Avian bordetellosis is a highly infectious, acute disease of the upper respiratory tract of young turkeys. Clinical signs include sneezing (snick), watery or foamy eyes, clear nasal discharge when gentle pressure is applied to the nares, mouth breathing, dyspnea, tracheal rales, and altered vocalization. Diagnosis is based on clinical signs, lesions, and isolation of Bordetella avium or Bordetella hinzii from the respiratory tract. Antimicrobial treatment is rarely effective. Sound husbandry practices can lessen the impact of an outbreak.
Avian bordetellosis is a highly infectious, acute upper respiratory tract disease of turkeys characterized by high morbidity rates and usually low mortality rates.
Although bordetellosis affects primarily turkeys, it has also been observed in quail and ostrich chicks. In cockatiels, Bordetella avium is known to cause temporomandibular rigidity (lockjaw syndrome). B avium is an opportunistic pathogen in chickens.
Damage to the upper respiratory tract resulting from prior exposure to other respiratory pathogens or to related, live vaccine strains, such as infectious bronchitis virus or Newcastle disease virus, or from an environmental irritant such as ammonia, is necessary to induce signs of bordetellosis in chickens.
Etiology and Pathogenesis of Bordetellosis in Poultry
The major etiological agent of bordetellosis is Bordetella avium.
B avium was once the only known etiological agent. A 2009 report described Bordetella hinzii as a cause of clinical signs of bordetellosis in experimentally infected turkey poults (1). Since that time, B hinzii has also been identified from turkeys diagnosed with the disease. Reanalysis of bacterial isolates from historical cases of bordetellosis suggests that some B hinzii infections may have been mistakenly ascribed to B avium or to other closely related bacteria for a considerable length of time.
The mechanism of pathogenesis for B avium and B hinzii depends on their ability to proficiently attach to the cilia of pseudostratified columnar epithelium. From this location, toxins and other effectors produced by the bacteria are optimally positioned to damage the underlying tracheal cartilage.
Bacteria initially adhere to ciliated epithelial cells of the nasal mucosa, subsequently progressing to the trachea and primary bronchi (see tracheal images of B avium 3 days and 7 days after infection).
Courtesy of Dr. Mark W. Jackwood.
Courtesy of Dr. Mark W. Jackwood.
Potential attachment factors of B avium, which can collectively participate in adherence, include pili, a hemagglutinin, the protein autotransporter Baa1, and components associated with lipopolysaccharide. Attachment factors of B hinzii remain unidentified; however, genome sequence comparisons and other data suggest that at least some might be unique from factors used by B avium.
Damage to the tracheal cartilage by B avium is likely due to the actions of an osteotoxin and a tracheal cytotoxin. It is not currently known whether B hinzii also produces these toxins or whether tracheal damage is mediated by other bacterial products.
A dermonecrotic toxin produced by B avium might further contribute to virulence; however, its specific role is unclear. B hinzii is not known to produce the toxin, and no corresponding gene has been identified in any of the 13 isolates for which genome sequences are publicly available.
As with many other bacterial pathogens, B avium must acquire iron for colonization and spread in the host. Mechanisms for iron uptake identified in B avium include heme receptors, siderophore receptors, and a transferrin-binding protein. Genome sequence annotations for B hinzii identify several genes potentially involved in iron acquisition; however, whether they are expressed and how they function have not been investigated.
In several other Bordetella spp, the timing and extent of expression of most virulence factors are controlled by proteins encoded by the bvg (Bordetella virulence genes) locus. This process, known as phenotypic modulation, leads to reversible upregulation or downregulation of virulence gene expression in response to local environmental conditions.
A bvg locus has been identified in B avium and is required for virulence. B hinzii also has a recognizable bvg locus; however, little is known about its possible role in virulence. Information currently available suggests that the precise manner in which virulence genes are regulated in both B avium and B hinzii may be unique, compared with other Bordetella spp in which phenotypic modulation has been more intensively studied.
Damage to the upper respiratory tract from bordetellosis can lead to secondary infections with Escherichia coli or other agents, which can substantially increase severity of the disease. Many turkeys infected solely with B avium recover within 4–6 weeks without serious consequences.
Epidemiology and Transmission of Bordetellosis in Poultry
B avium has been isolated from healthy individuals of many other wild and domesticated avian species besides turkeys, including ducks, geese, owls, partridges, parrot finches, and others. However, currently no evidence suggests that it causes disease in these hosts.
Bordetellosis has been identified in almost every part of the world where turkeys are intensively reared. Although the disease appears rare or inapparent in some locations, severe outbreaks occur in other geographical regions. The reasons for these epidemiological differences are not known.
The morbidity rate in young turkeys with bordetellosis is usually 80–100%. The mortality rate ranges from 0% in birds with uncomplicated disease to > 40% when secondary invaders such as E coli or Newcastle disease virus are present. When environmental conditions in turkey barns are less than optimal or when disease is complicated by secondary agents, the mortality rate often increases and clinical signs are more severe.
