INTRODUCTION
Rainbow trout from North America is one of the
most profitable members of the family in Turkish
freshwater farming. Black Sea trout, also known as
Turkish salmon, has now taken its place on the Turkish
fish market, following the decision of the General
Directorate of Fisheries and Aquaculture of the Ministry
of Agriculture and Forestry. Turkish salmon grows in
dam lakes until its weight reaches 180–220 g. After that,
it is put into farms in the cold-water areas of the Black
Sea. It is harvested when it weighs 3–4 kg.
In 2019, fish farms produced 116 053 tons of
Turkish Salmon in inland waters and 9692 tons in sea
farms [1]. This amount is constantly increasing
compared to previous years. Farmed trout from Turkey’s
southern Black Sea littoral proved to be a rich nutritional
source of fatty and amino acids, which normalize
atherogenicity and thrombogenicity indices of blood [2].
Trout is mobile and prefers clean and oxygen-rich
waters. As a result, even a slight contamination affects
this fish, long before the water quality deteriorates.
Even at low concentrations, metals in contaminated
foods have harmful effects on human health [3]. Metal
contamination occurs in nature; nevertheless, human
activities, such as mining and heavy industry, have
severe consequences for ecosystems and aquatic
environment. Despite advancements in sewage effluent
technology, sewage discharge remains a major challenge
in many developing countries [4].
Metals have a strong impact on marine environment
and make their way into human food chains. Such
toxicants as Hg, Cd, and Pb are associated with fish
consumption. Methyl Hg poisoning induced by prenatal
ingestion of contaminated fish causes infant mortality
and severe birth defects, such as mental retardation,
cerebral palsy, and various neurological disorders [5–7].
When Cd is deposited in the proximal tubular cells
of the kidney, it causes renal failure because of
the decreasing glomerular filtration rates [8]. Pb
poisoning affects renal, hematological, cardiovascular,
gastrointestinal, and reproductive systems. Moreover,
skeletal abnormalities may occur as a result of renal
dysfunction and Pb accumulation in the bones [9–11].
Even though some metals are necessary, when their level
in the tissues exceeds a certain threshold, they damage
both individual organs and the entire organism.
Fish, as an essential aquatic food in the human food
chain, has often been tested for metal contamination [3,
12–14]. Several studies have identified metal residues
in various fish species, including trout. Rainbow trout
has also been subjected to toxicological studies, which
detected accumulation in tissues and liver even at low
concentrations of Zn [15].
The current research dealt with both cancer and
non-cancer hazards associated with trace elements (Fe,
Zn, Cu, Al, Pb, Hg, and Cd) in Turkish salmon. Despite
the fact that wellness threat assessment models were
predominantly created in Europe and the United States,
the European model is still in development, getting ever
more complex [16]. The American model, according to
Gržetić and Ghariani, is detailed and accurate [16]. It
is accessible through the Risk Assessment Information
System (RAIS), which is backed up by chemical
characteristic established and gathered by the U.S. Environmental
Protection Agency (U.S. EPA) Integrated
Risk Information System [17]. Following [18–22], this
research was based on the American model produced by
the U.S. EPA [23, 24].
SRUDY OBJECTS AND METHODS
Turkish salmon samples collection. The object
of the study was Turkish salmon collected from the
Yakakent farm between February and June 2019 (three
individual samples per month). The samples were
randomly picked from fish offered for sale (Fig. 1).
The samples were washed, stored in iceboxes, and
transported to the Hydrobiology Laboratory, the
Department of Fisheries, to be tested for Fe, Zn, Cu, Al,
Pb, Hg, and Cd. Prior to the analysis, the fish samples
were documented for the required biological parameters,
e.g. wet body weight and total length. The measurements
were based on the European Parliament’s Animal Care
and Use Directive on the Protection of Animals Used for
Scientific Purposes [25]. After that, the samples were
filleted (Fig. 2), put into polyethylene bags, and stored
at 21°C.
