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Levels and toxicity of polycyclicaromatic hydrocarbons in marinesedimentsAnastasia Nikolaou, Maria Kostopoulou, Giusy Lofrano,

Sureyya Meric, Andreas Petsas, Maria Vagi

The occurrence of polycyclic aromatic hydrocarbons (PAHs) in the marine environment has attracted the attention of the

scientific community, as these compounds are frequently detected in seawater and sediments at increasing levels and can have

adverse health effects on marine organisms and humans. Several PAHs are potential human carcinogens and are included in the

priority list of the European Union�s Water Framework Directive (2000/60/EC). Research regarding their environmental levels

requires their determination by gas-chromatography and liquid-chromatography techniques, which have been developed and

optimized, especially for marine-sediment samples. Results of sample analyses reveal the increasing occurrence of many species

of PAHs worldwide, especially in marine sediments, where they finally accumulate, mostly in areas near intense industrial

activities. In parallel, research on the toxicity of PAHs and their mixtures is continuing and is aiming to provide more insight into

the health risks associated with the levels of PAHs in the environment.

ª 2009 Elsevier Ltd. All rights reserved.

Keywords: Health risk; Human carcinogen; Marine organism; Marine sediment; PAH; Polycyclic aromatic hydrocarbon; Priority list; Sample

analysis; Seawater; Toxicity

1. Introduction

The occurrence of polycyclic aromatichydrocarbons (PAHs) in the environmenthas been documented for several decades.During the 1950s, they were reported tobe present in food and cigarette smoke,and afterwards they were also detected inair samples, due to traffic-exhaust gases.In the marine environment, PAHs havebeen detected after oil spills since 1967.Monitoring programs have been intro-duced in order to evaluate the backgroundlevels of PAHs, as they can also derivefrom natural sources, and to estimatelevels of environmental pollution fromPAHs [1]. Many laboratories in the worldare analyzing samples and revealing theincreasing presence of PAHs in manyenvironmental matrices, especially marinesediments [2–27] (Table 1).

Several PAHs have been identified aschemical carcinogens. In 1775, an asso-ciation between the incidence of scrotalcancer in chimney sweeps and theirexposure to soot was noted by the British

Anastasia Nikolaou*, Maria Kostopoulou, Andreas Petsas, Maria Vagi

University of the Aegean, Faculty of Environment,

Department of Marine Sciences,

University Hill,

81100 Mytilene,

Greece

Giusy Lofrano

University of Salerno,

Department of Civil Engineering,

84084 Fisciano (SA),

Italy

Sureyya Meric

Present address: University of Naples, Federico II,

Department of Biological Sciences,

Section of Physiology and Hygiene,

Ecotoxicology Research Laboratory (ERL-UNINA),

I-80134 Naples,

Italy

*Corresponding author. Tel.: +30 2251036848; Fax: +30 2251036809;

E-mail: nnikol@aegean.gr

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0165-9936/$ - see front matter ª 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.trac.2009.04.004 6530165-9936/$ - see front matter ª 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.trac.2009.04.004 653

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Tab

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surgeon Sir Percival Pott [28]. In 1915, Japaneseworkers induced skin tumors in rabbits by applying coaltar [29]. The principal carcinogenic component of coal-tar pitch was identified as benzo[a]pyrene in 1933 [1]. Inthe decades that followed, the evolution of chromato-graphic techniques provided the opportunity for thedetermination of many other PAH species in aqueoussamples and more complex environmental matrices (e.g.,marine sediments [2–27]).

Procedures for the analysis of PAHs from sedimentsinclude Soxhlet extraction [30,31] ultrasonic extraction,microwave dissolution, pressurized liquid extraction(PLE) and supercritical fluid extraction (SFE) [32–38].Solid-phase microextraction (SPME) techniques havealso started to attract interest for sediment samples [19].Clean-up procedures [e.g., column chromatographyusing a variety of adsorbents (e.g., acid-modified andbase-modified silica gel, alumina and Florisil)] andaddition of chemical modifiers (e.g., Na4EDTA) have alsobeen developed to increase the extraction efficiency forPAHs from sediments [14]. The final extract is typicallyanalyzed by gas-chromatography (GC) or liquid-chro-matography (LC) techniques [1–27,39–41].

