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PRIMARY MENINGEAL T-CELL LYMPHOMA IN A HARBOR SEAL(PHOCA VITULINA)Author(s) Sophie LabrutDVM Monique WyersDVM Dipl ECVP Julien MiclardDVM andMarie-Anne ColleDVM PhD Dipl ECVPSource Journal of Zoo and Wildlife Medicine 38(2)323-328 2007Published By American Association of Zoo VeterinariansDOI httpdxdoiorg1016381042-7260(2007)038[0323PMTLIA]20CO2URL httpwwwbiooneorgdoifull1016381042-7260282007290385B03233APMTLIA5D20CO3B2

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323

Journal of Zoo and Wildlife Medicine 38(2) 323ndash328 2007Copyright 2007 by American Association of Zoo Veterinarians

PRIMARY MENINGEAL T-CELL LYMPHOMA IN A HARBOR SEAL(PHOCA VITULINA)

Sophie Labrut DVM Monique Wyers DVM Dipl ECVP Julien Miclard DVM andMarie-Anne Colle DVM PhD Dipl ECVP

Abstract A 15-year-old female harbor seal (Phoca vitulina) was referred to the Nantes Veterinary School NantesFrance with a clinical history of anorexia seizures and left hemiplegia Cerebrospinal fluid analysis revealed largenumbers of neoplastic lymphoid cells After injection of a contrast agent into the cerebrospinal space radiographsdemonstrated an asymmetry of the right lateral ventricle Necropsy examination revealed a marked edema of the rightfrontal lobe extending to the basal nuclei and thalamus in the brain Histological examination of the brain revealedleptomeningeal lymphoma Immunohistochemical labeling demonstrated that the neoplasm was of T-cell origin Nosignificant macroscopic or microscopic lesions were observed in the other organs examined including lymphoid organsThis is the first report of primary leptomeningeal lymphoma in a harbor seal

Key words Brain harbor seal lymphoma meningeal pinniped tumor

INTRODUCTION

Cancers have been reported in pinnipeds includ-ing mammary carcinomas a lingual squamous car-cinoma a hepatic carcinoma and a transitionalbladder carcinoma in Californian sea lions (Zalo-phus californianus) a rhabdomyosarcoma and apulmonary carcinoma in Steller sea lions (Eume-topias jubatus) a biliary adenocarcinoma in anorthern elephant seal (Mirounga angustirostris) agranulosa cell tumor in a southern elephant seal(Mirounga leonina) uterine leiomyomas in grayseals (Halichoerus grypus) a carcinoid of the lungin a hooded seal (Cystophora cristata) an adeno-carcinoma of the small intestine in a ringed seal(Phoca hispida) and a renal fibrosarcoma in anorthern fur seal (Callorhinus ursinus)1ndash3691318ndash

2022252629 Lymphomas have been recorded in a fewharbor seals (Phoca vitulina) a northern fur sealand a harp seal (Pagophilus groenlandicus) and allof these cases involved the lymph nodes1214232728

Brain tumors have not been previously reported inpinnipeds This case report describes a primary lep-tomeningeal lymphoma in a captive harbor seal

CASE REPORT

A 15-year-old female harbor seal from theOceanopolis aquarium in Brest (France) was re-ferred to the Nantes Veterinary School NantesFrance for evaluation of a 1-mo history of anorexiaand seizures Upon physical examination abnor-malities were limited to severe apathy moderate

From Unite drsquoAnatomie Pathologique UMR 703INRAENVN Ecole Nationale Veterinaire de Nantes BP40706 NANTES Cedex 03 France Correspondenceshould be directed to Dr Colle (frcollevet-nantesfr)

bilateral conjunctivitis associated with photophobiaand a mild corneal edema No abnormalities werenoted on a complete blood cell count Biochemicalanalyses of serum detected a moderate increase inblood urea nitrogen which was assumed to havebeen induced by dehydration Electrophoresis of se-rum proteins showed evolutive inflammatory syn-drome No abnormalities were seen on thoracic andabdominal radiographs or ultrasonographic scansSerological tests for toxoplasmosis were negativeAntirobe (clindamycin Pharmacia GuyancourtFrance) Sporanox (itraconazole Janssen-CilagSA Issy-les-Moulineaux France) and rehydrationtreatment were administered for 5 wk during whichno particular signs of illness were detected Suddenleft hemiplegia was then recorded associated withcontinuous seizures beginning 2 days later Physicalexamination revealed severe lethargy moderate bi-lateral conjunctivitis associated with photophobiaand a mild bilateral corneal edema The hemogramrevealed mild leukopenia (5 109 white bloodcellsL) that was primarily associated with a mildlymphopenia (05 109 cellsL) The harbor sealalso had a macrocytic normochromic anemia (4 1012 cellsL) Cerebrospinal fluid (CSF) was col-lected under general anesthesia induced with Hyp-novel (midazolam Produits Roche Neuilly-sur-Seine France) (02 mgkg im) and maintainedwith isoflurane (1ndash15 oxygen flow rate 1Lmin) The CSF was slightly turbid The CSF con-tained a large number of cells (3000 cellsml) Ce-rebrospinal fluid smears revealed numerous neo-plastic lymphoid cells After CSF collection radio-graphs were taken with a contrast agent (03 mlkgIopamiron 300 [iopamidol Schering SALys-lez-Lannoy France]) injected into the cerebro-spinal space which showed asymmetry of the right

324 JOURNAL OF ZOO AND WILDLIFE MEDICINE

Figure 1 Coronal section at the level of the caudate nucleus in a harbor seal formalin-fixed brain There is markededema of the white matter in the right cerebral hemisphere () with deformation of the corpus callosus

lateral ventricle A mass in the right side of thebrain was suspected The seal died 1 hr postanes-thesia

A complete necropsy was performed immediate-ly after death No macroscopic lesions were notedexcept in the brain Serial coronal sections of thewhole brain revealed a marked edema of the whitematter in the right frontal lobe extending to thebasal ganglia and thalamus (Fig 1) The leptome-ninges were also markedly thickened Tissue sam-ples from all major organs including the brain andthe cervical spinal cord were fixed in neutral buff-ered 10 formalin embedded in paraffin and rou-tinely processed for histological examination Im-munohistochemical staining with a standard avi-dinndashbiotinndashperoxidase complex-based method wasperformed on dewaxed sections of the brainLymph nodes were used as a positive control Poly-clonal antibody anti-CD3 (Dako Carpinteria Cal-ifornia USA) and anti-CD79a (Dako Carpinteria

California 93013 USA) were used to characterizethe tumor cells

The microscopic examination of the central ner-vous system (CNS) included tissues from the grosslesions described above and samples of the leftthalamus left and right occipital lobes cerebellumand brain stem at the level of pyramids and of themiddle cerebellar peduncles cervical spinal cordand eyes The lesions were similar in all samplesof the brain and cervical spinal cord but differedin intensity There was a poorly defined nonencap-sulated infiltrative growth in the brain that was pri-marily localized in the submeningeal space (Fig 2)In addition neoplastic cells were also noted withinthe brain parenchyma and perivascular spaces Thisgrowth consisted of a very dense population ofround tumor cells The lymphoid-type tumor cellswere medium-sized (about 12 m in diameter) andround with a slim rim of acidophilic cytoplasm around-to-ovoid nucleus with an irregular outline

