Skip to main content
NCBI home page
Environmental Health Perspectives logoLink to Environmental Health Perspectives
. 2003 Oct;111(13):1608–1612. doi: 10.1289/ehp.6226

Age- and sex-dependent distribution of persistent organochlorine pollutants in urban foxes.

Ramiro Dip 1, Daniel Hegglin 1, Peter Deplazes 1, Oscar Dafflon 1, Herbert Koch 1, Hanspeter Naegeli 1
PMCID: PMC1241682  PMID: 14527839

Abstract

The colonization of urban and suburban habitats by red foxes (Vulpes vulpes) provides a novel sentinel species to monitor the spread of anthropogenic pollutants in densely populated human settlements. Here, red foxes were collected in the municipal territory of Zürich, Switzerland, and their perirenal adipose tissue was examined for persistent organochlorine residues. This pilot study revealed an unexpected pattern of contamination by polychlorinated biphenyls (PCBs), with significantly higher levels of the predominant congeners PCB-138, PCB-153, and PCB-180 in juvenile foxes relative to adult animals. Further data analysis demonstrated that the observed difference was attributable to an age-dependent reduction of PCB concentrations in females, whereas male foxes retained approximately the same PCB burden throughout their life span. A similar sex-related bias between population members has been observed, primarily in marine mammals. Interestingly, the reduction of organochlorine contents with progressive age is reminiscent of human studies, where an extensive maternal transfer of xenobiotics to the offspring has been shown to result in increased exposure levels of infants relative to adults. To our knowledge, this is the first example of an urban wildlife species that faithfully reflects the dynamic distribution of toxic contaminants in the corresponding human population. Suburban and urban foxes occupy habitats in close proximity to humans, depend on anthropogenic food supplies, are relatively long-lived and readily available for sampling, can be easily aged and sexed, have a limited home range, and, therefore, meet several important requirements to serve as a surrogate species for the assessment of toxic health hazards.

