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EcoHealth

DOI: 10.1007/s10393-008-0177-x

Ó 2008 International Association for Ecology and Health

Lead Poisoning: Using Transdisciplinary Approaches to Solve


an Ancient Problem

Mark A. Pokras1 and Michelle R. Kneeland1

Wildlife Clinic and Center for Conservation Medicine, Cummings School of Veterinary Medicine, Tufts University, 200 Westboro Road,
North Grafton, MA 01536

Abstract: Conservation medicine examines the linkages among the health of people, animals, and the envi-
ronment. Few issues illustrate this approach better than an examination of lead (Pb) toxicity. Lead is cheap and
there is a long tradition of its use. But the toxic effects of Pb have also been recognized for many years. As a
result, western societies have eliminated or greatly reduced many traditional uses of Pb, including many paints,
gasoline, and solders because of threats to the health of humans and the environment. Legislation in several
countries has eliminated the use of lead shot for hunting waterfowl. Despite these advances, a great many Pb
products continue to be readily available. For example, wildlife agencies recognize that angling and shooting
sports deposit thousands of tons of Pb into the environment each year. In recent years, our knowledge of the
lethal and sublethal effects of Pb has grown dramatically. This discussion reviews the effects of lead on wildlife,
humans, and domestic animals. It also discusses the importance of bringing together all interest groups to find
safe alternatives, to develop new educational and policy initiatives, to eliminate many current uses of Pb, and to
clean up existing problems.

Keywords: lead, toxics, public health, conservation medicine

INTRODUCTION surprised to discover it was actually a lead (Pb) fishing


sinker. We were even more intrigued when a liver sample
‘‘I found a dead loon.’’ When New Hampshire biologist analysis concluded that the loon had died of lead poi-
Betsy McCoy said this over the phone in late 1987, we had soning. Inspired by this case, we have spent the past
no idea where this call would lead. As wildlife veterinar- 20 years working on the issue of lead poisoning, exam-
ians interested in conservation issues, we agreed to run a ining well over a thousand dead loons and testing hun-
few tests and perform a necropsy on the loon. Examining dreds of animals for lead toxicosis. Many conservation
the cadaver, the bird was found to be in good condition and health professionals now are beginning to realize the
with perfect breeding plumage and no indications of extent to which accumulation of this toxic material has
parasites or disease. The only interesting piece of evidence been underestimated in terms of its impact on both hu-
was a radiographic image revealing a metal object within man and animal health.
the bird’s gizzard (Fig. 1). During the necropsy, we were Although we are still struggling to understand the full
scope of the issue, lead poisoning is not a new problem.
Correspondence to: Mark A. Pokras, e-mail: mark.pokras@tufts.edu The toxic effects of lead have been reported for centuries in
Mark A. Pokras and Michelle R. Kneeland

