Banned

by Frederick Rowe Davis

  The development and deployment of DDT during World War II is a story of remarkable technological advancement. Employing techniques of toxicology, scientists conducted numerous tests of the new insecticide. Alongside the many reports of DDT’s spectacular success against numerous target insects, toxicology evaluations indicated relatively low toxicity in lab animals, field studies, and even humans. Enthusiastic accounts swamped concerns regarding threats to nontarget insects, the development of resistance, and uncertain chronic toxicity.

  The Toxicity Laboratory at the University of Chicago emerged as a major center for research and development in this new field study under Geiling’s deft leadership. The various research programs at the Tox Lab produced refined methods of toxicology, including the calculation of joint toxicity from the study of antimalarial drug therapies, the determination of toxicity of minute doses of drugs utilizing radioisotopes, and the calculation of LD50s for thousands of chemicals. Kenneth DuBois, in tandem with FDA researchers, developed the toxicological profile for some of the organophosphate insecticides, which caused cholinesterase inhibition in organisms, including humans, and could potentiate in combination with other pesticides from the class. With the possible exception of malathion, organophosphates as a class were among the most toxic of chemicals.

  As scientists at the Tox Lab and the FDA grappled with the new insecticides and developed new techniques, Congress began to consider the implications of the new chemicals for existing legislation. Congressional hearings explored the risks and benefits of pesticides, but the hearings were shrouded in the mists of scientific uncertainty. Repeatedly, committee members demanded a clear statement of the risks of DDT and were frustrated and angered as witness after witness failed to provide one. Nevertheless, Congress passed significant legislation in the form of FIFRA (1947), the Miller Amendment, and the Delaney Clause, which banned the use of cancer-causing agents in the production of foodstuffs. The aminotriazole cranberry scare in 1959 caused the FDA to apply the Delaney Clause and seize contaminated crops. Meanwhile, through the efforts of Tox Lab and FDA scientists, toxicology had begun to coalesce as an independent field of study and as a profession that, Geiling argued, should acknowledge its responsibility to the public.

  Despite Geiling’s ambitions for toxicologists, it was a science writer who publicized the problems pesticides presented for humans, wildlife, and ecosystems. In Silent Spring, published in 1962, Rachel Carson eloquently synthesized the research of toxicologists, ecologists, and doctors to portray the risks of indiscriminate use of insecticides. Many of her examples involved DDT and other chlorinated hydrocarbons, but she also noted the considerable risks associated with the use of organophosphates. Carson’s message reached millions of Americans when CBS aired a program dedicated to Silent Spring. Her book inspired further hearings when President Kennedy directed the PSAC to investigate effects of insecticides. Congressional hearings followed. Again, witnesses testified on the benefits and risks of pesticides. Carson herself distilled the message of Silent Spring into a call for specific research. As in other hearings, the committee listened to testimony from many experts regarding the toxicity of organophosphates, extrapolating what they could from the no-effect level and the multiyear process of bringing a new insecticide to market. However, these hearings did little to change pesticide legislation.

  Late in 1972, after extended litigation on several fronts, the EPA banned DDT and other chlorinated hydrocarbons. Banning the related compounds aldrin and dieldrin provided the first test cases of the recently passed FEPCA. Received wisdom marked the DDT ban as one of the great achievements of the environmental movement in the United States, and during the ensuing decades the gradual but pronounced recovery of populations of bald eagles, ospreys, peregrines, brown pelicans, and other wildlife confirmed the sense of accomplishment. The effects of DDT were pernicious, and banning the chemical in the U.S. mitigated risks to wildlife. But where would farmers turn when they could no longer spray DDT to control the insects that threatened their crops? DuBois, the Chicago toxicologist, worried that highly toxic organophosphates would become the insecticides of choice. In 1973, an English research lab synthesized pyrethroids, which were similar to the natural insecticide pyrethrum in chemical structure and insecticidal action. Synthetic pyrethroids combined high toxicity to insects with extremely low toxicity to mammals. But between 1966 and 1989, as DuBois had feared, organophosphates emerged as the most prolific insecticides deployed in American agriculture. Despite their high toxicity, organophosphates did not bioaccumulate in the environment, nor were they considered to be carcinogenic. Nevertheless, before 2006, when most uses of these insecticides were banned by the EPA, they caused thousands of poisonings among farm workers and huge mortality in wildlife inadvertently exposed. In the meantime, the University of Chicago Tox Lab scientists had dispersed to research universities, medical centers, and federal regulatory agencies. The roots laid down at the Tox Lab continue to feed the science of toxicology.

