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A screening of liver, kidney, andthyroid gland morphology inorganochlorine-contaminated glaucousgulls (Larus hyperboreus) from SvalbardChristian Sonne a , Silje A.B. Mæhre b , Kjetil Sagerup b , MikaelHarju c , Eldbjørg Sofie Heimstad c , Pall S. Leifsson d , Rune Dietza & Geir W. Gabrielsen ba Department of Bioscience, Faculty of Science and Technology,Arctic Research Centre (ARC), Aarhus University, Roskilde,Denmarkb Norwegian Polar Institute, Fram Centre, Tromsø, Norwayc NILU (Norwegian Institute for Air Research), Fram Centre,Tromsø, Norwayd Department of Veterinary Disease Biology, Faculty of Healthand Medical Sciences, University of Copenhagen, Frederiksberg,DenmarkAccepted author version posted online: 26 Oct 2012.Version ofrecord first published: 28 Nov 2012.

To cite this article: Christian Sonne , Silje A.B. Mæhre , Kjetil Sagerup , Mikael Harju , EldbjørgSofie Heimstad , Pall S. Leifsson , Rune Dietz & Geir W. Gabrielsen (2013): A screening of liver,kidney, and thyroid gland morphology in organochlorine-contaminated glaucous gulls (Larushyperboreus) from Svalbard, Toxicological & Environmental Chemistry, 95:1, 172-186

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© 2013 Taylor & Francis

Toxicological & Environmental Chemistry, 2013Vol. 95, No. 1, 172–186, http://dx.doi.org/10.1080/02772248.2012.744438

A screening of liver, kidney, and thyroid gland morphology inorganochlorine-contaminated glaucous gulls (Larus hyperboreus)from Svalbard

Christian Sonnea*, Silje A.B. Mæhreb, Kjetil Sagerupb, Mikael Harjuc, EldbjørgSofie Heimstadc, Pall S. Leifssond, Rune Dietza and Geir W. Gabrielsenb

aDepartment of Bioscience, Faculty of Science and Technology, Arctic Research Centre (ARC),Aarhus University, Roskilde, Denmark; bNorwegian Polar Institute, Fram Centre, Tromsø,Norway; cNILU (Norwegian Institute for Air Research), Fram Centre, Tromsø, Norway;dDepartment of Veterinary Disease Biology, Faculty of Health and Medical Sciences, University ofCopenhagen, Frederiksberg, Denmark

(Received 1 September 2012; final version received 24 October 2012)

Concentrations of organochlorine (OC) contaminants and histomorphology ofliver, kidney, and thyroid tissues were studied in nine adult and one subadultglaucous gulls (Larus hyperboreus) collected at Svalbard on 2 August 2011.Concentrations of liver polychlorinated biphenyls (PCB; range: 150–2820 ng g�1

ww), dichlorodiphenyltrichloroethane (DDT; range: 58–724 ng g�1 ww), andchlordanes (CHL; range: 11–126 ng g�1 ww) dominated the OC profile followedby hexachlorobenzene (HCB; range: 11–42 ng g�1 ww), mirex (range: 2–52 ng g�1

ww), and �-hexachlorocyclohexane (�-HCH; range: 1–7 ng g�1 ww). Histologicalexamination of the liver showed mononuclear cell infiltrations and granulomas in10 and 6 gulls, respectively, while intense intrahepatic lipid accumulation(steatosis) was found in two and focal necrosis in one gull. In kidney, glomerularsclerosis and adhesions was found in five and one gull, respectively. Thickening ofthe glomerular basement membranes and tubular necrosis was found in four andseven gulls, respectively, while mononuclear cell infiltrations were found in twoindividuals. In the thyroid gland, a high density of small follicles accompanied byfollicular epithelial cell proliferation was observed in five glaucous gulls. Gullswith hepatic steatosis had significantly higher �DDT levels than the gulls withouthepatic steatosis and a similar trend was found for �PCB. When normalizing OCconcentrations for lipid content in liver, gulls with lipid granulomas hadsignificantly lower �-HCH and significantly higher mirex levels, respectively, thangulls without lipid granulomas. Also; gulls with thickening of the glomerularbasement membranes had non-significantly higher �PCB levels than gullswithout. The histological findings were similar to those of controlled laboratorystudies and OC-contaminated wildlife (e.g., polar bears; Ursus maritimus) and thedata of this study therefore suggest that OC exposure may be a co-factor in thedevelopment of organ alterations in glaucous gulls. However, other environmen-tal factors such as age, element exposure, and infectious micropathogens cannotbe ruled out as co-factors, and it is uncertain if the tissue changes found exertadverse health effects on the population of Svalbard glaucous gulls.

