6-month-old, female, charolais, bovineThis calf belonged to a group of 210 beef calves with ages varying from 6-8 months. They were weaned at 3 months of age and placed in a pasture of 4 hectacres. This pasture was very wet and had accumulated water in several places. At one end of the pasture there was a feed trough where the calves had ad libitum access to corn silage and to concentrate (wheat bran) at the proportion o 1%/bw/day. During mid-fall of 2003 (3 months after being introduced onto the 4 ha.) 20 calves developed a respiratory disease with clinical signs including cough, rectal temperature of 40Â°C-41Â°C, serous nasal discharge, tachypnea, dyspnea, labored breathing through the mouth, and anorexia with weight loss. Four calves died after a clinical course of disease of 5-8 days. The remaining 16 sick calves were treated with Doramectin 1%, and recovered slowly.
The carcass was thin and dehydrated.Â The lungs had large, red-gray, firm, slightly depressed, patchy areas of consolidation, mainly in the dorsocaudal lobes.Â Alternating with the consolidated depressed areas there were pink-white bulging, emphysematous areas of the lung parenchyma.Â The lumen of the trachea and major bronchi contained large tangles of numerous slender, white, 5-8 cm, nematodes mixed with a mucinous, foamy exudate.Â These parasites had morphology compatible with Dictyocaulus spp. The areas of consolidation could be appreciated on the cut surface of the lungs (kodachromes C).Â At the cut surface multiple 1 mm in diameter, yellow foci could be observed randomly distributed in the lung parenchyma, and the parasites could be seen in the luminae of bronchi.Â There was an excess of 50 ml of yellow turbid fluid in the pericardial sac.Â Moderate dilatation was observed in the right ventricle of the heart, and a slight nutmeg pattern was seen in the liver.Â Large numbers of Haemonchus contortus were found in the abomasum and moderate numbers of Oesophagostumum spp. were found in the large intestine.
1) Interstitial pneumonia, proliferative, with nematodes and larvae consistent with Dictyocaulus viviparus, Charolais, bovine.
2) Bronchitis and bronchiolitis, chronic, suppurative, with epithelial hyperplasia and broncholitis obliterans, Charolais, bovine.
3) Heart, dilatation of the right ventricale (Cor pulmonmale), Charolais, bovine (slides not included) 4) Nutmeg liver, Charolais, bovine (slides not included)
Parasitic bronchitis and pneumonia
The parasite found in the airways was identified as the trichostrongilid nematode, Dictyocaulus viviparus.
The lesions present in the submitted slides are consistent with a patent infection of Dictyocaulus viviparus in cattle.Â Except for the aberrant migration of Ascaris suum larvae in the bovine lung, D.Â viviparous is the only lung worm in this animal species8.Â Bovine dictyocaulosis occurs worldwide but is seen more frequently in areas of high rainfall and intense irrigation6.Â In the southern hemisphere it occurs mainly after weaning in calves less than one year old, during the Fall (as was the case of the present outbreak) or Winter and even in the first months of Spring6.Â The adult D.Â viviparus may reach 8 cm in length, and is a nematode which has a direct life cycle3.Â The female worms lay eggs in the trachea and bronchi of affected animals.Â The eggs hatch rapidly and first stage larvae are coughed up, swallowed, and shed in the feces.Â In the pasture, depending on the climate, the larvae can develop within 7 days into an infective third stage larvae.Â Upon being ingested with the grass by cattle, they penetrate the small-intestinal wall and gain access to the mesenteric lymph nodes were they molt to the L4 stage; these are taken by blood and lymph to the lungs, where they locate in the pulmonary capillaries of the ventral portions of the caudal lobes 3,8.Â
Approximately seven days after ingestion, penetration of the alveoli occurs, and from there the larvae reach the bronchioles where the final molt (L5) takes place; during further development the young adults move up to the bronchi.Â The prepatent period is 3-4 weeks.Â
