Skip to main content
Environmental Health Perspectives logoLink to Environmental Health Perspectives
. 1993 Mar;99:351–368. doi: 10.1289/ehp.9399351

The use of mammals as sentinels for human exposure to toxic contaminants in the environment.

D J O'Brien 1, J B Kaneene 1, R H Poppenga 1
PMCID: PMC1567056  PMID: 8319652

Abstract

The use of sentinel species shows the potential to bridge the gap between animal-based and human-based environmental health research. With regard to the assessment of environmental contamination, the use of the terms "indicator," "monitor," and "sentinel" has often been confusing and ambiguous. A set of definitions is proposed as a standard to rectify this situation. The advantages of the use of sentinel species are provided, as well as criteria for sentinel selection, based on species characteristics. The recent use of mammals as sentinels for human exposure to toxic environmental contaminants is reviewed. A tabulated review of mammals proposed as indicators or monitors is included, as these may act as a database for the selection of sentinel species for future research efforts. The complexity and subtlety of factors interacting between an organism and its environment make it imperative that one provide a focused definition of what one wants the sentinel to assess and for what particular aspect of human health. Some examples of how sentinels might be selected for particular research questions are provided. While the potential for sentinel use in the field of environmental health is enormous, future investigators need to choose sentinels carefully, based on well-defined research questions, and confine conclusions drawn to the particular problem the sentinel was chosen to assess.

