Polycyclic aromatic hydrocarbons (PAHs) in

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Aug 14, 2014 - 2009; USEPA 2014). Generally, PAHs originate from natural sources (volcanic activity, forest fires, natural oil seeps and indirect synthesis.

Polycyclic aromatic hydrocarbons (PAHs) in Crassostrea rhizophorae and Cathorops spixii from the Caroni Swamp, Trinidad, West Indies La Daana K. Kanhai, Judith F. Gobin, Denise M. Beckles, Bruce Lauckner & Azad Mohammed Environmental Science and Pollution Research ISSN 0944-1344 Environ Sci Pollut Res DOI 10.1007/s11356-014-3450-2

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Author's personal copy Environ Sci Pollut Res DOI 10.1007/s11356-014-3450-2

RESEARCH ARTICLE

Polycyclic aromatic hydrocarbons (PAHs) in Crassostrea rhizophorae and Cathorops spixii from the Caroni Swamp, Trinidad, West Indies La Daana K. Kanhai & Judith F. Gobin & Denise M. Beckles & Bruce Lauckner & Azad Mohammed

Received: 21 March 2014 / Accepted: 14 August 2014 # Springer-Verlag Berlin Heidelberg 2014

Abstract Dietary exposure to polycyclic aromatic hydrocarbons (PAHs) may pose serious threats to human health. However, within the Caribbean, quantitative assessments regarding the risks associated with dietary PAH exposure remain sparse. This study investigated PAH presence in edible biota from the Caroni Swamp and quantitatively assessed the potential health threat to human consumers. Mangrove oysters (Crassostrea rhizophorae) and Madamango sea catfish (Cathorops spixii) collected from seven sites in the Caroni Swamp were analysed for 16 priority PAHs. Total PAH levels ranged from 109±18.4 to 362±63.0 ng/g dry wt. in Crassostrea rhizophorae and 7.5 ±0.9 to 43.5±25.5 ng/g dry wt. in Cathorops spixii (average± standard deviation). Benzo[a]pyrene levels in Crassostrea rhizophorae at all sites exceeded international guidelines from British Colombia (Canada) and the European Union (EU). Incremental lifetime cancer risk (ILCR) values based on the ingestion of Crassostrea rhizophorae ranged from 8.4×10−6 to 1.6×10−5 and slightly exceeded the commonly used 1× 10−6 acceptable level of risk. Information from this study is important in understanding the potential health risks posed by PAHs, it is critical towards the protection of public health, and it serves as a useful baseline for comparison with future work.

Responsible editor: Philippe Garrigues L. D. K. Kanhai (*) : J. F. Gobin : A. Mohammed Department of Life Sciences, The University of the West Indies, St. Augustine, Trinidad and Tobago e-mail: [email protected] D. M. Beckles Department of Chemistry, The University of the West Indies, St. Augustine, Trinidad and Tobago B. Lauckner Caribbean Agricultural Research and Development Institute, CARDI Building, The University of the West Indies, St. Augustine, Trinidad and Tobago

Keywords Polycyclic aromatic hydrocarbons . Oysters . Crassostrea rhizophorae . Catfish . Cathorops spixii . Caroni Swamp . Trinidad

Introduction Populations in small island developing states (SIDs) are often dependent on fish and shellfish harvested from local ecosystems as a source of food. In 2010, individual Caribbean islands captured between 24 (Montserrat) and 16,000 (Haiti) metric tonnes of marine fish from local waters (Masters 2012). For the period 2006–2010, Trinidad and Tobago was among the top three Caribbean countries with the highest marine fish capture from local waters (Masters 2012). Specifically, fish consumption for Latin America and the Caribbean for 2009 was estimated to be 5.7 million tonnes (FAO 2012). While fish and fishery products are a significant source of nutrients for humans, anthropogenic contaminants in edible biota may pose serious threats to human health (Han et al. 1998; Guo et al. 2007). Polycyclic aromatic hydrocarbons (PAHs), organic compounds which are composed of two or more fused aromatic rings, are a class of toxic, priority environmental contaminants whose lipophilicity and low aqueous solubilities favour their bioaccumulation in aquatic organisms often consumed by humans (Neff 1979; Government of Canada et al. 1994; EU 2008; Kumar et al. 2008; Gaspare et al. 2009; USEPA 2014). Generally, PAHs originate from natural sources (volcanic activity, forest fires, natural oil seeps and indirect synthesis by microbes and plants) and anthropogenic activities (Neff 1979; Daisy et al. 2002; Wilcke et al. 2000; Wilcke et al. 2003). However, anthropogenic activities involving the incomplete combustion of organic matter at high temperatures and the release of petroleum/petroleum products are considered to be the most important contributors of PAHs in the