Scientific interest in the quality of marine sediments isquite recent and has especially increased in the past10 years in relation to application of the European Union(EU)�s Water Framework Directive (WFD) (2000/60/EC)[42]. One of the main objectives of the WFD is achieve-ment and preservation of ‘‘Good Chemical Status’’ of

surface waters of the EU member states by 2015, while,in parallel, the monitoring of their quality is required. Incoastal areas where various human activities take place,the effects have already become obvious, having social,economic and environmental impacts [5,12]. However,the quality of marine waters is directly related to thequality of sediments, which are the final compartment ofstorage of a large number of xenobiotics, including manyPAH species [2–27]. According to the WFD, PAHs areconsidered priority substances due to their environ-mental behavior and their toxic effects [41]. Some PAHsare considered potentially carcinogenic for humans,particularly benzo[a]anthracene, chrysene, benzo[b]flu-oranthene, benzo[a]pyrene and benzo[ghi]perylene [43](Table 2). EU Directive 98/83/EC, which is relevant towater intended for human consumption, has set a limitof 0.10 lg/L for the total concentration of benzo[b]flu-oranthene, benzo[k]fluoranthene, benzo[ghi]peryleneand indeno[1,2,3-cd]pyrene, while EU Decision 2455/2001/C included PAHs in a WFD list of priority sub-stances and EU Directive 2008/105/EC set regulatorylimits for PAHs in inland, transitional and coastal waters[44]. The Convention for the Protection of the MarineEnvironment of the North-East Atlantic (OSPAR Con-vention) has been in force since 1998 and has beenratified by Belgium, Denmark, Finland, France, Ger-many, Iceland, Ireland, Luxembourg, Netherlands,Norway, Portugal, Sweden, Switzerland and UnitedKingdom, and approved by the European Community

Table 2. Carcinogenic action of PAHs [46,47]

PAHs Indicator of carcinogenesis1 Total estimation2 EPA Classification (EPA, 1994)3 Toxicity Equivalency Factor(TEF) (EPA; 1993)

Acenaphthylene D 0.001Anthracene I 3 D 0.01

Benzo[a]anthracene S 2A B2 0.1Benzo[b]fluoranthene S 2B B2 0.1Benzo[k]fluoranthene S 2B B2 0.1

Benzo[b]fluorene I 3Benzo[g,h,i]perylene I 3 D 0.01

Benzo[a]pyrene S 2A B2 1Benzo[e]pyrene I 3

Chrysene L 3 B2 0.01Fluoranthene I 3 D 0.001Fluorene I 3 D 0.001Indeno[1,2,3-c,d]pyrene S 2B B2 0.1Perylene I 3Phenanthrene I 3 D 0.001Pyrene I 3 D 0.001Dibenzo[a,h]anthracene S 2A B2 5

Dibenzo[a,h]pyrene S 2BBenzo[c]fluorene I 3

Benzo[j]fluoranthene S 2BDibenzo[a,e]pyrene S 2B

1No adequate data for humans.For animals: I, Insufficient data; L, Limited data; S, Sufficient data.21, Carcinogen for humans; 2A, Probable carcinogen for humans; 2B, Possible carcinogen for humans; 3, Not classified regarding carcino-genicity for humans.3D, not classifiable as to human carcinogenicity; B2, probable human carcinogen.

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and Spain [45]. However, no limits have yet been set formarine sediments, although they are the final receiversof PAHs in the marine environment.

The US Environmental Protection Agency (EPA) hasdetermined that contaminated sediments pose bothecological and human health risks throughout the USA.It is estimated that roughly 10% of the sediments fromUS lakes, rivers and bays are contaminated with toxicchemicals that can adversely affect aquatic organisms orimpair the health of wildlife or humans, who consumecontaminated fish or shellfish [46,47]. Contaminatedsediments are important sources of pollution and mayresult in ecotoxicological effects, which can occur at alllevels of biological organization, from molecular to eco-system [48,49]. Moreover, remobilization of toxic pol-lutants, which increases their bioavailability, can occurwhen contaminated sediments are disturbed anddredged [50]. US EPA has listed as priority pollutants 16PAHs in wastewaters and 24 PAHs in soils, sediments,hazardous solid wastes, and groundwater [51]. Longet al. have proposed sediment-quality guidelines forPAHs in the USA [52].

2. Sources and fate of PAHs in the marineenvironment

The introduction of PAHs into the marine environmentis performed via different processes [e.g., combustion oforganic matter (pyrolytic origin), slow transformation of

organic matter on the geothermal scale (petroleumhydrocarbons), and degradation of biogenic material(diagenesis)]. Naturally-formed PAHs are biosynthesisproducts or come from oil welling up, and they usuallyoccur in marine sediments at very low levels in the range0.01–1 ng/g dry weight (d.w.) (background concentra-tions), but, in some cases, their background levels insediments can be much higher (e.g., in anoxic sediments,perylene can occur at levels >400 ng/g [53] and back-ground concentrations of PAHs >1300 ng/g have beenmeasured in Alaskan sediments [54]).

