Environmental occurrence and biota concentration of phthalate esters in Epe and Lagos Lagoons, Nigeria

lable at ScienceDirect

Marine Environmental Research 108 (2015) 24e32

Contents lists avai

Marine Environmental Research

journal homepage: www.elsevier .com/locate /marenvrev

Environmental occurrence and biota concentration of phthalate estersin Epe and Lagos Lagoons, Nigeria

Aina O. Adeogun a, Oju R. Ibor a, Emmanuel D. Omogbemi a, Azubuike V. Chukwuka a,Rachel A. Adegbola c, Gregory A. Adewuyi b, Augustine Arukwe d, *

a Department of Zoology, University of Ibadan, Ibadan, Nigeriab Department of Chemistry, University of Ibadan, Ibadan, Nigeriac Department of Chemistry, The Polytechnic, Ibadan, Nigeriad Department of Biology, Norwegian University of Science and Technology (NTNU), Høgskoleringen 5, N-7491 Trondheim, Norway

a r t i c l e i n f o

Article history:Received 5 February 2015Received in revised form5 April 2015Accepted 7 April 2015Available online 15 April 2015

Keywords:Phthalate estersAquatic pollutionDeveloping countryLagos and Epe lagoons

* Corresponding author.E-mail address: [email protected] (A. Arukwe).

http://dx.doi.org/10.1016/j.marenvres.2015.04.0020141-1136/© 2015 Elsevier Ltd. All rights reserved.

a b s t r a c t

The high global occurrence of phthalates in different environmental matrixes has resulted in thedetection of their metabolites in human urine, blood, and breast milk, indicating a widespread humanexposure. In addition, the notorious endocrine disrupting effects of phthalates have shown that theymimic or antagonize the action of endogenous hormones, consequently producing adverse effects onreproduction, growth and development. Herein, we have studied the occurrence of phthalate esters (PEs)in water, sediment and biota of two lagoons (Epe and Lagos) in Nigeria. Two fish species (Tilapia gui-neensis, and Chrysichthys nigrodigitatus) and a crustacean (the African river prawn - Macrobrachiumvollenhovenii) were analyzed for PEs levels using a HPLC method and the derived values were used forcalculating bioconcentration factor (BCF), biota-sediment accumulation factor (BSAF) and phthalatepollution index (PPI) in the biota and environment. We observed that the growth and health condition ofthe fish species were normal with a k-factor of >1. Sediment PE levels were compared with water, at bothlagoons showing concentration pattern that is characterized as DEHP ¼ DEP > DBP. We observed thatDBP was the predominant compound in T. guineensis, C. nigrodigitatus and African prawn, at both lagoons,showing organ-specific differences in bioconcentration (BCF and BSAF) patterns in the fish species. Whilethere were no observed consistency in the pattern of PE concentration in fish organs, elevated DBP levelsin different fish organs may be related to fish habitat and degradation level of phthalates. Low con-centration of DEHP, compared with DBP and DEP, was measured in fish organs and whole prawn body.The BSAF values for DEHP were lowest, and highest for DBP for all species at both lagoons, and DEHPeasily accumulated more in the sediment (sediment PPI ¼ 0.28 and 0.16 for Epe and Lagos lagoon,respectively). Overall, our findings suggest a broader environmental and human health implication of thehigh PE levels in these lagoons since they represent significant sources of aquatic food resources for theneighboring communities.

© 2015 Elsevier Ltd. All rights reserved.

1. Introduction

Phthalic acid esters (phthalates) are ubiquitous environmentalcontaminants worldwide, due to their broad usage in flexibleplastics and consumer products (Zeng et al., 2008b; Dominguez-Morueco et al., 2014). Phthalates are used to enhance the plas-ticity of industrial polymers, resulting in their widespread usage in

a broad range of products that include e food packaging, toys,paints or internal polyvinyl chloride (PVC) coatings, constructionmaterials, personal care products and cosmetics (such as nail var-nish), electronic and medical devices and pediatric articles (such asbags for intravenous fluids, breathing masks or umbilical cathe-ters), among several others products (Berman et al., 2009; Calafatet al., 2004; Kimber and Dearman, 2010; Yan et al., 2009;Dominguez-Morueco et al., 2014). In addition, the widespreadapplication and use of phthalates by the general population, hasalso resulted in their notorious presence as solid waste products ofindustrial and domestic activities (Kimber and Dearman, 2010).

A.O. Adeogun et al. / Marine Environmental Research 108 (2015) 24e32 25

In the European Union (EU), an effective ban was placed on the useof six phthalates e namely: (di-(2-ethylhexyl) phthalate (DEHP),butylbenzyl phthalate (BBP), di-n-butyl phthalate (DBP), di-isononyl phthalate (DINP), di-isodecyl phthalate (DIDP) and din-octyl phthalate (DNOP)) in the production and sale of toys andinfant articles that could be introduced into the mouth of childrenyounger than three years old (Directive, 2005/84/EC; EuropeanParliament and the Council, 2013).

The environmental increase and distribution of phthalates hasgenerated strong societal concerns since they are shown to causecancer, developmental abnormalities and reproductive effects thatinclude reduction in sperm counts in males (Su et al., 2012).Furthermore, due to the high global occurrence of phthalates indifferent environmental matrices, their metabolites have beendetected in human urine, blood, and breast milk, indicating awidespread human exposure (Guo et al., 2012; Hines et al., 2011).Phthalates have been reported to possess overt endocrine dis-rupting properties, and shown to mimic or antagonize the action ofendogenous hormones, which consequently result in adverse ef-fects on reproduction, growth and development (Crisp et al., 1998;Crocker et al., 1983; Fisher, 2004). Although endocrine mode ofaction is not well understood for phthalates, it may likely bedependent on developmental timing and dosing regimes(Akingbemi et al., 2001). Studies on rodents and avian species haveidentified Leydig cells as one of the main targets of phthalate-induced reproductive toxicity (Akingbemi et al., 2004; Bello et al.,2014). In humans, exposure to phthalates may be associated withadverse health effects that include, but not limited to neuro-developmental problems (Whyatt et al., 2012), low semen quality(Huang et al., 2011), miscarriages (Toft et al., 2012), asthma andallergies (Hsu et al., 2012), breast cancer progression (Hsieh et al.,2012) and obesity (Hatch et al., 2010), most likely by targetingthe peroxisome proliferator (PP) pathways.