Full Text

The Full Text of this article is available as a PDF (245.2 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abraham K., Knoll A., Ende M., Päpke O., Helge H. Intake, fecal excretion, and body burden of polychlorinated dibenzo-p-dioxins and dibenzofurans in breast-fed and formula-fed infants. Pediatr Res. 1996 Nov;40(5):671–679. doi: 10.1203/00006450-199611000-00005. [DOI] [PubMed] [Google Scholar]
  2. Abraham K., Päpke O., Gross A., Kordonouri O., Wiegand S., Wahn U., Helge H. Time course of PCDD/PCDF/PCB concentrations in breast-feeding mothers and their infants. Chemosphere. 1998 Oct-Nov;37(9-12):1731–1741. doi: 10.1016/s0045-6535(98)00238-0. [DOI] [PubMed] [Google Scholar]
  3. Beckmen K. B., Ylitalo G. M., Towell R. G., Krahn M. M., O'Hara T. M., Blake J. E. Factors affecting organochlorine contaminant concentrations in milk and blood of northern fur seal (Callorhinus ursinus) dams and pups from St. George Island, Alaska. Sci Total Environ. 1999 Jul 1;231(2-3):183–200. doi: 10.1016/s0048-9697(99)00094-7. [DOI] [PubMed] [Google Scholar]
  4. Beeby A. What do sentinels stand for? Environ Pollut. 2001;112(2):285–298. doi: 10.1016/s0269-7491(00)00038-5. [DOI] [PubMed] [Google Scholar]
  5. Bernt K. E., Hammill M. O., Lebeuf M., Kovacs K. M. Levels and patterns of PCBs and OC pesticides in harbour and grey seals from the St Lawrence Estuary, Canada. Sci Total Environ. 1999 Dec 15;243-244:243–262. doi: 10.1016/s0048-9697(99)00400-3. [DOI] [PubMed] [Google Scholar]
  6. Cogliano V. J. Assessing the cancer risk from environmental PCBs. Environ Health Perspect. 1998 Jun;106(6):317–323. doi: 10.1289/ehp.98106317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Colborn T., vom Saal F. S., Soto A. M. Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environ Health Perspect. 1993 Oct;101(5):378–384. doi: 10.1289/ehp.93101378. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cook C. M., Sgardelis S. P., Pantis J. D., Lanaras T. Concentrations of Pb, Zn, and Cu in Taraxacum spp. in relation to urban pollution. Bull Environ Contam Toxicol. 1994 Aug;53(2):204–210. doi: 10.1007/BF00192034. [DOI] [PubMed] [Google Scholar]
  9. Corsolini S., Burrini L., Focardi S., Lovari S. How can we use the red fox as a bioindicator of organochlorines? Arch Environ Contam Toxicol. 2000 Nov;39(4):547–556. doi: 10.1007/s002440010139. [DOI] [PubMed] [Google Scholar]
  10. Doganoc D. Z., Gacnik K. S. Lead and cadmium in meat and organs of game in Slovenia. Bull Environ Contam Toxicol. 1995 Jan;54(1):166–170. doi: 10.1007/BF00196284. [DOI] [PubMed] [Google Scholar]
  11. Dougherty C. P., Henricks Holtz S., Reinert J. C., Panyacosit L., Axelrad D. A., Woodruff T. J. Dietary exposures to food contaminants across the United States. Environ Res. 2000 Oct;84(2):170–185. doi: 10.1006/enrs.2000.4027. [DOI] [PubMed] [Google Scholar]
  12. Fry D. M., Toone C. K. DDT-induced feminization of gull embryos. Science. 1981 Aug 21;213(4510):922–924. doi: 10.1126/science.7256288. [DOI] [PubMed] [Google Scholar]
  13. Frøslie A., Haugen A., Holt G., Norheim G. Levels of cadmium in liver and kidneys from Norwegian cervides. Bull Environ Contam Toxicol. 1986 Sep;37(3):453–460. doi: 10.1007/BF01607788. [DOI] [PubMed] [Google Scholar]
  14. Georgii S., Bachour G., Failing K., Eskens U., Elmadfa I., Brunn H. Polychlorinated biphenyl congeners in foxes in Germany from 1983 to 1991. Arch Environ Contam Toxicol. 1994 Jan;26(1):1–6. doi: 10.1007/BF00212786. [DOI] [PubMed] [Google Scholar]
  15. Giesy J. P., Kannan K. Dioxin-like and non-dioxin-like toxic effects of polychlorinated biphenyls (PCBs): implications for risk assessment. Crit Rev Toxicol. 1998 Nov;28(6):511–569. doi: 10.1080/10408449891344263. [DOI] [PubMed] [Google Scholar]