BRIDGING THE HUMAN/ANIMAL DIVIDE


While the concept of using animals as sentinels of human
health is not new to the conservation medicine arena,
wildlife professionals seldom realize the wealth of infor-
mation that can be gained by taking the opposite approach
and using humans as indicators of animal and environ-
mental health. A representative medium-size mammal,
Homo sapiens is by far the best understood and most widely
studied species on the planet, so why not utilize this
abundance of data to help us understand our nonhuman
counterparts? In fact, it is from the human literature that
we get some of the best measures for sublethal effects of
lead toxicity. Low-level lead exposure has been associated
Figure 1. Radiograph of an adult common loon (Gavia immer) with with a wide range of clinical and subclinical conditions in
ingested lead (Pb) fishing gear. The bright white objects just below humans, including cognitive deficiencies in children, renal
and to the left of center are a sinker and jighead present in the impairment, hypertension, cataracts, and reproductive
gizzard. Also present are several small stones normally ingested by problems such as miscarriage, stillbirth, and decreased
loons. The Tufts Wildlife Clinic has performed necropsies on over fertility in men and women (Patrick, 2006).
1000 loons in the past 20 years, revealing that about 48% of adult Deficits in cognitive and academic skills have been
loons on New England lakes die from lead poisoning. reported in children with blood lead concentrations lower
than 5 lg/dL (Lanphear et al., 2000). Another study found
both humans and animals (Nriagu, 1983). Grinnell (1894) that a net increase of 1 lg/dL in the lifetime average blood
published the first U.S. report of lead poisoning in ducks lead level was correlated with a loss of 0.46 IQ points
caused by ingestion of spent shot more than 100 years ago. (Canfield et al., 2003). In light of these findings in humans,
One of the most comprehensive clinical descriptions of the cognitive effects of sublethal lead poisoning are begin-
human lead poisoning was written by Tanquerel des ning to be studied in wildlife. In herring gull (Larus ar-
Planches in 1848. Dr. Alice Hamilton performed her gentatus) chicks, for example, affects on locomotion, food
extensive work on the social costs of industrial lead poi- begging, feeding, treadmill learning, thermoregulation, and
soning in the early 1900s (Sicherman, 2003). And yet, Hu individual recognition were observed in chicks dosed with
et al. (2007) are able to state, ‘‘In the world of environ- lead to produce feather lead concentrations equivalent to
mental health and environmental medicine, lead exposure those found in wild gulls (Burger and Gochfeld, 2005).
remains one of the most important problems in terms of Several studies have found an association between sub-
prevalence of exposure and public health impact.’’ We have clinical lead toxicosis and delinquent, antisocial, and
to ask ourselves why more progress to eliminate this per- aggressive behaviors in humans (Sciarillo, 1992; Needleman
sistent health threat has not been made. et al., 1996; Nevin, 2000). Similarly, the development of
A major impediment to progress is the disciplinary aggressive behaviors has been documented in domestic
separation that has long existed among groups investigating dogs and cats with elevated blood lead levels, as well as
issues related to lead poisoning. While there are multiple songbirds (Parus major) exposed to heavy metals (Koh,
organizations currently working on the problem, most efforts 1985; Janssens et al., 2003; Li et al., 2003). Pattee and Pain
are narrowly focused on one particular aspect of lead poi- (2003) document an increasing use of lead worldwide and
soning. In this article, we discuss the need for a conservation state that ‘‘lead concentrations in many living organisms
medicine-based approach to the lead-poisoning problem that may be approaching thresholds of toxicity for the adverse
overcomes barriers between the disciplines of human and effects of lead.’’ Environmental lead exposure at low levels
animal health, barriers within the field of animal health, and could very well be contributing to wildlife mortality by
barriers between researchers and the general public in order hindering the complex mental processes and social behav-
to finally eliminate this persistent health threat. iors required for reproductive success and survival.
Transdisciplinary Approach to Lead Poisoning

