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Environmental Pollutants and Bioavailability
ISSN: (Print) (Online) Journal homepage: https://www.tandfonline.com/loi/tcsb21
Effect of smoking and chargrilling on toxic
metal(loid) levels in tilapia from the Afram Arm of
the Volta Lake
Nomolox Solomon Kofi Adherr, Emmanuel Dartey, Bismark Dwumfour-
Asare, Emmanuel Agyapong Asare & Kofi Sarpong
To cite this article: Nomolox Solomon Kofi Adherr, Emmanuel Dartey, Bismark Dwumfour-Asare,
Emmanuel Agyapong Asare & Kofi Sarpong (2022) Effect of smoking and chargrilling on toxic
metal(loid) levels in tilapia from the Afram Arm of the Volta Lake, Environmental Pollutants and
Bioavailability, 34:1, 136-145, DOI: 10.1080/26395940.2022.2062453
To link to this article: https://doi.org/10.1080/26395940.2022.2062453
© 2022 The Author(s). Published by Informa
UK Limited, trading as Taylor & Francis
Group.
Published online: 05 Apr 2022.
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Eect of smoking and chargrilling on toxic metal(loid) levels in tilapia from the
Afram Arm of the Volta Lake
Nomolox Solomon Ko Adherr
a
, Emmanuel Dartey
a
, Bismark Dwumfour-Asare
b
,
Emmanuel Agyapong Asare
a
and Ko Sarpong
a
a
Department of Chemistry Education, Faculty of Science Education, College of Agriculture Education, Akenten Appiah-Menka University of
Skills Training and Entrepreneurial Development, Asante-Mampong Campus, Ghana;
b
Department of Environmental Health & Sanitation
Education, Faculty of Environment and Health Education, College of Agriculture Education, Akenten Appiah-Menka University of Skills
Training and Entrepreneurial Development, Asante-Mampong Campus, Ghana
ABSTRACT
This study assessed the eect of smoking and chargrilling on arsenic (As), cadmium (Cd),
mercury (Hg), and lead (Pb) levels in tilapia from cage farm and wild of the Afram Arm of Lake
Volta in Ghana. Method of assessment was an Inductively Coupled Plasma - Mass
Spectrometer. Culinary methods did not aect Cd levels in anyway, likewise Pb in cage sh.
Wild sh Pb levels decreased signicantly (p < 0.05) from raw (0.013 ± 0.004 mg/kg) after
smoking (0.0077 ± 0.0007 mg/kg), and chargrilling (0.006 ± 0.0004 mg/kg). Raw As levels
(wild: 0.0325 ± 0.0007 mg/kg, cage: 0.0478 ± 0.0009) increased signicantly by smoking (wild:
0.064 ± 0.002; cage: 0.0104 ± 0.006). Smoking introduced Hg (0.005mg/kg) in wild samples.
Chargrilling signicantly increased As levels in cage sh (0.072 ± 0.004). These contaminants
were always below the maximum permissible consumption levels. The CR of As was below
the threshold (10-4) likewise THQ and HI below (1), hence consuming tilapia from study site
either smoked or chargrilled is safe.
ARTICLE HISTORY
Received 1 December 2021
Accepted 31 March 2022
KEYWORDS
Afram river; chargrilling;
metal (loids); risk
assessment; smoking; tilapia;
Ghana
Introduction
Tilapia species holds a unique position amongst aqua-
culture shes. Tilapia is prominent in international trade
although produced in large amounts from subsistence
farmers from low-income settings [1]. Nile tilapia
(Oreochromis niloticus) is one of the most consumed
species [2]. Tilapia consumption has increased due to its
taste and nutritional benets [3] including high contents
of protein, lipids, minerals, and fat-soluble vitamins [1,4].
Tilapia’s contribution from the sheries sector to
food security is signicant in Ghana as it provides
about 60% of the protein requirement of the populace
[5]. While increased dietary consumption improves
population health [6], employment opportunities, and
nancial prots are created along the tilapia value
chain [7]. Tilapia occupies the upper aquatic food
chain like other shes [8] and becomes closely asso-
ciated with high risk of bioaccumulation of contami-
nants from sediments, food and water [9,10]. Concerns
with such risk are increasing for the sake of consumers’
health [11,12]. Some studies show that caged shes
[13,14] and the wild counterparts [3,9] alike bioaccu-
mulate toxic heavy metal(loid)s (HMs), which could
pose health risk to consumers. Generally, HMs in aqua-
tic environments do not only bioaccumulate at trophic
levels but they are non-biodegradable, and could
become highly toxic [12,15–17] even at low
concentrations [9,18]. HMs like As, Cd, Pb, and Hg are
found to be associated with various disorders and
diseases [19,20]. For example, Pb, As, and Cd could
interfere with the functions of the liver, kidneys, hae-
matopoietic, central nervous systems and others caus-
ing organs and systems failures [21–23].