  The lessons from the story of pesticides and toxicology are many. First, as we have seen repeatedly, risk and benefit form a tight helix in the case of insecticides. The knowledge that insects carry disease and destroy crops neglects the considerable nuisance they create as we try to remake landscapes to exclude them. Human efforts to control insects almost certainly predate history, and natural insecticides like pyrethrum offered the promise of control, but with the introduction of heavy metal insecticides in the late nineteenth century, farmers, already in the process of expanding agriculture to an industrial scale, discovered what seemed to be a magic bullet. The many millions of pounds of lead arsenate deployed in agriculture before World War II provided a clear indication that farmers had wholly embraced synthetic insecticides. During and after the war, DDT offered an apparently safer option with no obvious drawbacks, especially when compared with the far more toxic organophosphates, which were developed and introduced in the same time frame. Early testing, though extensive, failed to detect the most pernicious of the effects associated with DDT: namely, concentration in organisms and the environment resulting in endocrine disruption, particularly in topline predators, such as bald eagles, peregrines, ospreys, and brown pelicans. The risks of organophosphates, however, were absolutely clear to toxicologists shortly after the novel toxins arrived at the Tox Lab and the FDA.

  The second lesson is that there is a danger of focusing on any particular element of toxicity in weighing the risks and benefits of insecticides. DDT handily replaced the arsenates because it destroyed insects without the obvious toxicity of lead and arsenic and without damaging crops. In Silent Spring, Carson revealed the considerable dangers of chlorinated hydrocarbons and organophosphates. DDT and chlorinated hydrocarbons accumulated in ecosystems and organisms; the highly toxic organophosphates killed outright. If pressed, as she was during congressional hearings, Carson would have recommended further research into the effects of all pesticides, and she would have strongly urged reducing dependence on all chemical insecticides, certainly chlorinated hydrocarbons and organophosphates. The fact that organophosphates did not bioaccumulate would not offset the extraordinary risks they posed to humans and wildlife, a point that DuBois stressed. Recent studies revealing cognitive effects associated with prenatal exposures to organophosphates as well as possible endocrine effects serve to underscore this point.

  Third, pesticides do not offer simple solutions. Replacing arsenates with DDT did not completely solve the problems created by arsenates. The unintended consequences of banning DDT continue to reverberate in agriculture and public health in America and throughout the world. The toxicologists and other scientists in this story have indicated that the toxicology of insecticides and other chemicals is complex. Solutions require a comparable sophistication. The several court cases that challenged USDA’s DDT spraying campaigns signaled the need for further regulation of DDT. Comprehensive regulation would have taken organophosphates into account as well. Instead, most organophosphates remained in use for
another thirty years with hundreds of millions of pounds in annual agricultural applications. Surely, the dominance of organophosphates in agriculture represents one of the most tragic ironies of the DDT ban.

  But we still have not answered the obvious question: namely, why did highly toxic organophosphates replace chlorinated hydrocarbons in American agriculture? In Silent Spring, Carson seemed prescient in that she addressed risks of both chlorinated hydrocarbons and organophosphates, but, as I have shown, in developing her case Carson drew on the research and testimony of the toxicologists. Over the course of many hearings, Congress heard testimony regarding the toxicity of the organophosphates.

