Avian bordetellosis is a highly infectious, acute upper respiratory tract disease of turkeys characterized by high morbidity and usually low mortality. Other synonyms previously used for the disease include Alcaligenes rhinotracheitis, adenovirus-associated respiratory disease, acute respiratory disease syndrome, and turkey rhinotracheitis.
Although the disease primarily affects turkeys, quail are also susceptible, and it is an opportunistic infection in chickens. Damage to the upper respiratory tract from prior exposure to an upper respiratory disease agent or vaccine such as infectious bronchitis virus or Newcastle disease virus, or from an environmental irritant such as ammonia, is necessary to induce signs in chickens.
Bordetellosis has been identified in almost every area of the world where turkeys are intensively reared. Historically, it has been severe in focal areas and rare or nonapparent in other locations. The reasons for these epidemiologic differences are not known.
Etiology and Pathogenesis
The causative agent is Bordetella avium, a gram-negative, nonfermentative, motile, aerobic bacillus. It can be grown using many different media, including MacConkey agar, Bordet-Gengou agar, veal infusion broth, trypticase soy broth, blood agar, and brain-heart infusion broth. Strains of B avium typically produce small (0.2–1 mm diameter after 24 hr incubation), compact, translucent, glistening pearl-like colonies with smooth edges. After serial passage in the laboratory, a rough colony type with a dry appearance and a serrated, irregular edge can be observed for some isolates. Rough colonies represent a global suppression of virulence factors in B avium termed antigenic variation and are nonpathogenic. When the bacillus is grown in broth media high in nutrients, filamentous forms can be observed.
The mechanism of pathogenesis involves the ability of B avium to destroy ciliated epithelial cells in the trachea. Certain strains of the bacteria adhere to the ciliated pseudostratified columnar epithelium and produce toxins, some of which appear to be similar to those from other Bordetella spp. Toxins associated with pathogenic strains of B avium include a heat-labile toxin, tracheal cytotoxin, dermonecrotic toxin, and osteotoxin. Adherence factors associated with the bacterium include the hemagglutinin Baa1 autotransporter protein and possibly pili and components associated with lipopolysaccharide. Damage to the tracheal cartilage with distortion and discoloration of the tracheal rings is often observed and thought to be caused by the cytotoxin and/or the osteotoxin. Some mortality is due to suffocation from increased mucus production in the trachea and tracheal collapse. As with many bacterial infections, iron acquisition is necessary for colonization and spread of B avium in the host. Virulence factor expression is globally controlled by a virulence gene locus in response to environmental conditions that favor antigenic variation among B avium isolates.
Damage to the upper respiratory tract can lead to secondary infections with Escherichia coli or other agents, which can significantly increase the severity of the disease. In many cases, turkeys infected solely with B avium recover within 4–6 wk without serious consequences.
Epidemiology and Transmission
Morbidity is usually 80%–100% in young turkeys. Mortality can range from 0% in birds with uncomplicated disease to >40% if secondary invaders are present. Mortality can increase and signs can become severe if young turkeys infected with B avium also become infected with other agents (eg, E coli, Newcastle disease virus) or when environmental conditions in turkey barns are less than optimal. Bordetellosis is a major initiator of colibacillosis in turkeys. There is an age-related resistance to the disease. Turkeys >4–5 wk old are most often refractory to the disease but not infection, and thus can be a factor in spread of the bacterium.
B avium is highly contagious and easily transmitted from infected turkeys to susceptible birds by direct contact. It can also be transmitted through contaminated drinking water, feed, and litter, which can remain infectious for 1–6 mo.
Signs of the disease usually occur 7–10 days after infection and include sinusitis with a clear nasal discharge that can be observed when pressure is applied to the nares. Foamy-watery eyes, a snick or cough, mouth breathing, dyspnea, tracheal rales, and altered vocalization are also characteristic. Complicated disease can result in more exaggerated signs including airsacculitis.
Lesions are primarily found in the upper respiratory tract and consist of nasal and tracheal exudates, collapse of cartilaginous rings, and progressive loss of ciliated epithelium. In uncomplicated disease, the tracheal epithelium can return to normal 4–6 wk after the onset of signs.
At necropsy, turkeys with characteristic bordetellosis have watery eyes and extensive mucus in the sinuses and trachea, which rarely extends below the tracheal bifurcation. The lining of the trachea may have extremely mild hemorrhage in some cases, and softening of the tracheal rings is usually felt. In addition, a dorsal/ventral flattening of the trachea can sometimes be observed. Pneumonia and airsacculitis are observed only when the disease is complicated by another disease agent.
Diagnosis of infection is confirmed by isolation of B avium on MacConkey agar and identification using standard biochemical assays. Nonfermenting, small, slow-growing colonies from specimens from the anterior trachea are typical. The bacterium is best isolated from the anterior trachea; cultures taken from the sinuses frequently become overgrown with other, faster-replicating bacteria such as Proteus spp.
Serology is also important, and both microagglutination (detects IgM) and ELISA (detects IgG) tests are available. The microagglutination test can detect specific antibodies ~1 wk after infection. The ELISA test generally detects specific antibodies >2 wk after infection and has the added benefit of detecting maternal antibody. Monoclonal antibody-based agglutination and indirect immunofluorescent tests as well as PCR tests have also been used to identify B avium.
Other nonfermenters, B bronchiseptica and B hinzii, which are for the most part nonpathogenic, can sometimes be isolated from the trachea and must be differentiated from B avium. Pathogenic B avium can be differentiated by growth and colony morphology on MacConkey agar, no growth on minimal essential medium, a negative urease reaction, and hemagglutination of guinea pig erythrocytes. B avium also agglutinates chicken and turkey erythrocytes.
Treatment with antimicrobial agents by aerosol, injection, or in the water has not been effective, even though B avium may be highly sensitive. The tracheal epithelium of the turkey is a difficult location to medicate even though blood levels of the antimicrobial appear to be adequate. Resistance to streptomycin, sulfonamides, and tetracycline can be carried on plasmids and has been observed for some strains of B avium. Antimicrobial therapy may be helpful for secondary colibacillosis.
Control and Prevention
Vaccination with bacterins and a live temperature-sensitive mutant vaccine have given mixed results depending on the age of the turkey and the method of administration. Typically, turkeys >3 wk old respond positively to vaccination with the live temperature-sensitive vaccine. Vaccination is not widely practiced by turkey breeders, and the immunity that is passed to progeny generally comes from natural infections.
B avium is easily carried between farms. Thus, prevention should include a good biosecurity program. Rigorous cleanup and disinfection after field outbreaks is essential. Most of the commonly used disinfectants are effective.
B avium may be a rare opportunistic pathogen in people. In addition, a closely related organism, B hinzii, also isolated from poultry, has been associated with septicemia and bacteremia in older or immunocompromised people.
Last full review/revision June 2013 by Mark W. Jackwood, PhD