Meanwhile, cooking methods are known to inuence
the levels of HMs in sh [24,25]. For instance, the culin-
ary methods of smoking and grilling are able to induce
contaminants, toxic compounds and environmental
hazards including HMs into sh and meat cuisines [26].
These culinary methods are among centuries-old tradi-
tional processes like drying, salting, and fermentation
used to cook and/or preserve sh in West Africa includ-
ing Ghana [27,28]. While smoking has remained
a common culinary process for centuries, emergence
of fast food in the country has boosted the popularity
of grilling cuisines especially for tilapia and chicken [29].
Although improved local ovens such as chorkor and oil
drum stoves [30,31] are used, fuel sources could gener-
ate several chemical contaminants that could be carci-
nogenic and genotoxic to harm sh consumers [27].
Ghana has seen steady increases in tilapia produc-
tion and consumption and currently the country
is second to Egypt in Africa [7]. The phenomenon is
likely supported by the strong perception among con-
sumers that local tilapia has higher quality – more
nutritious, safe, and tastes better than imported ones
CONTACT Bismark Dwumfour-Asare dwumfourasare@gmail.com;emmldartey@yahoo.co.uk;
ENVIRONMENTAL POLLUTANTS AND BIOAVAILABILITY
2022, VOL. 34, NO. 1, 136–145
https://doi.org/10.1080/26395940.2022.2062453
© 2022 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits
unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
[32,33]. Meanwhile, some freshwater bodies including
the Volta Lake is experiencing intensive sh aquacul-
ture due to increased demand for tilapia [7], and the
concurrent events of other polluting anthropogenic
activities raise concerns about potential contamination
of riverine shes including tilapia [34]. Considering the
limited available studies on tilapia quality especially
from the many tributaries of the Volta Lake including
its Afram Arm, and the possible health risk posed by
grilling and smoking, this case study seeks to: 1) assess
the levels of key HMs, namely, As, Cd, Hg, and Pb in
fresh raw llets (muscles) of O. niloticus from cage farm
and wild catch; 2) assess the eect of chargrilling and
smoking on the levels of the HMs in cooked tilapia
llets; and 3) estimate the potential health risks con-
sumers are exposed to. The paper ultimately contri-
butes to literature on the heavy metal levels of riverine
fresh tilapia, eect of the culinary processes of smoking
and grilling on the HMs, and nally estimate the resul-
tant health risks that contaminated tilapia pose to
consumers.
Methods and materials
Study Sites
The Afram Arm is one of the rivers (tributaries) that
feed the Volta Lake that collects all the drainage of the
Kwahu Plateau [35]. The river is about 100 km and
stretches from latitude 6° 50’ 53.81” N and Longitude
0° 43’ 25.49” E. The Volta Lake is part of the Volta Basin,
covering approximately 400,000 km
2
area within six (6)
West African countries with 42% allocation in Ghana,
43% in Burkina Faso and 15% in Togo, Cote d’Ivoire,
Mali and Benin [36]. Locally, the lake serves the pur-
poses of inland transportation, irrigation and sh farm-
ing [37]. It contributes about 90% of Ghana’s inland
shery production, mainly in large-scale commercial
sh farms operated as cage aquaculture and also pro-
vides habitat for about 140 sh species dominated by
tilapia [5,37]. In Ghana, tilapia constitutes over 80% of
total aquaculture production by 86% of local sh farm-
ers [38]. About 98% of all tilapia catches from aqua-
culture farms in Ghana is supplied directly to local
markets [39]. Two towns, Adawso and Ekye
Amanfrom (shown in Figure 1), were selected for the
study. These towns are shing communities along the
Afram river and they are separated across opposite
sides of the river by a distance of 3 km across the
river. Transportation to and from the towns is by
a ferry operated by the Volta Lake Transport
Company and canoes [40]. The sherfolk ply their sh-
ing job across the river between the two towns. The
only cage farm available at the time of the study was at
Adawso, a town of the Afram Plain South District of the
Eastern region, which is well known for processing
smoked sh. The cage farm was similar to other
aquaculture farms usually mounted on the Volta
Lake – consisting of a frame made of welded gal-
vanised pipes, oatation (plastic or metal barrels), and
netting – nylon nets of various mesh sizes [41].
