Throughout the world, the most common respiratory disorders of sheep are rhinitis/sinusitis and pneumonia, caused by a wide range of host-pathogen-environment (HPE) interactions that reflect the various sheep husbandry systems used in different countries. In Australia, where extensive husbandry systems predominate, with the exception of verminous rhinitis (Oestrous ovis) and pneumonia (Mullerius and Dictyocaulus spp) and CLA, the prevalence of clinical respiratory disease in small ruminants is generally considered sporadic and of lower priority than other health issues such as internal and external parasitism (although with modern broad-spectrum anthelmintics and increasing use of combination vaccines that include CLA, the clinical importance of these entities has also declined in recent decades). However, abattoir surveys in Australia and certainly in European countries, suggests that the contribution of pneumonic diseases to lowered sheep productivity may be underestimated. Pneumonic lesions are frequently seen at necropsy in sheep of all ages and clinical signs are often evident when flocks of sheep are driven. It is unlikely that all these cases are due to inappropriate anthelmintic administration causing aspiration pneumonia. Further, as intensifications systems for sheep production are on the increase in Australia, it is likely that respiratory diseases will emerge as a more important cause of production loss to the Australian sheep industry that will be deserving of more investigation and detailed research.
However, there is no doubt about the importance of respiratory disorders in the many countries where sheep are housed for long periods and their respiratory tracts compromised by environmental insults (eg ammonia that compromises tracheal ciliary clearance mechanisms). This situation favours the establishment of the various pathogens that lead to pneumonias of an acute, sub-acute, chronic, or progressive nature, that are a major cause of veterinary attention in small ruminant systems in European and the North American countries particularly.
Acute LRT disorders
Acute ovine pneumonias may be associated with infection with parainfluenza type 3 (PI-3), adenovirus, and respiratory syncytial virus, most often affecting lambs (and kids). PI-3 is an enveloped RNA virus (family Paramyxoviridae) that induces a generally mild interstitial pneumonia with signs that may include coughing, a serous nasal and/or ocular discharge, fever (40°–41°C), and hyperpnoea (or dyspnoea?). The single PI-3 serotype for sheep that has been identified is distinct from the bovine PI-3 serotype and the diagnosis confirmed by its isolation from nasal swabs from affected animals, or by comparison of acute and convalescent serology. Treatment is usually only warranted in severely affected animals where secondary pathogens including Pasteurella multocida, Mannhaemia haemolytica, and Mycoplasma spp may have become established (note that PI-3 vaccines have not been specifically developed for use in small ruminants).
Ovine Respiratory Disease Complex
The pathogens M haemolytica (Mh), P multocida (Pm), Mycoplasma spp, Chlamydia pneumoniae, and Salmonella spp may also be associated with primary acute to subacute bronchopneumonia in sheep and goats, although Mh and Pm can be cultured from the upper respiratory tract of normal sheep and goats. Mycoplasma ovipneumoniae can cause a mild bronchopneumonia alone, although is more often isolated along with Mh from sheep and goats with severe pneumonia, suggesting that the Mycoplasma (potentially with some or all of the above viral infections) may predispose the lung to invasion by this organism, with peracute cases manifest as septicaemia also occurring. The HPE 'stress' factors involved in acute bronchopneumonia of small ruminants include: introduction of new animals; high stocking density; poor ventilation; and sudden alterations in nutrition (eg acute to subacute acidosis); although other factors may also predispose to development of pneumonia in this Ovine Respiratory Disease Complex, a major cause of mortality and morbidity in lambs in intensive husbandry in many parts of the world.
Chronic LRT disorders
Chronic, progressive viral pneumonia is relatively common in adult small ruminants in may parts of the world other than Australia and NZ, and includes progressive interstitial pneumonia due to lentiviruses (family Retroviridae) or ovine progressive pneumonia (Marshes progressive pneumonia in North America or Maedi in European countries) and ovine pulmonary adenocarcinoma (Jaagsiekte or the contagious lung tumor of sheep and infrequently, of goats). Note that the retrovirus that causes pneumonia in goats, CAE virus (Caprine Arthritis and Encephalitis) has been present in Australia since the 1970's. Chronic, progressive, interstitial proliferative pneumonia is usually associated with the lentiviruses (so-called slow-virus infections). In both progressive pneumonia and pulmonary adenocarcinoma, the entire lung can be affected in a gradual proliferative process of pulmonary tissue resulting in progressive dyspnoea, anorexia, and weight loss.