PAHs also originate from anthropogenic sources (e.g.,industrial production, transportation and waste incin-eration). Human activities are important sources of anumber of PAHs in the aqueous environment with thehighest values being recorded in estuaries and coastalareas, and in areas with intense vessel traffic and oiltreatment.

Based upon diagnostic ratios and/or predominance ofdifferent PAH congeners, Zaghden et al. [55] classifiedthree sources of PAHs: petrogenic; pyrolytic; and, natu-ral oil seeps of diagenetic origin [56]. Petrogenic PAHsare related to petroleum, including crude oil and its re-fined products. Biogenic PAHs are generated by bioticprocesses or by early stages of diagenesis in marinesediments (e.g., perylene). Pyrogenic PAHs are generatedby combustion of fossil fuels (coal and oil) and recentorganic material (e.g., wood) [20]. The use of ratios ofPAH components of the same molecular mass has been

Sediment sample

Extraction Soxhlet

Ultrasonic SPE, SFE, microwave

Clean up Solvent exchange

SPE cartridges

GC-MS HPLC-DAD

Figure 1. The typical procedure followed for the analysis of PAHs in marine sediments.

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established as a reliable method of inferring PAH sourcesand diagenesis of PAHs according to:

(i) the different thermodynamic stability of congeners;(ii) the characteristic composition of different PAH

sources; and,(iii) changes in the relative abundances of PAHs be-

tween source and sediment [56].Fluoranthene and pyrene (mass 202) are considered

good indicators of petroleum combustion while phenant-rene and anthracene (mass 178) are commonly used todistinguish between combustion and petroleum sources.PAHs of molecular masses 228 (benzo[a]anthracene andchrysene) and 276 (indeno[1,2,3-cd]pyrene and benzo-[ghi]perylene) are used less frequently as PAH-sourceindicators and few guidelines have been established fortheir interpretation [57,58].

PAHs take part in various physical, chemical andbiological processes in the marine environment, the mostcommon of which are:� adsorption and desorption;� sedimentary deposition;� atmospheric release;� biodegradation; and,� abiotic degradation

Higher molecular-weight compounds are associatedprimarily with particles and are likely to be removed bydry deposition, while lower molecular-weight com-pounds are found primarily in the gas phase and aresubject to transformation or removal by photochemicaldegradation [11].

The adsorption of PAHs occurs on the surface of or-ganic and inorganic particles. The rate of adsorption ispositively affected by the content of organic matter in theparticles. The final fate of PAHs is generally sedimentarydeposition, after transport in the water column, as re-ported for material collected in sediment traps [55].However, in situ factors (e.g., portioning of PAHs be-tween sorbed and aqueous phases, bioturbation andselective microbial degradation) may affect the observedcomposition of PAHs that results [59].

PAH molecules adsorbed on the sediments can besubject to slow-rate biodegradation and transformationto other forms via the actions of benthic organisms. Thehalf-life of fluoranthene in surface sediments ranges froma few days to some years, depending on the environ-mental conditions. Degradation of compounds contain-ing more than six rings has not been documented, whilethere is no evidence of degradation of PAHs in deepsediments [60,61]. The dissolution of PAHs in water islow, especially higher molecular-weight compounds.The dissolved molecules can be subject to photolysis andto chemical and biological oxidation, with both processesbeing inversely related to the content of dissolved or-ganic matter [59].

Abiotic removal due to photochemical reactions ofPAHs is important. Photo-oxidation is faster, with a half-

life of a few hours in the presence of intense sunlight.PAHs containing three or more rings in their moleculesshow intense ultraviolet (UV) absorbance at wavelengths>300 mm, which exist in sunlight, resulting in oxidationof the molecules. The photo-oxidation reactions of dis-solved PAH molecules include transfer of energy from thetriplet (excited) state of the aromatic system, resulting inproduction of atomic oxygen, which reacts with thecompound producing peroxide. Photolysis or pyrolysis ofendoperoxides produces various reaction products viadealkylation and breaking the ring [61–63]. By contrast,photo-oxidation of PAHs in the adsorbed phase is notperformed via peroxides. The compounds are photo-oxi-dized at a higher rate in adsorbed phase than in solution.Since PAHs in the environment occur combined withparticles, this kind of photo-oxidation has greater envi-ronmental importance. The photo-oxidation half-life forbenzo[a]pyrene under different conditions has been re-ported to be <1 day. Non-substituted anthracenes easilyform photodimers by reaction of a molecule in an excitedstate with another molecule in the basic state.

Atmospheric deposition, river run off, domestic andindustrial outfalls, and direct spillage of petroleum orpetroleum products are the main sources of anthropo-genic PAHs in the marine environment. Knowledge ofsources and possible transport pathways in aquaticsediments is the first step to effective pollution control.Vessels make a significant contribution by transportingthese compounds in the marine environment. Especiallyin harbors, where the renewal of waters through contactwith the open sea is limited, the accumulation of PAHscan be significant [2,64,65].