Sample collection
All fresh tilapia (O. niloticus) samples were collected
from Ekye Amanfrom and Adawso. In all sixty (60)
freshly harvested shes were purchased on the
same day: thirty (30) from the only cage farm and
another separate thirty (30) from two selected local
shermen out of seven who had just returned from
shing. The tilapia samples were picked based on the
available comparably sizeable range of 20.0–26 cm
since sh sizes inuence the levels of HM contaminants
in them [25]. The separate samples (from cage farm
and wild catch) were separately rinsed with deionised
water onsite to eliminate plankton debris and other
external adherents due to harvesting, handling, and
transfer. The sample fork length (L) and weight (W)
were measured using a rule with a pair of callipers
and an electronic chemical balance, respectively. The
scales and viscera (intestines, liver and gills) of tilapia
samples were removed using clean stainless–steel scis-
sors and forceps and rinsed with deionised water
onsite. Samples of ten (10) tilapia from each environ-
ment (cage farm and wild catch) were randomly
grouped into three (3), wrapped in sterile plain zipper
bags and labelled as ‘raw’, ‘chargrilled’, and ‘smoked’
groups. The raw groups were kept in an ice chest
containing ice blocks and dispatched within 24 hr to
the Metal Contaminants Laboratory of Ghana Standard
Authority (MCL – GSA) in Accra for further storage at
−20°C and analyses. The remaining groups (chargrilled
and smoked) were similarly packaged and temporary
stored and sent to local sh processors for chargrilling
and smoking.
Chargrilling procedure
A popular local griller was selected at Koforidua the
capital of the Eastern region to chargrill samples from
the cage farm and wild catch separately with no spi-
cing. Before chargrilling, the samples were briey
brined with 10% w/v NaCl solution to mimic the
usual seasoning condition for tilapia grilling. The
stove was preheated to the temperature of
120 ± 10°C after testing with infrared thermometer
before grilling started. A space of 15cm was main-
tained between the cooking grate and the heat source
(burning wood charcoal). Each chargrilling lasted
30 minutes in line with local standard practice. After
which, the samples were cooled, repackaged in plain
sterile zipper bags, stored in an ice chest containing ice
blocks, and transported within 24 h to the MCL – GSA
laboratory for analysis.
ENVIRONMENTAL POLLUTANTS & BIOAVAILABILITY 137
Smoking procedure
One of the popular local smoked sh processor at
Adawso was picked to smoke the tilapia samples
using a chorkor stove with neem (Azadirachta indica)
wood as fuel source. Tilapia samples were seasoned
with 10% w/v NaCl before smoking for similar reason
stated earlier. A distance of 35 cm was maintained
between the cooking grate and the heat source
which was operating at a temperature around
180 ± 20°C after testing with infrared thermometer.
The smoking was done for about four (4) hours accord-
ing to local standard practice. The samples were
cooled, packaged into plain sterile zipper bags, stored
in an ice chest containing ice blocks and transported
within 24 h to the MCL – GSA laboratory for analysis.
Digestion and analyses of samples
The stored samples were thawed at room temperature
for 1 hr. Fillets (muscles) of samples (raw, chargrilled,
smoked) were separated from the bones, head, and tail.
The llets from each group were digested using the
standard operating procedure according to the British
Standard [42]. The As, Pb, Hg and Cd levels in samples
Figure 1. Map of the Volta Lake and its Afram Arm with the two study communities Adawso and Ekye Amanfrom both marked
with a star.
138 N. S. K. ADHERR ET AL.
after a microwave pressure digestion were determined
using an Inductively Coupled Plasma – Mass
Spectrometer (ICP-MS) (Agilent Technologies 7700
Series) at the GSA Laboratory. Determination of mercury
was done by employing Cold-Vapour Atomic Absorption
Spectrometry (CVAAS) after pressure digestion according
to the British Standard [43]. The test solution was trans-
ferred to the reaction analysis unit, and the Hg was
reduced with divalent tin (Tin (II) Chloride) and ushed
into the cuvette (T cell) of the AAS instrument using
a carrier gas stream (Argon gas). The absorption at
253.7 nm (mercury line) at ambient temperature was
used as a measure of the mercury concentration in the
cuvette. For all analyses, deionised water and reagents of
analytical grade were used. Additionally, a certied refer-
ence standard (DORM4) and randomly spiked samples
with an ICP-MS quality control standard and blanks were
run along with the samples. The mean for each sample
was obtained from triplicate runs. The recoveries made
on the standards are presented in Table 1.
