www.elsevier.com/locate/marpolbul
Marine Pollution Bulletin 48 (2004) 743–748
Polychlorinated biphenyl and organochlorine pesticide residuesin Lophius budegassa from the Mediterranean Sea (Italy)
Maria Maddalena Storelli, Arianna Storelli, Grazia Barone,Giuseppe Onofrio Marcotrigiano *
Pharmacological-Biological Department, Section of Chemistry and Biochemistry, Veterinary Medicine Faculty, University of Bari,
Strada Prov. le per Casamassima Km 3, Valenzano, Bari 70010, Italy
Abstract
Persistent organochlorines, such as polychlorinated biphenyls, including coplanar congeners and DDT compounds, were mea-
sured in the liver of a teleost species: namely, Lophius budegassa. The mean concentrations of PCBs (1249 ng/g wet wt) were
comparable with DDTs mean levels (1459 ng/g wet wt). Among DDTs the compound found at the highest concentration was p; p0-DDE representing 76% of the total DDT burden. The PCB profiles were dominated by congeners 153, 180, and 138 accounting for
49.8%, 16.0% and 13.7% of the total PCBs. The total 2,3,7,8-TCDD toxic equivalent (TEQs) of six coplanar PCBs, including mono-
and non-ortho congeners, was 0.98 pg/g wet wt. The congeners with highest TEQs values were non-ortho-congeners followed by
mono-ortho ones.
� 2003 Elsevier Ltd. All rights reserved.
Keywords: PCBs; DDTs; Lophius budegassa; TEQs; Mediterranean Sea
Persistent organochlorines such as PCBs and DDTs,
are a group of compounds of great chemical stability
and persistence whose presence in the environment is aclear indication of anthropogenic pollution. The massive
and indiscriminate use of these xenobiotics for industrial
and agricultural purposes, caused their widespread dif-
fusion to all environmental compartments including a
wide range of organisms such as plankton, fish, marine
and land mammals and humans. The bioaccumulation
of organochlorine compounds is a complex phenome-
non ruled by either physico-chemical properties of thesecompounds or ecological and biological factors such as
feeding behaviours, habitat, age, sex, state of health as
well as the lipid composition of the animal’s tissue or
organ (Aguilar, 1984; Addison, 1989; Henriksen et al.,
1996). The liver is recognized as the organ where the
contaminants tend to concentrate, reflecting a short-
term exposure to pollutants (Albaiges et al., 1987).
*Corresponding author. Tel.: +39-80-544-3866; fax: +39-80-544-
3863.
E-mail address: [email protected] (G.O. Mar-
cotrigiano).
0025-326X/$ - see front matter � 2003 Elsevier Ltd. All rights reserved.
doi:10.1016/j.marpolbul.2003.10.026
Moreover, the liver plays a main role in distribution and
detoxification or transformation of xenobiotics, and
constitutes an important site of pathological effects in-duced by these contaminants (Evans et al., 1993).
Several studies have shown that these compounds
exert a number of toxic responses including immuno-
toxicity, reproductive deficits, teratogenicity, endocrine
toxicity and carcinogenity/tumor promotion (Ahlborg
et al., 1994). In recent years attention has been focused
on the toxicity of PCBs, especially of those congeners
so-called ‘‘coplanar’’ which are the most toxic membersof all 209 PCB congeners. In order to esteem the toxic
potency of these chemicals and, therefore, the risk for
the exposed organisms, the toxic equivalents factor
(TEF) approach was proposed.
In the light of what mentioned above this study at-
tempted to investigate the accumulation profile of indi-
vidual PCB congeners and DDTs in the liver of a
benthic species Lophius budegassa. Furthermore, 2,3,7,8-TCDD of mono- and non-ortho coplanar congeners
were estimated (TEQs), using TEFs based on fish tox-
icity data according to van den Berg et al. (1998), in
order to assess the relative ecotoxicological impact of
highly toxic PCBs in this species.
