AVIAN CHOLERA

GENERAL INTRODUCTION

Avian cholera, or fowl cholera, is caused by Pasteurella multocida and is a significant cause of mortality, especially in waterfowl, in many parts of the world, including the Americas, Europe, Asia and Africa.

AETIOLOGY

Pasteurella multocida serotypes 1, 3 and 4 are usually iso­lated from wildfowl, and type A are the most virulent strains owing to their capacity to resist phagocytosis.

Epidemiology

Outbreaks of fowl cholera in wild birds are reported from many countries, and disease occurs in many major flyways, with reports of outbreaks more frequent in North Ameri­ca’s wildfowl populations. Extensive epidemics of avian cholera involving hundreds or thousands of aquatic birds are probably more likely to be recognized and reported than the many smaller disease foci. Some species suffer greater mortality than others, and cases in coots and swans usually precede mortality in mallards (Anas platyrhynchos) and teal (Anas crecca). There is no consistent evidence for differential susceptibility by sex or host age, even though greater mortality in a particular sex or age has been reported in different publications.

Molecular characterization of P multocida isolated from wild and domestic birds in Denmark indicates that isolates from wild birds have indistinguishable patterns, irrespec­tive of species, origin and year of isolation, whereas several clones exist among domestic poultry¹-¹³). Spillover from wildfowl to poultry, or vice versa, is usually not clear.

Geographical Distribution and Hosts

Pasteurella multocida is highly infectious and produces sep- ticaemic and respiratory diseases in more than 180 species of wild birds, such as pelicans, cormorants, wading birds, herons, flamingo, swans, geese, ducks, eagles, hawks, falcons, gallinaceous birds, cranes, rails, coots, shorebirds, gulls, auks, pigeons, doves, owls, swifts, jays, crows, thrushes, starlings, sparrows and finches (see ⁽¹⁴) for further detail on species), but its host range may be still greater because many cases remain unreported or unconfirmed.

In the UK, a corvid respiratory disease (CRD), which affects primarily rooks ( Corvusfrugilegus) at breeding colo­nies and roosts and which has been recognized for 20 years, is now thought to be caused by P multocida infec­tion, possibly in association with other, as yet unknown, pathogens. Birds may be seen ill, weak and dyspnoeic, as the condition is chronic in nature. Dead birds have pneu­monia and airsacculitis, from which P multocida can be cultured. Little is known of the epidemiology; however, in one incident approximately 30 birds died over a 9-month period from a flock of about 200—300 birds. The P mul­tocida isolates from these birds were all capsular type F, but it is not known if this pathogen poses a risk to domestic poultry⁽¹⁵⁾.

Environmental Factors

In the past avian cholera was considered a disease of winter, but in recent decades outbreaks have been observed in spring and during the nesting season, and cases are recorded now throughout the year. Probably the concentrations of birds that collect in the winter period, for example in wetland habitats or spring staging grounds (migration stop-over localities), makes mortality more noticeable, thus biasing data collection. In colonial breeding birds, such as eider (Somateria mollissima) and cormorant (Pha- lacrocorax carbo^), the breeding season leads to high bird densities, which facilitate transmission between close­flocking individuals. This could explain why outbreaks of avian cholera in eiders are reported only in breeding colo- nies⁽¹³⁾. However, it could also be easier to detect outbreaks when birds are concentrated in breeding areas.

Many authors report that P multocida can persist for a long time in wetlands after avian cholera outbreaks and that bacteria survival in the environment is linked to water quality (calcium, magnesium, chloride, sodium and sul­phate concentrations), with survival increased by the pres­ence of salt and organic matter. However, field studies have shown that the bacteria can be isolated from water samples for only a few days, or at the most a few weeks, after an avian cholera outbreak. During an outbreak in Denmark no P. multocida isolate was obtained from water from a small water pond)¹³).

Probably the environment is not a good reservoir of P multocida in the absence of birds, and only the introduc­tion of infected birds can trigger outbreaks. Even though P. multocida can survive in water for more than 1 year under experimental conditions, field conditions in water­fowl habitats are very different, and the recovery of the bacterium is very rare in ponds and wetland water. Con­sidering the wide species distribution of the pathogen, it may be continually introduced to an area as carrier birds arrive. In wetlands the presence of ill birds can initiate an epidemic because infected carcasses may lead to a short­term accumulation of P multocida and thus act as a source of infection for susceptible birds. It is likely that many outbreaks involve small numbers of animals and are unde­tected. High bird density is probably the most frequent and important factor in initiating outbreaks¹-¹⁴).

Epidemiological Role of Wild Animals

Data collected from 1996 to 2003 in Denmark suggest that a P. multocida strain has survived during several years among wild birds in that country)¹³), and this supports the hypothesis that wild birds can act as a reservoir for P multocida — as does the fact that disease often occurs in areas where no sick animals have been introduced and wild birds are capable of spreading the infection to new areas.

