Is Pollution Causing Cancer in Beluga Whales?

Photo: Marco Langlois. University of Montreal

This female beluga whale was found dead floating in the St. Lawrence near Tadoussac, Quebec. The head of her calf was visible at the external genital opening when the whale was submitted for postmortem.

The St. Lawrence River is so polluted, the New York State Department of Environmental Conservation warns people who fish the river off New York's shores not to eat any American eel, channel catfish, carp, Chinook salmon, lake trout over 25 inches in length, or brown trout over 20 inches in length. The department further warns that white perch, white sucker, rainbow trout, smaller lake and brown trout, and coho salmon over 25 inches taken from the river should be eaten, at most, only one time per month.

"The St. Lawrence itself is draining one-fourth of North America's most industrialized area, and the Great Lakes, which are in the center of this area, are connected to the St. Lawrence," notes veterinary pathologist Andre Dallaire of the University of Montreal. And living in the midst of this river, adjacent to Québec Province and approximately 120 miles northeast of Québec City, is a population of beluga (also called white) whales, Delphinapterus leucas. Beluga whales live in the Arctic Ocean and the rivers and bays adjacent to it.¹ Many of these populations are migratory and spend only part of the year in one area, but the belugas that live in the St. Lawrence Estuary don't go anywhere. "It's a population that doesn't move around a lot; they have inhabited the St. Lawrence River since the last glaciation age, in a geographical area [encompassing] the connection of the Saguenay River with the St. Lawrence. They will move within this territory depending on their age, sex, and the season," says Dallaire. The area is about 150 miles upstream from the mouth of the St. Lawrence. "They are stuck there since 10,000 years [ago]," veterinary pathologist Daniel Martineau of the University of Montreal tells The Scientist.

On his Web site (www.medvet.umontreal.ca/services/beluga/beluga_homepage.htm), Martineau explains that this area is unique. The cold Labrador current, which flows in a deep channel up the St. Lawrence, "hits a huge, almost vertical, underwater wall," resulting in a channel depth of only 10 meters, where the Saguenay River flows into the St. Lawrence. This cold water "creates a local Arctic marine environment," bringing nutrients up from the river's bottom and creating an area with abundant plankton, small invertebrates, and fish. The belugas concentrate in that area and do not leave it. But pollutants are concentrated there, too. Not only does the St. Lawrence drain industrial northeastern North America, but there is an aluminum plant at the base of the Saguenay, and the St. Lawrence drains some heavily agricultural land.

The St. Lawrence population of belugas numbered about 5,000 in the late 1800s,² but now, according to those studying them, about 650 remain. Dallaire, who does postmortem examinations on dead whales that wash up onshore or are found floating on the river, notes that each year, about 15-17 are found dead, "and usually, about half are in good-enough condition [not to be autolysed] to bring here so we can do a full postmortem to try to determine cause of death."

Belugas, also called white whales, typically grow to about 10 feet long.

In 1992, veterinary pathologists at the College of Veterinary Medicine of the University of Montreal, including Martineau, started doing postmortems on the beluga whales that were found dead in and around the St. Lawrence in an effort to determine why that whale population, which had recently been declared endangered by the Canadian government, had decreased so tremendously. What they saw surprised them. From 1983 to 1998, Martineau reports on his Web site, the group has examined 119 of 246 dead belugas from the St. Lawrence. Ninety-four of these were in a good-enough state of preservation for diagnosis. "Seventeen beluga [18 percent of preserved carcasses] died of cancer," states Martineau's Web site.

In 1999, the group necropsied nine belugas. Final histomorphological classification of the tumors that were seen in three of those animals is pending. In one animal, there "was a carcinoma. This malignant tumor was most likely of neuroendocrine origin because of the histological appearance of the neoplastic cells. This particular animal has generalized cancer. You had metastasis throughout the body," says Dallaire. "There was another case in which the whale had developed a thyroid gland neoplasm."

In discussing the cancers he's seen in the belugas, Dallaire states, "Different types of tumors have been described in that cetacean population: adenocarcinomas originating from the intestine, the mammary gland, the stomach, the uterus ... tumors affecting the reproductive organs, like the ovary or the tubular sensitalia. And the interesting thing is that there isn't a whale population anywhere in the world in which you've seen that many tumors."