Abdominal pain and peripheral neuropathy are two exposure. For example, literature concerning lead poison-
symptoms of lead poisoning that have been described in ing in raptor species such as eagles and condors (Haliaeetus
human literature for centuries (Tanquerel des Planches, leucocephalus and Gymnogyps californianus) focuses pri-
1850). Commonly referred to as ‘‘painter’s colic’’ and marily on ingestion of lead gunshot embedded in prey or
‘‘wrist drop’’ respectively, these conditions are not specific scavenged carcasses (Janssen et al., 1986; Mateo et al.,
to humans. Abdominal pain is recognized as a clinical sign 2001). Studies of lead-related mortality in the common
common to nearly all lead-poisoned animals (Osweiler, loon (Gavia immer) have identified ingestion of fishing
1996). Sileo and Fefer (1987) observed ‘‘droop wing,’’ the sinkers as the prime route of exposure (Pokras and Chafel,
avian equivalent of human wrist drop, in Laysan albatross 1992; Sidor et al., 2003). In waterfowl such as ducks and
(Diomedea immutabilis) fledglings that had ingested lead geese, toxicosis resulting from accidental intake of spent
paint chips from abandoned buildings. lead shot has been reported in the literature for over
Veterinarians and wildlife professionals are just 100 years (Pain, 1992).
beginning to investigate the potential effects of sublethal Increased collaboration between researchers with
lead levels in animals, and the human lead-poisoning lit- expertise in different taxa is needed in order to advance our
erature serves as a wonderful resource to guide future re- knowledge of lead in the environment. Approaching lead
search. Similarly, physicians and public health officials poisoning as just a waterfowl problem or just a raptor
must also be willing to shift their anthropocentric focus in problem impedes progress toward effective policy changes.
order to fully identify lead exposure risks to humans. For For instance, the impact of lead fragments remaining in
example, there have been numerous case reports in which a carcasses and gut piles on condor populations has been
child was tested and found to have elevated blood lead thoroughly investigated, but we know almost nothing
levels after a pet dog was diagnosed. Thomas et al. (1976) about the effects on other avian, mammalian, and reptilian
reported that a blood lead concentration of diagnostic scavengers. While it is crucial to comprehend the pathology
significance in a family dog resulted in a sixfold increase in within a particular species, we must also gain a better
the probability of finding a child in the same family with understanding of lead effects at the level of ecosystems. We
similarly elevated blood lead levels. There is also a possible know lead can accumulate in organisms such as inverte-
connection between lead in the tissues of waterfowl or brates and plants, but we still have much to learn about
game animals and human health. Sportsmen and their how this influences the rest of the food chain (Pattee and
families may be exposed to high lead concentrations from Pain, 2003). Deciphering the intricate web of environ-
shot residue in the meat of hunted waterfowl. Johansen mental lead sources and exposure routes will allow us to
et al. (2006) found that hunters who reported regularly implement better strategies to reduce the occurrence of lead
eating birds hunted with lead shot had significantly higher poisoning in all species.
mean blood lead levels than hunters who reported not The gray squirrel (Sciurus carolinensis) may be a prime
eating hunted birds, 128 lg/L and 15 lg/L, respectively. illustration of our need for a more comprehensive under-
Even when bullet fragments are not present, secondary lead standing of lead exposure sources in wildlife. Recently, one
ingestion in waterfowl hunters can also occur through of these rodents was brought to the Tufts Wildlife Clinic
consuming the livers of chronically lead-poisoned birds and found to have a markedly elevated blood lead level of
(Guitart et al., 2002). over 65 lg/dL. Anecdotal stories of squirrels chewing on
lead chimney flashing have been reported by homeowners
for years, and recently a New Hampshire Fish and Game
OVERCOMING SPECIES ISOLATION biologist confirmed that she regularly receives calls about
‘‘problem’’ squirrels that continually gnaw on chimney
In addition to the separation that exists between the realms flashing. Analogous to children eating flecks of lead-based
of human and animal health, lead-poisoning research also paint, this may be evidence of pica (the persistent eating of
tends to be compartmentalized within specific taxonomic nonfood substances) in squirrels. It may also be one
groups. The research on lead toxicosis in wildlife concen- explanation for the lead-poisoned predators like red-tailed
trates predominantly on avian species. Most of the current hawks and barred owls that are periodically submitted to
literature falls within discrete categories such as raptors, the Wildlife Clinic. Because millions of homes nationwide
loons, or waterfowl, and discusses one specific route of have lead flashing around chimneys, doors, and other
Mark A. Pokras and Michelle R. Kneeland

