JPC SYSTEMIC PATHOLOGY
RESPIRATORY SYSTEM
September 2023
P-P16
Signalment (JPC #1711212): Herring gull
HISTORY: Unknown
HISTOPATHOLOGIC DESCRIPTION: Trachea: The mucosal epithelium is thickened up to five cell layers thick by disorganized epithelial cells that have enlarged, often vesiculate nuclei (hyperplasia) and increased numbers of goblet cells. Multifocally overlying the epithelium is a thin layer of eosinophilic, finely fibrillar material (fibrin). Within the lumen, there are sloughed epithelial cells, few macrophages and heterophils and multiple cross sections of adult strongylid nematodes that measure up to 500 µm in diameter with a 1 µm, smooth cuticle, a pseudocoelom lined by platymyarian-meromyarian musculature, an intestine lined by uninucleated cells with a prominent brush border, and several sections of ovaries and uteri containing developing eggs. Diffusely, the subepithelial connective tissue is markedly expanded by a moderate amount of clear space (edema), moderate numbers of lymphocytes and plasma cells, fewer macrophages and heterophils, and few reactive fibroblasts.
Liver: Multifocally and randomly affecting approximately 5% of hepatic parenchyma, there are few variably sized foci of pale, enlarged hepatocytes (degeneration) often admixed with eosinophilic material (fibrin) and cellular and karyorrhectic debris (necrosis), few to moderate numbers of macrophages and heterophils, and fewer lymphocytes.
Kidney: No significant lesions.
MORPHOLOGIC DIAGNOSIS: 1. Trachea: Tracheitis, proliferative and lymphoplasmacytic, diffuse, moderate, with goblet cell hyperplasia and intraluminal adult nematodes, herring gull (Larus argentatus), avian.
2. Liver: Hepatitis, pyogranulomatous and necrotizing, multifocal, random, mild.
ETIOLOGIC DIAGNOSIS: Tracheal syngamiasis
CAUSE: Syngamus trachea
SYNONYMS: Gapeworm, redworm, forked worm
GENERAL DISCUSSION:
- Class: Nematoda; Order: Strongylida; Superfamily: Strongyloidea; Family: Syngamidae; Genus: Syngamus
- Most common in young, flightless, free range birds (turkeys, pheasants, chickens, geese, guinea fowl, pea fowl, and quail with worldwide distribution)
- Characteristic lesions usually found in turkey/pheasants, less likely in chickens, and seldom if ever in guinea fowl; pheasants, turkey poults and young chickens are most susceptible
- Affects birds raised outdoors when access to infected intermediate hosts (e.g. earthworms) is available, especially after heavy rains that bring them to the surface
- Males burrow into the mucosal lining of the trachea acting as an anchor for the female
PATHOGENESIS:
- In the trachea, the worms attach to the mucosa and feed on blood, with consequent catarrhal tracheitis and occasional secondary lobar pneumonia
- Deep embedment of the male within the wall of the trachea can result in the development of connective tissue nodules
- Trachea becomes partially to completely occluded by worms and blood clots and causes subsequent gaping for air and death by suffocation
LIFE CYCLE:
- Adult females lay eggs in the bird’s trachea that are coughed up, swallowed, and passed out in the feces > Larvae may remain free or become encysted in transport hosts (earthworms,snails, slugs) and live for months to years in an encapsulated form in muscle > After ingestion by the bird (the definitive host), the larvae penetrate the wall of crop, esophagus, or duodenum, migrate through the liver, enter the blood stream via the portal system, and are carried to the lungs > Adult worms migrate to the large bronchi and trachea where copulation takes place and eggs are laid
- Prepatent period: 17-20 days
- Direct transmission occurs by ingestion of the infective larvae or embryonated eggs
- Indirect transmission occurs when transport hosts such as earthworms, snails, slugs, flies and other arthropods ingest infective larvae
TYPICAL CLINICAL FINDINGS:
- Chiefly affects young birds; turkeys susceptible at all ages
- Dyspnea, coughing, asphyxia, and “gaping”
- Death results from asphyxiation or from progressive emaciation, anemia, and weakness caused by the parasites
TYPICAL GROSS FINDINGS:
- Tracheal lesions range from mild catarrhal and hemorrhagic tracheitis to severe ulcerative tracheitis with bronchitis and pneumonia
- Lungs can be firm with focal areas of fibrin and air sacs can be thickened and covered in fibrin.