The belugas not only had high rates of cancer. Veterinary pathologist Sylvain DeGuise of the University of Connecticut, Storrs, who began participating in the beluga necropsies while he was a veterinary student, explains that they also found animals who had opportunistic infections from only mildly pathogenic organisms, "almost like people with AIDS, who must encounter pathogens that don't cause very severe diseases; but since they cannot fight them, they end up causing big problems."

And in the St. Lawrence cancers are not confined to belugas. "Tumors have been diagnosed in mammalian, avian, and aquatic animal species, either wild or domestic," says Dallaire. The group has been studying liver cancer in lake whitefish or cisco, Coregonus clupeaformis, a member of the salmonid family. These fish feed on bottom-dwelling insects in the river. "There are more cancers in that area in humans, more than in the rest of Québec," Martineau tells The Scientist.

Toxic Legacy

The scientists believe that the cancers and opportunistic infections result from living in a contaminated environment. "This is a quite polluted area and we found high concentrations of toxic chemicals in the tissues of those animals," says DeGuise. He and members of the group have reported on heavy metals, organochlorines, polycyclic aromatic hydrocarbons (PAHs), and tributyltins (which, notes Martineau, are used in paints for hulls of large ships) in tissues of belugas.

"The next question is what's the relationship between toxic chemicals and lesions in these animals?" asks DeGuise. "PCBs (polychlorinated biphenyls) and DDT, among others [are] related to immune suppression. It is very well-known in laboratory animals that you can suppress the immune system. A suppressed immune system will allow for a wide variety of infections and cancers."

The question is how to determine if the chemicals to which the whales are exposed are creating immunosuppression in the animals, leaving them vulnerable to cancer induction and opportunistic infection. DeGuise notes, "It's very easy to put five mice in a cage and expose them to chemical A and five mice you don't expose." But studying chemical toxicity in beluga whales, which can weigh as much as 2,000 kiloggrams, demands what DeGuise calls a "more creative" approach.

He has taken lymphocytes from belugas held in captivity at aquariums, particularly those held at the Mystic Marinelife Aquarium in Mystic, Conn., and exposed them to chemicals found in the St. Lawrence environment. "Then I looked at the effect of exposure to chemicals they would find in their environment in vitro." They found that several of the chemicals had negative effects on the lymphocytes at concentration levels similar to those found in the St. Lawrence. "It is likely that the whales will encounter chemical concentrations that were high enough to suppress immune function, as we saw in vitro," states DeGuise.

"The next step was to look at mixtures of contaminants," he explains. "In real life, we're not exposed to [one chemical]; we're exposed to complex mixtures of chemicals. If chemical 1 at low exposure doesn't have an effect and chemical 2 doesn't have an effect, the question [is]: Do they act synergistically; do they oppose one another?" continues DeGuise.

"One of the projects we're doing right now in the lab is in different species of marine mammals to compare the sensitivity to a fairly wide area of mixture[s] of chemicals," explains DeGuise. "We're also comparing it to mice as a standard in order to decide if chemicals are safe or not. In preliminary results, we're finding that belugas appear to be more sensitive than mice to mixtures, and they also appear to be sensitive to different mixtures, which is quite scary because mice have been the species in which all the [toxicological] testing has been done." DeGuise is concerned that if these mixtures do not affect mice but they do affect beluga whales, what is the true effect of these chemicals in humans?

The researchers, however, have been unable to capture live St. Lawrence belugas to assess their immune systems. Without such cells, it is difficult to compare their immune cells to those used in DeGuise's assays, which usually come from whales from Arctic populations that spend time in the Churchill area of the Hudson Bay, an area that DeGuise says is much less contaminated than the St. Lawrence. The bulk of the belugas in captivity are from the Churchill population, according to DeGuise.

Additional Reading   S.J. Culp et al., "A comparison of the tumors induced by coal tar and benzo[a]pyrene in a 2-year bioassay," Carcinogenesis, 19[1]:117-24, 1998. S. DeGuise et al., "True hermaphroditism in a St. Lawrence beluga whale (Delphinapterus leucas)," Journal of Wildlife Diseases, 30[2]:287-90, 1994. L. Martel et al., "Polycyclic aromatic hydrocarbons in sediments from the Saguenay Fjord, Canada," Bulletin of Environmental Contamination and Toxicology, 37[1]:133-40, 1986. D. Martineau et al., "Pathology of cetaceans," in: Toxicology of Marine Mammals, ed. J.G Vos, G. Bossart, and M. Fournier. Washington, D.C., Taylor and Francis (in press). D. Martineau et al., "Cancer in beluga whales from the St. Lawrence Estuary, Quebec, Canada: A potential biomarker of environmental contamination," Journal of Cetacean Research and Management (Special Issue 1):249-65 (previously Reports of the International Whaling Commission), 1999. D. Martineau et al., "Pathology and toxicology of beluga whales from the St. Lawrence Estuary, Quebec, Canada. Past, present and future," Science of the Total Environment, 154[2-3]:201-15, 1994. D. Martineau et al., "Pathology of stranded beluga whales (Delphinapterus leucas) from the St. Lawrence Estuary, Quebec, Canada," Journal of Comparative Pathology, 98[3]:287-311, 1988. C. Tremblay et al., "Estimation of risk of developing bladder cancer among workers exposed to coal tar pitch volatiles in the primary aluminum industry," American Journal of Industrial Medicine, 27:335-48, 1995.