Data presentation and statistical analysis
Levels of As, Cd, Hg and Pb in samples were descrip-
tively reported as mean with standard deviation (Mean
± SD) by wet weight. Statistical comparison of the
means of HMs in similar samples was performed by
independent samples T-test. All data were checked for
homogeneity of variances and normality with Levene
and Shapiro – Wilk tests, respectively [44]. One-way
ANOVA was performed to inferentially compare the
means of HMs in the dierent samples (raw, char-
grilled, smoked). For the ANOVA, which reported
a signicant dierence, a Tukey’s HSD post hoc test
was performed to establish the existence of any pair-
wise dierence. All statistical analyses were performed
at a 5% (0.05) (two-tailed) signicance level using IBM
SPSS Statistics Version 26.
Estimation of sh health
The health status (condition factor) of sh is critical in
determining the level of bioaccumulation of HMs.
Hence, an estimate of the health of the sample was
carried out using Equation (Eqn.) 1.
K¼100W
L3(1)
[45]
Where K is the condition factor; W is the weight of
sh (g); L is the fork length of sh (cm).
Estimation of health risk
Health risk assessment is the process of quantifying and
characterising the potential adverse health eects of
human exposures to environmental hazards [46,47].
The Target Hazard Quotients (THQ), Hazard Index (HI),
and Cancer Risk (CR) for As were estimated. The THQ for
HMs consumption of sh was calculated using Eqn. 2.
THQ ¼EFr�EDtot �FIR �C
RfDo�BWa�ATn
(2)
[9]
Where EF
r
is Exposure Frequency; C is the level of
detected metal; AT
n
is the Averaging Time (365 days/
year × number of exposure years), ED
tot
the total expo-
sure duration, BW
a
the adult Body Weight; FIR is the
Fish Ingestion Rate, R
f
D
o
is the Oral Reference Dose
with details and values provided in Tables 1, 2.
In interpreting the THQ, a value < 1 indicates an
exposure lower than the reference dose. A daily expo-
sure at this level is unlikely to cause any adverse eects
during a person’s lifetime, while a THQ ≥ 1 indicates
possible adverse eects [48]. Additionally, the Hazard
Index (HI) which is the additive eect of As, Cd, Pb and
Hg combined was estimated using Eqn. 3.
HI ¼THQðAsÞ þ THQðCdÞ þ THQðPbÞ þ THQðHgÞ(3)
[25]
For HI < 1, a population is less likely to experience
any health issue attributed to the HMs, while for HI ≥ 1,
the population’s health may be at risk due to the
ingested HMs [49].
According to the 50, As is a human carcinogen and
the HM has been linked to an increased incidence of
cancers among people with exposure in their environ-
ment and/or through diet. Previous studies on shes
suggest that at least 85% or more of As exists in the
organic form as arsenobetaine, arsenocholine, or
dimethylarsinic acid, and approximately 10% is avail-
able as inorganic toxicant [51,52]. Therefore, the life-
time Cancer Risk (CR) for As was determined using Eqn.
4 and based on the assumption that 10% of it is avail-
able in the inorganic toxic form [53].
CR ¼EFr�FIRtot �C�CSF
BWa�ATn
(4)
Table 1. Certified reference materials used and their respective
recoveries.
Heavy
metal(loid) Technique
CRM (DORM4)
Recovery
(%)
Certified value
(mg/kg)
Present Work
(mg/kg)
As ICP-MS 0.25 ± 0.02 0.23 ± 0.02 96.54 ± 2.5
Cd ICP-MS 0.41 ± 0.03 0.38 ± 0.02 93.0 ± 4.2
Pb ICP-MS 0.53 ± 0.02 0.57 ± 0.01 108.4 ± 3.6
Hg CVAAS 0.37 ± 0.03 0.36 ± 0.02 91.5 ± 3.2
Table 2. Oral reference doses (mg/kg/day).
Heavy Metal(loid)s Hg Cd As Pb
Reference dose [R
f
D
o
) 0.00016 0.001 0.0003 0.004
Source: 54
ENVIRONMENTAL POLLUTANTS & BIOAVAILABILITY 139
Where EF
r
is Exposure Frequency; C is the level of
detected metal; AT
n
is the Averaging Time (365 days/
year × number of exposure years), ED
tot
the total expo-
sure duration, BW
a
the adult Body Weight; FIR is the
Fish Ingestion Rate, CSF is the oral Carcinogenic Slope
Factor for inorganic As, and R
f
D
o
is the Oral Reference
Dose with values and details provided in Tables 2, 3.
