Pathology of Laboratory Fishes

7/22/2013 Pathology of Laboratory Fishes Jeffrey C. Wolf, DVM, DACVP Experimental Pathology Laboratories (EPL®), Inc. Sterling, VA What are Laborato...
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7/22/2013

Pathology of Laboratory Fishes Jeffrey C. Wolf, DVM, DACVP Experimental Pathology Laboratories (EPL®), Inc. Sterling, VA

What are Laboratory Fishes?

• Nearly any fish can be a laboratory fish

What are Laboratory Fishes?

• Nearly any fish can be a laboratory fish • >32,000 fish species • There are more fish diseases than you want to learn!

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Excluded (with some notable exceptions): • Food fishes • Foreign laboratory fishes • Marine fishes • Wild fishes • Silverfish • The band Phish • Popular fish snacks

Common Laboratory Fish in U.S. • Zebrafish • Japanese medaka • Fathead minnow • Guppy • Goldfish • Rainbow trout • Channel catfish • Nile tilapia

Common Laboratory Fish in U.S. • Zebrafish • Japanese medaka

-- very hardy and prolific

• Fathead minnow

-- U.S. native species -- externally dimorphic

• Guppy

-- livebearer

• Goldfish

-- represent coldwater fishes

• Rainbow trout • Channel catfish

-- larger model -- surrogate for Atlantic salmon -- representative catfish species

• Nile tilapia

-- also represents ornamental tropical fish

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Focus on: • Diseases likely to be encountered in laboratory setting • A few classic diseases (for you board prep types)

• Of the vast majority of fish that I evaluate in toxicologic studies, relatively few have any evidence of background disease • Far and away, the most common disease that you will encounter in laboratory fishes is …

The 800 lb acid-fast gorilla of fish research…

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striped bass: pale, lumpy, enlarged spleen due to granulomatous splenitis

striped bass kidney (Ziel-Neelsen stain): granulomas with acid-fast bacterial rods

Mycobacterium spp. (Piscine Tuberculosis) striped bass: pale, lumpy, enlarged spleen due to granulomatous splenitis

striped bass kidney (Ziel-Neelsen stain): granulomas with acid-fast bacterial rods

Mycobacterium spp. (Piscine Tuberculosis) • Gram-positive acid-fast rods; M. marinum, M. chelonei, M. fortuitum, M. abscessus, M. peregrinum • Virtually all fishes can be affected (although some species more susceptible than others) • Long latent period, low level mortalities • Numerous variably-sized granulomas in various tissues, often with necrotic centers • Relatively resistant fish species may have diffuse granulomatous inflammation

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Japanese medaka spleen: diffuse granulomatous inflammation

Japanese medaka kidney: numerous acid-fast bacilli

Mycobacterium spp. (Piscine Tuberculosis) • Gram-positive acid-fast rods; M. marinum, M. chelonei, M. fortuitum, M. abscessus, M. peregrinum • Virtually all fishes can be affected (although some species more susceptible than others) • Long latent period, low level mortalities • Numerous variably-sized granulomas in various tissues, often with necrotic centers • Relatively resistant fish species may have diffuse granulomatous inflammation • Ubiquitous, no cure, difficult to eradicate from infected populations and environment • Culture tricky; some labs have PCR assays • Zoonotic disease

channel catfish: caudal dermal necrosis

channel catfish: gill necrosis

channel catfish: gill necrosis

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Flavobacterium columnare (Columnaris Disease)

channel catfish: caudal dermal necrosis

channel catfish: gill necrosis

channel catfish: gill necrosis

Flavobacterium columnare (Columnaris Disease) • Gram-negative filamentous rods; Formerly known as Flexibacter columnaris or Cytophaga columnaris • Ubiquitous on fish surface and in aquaria • Serious, highly communicable disease of young salmonids, catfish and many other fishes • Associated with stress, predisposing factors include high water temperature, crowding, injury, and poor water quality (e.g., low O2, high ammonia) • Caudal and anal fins may become severely eroded • Caudal trunk skin sometimes involved: “saddleback disease” • Gills common site, and may be only affected area • Responsive to some water bath treatments

Flavobacterium columnare (Columnaris Disease)

wet mount of skin scraping: bacteria form “haystacks”

