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Martineau et al. 2002. Cancer in wildlife: a case study. Beluga from the St. Lawrence Estuary. Environ. Health Perspect. 110(3): 285-292.

Cancer in Wildlife, a Case Study: Beluga from the St. Lawrence Estuary, Québec, Canada

Daniel Martineau,1 Karin Lemberger,1 André Dallaire,1 Philippe Labelle,1 Thomas P. Lipscomb,2 Pascal Michel,3 and Igor Mikaelian4

1Département de Pathologie et Microbiologie, Faculté de Médecine Vétérinaire, Université de Montréal, St. Hyacinthe, Québec, Canada; 2Department of Veterinary Pathology, Armed Forces Institute of Pathology, Washington, DC, USA; 3Faculté de Médecine Vétérinaire, Université de Montréal, St. Hyacinthe, Québec Canada; 4Idexx Veterinary Sciences, West Sacramento, California, USA

 

Abstract
A population of approximately 650 beluga (Delphinapterus leucas) inhabits a short segment of the St. Lawrence estuary (SLE). Over 17 years (1983-1999), we have examined 129 (or 49%) of 263 SLE beluga carcasses reported stranded. The major primary causes of death were respiratory and gastrointestinal infections with metazoan parasites (22%), cancer (18%), and bacterial, viral, and protozoan infections (17%). We observed cancer in 27% of examined adult animals found dead, a percentage similar to that found in humans. The estimated annual rate (AR) of all cancer types (163/100,000 animals) is much higher than that reported for any other population of cetacean and is similar to that of humans and to that of hospitalized cats and cattle. The AR of cancer of the proximal intestine, a minimum figure of 63 per 100,000 animals, is much higher than that observed in domestic animals and humans, except in sheep in certain parts of the world, where environmental contaminants are believed to be involved in the etiology of this condition. SLE beluga and their environment are contaminated by polycyclic aromatic hydrocarbons (PAHs) produced by the local aluminum smelters. The human population living in proximity of the SLE beluga habitat is affected by rates of cancer higher than those found in people in the rest of Québec and Canada, and some of these cancers have been epidemiologically related to PAHs. Considered with the above observations, the exposure of SLE beluga to PAHs and their contamination by these compounds are consistent with the hypothesis that PAHs are involved in the etiology of cancer in these animals. Key words: aluminum, beluga, cancer, cetaceans, pollution, polycyclic aromatic hydrocarbons, whale, wildlife. Environ Health Perspect 110:285-292 (2002). [Online 12 February 2002]

http://ehpnet1.niehs.nih.gov/docs/2002/110p285-292martineau/abstract.html

 

Address correspondence to D. Martineau, Département de Pathologie et Microbiologie, Faculté de Médecine Vétérinaire, Université de Montréal, St. Hyacinthe, Québec J2S 7C6 Canada. Telephone: (450) 773-8521. Fax: (450) 778-8113. E-mail: martinea@medvet.umontreal.ca

Incidence data were provided to Health Canada from the Canadian Cancer registry at Statistics Canada. We gratefully acknowledge the cooperation of the provincial and territorial cancer registries, which supply the data to Statistics Canada. We thank S. De Guise, S. Lair, R.J. Letcher, L. Measures, and R. Norstrom for helpful discussions. We thank R. Plante and C. Guimont (Filmar) for recovering and transporting carcasses to our facility over the last 15 years, all students who helped with postmortem examinations, and our colleagues at the FMV for their consistent support.

We acknowledge the help of the Centre Océanographique de Rimouski for logistic support, and the financial support of World Wildlife Fund Canada, Alcan, Fisheries and Oceans Canada, Fondation de la Faune du Québec, Société des Parcs du Québec, and NSERC.

Received 25 May 2001; accepted 20 September 2001.