Keywords: hepatic; histopathology; kidney; liver; organochlorine contaminants;polychlorinated biphenyls; renal; thyroid gland

*Corresponding author. Email: csh@dmu.dk

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Toxicological & Environmental Chemistry 173

Introduction

Glaucous gulls (Larus hyperboreus) have been used as a bioindicator species ofenvironmental changes, including long-range transported contaminants and climate

change (Bustnes 2006; Bustnes, Gabrielsen, and Verreault 2010; Letcher et al. 2010;

Verreault, Gabrielsen, and Bustnes 2010). The reason for this is its position as an

Arctic top predator reflecting the food web concentrations of persistent organiccontaminants and potential adverse health effects (Gabrielsen et al. 1995; Letcher et al.

2010; Verreault, Gabrielsen, and Bustnes 2010). The contaminants that are

bioaccumulating to the highest concentrations in the Arctic are the chlorinated,

brominated, and perfluorinated alkyl substances (Letcher et al. 2010). Several studiesshowed that chronic exposure to these groups of anthropogenic chemicals may produce

adverse health effects in Arctic species, including the glaucous gull (Gabrielsen 2007;

Letcher et al. 2010; Verreault, Gabrielsen, and Bustnes 2010). These biological effectsare hormonal disruptions, reproductive and immune suppression, skeletal decalcifica-

tion and organ histopathology, and function among others (Sagerup et al. 2009;

Letcher et al. 2010; Sonne 2010; Sonne, Bustnes, et al. 2010, 2012; Sonne, Dam, et al.

2010; Sonne, Verreault, et al. 2010; Sonne et al. 2011; Sonne, Letcher, et al. 2012;Verreault, Gabrielsen, and Bustnes 2010).

In glaucous gulls breeding on Bjørnøya south of Svalbard, various biomarker health

endpoints such as circulating blood plasma concentrations of thyroid hormones,

vitamin A, progesterone, cortisol and white-blood cells were suppressed by contaminantexposure (Gabrielsen 2007; Letcher et al. 2010; Verreault, Gabrielsen, and Bustnes

2010). The potential adverse health outcome remains unknown; however, combined

with other stressors such as starvation periods and climate change, these perturbations

may induce lower fitness and thereby reduce survival and reproductive outcome(Bustnes, Gabrielsen, and Verreault 2010; Jenssen 2006; Letcher et al. 2010; Sonne

2010; Verreault, Gabrielsen, and Bustnes 2010). The glaucous gulls at Svalbard are

undergoing environmental and physiological changes on a seasonal basis which create

windows of vulnerability during, e.g. the breeding period (Letcher et al. 2010; Sonne2010; Verreault, Gabrielsen, and Bustnes 2010). This species is therefore ideal to study

such effects from multiple stressors including contaminant exposure, starvation, and

infectious diseases. Biomarker endpoints included in such assessments are hormoneconcentrations and ratios, biochemical profiles, and organ histopathology (Letcher

et al. 2010; Sonne, Verreault, et al. 2010; Verreault, Gabrielsen, and Bustnes 2010).

