Increasing PerfluoroalkylContaminants in East GreenlandPolar Bears (Ursus maritimus): ANew Toxic Threat to the ArcticBearsR . D I E T Z , * , † R . B O S S I , ‡ F . F . R I G É T , †

C . S O N N E , † A N D E . W . B O R N §

Department of Arctic Environment and Department ofAtmospheric Environment, National Environmental ResearchInstitute (NERI), University of Aarhus, Frederiksborgvej 399,P. O. Box 358, DK-4000 Roskilde, Denmark,and Greenland Institute of Natural Resources,P. O. Box 570, DK-3900 Nuuk, Greenland

Received November 2, 2007. Revised manuscript receivedJanuary 17, 2008. Accepted January 17, 2008.

A well-defined subsample of 128 subadult (3–5 years) polarbears (Ursus maritimus) from 19 sampling years within theperiod1984–2006was investigatedforperfluoroalkylcontaminants(PFCs). Linear regression analysis of logarithmic-transformedmedian concentrations showed significant annual increases forPFOS (4.7%), PFNA (6.1%), PFUnA (5.9%), PFDA (4.3%), PFTrA(8.5%), PFOA (2.3%), and PFDoA (5.2%). For four of the PFCs, aLOESSsmoothermodelprovidedsignificantlybetterdescriptions,revealing steeper linear annual increases for PFOSA of9.2% after 1990 and between 18.6 and 27.4% for PFOS, PFDA,and PFTrA after 2000. Concentrations of ΣPFCs, by 2006,exceeded the concentrations of all conventional OHCs(organohalogen compounds), of which several have beendocumented to correlate with a number of negative healtheffects. If the PFC concentrations in polar bears continue toincrease with the steepest observed trends, then the lowest no-adverse-effect level (NOAEL) and lowest-adverse-effect level(LOAEL) detected for rats and monkeys will be exceeded in2014–2024. In addition, the rapidly increasing concentrations ofPFCs are likely to cause cumulative and combined effects onthe polar bear, compounding the already detected threats fromOHCs.

IntroductionFour key criteria exist to include persistent organic pollutants(POPs) in international conventions: chemical persistence,bioaccumulating properties, long-range transport and ad-verse effects (1). Perfluoroalkyl contaminants (PFCs) havenot been fully documented to meet the criteria for inclusionunder the Stockholm convention on POPs; but PFCs with 8or more carbons are likely to be identified for inclusion onthe POPs list (e.g., see refs 2–5). The use of most conventionalPOPs or organohalogenated compounds (OHCs) such as

PCBs, HCB, PCDD/Fs and DDT are subject to phase outs,emission reductions, or limited use due to national bans andinternational conventions such as the UNECE LRTAP (LongeRange Transboundary Air Pollution) Convention and its POPsprotocol. However, a number of newly emerging contami-nants including PFCs, have not yet been regulated (6). Dueto the observed toxicity of PFOS, the 3M Company com-menced reduction of perfluorooctane sulfonyl fluoride(PFOSF) in 2001 (7, 8).

Smithwick et al. (9) argued that polar bears are animportant sentinel species for Arctic marine food webs,because they are apex predators with well-studied populationdynamics and circumpolar distribution. The presence anddistribution of PFOS in liver tissues of this species were firstdescribed by Giesy and Kannan (2) for bears from Alaska,and later Bossi et al. (5), Martin et al. (3), and Kannan et al.(10) reported that PFC concentrations in polar bears are thehighest in any species to date. Smithwick et al. (11, 12)provided further details on age, gender, and geographic trendsof PFCs. In addition, it has been shown that polar bears fromEast Greenland and southern Hudson Bay carry the highestPFC concentrations among polar bears (12). The high livertissue concentration observed in East Greenland (e.g., PFOS,2140 ng/g ww) was in the magnitude of ΣPCB, and such highexposures raised the question of how the concentrations ofPCAs have evolved over time. Detecting such a time trendbecame the goal of the present investigation.

Studies on Canadian and Alaskan polar bears haveindicated an increase in PFCs in the period from 1982 to2002 (9). Such time trends have not been conducted since;neither have they been conducted for the Eastern Arctic suchas Greenland. Studies of ringed seals (Phoca hispida) fromGreenland waters have, however, shown increases in PFCsin both East and West Greenland between 1982 and 2003(13). Time trend studies on PFCs in Canadian ringed sealsfrom two regions have shown both increases and in somecases followed by decreases, depending on the area, period,and congener in question (8).

