Pasteurella infections in wild mammals

AETIOLOGY

Pasteurella multocida has been differentiated into three subspecies: P multocida multocida, P multocida septica and P. multocida gallicida, based on their ability to ferment d -sorbitol and trehalose.

Infectious Diseases of Wild Mammals and Birds in Europe, First Edition. Edited by Dolores Gavier-Widen, J. Paul Duff, and Anna Meredith. © 2012 Blackwell Publishing Ltd. Published 2012 by Blackwell Publishing Ltd.

Mannheimia haemolytica (formerly Pasteurella haemo­lytica biotype A) was established in 1999 and includes all trehalose- negative strains of the P haemolytica complex that ferment mannitol, but not D-mannose. Mannheimia haemolytica is the most common and studied of the five species included in the genera. Although M. haemolytica ferments arabinose, strains that ferment trehalose are now classified as Pasteurella trehalosi. This last species includes isolates previously classified as P haemolytica biotype T and serotypes 3, 4, 10 and 15, whereas isolates previously clas­sified as P haemolytica biotype A 1, 2, 5—9, 12—14, 16 and 17 are now classified as M. haemolytica.

EPIDEMIOLOGY

Pasteurella multocida serogroup A is mainly associated with avian cholera, rabbit pasteurellosis and pneumonia in ruminants.

Pasteurella multocida serotype D is a commensal and may cause disease in stressed animals, whereas serogroups B and E cause haemorrhagic septicaemia. Endotoxaemia is probably the cause of haemorrhages and necrotic foci as well as of disseminated intravascular coagulation, all of which are frequently reported. Serogroup E is usually a non- commensal bacterium and is associated with acute and highly fatal clinical forms of haemorrhagic septicaemia that mainly affect species belonging to the Bovidae family.

Mannheimia haemolytica is one of the most important pathogens in domestic bovids, where it is the causative agent of pneumonic pasteurellosis — known as ‘shipping fever’ because of its occurrence in translocated animals. Field evidence suggests that viral and/or mycoplasmal agents predispose the host to pneumonia by impairing host defences, allowing a rapid proliferation of M.

Pasteurella spp. and Mannheimia spp. are distributed worldwide. Pasteurella multocida, can cause severe disease, such as haemorrhagic septicaemia and pneumonia in ungulates (Dama dama, Cervus elaphus, Odocoileus virgin- ianus, Odocoileus hemionus, Ovis musimon, Rupicapra rupi- capra, Capra ibex, Rangifer tarandus), avian cholera in birds, atrophic rhinitis in pigs and wild boar (Sus scrofa), and pneumonia or septicaemia in foxes (Vulpes vulpes), mink (Mustela vison), coypu (Myocastor coypus), rabbits (Oryctolagus curiculus), hares (L epus europaeus) and wild brown rats (Rattus norvegicus). Pasteurella multocida sero­type A is frequently isolated from healthy or dead bats belonging to several bat species of the genera Pipistrellus, Plecotus, Vespertilio, Myotis and Eptesicus. It has also been reported to cause severe outbreaks in captive fallow deer (Dama dama) herds^(1-4). Haemorrhagic septicaemia, an acute form of P. multocida infection of wild and domestic animals, killed 273 fallow deer out of a population of 1,800 during 1992—1996 in a large deer park in Denmark⁽⁵⁾.

Mannheimia haemolytica and P trehalosi are commensals of the nasopharynx and are frequently isolated from Bovidae such as Spanish ibex ( Capra pyrenaica )⁽⁶⁾, chamois (Rupicapra rupicapra), Alpine ibex ( Capra ibex) and mouf­flon (O vis musimon), as well as from European brown hares — where they cause pneumonia and septicaemia, with both single case reports or, more frequently, disease out­breaks (Ferroglio, unpublished data).

Mannheimia haemolytica is frequently isolated from small domesticated ruminants and also from wild rumi­nants. It is a cause of septicaemia and pneumonia, usually in young animals rather than in adults.