Transmission

Invertebrates have been considered as a possible mainte­nance source for P multocida; however, even if transmis­sion of infection through ingestion of infected invertebrate or arthropods species, such as maggots or flies, has proven to be possible, it is highly unlikely that this represents an important source of transmission)¹⁴). Ectoparasites have been found to transmit P. multocida, and in the soft tick Argas persicus the bacteria can survive for at least 1 month and may have a 1,000-fold increase. Among ectoparasites, poultry mites (Dermanyssus spp.) and lice have been dem­onstrated to be able to transmit the bacteria.

Apart from these routes, transmission mainly occurs through inhalation of aerosols. Aerosols are created by waterfowl splashing, and in the aerosol the bacterial con­centration could be 10 to 1,000 times higher than the water from which it originates. This occurs because animal movements lead to air bubble rupture, which ejects the bacteria present in the water surface microlayer into the atmosphere. Birds taking flight in large rafts by running across the water has been considered as a predisposing factor, particularly as coots, which run in large rafts, are usually the first to show disease and have a higher morbid­ity. Considering that bacteria are present in larger amounts at the water surface, species that graze frequently at the surface, such as coots, could also more easily ingest P mul­tocida. Transmission by predators or scavenging of infected birds could also be important in disseminating infection. The risk of P. multocida infection by ingestion of contami­nated food or soil is mainly due to the shedding of P multocida by diseased birds in faeces, or from the carcasses of dead birds, which increases the environmental contami­nation, facilitating the transmission of the bacteria.

PATHOGENESIS, PATHOLOGY AND IMMUNITY

Pasteurella multocida enter avian tissues through the mucous membranes of the pharynx, upper respiratory pas­sages and conjunctivae, and in some cases through cutane­ous wounds. Septicaemia results from this invasion when P. multocida avoids the host phagocytosis, and the pre­dominant lesions, haemorrhages and necrotic foci are caused by endotoxaemia. At necropsy, in acute forms birds are in good body condition. Gross lesions consist of petechial haemorrhages on the heart surface and focal necrosis in the liver and other internal organs. Mucoid enteritis with necrotic-diphtheritic lesions, is also found in chronic forms, as well as mucoid inflammation of the upper respiratory tract with mucopurulent exudate and cytoplasmatic vacuolation, loss of cilia and desquamation of individual cells. In some areas there is accumulation of numerous bacteria, surrounded by neutrophilic granulo­cytes in the lung parenchyma.

Birds that recover from infection are usually protected from reinfection, even if some authors report a low prevalence of birds with detectable antibodies after an outbreak.

CLINICAL SIGNS AND TREATMENT

Clinical signs are difficult to detect, particularly in acute disease, and the death of the birds maybe the only visible sign. In peracute or chronic forms, when birds are found alive, infected individuals show fever, depression and ano­rexia, mucoid oral discharge, ruffled feathers, diarrhoea, conjunctivitis and torticollis due to nervous system mani­festations. In many cases respiratory function is compro­mised and dyspnoea with tachypnoea is frequently seen in chronic infection.

Treatment is based on the use of sulfonamides, and antibiotics are commonly used. Sulfaquinoxaline sodium in feed or water usually controls mortality, as do sulfamet­hazine and sulfadimethoxine. High levels of tetracycline antibiotics in the feed (0.04%), drinking water, or admin­istered parenterally may be useful. Penicillin is often effec­tive for sulfa-resistant infections.

MANAGEMENT, CONTROL AND REGULATIONS

Monitoring for waterfowl mortality is probably the most important recommendation, because this allows detection of disease foci at their earliest stage and the implementa­tion of control actions in order to reduce transmission and prevent high losses. It has been suggested that one diseased bird may be sufficient to start an outbreak, owing to con­tamination of water and environment from the fluids of the dead animal, allowing transmission of the bacterium to susceptible birds. Scavenging infected carcasses and invertebrate dissemination can obviously increase the dis­semination of the pathogen. Considering that carcasses probably represent the major source of P. multocida, carcass removal can be the most successful management strategy to reduce the contamination and persistence of P multoc­ida and, even if no conclusive study has been done, it seems to be effective in controlling avian cholera out­breaks. Habitat manipulation could also be used to control outbreaks by selective drainage or water pumping and diversion in order to modify waterfowl species distribution and densities, and also to dilute the pathogen contamina­tion of the water. Clearly the reduction in wetlands increases the crowding of waterfowl and can favour trans­mission of the pathogen in crowded populations.

Pasteurella multocida vaccines are available for poultry; however, few cases of wildfowl vaccination have been reported, and this option is likely to be feasible only in small, captive flocks.

PUBLIC HEALTH CONCERN

Disease in humans caused by P multocida is not uncom­mon, and P multocida may be considered a zoonotic organism. No reports exist of direct transmission from wild birds or poultry to humans or vice versa, but the possibility for such infections cannot be excluded.

SIGNIFICANCE AND IMPLICATION FOR ANIMAL HEALTH

Avian cholera outbreaks can cause severe mortality in some areas, and reports from North America seem to indicate that during such outbreaks mortality can cause a popula­tion loss of about 0.2% in ducks and of 3.9% in swans. In common eider avian cholera outbreaks can have an important impact on post-hatching survival, and this affects recruitment into the breeding population and thus population dynamics¹-¹⁶).

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