Bovine respiratory disease (BRD) is the most important cause of morbidity and reduced production in intensively managed cattle. This complex is multifactorial in its aetiology. Along with host and environment stress factors, there are usually a range of pathogenic agents which are commonly involved. These include; pestivirus (BVDV), bovine herpesvirus (BHV-1) which causes infectious bovine rhinotracheitis (IBR), parainfluenzavirus-3 (PI-3), bovine respiratory syncitial virus (BRSV). In addition to the viral agents several bacterial agents are often involved. These commonly include; Mannheimia haemolytica which is often associated with a severe pleuropneumonia, Pasteurella spp., Histophilus somnus, and Mycoplasma spp.
This outbreak occurred on a semi-intensive feedlot/pasture based system near Moruya on the South Coast of NSW. Weaner cattle are both bred and purchased for finishing, followed by slaughter at the Moruya abattoir. The system, apparently well managed, had been functioning satisfactorily and without serious problems until early April 2010. At this time many of the cattle put on feed began to sicken and showed signs of respiratory disease.
The main property, including the feedlot paddocks, is composed of 156 ha of undulating country covered by of improved pastures. The pasture species are principally kikuyu, paspalum, white clover and couch grass. This holding maintains a population of about 300 Angus and Murray Grey cattle and their crosses (Limousin and Charolais). The cattle are stocked at around 25 head per 4 ha paddock. These paddocks have a central feed trough with shared water troughs on the fence line. A laneway system feeds from the feedlot paddocks to a set of yards at the edge of the holding.
The operation was characterised by weekly slaughter of 15 to 25 animals meeting abattoir specifications. These are replaced by new introductions at around weekly intervals. Mostly these are 8 to 12 month-old weaners which are usually kept on feed for around 70 days before slaughter. The operation puts through around 1000 weaners per year. The property is usually more lightly stocked for 2 months during October and November when demand for these premium cattle is reduced. The introductions were mostly purchased from saleyards, although a proportion also came direct from breeder's holdings or from the family's breeding herd of Angus cows mated to Limousin bulls. Many of the introductions may have been taken directly from their mothers prior to purchase and travelled up to 450km from point of purchase. The ration fed consisted mainly of cereal hay, biscuit meal and dried distiller's grain with the addition of a mineral premix. The ration had a tendency to be dusty, but has not been observed to cause any digestive upsets.
Newly introduced or purchased cattle were rested and preconditioned on a nearby holding for around 1 week prior to entry to the feedlots. This consisted of vaccinating with 5 in 1 clostridial vaccine, drenching with triclabendazole and fenbendazole, and dosing with an oral chelated trace element mixture (Maxi-Min®, Virbac). The treatment with 5 in 1 and the trace element mixture was repeated after 4 weeks.
Respiratory disease was first observed on 1 April 2010, affecting around 80 of 300 cattle on the property later in that month (cohort 1). Affected cattle of cohort 1 (and later in cohort 2) showed exercise intolerance when being yarded, were anorexic, pyrexic (range 39.2°C to 40.9°C), had an infrequent dry cough associated with an elevated respiratory rate. A serous nasal discharge was evident in some cases, predominantly those with the highest temperatures. This discharge was occasionally flecked with mucopurulent material. Scouring was not a feature of the disease outbreak. The duration of clinical signs was usually around 7 to 10 days, but was extended in chronic cases for up to2 months. The occasional more severely affected animals that had become anorectic and lethargic were treated by injection of 20 mg/kg long-acting oxytetracycline (Bivatop 200 LA Injectable, Boehringer Ingelheim). These treated cattle steadily improved if treated early in the course of the infection.
Respiratory disease with the same clinical signs as the initial outbreak was observed in another 2 cohorts of 8 to 12 month-old weaners which were introduced to the property in the subsequent 2 months (Cohort 1 of around 45 head was introduced in weekly subgroups over the previous 2 months). Cohort 2 of around 50 head were introduced on the 20 April, only one week prior to clinical signs developing. Clinical signs were observed in all of these introduced cattle. The disease was also observed in cattle on neighbouring properties and on other holdings of the owner. All subsequently introduced cohorts showed clinical signs in most, if not all, cattle.