Limitation of the study
The ndings from the study are limited to the few
samples used and the limited time period including
no consideration for dierent seasons. Muscles, viscera
(intestines, liver and gills) and bones are all edible parts
of tilapia sh which could be contaminated [60]; how-
ever, the current study considered analysis on only the
muscles of the sh which is principally consumed by
Ghanaians [3]. Also, background water and sediment
levels of contaminants were not assessed, however,
the raw fresh sh samples were used as control for
assessing the inuence of cooking methods (smoking
& grilling) on heavy metal levels in cooked tilapia.
Future studies will have to improve on the limitations
associated with the current study in terms of expand-
ing coverage of study sites beyond the tributary (Afram
river) to others as well, while increasing samples sizes
and allowing for seasonal variations (dry and wet
weather seasons).
Results and discussion
Characteristics of sampled sh
The mean condition factor (K) for raw cage (2.5 ± 1.3 g/
cm
3
) and wild (2.7 ± 1.8 g/cm
3
) sh samples were
statistically similar (p > 0.05) as shown Table 4. Thus,
indicating a comparable health status of O. niloticus
from both cage and wild environments. Also, the mean
K for the shes from the two settings was above 1
suggesting that the harvested tilapia were healthy
and not under stressful conditions [61].
Comparatively, the K for this study was higher than
1.43–1.93 g/cm
3
reported in a similar study by 11. The
dierence between the current and previous studies
may be due to the variance in tilapia species
(Sarotherodon melanotheron versus Oreochromis niloti-
cus) and water bodies (river versus lagoon).
Levels of HMs in raw samples
Three HMs were detected in raw samples from the two
settings in a similar order: As (0.0325 mg/kg) > Pb
(0.013 mg/kg) > Cd (0.0006 mg/kg), and As
(0.0477 mg/kg) > Pb (0.008 mg/kg) > Cd (0.0005 mg/
kg) for wild and cage environments, respectively, as
shown in Table 5. There was no signicant dierence in
the mean levels of Cd and Pb (p 0.05) in the samples
from the two environments. However, the As levels in
cage samples were signicantly higher than in wild
samples (p < 0.05).
BDL = Below Detection Level; Level of Detection:
(As, Hg, Pb < 0.001 mg/kg & Cd < 0.0001 mg/kg)
NA = No available MPL
a
EC ([73]European Commission, 2011), & FSAI [74]
(Food Safety Authority of Ireland, 2009)
A to D
Values in the same column with dierent
letters are signicantly dierent (p < 0.05).
The levels of As in raw samples of the current study
were comparable to 0.04 mg/kg found in O. niloticus
from the Pra and Ankobrah basins [3] but far lower
than 0.08 mg/kg detected in O. niloticus from the
Barekese reservoir all in Ghana [57]. The level of As in
the current study may be partly due to the runo and
leaching of insecticide, herbicide, and algaecide used
Table 3. Parameters for health risks assessment.
Parameters Unit Value Reference
FIR kg/capita/day 0.078 (55]
EDtot (THQ) years 64.1 [56]
EDtot (CR) years 70 [][57]
BWa kg 60 [58]
AT
n
(THQ) days 23,433 [55]
AT
n
(CR) days 25,550 [55]
EF
r
days/year 365 [55]
R
f
D mg/kg/day Table 1 [55]
CSF mg/kg/day 1.50 [59]
Table 4. Characteristics of fish samples.
Characteristics Environments Mean ± SD
Length (cm) Cage 23.3 ± 3.2
A
Wild 23 ± 3.0
A
Weight (g) Cage 29 ± 5.6
A
Wild 291.2 ± 5.8
A
K factor (gcm
−3
) Cage 2.5 ± 1.3
A
Wild 2.7 ± 1.8
A
Values in the same column with different letters are significantly different
(p < 0.05)
Table 5. Comparison of levels of HMs (mg/kg) detected in samples.
