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Need to update human health risk assessment protocols for polycyclic aromatic hydrocarbons in seafood after oil spills
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Need to update human health risk assessment protocols for polycyclic aromatic hydrocarbons in seafood after oil spills John W. Farrington Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA
A R T I C LE I N FO
A B S T R A C T
Keywords: Polycyclic aromatic hydrocarbons (PAHs) Alkylated PAHs Seafood contamination Human health risks Deepwater Horizon oil spill
The need to include alkylated polycyclic aromatic hydrocarbons in human health risks assessments for oil contaminated seafood after crude oil spills is set forth. This is placed within the context of a brief review of the literature for PAHs and human health risk assessments after oil spills. The example of human health risk assessments for oil contaminated seafood after the Deepwater Horizon oil spill is reviewed with the conclusion that PAHs such as alkylated chrysenes/triphenylenes/benzanthracenes should have been included in the human health risk assessment and not dismissed as present in very low concentrations relative to their parent PAHs.
1. Introduction The occurrence of oil spills in areas where seafood is harvested creates concerns about health risks for consumers of this harvested seafood as noted by Yender et al. (2002) and Yitalo et al. (2012), among others. The major petroleum chemicals involved in this concern are the polycyclic aromatic hydrocarbons (PAHs). The PAHs are only one class of a complex mixture of chemicals with individual components of environmental concern. Government agencies charged with responsibilities for assessing and communicating risks associated with consumption of seafood contaminated with human synthesized or human mobilized natural chemicals of known or potential public health concern have a very difficult task. There are a multitude of both legacy contaminants such as chlorinated pesticides, polychlorinated biphenyls, and polycyclic aromatic hydrocarbons (PAHs), as well as numerous emerging contaminants of environmental concern from many human controlled or influenced processes (e.g. Gaston et al., 2019; Bricker et al., 2014; Dodder et al., 2014 and references therein). The process of identification and quantifying individual chemicals within groups of these chemicals is challenging (e.g. Hites and Jobst, 2018). Assessing risks from all individual components of these complex mixtures and interactive synergistic or antagonistic effects among them is a herculean task. In addition, Rheinberg and Hammit (2012) note the need to balance risks from eating contaminated seafood against the loss of healthful benefits of polyunsaturated fatty acids (PUFAs) which are abundant in fish. Herein, the focus is on PAHs. The challenge of seafood contaminated by PAHs and the associated human health risk has been
known and researched for at least the past 60 years (e.g. Cahnmann and Kuratsune, 1956, 1957; Andelmann and Suess, 1970; NRC, 1972, 1975, 1985, 2003; Yender et al., 2002; Baird et al., 2007). The issue of risk of carcinogenic potency of certain PAHs has dominated considerations even though for seafood safety in oil spill areas there are other toxicities associated with other PAHs. I submit that there is a need to update an aspect of methodology used in assessment of human health risk by consumption of seafood contaminated or potentially contaminated by PAHs (polycyclic aromatic hydrocarbons) in the Macondo 252 Crude oil spilled from the Deepwater Horizon ‘s (DWH) Macondo well (Yitalo et al., 2012; Xia et al., 2012). Specifically, this involves alkylated PAHs. A brief review of human health concerns associated with PAH contaminated seafood provides context. Hopefully, this paper and other recent papers providing detailed discussions of human health concerns for seafood contaminate during oil spills will lead to improved assessments for human health risk from PAHs in general, whatever the source of the PAHs (e.g. Gohlke et al., 2011; Rotkin-Ellman et al., 2012; Rotkin-Ellman and Solomon, 2012; Dickey, 2012; Wickliff et al., 2014; Dickey and Hoettel, 2016; Wilson et al., 2015). 2. Overview of PAHs Polycyclic aromatic hydrocarbons are of environmental concern because several of them have been demonstrated to have proto-carcinogenic/carcinogenic properties as reviewed over the past decades (e.g. Andelmann and Suess, 1970; Neff, 1979; NRC, 1972, 1983; and a series of International Symposia on Polynuclear Aromatic Hydrocarbons beginning in 1980 –ISPAC, 2019; among others). Dipple (1985) provides a
E-mail address: [email protected]. https://doi.org/10.1016/j.marpolbul.2019.110744 Received 29 July 2019; Received in revised form 14 November 2019; Accepted 15 November 2019 0025-326X/ © 2019 Elsevier Ltd. All rights reserved.
Please cite this article as: John W. Farrington, Marine Pollution Bulletin, https://doi.org/10.1016/j.marpolbul.2019.110744
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to the more robust MFPPOH method can introduce overestimations of concentrations in a coal tar or crude oil sample of 2 to 614% depending on the alkylated PAH. Other advances in analytical chemistry of the past two decades have addressed the challenges of separating and quantifying alkylated PAHs. Two dimensional gas chromatography (GCxGC) combined with mass spectrometry-computer data systems avoids most if not all of the problems noted in the preceding with paragraph with the capability to separate, identify and quantify parent PAHs and alkylated PAHs in a wide molecular weight range (e.g. Frysinger et al., 2003; Nelson et al., 2019). John et al. (2014) used GC-triple quadrupole mass spectrometry for characterizing alkylated chrysenes. Thus the methods for quantitative analyses are available for a full range of alkylated PAHs. However, there have been relatively few analyses of this type for the alkylated higher molecular weight PAHs, e.g. 4 to 6 rings, perhaps due to the lack of standards of the specific alkylated PAHs (e.g. John et al., 2014).
