Pathology in Practice

CPT Caitlin M. Culligan 1Department of Biomedical and Diagnostic Sciences, College of Veterinary Medicine, University of Tennessee, Knoxville, TN 37996.

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Linden E. Craig 1Department of Biomedical and Diagnostic Sciences, College of Veterinary Medicine, University of Tennessee, Knoxville, TN 37996.

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History

A 37-year-old 2.0-kg (4.4-lb) sexually intact female African penguin (Spheniscus demersus) was found dead following a 2-day period of isolation from its exhibit mates as a consequence of recent conspecific-induced trauma that resulted in abrasions around its beak and forehead. The penguin had a history of degenerative joint disease, respiratory tract issues, and wounds inflicted by other penguins, but had not had any health issues during the preceding 2 to 3 years. The penguin had no other obvious problems and none of its exhibit mates had signs of illness.

Gross Necropsy Findings

Necropsy revealed marked pectoral muscle atrophy. The liver, lungs, and bone marrow were diffusely black (Figure 1). There were multifocal to coalescing, pinpoint to 1-mm-diameter, black spots on the epicardium as well as on the thyroid gland, parathyroid glands, pancreas, kidneys, brain, ovaries, and mucosal surface of the trachea. On cross section of the brain, there were bilaterally symmetric areas of black discoloration.

Figure 1—
Figure 1—

Photographs obtained at necropsy of a 37-year-old African penguin (Spheniscus demersus) that was found dead following a 2-day period of isolation from its exhibit mates because of conspecific-induced abrasions of the beak and forehead. A—The liver (red star) and lungs (white star) are diffusely black and there are pinpoint black spots on the epicardium. B—In cut section, the bone marrow of the right femur is diffusely black. C—There are black spots on the brain, particularly on the cerebellum (arrow).

Citation: Journal of the American Veterinary Medical Association 257, 4; 10.2460/javma.257.4.383

Formulate differential diagnoses from the history, clinical findings, and Figure 1—then turn the page →

Histopathologic Findings

Microscopically, the hepatic architecture was markedly effaced by numerous polygonal to spindle-shaped cells that contained numerous dark brown intracytoplasmic granules. These cells had indistinct cell borders, a moderate amount of cytoplasm that frequently contained numerous dark brown intracytoplasmic granules, and a round nucleus with stippled chromatin. Anisocytosis and anisokaryosis were moderate to marked, and mitotic figures were rare (Figure 2). The lung tissue was diffusely infiltrated by neoplastic cells similar to those in the liver. The neoplastic cells in the brain had a more perivascular distribution (Figure 3). Neoplastic cell infiltration of the myocardium and endocardium of the heart, tracheal mucosa, thyroid gland, bone marrow, pancreas, parathyroid glands, and scattered follicles of the ovaries and expansion of the renal interstitium of the kidneys were evident. No neoplastic cells were detected in sections of the skin.

Figure 2—
Figure 2—

Photomicrograph of a section of the liver of the penguin in Figure 1. Notice the marked effacement of the hepatic architecture by neoplastic cells containing dark brown intracytoplasmic granules. H&E stain; bar = 20 μm.

Citation: Journal of the American Veterinary Medical Association 257, 4; 10.2460/javma.257.4.383

Figure 3—
Figure 3—

Photograph (A) and photomicrograph (B) of a section of the brain of the penguin in Figure 1. On cut section, the brain has a bilaterally symmetric distribution of black discolorations. In the tissue section, the perivascular distribution of neoplastic cells is evident. H&E stain; bar = 50 μm.

Citation: Journal of the American Veterinary Medical Association 257, 4; 10.2460/javma.257.4.383

Morphologic Diagnosis and Case Summary

Morphologic diagnosis and case summary: disseminated malignant melanoma (affecting the brain, heart, lungs, liver, kidneys, trachea, thyroid and parathyroid glands, pancreas, bone marrow, and ovaries) in an African penguin.

Comments

Unlike the case in other avian species, malignant melanomas are common and an important cause of morbidity and death in captive penguins.1 These aggressive neoplasms have a high metastatic rate and typically originate from the skin of the foot or tarsus, from the subcutaneous muscle near the beak and oral cavity, or, less commonly, from the skin of the inguinal region.1,2 These tumors appear grossly as heavily pigmented, raised masses that become ulcerated over time. Microscopically, the neoplastic melanocytes are generally round to polygonal, but can be fusiform, and are heavily pigmented. There have been multiple reports of external malignant melanomas in penguins. However, in the bird of the present report, there were no external pigmented masses. The skin lesions caused by conspecific trauma were examined microscopically but did not contain neoplastic cells.