Full text

PDF
351

Selected References

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

  1. ALLCROFT R., BLAXTER K. L. Lead as a nutritional hazard to farm livestock. V. The toxicity of lead to cattle and sheep and an evaluation of the lead hazard under farm conditions. J Comp Pathol. 1950 Jul;60(3):209–218. doi: 10.1016/s0368-1742(50)80019-x. [DOI] [PubMed] [Google Scholar]
  2. Anas R. E. DDT plus PCB'S in blubber of harbor seals. Pestic Monit J. 1974 Jun;8(1):12–14. [PubMed] [Google Scholar]
  3. Andersen A., Hansen H. H. Cadmium and zinc in kidneys from Danish cattle. Nord Vet Med. 1982 Oct;34(10):340–349. [PubMed] [Google Scholar]
  4. Anderson-Bledsoe K. L., Scanlon P. F. Heavy metal concentrations in tissues of Virginia river otters. Bull Environ Contam Toxicol. 1983 Apr;30(4):442–447. doi: 10.1007/BF01610158. [DOI] [PubMed] [Google Scholar]
  5. Aulerich R. J., Ringer R. K., Iwamoto S. Reproductive failure and mortality in mink fed on Great Lakes fish. J Reprod Fertil Suppl. 1973 Dec;19:365–376. [PubMed] [Google Scholar]
  6. Bacher G. J. Mercury concentrations in the Australian fur seal Arctocephalus pusillus from SE Australian waters. Bull Environ Contam Toxicol. 1985 Oct;35(4):490–495. doi: 10.1007/BF01636543. [DOI] [PubMed] [Google Scholar]
  7. Best S. M. Some organoclorine pesticide residues in wildlife of the Northern Territory, Australia, 1970-71. Aust J Biol Sci. 1973 Oct;26(5):1161–1170. doi: 10.1071/bi9731161. [DOI] [PubMed] [Google Scholar]
  8. Bhat R. V., Krishnamachari K. A. Environmental lead toxicity in cattle. Bull Environ Contam Toxicol. 1980 Jul;25(1):142–145. doi: 10.1007/BF01985502. [DOI] [PubMed] [Google Scholar]
  9. Bigler W. J., Jenkins J. H., Cumbie P. M., Hoff G. L., Prather E. C. Wildlife and environmental health: raccoons as indicators of zoonoses and pollutants in southeastern United States. J Am Vet Med Assoc. 1975 Oct 1;167(7):592–597. [PubMed] [Google Scholar]
  10. Birke G., Johnels A. G., Plantin L. O., Sjöstrand B., Skerfving S., Westermark T. Studies on humans exposed to methyl mercury through fish consumption. Arch Environ Health. 1972 Aug;25(2):77–91. doi: 10.1080/00039896.1972.10666141. [DOI] [PubMed] [Google Scholar]
  11. Bleavins M. R., Aulerich R. J., Ringer R. K. Polychlorinated biphenyls (Aroclors 1016 and 1242): effects on survival and reproduction in mink and ferrets. Arch Environ Contam Toxicol. 1980;9(5):627–635. doi: 10.1007/BF01056942. [DOI] [PubMed] [Google Scholar]
  12. Bloom H., Noller B. N., Shenman G. A survey of blood lead levels in dogs and cats. Aust Vet J. 1976 Jul;52(7):312–316. doi: 10.1111/j.1751-0813.1976.tb02395.x. [DOI] [PubMed] [Google Scholar]
  13. Bowes G. W., Simoneit B. R., Burlingame A. L., de Lappe B. W., Risebrough R. W. The search for chlorinated dibenzofurans and chlorinated dibenzodioxins in wildlife populations showing elevated levels of embryonic death. Environ Health Perspect. 1973 Sep;5:191–198. doi: 10.1289/ehp.7305191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Buck W. B. Animals as monitors of environmental quality. Vet Hum Toxicol. 1979 Aug;21(4):277–284. [PubMed] [Google Scholar]
  15. Bunzl K., Kracke W., Kreuzer W. Stable lead, 210Pb and 210Po in the liver and kidneys of cattle. II. animals from an area near an abandoned lead mine. Food Cosmet Toxicol. 1980 Apr;18(2):133–137. doi: 10.1016/0015-6264(80)90066-8. [DOI] [PubMed] [Google Scholar]
  16. Burrows G. E. Lead toxicosis in domestic animals: a review of the role of lead mining and primary lead smelters in the United States. Vet Hum Toxicol. 1981 Oct;23(5):337–343. [PubMed] [Google Scholar]
