PLEASE SCROLL DOWN FOR ARTICLE This article was downloaded by: [Aarhus Universitets Biblioteker] On: 14 September 2010 Access details: Access Details: [subscription number 912931718] Publisher Taylor & Francis Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37- 41 Mortimer Street, London W1T 3JH, UK Toxicological & Environmental Chemistry Publication details, including instructions for authors and subscription information: http://www.informaworld.com/smpp/title~content=t713653210 Screening of thyroid gland histology in organohalogen-contaminated glaucous gulls (Larus hyperboreus) from the Norwegian Arctic Christian Sonne a ; Jonathan Verreault b ; Geir W. Gabrielsen c ; Robert J. Letcher d ; Pall S. Leifsson e ; Tine Iburg e a Section for Contaminants, Effects and Marine Mammals,Department of Arctic Environment, National Environmental Research Institute, Aarhus University, DK-4000 Roskilde, Denmark b Département des Sciences Biologiques, Centre deRecherche en Toxicologie de l'Environnement Université du Québec à Montréal, Montréal, Canada c Norwegian Polar Institute, Polar Environmental Centre, NO-9296 Tromsø, Norway d Wildlife and Landscape Science Directorate, Science and Technology Branch, Environment Canada, National Wildlife Research Centre, Carleton University, Ottawa ON, K1A 0H3, Canada e Faculty of Life Sciences, Department of Veterinary Disease Biology, University of Copenhagen, Bülowsvej 17, DK-1870 Frederiksberg, Denmark Online publication date: 13 September 2010 To cite this Article Sonne, Christian , Verreault, Jonathan , Gabrielsen, Geir W. , Letcher, Robert J. , Leifsson, Pall S. and Iburg, Tine(2010) 'Screening of thyroid gland histology in organohalogen-contaminated glaucous gulls (Larus hyperboreus) from the Norwegian Arctic', Toxicological & Environmental Chemistry, 92: 9, 1705 — 1713 To link to this Article: DOI: 10.1080/02772241003611920 URL: http://dx.doi.org/10.1080/02772241003611920 Full terms and conditions of use: http://www.informaworld.com/terms-and-conditions-of-access.pdf This article may be used for research, teaching and private study purposes. Any substantial or systematic reproduction, re-distribution, re-selling, loan or sub-licensing, systematic supply or distribution in any form to anyone is expressly forbidden. The publisher does not give any warranty express or implied or make any representation that the contents will be complete or accurate or up to date. The accuracy of any instructions, formulae and drug doses should be independently verified with primary sources. The publisher shall not be liable for any loss, actions, claims, proceedings, demand or costs or damages whatsoever or howsoever caused arising directly or indirectly in connection with or arising out of the use of this material.
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PLEASE SCROLL DOWN FOR ARTICLE
This article was downloaded by: [Aarhus Universitets Biblioteker]On: 14 September 2010Access details: Access Details: [subscription number 912931718]Publisher Taylor & FrancisInforma Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK
Toxicological & Environmental ChemistryPublication details, including instructions for authors and subscription information:http://www.informaworld.com/smpp/title~content=t713653210
Screening of thyroid gland histology in organohalogen-contaminatedglaucous gulls (Larus hyperboreus) from the Norwegian ArcticChristian Sonnea; Jonathan Verreaultb; Geir W. Gabrielsenc; Robert J. Letcherd; Pall S. Leifssone; TineIburge
a Section for Contaminants, Effects and Marine Mammals,Department of Arctic Environment, NationalEnvironmental Research Institute, Aarhus University, DK-4000 Roskilde, Denmark b Département desSciences Biologiques, Centre deRecherche en Toxicologie de l'Environnement Université du Québec àMontréal, Montréal, Canada c Norwegian Polar Institute, Polar Environmental Centre, NO-9296Tromsø, Norway d Wildlife and Landscape Science Directorate, Science and Technology Branch,Environment Canada, National Wildlife Research Centre, Carleton University, Ottawa ON, K1A 0H3,Canada e Faculty of Life Sciences, Department of Veterinary Disease Biology, University ofCopenhagen, Bülowsvej 17, DK-1870 Frederiksberg, Denmark
Online publication date: 13 September 2010
To cite this Article Sonne, Christian , Verreault, Jonathan , Gabrielsen, Geir W. , Letcher, Robert J. , Leifsson, Pall S. andIburg, Tine(2010) 'Screening of thyroid gland histology in organohalogen-contaminated glaucous gulls (Larushyperboreus) from the Norwegian Arctic', Toxicological & Environmental Chemistry, 92: 9, 1705 — 1713To link to this Article: DOI: 10.1080/02772241003611920URL: http://dx.doi.org/10.1080/02772241003611920
Full terms and conditions of use: http://www.informaworld.com/terms-and-conditions-of-access.pdf
This article may be used for research, teaching and private study purposes. Any substantial orsystematic reproduction, re-distribution, re-selling, loan or sub-licensing, systematic supply ordistribution in any form to anyone is expressly forbidden.
