Organochlorine-induced histopathology in kidney and liver tissue from Arctic fox (Vulpes lagopus)
Introduction
The Arctic is exposed to a wide variety of persistent organic pollutants, such as polychlorinated biphenyls (PCB) and organochlorine pesticides (OCP). These compounds are considered particularly harmful due to their persistence and bioaccumulation in the food chain. Therefore, Arctic top predators such as polar bears (Ursus maritimus), arctic fox (Vulpes lagopus), sledge dogs (Canis familiaris), killer whales (Orcinus orca) and humans (Homo sapiens) are exposed to the highest levels, and health effects at the immune, endocrine and reproductive level are therefore most likely to occur in these species (AMAP, 2004).
The arctic fox has a circumpolar distribution and the habitat is the Arctic tundra and pack ice (Macpherson, 1969, Wrigley and Hatch, 1976). Based on feeding ecology, they can be divided into two different ecotypes, such as “inland” (mainly living on lemmings) and “coastal” (feeding on birds and marine mammals) foxes (Braestrup, 1941). Such differences in habitat and feeding ecology seems to result in differences in tissue concentrations of PCBs/OCPs where coastal arctic foxes in Svalbard have higher levels compared to the inland arctic foxes from Canada and Alaska (Hoekstra et al., 2003, Fuglei et al., 2007). Arctic foxes living in Svalbard have a more marine diet and feed higher in the food chain compared to foxes in Canada and Alaska (Hoekstra et al., 2003, Fuglei et al., 2007). For coastal foxes at Svalbard, the food availability becomes limited during autumn and winter when they rely on carcasses of reindeer (Rangifer tarandus platyrhynchus), seals, Svalbard rock ptarmigan (Lagopus muta hyperborean) and food stored during spring and summer (Frafjord, 1993, Prestrud, 1992). To some extent, the arctic foxes follow the polar bears to feed on killed seal remains (Hiruki and Stirling, 1989). Finally the arctic fox are capable of killing and eating seal spp. (Phocidae) pups (Roth, 2002).
Studies of tissue concentrations of PCBs (polychlorinated biphenyls) in arctic foxes at Svalbard have shown consistently high levels (Norheim, 1978, Wang-Andersen et al., 1993, Severinsen and Skaare, 1997, AMAP, 2004, Fuglei et al., 2007). PBDEs (polybrominated diphenyl ethers) are also detected in arctic foxes from Svalbard, but in significantly lower levels and with a somewhat different metabolism and excretion of BDE congeners compared to other top predators (Fuglei et al., 2007, Wolkers et al., 2004, Muir et al., 2006). The PCB levels in arctic foxes from Svalbard are up to 40% higher than those found in male polar bears from Svalbard (AMAP, 2004, Bernhoft et al., 1997, Fuglei et al., 2007, Norheim, 1978, Severinsen and Skaare, 1997, Wang-Andersen et al., 1993). The PCB congener pattern found in arctic foxes is similar to that found in polar bears, suggesting a similar metabolism and possible effects on vital functions such as reproduction, immunity (disease resistance) and endocrine homeostasis (AMAP, 2004, Fuglei et al., 2007, Norheim, 1978, Wang-Andersen et al., 1993). Besides the endocrine and immune systems, also internal organs might be directly affected. In rats (Rattus norwegicus) and mink (Mustela vision), PCBs exposure has been associated with renal lesions and hepatotoxicity (e.g. Bergman et al., 1992, Bruckner et al., 1974, Chu et al., 1994, Jonsson et al., 1981, Kelly, 1993, Kimbrough et al., 1971, McCormack et al., 1978, Wade et al., 2002). In wildlife species such as polar bears (Sonne et al., 2005, Sonne et al., 2006a, Sonne et al., in press-a) and ringed seals (Phoca hispida) (Bergman et al., 2001) as well as sledge dogs (Sonne et al., 2007a, Sonne et al., in press-b, Sonne et al., 2008) PCB/OCPs exposure has been linked to liver and renal lesions.
