fish aflatoxins level.
result (mean∼0.24 mg/kg) recorded in Ghana freshwater
fishes [29].
Interestingly, stinging catfish flesh had the lowest Hg
level (0.085 ± 0.10 mg/kg), while the highest Hg con-
IP: 197.210.84.168 On: Mon,
centration (0.258 ± 0.27 mg/kg) was Copyright:
recorded in American
Atlantic Scientific
mackerel. The mean Hg values detected in the fishes exam- byproducts.
Delivered
ined in this research, were in similarity with the results
(mean∼0.148 mg/kg) obtained by Mielcarek et al. [26] for
freshwater fishes; but our study’s results were higher than
the results (0.079 mg/kg) recorded by Łuczyńska et al.
[8] for fishes sampled from others geographical regions.
Furthermore, based on the WHO recommended limit for
Hg contamination, the findings of this study depicted that
Hg level did not exceed the limit of 0.5 mg/kg approved
by WHO for fish flesh [33, 34]. The lowest Cd level
(0.092 ± 0.15 mg/kg) was observed in silver butter cat-
fish, while the uppermost Cd level (0.204 ± 0.22 mg/kg)
was noticed in Africa catfish. Concentration of Cd in the
fishes studied in our research is similar to results obtained
by Jarosz-Krzemi´nska et al. [30] for rainbow trout (Ono-
corhynchus mykiss). Despite the relative high Cd contam-
ination in the fish flesh, generally contamination values
did not exceed the WHO maximum tolerable contami-
nation (0.5 mg/kg) for all the fish products. In contrast,
the Cd level in the all fishes studied exceeded the con-
tamination level (0.05 mg/kg) approved by the European
Commission (EC) Regulation [33, 34]. Additionally, the
striped bagrid catfish recorded the maximum Pb accumu-
lation (0.329 mg/kg), while the African weakly electric
fish had the minimum Pb accumulation (0.173 mg/kg).
The Pb accumulation level in the fishes studied was gener-
ally lower than the Pb level for mudfish sampled from Pra
basin [4]. The differences in Pb levels in the studied fish
320
Uguru et al.
9 .4 2 2
8 .1 0 2 8 .1 1 8
5 .7 0 8 5 .6 4 8
5 .4 0 1
4 .7 1 7
0 .9 0 9
0 .5 6 4 0 .5 8 0 .6 4 4 0 .7 8 6
samples could be linked to variation, in the concentrations
and volume of toxic effluents in the different water bodies
in which the existed. Despite the fairly high Pb levels in
the10fish
Aprflesh,
2023Pb levels were within the acceptable limit
17:03:43
approvedPublishers
by appropriate public regulatory bodies for fish
Ingenta Both the European Commission (EC) and WHO
regulations set maximum allowable Pb contamination for
fish at 0.30 ppm and 0.5 ppm, respectively [33, 34].
Generally, the seafood had a higher absorptions of Hg
(0.222 mg/kg) and Pb (0.255 mg/kg), when compared
to the Hg (0.142 mg/kg) and Pb (0.243 mg/kg) values
recorded in the freshwater fish species. Similar trends of
results were obtained by Gonzalez et al. [31] and Barone
et al. [10] where sea/oceans water fishes recorded higher
heavy metal levels. Complex heavy metals pollution of
ocean/sea water and its sediments, generally result from
poor waste management and inappropriate regional plan-
ning. This leads to high amassing of these toxic materials
in the ocean fish bodies [10]. Likewise, related studies
attributed high bioaccumulation of toxic substances in
fish muscle to, pollution from mining wastes, agricultural
chemicals, batteries and petroleum products, which accu-
mulate in the water bodies [32].
As described in literatures, human contact with these
toxic elements, mainly through oral ingestion is very haz-
ardous to human health [4, 31]. Cd toxicity is associated
with respiratory disorder, cancer of the lungs, cardiovascu-
lar, hematological, renal problem and reproductive prob-
lems [35]. The impacts of toxicity of Hg may lead to
memory loss, nervous system and gastrointestinal tract dis-
orders, kidney failure, visual impairment and formation of
cancerous cells [36]. Likewise Pb toxicity is associated
Mater. Express, Vol. 13, pp. 316–326, 2023
Uguru et al. Toxic metals and aflatoxins occurrence in smoked-dried fish and their health risks assessment