review extending back to at least the year 1775. Although not the specific subject of this paper, it is important to acknowledge that several PAHs have been shown to have adverse effects on several types of aquatic organisms under certain exposure conditions (e.g. Neff, 1979; NRC, 1975, 1985, 2003; The Royal Society, 1980). Several sources contribute PAHs to the environment. These can be divided into natural sources and human made or mobilized sources. Each of those sources can each be subdivided into PAHs from natural petroleum seeps (petrogenic) and forest and grass fires (pyrogenic), oil spills and chronic oil inputs (petrogenic) and burning of fossil fuels (pyrogenic), creosote containing pyrolysis products, or cooking of food that chars natural organics chemicals or smoking food (pyrogenic) (Blumer and Youngblood, 1975; Blumer, 1976; Lima et al., 2005; Stout et al., 2015 among others). Early diagenesis (combinations of microbial and chemical reaction mediated) transformation of small amounts of biogenic molecules can lead to specific PAHs such as perylene and retene. Erosion of ancient sediments with organic matter in various stages of diagenesis can contribute PAHs to modern ecosystems. Loss of coal from bunkers in coal powered ships has contributed coal sourced PAHs to surface sediments in some depositional areas (e.g. Tripp et al., 1981). Several recent papers have reviewed differences in the composition of PAHs from several types of pyrogenic sources and petrogenic sources and various approaches to estimating the contributions from various sources of PAHs to a given sample (e.g. Lima et al., 2005; Stout et al., 2015). Fig. 1a–d provides examples of chemical structures of PAHs. Fig. 1a provides the relationship between chemical structure containing carbon and hydrogen atoms and the shorthand notation usually used. Fig. 1b depicts parent PAH with the exception of retene which is an alkylated PAH. Both retene and perylene (Fig. 1b) have a source in early diagenesis of organic matter in sediment. Fig. 1c contains structures of several different methylchrysenes and Fig. 1d contains structures of a few of the many possible additional alkylated chrysenes. The scope of challenges for analytical chemistry and for assessment of effects of PAHs on organisms and human health is illustrated by the fact that the structures of PAHs depicted in Fig. 1 are no more than an estimated 10% (conservatively) of PAHs in various sources of input to the environment. Analytical chemistry limitations existed in the 1960s through the 1980s for identification and quantification of mainly the alkylated PAH primarily due to lack of standards and standard reference materials and the inability of gas chromatography–mass spectrometry (GC–MS) of that time period to distinguish between isomers of alkylated PAH. These limitations and several other factors led the U. S. EPA to establish the list of Priority Pollutants which contained 16 PAHs, all of which could be identified and quantified. The interesting history of the establishment of the U.S. EPA list of 16 Priority Pollutant PAHs in 1976 is set forth by Keith (2015) in an issue of Polycyclic Aromatic Compounds, Volume 35, 2015 devoted to the U.S. E.PA's Sixteen PAH Priority Pollutants (Anderson and Achten, 2015). As Keith notes, the EPA Priority Pollutant list was adopted by many countries. Over the ensuing years, EPA added eighteen alkylated PAHs of the naphthalene, flourene, phenanthrene, pyrene, and chrysene homologs for the purpose of estimating toxic hazards of contaminated soils and sediments (e.g. Antle et al., 2014). Many analysts during the past three decades have used GC–MS with selected ion monitoring using the molecular ion or prominent fragment ion plus GC retention time to quantify PAHs as noted by Ziegler and Robbat Jr (2012) and Antle et al. (2014). A methodology using “three to five ions per isomer pattern and multiple fragmentation patterns per homolog (MFPHH) has been shown to be more accurate (e.g. Ziegler and Robbat Jr, 2012; Antle et al., 2014). These authors have shown that as the analyte PAHs of interest expanded to the alkylated PAHs (e.g. C4 - naphthalenes, C2 – chrysenes), selected ion monitoring or use of one ion plus retention times from full scan GC–MS (single ion extraction method or SIE) compared
3. Human health risk assessment for seafood contaminated, or potentially contaminated, by the Deepwater Horizon oil spill The Deepwater Horizon (DWH) oil spill claimed 11 lives, the most important aspect of the accident. It was the largest marine oil spill in the U. S. history up to that time. Numerous papers have described the accident, its immediate aftermath, and the short term and long term fates and effects. (McNutt et al., 2012 and publications and references therein listed on the Gulf of Mexico Research Initiative website (www. gulfresearchinitative.org). Yitalo et al. (2012) and Xia et al. (2012) reported on human health risk assessment for seafood contaminated or potentially contaminated with PAHs from the DWH oil spill. The protocols they used were founded in the report of Yender et al. (2002) and “current information from the FDA, NOAA, and the Environmental Protection Agency (EPA) to establish a unified Deepwater Horizon seafood protocol.” (US FDA, 2010). Experience from eight specific spills beginning in 1989 with the T/V Exxon Valdez and through 1999 guided Yender et al. (2002) in their review of key aspects of a more standardized guidance for both closing and opening fisheries when considering human health risk of seafood consumption from areas here oil spills had or might have contaminated seafood. They noted various important considerations based on reviews of the literature. For example, after an oil spill, habitat utilization and behavior of marine organisms have a significant influence on which organisms are exposed to and will take up petroleum hydrocarbons. An important additional factor is that, in general, fish have a relatively high capacity for metabolizing PAHs because of induction of high levels of activity of enzymes that metabolize PAHs. The capacity of induction of the metabolizing enzymes and metabolism of PAHs is reduced in most crustaceans (e.g. lobsters, crabs and shrimp) relative to fish. For mollusks such as oysters, mussels, clams, and scallops the capacity for induction of the metabolizing enzymes and metabolism of PAHs is of “very limited capacity” (Yender et al., 2002). Humans also have the capacity to metabolize PAHs and this is connected to both the elimination and toxicity of these compounds (e.g. Alquassim et al., 2019). Yitalo et al. (2012) reported on a significant and complicated effort for assessing human health risk from eating PAHs contaminated seafood in areas of the DWH spill. A key result was “When detected, the concentrations [of individual PAHs] were at least two orders of magnitude lower than the level of concern for human health risk.”(Yitalo et al., 2012). Their paper led to a healthy scientific debate and discussion in a series of published comments and replies about various aspects of the protocols – a scientific debate that should inform in a major way relevant protocols and methodology for similar human health risk seafood assessments for future oil spills. (Rotkin-Ellman et al., 2012; Rotkin-Ellman and Solomon, 2012; Dickey, 2012; Wickliff et al., 2014). One aspect to the protocol of Yitalo et al. (2012) that needs to be revisited relates to the statements in both documents (Supplemental 2
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Fig. 1. Examples of chemical structures of polycycicaromatic hydrocarbons. 1A. Example structure of 1-methylnaphthalene with carbon and hydrogen atoms shown and a shorthand notation. 1B. Parent PAH structures except retene. Retene and perylene are products of natural organic matter diagenesis (see text). All but retene, perylene, BkF, and Cor are on the US EPA list of 16 priority PAH (by permission from Lima et al., 2005). 1C. Example methyl chrysene structures. 1D. Example alkyl chrysenes.
Information of Yitalo et al. (2012) and US FDA (2010) concerning which PAHs to include in carcinogenic risk assessment. The US FDA (2012) statement notes: “In order to interpret the cancer risk for individual PAH compounds likely to be found in the Gulf of Mexico light crude petroleum, the carcinogenic activity relative to benzo(a)pyrene (BaP) is estimated as a toxicity equivalency factor (TEF)[with reference cited U.S.EPA, 1998 in reference list herein]. TEFs for chrysene, benzo[k]fluoranthene, benz[a]anthracene, indeno[1,2,3cd]pyrene, benzo[b]fluoranthene, and bibenz[a,h]anthracene are 0.001, 0.01, 0.1, 0.1, 0.1, and 1 respectively. Tissue concentrations of PAHs other than BaP are multiplied by their respective TEF and added to the tissue concentration of BaP to determine BaP equivalent (BaPE) concentration. The BaPE concentration is considered the most valid measure of the carcinogenic potency of a complex mixture of PAH compounds. For the purpose of this risk assessment, substituted alkylated homologs of the above PAHs will be excluded from analyses due to the very low concentrations determined in the MC 252 crude oil.” (underline my emphasis). The Yitalo et al. (2012) Supporting Information statement is similar, ending with “Concentrations of alkylated homologs of the carcinogenic PAH listed above [same as the US F &DA list above] were excluded as they are found in very low levels in the Louisiana light crude oil.” However, analytical chemistry data indicate otherwise. The alkylated homologs are reportedly in a similar concentration range and in some cases may be higher in concentration in the Macondo crude oil from the DWH well. Examination of the Certificate of Analyses for Standard Reference Material (SRM) 2779 Gulf of Mexico Crude Oil reports PAH data for the crude oil obtained from the insertion tube that was receiving oil directly from the Macondo Well (of the DWH oil spill) during response operations. NIST (2012) suggests that there are more than “low levels” of several of the excluded alkylated PAHs in the DWH Macondo Well sample. Tables 1 and 2 contain data taken from the Certificate of Analyses for SRM 2779. Although most are not Certified Values, they are Reference Mass Fraction Values because over 90% of the participating laboratories used the parent PAH response factor for the corresponding alkylated group. This constraint relates in part to the issues discussed previously in this paper regarding the methodology for analyses of alkylated PAHs. Chrysene, one of the PAHs in the Yitalo et al. (2012) and US FDA (2012) list is reported as Mass Fraction of 23.3 mg/kg in the Macondo oil. An alkylated homolog, 6-Methylcrysene is reported as 15.10 mg/kg. It is likely that Yitalo et al. (2012) did not have access to the results of the NIST Certification/Reference Values noted above when they were interpreting their results. Their paper was submitted June 2, 2011. The NIST Certificate was issued June 4, 2012 Likewise, the Xia et al. paper was submitted November 21, 2011, before the NIST Certificate of Analysis was issued. My purpose is not to criticize Yitalo et al. or Xia et al. Given the concentrations of PAHs reported by Yitalo et al., there
Table 2 Concentrations of selected individual PAHs and groups of alkylated congener PAHs in NIST SRM 2779.