Adaptations to Arctic conditions make animals particularly sensitive to the effects of PCB/OCPs. For example, to cope with high variations in food availability, animals build up large fat reserves when food is available, and utilize these reserves when food intake is limited. Hence, Arctic animals display marked seasonal cycles of “fattening” and emaciation. The deposition of lipophilic contaminants occurs mainly in these adipose tissues. However, when lipids are mobilized to meet energy demands, accumulated PCB/OCPs become bioavailable and may reach sensitive tissues like liver and kidney. Conclusions on previously conducted studies of negative health effects from PCB/OCPs in Arctic top predators have typically been based on correlations between the effect parameters and individual PCB/OCP levels (e.g. Braathen et al., 2004, Haave et al., 2003, Skaare et al., 2001, Sonne et al., 2004, Sonne et al., 2006b). Cause-effect relationships are difficult to establish in such wildlife studies and long-term contamination experiments under controlled conditions in the lab has therefore been warranted. Hence, the present study was undertaken, in which the impact from PCB/OCPs on liver and kidney morphology were investigated in farmed arctic fox fed for almost 2 years a diet containing “naturally” contaminated minke whale (Balaenoptera acutorostrata) blubber.
Section snippets
Animals and housing
The experimental animals were farmed arctic foxes of the blue colour type. Blue fox farming in Norway started about 90 years ago with wild arctic foxes caught in Greenland, Alaska, Iceland and Svalbard. The farmed foxes have similar yearly cycles in body fatness as the wild foxes and are therefore a good model for feral arctic foxes. During captivity, they have been bred for larger body weight to increase skin size. The experimental animals from which histopathology is reported in the present
Results
It should be noted that we – due to field logistics – did not have the opportunity to measure clinical-chemical blood and urine parameters. However, we measured liver and renal weights and the average of these is given in Table 3. The weights were all highest in the exposed group – most pronounced in the liver – although not statistically significantly (both p > 0.05). Furthermore, levels of PCBs and chlorinated pesticides was significantly highest in the minke whale blubber given the exposed
Discussion
Since the foxes were of very similar genetics (breed and brother-pairs), had the same age and body condition, received feed of the same composition, and had the same energy intake, the present study design allowed us to eliminate important confounding factors which may otherwise have impacted the histological parameters. However, the lipid classes in the feed differed between the control and the exposed group, as did some of the metal and vitamin concentrations. We can therefore not eliminate
Conclusions
Foxes fed contaminated whale blubber exhibited a significantly larger prevalence of renal lesions than foxes fed pork fat diet and similar indications were found for liver lesions. The current experiment were conducted in an ecologically realistic manner, both with regard to contaminant duration and dose, and the results are in agreement with earlier reports on wild polar bears, seal species and sledge dogs chronically exposed to environmental cocktail of similar PCB/OCP levels. The most severe
Conflict of interest – full disclosure
No conflicts of interest were reported.
Acknowledgements
We thank the staff at Ås for proper care of the foxes and Karoline Sivertsen and Ingeborg G. Hallanger for laboratory assistance. The Norwegian Research Council (Project No. 153484/S30) and the Lundbeck Foundation are acknowledged for funding of the study.
References (59)
- et al.
Organochlorines in polar bears (Ursus maritimus) at Svalbard
Environ. Pollut.
(1997) - et al.
Polychlorinated biphenyl-induced alteration of biologic parameters in the rat
Toxicol. Appl. Pharmacol.
(1974) - et al.
Subchronic toxicity of 3,3′,4,4′,5-pentachlorobiphenyl in the rat. 1. Clinical, biochemical, haematological, and histopathological changes
Fund. Appl. Toxicol.
(1994) - et al.
Organochlorine contaminant and stable isotope profiles in Arctic fox (Alopex lagopus) from the Alaskan and Canadian Arctic
Environ. Pollut.
(2003) - et al.
Effect of polychlorinated biphenyls and polychlorinated quaterphenyls in cynomolgus monkey (Macaca fascicularis)
Toxicology
(1982) The liver and biliary system
- et al.
Preliminary results of fasting on kinetics of organochlorines in polar bears (Ursus maritimus)
Sci. Total Environ.
(1995) - et al.
Greenland sledge dogs (Canis familiaris) exhibit liver lesions when exposed to low-dose dietary organohalogen contaminated minke whale (Balaenoptera acutorostrata) blubber
Environ. Res.
(2008) - et al.
Cadmium toxicity to ringed seals (Phoca hispida) – an epidemiological study of possible cadmium induced nephropathy and osteodystrophy in ringed seals (Phoca hispida) from Qaanaaq in Northwest Greenland
Sci. Total Environ.
(2002) - et al.