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environment (Baumard et al. 1998; Neff et al. 2005). For nonoccupationally exposed persons who are also non-smokers, dietary intake has been highlighted as the main route (>70 %) of human exposure to PAHs (Phillips 1999). This is of particular concern since certain PAHs have been categorised as (i) ‘carcinogenic to humans’, (ii) ‘probably carcinogenic to humans’ and (iii) ‘possibly carcinogenic to humans’ (IARC 2014). Specifically, human exposure to PAHs has been shown to contribute to a substantial risk of lung, skin, bladder and oesophageal cancer (Boffetta et al. 1997; Kamangar et al. 2005). Studies have also specifically indicated that human exposure to PAHs in food results in a higher than acceptable risk of cancer (greater than a one in a million chance of cancer which is equivalent to a risk level >1×10−6). In Korea, Yoon et al. (2007) investigated 27 food commodities and reported a dietary excess cancer risk of 2.3×10−5 while Moon et al. (2010) investigated 26 types of seafood and reported a cancer risk that slightly exceeded the commonly used 1×10−6 guideline value. In China, Xia et al. (2010) investigated seven categories of food and reported median incremental lifetime cancer risk (ILCR) values in the range of 10−6 to 10−5 (indicating high potential cancer risk) while in Spain, Falco et al. (2003) investigated 11 food groups and reported a 5/106 increase in the risk for developing cancer. The Caroni Swamp, a designated Ramsar site, is the largest mangrove-dominated wetland in Trinidad and Tobago (Juman and Ramsewak 2013). This estuarine system is located within the Caroni River Basin, an area which supports extensive domestic, agricultural and industrial activities (Juman et al. 2002). The potential for PAH contamination in the Caroni Swamp exists as the swamp (i) receives freshwater input from rivers (Caroni, Guayamare and Cunupia) which drain the Caroni River Basin (Juman et al. 2002), (ii) receives surface runoff from the adjacent Uriah Butler Highway (a major north–south highway in Trinidad), (iii) is subjected along its western border to tidal influence from the Gulf of Paria (a semi-enclosed body of water which supports high maritime traffic and oil exploration and exploitation activities) and (iv) is subjected to in situ boating activity from ecotourism and fish/shellfish harvesting activities. Previous studies have reported the presence of other contaminants such as chlorinated hydrocarbon compounds (Deonarine 1980; Sampath 1982) and metals (Klekowski et al. 1999; Kanhai et al. 2014) in the Caroni Swamp. Although the majority of the swamp is currently a prohibited area under the Forests Act, chapter 66:01 (Trinidad and Tobago 1915), the Blue River and Felicity areas are still among the most popular sites in Trinidad for the commercial harvesting of mangrove oysters (Laloo et al. 2000; Bullock and Moonesar 2003). Oyster cocktails, composed primarily of raw oyster tissues and a combination of spices, are a local delicacy which is sold by roadside vendors to the public. Other biota such as fish (catfish and tilapia) and crabs, for example the blue crab (Cardisoma guanhumi) and

