JPC SYSTEMIC PATHOLOGY
RESPIRATORY SYSTEM
September 2023
P-P13 (NP)
Signalment (JPC #1455856): California sea lion (Zalophus californianus)
HISTORY: Found stranded on the Santa Barbara coast
HISTOPATHOLOGIC DESCRIPTION: Lung: Approximately 80% of the bronchial and bronchiolar lumina and approximately 60% of alveolar lumina are filled with an exudate composed of numerous macrophages, fewer lymphocytes, plasma cells, neutrophils, multinucleated giant cells, and numerous cross and tangential sections of metastrongyle nematode adults and larvae admixed with variable amounts of mucus and fibrin. The adult nematodes are 80-200 µm in diameter and have a 5-10 µm thick smooth outer cuticle, a thin hypodermis from which small lateral cords arise, a pseudocoelom lined by coelomyarian-polymyarian musculature, a large intestinal tract lined by few multinucleated cells, and male or female reproductive organs, with uteri often containing intraluminal larvae. The larvae are 10-20 µm in width, deeply basophilic, and occasionally coiled. Diffusely, alveolar septa are congested and expanded by increased clear space (edema), eosinophilic fibrillar material (fibrin), and moderate numbers of lymphocytes and plasma cells. Multifocally, bronchiolar epithelium is characterized by one of the following: hyperplastic, piling up to 5 cell layers thick, with mild goblet cells hyperplasia; attenuated; lost (ulcerated); or necrotic with hypereosinophilic cytoplasm and nuclear pyknosis or karyorrhexis. Diffusely, interlobular septa, perivascular connective tissue, and pleura are moderately expanded by fibrin and edema.
Liver: There is diffuse moderate congestion of sinusoids and multifocally hepatocytes contain a single clear cytoplasmic vacuole (lipid).
MORPHOLOGIC DIAGNOSIS: 1. Lung: Pneumonia, granulomatous, multifocal to coalescing, moderate, with numerous intra-alveolar and intrabronchiolar metastrongyle nematode larvae and adults, California sea lion (Zalophus californianus), pinniped.
2. Liver, hepatocytes: Vacuolar change, lipid-type, multifocal, mild.
ETIOLOGIC DIAGNOSIS: Pulmonary parafilaroidiasis
CAUSE: Parafilaroides decorus
GENERAL DISCUSSION:
· Metastrongyle (lungworm) nematode that infects pinnipeds (otariids and phocids, Steller sea lion, California sea lion)
· Geographic range: Pacific waters of United States, northern and southern hemisphere
PATHOGENESIS:
· Minor pneumonia unless concurrent with secondary bacterial infections, heavy parasite burden, or immunocompromised; subclinical infections common
· Infection in young seals (<1 year)à impaired respiratory functionà decreased diving timeà decreased feeding abilityàreduced survival in first winter (Barnett, J Comp Pathol, 2019)
LIFECYCLE:
· Larvae are passed in the feces of the sea lion and ingested by the intermediate host (likely opaleye fish)à Larvae localize in the fish’s intestinal mucosa and submucosa and molt into infective stageà Intermediate host is ingested by the definitive host (sea lion), and infective larvae are released from the ingested fish tissue into the gastrointestinal tract of the sea lionà Larvae migrate to the lungs where maturation occursà Adult lungworms reside in the alveoli and terminal bronchioles, shed embryonated eggs into small airways where they develop into L1 larvaeà First-stage larvae (L1) coughed up and are swallowed by the sea lionà
· Sea lions begin to pass larvae in their feces 21 days post-infection
TYPICAL CLINICAL FINDINGS:
· Early signs: Mild dyspnea and a mild productive cough
· More severe infections: Anorexia, vomiting, weight loss, and respiratory distress
TYPICAL GROSS FINDINGS:
· Adult worms have thin, ridged cuticle and coelomyarian polymyarian musculature, difficult to detect grossly
· Small, raised nodules along pleural surface and in parenchyma adjacent to bronchioles
TYPICAL LIGHT MICROSCOPIC FINDINGS:
· Cross sections of small nematodes within alveolar spaces and bronchioles
