JPC SYSTEMIC PATHOLOGY
Signalment (WSC 95/96: 11-1): 1-year-old rainbow trout (Oncorhynchus mykiss)
HISTORY: This trout was harvested from Willow Creek, MT, where trout numbers have recently decreased.
HISTOPATHOLOGIC DESCRIPTION: Head: Multifocally within the cartilage of the calvarium and gill arches, there are few variably-sized granulomas that surround and replace chondrocytes and cartilaginous matrix. Centrally, the granulomas contain numerous, round to piriform, 8-10 um diameter myxozoans and moderate amounts of necrotic debris. The central core is surrounded by many epithelioid macrophages, fewer lymphocytes and multinucleated giant cells, which are occasionally further surrounded by concentric layers of reactive fibroblasts and fibrous connective tissue. The myxozoans have a 1-2 um thick, refractile wall, a 2 um diameter nucleus, and two piriform, 2x4 um polar capsules, each containing a 1 um diameter, basophilic nucleus. Multifocally, inflammatory cells expand perichondral and periosteal connective tissue, extend into the brain, and widely separate or replace neurons within extracranial and paravertebral ganglia.
MORPHOLOGIC DIAGNOSIS: Head and gill arches, cartilage and bone: Chondritis, granulomatous, multifocal, moderate, with perichondritis, periosteitis, ganglioencephalitis and numerous myxozoan organisms, rainbow trout (Oncorhynchus mykiss), piscine.
ETIOLOGIC DIAGNOSIS: Myxozoal chondritis
CAUSE: Myxobolus cerebralis
CONDITION: Whirling disease
CONDITION SYNONYM: Black tail
- Myxobolus cerebralis, one of the most pathogenic myxozoans of fish, is an extracellular metazoal organism (subphylum Myxozoa, class Myxosporea) that induces a range of signs and lesions including whirling behavior, blackened caudal regions and severe skeletal deformities
- A reportable disease that is a significant health and economic problem in hatcheries and wild populations of trout; has been implicated in the decline of wild trout populations in several western states and is a problem for several threatened and endangered species (bull trout, cutthroat trout, and steelhead)
- All salmonids (trout, salmon and grayling) are susceptible to infection; rainbow trout are most sensitive; brown trout and Coho salmon are resistant
- The severity is inversely related to age at exposure with 100% mortality in newly hatched fry and fingerlings, and few or no clinical signs in fish older than 6 months
- Myxozoa features: Multicellular spores; polar capsules in spores; endogenous cell cleavage in trophozoite and sporozoite; all non-sexual stages multinucleate with enveloping cells (primary) that contain enveloped (secondary) cells
- Two-host life cycle: Myxospore in salmonid hosts; triactinomyxon (TAM) in the obligate host, the Tubifex tubifex worm
- Myxospores released from cartilage when infected fish decompose or are ingested by a predator > myxospores ingested by tubifex (oligochaete) worm > sexual and asexual replication in intestine > develop into free living TAM (74-120 days) > released in the feces of the worm > TAM attaches to skin, respiratory epithelium (gill), or buccal cavity of salmonids via polar filaments > penetrates through secretory openings of mucous cells at the attachment sites > asexual reproduction > migrate via peripheral nerves and CNS to cartilage as trophozoites > mature into large plasmodia which feed on cartilage > undergo sporogenesis > formation of myxospores
- Myxospores require several months in the mud to reach full infectivity and can survive in water for over 1 year; TAMs are fragile and short lived
- tubifex remain infected for life and release TAMs intermittently
- Whirling behavior occurs because of multifocal constriction of the spinal cord and lower brain stem caused by inflammatory and necrotizing chondritis induced by the parasite feeding on cartilage
- Black tail is secondary to inflammation in the posterior region of the spine resulting in damage to the caudal nerves responsible for controlling pigment deposition
- Older fish are often asymptomatic because their skeletons are more highly ossified with less cartilage on which the parasite can feed
TYPICAL CLINICAL FINDINGS:
- Young fish (< 6 months): Blackened tail, erratic swimming, head and spine deformities, growth inhibition, lymphopenia, death
- Older fish: Spinal curvature, blunt nose, misshapen skulls, jaws and opercula, often asymptomatic with low mortality
TYPICAL GROSS FINDINGS:
- Prominent scoliosis or kyphosis of the spine, often black discoloration of the tail