From a developing country perspective, the increasing con-sumption of consumer products in Nigeria, consequently generatesincreased amount of solid waste per capita, with associated highproportion of organic material, compared to developed countries(Arukwe et al., 2012; Visvanathan and Glawe, 2006). Recently, wereported high concentrations of DEHP and DBP in leachates andsediment from a municipal waste deposit site at Owerri, Nigeria,whose levels in the sedimentswereup to1000 timeshigher than therun-off water sample from the same sites (Arukwe et al., 2012) andhigh environmental and biota levels of phthalates from twomunicipal water supply lakes in Ibadan, Southwestern Nigeria(Adeogun et al., submitted). A similar pattern was previously re-ported in several other rivers, showing higher levels of DEHP andDBP and lower levels of DMP and DEP (Yuan et al., 2002). The Epeand Lagos lagoons are part of the Southern lagoon system in Nigeriaand are important for foraging and breeding of fish species. Theselagoons contribute substantial portions of wild type artisanal fishproduction in Nigeria and serve as fishing habitats as well as nurs-ery, feeding and spawning grounds for a diverse number of fishspecies. In addition, Lagos lagoon is also a major seaport in Nigeria.The high level of waste materials discharged into the Lagos lagoonhas progressively polluted the shores of the lagoon (Eruola et al.,2011). As a result, several locations along the Lagoon are currentlyfacing an increasing number of serious environmental and ecolog-ical challenges. Most of these challenges are direct results of ur-banization and high commercial activities (including, but notlimited to seaport activities) along the axis of the Lagoon, contrib-uting to a massive deterioration of water quality and contaminantloadwith overt regional consequences on theaquatic ecosystemandon the human health of the user groups (Eruola et al., 2011).

The interplay between urbanization, commercial activities andecological/human health effects in the Lagos lagoon system is of

societal concern, and calls for an urgent management and sus-tainable use of the lagoon. The level of contaminant load to thelagoon is highest at the harbor area with a decreasing trend to-wards the metropolitan end of the lagoon (Eruola et al., 2011). Inaddition, the Epe area of the lagoon is putatively, the least influ-enced by anthropogenic contamination. However, the degree ofcontaminant load in the lagoon varies, even within the differentareas (Eruola et al., 2011). Therefore, a comprehensive and detailedcontaminant monitoring process is urgently needed in order todiscern the actual environmental contaminant load and biologicalconsequences. Therefore, the aim of the present study was toinvestigate the levels of phthalic acid esters in environmental(water and sediment) and biota samples of the two lagoon systems(Epe and Lagos) in Nigeria.

2. Materials and methods

2.1. Sampling sites

The Epe lagoon is located between longitudes 5�300e5�400E andlatitudes 3�500e4�100N. The lagoon receives River Osun that drainsa number of cities and agricultural lands (Fig. 1A). The study area isbordered on the west by a number of cultivated lands and receiveswoodwastes from local wood processing outfits located at the bankof the lagoon. The lagoon is used for transportation of timber logs(possible source of wood particles and leachates) from the villagesto the city of Lagos and is the second largest contributor to theviable commercial artisanal fisheries of the southern lagoon com-plex. The lagoon houses a major jetty at Epe, where different formsof anthropogenic wastes within and around the jetty are indis-criminately deposited (Edokpayi et al., 2010).

The Lagos lagoon is the largest of four lagoon systems in the Gulfof Guinea (Webb,1958). It stretches for about 250 km from Cotonouin the Republic of Benin to the western edge of the Niger delta. Thelagoon includes the forest belt and receives a number of importantlarge rivers such as Yewa, Ogun, Ona and Osun rivers, drainingmorethan 103626 km2 of the country and empties into the AtlanticOcean (Fig. 1B). The Lagos opening is by far the largest and forms anextensive harbor, which serve as the major outlet of fresh waterfrom the lagoon system during the rainy season. The central body ofthe lagoon is located between longitude 3� 230 and 3� 400E andlatitude 6� 220 and 6� 380N. This brackish region is of interest forcoastal dynamics and transport of pollutants from the hinterlandand the immediate shores of the lagoon (Ajao and Fagade, 1990).The lagoon provides places of abode and recreation, means oflivelihood and transport, a dumpsite for residential and industrialdischarge and a natural shock absorber to balance forces within thenatural ecological system. About 80e85% of the industries inNigeria are located in Lagos State and they all discharge their ef-fluents into the Lagos lagoon. The effluents discharged are mainlyuntreated, and very few industries have treatment plants in Nigeria(IPEP, 2006).

2.2. Chemicals and reagents

Acetonitrile, dichloromethane, sodium carbonate, anhydroussodium sulfate and aluminium oxide, N-hexane and ethyl acetatewere of HPLC grade, di-2- ethylhexylphthalate (DEHP), diethylph-thalate (DEP) and dibutylphthalate (DBP) standards were pur-chased from SigmaeAldrich (Switzerland).

2.3. Sample collection

Biota samples (n ¼ 150/species) of Chrysicthys nigrodigitatus,Tilapia guineensis and the invertebrate Macrobrachium

A.O. Adeogun et al. / Marine Environmental Research 108 (2015) 24e3226

vollenhovenii; water and sediment samples were collected fromfour stations, including two landing sites of Lagos and Epe lagoonsfromMayeJuly 2011. Fish were identified according to Idodo-Umeh(2003). All fish samples were collected in aluminium foil lined icechest, anaesthesized on ice and transported to the laboratory formorphometric measurements and PE analysis. The sediment sam-ples (n ¼ 3) were collected in clean stainless steel containers using

Fig. 1. Map of Epe (A) and Lagos (B) lagoons showing t

a van Veen grab and transported to the laboratory. The pH wasdetermined with a water Cyber scan 1000 pH meter, and the sed-iments were acidified to a pH 2 with concentrated hydrochloricacid (HCl) in order to prevent the alteration of organicmatter due tomicrobial activities, air dried and stored in aluminum foil prior toextraction. Water samples (n ¼ 3) were collected using 1L reagentbottles with aluminum foil-lined lid that was thoroughly washed

he sampling sites and surrounding environments.

Table 1BPhysicochemical parameters at the Epe and Lagos lagoons during the samplingperiods.

A.O. Adeogun et al. / Marine Environmental Research 108 (2015) 24e32 27

and rinsed with acetone, double distilled water and methanol. ThepH were recorded and acidified to a pH 2 with concentrated HClimmediately (Blair et al. 2009).

Parameter Lagoon

Epe Lagos

pH 7.21 ± 0.26 7.4 ± 0.18Dissolved Oxygen (DO: mg/L) 2.51 ± 0.72 2.51 ± 0.72Conductivity (mS cm�1) 200.50 ± 66.03 618.20 ± 27.40Total dissolved solids (TDS: mg/L) 226.14 ± 57.1 336.50 ± 18.6Salinity (mg/L) 0.27 ± 0.12 4.02 ± 0.34

2.4. Biometric measurement and physicochemical analysis

Fish biometric data (total length (cm) and bodyweight (g)) weretaken using a digital Vernier Caliper (Tresna Instruments, GuangxiProvince, China) and an Ohaun digital weighing balance (MettlerInstruments). The condition factor (k-factor) was estimated ask ¼ 100 W/L3. Where k is the condition factor, W is the weight ingrams and L is the total length in centimeters. Temperature wasmeasured at the sampling site using mercury in glass thermometer.The pH, dissolved oxygen (DO), conductivity, total dissolved solids(TDS) and salinity (mg/L) were measured using Consort C933TElectrochemistry meter. The biometric measurements and physi-cochemical parameter values of the lagoons are given in Table 1Aand B, respectively.