  DDT was similar to the arsenates that preceded it for its persistence in the environment. Regulation proceeded along similar lines. By the early 1970s, there were thousands of products containing DDT, which had not been a proprietary pesticide since its release after World War II. Banning DDT did not place a burden on any one chemical company in the way that banning a proprietary pesticide would have. Most, if not all, of the organophosphates were proprietary, which is to say individual chemicals were associated with specific chemical companies. Put more simply, in the aftermath of the DDT ban, the chemical companies producing proprietary organophosphates realized significant profits. Ironically, under FEPCA chemical companies demanded indemnification for stocks of pesticides banned under the legislation.

  During the DDT era, environmental toxicology relied on two key measures to determine the relative safety of pesticides: carcinogenicity and environmental persistence. In the case of organophosphates, with such low LD50s (high toxicities), carcinogenic and reproductive effects were obscured by symptoms of acute toxicity, such as convulsions, paralysis, and even death. Only recently have scientists tracked reproductive and neurological effects of low dose exposures to organophosphates. Organophosphates decompose rapidly in most environmental systems and thus slipped through the regulatory screens put in place by FIFRA and FEPCA, which focused on imminent hazard to humans and the environment and focused on restricting carcinogens and persistent pollutants. Again, recent studies have revealed the harmful effects of organophosphates in cognitive development and endocrine disruption. This research revealed significant gaps in pesticide legislation.

  When Carson referred to certain pesticides as “biocides” she certainly had organophosphates in mind. Recall that when scientists synthesized pyrethroids, they compared their toxicity to parathion, one of the most toxic pesticides (to all organisms). Since their development as nerve gasses during World War II, scientists were well aware of the toxicity of organophosphates to all organisms. Toxicologists at the Tox Lab and the FDA provided a clear picture of toxicity of organophosphates as cholinesterase inhibitors. In Silent Spring, Carson animated the dangers that organophosphates posed to wildlife and agriculture laborers. Numerous witnesses testified to the toxicity of organophosphates in hearings held at the state and federal level, particularly during PSAC and subsequent congressional hearings. Few classes of chemicals provided such a clear and consistent picture of extreme risk as the organophosphates (with malathion a notable exception).

  Despite Carson’s careful account and thoughtful recommendations, legislators, regulators, and the public focused more narrowly on the persistent chlorinated hydrocarbons in the aftermath of Silent Spring. Note the parallel with the regulation of the pesticides that preceded DDT, the arsenates, which were also pollutants that bioaccumulated in the environment. The ban on DDT in 1972 left farmers in search of a technological fix for the problem of insect infestations, which led them to the organophosphates, with the guidance of the USDA and the chemical industry. Although scientists developed synthetic pyrethroids shortly after the ban, their commercial development lagged and they remained prohibitively expensive.

  My attempt to understand the development of pesticides and toxicology through the sources to Silent Spring has revealed the tragic irony of legislation and pesticide use in the aftermath of the book’s publication. Along with a generation of toxicologists, Carson and her careful readers knew that the organophosphates posed an equivalent (and potentially greater) risk to humans and wildlife. Yet most of the organophosphates remained on the market and dominated agricultural pesticide applications in the United States until the EPA completed its comprehensive review in 2006. To this day, organophosphates are among the most widely used pesticides in the world, with tragic consequences for farm workers, children, and wildlife populations alike.

  Epilogue

  Risk, Benefit, and Uncertainty

  Even before the EPA began its review of the organophosphates, a new class of insecticides had joined the ranks of agricultural insecticides. Since the 1950s, scientists have attempted to synthesize compounds like the naturally occurring insecticide nicotine. Izuru Yamamoto at the Tokyo University of Agriculture coined the term “nicotinoid” for nicotine and related insecticidal compounds. Chemists first synthesized promising nicotinoids during the 1970s, but the initial compounds were unstable in light and thus unviable for development as insecticides. Agricultural chemists working with support from Bayer and Shell successfully developed and patented several “neonicotinoids,” also Yamamoto’s term, during the 1980s and 1990s. As a class, neonicitinoid insecticides showed promise as systemic insecticides that would be taken up by crops like some of the organophosphates.1 Toxicological analysis showed that the new insecticides were highly toxic to insects and minimally toxic to mammals. For example the LD50 in rats for imidacloprid (IMI) was 450 mg/kg, thiacloprid: 640 mg/kg, and clothianidin: > 5,000 mg/kg. However, both imidacloprid and thiacloprid indicated much lower LD50s for birds: 31 and 49 mg/kg, respectively.2