  16. Golden R. J., Noller K. L., Titus-Ernstoff L., Kaufman R. H., Mittendorf R., Stillman R., Reese E. A. Environmental endocrine modulators and human health: an assessment of the biological evidence. Crit Rev Toxicol. 1998 Mar;28(2):109–227. doi: 10.1080/10408449891344191. [DOI] [PubMed] [Google Scholar]
  17. Guillette L. J., Jr, Pickford D. B., Crain D. A., Rooney A. A., Percival H. F. Reduction in penis size and plasma testosterone concentrations in juvenile alligators living in a contaminated environment. Gen Comp Endocrinol. 1996 Jan;101(1):32–42. doi: 10.1006/gcen.1996.0005. [DOI] [PubMed] [Google Scholar]
  18. Hofer S., Gloor S., Müller U., Mathis A., Hegglin D., Deplazes P. High prevalence of Echinococcus multilocularis in urban red foxes (Vulpes vulpes) and voles (Arvicola terrestris) in the city of Zürich, Switzerland. Parasitology. 2000 Feb;120(Pt 2):135–142. doi: 10.1017/s0031182099005351. [DOI] [PubMed] [Google Scholar]
  19. Hunter D. J., Hankinson S. E., Laden F., Colditz G. A., Manson J. E., Willett W. C., Speizer F. E., Wolff M. S. Plasma organochlorine levels and the risk of breast cancer. N Engl J Med. 1997 Oct 30;337(18):1253–1258. doi: 10.1056/NEJM199710303371801. [DOI] [PubMed] [Google Scholar]
  20. Hutton M. The role of wildlife species in the assessment of biological impact from chronic exposure to persistent chemicals. Ecotoxicol Environ Saf. 1982 Oct;6(5):471–478. doi: 10.1016/0147-6513(82)90028-8. [DOI] [PubMed] [Google Scholar]
  21. Jorgenson J. L. Aldrin and dieldrin: a review of research on their production, environmental deposition and fate, bioaccumulation, toxicology, and epidemiology in the United States. Environ Health Perspect. 2001 Mar;109 (Suppl 1):113–139. doi: 10.1289/ehp.01109s1113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kimbrough R. D., Doemland M. L., Krouskas C. A. Analysis of research studying the effects of polychlorinated biphenyls and related chemicals on neurobehavioral development in children. Vet Hum Toxicol. 2001 Aug;43(4):220–228. [PubMed] [Google Scholar]
  23. Kottferová J., Koréneková B. Distribution of Cd and Pb in the tissues and organs of free-living animals in the territory of Slovakia. Bull Environ Contam Toxicol. 1998 Jan;60(1):171–176. doi: 10.1007/s001289900607. [DOI] [PubMed] [Google Scholar]
  24. Krieger N., Wolff M. S., Hiatt R. A., Rivera M., Vogelman J., Orentreich N. Breast cancer and serum organochlorines: a prospective study among white, black, and Asian women. J Natl Cancer Inst. 1994 Apr 20;86(8):589–599. doi: 10.1093/jnci/86.8.589. [DOI] [PubMed] [Google Scholar]
  25. Labrot F., Narbonne J. F., Ville P., Saint Denis M., Ribera D. Acute toxicity, toxicokinetics, and tissue target of lead and uranium in the clam Corbicula fluminea and the worm Eisenia fetida: comparison with the fish Brachydanio rerio. Arch Environ Contam Toxicol. 1999 Feb;36(2):167–178. doi: 10.1007/s002449900457. [DOI] [PubMed] [Google Scholar]
  26. Moss O. R., Gross E. A., James R. A., Janszen D. B., Ross P. W., Roberts K. C., Howard A. M., Harkema J. R., Calderón-Garcidueñas L., Morgan K. T. Respiratory tract toxicity in rats exposed to Mexico City air. Res Rep Health Eff Inst. 2001 Mar;(100):1–29. [PubMed] [Google Scholar]
  27. Poole K. G., Elkin B. T., Bethke R. W. Organochlorine and heavy metal contaminants in wild mink in western Northwest Territories, Canada. Arch Environ Contam Toxicol. 1998 May;34(4):406–413. doi: 10.1007/s002449900337. [DOI] [PubMed] [Google Scholar]