In fact, morphological changes in the thyroid gland of organochlorine (OC)-

contaminated Bjørnøya glaucous were previously investigated (Sonne, Verreault,et al. 2010). This pilot study, which included 10 glaucous gulls, showed a high density

of small follicles accompanied by follicular epithelial cell proliferations as well as focal

thyroiditis and nodular hyperplasia.No studies of multiple organ-systems of the Svalbard glaucous gulls have previously

been undertaken even though OCs are known to have adverse multiple morphological

organ effects in wild birds and mammals (Sonne et al. 2005, 2006, 2011; Letcher et al. 2010;

Sonne 2010; Sonne, Bustnes, et al. 2010, 2012; Sonne, Dam, et al. 2010; Sonne, Verreault,

et al. 2010; Sonne, Letcher, et al. 2012). The aim of this study was to analyze liverOC-concentrations and examine the histomorphology of liver, kidney, and thyroid tissue

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in nine adult male (eight adultsand 1 subadult) and one adult female glaucous gulls fromSvalbard, all collected during late August.

Materials and methods

Study design

The glaucous gulls included in this study were a homogenous study group composed ofnine adults (eight males and one female) and one subadult male collected in Fuglefjella(78�190N, 15�150E) close to Grumantbyen, Isfjorden at Svalbard (Figure 1, Table 1).All birds were euthanized by a shotgun in the post-breeding period, 29 August 2011.Organs were removed in the field within eight hours after death and the subsamples were

Figure 1. Sampling site at Fuglefjella (78�190N, 15�150E) near Grumant City (Grumantbyen),Isfjorden, Svalbard.

C. Sonne

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Toxicological & Environmental Chemistry 175

preserved in the phosphate-buffered formaldehyde solution (for histological examination)and polyethylene plastic bags in �20�C (for chemical analyses). The sampling was inaccordance with the current regulation of the Norwegian Animal Welfare Act andpermission for sampling was given by the Governor of Svalbard (2011/00488-29).

Chemical analyses

Liver tissue was collected for OC analyses summarized in Table 1. The chemical analyseswere made for a wide range of OCs at the NILU laboratory in Tromsø following themethods of Herzke et al. (2009). Briefly, liver samples (2 g) were homogenized with dryNa2SO4, packed into columns and extracted with acetone : cyclohexane (1 : 3,v/v). Analiquot of the extract was evaporated, and the lipid content was determined. The extractwas further cleaned up using gel permeation chromatography for lipid removal. All liverextracts were fractionated using Florisil and the first faction was collected usingdichloromethane : n-hexane (1 : 9,v/v), so that the fraction could contain neutral com-pounds such as polychlorinated biphenyls (PCBs) and OC pesticides. All extracts wereevaporated and transferred to gas chromatography (GC) vials with octachloronaphthaleneadded as recovery standard. The determination of the concentrations of chlordanes,�,�,�-hexachlorocyclohexanes (HCHs), and mirex was performed on an Agilent(Waldorff, Germany) GC/mass spectrometry (MS) operated in a single-ion monitoringmode (SIM) and run in the negative-ion chemical ionization mode (NICI).Hexachlorobenzene (HCB), PCBs, and dichlorodiphenyltrichloroethane (DDT) weremeasured using a GC/MS (Quattro Micro, Waters, Milford, MA, USA) in an electronimpact (EI) mode equipped with a programmable temperature vaporizer (PTV). PCBsdetermined included the following congeners: CB-18, -28, -31, -33, -37, -47/49, -52, -99,-101, -105, -118, -123, -128, -138, -141, -149, -153, -156, -157, -167, -170, -180, -183, -187,-189, and -194 (dixon-like PCBs were not a part of these standard measurements).Quantified OC pesticides included o,p0-DDT, o,p0-DDE and o,p0-DDD, p,p0-DDT,p,p0-DDE and p,p0-DDD, �,�,�-HCH, HCB, heptachlor, oxychlordane, trans-chlordane,

Table 1. Organochlorine concentrations (ng g ww) in liver tissue from 10 adult glaucous gullscollected at Svalbard on 29 August 2011.