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goldfish: deep ulcers

salmon: deep dermal and muscle ulcers

salmon kidney: necrosis with intralesional gram-negative bacteria

Aeromonas salmonicida (Goldfish Ulcer Disease)

goldfish: deep ulcers

salmon: deep dermal and muscle ulcers

salmon kidney: necrosis with intralesional gram-negative bacteria

Aeromonas salmonicida (Goldfish Ulcer Disease) • Gram-negative non-motile short rods; obligate pathogen, but can survive for long periods off host • Subcutaneous swelling leads to ulcerative dermatitis • Chronic disease in salmonids called “furunculosis” • Splenomegaly, renomegaly, and ascites • Necrosis of affected tissues with abundant bacterial colonies and few inflammatory cells due to leukocytolytic endotoxin • Transmission by direct contact with diseased fish, contaminated water, fomites, and infected eggs

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tilapia: ophthalmitis

tilapia: peri- and myocarditis

tilapia: meningitis

tilapia: Gram+ cocci/diplococci

Streptococcus sp. , e.g., S. iniae

tilapia: ophthalmitis

tilapia: peri- and myocarditis

tilapia: meningitis

tilapia: Gram+ cocci/diplococci

Streptococcus sp. , e.g., S. iniae • Primarily beta-hemolytic streptococci • A major problem in the tilapia industry, and occasionally affects other fishes • Associated with overcrowding and poor water quality in recirculating culture systems • Either acute fulminating septicemia, or chronic form limited primarily to the CNS • Granulomatous meningoencephalitis, polyserositis, epicarditis, myocarditis, and/or cellulitis • Should routinely culture brain tissue if Strep suspected • Ubiquitous organism, and S. iniae is a potential zoonotic pathogen

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Streptococcus iniae: Zoonotic agent

actual S. iniae-infected patient with cellulitis

wound staged to make a point

Streptococcus sp. , e.g., S. iniae • Primarily beta-hemolytic streptococci • A major problem in the tilapia industry, and occasionally affects other fishes • Associated with overcrowding and poor water quality in recirculating culture systems • Either acute fulminating septicemia, or chronic form limited primarily to the CNS • Granulomatous meningoencephalitis, polyserositis, epicarditis, myocarditis, and/or cellulitis • Should routinely culture brain tissue if Strep suspected • Ubiquitous organism, and S. iniae is a potential zoonotic pathogen • Latest tilapia pathogen: Francisella spp.

Classic Disease Alert

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exophthalmos

abdominal distention frontal bone necrosis peritonitis

focal hepatitis

Gram-negative rods in renal macrophages

focal hepatitis

Edwardsiella ictaluri (Enteric Septicemia of Catfish, Hole-in-the Head Disease of Catfish)

exophthalmos

abdominal distention frontal bone necrosis peritonitis

focal hepatitis

Gram-negative rods in renal macrophages

focal hepatitis

Edwardsiella ictaluri (Enteric Septicemia of Catfish, Hole-in-the Head Disease of Catfish) • Gram-negative motile pleomorphic curved rod • Most important disease of channel catfish, affects fingerlings and yearlings • Outbreaks seasonally dependent, occur when water temps are between 24-28oC • Bacteria enter via nasal route, results in chronic infection of the olfactory lobe of the brain that causes necrosis of overlying bone • Also enteritis, hepatitis, myositis, and interstitial nephritis; acute and chronic forms • Can survive for long periods in pond mud and may be latent in the gut of asymptomatic catfish

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zebrafish: aberrant swimming

zebrafish: brainstem

zebrafish: spinal cord

zebrafish: spinal nerve

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Pseudoloma neurophilium (Microsporidiosis)

zebrafish: spinal cord

zebrafish: spinal nerve

Pseudoloma neurophilium (Microsporidiosis) • • • •

Gram-positive intracellular obligate organism Lately classified with fungi rather than protista Direct transmission Most zebrafish colonies in U.S. are affected, although SPF zebrafish are available from Oregon State U • Causes neurologic impairment in spinal cord and myositis in epaxial musculature • No inflammation unless cysts (xenomas) rupture • Typical “bedroom slipper” appearance in wet mounts and histologic sections

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Pseudoloma neurophilium (Microsporidiosis) • • • • • • • •