- In turkeys and larger birds, small white nodules may be found along the trachea and are considered to be presumptive evidence of previous infection
- Nodules are rare in chickens and guinea fowl
- Emaciation and pale carcass from anemia
- In fresh tissue, worms are present in the distal trachea and are frequently bright red due to the ingestion of host blood, and the male and female worms are permanently fused in copula, resulting in a "y"-shaped appearance; males are 2-6mm and females 5-20mm long
TYPICAL LIGHT MICROSCOPIC FINDINGS:
- Males are up to 200 µm and females up to 350 µm in diameter with a pseudocoelom, 4-8µm cuticle, platymyarian-meromyarian musculature and a prominent intestinal brush border lined by few uninucleate cells
- Thin shelled eggs measure 50x90 µm, and have a thickened operculum at each pole
- At the point of attachment, nodules will contain proliferating perichondral cells with matrix and are associated with lysis of cartilage; multinucleated giant cells, macrophages and heterophils can be seen filling atria and parabronchi
- Catarrhal and hemorrhagic tracheitis
- Possible lymphoid follicles in the trachea
- Verminous pneumonia in heavy infections
ADDITIONAL DIAGNOSTIC TESTS:
- In live birds, detection of double-operculated, 50 X 90 µm strongyle eggs in coughed up mucus or on fecal flotation
DIFFERENTIAL DIAGNOSIS:
- Cyathostoma bronchialis: Larger worm, less firmly united in copula; eggs have an indistinct operculum; found in the larynx, trachea, bronchi, and abdominal air sacs of ducks, geese, and swans
- C. bronchialis is typically associated with water fowl and S. trachea with land birds, though they can be found in either group
- Syngamus skrjabinomorpha: Similar grossly and histologically but only found in chickens and geese in Russia
COMPARATIVE PATHOLOGY:
- Various Mammomonogamus spp. (formerly Syngamus spp.) parasites have been reported in the larynx, nasal cavity, pharynx, middle ear, and bronchi of humans and other mammals
REFERENCES:
- Abdul-Aziz, T., Barnes HJ., American Association Of Avian Pathologists. Gross Pathology of Avian Diseases: Text and Atlas. American Association Of Avian Pathologists; Aaap; 2018: 182.
- Anderson RC. The superfamily Strongyloidea. In: Anderson RC, ed. Nematode Parasites of Vertebrates. Wallingford, UK: CAB International; 1992:77-80.
- Crespo R, Franca MS, Fenton H, Shivaprasad HL. Galliformes and Colubriformes. In: Terio KA, McAloose D, St. Leger J, eds. Pathology of Wildlife and Zoo Animals. London, UK: Academic Press; 2018:766-767.
- McDougald LR. Internal parasites. In: Swayne DE, ed. Diseases of Poultry, Volume II. 14th ed. Ames, IA: Wiley-Blackwell Publishing; 2020:1171-1172.
- Schmidt RE, Reavill DR, Phalen DN. Respiratory system. In: Pathology of Pet and Aviary Birds. 2nd ed. Ames, IA: Wiley-Blackwell Publishing; 2015:32.
- Trupkiewicz J, Garner MM, Juan-Salles C. Passeriformes, Caprimulgiformes, Coraciiformes, Piciformes, Bucerotiformes, and Apodiformes. In: Terio KA, McAloose D, St. Leger J, eds. Pathology of Wildlife and Zoo Animals. London, UK: Academic Press; 2018:815.
- Wallner-Pendleton E. Diseases of the game birds. In: Boulianne M, ed. Avian Disease Manual. 8th ed. Jacksonville, FL: American Association of Avian Pathologists, Inc.; 2019:188.
- Wehr EE. Nematodes. In: Davis JW, ed. Infectious and Parasitic Diseases of Wild Birds. 1st ed. Ames, IA: Iowa State University Press; 1971:193-196.