IdNo Age group Gender Lipid (%) �26PCBa �-HCH HCB �6CHLb �3DDTc Mirex

GG-11-01 Adult Male 5.6 1544 6.47 40.1 67.8 657 32.1GG-11-02 Adult Female 4.4 858 1.58 17.5 38.1 340 11.5GG-11-03 Adult Male 4.3 150 0.86 11.3 11.0 58.3 3.23GG-11-04 Adult Male 2.9 898 3.58 34.9 54.2 459 14.9GG-11-05 Adult Male 6.2 2820 5.84 38.5 126 724 52.7GG-11-06 Subadult Male 2.4 160 0.77 18.1 16.8 67.6 2.61GG-11-07 Adult Male 3.3 1224 4.66 37.0 46.5 347 35.0GG-11-08 Adult Male 4.3 952 2.36 25.9 49.1 266 16.5GG-11-09 Adult Male 5.4 1995 6.97 42.2 82.8 612 33.0GG-11-10 Adult Male 4.2 1413 7.03 42.0 87.5 518 38.9

Notes: aCB-18, -28, -31, -33, -37, -47/49, -52, -99, -101, -105, -114/122, -118, -123, -128, -138, -141,-149, -153, -156, -157, -167, -170, -180, -183, -187, -189, -194.bHeptachlor, oxychlordane, t-chlordane, c-chlordane, t-nonachlor, c-nonachlor.cp,p0-DDE, p,p0-DDD, and p,p0-DDT.

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cis-chlordane, trans-nonachlor, and cis-nonachlor. All chemical analyses followed inter-national requirements for quality assurance and control (QA/QC), e.g., recommendationsof the Arctic Monitoring and Assessment Program (AMAP 2004). In addition, theNorwegian Institute for Air Research participates in the AMAP ring test program forPersistent Organic Pollutants in human serum. The QA/QC of the sample preparation andanalysis was ensured through the use of mass labeled internal standards for PCBs and OCpesticides. For each batch of 10 liver samples, one standard reference (NIST Whaleblubber 1945) and one blank were prepared. For further information, see Herzke et al.(2009).

Histology

The entire right thyroid gland, a periphery subsample of right liver lobe, and a distalrepresentative section of the right kidney were removed for histological examination andpreserved in a phosphate-buffered formaldehyde solution. In the laboratory, tissues wereexamined grossly and then trimmed, processed according to standardized procedures,embedded in paraffin, and sectioned at about 4 mm. The mounted slides were stained withhematoxylin (Al-Hematein)-eosin (HE) and periodic acid-Schiff (PAS) for routinediagnostics (Lyon et al. 1991; Bancroft and Stevens 1996). Briefly, the presence of fourliver, five renal, and two thyroid gland histological changes were noted as being eitherpresent (yes) or absent (no) since the intensity of changes did not differ among specimens(Table 2). Hepatic lesions were categorized as mononuclear infiltrations (interstitial andgranulomas), focal necrosis, and intrahepatic lipid accumulation (steatosis) while the renalchanges were of either glomerular (sclerosis, adhesions, basement membrane thickening),tubular (necrosis, hyalinization), or interstitial (mononuclear cell infiltrations) nature.

Table 2. Presence of histological changes in 10 glaucous gulls collected at Svalbard on 29 ofAugust 2011.

Liver Kidney Thyroid gland

Idno HCI LG FN STa GS GA GBMTb TNC RCI PTFC DSTF

GG-11-01 Yes Yes No Yes Yes No Yes Yes No – –GG-11-02 Yes Yes No No No No No Yes No Yes YesGG-11-03 Yes Yes No No No No No No Yes Yes YesGG-11-04 Yes Yes No No Yes No No Yes No Yes YesGG-11-05 Yes Yes No Yes Yes Yes Yes Yes No Yes YesGG-11-06 Yes No No No No No No No No – –GG-11-07 Yes No Yes No – – – – – Yes YesGG-11-08 Yes Yes No No Yes No Yes Yes No No NoGG-11-09 Yes No No No Yes No Yes Yes Yes No NoGG-11-10 Yes No No No No No No Yes No No No