Pneumonic lesions were identified in 15 of 49 beasts which were slaughtered during the study period. These cattle represented the heavier individuals, up to 70 days on feed, that were suitable for slaughter and included many that been clinical cases and the occasional beast that had been treated with antibiotics. These animals did not have nasal discharges, but some were still coughing occasionally and had fevers. Lesions observed in affected animals were 5 – 10 cm diameter areas of consolidation in the ventral areas of the cranial lung lobes. These were apparent in around one third of the animals killed (Figure 1). Thoracic pleuritic tags were observed in around one third of the cattle with pneumonic lesions, occasionally affecting half of ribcage. Pulmonary adhesions were not a feature of the pathology. The tracheas of some of the individuals with pneumonic lungs contained patechial haemorrhages along the length of the mucosa and variable quantities of mucopurulent exudate which extended into the bronchi of the worst affected animals (Figure 2). Two chronically affected cattle are thought to have died on farm from complications of infection. These two were not subjected to necropsy.
Significant and generally consistent changes in 5/5 lung samples collected on 21 June at the abattoir indicated a multifocal suppurative bronchopneumonia with lymphoid hyperplasia and multifocal non-suppurative interstitial pneumonia with oedema and atelectasis. There were extensive changes associated with inflammatory cells and moderate multifocal thickening of the interstitium. The alveoli contained proteinaceous material and macrophages. Airways contained exocytosed neutrophils, lymphocytes, plasma cells and fibrinocellular material. The lung tissue was frequently compressed by extensive proliferation of lymphoid follicles within the submucosa and hyperplasia of the epithelium.
A diffuse subacute tracheitis was observed in 1 sample submitted showing patechial haemorrhages. Marked reactive hyperplasia was observed in 2 bronchial lymph nodes.
Aerobic bacterial culture was performed on the most severe lung lesions from 5 animals and swabs collected from 2 tracheas in which a mucopurulent exudates were present. No growth occurred in 4 of 5 lung samples; Pasteurella multocida was cultured from the remaining tissue and one of the tracheal exudates whilst Histophilus somni was cultured from the other exudate. Real time PCR assays for BVDV, IBR, PI-3 and BRSV were negative for all of these samples. However, bovine coronavirus (BCoV) was detected in 2 of 5 lung lesions including the tissue from which P. multocida was cultured. There was no evidence to support the involvement of Chlamydia spp. based on the histopathology in the slaughtered cattle.
Swabs and plain bloods were taken from animals on a number of occasions (Table 1). These were taken from cattle with prolonged clinical signs and from acutely infected animals in this propagating epidemic, but not from fully recovered individuals. Acute and convalescent serology indicated that seroconversion for IBR did not occur in any of the 3 affected cohorts sampled. Most of the affected cattle on the property and all newly introduced animals had prior exposure to PI-3 and BRSV, these being common unapparent calfhood infections. The animals bred by the owner had not been previously exposed to BVDV, however, introduced stock showed serological evidence of exposure. Infection with BVDV was not identified in clinically affected individuals. However, there was evidence of recent BVDV transmission between animals in the newly introduced cohorts.
Infection with BCoV was identified by Real Time-qPCR using nasal swabs collected from acutely infected animals in cohorts 2 and 3 (Table 1). The presence of this pathogen was confirmed by virus isolation. RT PCR did not identify infection with BVDV, PI-3 or BRSV and virus isolation was negative for these pathogens.
