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Estimation of human health risk from polychlorinated biphenyls through consumption of fish from Black Sea, Bulgaria

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22 Scripta Scientifica Salutis Publicae, vol. 2, No. 2, 2016, online first
Medical University of Varna
ORIGINAL ARTICLES
ESTIMATION OF HUMAN HEALTH RISK FROM
POLYCHLORINATED BIPHENYLS THROUGH
CONSUMPTION OF FISH FROM BLACK SEA, BULGARIA
Stanislava Katelieva Georgieva
Department of Chemistry, Faculty of Pharmacy, Medical University of Varna
Address for correspondence:
Stanislava Georgieva
55 Marin Drinov Str.
Medical University ofVarna
9002 Varna, Bulgaria
e-mail: stanislavavn@mail.bg
Received: May 16, 2016
Accepted: December 20, 2016
ABSTRACT
INTRODUCTION: Fish are reliable indicators of the bioaccumulation of persistent toxic substances in the
environment, and they are usually used to estimate contaminant exposure risks to humans. The present
study evaluates the human daily intake of polychlorinated biphenyls (PCBs) through consumption of fish
from the Black Sea, Bulgaria. The health risks were assessed using a risk quotient (RQ) of the fish consump-
tion as the ratio of daily fish exposure level in relation to oral reference dose.
MATERIALS AND METHODS: PCBs were determined in the muscle tissue of four fish species widely con-
sumed by the population of Bulgaria: goby (Neogobius cephalargoides), sprat (Sprattus sprattus), horse
mackerel (Trachurus Mediterraneus ponticus) and shad (Alosa pontica pontica). Samples were collected
from the Bulgarian Black Sea coast in the period 2007 – 2011. The indicator and dioxin-like PCBs were de-
termined by capillary gas chromatography system with mass spectrometry detection.
RESULTS: The sum of the six indicator PCBs ranged from 7.2 to 27.3 ng/g ww (in goby and shad, respec-
tively). The EDI of I-PCBs in fish from Black Sea was calculated to be between 1.36 and 5.14 ng/kg bw day
through consumption of goby and shad, respectively.
DISCUSSION: RQ values calculated were much lower than one, suggesting that consumption of the fish spe-
cies would not pose any non-cancer risk. Dioxin - like PCBs were used in order to estimate the toxicity poten-
tial (TEQs) of PCB exposure. WHO-TEQs of the 6 “dioxin–like” PCB congeners ranged from 0.03 pg TEQ/g
ww (goby) to 0.28 pg TEQ/g ww (shad) and did not exceed the limit of 3 pg TEQ/g ww, according to Europe-
an Commission.
CONCLUSION: The estimated intake levels of dioxin-like PCBs in this study were several orders lower than
their respective TDI for adults. The dietary intake of polychlorinated biphenyls through marine fish for the
Bulgarian consumer does not pose a health risk.
Keywords: PCBs, fish, dietary intake, Black Sea, Bulgaria
INTRODUCTION
Persistent organic pollutants (POPs) like poly-
chlorinated biphenyls (PCBs) are chemicals of global
concern due to their persistence in the environment,
ability of biomagnification and bioaccumulation in
ecosystems. PCBs are highly lipophilic compounds
and they are rapidly accumulated in living organisms
(1). These very persistent compounds have the poten-
tial to affect the physiological functions of wildlife
Stanislava Katelieva Georgieva
Scripta Scientifica Salutis Publicae, vol. 2, No. 2, 2016, online first
Medical University of Varna 23
(2). Many authors have revealed that high fish and
seafood consumption increases the risk of PCB con-
tamination of the human body (1, 3). Humans are
exposed to these chemicals in different ways: main-
ly through the food they eat, but also through the
air they breathe, in the outdoors and indoors (4). Al-
though PCBs are regulated in the European Union,
they are still present in our food at low levels (3).
According to their toxicological properties,
PCBs are usually divided into two groups: dioxin-
like PCBs (dl-PCBs) and non-dioxin-like PCBs (ndl-
PCBs). The dioxin-like PCBs (dl-PCB) show a sim-
ilar toxicity as polychlorinated dibenzodioxins and
polychlorinated furans. The dl-PCBs are used in or-
der to estimate the toxicity potential of PCB expo-
sure as toxic equivalency (TEQ). TEQ is defined by
the sum of the concentration of each dl-PCB conge-
ner in a mixture multiplied by its toxic equivalency
factors (TEF), developed by the World Health Orga-
nization (WHO-TEF) (5). The sum of the six PCBs
(IUPAC No. 28, 52, 101, 138, 153 and 180) compris-
es about half of the amount of total non-dioxin-like
PCBs present in feed and food (6). They are called in-
dicator PCBs (I-PCBs) for evaluating the risk to hu-
man health (7).