Mass fraction value (mg/kg)
Pyrenea 1-Methylpyreneb 4-Methylpyreneb Chryseneb 6-Methylchryseneb
14.81 ± 0.39a 12.1 ± 1.8b 21.6 ± 1.5b 23.3 ± 5.2b 15.10 ± 0.56b
a b
Mass fraction (mg/kg)
Benz[a]anthracene Chrysene Triphenylene C1-Benzanthracenes/chrysenes/triphenylenes C2-Benzanthracenes/chrysenes/triphenylenes C3-Benzanthracenes/chrysenes/triphenylenes C4-Benzanthracenes/chrysenes/triphenylenes
7.03 ± 0.85a 23.3 ± 5.2b 17.7 ± 6.7b 110 ± 7c 130 ± 10c 93 ± 12c 71 ± 16c
a
Certified mass fraction value NIST SRM 2779 Table 1 (NIST, 2012). Reference mass fraction value NIST SRM 2779 Table 2 (NIST, 2012). c Reference mass fraction value alkylated PAH groups NIST SRM 2779 Table 3 (NIST, 2012). b
may have been minimum risk to human health even if the alkylated PAHs were included. My purpose here is to raise the point, going forward to future oil spills, that alkylated PAHs for higher molecular weight PAHs can be present in some crude oils, some bunker oils, and some higher numbered fuel oils at concentrations equal to or higher than their parent PAHs. As noted in the brief review above, this has been known for many years. Therefore, these specific alkylated PAHs should not be dismissed automatically for reasons of concentrations being too low to be considered for human health carcinogenic risk. If it is important, and I submit that it is, to include parent higher molecular weight PAH in risk assessments, then it is also important to consider their alkylated PAH homologs of approximately the same or higher concentration in a spilled oil. The Xia et al. (2012) paper reported on analysis of PAHs in several local samples of smoked meats and fish and noted that the PAHs in the processed foods were below the same FDA Level of Concern (LOC) concentrations noted above for contaminated (or potentially contaminated) Gulf of Mexico seafood samples. Xia et al. (2012) also noted that the PAHs concentrations in the processed food were “similar if not higher [in concentrations] for some PAHs to those detected in the seafood samples collected in the Mississippi Gulf Coast.” Baird et al. (2007) reviewed the issue of human risk from exposure to alkylated PAHs in aquatic systems and noted the paucity of toxicity data for the alkylated PAHs with the exception of 1- and 2-methylnaphthtalene. Carcinogenic risk data were generally not available for 2 to 6 ring alkylated PAHs. However, theoretical considerations based on chemical structures of parent PAHs and the tumorigenic or mutagenic active site in the molecules suggest strongly that specific alkylated PAHs will be shown to be either tumorigenic and/or mutagenic. Baird et al. (2007) recommended a thoughtful approach to assessing human health risks for alkylated PAHs. Summarizing their recommendations as a lead sentence in each step of their strategy: 1) “The PAH families (e.g. naphthalene, phenanthrene, pyrene) of alkylated PAHs that are typically found in fish tissues and sediments need to be more thoroughly identified, including the relationship between the source PAH mixture (e.g. crude oil) and the PAHs that are available for human exposure in fish and sediment.” 2) “Identify the individual isomers of relevant PAHs found in the aquatic environment and compare them to the specific activity of those identified in the literature.” 3) “After individual and mixtures of alkylated PAHs from aquatic environments with toxicological activity are identified, the potential for concern associated with the range of concentrations of alkylated
Table 1 Concentrations of selected individual PAHs in NIST SRM 2779. PAH name
PAH name
Certified mass fraction value NIST SRM 2779 Table 1 (NIST, 2012). Reference mass fraction value NIST SRM 2779 Table 2 (NIST, 2012). 4
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idea, drafting and completion of this paper.
PAHs observed in environmental samples needs to be estimated.” 4) “Once MOA [mode of action] known to be relevant to the toxicity and carcinogenicity of alkylated PAHs are identified, individual alkylated PAHs and common environmental mixtures of alkylated PAHs that frequently occur in the aquatic environment could be tested for their potential toxicity using a screening battery of in vitro and in vivo mechanistic studies.” 5) “Individual alkylated PAHs and mixtures of alkylated PAHs of concern identified through this process could be tested in long-term animal bioassays designed to capture the anticipated MOAs.”
Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgements Doctoral dissertation research in the laboratory of Professor James G. Quinn, to whom this Special Issue of Marine Pollution Bulletin is dedicated, provided an early introduction for me to the science-policy interface. That research brought me into the realm of interactions with state and federal agencies responsible for assessing risks to public health from seafood contaminated with organic chemicals of environmental concern. Professor Quinn, and others of my Ph. D. dissertation committee, provided calm, steady guidance while allowing me freedom to explore not only in scientific research, but also at the science-policy interface. I extend to them my profound gratitude for their wise advice. A special appreciation is extended to Jim Quinn for being an adviser and mentor for fifty-one years. I thank Bruce W. Tripp and Paul D. Boehm for comments on drafts of this paper and two anonymous reviewers for their helpful reviews. An appointment as Dean Emeritus, Woods Hole Oceanographic Institution, provided assistance in preparing this paper.
Developing and applying analytical methods that will distinguish between Chrysene and Triphenylene, and each of their alkylated homologs for the purpose of accuracy is one step in the risk assessment process (John et al., 2014; Nelson et al., 2019). This is important because Baird et al. (2007) and Sun et al. (2014) among others, review how subtle molecular structure changes can have a significant influence on toxicity, mutagenicity and toxicity. A recent example of this effect of subtle structure changes and the influence on effects has been published by Alquassim et al. (2019) comparing results of human aryl hydrocarbon receptor (AhR)reporter signaling, cytotoxicity, and gene expression responses to mono-methylchrysenes (see Fig. 1c). The authors noted that for a yeast-based reporter assay detecting human AhR mediated gene expression the 4methylchrysene was six times more potent as chrysene while 5-methylchrysene was one-third as potent as chrysene. Other methylchrysenes were more comparable to chrysene in this assay. In the interim, the State of California, USA has issued an updated protocol for seafood risk assessment in the event of oil spills contaminating seafood (Klasing and Brodberg, 2015). Apparently, this protocol takes a conservative approach compared to those discussed above (Yitalo et al., 2012; Xia et al., 2012; US FDA, 2010) and uses the following for calculation of cPAH [carcinogenic PAH] exposure equivalents in sea food as follows:
References Alquassim, A.H., Wilson, M.J., Wickliffe, J.K., Paneni, D., Overton, E.B., Miller III, C.W., 2019. Aryl hydrocarbon receptor signaling, toxicity, and gene expression responses to mono-methylchrysenes. Environ. Toxicol. 34, 992–1000. Andelmann, J.B., Suess, M.J., 1970. Polynuclear aromatic hydrocarbons in the water environment. Bull. World Health Organ. 43, 479–508. Anderson, J.T., Achten, C., 2015. Introduction to this special issue: a critical look at the 16 EPA PAHS. Polycyclic Aromatic Hydrocarbons 35, 143–146. Antle, P.M., Zeigler, C.D., Wilton, N.M., Robbat Jr., A., 2014. A more accurate analysis of alkylated PAH and PASH and its implication in environmental forensics. Int. J. Environ. Anal. Chem. 94 (4), 332–347. Baird, S.J., Bailey, E.A., Vorhees, D.J., 2007. Evaluating human risk from exposure to alkylated APHs in an aquatic system. Hum. Ecol. Risk. Assess. 13, 322–338. Blumer, M., 1976. Polycyclic aromatic hydrocarbons in nature. Sci. Am. 234, 35–45. Blumer, M., Youngblood, W.W., 1975. Polycyclic aromatic hydrocarbons in soils and recent sediments. Science 188, 53–55. Bricker, S., Lauenstein, G., Maruya, K., 2014. NOAA’s mussel watch program: incorporating contaminants of emerging concern (CECs) into a long-term monitoring program. Mar. Pollut. Bull. 81, 289–290. Cahnmann, H.J., Kuratsune, M., 1956. PAH in oysters collected in polluted waters. Proc. Am. Assoc. Cancer Res. 2, 99. Cahnmann, H.J., Kuratsune, M., 1957. Determination of PAH in oysters collected in polluted waters. Anal. Chem. 29, 1312–1317. Dickey, R.W., 2012. Correspondence. FDA risk assessment of seafood contamination after the BP oil spill. Environ. Health Perspect. 120 (2), A54–A55. Dickey, R., Hoettel, M., 2016. Seafood and beach safety in the aftermath of the Deepwater Horizon oil spill. Oceanography 29 (3), 196–203. https://doi.org/10.5670/oceanog. 2016.83. Dipple, A., 1985. Polycyclic aromatic hydrocarbon carcinogenesis. An introduction. In: Harvey (Ed.), Polycyclic Aromatic r and Carcinogenesis. ACS Symposium Series Volume 283. American Chemical Society, Washington, DC, pp. 1–17. Dodder, N., Maruya, K., Ferguson, P., Grace, R., Klosterhaus, S., La Guardia, M., Lauenstein, G., Ramirez, J., 2014. Occurrence of contaminants of emerging concern in mussels (Mytilus spp.) along the California coast and the influence of land us, storm water discharge, and treated wastewater effluent. Mar. Pollut. Bull. 81, 340–346. Frysinger, G., Gaines, R.B., Xu, L., Reddy, C.M., 2003. Resolving the unresolved complex mixture in petroleum contaminated sediments. Environ. Sci. Technol. 37, 1653–1662. Gaston, L., Lapworth, D.J., Stuart, M., Arnscheidt, J., 2019. Prioritization approaches for substances of emerging concern in groundwater: a critical review. Environ. Sci. Technol. 53, 6106–6122. Gohlke, J.M., Doke, D., Tipre, M., Leader, M., Fitzgerald, T., 2011. A review of seafood safety after the Deepwater Horizon blowout. Environ. Health Perspect. 119 (8), 1062–1069. Hites, R., Jobst, K., 2018. Is nontargeted screening reproducible? Environ. Sci. Technol. 52, 11975–11976. ISPAC, 2019. A short history of ISPAC (International Symposium on Polynuclear Aromatic Compounds). http://www.louisville.edu/org/ispac/history.htm, Accessed date: 20 March 2019.
“In order to determine exposure equivalents for cPAHs in seafood, the wet weight concentration of each cPAH is first converted to an equivalent concentration of BaP. To do this, individual cPAHs plus their alkylated homologs are multiplied by their respective PEF [potency equivalent factor] to derive a BaPE concentration for that chemical.” 4. Concluding thoughts There has been progress with addressing the challenges associated with risks associated with seafood contaminated with PAHs, no matter what the source of PAH. Much more needs to be done, especially with respect to alkylated PAHs. Over ten years have passed since the Baird et al. (2007) review and it is timely for another comprehensive review of human health risks associated with alkylated PAHs alone and in combinations with other alkylated and parent PAHs. Two other points seem obvious and worthy of further consideration. First, as noted in the paper by Xia et al. (2012) cited earlier, PAHs are present in a variety of foods from a variety of sources. It would seem appropriate to not consider human health risk from the various sources in isolation. For example, why not assess the human health risk from the PAHs in the oil spill contaminated seafood and then place it in the accumulative exposure for PAHs via all sources of food to obtain a more meaningful human health risk assessment? Second, it is clear, especially in coastal areas near population and industrial centers that PAHs are but one class of contaminants to consider individually and in combination for assessing human health risks associated with seafood consumption. Author contribution John W. Farrington declares that he is solely responsible for the 5
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120 (2), A 55–A56. Rotkin-Ellman, M., Wong, K.K., Solomon, G.M., 2012. Commentary. Seafood contamination after the BP gulf oil spill and risks to vulnerable populations: a critique of the FDA risk assessment. Environ. Health Perspect. 120 (2), 157–161. Stout, S.A., Emsbo-Mattingly, S.D., Douglas, G.S., Uhler, A.D., McCarthy, K.J., 2015. Beyond 16 priority pollutant PAHs: a review of PACS used in environmental forensic chemistry. Polycyclic Aromatic Hydrocarbons 35, 285–315. Sun, Y., Miller III, C.A., Wiese, T.E., Blake, D.A., 2014. Methylated phenanthrenes are more potent than phenanthrene in a bioassay of human aryl hydrocarbon receptor (AhR) signaling. Environ. Toxicol. Chem. 33 (10), 2363–2367. The Royal Society, 1980. The Effects of Oil Pollution: Some Research Needs. A Memorandum. The Marine Pollution Subcommittee of the British committee n Ocean Research. The Royal Society, London, U.K. Tripp, B.W., Farrington, J.W., Teal, J.M., 1981. Unburned coal as a source of hydrocarbons in surface sediments. Mar. Pollut. Bull. 12, 122–126. US FDA, 2010. Protocol for Interpretation and Use of Sensory Testing and Analytical Chemistry Results for Re-opening Oil-impacted Areas Closed to Seafood Harvesting Due to the Deepwater Horizon Oil Spill. U. S. Food and Drug Administration, Washington, DC Available at. http://www.fda.gov/Food. Wickliff, J., Overton, E., Frickel, S., Howard, J., Wilson, M., Simon, B., Ecgsner, S., Nguyen, D., Gauthe, D., Blake, D., Miller, C., Elferink, C., Ansari, S., Fernando, H., Trapido, E., Kane, A., 2014. Evaluation of polycyclic aromatic hydrocarbons using analytical methods, toxicology, and risk assessment research: seafood safety after a petroleum spill as an example. Environ. Health Perspect. 122 (1), 6–9. Wilson, M.J., Frickel, S., Nguyen, D., Bul, T., Echner, S., Simon, B., Howard, J., Miller, K., Wickliffe, J.K., 2015. A targeted health risk assessment following the Deepwater Horizon oil spill: polycyclic aromatic hydrocarbons exposure in Vietnamese-American shrimp consumers. Environ. Health Perspect. 123 (2), 152–159. Xia, K., Hagood, G., Childers, C., Atkins, J., Rogers, B., Ware, L., Armbrust, K., Jewell, J., Diaz, D., Gattan, N., Folmer, H., 2012. Polycyclic aromatic hydrocarbons (PAHs) in Mississippi seafood from areas affected by the Deepwater Horizon oil spill. Environ. Sci. Technol. 46, 5310–5318. https://doi.org/10.1021/es2042433. Yender, Michel, R.J., Lord, C., 2002. Managing seafood safety after an oil spill. In: Report From Seattle: Hazardous Materials Response Division. Office of Response and Restoration, National Oceanic and Atmospheric Administration (72 pp). Yitalo, G.M., Krahn, M.M., Dickhoff, W.W., Stein, J.E., Walker, C.C., Lassitter, C.K., Garrett, E.S., Desfosse, L.L., Mitchell, K.M., Nobler, B.T., Wilson, S., Beck, N.B., Benner, R.A., Koufopoulos, P.N., Dickey, R.W., 2012. Federal seafood safety response to the Deepwater Horizon oil spill. Proc. Natl. Acad. Sci. 109 (50), 20274–20279. www.pnas.org/cgi/doi/10.1073/pnas.1108886109. Ziegler, C.D., Robbat Jr., A., 2012. Comprehensive profiling of coal tar and crude oil to obtain mass spectra and retention indices for alkylated PAH shows why current methods err. Environ. Sci. Technol. 46, 3935–3942.