The publisher does not give any warranty express or implied or make any representation that the contentswill be complete or accurate or up to date. The accuracy of any instructions, formulae and drug dosesshould be independently verified with primary sources. The publisher shall not be liable for any loss,actions, claims, proceedings, demand or costs or damages whatsoever or howsoever caused arising directlyor indirectly in connection with or arising out of the use of this material.
Toxicological & Environmental ChemistryVol. 92, No. 9, October 2010, 1705–1713
Screening of thyroid gland histology in organohalogen-contaminated
glaucous gulls (Larus hyperboreus) from the Norwegian Arctic
Christian Sonnea*, Jonathan Verreaultb, Geir W. Gabrielsenc, Robert J. Letcherd,Pall S. Leifssone and Tine Iburge
aSection for Contaminants, Effects and Marine Mammals,Department of ArcticEnvironment, National Environmental Research Institute, Aarhus University,Frederiksborgvej 399, PO Box 358, DK-4000 Roskilde, Denmark; bDepartementdes Sciences Biologiques, Centre deRecherche en Toxicologie de l’EnvironnementUniversite du Quebec a Montreal, Montreal, Canada; cNorwegian Polar Institute,Polar Environmental Centre, NO-9296 Tromsø, Norway; dWildlife and Landscape ScienceDirectorate, Science and Technology Branch, Environment Canada, National WildlifeResearch Centre, Carleton University, Ottawa ON, K1A 0H3, Canada; eFaculty of LifeSciences, Department of Veterinary Disease Biology, University of Copenhagen,Bulowsvej 17, DK-1870 Frederiksberg, Denmark
(Received 25 December 2009; final version received 28 December 2009)
The associations between blood organohalogen contaminant (OHC)concentrations and thyroid gland histology were studied in 10 adultfemale glaucous gulls (Larus hyperboreus) from the Norwegian Arctic(Bjørnøya) during the incubation period. This histological investigationwas undertaken as previous glaucous gull studies from the same areareported negative relationships between circulating OHC concentrationsand thyroid hormone levels. Organohalogen concentrations have pre-viously been associated with altered blood plasma thyroid hormoneconcentrations, as a result of parenchymal thyroid gland alterations andperturbation of the hypothalamic-pituitary-thyroid (HPT)-axis. In thisstudy, PCB (range: 186–1027 ng g�1ww), DDT (77–203 ng g�1ww) andchlordane (18–65 ng g�1ww) concentrations dominated the blood plasmaOHC profile in incubating female glaucous gulls. High density of smallfollicles accompanied by follicular epithelial cell proliferations was seenin thyroid glands in seven of 10 gulls. Focal thyroiditis and nodularhyperplasia were found in two birds. No significant differences in plasmaOHC concentrations were noted between gulls exhibiting high densityof small follicles and cell proliferations and those birds not showinghistological changes. Based on these findings, data suggest that thehistological changes in thyroid glands of OHC-contaminated femaleglaucous gulls may be due to natural variance, although anOHC-induced thyroid stimulating hormone (TSH) perturbation resultingin epithelial cell hyperplasia and increased follicular density cannot be ruledout and remains to be verified. Hence, a large-scale histological study isrequired, in order to elaborate the potential linkage between changesin thyroid gland histology, OHC exposure and regulation of the HPT-axisin the Arctic-breeding glaucous gull.
