Read the Spanish translation: Conociendo al Plomo: el Ecosistema y los Aspectos Políticos
Abstract
Society has long understood the toxicity of lead (Pb) to humans,21,29 but lead poisoning in animals is far less well documented. It was not until late in the 19th century that the first reliable reports of toxicity in domestic animals and wildlife appeared.8,32 During much of the 20th century lead was marketed as a wonderful material of many uses. It took heroic efforts by physicians like Alice Hamilton and Herbert Needleman and researchers like Clair Patterson to build the scientific foundations necessary to implement significant policy change. By the late 1970s, lead had been eliminated from most gasolines and household paints and average blood lead had begun to decline in the U.S. population.2 Subsequent regulations also brought about modest restrictions on other uses of lead including solder, ceramic glazes, and a host of other products in an effort to protect human health; but a great many products containing lead remain on the market.
After an initial drop in lead use in the U.S. in the late 1970s, the amount of lead mined, smelted, manufactured into products, and marketed in the U.S. has remained remarkably constant from the early 1980s through the present day.31 Currently the major use of lead in the U.S. and most developed countries is for lead acid storage batteries. It is difficult to find precise numbers, but roughly 8% of lead use in the United States goes into fishing gear, bullets, and shot for firearms.3 It should be noted that although there has been a gradual decline in the sales of hunting and fishing licenses in the United States over the last 30 years, there has been a dramatic increase in participation in the non-hunting shooting sports (target, trap, skeet, etc.).33 These activities continue to deposit many thousands of tons of lead into the environment each year.30,33 Mining, smelting, manufacture, and recycling also contribute significantly to environmental pollution. This is a more significant problem in many developing countries.4,9,33
The veterinary literature contains abundant case reports of lead poisoning in domestic species, but few large-scale epidemiologic studies exist.18 In the realm of wildlife, significant mortalities in waterfowl have been documented for over 100 years,8 but it was the threat of lead poisoning to bald eagles (Haliaeetus leucocephalus) that brought about the adoption of non-toxic shot for waterfowl hunting in the U.S. in the late 1980s.1,33 In the U.S., nearly all bullets and shot used for hunting upland game birds and mammals (as well as for the shooting sports) are still made from lead.33 Even today, large numbers of eagles, loons, waterfowl, raptors, and many other species die annually from ingesting lead used for hunting and fishing activities.11,17,22,24,25,28,33 For one endangered scavenger, the California condor (Gymnogyps californianus), lead poisoning has been shown to be a major mortality factor that is significantly limiting the success of reintroduction efforts.33
Although clinical lead poisoning is still an important disease in human medicine, a great deal of recent research has focused on the sublethal, chronic effects of lead. Significant clinical effects on many systems have been documented including blood pressure and the cardiovascular system, reproductive system, renal function, the hematopoietic and immune systems, and both the central and peripheral nervous systems, including significant detrimental effects on learning, control of aggressive behavior, sensation, fine motor control, etc.10,23,26
Thus far, relatively little work has been done on sublethal effects in non-human vertebrates, but those studies that do exist document similar effects on a wide variety of vertebrates including mammals, birds, reptiles, amphibians, and fish.13 Deficits in cognitive skills have been reported in children with blood lead concentrations as low as 5 µg/dL.15 Another study found that a net increase of 1 µg/dL in the lifetime average blood lead level was correlated with a loss of 0.46 IQ points.7 Cognitive effects of sublethal lead poisoning are beginning to be studied in wildlife. Effects on locomotion, food begging, feeding, treadmill learning, thermoregulation, and individual recognition were observed in herring gull (Larus argentatus) chicks dosed with lead acetate to produce feather lead concentrations equivalent to those found in wild gulls.5 Several studies have found an association between sub-clinical lead toxicosis and delinquent, antisocial, and aggressive behaviors in humans.19,20,27 Similarly, the development of aggressive behaviors has been documented in domestic dogs and cats with elevated blood lead levels, as well as songbirds exposed to heavy metals.12,14,16 Hatchling turtles exposed to environmentally relevant lead concentrations showed physiologic and behavioral changes that would dramatically reduce their survival in the wild.6 Environmental lead exposure at low levels could be contributing to wildlife mortality by hindering the complex mental processes and social behaviors required for reproduction, migration, and a host of other activities.