2.5. Sample preparation, extraction and analysis

Whole samples of liver and kidney, and 10g of muscle and gillswere collected and homogenized into paste like texture in glassmortar and pestle and later dried using anhydrous Sodium sulfateaccording to USEPA (2012). Water sample (200 mL) was collectedand spiked with butyl benzoate and saturated with 6 g of sodiumchloride to prevent the formation of persistent emulsion. This wasextracted with three portions of 25 mL dichloromethane (DCM).The free fatty acids (FFA) interferences were removed by furtherextraction with sodium carbonate. The organic extracts were thendried with anhydrous sodium sulfate (Ogunfowokan et al., 2006).For the extraction of fish and sediment samples, the following stepswere performed rapidly to avoid loss of the more volatile extract-able compounds. Approximately 5 g of sample were added into theextracting chamber of the Soxhlet extractor. 120 mL of DCM wasintroduced into a round bottom flask, heated for six to eight hoursor cycles for complete extraction, and the extracts where kept in afume hood prior to clean up (Peterson and Freeman,1982). Detailedprotocols, including quality assurance are given in SM1.

3. Statistical analysis

Data are presented as mean and standard deviation. Thephthalate pollution index (PPI) of different sampling events wascalculated in order to compare the total PEs content in the differentenvironmental and biota matrixes using the equation PPI ¼ Cf1 Cf2… Cfn)1/n, where Cfn is the concentration of the PEs in samples(Adeniyi et al., 2008). Bioconcentration factor (BCF) and biota-sediment accumulation factor (BSAF) were calculated as: PE con-centration in organ/concentration in water or sediment, respec-tively. Single factor analysis of variance (ANOVA) was used tocompare phthalate concentration in water, sediment and biota.

Table 1ARelative Condition factor of fish species from Lagos and Epe lagoons.

Species Standard length (cm)

Min Max Mean ± SD

Lagos lagoonC. nigrodigitatus 22.50 29.0 24.74 ± 0.59T. guineensis 12.00 18.0 14.6 ± 1.14Epe lagoonC. nigrodigitatus 25.94 28.5 26.3 ± 0.33T. guineensis 12.0 17.5 14.21 ± 1.07

4. Results

4.1. Water and sediment phthalic ester concentrations

Phthalic ester (DBP, DEHP and DEP) concentrations in waterwere 0.13 ± 0.004, 0.18 ± 0.01 and 0.11 ± 0.01 mg/L, respectively(Fig. 2A) at the Epe lagoon. On the other hand, Epe lagoon sedimentsamples contained DBP, DEHP and DEP concentrations of0.18 ± 0.01, 0.28 ± 0.02 and 0.3 ± 0.03 mg/g, respectively (Fig. 2A). Atthe Lagos lagoon, the average water DBP, DEHP and DEP concen-trations were 0.13 ± 0.01, 0.09 ± 0.01 and 0.09 ± 0.01 mg/L,respectively (Fig. 2B). Lagos lagoon sediment samples containedDBP, DEHP and DEP concentrations of 0.14 ± 0.01, 0.16 ± 0.03 and0.19 ± 0.02 mg/g, respectively (Fig. 2B). Comparatively, there werehigher PE concentration in the sediment compared with ambientwater at both lagoons, and the pattern of PE concentration ischaracterized as DEHP > DBP ¼ DEP, and DBP > DEP ¼ DEHP at theEpe and Lagos lagoons, respectively (Fig. 2).

4.2. Phthalic ester concentrations in biota

T. guineensis: DBP was the dominant PE measured inT. guineensis at both the Epe and Lagos lagoons whose organ con-centration patterns were generally higher in the gills and liver,compared with muscle and kidney (Fig. 3A and B, respectively). Forall the PEs (DBP, DEP and DEHP), tissues levels in T. guineensis werecomparable with respect to the organ distribution patternsshowing DBP > DEP > DEHP (Fig. 3). The higher tissue levels of DBPalso reflected in the higher respective BCF of 3.11 and 2.25 in thegills and liver at Epe Lagoon; and 6.87 and 4.89 in the gills and liverat the Lagos lagoon, respectively (Table 2). The BSAF for T. guineensisfrom the Epe and Lagos lagoons was concomitantly higher for DBP,compared with DEP and lowest for DEHP (Table 3).

C. nigrodigitatus: For C. nigrodigitatus, a different pattern of PEsconcentration in the organs were observed for the Epe and Lagoslagoons (Fig. 4). In the Epe lagoon, the muscle and gills were thehighest DBP, DEP and DEHP accumulating organs (Fig. 4A), while atthe Lagos lagoon, the liver and kidney were the highest accumu-lating organs for DBP, compared with the muscle and gills (Fig. 4B).Furthermore, the kidney of C. nigrodigitatus strongly accumulatedDEP and DEHP at the Lagos lagoon, while the muscle, liver and gills

Body weight (g) k-Factor

Min Max Mean ± SD

184.0 380 242.9 ± 12.69 1.6190.0 189.0 136.9 ± 20.64 1.59

205.5 320.0 270.7 ± 9.04 1.45110.0 198.0 140.17 ± 18.4 1.59

Fig. 2. Concentration of phthalate esters (PEs) in water (mg/L) and sediment (mg/kg) from the Epe (A) and Lagos (B) lagoon, Nigeria. Values represent mean ± standard deviation (SD;n ¼ 3). Different letters indicate significant difference (p < 0.05) between the 3 classes of PEs (DBP, DEP, DEHP) analyzed using one-way ANOVA, while asterisk (*) indicate significantdifference between the concentrations of individual PE in water and sediment by paired student t-test, performed using Origin 8 software (OriginLab, USA). The level of significancewas set at p < 0.05.

Fig. 3. Concentration of phthalate esters (PEs) in Tilapia guineensis organs from Epe (A)and Lagos (B) lagoon, Nigeria. Values represent mean ± standard deviation (SD; n ¼ 3).Different letters indicate organ mean values that are significantly different within eachindividual PE. The level of significance was set at p < 0.05. Paired student t-test, per-formed using Origin 8 software (OriginLab, USA).

A.O. Adeogun et al. / Marine Environmental Research 108 (2015) 24e3228

did not show differences in accumulation patterns (Fig. 4B). ThesePE-specific differences in organ accumulation patterns also resultedin corresponding higher BCF (Table 2) and BSAF (Table 3) for DBP inthese organs at both lagoons.

M. vollenhovenii: In whole animal homogenate of the Africanriver prawn (M. vollenhovenii), a PE concentration pattern showingDBP > DEP > DEHP was measured at the Epe lagoon, while onlyminor differences in PE accumulation pattern was observed in thesame species at the Lagos lagoon (Fig. 5). The differences in PEsconcentration patterns were confirmed by the calculated BCF (2.81,1.64 and 0.34) and BSAF (1.99, 0.61 and 0.10) values forM. vollenhovenii from the Epe lagoon for DBP, DEP and DEHP(Tables 2 and 3, respectively). On the contrary, an opposite BCFpatternwas observed at the Lagos lagoon and shown in Table 2. TheBSAF forM. vollenhovenii, was highest for DBP > DEHP > DEP at theLagos lagoon (Table 3).