John, G.F., Yin, F., Mulabagal, V., Hayworth, J.S., Clement, T.P., 2014. Development and application of an analytical method using gas chromatography/triple quadrupole mass spectrometry for characterizing alkylated chrysenes in crude oil samples. Rapid Commun. Mass Spectrom. 28 (8), 948–956. Keith, L.H., 2015. The source of U. S. EPA’s sixteen PAH priority pollutants. Polycyclic Aromatic Hydrocarbons 35, 147–160. Klasing, S.A., Brodberg, R.K., 2015. Protocol for Seafood Risk Assessment to Support Fisheries Re-opening Decisions for Aquatic Oil Spills in California. November 2013 (Update March 2015). Office of Environmental Health Hazard Assessment, California Environmental Protection Agency, Sacramento, California (12 pp). Lima, A.L., Farrington, J.W., Reddy, C.M., 2005. Combustion-derived polycyclic aromatic hydrocarbons in the environment- a review. Environ. Forensic 6, 109–131. McNutt, M.K., Chu, S., Lubchenco, J., Hunter, T., Dreyfus, G., Murawski, S.A., Kennedy, D.M., 2012. Applications of science and engineering to quantify and control the Deepwater Horizon oil spill. Proc. Natl. Acad. Sci. 109 (50), 20222–20228. https://doi. org/10.1073/pnas.1214389109. Neff, J.M., 1979. Polycyclic Aromatic Hydrocarbons in the Aquatic Environment. Sources, Fates and Biological Effects. Applied Science Publishers LTD, Essex, England (262pp). Nelson, R.K., Gosselin, K.M., Hollander, D.J., Murawski, S.A., Garcia, A., Reddy, C.M., Radovic, J.R., 2019. Exploring the complexity of two iconic crude oil spills in the Gulf of Mexico (Ixtoc I and Deepwater Horizon) using comprehensive two-dimensional gas chromatography (GCxGC). Energy Fuel 33 (5), 3925–3933. https://doi.org/10.1021/ acs.energyfuels.8b04384. NIST, 2012. Certificate of Analysis. Standard Reference Material 2779. Gulf of Mexico Crude Oil. National Institute of Standards, Gaithersburg, MD USA. http://www-s. nist.gov/smors/certificate/2779.pdf. NRC, 1972. Committee on Biological Effects of Atmospheric Pollutants. Particulate Organic Matter. National Research Council, National Academies Press, Washington DC (361 pp). NRC, 1975. Petroleum in the Marine Environment. National Research Council, national Academy Press, Washington, DC (107pps). NRC, 1983. “Polycyclic Aromatic Hydrocarbons: Evaluation of Sources and Effects”. Committee on Pyrene and Selected Analogs, Board of Toxicology and Environmental Health Hazards, Commission on Life Sciences, National Research Council. National Academies Press, Washington DC (392 pp + 79 pp appendices). NRC, 1985. Oil in the Sea. Inputs, Fates and Effects. National Research Council, National Academy Press, Washington, DC (601 pp). NRC, 2003. Oil in the Sea II. Inputs, Fates and Effects. National Research Council, national Academies Press, Washington, DC (265 pp). Rheinberg, C.M., Hammit, J.K., 2012. Risk trade-offs in fish consumption: a public health perspective. Environ. Sci. Technol. 46, 12337–12346. https://doi.org/10.1021/ es302652m. Rotkin-Ellman, M., Solomon, G., 2012. FDA risk assessment of seafood contamination after the BP oil spill: Rotkin-Ellman and Solomon respond. Environ. Health Perspect.
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Viewpoint
Need to update human health risk assessment protocols for polycyclic aromatic hydrocarbons in seafood after oil spills John W. Farrington Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA
A R T I C LE I N FO
A B S T R A C T
Keywords: Polycyclic aromatic hydrocarbons (PAHs) Alkylated PAHs Seafood contamination Human health risks Deepwater Horizon oil spill
The need to include alkylated polycyclic aromatic hydrocarbons in human health risks assessments for oil contaminated seafood after crude oil spills is set forth. This is placed within the context of a brief review of the literature for PAHs and human health risk assessments after oil spills. The example of human health risk assessments for oil contaminated seafood after the Deepwater Horizon oil spill is reviewed with the conclusion that PAHs such as alkylated chrysenes/triphenylenes/benzanthracenes should have been included in the human health risk assessment and not dismissed as present in very low concentrations relative to their parent PAHs.
1. Introduction The occurrence of oil spills in areas where seafood is harvested creates concerns about health risks for consumers of this harvested seafood as noted by Yender et al. (2002) and Yitalo et al. (2012), among others. The major petroleum chemicals involved in this concern are the polycyclic aromatic hydrocarbons (PAHs). The PAHs are only one class of a complex mixture of chemicals with individual components of environmental concern. Government agencies charged with responsibilities for assessing and communicating risks associated with consumption of seafood contaminated with human synthesized or human mobilized natural chemicals of known or potential public health concern have a very difficult task. There are a multitude of both legacy contaminants such as chlorinated pesticides, polychlorinated biphenyls, and polycyclic aromatic hydrocarbons (PAHs), as well as numerous emerging contaminants of environmental concern from many human controlled or influenced processes (e.g. Gaston et al., 2019; Bricker et al., 2014; Dodder et al., 2014 and references therein). The process of identification and quantifying individual chemicals within groups of these chemicals is challenging (e.g. Hites and Jobst, 2018). Assessing risks from all individual components of these complex mixtures and interactive synergistic or antagonistic effects among them is a herculean task. In addition, Rheinberg and Hammit (2012) note the need to balance risks from eating contaminated seafood against the loss of healthful benefits of polyunsaturated fatty acids (PUFAs) which are abundant in fish. Herein, the focus is on PAHs. The challenge of seafood contaminated by PAHs and the associated human health risk has been
known and researched for at least the past 60 years (e.g. Cahnmann and Kuratsune, 1956, 1957; Andelmann and Suess, 1970; NRC, 1972, 1975, 1985, 2003; Yender et al., 2002; Baird et al., 2007). The issue of risk of carcinogenic potency of certain PAHs has dominated considerations even though for seafood safety in oil spill areas there are other toxicities associated with other PAHs. I submit that there is a need to update an aspect of methodology used in assessment of human health risk by consumption of seafood contaminated or potentially contaminated by PAHs (polycyclic aromatic hydrocarbons) in the Macondo 252 Crude oil spilled from the Deepwater Horizon ‘s (DWH) Macondo well (Yitalo et al., 2012; Xia et al., 2012). Specifically, this involves alkylated PAHs. A brief review of human health concerns associated with PAH contaminated seafood provides context. Hopefully, this paper and other recent papers providing detailed discussions of human health concerns for seafood contaminate during oil spills will lead to improved assessments for human health risk from PAHs in general, whatever the source of the PAHs (e.g. Gohlke et al., 2011; Rotkin-Ellman et al., 2012; Rotkin-Ellman and Solomon, 2012; Dickey, 2012; Wickliff et al., 2014; Dickey and Hoettel, 2016; Wilson et al., 2015). 2. Overview of PAHs Polycyclic aromatic hydrocarbons are of environmental concern because several of them have been demonstrated to have proto-carcinogenic/carcinogenic properties as reviewed over the past decades (e.g. Andelmann and Suess, 1970; Neff, 1979; NRC, 1972, 1983; and a series of International Symposia on Polynuclear Aromatic Hydrocarbons beginning in 1980 –ISPAC, 2019; among others). Dipple (1985) provides a
E-mail address: [email protected]. https://doi.org/10.1016/j.marpolbul.2019.110744 Received 29 July 2019; Received in revised form 14 November 2019; Accepted 15 November 2019 0025-326X/ © 2019 Elsevier Ltd. All rights reserved.