325LABRUT ET ALmdashPRIMARY MENINGEAL LYMPHOMA IN A HARBOR SEAL

Figure 2 Brain and meninges of a harbor seal demonstrating severe perivascular infiltration of the leptomeningesby neoplastic lymphoid cells (arrow) with extension to cerebral cortex () HampE stain 50

and coarsely clumped chromatin and two small ac-idophilic nucleoli (Fig 3) Marked cytonuclear ab-normalities (anisokaryosis anisocytosis and ma-cronucleolation) were noted The mitotic index wasvery high with 2ndash10 mitotic figures per high-pow-ered field Numerous apoptotic tumor cells werepresent A marked edema of the neuropil was alsopresent The meninges around the optic nerve wereinfiltrated with similarly described neoplastic cellsThe other optic segments did not reveal any abnor-mal lesions histologically The lesions of this har-bor seal were compatible with those of a highlymalignant primary leptomeningeal lymphomaLymphoid neoplastic cells were positive when im-munostained with the polyclonal antibody anti-CD3(Fig 4) They were negative for CD79a Histolog-ical examination of tissues collected during necrop-sy including lymphoid organs revealed no abnor-malities in any samples other than those from thebrain

DISCUSSION

This case report documents a highly malignantprimary T-cell leptomeningeal lymphoma in a har-bor seal The lesions mostly located in the rightfrontal cortex were compatible with clinical signsof seizures and left hemiplegia observed in this har-bor seal Meningeal lymphoma was diagnosedbased on the detection of neoplastic cells in theCSF Radiographs with a contrast agent revealedthat the tumor was infiltrating the right side of thebrain Pathology confirmed the primary nature ofthe brain tumor Primary brain lymphomas are un-common in humans and other animals11 In humansprimary brain lymphomas account for 2 of ex-tranodal lymphomas and 1 of intracranial tumorsand are the most common CNS tumor in immu-nocompromised patients11 Leptomeningeal lym-phoma is a rare neoplasm and is almost alwayssecondary in origin Only a few primary cases havebeen reported in humans mostly of B-cell ori-

326 JOURNAL OF ZOO AND WILDLIFE MEDICINE

Figure 3 Brain and meninges of a harbor seal as in Figure 2 demonstrating massive infiltration of the arachnoidalspace by medium-sized round neoplastic cells with a slim rim of cytoplasm (lymphoid type) Numerous mitotic figures(arrows) are noted HampE stain 400

gin162124 In animals meningeal lymphoma hasbeen reported in horses dogs and cats and mayinvolve the brain or spinal cord571015 Primary men-ingeal lymphoma has been reported in the brains oftwo dogs but in one of these cases ovary involve-ment was also noted5 Diffuse infiltration of the lep-tomeninges by neoplastic lymphocytes has been re-ported along the entire length of the spinal cord ina horse15 In cats one primary leptomeningeal lym-phoma without cerebral parenchymal extension wasof B-cell origin and another extending to the peri-vascular space of intraparenchymal vessels ofT-cell origin has been reported710 In this harborseal the lymphoma was of T-cell origin

There are few reports of lymphomas in pinni-peds Lymphomas have been documented in an in-fant northern fur seal a harp seal and a few harborseals1214232728 Only the lymph nodes were involvedin all these cases and no extension to the lepto-meninges was observed In this case no lesion was

found in any other location including the lymphnodes This is the first report of a primary brainlymphoma in a pinniped

Although neoplasms remain uncommon in pin-nipeds the number of reported cases has increasedconsiderably in recent years in both pinnipeds andin other marine mammals such as ceta-ceans48121317222526 This increase in the number ofreported cases may reflect an increase in the num-ber of animals examined by pathologists rather thana true increase in incidence22 However it is pos-sible that the number of cancers has genuinely in-creased and that this increase is associated with anincrease in the effects of pollution on wild marinemammals3817

Acknowledgments We would like to thank thetechnicians of the Pathology Department of NantesVeterinary School for technical assistance

327LABRUT ET ALmdashPRIMARY MENINGEAL LYMPHOMA IN A HARBOR SEAL

Figure 4 Brain and meninges of a harbor seal demonstrating that most of the neoplastic cells are positive forimmunostaining with the polyclonal antibody directed against CD3 (insert in higher magnification) Avidinndashbiotinndashperoxidase complex method hematoxylin counterstain 630

LITERATURE CITED

1 Acevedo-Whitehouse K A F Constantino-CasasD Aurioles-Gamboa H A Rodriguez-Martinez and CR Godinez-Reyes 1999 Hepatic carcinoma with spleenmetastasis in a California sea lion from the Gulf of Cali-fornia J Wildl Dis 35 565ndash568

2 Aschfalk A and L N Bacciarini 2002 Carcinoidin the lung of a hooded seal (Cystophora cristata) VetRec 151 770ndash772

3 Baker J R 1989 Pollution-associated uterine le-sions in grey seals from the Liverpool Bay area of theIrish Sea Vet Rec 125 303

4 Bossart G D R Ewing A J Herron C Cray BMase S J Decker J W Alexander and N H Altman1997 Immunoblastic malignant lymphoma in dolphinshistologic ultrastructural and immunohistochemical fea-tures J Vet Diagn Invest 9 454ndash458

5 Britt J O Jr J G Simpson and E B Howard1984 Malignant lymphoma of the meninges in two dogsJ Comp Pathol 94 45ndash53

6 Brown R J A W Smith and M C Keyes 1975

Renal fibrosarcoma in the northern fur seal J Wildl Dis11 23ndash25

7 Callanan J J B A Jones J Irvine B J WillettI A McCandlish and O Jarrett 1996 Histologic clas-sification and immunophenotype of lymphosarcomas incats with naturally and experimentally acquired feline im-munodeficiency virus infections Vet Pathol 33 264ndash272

8 De Guise S A Lagace and P Beland 1994 Tu-mors in St Lawrence beluga whales (Delphinapterus leu-cas) Vet Pathol 31 444ndash449

9 Fauquier D F Gulland M Haulena and T Spraker2003 Biliary adenocarcinoma in a stranded northern el-ephant seal (Mirounga angustirostris) J Wildl Dis 39723ndash726

10 Fondevila D M Vilafranca and M Pumarola1998 Primary central nervous system T-cell lymphoma ina cat Vet Pathol 35 550ndash553

11 Frosch M D Anthony and U De Girolami 2005The central nervous system In Kumar V A Abbas andN Fausto (eds) Robbins and Cotran Pathologic Basis of

328 JOURNAL OF ZOO AND WILDLIFE MEDICINE

Disease 7th ed Elsevier Philadelphia Pennsylvania Pp1347ndash1419

12 Griner L A 1971 Malignant leukemic lymphomain two harbor seals (Phoca vitulina geronimensis) Am JVet Res 32 827ndash830

13 Gulland F M J G Trupkiewicz T R Sprakerand L J Lowenstine 1996 Metastatic carcinoma of prob-able transitional cell origin in 66 free-living California sealions (Zalophus californianus) 1979 to 1994 J WildlDis 32 250ndash258

14 Landy R 1980 A review of neoplasia in marinemammals In Montali R and G Migaki (eds) TheComparative Pathology of Zoo Animals Smithsonian In-stitution Press Washington DC Pp 563ndash573