4.3. Phthalate pollution index (PPI)

The mean PPI values were significantly higher in sediment withrespective 0.25 and 0.16 at Epe and Lagos lagoon, compared withconcentrations of 0.14 and 0.10 mg/L in water, respectively (SM2,Table 1A and B, respectively). For T. guineensis, the gills and muscleshowed comparatively higher PPI values of respective 0.16 and 0.15,comparedwith liver andkidneywith respectivePPI valueof 0.12 and0.09 at the Epe lagoon (SM2, Table 1A). On the other hand,T. guineensis PPI values at the Lagos lagoon showed that the gills andliver had higher values at respective 0.14 and 0.18, compared withthe kidney and muscle at respective 0.11 and 0.12 (SM2, Table 1B).Furthermore, the muscle of C. nigrodigitatus showed the highest PPIvalue of 0.42 at the Epe lagoon,while the kidney showed the highestPPI value of 0.42 at the Lagos lagoon (SM2, Table 1A and B, respec-tively). M. vollenhovenii showed comparable PPI value at the Epe(0.12) and Lagos (0.24) lagoons (SM2, Table 1A and B, respectively).

5. Discussion

The global scale environmental occurrence of PEs has resulted inthe detection of phthalate metabolites in human urine, blood, andbreast milk, indicating a widespread human exposure (Guo et al.,2012; Hines et al., 2011), producing the endocrine disrupting

Table 2Bioconcentration factor (BCF) of phthalate esters (PEs) in biota from Lagos and Epe lagoons.

PEa Organs Species

Lagos Lagoon Epe Lagoon

T. guineensis C. nigrodigitatus M. vollenhoveniib T. guineensis C. nigrodigitatus M vollenhoveniib

DEHP Muscle 0.46 0.41 1.61 0.41 1.06 0.14Gill 0.21 0.27 0.52 0.66Liver 0.50 0.73 0.17 0.17Kidney 0.94 4.31 0.17 0.32

DEP Muscle 1.74 1.06 1.33 1.81 5.47 1.64Gill 1.70 1.33 0.99 3.00Liver 2.25 1.35 1.53 1.35Kidney 0.98 4.67 1.01 1.22

DBP Muscle 1.92 1.19 1.21 1.68 4.80 2.81Gill 6.87 1.28 3.11 5.82Liver 4.89 3.73 2.25 2.64Kidney 1.52 3.72 1.58 2.67

a Phthalate ester.b Whole body homogenate.

A.O. Adeogun et al. / Marine Environmental Research 108 (2015) 24e32 29

effects that may either mimic or antagonize the action of endoge-nous hormones, consequently resulting in adverse effects onreproduction, growth and development (Crisp et al., 1998; Crockeret al., 1983; Fisher, 2004). Therefore, from a developing countryperspective, a widespread environmental and biota occurrence ofPEs is inevitable because of (i) the high global annual productionand usage of >5 million tonnes, primarily as additives to PVCplastics, industrial solvents and components of several classes ofconsumer products (Huang et al., 2013), (ii) the high volume usageof these chemicals in plastics, personal care products (PCPs) andmany other consumer products (Blount et al., 2000), and (iii)because these compounds are not chemically bound to the prod-ucts in which they are used, and as a result can gradually bereleased into the environment (Kato et al., 2005). Given that indeveloping countries such as Nigeria, there are no effective man-agement systems for solid wastes, PEs represents serious environ-mental and human health concerns in these countries.

5.1. Phthalic ester levels in sediment and water samples

Phthalic esters (PEs) were detected and measured in both waterand sediment at Epe and Lagos lagoons showing that the sedimentcontained significantly higher levels of the individual PE comparedwith water. DEP and DEHPwere themost abundant PEmeasured insediment samples at both lagoons, compared with DBP. Overall,these findings are consistent with previously reported

Table 3Biota-sediment accumulation factor (BSAF) of phthalate esters (PEs) in biota from Lagos

PEa Organs Species

Lagos Lagoon

T. guineensis C. nigrodigitatus M. vollen

DEHP Muscle 0.25 0.22 0.86Gill 0.12 0.15Liver 0.27 0.39Kidney 0.50 2.30

DEP Muscle 0.84 0.51 0.64Gill 0.82 0.64Liver 1.08 0.65Kidney 0.47 2.24

DBP Muscle 1.80 1.12 1.14Gill 6.43 1.20Liver 4.58 3.50Kidney 1.43 3.49

a Phthalate ester.b Whole body homogenate.

environmental PE levels from other parts of the world (Gao et al.,2014; Huang et al., 2008; Langer et al., 2014; Wu et al., 2007). Thehigher sediment PEs concentrations of these compounds is probablyexplained by the lipophilic properties of the PEs that allows them toadsorb well on carbon-rich surfaces (logKoc 1.57- 5.22 for DMP-DEHP (Clara et al., 2010). Recently, we reported high PE levels inenvironmental (water and sediment) samples from twoman-mademunicipal water supply Lakes (Asejire and Eleyele) from South-western Nigeria (Adeogun et al., submitted). The higher concen-trations of PEs measured in sediment samples from the lakes andlagoons confirmed their accumulation potential on solid and parti-cle phases, low transport potential in sediment and high rate ofabsorption. When viewed together, these findings are also consis-tentwith another recent study, showing that PEswere the dominantcompound group detected in all sediment and the run-off watersample from a solid waste dumping site at Owerri, Eastern Nigeria(Arukweet al., 2012). The analysis of the run-offwater from the solidwastedumping site, showed that leachingof themorewater-solublePEs is possible and their transport into receiving rivers or naturalenvironments should therefore be assumed.

PEs are hardly evaporated because of their low volatility,resulting to potential particle-assisted transport during dry seasonsin tropical regions. During manufacturing, the di-esters of PEs arenot chemically bound to the products. Thus, an easy leakage of themost hydrophilic di-ester is expected, compared to the more hy-drophobic variants. The rates and degradation processes of di-

and Epe lagoons.

Epe Lagoon

hoveniia T. guineensis C. nigrodigitatus M. vollenhoveniib

0.27 0.70 0.100.34 0.440.11 0.110.12 0.220.68 2.05 0.610.37 1.120.57 0.510.38 0.461.19 3.40 1.992.21 4.121.60 1.871.12 1.89

Fig. 4. Organ-specific concentration of phthalate esters (PEs) in Chrysichthys nigrodi-gitatus from Epe (A) and Lagos (B) lagoon, Nigeria. Values represent mean ± standarddeviation (SD; n ¼ 3). Different letters indicate organ mean values that are significantlydifferent within each individual PE. The level of significance was set at p < 0.05. Pairedstudent t-test, performed using Origin 8 software (Origin Lab, USA).