with; deoxyribonucleic acid (DNA) abnormal functioning,
intellectual disability and chronic kidney failure [37].
3.2. Assessment of Health Risks of Heavy Metals
Contamination
3.2.1. Estimated Daily Intakes
The EDI results obtained from the fish samples are given
in Table II. Table II depicted that children EDI values
are higher when compared to the results for adults, and
varied widely among the 15 species of fishes sampled.
The mean Hg, Cd and Pb estimated daily intakes values
for children and adults, as revealed in this study finding
were 0.1200 and 1.63 × 10−5 mg/kg bw/day, 2.13 × 10−4
and 7.57 × 10−5, and 2.48 × 10−4 and 1.24 × 10−4 mg/kg
w/day respectively. This is similar to observations made
by Gonzalez [31], which stated that children are more pre-
disposed to food poisoning, when to compared to adults.
Similar to observations by Kortei et al. [4], this study’s
results depicted that Hg had the maximum EDI value while
Pb had the minimum EDI value. Individually, the maxi-
mum Hg EDI value was observed in Atlantic mackerel,
while the tilapia recorded the lowest Hg EDI; the Africa
catfish had highest Cd EDI, and the silver butter catfish
recorded the least Cd EDI; while the Herrings recorded
the maximum Pb EDI, and striped bagrid catfish had the
lowest Pb EDI. The high Cd EDI IP:values observed inOn:
197.210.84.168
the Mon, 10 Apr 2023 17:03:43
Copyright:
fishes is similar in trend with results obtained American Scientific
by Mielcarek
et al. [26]. Delivered bynoIngenta
3.2.2. Targeted Hazard Quotients and Hazard Index
Table III presents the THQ and HI values of the fish sam-
ples studied. The THQ results for children and adults as
regards to Hg, Cd and Pb were; 0.585 and 0.293, 0.151
and 0.076, and 0.071 and 0.035 respectively. According
to this study, children THQ was generally higher than the
THQ values for adults, which is in conformity with reports
by Kortei et al. [4]. This study depicted that stinging cat-
fish had the lowest Hg THQ value, and Atlantic mackerel
recorded the highest Hg THQ value; silver butter catfish
had the minimum Cd THQ, and Africa catfish had the
maximum Cd THQ; while the smallest and highest Pb
THQ values were recorded in the Herrings and striped
bagrid catfish flesh respectively. It was noted that among
the three heavy metals investigated, Hg had the highest
THQ value while Pb had the lowest THQ value. This is
similar to findings which stated the THQ trend in freshwa-
ter fish was Hg > Cd > Pb [4]. The results revealed that the
saltwater fishes investigated tend to have higher Hg and Pb
THQ values, but lower Cd THQ values, when compared to
the THQ values of the freshwater fishes. This affirms that
the indigenous freshwater fishes tend to be safer (in terms
of THQ) than the sea foods, which is similar to previous
findings on freshwater fishes toxic metals health hazard
levels [38].
Additionally, Table III reveals that the HI value for chil-
dren was 0.949 and the HI value for adult was 0.404.
The findings (Table III) depicted that there is no substan-
tial health risks connected with the consumption of the
fishes (since HI < 1); though individually, horse mack-
erel and blue whiting
have HI values were greater than
> 1) in children. This implies that there are
one (HI Publishers
substantial health risks connected with smoke dried
fish consumption; although children may experience some
health issues through the consumption of Atlantic mack-
erel, horse mackerel and blue whiting.
3.2.3. Heavy Metal Carcinogenic Risk Analysis
The CR results of the three heavy metals are presented
in Table IV. For individual heavy metals, the carcinogenic

Table II. The fish EDI (mg/kg bw/day).

Hg Cd Pb

Children Adults Children Adults Children Adults

Africa Catfish 0.0005 1.92E− 05 2.13E−04 1.07E−04 2.67E−04 1.34E–04

Tilapia 0.0002 8.76E−06 1.72E− 04 8.60E−05 2.98E−04 1.49E−04
Silver Butter Catfish 0.0004 1.40E−05 9.53E−05 4.78E−05 3.16E−04 1.58E-04
Moon fish 0.0937 1.21E−05 1.79E−04 8.95E−05 2.18E−04 1.09E−04
Stinging catfish 0.0734 8.22E−06 9.70E−05 4.84E−05 1.98E−04 9.89E−05
Bullseye Snakehead 0.1444 1.61E−05 1.37E−04 6.83E−05 1.92E−04 9.59E−05
Mudfish 0.1631 1.82E−05 1.87E−04 9.33E−05 2.65E−04 1.33E−04
striped bagrid catfish 0.1186 1.32E−05 1.57E−04 7.85E−05 3.44E−04 1.72E−04
Striped catfish 0.1299 1.45E−05 1.43E−04 7.17E−05 2.53E−04 1.26E−04
African weakly electric fish 0.1130 1.25E−05 1.35E−04 6.76E−05 1.80E−04 9.02E−05
Atlantic mackerel 0.2235 2.49E−05 1.01E−04 5.04E−05 2.65E−04 1.32E−04
Herrings 0.1787 1.99E−05 9.64E−05 4.82E−05 1.58E−04 7.92E−05
Horse Mackerel 0.1952 2.18E−05 2.03E−04 1.01E−04 2.69E−04 1.35E−04
Blue whiting 0.1882 2.10E−05 1.92E−04 9.59E−05 2.50E−04 1.25E−04
White croacker 0.1771 1.97E−05 1.65E−04 8.23E−05 2.55E−04 1.27E−04
Total 0.1200 1.63E−05 2.13E−04 7.57E−05 2.48E−04 1.24E−04

Mater. Express, Vol. 13, pp. 316–326, 2023 321

Toxic metals and aflatoxins occurrence in smoked-dried fish and their health risks assessment Uguru et al.

Table III. The THQ and HI evaluation in smoke-dried fish.

THQ

Hg Cd Pb HI

CHD Adult CHD Adult CHD Adult CHD Adult

Africa Catfish 0.690 0.345 0.213 0.106 0.076 0.038 0.979 0.489
Tilapia 0.314 0.157 0.172 0.086 0.085 0.043 0.571 0.286
Silver Butter Catfish 0.502 0.251 0.095 0.048 0.090 0.045 0.687 0.344
Moon fish 0.436 0.218 0.179 0.090 0.062 0.031 0.677 0.339
Stinging catfish 0.295 0.147 0.097 0.048 0.057 0.028 0.449 0.223
Bullseye Snakehead 0.579 0.290 0.137 0.068 0.055 0.027 0.771 0.385
Mudfish 0.655 0.327 0.187 0.093 0.076 0.038 0.918 0.458
striped bagrid catfish 0.476 0.238 0.157 0.078 0.098 0.049 0.731 0.365
Striped catfish 0.522 0.261 0.143 0.072 0.072 0.036 0.737 0.369
African weakly electric fish 0.453 0.226 0.135 0.068 0.052 0.026 0.64 0.32
Atlantic mackerel 0.897 0.448 0.101 0.050 0.076 0.038 1.074 0.536
Herrings 0.716 0.358 0.096 0.048 0.045 0.023 0.857 0.429
Horse Mackerel 0.782 0.391 0.203 0.101 0.077 0.038 1.062 0.53
Blue whiting 0.754 0.378 0.192 0.096 0.071 0.036 1.017 0.51
White croacker 0.711 0.355 0.165 0.082 0.073 0.036 0.979 0.473
Mean 0.585 0.293 0.151 0.076 0.071 0.035 0.949 0.404

