Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-10T12:39:26.316Z Has data issue: false hasContentIssue false
  • English
  • Français

Neoplastic diseases of commercially important marine bivalves

Published online by Cambridge University Press:  15 December 2004

Bruce J. Barber
Bruce J. Barber*
Affiliation:
Eckerd College, Galbraith Marine Science Laboratory, 4200 54th Ave. South, St. Petersburg, FL 33711, USA
*
barberbj@eckerd.edu
Get access

Abstract

This review summarizes the current state of knowledge regarding the two primary proliferative diseases of commercially important marine bivalves. Disseminated neoplasia is characterized by the presence of large (2−4 times the diameter of normal hemocytes), anaplastic, circulating cells that have a hyperchromatic and often pleomorphic nucleus containing one or more prominent nucleoli. Prevalence exceeding 90% has been reported; the disease is progressive and can result in significant mortality of affected populations. Softshell clams, Mya arenaria, and mussels, Mytilus trossulus, from the east and west coasts of North America, respectively, and cockles, Cerastoderma edule, from Ireland, appear to be especially susceptible. Disseminated neoplasia can be transmitted to uninfected individuals, indicating an infectious (perhaps viral) etiology, the expression of which may be aggravated by environmental degradation. Gonadal neoplasia consists of small, basophilic, undifferentiated cells that originate as small foci in gonadal follicles where they proliferate and eventually invade surrounding tissues. This disease primarily affects M. arenaria in Maine (USA) and Mercenaria spp. in Florida (USA) at prevalences up to 50%. Most affected individuals are female. Limited field studies to date indicate that the disease progresses slowly and mortality rates are low. The major impact is most likely a reduction in reproductive effort. The finding that prevalence of gonadal neoplasia is higher in hybrid Mercenaria spp. suggests a genetic etiology. Precise determination of the etiology and other aspects of both diseases will benefit greatly from future advances in cellular and molecular biological techniques.

Keywords

NeoplasiaBivalvesMolluscs
Type
Research Article
Information
Aquatic Living Resources , Volume 17 , Issue 4: Bivalve Diseases , October 2004 , pp. 449 - 466
Copyright
© EDP Sciences, IFREMER, IRD, 2004

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alderman, D.J., Van Banning, P., Perez-Colomer, A., 1977, Two European oyster (Ostrea edulis) mortalities associated with an abnormal haemocytic condition. Aquaculture 10, 335-340. CrossRef
Arnold, W.S., Bert, T.M., Hesselman, D.M., Blake, N.J., 1996, Gonadal neoplasia in hard clams (Mercenaria spp.) from the Indian River Lagoon, Florida. J. Shellfish Res. 15, 518.
Auffret, M., Poder, M., 1986, Sarcomatous lesion in the cockle Cerastoderma edule II. Electron microscopical study. Aquaculture 58, 9-15.
Balouet G., Poder M., 1980, A proposal for classification of normal and neoplastic types of blood cells in molluscs. In: Yohn, Lapin Blakeslee (Eds.), Advances in Comparative Leukemia Research 1979. Elsevier North Holland, Inc., pp. 205-208.
Balouet, G., Poder, M., Cahour, A., Auffret, M., 1986, Proliferative hemocytic condition in European flat oysters (Ostrea edulis) from Breton coasts: a 6-year survey. J. Invertebr. Pathol. 48, 208-215. CrossRef
Barber B.J., 1990, Seasonal prevalence and intensity and disease progression of neoplasia in soft shell clams, Mya arenaria, from the Shrewsbury River, New Jersey. In: Perkins F.O., Cheng T.C. (Eds.), Pathology in Marine Science. Academic Press, Inc., San Diego, pp. 377-386.
Barber, B.J., 1995, Seasonal prevalence of gonadal neoplasms in clams, Mya arenaria, in Maine and impact on oogenesis. J. Shellfish Res. 14, 238.
Barber, B.J., 1996, Effects of gonadal neoplasms on oogenesis in softshell clams, Mya arenaria. J. Invertebr. Pathol. 67, 161-168. CrossRef
Barber, B.J., Davis, C.V., 1994, Disease studies in Maine-1993. J. Shellfish Res. 13, 311.