Sample
As Cd Hg Pb
Mean ± SD Mean ± SD Mean ± SD Mean ± SD
Raw Wild 0.0325
A
± 0. 0007 0.0006
A ±
0.0001 BDL 0.013
A
± 0.004
Chargrilled Wild 0.036
A
± 0.001 0.0004
A
± 0.0002 BDL 0.006
B
± 0.0004
Smoked Wild 0.064
B
± 0.002 0.0003
A
± 0.0002 0.005 ± 0.001 0.0077
B
± 0.0007
Raw Cage 0.0478
B
± 0.0009 0.0005
A
± 0.0001 BDL 0.008
B
± 0.002
Chargrilled Cage 0.072
C
± 0.004 0.0007
A
± 0.0002 BDL 0.011
B
± 0.001
Smoked Cage 0.104
D
± 0.006 0.0003
A
± 0.0001 BDL 0.006
B
± 0.0004
Standard
a
NA 0.05 0.50 0.30
140 N. S. K. ADHERR ET AL.
by farmers along the banks of the lake [34]. Also, the
slightly high As levels in cage samples could be partly
attributed to sh feeds supplied by the sh farmers
[62]. This is because multiple sources of pollution are
common with aquatic ecosystems [63].
The levels of Cd and Pb detected in this study were
below the levels found in similar studies from Ankobrah
and Pra basins: Cd (0–0.008 mg/kg) and Pb (0.04–
0.42 mg/kg) [3]. Even though the levels of Hg in the
current study were below detection in all raw samples
(Table 5), the levels are dependent on several factors
such as body size, trophic position, sex, migratory biol-
ogy, foraging behaviour, and environmental conditions
like temperature, salinity, pH and dissolved oxygen [64].
The low levels of HMs in raw samples in the study may
have resulted from the minimal bioaccumulation of HMs
by sh into the llets [65,66]. The detection of HMs in
sh llets signals exposure to contaminated environ-
ment with potential to bioaccumulate overtime even
above maximum permissible limits (MPL) [62].
However, HMs levels in the raw tilapia are low and far
below the MPLs suggesting that the sh environment
(cage and wild) is not loaded with the contaminants,
and probably because the Afram Arm of the Volta Lake
is not overly polluted, especially by anthropogenic activ-
ities. Results on Hg may support that assertion of less
polluted environment because literature posits that for
slightly polluted aquatic environment Hg targets sh
muscle for storage [63].
The eect of culinary methods on levels of
HMs
Wild and cage sh samples after chargrilling contained
three HMs in the order of levels: chargrilled wild sh –
As (0.036 mg/kg) > Pb (0.006 mg/kg) > Cd (0.0004 mg/
kg); and chargrilled cage sh – As (0.072 mg/kg) > Pb
(0.011 mg/kg) > Cd (0.0007 mg/kg) (see Table 5).
Similarly, the three HMs were detected in cage sh
samples after smoking in the order: As (0.104 mg/kg)
> Pb (0.006 mg/kg) > Cd (0.0003 mg/kg). Smoked wild
sh, however, recorded the three HMs in addition to
Hg in the order of magnitude: As (0.064 mg/kg) > Pb
(0.0077 mg/kg) > Hg (0.005 mg/kg) > Cd (0.0003 mg/
kg). The mean levels of Cd in all samples were statisti-
cally similar (p > 0.05). Likewise, the mean levels of Pb
in all cooked (smoked and chargrilled) samples were
statistically similar (p > 0.05) (Table 4). Thus, the culin-
ary methods (smoking and chargrilling) did not aect
the levels of Cd in the sh samples, and also the levels
of Pb in cage sh. However, the levels of Pb in the raw
wild sh decreased by 40.7% and 53.8% after smoking
and chargrilling, respectively (Table 5). Nevertheless,
there was no signicant dierence in the eect of
smoking and chargrilling (p > 0.05) on the levels of
Pb in raw wild tilapia samples.
There are contradictory assertions in literature
regarding the eects of cooking methods on HMs
levels in sh. The results of this study follow suit by
corroborating and contradicting some ndings from
other studies. In a study by 24,67, and, it is reported
that chargrilling lowers the levels of HMs in sh. Also,
68,report that cooking methods (including grilling)
could signicantly increase Cd levels but decrease Pb
levels in sh. Similarly, our current study found that
chargrilling reduced Pb levels, but did not aect Cd
levels in wild tilapia. The eect of cooking may be
partly due to dierence in the sh species and culinary
procedures with the associated levels of leaching of
water and fat during cooking [25].
Some studies on Hg levels in sh present divergent
views on the eect of cooking. According to 69, grilling
did not aect Hg levels in sh sampled for their study.
However, 25,70, and,found that the Hg levels increased
in sh after cooking including frying, and grilling due
to pre-concentration, formation of complexes with Hg
species and sulfhydryl groups in the tissues and/or loss
of water and fat. Our study rather found that chargril-
ling did not aect Hg levels in the sh (either from the
wild or cage). Meanwhile, smoking contributed to the
detection of 0.005mg/kg Hg levels in wild sh samples.