Note: ∗ CHD = Children.

risk of Cd is generally higher than Pb; portraying Cd as Compared with recent studies, the heavy metals car-
having a higher carcinogenic risk potential when com- cinogenic risks are similar to those obtained by previous
pared to Pb. As portrayed by the results, the highest and authors [26, 31] on food samples. Recent investigation
lowest Cd carcinogenic risks were recorded in stinging into the metal toxicity revealed that the carcinogenic risks
IP: 197.210.84.168 On: Mon, 10 Apr
linked to 2023 17:03:43
Cd contamination, were higher than the cancer
catfish and Atlantic mackerel respectively; while American
Copyright: stinging Scientific Publishers
catfish and Atlantic mackerel had the minimum and risks associated
maxi- by Ingenta with Pb contamination in freshwater fishes
Delivered
mum Pb carcinogenic risks respectively. Generally, it was [26]. Generally, the CR values revealed that: in adults the
noted from the results that the freshwater fishes have lower studied metals’ contamination have insignificant chances
of causing cancer cell formation (CR < ×10−6 ). For chil-
heavy metals carcinogenic risks, when compared to the
dren, the CR values revealed a moderate cancer risks asso-
seawater fishes, which is in confirmation with findings by
ciated with Cd pollution (7.56 ×10−4), and an insignificant
Łuczy´nska et al. [8].
cancer risks associated with Pb pollution (1.02 ×10−6). CR
values less than 1 × 10−6 is considered to be an insignifi-
cant carcinogenic risk, CR values greater than 1 × 10−4 is
Table IV. Cancer risk results of the heavy metals through oral an indication of potent carcinogenic risk, while CR results
consumption. ranging between 10×10−3 and 10×10−5 are rated as mod-
Cd Pb erate in carcinogenic risk [39, 40].
Children Adults Children Adults
3.3. Aflatoxins Concentration in the Smoked-Dried
−6 −7 −9
Africa catfish 3.05 × 10 1.21 × 10 4.11 × 10 1.63 × 10−11 Fish
Tilapia 1.39 × 10−6 5.52 × 10−8 1.87 × 10−9 7.44 × 10−11
The ANOVA result on the effect of fish species on the
Silver butter catfish 2.21 × 10−6 8.80 × 10−8 2.99 × 10−9 1.19 × 10−10
Moon fish 5.91 × 10−4 7.67 × 10−8 7.98 × 10−7 1.03 × 10−10 aflatoxins level in the fish muscle is presented in Table V.
Stinging catfish 4.63 × 10−4 5.17 × 10−8 6.23 × 10−7 6.98 × 10−10 It was observed that the aflatoxins contamination in the
Bullseye Snakehead 9.10 × 10−4 1.02 × 10−8 1.23 × 10−6 1.37 × 10−10 fish flesh exhibited significant difference among the 15 fish
Mudfish 1.03 × 10−3 1.15 × 10−8 1.39 × 10−6 1.55 × 10−10 samples. This is similar to Santacroce et al. [41] and Singh
striped bagrid catfish 7.47 × 10−4 8.34 × 10−8 1.01 × 10−6 1.13 × 10−10 and Nsokolo [12] observations that that aflatoxins level in
Striped catfish 8.18 × 10−4 9.16 × 10−8 1.10 × 10−6 1.23 × 10−10
African weakly 7.12 × 10−4 7.94 × 10−8 9.60 × 10−7 1.07 × 10−10
different fish bodies exhibited significant variations.
electric fish Figure 3 presents the mean values of the fish aflatoxins
Atlantic mackerel 1.41 × 10−4 1.57 × 10−7 1.90 × 10−6 2.12 × 10−10 concentration. The mean aflatoxins concentration in the 15
Herrings 1.13 × 10−3 1.26 × 10−7 1.52 × 10−6 1.70 × 10−10 fish species sampled range between 0.564 ppb and 9.422
Horse mackerel 1.23 × 10−3 1.38 × 10−7 1.66 × 10−6 1.85 × 10−10 ppb. Findings of this research show that Atlantic mack-
Blue whiting 1.19 × 10−3 1.33 × 10−7 1.60 × 10−6 1.79 × 10−10
erel has the lowest aflatoxins level, and moon fish has
White croacker 1.12 × 10−3 1.25 × 10−7 1.51 × 10−6 1.68 × 10−10
Mean 7.56 × 10−4 1.03 × 10−7 1.02 × 10−6 1.39 × 10−10 the highest aflatoxins concentration. The aflatoxins con-
centration in the freshwater fish muscle was observed to be

322 Mater. Express, Vol. 13, pp. 316–326, 2023

Uguru et al. Toxic metals and aflatoxins occurrence in smoked-dried fish and their health risks assessment

