Two decades of biomonitoring polar bear health in Greenland: a review
© Sonne et al; licensee BioMed Central Ltd. 2012
Published: 24 February 2012
We present an overview of studies of anthropogenic pollutants in East Greenland polar bears over the period of 1999-2011. East Greenland polar bears are among the most polluted species, not just in the Arctic but globally, and represent an excellent biomonitoring species for levels and effects of global pollution in an apex predator. Therefore, an international multidisciplinary team joined to monitor and assess the patterns and concentrations of contaminants and their potential negative impact on polar bears. The review showed that East Greenland polar bears are exposed to a mix of chlorinated, brominated and fluorinated organic compounds as well as mercury which are all known to have endocrine, immune and organ-system toxic properties. For example, the concentrations of PCBs (polychlorinated biphenyls) in blubber ranged approximately 800-21,000 ng/g lw while mercury concentrations in liver and kidney ranged 0.1-50 μg/g ww. Regarding health endpoints, bone density seemed to decrease as a function of time and OHC (organohalogen compound) concentrations and further T-score for adult males indicated risk for osteoporosis. .The size of sexual organs decreased with increasing OHC concentrations. In the lower brain stem, mercury-associated decreases in NMDA-receptor levels and DNA-methylation was found The present review indicated that age was one of the major drivers for liver and renal lesions, although contaminants and infectious diseases may also play a role. Lesions in thyroid glands were most likely a result of infectious and genetic factors and probably, together with endocrine disrupting chemical (EDCs), the reason for disturbances/fluctuations in blood plasma thyroid hormone concentrations. Except for bone density reductions and neurological measures, all findings were supported by case-control studies of Greenland sledge dogs exposed long-term orally to similar combinations of contaminant concentrations. The studies of sledge dogs also indicated that the mixture of contaminants and fatty acids in the blubber of prey similar to that of polar bears induces cellular as well as humoral immune toxic changes. These controlled studies using model species for polar bears indicate that the correlative findings between health endpoint and contaminants in polar bears could be a cause-and-effect relationship. Physiologically based pharmacokinetic (PBPK) modelling showed that the risk quotients were ≥1 for ΣPCB, dieldrin and PFOS, which indicate an increased risk of prenatally reproductive pathology. In conclusion polar bears are susceptible to long-range transported chemicals that may have various adverse effects on multiple organ systems such as the reproductive and immune system.
The use of East Greenland polar bears (Ursus maritimus) as a biomonitoring key species for measuring exposure to OHCs (organohalogen compounds) and Hg (mercury) was initiated in Scoresby Sound in 1983 and is now the most comprehensive time trend studies of pollution on this species [1–7]. In addition, museum samples of skin and skulls collected since year 1892 have been included for Hg analysis and various patho-morphological and toxico-pathological density analyses [4, 6–11].
The studies of adverse health effects of pollution were started in 1999 by the implementation of a biomonitoring health programme via AMAP (Arctic Monitoring and Assessment Programme) [12–14]. The reason for choosing polar bears, and for upgrading the research intensity, was because the East Greenland polar bear subpopulation is one of the most contaminated and that local Inuit people rely on this species as a food resource in addition to ringed seal (Phoca hispida) that plays a much greater role. Because polar bears reflect temporal trends and biological effects of contaminants they may also serve as a proxy for human health exposure and possible effects despite the fact that the physiology, metabolism, food and way of life of these two species differ fundamentally [e.g. [5, 7, 13–15]].
We present an overview of contaminant concentrations and potential adverse health effects from anthropogenic contaminants in polar bears during the period 1999-2010. The health effects include decrease in bone density, morphological changes in sexual organs, liver, kidney and thyroid glands, as well as potential neurological alterations and impacts on the immune and endocrine systems. Finally, some speculations about the synergistic effects of environmental stressors (e.g. decrease in sea ice) on polar bear health are presented.
Levels of contaminants
Concentrations of various contaminants [Mean (Min-Max, n] divided on tissues in East Greenland polar bears sampled 1999-2002. All data are in ng/g lw except for nPCBs, PCDDs and PCDFs (pg/g lw), PFCs (ng/g ww) and mercury (µg/g ww). Reworked from Sonne (2010).