Please cite this article as: John W. Farrington, Marine Pollution Bulletin, https://doi.org/10.1016/j.marpolbul.2019.110744
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to the more robust MFPPOH method can introduce overestimations of concentrations in a coal tar or crude oil sample of 2 to 614% depending on the alkylated PAH. Other advances in analytical chemistry of the past two decades have addressed the challenges of separating and quantifying alkylated PAHs. Two dimensional gas chromatography (GCxGC) combined with mass spectrometry-computer data systems avoids most if not all of the problems noted in the preceding with paragraph with the capability to separate, identify and quantify parent PAHs and alkylated PAHs in a wide molecular weight range (e.g. Frysinger et al., 2003; Nelson et al., 2019). John et al. (2014) used GC-triple quadrupole mass spectrometry for characterizing alkylated chrysenes. Thus the methods for quantitative analyses are available for a full range of alkylated PAHs. However, there have been relatively few analyses of this type for the alkylated higher molecular weight PAHs, e.g. 4 to 6 rings, perhaps due to the lack of standards of the specific alkylated PAHs (e.g. John et al., 2014).
review extending back to at least the year 1775. Although not the specific subject of this paper, it is important to acknowledge that several PAHs have been shown to have adverse effects on several types of aquatic organisms under certain exposure conditions (e.g. Neff, 1979; NRC, 1975, 1985, 2003; The Royal Society, 1980). Several sources contribute PAHs to the environment. These can be divided into natural sources and human made or mobilized sources. Each of those sources can each be subdivided into PAHs from natural petroleum seeps (petrogenic) and forest and grass fires (pyrogenic), oil spills and chronic oil inputs (petrogenic) and burning of fossil fuels (pyrogenic), creosote containing pyrolysis products, or cooking of food that chars natural organics chemicals or smoking food (pyrogenic) (Blumer and Youngblood, 1975; Blumer, 1976; Lima et al., 2005; Stout et al., 2015 among others). Early diagenesis (combinations of microbial and chemical reaction mediated) transformation of small amounts of biogenic molecules can lead to specific PAHs such as perylene and retene. Erosion of ancient sediments with organic matter in various stages of diagenesis can contribute PAHs to modern ecosystems. Loss of coal from bunkers in coal powered ships has contributed coal sourced PAHs to surface sediments in some depositional areas (e.g. Tripp et al., 1981). Several recent papers have reviewed differences in the composition of PAHs from several types of pyrogenic sources and petrogenic sources and various approaches to estimating the contributions from various sources of PAHs to a given sample (e.g. Lima et al., 2005; Stout et al., 2015). Fig. 1a–d provides examples of chemical structures of PAHs. Fig. 1a provides the relationship between chemical structure containing carbon and hydrogen atoms and the shorthand notation usually used. Fig. 1b depicts parent PAH with the exception of retene which is an alkylated PAH. Both retene and perylene (Fig. 1b) have a source in early diagenesis of organic matter in sediment. Fig. 1c contains structures of several different methylchrysenes and Fig. 1d contains structures of a few of the many possible additional alkylated chrysenes. The scope of challenges for analytical chemistry and for assessment of effects of PAHs on organisms and human health is illustrated by the fact that the structures of PAHs depicted in Fig. 1 are no more than an estimated 10% (conservatively) of PAHs in various sources of input to the environment. Analytical chemistry limitations existed in the 1960s through the 1980s for identification and quantification of mainly the alkylated PAH primarily due to lack of standards and standard reference materials and the inability of gas chromatography–mass spectrometry (GC–MS) of that time period to distinguish between isomers of alkylated PAH. These limitations and several other factors led the U. S. EPA to establish the list of Priority Pollutants which contained 16 PAHs, all of which could be identified and quantified. The interesting history of the establishment of the U.S. EPA list of 16 Priority Pollutant PAHs in 1976 is set forth by Keith (2015) in an issue of Polycyclic Aromatic Compounds, Volume 35, 2015 devoted to the U.S. E.PA's Sixteen PAH Priority Pollutants (Anderson and Achten, 2015). As Keith notes, the EPA Priority Pollutant list was adopted by many countries. Over the ensuing years, EPA added eighteen alkylated PAHs of the naphthalene, flourene, phenanthrene, pyrene, and chrysene homologs for the purpose of estimating toxic hazards of contaminated soils and sediments (e.g. Antle et al., 2014). Many analysts during the past three decades have used GC–MS with selected ion monitoring using the molecular ion or prominent fragment ion plus GC retention time to quantify PAHs as noted by Ziegler and Robbat Jr (2012) and Antle et al. (2014). A methodology using “three to five ions per isomer pattern and multiple fragmentation patterns per homolog (MFPHH) has been shown to be more accurate (e.g. Ziegler and Robbat Jr, 2012; Antle et al., 2014). These authors have shown that as the analyte PAHs of interest expanded to the alkylated PAHs (e.g. C4 - naphthalenes, C2 – chrysenes), selected ion monitoring or use of one ion plus retention times from full scan GC–MS (single ion extraction method or SIE) compared
3. Human health risk assessment for seafood contaminated, or potentially contaminated, by the Deepwater Horizon oil spill The Deepwater Horizon (DWH) oil spill claimed 11 lives, the most important aspect of the accident. It was the largest marine oil spill in the U. S. history up to that time. Numerous papers have described the accident, its immediate aftermath, and the short term and long term fates and effects. (McNutt et al., 2012 and publications and references therein listed on the Gulf of Mexico Research Initiative website (www. gulfresearchinitative.org). Yitalo et al. (2012) and Xia et al. (2012) reported on human health risk assessment for seafood contaminated or potentially contaminated with PAHs from the DWH oil spill. The protocols they used were founded in the report of Yender et al. (2002) and “current information from the FDA, NOAA, and the Environmental Protection Agency (EPA) to establish a unified Deepwater Horizon seafood protocol.” (US FDA, 2010). Experience from eight specific spills beginning in 1989 with the T/V Exxon Valdez and through 1999 guided Yender et al. (2002) in their review of key aspects of a more standardized guidance for both closing and opening fisheries when considering human health risk of seafood consumption from areas here oil spills had or might have contaminated seafood. They noted various important considerations based on reviews of the literature. For example, after an oil spill, habitat utilization and behavior of marine organisms have a significant influence on which organisms are exposed to and will take up petroleum hydrocarbons. An important additional factor is that, in general, fish have a relatively high capacity for metabolizing PAHs because of induction of high levels of activity of enzymes that metabolize PAHs. The capacity of induction of the metabolizing enzymes and metabolism of PAHs is reduced in most crustaceans (e.g. lobsters, crabs and shrimp) relative to fish. For mollusks such as oysters, mussels, clams, and scallops the capacity for induction of the metabolizing enzymes and metabolism of PAHs is of “very limited capacity” (Yender et al., 2002). Humans also have the capacity to metabolize PAHs and this is connected to both the elimination and toxicity of these compounds (e.g. Alquassim et al., 2019). Yitalo et al. (2012) reported on a significant and complicated effort for assessing human health risk from eating PAHs contaminated seafood in areas of the DWH spill. A key result was “When detected, the concentrations [of individual PAHs] were at least two orders of magnitude lower than the level of concern for human health risk.”(Yitalo et al., 2012). Their paper led to a healthy scientific debate and discussion in a series of published comments and replies about various aspects of the protocols – a scientific debate that should inform in a major way relevant protocols and methodology for similar human health risk seafood assessments for future oil spills. (Rotkin-Ellman et al., 2012; Rotkin-Ellman and Solomon, 2012; Dickey, 2012; Wickliff et al., 2014). One aspect to the protocol of Yitalo et al. (2012) that needs to be revisited relates to the statements in both documents (Supplemental 2
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Fig. 1. Examples of chemical structures of polycycicaromatic hydrocarbons. 1A. Example structure of 1-methylnaphthalene with carbon and hydrogen atoms shown and a shorthand notation. 1B. Parent PAH structures except retene. Retene and perylene are products of natural organic matter diagenesis (see text). All but retene, perylene, BkF, and Cor are on the US EPA list of 16 priority PAH (by permission from Lima et al., 2005). 1C. Example methyl chrysene structures. 1D. Example alkyl chrysenes.