openings, this appears to represents an overlooked source efforts to eliminate several uses of lead. Groups in India,
of plumbism (lead poisoning) in wildlife. China, Australia, Nigeria, and other countries are focused
on eliminating leaded paints and gasoline, and reducing
human and animal exposure. Agencies concerned with the
LIMITATIONS OF REGULATIONS globalization of world economies and the internationali-
zation of recycling (e.g., electronics) are increasingly taking
In April of 2005, the U.S. Consumer Product Safety steps to reduce toxic exports to developing countries in
Commission announced a nationwide recall of 1.5 million which protection for worker health may be lacking
children’s fishing rods because it was found that the paint (Grossman, 2006). Even in developed countries, advocates
on the rod exceeded the 0.06% limit for lead. Parents were for environmental justice have pointed out that exposure to
instructed to discontinue the use of the product immedi- lead and other toxic material falls disproportionately on
ately. At the same time, an online retailer specializing in many of the most vulnerable in our communities, often
children’s fishing gear was selling a product called ‘‘The nonwhite populations with little education living in poorer
Ultimate Fishing Kit for Kids.’’ The kit was comprised of a neighborhoods (Bullard, 1994). Clearly all stakeholders
plastic tackle box packed with 78 pure lead fishing sinkers. must be included in discussions of conservation and
This and hundreds of other lead-stocked fishing kits de- environmental health.
signed for children are still widely available and have never Although the toxicity of lead has been widely under-
been subject to a recall. stood and reported for hundreds of years, progress to im-
This example highlights the disjointed nature of current prove regulatory measures has been excruciatingly slow.
efforts to reduce lead exposure. Because many agencies in the Lead is cheap and easy to work with, and consequently the
U.S. regulate the various aspects of lead use—ranging from serious health risks associated with this metal are often
the Department of Labor for mining safety, to the Envi- overshadowed by its economic value. The continued
ronmental Protection Agency for environmental pollution, prevalence of lead poisoning in both humans and animals
to the Fish and Wildlife Service for the hunting of migratory is a signal that current policies are inadequate. A unified
birds—initiatives to limit lead’s toxic effects have been approach focused on interdisciplinary collaboration be-
myopic, lacking multidisciplinary perspective. In the U.S., tween specialists in human health, animal health, and
the banning of lead-based paint for residential use in 1978, ecological health is needed if we hope to make further
the phasing out of leaded fuel for on-road vehicles between progress in developing more protective legislation.
1973 and 1995, and, most recently, the mass recall of im-
ported toys containing lead each represents an independent
effort mobilized by separate groups. These measures have led CONNECTING SCIENCE AND SPORT
to vast improvements in ecological health and helped protect
human lives in much of the developed world. Annest et al. The use of lead for hunting and fishing sports represents a
(1983) reported a 37% decrease in average blood lead levels particularly challenging situation. In the past 20 years,
in the U.S. between 1976 and 1980, associated with a Vermont, New York, Maine, Massachusetts, New Hamp-
reduction in the lead content of gasoline during this period. shire, Great Britain, Denmark, and Canada have all passed
But this and other lead products are still widely available in legislation restricting the use of certain types of lead fishing
developing countries. Lead is still a major component in gear. In 1991, lead shot pellets were banned for use in
some industrial paints, and leaded fuel continues to be sold hunting waterfowl in the United States (a similar ban was
for off-road uses such as aircraft, automobile racing, farm instituted in Canada in 1999). But this is the only use of
equipment, and marine engines. Even more alarming is the lead for shooting that has been banned in the U.S. The vast
multiplicity of common household products that often majority of bullets are still lead. Virtually all shot pellets
contain lead—everything from curtain weights, solder, and used for such things as hunting small game (e.g., squirrels),
batteries to imported ceramics, candy, and hair dyes (Cohen upland game birds (e.g., grouse, quail), ‘‘varmint’’ shooting
and Roe, 1991; Fuortes and Bauer, 2000; Lynch et al., 2000; (e.g., crows), and skeet and trap shooting are still made
Centers for Disease Control and Prevention, 2004). from lead; the use of such lead ammunition in the U.S.
Fortunately, there is increased pressure to reduce lead results in the introduction of thousands of tons of metallic
in the U.S. and abroad. The European Union is engaged in lead into the environment annually. Because of the risks to
Transdisciplinary Approach to Lead Poisoning