Since cage and wild samples were similarly smoked
and were of similar size and weight, the source of the
Hg in smoked samples is unclear. However, the
detected Hg could be partly linked to water loss during
the cooking leading to an increased Hg to mass ratio
and also formation of complexes with Hg species and
other groups [70]. Although least expected, the
detected Hg in smoked samples could have originated
from contamination from manipulation and proces-
sing techniques employed by the local smoker and
chorkor stove used.
The level of As in sh samples was signicantly
inuenced by the two culinary methods. Smoking sig-
nicantly increased As levels in both wild and cage sh
samples by about 96% and 117% (p < 0.05), respec-
tively. Chargrilling increasing eect on As levels was
comparatively low in cage sh around (50.63%) yet
signicant (p < 0.05). However, the variations in As
level could partly be attributed to some As loss with
water and volatiles including other gross constituents
(such as lipids, proteins and carbohydrates) in the
sh [71].
Generally, the eect of smoking on the levels of
HMs was more pronounced than chargrilling. The dif-
ference in culinary eect may be due to the dierence
in distances between the sh being cooked on the
cooking grate and fuel source (15 cm vs 35 cm), tem-
peratures or heat source (120°C vs 180°C), and cooking
durations (30 minutes vs 4 hours) employed in this
study (for chargrilling vs smoking respectively). The
temperature and distance could have aected the
ENVIRONMENTAL POLLUTANTS & BIOAVAILABILITY 141
water loss along with other constituents including
some HMs during cooking. However, chargrilling may
have resulted in lower water loss hence its lower HMs
levels in comparison to smoking. Although HMs (Pb,
Cd, and Hg) were detected in the cooked tilapia, the
levels were far below the maximum permissible limit
(MPL) according to EC (2006) and FSAI (2009), thus
strongly suggesting that it is safe to consume smoked
and chargrilled tilapia from both the cage and wild
environment within the study sites.
Health risk estimates
The health risk estimates for the HMs are presented in
terms of target hazard quotients (THQ) (as shown in
Table 6), hazard index (HI), and cancer risk (CR) (all
shown in Table 7). The THQ for As was the highest in
all samples due to the high As levels detected in tilapia
from both cage and wild environment and both cook-
ing methods. For instance, smoked cage tilapia had the
highest THQ for As (0.45) among all cooked samples,
indicating that the smoked cage sh has more non-
cancerous eect from As. Also, the additive inuence
of health risk from all the four HMs (As, Cd, Pb and Hg)
which is measured as HI generally increased in the
order: smoked > chargrilled > raw. Although the HI is
an indicative measure, it suggests that non-cancerous
health vulnerability due to additive inuence from the
HMs is highest in eating smoked sh, followed by
chargrillled and then raw tilapia. For the culinary trea-
ted sh, the mean HI of cage samples was signicantly
higher than that of wild tilapia. For our raw O. niloticus,
the HI were far below some values (as high as 1.883)
reported by 72, in a tilapia study from Malaysia. Again,
our study shows low THQ and HI (< 1), similar to
previous studies in Ghana [9,11,57], suggesting that
eating Ghanaian tilapia is associated with compara-
tively low vulnerability to non-cancerous health eects
from the key HMs (Cd, Pb, Hg and As). This could
corroborate with the already existing general percep-
tion in Ghana that local tilapia safe [32,33].
The Cancer Risk (CR) for As in cage tilapia were also
signicantly higher than wild tilapia (Table 7) in the
order: smoked (1.86 × 10
−5
) > chargrilled (1.28 × 10
−5
)
> raw (8.55 × 10
−6
) and smoked (1.15 × 10
−5
) > char-
grilled (6.36 × 10
−6
) > raw (5.82 × 10
−6
), respectively,
for cage and wild shes. Comparatively, the mean CR
values from our study (5.82 × 10
−6
to 1.86 × 10
−5
) for
raw, smoked and chargrilled tilapia were lower than
reported studies from Taiwan (3.4 × 10
−5
to 9.3 × 10
−5
)
[75], and Malaysia (7.3 × 10
−4
) [72]. Thus, our current
study implies that risk of developing cancers from
consuming tilapia (raw, smoked and grilled) from our
study site is around 600 to 2000 people in a -
hundred million (100,000,000). This is an indication of
a tolerable cancer risk level associated with eating sh
from the study site since the CR scores are far below
the threshold (10
−4
). For health risk assessment,
a lifetime CR of 1 chance in ten thousand (10
−4
) or
greater indicates severe risk [76] but that is far from the
case in this study.