15 Lester G D R J MacKay and B Smith-Meyer1992 Primary meningeal lymphoma in a horse J AmVet Med Assoc 201 1219ndash1221

16 Marsh W L Jr D R Stevenson and H J Long1983 Primary leptomeningeal presentation of T-cell lym-phoma Report of a patient and review of the literatureCancer 51 1125ndash1131

17 Martineau D K Lemberger A Dallaire P La-belle T P Lipscomb P Michel and I Mikaelian 2002Cancer in wildlife a case study Beluga from the StLawrence estuary Quebec Canada Environ Health Per-spect 110 285ndash292

18 Matsuda M S Hashiura Y Une H Sirouzu andY Nomura 2003 Two distinct carcinomas of mammarygland origin in a California sea lion J Wildl Dis 39241ndash243

19 Mawdesley-Thomas L E 1971 An ovarian tu-mour in a southern elephant seal (Mirounga leonina) VetPathol 8 9ndash15

20 Mawdesley-Thomas L E and W N Bonner1971 Uterine tumours in a grey seal (Halichoerus gry-pus) J Pathol 103 205ndash208

21 Menniti A L Moschettoni G Liccardo and PLunardi 2005 Low-grade primary meningeal lymphomacase report and review of the literature Neurosurg Rev28 229ndash233

22 Mikaelian I D Leclair and J Inukpuk 2001 Ad-enocarcinoma of the small intestine in a ringed seal fromHudson Bay J Wildl Dis 37 379ndash382

23 Osborn K 1988 Leukemic lymphoma in harborseals (Phoca vitulina) report of three cases occurring overtwo years and discussion of pathogenesis Annu ConfAm Assoc Zoo Vet 1988 96

24 Pernot P P Saint-Blancard R Dulou E Blondetand O Goasguen 2002 Primary dural lymphoma A casereport Neurochirurgie 48 124ndash127

25 Sato S H Kitamura M Mori M Fukazawa MTakeda and K Kadota 1998 Adenocarcinoma of thelung in a Steller sea lion (Eumetopias jubatus) J VetMed Sci 60 1349ndash1351

26 Sato T T Higuchi H Shibuya S Ohba S No-gami W Shirai H Watanabe and S Honda 2002 Lin-gual squamous cell carcinoma in a California sea lion(Zalophus californianus) J Zoo Wildl Med 33 367ndash370

27 Stedham M A H W Casey and M C Keyes1977 Lymphosarcoma in an infant northern fur seal (Cal-lorhinus ursinus) J Wildl Dis 13 176ndash179

28 Stroud R K and D R Stevens 1980 Lympho-sarcoma in a harbor seal (Phoca vitulina richardii) JWildl Dis 16 267ndash270

29 Zabka T S E L Buckles F M Gulland M Hau-lena D K Naydan and L J Lowenstine 2004 Pleo-morphic rhabdomyosarcoma with pulmonary metastasis ina stranded Steller (northern) sea lion (Eumetopias juba-tus) J Comp Pathol 130 195ndash198

Received for publication 20 May 2006

324 JOURNAL OF ZOO AND WILDLIFE MEDICINE

Figure 1 Coronal section at the level of the caudate nucleus in a harbor seal formalin-fixed brain There is markededema of the white matter in the right cerebral hemisphere () with deformation of the corpus callosus

lateral ventricle A mass in the right side of thebrain was suspected The seal died 1 hr postanes-thesia

A complete necropsy was performed immediate-ly after death No macroscopic lesions were notedexcept in the brain Serial coronal sections of thewhole brain revealed a marked edema of the whitematter in the right frontal lobe extending to thebasal ganglia and thalamus (Fig 1) The leptome-ninges were also markedly thickened Tissue sam-ples from all major organs including the brain andthe cervical spinal cord were fixed in neutral buff-ered 10 formalin embedded in paraffin and rou-tinely processed for histological examination Im-munohistochemical staining with a standard avi-dinndashbiotinndashperoxidase complex-based method wasperformed on dewaxed sections of the brainLymph nodes were used as a positive control Poly-clonal antibody anti-CD3 (Dako Carpinteria Cal-ifornia USA) and anti-CD79a (Dako Carpinteria

California 93013 USA) were used to characterizethe tumor cells

The microscopic examination of the central ner-vous system (CNS) included tissues from the grosslesions described above and samples of the leftthalamus left and right occipital lobes cerebellumand brain stem at the level of pyramids and of themiddle cerebellar peduncles cervical spinal cordand eyes The lesions were similar in all samplesof the brain and cervical spinal cord but differedin intensity There was a poorly defined nonencap-sulated infiltrative growth in the brain that was pri-marily localized in the submeningeal space (Fig 2)In addition neoplastic cells were also noted withinthe brain parenchyma and perivascular spaces Thisgrowth consisted of a very dense population ofround tumor cells The lymphoid-type tumor cellswere medium-sized (about 12 m in diameter) andround with a slim rim of acidophilic cytoplasm around-to-ovoid nucleus with an irregular outline

325LABRUT ET ALmdashPRIMARY MENINGEAL LYMPHOMA IN A HARBOR SEAL

Figure 2 Brain and meninges of a harbor seal demonstrating severe perivascular infiltration of the leptomeningesby neoplastic lymphoid cells (arrow) with extension to cerebral cortex () HampE stain 50

and coarsely clumped chromatin and two small ac-idophilic nucleoli (Fig 3) Marked cytonuclear ab-normalities (anisokaryosis anisocytosis and ma-cronucleolation) were noted The mitotic index wasvery high with 2ndash10 mitotic figures per high-pow-ered field Numerous apoptotic tumor cells werepresent A marked edema of the neuropil was alsopresent The meninges around the optic nerve wereinfiltrated with similarly described neoplastic cellsThe other optic segments did not reveal any abnor-mal lesions histologically The lesions of this har-bor seal were compatible with those of a highlymalignant primary leptomeningeal lymphomaLymphoid neoplastic cells were positive when im-munostained with the polyclonal antibody anti-CD3(Fig 4) They were negative for CD79a Histolog-ical examination of tissues collected during necrop-sy including lymphoid organs revealed no abnor-malities in any samples other than those from thebrain

DISCUSSION

This case report documents a highly malignantprimary T-cell leptomeningeal lymphoma in a har-bor seal The lesions mostly located in the rightfrontal cortex were compatible with clinical signsof seizures and left hemiplegia observed in this har-bor seal Meningeal lymphoma was diagnosedbased on the detection of neoplastic cells in theCSF Radiographs with a contrast agent revealedthat the tumor was infiltrating the right side of thebrain Pathology confirmed the primary nature ofthe brain tumor Primary brain lymphomas are un-common in humans and other animals11 In humansprimary brain lymphomas account for 2 of ex-tranodal lymphomas and 1 of intracranial tumorsand are the most common CNS tumor in immu-nocompromised patients11 Leptomeningeal lym-phoma is a rare neoplasm and is almost alwayssecondary in origin Only a few primary cases havebeen reported in humans mostly of B-cell ori-