744 M.M. Storelli et al. / Marine Pollution Bulletin 48 (2004) 743–748
1. Materials and methods
Specimens (no. 140) of L. budegassa (angler fish)
(length: 28–117 cm, aver. 86± 31.2 cm; weight: 0.25–17.6kg, aver. 10.1 ± 6.11) were caught in the South Adriatic
Sea between June and August 1999. From the total
number of specimens were formed 28 pools within which
individual fish were gathered as a function of their
similar size (Table 1). From fish of each pool, liver was
taken and kept in a deep freeze at )20 �C until chemical
analysis. To determine chlorobiphenyl (PCBs¼ sum of
17 congeners), DDT compounds (DDTs¼ p; p0-DDT,o; p0-DDT, p; p0-DDE, p; p0-DDD, o; p0-DDD) and HCB
concentrations the following method was used. Aliquots
(3 g) of the homogenised samples were ground with
anhydrous sodium sulphate in a mortar. The mixture
was extracted with petroleum ether according to Erney’s
procedure (Erney, 1983). The extracts were then con-
centrated and subsamples were taken in order to deter-
mine the tissue fat content by gravimetry. An aliquot(about 200 mg) of the remaining extract was dissolved in
hexane (5 ml) and mixed with H2SO4 conc. for the clean
up, following the procedure described by Murphy
(1972). After centrifugation, the hexane solution was
concentrated (about 1 ml) and transferred on a glass
column (i.d. 5 mm) filled with 1 g of florisil (activated at
Table 1
Percentage lipids, specimen numbers and weight range within each
pool
Pools % lipids No. of
specimens
Weight range Mean±SD
1 11.14 8 242–255 246± 5.24
2 6.37 8 284–293 287± 3.64
3 29.59 10 316–325 320± 3.34
4 22.93 8 382–392 386± 4.69
5 4.63 6 443–458 452± 6.30
6 16.89 6 569–579 574± 4.61
7 55.68 4 5092–5103 5100± 7.09
8 43.61 4 5593–5605 5600± 4.32
9 41.81 4 9498–9505 9500± 2.88
10 47.78 4 9593–9610 9600± 6.20
11 18.30 4 9694–9716 9700± 6.79
12 26.72 5 10,192–10,205 10,200± 5.54
13 43.98 6 10,993–11,008 11,000± 6.37
14 41.02 4 11,193–11,206 11,200± 5.44
15 36.16 5 11,487–11,509 11,500± 8.36
16 43.83 6 12,297–12,303 12,300± 2.58
17 34.64 4 12,495–12,503 12,500± 3.16
18 32.01 4 12,697–12,705 12,700± 3.16
19 42.01 4 13,197–13,203 13,200± 2.23
20 18.74 4 13,497–13,503 13,500± 2.54
21 18.89 4 14,392–14,410 14,400± 6.87
22 47.91 4 15,991–16,012 16,000± 7.82
23 49.89 4 16,496–16,504 16,500± 3.54
24 40.65 4 17,093–17,107 17,100± 5.44
25 33.04 4 17,192–17,209 17,200± 6.96
26 40.30 4 17,209–17,309 17,301± 9.09
27 54.58 4 17,390–17,407 17,401± 6.76
28 42.77 4 17,589–17,608 17,600± 9.61
120 �C for 16 h) for the separation of PCBs from other
organochlorine compounds. The first fraction eluted
with hexane (12 ml), contained PCBs and some DDTs,
whereas the second fraction, eluted with 10 ml of 15%ethylether in hexane, contained the remaining DDTs
and other organochlorine compounds. An aliquot of
initial fraction was run on a column (i.d. 5 mm) packed
with 125 mg of activated carbon (C. Erba, Milano, Italy)
for the separation of non-ortho PCB congeners, 3,30,4,40-T4CB, (IUPAC 77), 3,30,4,40, 5-P5CB (IUPAC 126),
and 3,30,4,40,5,50-H6CB (IUPAC 169) from other PCBs
following the method reported by Tanabe et al. (1987).Analyses were made on a Carlo Erba HR gas chro-
matograph 8000 Top with automatic injection system
and with an electron capture detector ECD-400, Ni63
(temperature: 310 �C). The GC was connected to an
IBM PS/2 55SX PC equipped with Chrom-Card version
1.2 software program for integration purposes (C.
