Cancer in Beluga: response. (Correspondence).

In their letter, Hammill et al. propose an analysis of mortality patterns for the St. Lawrence beluga (SLB) population without submitting data or methods. They state, however, that there is no difference in standing populations at 21-25 years of age between Alaskan beluga and SLB, supporting our conclusion that the high cancer rate in this age group cannot be explained by its overrepresentation in the SLB population (Martineau et al. 2002a). We have also shown in an earlier paper (Beland et al. 1988) and in an updated analysis (Beland et al. Unpublished data) that SLB do not die at a more advanced age than Arctic beluga. Hammill et al. suggest that the SLB population, the denominator used in estimating cancer rate, is larger than the value we used and thus the resulting cancer rate would be lower than that we obtained (Martineau et al. 2002b). We used 650, the population estimate that was both undisputed and published in a refereed scientific journal at that time (and still is) (Lesage and Kingsley 1998). Hammill et al. use a higher, recently developed correction factor of 2.09 to estimate the mean population size at 1,100. Importantly, Kingsley, a coauthor of the letter, previously stated that the mortality rate we used elsewhere, 1.4%, was unrealistically low (Kingsley 2002)--with which we concurred (Martineau 2002). Using a higher, more realistic annual 6% death rate from a population of 960, Kingsley (2002) estimated the SLB mortality rate at 58 deaths/year and derived an adjusted estimated annual rate (AAR) of 1,208, more than twice the AAR we estimated. (Using a population estimate of 1,100, he would have obtained an even higher AAR of 1,433.)

Our record includes emaciated individuals, a large number of young animals [22.4% of strandings were [less than or equal to] 6 years old (Beland et al. 1988)], and very few beach-cast animals that died over the winter. We assumed that the number of stranding occurring during winter is at least the same as that reported during the rest of the year (Martineau et al. 2002b). It is difficult to conceive that the ice cover and rough weather conditions which prevail in winter would lower mortality rates in animals that need to surface regularly for breathing, especially considering that SLB are often affected by pneumonia (Martineau et al. 1994). In addition, "carcasses with terminal diseases are often found after several days of rough weather" (Martineau et al. 2002b). Predation-induced mortality would muddle the issue, but predation seems not to be an important cause of mortality, as stated by Hammill et al.

Because the populations of pets used to determine cancer rates were exclusively animals examined in veterinary hospitals (Martineau et al 2002b; Priester and Mantel 1971; Priester and McKay 1980), many of these animals, if not most, were sick; thus, cancer rates are more frequent in these animals than in the general population of domestic animals--the same way that cancer patients are proportionally more numerous in a hospital than they are in the general human population (Priester and McKay 1980; Priester and Mantel 1971). In addition, most pet animals are sheltered and receive veterinary curative and preventive care along with abundant well-balanced food. Because cancer develops more frequently in older animals and humans, these factors, by prolonging life span, increase cancer rates relatively to free-ranging animals (Martineau et al 2002b; Fowler 1987).

The Saguenay River has been qualified as "extensively used" by SLB (Michaud 1993). SLB are grouped in three types of herds: adults and juveniles, only adults, and mixed herds. Among seven areas qualified as "extensively used" by SLB, the Saguenay River is one of only two areas frequented a substantial amount of time by the three types of herds. In addition, 5% of the population, on average, is found in the Saguenay River in the summer (Michaud 1993; Environnement Canada 1995). SLB are present in the Saguenay River, occasionally up to 100 km upstream, in the segment most contaminated by polycyclic aromatic hydrocarbons (PAHs) (Martel et al. 1986, 1987; Michaud 1993). Sainte-Marguerite Bay, located 24 km upstream the Saguenay River, is frequented daily by groups of SLB remaining in the bay up to 16 hr, probably for feeding (Michaud 1993). Benthic invertebrates are part of the diet of SLB, and benthic invertebrates are present in the Saguenay River (Lemieux 1996; Vladykov 1946). There is no reason to believe that SLB actively avoid these prey in the Saguenay River.

Mussels at the mouth of the Saguenay River accumulated PAHs produced by the local aluminum smelters, and clean mussels transplanted in the Saguenay River accumulated benzo[a]pyrene concentrations that were 200 times higher than pretransplantation concentrations, demonstrating that PAHs are also being exported into the St Lawrence Estuary (Cossa et al. 1983; Picard-Berube and Cossa 1983).

In conclusion, irrespective of uncertainties regarding population size, the percentage of mortality in SLB due to cancer is very high relative to other free-ranging mammals and to free-ranging cetaceans [for instance 2 of 90 dolphins (Cowan DF. Personal communication)] examined in similar conditions, and is higher than in pets and in humans [Figure 4 in Martineau et al 2002b] (Cowan et al. 1986; Howard et al. 1983; Kirkwood et al. 1997; Kuiken et al. 1993; Stroud and Roffe 1979). The contamination of the Saguenay River and immediate St. Lawrence estuary area by PAHs released massively by the local aluminum smelters over half a century and the exposure of belugas to these compounds make PAHs the most likely etiology for certain types of cancer in SLB as we stated in our article (Martineau et al. 2002b).