Gram-positive intracellular obligate organism Lately classified with fungi rather than protista Direct transmission Most zebrafish colonies in U.S. are affected, although SPF zebrafish are available from OSU Causes neurologic impairment in spinal cord and myositis in epaxial musculature No inflammation unless cysts (xenomas) rupture Typical “bedroom slipper” appearance in wet mounts and histologic sections Spore coats are partially birefringent under polarized light

rabbits: encephalitis and ophthalmitis

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Encephalitozoon cuniculi

rabbits: encephalitis and ophthalmitis

fathead minnow: microsporidia in kidney

fathead minnow: microsporidia in ovary

Classic Disease Alert

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fingerling trout: black tails

fingerling trout: cartilage necrosis associated with parasitic spores fingerling trout: spinal deformity

Myxobolus cerebralis (Whirling Disease, Blacktail)

fingerling trout: black tails

fingerling trout: cartilage necrosis associated with parasitic spores fingerling trout: spinal deformity

Myxobolus cerebralis (Whirling Disease, Blacktail) • Myxozoan parasite; 10-micron oval spore with 2 piriform polar capsules • Salmonids (rainbow trout most susceptible; brown trout and Coho salmon are resistant) • Most severe in young trout from non-endemic areas; older trout have little cartilage for parasites to feed on, but instead function as carriers • Pigmentation changes are caused by damage to sympathetic nerves adjacent to the spine • Characteristic frantic tail-chasing behavior (whirling) that can be triggered by auditory stimuli or feeding • Whirling behaviors disappear in survivors, spinal deformities persist

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Myxobolus cerebralis (Whirling Disease, Blacktail)

polar capsules highlighted by Giemsa stain

tubifex worms important in life cycle

goldfish: severe abdominal distension

goldfish: massively swollen kidneys

Hofferellus carassii (Kidney Bloater Disease)

goldfish: massively swollen kidneys

goldfish: severe abdominal distension

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goldfish: diffuse granulomatous peritonitis

goldfish mesentery: numerous small protozoons with eccentric nuclei

Goldfish Amebiasis

goldfish mesentery: numerous small protozoons with eccentric nuclei

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Goldfish Amebiasis • Exact taxonomic status remains undetermined • Necrogranulomatous inflammation of abdominal cavity, kidney, heart, brain • Parasites very small (only ~2-4 microns) and have slightly eccentric nuclei • Typically located at edges of necrotic areas • Precise mode of transmission undetermined

Cyprinid Herpesviruses

Cyprinid Herpesviruses • Cyprinid Herpes 1 – Carp Pox – Self-limiting dermal lesions in carp and koi – Focal epidermal hyperplasia – Can see occasional Cowdry type A intranuclear inclusion bodies – Lesions regress in warm weather

• Cyprinid Herpes 2 – Hematopoietic necrosis virus of goldfish

carp skin: epidermal plaque

– Juvenile goldfish – Stressed fish during periods of elevated temperatures – Lesions in spleen, kidneys, gills

• Cyprinid Herpes 3 – Koi herpesvirus – Primarily swollen, necrotic gills – Reportable disease

goldfish spleen: karyomegalic inclusions

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Classic Disease Alert

Cichlid: white growth on fin

Walleye: white growths

Skin: markedly swollen dermal fibroblasts

Lymphocystis • Iridovirus that affects most fresh and saltwater fishes • Small white nodules to cauliflower-like growths • Fibroblasts undergo massive cytomegaly • Basophilic cytoplasmic inclusions surrounded by hyaline capsule • Gains entry through epidermal abrasions • Occasionally internal infections • Often self-limiting

Cichlid: white growth on fin

Walleye: white growths

Skin: markedly swollen dermal fibroblasts

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channel catfish: ulcers, secondary bacterial infection

channel catfish: focal epithelial proliferation causes white spots

Ichthyophthirius multifilis ("Ich" or White Spot Disease)

channel catfish: focal epithelial proliferation causes white spots

gills: large ciliate protozoon with macronucleus

channel catfish: ulcers, secondary bacterial infection

gills: large ciliate protozoon with macronucleus

Ichthyophthirius multifilis ("Ich" or White Spot Disease) • Largest protozoan parasite of fish: trophozoites up to 100 m diameter • Oval or horseshoe-shaped nucleus • Aquarium and hatchery-reared freshwater fish • Severely infected fish may succumb to respiratory impairment • Trophozoites in skin and gill surrounded by epithelial hyperplasia

epidermal hyperplasia

horseshoe-shaped macronucleus

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Ichthyophthirius multifilis ("Ich" or White Spot Disease)

