During the mid-1970s, a Canadian Wildlife Service researcher discovered that birds in Lake Ontario were behaving in a bizarre way: unable to find mates, pairs of female herring gulls were nesting together and devotedly tending clutches of eggs that usually turned out to be infertile. Glen Fox, then in his early 30s and based in Hull, Que., wondered whether pollutants, including such now-banned chemicals as PCBs and DDT, were mimicking the effects of hormones and crippling the male birds' reproductive systems. That would explain why the male gulls were losing interest in sex, forcing desperate females to set up nest keeping together. Subsequent research showed that Fox's suspicions were correct - raising the question of whether manmade chemicals could have a similar effect on humans. Yes, say Fox and other scientists. In fact, they believe that it may already be happening - that widely used chemicals may be infiltrating fetuses and skewing sexual development in male babies. If true, that could explain a troubling decline in sperm counts that has been reported in some countries. "Whether or not this is what's going on," says Fox, "we just don't know yet for sure. But the potential is too big to ignore."
Does that mean still another environmental scare for a world beset by the greenhouse effect, the vanishing ozone layer and emerging killer viruses like Ebola? Maybe. The hypothesis is unproven and controversial. There are scientists who question both parts of the theory: that widespread declines in sperm counts are occurring and, even if they are, that manmade chemicals are necessarily to blame. But proponents insist that chemicals found in pesticides and herbicides, in plastics, cosmetics, paints, detergents and many other products, can impersonate hormones and could seriously compromise human fertility in the 21st century. And now adherents of that theory have a manifesto: Our Stolen Future, a new book that documents the way chemicals have ravaged some animal species by damaging their reproductive, nervous and immune systems - and argues that the same thing could be happening to humans. "We know that there are chemicals out there that can do this," says co-author Theo Colborn, a senior scientist with the Washington-based World Wildlife Fund. "There is more than enough evidence to be concerned."
There is no telling whether Our Stolen Future - written with journalist Dianne Dumanoski and zoologist John Peterson Myers - will eventually attain the same milestone stature as Silent Spring, Rachel Carson's 1962 book that sounded an early alarm over pesticides and the environment. But U.S. Vice-President Al Gore thinks it may: in a forward to the book, Gore says that Our Stolen Future "raises urgent and compelling questions that must be addressed." Some experts go further, arguing that to be on the safe side, governments should start banning suspect chemicals. "We don't know yet whether we have a horrendous problem or not," says Dr. Ana Soto, a medical researcher at Tufts University medical school in Boston. "But some of us wonder what the consequences might be if it takes too long to find out." Even chemical industry spokesmen concede that the issue requires investigation. "We're deeply troubled by the sweeping assertions that are being made," says Eric Alexander, a spokesman for the Ottawa-based Canadian Chemical Producers Association. "And we realize we're in an era where we can't just say, 'Trust us.' But scientists have an obligation to verify the facts."
Reproductive capability is not the only worry. Hormone-mimicking chemicals can disrupt other parts of the human endocrine system - the network of organs that send chemical messengers through the bloodstream to control cellular activity and bodily functions. There is already some evidence to suggest that estrogen-like substances can affect the cognitive development of babies. And some experts think that estrogen-like chemicals may be partly responsible for the soaring incidence of breast cancer in women.
But the most immediate mystery centres on sperm, the tiny, tadpole-like organisms that cause pregnancy by fertilizing a woman's egg. Sperm is measured in millions per millilitre. Canadian doctors regard about 30 million/mL to 100 million/mL as the norm, with most men ejaculating about three millilitres each time. In 1992, fertility experts were stunned when Danish researchers published an analysis of 61 studies involving nearly 15,000 men in the United States, Europe, Asia, Africa and other parts of the world. They concluded that, over a 50-year period, average sperm counts had plummeted by 42 per cent - from a global average of 113 million/mL in 1940 to only 66 million/mL in 1990.
The Danish study came under attack from critics who questioned its methodology, citing changes in sperm-measurement over the years and the scarcity of information about how some of the earlier studies were conducted. But a French report three years later appeared to support the Danish findings. Examining records at a Paris sperm bank, the French researchers charted a 33-per-cent drop in sperm counts - from an average of 89 million/mL in 1973 to 60 million/mL in 1992. And a study of Scottish men published in February found a similar rate of decline.