Fig. 5. Concentration of Phthalate esters (PEs: mg/g) in whole body homogenate ofMacrobrachium vollenhovenii from Epe and Lagos lagoon, Nigeria. Values representmean ± standard deviation (SD; n ¼ 3). Different letters indicate mean PE values thatare significantly different. The level of significance was set at p < 0.05. Paired student t-test, performed using Origin 8 software (Origin Lab, USA).

A.O. Adeogun et al. / Marine Environmental Research 108 (2015) 24e3230

esters will definitely influence their release properties (Afshariet al., 2004). For example, PEs are known to be soluble in humicsubstances that will be deposited in the sediment at dumping sites,and these will temporarily sink, but will be leached out duringrainfall for onward transport to aquatic sediment where they willmost likely persist for a longer period of time. Asakura et al. (2004)

reported a significant decrease of environmental contaminants inleachates from two landfills during a 20yr period, without a cor-responding decrease in the concentration of DEHP, showing thatwaste deposits might be a long-lasting source for PEs to the naturalenvironment through leachates. Furthermore, the degradationrates of PEs in the aquatic sediments will differ depending onredox-conditions and between PEs; lower half-lives (higherdegradation kinetics) under aerobic condition than anaerobic orfluctuation redox-conditions (Chang et al., 2005a; Roslev et al.,2007; Yuan et al., 2002). Previously, higher half lives of DEHP andDEP was observed in river sediments, while under aerobic condi-tions DEP and DBP showed comparable low half-life, compared toDEHP (Yuan et al., 2002). Consistent with our study at the Epe andLagos lagoons, DBP has been detected at mg/L concentrations inwastewater samples at 6.6 mg/L (Clara et al., 2010; Mohapatra et al.,2011). In Austria, DEHP was reported as the dominant PE measuredinwastewater effluents and run-off samples from roads, containinga maximum of 24 mg/L DEHP (Clara et al., 2010). The relationshipsbetween the levels of phthalate compounds in sediment andaquatic factors, and BSAF for phthalates was investigated in 17Taiwan's rivers, showing that the mean concentrations (range) ofDEHP, butyl benzyl phthalate (BBzP) and DBP in sediment at low-flow season were respective 4.1, 0.22 and 0.14 mg kg/dw, while athigh-flow season the levels were 1.2, 0.13 and 0.09 mg kg/dw(Huang et al., 2008) Furthermore, the authors also reported traceconcentrations of dimethyl phthalate (DMP), DEP and di-n-octylphthalate (DOP) in sediment were found in both the low- andhigh flow seasons (Huang et al., 2008). In view of these environ-mental data, the German production volume for DBP was reducedby a factor of 10 compared to DEHP, between 1999 and 2002(Simoneau et al., 2009). Overall, our findings from the two lagoonsin Nigeria are consistent with the environmental concentrations ofPEs in other parts of the world, showing the environmentalpersistency of PEs, particularly DEHP.

5.2. Phthalic ester levels in biota

In the present study, we measured PEs in two fish species(T. guineensis and C. nigrodigitatus) and one invertebrate (the Afri-can freshwater prawn e M. vollenhovenii). In both the fish speciesand African prawn, DBP was the predominant compound at bothlagoons, showing organ-specific bioaccumulation patterns in thefish species. While there were no observed consistency in thepattern of PE concentration in fish organs and whole body of theinvertebrate, elevated DBP levels in different fish organs may becorrelated with fish habitat and degradation level of phthalates(Yuan et al., 2002; Chang et al., 2005b). Interestingly, DEHP wasmeasured in fish organs and whole prawn body at low concentra-tions, compared with DBP and DEP in our study. For example, DEHPwas the predominant phthalate compound measured in Oreo-chromic niloticus and other fish species from 17 Taiwan Rivers byHuang et al. (2008). While metabolic capacity of the studied specieswas not evaluated in the present study, the correlation betweenpersistent environmental contaminants such as dioxins and poly-chlorinated biphenyls (PCBs) to their habitat and metabolic ca-pacity in biota has been previously reported, showing that fish suchas tilapia is more sensitive to PCBs contaminated sediment than towater (Mackintosh et al., 2004, 2006; Wan et al., 2005).

The biodegradation of PEs in the sediment should be expected toaffect their bioaccumulation (particularly DBP) in an omnivorousfeeder such as C. nigrodigitatus that feeds on seeds, insects, bivalvesand detritus and specializes with age and size to feed on larger fishand decapods; and a voracious herbivore, such as T. guineensis, thatfeeds on water plants, epipthyton and some invertebrates. Forexample, previous reporthas shownthat less than6%ofDEHP infine

A.O. Adeogun et al. / Marine Environmental Research 108 (2015) 24e32 31

sediment particles is readily available for microbial degradation(Marttinen et al., 2004). As a result, the lower DEHP concentrationsmeasured in C. nigrodigitatus and T. guineensis may be explained byingestion and digestion of coarse particles or sediment dwellingfood preys containing more DBP and DEP, than DEHP. Furthermore,the African freshwater prawn (M. vollenhovenii) is an omnivorousdetritivore that feeds on detritus and snails, and was shown in thisstudy to accumulate higher DBP, than DEP, and lowest for DEHP. Anexposure study in Europe showed that diet is a significant source ofexposure to DEHP and DBP in the general population (Wormuthet al., 2006). The higher concentration of DBP and DEP, comparedwith DEHP in these species most probably reflects the environ-mental behavior of DEHP. Previous report have shown that DEHP,longer and/or branch alkyl PEs, more easily undergo sorption insediment and are resistant to degradation (Zeng et al., 2008a). Thepersistency of DEHP in sediment is probably enhanced due tolimited light penetration that reduces photodegradation of PEs(Zeng et al., 2008a), while biodegradation may represent thedominant mechanism for PEs elimination in sediments (Stapleset al., 1997). It should be noted that DEHP was the highest concen-trating PE measured in sediment samples from both lagoons in thepresent study and this is also in accordancewith our recent report intwomunicipalwater supply lakes in SoutheasternNigeria (Adeogunet al. submitted). This observation is in accordance with previousstudies showing the importance of sediment as a sink for these PEsas has been frequently demonstrated in lakes, rivers and marineenvironments (Klamer et al., 2005; Lin et al., 2003; Liu et al., 2014;Zeng et al., 2008a).

In accordance with our recent study (Adeogun et al., submitted),the BSAF for PEs in the two fish species at both lagoons weregenerally comparable to the BCF values. The BSAF values for DEHPwere lowest, and highest for DBP for all species at both lagoons. Weobserved that DEHP easily accumulated in the sediment (sedimentPPI ¼ 0.28 and 0.16 for Epe and Lagos lagoon, respectively). Thelower BSAF of DEHP, compared with DBP and DEP, observed in thepresent study may be explained based on the possibility that theprimary food sources for C. nigrodigitatus and T. guineensis wereprobably not sediment or benthic dominating organisms. Further-more, BSAF in benthic animals might also change as the molecularweight changes from low (DBP, DEP) to high (DEHP) PEs. However,the species and PE related differences in BCF and BSAF observed inthe present study may also reflect the fact that physicochemicalproperties of organic pollutants in the environment and differencesin temporal bioavailability, metabolic capacity and rates, and theoctanol-water partition coefficient (Kow) may directly affect theirabsorption and elimination in organisms, including fish (Burkhard,2003; Maund et al., 2002). Therefore, all the above variables mayhave, individually and/or collectively affected the accumulation ofPEs in the species studied in the present study.