a critically endangered species, in October 2007, California introduced. But most of these products are poorly mar-
passed a bill banning the use of lead ammunition in areas of keted and have yet to be produced in the quantities needed
California condor habitat. to replace lead. Currently, there are few satisfactory
Unfortunately, these legislative initiatives designed to replacements for lead in bullets, and more technological
protect wildlife are often met with resistance from industry innovation is sorely needed. The U.S. Department of De-
and sportsmen. Much of this opposition to proposed lead fense and NATO have funded investigations in this area.
bans results from a lack of communication between sci- Depleted uranium and tungsten have been shown to suit
entists and the public. For example, many sportsmen’s the forces generated in firearms and the ballistic qualities
groups such as the U.S. Sportsmen’s Alliance condemn desired, but both appear to have toxicologic drawbacks. A
attempts to prohibit lead as an infringement on their rights, bullet made of copper instead of lead (the Barnesâ bullet)
rather than a means to protect the health of people and is gaining popularity among hunters, but there is concern
wildlife. There is a misconception that lead prohibition over the toxicity of copper in aquatic habitats. There is also
laws are introduced by groups who oppose shooting and apprehension among sportsmen because nontoxic alterna-
fishing sports solely as a tactic to limit these activities. tives are a bit more costly than lead. Collaboration between
Inaccurate information such as this continues to plague the sportsmen, manufacturers, and researchers to develop
complete and successful transition to nontoxic hunting and more nontoxic alternatives that meet the sportsmen’s needs
fishing gear. Therefore, establishing an open dialogue be- is an important piece of a successful phase out. This
tween researchers, sportsmen, and policy makers is critical. cooperative approach allows sportsmen to play a positive
Strict legislation banning the use of lead hunting and role in efforts to eliminate the use of lead, and, in the end,
fishing gear that does not provide for the interests of is the key to a permanent solution.
sportsmen would result in ardent protest, low compliance,
and ultimately would fail to resolve the lead-poisoning issue.
To bring an end to the problem once and for all, scientists BREAKING DOWN THE BARRIERS
and health professionals must find ways to better collaborate
with hunting and fishing groups. We need to approach the The effects of lead poisoning are not confined to human
issue in a way that encourages people to take a proactive role health nor to any one species of animal. Thus, we will never
in eliminating this environmental crisis. Appealing to the successfully gain control of the problem unless we take an
conservationist roots of hunters and anglers is one way to do approach that is all-inclusive. We cannot continue to view
this. Many sportsmen are either unaware of the ecological the different aspects of plumbism in isolation from one
harm caused by the use of lead gear or are skeptical of claims other. Paint, gasoline, occupational exposure, toys, bullets,
that a seemingly insignificant bullet or fishing weight could fishing gear, and all the other sources of lead are not sep-
lead to such damaging effects for wildlife. It is therefore arate issues but rather are components of the same fun-
essential that we ramp up our efforts to reach out to damental problem.
sportsmen and educate them about the scientific rationale Developing strategies to achieve better integration
for moving away from lead, and to do so in a way that does among conservation and health disciplines will broaden our
not condemn their practices or their sport. scientific understanding of lead poisoning and accelerate
An important part of the answer is to identify nontoxic progress toward solutions. Currently, studies on lead poi-
materials that can substitute for lead in sporting gear and soning in people, wildlife, and domestic animals are all
encouraging sportsmen to adopt their use. The ban on the published separately in journals devoted to those specific
use of lead shot for hunting waterfowl brought about sig- fields. Establishing resources that include lead-poisoning
nificant innovation in the industry, and nontoxic alterna- literature from all domains will promote a better flow of ideas
tives are now widely accepted by sportsmen. It is essential and scientific knowledge between disciplines and allow
that we extend the ban on lead to all other sporting uses of researchers to see the interconnectedness of human and
lead shot. For the majority of fishing activities, there is a animal plumbism. Conferences and meetings that address
wide variety of nontoxic alternatives available (although multiple aspects of lead poisoning provide a prime oppor-
not yet as wide a variety as some anglers would like). tunity for researchers and action groups to network with
Although most alternatives are made of other metals, some experts in different disciplines. The EPA’s National Lead
ceramic and even natural rock sinkers have recently been Poisoning Prevention Week in October concentrates pri-
Mark A. Pokras and Michelle R. Kneeland