The commensal nature and the ubiquitous species dis­tribution of Pasteurella spp. and Mannheimia spp. suggest that the pathogen is acquired during the early stages of life. Stressors, such as weather changes, poor condition and overcrowding, can trigger outbreaks, with high morbidity and mortality in wild animals.

I n wild ruminant disease-free herds, the subclinical P multocida carrier rate is usually very low (3—5%), even though after outbreaks up to 50% of animals harbour this bacteria in their nasopharyngeal or tonsillar mucosae. In a survey of healthy Spanish ibex (Capra pyrenaica his- panica), M. haemolytica was isolated from 11.5% of the ibex tested, while 8.1% and 3.4% of animals were positive for P multocida biotype A and P trehalosi, respectively¹-⁶). So it is plausible that wild species can act as maintenance host for these bacteria.

Pasteurellaceae spread, directly or indirectly, to suscepti­ble animals through saliva or nasal discharges from dis­eased animals. Contamination of food and water can occur and vectors — ticks and fleas — are probably capable of transmitting infection. Wound infection due to animal bites or scratches has been reported in humans, cats and dogs, as demonstrated by the fact that 54% of birds with bite wounds attributable to cats were infected with P multocida. The presence of numerous P multocida strains in bats suggests that interspecies transmission, following cat bites, is probably the most frequent source of infection in bats in Europe¹-⁴).

PATHOGENESIS, PATHOLOGY AND IMMUNITY

It is considered that disease is caused by the invasion by commensal P. multocida as a result of the decrease in the host immunity caused by stressor factors; however, aerosol or direct contact may give rise to transmission in addition to vectors, such as ticks and fleas. In P multocida infection septicaemia occurs as a result of the bacterial penetration of the pharyngeal mucous membranes by pathogenic bacteria, and it has been demonstrated that serotype A virulence is correlated with the capacity to avoid phagocytosis.

Fallow deer that die of P multocida infection show oedema in the pharynx, larynx and the tongue, with necrotic mucosae covered by mucoid or Abrinopurulent exudates. There are haemorrhages and oedema in mucosae and serosae, and haemorrhages are also present in lungs, lymph nodes, spleen and other organs. When pneumonia occurs, pulmonary lesions are similar to those observed in many domestic and wild ruminants and are represented by acute fibrinous pneumonia with pleuritis localized in the cranioventral part of the lung.

In European brown hares, P multocida causes purulent or catarrhal conjunctivitis, pneumonia, peritonitis, endo­carditis and enlargement of the spleen. In hares pneumo­nia can also be due to M. haemolytica, and usually gross lesions include purulent exudates in the trachea and bronchi, bronchiolitis and purulent pneumonia.

Mannheimia haemolytica inhabits the nasal cavity and the tonsillar crypts. Immunosuppression, caused for example by stress, results in the inability of the host to control the replication of M. haemolytica. After invading the lungs, M. haemolytica infects the lower respiratory tract and alveolar epithelia, resulting in rapid development of fibrinous pleuropneumonia, with deterioration of lung structure and function, by infiltration of neutrophils, fibrin and blood in bronchi, bronchioles and alveoli.

The virulence factors involved in infection include a leucotoxin that prevents phagocytosis and is lethal for leucocytes and platelets. The enzymes released by these lytic processes recruit further leucocytes by means of chemotaxis. A lipopolysaccharide (LPS) is also produced and stimulates the production of cytokines, oxygen radi­cals and proteases that damage the lung parenchyma. The LPS also acts to decrease cardiac output, thereby reducing blood circulation to the lungs. Other factors are released that act in concert to impair the innate defences of the lungs. Haemorrhage and thrombosis in the lungs may be due to platelet lysis, which is also caused by leucotoxin(⁷).

As is also the case for Pasteurella trehalosi, the main viru­lence factors are the leucotoxins, and all strains that exhibit β-haemolysis on sheep blood agar have the structural leu­cotoxin gene.