Table V. ANOVA results of the fish species on the tissue aflatoxins Nsokolo [12]. The variations in the aflatoxins level in fish
concentration. could be linked to storage and climatic/environmental con-
Sum of Squares Df Mean square F p-value ditions. Fungi tend to thrive better during the rainy sea-
son, when compared to the dry season. This is due to the
Between groups 1365.241 14 97.517 3.078 3.64E−05∗ damp environmental condition usually experienced during
Within groups 4277.564 135 31.686
Total 5642.805 149
the rainy season [41, 48]. Implications of aflatoxins toxic-
ity include cancer and liver problems; these complications
Note: ∗ = significantly different at p ≤ 005.
are more fatal in children [49].

lower than the concentration obtained by Akinyemi et al.
[42], but greater than the results reported by Sa’adatu and
Omeiza [1] for tilapia and African catfish. In related devel-
opment, another study indicated that the aflatoxins level
detected in dried fish samples was approximately 63.620
ppb [43].
The variation in aflatoxins level in the fish samples,
compared to the results obtained by other authors could
be attributed to variations in the numbers of fish sampled,
storage condition, sampling period and personal hygiene
[44]. Though the aflatoxins level in the fish investigated
was lower than the level Kortei et al. [45] reported the con-
centration level recorded in some fishes had the ability of
causing serious health crisis in people with compromised
immune systems.
Generally, the seafood contained lower aflatoxins level,
when compared to the aflatoxins level noted in On:
IP: 197.210.84.168
the Mon, 10 Aprin2023
Copyright:
freshwater fish. Higher aflatoxins content in the Scientific Publishers value higher than 0.001 can results
American
observed
freshwater fish can be attributed its poor storage and poor byinIngenta
Delivered
market display conditions, when compared to the salt
water fish. This results from the relatively higher prices of
freshwater fish, and the related fact that they stay longer
in the retailer’s open trays in fairly unhygienic conditions,
where they become prone to fungi attack and toxins pro-
duction. Prolong shelf life under moist and warm con-
ditions tend to enhance fungi growth [46]. It has been
experimentally verified that poor storage condition acceler-
ates aflatoxins production, which constitutes a major food
safety crisis [18]. Likewise, seafood tends to have larger
proportion of salt in their bodies, which impedes fungi
growth [47]; this could be linked to the lower afltoxins
concentration in all the salt water fish species sampled.
Despite the high level of aflatoxins content documented
in the fish bodies, 100% of the fish aflatoxins level was
within the approved dosage established by WHO and the
United States (US) standard, for fish meant for human con-
sumption; but 67% of the fish exceeded the EC approved
limits. SON, US and EU recommended maximum aflatox-
ins acceptable level of 20 ppb, 10 ppb and 4 ppb respec-
tively for fish products. Furthermore, it was noted that
aflatoxins level in the all the seafood investigated did not
exceeded the limit set by EC for fishery products.
Aflatoxins concentration obtained in this study are
similar to those obtained by Akinyemi et al. [42] for
smoked-dried freshwater fish, but were lower than the
dried fish aflatoxins concentration recorded by Singh and
3.3.1. Aflatoxins Health Risks Assessment
Table VI presents summarises of the aflatoxins EDI,
HI and adult population’s risk of liver cancer chances.
The aflatoxins EDI exposure ranged 5.87 × 10−4 –9.82 ×
10−3 g/kg bw/day for the children (mean∼4.81 ×
10−3 g/kg bw/day), and adults exposure ranged from
2.93 × 10−4 –4.91 × 10−3 g/kg bw/day (mean∼2.41 ×
10−3 g/kg bw/day). Similar to findings by Adebayo-Tayo
et al. [50], the EDI results reveals that the continuous con-
sumption of some indigenous fishes (tilapia, silver butter
catfish, bullseye snakehead, mudfish and moon fish), with-
out proper heeat or other treatments, may constitute serious
health hazards to humans. Despite the high EDI in most
freshwater fishes, their values were lower than the results
obtained by Huong et al. [51] for several food products.
Aflatoxins are responsible for most liver cancer and acute
hepatitis
human beings. The American Cancer Society
17:03:43
(ACS) stated that EDI
the formation of liver cancer [52].
Furthermore, the aflatoxins’ HI values (Table VI) ranged
−4
from 7.29 × 10 –7.31 × 10−4 (mean∼7.300 × 10−4 ) for
children, and 7.29 × 10−4 –7.30 × 10−4 (mean∼7.293 ×
10−4 ). Atlantic mackerel had the minimum HI (consump-
tion risk) with values of 7.289 × 10−4 and 7.287 × 10−4
for children and adults respectively; while African weakly
electric fish has the maximum consumption risk, with HI
values of 7.313 × 10−4 and 7.292 × 10−4 for children and
adults respectively. The HI values obtained are generally
lower than results by Kortei et al. [45] and Onyedum
et al. [48] recorded for other died food items. These results
imply that consumption of the smoked-dried fish will pose
some health risk to human beings. The HI results revealed
that there is insignificant health risk (HI ≤ 1) associated
with these fish consumption. Medically, there is a high
health consequence when the HI value of a particular food
product is above 1 [53].
3.3.2. Population Health Risk
The population health hazards of the fish samples are
presented in Table VI. It was noted that the population
risks ranged from 1.45 × 10−5 to 2.43 × 10−4 can-
cer/year/100,000 population Adults’ population chances of
developing liver cancer (Table VI) depicted that a very lit-
tle population will likely develop liver cancer due to the
fish consumption. Although cancer of the liver is a leading
cause of cancer related deaths globally [54]; this finding

Mater. Express, Vol. 13, pp. 316–326, 2023 323

Toxic metals and aflatoxins occurrence in smoked-dried fish and their health risks assessment Uguru et al.

Table VI. Risks assessment resulting from consumption of smoke-dried fish.