Barber, B.J., Davis, C.V., Crosby, M.A., 1998, Cultured oysters, Crassostrea virginica, genetically selected for fast growth in the Damariscotta River, Maine, are resistant to mortality caused by Juvenile Oyster Disease (JOD). J. Shellfish Res. 17, 1171-1175.
Barber, B.J., MacCallum, G.S., Robinson, S.M.C., McGladdery, S.E., 2002, Occurrence and lack of transmissibility of gonadal neoplasia in softshell clams, Mya arenaria, in Maine (USA) and Atlantic Canada. Aquat. Living Resour. 15, 319-326. CrossRef
Barry, M., Yevich, P.P., 1975, Part III. Histopathological studies. Mar. Pollut. Bull. 6, 171-173. CrossRef
Barry, M.M., Yevich, P.P., 1972, Incidence of gonadal cancer in the quahaug. Oncology 26, 87-96. CrossRef
Bert, T.M., Hesselman, D.M., Arnold, W.S., Moore, W.S., Cruz-Lopez, H., Marelli, D.C., 1993, High frequency of gonadal neoplasia in a hard clam (Mercenaria spp.) hybrid zone. Mar. Biol. 117, 97-104. CrossRef
Bower, S.M., McGladdery, S.E., Price, I.M., 1994, Synopsis of infectious diseases and parasites of commercially exploited shellfish. Annu. Rev. Fish Dis. 4, 1-199. CrossRef
Brousseau, D.J., 1987, Seasonal aspects of sarcomatous neoplasia in Mya arenaria (soft-shell clam) from Long Island Sound. J. Invertebr. Pathol. 50, 269-276. CrossRef
Brousseau, D.J., Baglivo, J.A., 1991a, Field and laboratory comparisons of mortality in normal and neoplastic Mya arenaria. J. Invertebr. Pathol. 57, 59-65. CrossRef
Brousseau, D.J., Baglivo, J.A., 1991b, Disease progression and mortality in neoplastic Mya arenaria in the field. Mar. Biol. 110, 249-252. CrossRef
Brousseau, D.J., Baglivo, J.A., 1994, Notes on epizootiological aspects (sex and age) of disseminated neoplasia in Mya arenaria from Long Island Sound. J. Invertebr. Pathol. 63, 214-216. CrossRef
Brown, R.S., 1980, The value of the multidisciplinary approach to research on marine pollution effects as evidenced in a three-year study to determine the etiology and pathogenesis of neoplasia in the soft-shell clam, Mya arenaria. J. Conseil 179, 125-128.
Brown, R.S., Wolke, R.E., Saila, S.B., Brown, C.W., 1977, Prevalence of neoplasia in 10 New England populations of the soft-shell clam (Mya arenaria). Ann. NY Acad. Sci. 298, 522-534. CrossRef
Cooper, K.R., Brown, R.S., Chang, P.W., 1982a, The course and mortality of a hematopoietic neoplasm in the soft-shell clam, Mya arenaria. J. Invertebr. Pathol. 39, 149-157. CrossRef
Cooper, K.R., Brown, R.S., Chang, P.W., 1982b, Accuracy of blood cytological screening techniques for the diagnosis of a possible hematopoeitic neoplasm in the bivalve mollusc, Mya arenaria. J. Invertebr. Pathol. 39, 281-289. CrossRef
Cosson-Mannevy, M.A., Wong, C.S., Cretney, W.J., 1984, Putative neoplastic disorders in mussels (Mytilus edulis) from southern Vancouver Island waters, British Columbia. J. Invertebr. Pathol. 44, 151-160. CrossRef
Elston, R.A., Kent, M.L., Drum, A.S., 1988a, Progression, lethality and remission of hemic neoplasia in the bay mussel Mytilus edulis. Dis. Aquat. Org. 4, 135-142. CrossRef
Elston, R.A., Kent, M.L., Drum, A.S., 1988b, Transmission of hemic neoplasia in the bay mussel, Mytilus edulis, using whole cells and cell homogenate. Dev. Comp. Immunol. 12, 719-727. CrossRef
Elston, R.A., Drum, A.S., Allen, S.K Jr., 1990, Progressive development of circulating polyploid cells in Mytilus with hemic neoplasia. Dis. Aquat. Org. 8, 51-59. CrossRef
Elston, R.A., Moore, J.D., Brooks, K., 1992, Disseminated neoplasia of bivalve molluscs. Rev. Aquat. Sci. 6, 405-466.