  17. Carter C. D., Kimbrough R. D., Liddle J. A., Cline R. E., Zack M. M., Jr, Barthel W. F., Koehler R. E., Phillips P. E. Tetrachlorodibenzodioxin: an accidental poisoning episode in horse arenas. Science. 1975 May 16;188(4189):738–740. doi: 10.1126/science.1168366. [DOI] [PubMed] [Google Scholar]
  18. Carter L. J. Michigan's PBB Incident: Chemical Mix-Up Leads to Disaster. Science. 1976 Apr 16;192(4236):240–243. doi: 10.1126/science.192.4236.240. [DOI] [PubMed] [Google Scholar]
  19. Cohen N., Kneip T. J., Goldstein D. H., Muchmore E. A. The juvenile baboon as a model for studies of lead poisoning in children. J Med Primatol. 1972;1(3):142–155. doi: 10.1159/000460377. [DOI] [PubMed] [Google Scholar]
  20. Crête M., Potvin F., Walsh P., Benedetti J. L., Lefebvre M. A., Weber J. P., Paillard G., Gagnon J. Pattern of cadmium contamination in the liver and kidneys of moose and white-tailed deer in Québec. Sci Total Environ. 1987 Oct;66:45–53. doi: 10.1016/0048-9697(87)90076-3. [DOI] [PubMed] [Google Scholar]
  21. Curley A., Sedlak V. A., Girling E. D., Hawk R. E., Barthel W. F., Pierce P. E., Likosky W. H. Organic mercury identified as the cause of poisoning in humans and hogs. Science. 1971 Apr 2;172(3978):65–67. doi: 10.1126/science.172.3978.65. [DOI] [PubMed] [Google Scholar]
  22. Diters R. W., Nielsen S. W. Lead poisoning of raccoons in Connecticut. J Wildl Dis. 1978 Apr;14(2):187–192. doi: 10.7589/0090-3558-14.2.187. [DOI] [PubMed] [Google Scholar]
  23. Dobson R. C., Fahey J. E., Ballee D. L., Baugh E. R. Dieldrin and heptachlor epoxide residues in fat from hogs foraging on corn stover in insecticidally treated fields. Bull Environ Contam Toxicol. 1972 May;7(5):311–320. doi: 10.1007/BF01684531. [DOI] [PubMed] [Google Scholar]
  24. Dorn C. R., Phillips P. E., Pierce J. O., 2nd, Chase G. R. Cadmium, copper, lead and zinc in bovine hair in the new lead belt of Missouri. Bull Environ Contam Toxicol. 1974 Nov;12(5):626–632. doi: 10.1007/BF01684930. [DOI] [PubMed] [Google Scholar]
  25. Dowd P. F., Mayfield G. U., Coulon D. P., Graves J. B., Newsom J. D. Organochlorine residues in animals from three Louisiana watersheds in 1978 and 1979. Bull Environ Contam Toxicol. 1985 Jun;34(6):832–841. doi: 10.1007/BF01609814. [DOI] [PubMed] [Google Scholar]
  26. Elangbam C. S., Qualls C. W., Jr, Lochmiller R. L., Novak J. Development of the cotton rat (Sigmodon hispidus) as a biomonitor of environmental contamination with emphasis on hepatic cytochrome P-450 induction and population characteristics. Bull Environ Contam Toxicol. 1989 Apr;42(4):482–488. doi: 10.1007/BF01700225. [DOI] [PubMed] [Google Scholar]
  27. Fanelli R., Bertoni M. P., Castelli M. G., Chiabrando C., Martelli G. P., Noseda A., Garattini S., Binaghi C., Marazza V., Pezza F. 2,3,7,8-Tetrachlorodibenzo-p-dioxin toxic effects and tissue levels in animals from the contaminated area of Seveso, Italy. Arch Environ Contam Toxicol. 1980;9(5):569–577. doi: 10.1007/BF01056936. [DOI] [PubMed] [Google Scholar]
  28. Frank A. In search of biomonitors for cadmium: cadmium content of wild Swedish fauna during 1973-1976. Sci Total Environ. 1986 Dec 1;57:57–65. doi: 10.1016/0048-9697(86)90009-4. [DOI] [PubMed] [Google Scholar]
  29. Freeman H. C., Horne D. A. Mercury in Canadian seals. Bull Environ Contam Toxicol. 1973 Sep;10(3):172–180. doi: 10.1007/BF01720700. [DOI] [PubMed] [Google Scholar]