In 2001, PFCs in the polymers and their degradationproduct as well as residuals during manufacture and use offire-fighting foams, cleaners, lubricants, and various coatingswere discovered as an anthropogenic and novel group ofpersistent organic pollutants in the environment and humans(2). Perfluorinated surfactants have distribution patternssimilar to those of PCBs, which likewise biomagnify in themarine food webs and show the highest concentrations inEast Greenland (e.g., see refs 6 and 14–17). Unlike PCBsswhich accumulate in lipid-rich tissuesPFCs bind to bloodproteins and accumulate mainly in the liver, kidneys, andbile secretions. Due to low volatility of PFCs, their atmo-spheric transport to remote regions such as the Arctic hadbeen unexpected (18–21). Theories about PFCs being trans-ported to the Arctic waters via ocean currents, wherebiomagnification will take place, have also been suggested(22, 23).

In the present paper we present PFC measurement inlivers of a well-defined sample of subadult (3–5 years) EastGreenland polar bears including a discussion on healthimplications and future wildlife exposure scenarios incombination with threats from conventional OHCs and highmercury loads (6, 24–37).

Materials and MethodsSamples and Age Determination. Polar bear samples werecollected from Ittoqqortoormiit (Scoresby Sound) in CentralEast Greenland from 1984 to 2006 in cooperation with local

* Corresponding author phone:+45 46301938; fax:+45 46301914;e-mail: rdi@dmu.dk.

† Department of Arctic Environment, NERI, University of Aarhus.‡ Department of Atmospheric Environment, NERI, University of

Aarhus.§ Greenland Institute of Natural Resources.

Environ. Sci. Technol. 2008, 42, 2701–2707

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Published on Web 02/29/2008

Inuit subsistence hunters. Samples were frozen to -20 °C,shipped to Denmark, and stored at-20 °C. In the laboratory,liver samples were lightly thawed before chemical analysiswas performed. The ages of the bears were estimated bycounting annual layering in decalcified thin sections (14 µm) stained in toluidine blue in the cementum of the canineor premolar tooth, as described by Dietz et al. (38). Smithwicket al. (11) documented that the ΣPFC increased significantlywith age. Hence, the 113 bears selected for this study weresubadults at age 3–5 years to exclude age as a factor ofvariability (see Table T2, Supporting Information). Thissubsample was selected from a total of 465 bears.

Extraction and Analysis. The extraction method wasbased on ion pairing as described by Bossi et al. (13). 13C2-PFDA and 13C4-PFOS were used as surrogate standards.Instrumental analysis was performed by liquid chromatog-raphy-tandem mass spectrometry (LC-MS-MS) with elec-trospray ionization (ESI). The extracts (20 µL injectionvolume) were chromatographed on a C18 Betasil column(2.1 mm × 50 mm, Thermo Hypesil-Keystone, Bellafonte,PA) using an Agilent 1100 Series HPLC (Agilent Technologies,Palo Alto, CA). The HPLC was interfaced to a triple quadrupoleAPI 2000 (Sciex, Concorde, Ontario, Canada) equipped witha TurboIon Spray source operating in negative ion mode.Instrument setup, quality assurance and calibration proce-dures as well as the standards and reagents used are describedin detail by Bossi et al. (13).

Statistic Methods. Analyses of temporal trends followedthe ICES (International Council for the Exploitation of theSea) temporal trend assessment procedure (39). The log-median concentration is used as the annual contaminantindex value. The total variation over time is partitioned intoa linear and a nonlinear component. Linear regressionanalysis is applied to describe the linear component, and aLOESS smoother (locally weighted scatterplot using aweighted quadratic least-squares regression smoothing) witha window width of 7 years is applied to describe the nonlinearcomponent. The linear and nonlinear components are testedby means of an analysis of variance. The theory behind themethod is described in detail by Fryer and Nicholson (40, 41).The statistical analyses were performed using version 2.3.1of the free software R.

Results and DiscussionObserved Increases. A well-defined subsample of 128subadult (3–5 years) East Greenland polar bears was selectedamong 463 individuals from 19 sampling years within theperiod 1984–2006 and analyzed for liver tissue PFC concen-trations. Annually significant increasing concentrations from2.3 to 8.5%/year were found using a log-linear model forseven of eight PFCs (PFOS, 4.7%; PFOA, 2.3%; PFNA, 6.1%;

PFDA, 4.3%; PFUnA, 5.9%; PFDoA, 5.2%; PFTrA, 8.5%), whilePFOSA did not show any significant trend (Table 1). Per-fluorohexane sulfonate (PFHxS) was not found in detectableconcentrations in any of the samples.