Turkeys appear to become relatively resistant to bordetellosis after 5–6 weeks of age, but disease in breeders and older flocks has occasionally been reported. Nonetheless, mature birds exposed to B avium can become clinically inapparent carriers capable of transmitting bordetellosis to susceptible turkeys. Prior infection with B avium can predispose turkeys to colibacillosis and increase the severity of related airsacculitis.
B avium is highly contagious and easily transmitted from infected turkeys to susceptible birds by direct contact. It can also be spread through contaminated drinking water, feed, and litter, which can remain infectious for up to 6 months. Other domesticated and wild birds from which B avium has been isolated should be considered possible reservoirs of infection.
No studies have yet directly addressed the transmission of B hinzii; however, given its close relationship to B avium, it seems likely that these two species have similar patterns of transmission.
Clinical Findings of Bordetellosis in Poultry
Clinical signs of bordetellosis 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. Older turkeys can develop a dry cough.
During the first 2 weeks of bordetellosis, the nares and feathers of the head and wings often appear crusted with wet, sticky exudate. By 1 week after disease onset, tracheal softening can sometimes be palpated through the skin of the neck. Copious production of tracheal mucus, as well as tracheal collapse, can result in death due to suffocation. Complicated disease often triggers more exaggerated signs, including airsacculitis.
Diseases that can cause similar signs and can resemble bordetellosis include Alcaligenes rhinotracheitis, adenovirus-associated respiratory disease, acute respiratory disease syndrome, and turkey rhinotracheitis.
Lesions
Lesions of bordetellosis are found primarily 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 weeks after the onset of clinical signs.
At necropsy, turkeys with characteristic bordetellosis have watery eyes and extensive mucus in the sinuses and trachea; rarely, the mucus extends below the tracheal bifurcation. Mild hemorrhage of the tracheal lining is apparent in some cases, and softening of the tracheal rings is usually evident, sometimes accompanied by dorsoventral flattening of the trachea (see flattened trachea image).
Courtesy of Dr. Jean Sander.
Pneumonia and airsacculitis can occur with bordetellosis only when the disease is complicated by another disease agent.
Diagnosis of Bordetellosis in Poultry
Clinical signs and lesions
Isolation of B avium or B hinzii
Serological testing
Diagnosis of bordetellosis is based on clinical signs and lesions, and on the isolation of B avium or B hinzii. The bacteria are best isolated from the anterior trachea, because cultures of samples taken from the sinuses are frequently overgrown with other, faster-replicating bacteria, such as Proteus spp.
Pearls & Pitfalls
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Both B avium and B hinzii are gram-negative, nonfermentative, motile, aerobic bacilli that grow on a variety of media, including MacConkey agar, Bordet-Gengou agar, blood agar, veal infusion broth, trypticase soy broth, and brain-heart infusion broth (see colony morphology image). B hinzii, but not B avium, grows on minimal essential medium.
Courtesy of Dr. Mark W. Jackwood.
When B avium is grown in broth media high in nutrients, filamentous forms can arise. MacConkey agar is recommended for primary culture because it differentiates nonfermentative Bordetella from fermentative opportunists, including E coli.
After incubation at 37°C for 24–36 hours, B avium typically produces translucent, glistening, pearl-like colonies with smooth edges, approximately 0.2–1 mm in diameter (see smooth colony image).
Courtesy of Dr. Mark W. Jackwood.
After serial passage in the laboratory, a rough colony type with a dry appearance and serrated, irregular edges can be observed for some isolates (see rough colony image). Such colonies, which are nonpathogenic, are the visible manifestation of phase variation, a process in which spontaneous mutations in the bvg locus irreversibly abolish the production of virulence factors.
Courtesy of Dr. Mark W. Jackwood.
Colonies of B hinzii are typically described as round, convex, glistening, and grayish and are generally larger (up to 2 mm in diameter) than those formed by B avium.
Standard biochemical tests can distinguish B avium and B hinzii from other nonfermentative bacteria; however, discriminating between the two species in this way is challenging (see the table Properties of Bordetella avium and Bordetella hinzii).
Properties of Bordetella avium and Bordetella hinzii
Test | Bordetella avium | Bordetella hinzii |
|---|---|---|
Oxidase | Positive | Positive |
Catalase | Positive | Positive |
Urease | Negative | Variablea |
Nitrate reduced to nitrite | Negative | Negative |
Triple sugar iron agar | Alkaline slant, no change in butt | Alkaline slant, alkaline butt |
Alkali production from malonamide | Negative | Positive |
Alkali production from malonate | Negative | Positive |
Alkali production from valerate | Negative | Positive |
Hemagglutination of guinea pig erythrocytes | Positive | Negative |
aMost B hinzii isolates test negative for urease, but some may test positive, depending on the method used. | ||
Although isolation of either B avium or B hinzii from birds with appropriate clinical signs is sufficient for diagnosis of bordetellosis, identification to the species level is desirable because it provides information about species-specific prevalence.