Introduction

The St. Lawrence River estuary (SLE), Québec, Canada, receives the effluent from one of the most industrialized regions of the world (Figure 1). It is inhabited by the southernmost population of beluga (Delphinapterus leucas), a population unique in its accessibility to investigation and its geographic isolation from the Arctic habitat where the other populations of beluga are found. The SLE beluga population has dwindled from an estimated 5,000 to the current estimated 600-700 animals, in part because of the hunting pressure that continued until 1979 (1-3). Because of this dramatic decline, SLE belugas received the status of endangered species from the Canadian government in 1980 (3). Yet no solid data indicate population recovery. To explain this apparent failure to recover, we initiated a study in 1982 to carry out systematic postmortem examination of dead SLE beluga that drift ashore and to determine tissue levels of chemical contaminants.

 

Figure 1
Figure 1. Distribution of beluga in the SLE and incidence of standardized rate ratio for digestive system cancer in (A) men and (B) women in Québec.

Live and dead SLE beluga are heavily contaminated by agricultural and industrial contaminants such as heavy metals, polycyclic aromatic hydrocarbons (PAHs), and polychlorinated biphenyls (PCBs), dichlorodiphenyltrichloroethane (DDT), and their metabolites(4-8).

In this article we present an overview of the results of necropsies conducted over 17 years (1983-1999). The rate of cancer in the SLE beluga population is higher than in any other population of wild terrestrial or aquatic animals.

Materials and Methods

The public and officials of various government agencies reported carcasses found dead stranded on the shoreline, which were transported to the postmortem room of the Faculté de Médecine Vétérinaire de l'Université de Montréal, 500 km to the southwest, where pathologists assisted by veterinary students examined them upon arrival. Samples of all organs and lesions were preserved in neutral 10% buffered formalin; fixed tissues were embedded in paraffin, sectioned 5-7 µm thick, and routinely stained with hematoxylin-phloxin-saffron. Special stains were used when needed.

We submitted all tumors to the Department of Veterinary Pathology of the Armed Forces Institute of Pathology (AFIP; Washington, DC) for archiving in the Marine Mammal Database and/or for consultation purposes.

We determined the age of 190 carcasses by counting dentine growth layers on longitudinal section of teeth, using the standard of two growth layers per year (9).

The standardized rate ratio of digestive system cancer in both men and women in Québec takes into account the standardized rate ratio for each health unit in Québec (10). This ratio represents the number of new cases of cancer diagnosed and reported in the province of Québec during the specified time period (1989-1993) divided by the expected incidence over the same period. These ratios were represented geographically using Arcview version 3.2 (ESRI, Redlands, CA).

The Centre Hospitalier Universitaire de Québec provided all the human cancer epidemiologic data.

Results

Mortality. The study was initiated in September 1982, but in this review we include only complete years between 1983 and 1999. During this time period, 263 belugas were found dead, drifting, or stranded along the SLE shoreline. We examined 129 carcasses in the postmortem room. Of these, we considered 100 to be reasonably well preserved (77%) based on the firm consistency of the liver. Eighty of the relatively fresh 100 belugas (80%) were adult (> 7 years old).

To interpret the data presented here, the following observations must be considered. First, 51% (134 of 263) of stranded reported animals have not been necropsied, so the cause of death and lesions affecting these animals remain unknown. The number of animals stranded dead during winter is also unknown. In the spring, summer, and fall, carcasses with terminal diseases are often found after several days of rough weather, suggesting that the number of strandings occurring during winter is at least the same as that reported during the rest of the year, because of the harsh weather conditions prevailing in that season. Young calves (< 1 year) are difficult to find in the wild because of their small size and blue-gray color. Therefore, calf mortality is probably underestimated.

A mathematical model suggests that there are fewer live animals in the 21- to 25-year age group in the SLE population than in the northwest Alaska (NA) population (11,12). Yet stranded dead SLE beluga in that age group died in higher numbers; SLE beluga stranded dead had a mortality peak between 21 and 25 years (Figure 2) (13). In NA beluga, the estimated age-specific death rate per age class is highest in the 0-5 year group, decreases abruptly in the 6-10 year age group, and then decreases slowly until maximum life span (38 years). Thus, the age structure of SLE beluga dying of natural causes appears clearly different from that of NA beluga, principally because most SLE belugas die at an earlier age (between 21 and 25 years old).

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