the mangrove crab (Ucides cordatus), are also periodically harvested from the swamp and sold to the public. Previous work (Laloo et al. 2000; Kanhai et al. 2014) collectively indicated that the bacteriological load and metal levels in mangrove oysters from the Caroni Swamp were capable of posing a threat to the health of local oyster consumers. However, to date, no local studies have assessed the carcinogenic risks posed to oyster consumers as a result of the consumption of PAH-contaminated oysters. Historically, little attention has been directed to PAHs in Trinidad and Tobago with Banjoo (2006) being the only local study to report on PAH levels in the sediments (32–5,446 ng/g dry wt.) and biota (33–1,409 ng/g dry wt.) of the Gulf of Paria. Benzo[a]pyrene (BaP) levels in oysters at certain sites in the Gulf of Paria (Brickfield and Chaguaramas) were above British Colombia’s maximum allowable concentrations for BaP (1–4 μg/kg wet wt.) in shellfish (Ministry of Environment Lands and Parks and British Columbia 1993), indicating that shellfish at these sites were possibly unfit for human consumption (Banjoo 2006). Based on elevated sediment PAH levels at certain sampling sites (one of which was in the Caroni Swamp), Banjoo (2006) recommended that future monitoring should assess the geographic extent of contamination in these areas and that in addition to shellfish attention should be directed to other commonly eaten finfish. Amongst the other Caribbean islands, Guadeloupe was the only country in which PAH levels in biota (66–961 ng/g dry wt. in Crassostrea rhizophorae) were investigated (Ramdine et al. 2012). To date, although these two studies assessed PAH levels in shellfish, no local or regional studies have investigated PAH levels in finfish or produced comprehensive quantitative assessments regarding the risks posed by PAHs in seafood to human health. Furthermore, since the Caroni Swamp is a designated Ramsar site, the identification and management of anthropogenic threats (e.g., chemical contaminants) are vital to maintaining ecosystem well-being. Following this, the objectives of this study were to determine the levels of PAHs in mangrove oysters (Crassostrea rhizophorae) and Madamango sea catfish (Cathorops spixii) from the Caroni Swamp and to assess whether PAH levels posed a risk for human consumption.

Materials and method Site description The Caroni Swamp is located on the west coast of the island of Trinidad, just southeast of the capital of Port of Spain. The swamp is bordered on the east by the Uriah Butler Highway, on the west by the Gulf of Paria, on the north by the Churchill Roosevelt Highway and on the south by the

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Chandernagore River (Nathai-Gyan and Juman 2005). This estuarine mangrove ecosystem is located within the Caroni River Basin (Juman et al. 2002). Three of the rivers which drain this catchment area enter the Caroni Swamp in its eastern region; the Caroni River enters in the north-eastern region while the Cunupia and Guayamare rivers enter in the south-eastern region (Fig. 1). The Caroni Swamp is an important habitat for a variety of commercial species of fish and shellfish (Nathai-Gyan and Juman 2005). The mangrove oyster (Crassostrea rhizophorae) and Madamango sea catfish (Cathorops spixii) are two species which are harvested from the swamp for human consumption.

Fig. 1 Map showing location of sampling sites in the Caroni Swamp, Trinidad ( IMA Institute of Marine Affairs 2009) BR Blue River, LL large lagoon, GOP Gulf of Paria, CD catfish drain, EC entrance canal, UMER Upper Madame Espagnol River, MMER Mouth of Madame Espagnol River

Sample collection Oyster (Crassostrea rhizophorae) and catfish (Cathorops spixii) samples were collected during the wet season (July/August) of 2011 at seven sites in the Caroni Swamp (Fig. 1). Two samples, comprising 50 Crassostrea rhizophorae each, were collected at each of the seven sites. Oysters were of a uniform size, generally ranging between 1.6–2.6 cm (shell length) and 2.3–4.3 cm (shell height). Two whole catfish (Cathorops spixii), between 9.5 and 11 in in length, were also collected at each of the sites (except the Gulf of Paria (GOP) site). Upon collection, all oyster samples were