For PFOS, PFOSA, PFDA, and PFTrA, a nonlinear LOESSsmoothermodelprovidedasignificantlybetter(P,0.020–0.001)time trend description than the log-linear model (Table 1).The LOESS smoother revealed steeper linear increases forthese four PFCs after 1990 or 2000 (Figure 1). For PFOSA, asignificant (P < 0.001) annual log-linear increase of 9.2%/year was estimated after 1990, and the remaining three PFCsshowed even steeper significant trends (p< 0.008) after 2000with yearly increases from 18.6 to 27.4% (PFOS, 19.7%; PFDA,18.6%; PFTrA, 27.4%). In 2006, the sum PFC median was 3375 ng/g ww of which PFOS (2 878 ng/g ww) was the majorcontributor, followed by PFNA (216 ng/g ww), PFUnA (91.9ng/g ww), PFDA (82.5 ng/g ww), PFTrA (65.3 ng/g ww), PFOSA(16.5 ng/g ww), PFOA (12.9 ng/g ww), and PFDoA (12.3 ng/gww) (see Table T2, Supporting Information). The smoothercurves were not influenced by the cluster of elevatedconcentrations in 1999 and 2000 for PFOSA, PFNA, and PFDAas these did not have an effect on the median which wouldhave been the case if the curve had been based on the means.Also the 2006 concentrations for half of the PFCs (PFOS,PFNA, PFDA, and PFTrA) were quite high. For three of these,where the LOESS smoother proved to be better than thelinear model for the entire period and a subsequent lineartrend was calculated for the 2000–2006 period, 2006 had asignificant effect on the calculated trends. Whether this sharpincrease will continue, the future sampling and analysis willshow. It should, however, be noted that the conservativeprediction presented in Figure 2 based on the significantlog-linear increases calculated for the entire period 1984–2006is not particularly affected by the high 2006 concentrations.

Increases similar to those found in the East Greenlandpolar bears have been detected in bears from northern BaffinIsland (5.9–21.2%/year) and in Alaska (5.1–13.2%/year) withinthe period of 1972-2002 (9). In addition, the East Greenlandpolar bear PFC increases were relatively similar to the annualincreases detected in ringed seals from the same area andperiod (1986–2003) ranging from 3.3 to 8.2% (13). Ringedseals from West Greenland showed annual increases of1.7–5.9% from 1982 to 2003, and ringed seals from Arviat andwestern Hudson Bay, eastern Canadian Arctic showedincreases from 3.6 to 26.0% (1992–1998/2005) and 4.5–10.6%(1972–2000/2005), respectively, recalculated from the pre-sented doubling time in years (8, 13). However, PFOS andPFOSA concentrations showed maximum concentrationsduring 1998 and 2000 in ringed seals from Arviat and ResoluteBay, with statistically significant decreases from 2000 to 2005.Such a decrease has been detected neither in the Greenland,

TABLE 1. Results of Linear Regression Analysis, Using Log-Transformed Annually Median PFC Concentrations, Including a Test ofWhether the LOESS Smoother Defined the Temporal Trend Better than the Linear Modela

log-linear regression (1984–2006)log-linear trend for linear period defined by LS

2000–2006 (n ) 5) or 1990–2006 (n ) 13)

contaminant P r ntest whether LOESS smoother (LS) is

better than the linear model P P r n

PFOS <0.001 0.047 19 0.020 0.004 0.197 5PFOSA 0.726 -0.006 19 0.006 <0.001 0.092 13PFOA 0.006 0.023 18 0.107PFNA <0.001 0.061 19 0.630PFDA <0.001 0.043 19 0.001 <0.001 0.186 5PFUnA <0.001 0.059 19 0.438PFDoA <0.001 0.052 19 0.072PFTrA <0.001 0.085 19 0.021 0.008 0.274 5a In significant cases, a log-linear regression was conducted for the latest linear period. P denotes the probability, R the

slope, and n the number of years used in the test. Italic numbers denote significant tests.

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Canadian, or Alaskan polar bears nor in ringed seals fromGreenland (ref 13, Bossi unpublished data, and present study).

