Silent Spring was one of the most influential books of the twentieth century. Its author, fisheries biologist Rachel Carson, warned that pesticides were destroying wildlife, that DDT in particular appeared to be exterminating shorebird populations, and that pesticides were becoming a staple of the American diet. For this she was reviled by the agricultural chemicals industry and called a fanatic, a Communist, and worse (see Lear 1998; Orlando 2002; Stouder 2012). But subsequent research (Frye 1995) bore out Carson’s claims and revealed the first evidence of endocrine disruption due to exposure to environmental chemicals.
The chemical components of DDT (dichloro-diphenyl-trichloroethane; Figure 1A) cannot be broken down and eliminated by vertebrate organisms; DDT remains in their bodies and builds up, becoming especially concentrated in organisms that feed on the DDT-containing tissues of other animals. This persistence, along with its solubility in lipids, results in tremendous bioaccumulation such that even though DDT has not been legally used in the United States since 1972, most of us have this chemical in our bodies. Indeed, it is so resistant to metabolic degradation, and so much was manufactured, that it remains not only in humans and other terrestrial animals but also in fishes, marine mammals, and seabirds. It has an environmental half-life of about 15 years, which means it can take 100 years or more for the concentration of DDT in the soil to fall below active levels.
Bioaccumulation of DDT was especially pronounced in some birds of prey living at the top of the food chain. Peregrine falcons and bald eagles became endangered because of DDT-induced fragility of their eggshells (Cooke 1973). Even seabirds were affected when DDT in runoff accumulated in the fish they fed on. Fragile eggshells resulted in high mortality as the developing bird embryos became desiccated, were easily preyed upon, and often were not able to withstand even minor physical forces (Figure 1B).
Discovering why DDT contamination results in thin eggshells was a formidable research challenge. It turns out that DDT acts as an estrogenic compound (see the next section), while its chief metabolic product, DDE (which lacks one of DDT’s chlorine atoms), inhibits androgens such as testosterone from binding to the androgen receptor (Davis et al. 1993; Kelce et al. 1995; Xu et al. 2006). Eggshell thinning is caused by several actions of DDT and DDE. Hens with high DDT levels have poorly developed shell glands, with capillaries deficient in carbonic anhydrase—an enzyme critical for the deposition of shell-strengthening calcium carbonate in the egg (Holm et al. 2006). High DDE levels in the shell gland also prevent calcium carbonate deposition by down-regulating the synthesis of prostaglandins (a group of fatty acid derivatives that regulate many vertebrate physiological processes). In birds, one of these prostaglandins is critical for the transport of calcium ions through the shell gland for use in shell formation (Lundholm 1997; Guillette 2006).
DDT use has been banned in the United States since 1972 and is also banned in most of Europe. The Stockholm Convention of 2001, which attempts a worldwide ban on the use of several dangerously persistent organic chemicals, limits the use of DDT to the control of disease-carrying insects (notably mosquitoes), and only in those countries where there is no affordable and/or comparably effective alternative for managing a serious public health threat (primarily malaria). As a result of the ban, levels of DDT in the birds diminished, and the bird population began recovering (Grier 1982; Newton and Wyllie 1992).
Despite these bans and limits, DDT is still having marked effects. It is still used extensively in tropical regions for growing exportable foods. With the globalization of our food supply, DDT continues to enter the U.S. food chain through imported fruits and vegetables and other products (Stutchbury 2008). Moreover, the spraying of DDT to grow exported foods in South America has been linked to the large decline in migratory songbirds (Stutchbury 2008, 2009).
Banning DDT turned out to be an excellent idea for reasons beyond eggshell fragility and wildlife endangerment. What wasn’t known in 1972 was that women who had been exposed to DDT before age 14 would have a greater than fivefold increase in their incidence of breast cancers later in life (Figure 6.2). Using a remarkable database of American patients studied for over 50 years, Cohn (2011) concluded that DDT exposure after adolescence might not lead to major health risks; but exposure to this endocrine disruptor in utero or at an early age can make a person susceptible to breast cancer later in life. We will see this type of effect in our discussions of BPA later in the chapter.
1. This idea that early exposure to an agent might predispose one to having cancers later in life also appears in the studies of breast cancer in the atomic bomb survivors of Hiroshima and Nagasaki. The part of that population most at risk comprised the women under the age of 20 at the time of the bombing (Ronckers et al. 2005).