Photograph by Cyril Ruoso, Minden Pictures/SPI
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Crab-eating macaques, native to Southeast Asia, are commonly used for research, including in the 2014 diesel exhaust tests commissioned by an association funded by Volkswagen, BMW, and Daimler.

Photograph by Cyril Ruoso, Minden Pictures/SPI

Was Volkswagen the First to Test Exhaust Fumes on Monkeys? Your Questions Answered.

The car industry-funded research outraged the public and even has some researchers wondering how it was approved.

For four hours at a time, 10 crab-eating macaques sat inside airtight chambers watching cartoons while researchers piped in diluted exhaust from a new Volkswagen Beetle. A few weeks later the monkeys were back in the chambers, this time breathing in exhaust from an older Ford F-250. The monkeys were taking part in an experiment in the United States commissioned by German automakers in 2014, the details of which came to light in a New York Times story last week.

The aim of the tests, carried out by the New Mexico-based Lovelace Respiratory Research Institute, was to prove that more sophisticated filter technology had lessened the harmful effects of diesel engine exhaust, which was designated a cancer-causing pollutant by the World Health Organization (WHO) in 2012. But as it turned out, the research was rigged—the car Volkswagen provided for the experiment had been equipped with the now infamous cheating software installed on millions of cars worldwide that produced lower-than-normal emissions under test conditions.

The research was commissioned by an industry group funded by BMW, Daimler, and Volkswagen. Volkswagen has since apologized and pledged never to use animals in research again, and the company suspended an executive who admitted to failing to halt the tests. BMW and Daimler have taken action against their executives who were on the board of the industry group. A spokesperson for Lovelace said in an email that the institute did not know that the Volkswagen Beetle used in the tests was rigged, and when they found out, they decided not to publish the results of the experiment.

The macaque tests came to light in a deposition of Lovelace senior scientist Jacob McDonald, provided by lawyer Michael Melkerson who is representing Volkswagen buyers in a class-action lawsuit.

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Volkswagen provided a Beetle for use in the monkey lab tests to determine if the company’s new diesel technology had lesser health effects. Researchers at the lab say they were unaware the Beetle came equipped with the now infamous emissions cheating software.

Volkswagen’s reputation has yet to recover from the 2015 emissions cheating scandal, which cost billions of dollars and resulted in several prison sentences. On top of that it is now also contending with outrage from animal advocates and the public who say that using macaques as test subjects was cruel and unnecessary, especially because Volkswagen, by providing a car rigged with cheating software, was seemingly motivated by desire to sell more of their new diesel cars rather than to advance scientific understanding about the health effects of diesel exhaust. (Automakers are required by law to test their cars’ emissions levels but not the health effects of their cars’ emissions. Those tests are usually done by environmental scientists, not the industry.)

It’s not every day that dirty air tests are thrust into the spotlight. Wildlife Watch wanted to know: How are these tests usually performed? How often do they involve animals, and who oversees tests? And when do scientists think it makes sense to involve animals?

HOW COMMON IS IT TO TEST POLLUTED AIR ON MONKEYS?

This isn’t the first time monkeys have inhaled toxic fumes as part of an experiment to benefit humans. When the health risks and potential liability are too high for tests on humans, and when rodents aren’t susceptible to a chemical or aren’t appropriate models for extrapolating human health effects, scientists may turn to monkeys.

Some studies conducted to understand the impact of ozone, a major component of smog, have involved monkeys. In 2006, for example, scientists wanted to know how ozone affected inner-city children, so they used baby rhesus monkeys as test subjects “because their airway structure and postnatal lung development is similar to those of humans.”

And when researchers with the University of Washington wanted to understand better how methanol, an alternative to gasoline that can be toxic at high levels, may affect pregnant women and their newborn children, they exposed about four dozen crab-eating macaques to it. Researchers exposed four groups of 11-12 female monkeys to one of four different concentrations of methanol vapors for two-and-a-half hours a day, seven days in a row during several periods, including before breeding and during pregnancy.

Such examples notwithstanding, putting monkeys in the lab for air pollution tests “is definitely unusual,” says Christopher Carlsten, director of the Air Pollution Exposure Laboratory, at the University of British Columbia, in Canada.

Charles Plopper, a researcher at University of California, Davis, who has studied the effects of ozone on monkeys, agrees. “Experiments with nonhuman primates are not routine and are generally the result of extensive prior investigation” using rodents and sometimes human clinical trials he said in an email. When they are used, it's mostly to identify out the cause of a health problem and figure how best to treat or prevent it.

ETHICS AND ACCURACY OF MONKEY TESTS

Some animal advocates say it’s never ethical to test on animals for the benefit of humans. “Our position is that just because we humans can snatch animals away from their families, throw them into tiny cages, and perform every atrocity imaginable on these animals doesn’t mean that we have the right to do this,” says Alka Chandna, of the laboratory investigations department at People for the Ethical Treatment of Animals.