Erba). For all the analyses a fused-silica capillary col-
umn SPB-608 Supelco (length¼ 30 m, inside diameter0.25 mm and film thickness 0.25 lm), was used. Helium
at a flow rate of 1 ml/min was used as gas carrier,
nitrogen as make-up gas 60 ml/min. Temperature was
programmed according to the following sequence:
injection at 50 �C. Oven steady for the first min and then
an increased from 50 to 180 �C at a rate of 15 �C/min.
Oven maintained at steady temperature for 1 min and
then increased from 180 to 220 �C at a rate of 4 �C/min;oven maintained at steady temperature for 20 min and
then increased from 220 to 275 �C at a rate of 5 �C/min;
from this point until the end of the analytical run, the
column remained isothermal at a temperature of 275 �C.The individual PCB congeners were 8, 20, 28, 35, 52, 60,
77, 101, 105, 118, 126, 138, 153, 156, 169, 180 and 209
numbering system (Ballschmiter and Zell, 1980) deter-
mined against the corresponding individual standardsobtained from ULTRA Scientific, Inc. (chemical purity
99%). The identity of the DDT group compounds was
confirmed by an alkali conversion to their respective
olefins and re-analysis by GLC. Analytical data, as for
DDT group compounds were obtained by a comparison
between sample peak area and external standards peaks
area (POCs mixture, bought from Supelco). Recoveries
were determined by adding known amounts of PCBs,DDTs and HCB standards (at three levels of concen-
trations) to empty samples before extraction (method of
additions) The recoveries were within 80–110%. The
limits of quantification were from 0.1 to 0.4 ng/g on a
wet wt basis for the PCB congeners, DDTs and HCB.
Quantification was done within the linear range of the
detector. Non-detected constituents were assigned a
value of zero. Residues in 100% of the samples wereconfirmed by gas–liquid chromatography-mass spec-
trometry (Fisons MD 800). Concentrations of PCBs,
DDTs and HCB, means of duplicate measurements are
presented as ng/g on a wet weight basis.
M.M. Storelli et al. / Marine Pollution Bulletin 48 (2004) 743–748 745
2. Results and discussion
The concentrations of PCB congeners and DDTs (ng/
g wet weight) in the liver of angler fish are presented inTable 2. Residue levels of PCBs were 140–3217 ng/g wet
wt, with a mean concentration of 1249 ng/g wet wt. The
concentrations of DDTs were comparable with PCB
levels ranging between 135 and 4684 ng/g wet wt, with a
mean of 1459 ng/g wet wt. Among DDT metabolites,
p; p0-DDE was dominant representing 76% of the total
DDT burden, followed by p; p0-DDT (11.5%), o; p0-DDT
(7.3%), p; p0-DDD (2.6%) and o; p0-DDD (2.3%).A positive correlation between the concentration of
PCBs (Fig. 1(a)) and fish size was observed, indicating
an active uptake with time or a decreasing metabolic
activity of the organisms for these pollutants. Also
DDTs and, clearly, p; p0-DDE (Fig. 1(b)), that was the
predominant component of the total DDT burden, in-
creased with fish size. Many developed nations have
banned the production and use of persistent pesticides,while developing countries have continued to use them,
therefore, through dispersion into atmosphere, these
compounds used in one part of the world, can become
globally distributed. The DDE/DDT ratio can be used
to indicate whether DDT inputs have occurred recently
or in the past in an ecosystem. Aguilar (1984) proposed
that a ratio greater than 0.6 implies the system is rela-
tively stable with no new inputs. The mean ratio foundin the liver of these organisms equal to 10.4 was con-
siderable above this threshold indicating no new inputs
of DDT into the ecosystem.