Highly sensitive and specific PCR assays for B avium (targeting a putative membrane protein gene, as annotated in the genome sequence of reference isolate 197N) and B hinzii (targeting the ompA gene) have been reported that can establish the status of suspect colonies; however, neither assay is recommended for direct testing of clinical samples.
A novel Bordetella sp first recognized in 2016—Bordetella pseudohinzii—can produce a positive result with the B hinziiompA PCR assay. Because the host range of B pseudohinzii appears to be restricted to mice, it seems unlikely that false-positive results would arise from poultry isolates.
Hemagglutination of guinea pig erythrocytes can also differentiate between B avium and B hinzii. A monoclonal antibody produced from mice immunized with B avium has been used to develop both a latex bead–based agglutination test and an indirect immunofluorescence test; however, whether the monoclonal antibody also reacts with B hinzii is unknown.
Serological testing can also help to establish a diagnosis of bordetellosis caused by B avium. A microagglutination test has been developed that detects B avium–specific IgM approximately 1 week after infection. An ELISA that detects IgG > 2 weeks after infection is also available and has the additional benefit of detecting maternal-derived antibodies. No data are available to indicate whether either of these methods produces positive results for birds infected with B hinzii.
Currently, no serological test is suitable for identification of birds infected with B hinzii.
Treatment of Bordetellosis in Poultry
Antimicrobials
Although antimicrobial treatment can be helpful for secondary colibacillosis, administration of antimicrobial agents via aerosol, injection, or drinking water has not been effective for the control of B avium, even when in vitro testing indicates that isolates are highly susceptible. This inefficacy likely reflects the difficulty of achieving therapeutic concentrations at the site of bacterial colonization (the tracheal epithelium), even when blood concentrations are deemed adequate.
For B avium, resistance to ampicillin, aztreonam, erythromycin, streptomycin, ceftiofur, lincomycin, sulfonamides, and tetracycline has been reported. Resistance profiles appear to vary by region, perhaps because of local or regional antimicrobial use. In a few instances, plasmid-mediated transfer of resistance between isolates has been demonstrated.
No information is available regarding the efficacy of antimicrobial treatment when bordetellosis is due to B hinzii. Human isolates are often resistant to many antimicrobials, including beta-lactams, quinolones, macrolides, and cephalosporins. Resistance to aztreonam has been reported for poultry isolates.
The addition of niacin (70 mg/L) to drinking water has been reported to lessen the severity of bordetellosis clinical signs.
Local guidelines must be followed for appropriate withdrawal times and residue avoidance in all food-producing animals.
Control and Prevention of Bordetellosis in Poultry
Vaccines against B avium that are composed of bacterins or modified live mutants generally provide limited efficacy. Results for a given vaccine depend on the following factors:
dosage
age of the bird
method of administration
environment
Vaccines can lessen the severity of bordetellosis; however, none are known to prevent infection. Vaccination is not widely practiced by turkey breeders, and the immunity passed to progeny generally comes from naturally occurring infections.
No B hinzii–derived vaccines have yet been developed. B hinzii and B avium are antigenically related; however, whether B avium vaccines affect the course of disease after infection with B hinzii has not been examined.
B avium is easily spread between farms, and the same might be true for B hinzii. Thus, prevention should include a good biosecurity program.
Rigorous cleanup and disinfection after field outbreaks of bordetellosis is essential. Most of the commonly used disinfectants are effective against B avium when applied as directed. No studies address the susceptibility of B hinzii to chemical disinfectants.
Maintaining optimal air quality and temperature, minimizing environmental stressors, and practicing sound husbandry lessen the severity of bordetellosis outbreaks.
Zoonotic Risk of Bordetellosis in Poultry
Both B avium and B hinzii are opportunistic pathogens in humans. Infections are rare and occur primarily in immunocompromised individuals. B hinzii infection is more common than B avium infection.
B avium has been isolated only from cases of respiratory disease. B hinzii has been reported as a cause of respiratory disease, endocarditis, septicemia, and GI tract infections.
Transmission to humans from an avian source through occupational exposure has rarely been reported.
Key Points
Avian bordetellosis is a highly infectious, acute upper respiratory tract disease of turkeys caused by either Bordetella avium or Bordetella hinzii.
It is characterized by high morbidity rates and low mortality rates; however, secondary infections can markedly increase severity of the disease.
Antimicrobial treatment during outbreaks is rarely effective. Maintaining high air quality, eliminating environmental stressors, and practicing sound husbandry decrease the impact of an outbreak.
Vaccines currently available can decrease the severity of disease but do not prevent infection. Rigorous biosecurity measures are required to prevent infection of clean flocks.
For More Information
Jacob J. Bordetellosis in Poultry. Small and Backyard Poultry, US Cooperative Extension System (eXtension); date unknown.
Ficken M. Bordetellosis (Turkey Coryza) in Turkeys. Texas A&M Veterinary Medical Diagnostic Laboratory (TVMDL); August 12, 2024.
References
Register KB, Kunkle RA. Strain-specific virulence of Bordetella hinzii in poultry. Avian Dis. 2009;53(1):50-54. doi:10.1637/8388-070108-Reg.1