EDI (g/kg bw/day) HI

Fish Children Adult Children Adult Population risk MOE

Africa Catfish 5.40E−03ab 2.70E−03ab 7.300E−04ab 7.294E−04a 1.33E−04 6.30E+07

Tilapia 6.78E−03ab 3.39E−03ab 7.304E−04ab 7.301E−04a 1.68E−04 5.01E+07
Silver Butter Catfish 7.24E−03b 3.61E−03b 7.298E−04ab 7.291E−04a 1.78E−04 4.71E+07
Moon fish 9.82E−03b 4.91E−03b 7.299E−04ab 7.293E−04a 2.43E−04 3.46E+07
Stinging catfish 5.95E−03ab 2.98E−03ab 7.300E−04ab 7.292E−04a 1.47E−04 5.70E+07
Bullseye Snakehead 8.44E−03b 4.23E−03b 7.302E−04ab 7.295E−04a 2.09E−04 4.02E+07
Mudfish 8.47E−03b 4.23E−03b 7.303E−04ab 7.294E−04a 2.09E−04 4.02E+07
striped bagrid catfish 5.64E−03ab 2.82E−03ab 7.303E−04ab 7.294E−04a 1.39E−04 6.03E+07
Striped catfish 4.92E−03ab 2.46E−03ab 7.291E−04ab 7.299E−04a 1.22E−04 6.91E+07
African weakly electric fish 5.90E−03ab 2.94E−03ab 7.313E−04b 7.292E−04a 1.45E−04 5.78E+07
Atlantic mackerel 5.87E−04a 2.93E−04a 7.289E−04a 7.287E−04a 1.45E−05 5.80E+08
Herrings 9.49E−04a 4.74E−04a 7.302E−04a 7.297E−04a 2.34E−05 3.59E+08
Horse Mackerel 6.04E−04a 3.02E−04a 7.296E−04ab 7.290E−04a 1.49E−05 5.63E+08
Blue whiting 6.73E−04a 3.35E−04a 7.299E−04ab 7.292E−04a 1.66E−05 5.07E+08
White croacker 8.19E−04a 4.10E−04a 7.298E−04ab 7.289E−04a 2.03E−05 4.15E+08
Mean 4.81E−03 2.41E − 03 7.300E−04 7.293E − 04 1.19E−04 1.96E + 08

Note: Columns with the same common letter indicate that the means are not significantly different (p ≤ 005).

portrayed that consumption of smoked-dried fish is respon- the aflatoxins concentration in the fish samples studied,
sible for an insignificant amount of the liver cancer cases, the findings revealed that the level of aflatoxins concen-
unlike in the case of groundnut kernels and cashew nuts tration in the fish bodies were within the range approved
that results in significant cases of liver cancer [18]. by WHO and Standards Organization of Nigeria (SON);
The findings revealed that the fish MOE ranged from though the aflatoxins concentration in the local (fresh-
3.46 × 10 to 5.80 × 10 . Furthermore the margin of expo-
7 8 IP: 197.210.84.168 On: Mon, 10
water) Apr 2023
fishes 17:03:43
were found to be slightly higher than the
Copyright:
sure results (Table VI) revealed that the exposure ofAmerican Scientific
acceptabe Publishers
thresholds set by the EC for fish products. Also
Delivered bytwo
Ingenta
aflatoxins parameters (EDI and HI) measured indi-
imported fish consumers was lower than that of the fresh-
water fish consumers. Nevertheless, despite the higher cated that insignificant health problems will be linked
MOE values of the indigenous fishes, their MOE values with aflatoxins exposure through the oral intake (consump-
were within the permissible limits approved by regulatory tion) of the fish samples. Similarly, the findings revealed
agencies. According to European Food Safety Authority that the native (freshwater) fish consumption will result in
(EFSA), there is a serious health risk concern if MOE is lower heavy metals toxicity, but higher aflatoxins poison-
less than 10,000 cancer [55]. Therefore, the high MOE ing; while the saltwater fish (seafood) posed a higher risk
values indicated that the fish constitute a very low public of toxic metals poisoning, but results in lower aflatoxins
health hazard to the general public. These findings (toxic- toxicity. Though, the results generally depicted very low
ity level) are far lower than those obtained for grains and risk of toxic metals and aflatoxins poisoning, there is need
to carry out proper overhauling of food processing and
nuts [18, 56]; hence the consumption of the fish is safer
storage methods to curtail aflatoxins exposure and reduce
than consumption of dried grains and nuts.
the prevalence of aflatoxins associated aliments, as well as
to prevent the accumulation of toxic metals and aflatoxins
4. CONCLUSION through smoke-dried fish consumption. Additionally, the
The concentrations of toxic metals and aflatoxins in com- heavy metals levels in seafood which are widely consumed
monly consumed fishes were evaluated in this study, to should be evaluated and regularly monitored, to prevent
ascertain their health friendliness and hazards. It was heavy metals poisoning in human beings.
observed that the mercury, cadmium and lead contam-
ination levels in the fish samples did not exceed the Ethical Compliance
acceptable limits approved by World Health Organization The experimental study was approved by the Ethical Com-
(WHO) and the European Council (EC). The CR values mittee and responsible authorities of Delta State University
obtained from the results indicated that adults have remote of Science and Technology, following all guidelines, regu-
chances of developing tumor through the fish consump- lations, legal, and ethical standards as required for humans
tion, but children tend to have moderate cancer risks asso- or animals.
ciated with toxic metal accumulations. Results of the HI
(HI < 1) indicated very slim chances of developing health Conflict of Interest
compilations, irrespective of the individual age. Regarding The authors declare no conflict of interest.