Most people do not have to be convinced that lead is toxic, but it has been difficult to turn this understanding into integrated and cogent policy. To protect common loons from lead toxicosis, educational and legislative efforts have been made by loon groups in several states to encourage anglers to switch to non-toxic fishing gear. At the same time, other groups are working hard to educate the public and policy makers on risks to birds of prey and swans from ingested lead. Child health advocates and state and federal agencies spend millions of dollars each year to educate the public about the continuing dangers of lead paint exposure in older housing. Consumer safety groups try to gather data and issue alerts on potential dangers from lead in toys, traditional medicines, imported food and cosmetics. Occupational health agencies regularly deal with issues of worker exposure to lead in mining, manufacturing, and recycling industries, as well as with segments of the construction industry. As a society, it seems that we have segmented both our knowledge about lead poisoning and attempts at education and regulation. It is uncommon for veterinarians, physicians, public health professionals, occupational health specialists, and other interested parties to come together share their knowledge and attempt to find common solutions to the many problems associated with lead toxicosis.
There is still a great deal of work that needs to be done to protect humans and other animals from the threat of lead poisoning. Zoo and wildlife veterinarians can play a crucial role in gathering the data and performing the studies that will bring about policy change. Future research on lead toxicosis should consider the following four points:
1. The effects of lead poisoning are similar among vertebrate species and it is reasonable to (cautiously) extrapolate among taxa.
2. Clinical lead poisoning is underreported in both domestic animals and wildlife and many of the subclinical effects of lead are often missed.
3. A major impediment to recent policy initiatives is the disciplinary separation that exists among groups investigating issues related to lead poisoning.
4. While the concept of using animals as sentinels of human health is not new to conservation medicine, wildlife professionals may not realize the wealth of information that can be gained by taking the opposite approach and using humans as indicators or sentinels for animal and environmental health, particularly in the area of sublethal effects.
Literature Cited
1. Anderson, W.L., and S.P. Havera. 1989. Lead poisoning in Illinois waterfowl (1977–1988) and the implementation of nontoxic shot regulations. Illinois Natural History Survey. Champaign, Illinois. 37.
2. Annest, J.L., J.L. Pirkle, D. Makuc, J.W. Neese, D.D. Bayse, and M.G. Kovar. 1983. Chronological trend in blood lead levels between 1976 and 1980. The New England Journal of Medicine. 308(23):1373–1377.
3. Biviano, M.B., D.E. Sullivan, and L.A. Wagner. 1999. Total Materials Consumption: An Estimation Methodology and Example Using Lead, a Materials Flow Analysis. U.S. Geological Survey Circular 1183, USDOI. Washington, DC. 26.
4. Bullard, R.D. (ed.). 1994. Unequal Protection: Environmental Justice and Communities of Color. Sierra Club Books. San Francisco, California. 400.
5. Burger, J., and M. Gochfeld. 2005. Effects of lead on learning in herring gulls: an avian wildlife model for neurobehavioral deficits. NeuroToxicology. 26(4):615–624.
6. Burger, J. 1998. Effects of lead on behavior, growth and survival of hatchling slider turtles. Toxicology and Environmental Health. Part A. 55(7):495–502.
7. Canfield, R.L., C.R. Henderson, Jr., D.A. Cory-Slechta, C. Cox, T.A. Jusko, and B.P. Lanphear. 2003. Intellectual impairment in children with blood lead concentrations below 10 microg per deciliter. New England Journal of Medicine. 348:1517–1526.
8. Grinnell, G.B. 1894. Lead poisoning. Forest and Stream. 42(6):117–118.
9. Grossman E. 2006. High Tech Trash: Digital Devices, Hidden Toxics, and Human Health. Shearwater Press, Washington, DC. 336.
10. Hu H., R. Shih, S. Rothenberg, and B.S. Schwartz. 2007. The epidemiology of lead toxicity in adults: measuring dose and consideration of other methodologic issues. Environmental Health Perspectives. 115(3):455–462.
11. Janssen, D.L., J.E. Oosterhuis, J.L. Allen, M.P. Anderson, D.G. Welts, and S.N. Wiemeyer. 1986. Lead poisoning in free-ranging California condors. Journal of the American Veterinary Medical Association. 189(9):1115–1117.
12. Janssens, E., T. Dauwe, E. Van Duyse, J. Beernaert, R. Pinxten, and M. Eens. 2003. Effects of heavy metal exposure on aggressive behavior in a small territorial songbird. Archives of Environmental Contamination and Toxicology. 45:121–127.
13. Kasthuri, J., and M.R. Chandran. 1997. Sublethal effect of lead on feeding energetics, growth performance, biochemical composition and accumulation of the estuarine catfish, Mystus gulio (Hamilton). J Environ Biol. 18(1):95–101.