Eversole, A.G., Heffernan, P.B., 1995, Gonadal neoplasia in northern Mercenaria mercenaria (Linnaeus, 1758) and southern M. campechiensis (Gmelin, 1791) quahogs and their hybrids cultured in South Carolina. J. Shellfish Res. 14, 33-39.
Farley, C.A., 1969a, Probable neoplastic disease of the hematopoietic system in oysters, Crassostrea virginica and Crassostrea gigas. Nat. Cancer Inst. Monogr. 31, 541-555.
Farley, C.A., 1969b, Sarcomatoid proliferative disease in a wild population of blue mussels (Mytilus edulis). J. Natl. Cancer Inst. 43, 509-516.
Farley, C.A., 1976, Proliferative disorders in bivalve molluscs. Mar. Fish. Rev. 38, 30-33.
Farley, C.A., 1978, Viruses and viruslike lesions in marine mollusks. Mar. Fish. Rev. 40, 18-20.
Farley C.A., 1994, Exogenous viruses as possible initiators of neoplasms in aquatic invertebrates. In: Rosenfield A., Kern F.G., Keller B.J. (Eds.), Invertebrate Neoplasia: Initiation and Promotion Mechanisms. U.S. Department of Commerce, Woods Hole, MA, pp. 26-27.
Farley, C.A., Otto, S.V., Reinisch, C.L., 1986, New occurrence of epizootic sarcoma in Chesapeake Bay soft shell clams, Mya arenaria. Fish. Bull. 84, 851-857.
Farley, C.A., Plutschak, D.L., Scott, R.F., 1991, Epizootiology and distribution of transmissible sarcoma in Maryland softshell clams, Mya arenaria, 1984-1988. Environ. Health Perspect. 90, 35-41. CrossRef
Ford, S.E., Haskin, H.H., 1987, Infection and mortality patterns in strains of oysters Crassostrea virginica selected for resistance to the parasite Haplosporidium nelsoni (MSX). J. Parasitol. 73, 368-376. CrossRef
Ford, S.E., Barber, R.D., Marks, E., 1997, Disseminated neoplasia in juvenile eastern oysters Crassostrea virginica, and its relationship to the reproductive cycle. Dis. Aquat. Org. 28, 73-77. CrossRef
Frierman, E.M., Andrews, J.D., 1976, Occurrence of hematopoietic neoplasms in Virginia oysters (Crassostrea virginica). J. Natl. Cancer Inst. 56, 319-322. CrossRef
Gardner, G.R., Yevich, P.P., Hurst, J., Thayer, P., Benyi, S., Harshbarger, J.C., Pruell, R.J., 1991, Germinomas and teratoid siphon anomalies in softshell clams, Mya arenaria, environmentally exposed to herbicides. Environ. Health Perspect. 90, 43-51. CrossRef
Green, M., Alderman, D.J., 1983, Neoplasia in Mytilus edulis L. from United Kingdom waters. Aquaculture 30, 1-10. CrossRef
Harshbarger, J.C., Otto, S.V., Chang, S.C., 1979, Proliferative disorders in Crassostrea virginica and Mya arenaria from the Chesapeake Bay and intranuclear virus-like inclusions in Mya arenaria with germinomas from a Maine oil spill site. Haliotis 8, 243-248.
Hesselman, D.M., Blake, N.J., Peters, E.C., 1988, Gonadal neoplasms in hard shell clams Mercenaria spp., from the Indian River, Florida: Occurrence, prevalence, and histopathology. J. Invertebr. Pathol. 52, 436-446. CrossRef
Hesselman, D.M., Barber, B.J., Blake, N.J., 1989, The reproductive cycle of adult hard clams, Mercenaria spp. in the Indian River Lagoon, Florida. J. Shellfish Res. 8, 43-49.
Hillman, R.E., 1993, Relationship of environmental contaminants to occurrence of neoplasia in Mytilus edulis populations from east and west coast mussel-watch sites. J. Shellfish Res. 12, 109.