The pattern of relative concentrations of PCB cong-
eners in the liver tissue was dominated by higher chlo-
rinated congeners. Hexa- and heptachlorobiphenyls
accounted for 69.6% and 16.0% of the total PCB con-
Table 2
PCB congeners and chlorinated pesticides residues in L. budegassa liver (ng/
Congeners Minimum Maximum
PCB 52 ND 23
PCB 60 ND 74
PCB 77b 1 12
PCB 101 ND 53
PCB 105 ND 10
PCB 118 4 357
PCB 126b 3 13
PCB 138 14 586
PCB 153 68 1666
PCB 156 ND 216
PCB 169b ND 8
PCB 180 22 6113
PCB 209 ND 157P
PCB 140 3217P
DDT 135 4684
ND¼ not detected; T¼ traces.a Concentrations expressed on lipid weight.b pg/g w.w.
centrations respectively, followed by penta-, deca- and
tetrachlorobiphenyls with a contribution of 9.9%, 3.2%
and 1.5%, respectively. Hexachlorobiphenyls 153 and
138, were the predominant congeners accounting for49.8% and 13.7% of the total PCB concentrations,
respectively, followed by PCB 156 with percentages of
6.0%. Among pentachlorobiphenyls the congener
exhibiting the greatest levels, with a contribution of
8.3%, was PCB 118, while PCB 101 and 105, detected in
86% and 25% of samples examined, respectively, con-
tributed to the total PCB concentrations in very low
percentages between 0.1% and 1.5%. Among tetrachlo-robiphenyls, PCB 60, detected in 85.7% of samples, was
the dominant congener accounted for 1.1% of the total
PCB load, while PCB 52, encountered in 43% of samples
showed lower percentages (0.3%). Other congeners with
less than 4 chlorine atoms (8, 20, 28 and 35) were below
the limit of detection.
PCBs 153, 138 and 180 represent the prevalent
congeners also in other marine organisms from theAdriatic Sea, i.e. cartilaginous fish Centrophorus granu-
losus and Squalus blainvillei (Storelli and Marcotrigiano,
2001), marine turtles Caretta caretta (Corsolini et al.,
2000; Storelli and Marcotrigiano, 2000a), and dolphins
Tursiops truncatus (Corsolini et al., 1995; Storelli and
Marcotrigiano, 2000b), and Grampus griseus (Storelli
and Marcotrigiano, 2000c). Of particular interest, in the
organisms in question, was the detection of PCB 209. Inthe studies mentioned above, on polychlorobiphenyls
contamination in pelagic marine organisms from South
Adriatic Sea the presence of the decachlorobiphenyl 209
was not encountered in any organism, either fish, rep-
tiles or mammals. The accumulation of PCBs among
the different compartments of an aquatic system is
often predicted by the equilibrium partitioning theory
g w.w.)
Median Mean± standard deviation
9 10± 6 (38)a
11 16± 15 (63)a
4 4± 2 (14)a
21 21± 12 (77)a
4 5± 3 (27)a
102 104± 76 (332)a
7 7± 3 (33)a
169 171± 122 (530)a
620 622± 424 (2814)a
73 78± 51 (263)a
3 4± 1 (18)a
191 199± 138 (677)a
32 44± 35 (185)a
1268 1249± 802 (4372)a
1347 1459± 998 (4423)a
R2 = 0.6433
0
500
1000
1500
2000
2500
3000
3500
0 5 10 15 20weight (kg)
ng/
g w
.w.
R2 = 0.6974
R2 = 0.6736
0
1000
2000
3000
4000
5000
0 5 10 15 20weight (kg)
ng/g
w.w
.
(a) (b)
Fig. 1. Correlation between PCBs (a), DDTs (r) and p; p0-DDE (�) (b) versus specimen weight (kg).
0
0.1
0.2
0.30.4
0.5
0.6
0.70.8
0.9
1
PCB52
PCB60
PCB77
PCB101
PCB105
PCB118
PCB126
PCB138
PCB153
PCB156
PCB169
PCB180
PCB209
Fig. 2. X/153 ratios in the liver of L. budegassa.