14. Koh, T.S. 1985. Diagnosis of lead poisoning in dogs. Australian Veterinary Journal. 62(12):434.
15. Lanphear, B.P., K. Dietrich, P. Auinger, and C. Cox. 2000. Cognitive deficits associated with blood lead concentrations <10 microg/dL in US children and adolescents. Public Health Reports. 115:521–529.
16. Li, W., W. Han, T.R. Gregg, F.W. Kemp, A.L. Davidow, D.B. Louria, A. Siegel, and J.D. Bogden. 2003. Lead exposure potentiates predatory attack behavior in the cat. Environmental Research. 92:197–206.
17. Mateo, R., R. Cadenas, M. Manez, and R. Guitart. 2001. Lead shot ingestion in two raptor species from Doñana, Spain. Ecotoxicology and Environmental Safety. 48(1):6–10.
18. Morgan R.V., F.M. Moore, L.K. Pearce, and T. Rossi. 1991. Clinical and laboratory findings in small companion animals with lead poisoning: 347 cases (1977–1986). J Am Vet Med Assoc. 199(1):93–97.
19. Needleman, H.L., J.A. Riess, M.J. Tobin, G.E. Biesecker, and J.B. Greenhouse. 1996. Bone lead levels and delinquent behavior. The Journal of the American Medical Association. 275(5):363–369.
20. Nevin, R. 2000. How lead exposure relates to temporal changes in IQ, violent crime, and unwed pregnancy. Environmental Research. 83(1):1–22.
21. Nriagu, J. 1983. Lead and Lead Poisoning in Antiquity. John Wiley & Sons. New York, NY. 437.
22. Pain, D.J. 1992. Lead poisoning in waterfowl: a review. In: Proceedings of an IWRB Workshop. Brussels, Belgium: 13–15 June 1991. International Waterfowl and Wetlands Research Bureau Special Publication No. 16, Slimbridge, UK. 7–13.
23. Patrick, L. 2006. Lead toxicity, a review of the literature: part I: exposure, evaluation, and treatment. Alternative Medicine Review. 11(1):2–22.
24. Pattee O.H., and D.J. Pain. 2003. Lead in the environment. In: Hoffman D.J., B.A. Rattner, G.A. Burton Jr., and J. Cairns Jr. (eds.). Handbook of Ecotoxicology. 2nd ed. Lewis Publishers, New York, NY. 373–408.
25. Redig, P.T., D.R. Smith, and L. Cruz-Martinez. 2009. Potential sources of lead exposure for bald eagles: A retrospective study. In: Watson, R.T., M. Fuller, M. Pokras, and W.G. Hunt (eds.). Ingestion of Lead from Spent Ammunition: Implications for Wildlife and Humans. The Peregrine Fund, Boise, Idaho. 208–209.
26. Schober, S.E., L.B. Mirel, B.I. Graubard, D.J. Brody, and K.M. Flegal. 2006. Blood lead levels and death from all causes, cardiovascular disease, and cancer: results from the NHANES III mortality study. Environmental Health Perspectives. 114:1538–1541.
27. Sciarillo, W.G., G. Alexander, and K.P. Farrell. 1992. Lead exposure and child behavior. American Journal of Public Health. 82(10):1356–1360.
28. Sidor I.F., M.A. Pokras, A.R. Major, R.H. Poppenga, K.M. Taylor, and R.M. Miconi. 2003. Mortality of common loons in New England, 1987–2000. Journal of Wildlife Diseases. 39(2):306–315.
29. Tanquerel des Planches, L. 1850. Lead Diseases: A Treatise. Tappan, Whittemore & Mason. Boston, MA. 441.
30. Twiss, M.P., and V.G. Thomas. 1998. Preventing fishing-sinker-induced lead poisoning of common loons through Canadian policy and regulative reform. Journal of Environmental Management. 53(1):49–59.
31. USGS. http://minerals.usgs.gov/minerals/pubs/commodity/lead/. Accessed April 27, 2010.
32. Walker, R.E. 1980–1981. Malleus and podagra: lead poisoning in horse and man. Vet Hist. 1(4):118–136.
33. Watson, R.T., M. Fuller, M. Pokras, and W.G. Hunt (eds.). 2009. Ingestion of Lead from Spent Ammunition: Implications for Wildlife and Humans. The Peregrine Fund. Boise, Idaho. 383.