324 Mater. Express, Vol. 13, pp. 316–326, 2023

Uguru et al. Toxic metals and aflatoxins occurrence in smoked-dried fish and their health risks assessment
Acknowledgments: Princess Nourah bint Abdulrah-
man University Researchers Supporting Project Number
(PNURSP2023R249), Princess Nourah bint Abdulrahman
University, Riyadh, Saudi Arabia. In addition, the authors
thank Taif, Umm Al-Qura, and Mansoura Universities for
their scientific contributions.
References and Notes
1. Sa’adatu, I. and Omeiza, G.K., 2021. Determination of aflatoxin B1
and G1 in fresh, sundried, and smoke-dried tilapia and african catfish
marketed for human consumption in FCT-Abuja, Nigeria. Interna-
tional Journal of Research and Innovation in Applied Science, 6(3),
pp.131–135.
2. Salvador, A.M., García-Maldonado, E., Gallego-Narb´on, A.,
Zapatera, B. and Vaquero, M.P., 2009. Fatty acid profile 433 and
cardiometabolic markers in relation with diet type and omega-3 sup-
plementation in spanish 434 vegetarians. Nutrients, 11(7), pp.1–16.
3. Tao, Y., Yuan, Z., Xiaona, H. and Wei, M., 2012. Distribution and
bioaccumulation of heavy metals in aquatic organisms of different
trophic levels and potential health risk assessment from taihu lake,
China. Ecotoxicology and Environmental Safety, 81, pp.55–64.
4. Kortei, N.K., Heymann, E.M., Essuman, E.K., Kpodo, F.M., Akonor,
P.T., Lokpo, S.Y., Boadi, N.O., Ayim-Akonore, M. and Tettey, C.,
2020. Health risk assessment and levels of toxic metals in fishes
(Oreochromis noliticus and clarias anguillaris) from ankobrah and
Pra basins: Impact of illegal mining activities on food safety. Toxi-
cology Reports, 7, pp.360–369.
5. Agbi, G.G., Akpokodje, O.I. and Uguru, H., 2021. Evaluating the
IP: metals
impact of traffic activities on the heavy 197.210.84.168 On: Mon,
concentrations along
Copyright:
a major highway in delta state. Nigeria. Direct American
Research Journal of Scientific
Public Health and Environmental Technology, 6, pp.45–51. Delivered by Ingenta
6. Food Agriculture Organization-FAO, 2018. The State of World
Fisheries and Aquaculture 2018-Meeting the Sustainable Devel-
opment Goals, FAO, Rome. Italy (http://www.fao.org/3/i9540en/
i9540en.pdf).
7. Taylor, C.M., Golding, J. and Emond, A.M., 2016. Blood mercury
levels and fish consumption in pregnancy: Risks and benefits for
birth outcomes in a prospective observational birth cohort. Inter-
national Journal of Hygiene and Environmental Health, 219(6),
pp.513–520.
8. Łuczy´nska, J., Paszczyk, B. and Łuczy´nski, M.J., 2018. Fish as
a bioindicator of heavy metals pollution in aquatic ecosystem of
pluszne lake, Poland, and risk assessment for consumer’s health.
Ecotoxicology and Environmental Safety, 153, pp.60–67.
9. Albuquerque, F., Herrero-Latorre, C., Miranda, M., Barreto Júnior,
R.A., Oliveira, F., Sucupira, M., Ortolani, E.L., Minervino, A. and
L´opez-Alonso, M., 2021. Fish tissues for biomonitoring toxic and
essential trace elements in the lower Amazon. Environmental Pollu-
tion, 283, pp.11–24.
10. Barone, G., Storelli, A., Meleleo, D., Dambrosio, A., Garofalo, R.,
Busco, A. and Storelli, M.M., 2021. Levels of mercury, methylmer-
cury and selenium in fish: Insights into children food safety. Toxics,
9(2), pp.39–45.
11. Bjorklunda, G., Dadarb, M., Mutterc, J. and Aasethd, J., 2017. The
toxicology of mercury: Current research and emerging trends. Envi-
ronmental Research, 159, pp.545–554.
12. Singh, I.S. and Nsokolo, E., 2020. Prevalence of aflatoxins in
smoked-dried and fresh fish in Zambia. Journal of Environmental
Protection, 11(1), pp.13–21.
13. Zoz, F., Iaconelli, C., Lang, E., Iddir, H., Guyot, S., Grandvalet, C.,
Gervais, P. and Beney, L., 2016. Control of relative air humidity as
a potential means to improve hygiene on surfaces: A preliminary
approach with listeria monocytogenes. Plos One, 11(2), pp.1–14.
Mater. Express, Vol. 13, pp. 316–326, 2023
14. Thiyagarajan, S. and Jamal, A., 2021. Mycological analysis of dried
fishes collected from open markets with special focus on mycotoxin
production. Journal of Microbiology, Biotechnology and Food Sci-
ences, 10(6), pp.22–36.
15. Jaimez, J., Fente, C.A., Vazquez, B.I., Franco, C.M., Cepeda, A.,
Mahuzier, G. and Prognon, P., 2000. Application of the assay of
aflatoxins by liquid chromatography with fluorescence detection in
food analysis. Journal of Chromatography, 882(1–2), pp.1–10.
16. Hussain, I. and Anwar, J., 2008. A study on contamination of afla-
toxin M1 in raw milk in the punjab province of Pakistan. Food
Control, 19(4), pp.393–395.
17. Rushing, B.R. and Selim, M.I. 2019. Aflatoxin B1: A review on