House, M.L., Kim, C.H., Reno, P.W., 1998, Soft shell clams Mya arenaria with disseminated neoplasia demonstrate reverse transcriptase activity. Dis. Aquat. Org. 34, 187-192. CrossRef
Kelley, M.L., Winge, P., Heaney, J.D., Stephens, R.E., Farell, J.H., Van Beneden, R.J., Reinisch, C.L., Lesser, M.P., Walker, C.L., 2001, Expression of homologues for p53 and p73 in the softshell clam (Mya arenaria), a naturally-occurring model for human cancer. Oncogene 20, 748-758. CrossRef
Kent, M.L., Elston, R.A., Wilkinson, M.T., Drum, A.S., 1989, Impaired defense mechanisms in bay mussels, Mytilus edulis, with hemic neoplasia. J. Invertebr. Pathol. 53, 378-386. CrossRef
Kent, M.L., Wilkinson, M.T., Drum, A.S., Elston, R.A., 1991, Failure of transmission of hemic neoplasia of bay mussels, Mytilus trossulus, to other bivalve species. J. Invertebr. Pathol. 57, 435-436. CrossRef
Koehn, R.K., 1991, The genetics and taxonomy of the species in the genus Mytilus. Aquaculture 94, 125-145. CrossRef
Krishnakumar, P.K., Casillas, E., Snider, R.G., Kagley, A.N., Varanasi, U., 1999, Environmental contaminants and the prevalence of hemic neoplasia (leukemia) in the common mussel (Mytilus edulis complex) from Puget Sound, Washington, USA J. Invertebr. Pathol. 73, 135-146. CrossRef
La Peyre, J., Li, Y., Buchanan, J., Cheng, P., Cooper, R., Tiersch, T., 2001, A systematic approach to develop an oyster cell line. J. Shellfish Res. 20, 546-547.
Landsberg, J.H., 1996, Neoplasia and biotoxins in bivalves: is there a connection? J. Shellfish Res. 15, 203-230.
Leavitt, D.F., McDowell Capuzzo, J., Smolowitz, R.M., Miosky, D.L., Lancaster, B.A., 1990, Hematopoietic neoplasia in Mya arenaria: prevalence and indices of physiological condition. Mar. Biol. 105, 313-321. CrossRef
Leavitt D.F., Miosky Dragos D., Lancaster B.A., Craig A.C., Reinisch C.L., Capuzzo J.M., 1994, Initiation and promotion of hematopoietic neoplasia in softshells, Mya arenaria, exposed to natural sediment. In: Rosenfield A., Kern F.G., Keller B.J. (Eds.), Invertebrate Neoplasia: Initiation and Promotion Mechanisms. U.S. Department of Commerce, Woods Hole, MA, pp. 23-25.
Lowe, D.M., Moore, M.N., 1978, Cytological and quantitative cytochemistry of a proliferative atypical hemocytic condition in Mytilus edulis (Bivalvia, Mollusca). J. Natl. Cancer Inst. 60, 1455-1459. CrossRef
McGladdery, S.E., Reinisch, C.L., MacCallum, G.S., Stephens, R.E., Walker, C.L., Davidson, J.T., 2001, Haemic neoplasia in soft-shell clams (Mya arenaria): Recent outbreaks in Atlantic Canada and discovery of a p53 gene homologue associated with the condition. Bull. Aquac. Assoc. Can. 101-3, 19-26.
McLaughlin S.M., 1994, Transmission studies of sarcoma in the softshell, Mya arenaria. In: Rosenfield A., Kern F.G., Keller B.J. (Eds.), Invertebrate Neoplasia: Initiation and Promotion Mechanisms. U.S. Department of Commerce, Woods Hole, MA, pp. 21-22.
Medina, D.J., Paquette, G.E., Sadasiv, E.C., Chang, P.W., 1993, Isolation of infectious particles having reverse transcriptase activity and producing hematopoietic neoplasia in Mya arenaria. J. Shellfish Res. 12, 112-113.
Miosky, D.L., Smolowitz, R.M., Reinisch, C.L., 1989, Leukemia cell specific protein of the bivalve mollusc Mya arenaria. J. Invertebr. Pathol. 53, 32-40. CrossRef
Mix, M.C., 1975, Proliferative characteristics of atypical cells in native oysters (Ostrea lurida) from Yaquina Bay, Oregon. J. Invertebr. Pathol. 26, 289-298. CrossRef
Mix, M.C., 1983, Haemic neoplasms of bay mussels, Mytilus edulis L., from Oregon: occurrence, prevalence, seasonality and histopathological progression. J. Fish Dis. 6, 239-248. CrossRef
Mix, M.C., 1986, Cancerous diseases in aquatic animals and their association with environmental pollutants: A critical literature review. Mar. Environ. Res. 20, 1-141. CrossRef
Mix, M.C., Hawkes, J.W., Sparks, A.K., 1979, Observations on the ultrastructure of large cells associated with putative neoplastic disorders of mussels, Mytilus edulis, from Yaquina Bay, Oregon. J. Invertebr. Pathol. 34, 41-56. CrossRef
Moore, J.D., Elston, R.A., 1993, Pathogenesis of disseminated neoplasia in eastern Pacific Mytilus trossulus. J. Shellfish Res. 12, 136.