Maedi-visna is a chronic, progressive viral infection characterised by a prolonged incubation period and predominantly two clinical manifestations; pneumonia and encephalomyelitis (Maedi means dyspnoea and Visna means wasting in Icelandic language). The virus also infects the udder causing a chronic mastitis and reduced milk yield. Generally, only one form of the disease occurs in one animal and often one form predominates in any one flock. The disease does occur in goats but transmission between sheep and goats does not usually occur in field cases. Vertical transmission, by the excretion of virus-infected leucocytes in colostrum and milk, is the main form of spread of Maedi-visna in flocks. Transmission to the foetus in utero occurs but is rare and it is believed that transmission via ova or sperm does not occur, with horizontal transmission occurring mainly by the inhalation of infected respiratory secretions from infected sheep. Infection is introduced into clean flocks by horizontal transmission from an introduced, infected sheep. Although the virus does not survive for more than two weeks outside the host, the incubation period is may exceed several years. Following infection, viral replication is restricted for a prolonged period, during which the viral genetic material resides in infected cells as proviral DNA until the infection progresses and clinical signs are associated with the chronic progressive proliferation of lymphoid tissue in lungs, brain, udder and joints.
The pulmonary lesions in Maedi are an interstitial pneumonia that restricts the alveolar space, leading to anoxia, although many sheep remain in a sub-clinical phase of the disease. The variation in expression of the disease as primarily respiratory, nervous or mastitic, is presumed due to different tissue tropism of the strains of the virus, differences between breeds and flocks of sheep in their susceptibility and the effects of different management factors. Animals with Maedi are listless, emaciated and dyspnoeic. There is coughing and nasal discharge but most affected sheep retain their appetite. Udder induration, hind-limb paralysis and, in some cases, swollen joints with or without lameness, may also be present in the flock. Clinical signs last for 3 to 12 months but the disease is inevitably fatal. Sheep pulmonary adenomatosis (Jaagsiekte) can produce similar clinical signs with similar flock history and, in some countries, can be simultaneously present in the same flock and the same sheep, although is usually characterised by a profuse nasal discharge and a shorter clinical course (the two diseases can be readily differentiated on histopathology). Parasitic pneumonia and melioidosis also have signs of chronic respiratory disease.
Diagnosis of Maedi is confirmed either by one of a number of techniques for virus identification or by serology used as a flock diagnosis. Note that negative serology in individual cases is not reliable evidence of freedom from infection, as the time between infection and seroconversion is variable and may be as long as one or more years, with some infected animals remaining seronegative. There is no treatment for Maedi-Visna. National control programs in endemically infected countries vary in their approach but are based largely on the identification of clean flocks by serological testing; separation of lambs from ewes and artificial rearing of lambs in flocks with low prevalence of infection; or complete destocking and replacement in flocks with moderate or higher levels of infection.
Ovine pulmonary adenomatosis (OPA, Jaagsiekte)
OPA is a chronic progressive pneumonia of sheep characterised by histological lesions of adenomatous proliferations in alveolar walls. Clinically affected sheep produce profuse watery mucous in the lungs leading to excessive discharge from the nose, aided at examination by 'wheelbarowing' the suspected affected animal. It is also caused by a retrovirus (and is one of the three so-called 'slow virus' infections of sheep with Maedi-visna and Scrapie, although the latter is now well recognised as a prion disorder or TSE). The disease occurs in Britain, continental Europe, South Africa, Israel, Asia and Iceland. Only sheep are infected in natural cases and transmission is presumed to occur by inhalation of infected droplets and by vertical transmission to the foetus. Close housing in winter, as occurs routinely in Iceland, promotes transmission but is not essential for flock outbreaks. The incubation period is 1 to 3 years and as the adenomatous proliferations encroach on the alveolar space and lead to anoxia, coughing occurs, although it is not a prominent sign. Emaciation, dyspnoea and panting after exercise, plus profuse watery discharge from the nose, are characteristic signs, with moist rales on auscultation over affected areas of lung. The disease is inevitably fatal and at necropsy, the lungs are enlarged, heavy from consolidation and there is frothy fluid in the bronchi. Histopathology is characteristic. There is no treatment. A vaccine has been used successfully in Kenya.