326 JOURNAL OF ZOO AND WILDLIFE MEDICINE

Figure 3 Brain and meninges of a harbor seal as in Figure 2 demonstrating massive infiltration of the arachnoidalspace by medium-sized round neoplastic cells with a slim rim of cytoplasm (lymphoid type) Numerous mitotic figures(arrows) are noted HampE stain 400

gin162124 In animals meningeal lymphoma hasbeen reported in horses dogs and cats and mayinvolve the brain or spinal cord571015 Primary men-ingeal lymphoma has been reported in the brains oftwo dogs but in one of these cases ovary involve-ment was also noted5 Diffuse infiltration of the lep-tomeninges by neoplastic lymphocytes has been re-ported along the entire length of the spinal cord ina horse15 In cats one primary leptomeningeal lym-phoma without cerebral parenchymal extension wasof B-cell origin and another extending to the peri-vascular space of intraparenchymal vessels ofT-cell origin has been reported710 In this harborseal the lymphoma was of T-cell origin

There are few reports of lymphomas in pinni-peds Lymphomas have been documented in an in-fant northern fur seal a harp seal and a few harborseals1214232728 Only the lymph nodes were involvedin all these cases and no extension to the lepto-meninges was observed In this case no lesion was

found in any other location including the lymphnodes This is the first report of a primary brainlymphoma in a pinniped

Although neoplasms remain uncommon in pin-nipeds the number of reported cases has increasedconsiderably in recent years in both pinnipeds andin other marine mammals such as ceta-ceans48121317222526 This increase in the number ofreported cases may reflect an increase in the num-ber of animals examined by pathologists rather thana true increase in incidence22 However it is pos-sible that the number of cancers has genuinely in-creased and that this increase is associated with anincrease in the effects of pollution on wild marinemammals3817

Acknowledgments We would like to thank thetechnicians of the Pathology Department of NantesVeterinary School for technical assistance

327LABRUT ET ALmdashPRIMARY MENINGEAL LYMPHOMA IN A HARBOR SEAL

Figure 4 Brain and meninges of a harbor seal demonstrating that most of the neoplastic cells are positive forimmunostaining with the polyclonal antibody directed against CD3 (insert in higher magnification) Avidinndashbiotinndashperoxidase complex method hematoxylin counterstain 630

LITERATURE CITED

1 Acevedo-Whitehouse K A F Constantino-CasasD Aurioles-Gamboa H A Rodriguez-Martinez and CR Godinez-Reyes 1999 Hepatic carcinoma with spleenmetastasis in a California sea lion from the Gulf of Cali-fornia J Wildl Dis 35 565ndash568

2 Aschfalk A and L N Bacciarini 2002 Carcinoidin the lung of a hooded seal (Cystophora cristata) VetRec 151 770ndash772

3 Baker J R 1989 Pollution-associated uterine le-sions in grey seals from the Liverpool Bay area of theIrish Sea Vet Rec 125 303

4 Bossart G D R Ewing A J Herron C Cray BMase S J Decker J W Alexander and N H Altman1997 Immunoblastic malignant lymphoma in dolphinshistologic ultrastructural and immunohistochemical fea-tures J Vet Diagn Invest 9 454ndash458

5 Britt J O Jr J G Simpson and E B Howard1984 Malignant lymphoma of the meninges in two dogsJ Comp Pathol 94 45ndash53

6 Brown R J A W Smith and M C Keyes 1975

Renal fibrosarcoma in the northern fur seal J Wildl Dis11 23ndash25

7 Callanan J J B A Jones J Irvine B J WillettI A McCandlish and O Jarrett 1996 Histologic clas-sification and immunophenotype of lymphosarcomas incats with naturally and experimentally acquired feline im-munodeficiency virus infections Vet Pathol 33 264ndash272

8 De Guise S A Lagace and P Beland 1994 Tu-mors in St Lawrence beluga whales (Delphinapterus leu-cas) Vet Pathol 31 444ndash449

9 Fauquier D F Gulland M Haulena and T Spraker2003 Biliary adenocarcinoma in a stranded northern el-ephant seal (Mirounga angustirostris) J Wildl Dis 39723ndash726

10 Fondevila D M Vilafranca and M Pumarola1998 Primary central nervous system T-cell lymphoma ina cat Vet Pathol 35 550ndash553

11 Frosch M D Anthony and U De Girolami 2005The central nervous system In Kumar V A Abbas andN Fausto (eds) Robbins and Cotran Pathologic Basis of

328 JOURNAL OF ZOO AND WILDLIFE MEDICINE

Disease 7th ed Elsevier Philadelphia Pennsylvania Pp1347ndash1419

12 Griner L A 1971 Malignant leukemic lymphomain two harbor seals (Phoca vitulina geronimensis) Am JVet Res 32 827ndash830

13 Gulland F M J G Trupkiewicz T R Sprakerand L J Lowenstine 1996 Metastatic carcinoma of prob-able transitional cell origin in 66 free-living California sealions (Zalophus californianus) 1979 to 1994 J WildlDis 32 250ndash258

14 Landy R 1980 A review of neoplasia in marinemammals In Montali R and G Migaki (eds) TheComparative Pathology of Zoo Animals Smithsonian In-stitution Press Washington DC Pp 563ndash573

15 Lester G D R J MacKay and B Smith-Meyer1992 Primary meningeal lymphoma in a horse J AmVet Med Assoc 201 1219ndash1221

16 Marsh W L Jr D R Stevenson and H J Long1983 Primary leptomeningeal presentation of T-cell lym-phoma Report of a patient and review of the literatureCancer 51 1125ndash1131

17 Martineau D K Lemberger A Dallaire P La-belle T P Lipscomb P Michel and I Mikaelian 2002Cancer in wildlife a case study Beluga from the StLawrence estuary Quebec Canada Environ Health Per-spect 110 285ndash292

18 Matsuda M S Hashiura Y Une H Sirouzu andY Nomura 2003 Two distinct carcinomas of mammarygland origin in a California sea lion J Wildl Dis 39241ndash243

19 Mawdesley-Thomas L E 1971 An ovarian tu-mour in a southern elephant seal (Mirounga leonina) VetPathol 8 9ndash15

20 Mawdesley-Thomas L E and W N Bonner1971 Uterine tumours in a grey seal (Halichoerus gry-pus) J Pathol 103 205ndash208

21 Menniti A L Moschettoni G Liccardo and PLunardi 2005 Low-grade primary meningeal lymphomacase report and review of the literature Neurosurg Rev28 229ndash233

22 Mikaelian I D Leclair and J Inukpuk 2001 Ad-enocarcinoma of the small intestine in a ringed seal fromHudson Bay J Wildl Dis 37 379ndash382

23 Osborn K 1988 Leukemic lymphoma in harborseals (Phoca vitulina) report of three cases occurring overtwo years and discussion of pathogenesis Annu ConfAm Assoc Zoo Vet 1988 96

24 Pernot P P Saint-Blancard R Dulou E Blondetand O Goasguen 2002 Primary dural lymphoma A casereport Neurochirurgie 48 124ndash127

25 Sato S H Kitamura M Mori M Fukazawa MTakeda and K Kadota 1998 Adenocarcinoma of thelung in a Steller sea lion (Eumetopias jubatus) J VetMed Sci 60 1349ndash1351

26 Sato T T Higuchi H Shibuya S Ohba S No-gami W Shirai H Watanabe and S Honda 2002 Lin-gual squamous cell carcinoma in a California sea lion(Zalophus californianus) J Zoo Wildl Med 33 367ndash370