Direct life cycle 1) Encysted trophozoites (trophonts) leave the fish and settle to the bottom of the tank 2) The trophozoites (tomonts) on the bottom of the tank divide into numerous tomites (theronts) 3) The motile theronts infect the skin of the fish

The life cycle takes approximately 4 days to complete. However, it can be shortened by increasing the water temperature

gill: free-swimming unattached ciliate protozoons

SEM: ciliate protozoon with denticular ring

Trichodina spp. (Trichodiniasis)

gill: free-swimming unattached ciliate protozoons

SEM: ciliate protozoon with denticular ring

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Trichodina spp. (Trichodiniasis) • Saucer-shaped, 50 micron diameter, peritrichal ciliated protozoans, that have a macro- and a micronucleus • Characteristic ring of interlocking denticles • Low numbers not always associated with disease • Can cause increased skin and gill mucus, respiratory distress • Simple life cycle, reproduces by binary fission

Trichodina spp. (Trichodiniasis)

Japanese medaka: trichodinids in urinary bladder

Japanese medaka: trichodinids in renal collecting ducts

gill wet mount: cyst-like structure

gill lamellae: individual epithelial cells distended with minute organisms

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Epitheliocystis (Chlamydia)

gill wet mount: cyst-like structure

gill lamellae: individual epithelial cells distended with minute organisms

Epitheliocystis (Chlamydia) • Obligate intracellular parasite; organisms stain red with Macchiavello stain • Affects many species of freshwater and marine fish • Grossly, multiple white nodules in gill lamellae and skin • Intact cysts rarely induce inflammation • Infected fish may be asymptomatic or show respiratory distress • Transmission mechanisms not well understood

Classic Disease Alert

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striped bass: cloudy ulcer

white mat out of water fungal hyphae

platy: cottony growth

Saprolegnia spp. (Water Molds) striped bass: cloudy ulcer

white mat out of water fungal hyphae

platy: cottony growth

Saprolegnia spp. (Water Molds) • Various groups of aquatic oomycete fungi: primarily Saprolegnia, Achlya, and Aphanomyces spp. • Affects all species and ages of freshwater and estuarine fish • Broad non-septate branching hyphae that produce motile flagellated zoospores • Most infections are secondary to trauma or primary pathogens • Saprolegnia spp. usually superficial, but other organisms (e.g., Aphanomyces spp.) can be invasive

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female medaka: massively swollen abdomen

Egg-bound Aged Female

female medaka: massively swollen abdomen

Egg-bound Aged Female • Seen in aged broodstock • Occurs due to lack of behavioral and/or hormonal triggers for ovulation (or occasionally oophoritis) • Egg mass often contains numerous atretic (degenerating) follicles • Leads to negative energy balance, starvation – Egg formation is energy intensive – Meanwhile, little room in abdomen for food intake

• Results in catabolism and atrophy of adipose tissue, skeletal and cardiac muscle, parenchymal and visceral organs • Very gradual progression

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skeletal muscle from normal female medaka

atrophic skeletal muscle from egg-bound female medaka

normal female medaka liver

severely atrophic liver from egg-bound female

yellow perch: skeletal muscle necrosis

yellow perch: spinal fractures

yellow perch: muscle atrophy

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Electrocution yellow perch: skeletal muscle necrosis

yellow perch: spinal fractures

yellow perch: muscle atrophy

Electrocution

yellow perch: spinal fractures

• Can occur naturally (lightening strike) or via human intervention (electroshock collecting, short circuits in aquaculture equipment) • Fish may have severe spinal curvature and still continue to feed • Histopath: – Acute: spinal fractures and myonecrosis – Chronic: denervation muscle atrophy, contralateral contraction

tilapia: clear bubbles in fins

tilapia: clear bubbles in viscera

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wet mount of fin: gas bubbles