metabolism, toxicity, occurrence in food, occupational exposure, and
detoxification methods. Food and Chemical Toxicology, 124, pp.81–
100.
18. Adetunji, M.C., Alika, O.P., Awa, N.P., Atanda, O.O. and Mwanza,
M., 2018. Microbiological quality and risk assessment for aflatoxins
in groundnuts and roasted cashew nuts meant for human consump-
tion. Journal of Toxicology, 2018, pp.1–11.
19. Rafli, Z.K., Damara, D.P., Andika, S., Widiastuti, S., Anggrahini,
S., Agustinus, P.R. and Endang, S.R., 2018. Mold contamination
and aflatoxin B1 levels in salted fish commodities from traditional
market in yogyakarta and surabaya. Indonesia. Malaysian Journal
of Microbiology, 14(2), pp.691–698.
20. Paul, W.K., Juliet, A., Bandyopadhyay, R. and Peter, J.C., 2018.
Aflatoxin contamination of dried insects and fish in Zambia. Journal
of Food Protection, 81, pp.1508–1518.
21. Adesokan, I.A., Onifade, D.A., Bolarinwa, O.O. and Awotoye, J.A.,
2016. Investigation of fungal and aflatoxin contamination of smoked
dried fish samples collected in ibadan, southwest Nigeria. Nigerian
Journal of Microbiology, 30(1), pp.3263–3265.
22.10 AprL.C.,
Chien, 2023 17:03:43
Hung, T.C., Choang, K.Y., Yeh, C.Y., Meng, P.J., Shieh,
M.J. andPublishers
Han, B.C., 2002. Daily intake of TBT, Cu, Zn, Cd and as
for fishermen in Taiwan. Science of the Total Environment, 285(1–3),
pp.177–185.
23. Sultana, M.S., Rana, S., Yamazaki, S., Aono, T. and Yoshida, S.,
2017. Health risk assessment for carcinogenic and non-carcinogenic
heavy metal exposures from vegetables and fruits of Bangladesh.
Cogent Environmental Science, 3(1), pp.12–27.
24. Hu, B., Jia, X., Hu, J., Xu, D., Xia, F. and Li, Y., 2017. Assessment
of heavy metal pollution and health risks in the soil-plant-human
system in the Yangtze river delta, China. International Journal of
Environmental Research and Public Health, 14(9), pp.10–22.
25. United States Environmental Protection Agency-USEPA, 2000. Risk
based Concentration Table. United States Environmental Protection
Agency, Philadelphia, PA, United States Government, America.
26. Mielcarek, K., Nowakowski, P., Pu´scion-Jakubik, A., Gromkowska-
K˛epka, K.J., Soroczy´nska, J., Markiewicz-Żukowska, R.,
Naliwajko, S.K., Grabia, M., Bielecka, J., Zmudzi´nska, A.,
Moskwa, J., Karpi´nska, E. and Socha, K., 2022. Arsenic, cadmium,
lead and mercury content and health risk assessment of consuming
freshwater fish with elements of chemometric analysis. Food
Chemistry, 379, pp.55–67.
27. Ismail, A., Riaz, M., Levin, R.E., Akhtar, S., Gong, Y.Y. and
Hameed, A., 2016. Seasonal prevalence level of aflatoxin M1 and its
estimated daily intake in Pakistan. Food Control, 60, pp.461–465.
28. Molina, V.B., 2013. Non-carcinogenic health risks of heavy metal in
mudfish from laguna lake. Science Diliman, 24(1), pp.23–32.
29. Anim, A.K., Ahialey, E.K., Duodu, G.O., Ackah, M. and Bentil,
N.O., 2011. Accumulation profile of heavy metals in fish samples
from nsawam along the densu river, Ghana. Research Journal of
Environmental and Earth Sciences, 3(1), pp.56–60.
30. Jarosz-Krzemi´nska, E., Mikołajczyk, N. and Adamiec, E., 2021.
Content of toxic metals and as in marine and freshwater fish species
available for sale in EU supermarkets and health risk associated with
its consumption. Journal of the Science of Food and Agriculture,
101(7), pp.2818–2827.
325
Toxic metals and aflatoxins occurrence in smoked-dried fish and their health risks assessment
31. Gonzalez, N., Calderon, J., Rúbies, A., Timoner, I., Castell, V.,
Domingo, J.L. and Nadal, M., 2019. Dietary intake of arsenic, cad-
mium, mercury and lead by the population of catalonia, Spain: Anal-
ysis of the temporal trend. Food and Chemical Toxicology, 132,
pp.11–21.
32. Vidmar, J., Zuliani, T., Novak, P., Drinčić, A., Ščančar, J. and
Milačič, R., 2016. Elements in water, suspended particulate matter
and sediments of the sava river. Journal of Soils and Sediments,
17(7), pp.1917–1927.
33. FAO/WHO, 2011. Food Standards Programme CODEX Commit-
tee on Contaminants in Foods. Working Document for Information
and Use in Discussions Related to Contaminants and Toxins in the
GSCTFF. Prepared by Japan and the Netherlands) CF/5 INF/1. The
Hague, the Netherlands.
34. European Commission—EC, 2006. The commission decision,
2006/504/EC. Official Journal of the European Union, 199,
pp.21–32.
35. Bhattacharya, S., 2020. The role of probiotics in the amelioration
of cadmium toxicity. Biological Trace Element Research, 197(2),
pp.440–444.
36. Yang, L., Zhang, Y., Wang, F., Luo, Z., Guo, S. and Strahle, U.,
2020. Toxicity of mercury: Molecular evidence. Chemosphere, 245,