27 Stedham M A H W Casey and M C Keyes1977 Lymphosarcoma in an infant northern fur seal (Cal-lorhinus ursinus) J Wildl Dis 13 176ndash179

28 Stroud R K and D R Stevens 1980 Lympho-sarcoma in a harbor seal (Phoca vitulina richardii) JWildl Dis 16 267ndash270

29 Zabka T S E L Buckles F M Gulland M Hau-lena D K Naydan and L J Lowenstine 2004 Pleo-morphic rhabdomyosarcoma with pulmonary metastasis ina stranded Steller (northern) sea lion (Eumetopias juba-tus) J Comp Pathol 130 195ndash198

Received for publication 20 May 2006

325LABRUT ET ALmdashPRIMARY MENINGEAL LYMPHOMA IN A HARBOR SEAL

Figure 2 Brain and meninges of a harbor seal demonstrating severe perivascular infiltration of the leptomeningesby neoplastic lymphoid cells (arrow) with extension to cerebral cortex () HampE stain 50

and coarsely clumped chromatin and two small ac-idophilic nucleoli (Fig 3) Marked cytonuclear ab-normalities (anisokaryosis anisocytosis and ma-cronucleolation) were noted The mitotic index wasvery high with 2ndash10 mitotic figures per high-pow-ered field Numerous apoptotic tumor cells werepresent A marked edema of the neuropil was alsopresent The meninges around the optic nerve wereinfiltrated with similarly described neoplastic cellsThe other optic segments did not reveal any abnor-mal lesions histologically The lesions of this har-bor seal were compatible with those of a highlymalignant primary leptomeningeal lymphomaLymphoid neoplastic cells were positive when im-munostained with the polyclonal antibody anti-CD3(Fig 4) They were negative for CD79a Histolog-ical examination of tissues collected during necrop-sy including lymphoid organs revealed no abnor-malities in any samples other than those from thebrain

DISCUSSION

This case report documents a highly malignantprimary T-cell leptomeningeal lymphoma in a har-bor seal The lesions mostly located in the rightfrontal cortex were compatible with clinical signsof seizures and left hemiplegia observed in this har-bor seal Meningeal lymphoma was diagnosedbased on the detection of neoplastic cells in theCSF Radiographs with a contrast agent revealedthat the tumor was infiltrating the right side of thebrain Pathology confirmed the primary nature ofthe brain tumor Primary brain lymphomas are un-common in humans and other animals11 In humansprimary brain lymphomas account for 2 of ex-tranodal lymphomas and 1 of intracranial tumorsand are the most common CNS tumor in immu-nocompromised patients11 Leptomeningeal lym-phoma is a rare neoplasm and is almost alwayssecondary in origin Only a few primary cases havebeen reported in humans mostly of B-cell ori-

326 JOURNAL OF ZOO AND WILDLIFE MEDICINE

Figure 3 Brain and meninges of a harbor seal as in Figure 2 demonstrating massive infiltration of the arachnoidalspace by medium-sized round neoplastic cells with a slim rim of cytoplasm (lymphoid type) Numerous mitotic figures(arrows) are noted HampE stain 400

gin162124 In animals meningeal lymphoma hasbeen reported in horses dogs and cats and mayinvolve the brain or spinal cord571015 Primary men-ingeal lymphoma has been reported in the brains oftwo dogs but in one of these cases ovary involve-ment was also noted5 Diffuse infiltration of the lep-tomeninges by neoplastic lymphocytes has been re-ported along the entire length of the spinal cord ina horse15 In cats one primary leptomeningeal lym-phoma without cerebral parenchymal extension wasof B-cell origin and another extending to the peri-vascular space of intraparenchymal vessels ofT-cell origin has been reported710 In this harborseal the lymphoma was of T-cell origin

There are few reports of lymphomas in pinni-peds Lymphomas have been documented in an in-fant northern fur seal a harp seal and a few harborseals1214232728 Only the lymph nodes were involvedin all these cases and no extension to the lepto-meninges was observed In this case no lesion was

found in any other location including the lymphnodes This is the first report of a primary brainlymphoma in a pinniped

Although neoplasms remain uncommon in pin-nipeds the number of reported cases has increasedconsiderably in recent years in both pinnipeds andin other marine mammals such as ceta-ceans48121317222526 This increase in the number ofreported cases may reflect an increase in the num-ber of animals examined by pathologists rather thana true increase in incidence22 However it is pos-sible that the number of cancers has genuinely in-creased and that this increase is associated with anincrease in the effects of pollution on wild marinemammals3817

Acknowledgments We would like to thank thetechnicians of the Pathology Department of NantesVeterinary School for technical assistance

327LABRUT ET ALmdashPRIMARY MENINGEAL LYMPHOMA IN A HARBOR SEAL

Figure 4 Brain and meninges of a harbor seal demonstrating that most of the neoplastic cells are positive forimmunostaining with the polyclonal antibody directed against CD3 (insert in higher magnification) Avidinndashbiotinndashperoxidase complex method hematoxylin counterstain 630

LITERATURE CITED

1 Acevedo-Whitehouse K A F Constantino-CasasD Aurioles-Gamboa H A Rodriguez-Martinez and CR Godinez-Reyes 1999 Hepatic carcinoma with spleenmetastasis in a California sea lion from the Gulf of Cali-fornia J Wildl Dis 35 565ndash568

2 Aschfalk A and L N Bacciarini 2002 Carcinoidin the lung of a hooded seal (Cystophora cristata) VetRec 151 770ndash772

3 Baker J R 1989 Pollution-associated uterine le-sions in grey seals from the Liverpool Bay area of theIrish Sea Vet Rec 125 303

4 Bossart G D R Ewing A J Herron C Cray BMase S J Decker J W Alexander and N H Altman1997 Immunoblastic malignant lymphoma in dolphinshistologic ultrastructural and immunohistochemical fea-tures J Vet Diagn Invest 9 454ndash458

5 Britt J O Jr J G Simpson and E B Howard1984 Malignant lymphoma of the meninges in two dogsJ Comp Pathol 94 45ndash53

6 Brown R J A W Smith and M C Keyes 1975

Renal fibrosarcoma in the northern fur seal J Wildl Dis11 23ndash25

7 Callanan J J B A Jones J Irvine B J WillettI A McCandlish and O Jarrett 1996 Histologic clas-sification and immunophenotype of lymphosarcomas incats with naturally and experimentally acquired feline im-munodeficiency virus infections Vet Pathol 33 264ndash272

8 De Guise S A Lagace and P Beland 1994 Tu-mors in St Lawrence beluga whales (Delphinapterus leu-cas) Vet Pathol 31 444ndash449

9 Fauquier D F Gulland M Haulena and T Spraker2003 Biliary adenocarcinoma in a stranded northern el-ephant seal (Mirounga angustirostris) J Wildl Dis 39723ndash726

10 Fondevila D M Vilafranca and M Pumarola1998 Primary central nervous system T-cell lymphoma ina cat Vet Pathol 35 550ndash553

11 Frosch M D Anthony and U De Girolami 2005The central nervous system In Kumar V A Abbas andN Fausto (eds) Robbins and Cotran Pathologic Basis of

328 JOURNAL OF ZOO AND WILDLIFE MEDICINE

Disease 7th ed Elsevier Philadelphia Pennsylvania Pp1347ndash1419

12 Griner L A 1971 Malignant leukemic lymphomain two harbor seals (Phoca vitulina geronimensis) Am JVet Res 32 827ndash830