Notes: HCI: Hepatic cell infiltrations. LG: Liver granulomas. FN: Focal hepatic necrosis. ST:steatosis. GS: Glomerular sclerosis. GA: Glomerular adhesions. GBMT: Glomerular basementmembrane thickening. TNC: Tubular necrosis and hyalinization. RCI: Renal cell infiltrations.PTFC: Proliferation of thyroid follicular cells. DSTF: Diverging size of thyroid follicles.a�DDT significantly higher in gulls with ST (p¼ 0.04) and a similar trend was found for �PCB(p¼ 0.06).b�PCB non-significantly higher in gulls with GBMT (p¼ 0.07).

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In the thyroid gland two changes were found: proliferation of thyroid follicular cellsand diverging size of thyroid follicles, and the histological examination procedure of theseare described in details elsewhere (Sonne et al. 2005, 2006, 2009, 2011; Sonne, Verreault,et al. 2010).

Statistical analyses

A Kruskal–Wallis test was applied to test for differences in the liver OC-concentration(P

PCB,P

DDT,P

CHL, HCB, mirex, and �-HCH) between individuals with andwithout lesions. In order to remove age and gender effects, the subadult male and adultfemale were both excluded from the analyses (Table 1). SAS statistical software packageV8 and enterprise guide V3.0 (SAS Institute Inc., Cary, NC, USA) was used for statistical

Figure 2. Interstitial cell infiltration (arrow) and granuloma (arrowhead) in the liver of an adultglaucous gull male (#GG-11-01). HE� 50, Bar¼ 50mm.

Figure 3. Massive steatosis (arrows) and necrosis (arrowheads) in liver tissue from an adult glaucousgull male (#GG-11-05). Arrows: macrovesicular lipid vacuole. Arrowheads: karyolysis. HE� 400,Bar¼ 25 mm.

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178 C. Sonne et al.

Figure 4. Glomerular sclerosis (arrow) and adhesions (arrowhead) to Bowman’s capsule in renaltissue from an adult glaucous gull female (#GG-11-02). PAS� 200, bar¼ 50 mm.

Figure 5. Thickening of the capillary basement membrane (arrow) in renal tissue from an adultglaucous gull male (#GG-11-09). PAS� 400, Bar¼ 25mm.

Figure 6. Hyalinization of tubular basement membrane (arrow) and acute tubular necrosis(arrowhead) in renal tissue from an adult glaucous gull male (#GG-11-09). PAS� 100, bar¼ 50mm.

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analyses and the level of significance was set to p� 0.05 while 0.055 p5 0.1 wasconsidered a trend.

Results

Lesions

Liver lesions

Histomorphological changes were found in the liver tissue of all individuals and thefrequencies of the lesions showed a high degree of variance (Table 2). The lesions weredivided into interstitial changes (mostly lymphocyte accumulations) and parenchymalhepatocytic lesions such as necrosis and steatosis macro vesicular lipid accumulations.Of interstitial changes, mononuclear lymphocyte infiltrates and granulomas (Figure 2)were found in 60–100% of the individuals accompanied by focal necrosis in a single gull. Itwas seen that the cell infiltrates only affected the incorporated hepatocytes while thenecrosis was of mild unifocal nature. Of parenchymal lesions, two gulls showed intensesteatosis increasing toward the periacinar zone 3 (Figure 3). No portal changes such aslymphohistiocytic infiltrations, bile duct proliferations, or fibrosis were found. It was notpossible to recognize the hypertrophic Ito-cells usually found in Arctic marine species.

