Conference 23 - 2013 Case: 03 20140423

Signalment:

Mature adult unknown gender Atlantic Salmon, (Salmo salar). These fish are from a research facility where they are held in 1500L tanks at approximately 12oC, pH of ~8, nitrogen gas saturation ~100 % and oxygen at 80 % saturation. Tissues were collected during end of study post-mortem examinations on extra salmon. The study duration was no greater than 24 months.

Gross Description:

The right pseudobranch was swollen and mottled.

Histopathologic Description:

Expanding and effacing the pseudobranch is a non-encapsulated, well demarcated, expansile, highly cellular mass composed of three haphazardly intermingled cellular populations embedded in small amounts of dense fibrous stroma. These cell populations consist of dense aggregates of basophilic blastemal cells, polygonal to cuboidal epithelial cells and islands of cartilage. Epithelial populations often consist of cuboidal cells which sometimes form structures resembling branchial lamellae. In other areas, dense cords and trabeculae of epithelial cells often are intermingled with numerous round cells with small dense, eccentrically located nuclei which are compressed against the cell margins by moderate amounts of pink, round cytoplasm (interpreted as mucous producing goblet cells). Blastemal cells are round to slightly spindloid, darkly basophilic and have sparse, poorly defined, cytoplasm, round to ovoid, dark nuclei with finely stippled chromatin and unapparent to small, nucleoli. Islands of cartilage are often surrounded by concentric layers of thin spindloid cells with scant, poorly defined, pale basophilic cytoplasm, fusiform, nuclei with finely stippled chromatin and unapparent nucleoli. The mitotic rate is 10 figures noted in ten randomly selected fields at high power objective (40x) with mitotic figures only observed within the epithelial populations. Multifocal aggregates of lymphocytes and granular leucocytes are present at the periphery of the mass.

Morphologic Diagnosis:

Pseudobranch: Branchioblastoma.

Condition:

Branchioblastoma

Contributor Comment:

There is increasing interest in the use of fish as models for carcinogenicity studies as well as ecosystem monitors within the environment.(6,7) Neoplasms of the gill and pseudobranch are rare compared to other locations such as the skin or liver, but have been previously described in koi carp (Cyprinus carpio).(3) To the authors knowledge, it has not been previously reported in Atlantic salmon (Salmo salar).

Branchioblastoma is a tumor of embryologic blast-type cells with mesenchymal and epithelial components. It is histologically considered a benign tumor because it is expansile and often well demarcated. However, the mass can interfere with gaseous exchange in the gill with potentially fatal consequences. Affected fish may present with respiratory distress, an inability to close their mouth or multilobulated mass/masses appearing to originate from a gill arch or the pseudo branch.(3)

Select differentials for a multilobular lesion in the region of the operculum, gill and oral cavity may include granulomatous or inflammatory lesions due to infection by bacteria (eg. Mycobacterium sp.), fungi (eg. Banchiomyces), microsporidia (eg. Loma sp.), myxozoa (eg. Myxobolus sp.), branchial trematodes, and iridovirus (eg. lymphocystis).

Neoplasia in fish is likely multifactorial and has previously been associated with exposure to carcinogens,(6) genetic causes,(5) and retrovirus infection.(1) No underlying cause was identified in this case.

JPC Diagnosis:

Pseudobranch: Branchioblastoma.

Conference Comment:

The pseudobranch is not found in all fish species, but where present it is a red, gill-like tissue attached to the internal surface of the operculum. It is composed of cartilage-supported parallel blood capillaries that create a counter-current system which likely functions to increase oxygen uptake. The pseudobranch has a direct vascular connection with the ocular choroid, which is composed of similar capillary arrays alternating with rows of slender fibroblast-like cells; it may also play a role in the filling of the air bladder.(4)

In addition to branchioblastoma, which can arise from the gill or the pseudobranch and may be spontaneous or carcinogen-induced,(3) conference participants briefly discussed teratoma as a rule-out with similar histological features. Branchioblastoma, as noted by the contributor, is composed of embryologic blast-type cells with mesenchymal and epithelial components; similarly, teratomas are classically defined as having at least two of the three embryonic layers- endoderm, mesoderm, and ectoderm (see WSC 2013-2014, conference 8, case 2). Teratomas occur most frequently in the gonads; however, these tumors can also develop at extragonadal locations, usually along the midline.(2) They are rarely (if ever) reported in fish. The moderator points out that branchioblastoma and teratoma have analogous etiopathogeneses; however, the neoplastic cell types comprising branchioblastomas are appropriate to the anatomic location (i.e. this tumor appears to be attempting to form normal gill tissue in a relatively normal location), while teratomas tend to produce poorly differentiated, disorganized tissue that does not belong (i.e. foci of squamous epithelium, bone and tooth within the gonad). Based on these broad attributes, this neoplasm is most consistent with a branchioblastoma.

References:

1. Coffee L, Casey J, Bowser P. Pathology of tumors in fish associated with retroviruses: a review. Vet Pathol. 2013;50:390-403.

2. Foster RA. Male reproductive system. In: McGavin MD, Zachary JF, eds. Pathologic Basis of Veterinary Disease. 5th ed. St. Louis, MO: Elsevier; 2012:1142-1143.

3. Kn+â-+sel R. Brandes R, Lechleiter S, Schmidt-Posthaus H. Two independent cases of spontaneously occurring branchioblastomas in koi carp (Cyprinus carpio). Vet Pathol. 2007;44:237-239.

4. Mumford S, Heidel J, Smith C, Morrison J, MacConnell B, Blazer V. Fish Histology and Histopathology. US Fish and Wildlife Service, National Conservation Training Center. http://nctc.fws.gov/resources/course-resources/fish-histology/index.html . Accessed April 26, 2014.

5. Shin J, Padmanabhan A, de Groh E, Lee J-S, Haidar S, Dahlberg S, et al. Zebrafish neurofibromatosis type 1 genes have redundant functions in tumorigenesis and embryonic development. Dis Model Mechan. 2012;5:881-894.

6. Williams D, Bailey G, Reddy A, Hendricks J, Oganesian A, Orner G, et al. The rainbow trout (Oncorhynchus mykiss) tumor model: recent applications in low-dose exposures to tumor initiators and promoters. Toxicol Pathol. 2003;31:58-61.

7. Wirgin I, Waldman J. Altered gene expression and genetic damage in North American fish populations. Mutation Res. 1998;399:193-219.