Eri Saikawa, who studies emissions and air pollution at Emory University, in Atlanta, Georgia, agrees that air pollution tests shouldn’t, and needn’t, be done on monkeys. She says it’s not logical to use animals to test effects on human health.

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Volkswagen CEO Mattihas Mueller (right) and the company’s head of external relations, Thomas Steg (left), leave the German Interior Ministry in August after a meeting of politicians and German automakers. Steg was suspended in connection with the scandal over the monkey research in January.

“If we want to understand health impacts on humans, there are so many different factors we have to think about in addition to just diesel,” Saikawa says. “Testing on animals I don’t think helps at all. I just don’t know how much we can learn from that and what we can infer.”

But some scientists believe it’s valid to test pollution on living beings when there’s a motivation to advance science and to learn something about human health. “What’s problematic, however, is a given study that’s not properly vetted, not properly conducted, motivated, or analyzed,” Carlsten says.

In the Lovelace deposition, McDonald said that the lab decided to test on macaques because it was too risky to use humans, given diesel’s designation by WHO as a carcinogen. But Carlsten and Saikawa question the motivations of the Lovelace experiment in general, not just the use of monkeys. “There are additional questions of legitimacy for any study that is funded by stakeholders with financial interest in the issue at hand,” Carlsten says.

ALTERNATIVES TO TESTING AIR POLLUTION EFFECTS ON MONKEYS

According to Saikawa, one way would simply be to compare the amount of emissions from the tailpipe of an older car to the emissions from their new diesel car.

But while that kind of experiment could show that the emissions are cleaner, it doesn’t prove that they’re less dangerous to human health, says Paul Locke, a Johns Hopkins environmental health scientist and attorney affiliated with the National Academies of Sciences’ Institute for Laboratory Animal Research and Johns Hopkins’ Center for Alternatives to Animal Testing.

So how can we demonstrate with certainty how humans are affected by pollution?

What's an Organ-on-a-Chip?

Some scientists, including Carlsten, favor testing on humans, despite the known risks of inhaling fumes from substances like diesel. A further complication is the appearance of exploitation: Studies like these offer a quick and easy way for needy people to make some cash. (The German automakers’ association also funded a human test in 2015 to study the effects of nitrogen dioxide that reportedly paid participants about $14 an hour.)

Carlsten emphasizes that people undergoing the tests are volunteers who give informed consent, and he says the exposure isn’t as bad as the public might imagine. The effects of these tests, he says, are similar to spending a couple of hours in a city like Beijing or Delhi, both known for their dirty air. And the experiments go through an independent review board to ensure that they’re ethical and truly contribute to scientific understanding.

Then there are artificial organs. Scientists have been developing “lungs on a chip” to use in drug and air pollution tests, including the PulMo at Los Alamos National Laboratory, in New Mexico. Pulak Nath, the scientist leading the project, says he’s hopeful that this kind of technology will reduce reliance on animal testing.

But no device will magically make animal testing unnecessary. Organs on a chip don’t have immune systems, and the interplay of toxins and the immune system is part of what can cause negative health effects.

WHO OVERSEES MONKEY TESTS?

Any institution in the U.S. that does testing on non-human primates is subject to the Animal Welfare Act, a federal law that regulates the treatment of lab animals, animals in zoos and circuses, and others. The law requires labs to have an Institutional Care and Animal Use Committee (IACUC), which is tasked with reviewing protocols, evaluating the care of lab animals, and conducting inspections. When researchers present a proposed test to the IACUC, they must explain, among other things, how they’ll minimize the pain and discomfort of animals.

Many people think this is similar to an institutional review board, which assesses proposed experiments using human subjects. But there’s one major difference: IACUCs are not required to evaluate the ethics and scientific merit of an experiment, Locke says.

When a public entity, such as a university, wants to test on animals, the National Institutes of Health (NIH), which provides at least some funding for nearly all academic research, decides whether there’s a legitimate and sufficient scientific reason to do so, Locke notes. Once the merit is established, NIH can grant funding, and then the research will be reviewed by an IACUC.

In privately funded research, no outside entity is required to consider merit. A Lovelace spokeswoman did not answer specific questions about the institute’s scientific review process but said in an email to Wildlife Watch that its IACUC “performed its function in full compliance with the Animal Welfare Act.”

That response leaves Locke wondering if there was any consideration of merit: “Lovelace has an excellent reputation. They’re known for doing quality science,” he says. But, he adds, “I don’t understand fully who reviewed this research from a scientific perspective. Who said this science was going to be valuable in terms of contributing knowledge to the world? Because that’s what science is supposed to do.”

Wildlife Watch is an investigative reporting project between National Geographic Society and National Geographic Partners focusing on wildlife crime and exploitation. Read more Wildlife Watch stories here, and learn more about National Geographic Society’s nonprofit mission at nationalgeographic.org . Send tips, feedback, and story ideas to ngwildlife@natgeo.com.