Endocrine disruption and differential gene expression in sentinel fish on St. Lawrence Island, Alaska: Health implications for indigenous residents☆
Graphical abstract
Introduction
Arctic Indigenous Peoples are among the world's most highly exposed populations to certain persistent organic pollutants (POPs) (Ayotte et al., 1996, Ayotte et al., 1997, Blais, 2005, Dewailly et al., 1989, Dewailly et al., 1999, Walker et al., 2003). The Arctic acts as a “cold trap” and is a hemispheric sink for certain POPs that are transported from lower latitudes through atmospheric global distillation (Blais, 2005, Wania and Mackay, 1993, Wania and Mackay, 1996). Once POPs enter the Arctic, their deterioration slows due to low temperatures and low intensity sunlight, which makes them available for long-term incorporation into biological systems (Bard, 1999, Wania and Mackay, 1993). POPs bioaccumulate and biomagnify in the lipid-rich arctic food webs, some to toxic levels (Bard, 1999, Wania and Mackay, 1993). Arctic Indigenous Peoples often subsist on high trophic level, long-lived animals, and thus may ingest levels of POPs that lead to adverse health outcomes, such as thyroid disorders, developmental disorders, and certain cancers (Ayotte et al., 1995, Wania and Mackay, 1993). These findings prompted the inclusion of concern about exposure to POPs by Arctic Indigenous Peoples in the Stockholm Convention on Persistent Organic Pollutants, which bans or restricts some of the world's most toxic POPs, including polychlorinated biphenyls (PCBs) (UNEP, 2001).
PCBs disrupt several endocrine pathways, including the thyroid and sex steroid axes, and, depending upon the particular congener, display estrogenic or anti-estrogenic effects (Brown et al., 2014b, Cooke et al., 2001, Letcher et al., 2010, Schell et al., 2008, Schell et al., 2014). PCB exposure in humans induces numerous adverse effects, including low birth weight, slow growth, reduced immunocompetence, cancer, reproductive impairment, neurological impairment, and reduced intelligence (Ayotte et al., 2003, Boucher et al., 2009, Carpenter, 2006, Dallaire et al., 2006, Dallaire et al., 2014, Lauby-Secretan et al., 2013, Schantz et al., 2003, Weisglas-Kuperus, 1998, WHO, 2016).
Global distillation is not the only source of POPs in the Arctic. Many locally contaminated sites also contribute POPs to the arctic environment with implications for the health of people and wildlife (Brown et al., 2014a). For example, Alaska has approximately 600 formerly used defense (FUD) sites dating from World War II and the Cold War, many of which are located adjacent to Alaska Native villages in remote parts of the state (Scrudato et al., 2012, von Hippel et al., 2016). When the U.S. military abandoned these sites at the end of the Cold War, a legacy of contaminants, including PCBs, remained. Given that the village residents did not elect to use chemicals at the FUD sites or benefit from them, and yet likely suffer the consequences of exposure, these sites present cases of environmental injustice (Rechtschaffen et al., 2009).
A multitude of factors determines the environmental fate of PCBs (Gioia et al., 2013, Lammel and Stemmler, 2012, Macdonald et al., 2005, Scheringer, 2009, Wania and Mackay, 1993). Global distillation results in a shift to a greater mass fraction of lightly-to intermediately-chlorinated PCBs with higher latitude because heavier PCBs are less volatile and condense out of the atmosphere closer to their emission source (Iwata et al., 1993, Scheringer, 2009, Wania, 2003, Wania and Mackay, 1993, Wania and Mackay, 1996). This latitudinal fractionation enriches arctic environments with less chlorinated PCBs (Iwata et al., 1994, Wania and Mackay, 1993). For example, atmospheric deposition results in tri-chlorinated congeners predominating in surface sediments of the Bering Sea (contributing 47–92% of total PCBs), followed by penta-chlorinated and hexa-chlorinated congeners (Hong et al., 2012). Conversely, PCBs derived from point sources such as FUD sites are more likely to be heavier congeners (Muir et al., 2000). Differentiating contamination due to atmospheric deposition vs. local sources is important for site characterization and remediation. For example, PCB contamination due strictly to global distillation could not be ameliorated via removal of materials from a FUD site. On the other hand, detection of PCB contamination from a FUD site could justify the initiation or extension of site clean-up.