How to Prove It?

Despite all the evidence, some pathologists working in the field note the difficulty of proving that contaminants in the St. Lawrence are causing the cancers. "It certainly has drawn our attention and obvious concerns about the quality of that environment [in the St. Lawrence]," remarks David St. Aubin, marine mammal pathobiologist and director of research and veterinary services at Mystic Marinelife Aquarium. "The belugas that are examined there [in Montreal] tend to be older animals. They've reached the end of their lives for a number of reasons; disease tends to be a factor there." St. Aubin notes that in any cross section of an older population--even in humans--"you will see tumors."

"When you're looking at animals like this, wild animals, you have a couple of methodological problems," opines Daniel Cowan, a medical and comparative pathologist at the University of Texas Medical Branch in Galveston. Cowan, who states, "Diagnosing cancer is my business," has "a long-standing scientific interest in diseases of marine mammals." He mainly sees bottlenosed dolphins and recently described kidney tumors in animals he necropsied. He's also seen a leukemia lymphoproliferative disorder in a cetacean.

"One of the facts of life when you're dealing with whales and dolphins: they are protected, all of them, and you can't do experiments on them," notes Cowan. "You're left with seeing what comes up, as a gift of nature--an animal that's stranded on a beach that you find or someone finds before it's rotted." He says that the Canadians "have the dead animals; they have the point sources [of pollution]." The problem is relating the two.

"In some cases it may be particular combinations of compounds that have occurred in an individual whale that represent a unique cocktail, and trying to ascertain what that is and duplicate it, we certainly can't do it experimentally in a whale or a dolphin," remarks St. Aubin. He notes that it's even difficult to replicate these types of exposures in laboratory animals because they may have different sensitivities to different compounds and may even be refractory to the compounds.

Martineau explains to The Scientist that long-term studies on effects of such environmental pollutants "are very rarely done in mice because there is a high cost involved. These studies are not done because economically, it's not important."

Says St. Aubin: "You never want to discount the environmental influences. They certainly are there and we know we're dealing with an environment that's less than pristine in the St. Lawrence. When it comes down to that, proving that in court is very difficult. It's accepted [that the pollutants can cause cancer] in the scientific community, but there's a lot of smoking guns. We can use the burden of evidence as drawing attention to pollution as playing a role, but we don't have the ability, nor will we have the ability, to administer compound X to an animal and then wait and see a tumor."

"You have to be very circumspect in what you say," notes Cowan. "You have to be [sure that] what you're saying is scientifically correct and defensible."

But Martineau states on his Web site that from 1983-1998, the researchers found that 27 percent of the adult belugas they necropsied had cancers. "Such a high percentage had never been observed in any wild animal species, terrestrial or aquatic (with the important exception of fish)."

And St. Aubin, who looks at cetaceans stranded from waters of Long Island, Rhode Island, and Narragansett Bay--animals that are migratory and not year-round residents of the area--notes that it's "difficult to relate anything we find here to the specific environment. In the animals we have examined here, we have not seen a surprising incidence of tumors."

Martineau says he expects that in other freshwater cetaceans who are limited in their environment--the susus (Ganges and Indus dolphins) of India, the baiji or whitefin dolphin of the Chang Jiang (formerly called the Yangzi River) of China, and the boutos or Amazon dolphins of Brazil--"if somebody examines carcasses of these cetaceans, they might find cancer."

 

Myrna E. Watanabe is a freelance science writer in Patterson, N.Y.

1. R.M. Novak, Walker's Mammals of the World, 5^th Edit., Vol. II, Baltimore, Johns Hopkins University Press; 1991; pp. 1009-1010.