Moore, J.D., Elston, R.A., Drum, A.S., Wilkinson, M.T., 1991, Alternate pathogenesis of systemic neoplasia in the bivalve mollusc Mytilus. J. Invertebr. Pathol. 58, 231-243. CrossRef
Morcillo, Y., Porte, C., 2000, Evidence of endocrine disruption in clams-Ruditapes decussata-transplanted to a tributyltin-polluted environment. Environ. Pollut. 107, 47-52. CrossRef
Morrison, C.M., Moore, A.R., Marryatt, V.M., Scarratt, D.J., 1993, Disseminated sarcomas of soft-shell clams, Mya arenaria Linnaeus 1758, from sites in Nova Scotia and New Brunswick. J. Shellfish Res. 12, 65-69.
Noel, D., Boulo, V., Chagot, D., Mialhe, E., Paolucci, F., Clavies, C., Hervaud, E., Elston, R.A., 1991, Preparation and characterization of monoclonal antibodies against neoplastic hemocytes of Mytilus edulis (Bivalvia). Dis. Aquat. Org. 10, 51-58. CrossRef
Oberdorster, E., Cheek, O., 2001, Gender benders at the beach: Encocrine disruption in marine and estuarine organisms. Environ. Toxicol. Chem. 20, 23-36. CrossRef
Oprandy, J.J., Chang, P.W., 1983, 5-Bromodeoxyuridine induction of hematopoietic neoplasia and retrovirus activation in the soft-shell clam, Mya arenaria. J. Invertebr. Pathol. 42, 196-206. CrossRef
Oprandy, J.J., Chang, P.W., Pronovost, A.D., Cooper, K.R., Brown, C.W., Yates, V.J., 1981, Isolation of a viral agent causing hematopoietic neoplasia in the soft-shell clam, Mya arenaria. J. Invertebr. Pathol. 38, 45-51. CrossRef
Pauley, G.B., 1969, A critical review of neoplasias and tumor-like lesions in mollusks. Nat. Cancer Inst. Monogr. 31, 509-529.
Peters, E.C., 1988, Recent investigations on the disseminated sarcomas of marine bivalve molluscs. Am. Fish. Soc. Spec. Publ. 18, 74-92.
Peters, E.C., Yevich, P.P., Harshbarger, J.C., Zaroogian, G.E., 1994, Comparative histology of gonadal neoplasms in marine bivalve molluscs. Dis. Aquat. Org. 20, 59-76. CrossRef
Poder, M., Auffret, M., 1986, Sarcomatous lesion in the cockle Cerastoderma edule I. Morphology and population survey in Brittany, France. Aquaculture 58, 1-8. CrossRef
Potts M.-S., 1993, Effects of Hematopoietic Neoplasia on Physiological Processes in the Soft-shell Clam, Mya arenaria (Linne.). Ph.D. Dissertation, University of New Hampshire, pp. 150.
Rasmussen, L.P.D., 1986, Occurrence, prevalence and seasonality of neoplasia in the marine mussel Mytilus edulis from three sites in Denmark. Mar. Biol. 92, 59-64. CrossRef
Reinisch, C.L., Charles, A.M., Stone, A.M., 1984, Epizootic neoplasia in soft shell clams collected from New Bedford Harbor. Hazard. Waste 1, 73-81. CrossRef
Reno, P.W., House, M., Illingworth, A., 1994, Flow cytometric and chromosome analysis of softshell clams, Mya arenaria, with disseminated neoplasia. J. Invertebr. Pathol. 64, 163-172. CrossRef
Sindermann C.J., 1990, Principal Diseases of Marine Fish and Shellfish. Academic Press, Inc., San Diego.