marily on childhood poisoning from lead paint, but would be thought provoking discussions, many people have contrib-
an ideal opportunity to spread public awareness and increase uted to the development of our thinking on this issue,
communication about any of the other issues associated with including: Joy Onasch, Harry Vogel, Rawson Wood,
lead poisoning. Bringing together a wide range of stake- Andrew Major; and Drs. Herbert Needleman, Ellen Silber-
holders to participate in the lead-poisoning dialogue will geld, Erica Miller, Milton Friend, Vernon Thomas, and J.
allow us to find solutions that are scientifically accurate, Christopher Franson. Our work has been supported in part
environmentally sound, economically viable, and socially by the Natural Areas Wildlife program of the New
acceptable. Hampshire Charitable Foundation.
An increasing number of organizations are now real-
izing the value of a conservation medicine-based approach
to the lead-poisoning issue and are making efforts to break REFERENCES
down disciplinary barriers. Several groups such as the
EPA’s Leadnet, The Lead Education and Abatement Design Annest JL, Pirkle JL, Makuc D, Neese JW, Bayse DD, Kovar MG
(1983) Chronological trend in blood lead levels between 1976
Group in Australia, and the Tufts Veterinary School’s Lead and 1980. New England Journal of Medicine 308:1373–1377
and Health group have formed listserves and contact dat- Bullard RD (editor) (1994) Unequal Protection: Environmental
abases to facilitate communications among people in di- Justice and Communities of Color, San Francisco: Sierra Club
Books
verse fields such as environmentalists, sportsmen,
Burger J, Gochfeld M (2005) Effects of lead on learning in herring
veterinarians, wildlife professionals, lead industry repre- gulls: an avian wildlife model for neurobehavioral deficits.
sentatives, citizen action groups, and environmental justice NeuroToxicology 26:615–624
groups. The Midwest Fish and Wildlife Conference held in Canfield RL, Henderson CR Jr, Cory-Slechta DA, Cox C, Jusko
TA, Lanphear BP (2003) Intellectual impairment in children
December 2007 included a session on lead poisoning that with blood lead concentrations below 10 microg per deciliter.
was attended by public health professionals, veterinarians, New England Journal of Medicine 348:1517–1526
wildlife biologists, sportsmen, and lead fishing tackle Centers for Disease Control and Prevention (2004) Childhood
lead poisoning from commercially manufactured French cera-
manufacturers. In addition, the Peregrine Fund is currently mic dinnerware—New York City, 2003. Morbidity and Mor-
working on their 2008 Lead Ammunition Conference that tality Weekly Report 53(26):584–586
will focus on implications for both human and animal Cohen AJ, Roe FJC (1991) Review of lead toxicology relevant to
the safety assessment of lead acetate as a hair colouring. Food
health. Finally, a session has been proposed for the Eco-
and Chemical Toxicology 29:485–507
Health II conference in December 2008 that would bring Fuortes L, Bauer E (2000) Lead contamination of imported candy
together a wide range of professionals to focus on lead and wrappers. Veterinary and Human Toxicology 42:41–42
its many health and environmental effects. Grinnell GB (1894) Lead poisoning. Forest and Stream 42:117–118
Grossman E (2006) High Tech Trash: Digital Devices, Hidden
Toxics, and Human Health, Washington, DC: Shearwater
CONCLUSION Guitart R, Serratosa J, Thomas VG (2002) Lead-poisoned
wildfowl in Spain: a significant threat for human consumers.
International Journal of Environmental Health Research 12:301–
Despite the fact that lead poisoning is well understood, it 309
still threatens the health of millions of people, domestic Hu H, Shih R, Rothenberg S, Schwartz BS (2007) The epidemi-
animals, and wildlife worldwide. Disciplinary barriers have ology of lead toxicity in adults: measuring dose and consider-
ation of other methodologic issues. Environmental Health
impeded the scientific understanding of lead toxicosis and
Perspectives 115:455–462
slowed policy initiatives to protect the health of animals Janssen DL, Oosterhuis JE, Allen JL, Anderson MP, Kelts DG,
and people. A conservation medicine-based approach Wiemeyer SN (1986) Lead poisoning in free-ranging California
focusing on increasing collaboration between professionals condors. Journal of the American Veterinary Medical Association
189:1115–1117
working in different fields offers the best hope for under-
Janssens E, Dauwe T, Van Duyse E, Beernaert J, Pinxten R, Eens M
standing and eliminating this ancient problem. (2003) Effects of heavy metal exposure on aggressive behavior in
a small territorial songbird. Archives of Environmental Con-
tamination and Toxicology 45:121–127
ACKNOWLEDGMENTS Johansen P, Pedersen HS, Asmund G, Riget F (2006) Lead shot
from hunting as a source of lead in human blood. Environ-
mental Pollution 142:93–97
We sincerely thank Dr. Joann Lindenmayer for her Koh TS (1985) Diagnosis of lead poisoning in dogs. Australian
constructive comments on this manuscript. With their Veterinary Journal 62:434
Transdisciplinary Approach to Lead Poisoning