Analytical procedures. The trace elements
in the Turkish salmon fillets were determined by
inductively coupled plasma mass spectrometry
(ICP-MS) after applying the pressure digestion method
at an environmental food analysis laboratory accredited
in Turkey (TÜRKAK Test TS EN ISO IEC 17025
AB-0364-T). European Standard method EN 15763
was used to determine trace elements using acid, wet
digestion, and standard reference material. The outputs
were presented as mg/kg wet wt.
Daily trace elements intake. Risk evaluations for
infants, children, and adults were conducted in order
to determine the potential hazards that may arise as a
result of consuming heavy metals with Turkish salmon.
The risks were defined by calculating the probability
of health hazard based on potential exposure. The
risk exposure depended on the daily consumption of
elements (mg/kg body weight per day). The estimated
daily intake (EDI) was calculated using element levels
and the amount of the fish consumed. The EDI of trace
elements was calculated using the following equation:
EDI =
Cmetal (mg
kg )X Wfish( kg
day)
BW (kg) ILCR = CDI × SF CDIcar. CDInon−car. =
Cfish (mg
kg )x EF (350 days
year ) x ED (26 years) x FIR(41000 day ATa (365 days
year x ED (26 years)) x BW (70 (1)
where Cmetal is trace elements levels in the fillet;
Wfish is the daily mean consumption of the fillet, which
was reported as 0.041, 0.027, and 0.013 kg/day for adults,
children, and infants, respectively [26]; and BW refers to
an average adult’s body weight of 70 kg, a child’s weight
of 30 kg, and an infant’s weight of 10 kg.
Carcinogenic and non-carcinogenic risks. The
incremental lifetime cancer risk (ILCR) model was
used to predict the likelihood of cancer risks in the fish
caused by exposure to carcinogenic trace elements:
ILCR = CDI × SF (2)
where CDI stands for chronic daily consumption of
a carcinogen in mg/kg of body weight per day, and
refers the lifetime mean diurnal dose of exposure to the
carcinogen. The cancer risk connected with the exposure
Figure 1 Turkish salmon Figure 2 Fillet of Turkish salmon
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to a carcinogenic or potentially carcinogenic material
was calculated using slope factors (SF) [17].
If the ILCR was < 10–6, it was regarded negligible; if
it was 10–6 < ILCR < 10–4, it was assessed as permissible
or tolerated; if the ILCR > 10–4, it was acknowledged
as substantial. The carcinogenic and non-carcinogenic
CDI values were obtained using the following
formula [17]:
Table 1 Trace elements content in the fillet of Turkish salmon
Months
Content, mg/kg wet wt.
Fe Zn Cu Al Pb Hg Cd
February 3.9a 2.2a 0.13a < 0.5a < 0.05a < 0.05a < 0.02a
March 4.2a 2.3a 0.11a < 0.5a < 0.05a < 0.05a < 0.02a
April 4.8b 2.7b 0.23b < 0.5a < 0.05a < 0.05a < 0.02a
May 5.5c 2.6b 0.24b < 0.5a < 0.05a < 0.05a < 0.02a
June 6.7d 3.1c 0.33c < 0.5a < 0.05a < 0.05a < 0.02a
Mean ± SD 5.02 ± 1.12 2.58 ± 0.35 0.21 ± 0.08 < 0.5 < 0.05 < 0.05 < 0.02
Letters a, b, c, and d show statistically significant differences (P < 0.05)
Cmetal (mg
kg )X Wfish( kg
day)
BW (kg) ILCR = CDI × SF CDIcar. =
Cfish (mg
kg )x EF (350 days
year ) x ED (26 years) x FIR(41000 mg
day )x 10−6 kg
1 mg
AT (365 days
year x LT(70 years)) x BW (70 kg)
=
Cfish (mg
kg )x EF (350 days
year ) x ED (26 years) x FIR(41000 mg
day )x 10−6 kg
1 mg
ATa (365 days
year x ED (26 years)) x BW (70 kg)
THQ = CDI
Rf.D. HI= THQ (Fe) + THQ (Zn) + THQ (Cu) + THQ (Al) + THQ (Pb) + THQ EDI = (3)
Cmetal (mg
kg )X Wfish( kg
day)
BW (kg) ILCR = CDI × SF CDIcar. =
Cfish (mg
kg )x EF (350 days
year ) x ED (26 years) x FIR(41000 mg
day )x AT (365 days
year x LT(70 years)) x BW (70 kg)
CDInon−car. =
Cfish (mg
kg )x EF (350 days
year ) x ED (26 years) x FIR(41000 mg
day )x 10−6 kg
1 mg
ATa (365 days
year x ED (26 years)) x BW (70 kg)
THQ = CDI
Rf.D. H I = T (H4)Q (Fe) + THQ where CDI – chronic daily intake of carcinogen;
Cfish – trace element concentrations in the fillet;
EF – exposure frequency; ED – exposure duration;
FIR – fish ingestion rate for adults; AT – averaging
exposure time for non-carcinogenic effects and 70 years
of lifetime (LT) for carcinogenic effect; ATa – averaging
exposure time for non-carcinogenic effects and 26 years
of exposure for carcinogenic effect; BW – body weight.