Diseases of the upper respiratory tract of sheep and goats in Australia include rhinitis/sinusitis and pharyngeal disorders. Sinusitis may be caused by the larvae of Oestrus ovis, nasal foreign bodies, and less commonly, nasal mycotic infections and tumours. Clinical signs associated with sinusitis may include some or all of: unilateral or bilateral, serous to mucopurrulent nasal discharge; decreased or lack of airflow through one or both nostrils; coughing; sneezing; and mild to severe respiratory distress. The various nasal neoplasms reported include adenopapillomas (nasal polyps), adenomas, adenocarcinomas, lymphosarcomas (goats), and squamous cell carcinomas (sheep). Pharyngeal disorders include trauma and abscessation, particularly in association with overly aggressive use of equipment used to administer boluses that cause injuries resulting in discrete abscesses or extensive and diffuse cellulitis that can interfere with swallowing and occasionally lead to respiratory distress. Bacteria commonly isolated after an incident of pharyngeal trauma include Trueperella, Pasteurella multocida, Mannheimia haemolytica, and Fusobacterium. Laryngeal chondritis is an obstructive upper respiratory tract disease characterised by severe dyspnea most commonly encountered in meat-breed rams 18–24 mo old. Acute onset of severe respiratory distress with marked inspiratory effort is caused by oedema of the arytenoid cartilages of the larynx, resulting in narrowing of the lumen and affected animals stand with the neck extended, head held lowered with flared nostrils, and mouth open.
Enzootic Nasal Tumour (ENT)
In European countries, ENT is caused by an exogenous retrovirus (ENTV) that can be transmitted experimentally by tumour homogenates, explaining the widespread occurrence of this condition within some flocks. ENT generally affects mature animals (2–4 yr old), although has been reported in animals as young as 4 mo old. The lesion may be unilateral or bilateral, resulting in either unilateral or bilateral serous, mucoid, or mucopurulent nasal discharge, with deviation of the nasal septum in advanced unilateral tumours. Affected animals show progressive signs of inspiratory dyspnea with open-mouth breathing, decreased airflow at the nares, dullness on percussion over the turbinates, sneezing, and head-shaking. Stridor may also be caused by compression of the larynx by enlarged retropharyngeal lymph nodes associated with abscessation of the head.
A major differential diagnosis of ENT in Spain, is a granulomatous rhinitis causing tumour-like projections of chronic inflammatory tissue from one or both nares, associated with infection with a Salmonella sp. Laryngeal chondritis also results in inspiratory dyspnea of varying severity. With advancing tumour growth, exophthalmos and facial deformity may occur, although metastasis is uncommon. Outcome depends on the tumour type, condition of the animal, and extent of the lesion, but affected animals are usually culled for animal welfare and commercial reasons (surgical removal of a noninvasive tumour is rarely undertaken).
Addressing respiratory disorders is the most challenging small ruminant health management concern in many overseas countries. With increasing pressure on the global food system to meet burgeoning demand from rapidly developing nations with extremely large populations rapidly altering their dietary preferences (eg China), intensive small ruminant husbandry systems are likely to become more prominent, and this has commenced in Australia (eg sheep feedlots). Despite our abundance of grazing lands, consumer demands for high quality meat and dairy products from sheep and goats is creating marketing opportunities that will result in more intensive small ruminant husbandry systems and inevitably, more respiratory disorders. Whilst it is reasonable to expect our national biosecurity system can protect our sheep industry from lentivirus infections (unlike our goat industry), diagnosis and management of small ruminant respiratory disease is very likely to be a more challenging task than it has traditionally been. Australian sheep veterinarians able to visit intensive small ruminant systems in other countries where there is frequently, extremely high dependence on antimicrobials and astounding use of vaccination (often autogenous) to manage respiratory disorders, are advised to do so, for as Louis Pasteur said: 'chance favours the prepared mind'.