Gas Bubble Disease • Due to supersaturation of the water by a gas (most often nitrogen) • Can occur naturally (e.g., heating of the water, photosynthesis) or in confinement systems (e.g., pump leaks allowing air to enter filtration system) • Signs include exophthalmia, with gas bubbles in the eyes, oral mucous membranes, gills and fins • Histologically, can see ocular lesions (cataracts, anterior synechia, and panophthalmitis) and ischemic necrosis of gill lamellae • Fish die due to asphyxiation caused by mechanical disruption of blood flow

wet mount of fin: gas bubbles

ventrolateral pharyngeal region: multilobular masses

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Thyroid Follicular Hyperplasia (Goiter)

ventrolateral pharyngeal region: multilobular masses

Thyroid Follicular Hyperplasia (Goiter) • Freshwater and marine fish (commercial salt solutions); certain species seem predisposed • Causes may include inadequate or excessive iodine, but more commonly due to substances in feed or water (goitrogens) that interfere with thyroid hormone homeostasis • Hyperplastic thyroids must be differentiated from follicular cell adenomas and rare thyroid carcinomas – Thyroid follicle proliferation in extra-pharyngeal locations does not necessarily indicate metastasis!

Kidney

Liver

Spleen

Eye

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Japanese medaka: thyroid follicular cell hyperplasia everywhere!

Adenoma Hyperplastic Thyroid

thyroid follicular cell carcinoma: compared to goiter, neoplasms are more anaplastic

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Kidney Tubules Hyperplastic Thyroid

Carcinoma Mitotic Figures

platyfish / swordtail hybrid: pigmented proliferations

Dark brown pigment in cytoplasm of pleomorphic spindle cells

Melanomas in Platyfish x Swordtail Hybrids

platyfish / swordtail hybrid: pigmented proliferations

Dark brown pigment in cytoplasm of pleomorphic spindle cells

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Melanomas in Platyfish x Swordtail Hybrids • Unique invasive melanomas occur in offspring when certain F1 hybrid platyfish/swordtails are crossed with swordtails • 25% frequency of melanomas when F1 generation hybrid females are back-crossed with wild-type swordtail males • Tumor development attributed to activity of a dominant-acting sex-linked oncogene: Xmrk – Ortholog of human EGFR gene – Full expression of Xmrk occurs when it is no longer inhibited by the suppressor gene Diff

• Important animal model for humans because there are no naturally occurring melanoma models in rodents

Pigment Cell Tumors of Fish • 3 types of pigment cells: – Melanophores • Dark brown pigment • Neoplasm: Melanoma (syn: Melanophoroma)

– Xanthophores • Red or yellow pigment • Neoplasm: Xanthophoroma (syn: Erythrophoroma)

– Iridophores • Silvery reflective platelets • Neoplasm: Iridophoroma (syn: Guanophoroma)

From Ostrander, 2000

Iridophoroma under polarized light

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female freshwater angelfish: proliferative lip lesion

Lip Fibromas (Fibropapillomas) of Angel Fish

female freshwater angelfish: proliferative lip lesion

Lip Fibromas (Fibropapillomas) of Angel Fish • Tumor of the mucocutaneous junction of the lips • Only adult female fish are affected • On cut sections, the tumors are solid white, or white with cavernous centers that contain clear fluid • Histologically, dense fibrovascular connective tissue arranged in whorls, streams and bundles, covered by a thick stratified squamous epithelium • The presence of deformed teeth in the some tumors has led to speculation that these may be odontogenic neoplasms • Cause is unknown; however a type "A" retrovirus was identified in affected tissue in one report • Laboratory transmission of the disease to other fish has not occurred

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zebrafish intestine: nematodes embedded in mucosa

zebrafish intestine: nematodes associated with mucosal epithelial hyperplasia and inflammation

Pseudocapillaria tomentosa

zebrafish intestine: nematodes associated with mucosal epithelial hyperplasia and inflammation

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Pseudocapillaria tomentosa • Third most problematic infection in zebrafish research facilities, after mycobacteriosis and microsporidiosis • Transmission occurs directly or via oligochaete worms (e.g., tubifex) • Diagnosis by visualization of oval eggs with bipolar plugs in fecal smears • Anthelmintic treatment possible but not well-tested, affected facilities tend to depopulate vs. treat • Presence of these worms has been associated with intestinal and biliary neoplasia

Kent, M.L., J. K. Bishop-Stewart, J. L. Matthews, and J.M. Spitsbergen. 2002. Pseudocapillaria tomentosa, a nematode pathogen of zebrafish (Danio rerio) kept in research colonies and associated neoplasms. Comp. Med. 52; 362-367.