Renal lesions

Chronic renal lesions were found in all individuals except the subadult male (#GG-11-06)who in general exhibited fewer organ lesions (Table 2). The renal lesions were categorizedbased on glomerular, tubular, and interstitial origin. Glomerular lesions were sclerosis,adhesions to Bowman’s capsule, and thickening of the capillary basement membrane(similar to membranous glomerulonephritis) (Figures 4 and 5). This was of multifocalnature and found in one–five of the gulls. Two types of renal tubular lesions were found inseven of the gulls (Table 2). These included PAS-positive hyalinization of the tubularbasement membrane and acute tubular necrosis (Figure 6). These two changes alwaysoccurred together and a single case (#GG-11-09) exhibited massive necrosis withproteinaceous (hyaline) secretion. No hyaline casts in the distal tubules or collectionducts were found. Interstitial mononuclear lymphocyte infiltrations were found in two ofthe gulls (Table 2). The infiltrates were demarcated similar to a granuloma and did notseem to affect the surrounding tubules or glomeruli (Table 2).

Thyroid gland lesions

In the thyroid gland, high density of small follicles accompanied by follicular epithelial cellproliferation was found in five gulls while the remaining three gulls had a low density ofsmall follicles and no epithelial cell proliferations (Figure 7, Table 2). No difference in thedistribution and the number of C-cells in the ultimobranchial bodies were seen between theindividual gulls.

Lesions versus OC concentrations

The chemical analyses of OCs included 26 PCB congeners, six chlordanes, three DDTcompounds, HCB, mirex, and �-HCH with the liver concentrations decreasing in theorder: �PCB (dominated by CB-153, -138, and -180)4�DDT (dominated by p,p0-

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180 C. Sonne et al.

DDE)4�chlordanes (dominated by oxychlordane)4HCB4mirex4�-HCH (Table 1).According to Table 1, OC-concentrations in the subadult male (#GG-11-06) and adultfemale (#GG-11-02) seemed to be among the lowest probably due to young age andreproductive status, respectively. Therefore, these two individuals were excluded from thestatistical analyses testing OC-concentrations in gulls with and without histologicalchanges. The analyses showed that the two gulls with hepatic steatosis had significantlyhigher �DDT levels than the six gulls without hepatic steatosis and a similar trend wasfound for �PCB (Table 1). When normalizing OC concentrations for lipid content in liver,gulls with lipid granulomas had significantly lower �-HCH and significantly higher mirexlevels, respectively, than gulls without lipid granulomas. Similarly, the four gulls withthickening of the glomerular basement membranes had non-significantly higher levels of�PCB than the three without.

Discussion

During August, the post-breeding gulls gain weight after being through a stressful periodof breeding and starvation (Gabrielsen 2009; Letcher et al. 2010; Verreault, Gabrielsen,and Bustnes 2010). In this study, OC concentrations were similar to those reported fromearlier investigations of glaucous gulls in the Norwegian Arctic (Gabrielsen 2007; Letcheret al. 2010; Sonne, Verreault, et al. 2010; Verreault, Gabrielsen, and Bustnes 2010). Whencompared to toxic threshold levels for �PCB in aviary species, the concentrations inglaucous gulls were in the range that exceeds those of toxicity on neuroendocrine,reproductive and immune systems for non-dioxin-like PCBs (350–11,000 ng g�1 ww)(AMAP 2004). Biological effects are therefore presumed to occur in Svalbard glaucousgulls (Gabrielsen 2007; Letcher et al. 2010; Verreault, Gabrielsen, and Bustnes 2010).

Liver

There are only a few studies reporting on OC-exposure and hepatic histopathology inavian species (Fabczak et al. 2000) and therefore information from mammals has been

Figure 7. Proliferation of thyroid follicular cells (arrow) and the diverging size of thyroid follicles(arrowhead) in an adult glaucous gull male (#GG-11-07). HE� 100, Bar¼ 50mm.