  30. Friedman M. A., Griffith F. D., Woods S. Pathologic analysis of mink mortality in New England mink. Arch Environ Contam Toxicol. 1977;5(4):457–469. doi: 10.1007/BF02220925. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Glickman L. T., Domanski L. M., Maguire T. G., Dubielzig R. R., Churg A. Mesothelioma in pet dogs associated with exposure of their owners to asbestos. Environ Res. 1983 Dec;32(2):305–313. doi: 10.1016/0013-9351(83)90114-7. [DOI] [PubMed] [Google Scholar]
  33. Glickman L. T., Schofer F. S., McKee L. J., Reif J. S., Goldschmidt M. H. Epidemiologic study of insecticide exposures, obesity, and risk of bladder cancer in household dogs. J Toxicol Environ Health. 1989;28(4):407–414. doi: 10.1080/15287398909531360. [DOI] [PubMed] [Google Scholar]
  34. Hamir A. N., Handson P. D., Sullivan N. D., Anderson G. Lead tissue levels of dogs from rural and urban areas of Victoria, Australia. Vet Rec. 1986 Jan 18;118(3):77–78. doi: 10.1136/vr.118.3.77. [DOI] [PubMed] [Google Scholar]
  35. Hamir A. N., Sullivan N. D., Handson P. D., Barr S. An outbreak of lead poisoning in dogs. Aust Vet J. 1985 Jan;62(1):21–23. doi: 10.1111/j.1751-0813.1985.tb06034.x. [DOI] [PubMed] [Google Scholar]
  36. Hayes H. H., Jr The comparative epidemiology of selected neoplasms between dogs, cats and humans. A review. Eur J Cancer. 1978 Dec;14(12):1299–1308. doi: 10.1016/0014-2964(78)90111-1. [DOI] [PubMed] [Google Scholar]
  37. Hayes H. M., Jr Canine bladder cancer: epidemiologic features. Am J Epidemiol. 1976 Dec;104(6):673–677. doi: 10.1093/oxfordjournals.aje.a112346. [DOI] [PubMed] [Google Scholar]
  38. Hecht H. Bestehen Beziehungen zwischen einer Belastung der Asung von Wildtieren mit Blei und Cadmium und ihren Rückständen in Wildbret? Z Gesamte Hyg. 1984 Jun;30(6):338–342. [PubMed] [Google Scholar]
  39. Hochstein J. R., Aulerich R. J., Bursian S. J. Acute toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin to mink. Arch Environ Contam Toxicol. 1988 Jan;17(1):33–37. doi: 10.1007/BF01055151. [DOI] [PubMed] [Google Scholar]
  40. Holden A. V. International cooperative study of organochlorine and mercury residues in wildlife, 1969-71. Pestic Monit J. 1973 Jun;7(1):37–52. [PubMed] [Google Scholar]
  41. Holterman W. F., de Voogt P., Peereboom-Stegeman J. H. Cadmium/zinc relationships in kidney cortex and metallothionein of horse and red deer: histopathological observations on horse kidneys. Environ Res. 1984 Dec;35(2):466–481. doi: 10.1016/0013-9351(84)90153-1. [DOI] [PubMed] [Google Scholar]
  42. Honda K., Tatsukawa R. Distribution of cadmium and zinc in tissues and organs, and their age-related changes in striped dolphins, Stenella coeruleoalba. Arch Environ Contam Toxicol. 1983 Sep;12(5):543–550. doi: 10.1007/BF01056550. [DOI] [PubMed] [Google Scholar]
  43. Jenkins J. H., Davis A. H., Bigler W. J., Hoff G. L. Mercury and cesium-137 in urban gray squirrels. Bull Environ Contam Toxicol. 1980 Aug;25(2):321–324. doi: 10.1007/BF01985532. [DOI] [PubMed] [Google Scholar]
  44. Khera K. S., Iverson F., Hierlihy L., Tanner R., Trivett G. Toxicity of methylmercury in neonatal cats. Teratology. 1974 Aug;10(1):69–76. doi: 10.1002/tera.1420100110. [DOI] [PubMed] [Google Scholar]
  45. Koh T. S., Babidge P. J. A comparison of blood lead levels in dogs from a lead-mining, lead-smelting, urban and rural island environment. Aust Vet J. 1986 Sep;63(9):282–285. doi: 10.1111/j.1751-0813.1986.tb08067.x. [DOI] [PubMed] [Google Scholar]
  46. Kuratsune M., Yoshimura T., Matsuzaka J., Yamaguchi A. Epidemiologic study on Yusho, a Poisoning Caused by Ingestion of Rice Oil Contaminated with a Commercial Brand of Polychlorinated Biphenyls. Environ Health Perspect. 1972 Apr;1:119–128. doi: 10.1289/ehp.7201119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Kurtz D. A., Kim K. C. Chlorinated hydrocarbon and PCB residues in tissues and lice of northern fur seals, 1972. Pestic Monit J. 1976 Dec;10(3):79–83. [PubMed] [Google Scholar]