PFC Levels Compared with Other OHC Contaminants.By 2006, ΣPFCs had increased to a higher concentration (3375 ng/g ww) than most of the conventional OHC (reportedin adipose on lw basis) reported up to the turn of themillennium. The only exception was ΣPCBs, which by 2000were reported to be 6 470 ng/g lw corresponding to 5823ng/g ww measured in adipose tissue of subadult polar bearsfrom the same region (42). However, according to Gebbicket al. (43), the ΣPCB concentration in liver is only 52% of theadipose concentration on a ww basis. This means that liverconcentrations in the subadult East Greenland polar bears

must be in the magnitude of 3 037 ng/g ww, which is lowerthat the ΣPFCs. At these concentration levels, a number ofadverse health effects have been detected in East Greenlandand Svalbard polar bears including reduced size of repro-ductive organs, liver and kidney tissue alterations, reductionof bone mineral density, disruption of various hormones,and impairment of the immune system (24, 26–34, 36, 37).

Trends in Relation to Transport Pathways. PFOS pro-duction by 3M, the major source of production worldwide,ceased in North America after 2001 and surprisingly soonthis was reflected in Canadian ringed seals, indicative of ashort-term transport pathway such as airborne transport (8).However, the continued increase in East and West Greenland

FIGURE 1. Temporal trends of eight PFC compounds in East Greenland polar bears based on medians (filled points) from 19 yearsfrom 1984 to 2006 derived from 128 bears (open points) between 2 and 5 years of age. Solid lines represent log-linear regressionlines or LOESS smoother lines in cases where the smoother was a significantly better description than the regression line. Brokenlines represent 95% confidence limits.

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indicates other primary sources and different pathways tothese regions compared with Arctic Canada, with implicationsfor the future trends in these contaminants. There is nodocumentation for increased production in Europe or Asiawhich could explain such differences. Therefore, it could bespeculated that the continued increase may represent a timelag in the transport to the East Greenland Arctic. Atmospherictransport is quite rapid (measured in days), whereas oceantransport could be expected to be much slower as oceancurrents over the Arctic Ocean may take decades or evencenturies (44–46). In a recent work, Wania (23) failed to resolvewhether current atmospheric sources or legacy oceanicsources are responsible for perfluorooctanoic acid (PFOA)and other perfluorinated chemicals in Arctic wildlife. How-ever, Wania (23) also concluded that past discharges appearto be the dominant source of PFOA in the Arctic Ocean,which could supply PFOA to the Arctic for decades, whichwas supported by R. Macdonald in an interview by Renner(44).

PFOS and PFOA have low volatility compared to OHCs,and the high water solubility of these compounds makes itprobable that PFOA and PFOS will spread directly via watercurrents (7). Although the percentage world use of PFC-related compounds varies according to source, the percentageuse in fire-fighting chemicals may be as high as 16.3% (7).PFOS in fire-fighting foams used on offshore oil platformsin Norwegian waters constitute the largest source; that todate has been 54000 kg; and some 15600 kg still remains (21).To these figures a PFOS input from other marine sourcesshould be added, such as mobile rigs, ships, and ferries, inthe magnitude of 1700 kg (21). Another way of estimating thetotal PFOS in the North Atlantic could be to calculate thetotal amount based on the average of 10 pg/L presented byYamashita et al. (47). Assuming an area of 30 million km2

and a water depth of 1000 m, as much as 300000 kg of PFOSmay be present in the North Atlantic. If the polar bearscontinue to experience an increase in PFCs in coming decadesdue to the above-mentioned sources and pathways, it isrelevant to model the continued increase and combine suchconcentrations with effect levels.

Toxic Implications. The liver is the primary target organfor PFCs. Laboratory tests have linked perfluorinated com-pounds to hepatic histopathological changes in variousvertebrates and humans (48–51). It has also been observedthat these chemicals cause peroxisome proliferation andinduction of various enzymes involved in lipid metabolism(52–55). In a study of liver histopathology in East Greenlandpolar bears sampled during 1999–2002, where the PFCconcentrations were significantly lower than today, none ofthe observed lesions could be linked to differences withinthe relatively limited range the PFC concentrations (56).