Many recent studies used the Target Hazard
Quotient (THQ) to peruse the potential non-carcinogenic
effect of elements in the edible tissues of fish. In the
present study, THQ was computed using the following
equation to assess non-carcinogenic risks for trace
elements in the fillet for adults [27–33]:
ILCR = CDI × SF CDIcar. =
Cfish (mg
kg )x EF (350 days
year ) x ED (26 years) x FIR(41000 mg
day )x 10−6 kg
1 mg
AT (365 days
year x LT(70 years)) x BW (70 kg)
days
) x ED (26 years) x FIR(41000 mg
day )x 10−6 kg
1 mg
days
x ED (26 years)) x BW (70 kg)
THQ = CDI
Rf.D. H I = T H Q ( F e ) + ( 5T)HQ (Zn) + THQ (Cu) + THQ (Al) + THQ (Pb) + THQ (Hg) + THQ (Cd)
where Rf. D. is an estimate of daily exposure that is
unlikely to have significant adverse effects over the
lifetime.
The U.S. EPA oral reference doses for Fe, Zn, Cu,
Al, and Cd are 0.7, 0.3, 0.04, 1, and 0.001 mg/kg/day,
respectively [23, 24]. The Rf. D. value for Hg inorganic
salts is 0.0003 in the Risk Assessment Information
System (RAIS). However, there is no Rf. D. value for
Pb and its compounds [17]. The oral slope factor, on the
other hand, is only indicated for Pb and its compounds
as 0.0085 mg/kg/day [17]. The Hazard Index (HI) was
found by summing up the THQs, as illustrated by the
equation below:
HI= THQ (Fe) + THQ (Zn) + THQ (Cu) + THQ (Al) +
+ THQ (Pb) + THQ (Hg) + THQ (Cd) (6)
In the current study, the term “non-carcinogenic
effect” (HI) describes the cumulative non-carcinogenic
effect. If HI > 1.0, the CDI of a certain element exceeds
Rf. D, which indicates that the element poses a potential
risk. Statistical analysis. The statistical analysis was
performed using the statistical software SPSS Version
21.0. The one-way analysis of variance (ANOVA)
was used to examine the difference in trace element
quantities in the fish samples across months, followed
by Duncan’s post hoc test. The threshold for significance
was set at P 0.05.
RESULTS AND DISCUSSION
Fifteen Turkish salmon were purchased for trace
element analysis. The fish had an average length of
51 cm and a weight of 2.90 kg.
Trace elements in the Turkish salmon. The
concentrations of the trace elements observed in the
samples of Turkish salmon were generally low (Table 1).
Fe appeared to be the most abundant element, followed
by Zn and Cu. As long as they do not exceed certain
concentrations, such essential elements as Fe, Zn, and
Cu are not harmful to biota, including fish.
