JPC SYSTEMIC PATHOLOGY

RESPIRATORY SYSTEM

SEPTEMBER 2023

P-P12

 

Signalment (JPC #2017865): 3‑year old Rambouillet ewe

 

HISTORY: Death following a clinical course of anorexia, depression, and dyspnea

 

HISTOPATHOLOGIC DESCRIPTION: Lung: Approximately 60% of the pulmonary architecture is consolidated, characterized by atelectasis and/or multifocal to coalescing inflammatory infiltrates centered on/surrounding bronchioles composed of variable numbers of macrophages, neutrophils, lymphocytes, plasma cells and eosinophils, fibrin, and edema. Within larger bronchiolar lumina, there are cross and tangential sections of adult trichostrongyle nematodes that are 350 µm in diameter and have a 4‑5 µm thick cuticle, platymyarian-meromyarian musculature, prominent lateral cords, a pseudocoelom, reproductive organs containing embryonated eggs, and a medium-sized intestine composed of few multinucleated cells lined by short microvilli (brush border). Within smaller bronchiolar lumina and adjacent alveoli, there are few tangential sections of 20-30 µm diameter nematode larvae that have 1-2 µm thick cuticle and a pseudocoelom that contains dark basophilic nuclei and a variably distinct digestive tract. Within other bronchiolar lumina, there are eosinophils, viable and degenerate neutrophils, fewer lymphocytes, plasma cells, and macrophages admixed with sloughed bronchiolar epithelium, fibrin, and debris. Multifocally in both more and less affected areas, bronchiolar epithelium is hyperplastic, up to 5 cell layers thick of the lung, and there is peribronchiolar lymphoid hyperplasia admixed with variable numbers of macrophages and moderate amounts of fibrin and edema. Alveolar septa are moderately thickened by finely beaded, eosinophilic material (fibrin), edema, lymphocytes, and macrophages. There is mild alveolar emphysema and the pleura is mildly expanded by fibrous connective tissue and edema.

 

MORPHOLOGIC DIAGNOSIS: Lung: Pneumonia, eosinophilic and lymphoplasmacytic, multifocal to coalescing, moderate, with atelectasis, peribronchiolar lymphoid hyperplasia, bronchiolar epithelial hyperplasia, and adult and larval trichostrongyle nematodes, Rambouillet, ovine

 

ETIOLOGIC DIAGNOSIS: Pulmonary dictyocauliasis

 

CAUSE: Dictyocaulus filaria

 

GENERAL DISCUSSION:

• Dictyocaulus filaria is the most important and pathogenic lungworm of sheep and goats (especially lambs and kids)
• Dictyocaulus viviparus is the only adult nematode known to infect cattle lungs
• Dictyocaulus spp. are currently classified under the family Trichostrongyloidea, despite the majority of lungworms being classified in the family Metastrongyloidea.

 

PATHOGENESIS:

• Most severe infections occur in animals under a year-old following exposure to contaminated pasture
• Adult nematodes live in the lumen of the bronchial tree 
• 3 phases of infection:
  1. Prepatent phase: 7-25 days post-infection, eosinophilic bronchiolitis; larvae penetrate capillaries into alveoli/bronchioles, emphysema
  2. Patent phase: 25 days +, eosinophilic catarrhal bronchitis/bronchiolitis, and eosinophilic granulomatous alveolitis, atelectasis; some infestations limited to small caudal bronchi; bronchi/bronchioles have adults, larvae, eggs, mucus, eosinophils
     1. Period of recovery: Adult worms eliminated, lung is consolidated with bronchiolitis obliterans, type II pneumocyte hyperplasia, and fibrosis

 

LIFE CYCLE:

 

TYPICAL CLINICAL FINDINGS (Both):

 

TYPICAL GROSS FINDINGS:

Both: 

• Wedge‑shaped, depressed, red to grey, consolidated foci at the posterior edge of the caudal lung lobes (atelectasis)
• Excess mucus within bronchi and bronchioles may obstruct airways (catarrhal bronchiolitis) 
• Multifocal granulomas surrounding eggs and dead larvae
• 2-4 mm gray nodules with green caseous center (adults with reinfection syndrome)

D. filaria:

• Most severe disease occurs in lambs and kids 
• Adult trichostrongyle nematodes are slender, threadlike, white, 3-10cm long, and located in small bronchi of the caudodorsal lung lobes

 

D. viviparous: 

• Most severe disease = primary infection; calves 1-4 months after beginning to graze develop cough termed “husk” or “hoose”
• Associated with allergic reinfection syndrome in partially immune adult cattle 
• Adults up to 8cm long in large bronchi of the caudodorsal lung lobes

 

TYPICAL LIGHT MICROSCOPIC FINDINGS:

Adults: Smooth cuticle, prominent lateral chords, multinucleate intestine, coelomyarian-polymyarian musculature, uterus with larvae or embryonated eggs

 

Prepatent phase (from larval migration into the lungs from capillaries):