In accordance with the present study, phthalates are lipophiliccompounds, and their adsorption to carbon-rich surfaces (logKoc1.57- 5.22 for DMP-DEHP) has been reported (Clara et al., 2010). It isimportant to note that the PPI values showed that the sediment is asink for PEs. For example, DEHP is notoriously known to producedevelopmental and endocrine disrupting effects (Knudsen et al.,1998; Li et al., 2013; Zhu et al., 2005), which has resulted in itsrestricted use by the European Union (EU). The reported environ-mental and biota PE concentrations in the present study are com-parable with concentration measured in other developing andindustrialized countries (Yuan et al., 2002; Zeng et al., 2008a;Simoneau et al., 2009; Clara et al., 2010). For example, DEHP wasthe dominant PE compound in a study from Austria and run-offsamples from roads contained a maximum of 24 mg/L (Clara et al.,2010). The higher BCF and BSAF of DBP, compared to DEHP andDEP, observed in Nigerian environments, probably reflect a more

rapid bioavailability of DBP due to its higher water solubility(Simoneau et al., 2009). The PE levels in the sediment samples fromlakes and lagoons in southwestern Nigeria, combined with recentlyobserved concentrations at a solid waste dump site from a differentpart in eastern Nigeria (Arukwe et al., 2012), are comparable to thecompound distribution patterns and concentration range reportedin many other countries (Asakura et al., 2004). There is a commondenominator in these studies from Nigeria that directly compareswith previously reported studies in several other rivers (Yuan et al.,2002), showing higher sediment levels of DEHP, and lower levels ofDBP and DEP. Degradation rates of PEs differ depending on redox-conditions and between PEs; with lower half-lives (higher degra-dation kinetics) under aerobic conditions than in anaerobic orfluctuating redox conditions (Chang et al., 2005a; Roslev et al.,2007; Yuan et al., 2002). In river sediments, DEHP and DEP havehigher half-lives than DBP, while under aerobic conditions DEP andDBP show similarly short half lives compared to DEHP (Yuan et al.,2002). Therefore, for environmental and human health reasons, thehigh environmental and biota PE levels that has been reportedNigeria, the presence of PEs and other chemicals of emergingconcern, with toxic or endocrine disrupting properties are ofserious concern. The reason for this is that the lakes and lagoons aresignificant sources of drinking water and aquatic food resourcesthat sustain life for the neighboring communities.

Acknowledgments

This work was partly supported by the Norwegian ResearchCouncil (AA).

Appendix A. Supplementary data

Supplementary data related to this article can be found at http://dx.doi.org/10.1016/j.marenvres.2015.04.002.

References

Adeniyi, A., Dayomi, M., Siebe, P., Okedeyi, O., 2008. An assessment of the levels ofphthalate esters and metals in the Muledane open dump, Thohoyandou, Lim-popo Province, South Africa. Chem. Cent. J. 2, 9.

Afshari, A., Gunnarsen, L., Clausen, P.A., Hansen, V., 2004. Emission of phthalatesfrom PVC and other materials. Indoor Air 14, 120e128.

Ajao, E.A., Fagade, S.O., 1990. A study of sediment and community in Lagos Lagoon.Oil Chem. Pollut. 7, 85e117.

Akingbemi, B.T., Youker, R.T., Sottas, C.M., Ge, R., Katz, E., Klinefelter, G.R.,Zirkin, B.R., Hardy, M.P., 2001. Modulation of rat Leydig cell steroidogenicfunction by di(2-ethylhexyl)phthalate. Biol. Reprod. 65, 1252e1259.

Akingbemi, B.T., Ge, R., Klinefelter, G.R., Zirkin, B.R., Hardy, M.P., 2004. Phthalate-induced Leydig cell hyperplasia is associated with multiple endocrine distur-bances. Proc. Nat. Acad. Sci. U. S. A. 101, 775e780.

Arukwe, A., Eggen, T., Moder, M., 2012. Solid waste deposits as a significant sourceof contaminants of emerging concern to the aquatic and terrestrial environ-ments e a developing country case study from Owerri, Nigeria. Sci. Total En-viron. 438, 94e102.

Asakura, H.,Matsuto, T., Tanaka,N., 2004. Behaviorof endocrine-disrupting chemicalsin leachate from MSW landfill sites in Japan. Waste Manag. 24, 613e622.

Bello, U.M., Madekurozwa, M.C., Groenewald, H.B., Aire, T.A., Arukwe, A., 2014. Theeffects on steroidogenesis and histopathology of adult male Japanese quails(Coturnix coturnix japonica) testis following pre-pubertal exposure to di(n-butyl) phthalate (DBP). Comp. Biochem. Physiol. Part C 166, 24e33.

Berman, T., Hochner-Celnikier, D., Calafat, A.M., Needham, L.L., Amitai, Y.,Wormser, U., Richter, E., 2009. Phthalate exposure among pregnant women inJerusalem, Israel: results of a pilot study. Environ. Intern. 35, 353e357.

Blair, J.D., Ikunomou, M.G., Kelly, B.C., Surridge, B., Gobas, F.A.P.C., 2009. Ultra-tracedetermination of phthalate ester metabolites in sea water, sediments and biotafrom an urbanised marine inlet by LC/ESI-MS/MS. Environ. Sci. Technol. 43,6262e6268.

Blount, B.C., Milgram, K.E., Silva, M.J., Malek, N.A., Reidy, J.A., Needham, L.L.,Brock, J.W., 2000. Quantitative detection of eight phthalate metabolites in hu-man urine using HPLC-APCI-MS/MS. Anal. Chem. 72, 4127e4134.

Burkhard, L.P., 2003. Factors influencing the design of bioaccumulation factor andbiota-sediment accumulation factor field studies. Environ. Toxicol. Chem. 22,351e360.

A.O. Adeogun et al. / Marine Environmental Research 108 (2015) 24e3232

Calafat, A.M., Needham, L.L., Silva, M.J., Lambert, G., 2004. Exposure to di-(2-ethylhexyl) phthalate among premature neonates in a neonatal intensive careunit. Pediatrics 113, e429e434.

Chang, B.V., Chiang, F., Yuan, S.Y., 2005a. Anaerobic degradation of nonylphenol insludge. Chemosphere 59, 1415e1420.

Chang, B.V., Liao, G.S., Yuan, S.Y., 2005b. Anaerobic degradation of di-n-butylphthalate and di-(2-ethylhexyl) phthalate in sludge. Bull. Environ. Contam.Toxicol. 75, 775e782.