The processes of industrialization and urbanizationthat are rapidly gathering pace in some countries (e.g.,India and China) increase the potential for associatedincreases in anthropogenic PAHs [63]. Studies focusedon heavily contaminated, developing coastal regionsshow that contamination levels in those regions aregrowing to those of polluted industrialized zones indeveloped countries [59].

Once PAHs are introduced into the marine environ-ment, physical transport and mechanical factors aremostly responsible for their observed distribution insediments [59]. They are present in both dissolved andparticulate phases. Due to their low solubility and theirhydrophobic nature, they readily associate with inor-ganic and organic suspended particles and may accu-mulate in sediments at high concentrations [9].

3. Analytical methods

Fig. 1 shows a generalized typical procedure for thedetermination of PAHs in marine sediment.

Table 3 summarizes information on the analyticalmethods applied by different researchers and the ana-

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Table 3. Analytical methods and concentration range reported by different researchers for PAHs in marine-sediment samples

PAHs studied Sample preparation Column and temperatureprogram used

Range of total concen-tration of PAHs

Ref.

Naphthalene; Acenaphthylene; Acenaphthene; Fluorene;Phenanthrene; Anthracene; Fluoranthene; Pyrene;Benz[a]anthracene; Chrysene; Benzo[b]fluoranthene;Benzo[k]fluoranthene; Benzo[a]pyrene;Benzo[ghi]perylene; Dibenz[a,h]anthracene;Indeno[1,2,3-cd]pyrene

Soxhlet extraction with dichloromethane for 16 h DB-5MS (70�C for 4 min,10�C/min to 300�C, held for10 min)

3.15–144.89 lg/kg d.w. [2]

Anthracene; Phenanthrene; Fluoranthene; Pyrene;Benzo[a]anthracene; Chrysene; Benzo[b]fluoranthene;Benzofluoranthene; Benzo[e]pyrene; Benzo[a]pyrene;Perylene; Indeno[1,2,3-cd]pyrene; Benzo[ghi]perylene;Coronene

Pressurized solvent extraction with a mixture ofdichloromethane and acetone (3:1, v/v) at 175oCand 10.5 MPa for 5 min.

HP5-MS (70�C for 2 min,30�C/min to 150�C,increased to 310�C at 4�C/min and held for 10 min)

6–8399 ng/g d.w. [5]

Rotary preconcentration, clean up with 5% H2Odeactivated silica-gel column, elution with elutedwith 20 mL hexane/dichloromethane (3:1, v/v).Activated copper treatment, pass through fullyactivated silica-gel column, elution with hexane/dichloromethane (3:1, v/v).

Naphthalene; Acenaphthylene; Acenaphthene; Fluorene;Phenanthrene; Anthracene; Fluoranthene; Pyrene;Benzo(a)anthracene; Chrysene; Benzo(b,k)fluoranthene

Ultrasonic extraction with dichloromethane for30 min, then shaken overnight, and againultrasonication for 30 min.

RTX5-MS (110�C for 2 min,25�C/min to 310�C, 5 min,held for 15 min)

0.383 lg/g d.w. [4]

Centrifugation for 10 min at 3000 rpm, rotaryevaporation to 3–6 ml, nitrogen evaporation to0.5 ml.

Benzo(a)pyrene; Benzo(ghi)perylene;Dibenzo(ah)anthracene; Indeno(1,2,3-cd)pyrene

Clean up with Enviropack 18 column (3 ml/500 mg), elution with 10 ml of 75:25 (v/v)pentane: dichloromethane mixture.Concentration with nitrogen to 0.3 ml, addition of2 ml hexane and concentration again to 0.5 ml.

Naphthalene; 2 methyl naphthalene; 1 methylnaphthalene; Acenaphthylene; Acenaphthene; Fluorene;Phenanthrene; Anthracene; 2 methyl anthracene; 9 methylanthracene; Fluoranthene; Pyrene; 1 methyl pyrene;Benzo(a)anthracene; Chrysene; Benzo(b)fluoranthene;Benzo(k)fluoranthene; Benzo(a)pyrene; Perylene;Indeno(1,2,3-cd)pyrene; Dibenzo(a,h)anthracene;Benzo(ghi)perylene

Centrifugation for 10 min, addition of Na2SO4

and activated copper.Equity-5 (40�C for 2 min,40�C/min to 100�C, 10�C/min to 200�C, 30�C/min to325�C, held for 8 min)

72–18381 lg/kg d.w. [9]