No Al, Pb, Hg, and Cd concentrations were
determined in the fillet samples. In both the European
Union Commission Regulation and Turkish Food Codex,
the maximum allowable values of carcinogenic Pb, Hg,
and Cd are 0.3, 0.5, and 0.05 mg/kg wet wt., respectively
[34, 35]. However, neither the European Union
Commission Regulation nor the Turkish Food Codex
gives any permissible values for Fe, Zn, Cu, and
Al [34, 35]. These elements were far below the
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permissible values, namely Al ≤ 0.5, Cd ≤ 0.02, and Pb
and Hg ≤ 0.05.
The sequence of trace elements according to
contamination was Fe > Zn > Cu > Al > Pb = Hg > Cd.
The reason for the low amounts of Al, Pb, Hg, and Cd
could be that the fish farms are located in areas not
contaminated by urban or rural sewage. The toxic
quantities of Fe, Zn, Cu, Al, Pb, Hg, and Cd in seafood
may have a negative impact on consumers’ health.
As a result, fish farms in coastal areas may be heavily
contaminated with non-carcinogenic and carcinogenic
hazardous materials that pose a substantial risk to
human health. Thus, trace element levels in fish from
this area should be regularly monitored and assessed.
In fact, the toxic elements in fish depend on water,
food, and sediment. However, accumulation of these
elements in food and water usually depends on other
factors, e.g. metabolic rate, physiology, ecology,
contamination tendency of food, sediment, and the
temperature, salinity, and solubility of water, as well as
on the interaction of these parameters.
In this study, food intake and uncontaminated
water column had an important effect on the amount of
trace elements in Turkish salmon, which resulted in a
considerable decrease in the toxic elements in question.
As metabolic activity decreases with growth and a
proportionally lower food intake, the accumulation of
elements decreases quite naturally. The trace elements
in Turkish salmon farmed in Yakakent appeared to be
below the permissible thresholds set by international
and national organizations, confirming the results
obtained by other researchers who studied trace element
accumulation in trout [31, 36].
Estimated daily intake of trace elements. Table 2
illustrates the EDI values of Turkish salmon farmed in
the Black Sea of Yakakent in 2019 for adults, children,
and infants.
The toxicity of trace elements in humans is
determined by their daily intake. In Turkey, the average
fish consumption per adult is still low and remains at
15–20 g/day, compared to the recommended amount
of 41 g/day [1, 26]. However, people who live near the
coast consume far more fish than those who live in
continental Turkey. As a result, the research relied on the
data approved by the UN Scientific Committee on the
Effects of Atomic Radiation [26]. The consumption of
these contaminated fish parts puts the health of the local
population at risk.
The EDI calculated for all chemical elements in the
fish samples was compared with the toxicologically
acceptable level and the oral reference dosage
(Rf. D. values). The intake of all the trace elements was
below the Rf. D. limits. Thus, the trace elements in
Turkish salmon pose no threat for the population of the
region.
Human health risks. The Risk Assessment
Information System classifies Cd, Hg, and Pb as
carcinogenic agents [17]. Chronic exposure to even
low levels of Cd, Hg, and Pb could lead to a variety
of cancers. If it exceeds a certain threshold value, it
can have a carcinogenic effect. Table 3 demonstrates a
lifetime risk analysis for Turkish salmon consumers.
Percent contribution to total risk by Fe, Cu, and
Zn was determined as 34.20, 24.80, and 41.01%,
respectively. According to U.S. EPA, at ILCR 10–6,
cancer threat is insignificant, the threshold risk limit
of ILCR > 10–4 requires preventive medical measures,
while ILCR > 10–3 signals that local public health is
under threat. In the present study, the samples of Turkish
Table 2 Estimated daily intake (EDI) of trace elements
in Turkish salmon farmed in Yakakent
Trace
elements
Rf. D.
Values
EDI (2019) mg/day/ kg body wt.