Glaucous gulls (L. hyperboreus) have been used as bioindicator species of long-rangetransported environmental contaminants and exposure-related biological effectsin the Norwegian Arctic for nearly 35 years (Verreault, Gabrielsen, and Bustnes2010). The glaucous gull was selected as biosentinel species in the Norwegian Arctic(Bjørnøya, Svalbard archipelago) due to (1) widespread distribution, (2) top trophicposition in the marine food web, and (3) elevated tissue and blood concentrationsof organohalogen contaminants (OHC) (Bustnes 2006; Verreault, Gabrielsen, andBustnes 2010). The OHC are of special interest as many of these chemicals arepotential endocrine disrupting substances that induce and/or are implicatedin various adverse endocrine effects on wild birds and mammals, including speciesspanning the Arctic regions (Letcher et al. 2010; Verreault, Gabrielsen, and Bustnes2010). Examples of OHC classes that have been determined at relativelyhigh concentrations in glaucous gulls breeding on Bjørnøya are the persistentand bioaccumulative legacy organochlorines (OC), brominated flame retardantsand perfluorinated alkyl substances (Verreault et al. 2005a, 2005b, 2005c,2007a, 2010).
The potential chemically induced adverse health effects or responses reportedin Arctic species that are chronically exposed to these substances include adverseeffects on hormone, reproductive, immune, and skeletal systems and other internalorgans (Gabrielsen 2007; Letcher et al. 2010; Verreault, Gabrielsen, and Bustnes2010). In glaucous gulls breeding on Bjørnøya, blood plasma T4
(3,5,30,50-tetraiodothyronine or thyroxine) levels were shown to be negativelyassociated with blood concentrations of OHC (mainly OC), while T3, (3,3
0,5-triiodo-L-thyronine or triiodothyronine) was quantitatively, positively associatedwith these OHC (Verreault et al. 2004, 2007b). The mechanisms underlying thispotential OHC-associated perturbation in thyroid hormone homeostasis areunknown. Competitive binding with blood carrier proteins (transthyretin andalbumin) (Ucan-Marın et al. 2009, 2010) and interactions with thehypothalamic-pituitary-thyroid (HPT)-axis were suggested as possible mechanismsresulting in disturbance of circulating T3 and T4 levels. Furthermore, in the samebreeding colonies, it was reported that changes in basal metabolic rateand thermoregulation capacity (heat transfer to eggs), processes controlled largelyby the thyroid hormones, was associated with OHC exposure (Verreault et al.2007b; Verboven et al. 2009). To our knowledge, there has been no reportedinvestigation on the potential impact of OHC exposure on thyroid gland histologyin breeding glaucous gulls from Bjørnøya, or in any other Norwegian Arcticbird species.
Morphological changes in the thyroid gland and their significance inOHC-exposed wildlife are not well understood. In studies of lab rats (Rattusnorvegicus) increase in follicular cell vacuolization and height as well as nuclearvesiculation and decreased colloid area were observed following PCB exposure,and suggested a sustained stimulatory effect on thyroid stimulating hormone (TSH)synthesis and release (Ness et al. 1993). Similarly, other non-specific lesions
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associated with OC exposure in avian species, including cormorants (Phalacrocoraxcarbo), American kestrels (Falco sparverius) and herring gulls (Larus argentatus)were reported (Moccia, Fox, and Britton 1986; Hoffman et al. 1996; McNabb andFox 2003; Saita et al. 2004). These histological alterations are rather non-specificand the clinical significance and link to thyroid hormone disruption is unknown.In order to investigate, whether the OHC concentrations found in glaucous gulls maybe associated with histological changes in the thyroid gland, follicle and epithelial celldensity and plasma OHC concentrations were determined in female gulls duringthe incubation period.
Materials and methods
All incubating female glaucous gulls included in this study were collected fromproximal colonies on Bjørnøya and exposed to similar environmental conditionsduring a 5-day period. The gulls can therefore be viewed as comprising a fairlyhomogenous study group in a wildlife context. Blood samples and thyroid glandswere collected from 10 adult female glaucous gulls breeding in three major coloniesalong the southern coast of Bjørnøya (74�220N, 19�050E) in the Norwegian Arctic(Verreault et al. 2004, 2005a). Briefly, gulls were live-captured post incubationbetween 1 June 2002 and 5 June 2002 using traps consisting of a snare placed on theedge of the nest bowl. Whole blood samples (for OHC analysis) were collected fromthe brachial vein, using heparinized syringes, and centrifuged at 2500� g (JouanBB3V) for 7min to obtain plasma that was stored at �20�C or at lower temperaturesprior to the chemical extraction. The right thyroid glands (for histological analysis)were removed within 10min after euthanasia and preserved in a phosphate-bufferedformaldehyde solution. Chemical analyses included a large suite of OHC compoundsand their metabolic products known or suggested to interfere with thyroid hormonehomeostasis and thyroid gland functioning and morphology. These were includedin order to test for differences between histology groups of high density of smallfollicles and epithelial cell proliferations versus groups of low density and no cellproliferations (Table 1). Chemical analyses of glaucous gull blood plasma sampleshave been comprehensively described in Verreault et al. (2005a).