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used for interpretation in the following sections. The hepatic interstitial cell infiltrationsand the single case of necrosis found in this study were non-specific inflammatoryreactions toward micro-pathogens (e.g., bacteria) and/or injury of local blood vessels fromtoxic compounds such as environmental contaminants (Kelly 1993; MacLachlan andCullen 1995). The zonal steatosis is ascribed to hyperphagia, fasting, decreased synthesis oflipoproteins (reduced liver function), or a result of exposure to toxic substances such aspersistent organic pollutants and mercury (Leighton et al. 1988; Kelly 1993; MacLachlanand Cullen 1995; Sagerup et al. 2009; Wayland et al. 2010). Hoffman et al. (1996) showedthat nestling of American kestrels (Falco sparverius) exposed to CB-126 led to mildcoagulative necrosis and increased oxidative stress. Despite CB-126 being a dioxin-likePCB, this indicate PCBs being a co-factor in the liver changes found in the Svalbardglaucous gulls.

The zonal pattern is characteristic during periacinar damage from low oxygen gradientwhich sensitize liver parenchyma to metabolic disorders, subsequently resulting in lipidaccumulation (Kelly 1993; MacLachlan and Cullen 1995). Therefore, the lesions found inthis study indicate exposure to OCs, elements, and/or micropathogens. This is supportedby other studies of both OC-exposed wildlife such as polar bears (Ursus maritimus), pilotwhales (Globicephala melas), and ringed seals (Phoca hispida) as well as controlledexperiments on rats (Rattus rattus), sledge dogs (Canis familiaris) and Arctic foxes (Alopexlagopus) reporting similar lesions as those found in the present glaucous gulls (Kimbrough,Gaines, and Linder 1971; Bruckner, Khanna, and Cornish 1974; Jonsson et al. 1981;Bergman et al. 1992; Chu et al. 1998; Sonne et al. 2005, 2006, 2011; Klaassen, Amdur, andDoull 2007; Sonne, Leifsson, Dietz, et al. 2008; Sonne, Leifsson, Wolkers, et al. 2008;Sonne, Verreault, et al. 2010). Furthermore, the statistical relationships betweencontaminants and steatosis/lipid granulomas supported OCs as co-factor in the develop-ment of glaucous gulls liver lesions.

Kidney

No avian studies reported on the relationships between OC-exposure and specific renallesions in avian species. The renal lesions in this study were all of chronic and non-specificnature and similar to those reported in the studies of terrestrial (sledge dogs and Arcticfoxes) and marine mammals (polar bears, pilot whales, and ringed seals) as well as humans(Maxie 1993; Cotran, Kumar, and Collins 1999; Bergman, Bergstrand, and Bignert 2001;Woshner et al. 2002; Sonne et al. 2005, 2006, 2007; Sonne, Leifsson, Wolkers, et al. 2008;Sonne, Dam, et al. 2010). Thickening of glomerular capillary walls are often incorpora-tions of immune-complex deposits at the epithelial side of the glomerular capillarybasement membrane due to immune challenges from micro-pathogen infections(Maxie 1993; Cotran, Kumar, and Collins 1999). Glomerular sclerosis was not exacerbatedby interstitial fibrosis in the present glaucous gulls despite the usual case (Maxie 1993;Churg, Bernstein, and Glassock 1995; Confer and Panciera 1995; Cotran, Kumar, andCollins 1999; Bergman, Bergstrand, and Bignert 2001; Woshner et al. 2002; Sonne et al.2006). Interstitial nephritis (mononuclear cell infiltrations) was only found in two glaucousgulls. The reason for that is unknown and may be ascribed to small sample size. Higherprevalence was found in ringed seals, bowhead whales, pilot whales, bottlenose dolphins(Tursiops aduncus), and polar bears probably due to other OC/element patterns andconcentrations, exposure to micro pathogens, and thereby incidences of chronic recurrentinfections (Bergman, Bergstrand, and Bignert 2001; Sonne-Hansen et al. 2002;