A. Soxhlet extraction for 24 h, usingdichloromethane-pentane 1:1 solvent mixture.Filtration of the extracts through a pre-cleanedPasteur pipette filled with solvent-rinsed glasswool and pre-cleaned anhydrous Na2SO4,(previously rinsed with dichloromethane) andconcentration in a rotary evaporator to finalvolume around 2 ml.Evaporation with nitrogen to dryness anddissolution in 1 ml solution containing theperdeuterated internal standards in cyclohexane(0.2 mg/L each): acenaphthene d10;phenanthrene d10, chrysene d12 and perylened12.B. Ultrasonication with pentane-dichloromethane1:1 v/vC. Ultrasonication with dichloromethane

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Fluoranthene; Pyrene; Benzo(a)anthracene; Chrysene;Benzofluoranthene; Benzo(e)pyrene; Indeono[1,2,3-cd]pyrene; Benzo[ghi]perylene

Soxhlet extraction with dichloromethane/methanol (v/v: 2:1) for 48 h. Clean up with silica/alumina column chromatography

HP-5 (50oC for 1 min, 10oC/min to 180oC, for 7 min,10oC/min to 230oC, for25 min, 20oC/min to 280oC,for 5 min)

68–1500 ng/g d.w. [27]

Naphthalene; Acenaphthylene; Acenaphthene; Fluorene;Phenanthrene; Anthracene; Fluoranthene; Pyrene;Benz[a]anthracene; Chrysene; Benzo[b+k]fluoranthenes;Benzo[e]pyrene; Benzo[a]pyrene; Indeno[1,2,3-cd]pyrene; Dibenz[a,h]anthracene; Benzo[g,h,i]perylene

Soxhlet extraction with acetone–hexane (1:1),desulfurization with activated copper,evaporation with nitrogen, purification by liquidchromatography on Florisil cartridge, furtherclean up on a silica-gel column

PTE-5 GC-MS, EI mode(70 eV electron energy), withion source, quadrupole andtransfer line temperatures of200�C, 100�C and 290�C,respectively

380–12,750 lg/kg d.w. [68]

Naphthalene; Acenaphthylene; Acenaphthene; Fluorene;Phenanthrene; Anthracene; Fluoranthene; Pyrene;Benz[a]anthracene; Chrysene; Benzo[b]fluoranthene;Benzo[k]fluoranthene; Benzo[a]pyrene; Indeno(1,2,3-cd)pyrene; Dibenzo(a,h)anthracene; Benzo[ghi]perylene;2-methylnaphthalene; 1-methylnaphthalene; 2,6-dimethylnaphthalene; 1,3,5-trimethylnaphthalene; 1-methylnaphthalene; Biphenyl; Benzo[e]pyrene; Perylene

Soxhlet extraction with methylene chloride.Extensive clean up by Si/Al columnchromatography and HPLC with size-exclusioncolumn

DB-5MS 1.5 min at 60�C,first rate 4�C/min to 300�C,isothermal pause 10 min at300�C

8.80–18 500 ng/d.w. [59]

Naphthalene; 2-methylnaphthalene; Acenaphthylene;Acenaphthene; 2,3,5-trimethylnaphthalene; Fluorene;Phenanthrene; Anthracene; 2-methylanthracene;Fluoranthene; Pyrene; 9,10-dimethylanthracene;Benzo(c)phenanthrene; Benzo(a)anthracene; Chrysene;Benzo(b)fluoranthene; Benzo(k)fluoranthene; 7,12-dimethylbenzo(a)anthracene; Benzo(a)pyrene; 3-methylchloranthrene; Indeno(1,2,3-cd)pyrene;Dibenzo(a,h)anthracene; Benzo(g,h,i)perylene;Dibenzo(a,l)pyrene; Dibenzo(a,h)pyrene

Ultrasonication with dichloromethane, shakenovernight and ultrasonicated again,centrifugation, evaporation under a nitrogenstream, clean up with solid-phase extractioncolumn

DB5MS 60�C to 310�C at arate of 15�C/min, finalholding time 13 min.

2005: 36 ± 3–1908 ± 114 ng/g d.w.2004: 28 ± 3–312 ± 24 ng/g d.w.

[67]

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lytical conditions used in each case. As can be seen fromTable 3, the HP-5 chromatographic column or equiva-lent is used most (in GC-MS analysis).

Clean-up procedures are applied by many researchersin order to increase the sensitivity of the methods, usu-ally by silica/alumina columns, after desulfurization byactivated copper [66,67,59,68].

Some studies still utilize the traditional time-consum-ing, but effective, Soxhlet extraction, while HPLCinstrumentation is also used in some cases with rela-tively good results.