The most expensive clean-up of an Alaskan FUD site to date occurred at Northeast Cape on St. Lawrence Island (SLI; Fig. S1). SLI is the largest island in the Bering Sea and has a population of ca. 1600 Siberian Yupik Alaska Natives who live a mostly subsistence lifestyle in two extant villages: Gambell and Savoonga. Northeast Cape is the site of a former Yupik village that the residents of Gambell and Savoonga would like to reestablish; it is actively used for subsistence activities (USATSDR, 2015). The U.S. Air Force acquired the lands at Northeast Cape in 1952 under Public Land Order 790 and established an Aircraft Control and Warning Station (AC&WS) in 1957 (ADEC, 2013b, USBLM, 2015). The Northeast Cape facility operated until 1972 as a surveillance station, first as an AC&WS, then as a White Alice (Alaska Integrated Communications and Electronics) site to detect and provide early warning of enemy aircraft and missile attacks during the Cold War (ADEC, 2013b). At least 30 contaminated locations occur in a 19 km2 area (ADEC, 2013b). Contamination of soils, surface waters, groundwater, and biota at Northeast Cape derives from fuel spills and releases of PCBs, pesticides, solvents, and metals (ADEC, 2013b, Byrne et al., 2015, Scrudato et al., 2012). Between 1985 and 2014, $120 million was spent on remediation of the FUD site at Northeast Cape, including the removal of structures, storage tanks and drums, and various contaminated wastes, soil and sediments (ADEC, 2013a, ADEC, 2013b, USACE, 2012). In 2014, the U.S. Army Corps of Engineers determined that sufficient cleanup occurred to cease active remediation activities.
SLI residents have concentrations of PCBs in their blood serum that are about six times higher, on average, than found in people who live in other U.S. states (Carpenter et al., 2005). Additionally, residents of Savoonga who also use Northeast Cape for subsistence activities have higher levels of PCBs in their blood serum than SLI residents who are not associated with Northeast Cape (Carpenter et al., 2005). Together, these findings suggest that atmospheric deposition of PCBs in the Arctic coupled with biomagnification into subsistence foods results in elevated PCBs in SLI residents (Welfinger-Smith et al., 2011), while some residents experience added exposure from military contamination at Northeast Cape (Carpenter et al., 2005).
From the slopes of the Kinipaghulghat Mountains above Northeast Cape, the Suqitughneq River flows north through the coastal tundra and the FUD site into the Bering Sea (Fig. S1). Freshwater habitats accumulate contaminants from their watershed (Luoma and Rainbow, 2008, Sumpter and Jobling, 1995) and fish have excellent utility as sentinels of the aquatic environment (Tierney et al., 2014). Therefore, at the request of SLI residents, we examined congener-specific profiles of PCBs and biological responses in fish collected from the Suqitughneq River to determine: 1) if remaining contamination is due primarily to the FUD site or to atmospheric deposition, 2) if biologically relevant levels of PCBs remain in fish at the conclusion of site remediation, and 3) if health findings in fish have implications for the health of the Yupik people on SLI. We examined two native fish species that commonly inhabit contaminated and clean freshwater sites on SLI: Alaska blackfish (Dallia pectoralis) and ninespine stickleback (Pungitius pungitius; hereafter ‘stickleback’). We previously demonstrated that concentrations of numerous POPs in stickleback tissues closely mirror concentrations in the blood serum of SLI residents, indicating that stickleback are an effective sentinel species on the island (Byrne et al., 2015, Byrne et al., 2017).
Section snippets
Fish collection and processing
Ninespine stickleback and Alaska blackfish were collected in June 2012 and June–July 2013 from the Suqitughneq River at Northeast Cape (Fig. S1), the Tapisaggak River at Northeast Cape (a nearby reference site located in a separate drainage; stickleback only), and Troutman Lake in the village of Gambell (stickleback only). Fish were sampled from the different sites on the same days and were processed with the same protocols. Fish were collected using unbaited 0.32 cm and 0.64 cm wire-mesh
Results & discussion
Despite fish mobility that makes site-based differences in contaminant load harder to detect, those fish collected at the intersection of the Suqitughneq River and streamlets that drain the FUD site had elevated PCB concentrations (Fig. 1). Stickleback and Alaska blackfish are low trophic level fish, yet their total PCB levels in the Suqitughneq River were above U.S. Environmental Protection Agency (EPA) guidelines for human consumption (cancer risk for human consumption of fish: for
Conclusions
Despite extensive remediation at Northeast Cape, short-lived, lower trophic level fish in the Suqitughneq River remain contaminated with high levels of PCBs. Furthermore, most of the contamination originated from the FUD site. PCBs may have been liberated from sediments during site remediation, causing contamination of resident animals (Scrudato et al., 2012), a phenomenon seen in some other PCB remediation projects (Voie et al., 2002). Alternatively, or in addition, PCBs may have migrated down
Acknowledgements
Research reported in this publication was supported by the National Institute of General Medical Sciences of the National Institutes of Health under Award Number P20GM103395. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. Funding was also provided by the National Institute of Environmental Health Sciences (NIEHS grant numbers 1RO1ES019620 and 2RO1ES019620), the University of Alaska Anchorage
References (81)
- et al.
Health risk assessment for Inuit newborns exposed to dioxin-like compounds through breast feeding
Chemosphere
(1996) - et al.
Arctic air pollution and human health: what effects should be expected?
Sci. Total Environ.
(1995) - et al.
PCBs and dioxin-like compounds in plasma of adult Inuit living in Nunavik (arctic Quebec)
Chemosphere
(1997) - et al.