Table 3
Mean concentrations of mono- and non-ortho coplanar PCBs (ng/g
wet weight) and their 2,3,7,8-TCDD toxic equivalents (TEQs pg/g wet
weight) in liver of L. budegassa
Mono-ortho TEF Concentrations TEQs
118 0.000005 104 0.52
105 0.000005 5 0.03
156 0.000005 78 0.39
Total 187 0.94
Non-ortho
77a 0.0001 4 0.0004
126a 0.005 7 0.035
169a 0.00005 4 0.0002
Total 15 0.04
Total 187.02 0.98
a pg/g w.w.
746 M.M. Storelli et al. / Marine Pollution Bulletin 48 (2004) 743–748
(Mackay, 1991). This theory focuses primarily onphysical and chemical mechanisms to estimate chemical
fate, ignoring biological mechanisms that may also
mediate the transfer of toxic chemical such as PCBs in
aquatic systems. The feeding behaviour, reflecting po-
sition of the organisms in the food chain, as well as
habitat constitute important factors influencing PCB
profile (Thompson et al., 1999). Angler fish, members of
the Lophiidae family, are large benthic organisms andvery active predators both on sandy, detrital and muddy
bottoms as well as on bottoms rich in vegetation, where
eat a wide array of fish, including spiny dogfish, skates,
eels, herrings, cods, haddocks and flounders. The diet of
angler fish, constituted by prey organisms with high
position in the trophic web, could affect the selective
accumulation of highly chlorinated congeners which
tend to be accumulated more efficiently than lowlychlorinated ones along the food chain (Muir et al., 1988;
Borga et al., 2001). Moreover, benthic organisms, are
exposed to sedimentary PCBs via several routes, as di-
rect contact with sediment, respiration of interstitial
water and incidental ingestion of sediment. PCBs, in
particular the heavier congeners, are known to associate
themselves with the finer fraction of sediment (Pierard
et al., 1996); these finer particles being more present inthe water above the sediments as suspended matter,
might be more available to benthic organisms. There-
fore, the lifestyle of angler fish, may be one of the factors
affecting the composition of PCB congeners. The
organism’s physiology with respect to xenobiotic elimi-
nation and physicochemical properties of the com-
pounds may also play an important role influencing
PCB pattern. Biotransformation of PCBs in animals canbe explained as the ratio of a PCB concentration con-
gener to that of a more persistent congener. PCB-153,
extremely persistent, is a good indicator of biological
alteration of PCBs (Tanabe and Tatsukawa, 1983;
Barrie et al., 1992; Kannan et al., 1995). In our samples
such ratio showed (Fig. 2) a depletion in the lower
chlorinated congeners, while the congeners most per-
sistent were PCBs 118, 138 and 180, followed by PCBs156 and 209. On the other hand, these latter not pos-
sessing adjacent H atoms neither meta–para, nor ortho–
meta positions (PCB 180, PCB 209), or only adjacent H
atoms in ortho–meta positions (PCBs 118, 138 and 156),
belong to the group of difficult to metabolize congeners.
The mono- and non-ortho congeners with coplanar
configuration listed in Table 3 made up together 15% of
the total PCB residue. The concentrations of three
highly toxic non-ortho congeners, such as 3,30,4,40-tetra-chlorobiphenyl (PCB 77), ranged from 1 to 12 pg/g wet
wt (mean 4 pg/g wet wt), 3,30,4,40,5-pentachlorobiphenyl(PCB126) varied between 3 and 13 pg/g wet wt (mean 7
pg/g wet wt) and 3,30,4,40,5,50-hexachlorobiphenyl (PCB169) from 2 to 8 pg/g wet wt (mean 4 pg/g wet wt).
Therefore, PCB 126 accounted for most of the PCB
M.M. Storelli et al. / Marine Pollution Bulletin 48 (2004) 743–748 747
coplanar content with percentage of 46.7%, followed by
PCB 169 and 77 showing the same percentages of 26.7%.