4. Levels of PAHs in marine sediments

PAHs are widespread contaminants in oceans. However,their concentrations in sediments of coastal bays, estu-aries and continental shelves are often much higher dueto greater pressures from specific anthropogenic inputs,suggesting direct influence of these sources on pollutant-distribution patterns [56]. Due to the chemical compo-sition of seawater, the occurrence of PAHs, which arevery hydrophobic compounds, will be at very low levelsof concentration (<1 ng/L), in contrast to concentrationin other aqueous matrices (e.g., wastewater, river water,rainwater and sediments), where, depending on thestudy area, the corresponding values are in the range1 ng/g d.w. to >100 ng/g d.w. [12]. Due to theirhydrophobic character, PAHs tend to adsorb onto theparticulate matter so that they are transported to andaccumulate in sediments.

Sprovieri et al. [56] found that the priority PAHs insamples of surface sediment collected from Naples harborwere in the range 9–31,774 ng/g. Three-ring and four-ring PAHs appeared dominant in the sediments studied,with median values of concentration generally greaterthan 60–70% of the total concentration of the PAHs.There was no correlation between grain size or totalorganic carbon and the distribution of PAHs or singlecongeners. Te Naples harbor showed a median and arange of variability greater than most other Mediterra-nean and European ports (e.g., Sardinia, Corsica, Spain,France and England) but similar to those measured incommercial harbors in the USA, the Middle East andAustralia. Total PAH concentrations measured by Vaneat al. [74] in sediments from the Mersey Estuary (UK)were in the range 626–3766 mg/kg, which were inter-mediate compared to other UK estuaries with similarhistories of industrialization and urbanization. Themolecular indices in this case suggested mainly pyroliticinputs, augmented by a variety of industrial or petro-genic sources.

A major part of recent studies on hydrocarbon pollu-tion has focused on the northwestern part of the Medi-terranean Sea [69,70], but there is a tremendous lack ofinformation regarding the eastern Mediterranean Sea

[71] and the southern Mediterranean Sea, and data arescarce for the coasts of Algeria and Egypt [72,73]. There istherefore an urgent need for better assessment of hydro-carbon contamination for the whole Mediterranean Sea.

5. Toxicity of PAHs in marine sediments

The ecotoxicity of individual PAHs or mixtures of someof PAHs has been investigated using different bioassays.The most indicative toxicity end-points have beenchanged in line with the species tested.

In one toxicity study of individual PAHs, the effect ofbenzo[a]pyrene (BaP) on Mytilus edulis fed daily withIsochrysis galbana algae that had previously been kept inthe presence of BaP for 24 h was investigated in terms ofblood-cell lysosomal membrane damage (neutral red-dyeretention assay) and induction of digestive glandmicrosomal mixed-function oxygenase (MFO) parame-ters [BaP hydroxylase (BPH) and NADPH-cytochrome c(P450) reductase activities]. It was reported that thebioaccumulation of BaP in tissues (and to a lesser extentin digestive gland microsomes) of M. edulis increasedwith both increasing BaP and algal exposure concen-trations, and over time. This pointed to impact on M.edulis in line with BaP exposure possibly due to a directeffect of BaP on the integrity of the blood-cell lysosomalmembrane. An increase in NADPH-cytochrome creductase activity was explained due to a transient re-sponse of the digestive gland microsomal MFO system toBaP exposure [74].

BaP was also reported to induce infertility in the malereproductive system. Microsomes isolated from liver andtestes of rat, mouse, hamster, ram, boar, bull andmonkey were incubated with BaP. Post incubation, theethyl-acetate-extracted samples were analyzed for BaPand metabolites by reversed-phase HPLC with fluores-cence detection. Given the ability of BaP 7-8-diol 9, 10-epoxide, 3-, and 9-hydroxy BaP to bind with DNA andform adducts, Smith et al. concluded that a risk waslikely to arise from accumulation of BaP metabolites intesticular tissues [75].

Ethoxy resorufin dealkylase (EROD) inducing potencyof 10 PAHs, generally used in risk assessment studies,was measured in H4IIE rat hepatoma cell line in vitrobioassays. The responses of the PAHs investigated toEROD activity varied:� anthracene (Ant) and phenanthrene (Phe) exhibited

no response;� naphthalene (Nap) gave no or a very weak response;� fluoranthene (Fla) and benzo[ghi]perylene (BghiP)

showed weak responses at the highest doses;� indeno [1,2,3-cd]pyrene (IP), benz[a]anthracene

(BaA), benzo[a]pyrene (BaP), chrysene (Chr) andbenzo[k]fluoranthene (BkF) displayed full bell-shapeddose-response curves.

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BaP EROD induction equivalency factors (BaP-IEFs)were calculated and increased in the order Ant < Phe< Fla < Nap < BghiP < IP < BaA < BaP < Chr < BkF [76].