Several methods have been proposed for the as-
sessment of the potential human health risks from
these chemicals exposure. Current non-cancer risk
assessment methods are usually based on the use
of the risk quotient (RQ). RQ is a ratio between the
estimated dose of a contaminant and the reference
dose below which there will not be any appreciable
risk (8). If RQ exceeds unity, there may be concern
for potential health effects. Another approach for es-
timating exposure and risks by dietary intake of tox-
ic substances is the TEQ methodology, use of toxic
equivalency factors (TEFs) (9,10). In most cases, di-
etary intake has been the major source of total hu-
man exposure to PCBs (11, 12). It has been report-
ed that meat, dairy products and fish, make up more
than 90% of the intake of PCBs for the general popu-
lation (13,14,15).
The aims of this study were:
to estimate daily intake of PCBs through con-
sumption of marine fish from the Black Sea
to assess the human health risk due to polychlo-
rinated biphenyls
MATERIALS AND METHODS
1. Sampling
Samples were caught by local professional fish-
ermen by net from 2007 to 2011. The sampling strat-
egy allows covering the entire Bulgarian Black Sea
coast and includes three important fishing regions:
North (near cape Kaliakra, Krapec and Balchik),
Varna Bay and South (Bourgas, Nessebar). The fish
species were selected according to their importance
to human consumption in Bulgaria: goby (Neogobi-
us cephalargoides), sprat (Sprattus sprattus sulinus),
horse mackerel (Trachurus Mediterraneus ponticus),
and shad (Alosa pontica pontica.)
2. Analytical Method
The method used for the preparation of the
samples, clean-up and quantitative determinations
of PCBs in fish samples has been previously de-
scribed in detail (16). Briefly, twenty grams of ho-
mogenized fish tissue were extracted with hexane/di-
chloromethane in Soxhlet Extractor. The extract was
cleaned-up on a glass column packed with 2 g neu-
tral silica, 4 g acid silica and 2 g neutral silica (Merck
KGaA, Darmstadt, Germany). The eluates were con-
centrated to near dryness and reconstituted in 0.5 ml
hexane. One micro liter of purified extract was in-
jected into GC/MS.
Gas chromatographic analyses of PCBs were
carried out by GC FOCUS (Thermo Electron Cor-
poration, Austin, Texas, USA) using POLARIS Q Ion
Trap mass spectrometer. Splitless injections of 1 μl
were performed using a TR-5MS capillary column
(Bellefonte, PA, USA) coated with cross-linked 5%
phenyl methyl siloxane with a length of 30 m, 0.25
mm ID and a film thickness of 0.25 μm. Helium was
applied as carrier gas at a f low of 1 ml/min.
Pure reference standard solutions (PCB Mix 20
- Dr. Ehrenstorfer Laboratory, Augsburg, Germany),
were used for instrument calibration, recovery de-
termination and quantification of compounds. Mea-
sured compounds were: the six indicator PCBs (I-
PCBs IUPAC No. 28, 52, 101, 138, 153 and 180) and
six dioxin-like PCBs (non-ortho PCBs 77, 126, 169
and mono-ortho PCBs 105, 118, 156). Each sample
was analyzed three times and an average of the re-
sults obtained was taken.
Estimation of Human Health Risk from Polychlorinated Biphenyls through Consumption of Fish from Black Sea, Bulgaria
24 Scripta Scientifica Salutis Publicae, vol. 2, No. 2, 2016, online first
Medical University of Varna
3. Quality Control
The quality control was performed by regu-
lar analysis of procedural blanks and certified refer-
ence material BB350 (PCBs in fish oil) – Institute for
Reference Materials and Measurements, European
Commission. Recovery of PCBs from certified refer-
ence material varied in the range 85 -109% for indi-
vidual congeners.
4. Statistical Analysis
The statistical analysis of the data was based on
the comparison of average values by a t-test and a sig-
nificance level of p<0.05 was used. When the p-val-
ue was lower than 0.05, it was considered statistical-
ly significant. All statistical tests were performed us-
ing SPSS 16 software. For the purpose of statistical
analysis, concentrations of contaminants reported as
“not detected” were assigned as the detection limit.
The data used in the present study were based on the
mean concentrations of the target contaminants in
the fish species.