Information of Yitalo et al. (2012) and US FDA (2010) concerning which PAHs to include in carcinogenic risk assessment. The US FDA (2012) statement notes: “In order to interpret the cancer risk for individual PAH compounds likely to be found in the Gulf of Mexico light crude petroleum, the carcinogenic activity relative to benzo(a)pyrene (BaP) is estimated as a toxicity equivalency factor (TEF)[with reference cited U.S.EPA, 1998 in reference list herein]. TEFs for chrysene, benzo[k]fluoranthene, benz[a]anthracene, indeno[1,2,3cd]pyrene, benzo[b]fluoranthene, and bibenz[a,h]anthracene are 0.001, 0.01, 0.1, 0.1, 0.1, and 1 respectively. Tissue concentrations of PAHs other than BaP are multiplied by their respective TEF and added to the tissue concentration of BaP to determine BaP equivalent (BaPE) concentration. The BaPE concentration is considered the most valid measure of the carcinogenic potency of a complex mixture of PAH compounds. For the purpose of this risk assessment, substituted alkylated homologs of the above PAHs will be excluded from analyses due to the very low concentrations determined in the MC 252 crude oil.” (underline my emphasis). The Yitalo et al. (2012) Supporting Information statement is similar, ending with “Concentrations of alkylated homologs of the carcinogenic PAH listed above [same as the US F &DA list above] were excluded as they are found in very low levels in the Louisiana light crude oil.” However, analytical chemistry data indicate otherwise. The alkylated homologs are reportedly in a similar concentration range and in some cases may be higher in concentration in the Macondo crude oil from the DWH well. Examination of the Certificate of Analyses for Standard Reference Material (SRM) 2779 Gulf of Mexico Crude Oil reports PAH data for the crude oil obtained from the insertion tube that was receiving oil directly from the Macondo Well (of the DWH oil spill) during response operations. NIST (2012) suggests that there are more than “low levels” of several of the excluded alkylated PAHs in the DWH Macondo Well sample. Tables 1 and 2 contain data taken from the Certificate of Analyses for SRM 2779. Although most are not Certified Values, they are Reference Mass Fraction Values because over 90% of the participating laboratories used the parent PAH response factor for the corresponding alkylated group. This constraint relates in part to the issues discussed previously in this paper regarding the methodology for analyses of alkylated PAHs. Chrysene, one of the PAHs in the Yitalo et al. (2012) and US FDA (2012) list is reported as Mass Fraction of 23.3 mg/kg in the Macondo oil. An alkylated homolog, 6-Methylcrysene is reported as 15.10 mg/kg. It is likely that Yitalo et al. (2012) did not have access to the results of the NIST Certification/Reference Values noted above when they were interpreting their results. Their paper was submitted June 2, 2011. The NIST Certificate was issued June 4, 2012 Likewise, the Xia et al. paper was submitted November 21, 2011, before the NIST Certificate of Analysis was issued. My purpose is not to criticize Yitalo et al. or Xia et al. Given the concentrations of PAHs reported by Yitalo et al., there
Table 2 Concentrations of selected individual PAHs and groups of alkylated congener PAHs in NIST SRM 2779.
Mass fraction value (mg/kg)
Pyrenea 1-Methylpyreneb 4-Methylpyreneb Chryseneb 6-Methylchryseneb
14.81 ± 0.39a 12.1 ± 1.8b 21.6 ± 1.5b 23.3 ± 5.2b 15.10 ± 0.56b
a b
Mass fraction (mg/kg)
Benz[a]anthracene Chrysene Triphenylene C1-Benzanthracenes/chrysenes/triphenylenes C2-Benzanthracenes/chrysenes/triphenylenes C3-Benzanthracenes/chrysenes/triphenylenes C4-Benzanthracenes/chrysenes/triphenylenes
7.03 ± 0.85a 23.3 ± 5.2b 17.7 ± 6.7b 110 ± 7c 130 ± 10c 93 ± 12c 71 ± 16c
a
Certified mass fraction value NIST SRM 2779 Table 1 (NIST, 2012). Reference mass fraction value NIST SRM 2779 Table 2 (NIST, 2012). c Reference mass fraction value alkylated PAH groups NIST SRM 2779 Table 3 (NIST, 2012). b
may have been minimum risk to human health even if the alkylated PAHs were included. My purpose here is to raise the point, going forward to future oil spills, that alkylated PAHs for higher molecular weight PAHs can be present in some crude oils, some bunker oils, and some higher numbered fuel oils at concentrations equal to or higher than their parent PAHs. As noted in the brief review above, this has been known for many years. Therefore, these specific alkylated PAHs should not be dismissed automatically for reasons of concentrations being too low to be considered for human health carcinogenic risk. If it is important, and I submit that it is, to include parent higher molecular weight PAH in risk assessments, then it is also important to consider their alkylated PAH homologs of approximately the same or higher concentration in a spilled oil. The Xia et al. (2012) paper reported on analysis of PAHs in several local samples of smoked meats and fish and noted that the PAHs in the processed foods were below the same FDA Level of Concern (LOC) concentrations noted above for contaminated (or potentially contaminated) Gulf of Mexico seafood samples. Xia et al. (2012) also noted that the PAHs concentrations in the processed food were “similar if not higher [in concentrations] for some PAHs to those detected in the seafood samples collected in the Mississippi Gulf Coast.” Baird et al. (2007) reviewed the issue of human risk from exposure to alkylated PAHs in aquatic systems and noted the paucity of toxicity data for the alkylated PAHs with the exception of 1- and 2-methylnaphthtalene. Carcinogenic risk data were generally not available for 2 to 6 ring alkylated PAHs. However, theoretical considerations based on chemical structures of parent PAHs and the tumorigenic or mutagenic active site in the molecules suggest strongly that specific alkylated PAHs will be shown to be either tumorigenic and/or mutagenic. Baird et al. (2007) recommended a thoughtful approach to assessing human health risks for alkylated PAHs. Summarizing their recommendations as a lead sentence in each step of their strategy: 1) “The PAH families (e.g. naphthalene, phenanthrene, pyrene) of alkylated PAHs that are typically found in fish tissues and sediments need to be more thoroughly identified, including the relationship between the source PAH mixture (e.g. crude oil) and the PAHs that are available for human exposure in fish and sediment.” 2) “Identify the individual isomers of relevant PAHs found in the aquatic environment and compare them to the specific activity of those identified in the literature.” 3) “After individual and mixtures of alkylated PAHs from aquatic environments with toxicological activity are identified, the potential for concern associated with the range of concentrations of alkylated
Table 1 Concentrations of selected individual PAHs in NIST SRM 2779. PAH name
PAH name
Certified mass fraction value NIST SRM 2779 Table 1 (NIST, 2012). Reference mass fraction value NIST SRM 2779 Table 2 (NIST, 2012). 4
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PAHs observed in environmental samples needs to be estimated.” 4) “Once MOA [mode of action] known to be relevant to the toxicity and carcinogenicity of alkylated PAHs are identified, individual alkylated PAHs and common environmental mixtures of alkylated PAHs that frequently occur in the aquatic environment could be tested for their potential toxicity using a screening battery of in vitro and in vivo mechanistic studies.” 5) “Individual alkylated PAHs and mixtures of alkylated PAHs of concern identified through this process could be tested in long-term animal bioassays designed to capture the anticipated MOAs.”
Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgements Doctoral dissertation research in the laboratory of Professor James G. Quinn, to whom this Special Issue of Marine Pollution Bulletin is dedicated, provided an early introduction for me to the science-policy interface. That research brought me into the realm of interactions with state and federal agencies responsible for assessing risks to public health from seafood contaminated with organic chemicals of environmental concern. Professor Quinn, and others of my Ph. D. dissertation committee, provided calm, steady guidance while allowing me freedom to explore not only in scientific research, but also at the science-policy interface. I extend to them my profound gratitude for their wise advice. A special appreciation is extended to Jim Quinn for being an adviser and mentor for fifty-one years. I thank Bruce W. Tripp and Paul D. Boehm for comments on drafts of this paper and two anonymous reviewers for their helpful reviews. An appointment as Dean Emeritus, Woods Hole Oceanographic Institution, provided assistance in preparing this paper.
Developing and applying analytical methods that will distinguish between Chrysene and Triphenylene, and each of their alkylated homologs for the purpose of accuracy is one step in the risk assessment process (John et al., 2014; Nelson et al., 2019). This is important because Baird et al. (2007) and Sun et al. (2014) among others, review how subtle molecular structure changes can have a significant influence on toxicity, mutagenicity and toxicity. A recent example of this effect of subtle structure changes and the influence on effects has been published by Alquassim et al. (2019) comparing results of human aryl hydrocarbon receptor (AhR)reporter signaling, cytotoxicity, and gene expression responses to mono-methylchrysenes (see Fig. 1c). The authors noted that for a yeast-based reporter assay detecting human AhR mediated gene expression the 4methylchrysene was six times more potent as chrysene while 5-methylchrysene was one-third as potent as chrysene. Other methylchrysenes were more comparable to chrysene in this assay. In the interim, the State of California, USA has issued an updated protocol for seafood risk assessment in the event of oil spills contaminating seafood (Klasing and Brodberg, 2015). Apparently, this protocol takes a conservative approach compared to those discussed above (Yitalo et al., 2012; Xia et al., 2012; US FDA, 2010) and uses the following for calculation of cPAH [carcinogenic PAH] exposure equivalents in sea food as follows:
References Alquassim, A.H., Wilson, M.J., Wickliffe, J.K., Paneni, D., Overton, E.B., Miller III, C.W., 2019. Aryl hydrocarbon receptor signaling, toxicity, and gene expression responses to mono-methylchrysenes. Environ. Toxicol. 34, 992–1000. Andelmann, J.B., Suess, M.J., 1970. Polynuclear aromatic hydrocarbons in the water environment. Bull. World Health Organ. 43, 479–508. Anderson, J.T., Achten, C., 2015. Introduction to this special issue: a critical look at the 16 EPA PAHS. Polycyclic Aromatic Hydrocarbons 35, 143–146. Antle, P.M., Zeigler, C.D., Wilton, N.M., Robbat Jr., A., 2014. A more accurate analysis of alkylated PAH and PASH and its implication in environmental forensics. Int. J. Environ. Anal. Chem. 94 (4), 332–347. Baird, S.J., Bailey, E.A., Vorhees, D.J., 2007. Evaluating human risk from exposure to alkylated APHs in an aquatic system. Hum. Ecol. Risk. Assess. 13, 322–338. Blumer, M., 1976. Polycyclic aromatic hydrocarbons in nature. Sci. Am. 234, 35–45. Blumer, M., Youngblood, W.W., 1975. Polycyclic aromatic hydrocarbons in soils and recent sediments. Science 188, 53–55. Bricker, S., Lauenstein, G., Maruya, K., 2014. NOAA’s mussel watch program: incorporating contaminants of emerging concern (CECs) into a long-term monitoring program. Mar. Pollut. Bull. 81, 289–290. Cahnmann, H.J., Kuratsune, M., 1956. PAH in oysters collected in polluted waters. Proc. Am. Assoc. Cancer Res. 2, 99. Cahnmann, H.J., Kuratsune, M., 1957. Determination of PAH in oysters collected in polluted waters. Anal. Chem. 29, 1312–1317. Dickey, R.W., 2012. Correspondence. FDA risk assessment of seafood contamination after the BP oil spill. Environ. Health Perspect. 120 (2), A54–A55. Dickey, R., Hoettel, M., 2016. Seafood and beach safety in the aftermath of the Deepwater Horizon oil spill. Oceanography 29 (3), 196–203. https://doi.org/10.5670/oceanog. 2016.83. Dipple, A., 1985. Polycyclic aromatic hydrocarbon carcinogenesis. An introduction. In: Harvey (Ed.), Polycyclic Aromatic r and Carcinogenesis. ACS Symposium Series Volume 283. American Chemical Society, Washington, DC, pp. 1–17. Dodder, N., Maruya, K., Ferguson, P., Grace, R., Klosterhaus, S., La Guardia, M., Lauenstein, G., Ramirez, J., 2014. Occurrence of contaminants of emerging concern in mussels (Mytilus spp.) along the California coast and the influence of land us, storm water discharge, and treated wastewater effluent. Mar. Pollut. Bull. 81, 340–346. Frysinger, G., Gaines, R.B., Xu, L., Reddy, C.M., 2003. Resolving the unresolved complex mixture in petroleum contaminated sediments. Environ. Sci. Technol. 37, 1653–1662. Gaston, L., Lapworth, D.J., Stuart, M., Arnscheidt, J., 2019. Prioritization approaches for substances of emerging concern in groundwater: a critical review. Environ. Sci. Technol. 53, 6106–6122. Gohlke, J.M., Doke, D., Tipre, M., Leader, M., Fitzgerald, T., 2011. A review of seafood safety after the Deepwater Horizon blowout. Environ. Health Perspect. 119 (8), 1062–1069. Hites, R., Jobst, K., 2018. Is nontargeted screening reproducible? Environ. Sci. Technol. 52, 11975–11976. ISPAC, 2019. A short history of ISPAC (International Symposium on Polynuclear Aromatic Compounds). http://www.louisville.edu/org/ispac/history.htm, Accessed date: 20 March 2019.
“In order to determine exposure equivalents for cPAHs in seafood, the wet weight concentration of each cPAH is first converted to an equivalent concentration of BaP. To do this, individual cPAHs plus their alkylated homologs are multiplied by their respective PEF [potency equivalent factor] to derive a BaPE concentration for that chemical.” 4. Concluding thoughts There has been progress with addressing the challenges associated with risks associated with seafood contaminated with PAHs, no matter what the source of PAH. Much more needs to be done, especially with respect to alkylated PAHs. Over ten years have passed since the Baird et al. (2007) review and it is timely for another comprehensive review of human health risks associated with alkylated PAHs alone and in combinations with other alkylated and parent PAHs. Two other points seem obvious and worthy of further consideration. First, as noted in the paper by Xia et al. (2012) cited earlier, PAHs are present in a variety of foods from a variety of sources. It would seem appropriate to not consider human health risk from the various sources in isolation. For example, why not assess the human health risk from the PAHs in the oil spill contaminated seafood and then place it in the accumulative exposure for PAHs via all sources of food to obtain a more meaningful human health risk assessment? Second, it is clear, especially in coastal areas near population and industrial centers that PAHs are but one class of contaminants to consider individually and in combination for assessing human health risks associated with seafood consumption. Author contribution John W. Farrington declares that he is solely responsible for the 5
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