Lanphear BP, Dietrich K, Auinger P, Cox C (2000) Cognitive Patrick L (2006) Lead toxicity, a review of the literature: part I:
deficits associated with blood lead concentrations <10 microg/ exposure, evaluation, and treatment. Alternative Medicine Re-
dL in US children and adolescents. Public Health Reports view 11:2–22
115:521–529 Pattee OH, Pain DJ (2003) Lead in the environment. In: Hand-
Li W, Han S, Gregg TR, Kemp FW, Davidow AL, Louria DB, et al. book of Ecotoxicology, Hoffman DJ, Rattner BA, Burton GA Jr,
(2003) Lead exposure potentiates predatory attack behavior in Cairns J Jr (editors), 2nd ed., New York: Lewis Publishers, pp
the cat. Environmental Research 92:197–206 373–408
Lynch RA, Boatright DT, Moss SK (2000) Lead-contaminated Pokras MA, Chafel RM (1992) Lead toxicosis from ingested
imported tamarind candy and children’s blood lead levels. fishing sinkers in adult common loons (Gavia immer) in New
Public Health Reports 115:537–543 England. Journal of Zoo and Wildlife Medicine 23:92–97
Mateo R, Cadenas R, Manez M, Guitart R (2001) Lead shot Sciarillo WG, Alexander G, Farrell KP (1992) Lead exposure and
ingestion in two raptor species from Doñana, Spain. Ecotoxi- child behavior. American Journal of Public Health 82:1356–1360
cology and Environmental Safety 48:6–10 Sicherman B (2003) Alice Hamilton: A Life in Letters, Urbana and
Needleman HL, Riess JA, Tobin MJ, Biesecker GE, Greenhouse JB Chicago: University of Illinois Press
(1996) Bone lead levels and delinquent behavior. Journal of the Sidor IF, Pokras MA, Major AR, Poppenga RH, Taylor KM, Mi-
American Medical Association 275:363–369 coni RM (2003) Mortality of common loons in New England,
Nevin R (2000) How lead exposure relates to temporal changes in 1987–2000. Journal of Wildlife Diseases 39:306–315
IQ, violent crime, and unwed pregnancy. Environmental Re- Sileo L, Fefer SI (1987) Paint chip poisoning of Laysan albatross at
search 83:1–22 Midway Atoll. Journal of Wildlife Diseases 23:432–437
Nriagu J (1983) Lead and Lead Poisoning in Antiquity, New York: Tanquerel des Planches L (1850) Lead Diseases: A Treatise, Boston:
Academic Press Tappan, Whittemore & Mason
Osweiler GD (1996) Toxicology, Philadelphia: Williams & Wilkins Thomas CW, Rising JL, Moore JK (1976) Blood lead concentra-
Pain DJ (1992) Lead poisoning of waterfowl: a review. In: Lead tions of children and dogs from 83 Illinois families. Journal of
Poisoning in Waterfowl, Special Publication No. 16, Pain DJ the American Veterinary Medical Association 169:1237–1240
(editor), Gloucester, UK: International Waterfowl and Wetlands
Research Bureau, Slimbridge

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