5. Dietary Intake Estimation
Human exposure assessment of PCBs through
oral ingestion is generally estimated using daily in-
take of the contaminant. The estimated total daily
intake (EDI) of the contaminants in a given fish spe-
cies was calculated as follows (17):
EDI = C x Intake / BW
where EDI is the estimated daily intake (ng/kg
body wt./day), C is the average concentration of mea-
sured PCBs (ng/g wet weight), Intake is the daily food
consumption of fish (13.2 g/ day for Bulgarian stan-
dard adult (18) and BW is the average consumer body
weight (70 kg for adult men).
6. Risk Assessment
The potential risks of non-carcinogenic effects
are evaluated by the risk assessment index known as
the risk quotient (RQ). RQ is defined as the ratio of
daily fish exposure level (EDI) in relation to reference
dose (RfD) considering non-carcinogenic effects of
the contaminants. The RQ was calculated as follows
(8,17):
RQ = EDI / RfD
where EDI is the estimated daily intake (ng/kg
body wt./day); and RfD is the reference dose (ng/kg
day). The RfD applied in this study was 20 ng/kg day
(8).
7. Toxic Equivalency (TEQ) Methodology
Toxic equivalency factors (TEFs) are being de-
veloped to assess the potency of polyhalogenated aro-
matic hydrocarbons, including dioxin-like polychlo-
rinated biphenyls (dl-PCBs), polychlorinated diben-
zo-pdioxins (PCDDs) and dibenzofurans (PCDFs).
Toxic equivalency factors (TEFs) are essentially
weighting factors by which the toxicity of a congener
is compared to that of 2,3,7,8-tetrachlorodibenzo-p-
dioxin (TCDD) – Table 1 (5).
In our study the concentrations of individual
dl-PCB congeners are multiplied by their TEFs and
the results summed to give a toxicity value expressed
in TCDD toxic equivalents (TEQs) through the fol-
lowing equation:
dl-PCB TEQ = ∑dl-PCBi x TEFi
RESU LTS
The concentration levels of individual PCBs
congeners were described in our previous study (16).
The PCBs load of each fish was estimated on the ba-
sis of the six indicator PCBs congeners (UPAC No.28,
PCB UPAC No. TEF -WHO 2005
non-ortho PCBs
PCB 77 0.0001
PCB 126 0.1
PCB 169 0.03
mono-ortho PCBs
PCB 105 0.00003
PCB 118 0.00003
PCB 156 0.00003
Table 1. Toxic equivalency factors (TEFs) for dioxin-like
PCBs (5)
Stanislava Katelieva Georgieva
Scripta Scientifica Salutis Publicae, vol. 2, No. 2, 2016, online first
Medical University of Varna 25
52, 101, 138, 153 and 180) recommended by the Euro-
pean Union for assessing the pollution by PCBs (7).
The lipid content, mean levels of total indica-
tor PCB congeners in investigated fish species from
the Black Sea coast of Bulgaria, estimated daily in-
take (EDI) and risk quotient (RQ) are shown in Ta-
ble 2. The lipid percentage ranged from 1.7% in goby
to 22.6% in shad.
The concentration levels of the individual six
dioxin-like PCBs (dl-PCBs) congeners (non-ortho
PCBs 77, 126, 169 and mono-ortho PCBs 105, 118,
156) were measured in our previous study (16). In
Table 3 the data was summarized and the sum of the
six dl-PCBs congeners (mean values) was presented
for the fish species investigated. In order to compare
the results obtained to permissible limits set forth in
the EU Council Regulation, the TEQ values and es-
timated daily intake (EDI) of dl-PCBs were calculat-
ed for each fish species and mean values are shown
in Table 3.
DISCUSSION
1. Indicator PCBs Levels
The mean levels of I-PCBs ranged between 7.22
ng/g ww (goby) and 27.26 ng/g ww (shad), calculated
as the sum of 6 Indicator PCB congeners. Our previ-
ous studies showed that the most abundant PCB con-
geners in fish species were the indicator PCBs consti-
tuting more than 80% of the total amount of PCBs
(19). The European Union has recommended a max-
imum level of 75 ng/g wet weight, calculated as the
sum of the six I-PCBs in the muscle meat of fish (7).
Our results for the sum of I-PCBs in all fish species
did not exceed this limit.