13 Gulland F M J G Trupkiewicz T R Sprakerand L J Lowenstine 1996 Metastatic carcinoma of prob-able transitional cell origin in 66 free-living California sealions (Zalophus californianus) 1979 to 1994 J WildlDis 32 250ndash258

14 Landy R 1980 A review of neoplasia in marinemammals In Montali R and G Migaki (eds) TheComparative Pathology of Zoo Animals Smithsonian In-stitution Press Washington DC Pp 563ndash573

15 Lester G D R J MacKay and B Smith-Meyer1992 Primary meningeal lymphoma in a horse J AmVet Med Assoc 201 1219ndash1221

16 Marsh W L Jr D R Stevenson and H J Long1983 Primary leptomeningeal presentation of T-cell lym-phoma Report of a patient and review of the literatureCancer 51 1125ndash1131

17 Martineau D K Lemberger A Dallaire P La-belle T P Lipscomb P Michel and I Mikaelian 2002Cancer in wildlife a case study Beluga from the StLawrence estuary Quebec Canada Environ Health Per-spect 110 285ndash292

18 Matsuda M S Hashiura Y Une H Sirouzu andY Nomura 2003 Two distinct carcinomas of mammarygland origin in a California sea lion J Wildl Dis 39241ndash243

19 Mawdesley-Thomas L E 1971 An ovarian tu-mour in a southern elephant seal (Mirounga leonina) VetPathol 8 9ndash15

20 Mawdesley-Thomas L E and W N Bonner1971 Uterine tumours in a grey seal (Halichoerus gry-pus) J Pathol 103 205ndash208

21 Menniti A L Moschettoni G Liccardo and PLunardi 2005 Low-grade primary meningeal lymphomacase report and review of the literature Neurosurg Rev28 229ndash233

22 Mikaelian I D Leclair and J Inukpuk 2001 Ad-enocarcinoma of the small intestine in a ringed seal fromHudson Bay J Wildl Dis 37 379ndash382

23 Osborn K 1988 Leukemic lymphoma in harborseals (Phoca vitulina) report of three cases occurring overtwo years and discussion of pathogenesis Annu ConfAm Assoc Zoo Vet 1988 96

24 Pernot P P Saint-Blancard R Dulou E Blondetand O Goasguen 2002 Primary dural lymphoma A casereport Neurochirurgie 48 124ndash127

25 Sato S H Kitamura M Mori M Fukazawa MTakeda and K Kadota 1998 Adenocarcinoma of thelung in a Steller sea lion (Eumetopias jubatus) J VetMed Sci 60 1349ndash1351

26 Sato T T Higuchi H Shibuya S Ohba S No-gami W Shirai H Watanabe and S Honda 2002 Lin-gual squamous cell carcinoma in a California sea lion(Zalophus californianus) J Zoo Wildl Med 33 367ndash370

27 Stedham M A H W Casey and M C Keyes1977 Lymphosarcoma in an infant northern fur seal (Cal-lorhinus ursinus) J Wildl Dis 13 176ndash179

28 Stroud R K and D R Stevens 1980 Lympho-sarcoma in a harbor seal (Phoca vitulina richardii) JWildl Dis 16 267ndash270

29 Zabka T S E L Buckles F M Gulland M Hau-lena D K Naydan and L J Lowenstine 2004 Pleo-morphic rhabdomyosarcoma with pulmonary metastasis ina stranded Steller (northern) sea lion (Eumetopias juba-tus) J Comp Pathol 130 195ndash198

Received for publication 20 May 2006

326 JOURNAL OF ZOO AND WILDLIFE MEDICINE

Figure 3 Brain and meninges of a harbor seal as in Figure 2 demonstrating massive infiltration of the arachnoidalspace by medium-sized round neoplastic cells with a slim rim of cytoplasm (lymphoid type) Numerous mitotic figures(arrows) are noted HampE stain 400

gin162124 In animals meningeal lymphoma hasbeen reported in horses dogs and cats and mayinvolve the brain or spinal cord571015 Primary men-ingeal lymphoma has been reported in the brains oftwo dogs but in one of these cases ovary involve-ment was also noted5 Diffuse infiltration of the lep-tomeninges by neoplastic lymphocytes has been re-ported along the entire length of the spinal cord ina horse15 In cats one primary leptomeningeal lym-phoma without cerebral parenchymal extension wasof B-cell origin and another extending to the peri-vascular space of intraparenchymal vessels ofT-cell origin has been reported710 In this harborseal the lymphoma was of T-cell origin

There are few reports of lymphomas in pinni-peds Lymphomas have been documented in an in-fant northern fur seal a harp seal and a few harborseals1214232728 Only the lymph nodes were involvedin all these cases and no extension to the lepto-meninges was observed In this case no lesion was

found in any other location including the lymphnodes This is the first report of a primary brainlymphoma in a pinniped

Although neoplasms remain uncommon in pin-nipeds the number of reported cases has increasedconsiderably in recent years in both pinnipeds andin other marine mammals such as ceta-ceans48121317222526 This increase in the number ofreported cases may reflect an increase in the num-ber of animals examined by pathologists rather thana true increase in incidence22 However it is pos-sible that the number of cancers has genuinely in-creased and that this increase is associated with anincrease in the effects of pollution on wild marinemammals3817

Acknowledgments We would like to thank thetechnicians of the Pathology Department of NantesVeterinary School for technical assistance

327LABRUT ET ALmdashPRIMARY MENINGEAL LYMPHOMA IN A HARBOR SEAL

Figure 4 Brain and meninges of a harbor seal demonstrating that most of the neoplastic cells are positive forimmunostaining with the polyclonal antibody directed against CD3 (insert in higher magnification) Avidinndashbiotinndashperoxidase complex method hematoxylin counterstain 630

LITERATURE CITED

1 Acevedo-Whitehouse K A F Constantino-CasasD Aurioles-Gamboa H A Rodriguez-Martinez and CR Godinez-Reyes 1999 Hepatic carcinoma with spleenmetastasis in a California sea lion from the Gulf of Cali-fornia J Wildl Dis 35 565ndash568

2 Aschfalk A and L N Bacciarini 2002 Carcinoidin the lung of a hooded seal (Cystophora cristata) VetRec 151 770ndash772

3 Baker J R 1989 Pollution-associated uterine le-sions in grey seals from the Liverpool Bay area of theIrish Sea Vet Rec 125 303

4 Bossart G D R Ewing A J Herron C Cray BMase S J Decker J W Alexander and N H Altman1997 Immunoblastic malignant lymphoma in dolphinshistologic ultrastructural and immunohistochemical fea-tures J Vet Diagn Invest 9 454ndash458

5 Britt J O Jr J G Simpson and E B Howard1984 Malignant lymphoma of the meninges in two dogsJ Comp Pathol 94 45ndash53

6 Brown R J A W Smith and M C Keyes 1975

Renal fibrosarcoma in the northern fur seal J Wildl Dis11 23ndash25

7 Callanan J J B A Jones J Irvine B J WillettI A McCandlish and O Jarrett 1996 Histologic clas-sification and immunophenotype of lymphosarcomas incats with naturally and experimentally acquired feline im-munodeficiency virus infections Vet Pathol 33 264ndash272