The lesions produced by D.Â viviparus depend on the susceptibility of the host and on the number of invading larvae.Â There are two main manifestations of clinical disease caused by D.Â viviparus.Â The primary infection occurs in calves younger than 1-year-old, and even older cattle previously unexposed to D.Â Viviparus, that come into contact with heavily parasitized pastures for the first time.Â This being the case for the calves of this report.Â The second manifestation is referred to as reinfection syndrome.Â This condition occurs 14-16 days after immune, adult cattle that have been infected previously with D.Â Viviparus, are placed on heavily contaminated pasture.Â Clinical signs include respiratory distress, marked coughing, increased respiratory rate, projectile diarrhea, dramatic milk yield drop, and harsh respiratory sounds.Â This second manifestation being the function of an allergic reaction1,3.Â
The primary infection can be subdivided into a pentration phase (1-7 days), a prepatent phase (approximately 7 to 25 days after infection), a patent phase (approximately 25 to 55 days after infection), and a postpatent phase (approximately 55 to 90 days after infection).Â The penetration phase is usually not associated with clinical signs3.Â As the larvae reach the alveoli in the prepatent phase there is coughing, increased respiratory rate, but death is infrequent unless complications occur.Â In this phase no adult worm can be found in the airways; even though D.Â viviparus larvae can be seen in the smears of expectorated mucous, they are not detectable in the feces.Â In the patent phase clinical signs are marked and include coughing, increased respiratory rate, labored breathing, decreased intake of food and water, loss of condition, harsh respiratory sounds, crackling sounds in the lung, and subcutaneous emphysema.Â Deaths are frequent in this phase and lesions observed at necropsy include bronchitis, bronchiolitis, parasitic pneumonia with consolidation and collapse of the lung lobes, and the presence of hyaline membranes.Â Secondary bacterial bronchopneumonia is seen in some cases1,6.Â As is the case in this report, adult worms, larvae, and eggs are observed in the airways.Â Many larvae are passed in the feces and can be detected by the Baermann technique.Â Recovery occurs in the late patent phase, with gradual waning of the clinical signs leading to a recovery over several months time.Â However, deaths may occur in 25% of cases due to complications such as sudden exacerbation of dyspnea at days 45-60, after secondary bacterial infection1,8.Â Lesions in these fatal cases include pulmonary edema, hyaline membranes, alveolar epithelial hyperplasia, and interstititial emphysema.Â
In the case reported here, Cor pulmonale was observed to be associated with hydropericardium and nutmeg liver.Â This was interpreted as being caused by impediment of blood transit through the lung, and thus congestive heart failure.
The diagnosis of this case was straightforward since the epidemiology, clinical signs, typical lesions, and the presence of large characteristic worms permitted a definite diagnosis.Â All things considered, if an animal with the above discussed symptoms was examined superficially, without necropsy and discovery of nematodes, ARDS would be a definite differential.
1.Â Lung: Bronchitis and bronchiolitis, chronic, multifocal to coalescing, moderate, with multifocal bronchiolitis obliterans, adult and larval nematodes and ova, etiology consistent with Dictyocaulus viviparus, Charolais (Bos taurus), bovine.
2.Â Lung: Pneumonia, interstitial, acute, diffuse, severe with fibrin.
3.Â Lung: Bronchopneumonia, suppurative, multifocal, marked.
The contributor gives an excellent overview of the life cycle of Dictyocaulus viviparus, and the various stages of infection.
Reinfection is necessary to maintain immunity as a decrease in the immune response is seen in as little as 100 days following infection.Â A hypersensitivity reaction seen in animals with the reinfection syndrome caused by D.Â viviparus, can have clinical signs and lesions indistinguishable from acute bovine pulmonary edema (ABPE).8
In the case presented at this conference there appears to be a more acute interstitial component underlying the verminous pneumonia with features of acute respiratory distress syndrome (ARDS).Â In addition, the multifocal suppurative bronchopneumonia may be the result of a secondary bacterial infection, which is not uncommon in these cases.
