JPC SYSTEMIC PATHOLOGY

RESPIRATORY SYSTEM

September 2023

P-P11

 

Signalment (JPC #1897187): Adult male goat.

 

HISTORY: Unknown.  

 

HISTOPATHOLOGIC DESCRIPTION: Lung: Multifocally and randomly affecting approximately 30% of the tissue section, the bronchial, bronchiolar, and alveolar lumina contain nematode eggs and larvae. Within alveolar lumina there are fewer adult nematodes. Adult nematodes are 50-75 µm in diameter, have a thin smooth hyaline cuticle, occasional cuticular ridges, polymyarian-coelomyarian musculature, lateral cords, and a pseudocoelom that contains a large intestine lined by few multinucleate cells and tubular reproductive organs containing ova or spermatozoa.  Larvae measure 100 X 15 µm and have a 1-2 µm thick smooth eosinophilic cuticle and a thin posterior tip. Embryonated eggs are ovoid, measure 40 X 60 µm, have an indiscernible shell, and contain multiple 8 µm diameter blastomeres. Multifocally within both small and large airways, there are larva admixed with mucus and cellular exudate. In airways and alveolar spaces all stages of nematodes are admixed with low numbers of macrophages, multinucleated giant cells, and fewer neutrophils; additionally, alveolar lumina contain variable amounts of fibrin, hemorrhage, edema, and necrotic debris. Affected alveolar septa are infiltrated and thickened up to 5x normal by macrophages, fewer lymphocytes and plasma cells, occasional eosinophils, and small amounts of eosinophilic beaded or fibrillar material (fibrin) and edema. Areas of infiltration often coalesce and efface pulmonary architecture to form solid nodules that occasionally contain nematodes. Multifocally there is bronchial and bronchiolar epithelial hyperplasia characterized by thickening of epithelium with loss of polarity of epithelial cells, as well as goblet cell hyperplasia. There is occasional peribronchiolar smooth muscle and lymphoid hypertrophy. Rarely within the alveoli or interstitium there is basophilic granular mineral. 

 

MORPHOLOGIC DIAGNOSIS: Lung: Pneumonia, granulomatous and eosinophilic, multifocal, moderate, with nematode adults, larvae, and eggs, breed unspecified, caprine.

 

ETIOLOGIC DIAGNOSIS: Pulmonary muelleriasis

 

CAUSE: Muellerius capillaris

 

GENERAL DISCUSSION:  

• Most common and ubiquitous lungworm of sheep and goats in Europe and Northern Africa; superfamily of Metastrongyloidea and family Protostrongylidae 
  1. Synonyms: “Small lung worm of sheep and goats” and “nodular lungworm”
• Adult worms are brown, long, thread-like, and range from 12-24 mm long; live in nodular lesions in alveoli and rarely bronchioles

 

PATHOGENESIS:

 

LIFE CYCLE:  

• Indirect: Eggs laid rapidly hatch -> L1 larvae are coughed up and swallowed -> pass in feces -> infect intermediate hosts (slugs or snails) -> molts twice to achieve infective larval stage -> sheep/goats eat slug -> migrate to lungs likely via lymphatics -> emerge in the alveoli 
• Large burdens are gradual and therefore usually only occur in animals >6 months old; additionally, sheep and goats become resistant throughout their life so large burdens are also uncommon in old animals

 

TYPICAL CLINICAL FINDINGS:

• Non-specific: Generally non-clinical; cough, hyperpnea, moderate dyspnea, and decreased weight gain
• M. capillaris may predispose to bacterial or viral infections that cause second order clinical signs

 

TYPICAL GROSS FINDINGS:

• Characteristic finding are subpleural nodules, usually 2-4mm (but up to 20mm), in dorsal region of caudal lung lobes, but may occur anywhere in lung and regional lymph nodes; adult worms within alveoli too small to visualize grossly
• Early lesions are soft and hemorrhagic, while established chronic infestations have raised gray-pink to yellow nodules +/- mineralization
• Goats: Diffuse interstitial pneumonia with absence of nodular lesions

 

TYPICAL LIGHT MICROSCOPIC FINDINGS:

• Nodules composed of masses of adult worms, embryonated eggs, and coiled larvae (300 µm X 15 µm)
• Adult nematodes:
  1. Polymyarian-coelomyarian musculature, 50-75µm diameter, cuticle with variably distinct ridges and hypodermal cords
  2. Intestine composed of few multinucleated cells with indistinct brush border
  3. Uteri containing thick-shelled embryonated eggs and larvae
• Alveolar septa expanded by fibrous tissue, lymphocytes, and smooth muscle hyperplasia
• Inflammatory infiltrate may be minimal; older animals developing resistance have dense eosinophilic aggregates around larvae and adults and alveolar spaces contain macrophages, eosinophils, and giant cells
• After larva are expelled from nodules, the inflammatory response subsides, but alveolar fibrosis persists and alveolar septa remain thickened 
• Larvae that escape into bronchioles are encased in mucus and cellular debris
• As worms die cellular debris becomes mineralized; mineralized debris persists indefinitely as spherical masses of calcium salts surrounded by a fibrous capsule
• Goats: Diffuse thickening of alveolar septa with mononuclear cells and fibromuscular hyperplasia
  1. Note: These lesions alternatively may be caused by caprine arthritis encephalitis virus or Mycoplasma infection 

 

ADDITIONAL DIAGNOSTIC TESTS:

• Baerman apparatus for fecal examination (larvae in fresh feces) and post‑mortem
  1. Occasionally the nodule may only contain one worm of each sex; this generates a sterile infection and the larvae will not be detected in feces

 

DIFFERENTIAL DIAGNOSIS: 

• Interstitial pneumonia; goat presentation

• CAE (lentivirus) 
• Mycoplasma spp.

• Parasitic pneumonia

• Cystocaulus ocreatus: Dark nodules with hair-like worms, adults and larvae located in small bronchioles and alveoli; worms may be seen grossly; bronchial epithelial hyperplasia; very similar to Muellerius spp. in life cycle and pathogenicity
• Protostrongylus rufescens: Soft, angular nodules with grossly visible worms, adults located in terminal bronchioles; often see prominent peribronchiolar lymphofollicular cuffs;  common in sheep, goat, and deer; snails act as the intermediate host;  European variety is called Neostrongylus linearis
• Dictyocaulus filarial (P-P12): Focal atelectasis or consolidation with emphysema and catarrhal bronchitis/bronchiolitis; thread-like adult worms in bronchi; occurs in sheep, goats, and other small ruminants; direct life cycle

 

COMPARATIVE PATHOLOGY:

• Muellerius capillaris listed as a cause of possible verminous pneumonia in wild bovidae, antilocapridae, giraffidae, tragulidae, and hippopotamidae; manifests as interstitial pneumonia or pulmonary granulomas; important to differentiate from tuberculosis in susceptible retions
• Lung worms implicated in multi-pathogen pneumonias, such as bighorn sheep pneumonia 

 

Lungworms of domestic species:

• Cattle: Dictyocaulus viviparous: Causes pneumonia (especially calves during first summer grazing), bronchitis, pulmonary edema, lobular atelectasis and interstitial emphysema; parasite lives in intrapulmonary bronchi
• Horses, donkeys: Dictyocaulus arnfieldi: Donkeys are the natural host; adult parasites cause obstructive bronchitis, eosinophilic bronchitis, edema, and atelectasis primarily in the dorsocaudal lung
• Pigs: Metastrongylus apri, M. pudendotectus, M. salmi
• Canids:  

• Dirofilaria immitus (P-P02)
• Angiostrongylus vasorum (P-P02)
• Oslerus osleri (P-P14B): Pinkish gray fibrous nodules at the tracheal bifurcation and adjacent bronchi

• Eucoleus aerophilus (P-P15)
• Filaroides hirthi
• Andersonstrongylus milksi (P-P14A)
• Crenosoma vulpis (P-P14C)

• Cats:  

  • Aelurostrongylus abstrusus (P-P09): Catarrhal bronchiolitis,

hyperplasia of submucosal glands, granulomatous alveolitis, alveolar fibrosis, and fibromuscular hyperplasia; grossly there are multifocal subpleural granulomatous nodules throughout the lung

• Eucoleus aerophilus (P-P15)

• Primates: Filaroides spp.

                                                

REFERENCES:  

1. Caswell JL, Williams KJ.  The Respiratory System. In: Maxie MG, ed. Jubb, Kennedy, and Palmer’s Pathology of Domestic Animals. Vol. 2. 6th ed. Philadelphia, PA: Elsevier Saunders; 2016:565-566. 
2. Jones EB, Gasper DJ, Mitchell E. Bovidae, Antilocapridae, Giraffidae, Tragulidae, Hippopotamidae. In: Terio KA, McAloose D, G. SLJ. Pathology of Wildlife and Zoo Animals. London: Elsevier/Academic Press; 2018:138-139.
3. 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; 2022:623.

 

 

 

 

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