· Most animals have minimal lymphocytic interstitial and peribronchiolar inflammation, occasional granulomas around degenerating parasites or larvae, mild bronchiole epithelial hyperplasia, and lymphocytic tracheitis
· Heavy infection or with secondary bacterial pneumonia causes significant inflammation, proliferative endarteritis
· Lobules with adult parasites (but no larvae) have minimal to absent inflammatory response
ADDITIONAL DIAGNOSTIC TESTS:
· Detection of the first stage motile larvae in fecal smears or nasal exudate
DIFFERENTIAL DIAGNOSIS:
Other lungworms of phocid pinnipeds:
· Otostrongylus circumlitis - the only other lungworm of phocid pinnipeds (seals: harbor, ringed, spotted, ribbon, Baikal, grey, bearded, northern elephant)
· Large roundworm found in large bronchi and bronchioles; causes
vasculitis
Other Parafilaroides spp: speciation based on host and geographic range
· P. gymnurus – final host: phocid seals (harbor, ringed, harp, spotted, grey, bearded, Baikal); range: coastal waters of Canada, Europe, and Russia
· Infection in harbor seals can be treated with ivermectin or moxidectin
· P. hydrurgae – final host: leopard seal; range: Southern Ocean
· P. hispidus – final host: phocid seals (ringed and grey); range: coastal waters of Canada
· P. caspicus – final host: Caspian seal; range: Caspian Sea
COMPARATIVE PATHOLOGY:
Selected pulmonary metazoan parasites in other species:
|
Species |
Agent |
Site of adult |
|
Dog |
Eucoleus aerophila, Spirocerca lupi |
Trachea, bronchi |
|
|
Angiostrongylus vasorum |
Pulmonary arteries |
|
|
Oslerus osleri |
Trachea, bronchi |
|
|
Dirofilaria immitis |
Pulmonary artery |
|
|
Filaroides hirthi, Andersonstrongylus milksi |
Bronchi, bronchioles, alveoli |
|
Linguatula serrata (pentastome) |
Nasal passages |
|
|
Cat |
Eucoleus aerophila, Filaroides rostratus |
Trachea, bronchi |
|
|
Aelurostrongylus abstrussus |
Bronchioles, alveolar ducts |
|
|
Paragonamus kellicoti (trematode) |
|
|
Cattle |
Dictyocaulus viviparous |
Bronchi, bronchioles |
|
Sheep, Goat |
Dictyocaulus filaria |
Bronchi, bronchioles |
|
|
Protostrongylus rufescens |
Bronchioles |
|
|
Muellerius capillaris; Cystocaulus ocreatus |
Alveoli |
|
Oestrus ovis (bot) |
Nasal cavity |
|
|
Horse, Donkey |
Dictyocaulus arnfieldi |
Bronchi, bronchioles |
|
Pig |
Metastrongylus apri; M. salmi, M. pudendotectus |
Bronchi, bronchioles |
|
Avian |
Syngamus trachea |
Trachea |
|
Cytodytes nudus (mite) |
Air sacs |
|
|
Rabbit (wild) |
Protostrongylus boughtoni |
Bronchi, bronchioles |
|
Pinnipeds |
Otostrongylus circumlitus |
Trachea, bronchi, |
|
|
Parafilaroides spp. |
Bronchioles, alveoli |
|
New World Monkey |
Filaroides cebus |
Bronchioles, alveoli |
|
Pneumonyssus simicola (mite) |
Bronchi, bronchioles |
|
|
Rats |
Angiostrongylus vasorum, Parastrongylus cantonensis |
Pulmonary arteries & capillaries |
References:
1. Barnett JEF, Bexton S, Fraija-Fernández N, Chooneea D, Wessels ME. Novel Pulmonary Vasculitis with Splendore-Hoeppli Reaction in Grey Seals (Halichoerus grypus) Associated with Otostrongylus circumlitus Infection. J Comp Pathol. 2019 Nov;173:83-91.
2. Colegrove KM, Burek-Huntington KA, Roe W, Siebert U. Pinnipediae. In: Terio KA, McAloose D, St. Leger J ed. Pathology of Wildlife and Zoo Animals. Cambridge, MA: Elsevier Inc. 2018:583-584.
3. Garner MM, et al. Evidence of Brucella infection in Parafilaroides lungworms in a Pacific harbor seal (Phoca vitulina richardsi). J Vet Diagn Invest. 1997;9:298-303.
4. Measures LN. Lungworms of marine mammals. In: Samuel WM, Pybus MJ, Kocan AA, eds. Parasitic Diseases of Wild Mammals. 2nd ed. Ames, IA: Iowa State University Press; 2001:283-288.
5. Simpson JG, Cornell LH. Diseases associated with stranding and captivity. In: Howard, EB, ed. Pathobiology of Marine Mammal Diseases. Vol 2. Boca Raton, FL: CRC Press, Inc.;1983:30-35.
6. Van Bonn WG. Pinnipedia, Metazoan Diseases. In: Fowler ME, Miller RE, eds. Zoo and Wild Animal Medicine. Vol. 8. Philadelphia, PA: WB Saunders, Co.; 2015:447.