Though there are no up-to-date Canadian statistics, some experts think that a decline may be under way. Dr. Alfonso Del Valle, medical director of ReproMed Ltd., a Toronto sperm bank, says that there is some evidence pointing towards a "trend for decline" over the past 30 years. Del Valle compared data gathered by his eight-year-old firm with records from an affiliate in Minneapolis that has been banking sperm since 1970. Sperm counts in individual men tend to vary, says Del Valle, and the output of donors at the Toronto clinic now fluctuate at slightly lower levels than they did a generation ago in Minneapolis - for example, between 70 and 90 million/mL instead of between 80 and 100 million/mL. "I think there is something happening," concludes Del Valle.
If sperm counts are indeed declining, there is so far no hard evidence to show that manmade chemicals are the cause. Experts say that many factors, including smoking, alcohol and drug use, stress, and venereal diseases can affect sperm production. Even tight underwear and the long hours many men spend sitting at office desks have been blamed: they overheat the testicles, which can cause sperm to die.
But some experts argue there are plausible reasons for thinking that manmade chemicals could be harming sperm production. Even though doctors increasingly are prescribing estrogen supplements for menopausal women, they would never do that for younger women who want to have children. The reason: too much estrogen in a mother's system can upset the hormonal interplay that triggers a male fetus's sexual development. In the early stages of pregnancy, the hormone testosterone plays a crucial role by signalling cells to start developing male sexual and reproductive attributes. And many experts say that if even tiny amounts of estrogenic chemicals - or others that have the ability to block testosterone - breach the fetal barrier during the critical period, they can upset that process and cause serious damage.
One result could be chemical interference with the development of a group of cells in the testicles - know as Sertoli cells - which control future sperm production. The same chemicals might be responsible for higher rates of testicular cancer, undescended testicles and malformed penises that have been reported in some countries. "We're talking about chemicals that can build up in us over time and do an end run around the body's defences," says Colborn. "And we know that some of these chemicals can affect the developing embryo."
Some of the first evidence that chemicals could damage reproductive systems emerged from the animal kingdom. During the 1970s and 1980s, researchers in North America and Europe increasingly found that hormone-mimicking chemicals were upsetting the neurological, immune and reproductive systems in animal species. Among the grotesque results: cormorants with beaks so badly twisted they had difficulty eating, fish and turtles with deformed or bisexual organs. In one of the most dramatic cases of reproductive failure, scientists studying the dwindling alligator population in central Florida's Lake Apopka - the scene of a massive spill of DDT-laced chemicals in 1980 - found that male alligators had high levels of female hormones. The majority of alligator eggs failed to hatch, and the baby male alligators that were born had abnormally small penises.
As the wildlife evidence grew, researchers began to wonder if something similar could be happening to humans. In fact, medical researchers already had persuasive evidence that exposing pregnant women to estrogen-like substances could have disastrous effects on their offspring. Starting in the late 1940s, doctors in North and South America began widely prescribing a synthetic estrogen called DES to pregnant women to prevent miscarriages. Daughters born to women who used DES often suffered from reduced fertility and rare forms of cancer; among their sons, there were reports of low sperm counts, undescended testicles and other problems. A May, 1993, article in the influential British medical journal The Lancet cited the DES evidence and suggested that numerous chemicals in the environment capable of behaving like by-then-banned DES might be responsible for the apparent decline in sperm counts.
As suspicions of a possible link mounted, researchers identified a growing number of chemicals that seem to possess the ability to imitate hormones. The list of suspects now includes the large family of chlorine-based substances, including DDT and other pesticides and PCBs - which were all banned during the 1970s but persist in the environment or, like DDT, are still used in developing nations. Also implicated are dioxins and furans, the toxic byproducts of some industrial processes (including bleaching in some pulp-and-paper mills), forest fires and other combustion; a group of chemicals called phthalates, which are used to give plastics flexibility and are found in paints, inks, adhesives, paper and cardboard used in food packaging; and alkyl phenols, chemicals that result from the breakdown of ingredients in detergents, cosmetics, spermicides and other household products.