2. Estimated Daily Intake (EDI) of I-PCBs
Fish and seafood accounts for a small portion
of human diet, but it has been proven to be one of
the major routes of human exposure to organic con-
taminants (12). The consumption of contaminated
fat-food can be a potential risk for the consumer. To
comprehensively evaluate risk exposure, the mean
EDIs for these harmful chemicals in each fish species
were calculated. On the basis of the measured con-
centrations in the fish samples, the daily dietary in-
Species nLipids,
%
Sum I-PCBs,
ng/g ww
EDI,
ng/kg /bw
Rf D,
ng/kg/day (USEPA)RQ
goby 18 1.7±0.6 7. 24.37 1.36±0.82 20 0.07
sprat 11 5.8±1.8 10.57±2.45 1.99±0.46 20 0.10
horse mackerel 18 11.7±2.6 10.96±4.56 2.05±0.93 20 0.10
shad 12 22.6±6.2 27.26±6.04 5.11.14 20 0.26
Table 2. Levels of total indicator PCBs (ng/g wet weight, mean and standard deviation) determined in fish collected from
the Black Sea, estimated daily intake (EDI) and risk quotient (RQ).
Species Sum dl-PCBs,
ng/g ww
pg TEQ-WHO 2005
/g ww
EDI,
pg TEQ / kg bw
TDI,
WHO 2000 (25)
goby 1.40.36 0.03±0.01 0.006
1-4 pg TEQ/kg bw
sprat 2.54±0.82 0.08±0.02 0.015
horse mackerel 2.01.84 0.06±0.02 0.011
shad 9.02.68 0.28±0.08 0.053
TDI - tolerable daily intake
Table 3. Sum of six dl-PCBs (ng/g ww mean and standard deviation), determined in fish, TEQs (pg TEQ/g ww) and EDI
(pg TEQs/kg bw)
Estimation of Human Health Risk from Polychlorinated Biphenyls through Consumption of Fish from Black Sea, Bulgaria
26 Scripta Scientifica Salutis Publicae, vol. 2, No. 2, 2016, online first
Medical University of Varna
take of PCBs was calculated. The estimated daily in-
take of the PCBs in fish species studied are shown in
Table 2. The estimated daily intake was calculated on
the basis of a fish consumption rate of 13.2 g/day (18)
for adults with body weight of 70 kg, on the mean ex-
posure level. The EDI of I-PCBs in fish from Black
Sea was calculated between 1.36 and 5.14 ng/kg bw
day through consumption of goby and shad, respec-
tively. Overall, the EDIs of these POPs via fish con-
sumption for adults in the present study were lower
than those reported in most previous studies (6,20).
3. Human health risk assessment
The non-carcinogenic effect of a toxic sub-
stance is considered to be acute exposure effects over
brief periods of time, such as hours or days. However,
this does not necessarily result in an acute response.
The RfD is an estimate of daily exposure in humans
that is likely to be without an appreciable risk of del-
eterious effects during a lifetime (17). The average
consumption together with the measured concentra-
tion of the contaminant are used to calculate the risk
quotient RQ. RfD values adopted in this study are the
criteria of the USEPA (Environment Agency of the
United States) (8). If the RQ value is less than 1, no
obvious health risks due to the intake or uptake of
contaminants via fish consumption would be experi-
enced. Conversely, an exposed population of concern
will experience health risks if the fish consumption
rate is equal to or greater than the RfD value (17).
The RQ values ranged from 0.07 to 0.26 for goby and
shad, respectively (Table 2). All the RQ values were
much lower than 1, suggesting that consumption of
the fish species would not pose any non-cancer risk.
4. Dioxin - Like PCBs Levels
TEQ values were calculated by multiplying the
individual dl-PCBs congener levels measured in each
sample with its toxic equivalency factors (TEF), es-
tablished by the World Health Organization (WHO-
TEF) (5). As it is shown in Table 3, the lowest total
TEQ values, expressed as pg TEQ/g ww, were estab-
lished in goby samples (mean 0.03 pg TEQ/g ww)
and the highest results were observed in shad sam-
ples (mean 0.28 pg TEQ/g ww).
The comparison of our results for TEQ val-
ues in fish with those in the literature showed low-
er levels than the TEQs in sardine from the Span-
ish Atlantic southwest coast (0.75 pg TEQ /g ww)
(21) and lower than those in salmon from the Bal-
tic Sea (12.6 pg TEQ /g ww) (22). The total WHO-
TEQ values measured in fish from the southern Bal-
tic Sea varied from 3.4 pg/g fresh weight to 15.2 pg/g
fresh weight (23). In a market study on the dietary in-
take of PCDD/Fs and PCBs performed in Finland,
Kiviranta et al. (24) measured the concentrations of
these pollutants in fish samples. The sum of PCDD/
Fs was 2.0 pg WHO-TEQ/g ww, and that of PCBs
1.5 pg WHO-TEQ/g ww. The European Union has
set a limit of 3.0 pg TEQ/g wet weight in the muscle
meat of fish for the sum of dioxin-like PCBs (7). In
our study TEQs of the six dl-PCBs for all investigat-
ed fish species did not exceed this limit.