Infants Children Adults
Fe 0.7 0.006526 0.004518 0.00294029
Zn 0.3 0.003354 0.002322 0.00151114
Cu 0.04 0.0002704 0.000187 0.00012183
Al 1.00 – – –
Pb – – – –
Hg 0.0003 – – –
Cd 0.001 – – –
Table 3 Chronic Rf. D values, oral slope factor (SP), non-carcinogenic and carcinogenic chronic daily intake (CDI), target hazard
quotient (THQ), hazard index (HI), and incremental lifetime cancer risk (ILCR) of trace elements in Turkish salmon in 2019
Elements Chronic Rf. D.,
mg/kg/day
Oral slope factor (SF),
mg/kg/day
Noncarcinogenic CDI,
mg/kg/day
Carcinogenic CDI,
mg/kg/day
THQ ILCR
Fe 7.00E-01 – 2.82E-03 1.05E-03 4.03E-03
Zn 3.00E-01 – 1.45E-03 5.38E-04 4.83E-03
Cu 4.00E-02 – 1.17E-04 4.34E-05 2.92E-03
Al 1.00E+00 – – – –
Pb – 8.5E-03 – – – –
Hg 3.00E-04 – – – –
Cd 1.00E-03 – – – –
HI = 1.18E-02 –
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salmon posed no cancer risk. Since none of the cancercausing
trace elements were detected, Turkish salmon
consumption can be considered beneficial. However, a
regular control the contamination levels of farmed fish is
essential.
Chemicals can be either non-carcinogenic or
carcinogenic in health risk assessments. Noncarcinogenic
trace elements have a threshold limit.
Therefore, they are regarded as having no adverse health
effects at doses below the threshold level computed
using the dose-response assessment method based on the
specific reference dose for each element. Carcinogenic
substances, on the other hand, are believed to have no
effective threshold limits. This assumption implies
that even low doses of the chemicals mean a low risk
of cancer developing over time. As a result, there is no
such thing as a safe level of exposure to carcinogenic
substances [21]. In this sense, risk analysis and regular
follow-ups are essential for human health.
The research also featured non-cancer risks of the
trace elements in Turkish salmon. The risk level of
hazard quotients (HQ) for adults was monitored for Fe,
Zn, Cu, Al, Pb, Hg, and Cd. It revealed that consuming
these trace elements through a fish-based diet posed
a significant non-cancer risk. Individual ingestion
of these trace elements from Turkish salmon in this
region, on the other hand, is safe (HQ < 1) for the local
population. Bat et al. and Yardim and Bat have obtained
similar results [31, 35]. The cumulative HI, which is the
sum of individual trace element THQs, was also used
to describe the non-cancer hazards posed by Turkish
salmon. Since the total of hazard quotients was ≤ 1,
Turkish salmon revealed no potential risk for human
health.
CONCLUSION
The hazard index was < 1, so the concentrations
of trace elements (Fe, Zn, Cu, Al, Pb, Hg, and Cd)
proved to pose no health threat via consumption.
Adults, children, and infants had the same risk
ranking, although infants were at a higher risk due
to their low body weight. However, since Turkish
salmon revealed no carcinogenic trace elements,
and the non-carcinogenic trace elements were
quite low, no consumer in any group is at risk.
Risk within the non-carcinogenic trace elements
in Turkish salmon was as follows: Zn (41.01 %) >
Fe (34.20 %) > Cu (24.80 %).
Food safety requires an intensive study program and
longitudinal studies on the health risk of trace elements
in aquaculture products cultivated in Turkey’s coastal
waters, regardless of how safe the current results are.
The practice of health management, according to Bassey
et al., begins with routine monitoring by regulatory
bodies, toxicologically assessment of wastewater using
conventional procedures, and raising public awareness of
health consequences [21].
CONTRIBUTION
The authors were equally involved in writing the
manuscript and are equally responsible for plagiarism.
CONFLICT OF INTERESTS
The authors declare no conflict of interests regarding
the publication of this article.
ACKNOWLEDGEMENTS
The authors wish to acknowledge the Department of
Hydrobiology, Fisheries Faculty, University of Sinop, for
providing laboratory facilities.