  48. Köck M., Kosmus W., Pichler-Semmelrock F. P., Sixl W. Accumulation of heavy metals in animals. Part 1: Lead and cadmium contamination in some wild animals. J Hyg Epidemiol Microbiol Immunol. 1989;33(4 Suppl):521–528. [PubMed] [Google Scholar]
  49. Layher W. G., Fox L. B., Broxterman R. Environmental contaminants in raccoons in Kansas. Bull Environ Contam Toxicol. 1987 Dec;39(6):926–932. doi: 10.1007/BF01689580. [DOI] [PubMed] [Google Scholar]
  50. Linzey A. V. Effects of chronic polychlorinated biphenyls exposure on reproductive success of white-footed mice (Peromyscus leucopus). Arch Environ Contam Toxicol. 1987 Jul;16(4):455–460. doi: 10.1007/BF01055267. [DOI] [PubMed] [Google Scholar]
  51. Ma W. C. Heavy metal accumulation in the mole, Talpa europea, and earthworms as an indicator of metal bioavailability in terrestrial environments. Bull Environ Contam Toxicol. 1987 Dec;39(6):933–938. doi: 10.1007/BF01689581. [DOI] [PubMed] [Google Scholar]
  52. Mascanzoni D., von Bothmer S., Mattei T., Cristaldi M. Small mammals as biological indicators of radioactive contamination of the environment. Sci Total Environ. 1990 Dec 1;99(1-2):61–66. doi: 10.1016/0048-9697(90)90211-c. [DOI] [PubMed] [Google Scholar]
  53. Nalley L., Hoff G., Bigler W., Hull W. Pesticide levels in the omental fat of Florida raccoons. Bull Environ Contam Toxicol. 1975 Jun;13(6):741–744. doi: 10.1007/BF01721946. [DOI] [PubMed] [Google Scholar]
  54. Newell K. W., Ross A. D., Renner R. M. Phenoxy and picolinic acid herbicides and small-intestinal adenocarcinoma in sheep. Lancet. 1984 Dec 8;2(8415):1301–1305. doi: 10.1016/s0140-6736(84)90821-3. [DOI] [PubMed] [Google Scholar]
  55. Norheim G., Sivertsen T., Brevik E. M., Frøslie A. Kvikksølv og selen i villmink (Mustela vision) fra Norge. Nord Vet Med. 1984 Jan-Feb;36(1-2):43–48. [PubMed] [Google Scholar]
  56. Paukert J., Obrusník I. The hair of the common hare (Lepus europaeus Pall.) and of the common vole (Microtus arvalis Pall.) as indicator of the environmental pollution. J Hyg Epidemiol Microbiol Immunol. 1986;30(1):27–32. [PubMed] [Google Scholar]
  57. Platonow N. S., Karstad L. H. Dietary effects of polychlorinated biphenyls on mink. Can J Comp Med. 1973 Oct;37(4):391–400. [PMC free article] [PubMed] [Google Scholar]
  58. Raisbeck M. F., Kendall J. D., Rottinghaus G. E. Organochlorine insecticide problems in livestock. Vet Clin North Am Food Anim Pract. 1989 Jul;5(2):391–410. doi: 10.1016/s0749-0720(15)30983-x. [DOI] [PubMed] [Google Scholar]
  59. Robens J., Anthony H. D. Polychlorinated biphenyl contamination of feeder cattle. J Am Vet Med Assoc. 1980 Oct 1;177(7):613–615. [PubMed] [Google Scholar]
  60. Ronald K., Frank R. J., Dougan J., Frank R., Braun H. E. Pollutants in harp seals (Phoca groenlandica). II. Heavy metals and selenium. Sci Total Environ. 1984 Sep;38:153–166. doi: 10.1016/0048-9697(84)90213-4. [DOI] [PubMed] [Google Scholar]
  61. Rowley M. H., Christian J. J., Basu D. K., Pawlikowski M. A., Paigen B. Use of small mammals (voles) to assess a hazardous waste site at Love Canal, Niagara Falls, New York. Arch Environ Contam Toxicol. 1983 Jul;12(4):383–397. doi: 10.1007/BF01057581. [DOI] [PubMed] [Google Scholar]
  62. Scharding N. N., Oehme F. W. The use of animal models for comparative studies of lead poisoning. Clin Toxicol. 1973;6(3):419–424. doi: 10.3109/15563657308990541. [DOI] [PubMed] [Google Scholar]