8 De Guise S A Lagace and P Beland 1994 Tu-mors in St Lawrence beluga whales (Delphinapterus leu-cas) Vet Pathol 31 444ndash449

9 Fauquier D F Gulland M Haulena and T Spraker2003 Biliary adenocarcinoma in a stranded northern el-ephant seal (Mirounga angustirostris) J Wildl Dis 39723ndash726

10 Fondevila D M Vilafranca and M Pumarola1998 Primary central nervous system T-cell lymphoma ina cat Vet Pathol 35 550ndash553

11 Frosch M D Anthony and U De Girolami 2005The central nervous system In Kumar V A Abbas andN Fausto (eds) Robbins and Cotran Pathologic Basis of

328 JOURNAL OF ZOO AND WILDLIFE MEDICINE

Disease 7th ed Elsevier Philadelphia Pennsylvania Pp1347ndash1419

12 Griner L A 1971 Malignant leukemic lymphomain two harbor seals (Phoca vitulina geronimensis) Am JVet Res 32 827ndash830

13 Gulland F M J G Trupkiewicz T R Sprakerand L J Lowenstine 1996 Metastatic carcinoma of prob-able transitional cell origin in 66 free-living California sealions (Zalophus californianus) 1979 to 1994 J WildlDis 32 250ndash258

14 Landy R 1980 A review of neoplasia in marinemammals In Montali R and G Migaki (eds) TheComparative Pathology of Zoo Animals Smithsonian In-stitution Press Washington DC Pp 563ndash573

15 Lester G D R J MacKay and B Smith-Meyer1992 Primary meningeal lymphoma in a horse J AmVet Med Assoc 201 1219ndash1221

16 Marsh W L Jr D R Stevenson and H J Long1983 Primary leptomeningeal presentation of T-cell lym-phoma Report of a patient and review of the literatureCancer 51 1125ndash1131

17 Martineau D K Lemberger A Dallaire P La-belle T P Lipscomb P Michel and I Mikaelian 2002Cancer in wildlife a case study Beluga from the StLawrence estuary Quebec Canada Environ Health Per-spect 110 285ndash292

18 Matsuda M S Hashiura Y Une H Sirouzu andY Nomura 2003 Two distinct carcinomas of mammarygland origin in a California sea lion J Wildl Dis 39241ndash243

19 Mawdesley-Thomas L E 1971 An ovarian tu-mour in a southern elephant seal (Mirounga leonina) VetPathol 8 9ndash15

20 Mawdesley-Thomas L E and W N Bonner1971 Uterine tumours in a grey seal (Halichoerus gry-pus) J Pathol 103 205ndash208

21 Menniti A L Moschettoni G Liccardo and PLunardi 2005 Low-grade primary meningeal lymphomacase report and review of the literature Neurosurg Rev28 229ndash233

22 Mikaelian I D Leclair and J Inukpuk 2001 Ad-enocarcinoma of the small intestine in a ringed seal fromHudson Bay J Wildl Dis 37 379ndash382

23 Osborn K 1988 Leukemic lymphoma in harborseals (Phoca vitulina) report of three cases occurring overtwo years and discussion of pathogenesis Annu ConfAm Assoc Zoo Vet 1988 96

24 Pernot P P Saint-Blancard R Dulou E Blondetand O Goasguen 2002 Primary dural lymphoma A casereport Neurochirurgie 48 124ndash127

25 Sato S H Kitamura M Mori M Fukazawa MTakeda and K Kadota 1998 Adenocarcinoma of thelung in a Steller sea lion (Eumetopias jubatus) J VetMed Sci 60 1349ndash1351

26 Sato T T Higuchi H Shibuya S Ohba S No-gami W Shirai H Watanabe and S Honda 2002 Lin-gual squamous cell carcinoma in a California sea lion(Zalophus californianus) J Zoo Wildl Med 33 367ndash370

27 Stedham M A H W Casey and M C Keyes1977 Lymphosarcoma in an infant northern fur seal (Cal-lorhinus ursinus) J Wildl Dis 13 176ndash179

28 Stroud R K and D R Stevens 1980 Lympho-sarcoma in a harbor seal (Phoca vitulina richardii) JWildl Dis 16 267ndash270

29 Zabka T S E L Buckles F M Gulland M Hau-lena D K Naydan and L J Lowenstine 2004 Pleo-morphic rhabdomyosarcoma with pulmonary metastasis ina stranded Steller (northern) sea lion (Eumetopias juba-tus) J Comp Pathol 130 195ndash198

Received for publication 20 May 2006

327LABRUT ET ALmdashPRIMARY MENINGEAL LYMPHOMA IN A HARBOR SEAL

Figure 4 Brain and meninges of a harbor seal demonstrating that most of the neoplastic cells are positive forimmunostaining with the polyclonal antibody directed against CD3 (insert in higher magnification) Avidinndashbiotinndashperoxidase complex method hematoxylin counterstain 630

LITERATURE CITED

1 Acevedo-Whitehouse K A F Constantino-CasasD Aurioles-Gamboa H A Rodriguez-Martinez and CR Godinez-Reyes 1999 Hepatic carcinoma with spleenmetastasis in a California sea lion from the Gulf of Cali-fornia J Wildl Dis 35 565ndash568

2 Aschfalk A and L N Bacciarini 2002 Carcinoidin the lung of a hooded seal (Cystophora cristata) VetRec 151 770ndash772

3 Baker J R 1989 Pollution-associated uterine le-sions in grey seals from the Liverpool Bay area of theIrish Sea Vet Rec 125 303

4 Bossart G D R Ewing A J Herron C Cray BMase S J Decker J W Alexander and N H Altman1997 Immunoblastic malignant lymphoma in dolphinshistologic ultrastructural and immunohistochemical fea-tures J Vet Diagn Invest 9 454ndash458

5 Britt J O Jr J G Simpson and E B Howard1984 Malignant lymphoma of the meninges in two dogsJ Comp Pathol 94 45ndash53

6 Brown R J A W Smith and M C Keyes 1975

Renal fibrosarcoma in the northern fur seal J Wildl Dis11 23ndash25

7 Callanan J J B A Jones J Irvine B J WillettI A McCandlish and O Jarrett 1996 Histologic clas-sification and immunophenotype of lymphosarcomas incats with naturally and experimentally acquired feline im-munodeficiency virus infections Vet Pathol 33 264ndash272

8 De Guise S A Lagace and P Beland 1994 Tu-mors in St Lawrence beluga whales (Delphinapterus leu-cas) Vet Pathol 31 444ndash449

9 Fauquier D F Gulland M Haulena and T Spraker2003 Biliary adenocarcinoma in a stranded northern el-ephant seal (Mirounga angustirostris) J Wildl Dis 39723ndash726

10 Fondevila D M Vilafranca and M Pumarola1998 Primary central nervous system T-cell lymphoma ina cat Vet Pathol 35 550ndash553

11 Frosch M D Anthony and U De Girolami 2005The central nervous system In Kumar V A Abbas andN Fausto (eds) Robbins and Cotran Pathologic Basis of

328 JOURNAL OF ZOO AND WILDLIFE MEDICINE

Disease 7th ed Elsevier Philadelphia Pennsylvania Pp1347ndash1419

12 Griner L A 1971 Malignant leukemic lymphomain two harbor seals (Phoca vitulina geronimensis) Am JVet Res 32 827ndash830