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Woshner et al. 2002; Sonne et al. 2005, 2006; Rosa et al. 2008; Lavery et al. 2009; Sonne,Dam, et al. 2010). Of environmental co-factors affecting renal histomorphology, there aremercury, cadmium, micro pathogens such as parasites, bacteria, fungi, and viruses that areall known to induce renal histopathological changes (Maxie 1993; Confer and Panciera1995; Cotran, Kumar, and Collins 1999). In addition to these, environmental OCcontaminants in similar concentrations were shown to be co-factors in previous studies ofrenal histopathology. The histopathological lesions found in glomeruli, tubules, andinterstitium were similar to those reported in polar bears, sledge dogs, Arctic foxes, ringedseals, bottlenose dolphins, pilot whales, and bowhead whales heavily contaminated withOCs (Bergman, Bergstrand, and Bignert 2001; Sonne et al. 2006, 2007, 2009; Rosa et al.2008; Sonne, Leifsson, Wolkers, et al. 2008; Lavery et al. 2009; Sonne, Dam, et al. 2010).The statistical relationship between thickening of the glomerular basement membranesand �PCB also supports this finding.

Thyroid gland

Only few studies reported on OC-induced morphological changes in thyroid glands ofbirds and mammals. Among studies of wild avian species exposed to OCs, herring gulls(Larus argentatus) from the North American Great Lakes and great cormorants(Phalacrocorax carbo) from Tokyo Bay had decreased thyroid follicular size and epithelialcell proliferation (Moccia, Fox, and Britton 1986; McNabb and Fox 2003; Saita et al.2004). These studies showed that environmental contaminants may influence thyroid glandmorphology while the mechanism behind the morphological changes is not fullyunderstood, but changes in the hypothalamic-pituitary-thyroid (HPT) axis of thyroid-stimulating hormone (TSH) synthesis and release is probably involved. Hoffman et al.(1996) showed that nestling of American kestrels (Falco sparverius) exposed to CB-126 ledto the development of smaller follicles. Similar controlled studies of rats, domestig dog(beagle breed), and Arctic foxes have established a link between PCB exposure andfollicular cell hyperplasia and thyroid cyst formation (Akoso et al. 1982; Fadden 1994;Sonne et al. 2009) similar to studies of OC-contaminated St. Lawrence beluga whales(Delphinapterus leucas) and East Greenland polar bears (Mikaelian et al. 2003; Sonne2010; Sonne et al. 2011). These studies support that cell proliferations and follicles ofvarying size observed in the present glaucous gull thyroid glands may be related to OCexposure. The mechanism could likely be sustained TSH stimulation beyond the normalrate of homeostatic processes while age could explain the cell proliferations and varyingfollicular size despite infections and autoimmune reactions cannot be ruled out asco-factors (Ness et al. 1993; Sonne 2010; Sonne, Verreault, et al. 2010; Sonne et al. 2011).

Considerations

It is not possible to estimate the potential clinical significance of the presenthistomorphological changes observed in glaucous gulls. The lesions observed are ingeneral not comparable to, e.g., chick-edema disease which is known to be lethal andprobably affecting reproductive outcome in, e.g., PCB-contaminated Great Lake seabirds(Gilbertson et al. 1991). It is therefore recommended to perform a more extensive study oforgan histopathology and health in a larger number (30 to 50þ) of glaucous gulls from theNorwegian Arctic or East Greenland in order to attain a better understanding of the

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significance of OC exposure and possible health effects. In addition, other co-factors suchas heavy metals and infectios diseases would be relevant to include.

Conclusion

Of the OC contaminants determined in liver tissue from 10 glaucous gulls from Svalbard,concentrations of PCBs dominated the profile followed by DDTs, chlordanes, HCB,mirex, and �-HCH, respectively. The concentrations were within the toxic threshold forchronic exposure and this was supported by histological examination showing chroniclesions in liver, kidneys, and thyroid glands. Due to this and the statistical relationshipbetween contaminant concentrations and the presence of lesions, despite limited; it issuggested that OC exposure may be a co-factor in the development of the histologicalchanges. It is uncertain if the present lesions exert adverse health effects on the populationof Svalbard glaucous gulls.

Acknowledgments

The study was funded by the Norwegian Polar Institute and the Norwegian Research Council(Arctic Field Grant). Capture and handling of glaucous gulls were in accordance to the NorwegianAnimal Welfare Act and approved the Governor of Svalbard (2011/00488-29).

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