Smolowitz, R.M., Leavitt, D.F., 1996, Neoplasia and other pollution associated lesions in Mya arenaria from Boston Harbor. J. Shellfish Res. 15, 520.
Smolowitz, R.M., Reinisch, C.L., 1986, Indirect peroxidase staining using monoclonal antibodies specific for Mya arenaria neoplastic cells. J. Invertebr. Pathol. 48, 139-145. CrossRef
Smolowitz, R.M., Miosky, D., Reinisch, C.L., 1989, Ontogeny of leukemic cells of the soft shell clam. J. Invertebr. Pathol. 53, 41-51. CrossRef
Sparks A.K., 1985, Synopsis of Invertebrate Pathology Exclusive of Insects. Elsevier, Amsterdam.
Sunila, I., 1991, Respiration of sarcoma cells from the soft-shell clam Mya arenaria L. under various conditions. J. Exp. Mar. Biol. Ecol. 150, 19-29. CrossRef
Sunila, I., 1992, Serum-cell interactions in transmission of sarcoma in the soft shell clam, Mya arenaria L. Comp. Biochem. Physiol. A 102, 727-730. CrossRef
Sunila I., 1994, Viral transmission and tumor promotion of sarcoma in the softshell, Mya arenaria. In: Rosenfield A., Kern F.G., Keller B.J. (Eds.), Invertebrate Neoplasia: Initiation and Promotion Mechanisms. U.S. Department of Commerce, Woods Hole, MA, pp. 11-13.
Sunila, I., Dungan, C.F., 1992, Different proteins in the hemolymph sera from sarcomatous and healthy soft shell clams, Mya arenaria L. Comp. Biochem. Physiol. B 102, 621-625. CrossRef
Twomey E., 1994, Distribution of sarcoma in the cockle, Cerastoderma edule, around the Irish Coast, 1982-91: Implications for pollution etiology. In: Rosenfield A., Kern F.G., Keller B.J. (Eds.), Invertebrate Neoplasia: Initiation and Promotion Mechanisms. U.S. Department of Commerce, Woods Hole, MA, pp. 3-5.
Twomey, E., Mulcahy, M.F., 1988a, Epizootiological aspects of a sarcoma in the cockle Cerastoderma edule. Dis. Aquat. Org. 5, 225-238. CrossRef
Twomey, E., Mulcahy, M.F., 1988b, Transmission of a sarcoma in the cockle Cerastoderma edule (Bivalvia; Mollusca) using cell transplants. Dev. Comp. Immunol. 12, 195-200. CrossRef
Van Beneden, R.J., Rhodes, L.D., Gardner, G.R., 1998, Studies of the molecular basis of gonadal tumors in the marine bivalve, Mya arenaria. Mar. Environ. Res. 46, 209-213. CrossRef
Van Beneden, R.J., Gardner, G.R., Blake, N.J., Blair, D.G., 1993, Implications for the presence of transforming genes in gonadal tumors in two bivalve mollusk species. Cancer Res. 53, 2976-2979.
Villalba, A., Carballal, M.J., Lopez, C., 2001, Disseminated neoplasia and large foci indicating heavy haemocytic infiltration in cockles Cerastoderma edule from Galicia (NW Spain). Dis. Aquat. Org. 46, 213-216. CrossRef
Weinberg, J.R., Leavitt, D.F., Lancaster, B.A., McDowell Capuzzo, J., 1997, Experimental field studies with Mya arenaria (Bivalvia) on the induction and effect of hematopoietic neoplasia. J. Invertebr. Pathol. 69, 183-194. CrossRef
White, M.K., Miosky, D., Flessas, D.A., Reinisch, C.L., 1993, The expression of an adhesion-related protein by clam hemocytes. J. Invertebr. Pathol. 61, 253-259. CrossRef
Yevich, P.P., Barry, M.M., 1969, Ovarian tumors in the quahog Mercenaria mercenaria. J. Invertebr. Pathol. 14, 266-267. CrossRef
Yevich, P.P., Barszcz, C.A., 1976, Gonadal and hematopoietic neoplasms in Mya arenaria. Mar. Fish. Rev. 38, 42-42.
Yevich, P.P., Barszcz, C.A., 1977, Neoplasia in soft-shell clams (Mya arenaria) collected from oil-impacted sites. Ann. NY Acad. Sci. 298, 409-426. CrossRef