Mycoplasma ovipneumoniae, which produces dysfunc­tion in the ciliary activity of the epithelial cells of the upper respiratory tract, may predispose bighorn sheep to M. haemolytica^'). Development of immunity in wildlife is poorly understood, but animals that have recovered from pasteurellosis usually remain healthy during subsequent outbreaks⁽⁵⁾.

CLINICAL SIGNS

Fallow deer infected with P. multocida show swelling of the head and the neck that can reach the shoulder and the sternum, with subcutaneous gelatinous oedema and scat­tered petechial haemorrhages. In outbreaks of septicaemic disease, affected animals have fever and depression and may have oedema of the head and neck and bleeding from orifices. Clinical signs of pneumonia are the same for both M. haemolytica and P trehalosi, and affected animals show dyspnoea and coughing, and mucous exudate is frequently visible from nostrils. Animals may recover from this infec­tion, but with reduced lung capacity.

Clinical signs of pasteurellosis in hares depend on the route of infection, and include oculonasal discharge with snuffling, conjunctivitis and pneumonia in the case of respiratory route infection, torticollis in the case of otitis, and vaginal discharge due to metritis. When subcutaneous abscessation occurs, often as a result of wound infection usually by bite wounds, it is common to see swelling in several sites.

DIAGNOSIS

Pasteurellosis is suspected from typical clinical signs and gross lesions, and is confirmed by isolation and identifica­tion of bacteria from representative lesions on blood agar or glucose agar plates supplemented with serum. Colonies after 24 hours’ incubation and growth are 1—2 mm wide, smooth, greyish and variably β-haemolytic. When septi­caemia is present, bacteria can also be easily recovered from cerebrospinal fluid. Species differentiation is based on phe­notype, but recently molecular methods have allowed a better characterization of isolates, providing greater value in epidemiological studies¹-⁴). Assessing the clinical signifi­cance of Pasteurella spp. or Mannheimia spp. isolates from diseased animals in combination with other pathogens presents difficulties, because it is not possible to trace lesions to a given pathogen. Also assessing the potential clinical significance of Pasteurellaceae when isolated from healthy animals is very difficult. Serology has limited value in clinical diagnosis; however, it has an important role in evaluating the immune status of animals and the epidemi­ology of the infection at the population level.

MANAGEMENT, CONTROL AND REGULATIONS

Only indirect measures can be adopted to control pas­teurellosis in wildlife. Action to increase the nutritional status of ungulate herds (i.e. artificial feeding) has been suggested by some authors, but overcrowding at feeding places could be a major risk for transmission of these pathogens. Considering that in some cases, especially in mountain ungulates on extensive natural pasture shared with wild ungulates, domestic animals can also be the source of infection, reducing the contact and thereby mutual transmission between domestic and wild animals is probably the most effective management action.

PUBLIC HEALTH CONCERN

Wild mammal pasteurellae are potentially zoonotic; however, reports of human disease linked with wild mammal infections are rare. A young farmer in England died from P multocida septicaemia thought to have come from a freak skin scratch he suffered from a wounded wild rabbit that he had shot. He had been in good health prior to the incident¹-⁹).

SIGNIFICANCE AND IMPLICATIONS FOR ANIMAL HEALTH

Pneumonia is one of the main health concerns in moun­tain ruminants, where pneumonia outbreaks are relatively frequent, with an important impact on the affected species at population level. Pasteurellaceae, mainly M. haemolytica and P trehalosi — occasionally P multocida if it is also iso­lated from diseased animals — are considered to be the main agents. In Alpine chamois (Rupicapra rupicapra) and Alpine ibex ( Capra ibex) — in which pneumonia outbreaks can cause up to 30% mortality in herds, affecting mostly kids and yearlings — 30% of affected animals tested posi­tive for P trehalosi, whereas 11% were positive for P mul- tocida A (Ferroglio, unpublished data).

I n bighorn sheep in North America, it seems that P trehalosi is more frequently isolated than M. haemolytica from healthy animals¹-¹⁰’¹¹); however, the role of domestic sheep and cattle as carriers of M. haemolytica to bighorn has been proven⁽¹¹’¹²⁾.