Pseudocapillaria tomentosa

P. tomentosa-infected zebrafish intestine: mucinous adenocarcinoma

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Liver of P. tomentosa-infected zebrafish: cholangiocarcinoma

Liver of P. tomentosa-infected zebrafish: cholangiocarcinoma

Zebrafish abdomen: nodular mass between esophagus and heart

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Endocrine System: Anatomy & Physiology

Anterior Kidney Brain

Pharynx

Heart

Liver

Zebrafish, Midline Sagittal Section

Ultimobranchial Body Tumor

Zebrafish abdomen: nodular mass between esophagus and heart

Ultimobranchial Body Tumor

• Spontaneous neoplasm of older (>1.5 years) zebrafish, primarily males • Certain zebrafish lines predisposed • Can be up to 50x the size of the normal gland, can compress adjacent structures • Malignant invasion of sinus venosus of heart has been observed in some cases • Unknown if neoplastic progression is associated with hormonal changes

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zebrafish: humongous fleshy mass protrudes from ventrally opened abdomen

zebrafish abdomen: humongous basophilic mass

a different zebrafish abdomen: humongous multinodular basophilic masses

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well-differentiated

poorly-differentiated

Seminomas in Zebrafish

well-differentiated

poorly-differentiated

Seminomas in Zebrafish

• Most common spontaneous zebrafish neoplasm • Occurs in older males • Most are well-differentiated, spermatocytic-type seminomas • Even large seminomas rarely invade locally or metastasize

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Japanese medaka liver: metastatic seminoma partially obstructs hepatic vein

head of a different Japanese medaka: tissue beneath brain

head of a different Japanese medaka: tissue beneath brain

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Ectopic Gonad Tissue

head of a different Japanese medaka: tissue beneath brain

Sex on the Brain

head of a different Japanese medaka: tissue beneath brain

The Three Most Overdiagnosed / Misdiagnosed Histopathologic Findings in Fish

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The Three Most Overdiagnosed / Misdiagnosed Histopathologic Findings in Fish 1.

Gill edema – –

“Epithelial lifting” is frequently an artifact of formalin fixation For true gill edema, look for blebbing and/or flocculent material beneath the elevated epithelium

Actual Gill Edema (and lamellar adhesions)

The Three Most Overdiagnosed / Misdiagnosed Histopathologic Findings in Fish 1.

Gill edema – –

2.

“Epithelial lifting” is frequently an artifact of formalin fixation For true gill edema, look for blebbing and/or flocculent material beneath the elevated epithelium

Renal tubular necrosis and glomerular changes – –

Tubular necrosis can occur secondary to incidental intratubular mineralization Fish glomeruli are morphologically variable, often appear hypercellular with thickened mesangial matrix

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Estrogenic Effects: Lesions in Kidney of Adult Male FHM

E2-exposed Male

Control Male Kidney

E2 Causes Nephropathy in Adult Male Fish: Mechanism

Estrogen Liver Vitellogenin Kidney Nephropathy due to protein overload

The Three Most Overdiagnosed / Misdiagnosed Histopathologic Findings in Fish 1.

Gill edema – –

2.

“Epithelial lifting” is frequently an artifact of formalin fixation For true gill edema, look for blebbing and/or flocculent material beneath the elevated epithelium

Renal tubular necrosis and glomerular changes – –

3.

Tubular necrosis can occur secondary to incidental tubular mineralization Fish glomeruli are morphologically variable, often appear hypercellular with thickened mesangial matrix

Hepatic lipidosis –



In cultivated fish, hepatocytes tend to be heavily vacuolated with fat and glycogen due to excess energy intake Sick fish more commonly have reduced liver vacuolation

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Hepatocyte Vacuolation

Liver from wild red drum

Hepatocyte Vacuolation



Less vacuolated: – –



Wild caught fish Sick, stressed, or starving fish

More vacuolated: – – –

Captive-reared fish Overfed or mal-fed fish Toxicant-induced

Liver from wild red drum

Liver from captive red drum

If this wasn’t a shark liver, it would be Lipidosis

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Questions?

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