Bronchiolitis obliterans is a lesion of chronic bronchiolar damage that consists of either fibrous polyps occluding the bronchiolar lumen or intraluminal aggregates of inflammatory cells that obstruct the airways.2 It can occur following a variety of pneumonias caused by agents such as bovine respiratory syncytial virus (BRSV), bovine parainfluenza virus 3 (BPIV-3), infectious bovine rhinotracheitis (IBD), D.Â viviparus, bacteria, toxic gases, and hypersensitivity reactions.2
Histologic features of metastrongyles include a body cavity, intestine lined by few multinucleated cells with microvilli, accessory hypodermal chords, coelomyarian musculature, and, in females, a uterus with larvae or embryonated eggs.4
Lungworms of selected domestic and wild mammals:
- Aelurostrongylus abstrusus cats; catarrhal bronchiolitis, submucosal gland hyperplasia, granulomatous alveolitis, alveolar fibrosis
- Eucoleus aerophilus (Capillaria aerophila) dogs, cats, foxes; dogs and cats usually have very mild infection
- Crenosoma vulpis foxes, occasionally dogs; eosinophilic catarrhal bronchitis and bronchiolitis
- Filaroides hirthi, Andersonstrongylus milksi (Angiostrongylus milksi, F.Â milksi) dogs, mink; pyogranulomatous, eosinophilic pneumonia
- Oslerus (Filaroides) osleri wild canids; single/multiple 1-10mm diameter, firm, gray-pink, sessile or polypoid, submucosal nodules in trachea and bronchi, usually at tracheal bifurcation
- Angiostrongylus vasorum dogs, foxes; inhabits pulmonary artery and right ventricle
- Dictyocaulus filaria sheep and goats; catarrhal and eosinophilic bronchitis and bronchiolitis
- Dictyocaulus viviparus cattle; pneumonia, bronchitis, pulmonary edema and emphysema
- Dictyocaulus arnfieldi horses, donkeys; obstructive or eosinophilic bronchitis, edema, atelectasis
- Muellerius capillaris sheep and goats; small subpleural nodules; alveolar fibrosis +/- granulomatous inflammation
- Protostrongylus rufescens sheep and goats; lambs and kids; adults live in bronchioles; results in pulmonary nodules and eosinophilic bronchiolitis.
- Metastrongylus apri pigs; growth retardation, bronchitis, catarrhal inflammation
We are grateful to Dr.Â Chris Gardiner, AFIP consultant in veterinary parasitology, for his review and comments on this interesting case.
1.Â Breeze RG: Parasitic bronchitis and pneumonia.Â Vet Clin North Am (food Anim Pract) 1:277-287, 1985
2.Â Caswell JL, Williams KJ: Respiratory system.Â In: Jubb, Kennedy, and Palmers Pathology of Domestic Animals, ed.Â Maxie MG, 5th ed., vol.Â 2, pp.Â 559-561, 615-653.Â Elsevier Limited, St.Â Louis, MO, 2007
3.Â Eysker M: Dictyocaulosis in cattle.Â Com Cont Ed Pract Vet 16:669-675, 1994
4.Â Gardiner CH, Poynton SL.Â An Atlas of Metazoan Parasites in Animal Tissues.Â Armed Forces Institute of Pathology, Washington, D.C., 2006
5.Â LÂ³pez A: Respiratory system.Â In: Pathologic Basis of Veterinary Disease, eds.Â McGavin MD, Zachary JF, 4th ed., pp.Â 522-548.Â Elsevier, St.Â Louis, MO, 2007
6.Â Panuska C: Lungworms of ruminants.Â Vet Clin Food Anim 22:583-593, 2006
7.Â Ruas JL: Pneumonia verminÂ³tica [Parasitic pneumonia].Â In: Doen_as de Ruminantes e Eq+ï¿½-+inos [Diseases of Ruminants and Horses], ed.Â Riet-Correa, F, Schild AL, M+ï¿½-ï¿½ndez MC, Lemos RAA, 2 ed, vol.Â 1, pp.Â 85-89, Varella, S_o Paulo, Brazil, 2001 [Text in Portuguese]
8.Â Smith JA, Grooms D: The interstitial pneumonias.Â In: Large Animal Medicine, ed.Â Smith BP, 3rd ed., pp.Â 571-581, Mosby Inc., St.Â Louis, MO, 2002