• Abundant eosinophils, fewer neutrophils, macrophages and multinucleated macrophages infiltrate alveolar septa and bronchiolar walls generating necrosis
• Hyaline membranes and hyperplasia of type II pneumocytes can occur
• BALT hyperplasia, hypertrophy of bronchiolar smooth muscle, 
• Interlobular septa are expanded by edema and emphysema
• Hyperplastic lymphadenitis with granulomas surrounding nematode larvae

 

Patent phase (from nematodes in bronchi and bronchioles):

• Chronic catarrhal, eosinophilic bronchitis/bronchiolitis with mucous hyperplasia
• Adult worms, eggs, larvae, and eosinophils, are present in bronchial lumina
• Smooth muscle and hyperplasia
• Atelectasis secondary to bronchiolitis

 

Period of recovery: 

 

Reinfection syndrome: 

 

ADDITIONAL DIAGNOSTIC TESTS:

• Baermann apparatus for fecal examination to detect larvae
• Detection of antibodies in serum or milk by ELISA

 

DIFFERENTIAL DIAGNOSIS:

3-methylindole toxicity/ ABPEE/ toxic interstitial lung disease/ “fog fever” (cattle): 

• Emphysema, differentiate from Dictyocaulus spp. prepatent infections by presence of larvae in alveoli
• Reinfection syndrome looks identical to 3-MI toxicity in cattle except alveolar exudate in D. viviparus infections contains eosinophils +/- larvae

Protostrongylus rufescens (small ruminants):

• Metastrongyle of sheep, goat and deer; Indirect life cycle; snail intermediate host
• Adults are smaller than Dictyocaulus (16‑35 mm), red 
• Pulmonary lesions are milder than D. filaria

Neostrongylus linearis (small ruminants):

Muellerius capillaris (P-P11) (small ruminants):

• Metastrongyle (Indirect life cycle) of sheep and goats (most common lungworm of sheep and goats, ubiquitous)
• In alveolar parenchyma; cause subpleural, nodular, granulomatous lesions; adults rarely in bronchioles; rare clinical respiratory disease even in heavy infections

Cystocaulus ocreatus (small ruminants):

• Brown-black hair-like worms; 5-20 mm diameter
• Adults and larvae found in alveoli and small bronchioles
• Dark, firm nodules in the dorsocaudal lung

 

COMPARATIVE PATHOLOGY:

Dictyocaulus filaria in other species:

Other Dictyocaulus spp.:

• Dictyocaulus arnfieldi: affects donkeys and horses

• Donkeys are asymptomatic
• Horses pastured with donkeys may be infected; patent infection develops only if exposed as foals

• In horses exposed as foals: Chronic catarrhal and eosinophilic bronchiolitis in small bronchi of caudal lobes

 

Other lungworms of domestic animals include:

• Metastrongylus apri (elongatus), M. pudendotectus, and M. salmi of swine (bronchi/bronchioles; associated with transmission of swine influenza)
• Crenosoma vulpis (P-P14) in fox and other canids (metastrongyle within bronchi/bronchioles; lesions similar to Dictyocaulus in ruminants)
• Filaroides hirthi (P-P14, bronchioles and alveoli of dogs; direct life cycle); Oslerus osleri (P-P14, submucosal fibrous nodules at the tracheal bifurcation, dogs; direct life cycle)
• Aelurostrongylus abstrusus (P-P09) in respiratory bronchioles and alveolar ducts of cats (metastrongyle)
• Eucoleus aerophilus (P-P15, formerly Capillaria aerophilia) in trachea and bronchi of carnivores (aphasmid)
• Migrating ascarid larvae may affect the lungs of a variety of animal species
• Flukes (Paragonimus spp. in cats, P-P07) may also be seen in the lungs
• Angiostrongylus vasorum (P-P02, metastrongyle), parasite of the pulmonary arteries and the right ventricle of dogs and foxes; overlap between these lesions and those produced by Dirofilaria immitis (P-P02)

 

REFERENCES:

1. Caswell JL, Williams KJ. Respiratory System. In: Maxie MG, ed. Jubb, Kennedy, and Palmer’s Pathology of Domestic Animals. Vol 2. 6th ed. Philadelphia, PA: Elsevier; 2016:554-555, 558, 565-567, 574. 
2. Gardiner CH, Poynton, SL: An Atlas of Metazoan Parasites in Animal Tissues. Washington DC: Armed Forces Institute of Pathology, American Registry of Pathology; 2006: 22,29.
3. Howerth EW, Nemeth NM, Ryser-Degiorgis MP. Cervidae. In: Terio KA, McAloose D, St. Leger J, eds. Pathology of Wildlife and Zoo Animals. London, UK: Academic Press; 2018:169. 
4. Jones MEB, Gasper DJ, Mitchell E. Bovidae, Antilocapridae, Giraffidae, Tragulidae, Hippopotamidae. In: Terio KA, McAloose D, St. Leger J, eds. Pathology of Wildlife and Zoo Animals. London, UK: Academic Press; 2018:138. 
5. Lopez A, Martinson SA. Respiratory System, Thoracic Cavities, Mediastinum, and Pleurae. In: Zachary JF, ed. Pathologic Basis of Veterinary Disease. 7th ed. St. Louis, MO: Elsevier; 2022:565-567, 574, 606, 616-618, 622-623.

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