Daniel Martineau
Karin Lemberger
Andre Dallaire
Pascal Michel
Faculte de Medecine Veterinaire,
Departement de Pathologie et Microbiologie
Universite de Montreal
Montreal, Quebec, Canada
E-mail: [e-mail]
Pierre Beland
St. Lawrence National Institute of Ecotoxicology
Montreal, Quebec, Canada
Philippe Labelle
University of California-Davis
Veterinary Medical Teaching Hospital
Davis, California
Thomas P. Lipscomb
Department of Veterinary Pathology
Armed Forces Institute of Pathology
Washington, DC

REFERENCES

Beland P, Vezina A, Martineau D. 1988. Potential for growth of the St. Lawrence (Quebec, Canada) beluga whale (Delphinapterus leucas) population based on modelling. ICES J Mar Sci (J Conseil) 45:22-32.

Cossa D, Picard-Berube M, Gouygou J-P. 1983. Polynuclear aromatic hydrocarbons in mussels from the estuary and northwestern gulf of St. Lawrence, Canada. Bull Environ Contam Toxicol 31:41-47.

Cowan D, Walker WA, Brownell J. 1986. Pathology of small cetaceans stranded along Southern California beaches. In: Research on Dolphins (Bryden MM, Harrison R, eds). London:Oxford University Press, 323-367.

Environnement Canada region du Quebec, Conservation de l'environnement, Centre Saint-Laurent. 1995. Caracterisation du secteur du Saguenay. Bilan regional--Secteur du Saguenay. Zones d'intervention prioritaire 22 et 23 (Gagnon M, ed). Montreal, Quebec, Canada:Centre Saint-Laurent, Environnement Canada.

Fowler ME. 1987. Zoo animals and wildlife. In: Veterinary Cancer Medicine (Theilen GH, Madewell BR, ed's). Philadelphia:Lea & Febiger, 649-662.

Howard EB, Britt JO Jr, Simpson JG. 1983. Neoplasms in marine mammals. In: Pathobiology of marine mammal diseases (Howard EB, ed). Boca Raton FL:CRC Press, 95-162.

Kingsley MCS. 2002. Cancer rates in St Lawrence belugas; comment on Martineau et al. 1999, cancer in beluga whales, J Cetacean Res Manag. Special Issue 1:249-265 [Letter]. Mar Mamm Sci 18:572-574.

Kirkwood JK, Bennett PM, Jepson PD, Kuiken T, Simpson VR, Baker JR. 1997. Entanglement in fishing gear and other causes of death in cetaceans stranded on the coasts of England and Wales. Vet Rec 141:94-98.

Kuiken T, Hofle U, Benett PM, Allchin CR, Kirkwood JK, Baker JR, et al. 1993. Adrenocortical hyperplasia, disease and chlorihated hydrocarbons in the harbour porpoise (Phocoena phocoena). Mar Poll Bull 26:440-446.

Lemieux C. 1996. Acquisitions de connaissances des habitats cotiers de I'Anse Saint-Jean et de la Bale Sainte-Marguerite dans la region du Saguenay. Rapport du Groupe-Conseil Genivar Inc. [in French]. Quebec, Canada:Division de l'habitat du poisson, Ministere des Peches et Oceans Canada.

Lesage V, Kingsley MCS. 1998. Updated status of the St. Lawrence River population of the beluga, Delphinapterus leucas. Can Field Nat 112:98-113.

Martel L, Gagnon MJ, Masse R, Leclerc A, Tremblay L 1986. Polycyclic aromatic hydrocarbons in sediments from the Saguenay Fjord, Canada. Bull Environ Contam Toxicol 37:133-140.

Martel L, Gagnon MJ, Masse R, Leclerc A. 1987. The spatio-temporal variations and fluxes of polycyclic aromatic hydrocarbons in the sediments of the Saguenay Fjord, Quebec, Canada. Wat Res 21:699-707.

Martineau D. 2002. Reply to comments of Kingsley on Martineau et al. 1999. 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 1:249-265 [Letter]. Mar Mamm Sci 18:574-576.

Martineau D, De Guise S, Fournier M, Shugart L, Girard C, Lagace A, et al. 1994. Pathology and toxicology of beluga whales from the St. Lawrence Estuary, Quebec, Canada. Past, present and future. Sci Tot Environ 154:201-215.

Martineau D, Lemberger K, Dallaire A, Michel P, Beland P, Labelle P, et al. 2002a. St. Lawrence beluga whales, the river sweepers? [Letter]. Environ Health Perspect 110:A562-A564.

Martineau D, Lemberger K, Dallaire A, Labelle P, Lipscomb TP, Michel P, et al. 2002b. Cancer in wildlife, a case study: beluga from the St Lawrence Estuary, Quebec, Canada. Environ Health Perspect 110:285-292.

Michaud R. 1993. Distribution estivale du beluga du Saint-Laurent; synthese 1986 a 1992. Rapp Tech Can Sci Halieut Aquat 1906:1-22.

Picard-Berube M, Cossa DP, Piuze J. 1983. Teneurs en benzo 3,4 pyrene chez Mytilus edulis L. de l'estuaire et du Golfe du Saint-Laurent [in French]. Mar Environ Res 10:63-71.

Priester WA, Mantel N. 1971. Occurrence of tumors in domestic animals. Data from 12 United States and Canadian colleges of veterinary medicine. J Nat Cancer Inst 47:1333-1344.

Priester WA, McKay FW. 1980. The Occurrence of Tumors in Domestic Animals. Bethesda, MD:National Cancer Institute. Stroud RK, Roffe TJ. 1979. Causes of death in marine mammals stranded along the Oregon coast. J Wild Dis 15:91-97.

Vladykov VD. 1946. Etudes sur les mammiferes aquatiques IV. Nourriture du marsouin blanc ou beluga (Delphinapterus leucas) du fleuve Saint-Laurent [in French]. Quebec, Canada:Departement Pecheries du Quebec.