BR

LL

EC

GOP CD

Gulf of Paria

UMER

MMER

Sampling site River Ramsar site boundary

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placed into labelled Ziploc bags while catfish were wrapped in aluminium foil prior to being placed in labelled bags. Samples were placed in a cooler with ice, transported to the laboratory and stored at −20 °C. Chemical analyses Thirty-five oysters (non-damaged and closed) from each sample were shucked and whole tissues removed, and the composite sample was homogenised. Whole catfish samples were also homogenised. Approximately 30 g of wet weight tissue was sub-sampled from each composite oyster sample and from each catfish for PAH analyses. All PAH analyses were performed by Pace Analytical Services, Inc (Green Bay, WI, USA). All tissue samples underwent Soxhlet extraction with the solvent methylene chloride for a period of 16 h according to USEPA (1996) and a subsequent gel permeation cleanup according to USEPA (1994). Samples were then subsequently analysed for the USEPA’s 16 priority PAHs following USEPA (2007). Two surrogate standards (2-fluorobiphenyl and terphenyl-d14) were used during these analyses. Percentage recoveries (mean±standard deviation) of these standards for oyster analyses were as follows: 2-fluorobiphenyl (76.7±5.4) and terphenyl-d14 (79.2 ± 4.5) and for catfish analyses were as follows: 2fluorobiphenyl (68.7±15.1) and terphenyl-d14 (77.8±8.5). Method blanks were simultaneously analysed with each batch of samples and used to derive method detection limits for the individual PAHs. An HP6890 Gas Chromatograph equipped with a 5,973 mass spectrometer operating in selected ion monitoring (SIM) mode was utilised. The capillary column used was a Restek XTI-5 (30-m length, 0.25-mm internal diameter, 0.25-μm film thickness). Validation of the method for PAHs in tissue samples was done by the analysis of laboratory control samples. Percentage recoveries for ten of the 16 PAHs in oyster samples ranged between 77 and 93 % while percentage recoveries (mean±standard deviation) for the remaining six PAHs were as follows: acenaphthylene, 64.5±0.7; anthracene, 73.5± 2.1; benzo[g,h,i]perylene, 29.0±1.4; dibenzo[a,h]anthracene, 40±1.4; indeno[1,2,3-c,d]pyrene, 37.0±2.8; and naphthalene, 55.0±8.5. In catfish samples, percentage recoveries for 12 of the 16 PAHs ranged between 75 and 96 % while percentage recoveries (mean±standard deviation) for the remaining four PAHs were as follows: benzo[g,h,i]perylene, 47.5 ± 2.1; dibenzo[a,h]anthracene, 58.5±0.7; indeno[1,2,3-c,d]pyrene, 52.5±0.7; and naphthalene, 70.0±15.6. Method detection limits for the 16 priority PAHs in oysters were between 0.14 and 0.81 μg/kg wet wt., and for PAHs in catfish, they were between 0.09 and 0.67 μg/kg wet wt. Lipid content was gravimetrically determined in all tissue samples following the guidelines in the Standard Operating Procedure from Pace Analytical Services, Inc (Pace Analytical Services 2011). In summary, after tissue samples underwent Soxhlet extraction, an aliquot of each sample extract was removed and placed into a weighed

aluminium pan. This pan was then placed on a drying rack in a fume hood for at least 12 h to allow evaporation of the extraction solvent. The pans were then reweighed, and the percent lipid for each extract was determined based on differences in weight. Moisture content was also determined in oyster and catfish samples following the procedure outlined by McDonald et al. (2006). Based on average dry weights for oyster and catfish tissues, relevant conversion factors (5.60 for oysters and 4.52 for catfish) were used to convert PAH concentrations reported on a wet weight basis to a dry weight basis. Data analyses Due to the non-normal distribution of the data, a log transformation was applied. Since significant correlations (Pearson’s correlation, p100–1,100 ng/g) to very high (>5,000 ng/g). To date, no information exists on PAH levels in Cathorops spixii from other countries. Comparisons made with other species of catfish revealed that total PAH levels in Cathorops spixii from the Caroni Swamp (7.5–43.5 ng/g dwt.) were lower than levels reported in catfish from the Arabian Gulf and the Bay of Chetumal, Mexico (Table 6). Both areas experienced sitespecific pollution events as the Arabian Gulf was subjected to the intentional discharge of approximately 9 million barrels of oil during the 1991 Gulf War (Al-Hassan et al. 2001) and the Bay of Chetumal in Mexico experienced a catfish mass mortality event in 1996 (Noreña-Barroso et al. 2004. In both studies, PAH levels were monitored in the liver (site of PAH storage prior to undergoing metabolisation), and therefore, this could have contributed to the detection of high PAH levels. In comparison to PAH levels in catfish from Korea and China, the PAH levels reported by this study were slightly higher (Wan et al. 2007; Moon et al. 2010). Previous studies have reported that the microbial load in locally harvested oysters pose a threat to the health of oyster consumers (Rampersad et al. 1999; Laloo et al. 2000). More recent work has also indicated that oysters harvested from the Caroni Swamp showed high levels of zinc contamination which are capable of threatening human health depending on oyster ingestion rate (Kanhai et al. 2014). This study confirmed PAH presence in both shellfish (specifically oysters) and finfish (specifically catfish) in the Caroni Swamp and further indicated that PAH levels in oysters posed only a

Author's personal copy Environ Sci Pollut Res Table 6 PAH levels reported by other studies for Crassostrea oysters and catfish Study