Malignant melanomas in other avian species, including ducks, parrots, raptors, and chickens, have been reported.2–4 In chickens, these neoplasms can originate from the viscera where they also have high metastatic rates despite low mitotic indices, and tend to efface the normal architecture of the affected organs.5 Chickens, as well as penguins, can have melanin pigment within their viscera, and these melanocytes can serve as points of origin for melanocytic neoplasms. To our knowledge, there is no published description of primary malignant melanoma originating from the viscera in a penguin, but that could be what occurred in the bird of the present report. However, the visceral organ that was the primary site could not be identified.

In humans, and potentially in chickens, UV light exposure is a risk factor for the development of malignant melanomas.6 However, in penguins, UV light exposure is not considered to be a risk factor. In a study by Duncan et al,1 the roles of UV light, age of the birds, viral pathogens, and chemical carcinogens in the development of malignant melanomas in penguins were examined. Of these factors, only advanced age was found to substantially influence the development of malignant melanomas in penguins. The bird of the present report was 37 years old; the lifespan of a captive African penguin is typically 30 years. Advanced age is also considered a risk factor for development of melanoma in horses, particularly in gray horses owing to a genetic mutation that affects their pigmentation.7,8 Melanomas in horses resemble dermal melanocytomas known as blue nevi in humans and generally are less likely to be malignant, compared with melanomas in other domestic species, because of gray horse-specific genetic characteristics that inhibit metastatic processes.7,9 In dogs, malignant melanoma is a common neoplasm that develops in the oral cavity; older dogs, especially Scottish Terriers, Golden Retrievers, Poodles, and Dachshunds,10,11 are more commonly affected.

A diagnosis of malignant melanoma is usually made on the basis of the morphologic features and pigmentation of neoplastic cells observed histologically in sections of affected tissues. In the bird of the present report, the diagnosis of malignant melanoma was easily made on the basis of the gross and histologic findings. Conversely, for neoplasms that are poorly pigmented or amelanotic, immunohistochemical analysis for PNL-2, a common melanocytic marker, has been shown to be highly useful.12 In 1 study,1 immunohistochemical analysis for PNL-2 in all primary and metastatic lesions of malignant melanomas in penguins yielded positive results, and this marker is considered to be the most sensitive for detection of melanocytic tumors in penguins.

References

  • 1. Duncan AE, Smedley R, Anthony S, et al. Malignant melanoma in the penguin: characterization of the clinical, histological, and immunohistochemical features of malignant melanoma in 10 individuals from three species of penguin. J Zoo Wildl Med 2014;45:534549.

    • Crossref
    • Search Google Scholar
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  • 2. Reid HA, Herron AJ, Hines ME II, et al. Metastatic malignant melanoma in a Mandarin duck (Aix galericulata). Avian Dis 1993;37:11581162.

  • 3. Shrader TC, Carpenter JW, Cino-Ozuna AG, et al. Malignant melanoma of the syrinx and liver in an African grey parrot (Psittacus erithacus erithacus). J Avian Med Surg 2016;30:165171.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4. Kufuor-Mensah E, Watson GL. Malignant melanoma in a penguin (Eudyptes chrysolophus) and a red-tailed hawk (Buteo jamaicensis). Vet Pathol 1992;29:354356.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5. Williams SM, Zavala G, Collett SR, et al. Metastatic melanomas in young broiler chickens (Gallus gallus domesticus). Vet Pathol 2012;49:288291.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6. Hacker E, Boyce Z, Kimlin MG, et al. The effect of MC1R variants and sunscreen on the response of human melanocytes in vivo to ultraviolet radiation and implications for melanoma. Pigment Cell Melanoma Res 2013;26:835844.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7. Seltenhammer MH, Heere-Ress E, Brandt S, et al. Comparative histopathology of grey-horse-melanoma and human malignant melanoma. Pigment Cell Res 2004;17:674681.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. Curik I, Druml T, Seltenhammer M, et al. Complex inheritance of melanoma and pigmentation of coat and skin in grey horses. PLoS Genet 2013;9:e1003248.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9. Seltenhammer MH, Simhofer H, Scherzer S, et al. Equine melanoma in a population of 296 grey Lipizzaner horses. Equine Vet J 2003;35:153157.