Clara, M., Windhofer, G., Hartl, W., Braun, K., Simon, M., Gans, O., Scheffknecht, C.,Chovanec, A., 2010. Occurrence of phthalates in surface runoff, untreated andtreated wastewater and fate during wastewater treatment. Chemosphere 78,1078e1084.

Crisp, T.M., Clegg, E.D., Cooper, R.L., Wood, W.P., Anderson, D.G., Baetcke, K.P.,Hoffmann, J.L., Morrow, M.S., Rodier, D.J., Schaeffer, J.E., Touart, L.W.,Zeeman, M.G., Patel, Y.M., 1998. Environmental endocrine disruption: an effectsassessment and analysis. Environ. Health Perspect. 1 (106 Suppl. l), 11e56.

Crocker, J.F., Blecher, S.R., Safe, S.H., 1983. Chemically induced polycystic kidneydisease. Prog. Clin. Biol. Res. 140, 281e296.

Directive N 2005/84/EC of the European Parliament and of the Council of 14December 2005 amending for the 22nd time Council Directive 76/769/EEC onthe approximation of the laws, regulations and administrative provisions of themember states relating to restrictions on the marketing and use of certaindangerous substances and preparations (phthalates in toys and childcare arti-cles). OJEC 344, 2005, 40e43, 27 December 2005.

Dominguez-Morueco, N., Gonzalez-Alonso, S., Valcarcel, Y., 2014. Phthalate occur-rence in rivers and tap water from central Spain. Sci. Total Environ. 500e501,139e146.

Edokpayi, C.A., Uwadiae, R.E., Njar, C.E., 2010. Non insect benthic Phytomacrofaunaorganism water quality relations in tropical coastal Ecosystem: Impact of landbased pollutants. J. Am. Sci. 6, 213e222.

Eruola, A.O., Ufoegbune, G.C., Ojekunle, Z.O., Makinde, A.A., Ogunyemi, I.O., 2011.Analytical investigation of pollutants in lagos coastal waters, Nigeria. Adv. Anal.Chem. 1, 8e11.

European Parliament and the Council, 2013. Directive N 2013/39/UE EuropeanParliament and of the Council of 12 August 2013 amending Directives 2000/60/EC and 2008/105/EC are amended in relation to priority substances in the fieldof policy waters. OJEC 226, 1e17, 24 August 2013.

Fisher, J.S., 2004. Environmental anti-androgens and male reproductive health:focus on phthalates and testicular dysgenesis syndrome. Reproduction 127,305e315.

Gao, D., Li, Z., Wen, Z., Ren, N., 2014. Occurrence and fate of phthalate esters in full-scale domestic wastewater treatment plants and their impact on receivingwaters along the Songhua River in China. Chemosphere 95, 24e32.

Guo, Y., Zhang, Z., Liu, L., Li, Y., Ren, N., Kannan, K., 2012. Occurrence and profiles ofphthalates in foodstuffs from China and their implications for human exposure.J. Agric. Food Chem. 60, 6913e6919.

Hatch, E.E., Nelson, J.W., Stahlhut, R.W., Webster, T.F., 2010. Association of endocrinedisruptors and obesity: perspectives from epidemiological studies. Intern. J.Androl. 33, 324e332.

Hines, C.J., Hopf, N.B., Deddens, J.A., Silva, M.J., Calafat, A.M., 2011. Estimated dailyintake of phthalates in occupationally exposed groups. J. Expo. Sci. Environ.Epidemiol. 21, 133e141.

Hsieh, T.H., Tsai, C.F., Hsu, C.Y., Kuo, P.L., Hsi, E., Suen, J.L., Hung, C.H., Lee, J.N.,Chai, C.Y., Wang, S.C., Tsai, E.M., 2012. n-Butyl benzyl phthalate promotes breastcancer progression by inducing expression of lymphoid enhancer factor 1. PloSOne 7, e42750.

Hsu, N.Y., Lee, C.C., Wang, J.Y., Li, Y.C., Chang, H.W., Chen, C.Y., Bornehag, C.G.,Wu, P.C., Sundell, J., Su, H.J., 2012. Predicted risk of childhood allergy, asthma,and reported symptoms using measured phthalate exposure in dust and urine.Indoor Air 22, 186e199.

Huang, P.C., Tien, C.J., Sun, Y.M., Hsieh, C.Y., Lee, C.C., 2008. Occurrence of phthalatesin sediment and biota: relationship to aquatic factors and the biota-sedimentaccumulation factor. Chemosphere 73, 539e544.

Huang, L.P., Lee, C.C., Hsu, P.C., Shih, T.S., 2011. The association between semenquality in workers and the concentration of di(2-ethylhexyl) phthalate inpolyvinyl chloride pellet plant air. Fertil. Steril. 96, 90e94.

Huang, J., Nkrumah, P.N., Li, Y., Appiah-Sefah, G., 2013. Chemical behavior ofphthalates under abiotic conditions in landfills. Rev. Environ. Contam. Toxicol.224, 39e52.

Idodo-Umeh, G.O., 2003. Freshwater Fishes of Nigeria Taxonomy, Ecological Note,Diet and Utilization. I. Idodo-Umeh Publishers, Edo State, Nigeria.

IPEP, 2006. The International POPs Elimination Project (IPEP), Assessment of theLagos Lagoon for POPs Sources, Types and Impacts. Friends of the Environment(FOTE), Nigeria - Anglophone Africa, 123pg.

Kato, K., Silva, M.J., Needham, L.L., Calafat, A.M., 2005. Determination of totalphthalates in urine by isotope-dilution liquid chromatography-tandem massspectrometry. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 814, 355e360.

Kimber, I., Dearman, R., 2010. An assessment of the ability of phthalates to influenceimmune and allergic responses. Toxicol 271, 73e82.

Klamer, H.J., Leonards, P.E., Lamoree, M.H., Villerius, L.A., Kerman, J.E., Bakker, J.F.,2005. A chemical and toxicological profile of Dutch North Sea surface sedi-ments. Chemosphere 58, 1579e1587.

Knudsen, F.R., Arukwe, A., Pottinger, T., 1998. The in vivo effects of octylphenol,butylbenzylphthalate and estradiol on liver estradiol receptor modulation andinduction of zona radiata proteins in rainbow trout: no evidence of synergy.

Environ. Pollut. 103, 75e80.Langer, S., Beko, G., Weschler, C.J., Brive, L.M., Toftum, J., Callesen, M., Clausen, G.,

2014. Phthalate metabolites in urine samples from Danish children and corre-lations with phthalates in dust samples from their homes and daycare centers.Int. J. Hyg. Environ. Health 217, 78e87.

Li, A., Tang, C., Hang, H., Cheng, X., Gao, Y., Cheng, H., Huang, Q., Luo, Y., Xue, Y.,Zuo, Q., Ba, Y., Cui, L., 2013. Influence of phthalates from Shaying river onchildren's intelligence and secretion of thyroid hormone. Wei sheng yan jiu J.Hyg. Res. 42, 236e240.

