Elsevier

Chemosphere

Volume 71, Issue 7, April 2008, Pages 1214-1224
Chemosphere

Organochlorine-induced histopathology in kidney and liver tissue from Arctic fox (Vulpes lagopus)

https://doi.org/10.1016/j.chemosphere.2007.12.028Get rights and content

Abstract

The effects of persistent organic pollutants on renal and liver morphology in farmed arctic fox (Vulpes lagopus) were studied under experimental conditions. Control animals received a diet containing pork (Sus scrofa) fat with low amounts of persistent organic pollutants, while the diet of the exposed animals contained whale blubber, ‘naturally’ contaminated with persistent organic pollutants. Polychlorinated biphenyls (PCB) and organochlorine pesticide (OCP) concentrations in the whale blubber were 488 and 395 ng/g wet weight, respectively. Animals were sacrificed and sampled when they were at their fattest (winter) as well as their lowest body weight (summer). The results show that PCB and OCP exposure causes renal (and probably also liver) lesions in arctic foxes. The prevalence of glomerular, tubular and interstitial lesions was significantly highest in the exposed group (chi-square: all p < 0.05). The frequency of liver lesions (steatosis, intravascular granulocyte accumulations, interstitial cell infiltrations, lipid granulomas, portal fibrosis and bile duct hyperplasia) were also highest in the exposed group, although not significantly (chi-square: all p > 0.05). The prevalence of lesions was not significantly different between lean (winter) and fat (summer) foxes for any of the lesions (chi-square: all p > 0.05). We suggest that wild arctic foxes exposed to an environmental cocktail of persistent organic pollutants, such as PCBs and OCPs, in their natural diet are at risk for developing chronic kidney and liver damage. Whether such lesions may have an impact on age and health of the animals remains uncertain.

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)

  • G. Wang-Andersen et al.

    Levels and congener pattern of PCBs in arctic fox (Alopex lagopus) in Svalbard

    Environ. Pollut.

    (1993)
  • J. Wolkers et al.

    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.

    (1998)
  • AMAP, 2004. AMAP Assessment 2002: Persistent Organic Pollutants in the Arctic. Arctic Monitoring and Assessment...
  • J.D. Bancroft et al.

    Theory and Practice of Histological Techniques

    (1996)
  • A. Bergman et al.

    Influence of commercial polychlorinated biphenyls and fractions there of on liver histology in female mink (Mustela vison)

    Ambio

    (1992)
  • A. Bergman et al.

    Renal lesions in Baltic grey seals (Halichoerus grypus) and ringed seals (Phoca hispida botnica)

    Ambio

    (2001)
  • A.U. Birnbaum et al.

    Differential toxicity of 2,3,7,8-tetrachloridibenzo-p-dioxin TCDD in C57BL-6J mice congenic at the AH locus

    Fund. Appl. Toxicol.

    (1990)
  • M. Braathen et al.

    Relationships between PCBs and thyroid hormones and retinol in female and male polar bears

    Environ. Health Perspect.

    (2004)
  • F.W. Braestrup

    A study of the arctic fox in Greenland Immigrations, fluctuations in numbers based mainly on trading statistics

    Medd. Grønl Biosci.

    (1941)
  • J. Churg et al.

    Renal disease

    (1995)
  • A.W. Confer et al.

    Thomsons Special Veterinary Pathology

    (1995)
  • R.S. Cotran et al.

    Robbins Pathologic Basis of Disease

    (1999)
  • K. Frafjord

    Food habits of arctic foxes (Alopex lagopus) on the western coast of Svalbard

    Arctic

    (1993)
  • E. Fuglei et al.

    Environmental contaminants in arctic foxes (Alopex lagopus) in Svalbard: relationships with feeding ecology and body condition

    Environ. Pollut.

    (2007)
  • M. Haave et al.

    Polychlorinated biphenyls and reproductive hormones in female polar bears at Svalbard

    Environ. Health Perspect.

    (2003)
  • L.M. Hiruki et al.

    Population dynamics of the arctic fox (Alopex lagopus), on Banks Island, Northwest Territories

    Can. Field Nat.

    (1989)
  • Johansen, P., Muir, D.C.G., Asmund, G., Rigét, F.F., 2004. Contaminants in Traditional Greenland Diet. Report to the...
  • H.T. Jonsson et al.

    Effects of prolonged exposure to dietary DDT and PCB on rat liver morphology

    Arch. Environm. Contam. Toxicol.

    (1981)
  • R.D. Kimbrough et al.

    The ultrastructure of livers of rats fed DDT and dieldrin

    Arch. Environ. Health

    (1971)
  • Cited by (52)

    • A risk assessment review of mercury exposure in Arctic marine and terrestrial mammals

      2022, Science of the Total Environment
      Citation 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 International
      Citation 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.

    • Canidae, ursidae, and ailuridae

      2018, Pathology of Wildlife and Zoo Animals
    View all citing articles on Scopus
    View full text