    • Search Google Scholar
    • Export Citation
  • 10. Bergman PJ. Canine oral melanoma. Clin Tech Small Anim Pract 2007;22:5560.

  • 11. Dennis MM, Ehrhart N, Duncan CG, et al. Frequency of and risk factors associated with lingual lesions in dogs: 1,196 cases (1995–2004). J Am Vet Med Assoc 2006;228:15331537.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12. Rambaud YF, Flach EJ, Freeman KP. Malignant melanoma in a Humboldt penguin (Spheniscus humbolti). Vet Rec 2003;153:217218.

  • Figure 1—

    Photographs obtained at necropsy of a 37-year-old African penguin (Spheniscus demersus) that was found dead following a 2-day period of isolation from its exhibit mates because of conspecific-induced abrasions of the beak and forehead. A—The liver (red star) and lungs (white star) are diffusely black and there are pinpoint black spots on the epicardium. B—In cut section, the bone marrow of the right femur is diffusely black. C—There are black spots on the brain, particularly on the cerebellum (arrow).

  • Figure 2—

    Photomicrograph of a section of the liver of the penguin in Figure 1. Notice the marked effacement of the hepatic architecture by neoplastic cells containing dark brown intracytoplasmic granules. H&E stain; bar = 20 μm.

  • Figure 3—

    Photograph (A) and photomicrograph (B) of a section of the brain of the penguin in Figure 1. On cut section, the brain has a bilaterally symmetric distribution of black discolorations. In the tissue section, the perivascular distribution of neoplastic cells is evident. H&E stain; bar = 50 μm.

  • 1. Duncan AE, Smedley R, Anthony S, et al. Malignant melanoma in the penguin: characterization of the clinical, histological, and immunohistochemical features of malignant melanoma in 10 individuals from three species of penguin. J Zoo Wildl Med 2014;45:534549.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2. Reid HA, Herron AJ, Hines ME II, et al. Metastatic malignant melanoma in a Mandarin duck (Aix galericulata). Avian Dis 1993;37:11581162.

  • 3. Shrader TC, Carpenter JW, Cino-Ozuna AG, et al. Malignant melanoma of the syrinx and liver in an African grey parrot (Psittacus erithacus erithacus). J Avian Med Surg 2016;30:165171.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4. Kufuor-Mensah E, Watson GL. Malignant melanoma in a penguin (Eudyptes chrysolophus) and a red-tailed hawk (Buteo jamaicensis). Vet Pathol 1992;29:354356.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5. Williams SM, Zavala G, Collett SR, et al. Metastatic melanomas in young broiler chickens (Gallus gallus domesticus). Vet Pathol 2012;49:288291.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6. Hacker E, Boyce Z, Kimlin MG, et al. The effect of MC1R variants and sunscreen on the response of human melanocytes in vivo to ultraviolet radiation and implications for melanoma. Pigment Cell Melanoma Res 2013;26:835844.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7. Seltenhammer MH, Heere-Ress E, Brandt S, et al. Comparative histopathology of grey-horse-melanoma and human malignant melanoma. Pigment Cell Res 2004;17:674681.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. Curik I, Druml T, Seltenhammer M, et al. Complex inheritance of melanoma and pigmentation of coat and skin in grey horses. PLoS Genet 2013;9:e1003248.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9. Seltenhammer MH, Simhofer H, Scherzer S, et al. Equine melanoma in a population of 296 grey Lipizzaner horses. Equine Vet J 2003;35:153157.

    • Search Google Scholar
    • Export Citation
  • 10. Bergman PJ. Canine oral melanoma. Clin Tech Small Anim Pract 2007;22:5560.

  • 11. Dennis MM, Ehrhart N, Duncan CG, et al. Frequency of and risk factors associated with lingual lesions in dogs: 1,196 cases (1995–2004). J Am Vet Med Assoc 2006;228:15331537.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12. Rambaud YF, Flach EJ, Freeman KP. Malignant melanoma in a Humboldt penguin (Spheniscus humbolti). Vet Rec 2003;153:217218.

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