Regarding mono-ortho PCBs, 55.6% consisted of PCB
118, 41.7% was PCB 156, while only 2.7% was ascribedto PCB 105. The fate and effects of pollutants are largely
governed by the presence of various xenobiotic metab-
olizing enzymes. Among them, the cytochrome P 450
mono-oxygenase system and conjugating enzymes are
the two most important multi-enzymatic systems in-
volved in the metabolism and detoxication of xenobiotic
compounds (Garc�ıa et al., 2000). Generally, in unex-
posed organisms the characteristic feature in the patternof non-ortho coplanar PCBs is PCB 77>PCB
126>PCB 169 (Watanabe et al., 2000), the same of that
observed in commercial mixture. This kind of pattern
denotes a little or non-existent metabolic activity (Tan-
abe et al., 1988; Ryan et al., 1993; Corsolini et al., 1995).
In fact the evidence of the enzymatic activity consists in
the decreasing of the PCB 77 concentration, due to
metabolic degradation. Another parameter used whe-ther there has been an enzyme induction following
exposition to PCBs, is concentration ratio between
PCB77/PCB169 and PCB126/PCB169. Low values of
such ratios are assumed to induce hepatic microsomal
enzyme following exposition to levels of PCBs. For
example, in the case of humans exposed to very high
PCB concentrations, such as ‘‘Yusho poisoning victims’’
the PCB77/PCB169 and PCB126/PCB169 ratios were1.8 and 1.9, respectively, while in healthy people were
3.8 and 3.9 (Tanabe et al., 1989). High values of PCB77/
PCB169 and PCB126/PCB169 ratios, 13 and 31 respec-
tively, denoting low metabolic activity were also found
in the liver of C. caretta specimens from Adriatic Sea
(Corsolini et al., 2000). In our samples the non-ortho
PCB concentration pattern 126> 169¼ 77 suggest a
certain enzymatic activity, which seems to be confirmedby low values of PCB77/PCB169 and PCB126/PCB169
ratios, equal to 1.0 and 1.8, respectively.
Structure–function relationships for PCB congeners
have identified two major structural classes of PCB that
elicit ‘‘TCDD-like’’ responses, namely the non-ortho
coplanar PCB 77, 126, 169 and mono-ortho PCB 105,
118, 156. These congeners have been considered in order
to estimate the toxicity potential (TEQs) of PCB expo-sure, using the TEFs for fish developed by van den Berg
et al. (1998) (Table 2). The mean total 2,3,7,8-TCDD
equivalent of 6 congeners was 0.98 pg/g. The isomers
with higher TEQs values were mono-ortho congeners
(0.94 pg/g) than non-ortho (0.04 pg/g). Calculations of
TEQs showed that PCB 118 contributed most to the
total toxicity (53.1%), followed by PCB 156 (39.8%)
PCB 126 (3.6%) and PCB 105 (3.1%). The comparisonof the TEQ values relatively to non- and mono-ortho
PCBs in the liver of the fish in question with those in the
same organ of other marine and terrestrial organisms
showed extremely low levels when compared with the
levels of TEQs in the liver of cormorant (1680 pg/g w.w.)
(Guruge and Tanabe, 1997), marine mammals stranded
along Atlantic coastal waters of Florida (18–660 pg/g
w.w.) (Watanabe et al., 2000), and elasmobranch (166–197 pg/g w.w.) (Storelli and Marcotrigiano, 2001), but
very close to those in marine turtles (0.25 pg/g w.w.)
from Adriatic Sea (Corsolini et al., 2000).
Considering the above observation it is plausible to
assume that the damage of TCDD-like toxicity tends to
be relatively modest. However, particular care and
attention should be paid when applying the toxicological
profiles obtained from one species to another species,because it is generally known that the degree of toler-
ance for toxic compounds is strictly species-dependent.
This observation implies the need for future studies on
bioaccumulation issues of these toxic compounds in
different marine species.
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