Observed developmental effects from exposure to PFOSand PFOA include increased pup mortality, reduction in fetalweight, cleft palate, placental edema, delayed skeletal os-sification, and cardiac abnormalities in rats, rabbits, and mice(57, 58). PFOA also reduces testosterone and increasesestradiol in rats (65). While PFDA and PFOA do not seem tohave a teratogenic effect (58), long-term PFC exposure mayserve as tumor promoters and inhibit gap junction inter-cellular communication (54, 55, 60) as well as impact onblood biochemistry and hematological parameters (61–65).Inhibition of the gap junction intercellular communication(GJIC), as the major pathway of intracellular signal trans-duction, may lead to teratogenesis, neuropathy, infertility,diabetes, autoimmune disorders, cancer, and other diseases,according to Trosko et al. (66). PFOA has induced testis cancer,and PFOS and EtFOSE have induced liver cancer in experi-mental animals (67). An excess of bladder cancer was found

FIGURE 2. Temporal trends ΣPFCs in East Greenland polar bears based on 19 year medians from 1984 to 2006 and predictions basedon logarithmic (base e) transformed median concentrations. In addition, a conservative predicted model for the period from 2006 to2070 using the significant log-linear increases calculated for the entire period 1984–2006 (black broken line) and a steeperincreasing prediction including the significant log-linear determination for the periods 1990–2006 (PFOSA) and 2000–2006 (PFOS,PFDA, and PFTrA) (red broken line). In addition experimentally derived PFOS NOAEL and LOAEL for (1) second generation rats (77)and (2) PFOS NOAEL for cynomolgus monkeys (57) are marked on the figure.

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among a production workforce in the PFOS occupationalenvironment (68). Moreover, the U.S. Environmental Protec-tion Agency (EPA) classifies PFOA as a carcinogen in animals(69). Some of the observed effects of perfluorinated com-pounds may be due to alterations in the permeability of cellmembranes, which can have adverse effects in relation to anumber of environmental contaminants. In a fish study ofa coexposure of cells to TCDD (dioxin) and PFOS, thecytochrome P450 1A1 activity induced by TCDD was in-creased (70). The above-mentioned effects and likely inter-action with other endocrine disrupting chemicals includePFCs among chemicals that should be internationallyregulated.

Effect Levels of PFCs. No information is available on effectlevels in Arctic biota, and fairly limited information appearsin the literature from controlled experiments on laboratoryanimals. In a subchronic dietary toxicity study of PFOS,exposed Sprague–Dawley rats decreased serum glucose andserum cholesterol, increased liver weight, and alanin trans-ferase (ALT) activity and displayed hepatocytic hypertrophyand cytoplasmic vacuolization (65). The no-adverse-effectlevel (NOAEL) of PFOS in liver was 358 µg/g in males and 370µg/g in females. Other investigations indicate lower effectlevels. In a two-generation reproductive toxicity study of PFOSin rats, pup survival in the first generation was significantlydecreased in the two highest dose groups, receiving 1.6 and3.2 (mg/kg)/day (71). All first-generation pups in the high-dose group died within 1 day of birth, and close to one-thirdof first generation pups in the 1.6 (mg/kg)/day group diedwithin 4 days of birth. For the second-generation offspring,the NOAEL for reduced pup weight was determined for liverconcentrations of 15 µg/g ww and the LOAEL (lowest-adverse-effect level) at 58 µg/g ww. PFOS concentrations associatedwith the NOAE in a cynomolgus monkey (Macaca fascicularis)study were 59–70 µg/g ww in the liver (51). It is uncertain ifpolar bears tolerate less or more PFOS compared to laboratorymammals, but in Figure 2 we have illustrated the aboveconcentrations relative to the observed and future concen-trations in East Greenland polar bears. If the PFC concentra-tions continue to increase, then the lowest NOAEL and LOAELwill be exceeded in 2014–2024, using the steeper linear trendsidentified for recent years. Using the most conservative lineartrend of the subadult bears, the NOAEL and LOAEL will notbe exceeded before 2035–2067. However, as this investigationhas presented trends for subadult animals, which have lowerPFC concentrations than adults (11), the NOAEL and LOAELwill be exceeded by adults much earlier than calculated herefor adult polar bears.

AcknowledgmentsDanish Cooperation for Environment in the Arctic (DANCEA),The Commission for Scientific Research in Greenland andCanada Research Chairs Program, and the Lundbeck Foun-dation are acknowleged for financial support. Jonas Brønlundgathered the samples through local hunters, and HanneTuborg Sandell and Birger Sandell helped with local contactsto hunters. The laboratory technicians at National Environ-mental Research Institute are acknowledged for conductingthe chemical analysis. Maja Kierkegaard made a majorcontribution to the age determination.

Supporting Information AvailableTable providing annual mean of age, median and range ofthe analyzed PFCs, and the number of polar bear liveranalyses conducted in the present study. This informationis available free of charge via the Internet at http://pubs.acs.org.

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