Subcutaneous adipose tissue
6,543 (897-20,407, 92)
28,409 (12,836-67,664, 20)
102 (2.4-785, 92)
194 (13-818, 92)
204 (26-866, 92)
1,414 (243-7,465, 92)
436 (73-1,580, 92)
70 (22-192, 92)
241 (125-442, 5)
124 (114-148, 5)
10 (7-12, 5)
20 (8-38, 5)
4 (3-5, 5)
14 (10-18, 5)
11 (1-36, 59)
14 (1-50, 57)
0.4 (0.1-0.9, 82)
According to Dietz et al. [3–5, 7] the concentrations of legacy chlorinated contaminants (PCBs and OC pesticides) have decreased and stabilized since 1990, while newer contaminants like PFCs and contemporary threats like Hg have increased. So, despite international regulations on all these groups of contaminants they persist and biomagnify in the environment, which results in a cocktail of toxic chemicals in the tissues of East Greenland polar bears.
Analyses on the skeletal system have exclusively focused on skulls. The reasons for this are because Natural History Museums have archived these since 1892 and because skulls are relatively easily obtained in connection with the subsistence hunt.
Studying impacts from OHCs optimally includes investigation of the reproductive tract as adverse effects on this organ-system have a direct impact on the population size .
Liver, kidneys and thyroid glands
Other key organs that are susceptible to endocrine disruption are the liver, kidneys, and various endocrine organs such and the thyroid glands and adrenals [13, 14]. Liver (n=79), renal (n=75) and thyroid glands (n=20) were analyzed histologically in bears sampled 1999-2002. The evaluation, when not having a control group, is very difficult not least due to the effects from age and infectious diseases [14, 24–28]. However, the various pathologies found in liver parenchyma and renal glomeruli, tubules and interstitium were similar to those found in controlled studies of Hg and OHCs in laboratory mammals and other OHC exposed wildlife [14, 24–27]. The overall most important parameters determining liver and renal pathology was age while also some statistical relationships were found between pathology and different chlorinated and brominated groups of contaminants as well as the liver and renal toxic Hg concentrations.
No histological lesions were found in any of the 50 adrenals examined while pathology was found in 8 out of 20 examined thyroid glands . None of the thyroid gland lesions including c-cell hyperplasia, interstitial fibrosis, and nodular hyperplasia were associated with age or gender, so environmental factors such as energetic stress and autoimmunity/genetic could be co-factors as well as OHCs. Such lesions may interfere with the hypothalamic–pituitary–thyroid (HPT) axis leading to endocrine disruptions having an impact on fecundity and foetal and neonatal development in East Greenland polar bears.
Villanger et al.  analyzed the circulating full blood concentrations of TT3 and TT4 in 62 East Greenland polar bears. The reason for analyzing thyroid hormones is the fact that this endocrine system is known to be extremely susceptible to EDC exposure including biotransformed metabolites such as OH-PCBs [13, 14, 33]. The analyses showed that various biological parameters such as age, size, and condition affected the circulating concentrations while different organochlorine contaminants and bromated flame retardants had negative as well as positive effects on the concentrations of both TT3 and TT4. The conclusions were that these correlations indicate biological effects on the HPT axis from EDC exposure, which is also supported by various in vivo studies of laboratory mammals as well as in vitro studies of polar bears [13, 14, 33].
Very little has been published on the East Greenland polar bear immune system [13, 14, 34]. However, investigations on Svalbard bears have indicated immune toxic effects at OHC exposure concentrations similar to the East Greenland polar bear’s [13, 14, 35, 36] and multiple studies in the laboratory and field show similar biological effects [13, 14, 37–39].
East Greenland polar bears are among the most contaminated species on our globe in spite of their remote Arctic habitat. This sub-population inhabits Arctic biotopes being constantly under pressure from global warming and associated environmental changes. Anthropogenic environmental contaminants seem to be a co-factor in various organ-system lesions in East Greenland polar bears. This includes reduced bone density and sexual and reproductive organ size, thereby having potential impacts on individual health and population maintenance. On top of this, also global warming seems to affect polar bears via negative energy balances, which may have consequences for fecundity and immune resistance. The main challenge in the future is to integrate the cumulative impact from these multiple stressors across temporal and spatial gradients by integrating empirical data and laboratory studies.
The Lundbeck Foundation, Danish Cooperation for Environment in the Arctic (Dancea), The Commission for Scientific Research in Greenland (KVUG) and The Prince Albert II Foundation are acknowledged for financial support. Jonas Brønlund organized the sampling in East Greenland with invaluable help from the local hunters. No conflicts of interest were reported.
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