Species

Location

Total (16 EPA PP) PAHs (ng/g dw)a

Gold-Bouchot et al. (1995) Sericano et al. (1996) Gold-Bouchot et al. (1997) Banjoo (2006)

Crassostrea virginica Crassostrea virginicab Crassostrea virginica Crassostrea rhizophorae Crassostrea corteziensis Crassostrea virginica

Terminos Lagoon, Mexico Galveston Bay, Texas, USA Mexico Gulf of Paria, Trinidad

20–1,240 (unspecified PAHs) 290–4,360 (24 PAHs) 127–615 (unspecified PAHs) 15.1–362

Pacific Coast of Mexico Terminos Lagoon, Mexico

120–3,520 388–2,246

Crassostrea gigasb Crassostrea sp.

San Francisco estuary, USA Urdaibai, Bay of Biscay, Spain Pearl River Estuary, China Savannah, GA, USA Korea Guadeloupe

25–6,899 (16 EPA PP PAHs + 6 PAHs) 289–1,406

Paez-Osuna et al. (2002) Noreña-Barroso et al. (1999) Oros and Ross (2005) Cortazar et al. (2008) Wei et al. (2006) Kumar et al. (2008) Moon et al. (2010) Ramdine et al. (2012) This study Al-Hassan et al. (2001) Wan et al. (2007) Noreña-Barroso et al. (2004) Moon et al. (2010) This study

Crassostrea rivularis Crassostrea virginica Crassostrea gigas Crassostrea rhizophorae Crassostrea rhizophorae Arius bilineatus Chaeturichthys sitgmatias Ariopsis assimilis Parasilurus asotus Cathorops spixii

Caroni Swamp, Trinidad

365–1,041 (15 EPA PP PAHs) 4–260 63.2 57.4–915 (16 EPA PP PAHs + triphenylene + dibenzo[ac]anthracene) 109–362

Arabian Gulf Bohai Bay, North China

40.6–333 wet wt. in liver, gills and muscle (13 EPA PP PAHs) 21±9.6 in muscle (16 EPA PP PAHs + 2 additional PAHs)

Bay of Chetumal, Mexico

6.6–762 μg/g in liver (11 EPA PP PAHs + 7 additional PAHs)

Korea Caroni Swamp, Trinidad

34.8 7.5–43.5 in fish tissues

Highlighted are the present study values a

Total PAHs refers to the sum of the EPA 16 (priority pollutant (PP) PAHs unless otherwise stated

b

Study utilised transplanted oysters

marginal added cancer risk to oyster consumers. Collectively, these findings indicate that local oyster consumers may be ingesting a literal ‘cocktail’ of chemical (metals, PAHs) and microbiological contaminants which may affect their health. This present study brings to the fore the public health issue of carcinogenic risk from ingested food, and it should act as a key stimulus for more far-reaching work on investigating the local carcinogenic risk from multiple food sources.

Conclusion This study provided the first comprehensive assessment of polycyclic aromatic hydrocarbons (PAHs) in the mangrove oysters (Crassostrea rhizophorae) and Madamango sea catfish (Cathorops spixii) in the Caroni Swamp. It also provided the first quantitative assessment of the carcinogenic risk posed to local oyster consumers as a result of the ingestion of PAHs in oysters. PAH levels in Crassostrea rhizophorae in this study were significantly higher than they were in Cathorops spixii. Although benzo[a]pyrene (BaP) was undetected in Cathorops spixii, BaP levels in Crassostrea rhizophorae at

all sites in the Caroni Swamp were above available international guidelines for BaP in shellfish. ILCR values ranged between 8.4×10−6 and 1.6×10−5, indicating that oyster consumption potentially poses only a ‘marginal added’ carcinogenic risk to humans who consume oysters from the Caroni Swamp. The findings of this study highlight the public health issue of carcinogenic risk from food (specifically ingested shellfish). Such information is important for consumers of shellfish and will serve as a crucial baseline for future work. Acknowledgments This work was funded by Campus Research Grants (CRP.5.NOV09.4 and CRP.5.MAR11.9) from the University of the West Indies (UWI), St. Augustine. The authors acknowledge the support of the Institute of Marine Affairs (IMA) by granting permission to utilise the map of the Caroni Swamp (Fig. 1).

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