The thyroid glands were examined grossly after which the tissue was trimmed,processed according to standardized procedures, embedded in paraffin and sectionedat about 4 mm after, which hematoxylin (Al-Haematein)-Eosin (HE) stainingwas applied for routine diagnostics (Lyon et al. 1991; Bancroft and Stevens 1996).The density of small follicles and epithelial cells, which has been associated toOHC exposure in cormorants, was measured according to methods by Saita et al.(2004) with minor modifications. Briefly, the thyroid gland follicular densitywas estimated by counting follicle number in five randomly chosen 200� 200 mmfields at 400� magnification. Likewise, follicular epithelial cell density was estimatedunder 400� magnification by counting the number of follicle cells around 10randomly chosen follicular lumens and expressed as number of cells�mm�2. Birdshaving a thyroid follicle count �50 and follicular epithelial cell density �15�mm�2
were assigned to the group with high density of small follicles and epithelial cellproliferations (Figure 1, Table 1). Kruskal–Wallis tests were applied to test fordifferences in OHC blood plasma concentration between histology groups of highdensity of small follicles and epithelial cell proliferations versus low density and no
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cell proliferations. The level of significance was set at p5 0.05. A SAS statisticalsoftware package V8 and enterprise guide V3.0 (SAS Institute Inc., Cary, NC, USA)was used.
Results
Active follicles with colloid inclusions that were lined with vacuolized high cuboidalepithelium were found in three of in female glaucous gulls (Figure 1). Furthermore,enlarged follicles with inactive follicular flat-cuboidal type epithelium withoutdistinct nucleus and cytoplasm were found in the remaining seven gulls. High densityof small follicles accompanied by follicular epithelial cell proliferation was presentin thyroid glands of seven gulls, while the remaining three gulls had a low densityof small follicles and no epithelial cell proliferations (Figure 2, Table 1). In addition,focal thyroiditis was found in one of these specimens, and was characterizedby mainly mononuclear cells clearly distinguished from the surrounding follicles andepithelial cells (Figure 2). Among the three glaucous gulls that had low density ofsmall thyroid follicles, one bird also exhibited follicular nodular hyperplasia, whichwas clearly demarcated and composed of active follicles containing sparse amountsof colloid and highly vacuolated cells (Figure 2). No marked differences in thedistribution and numbers of C-cells in the ultimobranchial bodies were seen betweenthe individual gulls. Table 1 shows that OHC plasma concentrations were detectedin decreasing in order: �PCB4�DDT4�chlordanes4�toxaphenes4�PCBmetabolites (hydroxylated and methylsulfonyl)4HCB4 dieldrin4�HCH.Concentrations and congener/compound patterns of these OHC in the presentbreeding female glaucous gulls was comprehensively described in Verreault et al.(2005a). Concentrations of OHC classes, except for �DDT (comprised of 96%p,p0-DDE) and toxaphenes, were quantitatively higher in seven glaucous gullsfor which a high density of small follicles and epithelial cell proliferationswas observed.
Figure 1. Left: Normal inactive thyroid tissue from adult female glaucous gull #E collectedat Bear Island 3 June 2002. Note that the thyroid follicles are similar in size and lined with asingle layer of flat inactive epithelium. Right: Normal active thyroid tissue from adult femaleglaucous gull #I collected at Bear Island 5 June 2002. Note that the thyroid folliclesare relatively similar in size and lined with active and high cuboidal epithelium. HE� 100,Bar¼ 175 mm.
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Only few studies have reported OHC-induced morphological changes in thyroid
glands of birds and mammals. Among studies in free-ranging birds, heavily
OHC-contaminated herring gulls from the North American Great Lakes were found
to have decreased thyroid follicular size when compared to a less-contaminatedpopulation (Moccia, Fox, and Britton 1986; McNabb and Fox 2003). These studies
showed that environmental contaminants may influence thyroid gland morphology.