Substrate oxidation in male blue foxes (Alopex lagopus) during feeding, fasting realimentation
J. Nutr.
(2002)
Levels and congener pattern of PCBs in arctic fox (Alopex lagopus) in Svalbard
Environ. Pollut.
Congener specific PCB and polychlorinated camphene (toxaphene) levels in Svalbard ringed seals (Phoca hispida) in relation to sex, age, condition and cytochrome P450 enzyme activity
Sci. Total Environ.
Theory and Practice of Histological Techniques
Influence of commercial polychlorinated biphenyls and fractions there of on liver histology in female mink (Mustela vison)
Ambio
Renal lesions in Baltic grey seals (Halichoerus grypus) and ringed seals (Phoca hispida botnica)
Ambio
Differential toxicity of 2,3,7,8-tetrachloridibenzo-p-dioxin TCDD in C57BL-6J mice congenic at the AH locus
Fund. Appl. Toxicol.
Relationships between PCBs and thyroid hormones and retinol in female and male polar bears
Environ. Health Perspect.
A study of the arctic fox in Greenland Immigrations, fluctuations in numbers based mainly on trading statistics
Medd. Grønl Biosci.
Renal disease
Thomsons Special Veterinary Pathology
Robbins Pathologic Basis of Disease
Food habits of arctic foxes (Alopex lagopus) on the western coast of Svalbard
Arctic
Environmental contaminants in arctic foxes (Alopex lagopus) in Svalbard: relationships with feeding ecology and body condition
Environ. Pollut.
Polychlorinated biphenyls and reproductive hormones in female polar bears at Svalbard
Environ. Health Perspect.
Population dynamics of the arctic fox (Alopex lagopus), on Banks Island, Northwest Territories
Can. Field Nat.
Effects of prolonged exposure to dietary DDT and PCB on rat liver morphology
Arch. Environm. Contam. Toxicol.
The ultrastructure of livers of rats fed DDT and dieldrin
Arch. Environ. Health
Cited by (52)
Toxic ties: Unraveling the complex relationship between endocrine disrupting chemicals and chronic kidney disease
2023, Environmental PollutionA risk assessment review of mercury exposure in Arctic marine and terrestrial mammals
2022, Science of the Total EnvironmentCitation Excerpt :The lack of effect studies has previously been concluded and further investigations recommended (e.g. AMAP/UN Environment, 2019, Dietz et al., 2019b, 2020). The closest recent example was POP effect studies using minke whale (Balaenoptera acutorostrata) blubber to expose sledge dogs (Canis familiaris) and Arctic fox (Alopex lagopus) as sentinels for the polar bear, which are better that seal data, but unfortunately this was never carried out with a focus on Hg (e.g. Bradley et al., 2018; Kirkegaard et al., 2010a, 2010b, 2011; Pedersen et al., 2015; Rogstad et al., 2017; Sonne, 2010; Sonne et al., 2005, 2006a, 2006b, 2006c, 2007a, 2007b, 2007c, 2008a, 2008b, 2008c, 2008d, 2008e, 2009a, 2009b, 2010b, 2014a, 2014b, 2017; Verreault et al., 2008). Other examples effect evaluation is the use of Risk Quotients comparing body burden and critical body residues estimated from PBPK modelling from rats and mice relative to immunologic, reproductive and carcinogenic effects, but such studies does not provide a better and more relevant picture relative to population effect of Arctic species in focus of this assessment (Sonne et al., 2009c, 2015, 2016; Dietz et al., 2015, 2018a).
Liver histopathology of Baltic grey seals (Halichoerus grypus) over three decades
2020, Environment InternationalCitation Excerpt :Bile duct proliferations were also reported in mammals exposed to mercury and PCB exposure, including captive controlled studies of mink (Bergman et al., 1992; Kelly 1993; Sonne et al., 2005; Sonne et al., 2013; Sonne et al., 2018). The positive relationship between mild multifocal bile duct hyperplasia and portal mononuclear cell infiltration found in the present study could not be found in previous studies of other marine mammals (Sonne et al., 2005, 2008, 2012) and the reason for the relationship is unknown. In the present study, livers from animals over 34 years of age were examined, within a timeframe in which the grey seals were exposed to PCB and DDT.
Mandibular shape in farmed Arctic foxes (Vulpes lagopus) exposed to persistent organic pollutants
2019, Science of the Total EnvironmentCanidae, ursidae, and ailuridae
2018, Pathology of Wildlife and Zoo Animals