Conclusions
Three key HMs are found in the raw fresh tilapia
(O. niloticus) from the Afram Arm of Volta Lake in
Ghana in the order of magnitude: As > Pb > Cd but
there was no signicant dierence in the levels of Cd
and Pb between wild and cage shes except for As.
The culinary methods – smoking and chargrilling, do
not inuence the levels of Cd in all cases, as well as Pb
levels in cage sh samples. However, smoking and
chargrilling decrease Pb levels in the wild tilapia and
the cooking eect could be around 41% and 54%,
respectively. The cooking methods inuence is signi-
cant on As levels because smoking could increase the
levels in wild sh by almost 97%, and in cage counter-
parts by 118%, whiles chargrilling could increase the
levels in cage by nearly 51%. Also, smoking could
introduce some detectable levels (0.005mg/kg) of Hg
Table 6. Target Hazard Quotient of heavy metal(loid)s in
O. niloticus.
Environment Culinary Method THQs Mean ± SD
Wild Raw Cd 0.0008 ± 0.0004
B
Pb 0.004 ± 0.003
B
Hg NA
As 0.141 ± 0.006
B
Grilled Cd 0.0005 ± 0.0002
B
Pb 0.0018 ± 0.0001
B
Hg NA
As 0.154 ± 0.006
B
Smoked Cd 0.0005 ± 0.0002
B
Pb 0.0025 ± 0.0002
B
Hg 0.043 ± 0.008
A
As 0.279 ± 0.008
C
Cage Raw Cd 0.0006 ± 0.0004
B
Pb 0.003 ± 0.001
D
Hg NA
As 0.207 ± 0.008
E
Grilled Cd 0.0008 ± 0.0003
B
Pb 0.0036 ± 0.0004
E
Hg NA
As 0.31 ± 0.02
C
Smoked Cd 0.0004 ± 0.0001
B
Pb 0.0018 ± 0.0001
F
Hg NA
As 0.45 ± 0.03
G
NA = Not applicable
A to F
Values within the same column with dierent letters are sig-
nicantly dierent (p < 0.05)
Table 7. Health risk estimates of consumption of O. niloticus.
Culinary
Method Environment Hazard Index Cancer Risk (As)
Raw Wild 0.146 ± 0.004
A
5.82 × 10
−6
A ± 2.60 × 10
−7
Cage 0.210 ± 0.008
B
8.55 × 10
−6
B ± 3.39 × 10
−7
Grilled Wild 0.156 ± 0.006
A
6.36 × 10
−6
A ± 2.57 × 10
−7
Cage 0.320 ± 0.020
C
1.28 × 10
−5
C ± 7.92 × 10
−7
Smoked Wild 0.320 ± 0.010
D
1.15 × 10
−5
D ± 3.43 × 10
−7
Cage 0.450 ± 0.030
E
1.86 × 10
−5
E ± 1.07 × 10
−6
A to E
Values in the same column with different letters are significantly
different (p < 0.05)
142 N. S. K. ADHERR ET AL.
especially in the wild tilapia samples. The detected
levels of HMs (Pb, Cd, and Hg) in raw and cooked tilapia
are below the maximum permissible limits, suggesting
that consuming the tilapia including raw, smoked and
chargrilled could be safe. The health risk assessments
further conrm that consuming the tilapia is safe since
the THQ and HI are below one (<1), and the CR for As is
well below the severe risk threshold (10
−4
). Smoking
and chargrilling tilapia from the study site are safe for
consumption because of insignicant health risks;
however, further studies should extensively look at
tilapia from other sources and fresh waterbodies in
Ghana. Such health risk assessment studies should
consider the inuence of dierent types of fuel sources
and types commonly used for smoking and grilling
tilapia in Ghana. Also analyses of HMs loads in back-
ground water and sediments of the waterbodies in
addition to their levels in raw and cooked tilapia vis-
cera are warranted.
Acknowledgments
The authors wish to acknowledge the support of all study
participants, laboratory experts in Ghana Standard Authority
Labs, local shermen, sh farmers, local sh processors (gril-
ling and smoking), and all other persons who contributed to
the success of this study.
Disclosure statement
No potential conict of interest was reported by the author(s).
ORCID
Bismark Dwumfour-Asare http://orcid.org/0000-0002-
6493-3892
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