Although there has been a severe toxic outcome fromindividual PAHs, as reported in Table 4 for the toxicity ofsome individual PAHs to Mytilus galloprovincialis [77],there was found almost no dose-response relationship forPAHs in the presence of complex mixtures (e.g., sedi-ments).

A positive relationship was found in a study performedon the sediments collected in the Izmit Bay, Turkey,where bulk and elutriate samples were toxic toPhaeodactylum tricornutum tested in batch bioassays. Thesediments collected from the inner sites of the bay werereported to be contaminated with Cd, Hg, As and PAHs,which were consistent with the high organic carboncontents. Bulk sediments displayed toxicity to themicroalgae throughout the bay [78].

However, in a survey conducted on marine sedimentsin Santa Monica bay, spatial and temporal patternsindicated that toxicity was most strongly associated withthe historical disposal of municipal wastewater sludge.The statistical significance between response by bio-assays and chemical analyses was negative (e.g., sea-urchin fertilization correlated negatively withconcentration of zinc, silver, copper, cadmium, totalPCBs and total PAHs, while amphipod survival had asignificant negative correlation only for silver [79]).

In the extracts of freeze-dried surface sediment samplesfrom the southern North Sea (fraction <63 lm), theconcentrations of the PAHs measured were in the range2.6–200 lg/kg d.w., with the highest concentrations atnear-shore locations and river mouths. Responses in themulti-bioassays toxicity tests were found to vary. Theresponses in Microtox and Mutatox genotoxicity assayswere low with higher responses observed at near-shorelocations. Relevant responses were obtained in umu-Cgenotoxicity and ER-CALUX assays for estrogenicity. Atthe oyster grounds, DR-CALUX responses appeared to belinked to the occurrence of larger PAHs (4–6 rings).By applying a non-destructive clean-up procedure,DR-CALUX responses were significantly higher thanthose obtained in the current protocol [80].

The 16 US EPA priority pollutant PAHs were inves-tigated in sediments of the Niger Delta comprising 2–6-ring congeners with molecular mass of 128–278.Concentrations of total PAHs in the range 20.7–72.1 ng/g d.w. showed no correlation with the toxicitybioassays of Vibrio fischeri and Lemna minor [81]. Sim-ilar results were reported by Bihari et al. [82], whofound that the organic extracts of the superficial sedi-ments collected from the coastal area of Rovinj(Northern Adriatic, Croatia) showed toxic potential thatwas consistent with the sediment type, but no corre-lation was observed between toxicity measured byMicrotox assay and concentrations of total PAHs andPAH congeners. The genotoxicity assessment of theorganic extracts from the sediment showed no signifi-cant genotoxic potential in the bacterial umu-test. Byusing hemolymph of M. galloprovincialis, the DNAdamage was positively related to total PAHs at foursampling sites, but the highest DNA damage was notobserved at the site with the highest total PAH contentin the sediment [82].

6. Conclusions and outlook

Due to continuously increasing anthropogenic activities,management of the pollution from sediments in coastalareas is attracting more attention. PAHs are character-ized by high toxicity and have been included in thepriority substances of the WFD. The distributions ofPAHs in the environment and potential human healthrisks have become the focus of much attention. Highermolecular-weight compounds are associated primarilywith particles and are likely to be removed by drydeposition, while lower molecular-weight compoundsare found primarily in the gas phase and are subject totransformation or removal by photochemical degrada-tion. Their presence in marine sediments combined withother potentially toxic compounds can result in negativeeffects, which have yet to be investigated to any greatextent, mainly due to lack of appropriate methodologyand the complexity of the subject matter. At present,significant research is being devoted to optimizing ana-

Table 4. Toxicity reference values for Mytilus larval development [77]

Compound Maximum observed porewater concentration (lg/L) 48-h EC50 (lg/L) Ref.

Anthracene* 0.3 4260 [83]Fluorene* <0.1 1260 [84]Fluoranthene* 1.1 58.8 [83]Phenanthrene* <0.1 410 [84]Pyrene* 1.0 >11900 [83]Quinoline <0.1 4300 [84]

Note: Asterisks indicate a compound identified as a COPC based on comparison of bulk sediment concentrations with numerical sedimentquality criteria (BCWLAP, 2003). PAH TRVs include a 10-fold uncertainty factor to address potential interspecies differences.

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lytical methodologies for the determination of traceconcentrations of PAHs in complex matrices (e.g., sedi-ments). For the southern Mediterranean Sea, in partic-ular, due to lack of data, there is an urgent need to assesshydrocarbon contamination.

AcknowledgementsThis review paper was inspired in the framework of theNATO project Harbor Sediments Pollution Assessmentand Dredged Material Management (clg 982446).