pp.12–26.
37. US Centre for Disease Control and Prevention, 2021. https://
www.cdc.gov/nceh/lead/news/cdc-updates-blood-lead-reference-
value.html.
38. Polak-Juszczak, L. and Nermer, T., 2016. Methylmercury and total
mercury in eels, Anguilla Anguilla, from lakes in northeastern
Poland: Health risk assessment. EcoHealth, 13(3), pp.582–590.
39. Mohammadi, A.A., Zarei, A., Majidi, S., Ghaderpoury, A.,
Hashempour, Y., Saghi, M.M., Alinejadg, A., Yousefi, M.,
IP: 197.210.84.168
Hosseingholizadeh, A. and Ghaderpoori, M., 2019. CarcinogenicOn:
and Mon, 10CaiApr
Copyright: American
non-carcinogenic health risk assessment of heavy metals in drinking
water of khorramabad, Iran. MethodsX, 6, pp.1642–1651.Delivered by52.
40. Gnonsoro, U.P., Assi, Y.E.D., Sangare, N.S., Kouakou, Y.U. and
Trokourey, A., 2022. Health risk assessment of heavy metals (Pb,
Cd, Hg) in hydroalcoholic gels of abidjan, cĉte d’Ivoire. Biological
Trace Element Research, 200, pp.2510–2518.
41. Santacroce, M.P., Conversano, M.C., Casalino, E., Lai, O.,
Zizzadoro, C. and Centoducati, G., 2008. Aflatoxins in aquatic
species: Metabolism, toxicity and perspectives. Review of Fish Biol-
ogy and Fisheries, 18, pp.99–130.
42. Akinyemi, A.A., Adejola, A.Q., Obasa, S.O. and Ezeri, G.N.O.,
2011. Aflatoxins in Smoked-Dried Fish Sold in Abeokuta, Ogun
State, South-West Nigeria. Proceedings of the Environmental Man-
agement Conference, Abeokuta, Nigeria, Federal University of Agri-
culture, 12, pp.478–487.
43. Kachapulula, P.W., Akello, J., Bandyopadhyay, R. and Cotty, P.J.,
2018. Aflatoxin contamination of dried insects and fish in Zambia.
Journal of Food Protection, 81(9), pp.1508–1518.
326
Uguru et al.
44. Hell, K., Fandohan, P., Bandyopadhyay, R., Cardwell, K. and
Kiewnick, S., 2008. Pre- and Postharvest Management of Aflatoxin
in Maize: An African Perspective. Mycotoxins: Detection Methods,
Management, Public Health and Agricultural Trade. Wallingford,
UK, CABI Publishing, 17, pp.219–229.
45. Kortei, N.K., Agyekum, A.A., Akuamoa, F., Baffour, V.K. and
Alidu, H.W., 2019. Risk assessment and exposure to levels of nat-
urally occurring aflatoxins in some packaged cereals and cereal
based foods consumed in Accra, Ghana. Toxicology Reports, 6,
pp.34–41.
46. Bukola, C. and Adebayo, T., 2008. Mycofloral of smoke-dried fishes
sold in Uyo, eastern Nigeria. World Journal of Agricultural Sciences,
4, pp.346–350.
47. Dharshini, A.D., Priyadharshini, M.L.M., Baskaran, D. and Raj,
G.D., 2018. A report on the sodium levels of salted dry fish in
chennai and recommendations to comply regulation. The Pharma
Innovation Journal, 7(11), pp.1–4.
48. Onyedum, S.C., Adefolalu, F.S., Muhammad, H.L., Apeh, D.O.,
Agada, M.S., Imienwanrin, M.R. and Makun, H.A., 2020. Occur-
rence of major mycotoxins and their dietary exposure in north-
central Nigeria staples. Scientific African, 7, pp.1–18.
49. Vidal, A., Mengelers, M., Yang, S., De Saeger, S.M. and De Boevre,
M., 2018. Mycotoxin biomarkers of exposure: A comprehensive
review. Comprehensive Reviews in Food Science and Food Safety,
17, pp.1127–1155.
50. Adebayo-Tayo, B.C., Onilude, A.A., Bukola, C., Abiodun, A. and
Ukpe, G.P., 2006. Mycofloral of smoke-dried fishes sold in Uyo.
Eastern Nigeria. World Journal of Agricultural Sciences, 4(3),
pp.346–350.
51. Huong, B.T.M., Brimer, L. and Dalsgaard, A., 2016. Dietary expo-
sure to aflatoxin B1, ochratoxin a and fuminisins of adults in Lao
2023Vietnam:
province, 17:03:43 A total dietary study approach. Food and
Scientific Publishers
Chemical Toxicology, 98, pp.127–133.
Ingenta
American Cancer Society, 2011. Atlanta, USA.
53. Ogunkunle, C.O., Fatoba, P.O., Ogunkunle, M.O. and Oyedeji, A.A.,
2013. Potential health risk assessment for soil heavy metal con-
tamination of sagamu, south-west Nigeria due to cement produc-
tion. International Journal of Applied Science and Technology, 3(2),
pp.89–96.
54. World Health Organization-WHO, 2012. Estimated cancer incidence,
mortality and prevalence worldwide in 2012.
55. European Food Safety Authority–EFSA, 2005. Opinion of the sci-
entific committee on a request from EFSA related to a harmonised
approach for risk assessment of substances which are both genotoxic
and carcinogenic. European Food Safety Authority Journal, 3(10),
pp.1–31.
56. Oyedele, O.A., Ezekiel, C.N., Sulyok, M., Adetunji, M.C., Warth,
B., Atanda, O.O. and Krska, R., 2017. Mycotoxin risk assessment
for consumers of groundnut in domestic markets in Nigeria. Inter-
national Journal of Food Microbiology, 251, pp.24–32.
Received: 25 January 2023. Accepted: 26 February 2023.
Mater. Express, Vol. 13, pp. 316–326, 2023