  Agricultural usage of neonicitinoids expanded as they became more widely available, but use exploded when the EPA cancelled the registrations of many of the organophosphates. In 2013, neonicotinoids surpassed organophosphates as the most widely used insecticides in the world. Scientists at the American Bird Conservancy recently argued that such widespread usage may spell disaster for birds, particularly those species that favor open grasslands.3 Like chlorinated hydrocarbons, neonicintinoids persist in soil. They can accumulate in the environment over time. Toxicities to birds compare with the toxicity of organophosphates. And birds are not alone in their vulnerability to neonicitinoids: bees have shown considerable susceptibility to the new insecticides.4 In addition, there are concerns that neonicitinoids will contaminate groundwater.5

  Even though neonicitinoids represent a new class of pesticide, or at least a recently synthesized form of an existing chemical (nicotine), their widespread proliferation in agriculture across America and throughout the world seems eerily familiar. Once again, a fog of scientific uncertainty surrounds the most widely used agricultural insecticides in the world. Neonicitinoids account for one-quarter of insecticides used worldwide, with an estimated value of $2.5 billion. The EPA has deemed the neonicitinoid insecticides safe. Yet more and more scientists worry that these chemicals are responsible for ecological disruption and the destruction of populations of birds, bees, and aquatic organisms. Such risks have prompted action on the part of the European Commission, which announced that it would restrict the use of three neonicitinoids (clothianidin, IMI, and thiametoxam) for a period of two years commencing December 1, 2013. Although the EPA reached scientific conclusions similar to those of the European Food Safety Authority regarding the potential for acute effects and uncertainty about chronic risk, it has not elected to restrict use of the neonicitinoids. Although the EPA is currently reviewing the neonicitinoids, for the time being the agency has accepted industry claims that the benefits of the new insecticides significantly outweigh the risks.6

  It would be foolish to overdraw comparisons between the past and present, yet the similarities speak to our discussion of risk, benefit, and uncertainty. When Rachel Carson penned Silent Spring, both organochlorines and organophosphates were widely used in agriculture. Yet uncertainty clouded both science and policy. In a stroke of genius, Car
son assembled a range of scientific and anecdotal sources into an impassioned call for reflection on the part of legislators and the public as well as for further investigation by toxicologists and environmental scientists. Establishing the EPA, the ban on DDT, and the passage of FEPCA all served as critical steps in the management of risk. Despite these and other developments, organophosphate use surged in the decades that followed.

  Contrary to Carson’s clarion call for reduction in the use of all insecticides, the ban on DDT and other organochlorines initiated a risk-risk trade-off in which agribusiness replaced DDT and the persistent organochlorines with highly toxic organophosphates, like parathion, that threaten the welfare of humans and wildlife despite relatively rapid disintegration in the environment. When Congress enacted FQPA, the EPA launched its comprehensive review of the organophosphates and carbamates, and U.S. restrictions on many of them followed. Nevertheless, neonicitinoids provided agribusiness with substitutes, albeit ones that may contaminate ecosystems and threaten nontarget organisms, including bees and birds. Initial assessments suggest that neonicitinoids pose lower risks to humans and other mammals than the organophosphates and carbamates. As regulators review these chemicals and the risks they pose to ecosystems and wildlife, we should look to Silent Spring and a century of pesticides and toxicology for models with which to evaluate novel risks.