- Fish that survive develop deformities, including a blunt nose, misshapen head and jaws
TYPICAL LIGHT MICROSCOPIC FINDINGS:
- Cartilage: Cartilage degeneration/lysis, granuloma formation, ovoid to ellipsoidal spores with two piriform-shaped polar capsules at anterior end
- Sporoplasm (group of infective germ cells enclosed in an envelope) contains an iodinophilous (glycogen) vacuole (best seen in fresh spores) that is characteristic of the genus Myxobolus; spores measure 6-10 um in diameter
ADDITIONAL DIAGNOSTIC TESTS:
- PCR, in situ hybridization, cytology (wet mount and Wright’s), electron microscopy
- Polar capsules stain blue with Giemsa; mature spores are strongly acid fast
- Hypovitaminosis C ("broken back syndrome"): Can cause spinal deformities and darkening of the skin, hemorrhages, soft enlarged vertebrae, and deformed gill filaments
- Mycobacterium: All species of fish susceptible, more common in older fish and in tropical saltwater fish; can sometimes cause vertebral deformities, miliary tubercles in liver, kidney, and spleen with acid-fast organisms (usually in high numbers)
- Ichthyosporidiosis (Ichthyophonus hoferi): A mycotic disease that can cause scoliosis; white foci (encysted "spores" surrounded by thick connective tissue wall) in heart, liver, and most other organs; black granulomas in the skin
- Infectious hematopoietic necrosis (rhabdovirus): Necrosis of submucosal eosinophilic granular cells (pathognomonic); can cause scoliosis
- Tryptophan deficiency: Can cause scoliosis and/or lordosis, calcium deposits in the kidneys and on bones surrounding the notochord
- Vitamin A toxicity: Pathogenesis unknown, may be related to differential development of the vertebral growth plates
- Organophosphates & organochlorines: Cholinesterase inhibition leads to muscle hypercontraction and eventual spinal deformation
- Trifluralin: Herbicid; causes vertebral hyperostosis and dysplasia in salmonids and other fish
Other Causes of Abnormal Swimming Behavior:
- Viral hemorrhagic septicemia (rhabdovirus): Serious disease in Europe; spiraling swimming behavior in the acute form
- Infectious pancreatic necrosis virus (birnavirus): Rotation of body along long axis during swimming; necrosis of pancreas; petechial hemorrhages of viscera (esp. pyloric ceca); clear gelatinous material in stomach
- Hypovitaminosis E: Can cause irregular swimming; muscle atrophy, skin darkening, steatitis, thickening of swim bladder wall with formation of constriction bands
- Flexibacter psychrophilis (“cold water disease”): Skin darkening
- Henneguya ictalur: Most commonly seen as a problem in farmed catfish; usually causes necrotizing branchitis (also known as proliferative gill disease, hamburger gill disease) and dermatitis
- Myxosoma cartilaginis: Common in the eastern U.S.; localizes in the cartilage at the base of fin rays and gill arches of bluegill, sunfish, and black bass; does not cause deformation or impaired movement
- Recent report of renal myxozoanosis in 2 crown river turtles (Hardella thurjii)
- Myxozoanosis occasionally seen in amphibians; also rarely seen in mammals, birds and reptiles
- Myxobolus albi diagnosed in cartilage of captive lumpfish resulting in exophthalmos and grossly visible white to tan scleral nodules
- Baldwin TJ, Vincent ER, Silflow RM, Stanek D. Myxobolus cerebralis infection in rainbow trout (Oncorhynchus mykiss) and brown trout (Salmo trutta) exposed under natural stream conditions. J Vet Diagn Invest. 2000; 12(4): 312-321.
- Cavin JM, Donahoe SL, Frasca S, Innie CJ, Kinsel MJ, Kurobe T, Naples LM, Nyaoke A, Poll CP, Weber EP. Myxobolus albi infection in cartilage of captive lumpfish (Cyclopterus lumpus). J Vet Diagn Invest. 2012; 24(3): 516-524.
- Densmore CL, Blazer VS, Waldrop TB, Pooler PS. Effects of whirling disease on selected hematological parameters in rainbow trout. J Wildl Dis. 2001; 37(2): 375-378.
- Feist SW, Longshaw M. Phylum myxozoa. In: Woo PTK ed. Fish Diseases and Disorders. Vol 1. 2nd ed. Oxfordhsire, UK: CAB International; 2006: 230-296.
- Gardiner CH, Fayer R, Dubey JP. Myxozoa. In: An Atlas of Protozoan Parasites in Animal Tissues. 2nd ed. Washington, DC: American Registry of Pathology; 1998: 14-15.
- Gilbert MA, Granath WO. Whirling disease of salmonid fish: Life cycle, biology, and disease. J Parasitol. 2003; 89(2): 658-667.
- Noga EJ, ed. Fish Disease: Diagnosis and Treatment. 2nd ed. Ames, IA: Wiley-Blackwell; 2010: 229-236.
- Nolan MW, Roberts HE, Zimmerman KL, Smith SA. Pathology in practice. 2010; 236(6): 631-633.