Functional characterization of a full length pregnane X receptor, expression in vivo, and identification of PXR alleles, in zebrafish (Danio rerio)
Aquat. Toxicol.
(2013) Global transport of anthropogenic contaminants and the consequences for the arctic marine ecosystem
Mar. Pollut. Bull.
(1999)- et al.
Exposure to sublethal levels of PCB-126 impacts fuel metabolism and swimming performance in rainbow trout
Comp. Biochem. Physiol., Part B
(2016) - et al.
Characterisation of transcriptional responses to dioxins and dioxin-like contaminants in roach (Rutilus rutilus) using whole transcriptome analysis
Sci. Total Environ.
(2016) - et al.
Exposure to polybrominated diphenyl ethers and perfluoroalkyl substances in a remote population of Alaska Natives
Environ. Pollut.
(2017) - et al.
Growth in Inuit children exposed to polychlorinated biphenyls and lead during fetal development and childhood
Environ. Res.
(2014) - et al.
Perchlorate exposure does not modulate temporal variation of whole-body thyroid and androgen hormone content in threespine stickleback
General Comp. Endocrinol.
(2015)
Exogenous iodide ameliorates perchlorate-induced thyroid phenotypes in threespine stickleback
General Comp. Endocrinol.
Occurrence of polychlorinated biphenyles (PCBs) together with sediment properties in the surface sediments of the Bering Sea, Chuckchi Sea and Canada Basin
Chemosphere
Association between serum organochlorines and global methylation level of leukocyte DNA among Japanese women: a cross-sectional study
Sci. Total Environ.
Persistent organochlorine residues in sediments from the Chukchi Sea, Bering Sea and Gulf of Alaska
Mar. Pollut. Bull.
CAR and PXR: xenosensors of endocrine disrupters?
Chem. Biol. Interact.
Carcinocenicity of polychlorinated biphenyls and polybrominated biphenyls
Lancet Oncol.
Exposure and effects assessment of persistent organohalogen contaminants in arctic wildlife and fish
Sci. Total Environ.
Recent climate change in the Arctic and its impact on contaminant pathways and interpretation of temporal trend data
Sci. Total Environ.
Hydroxylated polychlorinated biphenyls (OH-PCBs) induce vitellogenin through estrogenic activity in primary-cultured hepatocytes of the Xenopus laevis
Chemosphere
Perchlorate disrupts embryonic androgen synthesis and reproductive development in threespine stickleback without changing whole-body levels of thyroid hormone
General Comp. Endocrinol.
Why biota still accumulate high levels of PCB after removal of PCB contaminated sediments in a Norwegian fjord
Chemosphere
Neurodevelopmental, immunological and endocrinological indices of perinatal human exposure to PCBs and dioxins
Chemosphere
Site Report for Northeast Cape, St. Lawrence Island Alaska
Site Summary for Northeast Cape Formerly Used Defense Site
Genome evolution and meiotic maps by massively parallel DNA sequencing: spotted gar, an outgroup for the teleost genome duplication
Genetics
HTSeq–A Python framework to work with high-throughput sequencing data
Bioinformatics
Assessment of pre- and postnatal exposure to polychlorinated biphenyls: lessons from the Inuit Cohort Study
Environ. Health Perspect.
Biogeochemistry of persistent bioaccumulative toxicants: processes affecting the transport of contaminants to remote areas
Can. J. Fish. Aquat. Sci.
C-Myc and its target FoxM1 are critical downstream effectors of constitutive androstane receptor (CAR) mediated direct liver hyperplasia
Hepatology
Trimmomatic: a flexible trimmer for Illumina sequence data
Bioinformatics
Prenatal exposure to polychlorinated biphenyls: a neuropsychologic analysis
Environ. Health Perspect.
Polychlorinated biphenyl profiles in ringed seals (Pusa hispida) reveal historical contamination by a military radar station in Labrador, Canada
Environ. Toxicol. Chem.
PCB related effects thresholds as derived through gene transcript profiles in locally contaminated ringed seals (Pusa hispida)
Environ. Sci. Technol.
Persistent organochlorine pesticide exposure related to a formerly used defense site on St. Lawrence Island, Alaska: data from sentinel fish and human sera
J. Toxicol. Environ. Health, Part A
Polychlorinated biphenyls (PCBs): routes of exposure and effects on human health
Rev. Environ. Health
Polychlorinated biphenyls in serum of the Siberian Yupik people from St. Lawrence Island, Alaska
Int. J. Cicumpolar Health
Disruption of steroid hormone signaling by PCBs
Effect of prenatal exposure to polychlorinated biphenyls on incidence of acute respiratory infections in preschool Inuit children
Environ. Health Perspect.
DNA methylation and demethylation: a pathway to gametogenesis and development
Mol. Reprod. Dev.
Concentration of organochlorines in human brain, liver, and adipose tissue autopsy samples from Greenland
Environ. Health Perspect.
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This paper has been recommended for acceptance by Dr. Sarah Michele Harmon.