The mechanism(s) underlying this potential chemically induced morphological
alterations is(are) not fully understood, but may be attributed to changes in the
HPT-axis and TSH synthesis and release.In great cormorants, Saita et al. (2004) showed that exposure to several
and non- and mono-ortho coplanary PCB-induced epithelial cell proliferation and
formation of follicles of varying size, when compared with cormorants from a lower
OHC polluted site. These findings are of particular interest since glaucous gulls werefound to accumulate non-ortho PCB (CB-77, -126, and -169) and mono-ortho PCBs
(e.g., CB-81, -105, -118, and -156) with corresponding blood plasma TEQ values
ranging between 3 and 20 ng TEQ g�1 lw (Verreault et al. 2005a). Hoffman et al.
(1996) showed that in ovo CB-126 exposure in American kestrels led to thedevelopment of smaller follicles, which is in agreement with the observed cell
proliferation and follicles of varying size noted in the present glaucous gull thyroid
glands being related to OHC exposure and modulation of the HPT-axis and TSH
dynamics. Similarly, controlled studies of rats, beagle dogs (Canies familiaris)
and Arctic foxes (Vulpes lagopus) established a link between PCB exposure andfollicular cell hyperplasia and thyroid cyst formation (Akoso et al. 1982; Fadden
1994; Sonne et al. 2009). Such histological changes have also been reported
in OHC-contaminated beluga whales (Delphinapterus leucas) from the St. Lawrence
River Estuary (Mikaelian et al. 2003) and polar bears (Ursus maritimus) in EastGreenland (Sonne et al., pers. comm.).
Thyroiditis in vertebrates, as observed in female glaucous gulls in this study, is a
frequent finding as follicular leakage of colloid to the blood stream activates the
P
T
F
D
E
P
P
Figure 2. Left: Proliferation of follicular epithelial cells (P), follicles of varying small size (F)and thyroiditis (T) in adult female glaucous gull #H collected at Bear Island 4 June 2002.Right: Nodular hyperplasia in adult female glaucous gull #J collected at Bear Island 5 June2002. Note the highly active hyperplastic cuboidal epithelium (E) and depleted colloid mass(D). HE� 200, Bar¼ 350mm.
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immune system, which in turn may induce cellular infiltrations (Capen 2007).However, PCBs are also suspected to induce autoimmune responses resultingin thyroiditis and lymphocyte infiltrations and thereby thyroid hormone disorders(Langer 1998). Similarly, prevalence of nodular hyperplasia in vertebrates increaseswith age (Capen 2007), but was also documented in vertebrates exposed to PCB andgoitrogens (Bastomsky 1977; Barsano 1981; Mikaelian et al. 2003). The age effectcould not be determined, since exact ages were not available for the female glaucousgulls in this study. Based on these observations, OHC exposure cannot be ruledout as a potential contributing factor to development of these two specific thyroidlesions in the female glaucous gulls.
The HPT-axis controls the activity of the thyroid glands and OHC-inducedthyroid hormone disruptions is one of the likely co-factors involved in thehistological changes observed in this study (Verreault et al. 2007b). Therefore,a combination of OHC exposure-inducing sustained TSH stimulation beyond thenormal rate of homeostatic processes and age might explain cell proliferation,varying follicular size and even nodular hyperplasia (Ness et al. 1993). In the caseof thyroiditis, this may be due to either colloid leakage or other factors, such asautoimmune mechanisms that may also be linked to PCB exposure (Bastomsky 1977;Barsano 1981; Langer 1998; Mikaelian et al. 2003). In conclusion, the clinicalsignificance of the present findings on the observed thyroid gland changes, as well asthe potential linkage to OHC exposure, is not clear. It is therefore recommendedto perform a larger study of the Bjørnøya glaucous gull thyroid glands in orderto understand the significance of OHC exposure and possible disruption of theHPT-axis in this Arctic avian species.
Acknowledgements
Laboratory technicians (S.G. Chu and W. Gebbink) in the former Letcher Research Labsat the Great Lakes Institute for Environmental Research, University of Windsor (Windsor,Canada) are thanked for their assistance with the chemical analyses. The study was fundedby the Norwegian Pollution Control Authority and the Norwegian Research Council (to J.V.and G.W.G.). Capture and handling of glaucous gulls on Bear Island were approved by theNorwegian Animal Research Authority and the Governor of Svalbard.
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