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Anastasia Nikolaou obtained her BSc (1997) and PhD degree (2002)

in the Department of Environmental Studies, University of the Aegean,

Mytilene, Greece. She has been a lecturer in the Department of Marine

Sciences of the University of the Aegean (Mytilene, Greece) since 2005.

Her research interests include analytical methods for the determination

of toxic priority substances in water and sediment, water quality and

treatment/disinfection by-products, investigation of fate and toxicity of

organic compounds in the environment. She has participated in many

related national and international projects, authored or co-authored a

number of refereed papers and technical reports, and has been editor of

two books and guest editor for Desalination Journal.

Maria Kostopoulou obtained her BSc (1978) in Biochemistry in the

University of Paris VII (France), and her BSc (1981) in Chemistry and

PhD degree (1987) in the Department of Chemistry, University of

Athens, Greece. She has been an external Scientific Researcher in the

Department of the Environment of the University of the Aegean since

1992 and she has been working as an Assistant Professor in the

Department of Marine Sciences of the University of the Aegean (Myti-

lene, Greece) since 2001. Her research interests include analytical

methods for the determination of priority substances in environmental

matrices (wastewater, water and sediments), as well as toxicity eval-

uation of individual compounds and mixtures by the use of marine

microalgae. She has participated in many related national and inter-

national projects.

Giusy Lofrano holds BS and MSc Degrees (2003) in Civil Engineering

and PhD degree (2007) in Environmental Engineering from University

of Salerno, Italy. She is currently working on the application of Fenton

oxidation, photo-Fenton oxidation and ozonation to high-strength

wastewaters, particularly in the leather-tanning industry, to achieve

an economically feasible and environmentally friendly integrated

wastewater treatment. Her research interests are in the fields of bio-

logical treatment of wastewater, advanced oxidation processes, and

industrial pollution control. She has been co-author of articles on

constructed wetlands and advanced oxidation processes, she has par-

ticipated in related national and international projects and she is cur-

rently assisting the didactic activity of Wastewater Treatment Plant-I

and II courses at the Engineering Faculty of University of Salerno.

Sureyya Meric holds BS, MSc and PhD degrees in Environmental

Engineering from Istanbul Technical University (Istanbul, Turkey). She

has been working in this field for 20 years. Her post-doc studies were

focused on ecotoxicology of many chemicals and complex mixtures.

She has developed expertise in chemical and biological treatment of

wastewater, wastewater reuse, water treatment and disinfection, tox-

icity of disinfection by-products, activated sludge modeling, inhibition,

industrial pollution control, water quality and management, aquatic

and sediment toxicity monitoring. Impact assessment of priority-

emerging pollutants, xenobiotics and their removal by advanced oxi-

dation processes, and groundwater remediation. She has been inves-

tigator or co-ordinator of many national and international projects,

and a member of environmental organizations, committees and the

editorial boards of international journals.

Andreas Petsas holds BS (1998) and PhD (2006) degrees in Envi-

ronmental Studies from the University of the Aegean, Faculty of the

Environment. He has worked on kinetics of removal (hydrolysis, pho-

todegradation) of organophosphorous insecticides from various envi-

ronmental matrices, as well as on the toxicity of these compounds to

marine algae. He has participated in several national and international

projects on these subjects. Since 1999, he has been a scientific col-

laborator in the Water and Air Quality Laboratory of the Department of

Environmental studies of the University of the Aegean, and, since

2006, he is an adjunct lecturer at the Department of Marine Sciences of

the University of the Aegean. His research interests include develop-

ment and optimization of gas-chromatography analytical methods for

determination of organic pollutants in environmental samples and he

has co-authored several papers in international scientific journals.

Maria Vagi holds a BS degree in Chemistry (University of Thessalo-

nica, 1997), and a PhD degree (2007) in Environmental Studies,

University of the Aegean, Faculty of the Environment. She has worked

on kinetics of removal (hydrolysis and photodegradation) of several

categories of insecticides and organic pollutants from various envi-

ronmental matrices, as well as on the toxicity of these compounds to

marine algae. She has participated in several national and interna-

tional projects on these subjects. She has been a researcher in the

Water and Air Quality Laboratory from 1997 until 2007, and, since

Trends in Analytical Chemistry, Vol. 28, No. 6, 2009 Trends

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2000, she has been working as a laboratory-technical staff member at

the Department of Marine Sciences. Her research interests include

development and optimization of gas-chromatography analytical

methods for determination of organic pollutants in environmental

samples and she has co-authored several papers in international sci-

entific journals.

Trends Trends in Analytical Chemistry, Vol. 28, No. 6, 2009

664 http://www.elsevier.com/locate/trac