  63. Schilling R. J., Steele G. K., Harris A. E., Donahue J. F., Ing R. T. Canine serum levels of polychlorinated biphenyls (PCBs): a pilot study to evaluate the use of animal sentinels in environmental health. Arch Environ Health. 1988 May-Jun;43(3):218–221. doi: 10.1080/00039896.1988.9934936. [DOI] [PubMed] [Google Scholar]
  64. Schilling R. J., Stehr-Green P. A. Health effects in family pets and 2,3,7,8-TCDD contamination in Missouri: a look at potential animal sentinels. Arch Environ Health. 1987 May-Jun;42(3):137–139. doi: 10.1080/00039896.1987.9935810. [DOI] [PubMed] [Google Scholar]
  65. Soliman S. A. Comparative studies on the neurotoxicity of organophosphorus compounds in different animal species. Neurotoxicology. 1983 Winter;4(4):107–115. [PubMed] [Google Scholar]
  66. Somers J. D., Goski B. C., Barrett M. W. Organochlorine residues in northeastern Alberta otters. Bull Environ Contam Toxicol. 1987 Nov;39(5):783–790. doi: 10.1007/BF01855855. [DOI] [PubMed] [Google Scholar]
  67. Takeuchi T., D'Itri F. M., Fischer P. V., Annett C. S., Okabe M. The outbreak of Minamata disease (methyl mercury poisoning) in cats on Northwestern Ontario reserves. Environ Res. 1977 Apr;13(2):215–228. doi: 10.1016/0013-9351(77)90098-6. [DOI] [PubMed] [Google Scholar]
  68. Talmage S. S., Walton B. T. Small mammals as monitors of environmental contaminants. Rev Environ Contam Toxicol. 1991;119:47–145. doi: 10.1007/978-1-4612-3078-6_2. [DOI] [PubMed] [Google Scholar]
  69. Thomas C. W., Rising J. L., Moore J. K. Blood lead concentrations in three groups of dogs from a suburban Illinois community. J Am Vet Med Assoc. 1975 Dec 1;167(11):995–999. [PubMed] [Google Scholar]
  70. Thomas C. W., Rising J. L., Moore J. K. Blood lead concentrations of children and dogs from 83 Illinois families. J Am Vet Med Assoc. 1976 Dec 1;169(11):1237–1240. [PubMed] [Google Scholar]
  71. Tucker R. K., Leitzke J. S. Comparative toxicology of insecticides for vertebrate wildlife and fish. Pharmacol Ther. 1979;6(1):167–220. doi: 10.1016/0163-7258(79)90060-3. [DOI] [PubMed] [Google Scholar]
  72. Way C. A., Schroder G. D. Accumulation of lead and cadmium in wild populations of the commensal rat, Rattus norvegicus. Arch Environ Contam Toxicol. 1982;11(4):407–417. doi: 10.1007/BF01056066. [DOI] [PubMed] [Google Scholar]
  73. Witkowski S. A., Ault S. R., Field R. W. Lead concentrations in white-tailed deer mandibles and teeth. Bull Environ Contam Toxicol. 1982 May;28(5):561–565. doi: 10.1007/BF01605585. [DOI] [PubMed] [Google Scholar]
  74. Wren C. D. A review of metal accumulation and toxicity in wild mammals. I. Mercury. Environ Res. 1986 Jun;40(1):210–244. doi: 10.1016/s0013-9351(86)80098-6. [DOI] [PubMed] [Google Scholar]
  75. Wren C. D., Hunter D. B., Leatherland J. F., Stokes P. M. The effects of polychlorinated biphenyls and methylmercury, singly and in combination on mink. II: Reproduction and kit development. Arch Environ Contam Toxicol. 1987 Jul;16(4):449–454. doi: 10.1007/BF01055266. [DOI] [PubMed] [Google Scholar]
  76. Zakrzewska M. Effect of lead on postnatal development of the bank vole (Clethrionomys glareolus). Arch Environ Contam Toxicol. 1988 May;17(3):365–371. doi: 10.1007/BF01055174. [DOI] [PubMed] [Google Scholar]
  77. Zook B. C. Lead intoxication in urban dogs. Clin Toxicol. 1973;6(3):377–388. doi: 10.3109/15563657308990538. [DOI] [PubMed] [Google Scholar]

Articles from Environmental Health Perspectives are provided here courtesy of American Chemical Society

RESOURCES