Lin, Z.P., Ikonomou, M.G., Jing, H., Mackintosh, C., Gobas, F.A., 2003. Determinationof phthalate ester congeners and mixtures by LC/ESI-MS in sediments and biotaof an urbanized marine inlet. Environ. Sci. Technol. 37, 2100e2108.

Liu, H., Cui, K., Zeng, F., Chen, L., Cheng, Y., Li, H., Li, S., Zhou, X., Zhu, F., Ouyang, G.,Luan, T., Zeng, Z., 2014. Occurrence and distribution of phthalate esters inriverine sediments from the Pearl River Delta region, South China. Mar. Pollut.Bull. 83, 358e365.

Mackintosh, C.E., Maldonado, J., Hongwu, J., Hoover, N., Chong, A., Ikonomou, M.G.,Gobas, F.A., 2004. Distribution of phthalate esters in a marine aquatic food web:comparison to polychlorinated biphenyls. Environ. Sci. Technol. 38, 2011e2020.

Mackintosh, C.E., Maldonado, J.A., Ikonomou, M.G., Gobas, F.A., 2006. Sorption ofphthalate esters and PCBs in a marine ecosystem. Environ. Sci. Technol. 40,3481e3488.

Marttinen, S.K., Hanninen, K., Rintala, J.A., 2004. Removal of DEHP in compostingand aeration of sewage sludge. Chemosphere 54, 265e272.

Maund, S.J., Hamer, M.J., Lane, M.C., Farrelly, E., Rapley, J.H., Goggin, U.M.,Gentle, W.E., 2002. Partitioning, bioavailability, and toxicity of the pyrethroidinsecticide cypermethrin in sediments. Environ. Toxicol. Chem. 21, 9e15.

Mohapatra, D.P., Brar, S.K., Tyagi, R.D., Surampalli, R.Y., 2011. Concomitant degra-dation of bisphenol A during ultrasonication and Fenton oxidation and pro-duction of biofertilizer from wastewater sludge. Ultrason. Sonochem. 18,1018e1027.

Ogunfowokan, A.O., Torto, N., Adenuga, A.A., Okoh, E.K., 2006. Survey of levels ofphthalate ester plasticizers in a sewage lagoon effluent and a receiving stream.Environ. Monit. Assess. 118, 457e480.

Peterson, P.J., Freeman, P.T., 1982. Use of a transparent polyurethane dressing forperipheral intravenous catheter care. Nita 5, 387e390.

Roslev, P., Vorkamp, K., Aarup, J., Frederiksen, K., Nielsen, P.H., 2007. Degradation ofphthalate esters in an activated sludge wastewater treatment plant. Water Res.41, 969e976.

Simoneau, C., Hannaert, P., Sarigiannis, D.e, 2009. Effect of the Nature and Con-centration of Phthalates on Their Migration from PVC Materials under DynamicSimulated Conditions of Mouthing, p. 20. EUR 23813 EN.

Staples, C.A., Peterson, D.R., Urbanerton, T.F., Adams, W.J., 1997. The environmentalfate of phthalate esters: a literature review. Chemosphere 35.

Su, P.H., Chang, Y.Z., Chang, H.P., Wang, S.L., Haung, H.I., Huang, P.C., Chen, J.Y., 2012.Exposure to di(2-ethylhexyl) phthalate in premature neonates in a neonatalintensive care unit in Taiwan. Pediatr. Crit. Care Med. 13, 671e677.

Toft, G., Jonsson, B.A., Lindh, C.H., Jensen, T.K., Hjollund, N.H., Vested, A., Bonde, J.P.,2012. Association between pregnancy loss and urinary phthalate levels aroundthe time of conception. Environ. Health Perspect. 120, 458e463.

USEPA, 2012. Selected Analytical Methods for Environmental Remediation andRecovery United States Environmental Protection Agency. EPA/600/R-612/555.

Visvanathan, C., Glawe, U., 2006. Domestic Solid Waste Management in South AsianCountries e a Comparative Analysis, 3R South Asia Expert Workshop.

Wan, Y., Hu, J., Yang, M., An, L., An, W., Jin, X., Hattori, T., Itoh, M., 2005. Charac-terization of trophic transfer for polychlorinated dibenzo-p-dioxins, di-benzofurans, non- and mono-ortho polychlorinated biphenyls in the marinefood web of Bohai Bay, North China. Environ. Sci. Technol. 39, 2417e2425.

Webb, J.E., 1958. Ecology of Lagos lagoon. The life History of BranchiostomaNigeriense. Philos. Trans. Reg. Soc. Bull. 241, 355e391.

Whyatt, R.M., Liu, X., Rauh, V.A., Calafat, A.M., Just, A.C., Hoepner, L., Diaz, D., Quinn, J.,Adibi, J., Perera, F.P., Factor-Litvak, P., 2012. Maternal prenatal urinary phthalatemetabolite concentrations and child mental, psychomotor, and behavioraldevelopment at 3 years of age. Environ. Health Perspect. 120, 290e295.

Wormuth, M., Scheringer, M., Vollenweider, M., Hungerbuhler, K., 2006. What arethe sources of exposure to eight frequently used phthalic acid esters in Euro-peans? Risk Anal. 26, 803e824.

Wu, S., Wang, G., Gao, D., Xi, B., Yao, W., Liu, M., 2007. Occurrence of Camallanuscotti in greatly diverse fish species from Danjiangkou Reservoir in central China.Parasitol. Res. 101, 467e471.

Yan, X., Calafat, A., Lashley, S., Smulian, J., Ananth, C., Barr, D., Silva, M., Ledoux, T.,Hore, P., Robson, M.G., 2009. Phthalates biomarker identification and exposureestimates in a population of pregnant women. Hum. Ecol. Risk Assess. 15,565e578.

Yuan, S.Y., Liu, C., Liao, C.S., Chang, B.V., 2002. Occurrence and microbial degradationof phthalate esters in Taiwan river sediments. Chemosphere 49, 1295e1299.

Zeng, F., Cui, K., Xie, Z., Liu, M., Li, Y., Lin, Y., Zeng, Z., Li, F., 2008a. Occurrence ofphthalate esters in water and sediment of urban lakes in a subtropical city,Guangzhou, South China. Environ. Intern. 34, 372e380.

Zeng, F., Cui, K., Xie, Z., Wu, L., Liu, M., Sun, G., Lin, Y., Luo, D., Zeng, Z., 2008b.Phthalate esters (PAEs): emerging organic contaminants in agricultural soils inperi-urban areas around Guangzhou, China. Environ. Pollut. 156, 425e434.

Zhu, Z.P., Wang, Y.B., Song, L., Chen, J.F., Chang, H.C., Wang, X.R., 2005. Effects ofmono(2-ethylhexyl) phthalate on testosterone biosynthesis in leydig cellscultured from the rat testis. Zhonghua nan ke xue Nat. J. Androl. 11, 247e251.