13 Gulland F M J G Trupkiewicz T R Sprakerand L J Lowenstine 1996 Metastatic carcinoma of prob-able transitional cell origin in 66 free-living California sealions (Zalophus californianus) 1979 to 1994 J WildlDis 32 250ndash258

14 Landy R 1980 A review of neoplasia in marinemammals In Montali R and G Migaki (eds) TheComparative Pathology of Zoo Animals Smithsonian In-stitution Press Washington DC Pp 563ndash573

15 Lester G D R J MacKay and B Smith-Meyer1992 Primary meningeal lymphoma in a horse J AmVet Med Assoc 201 1219ndash1221

16 Marsh W L Jr D R Stevenson and H J Long1983 Primary leptomeningeal presentation of T-cell lym-phoma Report of a patient and review of the literatureCancer 51 1125ndash1131

17 Martineau D K Lemberger A Dallaire P La-belle T P Lipscomb P Michel and I Mikaelian 2002Cancer in wildlife a case study Beluga from the StLawrence estuary Quebec Canada Environ Health Per-spect 110 285ndash292

18 Matsuda M S Hashiura Y Une H Sirouzu andY Nomura 2003 Two distinct carcinomas of mammarygland origin in a California sea lion J Wildl Dis 39241ndash243

19 Mawdesley-Thomas L E 1971 An ovarian tu-mour in a southern elephant seal (Mirounga leonina) VetPathol 8 9ndash15

20 Mawdesley-Thomas L E and W N Bonner1971 Uterine tumours in a grey seal (Halichoerus gry-pus) J Pathol 103 205ndash208

21 Menniti A L Moschettoni G Liccardo and PLunardi 2005 Low-grade primary meningeal lymphomacase report and review of the literature Neurosurg Rev28 229ndash233

22 Mikaelian I D Leclair and J Inukpuk 2001 Ad-enocarcinoma of the small intestine in a ringed seal fromHudson Bay J Wildl Dis 37 379ndash382

23 Osborn K 1988 Leukemic lymphoma in harborseals (Phoca vitulina) report of three cases occurring overtwo years and discussion of pathogenesis Annu ConfAm Assoc Zoo Vet 1988 96

24 Pernot P P Saint-Blancard R Dulou E Blondetand O Goasguen 2002 Primary dural lymphoma A casereport Neurochirurgie 48 124ndash127

25 Sato S H Kitamura M Mori M Fukazawa MTakeda and K Kadota 1998 Adenocarcinoma of thelung in a Steller sea lion (Eumetopias jubatus) J VetMed Sci 60 1349ndash1351

26 Sato T T Higuchi H Shibuya S Ohba S No-gami W Shirai H Watanabe and S Honda 2002 Lin-gual squamous cell carcinoma in a California sea lion(Zalophus californianus) J Zoo Wildl Med 33 367ndash370

27 Stedham M A H W Casey and M C Keyes1977 Lymphosarcoma in an infant northern fur seal (Cal-lorhinus ursinus) J Wildl Dis 13 176ndash179

28 Stroud R K and D R Stevens 1980 Lympho-sarcoma in a harbor seal (Phoca vitulina richardii) JWildl Dis 16 267ndash270

29 Zabka T S E L Buckles F M Gulland M Hau-lena D K Naydan and L J Lowenstine 2004 Pleo-morphic rhabdomyosarcoma with pulmonary metastasis ina stranded Steller (northern) sea lion (Eumetopias juba-tus) J Comp Pathol 130 195ndash198

Received for publication 20 May 2006

328 JOURNAL OF ZOO AND WILDLIFE MEDICINE

Disease 7th ed Elsevier Philadelphia Pennsylvania Pp1347ndash1419

12 Griner L A 1971 Malignant leukemic lymphomain two harbor seals (Phoca vitulina geronimensis) Am JVet Res 32 827ndash830

13 Gulland F M J G Trupkiewicz T R Sprakerand L J Lowenstine 1996 Metastatic carcinoma of prob-able transitional cell origin in 66 free-living California sealions (Zalophus californianus) 1979 to 1994 J WildlDis 32 250ndash258

14 Landy R 1980 A review of neoplasia in marinemammals In Montali R and G Migaki (eds) TheComparative Pathology of Zoo Animals Smithsonian In-stitution Press Washington DC Pp 563ndash573

15 Lester G D R J MacKay and B Smith-Meyer1992 Primary meningeal lymphoma in a horse J AmVet Med Assoc 201 1219ndash1221

16 Marsh W L Jr D R Stevenson and H J Long1983 Primary leptomeningeal presentation of T-cell lym-phoma Report of a patient and review of the literatureCancer 51 1125ndash1131

17 Martineau D K Lemberger A Dallaire P La-belle T P Lipscomb P Michel and I Mikaelian 2002Cancer in wildlife a case study Beluga from the StLawrence estuary Quebec Canada Environ Health Per-spect 110 285ndash292

18 Matsuda M S Hashiura Y Une H Sirouzu andY Nomura 2003 Two distinct carcinomas of mammarygland origin in a California sea lion J Wildl Dis 39241ndash243

19 Mawdesley-Thomas L E 1971 An ovarian tu-mour in a southern elephant seal (Mirounga leonina) VetPathol 8 9ndash15

20 Mawdesley-Thomas L E and W N Bonner1971 Uterine tumours in a grey seal (Halichoerus gry-pus) J Pathol 103 205ndash208

21 Menniti A L Moschettoni G Liccardo and PLunardi 2005 Low-grade primary meningeal lymphomacase report and review of the literature Neurosurg Rev28 229ndash233

22 Mikaelian I D Leclair and J Inukpuk 2001 Ad-enocarcinoma of the small intestine in a ringed seal fromHudson Bay J Wildl Dis 37 379ndash382

23 Osborn K 1988 Leukemic lymphoma in harborseals (Phoca vitulina) report of three cases occurring overtwo years and discussion of pathogenesis Annu ConfAm Assoc Zoo Vet 1988 96

24 Pernot P P Saint-Blancard R Dulou E Blondetand O Goasguen 2002 Primary dural lymphoma A casereport Neurochirurgie 48 124ndash127

25 Sato S H Kitamura M Mori M Fukazawa MTakeda and K Kadota 1998 Adenocarcinoma of thelung in a Steller sea lion (Eumetopias jubatus) J VetMed Sci 60 1349ndash1351

26 Sato T T Higuchi H Shibuya S Ohba S No-gami W Shirai H Watanabe and S Honda 2002 Lin-gual squamous cell carcinoma in a California sea lion(Zalophus californianus) J Zoo Wildl Med 33 367ndash370

27 Stedham M A H W Casey and M C Keyes1977 Lymphosarcoma in an infant northern fur seal (Cal-lorhinus ursinus) J Wildl Dis 13 176ndash179

28 Stroud R K and D R Stevens 1980 Lympho-sarcoma in a harbor seal (Phoca vitulina richardii) JWildl Dis 16 267ndash270

29 Zabka T S E L Buckles F M Gulland M Hau-lena D K Naydan and L J Lowenstine 2004 Pleo-morphic rhabdomyosarcoma with pulmonary metastasis ina stranded Steller (northern) sea lion (Eumetopias juba-tus) J Comp Pathol 130 195ndash198

Received for publication 20 May 2006