5. Estimated Daily Intake (EDI) of dl-PCBs
The World Health Organization recommend-
ed the TEF approach, applying the recently estab-
lished WHO TEFs (5), for estimating the daily intake
for humans of dl-PCBs (Table 3) in units of TCDD
equivalents for comparison to the Tolerable Dai-
ly Intake (TDI). WHO has set a TDI for the sum of
PCDD/F-TEQ and dl-PCB-TEQ of 1–4 pg TEQ kg/
body weight (25), which is comparable with a toler-
able weekly intake of 14 pg TEQ/kg body weight as
fixed by the European Union Scientific Committee
on Food (26).
In this study, estimated daily intake of dl-PCBs
from Bulgarian food consumption data was from
0.006 to 0.053 pg TEQs kg/ body weight/ day (for
goby and shad, respectively). Both of these values
were lower than the TDI of 1 to 4 pg TEQs kg/ body
weight/ day recommended by WHO (25). These esti-
mations were also lower than those reported in Spain
- mean dietary intake of dl-PCBs from fish and sea-
food was estimated at 15.18 pg WHO-TEQ/ day in
2010 (27). Bordajandi et al. (28) analyzed a great va-
riety of food purchased across the city of Huelva
(Spain) - total daily intake of PCDD/Fs and PCBs
was estimated to be 2.63 pg WHO-TEQ/kg body
weight. The intake of PCDD/Fs plus dioxin-like
PCBs through fish and other seafood in various cit-
ies of Catalonia, Spain was estimated to be 38.0 pg
WHO-TEQ/day (29).
CONCLUSION
The PCB levels found in this study are general-
ly lower than those reported from the other regions.
Our results for the sum of I-PCBs in fish species in-
Stanislava Katelieva Georgieva
Scripta Scientifica Salutis Publicae, vol. 2, No. 2, 2016, online first
Medical University of Varna 27
vestigated ranged between 7.2 ng/g ww (goby) and
27.3 ng/g ww (shad) and did not exceed the maxi-
mum level of 75 ng/g ww. WHO-TEQs were found
in the range from 0.03 pg TEQ/g ww for goby to 0.28
pg TEQ/g ww for shad and did not exceed the limit
of 3.0 pg WHO-TEQ/g ww for sum of six dioxin-like
PCBs. The contamination of the fish species inves-
tigated with PCBs appears to be relatively low com-
pared to other European studies. The lower observed
levels of PCB in fish tissues than from fish tissues of
other aquatic ecosystems was potentially due to the
absence of PCB manufacturing in Bulgaria. The esti-
mated intake levels of dioxin-like PCBs in this study
were several orders lower than their respective TDI
for adults. We can conclude that the dietary intake
of polychlorinated biphenyls through marine fish for
the adult Bulgarian consumer does not seem to pose
a health risk.
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... The key properties of PCBs are environmental stability, biological persistence and lipophilicity which facilitate bioaccumulation along the food chain in a complex manner [4]. Humans are exposed to POP contaminants in several ways: mainly via food ingestion, inhalation, though outdoors and indoors [5]. PCBs are regulated by the European Union, WHO and FAO, as to the level of PCBs present in our food even at low levels. ...
... The mean distribution pattern of the indicator PCBs varied greatly between fish species (Figure 2 daily intake (EDI) and risk quotient (RQ) are shown in Table 3. Table 4. The EDI values in our study were lower compared to the EDI of I-PCBs in fish from Black Sea that was calculated between 1.36 and 5.14 ng/kg bw day through consumption of goby and shad, respectively [5]. The RfD values adopted in this study are the criteria of the USEPA (Environment Agency of the United States) [9]. ...
Thesis
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Concentration, seasonal variation and composition of marine litter at the coast of the Black Sea: A case study of the Ropotamo beach in the natural reserve of Ropotamo.
Thesis
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Concentration, seasonal variation and composition of marine litter at the coast of the Black Sea: A case study of the Ropotamo beach in the natural reserve of Ropotamo.
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