At the same time as nasal swabbing, swabs of conjunctival mucosa and rectum were also taken from affected cattle (cohorts 2 and 3). These were subjected to PCR examination. None of the conjunctival swabs provided a positive PCR for BCoV. However, 1 of 5 rectal swabs were positive for BCoV on 1/6/10, and 7 of 10 positive on 10/6/10. On only 3 of 8 occasions was there a positive rectal swab without a corresponding positive nasal swab. The association between a positive rectal and nasal swab was not statistically significant (P ~0.1) as the comparison was limited by the number of swabs taken.
|(positive results/number tested)||(positive results/number tested)|
*Cohort 1 = Original population of 300 cattle on the property in April 2010. Clinical signs first noted around 1/4/10.
*Cohort 2 = 8 – 12 month weaners introduced to the property one week prior to 27/4/10 when sampled during acute stage of infection.
*Cohort 3 = 8 – 12 month weaners introduced to the property one week prior to 1/6/10 when sampled during acute stage of infection.
In the absence of evidence to implicate concurrent infection with any other viral respiratory pathogens, it appears that bovine coronavirus has given rise to a widespread propagating winter outbreak of bovine respiratory disease in this herd. This virus induced an enzootic pneumonia and associated rhinotracheitis in many of those infected. The primary viral insult exacerbated by secondary bacterial invasion by some of the usual suspects, namely P multocida andH. somnus. Although there is limited information from bacterial culture, it is likely that Mannheimia haemolytica, which is usually associated with more severe disease, has not been significantly involved. The risk factors involved in this occurrence probably include the introduction of weaner cattle from a wide range of sources and stresses associated with cooler weather, aggregation, saleyards, trucking, feed changes, preconditioning treatments and are similar to, but not as severe as those found in a large commercial feedlot. It cannot be determined whether a virulent respiratory form of BCoV was introduced or whether an already present variant with enteric tropism mutated to become more adapted to the respiratory tract.
Although rare as a significant respiratory pathogen in Australia, BCoV should be considered in the diagnosis and control of bovine respiratory disease. One other outbreak of BRD associated with BCoV has been seen on live export cattle on boats from WA (P Kirkland, pers comm.). BCoV in Australia is usually associated with enteritis in calves under 3 weeks of age, and usually with a lower morbidity rate than the more common rotavirus infections. BCoV disease in calves is more severe than rotavirus and often results in blood-tinged scours. Affected calves may also suffer from an interstitial pneumonia, although this manifestation is more commonly recognised overseas.
To place them in a wider perspective, Coronaviruses primarily infect the upper respiratory and gastrointestinal tract of mammals and birds. Four to five different currently known strains of coronaviruses infect humans. The most notorious human coronavirus, SARS-CoV, which causes SARS, has an unusual pathogenesis because it causes both upper and lower respiratory tract infections and can also cause gastroenteritis. Coronaviruses are believed to cause a significant percentage of all common colds in human adults. TGE in pigs and FIP in cats are also caused by coronaviruses. Coronaviruses are RNA viruses which can mutate readily.
The peak incidence of infections occurs during the cooler months due to the heat sensitivity of the virus. Under cool conditions and moderate humidity coronaviruses are likely to survive for days in the environment, whereas at warmer temperatures survival may be limited to hours only. Respiratory trophic forms replicate in the epithelium of the upper respiratory tract. Persistence, with carrier states, is common.
In the northern hemisphere, as well as causing calf scours, BCoV is associated with outbreaks of winter dysentery in adult cattle and respiratory disease in calves and older age groups1,2. In an atypical outbreak in Italy the majority of cattle in a milking herd were affected by a severe diarrhoea, sometimes bloody, followed soon after by respiratory disease in the same animals. This was characterised by fever, coughing, ocular and nasal discharges1.
Currently weaner introductions to the affected farm near Moruya are rested and preconditioned for a month prior to entry into the concentrate feeding paddocks. However, despite this 'lower stress' approach and the higher temperatures experience during this wet summer, the disease continues to cause sporadic cases in introduced stock. There is some fear that even if the property was destocked of introduced animals, that the respiratory trophic BCoV would return 'over the fence' from neighbouring properties.