But there is still no proof that these chemicals are harming humans. Even Richard M. Sharpe, a British scientist who has played a leading role pointing to a possible connection between manmade chemicals and reproductive problems, urges caution. "I think it is a plausible hypothesis that estrogenic chemicals may be causing a decline in sperm counts," says Sharpe, a senior scientist at the British Medical Research Council's reproductive biology unit in Edinburgh. "But we are still very much at the bottom of the learning curve on this. I think a lot of people have overreacted and are treating the hypothesis as being more definite than it is."
Other scientists are deeply skeptical of the hypothesis. Stephen Safe, a Belleville, Ont.-born toxicologist who teaches at Texas A & M University in College Station, points out that many vegetables, including soya beans, broccoli, spinach and cabbage, are rich in natural substances that can mimic estrogen. "Most of the suspect chemicals," says Safe, "are only weakly estrogenic and they are found in the environment in tiny amounts. They might play some role in falling sperm production. But to blame the whole thing on estrogenic chemicals - I just don't see it."
In fact, the concern over manmade hormone imitators has begun to stir debate over natural estrogens. Some scientists maintain that phytoestrogens, as they are called, may actually pose a greater risk than the synthetic variety. As evidence of this, scientists say that once trees have been reduced to pulp in mills, they release natural estrogenic compounds that are suspected of causing some of the deformities in Great Lakes fish previously blamed solely on dioxin-laced pulp-mill effluents. Because some phytoestrogens are more potent and enter the human body in greater quantities, says Keith Solomon, head of the University of Guelph's toxicology centre, "I think we should be much more concerned about them than the synthetic ones." But experts who think that synthetic estrogens are a much bigger threat note that the human body rapidly breaks down and excretes phytoestrogens, while the synthetic ones survive much longer and can build up in body fat.
While the debate over estrogenic chemicals percolates, researchers are trying to find out more about what may be driving down sperm counts. In Ottawa, Warren Foster, head of reproductive toxicology at Health Canada, is overseeing a one-year study that will test sperm concentrations in at least 500 men across Canada and compare the results with earlier data. And in Quebec City, Pierre Ayotte, a Laval University toxicologist, is studying two groups of young men. Those in one group have low sperm counts, and Ayotte is trying to determine whether they also have high "body burdens" of PCBs, DDT and other known estrogenic chemicals.
At the same time, Dr. Eric Dewailly, a Laval environmental medicine specialist, is investigating the effects that similar chemicals may be having on children in Quebec fishing communities along the St. Lawrence River's North Shore. The fishermen and their families have a diet rich in fish and seabird eggs that contain such air- and water-borne contaminants as dioxins, PCBs and DDT. "We know that the blood and breast milk of people in the area have high levels of contaminants," says Dewailly, "and we want to see whether this affects the sexual maturation of males." Pediatricians in the area report no unusual problems in boys born there, says Dewailly. "The effects," he adds, "may be more subtle."
In Edinburgh, Sharpe is conducting animal studies to try to find out more about events in early pregnancy that could affect an unborn boy's future sperm-producing potential. "We're trying to understand which genes and which hormones are involved," he says, "and the way adverse influences might come into play." Sharpe thinks that environmental estrogens are a possible source of trouble. But there could be others, including cigarette-smoking mothers. "I am aware of some unpublished studies," says Sharpe, "that suggest smoking could be a factor."
With so much uncertainty, regulatory agencies are just beginning to evaluate the suspected endocrine-disrupters. Officials at Ottawa's environmental health protectorate are currently investigating a number of chemicals, including a phthalate used in floor coverings, hair spray, perfumes and other products. In Washington, Environmental Protection Agency officials say that they are working on the development of new screening methods aimed at detecting endocrine disrupters. According to Dr. Lynn Goldman, the EPA administrator responsible for pesticides and toxic substances, the chemicals high on the list for review include the pesticide endosulfan and bisphenol-A, a component in plastics used in such products as drinking-water bottles.
The problem, says Health Canada's Foster, is that identifying chemical culprits that may act subtly over time, or only in combination with other substances, is a lot harder than zeroing in on ones that are clearly life-threatening. "And we have to put it in context," adds Foster. "Every day, we get out of bed and do things that carry risk - driving on highways or smoking cigarettes. How do these suspect chemicals compare to cigarette smoking in terms of their potential to affect human health? We really don't know." That is just one of the questions that has to be answered as researchers investigate whether chemicals - manmade and pervasive - are imperilling the very stuff of human life.
Maclean's April 1, 1996