  28. Rodgers B. E., Wickliffe J. K., Phillips C. J., Chesser R. K., Baker R. J. Experimental exposure of naive bank voles (Clethrionomys glareolus) to the Chornobyl, Ukraine, environment: a test of radioresistance. Environ Toxicol Chem. 2001 Sep;20(9):1936–1941. [PubMed] [Google Scholar]
  29. Safe S. H. Polychlorinated biphenyls (PCBs): environmental impact, biochemical and toxic responses, and implications for risk assessment. Crit Rev Toxicol. 1994;24(2):87–149. doi: 10.3109/10408449409049308. [DOI] [PubMed] [Google Scholar]
  30. Santiago D., Motas-Guzmán M., Reja A., María-Mojica P., Rodero B., García-Fernández A. J. Lead and cadmium in red deer and wild boar from Sierra Morena Mountains (Andalusia, Spain). Bull Environ Contam Toxicol. 1998 Dec;61(6):730–737. doi: 10.1007/s001289900822. [DOI] [PubMed] [Google Scholar]
  31. Schöffel I., Schein E., Wittstadt U., Hentsche J. Zur Parasitenfauna des Rotfuchses in Berlin (West). Berl Munch Tierarztl Wochenschr. 1991 May 1;104(5):153–157. [PubMed] [Google Scholar]
  32. Seegal R. F. The neurochemical effects of PCB exposure are age-dependent. Arch Toxicol Suppl. 1994;16:128–137. doi: 10.1007/978-3-642-78640-2_15. [DOI] [PubMed] [Google Scholar]
  33. Severinsen T., Skaare J. U., Lydersen C. Spatial distribution of persistent organochlorines in ringed seal (Phoca hispida) blubber. Mar Environ Res. 2000 Apr;49(3):291–302. doi: 10.1016/s0141-1136(99)00078-1. [DOI] [PubMed] [Google Scholar]
  34. Shore R. F., Casulli A., Bologov V., Wienburg C. L., Afsar A., Toyne P., Dell'Omo G. Organochlorine pesticide, polychlorinated biphenyl and heavy metal concentrations in wolves (Canis lupus L. 1758) from north-west Russia. Sci Total Environ. 2001 Dec 3;280(1-3):45–54. doi: 10.1016/s0048-9697(01)00802-6. [DOI] [PubMed] [Google Scholar]
  35. Sures Bernd, Grube Katja, Taraschewski Horst. Experimental studies on the lead accumulation in the cestode Hymenolepis diminuta and its final host, Rattus norvegicus. Ecotoxicology. 2002 Oct;11(5):365–368. doi: 10.1023/a:1020561406624. [DOI] [PubMed] [Google Scholar]
  36. Tyler C. R., Jobling S., Sumpter J. P. Endocrine disruption in wildlife: a critical review of the evidence. Crit Rev Toxicol. 1998 Jul;28(4):319–361. doi: 10.1080/10408449891344236. [DOI] [PubMed] [Google Scholar]
  37. Vreugdenhil Hestien J. I., Lanting Caren I., Mulder Paul G. H., Boersma E. Rudy, Weisglas-Kuperus Nynke. Effects of prenatal PCB and dioxin background exposure on cognitive and motor abilities in Dutch children at school age. J Pediatr. 2002 Jan;140(1):48–56. doi: 10.1067/mpd.2002.119625. [DOI] [PubMed] [Google Scholar]
  38. Willingham A. L., Ockens N. W., Kapel C. M., Monrad J. A helminthological survey of wild red foxes (Vulpes vulpes) from the metropolitan area of Copenhagen. J Helminthol. 1996 Sep;70(3):259–263. doi: 10.1017/s0022149x00015509. [DOI] [PubMed] [Google Scholar]
  39. Winneke G., Bucholski A., Heinzow B., Krämer U., Schmidt E., Walkowiak J., Wiener J. A., Steingrüber H. J. Developmental neurotoxicity of polychlorinated biphenyls (PCBS): cognitive and psychomotor functions in 7-month old children. Toxicol Lett. 1998 Dec 28;102-103:423–428. doi: 10.1016/s0378-4274(98)00334-8. [DOI] [PubMed] [Google Scholar]
  40. van der Schalie W. H., Gardner H. S., Jr, Bantle J. A., De Rosa C. T., Finch R. A., Reif J. S., Reuter R. H., Backer L. C., Burger J., Folmar L. C. Animals as sentinels of human health hazards of environmental chemicals. Environ Health Perspect. 1999 Apr;107(4):309–315. doi: 10.1289/ehp.99107309. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Environmental Health Perspectives are provided here courtesy of National Institute of Environmental Health Sciences

RESOURCES